An introduction to food- and waterborne viral disease

1 An introduction to food- and waterborne viral disease N. Cook, Food and Environment Research Agency, UK and G. P. Richards, Delaware State University, USA

DOI: 10.1533/9780857098870.1.3 Abstract: Enteric viruses are the principal cause of food- and waterborne illnesses throughout the world. Among the enteric viruses are the noroviruses, sapovirus, hepatitis A and E viruses, Aichi virus, enteric adenoviruses, rotaviruses, and astroviruses. This chapter introduces the reader to food- and waterborne viruses including the diseases they cause, modes of transmission including potential zoonotic spread, documented outbreaks, implicated foods, virus detection methods, and control strategies. Key words: virus, food and water, disease transmission, outbreaks, detection and control.

1.1

Introduction to enteric viruses

Viral diseases have plagued mankind since before the dawn of civilization. Only in the past century have technological advances led to a characterization of the etiological agents and their epidemiology. Today, the significance of food- and waterborne viral illnesses throughout the world remains underestimated in large part, because of the difficulties in amassing accurate incidence data for outbreaks. In some cases, enteric viruses cause short-term illness or asymptomatic infection, while in other cases these viruses produce high mortalities. The most common enteric viruses from the standpoint of number of cases are human calicivirus species, particularly human norovirus. Currently, human caliciviruses are divided into two groups, the noroviruses and the sapoviruses. The incubation period for norovirus is 10–51 h (Dolin et al., 1982; Green et al.,

Published by Woodhead Publishing Limited, 2013

4

Viruses in food and water

2001; Wyatt et al., 1974), and symptoms range from mild to severe diarrhea, vomiting, and dehydration. Symptoms generally last for 24−48 h. Viruses may persist in stool for 1−2 weeks and can be detected in asymptomatic carriers (Graham et al., 1994; Richards et al., 2004; White et al., 1996). The existence of norovirus genogroups and strains having animal hosts raises the possibility of zoonotic transmission (Mattison et al., 2007), and surveillance of circulating noroviruses in the human population has revealed the presence of several uncommon genotypes, which may represent zoonotic strains (Verhoef et al., 2010); however zoonotic transmission has not been proven in any case. Sapovirus causes diarrhea and vomiting similar to norovirus, generally more often in young children than in adults; however, less is known about the incubation period for sapovirus or the duration of fecal shedding. Sapovirus can be present in pigs, but the strains are not genetically similar to those which infect humans (Reuter et al., 2010), and zoonotic transmission is unknown. Hepatitis A and hepatitis E viruses are both transmitted by food and water. Hepatitis A virus, a member of the Picornaviridae family, is a formidable pathogen capable of eliciting liver disease and death, although in most cases, the illness may go unnoticed and without apparent sequellae. The incubation period is 15–45 days and viral shedding may occur for months. Symptoms may include nausea, vomiting, anorexia (loss of appetite), fatigue, and fever. Hepatitis A virus infects the liver, leading to possible pain in the upper right quadrant, jaundice of the eyes or skin, and dark urine. The illness is potentially lethal, particularly in individuals with pre-existing liver disease. Hepatitis A virus is found only in humans and some simians, and no zoonotic transmission is known to occur. Hepatitis E virus, on the other hand, has four genotypes. Genotypes 1 and 2 are associated with human illness, while genotypes 3 and 4 are animal strains which are occasionally transferred to humans. For instance, genotypes 3 and 4 have been shown to spread zoonotically from pigs and deer to humans (Aggarwal and Naik, 2009). Hepatitis E virus is the sole member of the Hepeviridae family. Like hepatitis A virus it infects the liver and its symptoms are similar; however, it causes a higher incidence of death, particularly among pregnant woman where the death rate approaches 25% (Mast and Krawczynski, 1996), possibly from hormonal differences or other factors (Navaneethan et al., 2008). The incubation period of hepatitis E virus ranges between 2 and 8 weeks, and may be dependent on the virus dose (Anderson and Shrestha, 2002; Li et al., 1994; Tsarev et al., 1994). Rotavirus is a major pathogen causing infantile diarrhea. It is responsible for an estimated 800 000 deaths annually (Parashar et al., 1998), mostly in developing countries where rehydration therapy is not available. The incubation period for rotavirus is variable, from 11 h to 6 days and symptoms include diarrhea, anorexia, dehydration, depression, and occasional vomiting (Bishop, 1994; Kapikian and Chanock, 1990; Saif et al., 1994). Virus shedding in feces was shown to last for up to 57 days (Richardson et al., 1998) and longer in children with immunodeficiencies (Saulsbury et al., 1980). Rotaviruses are generally species-specific, but cross-species transmission is possible, and

Published by Woodhead Publishing Limited, 2013

An introduction to food- and waterborne viral disease

5

low level input of rotavirus strains or sequences into the human population from the animal population may be common. Food- or waterborne zoonotic transmission is a possibility (Cook et al., 2004). Among the many serotypes of adenovirus, types 40 and 41 are the typical enteric forms capable of eliciting food- and waterborne illness. Most enteric adenovirus cases are mild and transient except in immunocompromised individuals. Acute adenovirus gastroenteritis is characterized by watery diarrhea possibly containing mucus, fever, vomiting, abdominal pain and dehydration and may be accompanied by respiratory illness (Ruuskanen et al., 2002). Adenovirus strains with genetic similarity to human adenovirus have been found in non-human primates, raising the possibility of zoonotic transmission through the consumption of primate meat (Wevers et al., 2011). Other adenovirus serotypes are believed to be predominantly respiratory organisms. Adenovirus infection at an early age imparts long-term immunity against the particular serotype. Astroviruses cause mild and usually self-limiting illness, often in children. Symptoms include vomiting and diarrhea, and occasional fever, abdominal pain, and anorexia. Astrovirus has an incubation period generally between 24 and 96-h lasting for up to four days in most patients with fecal shedding for a week; however, immunocompromised and malnourished individuals are at greater risk of more severe symptoms and death from dehydration, and can shed viruses in their stools for up to a month. No zoonotic transmission of astrovirus has been observed, although the level of similarity between some human and animal strains suggests that it may be possible (Kapoor et al., 2009). Two other viral agents responsible for foodborne illness are Aichi virus (a picornavirus) and tick-borne encephalitis virus (a flavivirus). Aichi virus causes acute gastroenteritis in humans with symptoms including diarrhea, abdominal pain, vomiting, nausea, and fever (Yamashita et al., 1991, 2001). Viruses with similarity to Aichi virus can be found in some livestock species (Reuter et al., 2011), but zoonotic transmission has not been recorded. Tick-borne encephalitis virus is most commonly transmitted directly via bites; however, the disease can also be transmitted indirectly via the gastrointestinal route by consumption of unpasteurized milk products and infected dairy animals (Dumpis et al., 1999; Kriz et al., 2009).

