Influenza of avian origin in UK seal populations: qualitative assessment of the risk to the UK human population

Question 1

About the Human Animal Infections and Risk Surveillance group

Accepted Answer

This document was prepared by the UK Health Security Agency (UKHSA) on behalf of the joint Human Animal Infections and Risk Surveillance (HAIRS) group.

HAIRS is a multi-agency cross-government horizon scanning and risk assessment group, which acts as a forum to identify and discuss infections with potential for interspecies transfer (particularly zoonotic infections).

Members include representatives from:

UKHSA
the Department for the Environment, Food and Rural Affairs (Defra)
the Department of Health and Social Care (DHSC)
the Animal and Plant Health Agency (APHA)
the Food Standards Agency
Food Standards Scotland
Public Health Wales
Welsh Government
Public Health Scotland
Scottish Government
Public Health Agency of Northern Ireland
the Department of Agriculture, Environment and Rural Affairs for Northern Ireland
the Department of Agriculture, Food and the Marine
Health and Safety Executive, Republic of Ireland
Infrastructure and Environment, Government of Jersey
Isle of Man Government
States Veterinary Officer, Bailiwick of Guernsey

Information on the risk assessment processes used by the HAIRS group can be found at HAIRS risk assessment process.

Question 2

Version control

Accepted Answer

Date of initial assessment: June 2022

Version: 2.0

Reason for the review: Updated evidence base to reflect the latest detections in marine mammals and ensure algorithms were still fit for purpose. The global panzootic of highly pathogenic avian influenza A(H5N1) leading to mass mortality events in seals and sea lions is the main focus of the update.

Completed by: HAIRS members

Non-HAIRS group experts consulted: Ian Brown (APHA), Cat Man (APHA), James Barnett (Cornwall Marine Pathology Team), Johanna Baily (University of Stirling), Lara Turtle (Defra), Gavin Dabrera (UKHSA)

Information on the risk assessment processes used by the HAIRS group can be found online.

Question 3

Summary

Accepted Answer

Avian influenza (AI) is an infectious disease of birds caused by the influenza A virus. Birds are the hosts for most avian influenza viruses (AIV), and a variety of influenza subtypes can be found in birds, particularly in waterfowl and shore birds. Domestic poultry are especially vulnerable to infection, and the virus can rapidly cause epidemics in flocks. AIV have long been recognised in Europe, where there is longstanding annual surveillance for poultry and wild bird infections. Whilst there is no routine surveillance for diseases including AIV specifically in marine mammals in the UK, sporadic findings of AIV infecting seals have been reported. These include subtypes A(H3N8) isolated from a juvenile grey seal (Haliochoerus grypus) in 2017, and A(H5N8) from a grey seal and 2 common seals (or harbour seal (Phoca vitulina)) in 2020. Since 2021, AI A(H5N1) has been detected globally in several marine mammal species, including Otariidae (eared seals) and Phocidae (earless seals), causing mass mortality events. Although the UK is home to 38% of the entire world’s population of grey seals, and 30% of the European subspecies of common seals, there have never been reports of AIV transmitting from seals to humans, or vice versa, in the UK. Nevertheless, recent data from mass mortality events in South America suggests mammal to mammal transmission is possible. However, there have been very few reports of either mass mortalities or of AI A(H5N1) in wild mammals in the UK, with just a small number testing positive between 2021 and 2024.

Annexes A to D provide algorithms from which the probability and impact risk ratings are derived, neither of which were rated higher than ‘Low’. However, the quality of evidence in this assessment is frequently poor to satisfactory in what is the most recent scenario of the AIV global epidemic, that of emerging disease events affecting seal populations in the Southern Oceans. This AIV epidemic shows significantly rapid changes over short periods of time and over long international distances, therefore this assessment can only be a marker in a rapidly evolving situation, and updates will almost certainly be required.

Assessment of the risk of infection in the UK

Probability

General population: very low.

The probability of infection would be considered low for those working with infected seals.

Impact

Very low to low.

Level of confidence in assessment of risk

Poor to satisfactory.

AIV outbreaks in seal populations have occurred sporadically over time. Due to the absence of routine disease surveillance in UK seal populations, the true extent of AIV infections in seal populations cannot be determined. The recent mass mortality events in South and North America suggests that marine mammals are susceptible to AI A(H5N1) in highly contaminated environments, which results in a high case fatality rate. We would therefore expect the UK seal population to also be susceptible and for mass die-offs to be observed. There is a paucity of evidence on the susceptibility of humans to AIV’s infecting seals, and only 2 documented incidents of AIV transmission from seals to humans have been reported, both resulting in mild disease in human cases. One human case of AI A(H5N1) in Chile appeared to be due to exposure to high levels of environmental contamination, rather than direct exposure to an infected pinniped, however the sequence of the virus clustered closely to seal and avian origin viruses. Several questions relating to the viral ecology and adaptation to marine mammal hosts exist. Other evidence gaps which were included in the first iteration of the risk assessment were:

How does viral genetic diversity, particularly in recovering seal populations or subpopulations, impact disease maintenance and viral circulation?
Are small host populations more highly impacted by disease events, even in the absence of high mortality?
Do genetic differences between marine mammal hosts (for example, seal species) impact the ecological role of those hosts in virus maintenance and circulation?
Do marine mammal-adapted viruses share molecular signatures of other mammalian adapted viruses?

Some of these have now been answered for AI A(H5N1), notably:

that small and large host populations have been affected, most likely because of the continual introduction of the virus into the populations, from contact with infected wild birds, and the fluid nature of marine mammal populations
multiple seal species have been impacted by this virus (both eared and non-eared seals)
seal adapted viruses do share the same adaptations in the polymerase genes as other mammal adapted viruses.

However, it is still not known whether maintenance and circulation are affected by prior historical infection with other influenza viruses. The high mortality rate in seal pups rather than adults and the lower level of mortality observed in 2024 does suggest this is the case, but the compounding effect of poor food availability and food competition during a strong El Niño event has not been explored.

