Y. Yazici 1, D. Moniz Reed 2, C. Klem 2, L. Rosenblatt 2, G. Wu 2, J.M. Kremer 3

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1 Greter remission rtes in ptients with erly versus long-stnding disese in biologic-nive rheumtoid rthritis ptients treted with btcept: post hoc nlysis of rndomised clinicl tril dt Y. Yzici 1, D. Moniz Reed 2, C. Klem 2, L. Rosenbltt 2, G. Wu 2, J.M. Kremer 3 1 NYU Hospitl for Joint Diseses, New York, USA; 2 Bristol-Myers Squibb, Princeton, NJ, USA; 3 Center for Rheumtology, Albny Medicl College, Albny, NY, USA. Abstrct Objective Current im of rheumtoid rthritis (RA) tretment is to chieve remission in s mny ptients s possible. Rtes of remission nd clinicl outcomes fter tretment with btcept in biologic-nive rheumtoid rthritis (RA) ptients with erly disese nd n indequte response to methotrexte (MTX) versus ptients with 10 yers of disese were ssessed. Methods Dt from two trils ssessing the efficcy of btcept in MTX indequte responders were pooled for this explortory post hoc nlysis. Ptients with disese durtion of 2 yers t bseline (erly disese), originlly ssigned to n btcept 10 mg/kg tretment rm nd entered into long-term extension (LTE), were compred with ptients with 10 yers of disese (long-stnding RA). Remission, DAS28-CRP, ACR 70 responses nd the Routine Assessment of Ptient Index Dt 3 (RAPID3), improvement in physicl function s mesured by the Helth Assessment Questionnire Disbility Index (HAQ-DI). Results Twenty-three percent of these ptients (n=108) hd erly disese. A higher percentge of ptients with erly disese chieved DAS28-CRP remission versus ptients with long-stnding disese (35.2% vs. 19.4% t yer 1, p<0.01; 46.0% vs. 30.9% t yer 3, p<0.05). In ddition, higher percentge of the subgroup with erly RA chieved ACR70 responses. More ptients with erly RA hd meningful improvement in their HAQ-DI (75.2% vs. 60.4%; p<0.05) nd RAPID3 scores t one yer (men chnges from bseline of -9.6 vs. -8.1; p=0.009) Conclusions These dt provide dditionl support for the possible use of btcept in biologic-nive ptients who hve hd indequte response to MTX, erlier in their disese course. Key words rheumtoid rthritis, btcept, erly rthritis, DAS28, RAPID3 Clinicl nd Experimentl Rheumtology 2011; 29:

2 Yusuf Yzici, MD, Assistnt Professor Dine Moniz Reed, PhrmD Christin Klem, PhrmD Lis Rosenbltt, MD George Wu Joel M. Kremer, MD, Professor Plese ddress correspondence nd reprint requests to: Yusuf Yzici, MD, New York University School of Medicine, Seligmn Center for Advnced Therpeutics, NYU Hospitl for Joint Diseses, New York, USA. E-mil: Received on April 29, 2010; ccepted in revised form on Jnury 26, Copyright CLINICAL AND EXPERIMENTAL RHEUMATOLOGY Abbrevitions: ACR: Americn College of Rheumtology AIM: Abtcept in Indequte Responders to Methotrexte DAS28-CRP: 28-joint count Disese Activity Score using C-rective protein DMARD: disese-modifying nti-rheumtic drugs HAQ-DI: Helth Assessment Questionnire Disbility Index LDAS: low disese ctivity score LTE: long-term extension mtss: Gennt-modified totl Shrp score MTX: methotrexte TNF: tumour necrosis fctor RA: rheumtoid rthritis RAPID3: Routine Assessment of Ptient Index Dt 3 Competing interests Yusuf Yzici s been consultnt for Bristol-Myers Squibb, Celgene, Centocor, Genentech, Merck, Pfizer, Roche nd UCB, nd served on the speker bureus of Bristol-Myers Squibb nd Genentech. Dine Moniz Reed, Christin Klem, Lis Rosenbltt, nd George Wu re full-time employees nd stockholders in Bristol- Myers Squibb. Joel Kremer hs been consultnt nd speker for Bristol-Myers Squibb nd hs lso received grnt support from Bristol-Myers Squibb for reserch ctivities. The studies of btcept discussed were funded by Bristol-Myers Squibb. Introduction The consequences of indequtely treted rheumtoid