Surgery of the

JULIO de PABLOS
Growth Plate
JULIO de PABLOS

Surgery of the Growth Plate

ERGON
Surgery of the
Growth Plate
JULIO de PABLOS
With the patronage of the European Paediatric Orthopaedic Society

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written permission of the publisher.

© 1998 Ediciones Ergon, S.A.

C/ Arboleda, 1 - 28220 Majadahonda (Madrid)

ISBN: 84-89834-29-6
Depósito Legal: M-9599-1998
 To my parents,
Pilar Fernández and
Julio de Pablos Sr., M.D.
 Editor

Julio de Pablos M.D., Ph. D.

Orthopedic Consultant
Hospital de Navarra
Clinical Associate Professor of Orthopedics
University of Navarra Medical School
Pamplona, Spain
Prologue
The growth plate has interested surgeons
since the 18th century. Its great importance
for growth of a bone has been known but
lack of knowledge of functions of growing
cartilage has earlier forced surgeons to avoid
touching growth plates.
In 1993 Phemister published his method
of complete arrest of growth at an epiphysis.
Phemister’s epiphyseodesis was the first clearly
planned and published operation on a growth
plate. Epiphyseodesis is still an important
means to treat inequality of leg length and
some modifications are used. In 1949 Blount
introduced arrest of growth by means of
staples. Today staples seem to be used more
in order to correct angular deformities.
Until 1967 it was generally believed that a
deformity which follows growth disturbance
from a growth plate injury is progressive until
the end of the child’s growing period. In many
cases of premature partial closure of a growth
plate severe disability followed. In experiments
performed without clinical goals it had been
found that limited portions of growth cartilage
injured by X-rays persisted in the metaphysis
and prevented formation of bony bridges
with further growth of the bone. On the basis
of this finding an operation for elimination
of bony bridges in children’s growth plates
was planned. As an interposition material
after resection of a bone bridge autogenous
cartilage of sufficient amount is not available.
The German Lexer’s excellent experiments and
clinical results with free fat grafts preventing
scar formation and ossification spoke in favour
of using free fat grafts as an interposition
material.
Experience of the use of the procedure and
the use of different interposition materials
has today been obtained in several centers.
However, the multitude of variable factors
influencing the treatment of the fairly
uncommon condition makes international
conferences collecting as much experience
as possible desirable.
There have been advances in surgery of
the growth plate. However, our knowledge of
the normal functions and the pathophysiology
of the growth plate is by no means complete.
Our advances in this field of surgery may
in the future be dependent on advances in
basic science.
Prof. A. Langenskiöld
Helsinki, March of 1998
Preface
The growth cartilage (physis) is the
structure that makes children’s bones unique.
Its morphology and function, as well as its
reactions to all kinds of etiological agents,
have fascinated scientist for decades; as
a consequence, growth cartilage surgery
arose from all the knowledge that had been
gradually accumulated on those matters.
The first attempts to modify physeal
function by surgical manipulation were
described at the beninning of this century
and consisted mainly of growth arrest and
stimulation procedures. These techniques,
particularly the former, are still in use today and
the greatest controversies that arise refer to the
timing for their performance in order to avoid
as far as possible hiper- or hypo- corrections.
In the second half of this century the
concept of des-epiphysiodesis for the treatment
of physeal bony bridges arose, consisting of
their resection and the interposition of fat
tissue and other materials in an attempt to
Acknowledgements
I am deeply indebted to all Biologists, Engineers and Medical Doctors who have made
possible the publication of this Book.
I also very much appreciate the wonderful work which Ediciones Ergon S.A. made in the
printing and editing processes of the book.
avoid recurrence and restore the previously
damage physeal function. However des-
epiphysiodeses are also subject to controversy,
also referring mainly to the timing for their
application and, above all, the capacity of the
growth plate to regenerate.
For the last two decades, an enormous field
of research and future clinical applications
has been opened up with the use of physeal
distraction. However, no small number of
surgeons are reluctant about applying this
method because of its potential complications.
It was our wish to put some light on all
these questions and controversies, when we
began the edition of this Monographic book
on Growth Plate Surgery.
We trust and hope that the readers will
find updated and clear information in the
following pages on what we consider the state
of the art of Physeal Surgery and that they
will find it useful for the decision making in
their daily clinical practice.
Dr. Julio de Pablos
Pamplona, March of 1998
 Contributors

N. Aldini-Nicolo J. Richard Bowen

Istituto di Ricerca Codivilla-Putti Orthopedic Division
Istituto Ortopedico Rizzoli Alfred I Dupont Institute
Bologna, Italy Wilmington (DE), USA

Carmen Alfaro-Adrían Martin I. Boyer

Department of Radiology Department of Orthopaedic Surgery
Hospital of Navarra Washington University School of Medicine
Pamplona, Spain St. Louis (MO), USA

Sunen Apte Peter W. Bray

Orthopedic Division Division of Surgical Research
The Nuffield Orthopedic Center Hospital for Sick Children
Headington, Oxford, United Kingdom Toronto, Canadá

Jesús Azcárate Juan A. Bruguera

Orthopedic Division Orthopedic Division
Hospital de Mendaro Clínica San Miguel
Mendaro, Spain Pamplona, Spain

Gerard Bollini José Cañadell

Orthopedic Division Orthopedic Division
Hôpital d’Enfants de la Timone University of Navarra Medical School
Marseille, France Pamplona, Spain

K. Bose Román Capdevila

Orthopedic Division Orthopedic Division
National University Hospital Shriners Hospital for Crippled Children
Singapore, Republic of Singapore Mexico City, Mexico

Vaughan A. Bowen J. Antonio Cara

Division of Hand Surgery Orthopedic Division
Stanford University Medical Center Hospital del Sol
Stanford (CA), USA Marbella, Spain
Contributors

J.W.K. Chan Bruce K. Foster

Orthopedic Division Orthopedic Division
National University Hospital Adelaide Children’s Hospital
Singapore, Republic of Singapore Adelaide, Australia

James L. Cunningham G.X. Gao

School of Engineering Orthopedic Division
University of Bristol National University Hospital
Bristol, United Kingdom Singapore, Republic of Singapore

Kirk W. Dabney José Gascó

Orthopedic Division Orthopedic Division
Alfred I Dupont Institute University of Valencia Medical School
Wilmington (DE), USA Valencia, Spain

Julio de Pablos R. Giardino

Orthopedic Division Istituto di Ricerca Codivilla-Putti
Hospital of Navarra Istituto Ortopedico Rizzoli
Pamplona, Spain Bologna, Italy

J. de Waele Jorge Gil-Albarova

Orthopedic Division Orthopedic Division
University Hospital K.U. Leuven Hospital Clínico Universitario
Pellenberg, Belgium Zaragoza, Spain

Eng Hin Lee Ricardo Gil-Albarova

Orthopedic Division Unidad Mixta de Investigación
National University Hospital Hospital Clínico Universitario
The Invalid Singapore, Republic of Singapore Zaragoza, Spain

Guy Fabry Uri Givon

Orthopedic Division Orthopedic Division
University Hospital K.U. Leuven Alfred I Dupont Institute
Pellenberg, Belgium Wilmington (DE), USA

M. Fini Jesús González-Herranz

Istituto di Ricerca Codivilla-Putti Orthopedic Division
Istituto Ortopedico Rizzoli Hospital N.S. de Valme
Bologna, Italy Sevilla, Spain

Francisco Forriol H. Theodore Harcke

Orthopedic Research Department of Radiology
University of Navarra Medical School Alfred I Dupont Institute
Pamplona, Spain Wilmington (DE), USA
 Contributors

Fernando Idoate Kalevi Österman

Division of Radiology Orton Orthopaedic Hospital of the Invalid
Clínica San Miguel Foundation
Pamplona, Spain Helsinki, Finland

Seiichi Ishikawa Armando Peinado

Orthopedic Division Orthopedic Division
Alfred I Dupont Institute Hospital San Juan de Dios
Wilmington (DE), USA Martorell, Spain

John Kenwright Hamlet A. Peterson

Orthopedic Division Division of Pediatric Orthopedics
The Nuffield Orthopedic Centre Mayo Clinic
Headington, Oxford, United Kingdom Rochester (MN), USA

Rüdiger Krauspe Mikel San Julián

Orthopedic Division Orthopedic Division
Orthopädische Klinik König-Ludwig-Haus University of Navarra Medical School
Würzburg, Germany Pamplona, Spain

Anders Langenskiöld Fernando Seral

Orton Orthopaedic Hospital Orthopedic Division
The Invalid Foundation Hospital Clínico Universitario
Helsinki, Finland Zaragoza, Spain

Margarita Melgosa Renato Spinelli

Unidad Mixta de Investigación Orthopedic Division
Hospital Clínico Universitario Bologna University School of Medicine
Zaragoza, Spain Bologna, Italy

Giorgio Monticelli(†) José B. Volpon

Fondazione Don Carlo Gnoccho Orthopedic Division
Rome, Italy Ribeirão Preto School of Medicine
Ribeirão Preto (SP), Brazil
Colin F. Moseley
Orthopedic Division David J. Zaleske
Shriners Hospital for Crippled Children Division of Pediatric Orthopedics
Los Angeles (CA), USA Massachusetts General Hospital
Boston (MA), USA
John A. Ogden
Orthopedic Division
Georgia Baptist Medical Center
Atlanta (GA), USA
 Table of contents

PART I. THE GROWTH PLATE

1. Normal growth and patterns of growth........................................................................... 3
C.F. Moseley
2. The physis and evaluation of its disorders....................................................................... 6
U. Givon , J.R. Bowen
3. Radiology of the growth plate ......................................................................................... 11
J.A. Bruguera, F. Idoate, C. Alfaro-Adrián, J. de Pablos
4. Magnetic resonance imaging of growth plates ............................................................. 22
H.A. Peterson
5. The growth mechanism in the peripheral part of the normal growth plate ............. 29
A. Langenskiöld

PART II. BASIC RESEARCH

6. Growth cartilage arrest with staples. Experimental study .......................................... 33
J. González-Herranz
7. Physeal arrest. Research in percutaneous epiphysiodesis .......................................... 54
U. Givon, S. Ishikawa, K.W. Dabney, H.T. Harcke, J.R. Bowen
8. Trochanteric epiphysiodesis by means of absorbable screws.
An experimental attempt in rabbits ................................................................................ 64
J. Gil-Albarova, M. Melgosa, R. Gil-Albarova, M. Aldini-Nicolo, R. Giardino, F. Seral
9. Physeal distraction: Review of experimental evidence.
What is the response of the cells on the growth plate? ................................................ 70
J. Kenwright, S. Apte
10. Biology of bone lengthening by means of physeal distraction ................................... 75
J. de Pablos
11. The experimental basis of treating premature partial closure of a growth
plate by bone bridge resection and interposition of adipose tissue ........................... 81
A. Langenskiöld
12. Regeneration of the growth plate .................................................................................... 84
K. Österman
13. Management of partial growth arrest. Physis, fat or silastic? ..................................... 86
E.H. Lee, G.X. Gao, K. Bose
14. Treatment of bone bridges by physeal distraction ....................................................... 89
J. Azcárate
Table of contents

15. Hemichondrodiatasis: is bridge resection necessary? ................................................. 96

E.H. Lee, J.W.K. Chan, K. Bose
16. Growth cartilage transplants ........................................................................................... 99
A. Peinado
17. Reimplantation of growth plate chondrocytes into growth plate
defects in sheep ................................................................................................................ 107
B.K. Foster, A.L. Hansen, G.J. Gibson, J.J. Hopwood, G.F. Binns, O.W. Wiebkin
18. Epiphyseal reconstruction: a review of a proposal for an interface between
basic and reconstructive orthopaedic science ............................................................. 117
D.J. Zaleske
19. Vascularised epiphyseal plate transplantation ........................................................... 126
C.V.A. Bowen, P.W. Bray, M.I. Boyer

PART III. PHYSEAL FRACTURES

20. Fractures of the growth plate ......................................................................................... 143
J. de Pablos, C. Alfaro-Adrián
21. Skeletal growth mechanism injury patterns ................................................................ 171
J.A. Ogden
22. Classification of physeal fractures ................................................................................ 181
H.A. Peterson
23. Surgical treatment of physeal fractures ....................................................................... 196
C.F. Moseley
24. Bone remodeling in malunited fractures in children ................................................ 202
J. Gascó, J. de Pablos

PART IV. PHYSEAL SURGERY FOR THE TREATMENT OF LIMB LENGTH

DISCREPANCIES
25. The timing of arrest of physeal activity in the treatment of leg length
discrepancy ....................................................................................................................... 215
C.F. Moseley
26. The timing of epiphysiodesis ......................................................................................... 223
G. Fabry, J. de Waele
27. Physeal surgery for the treatment of limb-length discrepancy ................................ 229
U. Givon , J.R. Bowen,
28. Surgical correction of partial growth plate closure using physeal distraction ....... 238
G. Bollini, J.L. Jouve, J. Cottalorda, P. Frayssinet, J.M. Guillaume, J.C. Godchaux
29. Bone lengthening by physeal distraction ..................................................................... 250
J. de Pablos
30. Leg lengthening by distraction epiphysiolysis........................................................... 258
G. Monticelli, R. Spinelli, R. Forte, L. Iorio
31. In-vivo mechanical response of the human growth plate to distraction
close to skeletal maturity ................................................................................................ 261
J. Kenwright, J.L. Cunningham
 Table of contents

PART V. PHYSEAL SURGERY FOR THE TREATMENT OF ANGULAR

DEFORMITIES
32. Temporary stapling of the growth-plate according to Blount for the
treatment of axial deformities and leg-length-discrepancies .................................... 267
R. Krauspe, P. Raab, A. Wild, J.L. Vispo-Seara, A. Richter
33. Idiopathic genu valgum treated by epiphysiodesis in adolescence ........................ 275
J.B. Volpon
34. Arthroscopic hemiepiphysiodesis ................................................................................ 281
J. de Pablos, R. Capdevila, J.A. Bruguera
35. The biology and treatment of physeal arrest ............................................................... 286
J.A. Ogden
36. Bridge resection and interposition of substances ....................................................... 294
A. Langenskiöld
37. Operative treatment of partial premature epiphyseal closure ................................. 296
K. Österman
38. Treatment of physeal bony bridges by means of bridge resection
and interposition of cranioplast .................................................................................... 299
H.A. Peterson
39. Correction of angular deformities by physeal distraction ........................................ 308
J. de Pablos, J. Cañadell

PART VI. PHYSEAL SURGERY IN BONE NEOPLASMS

40. Physeal distraction in the conservative treatment of malignant bone
tumours in children ......................................................................................................... 321
J. Cañadell, M. San Julián, F. Forriol, J.A. Cara

Index......................................................................................................................................... 329
 Part I
The growth plate
1 Normal growth and patterns of growth
C.F. Moseley
WHAT IS GROWTH?
The word ‘growth’ means different things
to different people. Even within the medical
community doctors of different specialties
attach different meanings to the word. Tied
in closely to growth are the concepts of aging
and maturation (Fig. 1).
When a mother describes her child as being
the shortest in her class she is referring to the
relationship between stature and chronological
age. The pediatrician, on hearing that complaint,
determines the skeletal age of the child. Growth
to him is the relationship between stature and
skeletal age. The child who is shortest in her
class may actually be of a tall growth percentile
but delayed maturation.
The orthopaedic surgeon usually thinks
of growth when presented with a patient
with leg length discrepancy. In that context,
growth is the relationship between leg length
and skeletal age, and has been documented by
Green and Anderson for a white, Anglo-Saxon
population of children(1). They published data
on the lengths of the tibia and femur of boys
and girls related to skeletal age.
WHAT IS MATURATION
Like growth, maturation means different
things to different people. In general, it is
an orderly progression through stages
Reprinted with permission of Mapfre Medicina (vol. 4, suppl. 2)
Chronological
age
Leg Height
length
Skeletal
age
Figure 1. Ilustration of certain of the relationship
which are a part of the concept of growth. Different
people and doctors of different interest consider
different relationship to be most relevant and
important.
of development. It is usually assessed by
comparing the child to the general population
and quantified by stating the age at which a
normal child would have achieved the same
level of development. Although motor skills
development and intellectual development
are frequently important to the pediatric
orthopaedic surgeon, in this context we are
interested in the development of the musculo-
skeletal system.
Standards such as the Greulich-Pyle atlas
and the Tanner-Whitehouse atlas contain
representative x-rays for assessment of
3
C.F. Moseley
musculo-skeletal development (3,4) . The
orthopaedic surgeon determines the skeletal
age of his patient by comparing the shapes
of bones and parts of bones to the standards
in the atlas. We assume that a determination
based on shapes will directly relate to growth
in terms of length and this assumption seems to
be fairly dependable. Tanner, Whitehouse et al.
have suggested, however, that, in determining
skeletal age for purposes of growth in length,
it might be best to ignore the shapes of the
cuboid bones of the hand and wrist and to
pay attention only to the long bones and their
epiphyses. While this seems reasonable its
validity has not been demonstrated and its
importance has not been assessed.
Use of skeletal age in leg length problems
It is likely that these atlases of skeletal
maturation would be of different format had
they been designed expressly for the purpose of
evaluating leg length problems. In this context
the orthopaedic surgeon is not concerned with
advancement or delay in skeletal maturation
itself, but in how far along the path to adult
leg length the patient has progressed.
Since Green and Anderson have correlated
skeletal age with leg length it is possible to
draw a direct link between the x-ray and the
percentage of adult length achieved(1). The
orthopaedic surgeon using the modified
skeletal age atlas would derive an answer
expressed as a percentage of adult leg length,
rather than in years and months. Prediction
of the actual length at maturity would then
be a matter of simple arithmetic.
PATTERNS OF GROWTH
The growth spurt
Examination of the growth graphs of Green
and Anderson reveals the conspicuous absence
of an inflection point. Growth in absolute
terms (mm per year), not just proportional
terms (% increase per year) is fastest at birth
4
and slows down continuously throughout
the years of growth. There is no point where
the growth rate speeds up.
This is in contrast to the experience of
every parent who sees her child’s growth rate
increase markedly in early adolescence. It is
also in contrast to growth studies that have
appeared mainly in the pediatric literature
which show that children’s growth actually
shows two growth spurts where the growth
rate increases markedly(2). There seems to
be no question that there is a growth spurt,
but, if it exists, why doesn’t it show in the
data of Green and Anderson? One possible
explanation is that the averaging of data from
a number of children having growth spurts
at different times would tend to conceal this
feature. Another possible explanation is that
the growth spurt only exists with respect to
chronological age, and not to skeletal age. If this
were the case, it would mean that children have
a maturation spurt which is synchronous with
the growth spurt so that their advancement
through the stages of skeletal maturation
occurs at pace with their increased growth
rate and the relationship between skeletal age
and leg length, as expressed in the Green and
Anderson data, is maintained.
The growth patterns of girls and boys
The Tanner-Whitehouse technique is
particularly interesting in that the same
standard x-rays are used for boys and girls.
This allows a direct comparison of the skeletal
development of the two sexes, and one is able
to determine with some accuracy what the
skeletal age would be if the patient were of
the opposite sex.
By correlating the skeletal age with the
Green and Anderson data it is possible, as
discussed above, to estimate what percentage
of adult leg length has been achieved. Knowing
what the skeletal age would be if the patient
were of the opposite sex we can go one step
further and estimate what percentage of adult

leg length would have been achieved had
the patient been of that sex. It is puzzling to
find that the two answers are very close; that
it does not matter much what the sex of the
patient is. It appears that whatever difference
is injected in the determination of skeletal
age is canceled out in the determination of
percentage of adult leg length.
This means that, if we view growth in
terms of the relationship between skeletal
development and percentage of adult leg
length achieved, boys and girls have very
similar patterns of growth. It is even possible
that the patterns are the same and that the
difference we see here is due to the variation
that one would expect in the collection of
biological data.
CONCLUSION
Growth is similar to the weather in that
the closer one looks and the more data one
collects the more difficult it is to understand.
Normal growth and patterns of growth
The job of the orthopaedic surgeon who
deals with growth problems and leg length
problems is made easier by an understanding
of these concepts, particularly the triangular
relationship among chronological age, skeletal
age, and leg length.
BIBLIOGRAPHY
1. Anderson M, Messner M, Green W. Distribution of
lengths of the normal femur and tibia in children
from one to eighteen years of age. J Bone Joint Surg
1964;46-A(6):1197-1202.
2. Bayley N. Individual patterns of development.
Child Develop 1956;27:45-74.
3. Greulich W, Pyle S. Radiographic atlas of the
skeletal development of the hand and wrist.
Stanford: Stanford University Press, 1959; 2nd ed.
4. Tanner J, Whitehouse R, Marshall W, et al.
Assessment of skeletal maturity and prediction
of adult height (TW2 method). London: Academic
Press, 1975.
5
2 The physis and evaluation of its disorders
U. Givon and J.R. Bowen
INTRODUCTION
The physis, also known as the growth
plate is a band of cartilage located between the
metaphyses and epiphyses of long bones in
growing children. This structure is responsible
for longitudinal growth of the bones and may
be injured, causing cessation or disturbance
of growth(1,2). The physis has been the subject
of countless publications on its’ anatomy
and physiology. The purpose of this chapter
is to review the anatomy and physiology
of the physis, the different mechanism of
physeal injuries and to outline the indications,
operative techniques and problems associated
with physeal surgery.
The physis is divided into five zones:
The reserve zone, the proliferative zone, the
maturation zone, the degenerative zone and
zone of provisional calcification, the last three
making up the hypertrophic zone. The reserve
zone is adjacent to the epiphyseal blood supply
though the oxygen tension in this zone is the
lowest. The role of the reserve zone in the physis
is not completely clear and there is speculation
that it functions as a storage depot for nutrients.
In the hypertrophic zone which is the major
element in the longitudinal growth of the
bone, the cells are organized in columns, each
consisting of 15-17 chondrocytes. This area has
the highest oxygen tension and is biologically the
most active(2). The function of the proliferative
6
zone is cell proliferation and matrix production.
In the hypertrophic zone the cells are enlarged
5-10 times the original size. The hypertrophic
zone chondrocyte is metabolically active but
the ultimate fate of the cells is apoptosis. At
the area of provisional calcification matrix
mineralization occurs, later to be replaced
by bone cells and matrix in the primary and
secondary spongiosa areas of the metaphysis.
Studies performed using fluorochrome labeling
demonstrated that chondrocytes are replaced at
the metaphyseal border at the rate of 8 per day,
thus the continuation of growth is dependent
upon production of 8 new chondrocytes to
replace them(3).
In the primary spongiosa zone of the
metaphysis, the cartilaginous matrix is invaded
by vascular tissue and osteoblasts which line
the calcified cartilage. Little or no change in
the matrix is observed in this area. In the
secondary spongiosa zone, the osteoblasts start
laying bone on the cartilage and this layer is
later replaced by lamellar bone in a process
of remodeling. Chondrocyte derived growth
factors may be taking part in the growth of
metaphyseal blood vessels into the physis(2).
Traumatic, vascular, thermal, metabolic,
infectious and iatrogenic factors may damage
the physis and cause an injury that may affect
longitudinal growth of the bone, temporarily
or permanently.

Fractures through growth plate constitute
approximately 15% of the fractures sustained in
children(4). The fracture line usually goes through
the calcified hypertrophic zone or the primary
spongiosa, but there are reports of propagation
of fracture line into the germinal layer with
devascularization of this layer, mostly seen in
type 3 injuries(5). In patients nearing the end
of their growth, the fracture line is distinctly
between the metaphyseal bone and the cartilage.
In areas were the blood supply was damaged or
the physis is incorrectly aligned, trabecular bone
will eventually replace the cartilage and form a
bony bridge between metaphysis and epiphysis.
The bone will form only when the secondary
ossification center will extend to the damaged
region, thus a long time may elapse between
injury and bridge formation(4,6). Currently
there are two commonly used classification
systems: the Salter Harris classification(6) and the
modification by Ogden(4,5) to that classification,
emphasizing that even in cases of an injury with
good prognosis, there may be a local crush of the
physis with the later development of premature
closure. A further modification and addition
to the classification was done by Peterson(7,8) in
1994. Higher incidence of premature closure of
the physis after fractures is found around the
knees and ankles.
Experiments demonstrating damage to the
physis after epiphyseal vessel occlusion were
reported by Trueta(9) but no reports of proved
vascular damage to the physis in humans
were made in the literature.
Thermal damage to the growth plate
may be caused either by cold or heat related
injuries(10). Damage due to exposure to cold was
reported mainly after frost bite to the fingers
and was secondary to intra-cellular and extra-
cellular ice crystal formation and to venous
congestion and thrombosis. Heat generated
physeal injury may be caused by direct thermal
injury or through prolonged ischaemia due
to strangulation by circumferential eschar or
compartment syndromes(10). Some cases of leg
The physis and evaluation of its disorders
length discrepancy and deformity developing
after burns were reported(11,12) and electro-
cautery was described as an experimental
technique for epiphysiodesis(13). Physeal closure
was reported as a sequel to an ulcer due to
extravasation of intravenous infusion, probably
through damage to the perichondrial ring and
the formation of a circular bony bridge, the
same mechanism which was suggested in cases
of burns(14).
Metabolic compromise to the physis may
be seen in rickets and renal osteodystrophy.
Slipped epiphysis due to renal osteodystrophy
is usually due to the secondary hyper-
parathyroidism associated with chronic renal
failure. This happens through the primary
spongiosa layer and reacts favorably to
medical treatment(15,16). Growth arrest may
appear after osteomyelitis, especially in the
newborn. The destruction of epiphysis and
physis by the formation of pus will cause
growth arrest or an angular deformity which
may become apparent a few years later(17). A
iatrogenic cause for a growth arrest may be
the insertion of a threaded wire across the
physis for a period of a few weeks, while a
smooth pin of a diameter lower than 3% of
the cross sectional area of the physis, will only
rarely cause a bony bar(18). Similar results were
found when biodegradable implants of the
same diameters were used in rabbits(19,20). The
insertion of tendons through the proximal
tibial physis during ACL reconstruction gave
good results in various reports, and meticulous
technique may prevent growth arrest when
ACL reconstruction is performed in the
skeletally immature patient(21,22).
EVALUATION OF THE ABNORMAL
PHYSIS
Evaluation of the physis may be performed
using radiography, linear, multiplanar or
computerized tomography, bone scintigraphy
and magnetic resonance imaging. Radiography
7
U. Givon, J.R. Bowen
and MRI have become the most frequently
used imaging techniques for evaluation.
Radiography is the primary modality for the
follow up of children who sustained injuries
to the growth plate or underwent physeal
surgery. Most types of bars, fractures and
angular deformities can be diagnosed using
radiography and limb length may be monitored.
Systemic illness or partial damage to the growth
plate may cause temporary slowing of growth,
followed by a period of rapid growth which
will be demonstrated through growth arrest
lines (Harris lines)(23). When the Harris lines are
parallel to the physis, this may be an evidence
that the physis is intact, but when the lines
converge, partial damage may be present,
causing an angular deformity. Magnetic
resonance imaging (MRI) is valuable in the early
identification of cartilaginous and vascular
abnormalities preceding the formation of a
bony bridge, imaging the size and the location
of the bridge and for decision making before
physeal surgery is undertaken(24-26). Jaramillo
and coworkers reported the possibility of
mapping a bony bridge using MRI in the T1
and T2 sequences(25,26) and similar results were
reported by Havranek and Lizler(27). Other
examination sequences and technical details
were reported by Harcke and his associates(28),
including some normal variations of the physis
and the possibility that discontinuity of the
physis will be present in a normal bone.
They described the normal closure of the
maturing physis with progressive narrowing
of the cartilaginous signal until it completely
disappears, first in the center of the physis
and then in the periphery. Snyder and his
colleagues(29) reported the results of an MRI
study of patients undergoing epiphysiodesis.
They demonstrated that fibro-cartilaginous
elements could be identified in the physis
4 months after surgery and that a mature
bony bridge was evident after 8 months. MRI
studies are beneficial in the early diagnosis of
a developing bony bridge, but so far they have
8
not been useful in the physiological evaluation
of the recovery potential of the physis.
Tomography is a valuable technique for
evaluation of physeal bars and is usually
performed in the antero-posterior and lateral
views. This technique was used for mapping
of physeal bars by Carlson and Wenger(30). The
use of computed tomography was described
for evaluation of the physis using 3 mm thick
cuts in 1 mm increments(31). Bone scintigraphy
has been found useful in the evaluation of
the viability of the physis (32-34). Increased
uptake in the metaphyseal region, where new
bone is formed, demonstrates functioning
growth plates. Quantitative techniques for
the evaluation of the physis were described
by Harcke et. al.(34) and by Howman-Giles
et. al.(35) both using decreased uptake of the
radioisotope in part of the physis as a sign of
decreased activity at the primary spongiosa area
and of physeal closure. The authors suggest the
use of radiography for the primary imaging
and for follow-up of the physis after injuries
and an MRI examination, 8 months after the
injury, if a bony bar is suspected. A suggested
protocol for the study of the physis includes
coronal multiplanar gradient recalled sequence
to evaluate for bony bridges; coronal spin echo
sequence to evaluate the zone of provisional
calcification and the course of growth recovery
lines; sagittal spin echo proton density and T2
with fat suppression to evaluate the patency of
the physis and differentiate it from the articular
cartilage(36).
REFERENCES
1. Brighton CT, Longitudinal bone growth: the
growth plate and its’ dysfunction. Instr Course
Lec 1987;36:3-25.
2. Ianotti JP. Growth plate physiology and pathology.
Orthop Clin North Am 1990;21:1-17.
3. Ogden JA, Rosenberg LC. Defining the growth
plate. In Uhthoff HK, Wiley JJ eds. Behavior of

the growth plate. Raven Press New York, pp.
1-13; 1988.
4. Ogden JA. Skeletal growth mechanism injury
patterns. In Uhthoff HK, Wiley JJ eds. Behavior
of the growth plate. Raven Press New York, pp.
85-96; 1988.
5. Ogden JA. The pathology of growth plate injury.
Mapfre Medicina, 1993;4 (suppl 2):8-14.
6. Salter RB, Harris WR. Injuries involving the
epiphyseal plate. J Bone Joint Surg, 1963;45-A:587-
622.
7. Peterson HA. Physeal fractures: part 2, two
previously unclassified types. J Pediatr Ortho,
1994;14:431-438.
8. Peterson HA. Physeal fractures: part 3, classification.
J Pediatr Orthop, 1994;14:439-448.
9. Trueta J. The role of the vessels in osteogenesis.
J Bone Joint Surg, 1963;45-B:402-418.
10. Benoit PR. Thermal injuries of the growth plate. In
Uhthoff HK, Wiley JJ eds. Behavior of the growth
plate. Raven Press New York, pp. 119-122; 1988
11. Frantz CH, Delgado S. Limb length discrepancy
after third degree burns. J Bone Joint Surg, 1966;48-
A:443-450.
12. Fingerhut A, Brocard M, Ronat R. Clinodactilie par
brulure electrique. Quelques reflexions a propos
des deux cas. Sem Hop. Paris, 1983;59:2131-2134.
13. Rosen MA, Beer KJ, Wiater JP et al. Epiphysiodesis
by electrocautery in the rabbit and the dog. Clin
Orthop, 1990;256:244-253.
14. Sanpera I, Fixsen JA, Hill RA. Injuries to the physis
by extravasation. A rare cause of growth plate
arrest. J Bone Joint Surg, 1994;76-B:278-280.
15. Loder RT, Hensinger RN. Slipped capital femoral
epiphysis associated with renal osteodystrophy.
J Pediatr Orthop, 1997;17:205-211.
16. Krempien B, Mehls O, Ritz E. Morphological
studies on pathogenesis of epiphyseal slipping
in uremic children. Wirchows Arch A Pathol Anat
Histol 1974;362:129-143.
17. Langenskiöld A. Growth disturbance after
The physis and evaluation of its disorders
osteomyelitis of femoral condyles in infants. Acta
Orthop Scand, 1984;55:1-13.
18. Makela AE, Vainionpaa S, Vitonen K et al. The
effect of trauma to the lower femoral epiphyseal
plate. An experimental study in rabbits. J Bone
Joint Surg. 1988;70-B:187-191.
19. Makela AE, Vainionpaa S, Vitonen K et al. The
effect of penetrating biodegradable implant on
the epiphyseal plate: An experimental study on
growing rabbits with special regards to polyglactin
910. J Pediatr Orthop, 1987;7:415-420.
20. Bostman O, Makela AE, Tormala P et al.
Transphyseal fracture fixation using biodegradable
pins. J Bone Joint Surg, 1989;71-B:706-7.
21. Lipscomb B, Anderson AF. Tears of the anterior
cruciate ligaments in adolescents. J Bone Joint
Surg, 1986;68-A:19-28.
22. Andrews M, Noyes FR, Barber-Westin SD. Anterior
cruciate ligaments allograft reconstruction in
the skeletally immature athlete. Am J Sport Med,
1994;22:48-54.
23. Guille JT, Yamazaki A, Bowen JR. Physeal surgery:
Indications and operative treatment. Am J of Orthop,
1997;27:323-332.
24. Jaramillo D, Shapiro F, Hoffer FA et al.
Posttraumatic growth plate abnormalities: MR
imaging of bony bridge formation in the rabbit.
Radiology, 1990;175:767-773.
25. Jaramillo D, Hoffer FA. Cartilaginous epiphysis and
growth plate: normal and abnormal MR imaging
findings. AJR, 1991;158:1105-1110.
26. Jaramillo D, Hoffer FA, Shapiro F et al. MR imaging
of fractures of the growth plate. AJR, 1990;155:1261-
1265.
27. Havranek P, Lizler J. Magnetic resonance imaging
in the evaluation of partial growth arrest after
physeal injuries in children. J Bone Joint Surg,
1991;73-A:1234-1241.
28. Harcke HT, Snyder M, Caro P et al. Growth plate
of the normal knee: evaluation with MR imaging.
Radiology, 1992;183:119-123.
29. Snyder M, Harcke HT, Bowen JR et al. Evaluation
9
U. Givon, J.R. Bowen

of physeal behavior in response to epiphysiodesis
with the use of magnetic resonance imaging. J
Bone Joint Surg, 1994;76-A:224-229.
30. Carlson WO, Wenger DR. A mapping method to
prepare for surgical excision of a partial physeal
arrest. J Pediatr Orthop, 1984;4:232-238.
31. Porat S, Nyska M, Nyska A et al. Assessment
of bony bridge by computed tomography:
experimental model in rabbits and clinical
application. J Pediatr Orthop, 1987;7:155-160.
32. Harcke HT, Zaph SE Mandell GA et al. Angular
deformity of the lower extremity: evaluation
with quantitative bone scintigraphy. Radiology,
1987;164:437-440.
33. Murray IP. Bone scanning in the child and the
young adult. Part 1. Skelet Radiol, 1987;5:1-14.
34. Harcke HT, Macy NJ, Mandell GA et al.
Quantitative assessment of growth plate activity.
J Nucl Med, 1984;25:115.
35. Howman-Giles R, Trochei M, Yeats K et al. Partial
growth plate closure: apex view on bone scan. J
Pediatr Orthop, 1985;5:109-111.
36. Laor T, Chung T, Hoffer FA et al. Musculoskeletal
magnetic resonance imaging: how we do it. Pediatr
Radiol 1996;26:695-700.

10
3 Radiology of the growth plate
J.A. Bruguera, C. Alfaro, F. Idoate and J. de Pablos

Early diagnosis and treatment of injuries Early diagnosis still remains a challenge, but
and disturbances of the growth-plate are some techniques (Bone Scan, MRI) are capable
essential to avoid serious deformities and to detect early vascular changes that precede
late complications. Caffey(3) in 1957 pointed the formation of a bridge(13,16,32).
out that a direct injury to the proliferating
cartilage may cause shortening of the shaft
with spreading and cupping of the shortened
end. Imaging techniques have evolved since
then, from plain X-ray to the latest generation
of Magnetic Resonance machines.
Fractures involving the growth-plate as
described by Salter and Harris(28) are the most
common cause of physeal injury, but any other
condition such as tumours, infections, repetitive
stress(4), metabolic diseases, diet restriction(29)
or iatrogenic causes (irradiation, surgery)(3,23,24)
can also produce disfunctions of the growth-
plate. In case of a significant injury, growth
arrest by means of bone bridge or bone bar
formation will occur and therefore angular
(Fig. 1) or longitudinal (Fig. 2) deformity if
there is partial or total involvement. The lesion
affects the germinal and proliferating layers of
cartilage before a bridge of fibrous tissue, first,
and bone, second, forms across the physis(13).
Detection of the lesion, its location and
extension as well as evaluation of the potential
growth of the rest of normal physis are
Figure 1. Peripheral bony bridge in the proximal
the main aims of the imaging techniques.
phalanx of the second finger (arrow) in a 12 year-
The information obtained is essential for old girl due to a burn sustained when she was 4
preoperative indication and planning(5,13,26). year-old.

Partly reprinted with permission of Mapfre Medicina (vol. 4, suppl 2) 11

J.A. Bruguera, C. Alfaro, F. Idoate, J. de Pablos
Figure 2. Shortening and varus deformity of the
distal femur due to a massive postraumatic bone
bridge across the distal femoral physis.
The current Imaging techniques used are
plain X-ray, tomograms, US, CT scan, Bone
scintigraphy and MRI. We will review their
uses and applications.
PLAIN X-RAYS
Plain X-rays are normally the first step to
investigate suspected lesions of the physis.
Routine AP and L views should be taken. A
normal plate is recognised as a radiolucent
area between metaphysis and epiphysis. Gross
abnormalities are quite obvious on radiographs
(Fig. 3) but subtle damage to the physeal cells or
blood supply of the germinal cell layer could not
be recognised on X-rays and growth arrest may
not be evident until much later (Figs. 4-A and
4-B)(7,20). Some authors(20,27,28) have pointed out the
12
Figure 3. Salter and Harris type III injury with
evident anterior displacement of the fragment
(arrows).
necessity of requesting oblique views projections
and comparison views of the unaffected side
to help with the diagnosis.
Some radiological features have been
related to a physeal disfunction:
• Widening and irregularities specially of
the distal radial physis have been described
as secondary changes to over use or stress
fracture of the growth-plate(2).
• Growth Disturbance Lines (GDL) or
Harris lines described as transverse sclerotic
lines in the metaphysis may be indication of
trauma or other causes of growth disfunction
(Fig. 5). In case of bilateral affectation,
constitutional rather than local aetiology can
be suspected(29). They have been described as
reliable indicators of growth plate activity and
quite useful for the prognosis(14,23).

Figure 4-A. X-ray of the wrist of a 9 year-old girl
taken after injury. They were reported as normal.
Hynes and O’Brien(14) studied and described
the natural history of these lines in tibias
after trauma. According to them, these lines
first appear after 6 to 12 weeks post trauma.
They observed that if the line extends across
the whole width of the metaphysis in both
planes, the entire physis will continue to grow.
However, if the line cannot be seen across
and some focal defects are detected, growth
impairment is present. The angle between the
plate and the GDL is quite important. If the
line and the physis are not parallel, angular
deformity is expected. Therefore, they can
suggest the site of physeal arrest from the
character and displacement of the growth
disturbance lines.
• Growth Recovery Zones as described
by Siffert and Katz (29) are different from
Radiology of the growth plate
Figure 4-B. X-ray of the same patient 2 years later.
GDL and can be detected on plain X-rays.
These are dense metaphyseal bands probably
due to hyperosteogenesis associated with
hyperaemia.
Extension of radiolucent growth-plate into
the metaphysis corresponds to an increase
in the thickness of the hypertrophic cell
zone of the physis due to interruption of
the blood supply on the metaphyseal side
with no significant decrease in growth plate
activity(17,20). Kleiman et al.(19) have shown that
this is not related to a physeal injury but to a
healing metaphyseal fracture.
TOMOGRAMS
Bone bridges can be detected on plain X-rays
but their configuration and the area of the physis
13
J.A. Bruguera, C. Alfaro, F. Idoate, J. de Pablos
Figure 5. Growth Disturbance Lines noted in a hip
treated for DDH.
involved are better detected by tomograms. In
the same way, tomograms can be used to rule
out premature physeal closure (Fig. 6).
Different kind of tomograms can be
used: linear, circular, spiral, ellipsoidal or
hypocycloidal(7,23,24). According to Peterson(24),
hypocycloidal tomograms are superior because
the cuts may be as small as 1 mm thick and
give sharper focus.
The advantage of tomograms over plain
radiographs is that all the different zones
of the physis can be explored in AP and L
views and therefore reconstructed as a map
which is helpful in planning surgical approach
and ensuing complete removal of the bar(7).
However, pictures could be blurred and their
interpretation difficult(26).
Carlson and Wenger (6) described an
improved method to construct a reliable cross-
sectional map from polytomograms taken in
AP and L planes. The map obtained helps in
14
identifying lesions and in planning surgery.
However, the technique is still dependent on
the quality and sharpness of the tomography(26).
COMPUTED TOMOGRAPHY SCAN
In the late eighties, some authors reported
good results with Computed Tomography
Scan (CT)(9,22,26,34) in the assessment of bony
bridges. They showed good correlation with
histological and operational findings and some
advantages over polytomography.
Some of them are currently using CT as a
method of choice in the evaluation of physeal
disruptions and preoperative planning(9,22,26).
Others, restrict its use to provide additional
information in some cases where plain films and
tomograms are inadequate or inconclusive.(34)
For all of them, the main advantages of
CT are:
- more accurate data about the size of the
bony bridge and its location.
- ability to view the whole plate in the axial
plane that simplifies the understanding and
the calculation of the area of the bone bar.
- excellent correlation between images and
operative findings.
- very effective in case of central arrest
pattern.
- ability to define the extent of arrest lines.
- ability to view epiphyseal and metaphyseal
regions.
Murray and Nixon(22) consider that CT
scan remains superior than MRI to show
calcification within the soft tissue matrix as
well as pathologic fractures. In addition, it
costs less than MRI.
However, there are some disadvantages
as well:
- The examination is time consuming.
- CT is a radiation exposure technique.
- According to the type of scanner, some
times pictures are not very sharp.
- If the growth-plate is next to closure there
is a limited value of CT.

Figure 6. Adolescent Blount´s disease. In this case a bone bridge was ruled out after a tomogram was
performed (right).
Recently Loder et al. (21) reported the
usefulness of helical CT to assess bony physeal
bridges. This volume image technique allows
to prepare physeal maps to determine the
extent and location of physeal bony bars,
with good space resolution and less radiation
than conventional CT, in a scanning time of
approximately 20 seconds..
ULTRASOUND
Ultrasonography may be useful to detect
foreign bodies, peripheral bone bridges and
hematomas in acute injuries around the
perichondral area(8). However, its use is very
rare and the amount of information obtained
from the central area of the physis is very limited.
BONE SCAN
There is always a delay between the
injury or disorder of the growth-plate and its
actual radiological appearance. Physiological
and pathological changes can occur in the
Radiology of the growth plate
physis and its vicinity with no radiological
evidence. Bone scan is able to diagnose lesions
of the physeal plate at an early stages and
with certainty(32). It is a tool for evaluation of
physiological activity of the blood supply and
metabolism of the skeleton with the additional
advantage of permitting quantitation(10,13,35).
Different radionuclides have been used in
the past such as Strontium-85, Strontium-87m,
Fluorine-18, etc. in order to evaluate bone
disorders. Detecting and imaging accurately
those changes in the growth-plate was finally
possible with the availability of Tc-labelled
phosphate complexes and the use of high
resolution fast-imaging scintillation cameras.
99
Tc has a favourable biological behaviour and
as a result produces sharp-quality images
with low radiation exposures to the patient(30).
Methylene diphosphonate is currently being
used in many places due to its higher skeletal
uptake, actively localised in the physis, and
faster blood clearance.
The distribution of Tc-labelled compounds
depends on both blood flow and reactive bone
15
J.A. Bruguera, C. Alfaro, F. Idoate, J. de Pablos
Figure 7. Normal bone scan in a 10 year-old boy.
formation. A normal growth-plate shows a
uniform distribution of tracer throughout the
plate with small increase of activity laterally
(Fig. 7)(13). According to Howman-Giles et
al.(13), the advantage of bone scan is that it is
a planar view and gives and overall image of
the growth-plate.
Harcke et al.(10) described a technique for
a quantitative assessment of growth plates
around the knee based on bone scan. They
coined the concept of medial to lateral ratio
(M/L) as the ratio of counts in the medial
two segments with the lateral two segments.
This is a predictor of angular deformity and
according to them it seems to reflect accurately
the imbalance that can occur from over-
stimulation or partial closure.
Overstimulation by demonstrated
increased activity of the medial side of the
16
proximal growth plate of a tibia on bone scan
and a subsequent valgus deformity has been
reported by Zionts et al.(35). They suggested a
relative increased vascular supply post trauma
and consequent overgrowth of the medial side.
On the other hand, a “cold” proximal tibial
growth plate on bone scan post trauma has
been reported by Wegener et al. (33). They
attributed this effect to a vasculature occlusion
due to vasospasm from hematoma or soft
tissue swelling.
When a partial premature closure of the
growth plate is present, a “cold” spot in the
involved physis can be observed at the site
of the bridge (Fig. 8)
MRI
Since its first use for clinical purposes in
the early 1980s, Magnetic Resonance Imaging
(MRI) has revolutioned medical imaging.
First reports about the use of this imaging
technique to evaluate growth plates are only
from few years ago. Jaramillo et al.(16) published
an experimental study creating bone bridges
in growth-plate in rabbits and comparing
MRI, tomograms and histology.
The normal appearance of the physis on
MRI depends mainly on the age of the patient
and the pulse sequence used. Gradient-echo
(GRE) sequences have been proven accurate in
depicting abnormalities in the growth plates(25).
On GRE MR images bone has a low signal
intensity, whereas the physeal plate, which
is composed primarily of cartilage has a high
signal intensity(2). Other sequences, such as PD
weighted with fat suppression and T1 weighted
with or without contrast medium may be
useful for visualising this area, specially in
adolescent subjects where the growth plate is
thin and wavy, characteristics that may result
in significant volume averaging.
MRI has an excellent space resolution,
with a section thickness of 0.7 mm achievable
with 3D imaging sequence. MR also offers

A DuPont Institute, Wilmington, Delaware, USA).
multiplanar capabilities which allows
reconstruction in both sagital and coronal
planes. Borsa et al. (2) recently reported
that the image data processing to yield 3D
rendered and proyection physeal maps may be
particularly useful in preoperative planning.
According to the age of patients and MRI
findings in normal knees these authors formed
four groups.
Group I: children aged less than 1 year,
the physis showed intermediate signal
intensity on T1-weighted images and high
signal intensity on field-echo images. They
found a well-defined border between the
metaphysis, growth-plate and the margin of
the ossification centre.
Group II: children aged between 2 and
11 years. Intermediate signal intensity on
T1-weighted images and bright signal on
field-echo images.
Group III: older than 12 years. They
observed that on both T1-weighted and
Radiology of the growth plate
Figure 8. A) Valgus deformity of the distal femur
due to the presence of a bone bridge in the lateral
aspect of the physis. B) The bone scan shows a
“cold” area (arrow) where the bridge is located.
Also a low uptake area can be appreciated in the
inner aspect of the proximal tibia which could be
explained as an attempt to compensate the femoral
deformity. (Courtesy of J. R. Bowen, M.D., A. I.
field-echo images the growth-plate band was
not always visible across the entire plate,
specially the central area. They called it drop-
out phenomenon. This could be observed on
coronal and sagittal images.
Group IV: complete closure.
Ossified lesion already formed can be
detected by plain X-rays, tomograms and
CT. If the bridge is fibrous it may not be
detectable on X-rays or CT but may be seen
with MR. Recently, the use of Gadolinium,
in particular Gadolinium diethylene tiamine
penta-acetic acid (Gd-DPTA), as a magnetic
resonance contrast agent, has increased the
diagnostic possibilities of MR imaging. Tissues
with marked uptake will enhance on either
T1-weighted spin-echo or gradient-echo images.
Enhanced T1-weighted images could be
useful indicator of early bony bar formation.
Jaramillo et al.(16) in their experimental study,
showed that Gd-DTPA enhancement preceded
the deposition of bone due to the development
17
J.A. Bruguera, C. Alfaro, F. Idoate, J. de Pablos

A A’

B B’
Figure 9. Acute knee trauma in a 9 year old girl. A) Although there was a high clinical suspicion of a
fracture, conventional X-rays were normal. B) An MRI performed few days later clearly showed an
undisplaced proximal tibial physeal fracture type IV of Salter and Harris (arrows). Left: coronal image,
F.L.A.S.H. Right: sagital image, Spin-Echo T2 weighted.

18
 Radiology of the growth plate

A B
Figure 10. A) Sagital T1 weighted and B) GRE MR images through the distal femur show a laterally
located physeal bar (arrow). On T1 weighted images the physis has a low signal intensity, whereas on
GRE MR images physis and articular cartilage it has a high signal intensity.

of vascularity through the physis. As the bone
bridge matures, the enhancement decreases.
Imaging of cartilaginous enhancement may be
useful in the study of epiphyseal and physeal
cartilage, evaluating the extent of injuries
of the cartilage and in complex congenital
malformations(1).
Some indications of MRI for the evaluation
of lesions affecting the growth-plate have
been suggested(18):
- Acute trauma: MRI is useful in the
evaluation of fractures and detection of
cartilaginous and vascular abnormalities
specially if the conventional radiological
study is normal and there is a high clinical
suspicion of fracture (Fig. 9-A and 9-B).
MR also provide adequate valuation of
associated ligament, soft tissue and osseous
injuries(25).
- Bony bridges: It provides excellent
information of the size, shape and location
of bone bars for preoperative planning
and treatment(12) (Fig. 10-A and 10-B).
MRI also provides adequate postsurgical
assessment(31).
- Tumours: to detect transphyseal involve-
ment.
- Infection: Gd-DPTA is very useful to detect
invasion of the plate and detect zones of
metaphyseal abscess.
The necessity of sedating young patients
and the length of the examination, although
Havranek and Lizler(12) did not spend more
than 15 minutes with each one, are some other
disadvantages of the MR imaging.
Although to our knowledge no study has
compared the diagnostic effectiveness of MR
versus other imaging techniques, MR has
definite advantages and seems to be the most
versatile. It could be used few weeks post
injury to detect early changes or few months
later to evaluate the extension and situation
of well established bony bridges. In addition,
its multiplanar capabilities with no radiation
involved make it a very attractive technique.
REFERENCES
1. Barnewolt CE, Shapiro F, Jaramillo D. Normal
gadolinium-enhanced MR images of the developing
appendicular skeleton: Part I. Cartilaginous
epiphysis and physis. AJR, 1997;169:183-189.
2. Borsa JJ, Peterson HA, Ehman RL. MR imaging

19
J.A. Bruguera, C. Alfaro, F. Idoate, J. de Pablos
of physeal bars. Radiology 1996;199:683-
687.
3. Caffey J. Some traumatic lesions in growing bones
other than fractures and dislocations: clinical and
radiological features. Br J Radiol, 1957;30:225-38.
4. Caine D, Roy S, Singer KM, Broekhoff J. Stress
changes of the distal radial growth plate. A
radiographic survey and review of the literature.
Am J Sports Med, 1992;20:290-8.
5. Cañadell J, De Pablos J. PatologÌa del cartÌlago de
crecimiento. Rev Ortop Traum, 1988;32 IB,3:255-61.
6. Carlson WO, Wenger DR. A mapping method to
prepare for surgical excision of a partial physeal
arrest. J Pediatr Orthop, 1984;4:232-8.
7. Cass JR, Peterson HA. Salter-Harris Type-IV
injuries of the distal tibial epiphyseal growth
plate, with emphasis on those involving the medial
malleolus. J Bone Joint Surg, 1983;65-A:1059-70.
8. Davidson RS, Markowitz RI, Dormans J,
Drummond DS. Ultrasonographic evaluation
of the elbow in infants and young children
after suspected trauma. J Bone Joint Surg Am
1994;76:1804-1813.
9. De Campo JF, Boldt DW. Computed tomography
of partial growth plate arrest: Initial experience.
Skeletal Radiol, 1986;15:526-9.
10. Harcke HT, Zapf SE, Mandell GA, Sharkey CA,
Cooley LA. Angular deformity of the lower
extremity: Evaluation with quantitative bone
scintigraphy. Radiology, 1987;164:437-40.
11. Harcke HT, Synder M, Caro PA, Bowen JR. Growth
plate of the normal knee: Evaluation with MR
imaging. Radiology, 1992;183:119-23.
12. Havranek P, Lizler J. Magnetic Resonance Imaging
in the evaluation of partial growth arrest after
physeal injuries in children. J Bone Joint Surg,
1991;73-A:1234-41.
13. Howman-Giles R, Trochei M, Yeates K, Middleton
R, Barrett I, Scougall J, Whiteway D. Partial growth
plate closure: Apex view on bone scan. J Pediatr
Orthop, 1985;5:109-11.
20
14. Hynes D, O’Brien T. Growth disturbance lines
after injury of the distal tibial physis. J Bone Joint
Surg, 1988;70-B:231-3.
15. Jaramillo D, Villegas-Medina OL, Doty DK, Dwek
JR, Ransil BJ, Mulkern RV, Shapiro F. Gadolinium-
enhanced MR imaging demonstrates abduction-
caused hip ischemia and its reversal in piglets.
AJR 1996;166:879-87
16. Jaramillo D, Shapiro F, Hoffer FA, Winalski CS,
Koskinen MF, Frasso R, Johnson A. Posttraumatic
growth-plate abnormalities: MR imaging of
bony-bridge formation in rabbits. Radiology,
1990;175:767-73.
17. Jaramillo D, Hoffer FA, Shapiro F, Rand F. MR
imaging of fractures of the growth plate. AJR,
1990;155:1261-5.
18. Jaramillo D, Hoffer FA. Cartilaginous epiphysis
and growth plate: Normal and abnormal MR
imaging findings. AJR, 1992;158:1105-10.
19. Kleinman PK, Marks Jr SC, Spevak MR, Belanger
PL, Richmond JM. Extension of growth-plate
cartilage into the metaphysis: A sign of healing
fractures in abused infants. AJR, 1991;156:775-9.
20. Kumar R, Madewell JE, Swischuk LE. The normal
and abnormal growth plate. Radiol Clin North Am,
1987;25:1133-53.
21. Loder RT, Swinford AE, Kuhns LR. The use of
helical computed tomographic scan to asses bony
physeal bridges. J Pediatr Orthop 1997;17:356-359.
22. Murray K, Nixon GW. Epiphyseal growth plate:
Evaluation with modified coronal CT. Radiology,
1988:166:263-5.
23. Ogden JA. Current Concepts Review. The
evaluation and treatment of partial physeal arrest.
J Bone Joint Surg, 1987;69-A:1297-302.
24. Peterson HA. Partial growth plate arrest and its
treatment. J Pediatr Orthop, 1984;4:246-58.
25. Petit P, Panuel M, Faure F, Jouve JL, Bourliere-
Najean B, Bollini G, Devred P. Acute fracture
of the distal tibial physis: role of gradient-echo
MR imaging versus plain film examination. AJR
1996;166:1203-6

26. Porat S, Nyska M, Nyska A, Fields S. Assessment
of bony bridge by computed tomography:
Experimental model in the rabbit and clinical
application. J Pediatr Orthop, 1987;7:155-60.
27. Rogers LF. The radiography of epiphyseal injuries.
Radiology, 1970;96:289-99.
28. Salter RB, Harris WR. Injuries involving the
epiphyseal plate. J Bone Joint Surg, 1963;45-A:587-
622.
29. Siffert RS, Katz JF. Growth recovery zones. J
Pediatr Orthop, 1983;3:196-201.
30. Subramanian G, McAfee JG, O’Mara Re,
Rosenstreich M, Mehter A. 99M Tc-polyphosphate
pp 46: A new radiopharmaceutical for skeletal
imaging. J Nucl Med, 1971;12:399-400.
31. Synder M, Harcke HT, Bowen JR, Caro PA Alfred
I. Evaluation of physeal behavior in response to
epiphyseodesis with the use of serial magnetic
Radiology of the growth plate
resonance imaging. J Bone Joint Surg Am,
1994;76:224-9
32. Walter E, Feine U, Anger K. Szintigraphische
diagnostik und verlaufskontrolle bei epiphysen-
fugenverletzungen. Fortschr Geb Rontgenstr
Nuklearmed, 1980;132:309-15.
33. Wegener WA, Heyman S. Growth plate fracture.
An acute fracture of the proximal tibia with a
photopenic defect on bone scintigraphy. Clin
Nucl Med, 1990;15:447-9.
34. Young JWR, Bright RW, Whitley NO. Computed
Tomography in the evaluation of partial growth
plate arrest in children. Skeletal Radiol, 1986;15:530-
535.
35. Zionts LE, Harcke HT, Brooks KM, Mac Ewen G
D: Posttraumatic tibia vlaga: A case demonstrating
asymmetric activity at the proximal growth
plate on technetium bone scan. J Pediatr Orthop
1987;7:458-62.
21
4
Magnetic resonance imaging of growth plates
H.A. Peterson
Prior to the availability of magnetic
resonance imaging (MRI), plain film
radiography and tomography were used to
evaluate the normal and abnormal physis.
These were generally adequate to determine the
presence or absence of a physeal abnormality,
such as a bone bridge or bar. With the advent of
surgical techniques allowing excision of physeal
bars, a more accurate and detailed depiction
of the physis/bar complex became necessary.
This information is desirable both to determine
the feasibility of surgical resection and for
adequate preoperative planning. Previously,
multi-planar tomograms were used as sources
for the construction of hand drawn physeal
maps(2), a technique which is time consuming
as well as difficult to perform accurately. Some
authors(3,12) feel that CT scans, including sagittal
and coronal reconstructions techniques are
useful for bar evaluation. However, the limited
multi-planar capability and inadequate spatial
resolution of CT scans limit their use in physeal
mapping(11,16). Nuclear medicine bone scan
techniques have also been used in physeal bar
evaluation(7), but provide hazy and imprecise
maps and are limited to the distal femur.
On GRE MR images bone has low signal
whereas the physeal plate, which is primarily
composed of cartilage, has high signal(5,9,13).
These intrinsic signal differences provide
excellent contrast between the bony bar and
the adjacent physis. The excellent spatial
22
resolution of MRI, with slice thickness of 0.7
mm achievable with 3-D imaging are well
suited to imaging the physis. This is enhanced
by the multi-planar capabilities of MRI, which
allows imaging of the growth plate in sagittal,
coronal, or any other plane, thus diminishing
partial volume averaging that is inherent in
axial image acquisition of an axially oriented
structure. In addition, the image data can
be processed to yield 3-D rendered and 3-D
projection physeal maps which are particularly
useful in preoperative planning.(1)
These features make MRI useful in
evaluating the normal growth plate(5), the
growth plate following fracture (8,9,14), the
growth plate following epiphysiodesis(15),
and posttraumatic growth plate bars.(1,4,6,10,11)
A transverse map depiction of the physis
and its defect may be obtained from MR source
images on one of three ways:
1. Manual mapping technique.
Direct visualization of each image,
manually marking and measuring the area
of damage or bridge and recording it on
graph paper within an outline of a transverse
section of the physis being studied. When
this is accomplished using both coronal
and sagittal plane cuts, a map of the normal
and abnormal portion of the physis can be
constructed. This procedure is identical to that
previously employed using tomogram slices.

This method is time consuming, open to
(2)
technician error in measuring and recording
the data, and gives no information concerning
the surrounding soft tissues.
2. Rendering technique(1).
The source images from either coronal
or sagittal series, or any other plane, are
transferred to a computer workstation with
software for 3-D rendering (ANALYZE is
an example of such software). Each image is
segmented by manually defining the physis.
A rendered axial image is then generated.
This 3-D rendered physeal map accurately
demonstrates the contour of the physis and
the location, size, and contour of the defect in
the physis. The surrounding soft tissues are
not included. The rendering process, including
image acquisition, transfer to the workstation,
segmentation generated rendering takes
several hours.
Magnetic resonance imaging of growth plates
Figure 1. Projection of 3-D
images. Three dimensional
volume acquisition is
accomplished by obtaining cores
of tissue data in the axial plane.
These 3-D data are processed on
an MR imaging console with the
use of standard image-analysis
software for MR angiography
(GE Medical Systems). This
yields a 3-D projection physeal
map that demonstrates the size
and shape of the physis, and the
size, shape, and location of the
physeal bar (below).
3. Projection technique(1) (Fig. 1).
This 3-D volume acquisition is
accomplished using the following parameters:
a steady-state 3-D, GRE (grass) pulse sequence
(43/6 [minimum as needed]; 30˚ flip angle) is
obtained in the axial plane, slice thickness 0.7
mm (often 60 slices or more total), spectral fat
saturation, field of view 16 cm, 192 views used
with 1 NEX. The extremity coil is used in all
cases. This yielded an average imaging time
of 8 minutes 52 seconds in the initial series.(1)
No sedation or anesthesia is used. This 3-D
data (these cores of tissue data are called
voxels rather than 2 dimensional depictions
which are called pixels) is processed on an
MRI console using standard image analysis
software used in MR angiography which
is standard equipment in nearly all MRI
units. The entire process, including image
acquisition and projection is completed in
less than an hour. The 3-D projection physeal
23
H.A. Peterson

map generated in this way gives an accurate
anatomic cross cut of the body part at the
level of the physis demonstrating the size
and shape of the physis, the location, size
and contours of the physeal defect, and the
surrounding soft tissues (Fig. 2). Depiction
of the surrounding soft tissue, particularly
vessels and nerves, is helpful in choosing
the best surgical exposure (Fig. 3). The soft
tissue may be deleted by computer if desired.
With all three methods the percent of
physis involved with a defect (such as a bone
bridge, tumor, cyst, infection, etc.) is expressed
as a percentage, calculated as follows: area of
defect/area of physis = defect x 100%. In the
Rendering process, the computer counts the

B
A

C D

Figure 2. A seven year 3 month old boy sustained a Salter-Harris type IV fracture of the proximal left
tibia three years previously. A) Coronal MR source image shows physeal bar of the proximal tibia. B)MR
projection image shows a transverse cut through the proximal tibia at the level of the physis. The outline of
the tibia contains the outer white Ring on Ranvier, the inner uneven gray physis, and the irregular central
black bony bar. The tibia, along with the smaller adjacent fibular epiphysis are surrounded by muscle, fat,
and skin (the latter not well seen at the density of this projection). The dense white linear structures are
vessels, some of which are entering the tibia at this level. C) A computer mouse has been used to outline
the physis and the bar. The computer determines the number of voxels in the bar and the entire physis. In
this instance the bar occupies 11% of the physes. Its irregularity, however, would require removal of at least
20% of the physis for the remaining physis to re-establish growth. D) Computer manipulation of voxels of
the physis to further highlight the bar. Note irregularity of the bar.

24
 Magnetic resonance imaging of growth plates

A B C

E
Figure 3 A-F.

25
H.A. Peterson

G H

I J
Figure 3 G-J.

number of pixels in the entire physis and in the
bar. In the Projection technique, the computer
counts the number of voxels (volume pixels)
in the physis and in the bar.
3-D MR Rendering and Projection provide
similar maps of physeal anatomy. The projection
technique is superior because it provides a more
reliable and anatomically detailed depiction
of the physis, it includes the surrounding soft
tissues, it employs software that is already
available on most MRI systems and it requires
less operator input so that it is less time
consuming. A patient may be examined, the
MRI projection image obtained and evaluated,
and the result and recommendations discussed
with the parents and patient all in one day. This
is uniquely beneficial at tertiary care centers
where the patients travel great distances for
evaluation. Currently, only the projection
technique is employed at our institution.

26
 Magnetic resonance imaging of growth plates

Figure 3. An eight year, 8 month old boy injured her

right knee on a trampoline. A) Lateral radiogram
shows a displaced Salter-Harris type I physeal fracture
of the distal femur. B) Anterior posterior (AP) view. C)
Treatment consisted of closed reduction and internal
fixation using crossed Steinmann pins (note the sites L
at which the pins cross the physis). D) AP radiogram
18 months post injury. Note growth arrest lines in
the metaphyses of both proximal tibiae and the distal left femur (arrows), but not in the distal right femur.
E) Scanogram at age 11 years 0 month, 2 years 4 months post injury. The right femur is 3.2 cm shorter
than the left and the physis is not visible in the center of the distal right femur. Knee function is normal.
F) Coronal MR source image shows several areas of bone continuity from metaphysis to epiphysis in the
distal femur. G) Sagittal MR source image shows two physeal bars. The multiple bars as seen on figures F
and G are sometimes referred to as satellite bars, but could be irregularities of one bar. H) MR projection
image shows the bone of the patella (top, black) with its articular cartilage (1) in contact with distal femoral
articular cartilage, and the distal femoral growth plate (various shades of gray) with 2 irregular black areas
(bone bars). The white line outlining the physis is made by a computer mouse. The number of voxels within
the white line is determined by the computer and represents the area of the physis. A similar procedure is
performed on the two irregular physeal bars. The smaller bar on the left is in the lateral condyle and contained
3.6% of the voxels of the entire physis, the bar on the right side is in the medial condyle and contained 6.3%
of the voxels; total area of both bars is 9.9% of the physis. Note that the position of these bars corresponds
with the position of the Steinmann pins (see Figure 3C). Note the surrounding soft tissues; muscle, fat, and
skin. The intense white structures are vessels. This information is helpful in planning surgical exposure,
particularly if the bar extends to the surface of the bone. I) Bar excision utilizing a metaphyseal window
and motorized burr. Since both bars were removed through one window, approximately 20% of the physis
was no longer present at the conclusion of the procedure. J) Intraoperative radiogram now shows a normal
physis throughout and no physeal bar. The tiny titanium vascular clips in the metaphysis and epiphysis
are 40 mm apart. The Cranioplast, bone clips, and metaphyseal cortical cap are in place. K) Repeat MRI 14
months post bar excision (possible because of the use of titanium, rather than silver or steel, markers) shows
the epiphysis growing away from the Cranioplast plug (black ball in center of metaphysis). The white area
between the epiphysis and the Cranioplast plug appears similar to the physeal cartilage which adjoins it. L)
Scanogram 19 months postoperative, age 12 years 9 months. The patient is normally active and asymptomatic.
The metal markers are 56 mm apart. The physis remains open. The right femur has grown 37 mm, the left
42 mm (88%). Since the right femur is still 37 mm shorter than the left, treatment is indicated; the choices at
this time are shoe lift, epiphyseodesis of the distal left femur, or lengthening of the right femur (at maturity
so precise final discrepancy is determined).

27
H.A. Peterson

REFERENCES to the growth plate: Results of MR imaging after

epiphyseal and metaphyseal injury in rabbits.
1. Borsa JJ, Peterson HA, Ehman RL. MR imaging
Radiology 1993;187:171-178.
of physeal bars. Radiology 1996;199(3):683-687.
10. Jaramillo D, Shapiro F, Hoffer FA, Winalski CS,
2. Carlson WO, Wenger DR. A mapping method to
Koskinen MF, Frasso R, Johnson A. Posttraumatic
prepare for surgical excision of partial physeal
growth plate abnormalities: MR imaging of bony
arrest. J Pediatr Orthop 1984;4:232-238.
bridge formation in rabbits. Radiology 1990;175:767-
3. De Campo JF, Boldt DW. Computed tomography 773.
of partial growth plate arrest: initial experience.
11. Peterson HA. Scanning the bridge. In: Behavior of
Skeletal Radiol 1986;15:526-529.
the Growth Plate, Uhthoff HK, Wiley JJ editors,
4. Gabel GT, Peterson HA, Berquist TH. Premature New York, Raven Press, 1988; pp 247-258.
partial arrest: Diagnosis by magnetic resonance
12. Porat S, Nyska M, Nyska A, Fields S. Assessment
imaging in two cases. Clin Orthop 1991;272:242-247.
of bony bridge by computed tomography:
5. Harckle HT, Synder M, Caro PA, Bowen JR. Growth experimental model in the rabbit and clinical
plate of the normal knee: evaluation with MR application. J Pediatr Orthop 1987;7:155-160.
imaging. Radiology 1992;183:119-123.
13. Rogers LF, Poznanske AK. Imaging of epiphyseal
6. Havranek P, Lizler J. Magnetic resonance imaging injuries. Radiology 1994;191(2):297-308.
in the evaluation of partial growth arrest after
14. Smith BG, Rand F, Jaramillo D, Shapiro F. Early MR
physeal injuries in children. J Bone Joint Surg
imaging of lower extremity fracture separation: A
1991;73(8):1234-1241.
preliminary report. J Ped Orthop 1994; 14:526-533.
7. Howman-Giles R, Trochei M, Yeates K, Middleton
15. Snyder M, Harcke HT, Bowen JR, Caro PA.
R, Barrett I, Scougall J, Whiteway D. Partial growth
Evaluation of physeal behavior in response to
plate closure: apex view on bone scan. J Pediatr
epiphysiodesis with use of serial magnetic resonance
Orthop 1985;5:109-111.
imaging. J Bone Joint Surg 1994;76A:224-229.
8. Jaramillo D, Hoffer FA, Shapiro F, Rand F. MR
16. Young JWR, Bright RW, Whitley NO. Computed
imaging of fractures of the growth plate. Am J
tomography in the evaluation of partial growth
Roentgonol 1990;155:1261-1265.
plate arrest in children. Skeletal Radiol 1986;15:530-
9. Jaramillo D, Laor T, Zaleske DJ. Indirect trauma 535.

28
5 The growth mechanism in the peripheral
part of the normal growth plate
A. Langenskiöld
In 1987 Sandberg and Vuorio(8) studying
skeletal tissues in human fetuses found
in some experiments that the cells in the
cambium layer of the periosteum adjacent
to growth plates contained cartilage-specific
Type II collagen messengerRNA. According
to Ranvier’s view expressed in 1889(6), the
cells of the inner layer of periosteum laying
in close connection with the ossification
groove originate in cells of the epiphyseal
cartilage. Since then, the origin of the tissue
in the ossification groove of Ranvier and the
adjacent cambium layer of the periosteum has
been debated in the literature. Morphologic
studies have not given conclusive evidence
about the possible histogenetic relationship
between cartilage of the growth plate and
the tissue of the ossification groove(9), which
merge at a marked morphologic border.
It has been shown that a change in the type
of collagen synthesized does not necessarily
occur at the same time as the morphologic
change(5). The writer in cooperation with the
biochemists(3) decided to find out whether
the cambium layer of the periosteum close
to the growth plate contains Type II collagen
mRNA also at a later stage of development.
In fibular heads of one-month-old rabbits
Type II collagen mRNA was found in the
innermost layer of cells in the ossification
groove of Ranvier and in a thin layer of
cells in the adjacent cambium layer of the
periosteum.
The experimental results thus provide
strong evidence for the view that cells in the
ossification groove and in the cambium layer
of the bone cuff surrounding the plate originate
in the cartilage of the growth plate.
In 1967 Langenskiöld et al. (2) found in
experiments with autoradiography of growth
plates containing 35S phenomena which
showed interstitial growth and expansion
transversely to the long axis of the bone in
the germinative layer of the growth plate.
The only author except Langenskiöld
and coworkers who has observed interstitial
growth and resulting cell migration towards
the periphery in the germinal or stem cell layer
in the growth plate is Rigal(7). In order to further
study the evident cell migration towards the
periphery in normal growth plates experiments
with vital staining were performed(4). Vital
staining experiments may make visible certain
aspects of the normal developmental processes
that otherwise are hidden to direct observation.
Agar-agar carrying the dye Nile Blue was
implanted in the head of the fibula in one-
month-old rabbits. In frozen sections in 19 of
38 growth plates a row of stained cells could
be seen in the germinal cell layer in the area
between the implant and the inner corner
of the ossification groove. This finding was
29
A. Langenskiöld
predicted and produced additional proof for
the normal occurrence of migration of cells
towards the periphery in the germinal layer.
Experimental results published in 1950(1),
1967(2) and 1993(3,4) allow the conclusion that
stem cells in the germinal layer of a normal
growth plate migrate towards the periphery
and the ossification groove. Some of these cells
give rise to new cartilage cell columns at the
innerside of the groove. Other cells enter the
innermost layer in the ossification groove,
lose their surrounding ground substance
but retain their ability to synthesize Type II
collagen mRNA until they are osteoblasts in
the cambium layer of the periosteum of the
bone cuff.
The growth mechanism in the peripheral
part of the growth plate plays a great role in
the pathogenesis of several diseases of the
growing skeleton.
REFERENCES
1. Langenskiöld A, Edgren W. Imitation of
chondrodysplasia by localized roentgen ray
injury - an experimental study of bone growth.
Acta Chir Scand 1950;99:353.
2. Langenskiöld A, Videman T, Rytömaa T. An
autographic study with 35S-sulphate on the growth
30
in diameter of ephyseal cartilage in rabbits. Acta
Orthop Scand (Suppl 106)1967;1-25.
3. Langenskiöld A, Elima K, Vuorio E. Specific
collagen mRNAs elucidate the histogenetic
relationship between the growth plate, the tissue
in the ossification groove of Ranvier, and the
cambium layer of the adjacent periosteum - a
preliminary report. Clin Orthop 1993;297:51.
4. Langenskiöld A, Videman T, Nevalainen T. Vital
staining indicating cell migration towards the
periphery in the growth plate. Acta Orthop Scand
1993;64:683.
5. Von der Mark K, Conrad G. Cartilage cell
differentiation. Rev. Clin Orthop 1979;139:185.
6. Ranvier L. Trait( Technique d’Histologie, ed.2.
Paris, Savy, 1889, pp. 342, 353, 357.
7. Rigal W M. Diaphyseal aclasis. In: The growth plate
and its disorders (Ed. Rang M.) E. & S Livingstone
Ltd. Edinburgh 1969:91-102.
8. Sandberg M, Vuorio E. Localization of types I, II
and III collagen mRNAs in developing human
skeletal tissues by in situ hybridization. J Cell Biol
1987;104:1077.
9. Shapiro F, Holtrop M E, Glimcher M J. Organization
and cellular biology of the perichondrial
ossification groove of Ranvier: a morphological
study in rabbits. J Bone Joint Surg 1977;59A:703.
 Part II
Basic research
6 Growth cartilage arrest with staples.
Experimental study
J. González-Herranz
INTRODUCTION
Arresting growth by means of staples
or epiphysiodesis is a surgical procedure
which, after enjoying widespread favour
some decades ago, fell into almost complete
disuse(10,12,44). On the one hand, there was the
aversion involved in voluntarily damaging
healthy growth cartilage; on the other, there
was the development of external fixators
which simplified bone lengthening(25,26,38).
Furthermore, these are interventions which
entail many unknowns: will complete
correction be achieved?; how long will the
process take?; what is the ideal age?; for
how long should the staples be kept in?;
will growth resume anew or will it remain
permanently affected? These are questions
that make growth-arrest therapy a somewhat
thorny issue. Although there are different
methods that play a part in determining
growth prognosis(6,32,39) in certain cases the
rate and rhythm of growth can be altered(35,45).
Then again, the possibility of undertaking
such treatments does not present itself every
day, since it is unusual to find surgeons with
much experience in this field(15,36). As a result,
one tends to regard treatments of this nature
with a degree of circumspection.
Nonetheless, epiphysiodesis has witnessed
a certain resurgence, owing to the fact that it
is a straightforward, economical and aesthetic
Research conducted at the Department of Orthopaedics of the
University of Navarra Medical School
method, occasioning a low incidence of
complications. Growth arrest, with the aid
of image intensification control(14,16,18,41), or
selective surgical approach(9) is a technique
that is not unduly traumatic, easy to perform
and effective in terms of results. In many
countries, such as the United States, where
the population tends on average to be tall, the
combination of the high social and financial cost
of surgery and the frequency of malpractice
suits has caused surgeons to become less
interventionist(15,29), leading them back -to a
certain extent- to performing epiphysiodeses.
The least aggressive treatments are increasingly
becoming more attractive to patients and
surgeons alike.
Interest in growth arrest has led to the
development of a new method, namely,
percutaneous ablation of the epiphysiodesis,
under image intensification control, using
drills(14,16,18,19,41,42). While these new techniques
have failed to contribute any important
qualitative advantages, Blount’s method has
nonetheless been all but forgotten and its
reputation tarnished by old clichés, such as
insufficiency in contention due to the rupturing
or widening of the staples.
Growth arrest induced with Blount’s
technique is in no way a universal method
of treatment for the correction of asymmetries
or lateral deformities of the lower extremities,
33
J. González-Herranz
yet it is indicated in pre-adolescents -girls
aged 11 and boys aged 12- of average or above
average height presenting with moderate
asymmetries or angular deformities (from
2.5 to 5 cm). It is likewise applicable in cases
where lengthening is contra-indicated(29), or
as coadjuvant treatment, in a healthy limb,
to offset alterations in growth(35). Blount
stapling should not be employed in patients
aged 8 years or under; in the main, many of
the primary angular deformities of the lower
extremities of children, whether genu varum
or genu valgum, correct spontaneously(6,11,20);
similarly, moderate asymmetries and leg-
length discrepancies of different etiologies
also improve spontaneously(21).
Almost 50 years ago now, Blount (10)
conceived and devised stapling of the growth
cartilage for the treatment of asymmetries and
angular deformities in children, successfully
achieving temporary slowdown in growth in
cases where the duration of such stapling was
for a period under two years. Furthermore,
he observed that, on removing the staples,
the cartilage not only became thicker but
evinced an above-normal rate of growth, a
phenomenon which he termed the rebound
effect and explained as a growth stimulus
arising from decompression of the physis.
The cartilage subsequently returned to normal
and ultimately led to premature closure, 6
months earlier than predicted(11,28). In order to
avoid the controversy surrounding the length
of time during which the staples should be
kept in place, Lerat(37) advised that stapling be
used in girls and boys aged 12 and 13 years
respectively and that the staples be left in situ
until correction was complete, since no rebound
effect had been observed in these patients.
This technique differs from both the
Phemister procedure(44) and percutaneous
epiphysiodeses, in that the slowdown in
growth is temporary and that, under certain
conditions, there may be a subsequent renewal
in growth. Haas was the first to carry out
34
temporary epyphyseal growth arrest by using
a loop of wire around the epiphysis. When this
loop was removed, he observed that growth
renewed(33). With Blount’s method, growth
retardation is brought about mechanically
without directly damaging the growth
cartilage(31). Rupturing or widening of staples
occurs when the resistance of the staples proves
insufficient to arrest the growth cartilage,
and this can be prevented by inserting an
adequate number of staples equipped with
reinforced angles. The advantage of Blount’s
method over epiphysiodeses is that an error
of calculation can be corrected by removing
the staples.
Growth-cartilage behaviour depends on
the action of the mechanical conditions to
which it is subjected. Any modification to
these conditions can significantly alter its
behaviour, and longitudinal growth will
be affected by the magnitude and type of
variation in the physiological conditions.
Knowledge of growth-cartilage mechanics
and physiology will facilitate adaptation to
the clinical needs of many diseases and, more
particularly, ascertainment of the behaviour
of the physis following blockage to growth.
This study aimed: firstly, at verifying
growth-cartilage evolution post-stapling as
well as its growth-renewal capacity following
removal of staples; and at establishing the
relationship between stapling period and
physis response. The findings may be
applied to clinical practice. A further aspect
of importance is the effect of axial deformities
on adjacent bones.
Experimental Study
In order to ascertain the response of growth
cartilage subjected to pressure and the effect of
removing the staples, an experimental study
was carried out on rabbits. The advantage
of this animal lies in the fact that it is easy to
handle, has been used in numerous studies
on growth cartilage and manifests a skeletal

A. Length
B. Length of tibia
α. Angle of femoral condyle
β. Angle of tibia plateau
development of the lower extremities which
can be extrapolated to humans(22,48).
The rabbits were operated on between
the sixth and sixteenth weeks of life, which,
according to Cañadell and Tresserra’s rule
(22,48) (# No. Rabbit days x0.11 = # No. Human
years), corresponds to an age range in humans
of 4 to 12 years. While the alterations that
take place in the physis were more clearly
observable in the youngest rabbits, it was in
the oldest rabbits that the changes, albeit less
pronounced, adapted better to the model of
physeal stapling in the child.
In all cases, the intervention was performed
on the right distal femoral or proximal tibial
physes.
The staples, made of 1.2-millimetre-thick
stainless steel surgical wire, were bent into
a 7 x 7-mm U-shape, 4.6 mm across and 5.8
mm deep. Two staples were always placed
at each side of the site to be blocked. In no
case did we observe complications caused by
rupturing or expulsion of staples. These were
always placed perpendicular to the growth
cartilage, seen as a blueish-white line, without
the need to detach the periosteum.
The animals were distributed at random
into groups, with each group then undergoing
Growth cartilage arrest with staples
Figure 1.
a different surgical technique. Two rabbits
developed a wound infection and had to be
eliminated from the study.
Batch I. Stapling of the outer side of the
femur.
Batch II. Stapling of the inner side of the
tibia.
Batch III. Stapling of the inner side of the
femur.
Batch IV. Temporary stapling of the outer
side of the femur.
Batch V. Stapling of the femoral physis.
Batch VI. Temporary stapling of the
femoral physis.
A follow-up of animal progress was
conducted using weekly radiological
monitoring. Femurs and tibias were
radiographed after excision of muscles
and ligaments: in the radiographs, the
measurements depicted in Figure 1 were taken,
and asymmetry and angulation of the femur
and tibia duly evaluated. Lastly, a description
of the histological study was drawn up.
The following were measured in the
radiographic study of the anatomical
specimen:
1. Angle of inclination of femoral condyle.
Alfa Angle.
35
J. González-Herranz

Table 1. Batch I

N. Weight Days Shortening Femur

10 1000 1 0 mm 0%
14 1650 10 0 mm 0%
24 1500 15 1 mm 1.1%
2 600 23 3 mm 4.4%
51 660 35 7 mm 9.1%
26 1750 38 5 mm 5.2%
22 770 41 7 mm 8.9%
3 1100 44 5 mm 6.0%
50 650 60 14 mm 17.7%

Table 2. Batch II

N. Weight Days Shortening Tibia

31 600 10 1 mm 1.5%
43 1200 30 3 mm 3.2%
27 1400 45 4 mm 3.7%
28 1600 52 5 mm 4.6%
32 700 90 13 mm 12.0%

2. Angle of inclination of the tibial plateau. Batch IV - comprising 5 rabbits. These

Beta Angle.
3. Length of femur.
4. Length of tibia.
5. Width of distal femoral epiphysis.
6. Width of proximal tibial epiphysis.
For histological study purposes, hema-
toxylin-eosine and Masson’s trichrome stains
were used for all rabbits, and Alcian green
stain in isolated cases.
Batch I - comprising 9 rabbits. These
underwent stapling of the outer side of the
distal femur, were observed for 1-60 days
and thereafter killed (Table 1).
Batch II - comprising 5 rabbits. These
underwent stapling of the inner side of the
proximal tibia. The postoperative period was
10-90 days (Table 2).
Batch III - comprising 9 rabbits. These
underwent stapling of the inner side of the
distal femur growth cartilage and were killed
4-90 days postoperation (Table 3).
underwent stapling of the distal femur and
were killed 14-40 days postoperation (Table 4).
Batch V - comprising 13 rabbits. These
first underwent stapling of the outer face of
the distal femur, were kept for a period of 1-7
weeks, were reoperated and the staples then
withdrawn. They were killed 6-72 days after
the second intervention (Table 5).
Batch VI - comprising 9 rabbits. These
first underwent bilateral stapling of the
distal femur, were kept for a period of 8-35
days, were reoperated and the staples then
withdrawn. They were killed 7-30 days after
removal of staples (Table 6).
RESULTS
Batch I
The rabbits developed genu valgum and
a shortening of the right femur. Growth was
observed to slow down on the outer side,

36
 Growth cartilage arrest with staples

Table 3. Batch III

Right tibia
N. Days Shortening Femur Ang. B Leng.
33 4 0 mm 0% 0° 0 mm
42 21 4 mm 4.9% 0° 0 mm
41 35 6 mm 7.0% 4° + 3 mm
29 50 8 mm 7.6% 10° + 1 mm
37 60 12 mm 11.8% 10° 0 mm
38 71 13 mm 12.7% 8° + 1 mm
36 80 15 mm 14.4% 12° + 2 mm
35 85 16 mm 15.4% 16° + 4 mm
34 90 19 mm 18.1% 14° + 2 mm

Table 4. Batch IV Progress and development of the shortening

N. Weight Days
8 800 14
55 1200 21
9 800 27
7 900 31
6870 40
whilst continuing on the inner side. There
was broadening of the condyles, since growth
in width was not compromised. Angulation
took place progressively, with evidence of a
relationship between duration of stapling and
condyle angulation. In cases where condyle
angulation exceeded 24º, there was outward
dislocation of the kneecap, thus accentuating
the external aspect of the deformity. The major
part of the deformity took place in the first
month: thereafter, the arrest in growth on
the outer side had the effect of slowing down
bone growth and producing a shortening
of the femur. Detailed individual results
are given in percentage terms in Table 1.
Figure 2 illustrates the relationship between
the increase in condyle angulation and the
duration of blockage to growth on the outer
side of the femur. As normal values, we took
angulation of the condyles of the left femur.
is analysed in Figure 3. In no case did we
observe any angulation of the tibial plateau
in the tibia of the same side that might have
tended to compensate the genu valgum, or
any discrepancies in tibia length.
Batch II
The rabbits developed a varus deformity
and a shortening of the tibia. The tibial
plateau bent outwards due to the arrest
in growth of the internal portion of the
physis. The varus angulation became
rapidly more pronounced, particularly
among the youngest animals. Table 2 sets
out the results in percentage terms. Figure 4
illustrates how angulation of the tibial plateau
increased with stapling period, the steepest
slope being in evidence at the outset. The
shortening of the right tibia, though initially
small, increased when growth of the inner
side was definitively arrested. Latitudinal
epiphyseal growth was accentuated in the
stapled epiphyses. In no case did we observe
inward dislocation of the kneecap. Growth
stimulus was seen solely in the homolateral
femur of the longest-surviving rabbit, which,
in addition, developed a slight angulation
of the distal femoral epiphysis in order to
offset the varus deformity.

37
J. González-Herranz

Table 5. Batch V

N. Weight Staples Follow-up Total

17 2000 gr 8 19 27
12 2000 gr 14 22 36
15 1500 gr 14 54 68
13 1900 gr 14 58 72
44 1200 gr 14 28 42
18 1400 gr 17 26 43
40 1200 gr 21 16 37
23 1800 gr 24 15 39
39 1000 gr 30 20 50
16 1350 gr 32 4 36
19 1600 gr 37 14 51
1 850 gr 40 36 76
25 1550 gr 41 15 56
21 900 gr 42 6 48
20 1500 gr 46 15 61

Table 6. Batch VI

N. Weight Staples Days Follow-up Total

53 1500 gr 8 7 15
54 1500 gr 14 20 34
52 1500 gr 15 7 22
48 650 gr 21 12 33
46 600 gr 30 15 45
49 700 gr 30 7 47
5 900 gr 32 30 62
47 600 gr 33 28 61
45 1050 gr 35 9 44

Batch III though this was not constant. The findings,

The rabbits developed a varus deformity
and a shortening of the femur, due to medial
angulation of the femoral condyles. The
deformity became rapidly more pronounced
in the first 3 weeks. The kneecap was unstable
and became inwardly dislocated in cases where
angulation exceeded 22º. We observed that
the upper end of the right tibia manifested:
an outward (valgus) angulation that was
linked to the inward (varus) angulation of
the femoral condyle; and, growth stimulus,
set out in percentage terms, are detailed in
Table 3. Figure 5 shows how angulation of
the femoral condyles became progressively
more pronounced over the initial weeks. The
opposite or outward angulation of the tibial
plateau, likewise increased progressively, albeit
at a lower rate. The left tibia underwent no
change. Figure 6 depicts the shortening process
of the femur, its progressive accentuation,
as well as the irregular hypergrowth seen in
the right tibia.

38
 Growth cartilage arrest with staples

Alfa Angle Shortening

Femur
70°
20%
60°
50° 15%
40°
> 1000 gr
30° 10% > 1000 gr
< 1000 gr
< 1000 gr
20°
5%
10°
0° 0%
0 5 10 15 20 25 30 35 40 45 50 55 60
Days 0 5 10 15 20 25 30 35 40 45 50 55 60
Days

Figure 2. Figure 3.

Beta Angle Beta Angle

60° 20°
Right Beta
50°
0°
40°
-20°
30° Right
Left -40°
20°
10° -60° Right Alfa

0° -80°
0 10 20 30 40 50 60 70 80 90 0 14 24 34 44 54 64 74 84
Days Alfa Angle Days

Figure 4. Figure 5.

Shortening Angle
20% 60°
Under 1000 gr
Femur % 50°
15%
40° Over 1000 gr
10%
30°
5%
20°
0%
Tibia % 10°
-5% 0°
4 14 24 34 44 54 64 74 84 1 11 21 31 41 51 61 71 81
Hypergrowth Days Days

Figure 6. Figure 7.

