Abstract

Insufficient potable water resources and poorly treated drinking water quality are the world's number one cause for preventable morbidity and mortality from water-related pathogenic microorganisms. Pathogenic microorganisms, including mycotoxigenic fungi, have been identified in treated drinking water. This paper presents a review of mycotoxigenic fungi as a health risk to the public as these fungi are responsible for allergies, cancers and opportunistic infections mainly to immunocompromised patients. The exacerbating factors contributing to fungal presence in water distribution systems, factors that lead to fungi being resistant to water treatment and treated drinking water quality legislations are also discussed. This paper provides a review on the prevalence of mycotoxigenic fungi and their implications to public health in treated drinking water, and the need for inclusion in treated drinking water quality regulations.

INTRODUCTION

The environment is naturally rich in microbial diversity, most of which has not been studied yet and is currently unknown (Tekere et al. 2011; Fakruddin & Mannan 2013). Surface water, even when treated, has occasionally been associated with harmful infectious disease outbreaks, mostly caused by human and animal enteric pathogens (Bozzuto et al. 2010; Sibanda & Okoh 2013). Pathogenic microorganisms like bacteria, viruses and parasites are well known microbial water contaminants (Szewzyk et al. 2009). On the contrary, fungi have not been widely considered when discussing waterborne pathogens, but are now regarded as an emerging chronic water quality problem (Yamaguchi et al. 2007; Sonigo et al. 2011; Ashbolt 2015). Most countries' water quality legislations neither clearly address fungi, nor its perceived public health impacts or even set parameters for the control of fungi in treated drinking water (Oliveira et al. 2016; Babič et al. 2016, 2017). The European Union (EU) drinking water directive stipulates that treated drinking water should be ‘free from any microorganisms and parasites and from any substances which, in numbers or concentrations, constitute a potential danger to human health’ (Babič et al. 2017). While the intentions of the directive are clear and meant to protect public health, the fact that even in contaminated water, fungi are not usually present in ‘numbers or concentrations’ characteristic of bacteria and other microbial contaminants, has led to the omission of fungi from the battery of routine drinking water quality monitoring tests. Consequently, this has led to the lack of information about the possible human health impacts of its presence in drinking water sources (Babič et al. 2016).

MICROBIAL QUALITY OF TREATED DRINKING WATER

Microbial quality of water is usually monitored by measuring microorganisms using indicator organisms such as Escherichia coli (Obi et al. 2008). However, over-reliance on indicator bacteria to determine the sanitary and public health safety of treated drinking water has its own challenges, including the fact that other pathogens like enteroviruses and protozoa are more resistant to disinfection than E. coli, such that a zero count of E. coli does not essentially indicate the absence of other microorganisms (WHO 2011a; Meals et al. 2013). Heterotrophic plate count is the only indicator method for fungi as it is used to indicate changes in microbial concentration that show entry or re-growth in treated drinking water (Zerzghi et al. 2010; Babič et al. 2017). The problem, however, is that there is no regulatory value with the heterotrophic plate count, leading to a conclusion of compliance that is defined as a ‘no abnormal change’ which may ultimately not indicate the presence or absence of fungi (Babič et al. 2017). The available methods may not be reliable to detect and/or quantify all the waterborne pathogens including fungi that are also known to resist disinfection.

The WHO has an international obligation of issuing guidelines of universal application (WHO 2017) that also entail the issuing of directives, determination of legislation, setting of recommendations, and requires the testing and monitoring of drinking water quality (Babič et al. 2016). A preventative approach that only monitors the quality of treated drinking water, the ‘Water Safety Plans’ was endorsed by the WHO (WHO 2017). The plan considers factors that may contribute to endangering the quality of water from the source of water to the end user (José Figueras & Borrego 2010). While the WHO did not include fungi in the routine battery of microbiological parameters used to determine the quality of treated drinking water, it has labelled fungi as nuisance organisms because of taste and odour problems (Kinsey et al. 2003; Hageskal et al. 2006, 2009; Sonigo et al. 2011).

Other water quality legislations include those by the United State Environmental Protection Agency, an agency of the federal government of the United States created for the purpose of protecting human health and the environment by drafting and implementing regulations based on laws passed by Congress (Kanematsu & Barry 2016)). The EU Drinking Water Regulations (2014) recommend the application of water quality standards for Europe, European Union Countries and Northern Europe, and procedures for sampling frequency and methods of analysis (EU 2014). The above water quality legislative bodies also do not regulate the limits for fungi in treated drinking water, and the presence of fungi in tap water samples (Babič et al. 2016, 2017). The USEPA did look at the addition of microsporidia in drinking water regulations although it was later withdrawn from its ‘Contaminant Candidate List’ (Babič et al. 2017). Sweden is the only country that currently includes specific measures for the monitoring of micro-fungi in treated drinking water. The Swedish Drinking Water Guidelines specify a criterion of 100 CFU of micro-fungi per 100 mL in treated water as being fit for human consumption (Sammon et al. 2010).

The EU only issued a recommendation for mycotoxins to protect consumer's food and animal feeds from harmful effects of mycotoxins that became effective as legislation from the 1st October 2006 (Zain 2011). Mycotoxin regulations in food and feeds have been established in approximately 100 countries worldwide, with only 15 of these countries from Africa, to protect the consumer from harmful effects of these mycotoxins (Wagacha & Muthomi 2008). Ever since the 2003 FAO report which discovered that there were only aflatoxin regulations in Africa, there has been little or no progress regarding mycotoxin regulations in the continent (Misihairabgwi et al. 2017). Developing countries do not take into consideration mycotoxin regulations, predominantly due to lack of country-specific data of certain toxins, resources to obtain toxicological and exposure data and the analytical capacity to enforce the regulations (Wagacha & Muthomi 2008; Misihairabgwi et al. 2017).

OCCURRENCE AND PREVALENCE OF FUNGI IN TREATED DRINKING WATER

Fungi are natural inhabitants of composting plants, soil and water (Korzeniewska 2011; Calvo-Polanco et al. 2016). Terrestrial fungi are capable of migrating from soil into fresh water systems through animals, plants and soil (Wurzbacher et al. 1998; Magwaza et al. 2017). Fungal species like Fusarium and Aspergillus species have been identified to multiply in water reservoirs where they have been implicated in waterborne infections (Kanzler et al. 2007). Fungi in treated drinking water was first noticed in the 1960s and 1970s due to taste and odour problems, but was little considered as it was not the main focus for the analysis (Hageskal et al. 2009), and also because the contributory connection between the occurrence of fungi and water quality was not yet understood (Doggett 2000). The consumption of drinking water polluted by fungi had not been associated with serious disease casualties until studies performed in the 1980s revealed a number of cases linked to fungal contaminated treated drinking water (Hageskal et al. 2009).

Fungal deposition in water distribution systems is attributed to spores and not hyphae growth, which raises concerns that mycotoxins' production of taste and odour problems suggest that vegetative growth occurs in situ (Doggett 2000). In the water distribution system, the biomass of microorganisms suspended in the water phase is the main site of the occurrence of fungi belonging to moulds, including pathogenic species that are harmful to humans (Grabińska-Łoniewska et al. 2007). Fungi in treated drinking water have been identified in most countries, as shown in Table 1.

