The Journal of Bone and Joint Surgery 79:1489-97 (1997)
© 1997 The Journal of Bone and Joint Surgery, Inc.
Subclinical Slipped Capital Femoral Epiphysis. Relationship to Osteoarthrosis of the Hip*
DAVID A. GOODMAN, M.D. ,
JOHN E. FEIGHAN, M.D.,
ANGELA D. SMITH, M.D.,
BRUCE LATIMER, PH.D.,
ROBERT L. BULY, M.D. and
DANIEL R. COOPERMAN, M.D., CLEVELAND, OHIO
Investigation performed at the Cleveland Museum of Natural History, Cleveland
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Abstract
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We examined the femora of 2665 adult human skeletons from an osteological collection to determine the prevalence of post-slip morphology termed femoral head-tilt deformity by Murray and pistol-grip deformity by Stulberg et al. The hypothesis was that primary osteoarthrosis of the hip is a secondary manifestation of a subclinical developmental disorder of the hip. The prevalence of post-slip morphology was 8 per cent (215 of 2665 skeletons). Severe osteoarthrosis was more prevalent in association with post-slip morphology (116 [38 per cent] of 306 hips) than in the matched controls (seventy-nine [26 per cent] of 306 hips) (p < 0.005). In the skeletons that had unilateral post-slip morphology, severe osteoarthrosis was more prevalent in the involved hips (thirty-one [37 per cent] of eighty-three) than in the contralateral, normal hips (eighteen [22 per cent] of eighty-three) (p < 0.05).
Post-slip morphology, which was unrelated to age, was found to be a major risk factor for the development of high-grade osteoarthrosis. We noted evidence of high-grade osteoarthrosis in sixty-three (68 per cent) of the ninety-three hips with minimum post-slip morphology in skeletons from individuals who had been fifty-six years old or more at the time of death compared with forty-five (48 per cent) of the ninety-three control hips. With the numbers available, this difference was not found to be significant (p < 0.025). The osteoarthrosis in the hips with post-slip morphology was distinctly characterized by anterior flattening of the acetabulum, cystic degeneration in the anterior metaphyseal-epiphyseal region, and progression to global osteoarthrosis of the hip.
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Introduction
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Osteoarthrosis is second only to cardiovascular disease as a cause of severe chronic disability16, and it affects more than 60 per cent of the population who are sixty-five years old or more (11,402 of 14,032 in one study14). This disease leads to the expenditure of billions of dollars for medication, operations, and days lost from work. In 1977, the direct economic cost for the treatment of arthritis was 7.7 billion dollars and the indirect cost (lost income of both wage earners and homemakers) was 918 million dollars8,14,26.
Osteoarthrosis can be classified as primary or secondary. The secondary causes include trauma, metabolic disorders, vascular disease, congenital dysplasia of the hip, slipped capital femoral epiphysis, and Legg-Calvé-Perthes disease3,4. Osteoarthrosis without evidence of pre-existing disease is classified as primary or idiopathic. Lloyd-Roberts17 found that 59 per cent of 124 hips in 117 patients had evidence of osteoarthrosis with no apparent etiology. Some authors18 believe that idiopathic osteoarthrosis of the hip is the result of an as yet undetermined systemic metabolic or genetic abnormality of cartilage or subchondral bone, whereas others believe that most cases of primary osteoarthrosis of the hip are secondary to subclinical acetabular dysplasia, slipped capital femoral epiphysis, or Legg-Calvé-Perthes disease7,11,15,20,28-30.
We evaluated the femoral heads of adult human skeletons to determine the epidemiology of post-slip morphological changes and their relationship, if any, to osteoarthrosis of the hip.
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Materials and Methods
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We obtained 2972 complete human disarticulated skeletons from the Hamann-Todd osteological collection at the Cleveland Museum of Natural History that had been gathered from the unclaimed dead at the Cleveland city morgue between 1893 and 1938. There were 2457 skeletons from men (837 of whom had been black) and 515 skeletons from women (287 of whom had been black). The average age of the individuals at the time of death was forty-five years (range, one to ninety-six years). Forty-four of the skeletons were from individuals who had been less than twelve years old. A skeleton was excluded from the study if it had an open physis; the pelvis and femora were not intact; part or all of the lower extremity was missing; or there was evidence of osteomyelitis, Paget disease, ankylosing spondylitis, rheumatological disease, fracture of the femur or acetabulum, dysplasia of the hip, or Legg-Calvé-Perthes disease. Fifty-two skeletons were excluded because they were skeletally immature; sixty-one, because they were incomplete; and 194, because they had evidence of another disease. Thus, 2665 skeletons (2227 from men and 438 from women) were included in this study.
