key: cord-0952290-61rw93xn
authors: Mattison, K.; Bidawid, S.; Farber, J.
title: Hepatitis viruses and emerging viruses
date: 2014-03-27
journal: Foodborne Pathogens
DOI: 10.1533/9781845696337.3.891
sha: 57ada931d5b5d779a2667d7aee4a60b16b615c29
doc_id: 952290
cord_uid: 61rw93xn

This chapter describes viruses that are enterically transmitted and cause systemic disease. These are recognized as important food and waterborne pathogens. The chapter first summarizes the general characteristics of the viruses, then describes their typical epidemiological patterns. The chapter then discusses methods to detect and to inactivate the viruses, with an emphasis on strategies that can be implemented for food safety.

Viruses that are recognized as causes of foodborne and waterborne illness can be separated into four general groups: the viruses that cause gastroenteritis (Chapter 32), the viruses that cause hepatitis, the enteroviruses and emerging viruses.

The enterically transmitted hepatitis viruses (hepatitis A and hepatitis E) replicate and cause disease in the liver, while the enteroviruses (polio, echo and coxsackie) replicate in the small intestine but migrate to and cause illness in other organs. These two groups of viruses are transmitted by the faecal-oral route, either directly from person-to-person or indirectly when food or water is contaminated with faecal material from infected individuals. There are also some emerging viruses that are not usually transmitted via the faecal-oral route, but recent reports indicate they may infect via the gastrointestinal tract and have the potential to emerge as a food safety concern (influenza A, coronavirus, tickborne encephalitis). See Table 25 .1 for a summary of the viruses discussed in this chapter. frame that is post-translationally processed to yield all of the viral proteins (Kitamura et al., 1981) . Infection with poliovirus occurs following the ingestion of contaminated food or water. The virus replicates in the human intestinal tract resulting in asymptomatic infection or minor malaise in over 90 % of cases (Melnick, 1996) . Mild illness characterized by fever, headache, nausea and sore throat can occur in 4-8 % of infections. If the virus spreads to infect the nervous system, a further 1-2 % of cases experience stiffness in the back and neck, as well as mild muscle weakness. The major illness, paralytic poliomyelitis, occurs in approximately 1 % of cases and consists of meningitis plus persisting weakness of one or more muscle groups. The amount of damage to neurons is highly variable (Melnick, 1996) . In endemic countries, the virus affects predominantly young children, with most cases of poliomyelitis occurring in those below five years of age (Singh et al., 1996) .

Poliovirus was the first virus shown to be transmitted through food, and a number of outbreaks were associated with raw milk prior to the introduction of routine pasteurization (Dingman, 1916; Sullivan and Read, 1968) . Polio can be prevented using a live attenuated vaccine administered orally or by an injectable killed vaccine (Melnick, 1996) . As a result of the poliovirus eradication campaign led by the World Health Organization (WHO), infection with this virus has been eradicated or significantly reduced in many regions of the world and, as such, it is of questionable importance for routine food safety considerations (Lahariya, 2007) . However, due to its historic importance and the early development of an attenuated vaccine strain, there have been many studies on the spread and inactivation of poliovirus in food products.

The Influenza virus A genus is classified in the family Orthomyxoviridae (Fauquet et al., 2005) . This family is characterized by pleiomorphic, enveloped virions with a segmented single-stranded RNA genome (Fauquet et al., 2005) . The genome is 14 kb of negative-sense RNA in eight segments, and its complement codes for structural and non-structural proteins (Fauquet et al., 2005) . They are classified into sub-types on the basis of the two envelope glycoproteins, the hemagglutinase (H type) and the neuraminidase (N type) (Knossow and Skehel, 2006) . There are 16 known H types and 9 known N types, which can theoretically be mixed and matched in all possible combinations (Knossow and Skehel, 2006) .

All of the known sub-types of Influenza A viruses (82 H/N combinations out of a possible 144) have been found in wild birds (Van Reeth, 2007) . Viruses containing combinations of the H1, H2, H3, N1 and N2 types are considered to be established in the human population; i.e. there are circulating strains of these viruses that predominantly infect humans (Hay et al., 2001) . In addition, viruses of the H5, H7 and H9 sub-types have been found to cause sporadic human infections (Peiris et al., 1999; Shortridge et al., 2000; Koopmans et al., 2004) . The subtype of recent worldwide concern is the highly pathogenic H5N1 virus (Abdel-Ghafar et al., 2008) . This particular avian influenza virus sub-type has been detected in poultry from over 50 countries on three continents (Van Reeth, 2007) . It has infected humans in Vietnam, Thailand, Indonesia, Cambodia, China, Turkey, Iraq, Azerbaijan, Egypt and Djibouti (de Jong and Hien, 2006) . This virus replicates to abnormally high levels in the upper respiratory tract, causing an intense inflammatory response and an extremely high case fatality rate of over 60 % (de Jong et al., 2006) . The H5N1 avian influenza virus currently has a limited ability to spread from person to person. However, there is concern that this virus could acquire the ability to spread effectively in humans, leading to a worldwide pandemic (Rajagopal and Treanor, 2007) . The Spanish influenza pandemic, which killed approximately 50 million people worldwide is thought to have arisen from an avian H1N1 strain (Rajagopal and Treanor, 2007) .

To date, H5N1 avian influenza infections of humans have nearly all been linked to close contact between the afflicted individuals and infected poultry (de Jong and Hien, 2006; Van Reeth, 2007; Abdel-Ghafar et al., 2008) . However, the virus can be isolated from all parts of infected poultry including the blood, bones and meat (Lu et al., 2003b; Swayne, 2006a) . As a result, the consumption of raw or undercooked poultry products represents a potential source of infection (Swayne, 2006b) .

The members of the Coronaviridae family are pleiomorphic, enveloped, single-stranded RNA viruses (Fauquet et al., 2005) . The positive-sense, 30 kb genome codes directly for viral proteins (Fauquet et al., 2005) . These viruses typically cause mild respiratory disease; however, a particularly virulent strain known as the Sudden Acute Respiratory Syndrome Coronavirus (SARS-CoV) emerged in 2003 and caused over 8000 cases, with a nearly 10 % case fatality rate (Wang and Chang, 2004) . This virus caused systematic infections as well as respiratory illness, and was identified in the digestive tract, as well as in faeces and sewage (Chan-Yeung and Xu, 2003; Zhang, 2003; Wang et al., 2005) . This raises the possibility that the virus may have had the potential to spread through the faecal-oral route and food products. Although these viruses are able to persist for days in some buffered media, they are sensitive to heating, UV light and disinfection (Duan et al., 2003; Rabenau et al., 2005a, b) . No cases of foodborne spread were documented during this outbreak, although one cluster of cases in a housing complex was linked to an index patient suffering from diahrroea (McKinney et al., 2006) .

The echoviruses and coxsackieviruses are enteroviruses of the family Picornaviridae and share many features with the polioviruses. They have 30 nm, non-enveloped particles enclosing a positive-sense single-stranded RNA genome (Fauquet et al., 2005) . These viruses are common and infections are mostly asymptomatic. They can occasionally spread outside of the gastrointestinal tract to cause aseptic meningitis, myocarditis or encephalitis. Infection of newborns with these viruses can lead to serious or fatal infection (Abzug, 2004) . These viruses are transmitted via the faecal-oral route, but are not frequently associated with foodborne illness. A recent report identified milk from an infected mother as the source of coxsackievirus B infection (Chang et al., 2006) .

