key: cord-0924084-w3h7a95p
authors: Upfold, Nicole S.; Luke, Garry A.; Knox, Caroline
title: Occurrence of Human Enteric Viruses in Water Sources and Shellfish: A Focus on Africa
date: 2021-01-27
journal: Food Environ Virol
DOI: 10.1007/s12560-020-09456-8
sha: 7ab74262c05d3d4db84e895340bf9ced558025c5
doc_id: 924084
cord_uid: w3h7a95p

Enteric viruses are a diverse group of human pathogens which are primarily transmitted by the faecal–oral route and are a major cause of non-bacterial diarrhoeal disease in both developed and developing countries. Because they are shed in high numbers by infected individuals and can persist for a long time in the environment, they pose a serious threat to human health globally. Enteric viruses end up in the environment mainly through discharge or leakage of raw or inadequately treated sewage into water sources such as springs, rivers, dams, or marine estuaries. Human exposure then follows when contaminated water is used for drinking, cooking, or recreation and, importantly, when filter-feeding bivalve shellfish are consumed. The human health hazard posed by enteric viruses is particularly serious in Africa where rapid urbanisation in a relatively short period of time has led to the expansion of informal settlements with poor sanitation and failing or non-existent wastewater treatment infrastructure, and where rural communities with limited or no access to municipal water are dependent on nearby open water sources for their subsistence. The role of sewage-contaminated water and bivalve shellfish as vehicles for transmission of enteric viruses is well documented but, to our knowledge, has not been comprehensively reviewed in the African context. Here we provide an overview of enteric viruses and then review the growing body of research where these viruses have been detected in association with sewage-contaminated water or food in several African countries. These studies highlight the need for more research into the prevalence, molecular epidemiology and circulation of these viruses in Africa, as well as for development and application of innovative wastewater treatment approaches to reduce environmental pollution and its impact on human health on the continent.

Enteric viruses collectively represent a diverse group of pathogens that are responsible for a variety of notifiable diseases in humans through ingestion of contaminated food or water. Well-known human pathogens in this group are members of the Caliciviridae (e.g. norovirus), Picornaviridae (e.g. enterovirus, Aichi virus, hepatitis A virus), Hepeviridae (e.g. hepatitis E virus), Reoviridae (e.g. rotavirus), Astroviridae (astrovirus) and Adenoviridae (e.g. adenovirus 40, 41) (Fong and Lipp 2005; Bishop and Kirkwood 2008) . These viruses are a major public health concern globally due to the fact that they tend to be stable in the environment, are shed at high concentrations in the faeces of infected people and are transmitted by the faecal-oral route (Fong and Lipp 2005; Sánchez and Bosch 2016; Bouseettine et al. 2019) . Although these viruses are known to occur naturally in aquatic environments, one of the greatest risks they pose to public health arises from discharge of either raw (untreated) sewage or inadequately treated wastewater into ground or surface water sources utilised by humans for various activities including drinking, recreation, or consumption of foods such as molluscan bivalve shellfish harvested from polluted rivers or marine estuaries. Isolation of enteric viruses from such sewagecontaminated water sources and association of disease outbreaks as a result of human exposure to them are well documented in the literature (see for example : Lees 2000; Okoh et al. 2010; Gibson 2014; Richards 2016; Khora 2018; Masciopinto et al. 2019) .

Transmission of enteric viruses to humans is particularly concerning in developing countries of the world where it is estimated that 80-90% of untreated sewage is disposed into water sources such as rivers, streams and other aquatic ecosystems causing environmental pollution (WWAP and UNESCO 2017; Fayomi et al. 2019 ). Countries in Africa and especially those in the Sub-Saharan region where it is estimated that 55% of urban dwellers now live in informal settlements are most at risk from infectious diseases because of overcrowding and poor sanitation infrastructure (Neiderud 2015; Boyce et al. 2019; Weimann and Oni 2019) . Furthermore, people living in rural communities and informal settlements in Africa often rely on environmental surface and ground water sources polluted by wastewater and other contaminants originating from human activities for drinking, cooking and washing (Wang et al. 2014; Sibanda et al. 2015; Pichel et al. 2019; UNESCO 2019) . Growing concern about the human health impact of environmental pollution, in particular untreated sewage discharge into fresh and marine aquatic systems, has led to numerous studies describing the isolation and molecular detection of enteric viruses in water and food sources and their association with disease outbreaks in several African countries. For example, these viruses have been reported in bivalve shellfish and environmental water sources in North Africa (Morocco, Tunisia and Egypt) (Benabbes et al. 2013b; Zormati et al. 2018; Shaheen and Elmahdy 2019) as well as in several Sub-Saharan countries including Chad (Guerrero-Latorre et al. 2011) , Nigeria (Adeniji and Faleye 2014) , Ghana (Lutterodt et al. 2018) , Côte d'Ivoire (Momou et al. 2017) , Benin (Verheyen et al. 2009 ), Kenya (Kiulia et al. 2014) , Uganda (Katukiza et al. 2013b) , Tanzania (Mattioli et al. 2014) , Mozambique (Nenonen et al. 2006) and South Africa (Chigor et al. 2014; Onosi et al. 2020) . Although the role of enteric viruses in food-and waterborne disease transmission has been extensively reviewed for the developed world (Lipp and Rose 1997; Potasman et al. 2002; Sinclair et al. 2009; Westrell et al. 2010; Bellou et al. 2013; Romalde et al. 2017; Meghnath et al. 2019) and Egypt (Aboubakr and Goyal 2019) , to our knowledge, a review of the African continent where people are most at risk from exposure to these viruses is not available. Here, we present an overview of enteric viruses and then review what is known about bivalve shellfish and sewage-contaminated water sources as possible vehicles for transmission in African countries, with a view to highlighting the importance of further studies investigating the true prevalence, molecular epidemiology and circulation of these important human pathogens on the continent.

Enteric viruses encompass a broad range of viral pathogens which infect the human gastrointestinal tract, causing a wide variety of diseases and symptoms (Okoh et al. 2010) . Commonly studied enteric viruses are non-enveloped and display high levels of stability in the environment (Fong and Lipp 2005; Alidjinou et al. 2019) . Most enteric viruses have RNA genomes and belong to the Reoviridae (ds: double-stranded), Astroviridae, Caliciviridae, Hepeviridae or Picornaviridae (ss: single-stranded) families, while enteric viruses with DNA genomes are members of the Adenoviridae (ds) or Parvoviridae (ss).

Globally, rotaviruses (RVs; family Reoviridae) are a major cause of severe viral gastroenteritis in the paediatric population (Bányai et al. 2018 ) and account for a significant proportion of diarrhoea-related deaths among children under the age of five (29.3% in 2015) (Wang et al. 2016) . The introduction of RV vaccines has, however, reduced the burden of associated gastroenteritis in many countries (Troeger et al. 2018; Aliabadi et al. 2019) , including those within sub-Saharan Africa (Tate et al. 2016; Godfrey et al. 2020 ). The RV genome consists of 11 dsRNA segments encoding six structural (VP1-4, 6 and 7) and six non-structural (NSP1-NSP6) proteins (Crawford et al. 2017; Gómez-Rial et al. 2020) . Based on antigenic differences and the diversity of the VP6 capsid protein sequence, RVs are classified into ten species (A-J), of which species A, B, C and H cause human RV infections. Group A is the predominant cause of RV-gastroenteritis and is further classified into 32 G and 47 P genotypes based on differences in the sequences encoding the surface exposed capsid proteins VP7 (G antigen) and VP4 (P antigen) (Crawford et al. 2017) , respectively. Various G and P combinations have been identified, however, genotypes G1P[8] , G2P[4] , G3P[8] , G4P[8] , G9P[8] and G12P[8] are more commonly detected worldwide (Bányai et al. 2018) . RV genotypes isolated from wastewater correspond to those reported in clinical samples from the same regions (Sdiri-Loulizi et al. 2010a; Prez et al. 2020) , thus environmental monitoring provides useful data on the epidemiology of RVs circulating within populations (Abdel-Daim et al. 2019 ).

