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Seasonal Dynamics and Relative Persistence Potential of the Enteric Species of Enterovirus in Wastewater

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Seasonal Dynamics and Relative Persistence Potential of the Enteric Species of Enterovirus in Wastewater Seasonal Dynamics and Relative Persistence Potential of the Enteric Species of Enterovirus in Wastewater A dissertation submitted to the Graduate School Of the University of Cincinnati In partial fulfillment of the requirements for the degree of Doctor of Philosophy In the Department of Biological Sciences Of the McMicken College of Arts and Sciences By Nichole E. Brinkman B.S., Biological Sciences Northern Kentucky University, Highland Heights, Kentucky, December 1999 M.S., Biological Sciences University of Cincinnati, Cincinnati, Ohio, March 2007 Committee Chair: Dr. Brian Kinkle ABSTRACT Human enteroviruses (EV) are a large group of enteric pathogens containing approximately 104 serotypes, which cluster into four different species (EV-A-D). They can be transmitted from infected to susceptible individuals via a person-to-person route, contaminated food and water used for recreation, shellfish harvesting, or drinking. Assessments of public health risk due to exposure to waterborne enteroviruses require, in part, an understanding of the levels of these pathogens in water sources. Two key factors in determining their occurrence in water are 1) knowing the extent of the diversity of this group present in a particular water source and 2) the ability of individual members to persist in water. Data published to date regarding presence and persistence potential of enteroviruses has been limited to poliovirus, and members of one of the four enterovirus species, leaving the majority of serotypes uncharacterized. The objectives for this project were to assess the diversity of enteroviruses present in wastewater and evaluate the influence that the persistence potential may have on the diversity profile. Towards this end, a method to concentrate representative enterovirus species was identified and determined to equally recover enterovirus species from primary effluent of wastewater. This method was then applied to monthly wastewater samples collected locally over a one year period for deep sequencing of enteroviruses present. This culture-independent, next- generation sequencing approach allowed for hundreds to thousands of enterovirus genomic sequences in each sample to be identified. Analysis of these sequences revealed that members of EV-A, EV-B and EV-C are present in each month of the year, while EV-D is present sporadically. EV-C is present in relatively low abundance year-round, while EV-A and EV-B alternate in predominance in a pattern that coincides with season. Investigation into the persistence potential of enteroviruses in wastewater shows that persistence cannot be described by species, but is serotype dependent. Poliovirus (EV-C) and enterovirus 70 (EV-D) were ii observed to be most persistent, while CVA10 (EV-A) was least persistent. The members of EV- B examined (CVA9, CVB1 and echovirus 30) showed moderate levels of persistence. The work described here provides a new perspective of the diversity profile of enterovirus present in wastewater and begins to decode the relative persistence potential of, until now, unrepresented members. iii iv ACKNOWLEDGEMENTS I would like to thank my advisors, Brian Kinkle and Shay Fout, for their continued support and guidance throughout my tenure as a graduate student. I would also like to thank the remaining members of my committee, Eric Villegas, Nick Ashbolt and Dennis Grogan for their time, guidance and support. I am very grateful to Scott Keely for his assistance with statistical and bioinformatic analyses that was critical in several parts of the research presented here. In addition, his continued passion for science and relentless discussions about many scientific topics has made me a better scientist. I also thank several colleagues in my branch at the EPA, Shannon Griffin, Jennifer Cashdollar and Eunice Varughese for the many discussions we had about the research contained in this dissertation. These women are awesome lab mates and I am grateful to work with such dedicated civil servants. I would also like to thank my management at EPA, especially Ann Grimm, for their support of my pursuit of this degree. I also thank my family, especially my daughter Sydney, for their support and patience. I will always be grateful for their love and support. v TABLE OF CONTENTS ABSTRACT .................................................................................................................................... II ACKNOWLEDGEMENTS ........................................................................................................... V LIST OF TABLES ....................................................................................................................... VII LIST OF FIGURES ................................................................................................................... VIII LIST OF ABBREVIATIONS ........................................................................................................ X CHAPTER 1 GENERAL INTRODUCTION ............................................................................... 1 CHAPTER 2 EVALUATION OF METHODS USING CELITE TO CONCENTRATE NOROVIRUS, ADENOVIRUS AND ENTEROVIRUS FROM WASTEWATER ................... 29 ABSTRACT .................................................................................................................................. 30 INTRODUCTION ........................................................................................................................... 31 MATERIALS AND METHODS ....................................................................................................... 33 RESULTS ..................................................................................................................................... 41 DISCUSSION ................................................................................................................................ 47 REFERENCES .............................................................................................................................. 53 CHAPTER 3 SEASONAL DYNAMICS OF ENTERIC ENTEROVIRUS SPECIES IN WASTEWATER........................................................................................................................... 57 ABSTRACT .................................................................................................................................. 58 INTRODUCTION ........................................................................................................................... 59 MATERIALS AND METHODS ....................................................................................................... 61 RESULTS ..................................................................................................................................... 67 DISCUSSION ................................................................................................................................ 73 REFERENCES .............................................................................................................................. 78 CHAPTER 4 COMPARATIVE ATTENUATION PROFILES OF ENTERIC ENTEROVIRUS SPECIES IN WASTEWATER ..................................................................................................... 85 ABSTRACT .................................................................................................................................. 86 INTRODUCTION ........................................................................................................................... 87 MATERIALS AND METHODS ....................................................................................................... 89 RESULTS ..................................................................................................................................... 95 DISCUSSION .............................................................................................................................. 110 REFERENCES ............................................................................................................................ 117 CHAPTER 5 GENERAL CONCLUSIONS .............................................................................. 123 APPENDIX A ............................................................................................................................. 134 APPENDIX B ............................................................................................................................. 143 APPENDIX C ............................................................................................................................. 148 vi List of Tables Table 1.1. Human enteric enterovirus species and serotypes ......................................................... 6 Table 1.2. Top 5 serotypes of each enterovirus species reported to NESS over 39 years ........... 12 Table 2.1: Concentrations of indigenous enteric viruses in a composite primary effluent sample ....................................................................................................................................................... 47 Table 3.1. Analysis of reads obtained from 454 sequencing of VP1 ........................................... 68 Table 3.2. Analysis of reads obtained from 454 sequencing of VP4 ........................................... 69 Table 3.3. Read assignments to other viruses ............................................................................... 69 Table 4.1. Enterovirus serotypes .................................................................................................
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