Summary of Excreted and Waterborne Viruses


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December 6, 2017

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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.
https://doi.org/10.14321/waterpathogens.19

Acknowledgements: K.R.L. Young, Project Design editor; Website Design 
(http://www.agroknow.com)

Last published: December 6, 2017
Authors: 
Marta Rusiñol (University of Barcelona)Rosina Girones (University of Barcelona)

Summary

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 (10109 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.

1.0 TAXONOMIC CLASSIFICATION OF THE VIRAL AGENTS

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).

Table 1. Main viral waterborne pathogens

 

Family (genome, size)

Genus

Most important human pathogens

Related diseases

Adenoviridae (dsDNA, 70-90nm)

Mastadenovirus

Human adenovirus A-G (HAdV)

Gastroenteritis, respiratory disease, conjunctivitis, cystitis

Astroviridae (ssRNA, 28-41nm)

Mamastrovirus

Astrovirus 1-9 (HAstV)

Gastroenteritis, related to respiratory infections

Caliciviridae (ssRNA, 27-38nm)

Norovirus

Norovirus GI, GII (NoV)

Gastroenteritis

Sapovirus

Sapovirus GI, GII, GIV, GV (SaV)

Gastroenteritis

Hepeviridae (ssRNA, 25-30nm)

Orthohepevirus

Hepatitis E virus G1,2,3,4,7 (HEV)

Acute hepatitis

Picornaviridae (ssRNA, 24-30nm)

Enterovirus

Enterovirus A-D (EV-68 and EV-71), Rhinovirus A-C, Poliovirus 1-3, Coxsakievirus A-B

Paralysis, meningitis, hand-foot-and-mouth disease, heart anomalies, skin rush

Hepatovirus

Hepatitis A virus GI-III (HAV)

Acute hepatitis

Kobuvirus

Aichivirus A to C (AiV)

Gastroenteritis

Parechovirus

Parechovirus 1 to 16 (PeV)

Gastroenteritis, respiratory infections, encephalitis, meningitis, hepatitis

Reoviridae (dsRNA, 70-75nm)

Rotavirus

Rotavirus A to G (RoV)

Gastroenteritis

 

 

1.1 Viral pathogens of primary concern for waterborne diseases

1.1.2 Other groups containing new water-borne emerging viruses

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).

Table 2. Emerging viruses with potential for water-borne transmission

Family

(genome, size)

Genus

Human pathogens

Related diseases

Anelloviridae (ssDNA, 30-32nm)

Alphatorquevirus

Torquetenovirus (TTV)

Asymptomatic.
May be associated with various diseases: hepatitis, pulmonary diseases, hematologic disorders, myopathy and lupus.

Circoviridae (ssDNA, 15-20nm)

Cyclovirus

Human Associated Cyclovirus 1-11 (HuACyV)

Systemic infections, may play a role in development of paraplegia

Parvoviridae (ssDNA, 18-26nm)

Erythroparvovirus

Parvovirus B19 (PaV)

Fifth disease in children, arthropathy, hepatitis

Bocaparvovirus

Human bocavirus 1-4 (HBoV)

Gastroenteritis, related to respiratory infections

Protoparvovirus

Bufavirus (HBuV)

Gastroenteritis

Papillomaviridae (dsDNA, 50-60nm)

Alpha-papillomavirus

Human Papillomavirus 16, 18 (HPV)

Cervix, penis, anus and vulva cancers

Beta-papillomavirus

HPV 66

Related to genital warts

Picobirnaviridae (ssRNA, 33-41nm)

Picobirnavirus

Human picobirnavirus (HPBV)

May be implicated in gastroenteritis in humans

Polyomaviridae (dsDNA, 50-60nm)

Betapolyomavirus

Polyomavirus JC (PyV)

Progressive multifocal encephalopathy (PML)

 

BKPyV

Mild respiratory infection, polyomavirus-associated nephropathy polyomavirus-associated haemorrhagic cystitis

Alphapolyomavirus

Merkel cell PyV (MCPyV)

Associated to merkel cell carcinoma

 

1.2 EXCRETION OF VIRUSES

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.

