Hip Morphometry of Femoroacetabular Impingement Pattern in Patients with Ankylosing Spondylitis1 강직성척추염 환자에서 대퇴비구충돌증후군 고관절 모양에 관한 연구1

Home , Joint stiffness

Original Article pISSN 1738-2637 / eISSN 2288-2928 J Korean Soc Radiol 2015;72(6):385-392 http://dx.doi.org/10.3348/jksr.2015.72.6.385

Jong Yoon Lee, MD1, Eugene Lee, MD1, Jung-Ah Choi, MD1,2 1Department of Radiology, Seoul National University Bundang Hospital, Seongnam, Korea 2Department of Radiology, Hallym University Dongtan Sacred Heart Hospital, Hwaseong, Korea

Purpose: To analyze hip morphometry of femoroacetabular impingement (FAI) pat- Index terms tern in patients with ankylosing spondylitis (AS) and correlate them with sacroiliitis Ankylosing Spondylitis grades. Hip, Femoroacetabular Impingement Materials and Methods: 384 patients with AS were analyzed regarding demograph- Radiograph ics, radiologic signs of FAI for hip involvement, and sacroiliitis grades. FAI was classified into 3 types according to alpha angle, lateral center-edge angle and pistol grip Received August 11, 2014 Accepted February 24, 2015 deformity. Sacroiliitis was graded according to the New York criteria. Prevalence of Corresponding author: Jung-Ah Choi, MD FAI morphometry types was determined and evaluated for association with sacroili- Department of Radiology, Hallym University Dongtan itis grades. Statistical analysis regarding numerical variables, including age, sacroiliitis Sacred Heart Hospital, 7 Keunjaebong-gil, Hwaseong 445-170, Korea. score using t-test, sacroiliitis score in three groups using Kruskal-Wallis test and Tel. 82-31-8086-2577 Fax. 82-31-8086-2584 Mann-Whitney U-test, corrected by Bonferroni methods for post hoc analysis was E-mail: [email protected] done. This is an Open Access article distributed under the terms Results: Among 384 patients, 141 (36.7%) had FAI morphometry. Male predominance of the Creative Commons Attribution Non-Commercial was found in group with FAI pattern involvement (87.2%) (p = 0.000). Pincer type License (http://creativecommons.org/licenses/by-nc/3.0) (20.6%) was the most common. Hip involvement group also showed greater sacroi- which permits unrestricted non-commercial use, distri- bution, and reproduction in any medium, provided the liitis score (2.49 vs. 1.75, p = 0.000). Combined-type had greater sacroiliitis score com- original work is properly cited. pared with others (p = 0.002, 0.003). Conclusion: FAI morphometry was frequent in hips of AS patients (36.7%), especial- This study was supported by Basic Science Research Pro- gram through the National Research Foundation of Korea ly pincer type, more frequent in male, and associated with significantly greater grade (NRF) funded by the Ministry of Education, Science and of sacroiliitis; combined type FAI pattern had greater sacroiliitis score. Technology (NRF-2012R1A1A3010896). The authors would like to thank Dr. Soyeon Ahn for her assistance in statistical analysis.

INTRODUCTION tified as a major cause of early primary osteoarthritis (OA) of the hip (3). FAI refers to abnormal contact between the femoral Ankylosing spondylitis (AS) is a chronic inflammatory dis- head-neck junction or the acetabular rim (4). A number of pre- ease of the axial skeleton with involvement of peripheral joints disposing conditions have been described with deformities of and non-articular structures (1). Indeed, it is best known for its the femur and the acetabulum which result in FAI including symptom of lower back pain; however, patients often present Legg-Calvé-Perthes, slipped capital femoral epiphysis, coxa with hip or groin pain misleading the clinician to think that the magna, hip dysplasia, and fractures of the femoral neck (5). cause lies primarily in the hips. Hip involvement as a common Though FAI has not been recognized as a common radiologic problem in AS increases the burden and negative affects its prog- feature of AS, we noticed FAI like features in hips of AS patients nosis of AS than any other axial joints (2). and hypothesized that AS may be predisposed to FAI. To the Femoroacetabular impingement (FAI) has been recently iden- best of our knowledge, there has been no study about FAI pat-

