Norovirus and other Caliciviruses


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September 7, 2017

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Citation:

Katayama, H. and Vinjé, J. 2017. Norovirus and other Calicivirus. 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) www.waterpathogens.org/book/norovirus-and-other-caliciviruses 
Michigan State University, E. Lansing, MI, UNESCO.

https://doi.org/10.14321/waterpathogens.14

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

Last published: September 7, 2017
Authors: 
Hiroyuki Katayama (The University of Tokyo)Jan Vinjé (Centers for Disease Control and Prevention)

Summary

Norovirus is ubiquitous, associated with 18% (95% CI: 1720%) of acute gastroenteritis (AGE) worldwide, with similar proportions of disease in high-, middle-, and low- income settings. Norovirus is estimated to cause approximately 200,000 deaths annually worldwide, with about 70,000100,000 among children in developing countries. In both high- and middle-income countries with mature rotavirus vaccination programs, norovirus is now also the most common cause of pediatric gastroenteritis requiring medical care. Norovirus is extremely contagious and humans are the only known reservoir for human norovirus. Transmission occurs via direct person-to-person, foodborne, waterborne or through environmental fomites.

Noroviruses are a group of non-enveloped, single-stranded RNA viruses with an icosahedral symmetry classified into the genus Norovirus of the family Caliciviridae. Other genera within this virus family include Sapovirus, which also causes AGE in humans. Infections in humans are caused by viruses of genogroup (G) I, II and IV for norovirus and by GI, II, IV and V for sapoviruses. Since human norovirus and sapovirus cannot be routinely grown in cell culture, detection of the virus relies on sensitive molecular methods such as real-time reverse transcription polymerase chain reaction. In the environment, norovirus can be found in any water that comes into contact with human stool samples which can also lead to contaminated crops (irrigation) and shellfish (growing waters).

Norovirus is highly resistant to environmental degradation in various water types and long-term infectivity has been reported for groundwater which when seeded with the prototype norovirus (GI.1 Norwalk virus) was infectious for at least 61 days. Norovirus contamination of drinking water can be controlled by adequate free chlorine disinfection practices with provision of proper pre-treatment processes before chlorination. Appropriate hand hygiene is likely the single most important method to prevent norovirus infection which is best accomplished through handwashing with water and soap. The use of chemical disinfectants such as sodium hypochlorite is one of the key approaches to disinfect norovirus from contaminated surfaces and drinking water. However, the effectiveness of most water and waste water treatments and disinfection methods on reduction of infectious norovirus can only be measured by the use of cultivable surrogate viruses such as murine norovirus and Tulane virus. An exciting new development is a vaccine against norovirus which is soon entering phase 3 clinical trials.

1.0 Epidemiology of the Disease and Pathogen(s)

1.1       Global Burden of Disease 

1.1.1    Global distribution

Although child deaths have declined in recent decades, but diarrheal disease remains the fourth most common cause of mortality and second most common cause of morbidity worldwide in children under the age of 5 years (Global Health Data Exchange. 2013; Available from: http://vizhub.healthdata.org/irank/arrow.php.). Based on a large systematic literature review of 175 studies, which describe over 185,000 cases of acute gastroenteritis, norovirus is associated with 18% (95% CI: 1720%) of all diarrheal disease worldwide (Ahmed et al., 2014). This percentage is higher among community cases (24%) than among outpatients (20%) or inpatients (17%), which is in line with the notion that norovirus is causing more often less severe clinical symptoms, albeit still an important cause of severe diarrheal disease.  As a fraction of all diarrheal diseases, norovirus is more frequently detected in developed countries (20%) and low-mortality developing countries (19%) than those with high-mortality (14%) (Ahmed et al., 2014). This lower prevalence in low-income settings likely indicates a more prominent role for other pathogens that are largely controlled through water and sanitation improvements in developed countries, not that norovirus incidence is lower in developing country settings. In the United States, noroviruses are estimated to be associated with 570800 deaths, 56,00071,000 hospitalizations and 400,000 emergency department visits annually (Hall et al., 2013). Global age-stratified estimates of illnesses and deaths ranks norovirus as the number 1 cause of foodborne illness and number 4 cause of foodborne deaths (Kirk et al., 2015). The global estimated cost of norovirus disease which includes both direct health system costs and productivity losses is 60 billion per year (Bartsch et al., 2016).

In children under the age of 5 years, an estimated 71,000 die as a result of norovirus gastroenteritis making it the third most common etiological cause of diarrheal mortality, after rotavirus and, possibly, enteropathogenic Escherichia coli (Lanata et al., 2013)However, for norovirus, which causes mild disease in the majority of cases, much of the burden is morbidity, not mortality. The sapoviruses, which initially were thought to only cause AGE in children, are now recognized to cause outbreaks in people of all age groups including the elderly (Lee et al., 2012).

1.1.2 Symptomology

Norovirus infection affects individuals of all ages, with the highest rates among young children (Ahmed et al., 2014). With a life expectancy of 80 years, this means that a person will experience an average of approximately three to eight norovirus illness episodes in their lifetime, of which at least one will occur by 5 years of age (Phillips et al., 2010). Noroviruses are the leading cause of outbreaks of acute gastroenteritis and in several countries that have introduced rotavirus vaccines, where they have become also the most frequent cause of sporadic gastroenteritis (Payne et al., 2013).

Norovirus as well as sapovirus gastroenteritis is characterized by acute onset, nonbloody diarrhea, (projectile) vomiting, nausea, and abdominal cramps. Some per­sons might experience only vomiting or diarrhea. Low-grade fever and body aches also might be associated with infection, and thus the term “stomach flu” often is used to describe the illness but there is no biological association with influenza. Although symptoms might be severe, they typically resolve without treatment after 1–3 days in otherwise healthy persons. However, more prolonged courses of illness lasting 4–6 days can occur, particularly among young children, elderly persons, and hospitalized patients. Worldwide, the WHO estimated that noroviruses annually cause 685 million cases of diarrhea (95% confidence interval [CI]: 491 million1.1 billion) and 212,489 deaths (95% CI: 160,595278,420), with ~85% of these illnesses and ~99% of the deaths occurring in developing countries (Pires et al., 2015)

1.2 Taxonomic classification of the agent(s)

1.2.1 Physical description of the agent

Norovirus and sapovirus are non-enveloped 3035 nm particles with an icosahedral symmetry that enclose a positive-sense single-stranded RNA genome of 7.17.7 kilobases in length. Most norovirus genomes contain 3 open reading frames (ORF) while the genome organization of sapoviruses differs and contains 2 ORFs. The ORF1 of noroviruses encodes a polyprotein that is post-translationally cleaved into seven non-structural mature proteins (NS1-7) that are involved in viral replication. ORF2 encodes the major structural protein (VP1) of approximately 60,000 D, and ORF3 encodes a minor structural protein (VP2). The ORF1 of sapoviruses encodes the non-structural proteins followed by the major capsid protein in the same reading frame. Viral capsids contains 90 dimers of VP1 and a few gene copies of VP2. X-ray crystallographic structure studies using Norwalk virus-like particles have revealed that the VP1 has a shell (S) and the protruding (P) domain (Prasad et al., 1999). The S domain surrounds the viral RNA and the P domain, which is linked to the S domain through a flexible hinge, corresponds to the C-terminal part of the VP1. The P domain is further divided into the P1 and the highly variable P2 subdomain which contains the putative neutralization sites and interacts with histoblood group antigens (HBGAs). VP2 is located interior to the virus particle and is most likely involved in virion stability (Lin et al., 2014).

