Clearing Up Murky Waters: Clarifying the Relationship Between Indicator Organisms and Disease in Recreational Water Settings

Many infectious bacterial and viral agents exist in the world and are located in areas where humans may come into contact with them. Food, water, and environmental locations may be contaminated with infectious material, and detecting the presence of these harmful biologic agents is of import to public health agencies. One method that has been used to determine if infectious agents may be present in food or water is measurement of "indicator" bacteria or viruses. Indicator organisms are easily measured bacteria or viruses whose presence in water or food is thought to parallel the potential presence of infectious agents in the same food or water samples. Because there are so many potential bacteria (or viruses) that may infect a sample, it is impractical to test for all of them; rather, measurement of a single indicator organism may be more feasible./nIndicator bacteria have been used to determine if marine waters at beaches across the United States are safe for swimming. Guidelines issued by the U.S. Environmental Protection Agency (U.S. EPA) have focused on determining when recreational waters may pose a risk of excess gastrointestinal illness among swimmers when compared to non-swimmers. However, marine environments are very complex, and tidal patterns, solar inactivation, water temperature, and many other factors all can influence the presence or absence of indicator and infectious microorganisms in the water. Research has indicated that indicator organisms may be useful in predicting gastrointestinal illness in marine environments, but other health outcomes have been less studied. In order to verify that indicator organisms do track well with infectious organisms, a systematic review and meta analysis was conducted to determine if indicator organisms can predict a different health outcome, skin infection. Once the link between indicator organisms and health outcomes was established, the next goal was to explore different methods to strengthen the relationship between indicator organisms and health. Currently, the U.S. EPA advises that a single bacterial indicator, Enterococcus, be measured in marine waters. A binary cutoff of above or below 104 colony forming units per 100 mL is used to advise whether a beach is unsafe or safe for swimming. In order to improve prediction of illness at beaches using indicator organisms, several methods were considered. Flexible statistical modeling techniques, such as SuperLearning, were used, as well as consideration of multiple biological and physical indicators at the same time. The final aim was to examine the potential sources of the infectious agents, as well as the indicator bacteria, at Avalon beach in Southern California./nThe results of this investigation suggest that indicator bacteria can be quite useful in predicting human illness, but perform better under certain conditions. The systematic review and meta-analysis showed that there was a strong relationship between certain indicator organisms and skin infections in marine water settings. Higher concentrations of total coliform, fecal coliform, E. coli, Enterococcus, and fecal Streptococci were associated with increased risk of skin related illness in marine waters. These findings support the biological plausibility of using indicator organisms to predict illness, even in a complicated, dynamic environment such as a marine beach. The second investigation found that application of the U.S. EPA guidelines at Avalon Beach did not accurately predict when waters were unsafe for swimming. However, use of flexible statistical methods (SuperLearner) greatly improved prediction of gastrointestinal illness over traditional modeling methods, such as logistic regression. Further improvements were seen when, instead of using a single indicator organism, combinations of biological and physical indicators were used. By combining physical and biological indicators, it was possible to identify circumstances when elevated concentrations of Enterococcus predicted excess gastrointestinal illness in swimmers. When solar radiation levels were low, indicator bacteria concentrations were more strongly associated with adverse health outcomes, whereas higher solar radiation levels were protective. This finding is biologically plausible because it is thought that solar radiation can directly damage indicator bacteria as well as pathogens and render them non-viable. Thus, under high solar radiation conditions, indicator organisms as well as infectious organisms would be inactivated. The final analysis examined groundwater flow as a potential risk to swimmers at Avalon beach. Because of a leaking sewage infrastructure at Avalon, it is thought that groundwater flux might be transporting raw sewage contents into the ocean water. Sewage is known to carry potentially high levels of pathogenic organisms, and thus groundwater flow levels might pose a direct threat to swimmers. When groundwater flow was higher, the incidence of gastrointestinal illness was elevated among swimmers who swallowed water, relative to swimmers who swallowed water on days when groundwater flow was lower. Additionally, the relationship between groundwater flow and solar radiation was similar to that seen with Enterococcus and solar radiation. When solar radiation levels were high, groundwater flow was less predictive of excess gastrointestinal illness, as would be expected. When traditional analysis methods were used to relate traditional and rapid indicators to illness, relationships were much stronger when groundwater flow was high versus when groundwater flow levels were lower. In conclusion, the results of these analyses suggest that indicator organisms can be used to predict health outcomes in recreational water settings, but that their performance may be greatly improved by using flexible modeling techniques as well as other indicators, such as solar radiation.

Advisor: Colford, Jr., John M