SSRN Id4758165

1 The risk of acquiring avian influenza from commercial poultry products and
2 hen eggs: a qualitative assessment
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3 Erica Kintz1, Wioleta J. Trzaska1, Elaine Pegg1, Wendy Perry1, Alexander W Tucker2,
4 Alec Kyriakides3, Dragan Antic4, Kathryn Callaghan1, Anthony J. Wilson1
5 1. Food Standards Agency, UK
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6 2. Department of Veterinary Medicine, University of Cambridge, UK
7 3. Independent Food Safety Consultant, UK
8 4. Institute of Infection, Veterinary and Ecological Sciences, University of
9 Liverpool, UK
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11 Corresponding author: Erica Kintz (erica.kintz@food.gov.uk)
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12 Short title: Acquiring avian influenza from poultry products
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14 Highlights:
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16
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Please use 'Highlights' in the file name and include 3 to 5 bullet points (maximum 85
characters, including spaces, per bullet point).
17  Concern avian influenza outbreak would increase risk of transmission from
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18 food.
19  No new evidence that food serves as a source for human AI infections
20 identified.
21  Risk to UK consumers from poultry products remains very low overall.
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This preprint research paper has not been peer reviewed. Electronic copy available at: https://ssrn.com/abstract=4758165
22 Abstract (up to 400 words)
23 High pathogenicity and low pathogenicity avian influenza (HPAI and LPAI)
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24 viruses primarily infect birds, but they can also cause illness in other species,
25 including humans. Some avian influenza (AI) strains can cause fatality rates of over
26 50% in human infections. In October 2021, there was a substantial increase in the
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27 number of AI infections reported in birds in the UK. Given concerns that more
28 contaminated poultry products might reach retail, a risk assessment was performed
29 to ensure that advice relating to the handling and consumption of these products
30 remained appropriate.
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31 The products considered in this risk assessment were commercial chicken
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32 and turkey products, farmed duck and geese products, and table eggs. The risk
33 pathway included the likelihood an infected flock would be sent for further
34 processing, whether that product would be released to retail after inspection, viral
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36
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survival during distribution and storage, and the ability of AI virus to infect humans
via the gastrointestinal route. Data was obtained from literature searches and FSA
37 surveys.
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38 The risk assessments determined that the risk of acquiring AI from poultry
39 products for the UK population from handling and consuming commercial chicken or
40 turkey products was negligible with low uncertainty, and for farmed duck and
41 geese products was very low with medium uncertainty. The likelihood of infection
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42 for people in the UK from handling and consuming hen table eggs was very low with
43 low uncertainty. The uncertainty rankings relate to the differing amounts of data
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44 available for each group of poultry products. The severity of illness in humans from
45 AI infection was considered high with medium uncertainty. The conclusions of this
46 risk assessment for UK consumers largely reflected advice and assessments from
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47 other countries and previous UK assessments. Given this, current guidance for
48 handling and consuming poultry products was considered appropriate despite the
49 increase in infections in birds during the 2022/22 and 2022/23 avian flu seasons.
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50
51 Keywords
52 Avian influenza, qualitative risk assessment, exposure assessment, hazard
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53 characterisation, risk characterisation, commercial poultry, eggs.
54 Introduction
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55 Avian influenza (AI) viruses cause infections primarily in bird species,
56 although they are capable of spill-over infections into mammalian species, including
57 humans. Many different strains of AI viruses are found in birds, but they can be
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58 divided into two groups based on their virulence in poultry: high pathogenicity (HPAI)
59 and low pathogenicity (LPAI); both are capable of quickly spreading through a flock.
60 Mutations from LPAI to HPAI are possible and have been described in Australia, the
61 Netherlands, UK and Germany (Byrne et al., 2021). HPAI results in high death rates
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62 (up to 100% mortality within 48 hours) in some poultry species such as chickens and
63 turkeys, while LPAI viruses may cause no disease or only mild clinical signs (such as
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64 ruffled feathers and a drop in egg production) and may go undetected (Liu et al.,
65 2021).
66 The vast majority of human cases have reported close contact with poultry;
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67 there is no reported evidence of sustained human-to-human transmission (WHO,
68 2020). It’s worth noting that LPAI and HPAI refers only to the specific criteria in
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69 infected poultry, not the severity of illness with human infections (CDC, 2022a).
70 Certain strains of AI have been associated with human case fatality rates of over
71 50% (WHO, 2022a). The primary risk factor for human infection appears to be direct
72 or indirect exposure to infected live or dead poultry or contaminated environments,
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73 such as live bird markets. Slaughtering, defeathering, handling carcasses of infected

74 poultry, and preparing poultry for consumption, especially in household settings, are
75 also likely to be risk factors (WHO, 2020). There is no evidence to suggest that AI
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76 viruses can be transmitted to humans through properly handled and cooked poultry
77 or eggs. H5N1 human cases have been linked to consumption of dishes made with
78 raw, contaminated poultry blood (WHO, 2018).
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79 From October 2021, there began a substantial increase in the number of AI

80 infections reported both at commercial premises and in wild birds in the UK. The
81 most recent Food Standards Agency (FSA) assessment on the risk to consumers of
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82 exposure to AI from the food chain was in 2015 (ACMSF, 2015). Since the increase
83 in infections in birds and flocks may lead to an increased likelihood that poultry
84 products from infected birds are entering the retail market, an updated risk
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85 assessment was performed to ensure that advice relating to the consumption of
86 poultry products is still appropriate. This risk assessment did not focus on the
87 currently circulating outbreak strain but considered any AI virus.
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88 This assessment considered the risk of consumers acquiring an AI infection
89 from poultry products, including commercial chicken and turkey, farmed duck and
90 geese, and hen table eggs. The farm to fork risk pathway spanned the probability
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91 that infected animals would be sent for processing, to the ability of AI to cause
92 infections in humans via the gastrointestinal route.
93 Methods
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94 Risk Assessment Framework
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95 This risk assessment was conducted following the Codex Alimentarius’s
96 “Principles and Guidelines for the Conduct of Microbiological Risk Assessment”
97 (Codex Alimentarius Commission, 2014). The risk characterisation section followed
98 multidimensional representation of risk guidelines established by the Advisory
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Committee on the Microbiological Safety of Food (ACMSF), where the frequency of
100 occurrence and severity of detriment are considered separately alongside the
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101 associated uncertainties, following well established qualitative risk assessment
102 scales (ACMSF, 2020).
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104 Risk Question, Scope and Assumptions
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105 What is the risk to consumers, on a population basis, of becoming ill with AI viruses
106 via consumer handling of poultry products and food consumption, specifically of
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107 commercial chicken and turkey, farmed duck and geese, and hen eggs, during an AI
108 season?
109 In Scope
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110 • Any AI virus. This risk assessment is not focused solely on the HPAI H5N1 clade
111 2.3.4.4b circulating in the UK during the 2021/22 and 2022/23 AI seasons.
112 • Meat from commercial poultry production
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113 • Table eggs from UK hen laying flocks

114 • Food made at home using lightly cooked/raw UK hen eggs
115 • Any of the above poultry products consumed less than thoroughly cooked
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116 • Cross-contamination from any of the above products

117 Out of Scope
118 • Animal health risks of acquiring AI
119 • Occupational exposure from commercial poultry production
120 • Exposure to birds outside the context of handling of commercially-prepared poultry
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121 products or their consumption. The risk from general exposure to birds is considered
122 by the UKHSA risk assessment (UKHSA, 2023).
123 • Wild game birds. This is considered in the full FSA risk assessment (FSA, 2023).
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124 • Preparation and consumption of poultry products from backyard flocks. This is
125 considered in the full FSA risk assessment (FSA, 2023).
126 • Poultry products cooked by businesses to be consumed ready-to-eat.
127 • Eggs other than hen table eggs.
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128 • Imported poultry products.
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129 Key Assumptions
130 In reviewing the evidence to determine the risk to humans of exposure to AI from
131 poultry products, several key assumptions were made to assist in drawing
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133
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conclusions when a lack of data was available. These included:
• Uncharacterised strains of HPAI or LPAI will behave similarly to strains for which
134 clinical signs in birds, viral distribution in tissues, and viral survival have been
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135 studied.
136 • In bird species where AI infection has not been well characterised, that these birds
137 would react to AI infection in a manner similar to well-studied, related species (for
138 example, same family or order) with regards to development of clinical signs and
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139 viral distribution within tissues.