Table 3. Summary of the excretion characteristics of main water-borne viral pathogens

Viral Pathogen

Excretion concentrations

Clinical characteristics

Prevalence in feces/urine

Reference

Adenovirus

E+07 to E+11 GC/g of stool

IP: 3 to 10 days

ID: 1 to 4 days

DE: 11 days (1 to 192)

2.6% to 16% in fecal gastroenteritis samples

Bozkurt et al., 2015; Lion et al., 2010; Rimoldi et al., 2011

Aichivirus

E+06 to E+12 GC/g of stool

IP: 12 to 54h

ID: 2 to 3 days

DE: Undetermined

0.8% in fecal gastroenteritis samples

Bozkurt et al., 2015; Drexler et al., 2011; Le Guyader et al., 2008

Astrovirus

E+08 to E+13 GC/g of stool

IP: 3,9 to 5,2 days

ID: 1 to 4 days

DE: 2 to 30 days

11% mean incidence of gastroenteritis worldwide, with 7% and 23% incidences in urban and rural areas

Bosch et al.,2013; Caballero et al., 2003; Desselberger and Gray, 1995; Lee et al., 2013

Bocavirus

E+04 GC/ml of fecal supernatant

IP: Undetermined

ID: 1 to 4 days

DE: weeks

1.3% in fecal gastroenteritis samples

Lau et al., 2007; Proenca-Modena et al., 2013; Rimoldi et al., 2011

Enterovirus

Coxsackievirus: E+03 to E+06 TCID50/g of stool

IP: 2 days

ID: 2 to 3 days

DE: 50 days (44 to 142)

22.1% coxsackievirus in fecal gastroenteritis samples

Bozkurt et al., 2015; Melnick and Rennick, 1980; Khetsuriani et al., 2009

Hepatitis A

E+07 GC/ml of fecal supernatant

IP: 7 to 50 days

ID: 3 to 6 months

DE: 8 days (4 to 42)

20% of clinical hepatitis

Arankalle et al., 2006; Lee, 2000

Hepatitis E

E+03 to E+07 GC/ml of fecal supernatant

IP: 2 to 10 weeks

ID: 2 to 6 weeks

DE: 22 days (14 to 33)

 

70% of fecal samples from hepatitis patients

Chandra et al., 2010.; Kim et al., 2014; Takahashi et al., 2007

Norovirus

E+07 to E+09 GC/gr of stool

IP: 1,1 to 1,2 days

ID: 12 to 60h

DE: 28 days (13 to 56)

16.2 to 42.8% in fecal gastroenteritis samples

Atmar et al., 2008; Bozkurt et al., 2015; Kaplan et al., 1982; Lee et al., 2013; Rimoldi et al., 2011

Polyomavirus

E+05 GC/ml urine

Reactivation in patients with immunosuppressive conditions

DE: Several months or years

62.7% of helthy adults and 13.2% of children excrete polyomaviruses in theurine, mostly JC virus (41.2%)

Bofill-Mas and Girones, 2001; Kling et al., 2012; Polo et al., 2004

Rotavirus

E+10 to E+12 GC/gr of stool

IP: 2 days

ID: 3 to 8 days

DE: 10 days (4 to 57)

33 to 38.2% in fecal gastroenteritis samples

Bozkurt et al., 2015; Desselberger and Gray, 1995; Ramani et al., 2014; Richardson et al., 1998; Rimoldi et al., 2011

Sapovirus

E+07 to E+08 GC/g of stool

IP: 1,7 days

ID: 1 to 4 days

DE: 4 days (4 to 21)

3.8% in fecal gastroenteritis samples

Bozkurt et al., 2015; Lee et al., 2013; Rimoldi et al., 2011; Rockx et al., 2002; Torner et al., 2016

IP: Incubation Period, ID: Illness duration, DE: days excretion

1.3 TRANSMISSION

1.3.1 Global routes of transmission for viral infections

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.

Table 4. Transmission routes of the principal waterborne viruses

Viral Pathogen

Transmission routes

Seasonality

Reference

Adenovirus

Fecal-oral: contaminated food, person-to-person, drinking water

Airborne: respiratory secretions

Bathing water

Without clear seasonality

Mena and Gerba, 2009; Vetter et al., 2015

Aichivirus

Fecal-oral: contaminated food, person-to-person, drinking water

Without clear seasonality

Kitajima and Gerba, 2015

Astrovirus

Fecal-oral: contaminated food, person-to-person, drinking water

Higher incidence in the cold-weather period

Bosch et al., 2014

Bocavirus

Fecal-oral: drinking water

Airborne: aerosol, respiratory secretions

Vertical transmission?

Higher prevalences in cold months

Hamza et al., 2009; Schildgen et al., 2008

Enterovirus

Fecal-oral: drinking water

Respiratory secretions

Higher prevalences in warm/wet seasons

Sedmak et al., 2005

Hepatitis A

Fecal-oral: contaminated food, person-to-person

No clear seasonality

Fares, 2015; Ouardani et al., 2016

Hepatitis E

Fecal-oral: contaminated food, drinking water

Foodborne: raw meat

Occurs more frequently in winter

 

Inoue et al., 2009; Kotwal and Cannon, 2014

Norovirus

Fecal-oral: contaminated food, person-to-person, drinking water

Higher prevalences in cold months

de Graaf et al., 2016

Polyomavirus

The route of intra-human transmission is still unknown

Without seasonal distribution

Fratini et al., 2014

Rotavirus

Fecal-oral: contaminated food, person-to-person, drinking water

 

 

Year-round infection in countries within 10 degrees of the equator, Winter peaks in all other regions of the world

Estes et al., 1983

Sapovirus

Fecal-oral: drinking water

 

Peak observed mainly in the cold season

Dey et al., 2012

1.3.2 Animal Reservoirs of viral infections in humans

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).

