Marine Recreation and Public Health Microbiology: Quest for the Ideal Indicator

A Human Being; An Ingenious Assembly of Portable Plumbing. —Christopher Morley, Human Being Four-fifths of the population of the United States live in close proximity to the oceans or Great Lakes, and approximately 100 million Americans use the marine environment for recreation each year (Thurman 1994). Consequently, contamination of lakes, rivers, and coastal waters raises significant public health issues. Among the leading sources of chemical and biological contamination of these waters and associated beaches are sewer systems, septic tanks, stormwater runoff, industrial wastes, wastewater injection wells, cesspits, animal wastes, commercial and private boat wastes, and human recreation. In 1997, 649 beach closings or advisories were caused by sewage spills and overflows (NRDC 1998). In Florida alone, approximately 500 million gallons of sewage were released along the coast each year during the late 1980s (Neshyba 1987). Thus one of the primary concerns in public health is the risk that humans using the marine environment for recreational activities will encounter microbial pathogens. The risk to human health due to recreational exposure—swimming where sewage contaminates marine waters, for example—has been documented (Cabelli 1983, Rees et al. 1998). Studies conducted along beaches in Hong Kong reported that swimmers were at higher risk of gastrointestinal and respiratory illness and eye, ear, and skin infections than nonswimmers; not surprisingly, these risks were greatest at beaches known to be polluted (Cheung et al. 1990). Cheung and colleagues estimated that in 1990, approximately 58,000 episodes of illness in Hong Kong were the result of swimming at a single beach contaminated by sewage. In Great Britain, Alexander and colleagues (1992) concluded that children who swam in contaminated marine waters were more likely than those who did not to develop symptoms of illness. People who engage in other recreational activities, such as windsurfing, also face health risks in marine waters contaminated with human waste (Dewailly et al. 1986). Although it is clear that those who use polluted marine waters for recreation have a higher risk of developing microbial disease than those who do not, no universal measurement of pollution in marine environments that reflects public health risk has been defined. For over 50 years the method of choice has been microbiological analysis of water samples using the “indicator concept.” The historical indicator concept, originally defined to assess drinking water quality, is based on the presence or absence of bacteria or groups of bacteria in a given body of water. The historical characteristics of the ideal water quality indicator are listed in the box on page 818. These indicator bacteria are typically found in the intestines of animals and humans and are shed in feces. The indicator itself is not a pathogen, but its presence indicates the probable presence of pathogenic organisms. The box on this page lists the groups of bacteria that are currently used as indicators in the United States. Water quality is based on the numbers of these microbes in a given water volume. The microbes are counted through a media-based assay, in which certain nutrients and chemicals are used to identify specific species of live or colony-forming units (CFUs) of bacteria in the water sample. Concentration limits—that is, the maximum numbers of a species or group of bacteria—per sample volume were determined through epidemiological studies demonstrating a risk of illness when the limit was met or exceeded; in most cases, concentration is based on the number of CFUs per 100 milliliters of water. Researchers have reported a dose-response relationship between the level of indicator organisms in recreational marine waters and the risk of illness (Cabelli 1983, Fliesher et al. 1996). Originally, counts of both total and fecal coliforms were made to determine water quality, with intestinal bacteria groups such as the enterococci and species of Clostridium adopted in recent years as alternate indicators. Nonetheless, no microbial indicator has yet been identified that can be used effectively in all regions; for example, in the tropics, coliforms that are deposited in soils may survive in substrates, and thus their presence may not mean that fecal wastes are continuously entering the tested area. A nationwide consensus among public health officials and researchers on which bacterial indicator to use in monitoring recreational water quality has not yet been reached. Table 1 lists the pros and cons of the current indicator bacteria. For accurate assessments of the level of water quality and risk to public health, an indicator or suite of indicators that can be used to determine water quality in any setting must be identified, as must a detection assay that is both sensitive and specific—that is, one that can reliably ascertain low numbers of a target species. Water quality research conducted at the Massachusetts State Board of Health and Massachusetts Institute of Technology in the late 19th century had a significant influence on water quality microbiology (Winslow 1923). For example, research by Theodor Escherich identified coliform bacteria (Escherichia coli) as markers of fecal pollution (Wolf 1972). Continued research in the field of public health and water microbiology resulted in the publication in 1909 of the American Public Health Association's Standard Methods for the