Advertisement

Climate Change and Waterborne Disease Risk in the Great Lakes Region of the U.S.

      Abstract

      Extremes of the hydrologic cycle will accompany global warming, causing precipitation intensity to increase, particularly in middle and high latitudes. During the twentieth century, the frequency of major storms has already increased, and the total precipitation increase over this time period has primarily come from the greater number of heavy events. The Great Lakes region is projected to experience a rise these extreme precipitation events.
      For southern Wisconsin, the precipitation rate of the 10 wettest days was simulated using a suite of seven global climate models from the UN Intergovernmental Panel on Climate Change (IPCC) Fourth Assessment Report. For each ranking, the precipitation rate of these very heavy events increases in the future. Overall, the models project that extreme precipitation events will become 10% to 40% stronger in southern Wisconsin, resulting in greater potential for flooding, and for the waterborne diseases that often accompany high discharge into Lake Michigan.
      Using 6.4 cm (2.5 in) of daily precipitation as the threshold for initiating combined sewer overflow into Lake Michigan, the frequency of these events is expected to rise by 50% to 120% by the end of this century. The combination of future thermal and hydrologic changes may affect the usability of recreational beaches. Chicago beach closures are dependent on the magnitude of recent precipitation (within the past 24 hours), lake temperature, and lake stage. Projected increases in heavy rainfall, warmer lake waters, and lowered lake levels would all be expected to contribute to beach contamination in the future.
      The Great Lakes serve as a drinking water source for more than 40 million people. Ongoing studies and past events illustrate a strong connection between rain events and the amount of pollutants entering the Great Lakes. Extreme precipitation under global warming projections may overwhelm the combined sewer systems and lead to overflow events that can threaten both human health and recreation in the region.

      Background

      Climate Change and Hydrologic Extremes

      Global climate change is expected to cause warming temperatures, sea-level rise, and a change in frequency of extremes of the hydrologic cycle (more floods and droughts). This study focuses on the health implications of heavy precipitation, with an in-depth look at related health risks in the U.S. Such heavy precipitation events often result in substantial societal impacts, including an increased risk of waterborne disease outbreaks. Heavy precipitation can lead to stormwater discharge of contaminants into water bodies if the volume exceeds the containment capacity. The seasonal contamination of surface water in early spring in North America and Europe may explain some of the seasonality in sporadic cases of many types of waterborne diseases. According to the North American chapter of the most recent IPCC report,
      Intergovernmental Panel on Climate Change
      Climate change 2007: impacts, adaptation and vulnerability. Contribution of Working Group II to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change.
      heavy precipitation events are expected to increase under climate change scenarios (Figure 1).
      Figure thumbnail gr1
      Figure 1Projected changes in total precipitation from the late twentieth to the late twenty-first centuries, based on middle-of-the-road increases in greenhouse gases: annual (left), winter (center), and summer (right). Source: IPCC, 2007
      Intergovernmental Panel on Climate Change
      Climate change 2007: impacts, adaptation and vulnerability. Contribution of Working Group II to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change.

      Rainfall Projections for the Great Lakes Region

      For the Great Lakes region of the U.S., contamination events typically occur when daily rainfall levels exceed a threshold of about 5–6 cm (2–2.5 in).

      Hayhoe K, Hellmann J, Lesht B, Nadelhoffer K, Wuebbles D. 2008: Climate change and Chicago: projections and potential impacts. An Assessment Prepared for the City of Chicago. In press.

      • McLellan S.L.
      • Hollis E.J.
      • Depas M.M.
      • Van Dyke M.
      • Harris J.
      • Scopel C.O.
      Distribution and fate of Escherichia coli in Lake Michigan following contamination with urban stormwater and combined sewer overflows.
      Given that rainfall extremes are expressions of climate, there is heightened concern as to how this type of event might change in a warmer future climate.
      Meteorologic theory indicates that the intensity of a precipitation event is regulated primarily by the local amount of moisture in the atmosphere during a storm and that the moisture-holding capacity of the atmosphere increases exponentially with temperature.
      • Trenberth K.E.
      Conceptual framework for changes of extremes of the hydrological cycle with climate change.
      Consequently, expectations are high that more intense precipitation will accompany global warming. This possibility is supported by many modeling studies that have simulated the climatic response to increasing concentrations of greenhouse gases.
      • Barnett D.N.
      • Brown S.J.
      • Murphy J.M.
      • Sexton D.M.H.
      • Webb M.J.
      Quantifying uncertainty in changes in extreme event frequency in response to doubled CO2 using a large ensemble of GCM simulations.
      • Kharin V.V.
      • Zwiers F.W.
      Estimating extremes in transient climate change simulations.
      • Meehl G.A.
      • Arblaster J.M.
      • Tebaldi C.
      Understanding future patterns of increased precipitation intensity in climate model simulations.
      • Wilby R.L.
      • Wigley T.M.L.
      Future changes in the distribution of daily precipitation totals across North America.
      Precipitation intensity (total precipitation divided by the number of wet days) is projected to increase almost everywhere, particularly in middle and high latitudes where average precipitation is also expected to increase.
      • Tebaldi C.
      • Hayhoe K.
      • Arblaster J.M.
      • Meehl G.A.
      Going to the extremes.
      Most of the Great Lakes region is projected to experience a rise in both average and extreme precipitation events.
      Intergovernmental Panel on Climate Change
      Climate change 2007: impacts, adaptation and vulnerability. Contribution of Working Group II to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change.
      • Diffenbaugh N.S.
      • Pal J.S.
      • Trapp R.J.
      • Giorgi F.
      Fine-scale processes regulate the response of extreme events to global climate change.
      These anticipated future changes are consistent with recent trends over the U.S., including the Great Lakes area. Major storms have been occurring with greater frequency during the twentieth century, and the total precipitation increase over this period has resulted disproportionately from the increase in heavy events.
      • Changnon S.A.
      • Kunkel K.E.
      Climate-related fluctuations in Midwestern floods during 1921–1985.
      • Karl T.R.
      • Knight R.W.
      Secular trends of precipitation amount, frequency, and intensity in the United States.
      • Karl T.R.
      • Knight R.W.
      • Plummer N.
      Trends in high-frequency climate variability in the 20th-century.
      This trend has been accentuated by the increase in heavy events toward the end of the century, the time of most pronounced global warming.
      • Groisman P.Y.
      • Knight R.W.
      • Karl T.R.
      • Easterling D.R.
      • Sun B.M.
      • Lawrimore J.H.
      Contemporary changes of the hydrological cycle over the contiguous United States: trends derived from in situ observations.
      • Kunkel K.E.
      • Easterling D.R.
      • Redmond K.
      • Hubbard K.
      Temporal variations of extreme precipitation events in the United States: 1895–2000.
      These large-scale findings were tailored to the Wisconsin–Chicago region, where we are conducting research on the health impacts of extreme events. In one example, the recent and future simulated precipitation rate of the 10 wettest days were computed for the Madison WI area from seven global climate models (GCMs) used in the UN Intergovernmental Panel on Climate Change (IPCC) Fourth Assessment Report
      Intergovernmental Panel on Climate Change
      Climate change 2007: impacts, adaptation and vulnerability. Contribution of Working Group II to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change.
      (Figure 2). For each ranking (tenth wettest day to the wettest day), the precipitation rate of these very heavy events increases in the future, and the enhancements are most pronounced for the most extreme events (wettest and second wettest days). Overall, the models project that these extremely heavy precipitation events will become 10% to 40% stronger in southern Wisconsin, resulting in greater potential for flooding and for the waterborne diseases that often accompany high discharge into Lake Michigan.
      • McLellan S.L.
      • Hollis E.J.
      • Depas M.M.
      • Van Dyke M.
      • Harris J.
      • Scopel C.O.
      Distribution and fate of Escherichia coli in Lake Michigan following contamination with urban stormwater and combined sewer overflows.
      Figure thumbnail gr2
      Figure 2GCM-simulated precipitation amounts in southern Wisconsin for the 10 wettest days in the late twentieth and late twenty-first centuries (10 days total for each century), based on middle-of-the-road projected increases in greenhouse gases.
      GCM, global climate model
      A somewhat different approach was used to estimate future changes in extreme precipitation over Chicago. For this application, the GCM output from two representative models, the geophysical fluid dynamics laboratory (GFDL) model and the parallel climate model (PCM) was statistically downscaled to provide higher-resolution information. Statistical downscaling uses historical observational data to tailor projections from a global model to a local scale. A statistical relationship is first established between a location's measured precipitation and the corresponding climate model output during a prior time interval, typically around 30 years. This historical relationship—between climate model output at the relatively coarse scale of the GCM and the daily precipitation values recorded on the local scale—is then used to downscale future model projections to the same local scale. This method assumes that the relationships between large- and small-scale processes remain the same over time.
      The change was analyzed in the frequency of heavy daily precipitation events, ranging from 1 to 5 cm (0.4–2.0 in), between the late twentieth and late twenty-first centuries (Figure 3). Although the precise changes are dependent on the assumed greenhouse gas emissions scenario, the results clearly indicate more frequent extreme events, ranging from ≤10% increases for 1–1.5 cm (0.4–0.6 in) events to >60% for the heaviest storms (≥4 cm [≥1.6 in]) in the high-emissions scenario. Using 6.35 cm (2.5 in) of daily precipitation as the threshold for initiating combined sewer overflow into Lake Michigan,