Copyrights © 2015 The Korean Society of Radiology 385 Hip Morphometry of Femoroacetabular Impingement Pattern in Patients with Ankylosing Spondylitis tern of hip involvement in AS. In this study, we investigated the on AP radiographs. Excessive acetabular coverage can be quan- prevalence and radiographic patterns of FAI in hips of AS pa- tified with the lateral CE angle (8). The lateral CE angle is the tients. In addition, we evaluated the possible association between angle formed by a vertical line and a line connecting the femoral sacroiliitis grade and FAI according to different types. head center with the lateral edge of the acetabulum (Fig. 2) (9). A normal lateral CE angle varies between 25° (which defines a MATERIALS AND METHODS

Study Population This retrospective observational study was approved by the Institutional Review Board and informed consent was waived. Electronic medical records search revealed 543 patients diagnosed as AS or seronegative spondyloarthropathy from January 2004 to April 2012; out of these, 384 patients were included based on the following inclusion criteria: 1) clinically diagnosed as AS based on the New York criteria, 2) pelvis radiography, and 3) no previous hip surgery. We excluded patients with obvi- ous severe OA and ankylosis of the hip (n = 61) or unavailabili- ty of lateral radiographs (n = 98). The typical radiographic findings of severe OA include definite joint space narrowing and/or osteophyte formation. A total of 384 patients [288 (72.3%) men, 96 women; mean age, 35.9 years; range 15–80 years] were in- Fig. 1. Radiographic presentations of alpha angle on translateral radiograph by drawing a circle along the femur head circumference, cluded, of whom 296 patients were HLA-B27 positive. drawing a line between the center of the circle and the point of head- neck offset, according to the method described by Nötzli et al. (6). Radiographic Evaluation Images included anteroposterior (AP) and translateral views of the hip. All patients underwent pelvic radiography to assess routine evaluation of AS. All of the images were retrospectively reviewed by two radiologists. FAI-like features were evaluated regarding the following: alpha angle, lateral center-edge (CE) angle, presence of pistol grip deformity in AS patients. Then they were classified into 3 types: cam, pincer, and combined-types. The alpha angle was measured in the translateral radiograph in accordance with the method described by Nötzli et al. (6). The first line defining the α angle was located between the center of the femoral head and the point where the distance from the center of the femoral head to the peripheral contour of the femoral head exceeded the radius of the femoral head. The second line defining the α angle was the axis of the femoral neck, which was defined as a line that passed through the center of the femoral head and the center of the femoral neck at its narrowest point Fig. 2. Radiographic presentations of lateral center-edge angle on anteroposterior radiographs. The lateral center edge angle is the angle (Fig. 1) (7). formed by a vertical line and a line connecting the femoral head cen- The lateral CE angle and pistol grip deformity were measured ter with the lateral edge of the acetabulum.

386 J Korean Soc Radiol 2015;72(6):385-392 jksronline.org Jong Yoon Lee, et al dysplasia) (10) and 39° (which is an indicator for acetabular terpreted as indicating poor (ICC, 0–0.2), fair (ICC, 0.3–0.4), overcoverage) (11). Also flattening of the head-neck junction (so moderate (ICC, 0.5–0.6), strong (ICC, 0.7–0.8), or almost perfect called pistol grip deformity) was evaluated on AP radiographs (ICC, > 0.8) agreement. For the qualitative assessments (pistol- (Fig. 3). grip deformity), kappa analysis was used to evaluate interrater Cam type FAI was considered to be present when there was validity. Level of agreement was interpreted as indicating less flattening of the head-neck junction (pistol grip deformity) and/ than chance (κ ≤ 0), slight (κ = 0.01–0.20), fair (κ = 0.21–0.40), or α angle > 55°; pincer FAI was considered when the lateral CE moderate (κ = 0.41–0.60), substantial (κ = 0.61–0.80), almost angle > 39° was detected. Combined type was considered in perfect (κ = 0.81–0.99), or perfect (κ = 1). cases with findings of both types. Statistical analyses were performed using Statistical Package The prevalence of FAI types was determined and evaluated for for the Social Sciences (SPSS) software version 18.0 (SPSS Inc., the association with grades of sacroiliitis. Sacroiliac joints were Chicago, IL, USA). p values less than 0.05 were considered to graded according to the New York criteria established in 1966 be statistically significant. We performed t-test for numerical (9), which describe five grades of sacroiliitis from 0 to 4 (0 = no variables including age, sacroiliitis score, Kruskal-Wallis test for disease, 1 = suspicious for disease, 2 = minimal disease, 3 = mod- sacroiliitis score in three groups, and Mann-Whitney U-test, cor- erate disease, and 4 = severe disease). Images of 384 patients rected by Bonferroni methods for post hoc analysis. were analyzed by the first observer and they were also re-analyzed independently; a second observer evaluated the images RESULTS after consensus training session with the first observer. Among 384 patients, 141 (36.7%) had FAI pattern of hip joint Statistical Analysis involvement. Male predominance was found in the group with The measurements were performed by two radiologists (one FAI pattern involvement (M:F = 123:18, 87.2%) compared with with three years, the other with five years of experience) and the group without hip involvement (M:F = 165:78, 67.9%) (p = their interrater reliabililty was tested. For the quantitative assess- 0.000) (Table 1). The group with FAI pattern of hip involvement ments (lateral CE angle, α angle), intraclass correlation coeffi- also showed greater sacroiliitis score as compared with those cient (ICC) was used to evaluate interrater reliability. ICC was in- without hip involvement (2.49 ± 1.19, 1.75 ± 1.19, p = 0.000). HLA-B27 was not different between FAI (-) and FAI (+) groups

