JOSEPH M. WINSTON, M.D.2 and JAMES S. HEWSON, M.D.3 T HE EARLY ROENTGEN diagnosis of tuberculosis of the hip in children has received little attention in recent radiologic literature. This is primarily due to the decline of tuberculosis in this country and the advent of the antituberculous chemo- therapeutic agents. However, the disease is far from eradicated; new cases are still being seen, often after irreversible changes have occurred. The usual end-result of tuberculous dis- the principal distinguishing features of tuberculous arthritis. Since it appears that these criteria are not widely known, re- statement and further illustrations seem indicated. During the past fifteen years, there have been seen at the Alfred 1. duPont In- stitute 9 patients with early roentgen changes in the hips in whom there was microscopic proof of tuberculosis. Not included in this series are 3 cases which Fig. 1. A. Four-and-a-half-year-old white girl with intermittent discomfort in left hip for two and a half years. There was a difference in density of the femoral heads. Note cupping of acetabular fossa. B. Solid fusion eight years after onset. Lead shields the gonads. ease of a joint has been ankylosis (1) . There is a reasonable chance, however, since the discovery of antibiotics, of ob- taining a mobile joint if the disease is recognized in its early stage. It is im- portant, therefore, to be constantly re- minded of the methods of making an ac- curate diagnosis of this disease in children) to familiarize oneself with the early diag- nostic signs and symptoms, and to be aware of the differential diagnosis in their pres- ence. In 1924, Phemister (26) recorded clinically and roentgenographically were thought to be tuberculosis but in which either biopsy was not performed or the biopsy report and/or culture were negative. Also excluded are patients with well ad- vanced and of ten healed tuberculosis of the hip, admitted for reconstructive surgery. This paper will be limited to a discussion of early tuberculosis ofthe hip in children. Earlier literature, particularly in the nineteen twenties and nineteen thirties, is filled with reports of excellent results of 1 From the Departments of Radiology and Orthopedic Surgery, Hospital of the University of Pennsylvania, Philadelphia, Penna., and Alfred 1. duPont Institute of the Nemours Foundation, Wilmington, De1. Presented at the Forty-seventh Annual Meeting of the Radiological Society of North America, Chicago, Il1., Nov. 26-Dec. 1, 1961. 2 Now at Jeanes Hospital, Philadelphia, Penna. Instructor in Radiology, University of Pennsylvania. 3 Resident in Orthopedic Surgery, University of Pennsylvania. 241 242 JOSEPH M. WINSTON AND JAMES S. HEWSON Fig. 2. A. Normal right hip in 2-year-old boy with a mass over the left hip and limp of recent onset. The left hip was held in a position of flexion. B. Generalized demineralization of hip. There is widening of the epi- physeal plate with irregularity of the adjacent bony surfaces. Note cystic change in the femoral neck. C. Lateral view of left hip showing widened epiphyseal line and periosteal reaction. See Fig. 2, D for follow-up, August 1962 treatment of tuberculosis of the hip. Rollier (3), for instance, in 1930 reported 74 per cent cures, with function of the hip joint. Not' all the cases, however, were verified by tissue biopsy or bacteriologic examination. In 1921, Sundt (4) stated that in a series of 243 cases of hip disease seen from 1903 to 1918, 29.6 per cent were nontuberculous. Among these were cases of congenital coxa vara, epiphysiolysis, fracture, arthritis deformans, osteomyelitis, syphilis, synovitis of tuberculous origin, hysteria, and Legg-Perthes disease. Neil- son (5) in 1923 gave a differential diagnosis of hip conditions which had been .con- sidered tuberculous. In 1930 O'Connor (6), reviewing 189 cases admitted with a tentative diagnosis of tuberculosis, found 54 that were not tuberculous. The follow- ing year Milgram (7) reported that, of 88 cases of Legg-Perthes disease, 31 had been diagnosed as tuberculosis on the first admission. In addition} proved tuberculo- sis was initially misdiagnosed in 38.. 