      Hayhoe K, Hellmann J, Lesht B, Nadelhoffer K, Wuebbles D. 2008: Climate change and Chicago: projections and potential impacts. An Assessment Prepared for the City of Chicago. In press.

      the frequency of these events is expected to rise by 50%–120% by the end of this century. This translates into an expected occurrence of about one event every other year in the recent past to approximately one event every year (low-emissions scenario) to 1.2 events every year (high-emissions scenario) by the end of this century.

      Hayhoe K, Hellmann J, Lesht B, Nadelhoffer K, Wuebbles D. 2008: Climate change and Chicago: projections and potential impacts. An Assessment Prepared for the City of Chicago. In press.

      Figure thumbnail gr3
      Figure 3Projected change in the frequency of heavy precipitation in Chicago by the late twenty-first century, based on downscaled climate model output for high-end and low-end greenhouse gas emissions scenarios from two global climate models used in the Chicago Climate Impact Assessment. Source: Hayhoe and Wuebbles

      Hayhoe K, Hellmann J, Lesht B, Nadelhoffer K, Wuebbles D. 2008: Climate change and Chicago: projections and potential impacts. An Assessment Prepared for the City of Chicago. In press.

      The expected changes in the hydrologic cycle, including increases in extreme precipitation events, should have a direct bearing on waterborne diseases in the Great Lakes. For example, the 1993 Cryptosporidium outbreak in Milwaukee was preceded by the heaviest rainfall in 50 years in the associated watersheds.
      • Curriero F.C.
      • Patz J.A.
      • Rose J.B.
      • Lele S.
      The association between extreme precipitation and waterborne disease outbreaks in the United States, 1948–1994.
      Summertime bacteria concentrations in an inland lake in Wisconsin (Lake Geneva) exhibit positive, significant correlations not only with mean summertime rainfall but also with the duration between rainfall events, a variable that is expected to increase in the future.
      • Allen M.R.
      • Ingram W.J.
      Constraints on future changes in climate and the hydrologic cycle.
      The combination of future thermal and hydrologic changes may affect the usability of recreational beaches. Chicago beach closures are dependent on the magnitude of recent precipitation (within the past 24 hours), lake temperature, and lake stage (i.e., height of the water surface above an established level).
      • Olyphant G.A.
      • Whitman R.L.
      Elements of a predictive model for determining beach closures on a real time basis: the case of 63rd Street Beach Chicago.
      Projected increases in heavy rainfall, warmer lake waters, and lowered lake levels
      • Kunkel R.
      • Wendland F.
      • Hannappel S.
      • Voigt H.J.
      • Wolter R.
      The influence of diffuse pollution on groundwater content patterns for the groundwater bodies of Germany.
      would all be expected to enhance beach contamination in the future. Although more extreme rainfalls would seem to contradict the projection of lower lake levels, the latter expectation stems from a large anticipated increase in evaporation at the lake surface (which can offset the precipitation gain) and a higher proportion of future precipitation falling as heavy events, even if the total precipitation amount does not rise.

      Vulnerability Factors

      Even today, many of our community water systems can be overburdened by extreme rainfall events. Heavy rainfall or snow melt can exceed the capacity of the sewer system or treatment plant, which are designed to discharge the excess wastewater directly into surface water bodies.
      • Perciasepe R.
      Combined sewer overflows: where are we four years after adoption of the CSO control policy?.
      • Rose J.B.
      • Simonds J.
      King County water quality assessment: assessment of public health impacts associated with pathogens and combined sewer overflows.
      In urban watersheds, more than 60% of the annual loads of all contaminants are transported during storm events.
      • Fisher G.T.
      • Katz B.G.
      Urban stormwater runoff: selected background information and techniques for problem assessment with a Baltimore Maryland case study.
      In general, turbidity increases during storm events, and studies have recently shown a correlation between increases in turbidity and illness in communities.
      • Morris R.D.
      • Naumova E.N.
      • Levin R.
      • Munasinghe R.L.
      Temporal variation in drinking water turbidity and diagnosed gastroenteritis in Milwaukee.
      • Schwartz J.
      • Levin R.
      • Hodge K.
      Drinking water turbidity and pediatric hospital use for gastrointestinal illness in Philadelphia.
      Also, higher winter temperatures could further enhance flooding from the contribution of snow melt.

      Combined Sewage Overflows and Aging Water Infrastructure

      Older cities around the nation have combined sewer systems, which are designed to capture both sanitary sewage and stormwater and convey these flows to a wastewater treatment plant. Large rain events can overwhelm these systems, causing untreated sewage mixed with stormwater to be released directly into receiving waters. The U.S. Environmental Protection Agency (EPA) has estimated that 770 communities release more than 3.2 trillion liters (850 billion gallons) of combined sewage to the nation's waterways annually.
      U.S. Environmental Protection Agency
      Impacts and control of CSOs and SSOs.
      As infrastructure improvements to sewer system capacity are made, the number of combined sewer overflows can be decreased. For example, the construction of an inline storage system in Milwaukee reduced the number of combined sewer overflows from 40–60 per year to 0–4 per year (with the average approximating 1.5 per year over the past 10 years). However, it remains difficult to capture the most extreme events. Changing weather patterns that bring more extreme storms to some regions may outpace the infrastructure improvements.