rthritis (RA) include severe functionl decline, incresed mortlity, work disbility, joint replcement surgery, nd medicl costs (1, 2). Studies hve suggested tht substntil nd irreversible joint destruction lredy occurs within the first 2 yers fter disese onset (3, 4). Although there is no cure for RA, most ptients with erly disese cn be treted successfully, with some chieving incresed remission rtes compred with 10 to 15 yers go (5-10). The recognition of the potentil for severe long-term disbility nd comorbidity in mny ptients supports the use of effective erly therpeutic interventions to improve long-term outcomes (11, 12). Abtcept is biologic disese-modifying ntirheumtic drug (DMARD) for the tretment of RA nd JIA tht selectively modultes the CD80/CD86: CD28 costimultory signl required for full T-cell ctivtion. The efficcy of btcept in dult ptients with n indequte response to methotrexte (MTX) hs been demonstrted s monotherpy nd in combintion with MTX (13-15). The phse 2b IM tril estblished the efficcy of btcept in this ptient popultion (15, 16), nd the phse 3, rndomised, double-blind, plcebo-controlled Abtcept in Indequte Responders to Methotrexte (AIM) tril confirmed the clinicl benefits of btcept in lrger popultion of ptients with n indequte response to MTX (14). In the present study, dt from these two double-blind, plcebo-controlled trils were pooled for this explortory post hoc nlysis. The objectives of this nlysis were to ssess rtes of remission, clinicl outcomes, nd x-ry progression fter tretment with btcept in biologic-nive RA ptients with n indequte response to MTX who hve erly disese ( 2 yers durtion) compred with the rtes in ptients with 10 yers of disese (long-stnding RA). Methods The detils of the phse 2b nd AIM trils hve been published previously (14, Abtcept in erly RA / Y. Yzici et l. 16). Briefly, ll ptients who enrolled in the long-term extension (LTE) portion of both AIM nd the phse 2b trils received fixed dose of btcept 10 mg/kg in ddition to bckground MTX. To be eligible for nlysis, ptients hd to meet the following criteri: disese durtion t bseline of 2 yers (erly disese, chosen s common definition for erly RA) or 10 yers (longstnding RA), originlly ssigned to the btcept 10 mg/kg tretment rm, nd entered into the LTE. Adjustments to bckground disesemodifying nti-rheumtic drugs (DMARDs) nd other concomitnt medictions were permitted during the LTE portion t the discretion of the investigtor, bsed on the clinicl sttus of the ptient. Outcomes ssessed t the end of yers 1, 2, nd 3 included Americn College of Rheumtology (ACR) responses, remission nd low disese ctivity s defined by the 28-joint count Disese Activity Score using C-rective protein (DAS28-CRP), improvement in physicl function s mesured by the Helth Assessment Questionnire Disbility Index (HAQ-DI), nd the Routine Assessment of Ptient Index Dt 3 (RAPID3), n index of only the ptientreported outcome mesures of physicl function, pin, nd globl ssessment of disese ctivity tht is scored on scle of 0 to 30 (17). Rdiogrphic outcomes for ptients from the AIM tril were vilble for the btcept tretment group t bseline nd t the end of yers 1, 2, nd 3. Gennt-modified Shrp scores for joint spce nrrowing, erosions, nd the totl were determined for ptients with erly RA nd those with long-stnding disese. Sttisticl nlysis Sttisticl methods used in the AIM nd phse 2b studies hve been previously described (14, 16). In this study, ll efficcy nlyses were performed bsed on the s-observed dt, i.e. dt vilble for the specified prmeter t yers 1, 2, nd 3, except for the rdiogrphic nlysis. All sttisticl tests were bsed on two-sided 5% level of significnce, nd ll nlyses were performed using 495

