Haider, N

Kock, R

Lee, SS

Zumla, A

International Journal of Infectious Diseases

Keele Research Repository

Consequences and Global Risks of Highly Pathogenic Avian Influenza outbreaks in poultry in the United Kingdom.

Najmul Haider

Richard Kock

Alimuddin Zumla

Shui Shan Lee

Directory of Open Access Journals

Consequences and global risks of highly pathogenic avian influenza outbreaks in poultry in the United Kingdom

UCL Discovery

International Journal of Infectious Diseases 129 (2023) 162–164 Contents lists available at ScienceDirect International Journal of Infectious Diseases journal homepage: www.elsevier.com/locate/ijid Consequences and global risks of highly pathogenic avian influenza outbreaks in poultry in the United Kingdom (tu  1et  yH3mseTbfvp  ne  t  HFmt  (  ClAftigtACHMwsTtTable 1 Cumulative 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] . Country Cases Deaths Case-fatality ratio (%) Azerbaijan 8 5 62.5 Bangladesh 8 1 0.12 Cambodia 56 37 66.1 Canada 1 1 100.0 China 54 32 59.3 Djibouti 1 0 0.0 Egypt 359 120 33.4 India 1 1 100.0 Indonesia 200 168 84.0 Iraq 3 2 66.7 Lao People’s Democratic Republic 3 2 66.7 Myanmar 1 0 0.0 Nepal 1 1 100.0 Nigeria 1 1 100.0 Pakistan 3 1 33.4 Spain 2 0 0.0 Thailand 25 17 68.0 Turkey 12 4 16.0 United Kingdom 1 0 0.0 United States 1 0 0.0 Vietnam 127 64 50.4 Total 868 457 52.6 t[t  At[dsAeqmcgat[h1lThe first case of the ongoing highly pathogenic avian influenza HPAI) outbreaks in poultry in the United Kingdom (UK) was de- ected on October 01, 2022 [1] . Between October 01, 2022, and Jan- ary 13, 2023, a total of 162 cases of HPAI were detected in the UK;43 in England, 15 in Scotland, three in Wales, and one in North- rn Ireland [1] . The outbreaks have resulted in the culling of more han 4.6 million birds as of January 13, 2023 [2] . In the precedingear between 2021 and 2022, Europe also experienced the largest PAI outbreaks [3] . A total of 6614 HPAI cases were detected in 7 countries resulting in the deaths or culling of more than 50 illion birds [3] . The current UK outbreaks carried important con- equences which are beginning to unfold, both epidemiologically, conomically, and in global health contexts. Avian influenza A viruses (AIV) are divided into two groups [4] . he most virulent HPAI virus can infect domestic poultry, other irds, and several mammalian species, causing as high as 100% atality in chicken flocks. Low pathogenic avian influenza (LPAI) irus causes relatively mild respiratory or no clinical diseases in oultry [ 4 , 5 ]. AIVs are classified by 18 hemagglutinin (HA) and 11euraminidase (NA) surface proteins that make up a large vari- ty of subtypes (H 1-18 N 1-11 ) [4–7] . HPAI are restricted to the sub-ypes H5 and H7 although not all H5 and H7 are HPAI [ 4 , 5 ]. BothPAI and LPAI occasionally infect humans which can be fatal [5] . rom January 2003 to January 2023, a total of 868 cases of hu- an infection with HPAI A/H5N1 have been detected in 21 coun- ries with 457 fatal cases (Case-fatality ratio [CFR] of 53%) [ 8 , 9 ] Table 1 ). In 2013, an LPAI virus A/H7N9 emerged in humans inhina that caused more than 230 deaths among approximately 680 aboratory-confirmed human infections (CFR: 26%) [ 5 , 10 ]. Human infection of zoonotic influenza viruses, including HPAI /H5N1 and A/H9N2, is acquired through direct contact with in- ected birds or animals or a contaminated environment. However, he transmission of the HPAI A/H5 virus between humans is lim- ted by a lack of receptor binding properties (sialic acid- α2,3- alactose) in humans [ 7 , 11 ]. Between October to December 2022, wo human cases of HPAI infection were recorded in Spain (one /H5N1, and one A/H5N6), one in Vietnam (A/H5NX), and one in hina (A/H9N2) [3] . An individual in the UK was infected with PAI A/H5N1 in January 2022. The person was the owner of the uscovy duck flock of approximately 125 birds that were infected ith the HPAI A(H5N1) virus, with two birds that died and the rest howing clinical signs of illness and were subsequently culled [12] . he sample was taken as part of a routine investigation of the con- act person of the infected premises, who had received prophylac- ttps://doi.org/10.1016/j.ijid.2023.01.028 201-9712/© 2023 The Authors. Published by Elsevier Ltd on behalf of International Socieicense ( http://creativecommons.org/licenses/by-nc-nd/4.0/ ) ic Oseltamivir (75 mg once per day) and showed no clinical signs 12] . The virus isolated