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Enrico Marani

Wijnand F.R.M. Koch

The Pelvis
Structure, Gender and Society
The Pelvis

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Enrico Marani Wijnand F.R.M. Koch

The Pelvis
Structure, Gender and Society

123
sergiocamargo47@gmail.com
Enrico Marani Wijnand F.R.M. Koch
Department of Biomedical Signals Medisch Centrum Alkmaar Polikliniek
and Systems, MIRA Urologie
University of Twente Alkmaar
Enschede The Netherlands
The Netherlands

ISBN 978-3-642-40005-6 ISBN 978-3-642-40006-3 (eBook)


DOI 10.1007/978-3-642-40006-3
Springer Heidelberg New York Dordrecht London

Library of Congress Control Number: 2013950373

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Contents

1 ‘‘Construction Plan’’ of the Bony Pelvis. . . . . . . . . . . . . . . . . . . . 1


1.1 The Bony Pelvis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1
1.1.1 Gender Differences . . . . . . . . . . . . . . . . . . . . . . . . 6
1.1.2 Posture . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8
Literature . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 15

2 The Pelvis at War . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 17


2.1 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 17
2.1.1 Neanderthals . . . . . . . . . . . . . . . . . . . . . . . . . . . . 18
2.1.2 Pazyryk Mongolian War Skeletons . . . . . . . . . . . . . 18
2.1.3 Trojan Siege . . . . . . . . . . . . . . . . . . . . . . . . . . . . 19
2.1.4 Modern Weapons . . . . . . . . . . . . . . . . . . . . . . . . . 20
2.1.5 Pelvic Stability and Pelvic Fractures . . . . . . . . . . . . 22
2.1.6 Sarajevo . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 24
Literature . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 27

3 The Birth Canal . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 29


3.1 Evolution . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 29
3.2 The Human Birth Canal . . . . . . . . . . . . . . . . . . . . . . . . . . 35
3.2.1 Abortion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 35
3.2.2 Birth Passage Way . . . . . . . . . . . . . . . . . . . . . . . . 35
3.2.3 Position of the Fetus During Delivery . . . . . . . . . . . 37
3.3 The Uterus During Pregnancy . . . . . . . . . . . . . . . . . . . . . . 38
3.4 Pelvic Blood Vessels. . . . . . . . . . . . . . . . . . . . . . . . . . . . . 43
Literature . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 45

4 History. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 47
4.1 Historical Panorama I . . . . . . . . . . . . . . . . . . . . . . . . . . . . 47
4.2 Bladder Stones . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 48
4.2.1 The Perineum. . . . . . . . . . . . . . . . . . . . . . . . . . . . 49
4.2.2 The Method of Celsus . . . . . . . . . . . . . . . . . . . . . . 49
4.2.3 The Method of Marianus . . . . . . . . . . . . . . . . . . . . 50
4.2.4 Lateral Lithotomy . . . . . . . . . . . . . . . . . . . . . . . . . 50

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4.3 Vesalius (1514–1564) . . . . . . . . . . . . . . . . . . . . . . . . . . .. 51


4.4 Historical Panorama II. . . . . . . . . . . . . . . . . . . . . . . . . . .. 52
4.5 Hendrik van Deventer (1651–1724): Father
of Pelvic Science . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 55
4.5.1 Van Deventer and His Time. . . . . . . . . . . . . . . . . . 55
4.5.2 Van Deventers Life. . . . . . . . . . . . . . . . . . . . . . . . 56
4.5.3 Van Deventer’s Thesis . . . . . . . . . . . . . . . . . . . . . 57
4.5.4 Van Deventer and the Bony Pelvis . . . . . . . . . . . . . 58
4.5.5 Dissemination Through Europe. . . . . . . . . . . . . . . . 62
4.5.6 The Pelvis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 63
4.5.7 The Coccyx . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 63
4.5.8 Deflections of the Pelvis . . . . . . . . . . . . . . . . . . . . 63
4.6 The Pelvis According to Govard Bidloo (1649–1713) . . . . . . 64
4.6.1 The Life of Govard Bidloo
and Gérard de Laresse. . . . . . . . . . . . . . . . . . . . . . 64
4.6.2 Cowper’s Plagiarism . . . . . . . . . . . . . . . . . . . . . . . 65
4.6.3 Anatomia Humani Corporis . . . . . . . . . . . . . . . . . . 66
4.6.4 Bidloo’s Description of the Pelvis. . . . . . . . . . . . . . 66
4.6.5 Conclusion. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 68
4.7 The Sacrum Bifidum . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 68
4.8 In Summary . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 72
4.9 Historical Panorama III: The Study of Pelvic Soft Tissues. . . 72
4.10 A Medieval Contagious Disease: Syphilis . . . . . . . . . . . . . . 74
4.11 Medieval Dissections. . . . . . . . . . . . . . . . . . . . . . . . . . . . . 75
4.12 Renaissance . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 87
4.13 The Route to Vesalius . . . . . . . . . . . . . . . . . . . . . . . . . . . . 88
4.14 Charles Estienne’s De dissectione (1545). . . . . . . . . . . . . . . 89
4.15 The University of Padua and the Rise of Anatomy . . . . . . . . 96
4.16 Contribution of Surgery to Anatomy . . . . . . . . . . . . . . . . . . 101
4.17 Contribution of the Seventeenth-Century Scholars . . . . . . . . 104
4.18 Conclusion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 105
Literature . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 106

5 Concepts and Approaches in the Study of the Pelvis . . . . . . . . . . 111


5.1 Introduction . . . . . . . . . . . . . . . . . . . . ..... . . . . . . . . . . 111
5.2 Symmetry of the Pelvis . . . . . . . . . . . . ..... . . . . . . . . . . 112
5.3 Comparative Anatomy of the Pelvis . . . ..... . . . . . . . . . . 115
5.4 Ontogeny of the Pelvis . . . . . . . . . . . . ..... . . . . . . . . . . 116
5.5 Mechanical Approach to the Pelvis . . . . ..... . . . . . . . . . . 118
5.6 Sirene: A Seducing Pelvic Sound? . . . . ..... . . . . . . . . . . 120
5.6.1 Holism and the Deviant . . . . . . ..... . . . . . . . . . . 123

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5.7 Biomechanics . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . ... 125


5.7.1 Girdles: Bony Arches for the Support of Limbs . ... 126
5.7.2 The Closed Kinematic Chain . . . . . . . . . . . . . . ... 129
5.7.3 Finite Element Modeling
and Pelvic Forces . . . . . . . . . . . . . . . . . . . . . . ... 130
5.7.4 Finite Element Modeling
and the Pelvic Diaphragm . . . . . . . . . . . . . . . . ... 133
5.7.5 Finite Element Modeling
and Pelvic Organ Movement . . . . . . . . . . . . . . ... 134
5.8 The Pelvic Sacroiliac Joint and Low Back Pain . . . . . . . ... 136
Literature . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . ... 138

6 Sexual Organs and Society . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 143


6.1 Anxieties: Koro and Spermatorrhoea . . . . . . . . . . . . . . . . . . 143
6.2 Circumcision, Castration and Mutilation . . . . . . . . . . . . . . . 149
6.3 The Prepuce . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 153
6.4 G-spot: Clitoral and Vaginal Orgasm . . . . . . . . . . . . . . . . . 157
6.5 Eunuchs: Castration of Man . . . . . . . . . . . . . . . . . . . . . . . . 161
6.6 Phantoms of the External Genitalia . . . . . . . . . . . . . . . . . . . 165
6.7 Plastic Surgery of Sexual Organs . . . . . . . . . . . . . . . . . . . . 169
Literature . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 170

7 Anatomy of the Pelvic Wall . . . . . . . . . . . . . . . . . . . . . . . . . . . . 177


7.1 The Mature Pelvic Wall Muscles and Ligaments . . . . . . . . . 177
7.1.1 The Foramina of the Pelvis . . . . . . . . . . . . . . . . . . 177
7.1.2 The Urogenital Diaphragm. . . . . . . . . . . . . . . . . . . 179
7.1.3 The Levator Ani Muscle . . . . . . . . . . . . . . . . . . . . 180
7.1.4 The Corpus Intrapelvinum . . . . . . . . . . . . . . . . . . . 183
7.1.5 Again the Urogenital Diaphragm . . . . . . . . . . . . . . 183
7.1.6 Notions on Ligaments . . . . . . . . . . . . . . . . . . . . . . 184
7.1.7 Suspension Operations. . . . . . . . . . . . . . . . . . . . . . 186
7.1.8 More on Ligaments and Surgery in Stress
Incontinence. . . . . . . . . . . . . . . . . . . . . . ....... 187
7.1.9 Abdominal Operations. . . . . . . . . . . . . . . ....... 187
7.1.10 Vaginal Operations . . . . . . . . . . . . . . . . . ....... 188
7.2 The Relation of the Pelvic Wall Muscles
and the Sphincters. . . . . . . . . . . . . . . . . . . . . . . . ....... 189
7.3 Scarpa’s, Buck’s and Colles Fascias . . . . . . . . . . . ....... 193
Literature . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . ....... 197

8 Development of the Pelvic Diaphragm and More . . . . . . . . . . . . . 201


8.1 The Two Layers in the Pelvic Diaphragm . . . . . . . . . . . . . . 201
8.2 Early Embryology: Overview . . . . . . . . . . . . . . . . . . . . . . . 204
8.3 Development of the Human Pelvic Diaphragm . . . . . . . . . . . 206

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8.4 Detailed Description of the Development


of the Pelvic Diaphragm . . . . . . . . . . . . . . . . . . . . . . . . . . 208
8.5 Gender of the Pelvic Diaphragm. . . . . . . . . . . . . . . . . . . . . 210
8.6 Development of the Uropoetic System . . . . . . . . . . . . . . . . 211
8.6.1 Paired or Unpaired That is the Question!. . . . . . . . . 212
8.7 The Development of the Pelvic Sphincters. . . . . . . . . . . . . . 213
8.8 Surgery of Anorectal Malformations . . . . . . . . . . . . . . . . . . 215
8.9 The Development of the External Urethral Sphincter . . . . . . 220
8.10 Earliest Characteristics of Human Pelvic Development . . . . . 222
8.11 The Development of Higher Bladder Steering Centers . . . . . 223
Literature . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 226

9 Physiotherapy for Pelvic Muscles . . . . . . . . . . . . . . . . . . . . . . . . 229


9.1 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 229
9.2 Physiotherapy for Pelvic Floor Dysfunctions . . . . . . . . . . . . 231
9.2.1 Toilet Behavior . . . . . . . . . . . . . . . . . . . . . . . . . . 231
9.3 The Wise-Anderson Method. . . . . . . . . . . . . . . . . . . . . . . . 236
9.3.1 Anatomy Related to the Wise-Anderson Therapy . . . 237
9.3.2 Physiology Related to the Wise-Anderson
Therapy . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 237
9.3.3 Quality of the Published Results
on Trigger Points . . . . . . . . . . . . . . . . . . . . . . . .. 238
9.3.4 Trigger-Point Therapy . . . . . . . . . . . . . . . . . . . . .. 238
9.3.5 Quality of the Published Results
of the Wise-Anderson Method . . . . . . . . . . . . . . .. 239
9.4 Anatomy of Pelvic Floor Training . . . . . . . . . . . . . . . . . .. 241
Literature . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 242

10 The Subperitoneal and Lower Retroperitoneal Space. . . . ...... 245


10.1 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . ...... 245
10.2 Carcinoma’s in the Retro and Subperitoneal Space . . ...... 248
10.2.1 Detection of Pelvic Lymph Node Cancer
by Computed Tomography and Magnetic
Resonance Imaging . . . . . . . . . . . . . . . . . . ...... 249
10.2.2 Detection of Pelvic Lymph Node Cancer
by Size and/or Volume . . . . . . . . . . . . . . . ...... 253
10.2.3 The Development of the Lymphatic System
and Milroy’s Lymphoedema. . . . . . . . . . . . ...... 256
10.3 Lumbar Sympathectomy in the Sub-
and Retroperitoneal Areas . . . . . . . . . . . . . . . . . . . ...... 259
10.4 Testicular Descent . . . . . . . . . . . . . . . . . . . . . . . . ...... 264

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10.5 The Subperitoneal Blood Vessels and Ligaments


in the Female . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .... 270
10.5.1 Blood Vessels and Peritoneal Fluid. . . . . . . . . .... 271
10.5.2 Anastomoses: William Turner’s Subperitoneal
Arterial Plexus . . . . . . . . . . . . . . . . . . . . . . . .... 276
Literature . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .... 278

11 Vision and Waist-to-Hip Ratio . . . . . . . . . . . . .............. 283


11.1 Introduction . . . . . . . . . . . . . . . . . . . . . .............. 283
11.2 The Hidden Role of the Pelvis in Sexual
Arousal and Mating . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 284
11.3 Visual Sexual Information . . . . . . . . . . . . . . . . . . . . . . . . . 285
11.4 The Face and Sex . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 287
11.5 The Enlargement of Pupils. . . . . . . . . . . . . . . . . . . . . . . . . 288
11.6 Waist-to-Hip Ratio . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 290
11.7 Beautiful Buttocks and Vision . . . . . . . . . . . . . . . . . . . . . . 291
11.8 The Gluteus Muscle Group . . . . . . . . . . . . . . . . . . . . . . . . 295
11.9 Gait, the Pelvis and Vision . . . . . . . . . . . . . . . . . . . . . . . . 297
11.10 Spanking . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 300
Literature . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 302

12 Male and Female Bladder. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 305


12.1 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 305
12.2 The Dome of the Bladder; the Detrusor Muscle . . . . . . . . . . 307
12.3 Demonstrating the Detrusor Forces . . . . . . . . . . . . . . . . . . . 307
12.4 The Bladder-Neck or Trigone. . . . . . . . . . . . . . . . . . . . . . . 308
12.5 Detrusor Instability . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 309
Literature . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 311

13 The Pelvis and Herbal Medicine . . . . . . . . . . . . . . . . . . . . . . . . . 313


13.1 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 313
13.2 History . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 315
13.2.1 Herbal Medicine and Slavery in Suriname . . . . . . . . 320
13.3 Herbal Medicine and Pelvic Problems . . . . . . . . . . . . . . . . . 322
13.3.1 Herbal Medicine for Female Pelvic Problems. . . . . . 322
13.3.2 The Black Cohosh Studies . . . . . . . . . . . . . . . . . . . 324
13.3.3 Herbal Medicine for Male Pelvic Problems . . . . . . . 326
13.3.4 Prostatitis and Saw Palmetto . . . . . . . . . . . . . . . . . 326
13.3.5 Phytotherapy and Placebo . . . . . . . . . . . . . . . . . . . 328
13.3.6 Saw Palmetto Again . . . . . . . . . . . . . . . . . . . . . . . 330
13.3.7 Systems Biology. . . . . . . . . . . . . . . . . . . . . . . . . . 333
Literature . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 334

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14 Innervation of the Mature Human Pelvis . . . . . . . . . . . . . . . . . . 337


14.1 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 337
14.2 The Sacral Somatic Plexus. . . . . . . . . . . . . . . . . . . . . . . . . 338
14.2.1 Basic Arrangement . . . . . . . . . . . . . . . . . . . . . . . . 338
14.2.2 Sciatic Nerve . . . . . . . . . . . . . . . . . . . . . . . . . . . . 339
14.2.3 Pudendal Nerve . . . . . . . . . . . . . . . . . . . . . . . . . . 339
14.2.4 Alcock’s Canal . . . . . . . . . . . . . . . . . . . . . . . . . . . 339
14.3 Pelvic Plexus . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 341
14.4 Interconnecting Branches . . . . . . . . . . . . . . . . . . . . . . . . . . 342
14.4.1 Older Literature . . . . . . . . . . . . . . . . . . . . . . . . . . 343
14.5 The Autonomic Pelvic Plexus . . . . . . . . . . . . . . . . . . . . . . 344
14.5.1 Basic Arrangement . . . . . . . . . . . . . . . . . . . . . . . . 344
14.5.2 The Sympathic Trunk and Parasympathic
Innervation. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 344
14.5.3 The Hypogastric Nerves . . . . . . . . . . . . . . . . . . . . 345
14.5.4 The Pelvic Plexus . . . . . . . . . . . . . . . . . . . . . . . . . 345
14.6 What About the Pudendal Nerve? . . . . . . . . . . . . . . . . . . . . 347
14.7 Neuromodulation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 348
14.7.1 SANS . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 348
14.7.2 EPFS. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 349
14.7.3 Sacral Nerve Stimulation . . . . . . . . . . . . . . . . . . . . 349
14.8 Alternatives for Dorsal Rhizotomy . . . . . . . . . . . . . . . . . . . 350
14.8.1 The Cryotechnique . . . . . . . . . . . . . . . . . . . . . . . . 350
14.8.2 The Selective Stimulation Electrode . . . . . . . . . . . . 351
14.9 Central Connections . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 352
14.9.1 Micturition Control . . . . . . . . . . . . . . . . . . . . . . . . 352
Literature . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 356

15 Smooth Muscle Electromyography of Bladder and Uterus . . . . . . 361


15.1 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 361
15.2 History . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 362
15.3 Recording the Bladder EMG . . . . . . . . . . . . . . . . . . . . . . . 364
15.4 Single Smooth Muscle Cell Studies in the Pig Bladder . . . . . 366
15.5 Centers of Bladder EMG Activity. . . . . . . . . . . . . . . . . . . . 368
15.6 Again Fluorescent Spheres . . . . . . . . . . . . . . . . . . . . . . . . . 369
15.7 Uterine Electrical Activity . . . . . . . . . . . . . . . . . . . . . . . . . 371
Literature . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 375

16 Reflexes or Controller Action? . . . . . . . . ........ . . . . . . . . . . 377


16.1 Introduction . . . . . . . . . . . . . . . . . ........ . . . . . . . . . . 377
16.2 Noise. . . . . . . . . . . . . . . . . . . . . . ........ . . . . . . . . . . 379
16.3 The Reflex. . . . . . . . . . . . . . . . . . ........ . . . . . . . . . . 381
16.4 Short Neuron Reflex System . . . . . ........ . . . . . . . . . . 382
16.5 Reflex or Controller Mechanisms in the Pelvis. . . . . . . . . . . 383

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Contents xi

16.6 Flow Charts and Continence . . . . . . . . . . . . . . . . . . . . . . . 385


16.7 The Pelvic Autonomic Ganglia. . . . . . . . . . . . . . . . . . . . . . 388
16.7.1 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 388
16.7.2 Microganglia . . . . . . . . . . . . . . . . . . . . . . . . . . . . 389
16.7.3 The Dorsal Root Ganglia and Autonomic
Sensory Information . . . . . . . . . . . . . . . . . . . . . . . 390
16.7.4 Visceral Organ Cross-Sensitization . . . . . . . . . . . . . 394
16.7.5 Short Neuron System in the Repeat . . . . . . . . . . . . 396
16.7.6 Local Tissue Interactions: Urothelium Signaling. . . . 398
Literature . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 401

17 The Connective Tissue in the Pelvis . . . . . . . . . . . . . . . . . . . . . . 407


17.1 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 407
17.2 The Corpus Pelvinus . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 408
17.3 Connective Tissue Reinforcements in Fascias. . . . . . . . . . . . 412
17.4 Connective Tissue Pillars for Blood Vessels . . . . . . . . . . . . 413
17.5 The Rectosacral Fascia . . . . . . . . . . . . . . . . . . . . . . . . . . . 414
17.6 The Perirectal Fasciae . . . . . . . . . . . . . . . . . . . . . . . . . . . . 416
17.7 Perianal Connective Tissue . . . . . . . . . . . . . . . . . . . . . . . . 417
17.8 Descensus of the Pelvic Diaphragm . . . . . . . . . . . . . . . . . . 418
17.9 Prolapse. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 420
17.10 Conclusion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 421
Literature . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 421

18 Sitting: A Pelvic Function? . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 423


18.1 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 423
18.2 The Shoemaker and Sir Arbuthnot Lane . . . . . . . . . . . . . . . 425
18.3 Rowing . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 427
18.4 Wheelchair Sitting . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 430
18.5 Sitting and Delivery . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 432
18.6 Lumbosacral Curve and Pelvic Rotation During Sitting . . . . . 441
18.7 Belly Dancing and Pelvic Movements . . . . . . . . . . . . . . . . . 444
Literature . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 445

19 Sphincters . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 449
19.1 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 449
19.2 Similarity of Sphincter Transformation . . . . . . . . . . . . . . . . 450
19.3 The External Anal Sphincter . . . . . . . . . . . . . . . . . . . . . . . 450
19.4 The External Urethral Sphincter: Three Situations . . . . . . . . 452
19.5 Modeling the Sphincters . . . . . . . . . . . . . . . . . . . . . . . . . . 453
19.6 Onuf’s Nucleus. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 454
19.7 Sphincter Problems . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 456
19.7.1 Internal Urethral Sphincter (Smooth Muscular
Sphincter or Lissosphincter) . . . . . . . . . . . . . ..... 456

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xii Contents

19.7.2 External Urethral Sphincter (Striated Muscular


Sphincter or Rhabdosphincter) . . . . . . . . . . . . . . . . 460
Literature . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 462

20 Catheters . . . . . . . . . . . . . . . . . . . . . . . . . ........... ...... 467


20.1 History of Catheters . . . . . . . . . . . . ........... ...... 467
20.2 Catheterization and its Consequences ........... ...... 469
20.3 The Effects of Party Drugs on Lower Urinary Tract
and Sexual Function . . . . . . . . . . . . ........... ...... 471
20.4 Cannabis and Reproduction . . . . . . . ........... ...... 476
Literature . . . . . . . . . . . . . . . . . . . . . . . . . ........... ...... 478

21 The Pelvis During Childhood and Puberty . . . . . . . . . . . . . . . . . 481


21.1 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 481
21.2 Pubertal Fat Accumulation . . . . . . . . . . . . . . . . . . . . . . . . . 484
21.3 The Bony Pelvis and Puberty . . . . . . . . . . . . . . . . . . . . . . . 486
21.3.1 Bony Pelvis and Adolescent Deliveries . . . . . . . . . . 487
21.3.2 Bone Mineral Content, Osteoporosis, and Sports . . . 488
21.4 Pelvic Visceral Organs . . . . . . . . . . . . . . . . . . . . . . . . . . . 489
21.4.1 Early Development of the Uterus
and its Consequences . . . . . . . . . . . . . . . . . . . ... 489
21.4.2 Development of the Uterus Around Puberty
and Leiomyomas . . . . . . . . . . . . . . . . . . . . . . . . . 493
21.5 The External Genitals . . . . . . . . . . . . . . . . . . . . . . . . . . . . 496
21.6 Testis and Ovary . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 499
21.6.1 Testis and Penis . . . . . . . . . . . . . . . . . . . . . . . . . . 499
21.6.2 Decrease in Age of Puberty and Increase
in Height . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 500
21.6.3 Leptin and the Testis. . . . . . . . . . . . . . . . . . . . . . . 502
21.6.4 The Ovary and Puberty . . . . . . . . . . . . . . . . . . . . . 504
21.6.5 The Polycystic Ovary: The Anovulatory Woman . . . 506
21.6.6 The Ovary and Acupuncture . . . . . . . . . . . . . . . . . 508
21.6.7 The Mono-Ovulating Human Female:
The Alternating Ovulation . . . . . . . . . . . . . . . . ... 509
Literature . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . ... 512

22 The Pelvis and Aging . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 517


22.1 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 517
22.2 History of Aging Research. . . . . . . . . . . . . . . . . . . . . . . . . 519
22.3 Pelvic Organs During Aging . . . . . . . . . . . . . . . . . . . . . . . 522
22.3.1 Reproductive Organs . . . . . . . . . . . . . . . . . . . . . . . 523
22.3.2 The Uropoetic System . . . . . . . . . . . . . . . . . . . . . . 524
22.4 Hip Problems in Elderly . . . . . . . . . . . . . . . . . . . . . . . . . . 525

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Contents xiii

22.5 Falls . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 530


22.6 Genetics . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 531
Literature . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 533

Epilogue . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 537

Acknowledgments . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 539

Index . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 543

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Introduction: The Pelvis or My Pelvis?

Jonathan Sawday has written a very fine book on the scientific and social implication
of the interior discovery of the human body: ‘‘The body emblazoned’’ [1].
Notions about the interior of the human body lasted for centuries before we
came to our present understanding of its form and function. History determines our
insight into the constituents and their interconnected functions in the human body.
This perspective still defines our clinical approach in diagnostics and therapy. For
the pelvis and its organs it is a sad story, with rather depressing results, in which
humans often have been the experimental ‘‘specimens’’ for inadequate therapies,
that often made their situation worse, with nearly no follow-up, except for the
clinician’s mantra: ‘‘You have to learn to live with it’’.
This Introduction starts with the distinction between the body and my body, so
clearly laid down by Jonathan Sawday, which also implies for patients that it is my
body that clinicians use as the body for their experimental playing-field.
‘‘Whatever process is at work, the sense of interiority is inescapably central to
the experience of the body within history. Yet, a feature of our sense of interiority
is that it can never be experienced other than second-hand. We may look into other
bodies, but very rarely are we allowed to pry into our own. We may become
familiar with the generalised topography of the body, via different media-
photographs, X-rays, illustration, anatomical demonstration, written description,
TV documentary—but all these ‘voyages within’ (as the surgeon Richard Selzer
has termed them) are journeys of exploration which encounter bodies other than
our own. They are passages into the body, but not my body’’ (p.7) [1].
Fifteen years ago I (EM) was suspected of having a tumour in my right arm,
just at the inside of my elbow. I was taken to our Leiden Academic Hospital to
have it removed but refused to have general anaesthesia. I was brought into the
operation room, filled with nurses that I was teaching at that time, some of them
still in my class, and was operated upon while conscious.
I discussed the muscles, veins and ligaments that the surgeon had to pass and
could look in my own elbow. Moreover, as an anatomist I could follow and check
the surgeon. Of course I learned to understand the body in the dissection room ánd
I was able to discuss the ‘‘parts of the machinery’’ of my body with the surgeon,
based on what I knew from the body.

xv

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xvi Introduction: The Pelvis or My Pelvis?

My wife (EM) underwent a laparoscopy under local anaesthesia. She studied


French and Italian, and since she has a good understanding of the human body—in
fact she is married to an anatomist and one absorbs some knowledge from one’s
husband—she clearly could follow the organs that passed on the TV-screen.
However, for her it stayed the body. She could not feel that it was her body she
saw passing. It is like looking at some body on television. The TV-screen
objectifies and distances, distorting the personal view.
Our curriculum on the Head and Neck needed upgrading. So we produced a
‘‘self-teaching’’ system, called Caput that can be used on an ordinary PC by the
students. A medical student together with one of our scientists developed the
system. It is based on MRI sections of the medical student’s head. His fear was that
something abnormal would be found, but that was not the case and he now
reconstructs his own ventricle system and goes forward and backwards through his
own head. The journalist who announced Caput in our local journal exclaimed at
the top of the article ‘‘Looking into your own head!’’ [2].
Clearly the body and my body merge into one, if one has enough knowledge of
human anatomy. It stays divided if one lacks this knowledge. This conclusion
holds surely for all the organs of the pelvis and the pelvis itself. Here an extra
disturbing factor is present, shame: One encounters an extra social antidote to let
the body melt to my body in the pelvis. To paraphrase President Clinton’s election
slogan: It is the economy, stupid!- It is the pelvic knowledge, stupid!-
The motive for this book is in this slogan. Most of us have missing links if it
concerns the pelvis. Things we want to know that we do not asked due to shame.
This book gives you these facts that are knowable and helpful in understanding the
pelvis.
The technique used to guide the reader through the book is the ‘‘mind map’’
technique: One central theme, but branching into different facts and into various
comprehensions. Later on in other chapters these spider diagram methods are
repeated using the already learned information. The same holds for the concept
maps used in this book for the notions symmetry, comparison and holism.
The book starts with chapters that bring your anatomical knowledge up to date
(Chaps. 1–3) and goes on with history (Chap. 4). Without history one cannot
understand the pelvic mistakes still encountered now a days. With the main
concepts as treated in Chap. 5, the reader is ready to be astonished what the pelvic
sciences have to say on: sexual organs and society, physiotherapy, how man
analyses females by their pelvis, the impact of herbal medicine, that sitting is a
pelvic function, studies on puberty and aging, and on drugs. This all richly
sprinkled with elucidating anatomy and explanatory physiology.

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Introduction: The Pelvis or My Pelvis? xvii

Literature

The literature has been grouped into reference lists of several chapters in those cases where
arguments are difficult to entangle or published over several articles or books. In cases of
citation the article or book involved is indicated by the reference number together with a
capital Arabic letter.
1. Sawday, J. (1995). The body emblazoned. Routledge, London-New York.
2. Caput onthult de geheimen van het hoofd. Cicero (1998) 9:4–7.

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Chapter 1
‘‘Construction Plan’’ of the Bony Pelvis

The bony pelvis is not a fixed structure. It adapts to phenotypic stresses and
underwent evolutionary changes due to bipedal walking. This firm structure is
involved in positioning the pelvic organs, conducts forces over its components and
demonstrates gender and racial differences.

1.1 The Bony Pelvis

A multitude of terms for positions and movements are needed to describe the
inherent dimensionality of the pelvis. To navigate through an unfamiliar city is
difficult, but it is even more difficult to find your way in a subway, with its upper
and lower levels. If to the directions left and right are added up and down, the
human mind finds it difficult to handle the information flow. To make these
relationships more clear, all kinds of visual aids have been developed, of which an
atlas is the best known. In this chapter, we will try to avoid most anatomical terms,
although some are inevitable. Moreover, we will address ourselves to the bony
pelvis with an imaginary anatomical approach.
The morphology and lives of the Rhinogradentia, [1] (also known in their
English translation as ‘‘The Snouters’’), was written in Germany by Prof. Harald
Stümpke (Prof. Blockhead). In a playful way, this book relates the taxonomy of a
non-existing mammalian family that uses their nose as legs. From elephant and
tapir, with their tactile noses, to the snouters with their strolling noses is only a
small evolutionary step. The young scientist Gerolf Steiner was appointed as
professor at once, after the publication of his ‘‘Morphology and life of the snou-
ters.’’ To the snouter family belongs one species in particular, that is most
intriguing for the study of the pelvis: Otopteryx volitans (see Fig. 1.1a). The
extreme development of the nasal bone, together with the severe reduction in the
legs, is of course the most striking phenomenon for those interested in the evo-
lutionary development of the snouters. Our concern, however, is the pubic
expansion (processus pubici, nr. 10 in Fig. 1.1b): ‘‘a direct link between the
breastbone (sternum) and the pubic bones.’’ Indeed, Gerolf Steiner had to know his
comparative anatomy very well to incorporate this connection in his figure.

E. Marani and W. F.R.M. Koch, The Pelvis, 1


DOI: 10.1007/978-3-642-40006-3_1,  Springer-Verlag Berlin Heidelberg 2014

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2 1 ‘‘Construction Plan’’ of the Bony Pelvis

Fig. 1.1 Otopteryx volitans in situ (a) and skeleton (b). Processus pubicus is indicated by
number 10 in (b). Published by Gustav Fischer Verlag with kind permission from Springer
Science ? Business Media

Fig. 1.2 Differences in


pelvic constituents of a
normal goat and one walking
on his hind legs. From Slijper
in [2]

Let us start with the changes that can occur to the pelvis during normal life.
A goat born without forelegs had to move on his hind legs. In such a creature, in
comparison with the bony pelvis of a normal goat, one notices an increase in all
bony parts of the pelvis, but especially the increase in the length of the ischium and
the symphysis pelvis [2] (Fig. 1.2).

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1.1 The Bony Pelvis 3

Fig. 1.3 a Lateral view, b Frontal view. Pelves of Pan, Australopithecus, and Man (Reproduced
with permission from Broom and Robinson 1950 [2]). Note the changes in the sacroiliac
articulation, acetabulum, and the length of the ischium

We now change our viewpoint to the evolution of man. If we compare the


pelvis of the chimpanzee (Pan), Australopithecus and Homo, we notice a decrease
in the rostrocaudal length of the bony pelvis, an increase in the width, and an
enlargement [3] of the pubic thickness (Fig. 1.3).
Seemingly, both individually and evolutionarily, the pelvis is not a fixed
structure, but one that can adapt to the different situations offered by mother’s
nature.
Now, we have established that the pelvis is a structure that conforms to phe-
notypic stress during an individual’s lifetime and during evolution, let us look
again at the snouters.
Normally, the pelvis is connected to the rostral, ventral bones of the thorax by a
ligament known as the linea alba. This ligament relates the ventral pelvic part
called the symphysis to the sternum. In certain lizards, that is earlier in phylogeny,
the linea alba is covered with bony plates: the parasternalia, producing a bony
connection between the pelvis and the sternum, that developed in the linea alba. In
the famous Dinosaur family, the Tyrannosaurus possesses so-called gastralia, bony
structures that protect the belly, forming a continuation from thorax to pelvis. So
the pelvis, as a bony structure, can indeed be connected or extended to the thorax.
Where did this aggressive, outgrowing bony structure start in evolution? Fish
do not have a pelvis. The pelvis as a closed ring connected to the vertebral column
starts in the quadrupeds. Quadrupeds always have a dorsal pelvic part that

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4 1 ‘‘Construction Plan’’ of the Bony Pelvis

connects to the vertebral column (pars iliaca) and a part that constitutes the ventral
base of the closed ring (pars puboischiadica). You always will find an acetabulum,
the joint socket for the femur. By the way, the name acetabulum contains the
Italian/Latin word aceto (vinegar) referring to the vinegar-filled bowl used for
dipping the food at Roman dining tables [4A]. There is always an opening between
the ossi ischii and pubi: Whether this foramen is called obturatum and/or
puboischiadicum requires profound comparative analysis.
In all tetrapods, one can discern three pairs of bones (the pelvis is bilaterally
symmetric):
• One pair connecting to the vertebral column, the iliac bones (ossa ilii);
• One pair connecting to each other, the pubic bones (ossa pubi); and
• One pair stretching laterally and caudally, but also serving as intermediaries,
between os pubis and os ilium, the seat bones (ossa ischii).
The ligamentous–cartilaginous connection between self-linking pubic bones is
present in all tetrapodes and is the above-named symphysis.
Back to the evolutionary ‘‘future.’’ In the marsupials, a paired os marsupii exists
that supports the pouch and articulates with the pelvis. In ontogeny, this bony part
originated from the pelvis region, which conforms to the processus prepubica,
which has been noted in several primitive Amphibia and Reptilia [2]. This
aggressive evolutionary expansion of the pelvis had already come to an end when
Man arrived. Our species bony pelvis consists of the three pairs of bones that
reunite in one point: the acetabulum, to form a joint socket for the femur, which
supports the leg in bearing the rump.
The human bony pelvis—as far as defaecation, miction, or coitus are con-
cerned—is nothing more than a firm structure for the organs involved in these
functions. In humans, the pelvis stands crenellated on both legs in such away that
the pelvic opening is directed to the front. To exaggerate, the symphysis is the
lowest point at the anterior side of the pelvis (Fig. 1.4). The consequences of this
are clear: the anus directs its longitudinal axis horizontally, and the vagina always
projects itself oblique vertically in the standing position.
The pelvis itself is not a stiff structure. Some mobility is present in the sacral–
iliacal joint, which is considered a synovial joint between sacrum and pelvis. The
sacroiliacal ligament reduces the mobility enormously. If the pair of ossi pubi can
be considered as a girder, then the construction of the pelvis as a structure that
conducts the forces over the bony components, toward the legs and supporting the
organs in the pelvis, can be understood [4] (Fig. 1.5).
The sacrum and the iliac bone are parts of a suspension bridge construction: Its
synovial joint and the sacroiliacal ligaments organize mobility and suspension.
The contents of the pelvis stay free from this play of forces, because they rest on
the lower flexible girder made up of the pubic bones and symphysis.

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1.1 The Bony Pelvis 5

Fig. 1.4 Composition figure


including an oblique frontal
view of the human pelvis, a
half-human pelvis, and an
X-ray photograph of the
human pelvis. In all these
pictures, the symphysis is
nearly the lowest point of the
pelvis. a The dorsal part of
the iliac crest is nearly
horizontal. b The linea
terminalis (innominata)
parallels the sacrotuberal
ligament. c Tuber ischii and
symphysis are the lowest
points of the pelvis
(Reproduced with permission
from the Dept. of Anatomy
and Embryology, Leiden)

Upon inspection of the bony pelvis, it is clearly visible that the pelvis is con-
structed around holes. Confusion can arise because medical Latin uses so many
names to describe a hole: Foramen, hiatus, lumen, perforation, and antrum are all
used for a small hole, while excavatio, fossa, recessus, sinus, cavum, and bursa are
also used, mainly for relatively larger holes [5]. On all sides, the bony pelvis
encloses holes, with of course different names in medical Latin. The bony pelvis
looks like Emmentaler cheese. These bony parts provide little support for the
interior parts; therefore, all kinds of ligaments are used to help fix internal
structures in place and to close holes.

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6 1 ‘‘Construction Plan’’ of the Bony Pelvis

Fig. 1.5 a View from above


on the pelvis: 1 symphysis, 2
sacroiliacal joints, 3
sacrospinal ligament, 4
sacrotuberal ligament, 5 the
greater (majus) ischiadic
foramen, 6 the lesser (minus)
ischiadic foramen, 7 foramen
obturatum, 8 linea terminalis,
9 promontorium (Reproduced
with permission from the
Dept. of Anatomy and
Embryology, LUMC,
Leiden). b Oblique frontal cut
through the pelvis at the
femur and acetabulum.
Sacrum (1) and both ossa ilii
(2) from a suspension bridge
construction. Forces led
toward the legs. The both
pubic bones (3) can be
interpreted as a movable
girdle construction (Redrawn
and changed after Moffat
1993 [3])

1.1.1 Gender Differences

The female and male pelves are different in their construction. The basis for this
sexual dimorphism is the need in the female pelvis for a birth canal wide enough to
allow the passage of the fetus. A nearly intact Pleistocene adult female pelvis of
Homo erectus found in Ethiopia shows by the width of its pelvic canal that already
during the Pleistocene era, female hominids were giving birth to well-shaped
babies with large heads [6]. The relatively narrower birth canal in modern females
shows that evolution of the pelvic structures is still continuing.

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1.1 The Bony Pelvis 7

Fig. 1.6 Female differences


compared to male in the
pubic area, changed after
Bass and reproduced with
permission (1995) [8]

One of the characteristic differences between male and female pelves is the
angle (arcus) between both downsloping bony branches of the pubic bones (rami
inferiores), called ‘‘arcus pubis’’ in the female pubis and ‘‘angulus subpubicus’’ in
the male pubis. In females, this angle is 90–100 and in males around 70 (others
say 60). Further, the transverse diameter of the pelvic entrance is larger (in
females around 13 cm) and the narrowest passage diameter, which is the distance
between both spinae ischiadicae, is around 11 cm. In males, these diameters are
around 20–25 % smaller. The upper edge of the inside of the first sacral vertebra,
called the promontorium, protrudes deeper in the male, than the female pelvis,
giving a larger birth canal entrance in women. The female pelvis is bigger and
broader, whereas the male pelvis is narrower, more massive, and steeper [7].
Careful inspection of the pubic area (Fig. 1.6) reveals that there are more
specific characteristics: the ventral arc of the area around the symphysis and the
narrow aspect of the ischiopubic ramus just beneath the symphysis [8]. Based on
these characteristics, a pelvis can be identified as being male or female. Therefore,
in paleontology and paleontopathology, knowledge of the specific characteristics
of the pelvis is a tool for determining gender or even the pathological events the
male or female had undergone.
The degree of difference between the larger female pelvis and the steeper male
pelvis can, of course, be quantified (Fig. 1.7). The proportion of the lengths of the
pubis (AB) and of the ischium (CD) is used for this purpose. In females, this
proportion is at most 68, in males at least 72 [9]. Measures of pelvic bony
structures indeed can be used for diagnostic purposes: Urine incontinence in
women is clearly related to inlet and outlet of the pelvis.
From the measure taken in Fig. 1.7b, ‘‘The independent factors (related to urine
incontinence) were pelvic inlet diameter (3 in Fig. 1.7b), pelvic inlet anterior–
posterior diameter (4 in Fig. 1.7b), pelvic outlet diameter (7 in Fig. 1.7c), and
transverse perineal muscle cross-section diameter (6 in Fig. 1.7c)’’ [9B].
There is an extra point to be made here about the female pelvis: the discussion
around the ‘‘Rhombus of Michaelis’’ in midwifery (see Fig. 1.8).
In male, this area is clearly triangular, whereas in the female, this kite-shaped
area is obviously different in shape. ‘‘This wedge-shaped area of bone moves
backwards during the second stage of labor and as it moves back it pushes the
wings of the ilea out, increasing the diameters of the pelvis,’’ thus enlarging the

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8 1 ‘‘Construction Plan’’ of the Bony Pelvis

Fig. 1.7 a Measures according to Novotny (1983) [9], reproduced with permission from
Anthropologie, Brno. b Pelvic bones parameters using 3-dimensional technique: a anterior view,
b cranial view, c caudal view, A anterior, P posterior. 1 Pelvic flaring; 2 anterior superior iliac
spine (ASIS) to ASIS; 3 pelvic inlet diameter; 4 pelvic inlet A–P diameter; 5 maximum pelvic
A–P diameter; 6 pelvic outlet diameter (spine to spine); 7 pelvic outlet A–P diameter (Text and
figure reproduced with permission from Stav et al. 2007 [9B])

birth channel [10]. It should be clear that movement of the os ilium is possible only
if there is a movement in the sacroiliac joint. If some rotation occurs, the prom-
ontorium moves inward (caudoventral), while the coccygeal bones are moved
more outward (craniodorsal), widening the pelvic outlet, but narrowing the inlet.
This, supposedly, would be beneficial during the second phase of the birth. This
idea goes back several centuries, and we will come back to it in the section on
Hendrik van Deventer (Chap. 4).

1.1.2 Posture

To return to the sacroiliac joint, the surface of this joint is rough, although it is
often depicted in the handbooks as being smooth. On both sides, it has indentations
in which bulges of the opposite side fit (Fig. 1.9). The capsular ligaments are
strong, and this is enhanced by the stiff ligaments crossing over the joint. This
inhibition of movement in a joint by strong ligaments is called amphiarthrosis. But

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1.1 The Bony Pelvis 9

Fig. 1.8 Backside of a woman left, to the right drawing of the rhombus of Michaelis in man.
Note the continuation of the fascia of the back (thoracolumbalis) into the female gluteal fascia.
The buttocks with the fissure glutea, created by the upper edge of the fascia lata or leg fascia and
aponeurosis of the iliotibial tract, are subcutaneous fat structures, and the expression of the os
sacrum and upper lumbar vertebrae, called the ‘‘Rhombus or quadrilateral of Michaelis,’’ together
with the gluteal muscles is accentuated (left figure reproduced with permission from the Dept. of
Anatomy and Embryology, Leiden and courtesy J. F. M. Landsmeer )

just because a special term has been coined for the near absence of movement in a
joint, should we therefore believe that there is actual movement in such a joint?
In order to answer the question, ten patients with sacroiliac joint dysfunction
were treated according to the accepted physiotherapeutic methods. X-ray stereo-
photogrammetric analysis showed that the sacroiliac joint had not altered its
position [11], thus stressing the immobility of the sacroiliac joint.
The presence of strong movements in the sacroiliac joint during labor is hardly
scientifically based. A review of the papers from the fourth Interdisciplinary World
Congress on Lower Back and Pelvic Pain, held in 2001, reveals that most papers do
not meet scientific standards [12] concerning pregnant and postpartum women,
while even a clear definition of lower back pain versus pelvic pain is lacking.
Traumatic movement of the sacrum and becoming clenched between both ossa ilii
(nearly almost due to weak ligaments, but also due to enduring postpartum hormonal
changes in the ligaments) or chronic or degenerative affections can induce severe
pain in the sacroiliac joint. Sacroiliac pain is considered a subset of pelvic pain and
can be diagnosed in 5–6 % of the cases, depending on one-sided or two-sided
symptoms (see also Sect. 5.8). Nevertheless, most treatments proposed are poorly
supported by research as is the treatment of women in labor by midwives [10].
Are there known cases in which movement of the sacroiliac joint is present?
The article ‘‘Nonunion of unstable fractures of the pelvis’’ [13] indicates that a
fracture in or near this joint, although rare (Fig. 1.10), leads to an unstable pelvis
and painful pelvis (see ref. 14 for an overview of sacroiliac pain [14]). It occurs

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10 1 ‘‘Construction Plan’’ of the Bony Pelvis

Fig. 1.9 Ethanol preparation of transverse sections of the sacroiliac joint. Upper two figures
show bulging and indentations on transverse section. Lower two figures show insights into the
joint, showing the ridge-like structure of the bulges (Reproduced with permission from the
Department of Anatomy and Embryology, Leiden)

mainly among the elderly. Internal fixation is a limited palliative approach to these
complaints. Therefore, most movements in the sacroiliac joint can be pointed out
being pathologic.
The gluteal region requires further attention, because the superficial construc-
tion of the buttocks differs from race to race. Steatopygy is the strong infiltration of
fat into the tissue. Especially, in Hottentot women, an extra fat layer is noticed in
the gluteal region that is even more prominent because of an extra lordosis of the
vertebral column, resulting in a nearly horizontal surface of the gluteal region (see
Figs. 1.12 and 1.8) [15]. An extra lordosis must mean an even more tilted pelvis.
So the pelvis can be in various postures to the legs.
The pelvis in achondroplasia, the small people, also named in vulgar tongue
Lilliputs, shows another aspect (Fig. 1.11). Achondroplasia is characterized by a
retardation of the growth of cartilage during development. Especially, the pelvis
and the lumbar spine are important in determining this type of dwarfism. From the
pelvic bones, the os ilium is square, while ‘‘the pubic and ischial bones are short
and square and the overall pelvic configuration is short and broad’’ [15A]. The
inferior parts of the iliac bone are short, and ‘‘therefore, the sacrosciatic notch is
short’’ [15A]. Achondroplastic children that start to stand and walk produce a
posterior tilting of the sacrum, and reduced diameters of the pelvis are noted

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1.1 The Bony Pelvis 11

Fig. 1.10 CT photograph of


‘‘hypertrophic nonunion of
the right sacroiliac joint’’
[13], by tearing of the lateral
part of L5 (arrow), which
forms the medial bony part of
the joint (Reproduced with
permission from Vander
Bosch et al. [13])

Fig. 1.11 Lateral view of


glimmering of both vertebral
column and sacrum through
body of an achondroplast.
Note the angle between
vertebral column and sacrum
(see arrow; courtesy
C. Vleggeert-Lankamp)

compared to normal pelvises. The tilting here does not produce an extra lordosis
[15A]. The vertebral column becomes more oblique directed to the front. The
sacral tilting crenellates the pelvis further and brings the symphysis more inferior,
so that the symphysis becomes the real lowest pelvic point (Fig. 1.11).
So the next subject provides greater attention to the position of the pelvis and its
musculature in bipedal motion. Before discussing it, there are two more reasons to
use the example of the Hottentot woman (Fig. 1.12). Pelvimetry has been carried
out early in anatomy and anthropology (e.g., Turner [16]) to establish race rela-
tions, resulting in the nineteenth century indiscriminations like: ‘‘The Australians,

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12 1 ‘‘Construction Plan’’ of the Bony Pelvis

Fig. 1.12 Picture of the


Hottentot woman Saartjie
Baartmans, reproduced with
permission from the
Bibliothèque national de
France, see also Badou [15]

Bush, Kaffers and Andamanese present a closer approximation to the relative


proportions of the parts found in the pelves of apes…. The pelvis, therefore, in
those races shows a more degenerated character—a less departure from the usual
mammalian form—than is the case in Europeans’’ [16]. The typing of the pelves of
races in three classes, however, was counteracted by the female pelvis: ‘‘How
greatly the female pelvis is modified in the proportions of the pelvic brim (=index;
here proportions of transverse and conjugate measure of the pelvis) in relation to
the special sexual requirements, is shown from the fact that in none of the people
or races whose pelvic dimensions are analyzed in sufficient numbers to enable one
to obtain an average, does the female pelvis attain in the mean of each race
dolichopellic (mainly European pelvic measures!) proportions’’ [16].
The dimension of the sacral bone is the other objective. Turner [16] also mea-
sured the maximum length and breadth of the sacrum and developed a sacral index
(multiplying the breadth with 100 and dividing it by the length). ‘‘When the sacral
index is above 100, the breadth of the bone is of course greater than the length,
when below the length exceeds the breadth’’ [16]. The results are as follows: Kaffirs
92.8, Andamanese 94, Bush 94, Australians 98, Negroes 105.5, and Europeans 112.
We leave the biased conclusions from these results to Turner, but look now to
magnetic resonance imaging (MRI) studies in 2008 [17] for pelvic racial differ-
ences: ‘‘The pelvic inlet was wider among 178 white women than 56 African-
American women. The outlet was also wider.’’ And in the discussion: ‘‘The
conventional teaching regarding the anthropoid pelvis is characterized by a long
sacrum of ‘average curvature’. However, we unexpectedly found that African-
American women had a significantly shorter sacrum than the white subjects.’’
From Turner’s results from 1885, it appears that at the same breadth, his ‘‘Negro’’
sacral length should be shorter. The same MRI article states, citing Baragi’s (2002)

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1.1 The Bony Pelvis 13

Fig. 1.13 Orientation of the pelvis in gorilla and Man are as different as their anatomy is
(Reproduced with permission. Copyright  1967 Scientific America Inc. All rights reserved.
Figures from Napier [18])

article [17] on bony pelvic measurements: ‘‘Their findings demonstrated a smaller


posterior and total pelvic area in the African-American as compared to white
women.’’ Turner’s female ‘‘Negro’’ pelvic index was also smaller than the white
woman ones; nevertheless, it reached the European standard deviation. Although
Turner’s study was done in light of the supremacy of the white and the MRI study
for implications in obstetric practice, the same results are obtained 200 years later
with the most sophisticated medical instrument. Therefore, racial differences are
present in the bony pelvis and are important in clinical obstetrics.
We come back here to the tilted pelvis: Bipedal movement is made possible by
the crenellated pelvis in humans. The pelvic bony structures had to change in
shape and in orientation (see Figs. 1.3 and 1.13), because muscles had to change
their function: pelvic and femoral muscles altered from extensors into abductors
compared to quadruped posture in hominids. Hamstring muscles transformed to
stabilizers and extensors of the hip (Fig. 1.14) [18].
‘‘Bipedal posture brings a reversal in the roles played by the same pelvic and
femoral muscles. The gluteus medius and minimus have changed from extensors
to abductors and the function of extending the trunk has been assumed by the
gluteus maximus. The hamstrings act as stabilizers and extensors of the hip.
Quadruple posture needs two sets of muscles to act as the principle extensors of the
hip: the gluteal group (gluteus medius and minimus), connecting the pelvis to the
upper part of the femur and the hamstrings which connects the femur and the lower
leg bones (only biceps femoris is shown). In most primates the gluteus maximus is
quite small’’ [18]. The muscles of the back (especially the erector spinae) obtain
the extra function, keeping the body upright. To overcome sinking away of the os
sacrum in bipedal posture, the sacroiliac joint increases.

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14 1 ‘‘Construction Plan’’ of the Bony Pelvis

Fig. 1.14 Comparison between muscles and bony structures of pelvis and leg in Man and gorilla
(Reproduced with permission. Copyright  (1967) Scientific American, Inc. All rights reserved.
Figures taken from Napier [18])

Fig. 1.15 Extensive


hemipelvectomy including
part of the ramus inferior and
superior of the pubic bone at
the contralateral side and
most parts of the sacral bone
are removed besides the
hemipelvectomy
(Reproduced with permission
from Maljers [20])

Indeed, bipedal gait has more consequences for the form and function of the
pelvis and, of course, for the whole body.
These consequences can be well illustrated by some clinical examples.
Hemipelvectomy (Fig. 1.15) has been performed for the first time in 1889 or
1891 [19] and carries a series of synonymic names such as interinnomina-
abdominal, interilioabdominal, transpubic, transiliac, hindquarter amputation. It is
the total removal of the leg with a partial resection of the bony hemipelvis. The
sacroiliacal joint or synchondrosis normally stays intact; however, if the iliac bone
is also involved in the disease, a whole hemipelvectomy has to be done.

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1.1 The Bony Pelvis 15

The cause of the rare disease that needs hemipelvectomy is a cancer of the
connective tissue called sarcoma. Fibrosarcoma, osteosarcoma, and chondrosar-
coma (connective tissue, bone, and hyaline sarcoma) restricted to the leg only need
a leg amputation, and extension toward the pelvic bones brings forward a hemi-
pelvectomy [20].
The rather surprising fact that although a hemipelvectomy was carried out with
a postoperative mortality that is nowadays nearly zero, females can become
pregnant and labor babies. Till 1976, all over the world, 14 women with a hem-
ipelvectomy gave birth to 19 living babies [20], stressing the functional inde-
pendence of the internal pelvic organs from the bony skeleton.
In spinal cord injuries, posture in the standing position is impossible in patients
with a total chordotomy. However, postural passive control is possible in the
sitting position by these patients and the possibility of tilting the pelvis, which is
normally necessary for posture, can be studied [21]. Three groups were compared:
normal healthy persons, patients with a low total chordotomy (lesion from T9 till
T12), and high spinal cord total lesions (high lesion, from T2 till T8). Markers
were placed in such a way that the vertebral column, pelvis, and upper leg could be
followed in 3D. The task was to reach forward in the sitting position and reach
various distances. The erector spinae muscles are important for posture and thus
for pelvic tilt. Patients with a high spinal cord lesion could reach but did this
exclusively with arm and shoulder muscles, but no tilt of the pelvis was noted.
Low spinal cord lesion patients had some small possibility to tilt their pelvis, due
to their still present steering of the upper erector spinae muscles during bending
over to reach. Here, small upper rump movements were possible, forcing minimal
pelvic tilt. In normal persons, vertebral column and pelvic tilt were far larger than
those in patients [21]. So spinal cord injury patients tried to stabilize balance,
while normal persons could compensate for it.
Postural balance, in which pelvic tilt is important, needs intact hip, leg, and
rump muscles. Steering of postural balance requires an intact nervous system.

Literature

Literature has been grouped in reference lists of several chapters in those cases where
arguments are difficult to entangle or published over several articles or books. In cases of
citation the article or book involved is indicated by the reference number together with a
capital Arabic letter.
1. Steiner G (Stümpke, H) (1962) Bau und leben der Rhinogradentia. Gustave Fischer Verlag,
1–85
2. Ihle JEW, Nierstrass W (1941) Leerboek der vergelijkende ontleedkunde van de vertebraten,
vol I, Voortbewegingsorganen. Oosthoeks Uitg., Utrecht. And Broom R, Robinson JT
(1950) Notes on the pelves of the fossil ape-men Am J Phys Anthropol 8:489–494
3. Jordaan HVF (1976) The differential development of the hominid pelvis. SA Med J
50:744–748
4. Moffat DB (1993) Lecture notes on anatomy. Blackwell Science Publication, London,
pp 1–416

sergiocamargo47@gmail.com
16 1 ‘‘Construction Plan’’ of the Bony Pelvis

4A. Walker E (2002) When I use a word: pelvis. BMJ 325:264


5. Marani E (1991) Bluff your way in anatomy. Lecture notes, Leiden, pp 1–36
6. Simpson SW, Quade J, Levin NE, Butler R et al (2008) A female homo erectus pelvis from
Gona, Ethiopia. Science 322:1089–1092. Note: Analogous results were already published,
see: Trinkaus E, Howells WW (1979) The Neanderthals. Sci Am 94–105
7. Schünke M, Schulte E, Schumacher U, Voll M, Wesker K (2005) Prometheus,
anatomische atlas; algemene anatomie en bewegingsapparaat. Bohn, Stafleu, van
Loghum, Houten, The Netherlands
8. Bass WM III (1995) Human osteology: a laboratory and field manual, 4th edn. Missouri
Archeological Society. Columbia see also: Phenice TW (1969) A newly developed visual
method of sexing the os pubis. Am J Phys Anthropol 30:297–302
9. Novotny V (1975) Diskriminantanalyse der Geslechts-merkmale auf demos coxae beim
Menschen. In: Proceedings of 13th congress anthropol brno Czechoslovakia, pp 1–23 and
Novotny V (1983) Sex differences of pelvis and sex determination in paleoanthropology.
Anthropologie 21:65–72
9B. Stav K, Alcalay M, Peleg S, Lindner A, Gayer G, Hershkovitz I (2007) Pelvis architecture
and urinary incontinence in women. Eur Urol 52:239–244
10. Sutton J (2000) Birth without active pushing and a physiological second stage of labour.
Practicing Midwife 3:32–34 (see also: Kitzinger S (1993) Ourselves as mothers. Bantam,
London and discussions on the web)
11. Tullberg T, Blomberg S, Branth B, Johnsson R (1998) Manipulation does not alter the
position of the sacroiliac joint: a roentgen stereophotogrammetric analysis. Spine
23:1124–1128
12. Albert H (2001) Treatment of pelvic and low back pain in pregnant and postpartum
women. In: Proceedings of 4th international disciplinary world congress low back and
pelvic pain, pp 113–121
13. Van den Bosch EW, Van der Kleyn R, Van Zwienen MCMA, Van Vugt AB (2002)
Nonunion of unstable fractures of the pelvis. Eur J Trauma 28:100–103
14. Hansen HC, McKenzie-Brown A, Cohen SP, Swicegood JR, Colson JD, Manchikanti L
(2007) Sacroiliac joint interventions: a systematic review. Pain Physician 10:165–184
15. Badou G (2002) L’énigme de la Vénus Hottentote. Pte Bibliot. Payot, Paris and references
herein
15A. Thomeer RTWM (1982) Achondroplasia. Management of neurological complications.
Thesis, University of Leiden
16. Turner MB (1885) The index of pelvic brim as a basis of classification. Report on the
bones of the skeleton of the voyage of HMS Challenger. www.19thcenturyscience.org/
HMSc/HMSCreports
17. Handa VL, Lockhart ME, Fielding JR et al (2008) Racial differences in pelvic anatomy by
magnetic resonance imaging. Obstet Gynecol 111:914–920 and Baragi RV, Delancey JO,
Caspari R et al (2002) Differences in pelvic floor area between African American and
European American women. Am J Obstet Gynecol 187:111–115
18. Napier J (1967) The antiquity of human walking. Sci Am 216:56–66
19. Pringle JH (1916–1917) The inter-pelvi-abdominal amputation. Brit J Surg 4:283–290 and
Nilsonne U (1965) Radical amputation for malignant tumors of the extremities. Acta Chir
Scand 129:150–153
20. Maljers LDJ (1976) Hemipelvectomie. Thesis, University of Leiden and Sugarbaker P,
Malawar M, Henshaw R (2001) Anterior (chap 19) and posterior (chap 20) flap
hemipelvectomy. In: Malawer MM, Sugarbaker PH (ed.) Musculoskeletal cancer surgery.
Kluwer Academic Publishing, Amsterdam
21. Janssen-Potten YJ, Seelen HA, Drukker J, Huson T, Drost MR (2001) The effect of seat
tilting on pelvic position, balance control and compensatory postural muscle use in
paraplegic subjects. Arch Phys Med Rehabil 82:1393–1402

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Chapter 2
The Pelvis at War

Pelvic traumas can be studied from remains by osteoarcheology and by records of


modern warfare. Both approaches show that pelvic stability is a prerequisite to
survive in war situations but also in vehicle injuries.

2.1 Introduction

Pelvic remains have been collected from historical war graves and other archeo-
logical sites. Archeologists have studied these remnants. The pelvic results are so
to say ‘‘buried’’ into large overviews of all kind of skeletal rests of corpses. It is
therefore easily understandable that this chapter will miss several of the results
currently present in the literature and our treatment will not be complete. More-
over, the word ‘‘war’’ should not be taken too literally: civilian hostilities, fights
with animals are included, and some history is inevitable.
Bone cuts on skeletal remains have to be divided into knife and sword marks.
‘‘Swords have been one of the major weapons used in violent conflicts for much of
human history. Certain archeological situations, especially those dealing with the
recovery and analysis of battle casualties, may raise questions about what type(s)
of bladed weapon was used in a particular conflict’’ [1]. It is easy to discern knife
marks from sword marks, but even the type of sword can be traced, due to dif-
ferences in blade weight, grip, and sharpness [1]. Thus, osteoarcheology has the
means to determine the type of bladed weapons used.
Nowadays, damage of the bony pelvis in daily life is mostly due to high-energy
blunt traumas among which traffic accidents and falls are the most prevalent. In
nearly 20 % of such cases, the pelvis or acetabulum is fractured, and in half of the
cases, the patient needs surgical stabilization. Pure sacrum fractures accounts for
11 % of pelvic ring injuries. Pelvic trauma and pelvic fracture does affect geni-
tourinary function in 7–14.5 % and reproductive function in 46.5–60 % (dystocia)
in women. More studies on female pelvic trauma effects can be found in the
literature [2B]. Pelvic fracture is not the main cause of death, but combinations
with other injuries, such as head, thorax, or abdominal traumas are in [2]. Some
studies have reported a mortality rate of 13.9–24 % after acute pelvic fracture.

E. Marani and W. F.R.M. Koch, The Pelvis, 17


DOI: 10.1007/978-3-642-40006-3_2,  Springer-Verlag Berlin Heidelberg 2014

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18 2 The Pelvis at War

Severe bleeding from pelvic trauma produces mortality [2A], but in historical
cases, cause and effect are nevertheless, difficult to separate, especially in the
absence of good medical care.

2.1.1 Neanderthals

Remains of Neanderthals contain bony lesions, of which head and neck injuries are
the most reported. These traumatic lesions together with posttraumatic degenerative
changes were studied by their anatomical distribution in the human body: head,
neck, thorax, abdomen, extremities, and pelvis. They were compared to human
archeological samples, modern clinical samples and to injuries of Rodeo per-
formers in North America. Pelvic lesions were present only in 3.7 % of the cases
and belonged to the posttraumatic degenerative changes among Neanderthals. To
make a long statistic story short, Neanderthal lesions were comparable to those
found in the Rodeo performers. ‘‘It appears more likely that behavioral patterns
paralleling those of Rodeo athletes explain the Neanderthal injury patterns. This is
not meant to imply that Neanderthals would have met the behavioral qualifications
for membership in the Professional Rodeo Cowboy Association. More likely, it
relates to their normal means of predation’’ [3] and ‘‘Given the tendency of un-
gulates to react strongly to being impaled, the frequency of head and neck, as well
as upper limb, injuries seen in the Neanderthals should not be surprising’’ [3].
Mobility is an essential survival quality in hunters. Head and neck injuries can
be overcome, but it is surprising that the number of pelvic traumas found among
the Neanderthals is so small. One would imagine that bull fighting should produce
more pelvic traumas. But it is not that case: the statistic incidence is the same as
that for Rodeo cowboys, 3.3 %. ‘‘Those no longer capable of keeping up with the
social group, whether as a result of age or serious lower limb trauma, may have
simply been left behind, to die in localities where their remains were not preserved
and recovered’’ [3]. Walking and running are also dependent on the pelvic
integrity. Could it be that Neanderthal pelvic victims were left behind and
therefore their incidence among the known skeletal remains is low?

2.1.2 Pazyryk Mongolian War Skeletons

Pazyryk is the name given to Indo-European tribes that spread across the Eurasian
steppes. Their presence between the third and fifth centuries BC is characterized
by stone tumuli in the Altai region (Central Asia, near Kazakhstan). The warriors
were buried in these tumuli together with their horse and weaponry. These nomads
carried out cruel rituals like: ‘‘human sacrifices, scalping of enemies, and canni-
balism’’ [4]. Their warfare and violence can be studied by the traumatic injuries on
skeletal bony parts.

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2.1 Introduction 19

Fig. 2.1 Cut mark on the left lateral anterior side of the first sacral vertebra from a child
(numbered TSK/T2B). a Location of the cut mark, b defect detail, and c the direction from which
the blow was delivered and the Scynthian dagger: bar is 1 cm (reproduced with permission from
Jordana et al. [4])

‘‘Pelvic injuries exhibited by individuals BTG-VI/T12 and TSK/T2B (see


Fig. 2.1) would involve vascular iliac structures besides pelvic viscera causing
fatal hypovolemic shock. These deadly injuries could be compatible with the
action of the Scythian dagger’’ [4]. From the 10 skeletons with several injuries
each, two had perimortem pelvic injuries, indicating a far higher percentage than
was found in the Neanderthal study. Healing had occurred, mainly in injuries of
hand bones, skull, ribs, and clavicle, but not in pelvic structures.

2.1.3 Trojan Siege

‘‘The other information that we have of the Trojan siege is derived mainly from
Homer’s iliad in which the author gives detailed accounts of the wounds. Frolich
has analyzed Homer’s work and demonstrated that there was a variation in the
number of wounds caused by each weapon and the percentage of fatalities’’ [5]. It
is inevitably that spears had the greatest chance of hitting with a fatality rate of
nearly 80 %. Blows with the swords were very accurate with 100 % fatality.
‘‘Slingshots and arrows had a very low hit rate and medium fatality with arrows at
the worst’’ [5]. Of course, one knows that Homer’s iliad is a folk-tale, perhaps
based on historical events. Nevertheless, it well illustrates the effectiveness of
ancient weaponry, the more so because Homer may have had a medical education
and perhaps performed dissections [5A]. Pelvic casualties are also described in the
iliad. Meriones, the Cretan, hits Phereclus: ‘‘He struck him in the right buttock, and
the spear point went right on through under the bone into his bladder.’’ The salient
detail is, of course, that in Homer’s iliad, the pelvic acetabulum/hip fracture of
Aeneias is caused by a stone thrown by Diomedes not by a weapon. The twelve
cases with pelvic related injuries in Homer’s description are shown in Table 2.1

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20 2 The Pelvis at War

Table 2.1 The pelvic and urogenital injuries in Homer’s iliad (table is from Poulakou–Rebelakou
et al. [5A] with permission)
No Text. Ref Weapon Location Result Victim
1 Il IV, 489–493 Spear Groin Immediate death Leucus
2 Il V, 65–68 Spear Bladder Immediate death Phereclus
3 Il V, 516–519 Spear Abdomen Immediate death Deicoon
4 Il V, 615–617 Spear Abdomen Immediate death Amphius
5 Il V, 855–858 Spear Abdomen Miraculous healing God Ares
6 Il VI, 63–65 Spear Flank Immediate death Adrastus
7 Il XIII, 567–569 Spear Between privy parts Painful death Adamas
and navel
8 Il XIII, 650–655 Arrow Bladder Immediate death Harpalion
9 Il XIV, 446–447 Spear Flank Immediate death Satnius
10 Il XVI, 317–319 Spear Flank Immediate death Atymnius
11 Il XVI, 463–465 Spear Abdomen Immediate death Thrasymelus
12 Il XVII, 516–519 Spear Abdomen Immediate death Aretus

2.1.4 Modern Weapons

The approach used by archeologists has also been used for victims of modern
weapons of war. X-rays results have been published for victims in Vietnam,
Croatia, Serbia, Bosnia, Chad, Iran, Afghanistan, the USA, Great Britain, France,
Israel, Palestine, and Germany, and these were used to relate wounds to weapons.
‘‘Radiograms of injuries due to hand grenades show their content (globes) and
cover fragments. The globes are localized regionally in the victim’s body. Sur-
vivors of cluster bombs show singular or few globes having been hit by many
globes would have been lethal. Shotguns produce characteristic distributions of the
pallets and depth of penetration different from those of hand grenades and cluster
bombs; cover fragments are lacking. Gunshot wounds (GSW) can be differentiated
in those of low velocity bullets, high velocity projectiles, and projectiles, which
disintegrate on impact’’ [6]. And: ‘‘Radiographs may show, which weapon has
been employed; they can be read as war reports’’ [6].
While the scars and trauma from the past can be considered from a distance,
those of recent wars are nearer and more disturbing to our minds. But let us try to
treat these in the same way as we did with the Trojan results. What are the effects
of this modern weaponry on the pelvis. In Fig. 2.2, the effects of injuries inside
vehicles in Afghanistan are given.
The percentages of pelvic injury are low for vehicle injuries (2.8 %). ‘‘Many
para-axial injuries involve the thorax and abdomen, with accompanying trauma to
vital structures which is rapidly fatal if not treated immediately. Few such patients
survive the arduous trip across the mountains to our hospital’’ [6]. The para-axial
injuries include the pelvic ones. Thus, the 2.8 % is low, and this is presumably due
to the seats of the vehicle, which provide protection.

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2.1 Introduction 21

Fig. 2.2 Vehicle injuries after blasts and missile attacks (figure is reproduced with permission
from Vogel and Dootz [6])

Soft tissue results from the Vietnam war and World War I and II show far
higher percentages for pelvic wounds: for the bladder 18 % on average and for the
urethra 9 % with significant differences for each war and each researcher [7]. The
scud missile launched from Iraqi territory into the city of Al-Khobar in Saudi
Arabia that killed 28 and injured 100 USA soldiers shows that if a hospital is near
(King Fahd Hospital is 2 km away), the number of pelvic injuries was rather high,
up to 20 % of fractures [8]. Thus indicating that pelvic injuries are often related to
immediate death.
In the Aden war from 1964 to 1967, the rate of lethal pelvic injuries: acute,
survival of a few moments and despite first aid treatment was 15.5 %. Of those who
died despite First Aid Treatment, the pelvic iliac vessels were involved in 29 % of
the soldiers [9]. For the Northern Ireland hostilities, it was found that of total vessel
damage 11 % concerned pelvic vessels and 10 % of the pelvic injuries were
skeletal. A total of 12.5 % of the patients died from pelvic related wounds [10].
The database of the International Committee of the Red Cross indicates that
8.2 % of the wounded in several wars had wounds of the pelvis and buttocks, with
one-third pure pelvic wounds, while of the total wounds 10–20 % belonged to
abdominal wounds, administrated for those patients who could reach a hospital of
the Red Cross in five different war zones. It should be noted that abdominal
wounds by cluster bombs nearly always contain pelvic damage too, but these are
not always separately registered. For GSW, bleeding after pelvic fractures is
responsible for 5–30 % mortality, while in 18–64 % rectal, and in 24–57 %
genitourinary wounds are involved [10].
Real statistics are difficult to compile, since the conditions of civil hostilities
and of different wars are hardly comparable. A ‘‘bad,’’ rough, conservative, esti-
mate is that 10 % casualties for civilians and 15–20 % for soldiers are caused by

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22 2 The Pelvis at War

wounding of the bony pelvis and/or pelvic soft structures which is 1 in 10 for
civilians and 1 in 7 till 1 in 5 for soldiers. Pelvic vessel damages, but even pelvic
fractures, have the lowest survival rate. No distinction was made among fragment
wounding, bullets, or mines in this part.

2.1.5 Pelvic Stability and Pelvic Fractures

To understand the following part on the siege of Sarajevo stability and fractures of
the pelvis have to be considered. Historical overviews show that before the
introduction of X-rays (after the discovery in 1895) pelvic fractures were hard to
diagnose. ‘‘J. F. Malgaigne (1806–1865) described pelvic fractures in Paris. His
explanations of the pattern of fractures of the pelvis were based initially on the
history and clinical examination of patients and then on their autopsies (emphasis
ours)’’. In 1847, he published an atlas of traumatology, in which he characterized
ten patterns of pubic ramus fractures with a vertical fracture of the iliac bone
(Malgaigne injury) [12]. In the 1950s, the Canadian surgeon George F Pennal
(1913–1976) made the breaking through. He started with anatomical studies on
compressions of the pelvis: anteroposterior and lateral compression, and vertical
shearing forces were studied. Improvements of X-ray projections of the pelvis and
the use of the external fixator in the multi-fractioned pelvis improved the clinical
approach. His classification of pelvic fractures is still at the base of the modern
ones. His students continued his research and Marvin Tile and his colleagues
produced the classical book ‘‘Fractures of the pelvis and acetabulum.’’ So far, this
historical synopsis leaves out a series of important contributions of surgeons and of
researches that advanced the pelvic treatment before Pennal started his studies.
Let us start with pelvic stability. In an anterior–posterior view of the pelvis, the
sacrum functions like a key stone as in classic arcades. However, when the sacrum
is viewed from above, the sacroiliac joint looks like a straight line, although we
know that its surface is not flat but contains protuberances and is tightly fixed by
ligaments. Forward shifting of the sacrum is stopped by the protuberances within
the joint and the sacroiliac ligaments (see Chap. 1). Thus, stability of the pelvic
ring is organized by a key stone mechanism and fixation to the iliac blades of the
sacrum. One should note that the pubic bones are hardly involved in the stability of
the pelvic ring. ‘‘The anterior pubic rami act as a support to prevent anterior
collapse of the pelvic ring during weight bearing. However, congenital or trau-
matic absence of the anterior structures has little effect on pelvic stability’’ [13].
So, pelvic stability is mainly disturbed by fractures that engage bony parts of the
sacrum or ilium or disruption of sacroiliac ligaments.
Pelvic fractures are classified according to their effect on the stability of the
pelvic ring: stable, partial unstable, and unstable ones [14]. Description of the
whole classification is beyond the scope of this chapter. Here, we treat a few
categories. To the stable ones belong the fractures that have no influence on the
pelvic ring and those that do eventually: avulsion of small parts of bones like an

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2.1 Introduction 23

Fig. 2.3 Upper figures open book pelvic fracture, showing a bilateral and a unilateral open book
fracture, lower figures Malgaigne fracture. The fractures and tears are indicated in red. Reproduced
from ‘‘fractures of the pelvis and acetabulum,’’ by Tile M, Helfet DL, Kellam JF (2003) with
permission for their figures Ch 12: 12–18, 12–22, and 12–33 (Courtesey Marvin Tile [13])

edge of the ilium (isolated iliac wing fractures) has no effect on the pelvic ring and
a fracture of all 4 pubic rami (superior and inferior ones), called the straddle or
butterfly fracture, can effect the whole pelvic ring, although instability will not
directly be noticed [14]. Fractures of the coccygeal bones do not disturb the pelvic
ring stability, but can especially induce long-lasting pain [14].
The so-called open book injury (see Fig. 2.3) belongs to the partial unstable
ones: The symphysis is disrupted, the pelvis opens like a book and tearing of parts
of the sacroiliac ligaments and joint (but not the entire sacroiliac joint) occurs
together with disruption of the sacrospinous ligament and pelvic floor, often
inducing visceral injuries [14]. To the unstable ones also belong the Malgaingne
vertical shear (indicated above, see Fig. 2.3): A unilateral fracture of symphysis
over the sacrum or ilium, disrupting the sacral ligaments, pelvic floor, and the
pelvic soft tissues. It is a ‘‘complete disruption of the posterior sacroiliac complex’’
[14]. Most of these fractures are caused by traffic incidences. An analogous sub-
division of acetabular fractures is present, but not discussed here.
Open pelvic fractures, that occur during war, together with complex fracturing
will result in an average mortality of 25–30 %, while those that survive ‘‘become
severely disabled and have a long and difficult course, battling pelvic sepsis to
survive’’ [15]. Complication rates for external fixation of pelvic fractures in nor-
mal hospitals are estimated on 47 % [15].

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24 2 The Pelvis at War

Open also means laceration of perineal or gluteal areas. Disruption of pelvic


soft tissue, especially damage to rectum or colon is related to serious infection.
Open pelvic fractures are the most feared by the surgeon. Age is also an important
factor: persons older than 40 years have a survival chance of 22 %, while younger
ones show 82 % survival [15].
The current approach of dealing with unstable fractures is internal fixation of
the unstable pelvic ring. Before 1980, external fixation was the main choice.
Internal fixation reduces malunion, nonunion, and leg length discrepancies.
Moreover external fixation provides insufficient stability. Due to modern guidance
techniques, minimally invasive approaches are needed, and under certain condi-
tions, the patient can be mobilized earlier [16].

2.1.6 Sarajevo

Since its foundation in 1461 by the Ottomans, Sarajevo has always been a con-
tested city. In every political instability in the region, it has been involved,
besieged, or occupied. World War I started with the assassination of the Austrian
Archduke Franz Ferdinand of Austria and his wife Sofie in Sarajevo on June 28,
1914, because of Serbian-Bosnian political instability. During World War II, it
was part of a German puppet state, lead by Tomislav II. The whole Jewish pop-
ulation of the city was eradicated. On April 6, 1945, Sarajevo was liberated and
was integrated in Tito’s Yugoslavia, officially the Socialist Federal Republic of
Yugoslavia. After the disintegration of the Republic of Yugoslavia and the inde-
pendence declaration of Bosnia-Herzegovina, the city was besieged from April 5,
1992, till February 29, 1996, by the Yugoslav army under Ratko Mladic, called the
butcher of Sarajevo, who was arrested as this chapter was being completed.
Sarajevo was thus besieged for 4 years: 1992–1996. ‘‘The siege of Sarajevo was
the longest in modern times. It was an example of a method of warfare as old as
recorded history, in which attrition is focused on the civilian population with the
ultimate aim of attacking the citizens psychologically and physically. As well as
wounding and killing, the weapons used are those of fear, uncertainty, and depri-
vation. All will suffer, but the sick and elderly, the unborn children and infants, and
the wounded are particularly vulnerable to starvation and loss of basic amenities’’
[5]. Indeed for the Dutch population with its memories of five-year occupation by
Germany (1940–1945), the bombardment of Rotterdam, the Jew deportation and
near the end of the war, serious starvation in ‘‘fortress Holland’’ the siege of
Sarajevo was a ‘‘dramatic recollection’’ of World War II, especially so when the
Dutch troops could not protect the Bosnian Muslim population of nearby. In the
massacre of Sebrenica (July 11–22, 1995), over 8,000 men and boys were murdered
and numerous women raped and/or sexual assaulted by Ratko Mladic’s army.

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2.1 Introduction 25

Fig. 2.4 Relationship


between reduction in
available food for the
wounded patients in the State
Hospital Sarajevo and the pin
track infection from August
1993 to January 1994 [11].
Text and figure reproduced
with permission from Beavis
[11]

From the siege of Sarajevo comes the device known as Sarafix. Within a few
weeks to months after the start of the siege of Sarajevo devices for fixing fractures
(internal and external ones) were no longer available. Within the city, a device
called Sarafix was developed by an engineer and surgeons and applied in 3,000
cases. ‘‘HMD Response International provided a critical component of the fix-
ture—its surgical steel pins—as part of its support programme for the surgical
development’’ [5]. As we have seen above fixing pelvic fractures is an effective
procedure in healing.
The Sarafix is an iron rod or several coupled rods, on which one can slide and
fasten smaller steel rods that are secured to the damaged bony parts with steel pins.
The rod and the smaller ones are outside the body, only the ends of the smaller
rods enter the damaged area together with the pins. The system is not new and is
known as ‘‘fixateur externe’’ or external fixator, but made from inert metal alloys
such as vitallium and is used for osteosynthesis. Since pelvic fracture healing takes
3–6 months, reaction to the iron, so-called metallosis, will occur with increased
pain and a possible rejection of the fixator from the tissue involved.
Sophisticated materials were not available, but the simple Sarafix device
worked also very well for pelvic fractures: ‘‘The device was used at many sites
including complex pelvic injuries with bowel and vascular damage’’ [5], and in
82 % the knitting of fractures was achieved [11].
Threats to the patients were infection, osteomyelitis, and the starvation that set
in after first year of the siege. Infection and malnutrition were coupled. ‘‘A direct
relationship was observed between the reduction in food supplies and an increase
in wound infection when the pin track sites of the Sarafix device were inspected’’
[5] (see Fig. 2.4).
Immobilization of the pelvic fracture in order to heal is the method of choice,
and in Sarajevo due to starvation, the increasing risk of infection was fought by
open wound care. ‘‘War wounds are complex and inevitably get infected. In the
early months of the World War I, British Army Medical Officers were inexperi-
enced in treating such terrible wounds, and a massive number of lethal infections
occurred. In 1915, orders were given to remove all dead and foreign material and

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26 2 The Pelvis at War

Fig. 2.5 The Sarafix at


‘‘work.’’ Patient with open
hip and open perineal wounds
and the external fixator
Sarafix in place (figure
reproduced with permission
from Beavis [11])

to never primarily close wounds. The technique is known as debridement, from the
French to unsaddle or release. This tested method was employed in Sarajevo with
great success with the addition of an anti-tetanus toxin and antibiotics. Injuries
near the buttocks were particularly at risk of such infection’’ [5]. It worked, but as
one can imagine a pelvic fracture fixed by the Sarafix with open wound(s)
(see Fig. 2.5) must have been a terrible ordeal. And the same conditions which
made this procedure necessary are present today in other areas on the globe too.
From experience with pelvic stability and pelvic fractures, it was concluded that
the internal fixator is the better approach for reunion and pelvic stability. Pelvic
multi-fractures are difficult to treat and heal. Moreover, all war wounds are
infected. The surgeons in Sarajevo only had the external fixator possibility due to
the war conditions. The results are amazing: 82 % reunion; 3 % malunion, and
5 % nonunion. In 6 % of the cases bridging occurred but a defect remained and
amputation was necessary in 3 % of the patients treated. Of course, ‘‘simple’’
fractures were among these cases (tibia 37 % and femur 25 %) [11], but 10 % or
even more must have belonged to pelvic injury. Nevertheless, the outcome under
these conditions is unbelievably good, and the quote above demonstrates that it
also worked for pelvic fractures with soft tissue damage. The war surgeons in
Sarajevo earn our ‘‘pelvic’’ respect!
In conclusion, the pelvis is involved in 10–20 % of war casualties, of which
25–30 % will not survive, meaning that of 100 soldiers from 3 to 5–6 will die from
pelvic wounding. Figures may be higher, since not all casualties are registered for
their type of wounding during war. Bleeding from pelvic vessels is a serious threat,
but pelvic multi-fractures are an equally serious menace. If pelvic wounding is
present in multi-trauma situations mortality rates increase. Survival during war or
civil hostilities is dependent on stopping pelvic vessel bleeding, immobilization of
fractures, stopping infection, debridement and nutrition, and adequately restoring
soft tissue tears in the pelvic organs and pelvic ligaments.

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Literature 27

Literature

Literature has been grouped in reference lists of several chapters in those cases where
arguments are difficult to entangle or published over several articles or books. In cases of
citation the article or book involved is indicated by the reference number together with a
capital Arabic letter.

1. Lewis JE (2008) Identifying sword marks on bone: criteria for distinguishing between cut
marks made by different classes of bladed weapons. J Archeol Sci 35:2001–2008
2. Woltmann A, Eckardt H, Gaul L (2010) Management der Beckenverletzungen beim
Polytrauma. Trauma Berufskrankh 12 [Suppl 2]:183–187; Eid K, Keel M, Keller A, Ertel
W, Trentz O (2005) Einfluss der Sakrumfraktur auf das funktionelle Langzeitergebnis von
Beckenringverletzungen. Unfallchirurg 108:35–42; Zannis VJ, Wood McD (1980)
Laparotomy for pelvic fracture. Amer J Surg 140: 841–845
2A. Peiniger S, Maegele M (2010) Traumaassoziierte Blutung beim Schwerverletzten
Relevanz, Risikostratifizierung und aktuelle Therapieansätze. Der Unfallchirurg
doi:10.1007/s00113-010-1860-2
2B. Copeland CE, Bosse MJ, McCarthy ML, MacKenzie EJ, Guzinski GM, Hash CS, Burgess
AR (1997) Effect of trauma and pelvic fracture on female genitourinary, sexual, and
reproductive function. J Orthop Trauma 11:73–81 and Copeland CE (2003) Pelvic ring
disruption in women: genitourinary and obstetric implications, Ch 18:329–341. In: Tile M,
Helfet DL, Kellam JF (eds) Fractures of the pelvis and acetabulum. Lippincot Williams
and Wilkins, Philadelphia
3. Berger TD, Trinkhaus E (1995) Patterns of trauma among Neandertals. J Archeol Sci
22:841–852
4. Jordana X, Galtés I, Turbat T, Batsukh D, Garcıá C, Isidro A, Giscard P-H, Malgosa A
(2009) The warriors of the steppes: osteological evidence of warfare and violence from
Pazyryk tumuli in the Mongolian Altai. J Archeol Sci 36:1319–1327
5. Beavis JP, Ryan JM (2002) High energy transfer missile wounds in the siege of Sarajevo
and their relation to mine injuries. J Mine Action 6.3 Victim Assistance
5A. Poulakou-Rebelakou E, Rebelakos AG, Marketos SG (1998) Urologic references in the
Homeric epics. De Historia Urologiae Europaeae 5:249–257
6. Vogel H, Dootz B (2007) Weapons and wounds. Eur J Radiol 63:151–166
7. Selikowitz SM (1977) Penetrating high-velocity genitourinary injuries. Part I and Part II
Urol 9:371–376 and 493–499
8. Ahlberg A, Corea JR, Sadat-Ali M, Al-Habdan I, Marwah S, Moussa M, Al-Othman A,
Basyuni A (1994) The scud missile disaster in Al-Khobar, Saudi Arabia, 1991: the
orthopaedic experience. Injury 25:97–98
9. Brown RF, Binns JH (1970) Missile injuries in Aden, 1964-7. Injury 1:293–302
10. Barros D’Sa AAB, Hassard TH, Livingston RH, Irwin JWS (1980) Missile-induced
vascular trauma. Injury 12:13–30 and Whitfield C, Garner JP (2007) The early
management of gun shot wounds: Part II, the abdomen, extremities and special
situations. Trauma 9:47–71
11. Beavis JP (2005) Ballistic missile injuries in the siege of Sarajevo 1992–1995. Ballistic
Trauma Sect 4:569–575, Springer Verlag doi:10.1007/1-84628-060-5.29; Beavis JP (2002)
Some medical consequences of siege warfare in a modern city, Sarajevo 1992–1995. Diss
Dipl Med Care Catastrophes Soc Apothecaris and Salihefendic R et al (1997) Sarafix,
external fixator in the treatment of extensive war injuries of limbs. Proc Br Trauma Soc;
Injury 28:242–243
12. Prevezas N (2007) Evolution of pelvic and acetabular surgery from ancient to modern
times. Injury 38:397–407

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28 2 The Pelvis at War

13. Tile M, Hearn T, Vrahas M (2003) Biomechanics of the pelvic ring, Ch 4: 32–45. In: Tile
M, Helfet DL, Kellam JF (eds) Fractures of the pelvis and acetabulum. Lippincot Williams
and Wilkins, Philadelphia
14. Tile M (2003) Describing the injury: classification of pelvic ring injuries. Ch 12:130–167.
In: Tile M, Helfet DL, Kellam JF (eds) Fractures of the pelvis and acetabulum. Lippincot
Williams and Wilkins, Philadelphia
15. Barla J, Powell JN (2003) Open pelvic fractures. Ch 17: 321–328. In: Tile M, Helfet DL,
Kellam JF (eds) Fractures of the pelvis and acetabulum. Lippincot Williams and Wilkins,
Philadelphia and Palmer S, Fairbank AC, Bircher M (1997) Surgical complications and
implications of external fixation of pelvic fractures. Injury 28: 649–653
16. Moed BR, Kellam JF, McLaren A, Tile M (2003) Internal fixation for the injured pelvic
ring. In: Tile M, Helfet DL, Kellam JF (eds) Fractures of the pelvis and acetabulum.
Lippincot Williams and Wilkins, Philadelphia

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Chapter 3
The Birth Canal

Females have a curved tubular birth canal, as contrasted with most other mam-
mals. Its sections can be different, flatly formed or roundish and together with its
curved pathway, it has direct consequences for the fetal labor process. Birth is a
uterus affair. (Its pelvic vessels are organized in shunts to deliver still oxygen
during birth stress.) Its surrounding pelvic structures contribute to a safe envi-
ronment for development and guarantee oxygen and nutriments.

3.1 Evolution

Half way the 1980s, two articles appeared on the pelvis as a passageway by
D. B. Stewart, at that time an emeritus professor at the Brandon University in
Canada. Due to a university sabbatical leave, he could work on pelvic evolution
and adaptations, while in the second article, he concentrated on the modern human
pelvis [1]. At the start of this chapter, we will follow his setup and extend it with
recent views.
To begin with, a series of salient statements can be found in the articles: ‘‘We
have all been through it—the bony pelvis that is—unless like Macduff we were
‘from our mother’s womb untimely ripp’d’. The art of obstetrics developed
because of the concatenation, in man, of a curved tubular birth canal and a bulbous
ovoid fetal head, and the consequent complex mechanism of the descent of the one
through the other. It is interesting to speculate about how we got into this pre-
dicament: and about what may happen in the future, if our species has one’’ [1].
These sentences give in a nutshell the problems to be encountered.
How did a curved tubular birth canal originate? For the answer to this question,
we take first an evolutionary path. The anthropoids comprise two evolutionary
lines that attract our attention: the Australopithecines and the hominids. The fol-
lowing citation ‘‘Also, physical anthropologists should be aware that not all pelves
are ‘standard ones’…. For example, in a scholarly study of some Neanderthal
pelves, the fragments seem to have been reconstructed by comparison with a
recent British pelvis, which from its measurements seems to have been grossly
abnormal’’ [1] demonstrates that anthropologic studies should be approached with

E. Marani and W. F.R.M. Koch, The Pelvis, 29


DOI: 10.1007/978-3-642-40006-3_3,  Springer-Verlag Berlin Heidelberg 2014

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30 3 The Birth Canal

care, again stressed in the following example. The hominoid remains, called Lucy
and found in Ethiopia in 1974, were considered to be female remnants. However,
this long held opinion has been confronted with the view that Lucy is rather a
Lucifer. Anthropologists still dispute the sex of these remains [2–4]. So, pelvic
dimorphism (male or female?) can be hard to establish in fossils even nowadays.
The meaning is clear; one should read this part with caution, mistakes made by
anthropologists, that will come out later, are included!
There are few pelvises of Australopithecus that can be used for reconstruction,
due to the absence of several pelvic parts in the remnants (Fig. 3.1). In the liter-
ature, the left hip bone and other remnants of the pelvis of Lucy [2] and the
Sterkfontein ‘‘complete’’ pelvis [4A] are used. By means of mirror imaging, a
whole pelvis of Sterkfontein can be obtained [4A] and compared to earlier con-
structions of Lucy. The birth canal has been measured in humans and a subdivision
generally accepted is round (gynecoid), narrow (anthropoid), flat (platypelloid),
and shield-shaped (scutiform or android) that concerns the form of the hole that is
enclosed by the bony pelvis (Fig. 3.2).
One should note that damage is also present in the ‘‘complete’’ pelvis. There-
fore, ‘‘We chose the best preserved right hip bone to be completed using the left
one’’ and ‘‘the sacrum may be completed by mirroring’’ [4A] (see Fig. 3.1a,
stippled areas are completed areas; by the way, note the remarks on symmetry in
Sect. 5.2). The outcome of the 3D reconstruction of the Australopithecus pelvis is
shown in Fig. 3.1b. The reconstructed pelvis illustrates: ‘‘a very broad pelvis at the
level of the iliac blades and a large biacetabular diameter’’ [4A], a broad sacrum, a
less posterior tilted pelvis, a small sacral contact with the ilium, and the pelvis was
of the flat type (platypelloid).
Now, the question arises whether one can base female or male typing of a pelvis
on one or two specimens. Moreover, the sexual dimorphism of the pelvis has been
related to the dimensions of the birth canal. More precisely ‘‘species giving birth to
relatively large newborns share a suite of pelvic dimorphisms’’ [3]. In Chap. 1,
already, the large pelvic width in the Pleistocene pelvis was related to large babies
by the cited authors. The hypothesis for the relation between cranium of the fetus
and the pelvic inlet is seemingly affirmatively answered: ‘‘It is demonstrated that
the degree of selective pressure for enlargement of the female pelvic canal to
ensure successful delivery is mainly dependent on the relationships between cra-
nial dimensions of the fetus at term and corresponding dimensions of the female
pelvic inlet. These relationships are dependent on two main factors: (1) size of the
fetus at term relative to the size of the mother, and (2) degree of encephalization at
birth’’ [4]. This seems logical.
Nevertheless, a large study on 156 male and 172 female non-human primates of
six different species (nearly 60 per species: 30 male and 30 female) and 479 male
and 438 female human pelvises was carried out by Robert Tague to answer the
question on the relation between large baby heads and dimorphism. In his results,
he says: ‘‘the results suggest that the species in this study that gave birth to
relatively large newborns do not share a suite of pelvic dimorphisms’’ [3]. In the
discussion, it is repeated in other words: ‘‘therefore the hypothesis fails to be

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3.1 Evolution 31

Fig. 3.1 Reconstruction of


Australopithecus africanus
pelvis by Sterkfontein
remnants: a The various parts
of the Sterkfontein pelvis
selected, mirrored, and placed
on the original fossil and
represented on the pelvic
reconstruction (anterior
superior view). L left side;
R right side. b Reconstructed
pelvis from above (A), the
front (B) and the back (C)
(Reproduced with
permission, figures are taken
from Berge and Goularas
[4A])

supported that interspecific commonalities in pelvic dimorphism are closely


related to obstetrics.’’ There are shared patterns in pelvic dimorphism, but they
could not be converted to phylogeny or body size, due to the fact that even more
non-human primate pelvises are needed. Thus, for the moment, the sexual
dimorphism of the human pelvis can hardly be related to the big heads of the
babies, although supported by several other authors. In all studied species the
posterior inlet of the pelvis is highly dimorphic, implying that for all species extra

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32 3 The Birth Canal

Fig. 3.2 The relations


between diameters and pelvic
typing (figure reproduced
with permission from
Lohman and Ten Donkelaar
[14])

space is organized in the female pelvis to let the fetus enter the birth canal.
Moreover Australopithecus fulfilled the same characteristics as other anthropoids
if the Robert Tague’s calculations are applied to the pelvis of Australopithecus [3].
This characteristic of the posterior inlet, therefore, is not typical human, inde-
pendent of the size of the cranium of the baby.
It looks odd, but even human pelvic organ prolapse has been explained by the
evolution of the female pelvis [5]. The reasoning is as follows: bipedal posture
changes the function of the pelvic diaphragm muscles, but also the form of the
bony pelvis. For the bony pelvis, it concerns enlargement of the human ilia, due to
change of the function of the gluteal muscles, and increase in the sacrum width.
The consequence is that the area of the pelvic diaphragm and pelvic inlet increased
(see Chap. 1). ‘‘Modern women who have a smaller transverse inlet diameter of the
pelvis and a smaller pelvic floor area have been shown to have lower rates of
prolapse in a study using computed tomography pelvimetry’’ [5], but a more
difficult delivery! African American woman (see Chap. 1) also have a smaller
pelvic floor compared to European American women, and this is correlated to
lower rates of prolapse [5]. Lumbar lordosis also is involved. Less lumbar lordosis
tilts the pelvis less down and the pelvic diaphragm has to support more the pelvic
viscera and will have less support of the pubic bones. Evolution toward bipedal
motion has increased the lumbar lordosis. Evolution also increased the connective
tissue compartment in the pelvic diaphragm. The perineum is according to authors
a ‘‘uniquely human adaptation’’ [5], and of course, the adaptation of the tail
muscles into pelvic diaphragm support is part of the evolutional direction toward
bipedal lifestyle.
Macaca monkeys are known for prolapse and are used in prolapse experiments,
and prolapse is sometimes noticed in Gorilla too. Their pelvises are elongated and
their pelvic diaphragms are relatively smaller. The lumbosacral angle is nearly
absent in monkeys and apes (0–30o versus around 90o in humans) indicating that
abdominal muscles will take over the support of the pelvic viscera, but still there is
prolapse. So, there are as many arguments in favor as there are against female
pelvic evolution causing high rates of prolapse.

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3.1 Evolution 33

It all has to do with comparison. It is clear that the comparison between human
pelvises and pelvises of fishes asks for restrictions in the comparison. It all con-
cerns whether things are more similar or less similar and this contains a lot of
subjectivity. Although people are inclined to accept comparisons between pelvises
of humans, monkeys, and apes, still there are restrictions. One of the parameters in
biology is that there should be a common ancestor. Since science still discusses the
ancestral tree of man, one encounters a restriction in the comparison. Homologies
can also be discerned on other criteria, e.g., development. The close relation
between phylogeny and ontology (development from fertilized egg till the death)
is such a parameter (think of Haeckel’s phylogenetic law: embryology is a repe-
tition of phylogeny), but its use gives analogous problems [6]. To cite
S. L. Washburn, an anthropologist from Berkeley University in an honoring article
for R. A. Dart (1893–1988), discoverer of the first Australopithecus (africanus):
‘‘The ‘facts’ of human evolution are so uncertain that it may be best to regard the
study of human evolution as a game, rather than as a science’’ [7]. Thus, the best
one can say is that homologies between humans, apes, and monkeys do not give
ensured information on the birth canal evolutionary development and presumably
also not on human prolapse.
There is one line of argument in relation to evolution of the birth canal that
hardly can be withheld. Dystocia is obstructed labor with the consequence that in
the absence of adequate treatment by the obstetrician, the baby will die. Its rea-
soning is as follows: ‘‘For the practicing obstetrician with an interest in evolution,
the existence of dystocia presents a vexing problem—from an evolutionary point
of view, dystocia should not occur. Evolution is essentially survival of the most
reproductively. A tendency to difficult labor would, therefore, have a strong
negative pressure of selection in premodern times and should be very rare. Yet, it
is widely accepted that human childbirth can frequently be lengthy, difficult, and
possibly dangerous. Obstetricians know that many patients and their infants would
undoubtedly die without access to cesarean delivery to relieve obstructed labor.
How then can the frequency of dystocia in our society be explained from an
evolutionary point of view?’’ [8].
There are populations on earth that have a low percentage of obstructed labors
and others with high percentages: hunter-gatherers (Inuit are given as an example)
have low prolapse percentages (1.6 %) [8] and the province Winnipeg for the
teaching hospitals 10.5 % [8]. The solution is found in the adaptation to food,
using far more arguments in the article than given here. Hunters still have the
evolutionary developed food habits, while North Americans have a crop-deter-
mined feeding pattern. The pelvic evolution to adapt to this fast change from
hunting food via simple agriculture food to modern diet is too slow with the
consequence of dystocia. Parallel to hunters and simple agriculture food (ten
thousands of years ago), together with agriculture population increase inducing
diseases, a low average birth weight was present. The consequence was that the
pelvis could fulfill its function: nearly no obstructed labor. The pelvis is then too

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34 3 The Birth Canal

spacious and starts an evolutionary relative reduction in size. The modern nutrition
brings babies with higher birth weight and the pelvis is still evolutionary reducing
its size with the consequence of dystocia.
To cite the author, ‘‘We are poorly adapted to the affluence of modern diet. This
is attributed in large part to our legacy of relatively poor nutrition over the past
several thousand years on an agriculture-based diet. The greater degree of agri-
culturalization in individuals’ backgrounds, the less well adapted they are to a
modern affluent diet, and, therefore, the more likely they are to suffer dystocia in
an affluent society’’ [8].
Since pelvic evolution is a multi-variant process, one should be astonished if
only one change in condition could explain the pelvic evolution or evolution of the
human birth canal and thus dystocia.
The reverse argumentation concerns studies going back to Turner (see Chap. 1)
and summarized by Steward [1]. Above the four types of pelvises discerned were
summed up. Turner’s pelvic brim or index is at the base of these pelvic types. The
brim was calculated as antero-posterior pelvic diameter divided by the transverse
pelvic diameter and multiplied by hundred. Figure 3.2 shows the four different
pelvic types that originated from the three originally discerned by Turner and
expanded to four by others.
Turner’s ‘‘brim index stood the test of time, because it is expressed in relative
terms so that it is applicable to pelves of every size from dwarf to giant’’ [1].
Pelvic absolute size is related to body size and body size is genetically determined,
but environmental factors also influences the pelvic size as was detected by Baird
from the Aberdeen Maternity Hospital [1]. He noticed that difficult labors were
more common in women originating from social low class than in higher classes.
Lower class women mostly had small body height and they had the most difficult
labors. Difficult labors were clearly more absent in tall women most present in
higher classes. Moreover Baird found more flat brims (platypelloid) among the
small women. A relation with nutrition of the lower class women could not be
established with certainty. Nevertheless, ‘‘faulty bone development and growth
retardation were probably due to several factors including deficiency of calcium
and vitamin D. Probably, the flat pelvis develops as a result of subclinical rickets at
the toddler stage, when the child often misses its step and sits down hard. The body
weight transmitted through the lumbar vertebrae pushes the sacral promontory
downward and forward, and the pelvic side walls bow outward to compensate’’
[1]. The deformation of the pelvis into a flat one also includes more horizontal
position of the sacrum, increasing the lordosis and its consequences has been
described above. An analogous reasoning is held for decalcification resulting in,
e.g., the android type of pelvis.
The unsaid conclusion is that most types of pelvises discerned can be explained
by the pressure of environmental factors that changes one general type of the
human pelvis and thus the human birth canal.

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3.2 The Human Birth Canal 35

3.2 The Human Birth Canal

3.2.1 Abortion

The vision on pregnancy has been changed during the last century and as a
consequence the vision on the human birth canal has also changed. Medical sci-
ence developed techniques for prevention of fertilization and for abortion that do
have low risks, and as a consequence, one knows that safe manipulation of the
genital system, whether by medication or operation, is assured. In the Netherlands,
with 11 abortions per 100 pregnancies in 1980, it increased toward 15 in 2005. Still
the use of birth control, with a good distribution, good insurance, and a higher use
by women, induces a reduction in abortion. There exists interplay between pre-
vention and abortion. Delay in the acceptation of a liberal abortion law is mainly
organized by christen-democratic political groups. Nevertheless from 2000 on,
most (not all) West European countries do have a liberal abortion law, independent
of religious political pressure [9]. One of the unsaid arguments for acceptation is
the reliable morphological and functional knowledge of the genital system that
makes medical handling in prevention and abortion safe. What of that knowledge
is related to the birth passage way?

3.2.2 Birth Passage Way

The passage way for the fetus at term is curved in the human as compared to the
monkey (Fig. 3.3). The consequence of bipedal motion is a severe lordosis
increasing the angle between sacrum and vertebral column. This causes the curved
pathway in humans. Since the bony pelvis is covered with tissue, the passage way
itself is smaller than the one calculated for only the bony pelvis. During delivery,
urethra, bladder neck, bladder, rectum, levator ani, the urogenital diaphragm, and
obturator internus muscle all are in the pathway of the passing child.
At forehand, it is too simple to say that there is a causal relation between
prolapse and urine incontinence with childbirth [11].
Nevertheless, imagine the following situation: at the start of the twentieth
century, the large families with up to 13 children indicate that women had a very
high amount of deliveries. All the fetuses at term had to pass the urogenital
diaphragm for vaginal delivery. Let us say that in normal situations, the diameter
of the vagina is 2–3 cm, so the hole in the urogenital diaphragm has nearly the
same diameter. The head and shoulder of the passing fetus is nearly 12 cm [12] in
breath, which is a 4–6 times enlargement. After 13 newborns, one should expect
damage to the urogenital diaphragm, instead of a straight plate. It should become
corrugated and weak. Analogous reasoning can be brought forward for other
structures.

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36 3 The Birth Canal

Fig. 3.3 Main axis of the birth passage way in Macaca (left) and Man (right), reproduced with
permission from Raynal et al. [10]. Copyright (2005) Elsevier Masson SAS. All rights reserved

Nowadays, women ask for a cesarean section instead of a normal delivery to


overcome urogenital diaphragm problems: mainly are considered tearing, sexual
problems, and prolapse or urine incontinence at older age are considered [13].
Another reason is the pain during delivery.
Are these women justified in their concerns?
Incontinence after pregnancy and vaginal delivery varies between 3.7 and
15.2 % according to literature. Higher rates are encountered in a Norwegian study
(EPINCOT study) in which 21 % of the women complained of urine incontinence
after vaginal delivery. Only 8.7 % did have severe urine incontinence. After
cesarean delivery, the percentages were 15 and 6.2 %, respectively. Nullipara has
a lower risk for urine incontinence than multipara do. For nullipara, the cesarean
delivery gives a 3.5, and spontaneous delivery a 4.3 times higher risk of urinary
incontinence [16]. Thus, pregnancy and delivery, whether vaginal or cesarean,
increase urine incontinence in women. The same holds for anal incontinence: after
spontaneous vaginal delivery, it is 8 % and after cesarean delivery 5 % [16]. The
incontinence rate is on average higher in spontaneous/vaginal delivery than in the
cesarean delivery.
Nearly one in twelve mothers with normal deliveries will encounter inconti-
nence (in the families with several children even higher), which is one in twenty
for cesarean delivery (no information was found for several cesarean deliveries by
the same women), but what is the cause? The problem is that a causal relation is
difficult to establish. A series of variables are known to contribute. Here, we
concentrate on the levator hiatus covered by the urogenital diaphragm and the
position of the bladder neck.

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3.2 The Human Birth Canal 37

The difference in vaginal or cesarean delivery is made by the ‘‘stiffness’’ (the


word is not used by the authors, but is our interpretation) of the pelvic diaphragm,
mainly determined by the type of collagen present in the pelvic diaphragm. If the
levator hiatus is more distensible by pressure, vaginal delivery goes on, assuming
of course a suitable bony pelvis. If nearly no distension is present, cesarean
delivery is to be expected. The distension of the levator hiatus increased even up to
6 weeks postpartum, while in women that underwent cesarean delivery, this was
clearly less. At 6 months, the differences are less but still noticeable between both
groups. Moreover, the distension of the levator hiatus was to the right in vaginal
delivery and to the left in cesarean delivery [11]. Since MRI was used in the study,
the urogenital diaphragm itself cannot be seen. Therefore, enlargement of the
hiatus area was measured, but one may expect that it is also the urogenital dia-
phragm weakness that is mirrored in the distension of the levator hiatus.
The other result, indicating an important factor, concerns the position of the
bladder neck. The larger the fetus the more displacement of the bladder neck was
found. Vaginal delivery changed the position of the bladder neck after delivery
downward (lowering the position of the bladder neck can induce urine inconti-
nence). Not earlier than the sixth month after vaginal delivery, the bladder neck
returned to its former position. At cesarean delivery, this was not the case or far
less. Moreover, the rotational ability of the bladder neck in vaginal delivery was
greater [11]. So in women that have vaginal delivery, the bladder neck is less
tightly structured to its surroundings: a consequence of the difference in connective
tissue?

3.2.3 Position of the Fetus During Delivery

It is unknown why the fetal head position during delivery in humans is different
from animals. In animals, the fetus is born with his face toward the mother’s belly,
while in humans, the fetus looks with his face toward the back of the mother.
During the passage through the birth canal, the fetus makes a turn that is
responsible for the altered position in comparison to animals. It also has to flex the
head to pass (Fig. 3.4). The consequence is said that if ‘‘a human mother tries to
assist in delivery by guiding the infant from the birth canal, she risks pulling it
against the body’s angle of flexion, possibly damaging the infant’s spinal cord,
brachial nerves, and muscles. The human adaptation to this challenge is to seek
assistance during birth’’ [12]. So, birth became a human social event and as a
consequence some specialized in helping the mother, hence midwifery and
obstetricians. In animals, the mother can help by bending the baby and grasp it.
Therefore, it is a self-reliant event for the animal mother that retracts socially
during delivery [12].

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38 3 The Birth Canal

Fig. 3.4 Birth mechanisms


in Pan and Homo. The
pictures are depicted as the
‘‘midwife’s or obstetrician’s
view’’ of the head of the fetus
at term passing through the
birth canal. The pelvis is in
the inferior view. The sacrum
is at the bottom and the pubic
bones at the top. Block
arrows show the facial side.
Curved arrow indicates the
flexion of the human fetal
head (reproduced with
permission and changed after
Rosenberg and Trevathan
[12])

3.3 The Uterus During Pregnancy

The uterus constitutes the inner wall of the birth canal together with the vagina. It
is inevitable: the uterus is the working horse during pregnancy. It increases from
6.5 cm length to 31 cm and for the width from 4 cm up to 23 cm. Its contents
grows from around 3–4 cc till 4–5 l, which is an increase of over 100 times, its net
weight increases from 50–70 to 800–1,200 g. It has to increase its musculature,
withstand the fetus’s movements, keep the placenta and has to increase its vas-
cularization for the benefit of the fetus. The cervix together with the lower uterine
part has to withstand pressure and gravity before delivery. And the most important
is that the uterus has to feed the embryo and later the fetus by its blood circulation
via the placenta and umbilical cords. The placenta is out of the scope of the birth
canal and is mainly omitted from this part.
The consequence is that by increasing its volume, the other organs in the
abdomen and pelvis have to make space. The colon with cecum and vermiform
appendix are pushed upwards (Fig. 3.5). Bladder space as well as rectum space is
reduced. Both can hardly move upwards due to their adherences to the pelvic wall
by ligamentous structures. Dilatation of the right kidney and ureter can occur, the
left ones being spared by protection of the sigmoid colon.

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3.3 The Uterus During Pregnancy 39

Fig. 3.5 Uterus before and after pregnancy. Left upper figure fetus nearly at term, 1 placenta, 2
corps of uterus, 3 umbilicus, 4 fetus, 5 amnion, 6 allantois-chorion membrane, 7 cervix, 8 vagina.
Right upper figure Uterus directly after delivery of the newborn: 1 transverse colon, 2 greater
omentum, 3 lower part uterus, 4 bladder, 5 cervix fold, 6 fetal membrane, 7 vagina. Left lower figure
displacement of cecum and appendix during pregnancy, 1 iliac anterior–superior spine, 2 cecum
(McBurney’s point), 3–8 level of cecum and appendix during pregnancy. Right lower figure
retraction of the uterus after delivery, 1 position of uterus directly after labor, 2 few hours after
labor, 3 second day after labor, 4 sixth day after labor, tenth day after labor, which is two fingers
above pubic bones (figures are taken from Kamina [15] with permission of Editions Maloine, Paris)

The physiological increase in uterine smooth muscle or myometrium is just


above the cervix or uterus neck, the part that constitutes the birth canal wall too.
Up to the fourth month of pregnancy, the uterus increases its muscular mass 30
times. The rest of the uterus increase is found in reduction in its thickness used for
lengthening of the wall. Wall thickness starts at 2 cm and reaches 3 cm at the

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40 3 The Birth Canal

fourth gestational month. After that month, it decreases and reaches 1 cm thick-
ness (0.4 cm at its neck) at delivery. Up to the third month, the uterus remains in
the pelvic cavity. From the third month onward, the top of the uterus growth above
the level of the pubic bones increases by 4 cm each month [15]. There is an
increase in the debit of the blood passing from 50–100 ml/min to 500–800 ml/min
(increase of nearly 10 times), but diminishes after the sixth month [15].
During delivery, the uterus has to organize its contractions in such a way that
expulsion of the fetus of 5–9 pounds occurs: has to open up actively (and partly
passively) the cervix and guide the fetus into the vagina.
Its feat of strength still has to come: readaptation to the natural situation. It has
to expulse the placenta and fetal membrane rests to overcome persistent blood loss
and infection (Fig. 3.5). It has to absorb the extra muscular tissue and reduce the
increased amount of blood vessels. Twelve days after the delivery, it is back within
the pelvic cavity (Fig. 3.5), but has not restored its endometrial proliferation till
25 days after the delivery. In 6 days, it reduces its length by half, reaching natural
form not earlier than nearly the sixth week after delivery [15]. A 9 month growth is
reduced totally within 5–6 weeks. That is a 6–7 times faster reduction compared to
the growth of the gestational uterus.
The muscular construction of the uterus shows the following arrangement from
outside to the inside: in its upper part a thin layer of longitudinal fibers, a circular
layer, than a layer of blood vessels with small muscular bundles through it, and at
the inner side again circular smooth muscle bundles. The lower part contains
thicker longitudinal muscular fiber bundles. Toward the cervix, the amount of
muscular bundles diminishes and collagen containing connective tissue increases,
especially in the cervix.
The construction of the area that will form the entrance of the birth canal is
twofold: the cervix has that high collagen connective tissue content (70–95 %) and
the lower part of the uterus is mainly made of longitudinal and circular smooth
muscular bundles with blood vessels in the middle. Now, one can understand that
the base of the uterus can withstand the pressure of the fetus. However, a ring of
collagen and contracted circular muscular bundles can hardly open by itself as
needed during delivery. Relaxation of the circular bundles in itself does not
organize opening of the closed ring of muscular bundles.
The cervical collagen containing connective tissue changes during pregnancy.
Collagen is reduced by nearly 70 %. Sulphated glycosaminoglycans also a sub-
stance that characterizes connective tissue is lowered in pregnant women [17]
toward the end of pregnancy. This process of changing properties of the cervical
connective tissue is called ripening. A whole battery of processes is involved in
this ripening: a process controlled by nitric oxide (a gaseous neurotransmitter)
[18], ripening should be an inflammatory process, mediated by cytokines (inter-
leukins) [19], metalloproteinases contributing to destruction of collagen and to the
cervical reconstruction [20]. Hormones are also involved: estrogen stimulates the
process and progesterone inhibits ripening. At the muscular side, less active
uterine musculature has to be changed into a ‘‘vigorously active state.’’ Muscle
fibers are grouped in bundles of 20 up to 100 fibers, which form a coordinated

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3.3 The Uterus During Pregnancy 41

muscle unit, normally steered by one neuron. Here, ganglia and spinal cord are
involved. Contraction of longitudinal muscle bundles will not bring the fetus into
the vagina. Therefore, the extra longitudinal bundles that go from the lower part of
the uterus into the vagina are reinforced. It is the pressure of the weight of the fetus
together with the longitudinal muscular force that opens up the circular muscle
bundles at the bottom of the uterus: all these actions constitutes the entrance of the
fetus into the birth canal.
The average time of delivery in nullipara is between 6 and 20 h and in mul-
tipara between 3 and nearly 10 h [21]. The cervical wall and fetus cannot survive
so long without oxygen or feeding. Therefore, a solution is needed that overcomes
the pinching of the blood vessels. ‘‘The growth, development, and regression of
blood vessels are all key features of reproduction. It is for this reason that the study
of uterine microvascular structures has spanned several centuries using a variety of
techniques’’ [22]. From the 1750s onward, a steady stream of publications con-
tributed to the nowadays understanding of the blood vessels in the uterus. The
most difficult part was the endometrium with its changing situation during the
female cycle and the placental blood vessels. On both lateral sides of the uterus, an
artery ascends (a.uterina) from below and one descends from the top (a. overica)
meeting each other’s bed on two-third of the uterus where they anastomose. The
two-third made by the uterine artery. At regular places, arteries intrude into the left
and right half of the uterus wall. Here, they produce circular arteries that occurs
mutually and they meet each others bed. These arcuate arteries penetrate into the
myometrium (the muscular part of the uterus). The arcuate arteries are the origin of
the radial arteries, on their way to the lumen of the uterus. At the border of the
myometrium and endometrium, they form basal arteries, along the border that give
of new branches into the endometrium. These branches are called spiral arteries
due to their coiling (Fig. 3.6). During their journey through the endometrium, they
narrow nearly halfway, divide in smaller branches, and make a capillary network
or plexus around the uterine endometrial glands. Characterized by a large quantity
of smooth muscle cells, they are also richly innervated. The blood vessels, espe-
cially the spiral arteries, starting in the myometrium determine the blood flow
toward the endometrium. Presumably, they also are responsible for the induction
of the menstruation [23].
It is an extensive description, but we need it to understand what happens during
pregnancy and delivery. The first thing that happens during pregnancy is the loss
of the blood vessel’s muscles and also the elastic layer around them. This is
induced by the embryo surrounding protective tissue: the throphoblast. Their cells
penetrate deeply into the myometrium and change the structure of the blood
vessels they reach, even the deepest arcuate arteries. The result is serious dilatation
of the vessels. At the myometrial border and in the starting placenta, a fourfold
increase in diameter is organized. ‘‘By mid-pregnancy, the diameter of the arcuate
arteries exceeds that of the (already doubled in diameter, addition ours) uterine
vessels and by term some are twice the diameter’’ [23]. The systole in the uterine
artery is higher than the one in the arcuate artery, which is a serious pressure drop.
Moreover, anastomoses are organized between the arterial and venous beds in the

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42 3 The Birth Canal

Fig. 3.6 Distribution of the uterine blood vessels (see text), reproduced with permission from
Pijnenborg et al. [23]

myometrium. Everything is organized to facilitate vasodilatation in the uterus


wall, although vasoconstriction stays possible. Special shunts between vessels are
organized around and beneath the placenta. This all leads to reduction in the
systemic vascular resistance and pressure. Compare it to an inflated children’s
plastic bath or plastic ball, if strongly overblown, any sharp thing will easily
damage it (you noticed it of course during holidays), less puffed up it can with-
stand it. Less resistance makes flow simpler. So, any contraction of the uterus or
movement of the fetus will hardly influence the placental or uterus wall’s blood
circulation.
In the French literature, an extra mechanism is repeatedly indicated, being
nearly totally omitted in the Anglo-Saxon publications. Within the blood vessel
layer, in which the arteries are surrounded by a venous plexus, the smaller muscle
fiber bundles do adhere to the blood vessels. This organization (called ‘‘ligatures
vivantes de Pinard’’) should overcome bleeding during delivery. Uterine muscular
contractions, will by the muscle fibers, diminish the lumen of the vessels, lowering
their blood volume even making the vessel less inflated [15]. However, over-
contraction will organize bleeding of course. The idea comes from Adolphe Pinard
(1844–1934) a French surgeon and obstetrician [24]. He developed a fetal
stethoscope [24] and was the first who proved that physical activity at the end of
pregnancy by working-class mothers influenced ‘‘birth weight, stillbirth rate, and
neonatal mortality’’ [25] negatively. Therefore, Pinard, one of the exponents of the
starting maternity services in Paris, introduced the maternity leave, which is now
installed in all Western countries [24].
We now know its cause: ‘‘during exercise, there is a massive reduction in
vascular peripheral resistances and a decrease in blood volume. In animals, a drop

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3.3 The Uterus During Pregnancy 43

in blood pressure is prevented by an increase in the cardiac output. In upright man,


however, this reaction does not seem to be able to maintain blood pressure pre-
sumably as a result of an inefficient venous return limiting the cardiac output. At
all events, it is associated with a visceral vasoconstriction (thus also the uterus,
addition ours) mediated by the sympathetic system. Comparative evidence sug-
gests that this reaction does not protect the pregnant uterus: in experimental ani-
mals, utero-placental blood flow is depressed by sympatheticometic drugs’’ [25].
Thus, although blood pressure and resistance are low and the flow is high in the
uterus, and the body will do everything to help the pregnant uterus to get more
blood, the needed vasoconstriction due to exercise will deprive the uterus from
enough blood. Seemingly, there are still physiological conditions in which the
pregnant uterus cannot coop with circumstances, of which hard work at the end of
pregnancy is the ‘‘best’’ known.
Back to labor, strong uterus contractions are needed to bring the fetus through
the birth canal and to expel the fetus to become a newborn. One should notice the
following: serious postpartum bleeding is the first cause of maternal death in the
world, 140,000 a year, which is one woman each 4 min [26]. In France, it is 30 %
of death cases, and in 80 %, it is judged to have been unnecessary [26]. Its
incidence is in France 6.7 on 1,000 deliveries. Only a multidisciplinary approach
during delivery will reduce the incidence which is now compelled by clinical
‘‘recommendations’’ in France. It is the ‘‘ligatures vivantes de Pinard’’ that is also
responsible for the mechanical hemostasis of the placenta vessel bed as a conse-
quence of the uterine retraction within the first 24 h [26].

3.4 Pelvic Blood Vessels

Blood vessels play an important role in delivery as we have seen. The amount of
blood in the uterus increases before delivery with nearly 40 % [26], so to say an
extra amount of oxygen and both the fetus and birth canal wall can go over to a
more anaerobe metabolism directly before delivery as measured by the lactate
production [27]. There is one more shunt that will help. The uterine artery also
provides blood for the vagina and there exists vaginal-uterine anastomoses.
Although anatomy already discovered them, its importance became noticed due to
vaginal progesterone administration for hormonal replacement therapy. The pro-
gesterone was selectively distributed into the uterus. The amount of progesterone
taken up by the vagina and delivered to the blood circulation showed that the
progesterone concentration was significant lower in the blood circulation than in
the uterus tissue soon after administration. Therefore, a ‘‘portal system’’ flowing
from vagina toward the uterus is presumed beside direct diffusion and passage
through the lumina of vagina and uterus. The explanation however is mainly on the
involvement of arteries and venous plexuses. Normally, the direction is from artery
toward the venous plexus. The other way from venous plexuses toward arteries is a

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44 3 The Birth Canal

Fig. 3.7 Venous plexuses around the uterine artery and its branches toward vagina and uterus,
figure is from Corning et al. [28]

countercurrent transport. Since the branches toward vagina and uterus of the
uterine artery are surrounded by a venous plexus (Fig. 3.7), the possibility of
countercurrent transport exists, in which substances taken up by the veins will leak
toward the artery and be taken up into the artery [28]. Next, the uterus lower part
and cervix contain a serious lower amount of arteries, but an abundant venous
plexus [15]. Therefore, two systems can still bring in oxygen during delivery and
other substances, due to the countercurrent stream and the connections between the
venous plexuses of vagina and uterus. Note that in the pregnant uterus, venous-
arterial anastomoses exist (see above). A partial escape route is present during the
delivery for the birth canal wall and the uterus to obtain oxygen and feeding.
Do the blood vessels of the uterus give us more information? ‘‘The degree of
atherosclerosis in uterine and cardiac vasculature are closely related. Examination
of the uterine vessels at the time of hysterectomy (removal of the uterus, addition
ours) might therefore indicate that individual’s risk of death from ischemic heart
disease’’ [29]. The answer is affirmative for the arcuate artery!

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Literature 45

Literature

Literature has been grouped in reference lists of several chapters in those cases where
arguments are difficult to entangle or published over several articles or books. In cases of
citation the article or book involved is indicated by the reference number together with a
capital Arabic letter.
1. Stewart DB (1984) The pelvis as a passageway. I. Evolution and adaptations; II The
modern human pelvis. Br J Obst Gynaecol 91:611–617; 618–623
2. Häusler M, Schmid P (1995) Comparison of the pelves of Sts 14 and AL 288-1:
implications for birth and sexual dimorphism in australopithecines. J Hum Evol
29:363–383; Tague RG, Lovejoy CO (1998) AL288-1—lucy or lucifer: gender
confusion in the pliocene. J Hum Evol 35:75–94
3. Tague RG (1991) Commonalities in dimorphism and variability in the anthropoid pelvis,
with implications for fossil record. J Hum Evol 21:153–176
4. Leutenegger W (1973) Functional aspects of pelvic morphology in simian primates. J Hum
Evol 3:207–222
4A. Berge C, Goularas D (2010) A new reconstruction of Sts 14 pelvis (Australopithecus
africanus) from computed tomography and three-dimensional techniques. J Human Evol
58:262–272
5. Schimpf M, Talikangas P (2005) Evolution of the female pelvis and relationships to pelvic
organ prolapse. Int Urogynecol J 16:315–320
6. Dullemeijer P (1974) Concepts and approaches in animal morphology. Van Gorcum & Co,
Assen
7. Washburn SL (1973) The evolution game. J Hum Evol 2:557–561
8. Roy RP (2003) A Darwinian view of obstructed labor. Obstet Gynecol 101:397–401
9. Need A (2010) Kiezen in context. Fertiliteitsbeslissingen in West Europa vanaf 1960.
Oratie, Universiteit Twente
10. Raynal P, Le Meaux J-P, Chéreau E (2005) Anthropologic evolution of women’s pelvis.
Gynécol Obstét Fert 33:464–468
11. Toozs-Hobson P, Balmforth J, Cardozo L, Khullar V, Athanasiou S (2008) The effect of
mode of delivery on pelvic floor functional anatomy. Int Urogynecol 19:407–416
12. Rosenberg K, Trevathan W (2002) Birth, obstetrics and human evolution. BJOG
109:1199–1206
13. One should look into Google for ‘‘women ask for caesarian section’’. It is unfeasible to cite
the main ones, due to their amount
14. Lohman AHM, ten Donkelaar HJ (1997) Klinische anatomie en embryologie.
Wetenschappelijke Uitgeverij Bunge, Leiden
15. Kamina P (1995) Petit bassin et périnée. Tome 2, Maloine, Paris
16. Tunn R, Peschers U (2005) Birth trauma and incontinence. In: Becker et al (eds.) Urinary
and fecal incontinence II, pp 87–93. doi:10.1007/3-540-27494-4-6
17. Gramström L, Ekman G, Ulmsten U, Malmström A (1989) Changes in the connective
tissue of corpus and cervix during ripening and labor in term pregnancy. Int J Obstetr
Gynecol 96:1198–1202
18. Chwalisz K, Garfield RG (1998) New molecular challenges in the induction of cervical
ripening. Human Reprod 13:245–252 (Debate)
19. Senneström MB, Ekman G, Westgrun-Thorsson G et al (2000) Human cervical ripening,
an inflammatory process mediated by cytokines. Mol Human Reprod 6:375–381
20. Stygar D, Wang H, Vladic YS, Ekman G, Eriksson H, Sahlin L (2002) Increased level of
matrix metalloproteinases 2 and 9 in the ripening process of the human cervix. Biol Reprod
67:889–894
21. Schaepman-van Geuns EJ (1973) Praktische verloskunde. De Erven Bohn, Amsterdam

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46 3 The Birth Canal

22. Manconi F, Thomas GA, Fraser IS (2010) A historical overview of the study and
representation of uterine microvascular structures. Microvas Res 79:80–89
23. Burton GJ, Woods AW, Jauniaux E, Kingdom JCP (2009) Rheological and physiological
consequences of conversion of the maternal spiral arteries for uroplacental blood flow
during human pregnancy. Placenta 30:473–482; Figure 3.6 from Pijnenborg R, Vercruysse
L, Hanssens M (2006) The uterine spiral arteries in human pregnancy: facts and
controversies. Placenta 27:939–95
24. The late Prof. Pinard. The Lancet 223:5769: p 644, March 24, 1934; Fell MR (1956) A
modified Pinard’s foetal stethoscope. The Lancet. Aug 11
25. Briend A (1980) Maternal physical activity, birth weight and perinatal mortality. Med
Hypotheses 6:1157–1170
26. Ducloy-Bouthorst A-S, Blondè-Zoonekijnd E, Jaillete E et al (2007) Prise en charge d’une
hémorragie du post-partum. Reanimation 16:373–379; Ducloy-Bouthorst A-S, Blondè-
Zoonekijnd E, Jaillete E et al (2010) Transfusion and postpartum haemorrhage. Transf Clin
Biol 17:273–278
27. Schneider H, Danko J, Huch R, Huch A (1984) Homeostasis of fetal lactate metabolism in
late pregnancy and the changes during labor and delivery. Europ J Obstet Gynec reprod
Biol 17:183–192
28. Cicinelli E, de Ziegler D (1999) New hypotheses: transvaginal progesterone: evidence for
a new functional ‘‘portal system’’ flowing from the vagina to the uterus; Cicinelli E, Einer-
Jensen N, Galantino P, Pinto V, Barba B, Tartagni M (2001) Model of counter-current
transfer from vagina to urethra in postmenopausal women. Human Reprod 16:2496–2500;
Figure 3.7 from Corning HK (1919) Lehrbuch der topographischen Anatomie. 8th ed
Verlag J. F. Bergmann, Wiesbaden
29. Weeks A (2002) Can arcuate artery morphology predict mortality from ischaemic heart
disease? Maturitas 43:21–26

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Chapter 4
History

History is not simply a registration of passing facts. It is the interpretation of the evolution
of mankind and science. From its investigation an insight may be gained into the trends to
be developed in science. Each historical essay is both an evaluation and a selection of
known facts. The history of morphology is no exception; it can provide us with some
conceptual tools for detecting new approaches and new principles. These considerations
may justify a short historical survey of morphology [1].

History shows that most organs, but not their coherence and function, were known
by medieval scientists. The swing-over occurred in Italy in the sixteenth century in
the universities of Padua and Bologna. Due to the dissections of human bodies,
which demonstrated the interrelations between human organs, critical reviews, and
new findings originated. The Dutch seventeenth century research completed the
needed anatomical understanding, but the human bony pelvis was misleadingly
depicted and described by Van Deventer. It is remarkable that these incorrect
pelvic ideas still pertain up until today.

4.1 Historical Panorama I

The pelvis and its pelvic floor have always interested scientists, especially anat-
omists, among which many famous thinkers. In modern times, however, the study
of the genital apparatus of male and female is highly advanced, think for instance
about in vitro fertilization, abortion, sterilization operations for men and women.
Despite this, and however unlikely it may seem, knowledge of the muscles, nerves,
and ligaments of the pelvis and its organs has a low priority in current research.
Urinary and fecal incontinence, a most serious problem for young and elderly
people is, due to lack of knowledge of the normal structure and function of the
pelvis, a poorly understood affliction. Moreover, the layman is badly informed, and
incontinence is still regarded as shameful, which also hinders research.
Over the centuries, little has changed and the same problems were encountered
by famous thinkers who first studied the pelvis for the sake of knowing.
An historical survey of pelvic science starts with the bony pelvis nowadays.
From there on, one can fill in the space with soft tissue structures. In history, it was

E. Marani and W. F.R.M. Koch, The Pelvis, 47


DOI: 10.1007/978-3-642-40006-3_4,  Springer-Verlag Berlin Heidelberg 2014

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48 4 History

Table 4.1 Time-line to place the historical panorama’s of this chapter


Historical Panorama III Historical Panorama I+II
Towards a new anatomical cosmology

1000 1200 1400 1500 1700 1800


Early Translation High Scientific Scientific Revolution Enlightenment Modern Science
Middle period Middle Renaissance
Ages Arabic and Ages
Greek

the other way around. Strong emphasis was on pelvic soft tissues during Middle
Ages and Scientific Renaissance, while the focus on the bony pelvis occurred
during the period known as the Scientific Revolution. Here, we start with the bony
pelvis (Historical Panorama I and II) during the Scientific Revolution followed by
the coincidence of pelvic soft tissue studies (Historical Panorama III) that brought
a new anatomical cosmology (see the scientific periods in the timeline above,
Table 4.1). Moreover, at several places, we abandon the historical approach and
use the anatomical-embryological tactic: going backward in time. Knowing a
structure or fact at older ages makes it easier to follow its development by studying
stage by stage the earlier ones. The method is apt to repeat resistance among
historians, but effective if anatomical structures are considered historically.

4.2 Bladder Stones

In this part, we will consider the history of the treatment of bladder stones [2].
From Roman time onward, the bladder stone became the center of the pelvic
universe. Calculus vesicalis is the Latin name for this affliction. The diet in Europe
up to the twentieth century is held responsible for its prevalence. Erasmus (ca.
1500) had to deal with it. In one of his letters, he describes how he gave birth to a
large stone. Such patients suffered unbearable pain and had trouble urinating.
Some had to shake their pelvis to shift the stones from the urethra entrance before
they could urinate (Fig. 4.1), having to deal with ‘‘labor-like’’ bladder pain in
between. Therefore, one can understand the willingness of bladder stone sufferers
to undergo surgical treatment to remove the stones, whatever the consequences [2].
In principle, there are three methods to remove bladder stones; surgical
removal, crushing the stone and dissolving the stone by chemicals taken orally.
Today, crushing of the stone mechanically is the method of choice, whereas kidney
and ureter stones are preferably treated with shock wave therapy. The fragments
are removed directly through the urethra or by spontaneous evacuation by the urine
in case of upper urinary tract stones. In older days, the surgical removal of bladder
stones was frequently used, an operation already practiced by the Greeks, Romans,
and Hindus before the beginning of our era. Wound infection was totally

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4.2 Bladder Stones 49

Fig. 4.1 Stone cutter at


work. Print from Paracelsus,
Opus chyrurgicum.
Reproduced with permission
of Museum Boerhaave,
Leiden

misunderstood until Semmelweis in the middle of the nineteenth century. The


infection risk of such an operation was therefore high, whatever the skills of the
surgeon.
The bladder can be approached surgically by three routes. One can reach the
bladder over the pubic bones, through the rectum, or via the perineum. The
preference in days gone by was the perineal route. The surgical methods that were
developed can also be subdivided in three types: the method of Celsus, that of
Marianus, and the lateral lithotomy.

4.2.1 The Perineum

The perineum can be considered the last knot that ties the pelvic floor (Fig. 4.2).
It is the closure line of the skin between the anus and the scrotum or vagina, with a
ligamentous extension inward to the pelvis. The muscles of the pelvic bottom all are
tightly bound to this perineal knot that after contraction of the pelvic floor, muscles
will give the perineal shrug. The connection to the perineal body is essential for
this, and the effect of cutting the perineal body as done in lithotomy can easily be
imagined: disruption of the pelvic bottom and protrusion of its pelvic contents.

4.2.2 The Method of Celsus

In his book ‘‘De Re Medicina,’’ Celsus (ca. 25 BC–AD 50) described the simplest
form of lithotomy. In the Middle Ages, his name was attached to this method. The
surgical approach required nearly no sophisticated surgical instruments: only a
knife and a hook called the calculus forceps. A finger was brought into the rectum

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50 4 History

Fig. 4.2 The perineum or


perineal body in its function
to keep the integrity of the
pelvic floor. Reproduced with
permission from
D. B. Moffat, Lecture notes
on Anatomy. Blackwell
Scientific Publications
Oxford

and the stone was fixed against the perineum. An incision was made in the peri-
neum at the place where the stone bulged. The stone could be removed through
this opening. The operation was best carried out in young boys, because their
prostate had not yet fully developed. In adult males, the operation was normally
complicated by the fully developed prostate and seminal vesicles. Fistulas,
incontinence, and serious hemorrhage were common consequences.
In the Middle Ages, the risks involved were so high that physicians and sur-
geons avoided the procedure. Special ‘‘stone cutters’’ traveled through Europe to
perform the operation where needed. Some of them reached a high standard; others
remained charlatans who departed as soon as possible after surgery, to avoid
postoperative treatment, prosecution, or worse.

4.2.3 The Method of Marianus

Mariano Santo (1488–1550) described a new method for removing the bladder
stones. In women, the bladder stones could easily be removed via a dilated urethra.
The urethra in the woman is short. To apply the same technique to men, one had to
open the much longer urethra just in front of the bladder neck. The wound then had
to be dilated to remove the stones. A ‘‘grooved staff’’ was used to indicate the site
of operation and several dilators were needed. The technique was indicated by its
instruments as the Apparatus major, since many instruments were needed. The
Celsus method, in comparison, was called the Apparatus minor.
The intervention was extremely painful, and the rigorous dilatation of the tissues
involved left the patient with severe ruptures, incontinence, fistulas, and impotence.

4.2.4 Lateral Lithotomy

Jacques de Beaulieu (1651–1714), an itinerant stone cutter, used the lateral


lithotomy for the first time (Fig. 4.3). The perineum was incised lateral to the

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4.2 Bladder Stones 51

Fig. 4.3 Jacques de Beaulieu (1651–1714) known for his lateral lithotomy from Gogelein [2],
reproduced with permission of Museum Boerhaave Leiden

midline. Consequently, the bladder and part of the bladder neck were opened. This
all without anesthetics. The operations performed by de Beaulieu were not
unsuccessful. His claim to be a priest and the low fees he charged made him a
reliable person in the eyes of his contemporaries. He discussed his method with
Johan Jakob Rau in Amster-dam. Rau (1658–1719) adopted and improved the
method, as did William Cheselden (1688–1752), who required only sixty seconds
to perform the operation. By the beginning of the eighteenth century, many
variations on the lateral approach had been introduced and the method had spread
through all of Europe except France.
Many other methods to remove bladder stones have been used: The suprapubic
lithotomy, or via an incision in the rectum; lithotrity, crushing the stone, which came
into use at the end of the eighteenth century. All kinds of instruments were developed,
but most of them were never put into use. In 1824, the first crushing of the bladder
stone was carried out in a patient, quickly followed by methods to remove the debris
by expulsion with the urine. Flushing the bladder and suction were the most fre-
quently used systems. The development of cystoscopy brought the lithotomy into the
age of modern medicine, and a surgical approach was not needed anymore.
It is remarkable that lithotomy did not advance research. Pelvic science did not
profit from the empiric approach to the removal of bladder stones.

4.3 Vesalius (1514–1564)

The birth of scientific anatomy in Europe seems easily to be pinpointed. Andreas


Vesalius (1514–1564) is the scientist who changed the tide of the anatomical sci-
ence in favor of a real analysis of the human body [3, 4]. Although not the first (e.g.,
Berengario da Carpi) but he was the best of the new generation and the new
approach. In his opus magnum: ‘‘De humani corporis Fabrica libri septem’’

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52 4 History

Vesalius gave only a superficial description of the internal musculature of the


pelvis, but he paid much attention to the male genital apparatus in the part ‘‘De
musculis penis peculiaribus (XXXXIX).’’ Vesalius describes the distribution of
vessels, including the coherence of the testicular artery and the sperm ducts.
Moreover, the relationship between the sperm ducts at their entrance at the base of
the bladder is correctly presented. The sphincters of the urethra and anus were
known (colli vesicae et ani musculorum administratio LII). The whole urinary and
genital system was basically well described and was dissected as one unit (Fig. 4.4).
The contribution of Vesalius to the knowledge of the bony pelvis as presented
in ‘‘De Fabrica’’ was restricted to pictures of the os sacrum and of the pelvis as a
whole in his human skeleton figures, and to the demonstration of the attachment of
the penis. Although the Fabrica is a turning point in anatomical science Vesalius
avoided an extensive description of the pelvic bones. He did show the bony pelvis
to consist of three bones (Fig. 4.5), os ilium, os coxendicum, and an os pubis, that
were present on both sides of the os sacrum. His text on the os sacrum started with
a discussion of Galen’s vision of structure. Attention was given to the ossi coccyx
as being vertebrae containing holes for the nerves. This description corresponds to
the modern view (Fig. 4.6).
However, the closed bony pelvic ring was not noticed, nor was the presence of a
dorsal and a ventral part of the pelvic ring. A pelvis by itself, with muscle
structures and the membrana obturatum, was depicted in ‘‘De musculis penic
peculiaribus.’’ The viewpoint of the figures, a whole muscle preparation and a
bony pelvis with the penis and anal musculature (his Figs. 4.2 and 4.2, p. 225), is
such that we look into the anal canal. Together with the position of the pelvis in the
side view skeleton (his page 164), it is clear that the bony pelvis is wrongly placed
(both literally and metaphorically).

4.4 Historical Panorama II

In comparative anatomy, the interest in the uropoetic and genital system has
remained prominent. To summarize some vertebrates studied, together with their
scientists: [5, 6] Ruini, 1598, horse; Tyson, 1683, rattle snake; Perrault, 1676,
Indian turtle; Waller, 1693, black rat. However, these studies did not contribute to
the knowledge of the human pelvis which is understandable since these animals
except the snake are all tetrapeds. Man is a biped.
The interest in the human pelvis is another story. Frederik Ruysch (1638–1731)
looked into the differences between the male and female pelvis [6, 7]. Hendrik van
Deventer (1651–1724) studied the form and width of the bony pelvis in the female,
and the pathology of the pelvis (pelvis plana Deventeri), and is considered founder
of ‘‘pelvic science’’ [5]. Bernhard Albinus (1653–1721) studied the pelvic muscles,
while Eduard Sandifort (1742–1814) published a thesis entitled ‘‘Over het bekken
en zijn verwijding tijdens de baring’’ (On the pelvis and its dilation during
childbirth) [5].

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4.4 Historical Panorama II 53

Fig. 4.4 Resection of the urogenital system. a Drawing from Vesalius (1543) showing the ‘‘en
bloc’’ resection of the human urogenital system in the male. b Bidloo’s total resection of the
female urogenital system (1685; T50, with permission of the Leiden University Library).
c Modern resection of the male urogenital system (Courtesy W. Ovtscharoff and K. Usunoff ,
Sofia)

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54 4 History

Fig. 4.5 One half of the pelvis as pictured by Vesalius. The os coxendicum is the area lying
above the acetabulum surrounded by the letters A. S. T.

Fig. 4.6 The os sacrum together with its cocygeal vertebrae taken from Vesalius. Note that the
hiatus was already pictured by Vesalius (1543)

Symphysectomy (bisection of the connection between both pubic bones), as


introduced by the Frenchman Sigauls, was studied by Petrus Camper (1722–1789).
In the nineteenth century, obstetrics and gynecology became specialities in med-
icine. Important physicians in these fields were as follows: in London, William
Hunter (1728–1793) and Percival Pott (1713–1788); and in Paris, Jean Louis
Baudelocque (1746–1810). Later on, Ignaz Phillip Semmelweis (1818–1865)
detected the cause of puerperal fever [5].

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4.4 Historical Panorama II 55

The first half of the twentieth century saw the publication of a number of good
descriptions of the human body including several excellent descriptions of the
pelvis such as Rouvière’s ‘‘Anatomie humaine [8]’’ and part V of Testut’s ‘‘Traité
d’Anatomie humaine [9]’’ (with colored pictures).
To understand what happened during what had to be the turning point for the
pelvic science, one has to consider two Dutch scientists working during the Golden
Age of the Dutch Republic: Van Deventer and Bidloo.

4.5 Hendrik van Deventer (1651–1724): Father of Pelvic


Science

4.5.1 Van Deventer and His Time

To know Van Deventer’s time, we have to go back to the Dutch Golden Age. Here,
we start with Haller’s visit to The Netherlands. The development of Dutch Science,
reaching its summit with Boerhaave, is also characterized during its running start
by extrauniversity research as done by Van Leeuwenhoek and Van Deventer. We
start with Boerhaave and go backward to describe the extrauniversity research of
Van Leeuwenhoek and the consequences for Van Deventer [7A, 10, 10A, 11, 11A].
Haller, born in Bern in 1708, spent most of his active life in Germany. He was
what we nowadays call a ‘‘Wunderkind’’ and went to Leiden to finish his studies in
medicine. Both Boerhaave (the most famous European professor in medicine) and
Albinus junior (the Leiden anatomist) introduced him to the Dutch approach to
science, which was considered to be better than the attitude in Tübingen [5] where
Haller started his studies in medicine. Nearly 17 years old when he arrived. Haller
stayed two years in the Netherlands. He kept a diary, from which the famous
description of Boerhaave’s appearance is regularly cited. In a sense, an exchange
program for students was already working in those days. Unfortunately, this was
only for rich students, as the government of the day did not provide scholarships.
However, the official name for a student was an academic citizen of Leiden, and as
such one was entitled to have nearly 200 l of wine and 12 barrels of beer tax free
[5]. Note that in those days, water was often infected and alcoholic beverages were
the only drinks free from pathogenic organisms. Of course, other privileges were
distributed too. So Leiden attracted many foreign students, both due to the quality
of the university and the privileges the city provided for the students.
Boerhaave had immense success as a teacher. His students published his lec-
tures for him. Haller published the theoretical teachings of Boerhaave: Hermanni
Boerhaave praelectiones academicae in suas Institutiones medicas. Boerhaave
laid emphasis on the great systems of the human body among them the repro-
ductive system [10A]. Haller arrived at the moment Van Deventer’s pelvic results
started to spread over Europe. He does not mention Van Deventer in his diary.
Some decades earlier, another genius Antoni van Leeuwenhoek started working
near The Hague, namely in Delft. Nowadays, we would call him a self-made man,

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56 4 History

as Van Deventer partially was. He had no scientific training. He lived apart from
universities and worked on what he could see through his self-made single-lens
microscopes. Antoni van Leeuwenhoek who lived from 1632 till 1723 (note Van
Deventer’s lifetime) was sent to the Dutch school near Leiden for his education. In
1652 or 1653, he returned to Delft. Besides his own business as cloth merchant,
Van Leeuwenhoek was made chamberlain to the sheriffs of Delft. In 1679, after he
had acquired some mathematical skill, he was elected wine-gauger [12, 13]. In his
forties, Van Leeuwenhoek started manufacturing lenses for his simple microscopes
and began, in 1673, his important and well-known correspondence with the Royal
Society. This correspondence was to last 50 years and was performed outside the
universities.
Thus, the rise of Dutch science was also due to its open organization: research
was not exclusively concentrated in universities. Van Deventer is another example
of Dutch famous extrauniversity investigations and of non-acceptance by aca-
demic colleagues [7A]. One should note that Van Leeuwenhoek’s research was, so
to say, checked and discussed by Royal Society members, while Van Deventer’s
results were published in book form without screening of his results by others.

4.5.2 Van Deventers Life

Hendrik van Deventer (1651–1724) was born in Leiden. His father Hendrick Jansz
was from Deventer, and his mother Lijsbeth Jansdr presumably also from Deventer.
Both moved from Leiden to The Hague, when Hendrik was two years old. In his
youth, Hendrik van Deventer was trained as a goldsmith. However, at 17 years of
age, because of his belief in living humbly, he abandoned this occupation and, by
1672, he had joined the parish of the Labadists in Altona, Holstein. The parish
asked him to educate himself as their doctor. In 1675, the parish of the Labadists
moved to the Thetinga-State in Wieuwerd Friesland. Van Deventer was at that time
the physician of the parish. It should be noted that the parish of Labadists included
important persons, e.g., the flower- and insect- painter Maria Sibylla Merian. In the
region, he was already well known as a physician, and a separate house was bought
to give him a place to minister to those not belonging to the parish. Indeed, Van
Deventer was so well known that the king of Denmark asked his advice regarding
his children who were suffering from rickets. Van Deventer was the cause of the
end of the Labadist community in Wieuwerd in 1692. All profit came from his work
as a physician and chemist and he refused to share his earnings with the other poor
members any longer. Van Deventer did not leave Wieuwerd, but started or was
already working on his thesis around 1692. Whether the reason was his view on a
dissertation or it was the impoverishing of the community that was harmful to his
family is unknown, presumably both [7A, 10, 11].
When he returned to Groningen, he published his doctoral thesis on the first of
November 1694 [7A]. Subsequently, Van Deventer left the Labadist parish and
moved to The Hague. He lived in Voorschoten, between The Hague and Leiden,
and after overcoming the jealousy of his colleagues, he was accepted as a

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4.5 Hendrik van Deventer (1651–1724): Father of Pelvic Science 57

physician (doctor medicinae). For the last half of his life, Van Deventer stayed in
The Hague. It was there that he published his results on obstetrics and on the
anatomy of the pelvis. Van Deventer bought several houses in The Hague and built
his own ‘‘Sionslust’’ in Voorschoten, where he died [11]. Van Deventer has several
claims to fame: a good obstetrician [10], an excellent orthopeadic surgeon [11],
but also a theologian [11].
Although Van Deventer was not connected to a university, he was well
informed about developments in scientific circles. Just what was happening?

