Until recently, treatment of active ulcerative colitis
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1 ORIGINAL ARTICLE Prognostic Significance of Endoscopic Remission in Patients with Active Ulcerative Colitis Treated with Oral and Topical Mesalazine: A Prospective, Multicenter Study Gianmichele Meucci, MD,** Renato Fasoli, MD, Simone Saibeni, MD, Daniela Valpiani, MD, Renzo Gullotta, MD, k Enrico Colombo, MD, Renata D Inca', MD,** Maddalena Terpin, MD, and Giovanni Lombardi, MD on Behalf of the IG-IBD Background: It has been recommended that the treatment of active ulcerative colitis (UC) should be continued until complete healing of endoscopic lesions. However, the evidence supporting this recommendation is scanty. Aims of the present study were to assess the rate of patients with active UC who achieve clinical but not endoscopic remission after treatment with oral plus topical mesalazine and to compare the rate of relapse in patients with clinical/endoscopic remission and those with only clinical remission. Methods: Patients with active mild or moderate UC were eligible. All patients received mesalazine, 4 g/day orally and 2 g/day per rectum for 6 weeks. Those achieving clinical remission underwent colonoscopy: afterwards, all received maintenance treatment with oral mesalazine, 2 g/day orally for 1 year. Clinical remission was defined as normal frequency of bowel movements with formed stools, no abdominal pain, and no blood in the stools. Endoscopic remission was defined as normal-appearing mucosa or only mild redness and/or friability, without either ulcers or erosions. Results: In all, 81 patients were enrolled. Sixty-one (75%) achieved clinical remission. Endoscopic activity was still present in five (8%). The cumulative rate of relapse at 1 year was 23% in patients with clinical and endoscopic remission and 80% in patients with only clinical remission (P < ). Conclusions: Persistence of endoscopic activity is quite infrequent in patients with active UC achieving clinical remission after a 6-week treatment with oral plus topical mesalazine, but is a very strong predictor of early relapse. (Inflamm Bowel Dis 2012;18: ) Key Words: ulcerative colitis, mesalazine, endoscopic remission, mucosal healing Received for publication June 2, 2011; Accepted July 5, From the *Divisione di Gastroenterologia, Ospedale Valduce, Como, Italy, Servizio di Gastroenterologia ed Endoscopia Digestiva Unità Complessa di Medicina, Ospedale Costantino Cantù, Abbiategrasso, Italy, Cattedra di Gastroenterologia, Università degli Studi e IRCCS Policlinico, Milano, Italy, Centro di Gastroenterologia ed Endoscopia Digestiva, Ospedale Morgagni Pierantoni, Forlì, Italy, k Unità di Gastroenterologia ed Endoscopia Digestiva, Clinica San Carlo, Paderno Dugnano, Italy, Unità Operativa di Medicina Generale ad Indirizzo Gastroenterologico, Azienda Ospedaliera G. Salvini, Garbagnate Milanese, Italy, ** Dipartimento di Scienze Chirurgiche e Gastroenterologiche, Università di Padova, Padova, Italy, UOC Gastroenterologia ed Endoscopia Digestiva, Azienda Ospedaliera Ospedale Civile di Legnano, Legnano, Italy, UOC Gastroenterologia ed Endoscopia Digestiva, Ospedale Casa Sollievo della Sofferenza IRCCS, San Giovanni Rotondo, Italy. Reprints and current address: Gianmichele Meucci, Division of Gastroenterology, Ospedale San Giuseppe, Via San Vittore 12, Milano, Italy ( g.meucci@teletu.it). Copyright VC 2011 Crohn s & Colitis Foundation of America, Inc. DOI /ibd Published online 9 August 2011 in Wiley Online Library (wileyonlinelibrary. com). Until recently, treatment of active ulcerative colitis (UC) has focused on improving symptoms and endoscopic demonstration of mucosal healing has not been considered a necessary endpoint in patients achieving clinical remission. 1,2 However, recent data suggest that concentrating exclusively on clinical outcome measures may not be adequate to achieve long-term treatment success. Indeed, achievement of endoscopic remission has been shown to correlate with a reduced risk of colectomy, 3,4 hospital admissions, and need for immunosuppressive treatments. 4 Recently, a panel of experts recommended that the primary endpoint for therapeutic trials in patients with mildly to moderately active UC should be induction of remission, defined as complete symptom resolution and endoscopic healing. 5 Moreover, some experts at present recommend that the treatment of active UC should be continued until complete healing of endoscopic lesions is observed, 6 although no consensus exists on this topic. 2,7 In fact, the evidence supporting practical value associated with repeat endoscopy to monitor treatment progression is limited, and no consensus exists on how endoscopic remission should be assessed. 7 Mesalazine is currently the mainstay of treatment for patients with mild or moderate UC flares, 2 and combined treatment with oral and topical formulations appears to be 1006
