ULTRASONOGRAPHY IN THE EARLY DIAGNOSIS OF HIP JOINT INVOLVEMENT IN JUVENILE RHEUMATOID ARTHRITIS

MELANIA S. FEDRIZZI, MARCOS V. RONCHEZEL, MARIA ODETE E. HILÁRIO, HENRIQUE M. LEDERMAN, SÔNIA SAWAYA, JOSÉ GOLDENBERG, and DIRCEU SOLÉ

From the Division of Allergy, Clinical Immunology and Rheumatology, Department of Pediatrics, Escola Paulista de Medicina, Universidade Federal de São Paulo, Brazil.

M.F. Fedrizzi, MD, Post Graduate, Division of Allergy, Clinical Immunology and Rheumatology, Department of Pediatrics; M.V. Ronchezel, MD, Assistant Professor, Division of Rheumatology, Department of Pediatrics, Santa Casa de Misericórdia de São Paulo; M.O.E.Hilário, MD, Associate Professor, Division of Allergy, Clinical Immunology and Rheumatology, Department of Pediatrics; H.M.Lederman, MD, Professor of Radiology, Department of Diagnostic Imaging, Escola Paulista de Medicina; S.Sawaya, MD, Pediatric Rheumatologist, Hospital do Servidor Público Estadual de São Paulo; J. Goldenberg, MD, Associate Professor, Division of Rheumatology, Department of Medicine; D.Solé, MD, Associate Professor, Division of Allergy, Clinical Immunology and Rheumatology, Department of Pediatrics, Escola Paulista de Medicina, Universidade Federal de São Paulo. Address reprint requests to Dra. M.O.E. Hilário, Alameda dos Anapurús, 1370 ap 144, São Paulo, SP, 04087-004, Brazil

ABSTRACT.

Results. Conventional radiography showed alterations in 10 patients (18.9% )who had shown clinical manifestations of advanced stage disease of the hip joint, while ultrsound detected abnormalities in asymptomatic patients wjo had had normal radiographs. Ultrasound revealed the occurrence of 47.2 % involvement in the hips of patients with JRA. Thus, ultrasound was apparently more sensitive than conventional radiographs in diagnosing changes in the hip joints of patients with JRA. Further, such involvement was found with greater frequency in the systemic and polyarticular types of JRA, in children less than 5 years of age, in those with longer duration of disease, and in those who belonged to a poorer functional class. In 3 of 9 patients who initially had normal radiographs and altered ultrasound, we found severe hip alterations upon reevaluation by radiograph, after a period ranging from 21 to 39 months.

Conclusion. Ultrasonography is a method of diagnosis that must be considered in hip joint evaluation of patients with JRA.

Key Indexing Terms:

JUVENILE RHEUMATOID ARTHRITIS HIP JOINT

ULTRASONOGRAPHY RADIOGRAPHY

INTRODUCTION

Hip joint involvement in juvenile rheumatoid arthritis (JRA) is a poor prognostic factor, since the hip is a weight-bearing joint in which anatomical deformities can cause serious disabilities. In the literature, the incidence of hip joint involvement in JRA ranges from 38 - 63% of patients ^1-4. Brewer et al refer to hip joint involvement 63% of the time in the systemic-type onset, 48% of the time in polyarticular onset, and 36% of the time in pauciarticular type ¹. Ansell and Unlu report that hip joint involvement is relatively common in children with chronic arthritis, especially in very young children in the early stages of the disease. It is also common when the disease remains active for many years. When hip joint involvement occurs late, it is generally due to disease flares⁵. While in the growth phase the human skeleton is composed largely of cartilage not visible in the conventional radiographs, making evaluation of progressive changes such as loss of cartilage or joint space or the presence of joint effusion difficult⁶. In conventional radiographs, joint effusion is recognized primarily through displacement of the fat planes adjacent to the joint. While it can be easily diagnosed in the elbows and knees, effusion in the hip joint is not possible due to anterior localization of the fat planes⁶.

Ultrasonography has been used in the evaluation of joint disease. It is quick, easy, and non-invasive, and radiation-free. In 1980, Seltzer et al used ultrasound on 4 adult patients with "painful hip syndrome"⁷. In 3 patients they injected the hip with contrast material via arthrography: one patient received approximately 14 ml of anesthetic. The ultrasound images showed an echo-free (anechoic) area of 7 to 9 mm between the femoral head and the ileofemoral ligament, which we shall call the ultrasonographic joint space (UJS). The UJS was not seen on the noncontrasted side⁷. The UJS is composed of the synovial membrane, which has a thickness of roughly 3 mm, and a minimal quantity of synovial fluid. Joint effusion or thickening in the synovial membrane distends the joint capsule and increases the UJS.