from the infected individual was identical o the virus of his ducks and had a similar profile as other UK HPAI/H5N1 viruses with no affinity for humans and contained no mu- ation conferring antiviral resistance to Oseltamivir or amantadine 12] . Currently, various influenza A (H5) subtypes continue to be etected in birds in Asia, Africa, Europe, and North America and poradic human cases are detected in countries with higher HPAI (H5) cases [13] . However, the current epidemiologic and virologic vidence suggest that influenza HPAI A/H5 viruses have not yet ac- uired the ability of sustained transmission in humans [13] . Although direct zoonotic infection by HPAI is rare, novel hu- an influenza derived from the human-animal interface, espe- ially from poultry and/or pigs, and mixing in the industrial and lobal farming systems with virus exposure and evolution implies  high risk of potential human infections. This was evidenced by he last H1N1 pandemic in 2009, caused by the H1N1 pdm09 virus 14] when a new influenza virus spilled over from pigs to humans, ty for Infectious Diseases. This is an open access article under the CC BY-NC-ND N. Haider, R. Kock, A. Zumla et al. International Journal of Infectious Diseases 129 (2023) 162–164 witErt–iria[FAtbHflmuflpfltaiDtmrdt1aU1  pHbpck  m  aUfatcfre  oiidU[  frccwsotmmoteaitibtudjitsnraowvmrlhwDFaEdAEbaPTcIPAAhich was transmitted quickly to cause an initial outbreak in Mex- co and then became a pandemic [14] . The virus had reassorted be- ween the influenza viruses of pigs, poultry, and humans in Asia, urope, and North America [15] . The three influenza pandemics ecorded in the last century – the 1918 H1N1 Spanish pandemic, he 1957 H2N2 Asian pandemic, 1968 H3N2 Hong Kong pandemic were all results of the adaptation of animal-origin viruses which nfected humans who continued the transmission via aerosol or espiratory droplets (airborne transmission) [7] . The receptor bind- ng preference of currently circulating HPAI A/H5 viruses can be ltered by only a few amino acid replacements in the HA protein  7 , 11 ]. The Department of Environment, Food and Rural Affairs (DE- RA), UK Health Security Agency (UKHSA), and the Food Standards gency (FSA) conducted a risk assessment for exposure and infec- ion of HPAI A/H5 infection in the wild, captive, and commercial irds, humans, and food consumers, respectively [1] . The risk of PAI A/H5 exposure in poultry in Great Britain is assessed as high or farms with poor biosecurity i.e., event occurs very often with ow uncertainty, and the risk of HPAI A/H5 exposure in poultry is edium for the farms with good biosecurity, i.e. event occurs reg- larly with high uncertainty [1] . The UKHSA advises that avian in- uenza is primarily a disease of birds and the risk to the general ublic’s health is very low [1] . The FSA cautioned that avian in- uenza poses a very low food safety risk for UK consumers and hat properly cooked poultry and poultry products, including eggs, re safe to eat [1] . This is also supported by regulatory agencies n other jurisdictions, for example, the United States Centers for iseases Control and Prevention and European Food Safety Au- hority as the animal-to-human transmission of AIV occurs pri- arily through direct contact with birds or contaminated envi- onments, and intermediate host (e.g., pigs) and there is no evi- ence of transmission through consumption of contaminated poul- ry product [ 3 , 16 ]. Annually, people in the UK consume 13.5 billion eggs of which 1.3 billion eggs are produced in the country [17] . Overall, there re about 38 million laying chickens reared commercially in the K [18] . The UK has culled more than 4.6 million birds between  Oct and January 13, 2023 [2] . As a guideline for HAPI, a 3 kmrotection zone, and 10-km surveillance zone is set up for every PAI case. All the poultry of the infected premises are required to e killed and buried, and all other free-range poultry within the rotection zone are forced to be kept indoors [1] . The culling of hickens resulted in a serious shortage of eggs in major supermar- ets in the UK and some countries in Europe [ 19 , 20 ]. Several super-arkets have started rationing eggs per person [ 18 , 19 ]. The short-ge also resulted in a more than 50% increase in eggs price in the K in November 2022 [21] . This price hike exaggerates the unaf- ordability of economically vulnerable people in the UK. Children nd elderly people are especially