Complete clinical information was not available for these skeletons. The dissections had been performed by medical students, the soft tissue had been removed by boiling, and the bone had then been cleaned with brushes. In 1985, all of the bones were degreased with trichloroethane.
The femora were examined visually for evidence of post-slip morphology by two examiners who were blinded with regard to the age, gender, and race of the individual. Post-slip morphology was characterized by loss of the normal concavity of the anterosuperior region of the head-neck junction, increased concavity of the posteroinferior region of the head-neck junction, location of the fovea posterior to a line through the axis of the neck, posterior tilt of the edge of the articular surface in reference to the perpendicular of a line through the axis of the neck, and a roughened surface of exposed metaphyseal bone located anteriorly between the apparent original position of the epiphysis and its displaced position (Figs. 1-A, 1-B, 2-A, 2-B, 2-C and 2-D).
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Figs. 1-A and 1-B: Photograph and illustration showing anterior views of a normal femur, one with minimum post-slip morphology and one with severe post-slip morphology. Post-slip morphology is characterized by increased concavity of the inferior region of the head-neck junction (1), loss of the normal concavity of the superior region of the head-neck junction (2), and a roughened surface of exposed metaphyseal bone between the apparent original position of the epiphysis and its displaced position (3). This is best seen in the femur with severe post-slip morphology.
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Figs. 1-A and 1-B: Photograph and illustration showing anterior views of a normal femur, one with minimum post-slip morphology and one with severe post-slip morphology. Post-slip morphology is characterized by increased concavity of the inferior region of the head-neck junction (1), loss of the normal concavity of the superior region of the head-neck junction (2), and a roughened surface of exposed metaphyseal bone between the apparent original position of the epiphysis and its displaced position (3). This is best seen in the femur with severe post-slip morphology.
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Figs. 2-A through 2-D: Photographs and illustrations showing lateral views of a normal femur, one with minimum post-slip morphology and one with severe post-slip morphology.
Figs. 2-A and 2-B: Views from below show loss of the normal concavity of the anterior region of the head-neck junction (1) and increased concavity of the posterior region of the head-neck junction (2).
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Figs. 2-A through 2-D: Photographs and illustrations showing lateral views of a normal femur, one with minimum post-slip morphology and one with severe post-slip morphology.
Figs. 2-A and 2-B: Views from below show loss of the normal concavity of the anterior region of the head-neck junction (1) and increased concavity of the posterior region of the head-neck junction (2).
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Figs. 2-C and 2-D: Views from above show the fovea (3) located posterior to a line through the axis of the neck and the edge of the articular surface (epiphysis) (4) tilted posterior to the axis of the neck.
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Figs. 2-C and 2-D: Views from above show the fovea (3) located posterior to a line through the axis of the neck and the edge of the articular surface (epiphysis) (4) tilted posterior to the axis of the neck.
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The skeletons were divided according to age at the time of death: forty years or less, forty-one to fifty-five years, and fifty-six years or more. We compared the degree of osteoarthrosis in the hips with post-slip morphology with that in control hips and then repeated the comparison after the two groups had been subdivided in terms of age.
Statistical analysis was performed with the chi-square method.
The degree of maximum posterior tilt of the head in relation to the axis of the neck was measured with a goniometer. The findings were graded as minimum (an angle of 30 degrees or less), moderate (an angle of 31 to 45 degrees), and severe (an angle of 46 degrees or more). The posterior angulation for the femora with post-slip morphology ranged from 5 to 78 degrees, whereas the angulation for the controls ranged from -5 to +3 degrees. The absence of any overlap between these ranges validated our visual scoring system.