OVERALL RESULTS FOR BATCHES I, II weight and an initial age of 5 to 9 weeks (4

AND III to 7.2 years of life in humans).
Rabbits in Batches I, II and III were jointly Group B: those over 1000 grammes in
evaluated and distributed by weight into weight and an initial age of 10 to 14 weeks
two groups: (8 to 11 years of life in humans).
Group A: those under 1000 grammes in We observed that the degree of angulation

39
J. González-Herranz

Table 7a. Group A

N. Batch days Angle Shortening

33 III 4 2° 0 mm
31 II 10 5° 1 mm
42 III 21 24° 4 mm
2 I 23 36° 3 mm
41 III 35 40° 6 mm
51 I 35 50° 7 mm
22 I 41 52° 7 mm
37 III 60 40° 12 mm
50 I 60 60° 14 mm
38 III 71 46° 13 mm
36 III 83 46° 15 mm
35 III 83 58° 16 mm
32 II 90 50° 13 mm
34 III 90 62° 19 mm

Table 7b. Group B

N. Batch days Angle Shortening

10 I 1 6° 0 mm
14 I 10 8° 0 mm
24 I 15 18° 1 mm
43 II 30 30° 3 mm
26 I 38 43° 5 mm
3 I 44 54° 5 mm
27 II 45 34° 4 mm
28 II 52 36° 5 mm
29 III 50 40° 8 mm

and asymmetry, produced over a similar
period of time, proved to be greater among the
youngest rabbits. Data are set out in Tables 7a
and b. By plotting these data in graphical form
on an XY-axis, the evolution of the deformity at
the knee can be depicted in degrees (Fig. 7). It
will be noted that, as reported above, the major
part of the deformity developed during the
first month, with the rate of increase slowing
thereafter. In the youngest rabbits, the deformity
increased at a quicker pace.
Findings of the histological study
performed on Batch-I, -II and -III rabbits
with asymmetrical stapling of the growth
cartilage were as follows:
In the first week, cell columns were seen
to be inclined due to the effect of the pressure,
and the cartilage interior revealed the presence
of fissures. The bent bone trabeculae in the
metaphysis were cut transversely, displaying a
honeycomb pattern. Increased vascularization
was observed in the epiphysis (Photographs
1-A and B). No alterations were in evidence
on the nonstapled side of the growth cartilage.
In the second week of stapling, these
developments became more pronounced;
there was a considerable fall in the number
of hypertrophic and proliferative cells in the
cartilage, with the horizontal rents becoming
increasingly larger and the columns more

40

A B
Photo 1-A. Histological cross-section of the distal
femur. Rabbit 33, Batch III, subjected to 4 days of
asymmetrical stapling. (Masson’s trichrome stain.
Tessovar 5x).
Thickness on the stapled side is visibly diminished.
The perichondrial ring is enlarged.
disorganised. The columns of peripheral cells
situated in the proximity of the perichondrial
ring bent outwards, assuming a fan shape
(Photograph 2). In the metaphysis, the bone
trabeculae became ever fewer and thicker, with
no new trabeculae forming. The medullary
canal extended as far as the proximity of the
physis. In the epiphysis, the epiphyseal plate
grew thicker and there was a decrease in
vascularization, while on the nonstapled side,
the first signs of the effect of pressure were
by now in evidence.
Growth cartilage arrest with staples
Photo 1-B. Histological cross-section of the distal
femur. Rabbit 33, Batch III, subjected to 4 days
of asymmetrical stapling. (Masson’s trichrome
stain. 100 x).
The cartilage retains its arrangement in slightly
inclined, stacked columns. In the metaphyseal area,
the bone trabeculae are cut obliquely, displaying a
“honeycomb” pattern.
In the third week the formation of bony
bridges, initially small and limited to the areas
of greatest pressure, was first observed. In the
perichondrial ring, the cartilaginous cells grew
beyond the limits of the bone, giving rise to
exostosis (Photograph 3). Bone trabeculae in
the metaphysis, were few in number, thick
and arranged perpendicularly to the axis of
growth. The medullary canal extended as
far as the furthermost cells of the physeal
cartilage. Further thickening of the epiphyseal
plate was observable.
41
J. González-Herranz
Photo 2. Histological cross-section of the distal
femur. Rabbit 14, Batch I, subjected to 10 days of
asymmetrical stapling. (Masson’s trichrome stain.
100 x).
Seen in the outermost peripheral area, close to the
perichondrial ring, is the angulation of the cell
columns. The pressure-induced quasi-transversal
arrangement favours latitudinal epiphyseal growth.
The nonstapled side of the growth cartilage
continued to grow but the effects of the pressure
were now in evidence, with the presence of
fissures and loss of cartilage thickness being
similar to that observed in the cartilage which
had been subjected to a week of stapling.
In the fourth and subsequent weeks,
the growth cartilage manifested large-
sized bony bridges where remnants of
42
Photo 3. Histological cross-section of the distal
femur. Rabbit 8, Batch IV, subjected to 14 days of
asymmetrical stapling. (Masson’s trichrome stain.
Tessovar 5x).
The growth cartilage, though irregular in thickness
and shape, is intact throughout.
In the central area, that of lowest pressure, there
is continued formation of cartilaginous cells that
extend into the medullary canal. On either side, in
areas of greatest pressure, the cartilage is irregular,
and visible on the outer side is the formation of a
treelike bony excrescence, reminiscent of an exostosis
cartilage were present, and failed to
show the characteristic arrangement in
columns, while the cartilaginous matrix
had a more eosinophilic coloration and was
completely surrounded by lamellar bone,
at times forming cartilaginous islets. On
the nonstapled side, the growth cartilage
was preserved, yet there were evident signs
of inactivity, the cellular columns had lost

a great number of cells and there was no
formation of new bone trabeculae.
Growth arrest on the nonstapled side was
complete by the sixth week.
Batch IV
Following symmetrical stapling of the
distal femur, rabbit femurs manifested
a shortening linked to the duration of the
stapling period. The resulting asymmetry was
more pronounced than that brought about by
asymmetrical stapling. No angular deformities
resulted in any animal. Only in one rabbit was
there evidence of greater growth of the tibia
on the same side.
Histological examination of samples after
one day’s evolution revealed little change.
In the first week, there was progressive
loss of growth-cartilage thickness, owing
to the nonappearance of new proliferative-
layer cells and continued mineralization of the
fundamental substance of the physeal cartilage.
Cell columns and trabeculae bent in response to
the pressure, losing their parallel arrangement.
In peripheral areas the columns bent outwards,
this being the area of least pressure. In the
cartilage interior, horizontal rents appeared.
Due to angulation, the metaphyseal bone
trabeculae were cut obliquely, displaying a
honeycomb pattern. Transverse or latitudinal
growth continued despite the presence of
the staples.
Initially, the changes on the epiphyseal
side were less striking, with only an increase
in vascularization being observed in the
epiphyseal plate.
In the second and third weeks of stapling,
growth became fully arrested. The cell columns
displayed considerable variation in length,
with disorganisation being more marked in
areas of greatest pressure. In addition, fissures
were more frequent, at times showing blood
cells in the interior. Transversal growth not
only continued but was seen to increase, with
the perichondrial ring being supplemented by
Growth cartilage arrest with staples
Photo 4. Histological cross-section of the distal
femur. Rabbit 9, Batch IV, subjected to 27 days of
asymmetrical stapling. (Masson’s trichrome stain.
25x). The section of cartilage located between the
staple pins is the area subjected to greatest pressure.
It is here that bony bridges first begin to appear. In
the epiphyseal area, a thickening of the growth plate
and a decrease in vascularization are in evidence.
the action of cell columns positioned almost
transversally. The transversal diameter
widened constantly. Cell-column arrangement
became unrecognisable. The thickness of the
physis was always less than that of the control
side. The metaphyseal bone trabeculae were
enlarged and were not arranged longitudinally,
but rather in the honeycomb pattern described
above. The epiphysis too was observed to be
more flattened.
From the end of third week until the
conclusion of the study period (eighth week
of stapling), the growth cartilage continued to
undergo a loss in thickness and the columnar
arrangement became reduced to a few
disorganised cells, with no trace of the layers
of proliferative or hypertrophic cells. Fissures
became increasingly more frequent and larger,
developing into wide separations between the
cartilage and metaphysis, and constituting
genuine lyses. In the areas of greatest pressure
-those sited close to the staples- we observed
small bony bridges (Photograph 4) that,
with time, grew in frequency and size. The
epiphyseal plate was thicker, more compact
and less vascularized than the normal side.
43
J. González-Herranz
In the metaphysis, the trabeculae were few in
number, thicker and irregular. The medullary
canal was in contact with what remained of
the growth cartilage. The physis had become
reduced to a few rows of cells invaded by
vessels and left in a lethargic state. Although
longitudinal growth was arrested during the
entire period, in the peripheral area of the
physis latitudinal growth held steady, with
the perichondrial ring and some transversally-
arranged columns continuing to form bone.
On occasion this produced a type of exostosis
which totally concealed the implant, and it
became necessary to excise part of this tissue so
as to be able to extract the staples and perform
the histological cross-section, a task which at
times did not prove at all easy.
Batch V
In Batch-V rabbits among which stapling
had been maintained for periods of under three
weeks, on removal of staples, these were seen
to be covered by fibrocartilaginous tissue.
Where a longer time had elapsed however,
the staples in question were covered by bone,
rendering withdrawal difficult. Batch I served
as control for Batch V, which was used to
study physeal capacity for growth renewal
and the time required for the process to be
reversible. We observed that rabbits which
had undergone stapling for periods of under
2 weeks displayed hardly any angulation, and
that shortening of the femur was negligible or
nonexistent, regardless of the time the bone
was subsequently left to evolve. For stapling
periods of 17 to 24 days, there was a moderate
deformity and shortening, which remained
stable after removal of staples. Lastly, rabbits
which had undergone stapling for periods of
over 30 days, developed an outward (valgus)
angulation and a shortening linked to total
time of postoperative evolution, though this
was of a lower intensity than that observed
for Batch-I rabbits which had undergone
stapling for the same period. On occasion,
44
Photo 5. Histological cross-section of the distal
femur. Rabbit 53, Batch VI, subjected to 8 days of
symmetrical stapling and killed 7 days after removal
of staples. (Alcian green stain. Tessovar 10 x).
The cartilage is considerably thicker, with fissures
and cysts visible in the interior. The layers of
hypertrophic and proliferative cells are substantially
enlarged. New trabeculae have not yet formed.
Existing bone forms a horizontal bar parallel to
the physis.
the tibia on the stapled side manifested a
slight growth stimulus, unrelated to either
the magnitude of angulation or the gravity
of the shortening.
Batch VI
All rabbits exhibited shortening. In those
that underwent stapling for periods of 3 weeks
or less, asymmetry was moderate and in no
case was tibial growth stimulus observed. All
rabbits with stapling periods of 30 days or more
manifested a very pronounced shortening of
the femur, though this was of lower intensity
than that experienced by Batch-IV rabbits,
except in two similar cases -rabbits 5 and
46- in which permanent closure took place;
the latter two also registered greatest tibial
growth stimulus.
After staples kept in place for 1 and 2 weeks
had been removed and the rabbit in question
killed a week thereafter, substantial thickening
of the growth cartilage was observed, the cells
had recovered their column-like arrangement,
the layer of hypertrophic cells had become

enlarged to several times its normal size, there
was hardly any area of mineralization and
the newly-formed bone trabeculae were short
(Photograph 5). In areas where pressure had
been greatest, the cartilage was thicker than
in the remainder of the physis, which was
wider throughout than on the control side.
The fissures observed in the cartilage interior
had migrated and were situated closer to the
metaphysis.
In those rabbits which underwent stapling
for 1 or 2 weeks and were killed 2 and 3
weeks thereafter, the cartilage displayed a
thickness similar to normal and an area of
mineralization comparable to the healthy side,
with the nonstapled side being distinguishable
solely by virtue of the increased thickness of
the epiphysis. Four weeks after removal of
staples, cartilage thickness had diminished, all
layers being equally affected; in the interior,
horizontal rents again appeared, signalling a
loss in the cartilage’s power of growth. In the
metaphysis, some distance from the neoformed
trabeculae, thicker horizontally-arranged bone
trabeculae were observed, corresponding to the
metaphyseal plate produced on growth arrest.
This indicated that, after a period without
growth, growth had then resumed.
After 3 weeks of stapling and 2 weeks of
postoperative evolution, the cartilage was
observed to be less thick than on the normal
side, with the metaphysis continuing to show
the presence of growth arrest lines, which had
migrated distally from the physis. We observed
the first signs of bony bridges and areas of
inactive physes, a decrease in the number of
cells, loss of orientation, absence of formation
of new bone trabeculae, with an appearance
similar to cartilage subjected to pressure over
a long period, all indicating that the end of
longitudinal growth was very close.
After 1 month of stapling and 1 week of
postoperative evolution, it was observed
that there were areas in the cartilage where
growth had resumed, leading to the stacking
Growth cartilage arrest with staples
Photo 6. Histological cross-section of the distal
femur. Rabbit 45, Batch VI, subjected to 35 days
of symmetrical stapling and killed 9 days after
removal of staples. (Masson’s trichrome stain. 100x).
The cartilage is composed of a line of cells lacking
columnar arrangement. Vessels are first seen to
invade the physis. In the metaphyseal area, the
bone trabeculae are mature and no new bone is
being formed.
of cells and formation of normal-looking bone
trabeculae in the central area. In other areas
however, the cartilage had remained inactive,
growth in such cases being limited to the
periphery, where the cell columns that had lost
orientation had given rise to bone trabeculae
which were growing beyond the limits of the
bone. Longitudinal growth was practically
nonexistent (Photograph 6). In the second
week, the peripheral areas showed evidence
of substantial bony bridges (stemming from
bone trabeculae that had formed and grown
beyond the perichondrial ring) constituting
genuine exostoses, while in the remaining
growth cartilage, inactive and normal-looking
areas alternated. Over the following weeks, the
inactive areas of the growth cartilage became
steadily larger. After 4 weeks or more, the
growth cartilage, which in some sections
proved to be intact, had become totally inactive,
scarcely contributing to longitudinal growth;
in other sections, the bony bridges that were
present increased in size, affecting the greater
part of the cartilage. Growth arrest was by
now complete.
45
J. González-Herranz
To sum up: where a physis which had
been stapled for a period of under three
weeks was then freed, renewed growth
took place, the cartilage underwent rapid
growth in thickness and, on resumption
of longitudinal growth, the cell columns
aligned longitudinally, separating the old
bone trabeculae, radiographically interpreted
as growth arrest lines(40). Increase in growth-
cartilage thickness is brought about by the
layer of hypertrophic cells: this is attributed
to the cartilage’s lack of mineralization
capacity -the vascular invasion advances more
slowly than the proliferation of cartilaginous
cells(49,50)- and not to a post-decompression
growth stimulus; Christensen(24) has shown
that cartilage retains only 50 to 80% of its
growth capacity on being released after solely
1 week of stapling. Thereafter, the vessels
gradually mineralize the cartilage, replacing it
with normal bone trabeculae. Growth cartilage
subjected to pressure loses growth capacity
sooner than does the control side.
Growth cartilage progressively loses its
growth potential after 3-4 weeks of compression
regardless of the existence of bony bridges,
and premature physeal closure takes place.
DISCUSSION
Growth-cartilage arrest through insertion
of staples is a surgical technique that is
currently indicated in certain cases: in pre-
adolescents, i.e., 11-year-old girls and 12-year-
old boys(37,43). The optimum duration of the
stapling period is cause for controversy
however. Blount(11) stated that staples could
be kept in place for up to 2 years without
growth being irreversibly affected. He also
advocated hypercorrection to offset the
rebound effect, which in under-twelves is
not offset by premature closure of the physis.
Lerat advised the use of stapling in girls and
boys aged 12 and 13 years respectively and
maintenance of staples in situ until correction
46
was complete, since no rebound effect had
been observed in such patients(37).
The rebound effect, according to Zuege
and Blount, is greater in the youngest children
and disappears after the ages of 13 in girls and
14 in boys; after these ages, staples should
therefore be immediately removed as and
when correction is achieved. This effect is
more intense in asymmetrical stapling for
correction of angulations, than in correction
of leg-length inequality(52).
Experimental stapling-induced growth-
cartilage arrest, has been previously studied,
in both its morphological and histological
aspects(5,7,24,27). Thanks to these studies, the
chronological behaviour of growth cartilage
is now known, as are the effects produced
by pressure on the physis, e.g., the fact that
growth is arrested in under a week.
The primary goal of this study was: to
monitor and examine physeal evolution with
asymmetrical stapling of the distal end of the
femur and proximal end of the tibia; and to
evaluate post-operative progress in different
age groups, along with any resulting effects
on the chain of adjacent bones.
Batch-I rabbits developed a valgus
angulation and a shortening of the right femur.
Staple pressure exerted on the physis changes
the normal columnar cellular arrangement and,
seeking areas of least pressure, the growth
cartilage extends beyond its normal limits,
growing in width(34). Condyle angulation is
progressive and is linked to the duration of
stapling.
Outward dislocation of the kneecap causes
a fibrocartilaginous tissue to form on the outer
face of the femoral condyle, which covers the
staples and renders removal difficult. The
major part of the deformity develops in the
first month, after blockage to growth of the
outer side slows down bone growth, producing
the greatest shortening in the femur. In no
case did we observe any angulation of the
tibial plateau in the tibia of the same side that

might have tended to compensate the genu
valgum, or any discrepancies in tibia length.
Expressed in percentage terms, growth
arrest evinces a relationship with stapling
period and animal weight/age.
Asymmetrical stapling of the proximal
tibial physis (Batch II) caused angulation of the
tibial plateau, inducing a varus deformity of the
knee and a shortening of the tibia. The varus
deformity increases rapidly, particularly in the
youngest rabbits. The proximal tibial epiphysis
is broader due to the greater latitudinal growth
experienced by the stapled epiphyses. In no
case did we observe inward dislocation of the
kneecap. Growth stimulus is seen only after
a long period of evolution.
Asymmetrical stapling of the distal femur
(Batch III) caused a varus angulation and
a shortening of the femur. Expressed in
percentage terms, the resulting asymmetry
proves slightly less than for a Batch-I rabbit
of similar age and stapling period. The tibia
constantly shows a valgus angulation, in an
opposite direction to that of the femur, and a
growth stimulus which, though not constant,
is indeed present in the majority of cases. It
is known that an increase in pressure can
arrest growth and that a reduction in pressure
can stimulate longitudinal growth (23). The
varus deformity at the knee has the effect
of lowering the strain on the internal tibial
hemiepiphysis, which would respond with a
growth stimulus, thereby favouring a valgus
angulation and greater tibial length. A similar
situation has been reproduced by Burgos et
al. After excision of the internal condyle of
the femur, thus producing genu varum in the
rabbit, they observed that the proximal end
of the tibia developed a valgus angulation if
subjected to weight-bearing demands(17). This
effect has not been observed in cases where
the femoral deformity is valgus, arguably
due to the fact that weight-bearing demands
on the limb diminish when a deformity is
valgus in nature. This is in no way related
Growth cartilage arrest with staples
to post-traumatic unilateral genu valgum,
which is brought about by a disorder in the
consolidation of the medial aspect of the
fracture, leading to stimulus of the medial
epiphyseal plate which maintains the valgus
deformity(30).
In the Batch-IV rabbits, bilateral stapling
induced a more pronounced shortening
than in Batch-I and -III rabbits in similar
circumstances. Overall comparison of the
deformities induced in Group-A rabbits (under
1000 g in weight and an initial age of 5 to 9
weeks of life, equivalent to 4 to 7.2 years of life
in humans) as against Group-B rabbits (over
1000 grammes in weight and an initial age of
10 to 14 weeks, equivalent to 8 to 11 years of
life in humans) shows that, except for the first
two weeks when angulation of the femoral
condyles of the youngest animals was less
physiologically pronounced, for the remainder
of the period, angulation was always greater
in the youngest animals owing to their greater
growth potential. The same thing occurred
with regard to shortening, in that it was more
pronounced at lower ages.
On the basis of the results obtained, Batch-V
rabbits were divided into two groups:
- Group 1, comprising rabbits that had been
stapled for a period of under three weeks.
- Group 2, comprising rabbits that had been
stapled for a period of over three weeks.
Group 1 rabbits, corresponding to a
stapling period of under two years in children,
displayed a small degree of asymmetry ranging
from 1% of hypergrowth and no angulation of
the femoral condyles in rabbit no. 17, stapled
for only 8 days, to a 40º valgus angulation of
the femur in rabbit no. 40, stapled for 21 days.
In Group 2, corresponding to a stapling
period of over two years in children, mean
angulation was 45º and mean shortening
around 7%. There was only one exception:
rabbit no. 1 had an angulation of 58º and a
shortening of 23.7%. Observation showed
the situation in the remaining rabbits to be
47
J. González-Herranz
intermediate, in that they had an angulation
greater than a Batch-I rabbit with the same
stapling period yet less than the deformity
which they should have had, taking total
postoperative time into account. This indicates
that, despite the existence of bony bridges of
varying importance in all rabbits in this group,
continued longitudinal growth is in evidence.
Batch-VI rabbits, including those rabbits
that had undergone stapling for a period of
less than 3 weeks, exhibited a shortening that
was more marked and in accordance with
the stapling period. Those rabbits that had
undergone stapling for a period of over 3
weeks exhibited a very pronounced shortening,
of a magnitude considerably surpassing
that warranted by the stapling period yet
corresponding to them by virtue of the total
postoperative period. This therefore indicates
that longitudinal growth is definitively arrested
after three weeks of bilateral stapling. The
pressure exerted in the case of bilateral stapling
is far greater than that exerted by asymmetrical
stapling, where longitudinal growth persists
for a longer time. A growth stimulus in the tibia
of the stapled side was present in the majority
of rabbits with postoperative periods of over
45 days. Wilson-MacDonald et al. were able to
establish that, on subjecting the proximal tibial
growth cartilage to compression, a growth
stimulus was induced in the distal physis
of the same bone, which proved greater in
cases where incision of the periosteum had
been performed(51).
As regards the histological aspect, in
asymmetrical stapling changes induced
by the increase in pressure on the growth
cartilage are seen at an early stage(34). The
first manifestation, visible as from the first
week, is the “honeycomb” arrangement of
the metaphyseal trabeculae, attributable
to the angulation of the bone trabeculae,
which on being cut transversally, display a
honeycomb pattern(24). Already by the third
day, the width of the compressed physis shows
48
a marked reduction in thickness(13), which
can diminish to as little as one third of the
normal physis(3). However the hypertrophic
cells witness the greatest changes, at times
assuming the appearance of a hollow shell(2).
In the first week, the cell columns are observed
to bend, seeking the peripheral area of least
pressure, and fissures are seen to appear,
corresponding to degenerative zones devoid
of cartilaginous matrix and vessels. On the
epiphyseal side of the growth cartilage an
increase in vascularization is in evidence, with
penetration of the capillary endings into the
germinal-cell area, similar to what is observed
in the first weeks of physeal distraction(4). No
change is seen on the nonstapled side.
During the second week, the stapled side
reveals both an appreciable diminution in the
layer of hypertrophic and proliferative cells,
mimicking the typical cellular arrangement
in layers(13,24), as well as a greater number
of fissures with the presence of small bony
bridges. The peripheral cell columns situated
in the proximity of the perichondrial ring
bend outwards, growing beyond the limits
of the bone. The epiphyseal plate is enlarged
and shows reduced vascularization, whilst in
rabbits subjected to distraction, the increase
in vascularization remains evident until day
21(4). On the metaphyseal side, the presence
of small numbers of thick trabeculae indicates
growth arrest, with the medullary canal
extending as far as the proximity of the physis.
On the nonstapled side growth is observed
to continue; the cartilaginous-cell columns
remain intact giving rise to normal-looking
bone trabeculae, but in the cartilage interior
fissures begin to appear.
In the third week, the stapled side registers
serious changes: cartilage thickness has
diminished very considerably, it now being
impossible to distinguish the different types
of cartilaginous cells, which are no longer
arranged in columnar form, and the fissures are
larger, constituting genuine lyses. The presence

of bony bridges, initially small and limited
to areas of greatest pressure, is a constant
feature; Christensen and Alberty failed to
observe this development until day 45(3,24). In
the perichondrial ring, the cartilaginous cells
grow beyond the limits of the bone, altering
the appearance of the epiphysis which has
assumed a funnel-like shape(2). Increase in
latitudinal epiphyseal growth has likewise been
observed in epiphyses subjected to distraction,
yet the cause in this case is unknown(1). In the
metaphysis, the few trabeculae that remain
are thick, arranged perpendicularly to the
axis of growth and consist of mature lamellar
bone. The medullary canal extends as far as
the furthermost cells of the physeal cartilage.
The nonstapled side of the growth cartilage
continues to grow but the effects of the pressure
are by now evident, with presence of fissures
and loss of cartilage thickness similar to that
observed in cartilage subjected to a week of
stapling.
During the fourth and subsequent weeks:
the stapled side, in addition to the above,
showed the bony bridges to be located in the
peripheral area, joining the epiphysis to the
metaphysis, a sign of irreversible damage to
the growth cartilage; and the nonstapled side
showed the damage becoming increasingly
more striking, with fissures in evidence, scant
numbers of new trabeculae forming and those
that did, failing to arrange along the axis of
bone growth.
During the sixth and seventh weeks, the
nonstapled side became seriously affected,
with growth arrest becoming complete.
Within the space of a few weeks,
mechanical compression of the growth
cartilage reproduces the physiological process
of physeal closure(2,3,24).
In symmetrical stapling of the physis, the
changes that take place in the growth cartilage,
while similar to those described above, share
the peculiarity of being more pronounced and
appearing at a more accelerated rate.
Growth cartilage arrest with staples
In the second week, although the growth
cartilage is intact, changes are observed in
the columnar arrangement of cells, thickness
diminishes (mainly because of the layers of
hypertrophic and proliferative cells), whilst
the layer of germinal cells remains unaltered
throughout the period(2). In the cartilage
interior there are horizontal rents or fissures
coinciding with local invasion of vessels. In the
central area, where pressure is lowest, there
is continued proliferation of cartilaginous
cells which form tongues that extend towards
the metaphysis but make no contribution to
bone growth.
By the third week, the growth cartilage
has completely lost its normal arrangement.
The layer of germinal cells appears to be
transformed into fibro-cartilage, displaying
large waves and a dearth of cells, and the first
signs of bony bridges are in evidence(13). By
the time the layer of germinal cells, which
is the heart of the growth cartilage(8,47), has
become altered, the changes are already
irreversible. In the outermost peripheral area
of cartilage, where the pressure is greatest,
there is an almost constant presence of bony
bridges, a phenomenon reported by Amako
and Honda yet not observed by Alberty and
Christensen until the sixth week(3,5,24). The
transversal rents in the cartilage exhibit a
substantial increase in size. The epiphyseal
plate is formed by bone that is compact and
of greater thickness, in which the capillaries
that irrigate the germinal cells of the physis
have diminished to a considerable degree. In
the metaphysis, the medullary canal extends
as far as the proximity of the physis and the
trabeculae are few in number and broad.
In the fourth week we, like Bonnevialle and
cols.(13), observed the presence of evident bony
bridges, indicative of irreversible changes in
the growth cartilage. The remaining alterations
continue, becoming ever more accentuated.
In the fifth and subsequent weeks, the
growth cartilage shows signs of complete
49
J. González-Herranz
inactivity, being formed by few cells displaying
no specific arrangement and extensive bony
bridges.
The histological appearance of growth
cartilage subjected to asymmetrical
compression for a period of time and then
released, depends to a great extent on the
duration of the compression period. Group 1
rabbits undergoing stapling for a period of 3
weeks or less, present with slight variations:
the cartilage itself is wholly intact, there is
an enlargement of the hypertrophic- and
proliferative-cell areas, and the overall
appearance is similar to that exhibited by
growth cartilage subjected to distraction(3,4). In
cases that undergo stapling for longer periods,
fissures and cyst-like areas are observed in the
interior, while in the central area of the physis
a substantial and very striking proliferation
of cartilaginous cells is in evidence, with
these extending towards the medullary
canal and forming a cartilaginous tongue.
The metaphysis is marked by formation of
new bone trabeculae, differentiated from the
older trabeculae by reason of their greater
thickness. No changes are to be seen on the
stapled side.
A common histological finding among
Group-2 rabbits subjected to compression for
a period exceeding 4 weeks is the presence
of a fairly sizeable peripheral bony bridge.
In the central area and on the nonstapled
side, where pressure is lowest, the cartilage
is thicker, mainly due to the increase in
hypertrophic cells. In the metaphysis there
is little evidence of formation of new bone
trabeculae. On the nonstapled side, the growth
cartilage shows the characteristic columns that
form bone trabeculae but, due to the effect of
the pressure, these are bent and transversally
cut, displaying a honeycomb pattern. In the
outermost peripheral area, the angulation
of the columns is outward with respect to
the limits of the bone. In those rabbits with
lengthy postoperative periods, the growth
50
cartilage disappears altogether on the stapled
side, leaving only scattered islets of isolated
cartilaginous cells.
In Batch-VI rabbits undergoing stapling for
a period of 2 weeks or less, the growth cartilage
is enlarged, and the layers of hypertrophic and
proliferative cells very developed. In those
with shortest postoperative periods, the area
of cartilage mineralization is minimal, there
being no time for new bone trabeculae to form.
The appearance is similar to that of cartilage
subjected to distraction(1), owing to the fact
that multiplication of cartilaginous cells is
swifter than the invasion of metaphyseal
vessels, causing calcification of the matrix
and subsequent ossification. Where the
postoperative period is longer, formation
of new, normal-looking bone trabeculae
is observed. Overall, the growth cartilage
manifests signs evincing the effects of pressure,
fissures and cystic areas. In line with Amako
and Honda(5), we are of the opinion that, for
renewed growth to take place on removal of
staples, 2 weeks is the period during which
the physis can remain stapled. Alberty, on
the other hand, argues that such a period
should be at least 3 weeks, with the technical
difference here that he applied compression
progressively with the aid of an external
fixator(2).
The most important factor for normal
longitudinal growth is preservation of the
integrity of the epiphyseal capillaries and
the activity of the proliferative cells(4,8,46).
There is a relationship between changes
in vascularization and growth disorders.
Penetration of epiphyseal vessels into the
physis may lead to premature closure of the
physis(4).
In rabbits undergoing stapling for a period
of 3 weeks or more, the growth cartilage exhibits
the alterations characteristic of pressure:
fissures, loss of cell-column orientation
and small bony bridges in the outermost
peripheral areas, which are larger in rabbits

that undergo the longest stapling periods. The
process reaches a maximum in rabbits with
the longest postoperative periods, where the
growth cartilage disappears almost completely,
leaving behind only some small islets. In the
central area where the effects of pressure are
least pronounced, there is a proliferation of
cartilaginous cells which penetrate into the
medullary canal, yet make no contribution to
longitudinal bone growth. In the metaphysis
there are remnants of old trabeculae which
retain a transversal arrangement and formed
a bony bar.
CONCLUSIONS
1. - Asymmetrical, staple-mediated arrest
of the outer side of the distal femoral growth
cartilage induces a genu valgum deformity
in the rabbit, with no compensatory effect
on the tibia.
2. - Blockage to the inner side of the distal
femoral growth cartilage induces a genu varum
deformity, which in turn induces a growth
stimulus in the tibia and an angulation opposite
to that of the femur.
3. - The varus angulation of the tibia,
induced by asymmetrical stapling of the inner
side of the proximal tibial growth cartilage,
has no effect on femoral growth.
4. - Asymmetrical stapling of a growth
cartilage arrests growth on the stapled side in
the first week, while on the nonstapled side,
longitudinal growth remains normal for 3
weeks, thereafter slowing down progressively
until total arrest is seen in the 5th week.
5. - The maximum length of time during
which staples may be kept in place in order
for growth to renew, is three weeks in
asymmetrical and two weeks in symmetrical
stapling.
6. - The histological arrangement of the
growth cartilage that remains fertile after
being released from the staples, is similar to
that produced by ischaemia. The invasion of
Growth cartilage arrest with staples
metaphyseal vessels, which gives rise to the
mineralization of the cartilaginous matrix,
advances more slowly than the division and
stacking of cartilaginous cells, producing the
image of a broadening of the growth cartilage,
traditionally attributed to a growth stimulus.
REFERENCES
1. Alberty A, Peltonen J and Ritsilä V. Distraction
effect on the physis in rabbits. Acta Orthop. Scand.
1990;61:258-62.
2. Alberty A, Peltonen J and Ritsilä V. Effects of
distraction and compression on proliferation of
growth plate chondrocytes. A study in rabbits.
Acta Orthop. Scand. 1993;64:449-445.
3. Alberty A, Peltonen J and Lindberg LA. Early
ultrastructural changes of the growth plate
chondrocytes after compression and distraction
of the physis in rabbits. Eur. J. Exp. Musculoskel.
Res. 1993;2:18-24.
4. Alberty A. Effects of physeal distraction on
the vascular supply of the growth area: a
microangiographical study in rabbits. J. Pediatr.
Orthop. 1993;13:373-7.
5. Amako T and Honda K. An experimental study
of epiphyseal stapling. Kyushu J. Med. Sci., 1957;
8:131-8
6. Anderson M, Green WT and Messner MB. Growth
and predictions of growth in lower extremities.
J. Bone Joint Surg. 1963;45-A:1-14.
7. Baer MJ and Ackerman JL. A longitudinal vital
straining method for study of apposition in bone.
In Evans FG. Studies on the anatomy and function
of bone and joints. New York, Springer-Verlag
1966.
8. Barash ES and Siffert RS. The potential for growth
of experimentally produced hemiepiphyses. J.
Bone Joint Surg. 1966;48-A:1548-53.
9. Birch JG, Herring JA and Wenger DR. Surgical
anatomy of select physes. J. Pediatr. Orthop. 1984;
4:224-31.
51
J. González-Herranz
10. Blount WP and Clarke GR. Control of bone growth
by epiphyseal stapling. Preliminary report. J. Bone
Joint Surg. 1949;31-A:464-78.
11. Blount WP and Zeier F. Control of bone length.
J.A.M.A. 1952;148:451-7.
12. Blount WP. A mature look at epiphyseal stapling.
Clin Orthop. 1971;77:158-163.
13. Bonnevialle P, Durroux R, Cahuzac JP, Lebarbier
P, Laville JM and Pasquie M. Traitement des
déviations frontales du genou par épiphysiodèse
temporaire de Blount. Étude expérimentale et
clinique. Rev. Chir. Orthop. 1982;68:115-22.
14. Bowen JR and Johnsons WJ. Percutaneous
epiphysiodesis. Clin. Orthop. 1984;190:170-3.
15. Bowler JR, Mubarak SJ. and Wenger DR. Tibial
physeal closure and genu recurvatum after femoral
fracture: Occurrence without a tibial traction pin.
J. Pediatr. Orthop. 1990;10:653-7.
16. Brax P and Gille P. Lépiphysiodèse percutanée.
Chir. Pédiatr. 1989;30:263-5.
17. Burgos Flores J, Cuevas Sanchez B, Calvo Asensio
M, Gonzalez Herranz, P and Ocete Guzman G.
The study of infantile articular plasticity. Mapfre
Medicina. 1993. Vol 4, supl II: 289-93.
18. Canale ST, Russell TA and Holcomb RL.
Percutaneous epiphysiodesis: Experimental study
and preliminary clinical results. J. Pediatr. Orthop.
1986;6:150-6.
19. Canale ST and Christian CA. Techniques for
epiphysiodesis about the knee. Clin. Orthop.
1989;255:81-5.
20. Cañadell J, de Pablos J. Lesiones del cartílago de
crecimiento. Eunsa. Pamplona, 1988.
21. Cañadell J, Ponces J, Blanquet A, Escayola JL,
Figueras JM, Tresserra J y Hernández A. Nuestra
experiencia en el tratamiento de las diferencias de
longitud de las extremidades inferiores. Anales
de Medicina. 1962, Vol. 48-2. Barcelona.
22. Cañadell J. and Tresserra J. Estudio clínico-
experimental de la actividad relativa de las fisis
tibiales. Medicina Clínica. 1974;63:402-7.
52
23. Cañadell J. Verificación de los factores que influyen
sobre la actividad del cartílago de crecimeinto.
Tesis Doctoral. Universidad de Barcelona. 1967.
24. Christensen NO. Growth arrest by stapling. Acta
Orthop. Scand. 1973, Supp. 151.
25. De Bastiani G, Aldegheri R, Renzi-Brivio L and
Triviella G. Limb lengthening by callus distraction.
Callostasis. J. Pediatr. Orthop. 1987;7:129-34.
26. de Pablos J and Cañadell, J. Methods of bone
lengthening and their applications. Universidad
de Navarra. 1990.
27. Ehrlich MG, Mankin HJ and Treadwell BV.
Biochemical and physiological events during
closure of the stapled distal femoral epiphyseal
plate in rats. J. Bone Joint Surg. 1972;54-A:309-22.
28. Frantz CN. Epiphyseal stapling. A comprehensive
review. Clin Orthop. 1971;77:149-57.
29. Frediani P, Nocivelli P and Capilupi B. Il ruolo
dell’ epifisiodesi nel trattamento delle dismetrie
degli arti inferiori. Chir. Org. Mov. 1987;72:221-
6.
30. Frey P. Growth disturbance following metaphyseal
bending fractures of the proximal tibia. An
experimental study in mini pig. Z. Kinderchir.
1990;45:291-7.
31. Gelbke H. The influence of pressure and tension
on growing in experiments with animal. J. Bone
Joint Surg. 1951;33-A:947-954.
32. Greulich WW and Pyle SI. Radiographic atlas
of skeletal development of the hand and wrist.
Stanford University Press, Stanford, 1950.
33. Haas L. Retardation of bone growth by wire loop.
J. Bone Joint Surg. 1945;27-A:25-36.
34. Karbowski A and Camps L. Morphologische,
morphometrische und stereologische aspekte
einseitiger Blountscher klammerung der
wachstumsfuge im tierexperiment. Z Orthop.
1985; 123:403-8.
35. Langenskiold A. Growth disturbance after
osteomyelitis of femoral condyles in infants. Acta
Orthop. Scand. 1984;55:1-13.

36. Lee EH, Gao GX and Bose K. Management of
partial growth arrest: physis, fat or silastic? J.
Pediatr. Orthop. 1993;13:368-72.
37. Lerat JL, Bérard J and Rebouillat J. Place du
traitement chirurgical du genu valgum par
épiphysiodèse controlée chez l’ enfant et l’
adolescent. Lyon Chirurgical. 1978;74:31-36.
38. Lokietek W, Legaye J and Lokietek JC. Contributing
factor for osteogenesis in children’s limb
lengthening. J. Pediatr. Orthop. 1991;11:452-458.
39. Moseley CF. A straight-line graph for leg-length
discrepancies. J. Bone Joint Surg. 1977;59-A:174-
9.
40. Ogden JA. Growth slowdown and arrest lines. J.
Pediatr. Orthop. 1984;4:409-15.
41. Ogilvie JW. Epiphysiodesis: Evaluation of a new
technique. J. Pediatr. Orthop. 1986;6:147-9.
42. Ogilvie JW and King K. Epiphysiodesis: two-year
clinical results using a new technique. J. Pediatr.
Orthop. 1990;10:809-11.
43. Peterson HA. Partial growth plate arrest and its
treatment. J. Pediatr. Orthop. 1984;4:246-258.
44. Phemister DB. Operative arrest of longitudinal
growth of bones in treatment of deformities. J.
Bone Joint Surg. 1933;15:1-15.
Growth cartilage arrest with staples
45. Shapiro F. Development patterns in lower-extremity
length discrepancies. J. Bone Joint Surg. 1982;64-
A:639-51.
46. Siffert RS. Lower limb-length discrepancy. J. Bone
Joint Surg. 1987;69-A:1100-6.
47. Siffert RS. The effects of staples and longitudinal
wires on epiphyseal growth. J. Bone Joint Surg.
1956;38-A:1077-1088.
48. Tresserra J. Secciones músculo-ligamentosas en
el conejo común en período de crecimiento. Tesis
Doctoral. Universidad de Barcelona, 1964.
49. Trueta J. Studies of the development and decay
of the human frame. W.B.Saunders. Philadelphia,
1968.
50. Trueta J and Amato VP. The vascular contribution
to osteogenesis. Changes in the growth cartilage
caused by experimentally induced ischemia. J.
Bone Joint Surg. 1960;42-B:571-87.
51. Wilson-MacDonald J, Houghton GR, Bradley J and
Morscher E. The relationship between periostial
division and compression or distraction of the
growth plate. An experimental study in rabbits.
J. Bone Joint Surg. 1990;72-B:303-8.
52. Zuege RC, Kempken TG and Blount WP.
Epiphyseal stapling for angular deformity at
the knee. J. Bone Joint Surg. 1979;61-A:320-9.
53
7 Physeal arrest. Research in percutaneous
epiphysiodesis
U. Givon, S. Ishikawa, K.W. Dabney, H.T. Harcke and J.R. Bowen
INTRODUCTION
Lower limb length discrepancy or angular
deformity can be caused by congenital
disorders, trauma, infection, tumors, thermal
injury and other condition that affect the
growth of the lower limbs(1). Any direct insult
to the physis in children may inhibit normal
growth. Trauma, especially the Salter Harris
type 4 or type 5 fracture, can cause a growth
disturbance due to the formation of a bony
bridge and a tether between the epiphysis and
the metaphysis. Osteomyelitis adjacent to the
physis may result in damage to physeal cells
and growth disturbance unless treated early.
Tumor invasion of the physis, thermal injury,
iatrogenic damage or avascular necrosis due
to circulatory disturbance to the epiphysis
may also result in damage to the physis, and
subsequent length inequality.
For the patient with lower limb length
discrepancy or angular deformity due
to premature closure of the physis, there
are several treatment options, depending
on the degree of deformity at the time of
skeletal maturity. These options include no
treatment, a shoe lift, excision of physeal bar,
epiphysiodesis, elongation and prosthetics(1).
Each option has specific indications and the
reader is referred to the appropriate chapter.
Epiphysiodesis is one of the more frequently
performed procedures for limb length
54 Partly reprinted with permission of Mapfre Medicina (vol. 4, suppl 2)
equalization; it has the advantages of low
morbidity, relative ease of performance, high
rate of success and low complication rates.
The disadvantages of this procedure is that the
“normal” extremity must be operated on and
may result in patients having shorter stature
then predicted(1-6). Complications associated
with open epiphysiodesis were reported(7),
and in the last 2 decades several methods of
percutaneous epiphysiodesis were reported,
offering certain advantages over conventional
epiphysiodesis(2,8-12).
Research concerning the physis has
primarily concentrated on defining the
normal anatomy and physiology. Recently
research on various imaging techniques has
concentrated on improved methods to assess
both the normal and pathological anatomy of
the physis. In the past radiography and linear
and multiplanar conventional tomography
were widely used to assess physeal abnorma-
lities(1,4,6,14-18). Newer methods using bone
scintigraphy, computed tomography (CT), and
magnetic resonance imaging (MRI) have added
to our abilities of evaluating the physis(6,15,18-30).
Research investigating surgical arrest of the
physis has been limited and has involved
experimental work with animal models and
clinical research utilizing various imaging
modalities.
The aim of this chapter is to review

the recent clinical and animal research
investigating the effect of percutaneous
epiphysiodesis. Understanding the anatomy,
physiology and radiological features of the
normal and abnormal physis is important to
fully appreciate the clinical implications of
percutaneous epiphysiodesis.
NORMAL PHYSIS
In the immature skeleton the physes is the
main site of longitudinal growth of the long
bones(31). For example, the distal femoral physis
provides 70% of the longitudinal growth of
the femur, while the proximal tibial physis
provides 60% of the total tibial length(1). As the
child matures, the physis gradually narrows
until it is completely closed. The age at which
the physis is obliterated is specific for each
physis and is influenced by gender, nutritional,
endocrine and genetic factors(17).
Embryology of the physis
At the beginning of the seventh gestational
week, mesenchymal condensations transform
into cartilaginous anlage, which represents
the configuration of future long bones.
During the early fetal period, the process
of bone formation within the cartilaginous
anlage commences and the primary center
of ossification forms. At first, enchondral
ossification is confined to the two structures
called physes at the proximal and distal ends
of the primary ossification center. As grows
continues the physes move away from each
other. The secondary ossification center, the
epiphysis, appears at the end of each long
bone. The epiphysis serves as a centrifugal
growth mechanism, similar to the that of
the physis.
Anatomy and function of the normal
physis
The physis is composed of hyaline
cartilage and includes three major layers:
Physeal arrest. Research in percutaneous epiphysiodesis
the reserve zone, the proliferative zone, and
the hypertrophic zone. The hypertrophic
zone is further divided into the maturation
zone, the degenerative zone and the zone of
provisional calcification. The reserve zone is
just adjacent to the epiphysis. The cells in the
reserve zone contain more lipid bodies and
vacuoles than cells in other zones, and probably
functions as a storage area for the nutritional
requirements of the physis. The layer adjacent
to the reserve zone is the proliferative zone,
it’s function is thought to be matrix production
and cellular proliferation. The hypertrophic
zone functions mainly to prepare the matrix
for calcification, and then to calcify it. The
metaphysis takes part in the longitudinal
growth process in the primary spongiosa and
secondary spongiosa zones. In the primary
spongiosa zone, the cartilage is invaded by
vascular tissue and osteoblasts, but almost
no change in the matrix is observed. In the
secondary spongiosa zone, the osteoblasts
start laying bone on the cartilage, which is
later replaced by lamellar bone. Chondrocyte
derived growth factors may be taking part in
the growth of metaphyseal blood vessels into
the physis(32).
RADIOLOGICAL FEATURES OF THE
NORMAL PHYSIS
Plain Radiography
The normal physis is seen as a radioluscent
zone between the epiphysis and the metaphysis
of the long bone, with a varying appearance
dependent on age and gender. Soon after
birth the lower extremity epiphyses are
mainly cartilaginous, although the secondary
ossification is usually identified at the distal
femur and the proximal tibia. Other secondary
ossification centers appear during childhood.
As the secondary ossification center grows, the
white linear zone of provisional calcification
may be seen at the margin of the metaphysis.
When the epiphysis is similar to that of an
55
U. Givon, S. Ishikawa, K.W. Dabney, H.T. Harcke, J.R. Bowen
adult, the physis is clearly seen between the
epiphysis and metaphysis. With maturity the
physis becomes thinner and later completely
ossifies. At that stage the physis may appear
irregular because of asymmetrical fusion(33).
Conventional tomography
Tomography can frequently show a clear
view of the physis in the plane of interest.
Physes in the long bones have an axial
orientation, and therefore tomographic views
perpendicular to the physis may be useful in
examining a specific area of physeal cartilage,
metaphysis or epiphysis(15).
Scintigraphy
The radiographic physis and the
scintigraphic physis do not represent the same
structure. In the growing child, the physes
have increased uptake of technetium 99m
phosphate. The bands of intense uptake are
seen in the metaphyseal - epiphyseal areas
of the long bones, and represent deposition
in the zones of provisional calcification and
primary spongiosa, but not in the cartilaginous
physis. Radioisotope uptake has been shown
to correlate with linear growth of bone. In the
infant the scintigraphic physis has a globular
shape, but as the child matures, the physis
becomes a more distinct transverse band of
preferential uptake. This uptake gradually
diminishes with increasing age until physeal
closure(20).
Computerized Tomography (CT)
The major advantage of CT is the ability
to display the cross-sectional anatomy of
structures, in a plane not obtainable by
conventional radiographs. Although CT
scan may not be beneficial for evaluation of
the normal physis, it is still one of the best
modalities for imaging calcified structures.
As such it plays a role in assessing complex
fractures and other lesions affecting the physis
like bony bridges(15,24).
56
Magnetic Resonance Imaging (MRI)
In the radiologic examination of acute
and chronic disorders of the physes, MRI
is beginning to replace other imaging
techniques because it enables the physician
to have multiplane imaging capabilities, no
ionizing irradiation, and excellent soft tissue
contrast resolutions(16,25-30). Pulse sequence
selection is important in studying the physis.
Field echo images show cartilage with high
signal intensity, and are recommended in
conjunction with T1 weighted images. MRI
studies of the normal physis were reported
in detail by Jaramillo et al(25,26) and by Harcke
et al (25,28). According to Harcke’s report,
based on MRI studies of normal knees, the
appearance of the normal physis in a child can
be divided into four developmental stages. In
stage 1, children less then 2 years of age, the
physis is wide and the cartilaginous signal
is continuous. In stage 2, children between
the ages of two and 12 years, the secondary
ossification center is larger and occupies a
greater part of the epiphysis; therefore the
physis signal is thinner but generally well
delineated. The contour of the distal femoral
physis changes from transverse to binodal.
The signal intensity of the cartilage band
varies. On T1 weighted images, the cartilage is
visualized as an intermediate signal intensity,
and on field echo images, it has high intensity.
In stage 3, children older then 12 years, and
depending on the child’s sex and exact age,
physeal closure may become apparent. In
several cases, typically in 14 -15 year old
children, there is a non-identifiable area in the
central part of the physis. This phenomenon
was termed the drop out sign and should not
be confused with physeal closure (Fig. 1A
and 1B). In some cases the cartilage signal is
almost absent throughout most of the physis
on T1-weighted images, while the hyper-
intense signal is clearly visible in field echo
images. Pulse sequence, therefore clearly
influences cartilage visualization and failure
 Physeal arrest. Research in percutaneous epiphysiodesis

A B
Figure 1. Coronal magnetic resonance images of the knee in a normal 13 year old male illustrating the
“drop out” sign. A) T-1 weighted image (TR 650, TE 20) shows physeal cartilage with intermediate signal
intensity. Cartilage is not visible in the mid portion of the proximal tibial physis. B) Field echo images
(TR 700, TE 20, 90° flip angle) show cartilage with high signal intensity. Note that the proximal tibial
physeal cartilage is present across the entire width of the physis.

to select the correct sequence could lead to
misdiagnosis. In stage 4, during the period
of complete physeal closure, the physis is
exhibits a single low intensity band between
the metaphysis and epiphysis.
ABNORMAL PHYSIS
An abnormal physis can be seen under
many pathologic conditions, and the radiologic
image may vary according to the etiology(33).
Following the animal study by Jaramillo et
al.(16), histological findings after physeal injury
can be divided into four stages: hemorragic
due to disruption of cartilage (0-3 days), early
vascularization with subacute hemorrhage
(4-7 days), vascular invasion with peripheral
ossification (8-15 days), and central deposition
of bone and bone marrow formation (16-28
days, 7-8 weeks).
Radiologic evaluation of the abnormal
physis
Plain radiography is useful in the evaluation
of the abnormal physis. Other modalities such
as conventional tomography, scintigraphy CT
and MRI have been employed in for definitive
diagnosis in children with premature physeal
arrest. The purpose of using these modalities
is to assess the extent of physeal damage or
to define a bony bridge and select treatment
options. A bony bridge is usually discovered
months after injury, and the physeal damage
may be diagnosed only after a deformity has
already occurred(4,6,34). Therefore the patient
should be followed closely after a physeal
injury to enable early diagnosis of a bony
bridge before obvious deformity occurs(34).
Plain radiography
Plain radiography is recommended as

57
U. Givon, S. Ishikawa, K.W. Dabney, H.T. Harcke, J.R. Bowen
an initial imaging procedure to detect the
presence of a bony bridge(15,34); however, it
frequently does not define the size and location
of the bony bridge. In experimental study
using rabbits, Makela et al. reported that
plain radiography failed to show bony bridge
formation and was of little value in predicting
growth disturbance. They concluded that
radiography is not suitable for three-
dimensional interpretation of physeal arrest(18).
Other reviews state that most bony bridges in
the human can be adequately diagnosed by
plain radiography. Furthermore, this is the
conventional method of follow up of children
sustaining physeal injuries(6).
Radiographic appearance of physeal
abnormalities include widening, narrowing
and irregularity of the physis and a centrally
abnormal physis. Widening of the physis is
usually apparent in patients with Salter-Harris
type 1 injury, rickets and chondrodystrophies.
Physeal narrowing may be due to compression
injury as seen in the Salter-Harris type V
lesions, or in praecox puberty with premature
physeal closure. Irregularity may appear
in patients with trauma, tumor, infection
or radiation damage; although it may be a
normal developmental stage. A centrally
abnormal physis may result from damage
to the center of the physis, demonstrating
the classic “fishtail” deformity indicative of
a central bony bridge.
Conventional Tomography
Tomography may determine the
configuration and location of bony bar, and
may be useful for mapping the bridge(4). Carlson
and Wenger (14) have reported a mapping
method using bi-planar tomography. Using
that technique they concluded that an accurate
assessment of the size and location of the bony
bridge is feasible. However, conflicting reports
by other authors state that even high quality
tomograms do not provide adequate detail
of a relatively blurry image(24,29).
58
Scintigraphy
Scintigraphy has been proposed as a
technique for evaluation of the physis during
bony bridge formation. Harcke et al. used
quantitative scintigraphy for the evaluation
of patients with angular deformity of the
lower limbs. They demonstrated the ratio
of counts in the medial two segments of the
bone compared to the counts in the lateral
two segments correlated with varus or valgus
deformity. They proposed that this technique
may provide a possible means of monitoring
growth after trauma or infection(21) (Figs.
2A, 2B, and 2C). Howman-Giles et al. used
an apex view on bone scan as a method to
specifically image the physis of the distal
femur. They concluded that this technique
has the potential of the physis before or after
surgery(22).
Computerized tomography
Peterson stated that CT scans are of little
value in assessing a bony bar because of the
irregularity of the physis(4). On the other hand,
there have been several experimental and
clinical reports supporting the use of CT in
the evaluation of a bony bar(20,24,35). A common
view point in these reports is that CT scans can
provide a well defined demarcation between
the bridge and the cartilage. Thus, the use of
CT is still controversial.
Magnetic Resonance Imaging
More recently, MRI has been used
increasingly for the evaluation of physeal
arrest. Jaramillo et al. evaluated bony bridge
formation with MRI in a rabbit model(16).
In this experimental study they reported
that the abnormality in the cartilage and the
penetration of the physis by vascular tissue
was detected by MRI. Enhanced T1 weighted
images were useful as an indicator of early
bony bridge formation. The bony bridge
tended to be seen better on MRI then with
other imaging modalities. A clinical study of

Figure 2. Premature closure of the proximal tibial
physis in a 13 year old male following trauma.
A) Antero-posterior radiograph of the knee showing
demineralization, the physes appear open. B) Early
phase image (blood pool) from technetium 99m
phosphate bone scan. Uptake of tracer in the right
proximal tibial physis is diminished. C) Delayed
bone image (2 hours) shows decreased uptake in
proximal right tibial physis. This is noted in a physis
that is in the process of closing.
children with physeal injury demonstrated
that MRI is a sensitive modality able to
detect physeal abnormalities associated
with premature physeal closure and bony
bridge formation. Interruption of the physis
as seen in T2 weighted images was associated
with physeal closure in 6 out of 8 cases. MRI
provided accurate mapping of the bony
bridge crossing the physis(25,26). Other reports
support this as well, suggesting T1 weighted
images as the giving detailed information
about the anatomy of the affected area(27) or a
Physeal arrest. Research in percutaneous epiphysiodesis
C
combination of T1 and field echo images(28,29).
Another possible MRI finding is physeal
widening. Laor et al(36) described this finding
in detail and suggested that it may represent
a previous or ongoing metaphyseal injury,
causing cessation of bone formation and
replacement of hypertrophic chondrocytes.
This finding is more likely to be associated
with a growth disturbance when there is a
history of a single injury event rather than an
ongoing one; when the lesion has the shape of a
focal tongue rather than a band; and when the
59
U. Givon, S. Ishikawa, K.W. Dabney, H.T. Harcke, J.R. Bowen
lesion is centrally located in the metaphysis.
Histological examination performed in two
cases showed that the widening represented
hypertrophic chondrocytes extending into the
metaphysis(36). A recently published protocol
for the study of the physis includes coronal
multiplanar gradient recalled sequence to
evaluate for bony bridges; coronal spin echo
sequence to evaluate the zone of provisional
calcification and the course of growth recovery
lines; sagittal spin echo proton density and T2
with fat suppression to evaluate the patency
of the physis and differentiate it from the
articular cartilage(30).
MRI following percutaneous
epiphysiodesis
Snyder and his colleagues(29) followed 14
patients undergoing epiphysiodesis with MRI.
Examination performed two days after the
operation, demonstrated the epiphysiodesis
area in T1 and field echo images. The cartilage
was obliterated in the operated regions, but
was visualized well in the central region
of the physis. The central region appeared
normal in both pulse sequences. A second
MRI performed four months after surgery
demonstrated that fibro-cartilaginous
elements could be identified in the physis
(Figs. 3A and 3B). Field echo images showed
the early formation of an immature bony
bridge in both operated regions. In the central
region several changes were seen. The usual
intermediate signal on T1 was not seen in
eight out of 14 patients. The more sensitive
field echo sequence revealed a narrowed
physis. The presence of mature bony bridge
was evident in the operated regions after 8
months. The central unoperated region did not
demonstrate any presence of cartilage, both
in T1 and field echo sequences (Figs. 3C and
3D). Some physeal cartilage was still present
in the periphery of the physis. No growth
recovery lines were present in metaphysis.
The authors concluded that MRI studies are
60
useful for early diagnosis of a bony bridge,
but not in the physiological evaluation of
the physis.
PERCUTANEOUS EPIPHYSIODESIS
Most of the research done on epiphysiodesis
in the last two decades concentrated on the
development of improved surgical techniques
for epiphysiodesis. Open epiphysiodesis in
the Phemister technique was associated with
several complications, mainly joint stiffness,
infection and unsightly scars. The new methods
for epiphysiodesis, based on the use of image
intensification and percutaneous ablation of
the physis, offered some advantages over open
epiphysiodesis. These advantages include
less surgical dissection, less discomfort after
surgery and a smaller postoperative scar. The
first report of percutaneous epiphysiodesis
was published by Bowen and Johnson(2,8).
They used an osteotome to create an opening
in the physis and then curettes under image
intensification to ablate the medial and
lateral third of each physis. Care was taken
to avoid damage to vessels and nerves in the
popliteal region. Their method necessitated
less dissection, a smaller surgical scar and
less stiffness. The main disadvantage was
the possible neuro-vascular injury. Other
techniques for percutaneous epiphysiodesis
were developed lately. Canale reported a
method utilizing drills and then dental
burrs for epiphysiodesis(9). Ogilvie and King
described a method of drilling in various
directions under image intensification (10).
The use of cannulated drills used through
the whole width of the physis was described
by Gabriel et al.(11). Liotta et al. described a
combination of drilling and curetting through
the physis(12) and a similar technique was
reported by Horton and Olney(37). Macnicol
and Gupta reported on the use of cannulated
tubesaws(13) for ablation of the physis. All the
methods are utilizing image intensification
 Physeal arrest. Research in percutaneous epiphysiodesis

A B

C D

Figure 3. Serial magnetic resonance images in a 13 year old female following percutaneous epiphysiodesis
of the distal femoral physis. A) T-1 weighted image (TR 650 TE 20) six months after surgery. The medial
surgical defect has healed and shows mixed signal intensity. B) Field echo image (TR700, TE 20 40(flip
angle) six months after surgery. The physis of the distal femur is almost completely closed. High signal
cartilage is barely visible. C) T-1 weighted image 15 months after surgery. Mature surgical defect and
obliteration of the physis is noted. D) Field echo image 15 months after surgery. No physeal cartilage is
visible in the femur. Note that the proximal tibial physis is also closed.

61
U. Givon, S. Ishikawa, K.W. Dabney, H.T. Harcke, J.R. Bowen
control and all of them used minimal incisions.
No studies comparing these techniques were
performed so far and all the authors reported
satisfactory results. All authors found the
results of percutaneous epiphysiodesis to be
superior compared to open epiphysiodesis in
the Phemister method(9-13). All these methods
are acceptable in our view, and all of them
have similar advantages and disadvantages. A
study comparing the use of power instruments
to manual instruments is needed, to rule out
a possibility of damage to soft tissues induced
by the use of power instruments.
An experimental study in rabbits and
dogs, examining the use of electro-cautery for
physeal closure was reported by Rosen et al.(38).
They used regular electro-cautery machines
applied to a needle inserted into the physis.
The temperature in the physis was up to 56°
and histologic studies demonstrated disruption
of the cartilage structure with subsequent
bony bridge formation. No clinical work was
published about the use of electro-cautery.
In recent years, research on epiphysiodesis
resulted in several methods for percutaneous
epiphysiodesis, utilizing different instruments
but basically similar. Epiphysiodesis is now
a safe operation with an acceptable rate of
complications, but further research to look
at other modalities, even less invasive may
be indicated. The developments in imaging
techniques, especially in MRI enable us to
diagnose the patient developing a bony bridge
earlier. The changes seen on MRI seem to reflect
the histologic changes in the physis, and further
research should be aimed at understanding
the biochemical changes in the physis during
epiphysiodesis.
REFERENCES
1. Moseley CF. Leg-length discrepancy. In: Morissy RT
(ed.) Lovell and Winter’s Pediatric Orthopedics (3rd
edition), Philadelphia, Lippincott, 1990; 767-813.
62
2. B o w e n J R , J o h n s o n W J . P e r c u t a n e o u s
epiphysiodesis. Clin Orthop 1984;190:170-173.
3. Phemister DB, operative arrestment of longitudinal
growth of bones in the treatment of deformities.
J Bone Joint Surg, 1933;15-A:1-15.
4. Peterson HA. Partial growth arrest and its’
treatment. J Pediatr Orthop, 1984;4:246-258.
5. Bowen JR. Surgical treatment of leg length
discrepancy. In Dee R, Mango E, Hurst LC eds.
Principles of orthopaedic practice. 1st ed. New
York McGraw Hill: 1191-1208; 1989.
6. Guille JT, Yamazaki A, Bowen JR. Physeal surgery:
indications and operative treatment. Am J Orthop,
1997;27:323-332.
7. Menelaus MB. Correction of leg length discrepancy
for length inequality. J Bone Joint Surg, 1966;48-
B:336-339.
8. Timperlake RW, Bowen JR, Guille JT et al.
Prospective evaluation of fifty three consecutive
percutaneous epiphysiodesis of the distal femur
and proximal tibia and fibula. J Pediatr Orthop,
1991;11:350-357.
9. Canale ST, Christian CA. Techniques for
epiphysiodesis about the knee. Clin Orthop,
1990;255:81-85.
10. Ogilvie J, King K. Epiphysiodesis: two year clinical
results using a new technique. J Pediatr Orthop,
1990;10:809-811.
11. Gabriel KR, Crawford AH, Roy DR et al.
Percutaneous epiphysiodesis. Pediatr Orthop,
1994;14: 358-362.
12. Liotta FJ, Ambrose TA, Eilert RE. Fluoroscopic
technique versus Phemister technique for
epiphysiodesis. J Pediatr Orthop, 1992;12:248-251.
13. Macnicol MF, Gupta MS. Epiphysiodesis using
a cannulated tubesaw. J Bone Joint Surg, 1997;79-
B:307-309.
14. Carlson WO, Wenger DR. A mapping method to
prepare for surgical excision of a partial physeal
arrest. J Pediatr Orthop, 1984;4:232-238.

15. Harcke HT. Imaging of the immature skeleton.
In: Morissy RT (ed.) Lovell and Winter’s Pediatric
Orthopedics (3rd edition), Philadelphia, Lippincott,
1990;35-56.
16. Jaramillo D, Shapiro F, Hoffer FA et al.
Posttraumatic growth plate abnormalities: MR
imaging of bony bridge formation in the rabbit.
Radiology, 1990;175:767-773.
17. Kumar R, Madewell JE, Swischuk LE. The normal
and abnormal growth plate. Radiol Clin North Am,
1987;25:1133-1153.
18. Makela AE, Vainionpaa S, Vitonen K et al. The
effect of trauma to the lower femoral epiphyseal
plate. An experimental study in rabbits. J Bone
Joint Surg. 1988;70-B:187-191.
19. Harcke HT, Zaph SE Mandell GA et al. Angular
deformity of the lower extremity: evaluation
with quantitative bone scintigraphy. Radiology,
1987;164:437-440.
20. Murray IP. Bone scanning in the child and the
young adult. Part 1. Skelet Radiol, 1987;5:1-14.
21. Harcke HT, Macy NJ, Mandell GA et al.
Quantitative assessment of growth plate activity.
J Nucl Med, 1984;25:115.
22. Howman-Giles R, Trochei M, Yeats K et al. Partial
growth plate closure: apex view on bone scan. J
Pediatr Orthop, 1985;5:109-111.
23. Murray K, Nixon JW. Epiphyseal growth plate:
evaluation with modified coronal CT. Radiology,
1988;166:263-265.
24. Porat S, Nyska M, Nyska A et al. Assessment
of bony bridge by computed tomography:
experimental model in rabbits and clinical
application. J Pediatr Orthop, 1987;7:155-160.
25. Jaramillo D, Hoffer FA. Cartilaginous epiphysis
and growth plate: normal and abnormal MR
imaging findings. AJR, 1991;158:1105-1110.
26. Jaramillo D, Hoffer FA, Shapiro F et al. MR imaging
of fractures of the growth plate. AJR, 1990;155:1261-
1265.
Physeal arrest. Research in percutaneous epiphysiodesis
27. Havranek P, Lizler J. Magnetic resonance imaging
in the evaluation of partial growth arrest after
physeal injuries in children. J Bone Joint Surg,
1991;73-A:1234-1241.
28. Harcke HT, Snyder M, Caro P et al. Growth plate
of the normal knee: evaluation with MR imaging.
Radiology, 1992;183:119-123.
29. Snyder M, Harcke HT, Bowen JR et al. Evaluation
of physeal behavior in response to epiphysiodesis
with the use of magnetic resonance imaging. J
Bone Joint Surg, 1994;76-A:224-229.
30. Laor T, Chung T, Hoffer FA et al. Musculoskeletal
magnetic resonance imaging: how we do it. Pediatr
Radiol 1996;26:695-700.
31. Brighton CT, Longitudinal bone growth: the
growth plate and its’ dysfunction. Instr Course
Lec 1987;36:3-25.
32. Ianotti JP. Growth plate physiology and pathology.
Orthop Clin North Am 1990;21:1-17.
33. Paul WL, Juhl JH. Bone formation and skeletal
development. In: Essentials of Roentgen diagnosis
of the skeletal system. New York, Harper and
Row, 1967; 3-14.
34. Ogden JA. The evaluation and treatment of partial
physeal arrest. J Bone Joint Surg, 1987;69-A:1297-
1302.
35. Young WJ, Bright RW, Whitley NO. Computed
tomography in the evaluation of partial growth
arrest in children. Skeletal Radiol, 1986;15:530-535.
36. Laor T, Hartman AL, Jaramillo D, Local physeal
widening on MR imaging: an incidental finding
suggesting prior metaphyseal insult. Pediatr Radiol
1997;27:654-662.
37. Horton GA, Olney BW. Epiphysiodesis of the
lower extremity: Results of the percutaneous
technique. J Pediatr Orthop, 1996;16:180-182.
38. Rosen MA, Beer KA, Wiater JP et al. Epiphysiodesis
by electrocautery in the rabbit and dog. Clin Orthop,
1990;256:244-253.
63
8 Trochanteric epiphysiodesis by means of
absorbable screws.
An experimental attempt in rabbits
J. Gil-Albarova, M. Melgosa, R. Gil-Albarova, M. Fini, N. Aldini-Nicolo,
R. Giardino and F. Seral
INTRODUCTION
Relative overgrowth of the Greater
Trochanter (GT) is frequently caused by
the partial or complete physary arrest of
the proximal femoral physis (14), which is
often associated with a short, broad femoral
neck(1). Its relationship to avascular necrosis
of the femoral head, among other causes,
has been well documented (9,13,23) . This
relative overgrowth of the GT conditions
a bio-mechanical dysfunction of the hip,
which provokes lameness accompanied by
a positive sign of Trendelenburg (10). Most
authors recommend GT epiphysiodesis in
children under 8 years of age and the distal
and lateral transposition of the GT in older
chil-dren (1,6,10,23,25), considering that these
methods at least permit the improvement of
the biomechanics of the hip.
The most common clinical application
of absorbable implants in human clinical
practice is fixation of malleolar fractures,
elbow and hand fractures, and physeal
fractures(2,3,4,8,16,18,21). In this study, we investigate
the utility of SR-PGA screws as a method of
GT epiphysiodesis in immature rabbits.
ANIMALS AND METHOD
15 New Zealand white rabbits aged 10
64
weeks and weighing 1.750 ± 0.2 kg were used.
Through an incision over the left greater
trochanter, and after exposing the lateral face
of the same, respecting its vertex, a 4.5 mm
diameter PGA screw (Biofix®) was implanted
reaching the opposite cortical, after a 3.2 mm
drilling and 4.5 mm diestocking. The same
operation was performed on the right greater
trochanter, though without implanting a
screw. Intramuscular Cefazolin was used as
antibiotic prophylaxis (100 mg/kg), beginning
preoperatively and continuing for 3 days.
The animals were allotted into three
subgroups of 5 rabbits (A, B and C) according
to the postoperative follow-up (1, 2 and 3
months respectively). X-rays were taken in a
standardized anteroposterior projection of both
femurs preoperatively, after the operation and
monthly until the death of the animals. In these
X-rays the articulo-trochanteric distance (ATD)
and neck-shaft angle (NSA) were measured.
After sacrifice, both femurs were extracted
for histological study, by means of methacrylate
inclusion. Histological preparations were dyed
with Toluidine blue.
RESULTS
All the animals survived the intervention.
One animal of group A and another of
 Trochanteric epiphysiodesis by means of absorbable screws

Table 1. NSA values (º)

R L R L R L R L
Group A Preop Preop 1m 1m 2m 2m 3m 3m
A1 138 138 140 140
A2 139 139 142 142
A3 138 138 140 140
A4 139 139 140 140
Group B
B1 140 140 140 140 142 142
B2 139 139 140 140 142 142
B3 138 138 140 140 142 142
B4 138 138 140 140 140 140
B5 138 138 142 142 142 142
Group C
C1 140 140 140 140 142 142 142 142
C2 139 139 142 142 144 144 144 144
C3 140 140 142 142 142 142 144 144
C4 138 138 140 140 142 142 142 142

R: Right L: Left m: Postoperative months

Table 2. ATD values (mm)

R L R L R L R L
Group A Preop Preop 1m 1m 2m 2m 3m 3m
A1 -3 -3 -3 -2
A2 -3 -3 -3 -3
A3 -4 -4 -4 -4
A4 -3 -3 -3 -3
Group B
B1 -4 -4 -3 -4 -3 -4
B2 -3 -3 -3 -3 -3 -3
B3 -4 -4 -3 -4 -3 -4
B4 -4 -4 -4 -4 -3 -3
B5 -4 -4 -3 -3 -3 -3
Group C
C1 -4 -4 -3 -3 -2 -3 -2 -3
C2 -4 -4 -3 -3 -2 -3 -1 -3
C3 -3 -3 -2 -3 -2 -3 -1 -2
C4 -3 -3 -2 -2 -2 -2 -2 -2

R: Right L: Left m: Postoperative months

65
J. Gil-Albarova, M. Melgosa, R. Gil-Albarova, M. Fini, N. Aldini-Nicolo, R. Giardino, F. Seral

Figure 1. Two months post-operatively, any

degree of osteolysis in the left trochanteric area
was observed in all the animals.

group C died in the first postoperative

week due to diarrhea. The rest concluded
the study. When the femurs were extracted,
3 caseous accumulations was observed on
the left femur of three animals, without
exterior fistulization, whose culture was
positive to Pasteurella Multocida. Screws
maintained their macroscopic shape in the
animals sacrificed after one postoperative
month (Group A), not being recognizable
in subsequent stages.
Tables 1 and 2 show the results of the
radiological measurements. Due to the
morphology of the proximal extreme of
the rabbit femur, ATD values were always
negative. No relevant variations were observed
in the ATD and NSA values. Neither were
fractures produced. All the animals of our
study developed any degree of osteolysis
in the left trochanteric area from the second
postoperative month (Fig. 1).
In the histological study, the existence of
a bony bridge was found in the right greater
trochanter of all the animals as from the first
postoperative month (Fig. 2). This bony bridge
filled the whole growth plate perforation,
and showed progressive maturation in the
subsequent stages. However, the screw located
in the left greater trochanter maintained its
morphology at one post-operative month,
Figure 2. Right greater trochanter specimen after
1 month postop. Bone bridge across the growth
plate. (Toluidine blue x 40).
preventing the formation of bony tissue
through the growth plate perforation (Fig. 3).
Two months postoperatively, the
peripheral degradation of the screw
permitted the formation of bony tissue from
both sides of the growth plate giving rise
to small marginal bony bridges (Fig. 4).
Three months postoperatively, the greater
degradation of the screw was accompanied
by a greater bony growth through the physis
in the periphery of the screw, although
without reaching the dimensions of the
physary bridge observed in the right greater
trochanter (Fig. 5). At this moment, a thinning
of the trochanter physis was observed with
progressive ossification due to the skeletal
maturation of the animal.

66
 Trochanteric epiphysiodesis by means of absorbable screws
Figure 3. Left greater trochanter specimen after 1
month postop. Intimate contact among the SR-PGA
screw and the physis. It was possible to observe
small physeal fragments dragged to the metaphysis
by the screw itself. (Toluidine blue x 40).
DISCUSSION
Techniques of epiphysiodesis and GT
transposition use metallic screws as the most
common material of osteosynthesis(1,13,14,25),
although this type of implants is not
indispensable(6,10,23). The use of absorbable
osteosynthesis implants is increasingly
frequent in human clinical practice, with
the advantage over metallic implants of not
requiring posterior extraction (2,3,4,8,16,18,21).
However, absorbable screws present smaller
compression capacity, albeit sufficient to
maintain the stability of the osteotomy or of the
fracture in which they are applied, once it has
been reduced(3,4). Their application on physeal
fractures has proved that the degradation of
this type of material does not damage the
growth plate(2,5,8,16).
All the animals of our study developed
a bony bridge in the right trochanter physis
after perforation, such as other authors have
already reported(7,19). Drilling alone generated
a bony bridge with definitive trochanteric
epiphysiodesis. In the left greater trochanter,
our histological observations demonstrate
that during the time in which the screw
maintained its structure, it acted as material
of interposition at the level of the growth
Figure 4. Left greater trochanter specimen after
2 months postop. Peripheral SR-PGA screw
degradation allowed some bone formation from
both sides of the growth plate, across the physis.
(Toluidine blue x 100).
plate, preventing the formation of a bony
bridge, in a similar way to that observed by
other authors with other materials (11,12,22).
However, our radiological results suggest
that the compression capacity of PGA screws
on the trochanter physis in rabbits was
insufficient to prevent their growth(20,24) and
to provoke a relevant modification of the
ATD and the NSA, resulting unable to secure
an epiphysiodesis. A possible explanation
would be that physary growth pressure would
overcome the resistance of the implant, and
would be capable of breaking it as has been
reported previously(15,16).
In the same way as that reported by other
authors(15,17), the peripheral degradation of
the implant two months postoperatively
gave rise to the formation of only slight
bony bridges through the growth plate,
although of small size in comparison with
those observed in the right greater trochanter,
and insufficient to prevent physary growth.
The small size of these bony bridges together
with the loss of the mechanical properties
of the screws in process of degradation
may explain the absence of changes in
the values of the ATD and the NSA. The
greater degradation of the screws observed
67
J. Gil-Albarova, M. Melgosa, R. Gil-Albarova, M. Fini, N. Aldini-Nicolo, R. Giardino, F. Seral
Figure 5. Left greater trochanter specimen after 3
months postop. Greater degradation of SR-PGA
screw was accompanied by more bone tissue
formation across the growth plate, without reaching
the magnitude of the bone bridge observed in the
right greater trochanter. (Toluidine blue x 40).
three months postoperatively permitted the
development of peripheral bony bridges,
though always of smaller size that those
observed in the right greater trochanter. At
this time, neither the values of the ATD or
of the NSA showed any significant changes,
since the bony bridges formed were inefficient
on a closing physis on which the degraded
screw was not exercising any compression.
PGA screws were unable to obtain
epiphysiodesis of GT in rabbits, but our
results suggest two possible uses of absorbable
implants in growth plate surgery: as simple
material of interposition in the treatment of
a bony physary bridge, and as implants with
68
greater compression capacity to obtain an
physary arrest which could cease once the
implant has been absorbed, without damaging
the growth plate. In both cases, both the design
as well as the mechanical properties and the
absorption time of the material employed
should be established according to the clinical
requirements of the case in question.
REFERENCES
1. Bialik V, Rosenberg N. Transfer of greater
trochanter. J Pediatr Orthop (B) 1994;3:30-4.
2. Böstman O M, Mäkelä E A, Törmälä P, Rokkanen P.
Transphyseal fracture fixation using biodegradable
pins. J Bone Joint Surg (Br) 1989:71:706-7.
3. Böstman O M. Absorbable implants for the fixation
of the fractures. J Bone Joint Surg (Am) 1991:73:148-
53.
4. Böstman O M, Pihlajamäki H K, Partio E K,
Rokkanen P U. Clinical biocompatibility and
degradation of polylevolactide screws in the ankle.
Clin Orthop 1995;320:101-9.
5. Donigian A M, Plaga B R, Caskey P M. Biodegradable
fixation of physeal fractures in goat distal femur.
J Pediatr Orthop 1993;13:349-54.
6. Gage J R, Cary J M. The effects of trochanteric
epiphyseodesis on growth of the proximal end of
the femur following necrosis of the capital femoral
epiphysis. J Bone Joint Surg (Am) 1980;62:785-94.
7. Garcés G L, Múgica Garay Y, Lopez Gonzalez
Coviella N, Guerado E. Growth plate modifications
after drilling. J Pediatr Orthop 1994;14:225-8.
8. Hope P G, Williamson D M, Coates C J, Cole W
G. Biodegradable pin fixation of elbow fractures
in children. J Bone Joint Surg (Br) 1991;73:965-8.
9. Kalamchi A, MacEwen D. Avascular necrosis
following treatment of congenital dislocation of
the hip. J Bone Joint Surg (Am) 1980;62:876-88.
10. Langeskiöld A, Salenius P. Epiphyseodesis of the
greater trochanter. Acta Orthop Scand 1967;38:199-
219.
 Trochanteric epiphysiodesis by means of absorbable screws
11. Langeskiöld A. The possibilities of eliminating
premature partial closure of an epiphyseal plate
caused by trauma or disease. Acta Orthop Scand
1967;38:267-79.
12. Lee E H, Gao G X, Bose K. Management of partial
growth arrest: physis, fat or silastic?. J Pediatr
Orthop 1993;13:368-72.
13. Lloyd-Roberts G C, Wetherill M H, Fraser M.
Trochanteric advancement for premature arrest
of the femoral capital growth plate. J Bone Joint
Surg (Br) 1985;67:21-4.
14. Macnicol M F, Makris D. Distal transfer of the
greater trochanter. J Bone Joint Surg (Br) 1991;
73:838-41.
15. Mäkelä E A, Vainionpää S, Vihtonen K, Mero M,
Helevirta P, Törmälä P, Rokkanen P. The effect
of a penetrating biodegradable implant on the
growth plate. An experimental study on growing
rabbits with special reference to polydioxanone.
Clin Orthop 1989;241:300-8.
16. Mäkelä E A, Böstman O M, Kekomäki M,
Södergård J, Vainio J, Törmälä P, Rokkanen P.
Biodegradable fixation of distal humeral physeal
fractures. Clin Orthop 1992;283:237-43.
17. Otsuka N, Mah J Y, Orr F W, Martin R F.
Biodegradation of polydioxanone in bone tissue:
effect on the epiphyseal plate in immature rabbits.
J Pediatr Orthop 1992;12:177-80.
18. Pihlajamäki H, Böstman O M, Manninen M,
Päivärinta U, Törmälä P, Rokkanen P. Absorbable
plugs of self-reinforced poly-L-lactic acid for
fixation of fractures and osteotomies. J Bone Joint
Surg (Br) 1992:74:853-7.
19. Siffert R S. The effect of staples and longitudinal
wires on epiphyseal growth. An experimental
study. J Bone Joint Surg (Am) 1956;38:1077-88.
20. Siffert R S. The growth plate and its affections. J
Bone Joint Surg (Am) 1966;48:546-63.
21. Sinisaari I, Pätiälä H, Böstman O M, Mäkelä E A,
Hirvensalo E, Partio E K, Törmälä P, Rokkanen
P. Metallic or absorbable for ankle fractures. A
comparative study of infection in 3111 cases. Acta
Orthop Scand 1996;67:16-8.
22. Stadelmaier D M, Arnoczky S P, Dodds J, Ross
H. The effect of drilling and soft tissue grafting
across open growth plates. A histologic study.
Am J Sports Med 1995;23:431-5.
23. Stevens P M, Coleman S S. Coxa breva: Its
pathogenesis and a rationale for its management.
J Pediatr Orthop 1985;5:515-21.
24. Strobino L J, Colonna P C, Brodey R S, Leinbach
T. The effect of compression on the growth of
epiphyseal bone. Surg Gyn Obst 1956;103:85-93.
25. Tauber C, Ganel A, Horoszowski H, Farine Y.
Distal transfer of the greater trochanter in coxa
vara. Acta Orthop Scand 1980;51:661-6.
69
9 Physeal distraction: Review of experimental
evidence. What is the response of the cells
on the growth plate?
J. Kenwright and S. Apte
Physeal distraction is used for limb
lengthening or for correction of long bone
deformities in the skeletally immature patient,
but there is considerable concern that the
procedure may compromise growth potential
of the distracted physis. The majority of
clinical and experimental investigations have
confirmed the first experimental observation
made by Ring (1958), that distraction across
the physis leads to rupture through the
hypertrophic zone, and limb lengthening
can be achieved by distraction of the fracture
grap (llizarov and Soybelman, 1969; Monticelli
and Spinelli, 1981 a, 1981 b). High force
levels have been recorded in patients before
such fracture occurs (Crawford et al, 1988;
Kenwright et al, 1990). Most evidence suggests
that growth may be inhibited either partially
or completely following this procedure (Hert,
1969; Fishbane and Riley, 1978; Monticelli
and Spinelli, 198la; Connolly et al, 1986),
although it has been shown in an animal
model that if lower force levels or slower
rates of distraction are applied then the risk
of damage to subsequent longitudinal growth
can be reduced (de Pablos et al, 1986). Other
experimental studies have suggested that the
use of low magnitude forces or slow rates
of physeal distraction increases the length
of the bone with hyperplasia of the growth
plate but without fracture (De Bastiani et
70 Reprinted with permission of Mapfre Medicina (vol. 4, suppl 2)
al, 1986; Wilson-MacDonald et al, 1990). De
Bastiani et al (1986) term this overgrowth
without fracture chondrodiatasis and claim
it is not associated with disturbed growth
plate function. Slege and Noble (1978) also
showed that thickening of the growth plate
following slow rates of distraction with a
constant force led to an increase in bone length
with or without associated fracture: increased
overall cellular activity in the growth plate
was seen. Recently, Elmer et al (1993), using
a rabbit model for chondrodiatasis, found no
evidence of altered growth plate activity and
concluded that the growth plate is stretched
passively. Mechanical studies have shown
that short periods of distraction alter the
mechanical properties of the growth plate
so that less force is subsequently required to
cause growth plate fracture (Noble et al, 1982;
Kenwright et al, 1990). There is, however,
still controversy about the effect than even
slowly progressive distraction regimes will
have upon cellular activity of the physis,
both during and following completion of
the procedure.
The production of new chondrocytes in
the proliferative zone of the growth plate is
the fundamental mechanism of longitudinal
bone growth (Kember, 1983). In addition to
the direct contribution made by cell division
to longitudinal bone growth, cell proliferation
 Physeal distraction: Review of experimental evidence. What is the response of the cells on the growth plate?
also contributes to two additional mechanisms
of growth, i.e. cell hypertrophy and matrix
production, by supplying new cells which
will then enlarge and make new matrix. Cell
proliferation is also important in fracture
repair. The proliferation of precursor cells at the
site of injury is one of the earliest components
of fracture repair and produces a mass of
reparative tissue that will later differentiate
into cartilage and bone.
Although the analysis of cell proliferation
is thus of primary importance, it has, until
recently, been limited by the techniques
available. Traditionally, in situ studies
of cell proliferation have used mitotic, or
autoradiographic approaches (reviewed
in Kember, 1983). We have investigated
the effects of physeal distraction on cell
proliferation in the growth plate using a
novel immunohistochemical approach. The
thymidine analogue bromodeoxyuridine
(BUDR) is incorporated by cells in the
S-phase of the cell cycle, i.e. in DNA synthesis
phase and the number and distribution of
BUDR labelled cells is representative of
the proliferating cell population (Gratzner,
1982). The incorporation of BUDR into
newly synthesized DNA can be localized
immunohistochemically using monoclonal
antibodies (Gratzner, 1982; Magaud et al,
1989). The BUDR method has been found
to be a valid method of detecting S-phase
cells in decalcified paraffin-embedded (Apte,
1990) and undecalcified plastic-embedded
sections of skeletal tissues (Apte and Puddle,
1990). In effect, this method provides the
same data as provided by tritiated thymidine
autoradiography, but is a more rapid and
radiation-free approach. Furthermore, high
magnification and grain-counting (Elmer et al,
1992) is not required to visualise labelled cells,
so that a «bird’s-eye» view of cell proliferation
in relation to tissue architecture is obtained.
The present study demonstrates the application
of this technique in orthopaedic research.
In this investigation we have studied
the changes in the growth plate following
continuous distraction leading to bone
lengthening; a force level was used which
in previous studies (Sledge and Noble,
1978; Kenwright et al, 1990) had led to plate
hypertrophy either with or without fracture. It
is hypothesised that such distraction regimes
might have an effect upon cell production
n in the proliferating zone and subsequent
ossification of the hypertrophic zone of the
physis. We have also studied cell proliferation
in the metaphyseal fracture zone to establish
the underlying basis for the rapid healing
seen here.
RESULTS AND DISCUSSION
A maintained axial tension of 20 Newtons,
approximately equivalent to body weight
(Masound et al, 1986), applied across the
upper tibia growth plate in young rabbits
has fed to a Salter-Harris type 1 fracture
after approximately 4-5 days as assessed
by histology although the exact moment of
fracture was not defined mechanically. In
most instances fracture occurred at the growth
plate-metaphyseal junction suggesting that
the interface between cartilage and bone is a
weak link; this is also evident in the periphery
where cartilage is torn away from subperiosteal
and perichondrial bone, but the perichondrial
ring and periosteum remain intact.
Our histological findings share many
common features with those of previous
investigators. We noted an irregular increase in
thickness of the growth plate in all specimens
subjected to distraction, this being most
marked in the central region of the plate. Such
thickening has been described before under
conditions of low force or low rate distraction
sometimes with fracture and at others without
(Sledge and Noble, 1978; Peltonen et al, 1988;
Spriggins et al, 1989; de Pablos and Cañadell,
1990; Wilson MacDonald, 1990). We find that
71
J. Kenwright, S. Apte
this increase in growth pie thickness is due
to an increase in the hypertrophic zone. In
contrast, Sledge and Noble (1978, and De
Bastiani et al (1986) attributed the increased
growth plate thickness to increases in both
the proliferative and hypertrophic zones. We
believe that the most probable cause of the
accumulation of hypertrophic chondrocytes
was the induction of metaphyseal ischaemia.
Trueta and Amato (1960) studied the effect of
occlusion of various sources of blood supply
around the growth plate and showed that
occlusion of metaphyseal vessels resulted in
the accumulation of hypertrophic chondrocytes
in a pattern very similar to that seen in the
distracted growth plates in our study. A
recent study has shown that interruption of
metaphyseal blood flow results not only in a
lack of calcium in hypertrophic chondrocytes,
but also in inhibition of cartilage resorption
(Noguchi et al, 1993). Similar to Elmer et al
(1992), we also occasionally noted necrosis
within the growth plate. After 10 days of
distraction, islands of hypertrophic chon-
drocytes were observed within the metaphysis,
a phenomenon also described by Alberty et
al (1990).
The present study shows that the increased
thickness of growth plate cartilage following
distraction in our model is not a consequence of
increased cell proliferation in the proliferating
zone. On the contrary, cell division within
this layer was reduced if distraction was
maintained for 10 days. At the same time, there
was no evidence of anomalous cell proliferation
in the hypertrophic zone or reserve zone of
the growth plate. Normally, in the reserve
zone, chondrocytes divide very occasionally,
whereas cell proliferation does not normally
occur in the hypeprtrophic zone (Kember,
1983). Since fracture occurred at around 4-5
days and there was no significant increase in
length in group B animals, we conclude that
the significant increase in tibia length in group
C was due to distraction of the fracture gap.
72
Attachment of the external fixation pins
and frame alone without the application of
tensile force (group A) did not cause detectable
abnormalities; thus the changes which were
observed in the other two groups must have
been caused in part or completely by the
application of the axial tension. Since the blood
supply to the proliferative zone chondrocytes
is provided by loops of epiphyseal arteries
(Trueta and Morgan, 1960; Brookes, 1971) it
is possible that the occasional necrosis and
absence of cell proliferation in the proliferative
zone was the result of epiphyseal ischaemia.
In the present studies the periosteum did
not rupture and high levels of tension must
have acted at the junction of the periosteum
to the perichondrial ring. We hypothesize
that stretching of the periosteum through
which the avascular supply must pass may
account for ischemia at both the metaphyseal
and epiphyseal ends.
The results of this study show that the
histological picture of increased cellularity of
the growth plate associated with distraction
at the force levels described here was not
accompanied by increased cell proliferation but
by delayed mineralisation of hypertrophic cells
(although this has not been directly shown in
this study) so that thypertrophic chondrocytes
accumulated. The increase in bone length,
which was seen in group C but not in group
B, is probably due to distraction of the fracture
gap.
The complete absence of cycling cells in
some instances and necrotic disordered areas
of the proliferative zone in others, suggests that
the distraction procedure under the mechanical
conditions of the present experiment was
deleterious to the growth plate. The ultimate
influence on total growth has not been shown
in this present study. If the force levels used
in the present study are extrapolated to the
human situation they are seen to be very close
to, or to be lower than those used for the most
gradual clinical distraction of the physis used
 Physeal distraction: Review of experimental evidence. What is the response of the cells on the growth plate?
therapeutically in patients (Kenwright et al,
1990) and that similar abnormalities might
be seen in growth plate function. The results
would seem to corroborate the statements of
previous authors, who have cautioned against
the use of excessive force during distraction or
against using distraction in skeletally immature
patients, where loss of future growth from
a distracted physis will lead to significant
loss of leg length (Fishbane and Riley, 1978;
Monticelli and Spinelli, 1981; Cañadell and
de Pablos, 1985)
REFERENCES
1. Alberty A, Peltonen J, Ritsila V. Distraction
effects on the physis in rabbits. Acta Orthop Scan
1990;61:258-262.
2. Amamilo SC, Bader DL, Houghton GR. The
periosteum in growth plate failure. Clin Orthop
1982;194:293-305.
3. Apte SS. Validation of bromodeoxyuridine
immunohistochemistry for localization of Sphase
cells in decalcified tissue. A comparative study with
tritiated thymidine autoradiography. Histochem
1990;J,22:401-408.
4. Apte SS, Puddle BP. Bromodeoxyuridine (BrdUrd)
immunohistochemistry in undecalcified plastic-
embedded tissue. Elimination of the DNA
denaturation step. Histochemistry 1990;93:631-635.
5. Brookes M. The blood supply of bone. An approach
to bone biology. London: Butterworths, 1971
6. Cañadell J, De Pablos J. Breaking bony bridges by
physeal distraction: A new approach. Int Orthop
1985;9:223-229.
7. Connolly JF, Huurman WW, Lippiello L, Pankaj
R. Epiphyseal traction to correct acquired growth
deformities. An animal and clinical investigation.
Clin Orthop 1986;202:258-268.
8. Crawford EJP, Jones CB, Dewar ME, Aichroth
PM. Distraction forces in children undergoing
leg lengthening. Orthop Trans 1987;11:302.
9. De Bastiani G, Aldeghiri R, Renzi Brivio L, Trivela.
Limb lengthening by distraction of the epiphyseal
plate. A comparison of two techniques in the rabbit.
J Bone Joint Surg 1986ª;68-B:545-549.
10. De Bastiani G, Aldeghiri R, Renzi Brivio L, Trivella
G. Chondrodiatasis-controlled symmetrical
distraction of the epiphyseal plate. J Bone Joint
Surg 1986b;68B:550-556.
11. De Pablos J, Villas C, Cañadell J. Bone lengthening
by physeal distraction: An experimental study.
Int Orthop 1986;10:163-170.
12. De Pablos J, Cañadell J. Experimental physeal in
immature sheep. Clin Orthop 1990;250:73-80.
13. Drury RAB, Wallington EA. Carleton’s Histological
Technique. Oxford: Oxford University Press, 1980;
5th ed.
14. Elmer EB, Ehrlich MG, Zaleske DJ, Polsy C, Mankin
HJ. Chondrodiatasis in rabbits: A study of the
effect of transphyseal bone lengthening on cell
division, synthetic function, and microcirculation
in the growth plate. J Pediatr Orthop 1992;12:181-
190.
15. Fishbane BM, Riley LH. Continuous transphyseal
traction: Experimental observations. Clin Orthop
Related Res 1978;136:120-124.
16. Gratzner HG. Monoclonal antibody to 5-bromo
and 5-iododeoxyuridine: A new reagent for
detection of DNA replication. Science 1982;218:474-
475.
17. Ilizarov GA, Soibelmann LM. Some clinical
and experimental data concerning bloodless
lengthening of the lower extremities. Eksper Khiv
Anesthiol 1969;4:27-32.
18. Kember NF. The cell kinetics of cartilage. In:
Hall B K (ed). Cartilage. Structure, Function &
Biochemistry. New York, San Francisco, London:
Academic Press, 1983; 5th ed., 149-180.
19. Kenwright J, Spriggins AJ, Cunningham JL.
Response of the growth plate to distraction close
to skeletal maturity. Is fracture necessary? Clin
Orthop 1990;250:61-72.
73
J. Kenwright, S. Apte

20. Magaud JP, Sargent I, Clarke PJ, Ffrench M, Rimokh
R, Mason DY. Double immunocytochemical
labelling of cell and tissue samples with
monoclonal antibromodeoxyuridine. J Histochem
Cytochem 1989;37:1517-1527.
the metaphyseal blood supply of the growth plate
inhibits accumulation of calcium in proliferatibe
chondrocytes. An ultrastructural study. Proc. 31st
Annual Meeting of the orthopaedic Research
Society, 1993.

21. Masoud I, Shapiro F, Kent R, Moses A. A 27. Peltonen J, Kahri A, Karaharju E, Alitalo I.
longitudinal study of the growth of the New Regeneration after physeal distraction of the
Zealand white rabbit: Cumulative and biweekly radius in sheep. Acta Orthop Scand 1988;59:675-
incremental growth rates for body length, body 680.
weight, femoral length, and tibia length. J Orthop
28. Ring PA. Experimental bone lengthening by
Res 1986b;4:221-231.
epiphysial distraction. Br J Surg 1958;46:169-173.
22. Monticelli G, Spinelli R. Distraction epiphyusiolysis
29. Sledge CB, Noble J. Experimental limb lengthening
as a method of limb lengthening. I. Experimental
by epiphyseal distraction. Clin Orthop 1978;136:111-
study. Clin Orthop 1981ª;154:254-261.
119.
23. Monticelli G, Spinelli R. Distraction epiphysiolysis
30. Steen H, Fjeld TO, Ronningen H, Langeland N,
as a method of limb lengthening. III. Clinical
Gjerdet NR, Bjerkreim I. Limb lengthening by
applications. Clin Orthop Rel Res 1981b;154:254-
epiphyseal distraction. An experimental study
261.
in the caprine femur. J Orthop Res 1987;5:592-599.
24. Monticelli G, Spinelli R, Bonucci E. Distraction
31. Trueta J, Amato VP. The vascular contribution to
epiphysiolysis as a method of limb lengthening.
osteogenesis. III. Changes in the growth cartilage
II. Morphologic investigation. Clin Orthop
caused by experimentally induced ischaemia. J
1981;154:262-273.
Bone Joint Surg 1960;42-B:571-587.
25. Noble J, Diamond R, Stirrat CR, Sledge CB.
32. Wilson-MacDonald J, Houghton GR, Bradley J,
Breaking force of the rabbit growth plate and its
Morcscher E. The relationship between periosteal
application to epiphyseal distraction. Acta Orthop
division and compression or distraction of the
Scand 1982;53:13-16.
growth plate. An experimental study in the rabbit.
26. Noguchi Y, Yamaguchi T, Sugioka Y. Interruption of J Bone Joint Surg 1990;72-B:303-308.

74
10 Biology of bone lengthening by means of
physeal distraction
J. de Pablos
In this chapter we will take as reference an
experimental study made in the Department
of Orthopedic Surgery at the University of
Navarra(2) which had the following three basic
objectives:
- To identify the basic mechanism of
lengthening in physeal distraction.
- To study the histology of the reconstruction
of the lengthened segment.
- To evaluate the viability of the growth
cartilage following physeal distraction.
The experiment was carried out on 45
two-month-old lambs on which distal femoral
physeal distraction was performed by using
the experimental prototype of the Dynamic
Axial Fixator designed at the University
of Verona. The experiment was conducted
with the apparatus permanently working in
a rigid mode. Two screws were placed in the
distal epiphysis and another two in the upper
third of the diaphysis of the animal forming
two perpendicular planes. All operations
were performed in the left femur while the
right femur was used as a control. Physeal
distraction was begun 36 hours following
the placing of the apparatus and was carried
out twice a day until a 2 cm. lengthening was
obtained in all cases. Just after distraction,
the apparatus was blocked until its removal
45 days later. The lambs were divided into 3
groups, and each group into 3 sub-groups,
Reprinted with permission of Mapfre Medicina (vol. 4, suppl 2)
Research conducted at the Department of Orthopaedics of the University of Navarra Medical School
according to the speed of distraction employed
(2 mm/day, 1 mm/day and 0.5 mm/day)
and the timing of sacrifice (at the end of
lengthening, 1.5 months after lengthening
and 4 months postoperatively).
The evaluation of results was made on the
basis of the following studies: radiological
study, measurement of the specimens, and
histological study using hematoxyline-eosine
and Masson trichromic stains.
With respect to the first objective,
results were conclusive: lengthening, in
our experiments was begun constantly and
independently of the distraction rate employed
with a physeal fracture (epiphysiolysis) (Fig.
1). This observation is in agreement with the
majority of authors who have writen on this
matter(3-8,10,11,13,14,18,21-23). In our experiment,
this fracture was always located between the
hypertrophic and calcified layers of the growth
cartilage, which is reminiscent of a type I
traumatic epiphysiolysis of Salter and Harris(19)
and which had also been observed by other aut
hors(3,4,7,11,13,14,18,22,23) (Figs. 2, 3). We were never
able to discover signs that the lengthening by
means of physeal distraction was brought about
by a stimulus on physeal activity, or by plastic
deformity of the physis (as chewing gum) as
suggested by some authors(1,15,16,20). Kenwright
and Spriggins(9) in their experimental work
on rabbit tibias, conclude that it is possible
75
J. de Pablos
A B
Figure 1. Roentgenographic study of the lengthening focus in different postoperative stages. A) 10 days,
B) 2 months, C) 4 months.
A B
to perform bone lengthening by means of
physeal distraction without producing a
physeal fracture. However, in order to achieve
this objective the distraction must necessarily
be of such limited quantity (applied force and
rate) that the lengthening obtained is really
null as regards practical effects.
As a result, we feel that such terms as
“chondrodiastasis”(1) (physeal distraction
76
C
Figure 2. Panoramic histology.
Physeal fracture just after
distraction (10 days postop.).
A) Distraction rate: 2 mm/day.
B) Distraction rate: 0.5 mm/day.
without epiphysiolysis) does not really explain
what occurs and should thus be revised. Nor
do we agree with Paley’s(17) division of this
technique in physeal distraction by means of
epiphysiolysis, whether acute or sub-acute and
physeal distraction without epiphysiolysis. In
the first place because, in physeal distraction,
there always apppears to be epiphysiolysis
and secondly because epiphysiolysis is
 Biology of bone lengthening by means of physeal distraction

A B

Figure 3. Microscopic histology.

Masson’s trichromic. Physeal
fracture just after distraction at
rate of 2 mm/day. A) Epiphyseal
slope (x 40). B) Metaphyseal
slope (x 100).

A B C

Figure 4. The three main stages in the reconstruction of the lengthened segment. Masson’s trichromic.
A) Physeal fracture-hematoma (x 40). B) Fibrous tissue (x 40). C) Intramembranous ossification (x 100).

either controlled (rigid distraction) instead
of subacute, or brusque (elastic distraction)
rather than acute.
Histologically, the reconstruction of the
lengthened segment in physeal distraction
follows three stages which, as we mentioned
in describing other techniques, are well
differentiated even though they may overlap
from one stage to another. Firstly, the physeal
fracture already described gives place to a
hematoma which appears quickly and in
approximately 3 weeks is substituted by a
fibrous tissue quite rich in blood vessels,
mesenquimal cells and collagen fibers, with
significant repair potential. These fibers are
parallel to each other and are arranged in the
direction of traction. Once the fibrous tissue
substitutes the hematoma, it begins to ossify
at the ends and in the periphery as well. The
type of ossification observed there is a direct

77
J. de Pablos
A B
Figure 5. Viability of the growth plate after physeal distraction. C: Control side. E: Lengthened side.
Masson’s trichromic (x 100). A) Distraction rate: 2 mm/day. B) Distraction rate: 0.5 mm/day.
one which goes from fibrous tissue to bone
tissue with no intermediate cartilaginous
cells. This process is more reminiscent of
“desmal” ossification than “endochondral”
ossification (Fig. 4). The reconstruction of the
lengthened segment in experimental physeal
distraction, has always been “ad integrum” in
animals studied 4 months after distraction was
begun. This phenomenon was also observed
by Monticelli et al(11). We also agree with
these authors regarding reconstruction it was
more rapid and better remodelled in femurs
lengthened at a lower rate.
In regard to the the third objective, the
results obtained in our work show that the
viability of growth cartilage after distraction
is inversely related to the distraction rate
employed and in direct relation to the
brusqueness of the initial physeal fracture.
Thus, if circular fixator-distractors or other
elastic apparatuses are used, irreversible
physeal damage can be produced owing
to the brusqueness of the initial fracture,
though later the distraction speed stays within
adequate limits(7,11,12). The distraction rate
which we have found to cause less physeal
damage to the distal femoral physis of the
lamb has been 0.5 (2 x 0.25) mm/day. This
is an observation which coincides with that
78
of De Bastiani et al in their experiences with
rabbits(1). Nevertheless, at a rate of 2 (1 x
2) mm/day we have constantly observed
irreversible physeal damage (Figs. 5, 6).
These findings show that in clinical work an
adequate lengthening rate for children under 10
years of age is 0.5 mm/day and at this rate little
physeal damage is likely to occur (provided
the physis was normal before distraction). If
after a low speed physeal distraction there
is no closure of the physis, the possibility of
using this technique with immature patients
and repeating the experiment in later stages
of growth, if indicated, is feasible.
Although we have observed this on several
occasions in our clinical practice and the fact
we have repeated physeal distraction to two
patients in a minimal interval of two years
(Fig. 7), there is nevertheless the need to be
cautious when extrapolate results obtained
from animals to human patients. We say this
because, on the one hand, the behaviour of
the animal physis is undoubtedly different
from that of the human being and on the other
hand, because the experiment in question
was performed on normal physes whereas
in most cases in which physeal distraction is
used on humans, it is performed on previously
damaged physes.
 Biology of bone lengthening by means of physeal distraction

2.0

1.5
Discrepancy (cm)

0.5 mm/day
1.0
1 mm/day
2 mm/day
0.5

0 30 60 90 120
Figure 6. The average discrepancy
Days between lengthening and
contralateral limbs.

A B

Figure 7. Growth plate still open

23 months after a lengthening by
physeal distraction performed at
a rate of 0.5 mm/day. A) 1 month
postop., B) 23 months postop.

