Water quality indicators: bacteria, coliphages, enteric ...

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Water quality indicators: bacteria, coliphages, enteric viruses a

Johnson Lin & Atheesha Ganesh

a

a

School of Life Sciences, University of KwaZulu-Natal, Durban, South Africa Version of record first published: 26 Feb 2013.

To cite this article: Johnson Lin & Atheesha Ganesh (2013): Water quality indicators: bacteria, coliphages, enteric viruses, International Journal of Environmental Health Research, DOI:10.1080/09603123.2013.769201 To link to this article: http://dx.doi.org/10.1080/09603123.2013.769201

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International Journal of Environmental Health Research, 2013 http://dx.doi.org/10.1080/09603123.2013.769201

REVIEW ARTICLE Water quality indicators: bacteria, coliphages, enteric viruses Johnson Lin* and Atheesha Ganesh

Downloaded by [UNIVERSITY OF KWAZULU-NATAL] at 01:47 26 February 2013

School of Life Sciences, University of KwaZulu-Natal, Durban, South Africa (Received 23 May 2012; final version received 16 December 2012) Water quality through the presence of pathogenic enteric microorganisms may affect human health. Coliform bacteria, Escherichia coli and coliphages are normally used as indicators of water quality. However, the presence of above-mentioned indicators do not always suggest the presence of human enteric viruses. It is important to study human enteric viruses in water. Human enteric viruses can tolerate fluctuating environmental conditions and survive in the environment for long periods of time becoming causal agents of diarrhoeal diseases. Therefore, the potential of human pathogenic viruses as significant indicators of water quality is emerging. Human Adenoviruses and other viruses have been proposed as suitable indices for the effective identification of such organisms of human origin contaminating water systems. This article reports on the recent developments in the management of water quality specifically focusing on human enteric viruses as indicators. Keywords: water quality indicators; enteric viruses; E. coli; total/faecal coliforms; coliphages

Introduction Waterborne pathogens transmit diseases to around 250 million people each year resulting in 10 to 20 million deaths around the globe (Zamxaka et al. 2004; Wilkes et al. 2009). The assessment of the microbiological quality of drinking-water aspires to protect consumers from illnesses due to the consumption of water that may contain pathogens such as bacteria, viruses and protozoa, thereby thwarting water-related illness outbreaks. An indicator of microbial water quality is generally one specific species or group of microorganisms, which must have entered the water system at the same time as faeces, but this indicator is easier to measure than the full range of microorganisms which pose the health risk. A useful water quality indicator should carry some particular properties: be universally present in the faeces of humans and warm-blooded animals in large numbers; be readily detected by simple methods; not grow in natural waters, or general environment or water distribution systems; be persistent in water and lastly, the degree to which it is removed by water treatment is comparable to those of waterborne pathogens (WHO 1999). Many studies (Liang et al. 2006; Hewitt et al. 2007; Maunula et al. 2009) have associated the outbreaks of waterborne gastroenteritis with a diversity of enteric bacteria and viruses, although recreational exposure to polluted water has often been more linked to viral infections (Vantarakis & Papapetropoulou 1999). The presence or absence of indicator organisms is fundamental to most drinkingwater quality guidelines, water supply operating licences and agreements between bulk *Corresponding author. Email: [email protected] Ó 2013 Taylor & Francis


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J. Lin and A. Ganesh

water suppliers and retail water companies (Colford et al. 2006). In order to be an effective indicator of faecal contamination, an organism must be consistently present in faeces and in high numbers. At present, the bacterial indicators including total coliforms, faecal coliforms, Escherichia coli (E. coli), faecal streptococci and enterococci have been used to access quality in water quality management and health risk assessments because they are much easier and less costly to detect and enumerate than the pathogens themselves (Meays et al. 2004). The South African water quality guidelines are centered solely on E. coli as an indicator of pathogenic pollution and are subject to strict governmental regulations (DWAF 1996a, 1996b). None of the bacterial indicators currently used for monitoring meet all ideal criteria established for water quality (Ashbolt et al. 2001; Stevens et al. 2001; Bitton 2005). The concentration of faecal bacteria can provide some level of indication of enteric viruses when the contamination originates from human sources. This relationship may not exist when the source of pollution is of animal origin (Payment et al. 2000). Literature has shown that the presence of viruses does not always correlate with the detection of bacterial indicators such as E. coli, total coliforms, and intestinal enterococci (Baggi et al. 2001; Miagostovich et al. 2004; Skraber, Gassilloud, & Gantzer 2004a; Skraber, Gassilloud, & Schwartzbrod 2004b; Hauri et al. 2005; Espinosa et al. 2009; Jurzik et al. 2010). Furthermore, studies have revealed that enteric viruses were detected in raw, surface water, ground water and treated drinking water despite meeting quality standards for coliform bacteria (Gerba & Rose 1990; Cho et al. 2000; Pusch et al. 2005). The survival and incidence of bacterial viruses (phages) in water environments resemble those of human viruses more closely than most other bacterial indicators commonly used. The enumeration of bacteriophages which infect coliform bacteria (coliphages) has been widely accepted as a tool in water quality assessment (DWAF 1996a; Grabow 2001). Somatic coliphages occur in large numbers in sewage and polluted water environments and are easy to detect (Grabow 2001). Male-specific (F-RNA) coliphages are highly specific for sewage pollution and cannot be replicated in water environments, as their detection methods are more complicated (DWAF 2004a, 2004b). The presence of somatic coliphages and F-specific RNA (F-RNA) bacteriophages, however, does not always correlate with human enteric viruses (Hot et al. 2003; Jiang & Chu 2004). In addition, it is difficult to differentiate between human and animal faecal contamination whilst using somatic coliphages as indicators. Consequently, many human enteric viruses, enteroviruses (Kopecka et al. 1993; Gantzer et al. 1998), rotaviruses (Miagostovich et al. 2008), adenoviruses (Puig et al. 1994; Pina et al. 1998) and human polyomaviruses (Bofill-Mas et al. 2000; Hamza et al. 2009; McQuaig et al. 2009) have been proposed as indicators of wastewater contamination in aquatic environments. This review considers various water quality indicator organisms with specific focus on enteric viruses, the analytical methodologies (biochemical and molecular) and addresses the advantages and limitations of these indicators. Bacteria as indicators of water quality The indicator organisms presently used for the monitoring of drinking water in developed countries are total coliforms, faecal coliforms and/or E. coli. The reliance on these indicator organisms to determine the safety of drinking water is constantly under review (Ashbolt et al. 2001; WHO 2003; Tallon et al. 2005). Many other organisms such as