We selected a group of 215 femora without a deformity that were matched for age, gender, and race of the donor with those of the 215 skeletons with a deformity. The two groups were graded for osteoarthrosis on the basis of the presence of osteophytes, erosions, and flattening or exposure of trabecular bone25. Lipping of the femoral fovea was considered normal. The acetabulum was graded first, by an examiner who did not know the morphology of the corresponding femur; then the femur was graded, and a total hip score was calculated on the basis of these two grades. According to the osteoarthrosis scale, the absence of lesions was considered normal, at least one lesion that was less than five by five millimeters or osteophytic lipping was designated as a small lesion, at least one lesion that was more than five by five but less than ten by ten millimeters or lipping and one small lesion was designated as a moderate lesion, and at least one lesion that was more than ten by ten millimeters was designated as a severe lesion. The hip score was based on the location of the lesions on the femur and acetabulum. Grade 0 indicated the absence of lesions; grade 1, a small lesion on the femur or acetabulum, or both; grade 2, a large lesion on either the femur or the acetabulum and either a small or no lesion on the other bone or a moderate lesion on both bones; and grade 3, large lesions on the femur and acetabulum or a moderate lesion on one bone and a large lesion on the other.
Anteroposterior and lateral radiographs were made of the proximal aspect of seventy-five femora that had evidence of post-slip morphology as well as fifty control femora. The lateral radiograph was made by placing the femoral neck directly parallel to the cassette, thereby eliminating the neck-shaft angle and antetorsion of the neck on the shaft; in this way, the true posterior or anterior version of the head in relation to the axis of the neck was measured (Figs. 3-A and 3-B). The reviewers, who were blinded with regard to whether or not the femora had evidence of post-slip morphology, graded the osteoarthrosis with use of the classification system of Boyer et al.1. Grade 0 indicated no degenerative changes; grade 1, one subchondral cyst or osteophyte and no osteosclerosis; grade 2, one or a few subchondral cysts and osteophytes and slight subchondral sclerosis; and grade 3, multiple subchondral cysts and osteophytes and marked subchondral sclerosis. As with the visual scale, the location of the lesions was noted. Narrowing of the joint space could not be evaluated as the articular cartilage had been destroyed during the initial preparation of the skeleton. The radiographic findings correlated well with the visual grading scale, especially with regard to confirmation of the wear patterns. We found the visual scale to be more detailed.
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Figs. 3-A and 3-B: Radiographs of two normal femora from one individual (Fig. 3-A) and two femora with post-slip morphology from another individual (Fig. 3-B). The head-neck angle was measured with use of the physeal scar and the axis of the neck. An angle of 87 to 90 degrees was considered normal, and an angle of 86 degrees or less was characteristic of post-slip morphology.
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Figs. 3-A and 3-B: Radiographs of two normal femora from one individual (Fig. 3-A) and two femora with post-slip morphology from another individual (Fig. 3-B). The head-neck angle was measured with use of the physeal scar and the axis of the neck. An angle of 87 to 90 degrees was considered normal, and an angle of 86 degrees or less was characteristic of post-slip morphology.
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Results
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Epidemiology
Of the 2665 skeletons that met the inclusion criteria, 215 (8 per cent) had the morphological characteristics of post-slipped capital femoral epiphysis. One hundred and twenty-two skeletons had bilateral post-slip morphology, whereas sixty-nine hips had morphological findings on the left side only and twenty-four, on the right side only (a left-to-right ratio of 2.9:1). Thus, 337 (6 per cent) of the 5330 femora had post-slip morphology. The prevalence in men was 8 per cent (187 of 2227), and that in women was 6 per cent (twenty-eight of 438), for a male-to-female predominance of 1.3:1. Black men had the highest rate of post-slip morphology (eighty-two [10 per cent] of 813), and white women had the lowest (nine [5 per cent] of 182). Black men also had the highest rate of bilateral involvement (forty-nine [60 per cent] of eighty-two), and white women had the lowest (three of nine) (Table I).
Severity of Morphological Changes
The post-slip morphology was minimum (5 to 30 degrees) in 306 femora (91 per cent), moderate (31 to 45 degrees) in twenty (6 per cent), and severe (more than 45 degrees) in eleven (3 per cent).
