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The radiological features of avascular necrosis of the femoral head in homozygous sickle cell disease
ClinicalRadiology (1981) 32, 205-214 © 1981 Royal Collegeof Radiologists
0009-9260/81/00110205502.00
The Radiological Features of Avascular Necrosis of the Femoral Head in Homozygous Sickle Cell Disease R. E. J. LEE*, J. S. R. GOLD1NG and G. R. SERJEANT
Departments of Radiology, Orthopaedic Surgery, and the Medical Research Council Laboratories, University of the West lndies, Kingston, Jamaica Out of a total of 1031 patients with homozygous sickle cell (SS) disease attending a sickle cell clinic in Jamaica, 52 patients were found to have changes of avascular necrosis of the femoral head in 76 hips. Hip involvement was unilateral in 28 patients and bilateral in 24 patients (31 males and 21 females). The age of onset varied from nine to 45 years in the 40 patients in whom data appeared reasonably reliable and 82% developed this lesion between 10 and 29 years. Radiological change occurred, by definition, in the femoral head in all hips, in the acetabulum in 55 (72%) hips, femoral head migration occurred in 37 (49%) hips, and periosteal new bone formation in 24 (32%) hips. Two broad patterns of involvement were discernible according to the age at which avascular necrosis had occurred. Involvement of the immature femoral head epiphysis resulted in a flattened femoral head, epiphysio-metaphyseal overlap, a wide femoral neck and a mushroom Ceformity of the mature femoral head. In these lesions the articular surface and joint space was generally well preserved and little or no disability resulted in adult patients. Involvement of the mature femoral head was typically segmental, most commonly antero-superior, and with continued weight bearing resulted in collapse of the head and disruption of the articular surface. These lesions caused pain, limitation of movement, and commonly changes of osteoarthrosis.
Avascular necrosis of the femoral head is a wellrecognised complication of homozygous sickle cell (SS) disease but few detailed descriptions of the different radiological findings have been reported (Tanaka et al., 1956; Golding, 1956, 1973: Ennis et al., 1973; Middlemiss, 1976). A retrospective review of 52 patients with 76 hips affected by avascular necrosis in a large sickle cell clinic in Jamaica has allowed documentation of the different patterns of radiologlcal change in these lesions.
Patients with avascular necrosis of the femoral head were identified by symptomatic presentation (40 patients), or by incidental detection on skeletal surveys or abdominal radiographs (12 patients). Single radiographic studies were available in 19 patients (27 hips) and repeated studies, over periods of one month to 17½ years (mean 41 months), in 33 patients (49 hips). Lateral views of the hips were available in only 27 patients (35 hips). RESULTS
METHODS
The 52 patients with avascular necrosis were drawn from a total of 1031 patients with homozygous sickle cell (SS) disease attending the sickle cell clinics in Jamaica. There were 31 males and 21 females with ages at the time of the survey (1 January 1979) ranging from nine to 58 years (mean 27 years). Hip involvement was unilateral in 28 patients and bilateral in 24, giving a total of 76 hips. Age of onset is often unreliable in retrospective surveys but the occurrence of pain in the affected hip sometimes associated with a limp or limitation of movement was *Present address: Department of Radiology, Royal Victoria taken as the time of clinical onset. This had been Infirmary, Queen Victoria Road, Newcastle Upon Tyne, prospectively recorded in 24 patients and was reasonNE1 4LP. Requests for reprints should be addressed to: G. R. ably reliable in a further 16 patients. Age of onset Serjeant, Medical Research Council Laboratories, University was impossible to assess in the 12 patients without a history of specific symptoms. The age of onset in 40 of the West Indies, Kingston, Jamaica. The patients attended the sickle cell clinic of the University Hospital of the West Indies or peripheral sickle cell clinics operated by the staff of the MRC Laboratories in Jamaica. The study was confined to patients with SS disease, the diagnostic criteria including alkali and acid haemoglobin electrophoresis, characteristic Hb A2 levels, and family studies where possible. Details of these procedures are reviewed elsewhere (Serjeant, 1974).
206
CLINICAL RADIOLOGY
1 - Age of onset of avascular necrosis in 40 with an accurate history
Table
Age group (years)
p a t i e n t s w i t h r e a s o n a b l y reliable d a t a is s u m m a r i s e d in T a b l e 1. R a d i o l o g i c a l a b n o r m a l i t i e s were classified i n t o t h o s e a f f e c t i n g t h e f e m o r a l h e a d ( 7 6 hips in 52 p a t i e n t s ) , t h e a c e t a b u l u m ( 5 5 hips in 41 p a t i e n t s ) , f e m o r a l h e a d m i g r a t i o n ( 3 7 hips in 33 p a t i e n t s ) , a n d periosteal n e w b o n e f o r m a t i o n ( 2 4 h i p s in 2 2 p a t i e n t s ) . T h e site o f f e m o r a l h e a d a b n o r m a l i t i e s a p p a r e n t o n A P views in all h i p s a n d o n lateral views i n 35 h i p s is s u m m a r i s e d in T a b l e 2. Most lesions a p p e a r e d t o be s u p e r i o r o n A P views b u t were s h o w n t o b e a n t e r o s u p e r i o r w h e n lateral views were available (Fig. 1).
patients
Patients No.
%
0-9 10-19 20-29 30-39 40-49
2 17 16 4 1
5 42 40 10 3
Total
40
100
Table 2 - Comparison of apparent site of femoral head involvement on AP view with site by lateral view Apparent site on AP view
Site on lateral view when availcble Anterosup.
Superior
Superopost.
Whole head
2 .
1 .