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enterococci and faecal streptococci that are present in high numbers in the environment have been used as alternate water quality indicators. Total coliforms and faecal coliforms as an indicator of water quality Total coliforms are typically described as “All facultative anaerobic, Gram-negative, non-spore forming, oxidase-negative, rod-shaped bacteria that ferment lactose to acid and gas within 48 h at 35 °C or members of Enterobacteriaceae which are β-galactosidase positive” (APHA 1998). The total coliform group of bacteria was originally used as a surrogate for E. coli which, in turn, was considered to demonstrate faecal pollution, until more specific and rapid methods became available (Kornacki & Johnson 2001). Detection of total and faecal coliforms in raw water can provide authorities with an indication of any changes in water quality (WHO 1997). Classical methods for detection of total and faecal coliforms in natural waters include the most probable numbers (MPN) and the membrane filtration (MF) techniques on selective agar (APHA 1998). Although the tests are simple to perform, they are time-consuming, requiring 48 h for the presumptive results which do not allow the detection of all the target bacteria in natural environments. Since the late nineteenth century, bacteria have been used as water quality indicators (Medema et al. 2003). The use of coliforms as bacterial indicators of microbial water quality is based on the hypothesis that coliforms are present in elevated numbers in the faeces of humans and other warm-blooded animals. If faeces or its leachates have entered into drinking water, it is probable that these bacteria will also be present, even after significant dilution. It is generally accepted that the total coliform group of bacteria is diverse and can be considered as typical inhabitants of many soil and water environments which have not been impacted by faecal pollution. With a few exceptions, the coliform group of bacteria is not considered to be a health risk, but their presence indicates that faecal pollution may have occurred and pathogens might be present in the water environment as a result. Total coliforms signify only about 1% of the total population of bacteria in human faeces in concentrations of about 109 bacteria per gram (Brenner et al. 1982). However, total coliforms are generally considered unreliable indicators of faecal contamination because many of them are capable of growth in both the environment and in drinking-water distribution systems (LeChevallier 1990; Camper et al. 1991; Szewzyk et al. 1994). Ambiguity surrounds the use of total coliforms as a health indicator, as many authors have reported waterborne disease outbreaks in water meeting the total coliform regulations (MacKenzie et al. 1994; Payment et al. 1997; Gofti et al. 1999; Ootsubo et al. 2003; Ottson & Stenstrom 2003). Even though the presence of E. coli is considered a suitable and specific indicator of faecal pollution and faecal coliforms have a survival pattern analogous to that of bacterial pathogens, their efficacy as indicators of protozoan or viral contamination is limited. Many articles expressed the view that faecal coliforms are not effective indicators of faecal pollution in drinking water due to the large number of environmental species like Klebsiella spp. (Alonso et al. 1999; Edberg et al. 2000; Ashbolt et al. 2001; Leclerc et al. 2001). Even though there are some drawbacks using total coliforms and faecal coliforms as indicators, detection of total/faecal coliforms in drinking water may indicate failure in the treatment system, regrowth or infiltration in the distribution system which might have serious health implications. Therefore, coliforms are still recognized as acceptable indicators especially in the treatment and disinfection processes (WHO 2003).

