Shedding Light on Avian Influenza H4N6 Infection in Mallards: Modes of Transmission and Implications for Surveillance

VanDalen, Kaci K.; Franklin, Alan B.; Mooers, Nicole L.; Sullivan, Heather J.; Shriner, Susan A.

doi:10.1371/journal.pone.0012851

Cited by 61 publications

(81 citation statements)

References 35 publications

(43 reference statements)

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“…LPAIV infections followed by exposure to a different (i.e., heterologous) LPAIV HA subtype have been shown to induce no protection in chickens (7) and weak protection in Pekin ducks (7), mallards (8,9), and quails (10). Susceptibility of birds to LPAIV infection is suggested to vary by age, with, in most cases, decreased virus replication with increasing age, but this has been investigated mainly in very young birds (11,12). In naturally and experimentally infected mallards, avian influenza virus (AIV)-specific serum antibodies have been detected for a long period of time after infection (13,14), but little is known about their protective effect.…”

mentioning

confidence: 99%

Long-Term Effect of Serial Infections with H13 and H16 Low-Pathogenic Avian Influenza Viruses in Black-Headed Gulls

Verhagen

Höfle

Amerongen

et al. 2015

J Virol

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Infections of domestic and wild birds with low-pathogenic avian influenza viruses (LPAIVs) have been associated with protective immunity to subsequent infection. However, the degree and duration of immunity in wild birds from previous LPAIV infection, by the same or a different subtype, are poorly understood. Therefore, we inoculated H13N2 (A/black-headed gull/Netherlands/7/ 2009) and H16N3 (A/black-headed gull/Netherlands/26/2009) LPAIVs into black-headed gulls (Chroicocephalus ridibundus), their natural host species, and measured the long-term immune response and protection against one or two reinfections over a period of >1 year. This is the typical interval between LPAIV epizootics in wild birds. Reinfection with the same virus resulted in progressively less virus excretion, with complete abrogation of virus excretion after two infections for H13 but not H16. However, reinfection with the other virus affected neither the level nor duration of virus excretion. Virus excretion by immunologically naive birds did not differ in total levels of excreted H13 or H16 virus between first-and second-year birds, but the duration of H13 excretion was shorter for second-year birds. Furthermore, serum antibody levels did not correlate with protection against LPAIV infection. LPAIV-infected gulls showed no clinical signs of disease. These results imply that the epidemiological cycles of H13 and H16 in black-headed gulls are relatively independent from each other and depend mainly on infection of firstyear birds. IMPORTANCELow-pathogenic avian influenza viruses (LPAIVs) circulate mainly in wild water birds but are occasionally transmitted to other species, including humans, where they cause subclinical to fatal disease. To date, the effect of LPAIV-specific immunity on the epidemiology of LPAIV in wild birds is poorly understood. In this study, we investigated the effect of H13 and H16 LPAIV infection in black-headed gulls on susceptibility and virus excretion of subsequent infection with the same or the other virus within the same breeding season and between breeding seasons. These are the only two LPAIV hemagglutinin subtypes predominating in this species. The findings suggest that H13 and H16 LPAIV cycles in black-headed gull populations are independent of each other, indicate the importance of first-year birds in LPAIV epidemiology, and emphasize the need for alternatives to avian influenza virus (AIV)-specific serum antibodies as evidence of past LPAIV infection and correlates of protection against LPAIV infection in wild birds.

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confidence: 99%

Long-Term Effect of Serial Infections with H13 and H16 Low-Pathogenic Avian Influenza Viruses in Black-Headed Gulls

Verhagen

Höfle

Amerongen

et al. 2015

J Virol

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“…We hypothesize that the lack of contact transmission among cohoused ducks is due to the lack of large shared water resources conducive of oral-fecal transmission. For example, others have shown successful transmission among mallards in contact with a water source previously contaminated by experimentally infected mallards [18] and water-associated transmission has also been postulated for mammals [12]. Overall, the index mallards in the highdensity stack appear to have shed virus for insufficient time and in insufficient quantities to elicit transmission within this stacked cage setting.…”

Section: Discussionmentioning

confidence: 97%

“…Thus, the inoculated mallards did not shed sufficient virus to infect their cage mates or the birds in adjacent or lower cages (Figure 2). Viral transmission in the high-density stack may have had a different outcome if shedding by other routes was more prevalent, as AIV shed via the fecal route by mallards can be rapidly transmitted among conspecifics when a shared water source, sufficient in size for fecal-oral transmission, is present [18]. Only small water sources were available in these pens, which precluded their use for bathing and swimming.…”

