Evaluation of 5 versus 10 granulocyteaphaeresis sessions in steroid-dependent ulcerative colitis: A pilot, prospective, multicenter, randomized study
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1 PO Box 2345, Beijing , Chin World J Gstroenterol 2007 April 21; 13(15): World Journl of Gstroenterology ISSN wjg@wjgnet.com 2007 The WJG Press. All rights reserved. RAPID COMMUNICATION Evlution of 5 versus 10 grnulocytepheresis sessions in steroid-dependent ulcertive colitis: A pilot, prospective, multicenter, rndomized study Elen Ricrt, Mri Esteve, Montserrt Andreu, Frncesc Csells, Dvid Monfort, Miquel Sns, Ntli Oudovenko, Rúl Lfuente, Julián Pnés Elen Ricrt, Dvid Monfort, Hospitl de Snt Pu, Brcelon, Spin Mri Esteve, Hospitl Mútu de Terrss, Terrss, Spin Montserrt Andreu, Hospitl del Mr, Brcelon, Spin Frncesc Csells, Hospitl de l Vll d Hebró, Brcelon, Spin Miquel Sns, Julián Pnés, Hospitl Clínic, CIBER-EHD, Brcelon, Spin Ntli Oudovenko, Rúl Lfuente, Otsuk Phrmceuticl, Spin Supported by Otsuk Phrmceuticl Correspondence to: Elen Ricrt, MD, PhD, Gstroenterology Deprtment, Hospitl Clínic de Brcelon, C/Villrroel 170, Brcelon, Spin. ericrt@clinic.ub.es Telephone: Fx: Received: Accepted: The WJG Press. All rights reserved. Key words: Ulcertive colitis; Grnulocytepheresis; Steroid-dependence; Inflmmtory bowel diese tretment Ricrt E, Esteve M, Andreu M, Csells F, Monfort D, Sns M, Oudovenko N, Lfuente R, Pnés J. Evlution of 5 versus 10 grnulocytepheresis sessions in steroid-dependent ulcertive colitis: A pilot, prospective, multicenter, rndomized study. World J Gstroenterol 2007; 13(15): Abstrct AIM: To evlute the efficcy of 5 compred to 10 grnulocytepheresis sessions in ptients with ctive steroid-dependent ulcertive colitis. METHODS: In this pilot, prospective, multicenter rndomized tril, 20 ptients with modertely ctive steroid-dependent ulcertive colitis were rndomized to 5 or 10 grnulocytepheresis sessions. The primry objective ws clinicl remission t wk 17. Secondry mesures included endoscopic remission nd steroid consumption. RESULTS: Nine ptients were rndomized to 5 grnulocytepheresis sessions (group 1) nd 11 ptients to 10 grnulocytepheresis sessions (group 2). At wk 17, 37.5% of ptients in group 1 nd 45.45% of ptients in group 2 were in clinicl remission. Clinicl remission ws ccompnied by endoscopic remission in ll cses. Eighty-six percent of ptients chieving remission were steroid-free t wk 17. Dily steroid requirements were significntly lower in group 2. Eighty-nine per cent of ptients remined in remission during one yer followup. One serious dverse event, not relted to the study therpy, ws reported. CONCLUSION: Grnulocytepheresis is sfe nd effective for the tretment of steroid-dependent ulcertive colitis. In this popultion, incresing the number of pheresis sessions is not ssocited with higher remission rtes, but ffords significnt steroid-spring effect. INTRODUCTION Ulcertive colitis (UC) is chronic relpsing inflmmtory disorder. Corticosteroids re the minsty of tretment to induce remission. However, long-term corticosteroid use is not recommended due to both toxicity nd lck of efficcy. In ddition, steroid dependency nd resistnce occur frequently in ptients with UC [1]. In these ptients, immune modultors (zthioprine/6-mercptopurine) [2] nd more recently the chimeric monoclonl ntibody ginst tumor necrosis fctor, infliximb, hve shown therpeutic efficcy [3], but proportion of ptients re intolernt or suffer dverse events relted to these medictions. Therefore, other therpies re needed to provide non-surgicl nd sfe lterntives for ptients who fil to respond to conventionl tretment. In vitro nd in vivo studies hve suggested tht UC relpses re ssocited with n influx of grnulocytes nd monocytes/mcrophges into the mucosl tissue, nd these cell types re regrded s key meditors of mucosl dmge [4]. Reducing grnulocytes nd monocytes by pheresis hs the potentil to reduce bowel inflmmtion nd to improve ptient sttus. Severl controlled nd uncontrolled studies hve ssessed the sfety nd efficcy of grnulocytepheresis (GCAP) in steroid-dependent UC [5-8], steroid-refrctory UC [9-11], or s first-line therpy in nïve UC ptients [12,13]. However, the optiml tretment scheme is still to be estblished. In study by Hni et l [9], lmost 40% of ptients with steroid-dependent UC entered into remission fter 5 sessions of GCAP compred to