Noroviruses (NoVs; family Caliciviridae) are currently recognised as the leading cause of sporadic and epidemic viral gastroenteritis globally, resulting in approximately 677 million infections per annum (Pires et al. 2015; De Graaf et al. 2016) . NoV-associated gastroenteritis is usually self-limiting, although prolonged symptoms and secondary complications can arise in young children, the elderly and individuals with impaired immunity (Trivedi et al. 2013; Petrignani et al. 2018) . The NoV genome is organised into three open reading frames (ORF1-3) encoding a large nonstructural polyprotein (cleaved into six proteins), the major VP1 capsid protein and the minor VP2 capsid protein (De Graaf et al. 2016) , respectively. Reverse transcription polymerase chain reaction (RT-PCR) and quantitative real-time PCR (RT-qPCR) assays targeting the ORF1-ORF2 junction region have become standard in the detection and quantification of NoV from clinical and environmental samples. NoVs display a wide degree of genetic and antigenic variability and can be classified into different genogroups (GI-GX) as well as P groups based on amino acid diversity of the complete VP1 gene and nucleotide diversity of the viral polymerase sequence (Kroneman et al. 2013; Chhabra et al. 2019) , respectively. Human NoV infections are predominantly caused by the genogroups GI and GII, with GII.4 variants causing most cases in the last decade (Siebenga et al. 2009; Vinjé 2015; Mans et al. 2016) . In 2014, a novel variant of genotype GII.17 (GII.P17-GII.17) emerged as a major cause of NoV-associated gastroenteritis in Asia, and has since been reported globally (Chan et al. 2015; Lu et al. 2015; Chan et al. 2017; Hoa-Tran et al. 2017; Zhou et al. 2019) . Genotype GII.4 is most associated with transmission through person-person contact, while strains of Genogroup GI are more closely associated with waterborne transmission (De Graaf et al. 2016) . Strains belonging to GIV have been detected in both clinical and environmental samples; however, further studies are needed to fully understand the prevalence, epidemiology and medical significance of this genogroup (Muscillo et al. 2013; Kitajima et al. 2016; Teixeira et al. 2016) .

Sapoviruses (SaVs) also belong to the Caliciviridae and are aetiological agents of acute viral gastroenteritis, causing both sporadic and outbreak cases in a variety of settings (Oka et al. 2015) . Symptoms are generally milder than those caused by NoV and although infections occur in all age groups, SaV-associated gastroenteritis is more prevalent in children and infants (Liu et al. 2016) . The SaV genome usually contains two ORFs. The first (ORF1) encodes a single non-structural polyprotein and a major capsid protein (VP1), while a smaller capsid protein (VP2) is encoded by ORF2 (Makhaola et al. 2020) . SaVs are routinely detected by RT-PCR of the VP1 or polymerase encoding regions, and genotyping is based on differences within the VP1coding sequence (Hansman et al. 2007; Oka et al. 2015) . SaVs are phylogenetically clustered into 19 genogroups, of which GI, GII, GIV and GV contain human SaVs and are further subdivided into genotypes GI.1-GI.7, GII.1-GII.8, GIV.1 and GV.1-GV.2 (Oka et al. 2015; Diez-Valcarce et al. 2018; Makhaola et al. 2020) . Globally, strains belonging to genogroups GI and GII are more prevalent than SaVs belonging to genogroups GIV and GV (Fioretti et al. 2016; Yoneda et al. 2017; Mann et al. 2019; Supadej et al. 2019; Varela et al. 2019) . Recently, GI was confirmed as the most prevalent genogroup detected in people and the environment within African countries (Makhaola et al. 2020 ).

Human Astroviruses (HAstVs; family Astroviridae) are common aetiological agents of acute paediatric gastroenteritis, after rotavirus and the caliciviruses (Platts-Mills et al. 2015; Vu et al. 2017; Wohlgemuth et al. 2019) , and are detected at rates comparable to adenoviruses in cases of paediatric diarrhoea (Andreasi et al. 2008; Levidiotou et al. 2009; Hamkar et al. 2010; Akdag et al. 2020) . HAstV-associated gastroenteritis is also reported in the adult population, particularly in the elderly and individuals with compromised immunity Wohlgemuth et al. 2019 ). More recently, HAstVs have become associated with central nervous system (CNS) infections such as encephalitis and acute flaccid paralysis, in immunocompromised individuals Vu et al. 2016) . The HastV genome contains three ORFs. ORF1a and 1b encode the non-structural proteins involved in viral replication, while ORF2 encodes the capsid proteins, which are expressed on a sub-genomic RNA (Bosch et al. 2014 ). Astroviruses exhibit a high degree of genetic diversity and infect many host species which has complicated the classification of these viruses. Based on the full-length amino acid sequence of ORF2, HAstVs belong to the species MAstV-1 (HAstV-1-8), MAstV-6 (MLB1-3), MAstV-8 (VA2/HMO-A, VA4, VA5, BF34) and MAstV-9 (VA1/HMO-C, VA3/HMO-B) of the Mamastrovirus genus (reviewed by Donato and Vijaykrishna, 2017) . Additionally, classic HAstVs (MAstV-1 strains) have been further typed, according to ORF1a, into genogroups A (HAstv-1, -2, -3, -4, -5 and -8) and B (HAstv-6 and -7). Globally, HastV-1 strains account for more than half of all recently reported cases . asymptomatic, coxsackieviruses (e.g. CV-A6), echoviruses (e.g. E-30) and enteroviruses (e.g. EV-A71 and EV-D68) cause a broad range of illnesses such as hand-foot-andmouth disease, myocarditis, encephalitis and acute flaccid paralysis, which tend to be more severe in neonates and immunocompromised individuals (Tang and Holmes 2017; Baggen et al. 2018) . To date, more than 300 EV types have been identified and are classified within 15 species (Chen et al. 2020) . Human EVs belong to seven species, but only four (Enterovirus A-D) include viruses infecting the gastrointestinal tract (Baggen et al. 2018) . Originally, EVs were grouped into serotypes on the basis of the VP1 capsid protein, however, sequence-based methods targeting the VP1 capsid-encoding region are now typically used to classify EV by genetic similarity (Oberste et al. 1999a (Oberste et al. , 1999b Nix et al. 2006) . RT-PCR-based assays targeting additional sequences such as the 5' untranslated region (UTR) of the genome (Zhou et al. 2011 ) and the VP2 and VP4 capsid proteins (Royston et al. 2017 ) have also been developed, but their roles in genotyping are variable (Lindberg et al. 2003; Kottaridi et al. 2004; Nasri et al. 2007; Perera et al. 2010) . Globally, many studies have isolated EVs from sewage, fresh surface waters, ground water and seas, highlighting the widespread presence of these viruses in the environment (Rajtar et al. 2008) .

Aichi virus (AiV), a subtype of the species Aichivirus A (genus Kobuvirus) (Rivadulla and Romalde 2020) , was first isolated in 1989 during an outbreak of oyster-associated gastroenteritis in Japan (Yamashita et al. 1991 ) and has since been detected worldwide (Oh et al. 2006; Sdiri-Loulizi et al. 2009; Yang et al. 2009; Chuchaona et al. 2017; Bergallo et al. 2018; Kitajima et al. 2018; Japhet et al. 2019; Onosi et al. 2019; Northill et al. 2020) . Globally, the incidence rates of AiV in gastroenteritis cases are low (0.4-6.5%) (Rivadulla and Romalde 2020; Taghinejad et al. 2020 ), yet AiV-specific antibodies are present in 80-99% of the adult population (Kitajima and Gerba 2015) suggesting that most infections are asymptomatic (Bergallo et al. 2018) . In addition to the low prevalence of AiV-associated gastroenteritis, the virus is often detected in conjunction with other welldefined enteric pathogens (Oh et al. 2006; Ambert-Balay et al. 2008; Kaikkonen et al. 2010; Japhet et al. 2019) . Consequently, the clinical importance of AiV is unclear (Rivadulla and Romalde 2020) , although some studies do support the virus as an enteric pathogen causing gastroenteritis (Yang et al. 2009; Drexler et al. 2011; Rivadulla et al. 2019) . Human AiV is currently divided into three genotypes (A-C), based on differences in the sequences encoding the C-terminus of the 3C protease and the N-terminus of the 3D RNA-dependent RNA-polymerase (RdRp) (3CD junction) (Yamashita et al. 2000; Kitajima and Gerba 2015) . RT-PCR-based assays targeting this junction and the VP1 capsid protein are widely used for AiV detection and genotyping (Oh et al. 2006; Pham et al. 2007; Ambert-Balay et al. 2008; Lodder et al. 2013; Ibrahim et al. 2017a) . Genotypes A and B are prevalent in clinical and environmental samples from Africa, America, Asia and Europe (Rivadulla and Romalde 2020) , while genotype C has only ever been detected in one clinical sample from France (Ambert-Balay et al. 2008) .

Hepatitis A (HAV) is one of the major aetiological agents of acute hepatitis worldwide, infecting an estimated 1.5 million people per annum (WHO 2017; Lemon et al. 2018) . HAV is classified within the Hepatovirus genus of the Picornaviridae family and is subdivided into one serotype and six genotypes, of which three (I-III) infect humans (Smith and Simmonds 2018) . Several subtypes have been characterised, but HAV IA, IB, IIIA and IIIB are more commonly detected (Smith and Simmonds 2018) . HAV encodes a single polyprotein, which is cleaved into the capsid (VP1Px, VP2-4) and non-structural (2B, 2C and 3A-D) proteins (McKnight and Lemon 2018) . RT-PCR-based assays targeting the partial or full-length VP1 capsid protein, VP1-2A(Px) junction and VP1-2A(Px)-2B proteins are widely implemented for the detection and genotyping of HAV (Nainan et al. 2006; Coudray-Meunier et al. 2014) .