Examination of Water and Wastewater (Wolf 1972), a seminal work now in its 20th edition. The use of coliform bacteria as an indicator of fecal pollution has been a mainstay in the field ever since. The coliform group of bacteria (total coliforms) “comprises all aerobic and facultative anaerobic, gram-negative, nonspore-forming, rod-shaped bacteria that ferment lactose with gas and acid formation within 48 hours at 35.0°C” (Clesceri et al. 1998). Fecal coliforms, which originate from the intestines of warm-blooded animals, are distinguished from total coliforms by their ability to grow at elevated temperatures (44.5°C). Because many pathogenic organisms are fecal–oral pathogens, meaning that they enter the host via ingestion of contaminated food or water and are shed in the feces, the fecal coliforms are better indicators of contamination than the total coliforms. Moreover, the ability of fecal coliforms to withstand high temperatures, such as those found in shallow marine waters, presumably makes them better indicators than total coliforms in marine waters. All of these microbes (total and fecal coliforms) are used to monitor both drinking water, fresh water, and marine recreational waters. Using bacterial indicators to assess water quality poses several problems, however. For example, the use of fecal coliforms as an indicator of microbial water quality in tropical waters has been questioned (Hazen and Toranzos 1990) because such bacteria survive in sediments and can be found in areas far removed from human activity. Additionally, media-based assays cannot distinguish the source of origin (animal versus human), and the correlation between coliform and human pathogen concentrations has not been established over a wide range of sample locations. Another problem is that many of the media-based detection methods are subject to false positive results. In the marine environment, many indigenous populations of bacteria such as Pseudomonas and Vibrio can grow and mimic the coliforms (that is, they exhibit the same color as coliforms in media-based tests that rely on the color of the colonies to identify the type of bacteria present; see Figure 1). Researchers have demonstrated that, in Hawaii, fecal coliforms deposited in soils may survive on substrates. These surviving populations of coliforms can then be transported to bodies of water via groundwater. Thus, their presence in the water column does not indicate that fresh fecal wastes are polluting the region (Hardina and Fujioka 1991). Laboratory studies in which the coliform E. coli was inoculated into marine water samples have demonstrated survival periods as long as 3 years (Byrd and Colwell 1993). And although historically coliforms were thought to be quickly inactivated once introduced into the marine environment, some research has demonstrated their short-term survival in marine waters (Garcia-Lara et al. 1991). This difference in survival rates noted by different researchers creates a dilemma: Low or high numbers of coliform bacteria found in the water column may or may not indicate good or poor water quality. As early as the 1980s, the US Environmental Protection Agency (USEPA) recommended the use of enterococci for monitoring marine microbial water quality. Research indicates that enterococci (a subgroup of the fecal streptococcus group of bacteria) are a more accurate indicator than coliforms because they are more closely associated with human rather than with animal fecal matter and survive longer in aquatic environments (Cabelli 1983). Nevertheless, although enterococci may be a better indicator than coliforms in marine environments, this indicator too can be found in tropical soils not in close association to human activity (Hardina and Fujioka 1991). Thus, two of the problems associated with using coliforms apply also to the use of enterococci as a water quality indicator: Do high numbers or presence in samples indicate water pollution and risks to human health, and what was the source of origin (animal versus human)? In a study of water quality in Homosassa, Florida, higher numbers of enterococci (1380 CFU per 100 ml) were found in a wildlife park than were found in residential areas with canals where homes utilized septic tanks for waste disposal (Griffin et al. 2000). The enterococci guidance level for marine waters is a geometric mean of 35 CFU per 100 ml for five samples taken over a 30-day period and a single sample density of 104 enterococci CFU per 100 ml (Dufour et al. 1986, USEPA 1997). Another bacterial indicator that is currently being used to assess water quality is Clostridium perfringens. Clostridium perfringens is a gram-positive, anaerobic spore-forming, rod-shaped bacterium that is typically found in soils and in the intestines of animals. Fujioka and Shizumura (1985) have suggested that C. perfringens is a better indicator than coliforms and enterococci bacteria for tropical waters because it is a spore-forming organism and thus survives longer in marine environments (limits are 50 CFU per 100 ml for inland waters and 5 CFU per 100 ml for marine waters). The spore is an egglike vesicle that limits the inactivation potential of physical stresses such as heat, desiccation, and ultraviolet light. This species of bacteria, like some species of coliforms (E. coli 0157:H7 is an example) is a potential pathogen. Despite the current state of knowledge in regard to the limitations of coliform use in assessing marine water quality, 16 states and three territories, including Florida and the US