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VOL. 124, No.

NEUROGENIC DISORDERS OF THE FOOT IN


DIABETES MELLITUS*
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By ERNEST KRAFT, M.D., EFTHIMIOS SPYROPOULOS, M.D.,


and NATHANIEL FINBY, M.D.
NEW YORK, NEW YORK

D IABETIC neuropathy of the foot has


been found more frequently in recent
years.5 This observation can be linked to
the longevity of diabetic patients and the
dramatic decrease of infant mortality since
the insulin era.
It is estimated that one-
half of the adult
diabetic population owes
its survival to proper care since childhood.6
The actual increase of cases has been
confirmed at the St. Lukes Hospital Cen-
ter and the Veterans Administration Hos-
pital, Outpatient Clinic, and it has been
found that specific bone changes can be
easily identified roentgenologically.

ROENTGEN FINDINGS FIG. i. Precursor of a diabetic foot. Infraction of


medial cuneiform bone (arrow). In the absence of
Two types of bone changes can be dis-
trauma, a search for an underlying diabetes is
tinguished: (i) the Charcot joint (de- indicated.
structive type); and (2) bone absorption
(mutilating type).39 The former affects
tarsal bones, while the latter is confined
to the forefoot. Both types may develop
concurrently and even bilaterally but not
in symmetric fashion.
The Charcot joint (destructive type) is
caused by repeated
trivial injuries4 and
merely by walking.
These lesions tend to
remain unrecognized due to the absence of
pain. Therefore, bone and joint changes
are usually far advanced when first recog-
nized.
Initially, a relaxation of joint capsules
leads to a talipes valgus and an instability
of intertarsal and tarsometatarsal joints.
A lack of proprioceptive reflexes allows
constant grinding and shearing motions
which result in fragmentation and infrac-
Fic. 2. Another precursor of a diabetic foot. This 34
tion of tarsal bones (Fig. i; and 2). year old diabetic man suffered an unsuspected frag-
As the relaxation increases and trau- mentation of a navicular bone (arrows).

* Presented as an Exhibit at the Seventy-fifth Annual Meeting of the American Roentgen Ray Society, 5an Francisco, California,
September 24-27, 5974.
From the Radiology Services of the St. Lukes Hospital Center and the Veterans Administration Hospital, Outpatient Clinic, New
York, New York.

7
i8 E. Kraft, E. Spyropoulos and N. Finby MAY, 1975
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FIG. 3. (A) Lateral view shows marked dorsal dislocation of the medial fragment of the navicular bone
(arrow). (B) Anteroposterior view of the same foot illustrates marked thinning, spreading, and sclerosis of
the lateral fragment of the navicular bone (arrow).

matic events accumulate, dislocations com- jection, spreading, flattening, and sclerosis
bined with fractures occur. Figure 3 illus- of the lateral fragment are noted (Fig. 3B).
trates a marked dorsal dislocation of the Bone destruction progresses rapidly.4
medial fragment of a navicular bone in a Figure 4i1 shows normal tarsal bones,
diabetic man. In the anteroposterior pro- while months later advanced destruction
VOL. 524, No. i Neurogenic Disorders of Foot in Diabetes Mellitus 9

and disintegration of these bones become


evident (Fig. 4B). Another diabetic patient
presented merely with a swollen ankle
without bone changes (Fig. GA). Eight
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months later the same clinical impression


prevailed, but a far advanced destruction
of tarsal bones could be demonstrated on
roentgenograms of the still swollen ankle
(Fig. SB). The diseased foot had remained
clinically unremarkable.
As a result of progressive valgus de-
formities, tarsal bones deviate and bulge
medially, and the cuboid bone shifts away
from the fifth metatarsal base (Fig. 6). Sig-
nificant roentgen findings include erosion,
sequestration, and osteolysis (Fig. 7, A

.-..

FIG. 6. Moderately advanced destruction of cuneiform


bones and metatarsal bases. Progressive valgus
deformity. Tarsal bones deviate and bulge medi-
ally, so that the cuboid bone is shifted away from
the fifth metatarsal base.

and B).9 Metatarsal fragments may re-


main ununited, especially when a superim-
posed infection develops. A healing tend-
Fic. . (A) This 7 year old diabetic patient pre- ency follows prolonged immobilization as
sented with only a swollen ankle. The tarsal bones seen in Figure 8, A and B, which was ob-
were unremarkable. (B) Same foot 8 months later.
tained II months apart. Even in far ad-
The ankle was still swollen and the foot clinically
unremarkable. Far advanced destruction of tar-
vanced cases, bones may regenerate, there-
sal bones now evident on roentgenograms of the b\T exhibiting hyperostosis, periosteal cal-
ankle. cification, callus, and synostoses (Fig. 9).3
20 E.Kraft, E. Spyropoulos and N. Finby MAY, 5975
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Ftc. 7. (A) Far advanced destruction of tarsal bones with valgus deformity, surface erosion, sequestration, and
osteolysis in a 37 year old diabetic patient. (B) Lateral view of the same patient illustrates dorsal disloca-
tion of grossly sequestered cuneiform bones and a vertical talus.