3 Abtcept in erly RA / Y. Yzici et l. Percentge ptients (%) Fig. 1. Remission rtes in ptients with erly or long-stnding RA treted with btcept. Percentge of btcept-treted ptients with erly rheumtoid rthritis (RA) () or long-stnding RA (b) who were in remission (drk dimonds) or hd low disese ctivity score (LDAS, light squres), mesured t bseline through yer 3. Remission defined s 28-joint count Disese Activity Score using C-rective protein (DAS28- CRP) <2.6; LDAS defined s DAS28-CRP <3.2. p<0.01; b p<0.05, both versus long-stnding RA. LTE = long-term extension. The ptients vilble for nlysis t ech time point re shown in the tble below: LDAS DAS < 2.6 b Yer 1, n Yer 2, n Yer 3, n Percentge ptients (%) Tble I. Chrcteristics of ptients with erly rheumtoid rthritis (RA) ( 2 yers) or longstnding RA ( 10 yers) who entered the long-term extension (LTE) of the phse 2b nd phse 3 (AIM) trils of btcept in ptients with n indequte response to MTX, nd who met the inclusion criteri for this study. All ptients were in the btcept 10-mg/kg ctive therpy groups. With the exception of durtion of disese, ll bseline clinicl chrcteristics were similr between the two groups. SD: stndrd devition; DAS28-CRP: 28-joint count Disese Activity Score using C-rective protein; CDAI: clinicl disese ctivity index; RAPID3: Routine Assessment of Ptient Index Dt 3; HAQ-DI: Helth Assessment Questionnire Disbility Index; VAS: visul nlogue scle. Erly RA (n=108) Long-stnding RA (n=159) Age (yers), men ± SD 50.3 ± ± 12.1 Femle gender (%) Disese durtion (yers), men ± SD 1.2 ± ± 6.87 DAS28-CRP, men ± SD 6.3 ± ± 0.82 CDAI, men ± SD 44.4 ± ± 11.7 RAPID3, men ± SD 17.2 ± ± 0.44 Tender joints, men ± SD 30.7 ± ± 13.2 Swollen joints, men ± SD 21.4 ± ± 9.4 HAQ-DI, men ± SD 1.5 ± ± 0.68 Pin (100-mm VAS), men ± SD 60.0 ± ± 20.2 Ptient globl ssessment (100-mm VAS), men ± SD 64.0 ± ± Physicin globl ssessment (100-mm VAS), men ± SD 64.0 ± ± 15.1 Rheumtoid fctor positive (%) CRP level (mg/l), men ± SD 33.0 ± ± 28.0 SAS softwre, version 8.2 (SAS Institute, Cry, North Crolin). The rdiogrphic nlyses included ll observed dt t bseline nd t yers 1, 2, nd 3. Missing nnul rdio-grphic dt were imputed with liner extrpoltion for discontinued subjects, provided these subjects hd dt vilble t bseline nd for t lest 1 post-tretment time point prior to discontinution. Summry sttistics nd cumultive probbility plot were generted for chnges from bseline in the Gennt-modified Shrp scores t yers 1, 2, nd 3 by disese durtion cohort ssignment. Results Of the 616 ptients who were rndomised to the btcept 10 mg/kg tretment rms in the phse 2b nd AIM trils, 462 enrolled in the LTE period (75% of rndomised ptients 496

4 Abtcept in erly RA / Y. Yzici et l. who completed the double-blind phse). Twenty-three percent of these ptients (n=108) hd erly disese (men disese durtion 14±8 months; Tble I), 34% hd long-stnding disese (men disese durtion 17.5±6.87 yers; Tble I). The clinicl chrcteristics of this erly RA ptient popultion re reported in Tble I nd reflect study prticipnts with moderte-to-severe RA. With the exception of disese durtion (1.2 versus 17.5 yers), bseline chrcteristics were similr between the erly RA cohort nd the long-stnding RA comprtor cohort (subjects with disese durtion 10 yers). As would lso be expected, the men ge of the erly RA cohort ws pproximtely 5 yers younger thn the cohort with long-stnding disese (Tble I). Ptients with erly RA were significntly more likely to chieve DAS28- CRP remission versus ptients with long-stnding disese t yer 1 (35.2% in remission vs. 19.4%; p<0.01; Fig. 1A), yer 2 (32.0% in remission vs. 19.7%; p<0.05), nd yer 3 (46.0% in remission vs. 30.9%; p<0.05). A greter percentge of ptients with erly RA chieved low disese ctivity (DAS28- CRP <3.2) compred with ptients who hd long-stnding disese durtion (Fig. 1B). A high percentge of