Table 1

Conducted surveys for fungi in treated drinking water globally

Country and city Year Source of samples Fungal isolates Reference 
Greece, Thessaloniki 1998 Tap water (hospital and community) Acremonium sp., Alternaria sp., Aspergillus sp., Aureobasidium sp., Bipolaris sp., Chaetomium sp., Chryosporium sp., Cladosporium sp., Curvularia sp., Doratomyces sp., Emmosia sp., Epicoccum sp., Eurotium sp., Exophiala sp., Fusarium sp., Gliocladium sp., Mucor sp., Penicillium sp., Phialophora sp., Pyrenocheta sp., Rhizopus sp., Scopulariopsis sp., Sepedonium sp., Stachybotrys sp., Trichoderma sp., Trichothecium sp. and Verticillium sp. Arvanitidou et al. (1999)  
UK, USA 1996 Surface water and distribution systems Acremonium sp., Alternaria sp., Aspergillus sp., Aureobasidium sp., Cladosporium sp., Epicoccum sp., Fusarium sp., Mucor sp., Penicillium sp., Phialophora sp., Pythium sp. and Trichoderma sp. Kinsey et al. (1998)  
Greece, 85 2000 Municipal water supplies of haemodialysis units Penicillium sp., Aspergillus sp., Verticillium sp., Actinomycetales sp., Trichothecium sp., Chrysosporium sp., Absidia sp., Acremonium sp., Alternaria sp., Aurebasidium sp., Basidiobolus sp., Botrytis sp., Chaetomium sp., Cladosporium sp., Cryptococcus sp., Curvularia sp., Doratomyces sp., Epicoccum sp., Eurotium sp., Fusarium sp., Geotrichum sp., Gliogladium sp., Helminthosporium sp., Microsporum sp., Monosporium sp., Mucor sp., Phoma sp., Pyrenocheta sp., Rhizopus sp., Scopulariopsis sp., Sepedonium sp. and Trichoderma sp. Arvanitidou et al. (2002)  
Poland 2000–2002 Water distribution system Aspergillus sp., Cladosporium sp., Fusarium sp., Fusidium sp., Geotrichum sp., Gonatobotrys sp., Paeciliomyces sp., Penicillium sp., Phialophora sp., Sclerotinia sp., Sesquicillium sp., Stachybotrys sp., Trichoderma sp. and Verticillium sp. Grabińska-Łoniewska et al. (2007)  
Germany, North Rhine-Westphalia 1998/9 (12 months) Drinking water Phialophora sp., Acremonium sp., Exophiala sp., Penicillium sp., Verticillium sp., Fusarium sp., Phoma sp., Aspergillus sp., Cladosporium sp., Chalara sp., Paecilomyces sp., Mucor sp., Geomyces sp., Ochroconis sp., Conidiobolus sp., Humicoala sp., Myrothecium sp., Tilletiopsis sp., Plectosporium sp. and Volutella sp. Göttlich et al. (2002)  
Portugal, Braga 2003/4 Tap water Acremonium sp., Alternaria sp., Aspergillus sp., Chaetomium sp., Cladosporium sp., Penicillium sp., Phialophora sp., Rhizopus sp. and Mycelia sterilia sp. Gonçalves et al. (2006)  
Pakistan Year n/a once, 30 samples Municipal water and fruit juice Aspergillus sp., Monodictys sp., Penicillium sp., Trichoderma sp., Drechslera sp. and Fusarium sp. Nazim et al. (2008)  
Australia 2007/8 Municipal water Cladosporium sp., Penicillium sp., Aspergillus sp., Trichoderma sp., Fusarium sp., Pithomyces sp., Alternaria sp., Paecilomyces sp., Acremonium sp., Epicoccum sp., Curvularia sp. and Asporogenous sp. Sammon et al. (2010)  
Saudi Arabia, Jeddah City Year n/a (once) Treated water from hospitals and private houses Alternaria sp., Aspergillus sp., Acremonium sp., Chaetomium sp., Cladosporium sp., Fusarium sp., Rhizopus sp., Mucor sp., Penicillium sp. and Trichoderma sp. Gashgari et al. (2013)  
Country and city Year Source of samples Fungal isolates Reference 
Greece, Thessaloniki 1998 Tap water (hospital and community) Acremonium sp., Alternaria sp., Aspergillus sp., Aureobasidium sp., Bipolaris sp., Chaetomium sp., Chryosporium sp., Cladosporium sp., Curvularia sp., Doratomyces sp., Emmosia sp., Epicoccum sp., Eurotium sp., Exophiala sp., Fusarium sp., Gliocladium sp., Mucor sp., Penicillium sp., Phialophora sp., Pyrenocheta sp., Rhizopus sp., Scopulariopsis sp., Sepedonium sp., Stachybotrys sp., Trichoderma sp., Trichothecium sp. and Verticillium sp. Arvanitidou et al. (1999)  
UK, USA 1996 Surface water and distribution systems Acremonium sp., Alternaria sp., Aspergillus sp., Aureobasidium sp., Cladosporium sp., Epicoccum sp., Fusarium sp., Mucor sp., Penicillium sp., Phialophora sp., Pythium sp. and Trichoderma sp. Kinsey et al. (1998)  
Greece, 85 2000 Municipal water supplies of haemodialysis units Penicillium sp., Aspergillus sp., Verticillium sp., Actinomycetales sp., Trichothecium sp., Chrysosporium sp., Absidia sp., Acremonium sp., Alternaria sp., Aurebasidium sp., Basidiobolus sp., Botrytis sp., Chaetomium sp., Cladosporium sp., Cryptococcus sp., Curvularia sp., Doratomyces sp., Epicoccum sp., Eurotium sp., Fusarium sp., Geotrichum sp., Gliogladium sp., Helminthosporium sp., Microsporum sp., Monosporium sp., Mucor sp., Phoma sp., Pyrenocheta sp., Rhizopus sp., Scopulariopsis sp., Sepedonium sp. and Trichoderma sp. Arvanitidou et al. (2002)  
Poland 2000–2002 Water distribution system Aspergillus sp., Cladosporium sp., Fusarium sp., Fusidium sp., Geotrichum sp., Gonatobotrys sp., Paeciliomyces sp., Penicillium sp., Phialophora sp., Sclerotinia sp., Sesquicillium sp., Stachybotrys sp., Trichoderma sp. and Verticillium sp. Grabińska-Łoniewska et al. (2007)  
Germany, North Rhine-Westphalia 1998/9 (12 months) Drinking water Phialophora sp., Acremonium sp., Exophiala sp., Penicillium sp., Verticillium sp., Fusarium sp., Phoma sp., Aspergillus sp., Cladosporium sp., Chalara sp., Paecilomyces sp., Mucor sp., Geomyces sp., Ochroconis sp., Conidiobolus sp., Humicoala sp., Myrothecium sp., Tilletiopsis sp., Plectosporium sp. and Volutella sp. Göttlich et al. (2002)  
Portugal, Braga 2003/4 Tap water Acremonium sp., Alternaria sp., Aspergillus sp., Chaetomium sp., Cladosporium sp., Penicillium sp., Phialophora sp., Rhizopus sp. and Mycelia sterilia sp. Gonçalves et al. (2006)  
Pakistan Year n/a once, 30 samples Municipal water and fruit juice Aspergillus sp., Monodictys sp., Penicillium sp., Trichoderma sp., Drechslera sp. and Fusarium sp. Nazim et al. (2008)  
Australia 2007/8 Municipal water Cladosporium sp., Penicillium sp., Aspergillus sp., Trichoderma sp., Fusarium sp., Pithomyces sp., Alternaria sp., Paecilomyces sp., Acremonium sp., Epicoccum sp., Curvularia sp. and Asporogenous sp. Sammon et al. (2010)  
Saudi Arabia, Jeddah City Year n/a (once) Treated water from hospitals and private houses Alternaria sp., Aspergillus sp., Acremonium sp., Chaetomium sp., Cladosporium sp., Fusarium sp., Rhizopus sp., Mucor sp., Penicillium sp. and Trichoderma sp. Gashgari et al. (2013)  

Fungi in treated drinking water from the various investigations, as shown in Table 1, demonstrates that the most prevalent fungi are Acremonium sp., Alternaria sp., Aureobasidium sp., Aspergillus sp., Chaetomium sp., Cladosporium sp., Epicoccum sp., Exophiala sp., Fusarium sp., Geotrichum sp., Mucor sp., Paecilomyces sp., Penicillium sp., Phialophora sp., Phoma sp., Rhizopus sp., Trichoderma sp. and Verticillium sp. Most of the fungal genera described in the studies are dematiaceous fungi which are capable of secreting melanin or melanin-like pigment in their cell walls. This makes them thick-walled species with hydrophobic spores which give them the advantage to resist water treatment (Sonigo et al. 2011; Auwal & Taura 2013; Al-gabr et al. 2014; Babič et al. 2017). These persistent fungi normally originate from soil, wood and decomposing plant material (Fox et al. 2016), which explains why they end up in raw water. Cladosporium sp., Penicillium sp., Fusarium sp., Penicillium sp., Aspergillus sp., Phoma sp., Epicoccum sp., Trichoderma sp., Acremonium sp., Exophiala sp., Alternaria sp. and Phialophora sp. are capable of producing mycotoxins and other secondary metabolites that produce toxic chemicals which impair water quality and become a threat to humans and animals (Pitt et al. 2000; Pereira et al. 2010; Sonigo et al. 2011).

Treated drinking water distribution systems and microbial quality of water

There are a number of microorganisms that are a source of drinking water problems, and some of the problems have been linked to the presence of fungi in the distribution systems (Doull et al. 1982; Fish et al. 2015). When fungi enter the water distribution system, it can be harboured by places in the network such as reservoirs that generate stratification, stagnation, dead zones, depletion of residual disinfectants and biofilm formation (Oliveira et al. 2016). These conditions, together with chemical-physical characteristics like high turbidity and temperature, pH, total organic carbon (TOC) and dissolved oxygen (DO), are favourable to microbial growth, making these environments at potential risk of water quality degradation by fungi (Oliveira et al. 2016). Fungi have been shown to enter the water distribution system in many ways that may be unavoidable such as mains interruptions, installations and maintenance (Doull et al. 1982). Others may include treatment breakthrough, water storage problems and cross-connections (Gashgari et al. 2013). When introduced in water, fungal species become established in biofilms in the inner surfaces of pipes (Mains 2008).

Many water companies have encountered operational and technological challenges that have, at times, led to consumer complaints because of fungi related problems (Grabińska-Łoniewska et al. 2007; Douterelo et al. 2014a, 2014b; Hurtado-McCormick et al. 2016). Fungi also produce secondary metabolites that exude organic acids which contribute to microbiological corrosion in water pipes (Grabińska-Łoniewska et al. 2007). This corrosion inhibits proper disinfection as accurate concentrations of chlorine residual in the treated distribution water system are altered (Sonigo et al. 2011). Even though water distribution systems are expected to act as contamination barriers in protecting the public's health against contamination by microorganisms, fungi together with viruses and protozoa have been shown to thrive in pipe networks (Speight 2002; Douterelo et al. 2014a, 2014b). Different types of materials including stainless steel, cast iron galvanised steel, copper and polyethylene have been used to manufacture water distribution pipes, and these materials often favour the formation of biofilm in the water distribution systems (Mulamattathil et al. 2014).