Actions and recommendations

During April 2021, an information campaign was launched by the Seal Alliance and Defra to educate the public on keeping their distance from seals to protect human and seal health. The general public are advised against approaching and interacting with seals in the UK, even when the animals are in danger or distress.

If a member of the public observes a seal they deem in danger or distress, they should contact an appropriate helpline for advice and assistance (for example, the RSPCA in England and Wales, the SSPCA hotline in Scotland and the USPCA in Northern Ireland).

Individuals who come into close contact with seals as part of their work should consider utilising appropriate personal protective equipment (PPE) including aerosol-related respiratory precautions, and seal-specific precautions such as thick gloves and wooden boards or barriers if direct contact with a seal is necessary (for example, during a seal rescue), to avoid animal bites and reduce the exposure to potential zoonotic infections.

The APHA wildlife expert group maintains close interactions with non-governmental organisations (NGOs) including marine wildlife organisations and rescue centres. Where appropriate, NGOs should be encouraged to collect and submit samples from sick or dead seals to APHA Weybridge diagnostic laboratories for testing, of which AIV should be a considered differential, so to be alerted to changes in viral epidemiology and potential risk. In England, this has been delivered through the publication of a case definition for infection in seals, the formation of a wildlife stakeholder core group, sampling protocols and diagnostic test verification for marine mammals and updates to the legislation (1).

A review of seal health surveillance across the UK is recommended, with the long-term aim to establish routine disease surveillance in marine mammals in the UK.

Please note: this risk assessment provides an ecological perspective on AIV in seal populations globally and reviews the probability of AI exposure from infected seals to humans in the UK. The assessment provides reference to multiple AIV subtypes that have been reported to infect marine mammals, including seals. The assessment focusses on the potential zoonotic transmission pathway of AIV from seals to humans, rather than the potential for such viruses to become adapted for human-to-human transmission. Existing risk assessments for specific AIV subtypes can be found at Avian influenza: guidance, data and analysis.

Question 4

Step 1. Assessment of the probability of infection in the UK human population

Accepted Answer

This section of the assessment examines the likelihood of an infectious threat causing infection in the UK human population. Where a new agent is identified there may be insufficient information to carry out a risk assessment and this should be clearly documented. Please read in conjunction with the Probability Algorithm found at Annexe A.

Is this a recognised human disease?

Outcome

Yes or no.

Quality of evidence

Poor.

Note

As there are only 2 documented incidents involving AI transmission from seals to humans globally, which resulted in mild disease in the human cases, the quality of evidence in relation to human disease following contact with an infected seal is poor. The findings of thousands of dead marine mammals, mostly sea lions, around the western and eastern coast of South America between January and October 2023, with no proven human cases, suggests this would remain a very rare event. This question is therefore answered in the context of AIV from other sources, notably birds.

AIV typically infect a large range of avian species, but also demonstrate the ability to infect mammalian animal hosts and thus pose a potential zoonotic risk to humans. Gradual changes in AI genomes over time, through mutation or genome reassembly, have resulted in several AI subtypes that are either circulating or newly emerging with the potential to trigger global health threats to mammals (2). Although AIVs do not usually infect people, rare cases of human infection do occur following close contact predominantly with infected animals (predominantly infected birds), or their contaminated environments (3).

AIVs are classified into subtypes according to the combinations of different viral surface proteins hemagglutinin (H) and neuraminidase (N). They are further categorised into either high pathogenicity (HP) or low pathogenicity (LP), indicating the severity of disease caused in galliform poultry hosts (4). Most AIVs cause no or mild illness, such as fever or conjunctivitis, in humans. However, subtypes including Asian lineage A(H5N1), A(H5N6) and A(H7N9) are known to have the potential to cause severe disease in humans, with mortality rates of up to 50%. Whilst these subtypes do not easily infect people and have not acquired the ability to cause sustained transmission among humans (5), they are considered subtypes of public health concern.

Is this a zoonosis or is there zoonotic potential?

Outcome

Yes.

Quality of evidence

AIV from seals: poor.

AIV from birds: satisfactory.

Note

As there are still only 2 documented incidents involving AI transmission from seals to humans globally, which resulted in mild disease in the human cases, the quality of evidence in relation to transmission to humans following contact with an infected seal is poor. The findings of thousands of dead marine mammals, mostly sea lions, around the western and eastern coast of South America between January and October 2023, with no proven human cases, suggests this would remain a very rare event. This question is therefore answered in the context of AIV from other sources, notably birds.

HPAI viruses, particularly A(H5) subtypes, are remarkable because of their expanding non-avian host range (6). For example, AI A(H5N1) has caused severe and sometimes fatal disease in several naturally infected species (for example, big cats, pigs and humans). Where AI A(H5) subtypes circulate in animals, then sporadic human cases should not be unexpected in people with close contact or high levels of exposure. This is particularly evident for the Asian lineage subtype A(H5N1), with 893 human cases being reported from 24 countries between January 2003 and June 2024 (7). Human cases (463 deaths) of AI A(H5N6) are also being more frequently reported. As of 5 July 2024, a total of 92 laboratory confirmed cases of human infection with AI A(H5N6) virus, including 37 deaths, have been reported to the World Health Organization (WHO) from the Western Pacific Region since 2014. Human infections with other subtypes including AI A(H3N8) (3 cases in China), A(H7N4) (one case from China) and A(H9N2) (98 cases from China, 2 from Cambodia and 1 in Vietnam) have also been reported, predominantly following exposure to infected poultry or wild birds (8).

In February 2021, Russia reported the first human infections of AI A(H5N8) (9). Phylogenetic analysis of viral isolates from these cases indicated that the strain was genetically similar to AI A(H5N8) that had been circulating in wild and domestic birds in the Eurasian region since July 2020 (10), and possessed several molecular markers associated with mammalian adaption (11). Phylogenetic and whole genome sequencing analysis of the human virus at the protein level revealed critical mutations in proteins which contribute to increased virulence and avian-to-human adaptation (12). Whilst these human cases were asymptomatic and there was no clinical evidence of onward transmission, this incident reaffirmed the zoonotic potential of this subtype, which, along with other subtypes, may become more adapted to non-avian hosts over time (9).