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E. coli as an indicator of water quality E. coli is not only a member of thermotolerant coliforms that produce indole from tryptophan, but is also defined now as coliforms with the enzyme β-glucuronidase. It has been constantly detected in larger numbers than other species in the faeces of human and animals. The majority of E. coli strains are commensal bacteria of the gastrointestinal tract of warm-blooded animals (WHO 2003). Currently there are over 160 serogroups recognized, the majority of which do not cause disease (Salyers & Whitt 2002). Studies have shown that E. coli is the only coliform almost exclusively associated with a faecal source (Tallon et al. 2005). Huang et al. (1997) reported that the β-glucuronidase enzyme is specific to 94–97% of E. coli resulting in the development of simple, rapid, sensitive and reliable methods for their detection. At present, E. coli is considered the best bacterial indicator of faecal contamination in drinkingwater especially as some faecal coliforms could be non-faecal in origin (Baudizsova 1997). However, E. coli contamination does not always takes place due to direct faecal contamination: Leakages, unsafe handling and improper storage might also be the cause of detection of E. coli. Some studies have shown that a high concentration of E. coli can be found in tropical natural water systems (Lopez-Torres et al. 1987; Jimenez et al. 1989) as well as in effluents from pulp and paper mills (Archibald 2000; Gauthier & Archibald 2001) with no known sources of faecal contaminations. Furthermore, it is also recognized that E. coli may not be suitable as an indicator of some specific enteric pathogens such as protozoa and viruses. Faecal streptococci and enterococci The enterococci were first integrated into the functional group of bacteria known as “faecal streptococci” but now largely belong to the genus Enterococcus which was formed by the splitting of Streptococcus faecalis and Streptococcus faecium, along with less important streptococci, from the genus Streptococcus (Schleifer & Kilpper-Balz 1984). In addition, other Enterococcus species and some species of Streptococcus (namely S. bovis, and S. equinus) may occasionally be detected in waters. The term “faecal streptococci” refers to those streptococci commonly present in the faeces of humans and animals. The genus Enterococcus has recently been defined to include all streptococci sharing certain biochemical properties and having wide tolerance of adverse growth conditions. Rapid and simple methods, based on defined substrate technology, are available for the detection and enumeration of faecal streptococci/enterococci in MPN or MF techniques, based on their ability to grow in the presence of azide and their fermentation of carbohydrates to produce lactic acid (WHO 1993). For water examination purposes, enterococci/faecal streptococci can be regarded as indicators of faecal pollution, since they have a number of advantages as indicators over total coliforms and even E. coli (Geldreich 1997). The importance for their use as water quality indicators dates back to 1900 when they were found to be common commensal bacteria in the gut of warm-blooded animals (Gleeson & Gray 1997). These advantages include that they generally do not grow in the environment (WHO 1993) and they have been shown to survive longer (McFeters et al. 1974). Faecal streptococci rarely multiply in polluted waters and despite being approximately an order of magnitude less numerous than faecal coliforms and E. coli in human faeces (Feacham et al. 1983), they are still numerous enough to be detected after significant dilution. Their main value in


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assessing water quality is therefore, as an additional indicator of treatment efficiency. Furthermore, streptococci are highly resistant to drying and may be valuable for the purpose of routine controls after new mains have been laid or distribution systems repaired, or for detecting pollution by surface run-off to ground water or surface waters. Bacteriophages as indicators of water quality Bacteriophages that infect coliform bacteria are known as coliphages. Phages are valuable prototypes for enteric viruses because they share many underlying properties and features notably composition, morphology, structure, size and site of replication. In addition, their resistances against environmental factors make coliphages more applicable than faecal bacteria for indicating faecal contamination of water (Grabow 2001; Contreras-Coll et al. 2002; Yates 2007; Jurzik et al. 2010). The survival and incidence of bacterial viruses (phages) in water environments resemble those of human viruses more closely than most other bacterial indicators commonly used. Coliphages used in water quality assessment consist of major groups of somatic coliphages and F-specific RNA (F-RNA) phages (Skraber, Gassilloud, & Gantzer 2004a). Phage detection in environmental water samples involves concentration of the sample, decontamination of the concentrate, and carrying out of phage (plaque) assay by the double- or single-layer agar methods (Bitton 2005). A wide range of bacterial host cells have been used as some are more efficient than others in hosting phages. Most data on the incidence of phages in water environments are on somatic coliphages. This is because somatic coliphages are detectable by simple, inexpensive and rapid techniques, and the phages occur in large numbers in any water environment exposed to human or animal excreta. Phages have proven to be valuable tools in research on viruses and have been projected as microbial indicators of water quality, as they share many fundamental properties with human enteric viruses which pose a health risk, if present in water contaminated with human faeces (Grabow 2001).

Somatic coliphages as an indicator of water quality Somatic coliphages occur in large numbers in sewage and polluted water environments and are easy to detect, but they may be replicated by host bacteria in certain water environments (Grabow 2001). The United States Environmental Protection Agency (US EPA 2001a, 2001b) has proposed two methods (methods # 1601 and 1602) to detect somatic coliphages (host is E. coli ATCC 13706) in aquatic environments. Method 1601 (spot test) includes an overnight nutrient enrichment step of the water sample followed by “spotting” onto a host bacterial lawn. In method 1602 (double-overlay agar test), the water sample is supplemented with MgCl2, host bacteria, and double-strength molten agar and the plaques are counted after overnight incubation (US EPA 2001a, 2001b). Wild-type strains of E. coli are poor hosts for the detection of coliphages in wastewaters, as these strains have a complete O-antigen that conceals the mainstream phage receptor sites and their defence mechanisms which include nuclease enzymes that destroy phage nucleic acids recognized as foreign, thus preventing phage replication (Grabow 2001). E. coli strain C (ATCC 13706), also known as WG4, is a mutant in which the genes which code for these nuclease enzymes have been deleted. This strain of E. coli is susceptible to a broad range of coliphages and is the host most frequently used for detecting the presence of somatic coliphages in water environments (Grabow


