Role of Imaging in Management of Hemophilic Patients
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1 Pediatric Imaging Ng et al. Imaging of Hemophilic Patients W. H. Ng 1 W. C. W. Chu 1 M. K. Shing 2 W. W. M. Lam 1 K. W. Chik 2 C. K. Li 2 C. K. Li 3 S. C. Ling 3 Ng WH, Chu WCW, Shing MK, et al. Received May 18, 2004; accepted after revision August 26, Department of Diagnostic Radiology and Organ Imaging, Faculty of Medicine, The Chinese University of Hong Kong, Prince of Wales Hospital, Ngan Shing St., Shatin, N. T., Hong Kong. Address correspondence to W. H. Ng. 2 Department of Paediatrics, The Chinese University of Hong Kong, Prince of Wales Hospital, Shatin, N. T., Hong Kong. 3 Department of Paediatrics, Princess Margaret Hospital, N. T., Hong Kong. AJR 2005;184: X/05/ American Roentgen Ray Society Role of Imaging in Management of Hemophilic Patients OBJECTIVE. The purpose of this study was to evaluate the role of symptomatology and conventional radiographic scoring in predicting synovial hypertrophy, which could affect the clinical management of hemophilic patients. MATERIALS AND METHODS. Twenty males (mean age, 14.3 years old) with hemophilic arthropathy, including 34 symptomatic joints and 26 asymptomatic joints (16 knees, 20 ankles, and 24 elbows) had conventional radiographs of individual joints obtained that were rated according to the Arnold-Hilgartner stage and the Pettersson score. The patients also underwent MRI for the detection of synovial hypertrophy. The association of synovial hypertrophy and symptomatology was evaluated using the chi-square or Fisher s exact test. The best sensitivity, specificity, and positive and negative predictive values in detection of synovial hypertrophy using symptomatology and radiographic scoring were calculated. RESULTS. A significant association was seen between symptomatology and synovial hypertrophy of the knee and ankle joints (p < 0.05). The sensitivity, specificity, and positive and negative predictive values of symptomatology in detection of synovial hypertrophy of the knee were 100%, 78%, 78%, and 100%, respectively, and for the ankle were 83%, 75%, 83%, and 75%, respectively. The Arnold-Hilgartner stage and Pettersson score of the radiograph had a significant association with synovial hypertrophy of the knee and ankle joints (p < 0.05). Arnold-Hilgartner staging provided a better prediction of synovial hypertrophy, with sensitivity, specificity, value of 100%, 100%, 100%, and 100% for knees and 82%, 100%, 100%, and 82% for ankles. CONCLUSION. In hemophilic patients, the presence of symptomatology in the knee and ankle joints is associated with synovial hypertrophy, and scoring of the conventional radiographs using Arnold-Hilgartner staging is useful for the prediction of synovial hypertrophy. n patients with hemophilic arthropathy, recurrent hemorrhage I leads to synovial hypertrophy and hemosiderin deposition. Iron deposition stimulates synovitis, which is associated with the release of cytokines. Repeated synovitis leads to the progressive destruction of the cartilage and subchondral bone, resulting in joint space narrowing. End-stage joint destruction, angulation, or ankylosis may finally occur [1, 2]. To prevent hemophilic arthropathy, prophylactic treatment of children with severe hemophilia should be started before joint damage occurs [3, 4]. The later prophylaxis is started after the first incidence of hemarthrosis, the higher the risk of development of arthropathy [3]. Since the 1970s and early 1980s, the severity of hemophilic symptomatic arthropathy has been assessed with conventional radiography according to the Arnold-Hilgartner stage [5] (Table 1) and the Pettersson score [6] (Table 2). The Arnold-Hilgartner stage is frequently used in the United States and is graded by the worst findings in the joint as one advances through the stages of the disease. The Pettersson score is a detailed clinical and radiologic classification of hemophilic joints that has been adopted by the World Federation of Hemophilia. It estimates joint destruction radiologically and is an additive scale [6]. The radiographic scoring systems for staging joint disease have been proven to be inferior to MRI assessment [7 9]. MRI allows a precise noninvasive assessment of all the articular (synovium, cartilage, and bone) and periarticular structures, which is the main limitation of conventional radiography. MRI is sensitive for the detection of preclinical changes undetectable on AJR:184, May
