Avian influenza A virus susceptibility, infection, transmission, and antibody kinetics in European starlings

Abstract

Avian influenza A viruses (IAVs) pose risks to public, agricultural, and wildlife health. Bridge hosts are spillover hosts that share habitat with both maintenance hosts (e.g., mallards) and target hosts (e.g., poultry). We conducted a comprehensive assessment of European starlings (Sturnus vulgaris), a common visitor to both urban and agricultural environments, to assess whether this species might act as a potential maintenance or bridge host for IAVs. First, we experimentally inoculated starlings with a wild bird IAV to investigate susceptibility and replication kinetics. Next, we evaluated whether IAV might spill over to starlings from sharing resources with a widespread IAV reservoir host. We accomplished this using a specially designed transmission cage to simulate natural environmental transmission by exposing starlings to water shared with IAV-infected mallards (Anas platyrhynchos). We then conducted a contact study to assess intraspecies transmission between starlings. In the initial experimental infection study, all inoculated starlings shed viral RNA and seroconverted. All starlings in the transmission study became infected and shed RNA at similar levels. All but one of these birds seroconverted, but detectable antibodies were relatively transient, falling to negative levels in a majority of birds by 59 days post contact. None of the contact starlings in the intraspecies transmission experiment became infected. In summary, we demonstrated that starlings may have the potential to act as IAV bridge hosts if they share water with IAV-infected waterfowl. However, starlings are unlikely to act as maintenance hosts due to limited, if any, intraspecies transmission. In addition, starlings have a relatively brief antibody response which should be considered when interpreting serology from field samples. Further study is needed to evaluate the potential for transmission from starlings to poultry, a possibility enhanced by starling’s behavioral trait of forming very large flocks which can descend on poultry facilities when natural resources are scarce.

Development of a Rapid Fluorescent Diagnostic System for Early Detection of the Highly Pathogenic Avian Influenza H5 Clade 2.3.4.4 Viruses in Chicken Stool

“…However, a positive signal was not detected in the three cloacal samples collected from the same H5N6-infected group. This result corroborated the lower viral load of cloacal samples compared to fecal samples reported for AIVs [ 53 , 54 ], as this trend was observed for the H5N6 and H9N2 viruses included in the present study. We also observed more mucus in cloacal than in fecal samples, and thus our system should be further optimized to detect viruses in cloacal samples.…”

Strength in numbers: Avian influenza A virus transmission to poultry from a flocking passerine

“…In this study, we assessed the general premise that the risk of IAV transmission to poultry may be associated with flock size was evaluated for European starlings. A recent publication indicated that indirect transmission of IAV to starlings from water contaminated by IAV‐infected mallards is possible if not highly probable (Ellis et al., 2021). If large numbers of starlings become infected by drinking from and bathing in a small waterbody previously contaminated with virus by waterfowl, these same starlings could, in turn, travel to one or more livestock facilities where they could then environmentally transmit an IAV by depositing virus within feeders or waterers in facilities that do not exclude them.…”

“…We believe that the shared water sources in our animal rooms were likely the key vehicle from which quail were exposed to IAV in the current study. Notably, a recent study provided evidence that starlings become infected with IAVs following their exposure to relatively small water bodies used by IAV‐infected mallards ( Anas platyrhynchos ) (Ellis et al., 2021).…”

“…Interspecific transmission in the experimental system described herein likely occurred via oral secretions from starlings. Previous studies that evaluated oral and cloacal swabs in European starlings following LP IAV challenge indicated that a very small percentage of individuals shed via the cloacal route, and when cloacal shedding did occur, it was at very low quantities (Ellis et al., 2021; Nemeth et al., 2010). However, a different study reported higher levels of shedding by the cloacal as compared to the tracheal routes (Qin et al., 2011).…”

“…Following a ≥ 2‐week quarantine/acclimation period, starlings were assigned to one of three flock size treatments ( n = 10, n = 20 and n = 30) and moved to one of three independent BSL‐2 animal rooms. Because we have successfully inoculated European starlings and Bobwhite quail with H4N6 previously, no control animals were used (Ellis et al., 2021; Pepin et al., 2012). Animal methods were approved by the USDA NWRC institutional animal care and use committee.…”