Superior Supero-lateral Supero-medial Normal Lateral Medial Whole head Mushroom deformity
38 5 4 1 1 1 11 15
17 3 1 . . .
Total
76
21
.
.
. .
Mushroom
Total
1
-
1
-
-
4
5
20 4 1 1 0 0 4 5
1
6
5
35
.
.
.
.
. 2
.
. .
(a) (b) Fig. 1 - J.H., 19-year-old female. AP view (a) shows involvement of the superior segment but the lateral view (b) shows the lesion to be antero-superior with sparing of the postero-superior segment.
AVASCULAR NECROSIS OF THE FEMORAL HEAD
207
Table 3 - Radiological abnormalities in femoral head
Abnormality
Hips affected No.
Lesions of articular surface in mature femoral head Collapse of articular surface 62 Sequestration 29 Short cortical discontinuity 4 Upward projection of lateral part of head 5 Lucent subcortical line 8 Lytic defect 13 Osteophytes 20 Lesions resulting from involvement of immature femoral head Epiphysio-met aphy seal overlap 4 Mushroom head with intact cortex 10 Metaphyseal lucency with sclerotic borders 3 Medullary bone changes Patchy sclerosis 25 Dense solid shadow 21 Dense layer 15 Dense rings with lucent centres 14 Osteoporosis of medial part of head 8 Periosteal new bone formation on femoral neck 22
Antero-superior lesions accounted for 21/24 (88%) of all segmental involvements in lateral views. The radiological abnormalities in the femoral head and neck are summarised in Table 3. Collapse of the articular surface signified any defect in the normal smooth spherical shape of the femoral head. This varied from a short length of flattened articular cortex
82 38 5 7 11 17 26 5
13 4 33 28 20 18 11 29
to collapse of most of the femoral head (Figs 1 - 4 ) . Upward projection of the lateral part of the femoral head (Fig. 2) represents the remnant of the original articular surface after collapse of the medial or anterosuperior part of the head. A lucent subcortical line probably indicates subarticular trabecular fractures and is an early sign of structural failure preceding
Fig. 2 - E.B., 23-year-old male. Collapse of both femoral heads with sequestration. Collapse of the necrotic segment has left the lateral part of the left femoral head projecting lateral to the acetabular roof. The joint space is preserved.
208
CLINICAL RADIOLOGY
Fig. 3 - P.D., 20-year-old male. Segmental infarction with flattening due to collapse of bone centrally. A lateral roof osteophyte is shown on the acetabulum. collapse of the articular surface. Sequestration (Fig. 5) implies a loose fragment of articular surface and underlying bone, (Golding, 1973; Greenfield, 1975a; Davidson, 1976). The lytic defect (Fig. 6) may represent a hole in the articular surface and adjacent
underlying bone from which a sequestrum has become displaced or alternatively marked central collapse of a sequestrum. Neither explanation is entirely satisfactory and the cause must await pathological studies. Short cortical discontinuity (Fig. 7), a break in the articular surface of less than 2 mm in length, probably represents an early stage of sequestration. Medullary bone changes included dense solid shadows (Fig. 8), regions of increased density lying below an intact articular surface and measuring up to 2 cm in diameter. A dense layer (Fig. 9) was a linear, often serpiginous, sclerotic shadow forming the boundary between viable and necrotic bone. Dense rings with lucent centres, comprised of scierotic linear opacities surrounding small areas of normal bone and were thought to represent healing medullary infarctions. Diffuse patchy sclerosis (Fig. 10) was a further pattern observed. Epiphysio-metaphyseal overlap referred to a flattened widened epiphysis broader than its metaphysis, which appeared to 'creep' along the upper surface of the femoral neck and probably resulted in the wide femoral neck and the mushroom head deformity (Fig. 11) seen in some adults. These changes appear to result from infarction of the immature epiphysis. Irregular lucent areas in the metaphysis (Fig. 12) occurred in three patients (aged 11, 14 and 17 years) and in two crossed the growth plate resuiting in similar epiphyseal lesions. Acetabular abnormalities (Table 4) included
Fig. 4 - V.P., 29-year-old male. Almost total destruction of the right femoral head with lesser changes on the left. Both hip joints show features of osteoarthrosis which developed secondarily.
AVASCULAR
NECROSIS
Fig. 5 - C.R., l 1-year-old female. Dense sequestrated fragment in a lyric defect in an immature skeleton. Both upper and lower femoral neck surfaces show consolidated periosteal new bone.
changes in the shape of the articular surface (Fig. 11), lateral roof osteophytes (Fig. 3), and medullary bone changes (Fig. 10). Alteration in the relationship of the femoral head to the acetabulum was shown in 37 hips. A difference of 2 mm or more in the superior or medial joint space, when compared with the contralateral hip, was taken as significant. The superior joint space was measured vertically from the highest part of the femoral head except in major segmental collapse when the highest point of the remaining head was used. A decrease in this distance, inferring loss of or damage to the articular cartilage, was seen more often in association with segmental collapse of the femoral head which resulted in a cephalic migration of the head within the acetabulum. An increase in the superior joint space was recorded in one patient. Lateral migration of the femoral head was considered to be present when the medial joint space was increased. This was measured horizontally from the most medial part of the femoral head to the medial acetabular wall (lateral side of the 'teardrop' shadow). Of the 37 hips affected, 24 had lateral migration o f the head, seven cephalic migration (due to collapse o f the femoral head), five cephalo-lateral migration and one caudal
OF THE FEMORAL
HEAD
209
Fig. 6 - H.B., 22-year-old male. Large well-defined lytic defect (arrows). Lateral acetabular roof osteophyte present.