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et al. 1998; ISO 1998). One of the advantages for using somatic coliform as indicators is that somatic coliphages are detectable by relatively simple and inexpensive plaque assays, which yield results within 24 h. Somatic coliphages have been found to outnumber F-RNA phages in waste water and raw water sources by a factor of about five, and cytopathogenic human viruses by about 500 (Grabow 2001; Cimenti et al. 2007), thus making them valuable indicators for assessing the behavior of, and the possible presence of enteric viruses in water environments such as estuaries, seawater, freshwater, potable water, wastewater and bio-solids (Moce-Llivina et al. 2003). Somatic coliphage counts in the faeces of man and animals may vary from less than 10 plaque-forming units (pfu)/g to 108 pfu/g, although in human faeces counts rarely exceed 103 pfu/g and may often be undetectable. Somatic coliphages are often found more in faeces of patients suffering from systemic diseases. In natural waters, coliphages may also be detected in high numbers, primarily due to pollution from sewage. Inactivation of coliphages is determined by similar conditions as those which determine inactivation of bacteria; the most significant factors are temperature, suspended solids, biological activity and sunlight (Grabow 2001). There are many conflicting results questioning whether somatic coliphages can reliably predict the viral contamination of surface waters, concomitantly there are many reports considering coliphages as good indicators of enteric viral pollution (Kott et al. 1974; Fannin et al. 1977; Kott 1977; Gerba 1987; Borrego et al. 1990; Contreras-Coll et al. 2002). These reports demonstrated that somatic coliforms were detected in wastewater and other fecal contaminated waters in numbers equal to the enteric viruses. Blanch et al. (2004) reported that the ratio of the densities of somatic coliphages and phages infecting bacteroides can be used as a potentially good tracer with a high discriminatory capability. Hot et al. (2003) and Jurzik et al. (2010), on the other hand, concluded that somatic coliphages are not suitable parameters for predicting the presence of waterborne viruses as autochthonous coliphages are present in unpolluted waters (Morinigo et al. 1992). Male-specific F-RNA coliphages as an indicator of water quality F-RNA coliphages are single stranded RNA phages which belong to the Leviviridae family. These phages are classified into four sero- or genogroups on the basis of their serological cross-reactivity or their differences in genome organization (Bollback & Huelsenbeck 2001). Serogroups II and III are generally found in human sewage whilst serogroups I and IV are generally found in animal wastes (Osawa et al. 1981; Hsu et al. 1995; Grabow 2001; Cole et al. 2003). F-RNA coliphages infect E. coli (strain K-12) cells, as the receptor sites for male-specific coliphages are located on the fertility fimbriae of this bacterium, the F plasmid, codes for the F or sex pilus to which the F-RNA phage attach. The host-range of pilus-specific phages is not essentially limited to one or a few closely related species as assembly of pili is typically encoded on the F (fertility) plasmid and the host-range of pilus-dependent phages depends mostly on the successful transfer and expression of the plasmid. Birge (1981) reported the successful transfer of the F-plasmid of E. coli K-12 to Salmonella typhimurium, as well as Shigella and Proteus species, causing these recipient cells to become susceptible to male-specific coliphages. This phenomenon offers an attractive tool to distinguish between faecal pollution of both human and animal origin (Cole et al. 2003).



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Detection of F-RNA coliphages by plaque assays is not simple as the F fimbriae are produced only by host bacteria in the logarithmic growth phase making preparation of the host cultures particularly difficult (Grabow 2001). The US EPA has proposed the use of specific host cells such as S. typhimurium strain WG49 or E. coli strain HS [pFamp]R to detect male-specific phages in aquatic environments. This highly modified strain of S. typhimurium is not susceptible to a large number of somatic coliphages in water environments which tend to interfere with the detection of F-RNA coliphages using E. coli hosts (Grabow et al. 1998). Once detected, the F-RNA phage can be additionally characterized as being a derivative of human or animal origin by immunological or genetic methods (Hsu et al. 1995; Griffin et al. 2000). In serotyping, group-specific antisera are used whereas in genotyping, hybridization with groupspecific oligonucleotides is used (Grabow 2001; Sundram et al. 2006). The hybridization assay involves plating the phage on a particular host, transferring the plaques to a nylon membrane, denaturing the phage to expose the nucleic acid, cross-linking the nucleic acid to the membrane, and then detecting group-specific nucleic acid sequences with 32P- or digoxigenin-labelled oligonucleotide probes (Sundram et al. 2006). This technique is useful for identifying the four groups of F-RNA bacteriophages and therefore can be used in tracking sources of faecal pollution (Griffin et al. 2000). Methods based on direct genome detection reverse transcription (RT)-PCR (Dryden et al. 2006), the combination of RT-PCR and blot hybridization (Vinje et al. 2004), real-time RTPCR (O’Connell et al. 2006; Ogorzaly & Gantzer 2006) and multiplex real-time RTPCR (Kirs & Smith 2007; Wolf et al. 2008) have been described. Molecular methods have the advantage to be more rapid. Grabow et al. (1998) found that F-RNA phages outnumber cytopathogenic enteric viruses by a factor of about 100 in wastewaters and raw water sources, implying that their absence from raw and treated water supplies offers a significant indication of the absence of human enteric viruses. Several studies have confirmed that the resistance of F-RNA coliphages to unfavourable environmental conditions and disinfection processes resembles or exceeds that of most human enteric viruses (Burge et al. 1981; Kapuscinski & Mitchell 1983; Havelaar et al. 1990, 1993; Grabow et al. 1998; Olivieri et al. 1999; Bitton 2005). Espinosa et al. (2009) reported that F-RNA coliphages can be used as an index for the presence of enteric viruses. However, a high proportion of F-RNA coliphages from the animal samples contained genotype III which is similar to the ones in samples of human origin (Blanch et al. 2006). Recently, Ogorzaly et al. (2009) demonstrated positive correlations between the concentrations of F-RNA coliphages genotype II, bacterial indicators and human adenoviruses using real-time PCR. Therefore, it might be necessary to perform the genotyping in order to use it as the source tracing method. However, plaque assays for F-RNA coliphages need the culture of host bacteria in the logarithmic growth phase to ensure that F fimbriae are present (WHO 2008). Human pathogenic viruses as potential indicators of water quality Presently, there are no suitable models developed that can reliably predict the presence of enteric viruses in surface water (Jurzik et al. 2010). The presence of human enteric viruses in different potable water systems has not yet been successfully documented. There is no agreement concerning the suitability of some viruses/coliphages as indicators for enteric viruses in water. Viruses, although the smallest and most numerous of all biotic agents, represent the planet’s largest pool of genetic diversity and human