Effect of Aging
Seventy-nine (8 per cent) of the 941 skeletons from individuals who had been forty years old or less at the time of death, sixty-seven (7 per cent) of the 920 skeletons from individuals who had been forty-one to fifty-five years old, and sixty-nine (9 per cent) of the 804 skeletons from individuals who had been fifty-six years old or more had post-slip morphology. With the numbers available, the difference in the prevalence among the three age-groups was not found to be significant (p > 0.25).
Osteoarthrosis
The thirty-one hips that had moderate or severe post-slip morphology in general had more severe osteoarthrosis than either the age-matched control hips or the hips that had minimum post-slip morphology; however, because of the small number of hips, we could not make any meaningful comparisons.
We compared the prevalence of osteoarthrosis in the 306 hips that had minimum post-slip morphology with that in the age-matched control hips without any changes. Eighty-nine (29 per cent) of the hips with post-slip morphology had grade-0 osteoarthrosis, 101 (33 per cent) had grade-1 osteoarthrosis, seventy-eight (25 per cent) had grade-2 osteoarthrosis, and thirty-eight (12 per cent) had grade-3 osteoarthrosis compared with 132 (43 per cent), ninety-five (31 per cent), sixty-four (21 per cent), and fifteen (5 per cent) of the control hips. Thus, 116 (38 per cent) of the hips with minimum post-slip morphology had grade-2 or 3 osteoarthrosis compared with seventy-nine (26 per cent) of the control hips. This difference was significant (p < 0.005).
We also compared the prevalence of osteoarthrosis in the involved hips with that in the contralateral, normal hips in the eighty-three skeletons that had unilateral minimum post-slip morphology. Nineteen (23 per cent) of the involved hips and twenty-five (30 per cent) of the contralateral hips had grade-0 osteoarthrosis, thirty-three (40 per cent) of the involved hips and forty (48 per cent) of the contralateral hips had grade-1 osteoarthrosis, twenty-one (25 per cent) of the involved hips and thirteen (16 per cent) of the contralateral hips had grade-2 osteoarthrosis, and ten (12 per cent) of the involved hips and five (6 per cent) of the contralateral hips had grade-3 osteoarthrosis. Thus, thirty-one (37 per cent) of the eighty-three involved hips had grade-2 or 3 osteoarthrosis compared with eighteen (22 per cent) of the contralateral, normal hips. This difference was significant (p < 0.05).
Twelve (10 per cent) of the 115 hips with minimum post-slip morphology in skeletons from individuals who had been forty years old or less had grade-2 or 3 osteoarthrosis compared with five (4 per cent) of the age-matched control hips. With the numbers available, this difference was not found to be significant (p > 0.1). Forty-three (44 per cent) of the ninety-eight hips with minimum post-slip morphology in skeletons from individuals who had been forty-one to fifty-five years old had grade-2 or 3 osteoarthrosis compared with twenty-nine (30 per cent) of the age-matched control hips. This difference also was not found to be significant (p = 0.06). Sixty-three (68 per cent) of the ninety-three hips with minimum post-slip morphology in skeletons from individuals who had been fifty-six years old or more had grade-2 or 3 osteoarthrosis compared with forty-five (48 per cent) of the age-matched control hips. This difference was significant (p < 0.025).
Morphology of Osteoarthrosis
A characteristic feature particular to the unilateral post-slip morphology was flattening and widening of the anterosuperior aspect of the acetabulum (Figs. 4-A and 4-B). This appeared to be age-related since the hips with post-slip morphology in the skeletons from younger individuals had normal acetabula. Acetabular changes began to appear in the skeletons from individuals who had been fifty to sixty years old. Evidence of wear was seen in the anterosuperior region of the acetabulum and femur. The hips with post-slip morphology in skeletons from individuals who had been more than sixty years old had evidence of small cysts in the anterior metaphyseal-epiphyseal region of the femoral neck. In hips without post-slip morphology, the osteoarthrosis was characterized by wear in the superior aspect of the acetabulum. The skeletons from the oldest and more severely osteoarthrotic individuals had global osteoarthrosis.
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Figs. 4-A and 4-B: A skeleton from an individual who was sixty years old at the time of death.