140 • That AI viruses would behave similarly to viruses from previous AI outbreaks in
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141 their ability to mutate and/or transmit between species.

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143 Data Collection
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144 Evidence to support the risk assessment was obtained from a systematic literature
145 search performed in November and December 2022. Pubmed, Scopus and Science
146 Direct were searched using the search terms: ((avian influenza OR AI) AND (product
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147 or topic of interest)) (please see Supplemental File #1 for the full list of products and
148 topics covered in the search strategy). Zotero was used to manage citations and
149 remove duplicates. A grey literature search was also performed in Google using
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150 similar search terms and the first 100 references screened. Grey literature was also
151 obtained from the gov.uk and the nationalarchives.gov.uk websites. Bibliographies of
152 included studies were also scanned to identify additional sources. Consumption data
153 was acquired from the FSA’s National Diet and Nutrition Survey and Food & You 2
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154 survey (FSA, 2021; PHE and FSA, 2020).
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156 Quality Assurance
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157 Internal review of the FSA risk assessment was performed by senior leaders
158 of the microbiological risk assessment team of the FSA and staff with experience in
159 the area from the Animal Plant and Health Agency (APHA) (listed in the
160 Acknowledgements). Members of the Newly Emerging Pathogens subgroup of the
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161 ACMSF provided external review of the risk assessment in February 2023.
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162
163 Results
164 As the hazard was identified in the risk question, a hazard identification
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165 section is not presented. The exposure assessment considered the frequency of
166 occurrence for AI infections in humans considering infections in flocks on the farm all
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167 the way to the ability of the virus to cause infection via the gastrointestinal route
168 (Figure 1). Given the incomplete data for several sections of the risk pathway,
169 particularly human oral infectious dose, and the fact that this risk assessment was to
170 support risk management advice during an ongoing outbreak in the bird population, a
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171 qualitative assessment was performed to ensure a rapid response.

