Zoonotic Mutation of Highly Pathogenic Avian Influenza H5N1 Virus Identified in the Brain of Multiple Wild Carnivore Species

Abstract

Wild carnivore species infected with highly pathogenic avian influenza (HPAI) virus subtype H5N1 during the 2021-2022 outbreak in the Netherlands included red fox (Vulpes vulpes), polecat (Mustela putorius), otter (Lutra lutra), and badger (Meles meles). Most of the animals were submitted for testing because they showed neurological signs. In this study, the HPAI H5N1 virus was detected by PCR and/or immunohistochemistry in 11 animals and was primarily present in brain tissue, often associated with a (meningo) encephalitis in the cerebrum. In contrast, the virus was rarely detected in the respiratory tract and intestinal tract and associated lesions were minimal. Full genome sequencing followed by phylogenetic analysis demonstrated that these carnivore viruses were related to viruses detected in wild birds in the Netherlands. The carnivore viruses themselves were not closely related, and the infected carnivores did not cluster geographically, suggesting that they were infected separately. The mutation PB2-E627K was identified in most carnivore virus genomes, providing evidence for mammalian adaptation. This study showed that brain samples should be included in wild life surveillance programs for the reliable detection of the HPAI H5N1 virus in mammals. Surveillance of the wild carnivore population and notification to the Veterinary Authority are important from a one-heath perspective, and instrumental to pandemic preparedness.

Mass Mortality of Marine Mammals Associated to Highly Pathogenic Influenza Virus (H5N1) in South America

“…Brains were also congestive with hemorrhagic focus compatible with encephalitis, which explains the neurological signs observed in dying individuals (Fig. 1.2 D); this agrees with the result of other study on mammals infected with H5N1 (5). The small intestine showed necrotic focus compatible with duodenitis.…”

Highly pathogenic avian influenza A (H5N1) in marine mammals and seabirds in Peru

“…Similarly, the marine otter 43 is an aquatic mustelid that inhabits the same rocky shores of Peru and Chile inhabited by sea lions. HPAI A/H5N1-infected otters have been previously reported 2 , and although none were tested here, we have anecdotal knowledge that some otter carcasses have started to wash onto Peruvian and Chilean shores. Fortunately, marine otters do not live in large groups 46 , which might limit intraspecies contagion.…”

“…Direct contact also occurs on islands, islets, and guano headlands, especially in protected areas where large and dense breeding colonies of sea lions and seabirds cohabitate, and where indirect transmission is also possible via guano runoff into the surrounding waters 28,29,31,32 . Another scenario for transmission involves carnivory and scavenging of infected animal carcasses by marine and terrestrial carnivores, as well as by raptors, gulls, and other scavenger birds 2,33,34 . Fishing docks, where fishermen often dispose of waste by dumping it at sea, attract seabirds, sea lions, marine otters and others that come to feed.…”

“…The recent emergence of highly pathogenic avian influenza (HPAI) H5N1 viruses in mammals and birds in the Americas 1,2 presents a severe threat to wild and endangered species, to poultry production 3,4 , and to public health when the virus spills over into humans 3,5 . The H5N1 (clade 2.3.4.4b) virus arrived in North America in late 2021 from Eurasia and spread across the continent in wild birds, spilling over into poultry farms and infecting an alarming number of wild terrestrial mammals, including fox, skunk, bear, bobcat, and raccoon.…”

Spatio-temporal dynamics and drivers of Highly Pathogenic Avian Influenza H5N1 in Chile

“…One of the most worrying issues of the current panzootic is the increasing cases of H5N1 infections in wild mammals, both marine and terrestrial, causing unprecedented mass mortalities (Ramey et al 2022, Bordes et al 2023, Gamarra-Toledo et al 2023b, Leguia et al 2023, Puryear et al 2023. Worryingly, RNA sequencing has shown signs of early adaptation of the H5N1 2.3.4.4b clade virus to wild mammals (Vreman et al 2023) and humans (Centers for Disease Control and Prevention 2023), fueling the fears of a new human pandemic (Kupferschmidt 2023). In addition, recent reports of a dog and two cats dying from H5N1 after contact with dead birds in North America (Canadian Food Inspection Agency 2023) rises the potential of wildlife to dog transmission in South American countries like Chile, where a high population of dogs (both owned and stray) occurs on the coast (Cortés et al 2021).…”