Fig. 7 - R.F., 23-year-old male. Short cortical discontinuities (arrows) with underlying patchy sclerosis.
210
CLINICAL RADIOLOGY
Fig. 8 - A.W., 38-year-old male. Dense solid shadows in b o t h f e m o r a l heads.
Fig. 9 - J.C., 35-year-old male. Dense layer in medial half of right femoral head. Left femoral head shows flattening medially with adjacent loss of density. migration. The prevalence of migration was greater in younger patients and follow-up in eight patients revealed improvement in four hips and deterioration in four hips. Periosteal new bone formation (Fig. 5) on the femoral neck was lamellar in type and involved the inferior aspect in 20/22 (91%) hips spreading to affect
the anterior, posterior and superior aspects in four of these. Periosteal new bone formation was observed to develop on a previously normal femoral neck in four patients aged 13, 14, 22 and 42 years, over periods of 7 - 3 9 months, (mean 19 months). The diagnosis of osteoarthrosis, based on two or more of the following criteria: diminished joint space,
AVASCULAR
NECROSIS
OF THE
FEMORAL
HEAD
211
eburnation or juxta-articular sclerosis, marginal osteophytes, and subchondral cysts (Fig. 13) was made in 14 hips. DISCUSSION Two basic patterns of femoral head involvement were discernible according to the maturity of the femoral head at the time of necrosis. Avascular necrosis of the unfused epiphysis resulted in a widened flattened epiphysis, epiphysio-metaphyseal overlap, a wide femoral neck and a mushroom-shaped deformity of the mature femoral head. The mature acetabulum became widened as a result of moulding round the flattened femoral head. As adults, these patients showed no actual disruption of the articular surface and the intact, though generally distorted, articular surface allowed a good range of movement. These abnormalities were frequently discovered incidentally during radiographic studies without a clear history of onset, perhaps because the initial involvement of the growing epiphysis had occurred many years earlier and had been forgotten. The femoral head epiphysis normally fuses between 17 and 20 years but the delay in epiphyseal fusion characteristic of SS disease (Serjeant and Ashcroft, 1973) allows a longer period over which necrosis may involve the immature epiphysis. These changes are similar to those seen in Perthes' disease. Radiologically the two lesions are so similar that differentiation is based on other criteria such as the younger age of onset of Perthes' disease, its
Fig. 10 - D.B., 31-year-old male. Diffuse patchy sclerosis of whole femoral head and of the acetabular walls and ilium. comparative rarity in black populations and the absence of abnormal haemoglobins. Howeverl SS disease may occur in other racial groups and may cause hip involvement in young patients so this differentiation is not satisfactory. A comparative study of the radio-
Fig. 11 - M.C., 43-year-old male. Mushroom deformity of both femoral heads showing smooth articular surface and preserved joint space.
212
CLINICAL
RADIOLOGY
Fig. 12 - A.D., ll~year-old female. Lucent areas in right femoral capital epiphysis and adjacent metaphysis. A segmental lucency with scleroti~ margins shown in left femoral capital epiphysis. i
Table 4 - A c e t a b u l a r abnormalities in 76 hips
Abnormality
Shape of articular surface Upward lateral slope to roof Flat roof Shallow acetabulum Irregular articular surface Erosion of lateral roof margin Roof destruction Osteophytes Lateral roof Inferior Structural bone changes Sclerosis Osteoporosis Loss of definition of roof Subchondral cysts Roof lucency with sclerotic rim logical and clinical features of hip involvement in Perthes' and in SS disease is in progress. Avascular necrosis of the mature femoral head is typically segmental and most frequently affects the antero-superior part of the femoral head. Whether such segmental necrotic lesions are confined to the superior part of the femoral head or whether it is only lesions at this site that come to clinical attention because of deformity associated with weight bearing is currently unclear. An early radiological sign o f this lesion may be the lucent subcortical line described by Norman and Bullough (1963) in dysbaric
Hips affected No.
%
14 4 6 8 2 1
18 5 8 11 3 1
28 4
37 5
16 8 4 3 1
21 11 5 4 1
osteonecrosis. This is thought to result from subarticular trabecutar fracture and reabsorption preceding collapse of the articular cortex. The 'dense layer' occurring at the border between necrotic and viable bone represents thickened trabeculae made up of living bone laid down on dead trabeculae (Catto, 1976). Following disruption o f the articular surface, the clinical outcome depends on the site and degree of distortion of the femoral head and on the development o f secondary osteoarthrosis. Survival of the lateral part of the head after collapse and superior
AVASCULAR
NECROSIS OF THE FEMORAL HEAD
213
secondary osteoarthrosis, an association between lateral migration of the femoral head and osteophyte formation on the acetabular roof occurred in 24 hips. It is possible that the abnormal lateral mobility of the femoral head on weight-bearing produces stress on the acetabular margin and joint capsule predisposing to osteophyte formation. Follow-up of these patients with acetabular osteophytes will clarify the significance of osteophytes in relation to possible developing osteoarthrosis. Eighteen hips showed loss of the normal inferior concavity of the acetabular roof and 16 of these demonstrated lateral migration. One patient developed an upward and laterally sloping roof in an acetabulum that was normal 15 years before. This suggests that moulding of the acetabulum had occurred in this patient. Widening of the joint space has been previously noted in SS disease (Greenfield, 1975b) and in Perthes' disease (Waldenstrom, 1934; Eyring et al., 1965) although in the latter it was attributed to an ipsilateral small ossificication centre (Caffey, 1968). This