Our aim was to determine the value of ultrsound in the detection of early alterations and the subsequent evolution of hip joint disease in patients with JRA.

MATERIALS AND METHODS

-Patients - Fifty-three patients fulfilling the American College of Rheumatology diagnostic criteria for JRA were randomly selected between August and December of 1993. The group consisted of 27 (51%) males and 26 (49%) females, ranging in age from 2 and 16 years (median 9). Age at onset of disease ranged from 2 to 13 years (median 6). Duration of the disease ranged from 0.5 to 11 years (median 3). Systemic-type onset was present in 9 patients (17%); polyarticular onset in 18 patients (34%); and pauciarticular onset in 26 patients (49%). The evolutive type was systemic in 2 (4%), polyarticular in 25 (47%), and pauciarticular in 26 patients (49%). Thirty-eight patients (71.7%) belonged to functional class I, 11 patients (20.7%) to class II, and 4 patients (7.6%) to class III. Ten children free of the signs/symptoms related to rheumatic diseases between the ages of 4 to 12 years (median 8 yrs and 6 mo) were chosen for a control group.

-Clinical evaluation - Patients with JRA were evaluated according to age at the onset, type of onset, evolutive type, disease duration, functional class (I - IV)⁸ , and clinical alteration of the hip joint, if any.

-Radiographic evaluation - A radiograph of the pelvis in the anteroposterior position, with the patient in a supine position, was taken in each case. The radiograph were then evaluated by a radiologist who had no prior knowledge of the history or examination result of the patient. The radiographic study included an analysis of the femoral head and acetabulum to detect the osteopenia, erosions, subchondral cysts, sclerosis, alterations of development, and subluxation of the femoral head. Symmetry of joint spaces was also verified.

-Ultrasonographyc evaluation - The 53 patients with JRA and the 10 control group children underwent ultrsound of both hip joints. These were performed in the supine position with the legs extended and minimal internal rotation. A transducer of 7.5 MHz was placed longitudinally to the axis of the femoral neck. The examination proceeded in a lateral to medial direction across the hip joint, identifying the acetabular border, the femoral head and neck, and the ileofemoral ligament (Figure 1). The disease was considered present when the ultrasound showed distension of the joint capsule (convex form), increased echogenicity, and UJS greater than 0.6 cm (Fig 2). This value was obtained through a statistical analysis of the control group, in which the average UJS was 0.5 ± 0.05 cm. Therefore, utilizing 2 standard deviations we obtained an average of 0.5 ± 0.1 cm. The normal side difference between the hips was 0.05 cm.

-Re-evaluation - Nine of the 15 patients with normal initial radiographs and ulktrasound that revealed alterations were re-evaluated 28 mo after baseline. The clinical, radiological and ultradsound evaluation were repeated.

-Statistical method - Statistical analysis was performed using the Wilcoxon test, analysis of variance (Kruskal-Wallis rank), McNemar test, and Chi-squared test. A p-value of 0.05 was considered statistically significant.

RESULTS

Significant clinical manifestations of hip-joint involvement were pain, claudication, and a limited range of motion in 7 joints (6.6%). A limited range of motion alone was observed in 26 joints (24.5%). Radiographic examination of the hip joint, revealed abnormalities in 20 joints (18.9%) which included osteopenia and subchondral erosions on the femur and acetabulum, and narrowing of the joint space. The UJS ranged from 0.7 to 0.9 cm (mean - 0.8 cm) in patients with systemic JRA, 0.5 to 1.4 cm (mean - 0.7 cm) in patients with polyarticular JRA, and from 0.4 to 1.0 cm (mean - 0.6 cm) in patients with pauciarticular JRA. UJS in the control group ranged from 0.4 to 0.6 cm (mean - 0.5 cm). An increase in UJS was observed in 2 patients (100%) with systemic JRA, in 16 (64%) with polyarticular JRA (bilateral in 15 cases and unilateral in one case), and in 7 (27%) with the pauciarticular JRA (4 bilateral and 3 unilateral). The evolutive systemic type patients were excluded because to sample size was too small for proper statistical analysis. The measurements of UJS for the polyarticular and pauciarticular types were statistically different from those of the control group.

In table 1, we note that the evolutive systemic and polyarticular types show more alterations on conventional radiographs and ultrasound. However, in the pauciarticular type we found no alterations on radiographs alone, while 11 joints (21% ) presented abnormalities on ultrasound. When we compered the radiographic and ultrasound findings to the clinical characteristics of JRA, we found that in patients under 5 years of age (table 1), who had had the disease for 3 yrs or more and/or who belonged to functional class III, there was greater involvement of the hip joint. Furthermore, we noted that the radiographs were normal in all of the asymptomatic patients and in some of the patients who presented clinical manifestations of hip joint involvement. Twenty-one asymptomatic joints (19.8%) presented alterations on ultrasound. Finally, we observed that in all cases where the radiograph revealed changes, the ultrasound also showed alterations, while in 26 joints where the radiograph was normal the ultrasound demonstrated some degree of alteration (table 1).