4.5.3 Van Deventer’s Thesis

Around 2000, Van Deventer’s thesis was rediscovered in the John Rylands Uni-
versity Library, Deansgate in Manchester. This discovery ended a series of guesses
concerning its lost content. The thesis is tiny, only two small quarto pages. Such a
small thesis was not unusual in The Netherlands. The thesis defense occurred in
Groningen, presumably because there Van Deventer was allowed to use Dutch
during his argumentation. Van Deventer was not able to handle Latin, and
therefore, Groningen can be considered an alternative route to get still a medical
doctor’s diploma. To enter in the ranks of medical doctors, it was profitable to
have a university degree. It was his aim to enter in the medical circles of The
Hague, which turned out to be far more difficult than obtaining a doctors diploma
(see above) [11A].
Its title was Inaugurale positien in de medicine. Opgestelt in form van dispu-
tatie, ter verkrijginge van de doctorale gradus in die Faculteyt. (Inaugural posi-
tions in medicine. Organized in the form of disputations, for obtaining the degree
of doctor in that Faculty.). Such an exam lasted over four days. The first two were
spent on ‘‘ad primaria capita medicinae.’’ We should say two days of testing one’s
medical knowledge. It was followed by a philosophical part: discussion of an
aphorism of Hippocrates or another medical philosophical subject. This was fol-
lowed by a two days ‘‘disputatio de themate medico.’’ Van Deventer started with
the medical exam on October 27, 1694, followed by the explanation of a case ‘‘de
furore uterino’’ on 29th October. The 1st November he defended his twelve
‘‘theses miscellaneas.’’ He finished the exam ‘‘cum laude.’’
It is remarkable that the contents of his positions 6–8 are hardly different from
his arguments in ‘‘Dageraet der vroedvrouwen’’ (1696), ‘‘Manuele operatien’’
(1701), and ‘‘Nader vertoog’’ (1719). Clearly, he had already developed his ideas
during the gynecologic practice as physician for the Labadists in Altona and
Wieuwerd.
Somewhat before the rediscovery of Van Deventer’s thesis, a portrait was
studied by the Netherlands Institute for Art History that was painted by Thomas
van der Wilt (1659–1733, Fig. 4.7) [11A]. After a thorough research, the subject of
the portrait was identified as Van Deventer. One of the arguments is that the
portrait was used for the engraving of the printed portrait in ‘‘Manuele operatien’’

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58 4 History

in the editions from 1719 on. This engraving contained not only the name of the
engraver but also the name of van der Wilt, assuring, together with the striking
resemblance of both portraits, the identification of Van Deventer [11A].

4.5.4 Van Deventer and the Bony Pelvis

Van Deventer was clearly a good anatomist if students in our time cannot even
grasp the structure of the pelvis, how difficult must it have been at the turn of the
eighteenth century. How did Van Deventer arrive at his anatomical expertise?
Van Deventer was deeply interested in obstetrics. In those days, the entry of a
physician into the delivery room, in which a man should not be present during
delivery, indicated that something was badly wrong. His obstetric fame must have
been enormous [11] because he was regularly invited even for normal deliveries.
Van Deventer mostly worked together with midwives. He noticed that the
knowledge of these women, and also of the few male assistants, was miserable. As
a consequence, he wrote a manual for midwives ‘‘Manuale operatiën, zijnde een
nieuw ligt voor vroedmeesters en vroedvrouwen’’ (1701, 1st ed.; 1746, 3rd ed.,
[13] ‘‘Manual operations, being a new light for obstetricians and midwives’’).
It was his pedagogic interest that led him to transfer his knowledge to the
midwives, hoping that they would then carry out their work better. As he put it: ‘‘It
will surprise some people, that I will teach midwives about the pelvis, its bony
structures, and their different appearances. But I must say to them that they should
not think that this knowledge is impractical or unnecessary. On the contrary, I have
determined that this knowledge is not only useful but is essential. Yes, so nec-
essary that without a clear concept of these things, they stumble and are blind, both
in their thoughts and in their hands, when they must help women in problematical
or unnatural deliveries. From this, it must necessarily be concluded that they
cannot practice their craft without a lot of mistakes.’’
Het sal sommigen mogelijk vreemt voorkoomen, dat ik de Vroedvrouwen ga onderwijsen
van het Bekken, deselver Beenderen, en deselver verscheyde formen en gedaantens. Maar
tot de soodanige moet ik seggen, dat sy haar niet moeten inbeelden, dat derselver kennisse
onnut of onnodig is: want het is soo verre daar van daan, dat ik van die gedagte soude
konnen sijn, dat ik in tegendeel vaststelle, dat die kennisse haar niet alleen nuttig, maar
selfs geheel noodtsakelijk is; ja soo noodtsakelijk, dat, sonder een klaar Denkbeeldt daar
van te hebben, sy maar stommelende en blindelings met haar verstandt en ook met haare
handen konnen te werk gaan, wanneer sy Barende Vrouwen in de verkeerde of on-
natuurlijke geboortens moeten helpen; waar uyt noodtsakelijk moet volgen, dat sy haar
werk dan ook niet sonder vele misslagen konnen doen.

Somewhat further on he says: ‘‘but, because I thought the knowledge of the


bones to be genuinely necessary for all those who want to help women in delivery,
I also thought it necessary, as much as possible, to supply them with the necessary
illustrations, and these drawn simply and clearly as possible by a good artist.’’
(Note: the italics are Van Deventer’s).

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4.5 Hendrik van Deventer (1651–1724): Father of Pelvic Science 59

Fig. 4.7 Upper picture The


newly discovered portrait of
Van Deventer painted by
Thomas van der Wilt. ‘‘The
man is wearing a bright
purple silk gown, with a scarf
round his neck and a typically
French wig. The robe itself,
however, is more Dutch than
French. These robes were
called Japanese dress-coats
and were a variation on the
Japanese kimono. The setting
of the portrait is somewhat
unusual, but in the late
seventeenth century the
convention was to reserve
this position, dress and setting
for portraits of scientists,
poets and men of letters’’
(taken from Van der Weiden
[11B]. Reproduced by
permission of Sage
Publications Ltd London etc,
 Sage, 1997). Lower picture
(reproduced with
permission): ‘‘In the first
editions of the ‘Manuale
operation’ van Deventer
included a, rather awkward,
portrait by himself [11B]’’

maar dewyl ik de kennisse deser Beenderen soo wesentlijk nodig agte voor alle de geenen
die ondernemen de Barende Vrouwen te helpen, soo agte ik ook nodig, soo veel als my
doenlyk sal zijn, haar daar van de nodige Figuuren mede te delen en dat soo naakt en klaar
als ik deselven door een goet tekenaar na het leven hebbe konnen laaten verbeelden.

The idea of the narrowed pelvis as the cause of a difficult delivery had already
been put forward in the second half of the sixteenth century by J. C. Arantius, a

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60 4 History

Fig. 4.8 Frontal view of the pelvis taken from Van Deventer [14] (see text), reproduced with
permission of Museum Boerhaave, Leiden

pupil of Andreas Vesalius, but it had been forgotten [11]. The traditional idea that
the pelvic bones should part to make way for the child, had already been denied by
Vesalius [11]. It seems unlikely to suppose that Van Deventer would not have had
knowledge of the ideas of these two scientists, especially Vesalius. That, never-
theless, the idea of the narrowed pelvis as a cause of difficult delivery was renewed
by Van Deventer, must have been due to his enormous practical experience. As a
logical consequence of this concept, the study of the pelvis had to be started.
However, a problem immediately arises for those interested in anatomy. Why
should somebody show a bony pelvis from the front and a side view of half a
pelvis (Figs. 4.8 and 4.9). What is the pelvic knowledge demonstrated in the
figures and text?
The picture of the half pelvis has been recognized by several authors as
abnormal (Fig. 4.9). ‘‘Clearly a rachitic pelvis is used for this drawing as a model
for the artists, because the sharp kink turn in the ventral direction of the lower part
of the os sacrum is pathological [11].’’ It is remarkable that in the complete pelvis
(Fig. 4.8), five foramina, instead of four, are represented, so that the os sacrum is
composed of six sacral vertebrae. To return to the previous remark, the kink in the
half pelvis (Fig. 4.9) is very large, but it illustrates the view of Van Deventer very
well, namely that the delivery canal is determined by the space between the pubic

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4.5 Hendrik van Deventer (1651–1724): Father of Pelvic Science 61

Fig. 4.9 Side view of an half


pelvis taken from Van
Deventer [14] (see text),
reproduced with permission
of Museum Boerhaave,
Leiden

bones and the os coccygis. Van Deventer recommends that the tailbones be pushed
backward if the delivery canal is to small [14] (see also [11], pp. 111–112).
Looking at the general morphology of the pelvis as pictured, it appears to be a
male pelvis, and the left foramen obturatum is disproportional. In its frontal view,
the spina ischiadica is clearly visible on the left side (see f in Fig. 4.8), but not on
the right side. It is clear that the left os ischii has developed too much and is nearly
pathological. Note also the left and right acetabuli, which are unequal. The pelvis
has been drawn from a ventral view point and has not been tilted: ‘‘The first of the
next two figures shows a pelvis straight from the front [14].’’ In the side view, the
right side is drawn, so that there is no confirmation of the deviations on the left, if
indeed, it was the same pelvis.
The asymmetry of the pelvis as a whole is very distinct as can be seen by
covering up one half at a time. The marked increase in thickness of the os ischii, as
drawn and the detailed impressions of the left adductor muscle complex, could
indicate, together with the deeper-placed acetabulum, that a central hipluxation is
present. The fracture line in Fig. 4.8, just below the line f–g, shows that we are
dealing with a central hip luxation, and this is confirmed by the fact that the os
ischii is tilted. The retroversion of the acetabulum could be explained by this, if the
central hip luxation happened at young age.
Most remarkable is the presence of an opening in the body of the vertebra S2
(near C in Fig. 4.8). This can only be explained, for the time period concerned, by
a tuberculous osteomyelitis.
Van Deventer shows the (right) half of the pelvis (Fig. 4.9) because then one
has an unhindered view of the three bones that, together with the bony sacrum,

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62 4 History

constitute the pelvic ring. This again displays his pedagogical shrewdness so that
the midwife obtains the correct knowledge of the form of the pelvis. The only
problem is that the angle between sacrum and bony pelvis is incorrect. The
imaginary line (c–p), the linea terminalis, is normally perpendicular to the pelvis
and not at the angle drawn here. Indeed, it brings the symphysis nearer to the tail
vertebrae. Is this a case of the wish being father to the thought, or was it difficult in
those days to regroup the pelvic bony parts? Since between 1701 and 1708, Van
Deventer was writing the book ‘‘Beschrijving van de Ziektens der Beenderen en in
zonderheyd van de Rhachitis’’ [15] (Description of the illnesses of bones espe-
cially of rachitis), we know that he consciously pictured pathological pelvises.
In conclusion, Van Deventer depicts an entire pelvis that is pathological, with
its bony deviations displaying a central hip luxation and tubercular osteomyelitis.
The pelvis contained six vertebrae, a situation that is infrequently encountered in
the human population. The half pelvis is a rachitic pelvis and is wrongly recon-
structed from its separate parts.

4.5.5 Dissemination Through Europe

In 1770, ‘‘Clear instructions for childbirth for the benefit of midwifes of the prov-
inces by order of the Minister,’’ written by Joseph Raulin [16] (1708–1784) appeared
in France. Raulin was the Conseiller-Médecin-accoucheur (advising physician for
obstetrics) of the king of France, Censeur royale (censor), inspecteur des eaux
minerals, member of the Royal Society of London, professor at the College Royal de
médecin, and a member of the Academies of Bordeaux, Rouen, and Rome.
In his introduction, which was recast as a warning (Advertisement), the reasons
for publication are stated plainly [16]:
• The human race is degenerating in France;
• The population (in France) was weakened.

The Minister looked for the causes, and one of the main reasons was found to be
the ‘‘insufficiency of the midwifes during child-delivery’’ [16], who recklessly
practice without knowledge. Fatal examples were adduced, in which mother and
child were mutilated. ‘‘It is for these reasons, taken from the cry of nature, that I
decided to publish these instructions for child-birth’’ [16].
Raulin’s manual for midwives is instructive and a rather good guide to the
practice of that period. It comprises natural and unnatural birth and what measures
to take. It brought magistrates to support midwives and indicates when surgeons
should be involved; the cesarian section especially is restricted to surgeons. One
chapter, approved by the theological faculty of Paris, is devoted to the question of
how and when to baptize.
The chapter on anatomy of the pelvis is limited to knowledge necessary to carry
out the delivery ‘‘with understanding’’. It is interesting because it is written

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4.5 Hendrik van Deventer (1651–1724): Father of Pelvic Science 63

25 years after Van Deventer’s publication for midwives and obstetricians. Let us
follow the text on the anatomy of the pelvis (in translation: his pp. 36–39) [16].

4.5.6 The Pelvis

The bones, that constitute the cavity of the pelvis, are three, the os sacrum and the
two ossa innominata. The first one is placed posterior and the two others at the
lateral and anterior sides. The female pelvis is larger than the male one, so that the
fetus can easily pass through. The opening formed by these bones at the caudal
side is also bigger to facilitate the passage of the child.

4.5.7 The Coccyx

The coccyx articulates with the lower part of the os sacrum, by the interposition of
cartilage and some ligaments; it is also connected by its two lateral superior parts
to the os innominata. The articulation of the coccyx allows it to bend backward or
inward, according to the circumstances, which is advantageous during delivery.
The innominate bone is formed in the child by three distinct bones, which are
joined together by cartilage and which constitute one bone on each side in grown-
ups. It is not necessary to give the descriptions of the several parts. It is sufficient
to observe that the ossa pubi are among them. They are placed high at the labia
majores and stretch out laterally. By this property, they give the pelvis its size.

4.5.8 Deflections of the Pelvis

‘‘In its natural size, the pelvis facilitates delivery, but if the bones that constitute it,
deviate from their conformation or their configuration, that is if they are irregularly
arranged, the child is prevented from passing, mainly at the inside upper part of the
os sacrum and os pubis, especially if these are to close to each other. Sometimes,
this obstacle can be removed if the midwife turns away the coccyx by hand during
the contraction of the base of the uterus, which compresses the child’s body
between these bones: if this remedy does not help, the child can only be delivered
by a cesarian section. These abnormalities are found in women who are crippled,
hump-backed or suffering from a hip disease, but above all among those that have
rickets from their early years’’.
It is obvious that the pelvis is limited here to the bony pelvis. The uterus and
vagina are discussed later on, but their relations to the pelvis are minimally
described. The passage of the fetus is made possible by the opening between os
sacrum and os pubis, which is a correct description. Clearly, the function of os

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64 4 History

coccyx, and how to manipulate it is taken from Van Deventer. Moreover, the
difference between the female and male pelvis is apparently well-known, even in
its consequences for the delivery.
Thus, 25 years after Van Deventers approach, the instructions were adopted for
all of France and this indicates that Van Deventer’s work not only reached the
midwives in Dutch-speaking countries but also spread Dutch Golden Age pelvic
science to the entire Western world through the French language (lots of people
read French), but also by an English edition.
However, the most remarkable fact lies in the last sentence of the citation.
Rickets was detected as an illness that displaced the coccygeal bones. Had the world
of the anatomists already detected that Van Deventer had pictured a rachitic pelvis?

4.6 The Pelvis According to Govard Bidloo (1649–1713)

More than three centuries have passed since the publication of Govard Bidloo’s
‘‘Anatomia Humani Corporis’’ [17]. It is now appropriate to examine this con-
troversial study, which became famous due to the impertinent plagiarism of
Cowper. The pictures (also of the pelvis) are extremely good, because they were
produced by a talented artist: Gérard de Laresse (Fig. 4.10).

4.6.1 The Life of Govard Bidloo and Gérard de Laresse

Govard Bidloo [18] was born in Amsterdam on December 12, 1649 and died on
April 30, 1713. His life was overshadowed by the plagiarism of his main ana-
tomical publication by William Cowper (1666–1709; see below). His father
(Govert Bidloo) and mother (Maria Felzers) were Anabaptists also called Men-
nonites. (The followers of Menno Simonsz (1496–1561) formed a large parish in
recently liberated Amsterdam). Little is known about Govard Bidloo’s youth, but
in 1670, his name was entered in the registers of the Amsterdam Athenaeum as a
medical student. He attended the lectures of Frederick Ruysch (1638–1731), the
leading anatomist of this time, known for injecting blood vessels with hot wax.
After obtaining his medical degree, Bidloo started as surgeon in Amsterdam.
From here, he also traveled through Germany and France as an army surgeon. He
continued his studies in Leiden and defended his thesis in Franeker, where he
obtained his degree on the thesis: ‘‘De variis anatomicomedicis positionibus.’’
Upon his return to Amsterdam, he was drafted into the army of Holland, to fight
against Louis XIV who had attacked the Netherlands. He became professor of
anatomy in The Hague (1688) and later professor in anatomy (1694) and in surgery
(1702) in Leyden.
Intriguingly enough, Bidloo is known not only for his science, but also for his
poems and theatrical pieces. Such diversity of talent ran in the family: his brother
Lambert (1633–1724), known as a chemist and botanist, was also a famous poet.

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4.6 The Pelvis According to Govard Bidloo (1649–1713) 65

Fig. 4.10 Portraits of Laresse (left picture), Bidloo (middle picture) and Cowper (right picture).
Courtesey Prof. Dr. H. Beukers, Leiden University

Bidloo’s anatomical masterpiece ‘‘Anatomia humani corporis’’ [17] appeared in


1685. One year later, he published an opera entitled ‘‘Sans bonne chère, ni vin, pas
d’amour’’ (without a sweetheart, no wine, no love) [18]. Through his contacts within the
Amsterdam artistic circles, he learned of the reputation of Gérard de Laresse, and in him,
he found his medical artist for his master piece, which he had already started in 1676.
Gérard de Laresse [18] was born in Liège on September 11, 1640 and died on
July 28, 1711. He sprang from a (portrait) painter’s family. The household counted
four boys. The father was often abroad on a painting commission and this led to a
haphazard schooling of the boys. Gérard had a natural talent for drawing and
painting, and therefore, his father decided to apprentice him to Berthold Flémalle
(1614–1675) at the age of fifteen. After finishing his apprenticeship, he was sent to
Italy for further artistic study. However, on his way, he obtained so many com-
missions and became so famous that he returned to Liège and never made it to
Italy. His commissioners had him paint ancient and biblical scenes. Gérard earned
a lot of money, but he was a bigger spender. The non-fulfillment of a marriage
pledge was De Laresse nearly fatal. The so-called bride and her sister tried to kill
De Laresse, and while defending himself, he seriously wounded one of the ladies.
De Laresse fled to a convent, where he was helped by Marie Salme. He fell in love
with her, and during their escape from Liège to Maastricht, they married. Via’s
Hertogenbosch, they reached Amsterdam, where he climbed quickly to the top of
his profession and where Bidloo made his acquaintance.

4.6.2 Cowper’s Plagiarism

William Cowper (1666–1709) became a barber–surgeon in London in 1691 and


started a practice [5]. In 1694, he published his first scientific work, which can be
called modest [5]. In 1698, he published the unsold, stored remainder of the prints

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66 4 History

of Bidloo’s Anatomia under his own name. His plagiarism went so far that he only
replaced the portrait of Bidloo with his own. On the frontispiece, he changed the
shield with Bidloo’s name and placed his name printed on parchment over it.
Moreover, he changed the title page with the name of the book to: ‘‘The anatomy
of human bodies.’’ The whole text was translated into English and he improved it,
but clearly followed Bidloo’s construction. At the end, Cowper added an appendix
on muscles [18].
In the meantime, Cowper became a member of the Royal Society. Bidloo rose
to the position of physician to stadtholder–king Willem III, superintendent-general
physician of the Dutch army, and head of the medical service of the English army.
The plagiarism occasioned many letters, lawsuits, and publications, but the Royal
Society was too cowardly to expel Cowper, with the consequence that he remained
unpunished [5]. Because of its good English text, its beautiful pictures and a better
character font, the Cowper publication is considered superior to Bidloo’s original.

4.6.3 Anatomia Humani Corporis

Bidloo’s ‘‘Anatomia humani corporis’’ [17] is after Vesalius ‘‘De humani corporis
fabrica’’ one of the most important anatomical works of the early modern period,
and it received greater renown, which got extra attention because of the plagiarism
of Cowper. The 106 plates, although numbered to 105 [18], are all engraved by De
Laresse. The quality of the pictures is undeniable and the subjects are placed into
household objects such as a vase or an ink pot.
The anterior view of the skeleton, with the hourglass in hand, is placed in a
background of an opened tomb. Although the anatomical descriptions are limited,
they are already modern. Details are not avoided and the results of contemporary
research were taken into account. Bidloo knew the works of Antoni van
Leeuwenhoek (1632–1723) (and even worked with his microscopes), Malphigi
(1628–1695), Thomas Willis (1621–1675), and Reinier de Graaf (1641–1673).
Along with other microscopic pictures, the first illustration of a crush or fluff
preparation of a nerve is found in Bidloo’s ‘‘Anatomia humani corporis’’ [5].

4.6.4 Bidloo’s Description of the Pelvis

Bidloo describes two bones in the pelvis: the os sacrum and the os innominatum
(the name-less bone), in fact half of the bony pelvis. We divide the nameless bone
in os ilium, os ischii, and os pubis, but Bidloo differentiates the following:
• A gut bone, identical to our os ilium;
• A groin bone, the transition of the os pubis and os ischii;
• Hip bone, the acetabulum with its bone area above the joint.

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4.6 The Pelvis According to Govard Bidloo (1649–1713) 67

Fig. 4.11 Drawing from


Bidloo showing front and
backside of the sacral bone.
On both sides, front and
backside of the coccygeal
bones are depicted (1685;
T98). See also text,
reproduced with permission
of the Leiden University
Library

The groin bone subsequently is not always labeled in the figures, which creates
confusion about the definition of this bone.
In any case, Bidloo uses a totally different subdivision from what we are
accustomed to. The acetabulum and the foramen obturatum are described. The
acetabulum called the bush is for Bidloo the joint socket as well, in which the upper
leg with its caput fits. The texts of Fig. 98 (the sacrum) and 99 (half the pelvis) yield
no indications of the recognition of the tubers of the os ischium. Moreover, the
processi articularis superior (upper facet processi) are not well interpreted by
Bidloo. The impression of the sacroiliacal joint on the os ilium is pictured, but not
named. The sacroiliacal ligament is explicitly described, having an impression on
the os ilium, but the text gives no arguments for a sacroiliacal joint. Within the os
sacrum, the intervertebral disks (de vijf tusschen scheydingen, the five interdis-
sections or separations) are recognized (see Fig. 4.11 and the text of Fig. 4.12). The
promontorium is not included in the pelvis, because the sacrum is described without

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68 4 History

Fig. 4.12 Drawing from


Bidloo showing front and
backside of half a pelvis.
Note the impression of the
sacroiliac joint in the upper
part and of the acetabulum in
the lower part, reproduced
with permission of the Leiden
University Library

the lumbar vertebrae. The hollow parts at the dorsal side of the os sacrum are at the
sides of the foramina for the nerves, badly noted and only described up to the flat
inner side of the ventral os sacrum. The notion that the processi spinosi are fused is
absent. The caudal coccygeal vertebrae are shown in detail in two separate small
figures. The pictured hiatus sacralis is not referred in the text.

4.6.5 Conclusion

It is remarkable that in his Dutch text, Bidloo mentions fewer facts than the medical
artist pictured. De Laresse makes important contributions through his excellent
pictures, demonstrating a series of anatomical details which Bidloo overlooks.
Should Cowpers plagiarism, in historical perspective, be judged acceptable,
because through it the figures of De Laresse were widely disseminated and because
through Cowper’s text the anatomical drawings accelerated renewal in anatomy?

4.7 The Sacrum Bifidum

Pathology of the human body also drew interest among the scientists, besides the
studies of the normal morphology. For our approach, the bifid spine is the most
interesting since it is directly related to a structure, which closes the pelvic ring [19].

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4.7 The Sacrum Bifidum 69

Fig. 4.13 Sacrum bifidum


excavated at the St.
Catharijne Convent Utrecht
(Vredenburg B2.250-H)
dated 1200–1250 AD.
Courtesey J. van Gool

The bony pelvis is connected to the os sacrum of the vertebral column by the
sacroiliacal joints and the sacroiliacal ligaments. The connection is a stable one.
Most afflictions of the sacrum are related to the sacrum bifidum. Nowadays, his-
torical introductions to theses are becoming unfashionable. However, theses that
do contain such an introduction are particularly interesting, because research
efforts are placed in their historical context. On spina bifida, such a thesis exists
[19]. Moreover, the Leiden Anatomical Museum possesses a sacral spina bifida
pelvis: The thesis and the specimen together form the basis of this story.
The congenital defect of the sacrum known as the sacrum bifidum is as old as
mankind. The National Museum of Natural History in Paris possesses a sacrum
bifidum from the Neolithic era (5000 BC). Specimens from the early Bronze Age
(circa 3000 BC) and from the Iron Age (circa 1000 BC) are also known (Fig. 4.13).
An open sacral canal is not always followed by severe neurological problems, and
survival and solid ossification are possible. The bony results of such ossification are
the subject of archeological research [20]. In the literature, Hippocrates is always
cited as the first student of the sacrum bifidum. The term itself is used for the first
time in the seventeenth century. Nicolaas Tulp (1593–1674) is said to be respon-
sible for the popularization of the term, although this assertion [20] has not been
supported with documentations. The first use of the term remains unknown.
Credit for the first scientific description should probably be given to Volcher
Coiter (1534–1576), although this has not been verified [21]. In rereading Coiter’s
work in an English edition, I could find no reference to spina bifida. However,
Coiter evidently was familiar with the bony malformations, as indicated by the
next citation:
‘‘Indeed, every day experience teaches that deformities and dislocations of the limbs are at
no age more frequent than in youth’’ (…..) ‘‘Hence I am moved to no less pity than wonder
by those miserable and luckless children who fall into the unfeeling hands of incompetent
and arrogant barbers, butchers and old women and return from them, some with monstrous
heads, many hunch-backed, bow-legged, club-footed, with large and misshaped ankles,
knock-knees and limbs strangely contorted’’ [21].

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70 4 History

Fig. 4.14 Sacrum bifidum from the collection of Zaayer, reproduced with permission of the
Leiden Anatomical Museum, LUMC, Leiden

In Coiter’s description of the development of the skeleton, it is remarkable that


he already discerned the constituent parts of the pelvis, each having their own bony
nucleus. Moreover, Coiter noticed that the acetabulum is put together from the os
ilium, ischii, and pubis [21].
It was a small community of practitioners that studied spina bifida for the first
time: Bauhin (1605), Hildanus (1614), Schenck von Grafenborg (1587), Van
Foreest (1587) and Tulp (1596) are the best known [19]. Exchange of knowledge
was limited, and on several occasions, research was duplicated. The first monograph
on spina bifida was published in Switzerland, where in 1703, C. F. Hochstetter
defended a thesis on the subject (director Apinus). Halfway through the nineteenth
century, the barriers came down, and the subject was studied all over Europe.
The sacrum bifidum, as seen in the Leiden Anatomical Museum, is from the
collection organized by Zaayer (1837–1902) (Fig. 4.14). It belongs to the

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4.7 The Sacrum Bifidum 71

teratology section of this collection, and specifically to the subdivision ‘‘dry


preparations of human origin.’’ It concerns the pelvic girdle of a child with spina
bifida of the sacral vertebrae. These are still attached to the upper parts of the legs,
and lumbar vertebrae III to V are present. The ligaments at the posterior back side
are still partially extant. The defect goes from the sacral hiatus up to the highest
first sacral vertebra, just involving the articular process. From the sacral vertebra,
the arch and the dorsal processes (spinosus) are missing. Only the dorsal foramina
for the nerves are recognizable.
In 10 % of spina bifida cases, the meninges form a rupture sac (cèle) that only
contains spinal fluid: a meningocèle. The cèle is covered with skin. In the other
90 %, the spinal cord or myelum is affected: meningomyelocèle. The skin is often
not closed (spina bifida aperta), so that nerves and myelum are visible from the
outside. Both types of cèles are equally prevalent at the sacral level in patients.
This provides no indication of the type of distortion that was present.
The pelvis ossifies from three bony nuclei. The pubic bony nucleus fuses with
the one from the os ischii at the age of 7–8 years, and this fusion is nearly complete
in our specimen. One notes the fracture line, indicating the as yet incompleted
fusion in the ramus of the os ischii. The acetabulum is still cartilaginous. This joint
socket will only ossify later. The sup-position that we have the pelvis of a child of
seven years old seems warranted. It is plausible, too, that it is not a case of men-
ingomyelocéle, for most children with that type of affliction do not survive their first
year, and they certainly did not at the end of the nineteenth century.
In this context, we cannot resist commenting on part of the thesis of Folkerts
[22] (1946, director Woerdeman): ‘‘The ossification of the arches of the vertebrae
has been described by Bardeen and others. Each arch ossifies from two centers,
which melt together to one arch in the fetal situation. The ossification goes into a
craniolumbar direction till lumbar vertebra V. In the sacral bone, however, the
ossification starts in the middle arch and goes from there on in both cranial and
caudal direction. Olof Ask found in four young embryos already in the cartilagi-
nous situation the tendency to melt late and incomplete. Toldt means that the
closure of the arch of sacral vertebra I can occur between first year and fourteenth
year, Mall concluded its closure between seventh and fifteenth year. Systematic
X-ray research of Graesner and Beck, showed data in 10 % and the last author that
in 3 % of the adults a cleft in the arch of sacral vertebra I can exist.’’ [22].
From the forthgoing, it is clear that a cleft in the arch of sacral vertebra I have to
be considered in certain of the cases as a normal variation of the ossification
process. In the other cases, however, it constitutes an expression of a malformation
of the spinal cord that will go along with clinical disturbances. Variety and mal-
formation here smoothly pass into each other.
A meningomyelocéle is accompanied by incontinence, paralysis of the legs and,
in 80 % of the cases, with a hydrocephalus. Influences on motility are also known:
20 % of these patients have a congenital hipluxation, 40 % show trophic distur-
bances of the legs [23]. Our anatomical preparation seems to have no other abnor-
malities, which supports the diagnosis of meningocéle. Ossification normally occurs
around existing nerves, which develop first. If the nerve is absent, no foramen

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72 4 History

occurs. The dorsal foramina are present in the Leiden pelvis, an indication that the
nerve paths were normal. The Leiden pelvis therefore is a sacrum bifidum, with a
meningocéle, that only disturbed the arches of the sacral vertebrae (rachischisis).

4.8 In Summary

The history of the study of the bony pelvis and its floor demonstrates a lack of
factual knowledge. Vesalius was fundamentally concerned with the os sacrum. He
placed the bony pelvis wrongly, tilted, with its os pubis directed rostral. The start
of pelvic science by Van Deventer was based on an error, due to a malfunction of
the bony pelvis in some child deliveries. Bidloo described the bony elements of the
pelvis insufficiently precise, despite the high degree of perfection of the illustra-
tions made by his medical artist De Laresse. It was only later that the case of the
bifid spine was seen by Jacob Hovius (1710–1786) to be related to a deviation of
the os sacrum; even though this problem was studied by famous anatomists such as
Bidloo, Tulp, and Ruysch. One should expect that the worldwide study of spina
bifida in one way or the other should have stimulated the study of the whole (bony)
pelvis. Such is not the case: spina bifida was restricted to deficiency of the os
sacrum. If you do not know how the pelvic bones are constructed and brought
together, you cannot understand the arrangement or deficiencies of its organs.
One must regrettably conclude, therefore, that at the end of the seventeenth
century, pelvic science made an unhappy start, because it was based on faulty
data. Although explained by the distance between physicians and barbers or
surgeons, the former missing practical knowledge, the latter possessing it; nev-
ertheless, the situation for pelvic science was extremely unfortunate. In the sev-
enteenth century, you were treated for bladder stones by charlatans at the market,
whilst clysma’s or enema’s were a source of mirth in the stage-plays of that time.

4.9 Historical Panorama III: The Study of Pelvic Soft


Tissues

Before we can study the history of the soft tissues present in the pelvis, a brief
philosophical excursion is in order to define the term ‘‘pelvis.’’ Over the ages, the
perception of the body has varied. Before anatomists dissected bodies, it was
believed that medieval scientists studied only the exterior of the human body. It
was generally accepted that during this period, no one made a purely scientific
study of corpses [24]. In the sixteenth and seventeenth centuries and up to the
eighteenth century in Great Britain [24], the concept of body was almost reduced
to corpse, due to the rising scientific interest in anatomy and Cartesian separation
of mind and body:

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4.9 Historical Panorama III: The Study of Pelvic Soft Tissues 73

The role of scientific discourse with regard to the folk body* has been, traditionally, to
turn it inside out. Anatomy, for example, exteriorizes the folk body’s interior conceptually
as well as visually [25].

(* folk body is a conceptual frame work used by ordinary people to understand


the body)
Nowadays, mind and consciousness are strongly interwoven in the concept of
‘‘body’’ [26]. Note that terms such as ‘‘mind’’ and ‘‘consciousness’’ are hard to
define. ‘‘There is no non-circular definition of consciousness; the best that can be
done is to offer synonyms or examples [27]. We have no conception of our
physical or functional nature that allow us to understand how it could explain our
subjective experience’’ [27].
Here, we should also look into the term ‘‘body.’’ In our Master courses on
‘‘Theories of the sciences’’ (University Leiden, LUMC) and ‘‘Perspectives in
Anatomy and Physiology’’ (University Twente, BMTI), we discussed the term
body in the following way:
If someone misses an arm, does he have a body? The answer was clearly yes.
And if someone lacks one arm and one leg, does he have a body? Of course he has.
If somebody misses both legs and both arms, does he have a body? The answer
was still yes. So what determines our concept ‘‘body’’: only rump and head?
However, if you asked the same students: ‘‘and if somebody misses his head,
does he have a body?’’ Nearly 60 % of the students said there was no body.
The Cheshire cat in Lewis Carroll’s Alice in Wonderland appears in the
Queen’s croquet court only as a head. A dispute was going on between the exe-
cutioner, the King and the Queen, in which Alice got involved:
‘‘The executioner’s argument was, that you couldn’t cut off a head unless there
was a body to cut it of from: that he had never had to do such a thing before, and he
wasn’t going to begin at his time of life. The Kings argument was that anything that
had a head could be beheaded, and that you weren’t to talk nonsense. The Queens
argument was that, if something wasn’t done about it in less than no time, she’d have
everybody executed’’ [28]. We also can pose the question the other way around:
‘‘what is a body, with or without a head?’’ So, even the term body is hard to define.
In science one starts with entities that are well defined. However, studies on
those objects that are hard to describe are examined by investigating those parts of
that object that are definable. So investigating the mind is rather difficult. Nev-
ertheless, the subpart intelligence can be studied, think of IQ tests. This approach
is called operationalism. So, because we can hardly analyze the body, we inves-
tigate its parts and that is what Anatomy literally does by means of dissection. One
studies the digestive, muscular, nervous, or vascular parts. In fact that was what
Vesalius did: look at, e.g., his figure ‘‘the muscle man’’ [4].
For us the question then is can we study the ‘‘pelvis’’ as a sub-part of the
‘‘body’’ or to rephrase: can we define the pelvis? The bony pelvis is not a problem:
one can characterize it by its bones [29, 30, 31]. However, the total pelvis brings
up problems. Can one define, for example, the boundaries of the pelvis as a
possibility to define ‘‘the pelvis’’? We speak of the greater and lesser pelvis,

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74 4 History

already indicating that the border to the abdomen is less clear. In fact it is virtual.
‘‘The cavity of the greater pelvis is, of course, part of the abdomen; and because of
the inclination of the pelvis as a whole the cavity has little anterior wall, as far as
bone is concerned’’ [29]. So we do not find support in the bony pelvis for an upper
boundary. It is clear that abdomen and pelvis merge into each other [29, 30]. Still
we speak of the pelvic inlet or superior pelvic aperture. It ‘‘is variable in contour,
being rounded or oval, but encroached upon behind the sacral promontory’’ [29].
A more feeble definition is hardly possible for the inlet and thus for locating the
boundary between the pelvis and the abdomen. In short, a definition of the
‘‘pelvis’’ is hardly possible.
If so, can we perhaps characterize the organs that belong to the pelvis and study
these? Our intestine and sigmoid colon, if full of food, will move into the pelvis,
even our stomach can reach the interior of the pelvic cavity, especially after a lot
of food and drinks, and after defecation or during times of fastening, they move out
of the pelvis again. Therefore, pelvic organs are defined as those organs that are
fixed onto the pelvic walls or the fascias of the muscles of the pelvic floor [30, 31].
Since intestine and sigmoid colon have their attachments in the abdomen, they are
not considered as being pelvic organs.

4.10 A Medieval Contagious Disease: Syphilis

From the series of medieval contagious diseases, one will be dealt with: syphilis. We
need it for the Anatomy of the external genitals and plastic Surgery (of the nose).
Historians have not (yet) been able to settle the argument whether syphilis was
endemic in Europe from Greek times onward or was imported from the New
World. Here, we look into what the medieval doctors did know about the disease.
It was known that it is a sexual transmitted disease. ‘‘On July 25, 1463, a prostitute
of Dijon testified in open court that she had kept off an unwelcome suitor by
stating that she was sick with le gros mal (syphilis)’’ [32]. The first symptoms of
the disease were well known: lesions of the scrotum, penis, vulva, or tongue.
However, the non-sexual modes of infection were not known and this is now
considered to be the reason for its wide spreading in Europe [32]. Lues was
medicated by using mercurial ointments. Gerard de Laresse, who was treated in
this chapter had syphilis, became blind and died from it.
Alexander Benedictus, who accompanied the Venetian troops to the battle of
Fornovo (1495), where he was able to observe the disease closely, refers to its
genital origin and says that ‘‘this virus of prostitutes will soon infect the entire
universe.’’ ‘‘He had the opportunity to perform autopsies, and in one, performed on
a woman, he found the corresponding periostitis and osteitis’’ [33].
Although the cause, the spirochete bacterium Treponema pallidum, was
unheard of, early diagnostic features, pathology, and a faint therapy were recog-
nized. Confusion with other skin eruptions did occur: leprosy, psoriasis, and
eczema are the best known [32].

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4.11 Medieval Dissections 75

4.11 Medieval Dissections

It is clear that dissection of the body must have been already in use before the
battle of Fornovo. Let us start with a citation from around 1225 found in Anatomia
magistri Nicolai Physici [33B] describing anatomy of and sectional techniques on
animals and humans. ‘‘A different method was used upon the dead; they took a
crucified corpse and fastened it with rope to a stake in a running stream, with hands
and feed tied, so that after the skin, flesh, fat and other superfluous parts were
removed by the action of the water and the arrangement of the internal members
could clearly be observed….; but such treatment of the human body came to be
considered inhuman, especially by Catholics, and the practice of dissection was
transferred to animals’’: Interpreted by us that in early medieval times, dissections
occurred, although using a horrible method.
Nevertheless, the first anatomical dissection is attributed to Mondino dei Luzzi
(Mundinus) in February 1300, although Wilhelm of Saliceto (1201–1267), but also
Hugh (1252) and Theodoric of Lucca (1205–1298), did produce writings on ana-
tomical knowledge that only could be obtained by ‘‘surgical dissection’’ [32, 33] (for
extracts of their texts see later the part: Contribution of Surgery to Anatomy 4.16).
Mondino’s pupils Henri de Mondeville (1260–1320) and Lanfranc of Milan
(1315) strongly favored the collection of anatomical data. ‘‘From at least the early
twelfth century, opening the body was a common funerary practice, as the
examples of Chiara of Montefalco (1268–1308) and Margarita of Citta di Castello
(1287–1320) indicate’’ [33A]. Embalming bodies of saints or holy persons
occurred, and both for Chiara and Margarita, the opening of the body and the
removal of the heart have been described and is well documented [33A].
Dissections were carried out at Universities. One of the latest founded in 1477
was Tübingen: ‘‘At the University of Tübingen, for example, it was decreed that
every three years the body of a criminal shall be dissected. The dissection was
open to scholars and professional men, as well as to physicians and students. It
consisted in a perfunctory examination of the contents of the abdomen and thorax,
and lasted for only a few days’’ [34].
In 1368, the council of Venice already ordered that once a year a dissection
should be carried out. In several cities (Cremona 1286, Bologna 1302, Padua 1341,
Siena 1348, Venice 1368, Florence 1388, Lerida 1391, Vienna 1404) and uni-
versities (Montpellier 1366, Bologna 1405, Padua 1429, Prague 1460, Paris 1478,
Tübingen 1485), dissections were performed [32] in or at the end of medieval time.
An estimate is not possible, but it must have been over hundreds, including those
for the courts to establish crime.
The official dates as given here should be considered with care. There are clear
indications that dissections were carried out earlier. For Padua, the official date is
1341. However, ‘‘There are, moreover, definitive indications that the dissections of
human cadavers was practiced at Padua in the first half of the fourteenth century in
cases of special interest, or perhaps where foul play was suspected’’ [62]. So between
1300 and 1340, dissections were already performed, shifting the date earlier.

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76 4 History

Fig. 4.15 An exploratory operation from the work of Ruggiero Frugardi written around 1170
[32] with permission of Trinity College, Cambridge and Nero at the autopsy of his mother
Agrippina in Le cas des Nobles et Femmes, by Boccaccio, c. 1410. Note that liver and intestine
are topographically correct. Nero figure is reproduced with permission of the  British Library
Board. All rights reserved

On February 18, 1300 the papal bull was published with an interdiction. Its title was:
‘‘De Sepulturis Bonifacius octavus. Corpora defuncturum exenternantes, et ea
immaniter decoquentes, ut ossa a carnibus separata ferant sepelienda in terram
suam, ipso facto sunt excommunicati’’ (Those who cut up corpses and boil them
with the intention of separating the bones from the meat, to send home for a
funeral in its own country, are barred from the sacraments) [24, 34]. The crusaders
had the habit sending back only the bones of the distinguished nobleman for
burying in their home land. To preserve a corpse over months, as the return voyage
normally lasted in those times, was impossible. The pragmatic approach was to
send only those parts that will not decay. This was carried out with, e.g., Emperor
Frederic Barbarossa in 1190 and King Louis (Saint Louis) in 1270. In some cases,
the heart was also transported [24, 34].
Therefore, ‘‘dissection’’ in the broadest sense of the word was performed from
1100 onward (first crusade 1090; see Fig. 4.15). One would expect that the
medical doctors or surgeons who saw so many heavily wounded soldiers and were
aware of the gathering of the bony remnants of their crusade leaders must have
collected anatomical knowledge. The reports from 1100 on till 1450 are few and
produced minimal anatomical data, literature declares. The cause determined in
historical literature is the overwhelming power of Galen’s manuscripts that made
the sighted blind.
‘‘The reasons were not those given in many popular accounts: the Church did
not issue blanket prohibitions against dissection in medical schools as such, nor
did medieval lecturers on anatomy invariably delegate the actual work of dis-
section to assistants’’ [39]. It is hard to believe that by opening the abdomen, the
physician/doctor/anatomist or surgeon did not look into the pelvis. This is dem-
onstrated by Mundinus’s (1275–1326) texts. ‘‘To crown all, he depicted a seven
chambered uterus’’ [34]. There is some disdain in the remark [34].

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4.11 Medieval Dissections 77

Fig. 4.16 Upper figure of the uterus and its extrusions is from H. Braus [30] and lower two, left
Leonardo da Vinci’s drawing of female uropoetic-genital system, tracing from C Singer [39B].
Vigevano’s seven extrusions can be counted herein, reproduced with permission and right figure
contains the seven extrusion of the human uterus by Guido of Vigevano, reproduced with
permission of Bibliothèque et archives du château Chantilly

However, it is clear from the anatomical studies of Leonardo da Vinci


(1452–1519) (Fig. 4.16) that several ‘‘protrusions’’ are present on the uterus. This
could easily lead to a uterus containing several chambers. Moreover, one should
recognize that Leonardo’s drawing came two hundred years later. Indeed, the
cervix included, one can depict seven extrusions/connections going out of the
corpus of the uterus.
So, the internal female reproductive organs were studied during medieval times.
Giammatteo Ferrari da Grado (1432–1472) described the ovaries correctly, but
held a bifid uterus present in humans [33]. The exterior labia majores and minores
of course were well known, also due to syphilis. Vaginal dilatators were used in

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78 4 History

the fourteenth centuries, while intra-vaginal fumigation was applied in cases of


genital problems and depicted [45]. Pictures of the external male genitals were
produced by John Arderno (1307–1370/1390?), while his anal studies were per-
formed in order to repair rectoanal fistulas. He was able to distinguish rectoanal
cancers from fistulas and behaved accordingly. Dino del Garbo (±1280–1327)
‘‘proved that semen with the power to conceive was produced by the male only
and not by both male and female, as Aristotle and Avicenna had held. He also
remarked in passing that parthenogenesis (propagation without insemination) was
impossible’’ [62]. Mundinus extensively described the digestive tract with the
sigmoid colon and rectum. Moreover, scrotal hernias were operated [35]. Animals
were also used for dissection. ‘‘The animal used for dissection was the pig (chosen
for the allegedly close resemblance of its interior organs to those of human beings,
especially in the female)’’ [39]. Hidden in this sentence is of course that you have
to know the human Anatomy to make such a comparison. Surgery was well aware
of the relation between incontinence and paralysis, and spinal cord and/or brain
damage (see examples of Wilhelm of Saliceto in Sirasi [39, 43]).
The Bodleian Library contains a manuscript of the thirteenth century
(1280–1290) containing more than 24 medical texts on physiology, anatomy, and
obstetrics called Ashmole 399. Folio13v of these texts is on the anatomy of the
female reproductive organs and shows rather well the anatomical knowledge
present in those days. The same picture, surrounded by later-placed text, shows
both the non-pregnant and pregnant situations. The scripture makes it possible to
discern original and later-added text. A lot is written on the Ashmole 399 folios.
We restrict ourselves here to the anatomy. Moral or spiritual guidance by these
figures and text does not concern us here and are presumably incorrect [39B].
Already in 1915, Charles Singer pointed to this late medieval picture (Fig. 4.17)
and summarized the anatomical highlights [39B]. The ovaries are known and,
following Galen’s ideas, the figure indicates that the tuba fallopi brings the ovum
(called also semen in the Middle Ages) into the uterus (The ovulum creates here,
the child is fed here and grows, here the ovulum falls and to descend the ovaries
are drawn inside: hic stat semen creatus, hic nutrit infant and crescit, hic cadat
semen and cum ceciderit colliguntur testiculi in se). The fetus is depicted at the top
of the uterus penetrating the wall. Seemingly, the process of nidation into the
uterus wall was known. Others say that the figure should indicate that the uterus
wall had a gap on top. Blood vessels and nerves are indicated at the top (fundus) of
the uterus, where is written: this nerve joins the ovaries. ‘‘We would remind the
reader that the term ‘nervus’ was applied by medieval writers not only to nerves
but also to tendons, ligaments and ducts’’ [39B]. This can be interpreted as the
presence of the proper ligament of the ovaries (lig. ovarii properium) with its blood
vessels. The inside of the uterus (cavum uteri) is indicated with: This is the way
into the uterus (Hec est uia ueretri = uteri?). The cervix of the uterus contains the
words: This middle piece is muscular and this is a cover (eius medietas est
musculus Hoc est cooperimentum). The vagina has the vulva with its labia on both
sides, and a vaginal sphincter is indicated (lacertus clausus). Contractility of the
distal one-third of the vagina is known: This muscle becomes thick (fills) and

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4.11 Medieval Dissections 79

Fig. 4.17 Charles Singer’s line drawing abstracted from Ashmole 399, folio 13 verso, containing
the thirteenth-century text of the figure [39B]

contracts (Lacertus implet con[stringitque]). A muscle from one-third of the


vagina extends to lateral. This must be the urogenital diaphragm of which is also
said: This muscle becomes thick (fills) and contracts (Lacertus musculus hic implet
and stringit). Lateral to the vagina, a muscle (Lacertus) is pictured, pointing
downward away from collum mat[ricis]. Here, we encounter a problem: one would
think that the collum mat is the bony pelvis. Collum matrices mean the neck of the
stem or trunk. Charles Singer, although he states ‘‘a first glance suggest a dia-
grammatic representation of the pelvic wall’’ interpreted this as ‘‘an attempt to
indicate two halves of a bisected vagina,’’ but it could also be interpreted as the
crista iliaca. If this is the case, the lateral muscle could be explained as the levator
ani muscle. But this is pure speculation.
Menstruation is explained in this figure by an extra space for blood storage
(station sanguinis), which brings this blood toward the ovaries (This is the way of
the menstrual blood, Hec est uia sanguinis menstrui). Since pregnant women do
not menstruate, the fetus supposedly consumed this maternal blood to grow.

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80 4 History

The anatomy of the pregnant uterus was known since cesarean operations were
carried out in order to save the child after the death of the mother due to delivery.
The cesarean dissection was a duty imposed on midwifes and surgeons by the
Church ‘‘in order that it should not die unchristened and its soul been lost’’ [44].
However, the best known report of a cesarean operation on the living mother is
from Scipione Mercurio (1540–1610) not earlier than 1595 [46], but see later.
This brief overview of the historical literature shows that: Early Medieval
knowledge gathering at least involved the female and male genitalia and indeed
included pelvic organs (for overview see Table 4.2 please note the dates) which is
contradictory to the view generally held until recently.
A second point of attention is the quality of the illustrations of anatomical data
(compare Fig. 4.16). Medieval painters were quite capable of depicting the human
body, whether in Byzantine or early naturalistic style or in three dimensions for
sculpture. Cenne di Pepo Cimabue’s (1240–1302, teacher of Giotto) crucifixion
(Fig. 4.18) shows the body in general good proportions with the correct muscu-
lature shining through the skin. Several more crucifixes show this: The thirteenth-
century crucifix in the Santa Lucia church in Syracuse, the fifteenth-century one in
the Museo Regionale in Messina to name a few. The painting of the human body
came to perfection with Van Eyck (1395–1441) in Eve and Adam in the St. Bavo’s
altar piece (see Fig. 4.18).
So an exterior map of the body was present in medieval times. Why then is this
map not used as a reference framework for placing the internal organs or, in other
words, are topographic relations and projections clearly underscored?
It is known from both Albrecht Dürer (1471–1528) and Leonardo da Vinci
(1452–1519) that they studied the proportions of the body, and related anatomical
dissections were carried out by Leonardo. However, that is Renaissance. Before
this time, a diagrammatic picture of the proportions of the body was presented by
Vitruvius (85?–20 B.C.) [39D]. The body fits into a circle with the umbilicus as the
center of the body/circle, although not entirely. It still represents human measures
rather well. Manuscript copies circulated much earlier and were read in early
medieval and cathedral building time, because it was the only surviving archi-
tectural book from Roman time [39E].
Prostheses and orthoses were produced in medieval times [32, 36] even for the
hand. One needs some accurate measures for this. Geometry was well developed
due to cathedral building. Therefore, medieval medical scientists did have a rather
accurate map of the exterior of the body, while studying the interior of corpses.
The exterior map of the human body was indeed used to indicate the sites for
bloodletting and it could contain the ‘‘appropriate veins to incise for different
complaints’’ [39]. Henri de Mondeville used thirteen plates of the human body to
instruct his students; moreover, he depicted the separate organs along with these
maps [39A]. ‘‘Guido de Vigevano tried to develop new types of anatomical
illustration to use in teaching; Guido specifically announced his intention to use
pictures as a substitute for dissection. But the actual pictures produced were not
very anatomically informative. By the first half of the fifteenth century, however, a
few instances of relatively naturalistic anatomical illustration were beginning to

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4.11 Medieval Dissections 81

Table 4.2 Anatomical structures named in Second Salernitan Anatomy and Anatomia Cophonis
(1100–1150)a
Note: only anatomical structures are indicated, independent of their medieval
physiological meaning
Topography of pelvic structures:
Rectum, anus, anal fistula, uterus, vagina and cervix, bladder and mutual relations
Organs:
Testis, ovaries, tuba fallopi, bladder, uterus, rectum
Ligaments and vessels:
Ligaments and vessels uterus
Vessels and nerves for bladder
Ligaments and vessels testis/ovaries
A.v. iliaca communis, iliaca interna and externa
Vasa epigastrica
Course of art. testicularis and ovarica
Testis and ovaries:
Tuba, lig latum, cavum scroti = peritoneum, epidydimis, ductus deferens, scrotum, and hernia’s
Bladder:
Ureters from kidney, entrance in bladder, urethra, trigonum of the bladder, nerves for contraction,
relation to peritoneum
Uterus:
Internal structure wall, cavum uteri, fundus, cervix, morphology during life
Vulva:
Os pubis, clitoris, prepuce, m.bulbo/ischiocavernosus, labia, bulbi
Penis:
Glans, corpora cavernosa, innervation penis, urethra for semen and urine, bulbus penis
Pregnancy:
Ovulum, nidation, placenta, fetal membranes, relation vessels uterus and placenta, umbilical cord
and rectus diastasis
a
See G. W. Corner (1927) Anatomical texts of the earlier middle ages. Carnegie Inst 364,
Washington and D. Jacquart, C. Thomasset (1985) Sexualité et savoir medical au moyen age.
Pres Univ France

appear. Dissection itself provided a general map of the body to accompany books;
at best books and body helped to explain each other’’ [39]. So, the starting point of
topographical drawings has to be placed in the late Middle Ages.
Medieval writing and picturing were restricted to those learned to write and
read. Picturing was used to illuminate the manuscripts and was mainly done by
monks. Moreover, parchment or paper was expensive (Leonardo used every part of
a paper to make his notes). Involving artists was an expensive undertaking. From
Dante, a contemporary, we do know that Cimabue (1240–1302; Florentine painter,
teacher of Giotto) had a rich and wealthy life style, which he could maintain due to
his artistic income. One argument therefore is an economic one, due to the cost-
liness of parchment or paper and paintings/drawings by artists. The other is, only
few could study. They had to be wealthy or extremely gifted. Indeed, learned
doctors were few, even in the cities, not speaking of the country.

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82 4 History

Fig. 4.18 Crucifixion by Cimabue (1287–1288, Basilica di Santa Croce, Florence, proprietà del
FEC del Ministero dell’ Interno, Italy) and Adam and Eve (1426–1432) by Van Eyck (copyright
Sint-Baafskathedraal Gent,  Lukas-Art in Flanders vzw/foto Hugo). The painting of Eve is so
realistic that one can see her pregnancy and careful observers will notice that her right eye has a
defect like a drooping eye lid. Both figures are reproduced with permission

Another argument is given by Zwijnenberg in the project: Philosophy, anatomy


and representation: ‘‘The sensory experience obtained by the anatomist during a
dissection needs to be recorded by a medium outside his/her mind, in order to
become accessible knowledge that can be theorized, discussed and disseminated.
Since the Renaissance (italics ours), it has proven to be impossible to develop
comprehensible anatomical knowledge without the help of a medium, such as a
drawing or print’’ [39]. So, in early medieval times one of the following, theo-
rizing, discussing, and/or dissemination, suffered from the poor picturing. Theo-
rizing was difficult due to the Galen domination of theory. Dissemination was also
difficult, besides the few books that were available, the main way of dissemination
was oral. Discussing, of course, was performed in centers of excellence, the
medieval universities, where deviation of Galen’s/Avicenna’s Canon doctrine was
hardly acceptable and kept to a philosophical dispute [39]. Therefore, the exteri-
orized medium hardly could be a realistic painting, but for the wealthy few that
could write, it must have been restricted to working sketches. ‘‘Most medieval
anatomical illustrations were lacking in detail and were not intended to be

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4.11 Medieval Dissections 83

representative or naturalistic. Illustrative material about anatomy in medical works


was primarily schematic and mnemonic’’ [39]. This should explain the failure of
the breakthrough of topographical drawing in the late Middle Ages. The
involvement of artists in dissections (partly) contributed to the improvement of
anatomical illustration (see also [39]).
But there is a more valuable argument: The circulation of visual knowledge is a
problem in cultures that communicate orally and/or by means of manuscripts. It is
not a matter of skill in representation (as pointed out above) but rather a matter of
exactly repeatable visual statements. In the medieval manuscript culture, pub-
lishing means copying by hand. After a few successive copyings by scribes who
have no access to the original, illustrations become schematic and information is
lost. The same conclusion is drawn by Roberts and Tomlinson. They still add that
‘‘diagrams could indicate topology even if they did not convey the dimensions,
proportions or appearances of the parts considered. Such diagrams are found in
books of anatomy from medieval times to the present day’’.
So a clear distinction should be made between the original and the copies of
copies that present denatured information in almost schematic form in the Middle
Ages. Nevertheless, this denatured information still can be useful if it is in a
diagrammatic form [39C].
A different explanation is given by Rens Bod, professor in cognitive sciences at
the Universities of St Andrews and Amsterdam. In his book, ‘‘The forgotten
sciences. A history of the humaniora’’ [39C] that is dedicated to explore the meta-
principles and meta-systems present in these disciplines studying human culture,
he theorizes why in the early medieval times artists lose their interest in picturing
reality as exact as possible. The bible in its second prohibition bans picturing of
God and heavenly and earthly matters. Due to Pope Gregorius I (±540–604), who
argued that pictures are the device for teaching the illiterates, medieval artists still
imaged Christ, saints, and biblical scenes. ‘‘Artists were still free how to picture,
but in practice very soon lost interest in classical proportions, the anatomy and true
to nature reproduction’’ [35A]. The only importance in reproduction was adher-
ence to the Catholic Church doctrine and not realistic reproduction. The illiterate
should notice the biblical message, all other information in a picture lead away
from the task of teaching the Bible. Nevertheless, in medieval sculptures, the
anatomical dimensions are very realistic (Fig. 4.19).
Perception is also biased by theories. What we see is the result of ages of
theorizing. The medieval anatomists lived in another theoretic world. The uterus of
Vigevano is for us non-realistic, but for the medieval anatomist, it was probably an
actual representation of their reality. For us, topographic anatomy is a picture of the
body and on or in it projected the different organs composing our body. The
medieval scientist could have a different approach. There are medieval pictures of
human bodies with on it marks, marks to relate human body parts to the zodiac
[36A], and marks to relate to wounding of the body. Within the medical concept of
healing, cauterization by hot or cold iron was an accepted method [37A]. ‘‘The
rationale of cautery seems to have been to create ulcers from which noxious matter
would drain’’ [37A]. All types of organs were cauterized, e.g., spleen, stomach, and

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84 4 History

Fig. 4.19 Altar piece of the passion: Carved painted oak produced in Flandre, last quarter
fifteenth century. Exhibited in Exeter cathedral by the Royal Albert Museum. Note the correct
proportions of the bodies, face expressions, handgrip, e.g., of Maria and muscles shining through,
e.g., the criminal at Christ’s side, (photographs Marani)

liver. The cautery points, like the needle points in acupuncture, were indicated on
pictures of human figures: all this ‘‘to assure accuracy in cauterization for specific
ailments’’ [37A]. The same is true for bloodletting. Maps were produced in which
the bloodletting points are indicated (see above). Cautery points for elephantiasis,
scrotal hernias, head tumor, throat trouble, and short breath, suppuration of teeth,
kidney trouble, and superior member tumors are described. Another Ashmole
manuscript (Nr. 1462) from the thirteenth century pictures humans realistically in a
frontal, back-side and even a semilateral view with clear cautery points [37A]
(see Fig. 4.20). Topographic anatomy, for example the points to reach (read
localization of) the spleen, stomach, and liver, therefore is hidden in a concept of
medieval functionality, whether related to the zodiac, wounding, or cauterization.
Thus, the interior of the body was evidentially projected on the surface and precise.
Exteriorization of organs also occurred: heart, stomach, gall bladder, spleen, kid-
neys, bladder, uterus, omentum, liver, and lung preparations are depicted already in

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4.11 Medieval Dissections 85

Fig. 4.20 Cauterization points indicated on the human body in a thirteenth-century manuscript.
Folio 9r and v shows 14 bodies in total labeled. Bodleian Library, Oxford University with
permission

the 13th century and ‘‘more precisely detailed than those in the three Mondeville
manuscripts…We are forced to conclude that Mondeville’s 1,304 illustrations were
little or no improvement over their thirteenth-century predecessors, which indeed
they might well have emulated in some respects’’ [37B].
Not only the localization of organs, but also their organotypic characteristics
were well known in medieval times.
An overview of the pelvic organ knowledge present at the end of the medieval
time period can be given now. Our guide is the book of Johannes de Ketham, the
first printed medical book called Fasciculo de Medicina (1491 and 1493) [37].
‘‘This is a compendium of medical information that included a complete transla-
tion of Mondino di Luzzi’s Anothomia. Mondino’s book originally written in
1316, was the text favoured by most medical schools and the Fasciculo edition
was the first to be published in Italian. The Mondino publication was typical for
fifteenth century medical books in that it was essentially an unchecked reissue of
ancient anatomical manuscripts’’ [38] see also note [38A].
The pictures of the 1491 edition are redone in the 1493 edition, sampling in its
figures the known Anatomy. If we do not go into the image change like direction

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86 4 History

Fig. 4.21 Female figures from Ketham Fasciculo de Medicina: 1491, left, tabula tertia de
mulicre, and 1493 publication to the right. The original author was presumably Johannes von
Kirchheim (Ketham) around 1340, reproduced with permission of Museum Boerhaave, Leiden

of the face or hand expression [37], but restrict ourselves to pure topography, what
do these pictures tell us on the Anatomy of the uropoetic-genital system at the start
of the Renaissance?
In the 1493 edition, kidneys and ureters are well depicted. The uterus is given
with cervix and an opened vagina. Note the salpinx and the ovaries with an
indication of the lig. ovarii proprium (see Fig. 4.21). The cardinal ligament is
perhaps even shown here. The 1,491 picture is less clear in topographic sense, but
contains the fetus within the uterus. Bladder and its function were known of course
due to the bladder stones and its operation. Anal and rectal structures were known
by the fistula studies. So at the transition of the medieval period into the
Renaissance era, at least most pelvic soft tissue structures were known. This
knowledge was partly gathered from ancient Greek and Roman information, partly
from own human and animal research.
What ever the contribution of medieval Anatomy and Surgery, it hardly can be
denied that the interior of the human body and of the pelvis, topographically and
organotypically, were already well known at the start of the Renaissance.

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4.12 Renaissance 87

4.12 Renaissance

Here, we encounter a rare difficulty. The great scientist and artist in the early
Renaissance time, Leonardo da Vinci (1452–1519), produced a series of drawings
for his Anatomy book together with the professor in Anatomy of Pavia Marcan-
tonio della Torre (1481–1511) [40], but never published the book called ‘‘Treatise
on Anatomy,’’ due to the sudden death of Marcantonio della Torre from the
plague. We can hardly recover the dissemination of his findings into the scientific
world of those days, because Leonardo did keep his results rather secret for his
book. ‘‘Leonardo contributed little of substance to contemporary understanding of
the human body. His drawings and notes (…) remained unpublished until well
after his death’’ [37]. Nor do we know whether all the pictures for the book
survived or not. Some speak of more than 1,000 pictures, while only a small
percentage has been recovered.
Leonardo possessed a series of anatomical books that originated from the
Middle Ages. Leonardo da Vinci’s ‘‘Library,’’ contained a list of thirty-seven
books, titles, and authors’ names indicated in his Codex Atlanticus, and a list of
one hundred sixteen books, left in Florence, in 1504, due to one of his travels. That
list was rediscovered in the Madrid Codex II. In it a series of anatomical titles or
books containing medicoanatomical treatises, to name a few: the Opera of Plato
and Aristotle, Celsus’ De Medicina, Plinius’ Natural History, Ketham’s Fasciculo
di Medicina. It is supposed that Leonardo studied the work of Galen. One should
note that Leonardo’s first anatomical data ‘‘was relying on textbook anatomy’’
[38]. Leonardo had access to dissections in Milan and Venice from 1,500 on. ‘‘The
anatomical drawings of Leonardo da Vinci span the years between 1487 and 1513,
but only in the latter half of this time did Leonardo have detailed (italics ours)
knowledge gained through dissection. Da Vinci’s source of information in the
early years could only have been gleaned from textbooks and, as a result, Leonardo
spent much of his time producing drawings which tried to explain the conflicting
viewpoints presented in these books’’ [38]. Therefore, even Leonardo was strongly
influenced by the anatomical knowledge gathered during the Middle Ages. We
omit here the results mainly from before 1,500 and restrict ourself to his results
obtained by or with a base in anatomical dissection.
From some ten drawings [41], the following picture arises:
The bladder is well depicted with the urethra continuing into the penis. The
origin and course of the seminal ducts are anatomical correct, entering the urethra,
together with the art. testicularis and its origin from renal arteries. Kidneys and
ureter, together with the entrance in the bladder, are in conformity with modern
views. Seminal glands are depicted as the urachus (connection bladder umbilicus)
is (see folio; RL 19054r, RL 19101v urachus, RL 19095v, RL 19099r, RL
19098v).
Female organs and pregnancy are depicted. The placenta, as repeatedly dis-
cussed, is of a cow. Fetal membranes and the fetal development were studied by
Leonardo. Female external genitalia are depicted and the urethral orifice can be

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88 4 History

discerned in the vulva (see folio RL 19102r, RL 19095r, RL 12281r). In Fig. 4.16,
Leonardo’s study on the female pelvis has been depicted and ovaries, tuba, cervix,
vagina, lig. teres uteri, lig suspensorium ovarii and lig. ovarii proprium and arteries
and veins for the ovaries can be discerned.
Rectum and sigmoid colon are presented in relation to the digestive tract in the
abdomen. Anal studies were performed (RL 19031r, RL 19098v, RL 19095r). The
blood vessels toward the pelvic organs are presented, together with the vessels that
continue into the legs (KK 6287r, RL 19098v, RL 19052r, and RL 12281r).
No drawing portraying the lumbosacral plexus could be found in this material.
Spinal nerves are shown in relation to the spinal cord in folio RL 19034v. A faint
concentration of spinal nerves can be noticed at the lumbosacral level, but the
nerves are not depicted in relation to pelvic organs (see folio RL 19114r and RL
19035r), but in relation to the nerves of the leg. Such pictures are present in the
sketches on sexual intercourse, but they all stem from before 1,500 and expressed
the Greek wisdom that animal spirit necessary for ‘‘good sperm’’ was produced
from arterial blood at the base of the brain, transported by nerves all over the body.
Hence a spinal cord connection over nerves toward the penis was depicted by
Leonardo [38].
Who had access to Leonardo’s anatomical drawings? The French court of
François I gathered poets, artists, and scientists such as Marot, Cellini, and Leo-
nardo. Leonardo’s anatomical drawings were known and the Cardinal of Aragon
studied them [37]. The French court stimulated anatomical drawings and publi-
cations [37]. Still Leonardo’s drawings did not appear in the court motivated
‘‘costly anatomical scientific texts’’ [37].
It seems safe to claim that, although Leonardo unraveled most of the soft tissues
present in the pelvis, his results did not diffuse into scientific circles or publica-
tions of those days (see also [39]).

4.13 The Route to Vesalius

In the early sixteenth century, arts and science changed rapidly. Painters such as
Botticelli, Michelangelo, and writers such as Machiavelli were at work. The
Lutheran revolt took place and Henry VIII left the Catholic Church. Columbus
journeys took place between 1492 and 1502. Anatomy was in the scientific front
lines of a changing world. As Leonardo had access to dissection, others had too. So
at the start of the sixteenth century, several scientists were at work in Anatomy.
Let us have a look at the results: 1532: Charles Etienne described the veins of the
liver, 1534: Sylvius and Vesalius found the valves of the veins, 1546: discovery of
the stapes of the ear by Ingrassias, 1548: detection of the muscles of the upper
eyelid, and 1542: Eustachius published his anatomical tables [33]. In 1543,
Vasalius published his Fabrica [4]. But what was going on, let us say, between
1480 and 1530?

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4.13 The Route to Vesalius 89

Allesandro Achillini (1463–1512) was a lecturer in medicine and philosophy in


Bologna and Padua. He described two of the tympanic bones: malleus and incus.
Moreover, he discovered the orifices of the submandibular salivary glands (later on
re-described by Thomas Wharton), the ileocecal valve, rediscovered the fornix and
infundibulum and the cerebral cavities. He was well acquainted with the Anatomy
of the digestive tract.
Berengario da Capri (1480–1550), who alleviated the syphilis plague and
worked also in Bologna, dissected more than a hundred corpses. He gave the
properties of muscles, ligaments, tendons and described the abdominal muscles
precisely, the vermiform process of the cecum, stomach, thymus, the sexual
organs, and the connections between the biliary duct and the duodenum. He also
studied the Anatomy of the fetus. Leonardo was taught Anatomy by Andrea
Mantegna (1431–1506), Antonio Pollaiuolo (1432–1498), and Andrea del
Verrocchio (1436–1488) [42]. Others that studied Anatomy were Antonio Ben-
ivieni (1443–1502) and Alessandro Benedetti (1455–1525) to name a few more.
It is inevitably that a clear continuity between medieval and early renaissance
Anatomy existed (see also [43]).
Thus, in the transition from medieval times to renaissance, Italian scientists
progressed enormously with the Anatomy of the human body. Printing by
woodcuts, in practice for books before 1450, changed into letter printing that
disseminated results in multiple specimens without visual losses due to manual
copying. At its boiling point, the struggle for the first modern printed overall
human anatomical description was between Vesalius’ Fabrica (1543) in Italy and
Estienne’s De dissectione (1545) in France.

4.14 Charles Estienne’s De dissectione (1545)

The court culture of François I (1494–1547) has been described to be sexist and
macho, but also stimulated art and science to ‘‘revitalize sense of national destiny’’
[37]. To be rephrased in more euphemistic wording: ‘‘Undoubtedly, these scien-
tific texts were influenced by the ‘sexualized’ culture of the court. The images of
the dissected female form to be found in Estienne’s De dissectione of 1545,…,
were not merely posed in an extravagantly sexualized manner, but they were
reinterpretations of a ‘key’ Renaissance erotic text: Perino del Vaga’s sequence of
engravings showing gods and goddesses copulating with another’’ [37]. This
explains the form of Estienne’s female anatomical pictures, sexualized females as
is said. But, what brought it out for the pelvic content (see Fig. 4.23)?
First we have to look into the production of ‘‘De dissectione partium corporis
humani libri tres.’’ It is an intriguing story. Estienne (Latin name Carolus Steph-
anus) turns out not to be thé anatomist. He was merely the publisher. Estienne de la
Rivière is the anatomist (1569) and probably Rosso de Rossi (1496–1541) con-
tributed to the production. By the way, Books 1 and 2 contain male full-page

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90 4 History

figures (48 in total), and only Book 3 full-page female ones (10 in total)! (Are the
male figures positioned macho too?)
‘‘One feature makes the illustrations in the De dissectione unique among early
sixteenth-century illustrations. Many of the full-page plates indicate that the ori-
ginal woodblock had been modified before the printing of the woodcuts. A central
portion of varying size was removed from the woodblock, a new piece of wood
inserted, and this new piece then cut to match the original surrounding block (see
Fig. 4.22). None of the 17 plates in Book 1 indicate that the woodblocks had been
modified. Of the 31 plates in Book 2, all but two indicate alteration. At least seven
of these have a second smaller insertion, which is not connected with the larger
insertion and represents an anatomical part associated with the parts depicted in
the larger inset. Of the 10 full-page plates depicting females in the third book,
eight have insets, and one of these has a second smaller inset. There seems to be no
record of a printing of the unaltered woodcuts’’ [47].
But the article goes on: ‘‘The original, unaltered woodcuts probably depicted
anatomical figures. Around the edge of some of the new insertions can be seen
remains of the original illustrations of anatomical parts. The remains of the ori-
ginal illustrations that appear in cuts in book two possibly indicate that the original
illustrations depicted figures in which the skin that covered the trunk was pulled
down over the thighs and up over the shoulders. This manner of revealing the
internal parts can be seen in such illustrations as the woodcuts in a 1541 edition of
an anatomical treatise by Mondino dei Luzzi ( 1326).’’ Marks on the plates
coincided with unaltered plates published in 1557 with the skin removed as above
indicated. The story still continues: ‘‘Kellet has shown that some of the females
depicted in book three of the De dissectione are strikingly familiar in position to
the females in a series of engravings taken from two drawings by Rosso and 18
drawings by Perino del Vaga (1500–1547)’’ [47].
Originally, Charles Estienne wanted to publish under his own name only and
involved artists for his plates. However, Estienne de la Rivière, a colleague sur-
geon, started a lawsuit and forced Estienne to indicate his name that organization
of the figures was his and his aid in dissection and incisions. Fraud is from all ages.
Is it wrong to suppose that Estienne, whose stepfather and brother were printers,
started a republication of Mondino’ book, but were overtaken by scientific
developments? He started his collection of plates before 1539. From marks and
dates on the plates, it is known that the production of plates started already in 1530
[47]. The law suit retarded publication till 1545, but the book was ready earlier.
Seemingly, anatomical developments, even in France, were going fast, and Rosso
di Rossi, coming from Florence around 1530 (who already produced anatomical
pictures in Italy) and Rivière understood that development, with the consequence a
renewal of the original plates and text in Books 2 and 3?
After this detective story, let us consider the content of the De dissectione.
Book 1 still keeps to the traditional ideas: A Mondino copy. The muscle man as
depicted is simple. However, at the end of Book 2, an extensive myology is given,
in which separate muscles are depicted and described. In the plate on page 59
containing the nerves of the human body, the lumbosacral plexus is demonstrated.

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4.14 Charles Estienne’s De dissectione (1545) 91

Fig. 4.22 This print shows female figure of Estienne’s De dissectione p 279. One line of the
insets of woodblocks (black arrows) and adaptations to original figure (yellow arrow) are
indicated. Reproduced with permission of the Leiden University Library

The spinal nerves of L3 till S4 contribute, while L5 till S4 constitute the sciatic
nerve (should be L4 till S3) and L3 till L5 the femoral nerve (should be L2 till L4).
‘‘The older literature around 1,900 discerned a reductive and a progressive
development of the vertebral column in the lumbosacral area. Increase in the
vertebrae in humans in this area could be found in over 1,000 human specimens
between 4 and 6 %, while reduction could be noted in nearly 3 % of cases.
A rough estimate is that in 10 % of the humans a diverged lumbar-sacral spinal
column is present. At least, this shows the presence of variability in the vertebral

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92 4 History

column and as consequence variability in the plexus lumbosacralis,’’ explaining


the difference with nowadays generally accepted results.
On page 134, the blood vessel system is given: a liver blood system and a heart
blood system are discerned. The pelvis received two vessels from the heart system,
while eight are connected to the liver blood system.
As we arrive into Book 2: The plates indicate the kidneys, now containing one
abdominal aorta and one vena cava next to each other. Ureters are correctly shown
together with their entrance into the bladder. In the plate on page 180, the arteria
iliaca com. left and right cross over the veins, which is wrong, since only the
arteria iliaca dexter crosses over the left iliac vein both left arteria and vein parallel
each other (see Fig. 3.7). The vessel connections toward the kidneys are in general
correct. The ureter’s vessels reaching into the pelvis are accurately depicted. End
branches of vessels or nerves of overview figures are always shown as curling lines
and endings are never given. The plates on pages 175 and 196 show the rectum,
tied and cut at the sigmoid colon. Page 196 figure text is interesting:
A: Picture of the branches of the vena porta that enter the rectum. Productio
rami a vena porta in rectum inserti.
B: Ligaments on which the rectum intestine is hung and is stuck onto the sacral
bones and lumbar vertebrae. Ligamenti quibus intestinum rectum appenditur and
adheret ossi sacro and lumborum spondylis.
Remember that Estienne discovered the veins of the liver in 1534 and he,
therefore, indicates here the superior rectal veins in part A. In B, the first
description of the rectosacral fascia is given (see Chap. 10).
The inset woodblock shows the male pelvic outlets and related organs:
1. Outside sphincter of the bladder supports the penis in erection. Sphincter
vesicae extremum virgam erectam sustinens.
2. Outside of intestine rectum descending into the anus. Extrenum recti intestine
in podicem desinens.
3. Muscles that keep the penis upright. Musculi virgam erigentes.
4. Other very small muscles toward the lateral side of the penis. Alij duo muscoli
ad virgae latera, minimi.
5. Muscles against the anus, near to sphincter. Musculi ad anum attinentes, praeter
sphincterem.
6. Ureter openings for entrance in the bladder. Ureteris pori implanatio in
vesicam.
The spermatic ducts are treated on this figure on page 189. The vas deferens is
topographically correct and the text translated freely as: ‘‘The connection of the
spermatic blood vessels, sometimes going away from the heart, and again toward
it, next to the os pubis,’’ ‘‘Coniugatio vasorum spermatic corum tam diferentium,
quam ad ferentium, iuxta os pubis.’’ This indicates some knowledge of supply
vessels and return veins for blood to the organ.
An extensive dissection of the pelvic bottom, with its sphincters and involved
muscles, is given here for the male, together with the spermatic ducts and bladder
with its entrance of the ureters.

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4.14 Charles Estienne’s De dissectione (1545) 93

Fig. 4.23 Two details of pelvic pictures of Estienne’s De dissectione (pp. 279 left, 281 right).
They are insets into the full-page plate. Reproduced with permission of the Leiden University
Library. For explanation see text

Here emerges a rather good topographical overview for that time of the ana-
tomical structures of the male pelvis.
Before going into more detail of the female pelvis, the plate on page 260 shows
how to manage a cesarean operation. A pregnant female is shown, while on the
abdomen, just beneath the umbilicus, to the left a slightly curved incision is indi-
cated. The figure text is freely translated as: A necessary manipulation to get the
male fetus out, after death of the mother, ‘‘Necessaria confection post extincta
matrem, ad fetuvirium extra hendum.’’ The first possible report of a ceasarian
section in which the child died, but the mother survived and afterward gave birth to
several more children is from 1542 [46], presumably in France. After 1588, a report
is noticed on which both mother and child survived a cesarean operation. The Swiss
mother brought 6 more children to birth among which a set of twins [46].
To return to the female pelvis, The secondary female sexual characteristics are
presented in plates on page 285 and 287, in which an opened vagina together with
the cervix is demonstrated, while on page 287, the exterior of the female genital
parts are given with the urethral orifice and entrance of the vagina. The text
belonging to the figures depicted in Fig. 4.23 are of pages 279 and 281 is given
below.
The text to page 279 figure (see Fig. 4.23) is:
1. Spermatic vessel, at the left side of the renal veins. Vas spermaticum, a sinistra
emulgente.
2. Spermatic vessel from the cava, below the renal veins. Vas spermaticum, a
cava, sub emulgentibus.
3. Tight connection of the spermatic arteries and veins, before they reunite near
the testes (=ovaries). Copulatio venae and arteriae spermaticarum, ante quam
ad testes perueniant.

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94 4 History

4. Testes(=ovaries), next to the horns of the uterus and interweaving of the vessels
around it. Testes, iuxta cornua matrices and implicatio vasorum circa ipsas
5. The wrinkling bottom of the uterus, covered with endless many loops of vessels
that even evoke cavities in it in the pregnant woman. Fundum matrices rugo-
sum, osculis vasorum infinites conspersum: quae quidem acetabula vocant, in
praegmantibus.
6. Ligaments [that care] for the inner muscles of the loins, by which the uterus is
fastened around the vertebral column. Ligamenta musculos lumborum internos
operientia, quibus maxime uterus confirmatur circa spinam.
G-I are present on the inset woodblock containing among others: umbilicus (K),
allantois membrane (H), and vessels of chorion (I) (see Fig. 4.23).
The description and figure tell about the intermingling of the ovarian arteries
and veins, and where they originate. The inside of the pregnant uterus with its
blood vessels is described, while the inset shows the membranes of the fetus
together with the placenta and the umbilicus. In F, the idea is brought forward that
the psoas muscles, and perhaps, the crus sinistrum and dextrum of the diaphragm
do have connections to the backside of the pregnant uterus to keep it in place
against the vertebral column.
The text to page 281 figure is (see Fig. 4.23):
1. Insertions of the major veins in the uterus, together with the upper part around
the top of it. Implantationes duae a maiori vena in corpus matrices, anteriore
parte circa eius summii.
2. Start of the vein and the artery that enter into the uterus, sometimes toward the
vulva, but also to feed fetus, is thereupon twined. I think that one sees that the
artery of these vessels ascend with small arcs. For people say that the vena recta
ascends tortuously in front of the artery and from many places enters the wall of
the vulva, thus from the cervix to the horns of the uterus. The vein can enter at
the same places, but is more straight and splits at the top of the uterus;
therefore, it is considered larger or much voluminous special in the pregnant
woman, whose time for delivery is nearing (compare with Fig. 3.7).
Origo venae and arteriae in corpus matrices dispersae, tum ad ipsam vuluam
tum etiam ad fetum enutriendum, ex quibus secundina contexitur. Horum va-
sorum quod vidis per meandros sursum discurrere arteriam effe putato. Nam
vena recta sursum fertur, arteriae aute, anphractuose in multos locos dispersa,
and a multis locis per vuluae latus ipsum ingrediens, nempe a ceruci matricis ad
cornua. Vena totide habet ingressus sed rectius progeditur, and quod in imo
utero distribuit, id multo maius ac capacius esse videtur, praesertim praegnante
muliere, and cui proximum est purgationis tempus.
3. The place where the vessels beneath the horn enter and they proceed from this
place through the inner substance of the uterus, until they reach the cervix of
the uterus, which has been depicted at the second little stick. Locus in quem
vasa sub cornibus ingrediuntur, ea autem a praedicto loco par internam matricis
substantiam discurrentia, utque ad cercuicem uteri porriqantur, quod vides se-
cunda virgula depictum.

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4.14 Charles Estienne’s De dissectione (1545) 95

4. Vein and artery descending from the largest vessels toward the rectus muscles
in the epigastricum, where they end: especially in the woman well to see. Vena
and arteria a maioribus vasis ad rectos musculos epigastrii demissae, dum in
suo situ sunt: praecipue autem conspiciuntur in muliere.
5. Site of the rectus intestinus, as it is in the pregnant woman. Situs intestini recti
qualis est in muliere gravida.
6. Site of the bladder. Vesicae situs.
Do we see here a good description of the vena and arteria uterina together with
their role during pregnancy? Moreover, the epigastric vessels on the backside of
the m.rectus abdominis seem to be placed topographically correctly.
At least, a good try for the topographical description of the vessels of the female
pelvis is produced.
Why this extensive treatment of Estienne’s De dissectione? Firstly, to establish
that accurate anatomical data indeed are presented in the De dissectione as has
been shown above for pelvic structures (see also [48] and note [48A]). Most of the
articles on Estienne’s work concern the figures and hardly any substantial foun-
dation for the correctly collected anatomical data has been given in literature. The
trifling case of the seven-boned sternum that Estienne correctly dismissed, as
Vesalius did, that both put into figures, but denied in different ways in the text,
hardly contributes to what kind of good Anatomy was produced in the De dis-
sectione. Estienne was the first to collect and depict ‘‘modern’’ anatomical results,
as proved above.
Only a few years later (1537–1542), Vesalius did his dissections for his Fabrica.
It could indicate, since De dissectione was ready earlier (1539–1540) than
Vesalius Fabrica (1542–1543), that either the dissemination of anatomical
knowledge was fast or the creation of new data occurred at different places at the
same time or both (see also addendum to this chapter). The explanation, however,
is simple and banal: both were students of Sylvius and Vesalius knew some of the
figures Estienne had already printed before 1539. Vesalius was well aware of
Estienne’s work [48B]. That is why he traveled in a hurry over the Alps in
midwinter, rather dangerous, to reach Basel for the printing of his Fabrica. There
surely must have been a mutual rivalry, which is supported by a letter of Vesalius
in 1542 in which he complained that his first three plates were copied in Paris.
The anatomical results in Estienne’s Books 2 and 3 are for that time modern and
partly new. While Book 1 belongs still to the ‘‘unchecked reissues of ancient
anatomical manuscripts,’’ Books 2 and 3 are not. We know that around 1530, the
work was started as a n edition of Mondino. Somewhere after its start, anatomical
information gathering changed. One should remember that Estienne described the
veins of the liver in 1534 as a new discovery. Based on this, the break between
reissuing and dissections for new data occurs between 1530 and 1534, and that is
exactly the time Estienne spent in Padua to study Greek, botany, and natural
science, which is the same place where Vesalius (arrival in Padua, September

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96 4 History

1537) was appointed professor in Anatomy three months after his arrival. It
therefore seems that Padua between 1520 and 1550 have to be focussed on.

4.15 The University of Padua and the Rise of Anatomy

The University of Padua was founded in 1222, although some doubt is present on
the exact date [62]. The year 1222 has been taken because in that year, students
and professors escaped Bologna, due to problems with the city council and found a
welcome in Padua, supported by the bishop of Padua. Its medical (natural history)
studies were started around 1250 [62]. Here, we will not discuss the ups and downs
of its history, it suffice to say that Padua was conquered by the city of Venice in
1405. It was already a well-known university and wise politics of the Venice
council made the university more prosperous, the more so, because Padua became
the official university of the Venitian republic [49].
Characteristic of the assembly of students and professors, called University,
was the enormous liberty and support in Padua. Students at the start of the Uni-
versity chose their professors. Arbitrariness of city or other administrators was
unacceptable, although bishop and Pope stayed protector of the university, but also
were ecclesiastical authorities: the ‘‘formal source of all licentiates and doctorates
granted therein’’ [62]. Students were protected against extortion against extor-
tionate landlords. A social and financial protectionism was present for students
from abroad by their ‘‘universitas ultramontanorum,’’ the society of trans-Alpine
students. Students could rent money from the student’s city bank for 4–6 %;
normal was 10–15 % [49, 52]. There was no city tax and no toll for entering or
leaving the city for students [49]. Professors earned good salaries.
Influence on the lecturing of the professors by (papal) administrators was hardly
accepted, although Peter of Albano, who taught astrology and medicine around
1306–1316, had difficulties with the Inquisition. The system used was that each
lecturer had an opponent, who was involved in the disputation, the discussion, on
what was presented by the lecturer in his lectio. Professors could not be absent
more than two days a month (except medical doctors) and the roll (rotulo) indi-
cated when lectures were held. So professors could not shirk their duties.
In this landscape of liberty and duties, together with a strong financial support
early by the city and later on by the council of Venice, science flourished, so that
Padua became well known over whole Europe. To indicate the longlasting effect:
from 1553 to 1630 in total 10,536 students from Germany alone studied in Padua,
not speaking of the French, Italian, and English students [49]. Around 1230, the
university already had over 2,000 students.
At the end of the fifteenth century, Padua had 10 professors of medicine. Four
professors taught theoretical medicine, four practical medicine, and two surgery.
Of the last two, one had to teach Anatomy. This increase is enormous, since in the
thirteenth century, only three were present, while the total of professors hardly

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4.15 The University of Padua and the Rise of Anatomy 97

exceeds 30 through these ages [49]. It shows the importance of medicine, which is
not so astonishing in view of the regular epidemics sweeping over the countries.
A study in medicine in Padua, at the end of medieval time, was four years and
entailed a requirement to study theoretical medicine: authoritative texts like Galen
and Avicenna, but also Aristotle and practical medicine: dissections, the secrets of
pharmacy, and instruction at the bedside [49]. The last approach was absolutely
modern for that time.
One could get into a historians wasps’ nest, if involved into the discussion on
the continuity of science from the Middle Ages into the Renaissance. Some
advocate an absolute break, others a (partial) continuum [50, 51]. However, both
streams, happily enough, agree on the continuation of surgery and anatomy [50]
from the Middle Ages into the Renaissance period.
We should be aware that Anatomy is a data-collecting science, like botany. By
the way, there is nothing wrong with pure data collection, but if that is done badly
or insufficiently, one gets serious scientific troubles, as some authors in medieval
times showed us. Functional aspects are brought forward in physiology, and
although this distinction is very weak in the Middle Ages, still it is present.
Surgery and anatomy were more allied in those times. Therefore, initially, new
functional statements hardly are to be expected from anatomy. Once the normal
human heart has two chambers (medieval times thought three), one can verify this
by simply taking the human heart and checking. One can do it a thousand times
and as long as two chambers are found there are two present. You do not need
higher mathematics, as astronomy did. Anatomy is always thrown back on itself.
The medieval anatomical data collection stem between Galen and Avicenna and
from those scholars and practitioners treated above in the part on dissections. Any
anatomical discrepancy noted can easily be verified. How come those discrepan-
cies were just studied in Padua?
The classical model of studying modern science [53] is derived from
‘‘Aristotle’s Posterior Analytics, especially book 1’’ [53]. His work was translated
from Greek into Latin around 1265 by the Flemish Dominican William of
Moerbeke (1215–1286). Before this, only translations from Arabic by, e.g., Gerard
of Cremona (1114–1187) were available. Discrepancies in text are to be expected
and those were studied mostly by theology. Its old technique was to explain an
authoritative text (glossing). They produced statements from it: a gloss. The results
were coupled to the existing material. This set of results (=sententia) were put into
lexicons [54].
The change in approach occurred in Paris. Abelard (1142) became a famous
theologian, but not earlier than after a disputed love affair. Being member of the
council of the cathedral Notre Dame, he could live in the house of Fulbert, another
member of the council. As a contra achievement, he should be teacher of Heloise.
Fulbert was the uncle and guardian of Heloise. Abelard abducted Heloise and she
gave him a son in Brittany, to where they fled. Fulbert insisted on their return and
Abelard marries Heloise. However, suspicion on the real act of marriage and the
constant denial of Heloise to be married with Abelard makes Heloise’s family and
Fulbert furious, the more so because Abelard brought Heloise back to the convent

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98 4 History

where she grew up and made her a nun. So, Abelard stole Heloise’s virginity and
even divorced her by bringing her to a convent. Abelard was ambushed within the
precinct of the Notre Dame and castrated by confederates of Fulbert and
the family. He fled to the cloister of St Denis, which was under protection of the
French king, and later became monk in Cluny, where he was untouchable by
authorities. In St Denis and Cluny, he starts his new theology [56].
Abelard came up with critics on the procedure of glossing and ‘‘called for the
construction of an academic theology through speculation. No intellectual prob-
lems caused by the tension between understanding in search of faith or faith in
search of understanding could be resolved by the endless accumulations of quo-
tations from authorities. Intellectual effort was needed. The philology (study of
Greek and Latin texts) of the liberal arts became philosophy. Logic and dialectic
became all-important as the prime means of rational technique. They helped
toward an adequate understanding of a structure of words and meaning, and the
resolution of existing contradictions’’ [54, see also 56].
This is nothing else than a change in methodology. Medieval scholars seem-
ingly adapted this method to get better information out of their authoritative
manuscripts.
‘‘However, in the new intellectual movement of the time the future belonged to
rational methods, even more so after the West had been made familiar with the
works of Aristotle. The seven liberal arts were transformed into scholastic phi-
losophy in the course of interpretation of Aristotle. Albertus Magnus (1280,
studied in Padua around 1220) did great service for theology here; Thomas
Aquinas (1274) completed the interpretation of Aristotle in theology’’ [54]. The
consequence was that a new methodological approach for studying theological
science was now introduced and accepted by the Christian society and thus could
be in practice by the other sciences, without any friction with other or higher
authorities. And it is Aristotle’s methodology, which is in principle still in use
nowadays [53].
‘‘Most importantly, the physicians of the University of Padua surpassed
scholars in other universities in their desire to develop a methodology of scientific
proof and discovery. Beginning around 1,300, Paduan professors of medicine, all
trained in Aristotle’s logic, began a 300 year philosophical tradition’’ [55B].
The only thing that must happen now is bumping into discrepancies in ana-
tomical facts and to apply the Aristotle method. Where do you run into a lot of
problems? Correct, in a place where a lot of medical research is done? Padua had
the highest amount of medical professors and a lot of anatomical research [62]
together with sometimes adequate therapies.
The professors in medicine studied the authoritative manuscripts and gave
comments to it: Pietro d’Albano (1250–1315) translated the works of Hippocratus
and Galen in Padua; he was capable to read the works of Aristotle in Greek. He
tried to apply Aristotle’s dialectics on medicine. Questions, such as is pain a
symptom or a disease in itself, is the head created due to the brain or the eyes, do
nerves originate from the heart or the brain, and do veins originate in the liver,
were treated [62]. For Pietro, pain was a symptom and nerves originated from the

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4.15 The University of Padua and the Rise of Anatomy 99

brain and ‘‘he also thought the nerves responsible for the movement of muscles’’
[62]! The Canon of Avicenna was commentated upon by Gentile da Foligno,
working in Padua from 1337 till 1345 [62]. Consilia (medical consulting books)
were produced by Ugo Benzi (1376–1439), Antonio Cermisone (d. 1441), and
Bartolomeo Montagnana (1422–1460). Books on the plague were produced by
Pietro Tossignano (1376–1410) at the end of the fourteenth century and by Jacopo
d’Arqua, working in Padua from 1356 till 1384 [62]. Books on alcoholism,
hygiene, use of the wells of Padua for sanity, and application of pharmaceutics, to
name some, were produced [49]. Below it, are always the questions on fundaments
of science, as expressed in the type of questions of Pietro d’Albano [62].
The answers produced on those research questions are hardly to understand
nowadays, but one should appreciate that the frame work within and the instru-
ments scientists were working with were strongly limited.
As explained before, the method of Aristotle brought up modern science. From
1492 till 1497, Francesco Cavalli was appointed professor exclusively for the
Greek texts of Aristotle and he was succeeded by Niccolo Leonico Tomeo
(1456–1531). It shows how important Aristotle’s manuscripts were for the sci-
entific community and how it was absorbed in those circles. Even in the fourteenth
century, the study of Aristotle was already flowering [62]. Padua, indeed, had a
long tradition in the study of Aristotle.
The results we have already seen in the part ‘‘The route to Vesalius’’: ana-
tomical contradictions were studied with dissections.
Three important anatomists have to be named that smooth the way for modern
Anatomy by their analytical method in Padua. The professor in medicine Gabriele
de Zerbis (1445–1505), known even in Constantinople, wrote a book on the
Anatomy of the human body in Padua. He questions the correctness of the
descriptions of Galen and the Arabic books. He is the first gerontologist who
indicates how to cope with aging. It is Gabriele de Zerbis who laid the fundament
of the critical anatomical period to come, based on his methodological approach of
problems. He explicitly says that if literature brings up problems: go and see by
yourself! [55] Marcantonio dalla Torre and Alessandro Benedetti walked the same
way. ‘‘These men were the first to gain some insight into new anatomical truths
and new physio-pathological concepts, so that they realized more and more the
need for a return to experimental Galenic medicine, rejecting the traditional errors
of Arab Galenic doctrines’’ [49]. Benedetti was the first ‘‘to base his clinical
opinions on the results of pathological anatomical dissections, and for this purpose,
he devised the first anatomical theater that could be dismantled. So it was that in
the second half of the fifteenth century, in great part owing to the contribution of
Benedetti, there began great reform in medical science which had as its basis in the
observation of nature and the examination of the patient’’ [49]. One of these three
will be exemplified, and of course, we cannot avoid Benedetti due to its impor-
tance as indicated above.
Alessandro Benedetti (1450?–1512) published ‘‘Anatomice or the history of the
human body.’’ In it are pelvic chapters on: the seminal veins, semen, testicles,

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100 4 History

scrotum, penis, bladder and its ducts, seminal vessels of women, the sexual parts of
women, the menstrual flow, and on the anus.
His description on the ureters that are passing through a double-walled bladder:
‘‘The ducts are not opposite each other since the urine would sometimes be forced
to flow back to the kidneys when the bladder is full: but the more the latter becomes
filled the more the membranes mentioned are compressed and thus they contain this
liquid refused’’ [58], shows the function of the sheaths of Waldeyer, around the
entrance of the ureters, and is functionally well described and in origin Galenic. A
clear distinction is made between the trigone and the detrusor, which is based on
Aristotle. The difference in length between the female and male urethra is dis-
cerned. As a consequence, ‘‘women are less afflicted by stones in the bladder’’ [58].
From Lind’s translation, we take [58]:
On the Menstrual Flow
A few words remain to be said about the menstrual flow of women and its origin.
Aristotle calls it nothing but semen that has not been concocted. From the regions above
and below the kidneys and from the loins the menses come forth in very small veins to the
cotyledons of the vulva by which the fetus is nourished in the uterus (as often been said) or
at childbirth near the mouth of the vagina from two veins following the pubic bone near
the place where the urine issues. From this part the non-prolific semen of women is poured
forth in coitus, as I have said, with so great an impetus in many that it spurts out farther
like semen of males, of a different nature at any rate from that prolific semen which
overflows in the hollow of the vulva, as I described at greater length above.

While his description on bladder and his ducts, for instance, is anatomically
correct, here we still see the reverting to Aristotle’s descriptions. Nevertheless,
Benedetti describes here, presumably for the first time, ‘‘the secretion of moisture
in the vagina during coitus’’ [58] see also Sect. 6.4: G-spot, but also the female
urethral ejaculate at orgasm. In Padua, the study of Galen was paralleled with
experiments and dissections to verify the Galenic description, due to the inherent
new methodological approach. The results were a revival. This spread like a wild
fire and attracted students and scientists to Padua, among them Charles Estiennes
and Andreas Vesalius.
A small excursion to England is still needed. A lot of students from England
studied in Padua. ‘‘William Grocyn (1446–1519) and his lifelong friend, Thomas
Linacre (1460–1524), supplied the first links between the classical revival in Italy
and England, between the University of Padua and the University of Oxford. But
the pioneer belonged to the younger generation. It was Edwardes, the little-known
scholar and fellow of the Corpus Christi College, Oxford, who was responsible for
the two significant milestones; the first recorded dissection of a human body in
England about 1531 and the first book on anatomy written in England and pub-
lished a year later’’ [57]. Linacre’s translations from Greek into Latin made
Galen’s books available for the English scientists. Linacre was also physician and
his colleagues Clement and Wotton taught at Corpus Christi College, where
Edwardes (d. 1542) was influenced by the classical revival. He went to Cambridge
and lectured there and practiced as a physician. The booklet on Anatomy got
nearly no interest among surgeons and physicians. After this weak effort for

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4.15 The University of Padua and the Rise of Anatomy 101

revival of Anatomy, interest in Anatomy waned: ‘‘Whereas the medical faculties


of continental universities came to accept anatomy, such was not to be the case
with English medicine until well into the seventeenth century’’ [57]. The same
holds for Anatomy in Germany [58].
At the end of this part, some remarks should be made on Bologna. Lind [58] in
his book on ‘‘Pre-Vesalian Anatomy’’ advocates that the place to be for Anatomy
in those times was Bologna. ‘‘Padua, the great rival of Bologna, was the next most
significant center for anatomical studies and as a university center of the Venetian
Republic provided an appropriate environment for Benedetti, Massa and Zerbi,
who were professors there. Achillini, the Bolognese, also taught there from 1506 to
1508’’ [58] (Note Niccolò Massa [1485–1569], who studied in Padua and stayed in
Venice, published in 1559 and thus is outside the time frame of this part of this
chapter). Nevertheless, Randall4 addendum stated that the center of the new research
was Padua and not Bologna. Let us follow Siraisi [39] in her statement that it is not
productive to go in such comparisons between cities, the more since there was an
extensive exchange in professors and science between both cities.

4.16 Contribution of Surgery to Anatomy

Surgery extended from the twelfth century onward with good practice in head,
neck, and extremity wounds [33]. Most of the experience was gathered on battle
fields. As indicated above, a strong intermingling was present between Anatomy
and Surgery. To split it up is not productive [62]. Medieval surgery books show
that medieval knowledge of the soft tissues in the pelvis was not insignificant.
A few texts from Wilhelm of Saliceto (±1210– ±1277) are taken to show what
knowledge was present concerning pelvic structures (freely translated of course).
The description of the piece before the part cited below ends with the bony pelvic
structure: the os ileum.
From Book 4, chapter 4: ‘‘On the anatomy and form of the intestines from the
cavity of the stomach to the hips and the vertebrae at that place’’.
But from the ligament or its ligaments appears an innervated body, which looks like a
tendinous structure (ligament is used in the text). Below and in this tendon (-like structure)
many and large arteries and blood vessels are present, more than should be needed for its
volume. This body full of arteries, blood vessels and nerves is the penis. Its top, of which
the membrane is rather sensitive, is covered with skin that protects against injuries from
outside. And due to the friction of the skin over the head of the penis and also by its
moving about, the biggest pleasure is obtained during coitus, by which better sperm
appears and by which the sperm ducts by the extend of the moving about, better ejaculate
and (forces) the sperm ducts to push it outward.

There are two more ducts originating from the (area of the) omentum (siphac) going
downward, and when the scrotum expands two small tunics arise in which the testes are
present. Also, here at the backside of the testes, blood vessel branches come together, that
proceed from the kidneys, which turn several times around each other. They are sur-
rounded by flesh that are rich of glands and white (substance). Here at this place

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102 4 History

everything that is blood turns into white (substance). The flesh conducts this white
(substance) towards the testis, where sperm is produced’’ [59].
But in the woman, on the spot of the male penis, one finds the head of the uterus and
that is why the womb is full of nerves, in order to expand and enlarge. In the woman the
head of the womb is made of an innervated zone, that can enlarge on the moment of
delivery and always when necessary. The womb has here two additions, that are called
tubes and under these additions she has testicles, with the form of a penis upside down.
The neck of the head of the womb touches the testicles on the moment of sperm emission.
The womb neck contracts in order that sperm is pushed better into the direction of the
womb and its head. The uterus is exactly localized in between the colon and the bladder.
The womb is longer than the bladder and is connected to the vertebral column and the hips
by flexible ligaments. So, free movement (of the womb) is possible and can enlarge
especially during pregnancy and delivery [59].

From Lanfranc of Milan (1306) chapter 8 from his second treatise we take the
part on the bladder.
The bladder exists of two membranes, both full of nerves and the bladder has at its lower
end a fleshy neck, which is long in males and continues into the penis and passes through
the peritoneum. In the woman the neck is short and continues in the vulva. On both poles
of the bladder run the ureters. Near the neck they perforate a mantle and the urine that
enters, by its natural movement, through that opening ascends a little between both
mantles. At the inner side the mantle is perforated and the urine enters the bladder cavity.
Due to the filling of the bladder both mantles are closely put together. And because both
openings are not placed directly opposite of each other, no urine can go backwards into the
ureter, except if the bladder neck is so tightly closed, that nothing can pass. Man will have
enormous pain because the urine moves up backwards. And I, myself, am acquainted with
the pain of stones, until I knew the remedy. The bladder neck has one muscle, which opens
above its own opening and in the healthy human continence is carried out by its own free
compulsion. Relaxing (turn loose) the muscle urine comes out with the help of the
abdominal muscles.

The wounded bladder does not scar and this wound bites, ulcerates and rust. Hippocrates
did know this when he said: The incised bladder or brain or heart or liver or stomach or
intestine or diaphragm or kidneys or lungs are all deadly wounds. (Nowadays the bladder
cures fast, due to catheter use. Urine is responsible for the development of fistulas.)

When a doctor is called to a patient, who is wounded in these parts, he cannot leave. I
advise, that if the doctor in his region is already long time known as a good human being
and with good reputation and his reputation is known for a long time due to his good
operations, than it is opportune that he makes a diagnosis of a deadly wound for the family
and if the patient asks constantly for it, always promise his recovery [59].

If one compares the pelvic anatomical descriptions of Wilhelm of Saliceto,


Lanfranc of Milan, and Alessandro Benedetti they are qua content equal and
contained most pelvic soft tissues. Knowledge on pelvic anatomy is hardly
advancing in the thirteenth, fourteenth, and fifteenth century by surgeons.
Here, we come back to syphilis. Degeneration of the nose was well known due
to this disease (see portrait of De Laresse by Rembrand). Medieval surgery went so
far that skin flaps were put on the degenerated nose parts to restore the patients
face. First the text of Hugo and Theodore of Lucca (1205–1298) from Book 2
chapter 10 where Theodore deals with treating injuries of the nose by weapons:

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4.16 Contribution of Surgery to Anatomy 103

On the injuries of the nose

If the nose has been cut by a sword or a similar weapon, in such a way that it hangs wobbly
and in the case it is trusted to you, before it dies off, you have to be careful and cautious.
Place the nose back, as good as possible at the correct position, after you have first, if
necessary, the parts brushed up a little, to reunite them better. Then, with sutures you stitch
them together. After ending the suturing and the nose is at the correct place, one takes
gauze or rolls of soft flax, which are rolled slowly in gauzes and plunge them in very hot
wine. Than after you have them squeezed well, put them into the nostrils. They have to be
of proportions and length that they cover the whole wound, in such a way that the spongy
parts of the nose and its external parts are kept well in place and the patient can endure
them without too much pain [59].

In 1442, Branca da Branca developed the first rhinoplasty. It was applied but
kept secret in the family for two generations. The Branca family used the cheek or
forehead skin, called the Indian technique, where it was discovered, but also
developed the pedicle-flap using the arm skin. The same technique was described
by Heinrich von Pfolspeundt in 1460. Leonardo Fioravanti (1517–1588) traveled
through Calabria, after the last crusade. Here, he learned the Branca technique
from the Vianeos brothers, being local barber-surgeons. Finally, Gaspare Tag-
liacozzi (1545–1599) brought it to fame (by binding the patient’s arm to the nose
he used the skin flap for recovery) and published it (1597), but the technique was
forced to stop on religious grounds [60, 61].
It is clear that suturing, antiseptic treatment, and even plastic Surgery were in
use in late medieval times. However, injuries of organs of the thorax, abdomen,
and pelvis were hard to cope with.
Before we can go over to the last part of this chapter on the seventeenth-century
scholars, some remarks still are needed. The reader must have noticed that within
the citations from Middle Age texts on the anatomy of the pelvic content,
‘‘comparable descriptions’’ are given (e.g., uterus or entrance of the ureters into the
bladder/sheath of Waldeyer), indicating a restricted amount of sources. One should
note that not all the works of Aristotle (384–322 BC) were circulating during the
early Middle Ages. The Corpus Aristotelicum contains the works that were known
in that time. In it were the parts called: history of animals, parts of animals, and
generation of animals that treated among others the male and female generative
organs. From Galen, also not all anatomical works were known. The books I–IX
(from IX only the first 5 chapters) of ‘‘On anatomical procedures, De Anatomicis
Administrationibus’’ (an ape dissection guide) were in corrupted form acquainted
with; however, the other books came not earlier available in Greek than in 1525
and in Latin in 1531. These last books contained book XII: The generative organs
and fetal development. Galen’s other large work on Anatomy and Physiology, as
we should call it now: ‘‘On the usefulness of the parts of the body, De usu
partium,’’ was only partially available in Arabic; the corrupted version was
translated by Burgundio of Pisa around the end of the twelfth century. Only the
first twelve books were deciphered, but book 14 and 15 contained the information
on the reproductive tract and fetus. After the discovery of the original text, Pietro
d’Abano in 1310 and Niccolò da Reggio in 1317 provided a Latin translation.

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104 4 History

Therefore, in the early Middle Ages, an Aristotelic Anatomy was kept, while in the
late Middle Ages, Galen’s contribution was consolidated and extended. Here, it is
not the place to do comparative anatomy of the content of these classical books:
who contributed what to pelvic anatomy during the Middle Ages and what kind of
anatomical facts were contributed by the Middle Age scientists themselves? They
did contribute, as shown, with as a starting point the sources on hand that produce
comparable description by the Middle Age copying culture, due to the same basic
books.
Moreover, by reading Galen’s ‘‘On anatomical procedures I–IX,’’ one cannot
escape the idea that good Anatomy was known, although being ape Anatomy, but
the overlap with humans is rather large. This in contradiction to all those remarks
on differences between apes and humans: the surgeon and anatomist did know the
muscles, organs, bones, most of the main vessels and nerves [68A], although not
functionally. This again supports the view that Renaissance anatomy had a solid
foundation in Medieval Anatomy, also due to transmission of the classical ana-
tomical sources.

4.17 Contribution of the Seventeenth-Century Scholars

After the Renaissance works of the Italian anatomists such as Gabriel Fallopius
(1523–1562; all body parts), Giulio Aranzi (1530–1589; embryology), Hierony-
mus Fabricius ab Aquapendente (c1533–1619, anatomy, physiology, and embry-
ology; Teacher of Harvey in Padua), Giulio Casserio (1552–1616, ear), Adriaan
van der Spieghel (1578–1625, embryology), and Gasparo Aselli (1581–1626,
lymphatic system), the anatomical research shifted from Padua and Bologna to the
North, especially to the Netherlands and Leiden (Petrus Paaw, 1589–1617; Otto
Heurnius, 1618–1650; Joannes van Horne, 1651–1670; followed by Charles
Drelincourt, 1633–1697; Antonius Nuck, 1650–1692; and Govard Bidloo,
1649–1713). It was van Horne who taught De Graaf, Swammerdam, Ruys, and
Steno [69]. An enormous and widespread literature exists on Leiden anatomy in
the sixteenth till eighteenth centuries, which we will not repeat here. Instead,
highlights of Leiden studies on reproductive organs will be given.
In the seventeenth century, the internal pelvic organ descriptions become
definitive mainly due to the students and successors of van Horne. Drelincourt
studied the changes of the uterus during pregnancy and described fetal develop-
ment. Nuck is known for the cyst of Nuck. Studying the inguinal anatomy, he
found the possibility of cyst formation along the lig. teres in the labia majora.
Here, we concentrate on the studies of the female pelvic organs, but the same
results hold for the male ones. The female internal pelvic organs are described in
extenso by Regnoldus de Graaf (1641–1673; Fig. 4.24) and Jan Swammerdam
(1637–1680). Ovulum and ovulation of the female are discovered. External and

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4.17 Contribution of the Seventeenth-Century Scholars 105

Fig. 4.24 Regnoldus de


Graaf’s (1641–1673) figure
VII taken of ‘‘Alle de
wercken, so in de ontleed-
kunde als andere deelen der
Medicyne’’ (1686)
concerning the female
reproductive organs,
reproduced with permission
of the Leiden University
Library

internal sexual organs are depicted and studied. De Graaf examined the clitoris
(see Chap. 6, Fig. 6.4), indicated blood vessels and nerves in relation to the female
reproductive organs as Swammerdam did. Ligamentous connections are given.
Although others in the North contributed to the anatomy of the pelvic organs (e.g.,
Bidloo see above), it is undeniable that de Graaf ‘s and Swammerdam’s work
founded the authoritative topography, mesoscopical, and partially the microscopic
properties of the female and male reproductive organs.

4.18 Conclusion

The study of the internal pelvic organs got, via medieval and Italian knowledge, a
definitive understanding of its construction plan in the seventeenth century in the
Netherlands, exemplified here by the female reproductive organs. At the same
time, the study of the bony pelvis made an unhappy start, because it was based on
faulty data. It is noteworthy that this difference is still perceived at the subclinical
level in our times, where paramedical professions do not comprehend the con-
struction plan of the bony pelvis (see remarks on midwifery and physiotherapy in
Chap. 1) see remark [63A].

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106 4 History

Literature

Literature has been grouped in reference lists of several chapters in those cases where
arguments are difficult to entangle or published over several articles or books. In cases of
citation the article or book involved is indicated by the reference number together with a
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Tijdstroom, Lochem
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uitgevers, Leyden
15. Hendrik van Deventer (1739) Beschrijving van de ziektens der Beenderen en in zonderhijd
van de Rhachitis of Engels Ziekte etc. Benevens nieuwe ontleedkundige aanmerkingen:
Nagelaten aantekeningen, vertaalt en uytgegeven door Gerardus Dicten, te Leyden bij Joh.
Arnold Langerak

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Literature 107

16. Raulin J (1770) Instructions succintes sure les accouchments en faveur des Sage-Femmes
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Bidloo’s Anatomia humani corporis 1685. Tschr Gesch Gnk Natuurw Wisk Techn
8:4:187–208
18. Dumaître P (1982) La curieuse destinée des planches anatomique de Gérard de Laresse.
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stage and studio, pp 212. Amsterdam University Press; Sanders MA (2005) William
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chirurgicarum centuria. Dutch anatomists and the bifid spine. Utrecht University Museum.
Hellas and Rome Publication, Utrecht
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study. Thesis Utrecht University
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tabulae. In Nuyens BW. Th, Schierbeek A (eds) (1955) Opuscula selecta neerlandicorum
de arte medica XVIII, De erven F. Bohn N.V., Haarlem
22. Folkerts JF (1946) Spina bifida, diplomyelie en enuresis nocturna. Een klinische
anatomische studie. Thesis Amsterdam University
23. Oosterhuis HJG (1972) Klinische neurologie. Oosthoek, Utrecht.
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Garrison FH (1966) An introduction to the history of medicine. Saunders Co, Philadelphia
25. Liepert S, Ruecker S (2005) Voluntary and irrational action: the implications of body
theory for design research. Int Conf Eur Acad Design: ead006_cd_rom.zip
26. Judovitz D (2004) The culture of the body: genealogies of modernity. University of
Michigan Press, Ann Arbor
27. Guttenplan S (1995) A companion to the philosophy of mind. Blackwell, Massachusetts
28. Gardner M (2001) The annotated Alice, Lewis Carroll, Penguin Books, London and
Phillips R (1971) Aspects of Alice. Pinguin Books, Harmondsworth
29. Gray’s Anatomy (1975) 35th edn. pp 351–352, Longman Group, Edinburgh
30. Braus H (1929) Anatomie des Menschen. Springer, Berlin
31. Hafferl A (1969) Lehrbuch der topographischen Anatomie. Springer, Berlin
32. Garrison FH (1966) An introduction to the history of medicine. Saunders Co, Philadelphia,
see also O’Dowd MJ, Philipp EE (1994) The history of obstetrics and gynaecology.
Parthenon Publication Co. NY Note: T. Hunt in The medieval surgery (1992) Boydell
Press, argues ‘‘The illustration is a puzzling exception to the artist’s normal practice, that it
appears to depart from the accompanying text, which deals with neckwounds, where the
injury has been caused by a sword or similar weapon…A thorough investigation must be
made by digital palpation and this is what is depicted in the illustration; only the site of the
injury has been transferred to the abdomen, possibly to make the illustration clearer.’’,
which seems highly improbable. ‘‘It is not certain whether the instrument in the doctor’s
right hand is a probe, a scalpel or (more probably) a needle for stitching the wound’’. The
same instrument can be found in Lanfranco of Milan and in Theodor of Lucca in their
pictures. It concerns an elongated knife
33. Cumston CG (1987) An introduction to the history of medicine. Dorset Press, NY

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108 4 History

33A. Park K (1994) The criminal and saintly body: autopsy and dissection in Renaissance Italy
Renaissance Quartely 47:1–33; see also Park K (1995) The life of the corpse. Division and
dissection in late medieval Europe. J Histo Med All Sciences 50:111–132
33B. Corner GW (1927) Anatomical texts of the earlier Middle Ages. Carnegie Institution
Publication 364, Washington
34. Dempster WT (1934) European Anatomy before Vesalius. Ann of Med History. Vol VI
35. Lindberg D (1992) The beginning of Western science. University Chicago Press. See also:
M.Mc Vaugh (2001) Cataracts and hernias: Aspects of surgical practice in the fourteenth
century. Med Hist 45:319–340
35A. Bod R (2010) De vergeten wetenschappen. Een geschiedenis van de humaniora. B. Bakker,
Amsterdam
36. Kybert P (2000) The intelligent hand. IEE Review 46:31–35: see also reliquaries from the
Staatliche Museum zu Berlin und Kunstgewebe Museum. Three hands from 1350 (Inv.Nr
W33), end 11th century (W18) and end 12th century (W23)
36A. Zodiac maps related to the humors of the body are known from the 11th century (El Burgo
de Osma, Spain). The best known is the Anatomical Man (1412–1416) in Les très riches
heures du duc de Berry
37. Sawday J (1995) The body emblazoned. Routledge, London
37A. MacKinney L (1965) Medical illustrations in medieval manuscripts. Wellcome Hist Med
Library. W. Clowes and Sons, London
37B. MacKinney LC (1962) The beginnings of western scientific anatomy: new evidence and a
revision in interpretation of Mondeville’s role. Med Hist 6:233–239; Sudhoff K (1923) The
fasciculus medicinae of Johannes Ketham and Sudhoff K (1911) Neue Beiträge zur
Vorgeschichte des Ketham’s. Archiv Gesch medizin V, 4u5, 280–301
38. Morris AG (1986) On the sexual intercourse drawings of Leonardo da Vinci. S Afr Med J
69:510–513
38A. The liver is a right-sided organ, placed in this figure wrongly: ‘‘It is not unreasonable to
assume that the wood-cutter did in fact reverse the original drawing. (by 1509, Milan
edition, this situs inversus had been corrected).’’ Also the right kidney lying higher than the
left one supports this. Roberts KB. Tomlinson JDW (1992) The fabric of the body:
European traditions of anatomical illustration. Clarendon Press, Oxford
39. Siraisi NG (1990) Medieval and early renaissance medicine. An introduction to knowledge
and practice.University Chicago Press, Chicago and Zwijnenberg R (2004) Project:
Philosophy, anatomy and representation. www. Narcis. Info/research
39A. Mackinney LC (1962) The beginnings of western scientific anatomy: new evidence and a
revision in interpretation of Mondeville’s role. Medical History 6:233–239, see also M. Mc
Vaugh (2000) Surgical education in the Middle Ages. Dynamis Acta Hisp Med Sci Hist
Illus 20:283–304
39B. Singer C (1915) A thirteen century drawing of the anatomy of the uterus and adnexa. Sect
History of Medicine Proceed Royl Soc Med 9:43–47; Singer C (1957) A short history of
anatomy from the Greeks to Harvey. The evolution of Anatomy. Dover publ.; H. Braus
(1934) Anatomie des Menschen, II Eingeweide, Springer, Berlin and K Whittington (2008)
The cruciform womb: process, symbol and salvation in Bodleian Library MS. Ashmole.
Diff Visions. J New perspect Med Art 1–24
39C. Roberts KB, Tomlinson JDW (1992) The fabric of the body, European traditions of
anatomical illustration. Clarendon Press, Oxford, see also Ivins WM Jr. (1953) Prints and
visual communication. Harvard UP, London Routledge
39D. Vitruvian figures were depicted by Cesare Cesareano in 1521, Leonardo da Vinci in
between 1490–1492 and Albrecht Dürer in 1528.
39E. P.Burke in his booklet The Renaissance (1987) Studies in European history, St Martin’s
Press, states that Vitruvius books ‘‘were first printed in 1486 or thereabouts’’. This is
incorrect see: J.H. Jensenius (2001) Trekirkene før stavkirkene Con Text6 Arkitekt
høgskolen I Oslo. Moreover, C.H.Krinsky (1967) in Cathedral studies, engineering or

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Literature 109

history. Newcomb Society, 2004, described the discovery of 78 handwritten medieval


versions of Vitruvius books
40. Tabarrini M (1996) Prefazione and Vasari G, Vita di Leonardo da Vinci in: Leonardo
Trattato della pittura. Newton and Compton, Roma
41. Z}ollner F, Nathan J (2003) Leonardo da Vinci Leven en werk. Taschen, K} oln
42. Braunfels-Esche S (1961) Leonardo. Das anatomische werk, Stuttgart
43. Siraisi NG (1997) The clock and the mirror: Girolamo Cardano and renaissance medicine.
Princeton University Press
44. Donnison J (1977) Midwives and medical men. Heineman London
45. Bettmann OL (1956) A pictorial history of medicine. CC Thomas, Springfield
46. Churchil H (1997) Ceasarean birth: experience, practice and history. Elsevier Health
Sciences, Books for midwifes, Amsterdam
47. Burris GP (1965) The illustrations in the De Dissectione Partium Corporis Humani Libri
Tres (1545) of Charles Estienne (1504-1564). Proc Okla Acad Sci 151–155. Citation on
variability: Marani E, Lakke EAJF (2010) Peripheral nervous system topics. In G.Paxinos,
J Mai eds The human nervous system. Elsevier, NY
48. Rath G (1964) Charles Estienne: contemporary of Vesalius. Med Hist 8:354–359 and
Tubbs RS, Salter EG (2006) Charles Estienne (Carolus Stephanus) (ca 1504–1564):
Physician and anatomist. Clin Anat 19:4–7
48A. In Roberts KB and Tomlinson JDW (1992, The fabric of the body: European traditions of
anatomical illustration. Clarendon Press, Oxford) the description of Charles Estienne’s
anatomical work is met with ‘‘denigration’’. ‘‘The book as a whole, and more particularly
its illustrations, must therefore not be compared with the Fabrica (of Vesalius), to which it
perforce owed nothing: it should instead be thought of as another early attempt to resolve
the problem of using figures to illustrate anatomical text’’. The quality of the figures is
liable to disapproval, in itself there is no injustice in this. However, the text in relation to
the figures brings the book at a higher level
48B. Roberts and Tomlinson (1992): ‘‘Vesalius commented, in his letter of complaint to
Oporinus, 1542:’’ At Paris they have copied the first three plates very well, but the others
they have omitted, perhaps because they were difficult to engrave, though it was these first
three which students could have best dispensed with’’. The other plates concerned the
skeleton. Estienne’s book does not contain skeletal pictures
49. Fichtner G, Siefert H (1978) Padua, Medizinhistorische Reisen 2. F. K. Schattauer Verlag,
Stuttgart
50. Cochrane C (1976) Science and humanism in the Italian Renaissance. Am Historical Rev
81:1039–1057 and Rossetti L (1987) The University of Padua. An outline of its history.
Edizione Lint, Trieste
51. Lindberg DC (1968) The scientific revolution misconstrued: a reply to David Siemens and
others. JASA 20(87–91):97
52. Pirenne H (1947) Economic and social history of medieval Europe. Kegan, Trench,
Trubner & Co, London
53. De Jong WR, Betti A (2010) The classical model of science: a millennia-old model of
scientific rationality. Synthese 174(2):185–203
54. Frank IW (1995) A concise history of mediaeval church. Continuum, NY
55. Premuda L (1965) Die Anatomie an der oberitalienischen Universitaeten vor dem
Auftreten Vesals. Med Mschr 19:20-25
55B. Laughlin B (1995) The Aristotle adventure: a guide to Greek, Arabic and Latin scholars
who transmitted Aristotle’s logic to the Renaissance. Albert Hale Publ. Flagstaff, Arizona;
see also Talbot CH (1978) Medicine Ch. 12 in Science in the Middle Ages. Ed. Lindberg
DC, Univ Chicago Press, Chicago, London
56. Clanchy MT (2000) Abelard: a medieval life. Blackwell, Massachusetts
57. O’Malley CD, Russell KF (1961) David Edwardes. Introduction to Anatomy 1532. Oxford
University Press London
58. Lind LR (1975) Pre-Vesalian Anatomy. Am Philos Soc, Philadelphia

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110 4 History

59. Tabanelli M (1965) La chirurgia italiana nell’alto medioevo. Biblioteca della ‘‘Rivista di
storia delle scienze mediche e natural’’ vol XV: Parts I and II. L. S. Olschki, Florence
60. Zimmerman LM Veith I (1961) Great ideas in the history of Surgery. Balliére, Tindall and
Cox, London
61. Santoni-Rugiu P, Mazzola R (1997) Leonardo Fioravant (1517–1588): A barber-surgeon
who influenced the development of reconstructive surgery. Plast Reconst Surgery
99:570–579; Antiseptic methods were already introduced by Taddeo Alderotti
(1210–1295). He prescribed aqua vita (distilled wine) for cleaning the skin and scabies.
Trotula of Salerno around 1200 prescribed cotton with warm wine to be placed in the
vagina to overcome sexual arousal, see P. Prioreschi (2003) A history of medicine Vol V,
Medieval Medicine. Horatius Press, Omaha, NE
62. Siraisi NG (1973) Arts and sciences at Padua. The studium of Padua before 1350. Pont Inst
Mediaeval Studies. Toronto Canada
63A. Addendum Chapter 2: A series of articles around the 1900s still resound. They brought
forward that Leonardo’s book on human anatomy was plagiarized by Vesalius63. Another
charge was the take over of pictures from Estienne without permission by Vesalius64.
These accusations were investigated by J.P. McMurrich, and could clearly be denied65.
Serious criticism on the contribution of Leonardo da Vinci as an inventor and genius
scientist has been brought forward by J.H.Randall Jr.66 This point of view cannot be kept if
one notices the enormous amount of confirming books67 on Leonardo’s machines and
robots, its importance still for nowadays engineering68 and e.g. the articles in the journal
‘‘Leonardo’’ on Leonardo’s inventions68
63. Jackschath E (1902) Die Begrundung der modernen Anatomie durch Leonardo da Vinci
und die Wiederauffindung zweier Schriften derselben. Med Bldtter, xxv:770–772
64. Von Töply R (1903) Aus der Renaissancezeit. (Neue Streiflichter uber die Florentiner
Akademie und die anatomischen Zeichnungen des Vesal.) Janus viii:130–140
65. McMurrich JP (1906) Leonardo da Vinci and Vesalius: A Review. Med Library Hist J
338–350
66. Randall Jr. JH (1953) The place of Leonardo da Vinci in the emergence of modern science.
J Hist. Ideas XIV:191–202 and Randall Jr JH (1961) Chap III (The place of Leonardo da
Vinci in the emergence of modern science) in The School of Padua and the emergence of
modern science. Ed Antenore Padova 1959
67. See e.g. Rosheim ME (2006) Leonardo’s lost robots. Springer Berlin or Moon TC (2007)
The machines of Leonardo da Vinci and Franz Reuleaux. Springer Berlin
68. Popplow M (2004) Picturing machines. 1.Why draw pictures of machines? The social
context of early modern machine drawings. Mitpress.mit.edu; MIT Press Journal
‘‘Leonardo’’ (edited by R.F.Malina)
68A. Singer C (1956) Galen on anatomical procedures Oxford University Press London,
Duckworth WLH, Lyons MC, Towers B (1962) Galen on anatomical procedures. The later
books. Cambridge University Press. and May MT Galen on the usefulness of the parts of
the body. vol I, II Cornell University Press Ithaca, NY
69. Huisman T (2009) The finger of God. Anatomical practice in 17th century Leiden; De
Graaf R (1686) Alle de wercken, so in de ontleed-kunde als andere deelen der Medicyne.
Abraham Abrahamse, Amsterdam; J.Swammerdam in J. van Horne (1668) Suorum circa
partes generationis in utroque observationum prodromus. Leiden (apud Gaasbekios)

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Chapter 5
Concepts and Approaches in the Study
of the Pelvis

During the ages of pelvic studies, certain concepts and approaches were found
useful, and others were discarded. The applied techniques and models are dem-
onstrated using examples from morphological approaches (symmetry, ontogeny,
and comparative anatomy) and functional ones (kinematic chains, pelvic organ
movements). This chapter also concentrates on biomechanics of the pelvis together
with its lower extremities and focuses on finite element modeling, where mor-
phology and physiology reinforce each other for the study of pelvic forces and
movements. By applying these methods, for example, low back pain caused by
changes in the self-locking mechanism of the sacrum with its tightening ligaments
becomes doubtful.

5.1 Introduction

The conclusion of the previous chapter was that pelvic science made a false start.
This erroneous approach lasted for nearly two centuries, and one is driven to seek
the reasons for such a prolonged diversion. Dullemeyer’s approach [1] to the
concepts used in the study of morphology is helpful since the false start was based
on morphological evidence of the bony pelvis. Morphology was practiced, until
the beginning of the twentieth century, by the analysis of parts of organisms, single
organ systems, or its characteristic parts. These parts were classified by phylogeny
(phylogenetic trees), by ontogeny, or by way of comparative anatomy.
An attempt to modernize morphology resulted from the interest in function and
the rise of physiology at the end of the nineteenth century. Experimental embry-
ology became based on the principle of causality. At first, the application of this
principle failed in morphology, but was effectively applied in functional anatomy
that began around 1930.
An holistic scientist, on the other hand, tries to analyze parts of an organism or
organ system in relation to the totality of the organism or the organ system. Holism
integrates form and function. This relationship will be placed in a larger context
than the one in which the analysis is performed. For instance, form and function of

E. Marani and W. F.R.M. Koch, The Pelvis, 111


DOI: 10.1007/978-3-642-40006-3_5,  Springer-Verlag Berlin Heidelberg 2014

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112 5 Concepts and Approaches in the Study of the Pelvis

molar teeth are related to the jaw, which is in turn related to the head. So in
modern morphology, the analyzed morphological parts must always be related to
the interaction of form and function, and the influences on them from other parts
around them [1].

5.2 Symmetry of the Pelvis

No pelvis is equal and no pelvis is symmetric. The clinician knows that. Never-
theless, all anatomical illustrations of the pelvis are very symmetric. The con-
vention of showing the pelvis as symmetric goes back to Albinus (1697–1770) [2]
who raised anatomical illustration to the level of an ‘‘architectural’’ method. All
parts of the human body were pictured by Albinus using a pair of compasses and a
ruler. It is simple to produce symmetry. One takes one half of an organ and places
its mirror image next to it. A simple procedure was carried out for Albinus by the
medical artist Wandelaar. One half was drawn with charcoal, the paper was then
folded, and the symmetry is created by rubbing (Fig. 5.1). Shadowing of the mirror
side had to be corrected, but that was easy for a famous draftsman like Wandelaar.
What is symmetry? In geometry, it is defined as a construction, arrangement, or
framing, such that it can be divided by a line or plane into two parts that are each
others mirror images. In Vitruvius Pollio’s well-known book on architecture
‘‘De architectural libri X’’ (25 BC), the only surviving work on Roman architecture,
symmetry is one of the most important ideals of architecture, ideals that were
followed for centuries [3]. Symmetry was the hallmark of beauty in architecture.
Albinus believed in the homo perfectus and symmetry was a property, that
naturally belonged to the perfect man. His other credo was objectivity, which
meant that the parts of the human body had to be pictured precisely in their
measures and relations (Figs. 5.2a, b). These two demands could easily oppose to
each other, especially if exact measurements yielded no symmetry. Albinus had to
maintain symmetry in his anatomical pictures, and he, therefore, had to remove
less important parts and had to produce symmetry by the trick of putting the mirror
image to the original half of the picture.
By the way, Albinus even characterized the perfect man by indicating the ideal
height. Amazingly, by the excavation of Albinus skeleton, it was found that his
own height, 1.67 m, was exactly equal to the ideal height [4].
For his famous anatomical atlas ‘‘Tabulae sceleti et musculosum corporis
humani’’ (Leiden 1747), Albinus chose a skeleton that fulfilled his image of the
homo perfectus.
He describes it as a normal skeleton for that time, which had belonged to a
young man in the full bloom of his life. It had perfect proportions, without
abnormalities, neither in his bones nor in his ligaments and showed all the marks
of strength and flexibility. It was elegant, but not extravagant. It had no juvenile or
female characteristics nor was it coarse or angular. In fact, it was beautiful in all of
its parts [4].

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5.2 Symmetry of the Pelvis 113

Fig. 5.1 The symmetric


bony pelvis in a frontal view
as pictured by Albinus and
Wandelaar. How symmetry
was organized can still be
seen: The paper folding line
can be recognized in the
pelvis’ midsagittal plane and
in the shadow below it.
Reproduced with permission
from the Leiden University
Library

Fig. 5.2 a Drawing of the


human skeleton by Albinus
and Wandelaar. The inset was
sticked to this figure by an
anonymous. Reproduced with
permission from the Leiden
University Library.
b Photograph from Punt’s
study [4] of the drawing
method of Albinus and
Wandelaar. This method was
repeated in the Leiden
Laboratory of Anatomy.
Courtesy Dr. H. Punt and
with permission from the
Department of Anatomy and
Embryology, Leiden

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114 5 Concepts and Approaches in the Study of the Pelvis

Fig. 5.3 Enlargement of the


inset as present in Fig. 5.2a,
reproduced with permission
from the Leiden University
Library

Still there is something remarkable about the skeleton: the disproportionately


long legs. They approach the ideal body proportions as produced by Dürer in his
Adam figure. One can expect problems if one wants to retain the original measure
relations: The musculus iliopsoas attaches to the trochanter minor of the femur,
and with the lengthening of the bones, this connection shifts downwards. More-
over, the adductor muscle fan against the femur will also be extended.
At a visit to the Leiden University Library, where parts of the original drawings
and working books of Albinus and Wandelaar are stored, I found on one of the
originals of the skeleton pictures a drawing glued on it (Fig. 5.2a). The superpo-
sition of the real m. iliopsoas and its depiction by Albinus is shown after mag-
nification (Fig. 5.3). Clearly, one sees the difference. For the adductor muscles, in
another drawing, one can notice that the position of the muscles is changed. In this
Procrustian bed, the muscles had to be fitted to the changed length.
As the English plagiarized Bidloo’s atlas, so they plagiarized the Tabulae of
Albinus in 1749. The same format with the same background illustrations
appeared in the anatomical atlas, published by J. and P. Knapton. Although
Albinus wrote a clear warning to the Knaptons in his Tabulae ossium humanorium,
a second English edition appeared in which the same book as well as Albinus’s
re-edition of Eustachius’s work were again plagiarized. The French publishers
copied Albinus work in a smaller (quarto) edition, which competed strongly with
the original version in the French-speaking countries. Albinus had worked on his
books assiduous. The publication of his Tabulae sceleti et musculorum costs him
30,000 Dutch florins, for that time a gigantic sum. But smart publishers appro-
priated to the earnings that the book had to produce for Albinus. A consequence of
the enormous propagation was that the symmetry in the pictures of Albinus
became well known and its concept was taken over. Symmetry can no longer be
eliminated from human anatomy. It is even a modern ideal, that is strived for, and
that marks the standard of beauty.

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5.3 Comparative Anatomy of the Pelvis 115

5.3 Comparative Anatomy of the Pelvis

‘‘The relation between function and form in an element is of an a-causal character.


It is a relation or correlation instead of a causality, because the relation does not
contain a time parameter. A relation between two aspects can be found by
describing both aspects in a certain order and investigating whether this order is
similar in both descriptions. Therefore, the comparative method should consist of a
comparative listing or description of both aspects’’ [1].
The aspects studied in comparative anatomy are presence, position, size, shape,
structure, and composition [1].
Ironically, the presence of an element can best be comparatively studied if, in
any species, that element is absent. One is mostly aware of a presence by its
absence elsewhere. However, since in all tetrapods one can discern the three pairs
of bones, the absence of one of the pelvic bony elements is a nonstarter in pelvic
science. The presence of a paired os marsupii or the processus preapubica, that is
absent in vertebrates, should promote a comparative approach, but only for these
bony elements and not for the three paired bony elements of the vertebrate pelvis.
In Cetaceae, a strong reduction in the whole bony pelvis and leg bones is present.
Pelvic remnants serve mainly to adhere the penis in males. The pelvic ring
function is gone, and therefore, comparison is not possible.
Pelvic position has been studied and eloquently discussed by Böker [5]:
‘‘Sometimes the relation of a position to an activity is so strict that we find a
similar configuration in various organisms. This indicates a convergence if the
organisms are taxonomically not closely related. The corresponding positions of
the pelvic girdle in Chameleon and in big terrestrial mammals is well known.’’
The specific manner of locomotion in terrestrial mammals and in the species
Chameleon forces the pelvic girdle to be perpendicular to the vertebral column.
The importance of the position of the bony pelvis to the scientific understanding of
the position of the internal organs in relation to the osii pubi has been shown in the
part on Vesalius in Chap. 4, Sect. 4.3. Comparative anatomy stresses position of
the pelvis in the relation to the mode of locomotion.
The pelvic size is first of all related to the size of the animal, ‘‘which is another
way of stating that the functional demand is higher in big animals than in small
ones’’ [1]. The pelvic size is always studied relatively, thus in respect to other
pelvises, as shown for the evolutionary trend in Chaps. 1 and 3: ‘‘it is not sur-
prising that larger animals need thicker or stronger bones. Of special importance,
however, is the nature of the relation of the weight of the animal to the thickness of
the bone and to other properties than size: such as sculpture.’’ ‘‘Quantification of
size of the pelvis among several species is a necessary prerequisite to overcome
platitudes like pelvic size is related to the size of the animal as given above’’ [1].
Size can also be related to a number of different elements. There is little insight
into the relation between number and function, since the number of bony pelvic
elements seems to be constant. Comparison of series of varying numbers, there-
fore, cannot help to solve this problem.

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116 5 Concepts and Approaches in the Study of the Pelvis

Shape as a property of morphological elements is widely studied. ‘‘Part of the


shape of a bony element is determined by the manner of attachment and the force
exerted by muscles’’ [1]. This is not only true for attachment and force of the muscles
attached to the pelvic bones, but note that also a lot of ligaments have their
attachments and exert forces. The volume that the pelvis has to encircle is such a
property. Since the boundaries of this volume are difficult to distinguish from the
abdomen, it becomes difficult to estimate this volume (see 4.9). Nevertheless, the
shape stays an intriguing property of the bony pelvis; think about the os ilium with its
extended bowl-like bony plate for the attachment of the ilius muscle, and its clear
crista, or the spina iliaca anterior–superior as an adherence for the inguinal ligament.
Structure and composition have been related to the bony pelvis. The quanti-
tative composition and orientation of the substance of the bones also call for
attention. ‘‘The relative amounts of appetite crystals in bone is directly propor-
tional to the resistance to pressure,’’[1] which is expected to hold for the pelvic
bones too, and ‘‘the orientation of the trabeculae and the fibers of collagen is
related to the direction of the strain’’ [1].
The comparative approach then brings us a series of conclusions:
• On the presence nothing can be said.
• Position stresses pelvic involvement in locomotion.
• Size of the pelvis is related to the size of the animal/man.
• Shape is determined by the attachment of muscles and ligaments and by the
muscle forces exerted.
• Structure and composition are related to resistance to pressure and to the
direction of the strain.
In general, comparative anatomy has contributed to the understanding of
morphology of man and animals. However, the above-mentioned conclusions can
also be categorized as platitudes. The main problem is that the pelvis and its
contents cannot be considered as a closed system with relations to other closed
systems as can be done with the jaw. The open system, called pelvis, is hard to
tackle by a (scientific) comparative approach. The best example to illustrate this
problem is that everybody has a pelvis and an abdomen; however, the exact border
is impossible to draw: We therefore talk about a virtual border. In fact, this is
saying that we do not have a morphologically delimited structure, and therefore,
our approaches so strictly based on closed systems do not work.

5.4 Ontogeny of the Pelvis

A frequently heard statement is: ‘‘Anatomical knowledge is complete, so no fur-


ther research is necessary.’’ The pelvis studied so frequently, therefore, ought to be
known in all of its aspects. Well, let us see. The development of the pelvic bones
appears to be terra incognita. The Journal of Bone and Joint Surgery of 1996
contains a series of letters to the editor concerning this development [6].

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5.4 Ontogeny of the Pelvis 117

Bone can be produced, by membranous ossification (skull bones, calvaria), and


by enchondral ossification (tibia). So the question arises: Are the pelvic bones
produced by membranous or by enchondral ossification? Reviews in the above-
mentioned journal argued for production by membranous instead of enchondral
ossification [6–10].
‘‘In fact the ossification and later, the growth pattern of the pelvis is one of the
most fascinating examples of enchondral ossification, especially in view of the
appearance of multiple ossification centers, the enlargement of the acetabulum by
means of the Y-shaped growth plate, the marginal epiphyseal plate along the iliac
crest and the bipolar growth cartilage in the inferior branch of the pubic bone. These
features are worth remembering by anybody who works in the field of bone histo-
physiology and are important for the understanding of the numerous irregularities
and malformations of the pelvis’’ to quote Schenk of Bern in his letter [7]. In one of
the replies, it is argued that the pelvic bones originate by both membranous and
enchondral ossification [8]. The difference is important since scientists attribute
different regenerative capacity to the two types of ossification, which has conse-
quences for the transplantation in the pelvic bones. The third letter [9] holds
membranous ossification responsible, because the older literature denying mem-
branous ossification does not state that it is enchondral ossification; therefore, they
conclude, suddenly and mainly from the work of Ponseti (1978), that [10] ‘‘Thus,
although there is some uncertainty concerning the embryonic formation of the flat
portions of the human pelvis, the reported studies show that the human ilium grows
by both enchondral (phycal) and periosteal (appositional bone formation).’’
There are centers of enchondral ossification, which together with other forms of
ossification will produce the bony pelvis. The general view is that each of the
bones: os ilium, os isschii, and os pubis have their own enchondral ossification
centers. After outgrowth from these centers, they will meet in a Y-shaped fashion
at the joint socket: the acetabulum. There was a question as to whether there is an
enchondral ossification center for the ischial spines. It was answered by a dem-
onstration that the ossification center is inconstant (see [11]).
However, ontogeny of the bony pelvis does not stop after birth. The whole bony
pelvis continues to change up to the age of 20. Structures such as the ischial spine are
absent at birth and only begin to appear around the age of 10. Sex differences will
appear with as main feature the difference in directional growth of the anterior half
of the iliac crest, lateral migration of the ischia, and the enlargement of the pelvic
cavity by change of the subpubic angle and the length of the superior pubic ramus
(see 1.2) [12, 21]. The difference in directional growth certainly holds, too, for the
reunion of the enchondral ossification centers. For example, in the acetabulum, the
bones of the pelvis fuse totally after the age of 15, while the depth of the acetabulum
still changes after the same age [10]. So pelvic development does not stop after birth,
and in fact, its postnatal development lasts much longer than its prenatal one.
The literature on the development of the bony pelvis contains controversies,
lack of information, and different hypothesis. Anyone studying or looking for
information on the ontogeny of the bony pelvis must feel discouraged by the lack of
factual data.

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118 5 Concepts and Approaches in the Study of the Pelvis

5.5 Mechanical Approach to the Pelvis

The mechanical thinking of Murk Jansen: The large circumference of the


brain, the wide pelvic ring, and the multitude of hip afflictions in man.
Mechanical explanations for the afflictions of the pelvis have been published
frequently. They stay with you for a long time, especially if the explanation is
simple and a lot of pathology becomes clear. People like simplicity, because in that
case, the storage in one’s brain lobes is minimal. Mechanical explanations have
simplicity on their side, but whether they are therefore accurate is still a question.
To give examples is easy: the perineum is the central knob in the pelvis, which
after damage let us the pelvic contents protrude (Fig. 4.2). The sacroiliac joint with
its ligaments is a suspension bridge construction (Fig. 1.5). True or not, these
explanations are frequently used in anatomical handbooks to demonstrate the
importance of structures to the students [13].
Murk Jansen, professor of orthopedics in Leiden, was very interested in hip
afflictions: coxa vara, coxa fracta, coxa plana, coxa valga, epiphysiolysis, malum
coxae, and he put them all in the subtitle of his booklet on hip afflictions that was
published in 1927 [14].
‘‘The innate dislocations of the hip and the mentioned afflictions associated
with them are the less desirable inheritance of man. And we want to put forward
grounds to argue that they all find their primary cause in the strong development of
the human brain, which necessitated a wide pelvic ring, to allow birth without
complications.’’
His argument is an example of mechanistic thinking, and it starts with one article
of Le Damany [15] who ‘‘in an ingenious manner furnished the convincing evidence
that innate hip dislocations are caused by cramp for room in utero’’ (page 4) [14].
From this, Jansen infers:
We borrow from this the following: Already in the fetal stage man is differentiated from
animals by his wide extension of the pelvis. When there is pressure on the knee of the fetus
and the hip is bent, this wide pelvic ring, easier than in animals, offers the femur a fulcrum
against the area of the spina iliaca anterior superior, in such a way that the femur head will
be leveraged out of the hip joint (Fig. 5.4).

The pelvis is so wide, because man has a large brain; otherwise, the fetus cannot
pass through the pelvis during delivery. Murk Jansen produces a series of argu-
ments to support his thesis:
1. Luxation from the hip joint occurs in those cases in which the fetal membranes
are narrower than normal and the wide pelvic ring gives more than normal a
fulcrum to the, femur, bent in the hip joint, by which the femur head is lev-
eraged more powerful out of the acetabulum.
2. Man has a longer femur. This enhances the leverage.
3. Luxations of the hip are more frequently encountered by women, because the
female fetal pelvis is already wider (seemingly, woman consequently also have
bigger brains).

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5.5 Mechanical Approach to the Pelvis 119

4. Negroes have smaller brains than white men; consequently, they ‘‘are, like the
animals, spared from innate dislocations of the hip.’’ ‘‘Till here Le Damany’’
adds Murk Jansen to be safe [14].
If you have read ‘‘The Mismeasure of Man’’ by Gould [16], you know that
prejudice in skull research led to the theory that Negroes indeed have smaller
brains. This is clearly not true. Moreover, the skull volume of women is always
smaller than those of men. There are animals which have bigger brains than that of
man: the elephant and the large whales. In two pages, we find a series of wrong
suppositions.
In leverage, it is true that force on each side of the fulcrum is inversely related
to the length of the lever on that side, and thus, huge forces can be exerted. Is
however, the spina iliaca superior such a fulcrum? For without such a pivot point,
there is no leverage at all.
Mature people sitting on their heels cannot put their femur against their pelvis
and even young children in gymnastics cannot do this. If you know the devel-
opment of the abdomen wall, it is impossible for the fetus too.
And now the flattened hip joint, the second phenomenon described by Murk
Jansen:
‘‘If the fetal membranes stay too narrow, the head of the hip bone can also be
powerfully pressed against the ischio-pubic part of the floor of the hip joint’’ [14].
It causes a widening of the hip socket. To reach this, the fetus has to be perched in
a yoga position: ‘‘a posture that can be compared to the one of the tailor’’ [14].
This is in itself a contradiction, because if the fetal membranes are wrapped tightly
around the fetus the fetal legs will be pushed inward and not outward.
Murk Jansen starts his booklet with the remark that his theory is unclearly
presented and that there is serious opposition. Ingelrans, cited by Murk Jansen,
considers his theory: ‘‘touffue et difficile à suivre’’ (confused and difficult to follow)
[14].
Murk Jansen had simplicity on his side. His proposal explains a lot of pathology
of the hip socket, but what a series of wrong suppositions and approaches. He was
of course a man of his time (Negroes have small brains) and of course less was
known. Nevertheless, I cannot get rid of the impression that this approach suited
Murk Jansen well, because in his time mechanistic thinking was ‘‘bon ton.’’