      Case Study

      Climate and water quality in Milwaukee

      The urban environment presents unique risks of water contamination. Runoff from impervious surfaces contains metals, pesticides, pathogens, and fecal indicator bacteria. It has been linked to adverse public health effects.
      • Bannerman R.T.
      • Owens D.W.
      • Dodds R.B.
      • Hornewer N.J.
      Sources of pollutants in Wisconsin stormwater.
      • Gaffield S.J.
      • Goo R.L.
      • Richards L.A.
      • Jackson R.J.
      Public health effects of inadequately managed stormwater runoff.
      • Haile R.W.
      • Witte J.S.
      • Gold M.
      • et al.
      The health effects of swimming in ocean water contaminated by storm drain runoff.
      In most municipal areas, urban stormwater is conveyed in separated sewer systems and discharged directly into receiving waters. Aging infrastructure may cause sanitary sewage to infiltrate into stormwater pipes, where it is essentially discharged with no treatment. Beaches are often located in urbanized areas and highly susceptible to stormwater impacts.
      • Scopel C.O.
      • Harris J.
      • McLellan S.L.
      Influence of nearshore water dynamics and pollution sources on beach monitoring outcomes at two adjacent Lake Michigan beaches.
      • Whitman R.L.
      • Nevers M.B.
      Foreshore sand as a source of Escherichia coli in nearshore water of a Lake Michigan beach.
      • Yamahara K.M.
      • Layton B.A.
      • Santoro A.E.
      • Boehm A.B.
      Beach sands along the California coast are diffuse sources of fecal bacteria to coastal waters.
      Accelerating development of urban coastal areas and changing storm patterns may synergistically increase the amounts of urban stormwater released into coastal systems.
      The Milwaukee River Basin consists of 1440 km2 (556 miles2) of rural, agricultural, suburban, and urban land use. The basin's watersheds drain to three major rivers that converge in downtown Milwaukee and discharge through a 140 m (0.09 mile) channel leading to Lake Michigan. Following storm events, the fecal indicator bacteria Escherichia coli can be detected in the channel at levels as high as 2000–7000 colony forming units (CFU)/100 ml. These levels are 10 times higher than the EPA-recommended limit for recreational waters.
      US Environmental Protection Agency
      Improved enumeration methods for recreational water quality indicators: Enterococci and Escherichia coli.
      The presence of E. coli demonstrates that fecal pollution is present; however, given the complexity of this system, the bacteria may come from agricultural runoff, urban stormwater, or sanitary sewage. Human viruses have been detected at this same site following storm events with no reported sewage overflows, providing evidence that sanitary sewage may be continually released into the basins tributaries. Storm events of >3 inches of rainfall within 24 hours may overwhelm the combined sewer systems and lead to an overflow. In this case, the levels of E. coli detected in the channel leading to Lake Michigan can be up to 10 times higher (e.g., 20,000–50,000 CFU/100 ml) than when there are no sewage overflows.
      • McLellan S.L.
      • Hollis E.J.
      • Depas M.M.
      • Van Dyke M.
      • Harris J.
      • Scopel C.O.
      Distribution and fate of Escherichia coli in Lake Michigan following contamination with urban stormwater and combined sewer overflows.
      These events generally occur less than three times per year, and do not occur at all in dry years (Figure 4).
      Figure thumbnail gr4
      Figure 4Levels of E. coli in the Milwaukee estuary, which discharges to Lake Michigan, 2001–2007, during base flow (n=46); following rain events with no CSO (n=70); and following CSO events (n=54). Boxes indicate 75% of values, with median values drawn in each. Whiskers are 95% of values and outliers are shown as closed circles. There were significant differences in E. coli levels following rainfall and CSOs compared to base flow (p≤0.05).
      CFU, colony forming units; CSO, combined sewer overflow
      Milwaukee is not unique in terms of its impact on the lake; many cities around the Great Lakes are situated near major rivers that come from a complex mixture of watershed sources. The Great Lakes, which serve as a drinking water source for more than 40 million people, are particularly susceptible to fecal pollution and can become reservoirs for waterborne diseases. Ongoing studies and past events illustrate a strong connection between rain events and the amount of pollutants entering the Great Lakes. The 1993 Cryptosporidium outbreak in Milwaukee, which sickened more than 400,000 people, coincided with record high flows in the Milwaukee River, a reflection of the amount of rainfall in the watershed.
      • Curriero F.C.
      • Patz J.A.
      • Rose J.B.
      • Lele S.
      The association between extreme precipitation and waterborne disease outbreaks in the United States, 1948–1994.

      Land-Use Patterns

      Land cover conversion to impervious surfaces (such as roadways and parking lots) increases both the volume and velocity of stormwater runoff, while also reducing groundwater infiltration.
      • Arnold C.L.
      • Gibbons J.C.
      Impervious surface coverage.
      The percentage of impervious surface within a watershed, for example, explains most of the variability for indicator bacteria across watersheds.
      • Mallin M.A.
      • Williams K.E.
      • Esham E.C.
      • Lowe R.P.
      Effect of human development on bacteriological water quality in coastal watersheds.
      Bacteria levels also tend to be elevated in agricultural catchments with higher levels of grazing cattle and sheep.
      • Crowther J.
      • Kay D.
      • Wyer M.D.
      Faecal-indicator concentrations in waters draining lowland pastoral catchments in the UK: relationships with land use and farming practices.
      Zoning and development policies can be a strong influence on the amount of impervious surface within each municipality.
      • Stone B.
      • Bullen J.L.
      Urban form and watershed management: how zoning influences residential stormwater volumes.

      Pathways of Human Exposure

      Drinking Water

      Waterborne disease outbreaks stemming from drinking water source contamination require a combination of determining factors. The requirements include: contamination of the source water, transport of the contaminant to the water intake or well of the drinking water system, insufficient treatment to reduce the level of contamination, and exposure to the contaminant.
      Recontamination of treated water may also occur at the public or homeowner's distribution system level.
      Waterborne disease outbreaks from all causes in the U.S. are distinctly seasonal, clustered in key watersheds, and associated with heavy precipitation.
      • Curriero F.C.
      • Patz J.A.
      • Rose J.B.
      • Lele S.
      The association between extreme precipitation and waterborne disease outbreaks in the United States, 1948–1994.
      In Walkerton, Ontario, in May 2000, heavy precipitation combined with failing infrastructure contaminated drinking water with E. coli 0157:H7 and Campylobacter jejuni, resulting in an estimated 2300 illnesses and seven deaths.
      • Hrudey S.E.
      • Payment P.
      • Huck P.M.
      • Gillham R.W.
      • Hrudey E.J.
      A fatal waterborne disease epidemic in Walkerton Ontario: comparison with other waterborne outbreaks in the developed world.