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pathogenicity (Rosario et al. 2009). In nature, enteroviruses have many advantages for transmission compared with other viruses. All the identified human pathogenic viruses that pose significant public health risk in water environments are transmitted via the faecal oral route (Griffin et al. 2003) frequently causing asymptomatic or mild infections resulting in large numbers of progeny produced that are shed in the faeces. The virus particles are very stable under a wide range of environmental conditions (Keswick et al. 1982; Piirainen et al. 1998; Olivieri et al. 1999). Furthermore, enteric viruses are frequently resistant to most employed disinfection methods (Baggi & Peduzzi 2000; Carter 2005; Dongdem et al. 2009). It is imperative to consider human enteric viruses in water quality studies not only because of their incidence as causal agents for diarrhoeal diseases, but most especially because they can cause illnesses at low viral loads (Griffin et al. 2000); they survive in the environment for long periods of time and tolerate changing environmental conditions (Skraber, Gassilloud, & Gantzer 2004a; Espinosa et al. 2008). With the increasing popularity of molecular detection methods, developing countries may find a solution to the problem of infectious viruses in aquatic environments. The molecular detection methods are relatively fast and specific compared to the traditional methods, and such techniques could be incorporated into part of regular monitoring programmes to assess the virus levels (Okoh et al. 2010). One of the main hurdles with determining enteric viruses in water directly is that the detection methods are expensive, time consuming, and labour-intensive. The use of a conceptual synthetic virus as a means of determining acceptable levels for human enteric viruses in water has been proposed by the US EPA (Payment et al. 1997). However, the public perception of synthetic viruses will have to be overcome before it can be implemented. Since the presence of a few viral particles is sufficient to cause disease, detection of low concentrations of these viruses in environmental samples or in food matrices is significant. Therefore, the methods for detection of viruses in food and water samples must have a high level of sensitivity and specificity (Bosch et al. 2011) and a wide range of methods are available for detection of environmental viruses. Growth in tissue culture and plaque assay for enumeration are the gold standards for infectious virus quantification (Mattison & Bidawid 2009). However, the conditions under which many enteric pathogens should be cultured are not known (Mattison & Bidawid 2009) and other viruses grow slowly or do not produce a cytopathic effect (Bosch et al. 2011). Other methods such as electron microscopy and immunoelectron microscopy which directly visualize viral particles provide an alternative approach, but all these lack the sensitivity and higher titres needed in each sample (Mattison & Bidawid 2009). Molecular methods, using the PCR, RT-PCR and real-time PCR or real-time RT-PCR, have become the most commonly applied methods for the detection of viruses in food and environmental samples (Mattison & Bidawid 2009; Bosch et al. 2011). The inability to differentiate between infectious and noninfectious viruses whilst using PCR is one of the major limitations of molecular methods. However, integrated systems based on the molecular detection of viruses after cell culture infection are the most promising techniques to overcome this limitation (Rodriguez et al. 2009). In addition, many authors have reported that the number of infectious viruses do not correlate with the number of genomes detected by real-time RT-PCR in water samples (Baert et al. 2008; Butot et al. 2009). Recently metagenomic sequencing has been used to define the diversity of viral communities in reclaimed water and potable water (Rosario et al. 2009), in faecal samples from diarrhea patients (Finkbeiner et al. 2008) and in various aquatic samples (Williamson et al. 2008). Known viruses and novel viruses were detected by sequenc-



