Guidelines for Canadian recreational water quality: Microbiological pathogens and biological hazards: Pathogenic microorganisms
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- 2.0 Pathogenic microorganisms
- 2.1 Enteric bacterial pathogens
- 2.2 Naturally occurring pathogenic bacteria
- 2.3 Other pathogenic bacteria
- 2.4 Enteric viral pathogens
- 2.5 Enteric protozoan pathogens
- 2.6 Free-living protozoa
2.0 Pathogenic microorganisms
Numerous pathogenic microorganisms can potentially be found in recreational environments. The three main types are bacteria, viruses and protozoa. Many occur as a result of contamination from human or animal wastes, whereas some are free-living microorganisms that exist naturally in the recreational water environment. A fourth type that may be of concern at some beaches, particularly associated with beach sand, are fungi. It should be noted, however, that research to characterize the potential risks from fungi is ongoing.
Enteric pathogens are considered to pose the highest infectious disease risk to human health from recreational water exposures. The principal route of entry for human-infectious enteric pathogens in recreational waters is sewage-contaminated wastes (WHO, 2021). Point sources of pollution such as municipal sewage discharges or combined sewer overflows are the primary sources of sewage contamination. Non-point sources that may contribute to fecal loads in environmental waters include storm drains, river discharges (which capture runoff from urban and rural areas), and malfunctioning or improperly designed septic waste systems. Swimmers themselves, particularly young children, may contribute to contamination through fecal shedding and the accidental release of fecal material. Animal wastes, although capable of harbouring many bacterial and protozoan pathogens, are considered to be of low risk for the transmission of enteric viruses to humans (Cliver and Moe, 2004; Percival et al., 2004; Wong et al., 2012; Health Canada, 2019a).
2.1 Enteric bacterial pathogens
Enteric pathogenic bacteria occur in recreational waters as a result of contamination by human or animal fecal wastes. Transmission occurs via the fecal-oral route, through accidental ingestion of contaminated waters. Gastrointestinal symptoms are the most common manifestation of illness following infection with enteric bacterial pathogens, although some pathogens can cause illness with more severe outcomes. E. coli and enterococci are the primary indicator organisms used to indicate the potential risk of enteric illness (Health Canada, in publication-b) from enteric pathogenic bacteria.
Campylobacter bacteria are Gram-negative, motile, non-spore-forming, spiral, curved or S-shaped rods. They are thermophilic (growing optimally at 42°C and incapable of growth below 30°C) and microaerophilic (surviving best under partially anaerobic conditions) organisms. The genus Campylobacter (Class: Epsilonproteobacteria) is composed of over 30 species (LPSN, 2019); however, C. jejuni and C. coli are the major species of human concern in the water environment.
Campylobacter are predominantly considered to be zoonotic pathogens (Fricker, 2006) but can also be transmitted through human fecal wastes. They are part of the normal intestinal flora of a wide range of domestic (e.g., poultry, cattle, sheep, pets) and wild animals, particularly waterfowl (Moore et al., 2002; Pond, 2005; Fricker, 2006; Wagenaar et al., 2015; Backert et al., 2017). Important sources of fecal contamination include surface runoff contaminated with livestock waste or feces from wild animals (e.g., waterfowl), direct deposition from waterfowl (e.g., gulls and geese) overnighting on water bodies, and human sewage sources.
Symptoms of Campylobacter enteritis include a profuse, watery diarrhea (with or without blood), cramps, abdominal pain, chills, and fever. The incubation period is generally between 1 and 5 days and illness is typically self-limiting, requiring up to 10 days for recovery (Backert et al., 2017). Asymptomatic infections (those in which symptoms of disease are not exhibited) with Campylobacter spp. are also possible (Percival and Williams, 2014b). Dose-response information for Campylobacter infection and illness is not fully understood (Teunis et al., 2005; 2018). A high probability of infection and illness was found at doses of 500 to 800 C. jejuni in a human feeding study (Medema et al., 1996). Information from a foodborne outbreak suggests that the infectious dose may be even lower for certain strains or for children (Teunis et al., 2005; 2018). Some severe infections may lead to hospitalization and can be life-threatening, but fatalities are uncommon and are usually restricted to infants, the elderly or patients with other underlying illnesses (Pond, 2005).
Certain post-infection complications have been associated with Campylobacter enteritis, including Guillain-Barré syndrome and reactive arthritis; however, these are considered rare. Evidence also suggests that Campylobacter infection may be associated with the development of inflammatory bowel diseases such as Crohn’s disease, ulcerative colitis and irritable bowel syndrome (Backert et al., 2017; Huang et al., 2015).
Despite the fact that Campylobacter spp. have been widely isolated from surface waters in North America (Hellein et al., 2011; Khan et al., 2013a,b; Oster et al., 2014; Guy et al., 2018), there have been few recorded outbreaks of Campylobacter-associated illness as a result of recreational water activity. Between 2000 and 2014, Campylobacter spp. were implicated as the sole causative agent in one recreational water outbreak of gastroenteritis in the United States, as well as one outbreak where multiple pathogens were involved (Graciaa et al., 2018). Outbreaks have also been linked to drinking water (Health Canada, 2022). No outbreaks of campylobacteriosis have been identified in Canada related to recreational waters. Cases of campylobacteriosis in Canada and abroad are mostly sporadic, with most illnesses linked to consumption of contaminated food (Huang et al., 2015; Wagenaar et al., 2015; Pintar et al., 2017). However, recreational water contact is a potential exposure risk (Denno et al., 2009; Pintar et al., 2017; Ravel et al., 2017) and has been linked to sporadic cases internationally (Schönberg-Norio et al., 2004).
2.1.2 Pathogenic E. coli / Shigella
E. coli (genus Escherichia; Family: Enterobacteriaceae; Class: Gammaproteobacteria) are Gram-negative, motile or non-motile, facultatively anaerobic, non-spore-forming rod-shaped bacteria that are natural inhabitants of the intestinal tract of humans and animals. They can grow over a broad temperature range (7°C to 45°C), with optimal growth at 37°C (Ishii and Sadowsky, 2008; Percival and Williams, 2014c). The vast majority of E. coli strains are harmless; however, several serotypes or strains possess virulence factors enabling them to act as human pathogens. Pathogenic enteric strains can be separated into six groups according to their serological or virulence characteristics: enterohemorrhagic E. coli (EHEC), enterotoxigenic E. coli (ETEC), enteroinvasive E. coli (EIEC), enteropathogenic E. coli (EPEC), enteroaggregative E. coli (EAEC), and diffusely adherent E. coli (DAEC) (Croxen et al., 2013; Percival and Williams, 2014c). Some E. coli strains, such as uropathogenic E. coli (UPEC), can also cause extra-intestinal infections (Abe et al., 2008).
Advanced molecular typing and sequencing analyses have demonstrated that Shigella are also members of the EIEC pathotype (Croxen et al., 2013; Robins-Browne et al., 2016). The genus name Shigella and the disease name shigellosis (i.e., disease caused by Shigella spp.) are still used for historical purposes (Croxen et al., 2013). Shigella has traditionally been composed of four species: S. sonnei (1 serotype), S. flexneri (6 serotypes), S. boydii (15 serotypes) and S. dysenteriae (10 known serotypes). Two species, S. sonnei and S. flexneri, account for the vast majority of Shigella-associated illness in North America (CDC, 2005a), representing 95% of reported Shigella cases in Canada (Government of Canada, 2020). Other Shigella species are uncommon but remain important causes of disease in developing countries (CDC, 2005a).
The main sources of pathogenic E. coli vary between E. coli groups. EHEC are zoonotic pathogens, and cattle are considered the primary reservoir with human waste also recognized as an important source (Croxen et al., 2013; Percival and Williams, 2014c). For the remaining major pathogenic E. coli groups, including Shigella, human sewage is the principal source of contamination. In recreational waters, sources of human sewage may include obvious sources such as municipal sewage discharges as well as less obvious sources, such as fecal shedding by infected swimmers (Kramer et al., 1996; Levy et al., 1998). As EHEC are zoonotic pathogens, surface runoff contaminated with livestock waste is an important source of fecal contamination. E. coli that have been linked to extra-intestinal infections are usually strains that are part of the commensal flora of the human intestines, but cause adverse health impacts when they are deposited in non-intestinal systems, such as in the urinary tract (Shah, 2019).
