Characteristics of hip involvement in patients with ankylosing spondylitis in Korea

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1 ORIGINAL ARTICLE Koren J Intern Med 2017;32: Chrcteristics of hip involvement in ptients with nkylosing spondylitis in Kore Hyemin Jeong, Yeong Hee Eun, In Young Kim, Hyungjin Kim, Jejoon Lee, Eun-Mi Koh, nd Hoon-Suk Ch Deprtment of Medicine, Smsung Medicl Center, Sungkyunkwn University School of Medicine, Seoul, Kore Received : July 21, 2015 Revised : August 25, 2015 Accepted : September 12, 2015 Correspondence to Hoon-Suk Ch, M.D. Division of Rheumtology, Deprtment of Medicine, Smsung Medicl Center, Sungkyunkwn University School of Medicine, 81 Irwon-ro, Gngnm-gu, Seoul 06351, Kore Tel: Fx: E-mil: hoonsuk.ch@smsung.com Bckground/Aims: To evlute the clinicl course of hip rthritis nd the risk fctors for hip joint replcement in ptients with nkylosing spondylitis (AS). Methods: In this retrospective nlysis, we evluted 488 AS ptients t single tertiry hospitl. At bseline nd the most recent visit to the outptient clinic from the ptients with hip rthritis in AS, rdiogrphic hip rthritis ws evluted using the Bth Ankylosing Spondylitis Rdiology Hip Index (BASRI-h). Also the verge of the hip joint spce width (interbone distnce) t three distinct sites between the cetbulum nd femorl hed ws recorded. Results: Among 488 ptients with AS, 60 ptients (12.3%) hd hip rthritis. Erythrocyte sedimenttion rte were ssocited with hip involvement (odds rtio, 1.01; 95% confidence intervl [CI], 1.00 to 1.02; p = 0.004). Long disese durtion nd dvnced xil disese were ssocited with severe hip rthritis (3 BASRI-h) t bseline. BASRI-h nd interbone distnce did not significntly chnge in ptients with hip involvement during the follow-up period of 81.4 ± 35.7 months. Five ptients hd hip joint replcement surgery during follow-up period. The body mss index (BMI) nd BASRI-h t bseline were ssocited with joint replcement surgery (hzrd rtio [HR], 1.30; 95% CI, 1.00 to 1.67; p = nd HR, 20.64; 95% CI, 2.39 to ; p = 0.006, respectively). Conclusions: Most of the ptients with hip rthritis in AS showed no significnt rdiogrphic progression during the follow-up period. High BMI nd dvnced hip rthritis t bseline were ssocited with hip joint replcement surgery in ptients with AS. Keywords: Spondylitis, nkylosing; Hip; Body mss index INTRODUCTION Ankylosing spondylitis (AS) is chronic inflmmtory disese tht primrily ffects the xil skeleton. Hip involvement is common in AS ptients nd the reported prevlence of clinicl hip involvement in AS is from 24% to 36% nd prevlence of rdiogrphic hip rthritis rnges from 9% to 22% [1-3]. Unlike new bone formtion in xil spine, synovil inflmmtion within the hip joint cuses bone erosion nd joint spce nrrowing. The histologicl ppernce of the synovil membrne in AS is chrcterized by synovil lining cell hyperplsi nd lymphoid cell ggregtes, similr to those observed in rheumtoid rthritis (RA) [4]. Progressive flexion deformity nd destruction of hip joint might lso be observed. Eventully, hip involvement cuses functionl impirment nd disbility in ptients with AS [5]. Previous studies hve reported tht erly onset of disese Copyright 2017 The Koren Assocition of Internl Medicine This is n Open Access rticle distributed under the terms of the Cretive Commons Attribution Non-Commercil License ( by-nc/3.0/) which permits unrestricted noncommercil use, distribution, nd reproduction in ny medium, provided the originl work is properly cited. pissn eissn