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ing from each sample library which diminished sequencing costs and improved efficiencies; therefore, mass sequencing could become a powerful diagnostic tool. Of all human enteric viruses, those commonly detected in the environment that have been proposed as indicators of wastewater contamination in aquatic environment include Enteroviruses (EV) (Kopecka et al. 1993; Gantzer et al. 1998), Hepatitis A virus (HAV), Rotaviruses (RV) (Miagostovich et al. 2008), Adenoviruses (AdV) (Puig et al. 1994; Pina et al. 1998) and human Polyomaviruses (Bofill-Mas et al. 2000; Hamza et al. 2009; McQuaig et al. 2009). Due to the frequent detection of enterovirus in raw and treated wastewater (Payment et al. 1997) and their easy cultivation, the water regulation authority in Italy has considered using EV as viral references (D. Lgs 31/2001). However, EV (Skraber, Gassilloud, & Gantzer 2004a) and RV (Petrinca et al. 2009; Jurzik et al. 2010) have been found to exhibit seasonal fluctuations. Thus, the use of EV as a marker of faecal pollution could potentially underestimate the extent of faecal contamination. Bibby et al. (2011) did not detect the presence of EV and RV in class B biosolids in a viral metagenome analysis. Symonds et al. (2009) failed to detect any Hepatitis B viruses, Herpesviruses, Morbilliviruses, Papillomaviruses, Reoviruses and RV in their raw sewage samples in the USA. The WHO regards HAV as reference pathogens for drinkingwater risk analysis (Fewtrell & Bartram 2001), however, Rigotto et al. (2010) failed to detect HAV and only detected RV in few water samples in South Brazil. Other reports of HAV in environmental samples have also shown a low incidence in sewage samples and treated sewage in Brazil (Formiga-Cruz et al. 2005; Villar et al. 2007). These results indicate that HAV, RV and EV are not good candidates as water quality indicators. Human adenoviruses as an indicator of water quality Human adenoviruses (HAdVs) are members of the genus Mastadenovirus in the Adenoviridae family (Okoh et al. 2010). They possess double-stranded linear DNA and a nonenveloped icosahedral shell that has fibre-like projections from each of its 12 vertices (Stewart et al. 1993). Identification of adenovirus generally starts with virus isolation using cell culture, followed by antibody or antigen detection and visualization by electron microscopy (Fong & Lipp 2005). The progression of molecular technologies, such as PCR methods for detection and real-time PCR (qPCR) methods for quantification, has enhanced the speed and sensitivity of adenovirus detection in water samples drastically (van Heerden et al. 2003, 2004, 2005). Current adenoviruses comprises 51 serotypes classified in six species (A–F) (Okoh et al. 2010). HAdVs are prevalent and very stable, hence, they are considered as human specific and are not detected in animal wastewaters or slaughterhouse sewage (Girones 2005). HAdVs have been shown to frequently occur in raw water sources, treated drinkingwater supplies, urban rivers and polluted coastal waters (Puig et al. 1994; Tani et al. 1995; Pina et al. 1998; Jiang et al. 2001; Dongdem et al. 2009; Jurzik et al. 2010). The incidence of HAdVs in such waters was surpassed only by the group EV among viruses detectable by PCR based techniques (Chapron et al. 2000; Grabow 2001). HAdV infections have been reported to occur worldwide and throughout the year (Flomenberg 2005; Bofill-Mas et al. 2006) and approximately 90% of the human population is seropositive for one or more serotypes of adenoviruses (Fong et al. 2010) suggesting that there are no seasonal variations in the prevalence of these viruses. In view of their pervasiveness and detection as enteric pathogens, their detection in water (contaminated, drinking or recreational) represents a likely but unconfirmed source of HAdV infections (Grabow 2001). Studies in the United States found that adenoviruses, among all the


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proposed enteric virus indicators, were found ubiquitously in raw sewage samples (Symonds et al. 2009). HAdVs are also considered important because they are exceptionally resistant to some water treatment and disinfection processes, notably UV light irradiation. HAdVs have been detected in drinking-water supplies that met accepted specifications for treatment and disinfection with use of conventional indicator organisms (Chapron et al. 2000; Grabow 2001; Dongdem et al. 2009). The above studies thus support HAdVs as suitable indicators of human viral pathogens in aquatic environments (Puig et al. 1994; Pina et al. 1998; Fong & Lipp 2005; Albinana-Gimenez et al. 2006; Hundesa et al. 2006; Bosch et al. 2008; Jurzik et al. 2010; Okoh et al. 2010). However, this virus did not correlate with HAV or EV in urban waterways (Jiang 2002). McQuaig et al. (2009) only detected sparse numbers of AdV in a faulty septic tank system in comparison with that of Polyomavirus. Human polyomaviruses as an indicator of water quality Polyomavirus is a small, non-enveloped double-stranded DNA virus that is the sole genus in the family Polyomaviridae (ICTVdB 2006). The family Polyomaviridae, which originally contained only one single genus (Polyomavirus), has recently expanded into three genera: Orthopolyomavirus, Wukipolyomavirus, and Avipolyomavirus (Johne et al. 2011). Different laboratories use a variety of assays, e.g. electron microscopy (Schroedera et al. 2003), PCR (Johne et al. 2005; Lamontagne et al. 2011), or cell culture (Marshall et al. 1990), to detect polyomavirus particles in clinical samples. Five human Polyomavirus (BKV, JCV, KIV, WUV and MCV) have been identified (Kean et al. 2009). Weitschek et al. (2012) recently used the data mining techniques, by considering the complete sequences of the viruses and the sequences of the different gene regions separately, to effectively characterize the different five studied polyomaviruses. These viruses are known for producing lifelong, asymptomatic viruria in immunocompetent individuals (Polo et al. 2004). Over 70% of adults harbour antibodies to BKV or JCV human Polyomaviruses (HPyVs) (Meng & Gerba 1996; Lukasik et al. 2000). The obligate host specificity and abundance of BKV and JCV in municipal sewage have led to the successful use of these viruses to indicate human faecal pollution in environmental water samples (Albinana-Gimenez et al. 2006; McQuaig et al. 2006; Brownell et al. 2007). Bofill-Mas et al. (2000) suggested that JCV would be a useful indicator of human sewage in water. Studies also showed that only HPyVs were detected in an environmental sample contaminated by faulty septic tanks, whilst the detection of AdV in the same system was sparse (McQuaig et al. 2009). The obligate host specificity of viruses such as HPyVs is advantageous for specific identification of human sources. JCV or BKV have been detected by using conventional PCR in raw sewage from all over the globe (Bofill-Mas et al. 2000, 2001; McQuaig et al. 2009; Kokkinos et al. 2011). Lower concentrations of HAdV and JCV were also found using qPCR in different treatment steps of the plants in absence of bacterial standards (Albinana-Gimenez et al. 2009). Therefore, Polyomavirus has been proposed to be a suitable indicator of fecal contamination in river water by the detection of nucleic acids of these viruses (Bofill-Mas et al. 2006). Other enteric viruses as indicators of water quality At this point a suitable index for the enteric viruses both in wastewater and drinking waters cannot be exclusively stated. Pepper mild mottle virus (PMMoV) (Rosario et al.