In March 2023, Chilean health authorities reported Chile’s first human case of AI A(H5N1). Epidemiological investigations revealed the case lived near the seashore where seabirds infected with AI A(H5N1) had previously been detected. The investigation concluded that the case most likely acquired infection due to exposure to high levels of environmental contamination, rather than direct exposure to infected animals. However, the sequence of the virus clustered closely to seal and avian origin viruses (13).

In June 2024, the WHO reported a fatal human case of AI A(H5N2) in Mexico. This was the first human detection of AI A(H5N2) reported globally. Whilst the source of infection could not be determined, AI A(H5N2) had been detected in poultry in Mexico. It was concluded that AI A(H5N2) infection came secondary to complications associated with co-morbidities as a cause of death in this case (14).

In the UK, as of July 2024, 5 human infections with AI A(H5) were reported (15). In January 2022, a laboratory confirmed human case of AI A(H5) (neuraminidase confirmation unknown) was reported for the first time in the UK. The case lived in the Southwest of England with a large number of domestically kept birds which displayed onset of illness on 18 December 2021 and subsequently tested positive with HPAI A(H5N1). Genomic analysis of isolates from the infected birds demonstrated no strong correlates for specific increased affinity for humans (16). A further 4 cases of HPAI A(H5N1), unrelated to the first case, were reported between March and May 2023, in farm workers in England who had exposure to infected poultry. The cases remained clinically asymptomatic and no subsequent human to human transmission was detected (17).

Mammalian viral adaptation and changes to viral pathogenicity

LPAI viruses have demonstrated the ability to transmit from birds to mammal populations including swine, horses, mink, whales and common seals, spreading beyond the respiratory tract in some of these species and resulting in severe disease and mortality (6). Following increased awareness for potential spread of influenza A subtypes of avian origin to other hosts, additional surveillance and analyses have been established to identify subtypes infecting novel host species. Those have included cats, dogs and marine mammals, the latter being of interest due to the detection of numerous subtypes found infecting both cetaceans (H1N3, H13N2, H13N9) and pinnipeds (H7N7, H4N5, H4N6, H3N3, H1N1, H3N8, H10N7, H5N8) (18).

AI transmission from avian to mammalian species, may play an important role in the evolution of new mammalian viral strains (19). After interspecies and sustained transmission of AI in a new host population, viral adaptation may alter the transmissibility and/or pathogenicity of the virus in both terrestrial and marine mammals (20). For example, the pathogenicity of AI A(H7N7) isolated from seals increased in mammalian species such as mice, ferrets and rats, but only after several passages of the virus in chicken embryo cells (21). These findings suggest a loss in viral pathogenicity following adaptation to mammals, which could only be regained via passage through a poultry host. Whilst AI A(H7N7) found in dead seals was genetically similar to other AI viral strains, it behaved biologically more like a mammalian strain, replicating to high titres in ferrets, cats and pigs (22). By contrast, it replicated poorly and produced no clinical signs in avian species (chickens, ducks, turkeys and parakeets) and faecal shedding in these animals after experimental infection was not detected. This was probably due to its adaptation to mammalian hosts during replication in seals (22). The exact mechanism involved in viral transmission from bird to seal remains unclear. Moderate attachment of AIV to the cell receptors in the trachea and bronchi of common and grey seals suggests high susceptibility to these viruses within these species (23).

The recent AI A(H5N1) detections in marine mammals include mass mortality events of (24 to 29):

several thousand Pacific and South American sea lions (Otaria flavescens and Otaria byronia) in Peru and Chile
several thousand Southern Elephant seal pups (Mirounga leonina)
small numbers of common dolphins (Delphinus delphis)
Chilean dolphins (Cephalorhynchus eutropia)
marine otters (Lontra feline)
river otters (Lontra provocax)
Burmeister’s porposies (Phocoena spinipinnus)

In November 2023, AI A(H5N1) was also detected in the South Atlantic, in Southern Elephant seals and South American fur seals (as well as kelp gulls, brown skuas, terns and shags) in the South Sandwich Islands, South Georgia and Falkland Islands (30), prompting concerns this could spread around Antarctica in wild birds, to Australia and New Zealand.

Sequence analysis of the virus from sea lions in Peru and Chile strongly suggest there were just 2 incursions: the first in Peru, which spread into Chile, and a second into Chile. A third incursion could also be attributed to the spread in pinnipeds from Argentina to Uruguay and Brazil along the eastern coast of South America (26). Just before and during the mass mortalities were observed in mammals, large die-offs of “guano birds” were observed in the same coastal areas including Peruvian boobies, Peruvian pelicans, Guanay cormorants as well as Peruvian gulls and Humboldt penguins (27). More than 100,000 birds were estimated to have died and 30,000 sea lions. Again, sequence analysis of virus from these populations confirmed likely transmission from wild birds to the marine mammals.

Some mammal sequences showed typical polymerase gene adaptations to mammal receptors, such as PBS D701N. There has also been some limited spread back into the wild birds (terns and sanderling (27)), which suggests the virus has not adapted exclusively to mammals.

In October 2023, a die-off of Southern Elephant seals was reported off Peninsula Valdez, Argentina. Over a month’s duration, 95% mortality of seal pups was observed, which resulted in a breakdown of social structure in the colony and increased mingling of conspecifics including kelp gulls which were scavenging on the carcases (27). The sequence was identified as clade 2.3.4.4b B3.2 genotype, which is an ancestral virus for the B3.13 genotype detected in dairy cattle in the USA. B3.2 viruses have a reassortant genotype with 4 segments from the Eurasian H5 lineage 127 (PA, HA, NA, and MP) and 4 segments from low pathogenicity AIVs from the North American lineage (PB2, PB1, NP, and NS). These viruses cluster within Argentina marine mammals and coastal birds, less so with poultry cases and less so with the Peru and Chile marine mammals. Detailed analysis of the marine mammal sequences suggests a lower evolution rate compared to avian viruses, but whether this is attributable to the different transmission routes and exposure to infectious doses is not clear.