Hepatitis E Virus (HEV; family Hepeviridae) is classified within the genus Orthohepevirus and species Orthohepevirus A (Denner 2019). Eight genotypes have been characterised (HEV 1-8), although only five (HEV 1-4 and 7) are associated with human infection. Genotypes 1 and 2 are responsible for most sporadic and epidemic cases of hepatitis E, and are highly endemic in certain regions of Africa, Asia and Mexico (Smith and Simmonds 2018) . Genotypes 3, 4 and 7 are primarily zoonotic and are more typically associated with sporadic and clustered infections in developed regions (Nimgaonkar et al. 2018) . The HEV genome contains three ORFs (ORF1-3), although a fourth, ORF4, is present in genotype 1 (Nimgaonkar et al. 2018) . RT-PCRbased assays targeting the full or partial sequences of ORF1 (non-structural proteins) and ORF2 (capsid proteins) are typically used for the molecular characterisation and genotyping of HEV in clinical and environmental samples. However, other genomic regions are sometimes targeted as there is no consensus classification system for the differentiation of HEV genotypes (Al-Sadeq et al. 2018 ).

Human adenoviruses (HAdVs; family Adenoviridae) are endemic aetiological agents of enteric, respiratory and ocular diseases that are typically mild and self-limiting, but can develop into severe infections with unusual manifestations in immunocompromised individuals (reviewed by Khanal et al., 2018) . The global prevalence of enteric HAdVs in childhood diarrhoea varies from 1-8% and 2-31% in developed and developing countries (Meqdam and Thwiny 2007; Hassou et al. 2019) , respectively. In sub-Saharan Africa, HAdV was detected in approximately 10.8% of all gastroenteritis cases among children under five years of age between 2007 and 2019 . Currently, 103 HAdV types are reported and classified into seven species (A-G) within the Mastadenovirus genus (Kosulin, 2019; Mennechet et al., 2019; Brister et al. 2019) . Classification of the first 51 types was based upon serological profiles of the dominant capsid proteins, however, sequence analysis is now the standard method for characterising novel types (Mennechet et al. 2019) . The large dsDNA genomes of HAdV encode many genes, including those for the hexon, penton and fibre proteins which constitute most of the viral capsid (Vellinga et al. 2005; Mennechet et al. 2019) . PCRbased assays targeting the sequences encoding the hexon and fibre proteins have become the accepted method for HAdV detection, in both clinical and environmental samples (Jiang 2006) . HAdV species F, types 40 and 41 account for almost all cases of HAdV-related gastroenteritis. Types within groups A, C, D and G have been detected in patients presenting with diarrhoea, but potential roles for these viruses in the aetiology of gastroenteritis remain unclear (Lion 2014; Afrad et al. 2018) . Studies using next-generation sequencing (NGS) have documented the circulation of a wide range of HAdV species and types in sewage and wastewater in different countries (Ogorzaly et al. 2015; Iaconelli et al. 2017 ).

Human bocaviruses (HBoVs; genus Bocaparvovirus) are recent members of the Parvovirus family and have been detected globally in a variety of clinical samples (Guido et al. 2016 ). Four HBoVs are described and classified into two species (Primate bocaparvovirus 1: HBoV-1 and HBoV-3; Primate bocaparvovirus 2: HBoV-2 and HBoV-4) (Söderlund-Venermo 2019). HBoV-1 was first isolated from nasopharyngeal aspirates and is associated with respiratory tract infections in children (Christensen et al. 2019 ). HBoV-2 and HBoV-4 are frequently detected in stools from diarrheic patients (Guido et al. 2016 ) but also asymptomatic individuals (Paloniemi et al. 2014 ) and are often found in conjunction with other enteric viruses, such as RV and NoV (Huang et al. 2010; Campos et al. 2016) . Consequently, the role of HBoVs in gastroenteritis remains to be clarified (Ong et al. 2016) . Several PCR-based assays have been developed for the molecular detection of HBoV DNA in clinical and environmental samples (Lu et al. 2006; Iaconelli et al. 2016; La Rosa et al. 2016 , 2018 . These assays are specific for the sequences encoding the conserved non-structural protein (NS1) and moderately conserved nuclear phosphoprotein (NP1), while the hypervariable region encoding the VP1/ VP2 capsid proteins is commonly targeted for the differentiation of genotypes (Guido et al. 2016; Lee et al. 2016; Wagner et al. 2016) . Globally, HBoVs have been detected in environmental samples such as sewage wastewater (Blinkova et al. 2009; Iaconelli et al. 2016) , river water (La ) and shellfish (La Rosa et al. 2018; Onosi et al. 2020) , highlighting potential routes of transmission.

Human enteric viruses are shed at high concentrations (10 5 -10 13 viral particles per gram of stool) in the faeces of infected individuals (Bosch 1998; Atmar et al. 2008; Drexler et al. 2011; Bosch et al. 2014) , with or without illness and often long after the cessation of symptoms (Yotsuyanagi et al. 1996; Shastri et al. 1998; Murata et al. 2007; Takahashi et al. 2007; Kapusinszky et al. 2012; Crawford et al. 2017) . Untreated sewage wastewater is therefore a significant source of enteric pathogens and requires decontamination prior to discharge in the environment. However, traditional treatment processes do not completely reduce viral loads as many enteric viruses can withstand physical treatment procedures and disinfectants such as chlorination and UV irradiation (La Rosa et al. 2010; Okoh et al. 2010; Qiu et al. 2015; Sidhu et al. 2018; Prado et al. 2019 ). Consequently, a high concentration of surviving virions may be discharged into receiving water bodies such as springs, rivers, dams or marine estuaries upon the release of inadequately treated effluent. Alternatively, raw sewage may enter the environment through damaged sewage infrastructure and wet weather overflows such as heavy rainfall events (Ahmed et al. 2020b ). Moreover, many developing countries lack adequate sanitation infrastructure altogether, and surrounding water sources are easily contaminated with excreta containing enteric pathogens (Wang et al. 2014; Kayembe et al. 2018; Farkas et al. 2020) . Indeed, it is estimated that only 28% of sewage wastewater is treated prior to discharge into surface waters in low-and middle-income countries (WWAP and UNESCO 2017) .

Enteric viruses are highly stable in water environments, particularly when bound to particulate matter (Bosch 1998; Okoh et al. 2010; Seitz et al. 2011 ). Adsorption to solid particles facilitates the dispersion of viruses along water systems and the settling and accumulation of virions within sediments, where they may persist for prolonged periods (Goyal et al. 1984; Hassard et al. 2016) . Disturbance of these sediments releases viruses back into the water column, enabling further dissemination through the water system (Bosch 1998) . Enteric viruses have very low infectious doses (Okoh et al. 2010) ; for example, the 50% human infectious dose (HID) 50 of NoV is 18 virus particles, while for RV, only 1 focus forming unit (ffu) is required to infect 25% of susceptible adults (Yezli and Otter 2011; Hall 2012) . Therefore, the use of untreated water from environmental sources often leads to outbreaks of viral diseases, even in cases where contamination is marginal (Sinclair et al. 2009 ).

The risk of enteric virus transmission arises not only from contact with polluted water but also from the consumption of bivalve shellfish grown and harvested in virus-contaminated waters (Lees 2000; Bellou et al. 2013) . Bivalve shellfish (molluscs) including clams, mussels, oysters and scallops are active filter-feeding species that remove and sequester food particles together with a myriad of waterborne microbes. These bivalves sieve many gallons of water a day through their gills, (Burkhardt and Calci 2000; Rice 2001; Greening and Cannon 2016) , which can lead to the bioaccumulation of environmentally stable, viral pathogens within shellfish tissues, at concentrations far exceeding those in the overlying water column (Burkhardt and Calci 2000; Rehnstam-Holm and Hernroth 2005; Araud et al. 2016; Amoroso et al. 2020 ). Because of their ability to accumulate organic and inorganic contaminants, wild bivalve shellfish may be exploited as biological monitors for the surveillance of pollution in coastal environments (Viarengo and Canesi 1991; Donia et al. 2012; Gao et al. 2015; Kim et al. 2016) .