Virgin Islands, both located in the tropics, still use only coliforms as a marine water quality indicator (Table 2; USEPA 1998). Only seven states and three territories or trusts have adopted enterococci as a marine water quality indicator (USEPA 1998). Hawaii is the only state that utilizes C. perfringens as an indicator; Hawaii's indicator limits for marine waters are the most stringent of all (7 enterococci CFU per 100 ml and 5 C. perfringens CFU per 100 ml). States may set their own bacteriological limits for coliform and enterococci standards, and a number of states have set their limits above or below USEPA recommendations. There is a nationwide lack of uniformity regarding microbiological indicator type, limits, and monitoring area and frequency (that is, how many beaches will be monitored and how often) (NRDC 1998). Many states monitor only a limited number of their beaches; some do not monitor at all; and those few that do monitor frequently (eight states, most of them in the Northeast) have no uniform method of alerting the public or closing beaches when limits are exceeded (NRDC 1998). The lack of uniformity in monitoring marine public health is partially caused by the absence of consensus on what constitutes a good microbiological indicator of water quality and inadequate strategies for monitoring recreational waters. Also of concern are indigenous microbial pathogens such as Vibrio vulnificus, whose presence and densities do not correlate with the current fecal indicators. Clearly, there is a need to adopt a more accurate water quality indicator or suite of indicators and to develop new detection methods that are both specific and sensitive. “There are always alternatives.” —Spock (Star Trek, “The Galileo Seven”) Concern over the risk that indigenous populations of bacteria pose to bathers is growing. In particular, V. vulnificus has been associated with a variety of infections (Lamaury et al. 1997). Colonization of skin wounds is the primary mode of infection, and the resulting disease can be fatal (Kueh et al. 1992). Vibrio vulnificus occurs throughout the world in warm, moderately saline water. In the Chesapeake Bay, V. vulnificus was 0.6% to 17.4% of the total bacterial population in warm months (Wright et al. 1996). Even as far north as Canada (Prince Edward Island), New Hampshire, and Maine, V. vulnificus has been isolated from water, fish, and shellfish (Hariharan et al. 1995, O'Neill et al. 1990). Alabama, Florida, Louisiana, Texas, and Mississippi, all of which border the Gulf of Mexico, currently report V. vulnificus infections to the Centers for Disease Control (CDC 1996). Another Vibrio species that can cause wound infections is V. parahaemolyticus. Like V. vulnificus, it occurs throughout the world in moderately saline waters. Its highest concentrations occur during the summer, when the majority of infections are caused by eating undercooked seafood (CDC 2000). Infections are usually self-limiting, but this organism can cause severe disease (CDC 2000). New methods and media, including molecular techniques using polymerase chain reaction, are now available for sensitive and specific detection of V. vulnificus in seawater (Aono et al. 1997, Hoi 1998). Molecular techniques are showing promise in their ability to differentiate sources of isolated bacteria (Sinton et al. 1998). Antibiotic resistance patterns have been used to differentiate fecal streptococci isolates from aquatic environments by origin (either human or animal), with an accuracy rate of up to 95% (Wiggins 1996, Hagedorn et al. 1999). Multiple antibiotic resistance profiles have been used to accurately differentiate sources of E. coli (Parveen et al. 1997). Researchers have also used antibiotic resistance patterns of streptococci and fecal coliforms to successfully distinguish the origin of isolates (Harwood et al. 2000). A group of viruses that may serve as an alternate to the coliform indicators are the bacteriophages (viruses that infect only bacteria, and in most cases only a specific species of bacteria). A number of bacteriophages have shown promise as a primary indicator of water quality. One such group of bacteriophages are the F+-specific RNA coliphages. The coliphages utilize E. coli, which can produce pili (F+E. coli), as a host. The coliphages use the pili (appendages that the bacteria produce for attachment purposes) as a site for attachment to the bacteria. Hsu et al. (1995) developed a protocol that genotypes F+-specific RNA coliphages via four group-specific oligonucleotide (synthetic genetic) probes. These coliphages are classified based on which probe hybridizes with their respective acid and have been identified as isolates from animals. isolates are associated with human and feces. isolates are associated with human feces. In areas by fecal waste sources and animal wastewater were found to be the of F+-specific coliphages to and marine waters et al. 1998). have used the specific assay to determine fecal sources and water quality in Florida (Griffin et al. 2000). of microbiological indicators that and in some cases the were more indicators of fecal pollution than coliform indicators et al. 1996). The is an anaerobic bacterium found in the intestinal of humans and other Researchers found that numbers of bacteriophages in different water have from seven units per 100 ml to as high as per 100 ml in polluted water, per 100 in and per 100 ml in et al. 1996). bacteriophages no in the environment and demonstrated rates to human and and et al. 1995, et al. 1998). The