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1 Supplementary Appendix This appendix has been provided by the authors to give readers additional information about their work. Supplement to: Pan CQ, Duan Z, Dai E, et al. Tenofovir to prevent hepatitis B transmission in mothers with high viral load. N Engl J Med 2016;374: DOI: /NEJMoa (PDF updated June 16, 2016.)
2 Tenofovir to Prevent Hepatitis B Transmission in Mothers with High Viral Load Online Supplemental Materials Calvin Q. Pan, MD 1,2, Zhong Ping Duan, MD 3, Er Hei Dai, MD 4, Shu Qin Zhang, MD 5, Guo- Rong Han, MD 6, Yuming Wang, MD 7, Huai Hong Zhang, MD 8, Huai Bin Zou, MD 3, Bao Shen Zhu, MD 9, Wen Jing Zhao, MD 10, Hong-Xiu Jiang, MD 6, for the China Study Group for the Mother-to-Child Transmission of Hepatitis B. 1 Division of Gastroenterology and Hepatology, Department of Medicine, NYU Langone Medical Center, New York University School of Medicine, New York, NY, USA; 2 Beijing Youan Hospital, Capital Medical University, Beijing, China; 3 Artificial Liver Center, Beijing Youan Hospital, Capital Medical University, Beijing, China; 4 Division of Liver Diseases, The Fifth Hospital of Shijiazhuang, Hebei Medical University, Shijiazhuang, China; 5 Department of Artificial Liver, Hepatobiliary Disease Hospital of Ji Lin Province, Changchun, China; 6 Department of Gynecology and Obstetrics, The Second Affiliated Hospital of the Southeast University, Nanjing, China; 7 Institute for Infectious Diseases, Southwest Hospital, The Third Military Medical University, Chongqing, China; 8 Department of Medicine, Nanyang Center Hospital, Nanyang, China; 9 Department of Gynecology and Obstetrics, The Fifth Hospital of Shijiazhuang, Hebei Medical University, Shijiazhuang, China; 10 Central Laboratory, Hepatobiliary Disease Hospital of Ji Lin Province, Changchun, China. Professor Calvin Q. Pan, st Ave., Flushing, NY 11355, USA, or at panc01@nyu.edu. Page 2
3 Table of Contents List of Investigators and Members of the Study Group... Page 4 List of Sections 1. The Standard of Care at the Investigational Sites and Study Procedures... Page 5 2. Ethical Considerations, Randomization, and the Consent Process... Page 8 2a. Justification of Randomization... Page 8 2b. The Ethics Review and Patient Consent Process... Page 9 3. The Changes in HBV DNA and ALT Levels among Mothers... Page Assessment of HBV Transmission Rates between the Two Groups... Page Acknowledgements... Page References... Page 17 List of Tables Table S3. Maternal HBV DNA and ALT levels at each time point... Page 11 Table S4. Comparing transmission rates using various analyses... Page 14 List of Figures Figure S1. The follow-up and the immunization schedules... Page 7 Figure S3. The dynamic changes in the levels of HBV DNA and ALT... Page 13 Page 3
4 List of Investigators and Members of the Study Group The China Study Group for the Mother-to-Child Transmission of Hepatitis B include the following investigators and members: Calvin Q. Pan, MD, FACP, FACG, FAASLD (Leading principal investigator [PI]) NYU Langone Medical Center, New York University School of Medicine, New York, USA; Zhong Ping Duan, MD (Site PI), Huai Bin Zou, MD, Yu Chen, MD, Shan Gao, MD, and Xiao Hui Zhang, MD Beijing Youan Hospital, Capital Medical University, Beijing, China; Er Hei Dai, MD (Site PI), Bao Shen Zhu, MD, Su Wen Li, MD, and Hua Chun Yin, MD The Fifth Hospital of Shijiazhuang, Hebei Medical University, Shijiazhuang, China; Shu Qin Zhang, MD (Site PI), Wen Jing Zhao, MD, Han Chang, MD Hepatobiliary Disease Hospital of Ji Lin Province, Ji Lin, China; Guo-Rong Han, MD (Site PI), Hong-Xiu Jiang, MD, Wei Zhao, MD, Xin Yue, MD, and Yi Ding, MD, Jinmei Shi, RN The Second Affiliated Hospital of the Southeast University, Nan Jing, China; Yuming Wang, MD (Site PI), Jun Nan Li, MD, Hong Fei Huang, MD, and Yan Qiong Zhang, MD Southwest Hospital of The Third Military Medical University, Chong Qing, China; Huai Hong Zhang, MD (Site PI), Yu Feng Zhai, MD, Li Zhang, MD, and Xiao Hu Zhang, MD Nanyang Central Hospital, Nan Yang, China; and Lei Xiao, MD Guangzhou No. 8 People's Hospital, Guangzhou, China. Page 4