The consumption of shellfish harvested from faecally contaminated waters is directly associated with outbreaks of viral gastroenteritis (reviewed in Bellou et al., 2013) . Such outbreaks occur on a regular basis worldwide (Le Guyader et al. 2008; Westrell et al. 2010; Iritani et al. 2014; Lunestad et al. 2016; Woods et al. 2016; Meghnath et al. 2019 ) with potentially significant associated economic costs (Rheingans et al. 2009; Navas et al. 2015; Bartsch et al. 2016; Papadopoulos et al. 2019 ). Among the enteric viruses, NoV and HAV represent the majority of viral illnesses (Iizuka et al. 2010; Pepe et al. 2012; Fusco et al. 2013 Fusco et al. , 2019 La Bella et al. 2017) , although other viruses like HEV, HAstV, RV, SaV and AiV impact shellfisheries with symptoms that are more or less similar to those caused by NoVs (Pina et al. 1998; Le Guyader et al. 2008; Nakagawa-Okamoto et al. 2009; Iritani et al. 2014; La Bella et al. 2017; La Rosa et al. 2018) .

To reduce the risk of shellfish-associated infections, sanitary regulations based on bacterial indicators (e.g. Escherichia coli and Salmonella) in shellfish or their growing waters have been instituted in many countries. However, the inadequacy of the bacterial indicators for virus detection makes it necessary to develop new prevention strategies based on viral analysis, for improved regulatory standards (Flannery et al. 2009; Baert et al. 2011) . Furthermore, methods to process shellfish post-harvest (e.g. depuration, relaying and heat treatment) are effective at reducing bacterial loading, but their efficacy at reducing viral loading to non-infectious levels may be limited (Baker 2016; Richards 2016). Consequently, improved processing procedures need to be developed to enhance shellfish safety.

Over one-hundred studies from twelve African countries have reported on the presence of enteric viruses in environmental water samples ( Figure 1 ). These studies were identified using the electronic databases PubMed and Google Scholar and the search words "enteric virus", "rotavirus", "norovirus", "sapovirus", "calicivirus", "astrovirus", "enterovirus", "hepatitis A virus", "aichivirus", "hepatitis E virus", "adenovirus", "bocavirus", "wastewater", "sewage", "effluent", "influent", "drainage water", "drinking water", "ground water", "surface water", "irrigation water", "Africa" and "name of country" in various combinations. Most of the studies were conducted in South Africa (39), Egypt (23) and Tunisia (18), followed by Kenya, Ghana, Morocco and then Uganda with seven, five, five and three studies, respectively. Two studies were conducted each in Tanzania and Nigeria, while only one study was conducted each in Côte d'Ivoire, Benin and Chad. These studies were conducted between 1995 and 2020, and the duration of sampling ranged from one month to four years. Collectively, the reports describe the presence, prevalence and diversity of enteric viruses in sewage, wastewater effluent, ground and surface water, and even piped municipal water (reviewed below), indicating the widespread contamination of African water sources with these viral pathogens (Table 1) .

A wide range of viruses have been detected in sewage from wastewater treatment plants across Africa. Kiulia et al. (2010) detected HAdV in 87.5-100% and RVA in 20-100% of raw sewage samples from two sewage treatment plants in Nairobi, Kenya, while another study detected calicivirus (NoV and SaV) RNA in 82% of raw sewage samples collected from 21 sewage treatment facilities across South Africa (Murray et al. 2013a ). More recently, Shaheen et al. (2019a, b) detected AiV RNA and HBoV DNA in 16.6% and 41.6% of untreated raw sewage samples collected at the Abu-Rawash wastewater treatment plant in Giza, while HAdV and RV A were detected in 50% of urban sewage samples collected from the same site, with concentrations ranging from 10 3 -10 8 genome copies/litre (GC/L) (Elmahdy et al. 2020) . Enteric viruses were also recovered from final wastewater effluents in Egypt (Kamel et al. 2010 Hamza et al., (2017) detected HBoV-1, -2 and -3 at concentrations of 2.9 × 10 3 GC/L, 4.1 × 10 3 GC/L and 2.1 × 10 3 GC/L in 34.3%, 84.4% and 87.5% of treated effluent samples, respectively. These samples were collected from three wastewater treatment plants in Greater Cairo which ultimately discharge treated effluents into the River Nile and Al Manzala Lake (Hamza et al. 2017) . A separate study examined the prevalence of SaV at four Tunisian wastewater treatment plants between 2009 and 2010 and found that treatment did not sufficiently reduce SaV loads as concentrations of SAV RNA were relatively high in both influent and effluent samples (Varela et al. 2018) . These studies highlight the need for improved wastewater treatment methodologies that eliminate enteric viruses from wastewaters prior to discharge into African water environments.

There is a significant lack of basic sanitation services and proper wastewater treatment in many African countries (Wang et al. 2014) . For example, only 18%, 26%, 39% and 61% of people living in Algeria, Libya, Morocco and Murray and Taylor 2015) and Uganda (Katukiza et al. 2013a (Katukiza et al. , 2013b Sadik 2016) have reported the contamination of groundwater sources such as boreholes, springs and wells with enteric viruses including EV, HAdV, NoV, SaV and RV.

Untreated or partially treated sewage effluent is a major contaminant of surface water sources in many African cities (Omosa et al. 2012; Adewumi and Oguntuase 2016; Herbig 2019; Okubo et al. 2019) , and enteric viruses including EV, HAdV, HAV, HBoV and RV are frequently detected in African rivers, dams and lakes at high concentrations ranging from 1.3 × 10 1 -1.5 × 10 7 GC/L (Hamza et al. 2009; Chigor and Okoh 2012a; Katukiza et al. 2013b; Shaheen et al. 2019b ). The Nile is the main source of water for irrigation and domestic use in Egypt, however, many studies have found this river to be polluted with enteric viruses (El-Senousy et al. 2013a Shaheen et al. 2019b) . For example, 4%, 25%, 16.6%, 8.3% and 12.5% of water samples collected from the Rosetta branch of the Nile in 2017 and 2018 were contaminated with AiV, AstV, NoV, RV and HBoV, respectively (Shaheen et al. 2018 (Shaheen et al. , 2019a Shaheen and Elmahdy 2019) , while more recently, Rizk and Allayeh, (2020) detected RVA RNA in 18.75% of Nile water samples collected in Giza. Similarly, enteric viruses have been found in major surface waters in Kenya, Chad, Nigeria and Uganda (Kiulia et al. 2010 (Kiulia et al. , 2014 Guerrero-Latorre et al. 2011; Katukiza et al. 2013a Katukiza et al. , 2013b Baker et al. 2018; Bauza et al. 2019 ; van Zyl et al. 2019; Muhammad et al. 2020) . For example, two separate studies detected EV and HAdV in water samples from Homa Bay, Lake Victoria (Sadik 2016; Opere 2019) . Over the last 25 years, many studies have revealed the presence of enteric viruses in South African rivers and dams, which are essential water sources for the surrounding communities Sibanda and Okoh 2012; Saïd et al. 2014; Potgieter et al. 2020 ). For example, several studies have identified HAdV, HAV and (Shaheen et al. 2019b) in some cases EV, NoV and RV in water samples from the Tyume and Buffalo rivers of the Eastern Cape Okoh 2012a, 2012b; Okoh 2012, 2013) , the Klip River and Vaal dam in the Gauteng province , and the Umhlangane river in KwaZulu-Natal (Marie and Lin 2017) . From 2008 to 2010, Mans et al. (2013) reported the presence of NoV RNA in 66%, 95% and 21% of water samples from the Klip, Rietspruit and Suikerbosrant rivers, respectively. During this period, SaV RNA was detected in 39-54%, 83-92% and 14-20% of water samples from the same rivers (Murray et al. 2013b ). More recently, HAdV, NoV GI and GII together with EV, HAV, HAstV, HAdV and SaV were detected in water samples from the Madadzhe river in the Limpopo province, which is exploited for domestic and agricultural activities (Potgieter et al. 2020) .