7 per cent of 142 patients. Those cases with an insidious onset were incorrectly diagnosed 29 per cent of the time, those with a sudden onset were incorrectly diagnosed 61.9 per Vol. 79 EARLY DIAGNOSIS OF TUBERCULOSIS OF THE HIP IN CHILDREN 243 cent of the time, and at operation tuber- culosis was apparently unrecognized 67.3 per cent of the time. The roentgen diag- nosis of tuberculosis of the hip was missed 41.9 per cent of the time. Barr (8) re- ported on 106 consecutive cases in children and found that in 15 per cent the admission diagnosis was incorrect. PATHOGENESIS Tuberculosis of the skeleton is a sign of generalized disease and practically always arises as a result of hematogenous spread from primary foci in other regions (9, 10). In children the primary infection is usually in the lungs and the tracheo- bronchial lymph nodes (11). Campos (12) found that, of 500 cases of skeletal tuberculosis which he reviewed, 57 per cent had normal chest roentgenograms. Six of our patients had roentgen changes in the chest suggestive of tuberculosis. It is postulated that in children tuberculosis occurs about the hips because of the proportionately large blood supply to this rapidly growing area. The frequency of involvement of the metaphysis is due to the lodging of the bacilli in the end arteries in this region of the bone (11). Tuberculosis of the hip in children has a high incidence, accounting for about 20 per cent of cases of bone and joint tuberculosis (13). Buzby (14), in 1922, reported that 92 per cent of his cases of tuberculosis of the hip began before ten years of age and were always secondary to a focus elsewhere. Ponseti (15), in 1948, analyzed 31 cases of proved tuberculosis and found the age of onset ranging from one to twelve years. Tuberculosis in children may affect the hip joint in either of two ways (15). In young children the lesion mayat first be para-articular, with the joint space itself only gradually becoming involved. The most common sites of para-articular involvement are the femoral neck, the ilium on the pelvic side of the acetabular roof, and the junction of the shaft and neck. The other type involves the joint itself. The extra-articular foci of tuberculous osteitis are seen more often in children and Fig. 2. D. Same case as Fig. 2, A-C. Follow-up approximately one year later. very rarely in adults. In both types, it is probable that synovial membrane and bone are involved from the start, but in young children the bone lesion is more apparent initially and in the older person the synovial lesion. Wilkinson (16) re- ports that all patients with bone involve- ment had synovial changes. CLINICAL HISTORY The usual onset of tuberculosis of the hip is gradual and insidious. Indeed, as reported by Iversen (17) in 1937, it often starts without a demonstrable source. Dsually a limp precedes pain and there develops a stiffness of the involved hip. The affected leg is often shorter than the sound one (18). Muscle spasm may occur in an attempt to splint the joint. Night cries are provoked by the pain and sudden discomfort following the muscle relaxation that occurs with rest. The pain is re- ferred either from the inner aspect of the 244 JOSEPH M. WINSTON AND JAMES S. HEWSON August 1962 Fig. 3. A. Eighteen-month-old girl with a six-month history of limp and pain in the left lower extremity. The hip was held in external rotation. The initial study demonstrates subluxation of the left hip. The arrow indicates metaphyseal changes. There is evidence of periosteal production along the shaft. B. Periosteal production seen better on lateral projection. C. Seven days later. Note rapid progression of destructive changes in the metaphysis. D. Two months later. Further changes in the femoral head and meta- physes. See Fig. 3, E for follow-up. thigh to the knee, in the distribution of the obturator nerve, or to the anterior surface of the thigh, following the course of the femoral nerve. The patient often becomes worse as the day progresses. Usually there is some lumbar lordosis on standing erect. Typically, there are a rise in temperature of 1 1/2 to 2 0 in the eve- ning, some anorexia, and malaise. Six of our 9 patients complained of a limp and 7 presented with pain. Less fre- quent symptoms were night cries, fever, and lethargy. Limitation of motion was the most fre- quent finding on initial physical examina- tion. In the early stages this is usually due to reflex muscle spasm. Later it may be the result of actual pain on motion