study prticipnts with erly RA lso ttined significnt clinicl response s mesured by ACR70 response criteri, with sttisticlly significntly higher percentge of ACR70 responders t both yer 1 nd yer 3 for the erly RA cohort versus those with long-stnding disese (36.8% vs. 25.0% t yer 1, nd 44.3% vs. 30.4% t yer 3, p<0.05 for both comprisons; Fig. 2A nd 2B). In ddition, the percentge of ptients who chieved ACR50 response criteri lso tended to be higher for those with erly RA. In this sub-nlysis, the chnge in RAPID3 scores from bseline ws significntly greter t yer 1 in ptients with erly RA treted with btcept versus ptients with long-stnding disese treted with btcept (men chnge from bseline of -9.6 vs. -8.1; p=0.009). Furthermore, there ws trend for sustined greter benefit of Percentge ptients (%) b Percentge ptients (%) Fig. 2. ACR response in ptients with erly or long-stnding RA treted with btcept. Percentge of btcept-treted ptients with erly RA () or long-stnding RA (b) who chieved ACR20 (drk dimonds), ACR50 (light squres), nd ACR70 (drk tringles) response criteri, mesured t bseline through yer 3. P<0.05, both versus long-stnding RA. The ptients vilble for nlysis t ech time point re shown in the tble below: ACR 20 ACR 50 ACR Yer 1, n Yer 2, n Yer 3, n btcept tretment in the erly RA ptients compred with ptients with long-stnding disese s mesured by RAPID3 scores t yers 2 nd 3. Despite similr levels of functionl disbility t bseline s mesured by the HAQ-DI, significntly more ptients with erly RA hd cliniclly meningful improvement (HAQ-DI 0.3 unit) in their HAQ-DI scores t yer 1 compred with the estblished RA cohort (ssessed s the percentge of ptients chieving n improvement of 0.3 in the HAQ-DI, exceeding the minimum cliniclly importnt difference of 0.22 (18)). Rdiogrphic progression ws ssessed in the subset of ptients from these cohorts who prticipted in the AIM tril using the Gennt-modified Shrp scoring system. In ptients with erly RA nd ptients with long-stnding disese, btcept therpy in combintion with MTX resulted in progressively smller increses in rdiogrphic scores t ech of the three yers in this nlysis, suggesting tht btcept my hve n incresing disese-modifying effect on 497

5 Abtcept in erly RA / Y. Yzici et l. Tble II. Men Gennt-modified totl Shrp score (mtss) t bseline, nd men chnges in mtss t yers 1, 2, nd 3 for btcept-treted ptients with erly RA or long-stnding RA. RA durtion 2 yers (n=73) structurl dmge over time (Tble II). This benefit occurred in both groups, despite ptients with long-stnding disese hving higher Gennt-modified totl Shrp scores t bseline compred with ptients who hd disese durtion Men mtss (SD) RA durtion 10 yers (n=100) Bseline 23.8 (21.3) 69.8 (38.1) Yer (2.04) 0.60 (1.24) Yer (1.30) 0.46 (1.14) Yer (1.11) 0.13 (0.94) Men chnge from bseline in m TSS b Men chnge from bseline in m TSS Cumultive probbility Fig. 3. Chnge in rdiogrphic score in ptients with erly or long-stnding RA treted with btcept. Cumultive distribution of men chnges from bseline in Gennt-modified totl Shrp Scores (mtss) for btcept-treted ptients with erly RA () nd long-stnding RA (b) t yers 1, 2, nd 3. All rdiogrphic dt were obtined from prticipnts in the ctive therpy group of the phse 3 (AIM) tril of btcept in ptients with n indequte response to MTX. of 2 yers or less (69.8 vs. 23.8, respectively). The cumultive distributions of chnges in Gennt-modified totl Shrp scores (mtss) re lso similr for both tretment groups (Fig. 3) nd re similr to previously reported results for the totl popultion of ptients treted with btcept in the AIM study (19). Discussion The purpose of this post hoc nlysis ws to ssess rtes of remission nd clinicl outcomes fter tretment with btcept in biologic-nive RA ptients with erly disese ( 2 yers) nd n