1.2.2 Taxonomy

Previously, noroviruses were called Norwalk-like viruses or small-round structured viruses whereas sapoviruses were called Sapporo-like viruses or typical caliciviruses. In 2002, the International Committee on the Taxonomy of Viruses assigned Norwalk-like viruses to the species Norwalk virus, genus Norovirus and Sapporo-like viruses to the species Sapporo virus, genus Sapovirus in the family Caliciviridae (Mayo, 2002). Currently, the family Caliciviridae consists of five established genera, including Sapovirus, Norovirus, Lagovirus, Vesivirus, and Nebovirus (http://www.ictvonline.org/virusTaxonomy.asp), whereas five potentially new genera (Bavovirus, Nacovirus, Recovirus, and Valovirus) have been proposed.

Except for murine norovirus (GV) strains and the Cowden-1 porcine sapovirus (GIII) strain, norovirus and sapovirus cannot be routinely cultivated in vitro which prevents the classification of these viruses into distinct serotypes using neutralization. Therefore, classification is based on sequence-based typing into genogroups and to date at least 7 norovirus genogroups (GI-GVII) (Vinjé, 2015) and 7 sapovirus genogroups(Oka et al., 2015) are recognized. Viruses belonging to norovirus GI, GII and GIV infect humans where sapovirus GI, GII, GIV and GV have been reported to cause disease in humans. Each genogroup is further divided into genotypes: 9, 22, and 1 for norovirus GI, GII, and GIV and 7, 7, 1 and 2 for sapovirus GI, GII, GIV and GV, respectively.  

Despite the extensive genetic diversity among noroviruses, viruses from a single genotype, GII.4, are responsible for the majority of the norovirus outbreaks worldwide (Siebenga et al., 2009). Since the mid-1990s novel pandemic norovirus GII.4 variants have emerged every 23 years replacing previous predominant GII.4 strains. This process is likely driven by evasion of immunity in the human population. These global GII.4 variant strains include the GII.4 US95/96 strain in 1995, GII.4 Farmington Hills in 2002, GII.4 Hunter in 2004, GII.4 Den Haag in 2006, GII.4 New Orleans in 2009 and GII.4 Sydney in 2012. These new GII.4 variants are often, but not always, associated with an increase in the number of outbreaks (Leshem et al., 2013). In 2007, GIV sapoviruses were reported in several European countries suggesting a similar epidemic spread of a single genotype.

1.3 Transmission

Norovirus is extremely contagious and although several animal species have been described infected with norovirus, these viruses are genetically and antigenically diverse from the viruses that infect humans. Transmission of both norovirus and sapovirus occurs via fecal-oral and vomit-oral pathways by four general routes including direct person-to-person, foodborne, waterborne or through environmental fomites. The illness typically begins after an incubation period of 12–48 hours. Norovirus is shed primarily in the stool but also can be found in the vomitus of infected persons. Peak viral shedding occurs 2–5 days after infection, with a viral load of approximately 100 billion viral gene copies per gram of feces (Atmar, 2008). The level of noroviruses in the human feces in various settings are summarized in Table 1.

Table.1 Norovirus concentrations in feces

Area

Sample Type

Virus Genotype

Percent Positive

(# of samples)

Median

(GC/L)a

Minimum Concentration

(GC/L)

Maximum Concentration (GC/L)

Reference

Hong Kong

(China)

AGI patients

Norovirus GI

2.6%

(17/651)

8.40E+05

2.20E+04

3.00E+08

Chan et al., 2006

Hong Kong

(China)

AGI patients

Norovirus GII

7.1%

(46/651)

3.00E+08

2.50E+04

7.70E+10

Chan et al., 2006

Hong Kong

(China)

AGI short patients

Norovirus GII

62.2%

(25/40)

2.40E+08

7.76E+07

2.82E+09

Lee et al., 2007

Hong Kong

(China)

AGI long patients

Norovirus GII

37.8%

(15/40)

3.09E+10

6.92E+08

8.71E+10

Lee et al., 2007

Italy

AGI Infant patients

Norovirus GII

100%

(3/3)

NR

6.10E+03

1.40E+08

La Rosa et al., 2010

Japan

Feces from Health infants

Norovirus GII

12.7%

(17/134)

NR

NR

NR

Iwai et al., 2009

USA

Traveler ( >18) AGI patients

Norovirus GI

3.8%

(12/320)

1.73E+10

3.76E+07

1.18E+13

Ajami et al., 2010

USA

Traveler ( >18) AGI patients

Norovirus GII

5.6%

(18/320)

3.43E+07

3.26E+05

8.93E+09

Ajami et al., 2010

USA

Inoculum for Volunteer

Norovirus GI

100%

(1/1)

3.24E+08

NR

NR

Teunis et al., 2008

USA

Volunteer symptomatic

Norovirus GI

69%

(11/16)

2.50E+11

3.16E+09

1.58E+12

Atmar et al., 2008

USA

Volunteer asymptomatic

Norovirus GI

31%

(5/16)

1.20E+10

1.58E+09

5.01E+11

Atmar et al., 2008

NR: Not Reported; Method was Real-time PCR GC=gene copy calculated from copy/gram 

Although norovirus is highly contagious, not all individuals are susceptible to infection. This is dependent on the expression of histo blood group antigens (HBGAs) on gut epithelial surfaces where the virus is believed to attach to the human host (Marionneau et al., 2002). Persons carrying a functional fucosyltransferase 2 (encoded by FUT2 gene) are termed secretors and express HBGAs, whereas homozygous individuals with 428G>A nonsense mutations in the FUT2 gene, individual called non-secretors, are almost completely protected from GI.1 and GII.4 norovirus infections. However, polymorphisms in the FUT2 genes vary considerably depending on ethnicity and non-secretors can be infected by other norovirus genotypes (Jin et al., 2013).