2 Ng et al. TABLE 1 Arnold-Hilgartner Stage Stage Finding 0 Normal joint 1 No skeletal abnormalities, soft-tissue swelling present 2 Osteoporosis and overgrowth of epiphysis, no erosions, no narrowing of cartilage space 3 Early subchondral bone cysts, squaring of patella, widening of intercondylar notch of distal femur or humerus, preserved cartilage space 4 More advanced findings of stage 3, with narrowing of cartilage space 5 Fibrous joint contracture, loss of joint cartilage space, marked enlargement of epiphyses, and substantial disorganization of the joint Note. Data are taken from [5]. TABLE 2 Pettersson Score Finding Score Osteoporosis Enlarged epiphysis Irregular subchondral surface Partially involved 1 Totally involved 2 Narrowing of joint space Present, joint space > 1 mm 1 Absent, joint space 1mm 2 Subchondral cyst formation Erosions at joint margins 1 Cyst 1 > 1 Cyst 2 Gross incongruence of articulating bone ends (angulation or displacement between articulating bone ends) Slight 1 Pronounced 2 Joint deformity Slight 1 Pronounced 2 Note. Data are taken from [6]. conventional radiography [10]. The key to the successful early treatment of hemophilic joint disease is the recognition of synovial hypertrophy [11], which can affect and change the plan of management [12]. Because previous studies have shown that MRI is sensitive for the detection of synovial hypertrophy [7, 9], it should be used as the gold standard. Power Doppler sonography has been proven to be a reliable diagnostic method for qualitative grading of the vascularity of synovial tissue [13, 14] In clinical practice, MRI can give a better global picture and can show occult bleeding with hemosiderin deposits. However, if all hemophilic patients have all their joints screened by MRI, this will impose a constraint on major resources. The aim of this study is to assess the potential role of the Pettersson score and the Arnold-Hilgartner stage in the selection of patients and joints for MRI assessment, which would affect the management of symptomatic and asymptomatic joints. Because knees, elbows, and ankles are the most commonly affected joints in hemophilic patients [15], we have focused on these three joints in our study. Materials and Methods Patient Recruitment Twenty males (mean age, 14.3 years; range, 7 28 years) with hemophilia were recruited into the study. Patient and parent consent was obtained. All patients had at least one symptomatic joint. Symptomatic joint was defined as a joint with a history of clinical symptoms of pain, tenderness, swelling, or locking. Altogether, 34 symptomatic joints and 26 asymptomatic joints were assessed. These included 16 knee, 20 ankle, and 24 elbow joints. Conventional Radiographic Technique and Interpretation Conventional frontal and lateral radiographs of all symptomatic joints and their contralateral joints were obtained (MultiX FD, Siemens Medical Solutions). Scores were given to each joint according to the Arnold-Hilgartner stage [5] (Table 1) and the Pettersson score [6] (Table 2) by a radiologist on different occasions. The radiologist was informed of the clinical history of hemophilia but was blinded to the presence or absence of symptoms in individual joints. The second scoring was provided without reference to the first scoring. MRI Technique and Interpretation MRI of the joints and conventional radiography were performed within the same week. MRI was performed with a 1.5-T scanner (Sonata, Siemens). The imaging protocol included spin-écho T1- weighted coronal images (TR/TE, 450/14; flip angle, 90 ; matrix, ; number of excitations, 2; field of view, 150 mm), turbo spin-echo T2- weighted coronal images (2,470/97; turbo factor, 23; flip angle, 150 ; matrix, ; number of excitations, 3; field of view, 150 mm), turbo spinecho T2-weighted sagittal images (3,600/97; turbo factor, 23; flip angle, 150 ; matrix, ; number of excitations, 4; field of view, 150 mm), T2- weighted FLASH 2D sagittal images (51/25; flip angle, 20 ; matrix, ; number of excitations, 1; field of view, 150 mm), and T2-weighted double-echo steady state 3D sagittal images (22/6; flip angle, 25 ; matrix, ; number of excitations, 2; field of view, 150 mm). The images were searched for synovial hypertrophy by two radiologists on two different occasions. The final interpretation was agreed on by consensus. All three radiologists interpreting the images were blinded to the scoring of the other imaging. Statistical Methods A receiver operating characteristic (ROC) curve was constructed using SPSS statistical software (release 10.1, SPSS) for Windows (Microsoft) to identify the optimum Arnold-Hilgartner stage and Pettersson score for the detection of synovial hypertrophy in either symptomatic or asymptomatic joints, using MRI results as the standard of reference. Fisher s exact test (when the number of cases in any category is < 5) or chi-square test was used for assessing the association between the presence of synovial hypertrophy and the Arnold-Hilgartner stage and the Pettersson score in knee, ankle, and elbow joints. The staging and scoring at which the smallest p value was calculated were considered to be the optimal level. The sensitivity, specificity, positive predictive value, and negative predictive value of different stages or scores in the detection of the synovial hypertrophy using the optimal scoring or staging were calculated. The predictive value of joint space narrowing shown on conventional radiography was evaluated. Joints were classified into three groups on the basis of Arnold-Hilgartner (AH) stage: stage 0, stages 1 3, and stages 4 5. The association with synovial hyper AJR:184, May 2005
