High Rates of Viral Suppression After Long-term Entecavir Treatment of Asian Patients With Hepatitis B e Antigen Positive Chronic Hepatitis B
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1 CLINICAL GASTROENTEROLOGY AND HEPATOLOGY 2012;10: BRIEF COMMUNICATIONS High Rates of Viral Suppression After Long-term Entecavir Treatment of Asian Patients With Hepatitis B e Antigen Positive Chronic Hepatitis B CALVIN Q. PAN,* MYRON TONG, KRIS V. KOWDLEY, KE QIN HU, TING TSUNG CHANG, CHING LUNG LAI, # SEUNG KEW YOON,** SAMUEL S. LEE, DAVID COHEN, HONG TANG, and NAOKY TSAI *Division of Liver Diseases, Mount Sinai School of Medicine, New York, New York; Pfleger Liver Institute, University of California School of Medicine, Los Angeles, California; Center for Liver Disease, Digestive Disease Institute, Virginia Mason Medical Center, Seattle, Washington; Division of Gastroenterology, University of California, Irvine Medical Center, Orange, California; Medical College, National Cheng Kung University, Tainan, Taiwan, Republic of China; # Queen Mary Hospital, Hong Kong, China; **Kangnam St. Mary Hospital, The Catholic University of Korea, Seoul, South Korea; Liver Unit, University of Calgary, Calgary, Canada; Research & Development, Bristol-Myers Squibb Company, Wallingford, Connecticut; Research & Development, Bristol-Myers Squibb Company, Plainsboro, New Jersey; and University of Hawaii, Honolulu, Hawaii See related article, Lok AS et al, on page 619 in Gastroenterology. There are limited data on the effects of long-term entecavir therapy in Asian patients with chronic hepatitis B (CHB). We performed a post hoc analysis of 94 Asian hepatitis B e antigen positive (HBeAg ), nucleos(t)ide analogue-naive patients who received 5 years of therapy with entecavir (up to 2 years in study ETV-022 and the remainder in study ETV-901). Among patients completing week 240, 95% (63 of 66) had levels of hepatitis B virus DNA <300 copies/ml, and 76% (50 of 66) had normalized levels of alanine aminotransferase. In addition to patients who achieved a serologic response during ETV-022, a further 40% (26 of 65) achieved HBeAg loss, and 18% (12 of 65) underwent HBeAg seroconversion through year 5 of entecavir therapy. No resistance to entecavir was detected, and the safety profile was consistent with previous reports. The long-term efficacy and safety of entecavir are therefore comparable between Asians and the overall population of HBeAg patients with CHB. Keywords: Hepatitis B Virus; Antiviral Therapy; Nucleos(t)ide Analogue. Asian patients with chronic hepatitis B (CHB) have a higher risk of cirrhosis and hepatocellular carcinoma (HCC) and might show a different response to anti hepatitis B virus (HBV) treatment than white patients. 1 3 Entecavir has demonstrated superior virologic, biochemical, and histologic activity in clinical studies in treatment-naive hepatitis B e antigen (HBeAg) and HBeAg patients 4 8 and in patients with hepatic decompensation. 9 In long-term studies in HBeAg and HBeAg patients, entecavir was well-tolerated and provided potent virologic suppression with minimal resistance and substantial histologic improvement and regression of fibrosis This analysis evaluated the efficacy and safety of entecavir in Asian HBeAg CHB patients through 5 years. Methods Study Design and Patients This study was a post hoc subgroup analysis of Asian patients included in the overall long-term entecavir cohort, consisting of nucleos(t)ide-naive HBeAg patients treated in the phase 3 study ETV-022 (NCT ) and the rollover extension study ETV-901 (NCT ). The study design and patient selection criteria for ETV-022 and ETV-901 have been published previously. 