 

2.0 DATA ON OCCURRENCE OF VIRUSES IN WASTE WATER

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.

Table 5. Viral concentrations in wastewater effluents worldwide

Area

Viral Pathogen

Percent Positive

(# of samples)

Mean concentration

(GC/L)

Max concentration

(GC/L)

Reference

Asia

Norovirus GGII

36

2.51 E+06

NRa

Eftim et al., 2017

Bolivia

Rotavirus

NR

3.1 E+07

NR

Symonds et al., 2014

Brazil

Hepatitis A

25%

(6/22)

5.1 E+02

NR

Villar et al., 2007

Brazil

Polyomavirus

96%

(23/24)

4.6 E+05

3.2 E+05

Fumian et al., 2010

Brazil

Rotavirus

70.6%

(17/24)

NR

2.9 E+08

Prado et al., 2011

Canada

Adenovirus

100%

(16/16)

9.16 E+06

NR

Qiu et al., 2015

Enterovirus

100%

(16/16)

4.08 E+04

NR

Norovirus GGII

100%

(16/16)

1.2 E+06

NR

Sapovirus

12.5%

(2/16)

E+07

NR

Europe

Norovirus GGII

305

E+05

NR

Eftim et al., 2017

France

Astrovirus

82%

(14/17)

4.1 E+06

3.1 E+07

Le Cann et al., 2004

Germany

Adenovirus

100%

(13/13)

1.24 E+06

NR

Leifels et al., 2016

Enterovirus

92%

(12/13)

2.27 E+05

NR

Italy

Bocavirus

76%

(102/134)

4.7 E+04

E+05

Iaconelli et al., 2016

Japan

Adenovirus

100%

(72/72)

5.5 E+06

NR

Katayama et al., 2008

Japan

Astrovirus

36%

(10/28)

1.7 E+06

NR

Kobayashi et al., 2017

Hepatitis A

7%

(2/28)

9.7 E+02

1.8 E+03

Hepatitis E

11%

(3/28)

1.7 E+02

6.4 E+03

Japan

Enterovirus

65%

(47/72)

2.95 E+05

NR

Katayama et al., 2008

Norovirus GGI

94%

(68/72)

3.6 E+07 winter

2.39 E+04 summer

NR

Norovirus GGII

92%

(66/72)

3.9 E+07 winter

8.3 E+04 summer

NR

Japan

Sapovirus

100%

(12/12)

1.8 E+04

1.3 E+05

Haramoto et al., 2008

Japan

Polyomavirus

7%

(2/28)

2.7 E+02

7.2 E+02

Kobayashi et al., 2017

Nepal

Aichivirus

100%

(1/1)

NR

4.0 E+09

Haramoto and Kitajima, 2017

New Zealand

Enterovirus

100

(30)

NR

4.7 E+06

Hewitt et al., 2011

New Zealand

Norovirus GGII

13

6.31 E+03

NR

Eftim et al., 2017

North America

Norovirus GGII

107

5.01 E+04

NR

Eftim et al., 2017

Spain

Adenovirus

89%

(33/37)

8.38 E+05

2.9 E+07

Rusiñol et al., 2015

Polyomavirus

100%

(37/37)

7.47 E+05

1.7 E+07

Spain

Norovirus GGI

91%

(49/54)

NR

5.9 E+08

Pérez-Sautu et al., 2012

Norovirus GGII

98%

(53/54)

NR

3.4 E+09

Sweden

Adenovirus

100%

(7/7)

4.42 E+06

9.3 E+06

Hellmér et al., 2014

Switzerland

Hepatitis E

31%

(5/31)

7.81 E+04

NR

Masclaux et al., 2013

Uruguay

Astrovirus

45

(19/45)

NR

4.3 E+07

Victoria et al., 2014

USA

Adenovirus

100%

(48/48)

1.55 E+07

NR

Schmitz et al., 2016

USA

Aichivirus

100%

(11/11)

1.18 E+04

NR

Rachmadi et al., 2016

aNR: Not reported

Table 6. Viral concentrations in secondary effluents worldwide

Area

Viral Pathogen

Percent Positive

(# of samples)

Mean concentration

(GC/L)

Treatment

Reference

Brazil

Adenovirus

70%

(5/7)

3.78 E+03

CAS

Prado et al., 2011

 

Norovirus GGII

28.5%

(4/14)