3 Imaging of Hemophilic Patients Association of Presence of Synovial Hypertrophy in TABLE 3 Knee, Elbow, and Ankle Joints and Arnold- Hilgartner Stage [5] on Conventional Radiography Stage Knee Elbow Ankle > a a > a a > b b > a > b Smallest p value. Association of Presence of Synovial Hypertrophy in TABLE 4 Knee, Elbow, and Ankle Joints and Pettersson Score [6] on Conventional Radiography Score Knee Elbow Ankle > a a > a a > a b > b a > a a > a > a > > > b Smallest p value. trophy was evaluated using a 3 2 chi-square test. The sensitivity, specificity, positive predictive value, and negative predictive value of stages 4 and 5 in the detection of synovial hypertrophy were calculated. The association between symptomatology and synovial hypertrophy was evaluated using the chisquare or Fisher s exact test. The sensitivity, specificity, value by symptomatology were also calculated. For all statistical evaluation, only p values of less than 0.05 were considered to be statistically significant. Results Synovial hypertrophy was shown on MRI in 35 joints: seven symptomatic and no asymptomatic knee joints, 11 symptomatic and five asymptomatic elbow joints, and 10 symptomatic Association of Presence of Synovial Hypertrophy in Knee, Elbow, and TABLE 5 Ankle Joints and Category of Arnold-Hilgartner Stage [5] on Conventional Radiography Knee Elbow Ankle Stage Hypertrophy No Hypertrophy Hypertrophy No Hypertrophy Hypertrophy No Hypertrophy p < < 0.05 Note. Data are numbers of joints. TABLE 6 Performance Measures for Detection of Synovial Hypertrophy of Knee and Ankle Using Stage 3 of Arnold-Hilgartner (A-H) Stage [5] and Score 4 for Knee and Score 3 for Ankle of Pettersson Score [6] and two asymptomatic ankle joints. No synovial hypertrophy was shown on MRI in 25 joints, of which six joints were symptomatic, including two knee, two elbow, and two ankle joints. Tables 3 and 4 show the association between the presence of synovial hypertrophy and different Arnold-Hilgartner stages and Pettersson scores. Arnold-Hilgartner stages equal to or higher than stage 3 (with the smallest p value) gave the best prediction of the presence of synovial hypertrophy in the knee and ankle joints. Pettersson scores of 4 and 3 gave the best prediction for detection of synovial hypertrophy in the knee and ankle joints, respectively. In the elbow, neither Arnold-Hilgartner stage nor Pettersson score was useful for the prediction of synovial hypertrophy. Knee A-H stage 100% 100% 100% 100% Pettersson score 86% 100% 100% 90% Ankle A-H stage 82% 100% 100% 82% Pettersson score 82% 100% 100% 82% TABLE 7 Performance Measures for Detection of Synovial Hypertrophy of the Knee and Ankle Using Stage 4 or Higher of Arnold-Hilgartner Stage [5] Knee 43% 100% 100% 69% Ankle 45% 100% 100% 60% Table 5 shows the association between the presence of synovial hypertrophy and different Arnold-Hilgartner stages. A significant association was seen higher than stage 3 between the Arnold-Hilgartner stage and the presence of synovial hypertrophy in the knee and ankle joints, but not the elbow joint. Table 6 shows the sensitivity, specificity, value for the detection of synovial hypertrophy of the knee and ankle by optimal Arnold-Hilgartner stage and Pettersson score. The specificity and positive predictive value were all 100%, using either the Arnold-Hilgartner staging or the Pettersson scoring method. The Pettersson method, however, had a lower sensitivity and negative predic- AJR:184, May
4 Ng et al. TABLE 8 Association of Presence of Synovial Hypertrophy and Symptomalogy in Knee, Elbow, and Ankle Joints Symptomatic Asymptomatic p Knee Hypertrophy a No hypertrophy 2 7 Elbow Hypertrophy No hypertrophy 2 6 Ankle Hypertrophy a No hypertrophy 2 6 Overall Hypertrophy a No hypertrophy 6 19 TABLE 9 Performance Measures for Detection of Synovial Hypertrophy of the Knee, Elbow, and Ankle Joints Using Presence of Symptomalogy Knee 100% 78% 78% 100% Elbow 69% 75% 85% 55% Ankle 83% 75% 83% 75% Overall 84% 76% 82% 77% tive value for detecting synovial hypertrophy in the knee joint. Table 7 shows the sensitivity, specificity, value for detecting synovial hypertrophy of the knee and ankle according to Arnold-Hilgartner