Fig. 5.4 Original pictures


from Jansen [14] to
demonstrate the leverage
mechanism for the hip joint

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120 5 Concepts and Approaches in the Study of the Pelvis

5.6 Sirene: A Seducing Pelvic Sound?

Toward the end of the second world war, while Europe went through the horrible
terrors and in the Netherlands a hunger winter started, a Swiss anatomist was
quietly working behind his desk on ‘‘Missbildung und Vererbung.’’ Nowadays,
you would translate it by ‘‘deviation and genetics.’’ Its subtitle ‘‘on the genetical
and developmental physiological basics of human deviations’’ nothing leaves for
the imagination. Few scientists use the anatomical handbooks of this Swiss
anatomist Gian Töndury (1907–1985) anymore. A good clinician is interested in
them, because Töndury succeeded in organizing a large quantity of human devi-
ations according to the principle ‘‘the linearly increasing deformation, starting with
the normal gradient.’’ Scientists now use names like pathoembryology, embryo-
logical or fetal malformations, and fetal defects: They all belong simply to the
domain of teratology. Who ever would dare to say that teratology is a collection of
casuistic cases should study Töndury’s works. During the settling of an estate,
I found two reprints of Töndury ‘‘überreicht vom Verfasser’’ that concerned
human deviations and experiment [17, 18]. I went through them and noticed that
they concerned deviations of the pelvis. With great interest, I read the somewhat
dull, but extremely sound descriptions. First I was suspicious, because the papers
were published in the ‘‘Archive der Julius Klaus-Stiftung für Vererbungsfors-
chung, Sozialanthropologie und Rassenhygiene’’ (Archive of the Julius Klaus
foundation for genetics, social anthropology and racial hygiene), but that suspicion
disappeared the moment I realized the pure ‘‘pelvic mermaid content.’’
According to the dictionary, a sirene is a demonic creature, half wife, half bird
(see Homer); later, in art, half wife, half fish, that seduced the passing seamen with
songs and killed them: In science, it is rather a mermaid than a wife-bird. This
image is not only vivid in classical literature. One can think about the Lorelei
along the river Rhine. The number of clinical synonyms for the human mermaid
malformation is large: symmely, sympody, sympus, monopus, anchipode, and
sirenomely. This theme is still alive in anatomy, since regularly fetuses are born
with sirenomely. Bolk has dared to publish on it, and at Bolk’s memorial in 1975,
Nieuwenhuys placed the theme in its scientific and historical perspective [19].
Leg formation is determined by the interaction of the ectodermal and meso-
dermal structures during development. The rump mesoderm induces an apical
ectodermal ridge on the incipient limb bud. This ridge is important for the out-
growth of the leg mesoderm, and the ridge determines the sequence of the skeleton
parts. If something goes wrong, here then phocomelia develops (=mismatch of
hands or feet, mostly directly placed on the shoulder, as encountered in thalido-
mide babies) and oligodactyly (=inborn lack of fingers and toes), [20] but no
sirenomely!
Bolk’s explanation is a simple one: not all 32–33 segments of the human body
are produced in sirenomely. This means that the new segments constructing the
end of the human fetus are placed near to each other: for example, only segments
up to 22–23 are developed; this results in sympus apus: Femur and tibia are fused,

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5.6 Sirene: A Seducing Pelvic Sound? 121

Fig. 5.5 a Picture from Bolk [19] to demonstrate the segmentational continuity in the
extremities, even in the mermaids joined legs (b). b This figure [19] shows the leg segmentation
in relation to the bony structures of the leg, see Bolk [19]

because these segments are responsible for the production of femur and tibia.
Fused because segments 22–23 left and right are forming the end of the human
conus and thus at the end are placed at each other sides. In segmental production
up to 25, left and right fibula are fused, because segment 25 contains the fibula and
left 25 is apposed to the right 25. They indeed are the end of the human conus in
this deviation, and thus, we deal with a sympus monopus, etc. (Fig. 5.5).
The deviation will not always be restricted to the lower extremities: The pelvis
and its contents can also be affected. Here Töndury tries to give a fitting
explanation.
The common mouse had already been mutated in the Forties of the twentieth
century. The four known mutants (T, Sd, t0, t1) contained a deviant rump and a
damaged pelvic construction. Atresia ani (closure of the normal anal opening) but
also missing kidneys and an affected genital apparatus were found. In humans,
these deviations of the end of the rump cone are known as sirenoid-like deviations.
The sirenoid-common property is that the bilateral symmetry has been damaged.
In a real sirene, the caudal part of the spinal cord and vertebral column, the
derivatives of the cloaca (anus, perineum, vulva, vagina, urethra) are missing and
the organs of the urogenital tract are damaged.
Töndury succeeds, as Bolk did with the leg development, to order the devia-
tions linearly, now not in relation to the segmental idea, but in relation to genetic
determination ‘‘gen-bedingt.’’ In other words, sirenes are human individuals with a
lethal mutation, analogous to the common mouse mutants, that show nearly the
same deviations. The stronger the expression of the lethal gene, the stronger the
deviation.
But now Töndury fails to capitalize on this. Indeed, in 1943/1944, we had ideas
on mutations, but no proof, except for the findings of the Dutch scientist de Vries
in Oenothera flowers, but that was later found to be untrue. So Töndury could
accept that it was a gene mutation, but then what? Nowadays, we know that

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122 5 Concepts and Approaches in the Study of the Pelvis

Fig. 5.6 Töndury’s (1944) [17, 18] midsagittal drawings of four mermaids, numbered 1 till 4,
showing his sequence. Note the distortions in the vertebral row

‘‘some’’ gene is responsible for such an illness, and we are able to look into the
biochemical chain that is responsible for the illness. Töndury lacked these
instruments. The segmental end conus of the fetal human will be represented in the
mature human in dermatomes, skin segments.
Töndury noticed that the deviations could be arranged in a sequence (Fig. 5.6).
Sneakily, he uses the presence of the vertebrae, without stating this explicitly. He
himself had three sirenes in his possession, and with two more from the literature,
a sequence could be constructed from slightly affected to heavily affected fetuses.
By arguing backward to that part, say dermatome or if you want segment, he
produces Fig. 5.7, a schematic representation of the cone-like deviations of the
rump end. The further the deviation tends to rostral on the rump cone, the more

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5.6 Sirene: A Seducing Pelvic Sound? 123

Fig. 5.7 Schematic representation of the cone-like deviations of the rump end of five mermaids,
1 till 4 from Fig. 5.6 see Töndury [17, 18]

sirene-like a feature is found. In fact, Töndury noticed that segmental damage from
32–33 to 26–27 only produces pelvic deviations and that damage between 20–21
and 26–27 produces mermaids!
It is rather amusing to see that in spite of a new cause, ‘‘gene mutation,’’
44 years after Bolk, the same explanation, ‘‘segmentation,’’ is still used ignorantly.
Töndury does not refer to Bolk!

5.6.1 Holism and the Deviant

The following story is on conjoined twins and brings us to the study of malforma-
tions caused by the wrong development of the pelvis [21, 22]. Mutants or monsters
not only awoke fear, but also interested scientists. Collection of monsters started in
the sixteenth and seventeenth centuries and together with it causes like ‘‘too much or
too little semen, narrow wombs, indecent posture’’ [22A] were proposed. ‘‘It is
rational in sofar that it does not appeal to supernatural agents’’ [22A]. Although the
explanations are wrong, a start was made to understand these kinds of deviations.
What follows is the Ritta-Christina Parodi story on pathologic embryology. The
Parodi family earned money in Italy (Sardinia) by exposing their Siamese twins in
1828 and hoped to do so in Paris too in 1829. However, the magistrates refused
and brought the family to poverty. The cold in the house and the regular uncov-
ering of the twins for curious doctors induced sickness and death. The results of
the anatomical dissections were laid down in a large monograph by Etienne
Reynoud Augustin Serres (1832), ‘‘the brilliant young physician from the Hôpital
de la Pitié’’ [22A]. It is from this description and plates that we can direct our-
selves to the conjointment of pelvises. The double organization of the twins ends

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124 5 Concepts and Approaches in the Study of the Pelvis

Fig. 5.8 Left is the impression of the conjoined twins Ritta-Christina. The right side is the
skeleton of the conjoined twins after dissection. Plates are reproduced from Serres [22], with
permission from the Leiden University Library

near the start of the legs. The conjoint twins had four arms, but two legs (Fig. 5.8).
Let us follow partly the French text in translation on the pelvises of Ritta-
Christina:
The bony structure of the pelvis was less complicated than the one on the breast, but it was
not as simple as the outside did expect. There were two sacrums, one connected to the
vertebral column of Ritta and the other to that of Christina. However, these sacrums did
not occupy the backside of the (pelvic) space, but still the lateral and posterior parts did.
As a result, there should be a large gap at the backside, if not an unclear (bony) bridge had
covered the gap between both sacrums (P and Q in Fig. 5.8).

Thus, seemingly, the left os coxae (hip bones) of Ritta and the right os coxae of
Christina fused to make the unclear bony bridge that secured the connection
between both sacrums. In Serres words:
‘‘Those two rudimentary bones so brought to contact, stopped to conjoin, giving birth to
the unique piece, placed as a manner of shielding of the back of the pelvis, of which the
dimensions are larger than in a normal pelvis… It is only the iliac parts of the os coxae that
took the new form to accommodate to their use….’’ This indicates that Ritta’s left and
Christina’s right half os ischii and os pubis did not develop. The other consequence is that
Ritta’s right pubic bone did fuse with Christina’s left pubic bone via a clear symphysis.
(Left and right is always seen from the patient’s side).

Within his monograph on Ritta-Christina Serres also included another con-


joined twins, in which the double organization went below the pelvis. Serres was a
disciple of Geoffry Saint-Hilaire, who grounded Teratology the science of

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5.6 Sirene: A Seducing Pelvic Sound? 125

malformations. Saint-Hilaire and Serres looked for systematics in malformations.


In Ritta and Christina’s case, one should explain why only the os ilium appeared
rudimentary and pubis and ischii were not present:
‘‘But why in the two conjoined twins the ischii and pubic bones were missing,
while the ilium was so well developed? The reason is quite simple: The pelvis, like
the skull, like the breast, like all organization develops from outside to inside. Or,
according to this way of formation, the ilium appears first, next the os ischii, next
the os pubis. There is no exception to this rule. The absence, if it occurs like in
these cases, has to work out on the pubic and ischii bones’’ (non e vero, e ben
trovato! Even if it is not true it is well invented). One should note that embryology
was still in its infancy, and therefore, Serres was misrouted. Nevertheless, the basic
scheme Saint-Hilaire and Serres produced for the divisions of malformations still
holds [22].
Ritta and Christina were females, having one developed genital apparatus and
the other seriously reduced. There was one vulva, with its labia majores and
minores. So both in the lower extremities and the genital apparatus, the area of
division in two separate entities ended and fusion occured. We know now that
twins share the same genetic information. So what we are looking at is fusion of
genetic identical bony pelvic parts: producing the symphysis by pubic bones in the
front and fusion of iliac bones for the bony bridge at the backside of the pelvic
cavity. One could argue that pelvic bones are highly flexible in their adaptation to
misrouting during development.

5.7 Biomechanics

‘‘How animals move’’ [23] describe the start of the success story of the under-
standing of locomotion. It started early in the twentieth century with scientists such
as Gray in Great Britain and others in Germany and the USA. The notion that:
‘‘We cannot hope to analyze the physiological properties of a locomotory mech-
anism until we have a complete and accurate picture of all the forces acting on the
body during each phase of its motion’’ [24], urged quantification of structures and
application of kinematics for the understanding of animal movements. After World
War II, these studies advanced more and more with highlights like McNeill
Alexander’s ‘‘Dynamic of dinosaurs and other extinct giants’’ [25] that evolved
into Jurassic films with reconstruction of dinosaur locomotion from bony remnants
only. Surviving footprints allowed comprehension of velocity and kinematics of
the walking of dinosaurs. Indeed, the comparative approach of locomotion pro-
duced most of its knowledge.
Biomechanics and biomechatronics are now applied to human walking to help
the handicapped by electric stimulation of muscles in such a pattern that human
walking can be imitated.

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126 5 Concepts and Approaches in the Study of the Pelvis

‘‘How animals move’’ [23] contained a sentence that will be the leitmotif of this
part: ‘‘Gray also recognized that the musculature of the axial skeleton must be
coordinated with that of the limbs’’ [23]. Such coordination is by means of girdles.

5.7.1 Girdles: Bony Arches for the Support of Limbs

The first structures that can be related to girdles are present in fish. Fin articulating
structures are found as one whole cartilage, but they are not connected to the
vertebral column. The pelvic girdle of sarcopterygians (or lobe-finned fish: evo-
lutionary old fishes with fin-limbs that are thought predecessors of extremities of
tetrapods) shows one cartilage structure with a pubic, iliac and ischiadic portion,
while an obturator groove for the obturator structures can be observed.
In amphibians, it divides into three cartilages or bony pieces. The pars illium,
ischium, and pubis can already be discerned together with a real acetabulum [26].
These structures are always present around the cloaca, the primitive ending of both
rectal and urine systems. One should note that in primitive amphibians, there is
still no connection to the vertebral column. The pelvis is always bilaterally
symmetric. Left and right pelvic structures always show in the primitive situation
pelvic connections: at its upper part and at its lower part. The upper connection
will fuse with the vertebral axis (later in evolution producing the sacroiliac joints),
while the lower connection will be the future symphysis. In amphibians and
reptiles, these structures develop further and adapt to the specific conditions
needed for that animal species [26].
The condition to increase speed is that both rump and tail are clear of the
underground. In amphibians and reptiles, the belly still touches the ground,
although movement is on four legs [25]. In most mammalian species, the movement
on four legs increased the speed of the animal. Girdles are needed to anchor the
limbs to the vertebral column. In fact, the mammalian rump is suspended by girdle
muscles from the four legs above ground: best known is the horse. Let us stay with
the horse, since it is the animal that profited most of speed increase in the steppe and
the horse, as an example of cursorial (adapted to running) mammals, is regularly
used in comparisons with primates for biomechanics and body shape [27]. The
horse’s hindquarters produce most of the force that has to be brought to the fore-
hand by the strong connection of the pelvis to the axial skeleton and the tension of
the vertebral column toward the shoulder (Note that forehand and hindquarters each
carry 50 % of the horse weight). Comparison of the vertebral column with a bent,
homogeneous, elastic stave, or rod like a bow, in which the abdominal muscles
make the string, explains the function of the vertebral column as the intermediate
between both girdles [27]. Although this description of the mammalian vertebral
column stems from around World War I, it is of great value and is still used in the
description of the biomechanical interaction between horse and rider [28].
Another early comparative approach is relating, in a static situation, the ver-
tebral column, girdles and limbs to a two-armed cantilever bridge [28A]. The idea

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5.7 Biomechanics 127

(b) (a)

Tail Head

Fig. 5.9 Upper part: Two double-armed cantilever bridges representing the vertebral column
and limbs (the piers or columns of the bridge); f: thick lines, compression members of struts, thin
lines tension members of the struts; cc: main compression member; tt: main tension member,
square ttcc representing the girdle; a fore limbs, b hind limbs. Lower two figures show the stress
diagrams of the horse backbone and limbs (right) and such a stress diagram for the Dinosaur
(left); the first with main weight on front legs, the second with main weight on the hind legs.
Upper figs. reproduced with permission from Young (1975; Fig. 8.2) [28] and lower figs from
D’Arcy Thompson (1942; figs 478 and 479) [28A]

was introduced by D’Arcy Thompson and published during World War I:


‘‘Standing four-square upon its fore legs and hind legs with the weight of the body
suspended between, the quadruped at once suggests to us the analogy of a bridge,
carried by its two piers [28A].’’ This idea has won power due to the influence of
biomechanics (still in its infancy at the start of the twentieth century) in com-
parative anatomy and called the ‘‘engineers idea’’ in that time (Fig. 5.9). The
balance of the supporting beam or girder is determined by the weight born by the
piers, here metaphorically for fore or hind legs. Vertebrae are compression struts,
while ligaments and muscles are considered tension struts [28A].
The consequences for the pelvis are simple, and most mammals, except the
smallest ones, bear their heaviest weight on their front legs, like the horse, ele-
phant, and giraffe (Fig. 5.10). So the pelvic stress is less than the front girdle stress.
However, in man, we encounter a very different situation. Bipedals like the human
are bound to total stress on their pelvis. Comparison to the wallaby, by the way
totally different in its movements, is difficult because the large tail interferes in
stress assignment, since the tail makes part of the weight, which is absent in man.
By the way, especially for horse riders, the biomechanical forces that are
involved in the function of the horse pelvis have been studied and extensively
reported and are in several publications related to overloading of the musculo-
skeletal system, resulting in back problems and lameness of the horse [28].
Although a rather nice solution for the function of mammalian tetrapod pelvises
is given above, the question is: how does the pelvic girdle function in a bipedal
situation? The bow concept cannot be used, since the function of the abdominal
muscles is totally different. A string function is absent, and the vertebral column
with its lordoses and kyphose is hardly a bow.

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128 5 Concepts and Approaches in the Study of the Pelvis

Fig. 5.10 This figure shows the balance arrangement of the ‘‘bridge’’ girder in: a dog with
balanced cantilevers, b pig with single girder balanced on forelegs and hind legs, c elephant with
single girder balance largely placed about fore legs, d wallaby with single girder balanced on hind
legs, and e giraffe with single girder balanced mainly on fore legs. Figure and text are reproduced
with permission from Young (his Fig. 8.5) [28]

The human solution is described in Chap. 1 (see Figs. 1.13, 1.14). Pelvic and
femoral muscles changed their function. However, the biomechanical approach, as
evidently given for the horse and other quadrupeds, got less attention in the human
till stressed by the 1960s studies of Kummer [29].
Renewed interest in the pelvic girdle was also caused by the studies on low
back pain. Pelvic approaches to the low back pain have been described, but they
are too extensive to repeat here [30]. In fact, several center on the sacroiliac joint
[30]. A human pelvic girdle choice is inevitable: we treat the closed kinematic
chain, disregarding low back pain for the moment.

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5.7 Biomechanics 129

Fig. 5.11 Model of the


lower body: upper block is
the pelvis (as one of its six
links), the thighs (two other
links), the legs (two links),
and both feet (floor and feet
are the sixth link)
(Reproduced with permission
and courtesy from Huson,
[31A], p. 124)

5.7.2 The Closed Kinematic Chain

Suppose you are lying on your back with your legs in the air. You can make all
kind of movements with your legs. You can bend your knee, rotate your feet, and
bring down and spread your legs. You have great freedom of leg movement. Now,
if you are standing firmly on both feet, that freedom of movement of your legs is
restricted. So it is the chain of bones that make your legs behave differently if the
chain is open (lying on your back) or closed by standing on your feet. ‘‘The general
effect of a closure leads to an increase of its kinematic constraints, in other words it
is a reduction of the chain’s kinematic degrees of freedom of motion. Said in more
general terms, closure leads to a reduction of the chain’s mobility or a gain in
stability’’ [31A]. The gain in stability can be large. If one constructs a model of the
lower body part, thus pelvis and legs with its joints, this model stands by itself.
Of course, for this model, the joints are made as simple hinge joints. Nevertheless:
‘‘Notice that, in this position, the model can keep itself in an upright position while
standing on a flat surface without any external support, keeping its hips and ankles
still in a mid-position between full extension and flexion. Only the knees are
locked in full extension (Fig. 5.11)’’ [31A].
I could not believe it and constructed one myself (E. M.). It is no joke, it stands.
This self-locking effect is made possible by the pelvis. The pelvis can be con-
sidered a block (or to stay in this terminology: the pelvis itself is a closed kinematic
chain) due to the sacroiliac joint that permits nearly no movement, the fused sacral
vertebrae and the tight connection of the pubic bones by the symphysis. By standing
on your feet, the kinematic chain of your both legs is closed by the pelvis.
Thus, standing for bipedals is easy. It consumes hardly any energy, due to the
pelvic girdle that acts as a block, which closes the kinematic chain. Here, an
unexpected, nevertheless important, property of the pelvic girdle is found: the
consequences of its rigid joint qualities qualities.
The kinematic chain, whether open or closed, plays an important role in rob-
otica: whether for the understanding of human bipedal function (especially the
knee, tarsal motion of the foot and carpal organization of the wrist [31A], think
also of injuries of these joints), or for robots in the industry [31].

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130 5 Concepts and Approaches in the Study of the Pelvis

5.7.3 Finite Element Modeling and Pelvic Forces

It does not matter whether it is von Bertalanffy [32] or Alexander [25] in the 1960s
who claimed that mathematical approaches in biology are a prerequisite for sci-
entific solutions. The opposition ‘‘structure versus function’’ is based on an old
static view of the organism [32]. It will only be overcome by integration of both
morphology and physiology. Finite element modeling is the holistic tool to inte-
grate morphology and physiology, also of pelvic structures.
Finite element modeling was introduced in engineering around 1957 and in
orthopedics in 1972. It was used in orthopedics for the calculation of stresses and
strains in loaded bones. The results increased the knowledge of ‘‘artificial joint
replacements and new methods for fracture fixation’’ [32A]. In hip replacements,
knowledge of the stresses and loads in the acetabulum were needed, and therefore,
bipedal pelvic stresses and loads were studied that we will use in this chapter [35].
Let us see how stresses can explain the form of the pelvis as advocated by
Preuschoft [33]. He is concerned with the question: ‘‘Why did our ancestors
become bipeds and not quadrupeds’’? In the start of his review, he made a series of
remarks that are cited here: ‘‘Any progress of our knowledge about human evo-
lution must ultimately be linked to the fossil record, and fossils contain primarily
information about morphology. In turn, morphological traits must be closely
connected to biomechanics, in particular by causal morphogenesis (‘Wolff’s law’)
and by the interplay of mutations and selection (Darwin’s ‘survival of the fittest’).
In principle, both linkages allow the identification of selective pressures on the
basis of shape. In both cases, the main challenge is clearly to identify which
biomechanical factors lead to the observed form of the skeletal elements under
consideration, and which factors exert selective pressures on body shape. These
mechanisms are complementary, rather than alternatives. The shape of specific
skeletal elements can be explained by analysis of the mechanical stresses that the
elements must sustain in life, under normal function’’ [33].
To recapitulate: shape, in our case the shape of the pelvis, can be explained by the
analysis of the changing mechanical stresses, e.g., during standing, walking, and
running. Standing was already treated above (see Sect. 5.7.2). Walking and running
have also been studied by Mc Neill Alexander. His conclusion is: ‘‘In this paper,
I have compared the gaits of animals that walk or run bipedally, with human gaits.
The general conclusion is that no animal walks or runs as we do. We keep the trunk
erect; in walking, our knees are almost straight at mid-stance; the forces our feet
exert on the ground are very markedly two-peaked when we walk fast; and in
walking and usually in running, we strike the ground initially with the heel alone.
No animal walks or runs like that’’ [34]. Seemingly, there is a contradiction: either
we can deduce the pelvic form from our ancestors, as long as we calculate the force/
stress differences correctly, or the human gait is unique that comparison with
ancestors or other, even living bipedals like apes, kangaroos, reptiles, and birds, is
useless.

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5.7 Biomechanics 131

Fig. 5.12 Side views of


pelvic shapes of Chimpanzee
(d), Australopithecus (e) and
Homo (f). The iliac neck is
hatched. (Reproduced with
permission from Fig. 15
p. 378 of Preuschoft, [33])

Preuschoft explains the pelvic shape in the following way: ‘‘The resultant of all
forces acting on the Chimpanzee hip joint also passes through the iliosacral joint,
relieving the ilium from bending. In contrast, the iliac neck in humans is usually
exposed to bending moments. The iliac neck (hatched) therefore can be long in the
chimpanzee (a) and must be short in Homo (c)’’ [33]. Australopithecus takes an
intermediate position (Fig. 5.12).
Thus bending forces of the vertebral column present in human pelvises have to
be overcome. Shortening of the iliac neck, extended sagittal width of the neck and
the internal organization of the bone trabecular structure with on both sides high-
strength cortical bone should provide the bending strength of the ilium.
The sandwich construction of cortical bone with trabeculae in between is
indeed present in the ilium and is strongest represented at the iliac neck, around the
upper part of the acetabulum and the crista. ‘‘A simple engineering calculation for
the deflection of a beam shows that a 10 mm thick plate of trabecular bone with
two 0.5 mm thick cortical shells on either side would have the same resistance
against bending as a plate of solid cortical bone with a thickness of 7.3 mm. Thus
only a 50 % increase in thickness is needed to cause a 75 % decrease in weight’’
[35]. Moreover, calcium-equivalent densities are strongest in the iliac neck [35].
The forces the pelvic bones have to endure are due to movement or due to
stabilizing the body. These forces produce stress distributions that can be studied
with the finite element method. ‘‘It is basically a mathematical approach, whereby
a structure is divided into small geometrical entities, the elements. For each of
these elements there exists an analytical relation between force, deformation,
strain and stress, given their geometry, material properties and boundary condi-
tions. Owing to the large number of elements, handling of input and output data
and the actual calculation of the stresses and strains are performed using special
computer software’’ [35]. Thus contours of the pelvis are covered with a kind of
fishing-net. Stiffness distributions gathered from CT scans were introduced for

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132 5 Concepts and Approaches in the Study of the Pelvis

Pelvic cortical shell stress Pelvic trabecular core stress

Fig. 5.13 Lateral views of the stress intensity distributions for the left cortices and the left
trabeculae. Each of the eight phases of the walking cycle is shown [combination of Figs. 5.7 and
5.8 (pp. 97 and 98) of Dalstra [35], reproduced with permission]. For the sake of clarity, the eight
phases of the gait cycle that are discerned are given here: 1: double support, beginning of left
stance phase, 2: beginning of left single support phase, 3: halfway in left single support phase, 4:
end of left single support phase, 5: double support, end of left stance phase, 6: beginning of left
swing phase, 7: halfway in left swing phase, 8: end of left swing phase. MPa is millipascal for
stresses measured

each mesh of the net. The external hip joint forces and the muscle forces were
related to the net meshes for eight phases in the gait cycle, while the direction of
the forces were reduced from origo and insertion of the muscles (One should not
underestimate the amount of data to be collected in order to work with the finite
element method). Stress distributions for each of the gait cycle phases are the
results. Moreover, the stress intensities in the cortical shell and in the trabecular
layer can be discerned (see Fig. 5.13).
It must be obvious that the stress in the cortical shell differs from the stress in
the trabecular areas. The stress in the trabecular areas is 50 times lower than that in
the cortical shell. As to our problem (shape deduction from ancestors), the iliac
neck is not ‘‘the area of stress,’’ since phase two is the beginning of left single
support phase and six is the beginning of the left swing phase [35]. In all other
phases, the iliac neck is not the area of the highest stress. During the stance phase,
the highest stress is present at the insertion of the gluteus maximus and the incisura
ischiadica major, the backside of the iliac neck. The trabecular core shows the

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5.7 Biomechanics 133

Fig. 5.14 At the left, the reconstruction of the pelvic diaphragmatic muscles are shown. One
should note the hiatus at its upper part and the fissure made by the sacral/coccygeal area at its
lower part. The right figure gives the detailed data collection of the division of the levator ani
muscle into its elements. For the significance of marks, see the original article: Janda et al. Fig. 3
and text [36], reproduced with permission

highest stress peaks at the stance phase in the center of the iliac wing. The last
conclusion from these results can be understood because there is no trabecular area
at the iliac center; both cortical layers unite.
So loads or transfer of loads or exerted forces are not exclusively related to the
iliac neck during walking.

5.7.4 Finite Element Modeling and the Pelvic Diaphragm

The finite element method has also been used to model the pelvic diaphragm [36].
Before we consider the results, one should note that from its early development,
e.g., the ligament anococcygeum can be found, but is not described in this finite
element approach.
The clear absence of the ligaments present within the pelvic diaphragm
(Fig. 5.14) indeed does ask whether this data collection of the pelvic diaphragm is
worthwhile to be used in clinical approaches. One should remember that anatomy
is a study of data collections. If collecting data is done insufficiently one produces
problems, as we have here. First, let us establish that the ligaments are present: All
anatomical handbooks discern ligaments in the pelvis. We ourselves showed lig-
ament structures to be already present in early development in the pelvic dia-
phragm and extended by others [37]. Moreover, the gynecology group of Lille,

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134 5 Concepts and Approaches in the Study of the Pelvis

France, recently showed that MRI, as also used in this finite element study, hardly
discerns ligaments. Thus, ‘‘suspension elements, particularly pelvic ligaments, that
are difficult to identify on conventional imaging have to be incorporated according
to anatomical descriptions’’ [38A]. Here, we also encounter the difficulty to dis-
cern between collagen and muscle tissue in a formalin fixated aged cadaver, not
using histological techniques; results that are morphed with MRI data: a double
trap! By the way, the presence of such ligamentous structures presumably are
indicated by the white dots in Fig. 5.14. The finite element data also included
optimal muscle fiber length, using the sarcomere length, the physiological cross-
sectional area, and total muscle fiber length: a laborious job.
This finite element ‘‘thesis concluded, that: (1) Decreasing muscle activation
leads to the increasing width of the levator hiatus, which is associated with the
development of genital prolapse. (2) The compliance of the connective tissue of the
levator hiatus has not a large effect on the width of hiatus, therefore has not a large
effect on the development of genital prolapse (by the way this is disputed). (3) A
good quality of the muscle minimizes dispositions to the development of genital
prolapse even if there is a problem related to the compliant connective tissue of
levator hiatus. The muscle training can improve the quality and function of the
muscle tissue. (4) The surgeon has to focus on the levator hiatus width, which
should be reduced by use of mesh prosthesis in order to minimize the development
of genital prolapse. Design of a new biomaterial mesh prostheses for surgical repair
of the genital prolapse can be based on predictions of the FE model’’ [36A].
The Lille group in their comparative analysis of pelvic ligaments says: ‘‘Pelvic
ligaments differ in their biomechanical properties and there is good evidence that
the uterosacral ligaments play an important role in the maintenance of pelvic
support from a biomechanical point of view’’ [38B].
For this controversy, too, as we have frequently encountered, only excellent
anatomical knowledge will bring the correct qualitative data for a finite element
approach. Seemingly, pelvic anatomical structures can lead to strongly opposing
views.

5.7.5 Finite Element Modeling and Pelvic Organ Movement

Everybody is well aware of organ movement. If you have to climb the Eiffel tower
running, you will arrive exhausted and feel your hart, lungs, belly muscles, and
digestive organs strongly moving with regard to the other organs. Movement also
holds for the pelvic organs, even in really tranquil situations like sitting or sleeping.
This physiological mobility of the pelvic organs is vital for their functioning.
However, we hardly know how this physiological mobility is organized, nor are we
familiar with the stresses on pelvic organs and we do not understand how the pelvic

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5.7 Biomechanics 135

Fig. 5.15 Phases of addition of ligaments to get an accurate simulation of pelvic organ mobility:
a No ligaments. b Introduction of round, broad, and uterosacral ligaments. c Introduction of
paravaginal and umbilical ligaments. d Final configuration of ligamentous system (text and figure
reproduced with permission from Cosson, Fig. 6 [38A])

fascias and ligaments participate in this motion. The above-mentioned gynecology


group from Lille made a ‘‘three dimensional biomechanical model based on a finite
element approach, to define the major contributors to the static suspension of the
pelvis’’ [38A]. Movement and displacement of the pelvic organs can be studied
using MRI and dynamic MR images. An accurate simulation of the mobility of the
pelvic organs was impossible with only MRI results, in which the connective
structures are hard to discern. Addition in stages of the known different anatomical
connective structures into the model finally provided ‘‘a simulation of mobilities
that is consistent with those measured on MRI’’ [38A]. In Fig. 5.15, the ligaments
that had to be added to get an accurate simulation are given. Thus, connective tissue
matters. Moreover, the studied biomechanical properties of vaginal, rectal, and
bladder tissues differ significantly: ‘‘Vaginal tissue is more rigid than rectal tissue,
which, in turn, is more rigid than bladder tissue’’ [39]. Pelvic organ motion is
dependent on several factors of which the inherent properties of the pelvic organs
are as important as the connective structures.

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136 5 Concepts and Approaches in the Study of the Pelvis

To paraphrase Gray (as cited at the beginning of this part): ‘‘We cannot hope to
analyze the physiological properties of an organ movement mechanism until we
have a complete and accurate picture of all forces acting on the pelvis during each
phase of its function’’.

5.8 The Pelvic Sacroiliac Joint and Low Back Pain

Let us start with two citations of Mooney from his article on sacroiliac joint
dysfunction: ‘‘It is apparent from gross anatomy that this joint is not designed for
significant motion’’ and ‘‘The amount of displacement, however, is so minimal that
it has not been documented radiographically’’ [30, 40A]. Thus, as said before, the
pelvis can be considered as a block with ‘‘no’’ movement toward the os sacrum.
The recently detected small movements within the sacroiliac joint [40] do not
change this opinion: ‘‘All these studies point to the recognition that a small amount
of motion occurs at the joint, but is so minimal that it would be difficult to assess
from a physical examination standpoint’’ [40A].
The sacrum is held in between both iliac bones by the pulling of the ligaments.
This tension compresses both sacroiliac joints, and as a consequence, both pubic
bones compress the symphysis. The so-called self-locking mechanism of the
sacroiliac joint is organized by its interlocking form (see Fig. 1.9, upper right
picture) and by force. This so-called force closure of the sacroiliac joint supposes
that lateral force and friction are essential to withstand vertical load (see
Fig. 5.16).
Dysfunction of the so-called self-locking mechanism of the sacroiliac joint
could produce low back pain. Low back pain studies in patients in which anes-
thetics is administered into the sacroiliac joint show that only 13 % of patients do
have low back pain due to sacroiliac joint dysfunction. Nevertheless, there are
other less reliable studies that report from 86 % down to 22.5 % (see [40A]).
Thus, the pelvic block locked to the sacrum by ligaments and by its joints that
are both well innervated can cause low back pain. Form-closure or force-closure
changes are thought responsible (Fig. 5.16). The idea of nutation or nodding has
been introduced: ventral rotation of the sacrum relative to the iliac bones. Nutation
winds up the sacrotuberous ligament, due to diminishing ligament tension and of
course vice versa (5.17), and ‘‘therefore,’’ the force exercised on the self-locking
system should be different. If the sacrotuberous ligament can organize nutation,
other ligaments should produce counternutation. Presumably, it is the long dorsal
sacroiliac ligament that could fulfill this function. ‘‘This ligament is of special
interest since women complaining of instability and lower back pain during
pregnancy frequently experience pain within the boundaries of this ligament’’
([40A], see also [30]). Tension increases in this ligament, if the ipsilateral
sacrotuberous ligament and erector spinae muscles are artificially loaded and due
to its connection to the posterior thoracolumbal fascia, to the erector spinae
muscles and to the sacroiliac ligament. The thoracolumbar fascia is the mediator of

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5.8 The Pelvic Sacroiliac Joint and Low Back Pain 137

Fig. 5.16 Self-locking mechanism: a form closure, b forces closure, c combination of a and b,
while d shows the mechanism of an arch. Fj is mainly organized by ligaments and muscles,
reproduced from Snijders [41] with permission

The biceps attachment onto the


sacrotuberal ligament
(a) (c)

(b)

The long dorsal sacroiliac ligament

Fig. 5.17 Ligaments and fascias possibly involved in low back pain: a the continuation of the
biceps muscle onto the sacrotuberal ligament (see also b and its arrow in c); b the long dorsal
sacroiliac ligament; c even the fascia of the piriform muscle that adheres near the sacroiliac joint
into the posterior sacroiliac ligaments is thought to be involved (a and its arrow), reproduced
from Mooney [40A] with permission

forces between leg, spine, and arms. Muscles can enforce nutation or counternu-
tation. Since the forces via the fibers of the biceps muscle of the leg pass even into
the sacrum (Fig. 5.17), using the sacrotuberal ligament, biceps force is exerted on
the sacrum and thus influences the self-locking system. An analogous reasoning
can be given for the gluteus maximus.
Passive structures like the thoracolumbar fascia can be under traction of various
muscles (gluteus, latissimus dorsi, and external oblique muscle) and since this

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138 5 Concepts and Approaches in the Study of the Pelvis

fascia is connected to pelvic ligaments like sacroiliac and longitudinal ligaments,


low back pain can be induced. These structures together are thought to make a
kinematic chain that exerts its force on the sacrum.
To cite Mooney again on the sacroiliac joint and low back pain: ‘‘Thus we are
left with a clinical syndrome of low incidence and no consistent clinical findings,
and an invasive test (injection of anesthetics) as the basic gold standard on which
to make a diagnosis’’ [40A].
The reported studies can hardly be considered a tentative effort for a resolution
of low back pain. The more so, since in weight lifters the sacroiliac joint self-
locking mechanism was studied. ‘‘Weight lifting produces tremendous loads on the
sacroiliac joints, and it has been shown that sacroiliac dysfunction could decrease
performance in weight lifting’’ [42]. The outcome of the study, among other
results, was: ‘‘Specifically, hip flexion does not alter the sacroiliac locking during
hip extensor maximum voluntary contraction,’’ and ‘‘thoracolumbar fascia does
not seem to participate in the locking of the sacroiliac joint’’ [42]. These results
question the involvement of passive structures in low back pain, since the weight
lifters loads used were up to 250 N in increasing steps of 50 N. As to the proposed
treatments: ‘‘Treatment modalities include medications, physical therapy, bracing,
manual therapy, injections, radiofrequency denervation, and arthrodesis; however,
no published prospective data compare the efficacy of these modalities’’ [43].

Literature

Literature has been grouped in reference lists of several chapters in those cases where
arguments are difficult to entangle or published over several articles or books. In cases of
citation the article or book involved is indicated by the reference number together with a
capital Arabic letter.
1. Dullemeyer P (1974) Concepts and approaches in animal morphology. Van Gorcum Co,
Assen
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6. Letters to the editor (1996) J Bone Joint Surg Am 78A:1945–1946
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13. Moffat DB (1993) Lecture notes on anatomy, 2nd edn. Blackwell Science Publisher,
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15. Le Damany P (1923) La luxation congenitale de la hanche. Flammarion, Paris
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Surg 12:255–265

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Chapter 6
Sexual Organs and Society

Power can be exercised by mutilation of human sexual organs, or like eunuchs, one
can conquer power by castration. Sexual anxieties have brought mankind medical-
supported mutilations in spermatorrhoea. The removal of the prepuce is debated:
In females, it should cure several diseases (high sex drive, hysteria, epilepsia), and
in males, it should prevent masturbation and increases social status in Anglo-
Saxon countries. Circumcision should prevent in both sexes HIV and HPV for a
lifetime. The G-spot is also debated, and phantoms of sexual organs are still
difficult to explain.

6.1 Anxieties: Koro and Spermatorrhoea

Sexual anxieties have driven mankind into unwarranted attitudes toward sexual
organs and their functions. Consider two well-known conditions: koro and sper-
matorrhoea. Koro is the panic anxiety to loose the male or female external sexual
organs [1], including shrinkage of the breasts, while spermatorrhoea is the
‘‘emission of semen without copulation’’ [8], masturbation, and nocturnal emis-
sions included.
Koro was brought to attention of the medical sciences by Dutch doctors
working in the Dutch Indies (now Indonesia) toward the end of the nineteenth
century [2]. Epidemics of koro or in Chinese, suo-yang (shrinking of the penis or
decrease in yang/manhood), have occurred several times [1] e.g., in China in 1907
among students in Szechuan; in Singapore in 1967 and again in 1984–1985; in
Thailand along the borders with Vietnam in 1976; in India—Assam, West Bengal,
and Meghalaya in 1982, and again in West Bengal in 1985. Such epidemics are not
limited to Asia: They have also occurred in Nigeria, the Ivory Coast, Ghana,
Senegal, and North Eastern Congo.
These koro patients, over ten thousand men and woman in the twentieth century
hold their sexual organs in their hands to overcome retraction or disappearance.
Special instruments have also been developed to keep organs in place [1]. In
Chinese medicine, suo-yang is an illness that disturbs the equilibrium between yin
and yang; hence, yang should be enforced by, e.g., acupuncture treatment [1].

E. Marani and W. F.R.M. Koch, The Pelvis, 143


DOI: 10.1007/978-3-642-40006-3_6,  Springer-Verlag Berlin Heidelberg 2014

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144 6 Sexual Organs and Society

Two distinct forms of koro can be discerned: primary koro and secondary koro
[3]. Primary koro is the psychological expression of individual or group fear con-
cerning reproductive ability. Secondary koro is also known in the West due to mental
or somatic illnesses such as schizophrenics, psychosis, depression, urological
pathology, and, of course, drugs. The inducing fear in primary koro can come from
demons that will rob genitals (China) or socioeconomic stress, and as in Assam and
West Bengal, where ‘‘land-hungry immigrants’’ [1] were the cause, or malignant
magic in Africa, and let us not forget in the Middle Ages in the West, witches.
In 2008 [4], the World Association of Cultural Psychiatry published an article
on koro in West Bengal by Arabinda Chowdhury of the Indian Institute of
Chemical Technology in which ‘‘several ethno medical explanatory concepts like
increased body heat, supernatural, sexual, physical strain; fever and fear were
elicited as the emic framework of causes for this malady from the sufferers. Body
heat emerged as one of the primary concepts. These explanatory narratives were
put into different models of body heat pathology, viz., structural, sexual energy,
heat loss and heat avoidance and their modus operandi were elaborated.’’
Other explanations include oedipal castration anxiety [5], depersonalization
syndrome, obsessional disorder, dream explanation (‘‘loosing your virile member
signifies the failure of an undertaking’’) [1], heat–cold dualism (see citation above
[4]), and supernatural forces [1]. Koro is always related to virility and possible
infertility and a belief that it is related to or ends with a future death in some
cultures. The diverse explanations indicate a lack of good reasoning.
Koro has been endemic in ‘‘Muslim, Christian, and animist ethnic groups of the
Indonesian archipelago, but also among aboriginal tribes of Flores and in the
interior of Mindanao, Philippines, not to mention its occurrence in Thailand, India
and Africa’’ [1]. These facts undermine the argument that it is exported by Chinese
immigrants [1, 6]. Therefore, koro should be considered the expression of the
inherent consequence of sexual worry among (mainly) young people that can be
caused by social or psychological stress. It is too simple an explanation to think of
the primary koro patient as unstable, especially if the cultural framework is
‘‘simple’’ and different from the Western one.
While koro can also be seen as a worry about dysfunction of the sexual organs,
spermatorrhoea is considered an overactivity of the male organs. Let us start this
part on spermatorrhoea by citing the historian of medicine Frederick Mansfield
Hodges [7]. ‘‘As so many of the popular medical tracts of the nineteenth century
warned, the hapless male who had induced spermatorrhoea through venereal
excess or through congenital or inherited physical predispositions had symboli-
cally lost his manhood and could now only look on in horror and self-recrimination
as his vital essence drained away in uncontrollable seminal hemorrhage, rendering
him impotent, insane, epileptic, and bound for an early grave. The tragic irony is
that, in many cases, doctors promised to restore the victim’s symbolic manhood
through the surgical sacrifice of part or even all of the physical symbols of his
manhood.’’
Masturbation in Greek and Roman times was considered to be a mean to restore
imbalance of the humors. Due to the acceptance of Galenic medicine, masturbation

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6.1 Anxieties: Koro and Spermatorrhoea 145

was no problem during the Middle Ages till the seventeenth century [7A]. An
anonymous treatise published in 1710 called it pollution correlated with fits, epi-
lepsy, and death. For this ‘‘illness,’’ later known as spermatorrhoea, the author
offered a cure that could only be obtained from the book’s publisher. The medical
condition, which resonated with religious ideas about ‘‘mortification of the flesh,’’
was given a clinical foundation by the Swiss physician Samuel Tissot (1728–1797).
A milestone in the medicalization of spermatorrhea was the publication of Des
pertes seminales involontaires (‘‘On involuntary seminal discharges,’’ 3 volumes,
Paris, 1835–1845) by the surgeon Claude Francois Lallemand (1790–1853). These
volumes contained 150 case studies in which spermatorrhoea caused serious dis-
eases, leading to death in a number of cases [8]. This illness not only burdened the
patient, but also society; in Lallemands words: ‘‘a disease that degrades man,
poisons the happiness of his best days, and ravages society!’’ [8] An English
translation appeared in 1847, and from then on, this new socially constructed illness
spreads through the English medical profession like an epidemic. Not until 1869 did
the first ‘‘antidote’’ article appear in England, but by that time, the illness had also
been detected in America, with enormous consequences for patients that underwent
surgical treatment. As the urologist Dominic Hodgson put it: ‘‘…the tenacity with
which American doctors held on their belief in the concept of lost manhood after
almost all European doctors had abandoned it, and the extremes to which American
doctors were willing to go treat it, provide a vivid illustration of the uniqueness of
nineteenth century American medicine’’ [7, 8].
And of course there was money to be made from the disease [9]: A certain
Dr. Watson published a pamphlet entitled ‘‘Spermatorrhoea; its Philosophical,
Rational and Mechanical Mode of Cure, by an entirely Novel and most successful
System’’ in which he promised a cure. He diagnosed the disease from the urine
sample one sent (‘‘per post and prepaid’’) and remedy was sent to you. The
physician Henry Maund (1858) wanted to test Watson and sent in horse urine. The
diagnosis was as follows [9]:
Sir, having microscopically and chemically examined your urine, and also
considered your case, I am decidedly of opinion that your health is ‘‘critical’’ and
unless immediately attended to, impotency and its concomitant evils must ensue.
At the same time, I am glad to state, that your health (mental and physical) can be
restored, provided you adopt the means which I have found so eminently suc-
cessful in similar cases. The treatment required in your case will be ‘‘Local and
Constitutional’’ therefore a curative Instrument is most essential. If the means are
applied as directed I can guarantee a cure. Yours obediently, pro Dr. Watson, Wm
Hill, M.A., Sec.
Money could also be made from instruments of which the ring with four pins on
the inside is the best known, and it stopped nightly erections by means of the
unpleasant pin pricks. More sophisticated instruments were also developed. The
improved spermatorrhoea instrument designed by Reynolds [10] (Figs. 6.1, 6.2,
6.3, 6.4) was published by The United States Patent Office as Letters Patent 33, 162.

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146 6 Sexual Organs and Society

Fig. 6.1 The four figures of


Reynolds (1861) together
with part of the patent text.
a lower, b upper part of cone-
cap, c coil-spring, d and
e pressure plates, f and
g spring-bars, h secondary
pressure plate with roughened
surface, i locking mechanism
pressure plates, j belt

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6.1 Anxieties: Koro and Spermatorrhoea 147

Fig. 6.2 Left the scheduled types of female circumcision by the WHO, reproduced with
permission. Right picture: ‘‘Type III female circumcision. Note the presence of partial labia
majora and minora with a surgically absent prepuce and clitoris. A small anterior and posterior
opening is retained for the expulsion of urine and vaginal, cervical, and uterine secretions’’ (from
Chen [35], reproduced with permission)

Fig. 6.3 Distribution of the


lymphatic system in and
around the vulva. Lymphatic
fluid direction is indicated by
arrows: 1 lymphatic plexus at
the front of the symphysis,
2 lymphatic plexus of the
vestibulum, 3 lymphatic
plexus of the perineum,
4 lymphatic fluid direction
toward the inguinal lymph
nodes, 5 and 6 lymphatic
plexus of labium minus and
majus, respectively (with
permission from Kamina
[34])

As odd as it may seem, a counterforce with spring and pricking plates, the
application of engineering to ‘‘all day’’ problems was typical to the Industrial

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148 6 Sexual Organs and Society

Fig. 6.4 The third picture of De Graaf’s Alle wercken [46]. His Dutch text is given in translation,
and note that the seventeenth-century terminology is translated in the now being in force
anatomical terminology: First picture shows the Kittelaar in a frontal view. A De Kittelaar (the
tickler, clitoris), BB crus of the clitoris, C the glans of the clitoris, D prepuce of the clitoris, EE
bulbus of the clitoris, FF part of the periost, by which the crus of the clitoris is adhered to the lower
part of os pubis, GG muscles of the clitoris (m.ischiocavernosus), HH part of the ligaments by
which the muscles are attached to the tuber, II: the nerves, KK arteries, LL veins; Second picture
shows the Kittelaar from the backside. A De Kittelaar (the clitoris), BB crus from the reversed side,
CC the muscle over the crus, DD the fibers of the muscles, producing a hollow, EE the fibers of the
m.bulbospongiosus. Third and fourth picture show various transsections of the clitoris. a the
clitoris, b glans of the clitoris with bulbus, c cavernotic part with partition, d cavernotic part
without partition (reproduced with permission from the Leiden University Library)

Revolution. For example, James White, an English civil engineer, published


‘‘A new Century of Inventions’’ [11], in which ‘‘A mechanical assistant for the tea
table’’ (a self-standing teapot connected to a turntable with cups) was proposed:
‘‘My object is to obviate for them (the ladies) the necessity of tediously wielding a
ponderous teapot.’’ In all fairness, White also described a ventilator and a washing
machine for hospitals.
But what is the difference in the underlying concepts between spermatorrhoea
and koro: both are based on lack of knowledge of the uropoietic and genital
organs, both are based on individual and/or group fear, both indicate the loss of
manhood, both cause dysfunction of the genital organs, whether infertility or
impotence, and both point to an early death? Therefore, both koro and sperma-
torrhoea are expressions of the inherent consequence of sexual worry present in

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6.1 Anxieties: Koro and Spermatorrhoea 149

mankind that can take the form of social or psychological stress and/or fear.
Misuse of this fear by medical science in an effort to influence ‘‘the direction
society was taking and propose itself as the most appropriate institution to bring
about significant improvements in standards of conduct…’’ [7] was the root of the
spermatorrhoea evil poured forth on nineteenth-century patients.

6.2 Circumcision, Castration and Mutilation

‘‘Certain psychoanalytical interpretations consider sexual mutilations as funda-


mentally ambivalent: de-organising and evil when imposed on an unwilling sub-
ject, they become reorganizing and beneficial when intentional: the circumcision
that liberates the penis from its feminine part so as to accentuate its phallic
character, and thus aiming with the help of all these sexual mutilations, to over-
come a fundamental anxiety’’ [12]. So writes M. H. Libert, a urologist at the
Centre Hospitalier César de Pape in Brussels. We will hold this statement up to the
light, especially in the case of female circumcision, and come to a different con-
clusion: But first some history.
Ancient Egyptians, especially priests, used circumcision initially as a symbol of
social class. Foreskin offering was a sign of group solidarity and religious sub-
mission to the gods. Circumcision was carried out on boys 13–14 years of age.
Later all males underwent circumcision in Egypt. Visitors to religious events or
sacred places had to be circumcised as well, as the story of Pythagoras, visiting
religious happenings in Egypt, tells us. ‘‘Today all Egyptians are still circumcised,
whether Muslim or Copt’’ [12].
In their History of Circumcision, Dunsmore and Gordon write ‘‘For the Greeks,
circumcision was a shocking act! There was no greater inconvenience for an
athlete appearing naked in the arena than to exhibit himself with a naked glans…!’’
[12]. Hellenising Jews, those that assimilate to Greek and Roman culture, tried to
recreate their foreskins to avoid social harassment. During Nazi time, before and
during the Second World War, Jews enlarged the foreskin to escape the concen-
tration camps. Little is known on how and when during the Second World War
such clinical approaches were done [12]. Uncircumcision methods are known from
Celsus (25 BC–50 AD) which stayed in practice till the twentieth century [12].
In the Arabian Peninsula, circumcision was in use before the coming of Islam.
Circumcision is not prescribed by the Koran. Nevertheless, the Sunna (‘‘i.e., the
rules of conduct established by the prophet, who so commands’’ [12]) does. It is
also common practice in several African tribes as rite of passage for young males
into the ‘‘clan,’’ ‘‘to demonstrate their virile prowess as future hunters, warriors
and procreators,’’ and there is ‘‘no underlying religious imperative’’ [12]. The
circumcision of males among Jews was adopted in Egypt and is one of the main
ritual practices. It must be carried out 8 days after birth. According to Hebrew
scripture, the practice originated with Abraham in the sacrifice of his son Isaac. It
was also carried out on his other son Ismaël, the father of the Arabic peoples.

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150 6 Sexual Organs and Society

To date, little has been written on the history of female circumcision. Herodotus
(fifth century BC) should already have described female circumcision by Egyp-
tians, Ethiopians, Phoenicians, and Hittites [13]. However, this quote is doubtful,
since it concerns male circumcision. The quote that Agatharchides from Cnidus
has described female circumcision in the second century BC is also unsure. ‘‘It is
customary for the other Troglodytes to circumcise their genital organs, just as do
the Egyptians, but the tribe the Greeks call ‘Colobi’ have the custom of cutting off
with razors during infancy the whole portion that others circumcise’’ [13]. Since
partial circular removal of the male prepuce also occurred in Egypt, this is not a
sound quote for female circumcision. Dutch and English travelers do report on
female circumcision in sixteenth and seventeenth centuries [13]. Nowadays,
female circumcision is described for Christians, Muslims, Jews, and Africans.
Arguments to perform female circumcision, found in the literature, are ‘‘believe to
be an economic necessity since the men would be away from their homes for long
periods of time, and therefore, wanted assurance that any children born during
their absence were their own’’ [13], the other ‘‘main motivation seems to be in
controlling women’s sexual urges, and the belief that circumcision makes a
woman more feminine’’ [14]. In England, in the nineteenth century, excision of the
clitoris and labia minora was carried out, even without knowledge of the patient by
Isaac Baker Brown, President of the Medical Society of London. It must have been
‘‘several thousand such operations’’ [13]. The removal of female genital parts was
to cure ‘‘nymphomania (high sex drive) but also to prevent masturbation, hysteria,
epilepsy, melancholia and insanity’’ [13].
Female circumcision can be carried out by minor removal of vulvar parts and
by serious mutilation. The World Health Organization classified it into 4 types:
Type I: excision of prepuce and part or all of clitoris, Type II: excision of prepuce
and clitoris together with partial or total excision of labia minora, Type III: infi-
bulation and excision of part or all of external genitalia (Fig 6.2), and Type IV:
pricking, piercing, incision, stretching, scraping, or other harming procedures on
clitoris and or labia [13]. Female circumcision is considered mutilation, while
male is not.
One should note that male circumcision can be religious motivated or not and
can be performed on newly born, (pre)pubescents, or grown-ups, but it always has
a social or religious purpose. Female circumcision is performed on the women by
social power or the need for social integration [25, 26] and can be carried out at
birth, into adolescence, but few religious arguments can be found in the literature.
Female circumcision in southern Chad, which is the removal of the clitoris, as
carried out by the Sara people shows that ‘‘Initiation, which typically occurs
during adolescence, is the Sara’s primary ritual event. The ceremony is designed to
educate Sara girls to be responsible members of the adult community, to venerate
their ancestors and to respect the group’s traditions. During this period, character
traits valued by the Sara–strength, bravery, endurance and industry—are incul-
cated through a series of rites; with few exceptions, ritual circumcision is the
principal rite associated with the female ceremony’’ [25]. Lynda Newland, a social
anthropologist at the University of the South Pacific, has shown that in West Java,

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6.2 Circumcision, Castration and Mutilation 151

too, female circumcision has social function [26]. Here, circumcision involves
pricking into the vulva mouth and scraping off a little of tissue. ‘‘While my
fieldwork experiences shocked me at first, it quickly became clear that female
circumcision was not performed with any intention of violence, abuse, or even
harm toward girl-children and did not seem to have any measurable effect on their
lives. Instead, parents were fulfilling their obligations by circumcising boys and
girls to conform to a moral order deeply identified with Islam and to position them
appropriately in the Muslim community’’ [26]. Lori Leonard, an anthropologist at
the Johns Hopkins School of Public Health, concludes about the custom of the Sara
in Chad to remove the entire clitoris that ‘‘Female circumcision serves a clear and
essential function for most Sara. Efforts to reduce or eradicate the practice in
southern Chad will be more likely to succeed if they acknowledge that function.
The challenge, then, is to identify suitable alternatives to circumcision which
facilitate the transmission of group values without compromising women’s health
and well-being’’ [25], but West Java ‘‘zero tolerance policies toward female cir-
cumcision seem out of touch with the realities experienced at the grass-roots
level.’’ Therefore, a differential application of Beijing Declaration and Platform for
Action [27] is considered in those countries where female circumcision is ende-
mic, but is also considered to undermine the idea of abolishing this practice.
The examples given have no basis in fact or common sense. As J. L. Strickland,
a gynecologist at the University of Missouri at Kansas City, remarks, ‘‘Many
cultural myths are present in societies where female circumcision is practiced.
Female genitals may be seen as unattractive, with the smooth hairless appearance
having greater aesthetic value. Uncontrolled genital growth, infertility, poor
hygiene, and fetal death at the time of delivery have all been given as justification
for the need for genital alteration. Circumcision is thought to heighten male sexual
pleasure. The unfortunate reality is, however, that the risk of sexual dissatisfaction
and even infertility resulting from inability to satisfactorily penetrate the scarred
introitus is higher. As many as 35 % of women may have coital difficulty requiring
medical intervention’’ [28]. Diseases originating from female circumcision are
multiple: Direct effects are hemorrhage, infection, and severe pain; long-term
effects noted in literature are urinary disturbances (stream, dysuria, and retention),
ascending genital tract infections, tetanus, urinary tract, and vulvar abscesses are
reported, but also dysmenorrhea, dyspareunia, infertility, sexual dysfunction, and
pregnancy- and delivery-related complications (see Ref. [28]). In the field of
psychology, ‘‘Circumcision has been associated with anxiety and depression as
well as distressing sexual dysfunction in some groups’’ [28].
Returning to male circumcision and masturbation, in the nineteenth century,
scientists thought that the ‘‘illness’’ of masturbation could be cured by circumci-
sion: This ‘‘heinous sin of self-pollution’’ brings insanity [16], but ‘‘circumcised
boys do not masturbate’’ [15]. Around the end of that century, it was claimed that
circumcision not only cured paralysis, hip joint diseases, and sexual neurasthenia
(a temperament induced by exhausting climate, work, worry, alcohol, and
tobacco), but also edema, eczema, elephantiasis, gangrene, tuberculosis, and
several other conditions 16]. As a consequence of the increased social status of

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152 6 Sexual Organs and Society

being circumcised, 80 % of British upper-class men were circumcised compared to


50 % of the working class [17]. In the USA, circumcision reached nearly the same
high percentage for the entire male population (79 % [29]) around the 1980s, due
to the idea of protection against diseases. In his book Just a snip? A Social History
of Circumcision, Peter Aggleton of the Institute for Education, University of
London, states ‘‘It has frequently been claimed that male circumcision offers
protection against sexually transmitted infections for men, especially in develop-
ing countries. Yet in precisely these settings, few if any investigations contain
robust controls for confounding factors such as social background, sexual behavior
or penile hygiene. Most usually the studies cited report on small and adventitious
samples of men attending Sexual Transmitted Infections (STI) or HIV clinics’’
[17]. A large study among British males in 2003 concluded as follows:
‘‘We did not find any significant differences in the proportion of circumcised
and uncircumcised British men reporting ever being diagnosed with any STI
(11.1 % compared with 10.8 %, p = 0.815), bacterial STIs (6.4 cf 5.9 %,
p = 0.628), or viral STIs (4.7 cf 4.5 %, p = 0.786)… We also found no significant
associations between circumcision and being diagnosed with any one of the seven
specific STIs.’’ [22].
So, there is no correlation between circumcision and sexual transmitted
infections that could be established in men.
In the article ‘‘The prepuce: A mistake of nature,’’ researchers of hospitals in
Stockholm stress literature, indicating that circumcision of the just-born male
diminishes the occurrence of infantile urinary tract infection [17A]. American
urinary tract infections in the newborn are substantially lower compared to
European data: a difference of nearly 2.5 times in favor of the circumcised
American babies compared to non-circumcised European babies. For the USA,
this means that 20.000 urinary tract infections in babies are avoided. ‘‘That the
prepuce is a mistake of Nature seems improbable’’ and somewhat earlier, the
results ‘‘indicate that a common potentially lethal disease, early infantile male
urinary tract infection, can be prevented by extirpation of a piece of normal,
healthy tissue of universal occurrence in males’’ [17A]. In short, authors do not
believe in circumcision for health purposes. The authors are bacteriologists, and
they come up with an astonishing microbial explanation. When mothers in normal
situations deliver, they also defecate and infect their babies with their own gut
flora. By the placenta and mother milk, the immunoglobulins were and are
transferred that specifically protect against this maternal infection. The bacterial
flora adheres particularly to the inside of the prepuce. Moreover, the clean mucous
membranes of the baby’s prepuce tend to preserve the bacteria that occupy the
membranes for the first time, called the ‘‘race for the surface.’’ In the hospital
situation, this is overcome and a non-mother-like infection has to be obtained for a
sound gut flora, with the consequence that maternal protection by breast milk
immunoglobulins does not work. ‘‘Under such circumstances extirpation of the
prepuce could be especially effective as a preventive measure’’ [17A], explaining
the positive effect of circumcision on infantile urinary tract infection.

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6.2 Circumcision, Castration and Mutilation 153

Nowadays (2010), a bitter discussion [18, 19] has once again risen on cir-
cumcision. It is argued that circumcision protects against human immunodefi-
ciency virus (HIV) infections [20] and human papillomavirus (HPV) infections
[21]. But doctors opposing circumcision have produced a declaration against the
use of it [19] (for the list of their arguments see the declaration).
Moreover, and at the same time, as there are calls for a radical scaling-up of
male circumcision throughout Africa, the [17] ‘‘…circumcision experiment has
already been performed in the United States. How successful has it been? With the
highest rate of circumcision (in the developed world), the USA also has higher
rates of infant mortality and shorter male life expectancy than similar developed
nations; the highest rates of sexually transmitted diseases of any developed nation;
the highest rates (by far) of heterosexually transmitted HIV infection of any
developed nation; and rates of cervical and penile cancer that are similar to those
of other developed nations. Yet these are the very diseases that circumcision has
been touted as a sure preventive for: any impartial observer must conclude that the
century-long experiment has failed’’ [23].
Scientists in favor argue that circumcision of newborns is highly protective
against invasive penile cancer at newborn circumcision [24] and that ‘‘the most
significant protective effect of circumcision is against HIV/AIDS, a modern day
plague that has killed over 20 million people in the past 20 years, and is now being
carried by over 40 million men, women and children worldwide’’ [18]. One can
find more arguments in favor: prevention of severe infant urinary tract infection, of
cervical cancer in female partners, of local foreskin infections, of phimosis
(inability to retract the foreskin), and of penile skin disorders (see Ref. [18]).
Genital hygiene is easier to maintain [18]. Schoen [18] ends his introduction in
favor of male circumcision with the following statement: ‘‘Unlike conventional
vaccines, which each protect against a single disease (polio, diphtheria, tetanus,
measles), one procedure, newborn circumcision, protects against multiple disor-
ders for a lifetime, while many vaccines wear off after a number of years and
require booster immunizations.’’ It has to be said that the last citations are taken
from a debate article [18].

6.3 The Prepuce

It seems time to study the prepuce [30a, 53]. What do we know of its anatomy and
its functions?
The prepuce is present in the human male and female. It is a common feature in
most mammals and is present for over 100 million years, in apes for over 65
million years, and in primates for over 10 million years. It covers the glans penis
and the clitoris and has a common embryological origin. Clitoris and glans penis
are homologous structures, and this means that the removal of the clitoris in
females should be compared to taking away the glans in man. The ingrowth of a
lamellar structure in the glans and the consequent splitting of it produce the

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154 6 Sexual Organs and Society

separation of the prepuce from the glans penis during development. In fact, in
embryologic sense, the prepuce is glans. This lamella, since it covers the inside of
the prepuce and the future glans surface, produces the mucosa of both. This
mucosa layer separates slowly into prepuce and glans covering. This process can
take until puberty to complete, but is already completed in 80 % of the boys of five
years. It is this mucosa, but also the outer skin of the penis, that should be sensitive
for HIV uptake, due to the presence of a special type of cells: Langerhans cells
(LCs) are a type of dendritic cells that collect and bring infectious agents to the
immune system, especially T4 cells (the CD4+ ones), which in their turn give an
immune response [30]. These LCs are characterized by so-called Birbeck granules,
in which pathogens can accumulate, but of which the viral killer function is still
debated. LCs are believed to proceed into the lymph nodes by the lymphatic
vessels to activate the T cells [36]. ‘‘Recent evidence demonstrates that the LCs in
the foreskin have a protective effect against pathogens, including HIV, by pro-
ducing the protein langerin [31]…, it has now been shown that langerin transports
HIV-1 to locations within the LC where the virus is destroyed’’ [32]. One year
later, the same group showed that ‘‘HIV-1 infection of LCs and subsequent
transmission to T cells is an inefficient process. Langerin, a C-type lectin specif-
ically expressed by LCs, captures HIV-1 and acts as a protective barrier for HIV-1
infection by targeting HIV-1 to Birbeck granules for degradation. However, when
the Langerin function is blocked or saturated using high virus concentration this
barrier can be overcome. These conditions allow LC infection and subsequent
HIV-1 transmission to occur’’ [33]. The LCs stay present and are everywhere
distributed in the mucosa, left after circumcision, and therefore either protect
against or in the case of overload of virus spread the virus. It is not feasible to
remove all LCs from the remaining mucosa. However, there are currently rather
biased discussions on the number of LCs in the mucosa: less than in the outer skin
[37] or in equal amounts [38].
It must be clear that the immune response is important. The immune system
mainly resides in the lymphatic system, and this brings us back to female
circumcision.
In female circumcision by removing the clitoris, prepuce, and labium minora
and partially the labium majora, one removes the larger parts of the lymphatic
system of the female external genitals (Fig. 6.3). In fact, one reduces the female
immunological response to threatening diseases. Nevertheless, research on HIV
infections in circumcised women produces conflicting results: Either circumcision
either increases the possibility of HIV infection [39] or it does not [40].
The interaction between circumcision and HIV is difficult to disentangle due to
‘‘an underlying complex interplay of bio-behavioural and social variables’’ [41].
However, bacterial infections are directly related [40]. To indicate the complexity
of this problem, the following citation is given: ‘‘Circumcised male and female
virgins in nationally representative samples of Kenyans, Lesothoans, and Tanza-
nians were substantially more likely to be HIV infected than uncircumcised vir-
gins. Among adolescents, regardless of sexual experience, circumcision was just as
strongly associated with prevalent HIV infection. However, the relation between

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6.3 The Prepuce 155

circumcision and HIV infection changed direction (uncircumcised persons more


likely to be HIV positive) in adults’’ [42].
A second aspect is the innervation of external genitals. Frederico Andahazi’s
historical novel ‘‘El Anatomista’’ on the discovery of the clitoris [43] and its
sensibility won the Fortabat Prize in 1996 for the best first book by an Argentine
author, but Amalia Lacroze de Fortabat, the originator of the prize, refused to
present the prize due to its ‘‘scandalous’’ content. This book is illustrative of the
opposition of the Catholic Church to disclose genital anatomical findings. In 2010,
Le Monde published an article ‘‘La grande énigme du plaisir féminin’’ (The great
enigma of female pleasure), which started with the following statement: You
should realize, Sir, that there is no study for sexology at the university? It is only a
facultative specialization at the end of the education, even in gynecology. Con-
cerning medical research on the anatomy of the clitoris or G-spot, they are all
recent and don’t find financing. (‘‘Vous vous rendez compte, monsieur, qu’il
n’existe aucune formation à la sexology à l’université? Elle est juste une spe-
cialisation en fin d’études, facultative, même en gynécologie. Quant aux recher-
ches médicales sur l’anatomie du clitoris, ou le point G, ells sont toutes récentes, et
ne trouvent pas de financement’’ [44]). Much the same is stated in ‘‘The anatomy
of the clitoris’’ [45]: Even handbooks omit the anatomy of the clitoris [45].
The fact is that In Holland, around 1660, Regnoldus de Graaf (1641–1673)
studied the female sexual organs. From his posthumously collected works (Alle de
wercken, so in de ontleed-kunde als andere deelen der Medicyne [46]), the only
conclusion can be that he accurately described the female genital anatomy with
muscles, blood vessels, and the bilateral innervation of what he calls the Kittelaar
(tickler, see Fig. 6.4). The Kittelaar is in our terminology both the glans and crus
clitoridis. To support this statement, only one citation is given: ‘‘Hier staat aan te
merken dat de Senuen over de rugge des Kittelaars heenlopende, seer groot sijn en
tot in alle de Deelen der Schamelheydt verspreyt werden’’ (one should note that
the nerves pass over the back of the ‘‘Kittelaar,’’ they are very large and spread
into all pieces of the privy parts), and in his figures (first, third, and seventh plate),
it is clear that an adequate description of the anatomy, blood vessels, and inner-
vation of the female sexual organs has already been given in the seventeenth
century. In Germany, Georg Ludwig Kobelt [46] produced an entire book on the
external genitals as early as 1844, André Hovelacque’s [47] Anatomie des nerfs
craniens et rachidiens et du systèm grand sympathique contained two pages and
one figure about it in its overview of human nerves. Kobelt’s work found its way
into most handbooks in Germany, e.g., Cornings Lehrbuch der Topographisch
Anatomie [48], also containing several figures (idem Hafferl [49]). Dickinson [50]
wrote human sex anatomy, and Kamina [34] in France (Poitiers) renewed two
volumes on ‘‘Petit Bassin et Périnée’’ in 1995, with at least 16 pages dedicated to
the aspects of the vulva and clitoris. Statements such as ‘‘Typical textbook
descriptions of the clitoris lack detail and include inaccuracies. It is impossible to
convey clitoral anatomy in a single diagram showing only 1 plane, as is typically
provided in textbooks, which reveal it as a flat structure’’ [45] do not do justice to
these anatomists who studied the female vulva and clitoris, of course from

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156 6 Sexual Organs and Society

Fig. 6.5 Collage of two pictures: The reconstruction of the encapsulated fiber is taken from
Weddell et al. [52], adapted and reproduced with permission, while the sections of the clitoris and
glans penis with the localization of the encapsulated fiber endings are from Cold and McGrath
[53], adapted and reproduced with permission

perspective of the clinician, not that of the psychologist or anthropologist.


Moreover, since most Anglo-Saxon scientists lack knowledge of German and
French, one should not be surprised that such statements are produced (especially
not if one does a search from 1966 forward [45]) and one should not bother to
search the older literature, which seemingly now even holds for French scientists.
Since gynecologists see the vulva in frontal view, it is hardly astonishing that
anatomists give the same view in their descriptions, if that is 2D, so be it.
Most anatomists stress the sensibility of the male and female external genital
organs. The top of the clitoris is overwhelmingly rich in Ruffini corpuscles, which
are slow adapting mechanoreceptors, while the base of the clitoris contains Vater-
Pacini corpuscles, fast adapting mechanoreceptors. By the way, the theater piece
‘‘Vagina monologues,’’ written by Eve Ensler in 1996, explains that the clitoris has
twice the number of nervous innervations as the glans penis.
The entire mucous covering of the prepuce and both labia contain these recep-
tors. Rich distributions of free nerve endings are present over the whole vulva and its
clitoris [51]. ‘‘Once neural stimulation is presented to the distal nerve terminal the
sexual reflex is begun. Sexual arousal depends on a circuit or feedback loop’’ [51].
However, the insides of the prepuce and glans of the clitoris and the prepuce of
the penis are characterized by the so-called encapsulated fiber endings, also known
as Krause’s bulbs or Dogiel’s bodies, discovered by Dogiel already in 1893 in the
human genitals [54]. They are held responsible for the registration of fine touch
(Fig. 6.5). Meissner mechanoreceptors are also present. All these receptors are

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6.3 The Prepuce 157

responsible for sensations such as fine touch, pressure, proprioception, and tem-
perature. Free nerve endings are related to pain. In humans, the male prepuce is
covered with the sensors for fine touch not the glans; circumcision therefore
changes the penile sensation. ‘‘Most likely, the changes in copulatory behavior in
circumcised male mammals are explained by the sensory alterations caused by
preputial loss’’ [53], and ‘‘The imbalance caused by not having the input from the
now ablated fine-touch receptors may be a leading cause of the changes in sexual
behavior noted in circumcised human males’’ [53]. After circumcision in females,
in which the clitoris and labia are removed, the most sensory input is destroyed,
also meaning that libido, or sexual arousal, is absent or difficult [14, 51].

6.4 G-spot: Clitoral and Vaginal Orgasm

Despite numerous efforts, orgasm remains the most poorly understood of the sexual
responses, and attempts to propose an universally accepted definition of ‘‘orgasm’’ have
met with little success [63, 67].

Innervation of the external genitals brings us directly to the G-spot, an eroge-


nous zone on the anterior vaginal wall that expels urethral ejaculate at orgasm and
the discussion on vaginal and clitoral orgasm. Let it be clear from the beginning
that the G-spot is contested [55–57]. Originally, it was described by the Dutch
Regnoldus de Graaf [46] and later by Grafenberg in 1950 for sexual and orgasmic
problems in women in the International Journal of Sexology. Its place is at the
ventral side of the vagina at a depth of 5–10 mm from the vaginal entrance.
The point is that the female urethra and the anterior wall of the vagina are inti-
mately connected by connective tissue and only sparse innervations can be found
in this area.
Nevertheless, the anterior wall knows a series of nerves passing lateral to the
connective area between vagina and uterus. What in Fig. 6.6 is called posterior
urethral nerves that are of course also anterior vagina nerves. Hardly any single
neuron can be perceived in this area, and the innervation is mainly related to blood
vessels or in the vaginal wall or around the nearby vessels. The neuropeptides
(e.g., vasoactive intestinal polypeptide) that are found in these blood vessel nerves
are functional for vessel dilatation related to sexual arousal [59]. Neither a strong
concentration of innervating nerves nor corpuscles that can perceive sensibility at
the G-spot have as yet been found. There is no sound evidence; therefore, that
activation of the so-called posterior urethral nerves by penile pressure is involved
in sexual orgasm in females.
Koedt [60] states that the female orgasm is clitoric in origin and that the vaginal
orgasm is a fabrication by males, even a Freudian concoction. Although contested,
the influence of this feminist book went beyond a ‘‘progressive’’ sound. Under the
influence of feminism, research on the vaginal orgasm was already increasing.
The thickness of the urethrovaginal area is larger in women who experience

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158 6 Sexual Organs and Society

Fig. 6.6 Nerve complex


between vagina and urethra.
Figure is reproduced with
permission from Kalfa [58].
Rectum is in brown, vagina in
green and urethra with
sphincter in purple. Nerves
are transparent yellow, while
posterior urethral nerves are
solid yellow (arrows)

vaginal orgasm [61] compared to those that are without it, while ‘‘In a large
representative sample of the Swedish female adult population (N = 1,256), having
an orgasm from purely penile stimulation of the vagina (as opposed to orgasms
from clitoral stimulation) was associated with greater satisfaction (with sex life,
mental health, relationships with both partners and friends, and life in general),
more frequent sexual desire, greater likelihood of having one’s first orgasm from
intercourse rather than masturbation, and lesser masturbation frequency’’ [62].
These results are presented with the title ‘‘Vaginal orgasm is associated with better
psychological function.’’ The vaginal orgasm appears to exist psychologically, but
an anatomical or physiological basis for it has not been discovered (yet?). One
explanation given is that the clitoral bulbi reach deep just above the vestibulum or
entrance of the vagina. Pressure on these bulbi could be perceived and produces
the above-mentioned vaginal orgasm. Variability in the expansion of the bulbi
could be responsible for the difference in the presence of vaginal orgasm. To end
this section, the following citation [63] demonstrates how tricky orgasm research
can be:
‘‘Currently, attempts to account for variability in the orgasm response have taken
a limited categorical, anatomically based approach. The focus on genitopelvic
triggers (e.g., clitoris versus vagina) implies, for example, that female orgasm is
solely a physiological event mechanistically dependent on stimulation of genito-
pelvic parts and that ‘clitoral’ versus ‘vaginal’ orgasms are very different entities.
This approach indicates little about characteristics of the orgasm experience itself.
Much of the evidence for the validity of these typologies involves uncontrolled self-
reports without concurrent psychophysiological corroboration’’ [63].
So, the question arises, do we have objective criteria to determine an orgasm?
Yes, there are, but all are anatomically/physiologically based approaches (see
citation above): ‘‘Masters and Johnson [64] observed genitopelvic and anal muscle

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6.4 G-spot: Clitoral and Vaginal Orgasm 159

contractions initially occurring at 0.8 s intervals and then tapering off with longer
intercontractile intervals’’ [63]. Others confirmed and supported these results [63].
The mean duration in females is 16.7 s and in men 25 s. However, ‘‘the subjective
experience of orgasm is not completely dictated by the absolute presence or
absence of muscle contractions but may be more related to contractile qualities
such as strength and frequency’’ [63]. Nevertheless, it is objectively measurable.
Moreover, contractions of the anterior one-third of vagina and uterus are involved
in the orgasm [64]. Therefore, measuring contractions of smooth and striated sex
muscles is an objective indicator for orgasm, but anal contractions as well. Blood
pressure, sweating, body rigidity, muscle spasms, hyperventilation, vocalizations,
rocking pelvic motions, and shuddering are involved, but not all are objectively
demonstrated [63].
Now let us return to the 1,256 Swedish female adults. If we want to know more
on the ‘‘orgasm experience itself,’’ one of the prerequisites then is to objectively
determine that an orgasm has occurred. The ‘‘Sex in Sweden’’ study that is used to
obtain the results is based on interviews by trained research assistants. The study
showed that ‘‘The associations between vaginal orgasm and aspects of better
psychological function were not confounded by the nearly significant association
between vaginal orgasm and frequency (past 30 days) of penile—vaginal inter-
course. However, frequency of penile—vaginal intercourse was independently
associated with many of the same indicators of better psychological function’’
[62]. So, in fact, no objective measurements for orgasm were taken, nor did the
study show a direct relation between vaginal orgasm and better psychological
function. To substantiate such a relation, other indicators were used.
It is a long way that brings us back to innervation: Vaginal orgasm should pass
through by the vagus nerve (Xth cranial nerve) [62], given as an explanation in the
1,256 Swedish female adult articles, and since spinal cord-injured women still can
have orgasm [67], the vagus nerve should bypass the spinal cord.
However, the handbook on human and animal autonomic nervous system [65]
shows no involvement of the vagus nerve in the pelvic organs and ‘‘It will be
remembered that the gastrointestinal tract relies largely on the vagus for its
parasympathetic supply, but that this ceases at the terminal part of the transverse
colon’’ [66], therefore not reaching uterus, vagina, cervix, or clitoris [34, 47].
Nevertheless, NMRI research showed activity present in the end sensible nucleus
of the vagus nerve (nucleus tractus solitarii) in spinal cord-injured woman after
orgasm [68], but not in all. Evaluation of spinal lesions is not direct, and more
accuracy in determining lesion characteristics is wanted. In favor is also that
pregnant women with spinal cord injury below T12 noticed uterine contractions
and movement of their fetus in utero. Therefore, a bypass of the spinal cord is
looked for and mediation of the sensibility must pass along, e.g., the vagus nerve.
Since the vagus nerve does not reach the pelvic organs, the only possible
alternative is, as given by Courtois et al. [67], over the sympathetic routes. So
sensibility of pelvic organs uses the sympathetic pathways (Fig. 6.7), which are
demonstrated for the uropoietic system too [69]. One should note that cutting the
vagus nerve in animals (mainly rats) and consequently suppressing orgasm do not

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160 6 Sexual Organs and Society

Fig. 6.7 Neurophysiologic


model of pathways for
orgasm. Next to the spinal
cord at the left are the
sympathetic trunks, related to
the organs by their fibers. In
red are the spinal cord
bypassing sensory pathways.
Figure is taken from Courtois
[67]. Figure is adapted and
redrawn after Courtois [67]

prove anything, because sensory autonomic nerves can join the vagus nerve in the
entire neck region, and such cuts normally are carried out high in this area (these
nerves, called the aortic depressor nerves, are important for the baroreflex, but also
relay other sensory information, and in animals, the separation of sympathetic cord
and vagus nerve is not as outspoken as in humans). Moreover: ‘‘Sacral and lumbar
fibers arising from neurons in the base of the dorsal horn, which can be activated
by distension of the colon and the uterine cervix, also terminate in the caudal
solitary nucleus’’ [70]. Therefore, the brainstem relay center for sensory infor-
mation on the cervix is the nucleus of the tractus solitarii, to which the alternative
pathway over the sympathetic system projects.
A second objective parameter is the hormone prolactin. Only real orgasm, not
sexual arousal without orgasm, is clearly noticeable in blood samples. It stays high
up to 60 min after orgasm. It is, however, difficult to use in scientific research
although orgasm studies are based on it [71].
It is unmistakable that alternative pathways for vaginal orgasm are presented in
the literature. However, since definition of orgasm is difficult to give,

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6.4 G-spot: Clitoral and Vaginal Orgasm 161

psychophysiological parameters are hard to establish, and neuroanatomical


connections are falsely described, all criteria hardly contribute to underpin the
description of vaginal orgasm.

6.5 Eunuchs: Castration of Man

The term castration is of unknown origin. The most accepted idea is that it comes
from Sanskrit word castram, meaning knife and casati for cuts, or from the Indo-
European kastrom, which in its declension signifies cutoff, taken over in Latin as
castrum: an army camp not connected anymore to the main force. An alternative
explanation is that castrare comes from the castor, the beaver, which hides its
testes inside the body, and its scrotal appearance is due to large glands for territory
marking. The gland secretes castoreum that had medicinal value in early times as a
treatment for female infertility or for erectile dysfunction in man. The fairy tale
says that the beaver, if hunted, would bite off his testes to save his life [72].
However, medieval people were misled and what they conquered were the glands
and not the beaver’s testes. By the way, ‘‘Castoreum is still being used in the
perfume industry as well as in the food industry as a flavoring agent (FDA
approved). Extracts of castoreum are also used to flavor cigarettes’’ [72].
In the earliest food-producing economies of the Middle East and West, the
discovery ‘‘that wild bull could be changed by castration in a docile ox certainly
made one of the greatest contributions to civilization’’ [73]. The same holds for
other animals such as wild horses that were castrated by Scythians and Sarmatians.
Castration of animals is still kept in our society (e.g., cat, pig, sheep). The genesis
of large landed properties created slavery. To make slaves easier to handle and less
perilous, they were castrated and/or branded. Young men were castrated to satisfy
the libido of females, without the risk on pregnancy. In ‘‘Rome, where the cas-
tration of slaves, who were the lovers of some excellent matronae, it was con-
sidered as the surest ‘contraceptive’’’ [73]. Although forbidden by several
emperors and the Catholic Church, the habit stayed present, also during the fol-
lowing ages and disappeared in the fifteenth and beginning of the sixteenth cen-
tury. Human castration came back due to the need of the Popes for ‘‘treble voices’’
for the choirs of the Sistine Chapel. ‘‘Approximate 5,000 boys were castrated
annually for the purpose of singing in choirs’’ [81]. These so-called sopranists
were famous singers, also on stage. It was ended by the verdict of Pope Pius X
(1835–1914) on castration of boys for the choirs [73].
In the West, three ways of castration were in use producing eunuchs:
destruction of the testes of young boys by hand, cutting the scrotum and removing
the testes, or cutting of penis and scrotum with testis. Descriptions were already
available from Mesopotamia, from Greece, and in Latin from the Roman Empire,
before Christ and after Christ.
The crushing of testes was done in a warm bath. Seat children, still infant, and
‘‘soften the testes, than press and pulp the testicles with the fingers until they are

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162 6 Sexual Organs and Society

dispelled and vanish and can no more felt to the touch’’ [73]. These castrated
youngsters were called thlibiae. The other method was carried out by a cut into the
scrotum and removing the testes, leaving the penis in tact. Care was taken to peel
the testis from its surrounding membrane and not to disturb the blood vessels that
are not related to the testes. For these, spadones in Rome in the first century AD
hold ‘‘the sexual pleasure [of the Roman matronae] reaches the top if the testicles
of their slaves be entrusted to the physicians when they are already ripe and burn
with youth and when their pubes are already blackening’’ [73]. The third method
was to amputate penis and scrotum with testes. By pulling the pudenda and tightly
tied at its base, below the tie all was cut of with a sharp knife. These are castrati,
and this method was also applied on China’s eunuchs.
It is a pity that science started to study eunuchs only late. The word eunuch is
related to the Greek word eunoukhos (eune is bed and ekhein to keep) meaning
bed keeper or keeper of the harem [81].
Around 1640, nearly 70,000 eunuchs lived in China, and at the end of the
Chinese empire in 1912, still a considerable amount of eunuchs were present,
because 1,490 were dismissed in 1923 by the abdicated emperor. (normally, the
emperor had 2,000 eunuchs and princes nearly 30). The last eunuch in China died
in 1996 [81]. Eunuchs in China took considerable control of the emperor’s power,
due to their castration, with destructive consequences.
We owe to Wu and Gu [82], two Chinese urologists from the medical faculty of
the Being University, most information on the effects on the prostate. Still some
controversy exists [74]. Wu and Gu studied 26 eunuchs, and the total studied in
literature is 85 [74], including those of the Ottoman empire. Age groups differ,
nearly no blood sampling has been done, and long-term follow-up is lacking.
Nevertheless, the consequent bodily changes found are as follows: enlargement of
the pituitary, skeletal changes, development of breasts (gynecomastia), and, in
most cases, disappearance of the prostate [74].
In wars, castration of caught enemies was not uncommon. ‘‘It is interesting to
recall that at the time of Mussolini’s invasion of Ethiopia his soldiers were terrified
of being taken prisoner since a threat had been made that, if poison gas were used
against them, the Ethiopians would retaliate by castrating all Italian prisoners’’ [75].
Scrotal herniae were fought against in Greek and Roman time by castration,
prescribed by Galenus, even epilepsy. In Christianity, several sects favored cas-
tration for religious purposes. In politics, opponents could be made powerless by
castration. The well-known history of Abèlard and Helouise showed that it was
used to punish those suspected of sexual offense or rape [73–76]. Castrates could
be used for sex, as docile servants, as guards of harems, and as protectors of
princes and princesses. The variety of purposes to castrate man is overwhelming,
but all are related to man’s virility, or sex-related, or religious-related, or con-
nected to loose manhood for political or war reasons: all related to power.
A special subject is the castration of sex offenders. In 1892, the first castration
was carried out in Switzerland, and it became regular and legally from 1906 on in
Europe: Denmark (1929), Germany (1933), Norway (1934), Finland (1935),
Estonia (1937), Iceland (1938), and Sweden (1944). In several countries, castration

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6.5 Eunuchs: Castration of Man 163

was carried out, without legal support (The Netherlands, Switzerland, and
Greenland). Catholic countries and England do not have an attitude for castration
related to sex offenders. In Germany, between 1934 and 1944, around 2,800 men
were castrated, and in the same country, between 1955 and 1977, nearly 800 were
castrated. A rough estimate gives over 10,000 men, since the study of Heim and
Hursch [77] alone mentions 5,100 castrates found in the most important sex
research publications of Germany, Switzerland, Norway, and Denmark. ‘‘The fact
is that incarcerated sex offenders have a choice only between two evils: loss of
manliness or loss of freedom through long-term imprisonment. It is evident that
castration turns the clock back to medieval times, when amputation of the hands
was practiced as a means of curing thievery’’ [77]. Nevertheless, since ‘‘chemical’’
castration is possible now, the discussion is back again.
Modern castration can be done chemically or hormonally and of course still
surgically. The literature is large and politically filthy; therefore, a restriction is
made; the USA is chosen here. In Florida, but also California, enforced castration
is possible by law: Chaps. 97–184 of Florida’s law from 1997. This is not the place
to discuss civil rights nor American law in relation to Florida’s castration statute.
‘‘The new statute mandates court-ordered weekly injections of a sex-drive-
reducing hormone to qualified repeat sex offenders upon release from prison. It
may also be administered to first-time sex offenders’’ [78]. The used drug is
medroxyprogesterone acetate (MPA), also known under the name Depo-Provera.
‘‘MPA has been used successfully with only one type of sex offender, the para-
philiac, who demonstrates a pattern of sexual arousal, erection, and ejaculation that
is accompanied by a distinctive fantasy or its achievement’’ [78]. It does not work
in other types of sex offenders, especially not in those where the principal drive is
aggression. Medical control is prescribed by the law, and it is the court’s appointed
medical expert that makes the final decision.
What do we know on the effects of chemical or hormonal castration till now? A
meta-analysis of the 80 independent analyses on 22,000 sex offenders compared
the difference between treated and untreated offenders (30 of the analyses are from
North America). There is 37 % less recidive in treated, by all means, versus
untreated offenders (11.1 % recidive among treated and 17.5 % of the control
offenders). So treatment works, although less then wanted. However, the outcome
is surprising if one looks to the methods used: ‘‘Organic treatments (surgical
castration and hormonal medication) showed larger effects than psychosocial
interventions. However, this difference was partially confounded with methodo-
logical and offender variables. Among psychological programs, cognitive-behav-
ioral approaches revealed the most robust effect. Nonbehavioral treatments did not
demonstrate a significant impact’’ [79]. The same authors, with some more care,
said later: ‘‘As for now, our results indicate that cognitive-behavioral treatment is
promising. Also, hormonal medication seems to improve outcomes’’ [80]. Could it
be that cognitive-behavioral treatment is good replacement of ‘‘chemical’’ cas-
tration? But, the next citation shows that although one wants to solve the problem,
the quality of the scientific research shows serious weaknesses.

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164 6 Sexual Organs and Society

‘‘Treatment for sexual offenders is a very important topic of criminal policy.


Media reports on serious cases of sexually motivated murder, rape, and child abuse
have made people particularly concerned about this area of crime. In various
countries, policymakers have reacted by increasing measures of both punishment
and treatment. Because most incarcerated sexual offenders return to the commu-
nity, effective treatment is a cornerstone for preventing future offenses. However,
the empirical basis of sex offender treatment is less solid than such a cornerstone
should be. Although recent overviews suggest a moderately positive effect,
methodological problems, inconsistent results, and a lack of high quality studies
question how far we know what works for sex offenders’’ [79]. One should urge,
therefore, our politicians to open the possibilities to do quality research on treat-
ment of sex offenders, irrespective of the outcome.
Neuroscience came up with a hypothesis on sexual behavior in man and
mammals [83]. Any genital response is the outcome of a balance between a sexual
excitation and a sexual inhibitory system in humans. While the excitation system is
straight forward, the inhibitory system is rather diffusely spread over the nervous
system. Nevertheless, stress and depression are activators of the inhibitory system,
while sexual stimuli are directly arousing the sexual excitation system. Although
the system is present in all humans, it is characterized by a strong individual
variance.
‘‘There is normally a basal level of inhibition that has been called inhibitory
tone. This is clearly evident peripherally in the inhibitory tone maintaining flac-
cidity of the penis and examples of centrally acting inhibited tone have been
suggested [83].’’ Thus, in non-sexual situations, the inhibition dominates.
The testicle male hormones (androgens, testosterone) are responsible for the
maintenance of male sexual behavior (it disappears in castrates), so the basic
working of the sexual system needs hormones. Superposed on it is the inhibitory
system that uses b-endorphin (an opioid-like substance) and can, dependent on the
place it is injected in experimental animals, suppress copulatory behavior or
the precopulatory actions. b-endorphin is produced in the gate-keeper nucleus of
the hypothalamus [84] (called the arcuate nucleus), i.e., the nucleus that deter-
mines the central nervous system outflow to the pituitary hormone centers. It also
has widespread contacts through the brain, especially the limbic (sexual) system.
Perhaps this research can led to the ‘‘sex-suppressing’’ pill for sex offenders.
Let us return to the spadones. Lack of testosterone, produced by the testicles,
induces decrease in libido and of sexual behavior (see above). How possible if the
matronae of Rome distinctively used spadones for their sexual pleasure. Research
in castrated man showed: ‘‘During visual sexual stimulation, 4 of the 16 patients
(25 %) achieved a functional erection with a concomitant increase in penile
diameter of greater than 10 mm on both gauges. In each patient the erection was
maintained during the period of the visual sexual stimulation. All 4 patients
achieving erection had undergone surgical castration. No man treated with
chemical castration achieved a functional erection’’ [85]. Thus, chemical castra-
tion is different from spadone castration. Moreover, did the spadones themselves
still enjoy sex, since a rather extensive literature is present on whether penile

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6.5 Eunuchs: Castration of Man 165

nerves still function equally or not in the absence of testosterone. Let us place two
opinions opposite to each other:
1. ‘‘The results indicate that, in adult animals, testicular androgen has no role in
maintaining genital sensory fields, sensory thresholds, initiation of neural
responses, conduction velocity, or amount of neural activity evoked by a par-
ticular stimulus; therefore, peripheral sensory effects of castration seem not to
be the cause of the decline of sexual behavior following gonadectomy’’ [86].
This is a thorough electrophysiological study carried out in castrated and non-
castrated cats. Therefore, one should assume that erectile information is normal.
2. ‘‘In summary, androgens play a pivotal role in maintaining erectile tissue
architecture, and erectile physiology by modulating penile neural function and
structural integrity of the smooth muscle, endothelium, and connective tissue
matrix, as well as metabolic and signaling pathways’’ [87]. This review article
includes animal and human results. It indicates that neural function is disturbed.
Testosterone effects are seemingly not unequivocal, called ‘‘an unresolved
enigma’’ [88]. Problems of demonstrating a clear-cut relation between testosterone
and penile function are in the different levels of testosterone to have effect in
young and elderly men, the underestimating of the effect of testosterone on the
structure of penile tissues, the effect of Viagra (a phosphodiesterase-5 inhibitor) in
combination with testosterone application, and ‘‘Erectile potency is physiologi-
cally a complex interaction of vascular, neural, metabolic, endocrine and, last but
not least, psychological factors’’ [89].

6.6 Phantoms of the External Genitalia

Phantom limbs, thinking and feeling your extremity is still present, although
amputated, are well known. Itch of the toes or fingers is frequently reported in
phantom limbs. It mostly concerns the distal parts of the limb. The same holds for
phantom images of amputated female breasts, where breast pain can be noticed.
Less known and less reported in literature are the phantoms of the penis. Ampu-
tations are a therapy for penile cancer.
Mathilde Boon, a Dutch pathologist specialized in cytology, studied HPV
infections. Infected females transmit the virus to their males [90], sexual contact
infection is 85 %, and the penis is the organ that will be infected first. (Note that
the male is also a large vector [90].) In Western countries, this infection in males
does not induce penile cancer. However, it does in some developing countries:
Haiti and Uganda among the best known.
The Hindu population in Bali does not practice circumcision, as their Muslim
countrymen do in Indonesia, but also a high percentage of the male, mature Hindu
population on Bali, has more or less phimosis. It reaches nearly 50 %. The male
genital carcinomas are related to HPV for 75 % in Bali. Causes indicated by Boon
are as follows: no surgical treatment for phimosis, together with poor hygienic

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166 6 Sexual Organs and Society

circumstances and an early sexarche. The Balinese discovery and treatment for
penile cancer is late, and in several cases, the penile carcinoma has grown too far,
so only amputation is what remains [90].
The reports on phantoms of the penis after amputation mainly date from
Western publications [91]. ‘‘A man aged 70 years who began to have intermittent
erections two years after amputation of his penis. Prior to the amputation he had
been impotent and lacked desire. The erection was not provoked by sexual
phantasies. The phantom was so natural the subject was led to check for its
presence visually. This state was brought to an end four years later when the
subject suffered a gunshot wound of the spine productive of a paraplegia with loss
of sensation for pain and temperature below the level of the navel’’ [91]. However,
erotic stimuli can provoke the phantom [91] and the presence of such a phantom
can have a long duration (in one case, 20 years is reported [91]). It is now well
established that the phantom is a cortical phenomenon within the parietal lobes of
the brain and is a somatosensory creation of these lobes. The phantom of the penis
manifests itself under altered physiological conditions (e.g., arousal), which does
not hold in the same way for limb phantoms. ‘‘The occurrence of a phantom only
of the erect state may reflect a relatively greater sensory experience in that state,
resulting in a more abundant neural connectivity in the parietal cortex’’ [91].
Phantoms of the testis also exist. After the removal of testes (called orchiec-
tomy) for testis cancer, uni- or bilaterally, patients had the experience of the
presence of the removed testis for the correct size, or swollen, and pain in the
phantoms was perceived. Already described in 1844, the testis phantom is still
seldom reported. The general noticing of phantom testis can range from 22 to
53 % of the patients [91] and phantom testis pain in 25 % of the cases.
A side step toward brachial plexus avulsions is needed now to explain some of
the ideas on cortical reorganization. Brachial plexus avulsions mainly occur in
male motor and moped drivers that have a traffic accident. Propelled toward the
ground, the arm nerves can be pulled out of the spinal cord together with their
motoneurons. There is no connection anymore between the spinal cord and the arm
muscles, resulting in a lamed arm. Surgically, one can connect the intercostal
nerves that still have their motoneurons, with arm muscles, e.g., the biceps.
Amazingly, the patient can steer his biceps muscle with the respiratory intercostal
nerves. So the original motoneurons for the biceps in the spinal cord are absent or
disconnected. The respiratory motoneurons in the spinal cord are reconnected to
biceps muscle and produce contraction of the biceps (giving flexion of the elbow).
How is this possible?
Martijn Malessy and Raph Thomeer, Dutch neurosurgeons at the Leiden
Academic Medical Center, which is also the reference center for brachial plexus
avulsions in the Netherlands, studied these intercostal to musculocutaneous nerve
transfers (musculocutaneous nerve is the innervating nerve of the biceps). Thus,
the intercostal nerves are connected to the disconnected rest of the biceps nerve to
guide the outgrowing axons of the intercostal nerves to the right places in the
biceps muscle. ‘‘It was found that respiratory activity could initially be present
without any clinical contraction of the muscle, often to the patients’ surprise’’ [92].

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6.6 Phantoms of the External Genitalia 167

Thus, electrophysiology showed that the respiratory motoneurons still sent the
respiratory signal to the biceps muscle over the newly established connection
without initially initiating muscle contraction. ‘‘Starting with no response to either
flexion or respiratory efforts, the next level was a contraction (of the muscle)
following respiratory maneuvers only. Finally, patients could induce biceps con-
traction not only by respiratory maneuvers, but also by voluntary flexion attempts.
In fact, patients could flex the elbow while continuing to breath’’ [92].
Further research concentrated on the changes present in the central nervous
system. Two hypotheses were brought forward: The cortical hypothesis states that
the cortical neurons for biceps flexion grow out with a new axon that contact the
cortical neurons for respiration and thus steer the cortical respiration neurons. The
other, spinal cord hypothesis, claims that at the spinal cord level of the respiratory
motoneurons outgrowth of the biceps, cortical neurons occur; thus, steering with
biceps cortical neurons can be performed on spinal respiratory motoneurons.
Normally, the cortical biceps neurons have connections with several areas of the
spinal cord, and presumably, these corticospinal biceps connections toward the
respiratory motoneurons already exist.
Now, let us return to the phantom phenomenon. One should know that the
axons for motor steering are also accompanied by the sensory axons that bring
toward the cortex the sensibility of the biceps and the muscles for respiration. So
the system described above is in the reverse mode, present for the sensory
information (this is an oversimplification). Phantoms thus are the result of changes
in the sensory networks of the cortex or are the consequence of overlapping
sensibility networks in the spinal cord that trick the cortex. Now, keep in mind
what we described earlier for the patient’s case above: ‘‘This state was brought to
an end four years later when the subject suffered a gunshot wound of the spine
productive of a paraplegia with loss of sensation for pain and temperature below
the level of the navel’’ [91]. Although it is only one case, it still is suggestive for
the spinal cord networks that trick the sensory cortex.
The reverse situation is described for female orgasm by Horvat et al. from the
Clinical Hospital Sveti Duh in Croatia. A 49-year-old patient had uncontrollable
spontaneous orgasms for already 8 months. The cause finally determined was an
epileptic focus in the right frontotemporal area. An aneurysm was found in the
siphon of the left internal carotid artery [93]. Here seemingly, pressure on a
cortical area due to an enlargement of a large blood vessel induced the orgasms
and thus a cortical cause.
A third possibility is a peripheral overlap in sensory information toward the
brain, as is presumably the case in the foot orgasm syndrome [94]. A female
patient complained of spontaneous orgasms in her left foot. These orgasms
occurred in the absence of sexual desire and moved from her left foot, over her calf
toward the vagina, and could be induced by electric stimulation or manual pressure
at metatarsophalangeal joint II, III, and IV. Orgasms as a result of intercourse were
also noticed in the left foot. The explanation is in the sensibility passing over the
first sacral spinal ganglion. The nerve innervating the clitoris, the pudendal nerve,
and the medial plantar nerve for the sensibility of the feet both use the S1 ganglion.

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168 6 Sexual Organs and Society

The patient had damage of specific sensory axons of the foot. For the brain, the
area of the sensory information coming from S1 became purely sexual. After slow
and time-consuming regeneration of the sensory axons of the foot, S1 contained
again foot sensory information; send toward the brain, it was noticed in the brain
as sexual information [94]. Phantom orgasms after foot amputation originating in
the amputated foot during intercourse are reported in the literature [94]. Moreover,
in an anonymous message placed on the Internet, voluntary inducing orgasm by
one’s feet is reported [94].
Since the cortical area for the foot is next to the cortical area of the genitals,
cross-activation between the areas is well possible. In limb amputations, the cortex
originally used for foot information is use-invaded by the genital cortical adjacent
area. Literature even explains that this cross-activation between foot and genitalia
explains foot fetishism. Recently, this cross-activation between both areas is used
to explain foot-binding in medieval China. Chinese men viewed foot-binding as a
mean for better sexual intercourse, since vaginas were stronger muscled. Chinese
men thought that ‘‘walking on their bound feet caused women to develop more
‘voluptuous and sensitive’ genitals’’ [94A]. It led the author to hypothesize on
foot-binding and cross-activation of cortical areas. Here, we take over a large part
of the hypothesis: ‘‘It is known that the practice of foot-binding in Chinese women
prevented their feet from maturing normally. Hence, as time passed although a
girl’s brain would develop into adulthood, her feet would remain small and
become atrophic. We hypothesize that this resulted in under-utilisation of the foot
areas of the somatosensory and motor cortices, which in turn lead to cross-acti-
vation between the redundant foot cortex and the adjacent genital areas in these
women’s brains. Indeed, as the brains of these girls developed, what was once
destined to be foot cortex could have been entirely reassigned to her vagina.
Compared to women with normal feet, this caused women with bound feet to
devote a disproportionately larger area of the sensory and motor cortices of their
brains to their genitalia and pelvic floor musculature. We postulate that this had the
direct consequence of making these women more sensitive, responsive and plea-
surable lovers’’ [94A].
The more recent phantom studies make a sharp and consequent difference
between sexual organ phantom sensation and sexual organ phantom pain. Both,
sensation and pain, are of course somatosensory phenomena. Older literature does
not make such a clear distinction. Alternative solutions or hypothesis comes from
recent breast phantoms [95], because they keep a sharp eye on the differentiation
between sensation and pain, and on research design and assessment methods.
Moreover, the large amount of breast operations makes it possible to do statistics,
which is difficult for the sparse reported penile and testis phantoms. Becoming
aware of a phantom breast was present in ±20 % of the patients that underwent
mastectomy. (Range in the two most recent articles was 20–22.5 %, while older
literature reported 33.5 %, and the difference presumably depends on the different
older surgical techniques in which consequently the pectoralis major muscle was
also removed.) Old ideas as: the younger the mastectomy, the more chance on a
breast phantom, the fading away of the phantom after longer survival after the

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6.6 Phantoms of the External Genitalia 169

operation, and increase in pain noticing after longer survival times are all con-
tradicted in the recent literature [95], rather a reduction in pain over time is found.
However, the tumor growing through all structures of the breast (invading breast
tumors) compared to tumors that follow the breast ducts and do not penetrate the
walls of the ducts (ductal breast carcinomas) showed that invading breast tumors
produce more often breast phantoms. The explanation is based on the destruction
of innervation by invading tumors of the breast (producing pain) versus ductal
carcinomas (with relatively no pain) that hardly interfere with peripheral breast
innervation [95]. The explanation advocated is that we contain in our brains an
image of our whole body or genetically [95] or produced by the dorsal root ganglia
[96]. By the sensations of our body, sent to our brains, we adapt the body map.
After the removal of the organ (thus destruction of sensory information), the
adaptation disappears but not the part of the map in our brain representing that
organ [97]. As a consequence, we think the organ still to be present. The stronger
the perception of destruction: normal sensibility in ductal breast carcinomas versus
sensibility and pain present in invading breast carcinomas (the last one using
different pathways toward different brainstem target areas), the more chance of
phantom occurrence. Here seemingly, we have the interaction of spinal cord
networks (sensibility of the breast goes over the spinal cord) and cortical inter-
action. Indeed, the large group of sensory neurons called the thalamus that also
contains a representative map of the body and is the intermediate between spinal
cord information and the cortex is ‘‘phantom’’ active as the large sensory system
(medial lemniscus) does that brings the information toward the thalamus [97].
Why the phantom occurs in 25 % of the cases and stays absent in the other
75 % is an enigma.
What remains are the phantom studies on transsexuals. After a gender operation,
male to female or female to male, phantoms of the external genitals are present. The
above explanation that a map of the body is genetically present led to the conclusion
that male-to-female transsexuals should have genetically the female map, and
therefore, penile phantoms should be less encountered in this type of transsexuals.
This is statistically not proven. Both in non-transsexual men and in male-to-female
transsexuals, penile phantom perceiving is not significantly different [98].
As a last remark, prepuce phantoms are not reported in the literature, and
clitoral phantom data are hard to find, which is a surprise with over 100 million
circumcised women on the world.

6.7 Plastic Surgery of Sexual Organs

Two different approaches are found in the literature. The first concerns the res-
toration of circumcised sexual areas, especially the clitoris. The other is the plastic
surgery for esthetical adapting the vulva areas. Here, we do not discuss ethical
matters concerning these plastic surgical operations, but concentrate on the ana-
tomical and clinical side of the approach.

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170 6 Sexual Organs and Society

There are view institutions [99] that direct their research toward the restoration
of the circumcised clitoris. In 453 cases, French surgeons tried to repair the
damage. Their success rate is 75 %. By cutting the clitoral ligament that suspends
the clitoris (remainder), it can be brought forward and fixed in a more prone
situation. Scar tissue of course is removed. It is a 30-min operation, and the
operation works in the WHO types II and III (see above). Within 6 weeks, the
sensibility of the clitoris is returned [99].
The other side of the medallion is the wish of mainly Western women for
adaption of the external appearance of the vulva, called labiaplasty surgery, for
esthetic reasons, pain or to enhance sexual satisfaction (the last motive is debated).
Although there is a large variety in vulva appearances, still a generally accepted
esthetic look is seemingly favored. (Playboy or Penthouse is brought to the plastic
surgeon). For example, labia minora that stretches out of the labia majora is
considered unattractive, but also can be painful. The plastic surgeon diminishes or
even removes the labia minora. Hoodectomy, exposing the clitoris or liposuction
of the labia majora, can be performed. Since done under anesthetics and in a well-
organized clinic in the West, complications are hardly published. Nevertheless, the
American College of Obstetricians and Gynecologists published a list of risks of
the procedure: infection, bleeding, decreased feeling, pain, sexual dysfunction to
name a few [100]. Transsexual operations already showed that external sexual
organs are ‘‘easily’’ manipulated surgically. The close interrelation of male and
female external genitalia by a joint unspecific developmental stage continuing later
into a gender-specific developmental stage is the base for this. This surgical and
anatomical knowledge is applied in labiaplasty.
At the end of this chapter, a conclusion is difficult to draw: Humanity deals
bizarre with their sexual organs. While in the animal kingdom, we do not
encounter this manipulation of sexual organs, and humans do want to manage
them. Anxieties (koro and spermatorrhoea) and power (circumcision, castration,
and mutilation) play an important role. But castration can also be used to get
power (Eunuchs). In these modern times, it is remarkable that knowledge is
lacking (prepuce, phantoms, and G-spot) still supporting uncertainty concerning
sexual organs, presumably leading to extra attention for the esthetics of the sexual
organs. On the other hand, research contributed to sound clinical methods for the
restoration of mutilations or to help transsexuals.

Literature

Literature has been grouped in reference lists of several chapters in those cases where
arguments are difficult to entangle or published over several articles or books. In cases of
citation the article or book involved is indicated by the reference number together with a
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Chapter 7
Anatomy of the Pelvic Wall

Formerly everything that belonged to the human body, especially to the area of the sexual
organs, was terra incognita for the layman, and was reserved by the professional medical
man to himself. Nowadays a new phenomenon has arisen, that the layman also learns to
take an interest in sanitary science and so on. And by this, inevitably also on subjects,
concerning which it was earlier not suitable to speak, namely on the construction and
function of the sexual organs. This undoubtedly supports public health, and the practise of
purity and chastity [1].

The pelvic wall includes the urogenital and pelvic diaphragm. The localization of
both structures in the bony pelvis and their interrelation are easily mistaken. Different
compartments can be discerned within the pelvic cavity due to connective blades.
Sphincters are included in the pelvic wall musculature, except the male urethral
sphincter. Inguinal hernias were common in previous ages. Their operation needed
surgical landmarks: Scarpa’s, Colles, and Buck’s fascias being even now unclear in
terminology and localization. These fascias are still important in modern surgery.

7.1 The Mature Pelvic Wall Muscles and Ligaments

The study of the pelvis is best tackled by first distinguishing two main aspects: the
wall and the pelvic contents. The wall contains bony components and muscles,
while the content consists exclusively of viscera wrapped in fasciae. The first three
chapters extensively discussed the bony parts of the pelvis, so we can restrict
ourselves in this chapter to those ligaments and muscles of the pelvic floor which
contribute to the wall.

7.1.1 The Foramina of the Pelvis

At the back of the bony pelvis are two important ligaments. They connect the
edges of the bony pelvis to the os sacrum. The spina of the os ischium is the target
of the sacro-spinal ligament, while its tuber is the origin of the sacro-tuberal

E. Marani and W. F.R.M. Koch, The Pelvis, 177


DOI: 10.1007/978-3-642-40006-3_7,  Springer-Verlag Berlin Heidelberg 2014

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178 7 Anatomy of the Pelvic Wall

Lig.inguinale

Linea terminalis

Fig. 7.1 Inside view of half a pelvis. Left In brown are the sacrospinal (upper) and sacrotuberal
ligaments, constituting two spaces: the greater sciatic foramen (upper space) and the lesser sciatic
foramen (lower space). Right The arrows indicate the obturator foramen (left) and the subdivision
of greater sciatic foramen in a supraperiform foramen, an infraperiform foramen and the lesser
sciatic foramen (right side). The dotted line is the line of adherens of the levator ani muscle. The
inguinal ligament is indicated in the right-hand figure, at its extreme left  E. Marani

ligament. These two ligaments are like the blades of open scissors. The upper
blade (sacrospinale) is placed more nearer the bony pelvis, the other blade more to
the outside (sacrotuberale). Consequently, two spaces arise: one is above the
sacrospinal ligament, with a bony arcade above it made by the bony pelvis, which
is called the great sciatic foramen, and the triangle-like opening between the
blades of the scissors is named the lesser sciatic foramen (see Fig. 7.1) [2–5].
A natural foramen exists at the anterior side of the pelvis, totally surrounded by
bony structures (os ischii and pubis). This foramen is largely covered with a
connective plate called obturator membrane; however, at its upper side, there is
one small gap: the obturator canal. At the front, another ligament travels from the
os ilium (the spina iliaca anterior superior) to the os pubis near the symphysis: the
inguinal ligament. Through this opening, between os pubis and this ligament,
passes bloodvessels, a nerve, and muscles, to the front side of the leg.
The inside of the bony pelvis contains a bony edge that divides the pelvis in the
deep (or lesser) and the upper pelvis. It is called the linea terminalis (formerly
the linea innominata). This line continues on the upper side of the sacrum into the
promontorium, the buldging edge of the last intervertebral disc (Fig. 7.1).
The border between lesser and upper pelvis is not the line of attachment of the
pelvic diaphragm, a mistaken belief. The pelvic diaphragm is like pants that have
slipped-down, still hanging on the sacrospinal ligament, at the rear stuck to the
sacrum, and on the anterior side attached to muscles covering the obturator
membrane and the os ischii. The border passes below the obturator canal, leaving
it free for structures emerging from inside the pelvis (Fig. 7.1).

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7.1 The Mature Pelvic Wall Muscles and Ligaments 179

Fig. 7.2 The ‘‘knife’’ that


cuts the pelvic floor funnel,
producing the hiatus
 E. Marani

These relationships are of the utmost importance: one can leave the pelvis over
the sacro-spinal ligament, through the greater sciatic foramen, without penetrating
the pelvic floor. You will in this way reach the gluteal or buttock area. Structures
can do the same through the obturator canal, to reach the adductors of the leg. So,
there are highways leaving the pelvis, which do not pass through the pelvic dia-
phragm. Blood vessels and nerves use these passages. The highway through the
greater sciatic foramen is divided by the periform muscle into a supra- and an
infraperiform foramen, forcing structures to the upper gluteal or the lower gluteal
area and leg, respectively (Fig. 7.1).
Another way of visualizing the relationship is to imagine a funnel, instead of
the pelvic diaphragm, narrowed by the funnel opening, being the anus (Fig. 7.2).
Now, we place this funnel into the bony pelvic inner space, tied with its upper
wide edge to the sacrospinal ligament (Fig. 7.3). If you place a household funnel in
a drinking glass, you will notice that there is space between the glass wall and the
funnel wall. This space is outside the funnel (our pelvic diaphragm), but inside of
the glass wall (our bony pelvis), and is called the ischiorectal fossa. This space is
filled with fat, but the structures that have to reach the outer genitals and the pelvic
floor, nerves, and bloodvessels leave the pelvis by a special highway. They go over
the sacrospinal ligament, which means through the greater sciatic foramen, pars
infraperiform, through the lesser sciatic foramen, which is passing under the
sacrospinal ligament, but above the sacrotuberal ligament into this fossa. In this
way, one reaches the outside of the pelvic floor, which consists mainly of muscles,
which can be supplied from the outside.

7.1.2 The Urogenital Diaphragm

A horizontal section through the bony pelvis shows that the bony pelvis is not
circular. The bony pubic area forms, in such a section, a nearly straight line. The
bones of both ossis ischii that fuse near the symphysis with the ossis pubi

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180 7 Anatomy of the Pelvic Wall

Fig. 7.3 The pelvic floor funnel placed into the bony pelvis, adhered to the sacro-spinal
ligament. Note the obturator foramen is just left free on both sides of the symphysis  E. Marani

constitute an arc filled in by a plate called the urogenital diaphragm. If we consider


this plate a butcher’s knife, then it cuts off a part of our pelvic diaphragmatic
funnel. Stereometry can predict that if you section a cone in such a way that the cut
surface is a semi-circle, the same occurs with our pelvic funnel (Fig. 7.2) [2–5]
This semicircular hole at the upper side of our funnel is the hiatus. The margin
of this semicircle is tightly attached to the urogenital diaphragm (Fig. 7.3).
Let us look into the consequences (Fig. 7.4). There is a part of this urogenital
diaphragm that is bordered by the contents of the pelvis. However, since the
diaphragm is larger than the hiatus, it contains also a part that is adjacent to
the fossa ischiorectalis. The nerves and bloodvessels that turn around the funnel to
the ventral side and innervate the pelvic diaphragmatic muscles will meet the
urogenital diaphragm and have to penetrate or dive below the diaphragm to reach
the external genitals (Fig. 7.4).

7.1.3 The Levator Ani Muscle

Now that we have attached the pelvic diaphragm to the bony pelvis, we can look
inside the funnel (Fig. 7.5). Looking from outside, it forms a circle, with the anus
in the middle of its opening. If we divide the circle by a cross into four identical

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7.1 The Mature Pelvic Wall Muscles and Ligaments 181

Fig. 7.4 Placement of the urogenital diaphragm over the hiatus. Spaces are present for the dorsal
vein of the penis (or clitoris), the urethra, and in women the vagina. Insert: the sphincters of
urethra and vagina, in relation to the transverse deep perineal muscle  E. Marani

parts, then we have to recall that the body is bilaterally symmetric: Thus, the left
and right anterior quadrants are equal like the posterior ones [2–5].
The anterior ones are called the levator ani muscles, while the posterior ones are
the coccygeal muscles. This last muscle lies between the spina (remember:
attachment for the sacrospinal ligament) and the end of the sacrum and coccygeal
vertebrae. Formerly, its function was to wag the tail, but since man does not have a
tail anymore, its only function is to add to the perineal shrug. The term levator ani
muscle is correct: The muscle is thought to be built up from several muscles, but
embryology showed this to be false (see Chap. 8, Fig. 7.6).
One has to realize that each of these quadrants is separately innervated. Each of
the halves, but also each of the quadrants, can be functionally distinct.
The midline is constructed of ligaments, which prevent extrusion (prolapse) of
the anus. In young animals, for example, kittens, strong pressure on the abdomen
will overcome the tensile strength of these not-yet-fully-developed ligaments. The
consequence can be anal prolapse. One ligament connects the anus to the end of
the sacrum and coccygeal vertebrae: the anococcygeal ligament. The other liga-
ment is far more interesting: It connects the hiatal edge to the anus. The perineum,

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182 7 Anatomy of the Pelvic Wall

Fig. 7.5 View into the inside of the pelvis, showing the division of the pelvic floor into four parts
 E. Marani

Fig. 7.6 View into the inside of the pelvis, showing the subdivision of the levator ani muscle and
the perineal ‘‘knot’’ ligament (1), together with the anococcygeal ligament (2) for the suspension
of the anus  E. Marani

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7.1 The Mature Pelvic Wall Muscles and Ligaments 183

lying between the vulva and the anus, is related to this ligament, the perineal knot.
Stonecutters thus divided this ligament if they made a midline incision (Fig. 7.6).
During delivery of an infant, this ligament may be torn along a natural line of
weakness, toward the anus. Injury to the anus during delivery is one cause of anal
incontinence in old age.
The anus, consequently, is fixed by two cables, which will resist overextension
of the pelvic diaphragm if pressure is brought upon the pelvic diaphragm during
defecation. Indeed, belly strain can produce huge pressures, compared to other
pressures in the human body. The anococcygeal ligament is the attachment for
‘‘two muscles’’ of the pelvic diaphragm: Both the puborectal and the iliococcygeal
muscle (subparts of the levator ani muscle) attach to this ligament (Fig. 7.6). The
whole levator ani muscle contributes to anal continence, although the subpart
called puborectal muscle is the one usually discussed in the literature.

7.1.4 The Corpus Intrapelvinum

Our pelvic funnel is divided into two stories by a ceiling, the point of view of
course being from the lower story (Fig. 7.7). However in women, the ceiling
contains three large openings. Parts of the ceiling that contact these three structures
are consolidated by ligamentous structures. Ligaments are present to help to lift,
from anterior to posterior, the base of the bladder, the cervix, and the rectum.
These attachments from the pelvic wall to the organs are variously named. The one
to the bladder is called the paracysticum and the one to the cervix the paracolpium,
which extends to the uterus with connective tissue and fat (parametrium), and the
one to the rectum is termed the paraproctium (Fig. 7.7) [2, 5].
All structures that pass from posterior to anterior, (for example, the obturator
artery, vein, and nerve, which penetrate the obturator canal to pass into the leg
adductors), must first descend into the funnel. Reaching the bottom, they must climb
again. Therefore, all these structures use the floor of the second story to reach the
anterior side, or to reach the pelvic organs (Fig. 7.8). In between vagina and urethra,
this ceiling lowers with solid connective tissue, ending with a strong connection
between urethra and vagina (Fig. 7.9). This explains why prolapse or displacement
of the vagina will involve the urethra and can result in urinary incontinence.
Rectum and vagina are separated by a recessus filled with solid connective
tissue containing fat. There is a further space between the urethra and the os pubis,
named the cavum Retzii (Fig. 7.9).

7.1.5 Again the Urogenital Diaphragm

The urethra and vagina have to pass through the urogenital diaphragm inside the
hiatal arch. The diaphragm possesses a series of openings: Directly under the

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184 7 Anatomy of the Pelvic Wall

Fig. 7.7 Suspension ligaments inside the pelvis. The intrapelvic body (corpus intrapelvinum)
contains ligamental enforcements for supporting bladder, cervix, and rectum. The inset shows the
pelvic funnel in a person’s standing position: red pelvic floor funnel, green suspension ligaments,
and blue the urogenital diaphragm  E. Marani

symphysis, passage is provided for the dorsal deep vein of the clitoris or penis
(Fig. 7.4). Below this opening, the urethra penetrates, and beneath this is the
opening for the vagina. In women, the sphincter urethra is incorporated into the
diaphragm. The openings for urethra and vagina are surrounded by the sphincter
vaginae, and both are covered by the bulbospongiose muscle. The free margin of
the urogenital diaphragm is covered with the transverse perineal muscles. In men,
the urethral sphincter is hidden around and between the prostate and penis.
Women, by frequent wiping of the urethral ostium, can induce irritation of the
urethral sphincter, which lies quite superficial [2–5].

7.1.6 Notions on Ligaments

The term ligament is usually synonymous with plica and implies a small, protu-
berant band of connective tissue. However, this definition can be confusing in the
present case. The ligamentum latum is not a small, but a large, area of very thin

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7.1 The Mature Pelvic Wall Muscles and Ligaments 185

Fig. 7.8 The suspension structures of bladder, cervix, and rectum constitute a natural floor for
those structures that have to pass from dorsal to ventral  E. Marani

Fig. 7.9 Midsagittal section


through the pelvis. All organs
are covered or partially
enwrapped in peritoneum
(blue) at their upper side.
Pelvic spaces are indicated by
their names. The connection
between urethra and vagina is
called a septum, due to its
strong connective tissue
intermingling their walls
 E. Marani

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186 7 Anatomy of the Pelvic Wall

connective tissue consisting of peritoneal sheets. The name ligamentum teres or


ligamentum properii now means a strong round rope of connective tissue. The
phrase ‘‘ligament of Poupart,’’ which is the inguinal ligament, indicates the lower
thickened line of connective fasciae of the anterior abdominal wall muscles. This
ligament creates a passage below it for the vessels, nerves, and muscles that will
reach the anterior part of the leg [6].

7.1.7 Suspension Operations

Incontinence in female is supposed to be caused by a deviation of the position of


the urethra. It is thought of minor significance whether or not this has been caused
by a displacement of orifice, urethra, or bladder.
By reconstructing the original spatial relationship between urethra and bladder,
one should restore continence. Various reconstructive operations are known, either
using a transvaginal or an intraabdominal approach. In all these, the urethral
position is lifted by artificial ligaments (even wires) or by ligaments taken from
other abdominal parts which are (re)placed internally. In the section concerning
the comparative anatomy of the pelvis (Chap. 5), the position of the pelvic bones
was discussed. Here, we face the positioning of viscera, which by themselves are
not fixed structures. The position of uterus, bladder, and bowels change constantly
depending on functional demands (see Chap. 5).
So, what are the ‘‘correct’’ positions for pelvic viscera? They cannot be defined
in terms of unchangeable localizations with respect to the pelvic bones [6].
Position here is a relative, and therefore dangerous, notion. Females with clearly
displaced urethras who are nevertheless continent are well known by the physi-
cian; while others, with only a slight distortion, and seemingly normal positions,
do have micturition problems.
In the female patient population, suspension operations are carried out if
micturation disturbances are present together with distortion of the position
between bladder neck and urethra. The positional relation between bladder neck
and urethra is thus the main criterion. Both lateral and rostrocaudal displacements
are incorporated in it. The definition seems to include precision.
When considering modern research, the striking point is how to maintain the
operative construct after replacing the urethra. Structures are sought that can
effectively anchor sutures to the pelvic wall. The natural development of scar
tissue should ligate the sutures. Moreover, these structures have to be near the
bladder neck in order to keep the (artificial) ligaments and the sutures short in
order that the ‘‘rope’’ cannot bend away.

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7.1 The Mature Pelvic Wall Muscles and Ligaments 187

7.1.8 More on Ligaments and Surgery in Stress Incontinence

If pelvic floor training fails, and incontinence persists, urologist and patient can
decide for a procedure to redress the urethral prolapse. Remember, prolapse of the
urethra is a question of the relative position of urethra and bladder. Prolapse of the
urethra through the urogenital diaphragm is called urethrocele. This can easily be
observed if pressure is brought upon the pelvis. However, if only the proximal
urethra is displaced, and the meatus is still in place, the urethra tends to rotate
downward and foreward. This is called rotatory descensus of the urethra and
causes so-called type II stress incontinence [7].
Normally, the urethra itself prevents leakage by its smooth muscle sphincter
and by the epithelia that cover the inner surface of the urethral lumen. The
sphincter can easily close, while the epithelium is thick. However, elderly women
have a low estrogen level, which reduces the thickness of the epithelium. This type
of incontinence is called an intrinsic urethral defect (causing so-called type III
incontinence). This type III incontinence can also have an iatrogenic cause, due to
scarring after (incontinence) surgery.
The surgical approach is different for various types of incontinence. Let us try
to understand what happens in the case of the rotatory descensus. The opening of
the urethra in women is part of the urogenital diaphragm, which communicates via
the hiatus with the contents of the pelvis. The position of the diaphragm is nearly
horizontal, due to the position of the bony pelvis (see Fig. 1.4). After a series of
deliveries, the urogenital diaphragm will be weakened. The consequence can be
that the diaphragm curves downward, no longer supporting the vagina and thus the
urethra. Elevation of the bladder neck is the operative technique of choice the
urethra will follow.
If intrinsic urethral failure is the cause, the urethral tube is held tightly to the
vagina by connective tissue. The tube lumen is thus artificially narrowed, and the
sphincter will be able again to close the urethra fully.

7.1.9 Abdominal Operations

In three procedures, the abdominal wall has to be opened to get access to the
vagina or bladder neck [7]:
1. Cystourethropexy [8] was developed in 1949. The surgeon opens the space
between urethra and the pubic bone (cavum Retzii). By placing three stiches in
the vaginal wall directly beneath the urethra and by suturing these wires to the
periosteum of the pubic bone, the vagina is lifted. The urethra positioned above
the vagina will also be elevated. Problems included chronic urine retention in up
to 12 % of the patients, due to the extreme angle between urethra and bladder
neck and osteitis in up to 10 % of patients. This operation is no longer used.

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188 7 Anatomy of the Pelvic Wall

2. Retropubic urethro-colpo suspension, [9] also called the Burch operation, is in


fact almost the same procedure. The sutures are placed more laterally and are
not adhered to the pubic bone, but to the ileopectinal ligament (ligament of
Cooper). The ileopectinal ligament is the enforced fascia of the iliopsoas muscle
which courses under the inguinal ligament toward the leg. This procedure can
also be performed by laparoscopy. The success rate is 80 % after 5 years. It was
the procedure of choice for most patients with stress incontinence.
3. The fascia sling operation [10] uses a part of the abdominal fascia or part of the
upper leg fascia (fascia m.tensor fascia lata), which can be brought as a sling
under the proximal urethra and bladder neck, by which elevation is produced.
The disadvantage in this case is urine retention if the sling is too tightly fastened.

7.1.10 Vaginal Operations

1. Urethrosuspension [7, 11] passes sutures through the vaginal wall. These
sutures traverse the cavum Retzii and are sutured into the abdominal inner wall.
After 5 years, only 40 % are still continent. Presumably, the wires tear through
the vaginal wall, and the urethra descends again.
2. Vaginal wall sling [12] uses the connection of the bladder neck to the pelvic
wall (paracysticum). The paracysticum adheres to the arcus tendineus faciae
pelvis, which is an enforced part of the fascia of the m. levator ani. The
paracysticum is transacted, and its ends are sutured to the inner abdominal wall.
The same wires are placed spirally through the paraurethral tissue. The results
are equal to the Burch approach, but postoperative morbidity is lower.
3. The arcus urethrosuspension [7] leaves the paracysticum unaltered, but rein-
forces it, since wires are extended to the arcus tendineus fasciae pelvis, through
the vaginal wall. Results are unknown, since the operation was only introduced
in 1995 (see Figs. 7.1 and 7.10).
4. Two other operations are carried out to overcome incontinence: periurethral
injections [13] with Teflon or collagen. The wall is thickened, and the inner
wall of the urethra is easier to keep closed. Results are very poor.
5. An artificial sphincter prosthesis [14] can be implanted, with a manchet around the
proximal urethra. The pump to handle the manchet is placed in the labium majus.
Frequently, revision of the system is needed, always by an abdominal operation.

It is apparent that all these techniques have significant failure rates, from 20 to
100 %. Nevertheless, the best (?) remains in use. The important question is why do
not we have a higher success rate? Urologists do their utmost to help their patients,
but what is missing? Could it be that we do not understand the interior of the pelvis?
Should one look for the relative positions among the organs, instead of the position of
one organ in relation to a seemingly fixed structure, like the urethra toward the
urogenital diaphragm? Fundamental anatomical research seems indicated, and if
possible ambulant registration of pelvic organ positions during the day and the night.

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7.2 The Relation of the Pelvic Wall Muscles and the Sphincters 189

Fig. 7.10 Right part View onto the ligamental connective tissue that originates from the
adherences of the pelvic floor muscles and the connective tissue present in the pelvis called arcus
tendineus fasciae pelvis. Left part Three different types of attachments of the ATFP in the pubic
bone area with permission and lower figure courtesy M.J. Pit. Abbreviations: ATFP Arcus tendineus
fasciae pelvi; ATLA Arcus tendineus levator ani; CO Canalis obturatorius; mla Levator ani muscle;
mOI Obturator internus muscle; and LPU Pubourethral ligament, MPC part of levator ani

7.2 The Relation of the Pelvic Wall Muscles


and the Sphincters

The sphincters of the pelvic diaphragm are clearly described in the literature,
although serious controversies exist. It is the striated muscle complex that covers
the urogenital diaphragm, which causes the problem.
The original idea was proposed by Popowsky already in 1899 [22]. The
primitive cloacal sphincter develops into an anal and a urogenital sphincter. The
last one further divides into a urethral and a vaginal one in females. The Popowsky
hypothesis says that all striatal muscles present on the urogenital diaphragm
originate from the striatal cloacal sphincter. The hypothesis resisted the wear and
tear of scientific time and even eloquent recent research could not deny the
attractiveness of the hypothesis, although a bilateral origin of the cloacal sphincter
and thus a bilateral origin of the striated diaphragm muscles are favored. In fact,
we hardly know the origin of these muscles. Therefore, the following description is
a rather theoretical one, but still based on the main embryological developments.
The descriptions are given for the male, except the Popowsky picture.

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190 7 Anatomy of the Pelvic Wall

Fig. 7.11 View on the


abdomen of an embryo.
Lower extremities start to
develop. The entrance of the
cloaca (not yet separated
outlet of the rectum and the
urethra) is encircled by the
cloacal muscles  E. Marani

Fig. 7.12 In order to


separate anus and urethral
outlet, a transverse division of
the cloacal muscles develops.
 E. Marani

Sphincters are occlusion muscles. They occlude a storage vessel. Occlusion is


not difficult, but releasing the contents of the storage vessel on time is more tricky.
Some distortions are thought to find their origin in maldevelopment of the
sphincters. This provides a further reason to look into the pelvic sphincters.
Research into the earliest development of the human pelvis is not easy, since in
most European and American institutions, only a restricted amount of reliable
human material is available, on which a description can be based. Most of the
organs are already well developed within the first 4–8 weeks of development,
often even before the woman knows that she is pregnant.
Cloacal muscles encircle the primitive cloaca like two segments of an orange
(Fig. 7.11).
These primitive muscles convert with each other in their central regions. The
cloacal space is divided into an urethral and anal sinus [23]. Each will respectively
develop into the terminae of the uropoetic and rectal systems. In between these
structures, the perineum develops (Fig. 7.12).
In addition to a transverse subdivision of the cloaca, an imaginary horizontal
division also occurs in the sphincter areas, in such a way that above and beneath
the horizontal division, two separate muscle areas, anterior and posterior by the
transverse division, develop. In total, four areas can be discerned. The upper
anterior quadrant contains the m. ischiocavernosus and m. bulbospongiosus/cav-
ernosus. The upper posterior quadrant forms the urethral sphincter. Both the

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7.2 The Relation of the Pelvic Wall Muscles and the Sphincters 191

Fig. 7.13 Beside a transverse subdivision, an anterior–posterior subdivision of the muscles


occurs, resulting in four muscle entities, separated by the transverse perinei muscles  E. Marani

anterior and posterior lower quadrants make the superficial and deep anal
sphincters. Both upper and lower halves are seperated by the m. transversus perinei
profundus and superficialis (Fig. 7.13).
With all this in mind, the innervation of the pelvic floor is easy to describe:
• All deep structures will be innervated from the inside by the pelvic nerve
(Figs. 7.14 and 7.15).
• All superficial muscle groups will be innervated from the outside by the
pudendal nerve (Figs. 7.14 and 7.15).
The literature describes a double innervation, from inside and outside, for the
puborectal part. Placed at the margin of deep to superficial structures, this part of
the m. levator ani could have a special position by its sphincteric and diaphrag-
matic function.
Mature pelvic structures are embedded in fibrous and fatty connective tissue.
These structures, described as suspension structures and supporting tissue, con-
tribute to keep the pelvic organs in place. Changes in the position of pelvic organs
lead to pelvic functional distortions. It is remarkable to see, in sections of fetal
pelvis, that the most important pelvic structures remain seperated from these fat
pillows and connective plates and are surrounded in the immature pelvis. Of
course, very loose tissue is present between organs and their fat pads and con-
nective plates in these early stages.

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192 7 Anatomy of the Pelvic Wall

Fig. 7.14 Anteriorly placed


muscles will be innervated by
the pudendal nerve, while
posteriorly placed structures
are innervated by the n.
pelvinus  E. Marani

Fig. 7.15 The development


of the pelvic floor muscles
occurs later and are
considered anterior or outer
structures, which will be
innervated by the pudendal
nerve  E. Marani

Most scientists studying the neuroanatomy of the sphincters and pelvic floor
will say that this developmental description is an oversimplification, and they are
right [15]. However, remember that it was said that few facts are known on the
development of the sphincter and of the pelvic floor muscles, and conclusions from
this toward nervous development are seemingly inappropriate [23]. Let us select
one structure and see how the final results support or contradict the above-given
description.
The neuronal innervation of the external urethral sphincter has long been a
subject of scientific dispute. How this structure was innervated to carry out its
function in voiding and ejaculation was a topic of argument. The Leiden group of
Donker always stated that the rhabdosphincter or external urethral sphincter was

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7.2 The Relation of the Pelvic Wall Muscles and the Sphincters 193

somatically innervated from the inside of the pelvis [16]. Others stated that the
external urethral sphincter was exclusively targeted by the pudendal nerve, which
is from the outside. Moreover, several groups supported sympathic, parasym-
pathic, and somatic innervation of this striated muscle [17–19]. Recently, the male
rhabdosphincter has been thought to be innervated somatically from the inside and
the outside, a dual somatic innervation, and to contain a dual autonomic one, that
is parasympathic and sympathic, from the inside [20].
So, confusion is everywhere concerning this topic. The exact neuronal control of
the rhabdosphincter has been disputed for over 50 years; that is why one stays with
a simple explanation that fits. In Chap. 8, one will notice that developmental studies
do show the central organization for several central nervous systems [21–23].

7.3 Scarpa’s, Buck’s and Colles Fascias

The whole body is surrounded by a fascia that is placed directly below the sub-
cutis. This fascia can be adhered to the fascias of superficial muscles, to bony parts
or separated by still a layer of fat detaching it from lower-placed structures, but can
always be discerned. It can exist as one layer or being split into two or more layers,
especially in extremities and the back [24]. This coverage of the lower abdomen,
vulva, penis, and perineum is by a continuation of its upper abdominal part called
the fascia abdominis superficialis, and its continuation toward the perineum is the
fascia perinei superficialis. These topographical names of parts of one and the
same fascia are called in the Anglo-Saxon literature Scarpa’s fascia and Colles
fascia, respectively. Who were these two name-givers of fascias?
Antonio Scarpa (1752–1832) was a famous anatomist and surgeon, who studied
medicine in Padua, became professor of Anatomy and clinical Surgery first in
Modena, later on in Pavia. He published books on the following: auditory and
olfactory anatomy, innervation of the heart, bone tissue, congenital clubfoot,
aneurysms, and surgical topics. He was leading in all these aspects. His interest
and book on inguinal hernias translated in several languages brought to his
attention a fibrous fascia that stretched from the lower abdomen and the pubic
bones toward the penis. Later on, it got his name [25].
Abraham Colles (1773–1843) studied at Trinity College of the University of
Dublin and in Edinburgh medicine. He became professor of Anatomy, Surgery,
and Physiology at the Royal College of Surgeons in Ireland. He was a surgeon at
Dr. Steevens Hospital in Dublin. Besides his publications on what is now named
Colles fracture, he studied anatomically the inguinal and perineal regions [26].
Even the inguinal ligament is sometimes called Colles ligament, but also Poupart’s
ligament. Inguinal/perineal studies are at the base of the name giving, since sci-
ence at the turn of the eighteenth/nineteenth century struggled for explanations of
inguinal and perineal hernias and affections. If you were famous and seemingly
contributed to the solution, than your name was adopted.
There is a total difference in opinion between anatomists and surgeons con-
cerning this fascia. The start of this part gives the anatomical ‘‘reality’’. ‘‘Before

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194 7 Anatomy of the Pelvic Wall

proceeding to a discussion of the anatomy of the perineum it is interesting to note


that the pure anatomist has no counterpart for some of the terms used by surgeons.
Denonvillier’s fascia, the recto-urethralis muscle, Buck’s fascia, and Colles fascia
are surgical terms used to designate conveniently some anatomical landmarks
which to the anatomists are not definite structures’’ proclaimed Miley Wesson in
his 1923 article [27] in which he tried to substantiate the nomenclature of the
urogenital triangle by anatomical, embryological, and surgical results.
All started with inguinal hernias and perineal defects, as studied by Scarpa and
Colles, which forced surgeons, in the time before anesthetics were available, to
look for landmarks to operate secure and fast. There is no doubt that Scarpa’s
fascia and Colles fascia are the same structure only at different places and thus
named differently by different surgeons. So the question where Scarpa’s fascia
starts and ends (the same holds for Colles fascia) is irrelevant. Thus, Scarpa’s
fascia can go on into the penis, while others call that part still Colles fascia. Buck’s
fascia is of another order. It encircles the corpora cavernosa and the urethra and
thus leaves Colles/Scarpa’s fascia at the suspensory ligament of the penis [27], see
also [28] (Fig. 7.16).
Gurdon Buck (1807–1877) studied at the Columbia University College of
Physicians and Surgeons and worked as military plastic surgeon during the Civil
War and at the New York Hospital. He is known for the introduction of pre- and
postoperative photography in publications and for the description of the deep
penile fascia, bearing his name [29A].
But, why is this discussion in the literature on these fascias over and over again
so important. To start with infections, ‘‘Fourniers gangrene is an infective nec-
rotizating fasciitis of the perineal, genital or perianal regions. The infective process
leads to thrombosis of subcutaneous blood vessels, resulting in gangrene of the
overlying skin’’ [29]. It is the fascia which is infected, and once (mainly gut)
bacteria are settled within connective tissue, they are hard to fight, especially if
another disease is also at hand. The source of infection, although sometimes hard
to establish, is urogenital in 45 % of the cases, anorectal (35 %) or skin related
(21 %). It is often associated with alcoholism (in 25–50 % of the cases) or diabetes
(40–60 %). A new group of patients are the HIV-infected ones, and they are
especially in danger in socioeconomic bad situations. Immune suppression in
transplantation or by chemotherapy increases the risk on Fournier’s gangrene. The
mortality rate is 20–22 % and has not changed after the introduction of antibiotics.
It can occur in males and females [29]. Surgical treatment of the gangrene skin is
necessary, and it came as a surprise that unprocessed honey put on the closed
wound accelerated healing. ‘‘Honey has a low pH of 3.6 and contains enzymes,
which digest dead and necrotic tissue. It contains antimicrobial agents to which the
infecting organisms are usually sensitive. It also stimulates growth and multipli-
cation of epithelial cells at the wound edges. These changes occur within a week of
applying honey to the wound’’ [29]. Thus, weakening of the patient by illnesses
increase the settling of bacteria in the fascias in penis, scrotum perineum, and
vulva.

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7.3 Scarpa’s, Buck’s and Colles Fascias 195

Fig. 7.16 Normal penile


anatomy. Drawings illustrate
the shaft and a transverse
section through the penile
shaft also depicted in the
upper figure (lower figure
from Em Boulanger, 1902) S
and an opened frontal view of a S
the penis and abdomen to the
bottom (upper figure with S
permission Dept Anatomy a
and Embryology, Leiden,
courtesey J. M. F.
Landsmeer ). The tunica C
albuginea (gray line) is seen
enveloping the two corpora
cavernosa and the corpus
spongiosum. In red are
indicated: S the suspensory
ligament of the penis and Sa
Scarpa’s fascia. Green arrows
indicate a superficial fascia
called Colles fascia (C) that
surrounds the tunica
albuginea and urethra with its
corpus spongiosum. Note that
Colles fascia continues into
the prepuce (upper figure).
The deep dorsal vessels, the
superficial dorsal vein, and
the cavernosal arteries are C
also depicted to the right. One
should note that the stiffness
of penis is made by the
albuginea fascias

The question arises why is the infection restricted to the lower pelvis? The
gangrene can also be found on other bodily places, but its pelvic restriction is due
to the adherence borders of the fascia of Colles/Scarpa. Laterally, it is tightly fit to
even stronger blades of the thigh and leg, inhibiting passage, while medially, it is
strongly interwoven with the midline connective plate (linea alba). So, a left and a
right pocket are present (Fig. 7.17). The fascia of Colles/Scarpa fits like a bikini
string around the thighs and legs, only it does not pass between the buttocks. (One
should note that these fascias can be continuous up to the clavicle).

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196 7 Anatomy of the Pelvic Wall

Fig. 7.17 Left and right pocket, below Scarpa/Colles fascia, filled with X-ray contrast.
P indicates a metal pin placed over the scar of an appendicectomy (Note that the contrast is
stopped by the scar tissue, compare right and left) and F is the fundus of two pockets with perineal
extensions around the penis (photograph reproduced with permission from B. F. Martin [32])

The fascias are also important for incision for operations (e.g., hernias, cae-
sarian, and several gynecological ones) and closure of these wounds. Think of
laparotomy (opening of the abdomen) below the umbilicus. ‘‘Surgeons suture its
cut edges during the closure of an operation wound, knowing that, if they omit to
do so, the resulting scar will eventually become needlessly wide and unsightly’’
[30]. Flaps for vaginal and perineal reconstructions, so-called fascio-cutaneous
flaps, only function well if they are tightly sutured to Colles fascia. The same holds
for medial thigh lifts in plastic reconstructions, even a fascial anchoring technique
is described [31].
Since Scarpa/Colles fascia is overlying the fascia of the external abdominal
muscle, it can be free of or loosely bound to this abdominal fascia. It therefore can
organize a pocket, open at its upper edge near the umbilicus but spreading with three
fingers like that a glove into lateral, intermediate, and medial parts. The medial
finger continues into the scrotum or labia majus and is connected to the intermediate
pocket. The lateral pocket directs toward the perineal area. In cases of genital
edema, Fournier’s gangrene, or urethral rupture, these pockets will be filled with
fluid or even urine [32]. The discussion is not yet ended since Lancerotto et al. [32]
discern a superficial fat layer, a membraneous layer (fascia), and a deep adipose
layer before reaching the fascias of the superficial abdominal muscles. What looks a
simple problem now has bothered over two centuries anatomy and surgery.
Increasing confusion can be noted, since the subcutaneous fat layer above the fascia
of Scarpa/Colles is called the fascia (it is no fascia!) of Camper. By the way,
although Camper was famous also for the first correct explanation of the inguinal
hernia, this layer was never described by Petrus Camper (1722–1789) [32, 33].
The muddle is even greater if one considers the term fascia. Above, it was said
that the fascia of Camper is not fascia but adipose tissue. Some rectification is
needed if we consider the layers from skin to the muscles and the use of the term
fascia in different languages (Table 7.1).

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7.3 Scarpa’s, Buck’s and Colles Fascias 197

Table 7.1 Different meanings of the term fascia in various languages


Skin
Fascia begins here in English
Superficial fascia
Fatty layer
Fascia began here in French
Membranous layer
Loose connective tissue
Fascia begins here in German
Superficial investing fascia
Loose connective tissue
Epimisium
Muscle
Reproduced with permission from Wendell-Smith [34]

One of the problems arises from different terminology used! The Nomina
Anatomica published by the International Anatomical Nomenclature Committee
on behalf of the International Federation of Associations of Anatomists has
repeatedly pinpointed the problem and did a proposal, but still scientists use
confusion terminology [34]. Is it reasonable that Scarpa, Colles, Buck, and Camper
all had a different idea of what a fascia is and that this trouble is still not overcome
in modern times, due to our ignorance of these differences in fascia definition?