1.4 Population and Individual Control Measures

1.4.1 Vaccines

Since human noroviruses do not replicate in cell culture, recombinant norovirus capsid proteins which can be expressed as virus like particles (VLPs), have been considered as potential antigens for norovirus vaccines. VLPs are morphologically and antigenically indistinguishable to native viruses, but lack genetic material, so are non-replicating. Early studies showed that VLPs can elicit a humoral and mucosal response in mice and humans by oral, intranasal or parenteral administration (Herbst-Kralovetz et al., 2010; Tacket et al., 2003). A number of norovirus vaccines are now under development, and all are based on expressed VLPs.

Noroviruses are genetically and antigenically diverse. Acquired immunity is of limited duration against homotypic strains, there is some degree of protection against viruses in the same genogroup, but there is little or no heterotypic protection across genogroups. Accordingly, a norovirus vaccine would likely need to be at least bivalent to protect against GI and GII viruses. So far, all vaccine trials have involved challenge with a genotype included in the vaccine. Recently, Lindesmith and colleagues analyzed sera from human volunteers who had been immunized with a bivalent norovirus vaccine containing GI.1 and GII.4 virus-like particles (VLPs)(Lindesmith et al., 2015) of which the GII.4 component is a consensus (GII.4C) based on major capsid protein sequences from three GII.4 variants (GII.4 Houston/2002, GII.4 Yerseke/2006a and GII.4 DenHaag/2006b). At day 7-post vaccination substantial rises of IgG and blockade Abs were observed against GI.1 and GII.4 and also against GI.3, GII.3 and GII.14 VLPs, suggesting broad and rapid antibody response. That GI.1 and GII.4 VLPs would elicit a response to other genotypes in humans was hardly a foregone conclusion given the extreme antigenic diversity of noroviruses. This observation is consistent with observations of humans infected during experimental GI.1 Norwalk virus studies who mounted not only histoblood group blocking antibody responses to homotypic GI.1 VLPs but also responses to other norovirus VLPs including GII.4 Sydney that had not yet circulated at the time of the infections (Czakó et al., 2015; Lindesmith et al., 2010).

The norovirus vaccine candidate furthest along in the development pipeline is a bivalent, intramuscular VLP vaccine which is being developed by Takeda Pharmaceuticals (Bernstein et al., 2015). This formulation has shown a degree of protection against severe gastroenteritis outcomes following GII.4 challenge. Efficacy clinical trials using the bivalent GI/GII.4 formulation are planned to start in military recruits, followed by trials in the elderly and infants. One of the challenges in developing norovirus vaccines is that so many distinct (or different) population subgroups are affected which complicates the formulation of a research agenda and clinical development plan. For example, vaccination protocols would be different for a target population of young children, who likely would require at least two shots, than it would for older adults for which one booster shot may be sufficient for protection, or for a specific risk group, such as healthcare workers.

1.4.2 Hygiene measures

The main approaches to preventing and containing norovirus infections include implementing policies surrounding hand hygiene, patient isolation (separation of symptomatic patients) and cohorting (grouping of patients based on symptoms), staff exclusion from work, visitor restrictions, enhanced environmental cleaning and disinfection, and ward closures (Barclay et al., 2014). In general, hand hygiene adherence should be actively promoted among healthcare personnel, patients and visitors in patient-care areas affected by outbreaks of norovirus gastroenteritis. During outbreaks, hands should be washed with soap and running water for a minimum of 20 s after providing care for patients with suspected or confirmed infection (MacCannell et al., 2011; CDC et al., 2011). Despite widespread use, there is inconclusive evidence for the effectiveness of alcohol-based hand sanitizers for norovirus (Park et al., 2010; Macinga et al., 2008; Sickbert-Bennett et al., 2005). Therefore, during outbreaks, they should be used as an adjunct to hand-washing (Hall et al., 2011). Since aerosolization of noroviruses and close, direct contact with an infected individual contribute to the high risk of transmission (Phillips, 2011), the use of appropriate personal protective equipment, i.e., gloves and masks, when cleaning up vomit, is another measure to limit further spread of norovirus infection to staff in healthcare facilities (MacCannell et al., 2011).

 

2.0 Environmental Occurrence, Persistence and Survival

2.1 Detection methods

Because no robust cell culture system for norovirus or sapovirus currently exist, methods to detect these viruses are based on detection of viral RNA primarily using polymerase chain reaction (PCR). Since the initial description of PCR (Saiki et al., 1985), reverse transcription (RT)-PCR and, more recently, real-time RT-PCR (RT-qPCR) methods have become the gold standard for detection of norovirus in both clinical and environmental samples. Various combinations of oligonucleotide primers and probes for the sensitive detection of norovirus in food and water have been reported (Kageyama et al., 2003Stals et al., 2012; Vinjé, 2015). Standardized method have been developed for detecting both of these viruses (TAG 4 of CEN/TC 275/WG 6) and have been approved (CEN ISO/TS 15216-parts 1 & 2)(Hennechart-Collette et al., 2015; Standardization, 2013a, 2013b).

2.2 Data on occurrence

2.2.1 Sewage and sludge

In temperate climates, norovirus and sapovirus occurrence is quite seasonal with most infections during the winter months (Katayama et al., 2008). After development of PCR-based detection methods for norovirus and sapovirus, many papers have been published on the presence of these viruses in sewer systems from different regions of the world. The concentration of enteric viruses in the wastewater influent fluctuates dependent on timing of sampling. The occurrence data are summarized in Table 2. Here, the maximum concentration in the raw sewage reported is focused since it is important from a risk management perspective whereas lower virus concentrations reported may be the result of RT-PCR inhibition and/or low recovery of viruses during concentration. Maximum concentration of norovirus GI ranged from 105.4 gene copies /L  (Haramoto, 2006) to 106.7 gene copies /L (Katayama, 2008) with one paper reporting even 109 gene copies /L (Da Silva, 2007). Maximum concentration of norovirus GII ranged from 105.6 gene copies /L (Kitajima, 2014) to 108.6 gene copies /L (Simmons, 2011). Concentration of sapovirus (GI, GII, GIV and GV) ranged generally from 103 to 104 (Kitajima, 2011), but is more fluctuated, some  reporting  108,3 gene copies /L (Sano, 2011). In general, the concentration of sapoviruses is less than noroviruses (Iwai, 2009).