ACKNOWLEDGEMENTS 2. De Pablos J, Cañadell J: Experimental Physeal

The author wish to thank Prof. J. Cañadell
and Prof. C. Villas, mentors of this project,
and Prof. G. de Bastiani, Prof. R. Aldegheri
and Dr. L. Renzi-Brivio, from the University
of Verona, for their continuous support in
this experimental project.
REFERENCES
1. De Bastiani G, Aldegheri R, Renzi-Brivio L, Trivella
G: Limb lengthening by distraction of the epi-
physeal plate. A comparison of two techniques
in the rabbit. J Bone Joint Surg 1986;68-B:545-
9 par elongation du cartilage de croissance tibial
Distraction in Immature Sheep. Clin Orthop
1989;250:73-80
3. Fishbane BM, Riley LH: Continuous transphyseal
traction. A simple method of bone lengthening.
Johns Hopkins Med J 1976;13
4. Fishbane BM, Riley LH: Continuous transphyseal
traction: experimental observation. Clin Orthop
1978;136:120-4
5. Fjeld TO, Steen H: Limb lengthening by low rate
epiphyseal distraction: An experimental study in
the caprine tibia. J Orthop Res (en prensa).
6. Houghton GR, Duriez J: Allongement tibial

79
J. de Pablos
superieur. Etude experimentale chez le lapin. Rev
Chir Orthop 1980;66:351-6
7. Ilizarov GA, Soybelman LM: Some clinical and
experimental data on the bloodless lengthening
of the lower limbs. Exp Khir Anest 1969;4:27-32
8. Jani L: Tierexperimentelle Studie uber
Tibiaverlangerung durch Distraktionepiphysiolyse
Z Orthop 1973;111:627-30
9. Kenwright J, Spriggins T: Effects of distraction
on the growth plate of the tibia. An experimental
study. Abstracts Book of Recent advances of
external fixation. Riva de Garda. September 1986.
p 166
10. Letts RM, Meadows L: Epiphysiolysis as a method
of limb lengthening. Clin Orthop 1978;133:230-45
11. Monticelli G, Spinelli R, Bonucci E: Distraction
epiphysiolysis as a method of limb lengthening.
II Morphologic investigations. Clin Orthop
1981;154:262-73
12. Monticelli G, Spinelli R: Distraction epiphysiolysis
as a method of limb lengthening I. Experimental
Study. Clin Orthop 1981;154:256-61
13. Monticelli G, Spinelli R: Distraction epiphysiolysis
as a method of limb lengthening. III Clinical
applications. Clin Orthop 1981;154:274-85
14. Monticelli G, Spinelli R: Limb lengthening by
epiphyseal distraction. Int Orthop 1981;5:85-
90
80
15. Noble J, Diamond R, Stirratt CR, Sledge CB:
Breaking force of the rabbit growth plate and its
application to epiphyseal distraction. Acta Orthop
Scand 1982;53:13-6
16. Noble J, Sledge CB, Walker PS, Diamond R, Stirratt
CR, Sosman JL: Limb lengthening by epiphyseal
distraction. J Bone Joint Surg 1978;60-B:139-40
17. Paley D: Current techniques of limb lengthening.
J Pediatr Orthop 1988;8:73-92
18. Ring PA: Experimental bone-lengthening by
epiphyseal distraction Br J Surg 1958;49:169-73
19. Salter RB, Harris WR: Injuries to the growth plate.
I9n “The growth plate and its disorders”. Mercer
Rang. Ed Williams and Wilkins, Baltimore. 1969,
p 133
20. Sledge CB, Noble J: Experimental limb lengthening
by epiphyseal distraction. Clin Orthop 1978;136:111-
9
21. Steen H, Fjeld TO, Ronningen H, Langeland N,
Gjerdet NR, Bjerkreim I: Limb lengthening by
epiphyseal distraction. An experimental study
in the caprine femur. J Orthop Res 1987;5:592-9
22. Zavijalov PV, Plaskin JT: Distraction epiphysiolysis
in lengthening of the lower extremity in children.
Khirurgija 1968;44:121-37
23. Zavijalov PV, Plaskin JT: Elongation of crural
bones in children using a method of distraction
epiphysiolysis. Vestn Khir Grekova 1967;103:67-82
11 The experimental basis of treating
premature partial closure of a growth
plate by bone bridge resection and
interposition of adipose tissue
A. Langenskiöld
Until 1965 it was generally believed that a
deformity which follows growth disturbance
from a growth plate injury progresses until
the end of me child’s growing period. As a
result of experimental and clinical studies
started in 1947 we found in 1965 that the
cessation of growth and development of
angular deformity after partial growth plate
closure can be eliminated by operation.
Inspired by observations in a case of
Ollier’s disease Langenskiöld and Edgren
(1950) studied the effect of localized X-ray
injury of parts of growth plates in young
rabbits. They found that the presence of
injured or dead portions of cartilage in a
growth plate prevented the formation of
epiphyseo-metaphyseal bone bridges.
The injured portion of the growth plate
regenerated from adjacent parts of the plate.
The same finding was made by Heikel (1960)
after free transplantation of heads of the fibula
in rabbits aged 10-21 days. The observation of
a case in which a definite bone bridge causing
deformity in the distal end of the femur
disappeared after supracondylar osteotomy
changed our pessimistic attitude as far as such
bone bridges are concerned (Langenskiöld,
1967). On the basis of the experimental results
mentioned above and the german Lexer’s
work on the effect of free fat transplants
on scar prevention (Lexer, 1924) the first
Reprinted with permission of Mapfre Medicina (vol. 4, suppl 2)
operation of an epiphyseo-metaphyseal bone
bridge was performed in the upper end of
the tibia in 1965 (Langenskiöld, 1967). The
operation resulted in the correction of 10
degrees of recurvatum deformity. It must be
emphasized that the planning of the operation
was based on pure basic research which was
carried out without any clinical goals.
The new method was not used in further
cases before 1968 when Österman in his
work for the doctor’s degree (Österman,
1972) had shown the effect of the operation
in experiments on 178 rabbits. He provoked
bone bridges in the lateral periphery of the
distal femoral growth plate. When a valgus
deformity had appeared the bridge was
resected and replaced with a transplant of
autologous fat tissue, a piece of cartilage from
a pig or with bone wax.
The benefit of an interposion material
was clearly demonstrated. Deformities
were corrected by growth and defects in
the growth plates were regenerated. In 1975
twelve patients had been operated on, two of
the cases were reported in detail and a first
description of the operative technique was
given (Langenskiöld, 1975). It was stated that
despite a firm experimental basis for the use of
the operation in cases with a small peripheral
bone bridge, several matters were still under
consideration.
81
A. Langenskiöld
It was not yet clear how large a bridge
may be resected with an acceptable result.
Österman continued the rabbit experiments. A
bone cylinder including about two thirds of the
distal growth plate of the femur was removed
from the central part and replaced with an
autologous fat transplant (Langenskiöld and
Österman, 1979). Four weeks later almost
complete regeneration of the growth plate
was seen. In the same article 33 cases of bridge
resection in children were reported. Clinical
experience had now shown that the operation
is indicated when a large bridge situated in
the middle of a plate is concerned. The use
of free transplants got additional support
from the finding that fat grafts implanted
on the spinal dura remain there as fat tissue
(Langenskiöld and Kiviluoto, 1976).
However, the actual fate of the implanted
fat in human bones was not clear, especially
when the metaphyseal cavities were enlarged
and elongated with growth (Langenskiöld
1981). The fate of free fat grafts implanted
in children could not be studied in rabbits
because of the small amount of spongy
bone in the metaphyses. An answer to the
question “what happens to the fat” had to
be searched for in a bigger animal. In young
pigs round cavities were made in the region
of the growth plate in the proximal end of
the tibia including parts of the metaphysis
and the epiphysis (Langenskiöld et al. 1986).
These cavities elongated in a manner similar
to those seen in clinical cases and histological
section showed them to be filled by living
adipose tissue after several months. The
volume of this tissue had continuously
increased in parallel with the growth in
length of the bone. The number of the fat
vacuoles in the transplants increased and this
favours the assumption that the enlargement
resulted from multiplication of cells of the
revascularized adipose tissue.
As regeneration of growth plates in
experiments has not been reported from other
82
laboratories outside Finand a summary of
the 5 different series in which regeneration
appeared was published in 1989 (Langenskiöd
et al. 1989).
Clinical trials in humans without an
experimental basis is today to a large extent
outmoded and indefensible. We have tried as
far as possible to test in animal experiments our
method of treating premature partial closure
in children.
REFERENCES
- Heikel HVAH. Experimental epiphyseal
transplantation. Part II. Acta Orthop Scand 1960;30:1.
- Langenskiöld A. The possibilities of eliminating
premature partial closure of an epiphyseal plate
caused by trauma or disease. Acta Orthop Scand
1967;38:267.
- Langenskiöld A. An operation for partial
closure of an epiphyseal plate in children,
and its experimental basis. J Bone & Joint Surg
1975;57B:325.
- Langenskiöld A. Surgicai treatment of partial
closure of the growth plate. J Pediatr Orthop
1981;1:3.
- Langenskiöld A, Edgren W. Imitation of
chondrodysplasia by localized roentgen ray
injury - an experimental study of bone growth.
Acta Chir Scand 1950;99:353.
- Langenskiöld A, Kiviluoto O. Prevention of
epidural scar formation after operations on the
lumbar spine by means of free fat transplants.
Clin Orthop 1976;115:92.
- Langenskiöld A, Österman K. Surgical treatment
of partial closure of the epiphyseal plate.
Reconstruction Surgery and Traumatology 1979;17:48.
- Langenskiöld A, Videman T, Nevalainen T. The
fate of fat transplants in operations for partial
closure of the growth plate. J Bone & Joint Surg
1986;68B:234.
- Langenskiöld A, Heikel HVAH, Nevalainen T,
Österman K, Videman T. Regeneration of the
growth plate. Acta Anat 1989;134:113.
 The experimental basis of treating premature partial physeal closure by means of resection-interposition

- Lexer E. Die freien Transplantationen. 1 Teil. - Österman K. Operative elimination of partial

Stuttgart: Verlag von F. Enke, 1924. premature epiphyseal closure. Acta Orthop Scand
1972; 147. Munksgaard, Copenhagen.

83
12
Regeneration of the growth plate
K. Österman
Regeneration pattern of the growth
plate cannot be easily understood without
understanding the interstitial growth in width
of the growth plate. Significant injuries of the
growth plate usually lead to a bony connection
between the epiphysis and the metaphysis. Bone
formation may be a result of the damage and
dislocation of the physeal region and the bridge
formation is a rea lilt of an anatomical change
between the bone fragments on both sides of
the plate. The bone bridge may also be a result
of a compression injury or vascular damage to
the plate region which leads to a deterioration
of the cartilage and late bone bridge formation.
In both conditions the bone bridge when once
established, is able to prevent the normal
growth and leads to a progressive deformity.
The bony connection causes degeneration of
the growth cartilage by preventing the growth
in length. The mechanism is very similar to
what can be seen when the growth of the bone
is prevented with staples.
Degeneration of the growth plate associated
with bone bridging is so strong and dominating
a process that it easily prevents us from seeing
the regeneration of the growth cartilage.
Regeneration must therefore be studied
under specific conditions. In an extensive
study we have presented observations on the
regeneration of the plate in conditions where
the bone bridge formation is prevented either
84 Reprinted with permission of Mapfre Medicina (vol. 4, suppl 2)
by using specific experimental technique or
surgically (Langenskiöld et al., 1989).
Based on observations on the growth
of foci in dyschondroplasia Langenskiöld
and Edgren 1950 created a localized X-ray
irradiation injury in the epiphyseal cartilage.
They observed that the noninjured parts of
the growth cartilage were able to continue
growth and the regeneration of the plate took
over so that the injured part of the cartilage
was left behind in the metaphysis.
A similar phenomenon was observed
by Heikel 1960 after free transplantation
of the head of the growing fibula. In these
experiments a central necrosis of the growth
cartilage was seen but regeneration of the plate
took place from the adjacent living peripheral
part of the growth plate.
The removal of the physeal bone bridge
developed after an injury to the growth plate
and the prevention of its reappearance using
fat tissue transplants presents a new model
to study the growth plate regeneration. In
a series of 178 rabbits where a bone bridge
was provoked and a growth disturbance
was observed the bone bridge was removed
surgically and its reappearance was prevented
by using a free fat graft. In these experiments
the bone growth was restored and regeneration
of the plate was observed either partially or
totally (Österman, 1972).

In recent series Österman (1993) has shown
that regeneration of the growth cartilage is
seen even in cases where more than 50 per cent
of the volume of the plate has been removed
if the bridge formation can be prevented by
fat grafting.
The regeneration of the growth plate is
seen also in clinical conditions. A similar
development which is seen in connection
with Ollier’s disease is also seen when the
bone bridge has been removed surgically when
the growth and the development of the bone
defect has been followed up radiologically
(Langenskiöld and Österman, 1979).
Partial or almost total regeneration of the
plate can be explained easily if the concept
of interstitial latitudinal growth is accepted.
Especially in cases where the peripheral
part of the plate and the Ranvier area has
been removed surgically it is impossible to
explain the process by apposition growth.
On the other hand , in experiments where
the defect is situated in the central part of
the plate regeneration mechanism by lateral
apposition is also difficult to explain.
In conclusion, regeneration of the growth
cartilage can be seen in certain conditions,
Regeneration of the growth plate
regeneration mechanism seems to be associated
with the interstitial growth in width and
regeneration of the cartilage seems to explain
growth pattern in certain clinical conditions.
REFERENCES
- Heikel H V A. Experimental epiphyseal
transplantation. Part II: Histological observations.
Acta Orthop Scand 1960;30:1
- Langenskiöld A, Edgren W. Imitaion of
dyschondroplasia by localized roentgen ray
injury-an experimental study on bone growth.
Acta Chir Scand 1950;99:353
- Langenskiöld A, Heikel HVA, Nevalainen T,
Österman K, Videman T. Regeneration of the
growth plate. Acta Anat 1989;134:113
- Langenskiöld A, Österman K. Surgical treatment
of partial closure of the epiphyseal plate. Reconstr
Surg Traumatol 1979;17:48
- Österman K. Operative elimination of partial
premature epiphyseal closure. An experimental
study. Acta Orthop Scand 1972; suppl 147.
- Österman K. Healing of large surgical defects of
the epiphyseal plate. Clin Orthop 1993 (in press).
85
13 Management of partial growth arrest.
Physis, fat or silastic?
E.H. Lee, G.X. Gao and K. Bose

Correction of angular deformity as a result Group I: Creation of partial growth arrest

of partial growth arrest in always a challenging
problem. In the older child stapling or
epiphysiodesis of the physis on the convex
side of the deformity, or an osteotomy can be
performed to correct the angular deformity.
In the younger child, excision of the bony bar
(epiphysiolysis) and inserting fat, silastic, bone
wax or bone cement as interposition material
have met with varying degrees of success.
Recent experimental studies have advocated
the use of free physeal grafts. The aim of
this study was to compare the usefulness
of the physeal graft to fat and silastic in the
treatment of established growth arrest in a
rabbit model.
Four to six weeks old New Zealand white
rabbits were used. Four groups of experiments
were performed:
by excising the medial half of the proximal
tibial epiphyseal plate (12 rabbits).
Group II: Creation of partial growth arrest
as above. Three weeks later the bony bridge
was excised and a graft from the iliac apophysis
transferred into the defect (10 rabbits).
Group III: Creation of partial growth arrest
as in 1. Three weeks later, the bony bridge
was excised and fat was transferred into the
defect (10 rabbits).
Group IV: Creation of partial growth arrest
as in 1. Three weeks later, the bony bridge
was excised and silastic was transferred into
the defect (10 rabbits).
All these animals were allowed to move
freely in their cages without any form
of immobilisation to their legs. Clinical,
radiological and histological data were

Table 1. Group I: Excision of proximal half of tibial physis

Difference in medial/ Difference in length of

Time post-op Tibiofemoral angle lateral height of tibia operated and unoperated tibia
(week) (varus) (cm) (cm)
2 27.5° 0.75 0.2
4 32.5° 0.9 0.3
6 30° 0.75 0.6
8 27.5° 0.65 0.7
12 27.5° 0.6 0.6
16 43.5° 1.7 0.85

86 Reprinted with permission of Mapfre Medicina (vol. 4, suppl 2)

 Management of partial growth arrest. Physis, fat or silastic?

Table 2. Group II: Iliac apophyseal transfer

Difference in medial/ Difference in length of

Time post-op Tibiofemoral angle lateral height of tibia operated and unoperated tibia
(week) (varus) (cm) (cm)
2 2.5° 0.1 0.15
4 33° 0.45 0.35
6 27° 0.35 0.6
8 17.5° 0.3 0.2
12 21° 0.5 0.45

Table 3. Group III: Fat graft

Difference in medial/ Difference in length of

Time post-op Tibiofemoral angle lateral height of tibia operated and unoperated tibia
(week) (varus) (cm) (cm)
2 42.5° 0.55 0.25
4 36.5° 0.55 0.5
6 31.5° 0.5 0.6
8 51.5° 0.65 0.7
12 41° 0.5 0.7

obtained at 2, 4, 6, 8, 12 and 16 weeks in there was distal migration of the silastic. In

group I and at 2, 4, 6, 8 and 12 weeks after
the second operation in groups II, III and
IV. Results are shown in Tables 1, 2, 3 and 4.
Excision of the medial half of the epiphyseal
plate resulted in varus angulation at the tibia
which started as early as two weeks. A bony
bridge inevitably formed. Comparison of the
tibiofemoral angle, difference in medial and
lateral heights of the tibia and difference in
the length of the operated and unoperated
tibia showed a superior result in the group
that had physeal transfer. Histological sections
showed reformation of the bony bridge in
the group with fat graft, in the static group,
the physeal transfer group, the transferred
growth plate appeared intact.
In this controlled experiment involving
rabbits, excision of 50% of the growth
plate resulted in partial growth arrest in
all animals. After epiphysiolysis, the group
with physeal transfer showed a superior
result to the group with silastic which in
turn was superior to the group with a free fat
graft. The correction of the angular deformity
was however not complete in all groups.
The overall length was also not restored.
Further experiments are underway to look
into latter problem.

87
E.H. Lee, G.X. Gao, K. Bose

Table 4. Group IV: Silastic spacer

Difference in medial/ Difference in length of

Time post-op Tibiofemoral angle lateral height of tibia operated and unoperated tibia
(week) (varus) (cm) (cm)
2 27.5° 0.2 0.2
4 25° 0.25 0.3
6 36° 0.55 0.5
8 27.5° 0.5 0.4
12 50° 0.65 0.8

Figure 1. Roentgenographic appearance of both Figure 2. Roentgenographic appearance of both

femurs and tibiae 8 weeks after physeal graft. femurs and tibiae 8 weeks after fat graft.

88
14 Treatment of bone bridges by physeal
distraction. An experimental study
J. Azcárate
INTRODUCTION
Up until 1967, there were basically two
treatments for correcting angular deformities
secondary to physeal bone bridges: corrective
osteotomies and/or completion of the
epiphysiodesis(14).
That year, Langeskiold proposed resection
of the bone bridge with the interposition
of autologous fat for treating this type of
lesions(10).
Physeal distraction is also a technique used
for lengthening bone in skeletally inmature
patients. Basically, it consists of using the
physis as a point of low resistance which, when
subject to traction, undergoes epiphyseal -
metaphyseal separation. This way, lengthening
is achieved without the need for osteotomy
or osteoclasis(4,5,9,11,13).
At the Department of Orthopaedic Surgery
and Traumatology of the University Clinic of
Navarra, this method had already been used
for correcting angular deformities with partial
physeal closures(1). In the treated cases results
were satisfactory, although as the subjects were
childrens close to the age of bone maturity,
it was not possible to observe the degree of
deformity recurrence.
In order to ascertain in depth the
phenomena involved in the procedure des-
cribed, we designed the following experimental
study, intended to:
1. Demonstrate the possibility of breaking bone
Reprinted with permission of Mapfre Medicina (vol. 4, suppl 2)
Research conducted at the Department of Orthopaedics of the University of Navarra Medical School
bridges by means of physeal distraction.
2. Study the morfological aspects of both
the physis and the bone bridge after the
breakage.
3. Verify the possibility of relapse of the bone
bridge after its breaking and, in this case, to
study the possibility of preventing relapse
through the application of autologous fat.
MATERIAL AND METHOD
We used 30 male lambs aged one-and-a-
half months and weighing 8 - 13 Kg. All lambs
underwent epiphysiodesis at the level of the
right lateral femoral condyle, with excision
of an epiphyseal-metaphyseal fragment and
insertion of a graft from the ipsilateral iliac
crest.
The lambs were divided into three groups:
- Group A. Comprising 10 lambs. Five of
them (sub-group A.1) were sacrificed
two months after the operation and the
other five (sub-group A.2) six months
after it.
- Group B. Comprising 15 lambs. All of them
were fitted with an external axial fixation
device two months after the epiphysiodesis,
distraction commencing inmediately at a
rate of 1/2 mm per day. Five (sub-group B.1)
were sacrificed ten days after distraction
began. In the remainder, distraction lasted
for one month, five of the lambs being
89
J. Azcárate
Figure 1.
sacrificed two months after the distractor
had been fitted (sub-group B.2) and the
other five (sub-group B.3) four months
after its fitting.
- Group C. Comprising five lambs. In these,
the fixator was fitted two months after the
epiphysiodesis, distraction starting at the
rate of 1 mm/day for ten days, following
which the lambs were operated on again for
the purpose of grafting autologous fat to
the epiphysiodesis area. These lambs were
sacrificed four months after distraction
was begun.
Inmediate post-operative radiographic
studies, bimonthly radiological controls and
post-mortem analysis were carried out on all the
specimens. On the X-rays, the angle between the
diaphyseal axis and the tangent to the condyles
was measured, as was the femoral lenght.
Coronal sections of the distal epiphyses
90
Figure 2.
of all femurs were made for macroscopic and
radiographic examination.
Histological studies of the distal end of each
femur were done in all the specimens, using
haematoxylin-eosin and Masson trichromic
staining.
RESULTS
Radiological study
Group A
Radiologically, an interruption could be
seen in the radiotransparent line corresponding
to the physeal cartilage, this being associated
with femoral shortening and valgus. These
findings were more evident in sub-group A.2
with a distal femoral valgus of 20.6º (14º - 27º)
and a shortening of 13 mm (9-18 mm) (Fig.
1). In sub-group A.1 the femoral valgus was
of 8.6º (7º-10º) and the shortening 3.4 mm

Figure 3.
(1 - 6 mm). All the tibias showed a moderate
varus deformity (2.8 º on average in A.1 and
5º in A.2)
Group B
Sub-group B.1. The X-rays showed in
all cases a clear epiphyseal-metaphyseal
separation with a radio-transparent area
between both segments (Fig. 2). The X-rays
of the coronal sections showed that in all
cases the separation occurred at the level of
the physeal cartilage.
Sub-group B.2. In all the lambs in this sub-
group there was a varying degree of radiological
opacification in the area corresponding to the
epiphyseal - metaphyseal separation.
Sub-group B.3. The X-ray findings for this
sub-group were comparable with those of
sub-group A.2 with an obvious femoral valgus
deformity of 13.4º (5º-18º) on average and an
Treatment of bone bridges by physeal distraction
Figure 4.
operated limb averaging 4.2 mm longer than
the contralateral one (Fig. 3).
Group C
The femoral valgus of the limbs operated
in this group was less extreme than in the rest
of the sub-groups and imperceptible in two of
them (Fig. 4). The average valgus deformity
was 7º (2º - 12º) with an average shortening
of 0.2 mm. An ossification defect at the site
of the fat graft was evident in the X-rays of
the coronal sections.
Histological study
Group A
The growth cartilage in the lambs of both
sub-group A.1 and A.2 was interrupted at the
point of union of its central and lateral thirds
by mature trabecular bone connecting the
metaphyseal and epiphyseal segments. There
91
J. Azcárate
Figure 5.
were no significant changes in the growth
cartilage in these lambs when compared with
the contralateral physis (Fig. 5).
Group B
Sub-group B.1. In this sub-group there was
an epiphyseal - metaphyseal separation with
two clearly differentiated areas. On the one
hand there was a true physeal fracture sited
invariably between the layer of hypertrophic
cells and the calcification area. On the other
hand, a second area could be seen consisting
of broken trabeculae which corresponded
to the bone bridge produced in the first
operation,
Both areas were occupied by a haematoma
which showed areas of greater organisation at
the level of the more lateral zone corresponding
to the bone bridge area. The growth cartilage
showed a comparative enlarging of the layer
92
Figure 6.
of hypertrophic cells with regard to the control
side (Fig. 6).
Sub-group B.2. The lambs pertaining to
this sub-group showed an advanced degree
of ossification at the level of the epiphyseal
- metaphyseal separation zone, both in the
area corresponding to the physeal separation
and at the level of the broken bone bridge.
There was a periostal type of ossification
process at the level of the lateral and medial
margins, associated with signs of endochondral
ossification in the metaphyseal region of the
physis, which showed no structural differences
with regard to the control physis.
Sub-group B.3. In this batch, ossification of
the elongated area was complete. At the level
of the junction between the central and lateral
thirds of the growth cartilage, the physis was
clearly interrupted by a bone bridge formed by
mature trabeculae connecting the epiphyseal

Figure 7.
and metaphyseal segments. All these data were
comparable with those observed in sub-group
A.2. The morphological characteristics of the
physis were similar on the operated and the
control sides (Fig. 7).
Group C
The findings in the lambs of this group
were not constant, depending on the degree
of interposition achieved with the fat graft.
In those cases in which a correct
interposition of fat had been achieved, no
epiphyseal-metaphyseal contact occurred and,
therefore, no bone bridge was visible at that
level. When the fat was not correctly sited,
a certain degree of epiphyseal-metaphyseal
contact occurred, although it was always
less than in sub-group B.3. The fatty tissue
interposed underwent a fibrous transformation
with evidence of vascularisation inside.
The area of physeal separation showed
Treatment of bone bridges by physeal distraction
morphological data similar to those of sub-
group B.3 with complete ossification of the
elongated area. Observation of the remaining
physis in these lambs showed a comparative
thinning of the germinal and hypertrophic
layers on the operated side respect to the
control side (Figs. 8A and 8B).
DISCUSSION
The possibility of treating angular deformity
and limb shortening caused by a bone bridge
by means of physeal distraction has already
been described both from the clinical(1,8) and
the experimental(2,3,6,7,12) standpoints. Some of
these authors did some surgery on the bone
bridge before commencing distraction, such as
bone bridge osteotomy(12) or its resection with
interposition of fat(6-8). The possibility of bone
bridge breakage without prior intervention
was shown clinically in the Department of
Orthopaedic Surgery and Traumatology of
the University Clinic of Pamplona(1) and both
clinically and experimentally at the University
of Nebraska(2,3,12).
Contrary to the observations of Foster(6)
who recorded a high incidence of epiphyseal
fractures after physeal distraction, in our study
distraction constantly led to a clear physeal
separation. The reason for the high number of
fractures was probably due to the different type
of fixation device used. The cases treated by
this author also presented a tendency towards
premature physeal fusions.
In contrast with Foster´s work, the
experience of Connolly (3) in carrying out
distraction without prior resection showed
an optimistic result with the absence of
relapse of the deformity. We believe that the
short follow-up on his animals and the small
size of the bone bridge in his experimental
model were the reasons for such optimistic
results.
The recurrence of the deformity in our
experiment when only simple distraction of
93
J. Azcárate
A
the bone bridge was undertaken, led us to
complete the work with interposition of fat.
We knew of no prior work in this sense, except
for that of Foster et al(6,7) who had interposed
fat at the level of the resected bone bridge,
prior to distraction.
In relation to our findings, it is feasible
to think that with the correct interposition of
fat it should be possible to expect a definitive
correction of the deformity, even in cases
removed far from the age of bone maturity.
From the point of view of clinical
application, it is vital to know what
repercussions this procedure may have on
the physis subject to distraction. While from
the experimental standpoints, and at least
structurally, it does not appear to cause any
important damage to the physis, we cannot
foresee what the functional repercussions
would be. We therefore believe that before
using this method on children whose ages are
94
B
Figure 8 A and B.
a long way from that of bone maturity, It is
necessary to develop experimental work that
will provide information on the functionality
of the distracted physis.
CONCLUSIONS
1. Physeal distraction applied experimentally
to lambs which had previously undergone
epiphysiodesis can break the bone bridges
without the need for prior resection.
2. After distraction there is a recurrence of
the bone bridge and, whit it, the angular
deformity.
3. The application of autologous fat in
the area of disruption can prevent both
recurrence of the bone bridge and the
deformity, and this degree of prevention
is proportionate to the quality of the
interposition.
REFERENCES
1. Cañadell J, De Pablos J. Breaking bone bridges by
physeal distraction. Int Orthop (SICOT) 1985;9:223-
9.
2. Connolly JF. Epiphyseal traction to correct acquired
growth deformities. Orthop Trans 1984;8:477.

3. Connolly JF, Huurman WW, Lipiello L, Pankaj
R. Epiphyseal traction to correct acquired growth
deformities. An animal and clinical investigation.
Clin Orthop 1986;202:258-68.
4. De Pablos J, Cañadell J. Experimental physeal
distraction in inmature sheep. Clin Orthop
1990;250:73-80.
5. Fischenko PJ, Karimova LF, Pilipenko N P.
Distraction epiphysiolisis in congenital shortening
of lower extremities. Ortop Traumatol Protez
1976;37:44-62.
6. Foster BK, Rozenbilds M, Yates R. A pilot study
of the growth potential of the physis in a sheep
tibial model. J Bone Joint Surg (Br) 1984;66:778.
7. Foster BK, Rozenbilds M, Yates R. Further results
of distraction physeolisis in a sheep tibial model.
J Bone Joint Surg (Br) 1986;68:333.
8. Foster BK, Rozenbilds M, Yates R. Interpositional
and distractional physeolisis. The clinical results
of physeal bridge resection combined with
chondrodiastasis. Proceedings of the Meeting
Treatment of bone bridges by physeal distraction
on Recent Advances in External Fixation. Italy:
Riva di Garda, 1986;168.
9. Ilizarov GA, Soibelman A. Some clinical and
experimental data on bloodless lengthening of
lower extremities. Exp Khir Anest 1969;14:27-32.
10. Langeskiold A. The posibilities of eliminating
premature partial closure of an epiphyseal plate
caused by trauma or disease. Acta Orthop Scand
1967;38:267-79.
11. Monticelli G, Spinelli R. A new method of treating
the advanced stages of tibia vara (Blount disease).
Ital J Orthop Traumatol 1984;10:295-303.
12. Ray SK, Connolly JF, Huurman WW. Distraction
treatment of deformities due to physeal fractures.
Surg Forum 1978;29:543-6.
13. Ring PA. Experimental bone lengthening by
epiphyseal distraction. Br J Surg 1958;46:69-73.
14. Tadhdjian MO. Pediatrics Orthopaedics.
Philadelphia: W B Saunders, vol. II, 1972; 1462-
8, 1588-90.
95
15 Hemichondrodiatasis: is bridge resection
necessary?
E.H. Lee, J.W.K. Chan and K. Bose
Figure 1. Right (control) and left (experimental)
tibiae showing normal alignment with distraction
device in place after 4 weeks.
INTRODUCTION
De Bastiani and his colleagues has reported
on the technique of closed, gradual controlled,
asymmetric distraction of the growth plate to
96 Partly reprinted with permission of Mapfre Medicina (vol. 4, suppl 2)
correct angular deformities near ends of long
bones. They felt that in cases where the bony
bridge was small (less than 50%) resection
of the bridge was not necessary to achieve
good correction.
This study was designed to address
the question of whether bridge resection is
advantageous in the correction of growth arrest.
4 - 6 weeks old NZ white rabbits were used.
A growth arrest was created by excising the
medial half of the proximal growth plate of the
tibia. Three weeks later, an angular deformity
developed. Histological sections showed a bony
bridge across the growth plate. Two separate
experiments were then conducted. In group
I a distraction device was placed across the
bony bridge and distraction commenced the
following day at 0.5mm day. In group II, the
bony bridge was excised and distraction was
applied across the excised bridge in a similar
fashion. Distraction was continued for 4 weeks
(Fig. 1). Clinical radiological and histological
assessments were done at 1, 2, 4, 6, 8 and 12
weeks post-distraction.
RESULTS
Measurements were made of the tibio-
femoral angle and the difference between the
medial and lateral heights of the tibia (Figs.
2 and 3). The overall length of the tibia was
 Hemichondrodiatasis: is bridge resection necessary?

Figure 2. Measurement of tibiofemoral angle Figure 3. Measurement of medial and lateral height
(anatomical axis). of tibia.

Table 1. Excision of proximal half of tibial hysis

Difference in medial/ Difference in length of

Time post-op Tibiofemoral angle lateral height of tibia operated and unoperated tibia
(week) (varus) (cm) (cm)
2 28° 0.7 0.2
4 33° 0.9 0.3
6 30° 0.8 0.6
8 28° 0.7 0.7
12 28° 0.6 0.6
16 44° 1.7 0.9

also measured. These were compared with
that of the normal unoperated leg. Results
are shown in Tables 1, 2, 3 and 4.
Histological sections showed that in group
I (bridge intact), the area that was distracted
was full of new bone. In group II (brdige
excised) the intervening area had less bony
tissue.
Group II was found to have a superior
result to group I in correcting the angular
deformity. In addition, greater longitudinal
growth of the tibia was achieved with group II.
This experiment showed that in rabbits where
the bony bridge involves 50% of the growth
plate, bridge resection before distraction gives
a better correction.

97
E.H. Lee, J.W.K. Chan, K. Bose

Table 2. Measurement of tibiofemoral angle

Time post-op GroupI GroupII

(week) (Bridge Intact) (Bridge Excised)
1 21.5° 6°
2 13° 3°
3 15° 5°
4 11° 5°
6 25.5° 18°
8 17° 15°
12 17.5° 11°

Table 3. Difference in medial/lateral height (cm)

Time post-op GroupI GroupII

(week) (Bridge Intact) (Bridge Excised)
1 0.4 0.1
2 0.2 0.15
3 0.3 0.1
4 0.4 0.15
6 0.45 0.35
8 0.5 0.1
12 0.6 0.25

Table 4. Difference in length of operated and unoperated tibia (cm)

Time post-op GroupI GroupII

(week) (Bridge Intact) (Bridge Excised)
1 0.2 0.1
2 0.7 0.1
3 0.2 0.1
4 0.4 0.1
6 0.25 0.45
8 1.0 0.4
12 1.0 0.25

98
16 Growth cartilage transplants.
Experimental study
A. Peinado
In 1899, Helferich was the first to publish
results of epiphyseal transplants carried out
on laboratory animals. At the beginning
of this century a large number of studies
appeared on reimplants, autotransplants and
homotransplants which included the physis
along with large fragments of metaphysis
and diaphysis. The results were exciting in
some cases (Heller, Fohl) and discouraging
in others (Haas)
During the course of time, works done
by Lacroix, Urist, Ring and Trueta´s studies
on bone physiology, provided important
information on the feaseability of growth
cartilage transplants, which lead Harris to
present in 1965 his experimental results
on isolated physis transplants. In 1974,
Calderwood repeated Harris´s work, supplying
the laboratory animals with hyperbaric oxygen
for the purpose of evaluating the effects of
the oxygen on their survival and on any
improvement in the results.
MATERIAL AND METHODS
Following the technique described by
Harris, we performed reimplants of the isolated
distal ulnar physis in 46 rabbits, autogenous
transplants of one extremity to the other in 40
rabbits, and excision of the distal ulnar physis
without reimplantation in 14 rabbits.
Partly reprinted with permission of Mapfre Medicina (vol. 4, suppl 2)
Research conducted at the Department of Orthopaedics of the University of Navarra Medical School
In all 100 rabbits two to four weeks old
were used.
After anaesthetising the animal with ether,
a longitudinal incision is made to expose the
distal ulnar physis subperiosteally. Slight
pressure is sufficient to produce epiphysiolysis
and the physis can be separated from the
epiphysis with a scalpel blade. The base of
the epiphysis is curetted away to eliminate
any residue of growth cartilage germinal cells.
Reimplants
The physis was replaced in its own bed.
In five rabbits, reimplantation was bilateral
Autogenous transplants
Both ulnar physis were excised and
interchanged.
Excision of the distal ulnar physis
In order to get a reference on the changes
and deformities which occur when the distal
ulnar epiphysis stops growing completely,
the ulnar physis was excised in 14 rabbits.
A radiological study was carried out every
day for the first thirty days, then at variable
intervals and lastly when the animal was
sacrificed.
Histological studies were done by
sacrificing two rabbits from the reimplant
group and one from the autotransplant group
99
A. Peinado
at intervals of one, two, three, four, five , six,
seven, eight, nine, ten, eleven, twelve, twenty-
one and thirty days. The rest of the animals
were sacrificed at varable intervals after forty-
five days.
Both front paws were dissected and fixed
in 10% formol, and decalcified in 5% formic
acid. The bone tissue was impregnated with
paraffin, sections were made of it and stained
with eosin haematoxylin.
RESULTS
Some animals had to be rejected owing
to postoperative infection or disease. For
long-term evaluation of the results there
remained: twenty two reimplants, thirty seven
autotransplants and ten ulnar excisions of
more than forty five days .
The criteria for evaluating satisfactory
results were:
a) The normal radiological appearance of
both bones in the forearm.
b) The orderly histological structure of the
growth cartilage.
An additional criterion in the evaluation
of the unilateral reimplants was the study of
the growth of the ulna operated on, in relation
to the opposite, non operated side.
In accordance with these criteria, the results
obtained were as follows:
Unilateral reimplants
Nine successes out of thirteen cases (69%).
In these, the growth of the ulna varied between
80% and 92% of that of the control ulna.
Bilateral reimplants
Six satisfactory results out of nine (67%).
Excision of the ulnar growth cartilage
From the moment epiphysial-metaphyseal
bone union was observed (ten to twelve days),
average daily growth of the ulna was 0.009
mm. Table 1 shows the growth of the normal
100
Table 1. Daily growth rate of normal ulna
First five days...................................... 0.74 mm
Five to ten days................................... 0.76 mm
Ten to fifteen days .............................. 0.66 mm
Fifteen to forty eight days ................. 0.50 mm
Forty eight to sixty days .................... 0.43 mm
Growth rate in the two months ........ 0.54 mm
Table 2. Daily growth rate in unilateral
reimplants
First five days ..................................... 0.46 mm
Five to ten days .................................. 0.58 mm
Ten to fifteen days ............................. 0.58 mm
Fifteen to forty eight days ................ 0.45 mm
Forty eight to sixty days ................... 0.37 mm
Growth rate in the two months ....... 0.47 mm
Table 3. Average daily growth in the first
two months
Normal distal ulnar physis .............. 0.54 mm
Unilateral reimplants ........................ 0.47 mm
Bilateral reimplants ........................... 0.36 mm
Proximal ulnar physis ....................... 0.09 mm
ulna. Table 2 shows the daily rate of growth
of the unilateral reimplants. Table 3 shows the
daily rate of growth of the normal ulna, of the
unilateral reimplants, of the autotransplants
and of the proximal ulnar growth cartilage.
The radiological and histological changes
of the reimplants and the autotransplants are
almost identical.
Radiological changes
During the first three days there is a
progressive increase in the height of the
physis (Fig. 1)
In the satisfactory transplants, between
days five and seven, a horizontal line of
calcification can be seen (Fig. 2).
At the same time as this dense line
appears, the medial side of the distal radial
physis shows in the majority of the cases, a

Figure 1. Left reimplant. Increase in height of the
reimplant compared to the growth cartilage on
the normal side.
Figure 2. Left reimplant. Between the ulnar epiphysis
and the metaphysis, there is a dense transverse line
that divides the radiolucent space into two unequal
halves. This is the dense epiphyseal line.
typical V deformity (Fig. 3). This V deformity
disappeaers in two or three days and the
radial growth continues unchanged (Peinado).
Between days fifteen and thirty, the
dense epiphyseal line fuses with the distal
ulnar epiphysis, giving rise to a larger,
normal shaped ulnar epiphysis (Fig. 4). The
Growth cartilage transplants
Figure 3. Unsuccessful reimplant. Marked V
deformity in the distal radial physis. The radial
epiphysis inclines towards the ulna.
radiological appearances of the ulna and radius
in the satisfactory transplants is nornal or
shows a slight curvature in both bones (Fig. 5).
In the unsatisfactory transplants the
dense epiphyseal line does not form, or else
it does so incompletely or is sloping (Fig.
6). The ulnar inclination of the distal radial
epiphysis disappears a few days after the V
deformity appears and suddenly reappears
with every new V deformity of the radial
physis. Figure 7 shows the radiological
image of the bones of the forearm in the
unsuccessful transplants.
In one infected ulnar reimplant, we could
see the appearance of a complete lower radial
epiphysiolysis (Figs. 8, 9).
Excision of the ulnar physis
The radiological image of the ulnar physis
101
A. Peinado

Figure 4. Ulnar reimplant showing radiological changes Increase in height of the ulnar physis. Appearance
of the dense epiphyseal line. Appearance of the V deformity in the radial physis. Fusion of the dense
epiphyseal line with the ulnar epiphysis, to end with a normal shaped lower ulnar epiphysis.

Figure 5. Normal long-term left reimplant. Normal Figure 6. Unssuccesful autotransplant. No dense
growth. No deformities of radius and ulna. epiphyseal line has appeared.

102

Figure 7. Unssuccesful autotransplants. Bone
deformities of both bones.
Figure 8. Left infected reimplant. Wide gap between
lower ulnar epiphysis and metaphysis marked V
deformity of the radial physis.
excisions shows some constant aspects after
six week´s evolution:
- Hypoplastic ulnar epiphysis.
- Short, straight ulna.
- Pronounced widening of the ulnar
metaphysis.
- Complete incurvation of the radius.
- 90-Degree ulnar tilting of the radial
epiphysis (Fig. 10).
Growth cartilage transplants
Figure 9. The lack of rigidity of the tissue between
lower ulnar epiphysis and metaphysis,allows the
traction forces acting upon the lower radial epiphysis,
to produce a complete radial epiphysiolysis.
HISTOLOGICAL CHANGES
During the first 24 hours, the transplant
shows an increase in the height owing to an
increase in in the cells of the germinal layer
and in the layer of the hypertrophied cells.
In the following days, until the sixth day, the
height of these layers continues to increase
(Figs. 11, 12) while the layer of proliferative
cellsIn the following days, until the sixth day,
the height of these layers continues to increase
(Figs. 11, 12) while the layer of proliferative
cells decreases in height. Between day seven
and twelve, the transplant takes a normal
appearance.
The plane of cleavage between the ulnar
epiphysis and the transplant is usually visible
during the first three weeks (Figs. 13, 14).
Histological study of the V deformity
shows that the cause of the deformity is an
epiphysiolysis of the medial side of the radial
physis (Fig. 15).
103
A. Peinado
Figure 10. Left lower ulnar physis excision.
DISCUSSION
The overall results of these experiments
are in accordance with those presented by
other authors (Heller, Ring) in the sense that
the results are better in the reimplants than
in the autotransplants, probably because the
transplant fits into its bed better in the former
case. However, Harris reports better results
with the autotransplants.
The good results obtained with the
reimplants (68%) are comparable to Ring
(67%) and are better than the ones reported
by Harris (44%).
The 29% of good results in the auto-
transplants is comparable to Ring´s (27%) and
Calderwood´s in the groups not treated with
hyperbaric oxigen (28%), but lower than those
reported by Harris (54%) and by Calderwood
in the group treated with hyperbaric oxigen
(48%).
104
Figure 11. Normal histology of the lower ulnar
physis.
During the first five or six days, after the
operation, the radius grows faster than the
ulna despite the increase in height of the ulnar
physis, and the radial epiphysis pulls the
ulnar epiphysis with it. Towards the fifth day
after the operation, a band of endochondral
ossification, wich corresponds to the dense
epiphyseal line seen in the X-ray film, appears
on the epiphyseal edge of the transplanted
physis.
The fibrous conective tissue located
between the ulnar epiphysis and the dense band
of ossification, offers a progressive resistance
to stretching. Under these circumstances,
if the rate of growth of the transplant does
not reach almost normal proportions, the
distal radial epiphysis is pulled towards the
ulna. The consequence of this biomechanical
change, is a pronounce increase in the height
in the layer of the proliferative cells on the

Figure 12. Histology of a left reimplant five days
after the operation, showing the increase in its height.
Figure 13. Reimplant 24 hours after the operation.
The cleavage plane between the physis and the
epiphysis and metaphysis is evident.
Growth cartilage transplants
Figure 14. Reimplant nine days post-op. A broad
area of endochondral ossification can be seenbetween
the physis (bottom right) and the fibrous tissue
next to the ulnar epiphysis (top left).
radial half of the distal growth cartilage of
the radius and, subsequently, the appearance
of a hemiepiphysiolysis. This hemiepiphy-
siolysis, is the first radiological sign indicating
a reducction in growth of the transplant
(Peinado).
In the infected reimplant previously
showed. (Figs. 8, 9), the weak inflamatory
fibrous tissue replacing the ulnar physis,bended
itself, allowing a complete epiphy-siolysis
of the radial epiphysis.This case shows that
continuous inner shear forces acting on a
healthy growth plate, lead to an epiphysiolysis.
The active growth of the transplant is
diminished during the first ten to twelve days
and matches with the reduction in the number
of cells in the proliferative zone (Harris´s
avascular phase). The rate of growth of the
succesful transplants reaches normal figures
after ten or twelve days following the operation
coinciding with the disappearance of the V
deformity of the radial physis.
The radiological criterion was the most
accurate for evaluating the transplants and in
my opinion, the good results tend to decline
with time.
The main cause of the unsuccessful
cases was a faulty excision of the physis or
a displacement of the physis from its bed.
105
A. Peinado
Figure 15. Distal radial hemiepiphysiolysis.
REFERENCES
- Calderwood J. W. The Effect of Hyperbaric Oxigen
on the Transplantation of the Epiphyseal Growth
Plate in the Rabbit. J. Bone and Joint Surg (Br)
1974;56B:753-759.
- Fohl. Th Versuche Über die Transplantation der
Knorpelfuge. Arch. F Klin Chir 1929;CLV:232.
- Harris. R.W.; Martin R. Tile M. Transplantation
of Epiphyseal Plates. J. Bone and Joint Surg 1965;47
A:897-914.
- Heller E. Versuche Über die Transplantation der
Knorpelfuge. Arch. F. Klin. Chir. 1918;109:1-62.
106
- Helferich H. Versuche Über die Transplantation
des Intermediarknorpels wachsender rohren-
knochen. Dtsch Z Chir 1899;51:564-573.
- Hass S.L. Further Observations on the
Transplantation of the Epiphyseal Cartilage Plate.
Surg. Ginaec. And Obstet 1931;52:958-961.
- Lacroix P The Organization of Bones. Churchill
London 1951.
- Peinado. A. Distal Radial Epiphyseal Displacement
after Impaired Distal Ulnar Growth. An
Experimentel Study in Rabbits. J. Bone and Joint
Surg 1979;61-A:88-92.
- Ring P.A. Excision and Reimplantation of the
Epiphyseal Cartilage; of Rabbit. J. Anat 1955;89:
231-237.
- Ring P. A, Transplantation of Epiphyseal Cartilage;
an Experimental Study. J. Bone and Joint Surg
1955;37-B:642-657.
- Trueta J. Amato V P. The Vascular Contribution
to Osteogenesis. III Changes in the Growth
Cartilage Caused by Experimentally Induced
Ischaemia. J. Bone and Joint Surg 1960;42-B:571-
587.
- Trueta J Morgan J.D The Vascular Contribution to
Osteogenesis Y. Studies by the Injection Method.
J. Bone and Joint Surg 1960;42-B:97-109.
- Trueta J. Little. The Vascular Contribution to
Osteogenesis II. Studies with the Electron
Microscope. J. Bone and Joint. Surb 1960;42-B:367-
376.
- Urist M. R Silverman B F Buring K L. Dubuc F.
L Rosenberg L M The Bone Induction Principle.
Clin Orthop 1067;53:243-283.
17 Reimplantation of growth plate
chondrocytes into growth plate defects in
sheep
B.K. Foster, A.L. Hansen, G.J. Gibson, J.J. Hopwood,
G.F. Binns and O.W. Wiebkin
Injuries to the growth plate may result
in par­tial or total growth arrest due to the
formation of a bone bridge that replaces the
damaged segment of growth plate cartilage.
A variety of orthope­dic procedures have been
and are being investi­gated in an attempt to
achieve predictable correc­tion of deformities
caused as a result of growth arrest. These
involve the use of fillers to prevent the
formation of a bone bridge(1,8,14) and mo­re
recently the use of high-density cultures of
growth plate chondrocytes(6,7). We have shown
previously that chondrocytes isolated from
ovi­ne growth plate cartilage will form cohesive
car­tilage like discs containing chondroitin
sulfate and cartilage-specific type ll collagen
in culture(6). This paper describes the response
of chondrocyte cultures to implantation into
experimental growth plate defects, in an
ongoing attempt to offer so­me insight into
the prevention of such growth deformities.
Cultures were implanted into defects
created surgically in the growth plates of
immature lambs and the fate of the implant
assessed histologically from 2 to 24 weeks
postoperatively. The implant remained viable,
continued to maintain a proteo­glycan-rich
matrix throughout the period exami­n ed,
and in all cases prevented bone-bridge for­
mation. Some areas of apparent hypertrophic
development and endochondral calcification
Reprinted with permission of Raven Press (J Orthop Ressearch 1990;8:555-64)
were also observed, particularly after 6 weeks
posto­peratively. Implant support materials as
well as the influence of distractive forces were
also as­sessed for their capacity to stimulate
cellular pro­liferation.
MATERIALS AND METHODS
Preparation of cultures for implantation
Ovine chondrocyte cultures were
established from the epiphyseal cartilage of
fetal lambs(6,15). Briefly, the growth plates from
fetal lambs obtained from a local abattoir were
excised asep tically, freed of any adhering
connective tissue minced, and digested
sequentially with 0.5 mg/m of hyaluronidase
(~ 500 TRU/ml: EC 3.2.1.35, Sigma, St. Louis,
MO, USA), 2 mg/ml of trypsin (~ 500 U/
ml: EC 3.4.21.4, Difco Lab., Inc., De­troit, Ml,
USA), and 1 mg/ml of bacterial colla genase
(~ 150 U/ml: EC 3.4.19, Sigma, type III)(4,15).
The suspension was filtered and washed
thoroughly in Ham’s F-12 nutrient medium
(GIB­CO, Grand Island, NY, USA). The isolated
cells were inoculated into spinner culture
for 24 h in medium containing 10% fetal calf
serum (FCS). They were then washed and
plated into 16 mm tissue culture wells at a
density of 2-3 millon cells/ml, in Ham’s F-12
supplemented with 20% FCS, and 50 µg/
ml of L-ascorbic acid. After se­veral days in
107
B.K. Foster, A.L. Hansen,G.J. Gibson, J.J. Hopwood, G.F. Binns, O.W. Wiebkin

culture, the growth plate chondrocytes formed
a cohesive cartilage-like disc.
Supporting Substrates
In some experiments, cell cultures just prior
to implantation were embedded in rat tail
type I collagen gels as previously described(5,6)
or type II collagen. Type II collagen isolated
and purified from sheep articular cartilage
was lyophilized to form a gauze-like mat to
support the cultures in vivo since it failed to
form a satisfactory gel.
Cell Labeling
5-Carboxyfluorescein diacetate
succinimidyl ester (CFSE, Molecular Probes

Table 1. Summary of implantation experiments

Time in Postoperative Distraction Cell Survivald Bone bridge

Sheep Implant culturea periodb timeC Femur Tibia tormatione

1 Chondrocyte disc 19 2 – ++ ++ –
2 19 2 – + ++ + –
3 19 4 – – + –
4 19 4 – + ++ –
5 13 4 – n.d. – –
6 19 4 – n.d. ++ –
7 12 4 2 n.d. – –
8 12 4 2 n.d. ++ –
9 12 4 2 n.d. + –
10 12 6 – + ++ –
11 19 6 – + + –
12 19 6 4 n.d. + –
13 19 6 4 n.d. ++++ –
14 16 8 – +++ +++ –
15 16 12 – ++ + –
16 13 12 – n.d. +++ –
17 13 24 – n.d. +++ –
18 13 24 – – ++ –
19 Type I collagen gel 2 – +
20 Type I collagen gel 4 – ++
21 Type ll collagen 2 – –
22 No implant 2 – +
23 No implant 2 – +
24 No implant 4 – ++

The chondrocyte implants in sheep 5 and 6 were supported by type II and type I collagen matrices,
respectively.
a
Time in culture (days) prior to implantation.
b
Time after implantation (weeks).
c
Time of distraction in weeks, commenced 2 weeks postoperative.
d
Estimation from histology of the defect of the relative survival of implanted chondrocytes: –, no
chondrocyte detected; +, chondrocytes detected, relaove proportion and viability indicated by the number of
symbols femur and tibia indicate the site of the physeal defect; n.d., not done.
e
Detection and extent of bone bridge formation: –, no bone bridge formation detected; + , active bone bridge
formation; ++, extensive bone bridge established connecting metaphyseal and epiphyseal bone.

108
 Reimplantation of growth plate chondrocytes into growth plate defects in sheep
Inc., Eugene, OR, USA) is a vital cell marker(2)
that we have shown previously, when added
to cell culture medium for 14 tc 21 days, will
fluorescently label chon­drocytes without
effecting cell growth or matrix production(6).
CFSE (0.033 mM) was added to the medium
of selected cultures for the duration of the
culture period, prior to implantation.
Surgical Implantation
In total, 24 merino lambs were used,
of which 18 had growth plate implants of
cultured chon­d rocytes, 5 of which were
distracted. Three re­ceived implants of collagen
gels alone and three had experimental defects
left without implanta­tion (Table 1). The lambs
were 5-13 weeks of age, and weighed between
10 and 19 kg. They were either bred on a
laboratory annex farm, or obtai­ned from an
abatoir market and hence unlikely to be related
to donor lambs. One proximal tibial growth
plate was used in each animal, and in so­me
cases the distal femoral growth plate of the
same limb. The opposite hindlimb served
as an unoperated control. The lambs were
anaestheti­zed using intravenous pentothal
and flurothane nitrous oxide. A longitudinal
incision exposed the subcutaneous tissue until
the level of the growth plate was visualized.
Partial ablation of the growth plate cartilage
was achieved using a dental burr and minimal
adjacent bone was removed. Thus, the
growth plate defects were fashioned for the
compact fit of the implant, to insure a well-
vas­cularized bed of surrounding tissue(13).
Using a previously designed template, marker
pins (Kirschner wires) were placed 20 mm
apart, both proximally and distally to the
defect sites, thus insuring accurate localization
for subsequent his­tological sectioning of the
defect. Using a spatu­la, cultured cartilage
discs were transferred direc­tly from the tissue
culture wells into the surgical defects .
Antibiotics (Streptopen) were administered
in­tramuscularly during surgery, and for 3 days
pos­toperatively. The animals were allowed
to bear weight immediately. For short-term
experiments (less than 6 weeks), the animals
were housed at the laboratory animal house
facility, and others were returned to the farm
to graze normally. The animals were sacrificed
using intravenous nem­butal, and the limbs
removed and fixed in 10% buffered formalin
for histological analysis.
Orthopedic Distraction
This group comprised five animals, each of
which had a growth plate defect implanted with
cultured chondrocytes (Table 1). Orthofix frames
were fixed to the operated tibiae and orthopedic
distraction applied 14 days postoperatively as
des­cribed by Monticelli and Spinelli(12) for the
ti­mes indicated in Table 1.
Histology
Following fixation in formalin for 2-3
days, the bones were radiographed and
decalcified in De­cal for about 5 days. A second
radiograph veri­fied the absence of any residual
calcification. The defect sites were located by
identification of the Kirschner wires, and the
bones sectioned accor­dingly. The material
was processed and embed­ded in paraffin.
Sections were stained with he­matoxylin and
eosin (H & E), Alcian blue (0.3% in 3% acetic
acid), or toluidine blue (pH 6.5).
RESULTS
Cultured Chondrocyte Implants
We have previously shown(6) that cultured
chondrocytes isolated from fetal ovine growth
plate formed a cohesive disc within the first few
days and continued to maintain a chondroitin
sul­fate proteoglycan-rich matrix containing
type II collagen for several weeks in culture.
Cultured chondrocyte discs were usually
implanted after 19 days in culture; however,
discs formed after briefer culture periods were
also-used. This was not expected to change
109
B.K. Foster, A.L. Hansen,G.J. Gibson, J.J. Hopwood, G.F. Binns, O.W. Wiebkin

A B

Figure 1. Radioloyy of sheep tibia with implanted

defects. Taken A) immediately postoperative, B)
after 4 weeks (sheep 4), and C) after 24 weeks (sheep
18). Note that the defect increases in size from being
not detectably greater in width than the growth
plate in A (the defect is located within the growth
plate between the locating pins) to occupying a
large portion of the metaphysis in C. Note also
the minimal erosion of epiphyseal bone proximal
C to the growth plate.

matrix constituents sin­ce these showed little
change over this time pe­riod(6); however, the
number of chondrocytes implanted and their
rate of proliferation may ha­ve varied by up
to twofold (unpublished data).
A total of 27 defects were implanted with
growth plate chondrocyte cultures (9 femoral
and 18 tibial). When examined at various times
pos­toperatively, 23 of these showed good
evidence of implant survival (Table 1). At
the time of im­plantation, the defect occupied
an area only slightly wider than the growth
plate itself as evi­denced by postoperative
radiology (Fig. lA) and afforded a compact fit
of the implanted chon­drocyte cultures. When
examined after 4 weeks, the defect site had
expanded into the metaphysis (Fig. 1B) and
by 24 weeks had occupied a con­siderable area
extending from the growth plate deep into
the metaphyseal bone (Fig. 1C). The growth
plate defects, whether implanted with cul­tured
chondrocyte collagen gels or left without
implants, did not produce any significant gross
structural changes in the limb since the initial
de­fect size was restricted to less than 20%
of the growth plate area shown in previous

110
 Reimplantation of growth plate chondrocytes into growth plate defects in sheep

B D

C E

Figure 2. Chondrocyte cultures within an experimental defect (sheep 4) 4 weeks after implantation. A)
Low power view sho­wing part of the implanted chondrocyte culture (IC) adjacent to host growth plate
(GP) ar,d a metaphyseal spur (MS). Invading immune, inflammatory cells (III) can be seen within the
defect site. The squares show areas presente in higher magnification in B and C. Alcian blue stain, x 4.
B) Higher magnification of an area shown in A. Host metaphyseal spur (MS) of growth plate is seen
adjacent to the implanted chondrocytes culture (IC). Some immune, inflammatory cells (II) are seen
adjacent to the implant matrix. Alcian blue stain, x 260. C) Higher magnification of an area shown in
A showing the implanted chon­drocyte culture with a proteoglycan-rich matrix. Surrounding immune,
inflammatory cells (II) can also be seen. Alcian blue stain, photographed with a green filter, x 265. D) Area
of viable implanted chondrocyte culture (IC) adjacent to an eosinophilic re­gion of residual chondrocyte
culture matrix (RM). Perichondriumlike fibrous tissue (FT) surrounds the viable chondrocyte im­plant.
H&E, x 275. E) Edge of implanted chondrocyte culture adjacent to invading immune, inflammatory cells
(II). Areas of matrix depleted of proteoglycans (DP) and empty lacunar spaces (LS) are observed. Alcian
blue stain, x 610.

111
B.K. Foster, A.L. Hansen,G.J. Gibson, J.J. Hopwood, G.F. Binns, O.W. Wiebkin
studies(3) to be less than the minimum defect
size that will result in gross limb alterations.
After 2 weeks pos­toperatively, the implant
was seen as a folded ribbon of strongly Alcian
blue-positive cartilage containing rounded
healthy chondrocytes. Aggre­g ations of
immune inflammatory cells were fre quently
observed within the defect, often surroun
ding the matrix.
After 4 weeks, prominent areas of
implanted proteoglycan-rich cartilage-like
matrix were observed; however, the density
varied within the defect, as did chondrocyte
survival and prolife ration (Fig. 2A). Figure
2B (4 weeks postope ratively) shows an area
of the defect adjacent to the host growth
plate, and allows a direct comparison of
these two tissues. The chondrocytes of the
implant showed a similar shape to those of
the host, but tended to be slightly smaller.
The greater lacunar space of the host cells,
howe ver, exaggerated this size difference.
The cartilage matrix of the host occupied a
relatively larger area and showed a higher
proteoglycan concentration (as indicated
by the intensity of Alcian blue staining)
than the adjacent implant. Other areas of
implant, however, showed a proteogly­can
concentration similar to or greater than that of
the host tissue (Fig. 2A). When observed with
112
Figure 3. An area of cultured
chondrocyte matrix after 12
weeks postimplantation (sheep
18), showing ordered columns
ofmaturing chondrocytes (CC)
and associated endochondral
bone formation (EB). HBE, x194.
a green filter to reduce the intensity of ma­trix
staining, the chondrocytes in this proteogly­
can-rich area were seen to be arranged in
circu­lar clusters and completely filled their
lacunar spaces (Fig. 2C). Hematoxylin and
eosin stai­ning, however, highlighted other
areas where the implanted chondrocyte matrix
was eosinophilic and appeared devoid of
rounded chondrocytes (Fig. 2D). This matrix
contrasted markedly with adjacent areas
of viable cartilaginous implant in that it
contained elongated “fibroblastic” cells,
probably of host origin, and did not stain
with Alcian blue.
Accumulations and occasionally dense
aggre­gations of immune inflammatory cells
could be seen around the chondrocyte implant
(in Figs. 2C, 2D and 2E). In some areas, they
surrounded implant containing apparently
proliferating chon­drocytes. Here, a fibrous
perichondrium-like tis­sue was frequently
seen to encapsulate and ap­parently protect
the viable implant. In contrast, the necrotic
eosinophilic, residual implant appea­red
to be devoid of this fibrous envelope (Fig.
2D). In other areas, too, host cells appeared
to invade the viable chondrocyte implant,
where this was not surrounded by a fibrous
perichondrium­like tissue. The edge of the
implant matrix in these areas showed a loss
 Reimplantation of growth plate chondrocytes into growth plate defects in sheep
of proteoglycan stai­ning and empty lacunar
spaces were frequently observed (Fig. 2E).
Many of the features of the implant and
host response observed at 4 weeks were
also obser­v ed afte, longer postoperative
periods, particu­larly the variability of implant
survival and persis­tent host cellular immune
reaction. In addition, with increasing time
postoperatively, the implan­ted chondrocytes
showed evidence of cellular maturation. After
6 weeks, the viable cartilage implant stained
strongly with Alcian blue and fre­quently
contained chondrocytes at various sta­ges of
hypertrophy. From 8 to 24 weeks, eviden­ce
of endochondral calcification was frequently
observed. This was sometimes associated
with columnation and evidence of ordered
chondro­cyte development reminiscent of that
seen in the growth plate (Fig. 3).
Labeled implants
To assist recognition of the implant postope­
ratively, some were labeled in culture with
a fluo­rescent dye (CFSE). We have shown
previously that chondrocytes could be
uniformly and inten­sely labeled by incubation
in CFSE for the dura­tion of the culture period
without affecting cell viability in vitro(6).
Similarly, in vivo labeled cul­tures implanted
into defects proved to be no less viable than
Figure 4. Bone bridge formation
in a control defect im­planted
with a type I collagen gel after
4 weeks (sheep 20); gp, growth
plate; bb, bone bridge formed
across the experi­mental defect.
HBE, x40.
the unlabeled cultures. The fluores­cent label
was readily identified within the implan­ted
cells at 2 weeks. However, the discrete intra­
cellular fluorescence was reduced by 4 weeks
and very difficult to detect thereafter.
The effect of supporting matrices
The use of a type I collagen gel to support
the culture matrix within the defect site
made little or no difference to cell viability
or inflammatory response. The use of type
II collagen as a sup­port matrix gave rise to a
massive inflan~matory response and led to
rapid degeneration of the im­planted cells.
The use of orthopedic distraction
Where distraction was performed
subsequent to implantation of cultured
chondrocyte discs, no consistent effect on
implant proliferation or survival was observed.
The fate of the implant was generally similar
to that observed without distraction .
Defects left without chondrocyte implants
The five defects implanted with type I
collagen gels alone or left without implanted
material sho­wed evidence of bone bridge
formation as early as 2 weeks after surgery
and extensive bone brid­ge formation by 4
weeks (Fig. 4). The defect implanted with
113
B.K. Foster, A.L. Hansen,G.J. Gibson, J.J. Hopwood, G.F. Binns, O.W. Wiebkin
a type II collagen gel showed an extensive
immune response that surrounded rem­nats
of the implant but no signs of bone bridge
formation.
DISCUSSION
In a study of 1,974 fractures at the Adelaide
Children’s Hospital, 17.9% had growth plate
in­volvement, and the incidence of subsequent
growth arrest was 1.4%(11). Orthopedic treat­
ment of such bone deformation may require
sur­gical resection of the resultant growth plate
bo­ne bar, and replacement with an inert filter
at the site. This report outlines the survival
and prolife­ration of cultured growth plate
chondrocytes im­planted into experimental
growth plate defects in sheep. This, together
with the subsequent pre­v ention of bone
bridge formation, suggests that implantation
of cultured growth plate chondrocy­tes may
prove to be successful in the prevention of both
growth arrest and limb deformity follo­wing
growth plate damage.
Control defects implanted with collagen
gels or left without implants showed rapid
and exten­sive bone proliferation adjacent
to and within the implant size such that a
bone bridge was formed within 4 weeks
of surgery. Implanted chondro­c yte discs
prevented this phenomenon in all ex­perimental
studies, even in those few where implant
survival appeared to be minimal. In 23 of 27
implanted chondrocyte cultures, the chon­
drocytes continued to maintain a proteoglycan
­rich cartilage matrix, for the duration of the
ex­perimental period and in some cases showed
evi­dence of an ordered maturation. Columns
of cells similar to those seen in the normal
growth plates were sometimes observed and
subsequent hyper­trophic development and
endochondral calcifica­tion of the implant were
common after 6 to 8 weeks postoperatively.
Evaluation following longer postoperative
terms showed that there was an increase in
114
vascularity at the implant sites as fibrous
stroma extending into the defect was replaced
with adipose tissue. The defect remained at
the level of the growth plate and elongated
into the metaphysis as the bone increased in
length. The early stages of de­fect extension
into the metaphysis could be seen at 4 weeks
after surgery. This is consistent with a growth
rate across the ovine proximal tibial growth
plate of approximately 1 mm/week(3). Bone
dissolution associated with an inflamma­
tory reaction in response to the implant
does not appear to contribute significantly
to the expan­sion of the defect since the upper
epiphyseal margin of the defect remains at
the level of the growth plate and shows little
evidence of erosion even after 26 weeks.
This observation is consis­tent with that of
Langenskiold et al.(9), who found that, after
resection of growth plate bone bridges and
implantations of autologous fat in pigs, large
elongated cavities of fat were formed as the
bone grew in length.
A feature of the behavior of the implanted
chondrocyte discs was their variable
survival. Whi­le some implants continued
to proliferate, neigh­boring areas showed a
loss of chondrocytes and matrix devoid of
proteoglycan. The mechanism of chondrocyte
loss and implant invasion and dis­solution
appeared to be multiple. In some areas,
extensive eosinophilic implant remmants
were present. These were frequently
adjacent to ac­tive cartilage-like implant and
were devoid of rounded chondrocytes and
proteoglycan staining matrix. In other areas,
matrix dissolution and chondrocyte lysis
were observed at the outer mar­gins of the
cartilage-like implant. Although pos­sibly
different temporal stages of the same pro­
cess, these two types of cellular invasion may
indicate different reasons for implant failure.
Chondrocytes within a normal growth plate
un­dergo a limited number of cell divisions
before they are replaced by bone. This may
 Reimplantation of growth plate chondrocytes into growth plate defects in sheep
be reflected in limited cell survival in culture
and after implan­tation. The capacity for cell
division may also de­pend upon the stage of
maturity of the chon­drocytes at isolation.
Since the source material consisted of a
heterogeneous population of cells from
all growth plate zones, it was reasonable
to expect variable cell survival in culture.
Similarly, the length of the cell culture perrod
prior to im­plantation may have influenced
subsequent im­plant vitality. Culture time in
these experiments was determined by the
time required to form a cohesive disc in vitro
and the coordination of sur­gery and the cell
culture. Experiments in progress are aimed
at optimizing proteoglycan and colla­gen
synthesis, and rate of cell division in culture,
for the maximal growth of implants within
the ex­perimental defect.
Although an immune reaction, indicated
by the presence of granulocytes and
lymphocytic cells, was observed, in most
defects the cellular response appeared to be
no greater in areas ex­hibiting implant necrosis.
However, it is likely that the necrosis was
at least partially due to this host response.
An extensive immune reaction due to the
presence of a supporting type II collagen
matrix demonstrated the capacity of this
response for implant destruction. Similarly,
Malejczyk and Moskalewski(10) have shown
a loss of chondro­c ytes after allogenic
intramuscular transplantation of freshly
isolated epiphyseal) chondrocytes in mice.
They also observed an apparent protection of
transplanted chondrocytes by the development
of a surrounding fibrous perichondrium-like
tissue similar to that reported here. Further
protection of the implanted chondrocytes
from the immune system of the host is
provided by the proteogly­can-rich cartilage
matrix accreted during cultu­re. When freshly
isolated chondrocytes were im­planted into
an experimental defect (data not shown),
an extensive infiltration of immune cells
resulted in the rapid loss of implanted cells.
In the present experiments, a lymphocytic
infiltra­te, though much smaller in extent,
was observed throughout the experimental
period and may ha­ve been a consequence of
the ongoing exposure of cell surface antigens
as the implant matrix was slowly eroded and
protected chondrocytes expo­sed. The role
of the immune reaction in suppres­sion or
destruction of implanted chondrocyte cul­tures
is currently under investigation.
The use of chondrocyte cultures labeled with
a fluorescent marker enabled the convincing
de­monstration of chondrocyte survival for 4
weeks after implantation. After this time, loss
of mar­ker, probably from dilution due to cell
division, prevented conclusive assessment of
chondrocy­te origin. However, the extent and
location of cartilage-like islands isolated from
similar host tissue strongly suggested that the
cartilage is of implant origin. At present, we
cannot exclude the possibility that these are
outgrowths of host cartilage. Such extensive
repair response in car­tilage, however, has
not been reported to date and was not seen
in control defects in the ab­sence of implaned
cultures.
ACKNOWLEDGMENT
This work was supported by grants from
the National Health and Medical Research
Council, Australia and the Adelaide Children’s
Hospital Re­s earch Trust. We would like
to tank Darren Matt­h ew, Department of
Histopathology, Adelaide Children’s Hospital
for preparing histology sec­tions, and Mr Ray
Yates, Flinder Medical Center Animal House.
REFERENCES
1. Bright R W. Further canine sludies with medical
elas­tomer X7-2320 after osseous bridge resection
for par tial physeal plate closure. Orthop Res Soc
Trans 1981;27:108.
115
B.K. Foster, A.L. Hansen,G.J. Gibson, J.J. Hopwood, G.F. Binns, O.W. Wiebkin
2. Bronner-Fraser M. Alterations in neutral crest mi
gration by a monoclonal antibody that affects cell
ad­hesion. J Cell Biol 1985;101:610-617.
3. Foster E B. Epiphyseal plate repair using fat
interpo­sition to reverse physeal deformity. An
experimental sludy. M D. Thesis, University of
Adelaide, 1989.
4. Green W T. Behaviour of articular chondrocytes
in cell culture. Clin Orthop 1971;75:248-260.
5. Gibson G J, Schor S L, Grant M E. Effect of ma­trix
macro-molecules on chondrocyte gene expression:
synthesis of a low molecular weight collagen
species by cells cultured within collagen gels. J
Cell Biol 1982;93:767-774.
6. Hansen A L, Foster B K, Gibson G J, Binns G
F, Wiebkin O W, Hopwood J J. Growth-plate
chon­drocyte cultures for re-implantation into
growth-plate defects in sheep. 1. Characterisation
of cultures. Clin Orthop 1990;256:53-65.
7. Kawabe N, Ehrlich M G, Mankin H J. Growth
plate reconstruction using chondrocyte allograft
trans­plants. J Pediatr Orthop 1987;7:381-388.
8. Langenskiöld A. Surgical treatment of partial clo­
sure of the growth plate. J Pediatr Orthop 1981;1:3-
11.
116
9. Langenskiöld A, Österman K, Valle M. Growth of
fat grafts after operation for partial bone growth
arrest: demonstration by computed tomogra­phy
scanning. J Pediatr Orthop 1987;7:389-394.
10. Malejczyk J, Moskalewski S. Effect of immu­
nosuppression on survival and growth of cartilage
pro­duced by transplanted allogenic epiphyseal
chondrocy­tes. Clin Orthop 1988;232:292-303.
11. Mizuta T, Benson W M, Foster B K, Paterson D C,
Morris L L. Statistical analysis of the incidence of
physeal injuries. J Pediatr Orthop 1987;7:518-523.
12. Monticelli G, Spinelli R. Distraction epiphysioly sis
as a method of limb lengthening 1. Experimental
study. Clin Orthop 1981;154:254-261.
13. Olin A, Creasman C, Shapiro F. Free physeal
transplantation in the rabbit: an experimental
approach to focal lesions. J Bone Joint Surg (Am)
1984;66:7-20.
14. Österman K. Operative elimination of partial
prema­ture cpiphyseal closure. An experimental
study. Acta Orthop Scand 1972;147:1-79.
15. Wiebkin O W, Muir H. Synthesis of proteoglycans
by suspension and monolayer cultures of adult
chon drocytes and de novo cartilage nodules. J
Cell Sci 1977;27:199-211.
18 Epiphyseal reconstruction: a review of a
proposal for an interface between basic
and reconstructive orthopaedic science
D.J. Zaleske
The cartilaginous cell populations at the end
of a long bone play a crucial role in articulation
and, in the immature organism, growth.
Repairing these various cell populations
malfunctioning secondary to congenital
anomalies, infection, trauma, metabolic or
endocrine problems, neoplasms, inflammation
or degeneration has been a central concern
of orthopaedic science. Understanding their
origins provides a logical framework for
organizing the rapidly proliferating knowledge
base with which orthopaedic science needs
to be concerned.
A short digression about terminology is
necessary. The nomenclature throughout
biology for long bones is the customary
epiphysis, metaphysis and diaphysis.
The epiphysis, or the entire growing end
of a long bone, has gone through various
changes phylogenetically to accomplish its
dual missions of articulation and growth in
various environments(1). The evolution of a
secondary center of ossification within the
epiphysis was an advance allowing mechanical
support of delicate cell populations devoted
to articulation and growth; epiphyses of
various types are present in all vertebrates
but secondary centers of ossification within
epiphyses tend to be seen only in mammals.
This can create semantic confusion which has
no single solution. Some investigators refer
Reprinted with permission of Mapfre Medicina (vol. 4, suppl 2)
to the secondary center of ossification as the
epiphysis(2). The growth plate or physis lies
between the secondary center of ossification
and metaphysis. The cartilage surrounding
the secondary center of ossification then may
be termed the chondroepiphysis(3). However,
there are objections which can be raised against
this mammalian view. It would imply that
non-mammalian vertebrates do not have
“epiphyses”. Further, “the appearance of an
epiphysis” radiographically in clinical science
obscures the fact that the development of a
secondary center of ossification occurs some
time after (frequently considerably after) the
embryologic for­mation of the cartilaginous
end of a long bone. For these reasons the
term epiphysis will he used in this review
for the entire end of the long bone and the
term secondary center of ossification for the
bony support which can develop within it(4-6).
The embryologic origins of the vertebrate
epi­physis require a consideration of limb
develop ment. This topic has been reviewed
previously in the orthopaedic literature(7).
An indication of the impact of molecular
biology on this field may be gleaned from a
recent review of the same to pic in the basic
science literature(8). The two processes of
early development are morphoge­nesis and
cytodifferentiation. Much of what is known
about how vertebrate limb development
117
D.J. Zaleske
accomplishes these processes comes from
work with avian species(9-17); there are obvious
ana­logies with other vertebrates including
Homo Sa­piens. Soon after the establishment
of the cranio-caudad axis of the embryo, the
limbs begin as outpouchings or buds at the
lateral body wall. The upper limbs develop
earlier than the lower limbs. The buds begin
as surface ectoderm over­lying mesoderm.
As for any three-dimensional structure,
three axes exist. For a limb, these may be
conveniently oriented as anteroposterior (AP)
the axis along which the number and type of
di­gits will be specified, dorsoventral (DV),
and pro­ximodistal (PD). While ablative and
transplanta­tion experiments of key structures
in the develo­p ing avian limb have been
conducted and fruit­fully interpreted along
these axes, the possibility that nature does not
necessarily use exactly the same axes during
morphogenesis needs to be bor­ne in mind.
Shape may be viewed as the epiphe­nomenon
which results from an interactive cas­cade of
118
Figure 1. Longitudinal section
of the developing knee
re­g ion from a fifteen-day
post-conception mouse. The
distal femoral and proximal
tibial epiphyseal regions are
evident. The mesenchymal
anlagen are transforming into
early carti­lage. Joint cavitation
is proceeding. (Hematoxylin
and eosin, X40).
processes throughout the limb bud. Early
studies in embryology established activities
of va­rious structures or tissue reqions in the
limh bud during morphogenesis. This effort
continues along with efforts to explain these
effects at the mole­cular level. Information along
the AP axis has been found to be influenced by
a region of tis­sue termed the zone of polarizing
activity (ZPA). By transplantation of this
normally posterior re­gion anteriorly, digit
duplications have been pro­duced. Retinoic
acid has received much recent attention as
an agent associated with this acti­vity(18) and
further may be working to activate a group
of genes, homeotic genes, widely distri­buted
phylogenetically in establishing body seg­
mentation(8). The growth factors seem to be
attractive candidates for establishment of
mor­phogenetic messages along the DV axis.
The pro­ximodistal or PD axis is particularly
intriguing as it is along this axis that the
segmentation occurs establishing the joints
and kinetic heterogeneity which is employed

by nature in variously adap­ting the vertebrate
limb for power, speed, dexte­rity or propulsion
through fluids. The outgrowth along the PD
axis is under the control of the spe­cialized
thickening of the surface ectoderm, the
apical ectodermal ridge or AER. Although
various paradigms have been advanced,
the precise me­chanism for the specification
of the elements along this axis has not been
established. It is known that the order of
specification is from pro­ximal to distal(10).
Condensation of mesenchy­me occurs as the
first recognizable percursors or anlagen of
skeletal elements. The condensed me­senchyme
is intially continuous. Joints from as later
embryologic early fetal events in three sta­ges:
segmentation of the continuos mesenchyme
with interzone formation; cavitation; and
development of syrnovium and intra-articular
structu­res(19). By the end of the embryologic
period, cavitation has been initiated (Fig. 1).
The ba­sic architecture of the limb has been
established. The long bones, as organs, are
entirely cartilagi­nous as tissue, absolutely
and relatively foreshor­tened in comparison
to the hand or foot. In es­sence, proximal and
distal epiphyses have been juxtaposed; growth
away from each other occurs and vascular
Epiphyseal reconstruction
Figure 2. Longitudinal section
of the developing knee re­gion
from a seventeen-day post-
conception mouse. The distal
femoral and proximal tibial
epiphyseal regions are clearly
well-formed cartilage with
histological heterogeneity. The
primary center of ossification
has also formed. (Hematoxy­lin
and eosin, X40).
invasion heralds the formation of the primary
center of ossification. While conti­nued normal
growth requires many factors inclu­ding the
appropriate mechanical environment(20),
the major aspects of morphogenesis and
cytodifferentiation of the epiphysis have been
ac­complished by the early fetal period (Fig. 2).
The cartilage of the epiphysis is functionally
he­terogeneous with separate cell populations
for articulation and growth, both longitudinal
bone growth and epiphyseal enlargement,
having been established by the events of limb
development(4).
Nutrition of the epiphysis varies with
develop­mental time and size of the organism.
Articular cartilage is avascular and remains so
throughout life(21). The cartilaginous epiphyses
of small ani­mals can remain avascular and
still survive by dif­f usion from adjacent
vessels(7,22). As the epi­physes of large animals
grow in volume, some type of canalicular
system is required to prevent this limit from
being exceeded. Cartilage canals provide this
pathway(23,24). They also provide the channels
for invasion by a more aggressive vascular
tissue heralding the formation of the se­condary
center of ossification (Fig. 3). For Ho­m o
Sapiens, this is usually a post-natal event
119
D.J. Zaleske
with the exception being the distal femoral
secondary center of ossification occurring at
thirty-six weeks of gestation.
A variety of pathological conditions,
familiar to orthopaedic clinicians result
from alterations in the various chondrocytic
populations of the epi­physis at different times
of life. Attempts at re­pair or reconstruction
of these conditions have limitations. One
common change is degeneration of the
articular cartilage(25). In focal lesions, one
therapeutic approach is drilling of the defect to
allow vascular ingress from the subchondral
bone and transport of mesenchymal cells into
the region. This solution is less than perfect
because the fibrocartilage so produced does
not have the desired wear characteristics of
innate hyaline car­tilage. The addition of motion
favorably affects this cytodifferentiation(26). The
use of mesench­ymal stem cells thus enriching
the population of cells participating in healing
is an exciting con­cept with the potential of
being an important in­terface between basic
biology and reconstructi­ve surgery(27).
Tne problems encountered when
attempting to reconstruct the growing
epiphysis are yet more numerous. The
proliferating cartilage of the epi­physis has
a controlled kinetic program(28-30). Nature
120
Figure 3. Longitudinal section
of the distal femoral epi­physis
from an eleven-day post-natal
mouse. The secondary center
of ossification has now formed.
(Hematoxylin and eosin, X40).
has apparently installed many regulators of
controlled growth and safeguards against
un­controlled growth(31-38). Influencing the
proli­ferating cartilage of an epiphysis has not
proved as facile as an orthopaedic surgeon
would desire(39,40). The corollary of the focal
articular carti­lage lesion in proliferating
cartilage is the physeal bar. If small, the physeal
bar is a tether interfe­ring with the kinetic
program of the surrounding intact growth
plate. Resection and replacement with inert
fillers is the present solution, limited by the
requirement that at least fifty percent of the
growth plate (and probably more) must be
intact for the untethering to allow growth(41).
Focal replacement of the resected physeal
region with cartilage has been attempted
experimentally(42,43). It is still unclear whether
or not this transplanted cartilage, providing
a block to vas­cular invasion and reformation
of the bar, is also providing a cell population
to participate in ki­netic activity. Further,
even if the transplanted cartilage and some
kinetic activity, it might not match that of
the remaining physeal cartilage fo­llowing
untethering.
A more global involvement of the
proliferating and articular chondrocytic
populations of the epi­physis would require

tissue of appropriate mor­p hogenesis,
cytodifferentiation and immunologi­c al
compatibility for repair. While the immuno­
logy of articular cartilage may allow allogeneic
transplantation(44), allogeneic proliferating
car­t ilage does not fare well (45,46). Under
clinical circumstances, the proximal fibular
epiphysis is the only long bone epiphysis which
would usually be available for heterotopic
transplantation. The­se constraints have guided
experimental work. Under experimental
circumstances, epiphyseal transplantation
has been investigated with seve­ral models
at least since the turn of the century(47). The
advent of microvascular surgical tech­niques
have allowed transplantation of epiphyses with
secondary centers of ossification on vascu­
lar pedicles(48-55), a subject which has been
re­viewed in detail(56,57). While a predictable
tech­nology for clinical transplantation has
yet to be developed, several general trends
seem to be evol­v ing. When an epiphysis
has a secondary center of ossification and
thus a vascular supply, re-es­tablishment of
this vascular supply is necessary (although
not sufficient) for survival and func­tion of
proliferating cartilage(49,58). Replanta­tion of
a joint or contralateral transplantation of an
isolated epiphysis have given encouraging
re­sults when measuring growth(52), but hetero­
topic transplantation with the associated
problems of ligamentous reconstruction
and incongruity of an immature joint have
not proven as encoura­g ing (53). This set of
circumstances would seem to constitute a
formidable barrier to the develop­ment of an
interface between the basic science of limb
development and biologic reconstructive
surgery of the epiphysis. Autogeneic or synge­
neic tissue of appropriate morphogenesis
and cytodifferentiation are desirable yet are
limited or unavailable for Homo Sapiens or
any non-in­bred species.
Regeneration holds great fascination. Limb
re­generation in urodele amphibians bears
Epiphyseal reconstruction
striking resemblance to limb development
yet the possi­b ility exists that they are
different processes. Re­generation has also
been reviewed in the ortho­paedic literature(59)
and again, a more recent review in the basic
science literature reflects the enormous
impact of molecular biology in inves­tigating
this phenomenon(60). Even with this rapid
expansion in knowledge, epimorphic rege­
neration of an entire mammalian limb appears
remote. Yet development or regeneration of
an epiphysis or a joint can be investigated
in a very meaningful fashion at the present
time. That leads to a proposal for a focus
of effort by orthopaedic science, both basic
and reconstructive. For the former, what is
the mechanism for the morpho­genesis and
cytodifferentiation, including the ki­netics,
of epiphyses and how could this be reca­
pitulated in vitro utilizing chondrocytes(61) or
stern cells(27) from an organism for later trans­
plantation back into the same organism? For
the latter, if autogeneic or syngeneic epiphyses
or parts of epiphyses were available how might
they be employed in reconstructive surgery?
Such an interface among many workers will be
necessary to solve the biologic reconstruction
of epiphyses in the general case.
Several variations of epiphyseal
reconstruction in a murine model have been
conducted(62-66). These studies are not presented
as the solution to epiphyseal transplantation
but rather as a sti­mulus to further work into
the question of the use of syngeneic epiphyses
in reconstructive surgery. Inbred strains of
mice are readily available so syngeneic tissue
of varying developmental time exists for use
in experimental surgery. The mou­se suffers
from being small but it is the best known
model for mammalian development(67,68). Its
distal femoral and proximal tibial epiphy­ses
only become vascularized post-natally(69) and
allow non-vascularized transplantation(66). The
results of non-vascularized transplantation are
clearly variable, if growth is used as the para­
121
D.J. Zaleske
meter of success, but when one considers that
resection of an immature joint in a mammal
post­natally leaves a fibrous ankylosis with
no organi­zed growth from this tissue, the
production of structures by various modes of
transplantation is part of the iterative process
of the above pro­posal. Physeal regions(32,62,64),
hemiephyses(65) or entire epiphyses(66) can
be replaced in mice with syngeneic tissue
of normal or altered morphogenesis or
cytodifferentiation. From the basic science
side of the interface, work is being describing
the behavior of murine tissue in the developing
limb bud of the chick(70-72). If this chimeric
combination can be refined so that the limb
bud of one species can produce epiphyses of
appropriate morphogenesis and cytodifferen­
tiation for another, the proposal for biologic
re­pair of epiphyses comes closer to realization.
Would enormous amount of work remain?
Un­questionably, it would, including a great
deal of large animal work prior to clinical
application. Ho­wever, organizing the work
as proposed should give both orthopaedic
basic scientists and clini­cians something about
which to talk and get ex­cited together.
REFERENCES
1. Hinchliffe J R, Johnson D R. The Development of
the Vertebrate Limb. Oxford: Clarendon Press,
1980; 39-40, 85-80, 228.
2. Brighton CT. Longitudinal bone growth: the growth
plate and its dysfunctions. In: Griffin P P (ed).
Instruc­tional course lectures XXXVI. Park Ridge,
IL: Ameri­can Academy of Orthopaedic Surgeons,
1987;3-25.
3. Carter DR, Wong M. Mechanical stresses and en
dochondral ossification in the chondroepiphysis.
J Or­thop Res 1988;6:148-154.
4. Diao E, Zaleske DJ, Avella D, et al. Kinetic
and biochemical heterogeneity in vertebrate
chondroepi­physeal regions during development.
J Orthop Res 1989;7:502-510.
122
5. Mckibbin B. The structure of the epiphysis. In:
Owen R, Goodfellow J, Bullough P (eds). Scientific
Founda­tions of Orthopaedics and Traumtology.
Philadelphia: W B Saunders, 1980:169-175.
6. Shapiro F. Epiphyseal disorders. N EnglJ Med
1987;317:1702-1710.
7. Amprino, R. The development of the vertebrate
limb. Cliln Orthop 1984;188:263-284
8. Tabin CJ. Retinoids, homeoboxes, and growth
fac tors: toward molecular models for limb
development. Cell 1991;66:199-217.
9. Maccabe JA, Saunders JW Jr, Pickett M. The control
of the antero-posterior and dorso-ventral axes in
embryonic chick limbs constructed of dissociated
and re-aggregated llmb bud mesoderm. Dev Biol
1973;31:323.
10. Saunders JW Jr. The proximo distal sequence of
origin of the parts of the chick wing and the role
of ectoderm. J Exp Zool 1948;108:363.
11. Saunders JW Jr. The experimental analysis of chick
limb bud development. In: Ede DA, Hinchliffe
JR, Balls M (eds). Vertebrate limb and somite
morphoge­nesis. Cambridge: Cambridge University
Press, 1977; 1-24.
12. Saunders JW Jr. Developmental biology. New
York: MacMillan, 1982;476-482.
13. Saunders JW Jr, Cairns JM, Gasseling MT. The role
of the apical ridge of ectoderm in the differen­tiation
of the morphological structure and inductive
specificity of limb parts in the chick. J Morphol
1957;57:101.
14. Saunders JW Jr, Gasseling MT. Transfilter pro­
pagation of apical ectodermal maintenance factor
in the chick embryo wing bud. Dev Biol 1963;7:64.
15. Saunders JW Jr, Gasseling MT, Cairns JM. The
differentiation of prospective thigh mesorderm
grafted beneath the apical ectodermal ridge of the
wing bud in the chick embyo. Dev Biol 1959;1:281.
16. Saunders JW Jr, Gasseling MT, Gfeller MD.
Interaction of ectoderm and mesoderm in the
origin of axial relationships in the wing of the
fowl. J Exp Zool 1958;137:39.

17. Zwilling E, Saunders JW Jr, Gasseling MT.
Involvement of the apical ectodermal ridge in
chick !imb development. Anat Rec 1960;136:307.
18. Thaller C, Eichele G. Isolation of 3,4-didehydro­
retinoic acid, a novel morphogenetic signal in
the chick wing bud. Nature 1990;345:815-819.
19. Sledge CB, Zaleske DJ. Developmental anatomy of
joints. In: Resnick D, Niwayama G (eds). Diagnosis
of bone and joint disorders. Philadelphia: W B
Saun­ders, 1988:604-624.
20. Drahman DB, Sokoloff L. The role of move­
ment in embryonic joint development. Dev Biol
1966;14:401.
21. Mankin HJ. The reaction of articular cartilage
to in­jury and osteoarthritis. N Engl J Med
1974;291:1285­-1292.
22. Österman K. Operative elimination of partial
prema­ture epiphyseal closure. An experimental
study. Acta Orthop Scand (supplJ 1972, 147.
23. Chadpard D, Alexandre C, Riffat G. Uncalcified
cartilage resorption in human fetal cartilage canals.
Tissue Cell 1986;18:701-707.
24. Ganey TM, Love SM, Ogden JA. Development
of vascularization in the chondroepiphysis of the
rab­bit. J Orthop Res 1992;10:496-510.
25. Mankin HJ. The response of articular cartilage
to mechanical injury. J Bone Joint Surg (Am)
1982;64:460-466.
26. Salter RB, Simmonds DF, Malcolm BW, Rumble
EJ, Macmichael D, Clements ND. The biological
effect of continuous passive motion on the healing
of full-thickness defects in articular cartilage. J
Bone Joint Surg (Am) 1980;62:1232-1251.
27. Caplan AI. Mesenchymal stem cells. J Crthop Res
1991;9:641-650.
28. Kember NF. Cell divisions in endochondral ossifica
tion: a study of cell proliferation in rat bones by
the method of tritiated thymidine. J Bone Joint
Surg (Br) 1960;42:824-839.
29. Kember NF. Cell population kinetics of bone
growth: the first ten years of autoradiographic
Epiphyseal reconstruction
studies with tri­tiated thymidine. Clin Orthop
1971;76:213-230.
30. Kember NF. Cell kinetics and the control of growth
in long bones. Cell Tissue Kinet 1978;11:477-485.
31. Breur GJ, Farnum CE, Padgett GA, Wils­man NJ.
Cellular basis of decreased rate of longitudi­nal
growth of bone in pseudoachondroplastic dogs.
J Bone Joint Surg (Am) 1992;74:516-528.
32. Centrella M, McCarthy TL, Canalis E. Trans­
forming growth factor-beta and remodeling of
bone. J Bone Joint Surg (Am) 1991;73:1418-1428.
33. D’Ercole AJ, Applewhite GT, Underwood LE.
Evidence that somatomedin is synthesized by
multi­ple tissues in the fetus. Dev Biol 1992.
34. Hinchliffe JR, Johnson DR. Growth of cartila­ge.
In: Hall BK (ed). Cartilage, vol. 2. New York:
Aca­demic Press, 1983;255-295.
35. Trippel SB. Growth plate regulation: the somatome­
dins. Pathol Immunopathol Res 1988;7:43-47.
36. Underwood LE, D’Ercole AJ. Insulin and insu­
lin-like growth factors/somatomedins in fental
and neo­natal development. Clin Endocrinol Metab
1984;13:69-89.
37. Wilby OK. A model for the control of limb
growth and development. In: Ede DA, Hinchliffe
JR, Balls M (eds). Vertebrate limb and somite
morphogenesis. Cam­bridge: Cambridge University
Press, 1977;229-244.
38. Wolpert L. Cellular basis of skeletal growth during
development. Br Med Bull 1981;37:215-219.
39. Armstrong PF, Brighton CT. Failure of the rabbit
tibial growth plate to respond to the long-term
application of a capacitively-coupled electrical
field. J Orthop Res 1986;4:446-451.
40. Elmer EB, Ehrlich MG, Zaleske DJ, Polsky C,
Mankin HJ. Chondrodiatasis in rabbits: a study of
the effect of transphyseal bone lengthening on cell
division, synthetic function, and microcirculation
in the growth plate. J Pediatr Orthop 1992;12:181-
190.
41. Ogden JA. The evaluation and treatment of partial
123
D.J. Zaleske
physeal arrest. J Bone Joint Surg (Am) 1987;69:1297-
1302.
42. Lalanandham T, Ehrlich MG, Zaleske DJ, Deeney
V F, Mankin H J. Viability and metabolism of
cartilage transplanted to physeal regions. J Pediatr
Orthop 1990;10:450-458.
43. Olin A, Creasman C, Shapiro F. Free physeal
transplantation in the rabbit: an experimental
approach to focal lesions. J Bone Joint Surg (Am)
1984:66:7-20.
44. Tomford WW. Biologic characteristics of articular
cartlage allografts. In: Friedlaender GE, Goldberg
VM (eds). Bone and Cartilage Allografts. Park
Ridge, IL: American Academy of Orthopaedic
Surgeons, 1991;37-43.
45. Ford DJ, Gerber S, Green CJ. Epiphyseal growth
after vascular free transfer using the juvenile rabbit
knee as an experimental model: a comparison
of growth in autografts and allografts using
cyclosporin A for im munosuppression. J Bone
Joint Sorg (Br) 1987;69:495.
46. Harris WR, Martin R, Tile M Transplantation of
epiphyseal plates. An experimental study. J Bone
Joint Surg (Am) 1965;47:897-914.
47. Helferich H. Versuche uber die Transplantation des
Intermediarknorpels wachsender Rohrenknocken.
Dtsch Z Chil 1989;51:564-573.
48. Brown K L B, Cruess R L. Bone and cartilaye
trans plantation in orthopaedic surgery. J Bone
Joint Surg (Am) 1982;64:270-279.
49. Brown KLB, Marie P, Lyszakowski T, Da­niel R,
Cruess RL. Epiphyseal growth after free fibular
transfer with and without microvascular anas­
tomosis. J Bone Joint Surg (Br) 1983;65:493-501
50. Gotfried Y, Yaremchuk MJ, Randolph MA, Weiland
AJ. Histological characteristics of acute re­jection
in vascularized allografts of bone. J Bone Joint Surg
(Am) 1987;69:410-425.
51. Klines C, Hotchkiss RN, Randolph MA, Weiland
A J. Study of growth kinetics and morphology in
limbs transplanted between animals of different
ages. Plast Reconstr Surg 1990;85:273-280.
124
52. Nettelblad H, Randolph MA, Weiland A. Free
microvascular epiphyseal-plate transplantation.
J Bo­ne Joint Surg (Am) 1984;66:1421-1430.
53. Nettelblad H, Randolph MA, Weiland A. He­terotopic
microvascular growth plate transplantation of the
proximal hbula: an experimental canine model.
Plast Reconstr Surg 1986;77:814-820.
54. Nettelblad H, Randolph MA, Weiland AJ.
Physiologic isolation of the canine proximal
fibular epi­physis on a vascular pedicle. Microsurg
1984;5:98­101.
55. Teot L. Les transferts osseux libres vascularises
avec cartilage de croissance. Rev Chir Orthop
1982;68(II):40-42.
56. Bowen V. Experimental free vascularized
epiphyseal transplants. Orthopedics 1986;9:893-898.
57. Zaleske DJ. Biology of epiphyseal transplantation.
In: Friedlaender G E, Goldberg V M (eds). Bone
and Canilage Allografts. Park Ridge, IL: American
Academy of Orthopaedic Surgeons, 1991;27-36.
58. Zaleske DJ, Ehrlich MG, Piliero C, May JW Jr,
Mankin HJ. Growth-plate Behavior in Whole
Joint Replantation in the Rabbit. J Bone Joint Surg
(Am) 1982;64A:249-258.
59. Bucholz RW, Ogden JA. Patterns of ischemic
ne­crosis of the proximal femur-non operatively
treated congenital hip disease. In: The hip:
Proceeding of the sixth open scientific meeting
of the hip society. St. Louis: C V Mosby, 1978;43-
63.
60. Stocum DL. Limb regeneration: a call to arms
(and legs). Cell 1991;67:5-8.
61. Moskalewski S. Transplantation of isolated chon­
drocytes. Clin Orthop 1991;272:16-20.
62. Barr SJ, Zaleske DJ. Physeal reconstruction with
blocks of cartilage of varying developmental time.
J Pediatr Orthop 1992;12:766-773.
63. Barr SJ, Zaleske DJ, Mankin HJ. Physeal
re­c onstruction with cultured chondrocytes
of varying de­velopmental time. J Orthop Res
1993;11:10-19.