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2009), human Picobirnaviruses (hPBV) (Symonds et al. 2009), and Torque teno virus (TTVs) (Griffin et al. 2008) have been detected at substantial levels in human faeces. The researchers also propose that the detection of nucleic acids of these viruses might be a suitable indicator of faecal contamination in river water.


TTVs as an indicator of water quality TTV has a single-stranded DNA genome of approximately 3.8 kb in the family Circoviridae, genus Anellovirus (Hino 2002). TTV also demonstrates an extremely wide sequence divergence. At least 16 genotypes with evolutionary distance >0.30 have been described so far (Nishizawa et al. 1999). TTV can be detected by a conventional, single-round PCR assay (Takahashi et al. 1998; Biagini et al. 2001) and be quantified by qPCR (Haramoto et al. 2005; Carducci et al. 2009; Hamza et al. 2011). In vitro infection by TTV has been demonstrated in activated peripheral blood mononuclear cells and the Chang liver cell line after 2–3 day inoculation (Maggi et al. 2001; Mariscal et al. 2002; Desai et al. 2005). One potential problem with the use of human viruses as indicators is that the degree of infection and shedding in the human population at any given time might play the major roles in their abundance in wastewater. TTV is an enterically transmitted human virus, but it exhibits characteristics that distinguish it from other enteric viruses. TTV was first found in a serum sample of a non-A-E hepatitis patient (Nishizawa et al. 1997). Most papers have dismissed a significant role for TTV as an etiologic agent of significant diseases (Griffiths 1999; Simmonds et al. 1999). Transmission of TTV is primarily by the faecal oral route with high prevalence rate (Springfeld et al. 2000; Bendinelli et al. 2001) and with both persistent and transient infections (Okamoto et al. 1998). Vasilyev et al. (2009) found that about 94% of healthy individuals in the Russian population have more than 1000 TTV genome copies per 1 ml of blood and TTV viral load neither depends on gender, nor age. TTV was found to be spatially and temporally constant and abundant in inadequately treated water samples (Abe et al. 1999) as they were partially removed or in low number after treatments (Desai et al. 1999; Haramoto et al. 2005; Diniz-Mendes et al. 2008). Bibby et al. (2011) found that TTVs were highly abundant compared to adenoviruses in class B biosolids. TTV is also highly resistant to environmental stressors (Verani et al. 2006) and dry heat treatment (Takayama et al. 1999). TTV has constantly been found to co-locate with hepatitis A and E viruses (Vaidya et al. 2002; de Paula et al. 2007), rotavirus, enteric viruses and noroviruses (Verani et al. 2006). All the above evidence supports that TTV can be used as water quality indicators as proposed by Griffin et al. (2008). Haramoto et al. (2005) found that the concentration of coliforms did not correlate with the number of positive TTV samples. Carducci et al. (2009) were against using TTV qPCR as a water monitoring indicator due to the great variability in DNA copy counts and the reduction rates. Hamza et al. (2011) also reported that TTV does not seem to be a suitable indicator of faecal contamination in water compared to HAdV and PMMoV. PMMoV as an indicator of faecal pollution PMMoV is a positive-sense, single-stranded RNA virus that belongs to the Tobamovirus genus and infects various types of peppers (Capsicum spp.) (Fauquet et al. 2005).