Clinical, radiographic, and ultrasound re-evaluation of the 9 patients who initially presented with normal radiographs but an altered ultrasound was performed after an average of 28 mos (table 2). We found that 3 of these patients had developed severe radiographic alterations of the hip joint during that period (range of 21 - 39 months). While 2 of these patients had already presented clinical alterations during the initial evaluation, the 3rd patient only presented clinical manifestations and radiographic changes later. The ultrasound abnormalities we detected in these 3 patients were an increase in the UJS and changes in the echogenicity of the joint capsule. In addition, 4 patients still presented ultrasound changes in spite of their normal clinical and radiographic examinations. It should be noted that 3 presented an active form of the disease and were taking nonsteroidal anti-inflammatory drugs and methotrexate (in 2 cases) or sulfasalazine (in one case). The 2 cases in which re-evaluation failed to reveal any alteration of the hip joint had been in clinical remission for at least 2 yrs.

Table 2 indicates that the changes in clinical presentation were, in Patient 3, a slightly limited range of motion in the right hip during the first evaluation and pain, claudication, and a significant reduction in range of motion in both hips on followup; in Patient 4, pain and a reduced range of motion in both hips initially, with subsequent pain, claudication and more complete restriction of all posterior movements of the hip joints upon re-evaluation; and in Patient 9, pain and limited internal rotation of the hips bilaterally during re-evaluation. For the same patients, the radiographic changes detected during the re-evaluation were, in Patient 3, bone erosion, cysts, osteopenia, sclerosis, changes in morphology of the femoral head and acetabulum, narrowing of the joint spaces bilaterally, and subluxation of the left femoral head; in Patient 4, bilateral erosion of bone on the femoral heads and acetabuli, a bone cyst on the left femur, sclerosis, and narrowing of the joint space; and in Patient 9, bilateral erosion of bone and cysts on the femoral heads and acetabuli (more pronounced on the left), osteopenia, and an overall alteration in the morphology of the left femoral heads.

DISCUSSION

The clinical characteristics of our patients with JRA, such as the age at onset (median 9 yrs), and lack of diferentiation between the sexes, are similar to those of previous reports⁹. A large percentage of our patients originally presented characteristics of the pauciarticular type: few joints affected and good overall and evolutive prognoses. The second most frequent type was polyarticular, which generally involves significant alteration of the joints. Although others have found that 25% of patients with the systemic type develop into the polyarticular, in our sample 7 out the 9 such patients (78%) showed this progression. This discrepancy must be due to the size of our sample and not to differences in our population.

The clinical manifestations of hip joint involvement were present in approximately 30% of the patients, in most cases bilaterally. Typically, the pain occurs due to distention of the joint capsule, synovitis, or formation of the characteristic "pannus". It can be localized anywhere around the joint or referred to the knee. Limited range of motion can be secondary to pain, synovitis, and/or joint swelling. However, the clinical presentation does not always reveal the true extent of involvement of the hip joint, such that it is possible to have significant abnormalities without patient complaints^10,11.

Radiographic changes were detected bilaterally in the hip joints of 10 patients. All presented the same abnormalities. While periarticular osteoporosis is the earliest change, it is rather subjective and non-specific since it depends heavily on the choice of techniques and the professional interpretation of the study. Moreover, it can result from treatment with corticosteroids, inflammatory process, and/or general disease. As the disease progresses, the inflammatory process results in erosion of the cartilage and subchondral bone of the femoral heads and acetabuli, narrowing the joint spaces. Such changes generally occur late in the disease^2,3,11.

The time lapse for the development of such radiographic changes in our patients was about 6 yrs (range 2-11 yrs). Furthermore, these patients were diagnosed as having the systemic and polyarticular types of the disease. Jacobsen et al found that such destructive radiographic lesions are rare in the pauciarticular type of JRA. In the systemic and polyarticular types, however, they observed abnormalities in 10% of their patients after 5 yrs of disease ¹².

The use of ultrasound for the evaluation of hip joint involvement in JRA is relatively recent, and the research is scant. We used a high-frequency transducer (7.5 MHz), with its shorter wavelength, given the depth of the area under study, and the extent of penetration ^13,14 and level of details that our study required.