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173
174 Figure 1: Overall risk pathway for the different poultry products. The stage of
175 food chain, from the farm through to consumption and including the ability of the AI
176 virus to cause infection, is at the top of the figure. Boxes and arrows filled in grey are
177 opportunities for the virus to be removed from retail or from the product.
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178
179 Hazard Characterisation
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180 In humans, AI symptoms range from a mild flu-like illness, sometimes with
181 conjunctivitis (red, sore, discharging eyes), diarrhoea and abdominal pain, to a
182 severe respiratory illness with breathing difficulties and pneumonia (NHS, 2018).
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183 Both LPAI and HPAI virus strains can cause this range of symptoms and both types
184 have caused fatal infections in humans (WHO, 2022a). The incubation period in
185 humans is generally 3-5 days but can be longer (NHS, 2018).
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186 Although AI does not infect people easily and is not usually spread from
187 person to person, there have been cases of infections in humans, with high mortality
188 in some instances. The first laboratory-confirmed case in a human occurred in 1997,
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189 when H5N1 was detected in a patient in China (Wang et al., 2021). A majority of AI
190 cases in humans come from the Western Pacific Region, including China, likely due
191 to the widespread practice of keeping poultry in the backyard and the live poultry
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192 markets common in the region (Skufca et al., 2022). However, since 2003, AI has
193 travelled out of the region and caused human infections all over the world (Wang et
194 al., 2021).
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195 AI H7N9 has caused the largest number of human infections worldwide, with
196 1,568 cases reported and 616 deaths, giving a 39% case-fatality rate; no human AI
197 infections with an H7N9 strain have been reported since 2019 (EFSA, 2023; WHO,
198 2023a). Following that, AI H5N1 has caused 868 cases worldwide in humans with
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199 457 deaths, giving a 53% case fatality rate (WHO, 2022b). AI H5N6 has also been
200 associated with a high case fatality rate of 40% (83 cases and 33 deaths), although
201 this strain has not been reported in humans outside of the Western Pacific Region
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202 (EFSA, 2023; WHO, 2023a).
203 Other AI subtypes have been associated with human infections but either are
204 not associated with a high case fatality rate or have caused a very small number of
205 human infections worldwide. For example, AI H9N2 has been responsible for 115
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206 human cases of AI but with only two reported fatalities. Between February and May
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207 2003, an outbreak of H7N7 subtype in the Netherlands caused 89 human infections
208 (Fouchier et al., 2004). H5N2 AI strain has caused 20 human cases in Japan in 2005
209 (De Nardi et al., 2014). H5N8 led to 7 human cases in Russia in 2021 (EFSA, 2023).
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A very small number of human cases (1-3 each) have been associated with the
following AI strains: H3N8, H6N1, H7N2, H7N3, H7N4, H10N3, H10N7, and H10N8
212 (EFSA, 2023; Skufca et al., 2022; WHO, 2023a).
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214 UK avian influenza cases in humans
215 Infections with LPAI strains have been reported several times in the UK. The
216 first case of AI reported in the UK was an LPAI H7N7 case in 1996 that resulted in
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217 conjunctivitis (CDC, 2022d; Wang et al., 2021). Sporadic cases of LPAI H7N2 and
218 H7N3 were recorded in the UK between 2002 and 2007, which resulted in
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219 conjunctivitis and mild upper respiratory tract symptoms (CDC, 2022d; Wang et al.,
220 2021).
221 The first human case of HPAI H5N1 avian influenza in the UK was confirmed
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222 in December 2021 (Oliver et al., 2022). The case was asymptomatic and only
223 detected as the UKHSA had increased its surveillance of potentially exposed human
224 contacts given the dramatic increase in H5N1 infections in birds in the UK. The
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225 individual was tested after a confirmed outbreak in their domestic flock of Muscovy
226 ducks. The epidemiological investigation suggested that close contact with the flock
227 and their contaminated environment was the likely source of infection (Oliver et al.,
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228 2022).
229 The UKHSA are working together with the APHA and Defra to investigate the
230 risk to human health of AI H5N1 in England. Between 1 October 2022 and 15
231 December 2022, UKHSA health protection systems have recorded 2,085 human
232 exposure episodes of a person being directly exposed to an infected bird, with no
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233 detection of AI viruses in humans in 2022 (UKHSA, 2022). There have been no
234 severe human cases associated with H5N1 virus detected in the UK. There is
235 insufficient information to judge the risk of asymptomatic or mild disease due to the
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236 limited testing in human contacts with infected birds (UKHSA, 2022).
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238 Infectious dose
239 Although it is unknown what the infectious dose of AI is for humans due to the
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240 rarity of infection, several studies have investigated oral and intranasal inoculation of
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241 AI in animals (reviewed in O’Brien et al., 2021). One study in which ferrets were
242 exposed to different HPAI viruses (H5 and H7 subtypes) through consumption of
243 infected chicken meat showed that the dose of virus needed to infect ferrets through
244 consumption was much higher than via respiratory exposure (108.9-109.2 EID50
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compared to 107 EID50) and varied with the virus strain (Bertran and Swayne, 2014).
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247 Exposure Assessment
248 Commerical Poultry: Chicken and Turkey
249 Detecting AI before slaughter
250 Initial clinical presentation of HPAI infection in poultry (chicken and turkeys)
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251 might be sudden death, with little or no other preceding clinical signs or gross
252 pathology (More et al., 2017). In some cases, there may be signs of acute disease
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253 presenting with signs of systemic infection including respiratory, gastrointestinal and
254 neurological distress (Abd El-Hack et al., 2022; More et al., 2017; NADIS, 2016).
255 Golden et al. (2009) used a state-transition model to investigate the
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256 probability that an infected flock with HPAI H5N1 will remain undetected until
257 slaughter, considering three possible states, susceptible (not infected), infected, and
258 dead, and the transition probabilities that would predict the movements between
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259 those states (Golden et al., 2009). They predicted a high probability (0.94) that a
260 flock infected with HPAI H5N1 would be detected before being sent to slaughter
261 (Golden et al., 2009). The probability of detection was inversely related to the length
262 of the non-detection window (the time between infection and the flock being
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263 identified as infected), that is a function of the effective contact rate, latency, bird
264 mortality rate, and daily mortality threshold (Golden et al., 2009).
265 An investigation by Post et al. (2012) suggested that for LPAI, no clinical signs
266 were observed. Another study found that LPAI infection in chickens and turkeys
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267 manifests with mild respiratory distress and reduced egg production (Abd El-Hack et
268 al., 2022).
269 Therefore, given the veterinary inspection process in slaughterhouses and
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270 clinical signs in the flocks (for example reduced egg production), it is unlikely that
271 HPAI-infected birds will be sent for slaughter. The chances are higher for LPAI-
272 infected flocks since clinical signs may be less severe and signs of infection are less
273 likely to be detected by the post-mortem visual inspection.
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274 Viral distribution and titre in tissue
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275 HPAI induces a systemic infection in the host. Viral replication causes high
276 titres of infectious virus in internal organs (for example liver, heart), in muscles
277 (breast and thigh), blood and bones, and other tissues, in addition to respiratory and
278 gastrointestinal tracts (ACMSF, 2015; Harder et al., 2016; Swayne and Beck, 2005).
279
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Post et al. (2012) investigated HPAI and LPAI viral load and manifestation in
280 chickens, demonstrating that experimentally infected chickens with H7N1 HPAI
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281 developed illness with depression that led to death. Their qPCR data showed high
282 amounts of viral RNA load in all organs tested (lung, trachea, ileum, and brain),
283 which were detectable within 4 hours post inoculation and increased in each organ
284 until death (at 4 days post infection (dpi).)). For LPAI-infected birds, viral load was
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285 detectable in these organs beginning between 4-8 hours post inoculation. By day 7,
286 viral load was undetectable in a majority of the chickens in the trachea, ileum and
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287 brain; only the lungs still contained viral RNA at this time point. It was summarised
288 that, although both HPAI and LPAI could be detected in a broad range of tissues, the
289 pathogenicity and mortality differences between them could originate from
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290 differences in virus replication and the resulting host responses in vital organs (Post
291 et al., 2012).
292 LPAI infections in chickens either do not present or very rarely present any
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293 clinical signs. Both experimental infection studies (Bergervoet et al., 2019; Roy
294 Chowdhury et al., 2019) and field observations (Bertran et al., 2018) suggest that
295 LPAI viruses are primarily restricted to the respiratory and gastrointestinal tract and
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296 the presence of LPAI in muscle tissue in naturally infected birds has not been
297 demonstrated in published literature (EFSA et al., 2018; Shibata et al., 2018)
298 although some studies provide evidence that LPAI can be isolated from the muscles
299 and organs of experimentally infected poultry (Post et al., 2012; Shibata et al., 2018;
300 Slomka et al., 2018). It is therefore unlikely that a bird infected with LPAI will be
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301 detected via ante-mortem inspection as diagnosis is dependent on the presence of
302 clinical signs (EFSA et al., 2018). Also, the presence of the LPAI virus in muscle
303 tissues is not always associated with the presence of macroscopic lesions, and at
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304 the high speed of slaughter lines detection of the lesions and faecal contamination of
305 the carcasses by the visual post-mortem inspection can fail (EFSA et al., 2018).
306 Experiments performed by Pantin-Jackwood et al. (2017) demonstrated that
307 turkeys infected with dose of 103 EID50 (egg infectious dose) LPAI exhibited clinical
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308 signs of respiratory disease - mild lethargy and infraorbital swelling - with no
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309 mortality. Commercial turkeys are highly susceptible to LPAI viruses, often showing
310 increased mortality and are more likely to show clinical signs of respiratory distress,
311 sinusitis, and poor performance (Ngunjiri et al., 2021). Additionally, HPAI infection in
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turkeys has presented differently to chickens, with more neurological signs and no
haemorrhagic lesions present (Pantin-Jackwood et al., 2017). As a result of that,
314 there is agreement with the conclusion of the 2018 EFSA report (EFSA et al., 2018)
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315 that the virus is very unlikely to be disseminated systemically, although it should be
316 noted that turkeys are more susceptible than chickens and experimentally-infected
317 turkeys may exhibit some systemic infection (EFSA et al., 2018).
318 Infection of the liver in chickens is also a concern due to the consumption of
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319 chicken liver pate. Several HPAI and LPAI strains have been detected in the liver of
320 experimentally infected chickens (Post et al., 2012; Yamamoto et al., 2017). The
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321 initial viral titre in liver was 104.3 to 106.5 EID50/ml. Liver samples from birds
322 experimentally infected with HPAI H5N1 have been shown to be positive for virus
323 after 20 days when stored at 4oC and 3 days when stored at 20oC (Yamamoto et al.,
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324 2017). Nevertheless, Pohlman et al. (2017) described an outbreak of HPAI H5N8
325 that caused lethal infections wild birds and domestic poultry in Germany and
326 elsewhere in Europe and showed macroscopic changes in poultry organs, including
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327 necrotizing lesions in liver (Pohlmann et al., 2017).