Enteric pathogenic E. coli/Shigella cause diseases that range in severity from mild and self-limiting to severe and life-threatening depending on the group and strain involved. The main symptoms are watery or bloody diarrhea, accompanied by abdominal pain and fever. The incubation period ranges from 1 to 3 days, with the duration of infection lasting from 1 to 2 weeks (Percival and Williams, 2014c, 2014g). In most cases, diarrheal infections are self-limiting. Treatment generally involves oral rehydration to maintain fluid and electrolyte balance. With some infections, individuals can become asymptomatic carriers capable of shedding the organisms in their feces for weeks to months after infection (Croxen et al., 2013; Percival and Williams, 2014c, 2014g). Extra-intestinal E. coli, such as UPEC, are associated with urinary tract infections.
Some infections can progress to more serious and potentially life-threatening conditions. S. dysenteriae serotype 1, which produces Shiga toxin, is a major cause of dysentery in developing countries, but is uncommon in North America. EHEC (synonyms: shiga toxin-producing Escherichia coli/STEC and verotoxin-producing Escherichia coli/VTEC) also has the ability to produce Shiga-like toxins similar to those produced by S. dysenteriae. E. coli O157:H7 is the most prevalent EHEC serotype. EHEC infection causes haemorrhagic colitis, marked by grossly bloody diarrhea, severe cramping and abdominal pain with a general lack of fever. An estimated 4% to 17% of all cases of EHEC infection progress to what is known as hemolytic uremic syndrome (HUS)—a life-threatening condition involving large-scale destruction of red blood cells and kidney failure (Croxen et al., 2013; Keithlin et al., 2014). Children, the elderly and immunocompromised persons are at increased risk for developing HUS.
The dose of pathogenic E. coli/Shigella that is required to cause infection is estimated to range from less than 100 to 1,000 organisms for EHEC and EIEC/Shigella to greater than 1 million to 10 billion organisms for the other groups (Kothary and Babu, 2001; Croxen et al., 2013; Percival and Williams, 2014c, 2014g).
EHEC and Shigella are among the leading causes of bacterial gastrointestinal illness in Canada, the United States and Europe and are frequently related to food and travel-related exposures in North America (Health Canada, 2022a). They are also the members of the pathogenic E.coli /Shigella group most often implicated in illness associated with recreational waters. According to surveillance data published by the United States Centers for Disease Control and Prevention (US CDC) for 2000 to 2014, pathogenic E. coli were associated with 14% (19 out of 140) and Shigella with 10% (14 out of 140) of the total number of outbreaks of gastrointestinal illness reported for natural waters (Graciaa et al., 2018; CDC, 2020). Outbreaks have also been associated with drinking water (Health Canada, 2022). The majority of the E. coli related outbreaks were caused by E. coli O157:H7. The majority of Shigella-related outbreaks were linked to S. sonnei.
In Canada, very few E. coli / Shigella related outbreaks associated with recreational waters have been recorded to date. In August 2001, an outbreak of E. coli O157:H7-associated illness involving four children was linked to swimming at a public beach in Montreal (Bruneau et al., 2004). Weekly water samples collected around the time of the outbreak were shown to be within the recreational water quality limits specified by the Province of Quebec. It was suggested that a high swimmer population and the shallow depth of water encountered in the swimming area contributed to the transmission of the organisms. More recently, in September of 2020, seven confirmed cases of E. coli infection were linked to a swimming area of a conservation area. Most cases were reported in individuals under the age of 12 (City of Hamilton, 2020).
Salmonella are Gram-negative, facultatively anaerobic, motile, non-spore-forming rods that grow at temperatures from 5°C to 47°C, with optimum growth between 35°C and 37°C (Graziani et al., 2017). The genus Salmonella (Family: Enterobacteriaceae; Class: Gammaproteobacteria) is comprised of two species: S. enterica and S. bongori (Percival et al., 2004). S. enterica is further subdivided into six subspecies (S. enterica subsp.): enterica, salamae, arizonae, diarizonae, houtenae, and indica, and contains over 2,500 serotypes (Percival and Williams, 2014f; Andino and Hanning, 2015). The majority of the serotypes encountered in cases of human gastroenteritis belong to the subspecies S. enterica subsp. enterica (Lightfoot, 2004). When referring to Salmonella, it is common to use the serotype name in place of the species name. Thus, S. enteric serotype Enteritidis is used instead of S. enterica subsp. enterica serovar Enteritidis.
Salmonella bacteria of human importance are divided into two main groups according to the type of disease they cause. The typhoidal Salmonella (S. enterica serotype Typhi and S. enterica serotype Paratyphi) are the causative agents of enteric fever, a serious and life-threatening illness (Sanchez-Vargas et al., 2011). Humans are the only known source of the typhoidal Salmonella species (Percival and Williams, 2014f). The non-typhoidal Salmonella are a large group containing the rest of the S. enterica serotypes which cause gastrointestinal illness of varying severity (Sanchez-Vargas et al., 2011). Non-typhoidal Salmonella are considered zoonotic pathogens. Poultry, swine, birds, cattle, rodents, tortoises and turtles, dogs and cats can act as a reservoir for these bacteria (Percival et al., 2004; Graziani et al., 2017). Humans recovering from illness can be a source of Salmonella, and asymptomatic infections among humans are possible.
Gastroenteritis is by far the most commonly encountered Salmonella-associated illness. The main symptoms of non-typhoidal Salmonella are mild to severe diarrhea, nausea and vomiting. Symptoms usually appear between 12 and 72 hours from the time of infection, but this time lag may be reduced in cases where large quantities of cells have been consumed (Percival and Williams, 2014f). Illness is generally mild and self-limiting, lasting 4 to 7 days on average; however, long-term complications (reactive arthritis, irritable bowel syndrome) can occur in approximately 3% to 6% of cases (Keithlin et al., 2015). Treatment for infections with non-typhoidal Salmonella involves fluid and electrolyte replacement, with antibiotics only prescribed in severe cases. Some Salmonella have shown resistance to antibiotics. The Public Health Agency of Canada, the US CDC, and the World Health Organization have categorized non-typhoidal Salmonella resistant to ciprofloxacin, ceftriaxone or multiple classes (e.g., >3) of drugs as public health threats of serious to critical importance (CDC 2013a; WHO, 2017, PHAC, 2018). Reports on the infectivity of Salmonella have suggested that the median dose for the non-typhoidal species may range from less than 100 organisms to a high of 100,000 to 10 billion organisms (Hunter, 1997; Pond, 2005; Kothary and Babu, 2001).
Enteric fever (typhoid or paratyphoid fever) is a more severe and often fatal form of salmonellosis caused by S. serotype Typhi and S. serotype Paratyphi. Symptoms of the illness are prolonged high fever, vomiting, headaches, and numerous potentially fatal complications (Sanchez-Vargas et al., 2011). Waterborne outbreaks of enteric fever are more prevalent in developing countries where crowded living conditions and poor hygiene practices exist and are often associated with improperly treated drinking water supplies. Cases of enteric fever are rare in North America.
Salmonella is the second-leading cause of bacterial gastrointestinal illness in Canada with most cases being sporadic or associated with consumption of contaminated food (Health Canada, 2022a). Although Salmonella has been isolated from surface waters (Levantesi et al., 2012; Jokinen et al., 2015; Kadykalo et al., 2020), US CDC surveillance data for 1992 to 2014 indicate that Salmonella was not cited as a causative agent for any of the recreational waterborne outbreaks of gastroenteritis reported over that period (Garciaa et al., 2018; CDC, 2020). There have also been no documented Salmonella-associated outbreaks in Canadian recreational waters.
2.2 Naturally occurring pathogenic bacteria
Naturally occurring pathogenic bacteria are free-living microorganisms that are found in water environments. Unlike many enteric pathogens, they can thrive in the natural environment under favourable conditions. If these organisms are present in high enough numbers in a body of water, they may be transmitted to humans through inhalation, ingestion, or direct body contact with water, depending on the organism. These naturally occurring pathogenic bacteria are diverse, causing a range of illnesses including gastrointestinal and respiratory illnesses and infections of the eyes, ears or skin. As these organisms are not enteric pathogens, fecal indicators are not expected to correlate well with their presence. There is no recognized microbiological indicator for these pathogens.
Legionella are Gram-negative, thermotolerant, motile, short, rod-shaped bacteria that have strict nutrient requirements when grown in culture. The genus Legionella (Family: Legionellaceae; Class: Gammaproteobacteria) contains 61 species and 3 subspecies (LPSN, 2019). L. pneumophila (serotype 1) is the species most frequently associated with human disease (legionellosis). It is suspected that all Legionella species may be capable of causing illness, and at least 30 of the identified species have been implicated in human disease (Hall, 2006).