Whilst neurological and respiratory signs were observed in sick animals, it is uncertain about the attribution of mortality to infection with AI A(H5N1) alone, as there was a concurrent El Niño event. One aspect of a strong El Niño event is that there is a reduced upwelling of nutrient rich water in the Humboldt current, which can lead to population crashes of birds through reduction in normal prey. This would also mean marine mammals may be more likely to forage and scavenge as their hunting behaviour will be less successful, which could have led to animals consuming carcases of dead birds.

A small number of sea lions continued to die over the summer, but not in the same magnitude as in 2023 (Uhart, personal communication). The last breeding season was very successful for marine mammals, except those affected by AI A(H5N1), but the long-term impact is not known.

Influenza virus transmission between humans and seals

There are limited reports of influenza transmission between humans and seals. In 2010, whole genome sequencing of influenza A(H1N1) from healthy Northern elephant seals revealed greater than 99% homology with A/California/04/2009 (H1N1) (pH1N1) that emerged in humans from swine in 2009 (31). This was the first report of pH1N1 (A/Elephant seal/California/1/2010) in any marine mammal and provided evidence for cross species transmission of influenza A virus to free-ranging wildlife from humans (31).

There have been only 2 documented incidents of AIV transmission from seals to humans. During the 1979 to 1980 AI A(H7N7) outbreak in common seals in the northeast of the US, purulent conjunctivitis was observed in 4 people who had been involved in autopsies of dead seals, but no virus isolation was attempted in that period (32). However, during subsequent experimental infections of common seals using the identical virus, an infected animal sneezed on an investigator’s face, who then developed severe conjunctivitis. Two days post infection, AI A(H7N7) was isolated from a swab sample of the patient’s conjunctival membrane. The authors reported the virus as being antigenically very close to A/FPV/Dutch/27 (H7N7), which had been responsible for a case of human influenza virus infection following an accidental laboratory exposure in 1977. AI A(H7N7) infecting the seals proved to have the potential to cause conjunctivitis in humans but not sustained human-to-human transmission. The affected people reported in these studies recovered without complications, and antibodies to the virus were not detectable in the serum of infected individuals.

Is the disease endemic in the UK?

Outcome

No.

Quality of evidence

AIV in seals: poor.

AIV in birds: satisfactory.

AI is not considered endemic in the UK, and whilst outbreaks in birds can occur at any point in the year, the UK typically experiences a seasonal increase of AI associated with incursions of infected wild migratory birds during the winter. Infected migratory birds can subsequently infect local and sedentary wild bird species, poultry or other captive birds. This can result in local transmission either directly between birds or indirectly by birds encountering environmental contamination, including faeces and feathers from infected birds. Where infected birds are present, then transmission to other species, including mammals, may occur. For example, in coastal regions, contact between marine mammals (for example, seals) and infected seabirds at hauling-out sites or when feeding on a common food source may result in cross-species AIV transmission (20).

Sporadic findings of AI in seals have been reported in the UK. These include subtypes A(H3N8) isolated from a juvenile grey seal (Halichoerus grypus) in Cornwall during 2017 (33), and A(H5N8) from a grey seal and 2 common seals (or harbour seal (Phoca vitulina)) in Norfolk during 2020 (34). Due to the absence of routine disease surveillance in UK marine mammalian populations, it cannot be determined if AIV in these species is incidental, or if AIV’s exhibit endemicity in UK seal populations.

Grey and harbour seal populations are widespread across the North-East Atlantic Ocean. Both species forage in coastal and open sea, however, they return to land-based haul-out sites where they rest, moult and breed. These haul-out sites may be utilised by individual seals either on a year-round basis or at specific times of year for either breeding or moulting. While harbour seals commonly forage within 50km of their chosen haul-out site, grey seals often forage at more offshore sites (over 100km from land) and may utilise many different haul-out sites during the year (35).

During the HPAI A(H5N1) epizootic in the UK, a case definition for wild mammals was used to triage seal samples for testing at APHA Weybridge. This resulted in 5 findings in grey seals in Cornwall, one harbour seal in each of Fife, Orkney and Highland (all in 2022) and one harbour seal in Aberdeenshire in 2021. Three cetaceans (2 common dolphins and a harbour porpoise) tested positive in 2023, but no seals. This is against a backdrop of significant mortality events in coastal seabirds around the GB coast, including areas where seals would be using haul-out sites. Further retrospective testing of 23 seal pup brain samples from Cornwall in 2023 and 2024 were also negative. This retrospective testing will be included in future surveillance to compliment the report cases.

Characteristics of epizootics of influenza among seal populations (global)

Influenza A infection has been detected in marine mammals dating back to 1975, with additional unconfirmed outbreaks as far back as 1931. Over the past forty years, infectious virus has been recovered on approximately 10 separate occasions from both pinnipeds (common seal, Northern elephant seal (Mirounga angustirostris), and Caspian seal (Pusa caspica)) and cetaceans (Striped dolphin (Stenella coeruleoalba) and long-finned pilot whale (Globicephala melaena)). Recovered viruses have spanned a range of subtypes (H1, H3, H4, H7, H10, and H13) (20) and, in all but A(H1N1), show strong evidence for deriving directly from avian sources. Prior to the 2021 to 2024 panzoonotic, there were 5 unusual mortality events in seals directly attributed to influenza A viruses – these have primarily occurred in common seals in the North-eastern United States and in the North Sea. In July 2022, the US Department of Agriculture’s Animal and Plant Health Inspection Service’s National Veterinary Services Laboratories confirmed that samples from 4 stranded seals in Maine, US, tested positive for Highly Pathogenic AI A(H5N1) (36). No associated human infections were reported during these incidents. However, since 2021, the number and scale of mortality in pinniped populations in South and North America have sharply risen. Given this same level of mortality has not been seen in other regions of the world, it would suggest that this is related to the strains of virus circulating in North and South American wild birds, most of which are reassortants with American low pathogenic AI strains.