5 Section 1. The Standard of Care at the Investigational Sites and Study Procedures Participating sites were selected from among the top academic centers in their regions (all sites are classified by the health department as tier 3 hospitals, the highest level of excellence for patient care). All institutions follow the clinical guidelines that are published by the Chinese Medical Association. Pregnant mothers with hepatitis B infection typically register with the hospital s obstetrics clinic at gestational week 12 16, are followed-up every 6 8 weeks before gestational week 28, and are then followed-up every 4 weeks until their delivery. Maternal hepatitis B status, pregnancy complications, and fetal development are assessed during the follow-ups. At birth, the infant is assessed for Apgar scores, birth defects (the presence of any deformities), and growth and developmental milestones (height, weight, and head circumference). The standard vaccination schedule is: the first dose of the hepatitis B vaccine (10 µg) is administered within 12 hours after birth, and two subsequent vaccinations are provided at week 4 and week 24. In addition, 200 IU of hepatitis B immune globulin (HBIg) is administered at birth with the first hepatitis B virus (HBV) vaccine, although it is injected into a different limb. According to the Chinese clinical practice guidelines, the same dose of HBIg is also administered at week 4. Routine postpartum follow-ups for the mothers and infants are scheduled at week 4 and week 24, and infants receive the immunoprophylaxis during these visits. The infants hepatitis B status is also determined via blood tests at a visit between week 28 and week In the current study, all enrolled patients were followed-up according to the aforementioned schedule and standard of care before the delivery (Figure S1), 2 although we performed more frequent postpartum follow-ups. After the delivery, all participants and their infants were followed-up at weeks 4, 12, 24, and 28, and tenofovir disoproxil fumarate (TDF)- Page 5
6 treated mothers were also followed-up at weeks 8 and 16, or until their alanine aminotransferase (ALT) levels normalized (after week 16) if they were elevated after the cessation of antiviral therapy. The schedule for infant immunization in this study was the same as the standard of care. All HBV vaccines and HBIg were purchased from the same manufacturer via our research grant, were stored in the central laboratory in Beijing, and were distributed to the appropriate sites according to the patients follow-up schedules. The drugs shipping and storage were monitored by our clinical research organization and central laboratory to ensure compliance with the manufacturer s requirements. Gilead Sciences provided the TDF, which was also distributed from our central laboratory in Beijing. All infants received 10 µg of the HBV vaccine (ENGERIX-B ; GlaxoSmithKline Biologicals Ltd.) within 6 hours after birth, and two additional vaccinations at week 4 and week 24. The HBIg (200 IU; Hualan Biological Engineering Inc.) was administered intramuscularly at birth and week 4. Page 6
7 Figure S1. The follow-up and the immunization schedules HBeAg: hepatitis B e-antigen, HBV: hepatitis B virus, TDF: tenofovir disoproxil fumarate, HBIg: hepatitis B immune globulin. Page 7
8 Section 2. Ethical Considerations, Randomization, and the Consent Process 2a) Justification of randomization The management of pregnant mothers with chronic hepatitis B infection remains a challenge, because of issues regarding the prevention of vertical transmission and the safety concerns regarding fetal exposure to antiviral therapy. 1,3,4 Without immunoprophylaxis after birth, 80 90% of infants from hepatitis B e-antigen (HBeAg)-positive mothers may develop chronic hepatitis B. 1,3-8 Thus, the current recommendations from the Centers for Disease Control and the World Health Organization are to provide the HBV vaccine and HBIg within 12 hours after birth, which is followed by two additional vaccinations for infants from mothers with chronic hepatitis B. 2,9 This intervention can reduce the mother-to-child transmission (MTCT) rate in HBeAg-positive mothers from 90% to approximately 5 10%, although the MTCT rate varies among HBeAg-positive mothers with different levels of HBV viremia. A study by Zou et al. revealed a linear relationship between maternal HBV DNA levels and MTCT rates. 10 Among infants from mothers with HBV DNA levels of <6 log 10 copies/ml, log 10 copies/ml, log 10 copies/ml, and >8 log 10 copies/ml, the rates of developing chronic hepatitis B after immunoprophylaxis were 0%, 3.2%, 6.7%, and 7.6%, respectively (P<0.001 for the trend). Based on these results, we designed a randomized trial for several reasons: 1) Several studies have investigated the use of antiviral therapy to prevent MTCT and have reported inconsistent results, and only one randomized placebo-controlled trial of lamivudine treatment was performed during the third trimester. 15 However, approximately 30% of the enrolled patients were lost to follow-up, and the MTCT rate in the treatment arm did not significantly differ from that in the placebo arm, based on the observational data analysis. While we were performing the present study, several other studies of antiviral treatment during Page 8