Literature

Literature has been grouped in reference lists of several chapters in those cases where
arguments are difficult to entangle or published over several articles or books. In cases of
citation the article or book involved is indicated by the reference number together with a
capital Arabic letter.
1. Boulanger EM (1902) Handboek voor gehuwden. NV Gebroeders Graauw, Amsterdam,
Soerabaya
2. Hafferl A (1969) Lehrbuch der topographischen Anatomie. Springer, Berlin
3. Marani E (1996) Vorm en functie van het menselijk bekken. In: Urodynamica en Urine-
incontinentie. Boerhaave Cie., Leiden, The Netherlands
4. Marani E (1993) The human pelvic floor: an introduction. In: Boerhaave cursus: pelvic
floor. Boerhaave cie., Leiden, the Netherlands
5. Marani E, Lycklama à Nijeholt AA, Bastiaanssen E (1994) Urine-incontinentie: substraat,
werking en dysfunctie. In: Knook DL, Goedhart WJA (eds) Mictieproblemen bij oudere
mannen en vrouwen. Nieuwkoop, The Netherlands, Stichting Gerontologie
6. Marani E (1990) Bluff your way in anatomy, Students publication, Leiden and Christensen
LL, Djurhuus JC, Constantinou CE (1995) Imaging of pelvic floor contractions using MRI.
Neurourol Urodyn 14:209–216
7. Pit MJ (1996) De operatieve behandeling van urine stress-incontinentie. In: Urodynamica
en Urine-incontinentie. Boerhaave cie., Leiden, The Netherlands; Pit MJ et al (2003)
Anatomy of the arcus tendineus fascia pelvis in females. Clin Anat 16:134–137
8. Marshall VF, Marchetti AA, Krantz KE (1949) The correction of stress incontinence by
simple vesicourethral suspension. Surg Gynecol Obstet 88:509–518

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198 7 Anatomy of the Pelvic Wall

9. Burch JC (1961) Urethrovaginal fixation to Cooper’s ligament for correction of stress


incontinence, cystocele, and prolapse. Am J Obstet Gynecol 81:281–290
10. McGuire EJ, Lytton B (1978) The pubovaginal sling in stress urinary incontinence. J Urol
119:82–84 and Pereyra AJ (1959) Simplified surgical procedure for the correction of stress
urinary incotinence in women. West J Surg 67:223–226
11. Stamey TA (1973) Endoscopic suspension of the vesical neck for urinary incontinence in
females. Ann Surg 192:465–471
12. Raz S, Siegel AJ, Short JL, Snyder JA (1989) Vaginal wall sling. J Urol 141:43–46
13. Politano VA, Small MP, Harper JM, Lynne CM (1974) Periurethral Teflon injection for
urinary incontinence. J Urol 111:180–183
14. Light JK, Scott FB (1985) Management of urinary incontinence in women with artificial
urinary sphincter. J Urol 134:476–478
15. Marani E (1998) De ontwikkeling van de bekkensluitspieren. Profundum 4(1):4–6
16. Donker PJ, Droes JTPM, Ulden BM (1976) Anatomy of the musculature and innervation of
the bladder and the urethra. In: Williams DI, Chisholm GD (eds) Scientific foundations of
urology. Heinemann Medical Books, Oxford, pp 32–39
17. Elbadawi A, Schenk EA (1974) A new theory of the innervation of bladder musculature. 2.
Innervation of the vesicourethral junction and external sphincter. J Urol 111:613–615
18. Kumagai A, Koyanagi T, Takahashi Y (1987) The innervation of the external urethral
sphincter: an ultrastructural study in male subject. Urol Res 15:39–43
19. Lincoln J, Crowe R, Bokor J, Light JK, Chilton CP, Burnstock G (1986) Adrenergic and
cholinergic innervation of the smooth and striated muscle components of the urethra from
patients with spinal cord injury. J Urol 135:402–408
20. Hollabaugh RS, Dmochowski RR, Steiner MS (1997) Neuroanatomy of the male
rhabdosphincter. Urology 49:426–434
21. Lakke EAJF (1997) The projections to the spinal cord of the rat during development; a
time-table of descent. Adv Anat Embryol Cell Biol 135:1–143
22. Popowsky J (1899) Zur Entwicklungsgeschichte der Dammuskulatur beim Menschen.
Anat Hefte 12:13–49
23. Putte van der SCJ (2005) The development of the perineum in the human. Adv Anat
Embryol Cell Biol 177:1–135
24. Abu Hijleh MF et al (2006) The membranous layer of superficial fascia: evidence for its
widespread distribution in the body. Surg Radiol Anat 28:606–619
25. Fye WB (1997) Antonio Scarpa. Profiles in cardiology. Clin Cardiol 20:411–412 and
Rutkow IM (1998) Antonio Scarpa (1752–1832). The history of hernias. Hernia 2:95–97;
Ellis H (2006) Eponyms in groin surgery. Surgery 24:257–259
26. Little M (2006) The Gordon Gordon Taylor memorial lecture: Surgical giants and giants
among surgeons- The case of Abraham Colles. ANZ J Surg 76:1115–1120
27. Wesson MB (1923) Fasciae of the urogenital triangle. JAMA 81:2024–2030
28. Bertolotto M, Serafini G, Savoca G et al (2005) Color Doppler US of the postoperative
penis: anatomy and surgical complications. Radiographics 25:731–748
29. Smith GL, Bunker CB, Dinneen MD (1998) Fournier’s gangrene. Br J Urol 81:347–355
and Levenson RB, Aya KS, Novelline RA (2008) Fournier gangrene, role of imaging.
RadioGraphics 28:519–528
29A. Buck BJ, Selman SH (2011) Beyond Buck’s fascia: the life and contributions of Dr.
Gurdon Buck (1807–1877). Urol 78:492–495
30. Forster DS (1937) A note on Scarpa’s fascia. Anatomical notes. J Anat 72:130–131
31. Tham NLY (2010) The pudendal thigh flap for vaginal reconstruction: optimizing flap
survival. J Plast Reconst Aesth Surg 63:826–831 and Lockwood TE (1988) Fascial
anchoring technique in medial thigh lifts. Plasr Reconstr Surg 82:299–304
32. Martin BF (1984) The formation of abdomino-perineal sacs by the fasciae of Scarpa and
Colles, and their clinical significance. J Anat 138:603–616 and Park BJ, Sung DJ, Yeom
SK et al (2010) Communication between spaces formed by fasciae of male external
genitalia and perineum. Computed tomographic cadaveric study and clinical significance.

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Literature 199

J Comp Ass Tomogr 34:193–198; Lancerotto L, Stecco C, Macchi V et al (2011) Layers of


the abdominal wall: anatomical investigation of subcutaneous tissue and superficial fascia.
Surg Radiol Anat 33:835–842
33. Tobin CE, Benjamin JA (1944) Anatomical study and clinical consideration of the fasciae
limiting extravasation from the penile urethra. Surg Gynecol Obstet 79:195–204. Tobin
CE, Benjamin JA (1949) Anatomic and clinical re-evaluation of Camper’s, Scarpa’s and
Colles’ fasciae. Surg Gynecol Obstet 88:545–559
34. Wendell-Smith CP (1997) Fascia: an illustrative problem in international terminology.
Surg Radiol Anat 19:273–277

sergiocamargo47@gmail.com
Chapter 8
Development of the Pelvic Diaphragm
and More

There is no considerable muscle in the body whose form and functions are more difficult to
understand than those of the levator ani, and about which such nebulous impressions
prevail. (Dickinson, 1889)

Despite all publications on different muscles present within the pelvic diaphragm,
development shows that there are only two: the levator ani muscle and the coc-
cygeus muscle. The extended description given is needed to contradict literature.
The pelvic diaphragm does not contain gender differences. A nearly philosophical
question is paired and unpaired construction of pelvic organs, demonstrated by
development of the urogenital system and pelvic sphincters. Anal sphincter
development is treated together with anorectal malformations. Attention is given
to placodes, neural crest development, and the development of pelvic brain
centers.

8.1 The Two Layers in the Pelvic Diaphragm

In Sect. 4.9, it became manifest that a definition for pelvis was hard to make.
Surgeons are less philosophical and more practical. They introduced the term
pelvic floor on which we elaborate here more.
The definition of pelvic diaphragm versus pelvic floor is memorable, since
various people think they are identical. ‘‘The ‘pelvic floor’ is the bottom of this
pelvic container (the hollow ring formed by the bony pelvis is meant) and includes
all of the structures that lie between the pelvic peritoneum and the vulvar skin’’
[1]. The pelvic diaphragm is the bottom of the pelvic floor. A different definition of
the pelvic floor is given by Fritsch et al. [2] ‘‘The pelvic floor constitutes the caudal
border of the human’s visceral cavity.’’ And somewhat further on: ‘‘the tissues
comprising the pelvic floor are striated muscles closely correlated to the smooth
muscular layers of the pelvic organs as well as different kinds of connective
tissue.’’ Seemingly with pelvic floor is meant the pelvic diaphragm. The Dictio-
nary of modern medicine by J. C. Segen (1992) delineates the term pelvic floor:
‘‘surgical anatomy a well-defined region that is bordered anteriorly by the pubis

E. Marani and W. F.R.M. Koch, The Pelvis, 201


DOI: 10.1007/978-3-642-40006-3_8,  Springer-Verlag Berlin Heidelberg 2014

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202 8 Development of the Pelvic Diaphragm and More

Fig. 8.1 What she asked for,


of course, was a new pelvic
diaphragm, not a new pelvic
floor! with permission Daily
Mirror, 28 Nov, 2003, p. 23

and posteriorly by the sacrum, laterally by the ischial and iliac bones, superiorly by
the peritoneum and inferiorly by the levator ani and coccygeus muscles, the last
named forming the pelvic diaphragm.’’ Let us stick to this dictionary definition.
The discussion is not out of date as the following heading in an American
newspaper (Fig. 8.1) shows:
The pelvic diaphragm has changed function in evolution due to the biped
movement of humans. Consequences are due to the long axis of the body which is
vertical: a broad pelvis, large fixation area of the sacrum, and a convex bending of
the sacrum of nearly 90 with its ileum and a change of the function of muscles
(note that bending between sacrum and vertebral column is 140, see Chap. 1 and
Fig. 1.3 and [3]).
‘‘In most mammals, the pelvic diaphragm is largely sphincteric in action, to
secure continence, as the ventral abdominal wall achieves the supportive function
of the (pelvic) viscera. The muscular fibers, which form a distinct layer in the
pelvic floor of mammals, are all situated around the rectal and genito-urinary
canals, and the rest is made up of connective tissue and integuments (Thompson
1899)’’ [4A]. So in quadrupeds, the belly muscles have the function of support of
the pelvic and abdominal organs. In those mammals, in which the long axis of the
body is absolutely or approximately vertical (e.g., Homo sapiens), a great differ-
ence in the architecture of the pelvic floor is apparent. The outlet of the pelvic
cavity is modified and adapted for supportive maintenance of pelvic and

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8.1 The Two Layers in the Pelvic Diaphragm 203

abdominal viscera. In addition to a layer of muscles with mainly sphincteric


functions, a second layer has developed into a well-marked diaphragm, which
constitutes a muscular and tendinous sheet attached to the inner circumference of
the pelvis. In this pelvic floor, two distinct layers or diaphragms can be recognized,
with contrasting arrangement and function. The upper or superior layer forms a
more or less complete pelvic diaphragm (first so named by Meyer, in 1861),
designed for purposes of support, and the inferior layer forms sphincters around
the rectal and genito-urinary canal for purposes of maintaining continence [4A].
Of course, the sphincteric layer and pelvic diaphragm are well integrated, for
example the striated musculature of the anus and the levator ani are well inter-
connected. In cases of anorectal agenesis, the external striated musculature is still
present, but the inner smooth anal sphincter together with anus, anal canal, and
lower rectum are absent [4A]. The same interconnection holds for the genito-
urinary sphincters to their parts of the pelvic urogenital diaphragm. However, ‘‘the
existence of an embryologic (and consequently also a neuroanatomic) separation
between the two layers of the pelvic diaphragm has been discussed extensively in
the medical literature’’ [4A]. The consequence is that we can study the develop-
ment of the pelvic diaphragm first without going to deeply into the sphincteric
development.
It is obvious that older literature neglects the development of the pelvic dia-
phragm, except Popowsky [4A]. However, he had to do his study on an incomplete
series of embryo’s and fetuses, and therefore, ‘‘he was unable to describe the early
stages of the development of the levator ani’’ [4A]. He divided the levator ani in a
pars pubica and a pars iliaca, which could not be separated from the coccygeal
muscle, so he lumped all striated muscles of the pelvic diaphragm.
To come back for a moment on the above-mentioned anorectal agenesis, one of
the first publications of this deflection is by Nicolaes Tulp (1593–1674). In his
‘‘Inzichten over de geneeskunst in vier boeken met koperen platen’’ (Insights in
medicine in four books with cupper plates), the Dutch translation of his Latin
Observationes medicae (1641) [4B], he states:

But even unhappier as one of the two (other patients described above it)
Was the person who recently was born
With a closed arse and a rod
Of such type, that excrements of the gut
Through it unburdens itself daily
Maar nog ongelukkiger als een van beiden
Was hij die kortelings ter wer(el)d kwam
Met een gesloten aars en een roede van
Dat fatsoen, dat de drek van het gedarmte
Haar dagelijks door dezelfde ontlastte.

This description given by Nicolaes Tulp is clear enough to diagnose it as an


anorectal agenesis patient with a rectourethral fistula or a rectovesical fistula. His
remark, that surgery of that time, was not a match for this deflection, hold for
several centuries.

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204 8 Development of the Pelvic Diaphragm and More

8.2 Early Embryology: Overview

It is unfeasible to describe the whole development of the embryo till the moment
of first interest in this chapter part: the start and the expansion of the pelvic
diaphragm muscles. Figure 8.2 shows several of the main exterior factors that can
be noticed, e.g., on an ultrasound echo during the embryological and start of the
fetal period (fetal period begins in week 9 of development). Heart beat starts at
23–25 days of development. The leg bud and the genital tubercle are produced
around week 5 till 7 and both are involved together with the cloaca formation in
the organization of the intra- and extrapelvic structures. The initial movements of
the human embryo can be noticed around week 7 and 8. At week 7, the first
striation of the pelvic diaphragmatic muscles can be seen. Undifferentiated lumps
of mesenchymal tissue that will create the pelvic diaphragmatic muscles are
already present, of course, in the previous period. In this stage (week 7–8), general
embryonic movements start. It will be altered into sucking, into specific leg and
arm movements and leg and arm stretching later on (week 10–12). The pelvic
diaphragmatic muscles reach their final destinations in this period and at 12 weeks
a pelvic diaphragm is present at the commencement of the fetal period. Being

Fig. 8.2 Embryonal to fetal development indicating the time frame for limb bud development
and first movements like startle, leg movements, hiccup, sucking, and stretch  E. Marani

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8.2 Early Embryology: Overview 205

Fig. 8.3 Early embryonic and fetal development of structures in the pelvis. For explanation see
text (reproduced with permission of the Department of Anatomy and Embryology, Leiden,
courtesy Prof. Dr. J. M. F. Landsmeer )

striated musculature, the pelvic diaphragm muscles develop in the same time range
as the striated muscles for arms and legs.
In Fig. 8.3, an oblique frontal view and two horizontal sections through the
caudal area of the developing embryo are shown. By lifting the pericard (heart)–
liver swelling, in Fig. 8.3a, a view is possible on both the yolk sac duct and the
base of the allantois. Together with blood vessels, they constitute first a connecting
stalk and later on the umbilical cord. The continuum of yolk stalk and allantois in
the embryo is responsible for the gut, and by its caudal extension, the allantois will
produce the bladder in the embryo (follow canal in the penis upward in Fig. 8.3b
and c). Figure 8.3b shows the progressing ‘‘bony’’ pelvis with at the level of the
section the internal organs. Since the penis is just growing out (around 12 weeks),
thus entering the early fetal period, one discerns in front of the section, the bladder
and two tubes, the primitive ducts of Wolff (the primitive male gonadal ducts).
From the duct of Wolff, the ureter will expand and in Fig. 8.3c the bladder,
urethra, ureters, gonadal ducts, and rectum can be discerned shining through the
skin wall. The tubes can be followed toward the ascending kidneys and the
descending gonads.

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206 8 Development of the Pelvic Diaphragm and More

The development of gonads and its ducts has its homology in the development
of the legs. Mutants with affected limbs can have affected genitalia too: ‘‘In the
worst cases, male infants have just the vestiges of a scrotum and penis. Many of
the molecules that make limbs also make genitals, and it should be no surprise that
some mutations afflict both. The widely rumored correlation between foot and
penis size also, surprisingly, turns out to be at least partly true. No man should be
judged by the size of his feet, however for the correlation, though statistically
significant, is weak’’ [4C].
In the next paragraphs, the results of the study of the development of the pelvic
diaphragm [4A] in both the embryonic and fetal period will be discussed.

8.3 Development of the Human Pelvic Diaphragm

Three large muscles play their role in contributing to the human pelvic diaphragm:
m.obturatorius internus, m.levator ani, and the m.coccygeus (see Chap. 7 and Fig.
7.5). There are some smaller ones, e.g., the musculus sacrococcygeus ventralis
going from the sacrum to the coccygeal bones, but they are rudimentary. In whales
and dolphins, in fact in all cetaceans, the bony pelvis together with the hind leg
bones is vestigial and not connected anymore to the vertebral column. In males, a
pelvic bone is still present, to adhere the long and tough penis. In females, the
rudimentary pelvic bone is often not found [3, 5]. By the way, the bull’s pizzle
children at school were chastised with, is a bull’s penis, long and tough. Cetaceans
are thought to be evolutionary related to hoofed animals, which is also expressed
in their sub-skinned storage and construction of their penis [8]. So, in whales, there
is no round bony pelvis and there are no connections to the sacral bone. So to say
the rudimentary pelvis, with in it femur and connected tibia, is ‘‘free floating’’ of
course fastened by ligaments to the interior of the pelvic cavity. The area of
fixation for the levator ani, therefore, is minimal. It connects to the backside to the
chevrons, V like extrasmall bone components just beneath the vertebrae, to lateral
onto the fascias of the large inner compartment of the swimming muscles (hyp-
axial muscles) and with one or two ligaments to the rudimentary pelvic bone. It
encloses like in humans the digestive tract ending. In the midline at the front side,
both levator ani muscles form a closure ligament [5].
One should notice that levator ani attachment to fascias of muscles, in humans
the obturator internal muscles and in whales the hypaxial swimming muscles, is
variable in evolution, like pants that can slip down if the elastics are weak.
Whatever the points of fixation present, the levator ani, if present, will close the
pelvis as a diaphragm.
The two ligaments that connect in whales the levator ani to the pelvic bones,
gives the impression that the levator can be subdivided in a pubo- and an ilio-
coccygeal part. The levator ani is sometimes also subdivided in a pubo- and an
iliococcygeal muscles in humans, while a puborectalis muscle is noted too
(however, see below and Chap. 7 and Sect. 7.1.2).

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8.3 Development of the Human Pelvic Diaphragm 207

(a)

obturatorius int.
hiatus

anterior

levator ani

foramen obt.
coccygeus anus

posterior

(b)

Fig. 8.4 a The development of the muscles involved in the construction of the pelvic diaphragm.
The first circle is at 7 weeks postconception and the last is at 12 weeks post conception, which
holds for all depicted muscles. b Muscles of the pelvic diaphragm pulled down and forward
mirroring the fetal development  E. Marani

Before going into detail, the overall development of the pelvic diaphragm can be
described as in Fig. 8.4. If two planes are put perpendicular to each other and the
hollow of the pelvic diaphragm is neglected, then the main directions of the
development of the muscles can be indicated. The obturator internus muscle’s
primordium is located posterior on the ischial bone at its ramus from there on it
grows over the foramen obturatum. Its direction thus is back to front or dorsoventral.
The levator ani’s primordium is uninterrupted next to the anus. From there on,
it travels laterally in a fan-like manner. Its direction of development is
mediolateral.
The coccygeus muscle appears at the future spina ischiadica (which develops
later), just at the place where the obturator internus muscle leaves the pelvis. A
lateral and a medial coccygeal part can be distinguished (indicated by a stippled

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208 8 Development of the Pelvic Diaphragm and More

Fig. 8.5 Reconstruction of a


28-mm embryo nearly
58–59 days of postconception
[4]. In yellow are the pelvic
structures indicated,
including the uterus. Red is
the obturator internus muscle,
blue the levator ani, and
green is the coccygeus
muscle represented. All ‘‘to
become bony’’ pelvic
structures are still
cartilaginous [4A]. White
arrow indicates the foramen
obturatum  W. Koch

line in Fig. 8.4). The developmental direction here is lateromedial. In the open
cube in Fig. 8.4, both symmetric halves of the pelvis are drawn together with the
developmental course of these muscles. It is now clear that both the levator ani
muscles part, while both the coccygeus muscles approach each other.
If one now pulls the anus downward and forward, the last due to the bending of
the embryo’s cauda or tail, in such a way that a funnel originates (Fig. 8.4b) one
gets the picture as in Fig. 8.5 of an 8 weeks embryo. (Note that directions are
different in Figs. 8.4b and 8.5)
The direction of development changes for levator ani and coccygeus muscles
due to the creation of a downwards directed funnel, but not for the obturator
internal muscle. The change in direction is more upward for the levator ani and
partially more forward and backwards for the coccygeus muscle.

8.4 Detailed Description of the Development of the Pelvic


Diaphragm

In the cartilaginous pelvis, the connection between the pubic bones is not made
before 9 weeks postconception. It means that both halves of the pelvic diaphragm
are growing independently from each other at least to this postconceptional age.
One sees even up to 12 weeks such an independent outgrowth of the muscles
concerned, since both muscle halves do not reach each other.
The obturator internal muscle expands from behind the foramen obturatum. Its
expansion is dorsoventrally, and therefore, ‘‘the margins of the foramen obturatum

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8.4 Detailed Description of the Development of the Pelvic Diaphragm 209

and the caudal edge of the foramen ischiadicum majus are not the origins of the m.
obturatorius internus, but the insertions’’ [4A]. Another phenomenon is that the
connective thickening of the membrana obturatoria is induced by its contact with
the obturator internal muscle. Before that time, it is a thin mesenchyme-like
covering of the foramen. Therefore, the buildup of the membrane has also a
dorsoventral gradient. Moreover, the expansion of the obturator internal muscle
toward the trochanter major of the femur can be fascia, muscle, or tendon in
embryo and fetus, which is in accordance with the mature situation [4A].
The levator ani muscle can be discerned as a muscular entity 7 weeks post-
conception. Mesenchymal-like densities are found at that place earlier [6], but the
first signs that these densities will develop into a muscle are around the seventh
week. It clearly starts in relation to the external anal muscle and progresses toward
the os pubis and the os coccygeus, semi-rounding the hindgut, and sinus uro-
genitalis. During this early development, the pubic bones are still not united,
stressing the independent development of both levator ani muscles. Moreover, no
subdivision of the developing levator ani can be discerned, not by subfascias or by
muscle fiber distribution [4A].
Therefore, the presence of a separate pubococcygeus and iliococcygeus and/or
puborectal muscle has to be denied.
No muscle fibers are found to cross the midline behind the rectum. There are,
therefore, no indications of a puborectal sling. Presumably, the mature discerned
muscles in the levator ani are non-existing as separate entities. These mature
discerned muscles are nothing else but concentrations of levator ani fibers pro-
voked by pelvic diaphragm forces after birth.
Second, processes, which are all related to external factors, induce changes of
the medial levator ani position. In its development, the pubic bone expansion,
especially the formation of the symphysis pubica is important for the levator ani.
‘‘…the growing pubic bone, which more or less drags the m.levator ani toward the
midline, outlining the hiatus urogenitalis’’ [4A]. So the interaction between
the growing levator ani and pubic bones brings the levator ani muscles ventrally to
the midline. The rest of the closure of that part of the pelvic outlet by the levator
ani is organized by the perineum closure and by the development of the anococ-
cygeal ligament, behind the rectum. While the anococcygeal ligament is broad
early in development, it narrows, adding to the nearing of both levator ani muscles.
Midline closure of both levator ani muscles is organized by other structures and
the levator ani is, so to speak, passively involved.
The m.coccygeus, also called the tail-waving muscle, changed in bipeds from
motion function toward a support function. As a consequence, the coccygeal
muscle in adults can loose partly or totally its muscle fibers and can be reduced to a
fibrous-like plate. At 7 weeks post-conceptionally, the first indications of a mus-
cular structure are found [4]. Even at this stage, a subdivision into a ventral and a
dorsal part can be discriminated. The ventral part will increase in muscular volume
proceeding into the m.coccygeus. Its dorsal part, however, will reduce its muscular
characteristic, ending up in the construction of the fibrous sacro-spinal ligament
(see Fig. 7.1).

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210 8 Development of the Pelvic Diaphragm and More

8.5 Gender of the Pelvic Diaphragm

The growth of the pelvic diaphragm is not gender related, while the urogenital
diaphragm is. The embryological and fetal results do not give any indication for a
sexually based difference in males and females [4], although Fritsch [4D] does
proclaim a gender difference. ‘‘We have also shown that the distinct sexual dif-
ferences within the pelvic floor muscles as well as within the sphincter muscles can
already be found in early human life’’ [2]. The fetal material, in both studies, just
overlaps see [4A] and [4D] in the early fetal period from 34 till 50 mm length,
corresponding to 9 till 12 weeks, still rather different opinions.
But what are these sexual differences? ‘‘In the female, a small layer of con-
nective and adipose tissue separates the levator ani from the pelvic organs. This
layer is thin and already intermingled with connective tissue. In the male, the
levator ani is a well-developed muscle’’ [4] (see also [2]). So, a retard of devel-
opment is considered a sexual dimorphic characteristic as is the presence of a
fatty-connective layer. In Chap. 16, one will notice that the variability in con-
nective tissue is large both in males as in females.
When is the closure of the pelvic diaphragm? The moments in which levator ani
and coccygeus adhere to each other are unknown. Since the just born is more
sphincteric in pelvic floor behavior and crawling is an intermediate stage before
standing (Fig. 8.6), the function of the pelvic diaphragm as an organ supporting
structure is late after birth (around one to one and a half year). The spina iliaca
expands also late as a structure of the bony pelvis, being adherence for pelvic
diaphragmatic structures. Therefore, a large portion of the development of the
pelvic diaphragm is also postnatal. This postnatal development is responsible for
the pelvic bony gender differences (see Chap. 21).

Fig. 8.6 The position of the pelvis rotates downwards from the fetal period till the postnatal
situation. The vertebral column of the just born is rather straight. During the development of the
cervical lordosis, this position is nearly unchanged. In the standing/walking postnatal, the pelvis
is further tilted downwards to reach later its mature position

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8.6 Development of the Uropoetic System 211

8.6 Development of the Uropoetic System

Since we closed the embryo at its caudal end by the pelvic diaphragm, we turn now
to the development of uropoetic structures in the pelvic interior. One should note
that the processes of closing the diaphragm and developing the pelvic interior are
of course in time parallel.
Along the abdominal wall, a tissue type develops that has the capacity to make
nephron-like structures (week 3–4). Nephrons are the building units of kidneys that
have the capacity to filter blood, remove ions, and re-uptake substances into these
nephric tubular structures.
From the upper part of the nephrogenic tissue, a tube develops that descends
toward the cloaca, a hollow or cave, in which ends, both the urogenital and
digestive tract. This tube is called the duct of Wolff (Fig. 8.7). Later, it develops
into the spermatic duct. This upper part of nephrogenic tissue degenerates the tube
survives. On the moment the duct of Wolff contacts the cloacal wall, it induces the
ureter bud, which in its turn produces a tube that ascends backwards to the lower
part of the nephrogenic tissue (week 5), where it induces the kidney. In the mean
time, the cloaca starts to organize itself into a part for the digestive tract with the
anal sphincters and a part for the male uropoetic system with the urethral
sphincters. The middle part of the nephrogenic tissue will make the gonadal
structure. The germ cells invade from outside the gonadal structures to produce a
functional testis or ovary.

Fig. 8.7 The downward progression of the mesonephric duct (Wolff, green; upper row), the
outgrowth and upward progression of the ureter (blue, middle row) and the induction of the kidney
(red; lower row) by the ureter together with the division of the cloaca (thick yellow part, middle
row) into urine and digestive tract (yellow, lower row). Light blue indicates the primitive nephrical
tissue that will produce kidneys and gonads. Brown is the outer wall of the embryo with dorsal
thickened wall and the spinal cord in it (reproduced with permission from Gosling et al. [9])

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212 8 Development of the Pelvic Diaphragm and More

Fig. 8.8 Development of the ureter (blue) from the duct of Wolff (green) into the cloaca/bladder
(yellow). The trigone (red) is the area between entrances of ducts of Wolff and ureters
(reproduced with permission from Gosling et al. [9])

But where is the ureter induced? One should expect at the cloacal wall.
However, it originates from the caudal end of the duct of Wolff (Fig. 8.8). Now,
something strange happens. The place of branching of the ureter is displaced
toward the cloacal wall. Then, it walks partly over the now-originating bladder to a
more rostral position. The area between both ducts of Wolff and both ureters is the
future trigone of the bladder. Another consequence is that outside a sling of the
ureter around the duct of Wolff is formed (Fig. 8.8). The duct of Wolff will contact
the testis, making the testicular tube, in females it degenerates.
The induction of the kidney by the ascending ureter is an astonishing phe-
nomenon. The lower part of the nephrogenic tissue is awaiting the induction by the
ureter, so to say. The future kidney’s whole cellular machinery is beforehand ready
to start. Already in the 1970s, it was discovered that if a filter was placed between
this nephrogenic tissue and the arriving ureter or even other epithelial tissue (e.g.,
salivary gland), the kidney would originate only if the filter pores were large
enough to let pass small protrusions of the epithelial tissue placed at the opposite
side and to contact the nephrogenic tissue. If pores were too small, no kidney
induction was noticed. Seemingly, contact between the two types of tissue is a
necessary condition to start kidney development [9].

8.6.1 Paired or Unpaired That is the Question!

Most structures are constructed in duplicate in the body: left and right arm and leg,
the two eyes, left and right shoulder muscles. Man is bilateral symmetric: we have
a left and right side along a midline axis. There are structures that develop
unpaired. One should be careful, since some structures look unpaired, but are
constructed by a left and a right part, that fuse later on. Such a structure is the
uterus. If the melting of the two developing uterus parts is incomplete a bicornal
uterus, a uterus containing two chambers instead of one, is the result. Another
possibility is a bilateral symmetric origin, but one of the pair regresses: the spleen.
Real unpaired structures are thought the sphincters at the end of the urine and
digestive tract (but see Sect. 8.9). Nevertheless, they are bilaterally innervated.

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8.6 Development of the Uropoetic System 213

Here, we put in two citations:


1. ‘‘One interesting question is whether the situs (arrangement and shape of
internal organs) of an individual organ is specified independently or in relation
to the situs of adjacent organs. Several experimental situations have shown that
the laterality information for each organ is set independently, that of neighbors
disregarded. Therefore, each organ unit appears to receive and respond to the
Left–Right pathway independently. In the absence of signaling, each unit
makes a random decision and the final outcome is the sum of independent Left–
Right decisions with respect to each other’’ [13].
2. ‘‘Paired occurrence implies neither a strict mutual independence nor a strict
mutual interdependence. However, if mutual functional interdependence is
present, then such interdependence does not involve structural unity. In other
words, there remain two structurally independent halves.’’ (Landsmeer,
unpublished).

The inevitable conclusion is that individual organs ‘‘look’’ for their structure
and position on their own.
So, the organization of the mature pelvic structures is due to the individual
action of the developing pelvic organs. Now one should look back amazingly to
the ureters, growing upward, inducing the kidneys that on their turn will ascend to
find their definitive position high in the abdomen: All independent actions of these
developing organs?
Nevertheless, the left–right symmetries and asymmetries are genetically based.
Situs inversus (reversed arrangement of organs with respect to the midline) is
related to genetic disorders in humans like primary ciliary dyskinesia or like the
autosomal recessive cystic kidney disorder, establishing that left–right axis is, as in
experimental animals, genetically coded [13]. We will see later that genetic
information plays an important role in how developing organs will proceed to their
maturation. Thus, ‘‘looking on their own’’ is genetically based.

8.7 The Development of the Pelvic Sphincters

Some distortions find their origin in maldevelopment of the sphincters with the
extreme of anorectal agenesis (see above). This provides a further reason to look
into the development of the pelvic sphincters.
As we already know, sphincter muscles develop earlier and more or less
independent in relation to the pelvic diaphragm muscles. Cloacal walls encircle the
primitive cloaca like two segments of an orange (Fig. 7.11). Cloaca is sewer in
Latin and means space of joint of urine and fecal tubes, still present in birds. The
clot of a bird on your head or shoulder exists, indeed, of urine and feces. These
primitive walls join each other in their upper central region being the genital
tubercle. The cloacal space is in humans divided into a urogenital and anorectal

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214 8 Development of the Pelvic Diaphragm and More

Fig. 8.9 The ‘‘classic concept’’ of the subdivision of the cloaca (Reproduced with permission
from Larsens Human Embryology 4th ed. Elsevier Health Sci)

sinus. Each will, respectively, develop into the terminals of the uropoetic, genital,
and rectal systems, each with its own sphincter: external urethral sphincter, vaginal
sphincter, and the striated anal sphincter respectively. In between these structures,
the perineum (the exterior closure line between left and right pelvic parts)
develops (Fig. 7.12). Moreover, both urethra and rectum will produce, somewhat
later than the striated sphincters, an internal smooth muscle sphincter in relation to
their striated sphincters.
Originally, the endgut and future bladder (allantois) both end into the cloaca,
which is closed by the cloacal membrane. The separation of the cloaca into an
anal/rectal and a urogenital part was thought to occur by fold formation in the
lateral walls that near each other (Retterer or Rathke’s folds) and the area between
allantois and hindgut (urorectal septum or fold of Tourneux) growing downwards
to meet these closing folds (Fig. 8.9). However, rat scanning electron microscopy
[10] and human embryo series [11] do not show the Rathke’s folds. This brings up
problems for the normal development, but also for the explanation of anorectal
anomalies and its surgical consequences and induces new research.
Indeed, recent studies [10, 11] do confirm that the urorectal fold or septum
increases and descents, whether by a real descent or by bowing of the cloacal space
[6], the septum nears the cloacal membrane. However, it is the cloacal membrane,
reduced at its dorsal or ventral side that indicates whether a normal development or
an ectopic anal or ectopic urogenital orifice, respectively, will mature (see
Fig. 8.10). These wrongly placed openings are called fistulas, but in fact are real
displaced urethral or anal openings and the corresponding sphincters can be
refound at these ectopic openings. The cloacal membrane will not contact the
urorectal septum, but it degenerates by itself [14]. Therefore, the urorectal septum
is thought to make the perineum [11].
The whole development of the cloacal organs is regulated by growth factors
that are released due to a coordinated action of the limb bud, the genital tubercle,
and the cloaca. Epithelia and mesenchyme of these structures produce the growth

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8.7 The Development of the Pelvic Sphincters 215

Normal Abnormal
Ectopic anal Ectopic urethral
Genital Genital orifice orifice
walls tubercle

Urorectal Cloacal
septum membrane

Tail groove
Future anal
opening

Fig. 8.10 View on the outside of the cloacal membrane. Genital walls are displaced laterally to
show the cloacal membrane. The urorectal fold/septum position is projected onto the cloacal
membrane by a stippled line (green). If the dorsal part of the cloaca is absent, the hindgut has to
end with its anal opening into the urogenital sinus (red arrow). If the genital tubercle outgrowth is
too heavy, the urogenital sinus has to end into the anal/hindgut area (red arrow)  E. Marani

factor proteins. The so-called hedgehog proteins ‘‘exert fundamental functions on


mesenchymal tissue in the posterior part of embryos’’ [12].
A member of the hedgehog proteins, called Sonic hedgehog (Shh), has to be
produced in the cloacal membrane to produce the future cloaca. The cloacal
membrane regulates, by hedgehog growth hormones, the genital tubercle, pelvic
urethra, and bladder epithelium, bladder smooth muscles, but also the genital
organs. The effects of these growth factors still have to be elucidated. We do know
that anorectal malformations are related to malfunction of the Shh protein growth
factor, but how this occurs is still target of research [12].

8.8 Surgery of Anorectal Malformations

During development, two structures are born: the anal structures and the rectal
structures that have to connect to each other to have an ending digestive tract. The
hindgut encompasses this development. Presumably very early in development,
the cause of malconnection is instigated. This malconnection can be severe ending
in no connections at all between anus and rectum or can be driven to connect the
rectum to other structures of the urogenital sinus. Such malconnections are termed
anorectal malformations. For the understanding of what happened to the surgery of
anorectal malformations, one has to look first into the history of embryology of
pelvic structures.
Let us start with Kaspar Friedrich Wolff (1733–1794) [1]. Trained as a medical
doctor, he was interested in embryology. He produced his thesis ‘‘Theoria Gen-
erations (Theory of generation or reproduction)’’ [14] at the Kaiser Wilhelm

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216 8 Development of the Pelvic Diaphragm and More

Academy for military surgeons. It is still considered an ‘‘outstanding contribution


to the field of embryology between the work of Malphigi (1628–1694) in the 17th
and Von Baer (1792–1875) in the 19th centuries’’ [17]. Due to the lack of interest
in plant and animal embryology in the scientific world, he could not find a job.
However, his reputation by the studies he had performed, reached Russia, where,
in 1746, Catherine the Great offered him a professorship in Anatomy and Physi-
ology in St Petersburg at the Russian Academy of Sciences. Here, he worked and
published several articles on the embryology of the chick [14].
Wolff showed that organs and limbs developed from undifferentiated tissue,
which is called epigenesis. Nowadays, a generally accepted fact, but in his time, he
had to fight the idea of preformation [15]. Preformation in essence defends that all
structures are already in ‘‘miniature’’ present in the embryo and these preformed
elements by organogenesis will lead into the mature structure. The exponent of
preformation was Von Haller (1708–1777), the well-known scientist, we already
met in Chap. 4 on history.
Wolff combined the studies of embryology in botany and zoology. Using the
microscope, with in that time still strong chromatic aberrations and no coloration
of the tissue, the plant seeds and plant embryos show cellular borders clearer than
uncolored animal tissue does. It is this combination that brought forward Wolff’s
epigenesis. In the chick, he described the nephrogenic tissue, the duct of Wolff,
and the developing ureter, which is a ‘‘tour de force’’ regarding the instruments he
had available. Moreover, he had to fight the preformationists with Haller at their
head. The intriguing correspondence between Haller and Wolff shows that Wolff’s
application of logic in the field of embryology supported his epigenetic philoso-
phy. Not earlier than by Von Baer (1792–1875), nearly 50 years after his death,
Wolff got the honors he deserved for his studies [15].
The scientist that solved the basic problems concerning the development of the
female genital system is Müller. Johannes Petrus Müller (1801–1858) graduated as
a medical doctor in 1822 at the University of Bonn. He became professor in
Anatomy at the same University and later on professor in Anatomy, Physiology
and Pathology at the University of Berlin. He also became editor of, what was later
called in honor of him, Müller’s Archive. Overloaded with prizes at the end of his
career, he also taught scientists like Meissner, Henle, Schwann, and Virchow,
respectively, known for sensory receptors in the skin, lis of Henle in the nephron,
cellular theory, and general pathology. Müller researched in different scientific
fields, always producing new results in anatomy, chemistry, psychology, pathol-
ogy, zoology, paleontology, and embryology. He discovered the paramesonephric
duct (still nowadays called duct of Müller) in the female chick, an additional duct
in the female that is responsible for the development of the uterus (see later) and
proved that the duct of Wolff only persisted in the male and degenerated in the
female [14].
In fact, after the work of Wolff and Müller, the basic pattern of the development
of the urogenital system was laid down. Refinement still proceeded through the
ages, especially the involvement of hormones and now the contribution of
genetics. Embryology and pathology of the system were extended by Retterer and

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8.8 Surgery of Anorectal Malformations 217

Tourneux (Fig. 8.9). Anorectal malformations were beautifully demonstrated


being caused by embryological malformations, although Retterer’s theories are
nowadays contested (see above). The development of the anal external sphincter
and the development of the levator ani were studied late [16], in fact the levator
ani’s total development not earlier than in 2006 [4].
Since anorectal malformations occur with an incidence of 1:1,500 till 1:5,000
(there are regional differences) most hospitals were confronted with this malfor-
mation [17]. Therefore, surgery for anorectal malformations started early. In those
cases where the rectum ended blind and no anus was present, an outlet was tried to
be constructed:

1693 Saviard tried to open a high closed bowl by plunging a trocar through the
perineum
1787 Bell opened via a dissection of the perineum high-ended bowels in two
children and created anus openings that constantly had to be kept free
1786 Mantell tried to operate on a recto-vaginal fistula
1793 Duret used the technique of Littre (sigmoid colostomy: connecting the
colon to the skin with an exterior skin opening, developed in 1710) for
anorectal malformations
1798 Martin of Lyon proposed a double operation: colostomy by which the bowl
could be pushed downward and consequently using a perineal approach
1856 Chassignac succeeded with the Martin of Lyon technique in two infants

Aseptic approaches were difficult especially in children in which the blindly


ending bowl was full of excrements that had to be removed first before any
operation could go on. Success rates of these operations were rather low. Even
from 1900 till 1945, the mortality was over 50 % [16, 18].
In between 1800 and 1950, the surgical approach developed several new
techniques: 1834 Roux of Brignols tried to spare the external anal sphincter but cut
through the whole levator ani and thus the sphincter, because the close levator-
sphincter relation was badly known by surgeons, although Vesalius pointed to the
relation, and later in 1724, Santorini (1681–1737) described extensively the anal
sphincters and the relation with the levator ani muscle in his Observationes
Anatomicae [16]. In 1835, Amussat carried out the first proctoplasty, the con-
nection of the rectum to the perineal skin. However, he used a large T-cut over the
perineum that destroyed the anal sphincter. One should note that the Amussat
procedure had a mortality rate over 60 %, but stayed the first choice of operation in
anorectal malformations [18].
Not earlier than 1930, the diagnostic means improved by the description of the
radiographic invertogram to determine the rectal atresia, because by high local-
izations, the atresia was difficult to find during the operation. Still, till 1950, the
importance of the anal sphincter and levator ani muscle by its functions was
surgically unknown.
In 1953 Stephens, a London surgeon, put emphasis on the levator ani, but
minimalized the importance of the sphincters. In 1959 in Germany and in 1960 in

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218 8 Development of the Pelvic Diaphragm and More

Italy, variations or renewed approaches were published. Nevertheless, inconti-


nence stayed the most important problem and was thought to be due to the absence
of sphincteric function [18].
It lasted till 1961 before the importance of the presence of an external sphincter
was recognized. In nearly all anorectal malformations, the external sphincters are
still present with a variable functionality, which was a surprising finding for the
surgeons [16]. Still choices were made in favor of the levator ani, in the mean time
destructing the existing sphincter. The levator ani part bordering the external
sphincter, called puborectalis, should produce the sphincter function. Moreover till
1980, the reported results were subjective and not standardized, although several
reports were published and their comparison difficult of course [18]. Anorectal
malformations were finally internationally subdivided (1984, Wingspread classi-
fication) in: high-located, intermediate, and low-pelvic-located anomalies [18].
Certain malformations were no longer grouped under the anorectal ones,
decreasing the reservoir of pelvic anorectal deflections till then reduced to the
same denominator.
Thus till the 1980s, embryological results, together with the anatomical struc-
ture of the pelvic diaphragm and pelvic sphincters were not taken into account in
the anorectal malformation operations.
We owe to Pieter A. de Vries that embryology of the pelvic structures came
within the attention of the pediatric surgeons in the 1960s and 1970s, and con-
sequently, attention was given to the interrelation between anal sphincters and
levator ani muscles. His studies on the development of the pelvic diaphragm
showed ‘‘that normally the external sphincter and levator musculature become
identifiable at the same stage of development and are associated from the start’’
[16]. Moreover restricted anorectoplasties ‘‘appeared to confirm an opinion arrived
at by clinical, embryologic, and pathologic studies on the relationship of the
external sphincter to the levators, namely in anorectal anomalies, the external
sphincter is not, in fact, absent or necessarily deficient, but rather, like the
puborectalis, is altered in its configuration and relationships to the terminal bowel
when there is a deficient anal canal. Findings in subsequent female patients with
vulvar fistulas and in males with anocutaneous fistulas have further confirmed this
view. In these patients, the sphincter ani externus is largely or totally dorsal to the
fistula’’ [16]. So Pieter de Vries underlines the integrity of external anal sphincter
and the levator ani muscles. Then, something odd happens. In stead of trying to
keep the integrity of these fused structures, he together with Alberto Peňa,
introduced a perineal approach, in which both sphincter and levator ani muscles
are cut midsagittally: the resurrection of a 150 years earlier developed technique
by Roux of Brignols. This dissection is used in those cases in which higher rectal
defects are present: ‘‘The higher rectal defects were noted to have a wider sepa-
ration between the subcutaneous and superficial external anal sphincter and the
latter muscle from the levators. De Vries and Peňa completely divided all the
muscles posteriorly in the midline from the anal dimple to the coccyx. They
divided the rectourethral fistula from within the atretic segment by separating the
mucosa and smooth muscle to avoid urethral and neural damage. The distal atretic

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8.8 Surgery of Anorectal Malformations 219

segment was tampered to fit within the puborectalis and the divided muscles were
sutured posteriorly around and to the neorectum prior to performing the anoplasty.
Slight tension was placed on the anoplasty site to draw the skin in and avoid
prolapse’’ [18]. This operation is called posterior sagittal anorectoplasty (PSARP)
and ‘‘was a new landmark event in the history of anorectal malformations… and
was rapidly adopted by many pediatric surgeons throughout the world’’ [18].
Rintala gave the functional outcome during childhood for high malformations
before and after the era of PSARP. Point is that the tables are hard to compare.
However, the column of good results before the PSARP era shows 31 % measured
in a population of 204 patients. The PSARP era shows a total continence in 26 %
of a population of 65 patients [19].
Holschneider gives for 1962–1984 (before PSARP) a continence percentage of
13 % on 159 patients and for 1989–1997 (after PSARP introduction) 20 % con-
tinence in a population of 41 patients for the high malformations [19]. Since the
PSARP was developed for high-located malformations, the results are poor.
Nevertheless, it should be noted that after introduction of the PSARP technique,
increase in continence is noted for the intermediate (from 10 to 42 %; n = 33 and
36, respectively) and low malformations (67–76 %; n = 189 and 56, respectively)
[19]. Recently some modification of these results has been published, diminishing
the percentage of success rate of restoring low malformations in children toward
50–60 % [21]. Besides, mortality rate was reduced to 3–4 % of the operated cases.
The next approach that has been developed is the laparoscopy-assisted anorectal
pull-through operation [20]. The sphincter-levator ani complex can be kept
unimpaired, fistula closed and the rectum connected at the transition of levator ani
sphincter externus. The comparison between the classical PSARP (n = 13) and the
laparoscopy pull-through technique (n = 9) showed that the PSARP operation
produced greater sphincter asymmetry and sphincter irregularity, a greater occur-
rence of megarectum and constipation. Eight of the 9 laproscopic-treated patients
had an anorectal reflex, while only 4 out of the 13 PSARP patients [20]. One can bet
on the future better results of the laproscopic approach, since the sphincter–levator
ani complex will be unharmed, the ultimate consequence of the embryologic
studies, with the corollary of a functioning outlet system for the rectum.
Transanal repair, called transanorectoplasty or transanoproctoplasty, is the logic
consequence of the reasoning described above. It was developed by Adrian
Bianchi around the 1990s [20]. Although the method can be applied in most forms
of imperforate anus, only a few publications do recognize the method. Using
electro stimulation, the place of the anal sphincter is localized and freed from
surrounding tissue. Fistulae are dissected and the rectum mobilized so it can be
rerouted through the anal canal that is newly formed by anastomosing the perianal
skin. The front of the rectal wall and pelvic floor together with the perineal
muscles are apposed and the vulva is reconstructed. Transanoproctoplasty has been
carried out in 245 patients and the results show a limited morbidity. ‘‘It is sphincter
sparing and permits accurate placement of the rectum with its internal sphincter
within the anal canal. The anus lies accurately placed at the center of the external
anal sphincter muscle complex’’ [20A].

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220 8 Development of the Pelvic Diaphragm and More

8.9 The Development of the External Urethral Sphincter

Micturition problems and urine incontinence are also strongly related with the
function of the striated external urethral sphincter. Urine incontinence is frequently
encountered in women. We will come back to the external urethral sphincter in
Chap. 19 and restrict our self here to its development. Understanding of the
development of this striated urethral sphincter is a necessary prerequisite to realize
its consequences for the mature situation. It seems strange, but the lead is the male
external urethral sphincter, because the difference between male and female
sphincter gets the picture of possible malfunction.
The external urethral sphincter is during its development in close relation to the
levator ani muscle [4, 7, 8]. Gender differences are present and play a role in the
research outcome (Fig. 8.11).

Fig. 8.11 Left ‘‘The external urethral sphincter (EUS) and internal urethral sphincter (IUS) in a
male fetus (12 week of gestation). Three-dimensional reconstruction in (a) anterior view,
(b) posterior view. The EUS is shown in blue, and the IUS is shown in pink. The urethra and
prostate are shown in light gray’’ [8]. Right the female position. Lower left figure is a
reconstruction of 22 week of gestation. Note the increase in circular closure of the EUS. Right
The external urethral sphincter (EUS) in a female fetus (12 week of gestation). Three-
dimensional reconstruction of the EUS (blue) in (a) anterior view, (b) posterior view and
(c) 18 week of gestation. Note the open back side of the female EUS [8] (Figures reproduced with
permission from Wallner [8] parts 1A and B, 2A and B, 3 A and B, 4C)

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8.9 The Development of the External Urethral Sphincter 221

One should know that in man at the backside (posterior), a strip of connective
tissue is present along the developing urethra, a so-called raphe, in which striated
fibers of the external urethral sphincter insert, as more caudal fibers do into the
centrum tendineum [7]. The striated muscle fibers are circular, and in man,
the ventral side of the prostrate is covered with half circular fibers that insert into
the prostate capsule (Fig. 8.11). Only in a few instances (at 22 weeks of gestation
[8]), the raphe is also occupied with these striated fibers, producing a real circular
muscular system [7, 8]. One could compare this structure alongside the urethra to a
flexible garotting-post. Contraction of the external urethral sphincter closes over a
distance the urethra.
In females, the situation is different; the external urethral sphincter does not
surround the whole urethra (Fig. 8.11), since the vagina descends along the urethra
(Fig. 8.12). A strip is kept open for the passing vagina (Fig. 8.12). Although clear
pictures are given here, we will see in Chap. 19 that some misunderstanding still is
present.

Fig. 8.12 ‘‘Development of the vagina, urethra, and external urethral sphincter (EUS) in the
female fetus. Three-dimensional (3D) reconstructions in right-lateral views of the urethra (light
gray), vagina (purple), and EUS (blue) of female fetuses of (a) 12 weeks, (b) 14 weeks, and
(c) 18 weeks of gestation. Note that the vagina opens into the urethra relatively superior in the 12-
week fetus (a) but more inferiorly in the 14-week fetus (b). In the 20-week fetus, the vagina has a
separate opening from the urethra into the vaginal vestibule (c). Due to this developmental
process of the vagina, the vagina grows between the lateral portions of the inferior part of the
EUS, thereby making it impossible that the EUS only surrounds the urethra, as it does in the male.
Note that the 3D reconstructions of the different fetuses have been scaled to equal size. Figure and
text are reproduced with permission from Wallner Fig. 5A, B, and C’’ [8]

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222 8 Development of the Pelvic Diaphragm and More

8.10 Earliest Characteristics of Human Pelvic


Development

Within the early embryo, two new structures are born that expand its development.
They stay not inherently within the three layers (ectoderm, mesoderm and endo-
derm) that build up structures. They are the neural crest and the placode. The neural
crest develops from the neural tube and the placode organizes itself below skin areas.
Let us start with a romantic description on neural crest cells as given by Leroi
[22B]: ‘‘At about day 28 after conception, neural crest cells flow out of the newly
formed dorsal nerve cord and pour themselves around the fetal head to make the
face. But some neural crest cells travel much further than this. As a river fans out
over its delta, streams of neural crest cells course down from the escarpment of the
dorsal nerve cord and penetrate to the embryo’s farthest reaches.’’
Novel results are responsible for another look on the development of internal
structures. Fusion of swellings and luminization of tubular structures together with
apoptosis marks these new developments [6, 22A]. What is more, the directly
below the skin produced ectodermal–mesothelial cells, overcome long cell
migration pathways in mammalians. Places where such cells are produced are
called placodes that are, beside in the head, also present in the leg, pelvic, and tail
area (Fig. 8.13) [22].
Placodes are specialized transient parts of the columnar, pseudostratified sur-
face ectoderm, later epithelia that are capable of adding their cells to the mesoderm
compartment. They add their cells in the head region to sensory ganglia, producing
neurons and other types of cells for the special sense organs [22], but intervene
also in other regions of the embryo.
Placodal cells are induced very early, already at the edge of the neural plate at
the first somite stage in the chick, marked by Six, Eya, Id, Iro, and Fox genes, but
the dispersed cells have to sort out and group together to produce placodes.

Fig. 8.13 Placode and neural crest areas in the developing rodent (Reconstruction made from
Smits van Prooije [22], results, in our Neuroregulation group). Yellow central nervous system, red
and green neural crest contributions for cranial and spinal ganglia, blue limb placode and tail
placodes. Note that spinal ganglia (red) are mainly derived from neural crest cells

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8.10 Earliest Characteristics of Human Pelvic Development 223

Inductors of placode cells are endoderm, future heart mesoderm, and the neural
plate. A role is played by bone morphogenic proteins (BMP’s) as marker of the
border of the neural plate, and Iro-1 is regulated by BMP. Sox, Dlx, Fox, and Pax
genes are involved in determining placode cells. Only the transcripts Six and Eya
are ‘‘to be maintained in all developing placodes, while being lost from inter-
placodal domains’’ [23]. A clear genetic cascade is responsible for the generation
of placode cells.
Using lectin-coated colloidal gold, Smits van Prooije succeeded in 1986 to give
a total overview of the combined localization of the neural crest and placode cells
in the rat from the 5 till 41 somite stages, confirming earlier ‘‘partial’’ results in
chickens and mouse. The massive presence of labeled cells in the branchial arches
and limb bud shows the importance of the contribution of these placodal cells to
the development of the embryo and even fetus (Fig. 8.13) [22].
The migration routes are thought to contain extracellular matrix proteins like
fibronectin, laminin, and collagen that are capable to direct migration. These
pathways are unspecific highways, since these proteins can hardly be kept
responsible for homing of the migrating cells. Attracting and repellent factors are
discerned for homing the neural crest cells. Factors like glial-derived neurotrophic
factor and netrin/deleted colon cancer gene are now established as neural crest
attractants especially in the gut [24]. As good as we know now the neural crest
high ways, as bad we know the pelvic placodal migration ways. They contribute to
pelvic bony structures and to tail structures, but how, a mystery stays. The human
tail itself is an underexposed phenomenon: In week 6–8, a tail is present in the
human embryo containing around 10 vertebrae. It disappears at week 8 by
reduction and fusion, leaving the vestigial coccyx. Cell degeneration is caused by
apoptosis and necrosis. Sometimes, the true vestigial tail is persistent till
week 22–23 after gestation. This tail is an elongation of the coccygeal vertebrae
[25]. (By the way, the name coccyx is from the Greek word for cuckoo bird. Why,
is unknown? [26]) Placodes are suspected to contribute not only to the tail and the
bony pelvis but also to the urogenital apparatus and the digestive tract. But what
their involvement is in these structures stays also vague. As a consequence, most
malformations cannot be related to the earliest embryonic human development, but
that an early genetic malcomponent is present, is proven by the genetic engi-
neering of experimental animals.

8.11 The Development of Higher Bladder Steering


Centers

In Sect. 8.10, one noticed that the earliest development of peripheral neural
structures is still in its pelvic infancy. Therefore, a relation between peripheral and
central neural systems during early development is hard to make [27].
Various structures in the brainstem are held responsible for the control of
bladder and urethra and sphincters. In rats, the mother licks their puppy’s perineal

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224 8 Development of the Pelvic Diaphragm and More

region to induce defecation and urination. This system is not needed during the
fetal period. Therefore, the central neuronal system has to be organized just prior
to birth. Two higher control centers are known for their connection with the lower
spinal cord, where the sympathetic and parasympathetic system connected to
bladder and urethra, and to rectum and anus, are localized.
One center is known as the TLD (nucleus tegmento-latero-dorsalis), which lies
just below the fourth brain ventricle (Fig. 8.14 upper part). At embryonic day 17
(the in-utero development of the rat lasts 21–22 days), the first fibers are already
descended to the thoracic spinal cord, and before embryonic day 20, they have
arrived at the sacral spinal cord (Fig. 8.14) together with a mysterious system that
descends and destructs its connection later on (see Fig. 8.14). These TLD fibers do
contact Onuf’s nucleus and the sacral parasympathetic nucleus. The loop perineal
sensory activation—brainstem nucleus—of the motoneurons of Onuf’s and para-
sympathetic nucleus is called the spinal–bulbospinal reflex. This reflex is func-
tional at the second postnatal day [27].
The other system concerns the connection of the nucleus paraventricularis (a
hypothalamic nucleus) with the sacral spinal cord. These fibers are present at the
thoracic level at embryonic day 18/19 and reach the sacral spinal cord between
embryonic day 21 and postnatal day 1. The nucleus paraventricularis projects to
the sympathetic nucleus laying at the thoracic spinal cord level, and parasympathic
nuclei [27].
Thus around birth, the spinal–bulbospinal reflex is organized and is functional
directly after birth. In rats, the steering of the bladder, urethra, and its sphincter,
and of the rectum and anus, is regulated by licking of the perineal region by the
mother, which is needed to keep the nest hygienic.
Children in their first years of life are incontinent for urine and feces. Emptying
and filling is a pure reflex: after filling of the bladder, emptying occurs automat-
ically independent of time and place.
Unlike rats, in humans, the spinal–bulbospinal reflex starts working only at two
to three years of age. This means that cortical influence on this reflex loop will
be developed afterward, since the corticobulbar steering needs a working
spinal–bulbospinal reflex. Children have to learn to control the lower urinary tract,
which means having cortical steering of it. This learning process involves: feeling
the filled bladder, consciousness of the need of emptying, continence for urine, the
inducing of emptying totally the bladder, and regulating a normal frequency of
voiding. This complex process is learned without training and it is amazing that
most children are successful in learning to control this process.
Coordination is organized at the brainstem level, while conscious influence on
urination is a process of the brain cortex. The learning process follows two main
stages: by consciously closing the striated sphincter, the induced reflex will sup-
press the bladder contraction. Later on, the cortical function develops and children
learn to inhibit the micturition reflex and to void at a place and time of choice.
Training can help to increase the speed of learning.

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8.11 The Development of Higher Bladder Steering Centers 225

Fig. 8.14 Upper part shows a transversal section in which the rat nucleus tegmentalis
laterodorsalis, with in its center Barrington’s nucleus, is indicated by a white line. The lower
figure shows that injections in the spinal cord labels around birth the nucleus tegmentalis
laterodorsalis, indicating that the structural organization for spinal–bulbospinal reflex is ready
just before birth (figures courtesy Dr. E. A. J. F. Lakke)

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226 8 Development of the Pelvic Diaphragm and More

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mesoderm and mesectoderm in 5- to 41-somite rat embryos cultured in vitro, using WGA-
Au as a marker. Anat Embryol 177:245–256; Rickmann F, Fawcett WJ, Keynes RJ (1985)
The migration of neural crest cells and the growth of motor axons through the rostral half
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radioautographic analysis of the migration and localization of trunk neural crest cells in
the chick. Develop Biol 6:279–310
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Rapahel B (1983) Cerebro-craniofacial and craniofacial malformations: an embryological
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Chapter 9
Physiotherapy for Pelvic Muscles

Physiotherapeutic training of the pelvic diaphragm is prescribed for urine and fecal
incontinence in most Western countries. Strange enough convincing proof by a
double-blind randomized trial is missing. A new technique is trigger-point treat-
ment for pelvic pain. This method obtained hardly any positive evidence and
caused dispute between those in favor of the method and those against thinking it
is quackery. Anatomy shows that the pelvic diaphragm is different in incontinent
females and that training changes the pelvic diaphragm, despite absence of con-
vincing physiotherapeutic trials.

9.1 Introduction

The Netherlands is one of the few countries where child birth at home is still
regulgularly done. In the nineteenth century and start of the twentieth century,
hospital infections for the mother, known as puerperal fever, and of the newborn
baby were low simply because few pregnant women went to a clinic. Birth stayed
a family event in the Netherlands, supported by the population, clinicians, and
midwives. The amount of maternity clinics in the Netherlands grew not earlier
than in the 1930s rather late after the Semmelweis infection discussion that lasted
till 1900. This was in contrast to other European countries. Midwifery was
important, and the assistant–midwife was recognized by law together with
demands for her education in 1925, replacing the dry nurse and increasing hygiene
and feeding, the main cause of death of the baby at home [1].
In 1908, ‘‘De Bond ter Bescherming van Zuigelingen’’ (League for the Pro-
tection of Sucklings) was already erected, and in 1941, most of the Dutch popu-
lation was insured for diseases by law. Both trends, the private and official ones,
melted, and in 1943, labor care was organized into infant welfare centers that are
functional both in the prelabor and in the postlabor phases, but in that time still on
a semivoluntary base. Note that the important steps to create the Dutch infant
welfare centers occurred in the midst of the Second World War.

E. Marani and W. F.R.M. Koch, The Pelvis, 229


DOI: 10.1007/978-3-642-40006-3_9,  Springer-Verlag Berlin Heidelberg 2014

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230 9 Physiotherapy for Pelvic Muscles

Support for pregnant women was organized in the Netherlands directly after
World War II and directed toward information and exercises to prevent pain and
anxiety at child birth. During time, these exercises developed from the prevention
of pain and anxiety into a good bodily condition of the mother, because a sound
state would help the mother to endure better her pregnancy, labor, and her
childbed.
The physiotherapists involved in these courses erected the ‘‘Study Group for
Pre and Postnatal Education’’ in 1964. By law (1967), these courses on maternity
exercises were incorporated in the Dutch health care insurance. From then on, the
administration of diseases related to labor was centrally organized and postpartum
pelvic floor problems came better into view. The attention for postpartum pelvic
floor problems smoothly went into the awareness of pelvic floor problems in
women in general. The Rotterdam hospital Dijkzigt (later Rotterdam University
Medical Center of the Erasmus University) started physiotherapeutic courses for
the pelvic floor. They were initiated by the medical staff and organized and carried
out by Evelien Versprille-Fisher (1934–2010), who was originally responsible for
the labor courses in the same hospital. The physiotherapists who concentrated on
pelvic floor and labor problems organized ‘‘The Dutch Society for Pelvic Problems
and Pre and Postpartum Health Care’’ (1994). It was the start (1996) for physio-
therapeutic postmaster courses in this field and the foundation of a specialization
by a master ‘‘pelvic floor’’ (started in 2003 and initiated by Marijke Slieker-ten
Hove). Finally, the Dutch physiotherapeutic care for the pelvic floor matured. It
lasted over 70 years before law, insurances, and education were well based in this
discipline in the Netherlands.
The history in the UK is nearly the same but earlier: first ‘‘exercises for women
in the maternity ward’’ [1A] by Miss Randal in 1912 and in 1936 the exercises for
the pelvic floor muscles by Morris. The Obstetric Physiotherapists Association was
erected in 1948 [1A].
This history shows the social intimate relation between maternal and elderly
pelvic floor problems. The question, nevertheless, is what did this expansion of
Dutch physiotherapy generate in terms of pelvic problem solutions?
A complete overview of physiotherapeutic methods as applied for pelvic floor
dysfunctions is not possible in our brief space. The few cases are from Dutch
approaches published and supported by the Royal Dutch Association for Physio-
therapy and adopted form Evelien Versprille Fisher’s book [2], honorary member
of this association, being the start of literature reviews. Physiotherapeutes call
incontinence training pelvic floor training, but it is of course pelvic diaphragm
training. In this chapter, we follow their terminology anyhow. The other ana-
tomical point to make is that in the standing position, the urogenital diaphragm
and pubic bones support most of the pelvic organs not the pelvic diaphragm (see
Chaps. 1 and 7).

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9.2 Physiotherapy for Pelvic Floor Dysfunctions 231

9.2 Physiotherapy for Pelvic Floor Dysfunctions

9.2.1 Toilet Behavior

During obstipation, but also throughout miction problems, the position on the toilet
is important. Sitting is normal during defecation; one brings the normally hori-
zontal rectum into a vertical position. However, by keeping a more effective,
vertical position (see Fig. 9.1), defecation can be supported and better regulated.
Here, a simple approach, a bulging back, helps to bring the pressure on the rectum
in the correct direction, while a hollow back brings the bladder and urethra to that
position. It is the pelvic position that determines the effectiveness of miction and
defecation due to hollowing or bending the back, respectively [2].
‘‘There is a clear link between constipation and optimal functioning of the
urinary system, such that coexisting bladder and bowel disorders have become
known as ‘‘the dysfunctional elimination syndrome’’ [3]. Toilet habits are already
‘‘learned’’ during childhood, and incorrect habits have to be corrected, especially
in children with obstipation.’’ Correction of toileting posture to ensure a forward,
leaning sitting position with comfortable buttock support, thoracic and lumbar
spine extension, hip abduction and appropriate foot support that permits 90 of hip/
knee flexion is crucial. Learning to increase intraabdominal pressure by using
abdominal muscles other than the rectus abdominis, while at the same time
releasing the anal sphincter, can facilitate defecation. It is preferable for a child to

Fig. 9.1 a Position of the


bladder and rectum at
Miction Defecation
different positions of the
pelvis by changing the (a)
posture of the back. b View
of the sitting position on the
toilet (reproduced with
permission from Versprille-
Fischer [2])

(b)

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232 9 Physiotherapy for Pelvic Muscles

Fig. 9.2 Muscles around the


pelvic–abdominal cavity
involved in spinal stability,
intraabdominal pressure, and
continence, from Continence
and Women’s Health Group,
Australian Physiotherapy
Association, Western
Australia. Reproduced with
permission from Continence
and Women’s Health Group,
Sapsford [4]

learn effective recruitment and relaxation of structures as a means of attempting


defecation or completing rectal emptying than to simply sit on the toilet and wait
or to resort to Valsalva maneuvers, which elicit anal closure [3].
The cited text also shows that both the vertebral column and the abdominal
muscles play an important role, and later, we will see that respiration is also
involved, which concerns the diaphragm (Fig. 9.2).

9.2.1.1 Trunk Stabilization and Abdominal Muscles

‘‘In essence the passive human spine is an unstable structure and therefore further
stabilization is provided by the activity of the trunk muscles. These muscles are
often referred to (…) as the ‘‘core’’ muscles, assuming that there is a distinct
group, with anatomical and functional characteristics specifically designed to
provide for the stability. One of the muscles in this group to have received much
focus is the transversus abdominis muscle. It is widely believed that this muscle is
the main anterior component of trunk stabilization. It is now accepted that many
different muscles of the trunk contribute to stability and that their action may
change according to varying tasks’’ [5]. Low back pain is explained by the
instability of the vertebral column that is surmounted by trunk muscle exercises,
especially the transversus abdominis. Thus, exercises can strengthen the trunk
muscles, and low back pain will be overcome. The consequences are that ‘‘a whole
industry grew out of these studies with gyms and clinics worldwide teaching the
‘‘tummy tuck’’ and trunk bracing exercise to athletes for prevention of injury and
to patients as a cure for lower back pain’’ [5]. The critical review from which the
above citations are taken is destructive for the gym and clinic assumptions to
release back pain. Moreover, the conclusion for the abdominal muscles is that they

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9.2 Physiotherapy for Pelvic Floor Dysfunctions 233

contribute less than supposed to spinal stability: ‘‘abdominal musculature can


demonstrate dramatic physiological changes, such as during pregnancy, post-
partum and obesity, with no detriment to spinal stability and health. Damage to
abdominal musculature does not seem to be detrimental to spinal stability or
contribute to low back pain’’ [5]. Therefore, publications on abdominal muscles
and trunk stability should be read with care.
Manual therapy started to apply techniques that could strengthen the core
abdominal muscles with the consequence that the physiotherapeutic approach of
incontinence should be changed or new techniques should be added. ‘‘Research
has led to an increased understanding of the synergy between the abdominal and
pelvic floor muscles and in fact all the muscle groups surrounding the abdominal
capsule. The pelvic floor muscles are now considered to have the dual function of
providing trunk stability and contributing to continence and elimination of both
bladder and bowel’’ [6].
Trunk stability is now related to the pelvic floor muscles and abdominal
muscles. After small contractions of the pelvic floor muscles, reactions in the
transversus abdominis are noted. Alterations in position and function of abdominal
muscles coincide with pelvic floor muscle changes. Intraabdominal pressure
modifications like during laughing, sneezing, and coughing involves both
abdominal–pelvic floor muscles and the diaphragm. The new physiotherapeutic/
manual therapy approach for stress urine incontinence contains the following:
reeducation of diaphragmatic breathing and increase in the tonic activity of the
pelvic floor muscles: ‘‘Using an independent transverse abdominis contraction to
gain a pelvic floor muscle co-contraction helps to ensure the very low-level pelvic
floor muscles activation required’’ [6] and muscle strengthening with retraining of
laughing, sneezing, and coughing.
However, criticism on the tummy tuck approach is basic. ‘‘The control of the
trunk (and body) is whole. There is no evidence that there are core muscles that
work independently from other trunk muscle during normal functional movement.
There is no evidence that individuals can effectively learn to specifically activate
one muscle group independently of all other trunk muscles’’ [5]. At least, these
statements are supported by physiological results that show that the transverse
abdominis and the internal oblique muscles cannot function separately and in most
cases, the abdominal muscles must act as an entirely [7]. Both muscles have a
conjoint tendon with seemingly conjoint receptors for mechanical properties. It
therefore seems unwarranted to ask a patient to only activate tonically or
strengthen solely one of the abdominal muscles. Harm can hardly be done since,
‘‘Core stability exercise (that is, among others, activating solely the transverse
abdominal muscle, addition ours) is no better than other forms of manual or
physical therapy or general exercise. Find out what exercise the patient enjoys and
add it to the management plan’’ [5], and ‘‘So why give the patient complex
exercise regimes that will both be expensive and difficult to maintain? Perhaps our
patients should be encouraged to maintain their own preferred exercise regime or
provide them with exercises that they are more likely to enjoy. This of course
could include Core stability exercise. But the patient should be informed that it is

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234 9 Physiotherapy for Pelvic Muscles

Fig. 9.3 Resistance training


for pelvic floor muscles. By
the exorotation–abduction
and anteflexion movements
together with crawling
forward on the elbows, the
pelvic floor muscles are
tightened. Contra force at the
ankles increases the effect,
(reproduced with permission
from Versprille-Fischer [2])

only as effective as any other exercise’’ [5]. Does the last statement also hold for
the ‘‘abdominal derivative of stress urine incontinence’’: the pelvic floor muscles?

9.2.1.2 The Other Way Around: Pelvic Floor Muscles

Physiotherapy knows a series of simple trainings that are helpful to increase pelvic
floor muscle function, of which one is exemplified in Fig. 9.3. Most attention goes
to women for strengthening the pelvic floor muscles in stress urine incontinence,
but in males, after a prostatectomy stress, urine incontinence is also present and is
rather under exposed in the literature. Moreover, pelvic floor training is also
applied in children with nocturnal enuresis.
Let us start with bed-wetting by children. An accepted therapy is full spectrum
therapy. ‘‘Full spectrum therapy is a combination of alarm, reward, timed voiding
and drinking, over learning and pelvic floor muscle training’’ [8]. The contribution
of each of the parameters to success is unknown, and therefore, prospective ran-
domized studies are carried out. In a group of 63 children, 32 got pelvic floor
training in their therapy and 31 obtained the same therapy without pelvic floor

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9.2 Physiotherapy for Pelvic Floor Dysfunctions 235

training. Children with infection or anatomical or organic problems were excluded.


The outcome was ‘‘There is no beneficial effect of including pelvic floor muscle
training in full spectrum therapy. Older children and those with better motivation
experienced more rapid success. Factors predicting relapse were secondary
enuresis and psychosocial problems’’ [8]. Seemingly, a good motivation helps, and
psychosocial problems should be fought, not the pelvic floor.
Men who had a prostatectomy can get urine incontinence. However, till
recently, no acceptable overview of the in and outs of this incontinence was
available. It was known that directly after radical prostatectomy, nearly 90 % of
the men had urine incontinence complaints, while directly after transurethral
resection for benign hypertrophy of the prostate, this figure is 65 % [9, 10]. To get
more insight, the University of Aberdeen, supported by the National Health Ser-
vice, started the project MAPS: ‘‘Men After Prostate Surgery’’. The next statement
is from the introduction article for their trials: ‘‘Some physiotherapists treat these
men with pelvic floor muscle training and urge suppression techniques despite a
recent Cochrane review concluding that there is insufficient evidence to show
whether or not they are effective’’ [9]. Thus pelvic floor training is questionable in
these cases. The outcome of the double trial (radical prostatectomy and transu-
rethral resection of the prostate) for pelvic floor training is surprising. A one-to-
one introduction and checking by a physiotherapist has no more value than
instruction on paper, leaflets, and other written information. The article touched a
sensitive spot. The more so as the trial found higher percentages of the stress urine
incontinence due to the operation, while other publications indicated a far lower
percentage. After a year, still 75–77 % of the patients had urine incontinence of
which 38–40 % had a severe incontinence, and no difference was found between
pelvic floor treatment and controls. The same holds for transurethral resection:
after a year 62–65 % with severe cases up to 24 % [10]. Since the large Cochrane
overview [11] doubts the effectiveness of pelvic floor exercises in men, real doubt
exists on pelvic floor training to overcome urine incontinence after prostate
surgery.
Female pelvic floor training is in the short term thought beneficial to reduce
urine incontinence both postpartum and in elderly women [12, 13]. Condition is
that at least a three-month training period is performed and the training, supervised
by a physiotherapist, produces better results for stress and mixed urine inconti-
nence than written instructions. It is the first-line approach for urine incontinence
in females. Some articles indicate that pelvic floor muscle training is also bene-
ficial for urge incontinence. Nevertheless, the long-term follow-up effect is not
established as indicated by most papers [13, 14] and references herein.
There is basic criticism: ‘‘However, few women are wholly continent after
pelvic floor muscle training; 75–95 % are not dry. Despite this, a significant
proportion of patients are reasonably satisfied, e.g., almost half of patients in a
study by Lamers and van der Vaart [14] were satisfied despite 95 % having some
degree of leakage’’ [14A], see also [14]. Surgical approaches by mid-urethral
tension-free vaginal tapes claim at a follow-up of up to 8 years that 80 % of
patients are cured of stress urine incontinence [15].

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236 9 Physiotherapy for Pelvic Muscles

The results for pelvic floor muscle training are distressing: it does not work in
children for bed-wetting and probably not in men. While, in females, it is claimed
to work, still over 90 % of the females are leaking. And, of course, there is
discussion on the definition of leakage and the measurement of urine loss.
Restriction of the definition and measurements give a better outcome, which is
pleasing physiotherapy.

9.3 The Wise-Anderson Method

In their book ‘‘A headache in the pelvis: A new understanding and treatment for
chronic pain syndromes’’, David Wise and Rodney Anderson introduced a dif-
ferent medical approach for pelvic and low abdominal pain. The front cover
contains support by Erik Peper, author of ‘‘Make Health Happen’’ with the sen-
tences: ‘‘This is the book to read before you contemplate surgery, drugs or resign
yourself to continue to suffer with chronic pelvic pain. Return to health is possi-
ble’’ [16]. The book contains a lot shoutology like: ‘‘The language of a painful
pelvis can be difficult to decipher unless you listen carefully and want to under-
stand its language’’ and ‘‘Patients with pelvic pain that doctors cannot help do best
when they become their own advocates and navigate their way through the
bewildering world of treatments for pelvic pain using their common sense and
intuition’’, followed by ‘‘Most people we have helped have come to us through
their own research’’ [16]. The first part of the book contains a setoff against regular
medicine and a becoming conscious of an alternative method to relieve pelvic
pain. In favor is that the shoutology within the text can be helpful, since the text is
made for non-medical trained patients of all social layers, but also overdoes it [16].
The setup of these critics in the book is analogous to the critics homeopathy
brought up against regular medicine. It has the consequences that it is considered a
real or potential threat by regular medicine, which will start a combat against the
alternative method. Indeed, in a way, that happened: started at Stanford,
‘‘removed’’ from Stanford, accused of manipulation of Wikipedia and positive
advertisements of patients, call it and one can find it, especially on the Web. Put in
Wise-Anderson method and one will find criticism, accusations by videos and
spoken text, and comparisons of text fragments of the book, and the positive
advertisements of patients, indicating fraud. The economic aspects like buying a
tape needed for the method or one has to visit for several days a clinic indoors to
learn the method are left out here, although money making is one of the arguments
of opponents. It must be clear that one is skating over thin ice if judging the in
origin physiotherapeutic technique. In advance, the Wise-Anderson method is here
arbitrated by its anatomy, physiology, quality of the published outcomes, and
therapy of the method; all other arguments are loaded in the author’s opinion.

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9.3 The Wise-Anderson Method 237

9.3.1 Anatomy Related to the Wise-Anderson Therapy

The system is based on so-called pelvic floor internal and external trigger points
that are related to pain sensations. The idea and the external muscle diagnosis is
taken from Travell and Simons [17]. The detection of trigger points, as explained
in the book, is summarized here. The internal ones have to be targeted by a rectal
approach and concern the levator ani muscle, anterior middle and posterior por-
tion, the coccygeus, the sphincter ani, prostate, piriformis, obturator internus, and
the coccyx. In fact, the whole pelvic diaphragm is checked for trigger points.
External trigger points concern the muscles: adductor magnus, bulbospongiosis
and ischiocavernosus, quadratus lumborum, gluteus maximus, medius and mini-
mus, iliopsoas, lateral abdominals oblique, paraspinals and multifidi, pectineus,
and pyramidalis. Thus, muscles related to the thigh are externally checked for
trigger points by pain sensations. To each muscle, text or figures explain the
belonging pain sensation. The underlying anatomy for diagnosis is sound. Causes
for the occurrence of trigger points are seemingly unclear, but ‘‘labors who
exercise their muscles heavily every day are less likely to develop active trigger
points than sedentary workers who are prone to intermittent orgies of vigorous
physical activity’’ [17]. The text includes that latent trigger points are also present
that indeed are described.
The difficulty is do trigger points exist? In other words, do they have anatomical
or histological foundations? Trigger points are characterized as dysfunctional
endplate regions as the prime site, which extend to small tender muscular dys-
functional nodules that have small, taut strips of concentrated muscle fibers from
the center to each end of the muscle’s ligament. Trigger points, it is claimed, can
be detected with needle and surface electromyography and ultrasound techniques.
Topography of trigger points has been described, and maps are produced [17]. The
surprising fact is that they overlap with acupuncture points along meridians [18].
For the first time, this correlation was found by Melzack, the well-known pain
scientist. From then on, a series of anecdotal acupuncture results are published
concerning this correlation with single and double-blind randomized studies.
Acupuncture points are declared cutaneous spots in the healthy skin [18A], while
trigger points are muscular deviations from a normal muscular structure, but their
relation is unclear.

9.3.2 Physiology Related to the Wise-Anderson Therapy

There are three main theories to explain the trigger points: energy crisis hypoth-
esis, motor endplate hypothesis, and the radiculopathic model for muscular pain
[19]. The energy hypothesis contains that extramuscular activity by neuronal input
or trauma asks for extra calcium release and prolonged shortening of the muscle
fibers. This prolonged shortening disturbs the blood circulation. It results in

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238 9 Physiotherapy for Pelvic Muscles

ischemic situations, and due to the lack of oxygen, relaxation of the muscle fibers
is difficult. The ischemic substances induce pain. The motor endplate hypothesis
originated from the finding that at the endplates, near trigger points, the electrical
activity contains noise, related to extra acetylcholine transmission exemplified by
micropotentials. Summation of these micropotentials brings the activity over the
threshold-producing action potentials at the endplate causing contractions of a
limited amount of muscle fibers. The radiculopathic model argues that trigger
points are the consequence of compression or denervation of spinal nerves by
intervertebral disc pathology.
Weighing the arguments for the three hypotheses, the energy crisis hypothesis
has some weak support; the motor endplate hypothesis at least has the support
from needle EMG studies, while the radiculopathic model is not confirmed or
denied by neurophysiologic studies [19]. The most reliable hypothesis therefore
seems to be the endplate hypothesis, the more so because in experimental animals,
the trigger point needle EMG results could be confirmed. Trigger points are also
present in animals.

9.3.3 Quality of the Published Results on Trigger Points

If trigger points are structural anatomical entities, they should be recognized easily
by the manual or physiotherapist since pressure on trigger points, being active or
latent, produces pain. However, only one study out of six showed clear reliability
for finding the trigger points, due to the fact that an extensive training of the
clinicians preceded the study see [19] and references herein. In 2008, this result
was again affirmed: ‘‘The methodological quality of the majority of studies for the
purpose of establishing trigger point reproducibility is generally poor’’ [20].
Although the anatomical base for searching trigger points is sound, the spotting
of trigger points is disputed and seemingly not (always) repeatable by colleagues.
Moreover, a good explanation for trigger points is absent, although the motor
endplate hypothesis merits attention, due to the quality of the research in humans
and animals.

9.3.4 Trigger-Point Therapy

Stretch alone of muscles has no effect. Ischemic pressure in advance and stretching
afterward improves the pain scores. Transcutaneous electrical nerve stimulation
does not work, except if high frequencies are used. The duration of this effect is
unknown. Ultrasound does not contribute to pain relief, while laser application
reported both beneficial and no effects. Local anesthetic effects on pain are lasting
longer than the substance’s timely activity in the muscle, indicating a central
nervous system origin of the pain. It is hypothesized that counterirritation due to

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9.3 The Wise-Anderson Method 239

local destruction or ischemia of muscle fibers by the injected substance could reset
the central spinal pain transmission. Botulinum toxin blocks acetylcholine trans-
mission. Injections of 50 and 100 units compared to saline injections show all the
same improvement. Dry needle injection, like in acupuncture, was originally found
effective, but the more double-blind randomized controlled trials appear, the less
effect is reported. Dry-needling induces within 24 h intolerable pain in various
patients and therefore is not recommended [19].
The more therapies are subjected to double-blind randomized controlled trials,
the more the claimed effects become unconvincing.
In conclusion, the Wise-Anderson therapy for pelvic pain is based on still-
unproven assumptions that are published in anecdotal articles. Add to it that the
therapy can last 24 months and even longer before effects are noticed and a critical
approach is clearly allowed.

9.3.5 Quality of the Published Results of the Wise-Anderson


Method

Before we go into the publications on the results of the application of the Wise-
Anderson method, one has to realize that the method is mainly employed for men
with prostatitis, although women should benefit for other types of pelvic pain too.
Secondly, the method is directed to striated muscles and less to smooth muscles in
viscera. Thirdly, pain is also a psychological phenomenon: ‘‘Pain is the cardinal
chronic prostatitis/chronic pelvic pain syndrome symptom and is now being dis-
cussed, evaluated, and researched by experts outside of Urology. In a recent
National Institutes of Health sponsored meeting on chronic pelvic pain, it is
noteworthy that over 50 % of the discussion centered on the psychosocial aspects
and potential management models for chronic prostatitis/chronic pelvic pain
syndrome’’ [21] and the article ends: ‘‘As reviewed here, there is an obvious
association between chronic prostatitis/chronic pelvic pain syndrome psycholog-
ical and social variables that predict greater pain, disability, and poor quality of
life’’ [21]. Thus, whether one likes it or not, any randomized, double-blind con-
trolled study has also to fulfill the required parameters of psychological research,
especially in psychological studies bias is on the look.
The first question is: Why is this method on the incontinence market? The
figures presented are for the UK, because an overview in the USA is lacking to the
best of our knowledge. In the UK 2.4 million men do have lower urinary tract
problems associated with (benign) prostate problems. Only few physiotherapists
treat these men due to a lack of knowledge and lack of backing up by clinicians
and pelvic nurses [22]. The male prostatic/pelvic floor field is deficient of medical
physiotherapeutic support. The conclusion must be that there is an acute need for
medical care and the patients driven by pelvic pain are the first to search for it. The
failing of medical care in this field is responsible for the rise of alternative

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240 9 Physiotherapy for Pelvic Muscles

methods. Note that in the book ‘‘A headache in the pelvis’’ the Wise-Anderson
method is considered ‘‘alternative’’.
The second is does it work? Here, we encounter a problem that was detected
directly by the opponents. In the article ‘‘6-Day Intensive Treatment Protocol for
Refractory Chronic Prostatitis/Chronic Pelvic Pain Syndrome Using Myofascial
Release and Paradoxical Relaxation Training’’ [23], the total amount of patients
taken up in the study is 200, while the results are given for only 116 men. It is not
unusual that dropouts are present in such kind of studies, but the reasons have to be
indicated. They are not. Thus, 48 % of the patients are not included in the results.
The study used psychological support for the patients by David Wise and psy-
chological questionnaires to evaluate results. Why was an independent psychol-
ogist not involved? Who made the questionnaires? Is it bad to think of
psychological bias to be present?
From the result description is the next citation: ‘‘We followed 116 men for a
median of 6 months. Baseline total symptom index was 26 out of a maximum 43
points. Scores decreased by 30 % (p \ 0.001) at follow-up with 60 % of subjects
demonstrating a 6 point or greater decrease (range 6–30). Domains of pain, urinary
dysfunction and quality of life showed significant improvement (p \ 0.001)’’ [23].
A symptom index of 26 reduced to 19 is still within the severe scores according to
the NIH, and 30 % is still a placebo effect, this after 6 months of the 6 days
treatment. Moreover, pain reduction is one point on a scale of 10, which can be
called minimal. Moreover, a control group is missing. At least, this article does not
illuminate the effects of the Wise-Anderson treatment. Being a referee for several
journals (EM), I asked myself why an article with so many flaws could pass the
referee system of the Journal of Urology.
Before this article of 2011, a randomized, multi-center comparison between
global therapeutic massage and myofascial physical therapy was published in 2009
[24]. The protocol for massage was strict and deviations considered violation of
the trial, while myofascial therapy had extended possibilities and freedoms. Only
the myofascial therapy patients got a home program. The study was not blinded;
over 90 % of the patients knew their arm of the trial, as did the physiotherapists.
The study was introductory for a larger comparison and wanted to know whether
the setup is feasible or not. ‘‘Importantly, this randomized controlled trial was not
designed to assess whether myofascial physical therapy is superior to massage
therapy for treatment of Urologic Chronic Pelvic Pain Syndromes’’ [24]. Never-
theless, the outcome indicated such superiority: ‘‘The preliminary findings of a
beneficial effect of myofascial physical therapy warrants further study’’ [24]. At
least, this article is more careful in its text and indicates a larger study with up to
90 participants per trial arm, which was not available till now (2012).
It seems undeniable that the Wise-Anderson method has hardly any support
from randomized, double-blind, multi-center trials, while the publications from
their own group are liable to underpinned criticism. It is therefore impossible to
indicate whether the method gives more than a placebo effect. Please note that this
author has done everything to stay away from the personal attacks on David Wise
and Rodney Anderson as found on the Web.

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9.4 Anatomy of Pelvic Floor Training 241

9.4 Anatomy of Pelvic Floor Training

After these disappointing results, one could think that pelvic floor training is of no
value. Let us see what anatomy and physiology put on view. The levator ani
muscle is indeed different in female patients with combined urine and fecal
incontinence compared to controls (see Table 9.1) [25].
This holds for the thickness, the angle of the levator ani position, and the
enlargement of the pelvic hiatus (Table 9.1). In the healthy subjects, the levator ani
forms a dome, with its top to cranial, while in these patients, it is a funnel with its
point directed caudally. It is uncontestable that the position of levator ani position
is different and its structure is also changed in these incontinent women.
In five females with urine incontinence, the changes in the levator ani muscle
was measured by MRI before and after pelvic floor muscle training. The surface
area and the volume of the levator ani decreased, and its contraction increased.
Symphysis movement during contraction diminished [26]. ‘‘Findings from this
preliminary study indicate that pelvic floor muscle training results in anatomical
changes in the levator ani and reduction of pubic movement’’ [26]. That is all
anatomy provides, and the training effects are only from a preliminary study.
Physiological results are even worse. The general belief is that the levator ani
muscle elevates and closes the urethra and anus, contributing to continence.
Incontinence is battled by pelvic floor muscle training. The opposite view that the
levator ani opens the urethra and anus thus supports evacuation of urine, and feces
is also present [27]. The editorial comment put the difference in opinion and in
results back toward anatomy: ‘‘This controversy may be due to differences in
opinion about how the pelvic floor is subdivided. Most urologists think of the
pelvic floor as the pubococcygeus, iliococcygeus, and puborectalis, all working
together as a single unit. In contrast, this report describes the puborectalis as being
completely separate, both in orientation and innervation. They also describe the
levator ani muscle as being divided into two parts: the lateral masses (which
provide support) and the crura (which open the levator hiatus when they contract)’’
[27A]. It seemingly stays a puzzle to elucidate the function of the levator ani, due
to the difference of opinion on its morphology as found in the literature. The study

Table 9.1 Parameters of the levator plate complex


Parameter Study group (N = 18) Control group (N = 14) P value
Ureterovesical angle (degrees) 91 ± 23 73.5 ± 10 0.004
Levator hiatus (mm) 58.3 ± 8 46.5 ± 8 0.001
Levator angle (degrees) 3.0 ± 5 14 ± 10 0.004
Levator density (pixels) 157.3 ± 47 126.1 ± 23 0.025
Levator area (mm2) 19.5 ± 1 26.9 ± 1 0.001
Puborectalis thickness (mm) 9.5 ± 3 12.5 ± 3 0.016
Significance P \ 0.05
Parameters of the levator ani and urogenital diaphragm complex, reproduced with permission
from [26]

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242 9 Physiotherapy for Pelvic Muscles

of the development of the levator ani (see Chap. 8) was done to establish, once and
for all, the morphology of the levator ani with the idea that the unadulterated form
can be found by checking the whole trajectory of its development.
If one looks for overviews on pelvic floor training, the article of Kari Bø, a
well-known scientist in this field, shows that despite randomized controlled trials
‘‘Future studies are needed to assess whether pelvic floor muscle strength training
can lift a sagging, stretched and weak pelvic floor into a more optimal position
where it can counteract the rise in abdominal pressure’’. Several of the studies on
pelvic floor muscle training are considered weak by her too. This conclusion has
been supported more recently: ‘‘There is a need for at least one large, pragmatic,
well conducted, and explicitly reported randomized trial, comparing pelvic floor
muscle training with a control, to investigate the longer-term clinical effectiveness
of pelvic floor muscle training. Also, studies investigating different pelvic floor
muscle training regimens are required to establish the optimum method of deliv-
ering and undertaking this intervention’’ [13A]. Thus, it claims that pelvic floor
muscle training works are badly supported.
A logic thought is that EMG results could prove the physiological changes after
pelvic floor muscle training. However, ‘‘The results suggest that although it is
acceptable to use pelvic floor muscle surface EMG as a biofeedback tool for
training purposes, it is not recommended for use to make between-subject com-
parisons or to use as an outcome measure between-days when evaluating pelvic
floor muscle function’’ [28].
Although prescribed as a first-line intervention for urine and fecal incontinence,
establishment of the positive effect of pelvic floor muscle training is yet to be
proven. Moreover, the different methods in use do not contribute to the clarity of
the effect of pelvic floor muscle training.

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Literature has been grouped in reference lists of several chapters in those cases where
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24. FitzGerald MP, Anderson RU, Potts J et al (2009) Randomized multicenter feasibility trial
of myofascial physical therapy for treatment of urologic chronic pelvic pain syndrome.
J Urol 182:570–580
25. Eguare EI et al (2004) Dynamic magnetic resonance imaging of the pelvic floor in patients
with idiopathic combined fecal and urinary incontinence. J Gastrointest Surg 8:73–82
26. Dumoulin C, Peng Q, Stodkilde-Jorgensen H et al (2007) Changes in levator ani
anatomical configuration following physiotherapy in women with stress urinary
incontinence. J Urol 178:970–977
27. Shafik A, El-Sibai O (2001) Effect of levator ani muscle contraction on urethrovesical and
anorectal pressures and role of the muscle in urination and defecation. Urol 58:193–197
27A. Editorial comment
28. Auchincloss CC, McLaen L (2009) The reliability of surface EMG recorded from the
pelvic floor muscles. J Neurosci Methods 182:85–96

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Chapter 10
The Subperitoneal and Lower
Retroperitoneal Space

The detection of carcinoma’s in the pelvic spaces remains difficult, in spite of


modern CT and MRI techniques. These sub- and retroperitoneal spaces are treated
in this chapter using two leads: blood vessels present and the testicle that uses
these spaces to descent. The surprising result is that the blood vessels of the ovary
determine the peritoneal fluid, which is important to let the egg survive during
ovulation. The renewed attention for these blood vessels brought out the ana-
tomical description of the subperitoneal arterial plexus of William Turner of
150 years ago.

10.1 Introduction

This chapter concerns what is called the caul (membranes), an old word matching
the term mesothelia or membranes surrounding organs: in the abdomen called
peritoneum, in the thorax named pleura, or around the heart entitled pericardium.
Nowadays, it is exclusively used for the amniotic membrane. In the pelvis, it
concerns only the peritoneum.
Imagine that you blow up a large balloon in your room. The balloon is the
peritoneal sac. You are pressed to the back wall of your room with its paintings by
the inflated balloon, and the balloon even is between you and the window that was
a 4–5 m in front of you; it fills the whole room. To escape, you have to creep over
the floor to reach the door. The space you are creeping through, between floor and
balloon is called the subperitoneal space, while the space you left, between balloon
and wall, is the retroperitoneal space. The space between window and balloon is
the preperitoneal space and is just between the peritoneum and the belly wall. The
outer surface of the balloon is called the parietal peritoneum. In humans, the
abdominal and part of the pelvic space are filled by the balloon, with in it all types
of organs, most of it belonging to the digestive tract (Fig. 10.1). Now, imagine
again: the balloon covers, of course, your table and seats that are in the subperi-
toneal space. Indeed, all organs in the pelvis are covered with balloon surface, thus
with peritoneum. The same holds for your pictures and lamp at the wall. They are
covered with peritoneum at the retroperitoneal space. The main blood vessels that

E. Marani and W. F.R.M. Koch, The Pelvis, 245


DOI: 10.1007/978-3-642-40006-3_10,  Springer-Verlag Berlin Heidelberg 2014

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246 10 The Subperitoneal and Lower Retroperitoneal Space

Fig. 10.1 Schematic drawing that shows the peritoneal relations in abdomen and pelvis. Green
indicates the space between thoracic diaphragm and pelvic diaphragm. A sagittal section (black
lines left figure) is made and turned (see arrows, left figure). The peritoneal sac hangs on
attachment to the diaphragm and blood vessels (right figure, 1 vena cava inferior, 2 truncus
coeliacus, 3 art. mesenterica sup., 4 art. mesenterica inf.). The abdomen is subdivided in an upper
and a lower part by the greater omentum (5 upper abdomen 6 lower abdomen 7 os sacrum) 8
retroperitoneal area that is continuous with the subperitoneal space (both in coal dust) 9
preperitoneal direction to which the filled bladder bulges out. Dotted line is the virtual border
between abdomen and pelvis  E. Marani

are directed toward the pelvis, such as the abdominal aorta, stay retroperitoneal.
They are localized like your paintings and lamp, thus covered by peritoneum
(Fig. 10.1).
During development, the balloon has been filled with organs that press itself
into the balloon. So these organs are surrounded by peritoneum. On the moment
the peritoneum surrounds an organ (=viscerum), it is called visceral peritoneum
(i.e., the inside surface of the balloon). The organs can even hang on an elongation
of the peritoneum, constructed of two blades, one going downward and then
surrounding the organ and the other upward back to the balloon’s outer side, both
blades stick together, which is called a meso.
Blood vessels and lymphatic vessels to the digestive organs have to follow the
ingrowth of the organs and are in between both peritoneal blades, thus located into
the meso. The subperitoneal space is continuous with the retroperitoneal space;
otherwise, you could not creep to the door (Fig. 10.1).

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10.1 Introduction 247

What is present and what can happen in the retro- and subperitoneal space?
Within the retroperitoneal space are located the large vessels: the abdominal aorta
and the vena cava inferior (each with its branches for those organs that are present
in this space) and the kidneys with the ureter (of course there are more, but not
important at the moment). The ureter takes a pathway that starts at the kidney(s) in
the retroperitoneal space, but to reach the bladder, it has to bow below the peri-
toneal sac into the subperitoneal space (your escape-creeping way). The subperi-
toneal space contains bladder, vagina, and rectum (of course more) and, at its
lateral side, the continuation of the ‘‘bifurcated branches’’ of the aorta and vena
cava: the iliac veins and arteries. Along the arteries and veins are placed the lymph
nodes interconnected by their own lymphatic vessels in the whole sub- and ret-
roperitoneal space. They are our interest in the first part of this chapter.
However, before turning to that subject, one should know that the peritoneum is
an enigma for clinicians. In 1892, Smith [1] gave a lecture at the British Gyne-
cological Society on hysterectomy (removal of the uterus) in patients with a uterus
tumor. He cites 12 articles and congress reports between 1887 and 1891 with
different opinions on the topic: how to close the supravaginal part of the uterine
remnant with or without peritoneal flaps. One should think that surgeons should
have solved this problem ‘‘how to deal with the peritoneum’’ after at least a
century. However, closure or non-closure of the peritoneum of the uterus after
cesarean delivery produces an analogous discussion: ‘‘Nonclosure of the perito-
neum at primary cesarean section is associated with a significantly increased risk
of visceral adhesions [2],’’ while others say: ‘‘There are more advantages than
disadvantages to not closing the peritoneum. We encourage clinicians not to close
both parietal and visceral peritoneum [3]’’ or ‘‘Routine closure of the visceral
peritoneum should be abandoned at cesarean delivery [4].’’ Seemingly, the peri-
toneum is a hard nut to crack clinically and scientifically. Note that the gyne-
cologist is consequent in its terminology: peritoneum covering the uterus is
visceral peritoneum, and next to that part, peritoneum not covering the uterus, but
the abdominal wall, is parietal peritoneum. The anatomist would call it all parietal
peritoneum.
So, the first question is, what is the peritoneum? It is a serosal (caul) membrane
constructed by a layer of loose connective tissue, covered by a layer of flat cells,
so-called mesothelium. These cells are supported by a series of chemical sub-
stances (basal lamina) beneath it. Such a membrane makes the free movement of
organs possible. ‘‘This lubrication is achieved by a small amount of fluid and a
special adaptation of the mesothelial apical membrane that bears a significant
number of microvilli, covered by a surface film of hyaluronic acid-rich glyco-
protein [8].’’ This film by its ionic negativity and its smallness (30–60 nm) con-
tributes enormously to the lubrication. However, such membranes do more:
transport and uptake of fluid and of materials, regulation of white blood cells in
case of inflammation, synthesis of proinflammatory substances, repair of perito-
neal membranes, control of bleeding by coagulation, and antigen presentation to
help blood cells to attack intruders. Its physiologic properties are well known: ‘‘it
has been used for a live-saving procedure—peritoneal dialysis- as well as

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248 10 The Subperitoneal and Lower Retroperitoneal Space

intraperitoneal nutrition, chemotherapy, immunotherapy and the treatment of over


access of (a fluid called) ascites [8].’’ Now, suddenly it is no longer a simple rope
to keep organs in place, but a highly sophisticated bodily police agent, building
restorer, transporter, pump, and also the oil in machines.
‘‘The total area of the human peritoneum is approximately 1.8 m2 which is
almost equal to the body surface area of the skin [8].’’ This is the area of a nice
carpet. It is clinically used as a life-saving machine also due to its large surface
with special properties over which exchange can occur.
Still the peritoneum has its secrets. Two aspects, both related to the lymphatic
system in the peritoneum, are the stomata (little mouths) and milky spots. We
restrict ourselves to the pelvic peritoneum, especially the peritoneum covering the
uterus. This is for not going into the structural differences in the various peritoneal
regions. Stomata are small openings in between the flat superficial cells where
lymphatic endings have free access to the parietal and visceral peritoneal surface,
thus uncovered lymphatic vessel structures. Milky spots are lymphoid tissue
clumps within the peritoneum full of macrophages and lymphocytes [8] and ref-
erences herein. They are not comparable to small lymph nodes. The discussion on
how their constructs are is still going on [8]. We do know that after infection
and\or inflammation, their amount and different cell types increase [8]. These
structures seemingly are gatekeepers that can organize various forces to clean the
region and open new frontlines by extending the amount of attack sites. Whether
or not these structures contribute to the ‘‘live-saving procedure’’ is unknown.
The repair power of the peritoneum is huge. ‘‘The fact that areas as large as the
entire pelvis may be denuded of their peritoneum in radical operations in unusual
instances of carcinoma, and that the same surfaces are to be found completely
reperitonealized many months later, is indicative of the strong tendency of the
peritoneum to regenerate [9].’’

10.2 Carcinoma’s in the Retro and Subperitoneal Space

It lasted a long time after Erasistratus (300–225 BC), who discovered the chylif-
erous vessels in the goat (chyle is the content of lymphatic vessels), before the
lymphatic vessels were rediscovered. It was Gasparo Aselli (1581–1626), surgeon
and physician in Milan, and professor of anatomy in Pavia, studying the anatomy
of dogs, who noticed that after the dogs were given a good meal, white small
vessels appeared in the dog’s mesenterium (the meso of the intestine). Chyle is
white if a lot of fat is taken up and they were called lacteal vessels (milk vessels).
Sylvius de la Boë (1614–1672) and Thomas Bartholinus (1616–1680) disputed the
function of the lymphatic vessels and the involvement of the liver. The liver was
wrongly thought to metabolize the chyle. The system of a main duct (ductus
thoracicus) and a sac or receptaculum (cisterna chyli) in which chyle is accumu-
lated, together with the emptying in the venous system, slowly came forward.
A series of scientists, Jean Pecquet (1624–1674, France), Johannes van Horne

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10.2 Carcinoma’s in the Retro and Subperitoneal Space 249

(1621–1670, The Netherlands), Olof Rudbeck (1630–1702, Sweden), and Niels


Stensen (1638–1686, Denmark), all contributed. However, the controversies were
numerous [7], concerning who detected what structure of the lymphatic system for
the first time. It is clearly a seventeenth-century series of discoveries that based our
anatomical knowledge of the lymphatic system and not earlier than the twentieth-
century scientists started to understand the immunological and protective functions
of the system: The lymphatic system is responsible for taking up those fluids left
by the veins, and in the digestive tract, it takes up the fat that passes the digestive
wall and empties it by the thoracic duct in the venous system (left internal jugular
vein and a separate right-sided ending for right head and right arm), and it contains
part of the immune system and part of the protection system against bacteria and
viruses.
If the lymphatic immune surveillance for cancer cells fails, the lymphatic
system is also used by cancer cells to spread. The large lymphatic system vessels
and nodes are localized in the subperitoneal space and retroperitoneal space in the
pelvis. As an example in Fig. 10.2, the spread of kidney, bladder, and prostate
cancers are demonstrated along the lymphatic system in both subperitoneal and
retroperitoneal spaces.
One should notice that the spread of kidney cancer is also downward and from
prostate and bladder cancer both upward, meaning that the lymph nodes laying
against the sacral bone are often involved [5A] and are tricky to reach (see 17.5,
rectosacral fascia). Lymph nodes are grouped, e.g., those along the obturator
vessels, the iliac vessels, or the sacral ones. The number of groups surgically
dissected determines whether it is called a limited (mainly internal iliac and/or
obturator nodes) or an extended pelvic lymph node dissection.

10.2.1 Detection of Pelvic Lymph Node Cancer by Computed


Tomography and Magnetic Resonance Imaging

These cancers are assassins. Lymphogenic extensions of these cancers are clini-
cally difficult observable, unless they are found by computed tomography (CT) or
magnetic resonance imaging (MRI) (in CT, it is more problematic than in MRI), or
by typical antibodies or proteins for that type of cancer that are found in blood
determinations. The lymphatic sub- and retroperitoneal cancers, so to say, hide
behind the peritoneal sac and in the CT and MRI gray scales, as we will see later
on. As an example to understand the gray scales of the computed X-ray tomog-
raphy (CT), we look into gossypiboma, surgical sponges, or swabs left accidentally
in the operation area after closure of the wound. The occurrence rate is
1:100–5,000 operations. Such a spread means that we do not know the occurrence;
let us hope it is not 1:100. Bony structures will come out clearly white in the CT,
but organs and muscles show a variation in gray scaling. Air is nearly black.
(Absorbable hemostatic sponges appear gray; thus, they are difficult to detect, but

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250 10 The Subperitoneal and Lower Retroperitoneal Space

Fig. 10.2 Metastasis pathways for kidney cancer (a); bladder cancer (b); prostate cancer (c).
a Routes are different for various parts of the kidney (anterior A, middle B, and posterior C kidney
route), while 1, 2, and 5 are para-aortic lymph nodes, 3 and 4 nodes along vena cava, 6 and 7
lymph nodes along iliac arteries. b The bladder metastasis in A is along trigonum of the bladder,
B along the bladder back and C along the anterior bladder wall with 1 and 3 iliac nodes, 2 nodes
along internal iliac artery, 4 lateral node pathway, 5 frontal bladder nodes, 6 aortic nodes and 7
inguinal lymphatic nodes. c The prostate metastasis is in A along extern iliac artery, in B along
the internal iliac artery, C along lymph node pathways at the back of the pelvis and D the lowest
lymph node pathway with 1 and 4 lymph nodes at the iliac arteries, 2 at the internal iliac artery,
6 at the aorta and 7 the inguinal nodes, while 5 are intercalated nodes (reproduced with
permission from Donker and van der Werf-Messing [5])

contain up to 6-month small air bubbles). Those black spots are useful for their
identification [10]. Lymphatic nodes are small and contain nearly the same gray
scale as other tissues in the pelvis, and if containing a primary tumor or metastasis,
it has nearly the same gray scale. These abnormal ones are difficult to discern, like
pure sponges without air bubbles. Abnormal nodes are generally detectable by
their form, especially if enlarged.
We look here into the sensitivity of the used techniques, which means the
amount of correctly detected lymph node metastasis in advance of the operation,
mostly compared to verified pathology of dissected nodes after the operation or to
another imaging technique. And we focus on mainly prostate cancer and early
uterine cervical carcinomas. In the early days of CT and MRI, the CT misses the
early stages of both bladder and prostatic tumors, while MRI detected a lot of them
[11]: ‘‘Staging of early prostatic malignancies is imprecise by CT and accuracy in

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10.2 Carcinoma’s in the Retro and Subperitoneal Space 251

staging known bladder carcinoma has been reported to be only 64 %… Sensitivity


by CT is only 33 %’’ in the detection of pelvic lymph node metastases [11]. Thus,
while around the 1970s, we only had cystoscopy for the symptom hematuria, blood
(color) in the urine; in the 1990s, CT and MRI were available, but still missed a lot
(for CT 67 % and for MRI nearly 20–30 % [13]). Nevertheless, it is an enormous
progress compared to the 1970s. It also indicates that the sub- and retroperitoneal
mainly smaller affected lymphatic nodes are still hard to detect.
‘‘Magnetic resonance imaging (MRI) provides images with excellent anatom-
ical detail and soft tissue contrast but is relatively insensitive for the detection of
lymph node metastases [12]. However, the results of MRI can be improved by
using different imaging agents and acquisition techniques [13] see also [14].’’ But
how is this organized? We treat here one of these techniques that was only recently
introduced. Particles, which are magnetic and very small (10-9 m), so-called
nanoparticles, to which is added a substance that favors uptake by macrophages
and called lymphotropic superparamagnetic nanoparticles, are injected into the
venous blood stream. They are taken up by the macrophages and brought to the
lymph nodes, which is time-consuming, up to 24 h. Due to their magnetic prop-
erties, they are easily detected in the MRI. This occurs in normal nodes and the
metastatic ones. How then to differentiate? ‘‘In normal lymph nodes, the signal
intensity decreased homogeneously after the administration of lymphotropic su-
perparamagnetic nanoparticles, indicating normal delivery of the nanoparticles to
the lymph nodes and normal uptake of the particles by nodal macrophages. In
lymph nodes containing metastases, there was either a limited decrease in signal
intensity or discrete focal defects within the node owing to replacement of nodal
architecture by tumor deposits [12].’’ One deliberately introduces differences in
gray scaling to detect metastasis. The claimed detection is nearly 100 %, and
others say 92 % [12] or 80 % [15].
Positron emission tomography (PET) often in combination with CT and
injected radioactive substances such as 11C-choline or a radioactive glucose
(2-[fluorine18] fluoro-2-deoxy-D-glucose, abbreviated as 18FDG) are promising
new techniques [13, 14]. Some types of pelvic cancers use high amounts of
choline, and cancer cells do have a rather high metabolism and thus consume more
glucose and thus more 18FDG. Concentrations of radioactivity can be located with
PET. Nevertheless, ‘‘Choline PET/CT at the present time can not be recommended
for the diagnosis of primary prostate cancer but may be helpful in clinically
suspected prostate cancer with repeatedly negative prostate biopsies, in prepara-
tion of a focused re-biopsy. There is, on the other hand, an increasing body of
evidence that PET and PET/CT with radioactively labeled choline derivates is a
sensitive tool for the re-staging of patients with increasing prostate-specific antigen
serum levels after definitive local therapy [13].’’ So for the early detection, PET or
PET/CT with its choline radioactive substances is not useful, but if it is applied
after uncertainty in detection or after operation and/or therapy, it is a proper tool.
An analogous discussion is going on for 18FDG [14].
Looking at the literature, one should be hopeful for the technical non-invasive
detection of metastases in pelvic lymph nodes. Nevertheless, a serious discussion

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252 10 The Subperitoneal and Lower Retroperitoneal Space

in literature followed on two publications of Briganti [15]: They are something


like putting the cat (the surgeon) among the pigeons (imaging technical clinicians).
We use a part of his introduction on pelvic lymph node dissection in prostate
cancer: ‘‘Pelvic lymph node dissection represents the most accurate and reliable
staging procedure for the detection of lymph node invasion in prostate cancer.
Unfortunately, imaging procedures such as CT and standard MRI have very
limited ability to predict lymph node invasion. Other interesting imaging tech-
niques such as [11C] choline positron emission tomography/CT or MRI with
lymphotropic superparamagnetic nanoparticles are currently under investigation.
The latter technique is not yet available on the market, and the use of these
sophisticated imaging techniques is limited by significant costs. Thus, for the time
being, pelvic lymph node dissection remains the gold standard for nodal assess-
ment [15].’’ So, not the new non-invasive techniques, but the surgical removal of
pelvic lymph nodes is advocated to give a decisive answer in prostate cancer.
We have to make a small side step. Prostate-specific antigen (PSA) will play a
large role in pelvic lymph node metastasis understanding. Table 10.1 shows that
the relation between serum PSA and the prevalence of lymph node metastasis in
prostatic cancer can be calculated. Thus, PSA (among more criteria) can indicate
the metastasis risk, which is used to make the indication for an extended pelvic
lymph node dissection (PLND). Most Western countries have regulations or
guidelines formulated by their Urologic Societies for PSA-level-indicated treat-
ment. Although variability is found in the percentage of relations in various
studies, PSA still belongs to one of the best preoperative predictors for pelvic
lymph node metastasis and in need for PLND. Prostate-specific antigen is used to
determine the prostate cancer patient (among other criteria) into a low-risk or a
high-risk group: low-risk patient group is determined by an amount lower than 4 or
6 ng PSA, and others take lower than 10 ng of this antigen per milliliter.
Two aspects determine the clinical outcome of surgery in prostate cancer: (1)
the amount of operations done by the surgeon: ‘‘greater surgical expertise might
translate into a more meticulous nodal dissection, even when the same anatomical
pelvic lymph node dissection template is used [15A]’’ and (2) the extent of the
lymph node dissection, which is regularly debated. Literature ‘‘weakly’’ indicates
that an extended lymph node dissection increases the survival chance, see [15] for
references. However, ‘‘in view of the low rate of lymph node invasion among

Table 10.1 Relation between preoperative blood levels of PSA and the percentage of metastasis
in pelvic lymph nodes in patients with prostatic cancer (reproduced with permission after Triguert
[20])
Serum PSA in ng/ml Total amount Percentage of patients
of patients with positive pelvic nodes
B4 109 0.9
4.1–10 529 2.7
10.1–20 213 11
[20 129 19.4

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10.2 Carcinoma’s in the Retro and Subperitoneal Space 253

patients with low-risk prostate cancer, a staging extended pelvic lymph node
dissection might be spared in this patient category. Whether this approach is also
safe from oncologic perspectives is still unknown [15].’’ Now the question is, of
course, what is a low rate, beside that we do not know whether in low-risk patient
metastasis will, despite treatment, go on. False negativity occurs regularly in the
diagnostic phase: ‘‘Several studies have shown that the rate of lymph node inva-
sion in prostate cancer patients almost linearly increases with the extent of pelvic
lymph node dissection. Indeed, extended lymph node dissections might be nec-
essary to detect occult lymph node metastases that would otherwise not be
detected by limited lymph node dissections, as prostate cancer nodal metastases do
not follow a predefined pathway of spread [15].’’ False negativity ‘‘is 60 % if only
patients with lymph node metastases are considered [15].’’ In other cases, it is still
nearly 20 %, besides the never detected misses. The question of false negativity is
the more pressing because low-risk patients have a good survival probability and
high-risk patient seemingly can benefit from extended lymph node dissections.

10.2.2 Detection of Pelvic Lymph Node Cancer


by Size and/or Volume

‘‘Until now, CT and MRI have been the modalities of choice for the assessment of
lymph nodes in bladder and/or prostate cancer patients. With these modalities,
however, diagnosis is based on the size and shape of the nodes; smaller metastases
often go undetected and lymph nodes with reactive hyperplasia are vulnerable to
false-positive findings. Indeed, recent studies have shown that meticulous lymph
node dissection in patients with bladder or prostate cancer discloses a high rate of
metastases (25 %) in patients with preoperatively negative imaging studies
[12A].’’ From this statement, one can conclude that size and shape of the meta-
static pelvic lymph nodes are ordinary criteria, but rather a large false negativity is
present.
Above, we have seen how research tries to enhance the predictive values for
pelvic lymph node metastases by improving imagining techniques. Here, we study
the approach for size, shape, and volume of pelvic lymph nodes by CT and MRI,
directing ourselves first to one clinical trial. In 1999, the American National
Cancer Institute supported the American College of Radiology to start a series of
large cancer trials with various groups of clinicians from several hospitals called
American College of Radiology Imaging Network (ACRIN) with the mission ‘‘to
conduct clinical trials of imaging research to lengthen and improve the quality of
cancer patients live [16].’’ The gynecologic committee research strategy allowed
the study of the pelvic lymph node metastasis for early invasive cervical cancers
within a study for the early detection of such cancers by MRI and CT. The results
for the detection of cervix and uterus cancers are clear cut: ‘‘In patients with
cervical cancer, MRI is superior to CT and clinical examination for evaluating

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254 10 The Subperitoneal and Lower Retroperitoneal Space

uterine body involvement and measuring tumor size, but no method was accurate
for evaluating cervical stroma [17].’’ For the clinical judgment of these NMRI and
CT pictures by radiologists, the so-called reader variability, the outcome was also
clear: ‘‘Reader agreement was higher for MR imaging than for CT but was low for
both. MR imaging was significantly better than CT for tumor visualization and
detection of parametrial invasion. The modalities were similar for staging, sharing
low sensitivity and positive predictive values but relatively high for negative
predictive values and specificity [18].’’ These results are disappointing for the
patients, but finally, an established judgment on MRI and CT is given for the use in
the early detection of cervical cancers. The interobserver variability, seemingly, is
large, indicated by the high negative predictive value that there are clear misses by
the radiologist. In their own words, ‘‘These findings suggest that MR imaging and
CT are inherently imperfect for the evaluation of cervical cancer and that further
technologic advances are required to improve the imaging assessment of cervical
cancer [18].’’ One should note that 25 academic and community medical centers in
the USA are involved and each radiologist’s decision was checked by four radi-
ologists outside his institution.
Now, we look into their pelvic lymph node results. The aim of the study was
‘‘To compare MRI, CT, clinical exam and histopathological analysis for predicting
lymph node involvement in women with cervical carcinoma, prior to attempted
curative radical hysterectomy, verified by lymphadenectomy.’’ First, the setbacks
of the study: From the 172 women involved, 11 had no data on lymph node
metastasis, and on average, 20 % of the histological differentiation, pathologic
average tumor size, pathologic parametrial invasion, and of the pathologic uterine
involvement were missing, which was for histological lymph node involvement
6 % of the cases. The consequences were that the statistical analyses performed
were in several cases not significant. Now, ‘‘Tumor size could be measured by
MRI in 153 (89 %) women, compared with 126 (73 %) by CT. Considering only
cases where measurements were recorded, significant associations were detected
between histological lymph node involvement and average tumor size for MRI and
clinical assessment. After adjusting for multiple comparisons, no significant
association was found for CT or pathology [19].’’ Thus, although part of the data
were missing, the rest of the data on tumor size (remember total hysterectomy was
carried out, due to the tumor) showed a positive result for MRI, with a nearly 90 %
possibility to measure the size. Within the article, one finds one remarkable sen-
tence: ‘‘After adjusting for multiple comparisons, one of the four MRI multiob-
server re-readers demonstrated a significant association between histological
lymph node involvement and average tumor size [19],’’ indicating that an excellent
radiologist can indeed couple tumor size to the lymph node involvement and note
that 62 % of the lymph nodes were negative, and thus gambling by the radiologist
was not the case! The conclusion of this relatively large research project is weak:
‘‘MRI findings may help predict the presence of histological lymph node
involvement in women with early invasive cervical carcinoma, thus providing
important prognostic information [19].’’

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10.2 Carcinoma’s in the Retro and Subperitoneal Space 255

In conclusion, both CT and less MRI are weak means for the early detection of
cervical cancers and its involved lymph nodes status, and even blank rereading by
more radiologists does not improve the results. You have to do MRI because in a
large series of unpredictable cases, the result can be positive, but false negatives
are surely present. Of course, happily enough, the clinician has more options for
the early detection of cervical cancers.
Let us return to the prostatic cancers and look what size of the lymphatic nodes
in relation to metastasis shows in the prediction. The title of the article based on
CT is clear: ‘‘Lymph node size does not correlate with the presence of prostate
cancer metastasis [20].’’ Before a radical prostatectomy is carried out, spread of
the cancer is frequently tested by taking a large lymph node and have it tested for
metastasis by frozen section. ‘‘Multiple prognostic factors have emerged to
identify patients with nodal disease to prevent unnecessary local therapy. A serum
prostate-specific antigen (PSA) level of 20 ng/mL or higher, a Gleason sore of 7 or
higher, or clinically evident extraprostatic disease are risk factors for pelvic lymph
node metastasis. However, not all patients in these categories will have lymph
node metastases; therefore, some investigators advocate a frozen section evalua-
tion of the lymph nodes before performing radical prostatectomy either routinely
or if the lymph nodes feel enlarged. This relies on lymph node size as a surrogate
marker for metastatic spread [20].’’ The result is that by only checking the large
nodes, a false negativity occurs, in between 25–45 %. This study showed that in
73 % of the cases, lymph node metastases would have been overlooked, if only the
large lymph nodes were checked for and in 28 % metastasis were found later in
lymph nodes smaller than 1 cm in axial length. Moreover, if during the operation a
decision has to be made on extended lymph node dissection on frozen section of a
few lymph nodes taken out, a false negativity of 29 % is present. The title of the
article is a correct conclusion, but we had already seen that CT is not reliable.
Perhaps MRI is reliable in detection of metastasis by the size of the primary
tumor. Studies were made in cervical carcinoma patients. Here, it concerns vol-
ume: ‘‘The study demonstrates that tumor volume may be considered a predicting
factor in early cervical carcinoma patients, since it strongly correlates with pelvic
lymph node histological status [21].’’ Thus, if we know the tumor volume in the
cervix or uterus, we can predict lymph node metastasis: ‘‘The probability of lymph
node metastasis is 20 % for tumor volume of 17 cm3 and increases up to 50 % for
tumor volume of 40 cm3. An increase in tumor volume by 1 cm3 increased the risk
of lymph node disease by 6.2 % [21].’’ In fact, you do not predict where the
metastasis is localized, but you indicate a chance on metastasis presence. In fact,
the volume of the primary tumor does not indicate the localizations of the lymph
nodes containing metastasis, like in prostatic cancer.
Thus, for an unequivocal localization of pelvic lymph node metastasis, CT and
MRI do not fulfill the demands, whether or not radioactive isotopes, magnetic
particles, or classical measures such as size or volume are applied.

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256 10 The Subperitoneal and Lower Retroperitoneal Space

10.2.3 The Development of the Lymphatic System


and Milroy’s Lymphoedema

The general developmental principle is that the lymphatic system follows the
blood vessel system (Table 10.2). Thus, only after the invasion of blood vessels
into developing parts of the body, lymphatic vessels will emerge. This also holds
for wounded areas, and after the invasion of newly formed blood vessels, the
lymphatic system will follow. This idea was set forth by Florence Rena Sabine
(1871–1953) [22]. In the beginning, it was hardly accepted, but after her defense in
‘‘The origin and development of the lymphatic system,’’ it was taken over in most
handbooks on this topic and became a guiding principle for basic and clinical
studies [23]. By injecting the lymphatic system in various stages of the pig’s
development, the lymphatic vessels could be followed during their outgrowth. The
lymphatic sacs (see Fig. 10.3) are found to be the sprouting areas of the lymphatic
vessels. Lymphatic sacs are abundantly present in amphibians and reptiles. They
are considered primitive hearts that are responsible for the flow of the lymphatic
chyle.
Lymph nodes develop and keep their position at main entrances of and in the
rump. Extremities are mainly provided with lymphatic vessels, and nodes are few,
e.g., in the knee joint.
Genetic studies confirmed that embryonic veins change into lymphatic vessels
by an unknown external factor. Lymphatic vessel endothelial hyaluronan receptor
1 (Lyve1) and expression of the transcription factor prospero-related homeobox 1
(Prox1), and presumably Sox 18 transcription factor are responsible for appearance
of both and determine in the early development of the lymphatic vessels. Prox1
negative vessels stay blood vessels, while Prox1-positive vessels develop endo-
thelial cells for lymphatic vessels. Lymphatic endothelial cells that are Prox1
positive are also suspected of forming of the lymphatic sacs, by leaving the vessels
and regrouping into a lymphatic sac, a process called budding [23]. The budding
process is dependent on the production of mesoderm cells of lymphangiogenic
growth factor Vegf-c (=vascular endothelial growth factor-c). This Vegf-c attracts
Prox1/Lyve-1-positive cells because these cells have receptors for it [24]. A cas-
cade of factors is involved in the final staging of the lymphatic vessels, but why sac
formation occurs at restricted places is unknown.
The detection of Milroy’s disease occurred in 1891 by Nonne, but was pub-
lished for the first time by Milroy in 1892. As a physician in Omaha, USA, he was

Table 10.2 Timetable of embryonic development of lymph nodes


4th week: development of primitive circulation system
5–6th week: first lymphatic vessels present and development of lymphatic sacs or retinacula
8–10th week: development of lymph nodes
8th week: development of lymphoblasts
12th week: invasion of lymphoblasts into lymph nodes

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10.2 Carcinoma’s in the Retro and Subperitoneal Space 257

Fig. 10.3 Position of the lymphatic sacs, thoracic duct, and cisterna chyli in the human fetus,
according to Sabine in Keibel F, Mall FP (1910) Manual of human embryology. Lippincot Phil.
Lateral view is at the left and frontal overview at the right

visited by a vicar, who wanted a life insurance. On examination, his two legs were
swollen, due to a congenital malformation that was not troublesome. Since the
family history was kept for 250 years, the first occurrence could be traced. Of the
six generations studied, from 97 family members, 22 showed the disease (nearly
23 %) [24]. Both the older literature and recent research assured the presence of a
mutation.
In a series of researches of clinical cases, it also came out that development of
the lymphatic system can be changed due to a mutation. This congenital deflection,
also called hereditary or primary lymph edema, results in edema caused by
reduction in the lymphatic system and/or its malfunctioning. These hereditary
syndromes are subdivided into A (Milroy’s disease) and B and C syndromes. It is
characterized by swollen legs, swollen scrotum, swollen penis, or vulva. Secondary
or non-hereditary lymph edema is mainly caused by infection or the removal of
lymph nodes. Of each of the lymph edemas, one will be treated for its pelvic
consequences.
Milroy’s disease is a primary, congenital disease. It (can) appear(s) directly
after birth by swollen limbs or swollen external gender organs. It is clear from
genetic research with knockout mice, in which certain steps in the cascade are
removed during development, that Prox1 and Vegf removal in the cascade induces
the disease: reduction in the amount of lymphatic vessels (Prox1) and presumably
because the lymphatic vessel passage of fluid and substances is changed due to

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258 10 The Subperitoneal and Lower Retroperitoneal Space

alteration of the wall structure (Vegf). The disease is autosomal dominant with a
variable penetrance (50 %) and is located on chromosome 5q34–35 with a strong
heterogeneity. Mutations of chromosome 16q24 were also detected for this dis-
ease. The mutation changes the production of Vegf-receptor on the Prox1-positive
cells by the gene mutation FLT4, by which these Prox1-positive cells are no longer
sensible for the growth factor Vegf-c. It, therefore, becomes difficult to produce
lymphatic sacs. It occurs in 1:6,000 births in the London area. It is remarkable that
the disease involves legs, in a lesser amount the external sexual organs, but hardly
arm or face [24]. From all congenital lymph edema cases, 15 % is Milroy’s dis-
ease. Lymphography uses the slow stream present in the lymphatic system to add
contrast liquid that restricts itself to the lymphatic system. ‘‘Lymphography usu-
ally shows dilated, hyperplastic, incompetent lymphatic vessels (megalymphatics)
throughout the extremity and the trunk [25].’’
A series of specific mutations produces syndromes with hereditary lymph
edema: anhidrotic ectodermal dysplasia, Aagenaes’ syndrome, Hennekam syn-
drome, HTL syndrome, microcephaly chorioretinopathy, choanal atresia syn-
drome, yellow nail syndrome, Urioste syndrome, and pulmonary congenital
lymphangiectasia. Except for the last two syndromes, mutations and chromosomes
are known, but mutually different [24].
Primary and secondary lymph edema is well known in the tropics and is called
elephantiasis (Fig. 10.4). It is indicated in the literature that 20 % of the tropical
male population do have a form of elephantiasis, also caused by infections, and
best known of course are worm-like infections (filaria). ‘‘Penile lymph edema is
usually seen in conjunction with a similar process in the scrotum. This elephan-
tiasis, if severe, produces a very unsightly deformity and is the source of extreme
mental anguish. Owing to lymphatic stasis, the penis thickens and becomes
crooked, while the scrotum is considerably enlarged from hard, brawny edema and
a rough thickened skin. This is the result of fibrous organization, loss of elastic
fibers, hyperplasia of the collagenous connective tissue and secondary bacterial
infection (erysipelas). Erection is inhibited and cohabitation impossible, while the
much enlarged scrotum interferes with walking [25].’’ This citation brings up the
effects of lymph edema on the skin. Due to the blocking of the lymph fluid, it
accumulates below the skin, and after sometimes, the structure of the skin changes.
Enhancement of skin creases, development of fibrosis, increased skin thickness,
hyperkeratosis (hypertrophy of the horny skin layer), increased dermal turgor (skin
swelling/pressure), and formation of papills on the skin surface are the charac-
teristic changes. This stasis also makes infections more easily to enter the skin. In
Milroy’s disease, such infections are also reported.
Studies on hysterectomy and cervical cancers showed that 5–6 up to 20 % of
the patients developed the lymph edema depending on the study performed. Mid-
thigh circumferences can increase by the removal of the pelvic lymph nodes.
‘‘Preventing postoperative leg lymph edema has been investigated recently. In
2003, Fujiwara reported on the use of omentoplasty and omentopexy (attaching
omentum to abdominal wall, addition ours) to prevent complications after pelvic
lymphadenectomy [27].’’ The omentum (the protrusion between 5 and 6 in

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10.2 Carcinoma’s in the Retro and Subperitoneal Space 259

Fig. 10.4 Scrotal


elephantiasis: scrotal
diameter 14 by 12 cm, the
scrotum reaching the knees
by its weight of 1.6 kg
(reproduced with permission
from Masia et al. [26])

Fig. 10.1) was cleaved, lowered into the pelvis, and was covered with peritoneum.
In a 2005 study, also utilizing the omentum, Benoit reported on the use of pedi-
culated omentoplasty placed in the groin for preventing complications after ilio-
inguinal lymph node dissection in a series of seven patients. Each was treated with
a pediculated omentoplasty after groin dissection.
Complications, such as lymph edema, lymphorrhea, wound breakdown, skin
necrosis, and lymphoceles, were examined. Mid-thigh circumference increase
ranged from 1.5 to 7 cm in four cases but remained asymptomatic. Furthermore,
lymph edema of the lower limb decreased in the three remaining patients, who
previously had an enlargement of the thigh. The authors concluded that pedicled
omentoplasty seemed to facilitate the absorption or transport of lymph fluids and
resulted in less lymph edema in the lower limb even after radiation therapy.
Pedicled omentoplasty reduced both short-term and long-term postoperative
complications without affecting treatment outcome [27]. An analogous result was
obtained by Fujiwara [27]. Thus, an omental flap brought downward into the pelvis
will take over lymphatic function by the peritoneum large uptake capacity for
fluids and material. In fact, peritoneal dialysis was used (see 10.1). The peritoneal
circle we made is closed.

10.3 Lumbar Sympathectomy in the


Sub- and Retroperitoneal Areas

We have only one nervous system. It can be subdivided in subparts by function or


by form. The functional one is related to voluntary action. If you can influence
voluntarily the striated muscular action, we speak of the somatic (part of the)
nervous system. If you cannot influence the action, always related to smooth
muscles or glands, it is called the autonomic or vegetative (part of the) nervous
system. This autonomic nervous system is subdivided in a parasympathetic part
and in a sympathetic part, which have mutual antagonistic actions on the viscera

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260 10 The Subperitoneal and Lower Retroperitoneal Space

Fig. 10.5 Left overview of the sympathetic chain of Man. In red are the nerve supplies from the
spinal cord toward the ganglia (groups of neurons outside the spinal cord) and their connections
in black. The spinal nerves are indicated in yellow. Right scheme of the distribution of the
somatic fibers toward muscles and sympathetic fibers toward para and prevertebral ganglia
together with names of the various connections (Redrawn and changed after Pick [28])

they innervate. The blood vessels are exclusively innervated by the sympathetic
part of the nervous system. The sympathetic chain of ganglia is located along the
vertebral column (paravertebral, Fig. 10.5) or in front of the vertebral column
(prevertebral, Fig. 10.5). The sympathetic chain therefore is located retroperito-
neal and partially subperitoneal. It receives its information from neurons in the
spinal cord (Fig. 10.5).
This part on innervation also concerns blood vessels of the leg. Although the
topographic name changes from pelvic external iliac artery into femoral artery, it
is of course the same blood vessel. Peripheral obliteration of blood vessels is best
known for extremities and viscera. At the start of the twentieth century, amputa-
tion of the whole or the part of the extremity involved was the only measure to stop
the gangrene, the consequence of bad oxygen nutrition of tissue. In 1913, Leriche
(1879–1955) applied an existing method, periarterial sympathectomy, to overcome
dysphagia (bad digestion) of the intestine, caused by partial closing of the visceral
arteries. He, therefore, recommended tearing up the sympathetic parts that
innervate the intestines. Leriche extended the method and applied it in aortitis by
the destruction of the peri-aortal network of sympathetic nerves and also put the
technique on for the femoral artery during the disease of Raynaud (relapsing

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10.3 Lumbar Sympathectomy in the Sub- and Retroperitoneal Areas 261

cyanosis of fingers and toes, mainly in women) [28]. The idea was that the removal
of the sympathetic innervation will give vasodilatation and thus a better blood
stream through arteries, resulting in more oxygen into the tissues involved.
The anatomical scientific reaction was forceful. Already in 1914, it was shown
that the sympathetic fibers reach the blood vessels by the spinal nerves and not by
the periarterial networks (Fig. 10.5 right side). Experimental animal research
confirmed these results. Vasodilatation does not occur by the removal of the peri-
arterial network, and it does so after cutting the sympathetic outflow at the spinal
cord, confirming the spinal nerve pathway. In 1936, Leriche changed his tack: He
reverted the technique. However, spasm of leg muscles was cured by American
surgeons with lumbar destruction of the sympathetic chain around 1924. The claim
was that it worked. Surgeons became convinced that if painful spasm, painful
blood vessels, or other painful organs were present, resection of the sympathetic
chain was induced. In total, 27 diseases justified sympathetic chain resection at
that time [29].
The scientific doubt stayed, and 30 years later, the problematic situation was
unchanged, but the indications for lumbar sympathectomy were reduced: arte-
riosclerosis, diabetic angiopathy, and thromboangiitis obliterans. In fact, all dis-
eases were suspected of reduction in the arterial blood stream, whether by arterial
occlusion or changes in the arterial blood vessel wall and all producing ischemia.
An overview of literature showed that in 58 %, amelioration was claimed [29].
Gangrene was indicated to be reduced in 10 publications out of 13. The only
possibility to stop the uncertainty was looking into the oxygen behavior of skin and
muscles after a lumbar sympathectomy. ‘‘Elimination of the lumbar sympathetic
chain has no direct influence on the nutritive blood supply to the resting calf
muscles,’’ and if no nutritional lesions are present, blood supply to the subcuta-
neous tissue of the foot increases only in cold situations [29]. However, instead of
a lumbar sympathectomy, now the whole sympathetic chain from diaphragm to
sacrum should be removed [29].
One of the indications of bad arteries in legs is the so-called claudication.
Claudicatio intermittent is the phenomenon that the patient can walk a distance,
gets an unpleasant till painful feeling in the muscles, and has to stop walking. After
waiting for a period, he can walk the same distance and the unpleasant feeling in
the legs comes back. He or she has to stop again, and so on. It is related to
atherosclerosis of the bigger arteries.
The attitude toward lumbar sympathectomy started to change a few years later.
‘‘A review of the literature concerning lumbar sympathectomy and a study of fifty-
four patients upon whom the operation was performed were used to suggest that
lumbar sympathectomy is of questionable value in the treatment of arteriosclerosis
obliterans of the lower extremities. It is our opinion that lumbar sympathectomy
does not alleviate intermittent claudication, that it does not aid in the salvation of
gangrenous limbs, that it has no effect on amputation rate or level of amputation,
and that it is associated with a finite and significant mortality [30].’’ A clearer
statement is hardly possible. Reconstructive surgery of blood vessels even hastens
the down fall of the technique [31]. From the moment, it became clear that

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262 10 The Subperitoneal and Lower Retroperitoneal Space

vascular reconstructive surgery has its limits in ischemic patients, the option of
lumbar sympathectomy returned around the 1990s. Moreover, in the meanwhile,
chemical sympathectomy was developed and compared to surgical sympathec-
tomy. The outcome is, in general, that there is no difference [32] and the chemical
one is simpler to perform.
In 2009, a questionnaire was sent to UK and Irish vascular surgeons. It became
clear that no obvious criteria are present for the use of lumbar chemical sympa-
thectomy in serious vascular diseases. ‘‘Inoperable peripheral vascular disease
with rest pain was the main indication in over 80 % of responses with 27 % using
it for the treatment of ulcers. Only 21 % used lumbar chemical sympathectomy in
diabetics [33].’’
Lumbar chemical sympathectomy has found another application. In hyperhi-
drosis, the excessive sweating of the foot soles or groin can be overcome by
sympathectomy. ‘‘Although not a life-threatening condition, it can be a socially
and mentally debilitating disorder requiring frequent footwear changes, causing a
sensation of cold clammy lower extremities and social embarrassment. Conser-
vative management in the form of desiccating powders (containing aluminum
chloride), iontophoresis, and botulinum toxin injection is recommended but usu-
ally provides temporary relief only [34].’’ Note that a bilateral lumbar chemical
sympathectomy is necessary to overcome this excessive sweating.
Pelvic sympathectomies were also carried out for painful menstruation, pruritus
vulvae (itching of the vulva), and vaginismus (painful coitus and/or sexual dys-
function). The last two conditions are considered nowadays psychosomatic, and a
clinical multi-disciplinary approach will give better results than surgery [35].
Arterial dilatation can produce edema and pain in the female reproductive system,
the contrary of the pain reducing effect aimed at by sympathectomy. The part of
the sympathetic system to be removed is the superior hypogastric nerve plexus (the
black lines in Fig. 10.5 in between both sympathetic chains at 1st lumbar spinal
nerve). The pill can suppress ovulation and menstruation. The need for this
operation in extreme painful menstruations, therefore, is gone. The idea behind the
resection was that the nerve fibers relaying the pain information from the uterus
toward the central nervous system will be cut. Moreover, the vasoconstrictor
nerves should also been severed, abolishing pain due to ischemia [28]. Pelvic
sympathectomies are totally disappeared in techniques for sexual or pelvic floor
reeducation [35A].
An anatomical view on the pelvic part of the sympathetic system shows that
these ‘‘ganglia are extraordinarily variable in their number and location along the
lumbar sympathetic chain, and there is no constant pattern to their arrangement
[36].’’ These ganglia can be fused or not, contain variable connections with the
lumbar spinal nerves, and give cross-connections between both chains at the
lumbar level, and there are microganglia especially at the lumbar level and located
in the spinal roots [36]. All this information shows that lumbar sympathectomy
does not ensure that sympathetic information will not reach their targets, whether
by their microganglia that are not taken out or cross-connections or variability
toward their pathways. Moreover ‘‘As well as vasodilator innervation of erectile

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10.3 Lumbar Sympathectomy in the Sub- and Retroperitoneal Areas 263

tissue, the pelvic plexuses probably provide vasodilator innervation to much of the
pelvic circulation. Indeed, all reports on the distribution of neurons containing both
vasoactive intestinal polypeptide (VIP) and NOS in the pelvic viscera cited above
describe the presence of axons containing VIP and NOS around small and med-
ium-sized arteries. These are almost certainly vasodilator neurons [36].’’ NOS
produces the gaseous neurotransmitter nitric oxide and is found surprisingly also
colocalized with catecholamine neurotransmitters, which belong to the sympa-
thetic system. Moreover, some sympathetic axons use acetylcholine at the blood
vessel wall, and together with nitric oxide, it produces vasodilatation. Thus,
inherently sympathectomy also reduces the ‘‘restricted’’ vasodilation capacity of
the sympathetic system.
Special interest goes to the iliac arteries: the common and external iliac and
femoral arteries. Clinically, a subdivision in pelvic arteries (aorta till end of
external iliac artery), upper leg arteries (femoral till end popliteal (knee) artery),
and lower leg arteries (distal of the popliteal artery) is used, coinciding with the
sympathetic innervation, but not absolutely. The common iliac artery is innervated
by a continuation of the sympathic aortic plexus and by the lumbar sympathetic
ganglia. The external iliac artery is in its upper part innervated by the continuation
of the common iliac artery innervation, but halfway, it is taken over by autonomic
fibers of the genitofemoral spinal nerve (remember this nerve). The femoral artery
is mainly dependent on autonomic fibers of the femoral nerve [28]. This
description also supports the notion that a simple sympathetic innervation of the
supply vessels and large leg vessels does not exist, and again, the spinal nerves are
involved. If one knows that autonomic fibers do have a great potency of regen-
eration, the open places, caused by sympathectomy, will easily be occupied by the
still present, alternative innervation pathways.
And there is a direct cooperation between the somatic and autonomic systems in
the pelvis, inducing, e.g., incontinence after destruction of the sympathetic auto-
nomic part. Moreover, surgical sympathectomies are large operations in the
lumbar area. Thus, going from application in 27 diseases, its use is brought back to
extremely painful situations in atherosclerosis and diabetics. Nevertheless, it still
escapes general rules that indicate to anesthetists, radiologists, and surgeons its use
[33]. Seemingly, sympathectomy is not the manner to manipulate blood vessel
dilatation.
Do we know what the effects are if the sympathetic steering of the pelvic organs
is missing? For the bladder holds that sphincteric incontinence occurs, due to non-
function of the proximal urethra and for the male ejaculation is disturbed. ‘‘In
women, autonomic impairment does not appear to affect sexual function directly,
although this has been inadequately studied [35A].’’ Autonomic genetic disorders
have been studied frequently, but it looks like that the researchers are not inter-
ested in effects below the girdle. Only, for the Allgrove syndrome that includes
adrenal insufficiency, achalasia of the cardia, esophagal dysfunction, absence of
lacrimation and autonomic abnormalities [28], males are reported impotent.
Thus, for vasodilatation, the sympathectomy seems senseless, although it works
partially for gangrene in the lower legs, coming from empiric experience. Along

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264 10 The Subperitoneal and Lower Retroperitoneal Space

the sympathetic system, the small unmyelinated axons, responsible for pain, find
their way to the spinal cord and via long ascending systems and thalamic centers
and finally reach the cortex. We become aware of pain. Thus, pain transferred via
the sympathetic system can be interrupted by sympathectomy and is nowadays the
only ultimate remedy after the try of other pain-suppressing medication and
methods.
Unexpected side effects of sympathectomy are present. Here, we consider the
ureter. Its trajectory is in the retroperitoneal area near, but superficial, the sym-
pathetic chain. Chemical lumbar sympathectomy is carried out with aqueous
phenol solutions. After injection of this substance, it can spread and destruct not
only the desired part of the sympathetic chain, but also other structures. The case
history cited showed the connection between the kidney pelvis and ureter to be
affected. Nephrostomy placement (percutaneous drainage of the kidney) and
removal after three weeks of the tube did recover the patient [38].

10.4 Testicular Descent

The testis originates from the mid-part of the primitive kidney area, called
mesonephros, placed on both sides along the embryonic vertebral column. The
archetypes (primordial germ cells) of the ova are present outside the developing
embryo and migrate into the ovaries. The same holds for the spermatic archetypes
of the testis. Thus, the developing testes are placed retroperitoneal and have to
descent into the scrotum, by which they pass from retroperitoneal, via a subper-
itoneal route, toward low preperitoneal. At the lower frontal abdominal wall, there
is a channel (inguinal channel), through which the developing testis has to go, in
order to arrive into the later developing scrotum. Gonad construction is early in
development. The human testis descent is from the eight week till around birth. It
generally holds that fertile sperm in humans needs a lower temperature to mature,
which is present in the scrotum. Temperature regulation is organized by muscle
contraction (or relaxation) of the cremaster muscle. Contracting the testicle
ascends toward the abdomen, causing the temperature to rise somewhat. The
opposite applies for relaxation of the cremaster muscle. Every man knows what
happens to his scrotum, when it is cold, does not he?
Now, how is it possible that the testis can descend? Gravity is a bad argument
since the developing fetus hardly puts its legs down and its head up. Already in
1762, John Hunter (1728–1793), surgeon and anatomist in London, found a lig-
ament, stretching from the testis into the developing scrotum. He proposed that this
gubernaculum, as the structure is called, pulls the testis down [39A]. Disrespectful
said: Something like an elastic rope that under tension brings the testis down into
the scrotum. The same rope is present in female fetuses, but does not pull the
ovaries so much down (Fig. 10.6). It transforms into ligaments in the female.
There exists an abundant series of studies that include all kinds of theories on
testis descent (see [50]). We start with two recent review publications in order not

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10.4 Testicular Descent 265

Fig. 10.6 Final situation of testicular descent, compared to the female situation. The
gubernaculum (striped) pulled in man the testis with spermatic cord through the inguinal
channel, but in females, this does not occur (reproduced with permission from Moffat [39])

to discuss earlier literature: one is pure anatomical from the Rühr University
Bochum from 2000 [40] and the other is short-cell biological overview from the
Royal Children’s Hospital in Australia from 2004 [41]. The next citation is from
Hutson’s article from the Royal Children’s Hospital from Australia [41].
‘‘We are progressing toward a better understanding of normal and abnormal
testicular descents, which is one of the most obvious anatomical features of sexual
dimorphism. Its importance was appreciated by the church in the middle ages
when a female pope was elected, leading to a scandal when she gave birth to a
baby during a papal procession through Rome. Following this episode, the por-
phyry chair was produced as a way of determining definitively whether any future
pope was a man and hence could become the Holy Father. The chair has a cut out
in the seat such that the elected cardinal could sit on the chair, suitably robed, but a
junior cardinal could reach in from behind and palpate the scrotum. If the scrotum
contained 2 testes, they would chant ‘‘duo testes bene pendulum’’ (he has 2 testes
and they hang well), confirming masculinity and eligibility for the papacy. To this
day, a fused scrotum containing 2 testes is still the best test for manhood and is still
better than any genetic or hormonal test for a ‘‘man.’’
This citation shows, although bantering, how socially important this type of
research is. Moreover, in several cases, the descent fouls in humans and in animals.
This is called cryptorchidism. Two types are discerned: congenital and acquired.
Acquired cryptorchidism has prevalence in the normal population of 1–2 % [42,
43]. In the total, young male population cryptorchidism is present in 2–4 %. In
both types, the testis is found in the majority of cases somewhere within the
inguinal channel. The insertion of the gubernaculum was normal in nearly half of
the acquired cases, but only a minority of the gubernacula was correctly inserted in
the congenital cases: Up to only 20 % correct insertion is indicated in the

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266 10 The Subperitoneal and Lower Retroperitoneal Space

literature. The congenital studied cases do have more frequently aberrations within
the gubernaculum’s trajectory and structures [42]. The cause of this aberration, as
of infertile sperm, is sought in chemicals present in our environment and in alcohol
and nicotine consummated by the mother, among others. A cocktail of these causes
is held responsible. The discussion on this topic is emotional, sometimes
unequivocal and fought with passion, again indicating the social importance of the
research [43]. Compare it to the compassionate discussions that the Roman Empire
was codestructed by lead poisoning from their tableware, weakening the roman
people [44].
To understand the rather spectacular new developments in the field, one has to
study some developmental anatomy. Figure 10.7 shows most structures involved
and place them against the background of the large pelvic vessels: external iliac
and femoral arteries. The testis has to descend along the back side of the abdomen
and along the large arteries to reach the entrance of the inguinal channel. This is
called the transabdominal phase. The passing through the inguinal channel and
entrance in the scrotum is called the inguinoscrotal phase. The first step, descent
along the abdominal wall, is not relative, for example by growth of the back of the
fetus, but is also absolute in humans [40]. The transabdominal phase needs anti-
müllerian hormone but also an insulin-like hormone (relaxin-like factor; in com-
bination with androgens), which is produced by the fetal testis. The male
gubernaculum contains receptors for both hormones, and these receptors induce
reaction of the gubernaculum.
Directly above the gonad, there is a ligament present that stretches from the
developing diaphragm toward the top of the gonad, called the cranial suspensory
ligament. In males, this ligament deteriorates. In females, it stays and keeps the
ovary more or less in place, and the gubernaculum’s traction brings it somewhat
lower and let the ovary descend a bit, where it adheres to the uterovaginal angle by
the ovarian ligament (see Fig. 10.8).
To pass through the inguinal channel, the gubernaculum has to swell: so to say
enlarging the opening of the channel to let the testis pass. The insulin-like hormone
causes this. Here, we omit the discussions on length and divisions in the guber-
naculum and go on to the inguinoscrotal phase. It is regulated by androgens, male
hormones. The testis has to descent into the scrotum, which develops slowly, and
is present in humans in the eight month of fetal development. During the descent,
the testis is adhered to the peritoneal backside and ‘‘pulls’’ the peritoneum down
into the scrotum. So a part of the peritoneal space is drawn into the scrotum. It is
called the processus vaginalis. Part of the musculature of the abdominal wall
follows the testis descent, by surrounding the processus vaginalis, producing the
cremaster muscle, which is a continuation of abdominal wall muscle fibers. The
processus vaginalis closes at its upper end, so there is a part of the peritoneal space
in the scrotum, although separated from the peritoneal cavity. Since during
cryptorchidism the testis is in the inguinal channel and does not descend more, one
should think that the overflow from one hormonal situation to the other is blocked,
causing the arrest of the testis descent in the channel.