2 2194 ISSN CN /R World J Gstroenterol April 21, 2007 Volume 13 Number 15 80% fter 10 sessions. However, in this study the number of pheresis sessions ws not estblished rndomly but bsed on clinicl demnd, nd the question whether higher number of pheresis increses the efficcy of this tretment remins open. We report the results of smll pilot prospective, multicenter, rndomized study compring the efficcy of 5 GCAP nd 10 GCAP sessions to induce remission in steroid-dependent UC. The primry end point of the study ws clinicl remission t wk 17. MATERIALS AND METHODS Ptients This ws pilot open, prospective, multicenter, rndomized study evluting the efficcy nd sfety of 5 compred to 10 GCAP sessions in ptients with modertely ctive steroid-dependent UC. The study ws conducted in five centers in Spin ccording to the Declrtion of Helsinki nd the Good Clinicl Prctice guidelines. The study ws pproved by the Institutionl Review Bord of ech prticipting center nd written informed consent ws obtined from ll ptients. Ptients were included in the study if they were between 18 nd 75 yers of ge nd hd clinicl nd endoscopic evidence of modertely ctive UC defined s clinicl ctivity index (CAI) 6 nd 12 nd n endoscopic ctivity index (EAI) > 4 [14]. Additionl inclusion criteri were s follows: body weight 40 kg, use of 400 mg of prednisone (or equivlent) within 4 wk before study strt nd t lest one unsuccessful ttempt to tper corticosteroids, ffected colon length 25 cm, negtive stool culture nd no cytomeglovirus infection t screening s ssessed by immunohistochemistry of colonic tissue smples. Exclusion criteri included severe disese ctivity (CAI > 12), minoslicyltes strted or incresed in dosge within the prior 4 wk, or immune modultors strted within 2 mo prior the study entry; incresed steroid dose surpssing the bseline dose during the study period; severe locl or systemic infection; virl infection within 4 wk of study entry; hypotension (systolic blood pressure < 80 mm Hg nd/or distolic blood pressure < 50 mm Hg) or hypertension (systolic blood pressure > 180 mm Hg nd/or distolic blood pressure > 120 mm Hg); serious renl, heptic or crdiovsculr disese; significnt lbortory bnormlities such s bsolute neutrophil count < /L, pltelet count < /L, hemoglobin < 8 g/l, AST or ALT > 3 times upper norml rnge, bilirubin > 2.5 upper norml rnge, serum cretinine > 1.8 mg/dl, prtil thromboplstin time > 20% upper norml rnge, prothombrin time < 50%; pregnncy; brestfeeding; or known llergy to heprin. Methods Ptients were rndomly ssigned to receive 5 (group 1) or 10 (group 2) GCAP sessions over 5 or 10 consecutive weeks, respectively, in n out-ptient setting (Figure 1). Apheresis sessions lsted for 60 min t flow rte of 30 ml/h. The pheresis system used consisted of pump with n integrted monitor (Admonitor, Otsuk Electronics, Jpn) nd single use polycrbonte column (Adcolumn, JIMRO, Jpn) with cpcity of 335 ml filled with bout pieces of cellulose cette beds of 2 mm in dimeter bthed in physiologicl sline nd stem sterilized (JIMRO, Jpn). During the sessions, sodium heprin ws continuously infused t rte of 25 UI/min. All dverse events during the study period were registered. Clinicl nd endoscopic ssessment ws performed ccording to the Rchmilewitz Index (CAI nd