Table. 2 Calicivirus concentrations in raw sewage

Area

Virus

Genotype

Percent Positive

(# of samples)

Concentrations

Average

GC/La

(Range)

Reference

France

Norovirus GI

43%

(34/79)

(1.00E+09 Max)

da Silva et al., 2007

France

Norovirus GII

88%

(71/81)

(6.00E+07 Max)

da Silva et al., 2007

Ireland

Norovirus GII

95%

(21/22)

7.40E+04

Flannery et al., 2013

Italy

Noroviruses GI

100%

(6/6)

(6.46E+05 to 5.73E+07)

La Rosa et al., 2010

Italy

Noroviruses GII

100%

(12/12)

(6.80E+05 to 6.77E+07)

La Rosa et al., 2010

Italy

Norovirus

72%

(17/23)

in both rainy and dry

6.76E+05

(SDb±7.41E+02)c

Carducci and Verani, 2013

Italy

Norovirus

72%

(17/23)

in both rainy and dry

8.32E+05d

(SD ±7.24E+02)

Carducci and Verani, 2013

Japan

Norovirus GI

100%

(12/12)

(1.70E+02 to 2.60E+05

Haramoto et al., 2006

Japan

Norovirus GII

100%

(12/12)

(2.40E+03 to 1.90E+06)

Haramoto et al., 2006

Japan

Sapovirus

100%

(12/12)

(2.80E+03 to 1.30E+05)

Haramoto et al., 2008b

Japan

Norovirus GI

96%

(23/24)

(2.30E+06 Max)

Iwai et al., 2009

Japan

Norovirus GII

100%

(24/24)

 

(7.10E+07 Max)

Iwai et al., 2009

Japan

Norovirus GI

100%

(24/24)

4.90E+03e

(SD ±0.55)

Katayama et al., 2008

Japan

Norovirus GI

100%

(30/30)

1.90E+05f

(SD ±0.57 )

Katayama et al., 2008

Japan

Norovirus GII

100%

(24/24)

9.10E+03e

(SD ±0.56)

Katayama et al., 2008

Japan

Norovirus GII

100%

(30/30)

2.00E+05f

(SD ±0.63)

Katayama et al., 2008

Japan

Norovirus GIV

50%

(6/12)

(6.90E+04 Max)

Kitajima et al., 2009

Japan

Sapovirus

100%

(12/12)

1.80E+04

(SD ±0.47)

(9.30E+04 Max)

Kitajima et al., 2011

Japan

Norovirus GI

100%

(12/12)

(1.50E+06 Max)

Kitajima et al., 2012

Japan

Norovirus GII

100%

(12/12)

(9.10E+05 Max)

Kitajima et al., 2012

Japan

Norovirus GII

95%

(15/16)

1.20E+06

Miura et al., 2015

Japan

Sapovirus

68%

(11/16)

2.70E+04

Miura et al., 2015

Netherlands

Noroviruses

100%

(58/58)

(5.10E+03 to 8.50E+05)

Lodder and Husman, 2005

New Zealand

Norovirus GI

82%

(9/11)

1.26E+03

(SD ±1.1)

Wolf et al., 2010

New Zealand

Norovirus GII

82%

(9/11)

2.50E+04

(SD ±1.0)

Wolf et al., 2010

Spain

Norovirus GI

91%

(49/54)

(5.90E+08 Max)

Pérez-Sautu et al., 2012

Spain

Norovirus GII

98%

(53/54)

(3.40E+09 Max)

Pérez-Sautu et al., 2012

Spain

Sapovirus

 

(1.80E+08 Max)

Sano et al., 2011

Sweden

Norovirus GI

100%

(12/12)

(1.10E+04 to 2.20E+06)

Nordgren et al., 2009

Sweden

Norovirus GII

100%

(12/12)

(9.40E+06 Max)

Nordgren et al., 2009

Sweden

Noroviruses

36%

(8/22)

3.00E+02

(SD ±0.6)

(4.50E+03 Max)

Ottoson et al., 2006

Switzerland

Norovirus GII

97%

(58/60)

2.68E+05

Masclaux, 2013

Uruguay

Norovirus GII

51%

(49/96)

9.40E+05

Victoria, 2014

USA

Norovirus GII

100%

(8/8)

5.00E+07

(1.30E+05 to 4.00E+08)

Simmons et al., 2011

USA

Norovirus GII

75%

(6/8)

3.20E+05g

Simmons et al., 2011

a GC gene copies;  b SD standard deviation  c collected during the rainy season;   d collected duiring dry season r; e collected in summer; f collected in winter; g post preliminary treatment primary sewage

Detection of enteric viruses in sludge samples can be quite challenging as methods that have been optimized using spiking of viruses into the sludge do not always reflect the fate of indigenous virus originally present. The concentration of norovirus GII in sludge samples in membrane bioreactor were much lower than other enteric viruses that were detected (Simmons et al., 2011). Similar trends was also observed in a report from Japan where sapovirus was more abundant than norovirus in sludge samples (Miura, 2015).

A survey of air samples in a wastewater treatment plant in Denmark showed that norovirus GI was more frequently detected than norovirus GII (Uhrbrand 2011).

2.2.2 Surface waters

Surface waters, often receiving treated and in some occasion untreated wastewater, are also containing enteric viruses. Norovirus GI and GII in treated wastewater are usually less than 105 gene copies /L (Table 3) (Miura et al., 2015; Katayama et al., 2008), but sometimes reach 106.8 gene copies /L (Da Silva et al., 2007) and 106.7 gene copies /L(Nordgren et al., 2009). Sapovirus concentration in treated wastewater is not well documented, but reported to reach 103.9 gene copies /L (Table 3) (Kitajima et al., 2011).

Table. 3 Calicivirus concentrations in treated wastewater

Area

Virus

Genotype

Percent Positive

(# of Samples)

Concentrations

Average

GC/La

(Range)

Reference

Brazil

Norovirus GI

NR

2.97E+02

(2.06E+02 to 4.29E+02)

Victoria, 2010

Brazil

Norovirus GII

NR

4.40E+02

(1.80E+02 to 1.09E+03)

Victoria, 2010

France

Norovirus GI

24%

(18/75)

(6.00E+06 Max)

da Silva et al., 2007

France

Norovirus GII

14%

(11/71)

(3.00E+06 Max)

da Silva et al., 2007

Ireland

Norovirus GII

22

2.90E+04

Flannery et al., 2013

Italy

Norovirus

65%

(15/23) in both rainy and dry

6.31E+05

(SDb ±5.62E+02)

Carducci and Verani, 2013

Italy

Norovirus

65%

(15/23) in both rainy and dry

1.10E+06

(SD ±8.71E+02)

Carducci and Verani, 2013

Japan

Norovirus GI

100%

(12/12)

(7.70E+02 Max)

Haramoto et al., 2006

Japan

Norovirus GII

83%

(10/12)

(1.50E+03 Max)

Haramoto et al., 2006

Japan

Sapovirus

58%

(7/12)

(5.30E+02 Max)