indequte response to MTX, nd compre these rtes with those in ptients with longer disese durtion ( 10 yers). The objective ws to see if disese durtion t the time of btcept initition mde difference in clinicl response in this secondry nlysis of rndomised clinicl tril dtset. The group of ptients with erly RA hd significntly higher rtes of remission compred with those with long-stnding disese, despite the fct tht these trils were not powered to detect differences in these subsets, suggesting tht the dt re likely robust nd the effect represents true differences in tretment response. Greter improvements were observed in clinicl mesures of low disese ctivity (ACR70), ptient-reported outcomes (RAPID3 index), nd physicl disbility (HAQ-DI) in the erly RA cohort compred to the long stnding disese cohort. Rdiogrphic mesures of structurl dmge progression demonstrted tht btcept in combintion with MTX inhibits the progression of structurl dmge in RA ptients with both erly nd long-stnding disese. It should be noted tht the erly RA cohort nlysed here ws smll, nd neither the phse 2b tril nor the AIM tril ws originlly designed or powered to nswer the questions sked in this subnlysis. There re severl other limittions inherent in this type of nlysis. The subgroups were not generted by rndom ssignment, nd lthough the bseline clinicl disese chrcteristics pper similr, the sub-groups my not hve hd uniform disese chrcteristics nd disese prognosis. Finlly, the dt nlysed were s observed nd, despite high completion rtes (pproximtely 80%), my not reflect the full rnge of ptient popultions with erly RA (20, 21). These fctors must be considered when interpreting the results (22). However, the recent 498

6 report of the efficcy of btcept in n erly disese popultion provides support to the findings reported here (23). In conclusion, RA ptients with erly disese ( 2 yers durtion) in this study pper to hve more significnt improvement in their disese ctivity compred with ptients with long-stnding disese ( 10 yers), with bout hlf of the ptients in DAS28-CRP remission t 3 yers. Tken together, these dt my provide dditionl support for the use of btcept in biologic-nive RA ptients with erly disese who hve hd n indequte response to MTX. Authors contributions YY helped design the nlysis, interpret the dt, nd helped drft the mnuscript. DMR helped design the nlysis, interpret the dt, nd helped drfted the mnuscript. CK helped design the nlysis, interpret the dt, nd helped drft the mnuscript. LR helped design the nlysis, interpret the dt, nd helped drft the mnuscript. GW nlysed nd interpreted the dt nd helped drft the mnuscript. JMK helped design the study, collect nd interpret the dt, nd helped drft the mnuscript. All uthors red nd pproved the finl mnuscript. References 1. PINCUS T, CALLAHAN LF, SALE WG, BROOKS AL, PAYNE LE, VAUGHN WK: Severe functionl declines, work disbility, nd incresed mortlity in seventy-five rheumtoid rthritis ptients studied over nine yers. Arthritis Rheum 1984; 27: WOLFE F, MITCHELL DM, SIBLEY JT et l.: The mortlity of rheumtoid rthritis. Arthritis Rheum 1994; 37: MÖTTÖNEN TT: Prediction of erosiveness nd rte of development of new erosions in erly rheumtoid rthritis. Ann Rheum Dis 1988; 47: FUCHS HA, KAYE JJ, CALLAHAN LF, NANCE EP, PINCUS T: Evidence of significnt rdiogrphic dmge in rheumtoid rthritis within the first 2 yers of disese. J Rheumtol 1989; 16: GRIGOR C, CAPELL H, STIRLING A et l.: Effect of tretment strtegy of tight control for rheumtoid rthritis (the TICORA study): single-blind rndomised controlled tril. Lncet 2004; 364: GOEKOOP-RUITERMAN YP, DE VRIES-BOU- WSTRA JK, ALLAART CF et l.: Clinicl nd rdiogrphic outcomes of four different tretment strtegies in ptients with erly rheumtoid rthritis (the BeSt study): rndomized, controlled