2 Jeong H, et l. Hip rthritis in nkylosing spondylitis nd xil disese re ssocited with hip joint involvement nd hip replcement surgery in AS [1,3]. It hs been reported tht 5% of AS ptients need hip replcement surgery [1]. In recent study, the totl joint replcement surgery rte in ptients with RA decresed 40% with the widespred use of nti-tumor necrosis fctor (nti-tnf) gents, wheres the totl joint replcement surgery rte in spondylorthritis incresed 40% [6]. Despite the worse functionl outcome in ptients with hip involvement, there re few studies concerning hip rthritis compred with the xil disese in AS. The im of the present study ws to investigte the clinicl course of hip rthritis nd the risk fctors for hip joint replcement in AS. METHODS Study popultion The subjects were selected from pool of ptients who first visited the rheumtology outptient clinic of Smsung Medicl Center in Seoul, South Kore between Jnury 2001 nd Jnury 2011 in consecutive mnner. We selected ptients dignosed with AS bsed on fulfillment of the modified New York criteri [7]. We excluded the ptients who underwent totl hip replcement surgery for both hips before the initil visit t the outptient clinic. Ptients who hd unilterl hip replcement surgery were included. Clinicl chrcteristics nd lbortory dt were collected retrospectively. Peripherl rthritis included the knee, nkle, foot, elbow, wrist nd hnd joints. Disese durtion ws defined s the time from the symptom onset to the first visit to the outptient clinic. The follow-up durtion ws defined s time from the initil visit to the lst visit t the clinic. X-ry follow-up durtion ws the time from the bseline X-ry to the most recent imge tken. Hip involvement t bseline ws defined ccording to the clinicl opinion of the rheumtologist, such s pin nd limited rnge of motion nd rdiologicl evidence of hip rthritis, defined by t lest the score of 1 in the Bth Ankylosing Spondylitis Rdiology Hip Index (BASRI-h) scoring system [8]. This study ws pproved through the Institutionl Review Bord of Smsung Medicl Center. Rdiogrphs nd scoring Pired recent rdiogrphs nd bseline pelvis X-ry were nlyzed in 60 ptients with hip rthritis. Two trined rheumtologists (HJ nd IYK) scored the rdiogrphic hip rthritis using the BASRI-h scoring system (grde 0 to 4). We lso used published methods to mesure the verge interbone distnce between the cetbulum nd femorl hed of both hips t three distinct sites: (1) t 2 mm inner of the externl end of the cetbulum; (2) t the verticl line through the femorl hed center; nd (3) t the hed-neck center line [9]. Among 60 ptients with hip rthritis, five ptients hd unilterl hip involvement. The BASRI-h grde nd interbone distnce were clculted by the men of the right nd left hips except for the five ptients who hd unilterl hip replcement surgery before the initil visit. In these five ptients who underwent unilterl hip replcement surgery before the initil visit, the rtificil joint ws not included nd only one side of the joint ws used for nlysis. In ddition, when ptients underwent hip replcement surgery during the follow-up period, BASRI-h grde becme 4 nd interbone distnce becme 0 nd men vlue of the both hip joints were used for the nlysis. Severe rdiogrphic hip involvement ws defined s 3 BASRI-h grdes t bseline. A chnge in the BAS- RI-h nd interbone distnce between the bseline nd the most recent imge ws divided by time intervls between the time of bseline nd the most recent imge ws tken. The chnges were clculted fter subtrcting the vlue of the bseline imge from the vlue of the recent imges. Therefore, in cse of rdiogrphic progression, BASRI-h vlue becomes positive nd men of interbone distnce vlue becomes negtive. The scroiliitis grde ws defined s the sum of both the right nd left scroiliitis grdes ccording to the modified New York criteri [7]. The presence of syndesmophytes t bseline ws lso ssessed. The men vlue of two reders ws used for nlysis. The intr-clss correltion coefficient of the BASRI-h grde of two reders ws (95% confidence intervl [CI], 0.91 to 0.94; p < 0.001), nd the interbone distnce vlue ws (95% CI, 0.97 to 0.98; p < 0.001). Sttisticl nlysis Descriptive sttistics were used to identify the chrcteristics of the study popultion. Ctegoricl vribles were compred between groups using the chi-squre test or Fisher exct test. For continuous vribles, the dt were 159