In the control group, we evaluated a total of 20 hip joints in children with no sign or symptom of rheumatic disease. The mean width of the UJS to be 0.5 ± 0.05 cm. Our results are similar to those of Egund, et al, who studied a total of 38 hips in normal children with ultrasound and computed tomography (CT) and found the mean width of the UJS to be 0.54 ± 0.08 by CT and 0.53 ± 0.07 cm by ultrasound¹⁵. In 1991 Bialik, et al evaluated the hips of 18 children and 7 normal adults, finding similar mean values for the UJS ¹⁶ and confirming the earlier data of Wingstrand et al ¹⁷.

In this study, we evaluated 106 hip-joints in 53 patients with JRA and found 46 joints (43.4%) with an UJS greater than 0.6 cm, which is consistent with the findings of others studies ^15,18,19.

Kallio, et al studied 166 hip-joints in children with transient synovitis, Perths’ disease, osteomyelitis, and septic arthritis, and found 97 hips with effusions. In each case, the UJS measured greater than 0.6 cm ¹⁸. In 1986 Adam, et al found effusions in 52 hip joints in 87 children, and found the UJS to be 0.63 ± 0.15 cm ¹⁹. Egund, et al studied the hips of children with joint effusions, compared ultrasound and CT results, and found the mean CT measurement of the UJS to be 0.85 ± 0.17 cm, while the mean ultrasound measurement they obtained was 0.90 ± 0.19 cm ¹⁵.

We found 25 patients (47.2%) with significant changes in hip joints. This rather high percentage is comparable to results described by other authors: Jacqueline, et al, 63.5% ³, Isdale, 38% ², Rombouts and Rombouts-Lindemans, 34% ²⁰, and Woo, et al about 40% ²¹. In the majority of our cases, the hip joint alterations were bilateral. Furthermore, in 100, 94, and 51%, the hip joint alterations were of the evolutive systemic type, polyarticular type, and pauciarticular type, respectively. Thus, our findings of bilateral involvement and higher frequency of changes in the systemic and polyarticular types are consistent with those of other studies ^{1,2,12,22,23,24}.

We found that among the patients who developed the disease before the age of 5 yrs, a majority presented involvement of the hip joint. This is consistent with the hypothesis that involvement of the hip joint is greater in proportion to the precocity of onset of the disease ^5,25.

In analyzing the evolutionary time frame of the disease, we observed that patients who had had the disease for longer than 3 years presented a higher frequency of changes in the hip joint. Clearly, the longer the course of the disease, the higher the risk of changes in the joints involved; however, time is not the only factor. Type of onset, evolutive type, and disease activity are also important ².

The most common criteria for the evaluation of the functional states in the evolution of JRA are those of Steinbrocker et al ⁸. Functional capacity is associated with the disease duration and also with the type of JRA onset. Functional classes III and IV are seen more frequently after longer disease duration in both the evolutive systemic and polyarticular types, and are associated with a higher incidence of hip joint involvement, as confirmed by our study. These findings are consistent with those of previous reports ^2,12,23.

In comparing radiographs with ultrasonographic studies, we found that all the patients with radiological abnormalities also presented signs and symptoms of hip joint involvement. However, of special significance was that many patients with no clinical manifestations and/or normal radiographs presented changes on ultrasound. Such findings may be considered of great importance in the diagnosis and followup of these patients, since involvement of the hip joint is an indication of poor overall prognosis and implies severe functional disabilities. Moreover, in some of these cases, we detected severe radiographic changes upon re-evaluation. Six of the 9 patients with normal radiographs to date are under continuos observation in the clinic and submitted to periodic radiographic and ultrasound re-evaluation.

In the light of these results, we believe that ultrasound is an appropriate method for diagnosis of hip joint involvement that deserves consideration in the evaluation of patients with JRA. Ultrasound is non-invasive and radiation-free; it is less expensive and more sensitive than conventional radiography. It allows for early detection of changes in the hip joint and aggressive therapy such cytotoxic drugs and directed physiotherapy. Ultrasound is also useful in the followup of patients with JRA who present major risk factors for involvement of the hip joint, such as those with disease onset before the age of 5, an evolution to systemic or polyarticular types, long disease duration, and placement in poorer functional classes. Finally, ultrasonographic findings can be detected independently of clinical manifestations. Thus, we are convinced the ultrasound deserves the special attention of pediatric rheumatologists as well as other specialists .

ACKNOWLEDGMENT

We thank to professors Yara Juliano and Neil Ferreira Novo for the statistical analysis and James R. Marrone, Wladimir P. Lorentz and Murilo Rezende Melo for assistance with the manuscript and figures.

Table 1 - Radiographic and ultrasonographic hip-joint findings in patients with JRA according to the clinical characteristics of the disease (n = 106 joints)

* = p £ 0,05 NS = p > 0,05

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