Haramoto et al., 2008b

Japan

Norovirus GI

94%

(68/72)

1.40E+03

(SD ±7.8)

(2.90E+04 Max)

Katayama et al., 2008

Japan

Norovirus GII

92%

(66/72)

8.10E+02

(SD 6.0)

(5.50E+04 Max)

 

Katayama et al., 2008

Japan

Norovirus GIV

25%

(4/12)

(4.80E+03 Max)

Kitajima et al., 2009

Japan

Sapovirus

42%

(5/12)

4.30E+03

(SD ±1.6)

(8.10E+03 Max)

Kitajima et al., 2011

Japan

Norovirus GI

50%

(6/12)

(5.60E+03 Max)

Kitajima et al., 2012

Japan

Norovirus GII

50%

(6/12)

(3.80E+03 Max)

Kitajima et al., 2012

Japan

Norovirus GII

26%

(4/16)

(4.50E+04 to 1.10E+05)

Miura et al., 2015

Japan

Sapovirus

0%

(0/16)

NR

Miura et al., 2015

Netherlands

Noroviruses

100%

(5/5)

(9.00E+02 to 7.50E+03)

Lodder and Husman, 2005

Spain

Norovirus GI

94%

(17/18)

NR

Pérez-Sautu et al., 2012

Spain

Norovirus GII

100%

(18/18)

NR

Pérez-Sautu et al., 2012

Sweden

Norovirus GI

100%

(12/12)

(7.90E+05 Max)

Nordgren et al., 2009

Sweden

Norovirus GII

100%

(12/12)

(5.00E+06 Max)

Nordgren et al., 2009

Sweden

Noroviruses

18%

(4/22)

3.40E+01

(SD ±1.7)

(1.50E+02 Max)

Ottoson et al., 2006

US

Norovirus GII

0%

(0/8)

NR

Simmons et al., 2011

a GC gene copies; b SD Standard deviation; NR: Not reported



Norovirus occurrence data are summarized in Table 4. Noroviruses can also be detected in river water samples, and tend to show higher concentration during rain events probably due to sewer overflow (Hata, 2014). Noroviruses GI and GII in river water may reach 103104 gene copies /L (Haramoto, 2005), but rarely reach 105 gene copies /L (Lodder, 2005; Haramoto, 2012a, 2012b). Sapoviruses are less frequently found in river water samples used as source water for water supply in Japan (Haramoto, 2012a, 2012b), and concentration up to 105 gene copies /L have been reported (Sano et al., 2011). Many different sapovirus and norovirus genotypes have been detected in river water samples (Kitajima, 2010a; Kitajima, 2010b) and have a worldwide distribution including developing country such as Kenya (Kiulia, 2010).

Table. 4 Calicivirus concentrations in environmental waters

Area

Sample Type

Virus

Percent Positive

(# of Samples)

Concentrations

Average

GC/La

Mean (Range)

Reference

Brazil

Surface water

Norovirus GI

NRb

(1.71E+02 to 8.14E+03)

Victoria et al., 2010

Brazil

Surface water

Norovirus GII

NR

(1.14E+02 to 3.72E+03)

Victoria et al., 2010

Egypt

Surface water

Norovirus GI

<32%

(144)

5.30E+02

(SD ±2.40E+02)

El-Senousy et al., 2013

Egypt

Surface water

Norovirus GII

<32%

(144)

3.30E+02

(SD ±4.30E+02)

El-Senousy et al., 2013

Germany

Surface water

Norovirus GII

32%

(13/41)

(9.40E+00 to 2.70E+04)

Hamza et al., 2009

Hong Kong

Seawater

Norovirus GI

67%

(4/6)

(3.90E+02 to 2.28E+03)

Yang et al., 2012

Hong Kong

Seawater

Norovirus GII

100%

(6/6)

(5.30E+02 to 3.68E+03)

Yang et al., 2012

Italy

Seawater

Norovirus GII

12%

(3/26)

(7.60E+00 to 2.40E+02)

La Rosa et al., 2007; La Rosa et al., 2009

Japan

Surface water

Norovirus GI

53%

(34/64)

8.70E+01

(1.60E+03 Max)

Haramoto et al., 2005

Japan

Surface water

Norovirus GII

44%

(29/64)

6.10E+02

(7.00E+03 Max)

Haramoto et al., 2005

Japan

Surface water

Sapovirus

64%

(22/36)

(1.00E+02 Max)

Haramoto et al., 2008b

Japan

Surface water

Norovirus GI

13%

(8/64)

(2.70E+02 to 3.30E+04)

Haramoto et al., 2012

Japan

Surface water

Norovirus GII

1%

(1/64)

3.40E+02

(3.40E+02 Max)

Haramoto et al., 2012

Japan

Surface water

Sapovirus

3%

(2/64)

(4.60E+02 to 8.20E+02)

Haramoto et al., 2012

Japan

Surface water

Norovirus GIV

31%

(15/48)

(1.60E+02 to

1.50E+04)

Kitajima et al., 2009

Korea

Groundwater

Norovirus GI

0.18%

(2/1090)

NR

Lee et al., 2013

Korea

Groundwater

Norovirus GII

0.55%

(6/1090)

NR

Lee et al., 2013

Netherlands

Surface water

Noroviruses

100%

(8/8)

(4.00E+00 to 4.90E+03)

Lodder and Husman, 2005

New Zealand

Surface water

Norovirus GII

17%

(1/6)

2.00E+02

Wolf et al., 2010

Singapore

Surface water

Norovirus GI

20%

(20/93)

7.00E+00

(SD ±9.9E+01)

(2.16E+03 Max)

Liang et al., 2015

Singapore

Surface water

Norovirus GII

48%

(45/93)

1.04E+02

(SD ±2.5E+03)

(1.55E+04 Max)

Liang et al., 2015

Singapore

Surface water

Norovirus GI

25%

(16/65)

9.50E+01

Rezaeinejad et al., 2014

Singapore

Surface water

Norovirus GII

48%

(31/65)

3.70E+02

Rezaeinejad et al., 2014

Thailand

Surface water

Norovirus GII

13%

(3/24)

(2.80E-01 to 7.90E+02)

Hata et al., 2011

US

Seawater

Norovirus GI

7%

(5/72)

(1.40E+09 Max)

Gentry et al., 2009

US

Seawater

Norovirus GII

1%

(1/72)

(1.10E+02 Max)

Gentry et al., 2009

US

Groundwater

Norovirus GI

4%

(48/1204)

6.00E-01

(1.16E+02 Max)

Borchardt et al., 2012

a GC gene copy; NR: Not Reported

Both GI and GII noroviruses were detected in 32% of irrigation water samples (10 L) collected in Egypt. A study on fresh produce such as lettuce showed only GI norovirus and no norovirus GII (El-Senousy 2013), which may indicate that norovirus GI is more persistent on the surface of fresh produce. More data on the occurrence of norovirus and sapovirus is needed from developing countries in particular in countries where irrigation using untreated wastewater is a common practice.