of bacteriophages in seawater is to A and a significant correlation has been shown between the presence of and the presence of viruses or et al. and 1995, 1996, et al. 1998). was also found that the of to in sediments was to the found in that the of both may be in the environment et al. Additionally, bacteriophages were shown to be more to than bacteria such as and some et al. 1995, Research conducted in that a assay was to the assay because the are more from the environment and the assay is to et al. 1997). have also been used as biological in marine environments to study potential sources of fecal such as septic tanks and wastewater injection In Florida, from a septic into the marine environment within hours et al. A study conducted in the demonstrated an of from a injection into the and a to waters located on the of the et al. The of these of studies is that specific sources of pollution can be A biological such as the a chemical or an accurate of how organisms from a source into the Additionally, the from studies can be used for which can be used by public health to determine the of pollution and public health risk associated with recreational use of waters close to septic tanks, injection wells, or other potential sources of for human viruses in water has been the studies used techniques to determine the of the viruses in sewage. a assay, a water sample is to a of and the sample is then monitored over a period of to determine live viruses are viruses are the result is of within the or in The to this method is that it of to some viruses can infect and in or in and do not for all known human pathogens. For example, or which are for a number of of shellfish cannot be in et al. 1995, 1997, et al. et al. 1998). chain and assays were used to assess water quality for the RNA viruses et al. Fliesher et al. 1996, et al. 1997, et al. 1998). An for the is an Figure A single of a specific can be to of in A assay specific will only the organism of and sensitive can low numbers of the detection of the organism of The of this assay is that it only the organism is not it is which that it is to the organism cause an The of a assay with a assay, does the detection of viruses et al. 1997). Using an assay, in Florida at the of septic tanks on water quality of A and and In a study of and water quality in Florida, and assays in and of the et al. In a study in the Florida 95% of the samples were positive for the presence of human pathogenic viruses (Griffin et al. 1999). tanks were determined to be the primary source of Figure 3 that human viruses were at a majority of no site was in of the coliform and only three were in of the enterococci of these studies demonstrated a in two in In were at the of human wastes at a majority of the same bacterial indicator C. suggested good water quality. molecular and methods were used to study the microbiological risk to swimmers at beaches in Hawaii et al. 1996). was found that and of the samples from three different beaches were in of the state for enterococci (7 CFU per 100 of samples and of the and were at these same were used to maximum risks of infections per 100 swimmers for viruses and infections per swimmers for the et al. 1996). most of the assays have shown good with detection limits as low as one for a given volume of sample volume of the sample on the concentration and acid research has demonstrated of human viruses in waters the influence of human fecal wastes that these organisms may be used as indicators in any aquatic Table 3 new that may be in monitoring marine water samples for a variety of pathogens and indicators. the limitations of the current microbiological indicator and researchers have recommended that be to better public health in coastal waters USEPA 1999). is the need for monitoring and in both the water column and sediments for several of indicators and pathogens in with or research that monitor bodies of water for indicators and pathogens in indigenous of indicator organisms and the for a given assessments are for the and survival of indicator and pathogenic organisms. such can be used to develop both and to when high of organisms may be In association with new methods that do not rely on must be in the detection of indicators and pathogens. these methods may have the potential to be used as in to contamination in 1999). at the the of physical and more than the microbial indicator at human to a wide variety of coliforms at 48 Fecal coliforms at 48 within the total coliform such as coli, which have for at intestinal temperatures at 48 of bacteria such as Clostridium perfringens anaerobic bacterium that at where pathogens do grow in the environment to than are pathogens to and be isolated from all of water subject to Only found in sewage in higher numbers than pathogens of indicator to of contamination of indicator to a health or type of pollution detection of indicator bacteria chain of coliform indicators versus human pathogenic viruses in canals and waters of the Florida total coliform and fecal coliform to the concentration in each indicate the maximum limits for the respective coliform coliforms were isolated at the at site 16 and cons of the current indicators (total and fecal coliforms, and Clostridium and indicator and cons of the current indicators (total and fecal coliforms, and Clostridium and indicator water quality indicators for US states and territories water quality indicators for US states and territories of marine using new of marine using new

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