EAI) (14). CAI ws mesured t bseline, nd therefter on weekly bsis until wk 17 (primry endpoint). Endoscopic ssessment of disese severity ws performed t screening nd t wk 17. IBDQ ws used to ssess qulity of life. The primry endpoint ws clinicl remission t wk 17 defined by CAI 4. Secondry endpoints included chnges in qulity of life (IBDQ), endoscopic remission, nd steroid consumption. Endoscopic remission ws defined s n EAI 4. Steroid dose could be tpered t the investigtor's discretion. In the cse of worsening disese ctivity, steroid dose could be incresed without surpssing the bseline dose. Anlysis of the results were performed on n intention to tret (ITT) bsis. All ptients who completed t lest one pheresis session were considered in the nlysis. Results re presented s men ± SD or medin vlues. For quntittive prmeters sttisticl significnce in comprison to bseline within groups ws clculted using the Wilcoxon Signed Rnk Test. Differences in ctegoricl vribles were ssessed using Fisher s exct test. The Mnn-Whitney U-test ws used for comprison of results between groups. Sttisticl nlysis ws done by Systt 1.1. RESULTS Group 1:5 GCAP n = 9 for symptomtic hypotension n = 8 Completed 5 GCAP t wk 7 for protocol violtion 1 nd 2 ptients withdrwn t wk 7 nd 10 for disese ctivity n = 20 fter 8 GCAP disese ctivity wk 17 n = 5 Completed follow-up Group 2:10 GCAP n = 11 t wk 13 for protocol violtion 1 Figure 1 Study Design. 1 Steroid dose incresed over the initil dose. n = 10 Completed 10 GCAP wk 17 n = 9 Completed follow-up A totl of 20 ptients were included in the study. Nine ptients were rndomized to group 1 nd 11 ptients to group 2. One ptient in group 1 ws excluded from the study becuse of symptomtic hypotension t the time of
3 Ricrt E et l. Grnulocytepheresis in ulcertive colitis 2195 Tble 1 Demogrphics nd bseline chrcteristics Group 1 (n = 9) Group 2 (n = 11) Group 1 Group 2 Age (yr) 38.1 ± ± 16.6 Gender (mle/femle) 6/3 6/5 Smoking hbit (smoker/nonsmoker/former-smoker) 0/7/2 0/4/7 Steroid dose t study 43 ± ± entrnce (mg/d) Previous medictions 5-ASA 9 11 Azthioprine 5 6 Methotrexte 0 1 Cyclosporin A 1 3 Disese durtion (mo) 36 ± ± 42.8 Nº of previous flres in the 2.33 ± ± 1.09 lst 12 mo Nº of previous dmissions to 1.33 ± ± 1.25 hospitl Site of disese Proctosigmoiditis 1 4 Left sided colitis 4 4 Extensive colitis 2 1 Pncolitis 2 2 CAI 8.0 ± ± 1.2 EAI 8.7 ± ± 2.2 IBDQ 106 (230-70) 147 ( ) CRP (mg/l) 8 ( ) 4.6 ( ) All dt expressed s men ± SD or medin (mx-min). CAI: clinicl ctivity index; EAI: endoscopic ctivity index; CRP: C rective protein. venopuncture before inititing the first pheresis tretment. Demogrphics nd bseline disese chrcteristics re shown in Tble 1. Disese durtion ws longer in group 2 compred to group 1 (78 ± 42.8 mo nd 36 ± 32.3 mo, respectively) but the difference ws not sttisticlly significnt (P = 0.4). All other prmeters were similr between the two groups. The men number of relpses during the yer prior to study entry ws 2.33 ± 0.71 nd 2.22 ± 1.09 for groups 1 nd 2, respectively. Fifty-five per cent of ptients in group 1 nd 64% of ptients in group 2 were previously treted with immune modultors (zthioprine, methotrexte). One ptient in group 1 nd 3 ptients in group 2 hd required cyclosporine for previous steroid refrctory flres. All ptients in both groups were ctive in spite of receiving high steroid dose (43 ± nd 35 ± 14.9 mg/d of prednisone for group 1 nd 2, respectively). At wk 17, 3 of 8 ptients (37.5%) in group 1 nd 5 of 11 ptients (45.45%) in group 2 were in clinicl remission. CAI decresed from 8 ± 1 t bseline to 5.4 ± 3.0 t wk 17 in group 1, nd from 7.9 ± 1.2 t bseline to 5.3 ± 5.0 t wk 17 in group 2; the reduction in CAI score ws of similr mgnitude in both groups (P: NS) (Figure 2). All ptients who entered into clinicl remission in both groups were lso in