of the joint. Initially the extremity is flexed at the hips, abducted, and externally rotated. In this position the joint capsule is re- laxed, and the pain is relieved. As the disease progresses, the hip becomes ad- ducted and internally rotated as well as flexed. Atrophy of the muscles of the affected limb is a constant finding. Swelling due to Vol. 79 EARLY DIAGNOSIS OF TUBERCULOSIS OF THE HIP IN CHILDREN 245 periarticular inflammation may occur in any area about the hip. DIAGNOSIS Since there is a reasonable chance of obtaining a mobile joint if the disease is recognized in its earliest stages, early diag- nosis is imperative. In addition to the clinical history and physical findings, blood studies, skin tests, roentgen studies, and biopsy are helpful diagnostic aids. 1. Blood Studies: The white blood count and sedimentation rate are not specific, but an increase in the sedimenta- tion rate, a decreased hemoglobin and red count, and an increased white blood count are helpful laboratory findings. 2. Skin Test: The Mantoux skin test is of value only if negative on repetition. Mills et al. (19) reported that of 35 proved cases 34 gave a positive reaction, while of 20 patients with nontuberculous disease of the hip only 5 had positive reactions. 3. Roentgen Studies: The roentgeno- graphic changes can be divided into osseous, intra-articular, and peri-articular soft-tissue. Early roentgen changes include osteo- porosis, rarefaction, or merely the slightest alteration in density of the upper femur and iliac bones. More advanced changes con- sist of erosion of the acetabular surface, areas of cancellous bone destruction, ab- scesses or small cyst-like areas of bone destruction, widening of the zone of in- creased density of the acetabulum, hernia- tion of the acetabulum, and periosteal proliferation. The primary location of the disease, ac- cording to Badgley and Hammond (28), was in the acetabular area in 50 per cent, in the femoral epiphysis in 32 per cent, in the neck of the femur in 14 per cent, and in the greater trochanter in 4 per cent. Dobson (21), reported on 320 cases, of which 39.3 per cent involved the acetabu- lum, 34.1 per cent the acetabulum and femoral head, 19.2 per cent the head of the femur, and 7.4 per cent the femoral neck. Cholmeley (22) found 44 per cent located in the acetabulum, 2 per cent in the epi- Fig. 3. E. Same case as Fig. 3, A-D. Residual deformity at time of follow-up study four years later. physis, 17 per cent in the neck, and 2 per cent in the greater trochanter. Areas of contact of joint cartilage con- stitute a barrier to the extension of the disease and cause destruction to take place first at the joint margins where there is little or no contact or pressure. The destruction of articular cartilage by granulation tissue is characteristically slow in tuberculosis owing to the lack of pro- teolytic enzymes in the tuberculous exu- date. Since the destruction of bone follows the destruction of the overlying cartilage, bone changes are first seen in the peripheral and non-contact areas; the subchondral bone, like the articular cartilage, is well preserved in the regions of contact. As a result, the main force of the destructive lesion may manifest itself at points rela- tively remote from weight-bearing surfaces (10). Tuberculosis as a primary focus in the neck of the femur usually occurs as a 246 JOSEPH M. WINSTON AND JAMES S. HEWSON , ,It;u!,, . H . i t'; 'I' . . \\ n,' ...... ...,'
Fig. 4. A. Difference in density on two sides difficult to demonstrate on reproductions but very apparent on films. Such a difference is easily over- looked if films are not of excellent quality and if index of suspicion is not high. B. Decreased density of right hip. Note cystic changes in the acetabular fossa. C. Thirty months later. Note flattening of the femoral head, advanced cystic changes in the acetabular fossa, and reaction at edge of acetabulum. August 1962 circumscribed area of bone destruction in the metaphysis, and characteristically ap- pears as a wedge-shaped area upon the under surface of the fem.oral neck just distal to the epiphyseal line (9), in the distribu- tion of the infero-rnesial neck artery (26), with or without periosteal proliferation. In the acetabular region, destruction occurs in a posterior mediallocation (23). Odelberg-Johnson (27), divided the bone changes into 3 stages. In the first there is a loss of lime salts involving the entire hip region. The contours of the joint and the articular cartilage are preserved in this stage and there is some question of whether. Shenton's line is broken. Femoral growth is often disturbed so that the shaft involved is narrower and the cortex thinner than on the normal side. During the second stage, which includes the second year of illness, there is more pronounced bone atrophy, with blurred spongiosa, and there are ill-defined defects in the joint contour. The femur is dislocated upward and laterally, the articular cartilage becomes destroyed, and there is more pronounced shaft growth disturbance. In the third stage, which occurs not before the end of Vol. 79 EARLY DIAGNOSIS OF TUBERCULOSIS OF THE HIP IN CHILDREN Fig. 5. A. Seven-year-old girl with limp in the left leg for one year. Note irregularity to acetabular fossa. There is no evidence of swelling of the joint capsule. B. Two months later the changes in the acetabular fossa are more promi- nent. C. Ten months later. D. Evidence of good healing eight years after onset of symptoms. 247 the second year, there is beginning repair, and the destroyed areas are sharply de- fined, with sclerotic borders. At this stage there is an increased lime content and the spongiosa is more distinct. There may be an associated slight increase in the joint space due to distention with fluid. As mentioned above, tuber- culous exudate does not contain proteolytic enzymes, and cartilage therefore persists until later stages, when it is covered with a pannus of unhealthy granulation tissue (13). As a result, reduction in the depth or disappearance of the cartilage space is characteristically of late occurrence in tuberculous arthritis. The articular capsule may appear swollen, with associated thickening of the 248 JOSEPH M. WINSTON AND JAMES S. HEWSON August 1962 adjoining subcutaneous tissue. The swell- ing may be due to inflammation of the periarticular tissue or possibly infiltration of soft structures or a cold abscess. There may be widening and change in the con- tour of the shadow of the normal obturator internus muscle. This is due to dis- placement of the tendon of the obturator muscle as it passes adjacent to the ex- panded hip capsule. The leg may be in a position of flexion. Subluxation is not rare and, if it has oc- curred, further enhances the appearance of a narrowed joint space. Dislocation is thought to be due to a combination of muscle spasm plus the pressure of the head on the softened acetabulum, causing the head to travel upward and backward, with dislocation onto the posterior ilium. CULTURE AND BIOPSY The final method of diagnosis consists in obtaining material for culture and/or microscopic examination. Where there is evidence of synovial effusion into the joint or abscess formation, aspiration may be of help (25). The aspirated fluid should be examined microscopically, cultured, and inoculated into guinea-pigs. Unfor- tunately many patients will have no effu- sion. Even when fluid is obtainable, the results of culture are often nonconfirrn- atory. Fluid was obtained in 5 of our 9 patients and was positive in 3. Petragnani and Dubos preparation appeared to be the best culture media. Biopsy of regional lymph nodes may yield valuable information in a relatively high percentage of cases (24), particularly in the period between the third and fif- teenth months of the disease. The lymph drainage from the hip is not to the inguinal region, but to the iliac group and, there- fore, if node biopsy is attempted, it must be in the latter area. Lymph node biopsy is now rarely necessary because of the safety and greater accuracy of biopsy of the affected joint itself (22). DIFFERENTIAL DIAGNOSIS Differential diagnosis includes Legg- Perthes disease, nontuberculous infection, acute and chronic arthritis, congenital dislocation of the hip, and slipped epiphy- sis. Legg-Perthes disease clinically may simulate tuberculosis. Pain, limp, slight shortening of the leg, and mild muscular atrophy are present, although usually to a lesser degree. There is no limitation of extension and flexion is freer. In contrast to tuberculosis, the general condition of the child is good. Roentgenographically the changes, limited