According to the Food and Agriculture Organization, which maintains a list of all species affected by the panzootic, the following Pinnipeds have tested positive:

Otariidae (eared seals):
- Arctocephalus australis (South American Fur seal)
- Callorhinus ursinus (Northern Fur Seal)
- Otaria flavescens (South American sea lion)
Phocidae (non-eared seals):
- Halichoerus grypus (Grey seal) (tested positive in the UK)
- Mirounga leonina (Southern elephant seal)
- Phoca vitulina (Harbour seal) (tested positive in within the UK) *Pusa caspica (Caspian seal)

Are there routes of introduction into the UK?

Outcome

Yes for wider clades of AI A(H5N1), no for Eurasion and North American reassortant viruses.

Quality of evidence

Satisfactory.

The UK typically experiences a seasonal increase in AI incidents associated with incursions of infected wild migratory birds during the winter months. Infected migratory birds can subsequently infect local and sedentary wild bird species, poultry or other captive birds. In recent years, the strains of AI(H5N1) detected in the UK have been Eurasian origin or European low pathogenic AI reassortants of clade 2.3.4.4b. During the last 3 years, the strain dominance has changed, and different wild bird populations have been hosts to different strains to those found in poultry. The emergence of highly pathogenic AIV in seabirds Stercorariidae and Laridae, particularly during summer 2022, would have posed a significant threat to wild bird and marine mammal life. However, no mass mortality events in seals were reported. The routes of introduction from North or South America would be limited to wild bird incursions, rather than seal migration or population mixing.

Influenza A viruses in marine mammals with linked avian origin

The current knowledge of AI infecting marine mammals, including antigenic and phylogenetic analyses of isolated viruses, suggests that transmission from wild birds is the most probable route of AI introductions into marine mammal populations (25 to 29 and 37 to 41). For example, phylogenetic analysis of 3 AI subtypes including A(H1N3) and A(H13N2) from whales, and A(H7N7) from seals revealed high genetic relatedness to isolates from gulls and terns (42), with introductions of AI from wild birds into marine mammal populations likely occurring on multiple, independent occasions (19). The same is likely to be the case with the mass mortalities in South America (30). Prior to 2022, it was considered that whilst viruses can transmit to mammalian populations, the mammals are unlikely to act as reservoir hosts and sustain endemic infection. It remains the case for the majority of spill-over infections into marine mammals, but for certain species of seal, in particular circumstances, infected with certain strains, infection can be maintained within the species group due to the close direct contact. However, the role of bridging species in such circumstances cannot be ruled out. Often these mass mortality events are in areas where there is difficulty collecting samples or observing the interactions.

Several studies have highlighted the ability of AIV to infect seal species. For example, AI A(H5N8) was isolated from lung samples of 2 grey seals stranded on the Baltic coast of Poland in 2016 and 2017. The clade was closely related to A(H5N8) circulating in European avian species at the time (43). In December 2020, A(H5N8) nucleic acid was detected following post-mortem in brain and lung tissues of a grey seal and 2 common seals that had recently died at a wildlife rehabilitation centre in the UK. Genetic sequencing revealed a 99.9% similarity to A(H5N8) detected in mute swans (Cygnus olor) that were also housed at the centre and had died (36). In mid-August 2021, tracheal swabs and tissue samples obtained from 3 adult harbour seals found on the German North Sea coast were investigated for the presence of morbilliviruses, herpesviruses, and AI as part of regular health monitoring. All 3 harbour seals belonged to the same population of approximately 8,850 individuals in the Wadden Sea of Schleswig-Holstein. High viral loads of A(H5N8) were detected in brain tissue of the 3 seals. Whole genome sequencing revealed 2 genotypes – one similar to the HPAI A(H5N8), that dominated the 2020/2021 avian epizootic in Germany, and the other similar to Eurasian LPAI strains found in wild birds and poultry holdings in Germany during the past years. Further analysis revealed the presence of the E627K mutation in the genome (PB2 gene), indicating that replication of avian viruses in seals may allow HPAI to acquire mutations needed to adapt to mammalian hosts (44, 45).

In September 2021, the Danish Veterinary Consortium detected A(H5N8) in a deceased harbour seal found on a beach in Southwest Funen. The seal was emaciated with pronounced skin changes on large parts of the body. AIV was detected in the lung, but otherwise no other disease-causing organisms could be detected that could provide an explanation for the seal’s death. The Centre for Diagnostics examined 29 harbour seals and 15 grey seals in 2021, with only one testing positive for AIV. The detected virus was closely related to those circulating in wild birds and domestic poultry in Denmark and the rest of Europe during the Autumn of 2020 (46).

The recent viral incursions into sea lions and elephant seals have been sequenced, revealing not only PB2 E627K but also D701N as well as Q591K, PB1 L584F and Q621K (only in the Argentinian samples only) all of which suggest limited mammalian adaptation. There were no consistent adaptations in the HA gene which would be consistent with mammalian or human receptor binding (27).

The most notable event associated with AI in seals in Europe occurred in 2014, where increased mortality was reported among common seals along the coasts of Sweden and Denmark, associated with AI A(H10N7) infection (47 to 49). Subsequent spread of the virus to seals along the coast of Germany resulted in between 1,500 and 2,000 seal deaths (48). The virus was also detected in dead seals along the coast of the Netherlands between November 2014 and January 2015. Mass mortality suggested rapid seal-to-seal transmission during these outbreaks, and that seals may act as short-term intermediate hosts following a spill-over event that facilitates transmission within and possibly between species. In the wild, contact between marine mammals and bird species at hauling-out sites, or when feeding on the same food resources (for example, fish or krill species), may facilitate cross-species transmission of AIV (20).