328 Commercial Poultry: Ducks and Geese
329 Detecting AI before slaughter
330 Aquatic birds such as ducks and geese are a natural reservoir for AI. Some
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331 subtypes, especially LPAI, are highly adapted to these species of birds and therefore
332 infection tends to be subclinical (APHA, 2022). If signs of infection are not shown as
333 clearly as chickens, inspection of the carcass may not be sufficient to rule out
334 disease, particularly for LPAI infection (APHA, 2022). There is a lack of evidence
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335 regarding the clinical signs of HPAI infection in non-indication species; however,
336 some strains have been reported to cause mortality in domestic ducks (Spackman,
337 2020).
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338 Viral distribution and titre in tissue
339 Although there is limited specific research into the survival of avian influenza
340 within meat from game birds, such as ducks and geese, where specific evidence is
341 not available we have assumed that AI survival in meat from these types of birds will
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342 behave similarly to what’s been observed in other poultry meat. A 2012 study by
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343 Beato et al. determined that HPAI H7N1 could survive for up to 75 days in duck meat
344 kept at 4°C (Beato et al., 2012). Furthermore, Tumpey at al. (2002) showed that
345 HPAI H5N1 isolated from duck meat was highly pathogenic and able to replicate in
346 chicken following intravenous and intranasal inoculation (Tumpey et al., 2002).
347
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Surveillance data revealed that HPAI H5N1 infectious virus was detected in imported
348 frozen duck meat (Chmielewski and Swayne, 2011).
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349 HPAI has been found in a range of organs in ducks and geese including the
350 cloacal bursa, spleen, liver, kidney, heart, brain, lung, pancreas and skeletal muscle
351 (Bertran et al., 2014). The presence in the organs is believed to be due to the ability
352 of HPAI to infect endothelial cells resulting in viraemia and subsequent systemic
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353 spread (Vreman et al., 2022). LPAI infections typically are restricted to the
354 respiratory and intestinal systems and are rarely seen in other organs (Vreman et al.,
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355 2022).
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357 Commercial Hen Eggs
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358 Detecting AI before reaching market

359 Infection with HPAI in commercial poultry will lead rapidly to presentation of
360 clinical signs, typically within 2-3 days post-infection. There is often a drop in egg
361 production, which ranged from 10-55% when studied in flocks naturally infected (Lu
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362 et al., 2004; Swayne et al., 2012). Additionally, HPAI infection may lead to changes
363 in the egg, such as malformed eggs (Qi et al., 2016; Swayne et al., 2012). During an
364 outbreak, researchers found that up to 10% of eggs were malformed, including being
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365 “thin-shelled, soft-shelled or abnormally small” (Cappucci et al., 1985). These eggs
366 would be removed from the food chain during the grading process (APHA, 2018).
367 Class A eggs are not allowed to have foreign matter on them, which means eggs
368 with visible faecal contamination, which may carry the AI virus (see below) will also
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369 be removed from the food chain (APHA, 2018).
370 Flocks infected with LPAI viruses do not present with as many clinical signs
371 as those infected with HPAI viruses. The only evidence may be ruffled feathers and
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372 a slight drop in egg production; it is likely it may not be detected at all (Center for
373 Food Security and Public Health, 2022). LPAI viruses have not been found
374 replicating in as many tissues in birds and are typically restricted to the respiratory
375 and gastrointestinal tract (Harder et al., 2016). This means eggs are less likely to
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376 contain active LPAI virus as the reproductive tract is not infected.
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378 Viral presence and titres in and on eggs
379 During HPAI infections, the reproductive tissue of laying hens can be infected
380 (Harder et al., 2016). If the ovary is infected, this can lead to infectious virus being
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present in the yolk. If the oviduct is infected, virus will also be present in the albumen
382 (egg white). The virus can be present on the shell of the egg, although it is likely this
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383 is due to faecal contamination from passage through the cloaca (EFSA, 2006).
384 As chickens will likely stop laying eggs around 4 days post-infection due to
385 either clinical progression of disease or death, there is the possibility that eggs laid in
386 the period between infection and clinical detection could contain virus. Experimental
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387 infections determined that eggs laid early in the infection did not exhibit virus in or on
388 the egg, but it was found in the last eggs laid (Bauer et al., 2010; Cappucci et al.,
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389 1985). Studies from outbreaks of naturally infected flocks estimated 7-57% of eggs
390 may be HPAI positive (Bauer et al., 2010; Cappucci et al., 1985; Swayne et al.,
391 2012). Available data on viral titres isolated from HPAI-infected eggs and the time of
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392 collection post-infection are summarised in Table 1.

393 Given the clinical signs of HPAI in infected flocks, it is likely that the infection
394 would be identified, and eggs stopped from reaching the market. However, there is a
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395 small window between initial infection and the presentation of clinical signs where
396 contaminated eggs may be released from the farm containing viral loads between
397 101.5 – 106.2 EID50/ml.
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398 While some studies have not found LPAI in or on eggs from LPAI-infected
399 flocks (Lu et al., 2004), other evidence suggests that LPAI can be found in the
400 internal contents of eggs, although this has been reported less frequently than
401 finding HPAI in egg internal contents (Cappucci et al., 1985; Pillai et al., 2010). For
402 example, only 1.67% (2/120) of eggs from commercial layers were positive for H5N2
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403 LPAI compared to 24.6% (37/156) of eggs being positive for the high pathogenicity
404 version of the strain during a natural outbreak (Cappucci et al., 1985). There is still
405 the possibility for faecal cross contamination of the eggshell surface from passage
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406 through the cloaca. How the different LPAI viruses may behave in different bird
407 species as far as their ability to contaminate eggs internal contents and the shell is
408 unknown.
409
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410 Survival of AI virus in poultry products during retail and consumer stages
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411 Effect of temperature on AI survival
412 Poultry products
413 It is well documented that HPAI tolerates cold and freezing temperatures well.
414 H5N1 virus was shown to be able to survive for 240 days in feather tissue, 160 days
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415 in muscle meat and 20 days in liver at 4°C (Yamamoto et al., 2017). A study carried
416 out in 2012 proved that a high pathogenic strain H7N1 isolated from chicken, turkey
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417 and duck meat was still viable after being kept at 4°C for 135, 90, and 75 days,
418 respectively (Beato et al., 2012). Dai et al. (2022) demonstrated that HPAI was able
419 to survive at various temperatures (-20°C, 4°C, and 25°C) for several days; the lower
420 the temperature, the longer the viability of the HPAI (Dai et al., 2022). The infectious
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421 virus has also been proven to survive in tissues at 20-22°C for up to 6 days post
422 mortem (Busquets et al., 2010).
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423 LPAI is unlikely to be detected in meat, as routine testing is not currently

424 carried out in non-symptomatic flocks. It has been shown that LPAI virus is able to
425 survive freezing and refrigeration, and those low temperatures do not reduce the
426 concentration or viability of viruses (EFSA et al., 2018). In the experiment by Ejaz et
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427 al., 2007, in broiler-chickens infected with LPAI H9N2, and frozen at -20°C, virus was
428 detected in: bone marrow and legs after 6 weeks post-storage, neck and wings until
429 4 weeks post-storage, and breast until 2 weeks post-storage (Ejaz et al., 2007).
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430
431 Egg Products
432 Experimental infection with LPAI strain H5N2 in and on eggs provided some
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433 estimation of the viral survival during storage times of different lengths and
434 temperatures. When virus was applied on the eggshell and allowed to dry, it could
435 not be re-isolated from the surface after 3-4 hours, regardless of the temperature,
436 which ranged from 4°C to 20°C. The same held true even if the virus was mixed with
ed
437 “droppings” (assumed to be bird faeces). However, active virus could be isolated
438 from the internal contents of the eggs. Virus survived better in the yolk compared to
439 the albumen, and viral titres in both dropped off as either length of storage or
iew
440 temperature increased. At 4°C, virus was still detected after 17 days in both the yolk
441 and albumen, whereas it was only found in the yolk after 17 days at both 15°C and
442 20°C (de Wit et al., 2004).
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443
444 Effect of cooking on AI survival
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445 Poultry products
446 A study to determine the survival of AI subtype H5N1 by Wanaratana et al.
447 (2010) showed that all three H5N1 reference viruses used completely lost their
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448 infectivity when exposed to a temperature of 70°C for 60 min, or 75°C for at least 45
449 min. Zou at al. (2013) have tested H7N9 viral tolerance against heat treatment, and
450 found that it completely lost its infectivity at 56°C for 30 minutes, 65°C for 10
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451 minutes, 70°C, 75°C and 100°C for 1 minute (Zou et al., 2013). Both of these studies
452 were performed in vitro.
453 An in vitro study by Swayne in 2006 found that the reduction in virus infectivity
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454 titres was dependent on virus concentration and no HPAI virus was isolated after 1
455 second of treatment at 70°C; these results were later confirmed by the same
456 research group in both experimentally- and naturally-infected chickens (Swayne,
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457 2006; Thomas et al., 2008; Thomas and Swayne, 2007). A change in coloration in
458 the meat from pink-tan to white was associated with a loss in recovery of infectious
459 virus, which is important to note for less than thoroughly cooked (LTTC) poultry
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460 products. Other studies performed within poultry meat found inactivation after
461 heating to 63°C for 2 minutes (Isbarn et al., 2007).
462 Egg products
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463 Inactivation of AI in eggs at pasteurisation temperatures has been studied