3 The Koren Journl of Internl Medicine Vol. 32, No. 1, Jnury 2017 presented s the men ± SD, nd vribles were compred using t tests. Univrible logistic regression nlyses were performed to identify the predictors ssocited with hip involvement. Cox proportionl hzrds models were used to estimte the hzrds rtio (HRs) with 95% CI of hip replcement surgery in ptients with hip involvement. Schoenfeld residuls were exmined for the covrites, nd significnt deprtures from the proportionl hzrds ssumption were not detected. Vribles ssocited with p vlue outcomes 0.10 were included in the multivrible nlysis. Becuse the follow-up durtion ws different between ptients, generlized estimting eqution nlysis ws performed to ssess the chnges in the BASRI-h, interbone distnce, erythrocyte sedimenttion rte (ESR), C-rective protein (CRP) level, nd body mss index (BMI) over the follow-up period. We used n exchngeble correltion structure s working correltion in repeted-mesurement design. SAS version 9.4 (SAS Institute, Cry NC, USA) nd SPSS version 19.0 (IBM Co., Armonk, NY, USA) were used for nlysis. Sttisticl significnce ws considered for p < RESULTS In totl, 488 ptients with AS were included in the nlysis. The bseline chrcteristics of ptients re shown in Tble 1. Among the 488 ptients, 60 ptients (12.3%) hd hip involvement. In univrible nlysis, ESR ws ssocited with hip involvement in AS (odds rtio [OR], 1.01; 95% CI, 1.00 to 1.02; p = 0.004) (Tble 2). The ge t disese onset, sex, disese durtion, nd smoking sttus were not significntly ssocited with hip involvement. All the ptients used nonsteroidl nti-inflmmtory drugs t the initil tretment. Follow-up durtion fter the initil visit ws longer in ptients with hip rthritis thn ptients without (97.4 ± 38.4 months vs ± 55.3 months, p < 0.001). During the follow-up period, ptients with hip rthritis used more nti-tnf gents thn ptients without hip rthritis (48.3% vs. 23.4%, p < 0.001). Among the 60 AS ptients with hip rthritis, the men BASRI-h grde ws 2.0 ± 0.7, nd the men interbone distnce ws 2.9 ± 1.0 mm t bseline. Of the 60 ptients, 10 ptients (16.7%) hd BASRI-h grde 3 or 4 nd were Tble 1. Bseline chrcteristics of ptients (n = 488) Vrible Vlue Age t disese onset, yr 25.9 ± 9.2 Mle sex 408 (83.6) Hip involvement 60 (12.3) Disese durtion, mon 39 (12 114) Peripherl rthritis, ever 121 (24.8) Enthesitis, ever 49 (10.0) Uveitis, ever 102 (20.9) Syndesmophytes 127 (26) Scroiliitis grde 4.9 ± 1.7 Body mss index, kg/m ± 3.3 Erythrocyte sediment rte, mm/hr 37.8 ± 28.7 C-rective protein, mg/dl 1.01 ( ) HLA-B27 positive (n = 365) 337 (92.3) Current smoker 49 (10.0) Vlues re presented s men ± SD, number (%), or medin (interqurtile rnge). HLA, humn leukocyte ntigen. The scroiliitis grde refers to the sum of ech side of the scroiliitis grde ccording to the modified New York criteri. clssified s with severe hip rthritis nd other 50 ptients (83.3%) with BASRI-h grde 1 or 2 were clssified s not hving severe hip rthritis. Ptients with severe hip rthritis hd longer disese durtion (142.8 ± 93.8 months vs ± 64.9 months, p = 0.001) nd hd more dvnced xil disese (sum of ech side scroiliitis grde ws 6.8 ± 1.7 vs. 5.5 ± 1.4, p = 0.014; nd presence of syndesmophyte ws 70% vs. 20%, p = 0.003) thn ptients with no severe hip rthritis. In the 60 ptients with hip rthritis, the men of X-ry follow-up durtion ws 81.4 ± 35.7 months, with medin vlue of 78 months (rnge, 23 to 198). We observed no significnt rdiogrphic chnges for the hip joint during the follow-up period. The vlue of both the BASRI-h (p = 0.138) nd interbone distnce (p = 0.296) were not significntly chnged from the bseline to the time of the most recent imge tken. Among the 60 ptients with hip involvement, five ptients (8.3%) underwent joint replcement surgery during the follow-up period. Ptients with hip joint replcement surgery showed dvnced hip rthritis nd higher BMI t bseline compred with ptients without hip replcement surgery (27.8 ± 3.1 kg/m 2 vs ± 4.2 kg/m 2, p = 0.029). And initil BASRI-h grde 160

