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Hepatitis E Virus in the Terai of Nepal

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HEPATITIS E VIRUS IN THE TERAI OF NEPAL: COMMUNITY-BASED COHORT STUDY OF PREGNANT WOMEN IN SARLAHI DISTRICT AND INVESTIGATION OF THE 2014 OUTBREAK IN BIRATNAGAR, MORANG DISTRICT by Lisa J. Krain, ScM A dissertation submitted to Johns Hopkins University in conformity with the requirements for the degree of Doctor of Philosophy Baltimore, Maryland July, 2016 © 2016 Lisa J. Krain All Rights Reserved ABSTRACT In South Asia, hepatitis E virus (HEV) is an important cause of morbidity and mortality and poses a special threat to pregnant women. However, the burden of both infection and illness in the Terai of Nepal have received scant attention. We enrolled 2363 pregnant women in a community-based cohort study in Sarlahi District and followed threm through three months postpartum. Baseline anti-HEV IgG seroprevalence was 11.7% [95% confidence interval (CI): 10.2%-13.3%] and varied with age, socioeconomic factors, and meat consumption, but not with water source or latrine access. The incidence of HEV seroconversion was 32.3/1000 person-years (p*y) during pregnancy [95% CI: 14.8 to 61.3/1000 p*y] and 44.3/1000 p*y overall [95% CI: 27.1 to 68.4/1000 p*y]. One acute hepatitis E case (genotype 1) was confirmed, but most hepatitis-like illnesses were not attributable to hepatitis A, B, C, or E. Jaundice was linked to 1/2 maternal deaths. Earlier and extended serologic monitoring would permit improved surveillance of pregnancy outcomes and antibody kinetics. Environmental testing could help clarify exposure pathways and seasonal patterns. A large outbreak of waterborne hepatitis E occurred in Biratnagar municipality in 2014. We tested sera collected from healthy adults in Biratnagar and Dharan before the outbreak and from patients seen at three hospitals in Biratnagar during the outbreak. The population seroprevalence of anti-HEV IgG was low in Biratnagar (~5.6%) before the outbreak. Among 450 oubtreak patients, 42.2% were IgG+, 14.7% IgM+, and 2.9% HEV Ag+. Acute HEV markers varied geographically and by hospital. The outbreak underscores the need for access to clean water, and for improved epidemiologic surveillance and response. Hepatitis E virus threatens public health in the Terai. Rural and urban populations in Nepal remain highly vulnerable to infection, disease, and mortality due to HEV. Improvements in water, ii sanitation, and hygiene are needed to prevent both sporadic and epidemic hepatitis E, especially as development of the Terai increases. Targeted interventions may help alleviate the increased burden of disease borne by pregnant women, individuals with chronic medical conditions, and members of socially- and economically-disadvantaged groups. Dissertation Advisors & Readers: Kenrad E. Nelson, MD (advisor) Professor, Department of Epidemiology Infectious Disease Epidemiology Alain B. Labrique, PhD (committee chair) Associate Professor, Department of International Health Global Disease Epidemiology and Control Lisa P. Jacobson, ScD Professor, Department of Epidemiology General Epidemiology and Methodology, STATEPI Wikrom W. Karnsakul, MD Assistant Professor, Pediatrics Pediatric Gastroenterology Stephan Ehrhardt, MD (alternate) Associate Professor, Department of Epidemiology Clinical Trials and Evidence Synthesis William P. Ball, PhD (alternate) Professor, Department of Geography and Environmental Engineering Water Institute iii ACKNOWLEDGMENTS This dissertation reflects the dedication, work, and support of a multitude of people, and I am grateful to and for all of you. Ken Nelson has graciously shared his time, his vast experience, and his stories with me over many years. He has been a tireless advocate and a voice of reason. It has been a privilege to have him as an advisor and as a mentor. Alain Labrique lives the mHealth he preaches, having supervised my work from Baltimore, Brussels, Bangladesh, and even 30,000 feet. He has taught me much about the practice and politics of scientific research and public health, and I am fortunate to have had the chance to work with him. I am enormously grateful to David Celentano, Lisa Jacobson, Fran Burman, and Peggy Hayeslip for their encouragement, their wise advice, and their unwavering support throughout my doctoral training. I thank my committee for providing useful suggestions for improving and extending the work. I appreciate the faculty members who generously provided guidance on my dissertation research and work in Nepal: Chris Heaney, Joanne Katz, Jim Tielsch, Luke Mullany, and Mark Steinhoff. The Nepal Nutrition Intervention Project – Sarlahi (NNIPS), under the expert leadership of “Daak Saab” Subarna Khatry, Steve LeClerq, and Tirtha Raj Shakya, was instrumental in carrying out this research and was the key to its