Juveniles and migrants as drivers for seasonal epizootics of avian influenza virus

Abstract

Similar to other infectious diseases, the prevalence of low pathogenic avian influenza viruses (LPAIV) has been seen to exhibit marked seasonal variation. However, mechanisms driving this variation in wild birds have yet to be tested. We investigated the validity of three previously suggested drivers for the seasonal dynamics in LPAIV infections in wild birds: (i) host density, (ii) immunologically naïve young and (iii) increased susceptibility in migrants. To address these questions, we sampled a key LPAIV host species, the mallard Anas platyrhynchos, on a small spatial scale, comprehensively throughout a complete annual cycle, measuring both current and past infection (i.e. viral and seroprevalence, respectively). We demonstrate a minor peak in LPAIV prevalence in summer, a dominant peak in autumn, during which half of the sampled population was infected, and no infections in spring. Seroprevalence of antibodies to a conserved gene segment of avian influenza virus (AIV) peaked in winter and again in spring. The summer peak of LPAIV prevalence coincided with the entrance of unfledged naïve young in the population. Moreover, juveniles were more likely to be infected, shed higher quantities of virus and were less likely to have detectable antibodies to AIV than adult birds. The arrival of migratory birds, as identified by stable hydrogen isotope analysis, appeared to drive the autumn peak in LPAIV infection, with both temporal coincidence and higher infection prevalence in migrants. Remarkably, seroprevalence in migrants was substantially lower than viral prevalence throughout autumn migration, further indicating that each wave of migrants amplified local AIV circulation. Finally, while host abundance increased throughout autumn, it peaked in winter, showing no direct correspondence with either of the LPAIV infection peaks. At an epidemiologically relevant spatial scale, we provide strong evidence for the role of migratory birds as key drivers for seasonal epizootics of LPAIV, regardless of their role as vectors of these viruses. This study exemplifies the importance of understanding host demography and migratory behaviour when examining seasonal drivers of infection in wildlife populations.

Keywords: CT-value; age; infection intensity; infectious disease; nucleoprotein; origin; subtype; viral prevalence.

Fig. 1

Monthly prevalence (± 95% CI) of LPAIV infection and population numbers of mallards, from March 2010 until February 2011. (a) Viral prevalence (i.e. current infection), (b) number of unfledged juveniles of the resident population, (c) number of local and distant migrants, and (d) mallard counts in the Alblasserwaard (left y-axis) and across the Netherlands (right y-axis). The dotted line of the x-axis means that there is no data available.

Fig. 2

Monthly prevalence (± 95% CI) of AIV antibodies (i.e. past infection) in mallards from March 2010 until February 2011.

Fig. 3

Seasonal prevalence (± 95% CI) of LPAIV infection in juvenile (<1 year) and adult (>1 year) mallards. (a) Viral prevalence, and (b) seroprevalence.

Fig. 4

Degree of viral shedding (i.e. C_T-value) (mean ± SE) of LPAIV positive juvenile (<1 year) and adult (>1 year) mallards detected in (a) cloacal, and (b) oropharyngeal samples. The C_T-value is inversely proportional to the number of virus particles in a sample, with lower C_T-values indicating large quantities of virus.

Fig. 5

Prevalence (± 95% CI) of LPAIV infection in mallards for residents, local migrants and distant migrants from August until December. (a) Viral prevalence, and (b) seroprevalence.