      Recreational Water and Stormwater Issues

      Heavy runoff after severe rainfall can also contaminate recreational waters and increase the risk of human illness
      • Schuster C.J.
      • Ellis A.
      • Robertson W.J.
      • Charron D.F.
      • Aramini J.J.
      • Marshall B.
      • Medeiros D.T.
      Infectious disease outbreaks related to drinking water in Canada, 1974–2001.
      through higher bacterial counts. This association is strongest at beaches closest to rivers.
      • Dwight R.H.
      • Semenza J.C.
      • Baker D.B.
      • Olson B.H.
      Association of urban runoff with coastal water quality in Orange County California.
      Ear, nose, and throat; respiratory; and gastrointestinal illnesses are commonly associated with recreational swimming in fresh and oceanic waters. Less abundant and potentially more severe waterborne diseases such as hepatitis, giardiasis, cryptosporidiosis, and toxic algal blooms pose serious health threats to vulnerable human populations and local wildlife. Swimmers have an elevated risk of contracting gastrointestinal illnesses versus nonswimmers, and this risk generally increases with prolonged exposure.
      • Wade T.J.
      • Pai N.
      • Eisenberg J.N.
      • Colford Jr, J.M.
      Do U.S. Environmental Protection Agency water quality guidelines for recreational waters prevent gastrointestinal illness? A systematic review and meta-analysis.
      Frequent water users, such as lifeguards or recreational enthusiasts, are at risk for waterborne disease, and young children, the elderly, pregnant women, and the immunocompromised have the greatest risk of suffering serious complications.
      • Wade T.J.
      • Pai N.
      • Eisenberg J.N.
      • Colford Jr, J.M.
      Do U.S. Environmental Protection Agency water quality guidelines for recreational waters prevent gastrointestinal illness? A systematic review and meta-analysis.
      • Gerba C.
      • Rose J.
      • Haas C.
      • Crabtree K.
      Waterborne rotavirus: a risk assessment.
      Macrodemographic trends toward an older and more immunocompromised U.S. population suggest that vulnerability to waterborne pathogens will continue to increase.
      Precipitation events and subsequent runoff may flush pathogens and indicator bacteria directly into water bodies and overwhelm or decrease the efficiency of the sewage disposal infrastructure. Although pathogens tend to co-occur with indicator bacteria, indicators are prone to false positive readings. Indicator bacteria may survive in soil sediments or beach sand, become re-suspended during a precipitation event, and confound estimates of waterborne disease risk.
      • Whitman R.L.
      • Nevers M.B.
      Foreshore sand as a source of Escherichia coli in nearshore water of a Lake Michigan beach.
      • Colford Jr, J.M.
      • Wade T.J.
      • Schiff K.C.
      • Wright C.C.
      • Griffith J.F.
      • Sandhu S.K.
      • et al.
      Water quality indicators and the risk of illness at beaches with nonpoint sources of fecal contamination.
      • McLellan S.L.
      • Salmore A.K.
      Evidence for localized bacterial loading as the cause of chronic beach closings in a freshwater marina.
      The periodicity and amplitude of contamination events are likely affected by processes that re-suspend or transport pathogens.
      • Kim J.H.
      • Grant S.B.
      • McGee C.D.
      • Sanders B.F.
      • Largier J.L.
      Locating sources of surf zone pollution: a mass budget analysis of fecal indicator bacteria at Huntington Beach California.
      • Nevers M.B.
      • Whitman R.L.
      Nowcast modeling of Escherichia coli concentrations at multiple urban beaches of southern Lake Michigan.
      Indicator bacteria are influenced by precipitation events up to a week prior to sample collection although recent precipitation (0–3 days) tends to exhibit the strongest relationships with their numbers.
      • Curriero F.C.
      • Patz J.A.
      • Rose J.B.
      • Lele S.
      The association between extreme precipitation and waterborne disease outbreaks in the United States, 1948–1994.
      Interval time between rainfall events can increase pollutant accumulation and subsequent loading into water bodies.
      • Olyphant G.A.
      • Whitman R.L.
      Elements of a predictive model for determining beach closures on a real time basis: the case of 63rd Street Beach Chicago.
      • Ackerman D.
      • Weisberg S.B.
      Relationship between rainfall and beach bacterial concentrations on Santa Monica Bay beaches.
      A disproportionately large pollutant mass similarly may be transported with the first precipitation event following the dry season in mid-latitude locations.
      • Bertrand-Krajewski J.
      • Chebbo G.
      • Saget A.
      Distribution of pollutant mass vs volume in stormwater discharges and the first flush phenomenon.
      • Krometis L.A.
      • Characklis G.W.
      • Simmons 3rd, O.D.
      • Dilts M.J.
      • Likirdopulos C.A.
      • Sobsey M.D.
      Intra-storm variability in microbial partitioning and microbial loading rates.
      Figure 5 shows an example of rainfall and contamination levels for Lake Geneva WI. Unseasonably high precipitation typically increases indicator bacteria loading into water bodies.
      • Lipp E.K.
      • Kurz R.
      • Vincent R.
      • Rodriguez-Palacios C.
      • Farrah S.R.
      • Rose J.B.
      The effect of seasonal variability and weather on microbial fecal pollution and enteric pathogens in a subtropical estuary.
      Earth system processes like the El Niño Southern Oscillation (ENSO) strongly influence interannual precipitation and therefore must be taken into account, especially for contamination events between September and March.
      • Lipp E.K.
      • Kurz R.
      • Vincent R.
      • Rodriguez-Palacios C.
      • Farrah S.R.
      • Rose J.B.
      The effect of seasonal variability and weather on microbial fecal pollution and enteric pathogens in a subtropical estuary.
      • Chigbu P.
      • Gordon S.
      • Strange T.
      Influence of inter-annual variations in climatic factors on fecal coliform levels in Mississippi Sound.
      • Emiliani F.
      Effects of hydroclimatic anomalies on bacteriological quality of the Middle Parana River (Santa Fe Argentina).
      Figure thumbnail gr5
      Figure 5Relationship between rainfall and beach contamination, Lake Geneva, Wisconsin CFU, colony-forming units

      Resulting Waterborne Illnesses

      Agents of disease

      More than 100 different types of pathogenic bacteria, viruses, and protozoa can be found in contaminated water.
      • Asai S.
      • Krzanowski J.J.
      • Anderson W.H.
      • et al.
      Effects of toxin of red tide, Ptychodiscus brevis, on canine tracheal smooth muscle: a possible new asthma-triggering mechanism.
      American Society for Microbiology
      Microbial pollutants in our nation's water: environmental and public health issues.
      American Water Works Association
      Protecting public health.
      Many of these have been implicated in a variety of illnesses transmitted by food or water.
      Waterborne and foodborne diseases continue to cause significant morbidity in the U.S. In 2002, there were 1330 water-related disease outbreaks,
      • Lynch M.
      • Painter J.
      • Woodruff R.
      • Braden C.
      Surveillance for foodborne-disease outbreaks—United States, 1998–2002.
      34 from recreational water and 30 from drinking water.
      • Dziuban E.J.
      • Liang J.L.
      • Craun G.F.
      • et al.
      Surveillance for waterborne disease and outbreaks associated with recreational water—United States, 2003–2004.
      • Liang J.L.
      • Dziuban E.J.
      • Craun G.F.
      • et al.
      Surveillance for waterborne disease and outbreaks associated with drinking water and water not intended for drinking—United States, 2003–2004.
      In recreational water, bacteria accounted for 32% of outbreaks, parasites (primarily Cryptosporidium) for 24%, and viruses for 10%.
      • Dziuban E.J.
      • Liang J.L.
      • Craun G.F.
      • et al.
      Surveillance for waterborne disease and outbreaks associated with recreational water—United States, 2003–2004.
      Bacteria were the most commonly identified agent in drinking water (29%, primarily Campylobacter) followed by parasites and viruses (each 5%).
      • Liang J.L.
      • Dziuban E.J.
      • Craun G.F.
      • et al.
      Surveillance for waterborne disease and outbreaks associated with drinking water and water not intended for drinking—United States, 2003–2004.
      Gastroenteritis continues to be the primary disease associated with food and water exposure. In 2003 and 2004, gastroenteritis was noted in 48% and 68% of reported recreational and drinking water outbreaks, respectively.
      • Dziuban E.J.
      • Liang J.L.
      • Craun G.F.
      • et al.
      Surveillance for waterborne disease and outbreaks associated with recreational water—United States, 2003–2004.
      • Liang J.L.
      • Dziuban E.J.
      • Craun G.F.
      • et al.
      Surveillance for waterborne disease and outbreaks associated with drinking water and water not intended for drinking—United States, 2003–2004.

