Impact of body condition on influenza A virus infection dynamics in mallards following a secondary exposure

Dannemiller, Nicholas G.; Webb, Colleen T.; Wilson, Kenneth; Bentler, Kevin T.; Mooers, Nicole L.; Ellis, Jeremy W.; Root, J. Jeffrey; Franklin, Alan B.; Shriner, Susan A.

doi:10.1371/journal.pone.0175757

Cited by 9 publications

(11 citation statements)

References 41 publications

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“…The timing of the lysis peak in our study might be associated with virus excretion (and potentially with host susceptibility), as all birds were excreting virus at day 3 and day 7 postprimary exposure. Lower haptoglobin concentrations after LPAIV exposure in primary-exposed laboratory mallards is in accordance to Dannemiller et al (2017), who also reported lower haptoglobin concentrations after LPAIV H4N6 inoculation in comparison to baseline concentrations in wild-type domestic mallards. However, it should be noted that these birds had been naturally exposed to LPAIV H9 prior to the onset of their study (Dannemiller et al, 2017).…”

Section: Discussionsupporting

confidence: 87%

“…Lower haptoglobin concentrations after LPAIV exposure in primary-exposed laboratory mallards is in accordance to Dannemiller et al (2017), who also reported lower haptoglobin concentrations after LPAIV H4N6 inoculation in comparison to baseline concentrations in wild-type domestic mallards. However, it should be noted that these birds had been naturally exposed to LPAIV H9 prior to the onset of their study (Dannemiller et al, 2017). A decrease in haptoglobin concentrations after an immune challenge is also reported in other avian species (Mazur-Gonkowska et al, 2004;Troisi et al, 2007;Hegemann et al, 2013), as well as a fish species (Vinterstare et al, 2019).…”

Section: Discussionsupporting

confidence: 87%

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

et al. 2020

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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.

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Section: Discussionsupporting

confidence: 87%

Section: Discussionsupporting

confidence: 87%

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

et al. 2020

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“…In ducks, influenza infection typically occurs in the intestine, and seroconversion does not always occur [47]. However, ducks can respond to influenza vaccines [50], and show some evidence of protection from re-infection by the same strain [5,6] and some hetero-subtypic protection [291,292,293]. Duck antibody responses appear to prevent re-infection with the same strain, and this may drive the diversity of influenza viral subtypes in the wild [294].…”

Section: Other Potential Mechanisms Of Influenza Disease Resistanmentioning

confidence: 99%

Innate Immune Responses to Avian Influenza Viruses in Ducks and Chickens

Evseev

Magor

2019

Veterinary Sciences

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Mallard ducks are important natural hosts of low pathogenic avian influenza (LPAI) viruses and many strains circulate in this reservoir and cause little harm. Some strains can be transmitted to other hosts, including chickens, and cause respiratory and systemic disease. Rarely, these highly pathogenic avian influenza (HPAI) viruses cause disease in mallards, while chickens are highly susceptible. The long co-evolution of mallard ducks with influenza viruses has undoubtedly fine-tuned many immunological host–pathogen interactions to confer resistance to disease, which are poorly understood. Here, we compare innate responses to different avian influenza viruses in ducks and chickens to reveal differences that point to potential mechanisms of disease resistance. Mallard ducks are permissive to LPAI replication in their intestinal tissues without overtly compromising their fitness. In contrast, the mallard response to HPAI infection reflects an immediate and robust induction of type I interferon and antiviral interferon stimulated genes, highlighting the importance of the RIG-I pathway. Ducks also appear to limit the duration of the response, particularly of pro-inflammatory cytokine expression. Chickens lack RIG-I, and some modulators of the signaling pathway and may be compromised in initiating an early interferon response, allowing more viral replication and consequent damage. We review current knowledge about innate response mediators to influenza infection in mallard ducks compared to chickens to gain insight into protective immune responses, and open questions for future research.

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“…AIV prevalence is higher in young birds (Farnsworth et al 2012, Papp et al 2017) and usually higher males, but not always (Wallensten et al 2007). Young, immunologically naı ¨ve birds shed a higher amount of virus due to both age-specific susceptibility (Costa et al 2010) and the lack of humoral immunity (Jourdain et al 2010, Dannemiller et al 2017) such that differences in the spatial and temporal distribution of demographic classes may impact the distribution of AIV. Second, at the local scale, fecal/oral transmission among birds aggregated in one location and transmission from environmental reservoirs over longer timescales (VanDalen et al 2010) influences infection dynamics (Breban et al 2009, Fuller et al 2010, Farnsworth et al 2012, Belkhiria et al 2016, Papp et al 2017.…”

Section: Introductionmentioning

confidence: 99%

Continental‐scale dynamics of avian influenza in U.S. waterfowl are driven by demography, migration, and temperature

Gorsich

Webb

Merton

et al. 2020

Ecological Applications

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Emerging diseases of wildlife origin are increasingly spilling over into humans and domestic animals. Surveillance and risk assessments for transmission between these populations are informed by a mechanistic understanding of the pathogens in wildlife reservoirs. For avian influenza viruses (AIV), much observational and experimental work in wildlife has been conducted at local scales, yet fully understanding their spread and distribution requires assessing the mechanisms acting at both local, (e.g., intrinsic epidemic dynamics), and continental scales, (e.g., long‐distance migration). Here, we combined a large, continental‐scale data set on low pathogenic, Type A AIV in the United States with a novel network‐based application of bird banding/recovery data to investigate the migration‐based drivers of AIV and their relative importance compared to well‐characterized local drivers (e.g., demography, environmental persistence). We compared among regression models reflecting hypothesized ecological processes and evaluated their ability to predict AIV in space and time using within and out‐of‐sample validation. We found that predictors of AIV were associated with multiple mechanisms at local and continental scales. Hypotheses characterizing local epidemic dynamics were strongly supported, with age, the age‐specific aggregation of migratory birds in an area and temperature being the best predictors of infection. Hypotheses defining larger, network‐based features of the migration processes, such as clustering or between‐cluster mixing explained less variation but were also supported. Therefore, our results support a role for local processes in driving the continental distribution of AIV.

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Impact of body condition on influenza A virus infection dynamics in mallards following a secondary exposure

Cited by 9 publications

References 41 publications

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

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

Innate Immune Responses to Avian Influenza Viruses in Ducks and Chickens

Continental‐scale dynamics of avian influenza in U.S. waterfowl are driven by demography, migration, and temperature

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