4 Jeong H, et l. Hip rthritis in nkylosing spondylitis Interbone distnce A ESR B Other (n = 55) Hip surgery (n = 5) Bseline End of follow-up Bseline End of follow-up Other (n = 55) Hip surgery (n = 5) Bseline End of follow-up Bseline End of follow-up ( BASRI-h/yer: 0.16 ± 0.09 vs ± 0.06, p < 0.001; nd interbone distnce/yer: 0.19 ± 0.04 vs ± 0.07, p < 0.001). Tble 3 shows fctors ssocited with hip replcement surgery mong ptients with hip rthritis in AS. Multivrible nlysis reveled tht both BMI nd initil BASRI-h were ssocited with hip joint replcement surgery. In ddition, mong the 422 ptients without hip rthritis t bseline, no ptients showed significnt rdiogrphic chnges or hd hip replcement surgery during the follow-up period. Chnges in the interbone distnce nd cute phse rectnt in ptients with hip rthritis re shown in Fig. 1. The interbone distnce for five ptients with hip surgery decresed (p = 0.091) nd ws not significntly ffected in 55 other ptients. ESR nd CRP were significntly decresed t the end of follow-up from the bseline, regrdless of hip replcement surgery. In ddition, ESR nd CRP were significntly decresed in ll 488 ptients during the follow-up period, regrdless of hip joint involvement. BMI ws not chnged significntly during the follow-up period regrdless of hip joint involvement or hip replcement surgery. CRP C Other (n = 55) Hip surgery (n = 5) Bseline End of follow-up Bseline End of follow-up Figure 1. Chnges in the interbone distnce nd cute phse rectnt levels in ptients with hip rthritis. (A) The interbone distnce t bseline nd t the end of the follow-up period in ptients with nd without hip replcement surgery. Chnges in (B) erythrocyte sediment rte (ESR) nd (C) C-rective protein (CRP) t bseline nd the end of the follow-up period in ptients with nd without hip replcement surgery. p < ws higher in ptients with hip joint replcement surgery (2.6 ± 0.4 vs. 1.8 ± 0.7, p = 0.012). During the follow-up period, hip joint progression ws fster in ptients with hip replcement surgery thn ptients without surgery DISCUSSION In the present study, we ttempted to identify the rdiogrphic chnges in the hip joint nd evlute the ssocited fctors of hip rthritis in AS. Our study showed tht the prevlence of hip involvement ws 12.3% nd severe rdiogrphic hip rthritis were ssocited with longer disese durtion nd dvnced xil disese, which corresponds well with previous studies [3,10]. We found tht higher BMI ws ssocited with hip replcement surgery. These results re in greement with the RESI- SPONSER cohort, which showed tht BMI is higher in ptients with hip replcement surgery in AS compred with those without surgery [1]. Ottvini et l. [11] reported tht high BMI negtively influences the response to infliximb in AS. Ptients with psoritic rthritis (PsA) hve higher men BMI thn the generl popultion [12]. Also obese ptients with PsA re less likely to chieve sustined miniml disese ctivity compred with ptients of norml weight [13]. An ssocition between obesity nd inflmmtion hs been suggested. The levels of dipokines, such s leptin, TNF-α nd interleukin