      Surveillance

      Variability of indicator bacteria is controlled by the physical dynamics of each water body, and quality can be inferred from water's chemical and biologic qualities. Prevailing wind direction, toward or away from the beach, modulates biophysical environment and indicator bacteria relationships in large water bodies.
      • Nevers M.B.
      • Whitman R.L.
      Nowcast modeling of Escherichia coli concentrations at multiple urban beaches of southern Lake Michigan.
      Tidal cycles in large water bodies enhance indicator bacteria exchange from subsurface and soil reservoirs.
      • Boehm A.B.
      • Grant S.B.
      • Kim J.H.
      • et al.
      Decadal and shorter period variability of surf zone water quality at Huntington Beach, California.
      • Boehm A.B.
      • Weisberg S.B.
      Tidal forcing of enterococci at marine recreational beaches at fortnightly and semidiurnal frequencies.
      Elevated nitrate, ammonium, and caffeine in water quality measurements suggest recent cross-contamination with sewage-like materials.
      • Olyphant G.A.
      • Thomas J.
      • Whitman R.L.
      • Harper D.
      Characterization and statistical modeling of bacterial (Escherichia coli) outflows from watersheds that discharge into southern Lake Michigan.
      • Scott T.M.
      • Rose J.B.
      • Jenkins T.M.
      • Farrah S.R.
      • Lukasik J.
      Microbial source tracking: current methodology and future directions.
      Recent advances in molecular detection techniques have developed alternative indicators that are human-specific (e.g., demonstrating sewage inputs) such as human-specific Bacteroides spp., Methanobrevibacter smithii, and the surface protein gene present in enterococcus (esp).
      • Bernhard A.E.
      • Field K.G.
      Identification of nonpoint sources of fecal pollution in coastal waters by using host-specific 16S ribosomal DNA genetic markers from fecal anaerobes.
      • Scott T.M.
      • Jenkins T.M.
      • Lukasik J.
      • Rose J.B.
      Potential use of a host associated molecular marker in Enterococcus faecium as an index of human fecal pollution.
      • Ufnar J.A.
      • Wang S.Y.
      • Christiansen J.M.
      • Yampara-Iquise H.
      • Carson C.A.
      • Ellender R.D.
      Detection of the nifH gene of Methanobrevibacter smithii: a potential tool to identify sewage pollution in recreational waters.
      Precipitation and subsequent runoff events increase nutrient loading into water bodies, potentially enhancing floral productivity and water chlorophyll levels.
      • Nevers M.B.
      • Whitman R.L.
      Nowcast modeling of Escherichia coli concentrations at multiple urban beaches of southern Lake Michigan.
      Indicator bacteria survival is inversely related to water salinity and survival exponentially decreases with the duration and magnitude of solar radiation exposure.
      • Whitman R.L.
      • Nevers M.B.
      • Korinek G.C.
      • Byappanahalli M.N.
      Solar and temporal effects on Escherichia coli concentration at a Lake Michigan swimming beach.
      Surface water runoff also disturbs and re-suspends sediments, increases water turbidity, decreases solar radiation, and proportionally increases indicator bacteria loading into water bodies.
      • Nevers M.B.
      • Whitman R.L.
      Nowcast modeling of Escherichia coli concentrations at multiple urban beaches of southern Lake Michigan.

      Conclusion and Recommendations

      A broad range of improvements can be made toward attaining safe water quality in the U.S. These include such activities as data collection/surveillance, infrastructure improvements, land use planning, education, and research. Ultimately, better assessment of water quality and risk to the drinking water system from the watershed to the tap, as well as recreational water exposures, will allow for better prevention and controls to limit the impact of contamination events.

      Data Collection

      Based on the current state of surveillance, better indicators of fecal pollution are required. Public health officials and water managers need especially to be informed about the source of contamination, which could be from farm runoff, stormwater, or sanitary sewage.
      • Rose J.B.
      • Epstein P.R.
      • Lipp E.K.
      • Sherman B.H.
      • Bernard S.M.
      • Patz J.A.
      Climate variability and change in the United States: potential impacts on water- and foodborne diseases caused by microbiologic agents.
      Progress has been made in the field of microbial source tracking in terms of identifying source-specific alternative indicators, and molecular approaches offer a broader range of target organisms because they are not dependent on culture (for reviews, see Santo Domingo et al.
      • Santo Domingo J.W.
      • Bambic D.G.
      • Edge T.A.
      • Wuertz S.
      Quo vadis source tracking? Towards a strategic framework for environmental monitoring of fecal pollution.
      and Savichtcheva and Okabe
      • Savichtcheva O.
      • Okabe S.
      Alternative indicators of fecal pollution: relations with pathogens and conventional indicators, current methodologies for direct pathogen monitoring and future application perspectives.
      ). These have been used successfully in field studies.
      • Bower P.A.
      • Scopel C.O.
      • Jensen E.T.
      • Depas M.M.
      • McLellan S.L.
      Detection of genetic markers of fecal indicator bacteria in Lake Michigan and determination of their relationship to Escherichia coli densities using standard microbiological methods.
      • Brownell M.J.
      • Harwood V.J.
      • Kurz R.C.
      • McQuaig S.M.
      • Lukasik J.
      • Scott T.M.
      Confirmation of putative stormwater impact on water quality at a Florida beach by microbial source tracking methods and structure of indicator organism populations.
      • Santoro A.E.
      • Boehm A.B.
      Frequent occurrence of the human-specific Bacteroides fecal marker at an open coast marine beach: relationship to waves, tides and traditional indicators.
      However, widespread implementation will require extensive validation (including geographic differences), further assay development to reduce cost and complexity of new assay procedures, and standardization for use in public health laboratories.
      One of the disadvantages of the current system is that the outbreaks are detected after the fact—that is, after the contamination event and after individuals have become ill. The disease surveillance system is incapable of detecting outbreaks when diagnosed cases are not reported to health departments, such as when mild symptoms are attributed to other causes or when health problems cannot be treated medically. In addition, delays exist in detecting outbreaks because of the time necessary for laboratory testing and reporting of findings. Predictive forecasts of swimming-related health risk currently support beach management decisions at some U.S. coastal oceanic and Great Lakes beaches.
      • Nevers M.B.
      • Whitman R.L.
      Nowcast modeling of Escherichia coli concentrations at multiple urban beaches of southern Lake Michigan.
      • Bruesch M.E.
      • Biedrzycki P.A.
      Preliminary comparative analysis of two models used to predict E. coli levels in recreational water in Milwaukee.
      • Kuntz J.E.
      • Murray R.
      Non-point source of bacteria at the beach.
      Near-term forecast models require knowledge of the relationships between beach-specific environments and swimming health risks, collected and refined over multiple years of observations. Forecast models tend to have high sensitivity but relatively lower specificity and are therefore prone to false positive predictions of unsafe swimming conditions. Future research should investigate the extent to which dynamic environmental conditions can augment alternative human-specific pathogen indicators.

