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The Impact of Antibiotic Treatment on Diarrhea and Growth in Early Childhood

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The Impact of Antibiotic Treatment on Diarrhea and Growth in Early Childhood ARE OUR FAVORITE DRUGS KILLING THE WRONG BUGS? THE IMPACT OF ANTIBIOTIC TREATMENT ON DIARRHEA AND GROWTH IN EARLY CHILDHOOD Elizabeth Tacket Rogawski A dissertation submitted to the faculty of the University of North Carolina at Chapel Hill in partial fulfillment of the requirements for the degree of Doctor of Philosophy in the Department of Epidemiology. Chapel Hill 2015 Approved by: Daniel J. Westreich Steven R. Meshnick Sylvia Becker-Dreps Linda S. Adair Robert S. Sandler © 2015 Elizabeth Tacket Rogawski ALL RIGHTS RESERVED ii ABSTRACT Elizabeth Tacket Rogawski: Are our favorite drugs killing the wrong bugs? The impact of antibiotic treatment on diarrhea and growth in early childhood (Under the direction of Daniel J. Westreich) Diarrhea is a recurring illness in childhood that is associated with malnutrition, stunted growth, and cognitive impairment. Children with diarrhea and other common childhood illnesses are frequently treated with antibiotics, often against recommendations. Antibiotic exposures early in life may increase susceptibility to infections and affect child growth through modifications of the gastrointestinal microbiota. We assessed the impact of antibiotic treatment on diarrheal risk and growth in a birth cohort from 2009 to 2013 of 497 children from semi- urban slums of Vellore, India. We estimated the effect of antibiotic treatment for diarrhea on the timing of a subsequent episode using inverse probability of exposure-weighted Kaplan-Meier curves. We also estimated the effect of any early life antibiotic exposure on rates of diarrhea using negative binomial regression. Based on these results, we used the parametric g-formula to model the impact of hypothetical interventions to prevent unnecessary antibiotic exposures. To assess the impact on growth, we estimated the effects of antibiotic exposures in the first 6 months on height and weight z-scores using longitudinal general linear regression. More than half of children were given at least one course of antibiotics in the first 6 months and more than half of these exposures were likely unnecessary. Antibiotic treatment of diarrhea was associated with reduced time to a subsequent episode, especially among younger iii infants. In addition, the adjusted relative incidence rate of diarrhea from 6 months to 3 years of age was higher among children who received any antibiotics before 6 months compared to those who did not, especially among children who were no longer exclusively breastfed by 6 months. We estimated that preventing unnecessary antibiotic exposures before 6 months could substantially reduce the incidence of diarrhea in early childhood. There were no associations between early antibiotic use and growth in the first 6 months and from 6 months to 3 years. Early life antibiotic exposure was associated with increased diarrheal risk, but had no association with growth. While antibiotics must be used for treatment when necessary, the potential for increased susceptibility to diarrhea should be considered when making treatment decisions. iv ACKNOWLEDGEMENTS The completion of this dissertation would not have been possible without the help and care of many. From colleagues in the US and India to my family and friends, I am ever grateful for your continued support. I would first like to thank my Indian collaborators, Dr. Kang and her group at CMC. From the beginning, Dr. Kang was open and generous in her agreement to work with me. I must thank Naman for emailing me a link about her work, without which we might never have connected. Ever since Dr. Kang invited me to visit Vellore after a 10 minute phone conversation, I have been welcomed, encouraged, and challenged by her team. I thank Rajiv and Deepthi for spending so much time with me and cheerfully answering my endless questions. I am also grateful to Jenipha for tirelessly entering the data from the clinic records, and the clinic staff who taught me the nuances of the data. I thank all the many other individuals who were involved with the cohort studies at CMC, including the participants and their caregivers. I look forward to continue collaborating with such a strong and productive research team. My dissertation committee has been a source of outstanding support back at UNC. Steve put me to work my first semester and has supported many experiences since that have shaped my interests in epidemiology and public health. He sent me to Thailand for my first experience in international work and supported my crazy decision to take a year off and work at the Public Health Foundation of India in Delhi. When I came back with an idea and potential collaborators for my dissertation, he was immediately on board and ready to support the project. Steve gave v me the independence to purse my interests and has shared a wealth of knowledge and connections along the way. The Meshnick lab has been my home at UNC, and I am grateful for the help (and fun!) the entire lab has given over the years. Daniel has been an ideal mentor over the past 2 years. His passion and smarts have made me a better epidemiologist and have pushed this work far beyond what I could have expected. He helped me combine my interests in epidemiology methods with public health action so that my work is sufficiently nerdy, but also relevant and meaningful. Thank you for being actively interested in my professional growth. It has been wonderful to have a sounding board while figuring out my next steps. Thank you for always being available, prompt, and straightforward with feedback; I’ve learned so much. Dr. Becker-Dreps has been my “diarrhea lady,” and it’s been lots of fun swapping stories and comparing experiences between India and Nicaragua. Thank you for answering all my clinical questions and involving me with your microbiome work. I thank Dr. Adair for introducing me to the nuances of research in child growth. She spent hours with me talking through the complexities of the study questions and our data, and helped keep in perspective the many factors that interact together in the realm of child development. Thank you to Dr. Sandler for his consistently insightful comments about my writing. His extensive experience and broad perspective made me reconsider my assumptions and become a better writer. Thank you for reading every word I wrote! (I’m not sure anyone else did.) I would also like to thank Charlie Poole and Steve Wing for helping me to think critically in shaping my views about big picture epidemiology and public health. I hope to embody Charlie’s values as a public health worker (never a professional!). Thank you to Steve Cole for igniting my interest in methods and talking through methodological issues early on in this vi project. I thank Nancy, Carmen, and Valerie for all the work they do to keep our department together and for always providing a friendly smile and solution to the many issues I came up with. Finally, thank you to my family and friends. In the past 5 years, I have grown into a woman with a little experience, some skills, and a purpose. You have taught me so much about myself and the world. I especially thank my mom, who taught me how to write many years ago by editing with a sharp pencil on our couch and who has been my faithful confidante during all the highs and lows that the PhD process inevitably brings. UNC has been an incredibly supportive environment, from providing thousands of dollars in travel funds to having no issues with me taking a year off. I can’t imagine a better intellectual home. vii TABLE OF CONTENTS LIST OF TABLES ....................................................................................................................... xiii LIST OF FIGURES ..................................................................................................................... xvi LIST OF ABBREVIATIONS .................................................................................................... xviii CHAPTER I: SPECIFIC AIMS ...................................................................................................... 1 CHAPTER II: BACKGROUND AND SIGNIFICANCE .............................................................. 5 Burden and epidemiology of early childhood diarrhea ............................................................... 5 Burden ..................................................................................................................................... 5 Etiology.................................................................................................................................... 7 Risk factors .............................................................................................................................. 9 Diarrhea and growth .................................................................................................................. 13 Available and recommended treatments ................................................................................... 19 Antibiotics .............................................................................................................................. 20 Antibiotic prescribing patterns .............................................................................................. 22 Effect of antibiotics on diarrhea ................................................................................................ 27 Antibiotic-associated diarrhea .............................................................................................. 27 Other effects..........................................................................................................................
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