success. I appreciate the efforts of Senior Supervisors Uma Shankar Sah and Shishir Var Shrestha, Supervisors Punya Dahal and Shiv Raj Bhattarai, and of the rest of the Flu study staff: TLIs, ANMs, Lab Team, Birth Team, Flu Data Collectors, and Data Center personnel. I thank the administrative and support staff in Kathmandu and Hariyon for their iv assistance, and the drivers for their skill and dedication. The Dahals, , provided warm hospitality and tasty food. I am grateful to the entire NNIPS family, who sent out a search party on motorcycles through the bazaar and sugarcane fields of Hariyon to rescue me from a lovely family of “kidnappers” who’d invited me to their home for tea and dinner on a day I’d forgotten my phone! I owe a special debt of gratitude to the thousands of women and infants who participated in the study, as well as to the other Sarlahi residents who introduced me to their language and customs with patience and enthusiasm. It is my hope that this work will return some of that goodwill to my former neighbors by contributing to improved health in the villages of Sarlahi and beyond. My research collaborators on the Biratnagar outbreak study, Birendra Prasad Gupta and John Ticehurst, braved numerous logistical and bureaucratic delays in order to see the project realized, and it has been a pleasure to work with them. The Bill and Melinda Gates Foundation generously funded this research. The Walter Reed / AFRIMS Research Unit – Nepal (WARUN) in Kathmandu, under the direction of Sanjaya Shrestha, and the Armed Forces Research Institute of Medical Sciences (AFRIMS) in Bangkok, provided laboratory and logistical support. I thank the administrative staff and lab techs in the Departments of Epidemiology, International Health, and Environmental Health at Johns Hopkins, in Global Health at Cincinnati Children’s Hospital, and at NNIPS and WARUN for their assistance in moving people, specimens, and resources around the world. Johns Hopkins University librarians have been a vital, if unsung, force in my success as a researcher. I am also grateful to Allan Massie, the UCLA IDRE & Statistical Consulting Group, and many others who freely share their technical knowledge; the world is a better place for your generosity. v I have benefited tremendously from the collegiality of my fellow students, especially those in the former Silbergeld Lab Group and at NNIPS who showed me the ropes and shared with me the trials and tribulations of graduate school. I am especially grateful to my close colleagues and friends Amy Peterson and Neha Naithani, whose humor, enthusiasm, insights, and friendship have served as sources of comfort and inspiration. My parents and grandparents instilled in me a love of learning and a passion for doing good in the world, encouraged my curiosity, supported my education, and helped me navigate the challenges I encountered along the way. My husband Michael has done double duty on the professional and domestic fronts while I worked on my research in Baltimore, in Nepal, and in the family room of our house. His quiet thoughtfulness, his understanding, and the example he sets in his own work constantly remind me how fortunate I am to share my life with him. I am eternally grateful for my family’s love and support. vi TABLE OF CONTENTS ABSTRACT ...................................................................................................................................................................................... II ACKNOWLEDGMENTS ................................................................................................................................................................ IV LIST OF TABLES ........................................................................................................................................................................ XIII LIST OF FIGURES....................................................................................................................................................................... XIV INTRODUCTION ............................................................................................................................................................................ 1 EPIDEMIOLOGIC PATTERNS OF HEPATITIS E VIRUS INFECTION..................................................................................... 2 Clinical Presentation of Hepatitis E ....................................................................................................................... 2 Human-Associated Genotypes 1 and 2................................................................................................................. 3 Animal-Associated Genotypes 3 and 4 ................................................................................................................
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