The widespread contamination of African rivers, canals, dams and lakes with viral pathogens constitutes a significant health risk to the millions of people who depend on these surface waters for drinking, irrigational, domestic and recreational activities (Chigor et al. 2014; Sibanda et al. 2015; Pichel et al. 2019; UNESCO 2019) . From 2002 to 2004 van Zyl et al. (2006) detected RV A in 14% of irrigation water samples and 1.7% of corresponding raw vegetable samples collected in the Western Cape, Gauteng and Limpopo provinces of South Africa. In Egypt, marginal water from drainage canals, often contaminated with enteric pathogens, is unofficially used for the irrigation of crops, despite the increased risk of viral contamination of agricultural products. El-Senousy et al. (2013b) detected NoV RNA in 31.9% of irrigation water samples from the Daqahlia governorate in 2008 and 2009, while more recently, Okubo et al. (2019) identified AiV, EV, HAdV, HAV, HEV, NoVs (GI, GII and GIV) and RV in 100% of irrigation water samples from the Umoum agricultural drainage canal, and its tributaries. Enteric viruses have even been identified in treated drinking water produced at several treatment facilities across Africa (Ali et al. 2004; Ehlers et al. 2005 ; van Zyl et al. 2006; El-Senousy et al. 2014) . In South Africa, Grabow et al. (2001) recovered viable EV, HAdV and HAV in 23% of chlorinated drinking water samples, while van Heerden and colleagues detected HAdV in 29.8% and 5.32% of drinking water samples between 2001 -2002 and 2002 , respectively (van Heerden et al. 2004 , 2005b . Similar studies have reported the presence of EV, HAV, HEV, HAstV, NoV and RV in chlorinated drinking water in Egypt (Ali et al. 2004; El-Senousy et al. 2007 Rizk and Allayeh 2018) . Recently, Gad et al. (2019) detected HAdV DNA in 8.9%, and RV RNA in 15.6% of tap water samples from five Egyptian cities including Cairo and Giza. Furthermore, treated tap and kiosk water in Uganda and Ghana have been found to be contaminated with enteric viruses including EV and NoV (GII), respectively (Gibson et al. 2011; Sadik 2016) . 

Over the past two decades, only seventeen studies detecting human enteric viruses in African shellfish have been reported (Figure 2 and Table 2 ). These studies were identified by searching the PubMed and Google Scholar databases for studies which included terms such as "enteric virus", "rotavirus", "norovirus", "sapovirus", "calicivirus", "astrovirus", "enterovirus", "hepatitis A virus", "aichivirus", "hepatitis E virus", "adenovirus", "bocavirus", "shellfish", "mussel", "cockle", "periwinkle", "oyster" "Africa" and the names of African countries. The first report was published by Karamoko et al. (2005) , who detected HAdV in 20% of mussel samples grown in Casablanca, Morocco (Karamoko et al. 2005 ). Subsequently, two additional studies reported the presence of HAdV in African shellfish; Vos and Knox (2018) detected HAdV D17 in mussels collected from the Swartkops river estuary in Port NoV (GI and GII) in 15% and HAV in 6% of Moroccan shellfish at high concentrations, ranging from 4.7 × 10 3 to 7.7 x 10 7 GC/g digestive tissue. Similarly, enteric viruses have been detected in bivalve molluscs grown along the Tunisian coastline (Gharbi-khelifi et al. 2007; Zormati et al. 2018) . Elamri (2006) detected HAstV in 61%, NoV in 35%, HAV in 26% and EV in 4.3% (one mussel) of shellfish (mussels and clams) collected from Tunisian waters from July 2000 to September 2001. In two separate studies, 1.6% and 6.6% of shellfish collected from a fishing zone located near a wastewater outlet site in Monastir, Tunisia, tested positive for NoV (GI.2) and AiV A, respectively (Sdiri-Loulizi et al. 2010a , 2010b . Furthermore, Onosi et al (2019) reported the presence of AiV B in mussels collected from the Swartkops river estuary in Port Elizabeth, South Africa. In another study, the authors detected HBoV-2 in the same mussel samples, making it the first report of HBoV in shellfish from Africa (Onosi et al. 2020) . Finally, there are only single reports of enteric viruses in shellfish from Mozambique (Nenonen et al. 2006) and Nigeria (Babalola et al. 2019) , where HAV IB and NoV were detected in clams and periwinkles, respectively. To date, there are only a few reports of shellfish-associated gastroenteritis from Africa (Potasman et al. 2002; Bellou et al. 2013 ); however, the aforementioned studies highlight the risk of transmission and disease outbreak through the consumption of virus-contaminated shellfish grown in African waters. The presence of viral pathogens in edible molluscs is a health risk not only for local populations but also for people in countries where such foods are imported. For example, Moroccan molluscs exported to Spain were previously found to be contaminated with NoV and HAstV (Polo et al. 2010) , while recent outbreaks of gastroenteritis in North America, Australia and Europe were attributed to the consumption of food products imported from Egypt (Aboubakr and Goyal 2019) . Collectively, these reports highlight the need for efficient surveillance programmes and epidemiological studies to fully understand the burden of virus-contaminated shellfish on public health and economies in Africa.

Enteric viruses remain a serious public health threat globally, posing an enormous burden on the economies of many countries. This is particularly true of the developing world where most of the population tend to inhabit urban informal settlements or rural areas, and where the predominant mode of transmission is linked to sewage-contaminated water. This review testifies to the extent of the problem on the African continent by reviewing over 100 investigations conducted in 13 African countries in which the occurrence (Onosi et al. 2020) of enteric viruses was described in a wide range of samples including not only raw sewage but also groundwater, open water sources, bivalve shellfish and, alarmingly, drinking water. While many of these studies are limited to simple molecular detection of specific viruses in selected samples a few go further to describe the quantification, prevalence and links to disease outbreaks (see for example: El-Senousy et al. 2015 Elmahdy et al. 2019; Okubo et al. 2019) . When assessing the public health risks posed by enteric viruses in the environment, it must be acknowledged that standard molecular-based detection methods cannot discriminate between infectious viruses and non-viable virus particles and that additional data is needed for accurate risk estimates (Rodríguez et al. 2009; Leifels et al. 2016 ). The first step in attempting to alleviate the burden of disease will be to further understand the true prevalence, molecular epidemiology, viability and circulation of enteric viruses by conducting systematic surveillance studies and evaluating the virological safety of water and food prior to consumption or utilisation for daily living purposes. Recently, sewage epidemiology or wastewater-based epidemiology (WBE) has been successfully used as a surveillance and non-invasive early warning approach for outbreaks of pathogenic enteric viruses such as poliovirus, HAV and NoV (Asghar et al. 2014; Hellmér et al. 2014) . In light of the current COVID-19 pandemic, research groups worldwide are evaluating this tool as a way to predict future coronavirus outbreaks (Ahmed et al. 2020a; Bivins et al. 2020; Haramoto et al. 2020; Kumar et al. 2020; La Rosa et al. 2020; Medema et al. 2020; Nemudryi et al. 2020; Wu et al. 2020) . Along with clinical testing, WBE may represent a viable means of largescale population-wide surveillance of imminent infectious disease outbreaks, particularly in resource poor regions in African nations. Additionally, Quantitative Microbial Risk Assessment (QMRA) could be used to estimate population health risks posed by these waterborne pathogens and inform water management strategies (Howard et al. 2006; Owens et al. 2020) . Although QMRA has been widely used in developed countries (Bichai and Smeets 2013; Owens et al. 2020) , less-developed countries such as those in Africa, with limited data and resources, have greater challenges when applying this technique (Howard et al. 2006; Chigor et al. 2014; Van Abel and Taylor 2018) . A recent review of QMRA in sub-Saharan Africa (Van Abel and Taylor 2018) outlined these challenges such as the lack of quantification data and defined several steps including the collection of further data on virus detection, concentration and infectivity, to improve this methodology within the region. The fact that reports of enteric viruses in water environments to date are limited to only one quarter of Africa's 54 countries highlights the need for further investigations to better understand the occurrence of these pathogens and their associated public health risk on the continent. Moreover, because wastewater treatment systems in African countries tend to be either non-existent or poorly managed, the threat of human exposure to enteric viruses will remain. There is thus an urgent need for all stakeholders including governments, the private sectors and the public to invest heavily in basic sanitation services as well as the development of innovative wastewater treatment strategies to reduce faecal contamination of vital water sources utilised for irrigation, drinking, food-processing and domestic or recreational activities. Ahmed, W., Payyappat, S., Cassidy, M., Harrison, N., & Besley, C. (2020b (2015) . Prevalence of rotaviruses groups A and C in Egyptian children and aquatic environment. Food and Environmental Virology, 7(2), 132-141. https ://doi.org/10.1007/s1256 0-015-9184-6. Ezeh, A., Oyebode, O., Satterthwaite, D., Chen, Y. F., Ndugwa, R., Sartori, J., et al. (2017) . The history, geography, and sociology of slums and the health problems of people who live in slums. The Lancet, 389 (10068) 

Molecular Detection and Genotyping of Group A Rotavirus by Multiplex Semi-Nested RT-PCR in Sewage Water and Sludge

Involvement of Egyptian foods in foodborne viral illnesses: The burden on public health and related environmental risk factors: An overview. Food and Environmental Virology

Quantitative PCR Detection and Characterisation of Human Adenovirus, Rotavirus and Hepatitis A Virus in Discharged Effluents of Two Wastewater Treatment Facilities in the Eastern Cape

Isolation and identification of enteroviruses from sewage and sewage-contaminated water in lagos

Planning of wastewater reuse programme in Nigeria

Detection of enteric-and nonenteric adenoviruses in gastroenteritis patients

First confirmed detection of SARS-CoV-2 in untreated wastewater in Australia: A proof of concept for the wastewater surveillance of COVID-19 in the community