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PMMoV RNA can be detected in environmental samples using a RT-PCR assay (Zhang et al. 2006), electron microscopy and ELISA (Colson et al. 2010). As PMMoV is not dependent on active human infection, Rosario et al. (2009) proposed this plant pathogen as an indicator of human faecal pollution due to its widespread abundance in wastewater. In addition, PMMoV was the most abundant virus found in a metagenomic survey of RNA viruses from human faeces (Zhang et al. 2006) and was present at high concentrations in raw sewage and treated wastewater from throughout the United States (Rosario et al. 2009). The PMMoV virions are extremely stable (Fauquet et al. 2005) and retain their infectivity for plants after passage through the human gut (Zhang et al. 2006). PMMoV virions enter the human system through processed pepper products like curry and sources and are excreted in human faeces into the environment (Zhang et al. 2006) suggesting that humans may serve as vectors. Despite the ubiquity of PMMoV in human faeces, this virus was not detected in the majority of animal faecal samples tested except in the chicken and seagull samples (Rosario et al. 2009; Hamza et al. 2011). This virus was detected in the seawater samples which contained other pathogens and faecal pollution indicators and was not found in non-polluted samples. PMMoV was detected in all river water and wastewater samples using quantitative PCR in Germany (Hamza et al. 2011). Before PMMoV can be used as a faecal indicator, similar studies are needed in other parts of the world with different dietary preferences and to determine the prevalence of PMMoV in sewage from each geographic region, as well as in other water sources. The correlation between the detection of PMMoV, as an infectious human pathogen, and in various wastewater treatment processes is also not clear (Rosario et al. 2009). More studies are needed the relations of the viral detection with infectivity are needed. Picobirnaviruses as an indicator of water quality Picobirnavirus (PBV) belongs to the family Picobirnaviridae. PBV are small, non-enveloped viruses, with a bi-segmented double-stranded RNA genome (Ludert et al. 1991; Bhattacharya et al. 2007). One of the standard and reliable laboratory diagnoses of PBV is to detect the bi-segmented double-stranded RNA genome by polyacrylamide gel electrophoresis and silver staining (Herring et al. 1982). RT-PCR has served as an alternative to polyacrylamide gel electrophoresis, for molecular detection and characterisation of PBV (Rosen et al. 2000). hPBV have been often detected in individual faecal samples (Zhang et al. 2006; Bhattacharya et al. 2007). PBV infections have been reported from diarrhoeal animal specimens and humans as well as from asymptomatic cases (Gallimore et al. 1995a, b). Among the Dutch, nearly 20% of clinical diarrhea samples contained hPBV sequences (van Leeuwen et al. 2010). Symonds and coworkers (2009) used PCR to detect 10 different viruses in raw sewage samples throughout the United States, and found that AdVs and picobirnaviruses were detected in all of raw sewage samples and 25% and 33% of final effluent samples, respectively. Therefore, hPBV, like hAdV, have been proposed as a potential indicator of faecal pollution (Symonds et al. 2009). Recently, Giordano et al. (2011) demonstrated that closely related PBV strains can infect both pigs and humans in Argentina and that epidemiology of PBVs is not species restricted. Ganesh et al. (2011) also found close genetic relatedness (>98% nucleotide identity) between genogroup I picobirnavirus in diarrhoeic foals and a human genogroup I PBV strain detected from the same part of India using sequence comparison and phylogenetic analysis of the RNA-dependent RNA polymerase gene. In addition, Hamza et al. (2011)


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could only detect hPBV in 25% of wastewaters samples, so they did not support hPBV as a suitable indicator of faecal contamination in water. Future outlook – enteric viruses as water quality indicators Diarrhoeal diseases remain one of the most common causes of mortality in the world. The causes of diarrhea are presumably of infectious origin in many cases. The identification of causative agents in these diseases commonly fails using traditional approaches. The precise knowledge of the routes of transmission for the diarrhoeal diseases is still incomplete. The Centers for Disease Control and Prevention (CDC) suggested that nearly 50% of all acute gastrointestinal illnesses are suspected to be due to virus(es) as the causative agent (CDC 1988). In recent years, many viruses including Norovirus, were identified as new diarrhoeal agents (Hewitt et al. 2007; Protano et al. 2008; Said et al. 2008; Khamrin et al. 2011). Researchers have developed a multiplex PCR assay to identify 10 viruses from stool samples in a single tube, so that other viruses, such as Aichi virus, parechovirus, and human bocavirus, have also been considered as agents associated with diarrhoea in humans (Pham et al. 2007, 2010; Reuter et al. 2009; Chow et al. 2010; Khamrin et al. 2011). Until scientists fill this gap of knowledge, current knowledge in water monitoring will be challenged continuously. The results from the water quality monitoring studies throughout the world clearly indicate that the treated wastewaters from industry or agriculture may still contain pathogenic viruses. In developing countries especially, recycled water has often been associated with the presence and re-emergence of waterborne diseases (Baggi et al. 2001). From the public health perspective, it is important to assess any potential risk to the exposed population by using bacterial indicators, probably an indirect viral indicator since viral health risks, are not correlated with the presence of enteric viruses or their abatement. It would therefore be advisable to add virological monitoring including coliphages and human viruses to enhance water quality monitoring programmes for wastewater management. At the present status, the enumerations of HAdV and HPyV measured by quantitative PCR seem most promising. The potential to use PMMoV as a water quality indicator cannot be ruled out. However, more studies to understand the relations of the viral detection with infectivity are needed. There is no “universal” assay for all viruses. Our knowledge about microbiology, the unseen living world, is very superficial. Metagenomic studies show that 70% of sequences obtained from the environment have no match with any database (Eukaryotes, Bacteria, viruses or Archae) (Raoult & Forterre 2008; Cantalupo et al. 2011). Another major drawback of using human enteric viruses as indicators is that, the presence of human enteric viruses in different potable water systems has not yet been successfully documented. Because of this gap of knowledge, it is impossible to understand the potential infectious hazards of our environment to cause human diseases (Raoult 2009). The selection of individual pathogens may also be misleading as each species can tolerate different environmental conditions. In addition, the presence of one may not indicate the presence of another. It is important to acknowledge the limitations of molecular studies as the viral load in the human population may differ for each virus and the abundance of these viruses fluctuates daily and seasonally in raw sewage. The results of this type of study may have been biased by the differential recovery efficiency of the concentration and nucleic acid isolation methods for different viral groups. The cost of virus assessments has to be reduced significantly before this application becomes a reality. As the costs of next-generation sequencing

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decrease, virus metagenomes may also be able to provide a guide for subsequent cell culture and quantitative pathogen analyses so that the viral pathogens are not neglected in risk assessments.


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