The tickborne encephalitis virus is an enveloped, single-stranded RNA virus of the family Flaviviridae (Fauquet et al., 2005) . It is endemic to Europe and Russia, causing 10 000-12 000 cases of encephalitis every year, with a case fatality rate of 0.5 % (Gunther and Haglund, 2005) . Survivors can develop long-term neurological sequelae at rates of up to 40 % (Dumpis et al., 1999) . The majority of cases are transmitted by tick bites, but some have been associated with the consumption of raw milk from infected cattle or goats (Sixl et al., 1989; WHO, 1994; Dumpis et al., 1999; Kerbo et al., 2005) .

Additional emerging viruses of interest cause symptoms of gastroenteritis. These include the parvoviruses, toroviruses and picobirnaviruses. See Chapter 32 for a detailed description of the causative agents of viral gastroenteritis.

There is an inverse correlation between hepatitis A disease rates and viral endemicity (Shapiro and Margolis, 1993) . The Centres for Disease Control and Prevention in the USA has classified regions according to high (Central and South America, Africa, South Asia, Greenland), intermediate (Russia and Eastern Europe) and low (North America, Western Europe, Scandinavia, Australia) seroprevalence rates for hepatitis A (CDC, 2007) . This is important because many of the cases and outbreaks of hepatitis A in developed countries can be traced to travel in endemic countries (Steffen, 2005) . There may also be a higher risk for food produced in the highly endemic countries to be contaminated with the hepatitis A virus (Fiore, 2004) .

Disease rates in low endemicity countries are difficult to generalize. They are characterized by cyclical peaks and troughs, and they are changing in response to recent vaccination campaigns (Pham et al., 2005; Wasley et al., 2005) . Undiagnosed children may be an important source of the hepatitis A virus in communities, as a high percentage of hepatitis A infections have no known source (Staes et al., 2000; Nainan et al., 2005) . There has been a safe and effective vaccine available against hepatitis A since the mid-1990s; however, this virus continues to cause outbreaks, with contaminated food being one important source of infection (Fiore et al., 2006; Craig et al., 2007) .

Foodborne outbreaks of hepatitis A have been associated with many different food types and different settings (see Table 25 .2 for a summary of some outbreaks published over the past 10 years). Viruses are inert particles when present outside their host. The spread of hepatitis A infection through contaminated food, water or fomites is therefore dependent on the persistence of the virus after the introduction of contaminated human waste.

Documented outbreaks of hepatitis A due to shellfish have been caused by faecal contamination of shellfish growing waters (Conaty et al., 2000; Bosch et al., 2001; Bialek et al., 2007; Pontrelli et al., 2007; Shieh et al., 2007) . The hepatitis A virus survives for up to one month in dried faecal matter (McCaustland et al., 1982) . In mixtures of human and animal waste designed for waste treatment prior to disposal, it takes 7 d to reduce viral titre by 1 log 10 at 37 °C (Deng and Cliver, 1995) . Once introduced into the water environment, the hepatitis A virus also remains infectious for months, associating with marine sediment Bosch, 1998) . The hepatitis A virus has been shown experimentally to accumulate in mussels and oysters, and depuration is not effective at eliminating the virus from the shellfish tissue (Franco et al., 1990; Enriquez et al., 1992; Abad et al., 1997b; De Medici et al., 2001; Kingsley and Richards, 2003) . Extensive depuration for more than three weeks was required to completely eliminate detectable hepatitis A virus from oyster tissue (Kingsley and Richards, 2003) .

Fresh or frozen produce is another important source of foodborne hepatitis A outbreaks (Hutin et al., 1999; Dentinger et al., 2001; Calder et al., 2003; CDC, 2003b; Amon et al., 2005; Wheeler et al., 2005; Frank et al., 2007) . In these reports, the human fecal contamination might have been introduced during produce growth , harvest (Calder et al., 2003) , processing (Frank et al., 2007) or distribution. Consequently, the point of viral contamination can be difficult to identify (Hutin et al., 1999; Dentinger et al., 2001; CDC, 2003b; Howitz et al., 2005; Wheeler et al., 2005; Tekeuchi et al., 2006) . Once fresh produce is contaminated, the hepatitis A virus adsorbs to its surface and persists for days (Croci et al., 2002; Stine et al., 2005) . Freezing allows the virus to survive for months to years (Niu et al., 1992) . In addition, washing the contaminated produce does not usually substantially reduce the level of contamination (Croci et al., 2002) .

The remaining source of reported hepatitis A outbreaks are infected food handlers (CDC, 2003a; Prato et al., 2006; Schenkel et al., 2006; Hasegawa et al., 2007) . Hepatitis A virus has been shown to persist on experimentallycontaminated hands for more than 4 h (Mbithi et al., 1992) . The virus was Bialek et al., 2007; Shieh et al., 2007 Shieh et al., 2006 9 Japan Sushi bar (undetermined) Unknown Tekeuchi et al., 2006 Tekeuchi et al., 2006 15 Japan Restaurant (undetermined) Food handler Hasegawa et al., 2007 readily transferred between inoculated fingers, to foods or stainless steel surfaces and from stainless steel surfaces (Mbithi et al., 1992; Bidawid et al., 2000a) . The virus has been shown to attach to many of the surfaces common in food preparation settings, i.e. stainless steel, copper, polythene and polyvinyl chloride (Kukavica-Ibrulj et al., 2004) and to survive for more than 60 d on aluminium, china, latex and paper surfaces (Abad et al., 1994) . The most effective prevention of hepatitis A virus transmission is to prevent faecal contamination of foods and food preparation surfaces (see Section 25.5.1). In addition, there are some physical and chemical procedures known to effectively eliminate the hepatitis A virus from contaminated foods and surfaces (Tables 25.3 

The hepatitis A virus is resistant to acid treatment, both in buffered solutions and in food products (Scholz et al., 1989; Hewitt and Greening, 2004) . Heating is an effective mode of viral inactivation, but higher temperatures than those generally used to reduce bacterial counts are required (Parry and Mortimer, 1984) . Protection of the virus is also conferred by food matrices, and longer times and/or higher temperatures are required to completely inactivate the virus (Croci et al., 1999; Bidawid et al., 2000d; Deboosere et al., 2004) . For example, increasing the fat content (Bidawid et al., 2000d) or the sucrose concentration (Deboosere et al., 2004) of food preparations has been shown to increase the heat resistance of the virus. This may be due to a general effect of decreasing the water activity, but this possibility has not been systematically addressed. The result is that many traditional heat-inactivation or cooking protocols, such as pasteurization, steaming or baking, are insufficient to ensure the safety of hepatitis A-contaminated foods (Bidawid et al., 2000d; Croci et al., 2005; Hewitt and Greening, 2006) .

Heating to 85 °C is not possible for fresh fruits and vegetables, and even for milk and shellfish the procedures required may render foods unpalatable. Surface decontamination may be possible using targeted applications. Alternative physical inactivation methods show some promise for the inactivation of hepatitis A in food products. The virus is sensitive to UV light, but the light must access viral particles to inactivate them, which makes the technique difficult to apply to most food products (Nuanualsuwan et al., 2002) . High hydrostatic pressure is a newer technique that has the potential to inactivate the hepatitis A virus in food products while maintaining the organoleptic properties of raw products, particularly shellfish. The technique shows promise for the inactivation of hepatitis A virus in buffer, oysters, strawberries and green onions, although high pressure may reduce the palatability of fresh fruits and vegetables (Kingsley et al., 2002 (Kingsley et al., , 2005 Calci et al., 2005) .

Chemical methods are frequently used to eliminate virus dried on hands or on surfaces. The hepatitis A virus is more resistant to chemical disinfection than many enteric bacteria and enveloped viruses. Many commercially-available disinfectants are not effective when used on hepatitis A virus-contaminated Table 25 .4) (Mbithi et al., 1990; Abad et al., 1997a; Bidawid et al., 2000a; van Engelenburg et al., 2002; Jean et al., 2003; Bigliardi and Sansebastiano, 2006; Terpstra et al., 2007) . Notably, the active ethanol component of many commercial hand disinfectants has a very limited ability to reduce infectious hepatitis A virus titre from contaminated hands or surfaces (Mbithi et al., 1990; Bidawid et al., 2000a) . The most effective disinfectants are 2 % glutaraldehyde and 10 % sodium hypochlorite (5000 ppm free chlorine) (Grabow et al., 1983; Mbithi et al., 1990; Abad et al., 1997a; Jean et al., 2003) . Care must always be taken to follow appropriate time/concentration combinations for effective disinfection.

The hepatitis E virus is considered to be an endemic human pathogen in Central America, North Africa and South Asia (Panda et al., 2007) . It causes epidemic outbreaks of acute, enterically transmitted hepatitis in these countries, usually associated with faecally-contaminated water (Rab et al., 1997; Guthmann et al., 2006; Panda et al., 2007) . Such outbreaks have been particularly associated with the Indian subcontinent, although this may reflect a reporting bias rather than the true level of incidence (Panda et al., 2007) . During these classical outbreaks in endemic countries, person-to-person transmission does not contribute greatly to the number of cases (Hla et al., 1985; Somani et al., 2003) . The viral genome has been detected in raw and treated sewage, and outbreaks have been associated with chlorinated water supplies, indicating that basic treatment designed to eliminate faecal coliforms may not be sufficient to inactivate the hepatitis E virus (Jothikumar et al., 1993; Guthmann et al., 2006) . Sporadic cases of hepatitis E infection also occur in endemic countries and are likely contribute to the spread of the virus in the population (Nanda et al., 1994) .

In Western Europe, North America, Japan and Australia, the hepatitis E virus is an emerging concern (Teo, 2006) . Hepatitis E infections in these countries have historically been associated with travel to endemic regions (Zaaijer et al., 1993; Skidmore and Sherratt, 1996) . Recently, however, there have been reports of locally-acquired cases in developed countries, but the source of these infections remains uncertain (Mansuy et al., 2004; Ijaz et al., 2005; Waar et al., 2005; Reuter et al., 2006; Dalton et al., 2007; Perez-Gracia et al., 2007; Peron et al., 2007) . In two cases, the disease has been linked to the consumption of raw or undercooked meat from animals naturally infected with hepatitis E (Matsuda et al., 2003; Tei et al., 2003) . This has led to the hypothesis that the hepatitis E virus is an emerging foodborne zoonosis in developed nations (Teo, 2006) .

The hepatitis E virus is known to infect a wide range of animal species (Goens and Perdue, 2004; Vasickova et al., 2007) . Most of the studies and evidence for zoonotic transmission to humans have focused on strains isolated from swine (Goens and Perdue, 2004) . Studies have shown that these strains are very closely related to the human viruses and that they productively infect primates (Meng et al., 1997 (Meng et al., , 1998 . Phylogenetic analysis indicates that swine viruses are more closely related to their human counterparts within a country than to other swine isolates around the world (Meng et al., 1997; Hsieh et al., 1999; van der Poel et al., 2001; Pei and Yoo, 2002; Nishizawa et al., 2003; Banks et al., 2004) . Zoonotic transmission of this virus to the human population has been postulated to occur through the consumption of raw or lightly cooked meat from a naturally infected animal (Teo, 2006; Vasickova et al., 2007) . The evidence for this is strong in a few cases in Japan, but weak elsewhere (Matsuda et al., 2003; Tei et al., 2003) . However, infectious hepatitis E virus and/or viral RNA has been isolated from commercial pig livers in the USA, the Netherlands and Japan, indicating that this is a possible transmission route (Yazaki et al., 2003; Bouwknegt et al., 2007; Feagins et al., 2007) .

Testing the physical and chemical stability of the hepatitis E virus is challenging due to the lack of a cell culture system to propagate the virus. As such, the pH stability of this virus has yet to be formally demonstrated. The capsid protein acquires an increased heat stability at low pH, and the virus is known to infect via the gastrointestinal tract, implying some resistance to acidic conditions (Zafrullah et al., 2004) . The virus resists inactivation by heating at 56 °C, but heating to 71 °C completely inactivated the virus in naturally-contaminated pig livers (Emerson et al., 2005; Feagins et al., 2008) . Other physical and chemical methods of inactivation have not been tested, although an outbreak linked to chlorinated drinking water indicates that free chlorine residuals known to reduce fecal coliforms are not sufficient to inactivate the hepatitis E virus .

The poliovirus is no longer a prevalent enteric pathogen around the world. The widespread use of the oral polio vaccine, which confers intestinal immunity, has led to the eradication of the virus from three of the six regions of the world as defined by the WHO (Sabin, 1991; Lahariya, 2007) . These three regions are: the Americas, representing 35 countries, polio-free since 1994; the Western Pacific, representing 37 countries and territories, polio-free since 2000; and the European, representing 51 countries, polio-free since 2002 (CDC, 1994 (CDC, , 2001 (CDC, , 2002 . The disease is still endemic in Afganistan, India, Nigeria and Pakistan (Lahariya, 2007) . In recent years, there have also been other countries within the WHO regions of Africa, South-East Asia and the Eastern Mediterranean that have experienced outbreaks of poliomyelitis caused by both wild and vaccine-derived strains (Melnick, 1996; Chumakov et al., 2007) . Due to the prevalence of asymptomatic disease, the absence of poliomyelitis does not always correlate with the absence of the poliovirus, and intensive vaccination campaigns are still warranted (Chumakov et al., 2007) . Individuals in polio-free countries still routinely follow a course of vaccination with the killed vaccine (Wood et al., 2000 (Wood et al., , 2006 .

Similarly to the hepatitis A virus, the poliovirus can be introduced at any stage in the farm-to-fork continuum. The virus has a low infectious dose (Plotkin et al., 1959) and is frequently isolated from sewage during outbreaks and in endemic countries (Arya and Agarwal, 2007) . Once again, shellfish, fresh produce and food handlers are the most significant sources of foodborne virus transmission.

Poliovirus accumulates readily in shellfish and concentrates in the digestive tract (Di Girolamo et al., 1975) . Depuration of poliovirus is more effective than for hepatitis A, and most of the virus can be eliminated in free-flow depuration system after 5 d (Di Girolamo et al., 1975; Franco et al., 1990; Enriquez et al., 1992) .

The stability and accumulation of poliovirus is of significant concern in agricultural systems. The poliovirus is inactivated more readily than the hepatitis A virus by heating and storage treatments used to prepare manure for spreading on lands (Stramer and Cliver, 1984; Deng and Cliver, 1992) . However, once the environment is contaminated, the poliovirus survives for weeks to months in groundwater (Yates et al., 1985; Gordon and Toze, 2003) and in soil (Yeager and O'Brien, 1979; Hurst et al., 1980) . This virus has also been shown to persist for weeks to months on vegetables irrigated by spraying or flooding with contaminated waters (Tierney et al., 1977) . It has also been demonstrated to survive for weeks to months on fresh and frozen produce, and simple washing does not appear to effectively eliminate poliovirus from food surfaces (Kurdziel et al., 2001; Lukasik et al., 2003) .

Poliovirus is moderately acid stable, resistant to incubation at pH 3.0 for 30 min, but sensitive to pH 1.0 (Eubanks and Farrah, 1981; Siegl et al., 1984; Scholz et al., 1989) . Heating is extremely effective for the inactivation of poliovirus in buffered solutions, although food matrices may provide some protection and require longer heating times (see Table 25 .3) (McGregor and Mayor, 1971; Milo, 1971; Stramer and Cliver, 1984; Strazynski et al., 2002) . This may be due to protection provided by protein, fat, lowered a w or a combination of these parameters. Both UV light and ozone are effective in elimination of the poliovirus, and have been considered for the treatment of wastewater to be used in irrigation (Ma et al., 1994; Nuanualsuwan et al., 2002; Lazarova and Savoys, 2004; Tanner et al., 2004) .

Food handlers with inadequate hygiene are frequently implicated in the transmission of viruses via the fecal-oral route. The virus can be transferred from contaminated hands to surfaces, where it resists drying and can persist for days to weeks (Mbithi et al., 1993; Abad et al., 2001) . In a food service environment, there are a number of chemicals available to disinfect hands and surfaces potentially contaminated with the poliovirus (Table 25 .4). Reagents that implement quaternary ammoniums, glutaraldehyde or sodium hypochlorite as the active ingredient are effective against poliovirus on surfaces (Stramer and Cliver, 1984; Ma et al., 1994; Abad et al., 1997a; Weber et al., 1999; Lukasik et al., 2003) . The poliovirus is removed by soap and water handwashing for 5 min, but ethanol-based hand disinfectants (60-70 % ethanol) are only moderately effective against the virus (Schurmann and Eggers, 1985; Mbithi et al., 1993; Kramer et al., 2006) .

The WHO coordinates a Global Influenza Surveillance Network, with 119 National Influenza Centres in 90 countries (WHO, 2007) . These centres monitor the incidence of influenza, identify circulating strains and constantly update the risk for the emergence of a pandemic strain (Stohr, 2003) . The highly pathogenic H5N1 influenza virus of recent public health significance has caused a limited number of human infections worldwide, but has been circulating in poultry since 2003 with no signs of abating (ECDC, 2007) . These natural infections continue to pose a potential risk to humans who interact with infected flocks or who consume raw or undercooked poultry products (Swayne, 2006b) .

All influenza viruses are predominantly spread via aerosolized droplets that enter the respiratory tract of a susceptible host. Experimental models have shown that this transmission is most efficient at low temperatures and low relative humidity, in correlation with the winter seasonal peaks in influenza infections (Lowen et al., 2007) . The virus can persist for days when exposed to levels of solar radiation predicted for wintertime in temperate regions (Sagripanti and Lytle, 2007) . The H5 strains have been shown to persist for weeks or months in water (Brown et al., 2007) . Although the influenza virus is enveloped, it resists drying to some extent and exhibits a 1 log reduction in 24 h on stainless steel surfaces (Noyce et al., 2007) .

There is also a risk that the avian influenza viruses will spread through contaminated food products. Natural infections in chickens and ducks have been demonstrated to produce contaminated meat, blood and bone (Lu et al., 2003b; Swayne, 2006a; Thomas and Swayne, 2007) . The efficacy of physical and chemical inactivation methods has been shown to vary with influenza virus type, and not all methods have been tested with the relevant H5N1 strain (De Benedictis et al., 2007) . Tables 25.3 and 25.4 summarize the information available.

The influenza viruses have a highly variable response to acid (Scholtissek, 1985a, b) . The viruses are sensitive to heating, in buffer and in poultry products (Swayne and Beck, 2004; Swayne, 2006a, Thomas and . Although the highly pathogenic H5 strains have an increased heat resistance compared to low pathogenic avian influenza strains, they are inactivated at 70 °C, a temperature to which poultry is usually cooked (Swayne and Beck, 2004; Swayne, 2006a; Thomas and Swayne, 2007) . High-pressure treatment at 500 MPa has also been shown to be an effective means of inactivating the viruses (Isbarn et al., 2007) .

Influenza viruses are enveloped, which confers susceptibility to many types of disinfectants (De Benedictis et al., 2007) . Some of the agents specifically tested using avian influenza strains are listed in Table 25 .4 (King, 1991; Lu et al., 2003a; De Benedictis et al., 2007; Suarez et al., 2003) .

Classical virus detection methods involve the inoculation of cell cultures to amplify and detect infectious virus particles. These methods are rarely applicable to the isolation of foodborne viruses. Many of the important viruses do not grow in cell culture and the food extracts that need to be tested may be toxic to the cells. For example, although a model system exists for the study of inactivation kinetics, wild-type isolates of the hepatitis A virus grow very slowly, if at all, in culture and accumulate many mutations during this process (Cromeans et al., 1987; Konduru and Kaplan, 2006) . A recently developed hepatitis E culture system takes 60 d to amplify the virus to high levels . Alternative methods that rely on detection of the viral particle, such as electron microscopy and enzyme-linked immunosorbent assays, typically have detection limits on the order of 10 5 particles per gram of sample, while the infectious dose for foodborne viral infections has been estimated to be as few as 10-100 particles (Fiore, 2004; Koopmans and Duizer, 2004) . The advent of molecular methods for the detection of viral genomes has provided the increased detection sensitivity required to allow for a more accurate assessment of the viral contamination of food products . Although these methods do not distinguish between infectious and non-infectious particles, their advantages are so great that they are now used for the detection of all viruses in many food virology laboratories (Jothikumar et al., 2006; Sanchez et al., 2007) . Molecular techniques also have the advantage that they provide information on the genotype of the strains involved in outbreaks (Nainan et al., 2006) . This information can be useful in establishing an epidemiological link between cases of foodborne illness (Hutin et al., 1999) . Microarrays are also being developed that could provide genotyping without the need for sequencing amplicons (Pagotto et al., 2008) . The procedures outlined in the following sections describe viral extraction methods that are specific to different food types. In most cases, the extracted virus can be subsequently detected by a conventional, immunological or molecular method, as desired.

Methods to extract viruses from shellfish have been extensively studied. Most methods begin by homogenizing the shellfish tissue prior to viral extraction . Changing pH can be used to concentrate enteroviruses from oysters (Sobsey et al., 1975) . At low pH, virus adsorbs to shellfish tissue and can be concentrated by centrifugation. At high pH, the virus is eluted from the tissue. Ultrafiltration or ultracentrifugation are then able to concentrate the viral particles in solution. The main disadvantage of this type of system is that many contaminants remain in solution with the extracted virus and may interfere with downstream detection by either cell culture or molecular methods (Speirs et al., 1987) . Additional concentration steps using organic flocculation or polyethylene glycol precipitation can improve the detection efficiency (Traore et al., 1998) . Extremely sensitive detection is obtained by lysing the viral particles with a phenol-guanidinium chloride reagent and purifying the genome using magnetic poly(dT) beads (Kingsley and Richards, 2001) . This method has been standardized and published in the Health Canada Compendium of Analytical Methods for the microbiological analysis of potentially contaminated shellfish .

The development of procedures to isolate viruses from non-shellfish food samples has been more recent. Methods for viral isolation from fruits and vegetables employ washes or elution from the food surface, because homogenization releases many inhibitors of molecular reactions . Methods have been developed mainly for leafy greens, green onions and berries using a variety of concentration procedures (Bidawid et al., 2000c; Shan et al., 2005; Guevremont et al., 2006; Rzezutka et al., 2006; Butot et al., 2007; Papafragkou et al., 2008) . Polyethylene glycol precipitation (Guevremont et al., 2006) , immunomagnetic concentration (Bidawid et al., 2000c; Shan et al., 2005) , charge-based concentration (Bidawid et al., 2000c; Papafragkou et al., 2008) , ultracentrifugation (Rzezutka et al., 2006) and ultrafiltration (Butot et al., 2007) have all been reported to be useful for the isolation of virus particles from fruits and vegetables. For example, positively charged beads circulated and captured using the Pathatrix™ machinery yield detection limits below one plaque forming unit of the hepatitis A virus in some artificially-inoculated samples (Papafragkou et al., 2008) . In most cases, the choice of the method used is based on the reagents available to the testing laboratory, and the use of internal controls is not consistent. This is a concern because of the potential release of inhibitory compounds and should be addressed in future studies .

The detection of viruses in drinking water has traditionally involved concentration from large volumes of water using charged filters (Hill et al., 1976) . These methods used conventional cell culture methods to detect virus, and were thus hampered by a lack of sensitivity as well as the inability to detect non-culturable viruses. The advent of molecular methods has reduced the time and cost required for detecting viruses from water samples (Pillai, 1997) . These new methods have successfully been used to detect viral genomes or genome fragments in many types of raw and treated water samples (Kittigul et al., 2000; Albinana-Gimenez et al., 2006) . It has, however, been demonstrated that viral genome fragments (non-viable) are detected after wastewater treatment protocols that eliminate infectious virus (Simonet and Gantzer, 2006) . This raises concerns that the presence of genome fragments from enterically infecting viruses may not accurately predict the level of infectious virus in water samples.

The sources of hepatitis A in the food supply are highly variable. The long incubation period before infection is clinically apparent and the high rate of person-to-person transmission during hepatitis A outbreaks makes point sources difficult to identify Fiore et al., 2006) . The high proportion of asymptomatic infections in children under the age of five years generates another source of uncertainty in epidemiological investigations (Staes et al., 2000) . The accurate identification of disease transmission routes is a significant barrier to the implementation of effective control strategies to prevent hepatitis A virus transmission. The use of molecular detection and genotyping methods is one way to increase the odds of identifying linked cases of hepatitis A infection (see Section 25.4.1).

Due to the high degree of uncertainty in hepatitis A virus transmission, vaccination is one potential strategy for the control of infection (AAPCID, 2007) . There is a safe and effective vaccine, and it is currently recommended for use in travellers to and residents of areas of high endemicity (AAPCID, 2007; CDC, 2007) . Universal vaccination would be expensive, and has an unattractively high cost/benefit ratio when the healthy adult population of the developed world is the intended target (Anonychuk et al., 2008) . The use of sanitary measures to eliminate fecal contamination of foodstuffs should effectively limit foodborne hepatitis A outbreaks.

Pre-harvest control strategies are attractive because, when properly implemented, they minimize the need for downstream interventions. The most effective approach to prevent shellfish contamination is to prevent human sewage from entering shellfish growing waters. This sounds straightforward, but its enforcement can be difficult, particularly in remote areas with both commercial and recreational boat traffic. Imposing monetary penalties for waste dumping, mandating the use of waste containers that cannot easily be dumped overboard, and developing education outreach programs are three strategies with the potential to limit hepatitis A contamination of shellfish (Papafragkou et al., 2006) . If waters are contaminated, depuration can be used to reduce the levels of hepatitis A virus in shellfish prior to harvest, but viruses in shellfish tissue are purged more slowly than bacteria, and the hepatitis A virus in particular is not as readily depurated as other viruses (Richards, 2001; Chironna et al., 2002) . Unfortunately, current routine testing procedures do not look for viral contaminants in growing waters, and it has been repeatedly shown that the traditional bacterial indicators are not indicative of hepatitis A virus contamination (Croci et al., 2000; Muniain-Mujika et al., 2003; Pusch et al., 2005; Phanuwan et al., 2006; Villar et al., 2007) .

For the pre-harvest control of produce contamination, it is important to prevent human waste contamination of irrigation water. Although treatment regimens are available to allow the reuse of wastewater for irrigation, they are not necessarily effective against the hepatitis A virus Skraber et al., 2007) . Further research is necessary into the effectiveness of various water treatment protocols to determine if they are appropriate for the control of hepatitis A virus contamination. Produce is also sensitive to contamination introduced by human handling during harvest. Control procedures at this stage should include provision of toilet and hand-washing facilities, education on hygienic practices, reporting of active illnesses and provision of childcare so that young children, a prominent source of asymptomatic hepatitis A infections, are not present in the fields (Fiore, 2004; Koopmans and Duizer, 2004) .

After harvest, the physical and chemical decontamination methods discussed in detail in Section 25.3.1 can be used to eliminate the hepatitis A virus from contaminated foods and/or processing areas. These are more stringent procedures than those necessary to reduce most bacterial contamination, and must be implemented properly in order to be effective. Cooking will inactivate the hepatitis A virus, but the entire product must reach 85 °C to ensure viral reduction (Parry and Mortimer, 1984) . This is not suitable for fresh produce, and new technology must be developed to inactivate the virus in these products. Categories of food matrices must be individually tested to develop protocols that adequately reduce hepatitis A titre (Croci et al., 1999; Bidawid et al., 2000d; Deboosere et al., 2004) . The use of UV light and high hydrostatic pressure are promising, but their effectiveness must be further investigated before they will be useful for routine decontamination procedures (Nuanualsuwan et al., 2002; Kingsley et al., 2006) . Gamma irradiation is somewhat effective at reducing hepatitis A titre on lettuce and strawberries, but the dose for a 1 log reduction is approximately 3 kGy (Bidawid et al., 2000b) , while current regulations in the USA only allow doses up to 1 kGy for fresh foods (CFSAN, 2007) .

Food handlers are another source of hepatitis A virus infections (Fiore, 2004; Greig et al., 2007; Todd et al., 2007a, b) . Contamination may be introduced during the final preparation stages for ready-to-eat foods (Greig et al., 2007; Todd et al., 2007a, b) . The hepatitis A virus is excreted for up to two weeks prior to the development of symptoms (Fiore, 2004) . It is therefore important to stress proper hygiene and hand-washing practices for all food service workers. Proper hand-washing with soap and water has been shown to be more effective at removing hepatitis A virus from hands than ethanolbased hand rubs (Mbithi et al., 1993; Bidawid et al., 2000a) . Educational programs for food service workers must be designed with care to ensure the correct message is communicated. For example, gloved hands are frequently viewed as safer for food handling than bare skin, but care must still be taken to avoid cross-contamination of foods or surfaces. Preliminary data from our laboratory indicates that contaminated gloves spread virus very effectively (Bidawid et al., 2007) . Effective surface decontamination can also be used to interrupt hepatitis A virus transmission in food service settings, but as described in Section 25.3.1, not all commercial disinfectants are effective against the hepatitis A virus (Mbithi et al., 1990; Abad et al., 1997a; Bidawid et al., 2000a; van Engelenburg et al., 2002; Jean et al., 2003; Bigliardi and Sansebastiano, 2006; Terpstra et al., 2007) . For effective disinfectants, such as sodium hypochlorite, concentration and contact time must be followed precisely to effectively inactivate the virus on a contaminated surface (Grabow et al., 1983; Mbithi et al., 1990; Abad et al., 1997a; Jean et al., 2003) .

The control of hepatitis E infections in developing countries can be achieved by improving the availability of clean drinking water. This is linked to the availability of adequate hygienic facilities and improved hygienic practices. There is no vaccine available against hepatitis E, and the administration of pooled immunoglobulin from endemic areas does not appear to be protective (Khuroo and Dar, 1992; Panda et al., 2007) . Since it has been shown that the virus can survive the levels of chlorination currently recommended by the WHO, research into the physical and chemical inactivation of hepatitis E is urgently required to provide protocols that ensure the disinfection of contaminated water supplies . Experimental studies in pig livers and epidemiological evidence indicate that boiling water is sufficient to inactivate the virus (Velazquez et al., 1990; Feagins et al., 2008) .

As an emerging foodborne zoonotic agent, there is little information available about control measures that will prevent the spread of hepatitis E infection. The infection is endemic in many swine populations that have been examined, but does not cause overt disease. As a result, there is no incentive for control measures to improve animal health (Goens and Perdue, 2004) . If the link between infected animals and transmission to humans can be established outside of Japan, this might provide a rationale for the development of animal-specific prevention strategies. At this time, however, the most effective control measure against infection is thorough cooking of meats and organ meats prior to consumption (Feagins et al., 2008) . Because of the low rates of person-to-person transmission in documented outbreaks, transmission via food handlers and ready-to-eat foods is not expected to be a major source of infection (Hla et al., 1985; Somani et al., 2003) .

Control measures against poliovirus involve vaccination programs and the global eradication initiative (Arya and Agarwal, 2007; Chumakov et al., 2007) . The virus does not have a non-human host, and it cannot circulate if the human population has a high level of mucosal immunity to infection (Melnick, 1996) . Unfortunately, in addition to the four remaining endemic countries, 21 countries have experienced a resurgence or importation of poliomyelitis in recent years (Lahariya, 2007) . This is due to the high prevalence of asymptomatic infections, as well as to vaccine-derived strains causing disease in communities (Chumakov et al., 2007; Lahariya, 2007) .

Fortunately, some relatively straightforward measures can be implemented to ensure that the poliovirus, if circulating, does not enter the food supply. Pasteurization of milk products has been shown historically to disrupt poliovirus transmission (Sattar et al., 2001) . Similar time/temperature combinations (72 °C, 30 s) can be used to inactivate the virus in other potentially contaminated liquids (Strazynski et al., 2002) . Depuration of shellfish greatly reduces the risk of poliovirus transmission by this route, and proper hand-washing by food handlers interrupts the chain of transmission during final preparation of foods (Schurmann and Eggers, 1985; Franco et al., 1990; Enriquez et al., 1992) . It should be noted that for all of these measures, the conditions required to eliminate polio are less stringent than those required for the inactivation of hepatitis A (Table 25 .3).

The presence of the poliovirus in wastewater remains the most important means of transmission in endemic countries, and effective methods exist to remove polio from sewage (Pavlov, 2006; Arraj et al., 2005; Belguith et al., 2007; Dedepsidis et al., 2007) . New methods under development, such as ozone and UV light, are able to decontaminate poliovirus-contaminated wastewater (Lazarova and Savoys, 2004; Tanner et al., 2004) . The required focus on sewage treatment and clean water in the developing world is reminiscent of control measures to prevent the spread of many bacterial illnesses (Berry et al., 2006) . The integration of clean water programs aimed at reducing the burden of bacterial and viral illness can only serve to increase the likelihood that these programs will see some successes in limiting the spread of enteric disease.

Current strategies to mitigate the human health risks associated with the H5N1 avian influenza virus are mainly focused on preventing the disease from spreading in the animal population (Rajagopal and Treanor, 2007) . The elimination of H5N1 infections in birds would of course remove the risk to humans. Unfortunately, H5N1 infections in birds have become endemic in many countries (ECDC, 2007, Rajagopal and Treanor, 2007) . Therefore, accurate monitoring and understanding the circulation of the virus in wild and domestic birds is critical to the success of control programs (Olsen et al., 2006) . All H5 or H7 type avian influenza infections are notifiable to the World Organization for Animal Health (OIE, 2007) . Early detection of the H5N1 infection in a local poultry population is a key step in preventing the disease from becoming widespread (Sims, 2007) .

A vaccine is available against the H5 and H7 avian influenza virus subtypes, and its use in the poultry population is one way to control the spread of emerging highly pathogenic viruses (Capua and Marangon, 2007) . It is not possible to vaccinate all birds in areas where these viruses are endemic, and additional measures must be in place to prevent the spread of disease (Guan et al., 2007; Sims, 2007) . A combination of surveillance, vaccination, culling of infected birds and segregation of wild and domestic poultry is recommended to control the spread of emerging epidemic avian influenza strains (Guan et al., 2007) .

Control measures to prevent transmission of avian influenza through the food supply are more straightforward. All of the strains and sub-types of influenza are more susceptible to heating and to chemical disinfection than the other foodborne viruses described in this chapter (see Tables 25.3 and 25.4). Thorough cooking of poultry products and basic disinfection of food preparation surfaces is sufficient to prevent foodborne transmission of the influenza virus (De Benedictis et al., 2007) .

Two of the four viruses discussed in detail in this chapter are emerging zoonoses (hepatitis E and avian influenza). It is important that public health programs continue to monitor these diseases in both animals and humans in order to develop accurate risk assessment and prevention planning (Merianos, 2007) . The other two viruses (hepatitis A and polio) cause human illnesses that are vaccine-preventable. Calls from experts to continue and expand vaccine coverage with the goal of reducing the disease burden from these viruses is likely to continue (AAPCID, 2007; Chumakov et al., 2007) .

In addition to public health measures, the food production and processing industries can take action to reduce the spread of viruses through food. A recurring point in the above discussion is the remarkable resistance of viruses to decontamination procedures. Heating and disinfection protocols for viruses and food preparation surfaces are being defined in the literature, but they must also be recognized and implemented along the food production continuum. In addition, these viruses typically have a very low infectious dose (10-100 particles) and they can be excreted at high levels (10 6 -10 11 particles per gram of faeces). Since contamination of food products is typically a secondary event, a 5 log reduction in infectious particles has been considered effective for control. The recent development of sensitive and semi-quantitative detection methods will help to identify the critical control points along the food production and preparation continuum where virus contamination can be reduced. Unfortunately, many of these methods detect viral genomes instead of infectious virus particles. The regulation of viruses in foods will require a more detailed understanding of the correlation between the presence of viral nucleic acid fragments and a human health risk. 

the environment and in a drinking-water treatment plant

Molecular epidemiology of foodborne hepatitis A outbreaks in the United States

Cost-effectiveness analyses of hepatitis A vaccine: a systematic review to explore the effect of methodological quality on the economic attractiveness of vaccination strategies

Aetiological association of a virus-like particle with enterically transmitted non-A, non-B hepatitis

Molecular characterization of hepatitis A virus from a large outbreak from Kerala

Persistence of infectious hepatitis A virus and its genome in artificial seawater

Comparison of bacteriophage and enteric virus removal in pilot scale activated sludge plants

Poliomyelitis: concerns for polio-free countries

Natural hosts of hepatitis A virus

Evidence for the presence of hepatitis E virus in pigs in the United Kingdom

Enterovirus circulation in wastewater and behavior of some serotypes during sewage treatment in Monastir

Microbial ecology of drinking water distribution systems

Use of molecular epidemiology to confirm a multistate outbreak of hepatitis A caused by consumption of oysters

Contamination of foods by food handlers: experiments on hepatitis A virus transfer to food and its interruption

Inactivation of hepatitis A virus (HAV) in fruits and vegetables by gamma irradiation

Rapid concentration and detection of hepatitis A virus from lettuce and strawberries

Heat inactivation of hepatitis A virus in dairy foods

The potential for pathogen cross-contamination of foods with gloved hands: experiments with feline calicivirus as a surrogate for human enteric viruses

Study on inactivation kinetics of hepatitis A virus and enteroviruses with peracetic acid and chlorine. New ICC/PCR method to assess disinfection effectiveness

High mortality associated with an outbreak of hepatitis E among displaced persons in Darfur

Human enteric viruses in the water environment: a minireview

Human enteric viruses in Coquina clams associated with a large hepatitis A outbreak

Hepatitis E virus RNA in commercial porcine livers in The Netherlands

Enterically transmitted non-A, non-B hepatitis: serial passage of disease in cynomolgus macaques and tamarins and recovery of diseaseassociated 27-to 34-nm viruslike particles

Persistence of H5 and H7 avian influenza viruses in water

Procedure for rapid concentration and detection of enteric viruses from berries and vegetables

High-pressure inactivation of hepatitis A virus within oysters

An outbreak of hepatitis A associated with consumption of raw blueberries

Control and prevention of avian influenza in an evolving scenario

Certification of poliomyelitis eradication -the Americas

Certification of poliomyelitis eradication -Western Pacific Region

Certification of poliomyelitis eradication -European Region

Foodborne transmission of hepatitis A -Massachusetts

Hepatitis A outbreak associated with green onions at a restaurant

Health Information for International Travel

Foods Permitted to be Irradiated Under FDA's Regulations, US Food and Drug Administration

Coxsackievirus B3 in human milk

Epidemiology and clinical features of sporadic hepatitis E as compared with hepatitis A

Detection of hepatitis A virus in mussels from different sources marketed in Puglia region (South Italy)

Vaccination against polio should not be stopped

Report of a possibly milk-borne epidemic of infantile paralysis

Stability of SARS coronavirus in human specimens and environment and its sensitivity to heating and UV irradiation

Tick-borne encephalitis

Avian influenza update: recent outbreaks of H5N1 in poultry worldwide

Thermal stability of hepatitis E virus

Accumulation and persistence of hepatitis A virus in mussels

Inactivation of poliovirus and other enteroviruses by solutions of sodium fluoride at low pH

Virus Taxonomy: Eigth Report of the International Committee on the Taxonomy of Viruses

Detection and characterization of infectious hepatitis E virus from commercial pig livers sold in local grocery stores in the USA

Inactivation of infectious hepatitis E virus present in commercial pig livers sold in local grocery stores in the United States

Hepatitis A: detection by immune electron microscopy of a viruslike antigen associated with acute illness

Hepatitis A transmitted by food

Prevention of hepatitis A through active or passive immunization: recommendations of the Advisory Committee on Immunization Practices (ACIP)

Depuration of Mytilus galloprovincialis experimentally contaminated with hepatitis A virus

Major outbreak of hepatitis A associated with orange juice among tourists

Detection of infectious enteroviruses, enterovirus genomes, somatic coliphages, and Bacteroides fragilis phages in treated wastewater

Hepatitis E viruses in humans and animals

Influence of groundwater characteristics on the survival of enteric viruses

Inactivation of hepatitis A virus and indicator organisms in water by free chlorine residuals

Outbreaks where food workers have been implicated in the spread of foodborne disease. Part 1. Description of the problem, methods, and agents involved

A model to control the epidemic of H5N1 influenza at the source

Development of an extraction and concentration procedure and comparison of RT-PCR primer systems for the detection of hepatitis A virus and norovirus GII in green onions

Tick-borne encephalopathies: epidemiology, diagnosis, treatment and prevention

A large outbreak of hepatitis E among a displaced population in Darfur, Sudan, 2004: the role of water treatment methods

Hepatitis A in day-care centers. A community-wide assessment

Genetic identification and characterization of a novel virus related to human hepatitis E virus from chickens with hepatitis-splenomegaly syndrome in the United States

Outbreak of hepatitis A virus infection caused by food served in a restaurant

The evolution of human influenza viruses

Survival and persistence of norovirus, hepatitis A virus, and feline calicivirus in marinated mussels

Effect of heat treatment on hepatitis A virus and norovirus in New Zealand Greenshell mussels (Perna canaliculus) by quantitative real-time reverse transcription PCR and cell culture

Detection of virus in water: sensitivity of the tentative standard method for drinking water

A clinical and epidemiological study of an epidemic of non-A non-B hepatitis in Rangoon

Hepatitis A outbreak in a group of Danish tourists returning from Turkey

Identity of a novel swine hepatitis E virus in Taiwan forming a monophyletic group with Taiwan isolates of human hepatitis E virus

Effects of environmental variables and soil characteristics on virus survival in soil

A multistate, foodborne outbreak of hepatitis A. National Hepatitis A Investigation Team

Acute sporadic hepatitis E in children living in Cairo

Non-travel-associated hepatitis E in England and Wales: demographic, clinical, and molecular epidemiological characteristics

agri-food surfaces using immunological, virological and thermodynamic assays

Survival of poliovirus on soft fruit and salad vegetables

Global eradication of polio: the case for 'finishing the job

Technical and sanitary aspects of wastewater disinfection by UV irradiation for landscape irrigation

Influenza virus transmission is dependent on relative humidity and temperature

Survival of avian influenza virus H7N2 in SPF chickens and their environments

Pathogenesis of and immunity to a new influenza A (H5N1) virus isolated from duck meat

Phylogenetic analysis of global hepatitis E virus sequences: genetic diversity, subtypes and zoonosis

Reduction of poliovirus 1, bacteriophages, Salmonella montevideo, and Escherichia coli O157:H7 on strawberries by physical and disinfectant washes

Cell culture and PCR determination of poliovirus inactivation by disinfectants

Hepatitis E in the south west of France in individuals who have never visited an endemic area

Severe hepatitis E virus infection after ingestion of uncooked liver from a wild boar

Chemical disinfection of hepatitis A virus on environmental surfaces

Survival of hepatitis A virus on human hands and its transfer on contact with animate and inanimate surfaces

Comparative in vivo efficiencies of hand-washing agents against hepatitis A virus (HM-175) and poliovirus type 1 (Sabin)

Survival of hepatitis A virus in feces after drying and storage for 1 month

Internal components released from rhinovirus and poliovirus by heat

Environmental transmission of SARS at Amoy Gardens

Current status of poliovirus infections

Novel strains of hepatitis E virus identified from humans and other animal species: is hepatitis E a zoonosis?