endoscopic remission. Medin C rective protein (CRP) vlues showed trend to reduction in group 2 [medin 4.6 mg/l ( ) t wk 1 nd 2.6 mg/l ( ) t wk 17] but not in group 1 [medin 8.0 mg/l ( ) t wk 1 nd 10.4 mg/l ( ) t wk 17]. The steroid dose ws reduced in both groups. When compred with bseline, the dose of steroid ws significntly reduced (P < 0.05) since wk 4 in group 2 nd since wk 5 nd in group 1. Intergroup comprison showed tht dily steroid CAI requirements were significntly lower in group 2 during the period comprised between wk 9 nd 13 but not t wk 17 (P = 0.066) (Figure 3). All but one of the ptients who hd clinicl remission were free of steroids t wk 17. There ws n improvement in IBDQ scores between wk 0 nd wk 17 in both groups, but the differences were not sttisticlly significnt[medin 106 (230-70) t wk 0 nd 110 ( ) t wk 17 in group 1; medin 147 ( ) t wk 0 nd 178 ( ) t wk 17 in group 2]. Grnulocytepheresis with Adcolumn ws very well tolerted nd no mjor side effects were observed during the study. A totl of 11 non-serious dverse events nd one serious dverse event were reported in both groups. The serious dverse event ws community cquired pneumoni tht ws judged s not relted to the study therpy nd resolved with n orl ntibiotic. Seven ptients entered into the one yer long-term follow-up. Six out of these 7 ptients were in clinicl remission nd remined steroid free without ny chnges in UC therpy during this period. DISCUSSION t /wk Figure 2 Evolution of CAI in group 1 (5 GCAP) nd in group 2 (10 GCAP). A growing body of evidence suggests tht GCAP cn be therpeutic lterntive for UC. Most of the published studies re non-controlled, include heterogeneous UC popultion, nd use different GCAP regimens. The only shm-controlled study published so fr, included UC popultion of similr clinicl chrcteristics to the one selected for the current study, nd demonstrted significntly higher response rtes in ptients receiving ctive tretment [15]. In tht study, 7 sessions of shm or ctive pheresis were performed. In nother recent study, Hni et l [9] reported tht 10 GCAP regimen ws ssocited with higher remission rtes in steroid dependent UC ptients compred to 5 GCAP, but in this study the number of pheresis sessions ws bsed on clinicl judgment of the ttending physicin. No forml comprison of vrious tretment strtegies using pheresis hs been mde so fr in order to delinete n optiml tretment scheme. Our group decided to conduct smll pilot rndomized controlled tril to determine if there is therpeutic gin by performing 10 s opposed to 5 pheresis sessions for induction of remission in ptients with steroid-dependent ctive UC. Ptients
4 2196 ISSN CN /R World J Gstroenterol April 21, 2007 Volume 13 Number P < 0.05 Group 1 Group 2 Figure 3 Steroid consumption in group 1 (5 GCAP) nd in group 2 (10 GCAP). mg/d t /wk recruited in this study represent UC popultion tht is difficult to tret, 60% were under immune modultor tretment with zthioprine or methotrexte, nd 20% hd been previously treted with cyclosporine for steroid refrctory UC. None of the ptients included hd been previously treted with infliximb becuse infliximb ws not uthorized for UC tretment t the time the study ws performed. Our results show tht GCAP induced clinicl nd endoscopic remission in n importnt proportion of the ptients. At wk 17, ll but one of the responding ptients were free of steroid tretment. Furthermore, ll responding ptients but one completed one yer long-term follow up without requiring steroids or the introduction of ny other therpy. These results re in keeping with the findings reported by Domenech et l [8] nd support the steroid spring effect of GCAP in steroid dependent UC ptients. Interestingly, steroid consumption in our study ws lower in group 2, showing sttisticlly significnt difference in period strting when