Viral infections are the leading cause of gastroenteritis globally and in Europe and may also cause enterically transmitted hepatitis and illness after migrating from the human intestine to other organs. Various viruses have been implicated in foodborne illness, with two types of virus, Norovirus and Hepatitis A, causing the most significant burden of foodborne illness and outbreaks, as they are highly contagious. Rotavirus is one of the major causes of diarrhoea in children and Hepatitis E, while primarily associated with waterborne infections, has been associated with foodborne outbreaks. Food borne transmission is important in the epidemiology of these four viruses, in addition to person-to-person contact and environmental transmission. Adenovirus, Astrovirus, Sapovirus, tick borne encephalitis and Avian Influenza H5N1 may also cause viral infections where food is a vector.
Foodborne viruses originate from the human intestine and are excreted in high numbers in the faeces or through emesis. The low infectious dose and robust survival in food and various environments facilitates the spread of viral infections. Food may be intrinsically contaminated during primary production or contaminated when prepared or handled by an infected food handler. Symptoms are typically nausea, vomiting, diarrhoea and abdominal pain.
Viruses behave differently to bacteria in infectivity, persistence and epidemiology and this a concern because current food safety guidelines usually either have not been validated for foodborne viruses, therefore there is no understanding of the efficacy of the controls on viruses, or the control measures are not effective in controlling these viruses and there are currently no reliable indicator organisms for viruses. Good agricultural and manufacturing practices are necessary to avoid introducing viruses into raw materials and food handling environments, as well as the consideration of viruses during the development of HACCP. Enteric viruses often produce mild symptoms, are difficult to culture and there are limited global pathogenic viral surveillance systems globally, so it is expected that as diagnostic methods and surveillance systems improve more viral diseases are likely to emerge as illnesses with foodborne transmission.
Between 1886 and 1898 viruses were first recognised as organisms different from other disease-causing microbes. In 1886, Adolf Mayer was studying tobacco mosaic disease, but tests and attempts to isolate and culture a bacterial agent failed. In 1892, Dmitri Ivanovski demonstrated through an experiment that the disease was either caused by a toxin or by something much smaller than any previously described organism. In 1898 Martinus Beijerinck replicated Ivanovski's experiment and showed that the disease was caused by an infectious life form of some type. This organism became known as tobacco mosaic virus.
First recognised as a vehicle for viruses in 1914, food was identified as the vehicle in an outbreak of raw-milk associated poliomyelitis. Norwalk virus was identified in 1918 following an outbreak in a primary school in Norwalk, Ohio, which affected both children and adults. In the mid-1950s shellfish was identified as the transmission route in Sweden and then in the United States. Following the introduction of molecular methods in the 1990s, viruses were identified as being the leading cause of human gastroenteritis in developed countries.
Many different viruses can cause foodborne illness, including, noroviruses, adenoviruses, sapoviruses and astroviruses. Symptoms may be similar to gastroenteritis caused by bacteria and parasites. Norovirus and Hepatitis A are the most important viruses causing viral foodborne illness in Europe for the number of outbreaks and people infected1.
Viruses do not grow or make their own energy and can only replicate using a living host cell. Outside a host cell they are totally inert, incapable of reproducing or carrying out other metabolic processes and must induce living cells to replicate. Viruses have therefore been considered to lie at, or beyond, the edge of what is considered to be a living organism. Recent research 2 provides evidence using protein folds that suggests viruses may be living entities. The smallest of the microbial microorganisms, foodborne viruses are usually approximately spherical and 25−30nm diameter, typically being visible only using an electron microscope. Few have lipid envelopes or other defining structural features. Viruses often show a high resistance to stresses typically used in food manufacturing and preservation, such as heat, freezing and UV light.
Viruses may be shed in extremely high numbers (up to 107-1010 virus particles per gram of stools3) and vomit may contain a minimum of 106 particles4. Foodborne viruses have a low infectivity dose of 100 or less cells and this combined with the high numbers shed can lead to large outbreaks in a relatively short time.
Image courtesy of the Centers for Disease Control and Prevention
Noroviruses are a genetically diverse group of non-enveloped viruses in the Caliciviridae family, important human pathogens causing sporadic cases and epidemic outbreaks, consisting of several serologically distinct groups that have been named after the places where the outbreaks occurred. The 27−30nm viral particles are symmetrically icosahedral and the particles contain a single-stranded, positive sense RNA genome. Infection is through oral ingestion from contaminated food or water with replication occurring in the small intestine causing transient lesions of the intestinal mucosa with potential pathology of peripheral tissues. Transmission also occurs through aerosols creating during vomiting and fomites such as equipment.
The disease is self-limiting, typically 12−48 hours up to 3 days for the majority of people, with a low infection dose of 10−100 virus particles, mild, and characterised by nausea, vomiting, diarrhoea, myalgias and abdominal pain. Prolonged virus shedding of up to 8 weeks may occur in asymptomatic people and immunosuppressed individuals. Headache and low-grade fever may occur and there is anecdotal evidence that there may be other diseases caused by Norovirus including infant necrotising enterocolitis5. The primary route of transmission is person-to-person transmission through the faecal−oral and vomit-oral routes and indirectly through food (ready to eat including leafy vegetables and herbs, berries and foods handled after cooking), water and environment. In Europe, outbreaks in healthcare facilities are most common. Food is implicated in up to 24% of global outbreaks6. Crustaceans, shellfish, molluscs and their products and vegetables and juices are the foods most often implicated in European norovirus outbreaks in 20167.
|Image courtesy of Centers for Disease Control and Prevention|
Rotaviruses are a group of non-enveloped viruses in the Reoviridae family, consisting of 8 species (named A−H). Rotavirus A is endemic worldwide, causing approximately 80% of rotavirus gastroenteritis in humans, particularly through waterborne infection, with rotavirus B and C also being human pathogens. The 70nm viral particles are icosahedral and the particles consist of double-stranded RNA segments. Rotaviruses infect intestinal enterocytes, with early events after infection being mediated by virus−epithelial cell interactions. Rotaviruses infect cells differently depending on whether or not sialic acid is required for initial binding, and infection alters epithelial cell functions.
Rotavirus gastroenteritis is a self-limiting, mild to severe disease characterised by vomiting, watery diarrhoea and low-grade fever. Symptoms usually start 1−2 days after infection with vomiting followed by 3−7 days of diarrhoea caused by an infective dose believed to be 10−100 infectious viral particles; asymptomatic rotavirus excretion may play a role in perpetuating endemic disease with shedding occurring in excess of 30 days. Diarrhoea without fluid and electrolyte replacement may result in severe diarrhoea and death, particularly among children 6 months to 2 years of age, the elderly and the immunocompromised. Immunity is believed to be built up which reduces the severity of any subsequent infections. Outbreaks caused by Group B rotavirus have been reported in the elderly and adults with Group C rotavirus being associated with sporadic cases of diarrhoea in children in many countries8. 2 live oral vaccines are currently available commercially globally and have demonstrated efficacy in reducing disease by Rotavirus.
Hepatitis A 2 virus (HAV) is part of the enterovirus group of the Picornaviridae family and one of 6 forms (A, B, C, D, E, G) which was first identified in 1973. HAV has a single molecule of RNA surrounded by a 27−32nm protein capsid and a buoyant density in CsCl of 1.33 g/ml. Foods can be contaminated with the virus through contact with raw sewage, such as is the case with shellfish, or through contact with contaminated water; transmission is primarily via the faecal−oral route. HAV replicates exclusively in liver cells, is excreted in bile and shed in the faeces of infected people. Hepatitis A is less common in developed countries with 942 reported cases in England and Wales in 2017; reported cases have been generally decreasing since 2007, with an outbreak in 2017 leading to a 112.2% increase in reported cases9.
Hepatitis A is a liver infection which is usually a mild illness characterised by symptoms similar to influenza including sudden onset of fever, malaise, nausea, joint pain, dark-coloured urine, pale stools, anorexia and abdominal discomfort, followed in several days by jaundice, with complete recovery within 2 months. The illness is usually more severe the older the person is, with infected children under 6 years not experiencing noticeable symptoms. The minimum infectious dose required for HAV infection in humans is unknown, but presumably is 10−100 virus particles with the incubation period being dependent upon the number of particles ingested (fewer particles means a linger incubation period). The incubation period for hepatitis A varies from 10 to 50 days (average 28 days) with a long communicability period from early in the incubation period to about a week after the development of jaundice. The middle of the incubation period (2 weeks before symptoms develop) presents the greatest period of communicability, well before the first presentation of symptoms during peak shedding of the virus. Many infections with HAV are asymptomatic, especially in children. Symptoms are occasionally more severe, particularly in people with pre-existing liver conditions with convalescence taking up to 3 months. Patients suffer from feeling chronically tired during convalescence with an inability to work. Fatality is rare, usually occurring in the elderly. Once the virus has been contracted lifelong immunity develops8,9,10.
Routine vaccination of all food handlers is not recommended, because their profession does not put them at higher risk for infection.
This virus is rare within the EU but is recognised as having increased importance as an emerging infection11 HEV is a non-enveloped, positive-stranded RNA of approximately 7.5 kb spherical, probably icosahedral shaped virus with a diameter of 27−34 nm. The virion is composed entirely of viral protein and RNA, with a buoyant density of 1.29 g/cm3 in potassium tartrate/glycerol gradients. Although the capsid icosahedral shape, lack of outer lipid envelope and size of the genome resembles other faecally transmitted viruses including HAV and norovirus, hepatitis E has some distinguishing physicochemical and genetic properties which have led to the virus being assigned its own genus (Hepevirus) and family (Hepeviridae). There is a single serotype and at least five genotypes [human, swine (1-4) and avian (5)].
From the intestinal tract, the virus reaches the liver through an unknown route and mechanism. HEV appears to replicate primarily in liver and gall-bladder cells, but has been noted in the small intestine, lymph nodes, colon and salivary glands. The incubation period following exposure can range from 3 to 8 weeks, with a mean of 6 weeks. The disease usually is mild, asymptomatic and self-resolves in 2 weeks; it is usually seen in age groups 15−40 and can be asymptomatic in children. Symptoms include jaundice, malaise, anorexia, enlarged tender liver, abdominal pain, arthralgia, hepatomegaly, vomiting and fever. Chronic hepatitis has been reported in organ transplant recipients and in patients with active HIV infections. Extended faecal shedding when present occurs for approximately 2 weeks after jaundice develops. Fulminant hepatic failure has been observed especially in pregnant women where mortality rates rise from less than 1% to 25%. In immunocompromised patients hepatitis E can be persistent and also associated with increased mortality and morbidity in people with progressed liver disease.
Viruses can be considered intracellular parasites on the basis that production of progeny viruses takes place within the host cell. Progeny are formed from the production by the host cell of viral nucleic acid and protein; these viral constituents are capable of ‘self-assembly’ within the cell spontaneously forming viral progeny. Release of the virus is seldom reliant purely on lysis of the host cell and can be released in a number of ways.
The viral form that is transmitted from cell to cell and from one host to another is called a particle. If the virus particle’s outer layer contacts a homologous receptor on a susceptible cell’s plasma membrane, the virus’s protein coat, or lipid envelope if present, attaches and infection ensues. To be food or water-borne, a virus must be capable of infectivity upon ingestion by the host in a cell type that is accessible from the digestive tract.
The virus particle attaches and is engulfed by the host cell (usually the whole particle) through what is believed to be a passive process into the cytoplasm – the host cell does all of the work although a high proportion of particles are rejected after coming into contact with a homologous receptor. Uncoating of the protein coat or lipid envelope occurs during the engulfment process with nucleic acid and intrinsic viral enzymes being released into the host cell. As necessary, the viral nucleic acid is transcribed and translated by the cell; this induces production of viral nucleic acid, protein and other constituents required. As quantities are produced, the progeny self-assembly begins; viruses produced in the intestinal tract are called ‘enteric’.
If progeny fully mature within the host cell, then particulate release may not be immediate, and the particles may accumulate within the cell; release of the particles is typically gradual rather than the normal bacteriophage ‘burst. Viruses in animal cells may slowly ‘leak’ through the plasma cell membrane or may stay associated with the cell. The replication cycle may take from between 8 hours to over 24 hours in a single cell.
Enteric viruses are usually resistant to environmental stresses such as heat and acid. The majority are also resistant to freezing and drying, are stable in contact with lipid solvents and may be resistant to ultrahigh hydrostatic pressure. These properties enable foodborne viruses to survive in pickled, marinated and acidic foods. Enteric viruses are capable of surviving and retaining infectivity in marine, estuarine and fresh water for several weeks at 4°C and survival may be increased by attachment to sediment or particulate matter.
- Noroviruses are resistant to drying. They can survive on almost any hard surface (including glass, door handles and railings) for up to 12 hours. Norovirus can survive for at least 56 days on stainless steel and 15 days on carpet10. The virus is relatively resistant to high levels of chlorine (up to 10ppm free chlorine) and also varying temperatures. In chilled and frozen environments norovirus may be able to survive for months or even years. Norovirus remains infective after being subjected to pH 2.7 for 3 hours at ambient temperature. While the virus is inactivated by boiling, it can remain infective at 60°C for 30 minutes and can survive some pasteurisation and steaming processes.
- Rotaviruses are stable in the environment; in estuaries samples have been founds at levels of 1−5 infectious particles/gallon and can also survive secondary sewage treatment, with a persistent resistance to many of the new physical or chemical technologies for treating wastewater. Rotavirus is resistant to inactivation, with infectivity being unaltered at both low (3.5) and high (11) pH. To kill or inactivate rotavirus from contaminated well water, bringing the water to a rolling boil for one minute is advised. The virus is stable at low temperatures of -20°C and 4°C, with minimal loss of titre after 32 days, and is stable during 6 freeze/thaw cycles. Rotaviruses can survive on human hands for up to 4 hours, are stable for up to 4 days at 37°C and rapidly inactivated at 56°C. Rotaviruses are inactivated by UV light and by disinfectants, including chlorine, hydrogen peroxide and ethanol. Sanitary measures adequate for bacteria and parasites seem to be ineffective in endemic control of rotavirus, with similar incidence rates of rotavirus infection in countries with both high and low health standards.
- Hepatitis A is readily inactivated by heating foods to 85°C for 1 minute but is not subject to thermal denaturation at lower temperatures (70°C for up to 10 min). HAV can survive chilled and frozen temperatures for up to 2 years. Disinfection with a 1:100 dilution of household bleach in water (0.5mg free chlorine for 30 minutes), or cleaning solutions containing quaternary ammonium and/or HCl is also effective in inactivating HAV, although the virus is resistant to disinfection by some organic solvents and by a pH as low as 3, acid treatment (pH 1 for 2 h at room temperature) is effective. HAV can survive in the environment for at least 12 weeks at 25°C when excreted in human faeces and remain infectious after 1 month on environmental surfaces at ambient temperatures, three to four hours in faecal matter on a person's hand. It has been found to survive in experimentally contaminated fresh water, seawater, wastewater, soils, marine sediment, live oysters, and creme-filled cookies. Hepatitis A is more resistant to heat and drying than other enteroviruses.
- Hepatitis E is considered to be labile when not in the acidic conditions found in the gastrointestinal tract or in faecal material. HEV can withstand thermal inactivation at temperatures near those expected to be found within a rare-cooked steak (approximately 57°C). The levels of viable virus decrease rapidly at higher temperatures. Repeated freezing and thawing can gradually decrease the HEV levels. As HEV does not have a lipid envelope, it can somewhat withstand exposure to alcohols and detergents. HEV does seem especially susceptible to high salt concentration.
It is difficult to estimate the proportion of foodborne disease caused by viruses due to under-reporting, the lack of surveillance systems, often high levels of person to person infection and the inability of existing systems to determine the proportion of disease that is transmitted by foodborne routes relative to other common routes.
Increases in population, scarcity of clean water, changes in eating habits such as the increased consumption of food eaten raw and the globalisation of the supply chain are all contributing to the increase and spread of viral foodborne disease11.
- May 2005, 2 outbreaks in Denmark were reported from frozen imported raspberries.
- A cluster of outbreaks was attributed to contaminated commercial ice in 1987 in Wilmington, Delaware.
- 2005, an outbreak in France was reported from imported frozen raspberries
- Food poisoning outbreak caused by norovirus GII/4 in school lunch, Tochigi Prefecture, Japan in December 2007 affecting 18 children and 5 adults, possibly linked to salad
- January 2009, military base in Germany, 36 cases from norovirus contaminated salad
- January 2010 in Tennessee, USA – 13 people affected from cake in a restaurant
- February 2012, Missouri, USA, 139 cases from fruit salad at a banquet
- In 2017 an outbreak of norovirus at a restaurant chain in the US caused illness in over 130 people.
- A norovirus outbreak in 2018 in the US and Canada was linked to raw oysters from British Columbia, Canada.
- 188 lab confirmed outbreaks from January to August in 2018 in England12.
- 1982, outbreak in China due to contamination of water by raw sewage.
- April 2000, 19 confirmed cases and 108 self-reported cases in District of Columbia, United States, possibly from line cooks
- December 2000, outbreak attributed to contaminated water supplies in Tirane, Albania with 2722 children seen at Tirane Hospital
- 9907 patients in 2005 in Malatya City, Turkey, due to possible contamination of a large water depository from a water well, which supplied drinking water to two major districts of the city.
- 4375 laboratory confirmed outbreaks in England from January-August in England in 201812.
- Clam associated outbreak in Shanghai in 1988 with 280,000 people affected due to contamination and inadequate cooking.
- More than 50 residents in South Cambridgeshire, UK in 1991 where the vehicle was believed to be bread.
- 213 cases in Maine, United States in 1997 attributed to frozen strawberries
- November 2005 in France 111 cases were reported due to consumption of Oysters
- 2011, 7 people believed to have contracted HAV from sun dried tomatoes in UK.
- In 2013, 165 people became ill in a multistate US outbreak attributed to pomegranate arils.
- In 2016 an outbreak in the US was linked to frozen strawberries.
- In 2018 six EU countries reported confirmed that may have been associated with a single food product.
Hepatitis E has been the cause of sporadic cases and epidemic forms with the primary vehicle being ingestion of faecally contaminated drinking water.
- New Delhi in 1955 following the contamination of the city's drinking water when 29,000 cases of icteric hepatitis occurred.
- Indian subcontinent (1975, 1978, 1980) and USSR (1983): several major outbreaks.
- In 2007 in Corsica, 7 cases of Hepatitis E were attributed to raw figatellu (dish made with pig liver).
As enteric viruses are passed through the faecal−oral route, foods typically associated with food and waterborne viruses can occur at any point in cultivation, harvesting, processing, distribution, or processing/preparation. Water, shellfish and salads are the most frequent sources.
Foods implicated in outbreaks include molluscan shellfish (oysters, cockles, mussels), berries, salads, cold cuts, green onions, sun dried tomatoes, leafy greens, drinking water, fruit juices, milk and milk products, undercooked wild boar meat, deer meat, pig liver sausage and salad dressing and cake icings.
Detection and isolation of food or waterborne viruses is limited by the non-routine nature of testing for these viruses in food (virus particles require living host or tissue to replicate), long incubation of some (such as Hepatitis A virus) meaning that the implicated food is often unavailable, difficulty or inability to culture in laboratory cell cultures, lack of reliable detection in food matrices and the typically low level of virus particles in a contaminated food. In addition, detection is based on genomic copies so does not indicate viability.
Specialist laboratories may achieve detection using cell culture and complex extraction methods but techniques previously available are not suitable for routine application and recovery rates remain poor.
Norovirus is recognised in human stool specimens by enzyme-linked immunosorbent assays and commonly through PT-PCR to detect and differentiate noroviruses in vomit and stools. Immune electron microscopy and antibody tests can be used to identify norovirus in serum.
Rotavirus diagnosis may be made by rapid antigen detection of rotavirus in stool specimens. Strains may be further characterised by reverse transcriptase polymerase chain reaction (RT-PCR). Electron microscopy and polyacrylamide gel electrophoresis (PAGE) are used in some laboratories.
Hepatitis A is typically diagnosed by finding IgM-class anti-HAV in serum collected during the acute or early convalescent phase of disease.
Hepatitis E is diagnosed by immune electron microscopy, in faeces of acutely ill patients or by molecular detection of genomic RNA in serum or faeces. Additional diagnostic tests that are used in research studies (due to the specialised facilities required) are RT-PCR and immune electron microscopy.
Controls to reduce the risk of foodborne transmission of foodborne enteric viruses should focus on 13, 14, 15, 16:
- Use of potable water for irrigation and processing.
- Use of shellfish from approved waters.
- Active monitoring of shellfish production areas for contamination events
- Thorough cooking of shellfish prior to consumption (85−90°C for 4 minutes or steamed for 90 seconds).
- Excluding employees suffering from gastro-enteritis for 48 hours after symptoms have ceased and 1−2 weeks after the onset of jaundice.
- Exclude symptomatic food handlers from the entire food business site (not just food handling duties and areas). Once excluded, they should remain away for a further 48 hours from when symptoms stop or from the end of any treatment of the symptoms with medicine such as anti-diarrhoeal drugs.
- Food handlers with Hepatitis A should remain off work for seven days after the onset of jaundice and/or other symptoms. Any food handler who develops jaundice for an unknown reason should be excluded immediately and seek medical advice.
- Effective training in personal hygiene – practical advice about hand washing techniques and education on when to seek medical attention.
- Thorough cleaning with an effective disinfectant following any vomiting episode in a handling environment.
- Destroying any food that may have become contaminated through aerosols and cleaning up and disinfecting thoroughly over a wide area after someone has been sick in or near a food handling area,
- Easy access to hand washing and sanitary facilities for all employees (including field workers).
- Discourage children from areas where food is harvested, handled or processed.
- Correct disposal procedures for sanitary waste.
- Potable water or chlorinated water should be used for rinsing produce or for making ice for packing or consumption.
- Posting handwashing signs (after eating and visiting the toilet) with frequent written and verbal reminder.
- Development of a HACCP including the risks and control measures for foodborne viruses.
- WHO Estimates of the Global Burden of Foodborne Diseases. 2015. Foodborne viral disease in the European region/ World Health Organization. http://www.euro.who.int/__data/assets/pdf_file/0007/294604/Factsheet-Foodborne-viral-disease-EU-Norovirus-HepatitisA-en.pdf
- A phylogenomic data-driven exploration of viral origins and evolution. BY ARSHAN NASIR, GUSTAVO CAETANO-ANOLLÉS. SCIENCE ADVANCES25 SEP 2015 : E1500527. A study of the evolution of the proteomic makeup of cells and viruses using protein structural and functional data.
- Procedia Food Science. Volume 5, 2015, Pages 304-30. Transmission of Common Foodborne Viruses by Meat Products. Branko Velebita, Dragoslava Radin. https://doi.org/10.1016/j.profoo.2015.09.069.
- Public Health Reasons Vomiting and Faecal Episodes. Cortney Miller, MS, Angela Fraser, PhD, Roman Sturgis, MFA (editor), Anna Saunders, Xi Chen, MS Department of Food, Nutrition, and Packaging Sciences, Clemson University, Clemson, SC 29634.
- Karst SM. Pathogenesis of Noroviruses, Emerging RNA Viruses. Viruses. 2010;2(3):748-781. doi:10.3390/v2030748.
- Barclay L, Park GW, Vega E, et al. Infection control for norovirus. Clinical microbiology and infection: the official publication of the European Society of Clinical Microbiology and Infectious Diseases. 2014;20(8):731-740. doi:10.1111/1469-0691.12674.
- The European Union summary report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in 2016 European Food Safety Authority European Centre for Disease Prevention and Control. doi: 10.2903/j.efsa.2017.5077.
- Estes MK, Kang G, Zeng CQ, Crawford SE, Ciarlet M (2001). Pathogenesis of rotavirus gastroenteritis. Novartis Found Symp 238, 82−96; discussion 96−100.
- Laboratory reports of hepatitis A infections in England and Wales, 2017 Health Protection Report Volume 12 Number 27 27 July 2018.
- Buckley D, Fraser A, Huang G, Jiang X. Recovery Optimization and Survival of the Human Norovirus Surrogates Feline Calicivirus and Murine Norovirus on Carpet. Elkins CA, ed. Applied and Environmental Microbiology. 2017;83(22):e01336-17. doi:10.1128/AEM.01336-17.
- Goyal SM, editor (2006). Viruses in Foods. Springer US.
- Suspected and laboratory confirmed reported norovirus outbreaks in hospitals: outbreaks occurring in weeks 27 to 30, 2018 Health Protection Report Volume 12 Number 29 13 August 2018. Public Health England.
- Todd E, Grieg J. Viruses of foodborne origin: a review. Virus Adaptation and treatment. Volume 2015:7 Pages 25—45.
- International Journal of Food Microbiology. Volume 285, 20 November 2018, Pages 110-12. Foodborne viruses: Detection, risk assessment, and control options in food processing. Albert Boscha, Elissavet Gkogka, Françoise S.Le Guyader, FabienneLLoisy-Hamon, Alvin Lee, Lilouvan Lieshout, Balkumar Marthi, Mette Myrmel, Annette Sansom, Anna Charlotte Schultz, Anett Winkler, Sophie Zuber, Trevor Phister. doi.org/10.1016/j.ijfoodmicro.2018.06.001.
- Chilled Food Association (2016). Microbiological Guidance for Produce Suppliers to Chilled Food Manufacturers (3rd edition). https://www.chilledfood.org/product/microbiological-guidance-for-growers-mgg3-3rd-edition-2016/
- Food Standards Agency (2009). Food Handlers Fitness to Work. Regulatory Guidance and Best Practice Advice For Food Business Operators. https://www.food.gov.uk/sites/default/files/media/document/fitnesstoworkguide.pdf
- Avian Influenza and Food. IFST Information Statement. https://www.ifst.org/resources/information-statements/avian-influenza-and-food
- Koopmans M, Duizer E (2004). Foodborne viruses: an emerging problem. International Journal of Food Microbiology 90 (1), 23–41.
- Oogane T, Hirata A, Funatogawa K, Kobayashi K, Sato T, Kimura H (2008). Food poisoning outbreak caused by norovirus GII/4 in school lunch, Tochigi prefecture, Japan. Jpn J Infect Dis 61 (5), 423−424.
- Westrell T, Dusch V, Ethelberg S, Harris J, Hjertqvist M, Jourdan-da Silva N, Koller A, Lenglet A, Lisby M, Vold L (2010). Norovirus outbreaks linked to oyster consumption in the United Kingdom, Norway, France, Sweden and Denmark, 2010. Euro Surveill 15 (12), pii=19524. Available from: http://www.eurosurveillance.org/ViewArticle.aspx?ArticleId=19524
- Korsager B, Hede S, Bøggild H, Böttiger BE, Mølbak K (2005). Two outbreaks of norovirus infections associated with the consumption of imported frozen raspberries, Denmark, May−June 2005. Euro Surveill 10(6), E050623.1.
- Wadl M, Scherer K, Nielsen S, Diedrich S, Ellerbroek L, Frank C, Gatzer R, Hoehne M, Johne R, Klein G, Koch J, Schulenburg J, Thielbein U, Stark K, Bernard H (2010). Food-borne norovirus-outbreak at a military base, Germany, 2009. BMC Infect Dis 10, 30.
- Food Standards Agency (2009). Food Handlers: Fitness to Work Regulatory Guidance and Best Practice Advice For Food Business. Available from: http://www.food.gov.uk/multimedia/pdfs/publication/fitnesstoworkguide09v3.pdf
Institute of Food Science & Technology has authorised the publication of the following updated Information Statement on Foodborne Viral Infections, dated September 2018, replacing that of August 2013.
This updated Information Statement has been prepared by Julie Ashmore CSci FIFST, peer reviewed by professional members of IFST and approved by the IFST Scientific Committee.
The Institute takes every possible care in compiling, preparing and issuing the information contained in IFST Information Statements, but can accept no liability whatsoever in connection with them. Nothing in them should be construed as absolving anyone from complying with legal requirements. They are provided for general information and guidance and to express expert professional interpretation and opinion, on important food-related issues.