stage 4 or higher. The sensitivity and the negative predictive value were lower than using stage 3 or higher. The positive predictive value and the specificity were still 100%. Table 8 shows the association between the presence of synovial hypertrophy and symptomatology of the knee, ankle, and elbow joints. A significant association was seen between symptomatology and synovial hypertrophy in the knee and ankle joints (p < 0.05). Table 9 shows the sensitivity, specificity, value for detecting synovial hypertrophy of the knee, ankle, and elbow according to the presence of clinical symptoms. Using the presence of symptoms to predict the presence of synovial hypertrophy was relatively sensitive in knee and ankle joints, giving a sensitivity of %. The negative predictive value was also high 100% in knee joints. However, the predictive value in elbow joints was limited. Discussion Prophylactic therapy (infusion of factor concentrate on a regular basis) and synovectomy are used to prevent or delay joint destruction. Radiosynoviorthesis has been shown to be effective in decreasing bleeding frequency, reducing pain, and improving the global quality of life [16]. Prophylaxis is generally chosen for younger patients with recurrent hemorrhage into multiple joints, or for patients who cannot cooperate with the intensive postoperative physiotherapy [12]. Synovectomy tends to be used in older patients with a single targeted joint and in those in whom prophylactic therapy failed [12]. Synovectomy or prophylaxis will benefit even late-stage joints with recurrent hemorrhage [12]. The delay in the administration of prophylactic treatment increases the risk in development of arthropathy [3]. Once cartilage destruction and joint space narrowing occur, the symptoms of arthritis may persist even with the benefit of decreasing bleeding with synovectomy. However, prophylactic treatment will increase the incidence of side effects of transfusion. Increase in medical cost and hampering of venous access are other disadvantages of prophylactic treatment. The optimum timing of starting prophylaxis is still being debated. However, the presence of synovium is clinically relevant and is the key to success because both synovectomy and prophylaxis are beneficial only if hypertrophied synovium is present. MRI is the only noninvasive imaging technique available to detect chronic synovitis and synovial hypertrophy of hemophilic patients [3, 11], and therefore plays an important role in the selection of patients for treatment. Most studies used conventional MRI for detection of the synovial hypertrophy [7, 9, 11, 16, 17]. One recent study showed that MRI with gadolinium can help to differentiate the cartilage and fluid from hypervascular hypertrophic synovia [18] in hemophilic patients. However, our patients are relatively young, and some are not willing to have an IV injection. Moreover, the administration of gadolinium will increase the cost of the examination. Funk et al. [17] found no signs of arthrographic alterations on MRI or conventional radiography in 16 joints that suffered fewer than two episodes of bleeding [17]. However, in our study, synovial hypertrophy was found in eight asymptomatic joints. Our findings suggested the presence of an ongoing process of hemophilic arthropathy even before the joints became symptomatic, and were in agreement with previous studies [7]. Subclinical bleeding in the joints may have triggered early joint damage [6]. From our results, neither the presence of symptomatology nor radiographic findings can be used to replace MRI in the detection of synovial hypertrophy, which is in agreement with previous studies [7 9]. The presence of symptomatology results from intraarticular bleeding and the toxic effects of blood breakdown products and iron itself on cartilage, not from synovial hypertrophy itself. Synovial hypertrophy has increased vascularity that is friable and leads to increased bleeding into the joint. With continued bleeding comes continued cartilage destruction. Therefore, symptomatology is only indirectly related to synovial hypertrophy. However, when an individual joint was analyzed, the presence of symptomatology in knee joints gave a good prediction of synovial hypertrophy, with a negative predictive value of 1622 AJR:184, May 2005