Fig. 4-A: Anterior photograph showing flattening (wear) of the anterior aspect of the acetabulum with post-slip morphology (right side of photograph).
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Fig. 4-B The corresponding illustration, also showing flattening (wear) (1) of the anterior aspect of the acetabulum with post-slip morphology.
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Discussion
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Osteoarthrosis in general, and specifically osteoarthrosis of the hip, is not an inevitable consequence of aging18. Osteoarthrosis of the hip has been reported in 5 per cent of the population who are fifty-five years old or more14, and more than 80,000 total hip arthroplasties are performed each year23,31. Lloyd-Roberts noted primary osteoarthrosis in seventy-three of 124 hips17. Since the mid-1970s, metabolic (pseudogout), genetic (hereditary osteoarthrosis), and traumatic causes (labral tears) have been implicated in the etiology of secondary osteoarthrosis6,19,29; however, the etiology of primary osteoarthrosis is still unknown. Primary osteoarthrosis appears to be influenced by age16, gender23, and mechanical factors16. The influence of obesity16,29, osteoporosis12, and immunological factors13,22 is unknown.
Several authors20,26,28 have suggested that so-called primary osteoarthrosis of the hip is in fact secondary to acetabular dysplasia, slipped capital femoral epiphysis, Legg-Calvé-Perthes disease, and other disorders that were overlooked or clinically silent in childhood. These suggestions were based on observation of the radiographs of patients who had osteoarthrosis of the hip. We concluded that post-slip deformity was a major risk factor in the development of severe osteoarthrosis. One weakness of the present study is that the system used to grade the severity of osteoarthrosis cannot be used to describe the clinical situation, since a large number of both hips with post-slip morphology and control hips had grade-2 or 3 osteoarthrosis. However, the scale does provide a tool for comparison since the absolute percentages are not as important as the difference between groups.
Elmslie7 noted that a pre-existing deformity of the hip joint could be identified in patients in whom osteoarthrosis developed at a relatively young age. Law15 suggested that degenerative disease of the hip joint could be related to a mild slip of the proximal femoral physis. Murray20 described the femoral head-tilt deformity and used anteroposterior radiographs to measure the femoral head ratio. He noted a deformity in eighty of 200 patients that was similar to that produced by mild slipped capital femoral epiphysis. We found similar changes in the skeletons in the present study and noted that the changes were better visualized on the lateral radiograph with the beam directly perpendicular to the axis of the neck, thereby eliminating distortion secondary to the neck-shaft angle and anteversion of the neck (Figs. 5-A and 5-B).
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Figs. 5-A and 5-B: Anterior and true lateral photographs of a normal femur (N) and a femur with minimum post-slip morphology (S). The changes that are barely discernible on the anterior photograph are easily distinguished on the lateral photograph.
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Figs. 5-A and 5-B: Anterior and true lateral photographs of a normal femur (N) and a femur with minimum post-slip morphology (S). The changes that are barely discernible on the anterior photograph are easily distinguished on the lateral photograph.
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Resnick24 noted a superomedial pattern of osteoarthrosis, similar to the femoral head-tilt deformity described by Murray, in forty-eight of 100 patients who had a total hip replacement and concluded that the tilt deformity was secondary to the formation of osteophytes and remodeling of the osteoarthrotic hip and not to a minimum slip, which other authors20,26,28 believed could lead to primary osteoarthrosis. If Resnick's theory is accurate, then the prevalence of femora with post-slip deformity should increase with age; however, we did not find any such association. We believe that post-slip morphology, when present, is a constant characteristic in adults and is not an age-acquired phenomenon.
Stulberg et al.28 described the characteristic deformity of the femoral head and neck seen in patients who have a known history of mild slipped capital femoral epiphysis or Legg-Calvé-Perthes disease as a pistol-grip deformity and noted this deformity in thirty of seventy-five patients who had idiopathic osteoarthrosis. Solomon26 noted the femoral head-tilt deformity in fifty-nine of 196 patients who had primary osteoarthrosis.