64. Cundy PJ, Jofe M, Zaleske DJ, Ehrlich MG, Mankin
H J. Physeal reconstruction using tissue do­nated
from early post-natal limbs in a murine model. J
Orthop Res l991;9:360-366.
65. Wolohan MJ, Zaleske DJ. Hemiepiphyseal
re­construction using tissue donated from fetal
limbs in a murine model. J Orthop Res 1991;9:180-
185.
66. Zaleske DJ, Floyd WE, III, Hallett J, et al.
Epiphyseal replacement using developing tissue
donors in a murine model: a combined histological
and radio­graphic study. J Orthop Res 1988;6:155-
165.
67. Hanahan D. Transgenic mice as probes into com­
plex systems. Science 1989;246:1265-1275.
68. Jaenisch R. Transgenic animals. Science
1988;240:1468.
Epiphyseal reconstruction
69. Floyd WE, III, Zaleske DJ, Schiller AL, Tra­han C,
Mankin HJ. Vascular events associated with the
appearance of the secondary center of ossification
in the murine distal femoral epiphysis. J Bone Joint
Surg (Am) 1987;69A:185-190.
70. Cairns JM. Evidence for the operation of a growth
control system in the limb buds of the mouse
embryo similar to the chick embryo. Anat Rec
1959;134:543.
71. Cairns JM. Development of grafts from mouse
em­bryos to the wing bud of the chick embryo.
Dev Biol 1965;12:36-52.
72. Izpisua-Belmonte JC, Brown JM, Crawley A,
Duboule D, Tickle C. Hox-4 gene expression in
mouse/chicken heterosoecific grafts of signalling
re­g ions to limb buds reveals similarities in
patterning me­chanisms. Development 1992;115:553-
560.
125
19 Vascularised epiphyseal plate
transplantation
C.V.A. Bowen, P.W. Bray and M.I. Boyer

Damage to the epiphyseal plate from tumour,

trauma, infection or congenital malformation
may result in abnormal growth and deformity
of limb length, angulation, and rotation. The
number of clinical cases (Fig. 1) is not large,
but the burden is heavy because each patient
is faced with a lifelong challenge.
Cancellous bone grafts, non-vascular
cortical allografts, vascularized bone and
composite tissue transfers, distraction
osteogenesis and commercially manufactured
implants all have differing roles in the
management of limb segment deformity and
deficiency. Each has been developed and
used to solve clinical problems in paediatric
orthopaedics. None of these techniques,
however, achieve the ideal solution of
resolution of the presenting clinical problem
followed by continued growth in length to
maturity. The ability to use vascularised
epiphyseal plate transplantations provides
surgeons with a novel biological solution with
the potential for not only correcting deformities
but also for giving the patient with a new and
viable epiphyseal plate to provide ongoing
growth in length in the damaged bone. Figure 1. PA radiograph of the right wrist in a
child with an old injury which caused growth
A considerable amount of knowledge
arrest in the distal ulna epiphyseal plate. The distal
concerning the behaviour of epiphyseal plate radius epiphyseal plate is still open. The limb
transplants has now been accumulated from has become deformed as a result of asymmetric
years of experimental laboratory research growth, and the wrist lacks skeletal support on
and a small number of clinical cases(1,2,10). the ulna side.

126

Researchers have studied epiphyseal plate
vascularity, methods for maintaining viability
after transplantation, the feasibility of using
this technique to solve clinical problems, and
a variety of factors that need to be understood
for the optimum application of this technique(2).
Epiphyseal plate transplantation is now being
used in clinical practice with very satisfactory
results. Epiphyseal plates are, functionally and
anatomically, a unique and fascinating donor
material. In order to realize the full potential
of epiphyseal plate transplantation, however,
there are still many questions to be answered
and problems to be resolved.
The purpose of this paper is to review
(a) the development of epiphyseal plate
transplantation, (b) the current status of
clinical epiphyseal plate transplantation, (c) the
nomenclature, (d) the experimental studies with
vascularised epiphyseal plate transplants, (e)
the future of epiphyseal plate transplantation.
THE DEVELOPMENT OF
VASCULARISED EPIPHYSEAL PLATE
TRANSPLANTATION
The first experimental reports of free non-
vascularized epiphyseal plate transplants date
back to the nineteenth-century literature(1,2,10).
A number of different animal models and
experimental designs were used. Although
some of the studies produced encouraging
results, in general the longitudinal growth
produced by the transplants was unpredictable
and usually not very good. The varying results
could be attributed to a variety of factors (e.g.
differing experimental animals, surgical
techniques, experimental design etc), but the
biggest factor contributing to variability of
results was the inability to adequately ensure
the post-operative viability of the transplants.
Non-vascularized epiphyseal plate
transplants have to completely rely on the
diffusion of nutrients from the surrounding
graft bed for their survival. Unfortunately
Vascularised epiphyseal plate transplantation
they are strikingly sensitive to ischaemia(32,58,59),
which, if mild, will cause growth retardation
and, if severe, will lead to necrosis and growth
arrest. The early investigators did not initially
appreciated this problem, but, once it was
recognized, the main thrust of research became
directed at ways in which ischaemia could
be minimized and viability could be best
maintained in the peri-operative and post-
operative periods. The difficulties facing early
investigators can clearly be seen by looking
at the results of Harris’s experiment(30). In this
study an attempt was made to improve post-
operative viability by reducing the thickness
of the bony portion of the epiphyseal plate
transplants. The investigators hoped that this
technique would allow for better diffusion
of nutrients to the epiphyseal plate. Results,
however, showed unequal vascular ingrowth
into the bony portion of the transplants and
variable post-operative growth. Although
quite good results were achieved in some of
the experimental animals, there was a lot of
variation between experimental groups and,
often, even within the same experimental
group. Unreliable growth after transplantation,
therefore, made non vascularised transplants
unsatisfactory for clinical use.
Tackling the problem of post-operative
ischaemia by making grafts smaller lead to a
divergence in the way that epiphyseal plate
transplantation research has developed. Some
investigators have continued to experiment
with the transplantation of small grafts of
epiphyseal plate material. Others (including
ourselves) have used microvascular techniques,
which can satisfactorily maintain viability
in large blocks of transplanted tissue. The
use of large revascularised transplants has
the advantage that a recipient site bone
reconstruction can be made at the same that
the epiphyseal plate is introduced. In order
to achieve a good structural reconstruction, it
is necessary for the graft to include segments
of metaphyseal and epiphyseal bone large
127
C.V.A. Bowen, P.W. Bray, M.I. Boyer
enough to hold orthopaedic fixation devices.
This kind of graft needs to be considerably
larger than the small grafts used in the early
non revascularised transplants, and grafts of
this size must be immediately revascularised if
they are to maintain their structural integrity
and continue to grow in length.
Microvascular surgical techniques have
been used for transplanting large blocks of
tissue since the 1960s. The first microvascular
procedures were replantations of traumatically
amputated parts - usually digits in the
hand. Subsequently elective microvascular
transplantations, known as free tissue transfers,
have been used for the reconstruction of soft
tissue defects, skeletal defects, and composite
tissue defects with ideal donor tissue and
reliable post-operative viability. Using
microvascular techniques, it has been shown
that predictable post-operative viability can be
achieved in epiphyseal plate transplants(1,2,10).
Experimental and clinical research have
continued to progress simultaneously.
Experimental research has lead to increased
understanding of post-operative function in
revascularised epiphyseal plate transplants.
Clinical studies have documented success
in managing a number of different types of
patient problems using this technique.
CURRENT STATUS OF
CLINICAL EPIPHYSEAL PLATE
TRANSPLANTATION
The initial experience with the
revascularisation of growing bone segments
was with replantation. The first successful
clinical cases of extremity revascularisation
and replantation were done in the 1960s. The
technique rapidly caught on throughout the
world and it was not long before many cases
were recorded. In replantations done in children
(Fig. 2), surgeons found that epiphyseal plates
remained open post operatively and continued
to grow in length(19,26,51,52).
128
Figure 2. Clinical photograph taken several months
after a successful thumb replantation in a young
child. Radiographically the epiphyseal plates were
still open and the thumb continued to grow in length.
In other cases, epiphyseal plates have been
revascularised as part of composite grafts in
elective free tissue transfer procedures. In toe
to hand transfers, done in children(27,40,51,66) for
the reconstruction of congenital anomalies or
mutilating injuries to the hand, epiphyseal
plates remain open and grow in length in
the same way that they do after replantation.
Similarly, the epiphyseal plates in vascularised
joint transfers in children(33,53,67) maintain their
radiographic appearance and continue to grow
in length after transplantation. Nowadays,
the main indication for vascularised joint
transplantation is a child with damage to a
joint and adjacent epiphyseal plate in the hand.
Vascularised joint transplantation is the only
available procedure that can provide a long
term solution for this combination of problems.
In theory, revascularised epiphyseal plate
transplants could form the ideal solution to a
wide variety of clinical problems, particularly
those involving congenital absence of an
epiphyseal plate or damage or destruction of
an epiphyseal plate at an early age. Unlike
conventional limb lengthening techniques,
a revascularised epiphyseal plate transplant
should maintain its ability to grow and
produce longitudinal bone growth until it
reaches maturity and fuses. A number of cases

of skeletal reconstruction with vascularised
epiphyseal plate transplants have recently
been described(15-17,34,55,61,64,65). Although the
technique is still in its infancy and long term
results are not yet available, early results look
promising and the transplants have provided
a satisfactory solution for clinical problems.
Vilkki(65) has combined the use of vascularised
epiphyseal plate transplantation with distraction
lengthening for the treatment of radial club hand.
Innocenti(34) has elegantly demonstrated that the
use of revascularised free bone grafts containing
epiphyseal plates from the proximal fibula in
children is probably the best way to reconstruct
the distal radius and proximal humerus in
cases where skeletal defects are created in
these areas after tumour resection. Chung(17)
has also transplanted revascularised proximal
fibula epiphyseal plates for the reconstruction
of wrists, ankles and knees in children with
growth disturbances resulting from trauma,
tumours and congenital anomalies.
The main problem with clinical epiphyseal
plate transplants is the lack of suitable donor
sites. The only satisfactory options are the
proximal fibula, a metatarsal, or a toe phalanx.
The potential use of allograft donor sites,
therefore, is very attractive, but they have
the drawback that immunosuppression is
necessary to prevent rejection. Currently
available immunosuppressant drugs are too
toxic(18) to justify their long term use in clinical
non life threatening skeletal reconstruction
procedures. At the present time, therefore,
the use of allograft donor sites is restricted to
the research laboratory where investigators
are investigating some of the questions
that will be posed by the future use of this
material. No clinical cases of vascularised
allograft epiphyseal plate transplantation
have been reported, although Doi (20) has
described a clinical case of vascularised bone
transplantation, in which an adult fibula was
transplanted into a child with congenital
pseudarthrosis of the tibia.
Vascularised epiphyseal plate transplantation
Figure 3. A radiograph taken two months after
a dog’s distal ulna epiphyseal plate has been
transplanted as an autogenous orthotopic transplant
(i.e. removed and then transplanted back into its
original donor site). Note that union has occurred
at both the proximal osteosynthesis, where the graft
contained sufficient diaphyseal and metaphyseal
bone for plate fixation, and also at the distal
osteosynthesis where the epiphysis did not provide
sufficient bone for a plate and so skeletal fixation
was achieved with an adequate, but less satisfactory,
interosseous wire loop technique.
CLARIFICATION OF NOMENCLATURE
It has been pointed out that the term
‘epiphyseal plate transplantation’ is, strictly
speaking, not correct. This is true, as the
transplants are really vascularised composite
tissue grafts containing not only the epiphyseal
plate but also adjacent epiphyseal and
metaphyseal bone (Fig. 3).
It is essential to revascularise the adjacent
bone in order to achieve post-operative
viability in the epiphyseal plate transplants
revascularised using microsurgical techniques.
As it is possible to include quite large bony
segments in revascularised grafts, this
technique allows skeletal reconstruction to
be done at the same time as epiphyseal plate
transplantation. In addition, the inclusion
of these bone segments allows for adequate
internal fixation of the grafts without the
skeletal fixation device interfering with the
transplanted epiphyseal plate.
Although it might be more correct
terminology to call the grafts ‘vascularised
129
C.V.A. Bowen, P.W. Bray, M.I. Boyer

immature bone transplants’, the term

‘epiphyseal plate transplants’ is the one
that is commonly used and now generally
accepted.

EXPERIMENTAL STUDIES WITH

VASCULARISED EPIPHYSEAL PLATE
TRANSPLANTS
A large number of papers have now been
published describing studies that were done
to investigate a variety of aspects epiphyseal
plate transplantation. In 1994 Boyer(10) reviewed
the literature and classified experiments into
groups according to the kind of manipulation
that the epiphyseal plates had experienced:
A) Studies into the transplantation of non-
revascularised epiphyseal plates
B) Studies into the transplantation of
revascularised epiphyseal plates
1) Local vascular studies on unmanipulated
epiphyseal plates.
2) Studies of epiphyseal plate behaviour after Figure 4. In this gross section of a dog distal ulna
orthotopic transplantation. epiphyseal plate transplant the interosseous artery,
3) Studies of epiphyseal plate behaviour after which acts as the donor vascular pedicle in this
heterotopic transplantation. model, has been injected with latex. The diaphysis
4) Studies of epiphyseal plate behaviour after is at the top, the epiphyseal plate is located where
allograft transplantation. the specimen widens, and the epiphysis is at the
bottom of the illustration. The donor vascular pedical
Boyer’s first subgroup of revascularised can be seen coursing vertically downwards close to
studies contained experiments in which the periosteum of the diaphysis and metaphysis. It
epiphyseal plates were left in situ and bifurcates close to the epiphyseal plate and provides
were subjected to vascular studies (Fig. 4) periosteal vessels which supply the epiphysis, the
without being transplanted. The other three metaphysis, and the perichondrium around the
subgroups all consisted of experiments in epiphyseal plate. After transplantation, the whole
system can be revascularised microsurgically by
which epiphyseal plates had been transplanted
anastomosing recipient site vessels to the donor
with microsurgical revascularisation, and vascular pedicle in the diaphyseal region, where
experiments were allocated to a specific group the arterial diameter is about 1mm. (Actual length
according to the type of manipulation that the of photographed specimen was 4.1cm).
epiphyseal plates had undergone.

Autogenous epiphyseal plate transplants orthotopically focused on the effects of a number

revascularized in orthotopic sites (i.e. in their of different variables. Early experiments in this
normal anatomic location) group investigated the viability of epiphyseal
Investigations into the behavior of plates after they had been transplanted and
autogenous epiphyseal plates revascularized revascularised as microsurgical free tissue

130

transfers(5,14,21,22,47,68). Other experiments(4,8,63)
studied the vascularity of the transplants in more
detail, specifically by transplanting epiphyseal
plates with incomplete revascularisation. The
effect of devascularising either the epiphyseal or
metaphyseal circulations was examined(4,63), and
the effect of excluding the nutrient artery was
also investigated(8). Results demonstrated that,
using microvascular techniques, epiphyseal
plate transplants remain viable and continue
to grow in length after transplantation (Fig.
3), but that revascularisation of both the
epiphyseal and metaphyseal circulations (Fig.
4) was necessary for a satisfactory outcome.
It was found, however, that growth rates
were almost always less than in unoperated
controls. Exclusion of the main nutrient artery,
which occurred in all experimental models,
produced no noticeable effect on growth in the
long term (after about one month), although
histological specimens examined soon after
transplantation(6) did demonstrate features of
delayed ossification in the central part of the
epiphyseal plates.
The growth potential of an epiphyseal plate
transplant is a not only a function of growth
rate but also of the time over which growth
occurs. Almost all the experimental studies
have expressed the results as growth rates,
and therefore we carried out an experiment(7)
in which transplants were followed to skeletal
maturity. In this study there was no statistically
significant difference in the time of growth
arrest and epiphyseal plate fusion between
the experimental and control groups.
It has been important to study the effect
of ischaemia on epiphyseal plate transplants
because it is well recognized that they are very
sensitive to ischaemia and because microsurgical
transplantations cannot be done without at
least a short period of ischaemia. Hou(32),
who replanted immature extremities in rats,
emphasized the importance of revascularising
transplants as quickly as possible. Stark(59) and
Shimizu(58) have specifically investigated the
Vascularised epiphyseal plate transplantation
effect of ischaemia in experimental animals. Both
investigations demonstrated that epiphyseal
plate transplants can tolerate short periods of
ischaemia satisfactorily, although progressively
greater ischaemic times were associated with
increasing structural and growth abnormalities.
Both experiments showed that there was more
than enough time to microsurgically transplant
and revascularise transplants before loss of
growth potential from ischaemia became a
problem.
Another group of reports that can been
classified in this group consist of descriptions of
various techniques that have been specifically
developed to facilitate further research in this
field. Nolan(50) described an improved method
of skeletal fixation in the rabbit knee model in
order to decrease the risk of fixation failure
in long term studies. Stevens published a
description of the rabbit second metatarsal
model(60), which he developed in order to have
a model with different growth potential from
the epiphyseal plates in the rabbit knee model.
Autogenous epiphyseal plate transplants
revascularized in heterotopic sites (i.e. in sites
other than their normal anatomic location)
Once it was shown that epiphyseal plate
transplants could be done with predictable
post-operative viability using microvascular
techniques, research progressed to examine
the behaviour of transplants in the kind of
situations that were expected to arise clinically.
Investigators realized that the only situation
in which orthotopic transplantations would be
done was in patients undergoing replantation of
amputated parts. In reconstructive procedures,
in which epiphyseal plates would be part of
a free tissue transfer, the recipient site would
almost universally be heterotopic.
Teot(62) published the results of an interesting
experiment in which he transplanted part of
the iliac crest apophysis to a recipient site
in the ipsilateral distal femoral epiphyseal
plate, using an immature dog model. His
131
C.V.A. Bowen, P.W. Bray, M.I. Boyer
results were difficult to interpret for a number
of reasons, but he did demonstrate that
chondrocyte viability was maintained after
heterotopic transplantation. This early study
quite clearly demonstrated the need for more
detailed investigation of the post-operative
behaviour of epiphyseal plate transplants.
In our own laboratory, we demonstrated
that very satisfactory results could be achieved
when a distal ulnar epiphyseal plate transplant
was used to replace a distal radius epiphyseal
plate (Fig. 5) in an immature dog model(5). In
this model, the growth potential of the donor
epiphyseal plate was similar to that needed at
the recipient site. In human clinical situations,
however, it is unlikely that the growth potential
at the donor site would ever be such a good
match for that needed at the recipient site.
In order to accurately predict the growth
potential of transplants placed in heterotopic
locations it will be necessary to find answers
to a number of questions. For instance, Do
changes in biomechanical loading produce
altered growth potential? Will the longitudinal
growth achieved by transplants be similar to
that of their normal donor site or will their
growth potential change and be more like
that of their new recipient site location? What
would happen if a bone contained more than
its normal number of epiphyseal plates?
The literature contains three papers
describing experiments designed to investigate
the behaviour of microsurgically revascularised
epiphyseal plate transplants in altered loading
conditions(3,13,46). In each case the experimental
results were difficult to interpret, strongly
suggesting that the effect of loading is complex
in the type of transplant models studied.
Clearly a lot more work needs to be done in this
area before we achieve a clear understanding
of the behaviour of these transplants under
differing loading conditions.
Three studies have been published
describing experiments designed to investigate
the feasibility of increasing the length of a
132
Figure 5. Diagrammatic representation of our own
laboratory experiments in which revascularised
dog distal ulna epiphyseal plate transplants were
either used to replace an adjacent distal radius
epiphyseal plate or used to provide an extra
accessory epiphyseal plate in the diaphysis of the
adjacent radius.
growing long bone by transplanting an extra
epiphyseal plate to its diaphysis(5,22,57). The first
report was by Donski(22), who placed a distal
ulna epiphyseal plate into the contralateral
radial shaft. His transplants did not grow well,
but the reason was not clear because there were
several unknown variables (e.g. small group
size, intact adjacent ulna, incomplete transplant
vascularity). The second was from our own
laboratory(5) and described an experiment in
which canine distal ulna epiphyseal plates
were placed into the mid diaphyseal region of
the ipsilateral radius, leaving the epiphyseal
plates at the proximal and distal ends of the
radius in place (Fig. 5). Short term results
were promising, and increased length could
be achieved in recipient site bones. In the
long term, however, it was not possible to
prevent the constructs from fracturing - another
indication that the effect of biomechanical
forces on the transplants was an area that
would need further investigation. Shigetomi(57)
transplanted distal ulnas into the ipsilateral
humeral shaft in puppies, using a specially
designed extensible plate for skeletal fixation.
His short term results also looked promising,
but late collapse and bridging callus prevented

him from obtaining significant long term length
increase.
Glickman, also working in our laboratory,
has recently done an experiment investigating
whether or not donor epiphyseal plates
change their growth potential when they
are transplanted to recipient sites of different
growth potential (28). He used the rabbit
second metatarsal model which Stevens(60)
developed for this purpose. Metatarsals were
transplanted to sites of the same growth
potential (orthotopic transplants), higher
growth potential (heterotopic transplants
to the proximal tibia), and lower growth
potential (heterotopic transplants to a
metacarpal). Results showed that the donor
epiphyseal plates maintained their donor
site growth potential (rate and duration of
growth) irrespective of the recipient site to
which they were transplanted.
Allograft epiphyseal plate transplants
revascularized in orthotopic and heterotopic
sites
Currently there is considerable interest
in developing methods for future clinical
revascularised allograft epiphyseal plate
and bone transplantations. This is partly a
natural progression of the development of
nonvascularized intercalary and osteochondral
bone allografts, partly a logical progression
of the quite considerable knowledge now
gathered concerning microvascular autograft
epiphyseal plate transplants, and partly
because some clinical surgeons are keen
to use this reconstructive possibility. The
use of revascularised allograft epiphyseal
plate transplants offers considerably more
reconstructive possibilities than autograft
transplants, as donor site morbidity would
no longer be a consideration and the surgeon
would have a much greater choice of donor
sites and would theoretically be free to choose
ideal donor tissue. The drawback with using
transplants of this type is that patients would
Vascularised epiphyseal plate transplantation
be given immunosuppression to prevent
rejection from occurring. Currently available
immunosuppressive drugs are associated with
severe systemic toxicity(18). This is a problem
that will need to be resolved before it becomes
acceptable for allograft transplants to be used for
extremity reconstruction. Nevertheless, it seems
reasonable to consider(49) that revascularised
allograft epiphyseal plate transplantation
might be possible in the not-too-distant future.
For this reason, researchers have started to
investigate the use of allograft donor material
and to address some of the interesting questions
posed by the idea of using it.
Some investigators have transplanted
allograft epiphyseal plates as part of
composite tissue transplantations in skeletally
immature animals. Manfrini(41) transplanted
whole knees in immature rats, and the
transplantation of whole limbs in immature
animals has been described by a number of
different researchers(29,31,32,39). In each study
longitudinal skeletal growth continued after
transplantation.
Both Ford(25) and Boyer(11) have reported
the results of revascularised allograft
epiphyseal plate transplantations in animals
immunosuppressed with Cyclosporin A.
Cyclosporin A is known to have a direct
effect on epiphyseal plate growth(35), and yet
the results obtained by both investigators
demonstrated that successfully revascularised
allograft epiphyseal plate transplants grew
at rates similar to autograft controls. When
the growth rates of allograft transplants was
compared to unoperated control limbs, in Ford’s
series the allografts produced less growth,
whereas similar growth rates were achieved in
Boyer’s animals. Boyer recognized, however,
that the results of all experiments (autograft or
allograft) need to be interpreted with caution
as a number of different variables may affect
the growth potential of the transplants. Some
may produce growth stimulation (e.g. the
osteotomies needed to harvest the graft), others
133
C.V.A. Bowen, P.W. Bray, M.I. Boyer
may produce growth retardation (e.g. altered
blood flow, Cyclosporin A), whilst the effect
of others (e.g. biomechanical loading) is not
well understood.
As part of his study, Boyer also collected
data to evaluate the use of Tc99-MDP bone
scans(12) for assessing post-operative viability
in the transplants. This was done because
a number of investigators had used this
technique (Fig. 6) and it has proved to be a
good and useful minimally invasive method for
monitoring microsurgical bone grafts clinically.
He found that qualitative scans were a good
predictor of continued longitudinal growth
but that quantitative scans did not add any
useful information.
Stevens has recently completed an
experiment (9) in which epiphyseal plates
from a young (before the pubertal growth
spurt) rabbit were transplanted into older
immature (after the pubertal growth spurt)
rabbits as revascularised allograft transplants.
Such a heterochronic transplantation can
only be done using allograft donors. This
experiment was a very important stepping
stone to future clinical situations in which it
is unlikely that the characteristics of donor
epiphyseal plates will ever match those
needed at the recipient site. The age, sex,
and constitutional features of donors will
always differ from recipients. This poses
fascinating questions that will need to be
answered in order that sensible decisions can
be made when it becomes possible for allograft
transplantation procedures in children. For
instance, if the recipient patient was a seven
year old boy and a three year old female donor
became available, what would be the growth
potential of the donor epiphyseal plate after
transplantation? What would its growth rate
be, and at what age would it reach skeletal
maturity? The questions could be made even
more complex by the possibility that the donor
was constitutionally destined to be very tall
and the recipient very short, or vice versa. Of
134
Figure 6. Technetium 99-MDP bone scan
showing the experimental limb in a dog which
has undergone orthotopic transplantation of a
distal ulna epiphyseal plate. Localised areas of
increased uptake demonstrate the shoulder to the
left and the elbow epiphyseal plates in the centre.
The transplanted revascularised distal ulna clearly
shows increased uptake, and is seen as the lower,
and slightly smaller, of the two areas of increased
uptake at the right of the illustration. The slightly
larger area of increased uptake above it is the distal
radius epiphyseal plate.
course procedures, such as epiphysiodesis,
could be done to correct for inaccuracies
when the child approaches skeletal maturity,
but it would be better to have the ability
to predict growth potential at the time
transplant operations were planned. The
results of Stevens’s experiment demonstrated
that donor epiphyseal plates maintained
growth rates consistent with the age of the
animal from which the graft originated,
and did not change their growth rate to
match that of the recipient. Drzewiecki(23)
also described an interesting experiment in
which heterochronic transplants were done.
In their study the hind limbs of immature
rats were transplanted into synergistic adults.
Glickman’s experiment(28) (described earlier),
in which autograft epiphyseal plates were
transplanted to sites of different growth
potential, followed Stevens’ experiment
and also demonstrated that donors did not
change their growth characteristics to match
the recipient sites.

THE FUTURE OF EPIPHYSEAL PLATE
TRANSPLANTATION
Researchers are currently looking in three
different directions as they work at developing
other, futuristic, methods for biologically
correcting the growth problems associated
with epiphyseal plate damage from injury
and disease:
a) new methods for the use of allograft
donor material
b) foetal transplantation
c) the development of prefabricated
transplants
a) new methods for the use of allograft
donor material
One approach to the problem of the
systemic toxicity of currently available
immuno-suppressants is to develop newer,
less toxic drugs. FK506 has been investigated
for a number of uses, including extremity
transplantation. It can be used in concentrations
much lower than Cyclosporin A with good
results, but unfortunately is still too toxic to
be used for non life threatening conditions.
Its use is associated with Pneumocystis carinii
infection, nephrotoxicity, neurotoxicity, and
the development of diabetes. A number of
newer experimental drugs are also currently
being investigated and it will be interesting
to see how this approach develops over the
next few years.
In our laboratory, at the present time we are
investigating a method for doing revascularised
epiphyseal plate transplantation that would
only require short term immunosuppression.
Doi(20) used short term immunosuppression
in his case of micro-surgically revascularised
bone trans-plantation, and we also think
that it is probably ethically acceptable to
use immunosuppressants for a short time
in order to reconstruct damage to major
epiphyseal plates, especially if they occur
in very young children. Our technique is
based on the concept that cartilage cells are
Vascularised epiphyseal plate transplantation
immunologically protected, probably because
in intact cartilage the extracellular matrix acts
as a non immunogenic barrier preventing the
chondrocyte major histocompatibility complex
from being presented to the recipient’s
immune system(24). It has been demonstrated,
in allograft transplants, that proliferation and
maturation of epiphyseal plate chondrocytes
continues until the blood supply is disturbed
by the immune response(31,44). In our current
experiment, therefore, immunosuppression is
being stopped after bone union (and hopefully
vascular ingrowth) has taken place on each
side of the transplanted epiphyseal plates.
Although it is expected that rejection will
occur in the epiphyseal plates’ supporting
blood vessels and bone, it is hoped that there
will be sufficient epiphyseal and metaphyseal
revascularisation from the recipient site
to support continued function from the
epiphyseal plate and that the epiphyseal plate
chondrocytes will be protected from rejection
by their extracellular matrix.
b) foetal transplantation
Pho(56) has experimented with allograft
transplantation using foetal tissue in rabbits.
Foetal transplantation appears to be able to
offer donor material with low immunogenicity
and high growth potential. This material
would likely be particularly useful for the
reconstruction of congenital deficiencies and
trauma in the very young. Pho’s results suggest
that foetal transplantation will be a useful
reconstructive technique, although at present,
it is still in its infancy.
c) the development of prefabricated
transplants
There is currently quite a lot of interest
in the development of fabricated and
prefabricated free tissue transfers. These
can be created using autograft material,
thus avoiding the problems associated with
immunosuppression. In the future they might
135
C.V.A. Bowen, P.W. Bray, M.I. Boyer
also be made using combinations of autograft
and allograft donor material, or with allograft
donor material alone.
Ozbek(54) and Morrison(45) have published
the results of clinical cases in which
prefabricated free flaps, with autograft donor
tissue, were used. Khouri(37) has described and
classified fabricated and prefabricated free-flap
techniques. Khouri(37) has also investigated the
concept of tissue induction, which he sees as
an exciting extension of prefabrication, based
on advances being made in cell biology. In one
experiment he(38) investigated the possibility
that the mitotic effect of recombinant platelet-
derived growth factor might be used to
generate potentially useful tissue. In another
study Khouri(36) investigated the possibility of
creating bones using a tissue transformation
technique.
Other researchers have been working
with the process of molded vascularised
osteoneogenesis(48) as a method for creating
vascularised bone transfers. They have
described experiments(42,43) in which they
investigated the possibility of preforming
vascularised bone grafts in synthetic chambers.
Their results indicated that it was possible to
form bone in this manner.
So far the literature contains no reports of
prefabrications using epiphyseal plates, but it
is likely that there are future possibilities for
using this technique to create reconstructive
transplants.
REFERENCES
1. Bowen CVA. Experimental free vascularized
epiphyseal transplants. Orthopaedics 1986;9:893-898.
2. Bowen CVA. Microsurgical growth plate transfers.
In Behaviour of the Growth Plate. Uhthoff HK
and Wiley JJ (eds), Raven Press, New York, 1988;
pp55-59.
3. Bowen CVA, Crosby N, Wilkinson AA, Cassidy DJ
and Johnston GHF. A study of the effects of loading
136
on microsurgical free growth plate transfers. Ortho
Trans 1987;11:414.
4. Bowen CVA, Ethridge C, O’Brien BMcC, Frykman
G and Gumley G. Experimental microvascular
growth plate transfers. Part 1 - Investigation of
vascularity. J Bone Joint Surg 1988;70-B:305-310.
5. Bowen CVA, O’Brien BMcC and Gumley G.
Experimental microvascular growth plate transfers.
Part 2 - Investigation of feasibility. J Bone Joint
Surg 1988;70-B:311-314.
6. Bowen CVA, Bray PW, Boyer MI, Fowler JD and
Nolan L. Short term response of epiphyseal plate cell
populations following selective devascularisation
and microsurgical re-vascularisation. Microsurgery
1994;15:555-562.
7. Bowen CVA, Crosby NL and Singer S. The
growth potential of microvascular epiphyseal
plate transfers. Submitted for publication.
8. Bowen CVA, Crosby N, Feldkamp M, Johnston
GHF, Yang JP and Glickman AM. Microvascular
free growth plate transfers with and without
nutrient artery revascularization. Submitted for
publication.
9. Bowen CVA, Stevens DG, Boyer MI and Danska JS.
Epiphyseal plate transplantation between subjects
of different ages. Submitted for publication.
10. Boyer MI, Bray PW and Bowen CVA. Epiphyseal
Plate Transplantation: An Historic Review. Brit J
Plast Surg 1994;47:563-569.
11. Boyer MI, Danska JS, Nolan L, Kiral A, and Bowen
CVA. Microvascular Transplantation of Physeal
Allografts. J Bone Joint Surg 1995;77-B:806-814.
12. Boyer MI, Gilday G, Kiral A, Nolan L and Bowen
CVA. Can quantitative Tc99-MDP bone scans be
used to predict longitudinal growth of epiphyseal
plate allografts after microvascular replantation? An
experimental study. Microsurgery 1995;16:155-160.
13. Brown K, Kornacki J, Welter J, Poole A and Creuss
R. The effects of weightbearing on the growth of
heterotopically transplanted free vascularized
epiphyseal grafts in dogs. Ortho Trans 1986;10:241-
242.

14. Brown K, Marie P, Lyszakowski T, Daniel R
and Cruess R. Epiphyseal growth after free
fibular transfer with and without microvascular
anastomosis. J Bone Joint Surg 1983;65-B:493-501.
15. Chen ZW and Bao YS. Microsurgery in China.
Clin Plast Surg 1980;7:437-474.
16. Chen ZW and Zhang GJ. Epiphyseal trans-
plantation. In Pho R (ed.): Microsurgical Technique
in Orthopaedics. London, Butterworth 1988;121-
127.
17. Chung DW, Yoo MC and Han CS. Free epiphyseal
plate transplantation. Presented at the 12th annual
meeting of the American Society for Reconstructive
Microsurgery, Boca Raton, Florida, 1997.
18. Cockfield SM and Halloran PF. Cyclosporine: a new
decade. Ann Royal Coll Phys Surg Can 1991;24:25-
28.
19. Demiri E, Bakhach J, Tsakoniatis N, Martin D
and Baudet J. Bone growth after replantation in
children. J Reconstr Microsurg 1995;11:113-122.
20. Doi K, Akino T, Shigetomi M, Muramatsu K and
Kawai S. Vascularized bone allografts: Review of
current concepts. Microsurgery 1994;15:831-841.
21. Donski P, Carwell G and Sharzer L. Growth in
revascularized bone grafts in young puppies.
Plast Reconstr Surg 1979;64:239-243.
22. Donski P and O’Brien BMcC. Free microvascular
epiphyseal transplantation: An experimental
study in dogs. Brit J Plast Surg 1980;33:169-178.
23. Drzewiecki AE, Randolph MA, Hotchkiss RH
and Weiland AJ. Vascularized growth-plate
transplantation: A comparative study in the rat.
J Reconstr Microsurg 1992;8:93-100.
24. Elves MW. Newer knowledge of the immunology
of bone and cartilage. Clin Orthop 1976;120:232-258.
25. Ford D, Gerber S and Green C. Epiphyseal growth
after vascular transfer using the juvenile rabbit
knee as an experimental model: A comparision
of growth in autografts and allografts using
Cyclosporin A for immunosuppression. J Bone
and Joint Surg 1987;69-B:495.
Vascularised epiphyseal plate transplantation
26. Gaul J and Nunley J. Microvascular replantation in
a seven-month-old girl: A case report. Microsurgery
1988;9:204-207.
27. Gilbert A. Reconstruction of congenital hand
defects with microvascular toe transfers. Hand
Clin 1985;1:351-360.
28. Glickman AM, Yang JP, Stevens DG and Bowen
CVA. Epiphyseal plate transplantation between
sites of different growth potential. Submitted for
publication.
29. Guzman-Stein G and Shons AR. Functional
recovery in the rat limb transplant model: A
preliminary study. Transplant Proc 1987;19:1115-
1117.
30. Harris W, Martin R. and Tile M. Transplantation
of Epiphyseal Plates. J Bone and Joint Surg 1965;47-
A:897-914.
31. Hotokebuchi T, Arai K, Arita C, Miyahara H,
Sugioka Y and Kaibara N. Limb allografts in
skeletally immature rats with cyclosporin:
Behaviour of the growth plate. Transplant Proc
1989;21:3183-3185.
32. Hou SM, Wang TG and Liu MR. Longitudinal
growth after replantation of immature extremities
on rats. J Hand Surg 1993;18-A:828-832.
33. Hurwitz P. Experimental transplantation of small
joints by microvascular anastomoses. Plast Reconstr
Surg 1979;64:221-231.
34. Innocenti M. La ricostruzione scheletrica con la
fibula in accrescimento. Presented at 1o Corso
di Perfezionamento Teorico-Pratico in Chirurgia
Della Mano e Microchirurgia Ricostruttiva, Milan,
1997.
35. Kahan B. Drug therapy: Cyclosporine. NEJM
1989;321:1725-1738.
36. Khouri RK, Koudsi B and Reddi H. Tissue
transformation into bone in vivo. A potential
practical application. JAMA 1991;266:1953-1955.
37. Khouri RK, Upton J and Shaw WW. Principles of
flap prefabrication. Clin Plast Surg 1992;19:763-771.
38. Khouri RK, Koudsi B, Deune EG, Hong SP, Ozbek
137
C.V.A. Bowen, P.W. Bray, M.I. Boyer
MR, Serdar CM, Song SZ and Pierce GF. Tissue
generation with growth factors. Surgery 1993:
discussion 379;114:374-380.
39. Kniha H, Randzio J, Gold ME, Fudem GM, Cruz
HG, Park HM and Furnas DW. Growth of forelimb
allografts in young rabbits immunosuppressed
with cyclosporine. Ann Plast Surg 1989;22:135-141.
40. Lister G. Microsurgical transfer of the second
toe fo congenital deficiency of the thumb. Plast
Reconstr Surg 1988;82:658-665.
41. Manfrini M, Randolph M, Andrisano A. and
Weiland AJ. Orthotopic knee grafts in rats: A model
for growth plate transplantation. Microsurgery
1988;9:242-245.
42. Mizumoto S, Inada Y and Weiland AJ. Pre-formed
vascularized bone grafts using polyethylene
chambers. J Reconstr Microsurg 1992;8:325-333.
43. Mizumoto S, Inada Y and Weiland AJ. Fabrication
of vascularized bone grafts using ceramic
chambers. J Reconstr Microsurg 1993;9:441-449.
44. Mohtai M, Hotokebuchi T, Arai K and Sugioka Y.
Changes in growth-plate morphology associated
with rejection in rat limb allografts. J Bone and
Joint Surg 1992;74-A:1375-1384.
45. Morrison WA. Directions in customised
flap prefabricated donor sites. Presented at
International Surgical Week, 35th World Congress
of International Society of Surgery, Hong Kong,
1993.
46. Nettelblad H, Randolph B and Weiland AJ.
Heterotopic microvascular growth plate
transplantation of the proximal fibula: An
experimental canine model. Plast Reconstr Surg
1986;77:814-820.
47. Nettelblad H, Randolph M and Weiland AJ. Free
microvascular epiphyseal-plate transplantation.
J Bone and Joint Surg 1984;66-A:1421-1430.
48. Nettelblad H, Randolph MA, Ostrup LT and
Weiland AJ. Molded vascularized osteoneogenesis:
A preliminary study in rabbits. Plast Reconstr Surg
1985;76:851-856.
49. Nolan L and Bowen CVA. Extremity transplantation
138
- A review of its current state of development. J
Hand Surg 1993;18:153-159.
50. Nolan L, Bowen CVA and Boyer M. Skeletal
fixation in the rabbit knee transplantation model.
Microsurgery 1992;13:291-292.
51. Nunley J, Spiegl P, Goldner R and Urbaniak J.
Longitudinal epiphyseal growth after replantation
and transplantation in children. J Hand Surg
1987;12-A: 274-279.
52. O’Brien BMcC, Franklin JD, Morrison WA and
MacLeod AM. Replantation and revascularization
surgery in children. Hand 1980;12:12-24.
53. O’Brien BMcC, Gould J, Morrison W, Russell R,
MacLeod A. and Pribaz J. Free vascularized small
joint transfer to the hand. J Hand Surg 1984;9-
A:634-641.
54. Ozbek MR, Kutlu N, Khouri RK, Gultan SM and
Yormuk E. Prefabricated microvascular shoulder
free flap for forehead reconstruction. Handchir
Mikrochir Plast Chir 1993;25:139-143.
55. Pho RW, Patterson M, Kour A and Kumar V.
Free vascularised epiphyseal transplantation
in upper extremity reconstruction. J Hand Surg
1988;13:440-447.
56. Pho RW, Liew LP and Adani R. Experimental
transplantation of limbs. Ann Acad Med Singapore
1991;20:777-783.
57. Shigetomi M, Morrison WA, O’Loughlin KC,
Sakai K, Kuwata N, Ohti I, Hayward PG, Hurley
JV and O’Brien BMcC. Heterotopic vascularized
growth plate transfer in juvenile dogs. Microsurgery
1994;15:738-745.
58. Shimizu H, Tsai TM and Firrell JC. Effect of
ischaemia and three different perfusion solutions
on the rabbit epiphyseal growth plate. Microsurgery
1995;16:639-645.
59. Stark R, Matloub H, Sanger J, Cohen E and Lynch
K. Warm ischemic damage to the epiphyseal
growth plate: A rabbit model. J Hand Surg 1987;12-
A:54-61.
60. Stevens D and Bowen CVA. Heterotopic
microvascular epiphyseal plate transplantation:

A new model using the rabbit metatarsal.
Microsurgery 1995;16:488-492.
61. Taylor GI, Wilson KR, Rees MD, Corlett RJ and
Cole WG. The anterior tibial vessels and their role
in epiphyseal and diaphyseal transfer of the fibula.
Experimental study and clinical applications. Br
J Plast Surg 1988;41:451-469.
62. Teot L, Bosse J, Gilbert A and Tremblay G. Pedicle
graft epiphysis transplantation. Clin Orthop
1983;180:206-218.
63. Tomita Y, Tsai TM, Steyers C, Ogden L, Jupiter
J and Kutz J. The role of the epiphyseal and
metaphyseal circulations on longitudinal growth
in the dog: An experimental study. J Hand Surg
1986;11-A:375-382.
64. Tsai TM, Ludwig L and Tonkin M. Vascularized
Vascularised epiphyseal plate transplantation
fibular epiphyseal transfer: A clinical study. Clin
Orthop 1986;210:228-234.
65. Vilkki SK. Microvascular epiphyseal transplantation
and distraction lengthening in the treatment of
radial club hand. Presented at the 10th Symposium
of the International Society of Reconstructive
Microsurgery, Munich, Germany, 1991.
66. Vilkki SK. Advances in microsurgical reconstruction
of the congenitally adactylous hand. Clin Orthop
1995;314:45-58.
67. Wray R, Mathes S, Young V and Weeks P. Free
vascularized whole-joint transplants with ununited
epiphyses. Plast Reconstr Surg 1981;67:519-525.
68. Zaleske DJ, Ehrlich MG, Piliero C, May JW,
Mankin HJ. Growth-plate behaviour in whole
joint replantation in the rabbit. J Bone Joint Surg
1982;64-A:249-258.
139
 Part III
Physeal fractures
20
Fractures of the growth plate
J. de Pablos and C. Alfaro-Adrián
INTRODUCTION
According to Mercer Rang (98), “many
fractures in children heal well regardless of
whether they were treated by a professor in
a teaching hospital or by Robinson Crusoe
on a deserted island”, therefore, from an
orthopedic point of view, many children
fractures have a relative significance. However,
fractures of the growth plate or physis(103),
present two peculiarities that merit special
attention in pediatric orthopedics treatises.
The first peculiarity is the seriousness of
the sequelae that can result from treating
these fractures incorrectly, or even when
the treatment performed was correct. The
second characteristic is its high frequency:
according to authors like Rang, physeal
fractures constitute up to one third of skeletal
fractures in children(98).
In general, we understand physeal trauma as
an injury that directly affects the growth plate.
In this chapter, however, we will also mention
indirect trauma that, even when apparently not
affecting the physis at the time of injury, can in
fact lead to an alteration of its function in the
future (under or overgrowth).
BACKGROUND
We can state, without hesitation, that a
great deal of what we know today regarding
traumatisms to the growth plate and the
behavior of that structure under those
circumstances was already known by 1898
when John Poland published his book entitled
“Traumatic Separation of the Epiphysis”(94,95).
In that magnificent work, the author presented
a thorough historical review and described
experimental and clinical findings regarding
physeal injuries up until the 20th century.
As occurs with many other topics in Medicine
and Surgery, Hippocrates was one of the first
authors to describe skeletal bone fractures.
However, the descriptions of the possible physeal
fractures that appear in his writings are not precise
enough to insure that he was, in fact, referring
to them.
In the XVI century, Realdus Columbus
described clear cases of epiphyseo-metaphyseal
separation in newborns and in 1614 Paré, when
describing 2 cases of physeal fractures, was one
of the first authors to indicate the possibility of
confusing this type of fractures with articular
dislocations, more frequent in adults. Also in
the XVII century, Poupart spread the idea that
physeal fractures only occurred as a consequence
of a subjacent illness and, therefore, a simple
traumatism could not produce a fracture of a
healthy physis.
Sandifort in 1768 was the first to differentiate
simple post-traumatic physeal fractures from
those due to a previous weakening process of
143
J. de Pablos, C. Alfaro-Adrián

A
Figure 1. Normal growth plate. A) Schematic
representation of the different layers. Taken form:
Siffert RS, Gilbert MD. Anatomy and physiology of
the growth plate. In Rang M (ed). The growth plate
and its disorders. Baltimore, Williams & Wilkins,
1969. B) Histologic preparation of the distal femoral B
physis of a sheep where the same layers can be
identified. Masson’s trichromic x 40.

the physis. In 1803, Portal indicated that physeal
fractures were more frequently located in the
radius and the neck of the femur.
By the 20th century, publications that are
still popular today first appeared. The first
one is Blount’s classic(7), followed years later
by Rang’s(97,99) and Ogden’s(80) books, the latter
being the most thorough book on general and
physeal pediatric traumatology.
Perhaps the latest efforts to update
knowledge on general physeal pathology,
logically including traumatisms, were the
meeting which took place in Ottawa (Canada)
in 1987 and formed the basis for the Uhthoff and
Wiley edition of their book entitled “Behavior
of the Growth Plate”(114), and the meeting
held in Madrid (Spain) in 1993 which lead to
the publication of the monographic review
entitled “Surgery of the Growth Plate”(29).
STRUCTURE AND FUNCTION OF THE
GROWTH CARTILAGE
We must mention the reviews published by
Brighton in 1978 and 1984(12,13) that will serve
as a basis for many of the following ideas and
which, on the other hand we will frequently
observe, have not been substantially modified
regarding traditional teachings.
The growth plate, or physis, is a discoid
formation situated between the epiphysis and the
metaphysis of long bones and its main function
is the longitudinal and latitudinal growth of
those bones.

144

Although it is considered a simple structure,
the physis of an enchondral bone is a complex
set of cells, which vary from species to species
and even among different bones of the same
species(75,76). In any case, we will briefly describe
its common features.
The growth plate can be divided into three
different components, depending on its tissue:
a cartilaginous component, subdivided itself
into several layers (germinal, proliferative,
hypertrophic and provisional calcification),
a bone component (the metaphysis), and a
fibrous component surrounding the periphery
of the physis, which is comprised of Ranvier’s
groove(100) and Lacroix’s perichondrial ring(58)
(Fig. 1).
The germinal zone has also been called
the reserve zone, the small cell zone and the
resting zone, these last two denominations
being almost no longer in use(19). This layer
is, perhaps, the least known in terms of its
function and in this respect three possibilities
are juggled that could co-exist: storage of
cellular nutrients (mostly lipids), germinal
function (accumulation of stem cells) and,
lastly, a more controversial function of
mechanical protection (cushioning of the
remaining growth cartilage).
The proliferative layer seems to have a double
function: cartilaginous matrix production and
cell proliferation. The combined two functions
result in one main function: longitudinal bone
growth.
The hypertrophic layer has the function of
preparing the matrix for calcification and the
layer of provisional calcification has the function
of calcifying the matrix.
Regarding the functions of the metaphysis
(the bone component), we can mention the
invasion of the transverse septi at the provisional
calcification layer(116) and bone formation and
remodeling (which includes metaphyseal
funneling).
Lastly, focusing on the fibrous component,
the most widely accepted function of Ranvier’s
Fractures of the growth plate
groove is latitudinal growth of the growth plate,
and that of Lacroix’s perichondrial ring would
probably be providing mechanical support to
the growth plate.
Regarding the vascularization of
the growth plate, there seems to be less
doubt (16,110,111,113): the ramifications of the
epiphyseal artery irrigate the germinal layer
and reach the base of the proliferative layer.
Generally, and excluding the first twelve
to eighteen months of life, these vessels do
not reach the hypertrophic layer through
the proliferative layer, these two layers
acting as a barrier separating the epiphyseal
and metaphyseal irrigation systems. The
metaphyseal vessels come into close contact
with the provisional calcification layer and,
besides performing a nutritional function at
that level, they also play an essential role in
the enchondral ossification process, which
takes place there. Apparently, these vessels
provide the primary cells (osteoclasts and
osteoblasts) which will transform the calcified
cartilage into woven bone (primary cancellous
bone). We could say, therefore, that epiphyseal
blood circulation has an eminently nutritional
function for the physis, while metaphyseal
blood flow is fundamentally aimed at its
chondral ossification.
The bone component of the growth plate
(the metaphysis) receives adequate blood
supply provided by the metaphyseal arteries
in the periphery and the nutrient artery in the
center. Ranvier’s groove and LaCroix’s ring
are irrigated by the perichondral arterioles(12,13).
HISTOPATHOLOGY OF PHYSEAL
FRACTURES
In fractures of the growth plate, the
metaphyso-epiphyseal separation plane is
almost always the same: the line of transition
between the hypertrophic and provisional
calcification layers, that is, the union between
non-calcified and calcified cartilage (Fig.
145
J. de Pablos, C. Alfaro-Adrián

A B
Figure 2. Histopathology of experimental physeal fractures in sheep. A) Usual fracture plane in epiphyso-
metaphyseal separation located between the hipertrophic and provisional calcification layers. Masson’s
trichromic x 40. B) Longitudinal gap in the growth plate occupied by hematic tissue, which communicates
epiphyseal and metaphyseal circulations.

2). Authors like Rang(98) believe this to be
invariably so, while others, like Ogden(80),
although recognizing that this is the most
frequent separation line, point out the
possibility that this separation can occur in
other physeal layers. Rang(98) observed that
if we make a transverse histologic incision
in this transition area of the physis, we will
see that the amount of cartilaginous matrix is
smaller than the amount existing in the other
layers of the growth plate; this would explain
the relative weakness of this area. We believe,
without underestimating this fact, that this
transitional area of calcified and non-calcified
cartilage constitutes a plane of accumulation
of tensions under any traumatic agent, which
allows the fracture to take place there more
easily than at other levels.
Although some authors(98), define this
separation plane as “bloodless”, we have observed
that in experimental physeal fractures(37) this is
not so since invariably the gap that is formed
following physeal separation is immediately
occupied by a hematoma which becomes
progressively organized (Fig. 3).
In any case, what remains constant is
the fact that in these fractures the physeal
germinal layer always remains attached
to the epiphyseal bone, which is crucial in
order to understand the physiopathology of
these injuries. In fact, the blood supply to the
germinal layer of the physis depends wholly

146

A
Figure 3. Experimental physeal fracture in the
ovine distal femur. A) Roentgenographic aspect.
B) Histologic preparation where a hematoma can be
seen occupying the area of epiphyso-metaphyseal
separation. Masson’s trichromic x 40.
on the epiphyseal vessels, and, depending
on whether these are damaged or not after
a physeal fracture, ischemia will result at
that level. Dale and Harris(28) described two
large groups of epiphyses depending on the
type of irrigation they presented: epiphysis
completely covered by articular cartilage (that
is, totally intra-articular) and epiphysis with
insertions of soft tissues or partially extra-
articular. In the first case (i.e. femoral or radial
head), a traumatic epiphyso-metaphyseal
separation would theoretically entail total
ischemia of the epiphysis, and, consequently,
of the germinal layer of the growth plate. On
the other hand, a similar ischaemic damage
in the second type of epiphysis would have
a much lower probability of appearing, and,
therefore, the risk of permanent alterations of
the growth plate also is reduced. These ideas,
though they present a suggestive scientific
basis and obey a certain logic are, nevertheless,
purely theoretical and should not be rigidly
applied to clinical practice. For instance, in
radial proximal physeal fractures, premature
closure of the physis is infrequent(42) in spite
of the theory that would lead us to believe
the exact opposite.
Fractures of the growth plate
B
In 1984 we carried out an experimental
study(33,37) to observe, among other objectives,
the phenomena which took place following a
traumatic separation of the physis. This study
resulted in the following interesting findings:
Following a physeal fracture, the resulting gap
is immediately occupied by a hematoma that
begins to organize in the days following the
injury. Secondly, after approximately three
weeks, the gap is completely occupied by a
richly vascularized fibrous tissue (collagen
and fibroblasts). Finally, during that time,
desmal type ossification of that fibrous tissue
begins as the endochondral ossification of the
physis also resumes.
A remarkable fact during the first 15-20
days following the fracture and that was
exhaustively documented by Dale and
Harris (28) was the progressive thickening
of the injured physis which is observed in
relation to the contralateral intact physis and
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J. de Pablos, C. Alfaro-Adrián
Figure 4. Experimental epiphyso-metaphyseal
separation in the distal femur. 15 days post-fracture.
An evident thickening of the fractured physis (right)
can be appreciated when compared with the intact
growth plate of the contralateral distal femur (left).
This thickening is mainly due to cellular storage
in the hipertrophic layer of the injured physis.
Masson´s Trichromic x100.
which, after that time, gradually becomes
normal. These authors attribute this to the
fact that following the separation, the cells
of the physeal germinal layer continue to
multiply, which allows the physeal cells to
be stored mainly in the hypertrophic layer
as long as the metaphyseal vessels do not
re-invade the cartilage (normal enchondral
ossification is therefore temporarily prevented)
consequently leading to physeal thickening.
This process requires maintaining epiphyseal
blood supply post-fracture and, therefore,
physeal growth function. Trueta and Amato(112)
in a study within the framework of a series of
148
publications dedicated to the phisiopathology
of the growth plate clearly demonstrated how
metaphyseal ischemia produced, as its sole
effect, a delay of the endochondral ossification
of the physis and therefore its enlargement.
We have also observed this occurrence in
experimental physeal fractures (Fig. 4) and
share the above mentioned ideas(33,37).
Physeal fractures in patients with
myelomeningocele whose lack of sensitivity
makes these fractures go unnoticed and
therefore often untreated for various lengths
of time(66) are a special case. It is precisely
this lack of immobilization what prevents
endochondral ossification from resuming at
the level of the fractured physis and so when
it is detected a significant thickening of the
physeal radio-lucid fringe(102) is frequently
observed. This has lead some authors to call
this phenomenon “Charcot’s physis” given
its neurologic origin similar to what occurs
on the progressive arthropathy described by
that author(57).
Up until this point we have dealt with
strict physeal separation, that is, a fracture
whose trajectory runs parallel to the plane
of the growth plate. As we will see under
the heading entitled Classification, at a given
point, this trajectory can suffer an inflexion
and head towards the metaphysis, or else
perpendicularly cross the physis and continue
through the epiphysis. More seldomly,
the fracture line crosses the metaphysis,
perpendicularly to the physis and continues
in the epiphysis, wihtout true epiphyseal-
metaphyseal separation.
CLASSIFICATION
Before analyzing the classifications most
commonly referred to, we will mention those
previously devised and which are not less
important despite the date of their appearance.
The first of these seems to have been developed
by the French author FOUCHER(40) in 1863.

Figure 5. Poland’s classification of physeal
fractures(94,95).
Afterwards, although others have been
proposed, the classifications that were most
popular were POLAND’s(94,95), AITKEN’s(1,2)
and SALTER and HARRIS’(106,107), the latter,
published in 1963, being the most widespread
among orthopedic surgeons.
Poland (Fig. 5), who was clearly the
precursor of the classifications currently more
utilized, divided physeal fractures into four
large groups, that the same author defined
in the following way:
˙Group I: pure and complete epiphyso-
metaphyseal separation.
˙Group II: partial separation with fracture
of the diaphysis.
˙Group III: partial separation with fracture
of the epiphysis.
˙Group IV: complete separation with
epiphyseal fracture.
Fractures of the growth plate
Salter and Harris Classification(106,107)
This is the most widespread classification
and, as we will see, it is partially based on the
classification proposed sixty-five years earlier
by John Poland. An important characteristic
of this classification is that almost every
physeal fracture can be easily included in
one of its groups so that the discrepancies
among observers are infrequent.
The classification is based on the pathologic
anatomy of the fracture and five large groups
can be differentiated (Fig. 6).
-Type I
It is similar to Poland’s group I and
consists of a complete epiphyso-metaphyseal
separation. The germinal, proliferative and
hypertrophic layers of the physis remain
attached to the epiphysis while the provisional
calcification layer is joined to the metaphysis.
These fractures, when they do not
present visible displacement on X-rays, can
pose diagnostic problems. The clinical signs
(swelling) and symptoms (tenderness) at the
level of the physis will make us suspect a
fracture and, if needed, stress X-rays imitating
the lesional mechanism will put an end to
any doubts. On most occasions this will not
be necessary and three or four weeks of cast
immobilization should solve the problem.
Occasionally a differential diagnosis between
an undisplaced type I physeal fracture and
a type V fracture can arise. The importance
lies in that while type I fractures have a good
prognosis, type V fractures do the opposite.
Normally, type I physeal fractures are
the result of avulsion or shear forces. The
prognosis of these fractures is generally good,
healing in approximately 1 month. There
are exceptions, however: femoral proximal
epiphyseal separations can result in necrosis
of the epiphysis, due to its completely intra-
articular location, which is the most-serious
complication encountered in this type of
fracture. Letts (63) also pointed out that,
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J. de Pablos, C. Alfaro-Adrián
Figure 6. Salter and Harris classification of physeal fractures(106,107).
depending on the mechanism that produced
the fracture, peripheral compression injuries
of the physis could occur in addition to the
metaphyso-epiphyseal separation, and these
can cause bone bridges in the future even if
they go unnoticed initially.
Type I fractures in previously pathologic
bones (erroneously called pathologic fractures)
are also relatively common, such as in rickets,
osteomyelitis, myelomeningocele and hormonal
alterations. During the neonatal stage type I
physeal fractures are also more frequent than
other types of fractures.
-Type II
Type II is by far the most common type
of physeal fracture. Type II fractures are very
similar to type I fractures. However, in this case
the fracture line enters the metaphysis after
running along most of the physis, therefore
leaving a small, usually triangular, fragment
of it joined to the physis and the epiphysis.
The appearance of this fragment is known as
Thurstan Holland’s sign(50).
In this type of fractures the periosteum
remains intact on the side of the metaphyseal
fragment and is interrupted on the opposite
side.
Generally these fractures are produced
by a combination of lateral flexion forces
150
(varus-valgus) and shear forces and, except
in rare cases where part of the periosteum
is interposed and surgical reduction is
necessary, the most frequently indicated
treatment is conservative: closed reduction
and immobilization during approximately
4 weeks.
-Type III
In these fractures, part of the trajectory is
also a pure physeal separation, as in type I,
but at a given point an inflexion is produced
which crosses the physis and epiphysis until
it reaches the articular surface.
These fractures, according to Salter(107),
are produced by intra-articular shear forces,
to which angulation forces may or may not
be added. These fractures are much rarer
than type I and type II fractures, and their
prognosis is worse, due to two fundamental
reasons. First of all it is an intra-articular
fracture that can condition a joint incongruity
if it is not anatomically reduced. Secondly,
due to the characteristics of the fracture line,
communication of epiphyseal and metaphyseal
circulations is produced which in the mid-to-
long-term can condition the appearance of
premature closure of the growth plate (bone
bridges). This last point is another reason
why anatomical reduction of the fragments

is necessary and, therefore, open reduction
and internal fixation is frequently indicated.
Tillaux’s fracture (56) merits special
consideration in this section as it is perhaps
the most characteristic and probably the most
frequent type III physeal fracture. It is located
in the antero-lateral portion of the distal tibial
physis-epiphysis and, since it usually occurs
during adolescence, it usually does not create
future growth problems. Open treatment is
indicated in the case of articular incongruity.
-Type IV
In this type of fracture, the fracture line
begins in the articular surface and goes through
the epiphysis, the physis and the metaphysis;
it is a type of combination between fractures
type II and III. Considering the epiphyseal
surface as the beginning of the fracture line,
it usually crosses the physis perpendicularly
in the form of a longitudinal crack towards
the metaphysis but, occasionally, it takes a
localized transverse path, as in types I and
II, between the hypertrophic and provisional
calcification layer before it undergoes a vertical
inflexion and enters the metaphysis. This is
the case of the tri-plane fractures of the ankle
described by Marmor in 1979(65).
In type IV fractures, the same two
occurrences previously mentioned in type
III occur: the fracture is intra-articular and, due
to its tract, the blood flow of the metaphysis
and the epiphysis communicate. This, in the
case of poor reduction of the fragments can
lead to articular incongruity and/or premature
arrest of physeal function.
This fracture is usually a result of applied
avulsion or shear force. In the case of tri-plane
fractures the mechanism is the application of
extreme rotational force. The most frequent
example in this group is the fracture of the
humeral lateral condyle.
-Type V
As described by Salter and Harris(106,107),
Fractures of the growth plate
it is a physeal crushing or compression
injury. This compression-effect generated
between the epiphysis and the metaphysis
would literally crush the growth plate and
consequently produce a communication
between epiphyseal and metaphyseal
blood flow. This leads to a particularly
poor prognosis in this type of fracture of the
growth plate, with the consistent appearance
of physeal premature closure, generally
occupying all or a large part of the injured
growth plate.
This diagnosis can be made only “a
posteriori”, when premature closure of
the physis is observed in a bone that had
previously suffered an injury and that showed
no fracture at that time.
This last observation is precisely what
makes this type of physeal fracture so
controversial. Some authors defend it(55) and
others(86) do not accept it, precisely because
of the lack of evidence that a physeal fracture
did in fact take place. Some authors have
attributed the premature physeal closure
that has been observed following diaphyseal
fractures of the same or contiguous bone(11,55,70),
to this mechanism of injury. Peterson and
Burke believe, however, that these premature
closures could be a consequence of a temporary
ischaemia to the affected physis rather than
a crush-fracture(86,90).
According to Salter and Harris(106), the most
frequently affected physis in type V fractures
are those of the knee and the ankle.
Aside from the Salter and Harris
classification that we have just seen, over
the last few years other physeal fracture
classifications have appeared presenting the
peculiarities we will present in the following
sections.
Ogden’s Classification(78,79)
This classification adds other fractures
located in areas or structures of extraphyseal
growth. It consists of nine types of injuries of
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J. de Pablos, C. Alfaro-Adrián

which the first five remind us the classification

of Salter and Harris. The last four are organized
depending on whether the fracture affects
Ranvier’s zone (type 6), only the epiphysis
(type 7), the metaphysis (type 8) or the
growth mechanisms of the diaphysis and
the periosteum (type 9).
Several of these types were also divided
into subtypes (20 in total) depending on the
mechanism of injury, which for the author
is of maximum importance regarding the
appearance of sequelae.
It is a very complete classification but
perhaps also excessively complicated which,
from a practical point of view, renders it less
useful.

Shapiro’s classification(108)
This author, whose classification of
fractures of the growth plate follows a
physiopathologic point of view, tries to
complement the classifications proposed up
to that time, which were based mainly on an
histopathologic perspective (Fig. 7).
The classification is based on the two
factors which, in his opinion, determine the
future of the function of the affected physis:
the integrity of epiphyseal blood flow and the
separation of epiphyseal and metaphyseal
blood flows.
According to these criteria, Shapiro
differentiates the three basic types of physeal Figure 7. Shapiro’s classification of physeal
fractures. In type A, epiphyseal circulation fractures(108).
remains intact and there is no metaphyseal-
epiphyseal circulatory communication.
The prognosis is good. In type B the Peterson’s classification(89)
epiphyseal circulation remains intact but it In a large series of physeal fractures revised
is in communication with the metaphyseal over a 10 year period Peterson found that,
circulation facilitating the formation of an according to the Salter and Harris classification,
ulterior bone bridge. This type includes Salter 15.7% did not fall into any of the types
and Harris types III, IV, and V. Lastly, in type categorized; also he found no fracture that
C, the epiphyseal circulation is destroyed after could be classified as type V.
the fracture and the consequence is necrosis He differentiated two clearly defined
of the epiphysis and of the physeal germinal groups for those fractures that did not fall
layer. The prognosis for these is also poor. into any other classification. In the first group,

152

the fracture went through the metaphysis with
one or two additional paths that reached the
physis without going through it or extending
into it. This fracture differs from the Salter
and Harris type II in that it presents no
metaphyseal-epiphyseal separation. This
fracture is more frequent in the distal radius
and in the phalanges of the hand. The prognosis
is good with conservative treatment (cast
for 3-4 weeks). The second group fractures,
which are much less frequent, consist of open
fractures with loss of part of the physis. These
fractures are the result of injuries inflicted by
lawn mowers, firearms, etc. All these fractures
spontaneously evolve towards premature
physeal closure.
From these findings, Peterson’s
classification emerged organizing the groups
(from I to VI) in order of increased risk of
sequelae. The type with the best prognosis
(type I) is precisely the first group discussed
that was not classifiable within the Salter and
Harris classsification and, the one with the
poorest prognosis (type VI) is the group of open
fractures with loss of physeal substance. The
middle groups correspond to Salter and Harris
types I-IV. As mentioned, Salter and Harris
type V is not included in this classification.
In the remainder of the chapter we will
refer to the Salter and Harris classification, as
it is the most widespread currently accepted
classification.
INCIDENCE-PATHOPHYSIOLOGY
The incidence of physeal fractures
regarding the totality of fractures in children
is around 15%(48,67,106) although some authors
think this number could be closer to 30%(64,98).
In absolute terms, Peterson(89), in a study
carried out between 1979 and 1988 on 951
physeal fractures in 850 children, found an
incidence of 282.6 physeal fractures for each
100.000 individuals between 0 to 21 years of
age, per year.
Fractures of the growth plate
Regarding the age, it is a well known fact
that a higher incidence of physeal fractures is
produced in ages close to puberty, therefore
chronologically slightly sooner in girls than in
boys(18,27,67,69). There is also a widespread idea
that physeal fractures are more frequent in
boys than in girls(74,79,85), although some authors
do not find this difference(67). Therefore, we
can deduce that the patients that will most
frequently suffer physeal fractures will be
males eleven to fifteen years old. The classical
explanation for this fact is that boys participate
more violently and frequently in games and
contact sports and, also, that in boys the physis
remains open longer than in girls(78).
In our opinion, these reasons, more so the
first than the second, are no doubt important but,
after the study on experimental epiphysiolisis
carried out by Oliete on rabbits(82), we believe that
there are other factors that are more influential
on the differences mentioned. In this study,
Oliete observed that the resistance of the growth
cartilage, when shearing force was applied on
the epiphysis of different bones and in different
directions is, in both genders, significantly
lower during puberty than in previous stages
of development; also comparing animals of the
same skeletal age, the resistance was lower in
males than in females. Following this, and in
agreement with other authors(15,18,27,69), we could
conclude that the higher incidence of physeal
fractures in male adolescents can be related to
their more vigorous physical activities on the
one hand but, above all, to their weaker physis
as compared with girls of the same skeletal age.
This more pronounced weakness in males could
be directly related to hormonal factors, but we
cannot offer any solid scientific answer to this
respect as of this moment.
Topographically, it seems that in all
large series the distal radial physis appears
to be injured most frequently, followed by
physeal fractures of the phalanges and the
distal tibia(64,67,74,78,85). Peterson(89) differs from
these findings, as in his recently published
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J. de Pablos, C. Alfaro-Adrián
series there is a higher incidence of physeal
fractures in the phalanges than in the distal
radius. In general, the upper limb is much
more frequently affected than the lower limb,
up to 75% in the series by Mizuta et al.(67).
Open physeal fractures are extraordinary(64,89).
Regarding incidence according to the Salter
and Harris classification, Mann and Rajmaira(64)
contributed a series of 943 physeal fractures
and confirm that type II is the most frequent
(483 cases) followed by type I (210 c.), III (143
c.) and IV (102 c.). Type V Salter and Harris
fractures, besides the fact that their existence
is in doubt(86,89), are exceptional both in the
series previously mentioned (5 cases) as in
the others(67).
In any case, it is difficult to exactly
determine the relative incidence of the
different types of physeal fractures as their
severity varies greatly and so frequently they
are not controlled by the same study group.
Specifically, fractures of the distal radius and
the phalanges normally receive outpatient
treatment and do not go to the hospital, while
more important physeal fractures usually are
treated in a Hospital Division of Pediatric
Orthopaedics, which makes statistical analyses
complicated to carry out at times.
TREATMENT OF PHYSEAL
FRACTURES
The first step in the treatment of physeal
fractures is their detection. In the great majority
of cases this is easy but, in others, the diagnosis
may become practically impossible with the sole
aid of clinical examination and conventional
radiology. This can be due to the anatomical
complexity of the fracture site or to the fact
that the fractured bone is in a very early stage
of development, among other factors.
This is particularly true of physeal fractures
of the elbow in children between three and
six years old. Some authors recommend
performing a routine arthrography in the
154
event that a physeal fracture is suspected
after a clinical and conventional radiologic
examinations(72). Also, in other sites, Magnetic
Resonance Imaging(17) and Ultrasonogram(51)
have proven useful in the detection of occult
fractures or in the differential diagnosis with
dislocation in very young children (above all
in infants).
General Principles
Once a physeal fracture has been diagnosed,
treatment must be initiated which, regardless
of the method used, should tend towards(72):
- Restoring the anatomy
Within this section there are various issues
from among which the least important are
the shape of the bone and the orientation of
the joint as, particularly in young children,
bone remodeling (Wolff’s law) and changes
in growth direction depending on articular
loads (Heuter-Volkmann’s Law) allows for
a certain margin regarding the perfection of
the reduction of the fracture.
Much more important, however, is
re-establishing physeal integrity particularly
in fractures that cross the growth cartilage,
as if this is not accomplished meticulously
a physeal bone bridge more than likely will
appear. Lastly, and also of extreme importance
is the anatomic reduction of intra-articular
fractures, as future degenerative changes hinge
on the quality of this reduction.
- Avoiding permanent physeal damage, which
tends to lead towards complete or partial
physeal closure
There are injuries to the physeal cells
that are only detected ‘a posteriori’ once the
physeal closure is produced. Here we can
include type V fractures(55,106) and injuries by
compression produced by the metaphyseal
acute sharp end, which can dent the physis in
type II fractures during the fracture itself or
during its reduction(63). Except in this last case,
 Fractures of the growth plate

A B

A´ B´

Figure 8. Most type I and II physeal fractures do well with a conservative treatment. A) Initial situation
in a type I physeal fracture of the distal radius in a 7 year-old girl (AP and L views). B) Closed reduction
and cast immobilization (AP and L views).

in which an adequate reduction will minimize is anatomic reduction as previously discussed.

this complication, the physeal damage thus
produced is unavoidable. In any case, we
should suspect this possibility and alert the
family of the patient.
Another way in which permanent physeal
damage occurs is due to the inadequate reduction
of certain physeal fractures; the way to avoid them
Also, as we will see in the following sections,
technical errors in the fixation of the fracture
can lead to permanent physeal damage.
- Avoiding non-union
This is particularly important in intra-
articular fractures which, bathed in intra-

155
J. de Pablos, C. Alfaro-Adrián
A B
Figure 9. Distal femoral physeal fracture type II in a 4 year-old girl. A) Situation at hospital admission.
B) Immediately postoperative after closed reduction and k-wire fixation. A cast splint was also applied.
articular fluid (possibly containing factors
inhibiting osteogenesis) could present
consolidation problems if they are not reduced
adequately.
Also in avulsion fractures as in fractures
of the humeral condyle, the risk of non-union
is higher than in other types of fractures. This
is also a well-known fact regarding adult
fractures.
Specific indications
-Type I and II fractures
These fractures, conservatively treated,
do not tend to leave sequelae as there is no
communication between metaphyseal and
epiphyseal circulation, and the trajectory of
the fracture is not intra-articular.
In principle, an adequate closed reduction
and a cast (Fig. 8) should be sufficient, trying
not to make brusque movements, which as we
discussed particularly regarding type II fractures,
could produce a compression physeal injury(63).
In cases of severe displacement, the reduction
should be performed under general anesthesia,
which greatly facilitates an easy and less risky
reduction of the fragments.
Occasionally, if following the closed
reduction, instability of the fracture fragments
is observed, fixation with K-wires can be
considered which, since they cross the physis,
156
should be thin, unthreaded, as few as possible
in number and placed as nearly perpendicular
as possible to the physeal line (Fig. 9). They
should also be removed as soon as possible
(3 to 4 weeks).
Open reduction should be reserved
for exceptional cases, where closed
reduction would not have been possible or
unsatisfactory(42).
-Type III fractures
Type III fractures present two features
that condition their potential sequelae and,
therefore, their treatment. Firstly, they are
intra-articular fractures and, secondly, they
usually occur near skeletal maturity so growth
problems are less frequent. For these reasons,
we recommend an anatomic reduction of the
fracture which, in most cases, is possible only
surgically (Fig. 10).
At this point it is important to mention
that fixation should not cross the physis, but, if
there is no alternative, it should be performed
as mentioned above.
-Type IV fractures
Type IV fractures, if not treated adequately,
present a high incidence of sequelae both at the
physeal level (bone bridges) as well as at the
intra-articular level (degenerative arthritis).
 Fractures of the growth plate

A´
A

B B´
Figure 10. Closed reduction and internal fixation in a type III physeal fracture of the proximal tibia in a
14 year-old patient. A) Situation prior to surgery. B) One year after arthrotomy and internal fixation. In
this case, the aim of this treatment was mainly to avoid epiphyseal irregularities.

157
J. de Pablos, C. Alfaro-Adrián

A B
Figure 11. Displaced fracture of the humeral condyle (S-H type IV) in a 9 year-old boy. A) Immediately
preoperative. B) 4 weeks after open reduction and internal fixation with two K-wires, just prior to their
removal.

For these reasons, the treatment of these -Type V fractures

fractures requires, as a fundamental step,
the anatomical reduction of the fragments
and their perfect fixation. Therefore it is
recommendable to systematically perform
open reduction and internal fixation (Fig.
11), although there may be rare exceptions
in cases of minimal displacement of the
fragments which, moreover, must periodically
be checked radiologically.
The recommendations discussed regarding
internal fixation in the previous types are also
applicable for this fracture type.
Fracture of the humeral condyle presents the
additional risk of non-union, due to the traction
forces applied there; stable internal fixation is,
therefore, mandatory.
These fractures, if they exist, are always
diagnosed in their stage of sequelae.
In the acute phase we can at best suspect
that the physeal damage has occurred. What
we then recommend is to inform the family
from the very beginning of the situation,
and periodically observe the patient in the
future. Active treatment will be indicated at
the moment when secondary effects appear,
if at all.
Regarding Peterson’s classification(89),
type I fractures generally have a very
good prognosis. If they are displaced, we
recommend closed reduction and cast
immovilization, if they are not, just a cast
for 3-4 weeks should be sufficient.

158

Peterson type VI fractures, on the contrary,
have a poor prognosis, as they all tend to
form physeal bone bridges with time. This
same author(89) recommends resolving the
injuries to soft parts first and waiting for
the sequelae to stabilize prior to initiating a
definitive treatment.
SEQUELAE OF PHYSEAL FRACTURES
This is, probably, the most fundamental
part of this chapter due to the fact that
physeal fractures are important in pediatric
orthopedics precisely for their potential
negative consecuences.
In the previous sections, we pointed out the
more relevant sequelae of physeal fractures:
• Articular incongruence, and, consequently,
degenerative arthritis.
• Non-union of the fracture fragments.
• Growth disorders.
From among these, we are going to
concentrate on growth disorders as they
constitute the only secondary effect specific
to physeal injuries.
The most common sequelae of physeal and,
exceptionally, extra-physeal fractures(11,55,70)
is partial or total cessation of bone growth,
due to the appearance of a premature physeal
closure (also called physeal bone bridge or
epiphysiodesis). This is the most frequent
and functionally most important sequela
of physeal fractures and its consequence is
shortening and/or angular deformity of the
involved bone segment. In addition to these
consequences, although more infrequent
epiphyseal deformities can also be caused
by the mentioned physeal bone bridges(98).
In certain types of fractures, not strictly
physeal, a stimulus of the growth plate closest
to the fracture can occur. This overgrowth is
more frequent and intense in the lower limb(109)
than in the upper limb(35) and the mechanism
that produces it is, to date, unknown. In
any case, this phenomenon should only
Fractures of the growth plate
be considered a relative complication as
the generated length discrepancy usually
does not exceed 1.5 cm and, since it creates
minimal functional impairment, it usually
does not require treatment. A particular
phenomenon attributed to this stimulus effect
(overgrowth) that some fractures have on the
growth plate is the valgus deformity of the
tibia following certain proximal metaphyseal
fractures usually minimally displaced in young
children(26,104,105,118). In these cases, according to
Salter and Best(104,105), the deformity can persist
making the use of osteotomies necessary to
correct the problem. Zionts and MacEwen(118),
on the other hand, believe this phenomenon
is generally benign and a spontaneous
progressive improvement of the deformity
usually occurs without the need for surgery.
Prognostic factors in physeal fractures
The prognosis for physeal fractures
regarding future functional disorders depends
on a series of factors among which we can
highlight:
1) Type of fracture. As we indicated earlier,
the worst prognosis corresponds to Salter
and Harris type III and IV fractures(106) and
Peterson type VI(89). In the latter, the incidence
of bone bridges is 100%(89).
2) Remnant growth. Obviously, the younger
the skeletal age at the moment of fracture, the
more the remnant growth, and, therefore, the
greater the consequences of growth arrest,
should this occur.
3) Epiphyseal blood supply. Regardless of
the type of fracture, if the epiphyseal blood
supply is interrupted as a consequence of
the fracture, the subsequent ischemia of the
germinal cells of the affected physis can lead to
serious growth disorders (e.g., type I fractures
of the proximal femoral physis)(28,108).
4) Severity of the injury (speed and force). The
so-called “high energy” injuries always have
the poorest prognosis.
5) Skin integrity. Open physeal fractures,
159
J. de Pablos, C. Alfaro-Adrián
among which Peterson type VI are included,
have the worst prognosis. This can worsen if an
infection is added, a risk not to be disregarded
in these type of fractures.
Aside from these factors that we could call
“non-modifiable”, there are others that can
be acted upon and that are directly related
to the treatment of the fracture.
1) Anatomic reduction of the fragments. This
is very important, as has been mentioned,
when dealing with type III and IV fractures.
2) Quality of osteosynthesis. When indicated,
the reduction and internal fixation of the
fracture fragments has to be accomplished
without producing more lesions to add to
those already existing. Under the section
entitled “treatment” we have mentioned
the general principles recommended for
the proper use of osteosynthesis material in
physeal fractures.
Diagnosis of physeal bone bridges.
In this section we will briefly analyze the
methods used first for detection, and then for
determining the location and size of the bone
bridges, both aspects of maximum significance
in the decision-making of the treatment.
Conventional X-rays are always the
diagnostic method by which the study should
begin(17,23). Then, in most cases, we can confirm
or not the existence of a bone bridge.
The exact location and extension of the
physeal bone bridge usually is not easy to
determine precisely by conventional X-rays
and these data are extremely important to
determine if the bridge is easy to resect or
not, and which surgical approach is better.
For this purpose, lineal tomography making
cuts 0.5 to 1 cm thick in lateral and anterio-
posterior views can be much more useful(23).
Carlson and Wenger(24) proposed what they
called bi-plane tomography, with cuts every
0.5 cm, in order to document with precision
the location and size of the physeal bridge; this
is particularly useful if surgical resection of
160
the bridge is needed. Peterson(88,91), proposes
using ellipsoidal tomography, which can
achieve cuts of up to 1 mm in thickness. In any
case, tomography provides images of limited
definition so that the image re-constructions
achieved with these methods have to be
studied with a considerable margin of error(17).
Advances in nuclear medicine have also
been used for the study of premature arrest
of physeal function. The study of a premature
physeal closure by means of bone scans
will show, once the bone bridge has been
established and stabilized, a reduced or null
uptake of the isotope (Technetium-99) in the
area corresponding to the bridge compared to
the area of normal cartilage(46,47). An Australian
study group(52) proposed an isotopic study
in what they termed apical view with which
a lineal image of the entire physeal area is
obtained, thus eliminating the need for a map
such as the one previously described by means
of tomograms.
Computerized Axial Tomography,
although proposed by some authors in the past
decade(96,117), has not enjoyed the widespread
acceptance in the study of physeal bone
bridges as it has in other medical fields. Its
advantages, in terms of its simplicity and
safety in determining the location and size
of the bone bridge, are clear in flat physes,
but the great inconvenience is its use in the
study of redundant physes, as in the distal
femur, where just the detection of a bridge
can be problematic(23).
Since it began to be used in humans in the
beginning of the 80’s, Magnetic Resonance
Imaging (MRI) has revolutionized imaging
techniques in medicine. The first publications
on MRI applied to the study of the growth
plate date from a few years back(45,49,53,54). Its
great advantage in the study of physeal bone
bridges hinges on the excellent information
it provides on size, shape and location of
the bridges, which is helpful if subsequent
surgical treatment is indicated. Moreover,

Figure 12. MRI (sagital view) of a peripheral physeal
bridge in the anterior aspect of the distal tibia which
has produced a recurvatum deformity at that level.
12 year-old girl.
using sophisticated computer software, tri-
dimensional reconstructions can be obtained
in multiple projections that can render a
very accurate idea of the situation (Peterson
1993, personal communication). Also, the
fact that radiation is not required makes this
technique even more attractive. On the other
hand, the most important disadvantages are
the significant time this technique requires
and the consequent need to sedate younger
patients while they undergo the procedure,
as well as the fact that each study is still
quite costly.
Although the number of publications on
the use of MRI for human physeal bridges
is still limited, it appears to be the most
versatile method and, in our opinion, from
Fractures of the growth plate
a strictly technical point of view, it is the
most recommendable from among those
currently available for the study of physeal
bone bridges.
Types of premature physeal closures
Firstly, depending on its extension, physeal
bone bridges can be divided into two large
groups: total or partial.
Total premature physeal closures tend
fundamentally to produce a shortening of the
affected bone segment while partial closures
usually lead to more complex growth disorders
(shortening plus angular deformity).
Partial physeal closures can be classified,
depending on their location, in peripheral,
central and linear(15,81).
Peripheral bone bridges tend to produce
more or less pronounced angular deformities,
which are quite frequently associated with a
shortening of the involved segment (Fig. 12). In
the case of Ranvier’s groove being significantly
affected, a deformity of the epiphysis can
also result.
Central bridges (Fig. 13) usually produce
bone shortening and sometimes, a characteristic
“tent” shaped epiphyseal deformity(98). If the
bridge is not exactly located in the center of
the growth cartilage it is also quite possible
that the shortening be associated to an angular
deformity.
The third type of partial closure, lineal
bridge, is actually a combination of the two
previous types. According to Bright(15), a
lineal bridge is formed when types III and
IV fractures are not reduced in a satisfactory
way. These bridges generally tend to lead to
shortening and associated angular deformities.
Treatment of premature physeal closures
Management of physeal bone bridges
and consequent growth disorders varies
significantly depending on whether or not
the patient has reached skeletal maturity at
the moment of treatment(30).
161
J. de Pablos, C. Alfaro-Adrián
Figure 13. Central bridge of the distal femoral physis.
It has caused a severe shortening, a slight angular
deformity and a “tent” shaped epiphysis. Left:
X-rays of the lower limbs 2 years preoperatively.
Right: 10 months after lengthening by percutaneous
osteotomy.
-Skeletally immature patients (Algorithm I).
The principal difference between this group
and the group of skeletally mature patients
resides in the existence of open physes with
more or less remaining growth function. This
particular fact allows us to apply techniques
of “physeal surgery” in certain cases.
Calculating properly the skeletal age in
the case of these patients –the method most
commonly used being Greulich and Pyle’s(43)-is
more important and server to first, determine
if there is still remnant growth and second,
to quantify it(34). Methods to predict length
discrepancy at maturity can be used to achieve
162
these two objectives; the methods most utilized
being the so called Arithmetic method(115) but,
above all, the Remnant Growth Graphs(3) and
Moseley’s straight-line graph(71,73).
Another fact that distinguishes these cases is
that, in the case of skeletally immature patients,
bone bridges can be observed as such, whereas
in skeletally mature patients, we observe only
their sequelae.
The first factor we should note in a skeletally
immature patient is the extension of the bone
bridge.
If the bridge occupies less than half of
the physis, and there is sufficient remnant
growth (in girls up to 11 to 12 years and in
boys up to 13 to 14 years of skeletal age), the
treatment of choice, in our opinion, is the
resection-interposition technique described
by Langenskiöld in 1967(60-62). In practice,
this is the only direct treatment of physeal
bridges, due to the fact that all the others, as
we will see, treat the consequence (shortening
and/or deformity) without directly treating
the cause: the bridge. In Lansgenskiöld’s
technique, on the other hand, the bridge is
resected and autologous fat is interposed
aimed to obtain physeal regeneration, which
will not only prevent the reproduction of
the bridge but will also lead to functional
recovery of the growth cartilage. Although
this author and others from his group defend
the theory of physeal regeneration(59,83), we
believe the effectiveness of the method
resides simply in that it prevents the
relapse of the bridge (4). Various authors
have recommended substances other than
fat for interposition among which we could
highlight silicone(14) and low-grade thermal
release acrylic cement(87,88,92). Although it
has been used experimentally to prevent
the formation of bone bridges in severe
physeal fractures(5), we do not believe that
performing this technique in the clinic is
indicated, given the unpredictable evolution
of many untreated fractures. Therefore, this
 Fractures of the growth plate

IMMATURE Patients

Physeal Physeal
bridge >50% bridge <50%
Shortening Mixed RG+ RG-
Shortening+deformity
Deformity Shortening
or mixed
Complete
epiphysiodesis
>10 cm 5-10 cm <5 cm (If RG+)
Shortening Shortening
RG- RG+ >10 cm <10 cm Physeal Lengthening
Distraction Perc. Ost.

Lengthening Lengthening Contralateral Contralateral Lengthening Lengthening Langenskiöld

Perc. Ost. Perc. Ost. Shortening Epiphysiodesis Correction Correction
+ Perc. Ost. Perc. Ost.
+
Contralateral
Shortening
or
Epiphysiodesis
(depending on RG)

RG: Remnant Growth. Sufficient (+) or insufficient (-) according to Anderson & Green graphs.
Perc. Ost.: Percutaneous Osteotomy.

Algorithm I. Management of growth disorders produced by physeal bony bridges in immature patients.

treatment is recommended mainly for bony
bridges once they have been established(77).
Depending upon whether the final correction
with the resection-interposition techniques
has been completed or not, physeal
distraction can be associated if the physis
is still open(21,36,38,44,84). If, on the contrary, the
physis is already closed and correction is not
complete, bone distraction techniques by
means of osteotomy can be performed(30,31).
When remnant growth is not sufficient,
physeal distraction has proven to be very
effective in the treatment of shortenings/
deformities produced by bone bridges
of less than 50% of the physes (see fig. 3
in chapter 39). Although some authors
have associated other procedures prior to
the application of distraction, such as an
osteotomy of the bridge(68), Connolly(25,101)
observed, as has been our experience(4,20,32)
that physeal distraction is able of producing
the disruption of the bridge by itself (see figs.
5, 6 in chapter 14), allowing then lengthening
and/or correction of the involved bone
segment. In our experience in adolescents,
complete closure of the operated physis
frequently occurs following physeal
distraction, therefore we recommend its use
only in children close to skeletal maturity.
Some authors, in order to avoid the relapse
of the bridge following distraction, recommend
interposing substances in Langenskiöld’s
fashion(8). We have experimented with this
idea in young animals and observe that the
interposition of adipose tissue following
distraction could avoid the relapse of a bridge,
which is a constant occurrence when only
using physeal distraction(4). These distraction-
interposition techniques would be of great
utility in the case of very young children, but

163
J. de Pablos, C. Alfaro-Adrián
we do not recommend them, given that they
are technically difficult to perform, and, as
we have observed in adolescents, premature
total closure can still occur. Therefore, in very
immature children, we prefer to initially
use Langenskiöld’s technique, as we had
mentioned previously.
Lastly, there are unusual cases in which
a small, typically central, bone bridge has
produced shortening without angulation,
and there is barely any remaining growth
left. In these cases, an epiphyseal deformity in
the shape of a “tent” is frequently observed,
which makes applying physeal distraction
difficult. Therefore, in such a situation we
recommend using lengthening by means of a
percutaneous osteotomy to correct the length
discrepancy (Fig. 13).
The second principal group of patients,
within the group of skeletally immature
patients, consists of those who present a bone
bridge of over 50% of the physeal total. In these
cases, a simple shortening or mixed disorder
(shortening and angular deformity) is more
likely, while simple angular deformities are rare.
In the case of mixed disorders, especially
if there is significant remnant growth, the
first step is completing the epiphysiodesis in
order to stop the progression of the deformity,
preferably percutaneously (9,10), given that
these techniques are less invasive. With this
treatment, a stable deformity and progressive
shortening will remain which, in our opinion,
should be treated by means of lengthening/
correction by percutaneous osteotomy. If
after calculating the estimated discrepancy
with the prediction charts(3,71), the leg length
discrepancy is expected to be less than 10 cm
then lengthening-correction should be enough.
If, on the contrary, the length discrepancy
is estimated to be greater than 10 cm, we
should consider contra-lateral growth arrest
technique by means of stapling(6,41) or open or
percutaneous epiphyseodesis(10,93) associated
to lengthening/correction on the involved
164
side. If there is no remaining growth, contra-
lateral extemporaneous shortening could be
necessary.
In cases where a massive bone bridge has
produced only progressive shortening of the
injured bone, treatment will depend on the
estimated discrepancy at maturity. If the length
discrepancy is estimated to be between 5 and 10
cm, the ideal choice is performing lengthening
by percutaneous osteotomy. However, if the
length discrepancy is greater than 10 cm., it
is quite possible that a simple lengthening
will not be sufficient and that a technique
of physeal growth arrest or contra-lateral
shortening will also be necessary depending
on patient’s remaining growth.
Lastly, if the calculated length discrepancy
is under 5 cm., we would consider a contra-
lateral arrest, if there is sufficient remaining
growth left or a contra-lateral shortening if
there is not. In these cases, the final height
estimated for the patient is important. If the
patient is going to be of small stature, bone
lengthening could be indicated rather than
considering shortening or arrest techniques,
even in small discrepancies.
-Skeletally mature patients (Algorithm II).
In this section, we will briefly discuss the
treatments that can be offered to skeletally
mature patients, approximately up to twenty
years of age, who present sequelae of old
physeal bone bridges.
Firstly, we will focus on whether the
physeal premature closure has produced a
shortening, angular deformity or a mixed
disorder.
In the case of shortenings with or without
minimal angular deformity, as we observed in
skeletally immature patients, the magnitude
of the length discrepancy is important. If it
is greater than 10 cm, it is very probable that
lengthening by means of a percutaneous
osteotomy alone will not be sufficient, and that
contra-lateral shortening also will be needed,
 Fractures of the growth plate

MATURE Patients
(< 20 Years old)

Shortening Mixed
Shortening+deformity Deformity

Tibial VR Other
>10 cm 5-10 cm <5 cm Femoral VL
Lengthening
Correction
Perc. Ost.
+
Lengthening Lengthening Contralateral Contralateral Progresive Conventional
Perc. Ost. Perc. Ost. Shortening Shortening opening wedge osteotomy
+ (If necessary) osteotomy (closing or opening
wedge)
Contralateral
Shortening

Perc. Ost.: Percutaneous Osteotomy.

VR: Varus. VL: Valgus.

Algorithm II. Management of growth disorders produced by physeal bony bridges in mature patients.

in order to balance the discrepancy. However, to attempt correcting it solely by means of

when the length discrepancy is between 5
and 10 cm, lengthening could be sufficient
without the need for additional procedures.
Lastly, in cases of length discrepancy ranging
between 3 and 5 cm, contra-lateral shortening
of the homologous bone can be considered.
The latter treatment is less indicated when
the patient is short, or when the patient
simply does not accept this treatment, in
which case lengthening with the previously
mentioned techniques can be considered(22).
Pure shortenings of less than 3 cm., in our
opinion, do not require surgical treatment,
as shoe-lifts are sufficient in cases where the
shortening is between 1.5 and 3 cm, and no
treatment is required if the shortening is less.
In mixed disorders, the treatment we
recommend is lengthening-angular correction
by means of percutaneous osteotomy, its great
advantage with respect to more conventional
treatments being that correction of the deformity
and the length discrepancy can be achieved in
a single procedure. Occasionally, as we have
seen, leg length discrepancy is too important
distraction, and it becomes necessary to add
contra-lateral shortening to compensate.
In the cases in which the problem is mainly
the angular deformity, acute correction by means
of closing or opening wedge osteotomies can
be considered. The disadvantage of the first
type is that they produce some shortening
but on the other hand, correction is easier to
achieve than with opening wedge osteotomies.
The most important disadvantages of opening
wedge osteotomies include: difficulty to obtain
correction, potential soft tissue injuries due to
traction and consolidation problems(36) particularly
in the case of severe deformities.
In the lower limb, in cases of tibia vara and/
or valgus of the femur, we have been using for
the past few years the so-called progressive
opening-wedge osteotomy(30,31,39). With respect
to conventional acute corrective osteotomies,
this procedure offers the fundamental advantage
that, as it is progressive, traction injuries are
minimized and correction is more easily obtained.
Another advantage is that, due to the use of
external distractors, it is also possible to adjust

165
J. de Pablos, C. Alfaro-Adrián

A B C D E

F F´
Figure 14. Sequels of a physeal bridge in the inner aspect of the distal tibia after a S-H type IV fracture.
The varus deformity of the ankle is evident in this 16 years-old patient. Correction by percutaneous
osteotomy. A) Preoperative. B) Immediate postoperative. C, D, E) 7, 15 and 30 days postoperative. F)
X-rays 12 months postoperative.

the correction at any moment until the osteotomy REFERENCES

has been consolidated. There no shortening
is produced (an inconvenience presented by
conventional closing-wedge osteotomies) and,
in the correction of tibia vara, fibular osteotomy
is not necessary (Fig. 14).
1. Aitken AP. Fractures of the epiphyses. Clin Orthop
1965;41:19-23.
2. Aitken AP. The end results of the fractured
distal tibial epiphysis. J Bone Joint Surg 1936;18:
685-91.

