December 6, 2017
The designations employed and the presentation of material throughout this publication do not imply the expression of any opinion whatsoever on the part of UNESCO concerning the legal status of any country, territory, city or area or of its authorities, or concerning the delimitation of its frontiers or boundaries. The ideas and opinions expressed in this publication are those of the authors; they are not necessarily those of UNESCO and do not commit the Organization.
Rusinol, M. and Girones, R. 2017. Summary of Excreted and Waterborne Viruses. In: J.B. Rose and B. Jiménez-Cisneros, (eds) Global Water Pathogen Project. http://www.waterpathogens.org (J.S Meschke, and R. Girones (eds) Part 3 Viruses) http://www.waterpathogens.org/book/summary-of-excreted-and-waterborne-viruses Michigan State University, E. Lansing, MI, UNESCO.
Acknowledgements: K.R.L. Young, Project Design editor; Website Design
|Last published: December 6, 2017|
There are hundreds of viruses that infect humans and most are released into feces and urine making their way into the environment by excretion or secretion of bodily fluids or skin cells. The viruses infecting the enteric track are known to be excreted in high numbers and many of these viruses are commonly excreted by healthy people often long after symptom resolution.
The most important excreted known pathogens are transmitted by a variety of means including fecal-oral transmission routes and are members of six families, Picornaviridae, Caliciviridae, Hepeviridae, Reoviridae, Astroviridae (all RNA viruses) and the DNA virus family Adenoviridae. Viruses in these families cause asymptomatic infections and also outbreaks or sporadic cases with a wide range of symptoms from mild to severe gastroenteritis to meningitis, respiratory disease, conjunctivitis, miocarditis, paralysis, or hepatitis.
Recent data have shown the presence of new viral pathogens associated with gastroenteritis or other clinical symptoms in a set of novel viral families. In the Parvoviridae family, human bocaviruses 1 to 4 (HBoV) and human bufavirus (HBuV) are associated with respiratory and gastrointestinal diseases. Circoviruses are currently known to infect birds and swine, and no human pathogenic circoviruses have been definitively demonstrated yet, nevertheles new phylogenetically diverse Circoviruses have been shown to be present in sewage. A large portion of circular ssDNA viruses similar to the family Circoviridae have been revealed primarily through metagenomics in a diverse range of samples. Metagenomics in raw sewage water of United States, Spain and Ethiopia, showed sequences with identities between 20 and 50% to the Circoviridae family and in another study sewage from United States showed sequences 35 to 58% identical. The genera Cyclovirus have been suggested to cause human enteric infections and, a study identified and characterized the full genome of a novel cyclovirus (tentatively named cyclovirus-Vietnam [CyCV-VN]) in cerebrospinal fluid (CSF) specimens of two Vietnamese patients with CNS infections of unknown etiology.
A wide diversity of viruses is known to be commonly excreted, some are new pathogens recently described and some of them have not been associated yet to human diseases. A study analyzing stool samples from two healthy infant siblings collected at about weekly intervals during their first year of life were analyzed by PCR for 15 different enteric viral genera showed that ninety-two percent (66/72) of the fecal samples tested contained one to five different human viruses. Adenovirus, Aichi virus, Anellovirus, Astrovirus, Bocavirus, Enterovirus, Parechovirus, Picobirnavirus, and Rotavirus were detected. The study also confirmed long-term virus shedding for adenoviruses, anelloviruses, bocaviruses, enteroviruses, parechoviruses, and picobirnaviruses.
Excreted viruses are detected in urban sewage samples and survival is facilitated by organic debris of the clinical matrix in which the virus is shed (feces or vomit) and virus aggregate formation, offering protection in the route to new human hosts. The concentration of viruses observed in urban sewage is high and is related to the epidemiology of each viral infection. Viruses excreted in the population of all geographical areas and without defined seasonability, as it is the case of human adenoviruses, have been detected in wastewater and superficial waters in all geographical areas analyzed with levels of 104-7 GC/100 ml in raw sewage, 10 3-4 GC/100ml in secondary and tertiary effluent of wastewater treatment plants, 104-7 GC/100 g of biosolids, 101-5 CG/L in river water, and 101-3CG/L in seawater. Human adenoviruses and human polyomaviruses have been suggested as indicators of human fecal/urine contamination and MST tools in the environment and water based on the affordability of quantification techniques for DNA viruses, and their abundance in all geographical areas and periods of the year. Many classical and emerging viral pathogens have been detected in bathing water, river and seawater and their high stability and low infectious doses support the need for improving control of virus dissemination in water is an important concern requiring improved water treatments and regulations.
There are hundreds of viruses that infect humans and are released into the environment by excretion or secretion of bodily fluids or skin. The viruses infecting the gastrointestinal tract also known as enteric viruses, are excreted in high numbers (107 109 g-1 of feces) by infected individuals with or without disease, and in some cases long after the resolution of disease. These viruses can be transmitted by contaminated water via the fecal-oral route.
The most important waterborne viruses are members of six families, including RNA virus families such as Picornaviridae, Caliciviridae, Hepeviridae, Reoviridae, Astroviridae and the Adenoviridae within the family of DNA viruses. Viruses in these families cause asymptomatic infections and also outbreaks or sporadic cases with a wide range of symptoms from mild to severe gastroenteritis to meningitis, respiratory disease, conjunctivitis, myocarditis, paralysis, or hepatitis (http://ictvonline.org).
