MULTIPLE OSTEOCHONDROSES OF THE FEET IN A
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1 MULTIPLE OSTEOCHONDROSES OF THE FEET IN A WEST INDIAN FAMILY I. D. BROWN and D. G. SHAW, LONDON, ENGLAND From the Queen Elizabeth Hospitalfor Children, London Similar appearances in the feet of four related Negro boys are described. The clinical, radiological and pathological features suggest an X-linked recessive form of osteochondrosis. CASE HISTORIES Case 1-This boy was first seen at the age of six years with a three months history of pain and swelling on the inner aspect of his right foot. The pain had been gradual in onset, and was present only on walking. On examination there was a soft-tissue swelling over the medial side and dorsu,m of the foot. There was no tenderness and movements were full. His general health was good. Radiographs showed fragmentation and increased density of the right navicular bone, consistent with an ischaemic necrosis (Fig. 1). Investigations revealed haemoglobin 141 grammes per cent, an erythrocyte sedimentation rate of 2 millimetres in the first hour and a normal white cell count. Tissue was taken from the synovium of the right talo-navicular joint and from the navicular bone for examination. The specimen from the navicular bone consisted largely of normal cartilage but included a few fragments of necrotic bone surrounded by reactive fibrous and chondroid tissue. There was no histological evidence of any inflammatory process. Cultures of the synovial fluid were negative. Three months later the child was free from symptoms. There was residual midtarsal thickening but movements were full and painless. At the age of ten years this child presentcd again at another hospital with pain and swelling of the left foot. There were no symptoms on the right side. The left foot was warm, with swelling and tenderness over the medial border and especially around the first metatarsophalangeal joint, movement of which was painful. Radiographs showed fragmentation of the proximal part of the shaft and of the epiphysis of the proximal phalanx of the left great toe, with which was associated some irregular new bone formation laterally and a little periosteal reaction (Fig. 2). The first metatarso-phalangealjoint was narrowed with subchondral translucencies in the metatarsal head and the shaft had periosteal new bone formation. There were several small lucent areas in the distal part of the medial cuneiform bone. The haemoglobin, white cell count and sedimentation rate were within normal limits. A biopsy was taken from the proximal phalanx of the hallux and revealed reactive fibrous tissue and bone with scanty necrotic material, and no inflammatory changes. Cultures excluded infection, tuberculosis and fungal lesions. After operation he developed a wound infection, from which a heavy growth of staphylococcus aureus was cultured. This responded to antibiotics, and three months later the wound had healed. There was slight swelling but no tenderness and a full range of movements. Aged ten years and ten months, he returned with a recurrence of the swelling of his left foot and a discharging sinus at the site ofbiopsy under the base ofthe hallux. On examination, the left foot was swollen, chiefly along the medial border of the first metatarsal bone, but was not tender. There was a valgus deformity. The ankle and subtalar joints were mobile but the midtarsal joint was stiff. Similar signs were present on the right side. General examination revealed no other abnormality. Power, tone and all modalities of sensation were normal. In particular, pain sensibility was normal. All reflexes were present. Radiographs 864 THE JOURNAL OF BONE AND JOINT SURGERY
2 MULTIPLE OSTEOCHONDROSES OF THE FEET IN A WEST INDIAN FAMILY 865 showed that gross widening of the first metatarsal shafts was now present with a widened and irregular epiphysial plate and gross fragmentation of the proximal epiphysis (Fig. 3). The base of the proximal phalanx of the left hallux was widened, with epiphysial fragmentation, disorganisation of the joint space and irregularity of the distal articular surface of the first FIG. 1 FIG. 2 FIG. 3 Case 1. Figure 1-Radiograph of the right foot when the child was aged 6 years. Figure 2-Radiograph of the left foot at the age of 10 years. Figure 3-Radiographs of both feet when the child was aged I 0 years and 10 months. metatarsal bone. Periosteal reaction was present around the shafts of the second to fourth right metatarsal bones, with less marked reaction around the fifth metatarsal bone. There was irregularity of the left navicular bone and the distal part of the talus, the cuneiform bones and the bases of the second and third metatarsal bones. Similar but less advanced VOL. 55 B, NO. 4, NOVEMBER 1973