464 using experimentally inoculated egg samples. Swayne and Beck (2004) found that
465 for both HPAI and LPAI H5N2, viral titre was reduced by 90% within 20 seconds at
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466 61°C in both homogenised whole egg and in egg whites. Another study found there
467 was a 5-log reduction in H5N2 HPAI in 34 seconds for homogenised whole egg and
468 in 4 seconds for plain egg yolk at 60°C (Chmielewski et al., 2013). Viral reduction
469 could also be achieved at lower temperatures for longer treatments, ranging from 4.3
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470 minutes for reduction of HPAI in liquid egg at 55°C to 11 minutes for HPAI in whole
471 homogenised egg at the same temperature (Swayne and Beck, 2004).
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472
473 Consumption of poultry and egg products
474 National diet and nutrition survey (NDNS) data was used to estimate the
475 consumption of poultry products in the UK (DHSC, 2013; PHE and FSA, 2020, 2018,
476 2016, 2014). This data describes consumption either “with” or “without recipes”
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477 included- “with recipes” takes into account products that will contain the product or
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478 ingredient of interest if it is at least 5% of the overall food present. In the case of
479 “without recipes”, the product or ingredient of interest represents over 95% of the
480 food. In the NDNS data, chronic consumption is the amount consumed averaged
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481 over four days whereas acute consumption is the amount eaten on one day.
482 Chicken consumption is by far the most popular poultry eaten with 58.67% of
483 the studied population of 4 - 64-year-olds reporting eating chicken, compared with
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484 only 9.08% eating turkey (Table 2). In infants and children under four, 61.09% are
485 consuming chicken and only 5.70% turkey. A slightly different picture can be seen in
486 the over 65s, although once again chicken is the most popularly consumed poultry
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487 meat with 46.49% of respondents consuming it and 8.19% for turkey. Very low
488 numbers reported the consumption of offal from chicken or turkey. There was no
489 data found for children under 19. Only 0.04% of adults (2 out of 5094 respondents)
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490 reported consuming chicken or poultry offal and nobody over 65 years old. Given the
491 low numbers, it is difficult to estimate how accurately these data reflect true
492 consumption in the UK.
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493 To understand how often chicken and turkey is eaten less than thoroughly
494 cooked, data was obtained from the FSA’s survey Food and You 2 (FSA, 2021).
495 8,672 respondents were asked how often (always, most of the time, about half the
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496 time, occasionally, never) they eat either chicken or turkey when it is pink or has pink
497 or red juices (Error! Reference source not found.). The data indicated that while a
498 majority (93%) of respondents who eat chicken or turkey report never eating it pink
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499 or when it has pink or red juices, 4% report doing this at least occasionally.
500 Data from the NDNS on the consumption of commercially reared duck report
501 that in infants, duck is rarely consumed with only 0.26% reporting consuming (Table
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502 2). In the 4–64-year-old category, 1.28% report eating duck. The over 65s, is the
503 most popular age group for consuming duck, with 1.82% of participants reporting
504 duck consumption.
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505 In the Food and You 2 survey, 4,227 respondents were asked how often they
506 eat duck meat when it is pink or has pink or red juices (Table 3). The survey found
507 that around two thirds (67%) of respondents who eat duck report never eating it pink
508 or when it has pink or red juices, yet almost a third (31%) eat pink duck at least
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509 occasionally; 3% report always eating duck pink, 8% do this most of the time, 4%
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510 about half the time, and 16% occasionally.
511 The data for egg consumption include foods consumed “with recipes”,
512 meaning that data is included both when the egg is eaten as an individual item and
513
514
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when it forms part of a recipe. Since AI can be inactivated by thorough cooking of
eggs, data on eggs that would be LTTC was also included. In Table 4, “all egg
515 consumption” would include raw, poached, and thoroughly cooked eggs.
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516 The data reveal that a vast majority of the UK population, in all age groups,
517 consumes eggs. The amount that is eaten raw or poached is much smaller, with a
518 higher proportion of elderly consumers eating raw and poached eggs. While those
519 aged 5 – 64 years report eating raw and poached eggs less frequently than those
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520 that are 65+, they report eating larger servings of these products.
521 Data from the FSA’s Food and You 2 survey was also reviewed to support
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522 evidence on egg consumption in the UK (Table 5). Self-reported rates of