mechanism is most unlikely to contribute to this appearance in adults with SS disease. Osteoarthrosis defined on the basis of two or more criteria occurred in only 14 hips, all having osteophyte formation, 10 having a reduced superior joint space, three having subchondral cysts, and one manifesting complete destruction of the acetabular roof which articulated with the irregular stump of the femoral neck after total destruction of the femoral head. Fig. 13 - U.S., 41-year-old male. Osteoarthrosis complicating This series represents relatively gross bone changes a mushroom head deformity: narrowed joint space, juxta= articular sclerosis, marginal osteophyte and subchondral because avascular necrosis of the femoral head was cysts. frequently not diagnosed until articular disruption had occurred. Since avoidance of weight bearing in an migration of the medial part may result in a projec- avascular but undeformed femoral head may allow tion lying lateral to the acetabular roof and limiting preservation of an excellent functioning hip, diagnosis abduction (Golding, 1956). It is this antero-lateral of the pathology before deformity occurs is of pracsurviving portion which may bring the patient to tical importance. Annual limited skeletal surveys have surgical attention. Early involvement of the femoral been employed prospectively in dysbaric osteonecrosis head is not painful and may be well tolerated by the (Davidson, 1979) and annual antero-posterior and patient, but once the medial portion begins to collapse lateral views of both femoral heads may be considered the lower extremity is pushed into adduction and a justified in high risk age groups in SS disease. High limp, due to apparent shortening, develops rapidly. definition ffflms capable of demonstrating bone The acetabulum is usually intact and total replace- trabeculae would be required and since repair of ment of the femoral head component usually gives a lesions involves the laying down of new bone on satisfactory clinical result. dead trabeculae, the increased tissue may require an The high prevalence of acetabular abnormalities increased exposure (10kV more than standard). in the absence of secondary osteoarthrosis has not Radiation dosimetry on divers has shown that with been previously recognised. Lateral roof osteophytes adequate gonad shielding, the doses received are well occurred in 28 hips, in 20 of which there was no within the annual permissible body dose. Detection other evidence of osteoarthrosis. Osteophytes are of avascularity before radiological change has occurred seen as part of the normal ageing process and do not in the femoral head has been possible with radioalways indicate osteoarthrosis (Danielsson, 1964). isotope scanning using 99mTc phosphates in Perthes' In the present series, osteophytes were common in disease (Danigelis et al., 1975; Fasting et aL, 1978) young patients and although this may indicate early and this technique should be of value in the early
214
CLINICAL RADIOLOGY
detection o f avascular necrosis o f the femoral head in sickle cell disease. Although the scanning equipment necessary may not be available in many areas where sickle cell disease constitutes a c o m m o n public health problem, such early diagnosis is necessary to allow early therapy and avoid the problems o f chronic hip disease.
REFERENCES
Caffey, J. (1968). The early roentgenographic changes in essential coxa plana, their significance in pathogenesis. American Journal of Roentgenology, Radium Therapy and Nuclear Medicine, 103,620-634. Catto, M. (1976). Aseptic Necrosis o f Bone, ed. J. K. Davidson, pp. 44-45. Excerpta Medica, Amsterdam. Danielsson, L. G. (1964). Incidence and prognosis of coxarthrosis. Acta Orthopaedica Scandinavica, Supplement 66. Danigelis, J. A., Fisher, R. L., Ozonoff, M. B. & Sziklas, J. J. (1975). 99m-To polyphosphate bone imaging in LeggPerthes' disease. Radiology, 115,407-413. Davidson, J. K. (1976). Aseptic Necrosis of Bone, ed. J. K. Davidson, p. 168. Excerpta Medica, Amsterdam. Davidson, J. K. (1979). Recent Advances in Radiology and Medical Imaging, No. 6, ed. T. Lodge and R. E. Steiner, p. 152. Churchill Livingstone, London. Ennis, J. T., Serjeant, G. R. & Middlemiss, J. H. (1973). Homozygous sickle cell disease in Jamaica. British Journal of Radiology, 46, 943-950.
Eyring, B. J., Bjornson, D. R. & Peterson, C. A. (1965). Early diagnostic and prognostic signs in Legg-CalvePerthes' disease. American Journal of Roentgenology, Radium Therapy and Nuclear Medicine, 93, 382-387. Fasting, O. J., Langeland, N., Bjerkreim, L., Hertzenberg, L. & Nakken, K. (1978). Bone scintigraphy in early diagnosis of Perthes' disease. Acta Orthopaedica Scandinavica, 49, 169-174. Golding, J. S. R. (1956). The bone changes in sickle cell anaemia. Annals of the Royal College of Surgeons, 19, 296-315, Golding, J. S. R. (1973). Conditions of the hip associated with haemoglobinopathies. Clinical Orthopaedics and Related Research, 90, 22-28. Greenfield, G. B. (1975a). Radiology of Bone Diseases, p. 145. J. B. Lippincott Company, Philadelphia. Greenfield, G. B. (1975b). Radiology o f Bone Diseases, p. 66. J. B. Lippincott Company, Philadelphia. Middlemiss, J. H. (1976). Aseptic Necrosis of Bone, ed. J. K. Davidson, pp. 271-300. Excerpta Medica, Amsterdam. Norman, A. & Bullough, P. (1963). The radiolucent crescentic line - an early diagnostic sign of avaseular necrosis of femoral head. Bulletin of the Hospital for Joint Diseases, 24, 99-104. Serjeant, G. R. & Ashcroft, M. T. (1973). Delayed skeletal maturation in sickle cell anemia in Jamaica. Johns Hopkins Medical Journal, 132, 95-102. Serjeant, G. R. (1974). The Clinical Features of Sickle Cell Disease, pp. 26-27. North-Holland Publishing Company, Amsterdam. Tanaka, K. R., Clifford, G. O. & Axelrod, A. R. (1956). Sickle cell anemia (homozygous S) with aseptic necrosis of the femoral head. Blood, 11, 998-1008. Waldenstrom, H. (1934). First stages of coxa plana. Acta Orthopaedica Scandinavica, 5, 1-32.