Detection of Human Enterovirus and Adenovirus in Shellfish Collected in

Norovirus and other human enteric viruses in Moroccan shellfish. Food and Environmental Virology

Urban sanitation coverage and environmental fecal contamination: links between the household and public environments of

Aichivirus in children with diarrhea in Northern Italy

Using QMRA-based regulation as a water quality management tool in the water security challenge: Experience from the Netherlands and Australia

Enteric Viruses

Wastewater-based epidemiology: Global Collaborative to maximize contributions in the fight against COVID-19. Environmental Science and Technology

Frequent detection of highly diverse variants of cardiovirus, cosavirus, bocavirus, and circovirus in sewage samples collected in the United States

Human Enteric Viruses in the Water Environment: A Minireview

Human astroviruses

Waterborne Transmission of Enteric Viruses and Their Impact on Public Health

Risk Factors for Infectious Diseases in Urban Environments of sub-Saharan Africa: A Systematic Review and Critical Appraisal of Evidence. Tropical Medicine and Infectious Disease

HAdV Working Group

Selective accumulation may account for shellfish-associated viral illness

Human bocavirus in acute gastroenteritis in children in Brazil

Enterovirus D68 -the new polio? Frontiers in Microbiology

Global Spread of Norovirus GII

Rapid Emergence and Predominance of a Broadly Recognizing and Fast-Evolving Norovirus GII

Enterovirus and encephalitis

Updated classification of norovirus genogroups and genotypes

Quantitative RT-PCR detection of hepatitis A virus, rotaviruses and enteroviruses in the Buffalo River and source water dams in the Eastern Cape Province of South Africa

Quantitative Detection and Characterization of Human Adenoviruses in the Buffalo River in the Eastern Cape Province of South Africa. Food and Environmental Virology

Assessment of the risks for human health of adenoviruses, hepatitis a virus, rotaviruses and enteroviruses in the Buffalo River and three source water dams in the Eastern Cape. Food and Environmental

Human bocaviruses and paediatric infections. The Lancet Child and Adolescent Health

Detection and characterization of aichi virus 1 in pediatric patients with diarrhea in Thailand

Astrovirus VA1 identified by next-generation sequencing in a nasopharyngeal specimen of a febrile Tanzanian child with acute respiratory disease of unknown etiology

Hepatitis A Virus Subgenotyping Based on RT-qPCR Assays

Rotavirus Infection

Human norovirus transmission and evolution in a changing world

Hepatitis E Virus (HEV) -The Future

Genetic diversity of human sapovirus across the Americas

The broad host range and genetic diversity of mammalian and avian astroviruses

Molecular isolation of human norovirus and astrovirus in tap water by RT-PCR

Presence of hepatitis E RNA in mussels used as bio-monitors of viral marine pollution

Aichi virus shedding in high concentrations in patients with acute diarrhea

Detection of enteroviruses in untreated and treated drinking water supplies in South Africa

Norovirus Detection at Oualidia Lagoon, a Moroccan Shellfish Harvesting Area, by Reverse Transcription PCR Analysis

Detection of human enteric viruses in shellfish collected in Tunisia

Molecular detection of human adenovirus in urban wastewater in Egypt and among children suffering from acute gastroenteritis

Quantitative Detection of Human Adenovirus and Human Rotavirus Group A in Wastewater and El-Rahawy Drainage Canal Influencing River Nile in the North of Giza

Clinical and Environmental Surveillance of Rotavirus Common Genotypes Showed High Prevalence of Common P Genotypes in Egypt

Molecular Epidemiology of Human Adenoviruses and Rotaviruses as Candidate Viral Indicators in the Egyptian Sewage and Water Samples

Method validation for norovirus detection in naturally contaminated irrigation water and fresh produce

Prevalence of Human and Animal Rotaviruses and HEV in Egyptian Nile Water Resources

Viral pathogens in water: occurrence, public health impact, and available control strategies. Current Opinion in Virology

Evaluation of human enteric viruses in surface water and drinking water resources in Southern Ghana

Evidence of rotavirus vaccine impact in sub-Saharan Africa: Systematic review and meta-analysis

Rotavirus and autoimmunity

Human pathogenic viruses at sewage sludge disposal sites in the Middle Atlantic region

Assessment of cell culture and polymerase chain reaction procedures for the detection of polioviruses in wastewater

New methods for the detection of viruses: call for review of drinking water quality guidelines

Pit Latrines and Their Impacts on Groundwater Quality:: A Systematic Review. Environmental Health Perspectives

Human and Animal Viruses in Food (Including Taxonomy of Enteric Viruses)

Occurrence of waterborne enteric viruses in two settlements based in Eastern Chad: analysis of hepatitis E virus, hepatitis A virus and human adenovirus in water sources

Human bocavirus: current knowledge and future challenges

State of the world's cities 2012/2013: prosperity of cities

Noroviruses: The perfect human pathogens?

Prevalence of rotavirus, adenovirus, and astrovirus infections among patients with acute gastroenteritis in, Northern Iran

Detection and Characterization of Hepatitis A Virus Circulating in Egyptian Environment

Relative Abundance of Human Bocaviruses in Urban Sewage in Greater Cairo

Detection and quantification of human bocavirus in river water

Antigenic diversity of human sapoviruses

First environmental surveillance for the presence of SARS-CoV-2 RNA in wastewater and river water in Japan

Search of Enteroviruses in Water Media in Marrakech

Abundance and distribution of enteric bacteria and viruses in coastal and estuarine sediments-a review

Détection des virus entériques dans les Eaux Usées de la Région de Monastir par RT-PCR

Detection and genotyping of group A rotaviruses isolated from sewage samples in

Molecular detection of human noroviruses in influent and effluent samples from two biological sewage treatment plants in the region of Monastir

Enteric Adenoviruses: Emerging of a Public Health Threat

Detection of Pathogenic Viruses in Sewage Provided Early Warnings of Hepatitis A Virus and Norovirus Outbreaks

Pathogen Surveillance in the Informal Settlement, Kibera, Kenya Using a Metagenomics Approach

Talking dirty -effluent and sewage irreverence in South Africa: A conservation crime perspective

Molecular epidemiology of noroviruses detected in Vietnamese children with acute gastroenteritis from 2012 to 2015

Quantitative microbial risk assessment to estimate health risks attributable to water supply: Can the technique be applied in developing countries with limited data?

Detection of, and frequent co-infection with, human bocavirus in faecal specimens from children in Wuhan

Frequent detection and genetic diversity of human bocavirus in urban sewage samples. Food and Environmental Virology

Molecular characterization of human adenoviruses in urban wastewaters using next generation and sanger sequencing

Quantification and Molecular Characterization of Norovirus After two Wastewater Treatment Procedures

Quantification and genotyping of rotavirus a within two wastewater treatment processes

Detection of Sapoviruses in two biological lines of Tunisian hospital wastewater treatment

Detection of aichi virus genotype B in two lines of wastewater treatment processes

Molecular detection and genotypic characterization of enteric adenoviruses in a hospital wastewater

Removal of human astroviruses from hospital wastewater by two biological treatment methods: natural oxidizing lagoons and rotating biodisks

Detection of sapoviruses and noroviruses in an outbreak of gastroenteritis linked genetically to shellfish

Detection and genetic characterization of human enteric viruses in oyster-associated gastroenteritis outbreaks between 2001 and 2012 in Osaka City

Viral gastroenteritis among children of 0-5 years in Nigeria: Characterization of the first Nigerian aichivirus, recombinant noroviruses and detection of a zoonotic astrovirus

Presence and fate of coliphages and enteric viruses in three wastewater treatment plants effluents and activated sludge from Tunisia

Human adenoviruses in water: occurrence and health implications: A critical review

Aichi virus infection in children with acute gastroenteritis in Finland

Evidence of the co-circulation of enteric viruses in sewage and in the population of greater Cairo

Presence of enteric hepatitis viruses in the sewage and population of greater Cairo

Nearly constant shedding of diverse enteric viruses by two healthy infants

Adenovirus detection in shellfish and urban sewage in Morocco (Casablanca Region) by the polymerase chain reaction

Assessment of enterovirus contamination in mussel samples from Morocco

Incidence of enteroviruses in groundwater from public baths of Mohammedia (Morocco)

Quantification of microbial risks to human health caused by waterborne viruses and bacteria in an urban slum

Genomic copy concentrations of selected waterborne viruses in a slum environment in Kampala

High levels of faecal contamination in drinking groundwater and recreational water due to poor sanitation, in the sub-rural neighbourhoods of Kinshasa, Democratic Republic of the Congo