2 Endoscopic Remission in UC FIGURE 1. Study design. associated with maximum clinical improvement and an earlier clinical response compared with treatment with either formulation alone Conversely, data on the rate of endoscopic remission in patients treated with this regimen are at present scanty The aims of the present study were: 1) to assess the rate of patients with active UC who achieve clinical but not endoscopic remission following treatment with oral plus topical mesalazine, and 2) to compare relapse rates in patients achieving both clinical and endoscopic remission versus those with clinical remission only. PATIENTS AND METHODS Inclusion Criteria Eligible patients were those with active mild or moderate UC extending beyond the rectosigmoid junction. Patients requiring systemic steroids, those with previous or ongoing immunosuppressive treatment, and those with proctitis were excluded. Study Design This was a prospective, multicenter study. Study design is shown in Figure 1. All patients underwent baseline colonoscopy, followed by 6-week treatment with mesalazine, 4 g/day orally and 2 g/day rectally. Patients achieving clinical remission underwent a second colonoscopy; following this, and regardless of endoscopic remission status, all of them received maintenance treatment with oral mesalazine, 2 g/day for 12 months. Patients who did not achieve clinical remission were assessed as treatment failures, were no longer eligible for inclusion in study, and were treated as appropriate. Patients achieving clinical remission were followed for 1 year by means of monthly telephone interviews and clinical visits every 3 months. Definitions Disease activity was evaluated by means of the Mayo Index 11 (Table 1). Clinical remission was defined as normal frequency of bowel movements with formed stools, no abdominal pain, and no blood in the stools, i.e., a value of 0 on the 6-point Mayo subscore. 12 Clinical relapse (both at baseline and in patients attaining clinical remission) was defined as a worsening of bowel function plus reappearance of rectal bleeding. For assessment of endoscopic activity, the Mayo endoscopic subscore was used. Before starting the study a formal assessment of interobserver concordance among all participant endoscopists was carried out. This assessment revealed an excellent degree of concordance in separating grades 0 1 from grades 2 3 ((kappa 0.71) but a poor one in defining the single four grades, as well in distinguishing grade 0 from grade 1 (kappa values between 0,31 and 0,57) (Meucci et al, unpubl. obs.). Therefore, we decided to define endoscopic remission as a Mayo endoscopic subscore 1, i.e., normal-appearing mucosa or only mild redness and/or friability, without either ulcers or erosions. A subanalysis in which only patients with normal mucosa were considered in endoscopic remission was also planned. Statistical Methods For statistical analysis, data were input into a statistical software (Intercooled Stata, College Station, TX). The rate of clinical relapse was calculated by means of the Kaplan Meier method. For comparison of the rate of relapse in patients with and without endoscopic remission the log-rank test was used. For the assessment of factors associated with the rate of clinical remission, endoscopic remission, and clinical relapse, multivariate analyses were performed using a logistic step-wise regression model or Cox regression model, as appropriate. In logistic analysis, all parameters showing a P-value lower than TABLE 1. Components of the Mayo Score Stool frequency 0 Normal stools/day more than normal stools/day more than normal 3 4 stools/day more than normal Rectal bleeding 0 None 1 Visible blood with stool less than half the time 2 Visible blood with stool half of the time or more 3 Passing blood alone Mucosal appearance at endoscopy 0 Normal or inactive disease 1 Mild disease (erythema, decreased vascular pattern, mild friability 2 Moderate disease (marked erythema, absent vascular pattern, friability, erosions) 3 Severe disease (spontaneous bleeding, ulceration) Physician rating of disease activity 0 Normal 1 Mild 2 Moderate 3 Severe 1007