2.2.3 Groundwater and drinking water

Noroviruses and sapoviruses have been detected in groundwater (Table 4). For example, in 500 L ground water samples used for food-catering facilities in Korea norovirus was positive in only 0.64% tested (Lee et al., 2013), which is less than nationwide groundwater survey in Korea showing 8.7% positive (Lee et al., 2012). Also in a study from the US, 4% of groundwater samples used for tap water contained norovirus genomes with concentrations as high as 116 gene copies /L of norovirus GI (Borchardt, 2012).

Limited data are available on the presence of noroviruses in drinking water. A study in Japan found that 4% and 7% was positive for norovirus GI and GII respectively under the effort using whole concentrates onto RT-PCR detection from 100532 liters of tap water. However, most of these samples contained more than 0.5 mg/L of chlorine and therefore the detected norovirus was most likely not infectious. In a report from Spain, no norovirus was detected in tap water (Pérez-Sautu 2012). Waterborne norovirus outbreaks are reported and they can often be linked to a sewage-contaminated drinking water (Bitler et al., 2013)

2.2.4 Seawater and shellfish

Coastal seawaters are affected strongly by treated/untreated urban sewer discharge and also by combined sewer overflow during rain events. The concentration of norovirus in seawater varies greatly ranging from 102 to 103 gene copies / L in Brazil  (Victoria, 2010), whereas a coastal water sample in a study in the US contained 109 gene copies /L (Gentry, 2009). Oysters in England and Wales from cold waters (<5°C) had significantly higher norovirus content than those from warmer waters (>10°C), which may be due to the seasonal prevalence of the virus in the community or linked with oyster metabolic function (Campos et al., 2017).

Approximately 9% of the shellfish samples sold in the markets in France tested positive for norovirus (Schaeffer, 2013), whereas up to 90% of the oysters from harvesting areas in the United Kingdom tested positive with a higher positive ratio in the winter than in summer (Lowther, 2012). Those differences suggest that timing of harvesting and depuration of the oyster is important before the oysters are sold commercially. Ueki et al described the detection of the same norovirus genotype in patients, oysters, and from samples collected at the wastewater treatment plants (Ueki, 2005). Since noroviruses bound to oyster digestive tissues (Le Guyader et al., 2006) and norovirus genomes were not bioaccumulated (Dancer, 2010), detected genomes from oysters are likely to be originated from intact virus particles.

 In shellfish from Morocco, sapoviruses were less frequently found than noroviruses but at higher levels than other enteric viruses (Benabbes, 2013).

2.3 Persistence

Limited data are available on the persistence and survival of noroviruses and sapoviruses except for a few human challenge studies. Several cultivable surrogate viruses including murine norovirus and Tulane virus are often used for persistence studies, whereas feline calicivirus had been used but is less reliable due to its vulnerability to acid and base condition (Cannon et al., 2006). Norovirus GII and MNV showed long persistence (T90 > 21 days at 25ºC or cooler) in urine, in wastewater or in biofilms (Table 5). Published persistence and survival data show days of survival on the surface based on the surrogate study using murine norovirus, much longer persistency based on the RT-qPCR detection, and extremely long (>1,000 days) persistence under suitable condition such as in groundwater(Tables 6, 7, and 8).

Table. 5 Persistence of Calicivirus in urine, wastewater and biofilms

Area

Virus

T90

(Days)a

Temperature

˚C

Sample Type

Reference

Burkina Faso

MNVa

42

15

Urine

Makaya et al., 2015

Burkina Faso MNV

21

25

Urine Makaya et al., 2015
Burkina Faso MNV

3.5

42

Urine Makaya et al., 2015

Luxembourg

Norovirus GIIa

>49

4

Wastewater

Skraber et al., 2009

Luxembourg Norovirus GII

21

20

Wastewater

Skraber et al., 2009
Luxembourg Norovirus GII

>49

4

Biofilm

Skraber et al., 2009
Luxembourg Norovirus GII

>49

20

Biofilm Skraber et al., 2009

a Based on RT-qPCR

Table. 6 Persistence of Caliciviruses in PBS and Ground water

Area

Sample Type

Virus

T90

(Days)

Temperature

˚C

Reference

Burkina Faso

PBS

MNVa,b

28

15

Makaya et al., 2015

Burkina Faso PBS MNVa,b

12

25

Makaya et al., 2015
Burkina Faso PBS MNVa,b

42c

42

Makaya et al., 2015

USA

Groundwater

Norovirus GI Norwalkc

1151

RTd

Seitz et al., 2011

USA Groundwater Norovirus GI Norwalkc

707

RT

Seitz et al., 2011
USA

PBS

Norovirus GI Norwalke

120

4

Liu et al., 2012

USA PBS Norovirus GI Norwalke

35

RT

Liu et al., 2012
USA PBS Norovirus GI Norwalke

5.5

37

Liu et al., 2012

a MNV Murine Norovirus; b Plaque assay; c Real-time PCR; d RT:  Room temperature; e Rnase RT-qPCR

Table. 7 Persistence of Calicivirus in foods

Area

Virus

T90

(Days)

Temperature

˚C

Method

Matrix

Reference

Korea

 

MNVa

 