Fungi and microbial biofilms in water distribution systems

Microorganisms in the environment survive mainly by attaching themselves into and growing onto living and non-living surfaces from natural biotopes to non-natural appliances (Donlan 2001; Lahaye et al. 2016). Microorganisms produce extracellular polymers that facilitate attachment and matrix formation that help them attach and grow on surfaces (Donlan 2001). The micro-colonies of organisms that exist within extracellular matrices are called biofilms. A biofilm is described ‘as a layer of microorganisms in an aquatic environment held together in a polymetric matrix attached to a substratum such as pipes and sediment deposits’ in the water distribution system (Momba et al. 2000). Biofilms have a dynamic process of development on surfaces that entail attachment, growth, motility and extracellular polysaccharide production (Feng et al. 2015). Biofilms are formed inside the drinking water distribution systems the same way as plaque that forms on teeth (Mains 2008). Biofilms in water distribution systems provide a good habitat for microorganisms as they accumulate better in solid–liquid interfaces that enable them to be embedded in the gelatinous matrix of extracellular polymers excreted by the microorganisms leading to resistance of microbes from environmental stresses (Feng et al. 2015).

Microorganisms enter the distribution system after surviving water treatment processes, and due to recontamination and re-growth (Liu et al. 2016). Bacteria first colonise the pipe surfaces producing a slime layer that helps trap organic particles that can be used for food and energy. Many microorganisms including protozoa, algae, viruses, helminths and fungi then become attached to the biofilm (Donlan 2001; Mulamattathil et al. 2014). Fungal colony forming units (CFUs) held in biofilms have been shown to be 1,000 to 5,000 times greater than in water, although the density of fungal species in biofilms may vary according to locations (Sonigo et al. 2011). Filamentous fungi have also been isolated in biofilm samples in drinking water distribution systems in Colombian drinking water networks (Hurtado-McCormick et al. 2016).

To further protect fungi and other pathogenic microorganisms from destruction or elimination in water pipelines, bacterial populations in biofilms produce persister cells that neither grow nor die, and display resistance to antimicrobial agents (Berry et al. 2006; Feofilova et al. 2012; Scorzoni et al. 2017). The cells provide barriers that prevent disinfectants from penetrating as the disinfectant binds to the extracellular polymeric matrix rather than reacting with the cells. The enzymes in the matrix are also capable of biodegrading disinfectant residuals (Fish et al. 2016). A study by Sammon et al. (2011) showed reduced vulnerability of microorganisms in biofilms due to formation of a protected subpopulation of persister cells. Persister cells in fungi indicate that when the biofilm is destroyed by antimicrobial agents, a new biofilm, with a new sub-population of persisters is formed, which is, in reality, a modified phenotype, and that adhesion to a surface initiates dormancy (Ramage et al. 2012). Chlorine residual does not infiltrate thick biofilms and sediments as it may be biodegraded by the enzymes present (Mains 2008). To reduce the build-up of biofilms that harbour stubborn pathogens, maintenance of the water distribution systems must take into account flushing, pigging or water/air scouring of the pipes to flush out sediments that encourage proliferation of fungal populations (Alegre et al. 2010). Fungal mycelia growing on substrate are dense and sporulation is more prolific than the growths of fungi observed on pipe wall samples (Sammon et al. 2011). Biofilm formation not only affects the quality of water by reducing the effectiveness of chlorine residual but raises the costs of maintenance for the distribution system (van der Kooij 1998; Boe-Hansen et al. 2003). Biofilm recalcitrance towards disinfection may contribute to the dissemination of fungi to public drinking water (Göttlich et al. 2002).

PUBLIC HEALTH IMPLICATIONS OF MYCOTOXIGENIC FUNGI IN TREATED DRINKING WATER

The presence of fungi in treated drinking water and its health impacts were not taken seriously until cases caused by fungal contaminated water were reported in Finland and Sweden during the 1980s and 1990s (Dufour et al. 2003; Boe-Hansen et al. 2003). Waterborne filamentous fungi are known to act as pathogens or allergens that have adverse impacts on human health, and mostly on immune-compromised patients (Oliveira et al. 2016). Transmission of pathogenic microorganisms by drinking water has continued to be a major cause of water-related illnesses, as confirmed by the frequencies of outbreaks reported around the world (WHO 2011b). Fungal infections are a challenge to cure as fungal cells are eukaryotic, just like human cells (Yamaguchi et al. 2007). Pathogenic fungi are believed to have caused hostile infections that have contributed to high mortality rates (Arvanitidou et al. 1999; Khan et al. 2010; Mayer et al. 2013; Tsui et al. 2016; Pal 2017).

Fungal infections were quite low from the late 1950s and early 1960s, yet over the past two decades, fungal infections have dramatically increased as they are easily diagnosed (Khan et al. 2010). Most of the fungi that were identified in Table 1 are dematiaceous fungi responsible for causing a number of cutaneous and subcutaneous infections including invasive and contagious infections (Pfaller & Diekema 2004). A significant proportion of waterborne illnesses related to fungi are likely to go undetected by the communicable disease surveillance and reporting systems. The possible health impacts caused by fungi in treated water are still not well documented, although protective measures are recommended for people who are at high risk (Hageskal et al. 2009), especially the increasing population of patients having an impaired immune system, as their immune effector cells become compromised allowing fungi to colonise and attack the human tissues, leading to more complications (Oliveira et al. 2013).

Fungi have been implicated in a number of diseases causing allergies, respiratory illness, cutaneous infection and life-threatening meningitis (Pfaller & Diekema 2004; Sulaiman et al. 2014). Alternaria sp., Cladosporium sp., Aspergillus sp., Penicillium sp. and Fusarium sp. have been linked to allergies and respiratory illness (Korzeniewska 2011; Máiz et al. 2018). Cryptococcus and Candida cause meningitis (Black & Baden 2007), with the Candida species responsible for cutaneous infections (Khan et al. 2010; Volk 2013). Taste and odour problems in water are caused by Aspergillus sp., Acremonium sp., Phialophora sp. and Penicillium sp. (Hageskal et al. 2006; Sonigo et al. 2011). Fungi such as Rhizopus, Fusarium, Alternaria, Aspergillus and Penicillium produce mycotoxins that are harmful to public health as these mycotoxins are carcinogenic and have the ability to impair the immune system (Bhat et al. 2010; Sonigo et al. 2011; Magwaza et al. 2017). Mycotoxins of great concern for public health include aflatoxins (AF), ochratoxins (OT), trichothecenes, zearalenone (ZEN), fumonisins (F), tremorgenic toxins, and ergot alkaloids (Zain 2011). The types of infections caused by mycotoxigenic fungi depend on the type of mycotoxin, the concentration and length of exposure; as well as age, health, and sex of the exposed individual (Bennett & Klich 2003). Mycotoxins found in water may be extremely diluted and may not be of major concern, but their concentrations may increase resulting in hazardous levels to human health, particularly when water is stored in reservoirs for longer periods (Siqueira 2011). The absence of toxigenic fungi in treated drinking water may not provide assurance that the water is free of mycotoxins, as mycotoxins may persevere long after the fungi has died (Pitt et al. 2000). Mycotoxins have serious and chronic effects on humans and animals, as many of them are believed to be carcinogenic, cytotoxic, mutagenic and may lead to immunosuppressive complexes (Arroyo-Manzanares et al. 2015). Although now there are reports regarding advances in antifungal therapy, it is worth noting that the number of cases of infection and antifungal resistance are also alarmingly high, and the control of antifungal disease does not indicate any possibilities of being achieved soon (Araj et al. 2015; Meirelles et al. 2017; Rodrigues et al. 2017; Pellon et al. 2018). Treated drinking water quality without pathogenic microorganisms including fungi is very critical for the health of all humans and mostly those with immunodeficiency conditions. Table 2 shows the toxic effects of some of the mycotoxins, producing genera and health effects.