5 The Koren Journl of Internl Medicine Vol. 32, No. 1, Jnury 2017 Tble 2. Fctors ssocited with hip involvement in ptients with nkylosing spondylitis Vrible OR (95% CI) p vlue Age t disese onset, yr ( ) Mle sex ( ) Disese durtion, mon ( ) Peripherl rthritis ( ) Enthesitis, ever ( ) Uveitis, ever ( ) Syndesmophytes ( ) Scroiliitis grde ( ) Body mss index, kg/m ( ) Erythrocyte sediment rte, mm/hr ( ) C-rective protein, mg/dl ( ) HLA-B27 positive (n = 365) ( ) Current smoker ( ) OR, odds rtio; CI, confidence intervl; HLA, humn leukocyte ntigen. The scroiliitis grde refers to the sum of ech side of the scroiliitis grde ccording to the modified New York criteri. Tble 3. Fctors ssocited with hip replcement surgery in nkylosing spondylitis ptients with hip involvement Clinicl chrcteristic Age t disese onset ( ) Mle sex ( ) Peripherl rthritis ( ) Syndesmophyte ( ) Scroiliitis grde ( ) Univrible model Multivrible model HR (95% CI) p vlue HR (95% CI) p vlue Body mss index ( ) ( ) Erythrocyte sediment rte ( ) C-rective protein ( ) BASRI-h (initil) ( ) ( ) Interbone distnce (initil), mm ( ) Anti-TNF gent use ( ) HR, hzrd rtio; CI, confidence intervl; BASRI-h, Bth Ankylosing Spondylitis Rdiology Hip Index; TNF, tumor necrosis fctor. The scroiliitis grde refers to the sum of ech side of the scroiliitis grde ccording to the modified New York criteri. positively correlte with BMI, nd the concentrtions of dipokines re incresed in ptients with metbolic syndrome [14]. A recent study reveled tht elevted serum dipokines re ssocited with rdiogrphic dmge in AS [15]. The systemic overlod of dipokines hs been ssocited with chronic inflmmtion, nd this condition could be pplicble to the involvement of hip rthritis in AS. Biomechnicl fctors could influence rdiogrphic progression. Mechnicl strin drives enthesel inflmmtion nd new bone formtion in spondylorthritis vi the Erk 1/2 signling pthwy [16]. It hs been reported tht obesity is incresed in ptients with primry totl hip rthroplsty [17]. Thus, the high incidence of hip rthritis progression resulting in hip joint replcement surgery in obese ptients might reflect inflmmtion ssocited with mechnotrnsduction nd immune re

6 Jeong H, et l. Hip rthritis in nkylosing spondylitis sponse fctors. In the present study, most of the ptients showed no significnt rdiogrphic chnges during the follow-up period. Among the 60 AS ptients with hip rthritis, only five ptients showed rdiogrphic progression nd underwent joint replcement surgery nd the other 55 ptients showed lmost no rdiogrphic chnges during the follow-up period. Advnced hip joint dmge nd high BMI t bseline were risk fctors for the hip joint replcement surgery. Ptients in our study hd visited the rheumtology outptient clinic regulrly nd received stndrd tretment for AS such s non-steroidl nti-inflmmtory drugs or nti-tnf gents. Men ESR nd CRP decresed significntly over the follow-up period, regrdless of hip involvement or hip replcement surgery. These results suggest tht when AS ptients re treted properly, the possibility of significnt rdiogrphic hip chnges is low. Under these conditions, BMI might influence the rdiogrphic progression of the hip joint. In ddition, erly initition of tretment before rdiogrphic hip chnges occur my be helpful in preventing hip joint replcement surgery. This study hs some limittions. We conducted retrospective study, nd clinicl prmeters such s Bth Ankylosing Spondylitis Disese Activity Index, Bth Ankylosing Spondylitis Functionl Index, rnge of joint mobility, or level of dily physicl ctivity were not systemiclly vilble. The strength of this study is tht we provided the evidence tht BMI might influence the outcome of hip rthritis in ptients with AS. In summry, the present study reveled tht most of the ptients showed no significnt rdiogrphic chnges during the follow-up period. High BMI nd dvnced rdiogrphic hip rthritis t bseline were ssocited with hip joint replcement surgery in ptients with AS. Further study is wrrnted to clrify the role of obesity in the pthogenesis nd progression of hip rthritis in AS. KEY MESSAGE 1. Most of the ptients with hip rthritis in nkylosing spondylitis (AS) showed no significnt rdiogrphic progression during the follow-up period. 