5 Imaging of Hemophilic Patients 100%. Therefore, we suggest that whenever knee joint symptoms appear, radiography should be performed for further assessment. If the Arnold-Hilgartner stage of the knee joint is equal to or higher than 3, we can proceed to MRI for confirmation and to assess the severity. For the ankle joint, the presence of symptomatology gave only a fair prediction of synovial hypertrophy. The use of radiographic scoring in ankle joints would help to improve the prediction of presence of synovial hypertrophy. A scoring of stage 3 or higher by the Arnold-Hilgartner system would give a negative predictive value of 82%. Whenever symptoms are present or when the conventional radiographic Arnold-Hilgartner score is equal to or greater than 3, MRI is recommended for assessment. In the elbow joint, neither the presence of symptomatology nor radiographic scoring can help to predict synovial hypertrophy. This might suggest that if we need to detect synovial hypertrophy, regular surveillance of the elbow joint by MRI is required. Such surveillance would impose a major resources constraint. Therefore, it is questionable whether surveillance is practically feasible, even if only the dominant hand is to be screened. In general, when using radiography for scoring, both Pettersson and Arnold-Hilgartner allow good prediction of synovial hypertrophy in ankles. The prediction by Arnold- Hilgartner is slightly better in knee joints. In practice, for the sake of simplicity, we recommend the use of Arnold-Hilgartner staging in both ankle and knee joints. In our study, we have attempted to justify the screening protocol for individual joints for hemophilic patients in planning prophylactic therapy. The major disadvantages and limitations of our study are the relatively small sample size of asymptomatic joints. The lack of data on temporal progression disallows the justification of an optimal screening protocol study. Only a multicenter longitudinal study will allow collection of sufficient data to answer these questions. In conclusion, in hemophilic patients both symptomatology and scoring of radiographs of the knee and ankle joints are useful for the prediction of synovial hypertrophy. MRI of these two joints with either positive symptoms or an optimal Arnold-Hilgartner stage is indicated when prophylactic treatment is considered. References 1. Roosendaal G, Vianen ME, Wenting MJ, et al. Iron deposits and catabolic properties of synovial tissue from patients with haemophilia. J Bone Joint Surg Br 1998;80: Roosendaal G, van Rinsum AC, Vianen ME, van den Berg HM, Lafeber FP, Bijlsma JW. Haemophilic arthropathy resembles degenerative rather than inflammatory joint disease. Histopathology 1999;34: Fischer K, van der Bom JG, Mauser-Bunschoten EP, et al. The effects of postponing prophylactic treatment on long-term outcome in patients with severe hemophilia. Blood 2002;99: Van den Berg HM, Fischer K. Prophylaxis for severe hemophilia: experience from Europe and the United States. Semin Thromb Hemost 2003;29: Arnold WD, Hilgartner MW. Hemophilic arthropathy: current concepts of pathogenesis and management. J Bone Joint Surg Am 1977;59: Pettersson H, Ahlberg A, Nilsson IM. A radiologic classification of hemophilic arthropathy. Clin Orthop 1980;149: Dobon M, Lucia JF, Aguilar C, et al. Value of magnetic resonance imaging for the diagnosis and follow-up of haemophilic arthropathy. Haemophilia 2003;9: Baunin C, Railhac JJ, Younes I, et al. MR imaging in hemophilic arthropathy. Eur J Pediatr Surg 1991;1: Yulish BS, Lieberman JM, Strandjord SE, Bryan PJ, Mulopulos GP, Modic MT. Hemophilic arthropathy: assessment with MR imaging. Radiology 1987;164: Aledort LM, Haschmeyer RH, Pettersson H. A longitudinal study of orthopaedic outcomes for severe factor-viii-deficient haemophiliacs. The Orthopaedic Outcome Study Group. J Intern Med 1994;236: Kilcoyne RF, Nuss R. Radiological evaluation of hemophilic arthropathy. Semin Thromb Hemost 2003;29: Nuss R, Kilcoyne RF, Geraghty S, Wiedel J, Manco- Johnson M. Utility of magnetic resonance imaging for management of hemophilic arthropathy in children. J Pediatr 1993;123: Giovagnorio F, Martinoli C, Coari G. Power Doppler sonography in knee arthritis: a pilot study. Rheumatol Int 2001;20: Walther M, Harms H, Krenn V, Radke S, Faehndrich TP, Gohlke F. Correlation of power Doppler sonography with vascularity of the synovial tissue of the knee joint in patients with osteoarthritis and rheumatoid arthritis. Arthritis Rheum 2001;44: Resnick D. Bleeding disorders. In: Resnick D, ed. Diagnosis of bone and joint disorders, 3rd ed., vol. 4. Philadelphia, PA: Saunders, 1995: Nuss R, Kilcoyne RF, Rivard GE, Murphy J. Late clinical, plain X-ray and magnetic resonance imaging findings in haemophilic joints treated with radiosynoviorthesis. Haemophilia 2000;6: Funk MB, Schmidt H, Becker S, et al. Modified magnetic resonance imaging score compared with orthopaedic and radiological scores for the evaluation of haemophilic arthropathy. Haemophilia 2002;8: Rand T, Trattnig S, Male C, et al. Magnetic resonance imaging in hemophilic children: value of gradient echo and contrast-enhanced imaging. Magn Reson Imaging 1999;17: AJR:184, May
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