group 1 ptients were no longer receiving pheresis tretment, nd group 2 ws still under ctive pheresis tretment. Although the study filed to show ny difference in terms of clinicl remission between 5 nd 10 GCAP tretments, the forementioned differences in steroid requirement support the notion tht GCAP is effective for the tretment of UC. Comprison of the efficcy of diverse tretment modlities cross vrious studies is subject to numerous pitflls, but quite often it is the only indirect informtion on the reltive efficcy of vrious therpeutic options, since hed to hed comprisons re disppointingly scrce. The popultion included in the current study consisted of ptients with steroid-dependent course nd ctive disese in spite of use of steroids for two weeks, which represents popultion prticulrly difficult to tret. The overll 42% clinicl nd endoscopic remission rtes obtined in the present study compre fvorbly with those of recent studies using infliximb [3,16]. Although the study hs importnt limittions due to smple size, it is necessry to point out tht to our knowledge, this is the first rndomized comprison of two different GCAP regimens in strictly defined UC popultion. Even though the results show trend towrds lower steroid requirements in group 2 (10 GCAP), in our opinion these dt do not support the recommendtion of this regimen over 5 GCAP lterntive. Our study did not ddress the issue of intensifiction of GCAP (2-3 GCAP per week). A rndomized smll study in ptients with ctive UC showed tht n intensified pheresis regimen hd more rpid but not superior therpeutic effects thn one GCAP per week schedule, s ws performed in our study [17]. In conclusion, GCAP seems to be n effective, sfe, nd well tolerted therpy tht llows steroid withdrwl in steroid dependent modertely ctive UC ptients. However, 10 weekly GCAP tretments do not provide n dvntge in this ptient popultion s compred to 5 tretments in terms of clinicl or endoscopic remission but fford significnt steroid-spring effect. This informtion my be of significnt vlue both in clinicl prctice nd in the design of new clinicl trils using this tretment modlity. REFERENCES 1 Fubion WA Jr, Loftus EV Jr, Hrmsen WS, Zinsmeister AR, Sndborn WJ. The nturl history of corticosteroid therpy for inflmmtory bowel disese: popultion-bsed study. Gstroenterology 2001; 121: Frser AG, Orchrd TR, Jewell DP. The efficcy of zthioprine for the tretment of inflmmtory bowel disese: 30 yer review. Gut 2002; 50: Rutgeerts P, Sndborn WJ, Fegn BG, Reinisch W, Olson A, Johnns J, Trvers S, Rchmilewitz D, Hnuer SB, Lichtenstein GR, de Villiers WJ, Present D, Snds BE, Colombel JF. Infliximb for induction nd mintennce therpy for ulcertive colitis. N Engl J Med 2005; 353: Lugering N, Kuchrzik T, Stoll R, Domschke W. Current concept of the role of monocytes/mcrophges in inflmmtory bowel disese-blnce of proinflmmtory nd immunosuppressive meditors. Itl J Gstroenterol Heptol 1998; 30: Swd K, Muto T, Shimoym T, Stomi M, Swd T, Ngw H, Hiwtshi N, Askur H, Hibi T. Multicenter rndomized controlled tril for the tretment of ulcertive colitis with leukocytpheresis column. Curr Phrm Des 2003; 9: Hni H, Wtnbe F, Ymd M, Sto Y, Tkeuchi K, Iid T, Tozw K, Tnk T, Mruym Y, Mtsushit I, Iwok Y, Kikuch K, Snibdi AR. Adsorptive grnulocyte nd monocyte pheresis versus prednisolone in ptients with corticosteroid-dependent modertely severe ulcertive colitis. Digestion 2004; 70: Swd K, Hiwtshi N, Munkt A. A multicentre rndomized controlled study of sfety nd efficcy of dsorptive grnulocyte nd monocyte pheresis in ptients with ctive ulcertive colitis. Gstroenterology 2004; 126: A462 8 Domenech E, Hinojos J, Esteve-Coms M, Gomollon F, Herrer JM, Bstid G, Obrdor A, Ruiz R, Sro C, Gssull MA. Grnulocytepheresis in steroid-dependent inflmmtory bowel disese: prospective, open, pilot study.
