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Protecting Public Health at Inland Ohio Beaches: Development of Recreational Water Quality Indicators Predictive of Microbial and Microcystin Exposure

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Protecting Public Health at Inland Ohio Beaches: Development of Recreational Water Quality Indicators Predictive of Microbial and Microcystin Exposure Protecting Public Health at Inland Ohio Beaches: Development of Recreational Water Quality Indicators Predictive of Microbial and Microcystin Exposure DISSERTATION Presented in Partial Fulfillment of the Requirements for the Degree Doctor of Philosophy in the Graduate School of The Ohio State University By Jason W. Marion Graduate Program in Public Health The Ohio State University 2011 Dissertation Committee: Timothy J. Buckley, Advisor Jiyoung Lee, Co-Advisor Stanley Lemeshow John R. Wilkins III Copyright by Jason W. Marion 2011 Abstract Inland lakes are prone to contamination from a variety of sources within their watersheds. The changing environment can influence transport and fate of fecal indicators and may also influence the growth of harmful cyanobacteria, thereby occasionally creating health- related water quality concerns for recreational water users. To date, epidemiological and limnological studies pertaining to fecal indicators and harmful cyanobacteria have been limited with respect to inland U.S. lakes. The primary goals of this dissertation were to (1) evaluate illness risks associated with the fecal indicator E. coli, and (2) evaluate predictive tools potentially useful for the rapid prediction of E. coli densities and health- related concentrations of cyanotoxins in inland Ohio lakes. Through an epidemiological study and the collection of water quality data, predictive models for human illness and water quality advisories were developed. The relationship between water quality indicators and reported adverse health outcomes among users an inland Ohio beach were examined. Human health data collected via a prospective cohort study over 26 swimming days during the 2009 swimming season at East Fork Lake demonstrated that wading, playing or swimming in the water was found to be a significant risk factor for GI illness (adjusted odds ratio (aOR) of 3.2; CI=1.1, 9.0). Among water users (n = 806), E. ii coli density was associated with elevated GI illness risk where the highest E. coli quartile was associated with an aOR of 7.0 (CI=1.5, 32). Upon observing a significant illness association with E. coli densities among swimmers, the need for rapidly estimating E. coli densities was determined to have merit. Current approaches for quantifying E. coli densities rely on culture-based methods that require 18 or more hours to obtain a result. Using rapidly measured water quality parameters (e.g., total phosphorus, secchi depth, chlorophyll A), univariable models for rapidly estimating health-related E. coli densities were developed and considered for inland Ohio lakes using 182 beach water samples collected from seven Ohio lakes. Univariable logistic regression revealed that deviations in lake-specific water quality as measured by total phosphorus (p < 0.001), phycocyanin pigment (p = 0.018), and trophic state index (TSI) (p = 0.006) were predictive of E. coli levels exceeding recreational water quality criteria. Using the same samples, models were constructed for estimating cyanotoxin concentrations. Microcystin levels exceeding the 4 g/L low risk threshold set by the World Health Organization were detected by ELISA in 48 of 182 (26.4%) samples. A multivariable logistic regression model using practical and real-time measures of in vivo phycocyanin and secchi depth was constructed to predict beach conditions exceeding the low risk threshold for microcystin. The model (p = 0.030) predicted microcystin levels >4 g/L with acceptable discrimination as indicated by the area under the ROC curve (0.795). This study indicates a significant health risk for inland beach users and demonstrates the potential to predict health-related hazard levels using practical real-time measures are possible, enabling opportunities for interventions that protect public health. iii Dedication This document is dedicated to my parents Ronald and Patricia Marion. iv Acknowledgments I am extremely grateful to the support I received from my dissertation committee. This work would not have been possible without their encouragement and assistance in supporting my thinking. I am thankful for funding support from my advisor, Dr. Tim Buckley and my co-advisor, Dr. Jiyoung Lee. I am also particularly grateful to retired Ohio State Parks Chief, Dan West, and to Scott Fletcher with Ohio State Parks for supporting this research and enabling my work to receive financial support. The financial support provided by the Ohio Water Development Authority and the Public Health Preparedness for Infectious Diseases Program at OSU provided significant resources that will enable the work contained herein, to have significant impacts in its respective field. I am also forever grateful for the skills and training I received from my undergraduate mentors, Drs. Brian Reeder and David Smith at Morehead State University, who unknowingly had significant impacts on my thinking, and carrying out of the multiple studies contained in this dissertation. v Vita 1999................................................................Amelia High School, Batavia, OH 2001 ...............................................................A.A.S. Recreation and Wildlife Management, Hocking College 2004 ...............................................................B.S. Environmental Science, Morehead State University 2004 - 2006 ....................................................Graduate Associate, Institute for Regional Analysis and Public Policy, Morehead State University 2006 ...............................................................M.S. Biology, Morehead State University 2006 -2007 .....................................................Graduate Research Associate, College of Public Health, The Ohio State University 2008-2010 ......................................................Doctoral Fellow, Public Health Preparedness for Infectious Diseases, The Ohio State University 2010 ...............................................................M.S. Public Health, The Ohio State University vi Publications Marion, J.W., J. Lee, S. Lemeshow, and T.J. Buckley. 2010. Association of gastrointestinal illness and recreational water exposure at an inland U.S. beach. Water Research 44 (16), 4796-4804 Lee, C.S., J. Marion, J. Lee. 2011. A novel genetic marker for the rapid detection of Bacteroides fragilis in recreational water as a human-specific fecal indicator. Journal of Water and Health 9 (2), 253-264 Fields of Study Major Field: Public Health vii Table of Contents Abstract ............................................................................................................................... ii Dedication .......................................................................................................................... iv Acknowledgments............................................................................................................... v Vita ................................................................................................................................ vi Publications ....................................................................................................................... vii List of Tables ...................................................................................................................... x List of Figures .................................................................................................................. xiv Chapter 1: Introduction ...................................................................................................... 1 Chapter 2: Background ...................................................................................................... 6 Chapter 3: Association of Gastrointestinal Illness and Recreational Water Exposure at an Inland U.S. Beach ................................................................................................ 34 Chapter 4: Carlson‟s Trophic State Index as a Predictor of Advisory-Level E. coli Densities at Inland Ohio Beaches ......................................................................... 65 viii Chapter 5: In Vivo Phycocyanin Flourometry as a Rapid Screening Tool for Predicting Elevated Microcystin Concentrations at Inland Beaches...................................... 88 Chapter 6: Synthesis and Discussion .............................................................................. 114 References ....................................................................................................................... 122 Appendix A: Human Health Study Beach and Telephone Questionnaire ...................... 153 Appendix B: Human Health Study Recruitment Sign .................................................... 176 Appendix C: Water Quality Data Summary ................................................................... 177 ix List of Tables Table 3.1. Individual and household characteristics of persons surveyed at East Fork Lake (Ohio, United States) with complete surveys and telephone follow-up. ..... 47 Table 3.2. Descriptive statistics of beach water quality and beach usage during sampling days (N=26) at East Fork Lake (Ohio, United States). ......................................... 49 Table 3.3. Summary of beach exposures and reported illness by gender and age classification of respondents during the 2009 swimming season at East Fork Lake (Ohio, United States). ........................................................................................... 51 Table 3.4. Summary of gastrointestinal illnesses for beach users across various E. coli density
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