Legionella bacteria have two habitats—a primary reservoir in the natural environment and a secondary habitat in engineered water systems (NASEM, 2020). In the natural environment, Legionella occur in freshwater systems. They grow at temperatures between 25°C and 45°C (optimum range is 25°C to 35°C) but can survive at much higher temperatures (up to 70°C) (Allegra et al., 2008; Cervero-Aragó, 2015; 2019). They can be isolated from a wide range of freshwater habitats, including sediments, lakes, rivers, and natural thermal pools at temperatures as high as 60°C (Percival and Williams, 2014d; Burillo et al., 2017; NASEM, 2020). Marine environments typically do not provide appropriate growth conditions for these organisms. Free-living freshwater protozoa such as Naegleria or Acanthamoeba are natural hosts for Legionella, providing a protective environment against adverse conditions (such as elevated temperatures), along with nutrients and a means of transport (Thomas and Ashbolt, 2011; Bartrand et al., 2014; Percival and Williams, 2014e; Siddiqui et al., 2016; NASEM, 2020). Passage in free-living protozoa may also increase the virulence of amoebae-resisting microorganisms, such as Legionella (Visvesvara et al., 2007; Thomas and Ashbolt, 2011; Chalmers, 2014a). Human and animal feces are not considered a source of Legionella, although the organism can be detected in the feces of infected individuals experiencing diarrhea symptoms. Animals can be infected by Legionella, but zoonotic transmission of the organism has not been documented (Surman-Lee et al., 2007; Edelstein and Roy, 2015).
Legionella are typically encountered in low numbers in the aquatic environment. A review of outbreaks linked to recreational waters (including treated and natural waters) concluded that the risk related to natural rivers and lakes appear negligible (Leoni et al., 2018). Hot springs or other hydrothermal spas, with their elevated water temperatures, provide favourable conditions for the survival of Legionella, and they have been linked to cases of legionellosis (Leoni et al., 2018). Engineered water environments (e.g., cooling towers, premise plumbing in buildings and residences) are typically where Legionella can reach high concentrations, under the right conditions, resulting in an increased risk of human exposure and disease (NASEM, 2020).
Legionella are important agents of two respiratory diseases in humans: Legionnaires’ disease and Pontiac fever. Legionnaires’ disease is a more severe and sometimes fatal form of respiratory illness, while Pontiac fever is a milder illness causing flu-like symptoms but not pneumonia. Further information on the health impacts of Legionella can be found in Health Canada’s Guidelines for Canadian Drinking Water Quality: Guidance on Waterborne Pathogens (2022a). There is no consensus on whether there is a threshold of detectable Legionella below which there is no risk of infection (NASEM, 2020).
Despite the fact that Legionella species are thought to be ubiquitous in bodies of water, no outbreaks of legionellosis have been reported in Canada or the United States as a result of recreational activity in natural waters. This may be due to the low concentrations found in most natural waters as well as the lack of aerosolization. All reported outbreaks of legionellosis associated with human contact with recreational waters have been linked to the use of treated water facilities, such as hot tubs and spas (Moore et al., 1993; Kramer et al., 1996; Levy et al., 1998; Barwick et al., 2000; Lee et al., 2002; Yoder et al., 2004; Hlavsa et al., 2018).
Mycobacteria (Class: Actinobacteria) are aerobic to microaerophilic, non-motile, non-spore-forming, rod-shaped bacteria. Mycobacteria can grow at temperatures ranging from 15°C to 45°C (George et al., 1980; Cangelosi et al., 2004; Kaur, 2014). Optimal growth temperatures for individual species vary between 30°C and 45°C (De Groote, 2004; Stinear et al., 2004); however, mycobacteria are relatively heat-resistant and capable of surviving at temperatures greater than 50°C (Schulze-Robbecke and Buchholtz, 1992; Falkinham, 2016a). Mycobacteria vary in their ability to cause disease in humans. Some are strict pathogens, whereas others cause opportunistic infections or are non-pathogenic. The mycobacteria commonly isolated from the environment are collectively referred to as the non-tuberculous mycobacteria (NTM) and are considered opportunistic pathogens (Falkinham, 2016a, b). NTM need to be distinguished from M. tuberculosis (causative agent of tuberculosis) and M. leprae (causative agent of leprosy), which are strict pathogens. Neither M. tuberculosis nor M. leprae is a concern for recreational waters.
The NTM species most commonly described as having relevance for recreational water exposures belong to the Mycobacterium avium complex (M. avium and its subspecies, M. intracellulare and M. chimaera), which are known to cause respiratory illness; and M. marinum and M. kansasii, which can cause skin infections. The main routes of infection are inhalation of mycobacteria contained in aerosols and direct water contact or ingestion of contaminated water (Percival and Williams, 2014e; Falkinham, 2015; Falkinham et al., 2015). There is little evidence of person-to-person transmission. Illness is more commonly observed in individuals with some underlying condition that predisposes them to infection (abraded or traumatized skin; or a weakened or compromised immune system). The infective doses of NTM species are not known (Stout et al., 2016; Hamilton et al., 2017; Adjemian et al., 2018).
Non-tuberculous mycobacteria are considered ubiquitous in natural waters. They can be found in virtually every medium, including soils, wastewater, lakes, rivers, ponds, streams, groundwater, and treated water supplies. However, few NTM are encountered in marine waters (Pond, 2005; LeChevallier, 2006; Falkinham, 2016b; Percival and Williams, 2014e). NTM are capable of survival and growth within certain species of phagocytic protozoa, specifically members of the genus Acanthamoeba, as well as in biofilms (Percival and Williams, 2014e).
Like Legionella, NTM can survive in hot springs or other hydrothermal spas as a result of the elevated water temperatures. A Japanese study reported that both Legionella and NTM had been detected in these types of environments (Kobayashi et al., 2014). Exposures to NTM have been most strongly linked to swimming pool and hot tub use, and typically resulted in cases of skin and soft tissue infections and hypersensitivity pneumonitis (inflammation of the lungs). Although environmental mycobacteria are considered ubiquitous in most types of water, to date there have been no recorded outbreaks of mycobacterial-associated illness through contact with natural recreational waters in either Canada or the United States. For healthy individuals, the risk of acquiring a mycobacterial infection from recreational activity in natural waters is considered to be extremely low.
2.2.3 Pseudomonas aeruginosa
Pseudomonas spp. are gram-negative, motile, strictly aerobic oxidase-positive, non-spore-forming, slightly curved rod-shaped bacteria that grow at temperatures from 4°C to 42°C (optimum range is 28°C to 37°C) (Moore et al., 2006; Chakravarty and Anderson, 2015). The genus Pseudomonas (Family: Pseudomonadaceae; Class: Gammaproteobacteria) includes over 200 species (LPSN, 2020), with P. aeruginosa representing the most significant species of human concern.
P. aeruginosa is widely distributed in the aquatic environment and can be frequently isolated from fresh water, seawater and soils (Hunter, 1997). These bacteria are considered part of the natural aquatic flora (WHO, 2003). The organism has minimal growth requirements and is able to proliferate in waters with low nutrient levels. P. aeruginosa is infrequently isolated from human feces (Geldreich, 2006) but it can be recovered from sewage and wastewater (Degnan, 2006). If P. aeruginosa are present in high enough numbers in recreational waters, through direct body contact with the water. Ingestion is not considered to be a significant route of infection.
P. aeruginosa can cause respiratory, skin, eye, and ear infections as well as skin rashes, with the latter three conditions being the most common. Ear infections occur when P. aeruginosa enters and colonizes the outer ear canal. A few days after swimming, the swimmer’s ear may become itchy and painful, and discharges of pus may be observed. Skin irritations (dermatitis) present as a red, itchy rash, which occurs roughly 18 to 24 hours after water contact. Infection can progress to folliculitis (inflammation of the hair follicles of the skin), which is marked by an increased tenderness of the infected area and the presence of pus-filled blisters or pimples surrounding the hair follicles.
Several epidemiological studies have shown a link between Pseudomonas in natural waters and the incidence of eye and skin infections among swimmers (Seyfried and Cook, 1984; Springer and Shapiro, 1985; Ferley et al., 1989; Marino et al., 1995; van Asperen et al., 1995). Reported outbreaks of Pseudomonas dermatitis have virtually all been associated with treated water venues such as hot tubs, swimming pools or hotel whirlpool or spa baths (Moore et al., 1993; Kramer et al., 1996; Levy et al., 1998; Barwick et al., 2000; Lee et al., 2002; Yoder et al., 2004; Hlavsa et al., 2018). The incidence of P. aeruginosa infections from contact with natural recreational waters is not known, as illnesses are usually mild and are typically not reported.