3 Meucci et al TABLE 2. Patient Baseline Data Patients 81 Males 49 (60.5%) Mean age 48.6 years (19 79) First diagnosis 41 (50.6%) Disease extension - proctosigmoiditis 39 (48.1%) - left-sided colitis 24 (29.6%) - extensive colitis 18 (22.2%) 6-point Mayo clinical subscore (33.3%) (29.6%) (32.1%) (5.0%) Mayo endoscopic subscore (14.8%) (64.2%) (21.0%) 0.1 at univariate analysis were included and those showing a P-value higher than 0.3 removed, according to an automated backward stepwise procedure. For all tests, P < 0.05 was considered statistically significant. RESULTS In all, 81 patients were enrolled from nine participating institutions; patient baseline data are shown in Table 2. As shown in Figure 2, 74 patients had evaluable data at 6 weeks. Three patients were switched to more aggressive treatments because of worsening of symptoms, one patient was found not to be affected by UC, and the three remaining patients were lost to follow-up. Following 6 weeks of oral and topical mesalazine treatment, 61 patients achieved clinical remission (75.3% intention to treat, 78.2% per protocol). At multivariate logistic regression analysis no correlation was found between the rate of clinical remission and clinical or demographic variables such as gender, age, disease extension and duration, the degree of baseline endoscopic activity, FIGURE 3. Cumulative risk of clinical relapse according to endoscopic activity. duration of previous remission, number of relapses in the last year, smoking habits, and previous appendectomy. Among 61 patients achieving clinical remission, endoscopic examination showed endoscopic remission (as defined above) in 56 and persistence of endoscopic activity in only five (8.2%). Again, no correlation was found at logistic regressions analysis between the rate of endoscopic remission and clinical or demographic variables such as gender, age, disease extension and duration, the degree of baseline endoscopic activity, duration of previous remission, number of relapses in the last year, smoking habits, and previous appendectomy. However, all five patients not achieving endoscopic remission were affected with leftsided colitis, as compared with 42 out 56 of those achieving endoscopic remission (P ¼ 0.58 at two-sided chi-square test). Among 13 patients not achieving clinical remission, eight underwent repeat colonoscopy as part of their subsequent clinical work-up: in all, persistence of endoscopic UC activity was confirmed. As shown in Figure 3, the cumulative rate of clinical relapse at 1 year was 23% in patients with clinical and endoscopic remission and 80% in patients with only clinical remission (P < ). Among 56 patients achieving endoscopic remission as defined above, the endoscopic picture was graded as grade 0 (normal-appearing mucosa) in 28 and as grade 1 (mild redness and/or friability, without either ulcers or erosions) in the remaining 28. The cumulative risk of relapse at 1 year in these two groups were 26% and 19%, respectively, a nonsignificant difference (P ¼ 0.47). At Cox regression analysis, the only variable associated with a lower risk of relapse was achievement of endoscopic remission (P ¼ 0.001). FIGURE 2. Enrollment and outcomes. DISCUSSION Our data confirm that combination oral and topical mesalazine is highly effective in patients with mildly to moderately active UC. Indeed, the rate of patients 1008
4 Endoscopic Remission in UC achieving clinical remission was 75% in our study, a figure that is very close to that reported in two previous therapeutic trials, 9,10 and slightly lower than reported in a trial including only patients with left-sided colitis. 8 In all the above-mentioned trials the oral dosage of mesalazine ranged from 2 4 g/day and treatment duration from 6 8 weeks, thus not differing substantially from dosages and duration in the present study. Moreover, persistence of endoscopic inflammation appears to be quite infrequent in patients with active UC achieving clinical remission following a 6-week treatment with oral and topical mesalazine. Indeed, among 61 patients achieving clinical remission only five (8%) showed persistence of endoscopic disease activity despite complete resolution of symptoms. In 2007, Kornbluth et al 13 observed persistence of endoscopic inflammation in as many as 42% of patients achieving clinical remission after treatment with oral mesalazine. However, a different definition of endoscopic remission (sigmoidoscopic score of 0, i.e., completely normal mucosa) was used in that study. In the present study we decided to use a looser definition (endoscopic score <2) on the basis of the results of our preliminary assessment of interobserver concordance among participant endoscopists, which revealed a very poor degree of concordance in differentiating grade 0 from grade 1. We believe that our definition of endoscopic remission was more appropriate for the reasons outlined below. At any rate, very few discrepancies between the rates of clinical and endoscopic remission have been reported in most trials evaluating the efficacy of mesalazine (either orally, topically, or in combination) in patients with ulcerative colitis. 