9 pregnancy have reported a significant reduction in MTCT rates when mothers were treated during the third trimester. 11,16-19 However, these studies were all non-randomized studies and most of them included a small sample size. 2) Among the existing non-randomized studies, approximately 50% of the patients refused to take antiviral treatment during pregnancy and served as the control group, which may reflect the patients being uncertain regarding the riskbenefit ratio. 3) Various guidelines (e.g., European Association for the Study of the Liver, or American Association for the Study of Liver Diseases) have used the non-randomized trials results to recommend considering antiviral treatment for high viremic mothers, 20,21 although the 2015 World Health Organization guidelines do not recommend this approach, 9 because of the absence of high-quality data. Thus, there is no universal consensus among the major guidelines. In addition, the current standard of care (HBIg and a series of HBV vaccinations) can eliminate approximately 90% of MTCT among HBeAg-positive mothers. Therefore, we used this standard of care to provide adjuvant therapy to prevent transmission. However, at the time we designed this study, there were no high-quality data to guide the treatment of highly viremic mothers with HBV, and limited safety data for TDF use in mothers with mono-hbv infection. Thus, given that the efficacy of antiviral treatment for preventing transmission in mothers with hepatitis B and the risk of fetal exposure were not clearly established, it was medically justifiable for mothers to only receive antiviral therapy with close monitoring. 2b) The ethics review and patient consent process Before initiating the study, the study protocol was evaluated and approved by an American ethics review board (ERB) that has full accreditation from the Association for the Accreditation of Human Research Protection Program. In addition, each institution s ERB reviewed and approved the study protocol. During the study period, the American and local Page 9
10 ERBs provided dual supervision of the study sites, and annual ERB approval was sought after the individual boards assessed the site-specific reports and those from the external data monitoring committee. Pregnant women with chronic hepatitis B were recruited from the investigational sites, although no screening activity was initiated before the informed consent process. Before obtaining the patient s informed consent, the site investigator explained the following critical points to the patients: 1) The standard method for preventing MTCT of chronic hepatitis B is to administer HBIg and the HBV vaccine, which has an overall success rate of approximately 90%. 2) To further reduce the transmission rate among highly viremic mothers, antiviral therapy may be used, although there are no long-term safety data and its efficacy has not been well established. Therefore, further studies are needed to evaluate the risk-benefit ratio of antiviral therapy, and there is no guarantee that antiviral therapy during the third trimester can provide successful outcomes. 3) If the mother wished to enroll in the study, there would be a 50% of chance that she would either receive tenofovir until postpartum week 4 or receive no antiviral treatment, and that she must accept the assigned treatment and agree to the follow-up schedule. 4) Although safety data are available for fetal exposure to tenofovir in mothers who are infected with HIV or co-infected with HBV and HIV, the safety of fetal exposure in women who are infected with only HBV is not clearly understood. 5) The patients could withdraw from the study at any time after enrollment, and could then elect to receive standard care. After discussing the study details with the mother and the child s father and answering all of their questions, written informed consent was obtained from the patient. A copy of the informed consent was given to each patient. Page 10