Stulberg and Harris27 observed the pistol-grip deformity in thirty (40 per cent) of seventy-five patients in whom symptoms of degenerative joint disease developed late in life. About one-third of their patients were seventy years old or more when they had their first reconstructive procedure, whereas less than one-fourth of the patients had a reconstructive procedure before they were sixty years old. In the present study, significantly more hips with post-slip morphology from individuals who had been fifty-six years old or more at the time of death had high-grade osteoarthrosis compared with the control hips in that age-group. We believe that this indirect correlation adds validity to the osteoarthrosis severity scale used in the present study.
The prevalence of post-slip morphology was constant in all age-groups in this study of skeletons with closed physes, for which complete clinical data were not available. The constant prevalence suggests that minimum post-slip morphology may represent an anatomical variant in the shape of the proximal aspect of an adult femur or the sequelae of a subclinical, minimum, acute or chronic slip. The post-slip morphology may represent the pre-slip lesion seen in adolescents that often predisposes to slipped capital femoral epiphysis in the presence of risk factors such as obesity, hormonal imbalance, trauma, and possible weakening of the perichondrial ring. The osteoarthrosis was more severe in the hips with post-slip morphology than in the control hips and, in the skeletons with unilateral post-slip morphology, it was more severe in the involved hips than in the contralateral, normal hips. The finding in the involved hips in the skeletons with unilateral post-slip morphology indicated a stronger correlation because factors such as obesity, activity, and metabolic disease were controlled. Finally, high-grade osteoarthrosis did not develop in all of the hips with post-slip morphology in the skeletons from individuals who had been fifty-six years old or more, suggesting that factors other than post-slip morphology determine which hips are at risk for osteoarthrosis.
Slipped capital femoral epiphysis is a disorder of the adolescent hip of unknown etiology, and many slips are clinically silent or only slightly symptomatic2,5,9,10,21,22. The results of the present study show that the femora with post-slip morphology had the same epidemiological characteristics as femora associated with slipped capital femoral epiphysis30. The known annual incidence of slipped capital femoral epiphysis in the general population30 is about two per 100,000. Kelsey et al.14 reported an annual incidence of 3.4 per 100,000 in Connecticut and 0.7 per 100,000 in New Mexico. Those authors noted that, in Connecticut, the annual incidence per 100,000 population in the age-group of twenty-five years old or less was 7.8 per cent for black male patients, 6.7 per cent for black female patients, 4.7 per cent for white male patients, and 1.6 per cent for white female patients. Kelsey et al. reported a 2.5:1 male-to-female ratio on the basis of a study of 252 patients, whereas we found a male-to-female predominance of 1.3:1. Other authors2 have reported prevalences ranging from 1.7:1 to 5.8:1. The reported prevalence14,32 of bilateral slips has ranged from 20 to 80 per cent. Hägglund et al.10 noted a bilateral slip in 159 (61 per cent) of 260 patients. In the present study, 122 (57 per cent) of the 215 skeletons that had post-slip morphology had it bilaterally. The left hip is affected more than twice as often as the right in patients who have slipped capital femoral epiphysis10. In the study by Hägglund et al.10 169 of 237 unilateral slips were on the left (2.5:1), and in our study sixty-nine of ninety-three slips were on the left (2.9:1).
Carney et al.3 concluded that the natural history of a minimum slip is mild deterioration with time related to the severity of the slip and complications. They found that hips with a minimum slip that had been followed for forty to forty-nine years had good scores; however, since the patients were still relatively young (fifty to sixty years old), they may have just been reaching the age when clinically important osteoarthrosis starts to become apparent.
The post-slip morphology and the wear pattern of the post-slip osteoarthrosis may give a clue as to the pathophysiology of osteoarthrosis in these hips. One hypothesis is that the abnormal post-slip morphology exposes the prominent anterior metaphyseal portion of the femoral neck to the anterior surface of the acetabulum during flexion and internal rotation, producing greater wear in this region, which eventually progresses to global osteoarthrosis.
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Footnotes
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*No benefits in any form have been received or will be received from a commercial party related directly or indirectly to the subject of this article. No funds were received in support of this study.
Department of Orthopedics, University Hospitals of Cleveland, 11100 Euclid Avenue, Cleveland, Ohio 44106. Please address requests for reprints to Dr. Goodman.
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References
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Abstract
Introduction