5,12 Briefly, patients who had not achieved a complete response (HBV DNA 0.7 meq/ml and HBeAg loss) in ETV-022 or responders in ETV-022 who had relapsed during off-treatment follow-up were eligible to enroll in ETV-901. Patients included in the current analysis (hereafter called the entecavir long-term Asian cohort) received entecavir for up to 240 weeks, consisting of up to 96 weeks during ETV-022 (0.5 mg daily) and the remainder during ETV-901 (1.0 mg daily), with a 35-day treatment gap between the last dose in ETV-022 and the first dose in ETV-901. The studies were conducted in adherence to the ethical principles of the Declaration of Helsinki and the regulatory requirements of all participating countries. Written informed consent was obtained from all study participants. Efficacy and Resistance Analyses Time on treatment was defined from the first date of dosing in ETV-022 to the last date of dosing in ETV-901. Patients with week 240 evaluable samples were assessed at baseline and at weeks 48, 96, 144, 192, and 240 for serum HBV DNA 300 copies/ml (50 IU/mL; Roche COBAS Amplicor polymerase chain reaction [PCR] assay; Roche Molecular Diagnostics, Pleasanton, CA), alanine aminotransferase (ALT) normalization ( 1.0 upper limit of normal [ULN]), HBeAg loss, Abbreviations used in this paper: AE, adverse event; ALT, alanine aminotransferase; CHB, chronic hepatitis B; HBeAg, hepatitis B e antigen; HBV, hepatitis B virus; HCC, hepatocellular carcinoma; PCR, polymerase chain reaction; SEM, standard error of the mean; ULN, upper limit of normal by the AGA Institute /$
2 1048 PAN ET AL CLINICAL GASTROENTEROLOGY AND HEPATOLOGY Vol. 10, No. 9 Table 1. Baseline Demographics and Characteristics of the Entecavir Long-term Asian Cohort and Overall Entecavir Long-term Cohort ETV-022/-901 long-term cohorts Asian cohort (n 94) Overall cohort (n 146) 12 Age (y), mean (SEM) 35 (1.0) 36 (1.1) Male, n (%) 76 (81) 117 (80) Ethnicity, n (%) Asian 94 (100) 94 (64) White 0 49 (34) Black/African American 0 3 (2) Mean HBV DNA by PCR, log (0.25) 9.91 (0.18) copies/ml (SEM) HBV genotype, n (%) A 6 (6) 38 (26) B 38 (40) 39 (27) C 39 (41) 44 (30) D 1 (1) 6 (4) Other/missing 6 (6) 19 (13) Mean ALT, IU/L (SEM) (8.6) (7.04) and HBeAg seroconversion. Genotypic analysis of HBV DNA polymerase 14,15 was performed for all patients with HBV DNA 300 copies/ml at weeks 48, 96, 144, 192, and 240 or at the end of dosing if treatment was discontinued before year 5. Phenotypic susceptibility to entecavir 14,15 was determined on samples from all patients with virologic breakthrough (confirmed 1 log 10 increase in HBV DNA from nadir) or harboring HBV isolates with novel emerging amino acid substitutions. Safety Analysis Cumulative safety analyses were reported for all patients who rolled over to ETV-901 and included frequencies of on-treatment adverse events (AEs), treatment discontinuations because of AEs, ALT flares (ALT 2 baseline ALT and 10 ULN), and deaths while on treatment or during off-treatment follow-up. Statistical Analysis Continuous variables were summarized by using the mean and standard error of the mean (SEM). Binary variables were summarized by counts and percentages by using the Noncompleter Missing (NC M) method of handling missing data. Results Overall, 204 of 354 HBeAg patients (58%) randomized to entecavir in study ETV-022 were Asian. Of these, 94 patients rolled over to ETV-901 with a treatment gap of 35 days and constituted the entecavir long-term Asian cohort described in this study. Sixty-six of these patients (70%) received entecavir through 5 years; 28 patients discontinued treatment because of withdrawal of consent (11), completed treatment (4), death (5), loss of follow-up (2), minimal virologic response (2), or other reasons (4). Baseline and disease characteristics of the patients included in the long-term Asian cohort were similar to those in the overall long-term cohort 12 (Table 1), except for the distribution of HBV genotyopes, which included mainly genotypes B (40%; 38 of 94) and C (41%; 39 of 94). Among all Asian patients in study ETV-022, 69% (140 of 204) achieved HBV DNA 300 copies/ml at the end of year 1. Of those included in the long-term Asian cohort, 59% (55 of 94) had HBV DNA 300 copies/ml at the end of year 1; continued entecavir treatment through year 5 resulted in an increasing proportion of patients with undetectable serum HBV DNA, reaching 95% (63 of 66) at week 240 (Table 2, Supplementary Figure 1). The mean serum HBV DNA level fell early during therapy and continued to decrease during the 5-year treatment period, resulting in a mean reduction