Aeromonas are Gram-negative, facultatively anaerobic, non-spore-forming, variably motile, rod-shaped to coccoid-like bacteria. They are thought to share many morphological and biochemical characteristics with members of the Enterobacteriaceae family, which includes E. coli. The genus Aeromonas (Family: Aeromonadaceae; Class: Gammaproteobacteria) consists of approximately 30 species, but new species continue to be described (Moyer, 2006; US EPA, 2006; Janda and Abbot, 2010; Percival and Williams, 2014a; LPSN, 2019). Strains associated with human infections grow optimally at temperatures between 35°C and 37°C, but many strains can grow at temperatures between 4°C and 42°C (Janda and Abbott, 2010; Percival and Williams, 2014a). To date, 14 species have been implicated in human illness, but most infections (85%) are caused by 4 species: A. hydrophila, A.caviae, A. veronii (biotype sobria) and A. trota (Percival and Williams, 2014a; Bhowmick and Battacharjee, 2018).
Aeromonas species are natural inhabitants of the aquatic environment. They are frequently found in fresh, marine and estuarine waters, sediments, as well as sewage and wastewater effluents. Aeromonads have also been found in high concentrations in foreshore sands (Khan et al., 2009). Aeromonads are not commonly found in significant numbers in the feces of healthy individuals, however, some individuals may carry the organisms in their intestinal tract without showing outward signs of illness. Aeromonads are recognized animal pathogens and have been isolated from the intestinal tract of a number of animal species, including fish, reptiles, amphibians, birds and domestic livestock, with and without evidence of illness (Percival and Williams, 2014a). The occurrence of the bacteria in recreational waters is not dependent on fecal pollution as they can survive and reproduce in the natural environment. However, the organisms are present in high numbers in sewage and thus can be detected at significant levels in sewage-contaminated waters. Aeromonads can reach relatively high concentrations in eutrophic (nutrient rich) waters (Moyer, 2006). Since these organisms achieve optimal growth at elevated temperatures, the highest concentrations in natural waters are observed during the warmer months.
Aeromonas infections usually result in gastrointestinal illness and wound infections. Gastrointestinal illness is typically mild and self-limiting, although certain strains may cause a dysentery- or cholera-like illness, marked by severe abdominal cramps, vomiting, diarrhea (including bloody stools) and fever (Janda and Abbott, 2010). In recreational water users, Aeromonas infections are most often associated with wound infections. Typically, skin trauma such as an open wound or a penetrating injury is needed for an infection to occur. Wound infections are characterized by pain, swelling, redness and fluid accumulation around the infected area. Cellulitis (severe inflammation) is frequently observed with wound infections, and septicemia is also a fairly common outcome (Percival et al., 2004; Janda and Abbott, 2010), largely arising through the transfer of bacteria from the gastrointestinal tract or from wound infections. Common features associated with these infections are fever, jaundice, abdominal pain and septic shock (Janda and Abbott, 2010). Other, rarer complications include necrotizing fasciitis, meningitis, pneumonia, peritonitis and endocarditis (Percival et al., 2004; Janda and Abbott, 2010; Bhowmick and Battacharjee, 2018).
The dose of Aeromonas spp. necessary to cause infection is not clear. The single available challenge study used ingestion as the route of exposure and showed that only two out of five strains produced infection (14 out of 57 individuals) and diarrhea (2 out of 57 individuals) at high doses (104 to 1010 colony forming units, or CFU) (Morgan et al., 1985).
Despite their widespread occurrence, there have been no reported outbreaks of Aeromonas-associated illness as a result of recreational water activities in North America. Marino et al. (1995) reported a positive correlation between A. hydrophila concentrations and skin infections at two swimming beaches in Malaga, Spain. Currently, however, there is no evidence of a link between Aeromonad concentrations and the risk of acquiring swimming-associated gastroenteritis. Aeromonas infections are not reportable illnesses in Canada. Consequently, an estimate of the likely incidence of Aeromonas infections due to recreational water exposures in Canadian waters is not available.
2.3 Other pathogenic bacteria
In addition to enteric bacteria and naturally occurring bacteria, other pathogenic bacteria may enter recreational waters in urine or through direct contamination from bathers. If these organisms are present in high enough numbers in a body of water, they may be transmitted to humans, typically through direct contact with body surfaces and mucous membranes. The types of illness observed range from wound infections to life-threatening conditions. As these bacteria are not of fecal origin, fecal indicators are not expected to correlate well with their presence. There is no recognized microbiological indicator for these pathogens at the present time.
Leptospira are spirally coiled or corkscrew-shaped bacteria. They are Gram-negative, aerobic, long, thin and motile organisms that can live at temperatures ranging from 4°C to 40°C (Barragan et al., 2017). The genus Leptospira (Class: Spirochaetes) contains more than 20 known species, and over 200 pathogenic serotypes have been described. The more severe forms of leptospirosis infections are attributed to serovars (syn. serotypes) of L. interrogans (Pond, 2005; Wynwood et al., 2014; Levett, 2015).
Leptospira are divided into pathogenic, environmental non-pathogenic (saprophytic) and indeterminate (genetically distinct from pathogenic and saprophytic) species. They are encountered worldwide and are predominantly associated with freshwater environments. Pathogenic leptospires are important zoonotic pathogens that are carried in the renal tract (kidney) of infected animals and excreted in the urine. Small mammals, such as rats, mice and voles, are considered the most significant source of pathogenic Leptospira. These organisms can also be spread by domestic animals, such as cattle, pigs, dogs and cats, sheep, goats and horses (WHO, 2003; CDC, 2005b; Barragan et al., 2017). Heavy rainfall facilitates their spread, as runoff from contaminated soils can affect surface waters (Pond, 2005).
Human infection can occur following direct contact with the urine of infected animals or indirectly though contact with contaminated water, soil or mud. Leptospirae gain access through cuts or abrasions in the skin or through the mucous membranes of the eyes, nose and mouth. The incubation period in humans is approximately 10 days, but may range from 2 to 30 days (CDC, 2008). Leptospira infection can range in severity from a mild, influenza-like illness to more severe, and possibly fatal disease. Early symptoms include fever, chills, headache, muscle pains, vomiting and reddening of the eyes (PHAC, 2004). Recovery from mild illness is usually complete, but can take months to years (WHO, 2003). If left untreated, the disease can progress to more serious illness, also known as Weil’s disease. Severe cases of leptospirosis can be fatal, with death occurring as a result of kidney failure, cardiorespiratory failure or extensive hemorrhaging. The reasons for the differences in the severity of infection are not fully understood; however, it is believed that each pathogenic serovar possesses the capacity to cause either mild or severe disease (WHO, 2003). A case of Leptospira illness can be difficult to diagnose, as it may be mistaken for other infections or illnesses that produce similar symptoms. Mild forms of the illness may not be reported. Ingestion of as few as 1 to 10 organisms may lead to human illness (Pond, 2005).
Leptospirosis is considered to be a greater concern in developing countries, where poor housing standards and local infrastructure can result in exposure to rodent reservoirs, as well as in tropical climates. Incidental contact with contaminated water, such as through occupational or recreational activities in endemic areas, is also a source of exposure (Haake and Levett, 2015). A systematic review of waterborne disease related to extreme weather events worldwide identified Leptospira spp. as one of the more commonly reported pathogens associated with environmental exposure routes (e.g., wading in flood waters) (Cann et al., 2013). However, it is unclear whether any of these exposures were related to recreational water activities. In the United States, three outbreaks of leptospirosis linked to recreational waters were reported between 1991 and 2002 (Moore et al., 1993; Barwick et al., 2000; Lee et al., 2002). Between 2000 and 2014, Leptospira spp. were implicated in six outbreaks in the United States (Graciaa et al., 2018). Most of the outbreaks were associated with participation in adventure races/triathlons or exposure to drought impacted waters. Currently, the prevalence of Leptospira in Canadian waters is not known, and leptospirosis in not a reportable illness in Canada. There have been no documented cases of Leptospira infection linked to recreational water activity in Canada.
2.3.2 Staphylococcus aureus
Members of the genus Staphylococcus (Class: Bacilli) are Gram-positive, non-motile cocci. S. aureus is considered the species of greatest human health concern in the genus and is the species of most significance for recreational water use. This includes the antibiotic resistant strain known as methicillin-resistant Staphylococcus aureus (MRSA). MRSA infections are classified as community-acquired MRSA infections or hospital-acquired MRSA infections, depending on where the infection was acquired. Hospital-acquired infections are more common, and have resulted in outbreaks in these facilities (Government of Canada, 2022c). MRSA infections acquired from recreational water exposures would be classified as community-acquired MRSA.