The risk of influenza epizootics spreading from northern European seal populations to UK seal populations

There are 2 species of UK resident seal species: the common (harbour) seal and the grey seal. These 2 species breed at specific sites on the coast of Great Britain and Ireland which they typically reuse each year, and are resident around the coast all year round, hauling out to breed, nurse their young, moult and rest. While the harbour seal is a circum-polar species, there are 4 subspecies recognised, the eastern and western Pacific and eastern and western Atlantic. Only the eastern Atlantic subspecies P. vitulina occurs in Europe, where its range extends from Iceland and northern Norway southwards to northern France, including the Kattegat-Skagerrak and south-western Baltic. The UK population represents about 5% of the world population of P. vitulina, approximately 50% of the EU population, and 45% of the European subspecies. Grey seals are among the rarest seals in the world: the UK population represents about 40% of the world population and 95% of the EU population. Globally, there are 3 reproductively isolated populations of grey seal: a west Atlantic (northern North American) stock, a Baltic stock, and an East Atlantic stock. The latter extends from Iceland and northern Norway southwards to northern France, with the majority breeding around Great Britain and Ireland. The breeding season (which occurs from summer to early winter) requires residency for periods of time on the shore, with negligible inland movement. Occasionally, individual seals swim considerable distances (kms) upstream from river estuaries.

Vagrant seal species include bearded seal (Erignathus barbatus), ringed seal (Pusa hispida), harp seal (Pagophilus groenlandicus) and hooded seal (Cystophora cristata). These are putative carriers of epizootic viruses from Arctic waters, for example, phocine distemper virus (PDV), though there is no evidence of these species being infected with AIV. Walruses (Odobenus rosmarus) occasionally move through UK waters but are not known to carry AIV or PDV.

Seal populations (both resident and vagrant species) from other European countries, including Ireland, Iceland, the Faroe Islands, Norway, Sweden, Denmark, Germany, Netherlands, Belgium, France, Spain and the Arctic may move or migrate to the UK. There are known examples of seal movements between these countries and some of these movements could be considered migrations – for example, the grey seal movements across the Irish, Celtic and North Seas as confirmed through photo identification or satellite telemetry.

AIV circulation in such countries could therefore indicate a higher risk of disease introductions into UK seal populations. Common and grey seals from Ireland, France, the Netherlands, Belgium, Germany, Denmark and Norway are considered to mix with UK seal populations. Whilst it is not possible to determine which seal species may present a greater AIV transmission risk into UK seal populations, the risk of AI infections from seals from these countries will be higher than from the other listed countries in Scandinavia or the North Atlantic. However, the large A(H10N7) outbreak in 2014 to 2015 which started in the Baltic and travelled westward to the Netherlands, did not affect UK resident seals, demonstrating that transmission between seal populations in different countries is not guaranteed. Many factors could have prevented the onward transmission of this pathogen, including the time of year and weather conditions. Thus, it should not be assumed that Baltic or Netherlands AIV infections in seals will not reach UK seal populations.

Within the UK, seal populations (particularly grey seals) will move around coastal waters. Whilst grey seal populations are highly mobile, a slight divide between those in Southwest England and Wales and those in Scotland and the east coast of England is observed. However, even that divide has been breached. Common seals will move along the east and south coast of England and are also known to have crossed the North Sea.

Extrapolating from previous PDV epidemics, which were thought to have been introduced to naïve European seal populations by closely related species such as harp seals or hooded seals (50), transmission of AIV between seal species seems likely. PDV epidemics have affected the seal populations of several countries around the North Sea, including those of the UK, implying connectivity in these populations. There are current concerns regarding viral re-emergence of PDV due to receding Arctic sea ice, which may result in increased inter-species contact or altered intra-species dynamics (51), potentially increasing the likelihood of emergence or transmission of a novel virus.

With the AI A(H5N1) viruses circulating around the world in the last 4 years, reassortments are commonplace, particularly with regional LPAI viruses. The species host range has expanded considerably in both avian species and mammals. The low infectious dose and tissue tropism has meant animals consuming infected carcasses have been particularly prone to severe infection. Therefore, even though there have been no signals to suggest the same impact is occurring in the seal populations in the UK, and although the current level of circulating virus is low, the situation should merit continual monitoring.

Are effective control measures in place to mitigate against these routes of introduction?

Outcome

No.

Quality of evidence

Satisfactory.

There are no control measures preventing the migration of infected seals or wild birds into the UK. National surveillance and control of AIV in poultry and wild birds is conducted annually by UK Government’s Defra and APHA. UK public health agencies work closely with Defra, Scottish and Welsh governments and APHA during AI incidents where there are human exposures to infected birds (see (52)).

Disease surveillance, including of AIV, in marine mammal hosts is limited and poses numerous challenges due to the size, habitat, and protected status of these animals. National surveillance of seal mortalities in England and Wales presents specific challenges, for example, for maintained observer effort (particularly on islands) of seal carcases and the difficulties in getting large carcasses on hazardous coastal sites to suitable road-side collection points. Currently, morbidity and mortality surveillance of Cornish seal populations is arranged through multi-agency cover in that county. In the rest of England and Wales, although the APHA Diseases of Wildlife Scheme has a remit to investigate seal deaths and mass mortalities, the coverage is opportunistic and not systematic. Therefore, there is a risk that early identification of such events, including AIV outbreaks in seal populations, may not occur. It should also be noted that AIV may not initially be considered as the primary cause of mortality, given that there are more common causes of seal deaths including other infectious diseases such as bronchopneumonia, emaciation or starvation, anthropogenic trauma and predation (53).

Most sampling of marine mammal hosts is reflective of the bias in the literature toward outbreak investigation and has relied on opportunistic approaches, primarily to sample stranded or dead animals. While this approach has been successful for identifying virus in several outbreaks, it may be ineffective for monitoring or when disease manifestation is subtler. For example, sick animals may typically avoid interactions with humans until clinically moribund or dead, at which point, the chances of detecting virus may be far diminished due to degradation and the chances of viral isolation correspondingly smaller. Techniques have been developed to capture animals, but they are largely based on target sample sizes of only a few animals, inadequate for surveillance purposes and particularly for endemic viral circulation where only a small percentage of animals are expected to be shedding virus at any given time. Moreover, these operations tend to require costly support in terms of multiple personnel with handling, veterinary, and technical knowledge.

The UK Cetacean Stranding Investigation Programme (CSIP) has been running since 1990 and is funded by Defra and the Devolved Administrations. Whilst the remit of the programme is to investigate cetacean (for example, whale, dolphin and porpoises), sea turtle and basking shark (Cetorhinus maximus) strandings, the programme was expanded in December 2021 to include a one-year pilot for routine post-mortem of seals. This has continued and a case definition for triage purposes is used to ensure dead seals can be sampled. In addition, the sampling techniques and testing protocols have been optimized for seal samples.

