Commonground
Senior Moderator
- Article
- Open access
- Published: 11 November 2024
H5N1 high pathogenicity avian influenza virus has killed thousands of marine mammals in South America since 2022. Here we report epidemiological data and full genome characterization of clade 2.3.4.4b H5N1 HPAI viruses associated with a massive outbreak in southern elephant seals (Mirounga leonina) at Península Valdés, Argentina, in October 2023. We also report on H5N1 viruses in concurrently dead terns. Our genomic analysis shows that viruses from pinnipeds and terns in Argentina form a distinct clade with marine mammal viruses from Peru, Chile, Brazil and Uruguay. Additionally, these marine mammal clade viruses share an identical set of mammalian adaptation mutations which were also present in tern viruses. Our combined ecological and phylogenetic data support mammal-to-mammal transmission and occasional mammal-to-bird spillover and suggest multinational transmission of H5N1 viruses in mammals. We reflect that H5N1 viruses becoming more evolutionary flexible and adapting to mammals in new ways could have global consequences for wildlife, humans, and/or livestock.
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Excerpt:
Discussion
Since 2020, the world has witnessed a global epizootic of H5N1 clade 2.3.4.4b viruses with substantial ecological impact on wildlife species, including pinnipeds. Although H5N1 HPAI viruses were previously implicated in the mortalities of harbor seals (Phoca vitulina) and gray seals (Halichoerus grypus) in Europe in 2016–2021[SUP]35,36,37[/SUP] and in North America in May–July 2022[SUP]24,26[/SUP], the magnitude of those mortalities (< 200 deaths in total) would pale in comparison with the impacts that ensued when these viruses arrived in South America. At least 30,000 sea lions have died in Peru, Chile, Argentina, Uruguay, and Brazil[SUP]11,13,14,15,27,29,30,31,32[/SUP]. In addition, HPAI caused the largest mortality event of elephant seals recorded to date, with the death of > 17,000 pups and an unknown number of adults at Península Valdés, Argentina[SUP]33[/SUP]. Our epidemiological account of this outbreak provides clinical observations with ecological context for H5N1 HPAI infection in elephant seals. Furthermore, our viral genome data provides evidence for the evolution of a novel marine mammal clade of H5N1 (2.3.4.4b) HPAI virus that has spread among pinnipeds in several countries of South America, revealing mutations that may have enabled their ability to infect mammals while also retaining the ability to spillover to avian hosts.
While serological surveys indicate broad exposure to influenza A viruses (IAV) in pinnipeds globally, mass mortality events have been rare[SUP]38,39,40[/SUP]. Prior to 2022, the largest IAV outbreak in pinnipeds occurred in 1980, when H7N7 HPAI viruses killed 400–500 harbor seals at Cape Cod, USA, representing ~ 20% of the species’ local population[SUP]41,42[/SUP]. Other significant pinniped mortalities attributed to IAV comprise the death of 162 harbor seals in New England, USA, in 2011 due to H3N8 strain[SUP]43[/SUP] and 152 harbor seals in Denmark in 2014 due to H10N7 strain[SUP]44[/SUP]. Prior to 2023, no pinniped deaths had been attributed to IAV in South America. There are also no published studies reporting on the detection of IAV (or antibodies against them) in southern elephant seals. For northern elephant seals (Mirounga angustirostris), the only IAV detections were asymptomatic infections with human-like H1N1 strains in California, USA, in 2009–2012 and 2019[SUP]45,46,47[/SUP]. Considering that IAV surveys on the Atlantic coast of South America have only reported low pathogenicity avian influenza (LPAI) H11 and H13 strains in coastal birds[SUP]48,49,50[/SUP] and antibodies against H1 strains in fur seals[SUP]39[/SUP], it is likely that southern elephant seals at Península Valdés were naïve to H5 viruses until 2023.