S. aureus is not considered to be a natural inhabitant of environmental waters. The major reservoirs for this organism are the skin, nose, ears and mucous membranes of warm-blooded animals. The presence of S. aureus in recreational waters is predominantly due to releases of the organism from the mouths, noses and throats of swimmers and to discharges from existing infections (Plano et al., 2011). However, the organism can be isolated from human feces (Percival et al., 2004), and other sources, such as sewage and stormwaters, have been identified (Economy et al., 2019).
Transmission of S. aureus in recreational waters occurs via direct contact with waters containing a high enough number of organisms to cause an infection. Infection occurs through cuts or scratches on the skin and, to a lesser extent, through contact with the eyes and ears. Person-to-person spread of the organism is also possible. Ingestion is not considered to be a significant route of exposure. Concentrations of a few hundred cells per millilitre may be sufficient to initiate infection in injured or distressed skin (Percival et al., 2004).
S. aureus is predominantly associated with skin infections in recreational water users (Charoenca and Fujioka, 1995). Common infections include infected cuts and scratches, boils, pustules, dermatitis, folliculitis and impetigo (WHO, 2006). Infections are most often pus-forming, with symptoms often not becoming apparent until 48 hours after contact. The organism has been linked to other illnesses including eye infections, ear infections and urinary tract infections (WHO, 2006). S. aureus infections can become severe or life-threatening, especially when they are caused by MRSA (David and Daum, 2010). MRSA has been isolated from natural recreational water environments. Although up to 20% of S. aureus have been identified as MRSA from natural waters (Levin-Edens et al., 2012), studies usually report that less than 5% of isolates are methicillin-resistant (Goodwin et al., 2012; Plano et al., 2013).
Some epidemiological studies have explored the possibility of using staphylococci as an indicator of adverse health impacts from recreational activities. Several authors have demonstrated possible connections between staphylococci in recreational waters and gastrointestinal illness and skin conditions in swimmers (Seyfried et al., 1985; Calderon et al., 1991; Griffith et al., 2016). However, this finding is not consistent (Plano et al., 2013; Griffith et al., 2016). A link between the concentrations of staphylococci and bather density has also been found (Calderon et al., 1991; Plano et al., 2013). No consistent relationship has been reported between the concentrations of staphylococci and the quality of recreational waters as indicated by the presence of E. coli or enterococci (Calderon et al., 1991; Haack et al., 2013; Fogarty et al., 2015).
2.4 Enteric viral pathogens
Viruses are much smaller than bacteria, ranging in size from 20 nm to 350 nm. They have a nucleic acid core composed of either RNA or DNA which is surrounded by an external protein shell called a capsid. Some viruses (enveloped viruses) may also have a lipoprotein envelope surrounding the capsid. Non-enveloped viruses lack this external layer. Viruses are obligate intracellular parasites and must infect a host cell to replicate. Although they are incapable of replicating outside of their host environment, they can survive for extended periods outside a host. Most viruses of concern for transmission through water are non-enveloped viruses (e.g., enteric viruses). Non-enveloped viruses are more resistant to environmental conditions than enveloped viruses. Some enveloped viruses are shed in feces (e.g., coronaviruses including SARS-CoV-2); however, a fecal-oral route of transmission has not been documented and they are therefore considered low risk for transmission through water environments (La Rosa et al., 2020).
Enteric viruses—viruses that infect the human gastrointestinal tract and are shed in human feces—are thought to pose the greatest risk of infection to swimmers in recreational waters (Schoen and Ashbolt, 2010; Soller et al., 2010; Dufour et al., 2012; McBride et al., 2013; Eregno et al., 2016; Vergara et al., 2016). Sources of enteric viruses include municipal sewage, combined sewer overflows and septic tanks as well as shedding by infected bathers. Enteric viruses are considered to have a narrow host range, meaning that enteric viruses that infect animals do not generally infect humans and vice versa. Exposure to enteric viruses in recreational waters occurs via the fecal-oral route, through the accidental ingestion of contaminated water. Some viruses, like the adenoviruses, have additional routes of infection, such as inhalation or contact with mucosal membranes of the eyes. Gastrointestinal symptoms (nausea, vomiting, diarrhea) are the most commonly encountered symptoms of enteric viral illness. Some virus infections can result in more serious health outcomes, although these are considered to be much rarer.
There are more than 200 recognized enteric viruses that can be excreted in feces (Haas et al., 2014), including 140 serotypes known to infect humans (AWWA, 1999; Taylor et al., 2001). Enteric viruses are shed in high numbers in the feces of infected individuals and can reach concentrations as high as 1010 to 1012 particles per gram of feces (Gerba, 2000; Bosch et al., 2008). Even asymptomatic individuals are capable of excreting large numbers of viruses. The total viral load of sewage can be quite constant; however, the types and numbers of individual viruses are strongly influenced by the rates of epidemic and endemic illness within the population contributing to the sewage. As a result, the viral composition of sewage can vary considerably, often demonstrating strong seasonal trends (Krikelis et al., 1985; Tani et al., 1995; Pina et al., 1998; Lipp et al., 2001). The presence of viruses in surface waters is expected to vary regionally and is dependent upon (among other factors) the degree and type of fecal contamination and the rates of environmental inactivation. Numerous studies have reported the presence of enteric viruses in surface waters around the world, including Canada. Further information can be found in the Guidelines for Canadian Drinking Water Quality – Enteric Viruses guideline technical document (Health Canada, 2019a).
The enteric viruses most commonly associated with waterborne illness include noroviruses, enteroviruses, rotaviruses, adenoviruses and Hepatitis A virus, and they have been detected in marine and fresh waters used for recreational purposes in Canada, the United States, and Europe (Payment, 1984; Puig et al., 1994; Pina et al., 1998; Griffin et al., 1999; Chapron et al., 2000; Payment et al., 2000; Schvoerer et al., 2001; Denis-Mize et al., 2004; Jiang and Chu, 2004; Laverick et al., 2004). Outbreaks have been linked to many of these enteric viruses (see sections 2.4.1 to 2.4.6). As pathogenic viruses are difficult to detect in water, outbreaks of acute gastrointestinal illness of unknown etiology have also been attributed to viral infections. In the United States, 23% (14 out of 64) of documented outbreaks from 1991 to 2002 (Moore et al., 1993; Kramer et al., 1996; Levy et al., 1998; Barwick et al., 2000; Lee et al., 2002; Yoder et al., 2004), and 26% (37 out of 140) of documented outbreaks between 2000 and 2014 (Graciaa et al., 2018) had an unknown etiology.
E. coli and enterococci are used as indicators of fecal contamination and thus the possible presence of enteric viruses. However, the absence of indicator organisms does not necessarily indicate that enteric viruses are also absent. Fecal source tracking methods (e.g., qPCR for human-specific fecal markers) can be used to supplement monitoring and assessment tools to identify risks posed by enteric viruses. Further information on managing risks in recreational waters and fecal indicator organisms can be found in the Guidelines for Canadian Recreational Water Quality technical documents on Understanding and Managing Risks in Recreational Waters and Indicators of Fecal Contamination (Health Canada, in publication – a,d).
Noroviruses are small (35 to 40 nm in diameter), non-enveloped RNA viruses belonging to the Caliciviridae family. Noroviruses are currently subdivided into seven genogroups (G1 to GVII) of which genogroups GI, GII and GIV contain the genotypes usually associated with human illnesses (Verhoef et al., 2015). The incubation period associated with norovirus infection is 12 to 48 hours (CDC, 2013b; Government of Canada, 2022a). Health effects associated with norovirus infections are self-limiting, typically lasting 24 to 48 hours. The primary symptoms of illness are diarrhea, nausea, vomiting, abdominal pain and fever. The onset of projectile vomiting is considered a characteristic trait of norovirus infection. Asymptomatic infections with norovirus can occur (Graham et al., 1994), and some individuals are resistant to infection (Hutson et al., 2003; Lindesmith et al., 2003; Cheetham et al., 2007). In healthy adults, illness rarely progresses to more serious concerns (e.g., dehydration), but more serious infections may occur in vulnerable groups such as the elderly.