Do environmental conditions in the UK support the natural reservoirs or vectors of disease?

Outcome

Yes.

Quality of evidence

AIV in birds: good.

AIV in seals: poor.

In the UK, outbreaks of AI are reported annually in wild and domestic birds as detected through long-standing surveillance programmes (see above).

While there is no routine disease surveillance, including for AIVs, in marine mammals in the UK, sporadic and incidental findings of AI infecting seals have been reported. This includes the isolation of AI A(H3N8) from a seal pup in Cornwall in 2017 (33), and AI A(H5N8) from grey and common seals at a wildlife rehabilitation centre on the Norfolk coast in 2020 (34) and AI A(H5N1) detections in both harbour and grey seals between 2021 and 2022. No human cases were associated with these incidents.

The UK is home to 38% of the entire world’s population of grey seals, and 30% of the European subspecies of common seals, and thus further detections of AIV in seals may not be unexpected in the future, as AIVs continue to circulate in wild birds.

Will there be human exposure?

Outcome

No: general population.

Yes: for individuals interacting with infected seals.

Quality of evidence

Satisfactory.

The general population is unlikely to be exposed to an infected seal. Although the magnitude of human-seal interaction in the UK is unknown, interactions between the general public and seals on beaches or whilst participating in recreational activities near seal habitats (for example, water sports) would likely be transient in nature. However, disturbances to seals by humans is a significant and growing problem in the UK. Such interactions could result in physical injury to a member of the public, for example, being bitten by a seal, and exposure to other zoonoses being harboured by an infected animal.

Human infections of AI reported in the scientific literature have predominantly been attributed to close contact with infected poultry, wild birds or contaminated materials. As described above, there have been only 2 reported incidents of AI transmission from seals to humans. Both incidents involved AI A(H7N7), and the 5 human cases developed conjunctivitis with no further complications. No sustained human-to-human transmission was observed (32).

There have never been reports of AI transmitting from seals to humans, or vice versa, in the UK. Unprotected contact with infected seals and/or contaminated tissues and fluids from an infected seal present the greatest risk of exposure to humans, particularly to those who have regular contact with seals, such as volunteers or staff at rescue and rehabilitation centres, veterinarians treating sick seals, and seal pathologists. For individuals interacting with seals as part of their work, the risk of exposure would be higher, although mitigated if appropriate PPE is worn (see Action and recommendations at the beginning of this assessment).

Note

Whilst the zoonotic risk may be greater from a symptomatic seal to a human, zoonotic disease transmission from asymptomatic animals should not be excluded, and individuals handling apparently ‘healthy’ animals should take appropriate precautions.

Are humans highly susceptible?

Outcome

No.

Quality of evidence

AIV from seals: poor.

AIV from birds: satisfactory.

While there are many different AIV subtypes (54), most have never been observed to infect humans. Although the number of human infections with specific subtypes of AIV has increased in recent years (for example, AI A(H5N6) cases in China), human cases remain rare. There are 4 subtypes of greatest public health concern, all Asian lineage:

A(H5N1) (since 1997)
A(H7N9) (since 2013)
A(H5N6) (since 2014)
A(H5N8) (since 2016)

In recent years, with the global circulation of Eurasian clade 2.3.4.4b viruses, there have been a number of human cases as a result of close contact with infected animals and their contaminated environments. In North and South America, 3 human infections caused by AI A(H5) were reported between 2022 and 2023 from the USA in April 2022 (55), Ecuador in January 2023 (56) and Chile in March 2023 (13). The single human case in Chile could have been attributed to close contact with either dead wild birds or dead marine mammals, both of which were present in the area close to the case’s home. The patient was hospitalized with severe respiratory symptoms, requiring respiratory support due to pneumonia and recovered after treatment with oseltamivir and antibiotics. The viral sequence clustered with those from wild sea birds (pelicans and black gulls) collected in Chile (13). More recently, 4 human cases have been reported in the USA, in people with exposure to infected dairy cattle and 10 cases in poultry catchers, in contact with poultry infected with the same cattle virus. All cases reported mild respiratory and conjunctival symptoms (57 to 59).

Testing of poultry workers on AI A(H5N1) infected premises detected cases in Spain (2 cases (60)) and the UK (4 cases (17)), although with no serology testing available, it is difficult to apportion the test result to systemic infection.

Human infections with AIV are usually the result of close, prolonged and unprotected (for example, absence of PPE) contact with infected animals or their contaminated environments. Although people have been infected with AIV, subsequent human-to-human transmission is very rarely observed (see (54)).

There is a paucity of evidence on the susceptibility of humans to AIV’s infecting seals.

Outcome of probability assessment

The probability of human infection with AIV from seals in the general UK population is considered very low.

For individuals interacting with infected seals, the probability would be considered low and should be managed with appropriate PPE.

Question 5

Step 2: Assessment of the impact on human health

Accepted Answer

The scale of harm caused by the infectious threat in terms of morbidity and mortality: this depends on spread, severity, availability of interventions and context. Please read in conjunction with the Impact Algorithm found at Annexe C.

Is there human-to-human spread of this pathogen?

Outcome

Yes or no.

Quality of evidence

Poor.

Note

As there are only 2 documented incidents involving AI transmission from seals to humans globally, which resulted in mild disease in the human cases, the quality of evidence in relation to subsequent human-to-human is poor. This question is therefore answered in the context of AIV from other sources, notably birds.

Almost all human infections with AIV have been linked to close contact with infected birds or their contaminated environments (3). Although people have been infected with AIV, subsequent human-to-human transmission is very rarely observed (see (61)). Where human-to-human transmission has been reported, this has only involved a few individuals and is not sustained. However, because of the possibility that AIVs could mutate and gain the ability to transmit more readily between people, monitoring for human infection and onward transmission is essential for protecting public health.

Is there zoonotic or vector borne spread of this pathogen?

Outcome

Yes.

Quality of evidence

Poor.