Section: Discussionmentioning

confidence: 99%

Transmission of H6N2 wild bird-origin influenza A virus among multiple bird species in a stacked-cage setting

et al. 2017

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Live bird markets are common in certain regions of the U.S. and in other regions of the world. We experimentally tested the ability of a wild bird influenza A virus to transmit from index animals to naïve animals at varying animal densities in stacked cages in a simulated live bird market. Two and six mallards, five and twelve quail, and six and nine pheasants were used in the low-density and high-density stacks of cages, respectively. Transmission did not occur in the high-density stack of cages likely due to the short duration and relatively low levels of shedding, a dominance of oral shedding, and the lack of transmission to other mallards in the index cage. In the low-density stack of cages, transmission occurred among all species tested, but not among all birds present. Oral and cloacal shedding was detected in waterfowl but only oral shedding was identified in the gallinaceous birds tested. Overall, transmission was patchy among the stacked cages, thereby suggesting that chance was involved in the deposition of shed virus in key locations (e.g., food or water bowls), which facilitated transmission to some birds.

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“…Exposure and depuration: The two exposure beakers were inoculated with 2 mL of diluted AI virus stock (10 6 EID 50 /mL) such that the beaker water had a final virus concentration of approximately 10 3 EID 50 /mL (based on AI viral concentrations found in water of experimentally infected Mallards; VanDalen et al, 2010) and the control beaker was inoculated with 2 mL of BA-1 to serve as a negative control. The water in all three beakers was thoroughly stirred to create a homogeneous mixture.…”

Section: Snail Experimentsmentioning

confidence: 99%

“…In addition, AI viruses have an affinity for suspended solids in the aquatic environment, and viruses that bind to these solids can remain viable longer and may accumulate in the sediment (Bitton, 1980). This environmental persistence of AI viruses in water allows transmission among waterfowl without direct contact (VanDalen et al, 2010;Lebarbenchon et al, 2011), but it also exposes other animals that share the aquatic environment to AI viruses.…”

Section: Introductionmentioning

confidence: 99%

Failure of Transmission of Low-Pathogenic Avian Influenza Virus Between Mallards and Freshwater Snails: An Experimental Evaluation

Oesterle

Huyvaert

Orahood

et al. 2013

Journal of Wildlife Diseases

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ABSTRACT:In aquatic bird populations, the ability of avian influenza (AI) viruses to remain infectious in water for extended periods provides a mechanism that allows viral transmission to occur long after shedding birds have left the area. However, this also exposes other aquatic organisms, including freshwater invertebrates, to AI viruses. Previous researchers found that AI viral RNA can be sequestered in snail tissues. Using an experimental approach, we determined whether freshwater snails (Physa acuta and Physa gyrina) can infect waterfowl with AI viruses by serving as a means of transmission between infected and naïve waterfowl via ingestion. In our first experiment, we exposed 20 Physa spp. snails to an AI virus (H3N8) and inoculated embryonated specific pathogen-free (SPF) chicken eggs with the homogenized snail tissues. Sequestered AI viruses remain infectious in snail tissues; 10% of the exposed snail tissues infected SPF eggs. In a second experiment, we exposed snails to water contaminated with feces of AI virus-inoculated Mallards (Anas platyrhynchos) to evaluate whether ingestion of exposed freshwater snails was an alternate route of AI virus transmission to waterfowl. None of the immunologically naïve Mallards developed an infection, indicating that transmission via ingestion likely did not occur. Our results suggest that this particular trophic interaction may not play an important role in the transmission of AI viruses in aquatic habitats.

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Shedding Light on Avian Influenza H4N6 Infection in Mallards: Modes of Transmission and Implications for Surveillance

Cited by 61 publications

References 35 publications

Long-Term Effect of Serial Infections with H13 and H16 Low-Pathogenic Avian Influenza Viruses in Black-Headed Gulls

Long-Term Effect of Serial Infections with H13 and H16 Low-Pathogenic Avian Influenza Viruses in Black-Headed Gulls

Transmission of H6N2 wild bird-origin influenza A virus among multiple bird species in a stacked-cage setting

Failure of Transmission of Low-Pathogenic Avian Influenza Virus Between Mallards and Freshwater Snails: An Experimental Evaluation

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