Table 2

Fungal mycotoxins, producing fungal genera and health effects

Mycotoxin Genera Health effects Reference 
Aflatoxins Aspergillus sp. Human carcinogenic and others are hepatotoxic, aflatoxicosis, aspergillosis, nephropathy, teratogenic effect and decreases resistance and susceptibility to HIV, TB, and other opportunistic infections Campbell et al. (2004), Shadanaika (2005), Bloom (2008), Mukherjee (2012) and Šegvić et al. (2013)  
Fumonisins Fusarium sp. Oesophageal cancer Bennett (1987), Pitt (2000) and Shadanaika (2005)  
Citrinin Aspergillus sp., Penicillium sp. and Monascus sp. Nephrotoxic, teratogenic Shadanaika (2005)  
Ochratoxin A Aspergillus sp. and Penicillium sp. Nephrotoxic, hepatotoxic, teratogenic and carcinogenic Abbott (2002), Shadanaika (2005) and Dao et al. (2005)  
Patulin Aspergillus sp., Penicillium sp., Paecilomyces sp. and Byssochlamys sp. Immune toxicity, cytotoxic; tremorgenic and pulmonary oedema Campbell et al. (2004), Shadanaika (2005), Bloom (2008), and Puel et al. (2010)  
Sterigmatocystin Aspergillus sp. Carcinogenic Shadanaika (2005), and Coelho et al. (2010)  
Cyclopiazonic acid Aspergillus sp. and Penicillium sp. Convulsions Shadanaika (2005) and WHO (2011b)  
Trichothecenes Fusarium sp. Trichoderma sp. Toxic aleukia Shadanaika (2005)  
Deoxynivalenol Fusarium sp. Anorexia, nausea, vomiting, headache, abdominal pain, diarrhoea, chills, giddiness and convulsions Pitt (2000) and WHO (2011b)  
T-2 toxin Fusarium sp. Alimentary toxic aleukia WHO (2011b)  
Zearalenone Fusarium sp. Carcinogenic Kuhn & Ghannoum (2003)  
Ergot alkaloids Cladosporium sp. Gangrenous and convulsive forms of ergotism in humans Hussein & Brasel (2001) and Abbott (2002)  
Penicillic acid Penicillium sp. Carcinogenic Abbott (2002)  
Tenuazonic acid, alternariol, altenuene, and altertoxin-1 Alternaria sp. Inhalation allergy problems and mycotoxicoses Shadanaika (2005); Volk (2013) and Buse et al. (2013)  
Ergotamine Claviceps purpurea Neurotoxins (poisonous to nerves) WHO (2011b)  
Brefeldin Phoma sp. An antibiotic, responsible for reducing cancer stem cell activities, and inhibiting migration ability in human breast cancer Abbott (2002)  
Rhizonin Rhizopus sp. Hepatotoxic Abbott (2002) and Partida-Martinez et al. (2007)  
Mycotoxin Genera Health effects Reference 
Aflatoxins Aspergillus sp. Human carcinogenic and others are hepatotoxic, aflatoxicosis, aspergillosis, nephropathy, teratogenic effect and decreases resistance and susceptibility to HIV, TB, and other opportunistic infections Campbell et al. (2004), Shadanaika (2005), Bloom (2008), Mukherjee (2012) and Šegvić et al. (2013)  
Fumonisins Fusarium sp. Oesophageal cancer Bennett (1987), Pitt (2000) and Shadanaika (2005)  
Citrinin Aspergillus sp., Penicillium sp. and Monascus sp. Nephrotoxic, teratogenic Shadanaika (2005)  
Ochratoxin A Aspergillus sp. and Penicillium sp. Nephrotoxic, hepatotoxic, teratogenic and carcinogenic Abbott (2002), Shadanaika (2005) and Dao et al. (2005)  
Patulin Aspergillus sp., Penicillium sp., Paecilomyces sp. and Byssochlamys sp. Immune toxicity, cytotoxic; tremorgenic and pulmonary oedema Campbell et al. (2004), Shadanaika (2005), Bloom (2008), and Puel et al. (2010)  
Sterigmatocystin Aspergillus sp. Carcinogenic Shadanaika (2005), and Coelho et al. (2010)  
Cyclopiazonic acid Aspergillus sp. and Penicillium sp. Convulsions Shadanaika (2005) and WHO (2011b)  
Trichothecenes Fusarium sp. Trichoderma sp. Toxic aleukia Shadanaika (2005)  
Deoxynivalenol Fusarium sp. Anorexia, nausea, vomiting, headache, abdominal pain, diarrhoea, chills, giddiness and convulsions Pitt (2000) and WHO (2011b)  
T-2 toxin Fusarium sp. Alimentary toxic aleukia WHO (2011b)  
Zearalenone Fusarium sp. Carcinogenic Kuhn & Ghannoum (2003)  
Ergot alkaloids Cladosporium sp. Gangrenous and convulsive forms of ergotism in humans Hussein & Brasel (2001) and Abbott (2002)  
Penicillic acid Penicillium sp. Carcinogenic Abbott (2002)  
Tenuazonic acid, alternariol, altenuene, and altertoxin-1 Alternaria sp. Inhalation allergy problems and mycotoxicoses Shadanaika (2005); Volk (2013) and Buse et al. (2013)  
Ergotamine Claviceps purpurea Neurotoxins (poisonous to nerves) WHO (2011b)  
Brefeldin Phoma sp. An antibiotic, responsible for reducing cancer stem cell activities, and inhibiting migration ability in human breast cancer Abbott (2002)  
Rhizonin Rhizopus sp. Hepatotoxic Abbott (2002) and Partida-Martinez et al. (2007)  

Occurrence and concentration of mycotoxins in treated drinking water

Mycotoxins are fungal poisons that are produced as secondary metabolites by the mycelial structure of filamentous fungi as well as spores (Gupta et al. 2015). Not all fungi produce mycotoxins, as most mycotoxin producing species are filamentous ascomycetes, basidiomycetes and deuteromycetes with Penicillium, Aspergillus and Furasium being the most mycotoxin-producing genera (Abbott 2002). These mycotoxins do not have any biochemical implications in fungal growth and their development (Hussein & Brasel 2001). Fungal growth and mycotoxin production are the consequence of an interaction among the fungus, the host and the environment (Atanda et al. 2011). The right combination of these factors determines the amount of colonisation of the substrate, the type and amount of mycotoxin produced (Pitt et al. 2000). The synthesis of any particular mycotoxin depends not only on the species but also on the strain (Pitt et al. 2000). Although the chemical structures of mycotoxins vary significantly, they are generally low molecular mass organic compounds. Due to the fact that mycotoxins are minute and fairly stable molecules, they become very problematic to eliminate and this makes it easy for them to enter the food and feed chain while keeping their toxic properties (Omar 2013). Mycotoxins may be ingested through food or water containing poisonous fungi (Volk 2013) or ingested as mycotoxins secreted by fungi without eating the fungus itself. If ingested, mycotoxins cause tissue destruction, angioinvasion, thrombosis, infarction and other manifestations of mycosis (Campbell et al. 2004).

Mycotoxigenic fungi have been reported in treated drinking water (Paterson & Lima 2008; Al-gabr et al. 2014). While mycotoxin concentrations can be low in water because of dilution, water retention in storage tanks, the long distances water travels in distribution systems, depletion of chlorine residual and the resistance of some of the fungi to disinfection can cause mycotoxin concentrations to increase to unsafe amounts in drinking water (Barriga et al. 2012). Parameters such as temperature and pH also encourage growth and persistence of fungi in water (Hussain et al. 2011). Small amounts of mycotoxins consumed regularly could be harmful to human health (Hageskal et al. 2009).

FUNGAL–BACTERIA INTERACTIONS AND CORRELATIONS IN WATER DISTRIBUTION SYSTEMS

It is key to ascertain the prevalence of fungi and make deductions as to the interactions and correlations between fungi and bacteria and any need to include fungi in drinking water standards. Bacteria and fungi exist and interact in many environments as they often share a common substrate. Fungal interaction with bacteria range from disorderly polymicrobial assemblies to closely related symbiotic associations of fungal hyphae and bacterial cells (Frey-Klett et al. 2011). Bacteria are responsible for the initial construction of biofilms while fungi colonise pre-established bacterial biofilms, which is a form of commensalism as one benefits while the other is unaffected due to different ecological requirements of the two organisms (Sonigo et al. 2011).

Fungi and bacteria are believed to positively use their competitive interactions during fungal decomposition of unmanageable organic matter (De Boer et al. 2005). Fungi produce most enzymes because they have higher biomass and bacteria benefit from the enzymatic capacity of fungi, in particular when it comes to enzymes involved in degrading plant polymers (Mille-lindblom 2005). However, some fungal species tend to suppress bacterial growth through production of antibacterial substances, for example, penicillin from the fungus Penicillium notatum (Mille-Lindblom et al. 2006). Studies have found different relationships between fungi and bacteria depending on bacterial and fungal species compositions and biological mechanisms affecting the relationship (Sonigo et al. 2011). Understanding the interactions between bacteria and fungi in water will give an insight as to whether the presence of certain bacterial species in water can be used as an indicator of its fungal content (Gonçalves et al. 2006). To date, no conclusive correlation has been found between indicator organisms such as E. coli and other coliforms to fungi in treated drinking water systems (Oliveira et al. 2016). This is because fungi can resist disinfection while coliform bacteria would be eradicated (Kinsey et al. 2003). This lack of correlation between coliforms and fungi presence in drinking water distribution systems may mean that there is a possibility for bacteriologically safe water to contain some pathogenic fungi (Sonigo et al. 2011). Ashbolt et al. (2001) argued that with the change in monitoring standards, more indicators of process efficiency are required rather than the reliance on the ‘old-style’ E. coli as an indicator. However, a point worth noting is that fungi often colonise pre-established bacterial biofilms and, as such, the correlations deductible in biofilms are not necessarily the same as for water samples.

WATER TREATMENT PROCESSES AND INACTIVATION OF FUNGI

Water is crucial for the sustenance of life and, therefore, access to safe drinking water is necessary for human health and for economic development (WHO 2008; UN Water 2015). The objectives for water treatment are not only to produce water that is acceptable in terms of being aesthetically pleasing in appearance (clearness) and taste and odour (Momba et al. 2008), but the initial aim is the destruction or inactivation of pathogenic microorganisms to prevent the spread of waterborne diseases (EPA 2013). In general, most water utilities treat water via coagulation, flocculation, sedimentation and filtration, that are designed with the main objective of removing microbial pathogens with the addition of disinfection such as chlorine as a significant component in water treatment (Adam et al. 1998). Literature has revealed that water treatment plant processes do not completely remove all pathogenic microorganisms, including fungi in water that end up in treated water distribution systems to the consumer point of use (Sammon et al. 2011; Pereira et al. 2013).