523 consumption of eggs eaten raw, LTTC and thoroughly cooked indicated that, of the
524 respondents that consume eggs at home, 14% eat raw eggs once a week or more
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525 (Table 5). A higher percentage eat LTTC eggs (41%) and thoroughly cooked eggs
526 (49%) once a week or more. 61% of respondents never eat raw eggs, 22% never eat
527 LTTC eggs and 8% never eat thoroughly cooked eggs. Both data sets indicate that
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528 when eggs are consumed in the UK, they are most frequently eaten thoroughly
529 cooked.
530 Cross contamination
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531 Poultry products contaminated with live virus could potentially cross-
532 contaminate other products or surfaces in a consumer’s kitchen, serving as a source
533 of infection. The below sections explore the ability of AI viruses to survive
534 environmental exposure outside of poultry products and their ability to withstand
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535 disinfection.
536 Survival in faeces
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537 Both HPAI and LPAI are shed in the faeces of both symptomatic and
538 asymptomatic carriers of the disease. Faeces are associated with the further spread
539 and infectivity of the disease, particularly through the wild bird population
540 contaminating water and feed sources. The majority of studies that have investigated
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541 the persistence of AI in the environment have tended to concentrate on the
542 persistence of the virus in faeces.
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543 Experimentally, it has been shown that AI might remain infectious in faeces
544 within a wide range of days to several weeks depending on temperature conditions.
545 One study found that influenza viruses may remain infectious in duck faeces for
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546 periods of time ranging from a few days (at 30°C and 20°C) or a few weeks (at 10°C)
547 to several months (at 0°C) (Nazir et al., 2011); similar results were reported in other
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548 studies (Kurmi et al., 2013). Results differed between these two studies on whether
549 the viruses could survive in dried faeces to the same extent as wet. In the study that
550 compared survival in faeces at room temperature between an HPAI and LPAI strain,
551 the HPAI strain survived for at least three days longer (Hauck et al., 2017).
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552
553 Survival in environment
554 One study was identified that investigated how the virus persisted in the
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555 environment on different surfaces, including soil, glass, and metal, in different
556 humidity and temperature conditions (Wood et al., 2010). Overall, the study
557 concluded that the HPAI H5N1 virus used in the study tends to survive longer in the
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558 environment (outside a host) in areas that are relatively colder and have less
559 sunlight. Two articles studied AI viral survival in water. They found that all the AI
560 viruses tested in the study were, in general, most stable at lower temperatures
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561 (<17°C), neutral to basic pHs (either 7.0-8.5pH or 7.4-8.2pH), and in fresh to
562 brackish salinities (salinity ranging from 0 to 20,000 ppm or <0.5ppt) (Brown et al.,
563 2009, Keeler et al., 2014).
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564
565 Disinfection
566 AI can be inactivated by a range of disinfectants at the recommended
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567 concentrations, as reviewed in (Shahid et al., 2009). Contact times for disinfection
568 ranged from 5-15 minutes for most recommended concentration preparations,
569 although Virkon®-S needed 45 minutes when prepared at 0.2% (Shahid et al.,
iew
570 2009). When studying the survival of HPAI H5N1 against chlorination, it was found
571 that free chlorine concentrations (0.52–1.08 mg/L) typically used in drinking water
572 are sufficient to inactivate the virus by >3 orders of magnitude, after 1 min exposure
573 (Rice et al., 2007). Two studies have demonstrated that the effectiveness of
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574 disinfectants can be increased by adding anti-freeze agents when used in freezing
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575 conditions (Guan et al., 2015, Kabir et al., 2021).
576
577 Infectivity of AI via the gastrointestinal tract
578 Transmission of the H5N1 virus to mammals has been observed when
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579 domestic cats or tigers and leopards were fed with infected poultry (Keawcharoen et
580 al., 2004; Kuiken et al., 2004). A 2012 study by Reperant et al. showed that
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581 intragastric inoculation of domestic cats at a level of 107.8 TCID50 (50% Tissue
582 Culture Infective Dose) resulted in fatal systemic infection (Reperant et al., 2012). In
583 2011, Shinya et al. showed that the inoculation of hamsters with H5N1 directly into
584 the digestive tract at a level of 107.1-107.3 TCID50 allowed the virus to enter the
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585 bloodstream through the digestive lymphatic system (Shinya et al., 2011). These
586 results indicate infection is possible in mammals when avian influenza virus is
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587 ingested orally.

588 Some human infections are suspected to have occurred following the
589 consumption of fresh duck blood; one news article reported a Vietnamese women
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590 tested positive for the H5N1 strain, following drinking duck blood (IATP, 2005). This
591 evidence of transmission from poultry products to other mammalian species,
592 including humans, indicates infection via the gastrointestinal pathway is possible.
593 Since human cases of AI also report gastrointestinal symptoms, one study
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594 has investigated whether AI H5N1 virus can infect and replicate in the human GI
595 tract (Shu et al., 2010). While sialic acid (SA) α-2,6-Galactose (gal) (the preferred
596 receptor for human influenza viruses) was abundantly expressed along the entire GI
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597 tract, they did identify expression of SA α-2,3-Gal (the preferred receptor for avian
598 influenza viruses), which increased travelling from the ileum to the rectum. Using
599 human ex vivo colon samples, the research group was able to demonstrate infection
600 of the tissue by the AI virus. Increases in viral titre in the supernatant of the ex vivo
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601 cells suggested the virus was also capable of replication (Shu et al., 2010). For
602 evidence of active AI infection in the human GI tract, colonic samples of an H5N1
603 deceased patient were stained for presence of the nucleoprotein viral antigen, which
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604 was detected in the tissue. Furthermore, in two other H5N1 patients experiencing
605 diarrhoea as a symptom, viral RNA was recovered from faecal samples. However,
606 this was the only study identified during literature searches specifically investigating
607 expression of AI viral receptors in the human GI tract. While epidemiological
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608 evidence does not indicate that the GI tract is a common route for human infection
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609 by AI viruses, these results highlight that it remains a possibility.
610
611 Risk Characterisation
612
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Frequency of occurrence from commercial poultry
613 Data indicates that HPAI-infected commercial flocks of chicken and turkeys
614 would likely be identified before being slaughtered and that LPAI-infected flocks
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615 would not likely have the virus present in the muscle tissue or organs. This means
616 that contaminated meat is unlikely to reach the consumer. Consumption data
617 indicates that while chicken and turkey are the most commonly consumed poultry
618 products in the UK, they are also very unlikely to be eaten pink. Research
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619 demonstrates that AI viruses are heat-labile, so thorough cooking would inactivate
620 any virus present. Additionally, proper hygienic handling of raw product would reduce
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621 the amount of any virus encountered by consumers from cross-contamination.

622 Finally, there is a species barrier to infection: the receptors located in the upper
623 human GI tract are not conducive to infection with AI viruses.
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624 Given these considerations, the frequency of occurrence for the UK

625 population of acquiring AI from the handling and consuming of commercial chicken
626 and turkey is negligible (so rare that it does not merit to be considered). This is
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627 supported by the lack of evidence of any previous foodborne transmission of this
628 virus from cooked poultry products. The level of uncertainty related to this is low, as
629 there are several research studies demonstrating the inactivation of AI from cooking
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630 and disinfection.
631 Duck and geese are less likely to exhibit symptoms from AI infections, so it is
632 more likely that contaminated meat may reach the consumer. While these poultry
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633 products are eaten much less frequently than chicken and turkey, they are more
634 likely to be eaten less than thoroughly cooked. The frequency of occurrence for the
635 UK population of acquiring AI from the handling and consuming of commercial duck
iew
636 and geese is very low (very rare but cannot be excluded) with medium
637 uncertainty. This uncertainty is because less research has focused on ducks and
638 geese compared to other poultry.
639
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640 Frequency of occurrence from hen table eggs
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641 Evidence from both natural outbreaks and experimental infections
642 demonstrate that AI viruses can be present in the internal contents and on the shell
643 of eggs. Eggs are consumed by a large portion of the UK population and, compared
644
645
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to the other products considered in this risk assessment, are the product most likely
to be consumed either raw or undercooked. Given the evidence, the frequency of
646 occurrence to the UK population of acquiring avian influenza virus from handling and
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647 consuming hen table eggs is very low (very rare but cannot be excluded). The
648 uncertainty associated with this is low, as there was adequate data on AI in eggs,
649 consumption of LTTC eggs in the UK and viral inactivation from heating of egg
650 products.
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651
652 Severity of detriment for AI infection in humans
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653 As previously discussed, humans can exhibit a range of symptoms when