Almost all human infections with AIV have been linked to close contact with infected birds or their contaminated environments (3). To date, there have been no reported transmission events of AIVs from seals to humans in the UK. Globally, there have been only 2 reported incidents of AI transmission from seals to humans (32). Both incidents involved AI A(H7N7), and the 5 human cases developed conjunctivitis with no further complications. No sustained human-to-human transmission was observed.

Nevertheless, it is clear that with the AI A(H5N1) virus clade 2.3.4.4b Eurasian/North American reassortants, human infection from close contact with heavily contaminated environments or high viral loads in animal secretions is possible, albeit with usually mild symptoms only. The ability of this virus to transmit to humans through respiratory routes is not known. Experimental work using the Chilean human isolate and ferrets suggest transmission to indirect contact ferrets is not possible through aerosol routes but was highly effective at infecting animals through the ocular route. However, this is using only a limited number of animals (53,54).

For zoonoses or vector-borne disease is the animal host or vector present in the UK?

Outcome

Yes.

Quality of evidence

Good.

AI is not considered endemic in the UK, and whilst outbreaks can occur at any point in the year, the UK typically experiences a seasonal increase of AI associated with incursions of infected wild migratory birds during the winter. Infected migratory birds can subsequently infect local and sedentary wild bird species, poultry or other captive birds in the UK. This can result in local transmission. Where infected birds are present, then transmission to other species, including mammals, may occur.

The epizootic between 2021 and 2023 in the UK was unprecedented in duration and scale. Several thousand wild birds were affected, including sea bird colonies around the coast of the UK. These were detected during the summer, and it was likely there was heavy viral contamination of the environment where seals would haul out for breeding or moulting. Nevertheless, no mass mortality events in seals were observed.

The UK is home to 38% of the entire world’s population of grey seals, and 30% of the European subspecies of common seals. In the UK, there have been sporadic and incidental findings of AIV infecting seals. This includes the isolation of AI A(H3N8) from a seal pup in Cornwall in 2017 (33), and AI A(H5N8) from grey and common seals at a wildlife rehabilitation centre on the Norfolk coast in 2020 (34) and AI A(H5N1) from a small number of grey and common seals in 2021 and 2022.

Is the UK human population susceptible?

Outcome

See above evidence.

Are effective interventions (preventative or therapeutic) available?

Outcome

Yes.

Quality of evidence

Satisfactory.

There are no control measures preventing the migration of infected seals or wild birds into the UK. Additionally, disease surveillance, including of AIV, in marine mammal hosts in the UK is limited, but has been increased since 2021, based on the recommendations in the original version of this risk assessment. National surveillance and control of AIV in poultry and wild birds is conducted annually by UK Governments Defra and APHA. UK public health agencies work closely with Defra, Scottish and Welsh governments and APHA during AI incidents where there are human exposures to infected birds (see (52)).

In the UK, there are well established pathways for the prompt diagnosis and treatment of a human case of AIV (52). Cases and exposed individuals may be given antiviral medicine such as oseltamivir (Tamiflu) or zanamivir (Relenza), which help reduce the development of disease or severity, prevent complications and improve the chances of survival (61). To date, there have been no documented incidents of AIV transmission from an infected seal to a human in the UK, and so such pathways have never been applied in this scenario.

Outcome of impact assessment

The impact of AIV from seals on human health in the UK is considered very low to low.

Note: detailed risk assessments for individual AIV subtypes can be found at Avian influenza: guidance, data and analysis.

Question 6

Annexe A: Assessment of the probability of infection in the UK population algorithm

Accepted Answer

Question 7

The probability of infection in the general UK population is high

No

The probability of infection in the general UK population is moderate

Question 8

Annexe C: Assessment of the impact on human health algorithm

Accepted Answer

Question 9

The impact on human health in the UK is high

No

The impact on human health in the UK is very high

Question 10

References

Accepted Answer

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About the Human Animal Infections and Risk Surveillance group

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Summary

Assessment of the risk of infection in the UK

Probability

Impact

Level of confidence in assessment of risk

Actions and recommendations

Step 1. Assessment of the probability of infection in the UK human population

Is this a recognised human disease?

Outcome

Quality of evidence

Note

Is this a zoonosis or is there zoonotic potential?

Outcome

Quality of evidence

Note

Mammalian viral adaptation and changes to viral pathogenicity

Influenza virus transmission between humans and seals

Is the disease endemic in the UK?

Outcome

Quality of evidence

Characteristics of epizootics of influenza among seal populations (global)

Are there routes of introduction into the UK?

Outcome

Quality of evidence

Influenza A viruses in marine mammals with linked avian origin

The risk of influenza epizootics spreading from northern European seal populations to UK seal populations

Are effective control measures in place to mitigate against these routes of introduction?

Outcome

Quality of evidence

Do environmental conditions in the UK support the natural reservoirs or vectors of disease?

Outcome

Quality of evidence

Will there be human exposure?

Outcome

Quality of evidence

Note

Are humans highly susceptible?

Outcome

Quality of evidence

Outcome of probability assessment

Step 2: Assessment of the impact on human health

Is there human-to-human spread of this pathogen?

Outcome

Quality of evidence

Note

Is there zoonotic or vector borne spread of this pathogen?

Outcome

Quality of evidence

For zoonoses or vector-borne disease is the animal host or vector present in the UK?

Outcome

Quality of evidence

Is the UK human population susceptible?

Outcome

Quality of evidence

Does it cause severe disease in humans?

Outcome

Quality of evidence

Would a significant number of people be affected?

Outcome

Quality of evidence

Is it highly infectious to humans?

Outcome

Quality of evidence

Are effective interventions (preventative or therapeutic) available?

Outcome

Quality of evidence

Outcome of impact assessment

Annexe A: Assessment of the probability of infection in the UK population algorithm

Annexe B: Accessible text version of assessment of the probability of infection in the UK population algorithm

Question 1: Is this a recognised human disease?

Yes

No

Question 2: Is this a zoonosis or is there zoonotic potential

Yes

No

Question 3: Is this disease endemic in the UK?

Yes