2.4 E+06

CAS

Rotavirus

71%

(3/5)

1.9 E+04

CAS

Brazil

Polyomavirus

39%

(9/23)

4.3 E+04

CAS

Fumian et al., 2010

Canada

Adenovirus

100%

(16/16)

9.08 E+04

CAS

Qiu et al., 2015

France

Aichi virus

84%

(231/275)

1.55 E+03

CAS

Prevost et al., 2015

 

Astrovirus

84%

(231/275)

1.08 E+05

CAS

Enterovirus

64%

(175/275)

1.0 E+02

CAS

Norovirus GGI

98%

(270/275)

5.0 E+03

CAS

Rotavirus

84%

(231/275)

2.11 E+05

CAS

Germany

Enterovirus

46%

(6/13)

8.63 E+03

CAS

Leifels et al., 2016

Rotavirus

77%

(10/13)

1.3 E+04

CAS

Italy

Hepatitis A

14%

(3/21)

Undetermined

CAS

Iaconelli et al., 2015

Japan

Aichi virus

71%

(20/28)

5.5 E+02

DHS

Kobayashi et al., 2017

Astrovirus

32%

(9/28)

6.3 E+03

DHS

Enterovirus

21%

(6/28)

8.0 E+02

DHS

Hepatitis A

4%

(1/28)

1.5 E+03

DHS

Hepatitis E

0%

(0/28)

Non detected

DHS

Norovirus GGI

14%

(4/28)

6.5 E+01

DHS

Norovirus GGII

57%

(16/28)

7.2 E+01

DHS

Rotavirus

11%

(3/28)

4.3 E+02

DHS

Japan

Sapovirus

58%

(7/12)

1.5 E+02

CAS

Haramoto et al., 2008

Norway

Bocavirus

54%

(14/26)

2.72 E+04

CAS

Myrmel et al., 2015

Hepatitis E

8%

(2/26)

Undetermined

CAS

Norovirus GGI

100%

(26/26)

3.8 E+06

CAS

Singapore

Astrovirus

100%

(18/18)

3.9 E+04

CAS

Aw and Gin, 2010

Hepatitis A

28%

(5/18)

Undetermined

CAS

Spain

Adenovirus

78%

(25/32)

1.2 E+05

CAS

Rusiñol et al., 2015

Norovirus GGII

65%

(21/32)

5.05 E+05

CAS

Polyomavirus

59%

(19/32)

 

1.6 E+05

 

CAS

 

Sweden

Norovirus GGII

100%

(12/12)

1.0 E+05

CAS

Nordgren et al., 2009

United Kingdom

Adenovirus

10%

(5/48)

1.1 E+01

MBR

Purnell et al., 2016

 

Norovirus GGI

3%

(1/48)

1.1 E+01

MBR

Norovirus GGII

6%

(2/48)

1.1 E+01

MBR

CAS: conventional activated sludge; MBR: membrane bioreactor; DHS reactor: down-flow hanging sponge (DHS) reactor

Table 7. Viral concentrations in tertiary effluents worldwide

Area

Viral Pathogen

Percent Positive

(# of samples)

Mean concentration

(GC/L)

Treatment type

Reference

Brasil

Adenovirus

50%

(3/6)

2.88 E+03

Cl2

Prado et al., 2011

Hepatitis A

100%

(4/4)

2.8 E+04

Cl2

Rotavirus

66%

(3/4)

1.20 E+05

Cl2

Canada

Adenovirus

100%

(16/16)

8.71 E+04

UV

Qiu et al., 2015

Adenovirus

6%

(1/16)

1.86 E+04

UF and Cl2

Astrovirus

6%

(1/16)

3.54 E+03

UF and Cl2

Rotavirus

38%

(6/16)

7.94 E+02

UF and Cl2

Enterovirus

6%

(1/16)

7.41 E+02

UF and Cl2

Germany

Enterovirus

8%

(1/13)

6.0 E+03

UV

Leifels et al., 2016

Rotavirus

0%

(0/13)

Non detected

UV

Spain

Adenovirus

72%

(16/22)

1.9 E+03

Actiflo® and UV

Rusiñol et al., 2015

Hepatitis E

0%

(0/22)

Non detected

Actiflo® and UV

Norovirus GGII

54%

(12/22)

3.09 E+05

Actiflo® and UV

Polyomavirus

21%

(5/22)

4.67 E+02

Actiflo® and UV

USA

Adenovirus

13%

(3/23)

1.0 E+01

UV and Cl2

Francy et al., 2012

Enterovirus

0%

(0/23)

Non detected

UV and Cl2

Norovirus GGI

8%

(2/23)

1.0 E+01

UV and Cl2

UV: Ultraviolet, UF: Ultrafiltration, Cl2: Chlorination

References

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