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10.4 Testicular Descent 267

Fig. 10.7 Reconstruction of


the whole trajectory of the
gubernaculum together with
surrounding structures
(reproduced with permission
from Barteczko and Jacob
[40]): 1 testis, 2 abdominal
part of gubernaculum, 3
interstitial part, 4
subcutaneous part of the
gubernaculum, 5 internal
inguinal ring, 6 right inferior
epigastric artery, 7 right
cremaster artery, 8 right
external iliac artery, 9 right
femoral artery, 10 genital
branch of the genitofemoral
nerve, 11 pubic symphysis,
12 pubic region, 13 penis.
Barr 1 mm

Fig. 10.8 Derivatives of the


gubernaculum. Note the
location of the round
ligament into the female
inguinal channel (reproduced
with permission from Larsens
Human Embryology,
Schoenwolf GC, Bleyl S,
Brauer PR, Francis-West PH
(eds) Larsens human
embryology, 4th edn.
Elsevier Health Science)

Let us state that this description was the research situation before 1980, except
the insulin-like hormone [45], at the same time doing injustice to a lot of
researchers. Of course there are important deviations and extensions from this
restricted description, but they are not important for our story. Also, it should be
remembered that the basic embryonic pattern is female and changes into a male
pattern are induced by androgens, male hormones.
Already in 1948, L.G. Lewis discovered that if the genitofemoral nerve (see
Fig. 10.7 for its trajectory) was cut, the testes did not descend, ‘‘which was
interpreted at that time as showing that the cremaster muscle, when denervated,

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268 10 The Subperitoneal and Lower Retroperitoneal Space

could not pull the testis to the scrotum [41].’’ Lewis rat results were repeated by
the Australian group, and the cryptorchidism was recovered in their rats. Estab-
lishing the importance of the genitofemoral nerve, another research direction was
chosen. The protein coneurotransmitter calcitonin gene-related peptide (CGRP) of
the genitofemoral nerve induced rapid contractions of the gubernaculum
(100 beats per minute): to fast for smooth or striated muscles. An embryonic
cardiac muscle type is supposed to be responsible, but its origin is unknown [41].
At least the elastic property of the rope is now explained, muscular contraction.
The sensory fibers of the nerve contained the CGRP and not the motor fibers,
which is perhaps considered strange, because normally motor fibers eject neuro-
transmitters for muscle contraction, but sensory fibers containing neurotransmitters
are well known, e.g., for the vestibular acoustic cranial nerve. This coneuro-
transmitter is needed to signal and steer the androgen action. Moreover, the
genitofemoral nerve is also involved in the closure of the processus vaginalis. If
the closure fails, an inguinal hernial sac remains. Intestine parts can enter the
scrotum. Experiments on inguinal hernial sac in vitro and application of CGRP in
piglets with cryptorchidism showed the involvement of this coneurotransmitter in
processus vaginalis closure and migration of the testis toward the place of CGRP
application [41].
The gubernaculum has to grow, since the embryo/fetus grows. The complexity
of growth of the gubernaculum, mainly by growth of its distal tip, should be
regulated. Till now, the main regulators are thought to be the hormones involved.
Preprogrammed signals are needed to regulate the start and the process of the
hormonal cascade by transcription factors and growth factors. These regulating
factors play their role not only in brain, heart, and genital structures but also in the
limb buds that finally produce the extremities. Comparison between the factors
found in the gubernaculum and the limb buds indicates that gubernaculum growth
uses a comparable set of factors as present in limb bud formation. ‘‘The migrating
gubernaculum grows like a limb bud’’ and therefore is an appropriate title for the
article this part is borrowed from [46].
However, the most spectacular finding still has to come. The role of the gen-
itofemoral nerve has been described above extensively. Its importance is now
undeniable in the testis descent. The external inguinal ring, the outside opening of
the inguinal channel, lies at the lower abdominal wall. By studying the subcuta-
neous area just beneath this ring, breast tissue was found in normal fetal mice.
Breasts are constructed along a line called the mammary line. This inguinal
mammary bud, together with the gubernaculum, is innervated by the genitofemoral
nerve. Mice with a mutation that makes them totally insensitive to androgens
(TMF mice) were studied next. ‘‘Histologic sections of the TFM male mice
showed that there was persistence of the embryonic breast bud, as well as some
development of mammary ducts and mammary fibrous stroma around the end of
the gubernacular bulb. In addition, a branch of the genitofemoral nerve was seen to
supply the developing mammary tissue [47].’’ Other types of inducing dysfunction
of androgens in mice showed: ‘‘The postnatal gubernaculum was not migrating
properly toward the scrotum and tended to be diverted laterally. The embryonic

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10.4 Testicular Descent 269

breast bud in the inguinal region persisted, and mammary ducts and mesenchyme
were seen to be developing in the subcutaneous adipose tissue and partly attaching
to the gubernaculum [47].’’ One of the genetic factors detected by the limb bud
comparison was also found in this breast tissue that contained a nipple and
mammary gland ducts. Mammary tissue surrounded the gubernaculum, together
with the double innervation by the same nerve, indicates a close relationship. In
marsupials, an analogous development can be discerned. That relationship was put
into words by the Australian group as follows: ‘‘In conclusion, androgenic
blockade in rodents reveals a close link between mammary and gubernacular
development, which is also present in marsupials, which are very distantly related
in evolution. Given the preservation of this developmental process over such a
wide range of species, it suggests that the mammary line even in humans might be
important for testicular descent and may hold the key to the aetiology of crypt-
orchidism in children [47].’’ That the mammary line is related to gubernaculum
migration is also supported by the fibroblasts from the fat pads related to the
mammary line. Only the parts of the fat pad related to the gubernaculum motion
line expressed androgen receptors in their fibroblasts. How the relation between
the genitofemoral nerve, androgen receptor-positive fibroblasts and the tip of the
gubernaculum is, is still under research [48].
So, the testis descent is dependent on the genitofemoral nerve, needs growth
factors as present in limb buds, and needs the mammary line signaling to follow its
pathway downward. These are really surprising results, which demonstrate a new
extension into the understanding of testis descent.
One should expect that hormone therapy as applied clinically should be
effective. Due to the fact that the gubernaculum is wrongly placed in over 80 % of
cryptorchidism cases, hormone therapy does not work to increase or restart the
testis descent in most cases. Wrongly placed is near or at the inguinal ring. It
therefore is inevitable till now that ‘‘early surgical correction rather than hormonal
therapy is warranted in boys with cryptorchid testis [49].’’ There is only one small
problem: ‘‘The most distal, subcutaneous part of the gubernaculums inserts into
the symphyseal region [40].’’ Thus, not in the scrotum and that discussion is
decennials old [50].
The surgical approach of maldescensus of the testis started in 1881, when the
first successful operation was carried out by Max Schüller of Munich.
(Anglo-Saxon literature claims the first successful orchiopexy in 1877 by
Thomas Annandale (1838–1907). The Europeans reported 1881 [50].) The main
problem was to overcome the shortness of structures adhered to the testis, espe-
cially the mobilization and lengthening of the spermatic cord. If the correct length
has been reached, the testis can be fixed in the scrotum: fixing the testis in
the scrotum is called orchidopexy. All kinds of methods were used to obtain the
elongation of the spermatic cord. Fixing the testis outside the scrotum into the
thigh, or strips of the connective fascia of upper leg muscles sutured to the testis,
or the use of rubber bands adhered to thigh and testis to control the traction for
elongation. Even stiff silver wire placed between the testis and lower abdomen was
employed. Blood vessels to the testis could be cut, because collateral circulation

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270 10 The Subperitoneal and Lower Retroperitoneal Space

was discovered, for example, from the arteries supplying the ductus deferens and
cremaster muscle. This added to a tension-free lowering of the testis, although the
risk of testicular degeneration, resulting in atrophy, was known. Over and over,
new approaches and techniques were developed. Around 1980 nearly 1,000 pub-
lications had occurred in the literature. From 1935 on, hormonal treatment with
testosterone as well as synthetic androgens became available. Not earlier than
1938, testis descent by androgen treatment succeeded for the first time [49A], but
later it turned out only well in a restricted amount of cases.
Another androgen therapy has a history with an intriguing course. Androgen
therapy was carried out in old men, simply because nineteenth-century research
indicated revival of youth, called rejuvenation. It was started by Edouard Brown-
Séquard (1817–1894). As one of the founders of endocrinology, he experimented
with injection of semen in experimental animals. After noticing his own aging
process, he put in animal testicular extracts subcutaneously. He presented his
results at the Société de Biologie. In modern terms, he only reported placebo
effects. A series of following scientists applied monkey testis transplants at the
19–20th millennium turning. Eugen Steinach (1861–1944) and Serge Voronoff
(1866–1951) are the best known. Steinach who studied sexual dimorphism con-
cluded from his research that a surgical ligature of the spermatic ducts increased
the hormonal production of the testis in elder men, called the ‘‘autoplastic’’
treatment of aging.
The Americans, of course, took over the method. To get human testes, testes
were taken from suicide cases and executed criminals. Not the least were under the
European patients: Sigmund Freud (1856–1939) and William Butler Yeats
(1865–1939). The rejuvenating doctors were ridiculed in novels and caricatures in
journals. Vasoligation and testis transplantation ended toward the 1940s. Still
testosterone application for older men is ‘‘hot’’ according to the ongoing discus-
sion about: climacterium virile and partial androgen deficiency syndrome in aging
man [51].
Out of the scope of this part are vasectomy and the male pill. Male sterilization
is proclaimed harmless, although relations with prostate cancer are described in the
USA, but totally denied in European studies [52]. The same holds for athero-
sclerosis, increased presence in monkeys, but the effect is absent in humans after
sterilization. Androgen like and anti-androgen-like substances should play an
important role in the male pill and, although in development, clinical application is
not yet described [53] on the moment of writing this part.

10.5 The Subperitoneal Blood Vessels and Ligaments


in the Female

The gubernaculum stays adhered to the ovary and is transformed into ligaments
(Fig. 10.8). One of the ligaments thus formed is the round ligament stretching
from the top of the uterus into the labia majora (the equivalent of the scrotum).

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10.5 The Subperitoneal Blood Vessels and Ligaments in the Female 271

The upper part constructs the ovarian ligament, called ligamentum ovari proprii,
going from the uterus–tuba edge into the upper part of the ovary. The cranial
suspensory ligament finally degenerates and is replaced by a fold made by the
ovarian vessels, also called the suspensory ligament [40].

10.5.1 Blood Vessels and Peritoneal Fluid

All the ligaments and female genital structures are covered with peritoneum. ‘‘The
anatomist pur sang will probably frown when an ill-defined part of the peritoneal
cavity in the vicinity of ovaries and fallopian tubes is included in a discourse on
the human female genital tract. However, there are some arguments to do just
that’’ [54]. Is the human egg passed directly into the fallopian tubes or is it
projected into the peritoneal cavity and caught by the fimbriae (fringes at the end)
of the fallopian tubes? Substances such as dyes and inert small particles injected in
the peritoneal fluid are transported rather fast into the vagina. Moreover, ‘‘trans-
peritoneal migration of the ovum is feasible, as shown by the occurrence of
pregnancies in the tube contralateral to the ovary containing the corpus luteum
(scar of the released egg in the ovary, addition ours) [54]’’ and ‘‘the clinical
experience that peritoneal adhesions which restrict tubal and ovarian motility can
be associated with subfertility constitutes another reason to discuss utero-tubal
phenomena at the peritoneal level in relation to reproductive physiology [54].’’
Thus, the human egg is transported from the ovary into the peritoneal cavity,
and from there, it adheres to the tubal fimbriae and will be transferred toward the
uterus. To transpose: in females, there is an open connection via vagina, uterus,
tuba, that ends into the peritoneal cavity.
Now, the question arises if the fluid within the peritoneal cavity contributes to
the well preservation of the egg, as it passes from ovary, via peritoneal cavity into
the tuba. The lowest peritoneal cavity part in females, where peritoneal fluid
collects, is in between rectum and uterus, called the cavum Douglasi or excavatio
rectouterina or cul-de-sac. Already in 1970s, a Dutch gynecologist in Edinburgh,
under supervision of the head of the department of Obstetrics and Gynaecology of
the Royal Infirmary, collected peritoneal, tubal, and uteral fluid to study the
protein, progesterone, and estrogen contents of peritoneal fluid from the cavum
Douglasi in females and connected the results to the menstrual cycle. The peri-
toneal fluid as compared to the plasma content of blood showed: ‘‘Despite marked
changes in volume, the total protein content of the peritoneal fluid (ca. 60 % of the
concentration measured in plasma) remained fairly constant throughout the cycle,
although a slightly, but significantly, lower value was found in the late prolifer-
ative phase. After ovulation, the concentration of oestradiol and progesterone in
the peritoneal fluid was higher than in plasma in the majority of cases, suggesting
that some follicular fluid drains into the peritoneal cavity at that time. Proges-
terone, in contrast to oestradiol, was also found in higher concentrations in peri-
toneal fluid than in plasma before ovulation [54].’’ The fluid surrounding the egg

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272 10 The Subperitoneal and Lower Retroperitoneal Space

is, after its release of the ovary, brought into the peritoneal cavity, but cannot count
for the 18 ml fluid found at that moment in the peritoneal cavity. The content of
peritoneal fluid varied from 1 to 2 ml at the start of the cycle to around 18 ml
around ovulation and toward 3–5 ml at the end of the cycle. Presumably, the
permeability of the blood vessels is changed. Perhaps it is the effect of oestradiol,
with the consequence of changes in ‘‘inflow and outflow equilibrium [54]’’ of the
peritoneal membrane. The collection of fluid was rather exact: Afterward, 10 ml
saline was administered, and the patient was shifted twice in position, brought
back to the original position (Trendelenburg to anti-Trendelenburg), and the fluid
collected again: recovered volume 10.04 ml ± 0.21 (SD).
Although initially ovary exudates were held responsible for the pelvic fluid
[55], this was later on denied and the original conclusion supported that blood
vessels are responsible [55A]. It appeared that the molecular weight of the sub-
stances found in peritoneal fluid decides the pelvic fluid content by a changed
permeability factor [55A]. ‘‘The concentrations of the various proteins and protein
fractions in the peritoneal fluid depend predominantly on the hydrostatic pressure
in the ovarian capillary network, the diameter of the endothelial gaps, the electrical
charge of the individual proteins, and their molecular weight. Proteins with a low
molecular weight pass through the capillary wall more easily than those with a
high molecular weight [55A].’’ The pelvic blood vessels determine the composi-
tion of the peritoneal fluid.
The tissue lining the inside of the uterus is sometimes localized outside the
uterus. This is called endometriosis. It can reach the peritoneal cavity and causes
infertility and pain. ‘‘The current consensus is that endometriosis is a local pelvic
inflammatory process with altered function of immune-related cells in the peri-
toneal environment. Supporting this concept are recent studies suggesting that the
peritoneal fluid of women with endometriosis contains an increased number of
activated macrophages that secrete various local products, such as growth factors,
cytokines and possibly free oxygen radicals [56].’’ The macrophages that are
responsible for the destruction of sperm that reaches the peritoneal cavity are now
upregulated producing substances that help the endometrial cells to survive within
the pelvic cavity. Intrapelvic embryos or intrapelvic young fetuses are regularly
reported in weekly journals. A fertilized ovum, not caught by the fimbriae of the
tuba and thus present in the pelvic cavity, can develop, due to contact with the
pelvic peritoneal membrane. Pelvic membrane and pelvic cells do provide growth
capacities. The increase in inflammatory cells, macrophages together with eosin-
ophilic and neutrophilic blood cells, organizes oxidative stress in endometriosis.
This oxidative stress seemingly activates the supporting capacity to let endometrial
cells survive within the pelvic cavity [56].
The conclusion is inevitable: Pelvic blood vessels should not only be studied in
relation to pelvic organs but also with respect to the peritoneum.
All blood vessels for the female genital organs are placed within the double
blades of the peritoneum: one blade coming up from the bladder, going over the
tuba and round ligament, continuing in a blade descending toward the rectum. This
folded peritoneum is called the broad ligament. It stretches toward the side walls of

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10.5 The Subperitoneal Blood Vessels and Ligaments in the Female 273

Fig. 10.9 Blood vessels of


uterus, tuba and ovary and
their relations to the
peritoneum. Along the
vertical lines, a section is 5
6
made, represented below.
Ligaments of the uterus are
depicted in purple, and ovary
and ovarian ligaments are
depicted in blue. Blood
vessels and tuba are in red.
The peritoneum has been
colored green and is depicted
one sided. 1 round ligament, 1
2 tuba, 3 ovary, 4 cardinal
ligament, 5 ramus ovaricus, 2
ovary branch of uterine
artery, 6 ovarian artery
 E. Marani
3

the pelvis, where it adheres to the inner fascia blades of abdomen and pelvis. The
arteries, placed between the folded peritoneum, are supported by ligaments, also
between the folded peritoneum, to reach the organs (Fig. 10.9). The arteria uterina
goes over the cardinal ligament, which supports the cervix, and the artery for the
ovary uses the suspensory ligament. The extension of the uterine artery reaches the
own ligament of the ovary. Over this ligament, this branch, called ramus ovaricus,
supplies the ovary with blood. The ovary thus has a double supply of blood
(Fig. 10.9, left side). Now, note that in Fig. 10.9, the tuba is left blanco, which of
course is impossible, and each organ needs blood supply. It is because the fallopian
tube also uses the double blood supply of the ovary that is extensively depicted in
Fig. 10.10.
These blood vessels are important in sterilization operations. Three types of
operations are discerned here: (1) electrocoagulation of the tuba, (2) making a
tubal U, putting ligatures on both legs and in between both ligatures a cut or taking
out the part of the tuba in between both ligatures (Pomeroy technique), and last but
not least, (3) putting a clip on the tuba. In all three techniques, tubal blood flow is
locally damaged. Electrocoagulation is the most simple to discuss: ‘‘Tubal ster-
ilization by electrocoagulation is very likely to have an adverse effect on the
ovarian reserve in the postoperative period [58].’’ The coagulation field is difficult
to estimate during operation, and therefore, extra damage can easily occur. Since
such a strong collateralization of blood vessels between tuba and ovary is present,
one should not expect serious blood flow damage to the ovary. The contrary seems
true for the Pomeroy technique: ‘‘post bilateral tubal ligation by the Pomeroy

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274 10 The Subperitoneal and Lower Retroperitoneal Space

Fig. 10.10 Arteries of tuba


and ovary. a Normal
distribution viewed from the
backside. b Variation viewed
from the backside. c Detail at
the uteral angle viewed from
the front. d Arcades around
the tuba and the tubal
branches. 1 arcades around
tuba, 2 middle tubal artery,
3 medial tubal artery,
4 retrograde artery to the
front of the uterus, 5 medial
ovary artery, 6 lateral ovary
artery, 7 lateral tubal artery,
8 ovary artery, 9 ramus
ovaricus (reproduced with
permission from Kamina
[57])

technique may acquire an ovarian polycystic appearance and increased ovarian


pulsatility index, which may be associated with a tendency to develop post tubal
ligation symptoms [58].’’ The poststerilization syndrome arrives after five years by
menstrual irregularities, but earlier ‘‘dysfunctional uterine bleeding, dysmenor-
rhea, dyspareunia (painful coitus), exacerbation of premenstrual symptoms and
pelvic pain [58]’’ can be present. The literature is not equivocal: Short-term studies
do not find these aberrations, but a large multi-center study in the USA ascertained
the existence of sterilization menstrual effects, which were confirmed for clip
sterilizations by a later study [59]. Causes are not clear, and a series of reasons
were proposed among which the disturbed blood supply to the ovary concerning
both veins, followers of arteries in their trajectory, and arteries. After sterilization,
menstrual cycle changes and a good cause could be disturbance of the ovary blood
supply: ‘‘Pelvic venography performed in women following tubal ligation has
demonstrated the appearance of uterovaginal and ovarian varicosities [58].’’ These
studies are not without importance if one knows that 190 million couples

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10.5 The Subperitoneal Blood Vessels and Ligaments in the Female 275

Table 10.3 Extrapolated results on menstrual heavy periods and pelvic pain for the world
population of tubal sterilized women
Before sterilization (million) After sterilization (million)
Menstrual heavy periods 17 66
Pelvic pain 17 39

worldwide use sterilization by cutting or clipping. An increase of heavy menstrual


periods was noted in 26 % and increase in pain in 12 % of the 573 women studied
after clip sterilization with a long follow-up [59].
Congestion is ‘‘an excessive accumulation of blood in an organ [60]’’ and often
correlated with a reduced blood flow. Pelvic venous congestion, by severely
dilated veins, occurs after sterilization and produces pelvic pain. In such patients,
the peritoneal fluid was studied: The amount of fluid was 2–3 times higher, and
one type of prostaglandins was markedly higher compared to the control groups.
Normal vascular tone is also regulated by prostaglandins. Hypoxemia, followed by
tissue damage, induces prostaglandin production that makes pain nerves more
active and relaxes the vessel walls, thus vasodilatation and thus extra reduction in
blood flow. ‘‘It is estimated that high prostaglandins in peritoneal fluid may be
secondary to vascular stasis, simultaneously the latter be exacerbated by higher
prostaglandins, all of these make a vicious circle in attack of pelvic congestion
[60].’’
Now, the main question is, is the sterilization syndrome occurring frequently?
At least the guidelines of the American and Great Britain Colleges of Gynecology
and Obstetrics denied the substantial risk on menstrual problems after tubal ster-
ilization. There is no clear-cut epidemiologic study for the sterilization syndrome,
mainly because the syndrome itself is questioned. Therefore, the only thing one
can do is to extrapolate the outcome from a prospective cohort study [59] to the
world situation. Of course, it is not allowed: too many differences in presteril-
ization conception techniques, differences in applied operation techniques, varia-
tions in way of inquiries, and so on. Nevertheless, let us do this for the sake of
190 million sterilized women (Table 10.3).
So, if the syndrome exists, at least a women population as large as the whole of
France is involved and a women population as large as Spain acquires menstrual
heavy periods after tubal sterilization. We will not repeat this comparison for
pelvic pain. Perhaps the gynecologists and obstetricians could spend some extra
time on the existence of the sterilization syndrome and look into the anatomy of
the blood vessel organization of tuba and ovary, whether or not related to this
problem.
Before one starts believing that tubal sterilization has solely disadvantages
beside anticonception, the risk on ovarian cancer is lower [61]. Already early in
the 1980s, research indicated that the risk of a hysterectomy is at least three times
higher for women with tubal sterilization compared to women without a sterili-
zation operation. Causes for it are rather unknown, but heavy menstrual bleeding is
one of them [62].

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276 10 The Subperitoneal and Lower Retroperitoneal Space

Fig. 10.11 View from medial toward lateral. Supra and infrapiriform foramen in blue and
piriform muscle striped. Section through lumbar vertebral column is in black. 1 common iliac
artery, 2 extern iliac artery, 3 intern iliac artery, 4 gluteal superior artery, 5 gluteal inferior artery,
6 obturator artery, 7 internal pudendal artery with branches for rectum, perineum and arteries for
the penile structures, 8 lateral umbilical artery, 9 superior vesical artery, 10 uterine artery, 11
inferior vesical or vaginal artery. Note that the epigastric vessels and sacral branches are not
depicted and small arterial branches, e.g., middle rectal artery. Moreover, a large variability in
vessels is present, e.g., obturator artery. Veins in general follow the artery pattern with great
variability too  E. Marani

10.5.2 Anastomoses: William Turner’s Subperitoneal


Arterial Plexus

In Fig. 10.11, the ground plan of the pelvic blood vessel supply is given by the
main arteries. Aging brings atherosclerosis with the consequence of closure of
these main vessels. Closure of the external iliac artery should mean that the leg is
devoided of arterial blood. Amputation is the outcome, unless other ways of blood
supply can be organized. The whole pelvis is abundantly provided with collateral
connections. It does not matter what organ or structure discussed; collateral cir-
culation is present. They originate mainly from vessels outside the pelvis: the
ovary artery, the external iliac artery just leaving the pelvis, the upper rectal artery
that originates already in the abdomen, and the arteries for the sacrum that orig-
inate at the dead end of the aorta. Even the femoral artery contributes by a branch
directly after its origin (the deep inguinal artery). Let us treat one example. Closing
the external iliac artery after the branching of the internal iliac artery organizes the
internal iliac artery to take over and via the inferior and superior gluteal artery, the
obturator artery and the pudendal artery reach the femoral artery. These collateral
circulations are studied well in the literature; however, the variability in the ground
plan is surprising. One cannot predict the outcome.

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10.5 The Subperitoneal Blood Vessels and Ligaments in the Female 277

Sir William Turner (1832–1916) studied medicine and became Senior Dem-
onstrator for Anatomy at the Edinburg University. After his Bachelor of Medicine
study in London, he stayed in the anatomy discipline. He had several important
functions in the Edinburg University among them Principal. He was President of
the General Medical Council and Fellow of the Royal Society in London. He
published over 200 articles and started the Journal of Anatomy and Physiology
together with George Murray Humphry in 1865 [63]. You hardly can overlook the
man, but you can forget his results, as happened.
William Turner, after injecting colored gelatin in retroperitoneal blood vessels,
detected all kinds of collateral connections that stretched from the diaphragm into
the pelvis. Thus, a rich plexus of collaterals, described as the ‘‘subperitoneal
arterial plexus,’’ was found (subperitoneal meaning here behind the peritoneum).
‘‘Taking the location and extent of the sub-peritoneal arterial plexus from the
pelvis to the diaphragm into account, it seems that the sub-peritoneal arterial
plexus may serve as a route for the spread and dissemination of gastrointestinal
malignancies to the retroperitoneum and pelvis and vice versa [63].’’ Metastasis of
colorectal cancers to the kidney, ovarian cancers to the kidney, from kidney to
testes, to ovaries and to spermatic cord is described see for references [63]. ‘‘After
this plexus was first described in 1863, it was seldom mentioned by name in later
publications, although a number of authors during recent decades have pointed out
the existence and importance of such arterial anastomoses [63].’’ Well hidden into
the retro- and subperitoneal fat, it was totally forgotten and revived by modern
vascular radiology.
Thus, not only collateral circulation within the pelvis is present, but also this
pelvic collateral circulation is connected to an analogous system in the retro-
peritoneal area: a whole collateral circulation reaching from retroperitoneal to
subperitoneal space. For metastasis holds: The subperitoneal arterial plexus is
interwoven with the lymphatic system, since this collateral system also provides
blood vessels to most pelvic and abdominal lymph nodes.
Collateral circulations also play an important role in pelvic aneurysms. Aneu-
rysm is the bulging out of the blood vessel, everywhere where the vessel wall is
weak. Aneurysms are mainly found at the common, external, and internal iliac
arteries. Placing of a prosthesis or a bypass should help the blood flow to return to
normal. If one looks again to Fig. 10.11, it should be noted that closure of the
internal iliac artery (3 in the figure) will disturb the blood flow toward the buttock
with its gluteal muscular mass. The effect is proximal claudication or buttock
claudication. Thus, reopening by a vascular graft or prosthesis of the external or
common iliac arteries saves the upper leg/buttock, but it is often overlooked
whether the patient also has intern iliac difficulties or not. Still it is possible to
carry out the needed embolization of the internal iliac artery in such bypass
operations. The collateral circulation normally will take over. However, ‘‘Iatro-
genic occlusion of the internal iliac artery can result in severe complications,
including buttock ischaemia, rectosigmoid ischemia or sexual dysfunction. In
unusual cases, severe gluteal necrosis may occur [64].’’

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278 10 The Subperitoneal and Lower Retroperitoneal Space

Also in what is called lower limb artery occlusive disease, intern iliac artery
bypass is used due to the occurrence of proximal claudicatio. This disease is
present in 1 % of the Western population of 50 years going up to 20 % in those
that reach 70 years of age. Especially, in patients that have an aortobifemoral
operation, 30 % will demonstrate proximal claudicatio [65], which is under-
standable since both internal iliac arteries could be or are in a severe state of
occlusion too. In such cases, the collateral circulation is seriously hampered. Thus,
although the body organized safety measure to ensure the blood flow in and around
the pelvis, its borders are reached during aging.
In reference lists, literature can be grouped. In case of citation, the article
involved is indicated by the reference number and a capital letter.

Literature

Literature has been grouped in reference lists of several chapters in those cases where
arguments are difficult to entangle or published over several articles or books. In cases of
citation the article or book involved is indicated by the reference number together with a
capital Arabic letter.
1. Smith H (1892) Subperitoneal hysterectomy. The Lancet, 20 Feb 1892
2. Yijang Z, Qunxi C, Weiling W (2006) Closure vs non-closure of the peritoneum at
cesarean delivery. Int J Gynecol Obstetr 94:103–109
3. Tulandi T, Al-Jaroudi D (2003) Nonclosure of peritoneum: a reappraisal. Am J Obstet
Gynecol 189:609–612
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Chapter 11
Vision and Waist-to-Hip Ratio

The pelvis plays a central role in the human mating process. Sexual arousal also
starts by the pelvic contours, in fact by the waist-to-hip ratio. Men determine the
fitness of a female by this ratio. Added visual information of the face strengthens
the pelvic sexual arousal. The waist-to-hip ratio is codetermined by buttock fat and
muscles. The buttock fat distribution is gender depended and has consequences for
gait performance and recognition of persons.

11.1 Introduction

Buytendijk, a Dutch professor of physiology and psychology, wrote ‘‘de vrouw’’


(the female) [1], in which he pointed out the connection between personality and
perception. One of his remarks is that optical orientation is different in females and
males in experimental situations. Female subjects supposedly perceive less
objectively and less analytically than male subjects. However, females scored
equal to or better than men after repetition of the optical experiments. On the other
hand, together with the mouth, eyes are the strongest, developed mimic and
physiognomic connectors in human contact. ‘‘They are not only the expression of
mood and feelings, but are also indications, in their own language, of what a
person deliberately or thoughtlessly will say’’ [1]. The female eye is more widely
open (so-called basedoïde type) and smaller deep set eyes are more male-like
(tetanoïde type) [1]. Indications of emotions and mood can be expressed by, e.g.,
lowering one eyes, veiled eyes, nervously blinking, and predator eyes. All do show
the richness of the expression level of the eye and its coherence with construction
and mimics of the eye area [1]. So visual perception has gender-specific charac-
teristics, eyes can speak in their own way and send out a whole spectrum of
messages. But why vision in a book about the pelvis? It turns out that observing
the waist-to-hip relation, which is determined by the pelvis is rather important for
sexual functioning.

E. Marani and W. F.R.M. Koch, The Pelvis, 283


DOI: 10.1007/978-3-642-40006-3_11,  Springer-Verlag Berlin Heidelberg 2014

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284 11 Vision and Waist-to-Hip Ratio

11.2 The Hidden Role of the Pelvis in Sexual Arousal


and Mating

The importance of the eyes in sexual functioning leads us to the veils, burqa, or
niqab: a body veil with an eye-slit covering the face [3]. We can rest at ease, a
niqab does not interfere with driving a car [4], although in France it is forbidden,
because it is considered to be dangerous there, and Kuwait intended such a law,
but it was never put forward.
In ‘‘This weeks debate: Religious attire’’ in USA today of June 4–12, 2010, the
editor’s view is put next to P. Vimont’s on the French ban on full-face veils [3].
USA today
• Veil-banning is an expression of European fright about Islam.
• The debate is just another French anomaly, akin to its worries about the cultural
impact of Disney or Mc Donalds.
• European countries lack America’s knack for assimilating immigrants.
• Europeans are banning peaceful Muslim religious practice, driving youngsters to
radicalism.
• Only 1,900 women in France wear veils. ‘‘This is a threat?’’
• Telling women what they can wear is unjust.
P. Vimont’s arguments
• Veils are only banned in public schools and government services.
• Three concerns deserve a fair analysis:
1. Human dignity and fundamental rights. Full-face veils jeopardize the rec-
ognition and one’s individual identity.
2. Integration is hampered and cuts women off from all contacts.
3. Hiding one’s face and body represents a security challenge.
Although a two-fisted discussion (there is a lot more in news papers), a simple
point is overlooked. It is senseless to deny that males are sensitive to female facial
traits and vice versa, whether emotional and/or sexual. In this context, the veil is
not related to freedom alone, but it is also the expression of a different social
approach of male–female interrelations. Perhaps this is too subtle a detail in the
political discussions, in which the veil is a sign of female suppression, but it is
important in our approach. The purpose of the burqa or niqab is to suppress desire
of man or hide the attractiveness of females. In most cases, it leaves the eyes free,
but they can be covered by a net to make even the eyes invisible. So the question
arises, if only eyes are visible, what kind of information can still be sent out from
the women’s faces, information that is emotional or attractive and what can men or
children perceive still?
The Koran says: ‘‘Enjoin believing women to turn their eyes away of temptation
and to preserve their chastity; to cover their adornments (except such as normally
displayed); to draw their veils over their bosoms and not to reveal their finery except

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11.2 The Hidden Role of the Pelvis in Sexual Arousal and Mating 285

to their husbands, their fathers, their husband’s fathers, their sons, their step-sons,
their brothers, their brother’s sons, their sisters’ sons, their women servants, and
their slave-girls; male attendants lacking in natural vigor and children who have
carnal knowledge of women. And let them not stamp their feet in walking so as to
reveal their hidden trinkets’’ [2]. Women’s body beauty and attractive appearance
should be covered and reserved for special groups of relatives and servants. There is
no discussion that the veil is related to suppressing ‘‘female attractiveness’’ toward
strangers. Immediately at the onset of puberty, the veil should be used: ‘‘A Muslim
woman is obliged to wear hijab as soon as she reaches puberty’’ [3], clearly based
on arguments from Muslim believers. The hijab is a veil that covers the head, but
not the face. Note that it does not say burqa or niqab.
Education is also related to facial expression. In the case of Mrs. Azmi, a
teacher of mathematics and English at a bilingual Muslim school in England, the
head teacher noticed ‘‘that pupils sought visual clues from Azmi which they could
not obtain because they could not see her facial expressions…’’ [3]. Comparable
arguments have been put forward for high schools and universities in relation to
effective pedagogy [3], especially ‘‘to establish eye contact in asking and
responding to questions’’ [3]. The Egyptian Supreme Constitutional Court on
Islamic Law denied that the veil should cover the face and hand palms, based on
the Prophet’s citation [3] and female students are forbidden to wear the niqab at
school [3]. Moreover, for children that are taught before the age of puberty, at
school, there is no need to veil by the teacher (see Koran citation) [3]. In general,
different religious interpretations are presented about the wearing of a niqab in the
Muslim world, from not necessary at all to obligatory [3]. Covering the face does
indeed interfere with perceiving mimic expressions that are an integrated part of
communication between humans and this is the intention of burqa or niqab.

11.3 Visual Sexual Information

This part on visual clues directs itself to general sexual arousal by vision [5],
followed by visual information in mate choice and ending with visual information
by eye pupil tracking. Sexual arousal by visual stimuli (pornographic films, videos,
or photographs) is different for the male than female. A series of factors such as
sexual motivation, gender role expectations, and sexual attitudes, but also the
hormonal stage of the female cycle, does influence visual sexual arousal. The
literature shows in general that females respond less to visual sexual stimuli than
men do. In general, females take more notice of the situation around the sex
presentation itself. If that surrounding is removed, the effect is the same. Women
respond more to woman-made films than to man-made films, but men react more
to both types than women do, although men preferred man-made films. ‘‘There-
fore, it appears that men and women have different strategies when viewing visual
sexual stimuli’’ [5]. Why is not known, although the non-sexual details are con-
sidered responsible [5]. In men, a direct relation with testosterone is assumed,

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286 11 Vision and Waist-to-Hip Ratio

since hypogonadal men normally do not respond with arousal, but do if testos-
terone is administered. But testosterone also influences women’s responses;
addition of testosterone increases ‘‘lust’’ [5], and arousal reactions to erotic videos.
Females prefer masculine face traits during their ovulatory period, while during
other phases of the female cycle, this preference is nearly absent. Feminine male
faces are favored during the luteal phase. These results are related to the woman’s
main reproductive concern: ‘‘Although males with more masculine features may
provide genes with higher fitness, masculine males are less likely to invest in
offspring and enter partnered relationships. At ovulation, when conception is
likely, women may prioritize acquiring fit genes and be more attracted to mas-
culine men. During the luteal phase, in contrast, when hormones are preparing for
potential pregnancy, the priority may shift from mating with masculine males to
finding a stable partner who can provide more parental investment and resources’’
[5]. The cognitive female reactions, as studied by means of EEG or NMRI, are
indeed hormonal dependent. Some studies did not take into account whether
females used the pill or not and therefore, possibly, overlooked the effects of oral
contraception on their results. As a consequence, results are highly variable.
Males and females react equally to smiling or angry faces, independent whether
the faces are male or female. A simple measure is an EMG of ‘‘frowning’’ (cor-
rugators muscle activity) in cases of angry faces and ‘‘smiling’’ (zygomatic muscle
activity) in cases of friendly faces. Facial expressions are biological prewired and
directly related to emotional activity. However, the reaction of females is stronger,
especially to happy faces. So, equal reactions but more intense in women in a
spontaneous situation [12]. (Gender reactions to neutral faces are still in debate
[12]). The inescapable conclusion is that perceiving visual sexual stimuli is dif-
ferent from noticing other visual stimuli.
But let us first look to another aspect of visual sexual stimuli. It will look as if
contradiction rules. There is a difference between sexual arousal and sexual ori-
entation. ‘‘.. a man’s category specific sexual arousal pattern is his sexual orien-
tation. Most women lack this strong directional motivation, and so it is not
surprising that their sexual behavior is more malleable and sexually fluid’’ [8]. One
could simply say that man is unisexual directed (toward females in heterosexuals
and toward males in homosexuals), while females are bisexually directed. Thus, for
heterosexual females, arousal can occur by both male and female sexual stimuli.
Mate selection decisions are mainly influenced, at its start, by visual infor-
mation. ‘‘In evolutionary terms, humans face a pair of reproductive problems in
which only a small subset of all possible solutions can lead to genetic posterity:
how to signal one’s value on the mating market and how to evaluate the signals of
others’’ [7]. The driving force in mate choice is sexual arousal, as the consequence
of the sexual orientation of the man, of course, by the attractiveness of the woman
in heterosexuals. So the first point is: what is female attractiveness. The rest of the
body is of lesser importance: It is indeed the female breast and the female waist-to-
hip ratio that matters). In general, when men look at a picture of a nude female
with large breasts, they fixate more on the breasts, than on the midriff (=waist) and
least on the head during the first two seconds. And the dwell time relates the same:

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11.3 Visual Sexual Information 287

longest for the breasts, then midriff and finally the head during the first three
seconds. ‘‘Despite the large amount of attention paid to the breast area, it was the
waist-to-hip ratio that primarily determined male ratings of female attractiveness’’
[9]. One should note that the body mass index (height versus weight) is as good a
criterion as the waist-to-hip ratio. So the man looks often and long at the breasts,
but decides on the information he gets from the waist-to-hip relation and he makes
that decision in a rather short time, compared to the time spent on the breasts [9].
This research used manipulated photographs of nude women with the same face.

11.4 The Face and Sex

Normally, we do not meet a nude man or woman during our social contacts. So
there are other noticeable marks that influence mate selection. They are, among
others, partner status and face. ‘‘Relationship commitment in women suppresses
interest in alternative partners’’ [10]. Male partners reacted to opposite-sex face
photographs independently of their existing relationship [10]. Seemingly, females,
after obtaining a partner on the mating market, loose interest in other possible
candidates. This process of mate selection is controlled by the woman. She decides
how far the start goes and under what conditions it will be carried forward [11] and
will progress. One should note: ‘‘Somewhat contrary to stereotypical assumptions,
men ‘fall in love’ more readily; women are more cautious. On the other hand,
women are more likely to report being in love on their first experience of sexual
intercourse. The type of ‘love’ experienced differs to some extent, with women
being more likely to experience companionate love and men passionate love’’ [11].
The question ‘‘What makes a face attractive’’ [12] has been studied frequently.
Three main characteristics emerged: averageness, symmetry, and sexual dimor-
phism. There are of course other characteristics (pleasant expression, youthfulness,
liking a person [12]), but most studies looked for attractiveness, assuming that a
general aesthetic blueprint is present for it. Averageness is the intersection of facial
characteristics of a population. It became evident that the more average a face is,
the more attractive it is perceived. In other words, a more ‘‘common’’ face for that
population is more attractive. There are indications that this also holds for non-
Western populations and no difference has been found between men and women in
this respect. Symmetry contributes to attractiveness, and significant gender or race
differences are absent. Sexual dimorphism is the fact that female faces are different
from male ones, induced genetically and hormonally. Feminine characteristics
(small chin, full lips, and high cheekbones) are attractive and are race independent.
Masculine facial characteristics do contribute to attractiveness but clearly less than
facial femininity. Therefore, mate choices are made by average, symmetry and
masculine traits of the man, and in female, faces averageness and symmetry are
attractive. Femininity is preferred over averageness in female faces. Normally,
these characteristics are race independent, but presumably not for masculine
preferences [12].

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288 11 Vision and Waist-to-Hip Ratio

In his book ‘‘The naked ape’’ [13], the zoologist Desmond Morris advocates the
view that mimicking of the face is of utmost importance in the start of mate
selection, supported by the fact that humans have the best developed and most
complex mimic muscle system of all primates. The vast majority of Morris’
colleagues agree with him. So, we have seen what constitutes an attractive face
and with this face humans are capable of sending emotional and sexual messages
by means of our mimic muscles. Together they start the game of mate selection.
First market values are tested mainly by facial information, then sexual arousal is
induced, followed eventually by couple formation, with sexual intercourse as the
end phase. Vision is the mediator of the beginning of this process. The remark of
Morris that the breasts are a mirror image of the buttocks necessitates that attention
will be paid to the buttocks later on.

11.5 The Enlargement of Pupils

Sexual arousal coincides with pupil enlargement ‘‘and we react to it perhaps more
than we realize’’ [13]. Eckhard Hess already described the role of pupil size in
1965 and 1975 in Scientific American [14]. Dilated or constricted pupils make a
difference. Age differences determine whether a large pupil is found to express
happiness more than constricted pupils. Individuals older than 14 years will
interpret large pupils to signify a significantly happier person (Fig. 11.1).
Men unconsciously will choose female faces with large pupils as being more
feminine, as females do with photographs of males with dilated pupils (Fig. 11.2).
Women in the Middle Ages already knew about the effect of large pupils, because
females used the sap of Atropa belladonna (deadly nightshade). It contains atro-
pine that causes pupil dilation, due to its anticholinergic, sympathetic action. When

Fig. 11.1 Up to 14 years, no


difference between faces with
small pupils (gray bars) and
faces with large pupils (black
bars) was noted, from Hess
[14A]. (Reproduced with
permission. Copyright
 1975 Scientific American,
Inc. All rights reserved)

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11.5 The Enlargement of Pupils 289

Fig. 11.2 Schematic eyes


containing small, medium,
and large pupils. Gray bars
are for men, black bars for
women. ‘‘The paired eyes
with the largest pupils caused
the largest dilation in the size
of the subjects’ pupils,’’ from
Hess [14A]. (Reproduced
with permission. Copyright
 1975 Scientific American,
Inc. All rights reserved)

used regularly, it can even cause blindness eventually. Men are hardly interested in
photographs of their own sex with small or large pupils. However, women reacted
less to photographs of women with large pupils than those with small pupils.
The conclusion of Fig. 11.2 is that the viewer will react to large pupils auto-
matically with dilation of his or her own pupils. ‘‘The fact that even a pair of
schematic eyes will give rise to a dilation of the pupils suggests that the dilation
response is innate and not learned’’ [14]. So, if a woman in burqa or niqab sees an
attractive man, her pupils will dilate unconsciously. At the moment the man looks
at her seeing her large pupils, he will also react unconsciously by widening his
pupils; and so the first sexual visual contact is automatically established [15]. The
greater the distance the earlier eye contact will be established [16] (the eyes of
course must still be visible), and again the female cycle plays a role: large pupils
are preferentially liked by females in the follicular phase of the cycle [17]. Of
course, a comparable description can be given for men.

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290 11 Vision and Waist-to-Hip Ratio

11.6 Waist-to-Hip Ratio

The waist-to-hip ratio is important for mate selection, although men’s eyes linger
more on the breasts. The first sexual contact is unconsciously established by
vision. That is what we learned above. The waist-to-hip ratio is determined by the
pelvis but also by subcutaneous fat. Subcutaneous fat can be subdivided into a
superficial layer and a deep layer around abdomen and buttocks. In men, the deep
layer stops at the upper edge of the pelvis; in females, it goes beyond, over the
gluteus muscles [18]. This enlarges the hip region.
Through the centuries females have accentuated the waist-to-hip ratio (see
Fig. 11.3), not only by a bustle, but also using hoop skirts. ‘‘Likewise, modern
human females accentuate and call attention to the derriere by wearing tight skirts
and high heels, which emphasize the buttocks by puffing them out’’ [19]. This
indicates that this ratio has been important in time and over the past 30–120 years
waist-to hip ratio has changed little, even for Miss America winners and Playboy
playmates [20]. It is not only a question of fashion. The literature indicates that fat
on the female hips should indicate a good health and/or good receptivity, espe-
cially if the waist-to-hip ratio is 0.7. Females with such a ratio are found attractive
by men under the condition of normal body weight. Both overweight, as well as
underweight females with a ratio of 0.7 are less attractive, independent of the age
of men [20].
‘‘There is growing evidence indicating that waist-to-hip ratio is an accurate
somatic indicator of reproductive endocrinologic status and long-term health risk’’
[20]. Girls with a lower waist-to-hip ratio and matched body weight enter puberty
earlier, while ‘‘married woman with higher waist-to-hip ratio and lower body mass
index report having more difficulty becoming pregnant and have their first live
birth at a later age than married women with lower waist-to-hip ratios’’ [20]. High

Fig. 11.3 Extending the


waist-to-hip ratio by a bustle
in the nineteenth century
(reproduced with permission
from R. Joseph [19])

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11.6 Waist-to-Hip Ratio 291

levels of testosterone augment the waist-to-hip ratio, while estrogens lower it. This
is seemingly regulated via leptin, a hormone that is involved in control satiety and
adiposity by producing the feedback signal between the adipocytes and the
hypothalamus. Its different gender concentrations are presumably genetically
related and enhanced by the different postpubertal sex steroids in male and female
[20]. However, waist-to-hip ratio is found independent of leptin levels by some
authors, bringing the origin of this ratio into question [21]. So, fat distribution
around the pelvis is dependent on the hormonal situation and unconsciously sig-
nals, together with the pelvic size, to the male the woman’s reproductive quality
and also her health situation. Accentuating this ratio by fashion increases the
mating-market value of the female at first sight. Chadour, niqab, or burka, all take
away the vision on the waist-to-hip ratio, interfering with Muslim man’s mating
choice. If even the eyes are invisible, hidden by a net, any unconscious sexual
stimulus is made impossible for the male, but not for the female, thus forcing mate
selection to develop in another social context.
Let us dwell more upon the face before ending this part. Mature bodily traits
codetermined by the bony skull are present just before or around puberty, although
growth is still going on. The pelvis shows in its characteristics that the overall
pelvic shape is formed already at the start of the cartilaginous construction. Only
two shifts during development can be noticed: increase in the pelvic cavity and in
the sacral curvature, and these changes are developed before walking. ‘‘The shape
of the pelvis, thus, seems to precede the development of the locomotor function’’
[22]. Nevertheless, there are some characteristics that still can undergo changes by
the environment, e.g. the breath between the two trochanters. ‘‘Cultural factors
therefore played an important role in determining hip breath’’ [23], which brings
us back to the waist-to-hip ratio.
The conclusion is that female sexual attractiveness has to be determined in
normal life by face and waist-to-hip ratio. In Western society, both are evaluated
unconsciously by humans. Pupil enlargement is caused by these two parameters
and can consequently produce the first unconscious sign of sexual interest, based
on mutual pupil dilation. Therefore, the pelvis with its subcutaneous fat plays an
indispensable role in sexual arousal, but also signals health and reproduction
quality of the female by its contribution to the waist-to-hip ratio, a rather unex-
pected property of the pelvis.

11.7 Beautiful Buttocks and Vision

The waist-to-hip ratio is also (partly) determined by the buttocks. It appears that
each of us has an idea what constitutes beautiful buttocks, both for our own and for
the other sex. Both men and women look and discuss buttocks, especially of the
other sex. Desmond Morris supposed that early in human evolution, males were
attracted by the female buttocks accentuating the female genital zone. Vertical
sitting and upright posture together with facing the mating partner during the

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292 11 Vision and Waist-to-Hip Ratio

Fig. 11.4 Surgical lines and characteristics of the ideal buttocks (for explanation see text).
Reproduced with permission from Cuenca-Guerra and Quezada [24]

precoitus and coitus supposedly caused that the front of the body became visually
more important. As in the mandril and the galada-baboon, this caused a mirroring
of the female back onto the front, causing breasts and accentuation of the lips, the
last as a representation of the labia [13]. The conclusion is not that buttocks are
unimportant in sexual attraction, but that the front is equally, or even more,
important than the back. Beautiful buttocks are still important for humans. Plastic
surgeons do have to operate on buttocks and therefore needed a beauty model of
them. In the article ‘‘What makes buttocks beautiful,’’ an aesthetic analysis and a
classification of deviations from this beauty ideal are given [24].
Before we go on: Who determines the ideal buttock? In the article from Mexico
just cited, six certified plastic surgeons selected from 2,400 photographs of nude
women, 1,320 buttocks that were considered harmonious and beautiful. So plastic
surgeons determine what is beautiful and the plastic surgeons will diagnose and
will perform the operations. This is known as circular management within one’s
own profession! Moreover notice that only women were studied. Men are seem-
ingly excluded from having beautiful buttocks. It is nonsense to think that an ideal
of the buttocks exists: it differs from race to race, from culture to culture; it
changes over time and varies from person to person. A quick survey of Umberto
Eco’s Storia della Belleza (Story of beauty; 2004, Libri Bompiani) for the depicted
images of Venus through the ages shows these different ideals clearly.
Nevertheless, let us follow their ‘‘aesthetic analysis of the gluteal region,’’ The
anteroposterior projection is its most attractive feature! To make such a projection,
one needs anatomical, palpable, or visual landmarks.
In Fig. 11.4, part 1, the landmarks are the greater trochanter of the femur (A),
the point of maximal projection of the mons veneris (B), the point of maximal
gluteal projection (C), and the anterior superior iliac spine (D). For the ‘‘beautiful
buttock,’’ a ratio AC: AB = 2:1 is now considered correct. More characteristics of
beautiful buttocks are shown in part 2 of the figure: a lateral depression (1), an

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11.7 Beautiful Buttocks and Vision 293

Fig. 11.5 Determination of the site of implant (8) and the type 4 divergent buttocks before and
after the operation from behind (upper), from lateral (lower left) and with the lateral projection of
ideal proportion measures (lower right picture). Reproduced with permission from Cuenca-
Guerra and Quezada [24]

infragluteal fold also called the gluteal sulcus (2), supragluteal fossettes (3: one on
either side is added by the authors), and a V-shaped crease (4). Additional con-
tribution to beautiful buttocks was lumbar hyperlordosis, characterized by the
authors as: ‘‘This hyperextension of the spine in the lumbosacral region is an
ethnic feature (i.e., in black or mulatto persons), and sometimes is the result of a
forced posture since childhood. In these cases, the sacrum is horizontalized….,
which in a side view gives the impression of a greater buttocks projection than the
actual one, normally produced by the muscles in this region’’ [24].
Five types of deviant buttocks with their cause(s) have been identified for
surgical purposes that we will not treat here. Our pelvic interest lies in the way in
which the posterior pelvic surgical approach is performed.
Figure 11.5 upper part shows the surgical lines needed for the operation: A the
midline, found at the back of the standing patient, while sitting the line B, where
the buttock’s edge no longer rests on the table, can be obtained. Line C is the
safety line, one inch above line B, in order not to harm vessels and nerves in that
area. D is the line from the anterior superior iliac spine to the coccyx.

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294 11 Vision and Waist-to-Hip Ratio

Fig. 11.6 The pelvic types Pelvic type


as discerned by anthropology
have in general a direct
relation with the form of the Gynecoid Platypelloid Anthropoid Android
buttock present. Reproduced
and changed with permission
after Murillo [24]
Round Triangular Square Trapezoida

Buttock type

By organizing a line perpendicular to the midline at the height of the point of


maximal projection of the mons veneris (E), crossing with D is found. In F, the
crossing point between D and E, the place and the outline of the transplant is
indicated [24]. To much fat is removed by liposuction in case of excess. Together
this should result in a more beautiful buttock.
The results for the type 4 patient are given in their photograph, here the right
part of Fig. 11.5. ‘‘For instance, as soon as we identify a type 4 woman, thin, with
an android pelvis and little anteroposterior and side-to-side projection, we are
aware that we will need wide-based, almond-shaped, Vergara-type implants to
achieve a good projection’’ [24].
Now look at the three squares that indicate the 2:1 relation both in Figs. 11.4
and 11.5. One should note now that this relation is changed toward 2, 3:1 in the
result of the type 4 patient. Therefore, the authors’ own work shows that the 2:1
relation is not a fixed expression of harmonious and beautiful buttocks.
There is another aspect of buttock research that should be mentioned here.
Wheelchair users do have an very high chance of getting decubitus ulcers on the
buttocks, sometimes sitting over 16 h in their wheelchair. This is the more dan-
gerous in patients of whom the buttock skin is insensitive as in paraplegia and
quadriplegia patients. These ulcers start internally and move toward the skin. The
first external sign is redness of the buttock skin, but by then the damage has
already been done. Wheelchair cushions can help provided that they produce
adequate pressure relief. It appears that there is no linear relation between pressure
and the generation of ulcers. Therefore, a rather elaborate research program is
needed for the fight against skin ulcers [24].
There exists a direct relation between the types of buttocks as determined by
plastic surgeons and the construction of the pelvis, as described in the previous
chapters. The general relation is given in Fig. 11.6. The anthropoid pelvises are
mainly present in black women, and the related buttock form is square. The
android pelvic type is the male one and is mainly present in white females too. The
buttock type belonging to it is the trapezoidal one. Racial differences not only exist
in the pelvis but also in the buttocks.
This buttock study also brings up the effect of high-heeled shoes on the lordotic
curve of the lumbar spine. The general idea is that the pelvis will be tilted, buttocks

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11.7 Beautiful Buttocks and Vision 295

more expressed, and breasts will come up, which in total will accentuate the
female sexy appearance. Here, we concentrate again on the pelvic effects.
‘‘There are many Internet sites that support the belief that high-heeled shoes
cause increased lordosis. However, published research for this topic mostly does
not support this belief; some mixed results, small subject groups and questionable
methods have left the issue unclear’’ [25]. In other words, people do chat a lot on
this subject, and even health care providers give advice, but research does not or
cannot support the pelvic tilting concept. Studies performed already in 1928 and
1932 also did not support the tilting of the pelvis by high heels. But what does one
see that gives the impression of pelvic tilt? Researchers found ‘‘that the percep-
tions of physical therapists were influenced by soft tissue contours; increased
‘gluteal prominence’ may be inaccurately perceived as an increased lordosis’’ [25].
One does compensate with the gluteal muscles, the muscle belly will enlarge and
the buttock/gluteal area will be more pronounced.
It is not the least-respected clinicians who state: ‘‘Essentially, wearing high
heels for any length of time increases the normal forward curve of the back and
causes the pelvis tip forward,’’ as Dr Richard Brassard former president of the
American Chiropractic Association said [25]. On the Web, you will find several
more.
The other side of the coin is that research in this field has been severely
criticized, making the research results less secure: e.g., the researchers of the
School of Physical Therapy that restricted the population sample to women with
shoe size 35 (US size 5), resulting in a women section characterized by 53 kg
(116 lb) and 161 cm height (5’ 3’’) [25]. This clearly is a good intersection of the
Western population for high-heel studies! One should remember the remark on the
paramedics in Chaps. 1 and 2. Nevertheless, there is some ground in their
approach, since smaller women do get a different result than taller or heavier
women.
High heels are also thought to be connected to low back pain. However, some
studies question whether the supposed increased lordosis is related to low back
pain, and no studies are available on walking on high heels and its pain conse-
quences for the spine and joints involved.

11.8 The Gluteus Muscle Group

The gluteus maximus and its gluteal colleagues are important muscles at the dorsal
surface of the pelvis as already noted in the previous text. Its contraction also
influences our vision: we think to notice an increase in lumbar lordosis and it
appears to be a contraction of the gluteus muscle(s). It is time to study this muscle
group for one more moment. In Fig. 11.7a, the right side shows the gluteus
maximus and the left side the gluteus medius, while beneath it there is localized
the gluteus minimus muscle (see also Fig. 11.7b).

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296 11 Vision and Waist-to-Hip Ratio

Fig. 11.7 a Shows the localization of gluteus maximus (right leg of a) and medius (left leg of a).
In b the position of the gluteus minimus muscle is indicated. In c the typical female sway with
buttock bulging is shown (reproduced with permission Dept. Anatomy and Embryology, Leiden
University)

This complex of dorsal pelvic muscles performs a series of functions. The


gluteus maximus is the largest muscle of the human body and is a powerful
extensor. Its greatest power is generated during rising from a seat or climbing the
stairs. Next to extension, it is also an abductor (bringing in straddle one leg to the
other) and a lateral rotator (turning the foot outward). It inserts into tuberosity of
the femur, producing a bony crest on the femur by its exercised force. Its largest
part of the insertion is into a rather long and strong ligament (tractus iliotibialis)
that is at the lateral side of the leg and ends in the tibia (Fig. 11.7a). Contraction of
the gluteus maximus also helps to balance the trunk on the leg (hence activated in
high-heeled shoes). Both medius and minimus (Fig. 11.7a, b) are coming from the
ilium toward the greater trochanter of the femur. When standing on one leg,
gluteus medius and minimus muscles of the standing leg side prevent the pelvis
sagging to the other side [26]. During walking they contract alternately, induced by
the standing of the leg, showing in women that typical up and down shifting of the
buttocks (Fig. 11.7c).
The gluteus maximus, being a muscle, can withstand very little pressure. It
covers the ischial tuberosity in the standing position, but the moment one bends the
hip, it slips upward from the tuberosity. Try it yourself: go from the standing
position toward sitting position while covering your buttocks with your hands. You
feel the shift of the gluteus maximus. Thus, one sits on both the ischial tuberosities
and the gluteus maximus is neatly stretched along them. The ‘‘vascular muscle

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11.8 The Gluteus Muscle Group 297

tissue would not stand up to being sat on whereas fibro-fatty tissue, with its low
requirement of blood, accepts this insult with equanimity’’ [26].

11.9 Gait, the Pelvis and Vision

There is another aspect of the pelvic dorsal muscles that should be noted. We just
indicated the typical up and downward movement of the buttocks in females.
‘‘Females displayed greater peak hip internal rotation and adduction, as well as
gluteus maximus activity for all conditions’’ [27] (italics ours). These conditions
were walking and running, and males and females were compared. Moreover,
‘‘significant interactions (speed-gender and incline-gender) were present for the
gluteus medius ….’’ [27]. Thus, in walking and running, females use the gluteus
muscle complex more intensively than men. All these studies are done for another
purpose: females have a higher injury risk during running (injury rates in females:
62–76 % and in males: 24–32 %) [27] but also during aging. Thus, pelvic rotation
is greater, and gluteus muscle complex contraction is greater; hence, the buttock
movement of the walking female leads to a higher risk of injuries. A thesis by
Johansen [25] in 1991 showed that the main differences in the pelvic region during
walking are as follows: difference in the iliac crest, in fact the bi-iliocristal width,
the quadriceps angels were gender different, due to the greater distance between
the cristae, and the hip angle was different between the sexes during walking and
running. The difference in walking and running between men and women was
described earlier in the literature, and the consequences were that together with
arguments like females are weaker, have fragile bones and poorer physiological
performance, females were barred from long distance races. Not before 1980 were
women allowed to compete over 1,500 m. At the Olympic Games in 1984 in Los
Angles, women were allowed to run the 3,000 m and the marathon.
The consequence of the difference in walking patterns, as shown here for
heterosexual walking, is that the ‘‘don’t ask, don’t tell’’ approach of the American
army is baloney. Typical gender body movements can be discerned accurately by
any bystander in heterosexual and homosexual movements, and any bystander can
discern female and male movements [28]. So, female or male homosexuality is
hard to conceal as people move, and that is what soldiers do. And one sees more,
because ‘‘for women not using hormonal birth control, it would appear that some
information regarding female fertility appears to be encoded in gait’’ [29]. To
stretch the conclusion almost beyond its limits: the gluteal complex in action
signals, seemingly unnoticed, the male and female sexual nature and the fertility
situation of the female. Moreover, this is registered by our vision, partially con-
sciously and partly unconsciously.
One should dwell somewhat longer on gait. The importance of pelvic function
in gait cannot be denied, the gluteal muscles play an important role in motion,
which we treat here further in relation to vision.

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298 11 Vision and Waist-to-Hip Ratio

The striding gait is unique to man and it contains gender characteristics as we saw
above. This striding gait ability dates back nearly a million years and has had its
effects on the anatomy of the human body, especially the pelvis, as already explained
in previous chapters. ‘‘The antiquity of this human trait is particularly noteworthy
because walking with a striding gait is probably the most significant of the many
evolved capacities that separate men from more primitive hominids’’ [30].
Man’s bipedal mode of walking seems potentially catastrophic because only the rhythmic
forward movement of first one leg and then the other keeps him from falling flat on his
face. Consider the sequence of events whenever a man sets out in pursuit of his center of
gravity. A stride begins when the muscles of the calf relax and the walker’s body sways
forward (gravity supplying the energy needed to overcome the body’s inertia). The sway
places the center of body weight in front of the supporting pedestal normally formed by
two feet. As a result, one or the other of the walker’s leg must swing forward so that when
his foot makes contact with the ground, the area of the supporting pedestal has been
widened and the center of body weight once again rests safely within it. The pelvis plays
an important role in this action: Its degree of rotation determines the distance the swinging
leg can move forward, and its muscles help to keep the body balanced, while the leg is
swinging. At this point, the ‘‘stance’’ leg—the leg still to the rear of the body’s center of
gravity—provides the propulsive force that drives the body forward. The walker applies
this force by using muscular energy, pushing against the ground first with the ball of his
foot and then with his big toe. The action constitutes the ‘‘push off,’’ which terminates the
stance phase of the walking cycle. Once the stance foot leaves the ground, the walker’s leg
enters the starting, or swing phase of the cycle. As the leg swings forward, it is able to
clear the ground, because it is bent at the hip, knee, and ankle. This high-stepping action
substantially reduces the leg’s moment of inertia. Before making contact with the ground
and ending the swing phase, the leg straightens at the knee but remains bent at the ankle.
As a result, it is the heel that strikes the ground first. The ‘‘heel strike’’ concludes the swing
phase; as the body continues to move forward, the leg once again enters the stance phase,
during which the point of contact between foot and ground moves progressively nearer to
the toes. At the extreme end of the stance phase, as before, all the walker’s propulsive
thrust is delivered by the robust terminal bone of his big toe (J. Napier) [30].

Napier’s study of the evolution of gait and his description of bipedal walking in
man is still one of the clearest I know. The function of the gluteal muscles returns
unnamed in this description together with the rotation of the pelvis to determine
the maximum distance the step forward can be or how restricted the step forward
must be in a particular situation, think about a stony road. We already learned that
the pelvis is important in the distribution of forces from and to the leg. Moreover,
the acetabulum femur head cartilage is in elderly people the weakest point of hip
function. So, the interaction between the pelvis and the femur is rather important in
gait, as are the muscles responsible for flexion and extension of the hip. This all
centers on the relation between pelvis and femur, but it also informs us by our
vision.
Elvis Presley could be recognized from other musicians exclusively by his
pelvic movements, hence ‘‘Elvis the pelvis,’’ Even if only point lights are placed
on the joints of a person in the dark, one will recognize after a short learning
period the typical movements belonging to that person. The different styles of
movement are recognized by humans, which hold true for gender (see above),

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11.9 Gait, the Pelvis, and Vision 299

running versus walking, identity (e.g., Elvis), emotion, but also the style of serving
in tennis [31]. The contribution of each of the parts of the body to the recognition
has been studied. The pelvis is responsible for a good 22 %, but extremities have a
higher score near 30 %. Success in overall recognition is around 80 %, whether
phantoms, masking, or point light systems for the detection study are used. The
fine detection possibilities of the human vision of biological motion are expressed
in the recognition of the personal motion [32]. It also shows that human motion is
organized personally; otherwise, we could not recognize the tennis player by his
serve or Elvis Presley by his hip movements. Our visual registration detects the
fine anatomical variations (e.g., gender differences) and how these variations are
brought into the motion as carried out by the body. Such a variation is the dif-
ference in lumbar lordosis during normal gait between man and woman [33]. The
pelvis is related to the lordosis and moves during walking: in the mediolateral, the
anterior–posterior and in the vertical direction. My students in anatomy had
problems in accepting the relative small vertical deflection in relation to pelvic
movements. By a light-point fixed on the tightened belt of the teacher, the vertical
movement, an undulating movement of the light, can be followed in class during
walking (due to the swing, a forward–backward straddle is reached, it brings the
teachers belt lower, and in the next part of the stride brings it up again). The
2–4 cm difference (depending on ones length) in height between stand and straddle
causes the undulation of the light. We do recognize such typical personal behavior
of the pelvis even at large distances. So we easily recognize the person from more
than a hundred meters away by pelvic vertical movements of less than 4 cm, like
small mediolateral and anterior–posterior contributions.
The muscles of the leg, pelvis, and rump all contribute to walking and have to
be coordinated by the nervous system. For the leg muscles, three nerves relay
information toward the muscles: the femoral nerve for the extensors, the obturator
nerve for the adductors, and the sciatic nerve for the flexors in the upper leg. We
treat here only the biggest nerve in the human body: the sciatic nerve. It innervates
the backside of the upper leg and by its branches the whole lower leg. It looks like
a veritable cable, and it is covered by the gluteus maximus. However, since it
emerges just below the lower end of the gluteus maximus muscle, one can find its
entrance into the upper leg below the gluteus maximus in the infragluteal fold (see
Fig. 11.8). Here, this mighty nerve nears the surface and passes in between the
hamstrings, which it innervates [26]. Sciatic nerve accidents are to be expected:
the drunken student who sits down on a chair on which an empty glass stands,
falling backwards through a glass window, and accidents with electrical saws or
cutting machines. In order to reach both cut ends and restore the nerve (if possi-
ble), the entire gluteus maximus has to be freed from its attachment to the crista of
the ilium, a so-called question mark incision. The gluteal muscles themselves are
not innervated by the sciatic nerve. The superior gluteal nerve innervates the
gluteus medius and minimus, while the inferior gluteal nerve innervates the glu-
teus maximus [26]. The position of the sciatic nerve is also important in relation to
intramuscular injections given into the buttocks. Injections should avoid the sciatic
nerve. Therefore, intramuscular injections are always placed in the upper and outer

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300 11 Vision and Waist-to-Hip Ratio

Fig. 11.8 Palpation of the


infragluteal fold also called
the gluteal sulcus. Dotted
lines show the localization of
the sciatic nerve (reproduced
with permission Dept
Anatomy and Embryology,
Leiden and courtesy J. M. F.
Landsmeer )

quadrant of the buttock (Fig. 11.8) or in the lateral side of the thigh [26]. There is
an extensive literature on wrongly placed injections, especially in children with
serious consequences, which we will not treat here.

11.10 Spanking

The last part of this chapter is on spanking. Spanking is slapping the (nude)
buttocks with hands or instruments. Two types are known sexual spanking and
spanking of children as punishment. Sexual spanking has intriguing history in
France between the wars in the literature and in woman’s novels and was featured
in films such as ‘‘The Killer Inside Me.’’ Sexual spanking is called flagellantism,
and it is a serious abuse in children. The French pre-Second World War spanking
books concentrated on the erotic corporal punishment of teenaged girls mainly by
their older female supervisors.
Children’s spanking has now been forbidden by law in several Western
countries. Moreover, spanking of children does not help reduce antisocial
behavior; indeed, the opposite effect is found in research studies. According to the
literature, slapping and spanking can induce a ‘‘lifetime prevalence of anxiety
disorder, alcohol abuse and externalization problems’’ [34].
Spanking related to sexual performances was already described by Johann
Henrich Meibom (1590–1655), called Meibomii in his Latin text: ‘‘Tractus de usu
flagrorum in re medica and veneria’’ (1639), which was translated in 1761 as

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11.10 Spanking 301

‘‘A treatise on the use of flogging in medicine and venery.’’ The main argument of
the text is that since blood vessels are activated spanking induces better semen
production. An analogous reasoning is found today: spanking the buttocks brings
pain that in its turn will produce the human internal types of morphine called
endorphins. Endorphin production gives a pleasant feeling, like the production of it
in marathon runners. However, no literature can be found that supports this idea.
It is the structure of the buttocks that interests us here. Above, the buttocks were
described for the gluteal muscles and less attention was given to its fat compart-
ment. Here, we go deeper into the subcutaneous fat composition that constitutes
the so-called nates in the lower part of the buttocks. The nates come close to each
other just around the anus, and they compose most of the sitting surface of the
buttocks. Its fat is layered by strong connective tissue that encapsulates the local
fat in what is described as small connective chambers. Bleeding in this region is
kept within these chambers and therefore induces severe pains, when sat upon, by
its pressure in the enclosed connective chamber space. The buttock’s skin is rather
well connected to the fascia of the gluteal muscles, although movement of the skin
is still possible due to the subcutaneous fat in between them in the nates. The
overhang of the nates is organized by the leg fascia called the fascia lata. This leg
fascia is tightly strung around the leg muscles and reaches up to the sulcus
glutaeus. Here, it becomes looser. As a consequence, it is not the lower edge of the
gluteus maximus that constitutes the sulcus but rather the fascia lata, expressed by
the fact that the sulcus queers obliquely this muscle. The leg fascia is consolidated
by the tractus iliotibialis, which is strongly interwoven with it [35]. Consider this
fascia, a compression stocking that at its upper end sometimes causes the skin
above it to bulge out. That is what the fat compartment of the buttocks do,
overhanging the edge of the leg compression stocking, called the fascia lata.
Buttock pain is registered by the cutaneous nerves. The buttock skin is inner-
vated from above (superior gluteal skin nerves), its nerve branches arriving over
the crista iliaca, from the middle (medial gluteal skin nerves), branches coming out
of the sacrum and from below (inferior gluteal skin nerves) that are branches of the
posterior cutaneous nerve of the thigh [35]. Both the superior and inferior skin
nerves are important: the superior together with their blood vessels are important
in skin flaps used to restore decubitus in paralyzed persons and in posterior iliac
crest harvest for spinal arthrodesis procedures [36], while the topography of
inferior ones have to be known in leg amputations to avoid insensitive skin areas.
The extensive cutaneous innervation of the buttocks has been explained by some
authors by its evolutionary meaning. Both breasts and buttocks developed for
storage of nutrition, since in the primitive human communities, they argue, males
were out hunting and females had to go without food for rather long times [36].
Buttocks are even compared to the camel’s hump [36]. The registration and sig-
naling of the amount of nutrition available therefore are important, and since
buttocks are not visible, this registration has to be done by the cutaneous nerves.
The amount of skin stress should indicate the amount of storage available.
Perhaps for some people spanking is an erotic experience, but it damages the
gluteus maximus, because the muscle can barely withstand severe pressure and

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302 11 Vision and Waist-to-Hip Ratio

spanking will accumulate blood into the connective chambers of the subcutaneous
fat of the nates. As a consequence, the obstruction of the arterial and venous
transport will end into decubitus. Besides the ethical question of corporal pun-
ishment, spanking is also to be condemned from a psychomedical point of view,
especially in children where the buttocks are not yet fully developed.

Literature

Literature has been grouped in reference lists of several chapters in those cases where
arguments are difficult to entangle or published over several articles or books. In cases of
citation the article or book involved is indicated by the reference number together with a
capital Arabic letter.
1. Buytendijk FJJ (1962) De vrouw. Aula boeken, Antwerpen 11th edition
2. Dawood NJ (1983) The Koran, translation. Penguin Classics, Middlesex, England
3. Ssenyonjo M (2007) The Islamic veil and freedom of religion, the rights to education and
work: a survey of recent international and national cases. Cin J Intern Law 12:653–710.
Burqa is in Western societies a generalizing term for face covering garments. Analogous
wears can have different names: e.g in Afghanistan the chadari. The burqa was in origin an
item of clothing from the Indian Mogoul empire: first date 1580
4. Pearce EJ, Walsh G, Dutton GN (2008) Does the niqab (veil) wearer satisfy the minimal
visual field for driving? Ophth Physiol Optics 28:310–312
5. Rupp HA, Wallen K (2008) Sex differences in response to visual stimuli: a review. Arch
Sex Behav 37:206–218
6. Dimberg U, Lundquist L-O (1990) Gender differences in facial reactions to facial
expression. Biol Psychol 30:151–159; Vrana SR, Gross D (2004) reactions to facial
expression: effects of social context and speech anxiety on responses to neutral, anger and
joy expressions. Biol Psychol 126:123–178
7. Krupp DB (2008) Through evolution’s eyes: extracting mate preferences by linking visual
attention to adaptive design. Arch Sex Behav 37:57–63
8. Bailey JM (2009) What is sexual orientation and do women have one? In: Hope DA (ed)
Contemporary perspectives on lesbian, gay and bisexual identities. Springer
Science ? Business Media LLC, see also Bancroft J (2009) Human sexuality and its
problems. Churchill Livingstone, Edinburgh, pp 159–160
9. Dixson BJ, Grimshaw GM, Linklater WL, Dixson AF (2011) Eye-tracking of men’s
preference for waist-to-hip ratio and breast size of women. Arch Sex Behav 40:43–50
10. Rupp H, Librach GR, Feipel NC, Ketterson ED, Sengelaub DR, Heiman JR (2009) Partner
status influences women’s interest in the opposite sex. Hum Nat 20:93–104
11. Bancroft J (2009) Human sexuality and its problems. Churchill Livingstone/Elsevier,
Edinburgh
12. Rhodes G (2006) The evolutionary psychology of facial beauty. Annu Rev Psychol
57:199–226
13. Morris D (1967) The naked ape. A zoologist’s study of the human animal. Dutch version:
A. W. Bruna, Utrecht/Antwerpen
14. Hess EH (1965) Attitude and pupil size. Scientific American 212:412–454
14A. Hess EH (1975) The role of pupil size in communication. Sci American 233:110–119
15. Tombs S, Silverlman I (2004) Pupillometry. a sexual selection approach. Evol Hum Behav
25:221–228
16. Argyle M, Dean J (1965) Eye-contact, distance and affiliation. Sociometry 28:289–304

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17. Caryl PG, Bean JE, Smallwood EB, Barron JC, Tully L, Allerhand M (2009) Women’s
preference for male pupil-size: effects of conception risk, sociosexuality and relationship
status. Person Indiv Diff 412:503–508
18. Kaminski MV, Lopez de Vaughan RM (2006) The anatomy and physiology. Metabolism/
nutrition of subcutaneous fat. In: Shiffman MA, Di Giuseppe A (eds) Ch 5 Liposuction:
principles and practice. Springer, Berlin, Heidelberg; Kanehisa H, Miyatani M, Azuma K,
Kuno S, Fukunaga T (2004) Influences of age and sex on abdominal and subcutaneous fat
thickness. Eur J Appl Physiol 91:534-537
19. Joseph R (2000) The evolution of sex differences in language, sexuality and visual-spatial
skills. Arch Sex Behav 29:35–66
20. Singh D (1993) Adaptive significance of female physical attractiveness: role of waist-to-
hip ratio. J Person Soc Psychol 125:293–307; Roemmich JN, Clark PA, Berr SS, Mai V,
Mantzoros CS, Flier JS, Weltman A, Rogol AD (1998) Gender differences in leptin levels
during puberty are related to the subcutaneous fat depot and sex steroids. Am J Physiol
Endocrinol Metab 275:543–551
21. Martinez-Carpio PA, Fiol C, Hutardo I, Arias C, Ruiz E, Orozco P, Corominas A (2003)
Relation between leptin and body fat distribution in menopausal status. J Physiol Biochem
59:301–308
22. Marchal F (1994) Mise en evidence de changements précoces dans l’ontogenèse du basin
humain par une etude morphométrique. Bull Mem Soc Anthropol Paris T. 12, F. 1-2,
101–110
23. Sharma K (2002) Genetic basis of human female pelvic morphology: a twin study. Amer J
Phys Anthropol 117:327–333
24. Cuenca-Guerra R, Quezada J (2004) What makes buttocks beautiful? A review and
classification of the determinants of gluteal beauty and the surgical techniques to achieve
them. Aesth Plast Surg 28:340–347; Centeno RF (2010) Gluteal contouring surgery:
aesthetics and anatomy (pp 9–25), together with Murillo WL (2010) Buttocks remodeling
with fat transfer (pp 599–615) In: Shiffman MA, Di Giuseppe A (eds) A body contouring
and wheel chair studies. Springer Berlin; Todd BA, Thacker JG (1994) Three dimensional
computer model of the human buttocks, in vivo. J Rehabil Res 31:111–119; Van Geffen P,
Reenalda J, Veltink PH, Koopman BFJM (2007) Effects of sagittal adjustments on seat
reaction load. J Biomechan 41:2237–2245; Van Geffen P (2009) Dynamic sitting. Thesis,
University Twente, The Netherlands
25. Russell BS (2010) The effect of high-heeled shoes on lumbar lordosis: a narrative review
and discussion of the disconnect between Internet content and peer-reviewed literature.
J Chiropr Med 9:166–173; see also Johansen MK (1996) Gender differences in walking
with respect to movement of the pelvis. Thesis, University of British Colombia
26. Moffat DB (1987) Lecture notes on anatomy. Blackwell Science Publishing, Oxford,
London
27. Chumanov ES, Wall-Scheffler C, Heiderscheit BC (2008) Gender differences in walking
and running on level and inclined surfaces. Clin Biomechan 23:660–668
28. Johnson KL, Gill S, Reichman V, Tassinary LG (2007) Swagger, sway and sexuality:
judging sexual orientation from body motion and morphology. J Person Soc Psychol
93:321–334
29. Provost MP, Quinsey VL, Troje NF (2008) Differences in gait across menstrual cycle and
their attractiveness to men. Arch Sex Behav 37:598–604
30. Napier J (19127) The antiquity of human walking. Sci American 216(4):512–1212
31. Hill H, Pollick FE (2000) Exaggerating temporal differences enhances recognition of
individuals from point light displays. Psychol Sci 11:223–228; Loula F, Prasad S, Harber
K, Shiffrar M (2005) Recognizing people from their movement. J Exp Psychol Hum
Percep Perform 31:210–220; Roether CL, Omlor L, Giese MA (2010) Features in the
recognition of emotions from dynamic bodily expression. In: Ilg UJ, Masson GS (eds)
Dynamics of Visual Motion Processing Part 3. Springer, Heidelberg, pp 313–340

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32. Troje NF (2005) Person identification from biological motion: Effects of structural and
kinematic cues. Percep Psychophys 67:667–675; Mather G, Murdoch L (1994) Gender
discrimination in biological motion displays based on dynamic cues. Proc R Soc Lond
B253:273–279; Smith LK, Lelas JL, Kerrigan DC (2004) Gender differences in pelvic
motion and center of Mass displacement during walking: Stereotypes quantified. J Wom
Health Gender Based Med 11:453–462
33. Sizer PS, James CR (2008) Considerations of sex differences in musculoskeletal anatomy
Chap. 3. In: Robert-McComb JJ et al (eds) The active female. Humana Press, Totowa NJ;
Chung CY, Park MS, Lee SH, Kong SJ, Lee KM (2010) Kinematic aspects of trunk motion
and gender effect in normal adults. J NeuroEngineer Rehabil 7:1–9
34. Strauss MA, Sugarman DB, Giles-Sims J (1997) Spanking by parents and subsequent
antisocial behavior of children. Arch Pediatr Adolesc Med 151:761–767; MacMillan HL,
Boyle MH, Wong MYY, Duku EK, Fleming JE, Walsh CA (1999) Slapping and spanking
in childhood and its association with lifetime prevalence of psychiatric disorders in a
general population sample. CMAJ 161:805–809
35. Hafferl A (19129) Lehrbuch der topographischen Anatomie. Springer Berlin, NY
36. Arieli R (2004) Breasts, buttocks and the camel hump. Isr J Zoology 50: 87–91; Tubbs RS,
Levin MR, Loukas M, Potts EA, Cohen-Gadol A (2010) Anatomy and landmarks for the
superior and middle cluneal nerves: application to posterior iliac crest harvest and
entrapment syndromes. J Neurosurg 13: 356–359; Hwang K., Nam YS., Kim DJ., Han SH.,
Hwang SH. (2008) Posterior cutaneous nerve of the thigh relating to the restoration of the
gluteal fold. Ann Plast Surg 120:357–361

sergiocamargo47@gmail.com
Chapter 12
Male and Female Bladder

The bladder is built from two parts: the detrusor muscle making the dome and the
trigone constituting the base. The bladder is not passive but active during storage
as it is active during voiding. Uncontrolled detrusor activity occurs in both men
and women.

12.1 Introduction

A century ago children played with the dried, air filled, bladder of pig or cow, as
they now do with a balloon. The ‘‘rumble-pot’’ used on Epiphany eve was a jar
over which a pig’s bladder was stretched. A wet reed was pulled up and down
through a small hole in the middle. Children in the Netherlands sang in time to the
rhythm produced by the pot: ‘‘Rommelpot, rommelpot, wie geeft er koek en wie
een ei?’’ ‘‘Rumble-pottery, rumble-pottery who gives cake and who an egg?’’
Until a century ago the use of a bladder as a waterbag, wine bag or balloon was
well known. Dried bladders were in vogue in all kinds of trades. Modern times,
and our manufactured materials have made bladders obsolete.
Drying or fixation does not alter the impermeability of the bladder wall to air or
liquid. This property is inherent to the digestive and urogenital tract.
There are obvious differences between the male and female urinary tracts. Most
obvious is the length of the urethra; the male urethra is longer (Fig. 12.1a and b). The
female urethra is thought homologous to the cranial part of the male prostatic urethra
only (Fig. 12.1c). There is also a difference between the muscular layers of the male
and female bladder. The muscle layers involved in the urinary tract have been
studied in developing [1] and mature [2] male and female specimens. Though
the number of studies concerned with development of the muscles involved in the
urinary tract are few, the literature reports diverse conclusions, mainly because the
various muscle layers are difficult to discern in mature human specimens (see [1, 2]).
Homology of male and female bladder structures has been determined and most of
the descriptions in this chapter are taken from those studies [1].

E. Marani and W. F.R.M. Koch, The Pelvis, 305


DOI: 10.1007/978-3-642-40006-3_12,  Springer-Verlag Berlin Heidelberg 2014

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306 12 Male and Female Bladder

(a)

(b)

(c)

bulbar urethra

penile urethra

Fig. 12.1 a Midsaggital section of the female pelvis (courtesy prof. Dr. J. M. F. Landsmeer ).
b Midsaggital section of the male pelvis (courtesy prof. Dr. J. M. F. Landsmeer ). c Male bladder
and urethra (courtesy prof. Dr. K. Usunoff )

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12.2 The Dome of the Bladder; the Detrusor Muscle 307

12.2 The Dome of the Bladder; the Detrusor Muscle

The detrusor muscle in males, which constitutes the upper three quarters of the
urinary bladder consists of bundles of smooth muscle embedded in connective
tissue. Several authors propose a differentiation into an outer longitudinal, a
middle circular and an inner longitudinal layer [1, 2], though these are only present
on the ventral side of the bladder, where we can discern them. The inner longi-
tudinal layer consists of small bundles, which make up a rough network. However,
at the top of the dome these three layers are so intimately interwoven that they
cannot be discerned any longer. Dorsally, only two layers are present; an outer
longitudinal and an inner circular layer. On the lateral surfaces of the bladder these
layers are again interwoven so that they cannot be separated anymore in man.
In women we find the same construction. Only the composition and localization
of the lower edge of the bladder is different from man’s detrusor muscle, because
in males the prostate changes that position. The smooth muscles just above the
bladder neck in women contain more circular bundles.
The dorsal lower part of the detrusor muscle contains the entrances of the
ureters. The smooth muscles of the ureter constitute a network of fiber bundles.
The insertion of the muscle bundles of the detrusor into the network of ureteral
muscle bundles is called the sheath of Waldeyer. These bundles of Waldeyer
adhere to the adventitia of the ureter in men and women. The ureteral entrances are
continuous with the trigone, which constitutes the lower dorsal quarter of the
bladder. The structure and composition of the detrusor muscle is nearly the same
in males and females.

12.3 Demonstrating the Detrusor Forces

Since the detrusor in man and animals, contains mainly longitudinally and cir-
cularly directed smooth muscles separated into layers, the movement of a point on
the outside of the bladder cannot be predicted. However, one can study its dis-
placement in relation to other points. This has been done elegantly with the use of
fluorescent spheres glued to the outer fascia of the bladder. This fascia is inti-
mately connected to the connective tissue of the bladder muscles, and thus will
reflect the muscle contractions [3].
Changes in the distances between the fluorescent spheres can be registered with
a pair of cameras and calculated. A three-dimensional image is created, but since
the increase in thickness of the bladder muscles is minimal, in fact a two-
dimensional reconstruction is made of the fluorescent spheres of the isovolumetric
bladder.
Artificial stimulation of the nerves responsible for contraction of the isovolu-
metric detrusor in rabbits shows muscle contraction in a circular wave-like pattern.
Its center becomes more and more contracted. Finally the waves of contraction

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308 12 Male and Female Bladder

relax until the center loses its contraction activity. Paradoxically, circular wave-
like areas of relaxation are also noticed. Their centre continuously decreases the
contraction. After a certain time, the relaxation stops and the relaxation waves
retract until their centre is reached and the centre returns to a steady-state
condition.
In non-stimulated bladders, contraction can occur along one axis while per-
pendicular to this relaxation is present. Seemingly, in a rest situation the different
smooth muscle layers of the detrusor can react dimensionally differently. The
significance of this behavior is unclear. The anatomical divergence of the direction
of the muscle fibers in the various detrusor layers must have functional
consequences.
Previously such functional consequences could only be speculated about. Now,
however, the interplay of simultaneous contraction and relaxation has been proved
in a living bladder [3].
One other remark concerns the presence of contraction and relaxation simul-
taneously at the same site in the non-stimulated rabbit bladder. The muscle layers
are active, whether in contraction or relaxation. In the iso-volumetric situation,
contraction at one site must be accompanied by relaxation at another place. It is
concluded that the resting bladder contains its own activity caused by its muscles,
presumably to adapt to bladder filling or to changes in shape due to (viscera)
movements [3]. So the bladder musculature is constantly active.

12.4 The Bladder-Neck or Trigone

We are able to investigate the transitional zone from detrusor to bladder neck,
because trigone musculature develops later than the detrusor muscles. The blad-
der-neck muscle bundles are smaller, and in between them compact connective
tissue is found. The trigone contains two layers: an inner longitudinal and an outer
circular layer. The circular layer increases in thickness caudally. In females the
transitional zone contains longitudinal detrusor bundles, which intermingle with
the trigone layers.
While the older literature describes the continuation of the detrusor muscle as
co-organizing the smooth muscles of urethra, developmental studies contradict this
[1]. The different timing of the appearance of the detrusor and trigone muscles
makes it possible to check for this in sections. The detrusor only constitutes a small
part of the ventral wall of the urethra. The proximal part of the urethra is sur-
rounded by the trigonal smooth muscle. The smooth muscle of the urethra proper
will surround the ventral wall of the urethra prostatica, caudally of the trigonal
musculature, and the urethra membranacea is surrounded by a horseshoe shaped
muscular structure. This description holds for males and females.
Thus two borders can be discerned: between detrusor and trigonal musculature
and between trigonal and urethral smooth musculature. These borders are not
perpendicular to the bladder or urethra, but follow a curved or oblique path.

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12.4 The Bladder-Neck or Trigone 309

In males the dorsal part of the muscular wall of the urethra encompasses the
prostate. The prostate musculature can clearly be distinguished from the trigonal
musculature. Dorsally in men the trigonal musculature stops at the entrance of the
urethra, where a layer of prostate muscles commences.
In the mid seventies histochemistry was applied to the bladder and the urethra
[4]. In these studies certain assumptions were made, such as: presence of the
enzyme acetylcholinesterase corresponds to cholinergic innervation, and the gly-
oxylic fluorescence method detects only catecholamines, mainly noradrenalin.
Although these assumptions were partially incorrect, the innervation of the muscle
groups could nevertheless be studied.
The detrusor is not pictured in the Fig. 12.2a–d. The borders of the different
staining regions are drawn in both the male and female, trigone and urethra.
Figure 12.2a shows an extra smooth muscle layer in male on the dorsal surface;
the one encapsulating the prostate. Staining for acetylcholinesterase shows the
trigonal musculature, with its extension into the ventral urethra (Fig. 12.2b). The
caudal part that is left free, is occupied by the striated musculature of the urethral
sphincter (Fig. 12.2c). However, noradrenergic innervation (Fig. 12.2d) in women
is restricted to the ventral part of the trigonal musculature. In man both ventral and
dorsal trigone are noradrenergically innervated.
Since the noradrenergic innervation is considered responsible for support of the
occlusion during the filling phase, one could conclude that women are at a double
disadvantage. Males have an extra muscular layer at the base of the trigone due to
their prostate, and males have a more extensive occluding innervation of the
entrance of the urethra [4].

12.5 Detrusor Instability

Detrusor instability is defined as uncontrolled contractions of the detrusor. It can


be measured by a pressure catheter placed in the bladder. The method used is
important. Direct filling of the bladder (=cystometry; filling velocity 50 ml/min) or
drinking with the addition of a diuretic will yield different results. Diuresis
cytometry will demonstrate the uncontrolled detrusor contractions [5]. Simple fast
filling of the bladder will miss detrusor contractions, because it is an unnatural
process. Therefore, ambulant urodynamic registration of the natural bladder is the
procedure of choice [6].
The detrusor will always reflect pressure changes due to its active state (see
Sect. 12.3) as measured urodynamically. Only if this pressure change is above
15 cm water, will it be classified as an uncontrolled bladder contraction (Inter-
national Continence Society Committee on Standardisation of Terminology). This
value is arbitrary. Detrusor instability can lead to incontinence, but there are
women who have detrusor instability without incontinence [5, 7]. What induces
detrusor contraction? In general, movement of the body such as knee bending, stair
walking, coughing and, surprisingly, hand washing [6]. In incontinent females this

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310 12 Male and Female Bladder

Fig. 12.2 a Schematic midsagittal drawing of the male and female bladder base: trigone and
urethra. v = ventral, d = dorsal. b Localisation of acetyl cholinesterase activity is indicated.
c Localisation of striated muscles (somatic) and acetyl cholinesterase activity is shown. d The
localization of noradrenergic innervation is added to the results of Fig. 12.2c

Fig. 12.3 Uncontrolled detrusor activity, followed by a urethral relaxation (courtesy Dr. Mulder
[6])

will trigger uncontrolled detrusor activity, sometimes followed by an urethral


relaxation (Fig. 12.3).
Detrusor instability occurs in both men and women. In men, detrusor instability
is related to obstruction, mainly in young and aged males and to a far lesser extent
to prostate hyperplasia. Detrusor instability in male patients is expressed by
nocturesis according to some scientific groups, but debate continues. The main
point of the argument is that the phenomena which occur at night and cause
nocturesis also occur during the day.

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12.5 Detrusor Instability 311

In women, detrusor instability is expressed by incontinence. Remember that


males have an extra muscular layer and have a more extensive closure innervation.
The main attention thus goes to women, who form the largest urine incontinent
group and are therefore important to the diaper industry.
The first thing to look for in incontinent women, or those with a high voiding
frequency or urge, is detrusor instability measured by urodynamic techniques.

Literature

1. Droës JTPM (1972) De musculatuur van blaas en urethra in de menselijke foetus. Thesis
Leiden, the Netherlands
2. van Ulden BM (1975) De musculatuur van de blaashals en de urethra posterior bij de Man.
Thesis Leiden, the Netherlands
3. Kinder MV, Bos R, Willems PJB et al (1999) Three-dimensional registration of mechanical
bladder activity using polystyrene fluorescent spheres: a technical note. Arch Physiol Biochem
107:236–241
4. Klück P (1980) The autonomic innervation of the human urinary bladder, bladderneck and
urethra: a histochemical study. Anat Rec 198:439–447
5. van Venrooy GEPM, Boon TH, de Hond JAPM (1990) The diagnostic value of diuresis
cystometry. Int Urogynecol J 1:191–195
6. Mulder AFP, Vierhout ME (1996) Ambulant urodynamisch onderzoek. Profundum 1:22–27
7. van Waalwijk van Doorn ESC, Remmers A, Janknegt RA (1991) Extramural ambulatory
urodynamic monitoring during natural filling and normal daily activities: evaluation of 100
patients. J Urol 146:124–131

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Chapter 13
The Pelvis and Herbal Medicine

In traditional societies, a certain category of women seems to have a preferential rela-


tionship with care: the elderly. Not only are they more available, but also they have
acquired with age the necessary knowledge and experience. There are without doubt, some
reasons of a symbolic order to this that have not been adequately considered: illness is
often a privileged moment of relation with the past and therefore with age (F. Loux, Folk
medicine) [1].

The use of raw plant extracts to cure pelvic problems in males and females does
not work. Despite double-blind, randomized studies that clearly show the inef-
fectiveness of plant extracts like saw palmetto for prostatitis or black cohosh for
menopausal women, well-educated people still use these extracts. Herbal medicine
was spread over the world among others by slavery. It is remarkable that meta-
analyses that appeared after the double-blind, randomized studies keep reporting
significant effect of these plant extracts. Attention is given to placebo studies, in
which the effect of the psychodynamic component in the overall therapeutic effect
is stressed by phytotherapy. A different approach to study the consequences of
plant extracts is system biology.

13.1 Introduction

Bladder infections occur frequently in women. To overcome repeated infections


cranberry sap is prescribed even by the physician. It should prevent from new
infections after bacterial clearance of the bladder mostly done with antibiotics. It is
obvious that plant extracts are used even in modern times and everyone can
enumerate several everyday examples: from coffee in the morning till hot lemon
tea against cold in the evening. Herbal use and herbal medicine are clearly present
in our society. Aged females all have their own familial prescriptions and receipts.
Let us be clear at the start: herbal medicine belongs to alternative medicine, also
called unorthodox medicine. Nevertheless, it plays an enormous role in pelvic
diseases outside regular medicine as we will see later on.
Phytopharmacology, chemical knowledge of plants for medical practice, and
chemical taxonomy serve regular medicine still day by day to invent new

E. Marani and W. F.R.M. Koch, The Pelvis, 313


DOI: 10.1007/978-3-642-40006-3_13,  Springer-Verlag Berlin Heidelberg 2014

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314 13 The Pelvis and Herbal Medicine

medicaments. Expeditions are sent out to discover new plants that are used by the
natives for medical treatment. Plant extracts are regularly studied for their
chemical substances and for their use in medicine. Purification and their effective
concentrations are studied in animal experiments. A good basis is needed and
chemotaxonomy of plants provides such a framework. The simple idea that the
empirical detected ‘‘lemon juice that was formerly a pharmacon used in the British
navy to prevent scurvy [2]’’ is now replaced by highly sophisticated clinical
pharmacological research [2A].
Phytotherapy is the medical use of (raw) plant extracts that should be applied
both in prevention and as medicine. Raw plants or their extracts are used in most
cases as a tea, or the plants can be extracted and diluted in alcohol then called
tincture; no concentration of the active substance is known and other substances of
the plant are also extracted and diluted. To give some examples, garlic is against
affections like cold, influenza, cardiac problems, high blood pressure, high cho-
lesterol concentrations, ear ache, and worms (however, high amounts of garlic
damages sperm development and production), and fennel seeds if roasted works
against repeat of the stomach. Bay helps to digest fat and bay tea is effective
against scurf. Purple corn flower tea helps against cold. In most cases, the tea
works for several affections and mixing herbs increases the effect of the tea.
Why a turn to alternative medicine now our regular medicine is so advanced?
‘‘Alienation from the doctor–patient relationship is also apparent in a flight to
alternative therapies such as naturopathy, iridology, reflexology, and the like.
Lacking any scientific basis, these represent a return to the eighteenth century,
when all therapies, medical and non-medical alike, were based upon anecdotal
results rather than quantitative demonstrations in efficacy. For example, in the
United Kingdom, in 1981, alternative practitioners were 27 % as numerous as the
total number of general practitioners; the number of acupuncturists doubled
between 1978 and 1981; and the consultations of such non-orthodox practitioners
increased by 42 % from 1981 to 1985’’ [3]. In the state Michigan, 50 % of the
adults over 18 years use once a year alternative medicine, while the percentage for
herbal medicine is 20 % in 2001 [3A]. The marks for visits to practitioners of
alternative medicine range from 6 to 23 % and self medication from 25 till 49 % in
various countries in 2010 [3B]. Moreover, the figures are still rising.
Under the condition that the patient derives no or little benefit from regular
medicine (cancer is a good example), a turn toward alternative medicine occurs
and among them is herbal medicine [2B]. Others say: ‘‘… the majority of alter-
native medicine users appear to be doing so not so much as a result of being
dissatisfied with conventional medicine but largely because they find these health
care alternatives to be more congruent with their own values, beliefs, and philo-
sophical orientations toward health and life’’ [26A].
Placebo effects are large and hardly corrected for in alternative medicine.
However, several alternative medicine producers nowadays are forced by gov-
ernments to indicate concentration and active substance, bringing alternative
medicine back into phytopharmacology. The balance between herbal medicine and
phytopharmacology therefore is a complicated one.

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13.1 Introduction 315

In this chapter, the history of alternative herbal medicine is outlined. For the
pelvic herbal use in women and men, two plants were chosen: black cohosh and
saw palmetto, respectively. Moreover, the word magic is used that directly brings
about definition problems by historians and anthropologists. Magic is a socially
loaded word. Here, it is used in the sense: ‘‘The believe in not proven actions of
plant extracts within a philosophical framework different from regular medicine.’’
The word magic containing this meaning has been placed between quotation
marks.

13.2 History

Rembert Dodoens’ or using his Latin name Rembertus Dodonaeus’, herbal over-
view called Cruydt-boeck [4A] is an important mile-stone. It was published for the
first time in 1554. French and English translations appeared in 1557 and in 1578,
respectively. The Latin extended version was issued in 1583 and titled ‘‘Stirpium
historiae pemptades sex, sive libri XXX’’: On the history of herbs, organized within
six main groups and 30 books (chapters). In total, six editions were brought out,
the last one in 1664. Dodoens’ Cruydt-boeck is taken as the starting point for the
history of herbal medicine, since this herbal book comprises Greek, Roman, and
Middle Ages knowledge of medicinal plants. It partially is based on Galen’s and
Hippocrates’ hand down descriptions, but also on other Greek results. It is also
indirectly based on the accounts of Plinius. Roman medicine as recommended by
Cato and Celsus were also incorporated. The conquests of Alexander the Great
brought drugs from India and beyond. Emphasis on local herbs was provided by
the writer Marcellus Empiricus of Bordeaux in the fourth century [4]. A series of
herbal books printed in the fifteenth and sixteenth century were also used for the
plant descriptions. Medical application of plants through ages has been established
in this book and the plants from the New World are already partially incorporated
see Web [4A].
Studying the continuation from Galen into even the seventeenth century
demonstrates ‘‘that historians of ancient therapeutics have tended to accept the
Hippocratic/Galenic division between magic and medical therapy and have
assumed that that division was relatively stable; on the contrary, it was very
unstable and was not one that can easily be explained on grounds of social class, or
of medical literacy’’ [4]. Moreover, although Greek and Roman herbal medicine
was based on ratio, the magic portion of the medical old framework and the
instability of the system allowed the entrance of other non-rational-based methods.
Thus, Dodoens’ Cruydt-boeck contains herbal medicines that are based on magic
and on ratio, along the Galenic/Hippocratic system. One has to accept that system
as a medical adequate approach to heal patients; otherwise, it is of no value at all.
Next to each plant description with drawing, Dodoens herbal book gives the
medical application. We know now that his descriptions are based on magic

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316 13 The Pelvis and Herbal Medicine

applications too that hardly adds to healing of the patient. The consequence can be
concentrated in summary by: ‘‘The truly baroque abundance of pharmaceutical
preparations inherited from the seventeenth century presented a special problem.
They include aside from the entire range of galenic composite, many chemiatric
preparations, as well as sympathetic magic products of so-called Dreckapotheke,
containing excrements, animal products, drugs from the ‘New World,’ and a large
variety of folk medicine’’ [5].
One can also say it was a mess despite the herbal ‘‘taxonomy’’ carried out by
Dodoens and his predecessors. Herbal medicine contains even poisons that will kill
the patient, substances that have no healing capacity at all and mixtures of healing
and killing substances, leaving excrements out; in fact, seventeenth century herbal
medicine created charlatans among the physicians. Entering the eighteenth cen-
tury, the situation was not different at all. ‘‘The eighteenth century, which gave
itself the epithet ‘philosophical,’ had the difficult task of intellectually assimilating
the truly enormous baroque inheritance left by the seventeenth century, including
controversial theories, new knowledge, and new discoveries. Nevertheless,
although the traditional doctrine of humoral pathology was slightly broadened by
the grafting on of new ideas, the eighteenth century remained true to the basic
concepts at the root of the Hippocratic–Galenic system’’ [5]. Seemingly, the
eighteenth century medicine could not escape the framework of the Greek, Roman,
and Middle Ages’ medical system which has been compiled in the seventeenth
century herbal medical work of Dodoens. It will have large consequences as we
will see later on.
The physicians in the eighteenth century easily noticed that the herbal phar-
macology did not work. Only few opposed: Georg Ernst Stahl (1659–1734),
Friedrich Hoffmann (1660–1742) at the start and Anton von Störck (1731–1803) at
the end of the eighteenth century and not to forget Albrecht von Haller
(1708–1777, see Chap. 4) to name the most important ones, all Germans and later
on the German Samuel Hahnemann (1755–1843) founder of the homeopathy.
Earlier Daniel Ludwig (1625–1680) had tried to reduce the amount of therapeutics
attacking the polypharmacy as applied by the practitioners and physicians. Stahl,
Hoffmann, Störck, and Hahnemann all tried to get rid of the ‘‘unscientific’’
pharmacons, reducing the amount of recipes and their ingredients. Nevertheless,
all believed in a distinction between the body and a spirit or anima that is based on
the old framework of medicine. One will see that magic crept into medicine again.
Germany is in the eighteenth century the center of renewal of the basis of
(herbal) medicine in order to improve the healing of patients. New medicaments
were indeed found, simple recipes were applied, however into absurdum as has
been shown for homeopathy, and in general hardly based on ratio and experiments
(there are very important exceptions). Stahl and Hoffmann were trained both in
medicine and in chemistry, but both were close to the humoralistic tradition. Stahl
wanted a restoration of the Hippocratic medicine by his renewed framework for
medicine. Hoffmann took a mechanistic position, which, to put it briefly, postu-
lated ‘‘an ether-like fluid (the ‘spiritus animales’ of Descartes) to be present in the
nervous system,’’ which affected the nervous system and the muscles, regulating

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13.2 History 317

their tone. (…) Hoffmann, as well as Stahl, employed an arsenal of only a few
chosen medicines [5]. Seemingly, the reduction had success; however, the
replacement by new medicaments was less successful.
The reaction of regular medicine of the eighteenth century was predictable.
‘‘An unorthodox medical theory is one whose principles of causation and/or
practice directly challenge the beliefs, knowledge, and experience of the dominant
group of health practitioners in a society. The real or potential threat (of unor-
thodox medicine) usually results in a process of self-definition by regular physi-
cians, a corresponding combating of those practitioners who deviate from
established norms and a determined effort to retain or win back the patronage of
the laity’’ [6]. Indeed, the fight for the patronage of the laity was already started at
the beginning of the eighteenth century. At least in Germany, the promising results
of Stahl and Hoffmann were recognized by the ordinary people. The Aurum pot-
abile developed by Stahl’s pupil Christian Friedrich Richter (1676–1711) ‘‘was
considered a true wonder drug’’ [5]. The production of several medicines stayed
secret, still contributing to the mystery of their medicines. Hoffmann introduced
new medicines too. ‘‘Hoffmann’s drops (Spiritus anodynus) can still be bought at
every German chemist’s shop today’’ [5]. The drops were produced from two parts
ethanol and one part of ether; ‘‘they are reputed to stabilize circulation and to
tranquilize’’ [5].
The last half of the eighteenth century is dominated by the research of Störck.
He identified the plants he used with nowadays acceptable botanical means.
Extracts of single plants were tested on himself and on patients with incurable
chronic diseases. He produced liquids or pills from extracts of hemlock, autumn
crocus, hyoscyamus, thorn apple, monkshood, and pulsatilla [5]. He reported his
clinical results: curing tumors, ulcers, and eye ailments. He also used plant extracts
for rheumatism, gonorrhea, venereal ulcerations, female problems, lymphatic
tumors, and eye diseases [5]. The care with which Störck used his medicines was
not taken over by the physicians, who used them careless producing poisoning of
the patients. ‘‘The time was not yet ripe for the further development of this
therapeutic possibility’’ [5]. Thus, the modern method of phytopharmacology
indeed was introduced at the end of the eighteenth century by Störck, but the
colleagues destructed its further development by negligent behavior toward pre-
scribed dosages. You will be caught at it!
Störck brought up the idea that a poison (nightshade) inducing a disease
(madness) in healthy people could be an antidote for the same disease in sick
people. It is the identical idea that Samuel Hahnemann (1755–1843) used in
homeopathy.
Homeopathy was also developed in Germany. Hahnemann’s live started in
restricted poverty. Still he created the possibility to study medicine by translating
manuscripts on medical and chemical subjects. Add to it that he gave language
lessons and a basic student income was assured: so a self-made man. He acquired
outstanding knowledge of chemistry due to his translations, ‘‘which was to prove
very significant for his later life’s work’’ [7]. The physicians handwork made him
ashamed: ‘‘The thought of becoming a murderer, or of condemning my fellow man

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318 13 The Pelvis and Herbal Medicine

to a lifetime of ill-health, was so disturbing, indeed so abhorrent to me that in the


early years of marriage I gave up clinical practice altogether’’ wrote Hahnemann in
a letter [7]. Hahnemann did not stand alone: ‘‘All progressive doctors at the turn of
the nineteenth century were well aware that medicine had run itself into a dead-end
and that a radical change of direction was needed’’ [7]. What was needed was a
new framework for medicine and Hahnemann seemingly provided it. Basic to his
approach was Störck’s idea. In his own words: ‘‘We should imitate nature, which
sometimes cures a chronic affliction with another supervening disease, and pre-
scribe for the illness we wish to cure, especially if chronic, a drug with power to
provoke another, artificial disease, as similar as possible, and the former disease
will be cured: fight like with like’’ [7]. This ‘‘Principle of Similarity’’ was detected
by Hahnemann by using quinine that was effective against malaria symptoms. He
himself had no malaria, but after regular taking quinine, the same fever symptoms
occurred.
Still Hahnemann accepted a ‘‘life force’’ that could not been noticed visually.
Only if there was something wrong with the life force, it could be noted by the
physician via the patient’s symptoms. The symptoms should lead the physician to
the correct therapy. The consequence was that a thorough anamnesis was a pre-
requisite for healing the patient, because only in that way, a correct therapy could
be applied. We have seen that dosage is vital; it ruined Störck’s clinical correct
approach. Thus, high concentrations of chemicals could kill the patient, because
their resistance was already lowered by the disease. Dilution of the chemicals was
the solution. The reasoning in fact was some what different: ‘‘Hahnemann started
out at first with the normal dosages, but soon realized that a sick organism which is
already (over-)stimulated in a certain way, needs only a slight therapeutic stimulus
in the same direction from the ‘similar’ drug’’ [7]. His dilutions went ad absurdum:
his first dilution was one drop of drug to one hundred of alcohol that should be
shaken forcefully. Then, from this mixture, again a drop was taken and again to
one hundred of alcohol and so on, thirty times. One can calculated that no mol-
ecule of the extract is left in the final fluid. The followers started journals,
homeopathic societies were erected, books were produced also by Hahnemann,
and dissemination was ascertained. Moreover, since Hahnemann went with his
second wife, a French artist, to Paris, the propagation of the homeopathic ideas
reached the southern Europe countries. In fact, its spreading was over whole
Europe and America.
The extremely bitter, and indeed deliberately offensive, tone of the controversy was to a
large extent the fault of Hahnemann himself. From the outset, he had not simply criticized
allopathy on the basis of a new, ostensibly better theory, but had attacked it in the most
violent terms. The objects of this onslaught had defended themselves in similar vein and
thus began the state of open confrontation between homeopathy and allopathy which has
characterized their communication—or rather lack of it—to the present day [7].

Even recently, homeopathy produces heated discussions, stirred up in 1988 by


Nature [7D]. Jacques Benveniste (1935–2004) studied homeopathy by endless
dilutions. Together with his coworkers, he published an article called ‘‘Human

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13.2 History 319

basophil degranulation triggered by very dilute antiserum against IgE’’ [7D] that
was accepted by Nature on the condition that four other research groups endorsed
the results and a delegation of Nature could visit the laboratory to repeat the
experiments. Benveniste’s claim was that at high dilutions of the protein IgE
antiserum (thus not containing antiserum against IgE anymore) still degranulation
of these blood cells occurs. The delegation expressed their results after only one
week checking as: ‘‘High dilution’’ experiments a delusion [7D]. Benveniste was
dismissed as head of the INSERM 200 and the laboratory work ended. Benveniste
refused to withdraw his article and continued by gathering his own research money
till he died in 2004.
This Nature article started a series of research on what is called the ‘‘memory of
water.’’ At least high dilutions do behave rather strange. In fact water behaves
strange: its solid state floats on the liquid state, which is seldom encountered for
other substances. It produces by the uneven localization of its hydrogen parts a
field that induces field changes by adherences to other substances. Its largest
weight is at 4 C, while most substances have it at their melting point. Water after
infrared radiation will take more than a day to restructure. Water photolumines-
cence changes will take more than days to restructure. Thermodynamic energy
states of water molecules are continuously shifting. Water has odd properties that
are increasing in dilutions of salts that cause electric and electromagnetic effects.
These changes are encountered with long lifetimes. All these arguments, and there
are more, contribute to the likeliness of the presence of the ‘‘memory of water’’ see
[7F] for extension of the arguments. By the way: ‘‘simply proving that water does
have a memory does not prove that homeopathic medicines work’’ [7F].
Madeleine Ennis first found comparable results as Benveniste did, but
extending the research she could not substantiate the original results. She pub-
lished in 2010 an overview article ‘‘Basophil models of homeopathy: a sceptical
view’’ presenting her doubts and care [7D]. The high dilutions up to 10120 still
produce conflicting evidence as to its benefit for patients. Followers of Benveniste
still continue to work on dilutions. The best known are Belon and Sainte-Laudry
for their publications in Inflammation Research and Homeopathy between 2004
and 2009, concerning antiserum for IgE and also for histamine effects on baso-
phils. In fact, they confirmed Benveniste’s claim as published in Nature, which
was confirmed in blinded studies, for example the one Ennis participated in.
Several publications denied the biological effect of high dilutions. Here, we leave
out the difficulties in techniques and possible bias and subjectivity on which most
criticism is based (for an overview see Ennis article).
But does water behave strange by shaking endless dilutions? The article ‘‘NMR
water proton relaxation in unheated and heated ultrahigh aqueous dilutions of
histamine: Evidence for an air-dependent supramolecular organization of water’’
[7E] shows that at high dilutions nano-air bubbles have influence on the magnetic
field of water molecules that were endless diluted from a water histamine solution.
By heating this phenomenon disappeared. The article states at the end: ‘‘In con-
clusion, coming back to the controversy of homeopathy, this study reports physical
modifications in the solvent of ultrahigh aqueous dilutions of histamine. It is, of

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320 13 The Pelvis and Herbal Medicine

course, an intriguing result, but it is worth claiming, until proof to the contrary,
that it might merely reflect a trivial air-dependent phenomenon, or an unsuspected
bias, and should not be extrapolated to the so-called ‘memory of water,’ often
alleged to explain the effectiveness of homeopathy’’ [7E].
The ‘‘memory of water’’ will still exercise many minds in the future.
Thus, alternative medicine is not only based on ratio, but also on ‘‘magic.’’ If
regular medicine does not give a solution, people are willing to look at other
places, which is alternative medicine. Alternative medicine cannot guarantee
healing, methods are not transparent and chance is rather large that ‘‘healing’’ have
to be attributed to placebo effects. In cases of cancer, no verifiable fact ever
supported healing by alternative medicine. Evident, it is the old Galenic–Hippo-
cratic framework that governs alternative and herbal medicine.

13.2.1 Herbal Medicine and Slavery in Suriname

Suriname, a former Dutch colony and in origin an English one, but started by the
French, was conquered by the Dutch, while the English had conquered New
Amsterdam, now New York, during the second Dutch-English war (1664–1667).
In 1667, the peace treaty, held in Breda in the South of the Netherlands, ordered all
taken territory into the possession of the conquerors, except some islands in the
Caribbeans and West Africa. Suriname for the Dutch and New York from then on
belonged to England till the independence of the USA. Suriname’s wealth was
based on agriculture. Large estates were constructed and laborers were slaves.
They were brought in by the Dutch slave traders by ship and auctioned on special
markets. The slaves that could escape went, over the river falls, into the hinterland
of Suriname. Punishment for escaping was severe, hanged by a hook through the
ribs, with bound hands till death [7A]. Therefore, they had to hide in the hinterland
and organized their own sheltered communities, still keeping their original social
behavior, including their herbal medicine. Since the slave traders stocked food
crops in Africa for their journey, African plants arrived in Suriname, together with
‘‘stashed seeds in hair and unintentionally in beads of chains, hidden amulets and
through their bowels’’ [7A]. Most of these plants came from Ghana, Benin, and
Gambon were the Dutch caught their slaves. The Marrons, the name for the
escaped slaves, thus had available African plants for their herbal medicines. Still a
large series of African herbs are nowadays used in town for herbal medicines, now
the Marrons have left their isolation. Other medicinal herbs are totally forgotten. In
1863, slavery ended in Suriname and the estate owners started to recruit laborers
from China, Java, and India. All these people brought their own herbal medicine to
Suriname resulting in a mixture of herbal medical treatments. This story shows
that unforeseen ways spread the African herbal medicine to other continents and
the influence of Surinamese ‘‘in origin mixed’’ herbal medicine reached Europe by
the Netherlands, since immigration of Suriname people to the Netherlands was
rather large after the declaration of Suriname’s independence and the following

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13.2 History 321

local war. One should note that half of the Suriname population went to the
Netherlands in total over 300,000 [7A].
At the Naturalis Biodiversity Center in Leiden ethnobotany is stimulated and
carried out. The Suriname medicinal herbs are marketed in towns, e.g., Paramaribo,
the capital, and are studied and collected by scientists. The result is a book
‘‘Medicinale en rituele planten van Suriname’’ (Medical and ritual plants of
Suriname), in which 400 species are described. Nearly 70 herbs, shrubs, and trees
are depicted and described for their use during menstrual problems and a 30 against
gonorrhea. Prostate problems were treated with only three species and solutions for
uterine problems concerned nearly 50 species (see Fig. 13.1 for percentages). The
ginger plant (Zingiber officinale), e.g., is used for ‘‘cleaning the uterus’’ by a ginger
tea to which is added milk, lemon, nutmeg, or honey. Several herbs are also used
for magic and rituals: Wolf’s claw (Lycopodiella cernua or better known as
Lycopodium cernuum) can break love affairs, but is also used in combination with
lemon to stop menstruation.
Genital steam baths are frequently used in Suriname, in most cases for dry sex.
‘‘In many African cultures, plants and other intravaginal desiccants are used to
minimize vaginal secretions. This practice, known as ‘dry sex’, creates a vagina
that is dry, tight, and heated, which is supposed to generate an increased sensation
for the man during intercourse’’ [7C]. But not only for dry sex, reasons given are
Cleanse the uterus after birth, disguise bad smell, prevent and treat fever after
birth, strengthening the woman after birth, contract the uterus after delivery,
slimming after birth, cleanse the uterus after menstruation, stop the menstruation,
reduce uterus pain after delivery, and mystic (e.g., luck charms, love charms) [7C].
Several herbs are used for genital steam baths. The most in use are Campomanesia
aromaticaa (adojakers), Scoparia dulcis (broomweed), Costus scaber (Indianhead

stomach ache 1%
diabetes 2%
high blood pressure 4%
fractures 1 %
skin problems 5%

bitter tonics 7%

winti 56% pregnancy & child care 7%

genital steam bath 16%

Fig. 13.1 Left Percentage distribution of the diseases for which 192 studied species were sold on
the Paramaribo market in 2006. Winti is the African-Suriname faith in ghosts, winti is also the
god of the wind, called up by rhythmic music or protected from by plants. Right African-
Suriname woman taking a genital steam bath (reproduced with permission from journal and
author van Andel [7B, 7C])

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322 13 The Pelvis and Herbal Medicine

ginger), and Siparuna guianensis (fever tree, for percentages of diseases of studied
species see Fig. 13.1). Those that migrated from Suriname to the Netherlands still
use genital steam baths, and various herbs are available in the Netherlands in
Surinamese shops and markets [7C].
It is well known that dry sex increases the possibility on sexual transmitted
diseases and ‘‘dry sex is generally incompatible with the use of condoms’’ [7C].
HIV is a problem in Suriname. Already at the beginning of the 1980s, a HIV center
was started by the WHO at the medical faculty of the University of Suriname. Our
Anatomy Department (in the time I taught there) had to provide materials already
after one year, because the money was spent penny-wise but pound foolish. I
remember strongly that at the farewell dinner in honor of the vice president of the
WHO, who installed the HIV group, none of the professors wanted to be present,
because ‘‘Aids was not present in Suriname.’’ So it ended up with the dean (he
could not escape his duty), the vice president of the WHO and me at the dinner
table. The consequence of such an attitude: ‘‘Suriname is currently experiencing a
serious AIDS epidemic, with HIV being prevalent in more than 1 % of the adult
population’’ [7C].

13.3 Herbal Medicine and Pelvic Problems

Before we can consider male and female pelvic problems in relation to herbal
medicine, it must be clear that a choice has been made. There are so many different
approaches, together with a plethora of recipes that it asks for restriction. The
Reader’s Digest published Natural remedies in 1995 and translations occurred in
several languages somewhat later [8]. It describes alternative medicine for a series
of diseases, including herbal medicine that reached a large audience. Physicians
and scientists were checked with; the text therefore is rather restrained and
stripped from extravagant inactive recipes.

13.3.1 Herbal Medicine for Female Pelvic Problems

The results for the female pelvic affections as published by ‘‘Natural remedies’’ are
summarized in Table 13.1. The effects of the plant extracts are checked by
Dodoens results [4A], the worldwide taxonomic and herbal medicine descriptions
of de Wit [9], and by referenced results of Wikipedia. Web sites of firms that
produce herbal medicines were also consulted, in order to check whether new
applications were described.
The first result is that several pelvic herbal medicines have a rather wide spread
effect, involving several organs outside the pelvis. The ‘‘one plant extract for one
typical disease’’ is not present, which indeed is not favored by herbal medicine.
One plant extract has several different effects on various organs, e.g., yarrow is

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13.3

Table 13.1 Herbal medicine and the female pelvic affections (taken from Natural remedies, the Readers Digest, 1995)
Disease/syndrome Herb: latin name English name Effect of herb Other effects on
Chronic bladder infection Hamamelis virginiana Witch hazel Disinfection genitals Skin, antiviral, bleeding
Mixture of these plant extracts Achillea millefolium Yarrow Urination, soothe bladder ? urethra Bleedings, worms, influenza
Althaea officinalis Marshmallow Idem Cough, stomach ? gut diseases
Elytrigia repens Couch grass Idem Painful urination, water retention
Urtica dioica Stinging nettle Idem Rheumatism, kidney, respiration
Premenstrual syndrome Taraxacum officinale Dandelion Reducing body liquid/diureticum Liver, bile, eye, kidney, warts
Rubus idaeus Red raspberry Against painful cramps Hypophysis, uterus, ovaria
Anthemis nobilis Roman chamomile Against painful cramps Liver, abdomen, bladder
Herbal Medicine and Pelvic Problems

Irregular menstruations Vitex agnus-castus Chaste tree Regulation pituitary Anaphrodisiac, conceiving
Chamaelirium luteum Blazing star Normalizing uterine function Ovarian functions, fertility
Amenorrhea Actaea racemosa Black cohosh Recovery menstruation Liver, premenstrual tensions
Vaginal infection/secretion Geranium maculatum Spotted geranium Inflammation, venous health Hemorrhoids, diarrhea
Mixture of these plant extracts Trillium erectum Wake robin Menorrhagia, menopausal Bronchial ? pulmonary problems
Echinacea purpura Purple corn flower Stimulation immune system

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Vinca major Large periwinkle Alkaloid effects Leukemias ? lymphomas
Galium aparine Clivers Blood pressure ? temperature Wounds, fractures, skin, cystitis
Protection against miscarriage Chamaelirium luteum Blazing star Normalizing uterine function Ovarian functions, fertility
Viburnum opulus Guelder rose Toxic in high concentrations Against painful menstruation
Note Series of plant names are changed, e.g., Agropyron is Elytrigia, some changed their taxonomic place, e.g., Trillium
Several names are botanically not in use anymore, e.g., Cimicifuga, now Actaea
323
324 13 The Pelvis and Herbal Medicine

working on the uropoetic system, but also on bleedings, worms, and influenza.
Only the Purple corn flower has one sole effect that is stimulation of the immune
system, for which Dutch TV spots recommend the tea for cold and winter shivers.
Note that vitamin C is added to the tea.
The black cohosh, recommended for amenorrhea in 1995, has a contraindica-
tion for use during pregnancy, and guelder rose is by regular consumption poi-
sonous. Vinca major (Large Periwinkle) contains alkaloids that can be toxic.
Alkaloids are extracted and purified by phytopharmacology. One should note that
alkaloids are regularly used in medicine, e.g., nicotine, atropine, cocaine, strych-
nine, quinine, morphine, and scopolamine belong to the alkaloids. The various
alkaloids from the species of the Apocynaceae, to which Vinca belongs, each have
a different herbal effect, e.g., Vinca rosea (Madagascar periwinkle) has been
known for its anti-diabetic effect. Rauwolfia serpentia, belonging to the same
group, is used against wounds infected with worms and its fruits are a strong mean
for vomiting. Its effects are presumably due to its alkaloids.
Secondly, most of the herbs are of American origin and were hardly in use in
Europe before the eighteenth century. Indeed, herbal medicine had an enormous
development in the USA [10]. Witch hazel, for example, was used by the Indians,
and some of its applications were taken over. One should note its purposes except
disinfection: ulcers of the skin, scores, tumors, bites and stings, antiviral for
Herpes simplex 1, external and internal bleedings, and more remedies are still
reported.

13.3.2 The Black Cohosh Studies

A rather close look to black cohosh (Cimicifuga or Actaea, Fig. 13.2), on which
several placebo studies have been performed, is now well timed. In Table 13.1, it
was used for amenorrhea, but in a study of 2004, its effect for postmenopausal
complaints was summarized for which it is frequently used nowadays. ‘‘In the year
1985, the isoflavone formononetin was identified in a Cimicifuga extract. Since
this discovery was unexpected for this plant, but matched the historic indications, a
phytoestrogenic effect was formulated for black cohosh. In more recent analyses,
other research groups could not verify any isoflavones in Cimicifuga. One needs to
presume therefore that the herbal drug used for that first phytochemical investi-
gation was contaminated’’ [11]. The active substance is still unknown and the
outcome of the studies till 2004 is that ‘‘the effectiveness of black cohosh has been
proven by controlled clinical studies. It is equal to hormone therapy and with a
slower onset of its effect proves to be better tolerable than hormone therapy’’ [11],
although the authors had to admit that 2 out of 4 studies did not report any effect of
black cohosh and the duration of the studies was only three months, correlating
with the duration of placebo effects.
In 2006, the sNational Institutes of Health (NIH) published an overview of
effects and use of Cimicifuga and in the same year an article appeared in Annals of

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13.3 Herbal Medicine and Pelvic Problems 325

Fig. 13.2 The black cohosh (Cimifuga racemosa, Ranunculaceae), reproduced with permission
of Wiley–VCH Verlag from Osmers and Kraft [11]

Internal Medicine on vasomotor symptoms of menopause with black cohosh [12]


and other herbs with or without soy. The study compared the black cohosh effects
with hormone therapy and placebo up to one year. Its conclusion was: ‘‘Black
Cohosh used in isolation, or as part of a multibotanical regimen, shows little
potential as an important therapy of vasomotor symptoms’’ [12] for menopausal
women. The same year warnings for the induction of hepatitis by black cohosh
appeared by the European Medicines Evaluation Agency (EMEA) and use of black
cohosh together with cancer suppression medicines could reduce the effects of the
regular medicines. Moreover, since the study in the Annals included multibotan-
ical therapy with and without soy, results of these groups were also given: ‘‘In this
large, randomized, double-blind trial, none of the three herbal treatments had
clinically effects on any of the primary outcomes. The only substance that did
produce effect was estrogen therapy’’ [12]. The multibotanical therapy contained
black cohosh, alfalfa, boron, chaste tree, dong quai, false unicorn, licorice, oats,

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326 13 The Pelvis and Herbal Medicine

pomegranate, and Siberian ginseng. Participants of the study could not detect
difference between placebo and other substances due to uniformity of capsules or
medication boxes. A chemical company tested the products and single bats were
used. The outcome of the use of black cohosh is negative for menopausal com-
plaints, and under certain conditions, its use is even dangerous.
Analogous results are published for several other herbs and since in 2007 nearly
15,000 publications appeared on herbal medicine. The screening of herbs is on its
way, but it is a Sisyphean work. More is the pity that it goes with vile discussions
by believers in the unexplained effects of herbal medicine. Phytopharmacology for
the pure plant substances together with large, randomized, double-blind trials for
its applications will bring herbal medicine credibility and will expel ‘‘magic,’’
which makes herbal medicine unreliable.

13.3.3 Herbal Medicine for Male Pelvic Problems

Studies on the renal and lower urinary tract are frequently encountered in litera-
ture, e.g., numerous studies have been performed on plant extracts that are used as
diuretics. An overview [13] shows that of the 100 diuretic plant extracts in use,
only 21 indeed show real effects, and from these 21, only the six species belonging
to the horsetails (Equisetum) and purple sand spurry (Spergularia purpurea) have
‘‘a high level of efficacy’’ [13]. Its use is in lowering blood pressure during
hypertension. The diuretic effect by horsetails is due to its flavonoids [14]. The
effective substance of spurry is to the best of our knowledge not totally ascertained
till now, but the flavonoids extracted from spurry are a good candidate.
The herbal medical studies for male diseases encompass bladder, prostate, and
infections concerning the external genitals. Rare titles are found for the testis. But
as indicated, we will restrict ourselves, in this case to prostatitis.

13.3.4 Prostatitis and Saw Palmetto

Prostatitis in Natural remedies [8] is combated by extracts of purple corn flower


(Echinacea purpura) or by a mixture of meadowsweet (Filipendula ulmaria),
buchu (Barosma betulina), and corn silk (Zea mays). In literature, totally different
herbal medicines are described: saw palmetto (Fig. 13.3) from Serenoa repens,
pollen extract and quercetin. They all should help against non-inflammatory
chronic prostatitis (category 3B, according to the NIH classification) [15]. The
least one can say is that there is no herbal-specific treatment for prostatitis,
although saw palmetto is used by two million men in the USA. There are also few
large, randomized, double-blind trials for the reported herbal medicines. It opens
the possibility for publications in favor by supporters and critical ones by
opponents.

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13.3 Herbal Medicine and Pelvic Problems 327

Fig. 13.3 Saw palmetto saw palmetto (Serenoa repens)


(Serenoa repens) palm and
fruits, reproduced with
permission of forest images,
US forest service, picture
made by James H Miller and
Ted Bodner, southern weed
science society, USA

James H. Miller & Ted Bodner, Southern Weed Science Society, Bugwood.org

Saw palmetto is normally used for lower urinary tract problems, but also for
such problems related to benign prostatic hyperplasia in herbal medicine. ‘‘The
medicinal element of saw palmetto is taken from the partially dried ripe fruit of the
American dwarf palm tree, which is indigenous to the coastal regions of the
southern United States, from the Carolinas and Florida to California’’ [16]. A large
analysis of 21 trials showed that saw palmetto had improvement over placebo in 13
of the studies. In 12 studies, nocturia was reduced by 25 % compared to placebo.
The regular medicine finasteride in use for benign prostatic hyperplasia had in two
studies the same effect as saw palmetto [16]. Long-term effects are unknown and
side effects are reported to be minimal over periods shorter than a year. The
conclusion of the article is: ‘‘Saw palmetto appears to have efficacy similar to that
of medications like finasteride, but is better tolerated and less expensive’’ [16].
One should note that none of the studies were randomized and double-blind. There
is a small sentence that should be reported here: ‘‘Saw palmetto is also widely used
for treatment of chronic prostatitis, although scientific evidence of benefit is
lacking’’ [16]. (Italics ours).
Arnaldo Trabucco [17], urologist at St Johns Hospital in New York, issued a
letter: ‘‘Saw Palmetto warning: Problems with detecting prostate cancer.’’ The
argument is that if saw palmetto works, it will lower the prostate-specific antigen
(PSA) in the diagnostic test, which is the most important measure for prostatic

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328 13 The Pelvis and Herbal Medicine

cancer. Thus having benign prostatic hyperplasia and using saw palmetto, but the
same holds for finasteride, the appearance of prostatic cancer is masked. Prostate
cancer is the second most common death in the USA in men older than 55 [17].
Arnaldo ends his letter with: ‘‘To render a proper diagnostic evaluation, doctors
and patients must communicate with each other, which means that patients should
inform their doctors about their use of any over-the-counter vitamins, minerals, or
herbs. A man who treats himself may have a fool for a patient!’’ [17]. The previous
article denies this effect of saw palmetto, which should mean that saw palmetto
does not inhibit 5-alpha-reductase as finasteride does: ‘‘There has been some
concern that saw palmetto could mask prostate cancer by lowering PSA levels.
However, a randomized study of more than 1,000 patients did not demonstrate this
effect on PSA levels. The same study showed that finasteride decreased PSA levels
by 41 %’’ [12].
The approach by herbal medicines for prostatitis was also studied in a review by
the department of Urology of the Colombia University Medical Center [15]. The
outcome was sad. Statistical significant results for the effect of saw palmetto was
not reached in each of the three studies or not reported. More studies should be
carried out is the only possible conclusion to prove the effect of saw palmetto for
prostatitis.
Pollen extract and quercetin (a mixture of benzopyran and pentahydroxy fla-
vone) only have restricted research trials. Pollen extracts give no evident results.
Quercetin has been studied in one prospective, randomized double-blind, placebo-
controlled trial. Since Quercitin contains bioflavonoids, an effect was found in this
study with the duration of one month.

13.3.5 Phytotherapy and Placebo

In 1996, Franklin Lowe, urologist at the St Luke’s/Roosevelt Hospital Center in


New York, published a critical review on phytotherapy and benign prostatic
hyperplasia. The plant extracts studied are characterized by their phytosterols of
which sitosterols are thought to be the main effective substance. (An example of
sterols is cholesterol, which is the most important sterol in the animal kingdom).
Several modes of actions were proposed in literature, found in vitro, but not
confirmed in vivo: anti-inflammatory effects by inhibition of the prostaglandin
system, interference with the cholesterol metabolism, inhibition of prostate
growth, androgenic and estrogenic inhibition effects, and reduction in sex-hor-
mone binding to globulin [18]. Saw palmetto was also studied and the extract
indeed contained sitosterols, among other substances, and sitosterols are believed
to be the most effective part of the saw palmetto extract.
As always the cited studies were conflicting in their results, while culture
studies found inhibition of 5-alpha-reductase other in vivo studies denied such an
effect. The difference was explained by too high non-physiological dosages used in
the studies that indeed reported effects for saw palmetto. ‘‘Clinical studies have not

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13.3 Herbal Medicine and Pelvic Problems 329

yielded any definitive data on the possible mechanism of action of saw palmetto’’
[18]. However, clinical trials demonstrated positive effects on nocturia, dysuria,
flow rate, and postvoid residual content, although in three out of five studies, no
placebo effect was found, and in one double-blind study, no difference for saw
palmetto compared with placebo was detected. The fact that placebo-treated
patients did not indicate a positive effect is regarded as suspicious. One of the main
denominators to judge a clinical trial is its placebo effect.
Attention therefore to the placebo effect is genuine and justified, especially in
phytotherapy, in which the psychological effect is or can be large. Any medicine
has a psychodynamic and a pharmacodynamic effect. Risks of the use of a med-
icine are coupled to its pharmacodynamic aspect and not to its psychodynamic
effect (see Fig. 13.4) according to phytomedicine. The higher the psychodynamic
component of the drug, the lesser its side effects and risks. (The reasoning in itself
is incorrect: think of cod-liver oil. All children had to take it after the Second
World War in the Netherlands, especially those born from parents in Fortress
Holland with that severe hunger episode (1944–1945).) The rumor went ahead
among the children at school, and fathers and mothers had difficult times to let the
children swallow cod-liver oil; children did everything to escape it, including the
author E.M. But it was a real risk not to take vitamin D: risk-bearing psychody-
namic components do exist).
Psychodynamic effects have a large contribution in antidepressant drugs:
‘‘Differentiated analysis of a representative number of placebo-controlled studies
has shown that when used for depressive conditions, the psychodynamic compo-
nents contribute far more to the overall effect than do the pharmacodynamic
components. In this respect, modern synthetic antidepressants are no better than

Fig. 13.4 Therapeutic value expressed as the ratio between efficacy and safety. The greater the
contribution made by the psychodynamic component to the overall therapeutic effect in any given
indication, the less must be the risk of the drug used for this purpose (reproduced with permission
from Schulz [19])

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330 13 The Pelvis and Herbal Medicine

Hypericum (St John’s wort) products of plant origin’’ [19]. The pharmacodynamic
component is somewhere between 20 and 50 % of these types of drugs. In other
words, plant extracts can have nearly no pharmacodynamic effect but a rather high
psychodynamic effect and with less side effects and risks (Fig. 13.4). The FDA
licensed several antidepressants with a low pharmacodynamic and a large psy-
chodynamic effect. The reasoning of phytomedicine is that the therapeutic value of
a drug should not be based exclusively on pharmacodynamic effects but should
also include the psychodynamic effect, which in fact the FDA did. The conclusion
of this article [19] therefore is, ‘‘The quantification of the two therapeutic com-
ponents, as can be accomplished by a placebo-controlled drug trial, has revealed
that the overall outcome of therapy for various important indications of this kind is
attributable predominantly to the psychodynamic component. It may reasonably be
assumed that the contribution made by the pharmacodynamic effects to the overall
therapeutic response will amount to only about 20–50 %. This raises questions
regarding the clinical relevance and economic value of placebo-controlled studies.
When assessing data on drug efficacy for the purpose of licensing applications,
greater attention should be given to this reality’’ [19].
In fact, the question is, if a randomized double-blind placebo study finds psy-
chodynamic effects of a medicine does that deny the value of these placebo studies?
No, it shows that placebo studies indeed do find such effects and it is to the
administration whether they accept a medicine that has only a 20–50 % pharma-
codynamic effect or not. Licensing of medicines is to the FDA in the USA and other
administrative organs in other countries. The rigor such decisions are taken with is
concern of the administration, and of course, the political influence on the decision
makers plays an important role, especially in the USA. The other question that
arises: Is psychodynamics the same as magic? The difference is racer thin.

13.3.6 Saw Palmetto Again

One needed more studies to affirm the effect of saw palmetto in benign prostatic
hyperplasia (see Sect. 13.3.4). After 2003 [16, 17] a series of articles appeared on
this subject. In 2011, a paper was published with the title: ‘‘What do I tell patients
about Saw palmetto for benign prostatic hyperplasia?’’. The answer given is: ‘‘The
best current evidence suggests that saw palmetto is no more effective than placebo
in treating lower urinary tract symptoms caused by benign prostatic hyperplasia….
However, the authors do not strongly discourage its use when men currently taking
saw palmetto have confidence in its efficacy, because they may be enjoying a
placebo effect and it does appear to be safe’’ [20].
Let us have a look on what arguments this recommendation is based.
1. 15 phytotherapeutic products were tested for alpha-blockers and 5-alpha-
reductase inhibitors, the blockers and inhibitors being the most used in regular
medicine for benign prostatic hyperplasia. Within these 15 products, 12

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13.3 Herbal Medicine and Pelvic Problems 331

contained Saw palmetto in combination with other products and three solely
Saw palmetto. None of the 15 products contained blockers or inhibitors. ‘‘All
phytotherapeutic agents for benign prostatic hyperplasia in this study tested
negative for alpha-blockers and 5-alpha-reductase inhibitors. Inconsistent
results in trials using phytotherapeutic agents are probably not explained by the
presence of standard pharmaceuticals’’ [21].
2. Over 100,000 deaths are presumably caused in the USA due to drug interac-
tions. The figures are quite something: ‘‘69 % of herbal medicinal product users
in the UK do not appear to consult their physician when a serious adverse event
occurs’’ [22]. For Italy it is 61.7 %. It is clear that adverse effects of Saw
palmetto had to be studied. Saw palmetto seems not to influence the uptake
system in the gut, thus not interfering with the uptake of other medicines,
although several specific intestinal transporter systems still have to be studied
[22]. Adverse effects of Saw palmetto were not found by another study [22A].
3. ‘‘The Saw Palmetto Treatment of Enlarged Prostates (STEP) study was the first
randomized, placebo-controlled trial of saw palmetto to be funded by the NIH
and was designed to address the methodological weakness of earlier studies’’
[20]. The outcome of this study was that Saw palmetto had no effect on urinary
functions. Criticism on the study is hardly possible: randomized, a blinded
placebo approach (Saw palmetto tastes bitter!) and large amount of participants
and a long duration of one year. The product was chosen out of several others
because it had high concentrations of Saw palmetto sterols and fatty acids.

The study got criticism: ‘‘One significant limitation of the STEP study was that
it only assessed one dose of saw palmetto and, therefore, could not assess whether
higher doses or a longer duration of treatment might produce beneficial effects’’
[20]. Therefore, an even larger study was carried out, called CAMUS, ‘‘a large,
multicenter, randomized double-blind clinical trial of three escalating doses of an
alternative saw palmetto extract’’ [20]. The results are unequivocal: ‘‘Increasing
doses of a saw palmetto fruit extract did not reduce lower urinary tract symptoms
more than placebo’’ [20A].
If we summarize the results: (1) saw palmetto, if it works, does not act as
regular medicines for benign prostatic hyperplasia do, (2) it has no adverse effects
for the uptake of other medicines (3) saw palmetto does not work better than
placebo (Fig. 13.5).
One should think that the discussion is closed by the results of 2006 and 2011.
However, here, we reproduce Table 13.2 of the article of Kane [20].
Only one out of four meta-studies denies a positive effect of saw palmetto
(Table 13.2); the other three indicate positive effects for urinary symptoms related
to benign prostatic hyperplasia. New publications appeared, between 2006 and
2011. A few of them are randomly chosen, of which the conclusions are given:
1. (2007) ‘‘Most clinical trials of investigating the efficacy of botanicals suffer
from well documented methodological flaws. Saw palmetto has been clearly
shown as comparable to placebo in a trial of sound methodology. While

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332 13 The Pelvis and Herbal Medicine

Fig. 13.5 Change in the American Urological Association Symptom Index (AUASI) scores in
the saw palmetto and placebo groups. Means (±standard error) are given. ‘‘Values at screening
represent prerandomization screening values. The full range of the scale is from 0 to 35, with
higher numbers indicating more severe symptoms.’’ Below the figure is the total of patients
participating in the trial for each group (reproduced with permission from Kane [20])

Table 13.2 Meta-analysis evaluating saw palmetto and other herbal agents
First Year of Journal Study Main findings/conclusions
author publication design
Mantovani 2010 Minerva Analysis of This meta-analysis concluded that a daily
Urol 2 dose of 320 mg of saw palmetto can
Nefrol studies significantly reduce symptoms related
to BPH with a good tolerability
Tacklind 2010 Cochrane Cochrane This systematic meta-analysis showed that
Database reviews saw palmetto provides no improvement
Sys Rev in urinary symptoms secondary to BPH,
compared with placebo. Additionally, it
found that saw palmetto was well
tolerated
Boyle 2004 BJUI Meta- This meta-analysis showed significant
analysis improvement in LUTS and flow rate in
patients treated with saw palmetto for
BPH, compared with placebo
Buck 2004 J Urol Meta- This meta-analysis suggested a wide
analysis spectrum of activity of saw palmetto.
However, the precise mechanism of
action remained unclear. Balance and
caution are needed when extrapolating
the results of in vitro laboratory studies
to the complex human situation
Table is reproduced with permission from Kane et al. [20]. Mantovani F. Minerva Urol Nefrol
(2010) 62:335–40; Tacklind J et al. (2009) Cochrane database Syst Rev; 15: CD001423; Boyle P
et al. (2004) BJU Int 93:751–6; Buck AC (2004). J Urol 172:1792–9

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13.3 Herbal Medicine and Pelvic Problems 333

preliminary results appear promising, to our knowledge the remaining botani-


cals have yet to be evaluated in a trial of similar quality’’ [23].
2. (2008) ‘‘Prostataplex (a mainly Saw palmetto containing mixture) may have
short-term effects in improving symptoms and objective measures in Chinese
men with lower urinary tract symptoms associated with benign prostatic
hyperplasia’’ [24]. One should note that it was a placebo randomized trial.
However no placebo effect was found.
3. (2009) Saw palmetto products are a first-line intervention, usually patient ini-
tiated, in the management of benign prostatic hyperplasia/lower urinary tract
symptoms. These products are generally considered very safe and have minimal
side effects. The magnitude of their efficacy is still to be determined [25].

Does it ever stop? Here, two herbs were selected: black cohosh and saw pal-
metto. Despite randomized, double-blind placebo studies, magic is seemingly still
too strong for modern humans, if one considers the herbal use of these two
examples: both do not work better than placebo. Still they belong to the most
frequently used herbs in the USA. The most astonishing fact is that well-educated
people change over earlier to herbal medicine than less educated ones [26].