Recent data has shown evidence of new viral pathogens in the Parvoviridae family associated with gastroenteritis in humans. The clinical manifestations of parvovirus 4 (PARV4) remain unknown whereas human bocaviruses 1 to 4 (HBoV) and human bufavirus (HBuV) are associated with respiratory and gastrointestinal diseases (Väisänen et al., 2014)
New viruses with DNA in circular form that are phylogenetically diverse have been detected in sewage. These viruses have been included within the family Circoviridae which comprises virus species that infect birds and swine (Blinkova et al., 2009). A large portion of circular ssDNA viruses, similar to the family Circoviridae, was elucidated by metagenomics of a diverse range of samples. Metagenomics of urban sewage in the United States, Spain and Ethiopia, showed virome contigs with 20 to 50% similarities to viruses with circular genomes characteristic of the Circoviridae family (Cantalupo et al., 2011). In addition, PCR screening of viral nucleic acid recovered from sewage in the United States revealed genetic variants of DNA circoviruses (Blinkova et al., 2009). The genus Cyclovirus has been suggested to cause human enteric infections, and a study identified and characterized the full genome of a novel cyclovirus (tentatively named cyclovirus-Vietnam [CyCV-VN]) in cerebrospinal fluid (CSF) specimens of two Vietnamese patients with CNS infections of unknown etiology (Li et al., 2010; Phan et al., 2015). The authors suggested the potential for fecal-oral as well as foodborne transmission while high detection rates in feces from pigs and poultry (average, 58%) suggested the existence of animal reservoirs for such transmission routes (Tan et al., 2013).
The excretion of viruses in feces is high and viruses are commonly excreted by healthy people even after resolution of symptoms. Stool samples from healthy infants showed that ninety-two percent (66/72) of the tested fecal samples contained one to five different human viruses (Kapusinszky et al., 2012). Adenoviruses, aichi viruses, anelloviruses, astroviruses, bocaviruses, enteroviruses, parechoviruses, picobirnaviruses and rotaviruses were the viruses most frequently detected. Vaccination schedules have an effect on the excretion of viruses (Laassri et al., 2005). The summary of the level of excretion of the most important waterborne viruses is shown in Table 3.
Water and food are the main vehicles for transmission of viruses that replicate in the gastrointestinal tract causing the wide spectrum of diseases described in Table 2. Contaminated drinking water is an important cause of gastrointestinal disease (Altzibar et al., 2015; Braeye et al., 2015; Craun et al., 2010; Kauppinen et al., 2017). The burden of water-borne diseases directly related to viruses, was estimated at 136 outbreaks in Europe during 2000 and 2007 (39% of all diarrhea cases due to unsafe water) and at 64 outbreaks in the U.S. during 1971 and 2006 (Craun et al., 2010; ENHIS, 2009). The risk of emerging waterborne diseases increases where standards of water, sanitation and personal hygiene are low. More than half of the waterborne disease outbreaks linked to drinking water have been associated with untreated or inadequately treated ground water, indicating that contamination of ground water remains a public health problem (Yoder et al., 2011).
The global public health impact is higher when considering the food-borne transmission route. The American and European surveillance reports on the food-borne outbreaks estimate that between 45 and 51% of the total food-borne outbreaks are caused by water-borne viruses (Gould et al., 2013; Price-Hayward and Hartnell, 2016). The route from food production to consumption is very complex, with many points where pathogens can enter and reach the consumers (e.g. at the farm, during slaughter, during processing, in the kitchen). Of the viral pathogens that can contaminate food, HAV, HEV and NoV in bivalve shellfish, fresh produce, and prepared foods have been identified as the highest risk pathogens (EFSA, 2012). Foodborne cases of hepatitis E in humans are increasingly common and likely underestimated in the medical community (Meng, 2013). Sporadic and cluster cases of hepatitis E occur after consumption of undercooked or raw animal meats.
Humans are the main reservoirs of enteric viruses. With exception of rotavirus and hepatitis E virus, zoonotic transmission of water-borne viruses is rare. It is a well-known fact that animal RoV-A infect humans. Nowadays, there is convincing genetic evidence that interspecies transmission of RoV occurs. Animal RoV can infect humans via direct interspecies transmission events or reassortment between a human and animal rotavirus. Recent reviews on porcine, bovine and equine rotaviruses indicate that there are some globally important genotype specificities of RoVs in each of these host species. (Papp et al., 2013a; Papp et al., 2013b). Nevertheless, zoonotic viruses can emerge from animal reservoirs and affect humans only incidentally.
Hepatitis E virus is an emerging zoonotic water- and foodborne pathogen (Ricci et al., 2017; Uddin Khan et al., 2013). HEV-1 and HEV-2 are restricted to humans whereas HEV-3 and HEV-4 are naturally present in several animal species and can cross the species barrier. The zoonotic transmission of HEV-3 and HEV-4 from swine, wild boar and deer to human via the consumption of raw meat has been proven (Bouquet et al., 2012, 2011; Cook et al., 2017). In 2016, a small outbreak in China was related to HEV-4 found in food from the company’s cafeteria (Zhang et al., 2016). There is also an increasing evidence for zoonotic transmission of hepatitis E from camels (Sridhar et al., 2017).
Waterborne viral diseases are of major concern in both developing and developed countries and wastewater treatment plays a crucial role in mitigating viral pollution of aquatic environments. A summary of representative available data on the occurrence of viral pathogens in raw sewage, secondary and tertiary effluents of wastewater treatment plants is shown in Tables 5, 6 and 7.