from baseline of 7.47 log 10 copies/ml at week 240 (Supplementary Figure 2). No genotypic evidence of HBV mutants associated with entecavir resistance was detected in any of the patients during the 240 weeks of monitoring. Of the 28 patients who discontinued treatment before year 5, fourteen had HBV DNA 300 copies/ml at their last visit; among those with detectable viral load, no cases of entecavir resistance were observed. As with the virologic response, biochemical and serologic response rates increased during the 5-year treatment period (Table 2). At week 240, 76% of the patients (50 of 66) with elevated baseline ALT had ALT normalization. In addition to those patients who had achieved a serologic response with up to 2 years of entecavir treatment during ETV-022, an additional 40% (26 of 65) and 18% (12 of 65) of patients achieved HBeAg Table 2. Virologic, Biochemical, and Serologic End Points of the Entecavir Long-term Asian Cohort HBeAg ETV long-term Asian cohort ETV-901 (n 94) End point Week 48 Week 96 Week 144 Week 192 Week 240 HBV DNA 300 copies/ml, n/n (%) 55/94 a (59) 78/94 a (84) 79/88 (90) 67/72 (93) 63/66 (95) HBV DNA, log 10 copies/ml Mean Mean change from baseline ALT normalization ( 1.0 ULN), n/n (%) 59/94 (63) 70/93 (75) 65/89 (73) 65/75 (87) 50/66 (76) HBeAg loss, n/n (%) 0/94 a (0) 1/93 a (1) 20/88 (23) 27/74 (36) 26/65 (40) HBeAg seroconversion, n/n (%) 0/94 a (0) 0/93 a (0) 9/89 (10) 10/74 (14) 12/65 (18) HBsAg loss, n HBsAg, hepatitis B surface antigen. a At years 1 and 2, patients who achieved a complete response (HBV DNA 0.7 meq/ml [ copies/ml] and HBeAg loss) in study ETV-022 stopped therapy and were not included in long-term Asian cohort.
3 September 2012 LONG-TERM ENTECAVIR THERAPY IN ASIAN PATIENTS 1049 loss and HBe seroconversion, respectively, with continued treatment through week 240. On-treatment AEs were experienced by 95% of patients (89 of 94), of which 13% (12 of 94) were grade 3/4 events, and 11% (10 of 94) were serious AEs (Supplementary Table 1). The most common AEs, occurring in 10% of patients, were gastrointestinal disorders (47%), respiratory disorders (39%), cough (24%), headache (22%), influenza (20%), nasopharyngitis (18%), diarrhea (17%), and pyrexia (16%). No patient discontinued treatment because of an AE. One patient experienced an on-treatment ALT flare during year 2 associated with virologic breakthrough, but with no evidence of clinically relevant progression of hepatitis or drug resistance. There were no reports of increased blood lactate or lactic acidosis. Among the patients who discontinued before year 5, three AEs (grades 1/2) were reported in 1 patient during off-treatment follow-up, none of which were related to study medication. Five cases of benign, malignant, or unspecified neoplasms were reported as on-treatment AEs (hemangioma [2], lipoma [1], skin papilloma [1], sweat gland tumor [1]; all grade 1 or 2). Five deaths occurred on-treatment or during off-treatment follow-up, with investigator-assigned causes of liver failure (1), motorbike accident (1), car accident (2), or unknown (1). No death was attributed to entecavir therapy. The death caused by liver failure, at week 136, was secondary to progression of HCC originally diagnosed at week 51 of ETV-022. Discussion This study showed that among Asian CHB patients treated with entecavir for 5 years, 95% achieved and maintained durable HBV suppression; this is similar to the virologic response rate of 94% observed in the overall long-term entecavir cohort. 12 No evidence of HBV resistance to entecavir was detected throughout this study, suggesting that the continued viremia among the 5% of nonresponders at year 5 might have been due to nonadherence. Most patients in this cohort achieved ALT normalization, which was maintained until the end of the study. Thus, in previous partial responders in ETV- 022, continued entecavir therapy resulted in high rates of undetectable HBV DNA and ALT normalization. Long-term treatment with entecavir also resulted in an incremental proportion of patients achieving HBeAg loss and HBeAg seroconversion, in addition to those patients who had