3 866 I. D. BROWN AND D. G. SHAW changes were present in the right tarsal bones. Distally, the second left metatarsal bone was widened and fragmented, showing the features of a Freiberg s infraction. Investigations revealed a normal haemoglobin, white cell count and erythrocyte sedimentation rate. Serological tests for syphilis were negative. The sickle-cell test was negative and electrophoresis of haemoglobin was normal. The blood glucose was 1 10 milligrams/loo millilitres in a random sample. Plasma proteins, plasma calcium, phosphorus and alkaline phosphatase were normal as were Salmonella and Brucella agglutinins. Several cultures from the sinus were taken; in one, a moderate growth ofa coagulase positive staphylococcus was obtained. The remainder produced only a scanty growth of commensal organisms. The sinus persisted in spite of elevation and antibiotics and six months later it was explored and curetted. It was found to extend to the first metatarso-phalangeal joint. It subsequently healed and remained dry. In spite of the severe radiological changes, the right foot was pain-free. A skeletal survey revealed no other abnormality. Case 2-This boy was first seen, aged fourteen, at another hospital with a two-month history of pain in the right foot. Starting spontaneously, it became gradually worse and was aggravated by activity. The foot had become increasingly swollen. The left foot was initially I- pain-free, but later began to ache. There were no general symptoms. He had suffered 1 no previous serious illness. On examination the right foot showed swelling over the dorsum of the medial border with local warmth and tenderness. Movements were full. The left foot also showed swelling over the dorsum and tenderness over the first metatarsal bone. General examination revealed no other abnormality; the neurological examination was normal. Radiographs of the feet showed the presence of widening and periosteal new bone formation of the shaft of the first metatarsal bones, most marked at the proximal end where there were translucent areas bulging into the I metaphyses from the epiphysial growth S FIG 4 plates ofthe first (Fig. metatarsal 4). The bones epiphyses were fragmented. at the base Case 2-Radiographs of the feet at the age of 14 years... The distal aspects of the medial cuneiform bones were irregularly angulated where they were in contact with the metatarsals. There was periosteal new bone formation around the shaft of the second right metatarsal bone with minimal irregularity of the second left metatarsal bone. The lateral aspect of the epiphysis of the proximal phalanx of the right great toe was slightly irregular. The haemoglobin and white cell counts were normal but the erythrocyte sedimentation rate was 37 millimetres in the first hour. The antistaphylococcal titre was less than 2 units per millilitre. The sickle-cell test was negative as were tests for syphilis. A Mantoux test was also negative. He was admitted for biopsy, and a cavity was found at the proximal end of the first metatarsal shaft containing soft tissue of a granulomatous nature, culture of which was sterile. The specimen showed abundant necrotic bone with reactive fibrosis but nothing to suggest that the lesion was inflammatory. Radiographs of the skull, thoracic and lumbar spine, pelvis, both femora and tibiae and both arms were normal. Case 3-This patient aged fourteen presented at another hospital with a two-month history of pain and swelling of the left foot which was mainly over the dorsal and medial aspect. THE JOURNAL OF BONE AND JOINT SURGERY
4 MULTIPLE OSTEOCHONDROSES OF THE FEET IN A WEST INDIAN FAMILY 867 FIG. S FIG. 6 1#{149} F 1 5. FIG. 7 FIG. 8 Case 3 Radiographs of the feet of the child at the age of 14 (Fig. 5), two months later (Fig. 6), a further six months later (Fig. 7) and at the age of 16 years (Fig. 8). He had suffered no previous illnesses and was in good general health. General examination showed no other abnormality. Radiographs showed marked widening of the proximal part of the first metatarsal bone, with laminated periosteal reaction and widening of the epiphysial plate (Fig. 5). The epiphysis was fragmented. There was a fracture of the second metatarsal shaft and considerable callus formation. The third metatarsal shaft showed a small periosteal reaction probably from an undisplaced fracture. Investigations revealed a normal haemoglobin, white cell count and an erythrocyte sedimentation rate of 14 millimetres in the first hour. He was admitted for biopsy. The first metatarsal shaft was exposed and the base of the bone entered. A large cavity was curetted out and granular material was removed. No growth was obtained on culture of the material and cultures for fungi were negative. It has not been possible to trace the biopsy. He was treated empirically with penicillin and griseofulvin, and the wound healed uneventfully. Two months later radiographs showed that both the first metatarsal shafts were widened proximally, with widened epiphysial plates, fragmented epiphyses and disorganised first tarso-metatarsal joints. The fracture of the second left metatarsal bone had healed with much periosteal new bone. The shaft of the third metatarsal VOL. 55 B, NO. 4, NOVEMBER 1973