166

3. Anderson M, Green WT, Messner MB. Growth
and predictions of growth in the lower extremities.
J Bone Joint Surg 1963;45-A:1-14.
4. Azc‡rate J, de Pablos J, Cañadell J. Treatment
of premature partial physeal closure by means
of physeal distraction: An experimental study. J
Pediatr Orthop (B) 1992;1:39-44.
5. Baeza V, Oliete V. Experimental prevention of the
formation of physeal bone bridges by interposition
of different substances. MAPFRE MEDICINA
1993;4 Supl 2:87-91.
6. Blount WP, Clark GR. Control of bone growth
by epiphyseal stapling. Preliminary report. J Bone
Joint Surg 1949;31-A:464-78.
7. Blount WP. Fractures in Children. Baltimore:
Williams and Wilkins, 1955.
8. Bollini G, Tallet JM, Jacquemier M, Bouyala JM.
New procedure to remove a centrally located
bone bar. J Pediatr Orthop 1990;10:662-6.
9. Borges JL, Dabney KW, Bowen JR. Percutaneous
epiphysiodesis for the treatment of limb length
inequalities. Mapfre Medicina 1993;4 Supl 2:165-73.
10. B o w e n J R , J o h n s o n W J . P e r c u t a n e o u s
epiphysiodesis. Clin Orthop 1984;190:170-3.
11. Bowler JR, Mubarak SJ, Wenger DR. Tibial physeal
closure and genu recurvatum after femoral
fracture: Occurrence without a tibial traction
pin. J Pediatr Orthop 1990;10:653-7.
12. Brighton CT. Structure and function of the growth
plate. Clin Orthop 1978;136:22-32.
13. Brighton CT. The Growth plate. Orthop Clin North
Am 1984;15:571-95.
14. Bright RW. Operative correction of partial
epiphyseal plate closure by osseous bridge
resection and silicone rubber implant. J Bone Joint
Surg 1974;56-A:655-64.
15. Bright RW. Physeal injuries. In:Rockwood CA Jr,
Wilkins KE, King RE (ed.). Fractures in children.
Philadelphia: Lippincott, 1984;(vol 3);87-172.
16. Brookes M. The blood supply of bones. London:
Butterworth, 1971.
17. Bruguera JA, Alfaro C, de Pablos J. Detection
of physeal dysfunction by imaging techniques.
MAPFRE MEDICINA 1993;4 Supl 2:15-23.
Fractures of the growth plate
18. Burkhart SS, Peterson HA. Fractures of proximal
tibial epiphysis. J Bone Joint Surg 1979;61-A:996-
1002.
19. Cañadell J, De Pablos J. Lesiones del cartilago de
crecimiento. 2a ed. Barcelona: Salvat, 1988;13-21.
20. Cañadell J, de Pablos J. Breaking bony bridges by
physeal distraction. A new approach. Int Orthop
(SICOT) 1985;9:223-9.
21. Cañadell J, de Pablos J. Correction of angular
deformities by physeal distraction. Clin Orthop
1992;283:98-105.
22. Cañadell J, de Pablos J. Lesiones del Cartílago de
Crecimiento. 2a ed. Barcelona: Salvat, 1988; 238.
23. Cañadell J, de Pablos J. Patología del cartílago de
crecimiento. Rev Ortop Traum 1988;32:255-61.
24. Carlson WO, Wenger DR. A mapping method to
prepare for surgical excision of a partial physeal
arrest. J Pediatr Orthop 1984;4:232-38.
25. Connolly JF, Huurman WW, Lipiello L, Pankaj
R. Epiphyseal traction to correct aquired growth
deformities. An animal and clinical investigation.
Clin Orthop 1986;202:258-68.
26. Cozen L. Fractures of the proximal portion of the
tibia in children followed by valgus deformity.
Surg Gynecol Obstet 1953;97:183-8.
27. Chung SMK, Batterman SC, Brighton CT. Shear
strength of the human femoral capital epiphyseal
plate. J Bone Joint Surg 1976;58-A:94-103.
28. Dale GC, Harris WR: Prognosis in epiphyseal
separation. An experimental study. J Bone Joint
Surg 1958;40B:116-122.
29. De Pablos J, Albiñana J (ed.). Surgery of the Growth
Plate. MAPFRE MEDICINA 1993;4 Suppl 2.
30. De Pablos J, Azcárate JR, Cañadell J. Los métodos
de elongación ósea en el tratamiento de las
deformidades angulares de los huesos largos.
In: De Pablos J, Cañadell J (ed.). Elongación ósea.
Estado actual y controversias. Pamplona: Servicio
de Publicaciones de la Universidad de Navarra,
1990; 331-54.
31. De Pablos J, Barrios C, Azcárate J. Modificación del
aparato de Wagner para la corrección progresiva
de deformidades angulares en los huesos largos.
Rev Ortop Traum 1991;35-IB:489-93.
167
J. de Pablos, C. Alfaro-Adrián
32. De Pablos J, Cañadell J. Correction of angular
deformities by physeal distraction. MAPFRE
MEDICINA 1993;4 Supl 2: 231-8.
33. De Pablos J, Cañadell J. Experimental Physeal
Distraction in immature sheep. Clin Orthop
1990;250:73-80.
34. De Pablos J, Cañadell J. Tratamiento de las lesiones
del cartílago de crecimiento. Pamplona: EUNSA,
1986; 14-7.
35. De Pablos J, Franzreb M, Barrios C. Longitudinal
growth pattern of the radius after forearm fractures
conservatively treated in children. J Pediatr Orthop
1994;14:492-5.
36. De Pablos J, Franzreb M. Treatment of adolescent
tibia vara by asymmetrical physeal distraction. J
Bone Joint Surg 1993;75-B:592-6.
37. De Pablos J. Elongación ósea mediante distracción
fisaria. Estudio experimental (Doctoral Thesis).
Pamplona: Universidad de Navarra. 1984.
38. De Pablos J, Cañadell J. Métodos de elongación ósea y
sus aplicaciones. Pamplona: Servicio de publicaciones
de la Universidad de Navarra, 1989; 52-8.
39. De Pablos J., Azcárate JR, Barrios C. Progressive
opening wedge osteotomy for angular long-bone
deformities in adolescents. J Bone Joint Surg
1995;77B:387-391.
40. Foucher M. De la divulsion des epiphyses. Cong
Med Francia Paris 1863;1:63.
41. González-Herranz J. Experimental arrest of physeal
activity by means of stapling. MAPFRE MEDICINA
1993;4 Supl 2:35-51.
42. González-Herranz P, López JA, Burgos J, Ocete G,
Rapáriz JM, Pérez D. Epifisiolisis desplazadas de
la cabeza radial. Revisión de 42 casos. Rev Ortop
Traum 1990;34:641-4.
43. Greulich W, Pyle S. Radiographic atlas of skeletal
development of the hand and wrist. 2nd ed.
Stanford: Stanford University Press, 1959.
44. Hamanishi C, Tanaka S, Tamura K, Fujio K. Correction
of asymmetric physeal closure. Rotatory distraction
in 3 cases. Acta Orthop Scand 1990;61:58-61.
45. Harcke HT, Synder M, Caro PA, Bowen JR. Growth
plate of the normal knee: Evaluation with MR
imaging. Radiology 1992;183:119-23.
168
46. Harcke HT, Macy NJ, Mandell GA, MacEwen
GD. Quantitative assessment of growth plate
activity. J Nucl Med 1984;25:115.
47. Harcke HT, Zapf SE, Mandell GA, Sharkey CA,
Cooley LA. Angular deformity of the lower
extremity: Evaluation with quantitative bone
scintigraphy. Radiology 1987;164:437-40.
48. Harris WR. Epiphyseal injuries. AAOS Instructional
Course Lectures. 1958;15:206-14.
49. Havranek P, Lizler J. Magnetic Resonance Imaging
in the evaluation of partial growth arrest after
physeal injuries in children. J Bone Joint Surg
1991;73-A:1234-41.
50. Holland CT. Radiographical note on injuries to
the distal epiphyses of radius and ulna. Proc R
Soc Med 1929;22:695-700.
51. Howard CB, Shinwell E, Nyska M, Meller
I. Ultrasound diagnosis of neonatal fracture
separation of the upper humeral epiphysis. J
Bone Joint Surg 1992;74-B:471-72.
52. Howman-Giles R, Trochei M, Yeaters K, Middleton
R, Barrett I, Scougal J, Whiteway D. Partial growth
plate closure: apex view of bone scan. J Pediatr
Orthop 1985;5:109-11.
53. Jaramillo D, Hoffer FA. Cartilaginous epiphysis
and growth plate: Normal and abnormal MR
imaging findings. AJR 1992;158:1105-10.
54. Jaramillo D, Shapiro F, Hoffer FA, Winal SKI
CS, Koskinen MF, Frasso R, Johnson A. Post-
traumatic growth-plate abnormalities: MR imaging
of bony-bridge formation in rabbits. Radiology
1990;175:767-73.
55. Keret D, Méndez AA, Harcke HT, MacEwen GD.
Type V physeal injury: A case report. J Pediatr
Orthop 1990;10:545-48.
56. Kleiger B, Mankin HJ. Fracture of the lateral
portion of the distal tibial epiphysis. J Bone Joint
Surg 1964;46A:25-32.
57. Kumar SJ, Cowell HR, Townsend P. Physeal,
metaphyseal and diaphyseal injuries of the lower
extremities in children with myelomeningocele.
J Pediatr Orthop 1984;4:25-7.
58. La Croix P. The Organization of Bone. Nueva
York: Mc Graw-Hill, 1951.

59. Langenskiöld A. Growth plate regeneration. En: Uthoff
HK, Wiley JJ, editores. Behavior of the Growth Plate.
Nueva York: Raven Press, 1988; 47-50.
60. Langenskiöld A. The experimental basis of treating
premature partial closure of a growth plate by
bone bridge resection and interposition of adipose
tissue. MAPFRE MEDICINA 1993;4 Supl 2:83-4.
61. Langenskiöld A. The possibilities of eliminating
premature partial closure of an epiphyseal plate
caused by trauma or disease. Acta Orthop Scand
1967;38:267-79.
62. Langenskiöld A: Surgical treatment of partial closure
of the growth plate. J Pediatr Orthop 1981;1:3-11.
63. Letts RM. Compression Injuries of the Growth
Plate. In: Uthoff HK, Wiley JJ (ed.). Behavior of the
Growth Plate. New York: Raven Press, 1988;111-8.
64. Mann DC , Rajmaira S. Distribution of physeal
and non-physeal fractures in 2650 long-bone
fractures in children aged 0-16 years. J Pediatr
Orthop 1990;10:713-6.
65. Marmor L. An unusual fracture of the tibial
epiphysis. Clin Orthop 1970;73:132-5.
66. Medina JR. Physeal lesions in the myelodysplasic
patient. MAPFRE MEDICINA 1993;4 Supl 2:141-2.
67. Mizuta T, Benson WM, Foster BK, Paterson DC,
Morris LL. Statistical analysis of the incidence of
physeal injuries. J Pediatr Orthop 1987;7:518-523.
68. Monticelli G, Spinelli R. A new method of treating
the advanced stages of tibia vara (Blount’s disease).
It J Orthop Traum 1984;10:295-303.
69. Morscher, E. Strength and morphology of growth
cartilage under hormonal influence of puberty.
Reconstr Surg Traumatol 1968;10:3-104.
70. Morton KS, Starr DE. Closure of the anterior portion
of the upper tibial epiphysis as a complication
of tibia-shaft fracture. J Bone Joint Surg 1964;46-
A:570-4.
71. Moseley CF. A straight-line graph for leg length
discrepancies. J Bone Joint Surg 1977;59-A:174-8.
72. Moseley CF. Surgical treatment of physeal fractures.
MAPFRE MEDICINA 1993;4 Supl 2:135-40.
73. Moseley CF. The timing of arrest of physeal
activity in the treatment of leg length discrepancy.
MAPFRE MEDICINA 1993;4 Supl 2:151-7.
Fractures of the growth plate
74. Neer CS, Horowitz BS. Fractures of the epiphyseal
plate. Clin Orthop 1965;41:24-31.
75. Ogden JA, Grogan DP. Postnatal skeletal
development and growth of the musculoskeletal
system. In: Albright JA, Brand RA (ed.). The
Scientific Basis of Orthopedics. 2nd ed. New
York: Appleton and Lange, 1987.
76. Ogden JA, Rosenberg LC. Defining the growth plate.
In: Uthoff HK, Wiley JJ (ed.). Behavior of the Growth
Plate. Nueva York: Raven Press, 1988; 1-16.
77. Ogden JA. Current concepts review. The evaluation
and treatment of partial physeal arrest. J Bone
Joint Surg 1987;69-A:1297-302.
78. Ogden JA. Injury of the growth mechanisms of the
immature skeleton. Skeletal Radiol 1981;6:237-53
79. Ogden JA. Skeletal growth mechanism injury
patterns. J Pediatr Orthop 1982;2:371-77.
80. Ogden JA. Skeletal Injury in the child. Philadelphia:
Lea and Febiger, 1982.
81. Ogden JA. The biology and treatment of physeal
arrest. MAPFRE MEDICINA 1993;4 supl 2:216-21.
82. Oliete V. Epifisiolisis traumatica experimental
(Doctoral Thesis). Pamplona: Universidad de
Navarra. 1984.
83. Österman K. Regeneration of the Growth Plate.
MAPFRE MEDICINA 1993;4 Supl 2:85-6.
84. Peltonen J, Karaharju E, Alitalo J: Experimental
epiphyseal distraction producing and correcting
angular deformities. J Bone Joint Surg 1984;66-
B:598-602.
85. Peterson CA, Peterson HA. Analysis of the
incidence of injuries to the epiphyseal growth
plate. J Trauma 1972;12:275-81.
86. Peterson HA, Burkhart SS. Compression injury
of the epiphyseal growth plate: fact or fiction? J
Pediatr Orthop 1981;1:377-84.
87. Peterson HA. Management of partial physeal
arrest. In: Chapman MW (ed.). Operative
Orthopedics. 2nd ed. Philadelphia: WB Saunders,
1993;248-65.
88. Peterson HA. Partial Growth arrest and its
treatment. J Pediatr Orthop 1984;4:246-258.
89. Peterson HA, Madho KR, Benson JT, Ilstoup DM,
Melton J 3rd. (Part 1). Peterson HA (Parts 2 and
169
J. de Pablos, C. Alfaro-Adrián
3). Physeal fractures: Parts 1, 2 and 3. J Pediatr
Orthop 1994;14:423-48.
90. Peterson HA. Premature physeal arrest of the
distal tibia associated with temporary arterial
insufficiency: A case report. MAPFRE MEDICINA
1993;4 supl 2:273-6.
91. Peterson HA. Scanning the bridge. En: Uthoff HK,
Wiley JJ, editores. Behavior of the Growth Plate.
Nueva York: Raven Press, 1988;247-58.
92. Peterson HA. Treatment of physeal bony bridges
by means of bridge resection and interposition of
cranioplast. Mapfre Medicina 1993;4 supl 2:226-30.
93. Phemister DB. Operative arrestment of longitudinal
growth of bones in the treatment of deformities.
J Bone Joint Surg 1933;15:1-15.
94. Poland J. Traumatic separation of the epiphysis
in general. Clin Orthop 1965;41:7-18.
95. Poland J: Traumatic separation of the epiphyses.
London: Smith, Elder y Co., 1898.
96. Porat S, Nyska M, Nyska A, Fields S. Assessment
of bony bridge by computed tomography:
Experimental model in the rabbit and clinical
application. J Pediatr Orthop 1987;7:155-60.
97. Rang M. Children’s Fractures. Philadelphia: JB
Lippincott, 1974.
98. Rang M. Injuries of the Epiphysis, Growth Plate and
Perichondrial Ring. In: Rang M. Children’s Fractures.
Philadelphia: JB Lippincott, 1974;7-17.
99. Rang M. The Growth Plate and its Disorders. Baltimore:
Williams and Wilkins, 1969.
100. Ranvier L. Quelques faits relatifs au dévelopément
du tissu osseux. Comptes Rend Acad Sci 1873;77:1105.
101. Ray SK, Connolly JF, Huurman WW. Distraction
treatment of deformities due to physeal fractures.
Surgical Forum 1978;31:543-6.
102. Roberts JA, Bennett GC, MacKenzie JR. Physeal
widening in children with myelomeningocele. J
Bone Joint Surg 1989;71-B:30-2.
103. Rubin R. Dynamic Classification of Bone Dysplasia.
Chicago: Year Book Medical, 1964.
104. Salter RB, Best T. Pathogenesis and prevention of
valgus deformity following fractures of the proximal
metaphyseal region of the tibia in children. In: Uthoff
170
HK, Wiley JJ (ed.). Behavior of the Growth Plate. New
York: Raven Press, 1988; 189-94.
105. Salter RB, Best T. Pathogenesis and prevention
of valgus deformity following fractures of the
proximal metaphyseal region of the tibia in
children. J Bone Joint Surg 1972;54-B:767.
106. Salter RB, Harris WR: Injuries involving the
epiphyseal plate. J Bone Joint Surg 1963;45-A:587-
622.
107. Salter RB. Salter-Harris Classification of Epiphyseal
plate Injuries. In: Uthoff HK, Wiley JJ (ed.).
Behavior of the Growth Plate. New York: Raven
Press, 1988;97-103.
108. Shapiro F. Epiphyseal growth plate fracture-
separations. A patophysiologic approach.
Orthopaedics 1982;5:720-736.
109. Speed K. Longitudinal overgrowth of long bones.
Surg Gynecol Obstet 1923;36:787-94.
110. S pira E, Farin I. The vascular supply to the
epiphyseal plate under normal and patological
conditions. Acta Orthop Scand 1967;38:1-22.
111. Trueta J. La estructuradel cuerpo humano. Estudios
sobre su desarrollo y decadencia. Barcelona: Labor,
1975.
112. Trueta J, Amato VP. The vascular contribution to
osteogenesis. III. Changes in the growth cartilage
caused by experimentally induced ischemia. J
Bone Joint Surg 1960;42-B:571-87.
113. Trueta J, Morgan JD. The vascular contribution to
osteogenesis. I. studies by the injection method.
J Bone Joint Surg 1960;42-B:97-109.
114. Uhthoff HK, Wiley JJ. Behavior of the Growth
Plate. New York: Raven Press, 1988.
115. White J, Stubbins SJ. Growth arrest for equalizing
leg lengths. JAMA 1944;126:1146-9.
116. Young MH. Changes in the growth cartilage
resulting from ischaemic necrosis of the
metaphysis. J Pat Bac 1963;85:481.
117. Young JWR, Bright RW, Whitley NO. Computed
Tomography in the evaluation of partial growth
plate arrest in children. Skeletal Radiol 1986;15:530-
35.
118. Zionts LE, MacEwen GD. Spontaneous improvement
of post-traumatic tibia valga. J Bone Joint Surg
1986;68-A:680-7.
21 Skeletal growth mechanism injury
patterns
J.A. Ogden
Epiphyseal and physeal injuries, which
are uni­q ue to the developing skeleton,
constitute appro­ximately 15% of all fractures
in children(1,4,9,14,21,29). The first apparent attempt
to clas­sify these injury patterns into 3 types
was propo­sed by Foucher in 1863(6). Poland,
in 1898, clas­sified these fractures into four
types(28). Aitken subsequently designated only
three types(1). Ba­sed on the roentgenographic
appearance and ul­timate prognosis for growth
problems, Salter and Harris recognized five
types of injury(30). Their types 3, 4 and 5 were
associated with a signifi­cant risk of premature
growth arrest, whereas Types 1 and 2 were
allegedly free of long-term complications
such as premature growth arrest.
Histologic corroboration of the various
pat­terns is distinctly lacking, as these injuries
are not usually fatal. However, the general
assump­tion, based principally on animal
experiments, is that the separation (fracture)
occurs within and through the hypertrophic
zone of the physis(30). Some recent histologic
findings will be presen­ted in an accompanying
paper in this volume.
Due to the immense growth potential of
the longitudinal bones in young children,
and the pos­sible multiple-year delay between
injury and even­tual roentgenologic evidence of
premature closu­re, adequate long-term follow-
Reprinted with permission of Mapfre Medicina (vol. 4, suppl 2)
up is essential to ascertain whether any late
onset complications occur(21). Detailed long-
term studies of growth patterns following type
1 and 2 injuries to regions such as the proximal
humerus, distal femur, and proximal tibia have
shown that a generalized lon­gitudinal growth
decrease may affect the injured physis without
roentgenographic evidence of premature
epiphysiodesis or angular deformation(21).
While such decreased length may be only a few
millimeters, it represents subtle, permanent
injury to the entire physis, especially when
con­sidering the fact that the more frequent
respon­se to a fracture involving the immature
skeleton, especially one involving the femoral
shaft, is over­growth.
While the classification scheme of Salter
and Harris has proved to be of immense clinical
im­portance, certain anatomic patterns of injury
can­not be readily classified, complicated combina­
tions of different types occur and recognition
of growth impairment of physeal in types 1
and 2 is minimized. Further, the existence of
the type 5 patho-mechanism compression has
been ques­tioned(27). Injury to other important
chondro­-osseous growth mechanisms such as
the meta­physis, diaphysis, periosteum, zone of
Ranvier, and epiphyseal perichondrium were
not included in the Salter-Harris scheme. It is
also extremely important to remember that
171
J.A. Ogden
temporal anatomic changes at both macroscopic
and microscopic le­vels alter fracture response
patterns at different ages(19,20).
Growth and maturation of the immature
chondro-osseous skeleton occurs in many
different ways(21-23). The previous methods
of descri­bing fractures of the epiphysis and
physis consi­dered the central physeal region
necessary for longitudinal endochondral
ossification. The phy­s is is capable of
latitudinal (diametric) expansion through
the zone of Ranvier. The epiphysis con­tains
a progressively enlarging secondary ossifi­
cation center with its own spherical physis,
which also may be damaged. The periosteum
allows ex­p ansion of the metaphysis and
diaphysis diame­trically, contributing much
of the membranous bone that will mature
into osteon (lamellar) bone with Haversian
systems, progressively replacing the fetal
(woven) bone initially formed by endo­
chondral ossification. Similarly, the epiphysis
en­larges peripherally by the perichondrium,
a struc­ture histologically indistinguishable
from, and continuous with, the periosteum.
Each of these growth mechanisms is variably
vascular depen­d ent (5). The evaluation of
trauma to growing bones must consider the
effect on each and eve­ry one of these growth
mechanisms, as well as their discrete vascular
supplies.
A more comprehensive scheme based
on detailed review of injuries and anatomic
specimens has evolved(14-21). Additions to types
1 and 2 include subtypings to explain the
probable injury mechanisms predisposing to
premature, localized growth plate closure, a
complication being des­cribed with increasing
frequency. With the po­tential for resection
of osseous bridges, the im­portance of early
recognition of growth arrest in all types,
including types 1 and 2, must be ap­preciated.
Furthermore, the treating physician must
realize that there may be a delay, often se­veral
years, between an injury and the eventual
172
Figure 1. Type 1 injury patterns. A) Propagation
across the physeal cartilage. B) Propagation
(arrow) across the diseased primary spongiosa
(e. g., leukemia, thalassemia), with the physeal
interface variably involved. C) Disruption of a
localized segment (arrow) of the physeal.
formation of an osseous bridge, a factor directly
related to the progressive enlargement of
the se­c ondary ossification center and its
morphologic relationship to the permanently
injured area of the physis, which may be quite
small and peri­pheral(14,21).
TYPE 1
The epiphysis and most of the physis
usually separate transversely from the rest
of the physis arld metaphysis, leaving the
germinal region of the physis undamaged
(Fig. 1). Normal undu­lations of the physis,
which may includes small mammillary
processes extending into the meta­physis,
or larger curves such as the quadrinodal
contour of the distal femoral physis, may
cause propagation of the fracture into regions
of the germinal and resting zones of the physis
or into segments of the metaphysis. In infants
and young children, extensive remodeling
and contouring (undulation) of the growth
plate have not usually commenced, so the
fracture line tends to be a relatively smooth,
planar injury.
A subclassification, type 1B, occurs in children
with systemic disorders affecting endochondral
ossification patterns within the metaphysis (e. g.,
myeloproliferative disorders such as leukemia and
thalassemia, or neuromuscular sensory disorders).

Figure 2. Type 2 injury patterns. A) Partial
propagation (arrow) across both the physis and
metaphysis. B) Free and attached metaphyseal
fragments (arrow). C) Propagation (arrow) across
both the primary spongiosa and metaphysis. D)
Localiced disruption (arrow) of the physis at the
point of propagation into metaphysis.
In contrast to type 1A, in which the fracture
un­dulates through the zones of hypertrophic
carti­lage and provisional calcification, a type
1B frac­ture also propagates more extensively
deeply into the zones of degenerating cartilage
and primary spongiosa. Since the germinal
elements usually are undisturbed, subsequent
growth is normal in type 1A or 1B. However,
chemotherapeutic or radiotherapeutic treatment,
as well as expansi­le marrow hyperplasia within
the trabecular in­terspaces in the metaphysis and
the epiphyseal ossification center may impair the
normal growth processes. Thus, the fracture may
not affect growth, but the underlying disease
and its treat­ment might.
A further subclassification, 1C, defines those
less frequent fractures with an associated injury
to a germinal portion of the physis. A localized
region is subjected to either a crushing or tensile
injury that, disrupts all the layers of the physis,
and especially involves the germinal zone. Even­
tually an osseous bridge forms, but only after the
secondary ossification center has developed and
expanded to reach the damaged region. In type
1C cases, the initial injury may occur either before
or after the secondary ossification cen­ter has
Skeletal growth mechanism injury patterns
formed. Once there has been sufficient growth
of the secondary center to reach the ori­ginally
damaged area, the eventualn outcome is the
formation of a discrete osseous bridge across
the physis, similar to the complications of type
3 or 4 physeal injuries.
TYPE 2
The type 2 physeal injury pattern
initially pro­pagates transversely across the
hypertrophic and provisionally calcified zones
of the physis, but then turns to propagate
through a portion of the metaphysis (Fig.
2). This leads to the forma­tion of a variably
sized metaphyseal segment, re­ferred to as the
Thurstan Holland sign, which is diagnostic
of the injury(10,21). It represents re­direction of
fracture stresses into the metaphysis, which,
at many stages of skeletal development and
maturation, is structurzlly (biomechanically)
less able to withstand the propagating fracture
forces than are the adjacent portions of the
phy­sis and epiphysis. Although even the
metaphy­s eal fragment may be separated
microscopically (but not radiographically)
from the physis, the periosteum is usually
intact on the compression­failure side with the
metaphyseal fragment, whe­reas the opposite,
tension-failure side, where separation initially
occurs, is associated with dis­ruptive periosteal
damage. The tendencv of segments of the
periosteum to remain attached to the epiphysis,
physis, and metaphyseal fragment, while
concomitantly separating from the remain­der
of the metaphysis, is due to dense peripheral
attachments of the periosteum into the juxta­
physeal metaphyseal fenestrations, into the
pe­ripheral physis at the zone of Ranvier, and
the blending of the more superficial fibers into
the contiguous epiphyseal perichondrium(31).
The subclassification 2B involves
propagation of the fracture forces on the tensile
side to crea­te a free metaphyseal fragment,
even though it may appear radiographically
173
J.A. Ogden
irtact as the Thurs­tan Holland sign. The free
metaphyseal fragment may make reduction
more difficult and may ne­c essitate open
reduction to stabilize these com­m inuted
fragments.
The subclassification 2C is the inclusion of a
thin layer of metaphysis along with, or instead
of, the larger triangular fragment. This osseous
layer traverses most of the metaphysis. This
sub­type is more common in slowly growing
regions, such as a phalanx, that normally
have increased transverse trabeculation in the
juxtaphyseal me­taphysis (primary spongiosa).
Similar to type 1 injuries, subsequent
physeal growth is infrequently disturbed,
since the ger­minal layers of the physis remain
attached to the epiphysis and the circulation
to the epiphysis is not usually disrupted.
However, normal undula­tions of the physis,
especially in the distal femur, may cause
selective regions of more severe mi­cro inJury.
When the fracture force turns to propagate
in­t o the metaphysis, an angular moment
change is usually produced. Such force-
directional chan­ges may drive a segment of the
metaphysis into or against the physis, causing
comminution (ty­pe 2D) to a localized area.
This appears to be a particular complication
of injuries to the distal femur, distal tibia, and
distal,radius, and certain­ly is of sufficient risk
to warrant long-term fo­llow-up. This type 2D
injury may occur before an ossification center
has formed, as in the afo­rementioned type 1 B.
However, as the secondary ossification center
progressively enlarges, an os­seous bridge
to the metaphysis eventually may become
evident. Since this may be a localized in­jury,
subsequent abnormal growth is likely to be
eccentric and lead to angular deformation.
If a physis has significant normal variations
in contour, which is increasingly likely in
the second decade, rather than maintaining
the relatively smooth, transverse structure,
there may be an increased risk of type 2D
localized damage con­sequent to the shearing
174
forces, causing fracture propagation between
the various regions of the physis as well as
the metaphysis. The distal fe­mur undergoes
progressive development of qua­drinodal
curves in both the coronal and sagittal planes,
with a central, conical region extending
into the rnetaphysis. This central region is
parti­cularly susceptible to more extensive
damage when the fracture propagates across
it during va­rus or valgus displacement. This
anatomic con­touring is not unique to the distal
femur, but cer­tainly may explain its greater
predisposition to subsequent growth injuries,
particularly prema­ture epiphysiodesis, than
most other physeal re­gions. More peripheral
physeal regions, especially those forming
after the injury (i.e., in the zone of Ranvier),
may continue latitudinal or diametric growth.
However, such latitudinal growth may be
impaired, to a varying extent, by the conti­
guous restriction to longitudinal growth.
TYPE 3
This pattern extends from the articular
surfa­ce through the epiphysis, epiphyseal
ossification center (if present), and physis to
the aforemen­tioned relatively mechanically
weak zones of hypertrophy and calcification,
and then extends along the physis toward
the periphery (Fig. 3). In some instances,
transverse fracture propaga­t ion may be
through the primary spongiosa, lea­ving a thin
layer of metaphyseal bone with the epiphyseal
fragment (type 3B). This pattern occurs
frequently in the lateral humeral condyle,
in which there is marked lappet formation
of the pe­riphery of the epiphysis. There is
a tendency for this fracture pattern to occur
when the physis is undergoing the final phases
of physiologic epi­physiodesis. Such an injury
pattern is particularly common in the distal
tibia (Tillaux fracture).
Prognosis for future growth varies
considerably and is contingent upon (a)

Figure 3. Type 3 injury patterns. A) Epiphyseal
fragment (arrow) with propagation through the
physis. B) Epiphyseal fragments (arrow) with
propagation through the primary spongiosa.
C) Crushing injury (arrow) to peripheral physis.
D) Nonarticular cartilage avulsion of the ischial
tuberosity (arrow).
restoration of the con­tinuity of the physeal
and articular cartilages, (b) maintenance
of an adequate circulation to the injured
components, and (c) whether the peri­pheral
area (i. e., zone of Ranvier) is damaged.
Furthermore, a varus or valgus force may
cause localized compressive or tensile failure
in the pe­ripheral physis (type 3C), impairing
its future ca­pacity for growth.
The type 3D subclassification involves
non­articular epiphyseal regions such as the
ischial tuberosity. The epiphysis is avulsed
from the metaphysis and attenuates or
fractures the car­tilaginous/fibrocartilaginous
growth region inter­v ening between the
injured portion of the epi­p hysis and the
remaining, functionally separate portion of
the originally contiguous epiphysis. In some
instances, this connecting region may be
injured significantly and lead to progressive
growth disturbance.
TYPE 4
The fracture involves the articular
surface, ex­tending through the epiphysis
Skeletal growth mechanism injury patterns
Figure 4. Type 4 injury patterns. A) Combined
epiphyseal-physeal-,etaphyseal fragment (arrow).
B) Epiphyseal-physeal-metaphyseal fragments
combined with Type 3A or 3B lesion (arrow).
C) Propagation (arrow) through a nonarticular
epiphyseal region (e. g., intraepiphyseal cartilage
of the developing femoral neck).
(and secondary ossification center, when
present) across the full thickness of the physis
and, subsequently, through a significant
segment of the metaphysis, causing a complete
vertical (longitudinal) split of all zones of the
physis (Fig. 4). If the secon­dary ossification
center is small, the type 4 pat­tern may be
difficult to recognize. The presence of a
metaphyseal fragment witbout evidence of
other physeal separation (either clinically or
ra­diographycally) should make one suspect
a type 4 as well as the more frequent type
2 injury. Growth damage and premature,
localized epiphy­siodesis may occur due to
microscopic injury to regions of the growth
plate, injury to the zone of Ranvier, and
overlap of the metaphyseal and secondary
epiphyseal bone.
The subclassification 4B involves the
aforemen­tioned epiphyseal/metaphyseal unit,
plus the ad­ditional propagation of the fracture
lines through remaining portions of the physis
to create an ac­companying type 3 injury.
This tendency for frag­mentation (epiphyseal
comminution) is more com­mon as the patient
approaches skeletal maturity, a time when the
physis seems more susceptible to different
fracture propagation modes as com­pared to
the younger child. An example is the triplane
fracture of the distal tibia.
175
J.A. Ogden
A type 4C fracture may involve nonarticular
cartilaginous regions, such as the proximal femur,
in which the fracture propagates from the meta­
physis through the contiguous physis into the
epiphyseal region between trochanter and capi­tal
femur. Such a type 4C injury involves meta­physis,
physis; and epiphysis.
TYPE 5
This is an infrequent and difficult to
diagnose injury that usually involves the
weight-bearing epiphyses around the knee
or ankle. While these are articulations that
normally move significantly in only one plane
(flexion-extension), the injury may also involve
an area such as the distal ra­dius. The fracture
force variably disrupts the ger­minal regions
(Fig. 5). According to Salter and Harris, this is
a physeal compression injury(30). Infrequently,
the metaphysis may be driven com­pletely
through the growth plate into the epiphy­sis(21).
However, Peterson and Burkhart have sugges­
ted that direct crushing of the physeal germinal
cells does not occur(27). Instead, they have sug­
gested other etiologies such as prolonged
immo­bilization or neurologic or vascular
dysfunction.
Experiments using metaphyseal-physeal-
epi­physeal composites from calves suggested
that when a direct compression force is applied,
fai­lure is invariably in the metaphyseal
spongiosa, rather than the germinal or
dividing zones of the physis(12). Further, it
shear forces are added, the resultant fractures
may begin to propagate into the germinal
regions. This correlates well with several bones
under study from a patient fatally inJured in
an automobile accident. In each bone there
was a grossly evident compression failure
of a portion of the metaphyseal cortex (to­
rus fracture), accompanied by microscopic
ten­sile disruption of segments of the physis.
No in­tervening fracture propagation was
evident. The failure lines were through various
176
Figure 5. Type 5 injury patterns. Left: Eccentric
disruption (arrow) of the physis. Right: Telescoping
comminution of the metaphysis (arrow) into the
epiphysis.
layers, and of­ten longitudinal in orientation.
These findings suggest a type 5 injury may
have several mecha­nisms of etiology, rather
than just a simple longi­tudinally applied
abnormally high compression force.
Additional mechanisms may lead to the
same type of localized growth arrest. One is
electrical injury (high voltage wires or lighting).
Because of the unique aspects of propagation
of the elec­trical forces through the extremities,
there is highly variable, localized injury to
the growth pla­tes resulting in premature
slowdown of growth and eventual arrest
in certain areas of the physis(26). Another
etiologic factor is irradiation deli­vered for
therapeutic reasons(3). Frostbite may lead to
growth retardation, possibly due to ische­mia
rather than a direct thermal effect on the phy­
seal cartilage(7,8). Decreased arterial supply
to the physis, whether due to extraosseous
or in­traepiphyseal disruption, certainly may
lead to irregular growth(13,21). The physis and
epi­physis seem to assume a very characteristic
co­nical shape in such circumstances. Epiphyseal
vascular damage, especially to the small vessels
supplying the physis, may be an important
me­chanism, rather than direct cell injury, in
some type 5 injuries.
The prognosis in a type 5 injury is poor, since
premature growth compromise almost always

Figure 6. Type 6 injury patterns. Avulsion or crushing
of the peripheral physis or zone of Ranvier (arrow).
occurs. However, such premature growth alte­
ration may not occur until several years after the
initial injury. Growth arrest may be complete,
with premature epiphysiodesis. It also may
na­n ifest as a slowdown of endochondral
elongation (relative to the contralateral bone),
rather than a complete arrest of all growth
potential.
TYPE 6
This pattern (Fig. 6) selectively involves
the peripheral region of the growth plate (the
zone of Ranvier). It results from a localized
contusion or avulsion of the specific portion
of the growth mechanism concerned with
latitudinal or appo­sitional physeal growth.
The injury may result from an avulsion of
the overlying skin and sub­cutaneous tissues,
such as might occur from cat­ching the ankle
in bicycle spokes, a lawn mo­wer, or from
extension of an infection or burn. Because of
the highly selective and localized na­ture of
these particular lesions, peripheral osseous
bridge formation may frequently occur, leading
to localized epiphysiodesis and subsequent
pro­gressive angular deformity.
Involvement of the zone of Ranvier undoub­
tedly occurs in types 3 and 4 physeal injuries
where the fracture propagates to the periphery of
the bone. At such points, localized type 6 da­mage
may occur, increasing the risk of osseous bridge
formation. When treating types 3, 4 or 6, care must
Skeletal growth mechanism injury patterns
Figure 7. Type 7 injury patterns. A) Osteochondral
fragment (arrow) involving the physis and trabecular
bone of the secondary ossification center; B) Chondral
fragment (arrow) involving hypertrophic cells of
the physis of the secondary ossification center.
be taken not to strip the zone of Ranvier away
from the underlying physis when the periosteum
is elevated. This may disrupt the dis­crete blood
supply, as well as directly traumati­zing these
extremely important peripheral germi­nal cells,
and leading to permanent injury.
TYPE 7
These fractures are completely
intraepiphyseal and represent propagation
of the fracture from either the articular surface
or the perichondrial surface into the epiphyseal
cartilage and subse­quently into the secondary
ossification center (Fi­g. 7). They do not involve
the primary phy­sis at all, but rather affect the
spherical physis around the secondary center
of ossification. In nonarticular segments of the
epiphysis the peri­chondrium may be damaged
similar to periosteal damage in many of the
aforementioned injury patterns.
There are two basic types. Type 7A involves
propagation of the fracture through both epi­
physeal and articular cartilage and bone of the
secondary ossification center. The best example
of this pattern is osteochondritis dissecans(11).
Type 7B is more difficult to diagnose and repre­
sents a propagation of the fracture through the
cartilaginous portions, with involvement of some
of the preossifying regions of the expanding
177
J.A. Ogden
Figure 8. Type 8 injury patterns. A metaphyseal
fracture (arrow) temporarily cuts off the nutrient
artery (N), causing transient ischemia to the
metaphyseal segment between the fracture abd
the physis.
se­condary ossification center, analogous to
the hy­pertrophic, fracture-susceptible zone of
the main physis. This may be referred to as a
“sleeve” frac­ture. This type may occur in the distal
tibia. The­se types also may involve nonarticular
regions such as the tibial tuberosity, the greater
trochan­ter, and the fifth metatarsal at its proximal
base.
The Osgood-Schlatter lesion and some of the
other entities classified as “osteochondroses”
may, more appropriately, represent chronic,
stress-related type 7 fractures involving tissue
regions beginning to undergo the normal transi­
tion from cartilage to bone(25). During this chon­
dro-osseous transition phase, if subjected to
high tensile forces (a phenomenon particularly
evident in the tibial tuberosity), the ossification
region may be partially avulsed from the main
portion of the tuberosity. This may occur prior to
the ap­pearance of the ossification center.
TYPE 8
Injuries to the metaphyseal growth and
remo­deling mechanisms represent transient
phenome­na that are particularly related to
vascularity (Fi­g. 8). If a significant fracture
occurs through the normal central and/or
peripheral vascular pat­terns (which may occur
in normal bone as well as pathologic situations),
178
Figure 9. Type 9 injury patterns. Damage to
periosteum (arrow), with or without discrete
osseous injury, discrupts the normal membranous
ossification latitudinal growth mechanism.
the metaphyseal circu­lation involved in the
formation of the primary spongiosa from
the cartilage cell columns is tem­p orarily
disrupted. This causes transient thicke­ning
of the hypertrophic region of the physis, which
may predispose to epiphysiolysis after the
cast is removed, and also leads to failure of
nor­mal osseous remodeling with subsequent,
tran­siently increased osseous density when
the area is revascularized. Experimentally,
Spira and Fa­rin showed that blood vessels
could penetrate from the epiphysis through
the physis to tempo­rarily substitute for the
primary spongiosa meta­physeal vessels in the
rabbit(32). Comparable vascular ingrowth has
not, however, been des­cribed in the human.
TYPE 9
This is a selective injury to the diaphyseal
growth mechanism, which is appositional,
mem­branous new bone formation from the
periosteum (Fig. 9). Any direct injury to the
periosteum causing to the periosteum causing
permanent damage or complete loss (as in
an open injury) may affect the ability of the
bone to remodel and increase cortical volume
circumferentially. This may be associated
with severe fragmentation of a portion of the
diaphysis, and becomes a signi­ficant problem

when the damaged bone requires a thick
diaphyseal cortex for normal biomecha­nical
function, as the tibia does. The periosteum
may be damaged in a localized area and lead to
unusual patterns of extraperiosteal bone forma­
tion(24). Wringer injuries may be associated with
significant avulsion damage to the periosteum(2).
Damage to the interosseous area in paired bones
may cause contiguity of damaged periosteal
ele­ments leading to a synostosis.
While these injuries may not be conceived
of as damaging a growth mechanism, it must be
re­membered that one of the major mechanisms
for longitudinal as well as appositiolnal bone
growth is the control imparted by the highly
osteogenic periosteal sleeve(22,23). Damage to
this soft tissue component by injury must affect
localized areas of diaphyseal bone growth,
either transien­tly or permanently. Furthermore,
significant loss of periosteal growth mechanisms
may also affect intrinsic periosteal control of
longitudinal (phy­seal) growth.
REFERENCES
1. Aitken AP. Fractures of the epiphyses. Clin Orthop
1965;41:19.
2. Akbarnia BA, Campbell CJ, Bowen JR. Ma­nagement
of massive defects in radius and ulna wrin­ger
injury. Clin Orthop 1976;116:167.
3. Arguelles F, Gomar F, Garcia A, Esquerdo J.
Irradiation lesions of the growth plate in rabbits.
J Bone Joint Surg (Br) 1977;59:85.
4. Bouyala JM, Rigault P. Les traumatismes
du cartilage de conjugaison. Rev Chir Orthop
1979;65:259.
5. Brashear HR Jr. Epiphyseal avascular necrosis
and its relation to longitudinal bone growth. J
Bone Joint Surg (Am) 1963;45:1423.
6. Foucher M. De l’divulsion des epiphyses. Cong
Med France (Paris) 1863;1:63.
7. Giedion A. Cone-shaped epiphyses (SCE). Ann
Ra­diol 1965;8:135.
Skeletal growth mechanism injury patterns
8. Hakstian RW. Cold-induced digital epiphyseal
ne­crosis in childhood (symmetric focal ischemic
necro­sis). Can J Surg 1972;15:168.
9. Harris WR. Epiphyseal injuries. AAOS Instr Course
Lectures 1958;15:206.
10. Holland CT. Radiographical note on injuries to
the distal epiphyses of radius and ulna. Proc Roy
Soc Med 1929;22:695.
11. Langenskiöld A. Can osteochondritis dissecans
ari­se as a sequel of cartilage fracture in early
childhood? Acta Chir Scand 1955;109:204.
12. Moen CT, Pelker RR. Biomechanical and histolo­
gical correlations in growth plate failure. J Pediatr
Or­thop 1984;4:180-185.
13. Morscher E. Posttraumatic Zapfenepiphyse. Arch
Orthop Unfallchir 1967;61:128.
14. Ogden JA. Injury to the growth mechanisms of
the immature skeleton. Skel Radiol 1981;6:237-253.
15. Ogden JA. Skeletal growth mechanism injury
pat­terns. J Pediatr Orthop 1982;2:371-377.
16. Ogden JA. Skeletal growth mechanism injury pat­
terns. In: Uhthoff H K, Wiley J J (eds). Behavior of
the Growth Plate. New York: Raven Press, 1988.
17. Ogden JA. Injuries to the growth mechanisms of
long bones. In: Rob C, Smith R (eds). Operative
Surgery (4th ed). Boston: Butterworths, 1989.
18. Ogden JA. Epiphyseal fractures in children. Diagno­
sis and treatment. Video J Orthop Surg 1990; vol.
3, issue 6, part 2.
19. Ogden JA. Injury to the immature skeleton. In:
Tou­loukian R J (ed). Pediatric Trauma St. Louis:
CV Mos­by, 1990.
20. Ogden JA. Skeletal trauma. In: Grossman M, Dieck­
mann RA (eds). Pediatric Emergency Medicine: A
Cli­nician’s Reference. Philadelphia: W B Saunders,
1990.
21. Ogden JA. Skeletal Injury in the Child, 2nd ed.
Phi­ladelphia: WB Saunders, 1992.
22. Ogden JA, Grogan DP. Prenatal skeletal develop­
ment and growth of the musculoskeletal system. In:
179
J.A. Ogden
Albright JA, Brand RA (eds). The Scientific Basis
of Orthopaedics, 2nd ed., New York: Appleton
and Lan­ge 1987.
23. Ogden JA, Grogan DP, Light TR. Postnatal Ske­letal
Development and Growth of the Musculoskeletal
System. In: Albright J A, Brand R A leds). The Scien tihc
Basis of Orthopaedics, 2nd, ed., New York: Ap­pleton
and Lange, 1987.
24. Ogden JA, Pais MJ, Murphy MJ, Bronson ML.
Ectopic bone secondary to vulsion of periosteum.
Skel Radiol 1979;4:124.
25. Ogden JA, Southwick WO. Osgood-Schlatter’s
disease and tibial tuberosity development. Clin
Orthop 1976;116:180.
26. Ogden JA, Southwick WO. Electrical injury
in­volving the immature skeleton. Skel Radiol
1981;6:187-192.
180
27. Peterson HA, Burkhart SS. Compression in­jury
of the epiphyseal growth plate: Fact or fiction? J
Pediatr Orthop 1981;1:377.
28. Poland J. Traumatic Separation of the Epiphyses.
London: Smith, Elder, 1898.
29. Rang M. The Growth Plate and Its Disorders. Balti­
more: Williams & Wilkins, 1969.
30. Salter RB, Harris WR. Injuries involving the
epiphyseal plate. J Bone Joint Surg (Am) 1963;45:587-
598.
31. Speer D. Collagenous architecture of the growth
pla­te and periochondrial ossification groove. J
Bone Joint Surg (Am) 1983;64:399.
32. Spira E, Farin I. The vascular supply to the epiphy
seal plate under normal and pathologic conditions.
Acta Orthop Scand 1967;38:1.
22
Classification of physeal fractures
H.A. Peterson
INTRODUCTION
Injuries of the epiphyseal growth plate
(physis) have been of interest since antiquity.
Historians note the fable of the Amazons,
whose custom of separating the epiphyses of
newborn males assurred female supremacy
and beauty. Hypocrates receives credit for the
first written medical account of this injury.
A Neopolitan surgeon, Marcus Aurelius
Severinus, noted the problem of separation
of the proximal and distal tibial epiphysis in
1632. There followed written observations,
case reports, articles, theses, and treatises, best
summarized in the book by Poland in 1898(52).
Most of these writings attempted to
prove the existence of physeal separation
and to distinguish it from joint dislocation
and fracture of the metaphysis. There were
very few anatomic specimens and virtually
no recorded drawings. There was frequent
mention that this occurred mainly in very
young children. These were regarded as very
rare injuries. This early literature suggests
that none of these authors suspected any
injury other than a complete separation of
the epiphysis (Salter-Harris(61) type I injury).
Malgaigne (1855) noted that the lesion was
rarely confined entirely to the physis, being
almost always accompanied by a fracture
of the metaphysis which adhered to the
epiphysis(52). This may be the first reference
Reprinted with permission of Lippincott-Raven (J Pediatr Orthop 1994;14:439-448).
to the lesion now known as Salter-Harris
type II injury.
In 1863, Foucher(20) reviewed the literature,
described the pathology of the lesion, and
commented on the mechanism of injury. He
was the first to suggest several varieties of
separation and to propose a classification.
Unfortunately, there were no drawings. His
three types include one true injury of the
physis (the epiphyseal separation or Salter-
Harris type I injury). The other two types were
juxta physeal injuries which did not involve
the physis (Fig. 1). With only one fracture
type involving the physis, this can hardly
be called a classification of physeal fractures.
Foucher discussed at length whether these
separations through physeal cartilage should
be called fractures or injuries. He favored the
fracture designation.
Ollier (1867) called the lesions diaphyseal
separations because the separation almost
always took place between the diaphysis and
the cartilage (physis) and not between the physis
and the epiphysis(52). He has a point.
By 1868, Calignon was able to collect 79
published cases, but much of the documen-tation
was incomplete. Prior to this report, the possibility
of these injuries occurring on living subjects was
still doubted by certain authors. Manquat, in
1877, collected 130 cases of published epiphyseal
separations(52).
181
H.A. Peterson
Divulsion Fracture Fracture
épiphysaire épiphysaire préépiphysaire
Mr. Timothy Holmes (1868) may have been
the first to note arrest of development following
lesions of the epiphyseal cartilages. He speculated
that the precise line of discontinuity was the
chief point of importance in the probability of
growth arrest after such injuries. Poncet (1872)
was the first to remark upon the deformities
which result from them. This was done from
observations on the parallel bones of the forearm
(radius and ulna) and leg (tibia and fibula). The
thesis of Dittmayer (1887) dealt with arrest of
growth in length following traumatic separation
of the epiphysis(52).
Poland’s book, Traumatic Separation of the
Epiphysis, in 1898,(52) established the fracture as a
significant and not rare entity. His historical review
to that time was exhaustive. He documented
four specific injuries, provided drawings of each,
and thereby produced the first true classification
182
Figure 1. Classification of
Foucher.
Figure 2. Classification of
Poland.
(Fig. 2). He defined the subject for all future
investigators.
Following Roentgen’s discovery of the x-ray
(1895), the subject was studied more scientifically
since, prior to this, all observations were made from
compound fractures, or dissections of traumatic
amputations and injuries with death(48).
In 1933, Bergenfeldt(6) produced a massive
work of 422 pages. Three hundred and ten
cases in 295 patients seen in Stockholm between
1919 and 1928 are documented. All cases were
radiologically verified and, in most of them,
follow-up radiography was performed. Only 7
patients were lost to follow-up. A classification
of six types was defined (Fig. 3). These six types
included the first three of Poland and added
a fracture through the epiphysis, metaphysis,
and physis. These four fractures subsequently
were used by Salter and Harris as their first

four types as well(61). The type which is now
known as the Salter-Harris type II fracture
was separated into two, one with a very small
piece of metaphysis (Bergenfeldt II), and one
with a large piece of metaphysis (Bergenfeldt
III). This was justified because these two
injuries comprised 81 percent of the entire
series. This was the first study delineating
relative frequency of fracture types. The sixth
fracture type was a juxta epiphyseal fracture
through the metaphysis 2 to 3 mm from the
physis. Bergenfeldt noted that this fracture
may cause stripping of the periosteum of the
metaphysis to the physis which may cause
premature growth arrest. This work was
highly significant and should have become
the standard classification. It may have been
overlooked in the English literature because
the original text was in German.
Classification of physeal fractures
Figure 3. Classification of
Bergenfeldt, with percentage
of each type.
Figure 4. Classification of
Aitken.
Aitken(1) in 1936, in discussing physeal
injuries of the distal tibia, found three types
of fractures (Fig. 4). Two of these (I & II)
had been shown by Poland. Aitken added
a third type which later would become the
Salter and Harris type IV fracture(61). Aitken
documented the same three physeal injuries
while discussing fractures involving the
distal femur in 1952(4) and the proximal
tibia in 1956.(3) In 1965, he wrote an article(2)
discussing these three types of fractures in a
general context thereby becoming applicable
for all physeal injuries. Since Poland’s type
III and IV were very similar (Poland’s type IV
is a “double” type III), Aitken’s three types
of fractures became the standard by which
most people reported physeal fractures for
the next 25 years. Actually all three types had
been previously reported by Bergenfeldt(6).
183
H.A. Peterson
AP Lat.
Figure 5. Type II fracture of Johnson and Fahl.
The next proposed classification was by
Johnson and Fahl(27) in 1957. They described,
for the first time, ten cases of what later
became known as the triplane fracture(49). They
designated this their type II fracture (Fig. 5)
maintaining the same fractures as Aitken
for types I and III. Since the triplane fracture
traverses metaphysis, physis, epiphysis and
usually articular cartilage, it meets all criteria
for Bergenfeldt V, Aitken III, and Salter-Harris
IV fracture.
In 1963 Salter and Harris(61) published their
classic article entitled, “Injuries Involving
the Epiphyseal Plate.” The article is well
illustrated by drawings and radiographs and
comprises five types (Fig. 6). The first four
types are a combination of those described by
Poland (types I-III), Bergenfeldt (types I-V),
and Aitken (types I-III). A new fracture was
added. This was the compression injury which
they designated type V. They proposed that
the mechanism of injury was by longitudinal
compression damaging only physeal cells
(germinal layer). There was no osseous injury,
and radiographs at the time of injury were,
by definition, normal. This is different than
the crushing of physeal cells that can occur
with any physeal fracture as described by
184
Figure 6. Classification of Salter and Harris.
Letts(32). Since no structure is broken, this is
not a fracture. The term injury seems more
appropriate.
Salter and Harris reported no statistics on
the relative frequency of fracture types and no
data regarding gender, age, mechanism of injury
or outcome. They did, however, state that the
prognosis for these fractures could be based
on the radiographic type. Salter continued
to emphasize the prognostic value of this
classification as late as 1988(60), despite a growing
concern to the contrary(13,33,38,62,66). The prognosis
for premature growth arrest is now felt to be
related to a combination of factors, including
the specific physis injured, the force of injury, the
degree of displacement and comminution, and
age, as well as the type of fracture. Treatment
is also important.
Salter’s associate, Mercer Rang(53), added
an injury which has become known as a
Salter-Harris type VI. This was described
as a rare injury such as a direct blow to the
periosteum or perichondral ring (Fig. 7). It
was never specified whether the damage
was produced by peripheral transverse
compression of physeal cells or ischemia
due to vascular changes. Since no mention
was made of open trauma it is assumed that
these were closed injuries. Like the Salter-
Harris type V this should also be called
an injury rather than a fracture since the
original radiograph would be normal. Other

Figure 7. Physeal injury of Rang.
authors(30,42-44,71) have interpreted this injury
as being an avulsion of the perichondral ring
with portions of attached metaphyseal and
epiphyseal bone, yet designated as a Rang
or Salter-Harris type VI. Though drawings
have been provided, the only case depicted
radiographically(44) is an open lawnmower
excision of metaphysis, physis, and epiphysis,
which is more appropriately classified as
a part missing (see Physeal Fractures: Part
II. Two Previously Unclassified Types. JPO
1994;14). None of these type VI were found
in the Olmsted County study (see Physeal
Fractures: Part I. Epidemiology in Olmsted
County, Minnesota, 1979-1988. JPO 1994;14).
Interestingly, neither Salter(60) nor Rang(54)
included this type in subsequent publications.
The Salter-Harris classification gained
widespread acceptance throughout the world.
In recent years, however, several authors
have deviated from this classification.
Weber(71), in 1980, being unable to find any
type V injuries, chose to return to the Aitken
classification. Rang(54) notes that the Aitken
classification is “widely used” and Kling(30)
recently (1993) stated that it is “now used in
Europe”. Other authors(7,16,18,42,62,65), finding
the classification incomplete or lacking in
substantiation of prognosis, have developed
new classifications.
Most notable of these new classifications
are those of Ogden and Shapiro. Ogden(42)
Classification of physeal fractures
(1981) proposed a classification of 9 types
with 11 subtypes producing 20 types. The first
5 types are those of Salter and Harris. Type
6 is that of Rang. Types 7, 8, and 9 involve
the epiphysis, metaphysis and diaphysis,
respectively, and though they do not involve
the physis directly, they occasionally have
implications concerning growth. Though
this classification and the author’s depictions
of growth arrest with each type are valid, it
has not gained widespread use, probably
because the multiple subtypes are too difficult
to remember and because types 7, 8, and 9
are common non-physeal fractures which
rarely result in growth arrest.
Shapiro’s pathophysiologic classification
(1982) (62) is an attempt to better predict
prognosis. Shapiro correlates the osseous
injury with the epiphyseal circulation to the
epiphyseal osteoprogenitor cells and the
metaphyseal circulation to the metaphyseal
osteoprogenitor cells. By superimposing
the pathophysiologic classification on the
pathoanatomic classification Shapiro attempts
to better predict future physeal bone bridge
formation. No new anatomic types were
described in this scheme.
Other authors have proposed separate
classifications for different areas of the body
feeling that the Salter-Harris classification
does not apply as well(7,16,18).
This search for a classification which will
allow the collection of meaningful statistical
data and a better means of communication is a
natural progressive quest for knowledge. This
knowledge, in turn, should improve criteria
for prognosis, management, and follow-up of
patients with growth plate fractures.
A NEW CLASSIFICATION
The 951 physeal fractures reviewed in the
Olmsted County study and the two physeal
fracture types reported in Physeal Fractures:
Part II. Two Previously Unclassified Types (JPO
185
H.A. Peterson

Metaphysis Metaphysis Physis Epiphysis & Metaphysis & Physis

physis & physis physis physis missing
& epiphysis
Poland II Foucher I Poland III & IV
Bergenfeldt V
Bergenfeldt II & III Poland I Bergenfeldt IV
Aitken III
Aitken I Bergenfeldt I Aitken II
Salter & Harris IV
Salter & Harris II Salter & Harris I Salter & Harris III

Figure 8. Classification of Peterson.

transverse metaphyseal sclerosis(43). There is

Figure 9. Peterson Type I fracture.
1994;14) provide data from which to propose a
new classification. The classification is arranged
with the least involvement or damage of the
physis (type I) progressively to the greatest
damage (type VI) (Fig. 8).
Type I is a transverse fracture of the
metaphysis with extension to the physis,
detailed in Physeal Fractures: Part II. Two
Previously Unclassified Types (Fig. 9). There
may be a small eccentric cortical fragment not
attached to either epiphysis or metaphysis,
which is therefore not a Thurstan Holland
sign(23). The mechanism of injury is most likely
longitudinal compression as evidenced by the
cortical torus or buckling and the subsequent
only minimal disruption of physis (only if
there is an eccentric cortical fragment) and
no displacement of epiphysis on metaphysis.
Comminution is common, compounding rare.
Radiographs two to four weeks post injury
typically show trans-metaphyseal sclerosis
indicative of a healing compression fracture.
This fracture comprised 15.5% of fractures in
the Olmsted County study. The most common
sites are distal radius, finger phalanges, and
metacarpals. Nonoperative treatment by
closed reduction and immobilization usually
results in a good outcome. Only one case
(0.7%) was treated surgically in the Olmsted
County study. Premature physeal closure
occurred in 5 (3.4%) patients, none of which
required treatment.
Type II is a separation of a part of the
physis with a portion of the metaphysis
attached to the epiphysis (Thurstan Holland
sign(23)). Involvement and potential damage
of the physis may be minimal (Fig. 10A) or
progressively greater (Fig. 10B) until nearly all
the physis has been disrupted leaving only a
small metaphyseal fragment (Fig. 10C). This
metaphyseal fragment, being large or tiny, is

186

Figure 10. Peterson Type II fracture.
the reason Bergenfeldt designated each as a
separate type (Fig. 3, types II & III). Though
attention is usually focused on the size of the
metaphyseal fragment, the more important
factor is the amount of physeal tissue
disrupted. Indeed, the Thurstan Holland
metaphyseal fragment may be so tiny that it
is not visualized on routine anteroposterior
or lateral radiographs (Fig. 10C). Tangential
(oblique) views may be necessary to visualize
the fragment. In this case it differs little from
a type III fracture (Fig. 8) which involves
complete physeal disruption with no
osseous fracture. This fracture (Fig. 10C)
and the type III fracture can be managed
similarly, usually by closed reduction and
immobilization and probably have the same
outcome. The metaphyseal portion attached
to the epiphysis usually comprises 1/4 to 1/3
of the width of the physis (Fig. 10B). There
are no recorded cases of premature physeal
closure between the metaphyseal fragment
and the epiphysis. Brashear (9), applying
longitudinal compression by bending the
joints of rat knees, produced a type II fracture
each time. None of these developed physeal
closure at the compression site (metaphyeal
fragment-epiphyseal interface).
Regardless of the amount of physis disrupted,
the essential features of the type II fracture
are 1) disruption of a portion of the physis
Classification of physeal fractures
between the epiphysis and the metaphysis,
however small this may be, 2) a metaphyseal
fragment attached to the epiphysis, and 3)
no continuity from the epiphysis to the intact
major metaphyseal-diaphyseal complex. This
fracture is the same as Poland II, Bergenfeldt II
& III, Aitken I, and Salter-Harris II. Comminution
and open fracture are uncommon. This fracture
is the most common type and comprised 53.6%
of fractures in the Olmsted County study. The
most common site of this fracture is in finger
phalanges where it occurred 47.6% of the time.
Initial management was surgical for 23 (4.5%)
patients. Thirty-three (6.5%) developed premature
physeal closure. Twelve (2.4%) underwent late
surgical correction.
Type III is a separation of the epiphysis
from the diaphysis through any of the
layers of the physis disrupting the complete
physis (Foucher I, Poland I, Bergenfeldt I,
Salter-Harris I) (Fig. 8). Though no bone is
disrupted, the physeal cartilage is broken
and thus this may be called a fracture. This
fracture cannot be comminuted. The only
anatomic variations are the different layers
of the physis through which the fracture
traverses; at present this can be determined
only histologically. In one human distal
tibial physis, this transphyseal fracture was
histologically noted to involve all zones
of cartilage cells (germinal, proliferating,
hypertrophying, and provisionally calcified)
and helps explain why premature growth
arrest sometimes occurs following this
fracture (64). Compound (open) injury is
rare. This fracture comprised 13.2 percent
of physeal fractures in the Olmsted County
study. It occurs most commonly in the distal
fibula (in the author’s estimation, however,
type III fracture of the distal fibula is the
most commonly overdiagnosed fracture in
pediatric orthopedics). Surgical treatment
of the acute fracture was employed in 13
cases (10.3%). Nine cases (7.1%) had late
corrective surgery.
187
H.A. Peterson
Type IV is a fracture of the epiphysis
extending to and along the physis (Poland III &
IV, Bergenfeldt IV, Aitkin II, Salter-Harris III)
(Fig. 8). It may be comminuted or “double” as
noted by Poland (Fig. 2, type IV). Compound
fractures are uncommon. This fracture most
often occurs when a portion of the physis,
usually central, has begun to close. Therefore
it is more commonly seen in older children
(see Physeal Fractures: Part I. Epidemiology
in Olmsted County, Minnesota, 1979-1988).
Since the articular surface is disrupted, this
fracture is best managed by anatomic reduction
and maintenance of reduction. This often
means open reduction and internal fixation.
Premature growth arrest is common, but is
usually complete and not partial. Thus, there
is rarely angular deformity. Since most of the
children are relatively mature, bone length
discrepancy is uncommon. Significant length
discrepancy occurs only in the less common
young patients. This fracture comprised 10.9%
of fractures in the Olmsted County study. The
most common sites are finger phalanges and
the distal tibia (medial malleolus and lateral
plafond). Eighteen fractures (17.3%) were
treated by initial surgery, and 15 (14.4%) by
late surgery.
Type V is a fracture that traverses the
metaphysis, physis, and epiphysis (Fig. 8).
It usually, but not always, also traverses
the articular cartilage(49). This is the same as
Bergenfeldt V, Aitkin III, and Salter-Harris
IV. The triplane fracture(49) meets all these
criteria (Fig. 5) and is therefore a complex
type V, which is usually depicted in only one
plane. Comminution and compounding are
frequent. Type V fractures are best managed
by anatomic reduction and maintenance of
reduction to align both the articular cartilage
and the growth cartilage. This is particularly
true in the young patient with significant
growth remaining. Premature growth arrest
is common and occurs even with anatomic
reduction. This fracture comprised 6.5% of
188
Figure 11. Peterson Type VI fracture.
fractures in the Olmsted County study. The
most common sites are the distal humerus
(lateral condyle), finger phalanges, and distal
tibia where the fracture pattern is variable(15).
Twelve fractures (19.4%) were treated initially
by surgery and twelve (19.4%) by subsequent
surgery.
Type VI is a fracture where a portion of the
physis has been removed or is missing (Fig.
11) and is documented in Physeal Fractures:
Part II. Two Previously Unclassified Types.
Usually, but not always, an accompanying
portion of the epiphysis or metaphysis, or
both, is also missing. This occurs only with
open or compound fractures. Frequent inciting
trauma are injuries involving the lawn mower,
farm machinery (auger, corn picker, power
take-off, corn sheller), motor boat propeller,
snowmobile, and gunshot missiles. Rang(54)
reported this injury in the distal tibia produced
by a motor vehicle accident and Ogden(44) in
the distal fibula produced by a lawnmower.
Premature partial closure of the remaining
physis nearly always occurs, but sometimes
not until years later. This fracture comprised
only 0.2% of fractures in the Olmsted County
study, but is more common among referral
patients. All (100%) require initial surgery, at
least wound care, and most will require late
reconstructive or corrective surgery, especially
in young children.
 Classification of physeal fractures

DISCUSSION fractures might have been significantly higher,

This new classification has a sound
anatomic basis. It depicts physeal tissue
injury as a continuum (Fig. 8) from
relatively insignificant involvement (type
I), to progressively more involvement (type
IIA-C), to complete transphyseal disruption
(type III), to transphyseal disruption with
epiphyseal fracture which ensures damage
to the germinal layer of cells (type IV), to
longitudinal disruption of epiphysis, physis
and metaphysis (type V), to removal or loss
of some of the physeal cartilage (type VI).
There is an epidemiologic basis for the
classification as well. The Olmsted County
study, as well as all previous studies, show
type II to be the most common (Table 1). Type
II fracture is followed in order by types I, III,
IV, V, in the Salter-Harris classification (Table
1) and by types I, III, IV, V, and VI in this
new classification (Table 2). In the Olmsted
County study only physeal injuries were
reviewed. Had there also been a review of
fractures of the metaphysis (particularly of
the distal radius) and if these fractures had
oblique radiographs, the frequency of type I
possibly even higher than type II. This seems
natural since it is well known that fractures
of the metaphysis of long bones are the most
common fracture in children(31). Thus, the
frequency of all fractures in children could be
on a decreasing continuum from fracture of
the diaphyseal-metaphyseal complex, to type
I physeal fracture, progressively diminishing
to type VI physeal fracture.
There is also a prognostic basis for this
classification, as determined by the numbers
of each fracture type treated by surgery (both
immediate and late) in the Olmsted County
study group (Table 2). Since there is potential
for more physeal damage in each ascending
type, the amount of both immediate
surgery and late surgery correspondingly
increased. Type I fracture rarely developed
a complication (premature closure, angular
deformity, length discrepancy, or loss of
function), while type VI always did. The
low percentage of complications in type
I and II, particularly growth arrest, that
resulted in late surgery also suggests that
the complications in these two types may be

Table 1. Distribution of physeal fractures by type recorded in the English literature (Salter and
Harris classification)

Year Author I II III IV V Other Total

1933 Bergenfeldt(6) 23 251 19 13 0 4 310
1970 Rogers(58) 7 89 9 12 1 118
1974 Oh*(45) 34 73 14 12 0 133
1979 Mbindyo(36) 18 42 4 5 2 71
1986 Worlock(72) 30 121 5 15 0 191
1987 Mizuta(38) 30 257 23 42 1 353
1990 Mann*(35) 210 483 143 102 5 943
1994 Peterson x 126 510 104 62 0 149 951
Total 448 1705 316 248 9 153 2879
Percentage 15.6 59.2 11.0 8.6 0.3 5.3 100

# Incidence series of only one anatomic site not included

* Includes only: humerus, radius, ulna, femur, tibia, and fibula
x Physeal Fractures: Part I. Epidemiology in Olmsted County, Minnesota, 1979-1988

189
H.A. Peterson
Table 2. Number and surgery performed of physeal fractures by type among children in
Olmsted County, Minnesota, 1979-1988 (Peterson classification)
I II
Number (%) 147 (15.5) 510 (53.6) 126 (13.2) 104 (10.9) 62 (6.5)
Immediate Surgery (%) 1 (0.7) 23 (4.5)
Late Surgery (%) 0 (0) 12 (2.4)
less severe or less of a clinical problem than
those in the other types. With additional
follow-up the numbers of late surgical cases
may increase. For example, nearly all type
VI cases in our referral practice are treated
with late reconstructive surgery. This again
underscores the need for well-documented,
population-based, long term follow-up
epidemiologic studies.
The low incidence of type VI fractures in the
Olmsted County study was puzzling, especially
compared with our referral practice. However,
these severe injuries are more likely to be referred
to a medical center than uncomplicated ones.
Moreover, cases of open fractures were often
indexed as farm injuries, lawn mower injuries,
etc., and not as physeal injuries and therefore may
have been missed. As did our 1972 study(48), this
suggests a need for better and more complete
indexing of all diagnoses for every trauma
patient. This is best accomplished during the
initial emergency room or operating room
evaluation.
Thus, it is possible, maybe even likely, that
the most common physeal injury is the one
with the least amount of physis injured (type I)
and that the incidence progressively decreases
with progressively more involvement of the
190
III IV V VI Total
2 (0.2) 951 (100)
13 (10.3) 18 (17.3) 12 (19.4) 2 (100) 69 (7.3)
9 (7.1) 15 (14.4) 12 (19.4) 1 (50) 49 (5.2)
physis (types II-VI). If this proves to be true
then this classification would also have greater
relevance to prognosis. The higher the type
number, the more the physis is damaged, the
greater the need for immediate or late surgery.
Obviously, other factors such as anatomic
site, force of injury, degree of comminution,
amount of displacement, skeletal maturation
(age), and treatment are all vitally important
and, in specific cases, are more important
than type of fracture. For example, a type III
fracture of the distal fibula rarely develops
physeal arrest, while a type III fracture of the
distal femur has a high likelihood (nearly
always) of developing physeal arrest. This
is due to the small uniplanar distal fibula
physis compared with the large, irregular,
undulating physis of the distal femur.
When all factors are considered, the
prognosis of a physeal injury depends
upon these factors in descending degree
of importance: 1) the severity of injury,
including displacement, comminution, and
open versus closed; 2) age of the patient,
3) the physis injured, and 4) type of fracture.
Treatment is dependent on these factors
and in itself also has an important bearing
on prognosis.

Peterson
1969 Rang
1963 Salter & Harris
1938 Aitken
1933 Bergenfeldt
1898 Poland
1863 Foucher
Figure 12. Comparison of classifications of physeal fractures.
Comparison of classifications may have
more than historical value (Fig. 12). Future
new mechanisms of injury and future imaging
techniques may lead to inclusion of new or of
a previously described, but discarded, fracture
type.
Compression injury of the physis without
fracture (Salter-Harris (61) type V) was not
encountered in the Olmsted County study.
It is an interesting concept which proposes
that the physis can be subjected to sufficient
longitudinal force to compress the physeal
germinal cells without injuring any bone
trabeculae in the epiphysis or metaphysis. Since
no bone is broken and no physis disrupted,
this would be better called an injury than
a fracture. By definition radiographs are
negative and premature growth arrest is only
discovered months or years later. The Salter-
Classification of physeal fractures
Harris classification is the only classification
which includes this injury.
In 1979 Burkhart and Peterson (12)
presented two Salter-Harris Type V injuries
among a series of proximal tibial physeal
fractures. These were the only two type V
injuries of the proximal tibia on record. On
closer review of the original radiographs
fractures were noted (one was a Salter-Harris
type I and one was a type IV). Indeed, even
the example given by Salter and Harris(61)
is a follow-up radiograph and has many
features of a healed, previously displaced
Salter-Harris IV fracture. The radiograph
taken at time of injury is not shown. We then
(1981) wrote an article(51) questioning the
existence of the Salter-Harris type V injury
and proposed that in order to prove the
occurrence of such an injury, the following
191
H.A. Peterson
criteria should be met: 1) a documented injury
with negative radiographs in at least two
planes; 2) no treatment, and 3) documented
growth arrest weeks, months, or years later.
A plea was made for future investigators
to document such cases. None have been
published to date.
The Salter-Harris type V injury is not
included in this new classification of fractures
for the following reasons. It is not a fracture.
It is extremely rare, if it occurs at all (Table
1). There were no such occurrences in the
Olmsted County study. There are no cases in
the Mayo Clinic files (4,400,000 registrations)
in local or referral cases. Rang(54) in 1984
stated that the Salter-Harris type V injury
is so rare “there is much to be said for retiring
the term altogether. Bony bridging should
be regarded as a potential complication
of any growth plate injury and not as a
special type of injury”. Cases reported in
the literature are uncommon, are usually a
rare occurrence in a series, and details of the
cases are usually not provided. When they
are, there is invariably an associated fracture
or injury which has resulted in traction or
cast immobilization(5,12,13,24,26,28,29,39,57,58,63,66). In
these cases, one or more of the uninjured
physes in the injured extremity developed
physeal arrest. The premature closure has
always been complete and never partial
as depicted in the drawing by Salter and
Harris(61). Many cases of premature complete
physeal closure have been documented from
disuse, traction and cast immobilization even
when there was no fracture, such as closure of
the distal femoral and proximal or distal tibial
physes during immobilization or traction
treatment for congenital hip dislocation,
rheumatoid arthritis, polio, tuberculosis,
Perthes disease, etc.(8,17,19,34,46,56,57,59). Arterial
spasm associated with traction and even the
application of a cast alone are both known
to reduce blood flow to the extremity(25,40).
Reduced blood supply is known to alter
192
physeal growth (10,14,41,47,50,67-70). Attempts
to produce growth arrest by longitudinal
physeal compression in animals have been,
for the most part, unsuccessful(9,21,43,55). Two
experimental studies support the hypothesis
of a Salter-Harris type V injury. One used in
vitro growth plate cartilage explants and the
authors(22) hypothesized “that there might
be an unknown pathogenetic mechanism”
in addition to a high longitudinal force. In
the other study(37), only the rats in which the
ipsilateral femur also fractured developed
physeal arrest. These authors concluded
that the relationships among mechanical,
metabolic, and circulatory factors require
further study. The final reason for not
including this injury in a classification of
physeal fractures is that, since the initial
radiograph is normal and growth arrest is
discovered only in retrospect, it is of no benefit
in evaluating or treating an acute injury.
An open mind should be kept concerning
the compression injury. It may exist. If it
occurs it is extremely rare(11,30,32,38,43,45,54,72)
(Table 1) and might be considered an oddity.
Perhaps it would be more appropriately
included in a classification of physeal
“injuries” along with disuse, immobilization,
frostbite, thermal and electric damage, and
vascular impairment, all of which have
normal initial radiographs with premature
physeal arrest noted only months or years
later. Accepting premature physeal closure
as being due to undocumented growth
plate germinal cell compression obviates
innovative thought and investigation of
other possible underlying causes which
may be avoided or treated.
Future investigation of any problem
related to physeal fracture needs critical
analysis of radiographs. Supplemental
imaging including multiple tangential views,
tomograms, computerized tomography,
magnetic resonance imaging, and arthrograms
may, on occasion, be beneficial in determining

the precise fracture pattern. A classification
which includes all major fracture types should
be adopted. Epidemiologic studies should
include all body locations including the pelvis
and spine.
REFERENCES
1. Aitken AP: The End Result of the Fractured Distal
Tibial Epiphysis. J Bone Joint Surg 1936;18:685-
691.
2. Aitken, AP: Fractures of the Epiphysis. Clin Orthop
Related Research 1965;41:19-23.
3. Aitken AP, Ingersoll RE: Fractures of the Proximal
Tibial Epiphyseal Cartilage. J Bone Joint Surg
1956;38A:787-796.
4. Aitken AP, MaGill HK: Fractures Involving the
Distal Femoral Epiphyseal Cartilage. J Bone Joint
Surg 1952;34(A):96-108.
5. Beals RK: Premature Closure of the Physis
Following Diaphyseal Fractures. J Pediatr Orthop
1990;10(6):717-720.
6. Bergenfeldt E: Beiträge zur Kenntnis de
Traumatischen Epiphysenlösungen an den Langen
Röhrenknochen der Extremitäten. Eine Klinisch-
Röntgenologische Studie. Acta Chir Scand 1933;73;
(Suppl) 28:1-422.
7. Boissevain ACH, Raymakers ELFB: Traumatic
Injury of the Distal Tibial Epiphysis: An Appraisal
of Forty Cases. Reconstr Surg Traumatol 1979;17:40-
47.
8. Botting TDJ, and Scrase WH: Premature Epiphyseal
Fusion at the Knee Complicating Prolonged
Immobilization for Congenital Dislocation of
the Hip. J Bone Joint Surg 1965;47B:280-282.
9. Brashear HR, Jr: Epiphyseal Fractures: A
Microscopic Study of the Healing Process in Rats.
J Bone Joint Surg 1959;41A:1055-1064.
10. Brashear HR, Jr: Epiphyseal Avascular Necrosis
and Its Relations to Longitudinal Bone Growth.
J Bone Joint Surg 1963;45A:1423-1438.
Classification of physeal fractures
11. Bright RW: Physeal Injuries. In: Fractures in
Children, ed by CA Rockwood, Jr, KE Wilkins,
and RE King, Chapter 2, New York, JP Lippincott,
1991, pp 87‑170.
12. Burkhart SS, and Peterson HA: Fractures of
the Proximal Tibial Epiphysis. J Bone Joint Surg
1979;61A:996-1002.
13. Bylander B, Aronson S, Egund N, Hansson LJ, and
Selvik G: Growth Disturbance After Physeal Injury
of Distal Femoral and Proximal Tibia Studied by
Roentgen Stereophotogrammetry. Arch Orthop
and Traumatic Surg 1981;98:225‑285.
14. Caffey J: Traumatic Capping of the Metaphysis
of Growing Bones. Am J Roentgenol 1970;108:451-
460.
15. Cass JR and Peterson HA: Salter and Harris Type
IV Injuries of the Distal Tibial Epiphyseal Growth
Plate With Emphasis on Those Involving the
Medial Malleolus. J Bone Joint Surg 1983; 65A(8):
1059-1070.
16. Chadwick CJ, and Bentley G: Chadwick and
Bentley Classification of Distal Tibial Growth
Plate Injuries. In: Behaviour of the Growth Plate,
ed by NK Uhthoff and JJ Wiley, New York, Raven
Press, pp. 105-110, 1988.
17. Currarino G: Premature Closure of Epiphyses in the
Metatarsals and Knees: A Sequel of Poliomyelitis.
Radiology 1966;87:424-428.
18. Dias LS, and Tachdjian MO: Physeal Injuries of
the Ankle in Children: Classification. Clin Orthop
1978;136:230-233.
19. Gill GG: The Cause of Discrepancy in the Lengths
of the Limbs Following Tuberculosis of the Hip
in Children. J Bone Joint Surg 1944;26:272-281.
20. Foucher JTE: De la Divulsion des Epiphyses. Cong
of Med de France 1:63-72, 1863. (Reprinted in English
in Clin Orthop and Related Research 1984;188:3-9).
21. Gomes LSM, Volpan JB, and Goncalves
RP: Traumatic Separation of Epiphyses. An
Experimental Study in Rats. Clin Orthop
1988;236:286-294.
193
H.A. Peterson
22. Greco F, de Palma L, Specchia N, and Mannarini
M: Growth-Plate Cartilage Metabolic Response to
Mechanical Stress. J Pediatr Ortho 1989;9(5):520-
524.
23. Holland CT: A Radiographic Note of Injuries to
the Distal Epiphyses of the Radius and Ulna. Proc
R Soc Med 1929;22:23-28.
24. Hresko T, and Kasser JR: Physeal Arrest About
the Knee Associated with Nonphyseal Fractures
in the Lower Extremity. J Bone Joint Surg June
1989;71A(5):698‑703.
25. Hultén O: The Influence of a Fixation Bandage on
the Peripheral Blood Vessels and the Circulation.
Acta Chir Scand 1951;101:151-159.
26. Hunter LY, and Hensinger RN: Premature
Monomelic Growth Arrest Following Fracture
of the Femoral Shaft: A Case Report. J Bone Joint
Surgery 1978;60A:850-852.
27. Johnson EW, Jr, and Fahl JC: Fractures of the Distal
Epiphysis of the Tibia and Fibula in Children. Am
J Surg 1957;93:778-781.
28. Keret D, Mendez AA, Hareke HT, MacEwen GD:
Type V Physeal Injury: A Case Report. J Pediatr
Orthop 1990;10:545-548.
29. Kestler OC: Unclassified Premature Cessation
of the Epiphyseal Growth about the Knee Joint.
J Bone Joint Surg 1947;29:788-797.
30. Kling TF: Management of Physeal Injuries. In:
Operative Orthpaedics, 2nd Ed, ed by MW
Chapman, Chapter 215, pp 3035-3049, Philadelphia,
JB Lippincott, 1993.
31. Landin LA: Fracture Patterns in Children. Acta
Orthop Scand 1983;(Supp 1) 54:1‑109.
32. Letts RM: Compression Injuries of the Growth
Plate. In: Behavior of the Growth Plate, ed by
NK Uhthoff and JJ Wiley, pp 111-118, New York,
Raven Press, 1988.
33. Lombardo SJ, and Harvey JP, Jr: Fractures of the
Distal Femoral Epiphyses. Factors Influencing
Prognosis: A Review of Thirty-Four Cases. J Bone
Joint Surg 1977;59(A):742-751.
194
34. MacKenzie IG, Seddon HJ, and Trevor D:
Congenital Dislocation of the Hip. J Bone Joint
Surg 1960;42B:689.
35. Mann DC, and Rajmaira S: Distribution of Physeal
and Non-physeal Fractures in 2,650 Long-bone
Fractures in Children Ages 0 to 16 Years. J Pediatr
Orthop 1990;10:713-716.
36. Mbindyo BS: Considerations on Cases of
Epiphyseal Injury Observed at Kenyatta National
Hospital. East African Med J 1979;Sept:431-435.
37. Mendez AA, Bartal E, Grillot MB, Lin JJ:
Compression (Salter-Harris Type V) Physeal
Fracture: An Experimental Model in the Rat. J
Pediatr Orthop 1992;12:29-37.
38. Mizuta T, Benson WM, Foster BK, Patterson DL,
Morris LL: Statistical Analysis of the Incidence
of Physeal Injuries. J Pediatr Orthop 1987;71:518-
523.
39. Morton KS, Starr DE: Closure of the Anterior
Portion of the Upper Tibial Epiphysis as a
Complication of Tibial-shaft Fractures. J Bone
Joint Surg 1964;46:570-574.
40. Mustard WT, and Simmons EH: Experimental
Arterial Spasm in the Lower Extremities Produced
by Traction. J Bone Joint Surg 1953;35B:437.
41. Nicholson JT, Kopell HP, Matter FA: Regional
Stress Angiography of the Hips: A Preliminary
Report. J Bone Joint Surg 1954;36A:503-509.
42. Ogden JA: Injury to the Growth Mechanism of the
Immature Skeleton. Skeletal Radiol 1981;6:237-253.
43. Ogden JA: Skeletal Growth Mechanism Injury
Patterns. J Pediatr Orthop 1982;2(4):371-377.
44. Ogden JA: Injury to the Growth Mechanisms. In:
Skeletal Injury in the Child, 2nd Edition, Chapter
4, pp 97-174, Philadelphia, WB Saunders, 1990.
45. Oh WH, Craig C, Banks HH: Epiphyseal Injuries.
Pediatr Clin NA 1974;21:407-422.
46. Parke W, Colvin OS, Almond AHG: Premature
Epiphyseal Fusion at the Knee in Tuberculous
Disease of the Hip. J Bone Joint Surg 1949;31B:63-
73.

47. Pease CN: Focal Retardation and Arrestment of
Growth of Bones Due to Vitamin A Intoxication.
JAMA 1962;182:980-985.
48. Peterson CA, and Peterson HA: Analysis of the
Incidence of Injuries to the Epiphyseal Growth
Plate. J Trauma 1972;12:275-281.
49. Peterson HA: Distal Tibial Triplane Fractures. In:
Perspectives in Orthopaedic Surgery, Ed by JD
Heckmawn, St. Louis, Quality Medical Publis-
hing, Inc. Vol. 2, No. 1, pp 21-34, 1991.
50. Peterson HA: Premature Physeal Arrest of the
Distal Tibia Associated with Temporary Arterial
Insuffiency. J Pediatr Orthop 1993;13:672-675.
51. Peterson HA, Burkhart SS: Compression Injury
of theEpiphyseal Growth Plate, Fact or Fiction?
J Pediatr Ortho 1981;1:377-384.
52. Poland J: Traumatic Separation of the Epiphyses.
London, Smith, Elder, and Company, 1898.
53. Rang M: The Growth Plate and Its Disorders, Baltimore,
Williams and Wilkins, 1969, 203 pp.
54. Rang M: Injuries of the Epiphyses, The Growth Plate,
and the Periochondral Ring. In: Children’s Fractures,
2nd Edition, Chapter 2, p 10-25, Philadelphia, JP
Lippincott, 1983.
55. Rang M, Armstrong, P., Crawford, A. H., Kasser,
J. R., and Ogden, J.A.: Symposium: Management
of Fractures in Children and Adolescents. Part I.
Contemporary Orthop Dec., 1991;25(5):517-644.
56. Ratliff AHC: The Short Leg in Poliomyelitis. J
Bone Joint Surg 1959;41B:56-69.
57. Ratliff AHC: Complications After Fractures of the
Femoral Neck in Children and Their Treatment
(Abst). J Bone Joint Surg 1970;52B:175.
58. Rogers LF: The Radiology of Epiphyseal Injuries.
Radiology 1970;96:289-299.
59. Ross D: Distrubance of Longitudinal Growth
Associated with Prolonged Disability of the Lower
Extremity. J Bone Joint Surg 1948;30A:103-115.
Classification of physeal fractures
60. Salter RB: Salter-Harris Classification of Epiphyseal
Injuries. In: Behavior of the Growth Plate, ed by
NK Uhthoff and JJ Wiley, New York, Raven Press,
pp. 97-103, 1988.
61. Salter RB, Harris WR: Injuries Involving the
Epiphyseal Plate. J Bone Joint Surg 1963;45A:587-622.
62. Shapiro F: Epiphyseal Growth Plate Fracture-
Separation. A Pathophysiologic Approach.
Orthopedics 1982;5:720-736.
63. Smillie IS: Injuries of the Knee Joint. 4th Edition,
Edinburgh, Raven Press, 1970.
64. Smith DG, Geist RW, Couperman DR: Micros-copic
Examination of a Naturally Occurring Epiphyseal
Growth Plate Fracture. J Pediatr Orthop 1985;8:306-
308.
65. Specht EE: Epiphyseal injuries in childhood. Am
Fam Physician 1974;10(4):101-109.
66. Spiegel PG, Cooperman DR, Laros GS: Epiphyseal
Fractures of the Distal Ends of the Tibia and Fibula.
J Bone Joint Surg 1978;0A:1046-1050.
67. Troupp H: Nervous and Vascular Influence on
Longitudinal Growth of Bone: An Experimental
Study on Rabbits. Acta Orthop Scand 1961;(Suppl)
51:7-78.
68. Trueta J: The Role of the Vessels in Osteogenesis.
J Bone Joint Surg 1963;45B:402-418.
69. Trueta J, Amato VP: The Vascular Contribution to
Osteogenesis, III. Changes in the Growth Cartilage
Caused by Experimentally Induced Ischaemia. J
Bone Joint Surg 1960;42B:571-587.
70. Trueta J, Morgan JD: THe Vascular Contribution to
Osteogenesis, I. Studies by the Injection Method.
J Bone Joint Surg 1960;42B:97-109.
71. Weber BG: In: Treatment of Fractures in Children
and Adolescents, ed by BG Weber, CH Brunner,
and F Freuler, New York, Springer-Verlag, 1980.
72. Worlock P, Stower M: Fracture Patterns in Nottingham
Children. J Pediatr Orthop 1986;6:656-660.
195
23
Surgical treatment of physeal fractures
C.F. Moseley
INTRODUCTION
The presence of the physis is the single
most important factor differentiating fractures
in children from those in adults. Because of the
excellent ability of children to heal fractures
and to remodel their bones, it is usually
possible and desirable to treat children’s
fractures non-operatively. Disruption of the
physis or of the adjacent joint is the most
common indication for surgical treatment.
This discussion will use the Salter-Harris
classification of physeal fractures which is
widely used and relatively straightforward.
In this classification, pure type I and type II
fractures involve the growth plate but the
fracture line does not disrupt the zone of cells
which is doing the growing and so the risk of
growth disturbance is unlikely. In type III the
fracture does cross the growing zone but there
is little risk of growth disturbance because
these fractures almost always happen when
the growth plate is already partially closed.
In type IV fractures not only does the fracture
traverse the growth layer, but may expose
metaphyseal bone to epiphyseal bone leading
to a bony bridqe.
GOALS OF TREATMENT
Restore anatomy
Restoring the shape of the bone is much less
196 Reprinted with permission of Mapfre Medicina (vol. 4, suppl 2)
important in children than in adults because
children are better able to remodel their bones
(Wolff’s Law). Restoring the attitude of the
joint is also less important because of the ability
of the growth plate to change the direction
of its growth according to the loads placed
upon it (Heuter-Volkmann Law). Adults do
not share this mechanism of remodeling.
Restoring the integrity of the physis in certain
physeal fractures is, however, of great importance
since malalignment can lead to formation of a
bony bridge and subsequent growth disturbance.
In intra-articular physeal fractures restoring the
configuration and congruity of the joint is likewise
important to avoid early degenerative changes
and a lifetime of degenerate arthritis.
Avoid growth arrest
Complete or partial growth arrest can
result from physeal fractures by at least two
mechanisms. The first is an actual injury to
the cells of the growth plate due to the forces
of the fracture or the reduction. Injury to the
growth cells occurring at the time of fracture is
never evident at that time but must always be
suspected, especially in type II fractures of the
weight-bearing bones in which the sharp corner
of the metaphyseal fracture can compress and
injure the growth cells in the physeal fragment.
An invisible type V injury is therefore added
to the visible type II injury. Parents should be
 Surgical treatment of physeal fractures

A B
Figure 1. A) A minimally displaced type IV fracture of the medial malleolus. B) A tomogram taken one
year after closed treatment in a cast shows a bony bridge at the fracture site.

warned of this possible complication before the
reduction, and the child should be observed
carefully thereafter. Growth arrest by this
mechanism is unavoidable. The orthopaedic
surgeon can, however, avoid damaging the
physeal cells by performing the reduction in
an appropriate manner.
The second mechanism of growth arrest
occurs only in type IV fractures which are
not satisfactorily reduced. Type IV fractures
in certain locations, for example those of the
medial malleolus of the tibia, tend to displace
so that the bone of the epiphysis comes to
lie adjacent to the bone of the metaphysis,
potentially leading to formation of a bony
bridge between these two parts (Fig. 1).
This would obviously tether the growth of
the physis in that area and cause a growth
disturbance. Bone bridges by this mechanism
can be avoided by obtaining and maintaining
an anatomical reduction.
Bone bridges resulting from type V injury
are usually larger, less discrete and more
difficult to excise surgically than those resulting
from type IV fractures which tend to be limited
to all or part of the line of the fracture.
Avoid non-union
Type III and type IV fractures are intra-
articular by definition and their surfaces are
bathed in joint fluid. It may be that this inhibits
bone formation and promotes non-union. Type
III fractures in certain areas, e.g. proximal
femur, proximal radius) are also intra-articular
and entail the same risk.
Fractures of the lateral condyle of the humerus
are common injuries in children. They are type IV
fractures, but behave differently than the type IV

197
C.F. Moseley
Figure 2. The late result of an unrecognized condyle
fracture which occurred at the age of four years.
Non-union has occurred resulting in disorganization
of the elbow joint.
fracture of the medial malleolus (Fig. 2). In this
case it is an avulsion fracture and the fracture
fragment displaces away from the metaphysis
and not towards it. The threatening complication
is non-union, not bony bridge formation as in the
type IV fracture of the medial malleolus.
DIAGNOSIS OF OCCULT PHYSEAL
FRACTURES
Physeal fractures in children younger than
six years, and particularly three years, may be
difficult or impossible to diagnose by plain
x-rays. At this age most of the epiphysis may
be cartilage and fractures through that part
of the bone will not show. Doctors treating
patients in this age group must maintain a
high index of suspicion that a plain x-ray may
not show any or all of a fracture and must
judge whether or not further investigation
is warranted.
Occult fractures of the hip and patello-
femoral joint
Osteochondral fractures of either side of
the joint may occur in relation to dislocations
but are not physeal fractures. They are of some
importance, however, since they disrupt the
198
Figure 3. An occult injury of the elbow. The x-ray
shows a disturbance of the normal relationship
between the humerus and the forearm bones but
it is not clear whether this is a fracture of the distal
humerus or a dislocation of the elbow.
joint surface and reduction of the fragment
may be indicated. In the hip, the fragment
may become interposed in the joint leading
to a non-concentric reduction.
Occult fractures of the elbow
Physeal fractures around the elbow may be
occult and constitute pitfalls for the treating
doctor. In this anatomical area confusion
between the possible fracture patterns may
lead to misdiagnosis, mistreatment, and
unfortunate results.
Before ossification appears in the epiphysis
of the distal humerus it may be impossible
to distinguish radiologically between a
dislocation and a type I fracture (Fig. 3).
Both may show a disturbance of the normal
relationship between the humerus and
the forearm bones, but the location of the
disruption will not be evident.
The lateral condyle fracture is a type IV
physeal fracture, but, since the epiphyseal
portion of the fracture is through cartilage,
the only injury that can be seen is the fracture
of a flake of bone from the distal lateral
metaphysis. Although virtually all injuries
with that x-ray finding are lateral condyle
fractures it is theoretically possible that the
 Surgical treatment of physeal fractures

A B
Figure 4. A) An occult injury of the elbow. The x-ray shows displacement of the ossification center of
the medial epicondyle. B) The arthrogram showed that the injury was actually a fracture of the medial
condyle, a type IV fracture, which required open reduction and internal fixation to restore the joint
surface and the physis.

injury is a type II fracture instead, and that
open reduction might not be required.
Fractures on the lateral side of the elbow
are usually condylar fractures, and those
on the medial side are usually epicondylar
fractures. Condylar fractures do, however,
occur on the medial side but, in the young
elbow, the only radiological feature may be
displacement of the ossification center of
the epicondyle giving it the appearance of
an epicondylar fracture, the more common
injury (Fig. 4). The distinction is important
since there is no clear indication for surgical
treatment of the epicondylar fracture whereas
almost all displaced condylar fractures require
open reduction and fixation. Mistaking a
condylar fracture for an epicondylar fracture
could result in inappropriate treatment, non-
union of the fracture, and disorganization of
the elbow joint.
Assessment of occult fractures
It is of no use to have an assessment strategy
for occult fractures since they are either nor
recognized at all or are not recognized until
after the assessment has been completed.
One should actually perform more than the
routine x-rays in all injuries in young patients
where there is a possibility of an occult injury,
particularly those in which it is clear that
there has been a disruption, the exact nature
of which is not fully defined.
CT scan is not particularly useful in this
regard since it is unable to distinguish cartilage
from joint fluid and cannot define cartilaginous
fracture fragments that are loose in joints.