11 Section 3. The Changes in HBV DNA and ALT Levels among Mothers Table S3. Maternal HBV DNA and ALT levels at each time point Median values (IQR) TDF group (n=97) Control group (n=100) P-value * Maternal HBV DNA levels (log 10 IU/mL) Baseline 8.19 ( ) 8.18 ( ) 0.52 Gestational week ( ) 7.47 ( ) <0.001 At delivery 4.66 ( ) 8.01 ( ) <0.001 Postpartum week ( ) 7.93 ( ) <0.001 Postpartum week ( ) 7.52 ( ) 0.20 Postpartum week ( ) 8.28 ( ) 0.18 HBV DNA reduction (log 10 IU/mL) HBV DNA reduction at delivery 3.56 ( ) 0.20 ( ) <0.001 Levels of <200,000 IU/mL at delivery, n (%) 66/97 (68.0%) 2/100 (2.0%) <0.001 Maternal ALT Levels (U/L) Baseline 15.0 ( ) 17.0 ( ) 0.20 Gestational week ( ) 15.1 ( ) 0.13 At delivery 18.0 ( ) 15.0 ( ) 0.02 Page 11
12 Postpartum week ( ) 42.4 ( ) 0.42 Postpartum week ( ) No test (per protocol) N/A Postpartum week ( ) 42.0 ( ) 0.28 Postpartum week ( ) No test (per protocol) N/A Postpartum week ( ) 33.5 ( ) 0.84 IQR: interquartile range, TDF: tenofovir disoproxil fumarate, HBV: hepatitis B virus, ALT: alanine aminotransferase, N/A: not available. *P-values were calculated using the Mann-Whitney U test. When a patient s HBV DNA levels were <20 IU/mL, the result was imputed as 19 IU/mL. At delivery, the median (IQR) HBV DNA levels in the TDF group were significantly lower than those in the control group (4.66 [ ] log 10 IU/mL vs [ ] log 10 IU/mL, P<0.001). Page 12
13 ALT Levels (U/L) HBV DNA Levels (log 10 IU/mL) Figure S3. The dynamic changes in the levels of HBV DNA and ALT Controls TDF 0 80 Controls TDF TDF: tenofovir disoproxil fumarate, HBV: hepatitis B virus, ALT: alanine aminotransferase. The median values are shown, with the interquartile range indicated using the error bars. Page 13
14 Section 4. Assessment of HBV Transmission Rates between the Two Groups Table S4. Comparing transmission rates using various analyses Groups Cases (n) analyzed Non-infected infants (n) Infected infants (n) Infection rates (95% CI) P-value Intention-to-treat analysis (missing subjects = infected) TDF-treated % ( %) Control % ( %) Modified intention-to-treat analysis (missing subjects = non-infected) TDF-treated % (0 3.04%) 0.03 Control % ( %) Per-protocol analysis (missing subjects were excluded) TDF-treated % (0 3.20%) 0.01 Control % ( %) Imputing missing data analysis 1 (infected infants identified via randomization assuming a 6.82% infection rate)* TDF-treated % (0 3.04%) 0.01 Control % ( %) Imputing missing data analysis 2 (infected infants identified via randomization assuming a 12.08% infection rate)* TDF-treated % (0 3.04%) Control % ( %) TDF: tenofovir disoproxil fumarate, CI: confidence interval. Page 14
15 *In this study, 17 patients withdrew, which resulted in the absence of final outcome data (at the infants' age of 28 weeks). Therefore, the number of the infected cases among these patients was evaluated using randomized allocations. First, we produced an ordered list of patients by assigning infants in the TDF-treated group (n=5) to subject numbers 1 5, and assigning infants in the control group (n=12) to the remaining 12 subject numbers. Second, we used the Excel "randbetween" function to obtain lists of random numbers between 1 and 17 (Excel 2010, Microsoft Corp). If the allocated number was repeated, we used the next allocated number in the list. This enabled us to randomly assign infected cases from the top of each list (patient numbers in the lists below) to the 17 cases with missing data, using two different scenarios: 1) We assumed an infection rate of 6.82% among the 17 infants (based on the infection rate in the control group), and randomly selected one infant from List 1 (patient 17 was selected). 2) We also assumed an infection rate of 12.08% (the upper limit of the 95% CI for the infection rate in the control group), and randomly selected two infants from List 2 (patients 10 and 7 were selected). Random allocations of infected cases among the 17 missing patients using two scenarios List 1 (infection rate: 6.82%) List 2 (infection rate: 12.08%) Page 15