      Infrastructure Improvements

      This article has given specific examples of shortcomings in our current water systems. Upgrading sewage/stormwater infrastructure will obviously decrease the incidence of waterborne pathogen pollution.
      • Boehm A.B.
      • Grant S.B.
      • Kim J.H.
      • et al.
      Decadal and shorter period variability of surf zone water quality at Huntington Beach, California.
      • Nevers M.B.
      • Whitman R.L.
      • Frick W.E.
      • Ge Z.
      Interaction and influence of two creeks on Escherichia coli concentrations of nearby beaches: exploration of predictability and mechanisms.
      For example, ≤20% of childhood bacterial or viral diarrheal illnesses can be attributed to the density of holding tanks and other septic tanks.
      • Crowther J.
      • Kay D.
      • Wyer M.D.
      Relationships between microbial water quality and environmental conditions in coastal recreational waters: the Fylde coast UK.
      Improperly managed holding septic tanks discharge untreated sewage and contaminate surface water. Improving infrastructure may further reduce risks of contamination from extreme weather events.

      Land use/watershed protection

      Watershed protection will continue to be an extremely important factor influencing water quality.
      • Rose J.B.
      • Epstein P.R.
      • Lipp E.K.
      • Sherman B.H.
      • Bernard S.M.
      • Patz J.A.
      Climate variability and change in the United States: potential impacts on water- and foodborne diseases caused by microbiologic agents.
      Watershed water quality has a direct impact on source water and processed water quality as well as on recreational sites and coastal waters. Better farming practices (to capture and treat agricultural wastes) and surrounding vegetation buffers, along with improved city disposal systems to capture and treat wastes, would reduce the runoff of nutrients, toxic chemicals, trace elements, and microorganisms flowing into reservoirs, groundwater, lakes, rivers, estuaries, and coastal zones.

      Education and research

      According to Rose and others,
      • Rose J.B.
      • Epstein P.R.
      • Lipp E.K.
      • Sherman B.H.
      • Bernard S.M.
      • Patz J.A.
      Climate variability and change in the United States: potential impacts on water- and foodborne diseases caused by microbiologic agents.
      coordinated monitoring of physical, chemical, and biologic parameters should go toward building databases and integrated models that include environmental, ecologic, and social conditions, consequences, and costs. Collaborative, multidisciplinary training and research—involving health and veterinary professionals, biologists, ecologists, physical scientists, database specialists, modelers, and economists—is required to carry out comprehensive assessments and management plans. Interagency agreements will be needed to coordinate and support this initiative. Testing models and hypotheses based on observed temporal and spatial co-occurrences may help focus research policies. It is essential to better delineate—in time and location—the occurrence of disease and to maintain standardized health databases.
      Waterborne diseases remain a major public health problem in the U.S. and around the world. Enhanced understanding of the weather-sensitivity of many waterborne diseases is necessary along with improved surveillance, watershed/source water protection, and educational programs to improve the safety of our water. Scenarios of future global warming accompanied by climatic extremes only increase the importance of these improvements.
      The research conducted by Jonathan Patz, Stephen Vavrus, and Christopher Uejio is supported under a grant from the U.S. EPA STAR grants program, grant # R 832752010 entitled Health Risks from Climate Variability and Change in the Upper Midwest: a Place-based Assessment of Climate-related Morbidity. Contributions by Sandra McLellan are supported by NOAA Oceans and Human Health Initiative extramural grant NA05NOS4781243.
      No financial disclosures were reported by the authors of this paper.

      References

        • Intergovernmental Panel on Climate Change
        Climate change 2007: impacts, adaptation and vulnerability. Contribution of Working Group II to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change.
        in: Parry M.L. Canziani O.F. Palutikof J.P. van der Linden P.J. Hanson C.E. Cambridge University Press, Cambridge UK2007
      1. Hayhoe K, Hellmann J, Lesht B, Nadelhoffer K, Wuebbles D. 2008: Climate change and Chicago: projections and potential impacts. An Assessment Prepared for the City of Chicago. In press.

