Avian Influenza and Food

October 2020

Summary

Avian Influenza (‘bird flu’) is a viral disease of birds with naturally occurring avian influenza Type A viruses. These viruses are globally widespread in aquatic birds (from the orders Anseriformes and Charadriiformes) such as shorebirds and waterfowl and are highly contagious.  Avian influenza can infect all species of domestic and wild birds as well as mammals such as pigs, pet and zoo animals. To date, no avian influenza viruses have demonstrated sustained human-to-human transmission.

Influenza A viruses exist in multiple forms (at least 16 H subtypes and 9N subtypes in birds). The H5N1 subtype of influenza crossed the species barrier from avian to human in 1997 for the first time, and from 2003 has been recirculating in Europe, Africa and Asia since re-emerging in China. There are multiple subtypes and genotypes all linked to the ancestral virus reported in 1997. Outbreaks in poultry and wild birds have been reported in over 65 countries. 861 laboratory-confirmed human cases of avian influenza (H5N1) in 17 countries have been confirmed, of which 455 have died. Human cases of avian influenza H7N9 have been reported in China since 2013 and occasional cases also in China have been reported with novel H5N6. The zoonotic variant of H5N6 virus has been associated with some spread amongst poultry but limited to south east Asia.

The likelihood of sustained human-to-human transmission is currently low, however there are expectations of more human infections with viruses originating in animals. Globally, poultry production and trade continue to expand and as production increases so does the potential opportunities for pathogenic viruses such as avian influenza to continue to evolve including acquisition of host adaptation and the ability to cross species barriers.

Poultry, poultry products and eggs can be safely consumed as the virus is inactivated at 70oC in less than one minute during conventional cooking. Human cases of illness have been strongly linked to the slaughtering and/or handling of diseased or dead birds in countries experiencing outbreaks of avian influenza, typically in areas where humans live and work alongside infected poultry. Home preparation of live birds in these areas must be conducted using good hygiene practices to prevent contamination of the handler, such as wearing personal protective equipment.

Biology of Avian Influenza

Three of the five viruses (A, B and C) belonging to the Orthomyxoviridae family, specifically the genus influenza virus cause influenza and are single stranded RNA viruses1 (which do not encode messenger RNA, a key intermediary in gene expression) with segmented genomes. Influenza A viruses derive from wild aquatic avian hosts, while types B and C are typically isolated from humans. Type A viruses exhibit cross-species transmission and can infect warm blooded mammals including cats2, swine, dogs, horses, sea mammals and mink3 and are classified according to the surface glycoproteins into subtypes. There are at least 16 hemagglutinin (HA) and 9 neuraminidase proteins with the type of hemagglutinin and neuraminidase determining the subtype, for example, a virus with the protein types 5 HA and 8 NA has the subtype H5N84.

Genetic reassortment and gene mutation results in highly diverse influenza A viruses, with the former potentially leading to antigenic shifts resulting in a new virus that is not affected by existing immunity in birds and mammals including humans.  The 1918 influenza pandemic is likely to have been caused by a virus that developed completely from an unknown avian source following modification through an unknown mechanism of the eight genome segments, allowing human infection5.

Infectivity and Pathogenicity

Most avian influenza HA subtypes are of low pathogenicity for birds and typically cause few clinical symptoms in poultry, however the H5 and H7 viruses may mutate into highly pathogenic viruses after circulation in poultry flocks, with the potential to cause pandemics or epidemics6,7. HPAI strains can present in poultry (especially gallinaceous i.e. chickens and turkeys) with severe clinical signs and high mortality rates. The recent H5 and H7 viruses that have caused illness in humans has been demonstrated to have unstable hemagglutinin, an obstacle in the viruses having efficient airborne transmission8, necessary for spread between humans.

The infectivity, pathogenicity and transmissibility of avian influenza viruses and the adaption to new hosts depends on the capability of the viral HA to use and to bind to sialic acid receptors9. When bound, the enzyme neuraminidase destroys receptors and cleaves sialic acid, so releasing the virus. The specificity of the binding to receptors influences the infectivity and pathogenicity of the viruses; HA in avian influenza viruses prefer to bind sialic acid occurring at the end of sugar chains in glycoproteins with an α2-3 linkage, whereas human influenza strains typically bind to the α2-6 linkage. In birds, the α2-3 linked sialic acids are found in the intestinal mucosa with α2-6 links being prevalent in the in the upper human respiratory tract. The severe infection of humans by H5N1 may be explained by the α2-3 links to sialic acid in their lower respiratory tract as viral replication in this area, as opposed to the upper respiratory tract, is more likely to cause severe disease such as pneumonia10. This may also mean that the avian influenza subtypes with the highest human pathogenicity are less likely to be transmissible along the human-to-human route as, it is likely that replication in the upper respiratory tract is important for transmission.

Cases and Outbreaks

Cases

In 2005 H5N1 was identified in the UK in a quarantined imported cage bird11. The H5N1 strain was similar to the strain circulating in Asia and was likely contracted from other birds in quarantine. Since late 2016, avian influenza has been identified in wild birds from across the UK with most cases being in England12. In January 2018, the first occurrence of H5N6 in the UK was published by Defra with the death of mute swans in Dorset. Further cases of Avian Flu were detected in wild birds later the same month in Dorset, closely related to the H5N6 strain that was circulating in Europe in wild birds. In June 2018 H5N6 was identified in a wild greylag goose similar to the strain identified Northern Ireland in March from a Buzzard. All these H5N6 viruses could be differentiated from those zoonotic strains reported in Asia but were fully lethal for poultry although no outbreaks have occurred in the UK to date with this virus.

Outbreaks

In the UK, there have been several outbreaks of avian influenza, primarily on poultry farms and in backyard flocks with no cases of HPAI infecting humans. Confirmed outbreaks of HPAI in the UK since 2005 have occurred with several virus subtypes (H5N1, H7N7, H5N8). Cases have been detected in different poultry species including turkeys, chickens and ducks. A feature of outbreaks in 2016/17 with H5N8 were cases in backyard or household poultry.

HPAI viruses have been described in birds since 1878, in Italy, then Europe and globally. It is also worth noting that the cause of the human pandemics of influenza in 1918, 1957, 1968 and 1977 were caused by viruses with a combination of avian and human genes13.

Timeline of avian influenza major events14:

Spread of H5N1:

Bangladesh, China, Egypt, India, Indonesia, and Vietnam have largely been considered endemic for Eurasian HPAI H5N1 in poultry since 201115. HPAI strains including H5N2, H5N3, H5N6, H5N8 and H7N7 (21) continue to circulate.

Avian influenza in humans

In 1997, 18 cases of H5N1 were reported in Hong Kong, the first time the virus crossed the species barrier to humans, with 18 cases being confirmed and 6 of those cases resulting in deaths.

Since 1999 there have been sporadic cases of H9N2 generally in association with mild illness typified by influenza like respiratory signs or conjunctivitis. Cases of H5N1 HPAI zoonotic infection steadily increased from 2005 associated with expansion in virus range in poultry. Cases of H5N1 HPAI have reduced in recent years and been limited to a few countries where infection is endemic in poultry. In 2003 in the Netherlands, for the first time a large poultry outbreak with a different subtype (H7N7) was associated with human cases of exposed personnel resulting in mild illness in 83 cases and one death.

The following year, H7N3 was reported in British Columbia, Canada. The H5 HPAI viruses of multiple subtypes continue to cause significant global problems with ongoing outbreaks in poultry with some occasional impact on other populations, including wild birds and humans.

Infections of the novel avian influenza H7N9 subtype was reported in China in humans in 2013 and has since been reported in both poultry and humans. The majority of human cases reported exposure to poultry markets or live poultry. Human-to-human spread is thought to have occurred on rare occasions, however, there is no evidence of sustained person-to-person infection. A programme of vaccination in poultry in China has led to a large reduction in the number of human cases.

Food Handling

Infected domestic and wild birds shed avian influenza viruses in their oral secretions including high concentrations in their faeces. Transmission of the virus to humans is likely to occur by airborne (when a person breathes in droplets or dust containing the virus) or indirect contact with dust, feathers, clothes etc., with the eyes or nose potentially being important initial infection sites. While human-to-human transmission is currently limited, there is the possibility that H5N1 or related viruses may be transmitted through the human faecal-oral route16 in humans, and this route is known as a route between waterfowl and domestic poultry17. Globally, most human illness has been caused by two Asian lineage strains (H5N1 and H7N9) often with severe illness and mortality18. Symptoms in humans with avian influenza A virus infections includes subclinical symptoms such as conjunctivitis, fever and muscle aches and severe symptoms due to complications including severe respiratory illness, multi-organ dysfunction and secondary bacterial and fungal infections19. The ongoing outbreaks detailed in the section above have raised concerns regarding the risk to food from avian influenza. The majority of human illnesses have been attributed to exposure to live poultry in the week prior to symptoms of illness presenting. This exposure includes visiting a market selling live poultry20 or in households keeping poultry flocks in urban areas and the areas surrounding metropolitan areas. Avian influenza in domestic birds has been reported in 68 countries in 2018, primarily in Europe, Africa and Asia. 12 subtypes of the virus have been reported (7 in Europe), as opposed to the 4 reported 2005-2012 reflecting the increasing virus diversity. Since 2013 over 120,000,000 birds have died or been killed (exact estimates lacking, and this figure is probably a gross underestimate) and disposed of due to HPAI avian influenza outbreaks21. However, as shown by surveillance data in the United States, HPAI H5N1 can still enter the human food chain, as demonstrated by being detected in frozen duck meat imported from Asia22, as well as more recent reports of virus in duck carcases imported into Korea and Japan (Sakoda et al). There has been no research confirming that the disease can be transmitted to humans through food which is correctly handled and cooked, however there is evidence potentially linking human and carnivorous animal illness to the consumption of food made with raw contaminated poultry blood23, 24. Diseased or dead birds should not be handled in outbreak areas without personal protective equipment and measures must be taken to prevent personal being contaminated from blood, meat and bones and ensuring that such birds are not used for human consumption. Some species can be asymptomatic carriers and may not show clinical signs of the disease, as can vaccinated poultry in some countries. Virtually all parts of a bird infected with H5N1 HPAI or closely related viruses can be impacted, and the virus can survive through the marketing and distribution chain in fresh and frozen meat as the virus is viable at cold chain temperatures (35 days at 4°C in faeces and at ambient temperatures on surfaces for several weeks)23. In areas not impacted by outbreaks, there is a very low likelihood of the virus being present in fresh or frozen meat in the food chain and the risk to food handlers or consumer is very low. Correctly prepared and cooked poultry and poultry products are safe to eat. There is no food safety risk in the UK for consumers. On-farm biosecurity Minimize movement by staff and visitors in and out of bird enclosures and between sites/other poultry farms. Ensure staff and visitors/contractors understand the site’s biosecurity requirements. Ensure footwear is cleaned before and after visiting a poultry house, using Defra approved disinfection at all entrances and exits. Clean and disinfect any vehicles and equipment that comes into contact with poultry. Limit or prevent contact with non-commercial poultry and birds including live bird markets. Inspect the flock daily for signs of disease and mortality. Know the signs of disease and how to report suspected notifiable illnesses. Provide good ventilation and maintain litter in a relatively dry condition to prevent growth environments for pathogenic microorganisms. Minimise the congregation of waterfowl and wild birds. Monitor wild bird detections as these may proceed farmed poultry outbreaks24. Handling Good hygiene practices are essential after handling live poultry or poultry products pre- and post-slaughter to prevent cross-contamination. Wash hands thoroughly before preparing, cooking or eating with warm soapy water Wash hands after using the toilet, handling animals or their waste, after emptying bins, touching phone, door handles etc. and after touching the eyes, nose or mouth Staff should not work or enter food handling areas if they are suffering from a disease likely to be transmitted through food or carrying a disease which may be transmitted through food, have skin infections, infected wounds or sores, or have diarrhoea Do not wash raw meat, to prevent the spread of bacteria and viruses onto hands, workstations and utensils Separate raw and cooked or ready to eat foods and use separate chopping boards etc. for raw foods Thoroughly clean all equipment and surrounding areas after handling raw poultry products Do not use raw or undercooked eggs from outbreak areas that will not be subjected to further cooking methods Use potable water which is heat-treated and/or disinfected, including for poultry production, since avian influenza may contaminate drinking water sources, such as reservoirs and rivers. Cooking Poultry meat and products should be cooked to at least 70oC 25, 26. Food Standards Agency (FSA) advice is to cook the food until a temperature of 70oC is reached for two minutes Eggs from poultry where outbreaks are occurring should be cooked until the whites and yolks are firm. Heath measures for trade The World Organisation for Animal Health (OIE) Terrestrial Animal Health Code (Terrestrial Code) specifies commodities that are safe for trade27.

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Institute of Food Science & Technology has authorised the publication of the following updated Information Statement on Avian influenza and food,

This updated Information Statement has been prepared by J Ralph Blanchfield, peer-reviewed by professional members of IFST and approved by the IFST Scientific Committee. 

The author is grateful to Professor Ian H Brown for valuable suggestions and an external review of this Information Statement.

This information statement is dated October 2020, replacing that of November 2013. 

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.