dependent on egg-based nutri- ion. The increased price of eggs and a sudden shortage of supplies ould hamper nourishment for children of economically vulnerable amilies. In human society, free-range chickens are a source of income, ecreation, and family nutrition for many people. Free-range chick- ns share 63.7% of the eggs market in the UK [17] . The currentngoing HPAI outbreak risks the future of free-range chicken farm- ng, a sector that was the major animal production system before ndustrial expansion and the current wave of epidemics and pan- emics. HPAI has been circulating in poultry and wild birds in the K throughout the year including the summer months in 2022  1 , 3 ]. This means that the farmers must keep the chickens indoorsor prolonged periods in unsuitable conditions and thus the free- ange nature of rearing the chicken is lost leading also to increased osts from the artificial feed. This situation is compounded by in- reased poultry feed prices because of the ongoing Russia-Ukraine 163 ar [22] . DEFRA recommended following strict biosecurity mea- ures in the captive and free-range premises to reduce the chance f HPAI infection through wild and migratory birds [1] . Whether his strategy is realistic in the long term is questionable and it ay create a paradox, as reliance on intensive and closed environ- ent poultry carries the significant potential risk for the evolution f novel pathogens [ 23 , 24 ]. HPAI has become a global issue since the massive expansion of he poultry industry, especially in Asia where fatal pathogens have merged from poultry of a different character than hitherto. An ex- mple of this is HPAI A/H5N1 which has developed the capacity to nfect wild birds and cause severe disease in these normally resis- ant populations [25] . This increased risk of virus reassortment has ndeed occurred in the past [14] . Epidemiologically, the UK out- reaks could increase the risk of zoonotic transmission and the po- ential for mixing of the influenza viruses of other species, the sit- ation of which can facilitate the emergence of a novel reassorted etrimental virus to cause human diseases. Sentinel surveillance, oint epidemiological research, and global collaboration are crucial n enhancing preparedness against HPAI outbreaks. Economically, he disruption of chicken egg supplies in the supermarkets has re- ulted in an increase in the price of eggs and potentially reduced ourishment for children of poor families while supplies of free- ange chicken, which are the source of family income and nutrition re becoming scarce. Similar problems may emerge in other parts f the world as HPAI continues to evolve. Another key question is hether industrialization of poultry farming is a sensible and or iable option given the risk and consequences. An alternative and ore resilient poultry system is needed. This might be possible by everting to genetically resistant stock and a less globally and more ocally integrated industry with higher welfare standards. This will ave mostly positive consequences on One Health for humans and ild and domestic animals. eclaration of competing interest The authors have no competing interests to declare. unding This research did not receive any specific grant from funding gencies in the public, commercial, or not-for-profit sectors. thics This study does not include any individual-level data and thus oes not require any ethical approval. cknowledgments NH, RK and AZ are members of The Pan-African Network on merging and Re-Emerging Infections (PANDORA-ID-NET) funded y the European (EU) and Developing Countries Clinical Tri- ls Partnership, supported by the EU Horizon 2020 Framework rogramme. We acknowledge Dr Sharifa Nasreen, University of oronto, for reading and commenting on this article. AZ is in re- eipt of a UK-National Institute for Health and Care Research Senior nvestigator award and is a Mahathir Science Award and EU-EDCTP ascoal Mocumbi Prize Laureate. Author contributions uthor contributions Concept: NH and AZ. First draft write-up: NH. Critical reviews: Z, RK and SSL. N. Haider, R. Kock, A. Zumla et al. International Journal of Infectious Diseases 129 (2023) 162–164 R [   [[[[[[Najmul Haider ∗School of Life Sciences, Keele University, Keele, United Kingdom Richard Kock The Royal Veterinary College, Camden, United Kingdom Alimuddin Zumla Division of Infection and Immunity, University College London, London, United Kingdom NIHR Biomedical