16 Section 5. Acknowledgements We thank the patients who participated in this study, as well as the members of the China Study Group for the Mother-to-Child Transmission of Hepatitis B for their contributions to the study. Dr. Calvin Q. Pan designed the study protocol, obtained the research grant, and supervised the trial. All site investigators contributed to the collection of the clinical data. We thank the central coordinators, Drs. Frank R. Huang and Zheng Zeng, for their contributions to the data verification and site communication. The statistical analyses were performed by Drs. Calvin Q. Pan and Er Hei Dai. Dr. Linda Rolnitzky (Division of Biostatistics, NYU School of Medicine, USA) provided statistical advice and assistance for this study. Dr. Jing Hang Xu (Beijing University, China) and Dr. Helen Sun (St. George's University, Grenada) provided assistance with the data analysis. Dr. Calvin Q. Pan wrote the first draft of the manuscript, revised the manuscript with inputs from all authors, and communicated with the journal. Dr. Richard J Whitley (University of Alabama at Birmingham, USA) provided suggestions to improve the draft manuscript. We thank Gilead Sciences for providing research funding and the study drug (tenofovir disoproxil fumarate). Page 16
17 Section 6. References 1. Pan CQ, Duan ZP, Bhamidimarri KR, et al. An algorithm for risk assessment and intervention of mother to child transmission of hepatitis B virus. Clin Gastroenterol Hepatol 2012;10: Centers for Disease Control and Prevention (CDC). Hepatitis B vaccination recommendations for infants, children, and adolescents. December ( 3. Park JS, Pan C. Current recommendations of managing HBV infection in preconception or pregnancy. Front Med 2014;8: Pan CQ, Lee HM. Antiviral therapy for chronic hepatitis B in pregnancy. Semin Liver Dis 2013;33: Stevens CE, Beasley RP, Tsui J, Lee WC. Vertical transmission of hepatitis B antigen in Taiwan. N Engl J Med 1975;292: Beasley RP, Trepo C, Stevens CE, Szmuness W. The e antigen and vertical transmission of hepatitis B surface antigen. Am J Epidemiol 1977;105: Wong VC, Lee AK, Ip HM. Transmission of hepatitis B antigens from symptom free carrier mothers to the fetus and the infant. Br J Obstet Gynaecol 1980;87: Burk RD, Hwang LY, Ho GY, Shafritz DA, Beasley RP. Outcome of perinatal hepatitis B virus exposure is dependent on maternal virus load. J Infect Dis 1994;170: WHO. Guidelines for the Prevention, Care and Treatment of Persons with Chronic Hepatitis B, March ( Page 17
18 10. Zou H, Chen Y, Duan Z, Zhang H, Pan C. Virologic factors associated with failure to passive-active immunoprophylaxis in infants born to HBsAg-positive mothers. J Viral Hepat 2012;19:e Chen HL, Lee CN, Chang CH, et al. Efficacy of maternal tenofovir disoproxil fumarate in interrupting mother-to-infant transmission of hepatitis B virus. Hepatology 2015;62: Cao LH, Zhao PL, Liu ZM, et al. Efficacy and safety of nucleoside analogs on blocking father-to-infant vertical transmission of hepatitis B virus. Exp Ther Med 2015;9: Pan CQ, Han GR, Jiang HX, et al. Telbivudine prevents vertical transmission from HBeAg-positive women with chronic hepatitis B. Clin Gastroenterol Hepatol 2012;10: Han GR, Cao MK, Zhao W, et al. A prospective and open-label study for the efficacy and safety of telbivudine in pregnancy for the prevention of perinatal transmission of hepatitis B virus infection. J Hepatol 2011;55: Xu WM, Cui YT, Wang L, et al. Lamivudine in late pregnancy to prevent perinatal transmission of hepatitis B virus infection: a multicentre, randomized, double-blind, placebocontrolled study. J Viral Hepat 2009;16: Wu Q, Huang H, Sun X, et al. Telbivudine prevents vertical transmission of hepatitis B virus from women with high viral loads: a prospective long-term study. Clin Gastroenterol Hepatol 2015;13: Zhang H, Pan CQ, Pang Q, Tian R, Yan M, Liu X. Telbivudine or lamivudine use in late pregnancy safely reduces perinatal transmission of hepatitis B virus in real-life practice. Hepatology 2014;69: Page 18
19 18. Greenup AJ, Tan PK, Nguyen V, et al. Efficacy and safety of tenofovir disoproxil fumarate in pregnancy to prevent perinatal transmission of hepatitis B virus. J Hepatol 2014;61: Pan CQ, Mi LJ, Bunchorntavakul C, et al. Tenofovir disoproxil fumarate for prevention of vertical transmission of hepatitis B virus infection by highly viremic pregnant women: a case series. Dig Dis Sci 2012;57: European Association For The Study Of The Liver. EASL clinical practice guidelines: Management of chronic hepatitis B virus infection. J Hepatol 2012;57: Lok AS, McMahon BJ. Chronic hepatitis B: update Hepatology 2009;50: Page 19
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