13.3.7 Systems Biology

A different approach to herbal medicine is found in systems biology. ‘‘The


pharmaceutical industry is currently beleaguered by close scrutiny from the
financial community, regulators, and the general public. Productivity, in terms of
new drug approvals, has generally been falling for almost a decade and the safety
of a number of highly successful drugs has recently been brought into question’’
[27]. The criticism on pharmaceutical research concerns, among others, the ana-
lytic approach for only one target called: ‘one disease—one target—one-size-fits-
all’ [28]. This also includes that if a medicine during its development does not fit
the target, it is discarded. A more synthetic approach by checking whether the
substance or substances are valuable for other targets should be performed using
both in vitro and in vivo studies and multiple comparisons at the molecular, tissue,
and organ levels. Systems biology has been applied for Chinese herbal medicine:
‘‘Systems biology can also provide insight into the multi-target pharmacology of
herbal formulae. A metabolomic study investigated changes in lipid levels in
transgenic mice with mild hypercholesterolemia given either an herbal concoction
or a known drug (for example, rimonabant, atorvastatin, or niacin). The study
found that the herbal formula caused decreases in plasma cholesterol and tri-
glycerides, and increases in high-density lipoprotein. How the herbal formula does
this should help researchers pinpoint novel ways to treat metabolic disorders,
especially those related to lifestyle’’ [28]. Although this new approach is supported
heavily in science, it is still in its infancy and whether positive results for herbal
medicine are found or not remains to be seen.

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334 13 The Pelvis and Herbal Medicine

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http://priory.com/med/saw.htm. Last visited 16-12-2011
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336 13 The Pelvis and Herbal Medicine

26. Bales GT, Christiano AP, Kirsh EJ, Gerber GS (1999) Phytotherapeutic agents in the
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Chapter 14
Innervation of the Mature Human Pelvis

The peripheral nervous system is responsible for pelvic local steering. Certain
levels of filling of the bladder activate autonomic but also somatic spinal reflexes.
This interaction between autonomic and somatic systems is badly understood. The
basic connections of pelvic organs are described in this chapter. This makes it
possible to treat autonomic–somatic interactions but also neuromodulation and
dorsal rhizotomy.

14.1 Introduction

Anatomical studies of the innervation of the human pelvic floor and the pelvic
structures are few and far between, with the best of them performed years ago (see
Table 14.1). Table 14.1 [1–16] also shows that a straightforward approach to the
determination of the constituents of a peripheral nerve leads to a variety of con-
clusions. This is true for the pudendal nerve, the pelvic plexus and for the
innervation of the external urethral sphincter. All these structures are involved in
the control of pelvic function, or at least literature says so. However, the debate has
been going on for over 50 years. During last 20 years, a new therapy has been
developed for the artificial stimulation of bladder function; neurostimulation. This
intervention requires a dorsal rhizotomy, which involves severing the branches that
brings sensory information from the anal area, the buttock, and from parts of the
upper leg to the spinal cord. Consequently, one should at least be aware how the
connections are organized and this forced us to look again at the nerves mentioned
above. Therefore, this chapter concerns itself with the construction and the con-
nections of the sacral plexus. The sacral plexus is somatosensoric and motoric. The
autonomic innervation of the pelvis is vegetative sensory, plus sympathic and
parasympathic motoric. Special attention is paid to the innervation of the pelvic
floor muscles.

E. Marani and W. F.R.M. Koch, The Pelvis, 337


DOI: 10.1007/978-3-642-40006-3_14,  Springer-Verlag Berlin Heidelberg 2014

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338 14 Innervation of the Mature Human Pelvis

Table 14.1 Comparison of the literature on sacral plexusesa


Pudendal Pelvic External urethral Interconnecting branch
nerve plexus sphincter between S2 and S3
Paturet [13] S2–S4 S2–S4 ? Yes
Cunningham [2] ? ? ? Yes
v. Lanz and S1–S4 S2–S5 ? Yes
Wachsmuth [11]
Hovelacque [8] S2–S4 S2–S3(-S4) P Yes
Piersol [15] S2–S4 S2–S3 ? Yes
Gray [6] S2–S4 S2–S4 PN Yes
Gray [7] S1–S3 S3–S4 PN No
Gil Vernet [4] ? S2–S4 PP No
Gosling et al. [5] S2–S4 S2–S4 PP No
Langman and S2–S4 S3–S4 ? No
Woerdeman [10]
Morris [12] S2–S4 S3–S4 PN No
Pernkopf [14] ? ? ? No
Zuckerman [16] ? ? ? No
Jueneman et al. [9] S2–S4 S2–S4 PN No
Somatic Autonomic
Buruma and Maat ? S2–S4 ? No
[1]
Donker [3] ? S2–S4 PP No
a
From Marani et al. [19]
Abbreviations are S1, S2, S3, S4, and S5 First, second, third, fourth, and fifth sacral nerve
PP Pelvic plexus
PN Pudendal nerve
? Not found or not clearly described

14.2 The Sacral Somatic Plexus

14.2.1 Basic Arrangement

The general anatomy of the cone of the spinal cord connections to the periphery is
extensively described in literature [17]. Fine threads of myelinated and unmyeli-
nated axons (known as radiculi) leave the spinal cord dorsally and ventrally. These
radiculi gather at the dorsal and ventral sides to constitute radices. The spinal
ganglion is set within the dorsal radix. Dorsal and ventral radix fuse to constitute
the spinal nerve. After passing through the intervertebral foramen, the nerve
divides into a dorsal and a ventral ramus (Fig. 14.8). The present account concerns
the ventral rami which constitute the sacral plexus. While the ventral radix is more
motoric in origin, the ventral ramus is mixed conveying sensory and motor
information [18].

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14.2 The Sacral Somatic Plexus 339

14.2.2 Sciatic Nerve

The ventral rami arising from the first, second, and third sacral nerves generally
form a large branch, which unites with the ventral rami of the fourth and fifth
lumbar nerves to constitute the sciatic nerve. The ventral rami of the first and
second sacral nerves contribute largely, the third sacral ventral ramus much less.
The ventral rami of the fourth and fifth sacral nerves never contribute to the sciatic
nerve.

14.2.3 Pudendal Nerve

Contributions to the pudendal nerve complex can be made by the ventral rami of
the first till fourth sacral nerves, as can be seen in Table 14.1. However, in con-
tradistinction to Table 14.1, fibers from the fourth sacral spinal level to the
pudendal nerve complex were never found in our study [19].
All these nerve branches form one major trunk, the pudendal nerve. This nerve
continues through the infrapiriformic foramen and enters, through the lesser sciatic
foramen, into the ischiorectal fossa, passing into Alcock’s canal. The pudendal
nerve never branches before its passage through the infrapiriformic foramen [9,
19].
In all male cadavers studied, the ventral ramus of the second sacral nerve is
involved in the formation of the pudendal nerve complex. The ventral ramus of the
first sacral nerve is included in three out of five cases in our study [19]. The third
sacral nerve was involved in four out of five cases. A summary of all five male
plexuses studied is given in Fig. 14.1.
In all female cadavers of our study [19], the ventral rami of the second and third
sacral nerve take part in the pudendal nerve complex. Among the female plexuses,
there was in one case involvement of the ventral ramus of the first sacral nerve in
the pudendal nerve. A summary of the five female plexuses is present in Fig. 14.2.
In two cases (one male and one female), an interconnection between the sciatic
nerve and the pudendal nerve complex was found. This interconnection was
located distal to the infrapiriformic foramen, which made it impossible to deter-
mine its origin.

14.2.4 Alcock’s Canal

Family names are forbidden by the Nomina Anatomica. Few are still in use and
one of them is Alcock in Alcock’s canal. It is a tunnel-like space made by a
doubling of the fascia of the obturatorius internus muscle, in which nervus
pudendus with its artery and vein hide in the ischiorectal fossa [19A].

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340 14 Innervation of the Mature Human Pelvis

Fig. 14.1 Scheme of the ventral rami of the male sacral plexus. The contributions to the
pudendal nerve and pelvic plexus are illustrated (from Marani et al. [19])

Fig. 14.2 Scheme of the ventral rami of the female sacral plexus. The contributions to the
pudendal nerve, sciatic nerve, and pelvic plexus are shown (from Marani et al. [19])

Benjamin Alcock was born in Kilkenny, Ireland in 1801. He studied Anatomy


in Trinity College in Dublin and in 1827 he got his M.B. at the same university. He
became professor in Anatomy Physiology and Pathology at the just erected
Apothecaries Hall in Dublin, but changed university to Cork where he was
appointed Professor in Anatomy and Physiology in 1849 at the also newly opened
Queens College. He was dismissed in 1855 because he did not govern his
department according to the Anatomy Act, which was executed to overcome grave

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14.2 The Sacral Somatic Plexus 341

robbery of corpses for dissection. Although Benjamin offended his resignation, he


lost. ‘‘In 1859, being unmarried, he went to America and has not since be heard
of’’ [19A].
Benjamin Alcock was contributor to ‘‘The cyclopedia of Anatomy and Physi-
ology’’ edited by Robert B Todd in six volumes (published between 1835 and
1859). According to Macalister (1884) the writers of the cyclopedia displayed ‘‘a
thorough lack of originality,’’ but delivered good anatomical dissection results.
Benjamin Alcock was responsible for the parts: Femoral artery, fifth pair of nerves,
fourth pair of nerves, and Iliac arteries. His fame came from the part ‘‘Iliac
arteries’’ where he described the pudendal canal. Although several authors chan-
ged descriptions, it is now officially called canalis pudendalis, but everybody
speaks of Alcock’s canal.
‘‘Do you have pain in your genital area, rectum, perineum, or anywhere in your
sitting area? Is it made worse by sitting? Is the pain getting worse no matter what
you do? Have you been running around for a long time from doctor to doctor, and
none of them can figure out what your problem is? If you can answer ‘yes’ to some
or all of these questions, then you may have come to the right place’’ [19B]. The
right place is ‘‘The International Pudendal Neuropathy Association’’ called TIPNA
from which the above quotation is taken. Pudendal nerve entrapment syndromes
are so frequently encountered that a special society was erected. One should know
that bicycle riding is one of the main causes of pudendal compression, resulting in:
genital numbness (in 50–91 % of the cases), erectile dysfunction (in 13–24 % of
cases), priapism (lasting erection), infertility, change in PSA concentration, peri-
neal soft tissue damage, torsion of the spermatic cord and testis cancer: The last
item was detected for both bicycle and horse riding. There exists an overwhelming
literature on pudendal syndromes, accentuating the importance of this nerve for the
male urogenital system.
Pudendus anesthesia is frequently applied at the end of labor to release pain in
the perineal area and/or to make an incision possible to ameliorate delivery. A
needle is inserted through the vaginal wall toward the start of Alcock’s canal,
while the needle is directed 1 cm cranial and 1 cm lateral to the ischial spine that
can be palpated. The local anesthetic inhibits nervous action before the branching
of the pudendal nerve occurs, spreading its effect over the whole perineum, whole
vulva, and one-third of the lower vagina [19B].

14.3 Pelvic Plexus

The pelvic plexus is built from the ventral rami of the second, third, and fourth
sacral nerves, [1, 3–6, 13] although different opinions are present in literature (see
Table 14.1).
In our study, the ventral ramus of the third sacral nerve always contributed to
the pelvic plexus in the male cadavers [19]. In four cases, the ventral ramus of the
second sacral nerve did not contribute directly to the pelvic plexus, but only by

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342 14 Innervation of the Mature Human Pelvis

means of a connecting branch between the ventral rami of the second and third
sacral nerves. The one cadaver without this connection did not show any
involvement of the ventral ramus of the second sacral nerve in the pelvic plexus. In
all female cadavers, the ventral rami of the second and third sacral nerves par-
ticipated in the pelvic plexus. Involvement of the ventral ramus of the second
sacral nerve occured in one case solely by means of an interconnecting branch,
while the four other cases had direct connections as well.
In both male and female specimens, there were single cases in which the ventral
ramus of the fourth sacral nerve did not contribute to the pelvic plexus. However,
Baljet and Drukker [20] demonstrated contributions of S2 till S5 to the pelvic
plexus in human foetuses, using in toto acetylcholinesterase staining.

14.4 Interconnecting Branches

In all female (and in four out of five male) specimens, a branch connecting the
ventral rami of the second and third sacral nerves was found. This connecting
branch always sent fibers into the ventral branches of the third sacral nerve, which
contributed to the pelvic plexus, and never to the pudendal nerve. This agrees with
Gray [6]. The branches of the second sacral ventral ramus, contributing to the
pudendal nerve complex, split from the main second ventral branch after the
division of the interconnecting branch from the second into the third sacral ventral
ramus.
In all female specimens, the same interconnecting branch between the ventral
rami of the second and third sacral nerve was found. However, in four out of five
female cadavers, there were also other branches present, which contributed
directly to the pelvic plexus.
The literature is full of disagreement. The topics of controversy are as follows:
The branches contributing to the pelvic plexus [7, 11, 12, 15], the branches
involved in the pudendal nerve [9, 11–13, 15], and the innervation of the external
urethral voluntary sphincter by either the pelvic plexus [3–5] or the pudendal nerve
[6, 7, 9, 12, 21]. Moreover, the existence of these connecting branches
(Table 14.1) and the variability between the sexes are only glancingly discussed
[1, 6, 7, 9, 11–13, 15].
In our study 19, a branch connecting the second and third sacral ventral rami
was demonstrated. The relevance of this interconnecting branch varied between
males and females. In the male, it was crucial for the contribution of the second
sacral ventral ramus to the pelvic plexus in 80 % of our series. In 80 % of the
female cadavers, direct connections between the second sacral segment and the
pelvic plexus were present resulting in a reduced significance for the connecting
branch between the ventral rami of second and third sacral segments.

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14.4 Interconnecting Branches 343

14.4.1 Older Literature

In older literature, the main interest in the lumbar–sacral plexus derived from studies
concerning the development and abberations of the vertebral column [22–24].
Most changes in the vertebral column were related to the lumbar area, since the
number of sacral vertebrae is nearly constant in man. The main interest, therefore,
was directed toward the lumbar plexus, neglecting the sacral branches.
More attention is paid to the sacral plexus in comparative segmentational
anatomy. The description of Bolk [25] of the lumbar–sacral plexus in Orang, in
chimpanzee and in man did involve the sacral plexus. Connections between S2 and
S3 were described. Similar findings were repeated by Preuschoft [26] for the
gorilla.
Studies of the fetal human sacral plexus [27] demonstrated a connection
between the ventral roots of S2 and S3. Earlier studies of the mature sacral plexus
[28] had already demonstrated such a connection in man. An extensive description
of the lumbar–sacral plexus of man [29] showed, in most figures, an intercon-
necting branch between the rami ventrales of S2 and S3. The statistical study of
Bardeen and Wells Elting [30] was mainly directed to the types of lumbar–sacral
plexuses that deliver branches to the limb nerves.
Concerning the pattern of the pudendal nerve complex, there have been both
functional and anatomical definitions. The first, as used by Tanagho [21] and
Jueneman’s group, [9] described the pudendal nerve as the somatic axons of the
sacral plexus, and the autonomic axons as belonging to the pelvic plexus. The
second definition, found in classic literature [2, 7, 12-15] defined the pudendal
nerve as a major trunk coming from the sacral plexus, which left the pelvis by the
infrapiriformic foramen and entered via the lesser sciatic foramen, into the
ischiorectal fossa. No branching was described, before the pudendal nerve com-
plex reached the ischiorectal fossa. In our opinion [19] as based on our gross
anatomy results, the latter definition is correct. Our cadaver study [19] confirmed
the views of Donker [3], Gil Vernet [4], and Gosling and collaborators [5], whom
all considered the pudendal nerve unimportant for the innervation of the bladder
and external urethral voluntary sphincter. The sphincter was innervated by direct
branches from the ventral rami of the second and third sacral nerves, in which the
ventral ramus of the third sacral nerve was the major contributor.
In our series, the ventral branches contributing to the pudendal nerve were the
second and third sacral nerves.
In four cases (three males and one female), involvement of the ventral ramus of
the first sacral nerve was found as well; these being 60 % of the male and 20 % of
the female cases. In the handbook literature, two authors [7, 11] out of nine
mentioned involvement of the first sacral nerve in the pudendal nerve as well.
In one male and one female cadaver, a connection between the sciatic and
pudendal nerve was found. It was difficult to define its origin, but given the
contribution from the first sacral spinal segment to the pudendal nerve existed, and

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344 14 Innervation of the Mature Human Pelvis

observing the course of the fibers, it was most likely to be a contribution from the
first sacral nerve.
The branches contributing to the pelvic plexus differ greatly, both between
individuals and between the sexes.
The ventral rami of the sacral nerves are involved in the formation of the pelvic
plexus, and when decisions have to be made concerning the strategy of neur-
ostimulation and the extent of a dorsal rhizotomy, performed on bladder stimu-
lation patients, [21, 31, 33-38] it is important to be aware of the wide range of
branches and interconnections between the ventral rami of the sacral nerves,.
In the ideal neurostimulation procedure, single stimulation of the third sacral
ventral radix would be sufficient for proper voiding. Because of concomitant
increase in urethral resistance, ascribed to antidromic stimulation of other sacral
levels, dorsal rhizotomy on the second, third and fourth sacral level is performed.
Perhaps, the interconnecting branch between the ventral rami plays a more
important role in this concomitant unwanted stimulation than is currently believed.

14.5 The Autonomic Pelvic Plexus

14.5.1 Basic Arrangement

The autonomic motor neurons are localized within the lateral horn of the spinal
cord from C8 to L4 (sympathic) and from S3 to S5 (parasympathic). Their small
fibers leave the cord by the radiculi and radix ventralis. Just outside the inter-
vertebral foramen, these autonomic motor fibers bend away from the spinal nerve
toward the paravertebral ganglia of the sympathic trunk or toward prevertebral
ganglia. These preganglionic fibers are known as the ramus communicans alba.
Within the paravertebral ganglia, the presynaptic fibers project onto the ganglionic
neurons. Their axons return to the spinal nerve as ramus communicans griseum.
These fibers are postganglionic and use the spinal nerve to reach the peripheral
organs. The postganglionic fibers of the prevertebral ganglia usually follow blood
vessels to reach the viscera [39]. An overview of this system is given in Fig. 14.3.

14.5.2 The Sympathic Trunk and Parasympathic Innervation

The sympathic preganglionic innervation directed to the pelvic organs emerges


from the neuraxis between the 12th thoracic nerve and the 4th lumbar spinal
segments. Both sympathic trunks reach the pelvic area lying on the coccygeal
muscles. They are interconnected ventral to the os sacrum. The spinal parasym-
pathic preganglionic fibers to the pelvic organs originate from the third, fourth, and
to some extent the fifth, sacral segments.

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14.5 The Autonomic Pelvic Plexus 345

Fig. 14.3 Overview of the


whole autonomic system
(except brachial plexus) in a
crayon drawing by miss Sofie
van der Berg, dissection by
Willem Reychard,
reproduced with permission
of the Dept. Anatomy and
Embryology, Leiden

14.5.3 The Hypogastric Nerves

From the first lumbar nerve onward, lumbar splanchnic nerves cross the aortic
trunk. They first reach a prevertebral ganglion: the ganglion hypogastricus supe-
rior. Parallel to the bifurcation of the aorta into the aa. iliacae communes, the
splanchnic nerves divide into a left and right nervus hypogastricus, which both will
reach an extended plexus, the pelvic plexus [39, 40].

14.5.4 The Pelvic Plexus

The issue of whether the pelvic plexus is the same as the hypogastric inferior
plexus will not be discussed; they will be considered identical. The pelvic plexus
integrates hypogastric nerve, sympathic and parasympathic innervation
(Fig. 14.4). The presence of interplexal connections has not been proven. This
plexus innervates all the pelvic viscera, and branches can also ascend to the distal

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346 14 Innervation of the Mature Human Pelvis

Fig. 14.4 Schematic


drawing of the motor
innervation of the bladder,
the urethra, and the pelvic
floor (reproduced with
permission of the SWUN and
courtesy prof. P. Donker )

colon, renal pelvis, and upper ureter. Branches toward testis, ovary, and upper
pelvic vessels have been reported.
It is not disputed that smooth muscle and glands are supplied with both sym-
pathic and parasympathic autonomic innervation. It is the striated urethral muscle
that leads to debate in the literature. Is the striated muscle of this sphincter, mainly
innervated from inside or from outside the pelvic floor? Does the innervation
involve branches of the somatic sacral plexus passing the autonomic pelvic plexus,
or of the pudendal nerve outside of the pelvic floor? The position of the pelvic
plexus is given in Fig. 14.5a and b. Two articles focused on the composition of the
nerves of the pelvic plexus [3, 41] are pertinent to this question.
The Winckler study [41] used silver impregnation to distinguish myelinated
from unmyelinated or small myelinated nerves. This study showed that mainly
unmyelinated axons were present in the hypogastric nerve, whereas the pelvic
nerves contained myelinated fibers of different calibers and these nerves were
directed toward the pelvic plexus. Light microscopy can identify unmyelinated
fibers in between myelinated fibers only with difficulty. Nevertheless, this study
demonstrated that somatic innervation was directed toward the pelvic plexus,
though without resolving its sensory or motor characteristics. This interpretation

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14.5 The Autonomic Pelvic Plexus 347

Fig. 14.5 a Stereo-overview of the localization of the pelvic plexus in relation to pelvic
structures and the localization of the pudendal nerve, reproduced with permission and courtesey
Prof. Dr. P. Donker ). b Anatomical preparation of the pelvic plexus (courtesey C. P. Maas  and
M. C. de Ruiter)

was extended by Donkers finding [3] of myelinated fibers with a diameter over
15 lm directed to the striated muscles of the urethra. This indicates that the
striated urethral muscle is not supplied by the pudendal nerve, but by means of
motor axons which run in the pelvic plexus [3]. Non-myelinated fibers are plentiful
in these nerves, indicating that autonomic innervation uses the same pathways to
reach the pelvic organs [3]. The nerves to the rectum are mainly non-myelinated.
The muscles of the pelvic diaphragm (m. levator ani and m. coccygeus) are
innervated by nerves from the sacral plexus. These nerves are known as the rami
muscularis m. levator ani [42]. The discussion on the innervation of the pelvic
diaphragm becomes more complicated when one accepts that the levator ani is one
muscle and not a group of separate muscles (see Chap. 8).

14.6 What About the Pudendal Nerve?

The pudendal nerve passes through the foramen ischiadicum majus (pars infra-
periform) and minus to travel through the canal of Alcock. Prior to entering this
canal, it issues the nervus perforans ligamenti sacrotuberalis (dermal innervation
of the tuber). Within the canalis pudendalis (Alcock’s canal), the nervi rectalis
inferior, for the innervation of the anal sphincter, branches off. Subsequently, the
nervus pudendus divides into smaller branches: the nervi perineales for the m.
ischiocavernosis, which continue into the nervi scrotales for the dermal innerva-
tion of the scrotum, and for the innervation of the m. transversus perinei sup., and
the ventral part of the m. sphincter ani externus. It is claimed that the nervus
dorsalis penis (clitoridis) reaches the m. transversus perinei profundus. It is

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348 14 Innervation of the Mature Human Pelvis

Fig. 14.6 The fossa


ischiorectalis in which the
pudendal arborization and the
pelvic floor muscles have
been dissected out; drawing
by H. Wetselaar, dissection
by W. Reychard, with
permission of the Dept.
Anatomy, Leiden

doubtful whether the striated sphincter is innervated by pudendal branches. Dis-


section of the fossa ischio rectalis (Fig. 14.6) gives access to the canal of Alcock.
Individual nerves were observed that left the canal and enters the m. levator ani,
but these were never found to reach the external urethral sphincter. The contri-
bution of the S4 nerve to the pudendal nerve should selectively innervate the m.
levator ani [17] (see also Table 14.1), which however is contradicted by our study
since S4 did not contribute to the pudendal nerve.
One has to realize that the proposed non-involvement of the pudendal nerve in
the innervation of the urethral-striated sphincter is a view not taken by the
majority of researchers.

14.7 Neuromodulation

The construction plan of the sacral plexus is also important for several other issues
concerning incontinence. These are as follows:
1. SANS (=Stoller’s Afferent Nerve Stimulation); [44]
2. Electrical pelvic floor stimulation (EPFS); [43]
3. Neuromodulation of sacral nerve stimulation, [45]
Stimulation can be performed in the direction of the motoric components (2 and
3) of the nerve or in the direction of the sensory component (1). Let’s start with
SANS.

14.7.1 SANS

One of my urologic colleagues noticed that the midwife started rubbing his wife’s
lower leg above the ankle just before labor started. The midwife’s explanation was
that this treatment relaxed uterine contraction to allow more time for cervical
dilatation. In fact, the midwife stimulated the tibialis nerve. My colleague used this
same nerve in the SANS technique to modulate unstable contractions of the
bladder in urge or frequency incontinence.

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14.7 Neuromodulation 349

The optimal point to stimulate coincides with the Sp(spleen) 6 locus (Sanyinjiao)
of the acupuncturist. In acupuncture, this site is considered to be significant for
treatment of disturbances of the urogenital tract [46]. In SANS, a needle electrode is
connected to an electrical stimulator generating 1–10 mA. SANS is also termed
percutaneous peripheral nerve stimulation, since most probably the tibialis nerve is
stimulated. 50 % of the patients so treated experience a reduction in voiding and
urge episodes, in daytime and nighttime.
The tibial nerve originates from the spinal nerves L4, L5, S1, S2, and S3. Hence,
stimulation of the tibialis antidromically sends impulses to all these spinal seg-
ments, including the S2 and S3 branches (S3 mainly in males and S2, S3 in females)
which constitute the nerves to the pelvic plexus and thus to the bladder. Stimu-
lation of this nerve at the Sp 6 locus in rats reduces spinal neuronal cell activity
[47], and in this way, involuntary contractions of the bladder are also reduced.
However, the mechanism by which this stimulation of the tibial nerve works is
unknown. Factors which may be involved are the inhibitory interneurons at several
spinal cord levels, and the descending pain-suppressing system. Termination of
treatment results in return of incontinence.

14.7.2 EPFS

EPFS [48, 49] was mainly carried out by anal or vaginal plugs, with the disad-
vantages that leakage of electric current induced pain on stimulation and injured the
underlying mucosa. Intramuscular electrodes which could stimulate the pelvic floor
muscles were thought to be beneficial for urinary incontinence [43]. Electrodes
were implanted both in the levator ani muscle and also near the pudendal nerve. An
improvement of 80 % in overactive neuropathic bladder patients was recorded [43].
The placement of the electrodes remains a matter of debate. In animals, the elec-
trodes have to be placed in the sphincter muscle itself, [50, 51] while in humans
pelvic floor muscle implantation also seems to work out well [43].

14.7.3 Sacral Nerve Stimulation

Neuromodulation is carried out by stimulation of the third sacral segmental nerve


(S3) in patients with urge incontinence and with therapy-resistant idiopathic
detrusor instability [52]. Sacral nerve stimulation requires placement of an elec-
trode in the S3 foramen of the sacral bone. A dorsal approach made it easy to
identify the S3 foramen. The electrode had to be brought into the ventral side of the
opening against the S3 ventral ramus. This procedure was minimally invasive, as
compared to neurostimulation. Stimulation was first tried in an acute test stimu-
lation followed by a subchronic test phase [52]. Nearly 40 % of the selected
patients did not pass this test phase and were not selected for this treatment

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350 14 Innervation of the Mature Human Pelvis

technique. At permanent, implantation of the electrode stimulation occurs with a


frequency of 10 pulses per second and a pulse width of 210 ls, at an amplitude of
2.7 ± 0.4 V.
Correlation of clinical outcomes with urodynamic tests, both in classical
treatment and in chronic neuromodulation, was poor [52]. Urodynamic evidence of
bladder instability in patients treated with S3 stimulation was unchanged, although
the patient could have become completely continent. The most puzzling finding,
however, was that the same method was also beneficial for bladder retention, in
which the bladder is not hyperactive but rather hypoactive.
The placement of the electrode may be checked by pelvic floor contraction and by
bending of the great toe, which indicates the occurrence of orthodromic stimulation.
The explanation as to how neuromodulation works has been sought in the antidromic
stimulation of the inhibitory neurons in the spinal cord [52]. However, neither the
impedance nor the amperage of the stimulation at the nerve is in fact known. Con-
sequently, the clinician does not know what he is stimulating (non-myelinated, small
or large myelinated axons), nor whether solely antidromic, or antidromic and
orthodromic, stimulation occurs. Since only S3 is stimulated, it is possible that
patients in whom S2 is the main contributor to the bladder [19] will find the treatment
ineffective. This may explain the 40 % failure rate of the procedure.

14.8 Alternatives for Dorsal Rhizotomy

A dorsal rhizotomy has very significant consequences; loss of sensation. Clinicians


understand very well that dealing with lack of sensation in buttocks and back of
the upper legs is a matter of urgency in neurostimulation operations [31–34].
Gaining partial continence at the cost of losing sensation in the lower part of the
body is a choice between two evils. Two approaches are now being developed to
overcome the adverse effects of dorsal rhizotomy: a cryotechnique, and the
application of a cuff electrode.

14.8.1 The Cryotechnique

Cooling a nerve will reduce its capacity to pass action potentials over the cooled
nerve segment. Since the nerve(s) stimulated to restore the voiding function also
contains non-myelinated fibers for the detrusor, and myelinated fibers to the ure-
thral sphincter, unphysiological contraction of the bladder, the voiding mecha-
nism, and urethral closure, the anti-voiding mechanism, are evoked simultaneously
by the stimulation. Upon cooling the activity of myelinated fibers is blocked at a
higher temperature than the activity of unmyelinated fibers. Thus, by slowly
cooling, the nerve a temperature will be reached at which conduction in myelin-
ated fibers solely is blocked. At lower temperatures, all conduction is blocked.

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14.8 Alternatives for Dorsal Rhizotomy 351

Fig. 14.7 a ‘‘A symmetrical tripolar cuff electrode’’ [54] ( 1994, IEEE). b ‘‘Response of a
4-lm fiber. It shows the deviation of the membrane potential from the resting potential at each
mode of Ranvier after initiation of a rectangular pulse of 320 ls. The nodal potentials are shown
at 6 intervals of 60 ls after initiation of the pulse. At the top, the cuff and the position of the
contacts are shown’’ [54]. Proximally inhibition of the pulse occurs, distally the pulse propagates.
[54] (with permission and courtesey J. Holsheimer,  1994, IEEE)

If conduction has selectively blocked all myelinated nerves than it is possible


that after stimulation results in voiding without urethral closure. If at the same time
the dorsal radix for all incoming sensory information to the spinal cord can be
blocked too, a dorsal rhizotomy would not be necessary anymore [53]. However,
such a strategy calls for two cooling electrodes (one around the nerve, the other
around the dorsal radix) and presumably a stimulation electrode. It is only a matter
of time before a single multifunctional, electrode is constructed.

14.8.2 The Selective Stimulation Electrode

Electrodes can block large myelinated fiber conduction and, at the same time,
stimulate small myelinated and unmyelinated fiber conduction, since the threshold
stimulus current is inversely related to the fiber diameter. Nerve cuffs with a tripole
configuration, containing ring-shaped contacts, have been developed and applied
(Fig. 14.7). At the cathode, all fibers are excited, and at the anode, the conduction
of the large fibers is blocked. As a consequence, only action potentials of small
fibers reach their target. But all small axons are activated, including the sensory
ones. Moreover, the action potentials of small motor axons will also propagate
backward into the spinal cord, producing stimuli that are converted to reflex
actions of the bladder and the striated sphincter. Therefore, a dorsal rhizotomy
must still be carried out.

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352 14 Innervation of the Mature Human Pelvis

Using a multiple electrode, the selective stimulation could be carried out while
more proximally placed electrodes in a cuff could block all the retrogradely
directed conduction [54].

14.9 Central Connections

A dorsal root ganglion (DRG) is an accumulation of cell bodies of primary sensory


neurons. The central and peripheral processes of these cell bodies constitute the
sensory connection between periphery and spinal cord. Each dorsal root of the
spinal cord contains at the level of the intervertebral foramen an elongated
thickening called spinal ganglion or DRG. This thickening, which is sheathed by
the continuation of the surrounding membranes of the cord into those of the
peripheral nerves, is caused by the accumulation of cell bodies of primary sensory
neurons (DRG cells). These originally bipolar cells later on become (pseudo-)
unipolar. The single axonal process soon divides in a T-like fashion into a
peripheral branch, which is connected to somatic and visceral receptors, and a
central branch, which enters the cord. The continuity of peripheral and central
branches constitutes the major afferent axonal pathway to the cord [57] (Fig. 14.8).

14.9.1 Micturition Control

The micturition control has a peripheral part, described before, and a central part.
Information reaching the spinal cord is distributed toward the proper brainstem
areas, and these areas provide the spinal cord with information for the motor
control of bladder and urethra with its sphincters. The information also goes to the
cortex.
Incoming information can be send to higher centers in two forms: unchanged
propriospinal information or changed information, the last one due to projections
on spinal cord neurons that by their axons relay information to higher centers.
Large quantities of sacral pelvic ascending visceral signs belong to the changed
information. The pelvic visceral ascending information is changed during arrival at
the dorsal side of the start of the brain stem by neurons present in so-called dorsal
column nuclei or the solitary nucleus and is sent to the other or both sides of the
brain stem to project into the thalamus, the large relay center for sensory infor-
mation. From there on, it is processed toward the cortex [57A].
The changed information that projects onto the nucleus of the solitary tract,
which projects bilaterally, via the parabrachial nuclei to the thalamus and hypo-
thalamus, and from there on to the cortex, is discussed. The older literature
indicates that this information is relayed via the spinothalamic system and that no
general visceral pelvic information arrives at the solitary tract and its nucleus.

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14.9 Central Connections 353

(a) (b)

(c)

Fig. 14.8 a Dorsal view of part of the human cord with its membranes (dura and arachnoid
mater: DM + AM) put aside and dorsal root ganglia (DRG). The central connections of a DRG
through its dorsal root (DRT) and rootlets macroscopically define the corresponding spinal cord
segment (CS). b Square indicates the dorsal area seen in a (1: dorsal root ganglion, within dorsal
root, 2: ventral root). c Section through a dorsal root ganglion, enzymatically colored (NADHP
dehydrogenase) for dorsal root ganglion cells. scale bar is 100 lm (Taken with permission from
Marani [57], Dorsal root ganglion, Encyclopedia of Neurological Sciences, 01142., Elsevier)

The changed information is mainly for general pelvic sensory information,


while pelvic pain is relayed by the so-called postsynaptic dorsal column pathway.
Pelvic pain information ascends by the utmost medial part of the dorsal column or
gracile part (Fig. 14.9) and will end in the most rostral part of the gracile nucleus.
Clinically, it is possible to stop intolerable pelvic pain by a midline destruction of
left and right utmost medial parts of the gracile column at thoracic levels [58].
Central motor activity is better understood. In 1924, Barrington sent in an
article entitled: ‘‘The effect of lesions of the hind- and midbrain on micturition of
the cat.’’ Already in 1914 and extended in 1921, Barrington indicated that mic-
turition reflexes in the cat arose in the brain stem and not in the spinal cord. One
reflex is triggered by distension of the bladder and the other by fluid passing
through the urethra. Using the first stereotactic Horsley-Clarke apparatus, in fact
developed by Robert H. Clarke (1850–1926), which Barrington had in loan of
Clarke and using the stereotactic atlas, also codeveloped by Clarke, he succeeded
to accurately pinpoint the region that relayed the signals to the spinal cord that

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354 14 Innervation of the Mature Human Pelvis

Gracile nucleus

Fig. 14.9 Sensory and motor projections of pelvic structures involved in micturition. a Section
medulla oblongata, series H5797/45 see [57A], b Spinal and supraspinal structures (taken from
Holstege and Griffiths) [57A]

effectively contracted the bladder. From then on, the region carries his name:
Barrington’s nucleus. Nearly, all further research has been done in rat and cat,
human neuroanatomical or neurophysiological results are mainly lacking. How-
ever, clinical results showed that a comparable location is present in humans.
Knowing the origin of the bladder motor signals, Holstege and Griffiths stim-
ulated this area in the cat and indeed could show the specific intravesical pressure
changes belonging to contractions of the bladder and pelvic floor contractions by
EMG. Since the stimulation area was presumably larger than the small Barring-
ton’s nucleus (see Fig. 8.12), they called it the M (medial) region. This region
projects specifically to parasympathetic spinal cord regions, responsible for
bladder smooth muscle contractions. They proposed a more laterally placed area
(L-region) that projected onto the nucleus of Onuf, responsible for sphincter
contraction. So a nice on and off system was developed (see Fig. 14.9). However, a
few years later, the L-region was denied, which brings one back to the Barrington
results.

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14.9 Central Connections 355

A more specific look into the localization of Barrington’s nucleus brings up


surprising results. In Neuroanatomy, the nucleus tegmentalis laterodorsalis (TLD-
nucleus) encompasses Barrington’s nucleus and some more groups of neurons. It is
placed in the vicinity of the locus coeruleus, a noradrenergic nucleus that can send
its axons directly up to higher structures, bypassing the thalamus, the sensory
switch for cortical information production. Next to the locus coeruleus is found the
mesencephalic nucleus of the trigeminus [59].
Unknown neurons in this region are described. Intermingled with and lateral of
the mesencephalic trigeminal nucleus are neurons present that send their axons to
the spinal cord around birth, but retract that axon a few days after birth. Bar-
rington’s neurons will send their axons downward to the sacral spinal cord, but
within Barrington’s nucleus, also non-projecting neurons are present [59].
Barrington neurons with connections to the spinal cord will fire to cause con-
traction of the bladder by activating parasympathetic motor neurons. Barrington
neurons without spinal cord projections contain neuropeptide S, a neurotransmitter
that is related to stress, especially anxiety. The neurons intermingled with the
trigeminal mesencephalic tract showed firing ‘‘that is correlated with phases of
bladder contractility; they are likely part of the micturition circuit’’ [59A].
Moreover, Barrington’s projecting neurons contain corticotrophin-releasing factor,
which is also correlated to stress.
So, Barrington’s projecting neurons express a factor that is stress related, while
special stress-sensitive neurons are located directly next to these projecting neu-
rons. At somewhat more distance, non-projecting neurons seemingly codetermine
Barrington projecting neuronal activity. If one knows that several types of firing
frequencies are present within TLD neurons, that are supporting for ‘‘an increase
in bladder contraction rapidly and strongly via feed-forward regulation, while also
maintaining high-bladder pressure via positive feedback from bladder afferents’’
[59A], then the importance of this area becomes clear. However, Barrington’s
nucleus has nothing to do with the relaxation of the bladder [59].
Thus Barrington’s nucleus is a small nucleus that is responsible for activating
parasympathetic neurons that cause contraction of the bladder. It is stress sensitive
and needs a series of surrounding also small, non-spinal-cord-projecting neurons to
act properly via feed-forward and feedback systems.
In Chap. 19 we will meet Onuf’s nucleus, also one of the smallest nuclei and
responsible for pelvic sphincter contractions. Is it due to their smallness that
problems like incontinence and bladder dysfunctions are on the lookout? At least
we know that plasticity of small neuron groups is less than that of large neuron
groups.
To summarize, there exists no proper knowledge concerning the organization of
neuronal connections between spinal cord and the uropoetic target organs [55,
56]. Moreover, nearly all electro-stimulation invented to overcome bladder dis-
turbances of the uropoetic system have been devised from this ignorant position. In
this context, the relation between anatomy and physiology could be regarded as
the blind leading the blind.

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356 14 Innervation of the Mature Human Pelvis

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sergiocamargo47@gmail.com
Chapter 15
Smooth Muscle Electromyography
of Bladder and Uterus

Electromyography of smooth muscles is difficult to carry out. The frequency is


low, and therefore, all kind of disturbances interact with the real signal. Using
fluorescent spheres with the same diameter of the electrodes, both movements of
the bladder wall and electrical activity can be measured. Electrical activity can
show: single spikes, bursts, and continuous activity. The movement of the muscles
show that contraction and relaxation can be present at the same location, but in
different layers of the bladder. Uterine smooth muscle electric activity is even
more difficult to study, especially during labor.

15.1 Introduction

All kind of studies has been carried out to understand incontinence. However, the
most effective approach, the bladder EMG, which could provide proper under-
standing of incontinence, has been neglected to date. Effective and coordinated
storage and effective expulsion of urine are both a prerequisite for urinary func-
tion. Moreover, while efficient storage need not to be connected to muscle function
per se, seemingly it is.
Consequently, the activity of the bladder smooth muscle, the detrusor, should
be one of the targets of research [1] related to sound expulsion and is perhaps also
involved in storage. Dysfunction of voiding must be represented in detrusor or
sphincter malfunction. Bladder electromyography should demonstrate any aber-
rations of emptying of the bladder, since the muscle activity, seen by its electrical
activity, determines the voiding. In this chapter, we not only discuss urine and
uterine expulsion, but also whether or not muscle activity is present during storage.

E. Marani and W. F.R.M. Koch, The Pelvis, 361


DOI: 10.1007/978-3-642-40006-3_15,  Springer-Verlag Berlin Heidelberg 2014

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362 15 Smooth Muscle Electromyography of Bladder

15.2 History

The story starts in 1951 [1], when Corey et al. [2] placed electrodes into the human
bladder against the lateral surfaces of the vesical neck. The electrodes were
inserted transurethrally. Although an electrical signal could be found (amplitude
0.6 mV, frequency 0.1–1.0 Hz), the same signal could be produced by shifting the
electrodes somewhat (Fig. 15.1). This study concluded that movements of the
electrodes mimicked the wave-like contractions present in bladder muscles.
Brunsting [3] tested several types of electrodes and moved the electrodes over a
fixed cat bladder, a wet sponge, a rubber bulb, and stirred a saline solution with the
electrodes. In all these cases, the same ‘‘bladder waves,’’ as reported by Corey,
could be produced (Fig. 15.1). Brunsting argued that the electric bladder waves are
artifacts. It looks like Yiddish humor. The same fact differently interpreted.
Hook electrodes were implanted by Stanton et al. [4] through the vaginal wall
into the inner bladder wall of conscious female patients. Signals were recorded
(0.1–2 mV; 0.10–0.5 Hz) and compared to the signals of Corey. However, the
results of Brunsting were not discussed. Later on, it was stated that these elec-
tromyographic results could not be correlated to changes in bladder pressure.
The next try was in the 1980s: profuse random activity was picked up with the
electrodes (Craggs and Stepheson [5]; 1 mV, 0.07–1.0 Hz), but the activity was
interpreted as an artifact, due to fluid movements around the electrode tip. Activity
in the band of 40–200 Hz could not be correlated to bladder function, and activity
between 10 and 40 Hz also could not be attributed to bladder emptying. Seem-
ingly, we were back in the 1950s.
At the end of the 1980s, researchers in Japan [6] started electromyography too.
A balloon was inserted transurethrally into the bladder possessing electrodes at its
outer surface. By inflating the balloon, the electrodes were kept stationary. Normal
subjects showed signals of 0.05–1 mV: A low-voltage subject group (0.01 mV)
included spina bifida patients and a high-voltage group (0.3–2 mV) comprised
patients having mild spinal cord injuries. It was found that bladder volume and
electromyographic results were related. Nevertheless, the same group [7] subse-
quently indicated that many problems in their research still had to be solved,
especially those concerned with bladder movement.
To summarize: none of the studies has clearly established electric activity of the
bladder, and the occurrence of artifacts cannot be denied.
These drawbacks however can be explained (Kinder and van Leeuwen [1]), as
follows:
• Low frequencies, such as 1 Hz, coincide with artifact frequencies.
• Metal electrodes can produce voltages if moved in a conducting fluid and urine
is such a fluid.
• The bladder changes its contours during emptying, which makes it difficult to
keep electrodes in place.
• Implanted electrodes pick up electrical activity from heart and bowels.

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15.2 History 363

Fig. 15.1 Upper part Diphasic (A, B) ‘‘bladder waves’’ as described by Corey et al. [2]. Lower
part Examples of recordings from bladder of cat using externally implanted, needle-type
electrodes. A typical ‘‘bladder waves’’; B ‘‘bladder wave’’ occasionally seen during spontaneous
activity; C diphasic waves caused by pressing on one electrode to push it deeper into the bladder;
D diphasic wave produced by pressing one of two electrodes immersed in saline. Redrawn with
permission from Kinder and van Leeuwen [1]

So the questions arise is: There electrical activity in the bladder or not and can it
be recorded or not? Smooth muscle does have electrical activity, and since the
detrusor is smooth muscle ipso facto, there has to be activity. Thus, electrical
activity of strips taken out of the bladder can be measured [8], and single smooth
muscle cells can be caused to contract by electrical stimulation [9].
Moreover, one has to distinguish the electrical activity produced by the nerve
fibers entering the musculature to start contraction from the electrical activity of
the bladder musculature proper. Both activities will be detected when using
electrodes implanted in the bladder wall, although their frequency and amplitude
will differ. Another relevant phenomenon is the passive activity of the bladder
wall. The bladder wall contains elastic fibers, which are stretched by filling the
bladder, and will react just like a piece of elastic tissue during emptying: a passive
contribution to voiding [10]? The latter point makes it difficult to argue that there
has to be electrical activity over the whole voiding trajectory. This may explain
why, during voiding, there is not always a total correlation between electric
activity and bladder behavior.

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364 15 Smooth Muscle Electromyography of Bladder

Since reliable detrusor EMG data have not yet been achieved, recent research
has been directed to attempt to describe electromyography of the bladder (see
[1, 11, 12]).

15.3 Recording the Bladder EMG

The starting point of this approach was that, since the electrocardiogram could be
traced with recently developed very sensitive types of electrodes [13], the same
could be done for the bladder in the rabbit. Thus, a resin spoon containing 240
working electrodes was placed on a rabbit bladder [1]. The confusing electrical
activity of heart and bowels was stopped or determined, respectively. Signals with
a frequency between 0.7 and 500 Hz were looked for.
The first question investigated was: How long after the ending of the cardiac
activity would the rabbit’s bladder still react with a contraction? Adding carbachol
(a replacement for acetylcholine), bladder contractions that resulted in a change of
the bladder pressure could be evoked for up to 30 min. The second question was
whether artifactual EMG could be produced or not. Moving the electrode with a
certain frequency was found to result in the same frequency in the electrode signals.
Several other manipulations were carried out, but in general the actually produced
EMG could be detected and distinguished from the real bladder EMG [1].
The real bladder EMG in the rabbit stayed below the 25 frequency band. The
spikes found were of 1.2 Hz and could be described as a triphasic wave [1]
(Fig. 15.2). So the morphology of the spikes could be discerned and described.
Since the electrode had an array of 240 electrodes with distances of nearly 2 mm
between the electrodes, the same spike could be recognized on the adjacent
electrodes if it moved over the bladder. Time shifts of the spikes were found, so
propagation of the electrical activity over the bladder surface could be recorded
[1]. The propagation velocity was 30 mm/s, which is well in the range of spike
propagation in smooth musculature. Surprisingly, slower spike waves were also
encountered [1].
These electrical activities did not relate to pressure changes in the isovolumetric
bladder. However, this can be understood because the array of electrodes showed
the activities to be local effects. Thus, certain areas of the bladder contracted, while
the others were in a state of relaxation. This results in pressure changes below the
measurable level of the microtip pressure transducer in the bladder [1, 14].
In other words, electrical activity can be detected in the bladder, which is not
artefactual, and which contains specific characteristics such as spike propagation
and slow waves, which arise from smooth muscle activity.
In the following year, a research group based at the Urological Clinic of the
Hospital of the City of Mannheim published an article on smooth muscle elec-
tromyography of the urinary bladder in rats (Scheepe et al. [12]). The authors
summarize their findings as follows: ‘‘Analyzing the detrusor-EMG in different
frequency bands revealed the most clear correlation with intravesical pressure rise

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15.3 Recording the Bladder EMG 365

Fig. 15.2 a Single spikes detected by one electrode for a time period of 100 s on the rabbit
bladder dome. Bladder pressure is indicated in the lower trace. b The two main types of rabbit
electrical activities that could be discerned in single spike trains (courtesy M. Kinder see also
Kinder et al. [14])

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366 15 Smooth Muscle Electromyography of Bladder

in a frequency band above 3 Hz, whereas the activity below 3 Hz was apparently
random and unrelated to pressure rise. The evoked potentials were chiefly
biphasic, several mono and polyphasic events were also observed [15].’’
Subsequently, Neurourology and Urodynamics, the journal in which Scheepe
et al. [12] published their article, published a letter to the editor (called ‘‘editorial
comment’’) in which Kinder et al. [16] respond skeptically to the Scheepe
experiments. They interpreted every signal that exceeded twice the standard
deviation of the random noise level as bladder EMG. This means that accidental
knocking on the table where the experiment is carried out will be included in the
bladder EMG. So there we are again: contradictory facts concerning the bladder
EMG, but in the end: EMG of the bladder can be regarded as confirmed by two
scientific groups.
The main problem remaining is the frequency and form of the signals produced
by the bladder smooth muscle. In comparing the studies described here, it should
be stressed that the Scheepe et al. [12] article did not check for artificial distortions
that could be falsely interpreted as real bladder EMG (see [1]).
Nevertheless, the story continues: Kinder et al. [11], now they had established
that bladder smooth muscle activity could be measured directly on the rabbit’s
bladder, asked themselves whether these signals could be picked up on the surface
of the abdomen, if possible in humans or not [11]. A noninvasive method to record
the bladder electromyography in humans would significantly advance diagnostics,
catching up with striated muscle electromyography. What had to be demonstrated
was a relationship between bladder EMG noninvasively performed with Ag–AgCl
(silver) electrodes and a conventional urodynamic investigation according to
International Continence Society standards which had to be carried out simulta-
neously (at the same time, in the same individual). The results suggested that
‘‘slow voltage changes found during bladder contraction might be summed
membrane potential changes of bladder muscle cells (Fig. 15.3), but this concept
needs further testing [11].’’
The individual positive results had to be worked out in a series of volunteers to
show that the method is valid and can be applied for clinical use. The results of this
extended study are disappointing. Although in a few cases a relationship between
bladder EMG and urodynamic pressure changes is present, the overall results are
negative. In most cases, the surface signals detected by electromyography were
absent or too weak to be correlated with bladder pressure changes. Moreover, till
2013, this problem has not yet been solved [11].

15.4 Single Smooth Muscle Cell Studies in the Pig Bladder

Scientists consider that the pig is comparable to humans in its morphology and in
the functioning of its organs. To use pig bladder to study single smooth muscles
cells, therefore, seemed to be a reliable choice. Previous studies used strips of
bladder tissue and measured the spontaneous contractility of these strips [17, 18].

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15.4 Single Smooth Muscle Cell Studies in the Pig Bladder 367

Fig. 15.3 Micturition phase of female volunteer with full bladder. The upper two tracings show
the urodynamic pressure signals, intravesical and abdominal pressure, respectively and the lowest
the flow. The middle three traces show the bipolar electrode signals (RI-MB, MI-MB, RB-LB,
respectively) obtained from the abdominal skin. All signals are synchronized in time. At mark A,
the volunteer has a prevoiding contraction, not yet resulting in a flow. At mark B, both the
intravesical pressure and the recorded electrical activity rise, introducing the voiding contraction.
When the flow begins at mark C, the slow voltage wave has not yet reached its maximum value.
The electrical activity than declines to baseline values before the intravesical pressure signal does
or the flow has stopped (courtesy M. Kinder)

The construction of these strips in terms of smooth muscle cell organization and of
the type of interaction between these cells is unclear. Therefore, one could not
estimate the contractility properties of a single smooth muscle cell. So experiments
had to be carried out on single smooth muscle cells.
The first step was to obtain such isolated cells [9, 19]. Pig bladders were minced
with scissors, treated with enzymes, sucked through narrow openings of glass
pipettes, and sieved. One has to realize that enzymatic treatment will change the
constituents of the outer surface, and mincing and sieving will damage the cells.
Single cells had to be bathed in a solution in which artificial electrical stimu-
lation could be performed. Under these conditions, two different reactions
occurred after stimulation:
1. Upon electric stimulation a contraction occurred, this being followed, after the
stimulation was switched off, by an even more stronger contraction (called
after-contraction).
2. Upon electric stimulation a contraction occurred, while after the stimulus was
ended, a relaxation occurred (after-relaxation) [20].
To grasp the consequences of these findings, we have to take a side step. The
human bladder fills itself at 1 ml/min up to 350–500 ml after which expulsion

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368 15 Smooth Muscle Electromyography of Bladder

follows. The bladder itself enlarges during the filling phase. It is considered that
the wall is passively stretched by the increase in volume. So to accommodate the
increasing volume, the smooth muscle cells (and other components of the bladder
wall) must relax.
However if one studies a rabbit bladder by EMG in the filling phase, smooth
muscle cell contractions can be seen to occur randomly over the bladder, at
constant time intervals. So at least there is some evidence that the rabbit bladder is
not passive during the filling phase [11, 14, 21].
What if the smooth muscle cells in the bladder possessed the ability to relax
following contraction, which (see above) is a property of isolated cells [21]. In this
scenario, the bladder itself contributes actively to the enlargement of its surface. This
could explain the ongoing mechanical activity randomly over the bladder [17, 18].
Neuronal activity could therefore switch the smooth muscle cell from a stage of
after-relaxation in the filling phase to after-contraction during voiding. Overcon-
traction, which is present after the bladder is emptied, could reset the smooth
muscle cells back into an after-relaxation phase.

15.5 Centers of Bladder EMG Activity

‘‘The truth’’ concerning bladder electrical activity is impossible in the present state
of research. Consequently, models are used to predict electrical behavior in the
bladder. Several types of models have been used, and one should not be surprised
that different models predict different outcomes. A cellular automaton model of the
bladder has been proposed, which describes the contraction of the bladder dome
and the bladder neck, and assumes that dome and bladder are at rest (and thus
produce no smooth muscle cell contraction with after-relaxations as hypothesized
above [22]). This model is based on a layer of artificial smooth muscle cells that
are able to transmit their activity to their immediate neighbors. The cells are
arranged in a grid of 104 9 104 cells. The upper 80 rows represent the detrusor,
while the lower rows imitate the bladder neck. Cells can be inhibited or exited by
certain parts of the autonomic and somatic nervous system. By varying the con-
centration of nervous input points, or synapses, to the smooth muscle, and by
mapping these inputs for different parts, a semirealistic model can be made. The
upper part of the bladder, the detrusor, gets less excitatory parasympathetic and
more inhibitory sympathetic input. The bladder neck, or smooth muscle sphincter,
gets mainly sympathetic excitatory information. That sympathetic innervation can
be excitatory or inhibitory, as determined by different receptors, which transmit
different information to the smooth muscle cell. Moreover, the model does not
allow activity of bladder dome or bladder neck to transfer to each other [22].
Resulting overall activity turns out to be well organized. If activity starts in the
bladder neck, the activity in the detrusor dies out, and vice versa. Both bladder
neck and detrusor start their activity at random placed, small groups of smooth
muscle cells. This activity spreads over the bladder in a circular wave, with the

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15.5 Centers of Bladder EMG Activity 369

starting points as their centers, due to the capacity of the smooth muscle cells to
transmit their activity to their neighbors (Fig. 15.4).
The model shows that contraction does not have to start at the top of the dome
and does not have to go downwards to the bladder neck in a simple way. The same
holds for the bladder neck, where points of activity are generated, that then travels
as circular waves over the neck. Such travelling waves of smooth cell electrical
activity have been observed in the bladder EMG of rabbits.
The most striking result, however, is that smooth cells have not to remain
constantly contracted. Various smooth cells wander through a successive series of
contraction and rest situations. One could suppose that the smooth muscle cell has
the possibility to shorten in steps, or to adjust to an equilibrium necessary at that
moment. This gives the smooth muscle cell the possibility to react on tensile
strength caused by bladder filling, changes in body posture or to adapt to the
velocity of voiding.
In other words, bladder voiding is not a phenomenon which is initiated at a
single moment, and it does not involve a standardized pattern of contractions of
the smooth muscle cells.
It is not uncommon that electromyographic results cannot be related to function
or malfunction. This is known for striated musculature too.
So the first question is: Must electrical activity of the bladder be well correlated
with pressure changes in the bladder liquids? Since there is a rather forceful elastic
power in the filled bladder, one can argue that only a small electrical phenomenon
is needed to start the elastic force.
The second question concerns the frequency of the signals. Different species
were used in the experiments: 0.5–10 Hz signals were detected in rabbits, the over
3 Hz signals in rats. Are the different frequencies species differences?

15.6 Again Fluorescent Spheres

However, a novel technique has been developed, in which fluorescent polystyrene


spheres are attached to the bladder surface. Mechanical bladder activity will
change the position of the spheres. Using two cameras, the relative displacement of
the spheres can be studied in three dimensions. Since the increase in thickness of
the bladder wall in the isovolumetric bladder is minimal, a two-dimensional pic-
ture of the behavior of these spheres can be calculated [21] (see Sect. 12.3).
This optical tracing method has already been applied to quantify local defor-
mations of heart tissue, skin and striated muscles. It constitutes a reliable method.
Contraction and relaxation was seen to occur simultaneously and separately
across the bladder wall during spontaneous activity of the isovolumetric bladder
(Fig. 15.5). So in one strain direction, contraction could be noted, while in the
other strain direction of the same detrusor surface, relaxation was found. However,
after electrical stimulation of the nerve S2, contraction and subsequent relaxation
was induced. In contrast to spontaneous activity, one clear driving center was

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370 15 Smooth Muscle Electromyography of Bladder

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15.6 Again Fluorescent Spheres 371

b Fig. 15.4 Illustration of cellular automaton model of the bladder muscle (courtesy J. L. van
Leeuwen). The top three panels show the distribution of the neuronal terminals. The bottom nine
panels demonstrate the activity of detrusor (upper part of each panel) and of the bladder neck
(lower part of each panel) taken from a computer animation. Fully dark rims represent maximal
activity, and light dots depicts minimal activity. Frame 1: initial completely relaxed state. From
15 travelling activity waves over bladder neck. The (start of) the detrusor activity with relaxation
over the bladder neck can be noted in frames 30–100. This activity travels wave-like over the
bladder dome. The ending of voiding and restart of bladder neck activity is shown in panels 130
and 195

present, which lasted throughout the entire contraction phase. A confined area of
relaxation was present at the upper part of the dome and the contraction started at
the bladder neck during the stimulation of the isovolumetric bladder. The centers
are surrounded by a circular area of contraction or relaxation. The center contains
the highest value for contraction or for relaxation, diminishing toward the
boundary of the circular area (Fig. 15.5). So, no circular rim of activity, as pre-
dicted by the automaton model, was noted, but a steady decrease or increase over
the whole area was observed.

15.7 Uterine Electrical Activity

The uterus contains exclusively smooth muscle, forming the myometrium. The
myometrium is covered with serosa at its outside, and at its inside, it contains
the epithelial endometrium responsible for the reception of the fertilized egg. The
myometrium can be divided into three layers of smooth muscle. The cells of the
outer layer are oriented both circularly and longitudinally. The middle layer
contains diagonally oriented fibers, while those of the inner layer are purely cir-
cularly arranged. Contractions of the uterus can be circular or vertical. In preterm
labor, uterine contractions occur. These contractions can be mistaken for labor
contractions. In that case, the doctor will hospitalize the patient and will try to
overcome preterm delivery. The idea is that circular contractions are preventing
labor (ineffective contractions), while vertical contractions are the onset of a
possible delivery (effective contractions). If the obstetrician could distinguish the
two types of contractions, he would know for sure which patient had required
hospital care [23].
Contractions of the uterus can be measured using tocography. A mechanical
sensor measures the stiffness of the abdomen. The other diagnostic possibility is to
use intrauterine pressure measurements. Both methods, however, fail to distinguish
effective from ineffective contractions. So, there is still a need for a noninvasive
method to detect these two types of contractions.
Uterine contractions are present from the start of pregnancy. These contractions
are characterized by low amplitude and low frequency (every minute) in the first
30 weeks. They are called Alvarez waves. From the twentieth week onwards, a

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372 15 Smooth Muscle Electromyography of Bladder

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15.7 Uterine Electrical Activity 373

b Fig. 15.5 Two principal strains during electrical stimulation after prolonged stimulation of
sacral root 2. The right column shows a vector plot of the two principal strains. The left and
middle columns show a color plot for one principle strain each. Each horizontal row of three
panels represents the same moment in time. The top of each panel is oriented toward the bladder
dome, while the bottom is located a few millimeters above the bladder neck. The panels coincide
with increasing intravesical pressure and urethral pressure (rows 1 till 4) and decreasing, but still
above normal, intravesical pressure (row 5), but urethral pressure is already returned to normal.
Compare this figure to Fig. 5.4 the automaton model. The automaton model predicts waves over
the bladder, like present after dropping a stone in water. The real measurements show a whirl-
pool-like reaction. Moreover, in the same area, contraction (yellow–red) or relaxation (blue–
green) can be present together. Reproduced with permission of M. Kinder

second type of contraction is found: The Braxton Hicks contraction, possessing


higher amplitudes but an even lower frequency (once every 2 or 3 h). These
Braxton Hicks contractions become more frequent, and their strength increases
[23]. At the end of pregnancy, they transform into parturition contractions, which
will lead to dilatation of the cervix and delivery of the child. The early dilatation
contractions arrive every 30 min and have a duration of 30 s. Later, they occur
every 2–3 mins and last for 40–60 s. Hypoxia of the uterine muscles is held
responsible for the pain during labor. The severe contractions of the uterine
muscles disturb the passage of blood, leading to diminished oxygen content of the
muscle fibers [24].
Each myometrial cell is capable of emitting action potentials, and each cell can
relay its electric signal to its neighbors (called electric coupling) [25, 26]. So
spreading and propagation over the uterus of the electric signal occurs always from
wherever it originates in the myometrium. The electrical activity of the various
muscles differs: each has its own characteristics. In the myometrium, two types of
action potentials can be distinguished: a long plateau potential (slow wave) and a
spike-like potential (fast wave). The spike-like electrical changes are superim-
posed on the long plateau ones (Fig. 15.6). The representation of these signals is
called an electrohysterogram (EHG) [25, 26].
Detection by superficial abdominal electrodes of the electric activity of the
uterus shows yet another signal. Since the distance to the uterus is relatively large,
nearly 5 cm, the field seen by such electrodes contains several hundreds of muscle
fibers. The electrode gives a summation of a series of action potentials, propa-
gating over the region of the uterus registered by the overlying electrode. By
placing several electrodes in a calculated pattern, the whole frontal side of the
uterus can be electrically observed [23].
The signals from women have been recorded with the pain indicated by the
patient. For each record, it is then apparent whether the electrical activity coincides
with pain; electrical activity is thus related to contraction of the uterus. Moreover,
if the electrical activity propagates over the uterus, the same electrical activity is
registered by another nearby electrode [23].

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374 15 Smooth Muscle Electromyography of Bladder

Fig. 15.6 a The electrohysterogram (reproduced with permission from Devedeux et al. [24]).
Superimposed on the slow wave a fast wave is present. Together they show the total
electrohysterogram. b Using surface electrodes placed on the abdominal skin, the electrical
activity of the uterus is measured. The band-pass filter eliminates slow waves. These fast-wave
electrical signals are demonstrated for three channels (M2, M3, and LL3) of one patient. The
dashed vertical lines represent start and end of one contraction as indicated orally by the patient.
The solid vertical lines represent: A. contraction, B. movement artifact, C. resting phase (courtesy
Schaaf [23])

Analysis of the signals gathered from ten patients was the next step. Using
several types of analyses, the noise stayed too high to filter out those electrical
activities that could characterize the electrical components of the effective con-
tractions. It was calculated that at least 30 patients were needed to obtain the
significant measurements of the characteristics of the desired electrical compo-
nents [23]. So, as in the EMG of the bladder, electrical activity of uterine smooth
muscle can be measured, but assessment of what events relate to the electrical
activity is difficult.

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Literature 375

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16. Kinder MV, Gommer ED, Janknegt RA, Waalwijk Van, van Doorn ESC (1998) Recording
the detrusor electromyogram is still a difficult and controversial enterprise. Neurourol Urodyn
17:571–573
17. Van der Hoeven AAM, Van Duyl WA, De Bakker JV (1990) Detection of spontaneous
motion patterns in urinary bladder tissue in vitro. In: Van Kerrebroeck PhEV, Debruyne FMJ,
Van Duyl WA, Marani E (eds) Dysfunction of the lower urinary tract, pp 10–13
18. Van Duyl WA, Van der Hoeven AAM, De Bakker JV (1990) Synchronization of spontaneous
contraction activity in smooth muscle of urinary bladder. Neurourol Urodyn 9:547–550
19. Glerum JJ, Van Mastrigt R, Van Koeveringe AJ (1990) Mechanical properties of mammalian
single smooth muscle cells III: passive properties of pig detrusor and human a terme uterus
cells. J Muscle Res Cell Mot 11:453–462
20. Glerum JL (1991) Mechanical properties of mammalian single smooth muscle cells. Thesis
Rotterdam ISBN 90-9004485-X
21. Kinder MV, Bos R, Willems PJB, Drost MR, Holtzer CAJ, Janknegt R, Marani E (1999)
Three dimensional registration of mechanical bladder activity using polystyrene fluorescent
spheres: a technical note. Arch Physiol Biochem 107:236–241
22. Kinder MV, Van Leeuwen JL (1996) Recording and simulation of the electrical activity of
the bladder muscle. In: Marani E, Lycklama à Nijeholt AAB, Van Gool JD (eds)
Urodynamica en urine-incontinentie, Boerhaave postgraduate course, pp 135–149
23. Schaaf A (1997) Recording and analysis of electrical uterine activity during effective
contractions. Masters thesis Electrical Engineering, University Twente, Enschede
24. Devedeux D, Marque C, Mansour S, Germain G, Duchene J (1993) Uterine
electromyography: a critical review. Am J Obstet Gynaec 169:1636–1653
25. Chamberlain G, Dewhurst J, Harvey D (1991) Illustrated textbook of obstretics. Gower
Medical Publishing Co, London
26. Nakao K, Inoue Y, Okabe K, Kawarabayashi T, Kitamura K (1997) Oxytocin enhances
action potentials in pregnant human myometrium: a study with microelectrodes. Am J Obstet
Gynaecol 177:222–228

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Chapter 16
Reflexes or Controller Action?

The pelvic organs function by their reflex actions. These loops of signals pass over
existing connections, but their hierarchy is only partly known. Surprisingly, en
route unknown neuronal stations, called microganglia, are frequently present.
Nevertheless, the whole pelvic system contains a general controller mechanism to
overcome contradictory actions by separate parts. The pelvic autonomic ganglia
are treated in this chapter together with cross-sensitization: the neuronal influence
of pelvic separate parts on each other. The endothelium lining the urine system is
capable of informing and inducing actions within the local nervous system.

16.1 Introduction

The concept of the reflex dates from Descartes (1664), who described in his
‘‘Treatise of Man’’ the reflex as an involuntary motor response, reactive to a
peculiar and specific stimulus, which involves a ‘‘simple’’ spinal pathway. Note
that we distinguish somatic and autonomic reflexes, whose bases can be different.
Somatic reflexes concern striated muscles. Autonomic reflexes involve smooth
muscles and glands (Fig. 16.1). In both, a signal is detected, which is transferred to
the spinal cord or brain stem, and evokes a motor response: muscles contract or
glands start to secrete. Within the central nervous system, there may be no
interneuron involved or there may be one or more. A reflex is not restricted to a
certain level of the spinal cord or brain stem. The cornea reflex, for instance, is
registered by a branch of the trigeminal brain stem nerve after touching the cornea.
The signal is then transferred to the brain stem and relayed to another brain stem
level containing the facial brain stem nucleus and nerve, which closes both eyelids.
So, a reflex is not a simple or singular reaction, but nevertheless it is involuntary.
Before discussing general aspects of the autonomic system, in order to
understand the function of the uropoetic system, one specific reflex will be con-
sidered. This is the guarding reflex [1]. Here, a preliminary remark is needed: most
systems (e.g., heart and intestine) maintain the function of their reflexes, even if
higher control systems malfunction. However, several uropoetic reflexes do not, so
some scepticism concerning their true nature as real reflexes is justified.

E. Marani and W. F.R.M. Koch, The Pelvis, 377


DOI: 10.1007/978-3-642-40006-3_16,  Springer-Verlag Berlin Heidelberg 2014

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378 16 Reflexes or Controller Action?

Fig. 16.1 General scheme of


the sympathic (S) and
parasympathic (P) system
together with
neurotransmitters and
anatomical nomenclature
 E. Marani

Now, consider the following quotation, ‘‘The guarding reflex refers to a pro-
gressive, involuntary increase in the activity of the external urethral sphincter
during bladder filling’’ [1]. Thus, as the bladder fills, the activity of this sphincter
increases, in order to close the urethra against increasing pressure and to overcome
leakage.
There is, however, a problem with the definition: At low bladder volume the
reflex is involuntary, but at high bladder volumes it becomes conscious and vol-
untary [1]. You will have noticed this already yourself, when waiting for the bus,
with no toilet in your neighborhood. All day, you never noticed the filling of your
bladder, but you do now, when no toilet is near by!
Normal people may say ‘‘By definition reflexes are involuntary, the voluntary
part cannot belong to the reflex.’’ We are in fact dealing with two phenomena here.
The first is a reflex, which after substantial filling of the bladder is succeeded by
another process to maintain, continence after increase in pressure, and to make you
aware of it. Therefore, this last act cannot belong to the reflex. Otherwise, one
should extend the reflex definition to a voluntary act, but this is not (as far as I
know ‘‘never’’) explicitly done [1]. By the way, the number of reflexes involving
the pelvis are still increasing (see the Shafik-story later on).
For definition’s sake: a reflex is involuntary.

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16.2 Noise 379

16.2 Noise

Do you dislike formulas too, and do you only reluctantly remember the lessons in
physics and mathematics at school? Lessons you never really understood, and in
which you only learned tricks to solve the exercises? Probably, you have totally
forgotten why you used these tricks and what they meant. The only thing you
learned was noise: Noise related to definitions and understanding of physics and
mathematics. The nice thing was that you could forget these tricks after high
school, which created space in your brain for more social important facts.
Noise is everywhere. Especially in scientific experiments, one measures and
gets extra information, which you do not want to obtain. Noise is an unstructured
disturbance. It is, however, not so lacking in structure that you cannot put it in a
formula.
A reflex involves several structural units. The anal or urethral sphincter reflex
includes the following:
• The circular striated muscle fibers (and also smooth muscle fibers, but they will
not be discussed here);
• A neuron gathering sensory information from the sphincter;
• A neuron activating the muscle fiber(s); and
• Usually an interneuron, which accepts the sensory information and relays it to
the motorneuron.
The last two neurons are located in the central part of the nervous system, in
this case the spinal cord.
The electrical information, or action potentials, of the motorneuron will be
transmitted to the striated muscle fibers, which in turn will develop electrical
activity that leads to contraction. There is, however, a time delay between the two
electrical phenomena; an action potential lasts 1 ms or so, while the electrical
activity of striated muscles persists for more than 10–20 ms. This means that the
muscle, although fast reacting from the view of conscious awareness, is slow
reacting with respect to the incoming stimuli: For our perception, reacts late on the
stimulation of its own units. In fact, several action potentials can reach the muscle
fiber during the onset of contraction, leading to an enforcement of muscle fiber
contraction. Consequently, the decrease of muscle activity is also slow, compared
to the velocity of the action potential.
The information relayed to the muscle fibers is not noise free. Noise in this case
is non-information of electrical origin, which interacts with the series, or trains, of
action potentials directed toward the muscle. How disturbing is noise for the
(reflex) function of striated sphincter-like muscles?
Our neuroregulation group addressed the problem by modeling the motor
neuron group in the spinal cord (which is called Onuf’s nucleus) and the sphincter
muscles. The properties required were taken from the literature. Onuf’s nucleus
can be activated or inhibited by higher centers in the brain. The neurons were
modeled by a differential equation, which said whether a neuron could fire or not,

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380 16 Reflexes or Controller Action?

Fig. 16.2 Spinal cord


activity, Onuf’s nucleus
motoneurons activity with
noise (the sails) and the
striated sphincter activity
(thick base line), courtesy
M. Heldoorn

and also how capable of firing it was and whether this firing was fast or not. Ten of
these mathematical neurons were coupled, whereas in reality, Onuf’s nucleus
contains hundreds of neurons. We were thus assuming that the formula adequately
described the activity of these neurons and that a model describing them was
accurate. This is possibly not true!
The formula used, expressed in words, says ‘‘The velocity of the change of the
frequency of the neuron in time equals the input, minus the fire frequency of the
neuron.’’ A time constant is also introduced.
Onuf’s nucleus activates the sphincter muscles (only containing a hundred
striated muscle fibers in this model). Contraction or relaxation is detected by
stretch receptors present in the sphincter muscle and reported back to the spinal
cord interneurons by sensory neurons. Onuf’s function is represented by a formula,
which needs not to be described here. The series of action potentials produced by
the motoneurons of Onuf’s nucleus was changed by a simple noise generator,
which altered (by adding and substracting) electrical activity.
The model worked out well, so one could add noise to the electrical activity of
the motoneurons. Typical results are represented in Fig. 16.2. Here, we start with
increasing the activity of the spinal cord. It increases slowly to one (maximal
activity) in a time period of 0–0.05 s (upper curve). The motoneurons of Onuf’s
nucleus increase their firing activity, but with noise, because our noise generator is
active (the ‘‘sails’’ on the second curve from the top).
The muscle fibers of the striated sphincter react with increasing contraction (the
lower thick line). Now, we abruptly stop the activation of the spinal cord, over a
time period of 0.05–0.07 s, and Onuf’s motoneurons minimalize their firing fre-
quency. Still, there is noise. The muscle fibers respond diminishing their con-
traction, but only slowly. Suddenly, we again generate maximal activity in the
spinal cord, and slow it down linearly to zero over the time period 0.08–0.1 s. The
motoneurons follow with a high output, still containing noise. The muscle
response follows slowly, and finally, the muscle fibers tend to reduce contraction.

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16.2 Noise 381

However, the noise we put on the electrical activity of the motoneurons has no
consequence for the activity of the striated muscle fibers: the ‘‘sails’’ are not
repeated in the curve of the muscle fibers.
In other words, noise has to be very substantial indeed before it affects guidance
of the muscle fibers by disturbing the electrical input of Onuf’s motoneurons to the
muscle fibers. In reflexes, you can forget noise, and this part of the chapter too!

16.3 The Reflex

A reflex is an open (cornea reflex) or closed (knee tendon reflex) loop. It starts at
the effector side (muscle or gland) or skin receptors. Something is noticed in the
autonomic and somatic system and transferred by the sensory neuron (by the way,
this part of the loop is never shown as being in the autonomic part of the nervous
system) to the central nervous system. Here, it will be relayed directly or indirectly
to a motor neuron, which causes responses in, e.g., muscle or gland. So, in this
example, it activates involuntary muscles or glands. The somatic system uses a
direct connection from the motoneuron to the effector. The autonomic system uses
a two-step system (Fig. 16.1). The autonomous motorneuron in the central nervous
system transfers its message to a second neuron. Note that a variety of interactions
can still occur to this second autonomic neuron at the periphery of the body. At the
periphery, these neurons are situated outside the central nervous system and can
still interact before the message reaches the effector, since this second step neuron
can receive all kinds of neuronal input.
A reflex always minimally concerns a sensory or sensible neuron and a motor
neuron (or two in the autonomic system). At the periphery, the second autonomic
motor neuron is the only one that can be influenced.
The autonomic system is divided into two parts with antagonistic actions,
namely the parasympathic and the sympathic systems. This antagonistic behavior
is not organized by the nervous system, but by the molecular receptors present in
the target organs, which have to detect the motosignals of the autonomic system.
Each neurotransmitter posseses its own types of receptors. Different parts of an
organ can have different receptors for the same neurotransmitter as is the case for
the sympathic system of the bladder where the dome has alpha-receptors, and the
neck contains beta-receptors for noticing noradrenergic sympathic innervation.
The a-receptor inhibits contraction of the dome, while b-receptors in the bladder
neck induce contraction on the same neurotransmitter action of the symphatic
system. The parasympathic system of the bladder uses mainly the muscarine
receptor. However, it is more complex than this as there are additional neuro-
transmitters involved (Table 16.1).
Studies in the uropoetic system indicate that several neurotransmitters are used
by the autonomic nervous system. As a consequence, various types of receptors are
present.

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382 16 Reflexes or Controller Action?

Table 16.1 Occurrence of neurotransmitters in the bladder and ganglia and their receptors in
man and animalsa
Neurotransmitter Receptor References
1. Noradrenalin a, b adrenoreceptor [1, 7, 12, 88]
2. Acetylcholine Muscarinic [12, 21, 30, 36, 37, 88]
3. ATP Purinoreceptor P1, P2 2, 3, 5, 7, 23, 25, 27, 88]
4. Galanin ? [4, 47, 48]
5. Serotonin 5HT receptors [6, 28, 88]
6. VIP ? [8, 20, 41]
7. Subst P/Subst K Tachykinin? [9, 15, 16, 18, 24, 26, 27, 29, 31, 32, 40, 44]
8. Nairokinin NK-2, NK-1 [10, 11, 17–19, 44]
9. Bradykinin Bradykinin receptor [13, 22, 46]
10. Bombesin ? [14, 42, 43]
11. Angiotensin II Angiotensin II receptor [33]
12. NO (nitric oxide) ? [34, 35, 38]
13. GABA GABA-a receptor [39, 45]
14. CGRP ? [88]
15. Cannabis CB1, CB2, TRPV1 [88]
16. Prostagladins ? [88]
17. Glycine ? [88]
a: This cannot be a full list. Each year, new neurotransmitters and new receptors are discovered,
but also older ones denied. Moreover, emphasis changes day by day due to new research tech-
niques applied

We certainly do not know their function at the moment, indeed for some neu-
rotransmitters, the receptors are unknown (Table 16.1). So, nowadays, science is
looking at the top of the receptors iceberg.

16.4 Short Neuron Reflex System

The second motor neuron in the parasympathic system is localized in or directly on


the surface of the target organ, that is, it possesses an intra- or juxtamural position.
The second motor neuron in the sympathic chain is localized at the side of the
vertebral column, or in front of it, that is, it possesses a paravertebral or a pre-
vertebral position (Fig. 16.1).
A short neuron system has been proposed by Elbadawi [67] in which bladder
steering could be performed partially at the periphery. Steering loops are present
between parasympathic juxta- or intramural ganglia and sympathic pre- or para-
vertebral ganglia. These steering loops can be small, say at the organ level, or
longer, if distant ganglia are involved (Fig. 16.3). The matter is disputed, although
sympathic axon terminals are found on the parasympathic ganglia and vice versa.
It is also unknown whether this short neuron system actually has a steering rather
than a stabilization or modulating function. However, one thing is clear, if present

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16.4 Short Neuron Reflex System 383

Fig. 16.3 The short neuron system of the uropoetic system. PNS peripheral nervous system, CNS
central nervous system (courtesy M. Kinder)

in humans, the system is involuntary, and the system should be called a short
neuron reflex system.
The uncertainty concerning the short neuron reflex system is absent in dogs. ‘‘In
canines, coordination of reflexes can be provided by neuronal interplay either on a
spinal or subspinal level. Examples of spinal coordination, unknown in humans,
are the peculiar pattern of voiding in jets and the stepping movements of the hind
limbs in spinalized animals. The short neuron system intrinsic to bladder, trigonal
and urethral structures in several mammalian species provides for subspinal
interaction between sympathetic, parasympathetic and somatic efferents. In man,
such a system is known only in the alimentary tract’’ [66].

16.5 Reflex or Controller Mechanisms in the Pelvis

Recently, Shafik published a large series of articles concerning the pelvic reflexes.
Several new reflexes were described. These may be summarized as follows:
• Ano-urethral reflex: Stimulation of the external anal sphincter increases the
external urethral sphincter basal activity [58].
• Recto-urethral reflex: Rectal distention evokes external urethral sphincter con-
traction [57].
• Vagino-cavernosus reflex: Vaginal distention causes contraction of the caver-
nose muscles [56].
• Ano-vesical reflex: Distention of the anal sphincter results in an increase in
vesical pressure [55].

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384 16 Reflexes or Controller Action?

• Utero-cervical reflex: Slow uterine dilatation is followed by cervical contrac-


tion; fast uterine dilatation is followed by cervical dilatation [49].
• Genito-vesical reflex: Clitoral and cervical stimulation induces drop of vesical
pressure, but an increase in the external urethral sphincter activity [54].
• Clitoro-motor reflex: Stimulation of the clitoris produces increased activity of
the pelvic floor muscles [53].
• Vesico-cavernosus reflex: Rapid changes in vesical pressure are quickly fol-
lowed by cavernose muscle contraction in humans [52].
• Peno-motor reflex: Stimulation of the glans penis produces a fall in vesical
pressure and an increased activity of the puborectalis and levator ani pelvic floor
muscles [51]
• Vagino-levator reflex: Distension of the vagina results in the contraction of the
levator ani [50].
• Levator-urethral reflex: Contraction of the levator ani muscles evokes the
contraction of the external urethral sphincter [59].
• Vesico-levator reflex: Distention of the bladder produces the contraction of the
levator ani muscles [60].
Several other reflexes have been described or studied by Shafik e.g., a vagino-
uterine reflex, a deflation reflex, and an olfactory micturition reflex in dogs.
Let us try to relate these reflexes to some simple actions. Distention of rectum,
vagina, and bladder will be followed by contraction of all striated pelvic floor

Fig. 16.4 The structures that are guided by the controller and by the short neuron reflex system
 E. Marani

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16.5 Reflex or Controller Mechanisms in the Pelvis 385

structures including the striated sphincters. Activation of the pelvic floor or


sphincters causes contraction of the same structures. Activation of clitoris, penis,
and cervix has the same effects. In general, any change, or activation, of the state
of structures involved in the entrances to the pelvic organs will elicit pelvic floor
and sphincter contraction (Fig. 16.4).
The question arises, Do we in fact have a variety of reflexes, or is there
somewhere in the spinal cord and/or brain a central controller, that will act on any
evoked change in the situation of the pelvic floor substituents? There are some
indications that speak in favor of an organization of these reflex situations of the
pelvic floor. Vaginism is characterized by a painful muscular spasm of the vaginal
walls plus spasm of the pelvic floor and sphincters, resulting in painful coitus. The
description of vaginism coincides with the published reflexes listed above. How-
ever, a reflex needs real sensory input, which can be relayed to the spinal cord
motoneurons, but in vaginism, even the thought of the possibility of coitus may
evoke the spasm, that is, without the sensory input needed to start a reflex loop.
This situation can only be caused by a central controller, which can be influenced
by the emotions relayed by higher brain centers to the controller.
The other reflexes described are between organs: cervix and uterus, cervix and
bladder, and anus and bladder. These are seemingly real spinal reflexes, which
could also be organized by the short neuron reflex systems and need not to be
relayed via the spinal cord.

16.6 Flow Charts and Continence

In 1995, our group published an article [61] comparing the functional and ana-
tomical connections involved in bladder filling, bladder emptying, and the ending
of voiding. The results of the four most celeberated scientific groups in this
research field were summarized. Although ignored by these research groups, this
article showed that ‘‘cabling’’ of the process of continence is a vexatious issue
(Fig. 16.5).
An engineering procedure was adopted to align the different cabling schemes
these research groups used; the production of flow charts shows the connections
between the body structures involved in continence and their simultaneous activity
during various functions. Such flow charts have to be read from top to bottom
(Fig. 16.5). One starts at the top with muscle and the sensory organization; one
then passes through the peripheral system, including autonomic ganglia, to reach
the spinal cord. Now, one enters the control system of the higher brain stem and
brain centers, whose output again reaches spinal cord motor structures. The motor
structures of the spinal cord relay (via ganglia) to the muscles in the periphery. A
bar is placed next to the figures, in which the colors indicate peripheral, spinal
cord, or supraspinal involvement, and the bar length indicates the value the dif-
ferent research groups place upon these levels in their research.

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386 16 Reflexes or Controller Action?

Fig. 16.5 Flow charts depicting the neuronal connections involved in the uropoetic system as
described by the main four research groups in this field. Reproduced with permission from
M. Kinder et al. [61]

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16.6 Flow Charts and Continence 387

Bladder filling can be analyzed by these flow charts into reflex action (short
neuron and spinal cord sensibility and motor action) and controller functions
(supraspinal action, see the bars next to the figure Fig. 16.5). Comparison of the
various schemes shows that, both for reflex action and for controller action, no
agreement exists between the four research groups. In part, this disagreement
originates from the discussion concerning the muscles involved, but by even
neglecting this problem, the statement still holds for the neuronal functions and
connections described.
Bladder emptying does not change the picture at all. The controller actions are
even more different from each other, which also can be noted for the reflexes
needed for bladder emptying. There is discussion concerning the presence of a
supraspinal or controller action.
However, the biggest problem arises with the description of voiding and
switchover to bladder filling. In this case only two out of four research groups
discussed the completion of bladder emptying, while none of the groups consid-
ered the switchover from stopping voiding to restoration of the bladder-filling
process.
This flow chart approach emphasizes that several controversial facts still have
to be clarified:
1. ‘‘Proposals regarding reflex arcs and supraspinal connections involved in
micturition and continence are different and indeed are sometimes contradic-
tory, between one group and the other.
2. The significance of the sympathetic nervous system during bladder filling in
humans is still a matter of debate.
3. Little is know about how autonomic information from the lower urinary tract is
relayed to supraspinal structures.
4. Information about supraspinal (inter)connections and their function in mictu-
rition control is still fragmentary, e.g., concerning the existence of a direct
corticospinal tract to the nucleus of Onuf.
5. Control mechanisms active in terminating voiding are not totally clear.
6. The role of the pelvic floor musculature during the micturition cycle remains
vague but is probably underestimated.
7. There is a marked discrepancy between neuroanatomical knowledge and the
functional descriptions of the micturition cycle’’ [61].
Why do these discrepancies originate in the scientific research? It is beyond
doubt that the trouble is caused by the peripheral connections from organ to spinal
cord, and vice versa [62]. We do not have the instruments to study them, and
moreover, they are confusingly intricate.
From these studies [61, 62], at least three subdivisions of the nervous system
involved in micturition can be discerned:
1. A short neuron reflex system, present around or near the organ; examples
include the intra- and juxtamural ganglia, the plexus pelvicus, the plexus
hypogastricus, and the sympathic chain of ganglia.

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388 16 Reflexes or Controller Action?

2. A spinal system or long neuron reflex system, to which belongs the sympathic
and parasympathic sensoric and motoric centers including Onuf’s nucleus.
3. A supraspinal controller system, containing a urocontrol center or centers in the
brain stem, which can be influenced by the cortex.
To connect these various centers, different routes are involved [62], which
makes their unraveling difficult. Nevertheless, let us try to ascribe functions to
these three subdivisions. First, note that bladder has to routinely adapt itself to
different positions during movement (e.g., during walking upstairs) and also to the
mechanics of the bowels. The bladder seeks the less energetic position forced by
the changes toward gravidity. It would be easiest if this could be organized by the
bladder itself. The best candidate for such a system is the short neuron reflex
system, not involving spinal cord and supraspinal structures.
Continence (= storage) and the process of voiding could be regulated by the
autonomic spinal cord centers, while the voluntary act of starting and ending
voiding could be attributed to supraspinal cortical structures [65, 66, 67].
In some way, the supraspinal structures have to influence and organize the
spinal reflexes of the autonomic and somatic spinal centers, acting as a mediator
between the short neuron system and the spinal cord on one side and on the other
side the voluntary input of the cortex: We have here a reflex controller which can
cortically be influenced.
Although the arguments are somewhat indirect, the presence of an urocon-
troller in the brain stem which regulates urogenital diaphragm, pelvic floor, their
openings with their sphincters, and distal parts of the organs is strongly favored. A
short neuron reflex system adapts the organs to movements and gravity distur-
bances and regulates their interrelations as to absolute and relative (see Fig. 16.3)
positions.
Good candidates for the site of this urocontroller brain stem center are the
mesencephalic pontine gray, especially the nucleus tegmentalis laterodorsalis with
the nucleus of Barrington [63, 64] (M-region) and the nearby localized (L-region:
see also Sect. 14.9.1.)

16.7 The Pelvic Autonomic Ganglia

16.7.1 Introduction

‘‘At the macroscopic level there are dramatic species differences in the structure of
pelvic ganglia’’ [68]. Most research on pelvic autonomic ganglia is done in
rodents, but only few papers appeared on the human pelvic autonomic ganglia. The
question arises whether rodent results can be transferred to the human situation.
The answer is ‘‘only partially’’, but we do not know the restrictions. The questions
that arose from rodent studies are several [68]:

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16.7 The Pelvic Autonomic Ganglia 389

1. Is the organization of the human pelvic autonomic ganglia really different from
other mammals, or is what shows divers in other species concentrated in
humans?
2. Is topography present in the large pelvic autonomic ganglia as present in
rodents?
3. Along the pelvic autonomic pathways, small ganglia, so-called microganglia,
are present. Do we know their function?
4. The higher on the mammalian evolutionary ladder, the more dendrites are
present on the neurons of the pelvic autonomic ganglia. Are all these pelvic
ganglionic neurons in man multipolar?
5. Are sensory neurons present in pelvic autonomic ganglia or are these ganglia
pure motoric?
6. Are interneurons present in these ganglia and are the small Intensely fluorescent
cells (SIF cells) these interneurons?
7. Are the juxtamural ganglia (e.g., for the bladder) both sympathetic and/or
parasympathetic? They should be parasympathetic according to the general
subdivision of the autonomic nervous system.
8. How far extends the sexual dimorphism of the human pelvic autonomic gan-
glia? Does it concern only those for the reproductive organs or also other
ganglia?

The list can be extended toward questions concerning neurotransmitters,


receptors, especially estrogen and testosterone ones, androgen effects, changing
innervation during pregnancy, growth factors, and so on [68].
There are typical reflex systems that pass over the autonomic pelvic ganglia
e.g., the erectile reflex. Are they equally based in man, since erection is a rather
conservative property in mammalian species? Even the main neuroanatomical
peripheral connections are again scrutinized.
The connections studied in this part are the sensible/sensory connections with
special reference to the dorsal root ganglia and the mutual interconnections of
pelvic ganglia of the sympathetic prevertebral and paravertebral ones and with
those of the parasympathetic intramural and juxtamural ganglia. However, first
attention is paid to microganglia, because they could disturb the generally accepted
pattern (see Fig. 14.1).

16.7.2 Microganglia

For establishing the ground plan of the pelvic autonomic ganglia, one should know
whether main groups of autonomic ganglia can be discerned. A spread together
with large individual variability of microganglia over the connecting fibers
between spinal cord, main ganglia, and organ will disturb the generally accepted
map. Already in 1931, Streckfuss [69] showed for the sympathetic connections in
the thorax, called the thoracic splanchnic nerves, that they are full of small clumps

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390 16 Reflexes or Controller Action?

of neurons along their trajectory. It therefore should not come as a surprise that an
analogous situation could be present in the pelvis. ‘‘Ganglion cell clusters were
seen in or along nerve components such as the pelvic splanchnic, cavernous, and
hypogastric nerves, and the pelvic plexus, as well as near or along pelvic visceral
surfaces’’ in men [70]. Moreover, such groups of neurons contained both para-
sympathetic and sympathetic neurons [71]. Thus microganglia are present along
pelvic autonomic nerve bundles and are of mixed origin. The variability of these
microganglia is large, and the total amount of neurons can vary between 650 and
6,500 per male hemipelvis, which is on average 6,000 neurons per male pelvis.
The rather large dispersion per individual is also present for the microganglia of
the thoracic splanchnic nerves: from 6,300 to 33,000 neurons. In the thorax, it
concerns higher amounts of neurons that are involved in constituting the various
microganglia. Nevertheless, they hardly reach the total neuron content of one
human dorsal root ganglion (DRG) (50,000 see [72]) or a human abdominal
paravertebral ganglion in which estimates range from 22,000 to 60,000 neurons in
humans [81]. In rat, a pelvic ganglion contains already 14,500 neurons in male and
6,000 in female [81], which increases being higher on the mammalian ladder.
However, for the pelvic ganglia, ‘‘Accurate and specific pre and postganglionic
parasympathetic estimates are not available’’ [81]. Although accurate counts are
missing for the parasympathetic system, it still seems reasonable to consider the
human microganglia a ‘‘minor’’ deviation of the whole system
Nevertheless, it is inevitable in hysterectomies and prostate operations that
microganglia are removed, in fact disturbing the undersized relay stations of both
the sympathetic and parasympathetic parts of the autonomic peripheral nervous
system [70].

16.7.3 The Dorsal Root Ganglia and Autonomic Sensory


Information

Most sensory information from the pelvic viscera is thought to be relayed by


normal DRG cells: ‘‘Autonomic pathways generally are defined as being motor in
function. However, terms such as ‘‘sympathetic afferents’’ are used sometimes to
refer to sensory neurons with cell bodies in the dorsal root or cranial ganglia that
innervate visceral targets such as the heart or gastrointestinal tract. However,
almost any sensory input can generate a response that contains autonomic com-
ponents while few if any cranial or spinal afferent pathways are associated
exclusively with autonomic responses’’ [75]. Nevertheless, sensory neurons for
short circuitries are present especially in the digestive tract, the so-called intrinsic
primary afferent neurons or IPAN’s.
If there are no specialized DRG neurons for the autonomic system, their
principles also hold for autonomic sensory information, reason to look first into
DRG properties.

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16.7 The Pelvic Autonomic Ganglia 391

Fig. 16.6 Three types of organization of the dorsal root ganglion: a is with bipolar neurons,
b with exclusively pseudounipolar neurons, and c with pseudounipolar neurons with a convoluted
stem of the process. For further description, see text (with permission and courtesy Dr. S. Matsuda
et al. [74])

A DRG is a collection of primary sensory neurons. The central and peripheral


processes of these cell bodies form the sensory connection between the nervous
system and the periphery [72]. Within the mature dorsal root ganglia, all diameters
of neurons between 10 and over 100 mu are present but unorganized. In the C8
ganglion in man 40,000 to 50,000 neurons were counted. Light and dark neurons
(called A cells (large) and B cells (small), respectively) are discerned using dif-
ferent classical stainings, showing a comparable unorganized pattern [72]. The
structure of the DRG is badly understood. The phylogenetic studies [74] compared
the dorsal root ganglion with bipolar neurons (left panel, Fig. 16.6a), a DRG with
exclusively pseudounipolar cells (middle panel, Fig. 16.6b), and a DRG consti-
tuted from pseudounipolar cells with a convoluted stem of the process (right panel,
Fig. 16.6c). Only in the middle panel, the ‘‘processes of pseudounipolar neurons
can pass straight in the center of the ganglia. In this manner, pseudounipolarization
saves space, limits the process length and reduces conduction time’’ [7]. The
problem is that in mammalian DRGs, a series of neurons with a convoluted stem of
the process is present, the so-called initial glomerulus of Cajal (Fig. 16.6c).
Therefore, a relation between DRG structure and the presence of pseudounipolar
cells is difficult to establish [5]. In general, morphology and content of DRGs are
not well understood.
At the more functional side, we cite Devor [71]: ‘‘The dorsal root ganglion is an
odder beast than most of us realize’’ [71]. Unexplained peculiarities are described
by him concerning DRG’s:

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392 16 Reflexes or Controller Action?

1. The location of the ganglion.


2. The unique pseudounipolar form of its neurons.
3. The invasion of action potentials, traveling over the T axon, also reach the cell
body, although they go directly into the central nervous system.
4. Although isolated from their neighbors, still they can be activated by their
neighbors by subthreshold excitation.
5. ‘‘Why is the cell adapted for spike initiation’’, which normally only happens at
the sensory ending.
6. Why is the blood–brain barrier absent in the DRG? [71]

Answering these questions is difficult and sometimes hypothetical, nevertheless a few of


them can be treated and show the ‘‘odder beast’’ characteristics of the DRG:
1. Devor [72] states that the DRG resides midway between peripheral innervated tissue
and the spinal cord. Evolutionarily, the dorsal root ganglion cells are Rohon–Beard
ganglion cells in fishes, still in a modified form present in amphibian larvae. These cells
all are localized within the spinal cord, containing two dendrites, one for the skin and
one for the muscles. Their axon ascends, as DRG processes do. Seemingly, residing
midway is not a prerequisite to fulfill DRG functions, also because DRG neurons for
mastication are present within the brain stem.
2. The pseudounipolar form of the DRG neuron causes 0.2 % of its cytoplasm to be is
present in the perikaryon, while 99.8 % is refound in the axon [71], due to the length of
both axon legs toward periphery and central nervous system. Moreover, the transducer,
to produce action potentials from peripheral input, is the axonal terminal membrane in
the periphery. ‘‘Therefore, the mechano-, thermo-, and chemo-sensing molecules
responsible for generating the sensory signal must be synthesized in the DRG cell soma
and transported down to the axon end by axoplasmic flow’’ [71].
3. The generated action potentials in the periphery run directly into the spinal cord. Why
does this afferent spike still have to excite the soma? Devor has proposed several
solutions: it protects from conduction block at the T-junction and/or a coupling
between spike activity and cell metabolism is necessary.
4. Within the DRG virtual, no synapses are present and DRG neurons are enwrapped by
satellite cells. So, DRG neurons contain no structural apparatus to contact each other. It
therefore is even more astonishing that DRGs can cross-depolarize and can cross-
excite. Spike traffic over neurons can induce depolarization or excitation of neigh-
boring DRG neurons. ‘‘The ability of the soma to support spike discharge is essential
for this mutual crosstalk to occur’’ [71].
5. A special set of DRG neurons are capable of rhythmic firing. These neurons are
‘‘intrinsically resonant and display subthreshold sinusoidal oscillations of their resting
membrane potential’’ [73].
6. The blood–brain barrier is absent around DRG neurons. Therefore, chemical changes in
the blood content can be noted by the DRG neuron; a chemosensory function seems
present (1–6 is partially taken from [71, 72]).

To resume the answers, the place of these sensory neurons is not fixed, and due
to the enormous distance to bridge, compared to the soma size of the dorsal root
ganglion cells, logistic problems appear for the transport of structural entities over
the axons. Heavy spike activity over dorsal root ganglion axons consumes energy
and transmitters and therefore asks for the correct metabolic support. Using the
classical way of inducing activity in other neurons by synaptic transmission, dorsal

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16.7 The Pelvic Autonomic Ganglia 393

root ganglion neurons can excite or inhibit each other by additional methods. Some
of these neurons are capable of rhythmic firing, and due to the absence of the blood–
brain barrier, these neurons know what is happening with the bodily homeostasis.
There is one point that is hardly treated (but see [71]): the consequences of the
DRG localization along the bodily segments. In fact, the somatotopic represen-
tation in the central nervous system originates in the segmental distribution of the
DRG ganglia with the consequence that spinal segmental reflexes exist. In relation
to this, the repetitive firing of the DRG neurons (no. 5 of Devor) is kept responsible
for generating background sensation of the awareness of the body scheme [5].
Awareness of the position of your toe being lower than your hip is organized by
the positions of the DRG for the big toe (L5) being lower than the DRG of the hip
(L1) along the vertebral column. These positions can be known by our brain due to
the organized transfer of information from these DRGs toward brain stem and
brain. Such a consciousness is far less present for viscera.
Above, we learned that most sensory information from the pelvic viscera is
thought to be relayed by normal dorsal root ganglion cells with the typical DRG
properties, and no special visceral afferents are present.
Nevertheless, a different opinion was already stated by Pick in 1970: ‘‘The
altercation on the subject of visceral sensation is due partly to the erroneous idea
that a sensory innervation of inner organs and blood vessels can be considered only
if they respond to the same stimuli as do the receptors in the skin, namely to touch,
pressure, heat, cold and pain. Since this is apparently not the case under normal
conditions, it is understandable that clinicians have denied the presence of visceral
afferent nerves’’ [76]. Already in 1931, it was proven that distending hollow
visceral organs will induce pain: ‘‘distention rather than cutting, pinching or
burning is the adequate stimulus for exciting true visceral afferents’’ [76]. Most
viscera are insensitive to cutting and pinching and ‘‘the painless performance of a
colostomy with a red-hot cauterizer in fully conscious patients pointed to a lack of
visceral sensation, but left unexplained the intense pain so often experienced in
abdominal or other viscera’’ [76]. After a collection of twenty articles in favor of
visceral afferents, published between 1890 till 1936, Pick concluded: ‘‘To sum up,
there is little doubt that true visceral and vascular afferent fibers exist, but their
precise anatomical distribution and physiological significance are by no means
fully understood’’ [76].
The terminology ‘‘visceral afferents’’ is frequently used in recent literature, and
due to tracing techniques, in which a colorable substance is transported from the
ganglia into the organ or vice versa, the distribution of afferents into the visceral
organs can now be demonstrated. It can be carried out by injection of the ganglia
of cranial nerves and spinal dorsal root ganglia [77]. Thus, visceral afferents do
exist cranially and spinally. They can be directed to the organ but also to the
ganglia [77]. However, can we discern bundles of these visceral afferents, in other
words, do they constitute autonomic afferent nerves, which caused the original
denial of its existence. Such is not the case, because they hide in spinal nerves or
use sympathetic and parasympathetic motor bundles [76]. Moreover, a clear
labeling by grouping of their somas in the dorsal root ganglia is difficult, also due

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394 16 Reflexes or Controller Action?

Fig. 16.7 ‘‘(Upper row) Foci associated with the processing of anal (red) and rectal (blue)
sensations. Areas of significant increase in BOLD signal (95 % confidence for activation greater
than the background noise) are shown superimposed on a surface rendering of the MNI single-
subject template. (Lower row) Detail views on these renderings. The location of the detail images
is denoted by the black and white boxes in the upper row of images’’ [78]. The red numbers
(effects of anal stimulation) in the figure point to 1 left parietal 2 mesencephalon 3 left anterior
insula, while the blue numbers(effects of rectal stimulation) point to 1 left precentral operculum 2
mesencephalon 3 left thalamus 4 right pallidum 5 left anterior insula (Reproduced with
permission from Eickhoff et al. [78])

to the unorganized structure of the DRG. Let us say that a diffuse meshwork of
visceral afferents is present, which also means that the basic ground plan is made
by the motoric autonomic and somatic entities together with the ganglia. Within
the DRG pseudounipolar, neurons are present that connected solely to the viscera.
Structures that are near to each other partially use the same pathways: the somatic
anal sphincter innervation and autonomic rectum innervation coincide in their
pathway into the spinal cord. Nevertheless, the relayed information stays separated
as shown after distension of the somatic anus and distension of the autonomic rectum.
Brain projections are near to each other but clearly separated (see Fig. 16.7). ‘‘These
results demonstrate for the first time a functionally and anatomically distinct pro-
cessing of somatosensory and visceral afferents in the human brain in spite of their
partial convergence at the level of the spinal cord’’ [78].

16.7.4 Visceral Organ Cross-Sensitization

‘‘Around 600 BC, Sushruta, an Indian surgeon, described the Hritshoola, which
literally means heart pain. However, it was not until the late nineteenth century

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16.7 The Pelvic Autonomic Ganglia 395

that potential mechanisms underlying this well known symptom—referred pain—


were advanced as reflecting a ‘‘commotion’’ or ‘‘irritable focus’’ in spinal seg-
ments receiving input from an organ. These concepts were later expanded and
formulated as the ‘‘convergence–projection’’ theory of referred visceral sensation,
convergence denoting input from both somatic and visceral structures onto the
same second order spinal neuron. Whereas viscero-somatic referral and sensiti-
zation has been well documented clinically and widely investigated, viscero-vis-
ceral referral and sensitization (termed cross-organ sensitization) has only recently
received attention as important to visceral disease states’’ [79]. The best known
examples of referred pain are heart failure and pain in the skin of the left arm/
shoulder or lung and diaphragm failure in the skin of the left side of the neck.
Here, we focus on viscero-visceral interactions and not on viscero-cutaneous ones.
It is clinically well established that organs within the pelvis can influence each
other (for references see [79]). ‘‘The organs that appear most often involved in
pelvic-lower abdominal cross-sensitization, both in humans and animals, seem to
be the colon/rectum, the urinary bladder/pelvic urethra, the uterus and the pros-
tate’’ [79]. Of these organs, the bladder is the most vulnerable to diseases of other
pelvic organs, but inflammation of the bladder hardly induces problems in other
pelvic organs. The consequence of visceral organ cross-sensitization is that pain in
another organ occurs while the disease is not in the pain inducing organ: ‘‘For
example, patients with irritable bowel syndrome often exhibit signs of urinary
bladder hypersensitivity: nocturia, frequency and urgency of micturition, incom-
plete bladder emptying, back pain and, in women, dyspareunia’’ [79]. The opposite
accounts for obstipation often seen in children and elderly that coincides with
urinary retention. Is this perhaps based on the same mechanism: rectum distention
causing bladder relaxation and/or sphincter contraction? Most of the research is
done in rodents and cats. The relations found are colon and bladder, colon and
pelvic urethra, colon and uterus, bladder and colon, bladder and uterus, bladder
and heart, uterus and colon, uterus and bladder, uterus and pelvic urethra, and
uterus and vagina, thus between nearly all organs in the pelvis (see [79] for
references). Three explanations for visceral organ cross-sensitization are given in
Fig. 16.8. One of the mechanisms is the mutual cross-depolarization and cross-
excitation of the DRG neurons (4 in Devor’s list above, example 3 in Fig. 16.8).
Moreover, if one DRG neuron contacts several pelvic organs, their logistic
problems are even bigger (2 in Devor’s list above, but also 3, due to the increase in
spike activity, example 1 in Fig. 16.8). The order of effects that relate to visceral
organ cross-sensitization is as follows:
• ‘‘Organ insult/inflammation
• Peripheral excitation/sensitization
• Central sensitization’’ [79].

Thus, cross-sensitization is not only an effect of the central nervous system, but
also of the peripheral structures particularly the DRG neurons, in our case those
that are related to the pelvic organs.

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396 16 Reflexes or Controller Action?

Fig. 16.8 Three explanations of visceral organ cross-sensitization: 1, one and the same DRG cell
receives information from more than one organ, 2, different DRG cells project onto the same
spinal neuron or the same interneuron, 3 different DRG cells influence each other within the
ganglion (see part 3.0) or influence each other’s axon or chemically (circles, a) or electrically
(action potential, b). Colon DRG cells in green and bladder DRG cells in red. The figures are
reproduced with permission from Brumovsky and Gebhart [79]

16.7.5 Short Neuron System in the Repeat

In Fig. 16.3, the short neuron system has been pictured and reciprocal connections
between organ and ganglia are indicated, and one of these is denoted by a question
mark. They encompass the short visceral afferents of the ganglia. Within the local
ganglia of the digestive tract, the so-called enteric plexuses, the short visceral
afferents are present [75]. They are supposed to be present in the pelvic ganglia
too, although proof is missing [75, 80].
For the discussion of the short afferent neuron system, it is necessary to get rid
of a not-established principle. The sympathetic and parasympathetic system each
are divided into pre- and postganglionic levels. The relation between these levels
has been studied. For the parasympathetic system a low ratio and for the sym-
pathetic system a high ratio were supposed between these levels, and different
outflows for the systems were presumed. Moreover, this was the basis for the idea

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16.7 The Pelvic Autonomic Ganglia 397

of ‘‘contrasting functional capacities’’ [81] of these systems: in student handbooks,


expressed as ‘‘fight or flight’’ for the sympathetic system and ‘‘resting and
digesting’’ for the parasympathetic system. These capacities ‘‘have been widely
accepted for nearly three-quarters of a century’’ [81]. Remarkably, the original
ratio differences were based on one ganglion of each system. A large review of all
publications for different parts of the autonomic system showed that ‘‘the ranges of
the ratio indexes for the two divisions of the autonomic nervous system are largely
overlapping’’ [81]. Moreover, these ratios also differ between species, individuals,
gender but also developmental stages, and between the organs they innervate,
which is an interganglionic variation [81]. The same doubt holds for branching of
neurons, the presence of interneurons and non-preganglionic axons. Thus, on
forehand, no general structure for any of the autonomic ganglia can be postulated,
as was already noticed for the DRG, which means ‘‘back to the original
publications’’.
Thus, the question is can we ascertain the existence of the afferent leg of
reflexes between the organ and local plexuses (intra- and juxtamural ones; para-
sympathetic), between organ and vertebral plexuses (pre and paravertebral ones;
sympathetic) and between plexuses. For sure, spinal reflexes use the DRG con-
nection as their afferent leg (see above). Most studies are carried out on the enteric
plexus of the guinea pig, and for the digestive tract, all sorts of afferent legs are
indeed present [75, 82].
Injections of retrograde transported tracers into a digestive tract ganglion
(inferior mesenteric ganglion) show that the pelvic ganglia do project to these
ganglia. Thus, afferent connections between ganglia are present [83]. Resection of
the bladder shows that degenerated fibers are present in the superior and inferior
mesenteric ganglion, and aorticorenal ganglia supporting that or organ afferents or
ganglionic afferents toward ganglia localized at a higher localization are demon-
strated [84]. Removing the bladder without the intramural ganglia is impossible;
therefore, the type of afferents involved are difficult to estimate.
Infection with herpes simplex virus type two in the vagina of mice showed that
the ganglia located near the cervix contained this virus. Since the herpes virus is
retrogradely transported and parasympathetic ganglia of bladder and rectum are
found positive for the virus, pelvic interganglionic connections are proven.
Moreover, disturbed function of bladder and rectum after herpes simplex infection
are well known in mice. Since the same specific disrupted functions are familiar
with in man after herpes simplex infections, an analogous spread of the virus to
autonomic ganglia in humans is suggested [85].
Sympathetic projections to pelvic ganglia are well established in experimental
animals [85].
Although publications on humans are restricted, the animal experimental data
are in favor of connections between the pelvic autonomic ganglia. The corollary is
that visceral organ cross-sensitization can also occur by these interconnections
between pelvic and abdominal ganglia. If we extend Fig. 16.3 by splitting the
pelvic ganglia and indicating in red the interconnections of the pelvic ganglia
described above, Fig. 16.9 arises.

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398 16 Reflexes or Controller Action?

PELVIC
ORGANS

Fig. 16.9 Some of the autonomic peripheral connections toward the spinal cord, with permission
and changed after Kinder et al. [86]. Connections in red are the interganglionic ones described in
the text

The more studies appear on the pelvic ganglia, the more connections are
detected. Nevertheless, pelvic afferents to autonomic ganglia and ganglionic
interconnections are weakly based.

16.7.6 Local Tissue Interactions: Urothelium Signaling

The cells lining the lumen of the urethra, called urothelium, is the multi-cell layer
of epithelium that covers the inside of the uropoetic system and will react on
change in urine pH, inflammation, mechanic stress, and temperature changes. The
sensory neurotransmitters released from these cells can activate the sensory nerves
in the wall, the smooth muscle and/or the striated muscle (Fig. 16.10). Beside the
activation of nerves to inform ganglia and the spinal cord, there exists in the
urethral wall an intrinsic system that seemingly is capable of reacting immediately
to urethral threats. So, sphincter activity can be modulated by its urothelium.
For storage of fluid that has to be expelled from the body, it is necessary to
overcome any leakage from the bladder into the surrounding body compartments.

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16.7 The Pelvic Autonomic Ganglia 399

Fig. 16.10 Sensory functions of the urothelium expressed by the release of sensory neurotrans-
mitters from the urothelium due to mechanical stretch, but also by inflammation or other
disorders. This release of neurotransmitters interacts with various receptors on sensory nerve
endings located in the suburothelium and detrusor muscle fibers. Their effects on muscle cells and
nerves can cause contraction, pain, or stimulation of reflexes (reproduction with permission from
Birder et al. [87]); Ach acetylcholine, ATP adenosinetriphosphate, NO nitric oxide, PG
prostaglandin, DP force exerted

The demands for performing such a task are high. The urothelium fulfills these
demands: permeability is extremely low (for water, 5.15 ± 0.43 9 10-5 cm/s; for
urea, 4.51 ± 0.67 9 10-6 cm/s; for ammonia, 5.14 ± 0.62 9 10-4 cm/s; and for
protons, 2.98 ± 1.87 9 10-3 cm/s [87A]), and its passive transepithelial resis-
tance is between 10,000 and 75,000 X. One should note that the blood–brain
barrier reaches only 1,000 to 2,000 X. The urine surface of the epithelium is
covered by membrane plaques that contain uroplakins, which are glycoproteins
that are kept responsible for the epithelial impermeability. The types of uroplakins
differ in the various parts of the uropoetic system. Leakage between the epithelial
cells is overcome by tight junctions between these epithelial cells. These tight
junctions produce a resistance of over 300,000 X, forcing any passage from urine
constituents through the epithelial cells that actively can control such a passage to
modulate the urine composition. The proteins occluding and claudins surround the
tight junctions, but claudins encircle also the lateral side of the epithelial cells.
Both are transmembrane proteins and ‘‘how the claudins regulate the passage of
ions and molecules across the barrier, and how they response to various signals
from the inside and outside of the cells are still unknown’’ [87B]. This intricate
function of the urine barrier must withstand extreme folding of the apical mem-
brane during voiding and stretching during filling, which asks for specific lipids in
the apical membranes of the epithelial cells.

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400 16 Reflexes or Controller Action?

stretch
Urothelial cells

ATP
NOS
2 M
ACh
NO+ NO+ ATP

A, NA P2

Interstitial cell

Blood vessel Nerve terminal

Smooth muscle cell

Fig. 16.11 The complex relations of the urothelial cells with nerve terminals, smooth muscle
cells, and interstitial cells  E. Marani

However, the urothelium is not simply a passive barrier; it can modulate the composition
of the urine and it functions as an integral part of sensory web in which it receives,
amplifies, and transmits information about its external milieu to the underlying nervous
and muscular systems [87B].

The urothelium thus has a sensory function (see Fig. 16.10). The free nerve
endings of pain afferent nerves contain several receptors, which can be activated
by neurotransmitters that has been released by the urothelium (also nitric oxide
that penetrates the nerve endings without receptor).
The receptors involved are as follows: purinergic-, vanilloid-, prostanoid-, and
neurokinin ones. Only one of these receptors is discussed, others are represented in
Fig. 16.10. Vanilloid receptors normally react at a temperature above 43 C and a
pH lower than 6. However, pH change can alter temperature sensibility of these
receptors to body temperatures. The pH change occurs at inflammation. Vanilloid
receptors are present on the nerves that relay pain information from urethra to the
spinal cord (Ad and C fibers). ‘‘These nociceptive neurons cause initially excita-
tion then desensitization, and finally neurotoxicity’’ [87]. Vanilloids also reduce
NGF, and after prolonged reduction in NGF, neuronal death is the consequence.
Several pathways and receptors are involved in the contraction and relaxation of the
human female urethra. Adrenergic system (a- and b-adrenergic receptors), cholinergic
system (muscarinic receptors), nonadrenergic–noncholinergic pathways and mediators
such as NO, ATP, neuropeptides, prostanoids, serotonin and Rho-kinase are believed to
play important roles in the physiology of the urethral function. Insufficient urethral closure

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16.7 The Pelvic Autonomic Ganglia 401

and function might lead to stress urinary incontinence formation in women. Although the
adrenergic system seems to be playing a major role in urethral contraction, management of
stress urinary incontinence by a-adrenergic receptor agonist administration has not been
successful. Likewise, NO seems to be the major urethral relaxant, but the role of other
transmitters in urethral contraction and relaxation needs further research [87].

Thus, a simple epithelium lining the uropoetic system had to adapt its prop-
erties, all to control, store, and expel urine. Moreover, it has to influence afferent
nerves, smooth muscle cells, and interstitial cells (Fig. 16.11). Note that puri-
nergic (ATP) and nitric oxide (NO) neurotransmitter systems are also used for
influencing other structures.

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Chapter 17
The Connective Tissue in the Pelvis

The connective tissue in the pelvis appears as blades, ligaments, fascias, and
membranes. Enwrapping pelvic organs and bounding them tightly is among others
the function of the pelvic connective tissue. Its structures are pillar-like to embrace
blood vessels, leave-like for suspending the rectum, and striated for suspension of
the anus. Descensus of the pelvic diaphragm is mainly caused by connective tissue
weakness leading prolapse.

17.1 Introduction

Around all mature structures and organs present in or outside the pelvis a fat body,
called the corpus pelvinus are found. The part inside the pelvis is named the corpus
intrapelvinum (see Chap. 7). This fat body is surrounded by its own membrane.
Fat is an odd thing. Fat cells are storage cells that, if needed, can deliver extra
energy to the body. A century ago, people still fattened themselves up in summer
and autumn to store energy for use in the winter. An annual rhythm existed for
one’s fat metabolism.
These fat storage cells are mainly intermingled with loose connective tissue in
the subcutis. Particular sites are used for fat storage, e.g., the belly of men. The
gender difference in these sites of fat storage can easily be recognized in weight
watching publicity. But there is more. Fat storage is an important factor in growth.
Before each growth spurt during development, fat is accumulated. The baby does
this before its growth spurt at 2 years. In addition, the start of the menarche, the
first ovulation, is thought to be fat dependent. A minimum amount of fat has to be
stored before puberty can start. This is dramatically demonstrated by female ballet
dancers. Due to the excessive training, fat storage is minimal, and the menarche
may be postponed up to 21 or 23 years of age.
Several organs are wrapped in fat, e.g., the kidneys. This is called structural fat.
In anorexia nervosa, the patients lower their weight so excessively that even this
structural fat, laid down between the kidney fascias, decreases. As a consequence,
the kidney is no longer held in place, this being described as a floating kidney

E. Marani and W. F.R.M. Koch, The Pelvis, 407


DOI: 10.1007/978-3-642-40006-3_17,  Springer-Verlag Berlin Heidelberg 2014

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408 17 The Connective Tissue in the Pelvis

(=nephroptosis). Pelvic fat is also structural. Around 80 years of age, the metab-
olism of fat changes again. Fat storage is diminished, as is the structural fat in the
pelvis which is considered to prevent prolapse of the uterus or rectum.
Rats provide the most spectacular fat storage deficiency disease known. Ve-Tsin,
which is in fact sodium glutamate, in rats selectively destroys an hypothalamic
nucleus, known as the arcuate nucleus. Severe obesity arises in these animals.
(In our Western society, obesity is also a threat, as it induces diabetes.) Ve-Tsin is of
course present in Chinese food. Fortunately, our arcuate nucleus is not destroyed,
but the typical headache, though not the diarrhea, is caused by sodium glutamate.
Nearly every fat storage cell requires an adjacent capillary. That is why losing
weight diminishes the capillary net, and this decrease in the capillary net favors the
heart because it has to supply less tissue. In heart disease, reduction in tissue fat is
one of the ways to reduce the workload on the heart, which can return to a more
normal output after weight loss.
Obesity also has influence on the uropoetic tract. Severe obesity induces (urinary
stress) incontinence in women while slimming partially restores continence.
Women suffering from obesity manifest increased intra-abdominal pressures, which
adversely stress the pelvic floor and may contribute to the development of urinary
incontinence. In addition, obesity may affect the neuromuscular function of the genito-
urinary tract, thereby also contributing to incontinence. Weight loss may relieve urinary
incontinence … [1].

Increased body mass (index) is associated with urinary stress incontinence but
also with urogenital prolapse in Caucasian and Eastern Mediterranean populations.
The relation can be indirect due to obesity-induced neurogenic diseases, which
induce pelvic floor and urethral dysfunctions.
If 50 % or more of the body weight is lost, the decrease in the incidence of
urinary stress incontinence in women due to slimming is nearly 50 % [1].

17.2 The Corpus Pelvinus

Little is known about the interrelation of the structural pelvic fat tissue and pelvic
connective tissue at the histological level: Fatty tissue in the pelvis has been held
responsible for the production of lipomata, benign fat tumors and liposarcomas,
malignant tumors originating from fat and/or related connective tissue.
Isolated connective tissue bands or septa have been noted in the pelvine fat
body and are the source of much debate. They are suspected of a supporting
function, to keep organs in place. These connective tissue bands became of interest
to gynecologists who were seeking explanations for the following [2, 3]:
• ‘‘The passage ways of hematomas in the pelvis occurring postpartum or after
operations or trauma.
• The functional anatomical aspects of the genesis of prolapse or incontinence for
urine.

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17.2 The Corpus Pelvinus 409

• The factors influencing the recidivism of prolapse and incontinence in lege artis
operated patients.
• (…) whether morphological criteria can be postulated to determine the prefer-
able type of episiotomy [2, 3].’’

These are sufficient reasons for studying the pelvic connective tissue strips. A
part of this connective tissue system has already been described in Chap. 5, namely
the paracysticum, paraproctium, and paracolpium. These structures are thought to
possess a suspensive function for bladder neck, rectum, and cervix, respectively.
How these structures relate to the whole of the connective tissue in the corpus
pelvinus is rather intriguing.
The terminology on connective tissue elements in the pelvis is confusing, nearly
each country using its own [4]. Parametrium is used in German and English.
However, the terminology paraproctium, paracolpium, and paracysticum has a
German origin and is not used in English [5, 6]. German anatomical handbooks do
use this terminology [7, 8], but the definition is different in various handbooks (see
Table 17.1).
Here, we use these names (paraproctium, paracolpium, paracysticum) for
connective tissue blades or leaves that can be reinforced by ligaments within it.
So, the pubovesical ligament is considered a reinforcement of the paracysticum
(see Table 17.1) [8].
Anatomists have organized their terminology very clearly. There is a special
committee, that systematizes terminology, the outcome being the Nomina
Anatomica. However, none of the pelvic ligaments are accepted by this committee
except for one fascia (peritoneoperinealis) and one septum (rectovaginale) [4].
So in this respect, the Nomina Anatomica Committee has failed dismally and is
partly responsible for the terminological mess.
In the early fetal situation, the pelvic organs are free of any connection to the
corpus pelvinus [9]. Bladder and the proximal urethra, cervix and uterus, and the
rectum have a free space around them (Chap. 7). The corpus pelvinus extends
during fetal life and starts to make these connections sometime before the sixth

Table 17.1 Comparison of the definitions of paracysticum, paracolpium, parametrium, and


paraproctium. (m = male, f = female)
H. Leonhardt [7] Hafferl [8]
Paracysticum Space at both sides of the Connective tissue leaf to the bladder. In it: lig.
bladder. In it: lig. puboprostaticum (m) = lig. pubovesicale (f)
pubovesicale
Paracolpium Space at both sides of the Connective tissue leaf to the vagina
vagina
Parametrium Space at both sides of the Connective tissue leaf to the uterus.
uterus. In it: lig. cardinale In it: lig. cardinale
Paraproctium Space at both sides of the Connective tissue leaf to the rectum.
rectum. In it: the m. In it: the lig. rectouterina
rectouterina

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410 17 The Connective Tissue in the Pelvis

Fig. 17.1 Reconstruction of the septa in the corpus pelvinus. (Courtesy S. de Blok [3]). a The
connective tissue septa of the female pelvis caudal to the musculus levator ani in the fossa
ischiorectalis in caudal to cranial view. Abbreviations: cox os coxae; fem femur; Fit fossa
ischiorectalis; mgma Musculus gluteus maximus; mla Musculus levator ani; moi Musculus
obturatorius internus; vu Bladder, vesica urinaria; uv Uterus; r Rectum. b The connective tissue
septa at the level of the musculus levator ani. Abbreviations: cfem Caput femoris; fem Femur; fir
Fossa ischiorectalis; mgma Musculus gluteus maximus; mo Membrana obturatoria; moi Musculus
obturatorius internus; sp Symphysis pubis; ti Tuber ischiadicum; fo Foramen obturatorius; tm
Trochanter major;* indications of connective septa; 8 compartment mgma; 9 fascia of mgma

month of prenatal life. We know nearly nothing about how this process is orga-
nized and how this fat body develops between these organs nor about how these
connective strips adhere to them [9].
These connective tissue strips do attach to the pelvic organs and can be studied
[2] after the first sixth months of fetal life. The older literature does not consider
the connective tissue in the pelvis except for the presence of elastic and collagen
fibers. However, by sectioning pelvises of fetuses late in their development, and
using an intricate reconstruction system, the connective tissue strips have been
demonstrated in three dimensions [2, 3] (Figs. 17.1 and 17.2a).
The connective tissue of the female fetal pelvis is organized into a bilateral–
symmetrical system, which is closely similar in all individuals. The strips are
ribbon-like and hence are called septa (Fig. 17.2a), and border vessels, muscles,
bones, or viscera in an organized way. The main septa are organized rostrocaudally
and ventrodorsally, thus nearly parasagittally. Moreover, they contain muscle
cells. From these main septa, various smaller septa direct themselves to the organs
and to the pelvic wall (Figs. 17.2b and 10.3). On the pelvic wall side, the septa
adhere to the fasciae of muscles and to the periosteum of bony structures
(Fig. 17.2b). On the organ side, these smaller septa are aligned perpendicular to
the main ones and connect to the viscera of the organs. A concentration of smaller
septa forms the paraproctium, paracysticum, and paracolpium at the level of the
rectum, bladder neck, and cervix; reinforced perpendicular septa are directed to
the organ’s viscera (Figs. 17.1a, b and 17.2a). The main septa compartmentalize
the corpus (intra) pelvinus. Outside the pelvic floor, the corpus (extra) pelvinus in

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17.2 The Corpus Pelvinus 411

Fig. 17.2 a Reconstruction of the connective septa in the retroperitoneal space of the female,
cranial to the musculus levator ani in a cranial to caudal view. (Courtesy S. de Blok [3]).
Abbreviations (see also Fig. 17.1): atc Adipose compartment; af Arteria femoralis; cp Cavum
peritonei; mip Musculus iliopsoas; mra Musculus rectus abdominus; oc os coccygis; si Spina
ischiadica; ti Tuber ischiadicum; tm Trochanter major; vf Vena femoralis; 1, 2, 3 space for
bladder, uterus and rectum? 4, connective tissue septum that encloses the muscular bony
compartment; 5, continuation of the septa into the ventral abdominal wall muscular fasciae; 10,
adherence of three septa to the muscular bony compartment; *, general indications of connective
tissue septa. b Reconstruction of the isolated bones and connective tissue septa system in a
midsagittaly cut left-half reconstruction (courtesy S. de Blok [3]). Abbreviations: 1, 2, 3 space for
bladder uterus and rectum; cox os coxae; fem Femur; oc os coccygis

the ischiorectal fossa contains an analogous system of connective tissue septa. The
septa in this part of the human body possess a more reticulate arrangement.
These septa support the suspension of the pelvic organs and give the pelvic organs
the possibility of movement. This is inherent to the functioning of bladder and
rectum during filling and emptying and to the uterus during pregnancy. This intrinsic
pelvinar system is easily missed when using sharp sectioning during operations.
Some resistance may be noted, but due to its capacity for mobility and because of its
surrounding fat tissue, the connective septa will easily be cut. This always happens
during those operations (e.g., hysterectomy) involving the corpus pelvinus.
Could it be that prolapse is induced by operations? Could these septa sometimes
be overstretched during pregnancy resulting in prolapse at an older age?
Could decollagenation of these septa be induced, by analogy with decalcifi-
cation of bones due to female estrogen decreases at older ages, resulting in pro-
lapse and/or incontinence?
Could the compartmentalization be held responsible for the localized accu-
mulation of blood, forming clots in the corpus pelvinus? Moreover, could infec-
tions in the lower pelvis be restricted to such compartments, and therefore be hard
to fight? These questions should raise curiosity! Nevertheless, the connective
tissue septa are hardly studied nowadays in urology, gynecology, and anatomy.

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412 17 The Connective Tissue in the Pelvis

17.3 Connective Tissue Reinforcements in Fascias

Each muscle is surrounded by a thin blade or leaf of connective tissue, called the
muscle’s fascia. At various places in the body, these fascias are reinforced. In
particular, this is so for the muscles of the pelvic floor.
Moreover, fascias are not restricted to muscles. The corpus intrapelvinum
possesses its own fascia (the fascia endopelvina), surrounding its fat content. It has
its own reinforcements (Fig. 17.3).
Therefore, a two-layered system of fascias or blades can be discerned at the
bottom of the pelvis, one covering the upper side of the pelvic floor muscles
(the fascia pelvis parietalis) and one bordering the lower side of the pelvic fat body
(the fascia endopelvina). Since they lie over each other, they are difficult to separate.
Each of these two fascias contains its own reinforcements, and scientists have
debated their origins. Are they muscular or intrapelvinar, due to the adhesion of
the connective blades? Here, we will not go into these endless disagreements, but
will describe the most rational approach to date [10]; see also [4, 11]. Charac-
teristic reinforcements are present for each of the blades and, since both have the
typical arch form, they are named arcus. The pelvic floor muscles contain a
consolidation, called the arcus tendineus levator ani, while the other is the arcus
tendineus fascia pelvis, part of the endopelvine fascia.
The arcus tendineous levator ani reinforcements are already present early in
prenatal life and they function as a differentiator between the m. pubococcygeus
and the m. iliococcygeus [10]. Later, these muscles partially adhere to the rein-
forcements generating added tensile strength. Apparently, primitive connective
tissue has the capacity to induce differentiation [10].
The second layer, the intrapelvic caudal fascia, contains its own reinforced
connective tissue structures. They are grouped as the arcus tendineus fascia pelvis,
also known as the ‘‘white line’’ in the fascia [12] of the corpus pelvinus (=endo-
pelvine fascia). This connective reinforcement starts at the innerside of the pubic
bone, near the symphysis, and travels to the ischiadic spine. At this site, it splits.
One branch is directed toward the coccygeal bone and the other branch toward the
sacroiliac joint. Overall, it forms an Y (see Fig. 7.10).
Note that inherently the interpelvine fascia adheres to the same points: the
‘‘white line,’’ which is interpelvine fascia (reinforcement). Its anterior part is
considered an anchor for the ligaments and fibrous blades or strips originating
from the urethra and vagina, or only for the vagina [13]. These ligaments contain
muscle fibers. The whole arcus tendineus fascia pelvis presumably prevents the
proximal urethra and the anterior vaginal wall from descending caudally, ‘‘which
is crucial to maintain continence’’ [11] (see also [13]).
The conclusion drawn is that two connective tissue systems exist at the inner-
side of the pelvic floor to maintain continence; one, the arcus tendineus levator
ani, operates acting via the levator ani’s muscle activity. The other, the arcus
tendineus fascia pelvis, works passively, and upholds the proximal urethra and
vagina by the tensile strength of its white line [13].

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17.3 Connective Tissue Reinforcements in Fascias 413

Fig. 17.3 Gross-anatomical


preparation of the septa
around the bladder (courtesy
S. de Blok)

We are ignorant concerning a possible collaboration; whether the one adds or


takes over functions of the other.
At the end of this section, one last remark is appropriate: both the overall
description of the pelvic septa [2, 3] and the description of the arcus [12] alone
indicate that these connective ligaments contain muscle fibers. Seemingly, this
connective tissue is not as passive as has been thought, and active reaction of this
intricate connective tissue system in the pelvis seems possible.

17.4 Connective Tissue Pillars for Blood Vessels

While the arterial system in the pelvis is the same in different individuals, the
pelvic veins show enormous variation [7]. Nevertheless, three main pathways
returning venous blood from the pelvis can be discerned: one is along the internal
iliac veins, one along the ovarian veins, and one along the rectal veins. In front and
behind the corpus intrapelvinus, two plexi are present. The retropubic venous
plexus gives its blood to the internal iliac veins. The sacral plexus connects to the
same main vein [14]. The pelvic floor, mainly the muscular veins, is drained by
both the internal and external iliac veins [14]. All these veins can adhere to pelvic
wall structures such as periosteum, fascias covering bone, or muscles, respectively.
The veins that have to penetrate the intrapelvic corpus to reach the pelvic organs
are another story. Veins are weaker than arteries; therefore, extra support has to be
provided within the corpus intrapelvinus; and if this support is present, arteries can
use it too [8]. Note that most scientists explain this the other way around.

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414 17 The Connective Tissue in the Pelvis

Fig. 17.4 The pillar concept


of DeLancey [13]. The pillar
concept explains how blood
vessels can reach the pelvic
organs  E. Marani

The paracolpium reinforced by the parametrium above it is generally accepted


in the literature. It is also called Mackenrodt’s ligament or ligament cardinale.
Along this ligament, blood vessels reach the cervix of the vagina and the uterus
[13]. This ligament is also called the frontal connective tissue (matrix).
A perpendicular or a sagitally directed septum or pillar for the bladder is present
on both sides, by which vessels can reach the bladder [13]. Below it two con-
nective tissue pillars will reach the rectum (Fig. 17.4).
This pillar concept does not differ much from the one concerning septa (see
Sect. 17.2). The pillar approach is rather an abstract ideal description of reality that
originated in clinical empiricism.
However this approach strengthens the supportive function of the large septa or
pillars for the blood vessels.

17.5 The Rectosacral Fascia

In both male and female, internal fascias cover the inner wall of the pelvic space.
The corpus intrapelvinum has its own outer fascia which we have called the fascia
endopelvina. It lies on the fascia of the pelvic floor muscles (the fascia parietalis)
and sticks to the periosteum, e.g., of the pubic bone. The boundary fascia of the
intrapelvine body on the visceral side is called the fascia pelvis visceralis. In
between these two fascias (the intrapelvina and visceralis), the fat and connective
tissue septa are found.
These parietal, endopelvine, and visceral fascias must be considered during
total mesorectal excision in rectal cancer surgery [15]. The term mesorectal
excision means that the rectum and its surrounding fat have to be removed, that is
the fat between the rectum and the visceral fascia. However, intrapelvine fat,
namely extra mesorectal fat, is often taken out too. Two surgical methods are used
for total removal of the mesorectum: blunt posterior dissection, or sharp dissection.

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17.5 The Rectosacral Fascia 415

Fig. 17.5 The retrorectal space (courtesy M. de Ruiter and K. Havenga [15]). a Midsagittal
section through the pelvis. Small hook opens the space between rectum and pelvic wall.
b Enlargement of a showing the band of connective septum dividing the retrorectal space and
anchoring the rectum to the sacrum

Both methods work along the same planes: posteriorly along the fascia pelvis
parietalis, and along the visceral septa around the mesorectum. Note that there is
no fat body behind the rectum, but there is a space, and only one fascia endo-
pelvina exists in front of the rectum.
Blunt excision of the mesorectum leads to higher rates of local failure than
sharp dissection, for unknown reasons.
The space between rectum and the pelvis wall has been studied in midsagittal
dissections of the human pelvis. This so-called retrorectal space is enclosed on the
pelvic wall side by the parietal fascia, and at the dorsal-rectum side by the visceral
fascia. The parietal fascia adheres to the periosteum of the sacral bone. From this
strong attachment, a band of connective tissue, or a septum, traverses the retro-
rectal space, dividing it into an upper and a lower space. In front of the fourth
sacral vertebra, this septum, referred to as the rectosacral fascia, obliquely tra-
verses the retrorectal space to connect with the visceral fascia of the rectum. This
rectosacral fascia extends laterally, where it meets a natural connection of the
visceral and the parietal fasciae, forming the lateral borders of the retrorectal space
(Fig. 17.5a). The rectosacral fascia is thought to anchor the rectum to the sacrum.
By this mechanism, prolapse of the rectum can be prevented [15].

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416 17 The Connective Tissue in the Pelvis

The explanation for the difference between blunt and sharp excision is pre-
sumably due to the rectosacral fascia, which in blunt dissections guides the sur-
gical hand over the lower part of the retrorectal space into the mesorectal area.
‘‘In this manner, conventional blunt dissection may lead to inadequate resection of
mesorectal tissue, caudal to the retrosacral fascia. In case of most cancers of the
mid- or distal rectum, the majority of mesorectal lymph node metastases would
be found at approximately this level’’ [15]. Following inadequate resection of the
mesorectum, leaving behind metastasient cells, 85 % of the patients develop local
recurrence. In sharp excisions, the rectosacral fascia will easily be cut, reaching the
caudal retrorectal space.
The concept of the rectosacral fascia also has its opponents. In her paper [16] on
the topographical anatomy of the pelvic connective tissue, Helga Fritsch denies the
existence of a rectosacral fascia. Using the combination of MRI and plastinated
sections (3–13 mm thick) of the male and female pelvis, she and her co-worker got
remarkable results: she could not trace among other structures [16]:
1. The rectosacral fascia,
2. The cardinal ligament (=Mackenrodt’s ligament, see Sect. 17.4).

Negative results opposing positive results are important for arriving at scientific
truths. Let us restrict ourselves to the rectosacral fascia and take a look at
Fig. 17.5a and b. This figure is the result of research done in our laboratory.
Inspection of the preparations by several scientists convinced them that a con-
nection between sacral area and rectum exists.
Could it be that the applied technique of MRI and plastinated sections do not
show this and other ligaments? ‘‘The plastination technique causes minor but
inevitable changes of the topographical relations’’ [16], while the resolution of CT
and MRI in 1995 was still too low to discern all fascias [16]. Nonetheless, it is
striking that the existence of structures generally described ‘‘independently’’ by
several disciplines such as anatomy, gynecology, urology, and proctology are
denied. Have we perhaps blindly repeated each other?
These contradictory results emphasize the fact that a generally accepted picture
of compartmentalisation of the pelvis by connective tissue septa, ligaments and
fascias is still not available.

17.6 The Perirectal Fasciae

Several scientists recognize an extra fascia or septum that totally surrounds the
rectum [17, 18]. Whether this is the visceral or endopelvic fascia or whether around
this there exists an extra septum or fascia, is not clear. Blood vessels and nerves to
the rectum have to penetrate this extra septum to reach the fat (=capsula adiposa
rectalis) that surrounds the rectum, and passing this fat layer they reach the rectum.
If rectal cancer passes this outer septum, the rectal cancer is unoperable [18].

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17.6 The Perirectal Fasciae 417

The posterior side of the corpus intrapelvinum at the retrorectal space remains
an area of discussion [10, 18]. Here, the ureter, ovarian vessels, and large iliac
blood vessel reach, or are near, the corpus intrapelvinum, encircling the rectum.
The ureter has its own connective leaf that originates from the connective
blades surrounding the kidneys structural fat. This ureter leaf descends to the
pelvis and should connect to the Mackenrodt’s ligament or paracolpium. How this
is organized is unclear, as is the relation of the ureter leaf with the parietal
endopelvic fascia.

17.7 Perianal Connective Tissue

In the sitting position, the anus is the pelvic floor’s lowest part. Feces have to pass
it to leave the digestive tract. Fecal continence is guaranteed by the closure of the
anal sphincter. The sphincter muscle is mainly in a contracted state during life and
opening is an extraordinary event for the sphincters [19].
The anal sphincter consists of an inner smooth muscle sphincter plus an outer
striated muscle sphincter. Several operations are described in which the sphincters
were cut, and in most cases, incontinence was the consequence. After parturition,
damage to the anal sphincter can also lead to fecal incontinence. If the damage to
the sphincters is only partial, a connective tissue scar will maintain the sphincter
function. Even if the anal sphincter is cut totally, the end will retract but tone and
contractility will still be present, which is not the case with skeletal muscles.
The ischiorectal fossa borders on both sides of the anus (see Chap. 7) and it
confines connective tissue. Moreover, the longitudinal muscle layer of the rectum
continues into the longitudinal ligamentous layer, interspaced between the smooth
and striated anal sphincters. These connective tissues are collectively called the
perianal connective tissue, and it is the focus of this part of the chapter. The
longitudinal (conjoined) ligament or coat sends its small septa into the smooth
sphincter, and they terminate in the anal mucosa or anal skin. At the other side,
septa intrude into the external striated sphincter and join the connective septa of
the ischiorectal fossa. The smooth and striated fibers of both sphincters adhere to
the connective septa which are between them.
The perianal connective tissue contains many elastic fibers. So we have a fine
web of connective septa that adhere to skin and anal muscosa, connected to the
ischiorectal fossa connective tissue. Interwoven are the sphincter muscle fibers
separated by the longitudinal ligament.
Since the ischiorectal connective tissue is connected to periosteum and fascias
of the pelvic floor muscles, and as it possesses elastic properties, it will tend to
open the anus. Sphincter muscle cells have to overcome the elastic forces of the
connective tissue during closure.
The presence of the elastic web for opening the anus is understandable, since
relaxation of a sphincter muscle need not result in opening. The sphincters cannot

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418 17 The Connective Tissue in the Pelvis

exert opening forces, only closure forces, by their circular arrangement. Of course,
contraction makes the circle smaller [19].
Very substantial forces are exerted on the anal area during fecal passage. One of
the other functions of the connective web is to anchor the anus to the midline
ligaments (see Chap. 7). The longitudinal (conjoined) ligament connects the anal
area to the skin and the fascias of the pelvic floor muscles. This is the central
connective tissue cylinder of the anus from which the outside web deviates into the
ischiorectal fossa. This structure withstands the fecal passage forces.
Anal echography shows the sphincters but not the connective tissue. The lon-
gitudinal (conjoined) ligament is noticed as a dark circle in between the white
sphincters. The web in the ischiorectal fossa cannot be seen at all. Therefore,
confirmation of the functionality and the existence of the web with modern
techniques is hardly possible.
Indirect evidence is provided by scar formation after hemorrhoid operations.
‘‘Scar formation makes the network rigid so that it cannot follow the muscle
movements’’ [16]. Moreover, its elastic function is impaired, resulting in problems
with defecation. The same holds for operations on anal fistulas [19].
To come back to anal echography. Damage to the sphincters is easily recog-
nized with this technique. Damage that cuts the sphincter will nevertheless not
always result in incontinence. The sphincter does not need to retract totally, since
its fibers are interlaced and connected to the septa, maintaining (partial) function.
So sphincter damage will not always results in defecation dysfunction due to the
connective tissue network.
Two functions have been proposed for the perianal connective tissue: opening
of the anus, and anchoring it in such a way that defaecation forces can be
overcome. The intricate web of connective tissue septa corresponds to the earlier
descriptions [2], but the proposed function is more parsimoniously explained for
the perianal connective tissue.

17.8 Descensus of the Pelvic Diaphragm

Stress incontinence is also attributed to bladder neck prolapse [13, 20]. Muscle
dysfunction, especially of the levator ani muscle, is held responsible. Due to the
malfunction of the levator ani muscle, the bladder neck follows the descensus of
the pelvic floor and bladder neck and prolapse is the consequence (see Fig. 17.6).
Please note that this implies that the arcus tendineus fascia pelvis malfunctions too.
However, here we have a chicken-and-egg problem.
‘‘Muscle relies on collagenous ‘glue’ to transmit contraction to organs.
Overstretching of this ‘glue’ results in dissipation of the muscle’s contraction’’
[20]. So, either the muscle fiber does not function, or the adherence of the muscle
fiber to pelvic structures by means of its tendons or ligaments malfunctions.

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17.8 Descensus of the Pelvic Diaphragm 419

Fig. 17.6 Schematic


demonstration of the
consequences of malfunction
of the levator ani muscle.
Prolapse is the result of
descensus of the bladder
neck, as the bladder neck is
no longer supported by the
levator ani muscle. Upper
part of the figure shows
normal situation, and lower
part shows reduction in Reduction
muscle fibers and of of muscle Prolaps
connective tissue fibers
 E. Marani

Reduction of
collagen

While the one explanation proposes malfunction of muscle cells [13], the other
adds dysfunction of the connective tissue [20]. Damage to connective tissue of the
muscle can occur with aging, inducing collagen loss, or by hormonal influence on
tissue. Thus, steroid receptors are present within ligaments and muscle tendons,
indicating that hormonal therapy or hormonal levels caused by pregnancy also act
on connective tissue. During pregnancy, therefore, the hormonal changes not only
influence the organs but also the ligaments in the pelvis [20].
The key question is: Are structural changes in the pelvic musculature, involving
muscle cells and connective tissue, present during stress incontinence? Should this
hold for connective tissue too?
In ten patients with stress incontinence, samples were taken from the pubo-
coccygeus muscle, when this was cut to form a sling around the bladder neck to
restore continence [21]. In these samples, a decrease in the number of muscle
fibers, an increase in number of connective tissue cells in the muscle, and an
increase in the internal connective leaves were found. The collagen typing of the
connective tissue indicated its degeneration, and the striated muscle structure was
replaced by smooth muscle fibers [21].
However, the most surprising finding was the occurence of laterality. On the
right side, degeneration was quantitatively and qualitatively greater [21]. The
higher steering control centers show a right dominance for the urinary tract [22],
while sexual behavior is also known for its dominance [22]. The fact that the
dominant side for urinary tract steering is also mirrored in the degenerative process
of urethral muscles was not expected.

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420 17 The Connective Tissue in the Pelvis

Fig. 17.7 The extension


angle of the little finger
indicates the possibility of
prolapse and incontinence
 E. Marani

17.9 Prolapse

At the beginning of this chapter, the question was posed as to whether prolapse
could be related to dysfunction of the pelvic connective tissue, either by overst-
retching or by decollagenation. A further question, which must now be asked is:
How can one measure the state of connective tissue, especially in the pelvis?
An unexpected method was found in the literature: measuring the joint mobility of
the fingers (Fig. 17.7). Using a ‘‘fifth finger goniometer,’’ the angle a patient can
make with their fifth finger in overextension and with the hand flat on the table was
studied. The results showed that women with a rectal prolapse possessed a
significantly greater fifth finger angle than a control group without any sign of
prolapse [23].
Genital prolapse was studied too, and the same fifth finger angle phenomenon
was found, this statistically being significant [24, 25]. Although the etiology of
prolapse is very complex, and all kinds of factors can be involved joint movability
still can indicate prolapse. The explanation must be in the connective tissue.
‘‘Generalised connective tissue laxity may contribute to the development of rectal
prolapse in a number of ways’’ [23]. Laxity of pelvic floor connective tissue and of
pelvic or bladder ligaments are held responsible. Since the defect is generalized,
one should indeed find it in other ‘‘connective tissue’’ structures in the body.
In one paper [26], joint mobility was related to incontinence in women (with an
Ehlers-Danlos syndrome), but not to pelvic floor prolapse.
So, prolapse can be indirectly assessed from measurements of joint movements,
as these reflect laxity of the connective tissue in the body as a whole, resulting in
the pelvis in prolapse. Since finger and wrist joints contain connective tissue
ligaments largely lacking fat, the conclusion could also be that structural pelvic fat
is less involved in prolapse than was suggested in the first lines of this chapter.