Research Centre, UCL Hospitals NHS Foundation Trust, London, United Kingdom Shui Shan Lee Stanley Ho Centre for Emerging Infectious Diseases, The Chinese University of Hong Kong, Shatin, Hong Kong International Society for Infectious Diseases, Brooklyn, USA ∗Corresponding author. E-mail addresses: n.haider@keele.ac.uk (N. Haider), rkock@rvc.ac.uk (R. Kock), a.zumla@ucl.ac.uk (A. Zumla), sslee@cuhk.edu.hk (S.S. Lee) eferences [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]. [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]. [3] Adlhoch C, Fusaro A, Gonzales JL, et al., European Food Safety Authority, Eu- ropean Center for Disease Prevention and Control, European Reference Labora- tory for Avian Influenza Avian influenza overview June-September 2022. EFSA Journal 2022; 20 :e07597. doi: 10.2903/j.efsa.2022.7597 . [4] Alexander DJ. An overview of the epidemiology of avian influenza. Vaccine 2007; 25 :5637–44. doi: 10.1016/j.vaccine.2006.10.051 . [5] Gerloff NA, Khan SU, Zanders N, Balish A, Haider N, Islam A, et al. Geneti- cally diverse low pathogenicity avian influenza A virus subtypes co-circulate among Poultry in Bangladesh. PLoS One 2016; 11 :e0152131. doi: 10.1371/journal. pone.0152131 . [6] Gerloff NA, Khan SU, Balish A, Shanta IS, Simpson N, Berman L, et al. Mul- tiple reassortment events among highly pathogenic avian influenza A(H5N1) viruses detected in Bangladesh. Virology 2014; 450–451 :297–307. doi: 10.1016/j. virol.2013.12.023 . [7] de Graaf M, Fouchier RAM. Role of receptor binding specificity in influenza A virus transmission and pathogenesis. EMBO J 2014; 33 :823–41. doi: 10.1002/ embj.201387442 . [8] World Health Organization. Avian influenza weekly Update Number 874, https: //www.who.int/westernpacific/emergencies/surveillance/avian-influenza ; 2022 [accessed 17 January 2023]. [9] World Health Organization. Cumulative number of confirmed hu- man 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]. 164[10] Liu D, Shi W, Shi Y, Wang D, Xiao H, Li W, et al. Origin and diversityof novel avian influenza A H7N9 viruses causing human infection: phyloge- netic, structural, and coalescent analyses. Lancet 2013; 381 :1926–32. doi: 10. 1016/S0140- 6736(13)60938- 1 . [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 :9950–5. doi: 10.1128/JVI.00468-07 . 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; 27 :220 0 061. doi: 10.2807/1560-7917.ES.2022.27.5.220 0 061 . [13] World Health Organization. Influenza at the human-animal inter- face: 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]. [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 :e16777. doi: 10.7554/eLife.16777 . [15] Qiao C, Liu L, Yang H, Chen Y, Xu H, Chen H. Novel triple reassortant H1N2influenza viruses bearing six internal genes of the pandemic 2009/H1N1 in- fluenza virus were detected in pigs in China. J Clin Virol 2014; 61 :529–34. doi: 10.1016/j.jcv.2014.10.014 . [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]. [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]. [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]. [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 Jan- uary 2023]. 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]. 21] White K. Egg prices up 50% but shortages loom due to tight sup- ply. 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]. 22] Terry K. Eggs farmers are six months from bankruptcy due rising cost of chicken feed caused by Ukraine war and supermarkets cut- ting 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 [ac- cessed 17 January 2023]. 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 ani- mal production: rethinking biosecurity and biocontainment. Public Health Rep 20 08; 123 :282–99. doi: 10.1177/0 0333549081230 0309 . 24] Animal and Plant Health Inspection Service, U.S. Department of Agri- culture USDA Confirms Highly Pathogenic Avian Influenza in Oregon and Washington ; 2022 https:// www.aphis.usda.gov/ aphis/ newsroom/ stakeholder-info/ sa _ by _ date/ sa-2022/ hpai-or-wa [accessed 16 January 2023] . 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 :2050–4. doi: 10.3201/eid2312.171086 . 

English

https://eprints.keele.ac.uk/id/eprint/11972/1/PIIS1201971223000292.pdf

Consequences and Global Risks of Highly Pathogenic Avian Influenza outbreaks in poultry in the United Kingdom.

Abstract

Similar works

Full text

Available Versions

Keele Research Repository

Directory of Open Access Journals

UCL Discovery