Our data shows that elephant seal pups were severely impacted by H5N1 at Península Valdés, but the extent to which adult elephant seals were affected by HPAI is unclear. The unusually high number of adult carcasses at Punta Delgada, as well as the abnormal haul-outs and the confirmed case in Golfo Nuevo reported here, suggest that adult elephant seals are susceptible to H5N1 (2.3.4.4b) HPAI infection. Furthermore, a dead adult male elephant seal at Punta Tombo (a non-breeding area ~ 190 km southwest of Punta Delgada) was confirmed positive for H5N1 HPAI virus by national authorities in mid-September 2023[SUP]51[/SUP], prior to the onset of the Península Valdés outbreak. Beyond recorded beached carcasses, the complete disruption of the social and breeding structure at Punta Delgada (evidenced by the absence of harems and large alpha males and the presence of motherless pups) suggests that adult elephant seals abandoned the colony prematurely, perhaps after becoming infected. Yet, it is difficult to ascertain the number of adult deaths, which may have happened at sea and will only be accounted for via population censuses at Península Valdés in coming years. Nevertheless, the fact that in 2023 the adult females abandoned the beach probably before being impregnated (which normally occurs when pups are weaned[SUP]52[/SUP]) suggests that this population will likely experience an atypically low birth rate in 2024, even if most adult females survived.
From a disease evolution standpoint, there is growing concern that H5N1 viruses adapted to mammalian transmission could facilitate host jumps to other species, including humans. Mammal-to-mammal IAV transmission is believed to have occurred sporadically among pinnipeds over the years[SUP]41,42,43,44,53,54[/SUP]. The recent demonstration that the H5N1 strain from a human case in Chile (which belongs to the marine mammal clade discussed in this study) is transmissible between co-housed ferrets[SUP]55[/SUP] also supports the notion that mammal-to-mammal transmission could have played a role in the spread of these viruses in marine mammal communities in South America. We posit that the high mortality rate in elephant seal pups is also consistent with mammal-to-mammal transmission, as pups are toothless and nurtured exclusively through nursing from their mothers. Contact with wild birds is minimal and could not explain the death of ~ 95% of all pups born (~ 17,000) in a matter of weeks, over 200 km of coastline along Península Valdés. Some newborns may have been infected before birth, as transplacental transmission of H5N1 HPAI viruses has been reported in humans[SUP]56[/SUP], and high virus loads were detected in aborted sea lion fetuses[SUP]11,30[/SUP]. It could also be that mothers were infected and shed the virus through their milk, infecting their pups[SUP]57,58[/SUP]. Yet, how adult female elephant seals would have been infected in the first place without mammal-to-mammal transmission presents a thornier question. Prior to arriving to give birth at Peninsula Valdés in September, the elephant seals would have spent a solitary winter at sea in the South Atlantic and Southern Oceans[SUP]59[/SUP]. Feeding is an unlikely route of exposure to H5N1 HPAI viruses since elephant seals do not eat birds or mammals, feeding instead on squid, fish, and crustaceans captured in deep waters[SUP]52,60[/SUP], and adult elephant seals will fast while on land[SUP]52,61[/SUP]. Moreover, elephant seals are pelagic and only come to shore and aggregate for a few weeks to breed and later to molt, thus limiting the time window for interspecific interactions and transmission on land[SUP]52,62[/SUP]. The main interactions between birds and elephant seals involve opportunistic scavenging of elephant seals’ placental remains, molted skin, and carcasses by gulls[SUP]61[/SUP] (Supplementary Fig. 1E), which provides more opportunities for mammal-to-bird transmission than vice-versa. In this context, it seems unlikely that bird-to-mammal transmission alone could explain the simultaneity, extent, and speed of the outbreak in elephant seals at Península Valdés. Although there are still many unknowns about the precise viral transmission routes (e.g., contact, environmental, aerosol), seal-to-seal transmission seems the most plausible hypothesis to explain viral dissemination during this outbreak. In experimental infections in several wild mammals and in ferret models, nasal and oral H5N1 virus shedding has occurred as quickly as one-day post-inoculation and lasted about a week[SUP]63[/SUP], suggesting that elephant seals infected soon after hauling out on the beach could have begun shedding virus within a very short period of time.
...https://www.nature.com/articles/s41467-024-53766-5