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17.10 Conclusion 421

17.10 Conclusion

This overview of the connective tissue in the pelvis has noted some of the con-
tradictory publications that have appeared on this topic in the recent literature. It is
apparent that we lack knowledge of the morphology and function of the pelvic
connective tissue. What this implies is emphasized by two citations:
‘‘It is necessary at this point to emphasize that female urinary incontinence is a symptom,
and not a definitive diagnosis, which means that unless the reason behind the symptom is
diagnosed, correct therapy cannot be carried out.’’ [20]

‘‘There is no anatomical concept concerning the aetiology of urgency, or motor inconti-


nence. Indeed, the prevailing wisdom of nonsurgical treatment specifically excludes such a
concept. Instead, researchers have concentrated on the descriptive phenomena found in
urodynamic investigations. The result has been the conferring of clinical status to such
terms as ‘detrusor instability,’ an arbitrary (15 cm H2O) pressure rise on a machine,
whereas the underlying anatomical dysfunctions have been neglected. This is remarkable
in view of the traditional concept that function comes with restoration of anatomy – a
concept of particular relevance to the female pelvis and lower urogenital tract.’’ [20]

Literature

Literature has been grouped in reference lists of several chapters in those cases where
arguments are difficult to entangle or published over several articles or books. In cases of
citation the article or book involved is indicated by the reference number together with a
capital Arabic letter.
1. Cummings JM, Rodning CB (2000) Urinary stress incontinence among obese women:
Reviews of pathopysiology therapy. Int Urogynecol J 11:41–44
2. De Blok S (1982) The connective tissue of the female pelvic region. Acta Morphol Neerl-
Scand 20:65–92
3. De Blok S (1982) Spatial architecture of musculo-fibrous tissue in the female pelvic region.
Thesis University Amsterdam, Swets and Zeitlinger B.V., Lisse
4. Richter K, Fick H (1985) Die Anatomie der Fascia pelvis visceralis aus didaktischer Sicht.
Geburtsh u. Frauenheilk 45: 282–287
5. Warwick R, Williams PL (eds) (1973) Gray’s anatomy, vol 424. Longman, Edinburgh
6. Roper N (1978) Pocket medical dictionary. Churchill Livingstone, Singapore
7. Loenhardt H (1986) Atlas der Anatomie, vol 2. G. Thieme Verlag, Eingeweide
8. Hafferl A (1969) Lehrbuch der Topographischen Anatomie. Springer, Berlin
9. Fritsch H (1994) Topography and subdivision of the pelvic connective tissue in human
fetuses and adult. Surg Radiol Anat 16:259–265. Fritsch H (1993) Development and
organization of the pelvic connective tissue in the human fetus. Anat Anz 175:531–539
10. Fritsch H, Fröhlich B (1994) Development of the levator ani muscle in human fetuses. Early
Hum Dev 37:15–25
11. Reiffenstuhl G (1982) The clinical significance of the connective tissue planes and spaces.
Clin Obst Gynaecol 25:811–820
12. Pit MJ, De Ruiter MC, Lycklama à Nijeholt AAB, Marani E, Zwartendijk J (2003) The
anatomy of the arcus tendineus fasciae pelvis in females. Clinical Anat 16:131–137

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422 17 The Connective Tissue in the Pelvis

13. DeLancey JOL (1990) Functional anatomy of the female lower urinary tract and pelvic floor.
Neurobiol Incontinence Ciba Found Symp 151:57–76
14. Kaminga P, Chansigaud JP (1989) Anatomie fonctionelle des veines pelviennes chez la
femme. Phlébologie 42:363–384
15. Havenga K (1998) Total mesorectal excision in rectal cancer surgery. Thesis Leiden
University
16. Fritsch H, Hötzinger H (1995) Tomographical anatomy of the pelvis, visceral pelvic
connective tissue, and its compartments. Clin Anat 8:17–24
17. Grabbe E, Lierse W, Winkler R (1983) The perirectal fascia: morphology and use in staging
rectal carcinoma. Radiology 149:241–246
18. Fritsch H (1990) Entwicklung der Fascia recti. Anat Anz 170:273–280
19. Haas PA, Fox TA (1977) The importance of the perianal connective tissue in the surgical
anatomy and function of the anus. Dis Col Rect 20:303–313
20. Papa Petros PE, Ulmsten UL (1990) An integral theory of female urinary incontinence. Acta
Obstet Gynecol Scand 69(Suppl. 153):7–31
21. Fischer W, Pfister C, Tunn R (1992) Zur histomorphologie der Beckenbodenmuskulatur bei
Frauen mit Harninkontinenz. Zent bl Gynäkol 114:189–194
22. Blok BF, Holstege G (1998) The central nervous system control of micturition in cats and
humans. Behav Brain Res 92:119–125. (see als Blok BF et al (1997) Brain 29:112–121)
23. Marshman D, Percy J, Fielding I, Delbridge L (1987) Rectal prolapse: relationship with joint
mobility. Aust NZ J Surg 57:827–829
24. Al-Rawi ZS, Al-Rawi ZT (1982) Joint hypermobility in women with genital prolapse. Lancet
1(8287):1439–1441
25. Norton PA, Baker JE, Sharp HC, Warenski JC (1995) Genito-urinary prolapse and joint
hypermobility in women. Obstet Gynecol 85:225–228
26. McIntosh LJ, Stanitski DF, Mallett VT, Frahm JD, Richardson DA, Evans MI (1996) Ehlers-
Danlos syndrome: relationship between joint hypermobility, urinary incontinence, and pelvic
floor prolapse. Gynecol Obstet Invest 41:135–139

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Chapter 18
Sitting: A Pelvic Function?

Disabled people are totally depending on the possibility to sit if using a wheel-
chair. As long as the pelvis can rotate around the femur head, sitting is possible.
The ingenious mechanisms of pelvic movements is exemplified and explained in
rowing. Sitting conceals a dangerous dimension during labor, also clarified in this
chapter.

18.1 Introduction

Sitting is a combined action of the legs, the pelvis, and the trunk (Fig. 18.1): real
team work. The pelvic hinge for the sitting movement is the acetabulum. While the
vertebral column has to bend in standing up and sitting down, the pelvis rotates.
Flexion and extension occur in the legs. Studies on seated postures can be carried
out seemingly everywhere: a waiting area at an American airport is such a place
[1]. The author, hiding behind a book observed the seated persons and collected
information from 375 persons (232 men, 143 women), 5-min continuous obser-
vation each. Males preferred the slouched position (posterior aspect of the pelvis
not against the backrest) and sat preferentially with ankle over knee (50 %).
Females sat with knees crossed (81 %) and used a more erect posture [1]. Crossing
legs is the main posture in a public environment (nearly 90 % for ankle over knee
together with knee over knee). The social aspect of knee over knee for females is
disappointingly not treated by the author and the story does not tell whether the
author missed his plane or had to wait long for receiving his arriving guest.
You cannot sit without moving. Moving will prevent complications of pro-
longed sitting. On average, you will shift your sitting position nearly 7–8 times an
hour. Backward or forward nearly every 9 min, lateral movements, however, every
6 min [1, 2]. People in wheelchairs do have difficulties in performing these
movements, especially patients with spinal cord injuries. The slumped and passive
sitting posture is held responsible for the formation of ulcers, the most common
complication of prolonged sitting. Pressure ulcer is defined as ‘‘localized injury to
the skin and/or underlying tissue, usually over a bony prominence, as a result of

E. Marani and W. F.R.M. Koch, The Pelvis, 423


DOI: 10.1007/978-3-642-40006-3_18,  Springer-Verlag Berlin Heidelberg 2014

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424 18 Sitting: A Pelvic Function?

Fig. 18.1 Drawing of sitting


man by a student of the
Budapest Academy of fine
arts, taken from J. Barcsay
(1973) Anatomy for the
artists. Octopus books/
Sterling Publ. Co, London

pressure in combination with shear and or friction’’ [2, 3]. Its incidence in hospitals
and nursing homes is 15.5 % in the USA and 18.1 % in Europe [2].
Ulceration is not the only problem. Not being able to move during sitting is
related to a series of physiological deteriorations such as, lower back pain,
respiratory dysfunction, lumbar immobility, and joint stiffness [4].
It is the pelvis with its buttocks that makes being sitting possible (Fig. 18.1).
The involuntary, regular reposition of the legs by crossing during sitting helps to
move the buttocks and change the pressure. However, rather unexpected results
were found studying this crossing of the legs: ‘‘The activity of the internal oblique
muscle was significantly higher in the sitting position than in the supine position.
For the external and internal oblique abdominals, the activity was significantly
higher in the standing position than in the sitting position. When sitting, the
activity of the oblique abdominals is significantly lowered by crossing the legs in
the preferred way (either upper legs crossed or ankle on knee). In contrast, the
activity of the rectus abdominis is not significantly altered by leg crossing’’ [5]. It
indicates that more structures are involved in sitting, among which unexpectedly,
the abdominal muscles contribute too.
We already described in a previous chapter that the gluteus maximus will
retract from the pelvic protuberances during the sit down movement. However,
this only remains true as long as we are in the ‘‘secretary sitting posture’’: a 90
angle between upper leg and vertebral column. In all other situations, when
‘‘stretching out’’ in your chair, the gluteus maximus will still cover the trochanters.
Wheelchair users normally can hardly maintain the 90 angle, which is needed to
get the gluteus maximus muscle removed from under the trochanters. It is the
muscle that cannot withstand the sitting pressure. Since ulceration by pressure
occurs in the muscle, way before such a situation occurs in the skin, the people that
have difficulty maintaining a posture will get these ulcerations nearly unnoticed.

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18.1 Introduction 425

Why are we moving constantly during sitting? Without moving, oxygenation of


the tissue under pressure diminishes, and with each posture shift, the oxygen
content within the buttock tissue increases again. The difference measured is only
2.2 % [2]. Thus, a minimal timely reduction in the oxygenation is sufficient to be
noticed by the pelvic structures and is apparently dangerous for the underlying
tissue.
In the last decade, a new science appeared called ‘‘sedentary physiology’’
(in popular speech: TV or laptop (game) science) that distinguishes itself from
inactive physiology. Its target is to understand ‘‘the relationships of sedentary
lifestyles with major health outcomes and to provide an overview of the population
prevalence of sedentary behaviour’’ because ‘‘independent and qualitatively dif-
ferent effects on human metabolism, physical function, and health outcomes’’ [2A]
are found: Think for instance of cardiac metabolism, cancer, bone and vascular
dysfunction, and the best known, of course, obesity.

18.2 The Shoemaker and Sir Arbuthnot Lane

An article published in 1888 in the Journal of Anatomy and Physiology by Sir WM


Arbuthnot Lane (1856–1943) concerned the anatomical dissection of a male body
of initially unknown profession. As a staff member of Guy’s Hospital in London,
Lane became senior demonstrator in Anatomy and chief surgeon at the Great
Ormont Street Hospital for Sick Children. His theories on skeleton research can
best be taken from his obituary: ‘‘He had also become an authority in osteology
because of his notable thesis in which he particularly studied the changes in the
skeleton consequent on the stress and strain to which it is subjected by different
occupations, illustrating his observations by detailed studies of the anatomy of the
Coalheaver, the shoemaker and the Charwoman, out of which his general con-
clusion still remains true to the effect that we bear a simple mechanical rela-
tionship to our surroundings. Any change in that relationship produces a
corresponding alteration in our anatomy’’ [6]. He introduced iron plates for frac-
tures, later replaced by vitalium [cobalt–chromium alloy] ones, but the original
idea was his. Apart from being a master in reconstruction of the femur head
fracture, he also carried out the first end to end anastomosis between large and
small intestine.
His anatomical skills allowed him to deduce the labor history from the cadaver
brought into the gross dissection hall. He published three cases [7, 8] and we treat
here the shoemaker.
A body was brought in for dissection and studied by Arbuthnot Lane. He
concluded that the man had to be a shoemaker, not knowing his profession.
‘‘Having concluded, from a careful examination of the changes which the body
presented, that the man had been a shoemaker, I wrote to the medical officer of the
infirmary in which he died for any information he could give me, and he kindly
informed me that the man was entered on the books as a shoemaker’’ [8].

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426 18 Sitting: A Pelvic Function?

Shoemakers had to hand sew the shoes in those days. ‘‘In sewing the boot, the last
is fixed firmly between the front of the chest and the upper aspect of the thigh, and
the awl is used for making holes, through which the waxed threads are passed and
then pulled tight’’ [8]. The consequence is that hard pressure on the sternum
occurred, so that after years of carrying out that profession, damage of the sternum
(and also the shoulder and fingers) was found during the dissection. To keep the
boot firmly on the thigh, the pelvis and leg are also involved. Thus, during sitting,
both structures have to withstand the force and pressure; otherwise, hand-sewing is
not possible. What did our surgeon–anatomist noticed at the lower girdle?
‘‘In order that the thorax may be brought into such a vertical level as regards the
right thigh, that it may be able to fix the last upon it, it becomes apparent that the
fixed dorsal spine is rotated upon the pelvis and lumbar spine by means of a
vertical rotation of the last dorsal vertebra upon the first lumbar, of the first lumbar
upon the second, and probably in a diminishing degree to the fourth and fifth, since
the fifth lumbar does not rotate upon the sacrum around a vertical axis; also, that
the normal anterior convexity of the lumbar curve is diminished, the anterior
portions of the lower,’ and especially the lowest, fibrocartilage being compressed,
and a tendency to the forward and downward displacement of the lumbosacral
articulation being present. Since the sacroiliac synchondrosis is flexed, there exists
a tendency to the induration or the partial or complete removal ‘of the fibro-
cartilage where it is compressed between the opposing surfaces of bone drawn
violently together by the tightly drawn fibers of the posterior sacro-iliac ligaments,
and by the ligaments and fibro-cartilage of the pubic symphysis’’ [8].
Our conclusion should be as follows: lower vertebral column, sacroiliac joint,
symphysis, all are involved in hand-sewing shoes and the constant force on them
leads to damage that concerns cartilage and connective tissue but also shift of the
vertebrae mutually. However, the acetabulum and the bony structures around it
also suffer from the pressure: ‘‘Now, as far as the transmission of pressure is
considered, the concavity of the lumbar curve cannot be regarded as being limited
to that region, since the right thigh is fixed by the tonic contraction of powerful
muscles to the right innominate bone, and the innominate is drawn vigorously to
the lumbar spine and right chest; therefore, we must consider the concavity of this
arch as being formed by the lower half of the convexity of the dorsal spine, the
concavity of the lumbar spine, the upper portion of the body of the sacrum and its
lateral mass on the right side, and the innominate bone. Practically, the symphysis
pubis may be fairly regarded as forming a portion of the concavity of this arch’’
[8]. We stop citing our author here, but he noticed that sharp edges on the ace-
tabulum put emphasis on the pubic bones and other pelvic structures again and, as
he himself says, ‘‘I will not weary the reader by describing all of the very
numerous changes which the spinal column and pelvis of this workman had
undergone in consequence of the existence of the tendencies I have related’’ [8].
Deformation of skeletal structures, including the pelvic ones, is thus induced by
the forces and movements typical of a profession, such that one can identify that
specific profession in the nineteenth century due to its marked typical monotonous
repetition of movements: once a shoemaker, always a shoemaker.

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18.2 The Shoemaker and Sir Arbuthnot Lane 427

In our time such hard labor is absent, and our free time can be spent on sport or
being idle. Monotonous pressures on our body are thus also diminished. We
therefore encounter less specific professional-related skeletal changes or defor-
mations in our Western Society.

18.3 Rowing

In 1932, a new training description for the French army was published:
‘‘La préparation au B.A.P. au B.P.E.S.M. aux brevets de specialtiés’’ [9]. In this
military handbook, rowing is called the best of sports and the most complete one.
The arms, legs, and the trunk work together in a manner that it is the most
harmonious for the development of the body: the lung capacity reaches its greatest
extent, and its respiratory physiological action is executed during excellent
hygienic conditions. One may think that exaggerating is also a French art, but
literature shows that respiration in rowers is excellent and is combined with an
outstanding anaerobic metabolism during spurts [10]. Highest lung volumes are
indeed achieved by elite rowers during races [10].
During rowing one is seated on pelvis and buttocks, the femur moves in the
acetabulum and the vertebral column changes position regularly with each stroke
of the arms. We look here only at pelvic-related structures but vertebral column
has to tilt as regularly as the pelvis [11].
It all concerns postural control that is ‘‘essential for the efficient and effective
performance of all goal-directed movement’’ [12]. Any trainer will confirm that
rowing depends on the correct sitting position to keep the boat in the balance,
especially in the skiff that is placed low on the water. The balance has to be
maintained and in the mean time equal forces have to be exerted on the blades on
either side by the same person. Moreover, to pull the oars in a skiff with crossed
hands and to keep balance, the rigger is somewhat obliquely oriented. Although on
land posture is more easily kept in a sitting position than in a standing position, the
wobbling of the boat makes balance-sitting much more difficult, especially in the
learning phase. Think of people who turn over starting in a canoe during their first
try. ‘‘Recent studies found equilibrium control to be quite proactive, adaptive and
centrally organized, based on prior experience and intention. Balance can be
viewed as a skill acquired by the central nervous system through the use of many
systems, including passive biomechanical elements, available sensory systems and
muscles, and many different parts of the brain’’ [12]. Sitting in a stable situation is
a learned or acquired reflex. Everyone does it automatically, you don’t think about
it. You sit, although you noticed in advance the type of chair. Your learned reflex
fails during the act of sitting in a wobbly situation. You have to learn it (partially)
from scratch. Perhaps, the best example of a learned reflex is knitting. Grand-
mother can knit, talk, and if a stitch falls, she will still notice it automatically,
although her attention is engaged elsewhere, in the discussion, in which she is
actively participating [13].

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428 18 Sitting: A Pelvic Function?

Fig. 18.2 Phases of the rowing performance, reproduced with permission from McGregor [15].
Arrows indicate the direction of the trunk during the rowing stroke

Rowing in a skiff means that your seat moves forward and backward. You
therefore have to be sure of being seated in the correct posture. ‘‘If a rower lifts
him or herself from this sliding seat at any time, the seat will move away from
under them and the rowing action is disrupted. From a mechanical perspective, it is
clear that the need for the rower to remain in contact with the sliding seat at all
times imposes position-dependent constraints on the forces exerted at the oar
handle and the footstretcher’’ [14]. Indeed, strapping the oarsman or oarswoman to
the sliding seat helps the performance quality [14]. Mechanical power output was
found to be 12 % higher compared to not being fastened to the seat (the com-
parison was strapped versus normal rowing by the same oarsmen). The results are
interesting for sport racing in rowing, but it also shows that our sitting posture is
there to prevent slip of the pelvis by the buttocks, which minimizes our power
output in such cases and thus sitting on a sliding seat requires force. Normal sitting
also consumes energy, although far less.
Most studies of rowing are related to better sport performances or to lower back
pain with most attention going to the latter. In general, the lower back pain in
sports can vary from 1.1 to 30 % and is still increasing. In rowing, an increase has
also been noticed although double-blind studies are lacking. One can place an
oarsman in an MRI machine with a wooden rowing device and study his vertebral
column and sacrum. Here, we accept for the moment that displacement of the
sacrum is directly related to the pelvis, based on the criterion that there is nearly no
movement in the sacroiliac joint (see earlier chapters). In general, one can discern
a relax phase, from finish to recovery and a drive phase that starts at the catch point
(see Fig. 18.2). Our question is, what does the pelvis do and what does the group
of extensor and flexor muscles in and around the gluteal area do?
‘‘Angulation of the sacrum and pelvis appears greater at the catch and during
the drive phases where it is possible that the tendency to posteriorly rotate the
pelvis during the drive is a reflection of a compromised trunk stabilization
mechanism’’ [15]. The oarsmen have a flexion of their trunks of nearly 20 at the
catch and an extension of nearly 30 at the finish. Thus, from maximum flexion to
maximum extension is 50 (these results can differ for different rowing techniques
[15]). This is organized by both the lumbar spine angulation and by pelvic rotation.
The contribution of the pelvic rotation is hard to establish, but sacral angulation is
15 in the drive phase [15]. So let’s say two-fifth of the angulation is due to the

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18.3 Rowing 429

pelvis. Thus, on a sliding seat, the pelvis ‘‘wobbles’’ a 20. I am seated now in a
desk chair that can tilt forward and backward. Somewhat more than 30 backward
give the sensation of falling backward. We all have encountered this on a seat,
when we were not aware of its moving possibilities. And at a 50 forward and
backward tilt, I grasp both arms of my chair. My sitting is not at all secure
anymore. This is due, of course, to my moving center of mass, and this is noticed
in turn and anticipated by the nervous system in order to prevent falling. Sitting is
controlled by the nervous system.
Three groups of oarsmen were studied [15]: one normal group of elite rowers,
one group that gone through a period of lower back pain, and one group having
lower back pain. The lower back pain groups do compensate: ‘‘The rowers with no
history of back problems presented with greater rotation of the lumbar spine into
flexion at the catch, returning to a neutral upright position at the finish. Rowers
with either a current or previous history of low back pain tended to present with a
stiffness in the lower lumbar spine with little angulation occurring in these seg-
ments and consequently either gained their range by compensating either at the
pelvis or at the upper lumbar or lower thoracic spine. They also tended to tilt the
pelvis and overextend the spine at the finish position’’ [15]. Thus, compensation
for lower back pain is also found in pelvic rotation.
In a patient with spinal cord injury placed in the rowing setting with functional
electrical stimulation of the leg muscles, it was found that hip flexion and
extension were low, showing that pelvic movement in the seat is low for this
patient compared to elite rowers [16]. As long as one does not know the pattern of
recruitment of all, the involved muscles and their contraction intensity and timing
such experiments are doomed to fail.
Pelvic movement can be described by its angular velocity. During the drive
phase, pelvic angular velocity reached peak values of 200 per second [16]. It can
be translated in somewhat more than one rotation per second. Compare it to
bicycling and pedal rotation. During normal brisk biking, pedaling is around one
rotation per second. Of course, the pelvis does not rotate totally; an oarsman stroke
lasted less than 2 s and only in the drive part during 30 % of its time does the
pelvis rotate, which is less than half a second. Nevertheless, for a human body, it is
still a rather fast rotation.
The muscles studied [16] demonstrate that during the drive, the latissimus dorsi,
erector spinae, gluteus maximus, and biceps femoris are strongly active; all
muscles constituting a muscular bow around the back of the pelvis. Just before the
recovery phase, before finishing stroke, the abdominal muscles (external and
internal oblique, rectus abdominis, transversus abdominis) start their activity
which last to just before the midpoint of the recovery phase. During peak force,
needed during the stroke phase, the gluteus maximus, biceps femoris, and lower
erector spinae show the highest EMG activity, indicating that the muscles that
make the curve around the back of the pelvis are strongly involved. It should be
noted that only a restricted portion of muscles could be studied by EMG during
rowing, which may have distorted the real picture. Nevertheless, the gluteus
maximus must move beneath the trochanters; remember that only in the secretarial

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430 18 Sitting: A Pelvic Function?

sitting posture of 90 is the gluteus maximus aligned along the trochanters. Since
during rowing the trunk goes from about 70 till 120, the gluteus must shift. In
fact, the rower is lifted up a little due to gluteus movement and its contraction.
The abdominal muscle functions are still a mystery: Rib cage fractures occur
regularly during intensive rowing; it was discovered that the contraction of the
abdominal muscles caused rib fractures not in the drive phase but in the recovery
phase, especially the external oblique abdominal muscle [17]. Nevertheless, these
results show that during the recovery phase, the abdominal muscles do have an
important function in going back from extension to flexion.
Anthropometry is used in the early selection of elite rowers: e.g. short ham-
strings limit the flexion at catch and the rumor is that males suffer more from it
than women. Studies on highly ranked oarsmen and oarswomen show that: ‘‘high
ranked rowers were taller and heavier, had a smaller sum of total skinfolds, had
longer forearms and thighs, a greater biceps girth and had smaller hips with respect
to their shoulder width. Contrasting these significant anthropometric differences,
females of differing performance abilities were found to be of similar shape and
size in all aspects’’ [18]. Pelvic size in comparison to shoulder size is different in
male and female rowers. We already learned that the pelvic width in females is
relatively larger than in men. Could it be that training of the shoulder muscles in
men over accentuate the difference between shoulder and pelvic width, while due
to the apparently larger pelvic width in females this is less noticeable? At any rate,
for females with a relatively larger pelvic width, rowing–sitting should be easier
than for males.

18.4 Wheelchair Sitting

At the start of this chapter, some remarks were made about wheelchair sitting by
disabled people. Attention was focused on ulcers. At several technical universities
and Biomechanical departments of other universities, intensive research programs
are carried out to overcome ulceration in wheelchair users. In this part, we sum-
marize these results based mainly on Dutch research done in the Medical Faculty
of the University of Maastricht and by Department of Biomechanical and Tech-
nical Engineering of the University of Twente, both in the Netherlands.
The results on rowing indicated that pelvic rotation is involved in maintaining
the correct posture during sitting. In general, two systems maintain posture: one
system registering the body geometry and the other focusing on stability. These
two systems work in parallel [20], and, of course, both are working simultaneously
during sitting. Even pelvic rotation information controls vestibular (balance)
information during sitting [12]. This became apparent after studies on legs-up
rotation during sitting with stretched legs. Since muscle activation occurs
sequentially, such a pattern cannot be organized by simple reflexes, and therefore,
pattern generators are postulated. Their functions are twofold: a pattern choice of
the specific muscles to be activated followed by shaping and timing [12]. The

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18.4 Wheelchair Sitting 431

Fig. 18.3 Pressure on 200


intervertebral disks 180
normalized to
standing = 100 % (changed 160
after Nachemson and 140
Elfstrom [21])
120
100
80
60
40
20
0
lying sitting

pattern generators are localized in the central nervous system and coordinate
somatosensory (not only pelvic), vestibular, and ocular information. In most
patients with spinal cord injuries, the commands of the pattern generator no longer
reach the motoneurons of the spinal cord that steer the sitting muscles: Sitting
becomes slumped and passive.
Pressure is the other but passive factor that is important in wheelchair patients.
Remarkably the pressure on intervertebral disks in the sitting position is nearly the
double compared to the upright position (Fig. 18.3). In the standing position, there
is nearly no pressure on the trochanters, but during sitting, there is exerted 6–7
Newton per kg weight, reaching some 450 Newton per non-overweight individual
[19]. Thus, vertebral column and pelvis are loaded with more weight in the sitting
position than in the standing position. Here, we encounter the other danger for the
wheelchair user: sitting pressure cannot be changed by the pattern generators due
to the lack of sensory information. Luckily enough, the intervertebral disk pressure
diminishes on the moment the back is supported and backrest inclination produces
the largest effect [12]. Nevertheless, wheelchair patients still develop ulcers.
Measurements of the sitting pressure showed that both the trochanters and the
sacrum are the places with the highest pressure. Pelvic rotation, together with seat
inclination and chair recline, is now used to change the pressure (Fig. 18.4) [19].
A seat can be changed in the sagittal direction (forward–backward tilt) or
frontal direction (lateral tilt). By changing the seat in the sagittal direction
(Fig. 18.4), the pelvis of the sitting person rotates, but does so in the frontal
direction too. Sagittal tilt reduces the pressure on the sacrum and shows the
strongest change in the localization of the center of pressure. Frontal tilt reduces
the pressure under the trochanters. By movements of the seat, both sagittal tilt and
frontal tilt are organized independently of backrest or other chair parts [19]. Such a
passive motion technique is called decoupled pelvis rotation (DPR) [19].
‘‘Because pelvis alignment directly affects body posture and buttock load,
systems that control pelvis angle relative to the seat support could play an
important role in pressure ulcer prevention’’ [19]. Since these results were

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432 18 Sitting: A Pelvic Function?

Fig. 18.4 Chair for postural


adjustment. Situations of
sagittal seat inclination (1),
pelvic rotation (2) and chair
recline (3) are demonstrated,
reproduced with permission
from van Geffen 2008 [19]

obtained in research on healthy individuals, one still has to wait for the results
obtained with handicapped persons. ‘‘However, it must never be the intention to
apply dynamic seating surfaces and completely replace the need for postural
movement’’ [19]. Since ulceration is a complicated process, it would be surprising
if seat change alone would help, which the authors clearly realize.

18.5 Sitting and Delivery

Sitting in a special chair during delivery has been the subject of numerous inves-
tigations. Studies concerning the first stage of labor are inconclusive, due to the fact
that randomizing is nearly impossible for ‘‘blinding participants and caregivers to
the group to which they have been assigned, and very difficult to blind those
assessing outcomes’’ [22]. It is the second stage of labor in which the birth chair is
used and the sitting position can be scientifically compared to the recumbent nearly
flat position because the posture of the women can be standardized. ‘‘Although
chairs are preferred by some women, no advantages have been found with regard to
the length of second stage, need for instrumental delivery or degree of perineal
trauma. However, there has been one consistent finding: birthing chair delivery is
associated with a greater blood loss at delivery’’ [22].
The main points of discussion are upright delivery versus recumbent dorsal
delivery and the free will of the pregnant mother to choose the preferred delivery
method rather than the recumbent one imposed by medical staff for possible ‘‘fetal
monitoring, intravenous injections, and the stipulation that analgesia could be
necessary’’ [23]. In this noisy discussion, the birth chair is to fall under upright
positions and is therefore distorted in this debate. For example, a study concerning

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18.5 Sitting and Delivery 433

Roberts et al. Hendrik van Deventer Birth-mate

Fig. 18.5 Comparison of Roberts et al. [26] and Hendrik van Deventer [25] birth chairs and an
industrial birth stool, called Birth-mate. Legend does not contain all characters indicated: 10
birthing chair; 12 seat; 18 U-shaped opening; 20 handgrips; 50 padded leather cushion; 38 feet
rest; a reclining backrest; d seat with cushion of horse hair; i adjustment for seat by pins; e side
doors; f adjustable; g handgrips. Reproduced with permission

288 primipara and 348 multipara concludes that delivery by a birth chair causes an
increase in postpartum hemorrhage, as found by others, but also an increase in
perineal tears. And even if a birth chair is used, it is ‘‘less likely to have an intact
perineum’’ and ‘‘no evidence was found that the use of the chair was beneficial’’
[24]. This study belongs to those using the largest patient populations.
Let us first look at the birth chair. We put next to each other the portable birth
chair of Hendrik van Deventer (1651–1724) [25], the birth chair of Roberts [26] as
described in USA Patent 4,703,975 from 1987 and a recent industrial one
(Fig. 18.5). The three chairs are functionally almost identical. A reclining back-
rest, an adjustable seat height, and adaptable handgrips, for the woman to press
against, are present in Hendrik van Deventers proposal. Roberts’ proposal contains
a stiff backrest and instead of changing seat height an adjustable footrest is
introduced. Handgrips are parallel to the seat, which was already applied in the
fourteenth century birthing stool [26]. The industrial one, called Birth-mate and
claimed to be developed by Dutch midwives, is simply a three-quarter stool
without backrest or adjustments or handgrips present. Indeed, the 1701 birth chair
seems more sophisticated than the modern ones shown here.
There is controversy about the advantages and disadvantages of the various
models. Starting in 1800, a number of applications for patents on birth chairs was

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434 18 Sitting: A Pelvic Function?

filed in the USA [26]. The birth stool is perhaps overly simple. Japanese and
American super-sophisticated birth chairs are on the market. In these, the chair can
be tilted in such a way that the woman is back in a dorsal position. The first of
these found in literature by this author is the one by Howard, published in 1958
[30]. The basic idea is that all birth chairs have a seat with a hole in it, whether
mounted on legs, on paneled doors or a circular wall. As we have seen above, in
sitting, the sacrum and the trochanters have to be supported. The ‘‘Birth-mate’’ is
the simplest one that fulfills these demands. There are of course other approaches,
like sitting on an inflated ball in which the husband or assistant, sitting or standing
behind the woman helps maintain her balance (the same holds for the Birth-mate).
In the section on rowing, the problem of balance was discussed. There are many
number of different birth techniques, but we will not consider all these satisfying
ourselves with the knowledge that sitting is sitting.
Next are the cultural or social aspects of the birth chair to be considered. There
is no doubt that in the discussion, the safety of mother and child is of paramount
importance. But if this consideration can override all approaches, the question
remains: Is there another safe system than the recumbent dorsal position in bed? Is
it the midwives or obstetrician who limits mobility during delivery [23]? The main
social objection to recumbent dorsal delivery is that emotionally there is less
satisfaction with in maternal care. In other cultures, during labor, woman can
stand, walk, sit, pull on ropes, and be tied to trees during labor [23]. There are thus
other methods of delivering a baby that will emotionally satisfy the mother during
the birth process. However, the question is, of course, whether a particular method
increases birth, death or damages the mother and can it be introduced in our
clinics? It would be ridiculous to think that in our culture, we would tie up a
pregnant woman during delivery. There are cultural restrictions in our society, too.
So any upright delivery method should assure a balance between safety of mother
and child on the one hand and our cultural restrictions on the other. Since the
safety of mother and child is (and has been) studied, and the upright delivery
results at best only in blood loss and is not more beneficial, the overriding argu-
ment has won thus far. Even the large study (189 deliveries) in the Glasgow Royal
Maternity hospital, published in 1983, showed: ‘‘Overall blood loss was greater
among patients delivered in the chair, but more of this group had either an intact
perineum or only superficial damage.’’ The blood loss was not only during delivery
but there was also an increased frequency of postpartum hemorrhaging [27]. It
should be mentioned that there was serious criticism on this study, due to the
regular obstetric interventions in the compared groups. ‘‘Intervention on this scale
before the trial of chair against bed surely defeats the object of the chair, which is
to augment natural mechanisms of labor and avoid the need for excessive aug-
mentation and analgesia’’ [28].
Up to now, the most important argument for upright or sitting deliveries has not
been treated: ‘‘the direction of gravity and the direction of expulsive forces are
synergized’’ [29]. Three physiological/physical arguments plead in favor of the
upright position during delivery: Application of Newton’s law of gravity would
indicate that the upright position is mechanically more advantageous: to expel in

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18.5 Sitting and Delivery 435

the direction of the pull of gravity, while this force pulls the fetus in the same
direction. The fluids in and around the fetus will let it sink into the cervix in the
upright position, but in the recumbent position, it sinks more toward the pelvic
backside than in the cervix. Uterine contraction pressure will, through the fluids in
the fetus, be directed toward the cranium. In the upright position, mainly the
occipital brain areas will be under pressure, while in the dorsal position, the
pressure is toward the frontal lobes. Since occipital brain parts are more developed
at birth, one could argue that the occipital lobes can withstand such pressure better.
It is a weak argument; however, since fetal brain plasticity is rather large. An
analogous argumentation has been put forward for the brain stem, in which all
essential vegetative functions like heart rhythm and breathing are organized [29,
30]. Simple calculations should indicate that in the sitting position, only 65 % of
the force necessary for the dorsal position is needed [30].
Toward the end of the twentieth century, focus was on the fetal head-to-cervix
force. Before the cervix is effaced, this head-to-cervix force produces a seal that
makes it possible for intrauterine pressure to rise, which can be considered an
argument in favor of the birth chair. If the cervix is effaced, it is the uterine
efficiency that continues labor. The head-to-cervix force is sometimes considered a
clinical important resistance that can cause dystocia (difficult labor). ‘‘But does
this seal represent clinically important resistance? As resistance will contribute to
head-to-cervix force, then according to this model, dystocia should be more fre-
quent with greater head-to cervix force. In fact the opposite is observed. Head-to-
cervix force is more closely associated with vaginal delivery than intrauterine
pressure or even cervical dilatation. This suggests an influence by something other
than cervical compliance or intrauterine pressure. That factor is likely to be uterine
efficiency: the ability of the contraction to push the head onto the cervix. The
findings that head-to-cervix force is lower in labors that require oxytocine, and that
increasing force occurs with increasing frequency of contractions seems to confirm
this’’ [30A].
Thus, it is the frequency of the uterine contraction that, say after partial efface
of the cervix, determines labor outcome. Uterine contraction frequency and force
is regulated by hormone-receptor interaction (the hormones being oxytocine and
its receptor and progesterone and the gaseous nitro-oxide hormones [30B]), not by
uterine position.
Since the cervix is, so to say, the opening end of the uterus, it is remarkable that
amniotomy immediately when a cervix dilatation of 2 cm is reached promotes
labor and reduces its duration. Again, it is not the position, but removal of amniotic
fluid that reduces labor duration [30A]. So, the flaw in the chain of reasoning is the
extreme emphasis on gravity, while a series of other factors are also involved and
presumably more important. Moreover, sitting increases the lowest registered
pressure by the uterus on its contents between two contractions, called intra-
uterine resting-phase pressure, by nearly 25 mm Hg [30C], mainly by an increase
in abdominal pressure. For some, experimental results on animals support argu-
ments that increase in abdominal pressure will influence placental blood flow,

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436 18 Sitting: A Pelvic Function?

while for others, they indicate that increase in abdominal pressure results in an
acceleration of the birth process [30C].
One of the largest populations used in a study on maternal position at Midwife-
attended birth and perineal trauma concerned 5,814 women with spontaneous
vaginal birth of which 3,756 were included in the study [30F]. Why 1,058 women
were excluded is unclear. It is a strange reasoning: ‘‘other birth positions did not
have significant associations with perineal trauma, although for some positions
(sitting, squatting, kneeling, lithotomy, supine) the numbers were probably too
small to reach statistical significance’’ [30F]. Sitting delivery concerned 28 cases,
lithotomy 27, kneeling 54, squatting 47, supine 50, which are clearly too small.
Moreover, ‘‘the semirecumbent position was significantly associated with more
perineal trauma,’’ but the studied population was in a ‘‘large public tertiary referral
teaching hospital’’ [30F]. A good guess is that you are referred to a hospital if your
obstetric risk is high, because of the 3.756 woman, 1,679 (44.5 %) required per-
ineal suturing. From most of the factors related to perineal suturing, maternal age,
induced labor, regional anesthesia, deflexed head and newborn weight of 3.500 g
or more, it can be concluded that the women were correctly referred to the hospital
for an increased risk. The study also included the estimation of blood loss, but no
results are given, although it was indicated in the introduction that indeed blood
loss is the main difference between upright and recumbent position during
delivery. Due to its flaws, this study hardly contributes to the upright-recumbent
discussion. The more so, because already in 1997 (article known by the above
cited authors), it was advocated that choice of posture during delivery is only
acceptable if women have a low obstetrical risk [30G].
In conclusion, adverse results are present in literature on birth chair delivery.
Blood loss during delivery and postpartum hemorrhages and perineal tears are
clear risks. And remember, ‘‘one woman dies each 4 min due to postpartum
bleeding’’ (see Chap. 3)
The fact that ‘‘In other cultural circumstances, women during labor can stand,
walk, sit, pull on ropes, and be tied to trees’’ [23] were used as an argument for an
alternative delivery method. Let us look into the WHO report [31] on neonatal and
perinatal mortality. It defines stillbirth in the following way:
Stillbirth or fetal death is death prior to the complete expulsion or extraction from its
mother of a product of conception, irrespective of the duration of pregnancy; the death is
indicated by the fact that after such separation, the fetus does not breathe or show any
other evidence of life, such as beating of the heart, pulsation of the umbilical cord, or
definite movement of voluntary muscles [31].

Looking into Table 18.1, it is absolutely clear that the stillbirth rate is the
lowest in Europe, Australia and New Zealand, and Northern America. ‘‘Compli-
cations arising during birth are the main cause of death among almost all infants
who were alive when labor started, but were born dead’’ [31] and ‘‘Where women
receive good care during child birth, intrapartum deaths represent less than 10 %
of stillbirths due to unexpected severe complications’’ [31].

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18.5 Sitting and Delivery 437

Table 18.1 Intrapartum stillbirth mortality for the year 2000 by United Nations region and
subregion from WHO report [31] on stillbirths reproduced with WHO permission
Stillbirth Number Intrapartum Number of Intrapartum
rate of deaths as % intrapartum mortality
stillbirths of stillbirths deaths (000) rate
(000)
World 24 3328 33 1097 8
More developed regionsa 6 84 10 8 41
Less developed regions 26 3,244 34 1089 9
Least developed countries 31 850 35 301 11
Africa 32 1002 35 349 11
Eastern Africa 27 297 33 98 9
Middle Africa 41 191 37 71 15
Northern Africa 18 85 32 27 6
Southern Africa 21 26 28 7 6
Western Africa 41 403 36 147 15
Asiaa 27 2124 33 709 9
Eastern Asiaa 19 396 24 96 5
South-central Asia 34 1410 37 518 13
South-eastern Asia 19 223 30 68 6
Western Asia 18 94 29 27 5
Europe 8 61 10 6 1
Eastern Europe 15 41 10 4 1
Northern Europe 5 5 10 1 1
Southern Europe 5 7 10 1 0.5
Western Europe 4 8 10 1 0.4
Latin America and 10 112 25 28 2
Caribbean
Caribbean 18 14 31 4 6
Central America 11 37 24 9 3
South America 8 62 24 15 2
Northern America 3 16 10 2 0.3
Oceaniaa 23 6 35 2 8
Australia/New Zealanda 3 1 10 0.1 0.3
Melanesia 25 6 36 2 9
Micronesia 7 0.1 24 0.02 2
Polynesia 11 0.2 24 0.04 3
a
Australia/New Zealand and Japan have been excluded from the regional estimates but are
included in the total for developed countries

The WHO report also answers the question on obstetricians and midwives
posed above. Seemingly good Western obstetric care, which enforces the dorsal
recumbent or flat position, will help to overcome birth death and the West has
found and applied it. Infections are responsible for 26 % of newborns to die [31].
Even after subtracting this percentage, Western neonatal care is still far better. It is
thus not the infection of the neonate, it is also not the nutrition of the fetus: ‘‘Low
birth weight has long been debated as one of the causes of neonatal deaths. It is
associated with the death of many newborn infants, but is not considered a direct

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438 18 Sitting: A Pelvic Function?

cause. Around 15 % of newborn infants weigh less than 2,500 g, the proportion
ranging from 6 % in developed countries to more than 30 % in some parts of the
world. The main ‘culprit’ is preterm birth and the complications stemming from it,
rather than low birth weight per se. There is, however, no doubt that maternal
health and nutrition at conception are important determinants of weight at birth,
neonatal health and frequency and severity of complications, and that maternal
infections such as malaria and syphilis contribute to adverse pregnancy outcomes
and thus to mortality’’ [31]. It is all about obstetric care and the health of the
mother!
Active management, ‘‘a protocol for the supervision of the intrapartum care of
nulliparous women that evolves with continuous review,’’ shows that it can pre-
vent prolonged labor as long as this management is carried out by midwives with
an experienced consultant on standby [30A]. It is continuous obstetric review that
diminishes stress and a continuous companion, like a (student) midwife during
labor, helps a lot: ‘‘Certainly, systematic review of the effect of a trained com-
panion in labor shows a reduced operative delivery rate’’ [30A].
Indeed, ‘‘Woman’s views of labor have received scant attention in the debate
concerning active management of labor. Obstetricians’ impressions of women’s
preferences are often obtained from women with strong views or complainants that
may not be representative. The debate on childbirth has been about choice of
career or place of birth, rather than about labor’’ [30A]. This should be considered
a plea for more information not for putting aside the opinions of women.
Around 1900, a steady fall of neonatal deaths set in, coinciding with start of
maternity services, availability of licensed obstetricians and good hygiene. The
greatest reduction occurred after the Second World War when the obstetric care
became available to all social layers. The drop was from 50 to just above 5 per
1,000 births [33]. Could dorsal recumbent delivery also have contributed to replace
the birth chair, and thus reducing blood loss during delivery and perineal tears and
postpartum hemorrhaging? One should also think of the next pregnancy. More-
over, North America has the lowest level: 2 per 1,000 (see Table 18.1), and here,
the flat dorsal birth position was generally advocated starting around 1830 in the
USA [32], which is remarkable but is not conclusive as argument.
Amanda Carson Banks published an historical overview of birth chairs in her
book: ‘‘Birth Chairs, Midwives and Medicine’’ and placed the development and
disappearance of the birth chair in the context of changing social and medical
attitudes toward birth. The medical profession declared birth a ‘‘disease,’’ thereby
strengthening the physician’s economic position: ‘‘Professional obstetrical practice
was key to developing a market large enough to support the growing number of
doctors’’ [26A], and as a result, midwives were disadvantaged in this market. One
of the consequences of medical influence on delivery, Bank maintains, was the
disappearance of the birth chair and the introduction of recumbent delivery. There
is no objection to this reasoning, but an important point must be added. In the
eighteenth century, stillbirths occurred at a rate far higher than one in twenty. As
indicated by Banks too, in difficult cases, the doctor had to come to the assistance

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18.5 Sitting and Delivery 439

of the midwife. The conclusion must be that midwives lacked professional


knowledge. In 1770, the French Minister J. Raulin published the following judg-
ment on causes for birth problems: ‘‘shortcomings of the midwives during child-
delivery,’’ midwives who practice recklessly and without sufficient knowledge.
Roulin therefore ordered that instructions for midwifes be issued (see Chap. 4).
Moreover, with such a high rate of stillbirths, women’s fear that the child could die
called for adequate support and this support became (slowly) concentrated in the
obstetrical knowledge of the physician. By ignoring the impact of Hendrik van
Deventer as a teacher for midwives and promoter of the birth chair, in numerous
editions in Latin, Dutch, French, German, and English [26B]. Banks undermines
her general reasoning argument. In the late seventeenth and the eighteenth century,
serious efforts were attempted by doctors and administrators to increase midwives
knowledge to reduce stillbirths in Europe (see also various remarks in Chap. 2). It
began as early as the sixteenth century as is clearly shown by Banks in her chapter
Stones and Stools: e.g., Jacob Rueff (1500–1558) not only published his book on
midwifery (1544) but was also responsible for the examination of midwives in
Zurich. Culpepper published his ‘‘Directory for Midwives’’ in 1651 and his reason
was more knowledge for the pregnant woman and the low quality of nurses and
midwives [26C]. Thus, at least three centuries of vernacular publishing and calls
by medical doctors and by administrators for improvements in the quality of
midwifery can be documented, to no avail: stillbirth rates remained high. And it
took the physicians and obstetricians another 120 years (1830–1950) to attain
stillbirth rate reduction, containing the deepest set-back by the condemnation of
the results of Semmelweis (1818–1865). Fair is fair, the midwifery department in
Vienna had a 4 times lower rate of childbed deaths, and even in the 1940s and
1950s, nursing services in the USA had ‘‘lower infant and maternal mortality rates
than most hospitals and significantly lower incidents of iatrogenic (doctor-caused)
complications and nosocomial (hospital-caused) infections’’ [26A]. Opposition by
the midwives (‘‘concerns about the indiscriminate and escalating use of obstetric
surgery and its potential to cause more harm than good failed to impact upon
trends in type of childbirth and public preference’’ [26D]) slowed down the pro-
cess, but it was the physicians, not the midwives who were successful. Let us not
forget, however, that the physicians had an advantage, both economically and
scientifically.
There is one more aspect of the sitting position during delivery, since pregnant
women nowadays stay at work, often right up to term: ‘‘For the pregnant worker,
the primary problems associated with long intervals of sitting are poor back
postures and resulting back pain, long reaches that result from improper work-
station designs, edema and pooling of blood in the feet if proper footrests or rest
breaks are not provided. An increased rate of low back pain and disability is also
associated with jobs in which the worker must sit for extended periods of time.
And,…, the traditional seat and seated workplace leads to forward leaning work
postures in the pregnant worker that can compress the abdomen and strain the neck
and upper shoulders. Also, because of the increased abdominal dimensions and

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440 18 Sitting: A Pelvic Function?

Fig. 18.6 Lithotomic sitting


position during delivery
‘‘pioneer birth scene after
Engelmann’s illustration
showing woman, husband,
midwife, and two attendants’’
[32] (reproduced from
Witkonski 1887)

mass, mid-term and late-term pregnant women have increasing difficulty getting in
and out of office chairs and therefore have an increased risk of falls or slips’’ [30D].
Calculations from literature indicate that at least 45 % have mild pain, 25 % have
serious pain, and 8 % are severely disabled during pregnancy by ‘‘pregnancy-
related pelvic girdle pain’’ and ‘‘pregnancy-related lower back pain.’’ The figures
postpartum are lower, but still 7 % end up with ‘‘serious problems’’ [30E]. Several
ergonomic proposals to overcome sitting problems of the pregnant women have
been published, and attention for this problem is increasing. Moreover, the new-
born of mothers working in the third trimester of pregnancy will weight 150–400 g
less compared to mothers that stayed at home. Placental infarctions increase if
stand-up work goes on into late gestation, presumably by low uteroplacental blood
flow [30H] (already known by Adolphe Pinard (1844–1934) see Chap. 3).
To finish this part, there seems to be a direct relation between the lithotomic
(bladder stone-cutters) position (see Chap. 4, Fig. 4.1) and the sitting delivery
position. ‘‘The interaction of the evolving sciences of lithotomy and obstetrics is
not surprising since techniques used in obstetric surgery (e.g., cesarean section)
had features in common with those used in lithotomy’’ and ‘‘Although a precise
relation between the reclining birth position—the forerunner of the lithotomy
position—and the lithotomy operation is difficult to establish, the adoption of the
lithotomy position for birthing and extensive practice of the lithotomy operation
occurred at the same time and place in France in the seventeenth century’’ [32]
(Fig. 18.6). Such a link is also apparent in the USA in the practice of William
Shippen an obstetrician and lithotomist, and by Hugh Hodge, both practicing
roughly between 1750 and 1800 [32]. Seemingly history determined lithotomic
delivery position, as was the case with chair sitting and not scientific research for
the well-being of mother and child.

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18.6 Lumbosacral Curve and Pelvic Rotation During Sitting 441

18.6 Lumbosacral Curve and Pelvic Rotation During


Sitting

The pelvis rotates during the sitting movement, and throughout sitting, the lumbar
lordosis, so clearly present in standing, is obscured. ‘‘The posterior thigh and
gluteal muscles play an important part in flattening of the lumbar curve in sitting,
for they arise from the ischial tuberosity, the posterior aspect of the sacrum and the
ilium; as the thighs are flexed, they tend to rotate the pelvis by the tension of their
limited length’’ [34] (Fig. 18.7).
Thus, the rotation of the pelvis is the consequence of the limitations of the
muscles. In fact, the pelvis has to give in by rotation; otherwise, you cannot sit. The
lordosis is present between lumbar vertebrae and sacrum flattens, and in the sitting
position, the bow seems to turn externally. Can it become kyphose (hump) like?
‘‘Current ideas on what is ‘good posture’ are rather vague. The usual advice,
possibly based on aesthetic and military tradition, is ‘sit up straight’ and ‘don’t
slouch.’ Paradoxically, sitting straight is taken to mean sitting with a lumbar
lordosis and not allowing the lumbar spine to flex and flatten its curve. As far as
the lumbar spine is concerned, there is no reliable evidence that sitting up straight
is, in fact, beneficial. On the contrary, population studies have shown that lumbar
disc generation is rare among people who habitually sit or squat in postures which

3
4

Fig. 18.7 X-ray drawings of individual placed in the lateral recumbent position with different
angels between knee and hip. In black are indicated muscles (gluteal- (1), iliopsoas- (2), rectus
femoris- (3), and biceps femoris muscle (4), in which D shows the secretary position. Rotation of
the pelvis can be followed and seemingly is a play between the limitations of the different
muscles. Also noticeable is the change in lumbar curvature. ‘‘Note the normal position of the
balanced muscle relaxation at 135, with increase in the lumbar curve as thighs are brought
backward and decrease in this curve as the angle between the thighs and the trunk is reduced’’
[34]. Figure reproduced with permission from Keegan [34]

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442 18 Sitting: A Pelvic Function?

Fig. 18.8 Reduction in the


lumbar lordosis during
various positions (reproduced
with permission from Keegan
[34])

flatten the lumbar spine’’ [35]. We all encountered these remarks like ‘‘sit up
straight’’ during our youth. Thus is reducing the lordosis and flexing the lumbar
spine inducing intervertebral disk generation? The most involved disks are lumber
four and five [34].
Before answering both questions, we first have to look into the flattening of the
lumbar lordosis in various positions. Figure 18.8 shows the reaction of the lumbar-
sacral spine on the different positions as drawn from X-rays. The lordosis here can
be reduced toward a nearly flat line, never into a kyphosis. In the most extreme
flexed posture (sitting, knees up, arms around legs), the angle between the sacrum
and the first lumbar vertebra stays 20, [35]. Thus, lordosis is diminished but not
turned externally in the cases presented in Fig. 18.8 as questioned above. How-
ever, in slump sitting, the lumbar angle (between Th12 and S2) can be up to 5
kyphotic [36].
Sitting in flexion has advantages: less pressure on the vertebral joints, reduction
in stress on the back part of the intervertebral disk, with an increase in the frontal

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18.6 Lumbosacral Curve and Pelvic Rotation During Sitting 443

Fig. 18.9 Gravity effects of


changes in hip and knee
flexion on the curvature of the Hip flexion
lumbar spine as measured by
its midsagittal length.
Squares are lying situations,
triangles sitting positions
(reproduced with permission
from Eklund and Liew [37])

part, but this part can withstand with ease the extra stress, increase in metabolic
exchange in the intervertebral disk. Long periods of low load can damage the
intervertebral disk by its increased hydrostatic pressure. However, the consequent
movements during sitting will counter act this danger. The conclusion therefore is:
‘‘The disadvantages are not of much significance and we conclude that it is
mechanically and nutritionally advantageous to flatten the lumbar spine when
sitting and when lifting heavy weights’’ [35].
Slump sitting does have disadvantages: without head or back support, an
increased activity of thoracic spine muscles, cervical spine muscles (erector spinae
of these regions), and compensation of the extra head flexion is caused that can
induce stress in the cervical region with postural pain as the consequence [36].
Changes in lumbar lordosis, with the consequence of pelvic rotation, can have
consequences for posture at cervical spinal levels and the head.
In the previous part on the birth chair, we have seen that gravity plays an
important role in the discussion on birth chair use during delivery. There is one
more aspect of gravity that has been worked out in a hardly cited article [37].
Figure 18.9 demonstrates the results. The curvature of the lumbar area L5-T12
(note: not the sacro-lumbar angle) is measured by its length. The stronger the
curvature, the longer the measured distance is. By putting the test persons on bed
or being seated with different hip and knee angles, the effect on the lumbar cur-
vature can be measured. The difference between the bed lying and the being seated
situations is gravity. From the graph, it is clear that at 60 hip flexion, there is
nearly no gravity effect for both situations, whatsoever the knee flexion is.
However, lower hip flexion shows that gravity increases lumbar curvature for the

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444 18 Sitting: A Pelvic Function?

sitting position, while at higher hip flexions lying undergoes more lumbar bending.
Now remember that the recumbent delivery position could be flat (0 hip flexion)
or somewhat higher 30 till 60. In those cases, gravity reduces the lumbar cur-
vature, while in the sitting position during delivery (90 or somewhat higher),
gravity also reduces the lumbar curvature. Here, gravity has the same conse-
quences for both lying and sitting.

18.7 Belly Dancing and Pelvic Movements

We stay out of the discussion on the origin and history of belly dancing and
whether it is an erotic dance [38] or not, although several authors proclaim it is.
Belly dancing is characterized by hip movements and thus there is pelvic
involvement, together with upper and lower trunk movements, conjointly with
elegant arm movements.
Belly dancing is mainly typified by rolling one’s hips. In the chapter on vision,
it was described that lateral tilting of the pelvis during walking is organized by
gluteus medius and minimus muscles. Therefore, rolling of the hips needs
involvement of these two gluteal muscles. The greater the width of the pelvis, the
larger the deflection is. We already noticed that female pelvic width is relative
larger than the male ones. Although males do belly dancing, the visual effect is
greater in women.
Another stance in belly dancing is bending the trunk backward and putting belly
in and out. Bending the trunk backward must mean rotation of the pelvis, enforced
by contraction of the belly muscles. Thus, belly dancing concerns sagittal and
frontal tilt of the pelvis, as was portrayed in the part on wheelchairs. However,
trained belly dancers are capable to use upper and lower parts of their rectus
abdominal muscles separately and by it, without bending their trunk, moving their
pelves [39]. It is fascinating to notice that in gerontology (study of aging), belly
dancing is considered advantageous for women. Compared to a control group, all
kinds of beneficial qualities emerge in older women concerning muscle strength
and balance [40]. For younger women, the Chinese research shows that female
posture, respiration, and cardiac function improved. Moreover, flexibility and
counterpoise, as well as effects on menstruation disorders get better [40]. The most
unexpected research on belly dancing concerns anthropomorphic robots. To create
robots that can imitate human flexibility of the spine, a model was developed that
can reproduce spinal movements that are present during belly dancing [41].
There exists a belly dance disease. It is characterized by myoclonus, which
belongs to the involuntary contractions of muscles. Myoclonus is defined as reg-
ularly appearing, involuntary, fast, abrupt, short-lasting contractions of a part of a
striated muscle, the whole muscle or group of striated muscles [42]. These con-
tractions can be on one side or both sides. They always are related to the brainstem
nuclei of the cerebellum (the so-called triangle of Guillain-Mollaret) [42] or to
damage of higher centers [43]. The effect is via the motoneurons of the spinal cord

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18.7 Belly Dancing and Pelvic Movements 445

toward the striated muscles and can also appear by medicines and/or poisoning. If
they are segmentally appearing, the abdominal rectus muscle can contract as belly
dancers do [43]. Moreover, this myoclonal belly dancers disease can also produce
rocking movement as during coitus, thus inducing pelvic and back and fro hip
movements [44].

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English title (1724) of Nader vertoog: New improvements in the art of midwifery. Shewing
I. The true causes of the most difficult births, the great abuse and prejudice of forcing pains
by medicines, and the best method of delivering women in such cases by the hand only,
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Chapter 19
Sphincters

Sphincters are controlled by both the somatic and the autonomic nervous system.
Still there is no clear interpretation for this interaction, especially due to the fact
that the muscle type of the sphincter can transform. The sphincter steering nucleus
in the spinal cord therefore, has properties that belong to both systems.

19.1 Introduction

Unfortunately, even the latest textbooks vary tremendously in their description of the
external urethral sphincter, most even neglecting to state that it consists of an inner smooth
and an outer striated muscle layer [1].

The urethral external sphincter has been described as a circular sphincter, a half
circular, or an arch-like one stretching its legs backward. Moreover, there is
considerable anatomical interspecies variation, which makes it impossible to
extrapolate animal results to humans.
The main cause of this problem in males is that around birth, there is still no
outgrowth of the prostate; which will eventually develop between the external
urethral sphincter (EUS) and the urethral wall. Therefore, the mature arrangement
differs entirely from the early postnatal one. In fact the, prostate will finally
encircle the urethra near its extension into the bladder neck. The internal, smooth
sphincter will stay circular, lying around the lower part of the urethra (the
membranous urethra); its anterior part being thicker than its posterior wall.
The external striated urethral sphincter has a superior extension that adheres to the
anterior prostate. The muscle fibers themselves are circumferential [2].
At the urogenital diaphragm, the posterior part seems to be connected to the m.
bulbospongiosus, the urethra being continuous into the bulb penis.

E. Marani and W. F.R.M. Koch, The Pelvis, 449


DOI: 10.1007/978-3-642-40006-3_19,  Springer-Verlag Berlin Heidelberg 2014

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450 19 Sphincters

19.2 Similarity of Sphincter Transformation

Sphincters are often found at the beginning or end of tracts: examples include the
anal, urethral, and esophageal sphincters. Sometimes, however, a sphincter is
found in the middle of a tract, e.g., the pyloric sphincter. Terminal sphincters are
mainly striated muscle sphincters and do have to contain peculiar structures. There
is accumulating evidence that developmentally programmed transdifferentiation
takes place in these sphincters. ‘‘Transdifferentiation is a relatively rare phe-
nomenon in which cells of one differentiated type and function switch to a second
discrete identity’’ [3]. In this way, smooth muscle can be transformed to striated
muscle during development. This occurs despite smooth muscle cells being
mononuclear, while striated muscular cells are fused multinuclear cells. The
esophageal sphincter transforms in this way during development, with expression
of smooth muscle-specific genes declining and the expression of striated muscle-
specific genes increasing.
In a discussion on the origin of smooth and striated muscle cells in the urethral
sphincter [4], the same mechanism is proposed for its striated component. The
periurethral mesenchyme should transform itself from the smooth type to the
striated type. The study of the expression of muscle markers in the intrinsic ure-
thral sphincter of the rat shows that this jump to another muscle type can occur [4].
Smooth muscle expression starts at day 14 after gestation. At birth, markers of the
striated expression start appearing in the urethral sphincter area, characterized until
then by smooth muscle properties. Coexpression of striated and smooth muscle
properties supports the idea of transformation.
Confirmation of the transformation from smooth to striated muscle types in
both esophagus and urethra shows that this may be a general phenomenon for
sphincter development. It could also explain the dual innervation of the urethral
sphincter, by both autonomic and somatic nerves [3]. While this idea is intriguing,
most neuronal connections are already present before birth and there are no
indications that the somatic innervation of the urethral sphincter arises around the
time of birth.

19.3 The External Anal Sphincter

It might be expected that sphincter anatomy, especially the anal sphincter anat-
omy, would be clear and not a matter of debate. Surprisingly, however, several
conceptions of the anatomy of the anal sphincter are currently offered (see
Fig. 19.1). This is also the case for the EUS (see Sect. 19.1). Subdivisions in
internal and external sphincters, the conception of a tripartite anal sphincter, and
the statement that there is in fact only one sphincter are all debated [5, 6].
However, most authors agree on the existence of a circular striated anal muscle.
This contains slow- and fast-twitch muscle fibers, fast-twitch fibers predominating

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19.3 The External Anal Sphincter 451

Fig. 19.1 View on the ampullar and anal area: a Naming and localization of structures.
b Venous plexus in and around the sphincter of the anus (red muscle, blue venous vessels).
c Collagen threads (black) around the anus set with smooth muscle fibers (b and c  E. Marani)

by 73 %. The intact circular striated muscle shows a constant contraction time for
varying strengths of muscle contraction. It is in this respect comparable to limb
muscles [6, 7]. During voluntary contractions, the contraction, time of the circular
striated muscle is estimated at 237 ms. If these contractions are initiated by
transcranial magnetic stimulation of the brain’s motor cortex, contraction time is
90 ms [7], indicating that cerebral control mechanisms can speed up the con-
traction time [8]. Since brain and anus are far apart, the conduction time of the
signal is also important. The conduction time in humans from cortex to the striated
circular anal sphincter is 19.4 ms [9].
So we can now understand flatulation, which is nearly always conscious. As gas
passes the lumen of the anus through the partially relaxed sphincter, we can close
the striated circular sphincter with our brain within tenths of seconds. This is fast
enough to maintain continence.
Much research concerning the anal sphincter has been and is done using animal
experiments. Consequently, one has to realize that what’s true for the animal is not
automatically true for humans. If we consider spinal cord injuries in laboratory
mammals, the striated circular sphincter has lost its contraction capacity up to 2 h
after the injury. By 48 h, the EMG of the striated circular sphincter is elevated and
above control animal level. This is called hyperreflexia and it is permanent. In
humans, the reverse happens. Instead of hyper reflexivity, relaxation occurs
leading to incontinence, after a spinal cord injury [8].

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452 19 Sphincters

The striated circular sphincter is easily damaged, especially by overstretching,


which occurs often during anal intercourse [10]. Overstretching of the striated
circular sphincter induces an ischemic zone of necrosis and an edematous zone of
necrosis in the striated circular muscle [11].
The same holds for conventional surgical approaches, which damage the stri-
ated circular sphincter [11].
Although the striated circular anal sphincter is a fast contractor, it is a lousy
relaxator, and therefore overstretching can easily occur.

19.4 The External Urethral Sphincter: Three Situations

Taking decisions is not so easy, especially in the medical field. A whole new
science has arisen to teach medical doctors to take medical decisions. One
approach is to show what the consequences of different decisions are for one and
the same medical treatment; or how things will develop if a patient is treated in a
different way. In this section, we will behave analogously. The EUS will be placed
in three situations—one normal and two extremes—and we will discuss the out-
comes [5].
Just before voiding, the decision to void is not yet been taken in our nervous
system. However, bladder pressure is increasing, and as a consequence the pres-
sure in the urethra has to be raised; otherwise, involuntary leakage will occur. As
long as the decision of voiding is not taken, the stimulating effect on Onuf’s
nucleus has to last, since this spinal nucleus is responsible for contraction of the
external urethral, and anal sphincters. Pressure increase in the bladder causes
receptors in urethra and bladder to fire with a higher frequency inducing stimu-
lation of Onuf’s nucleus and thus giving rise to extra contraction of the urethral
sphincter. As voiding commences, the brain and brain stem increase the inhibitory
action on Onuf’s nucleus. Increased pressure of the bladder will overcome the
decreasing closure of the EUS, and voiding will start.
How fast is this decision-taking act of the brain and brain stem? There are two
ways of setting urinary tract in a state, which permits study of the decision-taking
process, namely coughing, and an unexpected rise of the abdomen pressure, such
as results from a sudden push in one’s belly.
The urologist and gynecologist test continence by the use of coughing. Before
coughing, the brain and brain stem will naturally increase the stimulation effect on
Onuf’s nucleus in anticipation of the coughing situation. Coughing will increase
bladder pressure, which in turn will cause leakage if the precough urethral pressure
is maintained. Increasing the urethral pressure will prevent leakage.
Coughing can be carried out while at the same time, a pressure urethral catheter
is checked. Inadequate pressure adaptation can be a sign that a nervous disturbance
is involved in incontinence.
A sudden hard push in one’s belly will increase abdominal pressure, which will
increase the bladder pressure. Since the push is unexpected, neither brain

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19.4 The External Urethral Sphincter: Three Situations 453

stimulation nor brain inhibition on any part of the uropoetic tract can be expected.
So Onuf’s nucleus cannot anticipate. Bladder pressure will rise without enough
counter pressure of the urethral sphincter causing urine leakage.
The pressure rise caused by the push arises within 30 ms; by coughing in nearly
100 ms; and the voiding change in normal situations is organized within 50 ms,
due to its reflex-like character.
One has to conclude that although the decision taking is fast, there are life
situations involving the EUS, for which the decision is nevertheless taken too
slowly.

19.5 Modeling the Sphincters

Morphology and functions of the anal and the EUSs are hard to understand.
Consequently, one approach for gaining insight into the consequences of the
structure and its function is to make a model. Using a model, one can check
the prescribed parameters to see whether they produce the same outcome as the
sphincter gives. If not, one can change the values of the parameters or expand the
model by adding other parameters. By trial and error and repeated modifications,
one can thus generate a realistic model.
A series of sphincter models have been developed the last 25 years, which can
be subdivided into simple sphincters with only an on/off switch for urethral
function, sphincters comprising a single muscle fiber, and multi muscle fiber
sphincters. Sometimes, the sphincter function is attributed to the whole urethra, or
alternatively special sphincter in the urethra is modeled.
The function of sphincters has to be coordinated with the opening, relaxation, or
closure of other units such as bladder or rectum. For the steering of sphincters, an
open or closed loop of neuronal connections has been modeled.
The first sphincter model steered by a realistic closed loop neuronal system was
developed by Hosein and Griffiths [12]. In this model, the urethra contained
sphincter properties, which could be guided by a balanced system of neuronal
connections. However, the sphincter itself could only be in a contracted or in an
uncontracted state. Based on neuroanatomical research, the connectivity between
the artificial nuclei approached reality. However, the interplay between a short
neuron system and the spinal cord was not modeled. Supraspinal relay stations
were incorporated, mainly based on the results gathered by Holstege and Griffiths
[13]. Prior to this model, simple electrical and simple mathematical descriptions
were published [14, 15], which, however, we will not discuss.
In the following 10 years, more sophisticated models have been developed
[16-21]. In most models, a Hill equation was used for the muscle function. The
Hill equation is a mathematical approach, which includes both a contractile and an
elastic element. If the contractile element does not work, the passive elastic
properties of the muscle are still present. It has become apparent that this equation

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454 19 Sphincters

is a realistic description of the behavior of the contractile elements actin and


myosin of the muscle fiber (see [22]).
In general, these models comprised a muscular part of the urethra, with
sphincter action, and adding to this a neuronal steering mechanism. Even the finite
element method was used solely to model the muscular sphincter compartment.
Nevertheless, a two-component model containing a realistic sphincter steering
system and a realistic neuronal steering system is still lacking. Although bladder
function has been realistically modeled in several models, the sphincter remains a
poorly modeled area.
Initial efforts were directed describing a realistic lower urinary tract with
emphasis on the bladder musculature and a simple on/off switch for the sphincter
[16, 17]. Current efforts are, in order to reduce the extension of the problem,
directed toward the modeling of the sphincter and its specific neuronal steering,
which is relayed by Onuf’s nucleus.
The modeling of several circular layers of muscle fibers around a lumen, with
each fiber guided by Onuf’s motoneurons, has shown that by cutting the inner-
vation of small parts of the modeled sphincter, severe dysfunction of the total
sphincter occurs [22].
This dysfunction in the model coincides remarkably well with anal sphincter
dysfunctions, such as are present following partial rupture of the sphincter mus-
culature or overstretching of the anal sphincter (see Fig. 19.2) [22].
Modeling of a realistic sphincter indeed shows that minimal damage can result
in severe dysfunction of the sphincter.
Moreover, the modeled results show that the tension generated in the entire
sphincter muscle will be the sum of the tension of all the active motor units of that
muscle. This leads to the conclusion that damage however small, to muscle fiber
units themselves or to their innervation, leads to loss of sphincter function. This
causes leakage and thus dysfunction of the mechanical valve-like function of a
sphincter [22].

19.6 Onuf’s Nucleus

Bronislaw Onufrowicz (1863–1928) observed this nucleus in 1899 in the human


sacral spinal cord. It was restricted to the first, second, and third sacral spinal cord
segments. Early discussions, following the initial (1899) paper, were centered on
whether the nucleus was a sympathic or a parasympathic structure. In 1977, the
nucleus was rediscovered, because of its connection with the preservation of
bladder-rectal functions in Amyotrophic Lateral Sclerosis (ALS). Since it was
shown that Onuf’s nucleus innervates small striated pelvic muscles, including the
anal and urethral sphincters, a somatic character was attributed to this nucleus.
This confusion is understandable since it was only later that transdifferentiation of
smooth muscle cells into striated muscle cells was discovered (see Sect. 19.2).

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19.6 Onuf’s Nucleus 455

Fig. 19.2 Modeling the anal


sphincter. At the right side,
the normal anal sphincter
situation is depicted for the
active state, fiber strain,
pressure, and fiber stress. At
the left side the situation after
partial de-innervation of the
anal sphincter is depicted for
the same parameters.
(Reproduced with
permission, courtesy
M. Heldoorn [25])

The autonomic character of the motoneurons of Onuf’s nucleus was indicated


by two lines of evidence. First that Onuf’s nucleus did not degenerate in Werdnig-
Hoffman disease, healed poliomyelitis, Duchenne’s muscular dystrophy, spinal
muscular atrophy, and ALS.
Second that while other somatic sacral motoneurons degenerated, and that in
Shy-Drager Syndrome, Fabry’s disease and multiple system atrophy both Onuf’s
nucleus and the parasympathic nucleus degenerate, somatic sacral motoneurons
were spared.
Even today, the debate over whether Onuf’s nucleus is sympathic, parasym-
pathic and/or somatic (or does not belong to one of these categories) continues.
The nucleus can be subdivided longitudinally in two parts. These are a
dorsomedial group, innervating the anal sphincter, and a ventrolateral group for the
innervation of the striated urethral sphincter. The nucleus also displays a sexual
dimorphism regarding motoneuron size and numbers.

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456 19 Sphincters

Although Onuf’s nucleus is small, it is very interesting one. The motoneurons


of Onuf’s nucleus are responsible for the continued contracted state of the muscle
fibers of the pelvic sphincters. The dendrites of Onuf’s nucleus are parallel aligned
and are electrotonically coupled [22, 24]. Incoming unmyelinated axons possess
the same coupling with dendrites. Moreover, typical specializations of double-
membrane foldings (crest synapses) between several dendrites and one incoming
axon can be present. Up to five dendrites can be related to one axon in humans.
Seemingly, incoming information is transferred to several dendrites, which are
electronically coupled to other dendrites. So both reflex information and brainstem
information will spread enormously through the nucleus, activating a whole set of
motoneurons which will fire and cause contraction of the striated muscle fibers in
the sphincter.
The motoneurons of Onuf’s nucleus possess extra properties, to increase their
tonic activity in the closure of the sphincters. The membrane input resistance is
low and after-hyperpolarizations are shorter, indicating that action potentials can
be readily caused and the interval between two action potentials can be very short.
Due to the fact that a side branch of Onuf’s motor axon can excitate, while
normally this recurrent axon collateral causes inhibition in moterneurons, fre-
quency of action potential train can be enhanced, and the duration prolonged.
The most recent discovery concerns a phenomenon called plateau potentials,
which increases the motoneuron exicitability [25]. So, Onuf’s nucleus contains
structural adaptation and motoneuron adaptations, all in order to maintain optimal
firing rates and force generation needed for sphincter closure.
A minimum of input to Onuf’s nucleus will cause a maximum of output toward
the sphincters.
Due to the fact that synaptic transmission is not used, milliseconds are gained
by the velocity of Onuf’s answer. Synchronized activation of neurons increase the
amplitude of the spikes generated by the neurons. Consequently, sensory infor-
mation input cause and amplify a rapid increase in motoneuron firing, inducing a
fast, strong contraction of the sphincters.

19.7 Sphincter Problems

19.7.1 Internal Urethral Sphincter (Smooth Muscular


Sphincter or Lissosphincter)

Pages are spent on urethral sphincters without a clear solution. This holds for both
the smooth and the striated urethral sphincter. The urethral sphincter studies, but
also the bladder studies, started two centuries ago in both German and Anglo-
Saxon scientific circles. The main results were collected in Von Bardeleben’s
German ‘‘Handbook of Human Anatomy’’ around 1900 and in the Journal of
Anatomy and the Journal of Anatomy and Physiology by Berry Hart (1901),

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19.7 Sphincter Problems 457

Griffith (1889, 1891), and Le Gros Clark (1883) to name the most important
Anglo-Saxon authors [1]. The restricted embryological studies of that time, but
also the research on mature specimens, showed a series of controversies that still
continues in modern time [26].
The discussion on the smooth internal urethral sphincter can roughly be sub-
divided in those authors that deny a smooth muscle sphincter and another group
that states its presence, but gives different compositions of its structure [26]. The
presence of a striated sphincter is generally accepted. However, its form is
debated. The confusion is enlarged by the gender differences of the urethra and the
presence of the prostate in males [26].
Serious efforts have been made to solve this entanglement. Two researchers
should be named: John DeLancey from the Department of Obstetrics and Gyne-
cology of Ann Arbor’s Women’s Hospital and John A. Gosling first at the
Anatomy Department of the Manchester School, later on in Hong Kong, and
Stanford University School. Both contributed by their clinical and anatomical
human research.
The structural blow for the non-believers in a smooth urethral sphincter came in
1972. The author Dröes, in his Leiden thesis, used fetal human specimens in which
he could discern detrusor smooth muscle, smooth muscle of the trigone and
smooth muscle of the urethra, and of course the striated muscle (Fig. 19.3) [26].
This result was confirmed several times in literature up to recently (2004) [2],
although small deviations of the main results have been described. Nevertheless,
the core three smooth muscle parts could be upheld [27].
These results by it self do not prove that a smooth urethral sphincter is func-
tioning, but the presence of its substrate in the urethra has been established. The
smooth musculature of the urethra contains an inner longitudinal layer and an
outer circular one [26, 27]. Till today, a good explanation of the function of the
longitudinal layer is missing. The circular layer extends over a large part of the
urethra in both sexes. It is rather a tube than a small ring, which is what one thinks
by the word sphincter. The measuring of the pressure over the tube shows that it is
at largest in the middle. So, there is a pressure gradient over the muscular urethral
tube. This property also of the smooth musculature of the urethra stays a puzzle.
In 1975, a glyoxylic acid method came available for the easy detection of
catecholamines. It was fast and reliable contrary to the Falck-Hillarp method,
which was restricted in its use. Due to the fast glyoxylic method, the presence and
distribution of noradrenaline in the human trigone and urethra could be established
(Fig. 19.4). The receptor for noradrenaline was determined to be the alpha
adrenergic receptor that supported the closure of the urethra. Beta adrenergic
receptors were detected in the bladder, which inhibit detrusor activity. The sym-
pathic catecholamine positive neurons were also present in the juxtamural and
intramural ganglia. The sympathic system does inhibit contraction of the bladder
and enhances contraction of trigone, and urethra was the outcome of research
(Fig. 19.4) [28]. Stress incontinence could be reduced by alpha adrenergic ago-
nists. It is restricted prescribed due to its negative effects on other systems. Thus
the closure activity of the urethra could pharmacologically be enhanced, indicating

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458 19 Sphincters

Fig. 19.3 Dröes [26] results in overview: Left upper figure shows direction of lower sections,
green ureter, brown adrenergic innervated area of bladder and urethra, right upper figure is a
reconstruction of smooth muscle cell layers in the male, lower three figures are sections (from left
to right) through the female frontal pelvis at 8 cm crown-rump length (crl), female pelvis at
11 cm crl, and female pelvis at 20 cm crl. Abbreviations centrum tendineum (ct), m.detrusor (d),
dorsal plate of sinus urogenitalis (dp), striated (du) and smooth (gu) urethramusculature, muscles
of rectum (r), m.sphincter ani (sa), vagina (v), ventral trigone (vt). Upper arrow dorsal circular
area of vesical trigone, middle arrow dorsal part of trigonal ring together with trigonal plate,
lower arrow area of urethra back side not covered with trigonal tissue. (Figures are reproduced
with permission and courtesey J.Droës)

that the smooth urethral musculature did have a sphincter function, which was also
supported by physiological results [28].
Some more light has been shed recently on bladder and urethral sphincter
problems by the discovery of the presence of the interstitial cells of Cajal in the
urinary tract. These cells were discovered by Ramon y Cajal, at first in the mus-
culature of the gut and later in other organs like the heart and the pancreas. Cajal
met serious criticism and scientists hardly believed his results. Not earlier than in
the 1970s, the situation changed due to the use of the electron microscope.
Nowadays, the interstitial cells are accepted as a morphological entity and are
characterized by electron microscopy, some populations by immunocytochemis-
try. Moreover, the cells can be brought into culture. These interstitial cells of Cajal
are the intermediates between the smooth muscle cells and the autonomic fibers, as
Cajal already stated. They organize the rhythmic contractions of the gut muscles
and therefore are characterized as pacemaker cells for the gut musculature [29].

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19.7 Sphincter Problems 459

Fig. 19.4 Schematic overview of spinal efferents for bladder and urethra. - inhibition, ? exci-
tation, adrenergic receptors (aa), adrenergic receptors (bb), cholinergic receptors (ach), detrusor
(d), external urethral sphincter (eus), ganglion mesentericum inferior (gmi), lumbar spinal cord
(lms), hypogastric nerve (nh), nervus pelvicus (np), nervus pudendus (npu), plexus pelvicus (pp),
spinal ganglion (sg), sacral spinal cord (sms), truncus sympathicus (ts), trigonum vesicae (tv),
vasoactive intestinal peptide receptors (vip) (reproduced with permission from Bastiaanssen,
Marani and Van Leeuwen [28])

We leave out here the discussions on interstitial cells and interstitial-like cells
or telocytes, doing injustice to those scientists that try to pinpoint the different
types of cell populations involved.
The idea of pacemaker cells has been brought forward by John Gosling and
his group in studies on the kidney-ureter transitional area already in 1972.
Studying the musculature of the pyelo-ureteric area, they discovered that beside
smooth muscle cells, there is another type of cell present to which they attributed
a pacemaker function. Now, we know that they are the interstitial cells of Cajal.
The whole trajectory kidney–ureter–bladder–urethra contains these cells and
function as intermediates between the autonomous nervous system and smooth
muscles [29].
Here, we focus on the urethra. The tone of the urethral smooth muscle is
contributing to urine continence. In the absence of neurotransmission, the tone is
held. However, most of the muscle cells themselves are not electric active. So, an
intermediate is responsible for keeping the tone of the urethral musculature: the
interstitial cells of Cajal. Electrophysiological and morphological studies show
that the interstitial cells are present over a large urethral area, forming a network,
and single-cultured interstitial cells showed pacemaker properties. The pacemaker

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460 19 Sphincters

Table 19.1 Use of antimuscarinics and a-blockers in urinary incontinence


Urinary incontinence in children Detrusor overactivity Antimuscarinics
Voiding dysfunction a-blockers, antimuscarinics
Urinary incontinence in men Urge incontin./ a-blockers, antimuscarinics
detrusoroveract
Urge incont./outlet obstruct a-blockers, 5a reductase inhibit
Urinary incontinence in women Urge incont/overact bladder Antimuscarinics
Neurogenic urinary Overactive bladder Antimuscarinics
incontinence
Taken from Fourth international consultation on incontinence. Recommendations of the inter-
national scientific committee. Neurourology and urodynamics 29:213–240 (2010)

properties are based on calcium ion concentrations: the absence of calcium stops
pacemaker activity, low calcium concentration gives slow pacemaker function and
high calcium concentrations are related to high pacemaker activity. Moreover, the
urethral interstitial cells can be modulated in their activity by noradrenaline and
nitric oxide via the calcium system [29].
If we compare the network of interstitial cells within the urethra with elastic
stockings that can contract, the middle of the stocking will deliver the largest
contraction, as we saw in the urethra (due to the enforcement from edge to the
middle).
The clinical significance has yet to be determined, but ‘‘It has been reported that
increased numbers of interstitial cells of Cajal-like cells are found in bladder tissue
in patients who suffer from ‘over-active’ bladder’’ [29A] (urge incontinence).
Seemingly, both stress and urge incontinence can presumably be reduced to
dysfunction of the interstitial cells of Cajal.
Till now, only the pharmacons [30] that inhibit muscarine receptors and block
alpha adrenergic receptors are considered effective (see Table 19.1, taken from the
international recommendations). However, the first cracks in the classical concept
for urinary incontinence are appearing due to research on urinary incontinence in
children, other neurotransmitters and receptors are as important, and the search for
the function of the interstitial cells of Cajal, indicating another functional concept.

19.7.2 External Urethral Sphincter (Striated Muscular


Sphincter or Rhabdosphincter)

The problems with the striated muscular urethral sphincter start already in
embryological studies. Sebe et al. proposed one origin of both striated and smooth
urethral sphincters: ‘‘The female rhabdosphincter and lissosphincter have a com-
mon sphincter urethrae primordium that consists of a myoblast plate located in the
anterior aspect of the urogenital sinus’’ [31A]. Van der Putte in his description of
the perineum development found a separate smooth and striated sphincter origin.

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19.7 Sphincter Problems 461

The striated sphincter is bilateral in origin, but fuses to one sphincter: ‘‘An outer
layer revealing a transverse texture on the ventral side shows early smooth muscle
cell differentiation adjacent to the superficial urogenital sinus and forms the earliest
anlage for the internal urethral sphincter. A bilateral concentration of dense tissue in
that same area fuses ventrally and forms the anlage for the striated EUS’’ [31B].
The form of the external striated sphincter is also debated: ‘‘it still remains a
subject of confusion, since different configurations such as omega, ring and
elliptical shapes are described’’ [31A]. This sphincter can be divided in three parts
[32] in the female or considered one structure in the male by Oelrich [8]. The last
author divides the female urethral sphincter in two parts [32]. One can go on and
on: there is no agreement in the older literature. The most eloquent study on the
mature bladder neck and urethra is Dorschner’s [32], but it brought up a lot of
discussion, hardly contributing to a general concept.
A totally different concept is given by DeLancey and coworkers: ‘‘The female
urethra is composed of different regions along its length and can be understood by
dividing the length of urethral lumen into fifths, each approximately 20 % of the
total length. In the first quintile, the lumen of the urethra is surrounded by
the vesicle neck (0–20 %). Next, the sphincter urethra and smooth muscle encircle
the lumen from 20 to 60 % of the total urethral length. The arch-shaped com-
pressor urethra and urethrovaginal sphincter are found from 60 to 80 % of the total
urethral length, whereas the distal component includes only fibrous tissue and no
significant contractile elements’’ [32].
Similarities in function are generally recognized: ‘‘Traditionally continence is
thought to result from the presence of dual sphincteric mechanisms in both sexes, an
external or distal sphincter composed of striated muscle and an internal or proximal
sphincteric mechanism at the bladder neck, composed of smooth muscle’’ [33].
Thus a striated EUS exists, but its form is debated also caused by the gender
differences. Its function contributes to mid-urethral increase in pressure [33].
What then characterizes histologically the striated urethral sphincter? The first
fact is the smaller muscle fibers, in between a mean of 15 and 20 l Fiber typing
showed that various species contain different striated urethral muscle fiber types,
indicating that the composition of the muscle is different and animal results can
hardly be converted into human ones. The second fact is the typical fiber typing of
the human striated sphincter: both type 1 and type 2 fibers are present. Type 1 is
oxidative, fatigue-resistant and is called slow twitch fiber. Type 2 is glycolytic,
fatigue-sensitive and called fast-twitch fibers. The estimated percentages of each
of the fibers in the striated urethral sphincter are individually different, and this is a
human specific characteristic, while in human skeletal muscle, their proportions
are rather constant. ‘‘The presence of both types of fibers in the urethral sphincter
suggests that this muscle is adopted to serve a dual function, the type 1 fibers being
involved in the maintenance of continence at rest, while type 2 fibers are activated
during stress conditions. The results of the volumetric measurements of type 1 and
type 2 fibers indicate that the urethral sphincter might have an approximately equal
capacity of both functions’’ [33A]. However, one can find in literature papers that

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462 19 Sphincters

indicate that only type 1 fibers or only type 2 fibers are present [34]. The difference
depends on the technique used.
In this respect, DeLancey and coworkers remark on aging is noteworthy: ‘‘With
increasing age, striated muscle loss at the bladder neck and along the dorsal wall of
the urethra has been found. This leads to a horseshoe-shaped aspect of the striated
muscle layer in the midurethral cross section’’ [31A], explaining at least some of
the anatomical differences found (the use of young material versus older), but also
indicating that proximal muscle fibers are vulnerable to aging or they are of a
different composition.
The knowledge of the muscle cell types and of the loss of striated muscle fibers
advances tissue engineering. The more so, if it is possible that ‘‘transdifferentiation
of smooth to striated muscles occurs in the developing genitor-urinary tract’’ [35].
It is a controversial discovery and transdifferentiation should normally be lost
during further growth. Stem cells have been incorporated into the lesioned urethra,
but stem cells alone do not repair the damage. Only if collagen or other supporting
substances are added, partial recovery of the muscle layer of the urethra is noticed.
The research focuses on other cell types and scaffolds or combination of both.
Stem cell-derived myoblasts, autologous or in combination with fibroblast, are
injected in the urethra, and increase in sphincter tone and induction of regeneration
of the urothelium/mucosa has been reported [35]. Adipose-derived stroma cells are
another urethral approach. Scaffolds are brought to the clinic, but cell-seeded
scaffolds or cell types alone not [35]. The original urethral stem cell euphoria made
room for more careful approaches, extended animal research, and restrictions for
the use of embryological stem cells. Nevertheless, the outlook for positive results
still resounds in review articles. However, ‘‘Until now, all published studies have
been non-randomized, open studies, demonstrating a remarkable clinical
improvement in most of the patients treated’’ [35A].
The pelvic sphincters with their reflex arches relayed over Onuf’s nucleus and
its input from higher brain and brainstem centers is an intriguing area of research.
The research concerns the anatomy and the physiology of the pelvic sphincters,
which is enforced by the recently discovered transformation of the sphincter’s
nature around birth. Modeling will probably give answers concerning function
and dysfunction of sphincters while extended research on Onuf’s nucleus will
contribute to the understanding of the neuronal steering mechanisms of the pelvic
floor sphincters.

Literature

Literature has been grouped in reference lists of several chapters in those cases where
arguments are difficult to entangle or published over several articles or books. In cases of
citation the article or book involved is indicated by the reference number together with a
capital Arabic letter.
1. Kaye KW, Creed KE (1997) Anatomy and innervation of the external urethral sphincter.
Dialogues in Ped Urol 20:3–4

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2. Droës TTPM (1972) De musculatuur van blaas en urethra in de menselijke foetus. Thesis
Leiden, The Netherlands
3. Patapoutian A, Wold BJ, Wagner RA (1995) Evidence for developmentally programmed
transdifferentiation in mouse esophageal muscle. Science 270:1818–1820
4. Baskin LS, Borirakchanyvat S (1997) Studies on the origin of smooth and striated muscle
cells in the intrinsic urethral sphincter. Dialogues in Ped Urol 20:2–3
5. Herdmann J, Enck P, Zacchi DP, Ostermann U (1995) Speed and pressure characteristics
of external anal sphincter contractions. Am J Physiol 269:G225–G231
6. Krier J, Adams T, Meyer RA (1988) Physiological, morphological and histochemical
properties of cat external anal sphincter. Am J Physiol 255:9772–9778
7. Holmes GM, Rogers RC, Bresnahan JC, Beattie MS (1998) External anal sphincter
hyperreflexia following spinal transection in the rat. J Neurotrauma 15:451–457
8. Jost WH, Schimrigte K (1994) A new method to determine pudendal nerve motor latency
and central motor conduction time to the external and sphincter. Electroencephalogr Clin
Neurophysiol 93:237–239
9. Jost WH, Ecker KW, Schimrigte K (1994) Surface versus needle electrodes in
determination of motor conduction time to the external anal sphincter. Int J Colorectal
Dis 9:197–199
10. Li L, Zhang JL, Ju GW, He GR, Lui XH (1996) Damaging effects of anal stretching on the
external anal sphincter. Dis Colon Rectum 39:1249–1254
11. Hosein RA, Griffiths DJ (1990) Computer simulation of the neural control of bladder and
urethra. Neurourol Urodyn 9:601–618
12. Holstege G, Griffiths DJ (1990) Neuronal organization of micturition. In: Paxinos G (ed)
The human nervous system. Academic Press, Waltham, pp 297–306
13. Fröhlich J, Nádvornik P, Neuschl S (1977) Computermodell der Harnblase. Zentralbl
Neurochir 38:291–298
14. Drolet R, Kunov H (1975) On the peripheral bladder control system of the dog and
urodynamics: in vivo characterisation and hybrid computer simulation. Med Biol Eng
13:40–55
15. Bastiaanssen EHC (1996) The neural control of the lower urinary tract: modelling and
simulation. Leiden University, Leiden
16. Bastiaanssen EHC, Vanderschoot J, Van Leeuwen JL (1996) State-space analysis of a
myocybernetic model of the lower urinary tract. J Theor Biol 180:215–227
17. Usui S, Hirata Y (1995) Estimation of autonomic nervous activity using the inverse
dynamic model of the pupil muscle plant. Ann Biomed Eng 23:375–387
18. Van Duin F, Rosier PF, Bemelmans BL, Debruyne FM, Wijkstra H (1999) A computer
model for describing the effect of urethral afferents on simulated lower urinary tract
function. Arch Physiol Biochem 107:223–235
19. Van Duin F, Rosier PF, Rijkhoff NJ, Van Kerrebroeck PEV, Debruyne FMJ, Wijkstra H
(1998) A computer model of the neural control of the lower urinary tract. Neurourol
Urodyn 17:175–196
20. Gielen AWJ (1998) A continuum approach to the mechanics of contracting skeletal
muscle. Thesis Technische Universiteit Eindhoven
21. Heldoorn M, Van Leeuwen JL, Vanderschoot J (2001) Modelling the biomechanics and
control of sphincters. J Exp Biol 204:4013–4022
22. Sasaki M (1991) Membrane properties of external urethral and external anal sphincter
motoneurons in the cat. J Physiol 440:345–366
23. Sasaki M (1994) Morphological analysis of external urethral and external anal sphincter
motoneurons of cat. J Comp Neurol 349:269–287
24. Paroschy KL, Shefchyk SJ (2000) Non-linear membrane properties of sacral sphincter
motoneurons in the decerebrate cat. J Physiol 523(3):741–753
25. Heldoorn M, Van Leeuwen JL, Vandersloot J (2001) Modelling the biomechanics and
control of sphincters. J Exp Biol 204:4013–4022

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26. Dröes JTPM (1972) De musculatuur van blaas en urethra in menselijke foetus. Thesis
University Leiden; Dröes JTPM (1974) Observations on the musculature of the urinary
bladder and the urethra in the human fetus. BJUI 46:179–185
27. Koide T, Okuyama A, Mizutani S, Sonoda T (1979) Muscular development of the bladder
neck in the human fetus. Invest Urol 17:50–54; Gilpin SA, Goslin JA (1983) Smooth
muscle in the wall of the developing human urinary bladder and urethra. J Anat
137:503–512; Yucel S, Baskin L (2004) An anatomical description of the male and female
sphincter complex. J Urol 171:1890–1897
28. Furness JB, Costa M (1975) The use of glyoxylic acid for the fluorescence histochemical
demonstration of peripheral stores of noradrenaline and 5-hydroxytriptamine in whole
mounts. Histochem 41:335–352; Falck B, Hillarp NA, Thieme G, Thorp A (1962)
Fluorescence of catecholamine and related compounds condensed with formaldehyde.
J Histochem Cytochem 10:348–354; Klück P (1982) Over de zenuwvoorziening in de
wand van de lagere urinewegen van de mens. Thesis, Leiden University; Wilkinson R
(1986) The role of the sympathetic nervous system in the lower urinary tract. Clincal Sci
70(S14):1s–81s; Bastiaanssen EBC, Marani E, Van Leeuwen JL (1991) Anatomie en
fysiologie van de lage urinewegen. In: Cools HJM, de Graaff WJ, Marani E (eds) Urine-
incontinentie van jong tot oud. Boerhaave Cursus. ISBN 90-6767-213-0
29. Lang RJ, Klemm MF (2005) Interstitial cell of Cajal-like cells in the upper urinary tract.
J Cell Mol Med 9:543–556; Gosling JA, Waas AN (1971) The behaviour of the isolated
rabbit calix and pelvis compared with that of the ureter. Eur J Pharmacol 16:100–104;
Gosling JA, Dixon JS (1972) Structural evidence in support of a urinary tract pacemaker.
Brit J Urol 44:550–60; Dixon JS, Gosling JA (970) Electron microscopic observations on
the renal caliceal wall in the rat. Z Zellforsch Mikrosk Anat 103:328–340; Gosling JA,
Dixon JS (1971) Morphologic evidence that the renal calyx and pelvis control ureteric
activity in the rabbit. Am J Anat 130:393–408; Dixon JS, Gosling JA (1973) The fine
structure of pacemaker cells in the pig renal calices. Anat Res 175:139–53; Sergeant GP,
Hollywood MA, McHale NG, Thornbury KD (2006) Ca2+ signaling in urethral interstitial
cells of Cajal. J Physiol 576.3:715–720; Popescu LM, Faussone-Pellegrini M-S (2010)
Telocytes—a case of serendipity: the winding way from interstitial cells of Cajal (ICC) via
interstitial Cajal-like cells (ICLC) to telocytes. J Cell Mol Med 14:729–740; Huizinga JD,
Faussone-Pellegrini M-S (2005) About the presence of interstitial cells of Cajal outside the
musculature of the gastrointestinal tract. J Cell Mol Med 9:468–473
29A. Sergeant GP, Thornbury KD, McHale NG, Hollywood MA (2006) Interstitial cells of Gajal
in the urethra. J Cell Mol Med 10:280–291
30. Andersson K-E (2000) Drug therapy for urinary incontinence. Baillière’s Clin Obstet
Gynaecol 14:291–313; Khullar V, Cardozo L (1995) Drugs and the bladder. Curr Obstet
Gynaecol 5:110–116; Bael A et al EBDS (2008) The relevance of urodynamic studies for
urge syndrome and dysfunctional voiding: a multicenter controlled trial in children. J Urol
180:1486–1493
31A. Sebe P (2005) Fetal development of the female external urinary sphincter complex: an
anatomical and histological study. J Urol 173:1738–1742; van der Putte SCJ (2005) The
development of the perineum in the human. Adv Anat Embryol Cell Biol 177:1–135
31B. Perucchini D, DeLancey OL (2008) Functional anatomy of the pelvic floor and lower
urinary tract. In: Baessler K et al (eds) Pelvic floor re-education. Part I, 1.1:3–21;
Dorschner W, Stolzenburg J-U, Neuhaus J (2001) Structure and function of the bladder
neck. Adv Anat Embryol Cell Biol 159:1–109; Oelrich TM (1980) The urethral sphincter
muscle in male. Am J Anat 158:229–246; Oelrich TM (1983) The striated urogenital
muscle sphincter in the female. Anat Record 205:223–232
32. Brading AF (1999) The physiology of the mammalian urinary outflow tract. Exp Physiol
84:215–221
33. Tokunaka S, Okamura K, Fujii H, Yachiku S (1990) The proportions of the fiber types in
the human external urethral sphincter: electophoretic analysis of myosin. Urol Res
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33A. Schrøder HD, Reske-Nielsen E (1983) Fiber types in the striated urethral and anal
sphincter. Acta Neuropathol (Berl) 60:278–282
34. Emanuel M (1972) Mechanomyography of the external urethral sphincter. J Urol
107:795–801; Gosling JA, Dixon JS, Critchley HOD, Thompson S-A (1981) A
comparative study of the human external urethral sphincter and periurethral levator ani
muscles. Br J Urol 53:35–41
35. Borirakchanyavat S, Baskir LS, Kogan BA, Cunha GR (1997) Smooth and striated muscle
development in the intrinsic urethral sphincter. J Urol 158:1119–1122
35A. Tedesco FS (2010) Repairing skeletal muscle: regenerative potential of skeletal muscle
stem cells. J Clin Invest 120:11–19. doi:10.1172/JCI40373; Orabi H, AbouSchwareb T,
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G, Daum L, Amend B et al (2011) From tissue engineering to regenerative medicine in
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Zheng X, Jiang Z (2011) Adipose-derived stroma cell transplantation for treatment of
stress urinary incontinence. Tissue and Cell 43:246–253

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Chapter 20
Catheters

Although catheters were already in use in antiquity, its use in the Western world
begins not earlier than at the start of the seventeenth century. Prolonged cathe-
terization induces bacterial bladder infections. Once infected, bacteria have
ingenious methods to mark their footsteps for their followers. Party drugs like
ecstasy, speed, and ‘‘special K’’ can have dreadful effects on bladder function.
Cannabis is dealt in relation to sexual function.

20.1 History of Catheters

Catheters from 2000 years ago have been found in Pompeii and were described as
being used during stonecutting operations in Rome. The first flexible catheter was
developed by J. B. van Helmont in 1659 [1]. Van Helmont used a linen ribbon,
treated with linseed oil, and wound it around a small tube. In the nineteenth
century, Nélaton rediscovered the method. Later on, he used vulcanized caou-
tchouc. This is in a nutshell the history of catheters.
More narrowly, the development of the bendable catheter can be seen as a
struggle taking place over several centuries [1]. Let us start with Van Helmont. He
was in fact a chemist and was interested in bladder stones. He was born in Brussels
in 1577 or 1580—historians disagree. He died in 1664 in Brussels or Vilvoorde in
Belgium, formerly Flanders. Boerhaave called him the most famous chemist of his
time. Van Helmont studied medicine in Louvain until 1594. Losing interest, since
the doctors of those days could neither diagnose nor apply adequate therapy, he
started to study the Kaballa. It was lessons given by Martin Del Rio which
encouraged him to look in this (Jewish) system of occult theosophy or mystical
interpretation of the Scriptures. Not satisfied with it, he went on to study mystics
such as Thomas à Kempis (1379–1471) and Johan Tauler (1290–1361). Then, he
withdrew from university circles and started his own chemistry laboratory. He kept
himself busy with chemistry and after a while became well known in the scientific
circles inside and outside his own country.

E. Marani and W. F.R.M. Koch, The Pelvis, 467


DOI: 10.1007/978-3-642-40006-3_20,  Springer-Verlag Berlin Heidelberg 2014

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468 20 Catheters

In 1660, four years before his death, he published a book: ‘‘Dageraad of te


nieuwe opkomst der geneeskunst’’ (Dawn or the new rise of medicine). The first
chapters contained a philosophical treatment of medicine, and there followed a
series of chapters on bladder stones and the pestilence. Hidden in the part on
bladder stones, somewhat more than half a page is devoted to the flexible catheter.
A loose translation is as follows: ‘‘I saw that urine came out using a bent silver
small funnel, at the inner side stiffened by a silver wire. This application is very
painful, and produced a lot of blood, and often did not reach the bladder, it is
named the catheter. I investigated several substances, and in the end I found no
better one than something which is easily bent and can be brought in without pain.
I took a small strong linen ribbon with linseed oil and doped with a solution of
lead oxide, which varnishes the strip on both sides well. Then one winds the band
around a copper wire very flat. The tube can be made as long as one needs. Then
one again varnishes it on its outside with linseed oil. One stiffens it around a needle
of whale bone. This catheter is flexible and can be brought in hundred times a day
if necessary, reaching through the bladder sphincter, the needle is taken out and
one puts on it the syringe and in this manner the bladder empties. Catheters for
women can be short and rough, because the closure of the bladder is near the
surface. One calls it Dyoptrismum, I don’t bother about the different names.’’
The part between   was omitted in the article of Moonen [1], but it shows
that the different localization of the urethral sphincter was known. However, the
approach can hardly be called women-friendly.
The Dutch have claimed that the flexible catheter is an invention of the Low
Countries, unhappily forgotten. However, the statement is disputable.
Avicenna (980–1037) was the first to make flexible catheters from animal skin
coated with salves [1]. In the second half of the fifteenth century, Arcolano
described a flexible parchment catheter, as did Fabricius in the sixteenth century
[1]. Dalla Croce in the middle of the sixteenth century claimed flexible catheters
too [1], made from the skin of fishes and birds.
The limitation of these flexible catheters was that they could not be used as
indwelling ones, but at least, the need was already existing and partial solutions
were certainly known before Van Helmont published his method.
After Van Helmont, the gummicatheter was apparently introduced by the
German Theden around 1777, although the Frenchman Bernard thought it a French
invention [1]. The gummi–elastic catheter was introduced by Mercier (1811–1882)
in 1840. The Englishman Teevan wrote in 1888 that the problem of prostate
disease was solved: ‘‘Patients carry in their walking sticks or umbrellas but one
catheter’’ (see [1]). The disadvantage of this type of catheters was that the end with
the opening broke easily off and remained behind in the bladder; moreover, the
lumen was small and the catheter could not be sterilized.
It is Nélaton (1807–1873) who invented the vulcanized caoutchouc catheter,
which he called ‘‘sondes en caoutchouc rouge’’, which could be used as an
indwelling catheter. The type of catheter in current use was developed after World
War II.

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20.2 Catheterization and its Consequences 469

20.2 Catheterization and its Consequences

Catheters are used to empty the bladder by (over)extension of the urethral lumen.
This can improve the postoperative recovery of urethra, bladder neck, and bladder.
The procedure however also penetrates a natural barrier, reducing the sterility of
the urethra, often giving rise to infections in the bladder [2].
The use of catheters is frequent. Elderly people living at home can use them,
which concerns 1 % of the population older than 75 years of age [2]. In hospitals,
25 % of the patients above 65 years of age are treated with an indwelling catheter.
The increase in pelvic floor operations augments this percentage up to 35 % in the
Netherlands [2].
In dogs and cats, indwelling urinary catheters will cause infections. After
removal of the catheters, infections will persist. The animals with bacteriuria were
given antibiotics, which induced antibiotic-resistant bacteria [3]. The same occurs
in humans [2, 4]. Addition of disinfectants to the urine drainage bags, which kept
the bags sterile, does not overcome bladder infection [5], but will delay infection
[6]. Therefore, development of bacteria in the drainage bag cannot be held solely
responsible for bacteriuria.
Bacteria can reach the bladder by three routes, if an indwelling catheter is
present [7]:
1. By inserting the catheter;
2. By ‘‘traveling along the urethra in the small, fluid-filled cavity between catheter
and mucosa’’;
3. By contamination of the drainage system of the catheter.
Scanning electron microscopy [8] showed biofilm formation on the luminal
surfaces of the catheter after bacteriuria: ‘‘Single to mixed communities up to four
different species could be found in these films, with a thickness up to 490 l
containing a 400 cell thick layer of bacteria’’. So, the lumen of the catheter is also
occupied by bacteria and is a secondary access route if bacteriuria is present.
The most interesting question, of course, is how do urethra and bladder keep
themselves free of bacteria [2]. The meatus or the outlet of the urethra is the area
where bacteria collect in their efforts to enter the urinary tract. Women, cleaning
themselves at the toilet after defaecation, should always carry this out from urethra
toward the anus and not in the other direction. In natural situations, bacteria
sometimes can infect the bladder, which happens more in women than in men. The
length of the urethra is held responsible for the difference between women and
men: when on pilgrimage, it is clear that traveling from Amsterdam to Rome by
foot is different from the journey from Amsterdam to Peking by foot. In the latter
case, it is doubtful whether one should reach Peking at all. The same comparison
holds for bacteria in the female and male urethra.
But what is keeping the urinary tract non-infectious [2]. Regular voiding pre-
vents stagnant urine in which high concentrations of bacteria can easily develop.
However, this is so for indwelling catheters too. The same holds for the stream.

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470 20 Catheters

The only obvious difference is that urine can no longer contact the mucous layer of
the urethra. So, this interaction has to be responsible for the sterility of the urinary
tract, and/or it triggers the defense mechanism preventing bacteria finding their
way into the urinary tract.
Three modes of infection (infectiogenesis) are known [2]:
1. The natural barrier can be broken down by microorganisms. The invasive
capacity of bacteria is determined by their number and by the rate at which the
microorganisms involved proliferate.
2. Bacteria that in principle are harmless can enter the body due to defects in the
skin or in the mucous layers. Women will pass once every 14 days through a
stage of bacteriuria due to this type of infection. Normally, the clearance
capacity is enough to overcome this invasion of bacteria.
3. If the resistance of the patient is diminished, microorganisms will get their
chance to develop in the body. This is called endogenous reactivation.
Accumulation of bacteria between the catheter and the mucous layers of the
urethra increases the invasive capacity of the bacteria, but there is more. Bacteria
adapt to their environment. So, the mucous is the culture medium for bacteria, and
some species will develop extensively, while others are inhibited in their growth.
Proteus mirabilis and Escherichia coli are the two species that love the mucous
environment. Proteus is the species responsible for encrustation of the catheters,
and Escherichia belongs to our digestive tract flora. However, there is an inter-
species variation present [9].
Once the bacteria are present, they have the opportunity to taste the outer
surface of the mucous cells with their small tentacles, called fimbriae. These cells
carry all kind of proteins and sugars on their surface, also for protection against
bacteria. Nevertheless, bacteria can adhere to certain of these substances and
destruct the integrity of the lining urothelium [11, 13, 15]. Although it takes time
for bacteria to adhere, once they are successful despite the resistance of the
mucous cells, it is difficult to remove them. Even when the bacteria have left the
urinary tract, that they had conquered, still they leave their ‘‘footprints’’ so that
successors can again easily adhere to the mucous cells [10–15]. Few substances
can stop this bacterial strategy [16]. So, it is flushing urine regularly through the
urethra together with the protection against bacteria that prevents bacteria having
an opportunity to taste the outside of the mucous cell, and to induce cellular
changes, and prevent the accumulation of bacteria, decreasing their invasive
capacity.
If patients have bacteriuria, several species can be involved. Some are present at
high concentrations, others at low concentrations. There seems to be an equilib-
rium between species, in the sense that species that were present in high con-
centrations will return with a high concentration and vice versa. There seemingly
exists a rivalry between bacteria present at low and at high concentrations;
‘‘however, species at low concentration usually do not grow to high concentration
in the presence of other species at high concentration’’ [17].

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20.2 Catheterization and its Consequences 471

Indwelling catheters will cause bacteriuria within 7–10 days despite all the
improvements in the design. Thus, silver-coated catheters that will release silver
ions to reduce bacterial growth [18] (by the way the first types of catheters in the
Roman time and Middle Ages were made of silver) and antibiotic-coated slicone
rubber catheters [19] have been devised. Several claims have been published that
special types of catheters can overcome bacteriuria. One of them is the electrified
catheter, which still has to prove its value [20].
In general, catheterization for more than 7 days will cause bacteriuria.

20.3 The Effects of Party Drugs on Lower Urinary Tract


and Sexual Function

You, as a reader, must be wondering. What a leap jump from catheters to party
drugs! The authors must be on some hallucinating drug to warrant this step. Well,
they are not, and the step is not that hard to justify in light of the ‘‘mind map’’
structure we have explained in the preface. We start of by describing drugs
administered to the bladder through the use of catheters. Urologists do that a lot.
For example, bladder cancer is often treated by the intravesical administration of
medicinal drugs like mitomycin-C, bacillus calmette-guerin (BCG), epirubicine,
and keyhole limpet hemocyanin (KLH): All drugs are in liquid form and have to
be installed in the bladder to perform their tasks. Usually, these drugs are installed
via intermittent catheterization, meaning that a thin lubricated catheter is inserted
and after administration of the drug immediately removed. But bladder cancer is
way beyond the scope of this chapter. It is way more interesting to read about
recreational drugs and their effects on the urinary tract and sexual function.
A Sign of the times?
In my daily practice as an urologist, I (WK) cannot ignore that an increasing
number of young individuals, especially adolescent males, visit the emergency
department with urological complications after the use of recreational drugs. I
remember at least three cases in the past two years.
One of them was a 17-year-old adolescent presenting with an acute urinary
retention three times in one month, each time in the early hours of Sunday morning
(not a suitable time for a guy in his mid-forties). In the first two visits, I was quite
naive and believed his story that he only drank a couple of beers with his mates
and ended up in full urinary retention ‘‘out of the blue’’. I treated his urinary
retention using an indwelling silicon catheter for a few days, after which, it could
be removed and spontaneous micturition occurred. I had already started a full
urological work-up when he presented himself for the third time, now accompa-
nied by his friends. It was in fact a very experienced doctor in the emergency
department in my hospital who broke the case: ‘‘Wijnand’’, he said, ‘‘these guys
are completely stoned’’. In fact, every time my patient had to have his urinary
retention treated, he had used ecstasy in combination with more than a few beers.

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472 20 Catheters

Fig. 20.1 Structure of levo-amphetamine (left) and dextro-amphetamine (right). Taken from
Wikipedia (20 July 2013)

Being relatively rare a decade ago [21], urological complications of party drug
(ab)use will undoubtedly present more frequent as the consumption of these drugs
increases.
Pharmacology and toxicology of party drugs
Methylenedioxymethamphetamine (MDMA), GHB, ketamine, rohypnol,
methamphetamine, cocaine, and LSD are frequently used drugs at parties, where
MDMA called ecstasy is being employed most frequently. The use of these drugs
has rapidly increased since they are relatively cheap, readily available, and cause a
desired intoxicating effect.
In view of the scope of this book, we will only describe in this chapter the
effects of amphetamines and ketamines on lower urinary tract and sexual function
and of cannabis on reproduction.
Methylenedioxymethamphetamine (MDMA or ecstasy) and methamphetamine
(also known as speed) are synthetic drugs derived from the structural class of
amphetamines. Amphetamine was first synthesized in 1887, being one of a series
of compounds related to the derivative ephedrine. It is a chiral compound and a
homologue of phenethylamine. Amphetamine is in fact a racemic mixture of its
two optical isomers levo- and dextro-amphetamine, the latter being the most potent
one (Fig. 20.1).
No pharmacological use was found up until the late 1920s (1927) when it was
tested in search of an artificial replacement for ephedrine. Soon thereafter, it was
marketed under the name of Benzedrine in the early 1930s for the treatment of
nasal congestion and grew rapidly as medical professionals recommended it for all
kinds of ailments like alcohol hangover, narcolepsy, depression, weight reduction,
hyperactivity in children, and vomiting associated with pregnancy. The most
commonly reported effects of the drug are a sense of well-being and a decreased
feeling of fatigue. It was thus extensively used as a means of withstanding pro-
longed periods of exertion by athletes, soldiers, pilots, and truck drivers. Effects
like euphoria, increased self-confidence and self-esteem, and increased libido and
alertness are the most important reasons for its recreational use.
To understand the effects but also the (unwanted) side effects, we have to look
into the pharmacodynamics, especially the effect of the drug on the central nervous
system. Amphetamine exerts its effect mainly by modulating different neuro-
transmitters in the brain, predominantly in the brains reward circuitry. The neu-
rotransmitters involved are as follows: dopamine, serotonin, and norepinephrine.
The chemical messenger dopamine is active in the mesocortical and mesolimbic
reward pathways. Release of this neurotransmitter is correlated with a state of
euphoria [22, 23]. Serotonin is synthesized in serotonergic neurons of the central

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20.3 The Effects of Party Drugs on Lower Urinary Tract and Sexual Function 473

nervous system, where it has various functions. These include the regulation of
brain areas involved in mood, appetite, and sleep. Serotonin is also active in
cognitive functions like memory and learning. Modulation of serotonin at synapses
is also the main action in some pharmacological antidepressants (SSRIs). SSRIs
are serotonin-specific reuptake inhibitors, which increase the extracellular level of
serotonin by inhibiting its reuptake into the presynaptic cell, thus increasing the
active amount of serotonin in neurotransmission. In general, more neurotransmitter
means more effect of that neurotransmitter.
Amphetamine also causes increased blood and brain levels of norepinephrine
(or noradrenaline), which is a neurotransmitter like adrenaline in the central ner-
vous system [24]. Those parts of the body that are affected by this substance are
described as being noradrenergic. The part of the peripheral nervous system using
norepinephrine as a neurotransmitter is called the sympathetic nervous system (see
Fig. 16.1).
The noradrenergic effects of amphetamines lead us to the understanding of the
urological complications of ecstasy use. We have seen in Chap. 14 that the pelvic
organs are innervated through the pelvic plexus. The bladder and bladder neck are
supplied with both sympathetic and parasympathetic autonomic innervation (see
Fig. 14.4). Stimulating the sympathetic (noradrenergic) innervation of the bladder
neck leads to an increased tonus of the smooth muscular sphincter of the bladder
neck and urethra, causing closure or inability to relaxation. Thus, the noradren-
ergic effect of amphetamines causes an outflow obstruction at the level of the
bladder neck and as a consequence difficulty voiding or even urinary retention.
These symptoms of outflow obstruction can even become chronic, despite the
discontinuation in use of the MDMA [25] and necessitating prolonged use of an
indwelling catheter or intermittent self-catheterization.
In the literature, two articles appeared in 2000 [26] and 2003 [27] describing a
rather serious adverse reaction to the use of MDMA and ephedrine. The first is a
case report describing the presentation of a young man with priapism after use of
ecstasy. Priapism is a medical condition in which the erect penis does not return to
its normal flaccid state, despite the absence of physical and psychological stimu-
lation, within 4 h. Therapeutic intervention is mandatory since the prolonged
erection can cause permanent damage to the erectile tissue due to lack of oxy-
genated blood. Priapism can be caused by underlying hematologic diseases like
leukemia and sickle-cell disease or neurological conditions like spinal cord injuries.
Most often, however, it is iatrogenic due to the administration of erection-stimu-
lating intracavernously injected drugs like papaverine or alprostadil. Priapism is
rarely related to the use of sildenafil (Viagra), by the way. If it occurs, it usually
does in combination with concomitant medication, diseases as described above or
sildenafil overdose [28]. Priapism may be treated by the use of ephedrine or
phenylephrine orally or injected in the penis. Being adrenergic substances, they will
cause contraction of the smooth muscles in the corpus cavernosum, thus facilitating
the venous outflow and thereby restoring a flaccid state of the penis. Since adren-
ergic substances cause erectile failure, it is difficult to understand why ampheta-
mines (with adrenergic properties as we have seen above) would induce an erection,

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474 20 Catheters

Fig. 20.2 Structure of (R)-ketamine (left) and (S)-ketamine (right). Taken from Wikipedia (21
July 2013)

let alone a priapism. The second article describes the presence of priapism after the
use of ephedrine and cocaine. The investigators studied the effect of ephedrine on
isolated rabbit penile cavernosal tissue strips subjected to electrical field stimula-
tion. As expected, they found ephedrine to cause smooth muscle contraction in the
cavernosal strips. The cause of priapism due to exogenous adrenergic substances
has to be explained by the depletion of endogenous norepinephrine from sympa-
thetic nerve endings, leading to the inability of the smooth muscle to contract, thus
facilitating the inflow of blood in the erectile tissue and the restriction of blood
outflow. Likewise, cocaine appears to induce a refractory priapism also with
treatment being challenging [28]. The pharmacodynamic properties of cocaine can
explain the presence of priapism as a side effect, since cocaine acts biologically as a
serotonin–norepinephrine–dopamine reuptake inhibitor (SNDRI) also called triple
reuptake inhibitor. SNDRI blocks the respective transporter leading to increased
levels of extracellular serotonin, norepinephrine, and dopamine and therefore an
increase in serotonergic, noradrenergic, and adrenergic neurotransmission. It is thus
not completely surprising, even to be expected, that cocaine can also have a neg-
ative effect on bladder function [29].
Ketamine (street name ‘‘Special K’’) is, like amphetamine, a chiral compound,
and the pharmacological preparation is also racemic having two stereoisomers (S)-
ketamine and (R)-ketamine (Fig. 20.2). In the central nervous system, ketamine
acts as a non-competitive N-methyl-D-aspartate receptor (NMDA) antagonist. The
NMDA receptor is thought to be critical in synaptic plasticity, a cellular mecha-
nism for learning and memory. In fact, this receptor is a glutamate receptor (the
other is the AMPA receptor) [30].
Ketamine binds to the receptor, effectively inhibiting its channel and thus
blocking its function in learning and memory. NMDA receptor antagonists prevent
central sensitization in the dorsal horn neurons (see also Sect. 16.7.4), causing
interference with pain transmission in the spinal cord. Therefore, ketamine shows
analgesic effects by NMDA receptor antagonism, as well as by inhibiting nitric
oxide synthase. Inhibiting nitric oxide, a gaseous neurotransmitter involved in pain
perception, also causes analgesic effects. Ketamine also alters cholinergic neuro-
transmission and acts as a noradrenergic and serotonergic uptake inhibitor. In the
peripheral nervous system, ketamine affects the catecholaminergic transmission. It
stimulates the sympathetic nervous system by inhibiting the reuptake of cate-
cholamines and therefore induces catecholamine release. To refresh your memory,

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20.3 The Effects of Party Drugs on Lower Urinary Tract and Sexual Function 475

catecholamines present in the human body are epinephrine (adrenaline), norepi-


nephrine (noradrenaline), and dopamine.
Ketamine was originally developed in 1965 as a derivate of phencyclidine
(PCP) and was approved by the FDA in 1970 to be used for general anesthesia. It
is used most frequently as an analgesic in emergency medicine, for sedation in
intensive care medicine and for anesthesia in veterinary medicine. Typically, it
induces a state of dissociative anesthesia meaning it causes, apart from anesthesia
and analgesia, also effects like amnesia, sedation, and euphoria.
Due to its dissociative abilities, ketamine is frequently consummated in the club
scenes as a recreational drug. Users experience a state of depersonalization and
dissociation and in higher doses a state which is called ‘‘K-hole’’: profound dis-
tortions in or complete loss of bodily awareness, sensations of floating or falling,
hallucinations, euphoria, and total loss of time perception. It is not rare for users to
have a complete amnesia for their experiences due to the NDMA receptor
antagonistic properties of the drug that causes disturbances in memory functions.
For recreational use, ketamine is administered more frequently and over more
prolonged periods than in the situations for which it was intended, namely for
medical use. The adverse effects of prolonged exposure of the drug on cognitive
functions are chronic and may be severe [31]: ‘‘Cognitive deficits were mainly
observed only in frequent users. In this group, increasing ketamine use over the
year was correlated with decreasing performance on spatial working memory and
pattern recognition memory tasks. Assessments of psychological wellbeing
showed greater dissociative symptoms in frequent users and a dose–response effect
on delusional symptoms, with frequent users scoring higher than infrequent,
abstinent users and non-users, respectively. Both frequent and abstinent using
groups showed increased depression scores over the 12 months.’’
Frequent users consuming significant amounts of ketamine can also suffer from
physical complications of the drug, like a small painful bladder, ureteric
obstruction, papillary necrosis of the kidney, and liver dysfunction [32]. Especially
the side effects concerning the urinary tract are of interest in this chapter. Chu et al.
published an article in 2008 on significant lower urinary tract symptoms (LUTS) in
59 young abusers of street ketamine [33]. All patients had moderate to severe
LUTS, i.e., frequency, urgency, dysuria, urge incontinence, and occasionally
painful hematuria. More than two-third of abusers showed various degrees of
inflammation of the bladder mucosa at cystoscopy, similar to that seen in chronic
interstitial cystitis (IC). In twelve patients, a bladder biopsy was performed, and all
showed histological evidence of IC. Urodynamically detrusor overactivity or
decreased bladder compliance was found to some degree in all patients. Somewhat
striking was the presence of unilateral or bilateral hydronephrosis on renal ultra-
sound and even signs of papillary necrosis on radiological imaging in 7 % of
patients. These symptoms could well progress to renal failure. The same bladder
symptoms and the presence of bilateral upper ureteric narrowing were seen in
ketamine abusers studied by Lai et al. [34]. The treatment of bladder symptoms by

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476 20 Catheters

administration of a sodium hyaluronate solution in the bladder provided some


symptomatic relief. This solution is also used for the treatment of symptoms in
patients suffering from chronic IC also known as painful bladder syndrome (PBS).
It is at this point wise to shed some more light on this syndrome. The International
Continence Society (ICS) defines it as ‘‘the complaint of suprapubic pain related to
bladder filling, accompanied by other symptoms as increased daytime and night-
time frequency, in the absence of proven urinary infection or other obvious
pathology for the duration of more than six months’’ [35]. The ICS reserves the
diagnosis of IC to patients with typical cystoscopic and histological features. So,
IC is in fact part of PBS. PBS is a clinical diagnosis and probably strongly related
to other pain syndromes like irritable bowel syndrome, fibromyalgia and chronic
fatigue syndrome. Historically, the definition of IC has thus shifted from a severe
inflammatory bladder condition to a condition primarily described by symptoms.
Treatment of BPS remains challenging.
In some cases when bladder symptoms of ketamine abuse are severe and
conservative treatment is failing, removal of the bladder can be necessary [36].

20.4 Cannabis and Reproduction

The Netherlands is considered a sanctuary for drug abuse, which of course is not
true. Liberal law does not mean that there are no severe restrictions. The opium
law as well as the ‘‘Drank and horeca’’ (beverage and pub, hotel and catering) law
and the law on medicine contains strict Dutch regulations for amphetamines,
anabolic steroids, benzodiazepines, buprenorphine, cannabis, cocaine, crack,
ecstasy, GHB, heroine, ketamine, LSD, metamfetamine, methadone, methylfeni-
date, and paddos (mushrooms). Alcohol and tobacco are also restricted. Never-
theless, the use is totally forbidden (cocaine) or restricted to personal consumption
(cannabis) or its use is age related (alcohol).
The double standard of morals is the best demonstrated by the USA. Cannabis
in acute use is dangerous during actual car driving, but past use is not. As with
alcohol, the US police and its legislature wanted to know the concentration that is
dangerous and punishable. Such studies cannot be carried out in the USA, but are,
therefore, done in the Netherlands [37].
The comment of Senator Chuck Grassley of Iowa should not be missed: ‘‘The
Dutch government and Dutch academia have a tradition of supporting the legal-
ization of marijuana. This raises the question about the unbiased nature of any
study relating to the use of marijuana from the Netherlands’’ [37]. The reaction is
prejudiced and puts Dutch science in an unfavorable light.
Nevertheless, the outcome is that a legal limit for the active substance in
cannabis, tetrahydrocannabinol (THC), is 2–5 ng per ml blood. The acute cannabis

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20.4 Cannabis and Reproduction 477

effects at this concentration and higher are impairment of psychomotor, cognitive,


and actual driving performance and increase in the risk of becoming involved in
traffic accidents. Cannabis in combination with alcohol increases the cannabis
accident risk at least twofold and even more [37].
Besides the danger of the use of cannabis, like feeling high, relaxation, memory
impairment, cognitive and motor impairment, anxiety, and psychosis, it has also
therapeutic effects. The therapeutic effects of cannabis are as follows:, broncho-
dilation in bronchial asthma, antiemetic effect in the prevention of nausea and in
vomiting caused by anticancer drugs, appetite stimulation in anorexia, analgesia in
cancer pain, a decrease in spasticity, ataxia and muscle weakness in multiple
sclerosis, cerebral palsy, spinal cord injuries, and it can produce a decrease in
intraocular pressure in glaucoma [37]. So, besides the adverse effects, there are
also medical beneficial effects. Here, we treat the THC effect on reproduction.
The body contains cannabinoid receptors (CB). The CB-1 receptor is restricted
to the central nervous system, while the CB-2 receptor is present in the periphery
of the body. The human body produces its own endocannabinoids that influence
these receptors. They can also be activated by plant cannabinoids, synthetic can-
nabinoids, and spice. These receptors induce dopamine release in the human brain
(in the striatum). THC is stored in fatty substances in the body, stays longtime
stored in it, and its release is slow and in low concentrations. That is why so long
after smoking cannabis, THC presence can still be determined, for example, in
sportsman and woman. The effect after smoking marijuana for a short period of
time (e.g., 10 min) is short lasting (10–30 min), and there is a strong interindi-
vidual variability in the THC effect [37]. The antiemetic effect of cannabis in the
prevention of vomiting caused by anticancer drugs and the analgesia produced in
cancer pain induced its use in cancer patients.
However, there are two reports that found a link between cannabis and the
occurrence of testicular germ cell tumors: ‘‘The biologically active components of
marijuana may directly affect testicular germ cell tumors risk by altering gona-
dotropin and hormone levels during puberty; however, these components may
function through pathways other than the endocannabinoid system’’ [38]. A partial
explanation of the increase in testicular germ cell tumors in the USA since 1970
seems to be given.
‘‘As with research on all drugs of abuse, studies into the influence of cannabis
use during human pregnancy have been fraught with contradictions and contro-
versies’’ [39]. Nevertheless, nearly 10–20 % of pregnant women use cannabis in
the Western world, and its use is correlated with the following: low birth weight,
prematurity, intrauterine growth retardation, presence of congenital abnormalities,
perinatal death, and delayed time to commencement of respiration.
What is meant as a ‘‘trip for the brain’’ now comes out to be destructive for the
lower urinary tract, sexual function and the reproduction function of the pelvis.

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478 20 Catheters

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on incontinence. European association of urology, 5th edn
36. Lieb M, Bader M, Palm U, Stief CG, Baghai TC (2012) Ketamine-induced vesicopathy.
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and Cognition (LIBC) symposium 24 Sept 2012; Ramaekers JG et al (2006) Cognition and
motor control as a function of D9-THC concentration in serum and oral fluid: limits of
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38. Trabert B, Sigurdson AJ, Sweeney AM (2011) Marijuana use and testicular germ cell tumors.
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39. Park B, McPartland JM, Glass M (2004) Cannabis, cannabinoids and reproduction.
Prostaglandins Leukot Essent Fatty Acids 70:189–197

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Chapter 21
The Pelvis During Childhood and Puberty

Before pregnancy can occur, the bony pelvis has to be developed in a basic form
for pregnancy and delivery, followed by the internal genital organs. The early
pubertal development of genital organs is fat and hormone related. Since the basic
developmental concept is the female one, small deviations of the needed male
hormone concentrations induce already malformations. Stage of pubic hair
development is not always related to maturation of the genital organs. Also the
intriguing question on mono-ovulation in women is discussed in this chapter.

21.1 Introduction

‘‘Puberty can be defined as a maturational process of the hypothalamic–pituitary–


gonadal axis (Fig. 21.1), resulting in growth and development of the genital organs
and concomitantly physical and psychological changes toward adulthood leading
to the capacity to reproduce. The development of the sex characteristics encom-
passes the development of vulva, uterus, vagina epithelium (secondary), breasts,
sexual hair and fat composition (tertiary) in girls and enlargement of penis,
scrotum, prostate, seminal vesicles (secondary), growth of facial and sexual hair
and vocal cords (tertiary) in boys’’ [1].
Most of the primary, secondary, and tertiary pubertal characteristic changes
belong to internal and external pelvic organs. Puberty, therefore, is mainly a pelvic
event regulated by the nervous system.
Puberty knows two phases: a prepubertal phase in which the adrenal glands
produce androgens, called the adrenarche (6–9 years in girls, one year later in
boys). The increase in sexual hormones represents the start of the next phase called
the gonadarche (9–10 years in girls, boys one year later). During late childhood till
into puberty, both adrenarche and gonadarche are active [1]. A nocturnal rise in
luteinizing hormone (LH) produced by the anterior pituitary gland (Fig. 21.1) is
the earliest measurable endocrinological marker of puberty [1].

E. Marani and W. F.R.M. Koch, The Pelvis, 481


DOI: 10.1007/978-3-642-40006-3_21,  Springer-Verlag Berlin Heidelberg 2014

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482 21 The Pelvis During Childhood and Puberty

Fig. 21.1 Left panel hormonal relations between hypothalamus in the brain, anterior pituitary,
ovary, and uterus. GnRH gonadotropin releasing hormone; LH luteinizing hormone; FSH follicle
stimulating hormone; PG progesterone produced mainly by the corpus luteum; E estrogen
produced mainly by the follicle. Upper right panel Localization of the hypothalamus (white
arrow) in a midsagittal section of the brain’s central part. Lower right panel Position of the
arcuate nucleus (white arrow) in the hypothalamus at the stalk of the pituitary, note the
localization of the area preoptica (6). The nuclei projecting to the posterior lobe of the pituitary
are in red with the connections in red. All other nuclei project into the anterior pituitary lobe
(courtesy J. Voogd). Note upper and lower right panels are opposite each other. 1 Central
hypothalamic brain part, 2 pituitary, 3 ovarium, 4 uterus (courtesy Prof Dr. J. Voogd)

Puberty is started genetically. One gene is essential. The KiSS1 gene starts
puberty with the help of a network of related genes, called ‘‘tumor-related genes’’
and its proteins it codes for [2]. These tumor-related genes are effective or in tumor
suppression or in tumor formation. The activation of these genes leads to the
pulsatile release of gonadotropin releasing hormone (GnRH in Fig. 21.1). Around
puberty this, in turn, produces an increase in LH and follicle stimulating hormone
(FSH) that have their effects on the pelvic organs, at first in the primary sexual
organs. ‘‘In all these developments the arcuate nucleus of the hypothalamus, the
main center in the gating system for the control of the secretion of hypothalamic

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21.1 Introduction 483

hormones, plays a key role’’ [2A]. This nucleus, called infundibular nucleus in
humans (14 in Fig. 21.1), contains KiSS1, gonadotropin releasing hormone, shows
increase expression of members of tumor-related genes and contains catechol-
aminergic neurons that influence gonadotropin releasing hormone delivery. Male
and female differences are noted in this nucleus, especially in the amount of
synaptic contacts on its neurons, high in females and low in males, and in its glial
content [1, 2].
A second area that contains KiSS1 is the preoptic area (6 in Fig. 21.1). This area
also stimulates the release of gonadotropin releasing hormone. The difference is in
their reaction on the estrogen-like feedback: The preoptic area gives a positive
feedback only in females, while the arcuate nucleus gives a negative feedback in
both males and females. How a balanced ‘‘working together’’ of these two brain
areas is organized and what functions are exerted is still a matter of discussion [2B].
The relation between genes and puberty stretches even further. The connections
in the brain are different between males and females. Most of the connections are
organized in the so-called white matter of the brain. Studies on the white matter
during puberty in girls and boys, from adolescence till into maturity, show that
pubertal hormones are responsible for the white matter differences found. Such
differences are inheritable, as shown by monozygotic and dizygotic twin pair
studies. By the way, females reach their white matter maturity status earlier than
boys [2D].
Although we know now the genetic background for the start of puberty, it still
remains an enigma what and how puberty starts or in other words by what and how
the genetic activity of KiSS1 is initiated stays unclear [2B].
What also remains unclear is the cause of the amount of males and females born
in the population. The amount of males per 100 females is called the sex ratio. It is
in most countries 105 males on 100 females nowadays, with a lot of exceptions: In
general, more males are born than females. Studies on the sex ratio have been
carried out frequently and related to: cycle day of insemination, coital rate,
duration of gestation, side of ovulation (right-sided ovulation should give more
males), diet, and parasitic infections to name a few [2].
Now we make a jump to menarche to land again at the amount of males and
females born. The age on which menarche is appearing in daughters is influenced,
e.g., by heavy smoking during pregnancy of the mother, not by only pre-pregnancy
smoking. Seemingly, the time of menarche is programmed already in the uterus
and external factors can influence it [2].
Studies on puberty, in fact the age of the start of the menarche, gave remarkable
results [2C]. The sex ratio was 80 males on 100 females, if the population of
mothers had their menarche at the age of 9 years. For the successive years
of occurrence of the menarche, the sex ratio stays low, till the year of appearance
of the menarche is 12 years: 100 males on 100 females. At a menarche around
14 years, the ratio climbed to 111 males on 100 females. Note that 21,208 live
born infants were studied and the premenopausal mothers (n = 10,847) had an
attending age of 37.5 years (SD 7.2 years), range 22 till 54 years. The study
concluded: ‘‘Women entering menarche outside the normal range, especially those

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484 21 The Pelvis During Childhood and Puberty

with earlier menarche, may have an increased chance of producing female off-
spring’’ [2C]. It is undeniable that the article received critical replies still it
highlights a parameter unheard of. This introduction also shows how far the
subjects treated in this chapter are apart.
In this chapter, the pubertal changes that occur in and around the pelvis are
treated. Subjects like fat accumulation at hips in females, changes in the bony
pelvis, uterine alterations, and testis and ovary transformation will be considered.
Sometimes embryological features of the organs have to be dealt with, in order to
understand its modifications during puberty. Hormonal effects on the uterus are
large and exemplified by leiomyomas, benign cancers of the uterus.

21.2 Pubertal Fat Accumulation

Fat distribution is different in men and women after puberty. Before puberty, the
fat content and distribution differs only slightly. In boys, during the period from 10
to 20 years, free-fat weight increases twice as much as in girls. The fat accumu-
lation is opposite. In general, females accumulate twice as much fat, but race
variability is present. The bodily distribution is also different. Females build up
less visceral fat compared to males. Again race variability is present: male African
Americans accrue less visceral fat, while male South East Asians gather more
visceral fat compared to white males. At the end of puberty, the male contains
more abdominal fat, called the android type, while females have more adipose
tissue at buttocks and femoral regions, called the gynoid type [3]. These contour
differences play an important role in gender recognition (see chapter vision).
The current approach to the gender difference in fat distribution concentrates
mainly on the female fat storage. The discussion concerning the first menstruation
involves two topics: Is it related to skeletal growth or to fat storage? Here, we
concentrate on the fat storage. The overall fat distribution is less important for the
onset of menarche than the hip/buttock fat. The ‘‘twice as much’’ stored fat in
females during puberty may be needed later for extra energy during pregnancy and
lactation. The fat located at the female hips and buttocks shows that : ‘‘A 1 cm
increase in hip size is associated with 22 % higher odds of menarche, while a
1 mm increase in triceps skin fold is associated with 9 % lower odds of menarche
and a 1 cm increase in waist circumference, with 7 % lower odds’’ [3]. Thus, hip/
buttock fat storage is somehow related to menarche.
‘‘It has been hypothesized that ovulation in mammals is dependent on body
fatness. According to this hypothesis, a young female cannot ovulate for the first
time until she has accumulated a critical amount of fat relative to her lean mean
body mass. Likewise, the adult female will cease to ovulate if her fat reserves fall
below this critical level. It has been suggested that the evolutionary basis for this
hypothetical dependency is the need to delay pregnancy and lactation until the
female has accumulated sufficient energy reserves to sustain these activities in the
face of food shortness’’ [3A]. This critical fat weight hypothesis has earned a lot of

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21.2 Pubertal Fat Accumulation 485

attention. The most known examples are ballet dancers that will postpone the first
menarche due to their exhausting training or distance runners who delay menarche
with five months of each year of premenarcheal training [3]. Criticism concerns
the simplicity of the hypothesis, while so many organs are involved. A lot of
arguments do not support the hypothesis, especially rodent studies, and in humans,
low body fat is not always related to menstrual irregularities. In pigs where food
regulation was applied the hypothesis was not supported as was the case in young
heifers and ewe lambs. There is not a ‘‘robust’’ relation between fat and pulsatile
gonadotropin release. Due to the criticism, more attention was focused on energy
metabolism in general, which concerns glucose and fat metabolism together, and
thus attention focused also on insulin as we will see later on.
Where is the link between fat, glucose, and the hypothalamus, responsible for
puberty, as expressed in females by the first menarche, localized? It is the arcuate
nucleus: ‘‘The arcuate nucleus of the hypothalamus is believed to be the ‘master
hypothalamic centre’ for energy balance’’ [4].
The arcuate nucleus is a special hypothalamic nucleus since it misses the
blood–brain barrier that is present in most other parts of the brain. The addition of
the small molecule monosodium glutamate (also known as Ve-Tsin as an additive
in Chinese food) produces obese rats. Monosodium glutamate passes through the
rat blood–brain barrier and destructs parts of the arcuate nucleus [5]. This
destruction occurs in rodents not in humans (high concentrations do produce head
ache and vomiting in humans). Large molecules can also pass into the surround-
ings of the arcuate neurons due to the absence of the blood–brain barrier. The
arcuate nucleus, therefore, plays an important role in fatty acid sensing, which is in
its turn important for the control of energy homeostasis. Neurons sensitive to fatty
acids are present in the lateral hypothalamus, and fatty acids are capable to change
the firing rate of neurons in the arcuate nucleus [6]. Fatty acids regulate the
membrane, neuronal conductance of a ‘‘wide variety of ion channels’’ [6]. Studies
showed a differential effect on arcuate neurons, if oleic acid (an essential fatty
acid, people have to take it from plants) was administered. Three distinct sub-
populations of arcuate neurons could be discerned that reacted differently on oleic
acid if low or high concentrations of glucose were present.
Therefore, more than one population of arcuate neurons is involved in the
neural control of insulin secretion by fatty acids [6]. Seemingly, a balanced effect
of these subpopulations of arcuate neurons is present depending on the glucose
level noticed in the arcuate nucleus and this effect is via the hypothalamic network
and hormones passed toward the pancreas, regulating insulin delivery, producing
fine tuning of energy levels. Insulin codetermines the amount of energy rich
substances present in the body that can be converted to fat [8].
Thus, arcuate fatty acid sensing is present: ‘‘a local increase of fatty acids in the
brain triggered changes in insulin secretion and action (involving in particular the
hepatic glucose output), with or without food intake modifications. These changes
appeared to be due, at least in part, to modifications of autonomic nervous system
activity and more precisely to fluctuations of the sympathovagal tone. Indeed, the
two antagonistic parts of the autonomic nervous system, sympathetic nervous

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486 21 The Pelvis During Childhood and Puberty

system, and parasympathetic nervous system innervate the pancreas and insulin
target tissues, exerting catabolic and anabolic effects, respectively’’ [6]. Fatty acid
diet in anorexic tumor-bearing rats delays tumor appearance and growth and the
onset of anorexia. These parameters went along with a increase of 38 % of NPY
(neuropeptide Y, a neurotransmitter) content in the arcuate nucleus and alpha-
melanocyte stimulating hormone (alpha-MSH) decreased 64 % in the arcuate
nucleus [7], indicating that fatty acids do affect relay functions and the production
of proopiomelanocortins (forerunner hormone, for example, adrenocorticotropic
hormone involved in the stimulation of insulin secretion) in anorexia. Both in
anorexia and diabetes, delay of menarche is noticed, both related to deviations in
glucose metabolism.
It therefore seems important to understand the normal physiology of the arcuate
nucleus. Ionic conductances were studied in cultured arcuate neurons [2]. From the
five morphological types of rat arcuate neurons [2], none has been identified for
their type of oleic acid action in the presence of glucose till now. More information
on the hypothalamus and fat metabolism brings us out of the scope of this chapter,
if orexin, other regions of the hypothalamus responsible for extreme overeating
(ventromedial nucleus) and responsible for hunger feelings (lateral hypothalamus),
arcuate interactions, agouti-related peptides, and proopiomelanocortins are dis-
cussed (see [8] for review articles).
A causal relation as expressed in the critical fat weight hypothesis is no longer
tenable. It is replaced by a far more integrated system of neuronal connections and
hormone release that relates energy metabolism to hypothalamic steering during
puberty.
Alternative hypotheses for fat accumulation in women are published in the
literature, mainly as a reaction on the sexual signaling hypothesis of fat at hips,
buttocks, and breasts (see chapter vision). Humans differ from other mammals in
the absence of fur, to which the baby clings, e.g., in monkeys. Hip and buttock fat
should be involved in baby carrying. Squatting or sitting on the ground needs in
the furless human insulation that occurs by fat. And fat can be used to change
androgens in estrogens. This conversion into extra-gonadal estrogens is considered
a female endocrine function for the maintenance of ovulation for which fat storage
is needed [6].

21.3 The Bony Pelvis and Puberty

Two large study programs on adolescence were started before World War II. One
at the Yale University School of Medicine and the other was a study of Growth and
Development, supported by the Brush Foundation (Cleveland, USA, since 1928).
The impression of the researchers was that nearly no difference in the bony pelvis
of boys and girls before puberty can be noticed. Just (3–4 years) before the first
menstruation the pelvis was characterized by the acetabular constriction of the
pelvic canal; ‘‘an inward projection of the wall of the pelvis in the region of the

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21.3 The Bony Pelvis and Puberty 487

acetabula’’ [9]. During female puberty, growth increases and the acetabular con-
striction disappears, while the width of the pelvic canal increases more than its
antero-posterior diameter: an asymmetrical growth. ‘‘Accompanying this dispro-
portionate growth, there is a beginning widening and rounding of the forepart of
the pelvis and the beginning obliteration of the acetabular constriction. The portion
of the pelvic canal, which is immediately medial to the acetabula, appears to push
outward, with the result that the constriction in that region which characterizes the
pelvis of the prepuberal girl becomes gradually obliterated’’ [9]. Within
18 months, the remolding of the female pelvis is at its end and does not change
much anymore. The little continuing growth noticed is symmetrical.
The menarche always occurred during the end of this asymmetrical growth
spurt of the female pelvis. The menarche never appeared after the total remolding
of the pelvis, which was found in both studies. Thus: ‘‘The rapid change in size and
shape of the superior pelvic aperture at puberty as compared with its long period of
slow, symmetrical growth during early childhood suggests that it is another
expression of the increased activity of the gonads and of the other endocrine glands
which produce the more familiar bodily changes associated with that period of
life’’ [9]. Recent publications confirm these results with the highest growth speed
for the great pelvis 11.6 months before menarche and for the lesser pelvis
13.5 months before menarche [10].

21.3.1 Bony Pelvis and Adolescent Deliveries

‘‘About 20 % of deliveries in this country (USA) occur to women 18 years or


younger. The adolescent fertility rate, especially among young adolescents, con-
tinues to increase. Also, the number of adolescents has increased. Thus, adolescent
pregnancies are commonly managed in most obstetrical services in this country’’
[11]. Adolescent pregnancies raise the question whether the pelvic structures are
ready to receive and manage the embryo and fetus at the menarche. The research
results indicate that pelvic dimensions are changed already before the first men-
struation. Comparison of adolescents, mean 15.6 years, range 13–16, with older
women, mean 24.1 years, range 20–37, shows that average mid-plane dimensions
did not differ more than 0.1 cm: ‘‘The average mid-plane anterior–posterior
dimension (AP) was 12.4 cm for the adolescents and 12.5 cm for the older. The
average mid-plane transverse (T) diameter was 10.0 cm for the adolescents and
10.1 cm for the older. The average outlet AP diameter was 8.5 cm for the ado-
lescents and 8.4 cm for the older. The outlet, T diameter was 9.8 cm for the
adolescents and measured 9.9 cm for the older women’’ [11]. Differences were
found for the inlet diameters: the AP inlet diameter was 0.4 cm and T diameter
1 cm larger in older women. The fetal head adaptation for a smaller pelvic inlet is
more than 1 cm, pubic symphysis and sacroiliac joint can gain an extra 1–2 cm
during labor; therefore, adolescent pregnancies are generally speaking not in
danger for head pelvic disproportions [11].

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488 21 The Pelvis During Childhood and Puberty

Thus, before a human, female can be fertilized, growth spurts have recon-
structed the bony pelvis in such a way that the pelvis is capable to receive, keep
and let the fetus be born.

21.3.2 Bone Mineral Content, Osteoporosis, and Sports

‘‘It has been suggested recently that body fat is an important determinant of bone
mass in premenopausal and postmenopausal women, although other investigators
consider weight more important’’ [12]. Bone is made out of 15 % organic material
(mainly collagen) and out of 85 % of hydroxyapatite (calcium phosphate and
calcium carbonate). These minerals determine the bone mineral content, which is
the main determinant of the body mass. Dual-energy X-ray absorptiometry is used
to determine the bone mineral content and can directly be calculated to body mass.
The weight of the post pubertal females (14–18 years old) correlated directly with
body mass and not with body fat. However, the pelvic regional bone mineral
content, thus pelvic bone mass, was positively correlated with the percentage of
body fat for that structure. The lean body mass did not correlate with the pelvic
regional bone mineral content (it did so for arm and legs), indicating that pelvic
bone mass has a special relation to its local fat. What this relation is and how it is
organized is unknown.
Bone mineral content is also important in osteoporosis [13], which is the loss of
the density of the bone due to extra loss of calcium and phosphate. It is known
mainly from elderly women, due to the reduction in estrogens after menopause.
Using the same absorptiometric technique, several studies were directed to the
effect of sports on the bone density and bone mass in boys and girls. The reason:
‘‘Bone health later in life may rely on the bone mass accumulation during growth’’
[14]. Female handball players were studied: ‘‘Compared to the controls, handballers
attained better results in the physical fitness tests and had a 6 and 11 % higher total
body and right upper extremity lean mass. The handballers showed enhanced bone
content and bone density in the lumbar spine, pelvic region, and lower extremity’’
[14]. The same results were found for pubertal soccer players for legs and pelvis.
Moreover, this increase in bone density and mass could be linked to their increased
hormonal metabolism [15]. Thus, sports are beneficial for the pelvic bone mass and
pelvic bone density in both boys and girls. If mature soccer players are compared to
controls, pelvic bone mass, in fact ‘‘lower body’’ (pelvis and legs) mass, is sig-
nificantly higher. This does not hold for head and arms [16]. Nevertheless, exercise
knows its limit even for league soccer players: ‘‘We conclude that, in national-
league soccer, the bone mineral density needed to attain a bone strength com-
mensurate with that of duration of activity is achieved by 6 h of exercise per week.
Beyond this, additional exercise confers no higher bone mineral density’’ [16].
The conclusion is that exercise before and during puberty enhances the bone
mineral content. Continuing exercise even during aging keeps the bone mineral

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21.3 The Bony Pelvis and Puberty 489

content high and reduces osteoporosis. The lower body part, pelvis and legs,
benefits most of these exercises.