5 868 I. D. BROWN AND D. G. SHAW bone had become angulated and showed periosteal reaction which was also seen to a lesser extent around the left fourth and fifth metatarsal shafts (Fig. 6). Six months later radiographs of the left foot showed a periosteal reaction around the second right metatarsal shaft but that around the left metatarsals was less marked. There was destruction of the distal parts of both medial cuneiform bones (Fig. 7). He was re-admitted to the same hospital two years later with pain, swelling and tenderness of the left calf. A clinical diagnosis was made of deep vein thrombosis and he was treated with anticoagulants. The symptoms rapidly subsided. The foot was not painful at that time. When he was examined at this hospital he was aged sixteen and he was symptom-free. There was valgus deformity of both feet, more marked on the left. Gross thickening was present along the medial border of the foot with limitation of movements of the midtarsal and subtalar joints. Neurological examination was normal. In particular, pain sensibility was normal in both feet. Radiographs at this time showed that the periosteal new bone around the shafts of the left second to fifth and right second metatarsal bones had, to a large extent, remodelled, but irregular lucency persisted at the fracture sites of the left second and third metatarsal shafts. Remodelling had also occurred at the first metatarsal bases but grossly irregular and widened articulations with the cuneiform bones persisted (Fig. 8). Epiphysial fusion was now complete. Case 4-This boy presented at the age of seven years with a six-month history of swelling of the left foot. He had lived all his life in London and had had no serious illnesses. Clinical examination revealed swelling and warmth of the dorsum of the left foot with a mild valgus deformity and some diminution of movement at the subtalar and midtarsal joints. The rest ofthe examination was normal. Radiographs showed typical K#{246}hler sosteochondrosis (Fig. 9). FIG. 9 Case 4-Radiographs of the left foot at the age of 7 years. Family history-the family history, summarised in Figure 10, strongly suggests an X-linked recessive inheritance. The mother of the children in Cases 1 to 3 was a West Indian, who emigrated to England in Her feet and those of her parents were normal. The mother of the child in Case 4 was a sibling of the other affected children. Her feet, and those of her husband, were normal. The children in Cases 1 and 2 were born in the West Indies. The patients in Cases 3 and 4 were born in London and have never lived outside Britain. DISCUSSION We regard the bony changes in the feet of these children as a form of familial osteochondrosis. The radiological and histological features suggest that the primary pathological change was ischaemic necrosis of bone. The changes in the right navicular and second left metatarsal bones in Case 1 had the typical radiological features and age of onset of K#{246}hler s disease and Freiberg s disease, and histological appearances of the biopsy of the navicular bone were consistent with this. In the same patient, bone necrosis and fragmentation (accompanied by a periosteal reaction) were the essential changes in both first metatarsals. THE JOURNAL OF BONE AND JOINT SURGERY
6 MULTIPLE OSTEOCHONDROSES OF THE FEET IN A WEST INDIAN FAMILY 869 Cases 2 and 3 showed strikingly similar changes in the first metatarsal bones, and biopsy of the base of the first metatarsal bones in Case 2 revealed bony necrosis with reactive bone and fibrous tissue formation. In Case 3, considerable remodelling has taken place with reconstitution of the diaphysis but with residual deformity of the proximal epiphysis. A similar process of remodelling had begun in the right foot in Case 1. The changes in Case 4 have the typical radiological features of K#{246}hler s disease. I? I ci I I ci?? ci ci lit I J L ci?c$s I I d Affected male d 2 and case number 4 4. FIG. 10 The family tree. The clinical features were consistent with osteochondrosis. In each case the presenting symptom was pain of gradual onset, which persisted for several months. Disappearance of pain in Cases 2 and 3 coincided