0009-9260/81/00110205502.00
The Radiological Features of Avascular Necrosis of the Femoral Head in Homozygous Sickle Cell Disease R. E. J. LEE*, J. S. R. GOLD1NG and G. R. SERJEANT
Departments of Radiology, Orthopaedic Surgery, and the Medical Research Council Laboratories, University of the West lndies, Kingston, Jamaica Out of a total of 1031 patients with homozygous sickle cell (SS) disease attending a sickle cell clinic in Jamaica, 52 patients were found to have changes of avascular necrosis of the femoral head in 76 hips. Hip involvement was unilateral in 28 patients and bilateral in 24 patients (31 males and 21 females). The age of onset varied from nine to 45 years in the 40 patients in whom data appeared reasonably reliable and 82% developed this lesion between 10 and 29 years. Radiological change occurred, by definition, in the femoral head in all hips, in the acetabulum in 55 (72%) hips, femoral head migration occurred in 37 (49%) hips, and periosteal new bone formation in 24 (32%) hips. Two broad patterns of involvement were discernible according to the age at which avascular necrosis had occurred. Involvement of the immature femoral head epiphysis resulted in a flattened femoral head, epiphysio-metaphyseal overlap, a wide femoral neck and a mushroom Ceformity of the mature femoral head. In these lesions the articular surface and joint space was generally well preserved and little or no disability resulted in adult patients. Involvement of the mature femoral head was typically segmental, most commonly antero-superior, and with continued weight bearing resulted in collapse of the head and disruption of the articular surface. These lesions caused pain, limitation of movement, and commonly changes of osteoarthrosis.
Avascular necrosis of the femoral head is a wellrecognised complication of homozygous sickle cell (SS) disease but few detailed descriptions of the different radiological findings have been reported (Tanaka et al., 1956; Golding, 1956, 1973: Ennis et al., 1973; Middlemiss, 1976). A retrospective review of 52 patients with 76 hips affected by avascular necrosis in a large sickle cell clinic in Jamaica has allowed documentation of the different patterns of radiologlcal change in these lesions.
Patients with avascular necrosis of the femoral head were identified by symptomatic presentation (40 patients), or by incidental detection on skeletal surveys or abdominal radiographs (12 patients). Single radiographic studies were available in 19 patients (27 hips) and repeated studies, over periods of one month to 17½ years (mean 41 months), in 33 patients (49 hips). Lateral views of the hips were available in only 27 patients (35 hips). RESULTS
METHODS
The 52 patients with avascular necrosis were drawn from a total of 1031 patients with homozygous sickle cell (SS) disease attending the sickle cell clinics in Jamaica. There were 31 males and 21 females with ages at the time of the survey (1 January 1979) ranging from nine to 58 years (mean 27 years). Hip involvement was unilateral in 28 patients and bilateral in 24, giving a total of 76 hips. Age of onset is often unreliable in retrospective surveys but the occurrence of pain in the affected hip sometimes associated with a limp or limitation of movement was *Present address: Department of Radiology, Royal Victoria taken as the time of clinical onset. This had been Infirmary, Queen Victoria Road, Newcastle Upon Tyne, prospectively recorded in 24 patients and was reasonNE1 4LP. Requests for reprints should be addressed to: G. R. ably reliable in a further 16 patients. Age of onset Serjeant, Medical Research Council Laboratories, University was impossible to assess in the 12 patients without a history of specific symptoms. The age of onset in 40 of the West Indies, Kingston, Jamaica. The patients attended the sickle cell clinic of the University Hospital of the West Indies or peripheral sickle cell clinics operated by the staff of the MRC Laboratories in Jamaica. The study was confined to patients with SS disease, the diagnostic criteria including alkali and acid haemoglobin electrophoresis, characteristic Hb A2 levels, and family studies where possible. Details of these procedures are reviewed elsewhere (Serjeant, 1974).
206
CLINICAL RADIOLOGY
1 - Age of onset of avascular necrosis in 40 with an accurate history
Table
Age group (years)
p a t i e n t s w i t h r e a s o n a b l y reliable d a t a is s u m m a r i s e d in T a b l e 1. R a d i o l o g i c a l a b n o r m a l i t i e s were classified i n t o t h o s e a f f e c t i n g t h e f e m o r a l h e a d ( 7 6 hips in 52 p a t i e n t s ) , t h e a c e t a b u l u m ( 5 5 hips in 41 p a t i e n t s ) , f e m o r a l h e a d m i g r a t i o n ( 3 7 hips in 33 p a t i e n t s ) , a n d periosteal n e w b o n e f o r m a t i o n ( 2 4 h i p s in 2 2 p a t i e n t s ) . T h e site o f f e m o r a l h e a d a b n o r m a l i t i e s a p p a r e n t o n A P views in all h i p s a n d o n lateral views i n 35 h i p s is s u m m a r i s e d in T a b l e 2. Most lesions a p p e a r e d t o be s u p e r i o r o n A P views b u t were s h o w n t o b e a n t e r o s u p e r i o r w h e n lateral views were available (Fig. 1).
patients
Patients No.
%
0-9 10-19 20-29 30-39 40-49
2 17 16 4 1
5 42 40 10 3
Total
40
100
Table 2 - Comparison of apparent site of femoral head involvement on AP view with site by lateral view Apparent site on AP view
Site on lateral view when availcble Anterosup.
Superior
Superopost.