A novel virus in swine is closely related to the human hepatitis E virus

Genetic and experimental evidence for cross-species infection by swine hepatitis E virus

Surveillance and response to disease emergence

Thermal inactivation of poliovirus in the presence of selective organic molecules (cholesterol, lecithin, collagen, and beta-carotene)

Comparative analysis of viral pathogens and potential indicators in shellfish

Hepatitis A molecular epidemiology in the United States, 1996-1997: sources of infection and implications of vaccination policy

Diagnosis of hepatitis A virus infection: a molecular approach

Etiological role of hepatitis E virus in sporadic fulminant hepatitis

Characterization of Japanese swine and human hepatitis E virus isolates of genotype IV with 99 % identity over the entire genome

Multistate outbreak of hepatitis A associated with frozen strawberries

Inactivation of influenza A virus on copper versus stainless steel surfaces

Ultraviolet inactivation of feline calicivirus, human enteric viruses and coliphages

Avian Influenza, Terrestrial Animal Health Code, 16th edn, Paris, World Organization for Animal Health

Global patterns of influenza A virus in wild birds

Development of a DNA microarray for the simultaneous detection and genotyping of noroviruses

Hepatitis E virus

Foodborne viruses: prevention and control

Rapid and sensitive detection of hepatitis A virus in representative food matrices

The heat sensitivity of hepatitis A virus determined by a simple tissue culture method

Poliovirus vaccine strains in sewage and river water in South Africa

Genetic characterization and sequence heterogeneity of a Canadian isolate of swine hepatitis E virus

Human infection with influenza H9N2

Autochthonous hepatitis E infection in a slaughterhouse worker

Fulminant liver failure from acute autochthonous hepatitis E in France: description of seven patients with acute hepatitis E and encephalopathy

Seroprevalence of hepatitis A infection in a low endemicity country: a systematic review

Monitoring of human enteric viruses and coliform bacteria in waters after urban flood in Jakarta

Rapid molecular detection of microbial pathogens: breakthroughs and challenges

Clinical trials in infants of orally administered attenuated poliomyelitis viruses

Epidemiological and virological characterization of a large community-wide outbreak of hepatitis A in southern Italy

An outbreak of hepatitis A in Southern Italy: the case for vaccinating food handlers

Detection of enteric viruses and bacterial indicators in German environmental waters

Water-borne hepatitis E virus epidemic in Islamabad, Pakistan: a common source outbreak traced to the malfunction of a modern water treatment plant

Stability and inactivation of SARS coronavirus

Efficacy of various disinfectants against SARS coronavirus

Pandemic (avian) influenza, Semin Respir Crit Care Med

Identification of a novel variant of human hepatitis E virus in Hungary

Enteric virus contamination of foods through industrial practices: a primer on intervention strategies

An ultracentrifugation-based approach to the detection of hepatitis A virus in soft fruits

Perspectives on rapid elimination and ultimate global eradication of paralytic poliomyelitis caused by polioviruses

Inactivation of influenza virus by solar radiation

Hepatitis A virus detection in food: current and future prospects

Other foodborne viruses

Outbreak of hepatitis A in two federal states of Germany: bakery products as vehicle of infection

Stability of infectious influenza A viruses at low pH and at elevated temperature

Stability of infectious influenza A viruses to treatment at low pH and heating

Acid stability of hepatitis A virus

An experimental study on the epidemiology of enteroviruses: water and soap washing of poliovirus 1 -contaminated hands, its effectiveness and kinetics

The ratio of physical particles per infectious unit observed for poliomyelitis viruses

Rapid and quantitative detection of hepatitis A virus from green onion and strawberry rinses by use of real-time reverse transcription-PCR

Worldwide epidemiology of hepatitis A virus infection

Molecular confirmation of oysters as the vector for hepatitis A in a 2005 multistate outbreak

Interspecies transmission of influenza viruses: H5N1 virus and a Hong Kong SAR perspective

Hepatitis E virus infection among animals in northern India: an unlikely source of human disease

Stability of hepatitis A virus

Degradation of the poliovirus 1 genome by chlorine dioxide

Lessons learned from Asian H5N1 outbreak control

Epidemiological considerations on age distribution of paralytic poliomyelitis

Rare transmission mode of FSME (tick-borne encephalitis) by goat's milk

Hepatitis E infection in the UK

Occurrence and persistence of bacterial and viral faecal indicators in wastewater biofilms

Development of a simple method for concentrating enteroviruses from oysters

A serological study of intrafamilial spread from patients with sporadic hepatitis E virus infection

Methods for recovering poliovirus and rotavirus from oysters

Sources of infection among persons with acute hepatitis A and no identified risk factors during a sustained community-wide outbreak

Changing travel-related global epidemiology of hepatitis A

Effect of relative humidity on preharvest survival of bacterial and viral pathogens on the surface of cantaloupe, lettuce, and bell peppers

Overview of the WHO Global Influenza Programme

Septage treatments to reduce the numbers of bacteria and polioviruses

Thermal inactivation of poliovirus type 1 in water, milk and yoghurt

The effect of various disinfectants on detection of avian influenza virus by real time RT-PCR

Method for recovery of viruses from milk and milk products

Microassay for measuring thermal inactivation of H5N1 high pathogenicity avian influenza virus in naturally infected chicken meat

Occupational and consumer risks from avian influenza viruses

Heat inactivation of avian influenza and Newcastle disease viruses in egg products

Hepatitis E virus (HEV): molecular cloning and sequencing of the full-length viral genome

Development and evaluation of an efficient cell-culture system for Hepatitis E virus

Evaluation of electrochemically generated ozone for the disinfection of water and wastewater

Zoonotic transmission of hepatitis E virus from deer to human beings

Outbreak of food-borne infection with hepatitis A virus

Hepatitis E indigenous to economically developed countries: to what extent a zoonosis?

The two clinico-epidemiological forms of hepatitis E

Resistance of surface-dried virus to common disinfection procedures

Thermal inactivation of H5N1 high pathogenicity avian influenza virus in naturally infected chicken meat

Persistence of poliovirus 1 in soil and on vegetables grown in soil previously flooded with inoculated sewage sludge or effluent

Outbreaks where food workers have been implicated in the spread of foodborne disease. Part 2. Description of outbreaks by size, severity, and settings

Outbreaks where food workers have been implicated in the spread of foodborne disease. Part 3. Factors contributing to outbreaks and description of outbreak categories

Reverse transcriptase PCR detection of astrovirus, hepatitis A virus, and poliovirus in experimentally contaminated mussels: comparison of several extraction and concentration methods

Concentration of Norovirus Genogroups I and II from Contaminated Oysters and their Detection Using the Reverse-Transcription Polymerase Chain Reaction, Ottawa, Health Canada

Comparison of hepatitis A and E virus infections among healthy children in Mongolia: evidence for infection with a subgenotype IA HAV in children

Hepatitis E virus sequences in swine related to sequences in humans

The virucidal spectrum of a high concentration alcohol mixture

Avian and swine influenza viruses: our current understanding of the zoonotic risk

Hepatitis E virus: a review

Epidemic transmission of enterically transmitted non-A, non-B hepatitis in Mexico

Molecular detection of hepatitis A virus in urban sewage in Rio de Janeiro, Brazil

Hepatitis E is a cause of unexplained hepatitis in The Netherlands

Severe acute respiratory syndrome

Excretion and detection of SARS coronavirus and its nucleic acid from digestive system

Incidence of hepatitis A in the United States in the era of vaccination

The effect of blood on the antiviral activity of sodium hypochlorite, a phenolic, and a quaternary ammonium compound

An outbreak of hepatitis A associated with green onions

Outbreak of tick-borne encephalitis, presumably milk-borne

Meeting of National Influenza Centres -Western Pacific and South-East Asia regions

Stopping poliovirus vaccination after eradication: issues and challenges

Vaccination for the paediatrician

Virus persistence in groundwater

Sporadic acute or fulminant hepatitis E in Hokkaido, Japan, may be foodborne, as suggested by the presence of hepatitis E virus in pig liver as food

Enterovirus inactivation in soil

Polioviruses, coxsackieviruses, and echoviruses comparison of the genomes by RNA hybridization

Hepatitis E in The Netherlands: imported and endemic

Acidic pH enhances structure and structural stability of the capsid protein of hepatitis E virus

Severe acute respiratory syndrome and its lesions in digestive system