199
C.F. Moseley
A B
Figure 5.
MRI can provide a clear understanding of
these injuries but is not usually immediately
available when the children present, and a
awaiting this examination may result in an
unacceptable delay of treatment.
Since most for these patients will require a
general anesthetic in any case it is convenient
and expedient for the orthopaedic surgeon to
perform an arthrogram on the operating table
prior to undertaking treatment. In this way he
can satisfy himself with respect to the exact
nature of the injury, and decide confidently
on the best treatment approach.
INDICATIONS FOR SURGICAL
TREATMENT
Type I and type II fractures
These fractures require surgical treatment
only if closed reduction cannot achieve
satisfactory position. They can almost always
be treated by closed reduction since reduction
is usually not difficult. Growth disturbance
is unusual since these fractures do not cross
the growth layer of the physis .
Type III fractures
Type III fractures involve the joint surface
and must be anatomically reduced to restore
200
C
the joint. Stable closed reduction can sometimes
be achieved, but, if not, then open reduction
with internal fixation should be performed.
Growth arrest and bony bridges are almost
never a consideration since these fractures only
occur in adolescence when the growth plate is
in the process of closing.
The Tillaux fracture is an avulsion fracture
of the antero-lateral part of the distal tibial
epiphysis by the anterior tibio-fibular ligament.
It is an external rotation injury of the ankle. It
occurs at the particular stage of maturation
when the distal tibial physis, which closes from
medial to lateral, is partly closed. The fracture
passes through the epiphysis and the part of the
physis that is not yet closed. This fracture can
occasionally be reduced closed by distracting the
joint and exerting pressure over the fragment,
but if the fracture gap cannot be reduced to
less than one millimeter then open reduction
and internal fixation should be performed. It
is of no consequence if the fixation crosses the
physis since it is already in the process of closing.
The triplane fracture is so named because
the fracture surface exists in three planes; the
coronal plane in the metaphysis, the transverse
plane in the physis, and a curved portion,
similar to the Tillaux fracture, in the sagittal
and coronal planes in the epiphysis (Fig. 5). It

occurs at the same stage of physeal closure as
the Tillaux fracture, and can be either a two or
three part fracture. The fractures through the
bone and the physis are not as important as
that through the joint, and the joint must be
anatomically reduced by an open reduction.
This is best performed through an exposure just
anterior to the fibula which allows anatomic
restoration of the joint surface by fixation
of the Tillaux fragment to the larger distal
fragment. Once that has been achieved then
the unified distal fragment can be reduced
onto the body of the tibia. This latter reduction
does not have to be anatomic as long as good
alignment of the joint can be attained. If not,
then either a lag screw from the front of the
tibia or a second incision posterior to the fibula
may be necessary.
Type IV fractures
All type IV fractures must be reduced
anatomically for the sakes of both the joint
surface and the physis. All fractures displaced
more than one millimeter deserve open
reduction and internal fixation. Minimally
displaced fractures of the lateral condyle of
the elbow should first be x-rayed carefully
Surgical treatment of physeal fractures
to ensure that what appears to be minimal
displacement in one view is not significant
displacement in another. These fractures, if
not treated by internal fixation, should be
observed suspiciously for displacement which
can occur even during cast immobilization. In
fixing type IV fractures, which may occur at a
young age, it is important that the fixation not
cross the physis. If it is absolutely necessary
to do so then thin wires should be used and
removed at the earliest opportunity. Three
weeks is sufficiently long immobilization for
fractures about the elbow.
Anatomic reduction will minimize the
opportunity for the formation of bony bridges
and the risk of non-union.
CONCLUSION
Physeal fractures warrant careful
assessment with a high index of suspicion
for occult injuries, especially in young
children. Defining the true configuration of
the fracture with certainty and treating the
injury appropriately and carefully minimizes
the risk of complications which could have
serious long term consequences.
201
24 Bone remodeling in malunited fractures
in children
J. Gascó and J. de Pablos
INTRODUCTION
Remodeling in malunited fractures in
children is a well-known. In fact, it is one of
the factors which contribute to the tendency
to use closed reduction treatments in fractures
in children, contrary to the treatments usually
chosen for adults. But bone remodeling
processes are not limited to fractures and to
various degrees, they remain active during
a person`s entire life. As a result of this
ongoing remodeling process, the bone has
the dimensions and the structure of healthy
bone, and, conversely, when illnesses occur
that change these mechanisms, alterations are
produced which may influence the dimensions,
shape or both of the bone to greater or lesser
extent. These physiologic processes that allow
for normal bone formation during a person’s
growing phase could also be called modeling
processes(11).
The most well-known mechanism that produce
bone remodeling are longitudinal and latudinal.
Longitudinalgrowthnechanismsarefundamentally
controlled by the growth cartilage or physis.
This longitudinal growth will be symmetrical or
asymmetrical depending on factors discussed
subsequently. The possibility of helicoidal growth
of the physis, which could produce the remodeling
of fractures united with defective rotation, also has
been acknowledged(52). With latitudinal growth
mechanisms, the periostium and the endostium
play essential roles. These mechanisms are
202 Reprinted with permission of Lippincott-Raven (J Pediatr Orthop Part B 1997;6:126-132).
responsible for the bone aposition-resorption
phenomena that are so frequently in metaphyseal
and diaphyseal fractures with residual angular
deformity or escessive overriding.
Logically, because of the greater activity
of the previously mentioned structures during
chidhood, the bone remodeling processes are
more pronounced if they take place before the
skeleton matures.
The fact that closed reduction methods are
used more frequently in children increases the
risk of defective consolidation (malunion). When
this occurs, the remodeling processes become
acrtive in order to reestablish bone alignment with
respect to the mechanical axis and the relations
in their epiphysis.
The processes that have been studied in more
depth, with regards to malunited fractures in
children, are remodeling of angular deformities
and, to a lesser extent, remodeling of rotational
deformities.
Another phenomenon we will discuss is
post-fracture overgrowth in children, which,
although it cannot be strictly considered a
remodeling process, is closely related to these
processes.
REMODELING OF ANGULAR
DEFORMITIES
Malunited fractures in children do not
always remodel themselves, and sometimes
 Bone remodeling in malunited fractures in children

A B C

Figure 1. Malunited diaphyseal fracture of the left femur in a 7 year

old boy. Two months after injury the fracture has consolidated with
a 4.5 cm overriding and an angulation of 23º in the sagital plane (A,
B). Seven months after fracture a very active remodeling process has
occurred, and the angular deformity has been almost completely
D corrected (C, D).

unacceptable results must be corrected it is mechanically necessary (that is, in the

surgically. In the case of spontaneous
correction of residual angulations in children,
both the periosteum and the physis adjacent
to the fractures site are involved, and actively
participate to achieve,in varying proportions,
a correct alignment of the malunited fracture(1).
Although the basic mechanism that corrects
these deformities is not fully understood, two
well-known biological laws attempt to ascribe
the dominant role to the mechanical factor. The
first law, described by Wolff(86) in 1892, states
that new bone apposition is produced where
weight-bearing area), and that it is reabsorbed
where it is not needed. In this manner, when
fractures consolidate in angulation, new bone
is formed in concave areas, and resorption
predominates in convex ones. This process
produces a certain realignment in the bones,
and although it also occurs in adults, it is
more notable in children.
One of the theoretical explanations for this
apposition-resorption phenomenon in fractures
in children suggest that the periosteum, intact
within the concavity, produces the ‘filling’ in

203
J. Gascó, J. de Pablos
Figure 2. The main processes involved in the
remodeling of a malunited fracture in children
are asymmetrical longitudinal growth (physis)
and apposition-resorption, or drifting, of bone
(periosteum). Schematic representation.
that part of the bone, whereas in the convexity,
because the bone is denuded, resorption would
be more predominant(55). However, we do
not believe there is sound scientific support
for this theory.
Nevertheless, this apposition-resorption
phenomenon tends to greatly improve the
angulation of the fracture site and, to a lesser
degree, the diaphyseal alignment. Regarding
this last aspect, researchers have determined
that this process contributes aproximately 25%
of the total remodeling process(42,85,52).
The role of the periosteum during the
remodeling process has been widely discussed
historically. In 1867 Ollier(56) indicated that the
deeper layers of the periosteum were more
cellular and osteogenic. In 1912 MacEwen(47),
after doing experimental studies, stated that the
periosteum is not a bone-forming structure. The
periosteum’s osteogenic capacity and its role
during the reparative process and the remodeling
of fractures is now well known(27), however, and
204
our clinical observations have also confirmed
it (Fig. 1).
Heuter Volkman’s law(41,83), the second
of the classically accepted regulatory laws
regarding the remodeling process in fractures
states that the physes adjacent to the malunited
fracture tend to realign perpendicular to
the resultant force that acts through them,
modifying its orientation with respect to
the axis of the bone(28,30,42,66). Given this, in a
malunited fracture, according to its needs,
assymetrical bone growth will occur, which
in turn will modify the orientation of the
epiphysis and, consequently, of the joint.
This second mechanism, assymetrical physeal
growth, appears to be quicker and more
effective(52) regarding diaphyseal realignment,
contributing aproximately 74-75% of the total
remodeling produced.
Steinert(73) suggested in 1966 that the physes
could play an important role in the correction
of these deformities, but Pauwells(59,60) proved
that growth cartilage respoded to changes in
pressure by selective growth in different areas
of its structure. This was later experimentally
confirmed by several authors(1,25,42,66), indicating
that the part of the physis which corresponds to
the concave side of the deformity experiences
greater growth (Figs. 2, 3). Both physes would
participate from the extremities fractured in
this process, although in different proportions
depending on their involvement in the normal
growth of the extremity(28-30).
Many factors influence the remodeling
process of postfracture angular deformities,
and the following stand out among them:
Skeletal age, the location of the fracture within
the skeletal structure and the bone itself,
and the degree and orientation of the angle
of malunion
With regards to age, remodeling is more
likely to be complete in children of younger
skeletal age(2,5,8,15,20,31,32,44,57,61,62,64-66,70,82). Not every
author establishes age limits, but remodeling
seems to be better when the child is 8 to 10

Figure 3. Remodeling of a malunited distal radius
fracture in a 10 year-old boy. X-ray series 4 months
(top), 1 year (middle) and 2 years post-fracture
(bottom). The two main bone remodeling processes
(asymmetrical physeal growth and periosteal
drifting) are evident.
years old, and this factor is directly related to
the other factors we will discuss such as the
location, degree and orientation of the angle.
The location of the malunited fracture is an
important. In the skeleton the remodeling process
generally appears to be more reduced in the upper
extremities compared to the lower extremities,
probably because the lower extremities are
subjected to greater mechanical loads(1).
In the upper extremities, less remodeling
activity is observed in middle or proximal
diaphyseal fractures of the forearm(39,30,64,62,82,87),
in humeral fractures near the elbow(85), and, in
the hand, in fractures of the phalanx far from the
base and, therefore, the physis(4,45,50).
In the proximal humerus and the distal
forearm, however, the capacity for remodeling
is extraordinary, so that surgical repositioning
of fragments is rarely indicated.
The acceptable degree of angulation for
complete remodeling to be successful in each
location varies greatly (Table 1). Moreover,
Bone remodeling in malunited fractures in children
regarding the location within the bone, it is
generally accepted that the greater the distance
to the growth cartilage, the less extensive the
remodeling process.
Other important factors are the degree and
the orientation of the deformity, which are
closely related to its location and to the age
of the patient. Regarding the orientation of
the deformity, if angulation is produced in the
opposite orientation of the axis of movement
of the neighbouring joint, the remodeling will
also be less extensive(51).
In the forearm, volar and cubital angulations
of the radius show better remodeling(30), and the
bone deformity does not appear to be related
to the loss of pronosupination but rather to the
development of scar tissue in the soft parts,
which apparently can provoke tension on the
interosseous membrane(76,62).
In the tibia, angulations of the saggital
plane (antecurvatum/recurvatum ) show
better remodeling than coronal angulations
(varus,valgus)(6,8,18,24,54,71,79), and of this, varus
angulations also show better remodeling than
valgus angulations, whereas biplanar angulations
do not remodel as well(68).
In the femur, angular deformities of the sagital
plane appear to correct themselves better than
those of the coronal plane(15,48).
Remodeling occurs over a prolonged period
and appears to be completed 5 to 6 years after the
fracture(48,81,85). This is why surgeons recommend,
in the case of malunions and persistence of the
angular deformity, delaying corrective osteomies
for at last 1 year, unless the deformity is severe
enough to interfere with the proper limb
function.
REMODELING OF ROTATIONAL
DEFORMITIES
With fractures in children, angular
deformities can remodel themselves, although
rotational deformities do not. Despite this,
certain facts indicate that postfracture rotational
205
J. Gascó, J. de Pablos

Table 1. Acceptable limits in angular deformities after long bone fractures in children
(complete remodeling possible)

UPPER LIMB LOWER LIMB

Humerus Forearm Femur Tibia
(upper)
< 10 year-old 40-70º Distal - 20-40º 20-30º 10-15º*
Middle-10-20º
> 10 year-old 20-30º Distal - <20º 15-20º 10-15º*
Middle - 10º

* Better remodeling when angular deformity is in varus

deformities can correct themselves, and this
has been confirmed in certain experimental
studies done using dogs and rabbits(67,75,52),
where correction has been observed, both in
internal and external malrotation, in as many
as 56%.
Certain clinical observations correspond
with the findings of the previously mentioned
experimental studies, such as the frequent
occurrence of malrotations after conservative
treatment of fractured extremities for which
the patient is not treated until some years later,
suggesting that spontaneous correction of the
malrotation occurred(13). Another observation is
that Van Ness’rotationplasty has the tendency
to derotate, which suggest that it occurs at a
physeal level(77). It has been scientifically proven
that these torsional deformities can be corrected
with helicoidal growth of the growth plate(52).
However, contradictory clinical results indicate
that in children younger than 8 years, intense
rotational deformities correct themselves(31,35,84),
whereas other researchers believe that regardless
of age, remodeling of rotational deformities
occurs infrequently(22,80).
POST-FRACTURE OVERGROWTH IN
CHILDREN
Postfracture bone overgrowth in children
was first described by Volman(83) in 1862. A few
years later, Ollier(56), in an experimental study,
observed overgrowth ranging from 2 to 5 mm
in the tibias of rabbits that had undergone
periosteal stripping. Since then, many studies
have confirmed the presence of overgrowth
following fractures of the femur(2,9,14,26,63,74),
tibia(33,34,69,88) and the humerus(37) (Tables 2
and 3).
The incidence of bone overgrowth is well
known, and its appearance is not limited to
fractures. It is also observed in congenital
vascular diseases (Klippel-Trenaunay
Syndrome), inflammatory conditions
(osteomyelitis, juvenile rheumatoid
arthritis) and tumoral or pseudo-tumoral
lesions (osteoid osteoma, fibrous dysplasia,
neurofibromatosis). Researchers, do not
agree about the cause of this phenomenon,
and controversy still exist concerning the
factors that are implicated in its appearence
and severity.
It is generally accepted that overgrowth
after fractures in children is due to a biological
process of physeal stimulation resulting from
the hyperemia that is produced around the
fracture site during the consolidation and
remodeling process. This theory was proposed
by Ollier(56) in 1867 and was confirmed by
Bisgard(7) in 1936, proving that overgrowth
occurred in the physeal plate and not at the
level of the fracture site. In the case of limb

206
 Bone remodeling in malunited fractures in children

Table 2. Average femoral overgrowth

Author Year n Overgrowth (mm.)

Aitken(2) 1940 65 10
Hedberg(36) 1944 44 9
Vijanto and cols.(81) 1975 51 10,7
Meals(49) 1979 112 10
Reynolds(63) 1981 42 8
Shapiro(69) 1981 74 9,2
Clement, Colton(16) 1986 50 8,1
Stephens & cols(74) 1989 30 11
Hougaard(40) 1989 67 10,8
Corry, Nicol(17) 1995 50 6,9
TOTAL 585 9,3

n=Number of patients

Table 3. Average tibial overgrowth

Author Year n Overgrowth (mm.)

Reynolds (63)
1981 84 4
Greiff, Bergman(33) 1980 85 5
Zionts, MacEwen(88) 1986 7 10
Shannak(68) 1988 117 4,35
TOTAL 293 5,83

n= Number of patients

discrepancy, this led to the employment
of techniques now obsolete, such as heat
application, periosteal stripping, implantation
of foreign materials near the physis or lumbar
sympathectomies.
Less convincing are the theories that do not
consider postfracture overgrowth a biologic
phenomenon, but rather a compensatory
processthat occurs when the bone is shortened
after a fracture(21), or as a conbsequence of
postfracture release of an unknown local factor
that stimulates mitosis both in the physis and
in the periostic cells(43).
However, some aspects are still unclear, such
as the minimal growth stimulus after fractures of
the forearm(23), or the different growth response
observed at the healthy ipsilateral tibia after
femoral fractures: stimulation(63,69,74), growth
arrest(17) or no effect at all(26). Growth stimulation
of the femur ipsilateral to the fractured tibia has
also been observed(78). Although all of this has
been attributed to the hyperemia of the entire
extremity after the fracture, it is difficult to
accept that this phenomenon could occur from
such a distance.
The many factors involved have been
studied exhaustively by many authors in an
attempt to find criteria regarding acceptable
reduction after long-bones fractures in
children. Factors discussed are the age and
sex of the patient, the location of the fracture
and the position of the fragments.

207
J. Gascó, J. de Pablos
The patient’s age is of little relevance for
some authors(16,26,40,46,63,69), but others consider
it a decisive factor, more so the skeletal age
than the chronological age(33,34,36,72,74). The rate
of overgrowth is greater in children 4 to 5 years
old than in children 8 to 9 years old.
The patient’s sex is considered relevant only
by some authors(16,33,69,78), who believe that believe
that the growth plate of a boy responds with
greater intensity to hyperemia than does that
of a girl.
The location of the fracture is not a
relevant factor in postfracture overgrowth.
Nevertheless, it has been observed that it
occurs in a higher percentage in fractures
of the lower extremity, particularly of the
femur, in the diaphysis (Tables II and III)
and, above all, in those fractures that present
greater displacement(8,12,38). In fractures of
the forearm, overgrowth is nor as evident
and does not appear to occur in all cases(23).
The position of the fragments after reduction
is considered to be one of the important
factors (16,26,49,63,74), although some authors
have not seen it as such(53). Two positions
have been considered to generate growth
stimulus: the overriding of the fragments
and their angulation. The overriding of the
fragments is though to be the one factor that
provokes greater stimulus(2,26), and it seems to
be greater when produced after trauma rather
than after reduction. The consequence is that
the greater the energy of the trauma, the longer
it will take for the fracture to be repaired, and
therefore the longer the hyperemia and will
the stimulus on the growth cartilage will last.
This would apparenly explain the inverse
proportional relationship that exists between
the overriding of fracturary fragments and the
final discrepancy of the length of the lower
extremities(16).
The type of fracture also seems to influence
overgrowth. Some authors(3,26) have observed
that long spiroidal and oblique fractures seems to
generate a higher stimulus, although this is more
208
clesely related to the fact that there normally
exists a higher degree of angulation in fractures
with these characteristics. In general, unstable
fractures had a higher rate of overgrowth(10).
Others authors, however, have found that
overgrowth has no relationship with type of
fracture(19,58).
The angulation of the fragments activates
a remodeling process, not only at the level of
the fracture site, which only softens the angular
deformity, but also on a physeal level in order to
align both the physeal plate and epiphysis until
they are located perpendicular to the weigh-
bearing area of the affected bone. In tibial
fractures that remained with valgus or varus
angulation, the rate of overgrowth was higher
than in those with correct alignment, which
were reduced by 50%(63), probably because the
remodeling phase is more prolonged in the
former.
Growth stimulus after fractures is limited to
a certain time and can follow different patterns.
It appears to stop at about 18 months after the
fracture and peaks during the first 3 months,
although this varies according to the bone that is
fractured(8,12,16,21). Thus, in fractures of the femur it
lasts as long as 18 months, whereas in fractures
of the tibia it lasts approximately 15 months(63).
In most cases (91%), the growth stimulus follows
a plateau pattern(69) in which the growth rhythm
soon reaches a maximum and later stabilizes.
In the remained cases (9%), growth continues
until skeletal maturity is reached with greater
intensity during the first 18 months, which later
slows until the end of the growth period. The
stage in which growth occurs most rapididly is,
as previously noted, during the first 3 months
after the fracture.
Measuring overgrowth is also problematic.
Most studies assume that before the trauma
occurred both limbs were of identical length,
but it has been proven that in right-handed
persons, both the femur and the tibia are slightly
longer than their counterlateral counterpart(49),
the difference being slightly more than 1 mm.

Nevertheless, according to those authors, in
the upper limbs of right-handed patients the
right upper limb was longer. The overgrowth
was greater if the fracture had occurred in the
dominant limb.
Another problem results from the methods
used in the different studies to obtain the
measurements. Clinical methods of evaluation,
for example, are imprecise, with the error in
these cases ranging from approximately 5
and 10 mm(34). The most reliable method is
the radiologic, perhaps digital radiography,
and follow-up must continue for at least 18
months and preferably until the growth period
has ended. Measurements must always be
compared with those of the healthy limb, andthe
surgeon must remember that in the lower
limb no articular contractures should exist in
hips or knees, and that in the upper limb the
forearm must be placed in a neutral position.
The repercusions of overgrowth in the
treatment of fractures are obvious if we
consider that the most frequent complication
in the case of diaphyseal femoral fractures is leg
length discrepancy. To prevent this, a certain
overlapping of the fragments should be allowed.
Recommendations range from 3 cm(53) to 1 cm(74),
but because the mean femoral overgrowth is 1.5
cm, the maximun shortening allowed should be
the same. Logically, the maximum allowed will
depend on the age of the child, and in children
younger than 4 years old and older than 8
years, some authors recommend less residual
shortening than the indicated shortening(17).
However, limb length discrepancy in skeletal
maturity will not be significant from a practical
point of view and most patients will notice no
difference between the two limbs.
Regarding fractures of the tibia, the mean
overgrowth is lower than that of the femur.
In children between the ages of 5 and 9 years
it is 0.5 cm. For this reason, shortening is not
acceptable after reduction in children older
than 10 years, and, in any case, only minimal
shortening is acceptable in younger children.
Bone remodeling in malunited fractures in children
With diaphyseal fractures of the humerus
and the forearm, no precautions are necessary
regarding overgrowth,because the rate of
overgrowth is slight and a discrepancy of a few
millimeters between the upper extremities usually
causes no clinical problems.
REFERENCES
1. Abraham E. Remodelling potencial of long bones
following angular osteotomies. J Pediatr Orthop
1989;9:37-43
2. Aitken AP. Overgrowth of the femoral shaft following
fracture in children. Am J Surg 1940;49:147-8
3. Barfod B, Christensen J. Fractures of the
femoral shaft in children with special reference
to subsequent overgrowth. Acta Chir Scand
1959;116:235-50
4. Barton NJ. Fractures of the hand. J Bone Joint Surg
[Br] 1984;66:159-67
5. Baxter MP, Wiley JJ. Fractures of the proximal
humeral epiphysis. Their influence on humeral
growth. J Bone Joint Surg [Br] 1986;68:570-3
6. Bennek J, Steinert V. Knochenwachstum nach
deformverheilten Unterschenkelschaftfrakturen
bei Kindern. Zbl Chir 1966;91:633-9
7. Bisgard JD. Longitudinal overgrowth of long
bones with special reference to fractures. Surg
Gynecol Obstet 1936;62:823-35
8. Blount WP. Fractures in children. Baltimore : The
William & Wilkins Company 1955
9. Bohn WW, Durbin RA. Ipsilateral fractures of
the femur and tibia in children and adolescents.
J Bone Joint Surg [Am] 1991;73:429-39
10. Breitfuss H, Muhr G. Lässt sich vermehrtes Längen-
wachstum nach kindlichen Oberschenkelscha-
ftsbrüken vermeiden?. Unfallchirurg 1988;91: 189-94
11. Buckwalter JA, Glimcher MJ, Cooper RR, Recker
R.Bone Biology part II:Formation, Modeling,
Remodeling and Regulation of Cell Function. J
Bone Joint Surg [Am] 1995;77:1276-89
209
J. Gascó, J. de Pablos
12. Burdick CG, Siris IE. Fractures of the femur in
children. Ann Surg 1923;77:736-9
13. Brouwer KJ, Molenaar JC, Van Linge B.
Rotational deformities after femoral shaft
fractures in chilhood. A retropective study
27-32 years after the accident. Acta Orthop Scand
1981;52:81-9
14. Calati A, Poli A. Il fenomeno dell’hiperllungamento
osseo consequente a fratture diafisarie di ossa
lunghe riportate nell’infanzia e nell’adolescenza.
Minerva Ortop 1959;11/11:827-32
15. Canale ST, Beaty JH. Complications in Pediatric
Orthopaedic Surgery. Philadelphia: Ed Ch Epps,
JR Bowen. JB Lippincott 1995
16. Clement DA, Colton CL. Overgrowth of the femur
after fracture in childhood. J Bone Joint Surg [Br]
1986;68:534-6
17. Corry IS, Nicol RO. Limb length after fracture
of the femoral shaft in children. J Pediatr Orthop
1995;15:217-9
18. Cozen L. Fracture of the proximal Portion of the
Tibia in Children Followed by valgus deformity.
Surg Gynec and Obstet 1953;97:183-8
19. Cramer KE, Limbird TJ, Green NE. Open fractures
of the diaphysis of the lower extremity in children:
treatment, results and complications. J Bone Joint
Surg [Am] 1992;74:218-32
20. Curtis Jr RJ. Operative management of children’s
fractures of the shoulder region. Orthop Clin North
Am 1990;21:315-24
21. David VC. Shortening and compensatory
overgrowth following fractures of the femur in
children. Arch Surg 1924;9:438-49
22. Davids JR. Rotational deformity and remodeling
after fracture of the femur in children. Clin Orthop
1994;302:27-35
23. De Pablos J, Franzreb M, Barrios C. Longitudinal
Growth Pattern of the radius after forearm
fractures conservatively treated in children. J
Pediatr Orthop 1994;14:492-5
24. Dias L. Fractures of the Tibia and Fibula. In:
210
Rockwood C, Wilkins KE,King RE ed. Fractures
in children. Philadelphia: Lippincott 1991:1271
25. Dimitriu CG, Kapetanos GA, Symeonides PP. The
effect of partial periosteal division on growth of
the long bones. An experimental study in rabbits.
Clin Orthop 1988;236:265-9
26. Edvardsen P, Syversen SM. Overgrowth of the
femur after fracture of the shaft in childhood. J
Bone Joint Surg [Br] 1976;58:339-42
27. Eyre-Brook AL. The Periosteum: Its function
reassessed. Clin Orthop 1984;189:300-7
28. Friberg KSI. Remodelling after distal forearm
fractures in children. I. The effect of residual
angulation on the spatial orientation of the
epiphyseal plates. Acta Orthop Scand 1979;50:537-46
29. Friberg KSI. Remodelling after distal forearm
fractures in children. II. The final orientation of
the distal and proximal epiphyseal plates of the
radius. Acta Orthop Scand 1979;50:731-9
30. Friberg KSI.Remodelling after distal forearm
fractures in children. III. Correction of residual
angulation in fractures of the radius. Acta Orthop
Scand 1979;50:741-9
31. Fuller DJ, McCullough CJ. Malunited fractures
of the forearm in children. J Bone Joint Surg [Br]
1982;64:364-7
32. Gandhi RK, Wilson P, Mason Brown JJ, MacLeod
W. Spontaneous correction of deformity following
fractures of the forearm in children. Br J Surg
1962;50:5-10
33. Greiff J, Bergmann F. Growth disturbance
following fracture of the tibia in children. Acta
Orthop Scand 1980;51:315-20
34. Greville NR, Ivins JC. Fractures of the femur
in children. An analysis of their effect on the
subsequent length of both bones of the lower
limb. Am J Surg 1957;93:376-84
35. Hägglund G, Hansson LI, Norman O. Correction
by growth of rotational deformity after femoral
fracture in children. Acta Orthop Scand 1983;54:858-
61

36. Hedberg E. Femoral fractures in children. Acta
Orthop Scand 1944;90:568-72
37. Hedström Ö. Growth stimulation of long bones
after fracture or similar trauma. A clinical and
experimental study. Acta Orthop Scand 1969;122
(Supp l):7-134
38. Henry AN. Overgrowth after femoral shaft fractures
in children. J Bone Joint Surg [Br] 1963;45:222
39. Högstrom H, Nilsson BE, Wilner S. Correction with
growth following diaphyseal forearm fracture.
Acta Orthop Scand 47:299-303
40. Hougaard K. Femoral shaft fractures in children: A
propective study of the overgrowth phenomenon.
Injury 1989;20:170-2
41. Hueter C. Anatomische studies an den Extremitaten
g Elenken Neugeborene und Ewach sener. Wirchow
Arch 1862;25:572-99
42. Karaharju EO, Riöppy SA, Mäkinen RJ. Remodelling
by asymmetrical epiphyseal growth: an experimental
study in dogs. J Bone Joint Surg [Br] 1976;58:122-6
43. Kaya Alpar E. Growth plate stimulation by
diaphyseal fracture. Acta Orthop Scand 1986;57:135-7
44. Larsen CF, Kiaer T, Lindequist S. Fractures of the
proximal humerus in children. Nine-year follow-
up of 64 unoperated on cases. Acta Orthop Scand
1990;61:255-7
45. Leonard MH, Duvrabcik P. Management of
fractured fingers in the child. Clin Orthop 1970;73:
160-8
46. Lorenzi GL, Rossi P, Quaglia F, Parenti G, De
Guidi G, Pelilli E. Growth disturbances following
fractures of the femur and tibia in children. Ital J
Orthop Traumatol 1985;11:133-7
47. MacEwen W. The Growth of Bone, Observations
on Osteogenesis, an experimental inquiry into the
Development and Reproduction of Diaphyseal
Bone. Glasgow, James Maclehose and Sons
1912;33-8
48. Malkawi H, Shannak A, Hadidi S. Remodelling
after femoral shaft fractures in children treated
by the modified Blount method. J Pediatr Orthop
1986;6:421-9
Bone remodeling in malunited fractures in children
49. Meals RA. Overgrowth of the femur following
fractures in children: influence of handedness. J
Bone Joint Surg [Am] 1979;61:381-4
50. Mintzer CM, Waters PM, Brown DJ. Remodelling
of a displaced phalangeal neck fracture. J Hand
Surg 1994;19:594-6
51. Moseley CF. General features of fractures in
children. AAOS Instr Course Lec 1992;41:337-46
52. Murray DM, Wilson-MacDonald J, Morscher E,
Rahn BA, Käslin M. Bone growth and remodelling
after fracture. J Bone Joint Surg [Br] 1996;78:42-50
53. Neer CS II, Cadman EF. Treatment of fractures
of the femoral shaft in children. JAMA 1957;162:
634-7
54. Ogden JA, Ogden DA, Pugh L, Raney EM, Guidera
KJ.Tibia valga after proximal metaphyseal fractures
in childhood: a normal biologic response. J Pediatr
Orthop 1995;15:489-94
55. Ogden JA. The uniqueness of growing bones.
In: Rockwood CA Jr, Wilkins KE, King RE, eds.
Fractures in children. Third ed. New York, etc.
JB Lippincott 1991;1-86
56. Ollier L. Traitè experimental et clinique de la
regeneration des os et de la production artificielle
des tissues osseux. Paris. Victor Masson et Fils.
1867
57. Önne L, Sandblom PH. Late results in fractures
of the forearm in children. Acta Chir Scand
1949;98:549-67
58. Parrini L, Paleari M, Biggi F. Growth disturbances
following fractures of the femur and tibia in
children. Ital J Orthop Traaumatol 1985;11:139-45
59. Pauwels F. Eine Klinische Beubachtung als
beispiel und beweis für funktionelle Anpassung
des Knochens durch Langenwachstum. Z Orthop
1975;113:1-5
60. Pauwels F. Biomechanics of the Locomotor
Apparatus: Contributions on the Functional
Anatomy of the Locomotor Apparatus. New
York. Springer Verlag. 1980
61. Ponseti IV, Morcuende Rojo JA. Introducción a las
lesiones traumáticas en la infancia. In: Lesiones
211
J. Gascó, J. de Pablos
Traumáticas del niño. Burgos J, González Herranz
P, Amaya Alarcón S. Eds. Madrid. Panamericana
1995;5-11.
62. Price ChT, Scott DS, Kurzner ME, Flynn JC.
Malunited forearm fractures in children. J Pediatr
Orthop 1990;10:705-12
63. Reynolds DA. Growth changes in fractured long-
bones: aa study of 126 children. J Bone Joint Surg
[Br] 1981;63:83-8
64. Roberts JA. Angulation of the radius in children’s
fractures. J Bone Joint Surg [Br] 1986;68:751-4
65. Roy DR, Crawford AH. Operative management
of fractures of the shaft of the radius and ulna.
Orthop Clin North Am 1990;21:245-50
66. Ryöppy S, Karaharju EO. Alteration of epi-
physeal growth by an experimentally produced
angular deformity. Acta Orthop Scand 1974;45:
490-8
67. Schneider M. The effect of growth on femoral
torsion. An experimental study in dogs. J Bone
Joint Surg [Am] 1963;45:1439-49
68. Shannak AO. Tibial Fractures in Children: Follow-
up Study. J Pediatr Orthop 1988;8:306-10
69. Shapiro F. Fractures of the femoral shaft in children.
Acta Orthop Scand 1981;52:649-55
70. Sharrard WJW. Paediatrics Orthopaedics and
fractures. Oxford and Edinburgh. Blackwell
Scientific Publications. Vol.1; 1979:1488-9
71. Spissak L, Majesky I, Holleitnerova M. Nase
skusenosti autoremodelaciou diafyzarnych
zlomenin predkolenia u deti. Acta Chir Ortop
Traum Cech 1969;36:176-8
72. Staheli LT. Femoral and Tibial growth following
femoral shaft fracture in childhood. Clin Orthop
1967;55:159-63
73. Steinert V. Unterarmsfrakturen im Kindersalter.
Bruns’ Beitr Klin Chir 1966;212:170-84
74. Stephens MM, Hsu LCS, Leong JCY. Leg length
discrepancy after femoral shaft fractures in
children. J Bone Joint Surg [Br] 1989;71:615-8
75. Strong ML, Wong-Chung J, Babikian G, Brody
A. Rotational remodeling of malrotated femoral
212
fractures: A model in the rabbit. J Pediatr Orthop
1992;12:173-6
76. Tarr RR, Garfinkel AI, Sarmiento A. The effects of
angular and rotational deformities of both bones
of the forearm. J Bone Joint Surg [Am] 1984;66:65-
70
77. Torode IP, Gillespie R. Rotationplasty of the lower
limb for congenital defect of the femur. J Bone
Joint Surg [Br] 1983;65:569-73
78. Valderrama JF, Trueta J. The effect of muscle
action on the intra-osseous circulation. J Path
Bact 1965;89:179-86
79. Vaughan FMA. A simple method of bone
measurement. X-ray focus 1966;7:22-7
80. Verbeek HOF. Does rotation deformity, following
femur shaft fracture, correct during growth ?.
Reconstr Surg Traumat 1979;17:75-81
81. Vijanto J, Kiviluoto H, Paanamen M. Remodelling
after femoral shaft fracture in children. Acta Chir
Scand 1975;141:360-5
82. Vittas D, Larsen E, Torp-Pedersen S. Angular
remodeling of midshaft forearm fractures in
children. Clin Orthop 1991;265:261-4
83. Volkmann R. Chirurgische Erahrungen uber
Knochenverbiegungen und Knochenwachsthum.
Arch Pathol Anat 1862;4:512-40
84. Von Laer L, Herzog B. Beinlangdendifferenzen und
rotationsfheler nach Oberschenkelscha-ftfrakturen
im Kindersalter. Therapeutische Beeinflussung
und spontane Korrektur. Helv Chir Acta 1978;45:17-
21
85. Wallace ME, Hoffman EB. Remodelling of angular
deformity after femoral shaft fractures in children.
J Bone Joint Surg [Br] 1992;74:765-9
86. Wolff J. Das Gesetz der Transformation der Knochen.
Berlin. Verlag von August-Hirschwald 1982
87. Younger ASE, Tredwell SJ, MacKenzie WG, King
PM, Tennan W. Accurate prediction of outcome
after pediatric forearm fracture. J Pediatr Orthop
1994;14:200-6
88. Zionts LE, MacEwen GD. Spontaneous
improvement of post-traumatic tibia valga. J
Bone Joint Surg [Am] 1986;68:680-7
 Part IV
Physeal surgery for the treatment of limb
length discrepancies
25 The timing of arrest of physeal activity in
the treatment of leg length discrepancy
C.F. Moseley
INTRODUCTION
The correction of leg length discrepancy
by physeal arrest involves the slowing down
of the growth of the long leg so that the short
leg can catch up. The orthopaedic surgeon
treating patients with this problem must
therefore assess both the amount of correction
to be achieved by the physeal arrest in the
long leg and the ability of the short leg to
catch up.
Another way of looking at this is that it
is the discrepancy at maturity which must
be corrected and not the actual discrepancy
in a growing child. Whatever one’s point of
view, it is necessary to take growth inhibition
in the short leg into account and to predict
the future growth of the legs.
This article presents three methods by
which these tasks can be accomplished and
the treatment goal reached by the correct timing
of physeal arrest. Step-by-step instructions and
examples for each of these methods have been
published elsewhere and are shown here in
Figures 2-4(9).
Three methods of assessment and
prediction
If one is prepared to accept a first
approximation of the actual growth pattern
then assessment and prediction can be
Reprinted with permission of Mapfre Medicina (vol. 4, suppl 2)
carried out using simple arithmetic(6,11,12).
Variations of the Arithmetic Method have
been presented a number of times in the
literature and successful results have been
reported. This method is the simplest and
most convenient of the three.
The Growth Remaining Method utilizes
documented patterns of growth combined
with both arithmetic and graphic techniques.
Although Green and Anderson published
only growth data and not an actual method,
the method presented here is based on their
growth study data(1,2). It thereby avoids using
approximations of the growth pattern. It is
more accurate than the Arithmetic Method but
less convenient since it requires the availability
not only of the growth remaining graph but
the graph showing the actual bone lengths.
The Straight Line Graph Method began as a
method of presenting growth data but evolved
into a method for assessing and predicting
growth(7,8). It is based on the data of Green and
Anderson but uses a special graph instead of
arithmetic. The graph, as it is used clinically,
is shown in Figure 1. Because it requires that
copies of the graph and drawing materials be
at hand it is perhaps the least convenient of the
three methods but is more accurate than the
Arithmetic Method and less prone to error than
the Growth Remaining Method.
215
C.F. Moseley
The step-by-step instructions in figures 2-4
are designed to be photocopied and can be
made available wherever leg length problems
are seen.
Three phases of analysis
Whichever method of assessment and
prediction is used, the analysis involves three
phases. The first phase is the assessment of
past growth and uses accumulated leg length
and skeletal age data to determine the growth
percentile of the child and the inhibition of
growth in the short leg. The second phase
is the prediction of future growth and
216
Figure 1. The Straight Line
Graph as it is used in clinical
practice.
correlates the patient’s long leg length with
the skeletal age to predict the mature length
of the long leg. Then, by incorporating the
growth inhibition of the short leg, its length
at maturity can also be determined. The third
phase is the prediction of the effect of surgery
and involves modifying the predicted future
growth pattern according to the effect of the
proposed physeal arrest on the growth rate
of the long leg.
DATA COLLECTION
The collection of valid data by consistent
 The timing of arrest of physeal activity in the treatment of leg length discrepancy

Step by step instructions

The Arithmetic method

Leg length data (for examples for all three methods)

Sex: Female
Age Skeketal age Right lenght Left le lenght
7+10 8+10 60.0 58.0
8+10 9+4 64.4 61.9
9+3 10+3 70.0 66.2

Prerequisite growth information:

Distal femoral plate grows 10 mm per year. Girls stop growing at 14 years of age.
Proximal tibial plate grows 6 mm per year. Boys stop growing at 16 years of age.

A. Assessment of past growth

1. Longest time interval for data: 1. Longest time interval for data:
= date of last visit - date of first = 93 - 710 = 15 = 1.42 yrs
2. Years of growth remaining: 2. Years of growth remaining:
= 14 (16 for boys) - age at last visit = 140 - 93 = 49 = 4.75 yrs
3. Past growth of legs: 3. Past growth of legs:
= present length - first measured length long = 70.0 - 60.0 = 10.0 cm
4. Growth rate of long leg: short = 66.2 - 58.2 = 8.0 cm
= past growth/time interval 4. Growth rate of long leg:
5. Growth inhibition: = 10.0/1.42 = 7.04 cm/yr
= (growth of long - growth of short) 5. inhibition:
growth of long = (10.0-8.0)/10.0 = 0.2

B. Prediction of future growth

1. Future growth of long leg: 1. Future growth of long leg:
= years remaining X growth rate = 4.75 X 7.04 = 33.4 cm
2. Future increase in discrepancy: 2. Future increase in discrepancy:
= future growth of long leg X inhibition = 33.4 X 0.2 = 6.7 cm
3. Discrepancy at maturity: 3. Discrepancy at maturity:
= present discrepancy + future increase = (70.0 - 66.2) + 6.7 = 10.5 cm

C. Prediction of effect of surgery

Effect of epiphyseodesis: Effect of epiphyseodesis:
= growth rate X years remaining Femoral: = 1.0 X 4.75 = 4.75 cm
Tibial: = 0.6 X 4.75 = 2.85 cm
Both: = 1.6 X 4.75 = 7.6 cm

Figure 2. Step by step instructions for the Arithmetic Method. The left column describes the methos in
general terms. The right column shows a specific example using the data of a hypothetical patient.

217
C.F. Moseley

Step by step instructions

The Growth Remaing Method

A. Assessment of past growth

1. Growth of both legs: 1. Growth of long
= present length - first length = 70.0 - 60.0 = 10.0
2. Present discrepancy: Growth of short
= length of long leg - length of short = 66.2 = 58.2 = 8.0
3. Growth inhibition: 2. Present discrepancy:
= (growth of long - growth of short) = 70.0 - 66.2 = 3.8 cm
growth of long 3. Growth inhibition
= (10.0 - 8.0) = 0.2
10.0

B. Prediction of future growth

1. Plot present length of leng on Green-Anderson 1. 90

50
leg length graph for appropriate sex. 70
2. Project to right parallel to standard deviation Leg length
60
50
lines until maturity to determine mature cm
40
length of long leg. 30
3. Future growth of long leg: 20
Girls
= mature length - present length 10
0
4. Future increase in discrepancy: 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18
= future growth long X inhibition Skeletal age

5. Predicted discrepancy at maturity:

=present discrepancy + future increase
2. Length of long leg at maturity = 81.1
3. Future growth of long leg
= 81.1 - 70.0 = 11.1
4. Future increase in discrepancy
= 11.1 X 0.2 = 2.2
5. Discrepancy at maturity
= 3.8 + 2.2 = 6.0

C. Prediction of effect of surgery

1. Correction from proximal tibial arrest
1. The effect of epiphyseodesis of the distal
= 2.7
femoral and proximal tibial plates for a given
Correction from distal femoral arrest
sex and skeletal age can be determined from
= 4.1
the Green-Anderson growth remaining graph.
Correction from combined arrest
2. The effect of lengthening is not affected by
= 2.7 + 4.1 = 6.8
growth

Figure 3. Step by step instructions for the Growth Remaining Method. The left column describes the
method in general terms. The right column shows a specific example using the data hypothetical patient
used for the Arithmetic Method.

218
 The timing of arrest of physeal activity in the treatment of leg length discrepancy

Step by step instructions

The Straight Line Graph Method

A. Assessment of past growth

1. Plot the point for the long leg on the sloping line labelled
“LONG LEG” at the appropriate length.
2. draw a vertical line through that point representing the current
assessment.
3. Plot the point for the short leg on the vertical line.
4. Plot the point for skeletal age with reference to the sloping
lines in the nomogram.
5. Plot successive visits in the same fashion.
6. Draw a straight line through thr short leg points to represent
the growth of the short leg.

B. Prediction of future growth

1. Draw the horizontal straight line which best fits the points
previously plotted for skeletal age. The fit to later points is
more important than to earlier points. This is the growth
percentile line.
2. From the intersection of the growth percentile line with the
maturity skeletal age line draw a vertical line to intersect the
growth lines of the two legs. This line represents the end of
growth.
3. The points of intersection with the two growth lines indicate
the predicted lengths of the legs at maturity.

C. Prediction of effect of surgery

1. To predict the outcomes following epiphyseodeses draw trhee
lines to the right from the last point for the long leg parallel to
the three reference slopes. The intersections of these lines with
the vertical line representing the end of growth indicates the
predicted lengths of the long leg after the trhee possible types
of epiphyseodeses.
2. To predict the outcome following leg lengthening drawa line
parallel to the growth line of the short leg but elevated above it
by the amoint of length gained.

Figure 4. Step by step instructions fir the Straight Line Graph Method. The left column describes the method
in general terms. The right column shows a specific example using the data of the same hypothetical
patient used for the Arithmetic.

219
C.F. Moseley
technique is an essential component of this
process. Assessment based on inaccurate data
or accurate data collected by inconsistent
technique will result in errors and, in turn,
unsatisfactory patient out-comes.
Measurement of leg length
Leg length can be measured by a variety
of techniques. A single view of the legs
on a long film introduces a magnification
error but shows angulation deformity and
is useful in young children who cannot stay
still for multiple exposures. The scanogram,
with separate views of the hips, knees and
ankles, avoids the magnification error. The
measurement capability of most CT scan
software can provide the necessary measu-
rements with less radiation and less expense
than conventional x-rays(3,5).
Whatever the technique, it is important
that consistent bony landmarks be used and
that data from different techniques not be
mixed. It behooves the orthopaedic surgeon
to satisfy himself that these requirements
have been met by reviewing the x-rays before
making a surgical decision.
Determination of skeletal age
Only one method is available for the
determination of skeletal age in the context of
leg length discrepancy. The Greulich-Pyle atlas
provides standards of development of the hand
and wrist of boys and girls(4). Comparison of
the patient’s x-ray to these standards provides
the skeletal age but is fraught with significant
inter- and intra-observer error. The estimation
of skeletal age is the weak link in the analysis
of growth.
The method of skeletal age determina-
tion described by Tanner, Whitehouse et al
is attractive in that it provides a skeletal age
in tenths of years(10). However, since it has
not been correlated to leg length and gives
different skeletal ages than the Greulich-Pyle
method, it is useless in this context.
220
ASSESSMENT OF PAST GROWTH
This is the first phase of the assessment
and uses accumulated leg length and skeletal
age data. The accuracy of this assessment is
improved by a greater number of data points
and a greater interval between the first and
the most recent measurements.
Assessment of the relationship between
the growth of the two legs
Calculation of the growth inhibition in
the short leg is necessary in the Arithmetic
and Growth Remaining Methods, but is an
automatic part of the Straight Line Graph
Method.
Assessment of the relationship between
the leg length and maturity
The Growth Remaining and Straight
Line Graph Methods take into account the
growth percentile. This may be of some
importance since taller children attain
more correction from physeal arrest than
short children, but the magnitude of the
difference is small.
PREDICTION OF FUTURE GROWTH
This is an essential step in the timing of
physeal arrest and its omission is the most
common error made. If the surgeon does
not predict the discrepancy at maturity then
growth inhibition in the short leg will result
in under-correction. Calculation only of the
shortening of the long leg ignores the fact that
the short leg has to catch up.
Prediction of the discrepancy at maturity
Descriptions of the Arithmetic Method in
the literature are not clear on how this step is
performed. One methods is to calculate the
annual increase in the discrepancy in past years
and, assuming that rate will continue until
growth ceases, to use that figure to calculate
the future increase.
 The timing of arrest of physeal activity in the treatment of leg length discrepancy
In the Growth Remaining Method the mature
length of the long leg can be determined by
graphically comparing the patient with the
population studied by Green and Anderson. The
points for the lengths of the femur and tibia of
the long leg are plotted on the appropriate graph
and extrapolated into the future. The mature
length of the short leg can then be calculated
since the growth inhibition is known.
The Straight Line Graph Method
automatically depicts the future growth of
the two legs and the ultimate discrepancy.
If it is of interest the discrepancy at maturity
can be read from the graph, but the numerical
value is not needed to use the method.
PREDICTION OF THE EFFECT OF
SURGERY
The Arithmetic Method predicts the
effect of physeal arrest by assuming that the
contribution of the growth plates is constant
over time. This is obviously only a first
approximation of the true state of affairs,
but appears to have been accurate enough to
produce good results in the hands of certain
authors.
The Growth Remaining Method uses graphs
of the growth remaining in the physes about
the knee for boys and girls as determined from
the growth studies of Green and Anderson.
In this way the inaccuracy of approximations
is avoided. As in the Arithmetic Method the
total shortening resulting from the physeal
arrest is compared with the discrepancy at
maturity to determine if the time is appropriate
for the surgery.
In the Straight Line Graph Method there is
a strict correlation between the rate of growth
of the leg and its line on the graph. A physeal
arrest therefore reduces the slope of the long
leg by a known amount which corresponds
to the specific plate arrested, and a line can
be drawn on the graph with predetermined
slope to represent the growth of the leg after
the arrest. If the timing is perfect this line will
meet the line representing the short leg excatly
at maturity.
CONCLUSION
Although this paper has dealt only with
physeal arrest, it is apparent that, once the
discrepancy at maturity has been predicted,
the orthopaedic surgeon is in a position to
consider the effects of acute shortening or
lengthening procedures also.
Of the three methods dealt with here, the
Arithmetic Method is the least accurate but
the most convenient. It may be appropriate,
therefore, to reserve its use for rough
approximations before the time for surgery
approaches. Both the Growth Remaining
Method and the Straight Line Graph Method
can be used with sufficient accuracy to achieve
satisfactory clinical results. Whereas the Growth
Remaining Method uses only the first and last
data points the Straight Line Graph Method
offers the potential advantages of utilizing all
the amassed leg length and skeletal age data,
thereby reducing the errors inherent in single
estimations, particularly of skeletal age.
Anything that can be accomplished
mathematically or graphically can also be
accomplished by computer, and computer
programs exist which perform all the functions
of the Straight Line Graph Method.
Finally, the orthopaedic surgeon must
remember that it is a patient that is being treated
and not just a leg length discrepancy. The goal
of treatment may be modified by many clinical
factors and perfect correction of the discrepancy
is not always the appropriate clinical goal.
The determination of timing of physeal
arrest is a process which presents some
complexity and requires a certain degree of
knowledge and familiarity with the available
techniques. If these requirements are met then
timing can be determined confidently and
good clinical results can be assured.
221
C.F. Moseley

BIBLIOGRAPHY 7. Moseley C. A straight-line graph for leg-length

discrepancies. J Bone Joint Surg 1977;59-A (2):174-
1. Anderson M, Green W, Messner M. Growth and
178.
predictions of growth in the lower extremities. J
Bone Joint Surg 1963;45-A:1. 8. Moseley C. A straight-line graph for leg length
discrepancies. Clin Orthop Rel Res 1978;136:33-
2. Anderson M, Green W T. Lengths of the femur and
40.
tibia; norms derived from orthoro-entgenograms
of children from five years of age until epiphyseal 9. Moseley C F. Assessment and prediction in leg-
closure. Am J Dis Child 1948; 75:279-290. length discrepancy. AAOS Instr Course Lect 1989;
38~325):325-30.
3. Glass R, Poznanski A. Leg-length determination
with biplanar CT scanograms. Radiology 10. Tanner J, Whitehouse R, Marshall W, et al.
1985;156:833-834. Assessment of skeletal maturity and prediction
of adult height (TW2method~. London: Academic
4. Greulich W, Pyle S. Radiographic atlas of the
Press, 1975.
skeletal development of the hand and wrist.
Stanford: Stanford University Press, 1959; 2nd ed. 11. Westh R, Menelaus M. A simple calculation for
the timing of epiphyseal arrest: a further report.
5. Helms C, McCarthy S. CT scanograms for measuring
J Bone Joint Surg 1981;63B:117-119
leg length discrepancy. Radiology 1984;151:802.
12. White J, Stubbins S J. Growth arrest for equalizing
6. Menelaus M. Correction of leg length discrepancy
leg lengths. JAMA 1944;126:1146-1149.
by epiphyseal arrest. J Bone Joint Surg 1966;48B:
336-339.

222
26 The timing of epiphysiodesis
G. Fabry and J. De Waele
INTRODUCTION
Epiphysiodesis of the growth plates around
the knee is the most frequently used operative
procedure for equalization of limb length since
its introduction by Phemister in 1933. The low
morbidity, relatively uncomplicated operative
technique and low incidence of complications
make it an excellent method for correction of
moderate leg length discrepancies, if calculations
are correctly done.
However, errors can occur at different phases
of the procedure of measuring and evaluating
the data. Usually a standing teleradiography
is taken to measure leg length discrepancy.
Imbalances, however, with ad- or abduction of
the hips, flexion of hips or knees can be causes
of error. Irregularities in the growth curve can
occur, but can also be due to differences in the
taking of the 6-monthly radiographs.
Recently computer tomography has been
proposed in leg length measuring, adding
however no major advantages. Important is
to use the same method all along in the same
patient.
A major step in the procedure is the
estimation of the bone age. Different methods
have been described. The most frequently
used is the atlas of Greulich and Pyle,
showing the maturation of hand and wrist.
A few drawbacks, however, are the fact
Reprinted with permission of Mapfre Medicina (vol. 4, suppl 2)
that it describes the bone age of American
children around 1950, and that between 9
and 13 year in girls, and 11 and 15 in boys,
the evaluation of the bone age is inaccurate.
Since this is a cruciate period in determining
the time of epiphysiodesis, complementary
methods should be added. Dimeglio has tried
to refine the method by adding 4 signs of bony
maturation: alignment, rectangle, fusion and
cupping of the epiphyses.
A quotation method has been developed by
Tanner and Whitehouse, claiming an accurateness
to 1/10 of a year. The application is however not
so easy and takes a long time, making it less
popular. Sauvegrain uses the elbow to determine
the bone age; this method, easy to use after the
age of 10, is an ideal complement to the Greulich
and Pyle atlas.
Prevision of future growth is the last step in
determining the exact time of epiphysiodesis. In
this regard the method of Green and Anderson
is most widely used. From these curves, several
mathematical methods have been deducted, often
relatively complex. In 1977 Mosely introduced a
graphic method, adding different advantages:
(1) the graphic representation of the growth
of the lower extremities, (2) the integration of
the standard deviations and (3) the use of only
two parameters, the bone age and the length
of femur and tibia.
223
G. Fabry, J. De Waele

Table 1. Etiology of leg length discrepancy (Group A and B)

I. Growth retardation: 48 patiens (57.8%)

Congenital: - hemiatrophy 12
- congenital dislocation of the hip 2
- talipes equinovarus 1
- bowing of the tibia 2
- congenital pseudarthrosis of the tibia 1
Infection: - arthritis of the hip 4
- osteomyelitis of the femur 4
Neuromuscular: - cerebral palsy 4
- poliomyelitis 5
Trauma: - femoral fracture 2
- tibial fracture 1
- damage of the epiphyseal plate 1
Legg-Calvé-Perthes
Tumor: - aneurysmal bone cyst 1
Neurovascular: - Volkmann contracture 1

II. Growth stimulation: 18 patiens (21.7%)

Congenital: Klippel-Trenaunay 2
- hemihypertrophy 1
- elephantiasis 1
Infection: - osteomyelitis 1
Trauma: - femoral fracture 6
- tibial fracture 2
- femoral and tibial fracture 3
Tumor: - hemangioma 1
- neurofibromatosis 1

III. Idiopathic: 17 patiens (20.5%)

A study, performed in our department, shows
the different pitfalls, encountered in the timing
of epiphysiodesis.
MATERIALS AND METHODS
This retrospective review concerns 83
patients (37 girls and 46 boys), who underwent
an epiphysiodesis in our department between
1968 and 1986.
In 47 patients, the timing of the
epiphysiodesis was based on the method
of Anderson and Green (Group A); in 36
patients the Moseley chart was used (Group
B). The largest number of patients presented
with leg length discrepancy due to growth
retardation (57.8%). Growth stimulation
was seen in 21.7% of cases. The most
frequent cause of leg length discrepancy
is congenital (30.1%), or unknown (20.5%)
(Table 1). The average chronologic age at
time of epiphysiodesis respectively for girls
and boys was 12 years and 5 months and
13 years and 10 months in group A; and 12
years and 2 months and 13 years and 11
months in group B.

224
 The timing of epiphysiodesis

Table 2. Average chronologic age, bone age and leg length discrepancy (LLD) at time of
epiphysiodesis

Group A (47) Group B (36)

Female(20) Male (27) Female (17) Male (19)
Average chronologic age 12y.+5m. 13y.+10m. 12y.+2m.
13y.+11m.

Average bone age 12y.+3m. 13y.+2m. 11y.+10m. 13y.+6m.

Average LLD 3.8 cm 2.94 cm

(minimum - maximum) (1.4 ———> 8.8) (1.7 ———> 8.2)

Table 3. Site of epiphysiodesis The average preoperative follow-up period

Group A Group B
Distal femur 8 8
Proximal tibia 8 6
Both 31 22
The average bone age, respectively for
girls and boys, was 12 years and 3 months
and 13 years and 2 months in group A; and
11 years and 10 months and 13 years and 6
months in group B.
The average leg length discrepancy in group
A measured 3.8 cm, ranging from 1.4 cm to 8.8
cm; and 2.94 cm in group B ranging from 1.7 cm
to 8.2 cm (Table 2).
The site of epiphysiodesis was 8 times
in the distal femur in both groups; 8 times
in group A and 6 times in group B in the
proximal tibia; and the distal femur and the
proximal tibia, 31 times in group A and 22
times in group B (Table 3). These figures show
that both groups are comparable, concerning
age and site of epiphysiodesis.
In all cases of proximal tibial epiphysiodesis,
a proximal fibular epiphysiodesis was also
performed. The technique described by
Phemister in 1933 was used in all cases. Bone
age was estimated with the help of the atlas
of Greulich and Pyle.
measured 3 years and 2 months in group A,
ranging from 1 month to 15 years and 4 months;
and 2 years and 2 months in group B, ranging
from 2 months to 7 years and 8 months (Table 4).
The preoperative follow-up was less than 1 year
in 36 patients or 43.4%. Postoperative follow-up
and last radiological measurement was done at
maturity (approximately at 16 years bone age
for girls and 18 for boys).
The postoperative follow-up period
respectively for girls and boys measured 3 years
and 7 months and 4 years and 8 months in group
A, and 4 years and 1 month and 4 years and 9
months in group B (Table 4).
RESULTS
A final length discrepancy of less than 1.5
cm (which is well tolerated) was judged as
a satisfactory result. At bone maturity, the
average leg length discrepancy in group A
measured 1.9 cm and in group B 1.48 cm (Table
5).
In group A, 24 patients out of 47 had a
satisfactory result (51%), as to 23 patients out
of 36 in group B (63.9%). 8 patients (6 or 25% in
group A and 2 or 8.7% in group B) developed an
overcorrection, and 37 (16 or 66.7% in group A and
21 or 91.3% in group B) an undercorrection.
In 15 patients, the poor results were caused
by mistakes in estimation of bone age and thus

225
G. Fabry, J. De Waele

Table 4. Pre- and post-operative follow-up

Group A Group B

Pre-operative 3y.+2m. 2y.+2m.

(Range) (1m ----> 15y.+4m.) (2m ----> 7y.+8m.)
Post-operative Female Male Female Male
3y.+7m. 4y.+8m. 4y.+1m. 4y.+9m.

Table 5. Results

Group A Group B

Average final leg length 1.9 cm 1.48 cm

discrepancy
Good µ 1.5 cm 24 (51%) 23 (63.9%)
Overcorrection 6/24 (25%) 2/23 (8.7%)
Undercorrection 16/24 (66.7%) 21/23 (91.3%)
Poor 23 (49%) 12 (36.1%)
Mistakes in estimation 7/23 (30.4%) 8/13 (61.5%)
Too late at first visit 8/23 (34.8%) 3/13 (23.1%)
Unpredictable growth rate 7/23 (30.4% 2/13 (15.4%)
Unknown cause 1

in prediction of the time of epiphysiodesis Two patients had to undergo an

(30.4% of poor results or 15% of the total in
group A and 61,5% of poor results or 22%
of the total in group B). In 11 patients the
poor result was unrelated to the method
used and caused by a too late referral, so that
full correction of the leg length discrepancy
could not be obtained (34.8% of poor results
or 17% of the total in group A and 23.1% of
poor results or 8% of the total in group B). In
9 patients unpredictable changes in growth
rate caused a poor result (30.4% of poor results
or 15% of the total in group A, and 15.4% of
poor results or 6% of the total in group B).
COMPLICATIONS
In total, 8 patients or 9.6% presented with
a complication (Table 6).
epiphysiodesis of the other side due to
overcorrection of more than 1.5 cm. In one
patient, the leg length discrepancy had not
improved one year after the epiphysiodesis
of the distal femur. For that reason, an
epiphysiodesis of the proximal tibia was
added without, however, a good result.
Three patients developed a valgus
deformity of the knee after the
epiphysiodesis, secondary to asymmetrical
fusion of the physis. This represents a
serious complication. In one of them, a
varus osteotomy had to be performed. In
another patient, who developed a varus
deformity after the epiphysiodesis of the
proximal tibia, correction was achieved by
stapling of the lateral side of the growth
cartilage of the distal femur.

226

Table 6. Complications
- Overcorrection 2 better accepted by the patient and his parents;
- Absence of closure of epiphyseal plate 1
- Asymmetrical closure 4
- Deep infection 1 mistake.
One patient had a deep infection responding
well to antibiotics.
DISCUSSION
Epiphysiodesis is potentially a very
effective method of equalizing moderate
leg length discrepancies, i.e. differences
between 2 cm and 5 cm. Larger discrepancies
or discrepancies at maturity must be corrected
with other techniques.
In order to have an accurate timing of
epiphysiodesis, several conditions must be
fulfilled. Preoperative evaluation of growth
over several years with exact radiographical
measurements of leg lengths according to
a standard method is necessary. With each
measurement of leg length, an estimation of
bone age must be done. So far, the Atlas of
Greulich and Pyle has been used taking into
account its shortcomings. Sometimes the lapse
of time between the bone ages is more than 1
year. The atlas has been made on the basis of
X-rays of North-american children in the first
half of the twentieth century; growth patterns
have changed since. Some important reference
points are the appearance of the sesamoid bone
of the thumb and the closure of the growth
cartilage of the distal phalanx of the middle
finger. An epiphysiodesis performed after the
closure of the growth cartilage of the distal
phalanx of the middle finger will have no
effect on leg length discrepancy.
A third condition which must be fulfilled
is that the Moseley chart or the method of
Green and Anderson must of course be used
correctly.
The timing of epiphysiodesis
Overcorrection was less frequent than
undercorrection. In fact, an undercorrection is
an overcorrection is more felt as a medical
The number of patients, coming too late
for epiphysiodesis is still relatively high
(17% in group A and 8% in group B). The
percentage of unpredictable growth rate
as a cause of poor results, has come down
from 30.4% in group A to 15.4% in group
B. The reason is probably that the different
variables as growth inhibition, bone age
and relative height are automatically built
in into the Moseley graph, which improves
predictability. The most important problem,
very prominent in group B, remains, however,
the determination of bone age. A reason
might be that very often different residents
and surgeons determine the bone age and fill
in the Moseley chart. Important is that some
months before operation, a recalculation of
leg length and redetermination of bone age
is done, by the same person.
Seven patients had to be reoperated
on. They represent a serious complication.
Especially a high tibial osteotomy is prone
to complications.
Since 1979 Moseley’s straight line graph
has been used to determine the time of
epiphysiodesis. It has the advantage of being
a concise, one page, graphic illustration of
the growth pattern of the long and short
limbs. The results in our series when using the
Moseley chart, are however not statistically
different than with the Anderson and Green
method.
A considerable number of mistakes were
still made using the Moseley chart. These
mistakes are due to difficulty in estimating
bone age, in extrapolating points to straight
lines, and in interpretation of the data on the
graph. With the help of Dr. Moseley we made
a computer program, making the use of his
method very easy and eliminating graphical
227
G. Fabry, J. De Waele

errors. The determination of the bone age, and abnormal growth rate are omitted, the
however, remains a possible source of error. surgeon was only responsible for 18% poor
However, when the uncontrollable results in the total group of patients (15% in
causes of poor results, such as late referral group A, 22% in group B).

228
27 Physeal surgery for the treatment of
lower limb length discrepancy
U. Givon and J.R. Bowen
The most common presentations of physeal
injuries and the resulting premature closure of the
physis are limb length discrepancy and angular
deformity. These deformities effect quality of life
and may lead to long term morbidity. Several
treatment modalities were developed and
improved in the last decades. The aim of this
chapter is to review the treatment methods
based on surgery of the physis.
TREATMENT OF LOWER LIMB
LENGTH DISCREPANCY
Decision making in the treatment of
lower limb length discrepancy is based on
the predicted difference at the end of growth.
Treatment options include conservative
treatment, shortening or inhibiting the
growth in the longer extremity, lengthening
of the shorter extremity and prosthetic
replacement (1-3) . A shoe lift is used for
discrepancies of up to 2 cm or in a case of
a child waiting for the appropriate age for
surgery. The shoe lift should be rounded at
the front to prevent tripping and hollow to
reduce weight. Full equalization is not needed
and a small part of the discrepancy may be
compensated by pelvic tilt, knee flexion and
foot equinus. Epiphysiodesis or shortening
are suitable for discrepancies of 2-5 cm, but in
the case of epiphysiodesis at least two years
of remaining growth are necessary to achieve
a good result. In the case of a discrepancy
of 5-15 cm, an elongation procedure may be
undertaken if there is adequate function of
joints, muscles and nerves and good bone
quality. The patient mental ability to cope
with the rigors of an elongation process may
play a part in decision making. When the
discrepancy is more than 15-20 cm or there
is any other contraindication for elongation,
amputation and prosthetic fitting should be
considered. In general, it is advisable to correct
any coexisting deformity prior to undertaking
any operative length equalization(1).
Epiphysiodesis is defined as the controlled
arrest of growth in the physis of a skeletally
immature patient. This procedure is most
frequently performed for discrepancies of 2-5
cm. The operative goal of an epiphysiodesis
is to achieve bony fusion of the metaphysis
and epiphysis in the periphery of the physis,
to tether the physis and prevent growth. The
epiphysiodesis has to be well timed in order to
achieve equal lengths in both lower limbs at the
time of skeletal maturity.
Planning of the operation is based on
the patient’s skeletal age and the calculation
of the remaining growth and the estimated
discrepancy at skeletal maturity. Several
methods for planning were described by
Menelaus (4), Anderson and Green (5) and
229
U. Givon, J.R. Bowen
Figure 1. Open epiphysiodesis: A block of bone
removed from the distal femoral physis with a
White-Stubbins chisel, rotated 90° and reinserted
into the bone obliterating the epiphysiodesis site.
Moseley(6,7). Different developmental patterns
were described for various etiologies for lower
limb length discrepancy [8] and these patterns
could influence the timing for surgery. The
reader is referred to the literature concerning
the calculations associated with the planning
of the operation.
EPIPHYSIODESIS
Phemister(9) described the first technique
of open epiphysiodesis in 1933. A variation
on the technique and a special chisel were
reported by White and Stubbins in 1944(10). This
operative technique was widely described in
the literature(1,2,9,10). Reported complications of
stiffness, angular deformities and unsightly
scars were reported (1,4,11). Percutaneous
epiphysiodesis (12,13) became a common
technique of epiphysiodesis in the last decade,
but open epiphysiodesis is still in use.
Technique - Open epiphysiodesis
(modified Phemister technique).
Epiphysiodesis is performed with
the patient under general anesthesia and
tourniquet control. The physis is located using
image intensification and a 1 cm incision is
performed over the lateral side. The physis
230
is visualized and a 1 cm cube is excised from
the epiphysis, physis and metaphysis using
the White chisel. A small curette is then
used to destroy the physis. The excised cube
of bone is then reinserted into the wound
rotated 90 degrees (Fig. 1). The process is
repeated on the medial side of the physis.
About 50% of the area of the physis has to be
destroyed to ensure physeal closure If both the
proximal tibia and the distal femur should be
epiphysiodesed, four separate incisions should
be made. Localization of the physis with image
intensification and small incisions improved
the cosmetic aspects of this operation.
Technique - Percutaneous epiphysiodesis.
Percutaneous epiphysiodesis is performed
with the patient under general anesthesia with
tourniquet control on the proximal thigh and
under image intensification. After identification
of the physis, a 3 mm stab wound is performed
with a scalpel over the lateral side of the physis
(Fig. 2A). A 3 mm wide osteotome is used to
make a longitudinal slit in the perichondrium
and is then driven 1 cm into the physis. The
osteotome is rotated 180 degrees to create a
hole in the cortex to one third of the width of
the growth plate. A 3 mm curette is inserted
into the defect in the growth plate and is used
to ablate the physis cephalad and caudad
in windshield wiper fashion (Fig. 2B). Each
swipe of the curette is verified with the image
intensifier to prevent injury to the posterior
neuro-vascular structures. In the femur the
procedure is repeated on the medial side of the
physis. The middle third of the growth plate is
left intact to provide mechanical stability and
protect the midline neuro-vascular structures
(Fig. 2C). The wound is closed with a single
subcuticular stitch.
The proximal fibular physis is usually not
approached in the percutaneous route because
of the proximity of the common peroneal
nerve. A 1 cm longitudinal anterior incision is
performed between the fibular and the tibial
 Physeal surgery for the treatment of lower limb length discrepancy

B C
Figure 2. Percutaneous epiphysiodesis: A) A curette in the distal femur. Notice the minimal incision.
B) A curette in the medial part of the physis. Dye has been injected into the lateral aspect demonstrating
adequate ablation of the physis. C) Epiphysiodesis sites in the distal femur and proximal tibia shown.

physes. The fibular physis is visualized and
then ablated with a curette. The lateral third of
the tibial physis is ablated in the percutaneous
technique using the same incision.
After surgery the knee is wrapped with
a small compressive dressing to prevent
the formation of a hematoma. The knee is
maintained in a knee immobilizer for 2 weeks.
During the next 2 weeks the immobilizer is
removed daily for range of motion exercises.
Full weight bearing crutch supported gait is
allowed as soon as tolerated which is usually
after 48 hours.
Slightly different surgical techniques,
utilizing drills and dental burrs(14); drilling in
various directions under image intensification(15);
cannulated drills used through the whole
width of the physis (16), a combination of
drilling and curetting(17) and cannulated
tubesaws(18) were described by other authors.
No studies comparing these techniques were
performed so far and all the authors reported
satisfactory results. Comparison of the results
of percutaneous epiphysiodesis to open
epiphysiodesis in the Phemister method showed
the percutaneous method to be superior(13-17,19).
Most of the complications described
after open epiphysiodesis, mainly infection,
stiffness and ugly scars were not reported after
percutaneous epiphysiodesis. The surgical
dissection involved in adequate exposure in
the open method probably had a role in the
cause of these postoperative problems. The
use of power instruments in percutaneous
epiphysiodesis may cause soft tissue burning
and damage around the incision(13).

231
U. Givon, J.R. Bowen
STAPLING
A different technique for the treatment of
limb length inequality and angular deformities
was described by Blount(20-22). This technique
was based on temporarily delaying physeal
growth at a younger age by inserting metal
staples across the physis, and removing
them just before physeal closure to enable
perfect limb length equalization. Various
complications were reported including over
and under correction, premature physeal
closure and continued growth despite the
stapling causing staples to dislodge or
fracture(2,20-22). The necessity to insert three
staples on each side caused unsightly scars.
This technique did not achieve satisfactory
results in all hands and is not in wide use today.
CORRECTION OF ANGULAR
DEFORMITY
Angular deformity may be corrected by
arresting the growth at one side of the physis
and operative techniques were described for
various bones(20,21,25-27). The majority of these
operations are performed on older patients
who are still skeletally immature and have
some growth potential in the other side of the
physis. The physician treating these patients
should be aware on the normal values for
physiologic varus and valgus in every age
group. As a rule of thumb children less than
18 months have a varus positioning of their
lower limbs, gradually turning into valgus
around 3 years of age. By the age of 5 to 7
years, there should be complete resolution
of any physiologic malpositioning. The
treating physician is advised to monitor the
growth of the child for several years prior to
undertaking any surgical solution. In patients
presenting at an age when there is not sufficient
growth potential left, an osteotomy may be
the procedure of choice.
Stapling was a well accepted technique for
addressing genu varum or genu valgum, as
232
described by Blount(20-22) and by Howorth(25).
However, the procedure had all the
disadvantages of stapling when used for leg
length correction: staple break down, staple
bending, staple dislodgement, permanent
closure of the physis and scarring. The procedure
necessitated 2 operations - one for staple insertion
and a second operation for their removal. Bowen
and colleagues(27,28) have devised a method of
hemiepiphysiodesis for the treatment of angular
deformities around the knee in the growing
child. The procedure is performed either at the
distal femur or the proximal tibia, depending
upon which contributes more to the deformity.
Hemiepiphysiodesis will cause some shortening
of the operated limb, as part of the physis will
cease to function. The shortening is proportional
to the angle of correction and can be calculated
through the equation :
LLD = r - cos θ
where LLD is the lower limb length discrepancy,
r is the length of the limb measured distal to
the epiphysiodesis site and θ is the angle of
correction.
A chart has been developed for the planning
of the correct time of the hemiepiphysiodesis,
allowing the remaining half of the physis to
correct the malalignment. The physician has
to have the size of the angular deformity as
well as the width of the bone at the site of
the physis or the physeal distance, obtained
from standing radiographs, the patient’s
skeletal age is calculated from a radiograph
of the left wrist and the growth percentile
is obtained from the normal growth charts.
The intersection of the physeal distance and
angular deformity are located and a horizontal
line is made to the appropriate percentile on
the Green Anderson graph, depending on the
sex of the patient and the bone to be operated
(Fig. 3). A vertical line is dropped from that
intersection point to find the skeletal age at
the which correction should be done. When
this calculation method is applied to children
with angular deformities caused by skeletal
 Physeal surgery for the treatment of lower limb length discrepancy
Figure 3. Chart of angular deformity versus growth
remaining.
dysplasias, one should bear in mind that their
growth pattern does not conform exactly to
these calculations.
Technique - Hemiepiphysiodesis
The limb is prepared and draped as for
complete epiphysiodesis. If the deformity is
in valgus the medial side is approached, and
if the deformity is in varus the lateral side is
approached. The epiphysiodesis may be either
open or percutaneous. The medial or lateral
third of the physis is ablated to create a bony
bar, as described previously. The proximal
fibula has to be addressed if the lateral side
of the proximal tibia is treated.
Stapling for angular correction is performed
on the selected aspect of the knee, using the
same technique as for leg length discrepancy.
The staples will have to be removed if the
planned date of correction will occur before
closure of the physis. A rebound phenomenon
was described when the staples were removed(1)
and extra 5 degrees of correction should be
allowed for this unpredicted development.
Most surgeons attempt to time the stapling
to coincide with skeletal maturity.
Other uses and techniques of asymmetric
epiphysiodesis were described such as
epiphysiodesis of the medial maleolus
using a screw was described to correct ankle
valgus(29,30). Convex epiphysiodesis of the spine
for treatment of congenital scoliosis due to
hemivertebrae was found to be beneficial(31)
but it failed in the case of idiopathic infantile
scoliosis(32).
Another method for the correction of
angular deformities is by physeal distraction.
This method is based on closed gradual
distraction of the growth plate using an
external fixator. Originally described for
limb length equalization(33,34) it was used for
treatment of angular deformities around the
knee by several authors(35-37). Good results were
reported using different kinds of unilateral
external fixators, usually with free hinges
close to the physis.
EXCISION OF PHYSEAL BARS
Premature partial arrest of the physis may
cause shortening and an angular deformity
of the involved bone if the remaining growth
potential is high. Damage to the physeal
cartilage will cause invasion of the damaged
area by fibro-vascular tissue followed by the
formation of trabecular bone at the periphery
of the vascular channel and then enlarging to
form a discrete bridge. The size of the created
bony bridge is dependent on the size of the
physeal defect caused by the injury(38). The size
and location of the bar will dictate the type
of bony deformity which will develop. If the
bar is located peripherally angular deformity
and shortening will ensue. If the bar is located
centrally, growth remaining in the periphery
will cause tenting of the center of the physis
and shortening without angular deformity.
Trauma is the most common etiology
of physeal bar formation but any of the
reasons mentioned above may cause physeal
bridging(38,39). Since the formation of a bony bar
233
U. Givon, J.R. Bowen
is a slow process, it may become apparent only
years after the trauma. First signs of developing
bony bars may be demonstrated by MRI 4
months after the trauma and 8 months after
the trauma the diagnosis is clear(40). A high
index of suspicion practiced by the treating
physician and the timely use of the proper
imaging techniques may enhance diagnosis
and treatment before permanent deformity
occurs.
The distal femur and the proximal tibia
are involved in 3% of the cases of physeal
trauma yet they are the most common sites
for physeal surgery. These growth plates are
large and have irregular contours, which may
be predisposing towards the formation of
bony bars(1). In addition, angular deformities
or shortening around the knee are likely to
be functionally and cosmetically disturbing,
and will the patient is more likely to seek
medical help.
Excision of bony bars was first described
by Langenskiöld in 1967 (41,42). Since then,
various clinical studies have supported the
efficacy of this treatment method, subject to
adequate patient selection and pre-operative
planning (43-45). Prior to undertaking any
attempt of physeal bar resection, the amount
of deformity and the remaining growth should
be evaluated. If there is not at least one year
of remaining growth the deformity will not
be corrected and the surgeon should consider
other solutions(42). Any deformity larger than
20 degrees is not likely to be corrected after
bony bar resection and will necessitate an
additional metaphyseal osteotomy and bars
occupying more than 50% of the area of the
physis should not be resected(43) since the
growth potential of the remaining physeal
tissue is unpredictable. Physeal bars caused
as the result of infection are likely to be more
extensive, harder to define during surgery
and bear a worse prognosis.
Mapping of the physeal bar is performed
with the use of tomography, computerized
234
tomography and MRI as described above.
A technique of 3D MR reconstruction was
reported to improve imaging of the bony bar,
but this technique is not widespread and takes
several hours of MRI processing to achieve a
good result(46).
Physeal bar resection
The involved limb is prepared and draped
free. The physeal bar is identified using
pre-operative imaging studies and image
intensification. The bar is usually as dens
as cortical bone and is easily identifiable in
the cancellous bone of the metaphysis. In
the case of a peripheral bar, the periosteum
is raised over the bar and the bar is excised
under direct vision using a motorized burr.
The use of this instrument allows excellent
visualization of the bar and the ablation of
as little as possible of the normal physeal
tissue. In the case of a centrally located bar,
it is approached through a cortical window
performed in the metaphysis 2 cm above the
involved growth plate. A tunnel is made with
a burr down to the level of the bar and it is
excised under image intensification control.
Normal physis which is white and shiny,
should be seen in the borders of the cavity
created by the burr (Fig. 4). A small dental
mirror or an arthroscope(47) may be used for
visualization of centrally located bars. Blood
should not be allowed to accumulate in the
resected area as it will enable the recurrence
of the bar. An interposition material of the
surgeon’s choice should be placed in the
cavity in the physis and the resected area
in the metaphysis should be filled with
morselized bone graft. Metal markers should
be placed in the epiphysis and metaphysis,
so that subsequent growth can be monitored
radiographically. A different approach to
a central bar was described by Jackson(48).
He reported one case where he removed a
predrilled wedge of bone from the metaphysis
reaching to the bar. Using this procedure the
 Physeal surgery for the treatment of lower limb length discrepancy

A B

Figure 4. Resection of a central physeal bar. A male patient diagnosed at the age of 7 years, 2 months
as having a central bony bridge as a result of a Salter Harris type 3 injury. A) Preoperative views of the
patient at the age of 10 years, 8 months. B) Postoperative view demonstrating resection of the bar and
interposition by silicone rubber.

bar was accessible for excision under direct
visualization and the bone was replaced
and screwed over the interposition material
holding it in place.
There are various opinions about the
type of interposition material to be placed
in place of the excised bar. Autogenous fat
is preferable because it is easily obtained
and does not require a second procedure for
removal(42). The grafted fat is incorporated,
remains a living tissue and was found to
grow with the cavity(49). Other possibilities
are radiolucent inert materials unaffected
by long term exposure in the body such as
cranioplast which is methyl-methacrilate
without barium. Silicone rubber was also
used in the past for interposition. Patients
treated with a fat graft may need protection
against fracture. If cranioplast is used,
sufficient support should be present to
eliminate the need for external support,
thus making it more suitable for use in
the case of large defects. All interposition
materials may be left in place unless they
cause problems. Removal of the artificial
substances has been reported to be associated
with technical difficulties and may require
the use of chisels and burrs.
Recurrences may be treated by a second
attempt of resection, if sufficient growth
remains. A recurrence may be diagnosed
by the fact that the interposition material
grows with the metaphysis and not with the
epiphysis. If insufficient growth remains,
an osteotomy or an elongation procedure
may be used. In general, bar resection can
be expected to yield satisfactory results if
the bar is less than 50% of the physis area

235
U. Givon, J.R. Bowen
and is not the result of infection. The type
of interposition material does not effect the
results of the operative procedure(1,50). There
always remains, however the possibility of
failure of the procedure and the patient and
the family should be aware that additional
procedures may be needed in the future.
Physeal surgery is a developing field of
interest and there are exciting possibilities for
further improvements in the future. injudicious
use of these techniques may cause unnecessary
morbidity and expense.
REFERENCES
1. Guille JT, Yamazaki A, Bowen JR. Physeal surgery:
Indications and operative treatment. Am J of Orthop,
1997;27:323-332.
2. Bowen JR. Surgical treatment of leg length
discrepancy. In Dee R, Mango E, Hurst LC eds.
Principles of orthopaedic practice. 1st ed. New
York McGraw Hill: 1191-1208; 1989.
3. Burgansky Z, Ganel A, Givon U. Leg lengthening
for length inequality. Harefua, 1997;132:392-396.
4. Menelaus MB. Correction of leg length discrepancy
by epiphyseal arrest. J Bone Joint Surg, 1966;48-
B:336-339.
5. Anderson m, Green WT Messner MB. Growth
and prediction of growth in the lower extremity.
J Bone Joint Surg, 1963;45-A:1-14.
6. Moseley CF. A straight line graph for leg length
discrepancies. J Bone Joint Surg, 1977;59-A:174-179.
7. Moseley CF. Leg length discrepancy: Assessment
and growth prediction. In Dee R, Mango E, Hurst
LC eds. Principles of orthopaedic practice. 1st ed.
New York McGraw Hill: 1186-1191; 1989.
8. Shapiro F. Developmental patterns in lower
extremity length discrepancy. J Bone Joint Surg,
1982;64-A:639-651.
9. Phemister DB. Operative arrestment of longitudinal
growth of bones in the treatment of deformities.
J Bone Joint Surg, 1933;15-A:1-15.
236
10. White JW, Stubbins SG. Growth arrest for
equalizing leg lengths. JAMA, 1944;126:1146-1149.
11. Stephens DC, Herrick W, MacEwen GD.
Epiphysiodesis for limb length inequality: results
and indications. Clin Orthop. 1977;136:41-48.
12. B o w e n J R , J o h n s o n W J . P e r c u t a n e o u s
epiphysiodesis. Clin Orthop, 1984;190:170-173.
13. Timperlake RW, Bowen JR, Guille JT et al.
Prospective evaluation of fifty three consecutive
percutaneous epiphysiodesis of the distal femur
and proximal tibia and fibula. J Pediatr Orthop,
1991;11:350-357.
14. Canale ST, Christian CA. Techniques for
epiphysiodesis about the knee. Clin Orthop,
1990;255:81-85.
15. Ogilvie J, King K. Epiphysiodesis: two year clinical
results using a new technique. J Pediatr Orthop,
1990;10:809-811.
16. Gabriel KR, Crawford AH, Roy DR et al.
Percutaneous epiphysiodesis. Pediatr Orthop,
1994;14: 358-362.
17. Liotta FJ, Ambrose TA, Eilert RE. Fluoroscopic
technique versus Phemister technique for
epiphysiodesis. J Pediatr Orthop, 1992;12:248-251.
18. Macnicol MF, Gupta MS. Epiphysiodesis using
a cannulated tubesaw. J Bone Joint Surg, 1997;79-
B:307-309.
19. Porat S, Peyser A, Robin GC. Equalization of lower
limbs by epiphysiodesis: results of treatment. J
Pediatr Orthop, 1991;11:442-448.
20. Frantz CH. Epiphyseal stapling: a comprehensive
review. Clin Orthop 1971;77:149-157.
21. Blount WP, Clarke GR. Control of bone growth
by epiphyseal stapling. J Bone Joint Surg, 1949;31-
A:464-478.
22. Blount WP. A mature look at epiphyseal stapling.
Clin Orthop, 1971;77:158-163.
23. Pilcher MF, Epiphyseal stapling.; thirty five cases
followed to maturity. J Bone Joint Surg, 1962;44-
B:82-85.
 Physeal surgery for the treatment of lower limb length discrepancy
24. Poirier H. Epiphyseal stapling and leg equalization.
J Bone Joint Surg, 1968;50-B:61-69.
25. Howorth B. Knock knees, with special reference
to the stapling operation. Clin Orthop, 1971;77:233-
246.
26. Zuege RC, Kempken TG, Blount WP. Epiphyseal
stapling for angular deformities at the knee. J Bone
Joint Surg, 1979;61-A:320-329.
27. Bowen JR, Leahey JL, Zhang ZH et al. Partial
epiphysiodesis at the knee to correct angular
deformity. Clin Orthop, 1985;198:184-190.
28. Bowen JR, Torres RR, Forlin E. Partial
epiphysiodesis to address genu varum or genu
valgum. J Pediatr Orthop, 1992;12:359-364.
29. Beals RK. The treatment of ankle valgus by surface
epiphysiodesis. Clin Orthop, 1991;266:162-169.
30. Stevens PM, Belle RM. Screw epiphysiodesis for
ankle valgus. J Pediatr Orthop, 1997;17:9-12.
31. Thompson AG, Marks DS, Sayampanathan SRE
et al. Long term results of combined anterior and
posterior epiphysiodesis for congenital scoliosis
due to hemivertebrae. Spine, 1995;20:1380-1385.
32. Marks DS, Ikbal MJ, Thompson AG et al. Convex
spinal epiphysiodesis in the management of
progressive infantile scoliosis. Spine, 1996;21:1884-
1888.
33. Di Bastiani G, Aldegheri R, Renzi Brivio L et
al. Chondrodiastasis - a controlled symetric
distraction of the epiphyseal plate. J Bone Joint
Surg, 1986;68-B:550-556.
34. Aldegheri R, Trivella G, Lavini F. Epiphyseal
distraction. Clin Orthop, 1989;241:117-127.
35. Ganel A, Heim M, Farine I. Asymmetric epiphyseal
distraction in treatment of Blount’s disease. Orthop
Review, 1986;25:237-240.
36. Aldegheri R, Trivella G, Lavini F. Epiphyseal
distraction: hemichondrodiastasis. Clin Orthop,
1989;241:128-136.
37. Canadell J, De Pablos J. Correction of angular
deformities by physeal distraction. Clin Orthop,
1992;283:98-105.
38. Ogden JA. Skeletal growth mechanism injury
patterns. Mapfre Medicina, 1993;4 (suppl 2):125-132.
39. Ogden JA. The evaluation and treatment of partial
physeal arrest. J Bone Joint Surg, 1987;69-A:1297-
1302.
40. 1Snyder M, Harcke HT, Bowen JR et al. Evaluation
of physeal behavior in response to epiphysiodesis
with the use of magnetic resonance imaging. J
Bone Joint Surg, 1994;76-A:224-229.
41. Langenskiold A. The possibilities of eliminating
premature partial closure of the epiphyseal plate
caused by trauma or disease. Acta Orthop Scand,
1967;38:267-279.
42. Langenskiold A. Surgical treatment of partial
closure of the growth plate. J Pediatr Orthop,
1981;1:3-11.
43. Kasser JR. Physeal bar resections after growth
arrest about the knee. Clin Orthop, 1990;255:68-
74.
44. Broughton NS, Dickens DRV, Cole WG et al.
Epiphysiolysis for partial growth plate arrest:
results after four years or at maturity. J Bone Joint
Surg, 1989;71-B:13-16.
45. Williamson RV, Staheli LT. Partial physeal growth
arrest: treatment by bridge resection and fat
interposition. J Pediatr Orthop, 1990;10:769-776.
46. Borsa JJ, Peterson HA, Ehman RL. MR imaging
of physeal bars. Radiology, 1996;199:683-687.
47. Stricker S. Arthroscopic visualization during
excision of a central physeal bar. J Pediatr Orthop,
1992;12:544-546.
48. Jackson A. Excision of the central physeal bar: a
modification of Langenskiold’s procedure. J Bone
Joint Surg, 1993;75-B:664-665.
49. Langenskiold A. The fate of fat transplants in
operations for partial closure of the growth plate.
J Bone Joint Surg, 1986;68-B:234-238.
50. Martiana K, Low CK, Tan SK et al. Comparison of
various interpositional materials in the prevention
of transphyseal bridge formation. Clin Orthop,
1996;325:218-224.
237
28 Surgical correction of partial growth plate
closure using physeal distraction.
Experimental and clinical experience
G. Bollini, J.L. Jouve, J. Cottalorda, P. Frayssinet,
J.M. Guillaume and J.C. Godchaux
A lesion of the growth plate may entail
the development of an physeal bone-bridge,
whether its cause is due to traumatic injury or
the result of vascular or infectious disorders.
If the bone-bridge is small, involving under
10% of the overall surface of the growth plate,
it may break spontaneously with no adverse
effect on the length of the lower limb or its
alignment(20).
When the bone-bridge is larger, the bone
stops growing, and this leads to a shortening
of the limb, or misalignment if it grows
asymmetrically.
When a bone-bridge develops at the edge of
the growth plate it is relatively easy to treat but
all the authors stress the difficulties involved in
removing a centrally or paracentrally positioned
bone-bridge(23,30).
The most commonly used procedure for
resecting a bone-bridge is performed via
transmetaphyseal approach, thus affording access
to the lesion which can then be resected and
replaced by an interposition material(14,31,37) such
as methylmethacrylate(22,30,42), silicone(2,3), wax, or
cartilage(27), or fatty tissue(24-26,35,36,43).
At the same time, many authors have
described the use of an epiphysiolysis
procedures to lengthen limbs; breaking
the epiphysiodesis bone-bridges by
applying progressive distraction has also
been described(4,6,8,16). Since 1988, we have
238
developed an original desepiphysiodesis
procedure(1) based on epiphyseal distraction
using an Ilizarov fixation system to induce
a Salter type 1 fracture. This affords direct
exposure of the epiphysiodesis bone-bridge
which is separated and pulled away from
the epiphysis. It is then easily resected and
replaced by a methylmetacrylate (Fig. 1). The
angular defect caused by the epiphysiodesis
bone-bridge can then be corrected at the site
of epiphysiolysis.
This operation has been adopted as a
standard procedure in our hospital since 1985.
During this period, some experimental
research work has been carried out to ascertain
the force which should be applied to induce the
rupture of the epiphysiodesis bone-bridge(7),
study the likelihood of spontaneous regeneration
of the growth plate or replace it with a growth
plate cartilage graft(12,18).
This chapter sums up the result of our clinical
and experimental work.
TECHNICAL ASPECTS OF
DISTRACTIONAL DISEPIPHYSIODESIS
This procedure concerns central or
paracentral epiphysiodesis bone-bridges(3).
It is indicated when an epiphysiodesis
bone-bridge is located centrally or
paracentrally and appears to be irreversible,
 Surgical correction of partial growth plate closure using physeal distraction
inducing a shortening and/or misalignment of
the limb(10). The site of the bone-bridge should
be determined on the base of the radiography
data, MRI, bone-scan (5,17). Although it is
difficult to determine the exact size of the
bone-bridge in proportion to the overall
surface of the growth plate, we propose this
procedure in cases in which the epiphysiodesis
bone-bridge leaves 50% of the growth plate
intact and operational(32).
The operation should be performed in
two stages (Fig. 2):
The first stage of the operation: the aim is
to detach the affected epiphysis by applying
transphyseal distraction using an Ilizarov
type external fixation device. Under general
anaesthetic, two 1,5 mm. pins should be
anchored under radioscopic control into the
epiphysis; two more pins are then placed in
Figure 1. Schematic diagram of
the procedure: A) bone bridge
of the distal tibia; B) during the
epiphysiolysis stage; C) after
surgical removal of the bony
bar; D) after insertion of the
plug.
the metaphysis. Rings are then positioned
and connected to 3 threaded rods. During
this stage of the operation, the growth plate
is not directly approached.
In the postoperative period, distraction
is applied to the threaded rods at a rate of
1 mm per day (Twice 0.5 mm. during one
day). Within a period ranging from 5 to 15
days, the epiphysis breaks away. The child
will suddenly feel a sharp pain due to the
mechanical strain, which can easily controlled
with pain-killers.
An x-ray should then be performed to
check that the bone-bridge has indeed ruptured
and separated from the body of the epiphysis.
The distraction which has been interrupted
for 24 hours should then be resumed for 3
to 5 days in order to obtain a large enough
gap between the epiphysis and metaphysis.
239
G. Bollini, J.L. Jouve, J. Cottalorda, P. Frayssinet, J.M. Guillaume, J.C. Godchaux
The second stage of the operation is
indicated at the end of the distraction
period. This stage is performed under
general anaesthesia, using a pneumatic
tourniquet. The Ilizarov external fixation
device is removed. Surgical approach should
be chosen according to anatomical criteria,
especially the position of the epiphysiodesis
bone-bridge. In order to avoid damaging the
perichondral ring, the periosteum should
be incised on the metaphysis and carefully
pushed downwards to afford direct access
to the epiphysiolysis focus. The bone-bridge
is then easy to locate, it is generally attached
to the metaphysis. The growth plate which
is still intact is attached to the epiphysis.
The bony bridge should be resected
with small instruments and a cavity should
be hollowed out in the metaphysis and
epiphysis to house a methylmetacrylate
240
Figure 2. Technical aspect: A)
Epiphysiolysis using an Ilizarov
fixator; B) resection of the bone
bar after dissection of the
periosteal flap; C) shaping the
epiphysis to prepare the space
to house the plug; D) insertion
of the plug.
plug. This stage of the operation should
be carried out with extreme care around
the epiphysis in order to avoid damaging
the intact growth plate, which is perfectly
visible. The plug is shaped according to
the size of the resected area. Once the
methylmetacrylate is heated, the plug should
be inserted to fill the void where the bone-
bridge has been removed. In our most recent
cases, we have anchored the plug and kept
it in place using a transepiphyseal pin to
avoid it migrating when the growing process
resumes. The metaphyseal periosteal flap is
then replaced in its original position. The
operation is finished by placing the limb in
a plaster, correcting any axial deviation in
the epiphysiolysis focus. The plaster should
be left on for 2 months. From the first month
after surgery onwards partial weight bearing
with crutches is allowed.
 Surgical correction of partial growth plate closure using physeal distraction

A B C

Figure 3. Multiple epiphysiodesis caused by neonatal septicemiae.

A) Aspect at 3 years old: a desepiphysiodeseis of the distal left
femur growth plate is scheduled. B) X Ray of the epiphysiolysis.
C) Post operative aspect after the second stage procedure with
insertion of the interposiotional material. D) Result at 3 years
D follow-up.

CLINICAL STUDY The seat of the lesion was lower femoral,

During the period between 1985 and 1993, at
the Timone Children’s Hospital we performed
12 desepiphysiodeses with distraction in 10
children, 3 boys and 7 girls. The aetiology was
consecutive to a traumatic injury in 8 cases (Fig.
4) and secondary to infection in 4 cases (Fig. 3).
The infectious aetiologies were the result of
neonatal septicaemia with purpura fulminans
in two patients.
6 cases, upper tibial, 3 cases, lower tibial, 3
cases.
The age at which the epiphysiodesis bone-
bridge had developed ranged from the neonatal
period in the cases of neonatal septicaemia to 11
years 10 months with a mean age of 5 years.
The age at desepiphysiodesis ranged from
3 years and 2 months to 13 years and 2 months,
with a mean age of 7 years and 3 months.

241
G. Bollini, J.L. Jouve, J. Cottalorda, P. Frayssinet, J.M. Guillaume, J.C. Godchaux
A B
Figure 4. A) Post traumatic epiphysiodesis in a 12 years old girl. B) Operative view after insertion of the
interpositional plug. C) Radiologic aspect at 5 years follow-up.
The period between the first stage of the
operation when the external fixation device was
positioned and rupture of the epiphysiodesis
bone-bridge ranged from 5 to 20 days, with a
mean value of 8.5 days for 11 patients. In one
case of infectious origin, the epiphysiodesis
bone-bridge which extend from the center to
the edge of the growth plate did not rupture
with distraction alone and the bone-bridge had
to be surgically weakened by osteotomy via
metaphyseal approach.
The distraction did not in any case induce an
epiphyseal lesion. The interpositional material we
used was in all cases methylmetacrylate.
We had no problems due to infectious
complications, nor vascular or nerve lesions
resulting from distraction or from the pins.
A distinction can be made between the
results according to the cause of the initial
lesion.
Bone growth resumed in 6 cases in the
group of patients with epiphysiodeses induced
by traumatic injury (8 cases). The epiphyseal
angle was corrected for 4, in two further cases,
the angle improved.
242
C
The amount of length discrepancy remained
unchanged in two patients at follow up while
it improved in four patients probably due to
growth stimulation of the opposite growth plate
of the shaft.
The two remaining cases were patients for
whom the desepiphysiodesis was performed,
but growth did not effectively resume. For the
record, these patients were aged respectively
11 years and 7 months and 12 years when
operated.
In the 4 cases of epiphysiodesis resulting
from infection, our results were rather more
variable. The patients all resumed their growth,
however their subsequent development was
much more irregular, both in terms of the
correction of the angle and of the length of
the limb.
EXPERIMENTAL STUDY
Epiphyseal distraction and centrally
located bone bar
We performed an experimental study
in rabbits(21,39), to ascertain the relationship
 Surgical correction of partial growth plate closure using physeal distraction
between the elongation force required to
achieve epiphysiolysis and the size of the
epiphysiodesis bone-bridge. Epiphysiodesis
bone-bridges were created in the epiphyses of
the lower femur of rabbits by endo-articular
approach to avoid damaging the perichondral
ring. The growth plate was drilled with drill
bits of increasing calibre, 2.5, 3.5 and 4.5
mm in diameter. These orifices were equal
respectively to 3.1%, 7.8%, 15.2% and 25.1%
of the overall surface of the growth plate. The
rabbits were operated at the age of 9 weeks
and sacrificed 3 weeks later.
A clinical, radiological and biomechanical
study was carried out. The biomechanical
study consisted of using 2 mm epiphyseal
and metaphyseal pins and applying constant
distraction at a rate of 20 mm per minute until
epiphysiolysis was achieved. Epiphysiolysis
is defined as the separation of the femoral
epiphysis from the adjacent metaphysis. The
force required to achieve the epiphysiolysis
and the percentage of elongation was recorded
on a computer.
On the contrary to our forecasts, analysis
of the results demonstrated that the mean
force required to achieve epiphysiolysis did
not significantly differ from one group of
rabbits to another, suggesting that the presence
of bone-bridges did not change the growth
plate’s resistance to elongation.
However, for the record, small sized bone-
bridges, equal to 3.1% and 7.8% of the surface
of the growth plate, broke away from the
epiphysis in a Salter-Harris type II fracture.
Sometimes in the same group the force
required to achieve epiphysiolysis differed
for animals of the same size. Rudicel also
recorded the same features in rabbits of the
same age(39).
Several publications have already
mentioned the possibility of breaking an
epiphysiodesis bone-bridge by using an
external fixation device.
In these articles, the distraction stage was
longer and extended over several days. It is
thus difficult to draw a comparison between
our experimental work and these studies.
Growth plate behaviour after
desepiphysiodesis and various modes of
fixation with interpositional materials
In the course of an experimental study,
we sought to ascertain how the growth plate
developed after desepiphysiodesis with an
interpositional plug held in position with
pins either in the metaphysis or the epiphysis
We used a 3 week old rabbit as an
experimental animal. A defect was created
in the centre of the growth plate via endo-
articular approach. Three groups were studied.
The first group (A) was used as a
control group, the central orifice, 4.5 mm in
diameter was not filled. Group B was made
up of a series of rabbits who received a 4.5
mm diameter silicone cylinder to plug the
created orifice. A pin was used to fix the
filling material to the metaphysis. Group C
was identical, except that the silicone cylinder
was fixed to the epiphysis with a pin. The
rabbits were sacrificed two months after
the operation. The femurs were removed,
measured clinically, x-rayed and a histological
analysis was performed.
Clinically we observed a shortening of
the operated femur in comparison to the
contralateral femur : 13.3% in group A, 5%
in group B, 1.7% in group C (Fig. 5).
The x-ray examination confirmed that
a central epiphysiodesis bone-bridge had
developed in group A, all the rabbits in group
B presented x-rays showing that the plastic
tube had risen into the metaphysis, the rabbits
in group C kept their plastic tube fixed in the
epiphysis, where it stayed interposed at the
level of the growth plate.
The histological analysis showed
that an epiphysiodesis bone-bridge had
formed for all animals in group A. In group
B the plastic tube had migrated into the
243
G. Bollini, J.L. Jouve, J. Cottalorda, P. Frayssinet, J.M. Guillaume, J.C. Godchaux

Figure 5. Various modes of fixation of interpositional material in rabbits.