        • McLellan S.L.
        • Hollis E.J.
        • Depas M.M.
        • Van Dyke M.
        • Harris J.
        • Scopel C.O.
        Distribution and fate of Escherichia coli in Lake Michigan following contamination with urban stormwater and combined sewer overflows.
        J Great Lakes Res. 2007; 33: 566-580
        • Trenberth K.E.
        Conceptual framework for changes of extremes of the hydrological cycle with climate change.
        Clim Change. 1999; 42: 327-339
        • Barnett D.N.
        • Brown S.J.
        • Murphy J.M.
        • Sexton D.M.H.
        • Webb M.J.
        Quantifying uncertainty in changes in extreme event frequency in response to doubled CO2 using a large ensemble of GCM simulations.
        Clim Dynamics. 2006; 26: 489-511
        • Kharin V.V.
        • Zwiers F.W.
        Estimating extremes in transient climate change simulations.
        J Clim. 2005; 18: 1156-1173
        • Meehl G.A.
        • Arblaster J.M.
        • Tebaldi C.
        Understanding future patterns of increased precipitation intensity in climate model simulations.
        Geophys Res Lett. 2005; 32 (doi:10.1029/2005GL023680)
        • Wilby R.L.
        • Wigley T.M.L.
        Future changes in the distribution of daily precipitation totals across North America.
        Geophys Res Lett. 2002; 29 (doi:10.1029/2001GL013048)
        • Tebaldi C.
        • Hayhoe K.
        • Arblaster J.M.
        • Meehl G.A.
        Going to the extremes.
        Clim Change. 2006; 79: 185-211
        • Diffenbaugh N.S.
        • Pal J.S.
        • Trapp R.J.
        • Giorgi F.
        Fine-scale processes regulate the response of extreme events to global climate change.
        Proc Natl Acad Sci. 2005; 102: 15774-15778
        • Changnon S.A.
        • Kunkel K.E.
        Climate-related fluctuations in Midwestern floods during 1921–1985.
        J Water Resources Plann Manage. 1995; 121: 326-334
        • Karl T.R.
        • Knight R.W.
        Secular trends of precipitation amount, frequency, and intensity in the United States.
        Bull Am Meteor Soc. 1998; 79: 231-241
        • Karl T.R.
        • Knight R.W.
        • Plummer N.
        Trends in high-frequency climate variability in the 20th-century.
        Nature. 1995; 377: 217-220
        • Groisman P.Y.
        • Knight R.W.
        • Karl T.R.
        • Easterling D.R.
        • Sun B.M.
        • Lawrimore J.H.
        Contemporary changes of the hydrological cycle over the contiguous United States: trends derived from in situ observations.
        J Hydrometeorology. 2004; 5: 64-85
        • Kunkel K.E.
        • Easterling D.R.
        • Redmond K.
        • Hubbard K.
        Temporal variations of extreme precipitation events in the United States: 1895–2000.
        Geophys Res Lett. 2003; 30 (doi:10.1029/2003GL018052)
        • Curriero F.C.
        • Patz J.A.
        • Rose J.B.
        • Lele S.
        The association between extreme precipitation and waterborne disease outbreaks in the United States, 1948–1994.
        Am J Public Health. 2001; 91: 1194-1199
        • Allen M.R.
        • Ingram W.J.
        Constraints on future changes in climate and the hydrologic cycle.
        Nature. 2002; 419: 224-232
        • Olyphant G.A.
        • Whitman R.L.
        Elements of a predictive model for determining beach closures on a real time basis: the case of 63rd Street Beach Chicago.
        Environ Monit Assess. 2004; 98: 175-190
        • Kunkel R.
        • Wendland F.
        • Hannappel S.
        • Voigt H.J.
        • Wolter R.
        The influence of diffuse pollution on groundwater content patterns for the groundwater bodies of Germany.
        Water Sci Technol. 2007; 55: 97-105
        • Perciasepe R.
        Combined sewer overflows: where are we four years after adoption of the CSO control policy?.
        EPA Office of Wastewater Management, Washington DC1998
        • Rose J.B.
        • Simonds J.
        King County water quality assessment: assessment of public health impacts associated with pathogens and combined sewer overflows.
        Report for Water and Land Resources Division, Dept of Natural Resources, Seattle WA1998
        • Fisher G.T.
        • Katz B.G.
        Urban stormwater runoff: selected background information and techniques for problem assessment with a Baltimore Maryland case study.
        U.S. Geological Survey Water-Supply Paper 2347, Baltimore MD1988
        • Morris R.D.
        • Naumova E.N.
        • Levin R.
        • Munasinghe R.L.
        Temporal variation in drinking water turbidity and diagnosed gastroenteritis in Milwaukee.
        Am J Public Health. 1996; 86: 237-239
        • Schwartz J.
        • Levin R.
        • Hodge K.
        Drinking water turbidity and pediatric hospital use for gastrointestinal illness in Philadelphia.
        Epidemiology. 1997; 8: 615-620
        • U.S. Environmental Protection Agency
        Impacts and control of CSOs and SSOs.
        U.S. Environmental Protection Agency Office of Water, Washington DC2004 (Report No.: EPA 833-R-04-001)
        • Bannerman R.T.
        • Owens D.W.
        • Dodds R.B.
        • Hornewer N.J.
        Sources of pollutants in Wisconsin stormwater.
        Water Sci Technol. 1993; 28: 241-259
        • Gaffield S.J.
        • Goo R.L.
        • Richards L.A.
        • Jackson R.J.
        Public health effects of inadequately managed stormwater runoff.
        Am J Public Health. 2003; 93: 1527-1533
        • Haile R.W.
        • Witte J.S.
        • Gold M.
        • et al.
        The health effects of swimming in ocean water contaminated by storm drain runoff.
        Epidemiology. 1999; 10: 355-363
        • Scopel C.O.
        • Harris J.
        • McLellan S.L.
        Influence of nearshore water dynamics and pollution sources on beach monitoring outcomes at two adjacent Lake Michigan beaches.
        J Great Lakes Res. 2006; 32: 543-552
        • Whitman R.L.
        • Nevers M.B.
        Foreshore sand as a source of Escherichia coli in nearshore water of a Lake Michigan beach.
        Appl Environ Microbiol. 2003; 69: 5555-5562
        • Yamahara K.M.
        • Layton B.A.
        • Santoro A.E.
        • Boehm A.B.
        Beach sands along the California coast are diffuse sources of fecal bacteria to coastal waters.
        Environ Sci Technol. 2007; 41: 4515-4521
        • US Environmental Protection Agency
        Improved enumeration methods for recreational water quality indicators: Enterococci and Escherichia coli.
        US Environmental Protection Agency Office of Water, Office of Science and Technology, Washington DC2000 (Report No: EPA 821/R-97/004)
        • Arnold C.L.
        • Gibbons J.C.
        Impervious surface coverage.
        J Am Plann Assoc. 1996; 62: 243-258
        • Mallin M.A.
        • Williams K.E.
        • Esham E.C.
        • Lowe R.P.
        Effect of human development on bacteriological water quality in coastal watersheds.
        Ecol Appl. 2000; 10: 1047-1056
        • Crowther J.
        • Kay D.
        • Wyer M.D.
        Faecal-indicator concentrations in waters draining lowland pastoral catchments in the UK: relationships with land use and farming practices.
        Water Res. 2002; 36: 1725-1734
        • Stone B.
        • Bullen J.L.
        Urban form and watershed management: how zoning influences residential stormwater volumes.
        Environ Plann B Plann Des. 2006; 33: 21-37
      2. (Anonymous)Cryptosporidium in water supplies. Department of the Environment, Department of Health, London1990
        • Hrudey S.E.
        • Payment P.
        • Huck P.M.
        • Gillham R.W.
        • Hrudey E.J.
        A fatal waterborne disease epidemic in Walkerton Ontario: comparison with other waterborne outbreaks in the developed world.
        Water Sci Technol. 2003; 47: 7-14
        • Schuster C.J.
        • Ellis A.
        • Robertson W.J.
        • Charron D.F.
        • Aramini J.J.
        • Marshall B.
        • Medeiros D.T.
        Infectious disease outbreaks related to drinking water in Canada, 1974–2001.
        Can J Public Health. 2005; 96: 254-258
        • Dwight R.H.
        • Semenza J.C.
        • Baker D.B.
        • Olson B.H.
        Association of urban runoff with coastal water quality in Orange County California.
        Water Environ Res. 2002; 74: 82-90
        • Wade T.J.
        • Pai N.
        • Eisenberg J.N.
        • Colford Jr, J.M.
        Do U.S. Environmental Protection Agency water quality guidelines for recreational waters prevent gastrointestinal illness?.