654 infected with AI, ranging from asymptomatic infections or mild conjunctivitis to severe
655 respiratory illness. Considering recorded AI infections worldwide, there is a high case
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656 fatality rate of up to 50%, depending on the strain. Given this, the severity of
657 detriment from AI infection in humans is high (severe illness: causing life-
658 threatening or substantial sequelae or illness of long duration) with medium
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659 uncertainty. This uncertainty is due to the lack of surveillance for AI infections in
660 people, meaning asymptomatic infections may go undetected. This would artificially
661 inflate the case mortality of reported infections compared to true infection numbers.
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662
663 Key Uncertainties
664 A key uncertainty for commercial poultry was the lack of evidence related to
ed
665 LPAI infections in commercial flocks. Prevalence of these infections in birds is not
666 known given the lack of symptoms and the absence of active surveillance. It is
667 unknown if LPAI viruses can infect meat or consumable tissue in LPAI-infected birds
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668 or what the risk of cross-contamination may be during slaughter. These issues
669 warrant further investigation since LPAI viruses can still cause serious illness in
670 humans.
671 HPAI infections in flocks typically cause a drop in egg production to alert staff
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672 to the presence of the illness. The likelihood that eggs with AI contamination might
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673 be sent for grading and sale in the time period between infection and detection is not
674 well understood. Information was also lacking on the ability to detect LPAI infection
675 in laying flocks and on the ability of LPAI virus to contaminate eggs during natural
676
677
outbreak conditions.
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While the uncertainties related to the frequency of occurrence of AI in humans
678 and the severity of detriment are due to either a lack of data or variability in the
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679 population, there are some additional uncertainties around the ability of AI to cause
680 infection from food through the oral route. This is due to the lack of epidemiological
681 evidence associated with AI cases from handling and consuming food, the potential
682 infectious dose required for infections via the oral route and the ability of the AI virus
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683 to infect tissue from receptors available along the human gastrointestinal tract.
684 Another additional uncertainty is around the effect mutations may have on the ability
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685 of the virus to transmit between species or cause infections in humans from
686 consumption of contaminated food.
687
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688 Discussion
689 In this risk assessment, we assigned the risk to the UK population of acquiring
690 AI from handling and consuming commercial poultry products, which ranged from
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691 negligible (for commercial chicken and turkey) to very low (for farmed duck and
692 geese and hen eggs). These risk characterisations are similar to the risk assessment
693 reviewed by ACMSF in 2015, which assigned the risk of acquiring AI viruses via
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694 thoroughly cooked poultry products to be very low (ACMSF, 2015); it did not
695 consider the risk of individual poultry products separately or separate the probability
696 of exposure from the severity of detriment, as subsequently recommended in the
697 2020 ACMSF report on risk representation (ACMSF, 2020). The WHO advice, last
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698 updated in 2020, says that thoroughly cooked poultry meat is safe to consume
699 although consuming raw or incompletely cooked meat and eggs from areas
700 experiencing active outbreaks should be avoided (WHO, 2020). Similar
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701 recommendations are given by the CDC, where all poultry meat and egg products
702 are advised to be properly cooked before consumption. Although there is no
703 evidence of human AI infection after eating properly cooked poultry products, they
704 also recognise that uncooked poultry products, like blood, may have contributed to a
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705 small number of human infections in Asia (CDC, 2022b). On the whole, most
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706 available epidemiological evidence suggests that human infections with AI viruses
707 most frequently occur following direct or close contact with infected (ill or dying)
708 poultry (CDC, 2022c; Wiwanitkit, 2007).
709
710
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There is sporadic evidence for infections via ingestion of the virus from both
animal and human cases. The CDC states that sporadic H5N1 AI infections in
711 predatory and scavenging mammals are not unexpected, taking into account the
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712 widespread infection in wild birds. Therefore, the mammals that eat infected sick or
713 dead bird or poultry, including wild or feral animals such as foxes; stray or domestic
714 animals such as cats and dogs; and zoo animals, can become infected with AI
715 viruses (CDC, 2023). Mammals scavenging on infectious dead or sick birds will be
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716 exposed to very large quantities of virus, giving a possibility for the virus to enter a
717 host population where it doesn't normally circulate (Defra, 2023).
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718 Shortly after this risk assessment was completed in March 2023, further
719 evidence of uncooked food as a potential transmission pathway was reported. In
720 June 2023, Poland notified the WHO of a number of unusual cat deaths. 29 (62%)
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721 out of 47 samples tested from 46 cats were found to be positive for AI H5N1 (WHO,
722 2023b). The source of exposure of cats to the virus is still under investigation, with
723 possibilities ranging from the cats coming into contact with infected birds, eating
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724 infected birds or eating food contaminated with the virus (LUENA, 2023). This
725 incident raises the possibility that raw pet food could be source of AI virus which
726 could lead to human infections from cross-contamination.
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727 While there is no epidemiological evidence that AI infections in humans occur

728 from thoroughly cooked food, there is evidence to support that less than thoroughly
729 cooked food may serve as a source of infection. At the moment, the species barrier
730 due to different receptors for infection between avian and mammal hosts appears to
731 be a reason that human cases do not correlate with cases in birds (WHO, 2023c); it
ed
732 is telling that even after the current outbreak of the HPAI H5N1 strain, food was not
733 revealed as a potential source of infection in humans despite the research indicating
734 it might be possible. Similar concerns about the potential for foodborne transmission
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735 of the SARS-CoV-2 virus were also raised during the COVID-19 pandemic (FSA,
736 2020). As mutations may change how the virus infects human hosts, more research
737 into the ability for respiratory viruses to potentially cause infections through the
738 gastrointestinal tract seems warranted.
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739 Glossary
ed
740 AI- avian influenza
741 dpi- days post infection
742 EID50 - 50% Egg Infectious Dose
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743 HPAI- high pathogenicity avian influenza
744 LPAI- low pathogenicity avian influenza
745 LTTC- less than thoroughly cooked
746 NDNS- National Diet and Nutrition Survey
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747
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748 Acknowledgements
749 We would like to thank the ACMSF’s Newly Emerging Pathogens subgroup for their
750 review of the original FSA risk assessment and Gary Barker for reviewing draft
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751 versions of this manuscript. We’d also like to thank Ashley Banyard, Mark Jackson,
752 Marco Falchieri, and Rachel Taylor of the UK’s Animal and Plant Health Agency for
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753 discussion during preparation of the original risk assessment or for its review.
754
755 Declaration of Interests

756 None of the authors have any interests to declare for this publication.
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757
758 CRediT author statement

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759 Erica Kintz: Project administration, Conceptualisation, Investigation, Writing- Original

760 Draft. Writing- Reviewing and Editing
761 Elaine Pegg: Investigation, Writing- Original Draft, Writing- Reviewing and Editing
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762 Wendy Perry: Investigation, Writing- Original Draft, Writing- Reviewing and Editing
763 Wioleta Trzaska: Investigation, Writing- Original Draft, Writing- Reviewing and
764 Editing
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765 Anthony Wilson: Conceptualisation, Writing- Reviewing and Editing

766 Kathryn Callaghan: Writing- Reviewing and Editing
767 Dan Tucker: Writing- Reviewing and Editing
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768 Alec Kyriakides: Writing- Reviewing and Editing