2. High body mss index nd dvnced hip rthritis t bseline were ssocited with hip joint replcement surgery in ptients with AS. Conflict of interest No potentil conflict of interest relevnt to this rticle ws reported. Acknowledgments This study ws finncilly supported through grnt from the Kore Helth Industry Development Institute (HI14C2285). REFERENCES 1. Vnder Cruyssen B, Munoz-Gomriz E, Font P, et l. Hip involvement in nkylosing spondylitis: epidemiology nd risk fctors ssocited with hip replcement surgery. Rheumtology (Oxford) 2010;49: Burki V, Gossec L, Pyet J, et l. Prevlence nd chrcteristics of hip involvement in spondylorthritis: single-centre observtionl study of 275 ptients. Clin Exp Rheumtol 2012;30: Chen HA, Chen CH, Lio HT, et l. Fctors ssocited with rdiogrphic spinl involvement nd hip involvement in nkylosing spondylitis. Semin Arthritis Rheum 2011;40: Revell PA, Myston V. Histopthology of the synovil membrne of peripherl joints in nkylosing spondylitis. Ann Rheum Dis 1982;41: Yılmz O, Tutoglu A, Grip Y, Ozcn E, Bodur H. Helth-relted qulity of life in Turkish ptients with nkylosing spondylitis: impct of peripherl involvement on qulity of life in terms of disese ctivity, functionl sttus, severity of pin, nd socil nd emotionl functioning. Rheumtol Int 2013;33: Mertelsmnn-Voss C, Lymn S, Pn TJ, Goodmn SM, Figgie MP, Mndl LA. US trends in rtes of rthroplsty for inflmmtory rthritis including rheumtoid rthritis, juvenile idiopthic rthritis, nd spondylorthritis. Arthritis Rheumtol 2014;66: vn der Linden S, Vlkenburg HA, Cts A. Evlution of dignostic criteri for nkylosing spondylitis: proposl for modifiction of the New York criteri. Arthritis Rheum 1984;27:

7 The Koren Journl of Internl Medicine Vol. 32, No. 1, Jnury McKy K, Brophy S, Mck C, Dorn M, Clin A. The development nd vlidtion of rdiogrphic grding system for the hip in nkylosing spondylitis: the bth nkylosing spondylitis rdiology hip index. J Rheumtol 2000;27: Konst M, Sfikkis PP, Bourni VK, Krrs D, Iliopoulos A. Absence of rdiogrphic progression of hip rthritis during infliximb tretment for nkylosing spondylitis. Clin Rheumtol 2013;32: Zho J, Zheng W, Zhng C, Li J, Liu D, Xu W. Rdiogrphic hip involvement in nkylosing spondylitis: fctors ssocited with severe hip diseses. J Rheumtol 2015;42: Ottvini S, Allnore Y, Tubch F, et l. Body mss index influences the response to infliximb in nkylosing spondylitis. Arthritis Res Ther 2012;14:R Bhole VM, Choi HK, Burns LC, et l. Differences in body mss index mong individuls with PsA, psorisis, RA nd the generl popultion. Rheumtology (Oxford) 2012;51: Eder L, Thvneswrn A, Chndrn V, Cook RJ, Gldmn DD. Obesity is ssocited with lower probbility of chieving sustined miniml disese ctivity stte mong ptients with psoritic rthritis. Ann Rheum Dis 2015;74: Deng Y, Scherer PE. Adipokines s novel biomrkers nd regultors of the metbolic syndrome. Ann N Y Acd Sci 2010;1212:E1-E Syrbe U, Cllhoff J, Conrd K, et l. Serum dipokine levels in ptients with nkylosing spondylitis nd their reltionship to clinicl prmeters nd rdiogrphic spinl progression. Arthritis Rheumtol 2015;67: Jcques P, Lmbrecht S, Verheugen E, et l. Proof of concept: enthesitis nd new bone formtion in spondylorthritis re driven by mechnicl strin nd stroml cells. Ann Rheum Dis 2014;73: Singh JA, Lewllen DG. Incresing obesity nd comorbidity in ptients undergoing primry totl hip rthroplsty in the U.S.: 13-yer study of time trends. BMC Musculoskelet Disord 2014;15: