Consequences and global risks of highly pathogenic avian influenza outbreaks in poultry in the United Kingdom
2023; Elsevier BV; Volume: 129; Linguagem: Inglês
10.1016/j.ijid.2023.01.028
ISSN1878-3511
AutoresNajmul Haider, Richard Kock, Alimuddin Zumla, Shui Shan Lee,
Tópico(s)Viral Infections and Vectors
Resumo•Ongoing HPAI outbreaks have resulted in the culling of >4.6 M birds in the UK.•The outbreak could increase the risk of zoonotic transmission.•Increase potential for mixing of the influenza viruses of other species.•The UK faces significant disruption of chicken egg supplies in the supermarkets.•Free-range chicken eggs are becoming scarce. The first case of the ongoing highly pathogenic avian influenza (HPAI) outbreaks in poultry in the United Kingdom (UK) was detected on October 01, 2022 [[1]DEFRA, American Public Health Association. Bird flu (avian influenza): latest situation in England, https://www.gov.uk/government/news/bird-flu-avian-influenza-latest-situation-in-england; 2023 [accessed 14 January 2023].Google Scholar]. Between October 01, 2022, and January 13, 2023, a total of 162 cases of HPAI were detected in the UK; 143 in England, 15 in Scotland, three in Wales, and one in Northern Ireland [[1]DEFRA, American Public Health Association. Bird flu (avian influenza): latest situation in England, https://www.gov.uk/government/news/bird-flu-avian-influenza-latest-situation-in-england; 2023 [accessed 14 January 2023].Google Scholar]. The outbreaks have resulted in the culling of more than 4.6 million birds as of January 13, 2023 [[2]World Organization of Animal Health. World Animal Health Information System- Quantitative data by World Region: Europe, country: United Kingdom, Animal Type: terrestrial, Disease: HPAI. 2022–2023, https://wahis.woah.org/#/dashboards/qd-dashboard; 2023 [accessed 14 January 2023].Google Scholar]. In the preceding year between 2021 and 2022, Europe also experienced the largest HPAI outbreaks [[3]Adlhoch C Fusaro A Gonzales JL et al.European Food Safety Authority, European Center for Disease Prevention and Control, European Reference Laboratory for Avian InfluenzaAvian influenza overview June-September 2022.EFSA Journal. 2022; 20: e07597https://doi.org/10.2903/j.efsa.2022.7597Crossref PubMed Scopus (22) Google Scholar]. A total of 6614 HPAI cases were detected in 37 countries resulting in the deaths or culling of more than 50 million birds [[3]Adlhoch C Fusaro A Gonzales JL et al.European Food Safety Authority, European Center for Disease Prevention and Control, European Reference Laboratory for Avian InfluenzaAvian influenza overview June-September 2022.EFSA Journal. 2022; 20: e07597https://doi.org/10.2903/j.efsa.2022.7597Crossref PubMed Scopus (22) Google Scholar]. The current UK outbreaks carried important consequences which are beginning to unfold, both epidemiologically, economically, and in global health contexts. Avian influenza A viruses (AIV) are divided into two groups [[4]Alexander DJ. An overview of the epidemiology of avian influenza.Vaccine. 2007; 25: 5637-5644https://doi.org/10.1016/j.vaccine.2006.10.051Crossref PubMed Scopus (635) Google Scholar]. The most virulent HPAI virus can infect domestic poultry, other birds, and several mammalian species, causing as high as 100% fatality in chicken flocks. Low pathogenic avian influenza (LPAI) virus causes relatively mild respiratory or no clinical diseases in poultry [[4]Alexander DJ. An overview of the epidemiology of avian influenza.Vaccine. 2007; 25: 5637-5644https://doi.org/10.1016/j.vaccine.2006.10.051Crossref PubMed Scopus (635) Google Scholar,[5]Gerloff NA Khan SU Zanders N Balish A Haider N Islam A et al.Genetically diverse low pathogenicity avian influenza A virus subtypes co-circulate among Poultry in Bangladesh.PLoS One. 2016; 11e0152131https://doi.org/10.1371/journal.pone.0152131Crossref PubMed Scopus (34) Google Scholar]. AIVs are classified by 18 hemagglutinin (HA) and 11 neuraminidase (NA) surface proteins that make up a large variety of subtypes (H1-18 N1-11) [4Alexander DJ. 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HPAI are restricted to the subtypes H5 and H7 although not all H5 and H7 are HPAI [[4]Alexander DJ. An overview of the epidemiology of avian influenza.Vaccine. 2007; 25: 5637-5644https://doi.org/10.1016/j.vaccine.2006.10.051Crossref PubMed Scopus (635) Google Scholar,[5]Gerloff NA Khan SU Zanders N Balish A Haider N Islam A et al.Genetically diverse low pathogenicity avian influenza A virus subtypes co-circulate among Poultry in Bangladesh.PLoS One. 2016; 11e0152131https://doi.org/10.1371/journal.pone.0152131Crossref PubMed Scopus (34) Google Scholar]. Both HPAI and LPAI occasionally infect humans which can be fatal [[5]Gerloff NA Khan SU Zanders N Balish A Haider N Islam A et al.Genetically diverse low pathogenicity avian influenza A virus subtypes co-circulate among Poultry in Bangladesh.PLoS One. 2016; 11e0152131https://doi.org/10.1371/journal.pone.0152131Crossref PubMed Scopus (34) Google Scholar]. From January 2003 to January 2023, a total of 868 cases of human infection with HPAI A/H5N1 have been detected in 21 countries with 457 fatal cases (Case-fatality ratio [CFR] of 53%) [[8]World Health Organization. Avian influenza weekly Update Number 874, https://www.who.int/westernpacific/emergencies/surveillance/avian-influenza; 2022 [accessed 17 January 2023].Google Scholar,[9]World Health Organization. Cumulative number of confirmed human cases for avian influenza A(H5N1) reported to WHO, 2003–2023, 5 January 2023, https://www.who.int/publications/m/item/cumulative-number-of-confirmed-human-cases-for-avian-influenza-a(h5n1)-reported-to-who-2003-2022-5-jan-2023; 2023 [accessed 17 January 2023].Google Scholar] (Table 1). In 2013, an LPAI virus A/H7N9 emerged in humans in China that caused more than 230 deaths among approximately 680 laboratory-confirmed human infections (CFR: 26%) [[5]Gerloff NA Khan SU Zanders N Balish A Haider N Islam A et al.Genetically diverse low pathogenicity avian influenza A virus subtypes co-circulate among Poultry in Bangladesh.PLoS One. 2016; 11e0152131https://doi.org/10.1371/journal.pone.0152131Crossref PubMed Scopus (34) Google Scholar,[10]Liu D Shi W Shi Y Wang D Xiao H Li W et al.Origin and diversity of novel avian influenza A H7N9 viruses causing human infection: phylogenetic, structural, and coalescent analyses.Lancet. 2013; 381: 1926-1932https://doi.org/10.1016/S0140-6736(13)60938-1Abstract Full Text Full Text PDF PubMed Scopus (487) Google Scholar].Table 1Cumulative number of confirmed human cases of avian influenza A(H5N1) reported to World Health Organization, 2003-2022 (until 25 Nov 2022). Adapted from World Health Organization [9]World Health Organization. Cumulative number of confirmed human cases for avian influenza A(H5N1) reported to WHO, 2003–2023, 5 January 2023, https://www.who.int/publications/m/item/cumulative-number-of-confirmed-human-cases-for-avian-influenza-a(h5n1)-reported-to-who-2003-2022-5-jan-2023; 2023 [accessed 17 January 2023].Google Scholar.CountryCasesDeathsCase-fatality ratio (%)Azerbaijan8562.5Bangladesh810.12Cambodia563766.1Canada11100.0China543259.3Djibouti100.0Egypt35912033.4India11100.0Indonesia20016884.0Iraq3266.7Lao People's Democratic Republic3266.7Myanmar100.0Nepal11100.0Nigeria11100.0Pakistan3133.4Spain200.0Thailand251768.0Turkey12416.0United Kingdom100.0United States100.0Vietnam1276450.4Total86845752.6 Open table in a new tab Human infection of zoonotic influenza viruses, including HPAI A/H5N1 and A/H9N2, is acquired through direct contact with infected birds or animals or a contaminated environment. However, the transmission of the HPAI A/H5 virus between humans is limited by a lack of receptor binding properties (sialic acid-α2,3-galactose) in humans [[7]de Graaf M Fouchier RAM. Role of receptor binding specificity in influenza A virus transmission and pathogenesis.EMBO J. 2014; 33: 823-841https://doi.org/10.1002/embj.201387442Crossref PubMed Scopus (289) Google Scholar,[11]Auewarakul P Suptawiwat O Kongchanagul A Sangma C Suzuki Y Ungchusak K et al.An avian influenza H5N1 virus that binds to a human-type receptor.J Virol. 2007; 81: 9950-9955https://doi.org/10.1128/JVI.00468-07Crossref PubMed Scopus (163) Google Scholar]. Between October to December 2022, two human cases of HPAI infection were recorded in Spain (one A/H5N1, and one A/H5N6), one in Vietnam (A/H5NX), and one in China (A/H9N2) [[3]Adlhoch C Fusaro A Gonzales JL et al.European Food Safety Authority, European Center for Disease Prevention and Control, European Reference Laboratory for Avian InfluenzaAvian influenza overview June-September 2022.EFSA Journal. 2022; 20: e07597https://doi.org/10.2903/j.efsa.2022.7597Crossref PubMed Scopus (22) Google Scholar]. An individual in the UK was infected with HPAI A/H5N1 in January 2022. The person was the owner of the Muscovy duck flock of approximately 125 birds that were infected with the HPAI A(H5N1) virus, with two birds that died and the rest showing clinical signs of illness and were subsequently culled [[12]Oliver I Roberts J Brown CS Byrne AM Mellon D Hansen R de et al.A case of avian influenza A(H5N1) in England, January 2022.Euro Surveill. 2022; 272200061https://doi.org/10.2807/1560-7917.ES.2022.27.5.2200061Crossref PubMed Scopus (26) Google Scholar]. The sample was taken as part of a routine investigation of the contact person of the infected premises, who had received prophylactic Oseltamivir (75 mg once per day) and showed no clinical signs [[12]Oliver I Roberts J Brown CS Byrne AM Mellon D Hansen R de et al.A case of avian influenza A(H5N1) in England, January 2022.Euro Surveill. 2022; 272200061https://doi.org/10.2807/1560-7917.ES.2022.27.5.2200061Crossref PubMed Scopus (26) Google Scholar]. The virus isolated from the infected individual was identical to the virus of his ducks and had a similar profile as other UK HPAI A/H5N1 viruses with no affinity for humans and contained no mutation conferring antiviral resistance to Oseltamivir or amantadine [[12]Oliver I Roberts J Brown CS Byrne AM Mellon D Hansen R de et al.A case of avian influenza A(H5N1) in England, January 2022.Euro Surveill. 2022; 272200061https://doi.org/10.2807/1560-7917.ES.2022.27.5.2200061Crossref PubMed Scopus (26) Google Scholar]. Currently, various influenza A (H5) subtypes continue to be detected in birds in Asia, Africa, Europe, and North America and sporadic human cases are detected in countries with higher HPAI A(H5) cases [[13]World Health Organization. Influenza at the human-animal interface: summary and risk assessment, 11 November 2022, https://www.who.int/publications/m/item/influenza-at-the-human-animal-interface-summary-and-assessment-11-nov-2022; 2022 [accessed 14 January 2023].Google Scholar]. However, the current epidemiologic and virologic evidence suggest that influenza HPAI A/H5 viruses have not yet acquired the ability of sustained transmission in humans [[13]World Health Organization. Influenza at the human-animal interface: summary and risk assessment, 11 November 2022, https://www.who.int/publications/m/item/influenza-at-the-human-animal-interface-summary-and-assessment-11-nov-2022; 2022 [accessed 14 January 2023].Google Scholar]. Although direct zoonotic infection by HPAI is rare, novel human influenza derived from the human-animal interface, especially from poultry and/or pigs, and mixing in the industrial and global farming systems with virus exposure and evolution implies a high risk of potential human infections. This was evidenced by the last H1N1 pandemic in 2009, caused by the H1N1 pdm09 virus [[14]Mena I Nelson MI Quezada-Monroy F Dutta J Cortes-Fernández R Lara-Puente JH et al.Origins of the 2009 H1N1 influenza pandemic in swine in Mexico.eLife. 2016; 5: e16777https://doi.org/10.7554/eLife.16777Crossref PubMed Scopus (182) Google Scholar] when a new influenza virus spilled over from pigs to humans, which was transmitted quickly to cause an initial outbreak in Mexico and then became a pandemic [[14]Mena I Nelson MI Quezada-Monroy F Dutta J Cortes-Fernández R Lara-Puente JH et al.Origins of the 2009 H1N1 influenza pandemic in swine in Mexico.eLife. 2016; 5: e16777https://doi.org/10.7554/eLife.16777Crossref PubMed Scopus (182) Google Scholar]. The virus had reassorted between the influenza viruses of pigs, poultry, and humans in Asia, Europe, and North America [[15]Qiao C Liu L Yang H Chen Y Xu H Chen H. Novel triple reassortant H1N2 influenza viruses bearing six internal genes of the pandemic 2009/H1N1 influenza virus were detected in pigs in China.J Clin Virol. 2014; 61: 529-534https://doi.org/10.1016/j.jcv.2014.10.014Crossref PubMed Scopus (23) Google Scholar]. The three influenza pandemics recorded in the last century – the 1918 H1N1 Spanish pandemic, the 1957 H2N2 Asian pandemic, 1968 H3N2 Hong Kong pandemic – were all results of the adaptation of animal-origin viruses which infected humans who continued the transmission via aerosol or respiratory droplets (airborne transmission) [[7]de Graaf M Fouchier RAM. Role of receptor binding specificity in influenza A virus transmission and pathogenesis.EMBO J. 2014; 33: 823-841https://doi.org/10.1002/embj.201387442Crossref PubMed Scopus (289) Google Scholar]. The receptor binding preference of currently circulating HPAI A/H5 viruses can be altered by only a few amino acid replacements in the HA protein [[7]de Graaf M Fouchier RAM. Role of receptor binding specificity in influenza A virus transmission and pathogenesis.EMBO J. 2014; 33: 823-841https://doi.org/10.1002/embj.201387442Crossref PubMed Scopus (289) Google Scholar,[11]Auewarakul P Suptawiwat O Kongchanagul A Sangma C Suzuki Y Ungchusak K et al.An avian influenza H5N1 virus that binds to a human-type receptor.J Virol. 2007; 81: 9950-9955https://doi.org/10.1128/JVI.00468-07Crossref PubMed Scopus (163) Google Scholar]. The Department of Environment, Food and Rural Affairs (DEFRA), UK Health Security Agency (UKHSA), and the Food Standards Agency (FSA) conducted a risk assessment for exposure and infection of HPAI A/H5 infection in the wild, captive, and commercial birds, humans, and food consumers, respectively [[1]DEFRA, American Public Health Association. Bird flu (avian influenza): latest situation in England, https://www.gov.uk/government/news/bird-flu-avian-influenza-latest-situation-in-england; 2023 [accessed 14 January 2023].Google Scholar]. The risk of HPAI A/H5 exposure in poultry in Great Britain is assessed as high for farms with poor biosecurity i.e., event occurs very often with low uncertainty, and the risk of HPAI A/H5 exposure in poultry is medium for the farms with good biosecurity, i.e. event occurs regularly with high uncertainty [[1]DEFRA, American Public Health Association. Bird flu (avian influenza): latest situation in England, https://www.gov.uk/government/news/bird-flu-avian-influenza-latest-situation-in-england; 2023 [accessed 14 January 2023].Google Scholar]. The UKHSA advises that avian influenza is primarily a disease of birds and the risk to the general public's health is very low [[1]DEFRA, American Public Health Association. Bird flu (avian influenza): latest situation in England, https://www.gov.uk/government/news/bird-flu-avian-influenza-latest-situation-in-england; 2023 [accessed 14 January 2023].Google Scholar]. The FSA cautioned that avian influenza poses a very low food safety risk for UK consumers and that properly cooked poultry and poultry products, including eggs, are safe to eat [[1]DEFRA, American Public Health Association. Bird flu (avian influenza): latest situation in England, https://www.gov.uk/government/news/bird-flu-avian-influenza-latest-situation-in-england; 2023 [accessed 14 January 2023].Google Scholar]. This is also supported by regulatory agencies in other jurisdictions, for example, the United States Centers for Diseases Control and Prevention and European Food Safety Authority as the animal-to-human transmission of AIV occurs primarily through direct contact with birds or contaminated environments, and intermediate host (e.g., pigs) and there is no evidence of transmission through consumption of contaminated poultry product [[3]Adlhoch C Fusaro A Gonzales JL et al.European Food Safety Authority, European Center for Disease Prevention and Control, European Reference Laboratory for Avian InfluenzaAvian influenza overview June-September 2022.EFSA Journal. 2022; 20: e07597https://doi.org/10.2903/j.efsa.2022.7597Crossref PubMed Scopus (22) Google Scholar,[16]US Centers for Disease Control and Prevention. Information on bird flu, https://www.cdc.gov/flu/avianflu/index.htm; 2023 [accessed 16 January 2023].Google Scholar]. Annually, people in the UK consume 13.5 billion eggs of which 11.3 billion eggs are produced in the country [[17]Egg Info, British lion eggs. Egg Info: industry data for 2021, https://www.egginfo.co.uk/egg-facts-and-figures/industry-information/data; 2022 [accessed 2023 Jan 14].Google Scholar]. Overall, there are about 38 million laying chickens reared commercially in the UK [[18]Loth S. UK egg shortage: who's rationing packs, egg safety warning and what the problem is, Which? News, https://www.which.co.uk/news/article/uk-egg-shortage-whos-rationing-packs-egg-safety-warning-and-what-the-problem-is-aD2o92E97swV; 2022 [accessed 17 January 2023].Google Scholar]. The UK has culled more than 4.6 million birds between 1 Oct and January 13, 2023 [[2]World Organization of Animal Health. World Animal Health Information System- Quantitative data by World Region: Europe, country: United Kingdom, Animal Type: terrestrial, Disease: HPAI. 2022–2023, https://wahis.woah.org/#/dashboards/qd-dashboard; 2023 [accessed 14 January 2023].Google Scholar]. As a guideline for HAPI, a 3 km protection zone, and 10-km surveillance zone is set up for every HPAI case. All the poultry of the infected premises are required to be killed and buried, and all other free-range poultry within the protection zone are forced to be kept indoors [[1]DEFRA, American Public Health Association. Bird flu (avian influenza): latest situation in England, https://www.gov.uk/government/news/bird-flu-avian-influenza-latest-situation-in-england; 2023 [accessed 14 January 2023].Google Scholar]. The culling of chickens resulted in a serious shortage of eggs in major supermarkets in the UK and some countries in Europe [[19]Russell R. Egg shortages: what's causing the problem and how long will it last? BBC, https://www.bbc.com/news/explainers-63778665; 2022 [accessed 17 January 2023].Google Scholar,[20]The local. Why there might be an egg shortage in France: not un œuf! The local, https://www.thelocal.fr/20221115/not-un-ouef-why-there-might-be-an-egg-shortage-in-france/; 2022 [accessed 14 January 2023].Google Scholar]. Several supermarkets have started rationing eggs per person [[18]Loth S. UK egg shortage: who's rationing packs, egg safety warning and what the problem is, Which? News, https://www.which.co.uk/news/article/uk-egg-shortage-whos-rationing-packs-egg-safety-warning-and-what-the-problem-is-aD2o92E97swV; 2022 [accessed 17 January 2023].Google Scholar,[19]Russell R. Egg shortages: what's causing the problem and how long will it last? BBC, https://www.bbc.com/news/explainers-63778665; 2022 [accessed 17 January 2023].Google Scholar]. The shortage also resulted in a more than 50% increase in eggs price in the UK in November 2022 [[21]White K. Egg prices up 50% but shortages loom due to tight supply. Grocer, https://www.thegrocer.co.uk/eggs-and-poultry/egg-prices-up-50-but-shortages-loom-due-to-tight-supply/673374.article; 2022 [accessed 17 January 2023].Google Scholar]. This price hike exaggerates the unaffordability of economically vulnerable people in the UK. Children and elderly people are especially dependent on egg-based nutrition. The increased price of eggs and a sudden shortage of supplies could hamper nourishment for children of economically vulnerable families. In human society, free-range chickens are a source of income, recreation, and family nutrition for many people. Free-range chickens share 63.7% of the eggs market in the UK [[17]Egg Info, British lion eggs. Egg Info: industry data for 2021, https://www.egginfo.co.uk/egg-facts-and-figures/industry-information/data; 2022 [accessed 2023 Jan 14].Google Scholar]. The current ongoing HPAI outbreak risks the future of free-range chicken farming, a sector that was the major animal production system before industrial expansion and the current wave of epidemics and pandemics. HPAI has been circulating in poultry and wild birds in the UK throughout the year including the summer months in 2022 [[1]DEFRA, American Public Health Association. Bird flu (avian influenza): latest situation in England, https://www.gov.uk/government/news/bird-flu-avian-influenza-latest-situation-in-england; 2023 [accessed 14 January 2023].Google Scholar,[3]Adlhoch C Fusaro A Gonzales JL et al.European Food Safety Authority, European Center for Disease Prevention and Control, European Reference Laboratory for Avian InfluenzaAvian influenza overview June-September 2022.EFSA Journal. 