Coagulation and flocculation

Coagulants aid in destabilising colloidal particles in water to promote agglomeration to form larger sized particles known as flocculants (flocs) which can be effectively removed by sedimentation or flotation (Al-mamun et al. 2016). Sedimentation and flotation processes remove a great many of the microorganisms including fungi as they are trapped within the particles and settle to the bottom in sedimentation tanks or float out in flotation tanks, where they are eventually disposed of with the sludge (Kinsey et al. 2003). Most of the time there are light broken flocs or non-flocculated colloidal particles that are suspended in water (Jun et al. 2009; Oyegbile et al. 2016; Rasteiro et al. 2016; Marques et al. 2017), to which, microorganisms have the ability to attach themselves. These suspended particles, depending on the quality of water, end up being transferred to the filtration process (Thupaki et al. 2013).

Filtration

It is very important that all the particles are removed to maintain turbidity (particles suspended in water) of less than one nephelometric turbidity units (1 NTU) for effective disinfection of water (WRC 2002). Rapid sand filters are commonly used although they do not have enough retention time to remove all microorganisms from water which are hidden in the particles (O'Connor & O'Connorr 2001). Fungi can grow attached to a substrate and colonise filters in water treatment plants giving them a good opportunity to resist water treatment (Hageskal et al. 2009). If fungi survive sedimentation and flocculation, rapid sand filtration does not become an effective treatment for fungi (Kinsey et al. 2003) as these filters have been shown to partially remove microorganisms, especially fungi that end up in the distribution system (Kinsey et al. 2003). After filtration, the final and most trusted treatment process for destroying pathogenic microorganisms is disinfection (Tellen et al. 2010).

Disinfection

The use of disinfection in water treatment as a public health measure has shown a major decline in people contracting water-related diseases from drinking water (EPA 2013). Fungi and other bacteria have the ability to become dormant in order to preserve their lives when conditions are no longer conducive. But when the conditions become favourable again, they return to their normal state, recovering their metabolic activity and starting the process of spore germination (Luu et al. 2015). This is the phenomenon with the melanised thick-walled fungal species that are more resistant to water treatment and disinfection (Hageskal et al. 2012). When the turbidity of water is greater than 1 NTU usually with organic particles, the particles interfere with disinfection as microorganisms get entrapped in the particles or adsorbed onto particle surfaces (Spellman 2014), resulting in microorganisms being protected from disinfection that is required for their elimination (Al-berfkani et al. 2014). Different fungal species vary in their resistance to disinfection. Penicillium and Aspergillus species are more resistant to chlorine disinfection than the Cladosporium and Phoma species (Pereira et al. 2013). Ozone and UV radiation are more capable in the destruction of many pathogenic organisms than chlorine, but their disadvantages are high costs and mostly the inability to have residual that persists long enough to prevent the re-growth of microorganisms in the distribution system (Freese & Nozaic 2004).

Ozone

Ozone inactivates fungal species by causing an irreversible cellular damage (Rojas-Valencia 2011). There are resistant species to ozone like Trichoderma viride that is slightly affected only in elevated concentrations and Penicillium spinulosum which is the most resistant due to its hydrophobic surface (Hageskal et al. 2012).

UV radiation

Fungi with pigmented spores such as Aspergillus and Penicillium have better defence against radiation and are not responsive to UV treatment (Hageskal et al. 2009). The radiation cannot destroy fungal species even in slightly turbid water as the fungi tend to be harboured within the particles and escape disinfection (EPA 2013). Furthermore, disinfection methods by exposing some species of fungi to UV light may seem futile as strongly melanised spores of Aureobasidium pulullans and Aureobasidium melanogenum have shown resistance to elongated radiation interactions (Castiglia & Kuhar 2017).

Free chlorine

Chlorine is the mainly used form of disinfection in most water treatment plants in many countries. Although chlorine is widely used as a strong oxidant, that is reliable in removing or the inactivation of many harmful microorganisms in water when evaluated against other microorganisms, fungi were discovered to be more resistant to chlorine inactivation than the commonly used indicator organism E. coli (Luyt et al. 2012; Oliveira et al. 2013; Al-berfkani et al. 2014).

CONCLUSION

Water treatment is very important in controlling pathogenic microorganisms from reaching consumers. There are guidelines in place to test and monitor pathogenic microorganisms like bacteria, viruses and parasites in treated drinking water from the water source to the final drop of the tap. Fungi have been left out of the battery of drinking water quality monitoring parameters, yet scientific literature has proven the presence of fungi and their mycotoxins in treated drinking water. Melanised and slimy conidia have been found in treated water distribution systems with a prevalence of Cladosporium, Phoma, Alternaria, Aspergillus, Penicillium, Exphiala, Fusarium, Acremonium, Exophiala and Phialophora and that has the general capacity to resist disinfection regimes (Göttlich et al. 2002). The growing list of documented pathogenic fungi from treated drinking water can no longer be ignored as water contaminants. The potential health impact of waterborne fungi is still not clear, while precautions are needed for high-risk patients.

In many countries, little focus has been centred on the occurrence of fungi and their mycotoxins in treated drinking water supply networks. Monitoring and keeping the amount of fungi under surveillance after water treatment and in distribution systems is fundamental in guiding against harm to human health, and also to improve the aesthetic quality of water in relationship to taste and odour. This can also include the need to evaluate the removal of secondary metabolites by drinking water treatment processes. Although routine examination of fungi can be difficult as cautious and experienced personnel are key, nevertheless, this cannot be disregarded anymore as fungi influence water quality in many ways.

ACKNOWLEDGEMENTS

The authors are grateful to the Water Research Commission (WRC), Pretoria, South Africa for funding this study under the WRC Project No. K5/2568 and the Department of Environmental Sciences, University of South Africa for hosting the research.

REFERENCES

REFERENCES
Abbott
S. P.
2002
Mycotoxins and indoor molds
.
Indoor Environment Connections
3
(
4
),
14
24
.
Adam
K.
,
Heath
R. G. M.
&
Steynberg
M. C.
1998
Invertebrates as biomonitors of sand-filter efficiency
.
Water SA
24
(
1
),
43
48
.
Al-berfkani
M. I.
,
Zubair
A. I.
&
Bayazed
H.
2014
Assessment of chlorine resistant bacteria and their susceptibility to antibiotic from water distribution system in Duhok province
.
Journal of Applied Biology and Biotechnology
2
(
6
),
10
13
.
Alegre
H.
,
Pitchers
R.
,
Saegrov
S.
,
Vreeburg
J.
,
Bruaset
S.
&
Rostum
J.
2010
Water Quality-Driven Operation and Maintenance of Drinking Water Networks. Best Management Practice
.
Techneau WA5.6 (D 5.6.7)
.
Al-gabr
H. M.
,
Zheng
T.
&
Yu
X.
2014
Occurrence and quantification of fungi and detection of mycotoxigenic fungi in drinking water in Xiamen City, China
.
The Science of the Total Environment
466–467
,
1103
1111
.
Al-mamun
A.
,
Alam
Z.
&
Raus
R. A.
2016
Fungal coagulant for reduction of water turbidity
. In
3rd International Conference on Civil, Biological and Environmental Engineering (CBEE-2016)
,
February 4–5, 2016
,
Bali, Indonesia
, pp.
10
12
.
Araj
G. F.
,
Asmar
R. G.
&
Avedissian
A. Z.
2015
Candida profiles and antifungal resistance evolution over a decade in Lebanon
.
Journal of Infection in Developing Countries
9
(
9
),
997
1003
.
Arroyo-Manzanares
N.
,
Huertas-Pérez
J. F.
,
Gámiz-Gracia
L.
&
García-Campaña
A. M.
2015
Simple and efficient methodology to determine mycotoxins in cereal syrups
.
Food Chemistry
177
,
274
279
.
Arvanitidou
M.
,
Kanellou
K.
,
Constantinides
T. C.
&
Katsouyannopoulos
V.
1999
The occurrence of fungi in hospital and community potable waters
.
Letters in Applied Microbiology
29
(
2
),
81
84
.
Ashbolt
N.
,
Grabow
W.
,
Snozzi
M.
2001
Indicators of microbial water quality
. In:
Water Quality: Guidelines, Standards and Health
(
Fewtrell
L.
&
Bartram
J.
, eds).
IWA Publishing and WHO, London, UK
, pp.
289
316
.
Atanda
S. A.
,
Pessu
P. O.
,
Agoda
S.
,
Isong
I. U.
,
Adekalu
O. A.
,
Echendu
M. A.
&
Falade
T. C.
2011
Fungi and mycotoxins in stored foods
.
African Journal of Microbiology Research
5
(
25
),
4373
4382
.
Auwal
H.
&
Taura
D.
2013
Prevalence of moulds in households drinking water of some local government areas of Kano
.
Nigeria. Greener Journal of Biological Sciences
3
(
5
),
179
186
.
Babič
M. N.
,
Zalar
P.
,
Ženko
B.
,
Džeroski
S.
&
Gunde-Cimerman
N.
2016
Yeasts and yeast-like fungi in tap water and groundwater, and their transmission to household appliances
.
Fungal Ecology
20
,
30
39
.
Babič
M. N.
,
Gunde-Cimerman
N.
,
Vargha
M.
,
Tischner
Z.
,
Magyar
D.
,
Veríssimo
C.
,
Sabino
R.
,
Viegas
C.
,
Meyer
W.
&
Brandão
J.
2017
Fungal contaminants in drinking water regulation? A tale of ecology, exposure, purification and clinical relevance
.
International Journal of Environmental Research and Public Health
14
(
6
),
636
.
Barriga
L. F. S.
,
León
A. J. M.
,
Narvaez
D.
,
Pérez
M. F. L.
,
Groot
H.
&
Rodríguez
M. S. S.
2012
Toxicological and Products Formation Approach of Fungal Organic Matter From Drinking Water Distribution System
.
Environmental Engineering Research Center
,
Bogotá
,
Colombia
.
Bennett
J. W.
&
Klich
M.
2003
Mycotoxins
.
Clinical Microbiology Reviews
16
(
3
),
497
516
.
Berry
D.
,
Xi
C.
&
Raskin
L.
2006
Microbial ecology of drinking water distribution systems
.
Current Opinion in Biotechnology
17
(
3
),
297
302
.
Bhat
R.
,
Rai
R. V.
&
Karim
A. A.
2010
Mycotoxins in food and feed: present status and future concerns
.
Comprehensive Reviews in Food Science and Food Safety
9
(
1
),
57
81
.
Bloom
E.
2008
Mycotoxins in Indoor Environments. Determination Using Mass Spectrometry
.
Doctoral dissertation
,
Faculty of Medicine, Lund University
,
Sweden
.
Boe-Hansen
R.
,
Martiny
A. C.
,
Arvin
E.
&
Albrechtsen
H.-J.
2003
Monitoring biofilm formation and activity in drinking water distribution networks under oligotrophic conditions
.
Water Science & Technology
47
(
5
),
91
97
.
Bozzuto
G.
,
Ruggieri
P.
&
Molinari
A.
2010
Molecular aspects of tumor cell migration and invasion
.
Ann Ist Super Sanità
48
(
4
),
66
80
.
Buse
H. Y.
,
Lu
J.
,
Struewing
I. T.
&
Ashbolt
N. J.
2013
Eukaryotic diversity in premise drinking water using 18S rDNA sequencing: implications for health risks
.
Environmental Science and Pollution Research
20
(
9
),
6351
6366
.
Calvo-Polanco
M.
,
Sánchez-Castro
I.
,
Cantos
M.
,
García
J. L.
,
Azcón
R.
,
Ruiz-Lozano
J. M.
,
Beuzón
C. R.
&
Aroca
R.
2016
Effects of different arbuscular mycorrhizal fungal backgrounds and soils on olive plants growth and water relation properties under well-watered and drought conditions
.
Plant Cell and Environment
39
(
11
),
2498
2514
.
Campbell
A. W.
,
Thrasher
J. D.
,
Gray
M. R.
&
Vojdani
A.
2004
Mold and mycotoxins: effects on the neurological and immune systems in humans
.
Advances in Applied Microbiology
55
,
375
406
.
Castiglia
V. C.
&
Kuhar
F.
2017
Deterioration of expanded polystyrene caused by Aureobasidium pullulans var. melanogenum
.
Review Argent Microbiology
47
(
3
),
256
260
.
Coelho
M. A. Z.
,
Amaral
P. F. F.
&
Belo
I.
2010
Yarrowia lipolytica: an industrial workhorse
.
Current Research, Technology and Education Topics in Applied Microbiology and Microbial Biotechnology
2
,
930
944
.
Dao
H. P.
,
Mathieu
F.
&
Lebrihi
A.
2005
Two primer pairs to detect OTA producers by PCR method
.
International Journal of Food Microbiology
104
(
1
),
61
67
.
De Boer
W.
,
Folman
L. B.
,
Summerbell
R. C.
&
Boddy
L.
2005
Living in a fungal world: impact of fungi on soil bacterial niche development
.
FEMS Microbiology Reviews
29
,
795
811
.
Doggett
M. S.
2000
Characterization of fungal biofilms within a municipal water distribution system
.
Applied and Environmental Microbiology
66
(
3
),
11
14
.
Donlan
R. M.
2001
Biofilm formation: a clinically relevant microbiological process
.
Clinical Infectious Diseases
33
(
8
),
1387
1392
.
Doull
J.
,
Andelman
J. B.
,
Buhler
D. R.
,
Characklis
W. G.
,
Christman
R. F.
,
Cohen
S. D.
,
Engelbrecht
R. S.
,
Hayes
A. W.
,
Hughes
J. M.
,
Olivieri
V. P.
,
Pike
M. C.
,
Schnell
R. C.
,
Street
J. C.
&
Tate
C. H.
1982
Drinking Water and Health. National Research Council (US) Safe Drinking Water Committee
.
National Academies Press
,
Washington, DC
,
USA
, pp.
1
312
.
Douterelo
I.
,
Boxall
J. B.
,
Deines
P.
,
Sekar
R.
,
Fish
K. E.
&
Biggs
C. A.
2014a
Methodological approaches for studying the microbial ecology of drinking water distribution systems
.
Water Research
65
,
134
156
.
Dufour
A.
,
Snozzi
M.
,
Koster
W.
,
Bartram
J.
,
Ronchi
E.
&
Fewtrell
L.
2003
Assessing Microbial Safety of Drinking Water: Improving Approaches and Methods
.
IWA Publishing/WHO/OECD
,
London
,
UK
.
European Union (EU)
.
2014
European Union (Drinking Water) Regulations 2014, S.I. No. 122 of 2014
.
Environmental Protection Agency (EPA)
2013
Water Treatment Manual: Disinfection
.
The Environmental Protection Agency-Ireland
,
Wexford
,
Ireland
(11/11/1000), 1–200
.
Fakruddin
M.
&
Mannan
K. S. B.
2013
Methods for analyzing diversity of microbial communities in natural environments
.
Ceylon Journal of Science (Biological Sciences)
42
(
1
),
19
33
.
Feng
G.
,
Cheng
Y.
,
Wang
S.
,
Borca-Tasciuc
D. A.
,
Worobo
R. W.
&
Moraru
C. I.
2015
Bacterial attachment and biofilm formation on surfaces are reduced by small-diameter nanoscale pores: how small is small enough?
Biofilms and Microbiomes
1
,
15022
.
Feofilova
E. P.
,
Ivashechkin
A. A.
,
Alekhin
A. I.
&
Sergeeva
Y. E.
2012
Fungal spores: dormancy, germination, chemical composition, and role in biotechnology (review)
.
Applied Biochemistry and Microbiology
48
(
1
),
1
11
.
Fish
K. E.
,
Collins
R.
,
Green
N. H.
,
Sharpe
R. L.
,
Douterelo
I.
,
Osborn
A. M.
&
Boxall
J. B.
2015
Characterisation of the physical composition and microbial community structure of biofilms within a model full-scale drinking water distribution system
.
PLoS ONE
10
(
2
),
1
22
.
Fox
A. R.
,
Houser
K. H.
,
Morris
W. R.
&
Walton
R. C.
2016
Dematiaceous fungal endophthalmitis: report of a case and review of the literature
.
Journal of Ophthalmic Inflammation and Infection
6
(
1
),
43
.
Freese
S. D.
&
Nozaic
D. J.
2004
Chlorine: is it really so bad and what are the alternatives?
Water SA
30
(
5
),
566
572
.
Frey-Klett
P.
,
Burlinson
P.
,
Deveau
A.
,
Barret
M.
,
Tarkka
M.
&
Sarniguet
A.
2011
Bacterial-fungal interactions: hyphens between agricultural, clinical, environmental, and food microbiologists
.
Microbiology and Molecular Biology Reviews
75
(
4
),
583
609
.
Gonçalves
A. B.
,
Paterson
R. R. M.
&
Lima
N.
2006
Survey and significance of filamentous fungi from tap water
.
International Journal of Hygiene and Environmental Health
209
(
3
),
257
264
.
Göttlich
E.
,
van der Lubbe
W.
,
Lange
B.
,
Fiedler
S.
,
Melchert
I.
,
Reifenrath
M.
,
Flemming
H.-C.
&
de Hoog
S.
2002
Fungal flora in groundwater-derived public drinking water
.
International Journal of Hygiene and Environmental Health
205
,
269
279
.
Grabińska-Łoniewska
A.
,
Koniłłowicz-Kowalska
T.
,
Wardzyńska
G.
&
Boryn
K.
2007
Occurrence of fungi in water distribution system
.
Polish Journal of Environmental Studies
16
(
4
),
539
547
.
Gupta
V. K.
,
Mach
R. L.
&
Sreenivasaprasad
S.
2015
Fungal Biomolecules: Sources, Applications and Recent Developments
.
John Wiley and Sons
,
Chichester
,
UK
, pp.
153
160
.
Hageskal
G.
,
Knutsen
A. K.
,
Gaustad
P.
,
De Hoog
G. S.
&
Skaar
I.
2006
Diversity and significance of mold species in Norwegian drinking water
.
Applied and Environmental Microbiology
72
(
12
),
7586
7593
.
Hageskal
G.
,
Lima
N.
&
Skaar
I.
2009
The study of fungi in drinking water
.
Mycological Research
113
(
2
),
165
172
.
Hageskal
G.
,
Tryland
I.
,
Liltved
H.
&
Skaar
I.
2012
No simple solution to waterborne fungi: various responses to water disinfection methods
.
Water Science and Technology: Water Supply
12
(
2
),
220
226
.
Hurtado-McCormick
S.
,
Sanchez
L.
,
Martinez
J.
,
Calderon
C.
,
Calvo
D.
,
Narvaez
D.
,
Lemus
M.
,
Groot
H.
&
Rodriguez Susa
M.
2016
Fungi in biofilms of drinking water network: occurrence, diversity and mycotoxins approach
.
Water Science and Technology: Water Supply
16
,
905
914
.
Hussain
T.
,
Ishtiaq
M.
,
Hussain
A.
&
Sultana
K.
2011
Study of drinking water fungi and its pathogenic effects on human beings from District Bhimber, Azad Kashmir, Pakistan
.
Pakistan Journal of Botany
43
(
5
),
2581
2585
.
José Figueras
M.
&
Borrego
J. J.
2010
New perspectives in monitoring drinking water microbial quality
.
International Journal of Environmental Research and Public Health
7
(
12
),
4179
4202
.
Jun
N.
,
Weipeng
H.
,
Xinin
S.
&
Guibai
L.
2009
Impact of dynamic distribution of floc particles on flocculation effect
.
Journal of Environmental Sciences
21
,
1059
1065
.
Kanematsu
H.
&
Barry
D. M.
, (eds)
2016
World Health Organization's standards from the viewpoint of health risks
.
In:
Corrosion Control and Surface Finishing
.
Springer Verlag
,
Tokyo
,
Japan
, pp.
79
88
.
Kanzler
D.
,
Buzina
W.
,
Paulitsch
A.
,
Haas
D.
,
Platzer
S.
,
Marth
E.
&
Mascher
F.
2007
Occurrence and hygienic relevance of fungi in drinking water
.
Mycoses
51
(
2
),
165
169
.
Khan
M. S.
,
Ahmad
I.
,
Aqil
F.
,
Owais
M.
,
Shahid
M.
,
Musarrat
J.
2010
Virulence and pathogenicity of fungal pathogens with special reference to Candida albicans
. In:
Combating Fungal Infections: Problems and Remedy
(
Ahmad
I.
,
Owais
M.
,
Shahid
M.
&
Aqil
F.
, eds).
Springer-Verlag, Berlin
,
Heidelberg
,
Germany
, pp.
21
45
.
Kinsey
G. C.
,
Paterson
R. R.
&
Kelley
J.
1998
Methods for the determination of filamentous fungi in treated and untreated waters
.
Journal of Applied Microbiology
85
(
Suppl. 1
),
214S
224S
.
Kinsey
G.
,
Paterson
R.
&
Kelley
J.
2003
Filamentous fungi in water systems
. In:
Handbook of Water and Wastewater Microbiology
(
Horan
N. J.
, ed.).
Academic Press
,
London
,
UK
, pp.
77
98
.
Korzeniewska
E.
2011
Emission of bacteria and fungi in the air from wastewater treatment plants – a review EWA
.
Bioscience Reports
1
(
3
),
393
407
.
Liu
S.
,
Gunawan
C.
,
Barraud
N.
,
Rice
S. A.
,
Harry
E. J.
&
Amal
R.
2016
Understanding, monitoring and controlling biofilm growth in drinking water distribution systems
.
Environmental Science and Technology
50
(
17
),
8954
8976
.
Luu
S.
,
Cruz-mora
J.
,
Setlow
B.
,
Feeherry
F. E.
,
Doona
C. J.
&
Setlow
P.
2015
The effects of heat activation on bacillus spore germination, with nutrients or under high pressure, with or without various germination proteins
.
Applied and Environmental Microbiology
81
(
8
),
2927
2938
.
Luyt
C. D.
,
Tandlich
R.
,
Muller
W. J.
&
Wilhelmi
B. S.
2012
Microbial monitoring of surface water in South Africa: an overview
.
International Journal of Environmental Research and Public Health
9
(
8
),
2669
2693
.
Magwaza
N.
,
Nxumalo
E. N.
,
Mamba
B. B.
&
Msagati
T. A. M.
2017
The occurrence and diversity of waterborne fungi in African aquatic systems: their impact on water quality and human health
.
International Journal of Environmental Research and Public Health
14
(
6
),
546
.
Mains
C.
2008
Biofilms Control in Distribution System
.
Tech Brief, National Environmental Service Center (NESC) at West Virginia University
,
Morgantown, WV
,
USA
.
Máiz
L.
,
Nieto
R.
,
Cantón
R.
,
de la Pedrosa
E. G. G.
&
Martinez-García
M. Á
, .
2018
Fungi in bronchiectasis: a concise review
.
International Journal of Molecular Sciences
19
(
1
),
1
13
.
Marques
R. D. O.
,
Seckler
S.
&
Filho
F.
2017
Flocculation kinetics of low-turbidity raw water and the irreversible floc breakup process
.
Environmental Technology
37
(
7
),
901
910
.
Mayer
F. L.
,
Wilson
D.
&
Hube
B.
2013
Candida albicans pathogenicity mechanisms
.
Virulence
4
(
2
),
119
128
.
Meals
D. W.
,
Harcum
J. B.
&
Dressing
S. A.
2013
Monitoring for Microbial Pathogens and Indicators
.
National Nonpoint Source Monitoring Program Tech Notes 9, Tetra Tech
,
Fairfax, VA
,
USA
.
Meirelles
G. C.
,
Pippi
B.
,
Hatwig
C.
,
Barros
F. M. C.
,
De Oliveira
L. F. S.
,
De Von Poser
G. L.
&
Fuentefria
A. M.
2017
Synergistic antifungal activity of the lipophilic fraction of Hypericum carinatum and fluconazole
.
Brazillian Journal of Pharmacognosy
27
,
118
123
.
Mille-Lindblom
C.
2005
Interaction Between Bacteria and Fungi on Aquatic Detritus – Causes and Consequences
.
PhD thesis
,
Faculty of Science and Technology, Uppsala University
,
Sweden
.
Misihairabgwi
J. M.
,
Ezekiel
C. N.
,
Sulyok
M.
,
Shephard
G. S.
&
Krska
R.
2017
Mycotoxin contamination of foods in Southern Africa: a 10-year review (2007–2016)
.
Critical Reviews in Food Science and Nutrition
1549
(
7852
),
1
13
.
Momba
M. N. B.
,
Kfir
R.
,
Venter
S. N.
&
Cloete
T. E.
2000
An overview of biofilm formation in distribution systems and its impact on the deterioration of water quality
.
Water SA
26
(
1
),
59
66
.
Momba
M. N.
,
Obi
C.
&
Thompson
P.
2008
Improving Disinfection Efficiency in Small Drinking Water Treatment Plants
.
Water Research Commision report, WRC 1531/1/08
,
Pretoria
,
South Africa
.
Mukherjee
S.
2012
Aflatoxin Effect On Health
.
USAID/East Africa
.
Mulamattathil
S. G.
,
Bezuidenhout
C.
&
Mbewe
M.
2014
Biofilm formation in surface and drinking water distribution systems in Mafikeng, South Africa
.
South African Journal of Science
110
(
11–12
),
1
9
.
Nazim
S.
,
Dawar
S.
,
Tariq
M.
&
Zaki
M. J.
2008
Quantitative estimation of mycoflora in drinking water and fruit juices of Karachi
.
Pakistan Journal of Botany
40
(
3
),
1263
1268
.
Obi
C. L.
,
Igumbor
J. O.
,
Momba
M. N. B.
&
Samie
A.
2008
Interplay of factors involving chlorine dose, turbidity flow capacity and pH on microbial quality of drinking water in small water treatment plants
.
Water SA
34
(
5
),
565
572
.
O'Connor
J. T.
&
O'Connor
T. L.
2001
Removal of Microorganisms by Rapid Sand Filtration
.
H2O'C Engineering
,
Columbia, MO
,
USA
.
Oliveira
B. R.
,
Crespo Barreto
M. T.
,
San Romao
M. V.
,
Benoliel
M. J.
,
Samson
R. A.
&
Pereira
V. J.
2013
New insights concerning the occurrence of fungi in water sources and their potential pathogenicity
.
Water Research
47
,
6338
6347
.
Oliveira
H. M. B.
,
Santos
C.
,
Paterson
R. R. M.
,
Gusmão
N. B.
&
Lima
N.
2016
Fungi from a groundwater-fed drinking water supply system in Brazil
.
International Journal of Environmental Research and Public Health
13
(
304
),
1
11
.
Omar
H. E. M.
2013
Mycotoxins-induced oxidative stress and disease
.
Chapter 3
. In:
Mycotoxin and Food Safety in Developing Countries
.
InTech Open Science
,
Rjeka
,
Croatia
, pp.
63
92
.
Oyegbile
B.
,
Ay
P.
&
Satyanarayana
N.
2016
Flocculation kinetics and hydrodynamic interactions in natural and engineered flow systems: a review
.
Environmental Engineering Research
21
(
1
),
1
14
.
Pal
M.
2017
Morbidity and mortality due to fungal infections
.
Journal of Applied Microbiology and Biochemistry
1
,
2
3
.
Partida-Martinez
L. P.
,
De Looß
C. F.
,
Ishida
K.
,
Ishida
M.
,
Roth
M.
,
Buder
K.
&
Hertweck
C.
2007
Rhizonin, the first mycotoxin isolated from the zygomycota, is not a fungal metabolite but is produced by bacterial endosymbionts
.
Applied and Environmental Microbiology
73
(
3
),
793
797
.
Paterson
R. R. M.
&
Lima
N.
2008
Fungal Growth and Mycotoxin Production in Drinking Water
.
IBB – Biological Engineering Centre, University of Minho
,
Braga
,
Portugal
.
Pellon
A.
,
Ramirez-garcia
A.
,
Buldain
I.
,
Antoran
A.
,
Souto
L. M.
,
Rementeria
A.
&
Hernando
F. L.
2018
Pathobiology of lomentospora prolificans: could this species serve as a model of primary antifungal resistance?
International Journal of Antimicrobial Agents
51
,
10
15
.
Pereira
V. J.
,
Fernandes
D.
,
Carvalho
G.
,
Benoliel
M. J.
,
San Romao
M. V.
&
Barreto-Crespo
M. T.
2010
Assessment of the presence and dynamics of fungi in drinking water sources using cultural and molecular methods
.
Water Research
44
,
4850
4859
.
Pereira
V. J.
,
Marques
R.
,
Marques
M.
,
Benoliel
M. J.
&
Barreto-Crespo
M. T.
2013
Free chlorine inactivation of fungi in drinking water sources
.
Water Research
47
(
2
),
517
523
.
Pitt
J. I.
2000
Toxigenic fungi and mycotoxins
.
British Medical Bulletin
56
(
1
),
184
192
.
Pitt
J. I.
,
Bacilico
J. C.
,
Abarca
M. L.
&
Lopez
C.
2000
Mycotoxins and toxigenic fungi
.
Medical Mycology
38
(
1
),
41
46
.
Puel
O.
,
Galtier
P.
&
Oswald
I. P.
2010
Biosynthesis and toxicological effects of patulin
.
Toxins
2
(
4
),
613
631
.
Ramage
G.
,
Rajendran
R.
,
Sherry
L.
&
Williams
C.
2012
Fungal biofilm resistance
.
International Journal of Microbiology
2012
(
528521
),
1
14
.
Rasteiro
M. G.
,
Garcia
F. A.
,
Hunkeler
D.
&
Pinheiro
I.
2016
Evaluation of the performance of dual polyelectrolyte systems on the re-flocculation ability of calcium carbonate aggregates in turbulent environment
.
Polymers
8
(
174
),
8
12
.
Rodrigues
C. F.
,
Rodrigues
M. E.
,
Silva
S.
&
Henriques
M.
2017
Candida glabrata biofilms: how far have we come?
Journal for Fungi
3
(
11
),
1
30
.
Rojas-Valencia
M. N.
2011
Research on ozone application as disinfectant and actions mechanisms on wastewater microorganisms
. In:
Science Against Microbial Pathogens: Communicating Current Research and Technological Advances
(
Mendez-Vilas
A.
, ed.).
Microbiology Book Series
,
Formatex
,
Espana
, pp.
263
271
.
Sammon
N. B.
,
Harrower
K. M.
,
Fabbro
L. D.
&
Reed
R. H.
2010
Incidence and distribution of microfungi in a treated municipal water supply system in sub-tropical Australia
.
International Journal of Environmental Research and Public Health
7
(
4
),
1597
1611
.
Sammon
N. B.
,
Harrower
K. M.
,
Fabbro
L. D.
&
Reed
R. H.
2011
Three potential sources of microfungi in a treated municipal water supply system in sub-tropical Australia
.
International Journal of Environmental Research and Public Health
8
(
3
),
713
732
.
Scorzoni
L.
,
de Paula e Silva
A. C. A.
,
Marcos
C. M.
,
Assato
P. A.
,
de Melo
W. C. M. A.
,
de Oliveira
H. C.
,
Costa-Orlandi
C. B.
,
Mendes-Giannini
M. J. S.
&
Fusco-Almeida
A. M.
2017
Antifungal therapy: new advances in the understanding and treatment of mycosis
.
Frontiers in Microbiology
8
(
36
),
1
23
.
Šegvić
K. M.
,
Rašić
D.
&
Peraica
M.
2013
Deleterious effects of mycotoxin combinations involving Ochratoxin A
.
Toxins
5
(
11
),
1965
1987
.
Shadanaika
M.
2005
Mycotoxigenic Fungi in Spices; Molecular Methods of Detection and Control
.
PhD thesis
,
University of Mysore
,
India
.
Sibanda
T.
&
Okoh
A. I.
2013
Real-time PCR quantitative assessment of hepatitis A virus, rotaviruses and enteroviruses in the Tyume River located in the Eastern Cape Province, South Africa
.
Water SA
39
(
2
),
295
304
.
Siqueira
V. M.
2011
Characterising Filamentous Fungal Biofilm in Drinking Water Distribution Systems Using Microscopic and Molecular Techniques
.
PhD thesis
,
Universidade do Minho
,
Portugal
.
Sonigo
P.
,
De Toni
A.
&
Reilly
K.
2011
A Review of Fungi in Drinking Water and the Implications for Human Health
.
Final report WD 0906
.
Bio Intelligence Service
,
Paris
,
France
.
Speight
V.
2002
Water distribution systems: the next frontier
.
The Bridge
38
(
3
),
31
37
.
Spellman
F. R.
2014
Handbook of Water and Wastewater Treatment Plant Operations
,
3rd edn.
CRC Press
,
Boca Raton, FL
,
USA
.
Szewzyk
U.
,
Szewzyk
R.
,
Manz
W.
&
Schleifer
K. H.
2009
Microbiological safety of drinking water
.
Microbial Ecology
54
,
81
127
.
Tekere
M.
,
Lötter
A.
,
Olivier
J.
,
Jonker
N.
&
Venter
S.
2011
Metagenomic analysis of bacterial diversity of Siloam hot water spring, Limpopo, South Africa
.
African Journal of Biotechnology
10
(
78
),
18005
18012
.
Thupaki
P.
,
Phanikumar
M. S.
,
Schwab
D. J.
,
Nevers
M. B.
&
Whitman
R. L.
2013
Evaluating the role of sediment-bacteria interactions on Escherichia coli concentrations at beaches in southern Lake Michigan
.
Journal of Geophysical Research: Oceans
118
(
12
),
7049
7065
.
Tsui
C.
,
Kong
E. F.
&
Jabra-Rizk
M. A.
2016
Pathogenesis of candida albicans biofilm
.
Pathogens and Disease
74
(
4
),
1
13
.
UN Water
2015
International Decade for Action ‘Water for Life’ 2005–2015
.
Focus Areas: Water and sustainable development
. .
Van der Kooij
D.
1998
Potential for biofilm development in drinking water distribution systems
.
Journal of Applied Microbiology
85
(
Suppl 1
),
39S
44S
.
Volk
T. J.
2013
Fungi
.
Encyclopedia of Biodiversity
3
,
624
640
.
Water Research Commission (WRC)
2002
Quality of Domestic Water Supplies: Treatment Guide
.
Water Research Commission
,
Pretoria
,
South Africa
,
No: TT 181/02 4(1),
1
99
.
World Health Organization (WHO)
2008
Guidelines for Drinking-Water Quality
.
Incorporating 1st and 2nd addenda, volume 1, recommendations, 3rd edn
.
WHO
,
Geneva
,
Switzerland
.
World Health Organization (WHO)
2011a
Guidelines for Drinking-Water Quality: Surveillance and Control of Community Supplies
.
World Health Organization
,
Geneva
,
Switzerland
.
World Health Organization (WHO)
2011b
Mycotoxins. Children's Health and the Environment
.
WHO Training Package for the Health Sector
. .
World Health Organization (WHO)
2017
Guidelines for Drinking-Water Quality
,
4th edition incorporating the 1st addendum
.
WHO
,
Geneva
,
Switzerland
.
apps.who.int/iris/bitstream/10665/254637/1/9789241549950-eng.pdf. (accessed 29/01/2018)
.
Wurzbacher
C.
,
Kerr
J.
,
Grossart
H.-P.
1998
Aquatic fungi
. In:
The Dynamical Processes of Biodiversity – Case Studies of Evolution and Spatial Distribution
(
Grillo
O.
&
Venora
G.
, eds).
InTech
,
Rjeka
,
Croatia
, pp.
227
258
.
Yamaguchi
M. U.
,
de Rampazzo
R. C. P.
,
Yamada-Ogatta
S. F.
,
Nakamura
C. V.
,
Ueda-Nakamura
T.
&
Filho
B. P. D.
2007
Yeasts and filamentous fungi in bottled mineral water and tap water from municipal supplies
.
Brazilian Archives of Biology and Technology
50
(
1
),
1
9
.
Zain
M. E.
2011
Impact of mycotoxins on humans and animals
.
Journal of Saudi Chemical Society
15
(
2
),
129
144
.