21.4 Pelvic Visceral Organs

During puberty, the pelvic sexual organs are subject to their largest increase in
volume, due to the hypothalamic hormonal steering (Table 21.1). This increase is
sixfold or more for ovary and uterus. Moreover, local parts can differentiate dif-
ferently: the cervix is the largest part of the uterus till puberty, but the fundus and
corpus of the uterus contains the highest increase in volume and the cervix is
lagging behind in pubertal growth, producing the pear-shaped uterine appearance.

21.4.1 Early Development of the Uterus


and its Consequences

Females are characterized by the same sex chromosomes (XX), while males have a
different genetic code for sex chromosomes (XY). The first stages of genital
development are sex indifferent. Later on, it is the male development that diverges
from the female pattern (see Chap. 8). In other words, the basic pattern for all
humans is female, if development wants a male, hormones have to organize the
deviation. The hormones are a ‘‘late’’ embryonic consequence of the genetic code
XY.
In the sex indifferent stage, next to each duct of Wolff develops an extra tube,
the duct of Müller (see Fig. 8.3). It originates parallel to the duct of Wolff, but
more laterally and is also called the paramesonephric duct. The mesonephric duct
(Wolff) grows as an extending cord and subsequently develops a lumen. The
paramesonephric duct (Müller) develops as an invagination of the dorsal wall and
remains rostrally open. Moreover, the caudal parts of Müller meet in the middle
prior to attaining to the dorsal wall of the urogenital sinus. The meeting place just
in front of the urogenital sinus will fuse into one tube with one hollow in humans:
the uterus. The parts that are not fused each produce a uterine tube with an opening
at their rostral part, called the ostium abdominale, by which the egg will be caught
and transported into the uterine tube for fertilization. The general scheme is that
Müllerian tubes start fusion at their caudal area to produce the uterus and that this
fusion progresses half way toward rostral: a unidirectional fusion. There are,
however, examples of mal-fusion present that contradict this scheme because they
indicate a bidirectional fusion [23].
Since the uterus is a fusion of two tubes, a series of malformations can arise
(see Fig. 21.4):

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490 21 The Pelvis During Childhood and Puberty

Table 21.1 Ovarian and uterine volume and shape during life till maturity (adapted and renewed
with permission from Stranzinger and Strouse [17] and from Kamina [18])
Age Ovarian volume (ml) Uterine volume (ml) Uterine shape
Neonate 1–3.6 2.6–4 Spade
3 months–1 year 1–2.7 0.8–1.3 Tubular
1–2 years \1–1.6 0.8–1.3 Tubular
2–8 years 1–4.3 0.8–1.6 Tubular
8–16 years 2–18.3 0.8–25 Pear shaped after puberty
Mature 18–24[ 25–40[ Pear shaped

Although it is an old scheme and modern studies changed the subdivision, it


shows clearly the deviations from the normal situation (normal is 8: uterus sim-
plex; Fig. 21.2). Double uterus, partial double, half separated, or still totally
separated by a septum, without uterine tubes or with one, all deviations are pos-
sible, stressing the variability of disorders of sexual development. A lot of these
uterine malformations go undetected during childhood and are noted mostly during
or after adolescence. The incidence is 3–4 % in the normal population of which
50 % have clinical symptoms. During pregnancy, a septate uterus gives a risk of
28–45 % on miscarriage in the first trimester and pregnancy loss is 90 % over the
whole period. In checks for abnormal bleeding, uterine malformations are found in
10 % of the cases. These uterine congenital malformations are related to: poor
reproduction result, preterm delivery, intrauterine growth problems, come off of
the placenta, fetal problems and death, and the death of the mother [24].
Male testes develop by the 7th week as a consequence of the XY genetic code.
The testes produce two hormones: the anti-Müllerian hormone and testosterone.
The anti-Müllerian hormone induces regression of the female internal genital
organs, while testosterone supports the development of the duct of Wolff into the
male internal organs.
‘‘In the absence of testicular hormones, the different primordial of the internal
and external genitalia follow the female pathway irrespective of the presence or
absence of the ovaries.’’ So Müller duct development is autonomous. The ultimate
consequence is noticed, if a lack of anti-Müllerian hormone secretion or testos-
terone action occurs in males, Müller will not go into regression and a persistent
Müller duct will be present, called persistent Müllerian duct syndrome (PMDS).
These patients are detected because their testes have not been descended (called
cryptorchismus) and research shows the testes, epidydimus, and sperm duct to be
adhered to a uterus with its fallopian tube, inhibiting the descent of the testes
(Fig. 21.3). Part of these patients does have a genetic mutation for the production
of anti-Müllerian hormone or a genetic mutation for the receptor for anti-Müllerian
hormone. More genetic mutations are suspected to be involved in the persistent
Müllerian duct syndrome.
We know now that at least testosterone effect has to be present between week 9
and 14 of development too; otherwise, the uterus and vagina will still develop with
the consequence of a persistent Müllerian duct syndrome [20]. Even too moderate

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21.4 Pelvic Visceral Organs 491

Fig. 21.2 Seven different malformations of the uterus (1–7) and the normal appearance (8)
(Reproduced with permission from Jarcho, Malformations of the uterus [24])

testosterone levels can induce the persistent Müllerian duct syndrome [21]. Still
half of the reproductive organs can be female, if one of the testes is badly
differentiated.
‘‘Considering that disorders of sexual development are among the most com-
mon birth defects, a reference range of normal sex development is essential to
define whether and when a variation or disorder is present’’ [22]. Therefore, the
study of the normal development of the sexual organs is a prerequisite for the
determination of defects, giving a firm base to this type of research.

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492 21 The Pelvis During Childhood and Puberty

Fig. 21.3 Anatomy of the


internal genital organs in
persistent Müllerian duct
syndrome. Testis, epididymis,
and spermatic duct (ductus
deferens in the figure) are
adhered to uterus and
fallopian tube (Reproduced
with permission from Loeff
et al. [19])

One should take notice of the fact that there is no uniform anatomy of the
female reproductive tract in mammals, nor a uniform function exists. ‘‘Among
placental mammals a double uterus is found in rodents, such as the mouse, hare,
marmot, and beaver, and also in elephants, certain bats and aardvark. A beginning
of fusion between the two uteri is evident in pigs, cattle, certain rodents, certain
bats, and carnivores. A two-horned uterus is characteristic for ungulates, ceta-
ceans, insectivores, and carnivores, while a single uterus, the uterus simplex, is
found in apes and humans’’ [24]. The strongest deviation of a ‘‘general’’ function is
found in marsupials, as an example is used the kangaroo, where the tract contains
two uteri and is specialized in pathways to let enter the sperm (lateral vaginal
canal) that are different from the one to let the fetus pass during labor (pseudo-
vaginal canal, see Fig. 21.4). Moreover, if a young is present in the pouch,
drinking from the teat, the fertilized egg will stop early in development (in the
blastocyst stage) to grow, which is called diapause. The uterus is at that moment in
an embryo storage stage (Fig. 21.4); a situation not known in humans.
The attention in the kangaroo for the extraordinary construction of the vagina
also brings up considerations concerning the human vagina. The development of
the human vagina still raises controversies. The ducts of Wolff and Müller end,
next to each other, on the dorsal wall of the urogenital sinus. Here, two bulges are
present that are responsible for the different points of view. Are these bulges
related to Wollf’s duct endings or not. If yes than the outgrowing plate, which will
form the vagina, contains also Wolffian, thus male material, otherwise not. His-
tochemical results are in favor of participation of Wolff’s duct in the production of
the vagina [21]. The plate will grow, will be filled with cells and afterward a
hollow appears in it produced by cell death of these inner cells, which finally
constitutes the vagina (see Fig. 21.6). For the vagina holds that malformations like
double vaginas, vagina without uterus can be present.

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21.4 Pelvic Visceral Organs 493

Fig. 21.4 Left figure shows the urogenital apparatus of marsupials. The pseudovaginal canal is
only opened for passage of the fetus. Right side shows that the female red kangaroo is forced to
bring the embryo in diapause, if the joey is on the teat drinking (Reproduced with permission of
the Cambridge University Press from R. V. Short (1972) Species differences in: Reproduction of
mammals 4: Reproductive patterns)

21.4.2 Development of the Uterus Around Puberty


and Leiomyomas

The uterus wall is made of smooth musculature. As we have shown in the table,
the release of hormones at the start of puberty is responsible for a strong growth of
the uterus (see Table 21.1), which also means a strong growth of the uterine
smooth muscles. These hormones are also responsible for the development of
benign tumors of the uterine smooth muscles, called fibroids or leiomyomas
(Fig. 21.5). The incidence is 25–50 % and in autopsies over 70 % leiomyomas are
found [25]. ‘‘Leiomyomas of the uterus are also implicated in female infertility and
are the most common indication for hysterectomy in Western industrialized
countries. In the USA, 200,000 hysterectomies are performed for uterine fibroids
each year. Fibroids may cause abnormal menstrual bleeding (menorrhagia with
secondary anemia, dysmenorrhea) or pelvic pressure due to their mass effect
(urinary frequency, constipation, pelvic pain, dyspareunia)’’ [25, 26A]. ‘‘Fibroids
are two times more common in nulliparous women as compared to women who
have given birth and multiple pregnancies reduce the risk further’’ [25]. Preg-
nancies thus strongly reduce the occurrence of fibroids. These benign tumors are
absent before puberty. Remarkable is that an early menarche increases the risk on
fibroids [25]. In adolescence, fibroids are reported to be present [26A].
Black women have a 2–3 times higher frequency of fibroids and a three times
higher risk. The fibroids occur at younger age, and the disease consequences are
heavier compared to white females. ‘‘Exposure to oral contraceptives between the

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494 21 The Pelvis During Childhood and Puberty

Fig. 21.5 Localization and


types of leiomyomas.
Fibroids can be localized in
the musculature (intramural),
directly beneath the
connective sheath
surrounding the uterus
(subserosal), on a stalk
(pedunculated), or directly
below the endometrium
(submucosal). However, most
fibroids are mixed types, as
indicated by A, B, and
C (Reproduced with
permission from Stewart
[26A])

ages of 13 and 16 years led to an increased relative risk of myomas, whereas use in
general showed protection in direct proportion to duration of use’’ [26A]. Thus, the
pill during puberty increases the risk on fibroids.
Hormonal influences on the uterus are striking, even in the normal situation:
Neonatal maternal and placental hormones increase uterine size, and after the slow
withdrawal of these hormones at the age of 6–12 months, the uterus decreases in
size (see Table 21.1). Thereafter, its size stays constant till puberty. The uterus
starts to react again at puberty to get its pear-shaped appearance, due to the
pubertal hormones. The hormonal gonadal effect during puberty not only influ-
ences pelvic organs, but also growth with the consequence that a direct relation
between the height of the uterus, or volume of the ovary, and age, height and
weight of the pubertal girl was found. To give one example [26]:
Uterine height ¼ ðminus!Þ1:9 þ 0:406  age þ 0:064  weight:
Thus, normal exterior measures indicate the normal interior height of the uterus
or volume of the ovary. In cases of doubt of a regular pubertal development,
noninvasive techniques can check for the real measures of uterus and/or ovary,
which can be compared to the calculated exterior ones and the gathered normal
racial population data. Such measurements are also present for the changing
relation between uterine corpus with fundus and its cervix.
Another measure concerns the blood flow in the uterine artery. Using Doppler
techniques, the flow in this artery can be followed. In prepubertal girls, only

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21.4 Pelvic Visceral Organs 495

systolic flow could be found in the uterine artery. Systolic flow with interrupted
diastolic flow was found in early pubertal girls, while systolic flow with continues
diastolic flow was present in late pubertal girls and girls that passed their menarche
[27]. The change in blood flow is due to the estrogen hormone production of the
ovary. Estrogen receptors are present on the blood vessel wall and in postmeno-
pausal women or women with non-functional ovaries, thus both with a lack of
estrogens, the diastolic flow also disappears [27]. The resistance of the uterine
artery increases, if lack of estrogens is present. It decreases with estrogen therapy
in postmenopausal women. The increased resistance is kept responsible for the
absence of the diastolic flow [27]. The uterine blood flow therefore is considered a
measure of ovary function, by its estrogen effect, and thus regarded a good
measure for the female pubertal situation.
Let us go back to the leiomyomas. The pulsatile release of gonadotropin
releasing hormone is responsible for the onset of puberty for the pelvic sexual
organs by producing FSH and LH, which in turn produce estrogen and proges-
terone (see introduction and Fig. 21.1). Most leiomyomas present itself after the
age of 30 years that is in the mature female. ‘‘Treatment with gonadotropin
releasing hormone analogs improves fibroid-related symptoms and leads to a
transient reduction in fibroid size. Maximum size reduction is seen after about
3 months of treatment. Once gonadotropin releasing hormone analogs are dis-
continued, however, leiomyomas will again increase in size’’ [25]. The release of
gonadotropin releasing hormone influences indirectly the uterine smooth muscular
pubertal growth, but in cases of benign uterine smooth muscular tumors, the direct
addition of this hormone suppresses the tumor growth. ‘‘Gonadotropin releasing
hormone agonists, the mainstay of medical therapy for myomas, work by first
increasing the release of gonadotropins, which is followed shortly by desensiti-
zation and down regulation to a hypogonadotropic hypogonadal state clinically
resembling the menopause’’ [26A, 28] (the same return pathway toward hypo-
thalamus and pituitary as E in Fig. 21.11 is used by the gonadotropin releasing
hormone). Since leiomyomas need estrogens to grow and low levels of estrogens
induce genetic damage, gonadotrophin addition reduces the fibroid tumor [28].
Thus, gonadotropin releasing hormone has a different effect during puberty due to
its pulsatile release compared to continue addition in medical therapy during
maturity.
In leiomyomas, the uterine artery also can play a role: ‘‘Embolization of the
uterine artery induces infarction of fibroids while uterine perfusion is maintained.
Infarction leads to coagulation necrosis and subsequent complete hyalinization of
the fibroids. Further transformations cause softening and shrinkage of the tumors.
Follow-up for 3–24 months has shown that there is an average size reduction in the
uterus of 23–60 %, while the dominant fibroid decreases by 42–78 % on average’’
[25]. It is claimed that the embolization of the uterine artery has a lower risk than
other surgical treatments of fibroids.

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496 21 The Pelvis During Childhood and Puberty

21.5 The External Genitals

The genital organs are subdivided in internal and external ones. Its border is placed
inside the vagina. The urogenital or vaginal plate, the end of the uterovaginal tube
in development, transforms into the vagina. The uterovaginal tube, as a conse-
quence of this development, is subdivided into pelvic and phallic parts with its
border inside the vagina.
The rest of the external genitals develops from the genital tubercle or phallus,
from the urogenital folds, and from the labioscrotal swellings (Fig. 21.7). The
division into external and internal genital organs is important ‘‘because it is related
to the function of these organs, i.e., the internal genitals have a reproductive
function, while the external ones have the function of giving pleasure’’ [30]. The
consequence is that the vaginal area near the vaginal entrance is related to
‘‘pleasure.’’ Here, a repetition of the G-spot discussion is not necessary, but it
explains why the entrance of the vagina is got mixed up with it.
The external genitals develop indifferently during the embryological period,
and the male hormones deviates the development into penis and scrotum. The
female development is nearly autonomous (Fig. 21.6). Testosterone from the testes
has to be converted into dihydrotestosterone, by an enzyme called 5-a reductase, to
produce prostate, seminal vesicles, bulbourethral glands, and the male external

Fig. 21.6 Development of the external genitals. a is during the embryological indifferent period.
b (male) and c (female) occur during the fetal period (with permission from Schoenwolf GC,
Bleyl S, Brauer PR, Francis-West PH (eds) Larsens human embryology, 4th edn. Elsevier Health
Science)

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21.5 The External Genitals 497

Fig. 21.7 Relation between


body weight and testis weight
in elephants (reproduced with
permission from Short RV
(1972) Species differences.
In: Reproduction of mammals
4: Reproductive patterns.
Cambridge University Press)

genitals. Before puberty the female and male external genitals are already present
in its final form.
Puberty makes the genital organs functional. For the female, this includes the
menarche and consequently changes of the exterior of the female organs. The
pubertal exterior changes are not only dependent of the gonadal maturation but
also the adrenal maturation is involved. ‘‘Because adrenarche and gonadarche
proceed independently, the appearance of pubic hair does not provide information
about pituitary-ovarian maturation’’ [31].
Pubic hair in girls can be related to five stages, the so-called Tanner stages
[31A] in which puberty is divided. Beside the pubic hair increase, the mons veneris
and labiae majores increase in volume due to extra fat deposits. Skin increases in
thickness, labiae are more rugose, the clitoris increases in size, the introitus
(vaginal entrance) becomes larger, and glands in the vulva become active. The
vulva and its structures become more prominent and are covered with increasing
pubic hair during puberty. An analogous development occurs in boys: pubic hair
increase and structures become more prominent and the first seminal emissions
occur.
Lower genital tract diseases occur in children and adolescents. Since vulva and
vagina are continuous, vulva diseases are intimately related to vaginal diseases.
‘‘The most common presenting lower genital problem of a preadolescent child is
vulvovaginitis. Most cases of pediatric vulvovaginitis are of dermatologic origin or
may relate to atrophy and/or hygiene problems. Wiping front to back, cotton
underwear in the daytime with none at night, and avoidance of tight leotards,
prolonged contact with wet bathing suits, and irritants such as bubble baths will go
a long way in dealing with this problem. Presenting symptoms of vulvovaginitis
include discharge, irritation or pruritus, burning on contact with urine, and vulvar
redness or abnormal odor. Bleeding may occasionally occur’’ [32]. Most of the
examples are hygiene related and can easily be anticipated.
Child sexual abuse is also determined by vulva deviations. ‘‘While it is critical
to be aware of potential sexual abuse and investigate it, sometimes lack of
familiarity with the presenting signs of some of these vulvovaginal conditions can
lead to an erroneous diagnosis of abuse, and one should be aware for example that

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498 21 The Pelvis During Childhood and Puberty

lichen sclerosus (white spot disease) can be associated with vulvar purpura, and
the child with lichen sclerosus may have blood-filled blisters from minimal
straddle activity such as riding a tricycle’’ [32]. Therefore, examination should
always be carried out by gynecologists trained in sexual abuse of children, as we
learned in the Netherlands, by the Bolderkar-affaire. Parents were accused of child
abuse, due to sessions with dolls equipped with external genitals [33]. The badly
trained interviewer(s) let prevail their own superstition, while theoretically a 90 till
98 % chance on false positivity exists for non-sexual abused children with this doll
method. Only later on it came out that all these accusation in the Bolderkar-affaire
were totally wrong. Analogous situations have been reported from Cleveland
(England), Rochdale, Orkney islands, and California at the Mc Martin Preschool.
Do not mistake it: child sexual abuse should always be investigated, but at all
times with experimental verified psychological and clinical methods and with
trained experts: the ‘‘sex’’ doll method is hardly verified [33].
Knowledge of the anatomy and physiology of the external genital organs and its
development is imperative. Nowadays, no doubt exists. How different it was in the
nineteenth century. Anatomy of the human body was hardly known in middle and
lower classes in Europe and in the USA. Anatomy museums appeared as a kind of
amusement. The writer Michael Sappol in his book ‘‘A traffic of dead bodies’’
listed a forty of these anatomical museums in the time span from 1774 till 1930
[34]. The bourgeois attitude was of a schizoid character. The upper class could get
the information by legal institutions and medical schools, but middle and lower
class were denied the sexual knowledge. The wax nudes in the museums, and
sometimes the whole museum, were destroyed on advice of Anthony Comstock
(1844–1915), leader of the New York Society for the Suppression of Vice. ‘‘On
January 9, 1888, warrants were issued against the aforementioned Egyptian Musée
and European Museum, plus the Parisian Museum and Kahn’s Museum of
Anatomy—‘all the so-called anatomical museums’—not connected to the city’s
‘recognized medical colleges.’ Between 4:00 and 8:00 pm, the police assisted by
the Society for the Suppression of Vice mounted raids against museums. The
proprietors and employees were arrested, fourteen men in all and charged with
‘exhibiting obscene figures and images.’ The ‘hideous specimens’ including some
‘five or six loads of female figures in wax and clay’ were confiscated, and most of
them later destroyed [34].’’
Comstock’s influence was enormous. Information on birth control was con-
sidered ‘‘obscene, lewd, or lascivious.’’ Some anatomy books could not be sent by
post to the students due to pictures of internal and external genitals. Actions
against contraceptives were organized, and in the mean time, the Comstock act
was added to the United States Post Office Act, by which Comstock got police
jurisdiction that he forcefully exercised by arresting people, burning books, plates,
pictures, and statues [34]. Such laws are still in effect in the USA, although the
Supreme Court added the so-called Miller test (three-prong obscenity test) to
define what is obscene. One of the parts of the test asks for prove that there is
absence of serious literary, artistic, political, or scientific value. In other words, in
extreme cases, one has to prove that scientific value is present in publications on

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21.5 The External Genitals 499

internal or external genitals, pictures, photographs, and so on for not being


obscene. Although the other two parts have to be positively affirmed before
something can be judged obscene, it still is a strange approach. Comstock also
acted against Bernard Shaw’s play ‘‘Mrs. Warren’s Profession.’’ Shaw introduced
the term Comstockery: ‘‘Comstockery is the world’s standing joke at the expense
of the United States’’ [35].

21.6 Testis and Ovary

21.6.1 Testis and Penis

The exterior male genitals are nowadays less frequently depicted in paintings and
sculptures. This holds especially for young adolescents and is intimately related to
the forbidden pedophilic pornography. The consequence is that few people know
the relation between pubertal form, pubertal age, and pubertal development of the
male genitals (Table 21.2).
The human testis grows in volume during puberty from less than 3 ml to more
than 14 ml. This increase is regulated by FSH and coincides with thinning of the
scrotum and increase in the scrotal color. The penis enlarges and increases in
circumference during puberty (Table 21.2). Pubic hair augments and its start is just
above the phallus, before it spreads toward the thighs [37].
The intimate relation between growth and testis is best exemplified by ele-
phants. Female elephants undergo a reduction in growth by age. Male elephants, at
the contrary, have a nearly linear growth increase during life time. After puberty,
the elephant testes keep their growth velocity ending up with a nearly
10 9 increase in weight (Fig. 21.7). ‘‘The most remarkable difference from other
terrestrial species is the intra-abdominal testicles, which can reach a mass of up to
2 kg each in an adult bull. During musth (frenzy of male elephants), the testicular
volume can increase up to four times the non-musth volume’’ [36A].
In humans, growth stops, as well as the testicular increase ends. Human growth
is directly related to lengthening of the skeleton, which in its turn seems related to
puberty, due to the growth spurt during puberty. It goes without saying that

Table 21.2 The main increase characteristics of the male exterior genitals related to age
Stages of growth male Age (years)
Enlargement testis and scrotum, pigmentation, thinning scrotum 11.6 (2 9 SD: -9.5; +13.8)
Lengthening penis and continuous growth testis and scrotum, 12.9 (2 9 SD: -10.8; +15)
increase pigmentation
Adult shape 15.0(2 9 SD: -12.8: +17.1)
SD standard deviation. Two times the SD gives the spread around the mean (reproduced with
permission from Root [36])

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500 21 The Pelvis During Childhood and Puberty

skeletal growth and puberty relations are studied. ‘‘Many conditions that delay
skeletal maturation also delay the onset of puberty, whereas conditions that
accelerate skeletal maturation often hasten the onset of puberty, raising the pos-
sibility that skeletal maturation influences pubertal onset’’ [37A]. There is no
relation between bone skeletal development and puberty development, also not
with puberty advancement and height, age, and bone mass index advancement
[37A]. ‘‘Our findings do not support the hypothesis that skeletal maturation
directly influences the age of pubertal onset in normal boys’’ [37A].

21.6.2 Decrease in Age of Puberty and Increase in Height

An early onset of puberty is noticed in our modern societies (Fig. 21.8), causing
sociological and educational problems.
‘‘Although many similar considerations might apply to males, the reproductive
and life history strategies of the two genders are quite distinct and this might be
reflected in the more frequent presentation of females with early-onset puberty.
Further, the absence of an easily assessable marker of potential reproductive
competence means that discussion will focus on the female’’ [38]. Clearly, this
earlier onset of puberty in the literature is more correlated with females than with
males. Recent literature keeps the years 11 till 15 for male puberty together with
the spread of 9 till 17 years. The modern study of secular changes in the timing of
puberty is seriously hampered, because there are hardly enough data available to

Fig. 21.8 Decrease in the age at menarche for the time span 1830 till 1960 (year of menarche)
for European countries and the USA (reproduced with permission from Tanner [40])

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21.6 Testis and Ovary 501

reliably assure such changes in boys [39]. Moreover, racial differences are present,
e.g., start of puberty in non-hispanic black boys and girls is nearly one year earlier
than in non-hispanic whites and Mexican-Americans, while their ending of ado-
lescence is nearly one and a half year earlier [39].
Having pointed to biases that are possible, the earlier onset of puberty could
only be studied well in females. One should notice that the decline in age at
menarche for Norway is 3 years. Due to a later start of the registration of the age at
menarche in other countries, lower values are found. Still it is for Sweden 2 years,
and nearly two years for the USA (see Fig. 21.8). An analogous situation is
supposed for boys by some authors (see later).
This must also mean that the related growth spurt is earlier. Thinking it through
the question arises why do humans have such a long period of small growth after
the postnatal period till puberty and why is this time window variable. Comparison
to other species shows that an intimate relation between growth spurt and men-
arche/puberty is present in primates, but not, for example, in mouse and rat. In
these species, growth is still proceeding after puberty, while in humans a strong
growth decline is found after puberty [41].
‘‘The essence of the primate system of development is that it is advantageous
that children should pass through a long period when they are relatively small and
weak. During this time, they can be kept in order, they are obedient (originally
because they are too weak to rebel), and they can be taught. Delayed growth may
also produce an important economy in food. If the species is to hold a considerable
part of its biomass in a stage when it is learning but not producing, then it is more
economical to feed a few kilograms of child than greater weights of adults’’ [41].
Now consider that human height has only increased: the last hundred fifty years
something less than 1 cm per decade and of course different for various countries.
However, the general increase in height holds for Europe and Northern America.
Therefore, an earlier maturation together with an increase in height is present,
which also includes weight. All kind of explanations are given: better nutrition,
better environment, although the economical poorer classes ‘‘have gained only a
little more than the richer’’ [41]. Increase in height should be related to heredity.
Hybrid vigor (called heterosis) and selection have been proposed among others. In
general, none of them give the solution. ‘‘We are left without any single con-
vincing explanation. The phenomenon must be a recent one, since it obviously
cannot be extrapolated backwards indefinitely’’ [41].
This is the situation as it was studied, say around 1980. In 1986 till 1998, the
Dutch results came out: the mean height increased from 161 cm in 1860 till
181 cm in 1990, supporting the increase in height in Europe and in USA. ‘‘The
Dutch are currently the tallest nation in the world—young men averaged 184 cm
and young women 171 cm in the 1997 Dutch reference. The rate of increase in
Dutch conscript height was greater in the twentieth century than in the nineteenth
and greater after the Second World War than before. In recent years, the rate has
slowed although small increases were still evident up to the 1980s, while con-
scripts from other European countries, particularly in Southern Europe, have
continued to increase in height’’ [42]. So, seemingly, a plateau is reached, which is

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502 21 The Pelvis During Childhood and Puberty

also supported by the trends in Scandinavia. The Dutch overview has a strict
inclusion criterion: two Dutch parents for each child, excluding heterosis from
other countries. At the end of the twentieth century, women increased less than
men, accentuating the gender height difference. But most important are Japanese
studies that showed that the secular trend of increase in height is in the first two
years of life and is caused by the increase in leg length [42].
‘‘Several other studies have shown that in the latter half of the twentieth cen-
tury, menarcheal age stopped falling and it has now stabilized at about 13 years
and may even have risen slightly in some places. This cessation in trend has also
occurred in Dutch boys since 1980, as judged by testicular volume, but not yet in
US boys based on pubertal stage’’ [42].
Thus, age at menarche and increase in height has stopped or nears a plateau and
boys indeed showed a decrease in age at puberty, which also tends to end. It is the
growth of the legs in the first two years of life that mainly determines height: it is
not related to puberty or its growth spurt.
Here, we see that the age at menarche was going down, while above (see
introduction of this chapter) we have seen that a lower age at menarche should
produce a lower sex ratio. In fact, more females, or less males, should be born.
Hardly any opinion can be made to this question. We know that at the end and
directly after the World Wars I and II, more males were born in all of the bel-
ligerent countries. Sex ratios, defined as amount of males per 100 females born,
were going up. For other wars (e.g., The Korean war, 1950–1952; The Vietnam
war 1965–1973), data of sex ratio rise are disputed, due to lack of data or different
interpretations [43]. Thus, a declining sex ratio as should be expected from the
decline of age at menarche is at least masked by the induction of sex ratio increase
by both World Wars.
And what about the pelvis: We hardly know anything. Heterosis between
separated villages in Ukrania has been studied. The outcome was that the width of
the pelvis had a small increase in boys, but this increase was absent in the children
that were subjected to stronger heterosis. So mixing of parents (outbred) from
different genetically similar (inbred) areas did not influence pelvic width in girls
and the small difference found in some boys could not really be related to heterosis
[44]. Other body parts indeed underwent influence of Ukranian heterosis, but not
the pelvis.

21.6.3 Leptin and the Testis

Leptin is a hormone secreted by adipose tissue that is involved in the signaling of


fat metabolism toward the brain. In the beginning considered as an anti-obesity
hormone, it later became clear that it is involved in ‘‘inflammation, angiogenesis,
hematopoiesis, immune function, and most importantly, reproduction’’ [45].
Leptin is not only produced in fat tissue, but also in the hypothalamus among other
tissues. Leptin can be noticed by its receptors in the anterior pituitary, ovary, and

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21.6 Testis and Ovary 503

Fig. 21.9 Leptin effects on


hypothalamus, pituitary, and
testis by leptin produced in
white adipose tissue (WAT),
GnRH gonadotropin releasing
hormone, LH luteinizing
hormone, FSH follicle
stimulating hormone
(reproduced with permission
from Tena-Sempere and
Barreiro [47])

testis. Leptin production or its inhibition occurs by hormones: insulin increases


leptin production as estrogens do, while androgens suppress leptin production.
Leptin increases gonadotropin releasing hormone secretion and other hypotha-
lamic prohormones and neurotransmitters, but also anterior pituitary hormones
like: LH and FSH. It is obvious that leptin is related to gonadal steering, due to its
influence on gonadotropic hormones.
‘‘What are the data linking leptin concentrations and pubertal development?
Several large studies in children have shown a strong correlation of serum leptin
levels with adiposity as determined by body mass index. In general, girls have
higher leptin levels than boys, although some investigators note that the concen-
trations are indistinguishable at the same relative fat mass. As pubertal development
begins in boys, or just before its onset, there is a marked relative rise in leptin levels,
whether reported cross-sectionally or longitudinally’’ [46]. Leptin levels in boys
have their highest peak just before puberty or at start of puberty. Testosterone
appearance coincides with a decrease in leptin levels toward baseline levels. In girls,
a consequent rise of leptin levels occurs during puberty and a direct relation between
the leptin increase and menarche was established. This gender difference is called
the sexual leptin dimorphism. ‘‘Leptin appears to be a necessary but not sufficient
factor for the initiation of puberty in humans’’ [45]. The interaction between leptin
and the gonads is still unclear and is certainly multi-factual. Although the literature
hypothesizes leptin actions for the hypothalamus, pituitary, ovary, and uterine
endometrial effects, attention is focused here on the testis (see Fig. 21.9).
Production of leptin occurs in the fat tissues. Leptin increases production of
gonadotropin releasing hormone within the hypothalamus. Simultaneously regu-
lation of LH and FSH occurs in the pituitary, while there is also an induction of LH
and FSH by pulsatile release of gonadotropin releasing hormone. Leptin’s pituitary
action can be excitation or inhibition. Leptin has a direct effect on the testis, where
its effect is dependent of testosterone: Leptin can decrease testosterone effects, but
testosterone inhibits leptin production in the fat tissue. Together with testicular
feedback mechanisms, a tentative scheme of leptin testicular effects is illustrated in
Fig. 21.9 [47].

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504 21 The Pelvis During Childhood and Puberty

Thus, leptin is involved at the start of male puberty. Still a good understanding
of leptin’s function in male puberty is absent, which is due to leptin’s multifactual
properties in various cycles like energy metabolism, neuro-endocrine system and
reproduction.

21.6.4 The Ovary and Puberty

In ancient societies where the ovary was unknown, the uterus was thought the
organ of reproduction. In ancient Greece, the female was clearly inferior to the
male, but she was considered the mean of reproduction. Interest, therefore, in
infertility was large with the female always being the source of infertility. Male
infertility was hardly accepted. The logical consequence was that the uterus
contained the cause of infertility [48]. Uterine remedies, like fumigation, as carried
out during the Middle Ages, did not work.
Although Aristotle (384–322 BC) knew that the spaying of animals prevented
fertilization, the relation with ovary function was not made. The ovary as an
anatomical structure was recognized around 50 AD by Soranus of Ephesus. In the
late Middle Ages, Henry de Mondeville, Leonardo da Vinci and Berengario da
Capri (see Chap. 2) all discerned the ovary as a peculiar structure, although its
function stayed unknown. It lasted till the seventeenth century before convincing
evidence was produced that human females produced eggs (see part Chap. 2 on
Regnoldus de Graaf [1641–1673]) and real research on ovary function and
infertility could start. The first to describe that the ovary contained eggs was Niels
Stensen for the dogfish in an addition to his Elementorum Myologiae Specimen
(1667). In 1675, he extended his findings to several mammalian species in ‘‘Ova
Viviparorum Spectantes Observationes.’’ The work of Regnoldus de Graaf in
‘‘Epistola de nonnullis circa partes genitals inventis’’ (1668, one year later than
Stensen’s publication) established that the human females contained eggs in the
ovary, although de Graaf held the surrounding cells and its interior (together called
follicle) for the eggs. His results were confirmed in 1678 by Caspar Bartholinus
(1655–1738). The follicle error was corrected by Malpighi (1628–1694), who
supposed the egg within the follicle and correctly said that the follicle cells were
present to protect the ovum and did not leave the ovary. The production of the
corpus luteum (luteum = yellow) from it was not understood by Malphigi,
although he named and studied the corpus luteum in the cow (in the cow, the
corpus luteum is yellow). In the mean time, a serious discussion between de Graaf
and Swammerdam arose who discovered the egg first. Both game-cocks had to
admit that Stensen was the first. Still the honor went to de Graaf [49].
In fact, the basic functioning of the ovary was known at the start of the eigh-
teenth century, although different opinions were advocated still [49].
Human females produce an enormous amount of germ cells (Fig. 21.10).
Counts go up to 7 million of which in females over 400,000 germ cells will
develop in premature eggs (primary oocyte, Fig. 21.10) with their specialized

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21.6 Testis and Ovary 505

Fig. 21.10 Left panel shows the amount of germ cells at age, while the right panel shows the
development of germ cells into an egg related to stages of birth and ovulation (reproduced with
permission from the Cambridge University Press from R. V. Short (1972) Species differences in:
Reproduction of mammals 4: Reproductive patterns

surroundings then called primordial follicles. One can calculate that females need
in between 200 till 500 eggs for their reproductive years. There is an overpro-
duction of primordial follicles that need their stages of development to mature to a
full grown egg that can be fertilized. In each of the stages of development to be
passed, the follicles can degenerate. Finally, only few will make it into an ovulated
oocyte. Why this inherent reduction occurs is unknown.
The development of the germ cell into an egg that can be fertilized varies for
different species in time. While most mammals are born with primary oocytes in
the ovary (Fig. 21.10), the rabbit, ferret, mink, vole, and hamster are born with less
developed germ cells. Follicular development to nearly mature oocytes
(Fig. 21.10) occurs in all mammals before and during puberty. However, the first
reduction in chromosomes happens in dog and fox after ovulation. In most
mammals, this occurs before ovulation. Experimental results obtained in one
species therefore are difficult to transmit to another species, especially man.
Ecological effects on animal reproduction should be considered with care if
applied to humans. One of these articles has the subtitle: ‘‘What do pseudoher-
maphroditic polar bears have to do with the practice of pediatrics’’ and its first
sentences are: ‘‘What do pseudohermaphroditic polar bears and girls with pre-
mature breast development have in common? Hormones. Sexual differentiation
and the initiation of secondary sexual characteristics, such as breast growth, are
under the control of sex hormones, estrogen and androgen. Abnormal

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506 21 The Pelvis During Childhood and Puberty

differentiation of the internal or external genitalia in bears and early onset of breast
development in girls also may have a common element-exposure to environmental
hormones. It has been shown that many common pesticides and environmental
contaminants can act as estrogens or anti-androgens’’ [49A]. It is an extensive and
rather good overview of ecological effects on sexual development in the animal
kingdom including men. The pediatric conclusion is far more balanced: ‘‘Because
so much of the material is so new and experimental, concrete recommendations are
difficult to make’’ [49A]. However, such a subtitle does attract readers.
Most people do not know that the ovary is a hard working organ. It begins
already during earliest months of fetal life by the production of germ cells. The
follicles start to appear in the fourth month of the pregnancy and their number
increases. The start of the reduction in the amount of DNA during meiosis causes
the death from the sixth month on of a large amount of these follicles. Thus,
degeneration of germ cells is one of the processes going on during fetal life
(Fig. 21.10). The situation is hardly different from birth to puberty. The ovary is
still working: letting follicles grow and afterward they degenerate, called atresia.
The ovary grows during childhood. In the first year, three large, fluid-filled fol-
licles can be discerned, around 6–7 years of age six are present and just before
puberty 12 are found. All these developed large follicles that are produced before
the menarche will disintegrate. This amount of large follicles, together with the
scars left, is responsible for the ovary’s increase in volume (Fig. 21.11). Seem-
ingly, a screening process is present that is needed for the selection of the egg cells
at fertile life. So to say the ovary is trained in this process during childhood and
hormone increase at puberty let some of them pass for ovulation [50].

21.6.5 The Polycystic Ovary: The Anovulatory Woman

So, proliferation and degeneration go hand in hand in the ovary and eggs are
produced at each cycle at one side. But it can go wrong. In nearly 5–10 % [50]
(recently 22 % was found [51]) of the women polycystic ovaries are found, which
means that no ovulation occurs. Polycystic means that several Graafian follicles
are empty and filled with fluid, while the supporting cells are also damaged. It is a
multifactor syndrome determined by: of course, presence of polycystic ovaries,
mostly established nowadays by ultrasonic methods, and androgen excess, with
symptoms like disturbances of the menstrual cycle, obesity, male hair distribution
(hirsutism), and acne. ‘‘Polycystic ovary syndrome is the most common endocrine
disorder of women in their reproductive years. It also has a huge implication for
society as a whole, as these women are at an increased risk of obesity, have a
markedly increased risk of diabetes and death after a myocardial event and might
also be at long-term risk for other cardiovascular disease’’ [51].
It is only possible to determine the disorder nearly two years after the menarche
and over 12 cysts, measuring 2–9 mm, have to be present in the ovary using
ultrasound tests (see Fig. 21.12 right panel) and/or an ovary containing over 10 ml

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21.6 Testis and Ovary 507

Fig. 21.11 The ovaries of children at different ages: a newborn; b 10 months; c 9 years old
(reproduced with permission from Peters et al. [50])

volume [51]. Vessels next to the ovary can appear like cysts, especially if blood is
dammed up or congested (see Fig. 21.12 left panel) [17]. A fault diagnosis can be
the consequence.
We know that a too high frequency of the pulsatile gonadotropin releasing
hormone discharge is involved, causing a rather high level of LH. This high level
changes the ovulum surrounding cells in their activity of FSH production. Low
FSH levels stop the development of the egg and can lead to degeneration. The high
concentrations of circulating androgens do also affect the insulin metabolism
producing hyperinsulinemia. Although the relation between androgen and insulin
levels is linear, such a relation is not proven for obesity.
Obesity is present in 35–50 % of the women with polycystic ovaries. An
increase in waist-to-hip ratio is noticed and visceral, abdominal fat increases. The
raised insulin, androgen, LH and leptin levels in women with polycystic ovaries
are somehow involved in their obesity, although the mechanism is hardly under-
stood. Increased risks on diabetes 2 and cardiac failure are present in obese
anovulatory women.

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508 21 The Pelvis During Childhood and Puberty

Fig. 21.12 Left ‘‘A 13-year-old female with prominent parauterine vascular plexus. Longitudinal
scan of the bladder (asterisk) and left ovary demonstrates prominent parauterine vessels (arrow)
which may simulate follicles on grayscale images. Doppler flow helps to differentiate vessels
from follicles. Note a 2.8 cm prominent follicle (cursors)’’ [17]. Right ‘‘A 15-year-old girl
presenting with 6-day history of abdominal pain. She had had only one period at age 12 and not
menstruated since. In this sexually active adolescent a transvaginal ultrasound was performed.
The right ovary (cursors) measures 4.5 9 2.2 9 3 cm (15 ml); multiple follicles (F) are noted.
The ovarian stroma (arrow) demonstrates increased echogenicity. The left ovary appeared
similar. Findings are consistent with PCO’’ (reproduced with permission from Stranzinger and
Strouse [17])

Polycystic anovulatory women still can have a spontaneous ovulation in the less
severe cases, while treatment is possible to abolish the infertility. The symptoms
are graded in their appearance for the various women, and therefore, the disease is
sometimes difficult to establish.
The increased frequency of gonadotropin releasing hormone is caused by the
hypothalamic and pituitary’s networks. The high levels of androgens during
childhood and puberty are presumably responsible for the change in network
function producing the increased pulsatile frequency of this hormone, with all its
consequences described above. Seemingly, there is a genetic predisposition for the
disease due to the familial clustering present [51].

21.6.6 The Ovary and Acupuncture

‘‘Despite the lack of a large body of evidence, we should not ignore the fact that
many women with reproductive disorders, and in particular women with polycystic
ovary syndrome, use acupuncture. Clinical and experimental evidence demon-
strates that acupuncture can be a suitable alternative or complement to pharma-
cological induction of ovulation, without adverse side effects. Clearly, acupuncture
modulates endogenous regulatory systems, including the sympathetic nervous
system, the endocrine system, and the neuroendocrine system’’ [52].

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21.6 Testis and Ovary 509

Above we have seen that ovulation still can occur in cases of polycystic ovary
syndrome. Therefore, randomized trials are necessary to ascertain that acupuncture
indeed induces ovulation in this syndrome. The hypothetical way of the acu-
puncture effect is that the placed needles activate the pain system. This information
reaches the hypothalamus via the spinal cord. One of the substances that is
increased is beta-endorphin in the hypothalamus, which changes gonadotropin
releasing hormone discharge and by it the FSH and LH production. Beta-endor-
phins are a cleavage product of the prohormone proopiomelanocortin, which we
already encountered at the arcuate fatty acid sensing. The other pathway is by the
spinal cord that can mediate effects of the autonomic nervous system, which also
innervates the gonads [52]. The effects reported was in between 40 and 50 % in
uncontrolled trials, whether ovulation and/or menstrual cycles were induced.
These trials contained anovulatory women, thus not only polycystic ovary women,
making it difficult to decide whether the acupuncture had effect in polycystic ovary
syndrome or not. A placebo effect can reach up to 30 % of cases studied. The
authors wisely said: ‘‘Randomized clinical trials are warranted to evaluate the
clinical effect of acupuncture in reproductive disorders’’ [52].

21.6.7 The Mono-Ovulating Human Female:


The Alternating Ovulation

This part is placed at the end of this chapter because we do not know why women
produce one egg per cycle and why the left and right ovaries are mutually active.
The alternating ovulation theory is questioned. Some authors privilege random
production, others right- or left-sided ovulation.
One thing is clear the left ovary must know the existence of the right ovary and
vice versa, if the alternating ovulation theory is correct, since it is the ovary that
organizes. But do not let us get ahead of the story.
We start with sheep. ‘‘In female mammals, the underlying mechanisms that
control the number of ovulating follicles in each estrous cycle, i.e., the ovulation
rate, are still poorly understood. Women, cattle, goats, and ewes have generally
one or two offspring, whereas other mammals, such as rodents, dogs, or sows, are
highly prolific and produce four or more offspring’’ [53]. By the way, dizygotic
twins are in humans 1 % of the births, confirming that human females are mono-
ovulating in 99 % of the cases.
In sheep, different breeds exist that have different prolificacies. In these breeds,
it was found that the ovulation rate (amount of ovulating follicles per cycle) can be
genetically manipulated. This can be done by a set of genes or in certain breeds by
influencing one gene. These single genes that determine the ovulation rate in
several breeds are called fecundity genes. They have romantic names like: In-
verdale, Hannah, Belclare, Booroola, according to the breed’s name. These genes
change a protein system called the bone morphogenetic protein system, indicated

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510 21 The Pelvis During Childhood and Puberty

Fig. 21.13 Effect of mutation in fecundity gene on follicle development and ovulation. For
explanation see text. GC granulose cell, E2 estradiol (reproduced from Fabre et al. [53])

by its abbreviation BMP. The change of one or two amino acids in the BMP
protein is sufficient to diminish its effect. This system was known by its function in
bone formation, but is also active in the reproductive system. It belongs to a family
of growth factors and receptors like: growth and differentiation factors (GDF),
activin/inhibin peptides, anti-Mullerian hormone (AMH, see Fig. 10.4). All these
proteins and their receptors are expressed in the oocyte and can influence its
nucleus and by which other substances are secreted differently by the oocyte. They
also influence the supporting cells of the oocyte, so-called theca and granulose
cells. The mutated genes reduce the BMP protein effect, and by it the ovulation
rate increases.
It is based on the fact that reduction in the effect of BMP increases the effect of
FSH, producing more follicles to develop in maturity (Fig. 21.13). The feedback
toward the hypothalamic–pituitary axis stays equal, because more maturing small
follicles produce the same feedback as one large follicle does. This feedback is
organized by estrogen-like substances and inhibin, the last we discuss later on.
‘‘The oocyte, acting through specific secreted proteins, is not only implicated in
follicular growth but also in the control of the number of ovulating follicles’’ [53].
Thus, in sheep, the mutual involvement of the oocyte and the hypothalamic–
pituitary axis determines the amount of eggs and that process is regulated genet-
ically by one or several genes. Now we know how mono-ovulation versus poly-
ovulation is organized, but still we do not know whether alternate ovulation is
present or not.
In 1985, a glycoprotein was isolated from bovine sperm fluid that could block
FSH effects, called inhibin, while one year later its antagonist activin was detected,
capable of enhancing FSH effects (see Fig. 21.14 for actions). Although we know

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21.6 Testis and Ovary 511

Fig. 21.14 Overview of the external and internal factors involved in the egg development in the
multilayered follicle. Stippled arrow denotes inhibition, and straight arrows indicates activation.
AMH anti-Müllerian hormone, BMP bone morphogenetic protein, EGF epidermal growth factor,
FGF fibroblast growth factor, FSHR, FSH receptor, GDF growth and differentiation factor, GH
growth hormone, IGF insulin-like growth factor, LIF leukemia inhibiting factor, KL Kit ligand,
NT neurotropin, TGF transforming growth factor, VIP vasoactive intestine protein (reproduced
with permission from van den Hurk and Zhao [55])

now that these glycoproteins are present in various tissues in the body, it originally
was thought to be glycoproteins solely involved in the feedback and control
mechanisms of the hypothalamic–pituitary–gonadal axis. Since the human female
is mono-ovulating a dominant follicle occurs, the one that will produce the egg. To
keep its dominance, it has to suppress the others that are also in development. So to
say it has to kill its competitors. This dominant follicle secretes large amounts of
estradiol and inhibin (Fig. 21.13) into the circulation, by which inhibin reaches the
other developing follicles in the same ovary, but also the other ovary. The inhibin
action is presumably related to the suppressing of the oocyte competitors devel-
opment [54]. In polycystic ovary syndrome (see Sect. 21.6.5), inhibin is not
released in a pulsatile way, but keeps a constant level, thus constantly reducing
FSH effect. This causes the mal-development of the ovum with infertility as its
consequence.
The amount of factors, receptors, and hormones involved in oocyte develop-
ment that are detected increase steadily (see Fig. 21.14, which shows only
development of the factors, receptors, and hormones for one of the stages). It
indicates that the process of egg development has been underestimated till recently
and it is impracticable to treat all the systems involved (for overview see Van den
Hurk and Zhao [55]).
Non-random distribution of the dominant follicle was found in cows after
pregnancy. The corpus luteum of the previous pregnancy changes presumably the
ovarian situation in such a way that the other ovary produces the next egg [55].
Studies in humans are difficult to interpret. However, studies on primates showed a
random occurrence of ovulation. In a study concerning 572 natural human female
cycles, it was found that after a right-sided ovulation the following ovulation was

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512 21 The Pelvis During Childhood and Puberty

in 56 % again at the right side and in 44 % at the left side. If the initial ovulation
was at the left side, in 52 % of the cases, a right-sided ovulation occurred again
and in 48 % a left-sided ovulation was found. Statistics showed no significance for
the same or other side after left- or right-sided ovulation. The conclusion drawn is
that the process of ovulation is a random event not influenced by the history of the
previous location of ovulation [56, 57].
This intricate system of producing a fertile egg normally needs some cycles to
be in function. Therefore, the menarche during puberty will be followed by a few
cycles in which the system has to start up and egg production is still in its
childhood.
Studies on ovulation and the ovum got a boost by the possibility to culture
primordial oocytes and let them develop into ovulating follicles (see Fig. 21.10).
These studies started together with cryopreservation of human eggs and sperm.
Both techniques are applied in the preservation of fertility in man and woman
weight down by cancer. Whether it is in woman with breast-, ovarian-, borderline-,
cervical- or endometrial cancer both chemotherapy and/or radiation can destroy
women’s fertility, which also holds for male fertility.
Before chemotherapy and/ or radiation therapy cortical strips of the ovary,
containing primordial follicles, ripe follicles or eggs are collected and cryopre-
served to be replaced into the ovaries after successful therapy. Happily, in the
majority of these females their cycle returns spontaneously after therapy. Ovarian
cryo-banks are now overcrowded with tissue since these pretreatment measures are
only needed in restricted cases.
The same holds for men, in which sperm collection should be offered to all
before therapy. Sadly enough these possibilities to preserve fertility are often not
or inconsequently offered to both male and female patients.
To preserve fertility surgical techniques are also adopted: Uterine transplan-
tation is still studied and is one method, the other is radical trachelectomy
(removal of only the cancerous cervix segment and reconnect rest of uterus and
vagina) to replace radical hysterectomy and lymph node dissection in cervical
cancer [58].

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Chapter 22
The Pelvis and Aging

In this chapter on aging, beside other subjects, attention is given to imbalance and
the role of the pelvis, especially femur–pelvis–trunk balance problems and its
consequences: falls. The degeneration of the genital organs and of the uropoetic
system in the elderly are considered. A view on genetics in relation to aging
finishes the chapter.
Death would not have been an evolutionary necessity in a world of unlimited resources.
The pervasive nature of the limited resources paradigm can be easily illustrated. The
unrestrained growth of a bacterial culture for 14 days would yield a biomass exceeding the
actual biomass on earth. After 200 generations, the number of bacteria would even exceed
the total number of atoms in the universe [4].

22.1 Introduction

In 1968, IBM Nederland published ‘‘Mens and Machine’’ (Man and Machine)
containing texts on automatons, androids, and robots [1]. This overview indicated
that several authors described that robots can fall in love, or man can fall in love
with an automaton, but all automatons, androids, or robots missed the reproductive
organs and those for sexual pleasure; seemingly, platonic love is the case. Even the
well-known duck of Jacques de Vaucanson (1709–1782) that had a functioning
digestive tract, producing even excrements, lacked genital organs (Fig. 22.1).
Construction and restoration of robots are carried out from the outside. Con-
struction and restoration in the living being occurs inside the body and are
immanent properties. Such regenerative capacity, whether on DNA, cellular, or
tissue level is inherent to the biological world. The turnover of structures, like cells
or tissues, is rather high in the living being. There is a constant renewal. The
turnover of the total protein content in the human body lasts 100 days. So, at least
three times in a year, our body is totally renewed. For certain tissues, it is even
faster.
In 2003, IBM published ‘‘the vision on autonomic computing’’ that concerned
the information and communication technology (ICT) interest in the (autonomic)

E. Marani and W. F.R.M. Koch, The Pelvis, 517


DOI: 10.1007/978-3-642-40006-3_22,  Springer-Verlag Berlin Heidelberg 2014

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518 22 The Pelvis and Aging

Fig. 22.1 The eating duck


automaton. The figure is from
the ‘‘Grand Dictionnaire
Universel du XIXe Siècle’’ of
1867, because Vaucanson
kept the construction of the
duck secret

nervous system of vertebrates in general and man specifically. It originates from an


emerging field known as autonomic computing. This term was first introduced by
IBM in 2001 [2], and it has inspired many ICT researchers to propose and evaluate
new closed-loop architectures for managing (i.e., monitoring and controlling)
information and communication components and networks [2A]. Autonomic
computing aims at computing systems that can manage themselves. The conno-
tation autonomic is used as analogy to the autonomic nervous system of man as the
autonomic nervous system regulates body functions (organs such as smooth
muscles, glands, and viscera) autonomously (i.e., unconsciously). However, most
approaches in autonomic computing only point toward this analogy and rarely
study or apply the true control features known today about the autonomic nervous
system. Still updates have to be found elsewhere, and only a limited amount of bits
are used for program restoration and checks within the PC or server.
The inherent programs of restoration in living systems, like those in computers,
become worn out over the years of use. Restoration in elderly is still going on, but
no longer at their optimal possibilities. This is called aging. So, in elderly inherent
restoration is still going on, but its quality is reduced.
‘‘The rate-of-living theory of aging postulates that longevity is inversely pro-
portional to metabolic rate. Although the theory is flawed in its strict sense its
circumstantial features reflect some important implications of the oxidative
damage and mitochondrial theories of aging. There is no doubt that a variety of
metabolism-related features have an impact on aging-dependent processes’’ [3].
Aging has not only been related to the damage by oxidative stress and dysfunction
of mitochondria, but also to programmed cell death and malfunction of DNA
repair [3]. Discussions on terminology are present in the literature: Aging is
defined as: ‘‘The inherent decline over time, from the optimal fertility and viability
of early maturity that may precede death and may be preceded by other indica-
tions, such as sterility.’’ Senescence in their formulation (in Gene Ontology [4]) is
a subcategory and not a synonym of aging and is defined as: ‘‘The process that
occurs in an organ near the end of its active life that is associated with the

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22.1 Introduction 519

dismantling of cell components and membranes, and an overall decline in


metabolism’’ [4]. Whatever the philosophical and scientific discussions and
research, here we stick to the simple definition that aging is the worn out of the
living being.

22.2 History of Aging Research

The maintenance of health is undoubtedly the chief good and foundation of all other goods
in this life… and I am sure that we might free ourselves from innumerable diseases both of
the body and the mind, and perhaps even from the infirmity of old age, if we had sufficient
knowledge of their causes (René Descartes, 1637, cited from J. Cottingham’s The ratio-
nalists, Opus, Oxford University Press, 1988).

‘‘Oedipus may well be the best-known old man from Greek and Roman
mythology, in part because of the fame of Sophocles’ plays about him, in part
because his story is intimately connected to a riddle that has implications for a
concept of the life span. According to tradition, the Sphinx sat outside of Thebes
and asked passersby a riddle. If they could not answer the riddle, she killed and ate
them. In its simplest form, the Sphinx asked: What has one voice and is four-
footed, two-footed, and three-footed? What goes slowest when it has the most
feet? Oedipus answered that the riddle fit human experience, because infancy goes
on all fours, maturity on two feet, and old age with the help of a cane (the third
‘foot’). At hearing the correct answer, the Sphinx killed herself. The answer may
imply that to some degree the human life span is circular; that is, it begins in
dependency in childhood and returns to dependency in old age’’ [4].
Greek and Roman mythology hardly contributes more to aging, except that it is
in most cases a situation of misery [4]. It is sometimes related to immortal life, like
the Gods possessed.
An exception is Epicurus (341–270, Fig. 22.2). He is also known as the
‘‘philosopher in the garden.’’ Epicurus gathered his friends and disciples in a
garden, called Kepos. Here, he proclaimed his philosophy: live ‘‘simple’’ but
enjoy. He opts for ‘‘Joy of living.’’ One can reach such a situation by health and
peace of mind. One can arrive at it by ‘‘self-restraint, being in control of one’s life,
a knowledgeable way of handling matters of dying and death and the awareness of
the importance of balance for all aspects of life. Thus, the principles are sketched
of an Epicurean health care, which aims at joy of living as the ultimate objective of
human actions in general and medicine in particular’’ [4A]. This also holds for the
elderly. Sex and food should be enjoyed, but ‘‘Joy of living’’ should be considered
with a clear brain or judgement, called phrosyne. So enjoy in moderation. Epicurus
has been severely misinterpreted in hedonism, but in modern terms, he says don’t
stress, but look for happiness, don’t overeat or over-drink, enjoy sex and in
decisions in these matters use your brain. In fact, that is what modern gerontology
advocates too.

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520 22 The Pelvis and Aging

Fig. 22.2 Bust of Epicurus


from the Musei Capitolini in
Rome, photo Marani

We leave out all Middle Ages’ nonsense on maiden breath that made old people
young, secret medications to overcome aging, immortality by the fountain of live
and pure, blessed live that gives prolongevity (eternal longevity), but turn to one of
the famous medical doctors that lived at the end of this period.
Garbriele de Zerbis (1445–1505), who we encountered shortly in Chap. 4, is a
pre-renaissance scientist. He tried to organize gerontological principles and gives
directions for aged people in his Gerontocomica, scilicet de senum cura, atque
victu (1489) [Gerontocomica, care for elderly is required, also by (good) food]. De
Zerbis published a small book on the ethical conduct of the physician (De cautelis
medicorum [4B]), in which he hardly brought up new ethical aspects but stressed
again the importance of correct behavior toward the patients. It shows his profound
sympathizing with the sick. This is his basis for the study of aging, at least to help
the elders to overcome neglect.
The word gerontocomos is from the Greek and means: ‘‘people whose business
it is to handle skilfully the care of aged,’’ which is de Zerbis proper definition [4C].
The book gives the various periods and peculiar qualities of old age and causes of
old age in Man. It treats its ‘‘swiftness and slowness’’ and its causes, together with
accidental accompaniments of old age like: gray hair, baldness, and wrinkles. De
Zerbis also indicated the early signs of aging and the foreknowledge of brevity and
longevity. A chapter entitled: ‘‘The necessity or inevitability of the advent of old
age of man as he passes through the stages of life to death in an orderly manner’’
leaves no doubt that de Zerbis refused to believe the humbug on eternal life.
Then, the book gives advices and guidelines on how the gerontocomos should
behave: his conditions and duties. Simple things, such as the proper bed for the
aged, baths and rest, clothing, how often old people should be fed each day and
the time, are given. Food is the main target of de Zerbis to organize good health of
the elderly: benefits of wine in recovery of the aged, selection of water, bread,
meat of wild animals and birds. Milk products and eggs, together with salt and oil
are discussed, but also honey, sugar, garden vegetables, aromatic herbs, and fruits.

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22.2 History of Aging Research 521

The patients’ day and night rhythm is advised. When and how, to use blood-
letting, clysters and purging by urination is also indicated. Picking the teeth and
dentifrice in preserving the health of the aged are not forgotten.
Since this book considers the pelvis, some citations are given from the small
chapter: ‘‘Permission and prohibition of sex in the resumptive regimes. Thus, when
the warmth and humidity of which the life of old men consists are evacuated (by
coitus, addition ours), a speedy death results. For those old men who are in the first
stage of old age sex is not entirely forbidden as it is for those more advanced in old
age, for the powers of the former are not so weak nor the frigidity and dryness of
their bodies so great. (In the humor theory of the Middle Ages, one becomes old by
loosing heath and by drying out) …… But if in any way sex may be permitted to
old men, let the act be carried out at such a great interval of time that the old man
may not feel the weakening of strength from it…… Sex is not useful in summer or
autumn although it is more tolerable in autumn. If possible, sex should be com-
pletely avoided in summer’’ [4C].
Although the Middle Ages’ philosophical concept behind aging, due to believe
in humors, is totally different from nowadays approach, the directives and advices
are not too bad. At least the elderly were guarded properly and were well fed as
long as de Zerbis instructions were followed by the physicians and neglect
overcome.
Before one thinks: ‘‘this concerns the Middle Ages,’’ it is perhaps good to
remark here that elderly neglect and abuse, somatic and/or psychological, nowa-
days is in between 3 and 17 % of the population above 65 years: Norway and USA
3 %, Canada 4 %, Finland 5 %, Britain 9 %, and Sweden 17 %, and that it is
related to the spouse in 58 % and their adult children in 24 % of the cases; aged
men and women are equally neglected or abused [4F].
Also in Padua lived, at the end of his career, Luigi Cornaro (1464–1566: note
his age!). He wrote discourses on ‘‘How to live 100 years, or discourses on the
sober live.’’ Being in a weak health until his 35th years, the physicians ordered that
he should refrain from overeating and over-drinking, which he consequently
carried out. The main theme is ‘‘be sober,’’ don’t consume too much and you will
become hundred years without disease and the inescapable death will pass easily
(remember that longevity is inversely proportional to metabolic rate, see intro-
duction). Agricultural activity, working in the garden and rest at fixed times will
help. ‘‘Cornaro believed that longevity could be extended by simple reforms of an
individual’s life habits. He believed that some very simple hygienic practices
would influence the length of life and the condition of a person’s health. This view
has it counterparts today, that personal dietary habits, exercise and activity pat-
terns, exposure to noxious environmental influences, and stress influence how long
and how well we live’’ [4D]. Thus, at the start of the Renaissance guidelines for
longevity and aging were present, well comparable to ours. Whether its spread
reached more than the rich, educated ranks of society stays doubtful, although
Cornaro’s discourses resided rather long in the interests of people.
Throughout the end of the Middle Ages and Renaissance, the ‘‘artigiani’’ or the
hand workers started to apply simple arithmetic to increase production quality in

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522 22 The Pelvis and Aging

their professions. It is the start of the study of mechanics for all kind of purposes. It
eventually will lead to relevance in astronomy, arts, and other sciences. The time
span in which these developments occur is between 1543, Copernicus’ De revo-
lutionibus orbium coelestium, and 1678 with Newton’s Philosophiae naturalis
principia mathematica [4E]. Mechanics is also used in anatomy. Leonardo da
Vinci is the best-known example, but also by Giovanni Borelli (1608–1679) in his
De motu animalium (movement of animals, 1675) with rather clear similarities (or
is it plagiarism?) with Leonardo’s work [4F]. Borelli, a professor of mathematics
in Messina, Sicily, and later on in Pisa, studied the movement of animals in a
biomechanical approach. The influence of mechanics has been summarized in:
‘‘The mechanization of the world picture’’ [4E] and its power can still be recog-
nized in aging studies, especially at the moment statistics is added.
We make a jump now toward the nineteenth century. The collection of large
amounts of data on mortality and age, sex, and several other properties of human
life, together with applying mathematics by Adolphe Quetelet (1796–1874) laid
the foundation for modern gerontology. Francis Galton (1822–1911), Charles
Darwin’s cousin, corresponded with Quetelet on mathematics, but was also
interested in human health and aging. Galton placed his results in the concept of
the ‘‘human machine,’’ the mechanistic idea frequently used in anatomy and
physiology in those days. ‘‘One of his major contributions to the study of aging
was his gathering of data at the International Health Exhibition of London of 1884.
Over 9.337 males and females aged 5–80 years were measured on 17 different
functions’’ [4D]. So the nineteenth century science organized the tools like data
collection and mathematics that made the study of aging possible in the twentieth
century and brought it out of isolated facts to general propositions that could be
tested by mathematics, which is indispensable in gerontology.

22.3 Pelvic Organs During Aging

Armand Leroi in his book Mutants (2003) [4E], by discussing that genetic
mutations can be the cause of aging and considering existing theories, notes:
‘‘… ageing is the collective consequence of many different mutations that grad-
ually wear down and then destroy our bodies. Perhaps this is why, despite much
effort, the mechanistic causes of ageing remain so elusive. The root of ageing’s
evil has been claimed, at one time or another, to lie in any one of a dozen aspects
of human biology. Some have claimed that it is caused by the fermentation of
bacteria in our guts; others by a slowdown in the rate at which the body’s cells
divide; yet others have pointed to the exhausting effects of bearing and raising
children. Others again have proposed that ageing is caused by the exhausting of
some vital substance, or else that chemicals produced by our own cells gradually
poison us. Many of these ideas are probably absurd, but some probably contain at
least an element of truth.’’ However, even genetics hardly give an answer. Pre-
sumably large amounts of genes or mutated ones that have their effect late in one’s

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22.3 Pelvic Organs During Aging 523

lifetime are involved in aging. Although the screening for these genes are on the
way, a clear genetic solution is still absent. It therefore seems senseless to con-
struct a theoretical frame in which aging of the pelvis should be explained, which
means that mainly an overview of data can be given. (By the way switching on or
off, a gene is also a mechanistic view).

22.3.1 Reproductive Organs

‘‘Signals from the brain modulate reproductive maturation and aging in animals.
Thus, an interplay between gonads and brain drives the dynamics of both repro-
ductive phase and aging and elicits reproductive cessation as aging-related fea-
ture’’ [5]. The consequence of this cessation is hormone withdrawal or hormonal
decrease. The pelvic reproductive organs react on this change by an alteration of
the morphology and cellular structure of its organs. The uterus is reduced by 60 %
and its endometrial thickness is fourfold diminished. The cervix is decreased to
80 % of its mature volume, being the least in uterine reduction. The ovary is
reduced to 60 % of its volume during reproductive life, although larger shrinkages
are reported in the literature: a nearly fourfold reduction in postmenopausal
Swedish women [6].
‘‘Androgen decline in the aging male’’ is called ‘‘andropause’’ [6]. The prostate
doubles its volume during andropause. A strong shrinkage of the testis was also
found from 60 years of age on. Decrease in semen volume or semen quality gives
contradictory results in the literature [5]. In general, the changes of the internal
reproductive organs are large, both in males and in females. The male, nevertheless,
stays capable to reproduce at old age, while females loose that ability due to their
menopause. Menopause is a typical human phenomenon. A nearly abrupt ending of
female fertility that is within months is absent in mammalian species, presumably
except in whales. In most mammals, fertility slowly fades out with age.
Aged men encounter serious health risks due to their prostate. Infections are
mainly overcome in youngsters by the high concentration of zinc in the prostatic
fluid. ‘‘There is a great deal of popular literature purporting that intake of zinc is
beneficial in preventing urinary infections and prostate disease, but this is
unsubstantiated’’ [5A]. Bacterial prostatitis is the most common cause of infections
of the uropoetic system in aged men. Nevertheless, science does not know the
cause of bacterial prostatitis, ‘‘and as a result, physicians are frequently unsuc-
cessful and frustrated in their attempts to treat patients’’ [5A].
The other threat is enlargement: benign and malicious ones. Benign prostatic
hyperplasia starts at the age of 30 and a constant rise occurs via 50 % at the age of
50 till 75 % at an age of 80. It is noted by the patient due to problems with initiating
the stream, slow force of the stream up to dripping, start and stop of the stream,
straining to urinate, and incomplete bladder emptying [5A]. Medical treatment is a
pharmacological one before surgical treatment is applied, which is inevitable if
kidney failure (obstructive uropathy), urinary retention, or recurrent urinary tract

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524 22 The Pelvis and Aging

infections occur. Adenocarcinoma of the prostate is the second main cause of


cancer death in the USA. ‘‘Men in the USA have a 9.5 % lifetime risk of developing
prostate cancer and a 2.8 % lifetime risk of dying of prostate cancer. Clearly,
prostate cancer is a major health problem in aging males’’ [5A] (Italics ours).

22.3.2 The Uropoetic System

Dysfunction of bladder and urethra is mainly connected to urinary incontinence.


In order to study the epidemiology of urinary incontinence, one needs a workable
definition. Such a definition is given by the International Continence Society (ICS).
‘‘In 1988, the ICS defined urinary incontinence as the involuntary loss of urine that
is objectively demonstrable and is a social or hygienic problem. Recently (2002),
the ICS redefined it as the complaint of any involuntary leakage of urine. The
impact of the new definition is that more cases of urinary incontinence will be
discovered and hopefully treated’’ [7]. The other impact is that results before 2002
can hardly be compared to results from after 2002. It is, however, clear that the old
definition is a more conservative one and therefore our premise. Where it is nec-
essary results from after 2002 will be added, indicated by *.
There exists a gender difference in urine incontinence caused by the difference
in anatomy of the uropoetic system and the difference in hormonal function in the
elderly. The results given here are a mean from a series of studies carried out
between 1980 and 1992 [8]. The aged population starts at the cohort from 60 till
65 years.
Incontinence prevalence is 15–20 % (24 %*) of the aged male population and
is for women 20–25 % (53 %*). In a Dutch study, 62.5 % was found in a popu-
lation of females aged between 45 and 85 years [7A]. These figures rise to
30–50 % in nursing homes for both sexes. Thus, one out of three or one out of two
persons in a nursing home is incontinent. The rise in urinary incontinence in
women starts at an age of 25 years and is continuous till 50 years when the
prevalence reaches its peak. Afterward, a decrease occurs till the age of 65. Then, a
steady increase happens again. For men, it starts at 45 years of age with a constant
rise till 75 years, after which the percentage is constant. In the young healthy
population (their early twenties), 3 % males and 15 % females are already urinary
incontinent.
The prevalence data are seriously undermined, since even women in managed
care institutions stay undiagnosed for urinary incontinence [9]. This must mean
that percentages presumably are higher than those published.
The cost increase for incontinence is estimated 3–10 % of the nursing home
expenditure. The insurance companies in the Netherlands spent in 1980 40 million
guilders and in 1990 180 million on incontinence materials: a more than fourfold
increase that is still rising. In 2001, a commission, installed by the Dutch Minister
of Health, estimated the total expenses of incontinence treatment (doctors, nursing
home costs, incontinence materials, etc.) in the Netherlands on 612 million

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22.3 Pelvic Organs During Aging 525

guilders, leaving out the costs of physiotherapy. One can estimate that in the
Western world, the costs are billions (USA alone 2 billion dollars) [9], if on the
Dutch population of 16 million already 612 million guilders (results from before
the euro) were spent. Indeed, aging is the main factor for the increase in urinary
incontinence and elderly people are more dependent on support of family, insti-
tutions, and/or nurses and are a heavy cost burden on the health insurance system.
Special studies bring up astonishing results: ‘‘Urinary incontinence was expe-
rienced by 41.5 % of the female athletes. Its prevalence across the 3 types of sport
(female athletics, basketball, and indoor football athletes) was similar and was not
affected by age. However, athletes who experienced urinary incontinence had a
lower body weight (P = 0.011) and a lower body mass index (P = 0.035). Most
(95.5 %) athletes had never discussed their condition with a health professional. In
the focus group, all athletes described preventive urination to avoid urine leakage.
It was mentioned that urinary incontinence affected their performance and made
them feel uncomfortable and frustrated’’ [10]. Sports are thought to be beneficial
toward urinary incontinence. The study was carried out in Portugal, not a country
thought of underdevelopment.
Racial results are also staggering. The National Health and Nutrition Exami-
nation Survey provided information on urinary incontinence in community-
dwelling men. Black man indicated the highest prevalence of urinary incontinence
21 % (17 % for all men in this study), while black women have the lowest
prevalence: 20 % (38 % for all women in the study) [11]. Moreover, low levels of
education and poverty are related to higher percentages of urinary incontinence
[11, 12]. One should not underestimate the social factor during aging.
The extensive prevalence studies seemingly go on all fours, despite their enor-
mous amounts in the literature. Whether this is due to non-diagnosis, racial differ-
ences or social circumstances, the spread in results are large. Only one fact is beyond
doubt: females suffer more from urinary incontinence then men, although at old age
the difference seemingly disappears. It also indicates that large studies (with some
exceptions [13]) that include the correct set of parameters are missing. Moreover, the
results for certain countries are rather different for women with urinary inconti-
nence: ‘‘The lowest prevalence was in Spain (23 %), while the prevalence was 44,
41, and 42 % for France, Germany, and the UK, respectively’’ [13]. The question on
doctors consult showed: ‘‘About a quarter of women with urinary incontinence in
Spain (24 %) and the UK (25 %) had consulted a doctor about it; in France (33 %)
and Germany (40 %), the percentages were higher’’ [13]. However, always less than
half of the women with urinary incontinence consult a doctor.

22.4 Hip Problems in Elderly

Before one can understand why hip problems are so frequent in older people,
attention should go to the change in gait movements of elders. The question
studied in several papers is: ‘‘Does aging changes the coordination of head, trunk,

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526 22 The Pelvis and Aging

and pelvis movements during walking and standing while executing a rapid head
motion? Since most falls in aged persons occur in their own residence during
walking or in positional transitions, such as getting up, turning around, bending
over, it is necessary to understand balance control during similar tasks’’ [14].
One can easily notice in the streets that elderly people walk differently, react
slowly on traffic lights, think of their behavior at pedestrian crossings. How often
are people not irritated by their slow adaptation to the pedestrian lights? Thus,
aging changes their gait, but also their head movements. The interrelations
between head and trunk–pelvis–leg adaptation to movements are changed in aged
people, while this combination arranges their balance, since in the head the ves-
tibular system is localized that steers trunk, pelvis, and legs for equilibrium. Aged
people have to adapt to a changed balance. Research shows that head movement in
aged people is nearly 50 % slower than in young ones and during walking this
phenomenon stays present although somewhat less. Trunk movements, especially
horizontal ones, during gait are larger in young persons [14]. ‘‘Pelvic motions
induced by head movements were significantly larger during walking as compared
to standing in young subjects but not in the elderly. Furthermore, a significant
interaction effect due to postural condition and head motion direction was
observed such that pelvic rotations induced by horizontal head motions were
significantly larger than pelvic tilts induced by vertical head motions during
walking but not during standing’’ [14]. Thus, in young and old persons, horizontal
head movements are different in their consequences for pelvic rotation than ver-
tical ones, and the pelvic movement is larger in young people. In every type of
movement, the elderly reduces the needed trunk–pelvic change as compared to
youngsters. ‘‘Head motions were significantly slower and smaller in elderly sub-
jects and resulted in disrupted horizontal plane trunk–pelvis coordination during
walking’’ [14]. The cause is in the reduced function quality of the motor–sensory
system and the same holds for the vestibular system [14]. It is all the consequence
of the decline of the aged nervous system.
‘‘Falls in older people are a major public health problem, with one in three
community-dwelling people aged over 65 years falling each year. Approximately
two-thirds of falls in older people occur while they are walking, and it is therefore
not surprising that a number of studies have reported significant differences in gait
patterns between older fallers and non-fallers. These differences include reduced
velocity and step length, increased variability in step length and cadence, reduced
peak hip extension, and less rhythmic accelerations of the upper body. These
findings suggest that, despite adopting a more conservative basic gait pattern, older
people who fall have difficulty maintaining the stability of the body’’ [15].
Although the older people try to adapt to their walking problems, some are more
sensible to such gait problems than others.
Gait analysis together with asking for fear of falling and looking to sensori-
motor functions resulted in Fig. 22.3. Decline of sensorimotor function causes
reduction in the step length. Both have an indirect effect on head stability. The fear
of falling is strongly related to decrease in step length but has nearly no direct
influence on head stability. Reduced step length has a large influence on pelvic

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22.4 Hip Problems in Elderly 527

Fig. 22.3 Multivariate model of Menz et al. [15] for the relations between gait changes and their
causes. Values are standardized regression coefficients. Reproduced with permission

stability; it increases pelvic instability and has a less but still significant effect on
upper body attenuation. It is mainly the pelvic (in)stability that is directly related
to the head (in)stability. A less direct effect is caused by upper body attenuation.
Absence of head stability (during head movement, the head can still be stable!)
induces feeling of lack of equilibrium and induces falls [15]. Here, the study
started not at the head position but at the other side: the gait of older people with
reduced step length. In both studies, the importance of the pelvis in balance of
elderly people is undeniable, and consequently, the pelvis is significant in falls.
‘‘Since older people have a lower hip extension, mainly by contractures, they
have to compensate for it by an anterior pelvic tilt that is necessary to keep a
reasonable step length,’’ is the result of another kinematic study [16]. Moreover, step
length is indeed changed even in youngsters, if pelvic rotation is inhibited [15A].
In all directions, mediolateral and sagittal, the pelvis has to be adapted in its
movements to changed step length, inducing pelvic instability in elderly with the
consequence that equilibrium is absent by head instability and causes fall.
Till now we looked into the relation trunk–pelvis–legs. Some other aspects of
aging can be noted if one focuses on vertebral column and pelvis in aging.
The pelvis bears the vertebral column, which by its sagittal S form makes
stability and resilience possible. Human balance is also pertained by vertebral
column balance. ‘‘The mechanically obligatory sagittal curves contribute to a
spinal balance that is constantly changing according to posture and movement and
which varies from one individual to another according to morphotype, age, and
pathology. Sagittal balance fundamentally expresses a postural strategy mobilizing
the dynamic structure of the lumbar–pelvic–femoral complex in an authentic
balance by which obligatory coupled movements transmit stresses in a single
structure, the spine, to the two-part structure of the lower limbs, and vice versa’’
[17]. Imbalance can occur by loosing the S form of the vertebral column, inducing
deformation of the lumbar spines mainly noted by low back pain. It is the lum-
bopelvic stability that protects the lumbar spines: ‘‘Lumbopelvic stability, pro-
vided by both passive joint characteristics and active muscle activity, protects the
lower back from injury during loading conditions’’ [18].
The vertebral column balance, if disturbed, can only be brought back by exertion
of more muscle power. The main muscles involved are the abdominal and pelvic

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528 22 The Pelvis and Aging

muscles in order to get the center of mass back before the sacral second vertebra [17,
18]. Studies on low back pain in women showed that pelvic surgery performed earlier
in life will produce low back pain during aging. This occurs mainly because pelvic
muscles and abdominal ones are maltreated and did not recover from surgery: ‘‘Our
findings suggest that a potential injury to the pelvic and lower abdominal muscula-
ture, surgical menopause in this case, puts women at increased risk for low back pain
later in life. Women reporting a surgical menopause described moderate low back
pain more often than women with no history of gynecologic surgery. Biomechanics
and neurophysiologic research is posing mechanisms for how the deep pelvic and
abdominal muscles provide lumbopelvic stability’’ [18]. The unspoken consequence
is of course imbalance by loss of lumbopelvic stability.
The same holds for spine surgery, in which the pelvic and abdominal muscle
activity cannot overcome the loss of lumbar lordosis anymore. It was ‘‘demon-
strated how subjects able to retrovert the pelvis on lateral views were unable to
maintain the retroversion while walking, due to gluteus maximus deficiency: the
trunk tilted considerably forwards, due to pelvic anteversion’’ [17]. The conse-
quence is imbalance during walking, which the patient tries to overcome by flexion
in the knees and position change of the pelvis (Fig. 22.4). The answer is surgery to
restore lumbar lordosis and thoracic kyphosis; note the amount of screws and the
cable along the implants in Fig. 22.4.
Thus, both in spine surgery in aged people and in aging after gynecological
surgery pelvic muscles play an important role in keeping balance or in keeping
posture in aged people. Imbalance in aged persons can also be due to deformation
of the vertebral column or the appearance of low back pain that indicates pelvic
and abdominal muscle damage.
There are two more aspects on which we should zoom in: shoes and handgrip.
Now, we have established how important pelvic movement is in keeping balance in
aged persons, the question arises: what are the consequences for the overall
movement? We leave out here muscles of the leg, which is highly incorrect, since
muscle leg activity also plays an important role, but otherwise one ends up with
ankle and knee anatomy and function of the elderly, which is good for another book.
Let us start with shoes. ‘‘The results indicate that shoes with elevated heels or
soft soles impair walking stability in older people, especially on wet floors, and
that high-collar shoes of medium sole hardness provide optimal stability on level
dry, irregular, and wet floors’’ [19]. Eight different types of shoes and three dif-
ferent floors were tested: a dry linoleum floor, an irregular floor covered with
artificial grass, and a wet linoleum floor. The irregular and wet floor induced
reduced step length and we know from the text above what this means. The soft
sole shoes are behaving the worst in testing normal floor versus wet floors in this
study, while other studies contradict these results. It is important to find out the
difference, since grandmothers on slippers are burned on our retinas.
The comparison between high-heeled and low-heeled shoes in young and aged
people shows that the high-heeled shoes forces elderly to adapt their gait more
during stair walking. In general, high-heeled shoes are less fit for elder women [20],
which does not come as a surprise. What is a surprise is that unstable shoes, as used

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22.4 Hip Problems in Elderly 529

Fig. 22.4 Restoration of


lumbar lordosis in an aged
person. a Concerns
identification of flexion
contracture. b Shows the
disappearance of the flexion
contracture due to operation.
(Reproduced with permission
from Husson et al. [17])

in physiotherapy to improve balance, indeed increases some aspects of balance in


women aged over 50 (mean age 60, spread 53–66 years) [21]: ‘‘results of the
present research suggest that dynamic balance tasks such as standing on an unstable
surface and responding to an external threat to balance can be improved by pro-
longed use of the footwear’’ [21]. In general, high-heeled or soft shoes are detri-
mental for aged people in keeping balance, but balance training is possible.
The second aspect is object transport during walking: said in normal language,
carrying something during walking. If one carries a box the finger grip adjusts to
the walking difficulty one encounters and to the box surface for a good grip. By
passing an obstacle, your finger grip increases. However, aged people show:
‘‘Grasp control changes in older adults only during obstacle crossing suggest that
overall task demands (balance requirements, attention demands) may contribute to
declines of manual dexterity in functional tasks. This highlights the need to
investigate grasp control within complex tasks when aiming to understand

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530 22 The Pelvis and Aging

impairments of older adults encountered in daily life’’ [22]. It explains why aged
people drop objects easily by obstacle crossings. Thus placing the cup of tea on the
table, while the chair is still in front (between table and the aged person) can
induce the drop of the cup of tea. By adding speech during gait, ‘‘walking while
talking,’’ the aged people that already has a slow gait, experience a 20 % reduction
in gait, while younger people lessen by 9 %. ‘‘In practical terms, this means that a
large proportion of healthy community-dwelling older adults may not walk fast
enough to safely cross the street’’ [22]. The consequence: if you help an older
person crossing the street, don’t talk!
Thus keeping balance, in which the pelvis plays such an important role, stret-
ches further then fall. It impairs largely a series of lower body movements but has
also consequences for the upper extremity. This should mean that physiotherapy
have to pay more attention to the pelvis, both its bony and muscular parts, and to
foot wear.

22.5 Falls

Now that we know the causes and mechanisms of falls in the aged, it is time to
look at the consequences. ‘‘Studies have consistently shown that 30–60 % of
individuals aged 65 and older will experience one or more falls in a given year.
These incidence rates are remarkably high particularly when one considers that
most studies are likely to underreport the true incidence of falls. Incidence rates
appear to be higher in institutional settings, females experience more falls than
males, and the frequency of falling increases with age’’ [24]. Overviews show that
20–30 % of the falls results in soft tissue damage and 5–10 % produces bone
fractures. Hip fractures are the most common fractures after fall in aged people.
The USA is confronted with 250,000 hip fractures each year for people older than
65 years. Hospital care is lasting longer (21 days in 1996) and the health care costs
are 9 billion dollars. ‘‘In many cases, the hip fracture is ‘the beginning of the end.’
In nearly 30 % of the cases, death occurs within one year of the fracture, usually
due to complications such as pneumonia, thrombosis or fat embolism. Even if the
faller does survive, there is often a loss of mobility and independence’’ [24]. If
lonely aged persons fall and stay at the floor for one hour or more, 50 % of them
will die within 6 months. Psychological consequences are extreme fear for another
fall with the consequence of restricted mobility [24].
Mechanical perturbation and posture control failure are the main causes. They
occur virtually anywhere, but at home frequently in the bedroom and bathroom
and 5–10 % of the falls occur on stairs. ‘‘Even though the elderly use stairs much
less than younger adults, persons over 65 account for 85 % of the deaths resulting
from stairway falls. Head injuries, relatively rare in level surface falls, comprise
approximately 30 % of the injuries due to stairway falls’’ [24]. There is no relation
with the seasons. So, slipping in winter is not significant more than that in other
seasons. Most falls (50 %) occur during walking and 25 % of them are related to

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22.5 Falls 531

slipping. All others are related to bumping into an obstacle, pushes (aggressive
behavior of others belongs to it), and missteps (think of uneven pavements).
Seemingly, there are intrinsic and extrinsic causes. Balance control being one of
the most important of the intrinsic ones. Most of the extrinsic ones are well known
(see above). There are medical factors that are important in relation to falls: visual
impairment (cataract), neurological disorders (dementias), abnormalities of the feet,
and osteoporosis to name a few. Let us not forget medication: antidepressants and
sedative medication easily induce falls due to a change in the control of balance.
Aged people are more vulnerable to traffic accidents [25]. They do not produce
more accidents then younger people, but the impact of accidents is simply greater
in the elderly. One should note that older people drive safer compared to
youngsters, especially compared to youngsters below 20. Moreover, aged drivers
are nowadays more experienced than 20 years ago [25]. There is a lot more to say
on the aged and traffic, but brings us out of the scope of this chapter.
Whatever the situation, the aged are for it. Falls are unavoidable in the aged
with dreadful consequences. We have seen the importance of the pelvis in falls.
This significance of the pelvic structures is rather underestimated and prevention
does not care at all for the vital involvement of pelvic structures in falls.
But are there no preventive measures possible? One has to point to the robot gait
trainer LOwer-extremity Powered ExoSkeleton (LOPES) developed at the Twente
University at the department Biomechanical Engineering in the Netherlands.
‘‘Besides the common hip and knee flexion and extension, the LOPES robot
allows pelvis translations in the horizontal plane and hip ad-/abduction. These
additional ‘natural human motions’ may be beneficial for training as they allow
leaving balance control related tasks to a patient [25A].’’ This robot system trains
also the pelvic movements and helps in balance training. Most other robot systems
do not permit pelvic rotation [7A]. Although developed for stroke patients with an
affected leg, its contribution to elderly is presumably the present-day prospect.
From Leonardo da Vinci’s and Giovanni Borelli’s studies on, biomechanics has
been developed into a powerful mechanistic approach of gait, resulting in a robotic
aid that can be applied in the recovery of disturbed human movements. It lasted
nearly 350 years before recovery robots could be built, indicating that human gait
was a hard case to tackle.

22.6 Genetics

A series of diseases induce aging by the late effect of the matching mutation.
Huntington and Alzheimer belong to these types of illness. Mouse studies by
removing genes or changing genes also induce early aging or even longevity. The
question is: are these mutations present in humans and do they induce human
aging? At cell, tissue, and organ levels, aging has been studied, but only few studies
bring up the involvement of genes in the human population during normal aging.

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532 22 The Pelvis and Aging

We direct ourselves to the ‘‘Leyden Academy on vitality and ageing’’ research


that has the possibility to study over 1,200 aged persons in combination with data
of other institutions. A lot of the participants are over 80 years old. In this cohort
of aged people over 85 years, called the oldest old, it is meaningful to look into
genetic effects on aging and longevity.
‘‘In conclusion, although the study of model organisms has revealed potential
candidate genetic mechanisms determining aging and life span, to what extent they
explain variation in human populations is still uncertain’’ [26]. The summary of
genes and proteins involved in aging till 2008 concern: insulin/IGF-1 signaling
(IGF, insulin growth factor), klotho gene, forkhead transcription factors, apoli-
poprotein E gene, anti-oxidative enzymes, macromolecule repair mechanisms, and
p53 gene [26]. From this series, two, insulin/IGF-1 signaling and p53 gene, were
tested in the Leyden 85 ? study.
Decreased insulin/IGF-1 signaling is associated with ‘‘reduced body height and
improved age survival’’ [27]. These effects are restricted to women. The gender
difference is based on the relation between growth hormone (-releasing hormone)
and insulin growth factor that differ in males and females (see also leptin and testis
in the chapter pelvis and puberty).
The p53 gene is known for its protection toward cancer in mouse studies. The
Leyden study showed that p53 indeed protects against cancer in humans. However,
this protection is at a cost of longevity [28]. The first contours of the genetic
involvement in normal aging are appearing. Nevertheless, the results till now are
too few to produce a multifactor genetic hypothesis for normal aging.
More general theories are developed on non-mammalian species results. The
disposable soma theory says that all efforts put into longevity by the organism,
which are metabolic, are deleterious for early fitness attribute, meaning repro-
duction [29]. Longevity is at cost of reproduction. A study concerning the British
aristocracy around 1700 (‘‘a closed and environmentally uniform society’’ [29])
showed that ‘‘women with more durable somas (greater investment in maintenance
and repair) lived longer at the cost of reproductive success’’ [29]. So ladies over
80 years old had produced fewer children than those that died before and on their
80s. Eight studies did find such a relationship and eight reported a negative
relationship [30]. In short, the hardly discussed issue is the inverse answer: pro-
ducing children was dangerous. Embryo, fetus, and birth around 1700 were a threat
to the mother (Chap. 2, [30]), and genetic inbred was already large in British
aristocracy, even before 1700 (70 % of the wives of peers came from aristocracy,
including peers, baronets and knights, and 60 % of the wives of peers were
daughters or close relatives of peers [30A]). Both factors contribute to pelvic
problems. Inbred and pelvic changes are well known in humans [30A] and ani-
mals, e.g., dogs [30], both based on genetic studies. Clearly, a lady with only one
or none birth had a larger survival chance, due to fewer pelvic dysfunctions and
thus a higher chance on longevity.
The discussion on longevity and reproduction is still going on and concerns also
socioeconomical parameters, birth intervals, gender differences, health selection,
and frailty [30]. The final word on aging and genetics has not been spoken till now.

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22.6 Genetics 533

At the end of this chapter, we return to handgrip strength. In the part 4.0 on hip
problems in elderly, the imbalance caused by mainly pelvic restricted movements
has its effects on the upper extremity too and on handgrip behavior by passing
obstacles. The Leyden group also studied handgrip strength. The result is that in
550 aged persons of 85 years, ‘‘poor handgrip strength predicts accelerated
dependency of activities of daily living and cognitive decline in the oldest old.
Measuring handgrip strength could be a useful instrument in geriatric practice to
identify those oldest old patients at risk for this accelerated decline’’ [31].

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(2003) Reproduction and longevity among the British peerage: the effect of fraity and
health selection. Proc R Soc Lond B 270:1541–1547. Cannon J (1984) Aristocratic
century: the parage of eighteenth century England. Cambridge University Press,
Cambridge
31. Taekema DG, Gussekloo J, Maier AB, Westendorp RGJ, De Craen AJM (2010) Handgrip
strength as a predictor of functional, psychological and social health. A prospective
population-based study among the oldest old. Age Ageing 39:331–337

sergiocamargo47@gmail.com
Epilogue

To understand why pelvic science is in arrear in comparison to other sciences, the


first chapters of ‘‘The pelvis, another view’’ focused on history. Poor research into
the morphology of the bony pelvis and into the topographical relations and
suspensions of the pelvic organs in combination with premature clinical
application of the results explains the present state of pelvic science.
Throughout the years, the same mistake was repeatedly made, both in diagnosis
and in the surgical treatment of urinary and fecal incontinence.
The other chapters highlighted several new developments and interesting study
objects.
Inside as well as outside the pelvis, an intricate connective tissue architecture is
present, which is largely neglected in anatomical research and in pelvic surgery.
In cardiology, the electrocardiogram is the gold standard for most diagnoses,
while flow is (far) less used. The reverse is true in urology. Urinary flow and
pressure, however, are determined by a series of partially unknown parameters and
therefore difficult to interpret. Smooth muscle electromyography has been largely
neglected, and those few studies that were performed were ill received due to the
interaction with noise.
Moreover, recent research indicates that smooth muscle electrical activity is
related to smooth muscle relaxation and contraction both. This calls for a new and
modern approach of smooth muscle electromyography.
The approach to sphincter research is inadequate in most studies, because the
sphincter is modeled as a simple switch. Recent studies use more sophisticated
modeling techniques, which open a better understanding of sphincter function.
However, since experimental data on sphincter morphology and physiology are
still lacking, the models contain too many estimated parameters.
This book is a plea for more thorough research in pelvic science. A general
research effort is needed, like the decade of the brain, and fundamental research
should be stimulated. Problems emerging from clinical and surgical procedures
can only be solved if it is known how the normal pelvic anatomical and
physiological interactions can be restored. Main focus should thus be on
fundamental research.

E. Marani and W. F.R.M. Koch, The Pelvis, 537


DOI: 10.1007/978-3-642-40006-3,  Springer-Verlag Berlin Heidelberg 2014

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Acknowledgments

During the preparation of the manuscript, which is a sequel of ‘‘The Pelvis, another
view’’, several people assisted and helped us out on (nasty) problems. First of all,
we have to thank Richard Horobin and Albert Van Helden for correcting our
English and the discussions they induced by small but very important remarks on
several matters. Albert van Helden started discussions on ‘‘depiction in Anatomy’’
for which we are very grateful. Moreover, he advised on the historical part and
provided us with extra literature on Aristotelian philosophy. Due to his approach we
rearranged several of the pictures in the part on anatomy of the uropoetic system
and found support in our vision on ‘‘Philosophy’’ at the University of Padua.
The cooperation of the library of the Leiden Museum Boerhaave is appreciated.
The copyright department (J. A. N. Frankhuizen) and the ‘‘Douza-kamer’’ of the
Leiden University Library were very helpful in reproducing figures. Marc Kappers
of the Medische Bibliotheek of the Foreest Medical School Alkmaar was an expert
in tracing the literature.
Several scientists gave us the possibility to cite freely from their texts:
• Dolf Gogelein for the use of his booklet on stone cutting;
• Matti Kinder for the article on ‘‘A method for the electromyographic mapping of
the detrusor smooth muscle’’;
• Marijke Slieker-ten Hove for information on physiotherapy in The Netherlands;
• Dick Daems  for the free citation of the opening address of the first Erasmus
Winterschool;
• Hans Landsmeer  and Piet Donker , together they started the Leiden research
group on the uropoetic system in the 1980s, and both provided us with pictures
for use in this and other publications;
• Peter Veltink for providing us with literature and advice on engineering aspects;
• Ciska Heida for corrections on skiff rowing;
• Hans Maathuis for information on the part ovulation and peritoneal space;
• Selma Mourad for check on development of the ovary;
• Jan Voogd, Jos Droës, Carmen Vleggeert-Lankamp and John Gosling for figures;
• Toon Huson for explanation on the closed kinematic chain;
• Paul Klück for some of his figures that were never published;
• Henk Punt for checking the part on symmetry;
• Tinde van Andel for checking on the Suriname story;

E. Marani and W. F.R.M. Koch, The Pelvis, 539


DOI: 10.1007/978-3-642-40006-3,  Springer-Verlag Berlin Heidelberg 2014

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540 Acknowledgments

• The SWUN (Dutch working-group urodynamica)-members are thanked for the


discussions on all kinds of uropoetic subjects;
• The support of both the Maatschap Urologie Alkmaar and the Stichting Urologie
Research Alkmaar is appreciated.
A lot of discussions directed the text:
We enjoyed the discussion with Matti Kinder on electromyography. Jan van
Gool was always accessible to explain difficult urological matters and we esteemed
his approaches very much.
Together with SWUN-members EM organized several courses on
‘‘Urodynamics and Urine-incontinence’’ (1996) from which we learned a lot as
from the International Satellite Symposium ‘‘Pelvic Floor’’ (1993) and
postdoctoral course Urine-incontinentie van jong tot oud (1991). The 40th
Annual Meeting of the Society for Research into Hydrocephalus and Spina bifida
published ‘‘Dutch Anatomists and the Bifid Spine’’ (1994), which was a great help
in preparing the first parts of this manuscript. Pelvic master classes were held at the
Twente University that reunited several of the mentioned scientists to consider
pelvic problems.
Dineke Mulder (for the figures on ambulant urodynamics) and the whole
editorial board of Profundum are acknowledged. Some of the chapters are
extensions of small articles EM wrote for this journal. Our colleague De Blok is
acknowledged for the figures of septa in the corpus pelvinus from his thesis.
From our own group we thank: Erica Bastiaanssen, Marcel Heldoorn and Johan
van Leeuwen for their research and discussions on modelling, and their pictures
we could use, Egbert Lakke for his research on the descending projections of the
nucleus tegmentalis latero-dorsalis in the rat and the subsequent studies published
in his thesis, and his permission for using his figures. We thank Maarten Jan Pit for
the arcus tendineus fasciae pelvis figures. The Leiden Department of Anatomy is
acknowledged for the pictures and photographs made available to us, especially on
the retro-rectal space by Marco de Ruiter. The course on ‘‘Surgical Anatomy of the
Lesser Pelvis’’ opened my eyes for the clinical anal sphincter problems, so clearly
emphasized by B. Delemarre  and by his thesis.
My Bulgarian friends Wlado Ovtscharoff and Kamen Usunoff  provided me
with diapositives of classical preparations of the urogenital tract and of the male
uropoetic system not available anymore at our direct anatomical environment.
The Twente University contributed a lot. Its engineering approach to
biomedical problems is a special art: We thank Willemien Wallinga de Jong for
explaining the ins and outs on her ‘‘labor’’ studies and A. Schaaf for providing EM
with her manuscript. The Biomedical Technology Institute (now MIRA Institute)
gave EM the possibility to be lodged in his own one room-apartment, where he
wrote in the evenings several parts of this book. The Twente master-class
‘‘Anatomy and physiology of the pelvis’’ (2007) induced several discussions on
uropoetic engineering.
The former ‘‘Jan Drukker ’’ group published a series of theses on the
peripheral autonomic nervous system. We used a lot their thoughts on this subject

sergiocamargo47@gmail.com
Acknowledgments 541

as published by Gerbrand Groen, Bob Baljet and A. B. Boekelaar (), in the former
Acta Morphologica Neerlando-Scandinavica. The support of our secretary Wies
Elfers is acknowledged. The people of Marcillac-Lanville are thanked for the nice
and kindly ambiance during holiday summer times.
Last but certainly not least, both authors thank their wives Jantine and
Anne-Marie for their patience and support during the preparation of the book.

sergiocamargo47@gmail.com
Index1

A
Abdomen, 18, 20t, 74, 75, 76, 88, 193 in sheep, 509
of embryo, 190f ovarian cryo-banks, 512
and ligament, 181 right-sided ovulation, 511, 512
and peritoneum, 245, 246f Alternative medicine, 314
in pregnant women, 93 Cruydt-boeck (Dodoens’), 315
pressure, 452 Galenic/Hippocratic system, 315, 316
tocography, 371 homeopathy, 316
upper rectal artery, 276 placebo effects, 314
Abortion, 35, 47 unorthodox medical theory, 317
Achondroplasia, 10 Alvarez waves, 371
Activin/inhibin peptides, 510 Amenorrhea, 323t, 324
Acupuncture, 143, 349 American College of Radiology Imaging
and ovary, 508–509 Network (ACRIN), 253
beta-endorphins, 509 American Urological Association Symptom
points, 84, 237, 238 Index (AUASI) scores, 332f
Adenocarcinoma of prostate, 524 Amphetamines, 472, 473, 476
Adolescents Amphiarthrosis, 8
circumcision, 154 Anal sphincter, 191, 203, 211, 214, 217, 347,
deliveries, 487–488 394, 417. See also External anal
exterior male genitals, 499 sphincter
lower genital tract diseases, 497 after partial de-innervation, 455f
transvaginal ultrasound, 508f animal experiments, 451
Alcock, Benjamin, 340–341 defecation, 231
The Cyclopedia of Anatomy and Physiol- development, 201
ogy, 341 and levator ani muscles, 218
Alcock’s canal, 339, 341, 347, 348 normal, 455f
Alpha adrenergic receptor, 400, 401, 457, proctoplasty, 217
459f, 460 reflex, 379
Alpha-melanocyte stimulating hormone transanal repair, 219
(alpha-MSH), 486 Androgens, 164, 165, 266, 267, 268
Alpha-receptors (a-receptors), 381 anti-androgens, 506
Alternating ovulation, 509–512 excess, 506
egg development, 511f fat, effect of, 486
left-sided ovulation, 512 and leptin production, 503
mono-ovulation, 509 in puberty, 481, 508
mutation in fecundity gene, 510f in sexual differentiation, 505
synthetic androgens, 270

1
Note Page numbers followed by ‘‘f’’ and ‘‘t’’ indicate figures and tables respectively

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544 Index

Androgens (cont.) B
testicular androgens, 165 Bacterial prostatitis, 523
therapy, 270 Barrington’s nucleus, 225, 354, 355
Andropause, 523 Basedoïde type, 283
Angulus subpubicus, 7 Beaulieu de Jacques, 50–51, 51f
Anorectal malformations, surgery of, 215–219 Beijing Declaration and Platform for Action,
early approaches, 217–218 151
external sphincters, 218 Belly dancing and pelvic movements, 444–445
PSARP technique, 219 belly dance disease, 444
restricted anorectoplasties, 218 myoclonal belly dancers disease, 445
transanal repair, 219 triangle of Guillain-Mollaret, 444
Anorexia nervosa, 407 Benedetti, Alessandro, 89, 99–100, 101, 102
cannabis, therapeutic effects of, 477 Benign prostatic hyperplasia, 327, 328, 330,
fatty acid diet, 486 331, 333, 523
Ano-urethral reflex, 383 Benzopyran, 328
Ano-vesical reflex, 383 Beta adrenergic receptor, 400, 457, 459f
Anovulatory woman, 506–508 Beta-endorphins, 164, 301, 509
Anterior vagina nerves, 157 Beta-receptors (b-receptors), 381
Anthropometry, 430 Bidloo, Govard, 64, 65f, 104
Anti-Müllerian hormone (AMH), 266, 490, Anatomia Humani Corporis, 66
510, 511f life of, 64–65
Arcuate nucleus, 164, 408, 482, 483 pelvis
of hypothalamus, 485 description of, 66
normal physiology of, 486 half, backside of, 68f
Arcus pubis, 7 sacral bone, 67f
Arcus tendineus faciae, 188, 189f, 412, 418 Biomechanics, 125–126
Arcus tendineus levator ani, 412 balance arrangement of ‘‘bridge’’ girder,
Arcus urethrosuspension, 188 128f
Artificial sphincter prosthesis, 188 comparison with bridges, 127f
Atropa belladonna (deadly nightshade), 288 girdles, bony arches for limb support,
Australopithecines, 29 126–128
Australopithecus pelvis, 3, 3f, 30 model of lower body, 129f
Robert Tague’s calculations, 32 Birth canal. See also Human birth canal
shape of, 131, 131f dimorphism, 29–30
3D construction, 30, 31f Birth chairs, 433, 434
Autonomic computing, 518 disadvantages, 436
vision of, 517 Birth-mate, 433, 433f, 434
Autonomic nervous system, 159, 259 Black cohosh (Cimicifuga or Actaea), 324–326
acupuncture effect, 509 Bladder cancer
arcuate fatty acid sensing, 485 bacillus calmette-guerin (BCG), 471
autonomic computing, 518 epirubicine, 471
neurotransmitters, 281 keyhole limpet hemocyanin (KLH), 471
pelvic autonomic ganglia, 389 mitomycin-C, 471
pre- and postganglionic levels, 397 Bladder carcinoma, 251
Autonomic pelvic plexus, 344 Bladder electromyography (bladder EMG),
basic arrangement, 344, 645f 361
hypogastric nerves, 345 centers of activity, 368–369
parasympathic innervations, 344, 346f bladder voiding, 369, 372–373f
pelvic plexus, 345–347 cellular automaton model,
position of, 346, 347f 368, 370–371f
sacral plexus nerves, 347 fluorescent spheres, 369–371
sympathic trunk, 344 history, 362
Autonomic reflexes, 377 bladder waves, 363f
Autopsies, 22, 74, 76f, 493 drawbacks, 362

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Index 545

hook electrodes, 362 Braxton Hicks contraction, 373


nerve fibers, electrical activity, 363 Breast, 162
recording of, 364–366 and buttocks, 288
in rabbit’s bladder, 364, 365f, 366 for storage of nutrition, 301
in rats, 364, 366 embryonic breast bud, 268–269
single smooth muscle cell studies, in pig environmental hormones, 506
bladder, 366–368 female attractiveness, 286–287, 290
Bladder neck. See Trigone mammary line, 268
Bladder steering centers, 223–225 phantoms of, 165, 168
consciousness, 224 tumors, 169
coordination, 224 Buck’s fascias, 177, 193–197
micturition reflex, 224 Budding, 256
nucleus paraventricularis, 224 Buttocks, 291
in rats, 223 before and after surgery, 293f
spinal-bulbospinal reflex, 224 high-heeled shoes, 294
in human, 224 increased lordosis, 295
TLD, 224, 225f ideal buttocks, 292
Bladder stones, 48–49 lumbar hyperlordosis, 293
perineum, 49, 50f pain, 301
lateral lithotomy, 50–51 pelvic types, 294f
method of Celsus, 49–50 surgical lines for operation, 293, 293f
method of Marianus, 50
removal, 48
Blood vessels, 43. See also Subperitoneal C
blood vessels and ligaments Calcitonin gene-related peptide (CGRP), 268
connective tissue pillars for, 413–414 Calculus vesicalis, 48
pillar concept of DeLancey, 414f Campomanesia aromaticaa (adojakers), 321
Bone cuts, 17 CAMUS study, 331
Bone mineral content Cannabis, 476–477
dual-energy X-ray absorptiometry, 488 cannabinoid receptors in body, 477
and osteoporosis, 488 tetrahydrocannabinol (THC), 476
and sports, 488–489 effect of, 477
Bone morphogenetic protein (BMP), 223 and testicular germ cell tumors, 477
protein, 510 therapeutic effects of, 477
system, 509–510, 511f Cardiac output and blood pressure, 43
Bony pelvis, 1–6 Castration, 149–153, 161. See also
anatomy, 6f Circumcision
evolution of, 6 castrates, 162–163
foramina of pelvis, 177–179 definition, 161
gender differences, 6–8 modern castration, 163
in gorilla and man, 13f Catheterization and consequences, 469–471
and leg in, 14f bacteriuria, 469
orientation, 13f disinfectants, 469
posture, 8–15 Escherichia coli, 470
in bipedal motion, 11, 13 indwelling catheters, 471
postural balance, 16 modes of infection, 470
sacral bone, 12 Proteus mirabilis, 470
sacroiliac joint (see Sacroiliac joint) Catheters, 467
in spinal cord injuries, 15 history of, 467–468
and puberty, 486–487 gummi–elastic catheter, 468
and adolescent deliveries, 487–488 gummicatheter, 468
female puberty, 487 Cavum Douglasi, 271
menarche, 487 Cervical cancers, 153, 253, 254, 255, 258, 512
Borelli, Giovanni, 522, 531 Child birth, physiotherapy

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546 Index

Child birth, physiotherapy (cont.) neuronal connections in uropoetic system,


in the Netherlands, 229–230 386f
in the UK, 230 Cornea reflex, 377, 381
Chimpanzee (Pan), 343 Corpus pelvinus, 408–412
birth mechanisms, 38f connective tissue strips, 408, 410
pelvic shapes of, 131f female fetal pelvis, 410
pelvis of, 3, 3f septa (see Septa)
11
C-choline, 251, 252 gynecologists’ view, 408–409
Chronic bladder infection, 323t ischiorectal fossa, 411
Cimicifuga racemosa (black cohosh), reconstruction of septa in, 410f
324–325, 325f Costus scaber (Indianheadginger), 321–322
Circumcision, 149–153 Cowper, William, 64, 65f
in Arabian Peninsula, 149 plagiarism of, 65–66
female circumcision, 150 Cross-organ sensitization, 395
and HIV, 154 Cryptorchidism, 265, 266, 268, 269
male sexual pleasure, 151 Cryptorchismus, 490
and masturbation, 151 Cystourethropexy, 187
and social class, 149 Cytokines (interleukins), 40
in southern Chad, 150
Cisterna chyli, in human fetus, 278, 257t
Claudication, 261 D
proximal or buttock claudication, 277 Decubitus ulcers, 294
Clitoral orgasm, 157 Deflation reflex, 384
Clitoro-motor reflex, 384 Depo-Provera. See Medroxyprogesterone ace-
Cloacal membrane, 214, 215, 215f tate (MPA)
Closed kinematic chain, 129 Detrusor muscle, 305, 307
Cocaine, 324, 472, 474, 476 forces demonstration, 307–308
Coccygeus muscle, 201, 202, 206, 207, 208f, instability of, 309–310
209, 210, 237, 347 and incontinence, 309
Cod-liver oil, 329 midsagittal drawing, 310f
Collagen, 223 uncontrolled detrusor activity, 310f
cervical collagen changes, 40 Dextro-amphetamine, 472f
Colles fascias, 193–197, 195f, 196f Disease of Raynaud, 260
Computed tomography (CT), 249 Dorsal rhizotomy, alternatives to, 350
in pelvic lymph node cancer detection, cryotechnique, 350–351
249–250 selective stimulation electrode, 351–352
Connective tissue in pelvis, 407–408 symmetrical tripolar cuff electrode,
corpus pelvinus (see Corpus pelvinus) 351f
pelvic diaphragm, descensus of, 418–420 Dorsal root ganglion (DRG), 390
perianal connective tissue, 417–418 and autonomic sensory information,
perirectal fasciae, 416–417 390–394
pillars for blood vessels, 413–414 anal and rectal sensations, 394f
prolapse, 420–421 DRG neurons, 393
fifth finger goniometer, 420f ‘‘odder beast’’ characteristics of, 392
genital prolapse, 420 types of organization of, 391f
rectosacral fascia, 414–416 visceral afferents, 393
reinforcements in fascias, 412–413 Dry needle injection, 239. See also
Continence, flow charts and, 385–388 Acupuncture
bladder emptying, 387 The Dutch Society for Pelvic Problems and
bladder filling, 387 Pre and Postpartum Health Care, 230
controversial facts, 387 Duct of Müller, 216, 489
micturition (see Micturition) paramesonephric duct, 489

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Index 547

Duct of Wolff, 205, 211, 216, 489, 490 vulva deviations and child sexual abuse,
development of ureter from, 212f 497–498
mesonephric duct, 489 white spot disease, 498
Ductal breast carcinomas, 169 External urethral sphincter (EUS), 220–222,
Dutch regulations for drugs, 476 452–453, 460–462
Dystocia, 33–34 adipose-derived stroma cells, 462
nutrition and, 33–34 concept by DeLancey and coworkers, 461
in females, 221
fetus, 220f, 221f
E form of, 461
Early embryology, 204–206 increased pressure, 452
development, time frame of, 204f coughing, 452–453
heart beat, 204 in males, 221
pelvis fetus, 220f
pelvic diaphragmatic muscles, 204 stem cell-derived myoblasts, 462
structures in, 205f striated urethral sphincter, characteristics
Eating duck automaton, 518f of, 461
Ecstasy (party drug), 467
urine retention, 471
Ehlers-Danlos syndrome, 420 F
Electrical pelvic floor stimulation (EPFS), 348, Face and sex, 287–288
349 feminine facial characteristics, 287
Elephantiasis, 84, 151, 258 masculine facial characteristics, 287
scrotal elephantiasis, 259f vision, 288
Energy crisis hypothesis, 237, 238 Fascia endopelvina, 412, 414, 415
Epicurus, 519, 520f Fascia lata, 9f, 301
Epigenesis, 216 Fascia pelvis parietalis, 412, 415
Erectile reflex, 389 Fascia sling operation, 188
Estienne, Charles, 90, 100 Fascias, 206, 307
De dissection, 89–96 connective tissue reinforcements in,
female figure of, 91f 412–413
pelvic pictures of, 93f of glutal muscles, 301
Eunuchs, 161–165. See also Castration for incision for operations, 196f
Excavation rectouterina. See Cavum Douglasi ligaments and, 137f
Experimental embryology vs. holistic science, meaning, 197t
111–112 of muscles, 74
External anal sphincter, 450–452 Fat cells, 407
ampullar and anal area, view of, 451f Fecal continence, 417
damage chances, 452 Fecal incontinence, 47, 229, 241, 242, 417
External genitals, 496–499 Female circumcision, 147f, 149, 150, 151, 154
body weight and testis weight, in elephant, Female pelvis, 32, 88
497f connective tissue septa of, 410f
development of, 496f at different crown-rump length, 458f
innervation of, 155 evolution, human pelvic organ prolapse, 32
lower genital tract diseases, 497 in Hottentot woman, 12f
Miller test (three-prong obscenity test), 498 and male pelvis, 52, 63
phantoms of, 165–169 midsaggital section of, 306f
Bali Hindu population, 165 remolding of, 487
Indonesian Muslim population, 165 sexual dimorphism, 6
penis, 166 Femoral nerve, 91, 263
testes, 166 Fibroids, 493, 495. See also Leiomyomas
transsexuals, 169, 170 localization of, 494f
pubic hair, in girls, 497 Fibronectin, 223
sensibility of, 156 Finasteride, 327, 328

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548 Index

Finite element modeling therapeutic value, 329f


and pelvic diaphragm, 133–134 prostatitis, 326–327
reconstruction of, 133f saw palmetto (Serenoa repens),
and pelvic forces, 130–133 326–328, 327f
and pelvic organ movement, 134–136 saw palmetto (see Saw palmetto)
pelvic organ mobility, 135f systems biology, 333
Fistulas, 50, 78, 81t, 86, 214, 218, 219, 418 High-energy blunt traumas, 17
Flagellantism, 300. See also Spanking Hip problems in elderly, 525–530
2-[fluorine18] fluoro-2-deoxy-D-glucose gait analysis, 526, 527f
(18FDG), 251 grasp control changes, 529
Foot orgasm syndrome, 167–168 head movements, 526
Foot-binding, in Chinese women, 168 human balance, 527
Fossa ischiorectalis, 348f lumbar lordosis, restoration of, 529f
Fractures of the pelvis and acetabulum (Tile), shoes and handgrip, 528
22 spine surgery, 528
trunk movements, 526
trunk-pelvic change, 526
G vertebral column balance, 527–528
Gait. See also Hip problems in elderly History of Circumcision (Dunsmore and Gor-
phases of gait cycle, 132f don), 149
and vision, 297 HIV clinics, 152
gluteal sulcus, 300f Hoffmann, Friedrich, 316
and pelvis, 299 Hoffmann’s drops (Spiritus anodynus), 316
striding gait, 298 Holism and deviant, 123–125
walking and running, 130 conjoined twins, 124–125, 124f
Gastralia, 3 Homeopathy, 317
Genito-vesical reflex, 384 ‘‘high dilution’’ experiments, 319
GHB, 472, 476 high dilutions of
Gluteus muscle group, 295–297 histamine, 319
gluteus maximus, 295, 296f protein IgE antiserum, 319
gluteus medius, 296f propagation of, 318
gluteus minimus, 295, 296f recent discussions on, 318–319
Glyoxylic acid method, 457 Homer’s iliad, pelvic and urogenital injuries,
Goat, pelvis constituents, 2, 2f 20t
Gonad construction, 264 Hominids, 6, 13, 29, 298
Grafenberg, 157 Homo (man), pelvis of, 3, 3f
Growth and differentiation factors (GDF), 510, birth mechanisms, 38f
511f pelvic shapes of, 131f
G-spot, 143, 155, 157, 170 Homo erectus, 6
Guarding reflex, 377, 378 Homo sapiens, 202
Gunshot wounds (GSW), 20, 166, 167 Hoodectomy, 170
Hormones, 505, 506
adrenocorticotropic hormone, 486
H alpha-melanocyte stimulating hormone,
Hahnemann, Samuel, 316, 317 486
homeopathy, 317, 318 androgens, 164, 266, 267
Hemipelvectomy, 14–15 anti-Müllerian hormone (see Anti-Mülleri-
in cancer, 15 an hormone (AMH))
Herbal medicine, 322 estrogen, 40, 495
black cohosh studies, 324–326 follicle stimulating hormone (FSH), 482f,
for female pelvic problems, 322–324 503f
from Natural remedies, 323t in genetics, 216
for male pelvic problems, 326 gonadotropin releasing hormone, 482f,
phytotherapy and placebo, 328–330 483, 495, 503, 507, 508

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Index 549

growth hormone, 511, 532 in males, 524


hormone-receptor interaction, 435 Inguinal hernias, 177, 193, 194, 196, 268
hypothalamic hormone, 482–483 Inhibin, 510, 511
insulin-like, 266, 267 Initial glomerulus of Cajal, 391
leptin, 291, 502, 503 Internal urethral sphincter, 220f, 456–460
luteinizing hormone (LH), 481, 482f glyoxylic acid method, 457
prolactin, 160 interstitial cells of Cajal, 458, 460
pubertal hormones, 483, 494 spinal efferents for bladder and urethra,
during puberty, 477 459f
sexual hormones, 481 stress incontinence, 457
testosterone, 164 structural blow of, 457, 458f
therapy, 269, 324, 325 International Journal of Sexology, 157
Horsetails (Equisetum), 326 The International Pudendal Neuropathy Asso-
Horsley-Clarke apparatus, 353 ciation (TIPNA), 341
Hottentot woman, 11, 12f Intrapartum stillbirth mortality, 437t, 438
Human birth canal Intrinsic primary afferent neurons (IPAN’s),
abortion, 35 390
birth passage way, 35–37 Intrinsic urethral defect, 187
fetus position during delivery, 37–38 Invading breast tumors, 169
Human bony pelvis, 4, 5f, 47. See also Bony Irregular menstruations, 323t
pelvis Ischium, 126
Human immunodeficiency virus (HIV) infec-
tions, 153
Human papillomavirus (HPV) infections, 143, K
153, 165 Ketamine, 472, 474–476
Human pelvic development chronic interstitial cystitis (chronic IC),
bone morphogenic proteins (BMPs), 223 475
ectodermal-mesothelial cells, 222 lower urinary tract symptoms (LUTS), 475
lectin-coated colloidal gold, 223 N-methyl-D-aspartate receptor (NMDA)
neural crest cells, 222 antagonist, 474
placodal cells, 222–223 painful bladder syndrome (PBS), 476
placodes, 222, 223 phencyclidine (PCP), 475
Human pelvic diaphragm, development of, physical complications, 475
206 structure of, 473f
coccygeus muscle, 206, 207, 209 K-hole, 475
levator ani muscle, 206, 207, 209 Kidney cancer, 249
muscles involved in, 207f metastasis pathways for, 250f
obturatorius internus muscle, 206, 207, Kittelaar (clitoris), 148f, 155
208–209 Knee tendon reflex, 381
reconstruction of embryo, postconception, Koro, 143–144, 148–149
208f primary, 144
Human skeleton, 52, 113f secondary, 144
Hypericum (St John’s wort), 330
psychodynamic effect, 330
L
Labiaplasty surgery, 170
I Laminin, 223
Iliac bone (ossa ilii), 4, 10, 14, 22, 125, 136, Lane, Sir Arbuthnot, 425–427
202 shoemaker’s posture, 425–426
Immune system, 154, 249, 323t, 324 lower vertebral column, 426
Immunoglobulins, 152 sacroiliac joint, 426
Incontinence. See also Urinary incontinence symphysis, 426
in athletes, 525 skeletal structure, deformation of, 426–427
in females, 524 Langerhans cells (LCs), 154

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550 Index

Laresse de Gérard, 64, 65f, 66, 68, 72, 74, 102 Lymphotropic superparamagnetic nanoparti-
Lateral lithotomy, 50–51 cles, 251
Leiomyomas, 493
development of uterus, 493
gonadotropin releasing hormone agonists, M
495 Macaca, birth passage way, 36f
hormonal influences, 494 Magnetic resonance imaging (MRI), 249
localization and types of, 494f in pelvic lymph node cancer detection,
uterine artery (see Uterine artery) 249–250
Leonardo da Vinci, 77, 80, 87, 504, 522, 531 Male bladder and urethra, 306f
Leptin, 291, 502–503 Male pelvis, midsaggital section of, 306f
effects, 503f Male sterilization, 270
levels of, 503 Malgaigne injury, 22, 23f
production of, 503 Man, birth passage way, 36f
Levator ani muscle, 206, 207, 209, 241 MAPS (Men After Prostate Surgery) project,
malfunction of, 419f 235
Levator-urethral reflex, 384 Marrons, 320. See also Suriname slavery
Levo-amphetamine, 472f Marsupials, 4
Ligamentum ovari proprii, 271 Masturbation, 143, 144, 150, 151, 158
Ligatures vivantes de Pinard, 42, 43 Mature human pelvic nervous system
Linea alba, 3 autonomic pelvic plexus (see Autonomic
Lissosphincter. See Internal urethral sphincter pelvic plexus)
Lithotomy, 49 central connections, 352
Low back pain, 136–138 human cord with membranes, 353f
self-locking mechanism of, 136, 137f micturition control (see Micturition
Lower urinary tract and sexual function, 471 control)
amphetamines, 472–473 interconnecting branches, 342
ketamine (see Ketamine) older literature, 343
MDMA, 473 neuromodulation (see Neuromodulation)
LOwer-extremity Powered ExoSkeleton pelvic plexus, 341–342
(LOPES), robotic gait trainer, 531 peripheral nervous system, 337
LSD, 472, 476 sacral somatic plexus (see Sacral somatic
Ludwig, Daniel, 316 plexus)
Lumbar lordosis, 32 Mature pelvic wall muscles and ligaments, 177
Lumbar sympathectomy, 259–264 abdominal operations, 187–188
chemical lumbar sympathectomy, 262, 264 cystourethropexy, 187
claudication, 261 fascia sling operation, 188
NOS, 263 retropubic urethro-colpo suspension,
side effects of, 264 188
sympathetic chain of man, 260f corpus intrapelvinum, 183
vasoactive intestinal polypeptide (VIP), foramina of pelvis, 177–179. See also to
263 bony pelvis
Lycopodium cernuum, 321 ischiorectal fossa, 179
Lymph edema linea terminalis, 178
hereditary, 258 sacro-spinal ligament, 179, 180f
non-hereditary, 257 sciatic foramen, 178
Lymphatic nodes, 250, 256 spina, 177
Lymphatic sacs, 256 tuber, 177
in human fetus, 257f levator ani muscle, 180–183
Lymphatic system, 256 subdivision of, 182f
Lymphatic vessel endothelial hyaluronan ligaments and surgery in stress inconti-
receptor 1 (Lyve1), 256 nence, 187
Lymphography, 258 ligaments, notions on, 184–186

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Index 551

pelvis, midsagittal section, 185f Mobility, 18


suspension ligaments, 184f Modern weapons, 20
suspension structures of bladder, cer- Monosodium glutamate, 485. See also
vix, and rectum, 185f Ve-Tsin
suspension operations, 186 Morphology and life of the snouters (Steiner),
urogenital diaphragm, 179–180, 183–184 1
placement over hiatus, 181f The morphology and lives of the Rhinograd-
stereometry, 180 entia (Stümpke), 1
vaginal operations, 188–189 Motor endplate hypothesis, 237, 238
arcus urethrosuspension, 188 Müller, Johannes Petrus, 216
urethrosuspension, 188 Multipara, 36
vaginal wall sling, 188 average time of delivery, 41
Medieval dissections, 75 Mutilation, 149–153. See also Circumcision
Ashmole, 78, 399
line drawings from, 79f
menstruation, 79 N
cesarean operations, 80 The naked ape (Morris), 288
exploratory operation, 76f Nanoparticles, 251
female uropoetic-genital system, 77f Neanderthal lesions, 18
intra-vaginal fumigation, 78 Nerve complex between vagina and urethra,
medieval sculptures, 84f 158f
Adam and Eve, 80, 82f Neuromodulation, 348
cauterization points, 84, 85f EPFS, 349
crucifixion, 80, 82f sacral nerve stimulation, 349–350
kidneys and ureters, 86f electrode placement, 350
uterus and its extrusions, 77f third sacral segmental nerve (S3), 349
vaginal dilatators, 77–78 SANS, 348–349
Medroxyprogesterone acetate (MPA), 163 Neuropeptide Y (NPY), 486
Menopause, 325, 488, 495, 523, 528 Neurophysiologic model of pathways for
Meso, 246, 248 orgasm, 160f
Mesonephros, 264 Neurotransmitters, 355, 378f, 381, 389, 400,
Mesorectal excision, 414 460, 472, 473, 503
Metalloproteinases, 40 in bladder and ganglia, 382t
Methamphetamine, 472 catecholamine, 263
Methylenedioxymethamphetamine (MDMA), coneurotransmitter, 268
472, 473. See also Ecstasy neuropeptide Y, 486
Microganglia, 377 nitric oxide, 40, 263, 399f, 400, 460
Micturition sensory neurotransmitters, 399f
control of, 352–355 Nitric oxide synthase (NOS), 263, 474
Barrington’s nucleus, 355 Noise, 379–381
L (lateral) region, 354 Onuf’s nucleus (see Onuf’s nucleus)
M (medial) region, 354 Nomina Anatomica Committee, 409
pelvic structures involved in, 354f Non-hereditary lymph edema, 257
TLD-nucleus, 355 Nucleus tegmentalis laterodorsalis (TLD-
long neuron reflex system, 387 nucleus), 355
phase, female with full bladder, 367f Nullipara, 36
problems, 220 average time of delivery, 41
short neuron reflex system, 387
supraspinal controller system, 387
Midwifery, 229 O
Milroy’s lymphoedema, 256, 257 Obesity, 233, 408, 425, 506
autosomal dominant, 258 and polycystic ovary, 507
chromosome 16q24 mutation, 258 urinary stress incontinence, 408
Miscarriage, 323t, 490 Obturator nerve, 299

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552 Index

Obturatorius internus muscle, 206, 207, Pelvic blood vessels, 43


208–209 Pelvic diaphragm, 201–203
Olfactory micturition reflex, 384 biped movement of humans, 202
Omentopexy, 258 descensus of, 418–420
Omentoplasty, 258 extension angle of little finger, 420f
Onuf’s nucleus, 379, 454–456 stress incontinence, 418, 419
motoneurons activity, 380f development of, 208–210
motoneurons of, 456 gender of, 210
plateau potentials, 456 rotating position of, 210f
tonic activity, 456 in Homo sapiens, 202
muscle fibers, 380 levator ani, division, 203
Onufrowicz, Bronislaw, 454 versus pelvic floor, 201
Open book injury, 23, 23f in quadrupeds, 202
Otopteryx volitans in situ, 2f Pelvic dimorphism, 30
Ovary and baby heads, 30
and acupuncture (see Acupuncture and and birth canal, 30
ovary) fetus, extra space, 31–32
of children at different ages, 507f Pelvic floor dysfunctions
FSH production, 507 pelvic floor training, 241–242
LH, 507 toilet behavior, 231–235
polycystic ovary abdominal muscles, 232–233
gonadotropin releasing hormone, 508 pelvic floor muscles, 234–235
Graafian follicles, 506 position of bladder and rectum, 231f
and obesity, 507 resistance training, 234f
parauterine vascular plexus, 508f spinal stability, muscles, 232f, 233
and puberty (see Ovary and puberty) tummy tuck approach, 233
Ovary and puberty, 504–506 Wise-Anderson method (see Wise-Ander-
germ cells son method)
at age, 505f Pelvic fractures, 17, 22, 23f, 24, 26
degeneration of, 506 bull fighting, 18
development of, 505 Pelvic ligaments, 26, 134, 138
production, 504 extension angle of little finger, 420f
primordial follicles, 505 Pelvic lymph node cancer detection, 249–250
by computed tomography, 249–253
by magnetic resonance imaging, 249–253
P by size or volume, 253–255
Paracolpium, 409t, 410, 414 Pelvic lymph node dissection (PLND), 249,
Paracysticum, 409t, 410 252
Parametrium, 409, 409t Pelvic pain, 9, 236, 239
Paraproctium, 409t, 410 menstrual heavy periods and, 274, 275t
Parasympathic system, 381, 382 postsynaptic dorsal column pathway, 353
general scheme of, 378f Pelvic remains, 17
Parietal peritoneum, 245 Neanderthals, 18
Pars illium, 126 Pazyryk Mongolian War skeletons, 18–19
Pazyryk Mongolian War skeletons, 18–19 Trojan Siege, 19
Pelvic autonomic ganglia, 388–389 Pelvic shapes, 131, 131f, 291
dorsal root ganglia (see Dorsal root gan- stress intensity distributions, 132f
glion (DRG)) Pelvic size, 34, 115, 291, 430
microganglia, 389–390 Pelvic soft tissues, 72–74
visceral organ cross-sensitization, 394–396 Pelvic sirene, 120–122
cross-organ sensitization, 395 midsagittal drawings, 122f
explanations of, 396f schematic representation of cone-like
Hritshoola, 394 deviations, 122, 123f
order of effects, 395 Pelvic sphincters, development of, 213–215

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Index 553

‘‘classic concept’’ of subdivision of cloaca, genetics of, 531


214f Alzheimer disease, 531
cloacal membrane, 215f Huntington disease, 531
Pelvic stability, 22–24, 26 p53 gene, 532
Pelvic structure handgrip strength, 533
android type of pelvis, 34 hip problems in elderly (see Hip problems
in birth, 29 in elderly)
comparison, 33 history of aging research, 519–522
diameters and pelvic typing, 32f pelvic organs during aging, 522–523
in modern women, 32 reproductive organs, 523–524
evolution, 29–35 uropoetic system, 524–525
pelvic organ prolapse, 32 Pelvis comparative anatomy, 115–116
in Macaca monkeys, 32–33 morphology of man and animals, 116
Pelvic visceral organs, 489 pelvic position, 115
early development of uterus and conse- pelvic remnants, 115
quences, 489–493 shape of, 116
ovarian and uterine volume and shape, structure and composition, 116
490t Pelvis ontogeny, 116–117
uterus malformations, 491f enchondral ossification, 117
vaginal malformations, 492 Pelvis symmetry, 112–114
kangaroo, vagina in, 492 frontal view, 113f
leiomyomas (see Leiomyomas) symmetry, definition, 112
male testes development, 490 Penile anatomy, 195f
anti-Müllerian hormone, 490 Peno-motor reflex, 384
testosterone effect, 490–491 Pentahydroxy flavones, 328
marsupials, urogenital apparatus of, 493f Perianal connective tissue, 417–418
Pelvic wall muscles and sphincters, 189–193 anal echography, 417
abdomen of embryo, view on, 190f Perirectal fasciae, 416–417
cloacal muscles, 190 Peritoneal dialysis, 247
pelvic floor Peritoneum
innervation of, 191 closing of, 247
muscles, development of, 192f definition, 247
pelvinus nerve, 192f milky spots, 248
pudendal nerve, 192f nonclosure of, 247
Pelvis stomata, 248
and herbal medicine, 313–315 Periurethral injections, 188
bladder infections, 313 Persistent Müllerian duct syndrome (PMDS),
hidden role in sexual arousal and mating, 490
284 internal genital organs in, 492f
and human mating process, 283 Phytopharmacology, 313–314
mechanical approach to, 118–120 Phytotherapy, 314
Jansen’s view, 118–119 Plastic surgery, of sexual organs, 169–170
leverage mechanism for hip joint, 119 Polycystic ovary syndrome, 506
skull volume of women vs. men, 119 Pomeroy technique, 273
peritoneal relations, 246f Positron emission tomography (PET), 251
reflex or controller mechanisms in, Posterior sagittal anorectoplasty (PSARP), 219
383–385 Posterior urethral nerves, 157
new reflexes, 383–384 Premenstrual syndrome, 323t
Pelvis and aging, 517–519 Prepuce, 153–157. See also Circumcision
falls, 530–531 Priapism, 473
causes of, 530–531 sildenafil (Viagra), 473
hip fracture, 530 Prolactin, 160
in males versus females, 530 Prostaglandins, 275, 378, 399f
traffic accidents, 531 Prostataplex, 333

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554 Index

Prostate cancer, 252 Red Cross, 21–22


preoperative blood levels of PSA, 252t Reflex, 381–382
Prostate-specific antigen (PSA), 252 Renaissance era, 87–88
and metastasis percentage, 252t Retroperitoneal space, 245–248
Pubertal fat accumulation, 484 carcinoma in, 248–249
android type, 484 pelvic lymph node cancer, 249–250
arcuate neurons, 485 (see also Arcuate lumbar sympathectomy (see Lumbar
nucleus) sympathectomy)
gynoid type, 484 Retropubic urethro-colpo suspension, 188
sexual signaling hypothesis, 486 Retterer folds, 214
Puberty, 481 Rhabdosphincter. See External urethral
adrenarche, 481 sphincter
gonadarche, 481 Rhombus of Michaelis, 7
KiSS1, 482 in male and female, 9f
infundibular nucleus, 483 Richter, Christian Friedrich, 317
luteinizing hormone (LH), 481, 482f Aurum potabile, 317
tumor-related genes, 482 Rohypnol, 472
white matter of brain, 484 Rotatory descensus, 187
Pubis, 7, 70, 125, 126, 178, 201 Rowing, 427–430
os pubis, 52, 63, 66, 72, 81t, 92, 117, 148f, abdominal muscle functions, 430
183, 209 anthropometry, 430
symphysis pubis, 410f, 426 lower back pain, 428
Pudendal nerve, 347–348 pelvic movement, 429
Pudendal nerve complex, 343 pelvis wobbling, 429
Pudendus anesthesia, 341 phases of, 428f
Pupil enlargement, 288 spinal cord injury, 429
feminine, large pupils, 288 stroke phase, 429
masculine, dilated pupil, 288 Ruysch, Frederik, 52
pupil size
and age, 288f
in men and women, 289f S
Purple corn flower, 324 Sacral bone, 12
Purple sand spurry (Spergularia purpurea), Sacral somatic plexus
326 Alcock’s canal, 339–340
basic arrangement, 338
pudendal nerve, 339
Q sciatic nerve, 339
Quadrupeds, 3–4, 13, 127, 128, 202 ventral rami
Quercetin, 326, 328 female sacral plexus, 340f
male sacral plexus, 340f
Sacroiliac joint, 8, 136–138
R during labor, 9
Radiculopathic model for muscular pain, 237, dysfunction, physiotherapeutic methods, 9
238 fracture in, 9–10
Rate-of-living theory of aging, 518 hypertrophic nonunion of, 11f
Rathke’s folds, 214 ligaments and fascias in, 137f
Rauwolfia serpentia, 324 transverse sections, ethanol preparation of,
Rectosacral fascia, 414–416 10f
concept opponents, 416 Sacrum, 4, 6f, 9f, 10, 11f, 22, 30, 38f, 67, 181,
fascia endopelvina, 414 426, 441
fascia parietalis, 414 biped movement of humans, 202
fascia pelvis visceralis, 414 in conjoined twins, 124
retrorectal space, 415f fractures, 17
Recto-urethral reflex, 383 os sacrum, 52, 54f, 60, 68, 72, 177, 344

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Index 555

to bony pelvis, 69 Nuck, Antonius, 104


and low back pain, 136 cyst of Nuck, 104
and os innominatum, 66 Paaw, Petrus, 104
pelvic cavity constituent, 62 Swammerdam, Jan, 104
rectosacral fascia, 415 van der Spieghel, Adriaan, 104
during rowing, 428 van Horne, Joannes, 104
self-locking mechanism of, 111, 136 Sex in Sweden study, 159
sitting pressure, 431, 434 Sexual anxieties, 143. See also Koro;
width, 32 Spermatorrhoea
Sacrum bifidum, 68–72 Sexual offenders, 163
meningomyelocéle, 71 treatment, 164
from Neolithic era, 69, 69f Sexual transmitted infections (STI), 152
from Zaayer collection, 70–71, 70f Short neuron reflex system, 382–383,
Sarafix, 25, 26f 396–398
Sarajevo, 24–26 structures guided by, 385f
Saw palmetto (Serenoa repens), 326–328, of uropoetic system, 383f
327f, 330–333 Siparuna guianensis (fever tree), 322
benign prostatic hyperplasia, 330 Sitting, 423–425. See also Sitting and delivery
and finasteride, 327, 328 curvature of lumbar area, 443
meta-analysis evaluating, 332t in flexion, advantages, 442–443
prostataplex, 333 gravity effects of changes in hip and knee
prostate-specific antigen (PSA) lowering, flexion, 443f
326 lumbosacral curve and pelvic rotation
Saw Palmetto Treatment of Enlarged Prostates during, 441–444
(STEP) study, 331 lateral recumbent position, 441f
Scarpa’s fascias, 193–197, 196f reduction in lumbar lordosis, 441, 442f
Sciatic nerve, 299 and moving, 423, 424
intramuscular injections, 299–300 slump sitting, disadvantages, 443
Scoparia dulcis (broomweed), 321 ulceration, 424
Scrotal elephantiasis, 259f wheelchair users, 424
Scrotal hernia, 162 Sitting and delivery, 432
Second Salernitan Anatomy and Anatomia birth chairs and birth stools, 433f
Cophonis, 81t midwife-attended birth, 434
Sedentary physiology, 425 sitting position during delivery, 439
Senescence, 518 lithotomic sitting position, 440f
Septa, 410 upright delivery versus recumbent dorsal
gross-anatomical preparation of, 413f delivery, 432
reconstruction of connective septa in, 411f Small intensely fluorescent cells (SIF cells),
Serotonin, 472–473 388
Serotonin-norepinephrine-dopamine reuptake Smooth muscular sphincter. See Internal ure-
inhibitor (SNDRI), 474 thral sphincter
Seventeenth-century scholars, 104 Somatic reflexes, 377
ab Aquapendente, Hieronymus Fabricius, Sox 18 transcription factor, 256
104 Spanking, 300–302
Aranzi, Giulio, 104 children’s spanking, 300
Aselli, Gasparo, 104 nates, 301
Bidloo, Govard, 104 to sexual performances, 300–301
Casserio, Giulio, 104 Special K (party drug). See Ketamine
de Graaf, Regnoldus, 104 Speed (party drug). See Methamphetamine
on female reproductive organs, 105, Spermatorrhoea, 143–145, 148–149
105f instrument by Reynold, 145–146, 146f
Drelincourt, Charles, 104 Spinal-bulbospinal reflex, 224
Fallopius, Gabriel, 104 Stahl, Georg Ernst, 316
Heurnius, Otto, 104 Steatopygy, 10

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556 Index

Stoller’s afferent nerve stimulation (SANS), calcitonin gene-related peptide (CGRP),


348–349 268
Stress incontinence, 187 cranial suspensory ligament, 266
Striated muscular sphincter. See External ure- cryptorchidism, 265
thral sphincter final situation of, 265f
Striated urethral sphincter, 220 gonad construction, 264
Structural fat, 407 gubernaculum
in anorexia nervosa, 407 derivatives of, 267f
pelvic fat, 408 reconstruction, 267f
Study Group for Pre and Postnatal Education, rejuvenation, 270
230 Testis, 499
Subcutaneous fat, 290 leptin (see Leptin)
Subperitoneal blood vessels and ligaments, male exterior genital and age, 499t
270–271 puberty and height, 500–502
blood vessels and peritoneal fluid, 271 decrease in age at menarche, 500f
arteries of tuba and ovary, 274f hybrid vigor, 501
broad ligament, 272 increasing sex ratios, 502
cavum Douglasi, 271 nutrition and height, 501
congestion, 275 Ukranian heterosis, 502
endometriosis, 272 testis and penis, 499–500
pelvic venography, 274 in elephants, 499
relations to peritoneum, 273f in humans, 499
in sterilization operations, 273 Testosterone, 164–165
William Turner’s subperitoneal arterial Tetrapods, 4
plexus (see William Turner’s subperi- Theoria Generations (Theory of generation or
toneal arterial plexus) reproduction), Wolff, 215
Subperitoneal space, 245–248 Thoracic duct, in human fetus, 257f
carcinoma in, 248–249 Throphoblast, 41
pelvic lymph node cancer, 249–250 TLD (nucleus tegmento-latero-dorsalis), 224
lumbar sympathectomy, 259–264 Barrington’s nucleus, 225f
Sulphated glycosaminoglycans, 40 Transcription factor prospero-related homeo-
Suo-yang, 143 box 1 (Prox1), 256
Suprapubic lithotomy, 51 Trigger points, 237
Surgery to anatomy, 101–104 and acupuncture points, 237
Suriname slavery, 320 dry needle injection, 239
genital steam baths, 321, 321f quality of published results on, 238
dry sex, 321, 322 theories to, 237–238
herbal medicine in, 320 trigger-point therapy, 238–239
for prostate problems, 321 Trigone, 305, 308–309
for stopping menstruation, 321 Trojan Siege, 19
for uterine problems, 321 Tubal sterilization, 275
Sympathetic chain of Man, 260f Turner’s pelvic brim or index, 34
Sympathic system, 381
general scheme of, 378f
Symphysectomy, 54 U
Syphilis, 74 University of Padua and anatomy, 96–101
Aristotle’s methodology, 98
universitas ultramontanorum, 96
T Upright delivery method, 432, 434–435
Tail-waving muscle. See Coccygeus muscle fetal head-to-cervix force, 435
Tanner stages, 497 Urethral sphincter reflex, 379
Terminal sphincters, 450 Urethrocele, 187
Testicular descent, 264–270 Urethrosuspension, 188
androgens, 267 Urinary incontinence, 7, 47, 220

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Index 557

antimuscarinics and a-blockers in, 460f Vaginouterine reflex, 384


bladder neck position, 37 van Deventer, Hendrik, 55–56, 59f
in females, 235, 236 and bony pelvis, 58–62
levator hiatus, 36 frontal view of pelvis, 60f
collagen type, 37 side view of half pelvis, 61f
nocturnal enuresis, 234 coccyx, 63
nullipara versus multipara, 36 deflections of pelvis, 63–64
prolapse and, 35 dissemination through Europe, 62–63
prostatectomy, 235 life of, 56–57
stress urine incontinence, 235 pelvis, 63
vaginal delivery, 36, 37 thesis of, 57–58
Urogenital system, resection of, 53f van Leeuwenhoek, Antoni, 56
Uropoetic system, development, 211 Vanilloid receptors, 400
development of ureter, 212f Vasoactive intestinal polypeptide (VIP), 157,
downward progression of mesonephric 263
duct, 211f Vaucanson de Jacques, 517
paired versus unpaired, 212–213 Vegf-c (vascular endothelial growth factor-c),
upward progression of ureter, 211f 256
Urothelium, 398 Vehicle injuries, 21f
with interstitial cells, 400f Veils, 284
with nerve terminals, 400f facial expression and education, 285
sensory functions of, 400f human identity, 284–285
signaling, 398–399 in USA, 284
with smooth muscle cells, 400f Vimont’s arguments, 284
Uterine artery, 44, 495 Vesalius, Andreas, 51–52
blood flow in, 494–495 os sacrum, 54f
estrogen production and, 495 pelvis as pictured by, 54f
venous plexuses, 44f route to, 88–89
Uterine electrical activity, 371, 373–374 Vesico-cavernosus reflex, 384
electrohysterogram, 374f Vesico-levator reflex, 384
endometrium, 371 Ve-Tsin, 408, 485
myometrium, 371, 373 Vinca major (large periwinkle), 324
uterine contraction, 371 Vinca rosea (Madagascar periwinkle), 324
Uterine height, formula, 494 Visceral peritoneum, 246
Utero-cervical reflex, 384 Visual sexual information, 285–287
Uterus feminine male faces, 286
blood vessels in, 41 mate selection decisions, 286
distribution of, 42f sexual arousal, 285
cervical collagen changes, 40 zygomatic muscle activity, 286
muscular construction of, 40 von Störck, Anton, 316, 317, 318
during pregnancy, 38 Vulva, distribution of lymphatic system, 145f
before pregnancy, 39f
ripening, 40
W
Waist-to-hip ratio, 290
V in child birth, 290
Vagina monologues, 156 cultural factors in, 291
Vaginal infection/secretion, 323t leptin, 291
Vaginal orgasm, 157 in puberty, 290
Vaginal wall sling, 188 Waist-to-hip relation, 283
Vaginal-uterine anastomoses, 43 Wheelchair sitting, 430–432
Vaginism, 385 chair for postural adjustment, 432
Vagino-cavernosus reflex, 383 decoupled pelvis rotation (DPR), 431
Vagino-levator reflex, 384 pressure in, 431, 431f

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558 Index

William Turner’s subperitoneal arterial plexus, Z


276–278 Zerbis de Gabriele, 99, 520
collateral circulations, 277 for elderly
proximal claudicatio, 278 food, 520–521
subperitoneal arterial plexus, 277 health, 521
Wise-Anderson method, 236 sex, 521
anatomy related to, 237 Zingiber officinale, 321
physiology related to, 237 Zygomatic muscle activity, 286
quality of published results on, 239–241
Witch hazel, 324

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