Noroviruses are the etiologic agent of primary concern to swimmer’s health (Schoen and Ashbolt, 2010; Soller et al., 2010; Dufour et al., 2012; McBride et al., 2013; Eregno et al., 2016; Vergara et al., 2016). Between 1991 and 2002, the US CDC reported that 13% (8 of 64) of disease outbreaks reported in natural waters in the United States were caused by noroviruses (Moore et al., 1993; Kramer et al., 1996; Levy et al., 1998; Barwick et al., 2000; Lee et al., 2002; Yoder et al., 2004). More recent US CDC reports indicate that between the years 2000 and 2014, 22% (21 of 95) of outbreaks in untreated recreational water (with known etiology) were caused by norovirus, which accounted for 47% (1,459 of 3,125) of the cases of illness (Graciaa et al., 2018). Data on norovirus outbreaks related to recreational waters is not available for Canada. Exposure to noroviruses in recreational areas results from contamination by human fecal matter, such as through municipal sewage discharges and combined sewer overflows (McBride et al., 2013; Eregano et al., 2016; Wade et al., 2018) or through fecal shedding by infected beachgoers (Schets et al., 2018).
Enteroviruses are a large group of small (20 to 30 nm), non-enveloped RNA viruses belonging to the genus Enterovirus and the Picornaviridae family. Within the genus, four species designated Enterovirus A, Enterovirus B, Enterovirus C and Enterovirus D have been associated with human illness (EV-A to EV-D). Members of the EV-A to EV-D species include enteroviruses, polioviruses, coxsackieviruses and echoviruses (Simmonds et al., 2020).
The incubation period for enteroviruses ranges from 2 to 35 days (AWWA, 2006) and the symptoms and severity of illness vary considerably among the individual virus types. Many enterovirus infections are asymptomatic. Mild symptoms may include fever, malaise, sore throat, vomiting, rash and upper respiratory tract illness. Acute gastroenteritis is less common. More serious outcomes have been associated with individual virus groups, including myocarditis (coxsackievirus), aseptic meningitis (coxsackievirus, poliovirus), encephalitis (coxsackievirus, echovirus), poliomyelitis (poliovirus), and non-specific febrile illnesses of newborns and young infants. However, these illnesses are not considered to be common (Rotbart, 1995; Roivainen et al., 1998). Other complications include myalgia, Guillain-Barré syndrome, hepatitis and conjunctivitis. Enteroviruses have also been implicated in the etiology of chronic diseases, such as inflammatory myositis, dilated cardiomyopathy, amyotrophic lateral sclerosis, chronic fatigue syndrome and post-poliomyelitis muscular atrophy (Pallansch and Roos, 2007; Chia and Chia, 2008). There is also some research supporting a link between enterovirus infection and the development of insulin-dependent (Type 1) diabetes mellitus (Nairn et al., 1999; Lönnrot et al., 2000; Laitinen et al., 2014; Oikarinen et al., 2014).
Enteroviruses are endemic worldwide, and have been detected in water sources in Canada and the United States (Health Canada, 2019a). However, few enterovirus outbreaks have been reported around the world. No recreational water-related outbreaks were reported in the United States from 2000 to 2014 and only one case was reported prior to the year 2000 (Sinclair et al., 2009; Graciaa et al., 2018). No outbreaks related to enteroviruses in recreational areas have been reported in Canada.
Rotaviruses are larger (60 to 80 nm), non-enveloped, double-stranded RNA viruses which belong to the Reoviridae family. These viruses have been divided into eight serological groups, designated as A to H (Marthaler et al., 2012); three of the groups (A, B and C) infect humans, with group A being the most common and widespread (Estes and Greenberg, 2013).
In general, rotaviruses cause gastroenteritis, which is characterized by vomiting and diarrhea. The severity of gastroenteritis can range from mild, lasting less than 24 hours, to severe infections, which can become life-threatening as a result of dehydration and electrolyte imbalance. Groups considered vulnerable to severe disease and illness-induced mortality include young children, immunocompromised individuals and the elderly. Rotavirus infection has been identified as the number one cause of infantile gastroenteritis worldwide. The vast majority of rotavirus infections are believed to result from person-to-person transmission (Butler et al., 2015). As a result of the immunity acquired during childhood, infections among healthy adults are often asymptomatic (Percival et al., 2004). In young children, extra-intestinal manifestations, such as respiratory symptoms and seizures, can also occur (Candy, 2007).
Group A rotavirus is endemic worldwide; however, a rotavirus vaccine is available. Rotaviruses have been isolated from surface water sources in Canada and the United States (Rose et al., 1987; Corsi et al., 2014; Pang et al., 2019) and from individual stool samples after recreational water exposures (Dorevitch et al., 2012; Hintaran et al., 2018). Nonetheless, no outbreaks of rotavirus associated with recreational water have been reported.
Adenoviruses are large (70 to 100 nm) non-enveloped, double-stranded DNA viruses belonging to the Adenoviridae family. Over 60 individual serotypes have been identified as being capable of causing human illness, with the clinical features and severity of illness varying considerably among the individual types (Percival et al., 2004). Most adenovirus serotypes cause respiratory illness, which presents with pharyngitis and cough and cold-like symptoms. Conjunctivitis can also occur as a result of infection of the eye. The majority of waterborne isolates are types 40 and 41 and cause gastrointestinal illness (Mena and Gerba, 2009), which may last a week (PHAC, 2010). Adenoviruses are thought to be second only to rotaviruses as a cause of childhood gastroenteritis (Crabtree et al., 1997), with the majority of illnesses believed to be associated with person-to-person transmission (Butler et al., 2015). Infections are generally confined to children less than five years of age (FSA, 2000; Lennon et al., 2007) and are rare in adults. Adenoviruses have been detected in surface water sources around the world (Xagoraraki et al., 2007; Sassoubre et al., 2012; Lee et al., 2014; Marion et al., 2014; Vergara et al., 2016; Steele et al., 2018) but very few outbreaks linked to recreational waters have been recorded worldwide (Sinclair et al., 2009; Graciaa et al., 2018). No adenovirus outbreaks associated with recreational waters have been reported in Canada.
2.4.5 Hepatitis viruses
Six types of hepatitis viruses have been identified (A, B, C, D, E and G), but only two types, hepatitis A and hepatitis E, appear to be transmitted via the fecal-oral route and may therefore be associated with waterborne transmission. Hepatitis viruses are very stable in the environment, but their survival time is temperature dependent (van der Poel and Rzezutka, 2017). Although hepatitis viruses may survive in the environment, no outbreaks related to recreational waters have been recorded in Canada.
Hepatitis A virus (HAV) is a small (27 to 32 nm), non-enveloped single-stranded RNA virus belonging to the genus Hepatovirus within the Picornadiridae family. The major target organ for HAV is the liver. The incubation period of HAV infection is between 15 and 50 days (CDC, 2015). The majority of HAV infections are asymptomatic. Illness is most frequently reported among adults, with the severity of illness increasing with age. Children usually have mild or no symptoms (Yayli et al., 2002). Symptoms of HAV infection may include anorexia, malaise and fever, followed by nausea, vomiting, abdominal pain and jaundice. Infection is typically self-limiting, but in some cases HAV can cause liver damage leading to death. Convalescence may also be prolonged (8 to 10 weeks), and in some cases, individuals may experience relapses for up to six months (CDC, 2015). In Canada, the incidence of HAV has declined significantly since the introduction of the HAV vaccine in 1996 (PHAC, 2022). Most cases of HAV occur in contacts of infected individuals, in travellers returning from countries were HAV is common and in communities with inadequate sanitation (PHAC, 2022).
Hepatitis E virus (HEV) is a small (27 to 34 nm), non-enveloped, single-stranded RNA virus belonging to the Hepeviridae family. Human-infectious HEV are classified into four genotypes. Genotypes 1 and 2 have been found only in humans, whereas genotypes 3 and 4 appear to be zoonotic (transmitted to humans from deer, pigs and wild boars) (Smith et al., 2014). The incubation period for HEV varies from 15 to 60 days. Symptoms include malaise, anorexia, abdominal pain, arthralgia, dark urine, fever and jaundice, usually resolving in 1 to 6 weeks, although cases with a weakened immune system may develop long-lasting illnesses that can lead to more advanced liver disease (Government of Canada, 2022b). Infection is more often reported in young to middle-aged adults, and can lead to death in rare cases. In pregnant women, the fatality rate can approach 20% to 25% (Matson, 2004). Illnesses associated with HEV are rare in developed countries, with most infections being linked to international travel.
Astroviruses are small (28 to 30 nm), non-enveloped, single-stranded RNA viruses belonging to the Astroviridae family. Genotypes A and B are capable of infecting humans (Carter, 2005). Of the viral agents known to cause enteric illness, the significance of astroviruses as a cause of waterborne illness is perhaps the least well characterized (Percival et al., 2004). Illness in infected individuals appears to be similar to rotaviral illness, although it is markedly less severe (diarrhea lasting 2 to 3 days that does not lead to significant dehydration). Other symptoms include headache, malaise, nausea, vomiting and mild fever (Percival et al., 2004; Méndez and Arias, 2007). Infections caused by serotypes 1 and 2 are commonly acquired during childhood (Palombo and Bishop, 1996), and those caused by other serotypes (4 and above) may not occur until adulthood (Carter, 2005); however, infection in adults is uncommon (Oishi et al., 1994; Caul, 1996; Gray et al., 1997). Re-infection is rare, as healthy individuals generally acquire protective immunity to the disease (Gofti-Laroche et al., 2003).
Astroviruses can be transmitted through food, water, fomites and person-to-person contact (Bosch et al., 2014; Butler et al., 2015). The degree of transmission that occurs through water, in particular through recreational water, is not known. Person-to-person contact is believed to be the main route of transmission (Butler et al., 2015). No outbreaks of astroviruses associated with recreational waters have been recorded in Canada; however, astroviruses have been recovered from surface water sources in Canada (Jones et al., 2017; Pang et al., 2019).
2.5 Enteric protozoan pathogens
Pathogenic protozoa that are of significance in relation to recreational waters include both enteric and free-living species. Enteric protozoa are common parasites that infect the intestinal tract of humans and other mammals. They are obligate parasites, meaning that they must infect a host to replicate and are incapable of growth outside the host environment. The most important stage of their life cycle involves the production of cysts or oocysts, which are shed in large numbers in the feces. These cysts or oocysts are extremely resistant to environmental stresses and can survive for long periods in the environment. Sources of enteric protozoa that can impact recreational waters include those that contain human or animal feces (e.g., waste water discharges, agricultural runoff, direct deposition of feces). Transmission to humans occurs through ingestion of contaminated water. The most common enteric protozoa of concern in recreational waters are Giardia and Cryptosporidium, which cause illness that typically manifests as gastrointestinal symptoms (diarrhea). E. coli and enterococci are the primary organisms used to indicate the presence of fecal contamination and thus the possible risk of enteric illness, including the risk of illness from enteric protozoa. Enteric protozoa can survive longer in the environment than the bacterial indicators and may be present after E. coli and enterococci have died off.
Giardia spp. are flagellated protozoan parasites. They have a two-stage life cycle consisting of a trophozoite (feeding stage) and an environmentally resistant cyst stage. Six Giardia species are recognized at present. G. lamblia (syn. G. intestinalis and G. duodenalis), found in humans and a wide range of other mammals, is the only human-infective species. Other species (G. muris, G. agilis, G. microti, G. psittaci and G. ardea) have been reported in animals, including rodents, birds and amphibians. Molecular characterization of G. lamblia has identified eight genetically distinct assemblages (designated A through H) which differ in their host range (Boarato-David et al., 2017). Assemblages A and B infect humans and other mammals, whereas the remaining assemblages (C, D, E, F and G) have not yet been isolated from humans and appear to have restricted host ranges (Plutzer et al., 2010).
The most common symptoms associated with Giardia infection (also known as giardiasis) include sudden explosive, watery, pale, greasy and foul-smelling diarrhea, nausea, intestinal upset, fatigue, low-grade fever and chills. The severity of Giardia infection can range from no observable symptoms (asymptomatic infections) to severe gastrointestinal illness requiring hospitalization. Giardia infection can also lead to lactase deficiency (i.e., lactose intolerance) and general malabsorptive syndrome, and some research suggests that it could also lead to irritable bowel syndrome or chronic fatigue syndrome in some individuals (Cotton et al., 2011; Wensaas et al., 2012; Hanevik et al., 2014). The median dose for infection is around 50 cysts (Hibler et al., 1987), although subjects have shown infection at much lower doses (Rendtorff, 1978). The time between ingestion and the excretion of new cysts (prepatent period) ranges from 6 to 16 days. Infection is usually self-limiting, clearing within 1 to 3 weeks on average; however, some patients may be asymptomatic carriers for longer periods. In other cases, individuals (particularly children) may experience recurrent bouts of the disease, persisting for several months to a year. Persistent illness can be treated using a number of antiparasitic drugs.
Human and animal feces (especially cattle feces) are major sources of G. lamblia. Other recognized animal hosts include pigs, beavers, muskrats, dogs, sheep and horses. Many of these animals can be infected with G. lamblia originating from human sources (Davies and Hibler, 1979; Hewlett et al., 1982; Erlandsen et al., 1988; Traub et al., 2004, 2005; Eligio-Garcia et al., 2005). Epidemiological and molecular data suggest that it is only these human-source strains that have been significantly associated with human illness (Hoque et al., 2003; Stuart et al., 2003; Berrilli et al., 2004; Thompson, 2004; Hunter and Thompson, 2005; Ryan et al., 2005). Giardia is commonly encountered in sewage and surface waters. In general, concentrations in raw and treated domestic wastewater typically range from 5,000 to 50,000 cysts/L and from 50 to 500 cysts/L, respectively (Medema et al., 2003; Pond et al., 2004). Surface water concentrations typically range from < 2 to 200 cysts/100 L (Gammie et al., 2000). Canadian studies have found that the majority of Giardia isolates in surface water were assemblages A and B (Edge et al., 2013; Prystajecky et al., 2015).
Surveillance data published by the US CDC for 1992 to 2002 indicate that Giardia was responsible for 9% (6 out of 64) of the total number of outbreaks of gastroenteritis reported for natural recreational waters (Moore et al., 1993; Kramer et al., 1996; Levy et al., 1998; Barwick et al., 2000; Lee et al., 2002; Yoder et al., 2004). More recently, for 2000 to 2014, Giardia was found to be responsible for 3% (9 of 140) of these outbreaks (Graciaa et al., 2018). Locations included recreational lakes, a recreational river and a pond setting. Although Giardia has not been linked to outbreaks in natural recreational waters in Canada, it is likely that cases have occurred but were not detected or reported.
Cryptosporidium are small, non-motile protozoan parasites. These organisms possess a complex, multi-stage life cycle, which includes the production of a round, thick-walled, environmentally stable oocyst. Twenty-nine species are currently recognized as belonging to the genus (Ryan et al., 2014; Zahedi et al., 2016). Two predominant genotypes have been linked to human illness: C. hominis (genotype 1), reported only in humans, and C. parvum (genotype 2), reported in humans, calves and other ruminants. Other species and genotypes have been identified from human infections, but much less frequently. Humans and cattle are the most significant sources of Cryptosporidium. Sheep, pigs and horses are also considered to be reservoirs (Olson et al., 1997). Rodents are not a significant source of human-infective Cryptosporidium (Roach et al., 1993).
Cryptosporidium infection can result in illness varying in severity from asymptomatic carriage to severe, life-threatening illness in immunocompromised individuals. The primary characteristic of illness is profuse, watery, non-bloody and sometimes mucoid diarrhea. Other symptoms include cramping, nausea, vomiting, abdominal pain, weight loss, dehydration, anorexia and low-grade fever (CDC, 2021c).
As is the case with other pathogens, although a variety of median infective doses have been reported for Cryptosporidium, a single organism is theoretically sufficient to initiate infection. Volunteer feeding studies suggest that the median infective dose of Cryptosporidium is between 9 and 2,066 oocysts (DuPont et al., 1995; Okhuysen et al., 1998, 1999, 2002; Chappell et al., 1999, 2006; Messner et al., 2001). The prepatent period is roughly 4 to 9 days. Most healthy individuals experience a complete recovery, with the disease resolving itself in about 1 to 2 weeks. Oocysts may continue to be shed in feces for a short period following recovery. In most reports of individuals with severely weakened immune systems (i.e., AIDS patients), the infection is never completely cleared, and may develop into an infection with long bouts of remission followed by mild symptoms. Extraintestinal cryptosporidiosis (i.e., in the lungs, middle ear, pancreas, etc.) and death have been reported, primarily among persons with AIDS (Farthing, 2000; Mercado et al., 2007), but these cases are considered rare.
Crytosporidium oocysts are commonly found in water affected by human or livestock wastes. Contamination may occur through sewage discharges, fecal shedding by swimmers and stormwater runoff. Waterfowl (ducks, geese) may pick up oocysts from their habitat and deposit them elsewhere through discharge in their feces. Typical concentrations in raw wastewater are on the order of 1,000 to 10,000 oocysts/L (Guy et al., 2003). In Canadian surface waters, concentrations generally range from 1 to 100 oocysts/100 L (Gammie et al., 2000).