5 Ricrt E et l. Grnulocytepheresis in ulcertive colitis 2197 Aliment Phrmcol Ther 2004; 20: Hni H, Wtnbe F, Tkeuchi K, Iid T, Ymd M, Iwok Y, Snibdi A, Mtsushit I, Sto Y, Tozw K, Ari H, Furut T, Sugimoto K, Bjrnson I. Leukocyte dsorptive pheresis for the tretment of ctive ulcertive colitis: prospective, uncontrolled, pilot study. Clin Gstroenterol Heptol 2003; 1: Ngnum M, Funkoshi S, Skurb A, Tkgi H, Inoue N, Ogt H, Iwo Y, Ishi H, Hibi T. Grnulocytpheresis is useful s n lterntive therpy in ptients with steroid-refrctory or -dependent ulcertive colitis. Inflmm Bowel Dis 2004; 10: Kruis W, Mongersten J, Dignss A. Leucocytpheresis in steroid refrctory ulcertive colitis: results of multicenter pilot study. Gut 2004; 53 (Suppl VI): A Suzuki Y, Yoshimur N, Snibdi AR, Sito Y. Selective grnulocyte nd monocyte dsorptive pheresis s first-line tretment for steroid nive ptients with ctive ulcertive colitis: prospective uncontrolled study. Dig Dis Sci 2004; 49: Ymmoto T, Umege S, Kitgw T, Ysud Y, Ymd Y, Tkhshi D, Mukumoto M, Nishimur N, Ysue K, Mtsumoto K. Grnulocyte nd monocyte dsorptive pheresis in the tretment of ctive distl ulcertive colitis: prospective, pilot study. Aliment Phrmcol Ther 2004; 20: Rchmilewitz D. Coted meslzine (5-minoslicylic cid) versus sulphslzine in the tretment of ctive ulcertive colitis: rndomised tril. BMJ 1989; 298: Swd K, Kusugmi K, Suzuki Y, Bmb T, Munkt A, Hibi T, Shimoym T. Leukocytpheresis in ulcertive colitis: results of multicenter double-blind prospective csecontrol study with shm pheresis s plcebo tretment. Am J Gstroenterol 2005; 100: Jrnerot G, Hertervig E, Friis-Liby I, Blomquist L, Krlen P, Grnno C, Vilien M, Strom M, Dnielsson A, Verbn H, Hellstrom PM, Mgnuson A, Curmn B. Infliximb s rescue therpy in severe to modertely severe ulcertive colitis: rndomized, plcebo-controlled study. Gstroenterology 2005; 128: Skurb A, Ngnum M, Hibi T. Intensive therpy of grnulocyte nd dsorption pheresis induces rpid remission in ptients with ulcertive colitis. Gstroenterology 2003; 124 Suppl 1: A522 S- Editor Liu Y L- Editor Lutze M E- Editor Chen GJ
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