Table 1. Demographics & Presence of FAI Pattern in Patients with Ankylosing Spondylits FAI Pattern (+) FAI Pattern (-) p-Value Sex 0.000* Male 123 (67.9%) 165 (87.2%) Female 18 (32.1%) 78 (12.8%) Sacroiliitis grade 2.49 ± 1.19 1.75 ± 1.19 0.000† Total number 141 243 *Analyzed by t-test. †Analyzed by χ2 test. FAI = femoroacetabular impingement

Table 2. Grade of Sacroiliitis Accoding to Pattern of FAI in Patients with Ankylosing Spondylits Pattern of FAI Prevalence Grade of Sacroiliitis p-Value Pincer 79 (20.6%) 2.33 ± 1.19 Cam 25 (6.5%) 2.16 ± 1.25 Combined 37 (9.6%) 3.05 ± 0.97 0.002* Fig. 3. Radiographic presentations of flattening of the head-neck junc- *t-test with Bonferroni correction. tion (so called pistol grip deformity) on anteroposterior radiographs. FAI = femoroacetabular impingement jksronline.org J Korean Soc Radiol 2015;72(6):385-392 387 Hip Morphometry of Femoroacetabular Impingement Pattern in Patients with Ankylosing Spondylitis

(75.3% vs. 75.2%, respectively, p = 0.977). ers for each quantitative measurement and ranged from strong to Regarding type of FAI (n = 141), it was composed of pincer- almost perfect (0.78, 0.86). For the qualitative parameters, kap- type (n = 79/384, 20.6%), cam-type (n = 25/384, 6.5%), and com- pa analysis showed moderate agreement (0.54). bined-type (n = 37/384, 9.6%); pincer type was the most common among the FAI types (Figs. 4-6). Sacroiliitis grade was DISCUSSION different according to FAI types p( = 0.002); combined-type FAI pattern (n = 37, 3.05 ± 0.97) had greater sacroiliitis score than The importance of hip involvement in patients with AS has pincer (n = 79, 2.33 ± 1.19, p = 0.002) and cam-types (n = 25, 2.16 ± been recognized for several years as a common and disabling 1.25, p = 0.003), respectively (Table 2). problem, whereas involvement of other peripheral joints is less ICC was used to evaluate agreement between the two observ- common. Hip involvement is an important prognostic factor

A B Fig. 4. Pelvic radiograph of 33-year-old man with ankylosing spondylitis. A. Pincer type femoroacetabular impingement pattern showing lateral center-edge angle estimated to be 52.3°. B. Demonstrating bilateral sacroiliitis grade 3, showing subchondral sclerosis and irregularities of the joint surface, including erosions.

A B Fig. 5. Pelvic radiograph of in 26-year-old man with ankylosing spondylitis. A. Cam type femoroacetabular impingement pattern showing alpha angle estimated to be 62.4°. B. Demonstrating bilateral sacroiliitis grade 2, showing equivocal subchondral sclerosis.