Secondary osteoarthritis can also develop narrowing (Fig. ii). Bones tend to become
with spur formations (Fig. io, A and B). sclerotic, thereby simulating an osteo-
Bone absorption (mutilating type) af- myelitis.
fects metatarsal heads and toe phalanges. At times, the bases of proximal phalanges
The epiphyseal ends gradually vanish, broaden and form a cup shape. Varieties of
while the shafts taper with pencil-point resulting deformities are known as: (i) in-

Fic. 8. (A) A milder case of bone destruction of metatarsal bases and of contiguous cuneiform bones ii and
III with a healing tendency. (B) Same foot with healing II months later. A synostosis is now evident in the
tarsometatarsal joints.
VOL. 524, No. i Neurogenic Disorders of Foot in Diabetes Mellitus 21

trusion; (2) mortar-in-pestle; () pencil-


in-cup; and (4) balancing pagoda.6 Synos-
toses of tarsometatarsal and intertarsal
joints may accompany this process of bone
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absorption (Flg. 12).


In far advanced stages, proximal pha-
langes are absorbed. The involved toes be-
come foreshortened but remain painless in
spite of a telescoping effect. Thick plantar
callosities frequently accompany the dis-
ease process and may result in dislocations
(Fig. ii).
There usually is dorsiflexion of toes and
a talipes cavus, in contrast to the valgus
deformity in the Charcot type. Osteomy-
elitis is frequently suspected when seques-
tered necrotic bones extrude through a
neuropathic ulcer or mal perforant.#{176}3
However, an associated infectious bone
lesion is usually absent.

VASCULAR CHANGES

Vascular calcifications are encountered


in the majority of cases (Fig. ii) without
necessarily causing signs of occlusion.
Specific angiographic findings include: (i)
arterial stenosis; (2) decreased perfusion;
and (,) diminished flow through small
arterial branches.6

MATERIAL

The material comprises 22 patients with


diabetes mellitus, 2 with sciatic nerve
lesions, and 2 with an unknown etiology.
FIG. 9. More advanced destruction with healing. Note
Their age ranged from 29 to 72 years with periosteal callus and fusion of the second and third
an average of The sexes were. evenly tarsometatarsal loints.
divided.
The Charcot type was encountered in u a degeneration of the posterior column of
patients, bone absorption in 12, and a com- the spinal cord takes place, as in tabes
bination of both types in 3. Bilateral in- dorsalis. In bone absorption, a peripheral
volvement was present in 2 patients, with neuropathy affects the postganglionic seg-
bone absorption of both feet in one. The ments of the spinal nerves, also sympa-
second patient presented with bone absorp- thetic, sensory, and motor fibers.6 Re-
tion in one foot and a Charcot joint in the cently, an avascular necrosis has also been
other. Vascular calcifications were ob- suggested as an etiologic factor.2
served in 13 patients (o per cent).
DIFFERENTIAL DIAGNOSIS
PATHOGEN ESIS
The differential diagnosis of the Charcot
Both types of foot lesions can be traced type includes osteomelitis and tubercu-
to neurologic deficits. In the Charcot type, losis. In these conditions, fistulae are fre-
22 E. Kraft, E. Spyropoulos and N. Finby MAY, 1975

1
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quently encountered and clinical mani fes-


tations predominate, in contrast to their
absence in the Charcot type.
In tabes dorsalis, roentgen findings of
bags-of-bones are essentially identical
with those in diabetic neuropathy. A
tabetic foot, however, can be excluded be-
cause specific lesions in tabes usually occur
only in larger joints and in the spine9 and
practically never in the foot. Even in the
ankle joint, diabetic neuropathy is more
likely to develop than a tabetic lesion
(Fig. I3).12 A combination with bone ab-
sorption in the forefoot, when present, can
readily clarify the diagnosis of a diabetic
condition.5
Bone absorption (mutilating type) by
itself cannot be distinguished from other
neuropathic disorders such as sciatic nerve
lesions, leprosy, alcoholic neuritis,47 syr-
ingomyeli a, burns, frostbite, neurologic
deficit, psoriasis, scleroderma, familial os-
teolysis, arthritis mutilans, and infected
callus. However, a combination with de-
structive changes of tarsal bones appears
characteristic of diabetes mellitus (Fig.
8
Fic. II. Bone absorption (mutilating type). Penciling
of the proximal interphalangeal joint of the second DISCUSSION
toe with subluxation (arrow). Dislocation of the
first metatarsophalangeal joint due to an underly- In the Charcot type, tendon reflexes are
ing callosity. Marked vascular calcifications. practically absent. There are zones of
VOL. 524, No. i Neurogenic Disorders of Foot in Diabetes Mellitus 23
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FIG. 12. Bone absorption (mutilating type). Ununited


fractures of all metatarsal bones. Tapering of the
fifth metatarsal shaft. Mortar-in-pestle configura-
tion of metatarsophalangeal joints Il-V. Synostosis
of intertarsal and tarsometatarsal joints.