with radiographic remodelling, a clinical pattern similar to other examples of osteochondrosis. The chief differential diagnoses are neuropathic and infective disease. Neurological examination was normal. The radiological changes differ from the common patterns of tarsal disintegration described in neuropathic feet (Harris and Brand 1966). Moreover the presenting symptom has been pain in our cases. It is known that certain infective conditions, especially in tropical countries, can produce bizarre radiological features (Middlemiss 1961), but the fact that both feet in three siblings show changes of marked similarity makes this highly unlikely. The specimens taken in each of the biopsies were sterile to routine, tubercle, and fungal cultures. Serological tests for spirochaetes were negative in all patients. There was no microscopical evidence suggesting an infective process. Sickle-cell disease is an important cause of avascular necrosis of bone in West Indians. Screening tests for sickle-cell disease were negative in these children, and electrophoresis revealed no abnormal haemoglobins. In several reports trauma has been regarded as an important etiological factor in osteochondrosis affecting the feet. The delayed ossification of the navicular in K#{246}hler s disease, and its position at the apex of the longitudinal arch of the foot, could predispose it to injury by compression (Waugh 1958). Braddock (1959) found experimental grounds for regarding Freiberg s disease as an osteochondral fracture. It is of interest that both of these conditions were present in the feet of one of our patients. It is agreed that several of the osteochondroses can be genetically determined. Goff (1954) stated that Perthes disease might be a recessive Mendelian trait complex with varying degrees of penetrance. Cases have been reported in twins (Giannestras 1954). Goff found a 22 per cent familial incidence of K#{246}hler s VOL. 55 B, NO. 4, NOVEMBER 1973
7 D. BROWN AND D. G. SHAW disease. There are several reports of a familial incidence of osteochondritis dissecans (Stougaard 1964). Cullen (1970) reported two cases of Thiemann s disease in West Indian siblings. The inheritance of the trait here described seems to be X-linked recessive. Although osteochondrosis has been described at many sites, reports of involvement of the first metatarsal bones are scanty. Wagner (1930) described epiphysial fragmentation of a first metatarsal base in a six-year-old child, attributing the lesion to trauma. Murray and Jacobson (1971) described post-traumatic necrosis of the epiphysis of a first metatarsal bone. We have not been able to find further reports of avascular necrosis at this site. Whereas trauma may be a precipitating cause of osteonecrosis, it is possible that in our cases an inherited anomaly of vasculature of the bone may be the basic lesion. We have no evidence concerning this conjecture. SUMMARY 1. Four cases are described of multiple bony changes in the feet of members of a West Indian family. 2. The basic process is believed to be avascular necrosis of bone. The inheritance appears to be X-linked recessive. We are grateful to Mr R. E. Candlin, Mr M. F. Pilcher and Mr J. N. Fixsen for permission to study their patients, to Dr C. 0. Carter of the Hospital for Sick Children for advice on genetics, and to Professor H. A. Sissons of the Institute of Orthopaedics for reporting on the histology. REFERENCES BRADDOCK, G. T. F. (1959): Experimental Epiphysial Injury and Freiberg s Disease. Journal of Bone and Joint Surgery, 41-B, 154. CULLEN, J. C. (1970): Thiemann s Disease. Journal ofbone and Joint Surgerj, 52-B, 532. GIANNESTRAS, N. (1954): Legg-Perthes Disease in Twins. Journal of Boize and Joint Surgery, 36-A, FF, C. W. (1954): Legg-Calv#{233}-Perthes Syndrome and Related Osteochondroses of Youth. Springfield, Illinois: Charles C. Thomas, Publisher. HARRIS, J. R., and BRAND, P. W. (1966): Patterns of Disintegration of the Tarsus in the Anaesthetic Foot. Journal of Bone and Joint Surgery, 48-B, 4. MIDDLEMISS, J. H. (1961): Tropical Radiology. London : William Heinemann Medical Books Ltd. MURRAY, R. 0., and JACOBSON, H. G. (1971): The Radiology ofskeletal Disorders. Edinburgh and London: Churchill Livingstone. STOUGAARD, J. (1964) : Familial Occurrence of Osteochondritis Dissecans. Jouriial of Bone and folio Surgery, 46-B, 542. WAGNER, A. (1930): Isolated Aseptic Necrosis in the Epiphysis of the First Metatarsal Bone. Acta radiologica, II, 80. WAUGH, W. (1958): The Ossification and Vascularisation ofthe Tarsal Navicular and their Relation to KOhler s Disease. Journal ofbone and Joint Surgerv, 40-B, 765. THE JOURNAL OF BONE AND JOINT SURGERY
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