388 J Korean Soc Radiol 2015;72(6):385-392 jksronline.org Jong Yoon Lee, et al

A B Fig. 6. Pelvic radiograph of 31-year-old man with ankylosing spondylitis. A. Combined type femoroacetabular impingement pattern showing lateral center-edge angle estimated to be 45.0° and positive pistol grip deformity. B. Demonstrating bilateral sacroiliitis grade 4, showing complete ankylosis. associated with radiographic progression (1); approximately 8 tal femoral epiphysis is known as a predisposing condition of to 15% of AS patients with long-term follow-up have to undergo FAI; Dodds et al. (17) reported that among patients with after total hip joint replacement arthroplasty (12, 13). Though radio- slipped capital femoral epiphysis, 32% had clinical signs of FAI. graphic and clinical signs of hip involvement showed positive Although AS has not been previously investigated as a predis- correlation in many studies, there has been no definite consensus posing factor of FAI, FAI pattern of hip involvement was fre- on how to assess hip involvement (1) and radiologic pattern of quent in AS and higher prevalence of FAI-type features were hip involvement in AS patients. found than in asymptomatic general population in our study. Especially in the very early phase of hip involvement, patients Regarding type of FAI, pincer type FAI was the most common may not have classic radiographic signs of OA, such as joint pattern in our study of AS patients, followed by combined and space narrowing, bone erosion, osteophyte formation or sub- cam types. Most FAI patients (86%) are reported to have a com- chondral sclerosis on hip radiograph. During hip radiograph bination of both forms of impingement and only a minority interpretation in AS patients, we found radiologic pattern of (14%) to have the pure cam or pincer type of FAI in the general hip involvement similar to FAI in AS patients. So we postulated population (18). Although the mechanism is unclarified, we that the deformities caused by hip involvement in AS patients hypothesize that pincer type FAI pattern may be caused by pro- can change the mechanical function of the hip joint and con- nounced periarticular ossification at the acetabulum as a result tribute to FAI-like features on radiographs. We expected that of hip involvement of AS. This enthesopathy of acetabular rim AS patients have higher prevalence of FAI-like features than the may result in further overcoverage of the femoral head, which general population and have association with higher grades of would produce the characteristic features of pincer type FAI. In sacroiliitis. AS patients with advanced hip OA, coxa profunda or protrusio In this study, we found FAI pattern of hip involvement in acetabuli is usually seen on AP hip radiographs. Protrusio ace- 36.7% of patients with AS. FAI has been reported to be present tabuli is very common, occurring in as many as 33% of those in 10–15% of general population (14). And recent CT study has with AS in the hip (19). A coxa profunda is defined as the floor shown that two or more abnormal parameters of FAI were pres- of the fossa acetabuli touching or overlapping the ilioischial line ent in 29% of joints in asymptomatic young populations (15). medially and protrusio acetabuli occurs when the femoral head Also, FAI-like pattern was found in 35.3% of primary OA caused is overlapping the ilioischial line medially. These two findings mostly by developmental dysplasia of the hip (16). Slipped capi- increase the relative depth of the acetabulum and generally a jksronline.org J Korean Soc Radiol 2015;72(6):385-392 389 Hip Morphometry of Femoroacetabular Impingement Pattern in Patients with Ankylosing Spondylitis deep acetabulum is associated with excessive acetabular cover- AS patients, but it has limitations in evaluation of intra-articular age, which would predispose to further pincer type FAI (3). structure damage. So if “FAI morphometric” features are pres- Our findings of the positive correlation between hip involve- ent on routine conventional radiographs or patients presenting ment and sacroiliitis grade are consistent with results of other with severe hip symptoms, additional MRI should be done to studies, suggesting a strong association of hip disease with more visualize specific morphology around the hip joint that might severe axial involvement (20-22). Sacroiliitis is the most frequent need to be addressed surgically in the case of a clinical diagno- and earliest radiographic manifestation of AS. Doran et al. (20) sis of FAI. noted that radiologic hip involvement is significantly associated In conclusion, FAI pattern of hip involvement was frequently with higher scores of radiologic change in the spine. In our study, seen in AS (36.7%), more frequent in male patients and associ- hip involvement group also showed greater sacroiliitis score than ated with significantly greater grade of sacroiliitis (2.49 ± 1.19). AS without hip involvement. Regarding FAI pattern types, com- Regarding type of FAI, pincer type was the most common pat- bined-type FAI pattern had greater sacroiliitis score compared tern, followed by combined and cam types. Combined type FAI with pincer and cam-types, respectively (p = 0.002, 0.003). We pattern had greater sacroiliitis score than pincer and cam-types. postulated that combined type is combination of both impingement types and it may be seen in