tril. Arthritis Rheum 2005; 52: BREEDVELD FC, WEISMAN MH, KAVAN- AUGH AF et l.: The PREMIER study: A multicenter, rndomized, double-blind clinicl tril of combintion therpy with dlimumb plus methotrexte versus methotrexte lone or dlimumb lone in ptients with erly, ggressive rheumtoid rthritis who hd not hd previous methotrexte tretment. Arthritis Rheum 2006; 54: BATHON JM, MARTIN RW, FLEISCHMANN RM et l.: A comprison of etnercept nd methotrexte in ptients with erly rheumtoid rthritis. N Engl J Med 2000; 343: KLARESKOG L, VAN DER HEIJDE D, DE JAG- ER JP et l.; TEMPO (TRIAL OF ETANERCEPT AND METHOTREXATE WITH RADIOGRAPHIC PATIENT OUTCOMES) STUDY INVESTIGATORS: Therpeutic effect of the combintion of etnercept nd methotrexte compred with ech tretment lone in ptients with rheumtoid rthritis: double-blind rndomised controlled tril. Lncet 2004; 363: ST CLAIR EW, VAN DER HEIJDE DM, SMOLEN JS et l.; ACTIVE-CONTROLLED STUDY OF PATIENTS RECEIVING INFLIXIMAB FOR THE TREATMENT OF RHEUMATOID ARTHRITIS OF EARLY ONSET STUDY GROUP: Combintion of infliximb nd methotrexte therpy for erly rheumtoid rthritis: rndomized, controlled tril. Arthritis Rheum 2004; 50: EMERY P: Erly rheumtoid rthritis: therpeutic strtegies. Scnd J Rheumtol Suppl 1994; 100: LARD LR, VISSER H, SPEYER I et l.: Erly versus delyed tretment in ptients with recent-onset rheumtoid rthritis: comprison of two cohorts who received different tretment strtegies. Am J Med 2001; 111: MORELAND LW, ALTEN R, VAN DEN BOSCH F et l.: Costimultory blockde in ptients with rheumtoid rthritis: pilot, dose-find- Abtcept in erly RA / Y. Yzici et l. ing, double-blind, plcebo-controlled clinicl tril evluting CTLA-4Ig nd LEA29Y eighty-five dys fter the first infusion. Arthritis Rheum 2002; 46: KREMER JM, GENANT HK, MORELAND LW et l.: Effects of btcept in ptients with methotrexte-resistnt ctive rheumtoid rthritis: rndomized tril. Ann Intern Med 2006; 144: KREMER JM, DOUGADOS M, EMERY P et l.: Tretment of rheumtoid rthritis with the selective costimultion modultor btcept: twelve-month results of phse iib, doubleblind, rndomized, plcebo-controlled tril. Arthritis Rheum 2005; 52: KREMER JM, WESTHOVENS R, LEON M et l.: Tretment of rheumtoid rthritis by selective inhibition of T-cell ctivtion with fusion protein CTLA4Ig. N Engl J Med 2003; 349: PINCUS T, BERGMAN MJ, YAZICI Y, HINES P, RAGHUPATHI K, MACLEAN R: An index of only ptient-reported outcome mesures, routine ssessment of ptient index dt 3 (RAPID3), in two btcept clinicl trils: similr results to disese ctivity score (DAS28) nd other RAPID indices tht include physicin-reported mesures. Rheumtology (Oxford) 2008; 47: WELLS GA, TUGWELL P, KRAAG GR, BAKER PR, GROH J, REDELMEIER DA: Minimum importnt difference between ptients with rheumtoid rthritis: the ptient s perspective. J Rheumtol 1993; 20: GENANT HK, PETERFY CG, WESTHOVENS R et l.: Abtcept inhibits progression of structurl dmge in rheumtoid rthritis: results from the long-term extension of the AIM tril. Ann Rheum Dis 2008; 67: PINCUS T, YAZICI Y, SOKKA T: Quntittive mesures of rheumtic diseses for clinicl reserch versus stndrd clinicl cre: differences, dvntges nd limittions. Best Prct Res Clin Rheumtol 2007; 21: YAZICI Y, KAUTIAINEN H, SOKKA T: Differences in clinicl sttus mesures in different ethnic/rcil groups with erly rheumtoid rthritis: implictions for interprettion of clinicl tril dt. J Rheumtol 2007; 34: ASSMANN SF, POCOCK SJ, ENOS LE, KASTEN LE: Subgroup nlysis nd other (mis)uses of bseline dt in clinicl trils. Lncet 2000; 355: WESTHOVENS R, ROBLES M, XIMENES AC et l.: Clinicl efficcy nd sfety of btcept in methotrexte-nive ptients with erly rheumtoid rthritis nd poor prognostic fctors. Ann Rheum Dis 2009; 68:

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