8.18

10

Cell culture
 

Soy source 5% NaCl

Park and Ha, 2015

Korea MNV

4.68

10 Cell culture

Soy source 10% NaCl

Park and Ha, 2015
Korea MNV

3.39

10 Cell culture

Soy source 15% NaCl

Park and Ha, 2015
Korea MNV

2.96

10 Cell culture

Soy source 20% NaCl

Park and Ha, 2015

Netherlands

MNV

7

10

Cell culture

Strawberry

Verhaelen et al., 2012

Netherlands MNV

3

21

Cell culture

Raspberry

Verhaelen et al., 2012
Netherlands

MNV

3

21

Real-time PCR

Strawberry

Verhaelen et al., 2012
Netherlands MNV

1

21

Cell culture

Strawberry Verhaelen et al., 2012
Netherlands

Norovirus GI.4

2

21

Real-time PCR

Strawberry Verhaelen et al., 2012

USA

Norovirus GI Norwalk

16.6

4

Real-time PCR

Lettuce

Escudero et al., 2012

USA Norovirus GI Norwalk

9

22

Real-time PCR

Lettuce Escudero et al., 2012
USA

Norovirus GII Snow Mountain

25

4

Real-time PCR

Lettuce Escudero et al., 2012
USA

Norovirus GII Snow Mountain

16.6

22

Real-time PCR

Lettuce Escudero et al., 2012
USA

MNV

107

RTb

Real-time PCR

Lettuce Escudero et al., 2012
USA MNV

333

4

Real-time PCR

Lettuce Escudero et al., 2012
USA MNV

4.5

RT

Plaque assay

Lettuce + Artificial feces

Escudero et al., 2012
USA MNV

11

4

Plaque assay

Lettuce + Artificial feces Escudero et al., 2012

USA

MNV

4.84

18

Plaque assay

Spinach semi-savoy whole

Hirneisen and Kniel, 2013

USA MNV

2.55

18

Plaque assay

Spinach semi-savoy, adaxial

Hirneisen and Kniel, 2013
USA MNV

3.77

18

Plaque assay

Spinach semi-savoy, adaxial

Hirneisen and Kniel, 2013
USA MNV

2.5

18

Plaque assay

Spinach smooth, whole

Hirneisen and Kniel, 2013
USA MNV

1.94

18

Plaque assay

Spinach smooth, adaxial

Hirneisen and Kniel, 2013
USA MNV

2.71

18

Plaque assay

Spinach smooth, adaxial Hirneisen and Kniel, 2013
USA

Tulane Virus

5.73

18

Plaque assay

Spinach semi-savoy whole

Hirneisen and Kniel, 2013
USA Tulane Virus

2.61

18

Plaque assay

Spinach semi-savoy, adaxial

Hirneisen and Kniel, 2013
USA Tulane Virus

4.38

18

Plaque assay

Spinach semi-savoy, adaxial

Hirneisen and Kniel, 2013
USA Tulane Virus

3.07

18

Plaque assay

Spinach smooth, whole

Hirneisen and Kniel, 2013
USA Tulane Virus

2.25

18

Plaque assay

Spinach smooth, adaxial

Hirneisen and Kniel, 2013
USA Tulane Virus

2.24

18

Plaque assay

Spinach smooth, adaxial Hirneisen and Kniel, 2013

a MNV murine norovirus;  b RT: Room Temperature

Table. 8 Persistence of Calicivirus on fomites

Area

Virus

T90

(Days)

Temperature

˚C

Sample Type

Reference

France

MNVa,b

4.3

9

Glass, humidity 10%

Noue et al., 2014

France MNVa,b

3.3

9

Glass, humidity 35%

Noue et al., 2014
France MNVa,b

1.4

9

Glass, humidity 55%

Noue et al., 2014
France MNVa,b

3.4

9

Glass, humidity 85%

Noue et al., 2014
France MNVa,b

3.7

9

Glass, humidity 100%

Noue et al., 2014
France MNVa,b

2.8

25

Glass, humidity 10%

Noue et al., 2014
France MNVa,b

1

25

Glass, humidity 35%

Noue et al., 2014
France MNVa,b

<0.42

25

Glass, humidity 55%

Noue et al., 2014
France MNVa,b

<0.42

25

Glass, humidity 85%

Noue et al., 2014
France MNVa,b

0.58

25

Glass, humidity 100%

Noue et al., 2014

Korea

MNVb

4.8

15

Wood, 30% humidity

Kim et al., 2012

Korea MNVb

7.2

15

Wood, 50% humidity

Kim et al., 2012
Korea MNVb

6.6

15

Wood, 70% humidity

Kim et al., 2012
Korea MNVb

10.2

25

Wood, 30% humidity

Kim et al., 2012
Korea MNVb

7.2

25

Wood, 50% humidity

Kim et al., 2012
Korea MNVb

2.4

25

Wood, 70% humidity

Kim et al., 2012
Korea MNVb

3.2

32

Wood, 30% humidity

Kim et al., 2012
Korea MNVb

0.48

32

Wood, 50% humidity

Kim et al., 2012
Korea MNVb

1.6

32

Wood, 70% humidity

Kim et al., 2012
Korea MNVb

1.12

40

Wood, 30% humidity

Kim et al., 2012
Korea MNVb

0.48

40

Wood, 50% humidity

Kim et al., 2012
Korea MNVb

0.08

40

Wood, 70% humidity

Kim et al., 2012

Korea

MNVb

0.54

15

Steel, 30% humidity

Kim et al., 2012

Korea MNVb

0.6

15

Steel, 50% humidity

Kim et al., 2012
Korea MNVb

0.6

15

Steel, 70% humidity

Kim et al., 2012
Korea MNVb

3.2

25

Steel, 30% humidity

Kim et al., 2012
Korea MNVb

1.26

25

Steel, 50% humidity

Kim et al., 2012
Korea MNVb

0.22

25

Steel, 70% humidity

Kim et al., 2012
Korea MNVb

0.08

32

Steel, 30% humidity

Kim et al., 2012
Korea MNVb

0.06

32

Steel, 50% humidity

Kim et al., 2012
Korea MNVb

0.12

32

Steel, 70% humidity

Kim et al., 2012
Korea MNVb

0.07

40

Steel, 30% humidity

Kim et al., 2012
Korea MNVb

0.07

40

Steel, 50% humidity

Kim et al., 2012
Korea MNVb

0.08

40

Steel, 70% humidity

Kim et al., 2012

Korea

MNVb,c

11

RTe

Ceramic

Kim et al., 2014

Korea MNVb,c

20.5

RT

Wood

Kim et al., 2014
Korea MNVb,c

7.23

RT

Rubber

Kim et al., 2014
Korea MNVb,c

4.05

RT

Glass

Kim et al., 2014
Korea MNVb,c

3.82

RT

Stainless steel

Kim et al., 2014
Korea MNVb,c

5.74

RT

Plastic

Kim et al., 2014

USAb

Norovirus GI Norwalk

9.1

4

Stainless steel

Liu et al, 2012

USAb Norovirus GI Norwalk

3.4

37

Stainless steel Liu et al, 2012
USAb Norovirus GI Norwalk

4.8

RT

Stainless steel Liu et al, 2012

USA

Norovirus GI Norwalkd

28.5

RT

Formica

Escudero et al., 2012

USA Norovirus GI Norwalkd

31.3

RT

Stainless steel

Escudero et al., 2012
USA Norovirus GI Norwalkd

34.4

RT

Ceramic Tile

Escudero et al., 2012
USA

Norovirus GII Snow Mountaind

33.3

RT

Formica

Escudero et al., 2012
USA Norovirus GII Snow Mountaind

33.3

RT

ceramic tile

Escudero et al., 2012
USA Norovirus GII Snow Mountaind

43.4

RT

Stainless steel

Escudero et al., 2012
USA

MNVa

2.3

RT

Formica

Escudero et al., 2012
USA MNVa

4

RT

Ceramic tile

Escudero et al., 2012
USA MNVa

4.3

RT

Stainless steel

Escudero et al., 2012
USA MNVa

5.2

RT

Ceramic tile + Artificial feces

Escudero et al., 2012
USA MNVa

5.8

RT

Stainless steel+artificial feces

Escudero et al., 2012
USA MNVa

5.8

RT

Formica + Artificial feces

Escudero et al., 2012
USA

MNVd

50

RT

Ceramic tile

Escudero et al., 2012
USA MNVd

62.5

RT

Stainless steel

Escudero et al., 2012
USA MNVd

83

RT

Formica

Escudero et al., 2012

 a Murine Norovirus; bPlaque assay; c use of the Weibull model;  d Real-time PCR; e RT: Room Temperature