        Environ Health Perspect. 2003; 111: 1102-1109
        • Gerba C.
        • Rose J.
        • Haas C.
        • Crabtree K.
        Waterborne rotavirus: a risk assessment.
        Water Res. 1996; 30: 2929-2940
        • Colford Jr, J.M.
        • Wade T.J.
        • Schiff K.C.
        • Wright C.C.
        • Griffith J.F.
        • Sandhu S.K.
        • et al.
        Water quality indicators and the risk of illness at beaches with nonpoint sources of fecal contamination.
        Epidemiology. 2007; 18: 27-35
        • McLellan S.L.
        • Salmore A.K.
        Evidence for localized bacterial loading as the cause of chronic beach closings in a freshwater marina.
        Water Res. 2003; 37: 2700-2708
        • Kim J.H.
        • Grant S.B.
        • McGee C.D.
        • Sanders B.F.
        • Largier J.L.
        Locating sources of surf zone pollution: a mass budget analysis of fecal indicator bacteria at Huntington Beach California.
        Environ Sci Technol. 2004; 38: 2626-2636
        • Nevers M.B.
        • Whitman R.L.
        Nowcast modeling of Escherichia coli concentrations at multiple urban beaches of southern Lake Michigan.
        Water Res. 2005; 39: 5250-5260
        • Ackerman D.
        • Weisberg S.B.
        Relationship between rainfall and beach bacterial concentrations on Santa Monica Bay beaches.
        J Water Health. 2003; 1: 85-89
        • Bertrand-Krajewski J.
        • Chebbo G.
        • Saget A.
        Distribution of pollutant mass vs volume in stormwater discharges and the first flush phenomenon.
        Water Res. 1998; 32: 2341-2356
        • Krometis L.A.
        • Characklis G.W.
        • Simmons 3rd, O.D.
        • Dilts M.J.
        • Likirdopulos C.A.
        • Sobsey M.D.
        Intra-storm variability in microbial partitioning and microbial loading rates.
        Water Res. 2007; 41: 506-516
        • Lipp E.K.
        • Kurz R.
        • Vincent R.
        • Rodriguez-Palacios C.
        • Farrah S.R.
        • Rose J.B.
        The effect of seasonal variability and weather on microbial fecal pollution and enteric pathogens in a subtropical estuary.
        Estuaries. 2001; 24: 266-276
        • Chigbu P.
        • Gordon S.
        • Strange T.
        Influence of inter-annual variations in climatic factors on fecal coliform levels in Mississippi Sound.
        Water Res. 2004; 38: 4341-4352
        • Emiliani F.
        Effects of hydroclimatic anomalies on bacteriological quality of the Middle Parana River (Santa Fe Argentina).
        Rev Argent Microbiol. 2004; 36: 193-201
        • Asai S.
        • Krzanowski J.J.
        • Anderson W.H.
        • et al.
        Effects of toxin of red tide, Ptychodiscus brevis, on canine tracheal smooth muscle: a possible new asthma-triggering mechanism.
        J Allergy Clin Immunol. 1982; 69: 418-428
        • American Society for Microbiology
        Microbial pollutants in our nation's water: environmental and public health issues.
        American Society for Microbiology, Office of Public Affairs, Washington DC1998
        • American Water Works Association
        Protecting public health.
        AWWA, Boston1996
        • Lynch M.
        • Painter J.
        • Woodruff R.
        • Braden C.
        Surveillance for foodborne-disease outbreaks—United States, 1998–2002.
        MMWR Surveill Summ. 2006; 55: 1-42
        • Dziuban E.J.
        • Liang J.L.
        • Craun G.F.
        • et al.
        Surveillance for waterborne disease and outbreaks associated with recreational water—United States, 2003–2004.
        MMWR Surveill Summ. 2006; 55: 1-30
        • Liang J.L.
        • Dziuban E.J.
        • Craun G.F.
        • et al.
        Surveillance for waterborne disease and outbreaks associated with drinking water and water not intended for drinking—United States, 2003–2004.
        MMWR Surveill Summ. 2006; 55: 31-65
        • Boehm A.B.
        • Grant S.B.
        • Kim J.H.
        • et al.
        Decadal and shorter period variability of surf zone water quality at Huntington Beach, California.
        Environ Sci Technol. 2002; 36: 3885-3892
        • Boehm A.B.
        • Weisberg S.B.
        Tidal forcing of enterococci at marine recreational beaches at fortnightly and semidiurnal frequencies.
        Environ Sci Technol. 2005; 39: 5575-5583
        • Olyphant G.A.
        • Thomas J.
        • Whitman R.L.
        • Harper D.
        Characterization and statistical modeling of bacterial (Escherichia coli) outflows from watersheds that discharge into southern Lake Michigan.
        Environ Monit Assess. 2003; 81: 289-300
        • Scott T.M.
        • Rose J.B.
        • Jenkins T.M.
        • Farrah S.R.
        • Lukasik J.
        Microbial source tracking: current methodology and future directions.
        Appl Environ Microbiol. 2002; 68: 5796-5803
        • Bernhard A.E.
        • Field K.G.
        Identification of nonpoint sources of fecal pollution in coastal waters by using host-specific 16S ribosomal DNA genetic markers from fecal anaerobes.
        Appl Environ Microbiol. 2000; 66: 1587-1594
        • Scott T.M.
        • Jenkins T.M.
        • Lukasik J.
        • Rose J.B.
        Potential use of a host associated molecular marker in Enterococcus faecium as an index of human fecal pollution.
        Environ Sci Technol. 2005; 39: 283-287
        • Ufnar J.A.
        • Wang S.Y.
        • Christiansen J.M.
        • Yampara-Iquise H.
        • Carson C.A.
        • Ellender R.D.
        Detection of the nifH gene of Methanobrevibacter smithii: a potential tool to identify sewage pollution in recreational waters.
        J Appl Microbiol. 2006; 101: 44-52
        • Whitman R.L.
        • Nevers M.B.
        • Korinek G.C.
        • Byappanahalli M.N.
        Solar and temporal effects on Escherichia coli concentration at a Lake Michigan swimming beach.
        Appl Environ Microbiol. 2004; 70: 4276-4285
        • Rose J.B.
        • Epstein P.R.
        • Lipp E.K.
        • Sherman B.H.
        • Bernard S.M.
        • Patz J.A.
        Climate variability and change in the United States: potential impacts on water- and foodborne diseases caused by microbiologic agents.
        Environ Health Perspect. 2001; 109: S:211-S:221
        • Santo Domingo J.W.
        • Bambic D.G.
        • Edge T.A.
        • Wuertz S.
        Quo vadis source tracking?.
        Water Res. 2007; 41: 3539-3552
        • Savichtcheva O.
        • Okabe S.
        Alternative indicators of fecal pollution: relations with pathogens and conventional indicators, current methodologies for direct pathogen monitoring and future application perspectives.
        Water Res. 2006; 40: 2463-2476
        • Bower P.A.
        • Scopel C.O.
        • Jensen E.T.
        • Depas M.M.
        • McLellan S.L.
        Detection of genetic markers of fecal indicator bacteria in Lake Michigan and determination of their relationship to Escherichia coli densities using standard microbiological methods.
        Appl Environ Microbiol. 2005; 71: 8305-8313
        • Brownell M.J.
        • Harwood V.J.
        • Kurz R.C.
        • McQuaig S.M.
        • Lukasik J.
        • Scott T.M.
        Confirmation of putative stormwater impact on water quality at a Florida beach by microbial source tracking methods and structure of indicator organism populations.
        Water Res. 2007; 41: 3747-3757
        • Santoro A.E.
        • Boehm A.B.
        Frequent occurrence of the human-specific Bacteroides fecal marker at an open coast marine beach: relationship to waves, tides and traditional indicators.
        Environ Microbiol. 2007; 9: 2038-2049
        • Bruesch M.E.
        • Biedrzycki P.A.
        Preliminary comparative analysis of two models used to predict E. coli levels in recreational water in Milwaukee.
        (Great Lakes Beach Conference, Oct 3)2002
        • Kuntz J.E.
        • Murray R.
        Non-point source of bacteria at the beach.
        Laboratory HD, Stamford CT1996
        • Nevers M.B.
        • Whitman R.L.
        • Frick W.E.
        • Ge Z.
        Interaction and influence of two creeks on Escherichia coli concentrations of nearby beaches: exploration of predictability and mechanisms.
        J Environ Qual. 2007; 36: 1338-1345
        • Crowther J.
        • Kay D.
        • Wyer M.D.
        Relationships between microbial water quality and environmental conditions in coastal recreational waters: the Fylde coast UK.
        Water Res. 2001; 35: 4029-4038