Whole head
2 .
1 .
Superior Supero-lateral Supero-medial Normal Lateral Medial Whole head Mushroom deformity
38 5 4 1 1 1 11 15
17 3 1 . . .
Total
76
21
.
.
. .
Mushroom
Total
1
-
1
-
-
4
5
20 4 1 1 0 0 4 5
1
6
5
35
.
.
.
.
. 2
.
. .
(a) (b) Fig. 1 - J.H., 19-year-old female. AP view (a) shows involvement of the superior segment but the lateral view (b) shows the lesion to be antero-superior with sparing of the postero-superior segment.
AVASCULAR NECROSIS OF THE FEMORAL HEAD
207
Table 3 - Radiological abnormalities in femoral head
Abnormality
Hips affected No.
Lesions of articular surface in mature femoral head Collapse of articular surface 62 Sequestration 29 Short cortical discontinuity 4 Upward projection of lateral part of head 5 Lucent subcortical line 8 Lytic defect 13 Osteophytes 20 Lesions resulting from involvement of immature femoral head Epiphysio-met aphy seal overlap 4 Mushroom head with intact cortex 10 Metaphyseal lucency with sclerotic borders 3 Medullary bone changes Patchy sclerosis 25 Dense solid shadow 21 Dense layer 15 Dense rings with lucent centres 14 Osteoporosis of medial part of head 8 Periosteal new bone formation on femoral neck 22
Antero-superior lesions accounted for 21/24 (88%) of all segmental involvements in lateral views. The radiological abnormalities in the femoral head and neck are summarised in Table 3. Collapse of the articular surface signified any defect in the normal smooth spherical shape of the femoral head. This varied from a short length of flattened articular cortex
82 38 5 7 11 17 26 5
13 4 33 28 20 18 11 29
to collapse of most of the femoral head (Figs 1 - 4 ) . Upward projection of the lateral part of the femoral head (Fig. 2) represents the remnant of the original articular surface after collapse of the medial or anterosuperior part of the head. A lucent subcortical line probably indicates subarticular trabecular fractures and is an early sign of structural failure preceding
Fig. 2 - E.B., 23-year-old male. Collapse of both femoral heads with sequestration. Collapse of the necrotic segment has left the lateral part of the left femoral head projecting lateral to the acetabular roof. The joint space is preserved.
208
CLINICAL RADIOLOGY
Fig. 3 - P.D., 20-year-old male. Segmental infarction with flattening due to collapse of bone centrally. A lateral roof osteophyte is shown on the acetabulum. collapse of the articular surface. Sequestration (Fig. 5) implies a loose fragment of articular surface and underlying bone, (Golding, 1973; Greenfield, 1975a; Davidson, 1976). The lytic defect (Fig. 6) may represent a hole in the articular surface and adjacent
underlying bone from which a sequestrum has become displaced or alternatively marked central collapse of a sequestrum. Neither explanation is entirely satisfactory and the cause must await pathological studies. Short cortical discontinuity (Fig. 7), a break in the articular surface of less than 2 mm in length, probably represents an early stage of sequestration. Medullary bone changes included dense solid shadows (Fig. 8), regions of increased density lying below an intact articular surface and measuring up to 2 cm in diameter. A dense layer (Fig. 9) was a linear, often serpiginous, sclerotic shadow forming the boundary between viable and necrotic bone. Dense rings with lucent centres, comprised of scierotic linear opacities surrounding small areas of normal bone and were thought to represent healing medullary infarctions. Diffuse patchy sclerosis (Fig. 10) was a further pattern observed. Epiphysio-metaphyseal overlap referred to a flattened widened epiphysis broader than its metaphysis, which appeared to 'creep' along the upper surface of the femoral neck and probably resulted in the wide femoral neck and the mushroom head deformity (Fig. 11) seen in some adults. These changes appear to result from infarction of the immature epiphysis. Irregular lucent areas in the metaphysis (Fig. 12) occurred in three patients (aged 11, 14 and 17 years) and in two crossed the growth plate resuiting in similar epiphyseal lesions. Acetabular abnormalities (Table 4) included
Fig. 4 - V.P., 29-year-old male. Almost total destruction of the right femoral head with lesser changes on the left. Both hip joints show features of osteoarthrosis which developed secondarily.
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Fig. 5 - C.R., l 1-year-old female. Dense sequestrated fragment in a lyric defect in an immature skeleton. Both upper and lower femoral neck surfaces show consolidated periosteal new bone.
changes in the shape of the articular surface (Fig. 11), lateral roof osteophytes (Fig. 3), and medullary bone changes (Fig. 10). Alteration in the relationship of the femoral head to the acetabulum was shown in 37 hips. A difference of 2 mm or more in the superior or medial joint space, when compared with the contralateral hip, was taken as significant. The superior joint space was measured vertically from the highest part of the femoral head except in major segmental collapse when the highest point of the remaining head was used. A decrease in this distance, inferring loss of or damage to the articular cartilage, was seen more often in association with segmental collapse of the femoral head which resulted in a cephalic migration of the head within the acetabulum. An increase in the superior joint space was recorded in one patient. Lateral migration of the femoral head was considered to be present when the medial joint space was increased. This was measured horizontally from the most medial part of the femoral head to the medial acetabular wall (lateral side of the 'teardrop' shadow). Of the 37 hips affected, 24 had lateral migration o f the head, seven cephalic migration (due to collapse o f the femoral head), five cephalo-lateral migration and one caudal
OF THE FEMORAL
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Fig. 6 - H.B., 22-year-old male. Large well-defined lytic defect (arrows). Lateral acetabular roof osteophyte present.