2022; 20: e07597https://doi.org/10.2903/j.efsa.2022.7597Crossref PubMed Scopus (22) Google Scholar]. This means that the farmers must keep the chickens indoors for prolonged periods in unsuitable conditions and thus the free-range nature of rearing the chicken is lost leading also to increased costs from the artificial feed. This situation is compounded by increased poultry feed prices because of the ongoing Russia-Ukraine war [[22]Terry K. Eggs farmers are six months from bankruptcy due rising cost of chicken feed caused by Ukraine war and supermarkets cutting prices amid cost-of-living crisis, industry experts warn. Mail Online, https://www.dailymail.co.uk/news/article-10777831/Eggs-farmers-six-months-bankruptcy-rising-cost-chicken-feed-caused-Ukraine-war.html; 2022 [accessed 17 January 2023].Google Scholar]. DEFRA recommended following strict biosecurity measures in the captive and free-range premises to reduce the chance of HPAI infection through wild and migratory birds [[1]DEFRA, American Public Health Association. Bird flu (avian influenza): latest situation in England, https://www.gov.uk/government/news/bird-flu-avian-influenza-latest-situation-in-england; 2023 [accessed 14 January 2023].Google Scholar]. Whether this strategy is realistic in the long term is questionable and it may create a paradox, as reliance on intensive and closed environment poultry carries the significant potential risk for the evolution of novel pathogens [[23]Graham JP Leibler JH Price LB Otte JM Pfeiffer DU Tiensin T et al.The animal-human interface and infectious disease in industrial food animal production: rethinking biosecurity and biocontainment.Public Health Rep. 2008; 123: 282-299https://doi.org/10.1177/003335490812300309Crossref PubMed Scopus (170) Google Scholar,[24]Animal and Plant Health Inspection Service, U.S. Department of AgricultureUSDA Confirms Highly Pathogenic Avian Influenza in Oregon and Washington.2022https://www.aphis.usda.gov/aphis/newsroom/stakeholder-info/sa_by_date/sa-2022/hpai-or-waGoogle Scholar]. HPAI has become a global issue since the massive expansion of the poultry industry, especially in Asia where fatal pathogens have emerged from poultry of a different character than hitherto. An example of this is HPAI A/H5N1 which has developed the capacity to infect wild birds and cause severe disease in these normally resistant populations [[25]Kleyheeg E Slaterus R Bodewes R Rijks JM Spierenburg MAH Beerens N et al.Deaths among wild birds during highly pathogenic avian influenza A(H5N8) virus outbreak, the Netherlands.Emerg Infect Dis. 2017; 23: 2050-2054https://doi.org/10.3201/eid2312.171086Crossref PubMed Scopus (55) Google Scholar]. This increased risk of virus reassortment has indeed occurred in the past [[14]Mena I Nelson MI Quezada-Monroy F Dutta J Cortes-Fernández R Lara-Puente JH et al.Origins of the 2009 H1N1 influenza pandemic in swine in Mexico.eLife. 2016; 5: e16777https://doi.org/10.7554/eLife.16777Crossref PubMed Scopus (182) Google Scholar]. Epidemiologically, the UK outbreaks could increase the risk of zoonotic transmission and the potential for mixing of the influenza viruses of other species, the situation of which can facilitate the emergence of a novel reassorted detrimental virus to cause human diseases. Sentinel surveillance, joint epidemiological research, and global collaboration are crucial in enhancing preparedness against HPAI outbreaks. Economically, the disruption of chicken egg supplies in the supermarkets has resulted in an increase in the price of eggs and potentially reduced nourishment for children of poor families while supplies of free-range chicken, which are the source of family income and nutrition are becoming scarce. Similar problems may emerge in other parts of the world as HPAI continues to evolve. Another key question is whether industrialization of poultry farming is a sensible and or viable option given the risk and consequences. An alternative and more resilient poultry system is needed. This might be possible by reverting to genetically resistant stock and a less globally and more locally integrated industry with higher welfare standards. This will have mostly positive consequences on One Health for humans and wild and domestic animals. The authors have no competing interests to declare. This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.
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