paresthesia, anesthesia, diminished vibra-


tion, and lack of pinprick sensation. An
absence of position orientation and of pro-
tective pain leads to overburdening of tar-
sal joints and to destructive changes.
In the bone absorption or mutilating
type, a peripheral neuropathy may simu-
late the effects of a sympathectomy. A FIG. 14. Combination of bone absorption of the fifth
metatarsal bone with bone destruction of tarsal
bones is considered characteristic of a neurogenic
disorder of the foot in diabetes mellitus.

dysregulation is believed to cause vaso-


dilatation, hyperemia, and osteolysis.
The patients usually present with a se-
vere chronic diabetes mellitus which has
become resistant to management or has
been grossly neglected.8 Occasionally, how-
ever, the disease remains mild, of short
duration, and even unrecognized.5 Thus,
specific roentgen changes of the foot can
serve as clues to the detection of the
diabetes.8
According to Ellenberg,6 diabetic osteop-
athy may even precede an overt diabetes.
In such an instance, the underlying meta-
bolic disorder can also be confirmed by
other associated findings such as nephrop-
athy, retinopathy, myelopathy, specific
skin lesions, peripheral neuritis, and dis-
eases of the cardiovascular system, the
in a woman severe complications of gastrointestinal tract, and the endocrine
diabetes mellitus. system.5
24 E. Kraft, E. Spyropoulos and N. Finby MAY, 1975

An almost exclusive localization ofthe Diabetes mellitus. Fortschr. a. d. Geb. d.


R#{246}ntgenstrahlen u. d. Nuklearmedizin, 1969,
osteopathy in the foot represents an out-
110, 223-234.
standing feature of the diabetic neurop-
4. EICHENHOLZ, S. M. Charcot Joints. Charles C
athy. The ankle is less frequently affected
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Thomas, Publisher, Springfield, Ill., 1966.


(Fig. 13), while involvement of other parts . ELLENBERG, M. Diabetic complications without
of the skeleton is exceptional and merely manifest diabetes: complications as presenting
clinical symptoms. 7.A.M.A., 1963, 183, 926-
confined to single case reports.7
930.
6. ELLENBERG, M. Diabetic foot. New York 7.
SUMMARY
Med., 1973, 73, 2778-278!.
Neurogenic disorders of foot thein 7. FELDMAN, F., JOHNSON, A. M., and WALTER,
J. F. Acute axial neuroarthropathy. Radiology,
diabetics have been found with increasing
1974, III, 1-16.
frequency in recent years. Therefore, fa-
8. FOCHEM, K. Zum R#{246}ntgenbild der Osteoarthro..
miliarity with the spectrum of roentgen pathia diabetica. Radiol. c/in. et biol., 1969,
findings appears essential. 40, 28 1-290.
Significant include
changes Charcot 9. FRIEDMAN, S. A., and RAKOW, R. B. Osseous
joints of the tarsus (destructive type), and lesions of foot in diabetic neuropathy. Dia-
betes, 1971, 20, 302-307.
bone absorption of the forefoot (multilat-
TO. GoNDos, B. Roentgen observations in diabetic
ing type). osteopathy. Radiology, 1968, 9!, 6-13.
Charcot joints have been observed in II II. KLfJMPER, A., STREY, M., WELLER, S., ROTH, U.,
patients, bone absorption in and
12, a and MiLLER-BERG, H. Neurogene Osteolysen
combination of both types in 3. This com- bei Diabetes mellitus. Fortschr. a. d. Geb. d.
R#{246}ntgenstrahlen u. d. Nuk/earmedizin, 1968,
bination strongly suggests a diabetic neu-
ro8, 221-233.
ropathy. 12. KNUTSSON, F. Diabetic arthropathy. Acta
Pathogenesis and differential diagnosis radiol., 1951,36, 114-120.

are briefly discussed. 13. LEVIN, M., and ONEAL, L. W. The Diabetic
Foot. C. V. Mosby Company, St. Louis, 1973.
Ernest Kraft, M.D. 14. NORMAN, A., ROBBINS, H., and MILGRAM, J. E.
140 West End Avenue Acute neuropathic arthropathy: rapid, se-
New York, New York 10023 verely disorganizing form of arthritis. Radio/-
ogy, 1968,90,1159-1164.
i. P000NOWSKA, M. J., COLLINS, L. C., and DOB-
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