A Comparative Study of the Innate Humoral Immune Response to Avian Influenza Virus in Wild and Domestic Mallards

Abstract

Domestic mallards (Anas platyrhynchos domesticus) are traditionally used as a model to investigate infection dynamics and immune responses to low pathogenic avian influenza viruses (LPAIVs) in free-living mallards. However, it is unclear whether the immune response of domestic birds reflects the response of their free-living counterparts naturally exposed to these viruses. We investigated the extent to which the innate humoral immune response was similar among (i) wild-type domestic mallards in primary and secondary infection with LPAIV H4N6 in a laboratory setting (laboratory mallards), (ii) wild-type domestic mallards naturally exposed to LPAIVs in a semi-natural setting (sentinel mallards), and (iii) free-living mallards naturally exposed to LPAIVs. We quantified innate humoral immune function by measuring non-specific natural antibodies (agglutination), complement activity (lysis), and the acute phase protein haptoglobin. We demonstrate that complement activity in the first 3 days after LPAIV exposure was higher in primary-exposed laboratory mallards than in sentinel and free-living mallards. LPAIV H4N6 likely activated the complement system and the acute phase response in primary-exposed laboratory mallards, as lysis was higher and haptoglobin lower at day 3 and 7 post-exposure compared to baseline immune function measured prior to exposure. There were no differences observed in natural antibody and haptoglobin concentrations among laboratory, sentinel, and free-living mallards in the first 3 days after LPAIV exposure. Our study demonstrates that, based on the three innate humoral immune parameters measured, domestic mallards seem an appropriate model to investigate innate immunology of their free-living counterparts, albeit the innate immune response of secondary-LPAIV exposed mallards is a better proxy for the innate immune response in pre-exposed free-living mallards than that of immunologically naïve mallards.

Avian influenza antibody prevalence increases with mercury contamination in wild waterfowl

“…Sera samples were tested for the presence of influenza A antibodies using commercially available blocking enzyme-linked immunoassay (ELISA; AI MultiS-Screen Avian Influenza Virus Antibody Test Kit; IDEXX Laboratories, Westbrook, Maine, USA). We considered samples with a signal-to-noise ratio less than 0.5 to be positive for the presence of influenza antibodies [45,67].…”

“…lymphocyte production [38,42,43], antibody titres [10]). Both innate and adaptive immunity influence the probability and severity of influenza infection [44,45], so mercury contamination could affect the prevalence of influenza infection and its impacts waterfowl populations.…”

Birds and human health: Pathways for a positive relationship and improved integration

“…2003, Van Dijk et al . 2020) to further understand and predict emerging infectious diseases could contribute significantly to disease mitigation (Neo & Tan 2017). Bird species including Common Chiffchaffs Phylloscopus collybita , Atlantic Canaries Serinus canaria , Zebra Finches Taeniopygia guttata , Budgerigars Melopsittacus undulatus and European Goldfinches Carduelis carduelis have been used to further understand avian malaria (Valkiūnas et al .…”

Waterfowl recently infected with low pathogenic avian influenza exhibit reduced local movement and delayed migration

“…Sera samples were tested for the presence of influenza A antibodies using commercially available blocking enzyme-linked immunoassay (bELISA; AI MultiS-Screen Avian Influenza Virus Antibody Test Kit; IDEXX Laboratories, Westbrook, ME) and following the manufacturer's instructions. We considered samples with a signal-to-noise (S:N) ratio <0.5 to be positive for the presence of influenza antibodies, indicating prior infection (Brown et al, 2009;van Dijk et al, 2020); detectable antibodies to influenza generally last 6 months to 1.5 years (Fereidouni et al, 2010;Hoye et al, 2011;Shriner et al, 2021), but usually peak within 3 weeks of infection (Fereidouni et al, 2010;Shriner et al, 2021). All antibody detections were assumed to represent prior infection with LPAIVs, since HPAIVs were not known to be present in North America in the year preceding sampling; however, it was not possible to confirm the subtype or viral diversity that produced these prior infections.…”