Surveillance data in the United States for 1992 to 2002 show that 6 (9%) of the 64 outbreaks of gastrointestinal illness reported as being linked to natural recreational waters were caused by Cryptosporidium (Moore et al., 1993; Kramer et al., 1996; Levy et al., 1998; Barwick et al., 2000; Lee et al., 2002; Yoder et al., 2004). More recently, from 2000 to 2014, 12 (9%) of 140 recreational outbreaks were attributed to this pathogen (Graciaa et al., 2018). Recreational lakes were the setting for the majority of the outbreaks. A large outbreak at a New Jersey lake in 1994 involving 418 cases was the first recorded US outbreak of cryptosporidiosis related to recreational water use (Kramer et al., 1996). Treated recreational water venues such as water parks and community and motel swimming pools have provided the setting for the majority of outbreaks of cryptosporidiosis (Hlavsa et al., 2018). Surveillance in Canada has been limited. To date, there have been no reported outbreaks of cryptosporidiosis associated with natural recreational waters. As with Giardia, it is expected that cases have occurred but have not been detected or reported.
2.5.3 Other enteric protozoa of potential concern
Other enteric pathogenic protozoa of potential concern include Entamoeba, Toxoplasma and Cyclospora. Humans are the only significant reservoir of Entamoeba. Most infections occur through person-to-person contact, but they can also be acquired through ingestion of fecally contaminated water and food. Entamoeba infections can range from being asymptomatic to causing gastrointestinal illness, which may be serious or life-threatening (Kucik et al., 2004). Toxoplasma affects almost all warm-blooded animals, including humans, and can be shed in human and animal feces. It is usually transmitted through the ingestion of raw or undercooked infected meat, through contaminated foods or water, or through handling of contaminated soil or cat feces. Most Toxoplasma infections cause mild, flu-like symptoms; however, infection can be life-threatening for both immunocompromised and pregnant individuals (Shapiro et al., 2019). Cyclospora is like Entamoeba in that it only occurs in humans. Transmission is thought to occur through the ingestion of food or water contaminated with human feces. In Canada, most reported cases of illness are linked to contaminated food and travel (Ortega and Sanchez, 2010). Cyclospora infection causes symptoms similar to those associated with Cryptosporidium.
Entamoeba, Toxoplasma and Cyclospora can conceivably contaminate recreational waters. Toxoplasma has been linked to a drinking water-associated outbreak in Canada, which indicates that surface waters can be contaminated with this pathogen (Isaac-Renton et al., 1998). However, no recreational waterborne outbreaks have been reported for Toxoplasma, Entamoeba or Cyclospora in Canada. Consequently, based on current evidence, recreational water activity is not considered to be a significant risk factor for illness caused by these organisms.
2.6 Free-living protozoa
Free-living protozoa, unlike enteric protozoa, occur naturally in recreational waters and do not need a host organism in order to complete their life cycle. Transmission to humans can occur in waters containing sufficient quantities of the organisms, through mechanisms such as inhalation or through direct contact with mucous membranes (e.g., those of the eye). These organisms cause various types of illness, including infections of the central nervous system and eye infections. As these protozoans are not of fecal origin, fecal indicators are not expected to correlate well with their presence. Currently, there is no recognized microbiological indicator for these pathogens.
The free-living protozoa recognized as being the most significant from the perspective of natural recreational waters are Naegleria and Acanthamoeba.
2.6.1 Naegleria fowleri
Naegleria are thermophilic, free-living freshwater amoebae. The genus Naegleria is composed of over 40 species; however, only N. fowleri is a pathogen in humans (Marciano‐Cabral and Cabral, 2007; Yoder et al.. 2010). N. fowleri are thermophilic organisms that grow well at temperatures between 25°C and 40°C (optimum: 37°C) and can tolerate temperatures exceeding 50°C to 60°C (Hallenbeck and Brenniman, 1989; Visvesvara et al., 2007; Zaongo et al., 2018). The organism has a multi-stage life cycle consisting of a motile feeding trophozoite stage, a non-replicating flagellate stage and an environmentally resistant cyst stage. The cysts are the most resistant form of the organism and can survive under adverse environmental conditions.
N. fowleri has been found around the world in warm fresh water and soil. The organism has been isolated from both natural and artificial warm water supplies, including lakes, rivers, hot springs, swimming pools, hydrotherapy baths and tap water. It is most commonly detected in tropical and subtropical fresh waters and in hot springs. While survival of N. fowleri in northern waters is less common, the pathogen has been found in lake water in states as far north as Minnesota (Yoder et al., 2010, 2012). No human or animal reservoirs have been identified.
N. fowleri causes a disease of the central nervous system called primary amoebic meningitis (PAM), which is almost always fatal. Human infection occurs when water containing the amoeba enters the nasal passages (e.g., during diving, jumping, falling or swimming underwater). Following entry into nasal passages, the organism travels to the brain, where it damages the cells of the olfactory system and cerebral cortex. The onset of illness is rapid with symptoms occurring 1 to 7 days after exposure. The disease progresses rapidly, with death generally occurring within 5 days (Visvesvara et al., 2007; Chalmers, 2014b). Symptoms include severe headache, high fever and vomiting, followed by a stiff neck, altered mental status, seizures, coma and ultimately death. PAM has an extremely high fatality rate (greater than 97%) (Capewell et al., 2015). Successful treatment requires prompt diagnosis and aggressive antimicrobial therapy (CDC, 2019).
Cases of PAM are extremely rare. It is estimated that in the United States, one case occurs among approximately every 2.5 million swimmers (Visvesvara and Moura, 2006). From 1962 to 2015, 138 cases of PAM were reported in the United States, with between 0 and 8 cases reported annually (Cope and Ali, 2016). The majority of exposures have occurred at lakes and ponds; exposures at rivers or streams have been less frequently reported (Yoder et al., 2010). There have been some cases of illness where improperly maintained swimming pools were the probable sources of exposure (Yoder et al., 2010; Cope and Ali, 2016). Cases are more common in the southern United States. However, with climate warming, cases have been identified farther north, for example, in Minnesota, Kansas, and Indiana (Cope and Ali, 2016). To date, there have been no recorded cases of PAM linked to recreational water contact in Canadian waters. The bulk of the evidence suggests that amoebic meningoencephalitis is an unlikely health concern in Canada. However, researchers have suggested that increasing lake temperatures brought on by climate change could result in this organism becoming more prevalent in Canadian surface waters (Rose et al., 2001; Schuster and Visvesvara, 2004).
Acanthamoeba are free-living amoebae. Approximately 20 different genotypes of Acanthamoeba have been identified (Juárez et al., 2018). Acanthamoeba genotype T4 is the predominant type encountered in cases of illness and in the environment; however, other genotypes have also been associated with disease (Chalmers, 2014a; Juárez et al., 2018).
Acanthamoeba are considered ubiquitous in the environment. They can be found in fresh, estuarine and marine waters, hot springs, soils and sewage. Acanthamoeba spp. have low nutrient requirements and grow at temperatures from 12°C to 45°C (optimum: 30°C) (Chalmers, 2014a). Their life cycle consists of two stages: a feeding trophozoite (25 to 40 µm) and a resistant cyst (10 to 30 µm) that can withstand temperatures between -20°C and 56°C and resist desiccation and disinfection (Chalmers, 2014a; Juárez et al., 2018).
Acanthamoeba are opportunistic pathogens that can cause rare but severe human diseases affecting the eye, skin, lungs, brain and central nervous system (Visvesvara et al., 2007; Chalmers, 2014a; de Lacerda and Lira, 2021). The most common form of illness is amoebic keratitis (AK), a painful, vision-threatening disease of the cornea (Juárez et al., 2018). Infection occurs via direct contact with the mucous membranes of the eye. AK is usually associated with poor hygiene practices in contact lens wearers (use of contaminated solutions and inadequate disinfection). In rare cases, Acanthamoeba can also cause disseminated infections, which originate in the skin and lungs and then spread to other areas of the body. One such example is granulomatous amoebic encephalitis, a fatal disease of the central nervous system. The rare cases of disseminated illness, which are not thought to be waterborne, primarily occur in individuals with weakened immune systems or underlying disease (Chalmers, 2014a). Despite the widespread occurrence of Acanthamoeba in environmental waters, recreational water contact is not considered to be a significant risk factor for acquiring illness. As mentioned above, the majority of cases are linked to the use of contact lenses (de Lacerda and Lira, 2021), some of which could be a result from wearing contact lenses while swimming in lakes or ponds. To reduce this risk, contact lenses should be removed before engaging in primary contact water activities (CDC, 2021b).
As mentioned in section 2.3.2, Acanthamoeba may also host certain free-living bacterial pathogens, namely Legionella and Mycobacterium (Visvesvara et al., 2007; Juárez et al., 2018). Survival within Acanthamoeba can provide these organisms with an environment suitable for replication, as well as protection from environmental stresses.
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