more advanced state of hip in- REFERENCES volvement than pure pincer and cam types. Inflammatory low back pain is the most typical presenting 1. Baraliakos X, Braun J. Hip involvement in ankylosing spon- symptom of AS, which most likely represents sacroiliac and spi- dylitis: what is the verdict? Rheumatology (Oxford) 2010; nal involvement (23); hip joint stiffness and groin pain have been 49:3-4 suggested to indicate hip involvement. In our study, among pa- 2. Vander Cruyssen B, Muñoz-Gomariz E, Font P, Mulero J, de tients with FAI pattern hip involvement, 66.7% patients pre- Vlam K, Boonen A, et al. Hip involvement in ankylosing sented with hip or inguinal pain rather than lower back pain. spondylitis: epidemiology and risk factors associated with We expected that patients with FAI involvement often showed hip replacement surgery. Rheumatology (Oxford) 2010;49: painful symptom before the onset of classical radiographic de- 73-81 generative change of AS (3). Also FAI triggers damage to the ace- 3. Tannast M, Siebenrock KA, Anderson SE. Femoroacetabular tabular labrum and articular cartilage in the hip, which would impingement: radiographic diagnosis--what the radiologist aggravate hip pain. Radiographic findings may be very subtle should know. AJR Am J Roentgenol 2007;188:1540-1552 and missed easily in the early stage of hip involvement of AS. 4. Sutter R, Dietrich TJ, Zingg PO, Pfirrmann CW. Femoral an- Thus, early diagnosis and treatment are critical to prevent devel- tetorsion: comparing asymptomatic volunteers and patients opment of OA and/or delay the need for a more radical treat- with femoroacetabular impingement. Radiology 2012;263: ment option (24). 475-483 There are several limitations to our study. The group with hip 5. Hack K, Di Primio G, Rakhra K, Beaulé PE. Prevalence of involvement showed FAI like feature on radiograph, but it is cam-type femoroacetabular impingement morphology in unclear whether these patients had typical clinical hip symp- asymptomatic volunteers. J Bone Joint Surg Am 2010;92: toms of FAI. Many patients visited the rheumatologist for man- 2436-2444 agement of AS and in such cases there was no objective physi- 6. Nötzli HP, Wyss TF, Stoecklin CH, Schmid MR, Treiber K, cal exmaination done regarding FAI, particularly flexion and Hodler J. The contour of the femoral head-neck junction as internal rotation (9). 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diology 2006;240:778-785 osteoarthritis of the hip. Int Orthop 2009;33:1229-1232 8. Murphy SB, Kijewski PK, Millis MB, Harless A. Acetabular 17. Dodds MK, McCormack D, Mulhall KJ. Femoroacetabular dysplasia in the adolescent and young adult. Clin Orthop impingement after slipped capital femoral epiphysis: does Relat Res 1990;(261):214-223 slip severity predict clinical symptoms? J Pediatr Orthop 9. Tannast M, Siebenrock KA, Anderson SE. [Femoroacetabular 2009;29:535-539 impingement: radiographic diagnosis--what the radiologist 18. Beck M, Kalhor M, Leunig M, Ganz R. Hip morphology in- should know]. Radiologia 2008;50:271-284 fluences the pattern of damage to the acetabular cartilage: 10. Murphy SB, Ganz R, Müller ME. The prognosis in untreated femoroacetabular impingement as a cause of early osteo- dysplasia of the hip. A study of radiographic factors that pre- arthritis of the hip. J Bone Joint Surg Br 2005;87:1012- dict the outcome. J Bone Joint Surg Am 1995;77:985-989 1018 11. Tönnis D, Heinecke A. Acetabular and femoral anteversion: 19. McBride MT, Muldoon MP, Santore RF, Trousdale RT, Wenger relationship with osteoarthritis of the hip. J Bone Joint Surg DR. Protrusio acetabuli: diagnosis and treatment. J Am Am 1999;81:1747-1770 Acad Orthop Surg 2001;9:79-88 12. Gran JT, Skomsvoll JF. The outcome of ankylosing spondy- 20. Doran MF, Brophy S, MacKay K, Taylor G, Calin A. Predictors litis: a study of 100 patients. Br J Rheumatol 1997;36: of longterm outcome in ankylosing spondylitis. J Rheuma- 766-771 tol 2003;30:316-320 13. Robertson LP, Davis MJ. A longitudinal study of disease ac- 21. Brophy S, Mackay K, Al-Saidi A, Taylor G, Calin A. The natu- tivity and functional status in a hospital cohort of patients ral history of ankylosing spondylitis as defined by radiologi- with ankylosing spondylitis. Rheumatology (Oxford) 2004; cal progression. J Rheumatol 2002;29:1236-1243 43:1565-1568 22. Brophy S, Calin A. Ankylosing spondylitis: interaction be- 14. Leunig M, Beck M, Dora C, Ganz R. [Femoroacetabular im- tween genes, joints, age at onset, and disease expression. J pingement: trigger for the development of coxarthrosis]. Rheumatol 2001;28:2283-2288 Orthopade 2006;35:77-84 23. Sampaio-Barros PD, Bertolo MB, Kraemer MH, Neto JF, Sa- 15. Chakraverty JK, Sullivan C, Gan C, Narayanaswamy S, Ka- mara AM. Primary ankylosing spondylitis: patterns of dis- math S. Cam and pincer femoroacetabular impingement: ease in a Brazilian population of 147 patients. J Rheumatol CT findings of features resembling femoroacetabular im- 2001;28:560-565 pingement in a young population without symptoms. AJR 24. Hickman JM, Peters CL. Hip pain in the young adult: diag- Am J Roentgenol 2013;200:389-395 nosis and treatment of disorders of the acetabular labrum 16. Takeyama A, Naito M, Shiramizu K, Kiyama T. Prevalence and acetabular dysplasia. Am J Orthop (Belle Mead NJ) of femoroacetabular impingement in Asian patients with 2001;30:459-467