1.2

Food and water as vehicles of virus transmission

Water represents an important vehicle for the transmission of enteric viruses. Rivers, lakes, streams, and coastal waters are regularly contaminated by septic tanks, storm water runoff, and effluents from inefficiently operated sewage treatment plants or from overflows from treatment plants impacted by flooding events. Swimmers at bathing beaches also contribute to some level of viral contamination of the water. When contaminated waters are directly used

Published by Woodhead Publishing Limited, 2013

6

Viruses in food and water

for drinking purposes, they represent a significant hazard to the consumer. Likewise, when such waters are used for the irrigation of crops, the processing of foods, or the production of ice, virus transfer to foods and beverages, and ultimately to humans, can occur. Food may also become contaminated directly by the unsanitized hands of harvesters in the farm fields, truckers, processors, and those who prepare and serve foods in restaurants and at home. Fecally polluted marine waters may also lead to the contamination of oysters, clams, mussels, and cockles, which represent a significant cause of illness to those who consume raw or undercooked shellfish. This is in large part due to the ability of bivalve mollusks to concentrate and retain viruses from the water column within their edible tissues as a normal part of their filter feeding abilities. Virus levels within the shellfish can increase at least 100-fold over the concentrations in the water. Berry fruits and leafy green vegetables are also common vehicles for virus transmission, particularly when they are consumed raw. Thorough washing of the surfaces of produce is a useful intervention to reduce virus levels, but some foods, such as raspberries, strawberries, and crinkly lettuce, are difficult to thoroughly wash. Foods that are extensively handled are more likely to become contaminated. A case in point is doughnuts which are often handled while frostings are applied or fillings are injected. Alternatively even foods that are cooked can become vehicles for transmission, if they subsequently come into contact with contaminated foods or surfaces: for example, a hamburger may become contaminated by the bun (if it was handled by a person with contaminated hands), or the lettuce, tomato, or onion toppings if they were previously contaminated during production or preparation. Likewise, ill food workers may contaminate food processing equipment, contact surfaces, or foods directly by feces or vomit. Aerosols from vomiting can be transmitted long distances.

1.3

Outbreaks of food- and waterborne viral illness

Enteric viral illnesses often go unrecognized or unreported for several reasons. In some cases, the symptoms are mild enough that no medical intervention is required. In other instances, as in the case of norovirus gastroenteritis, severe diarrhea and projectile vomiting deters patients from traveling to the doctor’s office until symptoms resolve, but by then, remission of symptoms is rapid and a doctor may no longer be needed. Some situations preclude a visit to the doctor because of a lack of health insurance, inability to pay, or the inaccessibility of a medical center. In cases where the sick do seek medical treatment, the cause of the illness may not be readily discerned and treatment options are often based on their symptoms. In many locations, viral diseases are not reportable and there is little or no tracking of illnesses or outbreaks. Testing for specific etiological agents of viral illness is difficult, time-consuming, costly and seldom performed, except when larger outbreaks occur. In such cases, epidemiological traceback to food or water is possible.

Published by Woodhead Publishing Limited, 2013

An introduction to food- and waterborne viral disease

7

Sporadic publications are the only way to document many of these outbreaks. Below are some such outbreaks reported for various food commodities.

1.3.1 Produce A wide variety of fruits and vegetables have been associated with outbreaks of hepatitis A and norovirus illness. Such produce is generally consumed raw or after minimal processing, and any contaminating viruses can remain in an infectious state up to the point of consumption. Outbreaks of hepatitis A have been linked with tomatoes (Petrignani et al., 2010), green onions (Centers for Disease Control and Prevention, 2003; Dentinger et al., 2001; Wheeler et al., 2005), raspberries (Ramsay and Upton, 1989; Reid and Robinson, 1987), strawberries (Niu et al., 1992), blueberries (Calder et al., 2003), fruit juices (Frank et al., 2007), and other produce. Norovirus was responsible for major outbreaks from celery (Warner, 1992; Warner et al., 1991), fruits and berries including fresh and frozen raspberries (Cotterelle et al., 2005; Hjertqvist et al., 2006), lettuce (Alexander et al., 1986; Ethelberg et al., 2010), coleslaw and green leaf salad (Zomer et al., 2009); radishes (Yu et al., 2010), cantaloupe (Bowen et al., 2006), pumpkin salad (Götz et al., 2002), and tropical fruits and juices (Straun et al., 2011; Visser et al., 2010). Other viruses, for example rotavirus, undoubtedly contribute to produce-associated illness, but are not fully recognized because the product is not routinely tested or because cases of illness occur sporadically rather than in large outbreaks. Contamination of fruits and vegetables may occur through fertilization of crops with sewage sludge, irrigation with wastewater, harvesting and handling with unsanitized hands, rinsing with contaminated water, and cross-contamination during preparation (Richards, 2001).

1.3.2 Shellfish Molluscan shellfish can become readily contaminated with enteric viruses and have been associated with some of the largest outbreaks on record. Contaminated clams were reportedly responsible for 293 000 cases of hepatitis A in China (Halliday et al., 1991). Other outbreaks of shellfish-associated hepatitis A have been noted worldwide (Conaty et al., 2000; Guillois-Bécel et al., 2009; Pintó et al., 2009; Richards, 1985) and are currently problematic in some regions of the world. Norovirus remains a common cause of shellfish-associated illness and is credited with widespread outbreaks (Berg et al., 2000; Simmons et al., 2001; Webby et al., 2007; Westrell et al., 2010). In 1983, the United States had multiple shellfish-associated norovirus outbreaks affecting over 2000 shellfish consumers in New York and New Jersey, most of which occurred over a 3-month period (Richards, 1985). Shellfish-associated norovirus outbreaks continue to occur around the world. Sapovirus has also been responsible for oyster-related outbreaks (Nakagawa-Okamoto et al., 2009). Hepatitis E virus-contaminated shellfish have been associated with

Published by Woodhead Publishing Limited, 2013

8

Viruses in food and water

several outbreaks (Cacopardo et al., 1997; Said et al., 2009; Tomar, 1998), perhaps because of the ability of shellfish to concentrate viruses within their edible tissues. Adenoviruses are commonly detected in shellfish, but have not led to recognized outbreaks, probably because only some of the serotypes of adenovirus are capable of eliciting gastrointestinal illness, and children, who are most susceptible, are not frequent consumers of raw shellfish (Lees, 2000). Astrovirus, Aichi virus, and rotavirus have also led to outbreaks of shellfish-borne illness (Ambert-Balay et al., 2008; Le Guyader et al., 2008; Yamashita et al., 2000). Although thorough cooking inactivates enteric viruses, the incidence of shellfish-borne viral illness is high, in large part because many consumers prefer their shellfish raw or only lightly cooked.

1.3.3 Bakery products Large outbreaks of norovirus have been associated with bakery products. An outbreak affecting 2700 guests at 46 weddings was attributed to the contamination of wedding cakes handled by two ill workers at one bakery (Friedman et al., 2005). In a similar event, an estimated 3000 individuals developed norovirus after eating frosted cake prepared by an ill worker (Kuritsky et al., 1984). Rolls prepared by an ill baker led to 231 illnesses at a lunch buffet (de Wit et al., 2007). Outbreaks of hepatitis A have also been attributed to bakery products when frostings and glazes were contaminated by ill workers (Schoenbaum et al., 1976; Weltman et al., 1996). Filled doughnuts and other pastries were associated with outbreaks where two employees were diagnosed with hepatitis A (Schenkel et al., 2006). Although pastries may be cooked and cooking inactivates enteric viruses, contamination after cooking poses a threat of enteric virus illness.

1.3.4 Meats and dairy products Chicken, pork, and beef products have been associated with norovirus illness, usually as a result of contamination after cooking (Vivancos et al., 2009; Zomer et al., 2010). Delicatessen meats were linked to an outbreak of norovirus (Malek et al., 2009) and hepatitis A (Gustafson et al., 1983; Schmid et al., 2009). Cheese was also related to a norovirus outbreak (Vivancos et al., 2009) and to hepatitis A (Gustafson et al., 1983). Transmission has been associated with product handling by an ill worker. Hepatitis A has been associated with milk consumption (Murphy et al., 1946; Raska et al., 1966). Milk and cheeses are also vectors for tick-borne encephalitis, often from sheep and goat milk from Europe and Asia where tick-borne encephalitis is endemic (Bogovic et al., 2010; Gresikova et al., 1975; Holzmann et al., 2009; Kerbo et al., 2005). Although the transmission of rotavirus illness was linked to tuna and chicken salad (Centers for Disease Control and Prevention, 2000), relatively few cases of foodborne rotavirus diarrhea have been reported.

Published by Woodhead Publishing Limited, 2013

An introduction to food- and waterborne viral disease

9

1.3.5 Water Contaminated drinking water is likely responsible for the majority of cases of enteric virus illness. One report indicates that an estimated 60% of the norovirus illnesses in the United States are from contaminated water (Mead et al., 1999). Noroviruses have been listed as the primary cause of waterborne illness worldwide (Leclerc et al., 2002). Waterborne rotavirus infections are responsible for significant morbidity and mortality, particularly in children (Divizia et al. 2004; Glass et al., 2001; Villena et al., 2003). Both rotavirus and caliciviruses were detected in 40% of the sick individuals during a waterborne outbreak involving sewage-contaminated drinking water (Räsänen et al., 2010). Occasional waterborne outbreaks of hepatitis E have been documented (Corwin et al., 1996; Naik et al., 1992; Rab et al., 1997). Astrovirus has been associated with outbreaks of gastroenteritis from contaminated drinking water (Gofti-Laroche et al., 2003; Kukkula et al., 1997); however, in 89 outbreaks of waterborne illness affecting 4321 people in England and Wales, astrovirus was associated with only 1% of the outbreaks (Smith et al., 2006). The transmission of most enteric viruses via water and foods is not fully recognized due to poor detection efforts and inadequate reporting practices. In addition to the foodborne route of transmission, viral disease can also be acquired through environmental exposure. Viruses such as norovirus and adenovirus may be highly prevalent in sewage-polluted recreational waters (Wyn-Jones et al., 2011), and enteric viruses have frequently been implicated in disease outbreaks or cases linked to swimming, canoeing, etc. (Sinclair et al., 2009).

1.4

Virus detection

Virus screening of various food products and water is seldom performed because of the cost and difficulty in conducting the assays. Detection of foodborne viruses is challenging and requires the use of complex methods. These methods are composed of sample treatment and assay stages. Sample treatment is a multi-step process aimed at removing viruses from a food sample and concentrating them for delivery to the assay, principally nucleic acid amplification by PCR. Methods are improving and some protocols are available for extracting, concentrating, and analyzing viruses from shellfish, meat, and some ready-to-eat foods (Richards et al., in press). Currently, a group (CEN TC 275/WG6/TAG4) set up by the Committee for European Standardization is developing methods to detect norovirus and hepatitis A virus in salad vegetables, shellfish, and soft fruit (Lees and CEN WG6 TAG4, 2010). Publication of these international standards is scheduled for 2013. Methods are also becoming available to test for viruses in the rinse from fruits and vegetables (Richards et al., in press). Extracts and rinses often contain substances

Published by Woodhead Publishing Limited, 2013

10 Viruses in food and water inhibitory to the molecular methods used to identify the presence of viruses, namely real-time reverse transcription polymerase chain reaction (RT-PCR); therefore, numerous controls must be included to ensure the effectiveness of the extraction process and the validity of the assay (D’Agostino et al., 2011). Such methods are most often employed in response to a suspected food- or waterborne outbreak to facilitate an epidemiological investigation of the incident. Virus extraction and analysis is generally labor-intensive, requires the use of expensive equipment and reagents, and demands a qualified technician to perform such procedures; therefore, viral assays are not performed routinely on any food product. A potential breakthrough was recently published showing that many enteric viruses may become sequestered within the shellfish hemocytes and that extracting and testing the hemocytes for viruses may offer a simpler approach for virus detection from live shellfish (Provost et al., 2011). The use of hemocytes alone may simplify the separation and concentration of viruses from shellfish, since hemocytes may be a source of already concentrated viruses. If the hemocytes contain the majority of viruses, then testing just the digestive tissues would likely miss the majority of the viral contaminants. The evaluation of infectivity of viruses is problematic, particularly using molecular diagnostic techniques (Richards, 1999). The salient issue therefore is whether viruses detected by molecular assay are actually infectious (Cliver, 2009). A recent study has demonstrated a potential breakthrough in that human noroviruses that are likely to be infectious bind to porcine mucin, whereas noroviruses that have been inactivated by heat, UV irradiation, and high pressure processing appear not to bind to mucin (Dancho et al., 2012). Thus, binding of NoV to mucin followed by RT-PCR testing may lead the way to better identifying and quantifying infectious NoV.

1.5

Control of virus contamination of food and water

Both physical (e.g., disinfection) and procedural (e.g., compliance with guidelines and regulations) measures can assist in reducing the potential for transmission of viruses via food and water. Currently, most treatment of drinking water or water for use in food production is performed by chlorination, and the effectiveness of this treatment is borne out by the evidence that outbreaks of disease due to contaminated drinking water generally only occur when the water treatment or distribution system has failed, for example, a breach in a water pipe allowing the ingress of sewage. In most countries, the effectiveness of potable water treatment is generally evaluated by determining the presence of coliform bacteria in compliance with national regulations. This is also the case for recreational waters or waters used in shellfish production. Since the presence of coliform bacteria has not

Published by Woodhead Publishing Limited, 2013

An introduction to food- and waterborne viral disease 11 been proven to consistently or reliably correlate with the presence of enteric viruses, the consideration of adoption of virus standards has been recommended (Wyn-Jones et al., 2011). As discussed above, the foodstuffs most at risk of being vehicles for the transmission of viral disease are those which are eaten raw or after only minimal processing. Consequently, they are seldom if ever subject to thorough disinfection. The effect of processes which are currently used in the food industry may not be sufficient to eliminate all infectious viruses which may contaminate the treated foodstuff (Koopmans and Duizer, 2004). The most reliable control of foodborne viral contamination will therefore be to prevent the contamination from occurring in the first place, and this should be achieved by effective guidelines made available to the food industry. Over the past decade, the role of viruses as the most prevalent agents of foodborne disease has become widely recognized, and consequently, there are current international efforts aimed at tackling the problem of contamination of foods by pathogenic viruses by provision of formal guidance. For instance, the Codex Alimentarius Commission Committee on Food Hygiene has developed guidelines on the control of viruses in food (Codex Alimentarius Commission, 2011). The European Framework 7 research project ‘Integrated monitoring and control of foodborne viruses in European food supply chains’ has produced basic guidance sheets on prevention of virus contamination of berry fruits, leafy greens, and pork products (available at http://www.eurovital.org/ GuidanceSheets1.htm). These are intended to complement the Codex guidelines and be used in concordance with them. In conclusion, enteric viruses transmitted by food and water pose significant challenges to public health globally. These challenges will be met by ongoing research into the mechanisms and conditions underlying how viruses contaminate food and environmental matrices, which should ultimately allow the determination of means to break the route of transmission from source to target. Research on enteric virus inactivation processes will also lead to the development of enhanced processing strategies to reduce viral contaminants in the food industry. In the subsequent sections and chapters of this book, extensive details will be provided on key aspects of virus contamination of food and waters, such as the prevalence, persistence, detection, and control of these pathogens, and issues which may become significant in the future will be discussed. This information will provide a comprehensive and current overview of the challenges of food- and waterborne viruses.

1.6

References

and NAIK S (2009), Epidemiology of hepatitis E: current status. J Gastroenterol Hepatol, 24, 1484–1493.

AGGARWAL R

Published by Woodhead Publishing Limited, 2013

12 Viruses in food and water ALEXANDER W J, HOLMES J R, SHAW J F, RILEY W E

and ROPER W L (1986), Norwalk virus outbreak at a college campus. South Med J, 79, 33–36, 40. AMBERT-BALAY K, LORROT M, BON F, GIRAUDON H, KAPLON J, WOLFER M, LEBON P, GENDREL D and POTHIER P (2008), Prevalence and genetic diversity of Aichi virus strains in stool samples from community and hospitalized patients. J Clin Microbiol, 46, 1252–1258. ANDERSON D A and SHRESTHA I I (2002), Hepatitis E virus. In: Clinical Virology, 2nd ed., D D RICHMAN, R J WHITNEY and F G HAYDEN eds, ASM Press, Washington, DC, pp. 1061–1074. BERG D E, KOHN M A, FARLEY T A and MCFARLAND L M (2000), Multi-state outbreak of acute gastroenteritis traced to fecal-contaminated oysters harvested in Louisiana. J Infect Dis, 181(Suppl 2), S381–S386. BISHOP R F (1994), Natural history of rotavirus infections. In: Viral Infections of the Gastrointestinal Tract. 2nd ed., A Z KAPIKIAN ed., MARCEL DEKKER, New York. pp. 131–167. BOGOVIC P, LOTRIC-FURLAN S and STRLE F (2010), What tick-borne encephalitis may look like: clinical signs and symptoms. Travel Med Infect Dis, 8, 246–250. BOWEN A, FRY A, RICHARDS G and BEUCHAT L (2006), Infections associated with cantaloupe consumption: a public health concern. Epidemiol Infect, 134, 675–685. CACOPARDO B, RUSSO R, PREISER W, BENANTI F, BRANCATI G and NUNNARI A (1997), Acute hepatitis E in Catania (eastern Sicily) 1980–1994. The role of hepatitis E virus. Infection, 25, 313–316. CALDER L, SIMMONS G, THORNLEY C, TAYLOR P, PRITCHARD K, GREENING G and BISHOP J (2003), An outbreak of hepatitis A associated with consumption of raw blueberries. Epidemiol Infect, 131, 745–751. CENTERS FOR DISEASE CONTROL and PREVENTION (2000), Foodborne outbreak of Group A rotavirus gastroenteritis among college students – District of Columbia, March-April 2000. MMWR Morb Mort Wkly Rep, 49, 1131–1133. CENTERS FOR DISEASE CONTROL and PREVENTION (2003), Hepatitis A outbreak associated with green onions at a restaurant – Monaca, Pennsylvania, 2003. MMWR Morb Mortal Wkly Rep, 52, 1155–1157. CLIVER DO (2009), Capsid and infectivity in virus detection. Food Environ Virol, 1, 123–128. Codex Alimentarius Commission (2011). Report of the Forty-Third Session of The Codex Committee on Food Hygiene, Miami, USA, 5–9 December 2011. FAO/WHO, Geneva. CONATY S, BIRD P, BELL G, KRAA E, GROHMANN G and MCANULTY J M (2000), Hepatitis A in New South Wales, Australia from consumption of oysters: the first reported outbreak. Epidemiol Infect, 124, 121–130. COOK N, BRIDGER J, KENDALL K, ITURRIZA-GÓMARA M, EL-ATTAR L and GRAY J (2004), The zoonotic potential of rotavirus. J Inf, 48, 289–302. CORWIN A L, KHIEM H B, CLAYSON E T, PHAM K S, VO T T, VU T Y, CAO T T, VAUGHN D, MERVEN J, RICHIE T L, PUTRI M P, HE J, GRAHAM R, WIGNALL F S and HYAMS K C (1996), A waterborne outbreak of hepatitis E virus transmission in Southwestern Vietnam. Am J Trop Med Hyg, 54, 559–562. COTTERELLE B, DROUGARD C, ROLLAND J, BECAMEL M, BOUDON M, PINEDE S, TRAORÉ O, BALAY K, POTHIER P and ESPIÉ E (2005), Outbreak of norovirus infection associated with the consumption of frozen raspberries, France, March 2005. Euro Surveill, 10, E050428 050421. D’AGOSTINO M, COOK N, RODRIGUEZ-LAZARO D and RUTJES S (2011), Nucleic acid amplification-based methods for detection of enteric viruses: definition of controls and interpretation of results. Food Environ Virol, 2, 55–60.

Published by Woodhead Publishing Limited, 2013

An introduction to food- and waterborne viral disease 13 DANCHO B A, CHEN H

and KINGSLEY D H (2012), Discrimination between infectious and non-infectious human norovirus using porcine gastric mucin. Int J Food Microbiol, 155, 222–226. DE WIT M A, WIDDOWSON M A, VENNEMA H, de BRUIN E, FERNANDEZ T and KOOPMANS M (2007), Large outbreak of nrovirus: the baker who should have known better. J Infect, 55, 188–193. DENTINGER C M, BOWER W A, NAINAN O V, COTTER S M, MYERS G, DUBUSKY L M, FLOWER S, SALEHI E D and BELL B P (2001), An outbreak of hepatitis A associated with green onions. J Infect Dis, 183, 1273–1276. DIVIZIA M, GABRIELI R, DONIA D, MACALUSO A, BOSCH A, GUIX S, SÁNCHEZ G, VILLENA C, PINTÓ R M, PALOMBI L, BUONUOMO E, CENKO F, LENO L, BEBECI D and BINO S (2004), Waterborne gastroenteritis outbreak in Albania. Water Sci Technol, 50, 57–61. DOLIN R, REICHMAN R C, ROESSNER K D, TRALKA T S, SCHOOLEY R T, GARY W and MORENS D (1982), Detection by immune electron microscopy of the Snow Mountain agent of acute viral gastroenteritis. J Infect Dis, 146, 184–189. DUMPIS U, CROOK D and OKSI J (1999), Tick-borne encephalitis. Clin Infect Dis, 28, 882–890. ETHELBERG S, LISBY M, BOTTIGER B, SCHULTZ A C, VILLIF A, JENSEN T, OLSEN K E, SCHEUTZ F, KJELSO C and MULLER L (2010), Outbreaks of gastroenteritis linked to lettuce, Denmark, January 2010. Euro Surveill 15(6), 19484. FRANK C, WALTER J, MUEHLEN M, JANSEN A, VAN TREECK U, HAURI A M, ZOELLNER, I, RAKHA M, HOEHNE M, HAMOUDA O, SCHREIER E and STARK K (2007), Major outbreak of hepatitis A associated with orange juice among tourists, Egypt, 2004. Emerg Infect Dis, 1, 156–158. FRIEDMAN D S, HEISEY-GROVE D, ARGYROS F, BERL E, NSUBUGA J, STILES T, FONTANA J, BEARD R S, MONROE S, MCGRATH M E, SUTHERBY H, DICKER R C, DEMARIA A and MATYAS B T (2005), An outbreak of norovirus gastroenteritis associated with wedding cakes. Epidemiol Infect, 133, 1057–1063. GLASS R I, BRESEE J, JIANG B, GENTSCH J, ANDO T, FANKHAUSER R, NOEL J, PARASHAR U, ROSEN B and MONROE S S (2001), Gastroenteritis viruses: an overview. Novartis Found Symp, 238, 5–25. GOFTI-LAROCHE L, GRATACAP-CAVALLIER B, DEMANSE D, GENOULAZ O, SEIGNEURIN J M and ZMIROU D (2003), Are waterborne astrovirus implicated in acute digestive morbidity (E. MI. R.A. study)? J Clin Virol, 27, 74–82. GÖTZ H, DE JONG B, LINDBÄCK J, PARMENT P A, HEDLUND K O, TORVÉN M and EKDAHL K (2002), Epidemiological investigation of a foodborne gastroenteritis outbreak caused by Norwalk-like virus in 30 day-care centres. Scand J Infect Dis, 34, 115–121. GRAHAM, D Y, JIANG X, TANAKA T, OPEKUN A R, MADORE H P and ESTES M K (1994), Norwalk virus infection of volunteers: new insights based on improved assays. J Infect Dis, 180, 34–43. GREEN K Y, CHANOCK R M and KAPIKIAN A Z (2001), Human caliciviruses. In: Fields Virology, Vol. 1, D M KNIPE and P M HOWLEY, eds, Lippinscott Williams & Wilkins, Philadelphia, PA. pp. 841–74. GRESIKOVA M, SEKEYOVA M, STÚPALOVA S and NECAS S (1975), Sheep milk-borne epidemic of tick-borne encephalitis in Slovakia. Intervirology, 5, 57–61. GUILLOIS-BÉCEL Y, COUTURIER E, LE SAUX J C, ROQUE-AFONSO A M, LE GUYADER, F S, LE GOAS A, PERNÈS J, LE BECHEC S, BRIAND A, ROBERT C, DUSSAIX E, POMMEPUY M and VAILLANT V (2009), An oyster-associated hepatitis A outbreak in France in 2007. Euro Surveill, 14, 19144. GUSTAFSON T L, HUTCHESON R L JR, FRICKER R S and SCHAFFNER W (1983), An outbreak of foodborne hepatitis A: the value of serological testing and matched case-control analysis. Am J Public Health, 73, 1199–1201.

Published by Woodhead Publishing Limited, 2013

14 Viruses in food and water HALLIDAY L M, KANG L Y, ZHOU T K, HU M D, PAN Q C, FU T Y, HUANG Y S and HU S L (1991),

An epidemic of hepatitis A attributable to the ingestion of raw clams in Shanghai, China. J Infect Dis, 164, 852–859. HJERTQVIST M, JOHANSSON A, SVENSSON N, ABOM P E, MAGNUSSON C, OLSSON M, HEDLUND K O and ANDERSSON Y (2006), Four outbreaks of norovirus gastroenteritis after consuming raspberries, Sweden, June–August 2006. Euro Surveill, 11, E060907 060901. HOLZMANN H, ABERLE S W, STIASNY K, WERNER P, MISCHAK A, ZAINER B, NETZER M, KOPPI S, BECHTER E and HEINZ F X (2009), Tick-borne encephalitis from eating goat cheese in a mountain region of Austria. Emerg Infect Dis, 15, 1671–1673. KAPIKIAN A Z and CHANOCK R M (1990), Rotaviruses. In: Virology, 2nd ed., B N Fields and D M Knipe, eds, Raven Press, New York. pp. 1353–404. KAPOOR A, LI L, VICTORIA J, ODERINDE B, MASON C, PANDEY P, ZAIDI S Z and DELWART E (2009), Multiple novel astrovirus species in human stool. J Gen Virol, 90, 2965–72. KERBO N, DONCHENKO I, KUTSAR K and VASILENKO V (2005), Tick-borne encephalitis in Estonia linked to raw goat milk, May–June 2005. Euro Surveill, 10, E050623 2. KOOPMANS M and DUIZER E (2004), Foodborne viruses: an emerging problem. Int J Food Microbiol, 90, 23–41. KRIZ B, BENES C and DANIEL M (2009), Alimentary transmission of tick-borne encephalitis in the Czech Republic (1997–2008). Epidemiol Mikrobiol Imunol, 58, 98–103. KUKKULA M, ARSTILA P, KLOSSNER M L, MAUNULA L, BONSDORFF C H V and JAATINEN P (1997), Waterborne outbreak of viral gastroenteritis. Scand J Infect Dis, 29, 415–18. KURITSKY J N, OSTERHOLM M T, GREENBERG, H G, KORLATH J A, GODES J R, HEDBERG C W, FORFANG J C, KAPIKIAN A Z, MCCULLOUGH J C and WHITE K E (1984), Norwalk gastroenteritis: a community outbreak associated with bakery product consumption. Ann Intern Med, 100, 519–21. LECLERC H, SCHWARTZBROD L and DEI-CAS E (2002), Microbial agents associated with waterborne diseases. Crit Rev Microbiol, 28, 371–409. LEES D (2000), Viruses and bivalve shellfish. Intl J Food Microbiol, 59, 81–116. LEES D and CEN WG6 TAG4 (2010), International Standardisation of a method for detection of human pathogenic viruses in molluscan shellfish. Food Environ Virol, 2, 146–55. LE GUYADER F S, LE SAUX J C, AMBERT-BALAY K, KROL J, SERAIS O, PARNAUDEAU S, GIRAUDON H, DELMAS G, POMMEPUY M, POTHIER P and ATMAR R L (2008), Aichi virus, norovirus, astrovirus, enterovirus, and rotavirus involved in clinical cases from a French oyster-related gastroenteritis outbreak. J. Clin. Microbiol, 46, 4011–17. LI F, ZHUANG H, KOLIVAS S, LOCARNINI S and ANDERSON D (1994), Persistence and transient antibody responses to hepatitis E virus detected by Western immunoblot using open reading frame 2 and 3 and glutathione S-transferase fusion proteins. J Clin Microbiol, 32, 2060–6. MALEK M, BARZILAY E, KRAMER A, CAMP B, JAYKUS L A, ESCUDERO-ABARCA B, DERRICK G, WHITE P, GERBA C, HIGGINS C, VINJE J, GLASS R, LYNCH M and WIDDOWSON M A (2009), Outbreak of norovirus infection among river rafters associated with packaged delicatessen meat, Grand Canyon, 2005. Clin Infect Dis, 48, 31–7. MAST E E and KRAWCZYNSKI K (1996), Hepatitis E: an overview. Annu Rev Med, 47, 257–266. MATTISON K, SHUKLA A, COOK A, POLLARI F, FRIENDSHIP R, KELTON D, BIDAWID S and FARBER J M (2007), Human noroviruses in swine and cattle. Emerg Inf Dis, 13, 1184–8. MEAD P S, SLUTSKER L, DIETZ V, MCCAIG L F, BRESEE J S, SHAPIRO C, GRIFFIN P M and TAUXE R V (1999), Food-related illness and death in the United States. Emerg Infect Dis, 5, 607–25.

Published by Woodhead Publishing Limited, 2013

An introduction to food- and waterborne viral disease 15 MURPHY W J, PETRIE L M

and WORK S D (1946), Outbreak of infectious hepatitis, apparently milk-borne. Am J Public Health Nations Health, 36, 169–73. NAIK S R, AGGARWAL R, SALUNKE P N and MEHROTRA N N (1992), A large waterborne hepatitis E epidemic in Kanpur, India. Bull World Health Organ, 70, 597–604. NAKAGAWA-OKAMOTO R, ARITA-NISHIDA T, TODA S, KATO H, IWATA H, AKIYAMA M, NISHIO O, KIMURA H, NODA M, TAKEDA N and OKA T (2009), Detection of multiple sapovirus genotypes and genogroups in oyster-associated outbreaks. Jpn J Infect Dis, 62, 63–6. NAVANEETHAN U, Al MOHAJER M, and SHATA M T (2008), Hepatitis E and pregnancy: understanding the pathogenesis. Liver Int, 28, 1190–9. NIU M T, POLISH L B, ROBERTSON B H, KHANNA B K, WOODRUFF B A, SHAPIRO C N, MILLER M A, SMITH J D, GEDROSE J K, ALTER M J and MARGLIS H S (1992), Multistate outbreak of hepatitis A associated with frozen strawberries. J Infect Dis, 166, 518–24. PARASHAR U D, BRESSE J S, GENTSCH J R and GLASS R I (1998). Rotavirus. Emerg Infect Dis, 4, 561–70. PETRIGNANI M, HARMS M, VERHOEF L, VAN HUNEN R, SWAAN C, VAN STEENBERGEN J, BOXMAN I, PERAN I SALA R, OBER H, VENNEMA H, KOOPMANS M and VAN PELT W (2010), Update: a foodborne outbreak of hepatitis A in the Netherlands related to semi-dried tomatoes in oil, January-February 2010. Euro Surveill, 15(20), 19572. PINTÓ R M, COSTAFREDA M I and BOSCH A (2009), Risk assessment in shellfish-borne outbreaks of hepatitis A. Appl Environ Microbiol, 75, 7350–5. PROVOST K, DANCHO B A, OZBAY G, ANDERSON R S, RICHARDS G P and KINGSLEY D K (2011), Hemocytes are sites of enteric virus persistence within oysters. Appl Environ Microbiol, 77, 8360–9. RAB M A, BILE M K, MUBARIK M M, ASGHAR H, SAMI Z, SIDDIQI S, DIL A S, BARZGAR M A, CHAUDHRY M A and BURNEY M I (1997), Waterborne hepatitis E virus epidemic in Islamabad, Pakistan: a common source outbreak traced to malfunction of a modern treatment plant. Am J Trop Med Hyg, 57, 151–7. RAMSAY C N and UPTON P A (1989), Hepatitis A and frozen raspberries. Lancet, 1, 43–4. RÄSÄNEN S, LAPPALAINEN S, KAIKKONEN S, HÄMÄLÄINEN M, SALMINEN M and VESIKARI T (2010). Mixed viral infections causing acute gastroenteritis in children in a waterborne outbreak. Epidemiol Infect, 138, 1227–34. RASKA K, HELCL J, JEZEK J, KUBELKA Z, LITOV M, NOVÁK K, RADKOVSKÝ J, SERÝ V, ZEJDL J and ZIKMUND V (1966), A milk-borne infectious hepatitis epidemic. J Hyg Epidemiol Microbiol Immunol, 10, 413–28. REID T M and ROBINSON H G (1987), Frozen raspberries and hepatitis A. Epidemiol Infect, 98, 109–12. REUTER G, BOROS A and PANKOVICS P (2011), Kobuviruses – a comprehensive review. Rev Med Virol, 21, 32–41. REUTER G, ZIMSEK-MIJOVSKI J, POLJSAK-PRIJATELJ M, DI BARTOLO I, RUGGERI F M, KANTALA T, MAUNULA L, KISS I, KECSKEMETI S, HALAIHEL N, BUESA J, JOHNSEN C, HJULSAGER C K, LARSEN L E, KOOPMANS M and BOTTIGER B (2010), Incidence, diversity, and molecular epidemiology of sapoviruses in swine across Europe. J Clin Microbiol, 48, 363–8. RICHARDS G P (1985), Outbreaks of shellfish-associated enteric virus illness in the United States: requisite for development of viral guidelines. J Food Prot, 48, 815–23. RICHARDS G P (1999), Limitations of molecular biological techniques for assessing the virological safety of foods. J Food Prot, 62, 691–7. RICHARDS G P (2001), Enteric virus contamination of foods through industrial practices: a primer on intervention strategies. J Indust Microbiol Biotechnol, 27, 117–25.

Published by Woodhead Publishing Limited, 2013

16 Viruses in food and water RICHARDS G P, CLIVER D O

and GREENING G E (in press), Food-borne viruses, In: Compendium of Methods for the Microbiological Examination of Foods, American Public Health Association, Washington, DC. RICHARDS G P, WATSON M A and KINGSLEY D H (2004), A SYBR green real-time RT-PCR method to detect and quantitate Norwalk virus in stools. J Virol Method, 116, 63–70. RUUSKANEN O, MEURMAN O and AKUSJÄRVI G (2002), Adenoviruses. In: Clinical Virology, 2nd ed., D D RICHMAN, R J WHITLEY and F G HAYDEN, eds, ASM Press, Washington, DC, pp. 515–35. SAID B, IJAZ S, KAFATOS G, BOOTH L, THOMAS H L, WALSH A, RAMSAY M, MORGAN D and HEPATITIS E INCIDENT INVESTIGATION TEAM (2009), Hepatitis E virus outbreak on cruise ship. Emerg Infect Dis, 15, 1738–44. SAIF L J, ROSEN B I and PARWANI A V (1994), Animal rotaviruses. In: Viral Infections of the Gastrointestinal Tract, 2nd ed., A Z KAPIKIAN, ed., Marcel Dekker, New York, pp. 279–367. SAULSBURY F T, WINKELSTEIN J A and YOLKEN R H (1980), Chronic rotavirus infections in immunodeficiency. J Pediatr, 97, 61–5. SCHENKEL K, BREMER V, GRABE C, VAN TREECK U, SCHREIER E, HÖHNE M, AMMON A and ALPERS K (2006), Outbreak of hepatitis A in two federal states of Germany: bakery products as vehicle of infection. Epidemiol Infect, 134, 1292–8. SCHMID D, FRETZ R, BUCHNER G, KÖNIG C, PERNER H, SOLLAK R, TRATTER A, HELL M, MAASS M, STRASSER M and ALLERBERGER F (2009), Foodborne outbreak of hepatitis A, November 2007–January 2008, Austria. Eur J Clin Microbiol Infect Dis, 28, 385–91. SCHOENBAUM S C, BAKER O and JEZEK Z (1976), Common-source epidemic of hepatitis due to glazed and iced pastries. Am J Epidemiol, 104, 74–80. SIMMONS G, GREENING G, GAO W and CAMPBELL D (2001), Raw oyster consumption and outbreaks of viral gastroenteritis in New Zealand: evidence for risk to the public’s health. Aust N Z J Public Health, 25, 234–40. SINCLAIR R G, JONES E L and GERBA C P (2009), Viruses in recreational waterborne disease outbreaks: a review. J Appl Microbiol, 107, 1769–80. SMITH A, REACHER M, SMERDON W, ADAK G K, NICHOLS G and CHALMERS R M (2006), Outbreaks of waterborne infectious intestinal disease in England and Wales, 1992– 2003. Epidemiol Infect, 134, 1141–9. STRAUN L K, SCHNEIDER K R and DANYLUK M D (2011), Microbial safety of tropical fruits. Crit Rev Food Sci Nutr, 51, 132–45. TOMAR B S (1998), Hepatitis E in India. Zhonghua Min Guo Xiao Er Ke Yi Xue Hui Za Zhi, 39, 150–6. TSAREV S A, TSAREV T S, EMERSON S U, YARBOUGH P O, LEGTERS L J, MOSKAL T and PURCELL R H (1994), Infectivity titration of a prototype strain of hepatitis E virus in cynomolgus monkeys. J Med Virol, 43, 135–42. VERHOEF L, VENNEMA H, VAN PELT W, LEES D, BOSHUIZEN H, HENSHILWOOD K, KOOPMANS M and The Foodborne Viruses in Europe Network (2010), Use of norovirus genotypes to differentiate origins of foodborne outbreaks. Emerg Inf Dis, 16, 617–24. VILLENA C, GABRIELI R, PINTÓ R M, GUIX S, DONIA D, BUONOMO E, PALOMBI L, CENKO F, BINO S, BOSCH A and DIVIZIA M (2003), A large infantile gastroenteritis outbreak in Albania caused by multiple emerging rotavirus genotypes. Epidemiol Infect, 131, 1105–10. VISSER H, VERHOEF L, SCHOP W and GÖTZ H M (2010), Outbreak investigation in two groups of coach passengers with gastroenteritis returning from Germany to the Netherlands in February 2009. Euro Surveill, 15, 19615.

Published by Woodhead Publishing Limited, 2013

An introduction to food- and waterborne viral disease 17 VIVANCOS R, SHROUFI A, SILLIS M, AIRD H, GALLIMORE C I, MYERS L, MAHGOUB H

and (2009), Food-related norovirus outbreak among people attending two barbeques: epidemiological, virological, and environmental investigation. Int J Infect Dis, 13, 629–35. WARNER R D (1992), A large nontypical outbreak of Norwalk virus. Int Food Safety News, 1, 55. WARNER R D, CARR R W, MCCLESKEY F K, JOHNSON P C, ELMER L M and DAVISON V E (1991), A large nontypical outbreak of Norwalk virus: gastroenteritis associated with exposing celery to nonpotable water and with Citrobacter freundii. Arch Intern Med, 151, 2419–24. WEBBY R J, CARVILLE K S, KIRK M D, GREENING G, RATCLIFF R M, CRERAR S K, DEMPSEY K, SARNA M, STAFFORD R, PATEL M and HALL G (2007), Internationally distributed frozen oyster meat causing multiple outbreaks of norovirus infection in Australia. Clin Infect Dis, 44, 1026–31. WELTMAN A C, BENNETT N M, ACKMAN D A, MISAGE J H, CAMPANA J J, FINE L S, DONIGER A S, BALZANO G J and BIRKHEAD G S (1996), An outbreak of hepatitis A associated with a bakery, New York, 1994: the 1968 “West Branch, Michigan” outbreak repeated. Epidemiol Infect, 117, 333–41. WESTRELL T, DUSCH, V, ETHELBERG S, HARRIS J, HJERTQVIST M, JOURDAN-DA SILVA N, KOLLER A, LENGLET A, LISBY M and VOLD L (2010), Norovirus outbreaks linked to oyster consumption in the United Kingdom, Norway, France, Sweden and Denmark. Euro Surveill, 15, 19524. WEVERS D, METZGER S, BABWETEERA F, BIEBERBACH M, BOESCH C, CAMERON K, COUACYHYMANN E, CRANFIELD M, GRAY M, HARRIS L A, HEAD J, JEFFERY K, KNAUF S, LANKESTER F, LEENDERTZ S A J, LONSDORF E, MUGISHA L, NITSCHE A, REED P, ROBBINS M, TRAVIS D A, ZOMMERS Z, LEENDERTZ F H and EHLERS B (2011), Novel adenoviruses in wild primates: a high level of genetic diversity and evidence of zoonotic transmissions. J Virol, 85, 10774–84. WHEELER C, VOGT T M, ARMSTRONG G L, VAUGHAN G, WELTMAN A, NAINAN O V, DATO V, XIA G, WALLER K, AMON J, LEE T M, HIGHBAUGH-BATTLE A, HEMBREE C, EVENSON S, RUTA M A, WILLIAMS I T, FIORE A E and BELL B P (2005), An outbreak of hepatitis A associated with green onions. N Engl J Med, 353, 890–7. WHITE K E, OSTERHOLM M T, MARIOTTI J A, KORLATH J A, LAWRENCE D H, RISTINEN T L and GREENBERG H L (1996), A foodborne outbreak of Norwalk virus gastroenteritis: evidence for post-recovery transmission. Am J Epidemiol, 124, 120–6. WYATT R G, DOLIN R, BLACKLOW N R, DUPONT H L, BUSCHO R F, THORNHILL T S and KAPIKIAN A Z (1974), Comparison of three agents of acute infectious nonbacterial gastroenteritis by cross-challenge of volunteers. J Infect Dis, 129, 709–14. WYN-JONES A, CARDUCCI A, COOK N, D’AGOSTINO M, DIVIZIA M, FLEISCHER J, GANTZER C, GAWLER A, GIRONES R, HÖLLER C, DE RODA HUSMAN A M, KAY D, KOZYRA I, LÓPEZPILA J, MUSCILLO M, SÃO JOSÉ NASCIMENTO M, PAPAGEORGIOU G, RUTJES S, SELLWOOD J, SZEWZYK R and WYER M (2011), Surveillance of adenoviruses and noroviruses in European recreational waters. Water Res, 45, 1025–38. YAMASHITA T, ITO M, TSUZUKI H and SAKAE K (2001), Identification of Aichi virus infection by measurement of immunoglobulin responses in an enzyme-linked immunosorbent assay. J Clin Microbiol, 39, 4178–80. YAMASHITA T, KOBAYASHI S, SAKAE K, NAKATA S, CHIBA S, ISHIHARA Y and ISOMURA S. (1991), Isolation of cytopathic small round viruses with BS-C-1 cells from patients with gastroenteritis. J Infect Dis, 164, 954–7. YAMASHITA T, SUGIYAMA M, TSUZUKI Y, SAKAE K, SUZUKI Y and MIYAZAKI Y (2000), Application of a reverse transcription-PCR for identification and differentiation of NAIR P

Published by Woodhead Publishing Limited, 2013

18 Viruses in food and water Aichi virus, a new member of the picornavirus family associated with gastroenteritis in humans. J Clin Microbiol, 38, 2955–61. YU J H, KIM N Y, KOH Y J and LEE H J (2010), Epidemiology of foodborne Norovirus outbreak in Incheon, Korea. J Korean Med Sci, 25, 1128–33. ZOMER T P, DE JONG B, KÜHLMANN-BERENZON S, NYRÉN O, SVENUNGSSON B, HEDLUND K O, ANCKER C, WAHL T and ANDERSSON Y (2010), A foodborne norovirus outbreak at a manufacturing company. Epidemiol Infect, 138, 501–6.

Published by Woodhead Publishing Limited, 2013