10,14 16 These findings are in keeping with previous observations showing that, in most patients with UC, endoscopic and clinical activity coincide and endoscopic assessment adds little to clinical indices of disease activity. 12,17 On the other hand, significant discrepancies between the rates of clinical and endoscopic remission have been reported in UC patients treated with other therapeutic regimens, such as oral corticosteroids 4,18 20 or leukocytapheresis. 21 However, persistence of endoscopic activity in the context of clinical remission was found to be a strong predictor of early UC relapse. In fact, four out of five patients not achieving endoscopic remission relapsed within 3 months, whereas as many as 77% of those achieving endoscopic remission maintained stable remission for as long as 1 year after completing the acute phase treatment. This is in accordance with the previous finding that even persistence of inflammation only at the histological level is a strong predictor of relapse as well In previous studies the frequency of previous relapses and young age was found to be associated with a higher risk of relapse 22,25,26 but these associations could not be confirmed in the present study. It must also be noted that in half of our patients achieving endoscopic remission as above defined the endoscopic picture was classified as grade 1; nevertheless, the rate of clinical relapse in this subset of patients was even slightly (albeit largely not significantly) lower than in patients with an endoscopic score of 0. Therefore, we believe that it is appropriate (at least for prognostic purposes) to consider in endoscopic remission not only patients showing a completely normal mucosa, but also those in whom only mild redness and/or friability, but not erosions or ulcers, are detectable. Some limitations of the present study need to be addressed. First, no formal assessment of patients adherence to treatment was made. In fact, while very high degrees of adherence to oral mesalazine have been reported in clinical trials, real-world adherence has been found to be quite low Since the present was a prospective, pragmatic study, a high degree of nonadherence can therefore be supposed. However, there is no plausible reason to suppose a lower adherence to treatment among patients not achieving endoscopic remission when compared with patients achieving it. Therefore, we believe that this limitation does not affect the main results of the study. Second, it has been recently proposed to differentiate patients showing only erythema from those with friability and to exclude friability from the definition of endoscopic score In the present study, no attempt was made to operate such a distinction. Whether a difference in relapse rate exists between patients with only erythema and those with friability should be a topic for subsequent research. In conclusion, our data suggest that the majority of patients with active UC achieve both clinical and endoscopic remission (or only persistence of minimal signs of inflammation) after combination treatment with oral and topical mesalazine. Therefore, systematic endoscopic assessment in this subset of patients could not be required. However, a minority of patients exist in whom marked endoscopic signs of inflammation persist despite complete symptoms disappearance, and in these patients early relapse is extremely frequent. Further research is needed to determine if other risk markers can be used to identify patients who would be good candidates for joint clinical and endoscopic assessment. REFERENCES 1. Lichtenstein GR, Rutgeerts P. Importance of mucosal healing in ulcerative colitis. Inflamm Bowel Dis. 2010;16: Kornbluth A, Sachar DB. Practice Parameters Committee of the American College of Gastroenterology. Ulcerative colitis practice guidelines in adults. Am J Gastroenterol. 2010;105: Frøslie KF, Jahnsen J, Moum BA, et al. Mucosal healing in inflammatory bowel disease: results from a Norwegian population-based cohort. Gastroenterology. 2007;133: Ardizzone S, Cassinotti A, Duca P, et al. Mucosal healing predicts late outcomes after the first course of corticosteroids for newly diagnosed ulcerative colitis. Clin Gastroenterol Hepatol. 2011;9:
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