jksronline.org J Korean Soc Radiol 2015;72(6):385-392 391 Hip Morphometry of Femoroacetabular Impingement Pattern in Patients with Ankylosing Spondylitis

강직성척추염 환자에서 대퇴비구충돌증후군 고관절 모양에 관한 연구1

이종윤1 · 이영준1 · 최정아1,2

목적: 강직성척추염 환자에서 고관절의 대퇴비구충돌증후군 양상의 고관절 모양에 대하여 분석하고 천장골염의 등급과 상관관계를 알아보고자 하였다. 대상과 방법: 384명의 강직성척추염 환자를 인구통계자료, 대퇴비구충돌증후군 양상의 영상소견과 천장골염의 등급을 중심으로 분석하였다. 대퇴비구충돌증후군을 알파각, 측면중심변연각, 권총손잡이변형을 중심으로 3가지 유형으로 나누 었다. 천장골염은 뉴욕 분류에 따라 0에서 4등급으로 나누었다. 대퇴비구충돌증후군 모양의 빈도와 천장골염과의 상관 관계를 분석하였다. 통계분석은 나이, 천장골염 등급에 대해서는 t-검증, 천장골염 등급의 세 그룹 간의 차이는 Kruskall- Wallis 검증과 Mann-Whitney U 검증을 사용하였고, Bonferroni 방법으로 사후 분석을 하였다. 결과: 384명의 환자 중에 141명(36.7%)이 대퇴비구충돌증후군 모양을 보였다. 남성이 유의하게 많았고(87.2%)(p = 0.000) pincer type (20.6%)이 가장 흔했다. 고관절의 대퇴비구충돌증후군 양상을 보이는 그룹이 천장골염 등급이 유의 하게 높고, 특히 combined-type이 유의하게 높은 천장골염 등급을 보였다. 결론: 대퇴비구충돌증후군 양상 고관절은, 특히 pincer type, 강직성척추염에서 자주 보였고, 남성에 유의하게 많았다. 이 그룹에서 천장골염 등급이 유의하게 높고, 특히 combined-type이 유의하게 높은 천장골염 등급을 보였다.

1분당서울대학교병원 영상의학과, 2한림대학교 동탄성심병원 영상의학과

392 J Korean Soc Radiol 2015;72(6):385-392 jksronline.org