mainly to the epiphysis, consist of irregularity in density, fragmen- tation' and compression. The femoral neck may become shorter and broader. At no time is there actual destruction of the articular cortex. In 1924, Phemister (26) recorded points which still stand as the principal dis- tinguishing features of tuberculous and nontuberculous suppurative arthritis. In pyogenic arthritis the articular cartilage is destroyed and broken down first at the point of contact and pressure of opposing articular surfaces. The infectious pro- teolytic ferments assist greatly in the rapid removal of the necrotic cartilage. As a result, there is early narrowing or disappearance of the joint space, and the earliest bone destruction occurs on the opposing or weight-bearing portion of the articular surfaces. In tuberculous arthritis the articular cartilage is not destroyed first but rather is protected at the point of contact and pres- sure of opposing articular surfaces. The earliest destruction is peripheral, along the free surfaces where tuberculous granuJlation can grow and remove the dead tissue. The first disappearance of the bony cortical shadow is usually seen peripherally about the margins of the weight-bearing portions of the articular surface where there has been absorption by the granulation. As a result, reduction in the depth of the joint space is characteristically late. Congenital dislocation of the hip may be confused clinically with tuberculosis. Ab- sence of pain, tendency to favor the affected limb, and unaltered general state are in favor of dislocation of the hip. Roent- Vol. 79 EARLY DIAGNOSIS OF TUBERCULOSIS OF THE HIP IN CHILDREN 249 genographically, the femoral neck is directed above the acetabulum which may be shallow. The epiphysis, if calcified, is in a high position and may show flattening owing to the abnormal pressure. In slipped femoral epiphysis the epiphy- seal line is wide and irregular with upward and forward displacement of the neck on the head of the femur. There may be anterior bowing of the neck and new bone may form between the lower border of the neck and the overhanging head. SUMMARY An insidious onset of pain, limp, and stiffness associated with limitation of motion and roentgen findings of rare- faction and the slightest alteration in density of the upper femur and iliac bones should make one suspicious of early tu- berculous involvement of the hip. It is hoped that more lesions will be recognized early, in order that a mobile joint may be the end-result and ankylosis the rarity. Jeanes Hospital Fox Chase Philadelphia 11, Penna. REFERENCES 1. CHOLMELEY, J. A.: Femoral Osteotomy in Extra-articular Arthrodesis of the Tuberculous Hip. J. Bone & Joint Surg. 38-B: 342-352, February 1956. 2. POMERANZ, M. M.: Roentgen Diagnosis of Bone and Joint Tuberculosis. Am. J. Roentgeno1. 29: 753-762, June 1933. 3. ROLLIER, A.: Conservative Treatment in Sur- gical Tuberculosis of the Lower Extremity. J. Bone & Joint Surg. 12: 733-748, October 1930. 4. SUNDT, H.: Tuberculous Hip Disease and Its Simulants. Tubercle, London 2: 289-299, 1920-1921. 5. NIELSON, A. L.: Abortive Type of Tubercu- lous Hip Joint Disease. J.A.M.A. 80: 1442-1443, May 19, 1923. 6. O'CONNOR, D. S.: Tuberculosis of the Hip Joint; End Result Study. New England J. Med. 203: 636-641, Sept. 25, 1930. 7. MILGRAM, J. E.: Diagnostic Inaccuracy in Tuberculosis of the Bone, Joint, and Bursa. J .A.M.A. 97: 232-235, July 25, 1931. 8. BARR, J. S.: Tuberculosis of the Hip in Chil- dren. 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DE F. : The Early Diagnosis of Joint Tuberculosis. J.A.M.A. 83: 1569-1573, Nov. 15, 1924. 25. MERCER, W.: The Management of the Tuber- culous Hip Joint. J. Bone & Joint Surg. 36-A: 1123- 1128, December 1954. 26. PHEMISTER, D. B., AND HATCHER, C. H.: Correlation of Pathological and Roentgenological Findings in the Diagnosis of Tuberculous Arthritis. Am. J. Roentgenol. 29: 736-752, June 1933. 27. ODELBERG-JOHNSON, G.: Different Types of Tuberculosis of the Hip in Children. Acta orthop. scandinav. 9: 197-209, 1938. 28. BADGLEY, C. E., AND HAMMOND, G.: Tuber- culosis of the Hip; Review of 76 Patients with Proved Tuberculous Arthritis of 77 Hips Treated By Arthro- desis. J. Bone & Joint Surg. 24: 135-147, January 1942. (Pro le summario in interlingua, vider le pagina 263)