- Two femurs on the left:
control femur and plug fixed to the metaphysis: mean shortening: 5%
- Two femurs on the right:
control femur and plug fixed to the epiphysis:
mean shortening: 1,7%

metaphysis, and opposite the defect in the
growth plate a bridge made up of a mixture
of fibrous, cartilaginous and sometimes
bony structures had grown. There was no
sign of regeneration of the growth plate.
In group C, the growth plate remained in
contact with the plastic tube and this group
obtained the best results. In some cases we
also recorded changes in the growth plate
at a distance from the central defect where
it had a degenerative aspect and showed a
decrease in the layer of column cells. These
modifications seem to occur sporadically,
whatever the group studied.
We drew two conclusions from this study: on
one hand when the inert interposition material
rose, no regeneration of the growth cartilage
occurred, and secondly a fibro-cartilaginous
bridge developed and although this bridge did
not have the mechanical strength of a bone-
bridge, it may be an obstacle hindering normal
growth.
Reimplantation of growth plate
chondrocyte cultures into central growth
plate defects
Autologous transplantation of growth
plate has not yet yielded satisfactory
results when used in indications for desepi-
physiodesis(9).
Chondrocyte culture is currently a procedure
that is commonly used and has been described
by many authors(11,13,15,19,29,34,38,40,41).
In order to achieve true regeneration of the
growth plate, we have perfected an original
growth plate culture procedure(18).

244
 Surgical correction of partial growth plate closure using physeal distraction
In the first stage, we defined the cell culture
parameters in order to optimise the in vitro
technique and obtain a sufficient quantity of
mature, functionally abundant chondrocytes.
The preparation of the chondrocytes
and their extra-cellular matrix was studied,
with different enzyme digestion protocols. A
treatment with trypsine (0.2%) for 30 minutes
at 37°, then collagenase (200 units per ml) for
6 hours was the method we chose. Subject to
these conditions, 40 ± 16.106 chondrocytes
per gram of growth plate was obtained, with
a cell viability rate of 79 ± 12%. The seeding
density, the nature of the substrate and the
culture medium were determined to optimise
cell growth.
The best yield was obtained when the
cells were seeded at a rate of 20,000 to 30,000
chondrocytes per cm2 on a type 1 collagen
substrate and a HAMP-12 culture medium,
non-supplemented with glucose or growth
factor.
After 7 days in culture, the optimum yield
was obtained (Fig. 6). An implantation bed was
used to implant the cell culture in vitro. Several
beds were tested and the best was AGAR which
yielded viable, functional chondrocytes 21 days
after implantation.
Inanexperimentalstudyinvivo,weimplanted
this culture and the culture bed on large
resected areas on the iliac ala in rabbits in order
to observe whether any enchondral ossification
would occur. The results were disappointing
because the cultured chondrocytes rapidly
disappeared. A new experiment was therefore
carried out. The culture was implanted in a
central growth plate defect created by endo-
articular approach.
This culture and its AGAR bed were held in
position by a proximal silicone plug and a wax
plug on the trochlea. The rabbits were sacrificed
6 weeks after the graft. Clinical, radiological
and histological studies were performed.
The clinical results were disappointing. The
graft did not stop the epiphysiodesis bone-
Figure 6. Aspect of chondrocytes at 7 days of culture
in vitro.
bridge from developing; the bone-bridge was
recorded in all the experimental animals.
However, the histological examination
consistently showed that cartilaginous islands
made up of functional chondrocytes were
present in the AGAR; these chondrocytes
were building up a cartilaginous matrix and
becoming organised into columns of mature
chondrocytes.
However, the islands were developing
irregularly and were not becoming organised
in a linear pattern and linking up with the intact
growth plate cartilage (Fig. 7).
We are currently studying a similar culture
based on ovine growth plate chondrocytes.
The cell lines obtained are fixed on a ceramic
base, which affords a strong tridimensional
support.
We now regularly obtain an efficient culture
on hydroxyapatite beds in vitro. Experimentation
is under way to implant these cultures in vivo.
DISCUSSION
The desepiphysiodesis procedure,
associating epiphysiolysis by distraction and
interposition of methylmetacrylate presents
two main advantages:
- Once the epiphysiolysis is achieved, it
affords a good view and direct surgical approach
to the bone-bridge, thus allowing precise,
245
G. Bollini, J.L. Jouve, J. Cottalorda, P. Frayssinet, J.M. Guillaume, J.C. Godchaux
Figure 7. Aspect of graft culture 6 weeks after
grafting. Layers of chondrocytes synthesising
abundant matrix and first signs of column
organisation can be clearly identified.
limited resection around the diseased area.
In epiphysiodeses resulting from infection or
vascular conditions, it also provides information
on the fibrous portion of some epiphysiodesis
bone-bridges which are not clearly visible on
the x-rays.
- It also provides a means of correcting an
axial deviation due to asymmetric growth of
the unharmed growth plate. The correction can
be achieved in the epiphysiolysis focus, after
inserting the interposition material. A plaster
can be used to immobilise the limb and keep it
in the correct anatomic position.
Progressive epiphyseal distraction, using an
Ilizarov external fixation device, permitted us in
11 cases out of 12 to achieve epiphysiolysis within
a period ranging from 5 to 20 days.
246
In one case we were not able to achieve
the rupture point. This case concerned a
paracentral and peripheral epiphysiodesis which
required surgical treatment with osteotomy
via metaphyseal approach in order to achieve
extemporaneous epiphysiolysis.
For the record, we have never had any
epiphyseal lesion caused by the distraction
applied to the pins. The Ilizarov external fixation
device seems to provide a good solution which
affords satisfactory distribution of the stress
on the whole of the epiphysis and makes this
operation feasible, even for children with small
sized epiphyses.
During our experimental work on rabbits,
the progressive distraction of the lower femoral
epiphysis in one single stage did not cause the
pins to section the epiphysis, except if the pins
were poorly positioned. It thus appears to us
important to position the epiphyseal portion
of the pins under radioscopic control to ensure
that they are properly placed in the centre of
the epiphysis so that they are supported by the
bony part of the epiphysis and not only by the
cartilage.
We did not find any direct relationship
between the size of the epiphysiodesis bone-
bridge and the amount of force required to
achieve epiphysiolysis in bone-bridges which
were equal to 3 to 25% of the overall growth
plate.
For larger size bone-bridges, Salter II type
epiphyseal fractures were obtained, whereas
for smaller bone-bridges, the fractures were
classified Salter I.
This has led us to performing the operation in
two surgical stages with progressive distraction
over a period of several days rather than
attempting to achieve epiphyseal separation
extemporaneously.
The main drawback in this method is the risk
of premature closure of the growth plate after
epiphysiolysis as described in bone lengthening
by epiphysiolysis(4,6,8,16).
It was difficult in our clinical study to
 Surgical correction of partial growth plate closure using physeal distraction
determine the real influence of this factor
on the patients we operated. As yet only 3
of them have achieved their final growth
status; it is also difficult to assess the real
influence of epiphysiolysis on this premature
closure if the growth cartilage has already
been subjected to prior traumatic injury. One
feature seemed important in terms of quality
when growth was resumed ; this was the
development of an epiphysiodesis bridge
after the methylacrylate plug had to a certain
extent risen into the metaphysis.
The experimental work that we carried out
on rabbits, plugging a defect that was equal to
25% of the growth plate with a silicone tube,
demonstrated that once a tube had migrated
into the metaphysis, no regeneration of the
growth plate was obtained. This correlates with
the clinical and radiological measurements
in this experiment, which show a significant
difference in the quality of the bone which
grows back when the interposition material
remains fixed to the epiphysis, in comparison
with the series in which the material was fixed
to the metaphysis.
Currently speaking, in the light of our
experimental work, it seems preferable to us
to anchor our interposition material to the
epiphysis using a trans-epiphyseal pin in
order to avoid the epiphysiodesis recurring.
The absence of regeneration of the growth
cartilage is contradictory to Österman’s
findings(35). This is perhaps due to the fact that
the growth plate defect created in our study was
mainly centrally located, and did not involve
the perichondral groove, nor the periosteum,
and lastly the interposition material left the
cartilage area suddenly when it rose, whereas
the interposition of graft material as described by
Österman is resorbed slowly and progressively.
It is obvious that the ideal interposition
material for desepiphysiodesis should be
made of growth cartilage. This is why we
have developed an in vitro culture of growth
cartilage with the aim of using it secondarily in
vitro. The culture procedure is now satisfactory
and reproducible in vivo. However, when
we interpose it in a growth plate defect, we
do not obtain a well organised structure that
builds up and extends the remaining growth
cartilage. The main obstacle seems to be
stabilising the culture adjacent to the remaining
growth plate. This is our current objective in
developing strong ceramic bases, colonised
in vitro by growth plate chondrocytes, that
can be anchored in the correct position beside
the remaining growth plate in an attempt to
induce effective bone growth. However, in
the short term, the clinical application for this
research pathway still seems very remote.
Many problems still have to be solved in this
area. Cell anomalies arise after several culture
cycles, especially nuclear anomalies in the
morphology and the number of chromosomes
in the cultured chondrocytes and a lot more
in-depth work remains to be done in this area.
REFERENCES
1. Bollini G., Tallet J.M., Jacquemier M., Bouyala
J.M. New procedure to remove a centrally located
bone bar. J. Pediatr. Orthop. 1990;10:662-666.
2. Bright R.W. Operative correction of partial
epiphyseal plate closure by osseous-bridge
resection and silicon-rubber implant: an
experimental study in dogs. J. Bone Joint Surg.
(Am), 1974;56:655-64.
3. Bright R.W. Partial growth arrest: identification,
classification and results of treatment. Orthop.
Trans., 1982;6:65-6.
4. Canadell J., De Pablos J. Breaking bony bridges
by physeal distraction. Int. Orthop., 1985;9:223-9.
5. Carlson W.O., Wenger D.R. A mapping method
to prepare of surgical excision of a partial physeal
arrest. J. Pediatr. Orthop., 1984;4:232-8.
6. Connolly J.F., Huurman W.W., Lippiello L., Pankaj
R. Epiphyseal traction to correct acquired growth
deformities. Clin. Orthop., 1986;202:258-68.
247
G. Bollini, J.L. Jouve, J. Cottalorda, P. Frayssinet, J.M. Guillaume, J.C. Godchaux
7. Cottalorda J., Jouve J.L., Bollini G., Panuel M.,
Guisiano B., Jimeno M.T. Epiphyseal distraction
and centrally located bone bar: An experimental
study in the rabbit. J. Pediatr. Orthop., 1996;16:664-
668.
8. De Bastiani G., Aldegheri R., Brivio L.R., Trivella
G. Chondrodiatasis-controlled symmetrical
distraction of the epiphyseal plate. J. Bone Joint
Surg., (Br), 1986;68:550-6.
9. Eulert J. Transplantation du cartilage de la crête
iliaque après désépiphysiodèse. Rev. Chir. Orthop.,
1979;65:65-75.
10. Ford L.T., Key J.A. A study of experimental trauma
to the distal femoral epiphysis in rabbits. J. Bone
Joint Surg., (Am), 1956;38:84-92.
11. Foster B.K., Hansen A.L, Gibson G.J, Hopwood
J.J, Binns G.F, Wiebkin O.W. “Reimplantation
of growth plate chondrocytes into growth plate
defects in sheep”. Mapfre Medicina. 1993;4 (supl
II):110-117.
12. Frayssinet P., Jouve J.L., Asimus E., Mathon D.,
Autefage A. Isolation, culture, and immobilisation
of sheep growth plate chondrocytes. Cell biology
and toxicology 1996;12(4-6):388.
13. Gibson G.J., Schor S.L., and Grant, M.E. Effects
of matrix macromolecules on chondrocyte gene
expression: Synthesis of a low molecular weight
collagen species by cells cultured within collagen
gels. J. Cell Biol. 1982;93:767.
14. Giner V.B., Sanz V.O. Experimental prevention
of the formation of physeal bone bridges by
interposition of different substances. Mapfre
Medicina, 1993;4 supl II:87-91.
15. Hansen A., Foster K., Gibson G., Binns G., Wiekin
O., and Hopwood J. “Growth-plate chondrocyte
cultures for reimplantation into growth-plate
defects in sheep”. Clin. Orthop. 1990;256:286-298.
16. Houghton G.R., Duriez J. Allongement tibial
par élongation du cartilage de croissance tibial
supérieur. Etude expérimentale chez le lapin.
Rev. Chir. Orthop., 1980;66:351-6.
17. Jaramillo D., Laor T., Zaleske D.J. Indirect trauma
248
to the growth plate: results of MRI after epiphyseal
and metaphyseal injury in rabbits. Radiology,
1993;187:171-178.
18. Jouve J.L. Culture in vitro de cartilage de croissance
et reimplantation in situ. Chirurgie , 1996;121:273-
279.
19. Kawabe N., Yoshinao. “ The repair of full-
thickness articular cartilage defects”. Clin. Orthop.
1991;268:279-293.
20. Kershaw C.J., Kenwright J. Epiphyseal distraction
for bony bridges: a biomechanical and morphologic
study. J. Pediatr. Orthop., 1993;13:46-50.
21. Khermosh O., Tadmor A., Weissman S.L., Michels
C.H., Chen R. Growth of the femur in the rabbit.
Am. J. Vet. Rest., 1972;33:1079-1082.
22. Klassen R.A., Peterson H.A. Excision of physeal
bars. The Mayo Clinic Experience 1968-1978.
Orthop. Trans., 1982;6:65.
23. Kohler R., Comtet J.J., Chappuis J.P., Daudet
M. Traitement des lésions du cartilage de
croissance par désépiphysiodèse. Lyon Chirurgical,
1980;76:254-257.
24. Langenskiöld A. The possibilities of eliminating
premature partial closure of an epiphyseal plate
caused by trauma or disease. Acta Orthop. Scand.
1967;38:267-279.
25. Langenskiöld A., Videman T., Nevalainen T. The
fate of fat transplants in operations for partial
closure of the growth plate. Clinical examples and
an experimental study. J. Bone J. Surg. 1986;68B:234-
238.
26. Langenskiöld A., Österman K., Valle M. Growth
of fat grafts after operation for partial bone growth
arrest: demonstration by computed tomography
scanning. J. Pediatr. Orthop. 1987;7:389-394.
27. Lennox D.W., Glodner R.D., Sussman R.D. Cartilage
as an interposition material to prevent transphyseal
bone bridge formation: an experimental model.
J. Pediatr. Orthop. 1983;7:389-394.
28. Makela E.A., Vainionpaa S., Vihtonen K., Mero
M., Rokkanen P. The effect of trauma ot the lower
 Surgical correction of partial growth plate closure using physeal distraction
femoral epiphyseal plate. An experimental study
in rabbits. J. Bone Joint Surg. (Br), 1988;70:187-91.
29. Malejczyk J., Moskalewski S. Effect of immuno-
suppression on survival and growth of cartilage
produced by transplanted allogenic epiphyseal
chondrocytes. Clin. Orthop. 1988;232:292-303.
30. Mallet J., Rey J.C. Traitement des épiphysiodèses
partielles traumatiques chez l’enfant par
désepiphysiodèse. Int. Orthopaedics. 1978;1:309-
315.
31. Martiana K., Kwang Low C., Kia An S., Wen YI
Pang M. Comparison of various interpositional
materials in the prevention of transphyseal bone
bridge formation. Clin. Orthop., 1996;325:218-224.
32. Moen C.T., Pelker R.R. Biomechanical and
histological correlations in growth plate failure.
J. Pediatr. Orthop., 1984;4:180-4.
33. Monticelli G., Spinelli R. Distraction epiphysiolysis
as a method of limb lengthening. Clin. Orthop.,
1981;154:274-85.
34. O’Keepe R., Puzas J.E., Brand J.S., Rosier R.N.
“Effect of transforming growth factor B on
DNA synthesis by growth plate chondrocytes:
modulation by factors present in serum”. Calcif.
Tissue. Int. 1988;43:352-358.
35. Österman K. Healing of large surgical defects of
the epiphysial plate. Clin. Orthop., 1994;300:264-
268.
36. Österman K. Operative elimination of partial
premature epiphysial closure: An experimental
study. Acta Orthop. Scand. 1972;(Suppl. 147):1.
37. Peterson H.A. Partial growth plate arrest and its
treatment. J. Pediatr. Orthop., 1984;4:246-58.
38. Robinson D., Halperin N., Nevo Z. Regenerating
hyaline cartilage in articular defets of old chickens
using implants of embryonal chick chondrocytes
embedded in a new natural delivery substance.
Calcif. Tissue Int. 1990;46:246-253.
39. Rudicel S., Pelker R.R., Lee K.E., Ogden J.A.,
Panjabi M.M. Shear fractures through the capital
femoral physis of the skeletally immature rabbit.
J. Pediatr. Orthop., 1985;5:27-31.
40. Shimomura Y., Yoneda T., Suzuki F. “Osteogenesis
by chondrocytes form growth cartilage of rat rib”.
Calcif. Tiss. Res. 1975;19:179-187.
41. Trippel S, Boston M.D, Wroblemski P.D, Makover
P.D, Whelan B.S., Schoenfeld D., Doctrow S.
“Regulation of growth-plate chondrocytes by
insulin-like growth-factor I and basic fibroblast
growth-factor”. J. Bone Joint. Surg. 1993;75A:177-189.
42. Vickers D.W. Premature incomplete fusion of the
growth plate: cause and treatment by resection
(physiolysis) in fifteen cases. Austr and New Zealand
J. of Surgery. 1980;50:393-401.
43. Visser J.D., Nielsen H.K.L. Operative correction
of abnormal central epiphyseal closure by
transmetaphyseal bone-bridge resection and
implantation of fat. Neth J. Surg., 1981;33:140-5.
249
29
Bone lengthening by physeal distraction
J. de Pablos

This technique, likewise called epiphyseal

distraction, resulted from the search to find the
safest and least invasive way of performing
bone lengthening. Among the bone lengthening
methods it is clear that physeal distraction is
surely the least invasive. However a series of
inherent drawbacks which will be pointed
out, made this technique less popular than
what would have been expected.
Physeal distraction uses the physis (growth
plate) as a “locus minoris resistentiae” of the
bone through which a metaphyseal-epiphyseal
separation (bone lengthening) can be obtained
when distractional forces are applied to its sides
(Fig. 1). It is a technique which does not need
Figure 1. Femoral lengthening by means of physeal
the performance of any osteotomy or osteoclasis
distraction.
(“bloodless”)(12) unlike the previously mentioned
techniques (Fig. 2).
The first experiment based on these ideas To perform this technique, any apparatus
was published by Ring in 1958(23), who performed can be used, provided that it allows distraction
physeal distraction by means of external tensors in a sufficiently stable manner and that
in dog femurs. Other authors followed with distraction can be applied in the epiphysis
experimental studies, years later, in an attempt to and in the diaphysis of the bone to be
solve the multiple doubts which arose concerning lengthened. For physeal distraction as well as
this technique(3,4,8-16,18,21,24,25). for lengthening by percutaneous osteotomy, we
It was in Russia, however, where this use Wagner’s apparatus modified by Cañadell,
technique began to be applied clinically and which we find to be stable and versatile (Fig.
satisfactory results were published by Zavijalov 3). The major difference between the Wagner
and Plaskin(27,28) in 1967 and 1968 and Ilizarov type monolateral fixator-distractor and the
in 1969(12). Later, other authors(1,2,6,7,17,19,20,22,26), circular devices of the Ilizarov type with respect
mostly European also, have continued with to physeal distraction, lies in the fact that the
the clinical use of this technique. former can work rigidly while the latter can

250 Partly reprinted with permission of Mapfre Medicina (vol. 4, suppl 2)


Figure 2. Physeal distraction applied to the proximal end of the tibia. Note the space between epiphysis
and metaphysis produced at the level of the physis. Left: 20 days postop, Center: 45 days postop. End
of distraction; Right: 100 days postop. The area of distraction is completely occupied by newly formed
bone. No graft was needed.
Figure 3. Modified Wagner apparatus showing
the “T” piece for physeal distraction.
do so only elastically. Thus, the initial physeal
fracture which is always produced in physeal
distraction can be obtained in a more controlled
manner by means of a monolateral distractor
(i.e., the modified Wagner apparatus), whereas
Bone lengthening by physeal distraction
with the elastic circular distractors the fracture
will unavoidably be produced in a brusque
manner. This latter situation has two far-
reaching consequences: firstly, the brusqueness
of the fracture can, in our opinion, lead to
permanent physeal injuries(5), and secondly,
it produces an intense pain felt by the child
when the fracture is produced a few days
after the beginning of distraction. Other than
this, there are no other significant differences
between either type of fixator-distractors with
respect to the rest of the distraction process
and the neutralization stage until consolidation
is obtained.
This technique has a series of advantages
as compared to other techniques commented
on in this chapter.
- Simple and rapid application.
- Can be performed in a single surgical
session.
- No need for surgical incision of the skin,
periostium or bone.
- Great ease in consolidation, with no need for
further complementary surgery, (i.e. bone
grafting or internal fixation).
251
J. de Pablos
- No noticeable cosmetic sequels due to skin
scars.
- In physeal distraction of the distal femur,
the distractional forces are applied distally
to the insertion of the adductor muscles,thus
minimizing the tension of these muscles
during lengthening. This, minimizes the
tendency to go into varus deformity, tipical
in diaphyseal femoral lengthenings, and
also reduces pressure in the hip joint.
Nevertheless, the following drawbacks can
be said to derive from this technique:
- Stiffness in the knee and ankle joints has
been observed on conclusion of treatment,
when distraction was applied at the femoral
distal physis and distal tibial physis,
respectively. This stiffness, mainly in
children under 10-12 years of age, usually
disappears with prompt and adequate
physical therapy, once the apparatus has
been removed.
- The risk of producing septic arthritis due
to the vicinity of the epiphyseal screws and
pins to the joint. This is particularly risky
in femoral distal physeal distraction in so
far as the epiphyseal screws are clearly
intra-articular. When such a technique is
indicated, daily and meticulous hygienic
care of the pin-tract wounds is extremely
important.
- Finally, the viability of the growth
cartilage subjected to distraction bears
further comment. Obviously, in the
case of permanent damage to the physis
(premature closure), the repercussions
would not only be functional (growth
arrest) but would also involve the
impossibility of repeating physeal
distraction later on, if necessary.
INDICATIONS FOR PHYSEAL
DISTRACTION
Although the advantages of physeal
distraction over other lengthening methods
252
are clear the potential risks that is poses, mainly
septic arthritis, made us to be very careful
when we indicate physeal distraction in a
particular patient.
Simple leg lengthening
For this purpose we indicate physeal
distraction only in immature patients in whom
consolidation is particularly difficult. To this
respect, physeal distraction is particularly
useful in cases of important congenital
shortening of femur and/or tibia. Also the
tendency to varus deformity during femoral
lengthening, which is very high in this type
of patients, is minimized when using physeal
distraction.
Also we recommend physeal distraction of
the distal femur in cases of femoral shortening
with an associated hip disorder, because with
this technique the stress on the hip joint is
also minimized.
Correction of angular deformities (Fig. 4).
When the deformity of a long bone in an
immature patient is located in the vicinity
of the growth plate we recommend physeal
distraction as the treatment of choice given
the advantages we find in this method over
other techniques:
- The operation itself is not extensive and
does not invade the site of correction.
Osteotomy is not needed.
- It acts directly on the cause of the deformity,
- There is no need for internal fixation nor
bone grafts.
- It is possible to obtain bone lengthening if
necessary simultaneously with the angular
correction.
- Adjustment of the angular correction and/
or lengthening during treatment is also
possible.
COMPLICATIONS OF PHYSEAL
DISTRACTION
Apart from the complications which may
arise with physeal distraction which are
 Bone lengthening by physeal distraction

Figure 4. Adolescent Blount’s

disease in a 14 year-old
boy.
A) Preop. roentgenogram.
B) X-rays series showing
progressive correction of
the tibial varus by means
of physeal distraction.
C) Preoperative clinical
appearance.
D) 6 month postoperative
clinical picture. Acceptable
cosmetic appearance. C D

common to all bone lengthening methods,
there are other specific hazards involved in
its use, these being the subject of this section.
These potential complications may be divided
into two broad groups:
-Those deriving from the physeal fracture.
-Those deriving from the epiphyseal location
of screws or wires of the distraction apparatus.
A) Complications deriving from the
physeal fracture
Although there is still controversy as to
whether bone lengthening may or may not
be achieved by physeal distraction without
physeal fracture (epiphysiolysis), the great
majority of authors are of the opinion that
the beginning of the lengthening by physeal
distraction is accompanied by an epiphyseal-
metaphyseal fracture-separation. This fact
entails two potential risks or complications;
one of these is immediate -the pain produced
by the fracture- and the other, arising in the
medium-to-long term is the premature closing
of the physis subjected to distraction.
With respect to the pain felt when the
physeal fracture occurs, one fact is noteworthy:
this pain is associated consistently with the
use of circular elastic fixator-distractors,
whereas it arises much less frequently when
a rigid monolateral apparatus is used. This

253
J. de Pablos

A B
Figure 5. Intraoperative images taken at a knee arthroscopy of a 10 year-old boy. A) A needle was placed
where the epiphyseal pins are supposed to be inserted in a physeal distraction of the distal femur.
B) Picture taken simultaneously through the arthroscope showing how the needle enters the joint in its
way to the epiphysis. The same would occur with an external fixation pin placed in the distal femoral
epiphysis as required for physeal distraction.

is logical, since in the case of rigid devices
(e.g. the modified Wagner type) the fracture
may be controlled and performed gradually,
whereas with circular devices, on account of
their elasticity, the tension rises gradually
until a threshold is reached, beyond which
the physeal fracture suddenly occurs. This
usually happens 3 to 7 days after beginning
the distraction, and reveals itself clinically
as a sharp pain that requires treatment with
analgesics for several days(19). For our part,
when using rigid fixator-distractors, we have
virtually never noted any pain of this type
being experienced by the patient during
physeal distraction.
With respect to the potential premature
closing of the physis subjected to distraction,
we shall concentrate on two specific issues:
• How important is this premature physeal
closure following physeal distraction?
• Can lengthening by physeal distraction
be performed without physeal damage in the
medium-to-long term?
The premature closure of a healthy physis
can lead to a significant growth deficiency when
the patient reaches skeletal maturity. However,
it is important to remember that most growth
cartilages to which physeal distraction is applied
show some prior defective function. This means
that we can nearly always achieve more growth
in these cartilages through physeal distraction
than can be achieved through natural growth,
and we therefore believe that the closure is of
only relative importance.
With respect to the second point, there
are several experimental papers showing
that, in animals, physeal distraction may
be achieved with minimal future physeal
damage(3,4). The most significant factors having
a bearing on this would seem to be the speed
of the distraction and the suddenness with
which the physeal fracture occurs. However,
in our clinical experience, perhaps owing to
the differences between animal and human
physeal behaviour, we have not obtained the
same results. Even under the best conditions,
i.e. slow distraction (0.5 mm/day) and
controlled fracture (which can only be achieved
with rigid distractors), premature physeal
closure is unpredictable. What would appear
to be certain is that distraction speeds of 1-1.5
mm/day or faster lead to permanent physeal

254

Figure 6. Distal tibia epiphyseal fracture during
physeal distraction due to incorrect pin placement
(the epiphysis is not completely pierced). Left:
immediately postop. Center: After ten days of
distraction an epiphyseal fracture appears on
X-rays. Right: 30 days postop after returning to the
starting position, completely piercing the epiphysis
and restarting distraction.
damage. Another factor which, in our clinical
experience, would seem to have a bearing on
physeal viability after distraction is the prior
damage to this structure, i.e. the greater the
prior damage the more likely it is that this
complication will arise.
We therefore recommend that this
technique be performed with rigid fixators
(e.g. Wagner as modified by Cañadell), at
slow distraction speeds (less than 1 mm/day
if possible), and with patients approaching
skeletal maturity in age.
B) Complications deriving from the
epiphyseal positioning of the screws
In physeal distraction, at least two of
the screws or pins must be inserted into the
epiphysis beside the growth cartilage to be
Bone lengthening by physeal distraction
subjected to distraction. This entails the risk
of physeal damage (e.g. fractures), which may
be aggravated if, as in the case of femoral
distal physis distraction, the epiphyseal screws
come into direct contact with the articular
cavity (Fig. 5). In this latter case the risks of
arthrosis, septic or traumatic arthritis, etc.,
and stiff joints spring readily to mind.
In our experience, we have seen fracture
of the distal tibial epiphysis on one occasion.
In that case, the cause of this was certainly
the incorrect placing of the screws, which
did not go completely through the epiphysis
(Fig. 6). This has also been ascertained in our
experimental cases.
With distraction at the proximal tibial physis,
another kind of epiphyseal fracture may appear
through the anterior tibial tubercule becoming
joined to the proximal tibial metaphysis
while the metaphysis-epiphysis separation
is occurring. In addition to the fracture itself,
the result is a iatrogenic low patella which can
have adverse effects on the biomechanics of the
knee. Close clinical and radiological surveillance
-especially on the lateral plane- over the first
days of the distraction is crucial. If this fracture
occurs it is advisable to desists and put off the
scheduled distraction.
In our opinion the most serious problem
involved in this technique is the possibility
that septic arthritis of the knee may set in
when the distraction at the femoral distal
physis is being performed. Assuming that the
indication for this technique is correct, this is
a risk that must necessarily be run, though
the greater the care and hygiene in the daily
management of the screw or pin wounds the
slighter that risk will be.
Stiffness of the joints, particularly the knee,
is usually a matter of concern to surgeons too.
In our experience, a great deal of knee stiffness
always appears in distraction at the femoral
distal physis (though not in distraction at the
proximal tibia where such stiffness is rare) (Fig.
7). However, the stiffness declines, to the point
255
J. de Pablos
Figure 7. Physeal distraction of the proximal tibia
showing good flexion of the adjacent knee. In such
cases knee stiffness is uncommon.
of near-normal motility in most cases, when the
apparatus is removed. In our clinical practice,
the intensive physical therapy recommended
by other authors only causes greater pain and
maintains a state of permanent inflammation
around the distal femoral screws that worsens
the stiffness and increases the risk of septic
arthritis. We prefer to let the child move
the involved joint as best he can during the
distraction process, leaving any physical therapy
until after the apparatus has been removed. In
short, we do not think that joint stiffness is a
greater problem with physeal distraction than
with other lengthening techniques.
As regards the possible appearance or
arthrosis, we are not aware of having had
such problems with our patients. In any case,
we believe this would have to be studied over
the very long term, and we have only sixteen
years experience with physeal distraction.
Finally we would like to stress once more
what we believe to be the points requiring
special attention for minimizing potential
complications:
• Ensure that the indication for the
procedure is correct. Use it with children
nearing the age of skeletal maturity.
• Use a fixator-distractor of proven quality,
and one that can work in the rigid mode.
• Do not exceed a distraction speed of 1
mm/day.
256
• Take painstaking care over hygiene
throughout the process, particularly with
respect to the screw wounds.
• Maintain close clinical-radiological
surveillance over the first few days of the
distraction.
• Do not force motion in the joints around
the distraction point while the distracting
apparatus is in place.
REFERENCES
1. Bensahel H, Huguerin Ph, Brard JL: L’allongement
trans-èpiphysaire du tibia. A propos d’un cas. Rev
Chir Orthop 1983;69:245-7.
2. Berchiche R, Witte KF: Allongement du squelette
jambier par èpiphysiolyse-dystraction. Traitement
des inègalitès des membres infèrieurs. Acta Orthop
Belg 1983;49:321-31.
3. De Bastiani G, Aldegheri R, Renzi-Brivio L,
Trivella G: Limb lengthening by distraction of the
epiphyseal plate. A comparison of two techniques
in the rabbit. J Bone Joint Surg 1986;68-B:545-9.
4. De Pablos J, Cañadell J: Experimental physeal
distraction in immature sheep. Clin Orthop
1990;250:73-80.
5. De Pablos J: Histology of physeal distraction and
the effect of the rate of distraction on physeal
preservation. Libro de resœmenes del 16th
Pediatric Orthopedic International Seminar. San
Francisco. Mayo 1988.
6. Eydelstein BM, Udalova NF, Bochkarev GF:
Dynamics of reparative regeneration after
lengthening by the method of distraction
epiphysiolysis. Acta Chir Plast 1973;15:149-
54.
7. Fischenko PJ, Karimova LF, Pilipenko NP:
Distraction epiphysiolysis in congenital shortening
of lower extremity. Ortop Traumatol Protez
1976;37:44-62.
8. Fishbane BM, Riley LH: Continuous transphyseal
traction. A simple method of bone lengthening.
Johns Hopkins Med J 1976;13.

9. Fishbane BM, Riley LH: Continuous transphyseal
traction: experimental observation. Clin Orthop
1978;136:120-4.
10. Houghton GR, Duriez J: Allongement tibial
par èlongation du cartilage de croissance tibial
supèrieur. Etude èxperimentale chez le lapin. Rev
Chir Orthop 1980;66:351-6.
11. Ilizarov GA, Soybelman LM, Chirkova AM: Some
roentgenographic and morphological data on
regeneration of bone tissue in experimental
distraction epiphysiolysis. Ortop Travmatol Protez
1970;31:26-45.
12. Ilizarov GA, Soybelman LM: Some clinical and
experimental data on the bloodless lengthening
of the lower limbs. Exp Khir Anest 1969;4:27-
32.
13. J a n i L : D i e d i s t r a k t i o n e p i p h y s i o l y s e .
Tierexperimentelle Studie zum Problem der
Beinverlangerung Z Orthop 1975;113:189-98.
14. J a n i L : T i e r e x p e r i m e n t e l l e S t u d i e u b e r
Tibiaverlangerung durch Distraktionepiphysiolyse
Z Orthop 1973;111:627-30.
15. Letts RM, Meadows L: Epiphysiolysis as a method
of limb lengthening. Clin Orthop 1978;133:230-45.
16. Monticelli G, Spinelli R, Bonucci E: Distraction
epiphysiolysis as a method of limb lengthening.
II Morphologic investigations. Clin Orthop
1981;154:262-73.
17. Monticelli G, Spinelli R: Allongement des membres
par distraction èpiphysaire. Rev Chir Orthop
1981;67:215-20.
Bone lengthening by physeal distraction
18. Monticelli G, Spinelli R: Distraction epiphysiolysis
as a method of limb lengthening I. Experimental
Study. Clin Orthop 1981;154:256-61.
19. Monticelli G, Spinelli R: Distraction epiphysiolysis
as a method of limb lengthening. III Clinical
applications. Clin Orthop 1981;154:274-85.
20. Monticelli G, Spinelli R: Limb lengthening by
epiphyseal distraction. Int Orthop 1981;5:85-90.
21. Peltonen J, Alitalo I, Karaharju EO, Helio H:
Distraction of the growth plate: experiments in
pigs and sheep. Acta Orthop Scand 1984;55:359-62.
22. Ricciardi L: Epifisiolisi distrazionale mono-
compartimentale. G Ita Ortop Traum 1984;16:57-61.
23. Ring PA: Experimental bone-lengthening by
epiphyseal distraction Br J Surg 1958;49:169-73
24. Sledge CB, Noble J: Experimental limb lengthening
by epiphyseal distraction. Clin Orthop 1978;136:111-
9.
25. Steen H, Fjeld TO, Ronningen H, Langeland N,
Gjerdet NR, Bjerkreim I: Limb lengthening by
epiphyseal distraction. An experimental study
in the caprine femur. J Orthop Res 1987;5:592-9.
26. Wevdenskogo SP: Distraction epiphysiolysis of
crural bones. Ortop Traumatol Protez 1971;10:53-55.
27. Zavijalov PV, Plaskin JT: Distraction epiphysiolysis
in lengthening of the lower extremity in children.
Khirurgija 1968;44:121-37.
28. Zavijalov PV, Plaskin JT: Elongation of crural
bones in children using a method of distraction
epiphysiolysis. Vestn Khir Grekova 1967;103:67-82.
257
30 Leg lengthening by distraction
epiphysiolysis
G. Monticelli†, R. Spinelli, R. Forte and L. Lorio
Distraction epiphysiolysis is a closed and
almost bloodless method for leg lengthening.
The use of this technique has to be limited to
cases in which the growth plate is still open;
that is, patients below the age of 14-16 years.
In our institution, we performe this
technique by using a circular external fixator
attached to the bone with Kirschner’s wires of
2 mm section, subjected to a tension of 120 kg.
This apparatus permits to satisfy all the
basic requirements of a well-performed
lengthening, i.e. the stability of the system
(rings), the elasticity (tensed Kirschner’s wires),
and the small thickness of the osteosynthesis
material. This last characteristic is important
when transfixing epiphyseal structures of no
more than 12-15 mm wide.
The two proximal wires are placed through
the epiphysis of the skeletal segment to be
lengthened, while the distal wires are placed
in the mid-inferior third, at the other side of
the growth plate.
During the first days after the placement
of the device, the lengthening rate should be
maintained at 0.5 mm/day, in three times.
After 10 days, the detachement of the
epiphysis or epiphysiolysis is usually completed.
Clinically, this feature can suddenly be noticed
by local pain, varying people to people in
severity, being in general moderate. The reason
258 Reprinted with permission of Mapfre Medicina (vol. 4, suppl 2)
to employ a 0.5 mm/day rate is because the
pain increases when using 1 mm/day.
In the first phase of the epiphysiolysis,
histological studies have shown the induction
of a great haematoma which do not disperse
through the adjacent soft tissue due to the
integrity of the periostium. This periosteal
integrity is basic condition in order to achieve
a good reparative process. The epiphyseal
detachment from the metaphysis occurs mostly
at the level of the hypertrophic or degenerated
cells of the growth plate, remaining preserved
the superior layers. However, this is not an
absolute route since in some cases we have
observed fracture lines at different cellular
layers.
After one or two days of rest, the
lengthening is restarted with a rate of 1.25
mm/day, in three times.
During lengthening in the following days,
the haematoma is replaced by a mesenchymal
tissue in which fibroblasts can be differentiated.
Previously undulated, the collagen fibers of
this substance are going to be stretched by the
progressive traction. Around the second week,
these fibers will start their ossification by direct
mineralization. The ossified bundles of collagen
are cemented within them by an osteoid material
produced by bone-inducing cells derived from
the mesenchymal tissue.

Once the distraction is interrupted, this newly
ossified tissue become stronger and maturates
until forming a cortical tissue which in time
undergoes a remodelation process leading to
a completely normal haversian cortical bone.
The fixator is not removed until the thickness
of the newly formed corticals guarantee the
physiological loading of the extremity.
Theoretically, the distraction epiphysiolysis
can be applied to whatever epiphysis. However,
we dissuade to performe it at the distal femur
since the wires have to cross the intraarticular
space. This fact creates a clear risk for articular
infection and presumably a consolidation delay
in case that the haematoma could mix with the
synovial fluid. Furthermore, crossing the knee
joint, the Kirschner’s wires induce a temporal
but substantial decrease in the range of motion.
In our opinion, the distal tibia should
be discarded for lengthening by distraction
epiphysiolysis because of the high number
of problems and complications related to
the alteration of the anatomical relationships
between fibula and tibia at the ankle level.
Our clinical experience is based on 101 cases
treated with distraction epiphysiolysis. Of these,
83 were performed in the proximal tibia, 6 in the
distal tibia, 9 in the distal femur and 3 further
cases underwent bipolar lengthening of the
tibia. The hypometry varied from 3 to 27 cm,
the average shortening being 7 cm.
The etiology was congenital in 53%, post-
traumatic in 21 %, dysplasia in 15%, neurologic
in 6% and post-infection in 5%. The follow-up
was monitored by radiographic check-ups
every week during the period of distraction
and every two weeks until the removal of
the fixator. Later on, the radiographic control
was done once a month. Along the whole
treatment period, patients underwent daily
clinical examinations, medication when needed
and one or two sessions of physiotherapy.
The mean duration of treatment was
around one month per cm lengthened with
a variation of + 20%.
Leg lengthening by distraction epiphysiolysis
Distraction epiphysiolysis for treatment
of leg length discrepancy is a valid method,
although, as we have mentioned, it has its
indication in patients with a particular stage
in their bone maturity process and only in
certain localizations.
Distraction epiphysiolysis is not free from
complications, but the possible failures when
treating leg length discrepancies do not obscure
the validity of this method.
This method has the advantages of a notable
briefness and simplicity of execution and the
low aggression to the anatomical structures. In
fact, this aggression is reduced to the insertion
of 2 mm section Kirschner’s wires which takes
a maximum of 30 minutes operation.
Thus, together with the minimal anesthesia
required, the small trauma produced in the
extremity facilitates that the patient can
walk just after surgery, loading the operated
extremity.
Since we have observed that epiphysiolysis
can damage the growth plate, we performe
always this method in ages near to the closing
od the physis. Although this is the period
considered as ideal, distraction epiphysiolysis
can be applied to young people not so close
to maturity, that is, between 10 and 14 years.
In these cases, there are two way to proceed:
either by performing repeated lengthening
procedures, the last being by corticotomy
after reaching maturity, or by performing
a hypercorrection in the first lengthening
according to the tables for growth prediction,
in selected cases.
REFERENCES
- Monticelli G, Spinelli R. Allongement des membres
par distraction épiphysaire. Rev Chir Orthop
1981;67:215.
- Monticelli G, Spinelli R. Distraction epiphysiolysis
as a method of limb lengthening: I. Experimental
study. Clin Orthop 1981;154:254.
259
G. Monticelli, R. Spinelli, R. Forte, L. Lorio

- Monticelli G, Spinelli R, Bonucchi E. Distraction as a method of limb lengthening III. Clinical

epiphysiolysis as a method of limb lengthening: II. applications. Clin Orthop 1981;154:274.
Morphologic investigations. Clin Orthop 1981;154:262.
- Monticelli G, Spinelli R. Limb lengthening by
- Monticelli G, Spinelli R. Distraction epiphysiolysis epiphyseal distraction. Int Orthop 1981;5:85.

260
31 In-vivo mechanical response of the
human growth plate to distraction close
to skeletal maturity
J. Kenwright and J.L. Cunningham

INTRODUCTION
Distraction across the growth plate is used
fre­quently for lengthening the tibia or femur.
Recent experimental studies on epiphyseal
distraction have suggested that lengthening of
the growth plate without fracture is possible in
immature animals using low rates of distraction
and low distraction loads(1,2). It is claimed that
this re­duces markedly the risk of damage to
the growth plate and it is suggested that a
similar process can occur in young children
between 13-15 years of age when an accurate
assessment of leg length inequality is possible.
However, maturity can be difficult to assess
in this age range(4), and dis­traction may either
be performed too late and be impossible to
achieve, or too early with a subse­quent loss
of length due to fracture of the growth plate.
Hence, if this process of distraction without
fracture were possible in patients close to
skele­tal maturity it could be advantageous.
In this study, the mechanical events occurring
during various distraction regimes have been Figure 1. External fixator used for epiphyseal
mea­sured, and are related to in-vivo biological distraction showing load cell at distal end.
events, with the aim of identifying a regime which
might lead to lengthening without fracture.
attached to the external fixator (Fig. 1). Slow
distrac­tion rates of 0.5 mm/day were applied,
METHOD as were constant distraction loads. Axial force
Axial force acting during distraction was was mea­s ured prior to and immediately
moni­tored daily using a purpose built loadcell after each incre­m ent of lengthening, and

Reprinted with permission of Mapfre Medicina (vol. 4, suppl 2) 261

J. Kenwright, J.L. Cunningham

Load (N) Distance (mm)

Load (N) Distraction Controlled By:
Distraction Appelled: 0-5 mm/day
900
800 Rate= 0-5 mm/day
800 Load= 550N
700
700
600 Fibula divided
600
500 50
500
400 40
400
300 30
300
200 20
200
100 10
100

0 10 20 30 40 50 60 70 80 0 10 20 30 40 50 60 70
Days Days

Figure 2. Forces measured with time during constant Figure 3. Forces measured with time during constant
rate distractio. load distraction.

Load (N) Distance (mm) later. This overall pattern of fracture was seen
in all patients in the study.
800
Load controlled distraction was carried out
700
by applying a load below a level previously
observed as leading to failure. Despite this,
600
Fibula divided
50
lengthening with fracture still occurred after
500

40
8 days (Fig. 3).
400

30
The distraction loads for a 13 years old
girl who suffered traumatic partial closure of
300

20
the epiphysis are shown in Figure 4. In this
200

10
instance a peak force level of 800 N was reached
100

0 10 20 30
Figure 4. Forces measured with time for a patient
with partial epiphyseal closure.
distraction commenced within 48 hours of
frame application.
RESULTS
Figure 2 shows the sequential distraction
force readings for a boy of 13.5 years skeletal
age with a distraction rate of 0.5 mm/day.
The peak force is seen to rise steadily to 650
N at 13 days when there is a sharp decrease
reflecting failure of the growth plate which
was observed radiographically a few days
40 50
Days
60
at day 12 when sudden failure occurred with
progressive correction of deformity. Such
higher force levels are to be expected if there
are bony bridges.
In an amputation specimen from a 14 year
old made in which the growth plates had not
yet fused, in-vitro tibial growth plate failure
loads were determined using a tensile testing
machine. The distraction loads for failure of the
upper tibial epiphysis was found to be 1,700 N,
considerably greater than those found during
in-vivo lengthening.
CONCLUSIONS
For all the distraction regimes applied, it
was not possible to lengthen the limb without
there being evidence of fracture, as assessed
both ra diographically and by a sudden

262
 In-vivo mechanical response of the human growth plate to distraction close to skeletal maturity
reduction in the peak distraction force. With
both constant dis­traction rates and loads growth
plate failure oc­curred at a peak force level of
between 600-800 N, considerably below that
seen in-vitro. This fin­ding confirms earlier
experimental work(5) and indicates tltat there
is a biological response of the growth plate
which makes it more suscepti­ble to fracture
after several days of distraction. All the children
lengthened by this method were between 13
and 16 years old, and it would ap­pear that
fracture must always occur in this age group
when using epiphyseal distraction if a sig­
nificant increase in limb length is required.
REFERENCES
1. De Bastiani G, Aldegheri R, Renzi-Brivo L,
Tri­vella G. Limb Lengthening by distraction
of the epi­physeal plate. A comparison of two
techniques in the rabbit. J Bone Joint Surg 1986;68-
B:545-549.
2. Spiggins AJ, Bader DL, Cunningham JL, Kenwright.
Distraction physiolysis in the rabbit. Ac­ta Orthop
Scand 1989;60:154-8.
3. De Bastiani G, Aldegheri R, Renzi-Brivo L,
Tri­v ella G. Chondrodiastasis-controled
symmetrical dis­traction of the epiphyseal plate.
Limb lengthening in chil­dren. J Bone Joint Surg
1986;68-B:550-556.
4. Monticelli G, Spinelli R. Distraction epiphysioly­
sis as a method of limb lengthening. Clin Orthop
1981;154:254-85.
5. Noble J, Diamond R, Stirratt CR, Sledge CB.
Breaking force of the rabbit growth plate and its
ap­plication of epiphyseal distraction. Acta Orthop
Scand 1982;53:13-6.
263
 Part V
Physeal surgery for the treatment of
angular deformities
32 Temporary stapling of the growth-plate
according to Blount for the treatment
of axial deformities and leg-length
discrepancies
R. Krauspe, P. Raab, A. Wild, J.L. Vispo-Seara and A. Richter
Axial deviations and limb length
discrepancies are frequent causes of patient
presentation in the pediatric orthopaedic clinic.
Primary or secondary bow legs or knock knees
showing more than 5° difference to the normal
angle of 174° might become an indication for
corrective surgery.
Leg length discrepancies (LLD) of more
than 2 cm and its conservative management
(shoe lift, insoles) are rarely accepted, therefore
surgical treatment of these conditions are
frequently considered. There are several
techniques described in the literature and in
detail in this book.
Already in 1933 Phemister(8) published his
landmark paper about definitive growth arrest
by epiphyseodesis. Since then several further
developments were described. Since more
than 35 years the temporary epiphyseodesis
according to Blount(2) has been applied for
surgical therapy of various deformities in our
hospital. Though the majority of procedures
were performed around the knee some
anecdotal procedures at the ankle, elbow and
wrist were reported but without conclusive
results or recommendations. Especially in cases
of secondary LLDs the growth arrest at the
stapled normal leg was more predictable than
the growth potential of the affected short leg
including all difficulties in timing surgery and
duration of the epiphyseodesis. In our hands
the temporary epiphyseodesis according to
Blount is now exclusively applied for stapling
of the physis around the knee. Based on our
results we do no longer apply the stapling
method for primary or secondary shortening
as a unique procedure. The Blount stapling
might be much more an adjuvant procedure
for gross discrepancies which would otherwise
require excessive lengthening procedures
with increasing numbers and severity of
complications. We still use this technique
for focal gigantism with excellent results and
low discomfort for the patient. Since only the
growth of the long bones is controlled by
epiphyseal stapling the remaining gigantism
of the soft tissues has to be discussed with
the patient and the family for planning soft
tissue reduction procedures.
For knock knees and bow legs secondary
to trauma, infection or general dysplasias or
malformations in most of the cases temporary
stapling allows only for partial correction in
our hands. We therefore prefer other methods
like callus-distraction for correction of the
axis and lengthening. A stapling procedure
might be helpful as adjuvant procedure in
special cases to control the extent of frontal
deviation before or during a lengthening
procedure.
267
R. Krauspe, P. Raab, A. Wild, J.L. Vispo-Seara, A. Richter

C D
Figure 1. A) The staple. B) Schematic drawing of the staples in situ for temporary epiphyseodesis of the
medial growth plates of the distal femur and proximal tibia (example for correction of a genu valgum).
C) Intraoperative view of the staples inserted at the medial growth plate of the distal femur. D) Lateral
image intensifier x-ray showing three staples at the distal femur and four staples at the proximal tibia,
well balanced in the sagittal plane.

In idiopathic bow legs or knock knees
temporary epiphyseodesis according to
Blount allows for predictable good results if
timing and technique of surgery are carried
out correctly as well as postoperative follow-
up examinations are perfomed at regular
intervals. There is the disadvantage of a
second procedure for removal of the staples
and somewhat longer scars compared to the
definitive epiphyseodesis (Phemister). On
the other hand good results are obtained in
a high percentage applying a safe procedure
which at several institutions has proven to
effectively reduce growth potential at the
growth plates around the knee.
PATIENTS AND METHODS
In 1990 we reviewed 34 cases of angular
deformities and 24 cases with LLD out of
a total of 97 patients treated by temporary
stapling of the epiphyses at the knee. In most

268
 Temporary stapling of the growth-plate according to Blount for the treatment of axial deformities and …
Age at primary surgery
n n=58
6
5
4
2
1
0
3 4 5 6 7 8 9 10 11 12
female male
Table 1. Age distribution at time of primary surgery.
of the cases three staples were inserted under
image intensifier control (Fig. 1). All patients
included showed skeletal maturity, therefore
end results of this method could be obtained.
Since primary and secondary deformities as
well as primary and secondary LLD were
enclosed we were able to compare the results
of these groups. The age at the time of primary
surgery is of specific interest with respect to
complications i. e. loosening/dislocation of the
staples. Based on the outcome we developed
distinct guidelines for our present management
of deformities in children and adolescents. All
patients included in this study had complete
records, long x-ray films and a complete
assessment including roentgenogramms at
follow-up. If there were clinical signs of genu
ante- or recurvatum additional lateral x-rays
were taken. The mean follow-up time was 16
6/12 years. The degree of deformity ranged
from 6° - 20°, the degree of correction from
5° - 25 ° for angular deformities. There were
LLD from 2cm - 9cm with corrections showing
at follow-up LLD of 0cm - 7cm.
In patients with focal overgrowth
(gigantism, M. Klippel-Trenaunay) not only
the clinical and radiographic measurements of
the lengths of the long bones are necessary. In
addition the size of the feet and the differences
at the level of the pelvic wings have to be
considered for judging the final outcome.
The aim of all therapeutic efforts should be
a balanced horizontal lumbosacral segment
and consequently a straight spine.
RESULTS
The age at the time of primary operation
13 14 15
ranged from 3 to 15 years in both genders
Years with a mean of 9 years 6 months in girls and
10 years 4 months in boys (Table 1). There
was no difference of the mean ages between
patients with correction of the axis or LLD. The
duration of epiphyseodesis was 6-24 months
for correction of the axis and 2-8 years for
correction of LLD.
1) KNOCK-KNEES AND BOW-LEGS
There were 12 primary and 22 secondary
axial deformities. In 8/12 cases femoral
and tibial and in 4/12 cases tibial stapling
for idiopathic valgus or varus deformity
were performed. All patients showed
good (<5° from normal) and excellent (<3°
from normal) results in this group (Fig. 2).
For correction of secondary deformities
(Olliers disease, enchondral dysostosis, M.
Blount, posttraumatic, postinfectious and
other deformities) only 7/22 showed good
and excellent results (Fig. 3) but 15/22
required further surgery both for under- and
overcorrection (Table 2).
In idiopathic deformities the ideal age of
>9 years in girls and >11 years in boys were
seen in all cases. In secondary deformities
unsatisfactory results were seen in patients
who had surgery very early but also in
patients within the ideal age group. Taking
different parameters like age, degree of
deformity or remaining growth into account
there was no general or special observation
from which a more precise indication for this
technique could be worked out for secondary
deformities.
269
R. Krauspe, P. Raab, A. Wild, J.L. Vispo-Seara, A. Richter
A B
Figure 2. A) AP-x-rays of a twelve years old girl with bilateral genu varum preoperatively. B) After
correction over 18 months.
Pain and Function
Only 1/12 patients with idiopathic knock
knees or bow legs complained about slight
discomfort and dysaesthesia around the scar,
all others were painfree with full range of
motion and unlimited walking distance.
The broad spectrum of underlying diseases
in the group of secondary deformities includes
degenerative joint diseases, dysostosis and cases
with several operations. So it is difficult to judge
the influence of the Blount procedure as such
on the final outcome. Nevertheless 2/22 had no,
7/22 had mild pain and 13/22 had moderate
pain with daily activities. Three of these patients
were on crutches for out-door walking.
2) LEG LENGTH DISCREPANCIES
There were 17/24 patients treated for
270
LLD who had pathologic shortening and
subsequently a stapling procedure of the
longer normal leg and 7/24 who had focal
overgrowth (gigantism) treated on the affected
extremity. In the first group of LLD 10/17
showed a LLD of < 2cm at skeletal maturity.
But 7/17 still had discrepancies of > 2cm up
to 7cm in one case (Table 3).
The correction of focal overgrowth in
7 cases showed excellent results in five
patients with less than 1,5cm pelvic/sacral
obliquity. The remaining two patients showed
discrepancies of only 3cm and 5 cm at the
end of growth. This was less than 50% of
the predicted LLD prior to surgery in other
words more than 50% were corrected although
overall only a partial correction was achieved.
Accordingly 15/24 were rated as good and
9/24 were rated as fair or poor.
 Temporary stapling of the growth-plate according to Blount for the treatment of axial deformities and …

B C D

Figure 3. A) Clinical view of a unilateral genu varum (Blount’s disease) of an seven years old girl.
B) Corresponding x-rays. C) Postoperative x-ray one year after stapling, and D) the final clinical result
at 26 years follow-up.

Pain and Function influence the final outcome and it is impossible

At follow-up 8/24 patients had no and
13/24 mild pain with activies in daily life
and sports Three patients had to use a crutch
for longer distances. These three patients had
secondary LLD after trauma and/or infection
with signs of joint degeneration. As mentioned
before there are multiple factors which do
to figure out what are the sequelae of the
stapling procedure itself.
Side Effects
Patients who underwent surgery for
correction of the axis had no secondary leg
length discrepancy at follow-up but one patient

271
R. Krauspe, P. Raab, A. Wild, J.L. Vispo-Seara, A. Richter

Results Results
Axial deformities n LLD
n pathologic shortening
10
12 idiopathic
stapling of the longer leg
11 9 focal overgrowth stapling
secondary
10 8 of the longer leg
9 7
8 6
7
6 5
5 4
4 3
3 2
2
1
1
0 0
0-1 1-2 2-3 > 3 LLD cm
0-3° 4-5° 6°-9° > 9° Deviation excellent good fair poor
excellent good fair poor

Table 2. Results in primary and secondary axial Table 3. Results in LLD differentiated between
deformities pathologic short and pathologic long legs.

with 1cm. Of those who had epiphyseodesis
for LLD 4/24 showed mild deviations of the
axis (4°, 5°, 6° and 8°).
Complications
There were no deep infections or major
neurovascular lesions. Three patients had
delayed wound healing and nine swelling
and/or effusion of the adjacent knee joint
for more than five days.
There were more dislocations found at
the proximal tibia, 35% (17/49) than at the
distal femur, 26% (10/39) and more in patients
treated for LLD, 46% (11/24) than in patients
treated for axial deviation, 29% (10/34). These
figures include in majority cases of a single
dislocation of only one staple without altering
the course of management.
The most important finding of this category
was a significant difference of loosening/
dislocation of the staples in different age
groups (Table 4).
DISCUSSION
Children and adolescents presenting with
knock knees and bow legs are frequently
seen in pediatric orthopaedic clinics. After
birth bow legs and in toddlers and younger
children knock knees are regularly found.
Reaching adolescence the final axis of the
leg will establish itself in normal as well
as in pathologic cases. During adult life
several factors contribute to further or new
deviations of the axis i. e. overweight. The
pediatric orthopaedic surgeon has to consider
the general growth charts and to analize the
given individual deformity(1,5,7,10,12).
Secondary deformities can occur at any
time and stage of skeletal developement.
The most important findings are the size
of the area of damage of the physis and the
remaining growth potential. Not only the
significant higher complication rate in the
younger age group especially loosening of
the staples but the unpredictable growth at
different stages of the various conditions seem
to be of great importance for the selection of
treatment modalities in a given secondary
varus or valgus deformity of the leg. Several
contributions in this book cover these subjects
therefore we should only like to stress our
experiences with temporary stapling in
various secondary deformities. They are in
contrast to primary idiopathic deformities
less encouraging. Therefore we no longer
recommend the temporary epiphyseodesis
according to Blount as method of first choice
for secondary axial deformities or LLD due
to limb hypoplasia, trauma, infection or
others. In addition to unsatisfying results the
procedure is performed on a healthy longer

272
 Temporary stapling of the growth-plate according to Blount for the treatment of axial deformities and …
Table 4. Loosening & Dislocation showing
significant differences in the given age groups
Girls < 9Y Girls > 9Y
Boys <11Y Boys >11Y
(25 Ops=43%) (33Ops=57%)
76% (19/25) 6% (2/33)
extremity encountering local complications
on the unaffected leg.
In rare instances of focal overgrowth
(gigantism, M. Klippel-Trenaunay) gross LLD
are seen. Already at the age of six to eight years
the difference may reach up to 10 cm. Planning
the definitive epiphyseodesis in these cases is
very difficult as no charts fore overgrowing
extremities are so far described in the literature.
Timing is even more complicated as not only
the difference of the long bones has to be
considered but also the overgrowth of the foot
and hemipelvis. To prevent overcorrection,
the primature closure of the growth-plates
in limbs with focal gigantism has to be taken
into account. In these cases the temporary
epiphyseodesis allows for growth control.
At regular intervals of 4 months LLD, level of
the pelvis and spine are assessed. The normal
growing non-affected extremity will much
more likely allow to calculate the final length
based on growth charts(7). This management
allows for timing of surgery and duration of
the epiphyseodesis. Overcorrection should
not exceed the growth rate of one year and a
remaining growth of one year for the gigantic
extremity - size of foot and hemipelvis
encountered.
For practical purposes we finish the stapling
period when a straight spine is achieved by
underlying two centimeters under the affected
leg. On ideal conditions this stage should be
one year before growth arrest of the affected
leg. In recent cases seen in another three
patients the final LLD was within <1,5 cm
applying these parameters. However treating
these patients over a long period the gigantism
of the soft tissues becomes more obvious.
Therefore we always mention the possibility of
further plastic surgical procedures very early.
There are only few papers about the
temporary epiphyseodesis according to Blount
for correction of LLD. In 1986 Watillon and
Hoet (11) reported 29 procedures with 20
good results which had shortening secondary
to various diseases. In conclusion they
recommended this procedure for moderate
LLD and stapling at correct stage of growth.
Joint stiffness and the necessity of mobilisation
under anaesthesia were reported by Watillon
and Hoet as well as by Bonnevialle et al.
(1982)(3). In our series of 58 patients treated
for LLD and axial deformities we did not
have to deal with this kind of problem. New
technologies for lengthening of the short leg
have shown good results in several series.
The advantages of these procedures include
surgery on the pathologic extremity as well
as control of length and axis with higher
percentages of good outcome. Since the
complication rate raises up with increasing
lengthening temporary epiphyseodesis as
adjuvant procedure might be indicated to
prevent gross leg length differences. Therefore
this technique should be included into the
considerations of overall treament concepts
for LLD.
For the surgical treatment of axial
deformities some authors reported excellent
and good results using the Blount technique.
Howorth (1971)(6) reported on 15 out 16 patients
with idiopathic knock knees very good results
and Pistevos and Duckworth (1977)(9) found
good results in 43 out of 49 children treated
for knock knees with this method. In three
patients revision surgery for staple loosening
was necessary. In our study staple loosening
was seen in cases with secondary deformities
especially in the young age group (see Table 4).
273
R. Krauspe, P. Raab, A. Wild, J.L. Vispo-Seara, A. Richter
Our study on idiopathic deformities underlines
recommendations given by these authors,
timing of surgery at the age of > 9 years
in girls and > 11 years in boys as well as a
consequent follow-up on a regular base. Like
in secondary LLD our results of secondary
axial deviations treated with staples were
disappointing. Similar conclusions were also
drawn by Cabalzar (1978)(4). Zuege, Kempten
and Blount(12) published in 1979 the end results
of 44 patients with idiopathic knock knees
and bow legs and 12 patients with combined
axis deviation and LLD. Their results were
satisfactory in 66% and fair in 21% but poor in
13%. Revision surgery had to be performed in
10 out of 12 patients with combined deformities.
These authors concluded revision surgery in
those cases should not be considered as a
complication but is given by the method itself.
We feel that this procedure is safe,
predictable and shows a low complication
rate if performed at the correct age for patients
with idiopathic (primary) knock knees or bow
legs. In our study we also found good results
for growth control in cases of focal gigantism.
For secondary axial deviations and secondary
LLD we recommend other procedures like
osteotomies and callus-distraction but in
difficult conditions stapling of the epiphysis
might be helpful as an adjuvant procedure in
some of these cases.
REFERENCES
1. Anderson M., Green WT., Messner MB. Growth
and predictions of growth in the lower extremities.
J Bone Joint Surg 1963; 45-A: 1-14.
274
2. Blount WP., Clarke GR. Control of bone growth
by epiphyseal stapling. A preliminary report. J
Bone Joint Surg 1949;31-A:464-478.
3. Bonnevialle P., Durroux R. Cahuzac JP., Lebarbier
P. Laville JM. Pasquie M. Traitement des déviations
frontales du genou par épiphyseodèse temporaire
de Blount. Etude expérimentale et clinique. Rev
Chir Orthop 1982;68:115-122.
4. Cabalzar A. Erfahrungen mit der temporären
Epiphyseodese nach Blount. Z Orthop 1978;116:355-
362.
5. Greulich WW., Pyle SI. Radiographic atlas of
skeletal development of the hand and wrist. 2nd
ed Standford University Press. Stanford 1959.
6. Howorth B. Knock knees. With special reference
to the stapling operation. Clin Orthop 1971;77:233-
246.
7. Moseley CF. A Straight-line graph for leg-length
discrepancies. J Bone Joint Surg 1977;59-A:174-
179.
8. Phemister DB. Operative arrestment of longitudinal
growth of bones in the treatment of deformities.
J Bone Joint Surg 1933;15-A:1-15.
9. Pistevos G., Duckworth T. The correction of genu
valgum by epiphyseal stapling. J Bone Joint Surg
1977;59-B:72-76.
10. Siffert RS. The effect of staples and longitudinal
wires on epiphyseal growth. J Bone Joint Surg
1956;38-A:1077-1088.
11. Watillon M. Hoet F. L’agrafage épiphysaire dans le
traitement des inégalités de longeur des membres
inférieurs. Acta Orthop Belg 1986;52:209-216.
12. Zuege RC., Kempken TG. Blount WP. Epiphyseal
stapling for angular deformity at the knee. J Bone
Joint Surg 1979;61-A:320-329.
33 Idiopathic genu valgum treated by
epiphysiodesis in adolescence
J.B. Volpon
INTRODUCTION
Many healthy children may present
variations in the knee frontal angle, usually
not requiring treatment as they will show
spontaneous correction with growth(6,8,13,14).
However, in a minority of cases, the
expected correction may not occur or a child
with a previous normal knee angulation may
present an exaggerated valgus that appears in
adolescence(7) which, if not corrected in time,
will persist throughout life(9,12).
Temporary partial medial epiphysiodesis
stands as an option for the correction, and it can
be achieved with metal staples(1,7,9,11,12,15). This
procedure will arrest the bone growth at the
medial side of the bone allowing the opposite
side to grow normally, thus straightening the
knee. At this point the staples can be removed.
Many literature reports consider together
the treatment of both knee angular deformities
(valgus and varus) and do not distinguish
the idiopathic cases from those secondary to
miscellaneous underlying conditions(4,5,9,16).
In the present investigation we carried out a
prospective study in which only patients with
idiopathic genu valgum treated by stapling
were included.
MATERIAL AND METHODS
Twenty-three patients with adolescent
Reprinted with permission of Springer-Verlag
(International Orthopaedics (SICOT) 1997;21:228-231).
genu valgum were treated by medial partial
epiphysiodesis at the distal femurs or proximal
tibias (46 knees) with metal staples. There
were 13 boys with a median age of 14 years
and 3 months (range: 12 years - 15 years and
8 months) and 10 girls with a median age
of 12 years (range: 11 years - 12 years and 9
months); 17 white and 6 blacks.
The diagnosis was made in adolescent
individuals during the growth spurt, with
bilateral, symmetric and rapidly increasing
genu valgum without any underlying
pathologic condition (primary genu valgum).
Four patients referred genu valgum since
infancy that had worsened during adolescence.
In the remaining cases the knee had been
normal during infancy and the deformity had
appeared in adolescence. All patients were
previously photographed and had standard
AP and lateral X-rays taken from the knees in
the standing position. The longitudinal axis
of the femur and tibia were traced and the
angle between them were taken as the knee
frontal angle. Moreover, the intermalleolar
distance was measured with the patient in the
supine position, positioning the lower limbs
symmetrically with the patellae facing upward
and keeping the medial femoral condyles
gently touching.
Surgical correction was indicated for
healthy individuals during the growth spurt,
275
J.B. Volpon
14
DOT
male, 12+7 years old
12
10
IM DISTANCE (cm)
8
6
4
staple
removal
2
0 150
0 5 10 15 20 25 30
and when the intermalleolar distance was 10.0
cm or more. In all cases medial epiphysiodesis
of the distal femurs was performed with 3
stainless steel staples, following the technique
reported by Blount(1).
With an image intensifier the medial
periphery of the growth plate was identified
with a needle inserted into it and kept in place
throughout the operation as a guide. The skin
incision was centered in the probing needle
and placed either transversaly (10 knees) or
oblique, along the medial border of the vastus
medialis (36 knees). The periphery of the
growth plate was approached and three Blount
staples were driven into the bone at a distance
of 1.0 cm from each other. Care was taken to
place the staples well centered in the periphery
of the physis and neither too anteriorly
nor too posteriorly in the femoral condyle.
Staple positioning was checked in the image
intensifier, a radiograph was taken, the wound
was closed in layers and with intracuticular
stitches in the skin. Five individuals nearing
the end of growth or with severe deformities
(~16.0 cm of intermalleolar distance) had the
operation also performed in the proximal tibia
with 3 additional staples being inserted in
276
STATURE (cm)
180
stature 175
170
IM.D.
165
160
155
Figure 1. The intermalleolar
distance progression after stapling
35 40 45 50 55 60 had a reverse relationship with
TIME (month) stature. In this case there was no
need to remove the staples.
that bone. After operation knee motion and
early walking were encouraged.
The patients were seen at regular intervals
that varied from 2 to 6 months, and the
intermalleolar distance was recorded.
In 15 cases, stature was also routinely
recorded on the occasion of each visit. A
graph with a plot of intermalleolar distance
and stature versus chronological age was
constructed for each patient. Radiographs
were not routinely taken. For most patients the
staples were removed when the intermalleolar
distance reached zero or when there was a
slight knee varization. The median follow-up
was 36 months and all patients were followed
to the end of growth (16 cases), or to the
complete closure of the knee growth plates
(7 cases). At this point, they were X-rayed
and photographed.
The author took all the measurements and
examined all the patients during treatment
and follow-up.
RESULTS
The median intermalleolar distance before
the operation was 13.0 cm (range: 10.0 - 21.0

LCL
male, 14+15 years old
14
epiphysiodesis
12
10
IM DISTANCE (cm)
8 Figure 2. After stapling the
6 164
4 knee valgus. The knees were
2
0 160
0 5 10 15
cm) for boys and 12.0 cm (range: 10.0 - 21.0
cm) for girls. The final result showed a median
intermalleolar distance of 3.0 cm (range: 0 - 8.0
cm) for boys and 2.0 cm (range: 0.5 - 5.0 cm)
for girls.
For most cases, correction of the deformity
followed the increase in stature (Fig. 1). The
staples remained in place during a median
time of 11 months (range 8 - 15 months). In
almost all cases there was a rebound effect
that was greater shortly after staple removal
but slowing down in the following months
(Figs. 2 and 3). In 2 patients, growth continued
to occur unexpectedly after staple removal
and there was recurrence of valgus from an
initial intermalleolar distance of zero shortly
after staple removal to a final intermalleolar
distance of 7.0 cm in one case and 8.0 cm
the other (Fig. 4). In 6 cases, staple removal
was not necessary because the expected knee
alignment had occurred at the end of growth.
One patient underwent an additional operation
to replace two loose staples in one femur and
showed an uneventful recovery.
In one case a medial bone bridge had
formed in both femurs after staple removal.
This occurred in one of our first cases and
Idiopathic genu valgum treated by epiphysiodesis in adolescence
STATURE (cm)
168
166
medial side of the femoral
condyles there was a rapid
correction of the abnormal
162
allowed to display a slight
varus. With staple removal
the local growth was released
20 25 30 35 originating a rebound effect and
TIME (month) a final intermalleolar distance
of 2.0 cm resulted at the end of
the growth.
was due to poor technique, since the staples
were inserted too deeply into the bone, the
periphery of the growth plate was injured
at the time of their removal. Consequently,
a progressive varus deformity resulted. This
patient was reoperated upon and the bridge
was resected. The knee alignment turned to
valgus with 2.0 cm of final intermalleolar
distance, but there was a slight knee
asymmetry, and 1.0 cm of shortening on
the right side resulted (Fig. 5).
There were no cases of surgical infection
or limitation of joint motion. The scar was
antiesthetic in 7 cases. The best skin healing
occurred when the incision was placed in an
oblique fashion along the medial border of
the vastus medialis
DISCUSSION
Our results showed that the partial
epiphysiodesis provided an effective
correction of the excessive knee valgus that
was symmetrical and displayed a harmonious
course with no interference with physical
activities during its progress. The staples
cause a temporary growth arrrest on the
277
J.B. Volpon
14
IM DISTANCE (cm)
12
epiphysiodesis
10
4 staple
valgus removal
2
0
varus
-2
0 2 4 6 8 10 14 20
medial side of the bone and the method
takes advantage of the growth potential to
achieve correction. We agree with Masse
& Fermont that the indication to stapling a
knee for correction of a genu valgum should
be made with precision and moderation(10).
Close patient observation during the follow-
up period is mandatory and most of the
alleged complications can be prevented with
a careful technique.
The indication for the correction of a
progressive genu valgum is based on the
patient age and severity of the deformity.
Our results and those reported by others
indicate that ages between 11 - 13 years for
girls and 12 - 14 years for boys are adequate
for the operation because there is still enough
growth potential to correct the deformity(2,10).
When the operation is performed at an
earlier age the remaining growth is more
difficult to predict and there is a higher
rate of recurrences(10,11). The knock knee can
be expressed either by the intermalleolar
distance or by the radiological frontal angle.
The former is simple and can be promptly
taken. Volpon et al. demonstrated that the
278
PR
male, 15 years old
24 28 32 36 40 Figure 3. In this case the staples
TIME (month) were removed too early, and
there was recurrence of valgus.
intermalleolar distance is better correlated
with knee appearance with the additional
advantage of presenting smaller errors of
measurement(14). An intermalleolar distance of
10.0 cm impairs cosmesis and is an adequate
limit to indicate the correction. Based on
this information we chose the mininal age
of 11 years for girls and 12 years for boys,
and a minimal intermalleolar distance of
10.0 centimeters to perform the correction.
The two recurrences observed in the
present series may be explained by an early
staple removal. Masse & Zreik and Bowen
et al. presented trigonometric estimations to
decide about the appropriate age to perform
epiphysiodesis so that the knee correction
could be accomplished by the end of the growth
period, thus avoiding a second procedure to
remove the implant(3,11). Both methods require
the determination of skeletal age according
to Greulich and Pyle, not entirely valid for
Brazilian people(15). Consequently, we used
growth charts and the intermalleolar distance
to decide about the appropriate age to insert
and to remove the staples but the prediction
of the remaining growth for some individuals
 Idiopathic genu valgum treated by epiphysiodesis in adolescence

Figure 4. Radiological sequence showing a typical adolescent type of genu valgum, before treatment with
17º of knee frontal angle (A). Five months after stapling the medial femur the frontal angle changed to 8
degrees (B) and 6º at the skelletal maturity (C).

12
NM
male, 11+8 years old
IM DISTANCE (cm)

10

8 epiphysiodesis
Figure 5. With partial
6 epiphysiodesis on the medial
femurs the intermalleolar
4 staple removal distance reached zero 11 months
valgus
later when the staples were
2
taken out. This procedure was
0 traumatic and a bone bridge
across the growth plate caused
-2 bridge resection a progressive varus angulation.
varus
The bridge was promptly
0 10 20 30 40 50 60 70 removed and the knees turned
TIME (month) to valgus with 2.0 cm of final
intermalleolar distance.

may be difficult to ascertain and the estimated
final correction may not be achieved.
It must be emphasized that the periphery
of the growth plate should be left undisturbed
during the surgical approach, with no stripping
of the perichondrium and periosteum, with
gentle staple insertion until its cross bar
touches the cartilage surface. The same careful
technique must be followed during the staple
removal thus avoiding the formation of bone
bridges as occurred in one of our cases.
The stapling operation can be performed
through a small skin incision but conspicuous
and very apparent scars may result(12). This fact
is very important since many patients accept
the operation based on a cosmetic motivation.

279
J.B. Volpon
Therefore, gentle retraction of soft tissue is
recommended and adequate placement of the
incision is important. Our results were better
when the skin incision followed the border
of the vastus medialis muscle.
In conclusion, the correction of an
exaggerated genu valgum during adolescence
can be adequately achieved with stapling
of the medial knee growth cartilages, but
careful surgical technique and close patient
follow-up are important conditions to avoid
complications.
REFERENCES
1. Blount WP, Clarke GR (1949) Control of bone
growth by epiphyseal stapling. A preliminary
report. J Bone Joint Surg [A] 31:464-78.
2. Bowen JR, Leahey JL, Zhang Z-H, MacEwen GD
(1985) Partial epiphysiodesis at the knee to correct
angular deformity. Clin Orthop 198:184-90.
3. Bowen JR, Ruiz Torres R, Forlin E (1992) Partial
epiphysiodesis to address genu varum or genu
valgum. J Pediatr Orthop 12:359-64.
4. Dutoit M (1968) L’agrafage selon Blount dans les
déviations frontales idiopathiques des membres
inférieurs chez l’enfant. Chir Pédiatr 27:103-7.
5. Frantz CH (1971) Epiphyseal stapling: a
comprehensive review. Clin Orthop 77:
149-57.
6. Heath CH, Staheli LT (1993) Normal limits of
knee angle in white children - Genu varum and
genu valgum. J Pediatr Orthop 13:259-62.
280
7. Horworth B (1971) Knock knees. With special
reference to stapling operation. Clin Orthop 77:233-
46.
8. Kling TFJr, Hensinger N (1983) Angular and
torsional deformities of the lower limbs in children.
Clin Orthop 176:136-47.
9. Libri R, Sabett E, Stilli S, Andrisano A (1990) The
correction of valgus knee by temporary epiphyseal
stapling. Ital J Orthop Traumatol 16:221-28.
10. Masse P, Fermont F (1971) Traitement chirurgical
du genu valgum de l’adolescent. Rev Chir Orthop
57:219-24.
11. Masse P, Zreik H (1985) Peut-on déterminer l’âge
de l’épiphysiodèse dans le traitement du genu
valgum de l’adolescent? Rev Chir Orthop 71:319-25.
12. Pistevos G, Duckworth T (1977) The correction of
genu valgum by epiphysial stapling. J Bone Joint
Surg [B] 59:72-6.
13. Salenius P, Vankka E (1975) The development
of the tibiofemoral angle in children. J Bone Joint
Surg [A] 57:259-61.
14. Volpon, JB, Abreu EMA, Furchi G, Nisiyama
CY (1986) Estudo populacional do alinhamento
frontal do joelho no plano frontal durante o
desenvolvimento. Rev Bras Ortop 21:91-6.
15. Volpon JB, Andrade GB, Vieira RRB (1989)
Tratamento do geno valgo do adolescente
pela epifisiodese parcial temporária. Estudo
prospectivo. Rev Bras Ortop 24:159-64.
16. Zuege RC, Kempken TG, Blount WP (1979)
Epiphyseal stapling for angular deformity at the
knee. J Bone Joint Surg [A] 61:320-29.
34 Arthroscopic hemiepiphysiodesis.
Preliminary results in the correction of
idiopathic genu valgum in adolescents
J. de Pablos, R. Capdevila and J.A. Bruguera
INTRODUCTION
Certain degree of valgum angulation of
adolescents knees, particularly in females, is
considered normal. That is an intermalleolar
distance in a standing position of up to 8 cm(1)
and a distal femoral angle (angle formed by
the femoral diaphysis and the distal femoral
articular surface) of under 8º. Measurements
beyond these values with no other cause found
to explain the deformity, is called constitutional
or Idiopathic Genu Valgum (IGV).
In patients over 10 years old presenting
IGV, with an intermalleolar distance of over 10
cm., there is a low probability of spontaneous
correction of the deformity to occur. In these
cases surgery can be considered,(2) aiming at
an asymmetric growth arrest of the physeal
plate. Traditionally, this has been achieved
by stapling(3) or bone fusion.(4)
As an alternative to these open
techniques, the concept of using percutaneous
epiphyseodesis emerged. It was initially
indicated for treating limb discrepancies(5)
and later also used in cases of moderate
angular deformity such as IGV(6,7) offering
the main advantage of being a minimally
invasive technique.
This work presents the preliminary
experience in the correction of IGV with a new
internal distal femoral hemiepiphysiodesis
technique based on principles similar
to Bowen’s but approaching the physis
arthroscopically.
PATIENTS AND METHODS
Three cases of bilateral IGV in adolescent
girls ranging between 12 and 13 years of age
have been treated to date, with a minimum
postoperative follow-up of 20 months
(20-26 months). All 3 patients presented
preoperatively intermalleolar distances
ranging from 15 to 19 cm., and distal femoral
angle between 13º and 16º.
None of the patients had been operated
on previously and all three cases underwent
internal distal femoral arthroscopic
hemiepiphysiodesis with no other procedures
associated.
Surgical Technique
Routine set up for conventional surgical
arthroscopy is carried out in theatre, and
the surgical procedure is performed with
tourniquet. A standard anteroexternal portal
is used to introduce the arthroscope.
The first step is to identify the physeal
level, which is achieved using a percutaneous
needle under image intensifier control. The
needle will also indicate the level of the
281
J. de Pablos, R. Capdevila, J.A. Bruguera
Figure 1. Intraoperative X-Ray of the procedure.
Physeal ablation is initiated with a motorized
debrider under control with the arthroscope*.
internal portal used to introduce the surgical
instruments.
Subsequently, an incision is made on the
sinovium covering the internal surface of
the femoral condyle allowing us to approach
the bone and the physis, with the use of a
motorized debrider (cutter) (Fig. 1).
As of that moment, the ablation of the
physeal cartilage can be initiated by means of
an arthroscopic burr until an osteochondral
defect of approximately 2 cm. (width) by 1
cm. (height) by 1 cm. (depth) is obtained
(Fig. 2).
The defect is perfectly viewed through the
scope, at the bottom of which the physis must
be clearly identified. Once the right amount
of growth plate has been taken, thorough
washing, aspiration and closing of the wounds
are carried out. Compressive dressings are
applied as the last step in the procedure. In
the case of a bilateral involvement, both knees
are operated on during the same surgical time.
Twenty-four to forty-eight hours later
the patient is allowed partial weight-bearing
with the aid of crutches. At this moment knee
mobilization exercises (flexo-extension) and
strengthening of the quadriceps through
isometric exercises are initiated, and continue
until a satisfactory recovery of both functions
is observed.
282
Figure 2. Arthroscopic aspect of the surgical procedure.
Tissue ablation contains a small amount of epiphyseal
(E) and metaphyseal (M) bone as well as the physis*.
RESULTS
The formation of a physeal bone bridge in
the area of the surgical defect was observed
at follow-up. This was particularly visible in
the Magnetic Resonance Image where, after a
period of 12 months, mature physeal bridges
could be detected (Fig. 3).
The duration of the operation ranged from
20 to 35 minutes per joint and the hospital
stay varied between 24 and 48 hours.
At follow-up, correction of the deformity,
reaching normal values, was observed in all
cases (intermalleolar distance < 8 cm. and
femoral distal angle < 8º) (Figs. 4, 5).
No hypercorrections nor any other type
of intra or post-operative complications were
observed.
DISCUSSION
Although most of the patients presenting
IGV have a moderate angular deformity, in
the more severe cases it can require corrective
surgical treatment.
The effectiveness of epiphyseodesis and
percutaneous hemiepiphysiodesis in the series
published to date using Bowen´s technique(6)
or similar ones, (8-14) seems sufficiently
demonstrated.

B
Figure 3. Magnetic resonance. (Gradient-echo
sequence) Osteochondral defect immediately
following surgery (arrows) (A). Physeal bridge in the
operated area 14 months after surgery (arrows) (B).
Arthroscopic hemiepiphysiodesis can
be considered as one type of percutaneous
epiphysiodesis and therefore follows the
same basic principles. The innovation of
this operation is mainly technical (the use of
arthroscopy) and therefore this publication
is mainly focused in those technical aspects.
According to Bowen, percutaneous
hemiepiphysiodesis offers the important
advantage of its minimal surgical
aggressiveness. However, it does present two
significant inconveniences worth considering:
1) The use of X - rays during a significant
amount of time (image intensifier).
2) In the case of the distal femur, which
has a redundant physis, the fact that the defect
produced cannot be directly viewed makes a
more or less extensive tissue ablation necessary
in order to assure an adequate physeal lesion.
Arthroscopic hemiepiphysiodesis has
been effective in the first cases of IGV with
Arthroscopic hemiepiphysiodesis
Figure 4. Radiologic comparison of the distal
femoral angle. 14º before surgery (left) and 6º at
14 months after surgery (right).
long-term postoperative follow-up and is
advantageous regarding the percutaneous
techniques published to date.
The great difference that the arthroscopic
technique makes is that the surgeon operates
under direct vision. Therefore it is possible:
1. To achieve a reproducible physeal lesion
(above all in bilateral cases).
2. To achieve an adequate physeal lesion
with less tissue ablation.
3. To practically eliminate the use of X - rays.
On the other hand, we also feel that from
a surgical point of view the arthroscopic
technique is more elegant than the other
percutaneous techniques.
In cases of severe IGV, as in the cases we
presented, the correction of the deformities
is advisable from the point of view of the
mechanics (it improves gait dynamics), the
esthetics and the prevention of premature
knee arthritis.(15)
283
J. de Pablos, R. Capdevila, J.A. Bruguera

A B
Figure 5. Clinical aspect of the lower limbs. Situation before surgery showed an intermalleolar distance
of 19 cm. (A). Situation 14 months after surgery showed an intermalleolar distance of 8 cm. (B).

In our opinion, arthroscopic hemi- growth physiology, present clear differences

epiphyseodesis can be indicated in patients
close to skeletal maturity (adolescents) and
with a moderate to severe angular deformity
(as is the case on IGV).
Of course, as in any epiphyseodesis,
essential requirements are that the physis
still be functioning and that there is sufficient
remnant growth to correct the deformity. Covo
et al(7) described a method for calculating the
time for hemiepiphysiodesis in order to correct
angular deformities in immature patients.
We have not used these tables because they
were made with values based on Anderson
and Green´s values(16) which were determined
over 30 years ago, and also they were based
on North American patients who, regarding
with respect to spanish adolescents.
In our small series we have not observed
any complications worth mentioning, but
in our opinion there are two potential
complications which should be taken into
account: hemarthrosis and hypercorrection.
The first can be avoided with a compressive
dressing before removing the tourniquet and,
if it does occur, it is treated with aspiration
and a new compressive dressing.
It is more difficult for the second potential
complication to be significant because these
young patients, being close to skeletal
maturity, present a limited growth potential.
Nevertheless, from a theoretical point of view, if
a tendency towards hypercorrection is observed,

284

completing the epiphyseodesis will suffice
(which can also be done arthroscopically).
With respect to limitations of this technique
we can state that regarding the knee it can
only be used on the distal femur (not on
the proximal tibia) and that familiarity with
arthroscopic techniques is necessary.
We do not feel that the fact that it is an
irreversible surgical procedure is of great
significance due to the already mentioned
limited growth capacity of these young
adolescents.
REFERENCES
1. Cahuzac J, Vardon D and Sales de Gauzy J.
Development of the clinical tibiofemoral angle in
normal adolescents. J Bone Joint Surg [Br] 1995;77-
B:729-734.
2. Tachdjian MO: Pediatric Orthopaedics. 2nd. Ed.
Philadelphia. WB Saunders Company, 1990:2820-
2835.
3. Blount WP and Clark GR. Control of bone growth
by epiphyseal stapling; a preliminary report. J
Bone Joint Surg [Am] 1949;31-A:464-477.
4. Phemister DB. Operative arrestment of longitudinal
growth of long bones in the treatment of
deformities. J Bone Joint Surg [Am] 1933;15-A:1-15.
5. Bowen JR and Johnson WJ. Percutaneous
epiphysiodesis. Clin Orthop 1984;190:170-173.
6. Bowen JR, Ruiz Torres R and Forlin E. Partial
epiphysiodesis to address genu varum or genu
valgum. J Pediatr Orthop 1992;12:359-364.
7. Covo B, Dabney KW and Bowen JR. Percutaneous
epiphysiodesis for the treatment of angular
Arthroscopic hemiepiphysiodesis
deformities: The prediction tables. MAPFRE
Medicina 1993;4:197-201.
8. Ogilvie JW and King K. Epiphysiodesis: Two year
clinical results using a new technique. J Pediatr
Orthop 1990;10:809-11.
9. Atar D, Lehman WB, Grant AD and Strongwater
A. Percutaneous epiphysiodesis. J Bone Joint Surg
[Br] 1991;73-B:173.
10. Timperlake RW, Bowen JR, Guille JT and Choi IH.
Prospective evaluation of fifty-three consecutive
percutaneous epiphysiodeses of the distal femur
and proximal tibia and fibula. J Pediatr Orthop
1991;11:350-357.
11. Liotta FJ, Ambrose TA and Eilert RE. Fluoroscopic
technique versus Phemister technique for
epiphysiodesis. J Pediatr Orthop 1992;12:248-251.
12. Gabriel KR, Crawford AH, Roy DR, True MS and
Sauntry S. Percutaneous epiphyseodesis. J Pediatr
Orthop 1994;14:358-362.
13. Fraser RK, Dickens DRV and Cole WG. Medial
physeal stapling for primary and secondary genu
valgum in late childhood and adolescence. J Bone
Joint Surg [Br] 1995;77-B:733-735.
14. Mielke CH and Stevens PM. Hemiepiphyseal
stapling for knee deformities in children younger
than 10 years: a preliminary report. J Pediatr Orthop
1996;16:423-429.
15. Fernandez Palazzi F, Angulo A, Soria L and
Villegas M. Experience in the treatment of axial
deformities of the knee using Blount’s technique,
in San Juan de Dios Hospital, Caracas. MAPFRE
Medicina 1993;4:202-209.
16. Anderson M, Green W and Messner M. Growth
and predictions of growth in the lower extremities.
J Bone Joint Surg [Am] 1963;45-A:1-14
285
35 The biology and treatment of physeal
arrest
J.A. Ogden
While the disruption of normal physeal
growth, with formation of a restrictive osseous
bridge, may occur following any obvious
traumatic injury to a physis, such bridging
may also follow seem­ingly non-traumatic
infection (osteomyelitis or sep­tic arthritis),
thermal injury (burn, frostbite or electrical
injury), microvascular ischemia, meta­bolic or
hematological abnormality, tumour, the­rapeutic
irradiation, sensory neuropathy, or the insertion
of fixation devices(19,20,22,25,29). Traumatic physeal
injuries, especially in the up­per extremity, are
not usually associated with se­rious acute and
chronic complications(22,25,29). However, partial
to total growth arrest occa­sionally occurs, and
is more likely to occur fo­llowing physeal injury
in the lower extremity. Growth arrest is also
more likely to be a conse­quence of some of
the other less frequent, but more destructive
aforementioned causes. Total arrest affects
bone length, whereas partial phy­seal arrest
may also produce a progressive angu­lar
deformation when an eccentric bridge of bone
forms between the epiphyseal ossification cen­ter
and the metaphyseal bone, replacing a por­tion
of the physis. A long as the remaining phy­sis
attempts to grow “longitudinally” as well as
latitudinally by adding new bone peripherally
through the undamaged zone of Ranvier, angu­
lar, longitudinal, or latitudinal deformity may
oc­cur, either alone or in any combination(21,23).
286
Anatomical and physiological differences
of the physis and mechanism of injury all
affect risk factors. The rate of growth, size
(area) and the contour of each physis change
as the chondro­osseous skeleton progressively
matures(23). For example, while the distal radial
physis is one of the most frequently injured
growth regions, it is an extremely uncommon
site for a partial or com­plete physeal arrest(9,22),
although microinjury may occur(22). In contrast,
the proximal tibial and the distal femoral physis
account for only 3% of growth mechanism
injuries, but are among the most frequent
sites to sustain partial to com­plete physeal
damage(22,30). These physes are relatively large
in area, progressively “irregular” in contour,
and account for 60 to 70% of the growth of their
respective bones and leg length. Damage to
one of these specific growth plates in a young
child thus may have an extremely de­trimental
effect on longitudinal development. Type
3, 4 and 6 growth mechanism injuries ha­ve
the greatest potential to eventually form an
osseous bridge and certainly may do so rapidly
if anatomical, invariably open, reduction is
not undertaken(19,20). Even with accurate anato­
mical reduction, however, a physeal arrest
still may ensue in these patterns as well as
in type 1 or 2 physeal injuries(22,25).
Osseous bridging of the physis may not
beco­me evident radiographically until months
Reprinted with permission of Mapfre Medicina (vol. 4, suppl 2)

Figure 1. Peripheral osseous bridge.
to years have elapsed following the discrete
injury. Accor­dingly, it is important to follow
any child who has an obvious or even suspected
physeal injury for an adequate period of time
(ideally until skele­tal maturity). In most cases
some evidence of growth disruption will be
evident within the first year. If the physeal
injury occurs at a time when the epiphyseal
ossification center is not present or is small,
an osseous bridge may not be capa­ble of
forming until the epiphyseal ossification center
eventually expands sufficiently to justapo­se
the damaged physeal area, at which time a
bridge forms and angular deformity may
rapidly progress. The “bridge” is probably
present as da­m aged fibrovascular tissue
that only needs the appropiate osteogenic
stimulus. Radiographic bridging will most
likely occur before significant clinical signs
(angulation or shortening) occur. The earlier
the diagnosis is made, the sooner in­tervention
may be undertaken. The younger the patient
is at the time of the physeal injury, the more
likely it becomes that physeal disruption will
lead to a significant clinical problem. The
size and location of a physeal bridge and
the intrisic growth potential of the affected
physis will de­termine the progression of the
clinical deformity. If the partial physeal arrest
is situated peripherally or eccentrically, then
the remainder of the physis may continue to
The biology and treatment of physeal arrest
Figure 2. Linear osseous bridge.
grow, progressively producing an angular
deformity, as well as affecting length(16,20,36,41).
When the partial physeal arrest is central,
the peripheral physis attempts to grow, both
diametrically as well as longitudinally. This
causes “tenting” of the metaphysis, combined
with more extensive shortening of the bone.
The­re may be relatively little angular deformity
in the central arrest.
There are three basic patterns of partial
phy­seal arrest: peripheral, linear, and central.
They may affect growth potentials differently,
create diagnostic imaging patterns, and are
approached surgically by different methods. The
three types are arbitrary divisions, as one may
grade into an­other contingent upon the extent
of bridge for­mation centrally and peripherally.
The peripheral pattern (type 1 ) involves
a va­riable sized bridge extending in from
the physeal margin (Fig. 1). Such extension
may be only a few milimeters inward from
the periphery. The zone of Ranvier, the
specialized group of cells that is essential for
latitudinal growth of the phy­sis, is damaged
and overgrown with periosteum. This latter
tissue extends farther toward the epi­physis
than is normal and must be excised com­
pletely during surgical removal. This type of
os­seous bridge may create very severe angular
de­formation over a short time, especially
during a rapid growth period.
287
J.A. Ogden
The linear pattern (type 2) has an osseous
brid­ge extending across the physis, usually
connec­ting two separate segments of damaged
physeal periphery (Fig. 2). Perhaps, the most
common site is the medial malleolus following
a type 3 or 4 injury. Usually, there is normal
physeal and zo­ne of Ranvier tissue on either
side of the linear defect. This pattern also
may be associated with an angular deformity.
The central pattern (type 3) is the most
severe injury and the most difficult to correct
with sur­gical excision. A variable-sized osseous
bridge forms within the central portion of
the physis and is completely surrounded by
normal physis (Fi­g. 3). The peripheral zone of
Ranvier is unin­volved. Accordingly, the major
effect is central retardation of longitudinal
growth associated with continued latitudinal
growth that creates more and more physis
capable of attempting longitu­dinal growth.
Radiographically, a conical exten­sion of the
epiphyseal ossification center toward the
metaphysis characterizes these bridge pat­
terns. Because the zone of Ranvier “recovers”
latitudinal growth is unaffected(21).
In any of these three types of bridging,
it is im­portant to realize that the maturing
bridge usually is comprised of very dense,
sclerotic bone that is similar to cortical bone
. This is most evident at the time of surgery,
when it obviously con­trasts with the adjacent
trabecular (spongy) bone of the metaphysis
and secondary ossification center.
Plain radiography is the best imaging-
proce­dure to screen for the possibility of
an osseous bridge. However, this may not
clearly define the abnormality, especially since
radiographs of irre­gular physeal contours may
be misleading. The varios causes of physeal
damage, including trau­ma, usually cause a
temporary slowdown of growth that leads to
the formation of transver­sely oriented primary
spongiosa. This is followed by restoration of
more typical rapid growth which reestablishes
longitudinal orientation to the pri­m ary
288
Figure 3. Central osseous bridge.
spongiosa. The transversely oriented bone
becomes evident as the Harris line. If such a
Ha­rris line remains parallel to the physis as it
pro­gressively “separates” from the physis, then
da­mage to,the physeal growth mechanism is
unli­kely. However, if the physis and the Harris
line are not parallel or converge at a specific
point, the focal damage is likely present(21).
Growth plate activity may be further assessed
across its extent by quantitative scintigraphy(7).
Tomograms are usually helpful in
determining the configuration and the extent
of any osseous bridging, whether or not the
bridge is potentially resectable, and the
appropiate surgical approach(6). Excision of an
osseous bridge that constitu­tes 50% or more of
the overall estimated area of the physis rarely
leads to a good result. How­ever, if the bridge
does not increase in size du­ring a period of
growth (diametric area enlarge­ment), resection
may become feasible when the increased area
of the normal physis effectively decreases the
relative size of the bridge.
Young et al, used computed tomographic
scans to define the extent of coronal or
sagital arrest lines, which may be difficult
by conventional means(33). However, they
felt that computed tomographic scanning did
not have a place in the routine evaluation of
partial growth-plate arrest. Physeal tethering

may be recognized on compu­ted tomographic
scans by the obliteration of the low-density
physis by osseous bridges.
Magnetic resonance imaging may
demarcate the dense, sclerotic bone of the
partial physeal arrest quite effectively. Specific
delineation may requiere “non-standard”
pulse sequence selection that gives the
greatest contrast between physeal cartilage
and contiguous trabecular bone. This will
effectively isolate the bridge as dense bone
comparable to cortical bone. The technique
may also allow delineation of bridging prior
to its osseous phase.
Langenskiöld reported the first case
of osseous bridge resection in a human in
1967(9). He exci­sed the osseous bridge in the
proximal tibia and filled the surgical defect
with autogenous fat. There was a 10-degree
imporvement in the genu recurvatum, but there
was no evidence of signi­ficant longitudinal
growth restoration. Multiple succesful cases
with restoration of longitudinal growth have
since been reported(2-4,10-12,17,24,26-28,30-32).
The basic objective of such surgical
excision is to remove the osseous bridge
while preserving as much normal physis
as possible. This is best accomplished by
careful preoperative evaluation, planning
and familiarity with the surgical approa­ches to
various physes(1,4,5,30). Surgery be­comes more
complicated when the bridge is irre­gular.
To effectively accomplish bridge resection,
an operating microscope or magnifying loupes
are useful. The osseous bridge may be removed
using various tools-saw, osteotome, curette,
rongeur, and motorized burr. Radiography
(image inten­sification) during resection is
hepful to delinate both the location of the
bridge and the extent of removal as surgery
progresses. However, direct observation of
opaque white physeal tissue along the margins
of the resection is the best evidence of removal.
Further, observation of the exposed metaphysis
and epiphyseal ossification center should
The biology and treatment of physeal arrest
reveal normal “spongy” trabecular bone, not
the dense sclerotic bone of extension of the
osseous bridge into metaphysis and epiphyseal
ossification center.
A peripheral bridge should be approached
di­r ectly, exposing the often palpable
prominence that locates the site. The extension
of periosteum overlying the bridge must be
excised completely. Under direct vision, as well
as image intensifica­tion, the dense sclerotic
bridge is progressively removed from outside
to inside until normal phy­sis is visualized all
along the periphery of the ca­vity. The exposed
white physis should be evident out to the
cortical edges at either side of the sur­gical
defect (Fig. 4).
A linear bridge extending through the
physis requires careful evaluation of the
tomograms to determine the most appropriate
surgical approach to ensure complete removal
of the bar while still leaving viable physis on
either side. Creation of a tunnel through the
bone may be the best ap­proach, provided that
there is sufficient physis on either side. If there
is a small amount of phy­sis on one side, it may
be more realistic to treat the arrest similar
to the method described for the peripheral
bridge. Fluoroscopy helps in the selec­tion of
an appropriate area to begin tunneling.
A central bridge surrounded by normal
phy­sis and with an intact perichondrial zone
of Ran­vier should be approached through a
surgically created defect in the metaphysis (Fig.
5). This transmetaphyseal approach involves
removal of a segment of cortical bone followed
by removal of internal cancellous metaphyseal
bone until the physeal bridge is reached. This
is done by direct vision and fluoroscopy. After
removal of the en­tire bridge, the normal physis
must be visualized circumferentially within
the cavity. It may be as­sessed by the use of a
small dental mirror. An intracavity light may
also be heplful.
Some undermining of the metaphyseal and
epi­physeal bone away from the physeal edges
289
J.A. Ogden
may reduce the likelihood of reformation of the
brid­ge. Reformation of a bridge is less likely
when the interposition material remains in
the epiphy­seal ossification center than when
the epiphysis grows away from it, leaving it
only in the meta­physeal cavity.
Several interposition materials have been
recom­m ended: fat, methylmethacrylate,
silicone rubber, and cartilage(18,27,28). Lee et
al, in rabbit ex­periments, found that a physeal
graft from the iliac apophysis was superior to
silastic as an in­terposition material, and that fat
gave the poor­est results(14,15). My preference for
an inter­position material is autologous fat(27,28),
which may impair osteogenesis(18). It certainly
may be found intact, if not “enlarged” if the
area is re­explored(13). Enough fat is usually
available from the edges of the incision to fill
the defect. How­ever, additional fat may have
to be obtained from another site. Fat does
not provide hemostasis from the trabecular
seepage into the cavity. When the tourniquet
is released, the fat may be slightly displaced
from the physeal edges by such blee­ding.
Closure of the periosteum over the cavity
290
Figure 4. Resection of peripheral
osseous bridge. A) Location
of bridge, which may or may
not be covered by epiphyseal
cartilage. B) Resection of block
of bone containinf the bridge.
C) Curettage of margins to
demarcate the physis. D) Gap
filled with fat.
to contain the fat may predispose to new
peri­pheral bone formation, especially when
the pa­tient has a peripheral or linear bridge.
The interposition material should fill the
defect in the epiphyseal ossification center,
about the exposed physis, and then fill some,
if not all, of the metaphyseal cavity. If a
large metaphyseal cavity has been created,
especially during the ex­posure for a central
bridge, the remainder of the metaphyseal
cavity may be filled with the bone that
was removed to create that exposure and
the cortical metaphyseal window may be
repla­ced. However, any cortical bone that
originally traversed the growth plate must
not be reinser­ted. Similarly, the metaphyseal
periosteum may be reapproximated, but any
periosteum that cros­ses the physis must be
excised completely and not reattached. The
operative defect may predispose the bone to
fracture, since the fat provides no intrinsic
stability. Gradual ossification may oc­cur within
the cavity(21).
Mild angular deformity secondary to a
periphe­ral bridge has the potential to correct

sponta­neously with growth, especially if the
increased angulation is in the plane of motion.
Any angu­lar deformity of more than 20 degrees
probably will not correct spontaneously and
usually requi­res osteotomy. This may be
performed at the sa­me time as excision of the
bridge, or it may be done later. I prefer to wait
several months to see if the resection of the
bridge is going to lead to some restoration of
longitudinal growth. If there is any evidence
of bridge reformation, then the bridge may
be removed again during the correc­t ive
osteotomy. An osteotomy sometimes facili­
tates direct exposure, especially of a central
brid­ge(21).
Distraction epiphyseolysis may be used
to break the osseous bridge. If multiaxial
fixation (e.g., llizarov device) is used, the
surgeon may simul­tanteously address the
correction of the longitu­dinal and angular
deformities(4). This technique allowed some
improvement, but should be con­s idered
principally for adolescent patients who
The biology and treatment of physeal arrest
Figure 5. Resection of central
osseous bridge. A) Removal of
cortical window. B) Curettage
of bridge through metaphyseal
cavity. C) Removal of bridge
extension into the epiphyseal
ossification center. D) Cavity
filled with fat.
are approaching skeletal maturity in the
physis (assess the contralateral side)(4). This
assess­ment is necessary since the process is
associated with premature closure, compared
to the oppo­site side, even when growth is
seemingly res­tored .
Postoperative weight-bearing should be
defe­rred for eight to twelve weeks, especially
when fat has been used for the implantation.
The length of time must be individualized
based on the lo­cation, the size of the defect, the
age of the pa­tient, and the estimated strength
of the remaining bone(21).
The patient should be followed clinically
and radiographically until skeletal maturity.
Even when re-established, physeal growth
may cease at any time, and generally still
stops sooner than the opposite side. The
physis at the opposite end of a bone that
has been operated on sometimes overgrows
to compensate for the damage at the other
end(11). Peterson showed that the growth of
the involved bone compared with that of
291
J.A. Ogden
the contralateral side ranged from 0 to 200%,
with an average of 94%(26-28). In patients who
whe­re followed to skeletal maturity, the mean
value was 84%.
Recurrent formation of a bridge has been
trea­ted by repeat excision. If a bridge recurs
when the patient is near maturity or if the
entire physis ceases growing on the injured
side earlier than on the contralateral side (a
fairly frequent finding), physeal arrest of the
contralateral side should be considered.
ACKNOWLEDGEMENTS
The author gratefully acknowledges the
sup­port of the Shriners Hospital for Crippled
Chil­dren, the Skeletal Educational Association
and the Foundation for Musculoskeletal
Research and Education for ongoing basic and
clinical research in growth-plate development
and injury.
REFERENCES
1. Birch JG, Herring JA, Wenger DR. Surgical
anatomy of selected physes. J Pediatr Orthop
1984;4:224-231.
2. Bright RW. Operative correction of partial epiphy­
seal plate closure by osseous-bridge resection and
sili­cone-rubber implant. An experimental study
in dogs. J Bone Joint Surg 1974;56A:655-664.
3. Broughton NS, Dickens DRV, Cole WG, Menelaus
MB. Epiphysiolysis for partial growth arrest. J
Bone Joint Surg 1989;71B:13-16.
4. Cañadell J, De Pablos J. Breaking bony bridges
by physeal distraction. A new approach. Internat
Or­thop 1985;9:223-229.
5. Carlson WO, Wenger DR. A mapping method to
prepare for surgical excision of a partial physeal
arrest. J Pediatr Orthop 1984;4:232-238.
6. De Campo JF, Boldt DW. Computed tomography
of partial growth plate arrest. Initial Experience.
Skel Radiol 1986;15:526-529.
292
7. Harcke HT, Macy NJ, Mandell GA, Mace­wen GD.
Quantitative assessment of growth plate activity.
J Nucl Med 1984;25:115.
8. Klassen RA, Peterson HA. Excision of physeal bars:
The Mayo Clinic experience 1968-1978. Orthop
Trans 1982;6:65.
9. Langenskiöld A. The possibilities of eliminating
pre­m ature partial closure of an epiphyseal
plate caused by trauma or disease. Acta Orthop
Scandinavica 1967;38:267-279.
10. Langenskiöld A. Partial closure of the epiphyseal
plate. Principles of treatment. Internat Orthop
1978;2:95-96.
11. Langenskiöld A. Surgical treatment of partial clo­
sure of the growth plate. J Pediatr Orthop 1981;1:3-
11.
12. Langenskiöld A, Osterman L. Surgical treatment
of partial closure of the epiphyseal plate. Reconstr
Surg and Traumat 1979;17:48-64.
13. Langenskiöld A, Videman T, Nevalainen T. The
fate of fat transplants in operations for partial
clo­sure of the growth plate. Clinical examples
and an ex­perimental study. J Bone Joint Surg
1986;68B:234­238.
14. Lee EH, Gao GX, Bose K. Expermental studies
on the prevention of growth arrest in immature
rabbits. J Bone Joint Surg 1989;71B:726.
15. Lee EH, Gao GX, Bose K. Management of partial
growth arrest: physis, fat or silastic? J Pediatr
Orthop 1993;13:368-372.
16. Lennox DW, Goldner RD, Sussman MD. Car­tilage
as an interposition material to prevent transphy­seal
bone bridge formation: An experimental model.
J Pediat Orthop 1983;3:207-210.
17. Mallet J. Les epiphysiodeses partielles traumatiques
de l’extremete inferieure du tibia chez l’enfant.
Leur traitment avec desepiphysiodese. Rev Chir
Orthop 1975;61:5-16.
18. Montgomery WW, Van Orman P. The inhibitory
effect of adipose tissue on osteogenesis. Ann Otol
Rhi­nol Laryngol 1967;988-997.