Fig. 7 - R.F., 23-year-old male. Short cortical discontinuities (arrows) with underlying patchy sclerosis.
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Fig. 8 - A.W., 38-year-old male. Dense solid shadows in b o t h f e m o r a l heads.
Fig. 9 - J.C., 35-year-old male. Dense layer in medial half of right femoral head. Left femoral head shows flattening medially with adjacent loss of density. migration. The prevalence of migration was greater in younger patients and follow-up in eight patients revealed improvement in four hips and deterioration in four hips. Periosteal new bone formation (Fig. 5) on the femoral neck was lamellar in type and involved the inferior aspect in 20/22 (91%) hips spreading to affect
the anterior, posterior and superior aspects in four of these. Periosteal new bone formation was observed to develop on a previously normal femoral neck in four patients aged 13, 14, 22 and 42 years, over periods of 7 - 3 9 months, (mean 19 months). The diagnosis of osteoarthrosis, based on two or more of the following criteria: diminished joint space,
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eburnation or juxta-articular sclerosis, marginal osteophytes, and subchondral cysts (Fig. 13) was made in 14 hips. DISCUSSION Two basic patterns of femoral head involvement were discernible according to the maturity of the femoral head at the time of necrosis. Avascular necrosis of the unfused epiphysis resulted in a widened flattened epiphysis, epiphysio-metaphyseal overlap, a wide femoral neck and a mushroom-shaped deformity of the mature femoral head. The mature acetabulum became widened as a result of moulding round the flattened femoral head. As adults, these patients showed no actual disruption of the articular surface and the intact, though generally distorted, articular surface allowed a good range of movement. These abnormalities were frequently discovered incidentally during radiographic studies without a clear history of onset, perhaps because the initial involvement of the growing epiphysis had occurred many years earlier and had been forgotten. The femoral head epiphysis normally fuses between 17 and 20 years but the delay in epiphyseal fusion characteristic of SS disease (Serjeant and Ashcroft, 1973) allows a longer period over which necrosis may involve the immature epiphysis. These changes are similar to those seen in Perthes' disease. Radiologically the two lesions are so similar that differentiation is based on other criteria such as the younger age of onset of Perthes' disease, its
Fig. 10 - D.B., 31-year-old male. Diffuse patchy sclerosis of whole femoral head and of the acetabular walls and ilium. comparative rarity in black populations and the absence of abnormal haemoglobins. Howeverl SS disease may occur in other racial groups and may cause hip involvement in young patients so this differentiation is not satisfactory. A comparative study of the radio-
Fig. 11 - M.C., 43-year-old male. Mushroom deformity of both femoral heads showing smooth articular surface and preserved joint space.
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Fig. 12 - A.D., ll~year-old female. Lucent areas in right femoral capital epiphysis and adjacent metaphysis. A segmental lucency with scleroti~ margins shown in left femoral capital epiphysis. i
Table 4 - A c e t a b u l a r abnormalities in 76 hips
Abnormality
Shape of articular surface Upward lateral slope to roof Flat roof Shallow acetabulum Irregular articular surface Erosion of lateral roof margin Roof destruction Osteophytes Lateral roof Inferior Structural bone changes Sclerosis Osteoporosis Loss of definition of roof Subchondral cysts Roof lucency with sclerotic rim logical and clinical features of hip involvement in Perthes' and in SS disease is in progress. Avascular necrosis of the mature femoral head is typically segmental and most frequently affects the antero-superior part of the femoral head. Whether such segmental necrotic lesions are confined to the superior part of the femoral head or whether it is only lesions at this site that come to clinical attention because of deformity associated with weight bearing is currently unclear. An early radiological sign o f this lesion may be the lucent subcortical line described by Norman and Bullough (1963) in dysbaric
Hips affected No.
%
14 4 6 8 2 1
18 5 8 11 3 1
28 4
37 5
16 8 4 3 1
21 11 5 4 1
osteonecrosis. This is thought to result from subarticular trabecutar fracture and reabsorption preceding collapse of the articular cortex. The 'dense layer' occurring at the border between necrotic and viable bone represents thickened trabeculae made up of living bone laid down on dead trabeculae (Catto, 1976). Following disruption o f the articular surface, the clinical outcome depends on the site and degree of distortion of the femoral head and on the development o f secondary osteoarthrosis. Survival of the lateral part of the head after collapse and superior
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secondary osteoarthrosis, an association between lateral migration of the femoral head and osteophyte formation on the acetabular roof occurred in 24 hips. It is possible that the abnormal lateral mobility of the femoral head on weight-bearing produces stress on the acetabular margin and joint capsule predisposing to osteophyte formation. Follow-up of these patients with acetabular osteophytes will clarify the significance of osteophytes in relation to possible developing osteoarthrosis. Eighteen hips showed loss of the normal inferior concavity of the acetabular roof and 16 of these demonstrated lateral migration. One patient developed an upward and laterally sloping roof in an acetabulum that was normal 15 years before. This suggests that moulding of the acetabulum had occurred in this patient. Widening of the joint space has been previously noted in SS disease (Greenfield, 1975b) and in Perthes' disease (Waldenstrom, 1934; Eyring et al., 1965) although in the latter it was attributed to an ipsilateral small ossificication centre (Caffey, 1968). This mechanism is most unlikely to contribute to this appearance in adults with SS disease. Osteoarthrosis defined on the basis of two or more criteria occurred in only 14 hips, all having osteophyte formation, 10 having a reduced superior joint space, three having subchondral cysts, and one manifesting complete destruction of the acetabular roof which articulated with the irregular stump of the femoral neck after total destruction of the femoral head. Fig. 13 - U.S., 41-year-old male. Osteoarthrosis complicating This series represents relatively gross bone changes a mushroom head deformity: narrowed joint space, juxta= articular sclerosis, marginal osteophyte and subchondral because avascular necrosis of the femoral head was cysts. frequently not diagnosed until articular disruption had occurred. Since avoidance of weight bearing in an migration of the medial part may result in a projec- avascular but undeformed femoral head may allow tion lying lateral to the acetabular roof and limiting preservation of an excellent functioning hip, diagnosis abduction (Golding, 1956). It is this antero-lateral of the pathology before deformity occurs is of pracsurviving portion which may bring the patient to tical importance. Annual limited skeletal surveys have surgical attention. Early involvement of the femoral been employed prospectively in dysbaric osteonecrosis head is not painful and may be well tolerated by the (Davidson, 1979) and annual antero-posterior and patient, but once the medial portion begins to collapse lateral views of both femoral heads may be considered the lower extremity is pushed into adduction and a justified in high risk age groups in SS disease. High limp, due to apparent shortening, develops rapidly. definition ffflms capable of demonstrating bone The acetabulum is usually intact and total replace- trabeculae would be required and since repair of ment of the femoral head component usually gives a lesions involves the laying down of new bone on satisfactory clinical result. dead trabeculae, the increased tissue may require an The high prevalence of acetabular abnormalities increased exposure (10kV more than standard). in the absence of secondary osteoarthrosis has not Radiation dosimetry on divers has shown that with been previously recognised. Lateral roof osteophytes adequate gonad shielding, the doses received are well occurred in 28 hips, in 20 of which there was no within the annual permissible body dose. Detection other evidence of osteoarthrosis. Osteophytes are of avascularity before radiological change has occurred seen as part of the normal ageing process and do not in the femoral head has been possible with radioalways indicate osteoarthrosis (Danielsson, 1964). isotope scanning using 99mTc phosphates in Perthes' In the present series, osteophytes were common in disease (Danigelis et al., 1975; Fasting et aL, 1978) young patients and although this may indicate early and this technique should be of value in the early
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detection o f avascular necrosis o f the femoral head in sickle cell disease. Although the scanning equipment necessary may not be available in many areas where sickle cell disease constitutes a c o m m o n public health problem, such early diagnosis is necessary to allow early therapy and avoid the problems o f chronic hip disease.
REFERENCES
Caffey, J. (1968). The early roentgenographic changes in essential coxa plana, their significance in pathogenesis. American Journal of Roentgenology, Radium Therapy and Nuclear Medicine, 103,620-634. Catto, M. (1976). Aseptic Necrosis o f Bone, ed. J. K. Davidson, pp. 44-45. Excerpta Medica, Amsterdam. Danielsson, L. G. (1964). Incidence and prognosis of coxarthrosis. Acta Orthopaedica Scandinavica, Supplement 66. Danigelis, J. A., Fisher, R. L., Ozonoff, M. B. & Sziklas, J. J. (1975). 99m-To polyphosphate bone imaging in LeggPerthes' disease. Radiology, 115,407-413. Davidson, J. K. (1976). Aseptic Necrosis of Bone, ed. J. K. Davidson, p. 168. Excerpta Medica, Amsterdam. Davidson, J. K. (1979). Recent Advances in Radiology and Medical Imaging, No. 6, ed. T. Lodge and R. E. Steiner, p. 152. Churchill Livingstone, London. Ennis, J. T., Serjeant, G. R. & Middlemiss, J. H. (1973). Homozygous sickle cell disease in Jamaica. British Journal of Radiology, 46, 943-950.
Eyring, B. J., Bjornson, D. R. & Peterson, C. A. (1965). Early diagnostic and prognostic signs in Legg-CalvePerthes' disease. American Journal of Roentgenology, Radium Therapy and Nuclear Medicine, 93, 382-387. Fasting, O. J., Langeland, N., Bjerkreim, L., Hertzenberg, L. & Nakken, K. (1978). Bone scintigraphy in early diagnosis of Perthes' disease. Acta Orthopaedica Scandinavica, 49, 169-174. Golding, J. S. R. (1956). The bone changes in sickle cell anaemia. Annals of the Royal College of Surgeons, 19, 296-315, Golding, J. S. R. (1973). Conditions of the hip associated with haemoglobinopathies. Clinical Orthopaedics and Related Research, 90, 22-28. Greenfield, G. B. (1975a). Radiology of Bone Diseases, p. 145. J. B. Lippincott Company, Philadelphia. Greenfield, G. B. (1975b). Radiology o f Bone Diseases, p. 66. J. B. Lippincott Company, Philadelphia. Middlemiss, J. H. (1976). Aseptic Necrosis of Bone, ed. J. K. Davidson, pp. 271-300. Excerpta Medica, Amsterdam. Norman, A. & Bullough, P. (1963). The radiolucent crescentic line - an early diagnostic sign of avaseular necrosis of femoral head. Bulletin of the Hospital for Joint Diseases, 24, 99-104. Serjeant, G. R. & Ashcroft, M. T. (1973). Delayed skeletal maturation in sickle cell anemia in Jamaica. Johns Hopkins Medical Journal, 132, 95-102. Serjeant, G. R. (1974). The Clinical Features of Sickle Cell Disease, pp. 26-27. North-Holland Publishing Company, Amsterdam. Tanaka, K. R., Clifford, G. O. & Axelrod, A. R. (1956). Sickle cell anemia (homozygous S) with aseptic necrosis of the femoral head. Blood, 11, 998-1008. Waldenstrom, H. (1934). First stages of coxa plana. Acta Orthopaedica Scandinavica, 5, 1-32.