Because influenza viruses repeatedly infect all members of the human population, and humans occasionally come into contact with NHPs, either in the wild, in laboratories or in zoos, direct exposure of animals to infectious people must occasionally occur. However, only a few published articles provide evidence that influenza has been transmitted from humans to monkeys or apes. Only a few reports describe an influenza-like illness in wild or captive primates12,13 .
Four papers have reported the isolation of human seasonal influenza viruses in captive primates. In the first, researchers studying the microbial flora of common marmosets (Callithrix jacchus) imported from South America found an H2N2 virus from the lungs of an animal that had died of bronchopneumonia, at a time when the same virus was circulating among laboratory personnel14. Five years later, the same team isolated an H3N2 virus from 9 of the 25 recently imported white-lipped and white-moustached tamarins (Saguinus nigricollis and S. mystax), none of which showed signs of respiratory illness15. In 1975, Malherbe et al. found a virus with the electron-microscopic features of an influenza virus in tissues of recently imported yellow baboons (Papio cynocephalus), but they didn’t make a definitive identification16. In their investigation of the possible occurrence of influenza in lemurs in Madagascar, Clerc and colleagues reported in 1979 a virus apparently identical to the then-circulating 1977 H1N1 strain from throat swabs of 14 captive animals of 8 different species17. None of the animals displayed cough, respiratory distress or other signs of illness.
Influenza A virus infections occur in both mammals and birds and are classified, based on surface glycoproteins, into 17 haemagglutinin (HA) (H1eH17) and nine neuraminidase (NA) (N1eN9) subtypes18,19. NHPs are susceptible to infection with a number of human influenza A isolates, including viruses of the H3N2, H5N1 and H1N1 subtypes20. Nonetheless, the viral strain found on female emperor tamarin (Saguinus imperator 0.1) is H5N3. IAV H5N3 was identified in different country on different bird species but not on mammals : on terns in South Africa (1961) and on ducks in Singapore (1997). In January 2009, in France, a high mortality was reported on chickens (90/4932) and all the animals were culled after H5N3 confirmation. Other case was reported in Germany in December 2013 where ostriches and chickens were slaughtered after H5N3 confirmation. According to a French institution which manage Influenza A in France (ANSES Ploufragan laboratoires, 22440 Ploufragan, France), the only case of H5N3 infection in the French avifauna was found on Calidris canatus in the Baie of Mont-Saint Michel in 2019. No other case of H5N3 was reported since 2019. Next to the zoo, a nature reserve houses a lot of species, including birds. Nonetheless, between 2019 and 2021, Calidris canatus was not observed by daily observations and no suspicion of Influenza A was reported.
Currently, an epidemiologic survey is in process in order to know how the infection occurred but different hypothesis remains possible. Firstly, aquatic birds are the source of Influenza A virus (IAV), Avian influenza viruses naturally circulate in wild aquatic birds but are easily transmitted to poultry. Occasionally, they can infect humans who come into close contact with infected birds, for instance at wild poultry markets or commercial farms. One hypothesis is the transmission to an infected wild bird to the captive group of emperor tamarin (Saguinus imperator) but the curious fact is that only emperor tamarins (Saguinus imperator) are positive to H5N3 and show no clinical signs except one who died. One hypothesis is that pygmeae marmosets (Cebuella pygmaea 3.0) are more resistant than emperor tamarins (Saguinus imperator) against H5N3 subtype.
Secondly, a transmission of the subtypes H5N3 by humans is possible.. Indeed, callitrichids that are kept in captivity run an even greater risk of anthroponotic infections with pathogens from personnel working in primate-keeping institutes and, in case of zoos, from visitors. Viruses that can be transmitted via aerosolized droplets particularly pose a risk, as they do not rely on direct contact between individuals, and can travel considerable distances by air21. Moreover, some keepers take care of both callitrichids and wild birds of the rescue center in the zoo. Despite the presence of biosecurity’s measure, the possibility of a direct or indirect transmission with a prolonged contact with callitrichids is then possible.
In addition to NHPs, the main animal models involved in pre-clinical vaccine research are mice and ferrets, but other models such as the guinea pig, cotton rat, Syrian hamster and swine exist. However, these models are uncommon and reagents for many downstream analyses are limited22. Taking that into account, sera from another species which lived in the same enclosure (Dasyprocta azarae 1.2 and Chelonoidis carbonaria 0.0.2) were gathered in order to use ELISA technique to detect if the species have some Anti-Influenza A antibodies. Besides, a sera analysis from species that were in the same building than the group of emperor tamarin in their previous institution (one Leontopithecus rosalia, one Callithrix geoffroyi and two Callithrix jacchus) showed no Anti-Influenza A antibodies. Furthermore, all the birds of the collection are vaccinated against H5N2 and no clinical signs were observed.
In summary, a H5N3 infection was reported in a captive group of emperor tamarin (Saguinus imperator). Currently, all the three female emperor tamarin alive remain asymptomatic. An epidemiological survey is in progress to determine how the infection occurred. This condition has, to the best of our knowledge, not been reported in the literature.