achieved a complete response with 2 years of entecavir therapy during ETV-022. As is common during long-term studies, 28 patients discontinued study medication before year 5. The potential influence that these discontinuations might have had on the efficacy analysis was not specifically assessed; however, 14 of these patients had a viral load of 300 copies/ml at last observation, and no resistance to entecavir was observed in the remaining 14 patients. During the 5-year treatment and off-treatment period, the safety profile for entecavir in Asian CHB patients was consistent with the experience from the overall population of CHB patients. 10,12 One patient experienced an ALT flare that was associated with virologic breakthrough but not with any clinical events; because no antiviral resistance was detected, it is likely that this patient was noncompliant. The current 5-year analysis confirms and extends previous reports that demonstrated high rates of virologic, biochemical, and serologic responses in patients from Japan and Hong Kong with 3 years of entecavir therapy. 16,17 Furthermore, in a related subgroup analysis in nucleos(t)ide-naive HBeAg or HBeAg Asian CHB patients treated in studies ETV-022, ETV-027, and ETV-901, 5 years of entecavir therapy led to durable viral suppression, reduced liver inflammation, and reduced reversal of fibrosis and cirrhosis, 18 similar to the histologic improvements observed with long-term entecavir in the general population of CHB patients. 11 In summary, this analysis showed that entecavir treatment for up to 5 years in Asian HBeAg CHB patients, who have predominantly HBV genotype B or C infection, was welltolerated and achieved and maintained high rates of HBV DNA suppression with no resistance development. These results are consistent with the observations reported with entecavir in the overall study population of HBeAg CHB patients. 10,12,13 Supplementary Material Note: To access the supplementary material accompanying this article, visit the online version of Clinical Gastroenterology and Hepatology at and at doi: /j.cgh References 1. Fattovich G, Bortolotti F, Donato F. Natural history of chronic hepatitis B: special emphasis on disease progression and prognostic factors. J Hepatol 2008;48: Tong MJ, Pan CQ, Hann HW, et al. The management of chronic hepatitis B in Asian Americans. Dig Dis Sci 2011;56: Janssen HL, van Zonneveld M, Senturk H, et al. Pegylated interferon alfa-2b alone or in combination with lamivudine for HBeAgpositive chronic hepatitis B: a randomised trial. Lancet 2005; 365: Woo G, Tomlinson G, Nishikawa Y, et al. Tenofovir and entecavir are the most effective antiviral agents for chronic hepatitis B: a systematic review and Bayesian meta-analyses. Gastroenterology 2010;139: Chang TT, Gish RG, de Man R, et al. A comparison of entecavir and lamivudine for HBeAg-positive chronic hepatitis B. N Engl J Med 2006;354: Gish RG, Lok AS, Chang TT, et al. Entecavir therapy for up to 96 weeks in patients with HBeAg-positive chronic hepatitis B. Gastroenterology 2007;133: Lai CL, Shouval D, Lok AS, et al. Entecavir versus lamivudine for patients with HBeAg-negative chronic hepatitis B. N Engl J Med 2006;354: Leung N, Peng CY, Hann HW, et al. Early hepatitis B virus DNA reduction in hepatitis B e antigen-positive patients with chronic hepatitis B: a randomized international study of entecavir versus adefovir. Hepatology 2009;49: Liaw YF, Raptopoulou-Gigi M, Cheinquer H, et al. Efficacy and safety of entecavir versus adefovir in chronic hepatitis B patients with evidence of hepatic decompensation. Hepatology 2011;54: Manns MP, Akarca US, Chang TT, et al. Long-term safety and tolerability of entecavir in patients with chronic hepatitis B in the rollover study ETV-901. Expert Opin Drug Saf 2012 Jan 11 [Epub ahead of print]. 11. Chang TT, Liaw YF, Wu SS, et al. Long-term entecavir therapy results in the reversal of fibrosis/cirrhosis and continued histological improvement in patients with chronic hepatitis B. Hepatology 2010;52:
4 1050 PAN ET AL CLINICAL GASTROENTEROLOGY AND HEPATOLOGY Vol. 10, No Chang TT, Lai CL, Kew YS, et al. Entecavir treatment for up to 5 years in patients with hepatitis B e antigen-positive chronic hepatitis B. Hepatology 2010;51: Tenney DJ, Rose RE, Baldick CJ, et al. Long-term monitoring shows hepatitis B virus resistance to entecavir in nucleosidenaive patients is rare through 5 years of therapy. Hepatology 2009;49: Colonno RJ, Rose R, Baldick CJ, et al. Entecavir resistance is rare in nucleoside naive patients with hepatitis B. Hepatology 2006; 44: Tenney DJ, Rose RE, Baldick CJ, et al. Two-year assessment of entecavir resistance in lamivudine-refractory hepatitis B virus patients reveals different clinical outcomes depending on the resistance substitutions present. Antimicrob Agents Chemother 2007;51: Yokosuka O, Takaguchi K, Fujioka S, et al. Long-term use of entecavir in nucleoside-naive Japanese patients with chronic hepatitis B infection. J Hepatol 2010;52: Yuen MF, Seto WK, Fung J, et al. Three years of continuous entecavir therapy in treatment-naive chronic hepatitis B patients: viral suppression, viral resistance, and clinical safety. Am J Gastroenterol 2011;106: Chang TT, Lai CL, Yoon SK, et al. Long-term virological suppression, resistance and histological improvement in nucleos(t)ide-naive Asian chronic hepatitis B patients treated with entecavir in studies ETV-022/-027/-901 (abstract PP0565). Hepatol Int 2011;5: Reprint requests Address requests for reprints to: Calvin Q. Pan, MD, Division of Liver Diseases, Department of Medicine, The Mount Sinai Medical Center, Mount Sinai School of Medicine, Forty First Avenue, Flushing, New York cpan11355@yahoo.com; fax: Conflicts of interest These authors disclose the following: Calvin Q. Pan has received research grants from Gilead, Bristol-Myers Squibb, Novartis, Idenix, Roche, and Schering Plough and has also served as a consultant, adviser, and on speakers bureau for Gilead, Bristol-Myers Squibb, Novartis, Idenix, Roche, Schering Plough, Onyx, Three Rivers, Salix, Genentech, Vertex, and Pharmasset. Ke-Qin Hu has participated in speakers bureaus and has received grants/research support from Bristol-Myers Squibb, Gilead, and Merck. Kris V. Kowdley has received research grants/support from Bristol-Myers Squibb, Intercept, Abbott, Pharmasset, Merck, Mochida, and Conatus; has served as a consultant for Novartis; and has also received honoraria for participation in advisory boards for Vertex, Pharmasset, Merck, and Gilead. Ching- Lung Lai received honoraria from Bristol-Myers Squibb for participation in lectures. Samuel S. Lee has participated as a consultant for Bristol- Myers Squibb, Gilead, Janssen, Merck, Novartis, Pharmasset, Roche, and Vertex; has received research support from Bristol-Myers Squibb, Gilead, Merck, Roche, Novartis, Pharmasset, and Vertex; and has been a speaker for Bristol-Myers Squibb, Gilead, Merck, and Roche. David Cohen and Hong Tang are employees of Bristol-Myers Squibb. Naoky Tsai has participated in advisory boards and speakers bureaus for Bristol-Myers Squibb and Gilead and received research grants from Bristol-Myers Squibb and Gilead. The remaining authors disclose no conflicts. Funding The study was funded by Bristol-Myers Squibb.
5 1050.e1 PAN ET AL CLINICAL GASTROENTEROLOGY AND HEPATOLOGY Vol. 10, No. 9 Supplementary Figure 1. Proportion of patients achieving HBV DNA 300 copies/ml (by PCR) through 5 years of entecavir treatment. *Of all the Asian patients in study ETV-022, 69% (140/204) had HBV DNA 300 copies/ml at the end of year 1. Of those included in the longterm Asian cohort, 59% had HBV DNA 300 copies/ml at the end of year 1. Supplementary Figure 2. Mean serum HBV DNA (by PCR) through 5 years of entecavir treatment. The horizontal dashed line indicates the lowest level of detection (300 copies/ml). B/L, baseline. Supplementary Table 1. Cumulative Safety Results of Entecavir Long-term Asian Cohort (n 94) n(%) Any AE 89 (95) Grade 3/4 AE 12 (13) Serious AE 10 (11) Neoplasms (benign, malignant, unspecified) 5 (5) Hemangioma 2 (2) Lipoma 1 (1) Skin papilloma 1 (1) Sweat gland tumor 1 (1) Discontinuation because of AE 0 (0) All deaths 7 (7) On-treatment ALT flares 1 (1)
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