The Repertoire of Adenovirus in Human Disease: The Innocuous to the Deadly

Risk from Viral Pathogens in Seafood

Surveillance of aquatic animal viruses in seawater and shellfish in Korea

Aichi Virus 1: environmental occurrence and behavior

Genetically distinct genogroup IV norovirus strains identified in wastewater

Temporal variations in genotype distribution of human sapoviruses and aichi virus 1 in wastewater in Southern Arizona, United States

Norovirus GII.17 Predominates in Selected Surface Water Sources in Kenya

The detection of enteric viruses in selected urban and rural river water and sewage in Kenya, with special reference to rotaviruses

Intestinal HAdV infection: Tissue specificity, persistence, and implications for antiviral therapy

Amplification of echoviruses genomic regions by different RT-PCR protocols -a comparative study

Proposal for a unified norovirus nomenclature and genotyping

First proof of the capability of wastewater surveillance for COVID-19 in India through detection of genetic material of SARS-CoV-2

Food-borne viruses in shellfish: investigation on norovirus and HAV presence in Apulia (SE Italy)

Human bocavirus in children with acute gastroenteritis in Albania

First detection of SARS-CoV-2 in untreated wastewaters in Italy

Quantitative real-time PCR of enteric viruses in influent and effluent samples from wastewater treatment plants in Italy. Annali dell'Istituto superiore di sanita

Detection of human bocavirus species 2 and 3 in bivalve shellfish in

The impact of anthropogenic pressure on the virological quality of water from the Tiber River

Urban groundwater quality in sub-Saharan Africa: Current status and implications for water security and public health

Aichi Virus, Norovirus, Astrovirus, Enterovirus, and Rotavirus Involved in Clinical Cases from a French Oyster-Related Gastroenteritis Outbreak

Human Bocavirus in Korean Children with Gastroenteritis and Respiratory Tract Infections

Viruses and bivalve shellfish

From lab to lake -evaluation of current molecular methods for the detection of infectious enteric viruses in complex water matrices in an urban area

Type A viral hepatitis: A summary and update on the molecular virology, epidemiology, pathogenesis and prevention

Viral agents of acute gastroenteritis in hospitalized children in Greece

Precise genotyping and recombination detection of enterovirus

Detection of human enteric viruses in Umgeni River

Evolution of the genome of Human enterovirus B: incongruence between phylogenies of the VP1 and 3CD regions indicates frequent recombination within the species

Adenovirus infections in immunocompetent and immunocompromised patients

The Role of Seafood in Foodborne Diseases in the United States of America

Etiological Role and Repeated Infections of Sapovirus among Children Aged Less than 2 Years in a Cohort Study in a Peri-urban Community of

Aichi Virus in Sewage and Surface Water, the

Gastroenteritis Outbreaks Caused by Norovirus GII

Real-Time PCR Assays for Detection of Bocavirus in Human Specimens

Enteroviruses in the early 21st century: New manifestations and challenges

An outbreak of norovirus infection from shellfish soup due to unforeseen insufficient heating during preparation

Microbial groundwater quality status of hand-dug wells and boreholes in the Dodowa Area of Ghana

Environmental Surveillance for Noroviruses in Selected South African Wastewaters

The Molecular Characterisation of Human Adenoviruses from Human Specimens and Environmental Samples

Distribution and genetic variability of sapoviruses in Africa

Genetic diversity of sapoviruses among inpatients in Germany

Norovirus Epidemiology in Africa: A Review

Diverse norovirus genotypes identified in sewagepolluted river water in South Africa

Viruses in the environment -presence and diversity of bacteriophage and enteric virus populations in the Umhlangane River

Optimization of a PCR method for the detection of astrovirus type 1 in environmental samples

Human health risk assessment for the occurrence of enteric viruses in drinking water from wells: role of flood runoff injections

Enteric Pathogens in Stored Drinking Water and on Caregiver's Hands in Tanzanian Households With and Without Reported Cases of Child Diarrhea

Hands and water as vectors of diarrheal pathogens in Bagamoyo

Hepatitis A Virus Genome Organization and Replication Strategy. Cold Spring Harbor perspectives in medicine

Presence of SARS-coronavirus-2 RNA in sewage and correlation with reported COVID-19 prevalence in the early stage of the epidemic in the Netherlands

Outbreaks of norovirus and acute gastroenteritis associated with British Columbia Oysters

A review of 65 years of human adenovirus seroprevalence

Prevalence of group a rotavirus, enteric adenovirus, norovirus and astrovirus infections among children with acute gastroenteritis in Al-Qassim, Saudi Arabia

Effects of rainfalls variability and physical-chemical parameters on enteroviruses in sewage and lagoon in Yopougon

Environmental Survey of Rotavirus in Sewage Water within Maiduguri Metropolis

Prolonged Norovirus Shedding in Infants ≤6 Months of Age with Gastroenteritis. Pediatric Infectious Disease

Human calicivirus diversity in wastewater in South Africa

First detection of human sapoviruses in river water in South Africa

Application of a competitive internal amplification control for the detection of sapoviruses in wastewater. Food and Environmental Virology

Quantification and molecular characterisation of human sapoviruses in water sources impacted by highly polluted discharged wastewater in South Africa

GIV Noroviruses in wastewaters and in stool specimens from hospitalized patients. Food and Environmental Virology

Molecular characterization of astroviruses by reverse transcriptase PCR and sequence analysis: Comparison of clinical and environmental isolates from South Africa

Diagnosis of hepatitis A virus infection: A molecular approach

Detection of multiple sapovirus genotypes and genogroups in oyster-associated outbreaks

Basic rationale, current methods and future directions for molecular typing of human enterovirus

Economic costs of outbreaks of acute viral gastroenteritis due to norovirus in Catalonia (Spain)

How urbanization affects the epidemiology of emerging infectious diseases

Temporal detection and phylogenetic assessment of SARS-CoV-2 in municipal wastewater

Detection of hepatitis A virus genotype IB variants in clams from Maputo Bay

Hepatitis E virus: Advances and challenges

Sensitive, seminested PCR amplification of VP1 sequences for direct identification of all enterovirus serotypes from original clinical specimens

Effect of eliminating open defecation on diarrhoeal morbidity: An ecological study of Nyando and Nambale subcounties

Molecular characterization of the first reported aichivirus A in Australia

Typing of human enteroviruses by partial sequencing of VP1

Molecular evolution of the human enteroviruses: correlation of serotype with VP1 sequence and application to picornavirus classification

Human adenovirus diversity in water samples using a next-generation amplicon sequencing approach

Molecular characterization of the first aichi viruses isolated in Europe and in South America

Comprehensive review of human sapoviruses

Inadequately treated wastewater as a source of human enteric viruses in the environment

Health Impact of Agricultural Drainage Water for Farmers in the West Nile Delta

Surveillance of Invasive Bacterial Pathogens and Human Enteric Viruses in Wastewater Final Effluents and Receiving Water Bodies -a Case Study from Durban, South Africa

Sustainable tertiary wastewater treatment is required for water resources pollution control in Africa

Human bocavirus in stool: A true pathogen or an innocent bystander?

The first molecular detection of aichi virus 1 in raw sewage and mussels collected in South Africa. Food and Environmental Virology

The first detection of human bocavirus species 2 and 3 in raw sewage and mussels in South Africa

Detection of Pathogenic Human Adenoviruses and Enteroviruses in Water Samples Collected From Lake Victoria Along Homa Bay Town

Enteric pathogens associated with gastroenteritis among children under 5 years in sub-Saharan Africa: A systematic review and meta-analysis. Epidemiology and Infection

Incidence of human adenoviruses and hepatitis A virus in the final effluent of selected wastewater treatment plants in Eastern Cape Province South Africa

Human enteric bacteria and viruses in five wastewater treatment plants in the Eastern Cape, South Africa

Efficiency of hepatitis A virus removal in six sewage treatment plants from central Tunisia

Implementation of quantitative microbial risk assessment (QMRA) for public drinking water supplies: Systematic review

Human bocaviruses are commonly found in stools of hospitalized children without causal association to acute gastroenteritis

The health and economic impact of acute gastroenteritis in Belgium

Prevalence of vaccine-derived polioviruses in sewage and river water in South Africa

Norovirus Monitoring in Bivalve Molluscs Harvested and Commercialized in Southern Italy

A comparison of the VP1, VP2, and VP4 regions for molecular typing of human enteroviruses

Chronic sequelae and severe complications of norovirus infection: A systematic review of literature

Isolation and molecular characterization of aichi viruses from fecal specimens collected in Japan

The Problem of drinking water access: A review of disinfection technologies with an emphasis on solar treatment methods

Viral pollution in the environment and in shellfish: Human adenovirus detection by PCR as an index of human viruses

Hepatitis A virus in urban sewage from two mediterranean countries

Aetiology-specific estimates of the global and regional incidence and mortality of diarrhoeal diseases commonly transmitted through food