Survival of noroviruses have been studied using human volunteers as a read-out. In one study groundwater was seeded with Norwalk virus (GI.1) and fed to human volunteers which showed that up to 61 days of storage of the seeded groundwater at room temperature in the dark, was still able to infect volunteers (Seitz, 2011). In an older outbreak study, two carpet fitters who removed a carpet in a ward where an outbreak had occurred 3 weeks earlier, got norovirus gastroenteritis symptoms (Cheesbrough, 1997), indicating that virus on carpets may be viable virus for at least 12 days. Similar findings have also been reported in an outbreak in a hotel (Kimura et al., 2011). No data on the persistence of sapovirus have been published.

3.0 Reductions by Sanitation Management

3.1 Wastewater treatment   

In waste stabilization ponds, noroviruses were not effectively removed compared to other wastewater treatment systems (Da Silva et al., 2007). Although it is not quantitative enough due to limited number of data or left censored data sets, norovirus GI and GII were removed up to 1.8 log10 and 1.6 log10 by waste stabilization pond with a residence time of several weeks (Da Silva et al., 2008), and  norovirus GII was removed about 1 log10 in a study in Ghana (Silverman et al., 2013).

No data are available on observable norovirus or caliciviruses removals by pit Latrines, vault toilets or dry toilets, septic tanks, wetlands, aerated lagoons.   Thus other RNA viruses and coliphages that serve as surrogates for the human caliciviruses may best represent the efficiency of removal.

3.1.1 Composting of fecal wastes

MNV RNA could not be detected after 1 day at 65°C in dairy manure compost, while at 60°C for 3 days, 3 log10 reduction was observed (Wei, 2010). However, infectivity data were not reported.

3.1.2 Wastewater Treatment Facilities

In sewer treatment systems, the primary treatment of simple sedimentation did not show removal of viruses (Simmons, 2011). However, noroviruses are removed in secondary treatments, as systematically reviewed (Sano, 2016). Norovirus log10 removal by activated sludge systems is estimated to be 1.48 (95% confidence interval (CI): 0.962.00) and 1.35 (95% CI: 0.522.18) for norovirus GI and GII, respectively. Sapovirus are often negative in treated wastewater as shown in Table 3 so that removal efficiency tend to be difficult to determine, but norovirus and sapovirus showed similar removal by trickling filters to the activated sludge systems (Kitajima, 2014).  

It is noteworthy that norovirus genomes and bacteriophages are more persistent in biofilms of wastewater treatment (moving-bed biofilm reactor) than in wastewater (Skraber, 2009), indicating a possible harbor for norovirus during non-endemic period.

Membrane bioreactors (MBR) have become more popular in recent years due to its stable treatment of wastewater including its ability to remove viruses. MBR showed better removal of noroviruses than conventional activated sludge systems (Da Silva, 2007), where removal by membrane (Sina et al., 2011) and adsorption to suspended solids (Miura, 2015) play important roles. Sapovirus was effectively (>2 Log10) removed by MBR (Miura et al., 2015). Log10 removal efficiency of norovirus GII by MBR is estimated from meta-analysis to be 3.35 (95% CI: 2.394.30) (Sano, 2016).

3.1.3 Other water treatments

Coagulation treatment using aluminum sulfate as coagulant, reduced norovirus by 1.5 log10 which is similar to MS2 or poliovirus (Shin and Sobsey, 2015), where a river water used for source of tap water is used as test water; pH 6.6–7.0, turbidity 1.5–2.6 NTU, alkalinity 21–24 mg/L as CaCO3, and hardness 20 mg/L as CaCO3.   

Using river water as the source water, ultrafilters (UFs) were able to remove 1 to 4 log10 of norovirus virus-like particles depending on pore size, while almost no reduction was observed by simple application of microfilters (MF) at pore sizes of 0.1 um regardless of the material of filter (PVDF, polyvinylidene difluoride; PTFE, polytetrafluoroethylene; or MC, mixture of cellulose acetate and cellulose nitrate). However, addition of coagulant increased the removal efficiency of MF dramatically, reaching up to more than 4 log10, exceeding the removal of UFs (Matsushita, 2013).

3.2 Disinfection

3.2.1 Chlorine and ozone

One of the first studies looking at the effect of chlorine on Norwalk virus resulted in some surprising data on the resistance of this virus suggesting that noroviruses may be more resistance to chlorine compared to other enteric viruses (Keswick, 1985). However, the experimental design of this study has been questioned as the virus purification methods and dispersion methods were not well documented, nor the quantity of virus was not described in detail. More recent work using RT-PCR for the detection of norovirus RNA, clearly demonstrated that norovirus genomes are reduced 3 log10 after 10 min at 1 mg/L of chlorine, at pH 6,5, which shows similar resistance to chlorine to other enteric viruses (Shin and Sobsey, 2008).

Treatment by ozone showed that Norwalk virus as well as other enteric viruses can be reduced rapidly and extensively by ozone disinfection (Shin and Sobsey, 2003). No data are available on sapovirus.

3.2.2 Solar irradiation and UV disinfection

Solar irradiation may be one of the best options to reduce viruses under limited resources, yet no data are available on noroviruses inactivation due to the lack of an available cell culture method. MNV showed no reduction by irradiation of UV-A, which is the main UV right reaching on the surface of earth, indicating that solar radiation may not be sufficiently effective against noroviruses (Harding and Schwab, 2012).

A few studies have investigated the effect of ultraviolet irradiation on noroviruses but, since no cultivation method is available, only MNV data are available so far,  which showed no evidence of resistance higher than other (cultivable) enteric viruses (Lee and Ko, 2013). It is noteworthy that PCR data may overestimate the persistence of noroviruses after inactivation by UV (Rönnqvist, 2014); norovirus genome reduced only 0.62 log10 at 300mJ/cm2 by low-pressure mercury-vapor UV lamp, whereas MNV infectivity reduced 5 log10 at 90mJ/cm2.

References

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