19. Ogden JA. Injury to the growth mechanisms of
the immature skeleton. Skel Radiol 1981;6:237-253.
20. Ogden JA. Skeletal growth mechanism injury
pat­terns. J Pediatr Orthop 1982;2:371-377.
21. Ogden JA. Current concepts review. The evaluation
and treatment of partial physeal arrest. J Bone
Joint Surg 1987;69A:1297-1302.
22. Ogden JA. Skeletal Injury in the Child. Philadelphia:
W B Saunders, 1990 (2nd ed).
23. Ogden JA, Grogan DP, Light TR. Postnatal skeletal
development and growth of the musculoske­
letal system. In: Albright J A and 8rand R A.
The Scientific Basis of Orthopaedics. New York:
Century Crofts, 1987 (2nd ed);91-160.
24. Österman K. Operative elimination of partial
prema­ture epiphyseal closure: An experimental
study. Acta Orthop Scandinavica 1972;
supplementum 147.
25. Peterson CA, Peterson HA. Analysis of the
in­cidence of injuries to the epiphyseal growth
plate. J Trauma 1972;12:275-281.
26. Peterson HA. Operative correction of post-
fractu­r e arrest of the epiphyseal plate. Case
report with ten­year follow-up. J Bone Joint Surg
1980;62A:1018­-1020.
The biology and treatment of physeal arrest
27. Peterson HA. Growth plate arrest and its treatment.
J Pediatr Orthop 1984;4:246.
28. Peterson HA. Partial growth plate arrest and its
treatment. In: Lovell W W and Winter R B. Pediatnc
Orthopaedics. Philadelphia: J B Lippincott, 1985
(2nd ed);1083-1101.
29. Salter RB, Harris WR. Injuries involving the
epi­physeal plate. J Bone Joint Surg 1963;45A:587-
622.
30. Vickers DA. Premature incomplete fusion of the
growth plate: causes and treatment by resection
(physiolysis) in fifteen cases. Aust New Zeal J Surg
1980;50:393-401.
31. Visser JD, Nielsen h k L. Case report. Operative
correction of abnormal central epiphyseal
plate closu­re by transmetaphyseal bone-bridge
resection and im­plantation of fat. Netherlands J
Surg 1981;33:140­145.
32. Williamson R V, Staheli L T. Partial physeal
growth arrest: treatment by bridge resection and
fat interposition. J Pediatr Orthop 1990;10:769-76.
33. Young JWR, Bright RW, Whitley NO. Com­puted
tomography in the evaluation of partial growth
Dlate arrest in children. Skel Radiol 1986:15:530-
535.
293
36 Bridge resection and interposition of
substances
A. Langenskiöld
GENERAL REMARKS
Premature partial closure of a growth plate
may occur after trauma, after osteomyelitis,
in cases of neglected Blount’s disease and in
some congenital anomalies.
The indications and possibilities for a good
result can generally be readily determined
by common radiography and CT-scanding
in posttraumatic cases. However, when a
bone bridge has been formed as a sequel of
osteomyelitis radiolucent scar tissue present
in the growth plate area may give a wrong
idea of the amount of viable cartilage tissue
remaining (Langenskiöld, 1981).
In neglected infantile tibia vara or Blount’s
disease a bone bridge usually comprises a
large peripheral segment and resection is
seldom indicate (Langenskiöd, 1989). Vickers
and Nielsen (1992) have successfully treated
Madelung deformity by bridge resection and
implantation of fat. This operation has also
restored growth in the inherited order of delta
phalanx (Vickers, 1987).
A detailed description of the operative
technique was given by Langenskiöld and
Österman in 1983. Here it will be described
by Österman. Some rules should be stressed.
The fundamental principles of transplantation
surgery must be followed:
1. No drying of tissue surfaces.
2. No haematoma.
3. No oozing of blood.
294 Reprinted with permission of Mapfre Medicina (vol. 4, suppl 2)
In order to achieve complete haemostasis
before implantation of a free fat graft we have
used topical thrombin-solution. Vickers (1980)
has pressed bone wax in bleeding points
which can be recommended. He also pointed
out that bridging may be multifocal at the
periphery of the major component. We have
not always used an operative microscope but
this aid has at every operation been ready for
use. Anyhow, the resection should be radical
and complete.
Small peripheral bridges cause rapid
progression of angular deformity but rapid
correction by growth is seen after operation.
Common radiographs may give a wrong idea
of the size of a bridge. When pictures of an
epiphyseal region apparently show in two
projections that in the linear projection 50%
of the growth plate is occupied by a bony
bridge, the actual loss of area of the plate is
only 25%.
A thick layer of cortical bone compensates
for the loss of strength caused by the presence
of a large cavity in the metaphysis after
resection of a large central bridge. Therefore,
large centrally situated bone bridges taking
up as much as 50% of the area of the growth
plate should not be left untreated for fear that
the bone may be weakened by the operation
(Langenskiöld et al, 1987).
Fatty tissue can be well identified by means
of CT-scanning on the basis of its density in

Hounsfield units. In two adult patients the
fat grafts, enlarged during the growth period,
remained as adipose tissue for years. In a third
patient the elongation of the graft and partial
regeneration of the growth plate could be
demonstrated by CT-scanning (Langenskiöld
et al, 1987).
When we started using adipose tissue as
an interposition material it was on the basis of
Lexer’s extensive work which had shown that
free fat transplants stay viable and prevent
scar formation. When our own experience
both from experiments and clinical cases
has shown that a free autologous fat graft,
properly transplanted, is not an inert but a
living material we have continued its use.
In 1980 Baeza and Oliete published a study
in 123 rabbits on the effect of interposition
materials in prevention of growth disturbance.
Fat was found superior to silastic, and bone
cement caused more growth disturbance than
a haematoma.
The classic treatments, osteotomy,
epiphyseodesis, leg shortening and leg
lengthening cannot prevent deformity of
the joint surface and resulting osteoarthritis.
It seems therefore that the use of bone bridge
resection and implantation of an interposition
substance will not be a temporary phe-
nomenon.
Bridge resection and interposition of substances
REFERENCES
- Baeza V, Oliete V. Profilaxis de los puentes 6seos
del cartilago de crecimiento. Estudio experimental.
Rev Ortop Traumatol 1980;24:305.
- Langenskiöld A. Surgical treatment of partial
closure of the growth plate. J Pediatr Orthop 1981;1:3.
- Langenskiöld A. Tibia vara. A critical review.
Clin Orthop 1989;246:195.
- Langenskiöld A, Österman K. Surgical elimination
of post-traumatic partial fusion of the growth
plate. In: Houghton G R and Thompson G H.
Buttenrvorths International Medical Reviews,
Orthopedics 1. Problematic Musculoskeletal Injuries
in Children. London: Butterworths, 1983.
- Langenskiöld A, Österman K, Valle M. Growth of
fat grafts after operation for partial bone growth
arrest: Demonstration by computed tomography
scanning. J Pediatr Orthop 1987;7:389.
- Vickers D W. Premature incomplete fusion
of the growth plate: Causes and treatment by
resection (physolysis} in fifteen cases. Aust N Z
Surg 1980;50:393.
- Vickers D W. Clinodactyly of the little finger: a
simple operative technique for reversal of the
growth abnormality. J Hand Surg 1987;12B:335.
- Vickers D W. Madelung deformity: Surgicai
prophylaxis (physiolysis) during the late growth
period by resection of the dyschondrosteosis. J
Hand Surg 1992;17B.
295
37 Operative treatment of partial premature
epiphyseal closure
K. Österman
Removal of the bone bridge between the
epiphysis and the metaphysis and prevention
of its reappearance by using fat graft was
a new principle in pediatric orthopaedics
when presented first in 1967 by Langenskiöld.
Clinical experience gained since that has
proved that the operation must be carried
out according to systematic principles even
though the type, size and site of the bridge
varies individually much. As pointed out by
Langenskiöld (1979, 1981) and Langenskiöld
and Österman (1979, 1983) removal of the
bridge is not indicated only to restore the
longitudinal growth and to prevent the
angular deformity. In many cases it is also
indicated to prevent deformity of the joint
surfaces. The details of the operation were
presented by Langenskiöld (1975) after
experimental research by Österman (1972).
PRIMARY TREATMENT OF
EPIPHYSEAL INJURIES
Exact reposition of fractures crossing the
epiphyseal plate is important. Open reduction
and fixation may be necessary. Fixation material
crossing the epiphyseal cartilage should be
avoided. In case of crush injuries it may be
necessary to remove the loose fragments and
fill the cavity primarily with a free fat graft.
Clinical and radiological follow-up of these
296 Reprinted with permission of Mapfre Medicina (vol. 4, suppl 2)
injuries is important because the deformity
often develops slowly during several years.
REMOVAL OF THE BONE BRIDGE
OPERATIVELY
Preoperative planning
Plain radiograms and comparison with the
opposite side give usually the diagnosis. We
pay attention to the growth plate, the growth
asymmetry as presented usually by Harris
line, shortening bone contours of the joint
and especially the sclerotic bone in the region
of the injury. In the preoperative planning
conventional tomograms in two directions
give the best information about the size and
site of the bridge but CT or MRI can also give
us useful information in certain conditions.
Estimation of the skeletal age and the amount
of growth potential must also be taken into
consideration.
Operation technique
The operation is carried out using
tourniquet. In addition to the conventional
bone instruments, burr heads of different
sizes are needed. Binocular loupe or operation
microscope is often necessary and in some
cases arthroscope is needed to see behind the
corner. At the end of the operation small metal
markers are inserted into the epiphysis and
 Operative treatment of partial premature epiphyseal closure
the metaphysis for further measurements of
growth. It is important to check the primary
result of the operation also radiologically. Fat
transplant is inserted after strict haemostasis
into the cavity. The fat graft is usually taken
from the gluteal region.
Removal of the peripheral bridge
It is important to find out both corners
of the bridge. Usually palpation using a thin
hypodermic needle is necessary because the
remnants of the perichondrial ring cover
the peripheral part of the bridge. Bone is
removed radically without injuring the growth
plate. It is important to remove all sclerotic
deformed bone from the metaphysis and the
epiphysis and the bone is removed so that the
bluish epiphyseal cartilage becomes visible
and is slightly bulging compared with the
surrounding bone. Thus the primary contact
between the fat graft and the cartilage is
good. If the bony union has developed after
a fracture the border between the growth
plate and the bridge is usually clear but if
the bridge has developed after an infection
the growth line seen in the radiogram may
be partly replaced by a scar tissue which is
not capable to grow but can cause deformity
and should be removed. On the other hand,
sometimes there are islands of active cartilage
inside the bone bridge, which may confuse
the finding during the operation.
Removal of the central bridge
A centrally located bridge is removed
through the metaphyseal approach.
Preoperative evaluation of the lesion is
important to find out the best location for
the metaphyseal window.
In these cases the identification of the
sclerotic bone area and Harris line during
operation often give good landmarks. In order
to visualize the growth plate it is important to
use an arthroscope and radiological imaging
during the operation. When inserting the fat
graft the cavity is filled with small pieces of
fat to be sure that the epiphyseal area is in
good contact with the graft.
Postoperative care
Free mobilization of the joint and full
weight bearing is allowed immediately. In one
case only where a large postinfections bridge
was removed and the bone was osteoporotic
a slight compression fracture was observed
in the operation area. All posttraumatic cases
have started with full weight bearing without
any secondary fractures. Postoperative clinical
and radiological controls 2-3 times a year are
necessary to the end of the growth period. In
case of recurrence of the bridge reoperation
may be indicated. Additional procedures
e.g. epiphyseodesis of the opposite side or
correction osteotomy and lengthening of the
affected bone may be indicated.
CLINICAL MATERIAL
A total number of 54 patients were o
perated on at the Orthopaedic Hospital of
the Invalid Foundation from 1967 to 1990.
The distal femoral epiphysis was affected in
22 patients, the proximal tibia in 12 and the
distal part of the tibia in 9 patients. Other
locations were less common. The age of the
patients at the time of operation was 2-16 years.
Etiology was posttraumatic in 35 patients. In 14
patients the cause was osteornyelitis, Blount’s
disease in three and other reason in two. Free
fat transplant was used in all patients. In one
osteomyelitic case the transplant was removed
after postoperative reinfection. Lengthening
and correction of the residual angulation
deformity was carried out in three patients.
DISCUSSION
Removal of the bridge and prevention
of its reappearance allows the regeneration
of the growth plate and often the residual
297
K. Österman
growth potential is able to correct the deformity
and restore a sufficient longitudinal growth.
Modern possibilities of bone lengthening can
be used but these operations are heavier and
the risk of complications is common. However,
the removal of the bridge is the only way to
prevent the joint deformity during the growth
period and the removal of the bridge is often
indicated for that reason even if the remaining
growth period is short.
REFERENCES
Langenskiöld A. The possibilities of eliminating
premature partial closure of an epiphyseal plate
caused by trauma or disease. Acta Orthop Scand
1967;38:267-269.
298
Langenskiöld A. An operation for partial closure of
an epiphyseal plate in children and its experimental
basis. J Bone Joint Surg 1975;57B:325-330.
Langenskiöld A. Surgical treatment of partial
closure of the growth plate. J Pediatr Orthop
1981;1:3-11.
Langenskiöld A, Österman K. Surgical treatment
of partial closure of the epiphyseal plate. Reconstr
Surg Traumatol 1979;17:48-64.
Langenskiöld A, Österman K. Surgical elimination
of posttraumatic partial fusion of the growth plate.
Problematic musculoskeletal injuries in children.
Butter-worths lnt Med Rev Orthop l983;1:14-31.
Österman K. Operative elimination of partial
prernature epiphyseal closure. An experimental
study. Acta Orthop Scand 1972; suppl 147.
38 Treatment of physeal bony bridges
by means of bridge resection and
interposition of cranioplast
H.A. Peterson
BAR EXCISION: EXPERIMENTAL
Several investigators have performed
animal experiments creating a physeal
bar at a first operation, allowing the bar to
develop, excising the bar and inserting an
interposition material at a second operation,
and later sacrificing the animal to observe
the result. Although the results have been
varied, there has been enough success to
confirm that a bar can be successfully excised
and growth reestablished. Interposition
materials used include nothing, gold foil,
bone wax, fat, cartilage, silicone rubber,
methylmethacrylate and Cranioplast. When
no interposition material is inserted a bone
bar promptly reformed in every instance.
Because of variables in the experiments it
is difficult to determine superiority of one
interposition material over another.
Cartilage may be superior. Possible sources
of cartilage are another physis, an apophysis
such as the iliac crest, and laboratory procured
chondrocyte allograft transplants. There are
technical difficulties procuring and inserting
another physis. Apophyseal cartilage may not
have the same growth potential as epiphyseal
cartilage. Chondrocyte allograft transplants
require initial cartilage procurement followed
by laboratory time for the cartilage matrix
to develop. There will be immune response
problems if the intention is to transfer
Partly reprinted with permission of Mapfre Medicina (vol. 4, suppl 2)
the material from one human to another.
Nevertheless, since cartilage is the damaged
tissue, cartilage would be the ideal interposition
material. Hopefully more investigations will
solve this problem in the future.
A load sharing interposition material, such
as Cranioplast, may be superior in resection
of large bars in weightbearing areas.
A study in rabbits suggested that
reformation of a bar after excision can be
inhibited by the use of oral indomethacin
without the use of an interposition material.
Indomethacin has been shown to produce a
nonspecific inhibition of osteoblastic activity
that is triggered by fracture or postoperative
inflammation. No clinical trials using oral
indomethacin in conjunction with bar excision
has been reported in humans. Whether
indomethacin can be given in sufficient doses
in humans to prevent bone bar reformation
without inhibiting normal bone growth
remains to be seen.
BAR EXCISION: HUMAN
The first case in a human was reported
by Langenskiöld in 1967 (1). This was in a
15-year-old boy with genu recurvatum
secondary to a bone bar in the anterior
proximal tibia; the etiology was unknown.
The bone bar was excised and the space
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H.A. Peterson
was filled with autogenous fat. During
the 1.5 year follow-up the angle of genu
recurvatum improved 10˚, but there was no
documentation of longitudinal growth. The
first case documenting longitudinal growth
was performed in the distal tibia of a 5 year old
boy in 1968(4). During a 10 year follow-up the
involved tibia grew 16.7 cm. Sheet Silastic and
Gelfoam were used as interposition materials.
Multiple series of cases have since been
reported in which several different interposition
materials were utilized. Fat, bone wax and fat,
Silastic, Cranioplast and methylmethacrylate
are the most popular. There are not enough
cases followed to maturity in these studies
to determine superiority of one interposition
material over the others.
TECHNIQUE
The objectives of surgical excision of a
bone bar are two fold; to remove the bar
completely and to preserve as much of the
normal remaining physis as possible. This
requires knowledge of surgical anatomy and
careful preoperative evaluation and planning,
and may be difficult if the bar is irregular
or the epiphyseal-metaphyseal complex is
deformed. The preoperative evaluation is
significantly enhanced by magnetic resonance
imaging (see Part I, Chapter 4).
Physeal bars may be grouped into one of
three types, based on location and contour: 1)
peripheral, 2) linear, longitudinal, or elongated,
and 3) central(5,7,9).
Peripherally located bars should be
approached directly from the periphery
(Fig. 1). Periosteum overlying the bar
should be excised to prevent subsequent
bar reformation. Under direct vision the
bar is removed until normal physis can
be visualized on all sides of the cavity.
Accessory head lamp light and/or optical
loupes are helpful. The bone bar may be
removed by using an osteotome, curette,
300
Figure 1. Peripheral bar shown in anterior posterior
view (above) with transverse section through physis
(below). A) (With cross-hatched area) computed
from tomograms or MRI. B) Bar excised by direct
approach.
and rongeur, but is most precisely removed
with a motorized burr. This allows excellent
visualization of the physis, removal of as
little normal physis and metaphyseal bone as
necessary, and facilitates contouring of the
cavity in the epiphysis. Heat generated by
the burr has no apparent deleterious effect
on the viability of the remaining physis.
A bar that extends completely across the
physis is referred to as a linear, longitudinal
or elongated bar. These bars require careful
preoperative evaluation to determine surgical
approach and to ensure complete removal of
the bar (Fig. 2).
Centrally located bars have normal physis
peripherally and an intact perichondrial ring
of Ranvier (Fig. 3A). These bars should be
approached through the metaphysis by
removing a window of cortical bone and
cancellous metaphyseal bone to expose the
bar from “inside‑out” (Fig. 3B). This preserves
the perichondral ring of Ranvier. The sides of
the cavity should be flat and smooth. After
removal of the entire bar, the normal physis
must be visualized circumferentially in the
cavity. This is best accomplished by the use of
 Treatment of physeal bony bridges by means of bridge resection and interposition of cranioplast

Figure 2. Elongated or linear bar extends from anterior to posterior surfaces (often occurs after Salter-
Harris IV fracture). Although the bars shown in A, B, and C have the same appearance on an anterior
posterior radiogram (above), they have different contours and areas on the transverse sections (below).
To achieve complete bar removal with retention of as much normal physis as possible, the bar in B
would optimally be approached posteriorly, and that in C anteriorly.

Ultraviolet visualization of Tetracycline-

Figure 3. Central bar. A) Bar in center with growth
peripherally results in “tenting” or “cupping” of
the physis (this occurs after osteomyelitis, tumors,
internal fixation devices, and from metabolic
causes). B) Excision of the central bar through a
window in the metaphysis.
a small (5 mm diameter) dental mirror (Fig.
4A), or an arthroscope. There are reports of
the use of an operating microscope aiding
visualization of the bar. I have found this to
be too cumbersome to be useful.
labeled bone in rabbits has been reported to
allow complete excision of experimentally
created physeal arrests while minimizing
excision of normal physis.
Metal markers placed in the metaphysis
and epiphysis allow accurate radiographic
measurement of subsequent longitudinal
growth (Fig. 5). These markers also help
differentiate overgrowth of the physis at
the other end of the bone which may falsely
enhance the result. These markers should
be placed in cancellous bone, not in contact
with the cavity, because they might become
attached to the interposition material or,
if fat is used, they might dislodge into the
cavity. The markers should be in the same
longitudinal plane proximal and distal to the
defect. A position in the center of the bone is
preferrable since eccentric markers may become
extraosseous due to growth and metaphyseal
remodelling. Any metal marker will do; half of
a silver clip works nicely. Transversely oriented
Kirschner wires parallel with each other and
with the physis, one in the metaphysis and

301
H.A. Peterson
Figure 4. Technique. A) Visualization of normal physis using a dental mirror following complete bar
removal. B) Insertion of only enough Cranioplast, by use of syringe and catheter, to bridge all physeal
surfaces. C) Remainder of defect filled with pieces of bone previously removed.
one in the epiphysis, allow more accurate
assessment of angular growth (Fig. 6). Titanium
markers allow more clear subsequent MRI
evaluation if this is undertaken. Presently I
use 0.062 titanium break off wires.
Next, an interposition material is inserted
into the cavity. The object is to fill the cavity
to prevent blood from occupying the cavity,
organizing, and reforming a bone bar.
INTERPOSITION MATERIALS
As indicated in the previous sections on
“Bar Excision: Experimental” and “Bar Excision:
Human”, multiple interposition materials have
been used. Fat, bone wax and fat, Cranioplast,
and silastic, are the most popular.
Fat has the distinct advantage of being
autogenous(2). Langenskiöld prefers buttock
fat because of its more firm and globular
consistency. This requires a second incision.
No foreign material is inserted. Fat has the
disadvantage of lack of hemostasis in the
resected cavity. When the tourniquet is released,
fat tends to float out of the cavity. Closing
periosteum over the cavity to contain the fat
predisposes to new bone formation peripherally.
This is undesirable because it tends to tether
302
growth again. The operative defect weakens
the structure of the bone, and a cast is used to
protect a weight-bearing bone from fracture.
When fat grafts work well, the intraoperative
cavity enlarges as the bone (and fat graft) grow(3).
Postoperative fracture has been reported.
Misunderstandings concerning methyl-
methacrylate are somewhat related to
terminology. Pure methylmethacrylate,
trade name Cranioplast (Cranioplastic®,
manufactured by L. D. Caulk Co., Milford,
DE, distributed by Codman and Shurtleff,
Randolph, MA) has been used for over 5
decades by neurosurgeons to repair skull
defects and has been found to be an inert
and safe material. When used as an isolated
substance it has caused no rejection, infection,
or neoplastic change. Its thermogenic properties
are nil, as evidence by the neurosurgical
practice of pouring it in a semi-liquid form
directly on dura and brain tissue prior to
setting. It is also radiolucent.
When initial results from total hip
arthroplasty revealed prosthesis loosening,
a search for a “bone cement” was undertaken.
Cranioplast was found to work well, but
the radiolucent property made subsequent
prosthesis loosening difficult to detect. Barium
 Treatment of physeal bony bridges by means of bridge resection and interposition of cranioplast

Figure 5. Metal markers. A) Metal markers in cancellous bone of metaphysis and epiphysis, away
from the interposition plug and longitudinally oriented to each other. B) The plug has stayed in the
epiphysis, which grows away from the proximal marker and the growth arrest line which remain in
the metaphysis. C) The plug stayed in the metaphysis as the epiphysis grew.

was added to the methylmethacrylate. This
achieved radiopacity, but decreased the setting
time and increased the exothermic property
significantly. Thus, the material that is now
generally referred to as “methylmethacrylate”
is in fact, Cranioplast with barium added.
This “methylmethacrylate” is undesirable
as an interposition material for bar excisions
because it is radiopaque and possibly because
of its exothermic reaction. The radiopacity
obviates detection of recurrent bar formation.
For an interposition material, Cranioplast
has several advantages: it is easily available
and inexpensive, there is no FDA control
(as for Silastic), and no second incision is
needed (as for fat). It is light, easy to handle
and mold, thermally nonconductive, and
radiolucent. Both the liquid (monomer) and
the powder (polymer) are sterile as packaged
and may be mixed in the operating room. It
is unnecessary to take cultures. It provides
hemostasis (by virtue of occupying the entire
desired portion of the cavity), and it is strong
so that no postoperative immobilization is
necessary. There are no apparent side effects.
It may be the material of choice to support
the epiphysis after excavation of a large bar,
which might otherwise be prone to fracture.
In a cavity that is gravity dependent,
cranioplast can be poured in a liquid state.
If the cavity is not in a dependent position,
the cranioplast may be placed in a syringe
and pushed into the defect through a short
polyethylene tube (Fig. 4B). Or the cranioplast
can be allowed to set partially into a putty-like
state and then be pushed into the defect. As little
cranioplast as possible should be allowed to
remain in the metaphysis. After the cranioplast
has set, the remainder of the metaphyseal cavity
should be filled with cancellous bone previously
removed (Fig. 4C).
Silastic has many properties similar to
Cranioplast, but has had little use since its
withdrawal from commercial markets by
Dow Corning in 1987.
Mild angular deformity secondary to
peripheral bars may correct spontaneously
with growth after excision of the bar. Angular
deformities greater than 20˚ will probably not
correct spontaneously and usually require
osteotomy. This may be performed at the
same time as bar excision or later.

303
H.A. Peterson

A B C
Figure 6. Infant girl had hematogenous staphylococcal osteomyelitis of distal right femur at age 17 days
of life. A) Physeal bar and remaining physis are well visualized on anterior posterior hypocycloidal
tomogram at age 4 years 11 months. B) Five months after bar excision and insertion of Cranioplast
close‑up of scanogram shows the physis is open. The faintly increased sclerosis in the metaphysis adjacent
to the physis represents longitudinal growth evenly along the physis. The two Kirschner wires inserted
at the time of bar excision are now 28 mm apart. The genu valgum (femoral shaft-tibial shaft) angle are
unchanged. Note that the lucency of the Cranioplast is very close to the proximal marker, as well as the
physis. C) Close-up of scanogram 4 years postoperatively. Both right and left femur had grown 9.8 cm
from time of surgery (growth on right equals 100% of left). The metal markers are 83 mm apart, and
because this measurement is taken from a scanogram, there is no magnification of distance between
the two metal markers. Note that the Cranioplast plug initially stayed with the epiphysis (as evidenced
by increased distance from proximal marker; compared with B). Later the epiphysis grew away from
the Cranioplast (as evidenced by increased distance of plug from distal marker; compare with B). The
genu valgum and orientation of the pins to each other is unchanged. The ultimate growth as evidenced
by the distance between the metal markers was 10.9 cm. Though this was a great benefit to the patient
(a surgical success) the involved femur stopped growing sooner than the normal contralateral femur
which was then treated by surgical physeal arrest.

Postoperatively, if cranioplast is inserted formation has been successfully treated by

and no osteotomy performed, no cast or other
immobilization is necessary. Joint motion
and weight bearing are encouraged on the
day of operation, or as soon as operative
discomfort subsides. There have been no
complications from the long term presence
of Cranioplast in the body and its removal
is not necessary.
FOLLOW-UP
Re-established physeal growth may cease at
any time and frequently does so as the patient
approaches maturity. Therefore, follow-up
until maturity is mandatory. Recurrent bar
re-excision of the bar.
Scanograms are the most precise way to
measure the increasing distance between the
two metal markers(6). As the child grows, the
increasing length of the extremities allows
magnification of the distance between
the markers on regular roentgenograms,
teloroentgenograms, and orthoroentgenograms.
The magnification of these radiographic
measurements falsely enhances the result.
Scanograms have no magnification.
RESULTS
Assessment of results is difficult because

304
 Treatment of physeal bony bridges by means of bridge resection and interposition of cranioplast

Table 1. Physeal bridge resection 1968-1996. are undesirable and because the procedure
Distribution* occasionally works. The bar excision does
not preclude the use of all other methods of
No. %
limb length management.
Distal femur 61 34 From 1968 through 1996, 178 cases were
Distal tibia 52 29 treated by bar excision at the Mayo Clinic (Table
Proximal tibia 29 16 1). Cranioplast was used for the interposition
Proximal femur 2 1 material in 153 cases, fat in 13 cases, methyl
Distal fibula 2 1 methacrylate in 1 case, and sheet Silastic and
First metatarsal 2 1
Gelfoam in 1 case (this was the first case and
Proximal phalanx, great toe 2 1
has been reported(4)). The percentage of growth
Distal radius 15 9 of the bone operated on compared with the
Distal ulna 5 3 growth of the contralateral normal bone has
Proximal humerus 3 2 varied from 0% to 200%.
Phalanges (fingers) 2 1 Lesions of the larger physes did the best
Metacarpal 1 0.5
and were the easiest to accurately determine
Pelvis (tri-radiate) 1 0.5 the result because of the use of scanogram.
178 99 Ninety-eight patients with lesions of the distal
femur (43), proximal tibia (18), and distal tibia
* Bar re-excisions not included (37), had reached maturity.
Of the 43 distal femur lesions, 30 were
male and 13 female. The interval between
so many factors are involved. When the injury and bar excision was 2.8 years and
procedure works well, it is most gratifying. the average age at the time of bar excision
This renewed growth may diminish the was 10.5 years. The area of bar was >45%
angular deformity and the rate of progression in 11, >30% in 12, and <30% in 20. The site
of limb-length inequality. Occasionally, there of the lesion was medial (13), lateral (11),
may even be reduction of the length inequality central (10), posterior (9), and anterior (6)
(the treated limb grows faster than the normal (some lesions occupied more than one locus).
limb). Five patients obtained no growth from the
Only cases followed to maturity should bar excision. In the remaining 38 patients
be included in any reported series. Some the operated side grew 78% as compared
operated physes, although growing well with the normal side. Additional procedures
after the procedure, close earlier than their included epiphyseodesis (23), osteotomy (11),
contralateral physes. Thus, in some of these and lengthening (9). There were 9 recurrent
cases, surgical arrest of the contralateral physis bars and 2 infections (The cause of the bar in
is performed toward the end of growth to these two was osteomyelitis).
negate additional discrepancy. This favorably Of the 18 proximal tibial lesions, 9 were
enhances the result of bar excision expressed male and 8 female. The interval between injury
as a percentage. and surgery was 2.1 years and the average
Excision of bars constituting 50% or more age at time of surgery was 11.7 years. The
of the entire physis usually fails to restore area of the bar was >45% in 2, >30% in 1, and
satisfactory longitudinal growth. Bars larger <30% in 15. The site of the arrest was central
than 50% of the physis may be excised in (6), lateral (5), medial (4), anterior (4), and
very young children because the alternatives posterior (1) (some lesions occupied more

305
H.A. Peterson
than one locus). The average growth of the
operated side was 88% of the uninjured side.
Additional procedures included osteotomies
(11), epiphyseodesis (9), and lengthening (3).
There were 2 recurrences and 1 infection (The
cause of the bar in this case was osteomyelitis).
Of the 37 distal tibial lesions, 26 were male
and 11 female. The interval between injury
and surgery was 1.9 years and the average age
at time of surgery was 11.1 years. The area of
the bar was >45% in 3, >30% in 4, and <30%
in 30. The site of the bar was medial (14),
anterior (10), central (5), posterior (5), and
lateral (3). There was no growth in one patient;
the remainder averaged 93% as compared
with the unoperated side. Additional surgery
included physeal arrest (8), osteotomy (15),
and lengthening (1). There were 7 recurrent
bars, 2 fractures, and no infections.
CONCLUSIONS
1. Cranioplast is an effective interposition
material.
2. Radiographic imaging techniques and
types and materials of the metal markers
have changed over the years.
3. Though the operated physis usually
grows well (in the realm of 100%) for
months or years, it often stops growing
near maturity, slightly earlier than the
unoperated side. This diminishes the
overall result, emphasizes the need for
diligent follow-up until all physes are
closed, and sometimes requires additional
treatment such as physeal arrest of the
contralateral normal physis.
4. Additional procedures to correct alignment
and length discrepancy are often necessary,
not because the bar excision didn’t work,
but because the deformity or length
discrepancy was too great at the time of
bar excision. Parents need to be so advised.
5. Surgery, including bar excision, often
stimulates growth of the physis at the
306
opposite end of the bone. This affects the
overall result of the bar excision favorably.
ACKNOWLEDGEMENTS
The author thanks Dr. R. A. Klassen for
compiling the Mayo Clinic data results.
REFERENCES
Documentation for all statements in this
manuscript can be found in an extensive
bibliography in:
Peterson, H.A.: Physeal and Apophyseal Injuries.
In: Fractures in Children, 4th Edition, Vol. 3.
Rockwood, C.A. Jr., Wilkins, K.E., and Beaty, J.H.,
Ed., Philadelphia, Lippincott-Raven Publishers,
Chapter 6, pp 103-165, 1996.
Additional key references are as follows:
1. Langenskiöld A: The Possibilities of Eliminating
Premature Partial Closure of an Epiphyseal Plate
Caused by Trauma or Disease. Acta Orthop Scand
1967;38:267-279.
2. Langenskiöld A: An Operation for Partial Closure
of an Epiphyseal Plate in Children, and Its
Experimental Basis. J Bone Joint Surg 1975;57B:325-
330.
3. Langenskiöld A, Osterman K, Valle M: Growth
of Fat Grafts After Operation for Partial Bone
Growth Arrest: Demonstration by CT Scanning.
J Pediatr Orthop 1987;7:389-394.
4. Peterson HA: Operative Correction of Post Fracture
Arrest of the Epiphyseal Plate: Case Report with
10-Year Follow-Up. J Bone Joint Surg 1980;62A:1018-
1020.
5. Peterson HA: Partial Growth Plate Arrest and Its
Treatment. J Pediatr Orthop 1984;4:246-258.
6. Peterson HA: Scanning the Bridge. In: Behavior
of the Growth Plate. Uhthoff HK, Wiley JJ, eds.
New York, Raven Press, pp 247-258, 1988.
 Treatment of physeal bony bridges by means of bridge resection and interposition of cranioplast

7. Peterson HA: Partial Growth Plate Arrest. In: 9. Peterson HA: Management of Partial Physeal
Lovell and Winter’s Pediatric Orthopaedics, 3rd Arrest. In: Operative Orthopaedics, 2nd Ed., MW
Ed., Vol. 2. RT Morrissy MD, Ed, Philadelphia, JB Chapman MD, Ed, Philadelphia, JB Lippincott
Lippincott Co., Chapter 33, pp 1071-1089, 1990. Co., Chapter 217, pp 3065-3075, 1993.

8. Peterson HA: Treatment of Physeal Bony Bridges 10. Peterson HA: Premature Partial Closure of
by Means of Bridge Resection and Interposition the Triradiate Cartilage Treated With Excision
of Cranioplast. Mapfre Medicina 1993;4(Supl II): of a Physeal Osseous Bar. J Bone Joint Surg
226-230. 1997;79A(5):767-770.

307
39 Correction of angular deformities by
physeal distraction
J. de Pablos and J. Cañadell
INTRODUCTION
Physeal distraction is a thechnique of bone
lengthening applicable only in patients who
have not reached maturity. It is based on
utilization of the growth plate (physis) as
the “locus minoris resistentiae” of the bone,
through which -by distraction on its both
sides- separation of the metaphysis and
epiphysis is achieved and hence lengthening of
bone. It is therefore a technique that does not
require osteotomy or osteoclasia -”bloodless”(9)
lengthening- unlike other techniques that do
require such procedures.
The first experiments based on these
ideas were performed in animals by Ring(18)
in 1958 and the first clinical applications of
the technique were published in Russia by
Zavijalov and Plaskin in 1967(21) and 1968(22),
and Ilizarov and Soybelman in 1969(9), with
promising results. In Western Europe, it was
Monticelli and Spinelli(13) who began applying
physeal distraction in clinical practice.
The technique, originally conceived for
the purpose of simple lenthening on the
bones, is also applied currently for correcting
angular deformities in skeletally immature
long bones(5,12,15). We have been using physeal
distraction for the foregoing purposes since
1982(4).
The aim of the present work is to offer
a review of our clinical experience with
308 Partly reprinted with permission of Mapfre Medicina (vol. 4, suppl 2)
Research conducted at the Department of Orthopaedics of the
physeal distraction for the treatment of
angular deformities of the long bones over
the period from 1982 to 1991 and to offer what
we believe to be some useful conclusions for
future application.
PATIENTS AND METHODS
In our group, from 1982 until 1991 physeal
distraction has been applied on 65 occasions.
In 45 of these cases the objective was to
perform a simple lengthening; in the other
20 the method was essentially used to correct
angular deformities of the ends of long bones.
The latter group comprised 17 patients
(in three there were two bones involved), 11
male and six female with ages ranging from
11 to 14.5 years at the moment of beginning
the corrective treatment. Follow-up ranged
from a minimum of 11 months to a maximum
of 54 months. In the last X-ray controls carried
out, 10 of the 17 patients studied had reached
skeletal maturity.
In 12 out of the 20 deformities, the growth
plate at the level of the deformity did not
show radiological signs of premature closure,
whereas in the remaining 8 the radiological
images disclosed a bony bridge across the
physis.
Of the 12 angular deformities with no
bony bridge (10 patients) the location was
University of Navarra Medical School

A B C D
Figure 1. Correction according to Strategy I.
Postraumatic distal tibia vara. X-ray series.
A) Preoperative situation; B) 20 days postop.,
C) 35 days postop. A fibular osteotomy was
performed a that time, D) 50 days postop.
at the distal end of the femur in 7 (6 valgus
and 1 varus), on the proximal end of the tibia
in 2 (2 varus) and on the distal end of the
tibia in 3 (2 valgus, 1 varus). The aetiology
of the deformities was as follows: congenital
in 3 femoral valgus and 1 distal tibial valgus;
postraumatic in 1 femur valgus and 1 distal
tibial varus; after a burn in 1 femur valgus;
idiopathic in 1 bilateral femur valgus and 1
bilateral proximal tibial varus, and sequella
of an already-consolidated congenital
pseudoarthrosis of the tibia in 1 distal tibial
valgus. Apart from the angular deformity, in
this group there was a significant degree of
associated shortening (more than 1.5 cm) in
6 out of the 12 deformities.
Of the 8 angular deformities with bony
bridge (7 patients), the location was on the
distal end of the femur in 3 cases (2 valgus
and 1 varus); on the proximal tibia in 3 (3
varus) and the distal tibia in 2 cases (1 valgus,
1 varus). In one patient of this group the
Correction of angular deformities by physeal distraction
A B
Figure 2. Same case as Fig. 1. Global aspect of the
lower limbs. A) Preoperative. B) 1 year postoperative.
A slight length discrepancy has been corrected
simultaneously with the tibial angular correction.
involvement was bifocal, on the distal femur
and the proximal tibia. The aetiology of the
deformity was postraumatic in 1 femur varus,
1 proximal tibial varus, and 1 distal tibial
valgus; after Menigococcal sepsis in 1 femur
valgus, 2 proximal tibial varus and 1 distal
tibial varus, and after a knee Staphylococcal
arthritis in 1 femur valgus. In 3 of the 8
deformities shortening of the involved bone
segment was more than 1.5 cm.
Corrective treatment. In all cases corrective
treatment of the deformities was carried out by
physeal distraction with external monolateral
fixator-distractors. Specifically, the equipment
used were the ball-joint model of the Dinamic
Axial External Fixator (Orthofix)(6) in 8 cases
and modified Wagner apparatus in the rest.
The modification of the Wagner apparatus for
physeal distraction consisted in substituting
one of the conventional pin-holder clamps by
a “T”-shaped piece that allowed insertion of
the screws (epiphyseal and diaphyseal) on
perpendicular planes.
The surgical procedure was the same
in all cases and consisted simply in the
placement of the distractor apparatus with
two or three screws inserted into the diaphysis
perpendicular to its longitudinal axis and two,
309
J. de Pablos, J. Cañadell

A B C D E
Figure 3. Correction by Strategy II. Bony bridge and subsequent varus of the distal femur. A) Immediate
postoperative period. B) 10 days postoperatively. C) 60 days postoperatively. Lengthening 5.5 cm.
D) Single-step angular correction. E) 13 months postoperatively.

or exceptionally three, screws inserted into the
epiphysis parallel to the articular surface of
the corresponding bone. Attempts were also
made to achieve a maximum parallelism of the
longitudinal axis of the body of the apparatus
with respect to the axis of the bone shaft.
Where there was a physeal bony bridge, this
was not resected in any case. Distraction was
routinely begun 24 hours after the operation.
Two different strategies were employed
in the corrective process. In the first one
(“Strategy I”), used in 7 deformities,
asymmetric distraction of the physis was
begun from the very start of treatment in
such a way that a progressive correction of
the angular deformity was achieved.
This was attained by a simple free-moving
hinge system on the epiphyseal end of the
apparatus which, caused the longitudinal
distraction applied to the device to become
converted into angular movement of
the epiphyseal screws, thus achieving a
progressive correction of the deformity. The
rate of distraction applied to the apparatus
during this process of progressive angular
correction was 1.5 (2 x 0,75) mm/day. Once
this had been performed, in the cases in which
there was associated shortening, the movement
of the hinge was blocked and symmetric
physeal distraction continued at a rate of 1
(2 x 0.5) mm/day until the discrepancy had
been corrected (Figs. 1, 2).
The second method (“Strategy II”) used in
the remaining 13 deformities consisted in an
initial longitudinal distraction, with blocking
of angular movement, until a sufficient
degree of lengthening had been obtained to
permit angular correction in a single step.
Immediately thereafter, the angular movements
of the apparatus were blocked again and, if
there was associated shortening, symmetric
distraction was restarted until, at least ideally,
the discrepancy had been corrected. In this
second method, the rate of distraction applied
to the apparatus was always 1 (2x0.5) mm/
day (Fig. 3).
In all the tibial angular deformities
associated with shortening and in 1 case of
isolated tibial deformity, osteotomy of the
fibula was performed in association with
the distraction. In all these cases, distal tibia-
fibula stabilization was carried out either with
placement of a conventional 4.5 mm cortical
screw or with one of the screws of the fixator
placed in the distal tibial epiphysis.
At 8-10 days after the operation, no
restrictions were placed on the amount of
load put on the operated limb by the patients,
although neither were they required to load
more than was comfortable for them.

310

In all patients follow-up examined the
clinical and radiological evolution of the
patients at weekly intervals over the first
month and thereafter fortnightly in the later
phases of treatment.
Throughout the time during which the
apparatus was in place, the patient was
encouraged to actively move the joints adjacent
to the lengthened segment as much as possible.
After removing the apparatus, when necessary,
a specialized physiotherapy program was
initiated.
Except in the cases in which it was
imperative to discontinue treatment with
the apparatus for some reason of another, its
removal was empirically based on the follow-
up as visualized by conventional radiology.
RESULTS
Initially, correction of the angular deformity
was possible in all cases studied (with one
exception), regardless the presence or not
of a physeal bony bridge at the level of the
deformity (Figs. 4 and 5). On another two
occasions, there was a partial loss of the
correction achieved after removing the
apparatus; which needed the application of
plaster casts until definitive consolidation. The
remaining corrections persisted satisfactorily
after removal of the apparatus. Neither were
any recurrences in the corrected deformities
observed once the zone of distraction had
consolidated. Grading of the corrected
deformities ranged between a maximum of
32° in one case of proximal tibial varus with
a physeal bony bridge in a patient who had
suffered from Menigococcal sepsis in infancy
to a minimum of 16° in a distal femur valgus
(10° of excess), of congenital aetiology.
Regarding the extent of premature partial
physeal closure in the 8 deformities in which
this occurred, although only approximately,
in no case this exceeded 50% of the whole of
the affected physis.
Correction of angular deformities by physeal distraction
In all the cases with shortening associated
with the deformity, apart from correction the
angular deformity, attempts were also made to
correct the discrepancy, at least partially. The
maximum lenthening achieved in this group
of patients (9 in all) was 9 cm in a congenital
femoral shortening of 18 cm with distal valgus
and the minimum was 2.5 cm in a case of femur
shortening with associated distal valgus. Of the
9 shortenings, in 5, complete correction of the
discrepancy was obtained; in 2 at least 80% of
the discrepancy was corrected but correction
was not complete. In two cases lengthening
had to be interrupted prematurely due to
some kind of complication, thus not reaching
the above-mentioned 80%.
Consolidation periods varied considerably
and were directly related to the degree of
angular correction and lengthening required.
Specifically, the maximum was 9.2 months in
the case of the above maximum lengthening,
and the minimum 2.5 months in a case of a 16
bilateral proximal tibial varus of idiopathic
origin.
In all cases consolidation in the distraction
zone was achieved without the need for bone
graft nor internal fixation systems. With the
exception of 2 cases on the distal end of the
femur, 2 in the proximal tibia and 1 in the distal
tibia, in the rest of the deformities it was not
necessary to apply plaster casts to protect the
bone after removing the apparatus.
Regardless of the existence of physeal bony
bridges, in no case did the patients complain
of increased pain at the level of the distraction
zone at 2-3 days after starting treatment.
With respect to the complications that
appeared in the patients of the series a
distinction can be made between those with
a negative effect on the final result (major
complications) and those in which this did
not appear (minor complications). Among the
former, there was a case in which a dysfunction
of the distractor apparatus occurred, which
did not allow us to continue lengthening once
311
J. de Pablos, J. Cañadell

Figure 4. Previous congenital pseudoarthrosis.

Distal tibial valgus. Absence of bony bridge.
A) Preop. situation (left), imm. postop.(center), 15
days postop. (right). B) One step correction, 35 days
after surgery. C) Clinical situation, preoperatively.
D) Clinical situation, 6 months postoperatively.

A B

C D
312
 Correction of angular deformities by physeal distraction

1 2 3 4
A

1 2

B
Figure 5. Previous Meningococcal sepsis.
Distal femur valgus and proximal tibia vara
with physeal bony bridges. A) Femoral
correction: 1) preop.; 2) 15 days postop., 3)
30 days postop., 4) 45 days post (correction
completed). B) Tibial correction: 40 days
postop. C) AP view before (1) and 1 year
after surgery (2); L view before (3) and 1
year after surgery (4). C 3 4

the angular correction had been completed.
The remaining major complications included a
case of severe pin tract infection -thus making
premature removal of the apparatus necessary-
and two cases of partial loss of angular
correction after removing the apparatus
owing to insufficient consolidation of the
distraction zone. These account for 20% of
major complications with respect to the total
of 20 deformities treated.

313
J. de Pablos, J. Cañadell

Table 1.

Deformity correction
follow- Shor-
Case bridge up Site Degree tening etiology str Ang. def. Shortening Complications

M,11y no 42m Distal 22º valgus 18cm Congenital II Complete 9cm

femur
V,14y no 36m Distal 18º valgus 8cm Congenital II Complete Complete
femur
V,14.5y no 30m Distal 16º valgus 15cm Congenital II 0º 2.5cm Infection
femur
V,13.6y no 18m Distal 20º valgus —— Idiopathic II Complete ——-
femur
Idem no 18m Distal 20º valgus —— Idiopathic II Complete ——-
femur
M,13.5y no 25m Distal 14º varus —— Trauma II Complete ——-
femur
M,11.5y no 40m Distal 25º valgus 5.5cm Burn I Complete Complete
femur
M,11.6y no 12m Tibia 16ºvarus —— Idiopathic I Complete ——-
prox
Idem no 12m Tibia 16º varus —— Idiopathic I Complete ——-
prox
V,13.1y no 48m Tibia 28º varus —— Trauma II Complete ——-
distal
V,13.8y no 38m Tibia 14º valgus 4cm Congenital II Complete Complete
distal
V,12y no 38m Tibia 31º valgus 4.5cm Cong Ps II Complete Complete
distal
V,14y yes 20m Distal 20º valgus 6cm Arthritis II 5º 5cm Partial loss
femur
V,14.2y yes 46m Distal 12º varus 8cm Trauma II Complete 5.5cm Broken
femur distractor
M,13.5y yes 54m Distal 30º valgus —— Meningitis I Complete ——-
femur
Idem yes 51m Tibia 32º varus —— Meningitis I Complete ——-
prox
V,11,6y yes 15m Tibia 28º varus —— Meningitis II Complete ——-
prox
V,12.5y yes 20m Tibia 13º varus —— Trauma I Complete ——-
prox
M,12.6y yes 28m Tibia 31º varus —— Meningitis I Complete ——-
distal
V,13y yes 11m Tibia 23º valgus 3cm Trauma II 10º Complete Partial loss
distal

str: Strategy. Ang. def.: Angular deformity. Cong Ps: Congenital Pseudoarthrosis. Partial loss: Partial loss of angular
correction

As regards minor complications, the most
outstanding were transient or mild pin tract
infections (14% of the total of screws), which did
not prevent treatment from being completed,
and the transient rigidity observed on removing
the distractor, above all in the knee after distal
femur distraction and in the ankle following
distal tibia distraction. Such stiffness consistently
disappeared after a few weeks, falling to normal
ranges simply with physiotherapy.

314

Finally, after the corrective treatment, in
all cases premature complete closure of the
operated physis was observed with respect
to the contralateral. This did not lead to any
significant loss either in correction or in
lengthening in any cases.
More details on the patients’ methods and
results are given in Table 1.
DISCUSSION
The treatments most frequently
recommended for correction of angular
deformities of the long bones of the skeleton
are corrective osteotomies(19,20), and partial
physeal blocking by either epiphysiodesis(17)
or physeal stapling(2).
Single-step correction by osteotomy has the
drawbacks of its difficulty to be performed,
above all in important deformities, the
frequent need for internal fixation, which
involves a later surgical intervention for its
removal, and the impossibility of modifying
the correction achieved in the postoperative
period. Additionally, if the osteotomy is of
the “closing” type, with resection of a bone
wedge, a shortening of the corrected bone
occurs. If, by contrast, it is of the “opening
wedge” type, the risk of traction injuries to
the soft tissues increases and, frequently it
becomes necessary to add bone graft to stabilize
and facilitate consolidation at the level of the
correction made.
Regarding the methods of blocking partial
of the growth plate, its main limitations are
patient’s age when applying them (maximum
10-11 years, in our opinion), their low
predictability, which has recently improved
with the tables of Bowen et al(3), and the fact that
shortening of the bone may occur. Also, when
there is a physeal bony bridge, the maximum
benefit that can be derived from blocking of
the remaining growth plate is the halting of
the progression of the deformity but not its
correction.
Correction of angular deformities by physeal distraction
Specifically, in the case of this type
of deformity with physeal bony bridges,
Langenskiöld proposed a treatment by
resection of the bridge and the interposition
of different kinds of materials, in particular
autologous fat(10,11,14,16). This method, which
has been very effective in many cases, is also
limited by the age of the patient (in our opinion
10-11 years) and its difficult predictability.
The main advantages of physeal
distraction applied to angular deformites
in growing patients are essentially that one is
dealing with a method which does not need an
osteotomy and where correction is gradually
obtained. This means that correction and
consolidation are facilitated without the need
for bone grafting nor internal fixation and that
the risks derived from brusque distractions
decrease. Additionally, the method is fairly
non-invasive, it permits external adjustment
of the correction until consolidation occurs, it
acts at the site of the deformity and -perhaps
more important- it permits the orthopaedist
to perform lengthening associated to the
angular correction in the same treatment if
indicated.
In deformities with physeal bony bridges,
another advantage of physeal distraction is
that, if the bridge isn’t massive (less than 50%
approximately), no bridge resection nor other
surgical procedures are required since with
simple distraction the bridge can be disrupted.
This also the opinion of Connolly et al(5) as
stated in a recent clinical and experimental
report.
Although some authors advocate other
surgical interventions prior to physeal
distraction, such as resection of the bridge
accompanied by interposition of autologous
fat(8) or osteotomy of the bridge(12), in our
experience these were not necessary.
The main disadvantages of the proposed
method are those of external fixation-
distraction, in general, and physeal distraction
in particular. Among the latter, of special
315
J. de Pablos, J. Cañadell
interest are possible lesions to the growth
plate and also stiffness and joint sepsis.
With respect to physeal viability after
distraction, although in an experimental
study with young sheep carried out at
the University of Navarra(7) we observed
a highly satisfactory outcome in normal
physes subjected to slow distraction (0.5
mm/day), in the cases discussed here the
outcome was very different. The fact that in
the 20 deformities the growth plate showed
premature closure may have been because in
all cases the distracted physis had a previous
damage and because the rate of distraction was
more than 0.5 mm/day. This, together with
the fact that in another experimental study
carried out also at the University of Navarra(1)
a consistent recurrence of the bony bridge and
the deformity was observed when the method
was applied to previously deformed femurs
of skeletally immature sheep, means that our
recommendation for physeal distraction in
angular deformities -above all if there is a
physeal bony bridge- should be limited to
patients nearing skeletal maturity (in our
opinion, 10-11 years minimum).
The joint stiffness observed following
treatment was easily improved when
physiotherapy was started after removing
the apparatus.
Although in this series of patients we
observed no cases of septic arthritis we believe
that, above all in cases of physeal distraction
of the distal femur, there is a fairly high risk of
this occurring, such that extreme precautions
should be taken.
Pin-tract infections, a common problem
in all types of external fixation-distraction,
may become so important and/or aggressive
to make it necessary to interrupt treatment,
although this does not happen often.
Furthermore, it should be noted that it is even
less common to find osteomyelitis due to
pin-tract infection. At our own Department,
including all the cases of external fixation-
316
distraction, all the infections disappeared
after removing the screw corresponding to
the infected tract, however serious they were.
Another drawback that should be
mentioned regarding the proposed treatment is
that the patient is obliged to wear the apparatus
for several months with the discomfort
evidently inherent to this, above all if the
apparatus is circular.
Concerning the corrective strategy to be
used, we are not inclined to either in particular
since the results with both were similar.
However, it should be pointed out that with
a properly-placed monolateral distractor,
“Strategy I” is only valid in cases of femur
valgus an tibia vara. By contrast, “Strategy
II” can be applied for both varus and valgus,
regardless of whether these occur in the tibia
or in the femur. Another difference between
the two strategies is that with “Strategy I”
mounting stability is better since the fragments
of bone remain in contact during the angular
correction whereas in “Strategy II” this is not
the case. Accordingly, we tend to use “Strategy
I” in cases of femur valgus and/or tibia vara
with or without associated shortening and
“Strategy II” in the rest.
For the distraction phase in the type I
strategy, we have decided to apply a lengthening
rate in the body of the apparatus of 1.5 mm/
day in two increases of 0.75 mm each. This was
because in the light of a hypothetical situation
of a distance of 15 cm between the centres of
rotation of the epiphysis and the pin-holder
clamp and an epiphyseal width of 8 cm, 1.5
mm lengthening of the body of the apparatus
produces an angular correction of 0.6 and a
lengthening of the epiphyseal aspect closest
to the fixator of approximately 0.8 mm. When
distraction is carried out symmetrically, we
apply a rate of 1 mm/day over two increments
because this is our customary protocol in all
types of bone lengthening.
In physeal distraction, particularly when
this is carried out with an elastic circular

apparatus, the patient often feels an intense
pain in the area of distraction 2-3 days after
initiating the treatment(13). In our patients this
was not observed, perhaps due to the fact that
since we were using distrators that were more
rigid, the physeal fracture occurred in a more
controled and less brusque fashion, thus being
better tolerated by the patient.
We also believe that in general the results
have been satisfactory, with the exception of
the 4 cases in which there were complications.
As regards these, which we have designate
as major complications, we believe that
three of them could have been avoided. The
2 partial losses of angular correction were
due to premature removal of the apparatus
and dysfunction in the distractor in the third
case could easily have been compensated
if we had another to replace it, which was
not the case. In the fourth case, we believe
that the severe complication (arthritis) was
unavoidable since there is never any way of
absolutely preventing such situations.
Finally, regarding the fixator-distractor
apparatuses, we feel that the monolateral
ones are those of choice in most cases, and
only in very particular situations, in which
great versatility in mounting them is required
-such as cases with important associated
rotational deformities-, would the use of a
circular apparatus be the best option.
REFERENCES
1. Azcrate J, de Pablos J, Cañadell J: Treatment of
premature partial physeal closure by means of
physeal distraction: An experimental study. J
Pediatr Orthop (B). 1992;1:39-44.
2. Blount WP, Clark GR: Control of bone growth by
epiphyseal stapling. Preliminary report. J Bone
Joint Surg 1949:31-A:464-478.
3. Bowen JR, Leahey JL, Zhang Z, Mac Ewen GD:
Partial epiphysiodesis at the knee to correct angular
deformity. Clin Orthop 1985;198:184-190.
Correction of angular deformities by physeal distraction
4. Cañadell J, de Pablos J: Breaking bony bridges by
physeal distraction. A new approach. International
Orthopedics (SICOT) 1985;9:223-229.
5. Connolly JF, Huurman WW, Lipiello L, Pankaj
R: Epiphyseal traction to correct aquired growth
deformities. An animal and clinical investigation.
Clin Orthop 1986;202:258-68.
6. De Bastiani G, Aldegheri R, Renzi-Brivio L, Trivella
GP: Dynamic Axial External Fixation. Automedica,
1989;10:235-272.
7. De Pablos J, Cañadell J: Experimental Physeal
Distraction in immature sheep. Clin Orthop
1990;250:73-80.
8. Foster BK, Rozenbilds M, Yates R: Further results
of distraction physeolysis in a sheep tibial model.
J Bone Joint Surg 1986;68-B:333.
9. Ilizarov GA, Soybelman LM: Some clinical and
experimental data on the bloodless lengthening
of the lower limbs. Exp Khir Anest 1969;4:27-32.
10. Langenskiöld A: The possibilities of eliminating
premature partial closure of an epphyseal plate
caused by trauma or disease. Acta Orthop Scand
1967;38:267-279.
11. Langenskiöld A: Surgical treatment of partial
closure of the growth plate. J Pediatr Orthop
1981;1:3-11.
12. Monticelli G, Spinelli R: A new method of treating
the advanced stages of tibia vara (Blount’s disease).
Ita J Orthop Traum 1984;10:295-303.
13. Monticelli G, Spinelli R: Distraction epiphysiolysis
as a method for limb lengthening. III Clinical
applications. Clin Orthop 1981;154:274-85.
14. Ogden JA: The evaluation and treatment of partial
physeal arrest. J Bone Joint Surg 1987;69-A:1297-
1302.
15. Peltonen J, Karaharku E, Alitalo J: Experimental
epiphyseal distraction producing and correcting
angular deformities. J Bone Joint Surg 1984;66-
B:598-602.
16. Peterson HA: Partial growth plate arrest and its
treatment. J Pediatr Orthop 1984;4:246-258.
317
J. de Pablos, J. Cañadell
17. Phemister DB: Operative arrestment of longitudinal
growth of bones in the treatment of deformities.
J Bone Joint Surg 1933;15:1-15.
18. Ring PA: Experimental bone-lengthening by
epiphyseal distraction. Br J Surg 1958;49:169-73.
19. Sasaki T, Yagi T, Monji J, Yasuda K, Kanno Y:
Transepiphyseal plate osteotomy for severe tibia
vara in children: follow-up study of four cases. J
Pediatr Orthop 1986;6:61-65.
318
20. Tachdjian MO: Pediatric Orthopedics. WB
Saunders Co. Filadelfia 1972, pp 1462-1468 y
1588-1590.
21. Zavijalov PV, Plaskin JT: Elongation of crural
bones in children using a method of distraction
epiphysiolysis. Vestn Khir Grekova 1967;103:67-82.
22. Zavijalov PV, Plaskin JT: Distraction epiphysiolysis
in lengthening of the lower extremity in children.
Khirurgija 1968;44:121-37.
 Part VI
Physeal surgery in bone neoplasms
40 Physeal distraction in the conservative
treatment of malignant bone tumours in
children
J. Cañadell, M. San Julián, F. Forriol and J.A. Cara
Primitive malignant bone tumours occur
mainly in children and are located close to the
growth cartilage in 75% of cases(6,8). Growth
cartilage has classically been considered
to be capable of preventing spread of the
tumour in some cases because there are
not anasthomoses between epiphyseal and
metaphyseal vessels, but this barrier is not
impenetrable.
Physeal distraction has been extensively
used for bone lengthening(4,9) and for correcting
angular deformities(1,2,10) but we now describe
its use in facilitating the excision of malignant
hone tumours of the metaphysis while
preserving the epiphysis. Several studies has
been carried out in our Department on this
regard, in order to be sure of the accuracy of
the technique.
IMAGING STUDY
We carried out a study comparing several
image methods in the evaluation of the
extension and possible physeal affectation
in primitive malignant bone tumours. This
study could be corelated with the histological
features in such cases and thus we stablished
the current indications for our technique of
epiphyseal preservation by doing a physeal
distraction (epiphysiolysis) before excision
of metaphyseal bone tumours in children.
Partly reprinted with permission of Mapfre Medicina (vol. 4, suppl 2)
We have analyzed 65 metaphyseal
malignant bone tumours in children younger
than 16 years treated in our department
between 1982 and 1995. Fourty seven were
Osteosarcomas and eighteen Ewing´s Sarcoma.
The mean age of the patients was 11 years
(3-15). The minimal follow-up of the patients
was two years.
The image methods used were in all cases
X-ray; in 51 cases we included CT scan; we
used digital angiography in 48 cases (in the
cases of Osteosarcoma we used intraarterial
chemotherapy); and in 31 cases MRI.
All methods were evaluated by the same
radiologist.
Whenever possible the proximity to the
growth cartilaginous plate was evaluated
with the different methods. It was considered
as “distance zero” when the tumour was in
contact with the growth plate or invaded the
epiphysis. We have studied the following
statistical parameters of the above methods:
sensitivity, specifity, accuracy, positive
predictive value and negative predictive value.
In the anatomopathological study, the
physis was affected in 34 out of the 66 cases.
We performed a correlation study between
these anatomopathological findings and the
different image methods (Table 1).
The sensitivity was one hundred percent
in CT and MRI, and more than ninety percent
321
J. Cañadell, M. San Julián, F. Forriol, J.A. Cara
Table 1. Relationship between image
methods and anatomo-pathological findings
Image method False(-) False(+) Total
X-Ray (65) 1 6 7 (10.7%)
CT (43) 0 6 6 (13.9%)
Angiography (30) 1 3 4 (13.3%)
MRI (31) 0 3 3 (9.6%)
in X-ray and angiography. The specificity was
78.5% in the MRI.
The predictive positive value (the probability
that the lesion was actually present if it was
seen in the image method) was more than
eighty percent in all the methods studied. The
predictive negative value (the probability that
the lesion was in fact not present if it was not
detected in the image method) was one hundred
percent in CT and MRI. The accuracy of MRI
(predictive positive value plus predictive
negative value) was the best (90.3 %).
Regarding the MRI images, we found three
types of lesions:
-The tumour was not in contact with the
growth plate. In some cases there was edema
between the tumoral lesion and the growth
plate, an important feature to be differentiated
by an expert radiologist.
-The tumour was in contact with part or
all of the growth plate. In spite of that, some
of these cases were treated preserving the
epiphysis.
-The tumour transpassed the physis.
HISTOLOGICAL STUDY
Some years ago, an histological study was
carried out in our Department, in a historical
series of malignant bone tumours in children(5).
The proportion of cases with physeal invassion
by the tumour was similar to the one of the
image methods study study (fifty per cent).
Three kinds of morphological lesions at the
physis were seen:
322
-There were cases in which the growth
plate was not in contact with tumoral tissue.
-In other cases, areas of the growth plate
were in contact with tumoral tissue but were
not penetrated by the tumour. Voluminous
capillary sinusoids introduced themselves
between the columns of cartilaginous matrix.
The remainder of the physis appeared with
no alterations.
-The third type of lesion showed a physis
pierced entirely by tumoral tissue. These areas
crossed by tumour were surrounded by a
thinned growth cartilage, similar to the second
type of lesion.
Therefore, the possible invassion of the
epiphysis by the tumour seems to be a question
of time. There is a hipervascularization reaction
which leads to an early osification of the growth
plate, and after that, the tumour transgress
the physis.
CLINICAL STUDY
The fact that there are not anasthomoses
between epiphyseal and metaphyseal vessels,
and also the hability to determine wether the
epiphysis is affected by the image methods,
has allowed us to preserve the epiphysis and
the joint from resection in twenty-six cases
by using the physeal distraction following
our technique.
Between July 1981 and December 1996,
we operated on 353 patients with primary
malignant bone tumours. Twenty six of these
had physeal distraction before resection of the
tumour. Their mean age was 9.4 years; there
were twelve males and fourteen females. The
histological diagnosis was osteosarcoma in
sixteen patients and Ewing’s sarcoma in ten.
The indications for the technique were
as follows:
1) The tumour should be located at the
metaphyseal region
2) The physeal cartilage should be open.
3) The tumour should not transgress the
 Physeal distraction in the conservative treatment of malignant bone tumours in children
physis. Radiography, arteriography, CT and
particularly MRI were used to demonstrate this
preoperatively and histological examination
was used to corroborate the evidence
intraoperatively.
Operative technique. The surgical
technique consists of three phases (Fig. 1)
Phase one. Two pins are inserted into the
epiphysis and another two into the diaphysis
some centimeters away from the tumour An
external monolateral fixator with a T-shaped
piece for the epiphyseal pins is attached.
Distraction is begun in the operating room
and continues at the rate of 1 to 2 mm/day
until 2 cm of lengthening is achieved. The
Figure 1. Diagrams to show
the steps in the operation for
tumours of the femur (top) and
tibia (bottom).
mean time over which distraction was applied
was 15 days.
This first phase can be carried out while
the patient is finishing the course of adjuvant
chemotherapy.
Phase two. En-bloc resection of the tumour
is performed by diaphyseal osteotomy (the
metaphyseal one “is already done” because
the physis has been disrupted). If any doubt
exists about the possible invassion of the physis
by the tumour, the resected tumour is sent
immedialtely for histological examination,
and chains of PMMA containing gentamicin
are inserted into the space hold open by the
fixator. (Fig. 2)
323
J. Cañadell, M. San Julián, F. Forriol, J.A. Cara

A B C
Figure 2. A) In cases of any doubt about the invassion of the physis by the tumour, B) the tumour is
resected and the external fixator is mantained in place until the pathologist study the metaphyseal border
of resection. C) If no tumoural cells are found in the metaphyseal border of resection, the reconstruction
is carried out with an intercalary graft.

A B C
Figure 3. A) In case of no doubts about the invassion of the physis by the tumour, B) physeal distraction
is performed, C) and the reconstruction is carried out immediately after resection of the tumour.

Phase three. If no doubts exists about
the invassion of the physis by the tumour
(nowadays the MRI study is good enough), the
reconstruction of the bone defect is performed
with an intercalary graft in the same surgical
act (Fig. 3). If any doubt exists, reconstruction
of the limb is undertaken as soon as the
pathologist reports absence or presence of
tumour at the edges of the resected segment.
The kind of reconstruction performed

324
 Physeal distraction in the conservative treatment of malignant bone tumours in children

A B C
Figure 4. A) Radiograph showing a metaphyseal osteosarcoma of the femur in a 14-year-old boy. B)
After physeal distraction, resection of the tumour and autografting from the contralateral tibia. C) Final
result eight years later.

Table 2. used autografts from the contralateral tibia

as we did not have a bone bank (Fig. 4). Since
Site of tumor Excellent Good Fair Poor that date we have used allografts.
The use of autografts resulted in an
Distal femur 4 3 2 2 average of 2.8 operations per patient before
Proximal tibia 6 2 1 1
graft consolidation. With allografts this figure
Distal tibia 2 1 1 0
Distal fibula 1 0 0 0 was reduced to 0.74. Consolidation at the
metaphysis occurred before six months had
elapsed, but at the diaphyseal end it often
took longer than a year (Fig. 5).
depends on the anatomo-pathoplogical
result. Complications
Tumour recurrence. The patients were Infection. This occurred in two patients.
followed up for a mean time of 66 months (16 One was cured by systemic antibiotic therapy.
to 118). There were no local recurrences in the The other required removal of an allograft,
epiphyseal region, and only one in the diaphysis reattachment of the external fixator, insertion
(three years after the operation). Three patients of gentamicin-impregnated beads and systemic
developed pulmonary metastases at two, two antibiotic therapy. After infection was cured,
and three years after the operation. a new allograft was implanted.
Limb function. This varied with the Dislocation of the graft. Three patients
anatomical region involved. The results required a further operation, with the addition
measured by the criteria of Mankin et al(7) of autologous grafts.
are given in Table 2. Others. There was one peroneal nerve palsy,
Incorporation of graft. Before 1987 we still present one year after surgery, and one

325
J. Cañadell, M. San Julián, F. Forriol, J.A. Cara

A B

Figure 5. A) X-Ray showing a metaphyseal osteosarcoma of the femur in a 9-year-old girl. B) After physeal
distraction, resection of the tumour and reconstruction with an intercalary allograft.

case of fracture of the united allograft, treated This view is supported by the fact that
successfully by osteosynthesis with a plate no tumor recurred locally in the retained
and screws and autologous graft. epiphysis.

DISCUSSION
When resecting a tumour, the surgeon
must be certain that no malignant tissue is
left behind and most authors agree that a 5
cm margin is safe. This means that, when the
tumour is in the metaphysis, resection requires
the loss of the adjacent joint. Our technique,
using previous physeal distraction, avoid the
loss of the epiphysis. We believe that when
the growth cartilage is present, a margin of
safety is provided by the cartilage itself and
that 5 cm margin suggested by most authors
may in fact be unnecessary.
REFERENCES
1. Cañadell J and De Pablos J. Breaking bone bridges
by physeal distraction: a new aproach. Int Orthop,
9:223-9, 1985.
2. Cañadell J and De Pablos J. Correction of angular
deformities by physeal distraction. Clin Orthop,
283:98, 1992.
3. Daffner RH, Lupetin AR, Dash N et al. MRI in
the detedtion of malignant infiltration of bone
marrow. AJR, 146:353-8, 1986.
4. De Bastiani G, Aldegheri R, Renzi Brivio L and
Triviella G. Limb lengthening by distraction of the

326
 Physeal distraction in the conservative treatment of malignant bone tumours in children

epiphyseal plate. A comparison of two techniques transplantation in the management of malignant

in the rabbit. J Bone Loint Surg (Br), 68-B:545-9, tumors of bone. Cancer, 50:613, 1982.
1986.
8. Mercuri M, Capanna R, Manfrini M, et al. The
5. De Pablos J, Idoate M, Gil-Albarova J, Vázquez management of malignant bone tumors in children
J and Cañadell J. Estudio clínico sobre el “efecto and adolescents. Clin Orthop, 264:156, 1991.
barrera” de la fisis ante el osteosarcoma metafisario.
9. Monticelli G and Spinelli R. Distraction
Rev Ortop Traum, 34:472-81, 1990.
epiphysiolisis as a method of limb lengthening.
6. Hudson M, Jaffe MR, Jaffe N, et al. Pediatric III Clinical aplications. Clin Orthop, 154:274-85,
osteosarcoma. Therapeutic strategies, results 1991.
and prognostic factors derived from a lO-year
10. Peltonen JI, Karaharku EO and Alitalo I.
experience. J Clin Oncol, 8:1988-1997, 1990.
Experimental epiphysiolisis distraction producing
7. Mankin HJ, Doppelt SH, Sullivan TR and Tomford and correcting angular deformities. J Bone Joint
WW. Osteoarticular and intercalary allograft Surg (Br),66-B:598-602, 1984.

327
 Index
A B
Abnormal physis
Hematological abnormality of physis; 286
Metabolic abnormality of physis 286
Radiologic evaluation of the abnormal
physis; 57
Adolescence; 275, 281
AGAR; 245
Age
Chronological age; 5, 190
Patient’s age; 208
Skeletal age; 4, 220
Aitken; 183
Allograft; 133, 126
Amputation; 229
Apical ectodermal ridge; 119
Apparatus
Circular external fixator; 258, 317
Dinamic axial external fixator; 309
Fixator-distractor apparatuses; 317
Monolateral fixator-distractors; 309
Premature removal of the apparatus; 317
Wagner’s apparatus; 250
Modified Wagner’s apparatus; 309
Apposition-resorption phenomenon; 203
Arithmetic method; 215
Arthritis
Degenerative arthritis; 159
Premature knee arthritis; 283
Rheumatoid arthritis; 206
Septic arthritis; 252, 255, 286, 316
Traumatic arthritis; 255
Arthrogram; 200
Arthroscope; 296
Arthrosis; 255, 256
Articular incongruence; 159
Assessment of past growth; 220
Bar
Central bar; 242, 300
Excision of physeal bar; 54, 233
Experimental bar excision; 299
Growth plate bars 22
Linear bar; 300
Mapping of physeal bars 8
Peripheral bar; 300
Physeal bar resection; 234
Re-excision of the bar; 304
Technique of bar excision; 300
Barium; 302
Bergenfeldt; 182
Binocular loupe; 296
Blood supply; 15, 72
Epiphyseal blood supply; 159
Blount
Blount’s disease; 294
Blount stapling; 34, 267, 315
Bone bridge; 13, 81, 197, 238
Bone bridge breakage; 89, 93
Bone bridge resection; 81, 296
Diagnosis of physeal bone bridges; 160
Peripheral bone bridges; 161
Relapse of the bone bridge; 89
Bone cement; 295
Bone fusion; 281
Bone grafting; 315
Bone remodeling in malunited fractures; 202
Bone scan; 15
Bony bridge; 8, 19, 299
Bow legs; 267, 269, 272
Bridge
Bridge resection; 96, 294, 299
Central bridge; 161
Fibro-cartilaginous bridge; 244
329
Index

Lineal bridge; 161 Corrective Strategy I; 310, 316

Location of a physeal bridge; 287 Corrective Strategy II; 310, 316
Reformation of a bridge; 290, 291 Prevent the angular deformity; 296
Removal of the central bridge; 297 Axial deformity; 267, 273
Removal of the peripheral bridge; 297 Deformity of the joint surfaces; 296
Size of a physeal bridge; 287 Fishtail deformity; 58
Bromodeoxyuridine (BUDR); 71 Latitudinal deformity; 286
Burn; 7, 177, 286 Longitudinal deformity; 286
Burr Madelung deformity; 294
Dental burrs; 231 Overcorrection; 227, 232, 273
Motorized burr; 234 Remodeling of angular deformities; 202
Remodeling of rotational deformities; 205
C Undercorrection; 227, 232
Cannulated drill; 231 Desepiphysiodesis; 243, 245
Cessation of growth; 81 Distraction; 126, 163, 261
Charcot’s physis; 148 Asymmetric distraction of the growth plate; 96
Chart; 232 Distraction epiphysiolysis; 238, 245, 258
Green-Anderson charts; 223, 227 Distraction force; 263
Growth charts; 273 Distraction speed; 256
Moseley chart; 227 Epiphyseal distraction; 242
Chondrocytes; 107 Low distraction loads; 261
Chondrocyte survival; 115 Low rates of distraction; 261
Reimplantation of growth plate chondrocyte Transphyseal distraction; 239
cultures; 244 Drop out sign; 56
Chondrodiastasis; 76
Chondroepiphysis; 117 E
Closure Elongation; 54
Premature physeal closure; 14, 81, 161, 232, 296 Epiphyseal enlargement; 119
Physeal distraction of partial growth plate Epiphyseal reconstruction; 117
closure; 238 Epiphyses
Treatment of premature physeal closures; 161 Autogeneic epiphyses; 121
Types of premature physeal closures; 161 Syngeneic epiphyses; 121
Cold; 7 Epiphysiodesis; 22, 227, 275, 315
Collagen gels; 114 Arthroscopic epiphysiodesis; 281
Compensatory effect; 51 Asymmetric epiphysiodesis; 233, 275
Compression Completion of the epiphysiodesis; 89
Asymmetrical compression; 50 MRI following percutaneous epiphysiodesis; 60
Compression injury of the physis; 176, 191 Open epiphysiodesis; 60, 230
Computer programs; 221 Percutaneous epiphysiodesis; 54, 60, 230
Cranioplast; 235, 299, 302, 306 Premature epiphysiodesis; 171
Curetting; 231 Timing of epiphysiodesis; 223
Cycling cells; 72 Trochanteric epiphysiodesis; 64
Cyclosporin A; 133 Epiphysiolysis; 105
Cytodifferentiation; 120 Epiphysiolysis by distraction; 245, 258

D F
Deformity Farm machinery; 188
Angular deformity; 81, 93, 252, 281, 286 Fat; 82, 86, 235, 238, 290, 295, 299, 302
Correction of angular deformity; 232, 308 Autogenous fat; 235

330
 Index

Autologous fat transplant; 82 Greulich and Pyle method; 3, 162, 220, 223
Buttock fat; 302 Growth arrest; 7, 33, 86, 196
Femur valgus; 316 Growth cartilage
Fibrous dysplasia; 206 Growth cartilage transplant; 99
Fixator Viability of growth cartilage; 75, 78, 252
Circular external fixator; 258 Growth disorders; 159
Dinamic axial external fixator; 309 Growth disturbance lines; 12
Fixator-distractor apparatuses; 317 Growth percentile; 3
Insertion of fixation devices; 286 Growth plate; 6, 13, 22, 82, 84, 96, 107, 145, 159,
Internal fixation; 315 238, 244, 247, 261, 297
Monolateral fixator-distractors; 309 Growth plate defects; 107
FK506; 135 Growth recovery zones; 13
Fluorine-18; 15 Growth remaining method; 215
Fracture Growth retardation; 134
Bone remodeling in malunited fracture; 202 Growth spurt; 4
Compound fracture; 188 Growth stimulation; 133
Fracture Reduction Gunshot missiles; 188
Anatomic reduction; 160, 201
Closed reduction; 156 H
Open reduction; 156 Haematoma; 258
Position of the fragments after reduction; Harris; 8, 71, 149, 184, 192, 288, 296
208 Harris line; 8, 288, 296
Lengthening without fracture; 261 Harris’s classification; 71, 149
Occult fracture; 199 Salter-Harris type V injury; 192
Open fracture; 188 Helicoidal growth; 202, 206
Physeal fracture; 70, 143, 148-151, 153, 154, Hemarthrosis; 284
159, 196, 198, 253 Hemichondrodiatasis; 96
Type I fracture; 200 Hemiepiphysiodesis; 232, 233, 281-283
Type II fracture; 200 Arthroscopic hemiepiphysiodesis; 281, 283
Type III fracture; 200 Percutaneous hemiepiphysiodesis; 282
Type IV fracture; 201 Hemiepiphysiolysis; 105
Post-fracture overgrowth; 206 Heuter-Volkmann´s Law; 196, 204
Tillaux fracture; 174, 200 Hypercorrection 284
Triplane fracture; 188
Frostbite; 176, 286 I
Idiopathic genu valgum (IGV); 275
G Idiopathic genu valgum in adolescents; 281
Gadolinium; 17 Spontaneous correction of IGV; 281
Gait dynamics; 283 Immune reaction; 115
Gigantism; 269 Immunosuppression; 129, 133
Focal gigantism; 267 Indomethacin; 299
Gold foil; 299 Infection; 11, 19, 60, 177, 231, 246, 325
Graft Deep infections; 272
Bone grafting; 315 Pin tract infections; 314, 316
Cancellous bone grafts; 126 Injury
Dislocation of the graft; 326 Compound injury; 187
Free physeal grafts; 86 Crush injuries; 296
Incorporation of graft; 325 Electrical injury; 176, 286
Green and Anderson method; 223, 227 High energy injuries; 159

331
Index

Neuro-vascular injury; 60 Mechanism of lengthening; 75

Physeal compression injury; 176 Limb
Physeal injury; 11, 190 Limb discrepancies; 281
Physeal injury patterns; 171-178 Limb function; 325
Injury patterns Type 1; 172 Limb hypoplasia; 272
Injury patterns Type 1A; 172 Lower limb length discrepancy; 229
Injury patterns Type 1B; 172 Conservative treatment; 229
Injury patterns Type 1C; 173 Inhibiting growth; 229
Injury patterns Type 2; 173 Lengthening; 229
Injury patterns Type 3; 174 Limb shortening; 93, 229
Injury patterns Type 4; 175 Prosthetic fitting; 229
Injury patterns Type 5; 176 Prosthetic replacement; 229
Injury patterns Type 6; 177 Longitudinal growth; 6, 119, 202, 296
Injury patterns Type 7; 177 Low patella; 255
Injury patterns Type 8; 178
Injury patterns Type 9; 178 M
Primary treatment of epiphyseal injuries; 296 Magnetic resonance imaging (MRI); 8, 16, 22, 56,
Prognosis of a physeal injury; 190 58, 60, 160, 200, 289
Severity of injury; 159, 190 Field echo images; 56
Intermalleolar distance; 276, 281 Gradient-echo sequences; 16
Interposition; 294, 299, 315 MRI following percutaneous epiphysiodesis;
Interposition material; 234, 302, 306 60
Interposition of adipose tissue; 81 PD weighted; 16
Interposition of cranioplast; 299 T1 weighted images; 16, 56, 58
Interposition of methylmetacrylate; 245 T2 weighted images; 59
Interstitial growth; 29, 84 Major neurovascular lesions; 272
Irradiation; 176 Manual mapping technique; 22
Therapeutic irradiation; 286 Maturation; 3, 6
Ischaemia; 131, 286 Maturity; 305
Prediction of the discrepancy at maturity;
J 220
Joint sepsis; 316 Meningococcal sepsis; 313
Metabolic diseases; 11
K Metal markers; 234, 301
Klippel-Trenaunay syndrome; 206, 269 Metaphyseal ischemia; 148
Knock knee; 269, 267, 272, 278 Metaphyso-epiphyseal separation; 145
Methods of assessment and prediction; 215
L Methylmethacrylate; 238, 290, 299
Lacroix’s perichondrial ring; 145 Moseley’s straight-line graph; 162, 215, 227
Langenskiöld method; 162, 163, 234, 289 Motor boat propeller; 188
Latitudinal growth; 202 Myelomeningocele; 148
Lawn mower; 153, 177, 188
Leg length discrepancies (LLD); 267, 270 N
Measurement of leg length; 220 Neurofibromatosis; 206
Secondary LLD; 274 Non-union; 155, 159, 197
Lengthening; 229, 252, 258, 306 Normal growth; 3
Bloodless lengthening; 261, 308 Normal physis
Bone lengthening by physeal distraction; Anatomy of the normal physis; 55
250 Function of the normal physis; 55

332
 Index

O Physeal fractures Type IV; 151

Ogden’s classification; 151 Physeal fractures Type V; 151
Operating microscope; 289 Prognostic factors in physeal fractures; 159
Osgood-Schlatter lesion 178 Sequelae of physeal fractures; 143, 159
Ossification Surgical treatment of physeal fractures; 196
Desmal ossification; 78 Treatment of physeal fractures; 154
Endochondral ossification; 78 Physeal maps; 15, 22
Secondary center of ossification; 117 Physeal narrowing; 58
Osteomyelitis; 286 Physeal viability; 316
Osteochondritis dissecans; 177 Physeal widening; 12, 58, 59
Osteochondroses; 178 Physiotherapy; 259
Osteoid osteoma; 206 Physis
Osteotomy; 246, 306, 315 Abnormal physis; 57, 286
Corrective osteotomy; 89 Compression injury of the physis; 191
Progressive opening-wedge osteotomy; 165 Charcot’s physis; 148
Overgrowth Distal femoral physis; 286
Focal overgrowth; 273 Distal radial physis; 286
Post-fracture overgrowth; 206 Embryology of the physis; 55
Layers of the physis
P Germinal layer of the physis; 145, 187
Pain; 253 Hypertrophic layer of the physis; 145, 171
Pattern of growth; 3, 4 Proliferative layer of the physis; 6, 145,
Periosteal integrity; 258 87
Periosteum; 29, 72, 178, 204 Provisional calcification layer of the physis;
Peterson’s classification; 152 145, 187
Phemister´s technique; 33, 60, 230, 267 Normal physis; 55
Physeal arrest; 306 Proximal tibial physis; 286
Biology of physeal arrest; 286 Pin tract infections; 314, 316
Central pattern; 287, 288 PMMA containing gentamicin; 323
Linear pattern; 287, 288 Poland; 143, 183
Peripheral pattern; 287 Poland’s classification; 149
Timing of arrest of physeal activity; 215 Polytomograms; 14
Physeal distraction 70, 75, 89, 163, 233, 250, 308, Prediction of future growth; 220
321 Primary spongiosa; 6
Complications of physeal distraction 252 Prosthetics; 54
Indications for physeal distraction 252 Prosthetic fitting; 229
Physeal distraction for partial growth plate Prosthetic replacement; 229
closure; 238
Physeal fracture; 143, 196 R
Classification of physeal fractures; 148 Radiography; 7, 11
Complications from physeal fracture; 253 Autoradiography; 71
Frequency of physeal fractures; 143 Plain radiography; 55, 57, 288
Histopathology of physeal fractures; 145 Radionuclides; 15
Incidence-pathophysiology of physeal Ranvier’s groove; 29, 145, 175, 288, 300
fractures; 153 Regeneration of the growth plate; 82, 84, 121,
Occult physeal fractures; 198 247, 297
Physeal fractures Type I; 149 Remnant growth; 159, 284
Physeal fractures Type II; 150 Remnant growth graphs 162
Physeal fractures Type III; 150 Rendering technique; 23

333
Index

S Tillaux fracture; 174, 200

Salter; 184 Toddlers; 272
Salter’s classification; 149, 171 Toe to hand transfers; 128
Salter-Harris type V injury; 192 Tomography; 8, 14, 56, 58, 160, 199, 288
Scanogram; 220 Helical CT; 15
Scintigraphy; 56 Linear tomography; 7, 56, 58, 160
Bone scintigraphy; 8 Multiplanar tomography; 7
Quantitative scintigraphy; 58 Transplant; 99, 104, 121, 135
Screw Autologous fat transplant; 82
Absorbable screws; 64 Clinical epiphyseal plate transplantation; 128
Complications from epiphyseal screws; 255 Epiphyseal transplantation; 121, 128
Metallic screws; 66 Foetal transplantation; 135
PGA screws; 68 Growth cartilage transplant; 99
Sensory neuropathy; 286 Non-vascularized epiphyseal plate
Sequelae of physeal fractures; 143, 159 transplant; 127
Shapiro’s classification; 152 Vascularised epiphyseal plate transplant; 126,
Shoe lift; 54, 229 130
Silastic; 86, 295, 303 Tri-dimensional imaging; 22
Silicone; 162, 235, 238, 290, 299 Tumour; 11, 19, 286
Skeletal age; 4, 220 Malignant bone tumours; 321
Skeletal maturity; 256, 287 Metaphyseal bone tumours; 321
Skeletally immature bones; 308 Tumour recurrence; 325
Skeletally immature patients; 162
Skeletally mature patients; 164 U
Snowmobile; 188 Ultrasound; 15
Staples; 33 Ultraviolet visualization of Tetracycline-labeled
Loosening/dislocation of the staples; 269, 272 bone; 301
Metal staples; 275
Staple bending; 232 V
Staple dislodgement or fracture; 232 Vascularization of the growth plate; 145
Stapling; 34, 232, 267, 281, 315
Asymmetrical stapling; 47 W
Symmetrical stapling; 49 Wagner’s apparatus 250
Stiffness; 231, 252 Modified Wagner’s apparatus 309
Joint stiffness; 60, 255, 316 Wax; 238, 299, 302
Stimulus of the growth plate; 159 Wolff’s law; 196, 203
Straight line graph method; 162, 215
Strontium-85; 15 X
Strontium-87m; 15 X-rays; 12, 160, 199, 283
Surgical treatment of physeal fractures; 196
Z
T Zone of polarizing activity; 118
Tanner and Whitehouse method; 3, 220, 223 Zones of physis
Technetium 99m phosphate; 15, 56 Degenerative zone; 6
Tent shaped epiphysis; 287 Hypertrophic zone; 6, 145, 171
Thurstan Holland sign; 173, 186 Proliferative zone; 6, 187
Thymidine analogue bromodeoxyuridine; 71 Reserve zone; 6
Tibia vara; 316 Zone of provisional calcification; 6, 187

334