Pathogen-specific burdens of community diarrhoea in developing countries: A multisite birth cohort study (MAL-ED). The Lancet Global Health

Imported mollusks and dissemination of human enteric viruses

Infectious outbreaks associated with bivalve shellfish consumption: A worldwide perspective

Human Enteric Pathogens in Eight Rivers Used as Rural Household Drinking Water Sources in the Northern Region of South Africa

Performance of wastewater reclamation systems in enteric virus removal

Rotavirus contamination of surface waters from the northwest of Argentina

The History of Enterovirus A71 Outbreaks and Molecular Epidemiology in the Asia-Pacific Region

Assessment of human virus removal during municipal wastewater treatment in Edmonton

Genetic characterization of a novel hepatitis A virus strain in irrigation water in South Africa

Enteroviruses in water environment -a potential threat to public health

Shellfish and Public Health: A Swedish Perspective

Economic costs of rotavirus gastroenteritis and cost-effectiveness of vaccination in developing countries

Environmental Impacts of Shellfish Aquaculture: Filter Feeding to Control Eutrophication

Shellfish-Associated Enteric Virus Illness: Virus Localization, Disease Outbreaks and Prevention

A Comprehensive Review on Human Aichi Virus

Epidemiology of Aichi Virus In Fecal Samples From Outpatients With Acute Gastroenteritis in Northwestern Spain

Multiplex semi-nested RT-PCR for genotyping of rotaviruses group A in Giza tap water Egypt

Genotyping of Rotaviruses in River Nile in Giza

Application of PCR-based methods to assess the infectivity of enteric viruses in environmental samples

An Overview of 20 years of studies on the prevalence of human enteric viruses in shellfish from Galicia Spain

A new real-time RT-PCR targeting VP4-VP2 to detect and quantify enterovirus D68 in respiratory samples

Quantification of Multiple Waterborne Pathogens in Drinking Waters, Drainage Channels, And Surface Waters in Kampala, Uganda Over Seven Months of Seasonal Variation

Molecular characterisation of hepatitis A virus strains from water sources in South Africa

Survival of Enteric Viruses in the Environment and Food

Detection and molecular characterization of enteric viruses in environmental samples in

First molecular detection of Aichi virus in sewage and shellfish samples in the Monastir region of Tunisia

Detection and Genomic Characterization of Aichi Viruses in Stool Samples from Children in

Waterborne outbreak of gastroenteritis on the

Molecular detection of three gastroenteritis viruses in an urban sewage treatment plant and river water in Egypt

Environmental monitoring of Aichi virus and human bocavirus in samples from wastewater treatment plant, drain, and River Nile in Egypt

Environmental monitoring of astrovirus and norovirus in the Rosetta branch of the River Nile and the El-Rahawy drain

Quantitative PCR-based identification of enteric viruses contaminating fresh produce and surface water used for irrigation in Egypt

Prevalence of Astroviruses in a Children's Hospital

Seasonal and spatio-temporal distribution of faecal-indicator bacteria in Tyume River in the Eastern Cape Province

Assessment of the incidence of enteric adenovirus species and serotypes in surface waters in the Eastern Cape Province of South Africa: Tyume River as a Case Study

Real-time PCR quantitative assessment of hepatitis A virus, rotaviruses and enteroviruses in the Tyume River located in the Eastern Cape Province

Urban effluent discharges as causes of public and environmental health concerns in South Africa's aquatic milieu

Comparative enteric viruses and coliphage removal during wastewater treatment processes in a sub-tropical environment. Science of the Total Environment

Norovirus Illness is a Global Problem: Emergence and Spread of Norovirus GII.4 Variants

Quantification of human norovirus GII, human adenovirus, and fecal indicator organisms in wastewater used for irrigation in

Viruses in recreational water-borne disease outbreaks: A review

Surveillance of Microbial Pathogens in the Umgeni River

Classification and Genomic Diversity of Enterically Transmitted Hepatitis Viruses. Cold Spring Harbor Perspectives in Medicine

Molecular characterization of an outbreak of enterovirusassociated meningitis in Mossel Bay

Emerging Human Parvoviruses: The Rocky Road to Fame

Distribution of Norovirus and Sapovirus Genotypes with Emergence of NoV GII.P16/GII.2 Recombinant Strains in Chiang Mai

High frequency of aichivirus in children with acute gastroenteritis in Iran

Prolonged Fecal Shedding of Hepatitis E Virus (HEV) during Sporadic Acute Hepatitis E: Evaluation of Infectivity of HEV in Fecal Specimens in a Cell Culture System

Acute and chronic disease caused by enteroviruses

Global, Regional, and National Estimates of Rotavirus Mortality in Children <5 Years of Age

The occurrence of hepatitis A and astroviruses in selected river and dam waters in South Africa

Occurrence of Norovirus GIV in Environmental Water Samples from Belém City, Amazon Region, Brazil. Food and Environmental Virology

Clinical characteristics of norovirusassociated deaths: A systematic literature review

Rotavirus Vaccination and the Global Burden of Rotavirus Diarrhea Among Children Younger Than 5 Years

The United Nations World Water Development Report 2019: Leaving no one behind. UNESCO Digital Library

The Use of Quantitative Microbial Risk Assessment to Estimate the Health Risk from Viral Water Exposures in sub-Saharan Africa: A review. Microbial Risk Analysis

Prevalence, quantification and typing of adenoviruses detected in river and treated drinking water in South Africa

Incidence of adenoviruses in raw and treated water

Prevalence of human adenoviruses in raw and treated water

Molecular Epidemiology of Group A Rotaviruses in Water Sources and Selected Raw Vegetables in Southern Africa

Application of a molecular method for the detection of group A rotaviruses in raw and treated water

Detection of potentially pathogenic enteric viruses in environmental samples from kenya using the bag-mediated filtration system

Sapovirus in Wastewater Treatment Plants in Tunisia: Prevalence, Removal, and Genetic Characterization

Human Sapovirus Among Outpatients with Acute Gastroenteritis in Spain: A One-Year Study

The Adenovirus capsid: major progress in minor proteins

Detection of Adenoviruses and Rotaviruses in Drinking Water Sources Used In Rural Areas of Benin

Mussels as biological indicators of pollution

Group A Rotavirus in Sewage Samples from Barcelona and Cairo: Emergence of Unusual Genotypes

Advances in Laboratory Methods for Detection and Typing of Norovirus

Detection of enteroviruses in treated drinking water

The recovery and molecular identification of HAdV-D17 in raw sewage and mussel samples collected in the Eastern Cape Province of South Africa

Epidemiology of Classic and Novel Human Astrovirus: Gastroenteritis and Beyond. Viruses

Novel human astroviruses: Novel human diseases

Determining Persistence of Bocavirus DNA in the Respiratory Tract of Children by Pyrosequencing

Global, regional, and national life expectancy, all-cause mortality, and cause-specific mortality for 249 causes of death, 1980-2015: A systematic analysis for the Global Burden of Disease Study

Water and Wastewater Treatment in Africa -Current Practices and Challenges

A Systematised Review of the Health Impact of Urban Informal Settlements and Implications for Upgrading Interventions in South Africa, a Rapidly Urbanising Middle-Income Country

Enteroviruses: A Gut-Wrenching Game of Entry, Detection, and Evasion

Norovirus outbreaks linked to oyster consumption in the United Kingdom

United Nations Children's Fund (UNICEF) and World Health Organization

Astrovirus evolution and emergence

Detection and molecular characterization of norovirus from oysters implicated in outbreaks in the US

SARS-CoV-2 Titers in Wastewater are Higher Than Expected from Clinically Confirmed Cases. mySystems

The United Nations World Water Development

Isolation of Cytopathic Small Round Viruses with BS-C-1 Cells from Patients with Gastroenteritis

Application of a Reverse Transcription-PCR for Identification and Differentiation of Aichi Virus, a New Member of the Picornavirus Family Associated with Gastroenteritis in Humans

Aichi Virus Strains in Children with Gastroenteritis

Minimum Infective Dose of the Major Human Respiratory and Enteric Viruses Transmitted Through Food and the Environment

Epidemiological Characteristics of Sapovirus and Human Astrovirus Detected among Children in Nara Prefecture

Prolonged fecal excretion of hepatitis A virus in adult patients with hepatitis a as determined by polymerase chain reaction

Molecular characterization of enterovirus 71 and coxsackievirus A16 using the 5′ untranslated region and VP1 region

An Outbreak of Gastroenteritis Associated with GII

Influence of Environmental and Seasonal Factors on Microbial Contamination Levels in Clam Production Areas in Southern Tunisia: Escherichia coli, Salmonella spp., Hepatitis A Virus and Norovirus. Revue scientifique et technique (International Office of Epizootics)