769 Dragan Antic: Writing- Reviewing and Editing
770 Funding Sources
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771 This research did not receive any specific grant from funding agencies in the public,
772 commercial, or not-for-profit sectors.
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1110 Tables
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Reference Bird species & Egg product & titre Time taken Type of infection
iew
HPAI strain (EID50/ml) dpi^
(Bean et al., 1985) Hens White: 105.6 Last eggs laid experimental
H5N2 Yolk: 103.6 before death
(Promkuntod et al., Quails Egg internal contents: Not reported natural
2006) H5N1 104.6-106.2
v
(Swayne et al., 2012) Hens Shell: 102.99 1-4 dpi experimental
re
H5N2 Albumen: 103.01
Yolk: 102.17
(Uchida et al., 2016) Hens Shell: 102.7-5.5 3-4 dpi experimental
H5N8 er Albumen: 102.2-5.3
Yolk: 101.5-4.4
1113 ^dpi: days post-infection
pe
1114
1115
1116
ot
tn
rin
ep
Pr
1117 Table 2: Poultry consumption (without recipes) from NDNS data.
Age range % reporting Chronic Chronic Acute Acute
ed
Mean^ Max^ Mean^ Max^
Chicken consumption
Infants/children <4 61.09% 9.88 78.02 20.99 163.73
(n = 3,480) (n=1353)
iew
4yrs-64yrs 58.67% 32.43 233.03 94.26 233.03
(n = 10,228) (n=4329)
65+ 46.49% 32.00 240.00 98.00 400.00
(n = 1,538) (n=543)
Turkey consumption
Infants/children <4 5.70% 8.63 36.13 30.69 110.82
v
(n = 3,480) (n=219)
4yrs-64yrs 9.08% 23.65 113.60 79.05 367.13
re
(n = 10,228) (n=934)
65+ 8.19% 80.00 150.00 86.00 290.00
(n = 1,538) (n=126)
Duck consumption
Infants/children <4 0.26% er 11.10 34.00 34.00 74.50
(n = 3,480) (n = 10)
4yrs-64yrs 1.28% 24.34 119.77 89.42 286.74
(n = 10,228) (n = 132)
65+ 1.82% 20.00 58.00 79.00 230.00
pe
(n = 1,538) (n = 28)
1118
1119 Table 3: How often respondents to the FSA’s Food & You 2 survey reported
1120 eating chicken or turkey (n=8,672) or duck meat (n=4,227) pink.
ot
Response % of respondents eating % of respondents eating

chicken or turkey meat pink duck meat pink
Always 1% 3%
tn
Most of the time 1% 8%

About half the time 1% 4%
Occasionally 4% 16%
Never 93% 67%
rin
1121
1122 Table 4: Egg consumption data from the NDNS survey, split by age group.
Egg % reporting Chronic Chronic Acute Acute
consumption Mean^ Max^ Mean^ Max^
ep
Infants and children < 5 years of age (n = 4,227)

Raw eggs 1.4%
(n = 60) 2.4 34.4 4.2 30.1
Poached 1.2%
Pr
eggs (n = 49) 16 43 58.6 112.1

All egg 72.5%
consumption (n = 3,065) 9.9 100.3 29.5 232.6
People aged 5 – 64 years (n = 14,995)
Raw eggs 3.6% 1.2 28 4.3 80.7
(n = 541)
ed
Poached 5.4% 30.4 210 99 400
eggs (n = 815)
All egg 94.6% 22.7 870 59.5 870
consumption (n = 14,189)
People aged 65+ (n = 1,538)
iew
Raw eggs 4.8% 1.2 10 3.2 24
(n = 74)
Poached 9.1% 24 130 78 150
eggs (n = 140)
All egg 94.5% 23 150 60 280
consumption (n = 1454)
v
1123 ^: grams/person/day
re
1124
1125 Table 5: Frequency of eggs eaten raw, LTTC, or thoroughly cooked in the UK.
1126 Data from Food and You 2 (Wave 2) survey on the eating habits of UK consumers
er
1127 (FSA, 2021)
Occurrence Rawa LTTCb Cooked

pe
thoroughly
Every day 1% 1% 2%
Most days 2% 4% 5%
2-3 times a week 4% 12% 15%
ot
About once a week 7% 24% 27%

2-3 times a month 4% 15% 16%
tn
About once a month 4% 11% 15%

Less than once a 14% 9% 11%
month
rin
Never 61% 22% 8%

1128 a: eggs that are uncooked for example, in homemade mayonnaise or homemade
1129 desserts like mousse or soft meringues
1130 b: eggs that have a runny yolk for example, soft boiled
ep
1131 c: eggs that have a firm yolk for example, hard boiled
1132
Pr
1133 Supplemental File #1
ed
1134 Systematic Search Strategy
1135 (avian influenza OR AI) AND:
1136 1. Food
iew
1137 2. Foodborne transmission
1138 3. Poultry AND slaughterhouse
1139 4. Poultry AND farm
1140 5. Duck
v
1141 6. Goose
1142 7. Partridge
re
1143 8. Eggs
1144 9. disinfection
1145 10. cooking OR heat er
1146 11. refrigeration OR freezing OR chilling
1147 12. temperature
pe
1148 13. (survival OR persistence) AND (environment OR faeces)
1149 14. environment
1150 15. faeces
1151 16. infectious OR dose OR “infective dose
ot
1152
tn
rin
ep
Pr

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1 The risk of acquiring avian influenza from commercial poultry products and

2 hen eggs: a qualitative assessment

53 characterisation, risk characterisation, commercial poultry, eggs.

73 such as live bird markets. Slaughtering, defeathering, handling carcasses of infected

79 From October 2021, there began a substantial increase in the number of AI

85 assessment was performed to ensure that advice relating to the consumption of

113 • Table eggs from UK hen laying flocks

116 • Cross-contamination from any of the above products

139 viral distribution within tissues.

141 their ability to mutate and/or transmit between species.

171 qualitative assessment was performed to ensure a rapid response.

327 necrotizing lesions in liver (Pohlmann et al., 2017).

358 Detecting AI before reaching market

392 collection post-infection are summarised in Table 1.

423 LPAI is unlikely to be detected in meat, as routine testing is not currently

463 Inactivation of AI in eggs at pasteurisation temperatures has been studied

522 evidence on egg consumption in the UK (Table 5). Self-reported rates of

536 Survival in faeces

587 ingested orally.

621 the amount of any virus encountered by consumers from cross-contamination.

624 Given these considerations, the frequency of occurrence for the UK

630 and disinfection.

653 As previously discussed, humans can exhibit a range of symptoms when

727 While there is no epidemiological evidence that AI infections in humans occur

755 Declaration of Interests

758 CRediT author statement

759 Erica Kintz: Project administration, Conceptualisation, Investigation, Writing- Original

765 Anthony Wilson: Conceptualisation, Writing- Reviewing and Editing

768 Alec Kyriakides: Writing- Reviewing and Editing

794 Infectivity of H7 LP and HP influenza viruses at different temperatures and pH and

832 Document]. URL https://www.cdc.gov/flu/avianflu/reported-human-infections.htm

835 Avian Influenza (Flu) [WWW Document]. URL

838 Dis. Control Prev. URL https://www.cdc.gov/flu/avianflu/avian-in-humans.htm

842 Safety Concerns. Annu. Rev. Food Sci. Technol. 2, 37–57.

845 Department of Agriculture’s Egg Pasteurization Processes on the Inactivation of

923 Emerg. Infect. Dis. 10, 2189–2191. https://doi.org/10.3201/eid1012.040759

959 NHS, 2018. Bird flu [WWW Document]. nhs.uk. URL

996 J. 9, 61. https://doi.org/10.1186/1743-422X-9-61

1043 Microbiol. 108, 268–271. https://doi.org/10.1016/j.ijfoodmicro.2005.08.032

1047 81–85. https://doi.org/10.1637/7260-081104R

1078 Perspect. Med. 11, a038620. https://doi.org/10.1101/cshperspect.a038620

1082 (accessed 11.14.23).

1085 influenza-outbreaks-in-animals-pose-risk-to-humans (accessed 11.23.23).

Response % of respondents eating % of respondents eating

Most of the time 1% 8%

Infants and children < 5 years of age (n = 4,227)

eggs (n = 49) 16 43 58.6 112.1

Occurrence Rawa LTTCb Cooked

About once a week 7% 24% 27%

About once a month 4% 11% 15%

Never 61% 22% 8%

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