Tissue tropism and pathology of natural influenza virus infection in black-headed gulls (<i>Chroicocephalus ridibundus</i>)

Höfle, Úrsula; Bildt, Marco W. G. van de; Leijten, Lonneke; Amerongen, Geert van; Verhagen, Josanne H.; Fouchier, Ron A. M.; Osterhaus, Albert D. M. E.; Kuiken, Thijs

doi:10.1080/03079457.2012.744447

Cited by 31 publications

(27 citation statements)

References 24 publications

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“…This suggests that, overall, H13 and H16 virus infections are nonpathogenic for BHGU. Previous studies found no clinical signs ( 8 ) or histological lesions ( 9 ) in gulls naturally infected with H13 or H16 virus. No notable differences in virus prevalence were found related to gender, no consistent differences in virus prevalence were found related to capture method, and no AIVs in dead BHGU were detected outside epidemics (Technical Appendix).…”

Section: The Studymentioning

confidence: 79%

Epidemiology of Influenza A Virus among Black-headed Gulls, the Netherlands, 2006–2010

Verhagen¹,

Majoor²,

Lexmond³

et al. 2014

Emerg. Infect. Dis.

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Section: The Studymentioning

confidence: 79%

Epidemiology of Influenza A Virus among Black-headed Gulls, the Netherlands, 2006–2010

Verhagen¹,

Majoor²,

Lexmond³

et al. 2014

Emerg. Infect. Dis.

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“…Mucosal rather than serum antibodies may be a better correlate of protection, as LPAIV in BHGU (15) and mallards (23) infects the digestive tract. Although already suggested in 1980 by Kida and colleagues (18), mucosal antibodies against virus infections in birds have received little attention, perhaps because of technical difficulties in measurements.…”

Section: Discussionmentioning

confidence: 99%

“…Each group followed a different schedule of three intraesophageal inoculations (Table 1). This route of inoculation was chosen because virus replication was limited to the intestinal tract of BHGU naturally infected with LPAIVs H13 and H16 (15). The inoculum was egg allantoic fluid containing either 10 6 median egg infectious doses (EID 50 ) of LPAIV H13 or H16 (virus-inoculated birds) or no virus (sham-inoculated birds), diluted with phosphate-buffered saline (PBS) to a volume of 1.5 ml.…”

Section: Experimental Designmentioning

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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“…Predominantly birds from wetlands and aquatic environments (orders Anseriformes and Charadriiformes ) are infected with LPAIV [7], causing transient and mainly intestinal infections [8], [9], with no or limited signs of disease [10]. LPAIV can be classified in subtypes based on antigenic and genetic variation of the viral surface glycoproteins hemagglutinin (HA) and neuraminidase (NA).…”

Section: Introductionmentioning

confidence: 99%

Migratory Birds Reinforce Local Circulation of Avian Influenza Viruses

et al. 2014

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Migratory and resident hosts have been hypothesized to fulfil distinct roles in infectious disease dynamics. However, the contribution of resident and migratory hosts to wildlife infectious disease epidemiology, including that of low pathogenic avian influenza virus (LPAIV) in wild birds, has largely remained unstudied. During an autumn H3 LPAIV epizootic in free-living mallards (Anas platyrhynchos) — a partially migratory species — we identified resident and migratory host populations using stable hydrogen isotope analysis of flight feathers. We investigated the role of migratory and resident hosts separately in the introduction and maintenance of H3 LPAIV during the epizootic. To test this we analysed (i) H3 virus kinship, (ii) temporal patterns in H3 virus prevalence and shedding and (iii) H3-specific antibody prevalence in relation to host migratory strategy. We demonstrate that the H3 LPAIV strain causing the epizootic most likely originated from a single introduction, followed by local clonal expansion. The H3 LPAIV strain was genetically unrelated to H3 LPAIV detected both before and after the epizootic at the study site. During the LPAIV epizootic, migratory mallards were more often infected with H3 LPAIV than residents. Low titres of H3-specific antibodies were detected in only a few residents and migrants. Our results suggest that in this LPAIV epizootic, a single H3 virus was present in resident mallards prior to arrival of migratory mallards followed by a period of virus amplification, importantly associated with the influx of migratory mallards. Thus migrants are suggested to act as local amplifiers rather than the often suggested role as vectors importing novel strains from afar. Our study exemplifies that a multifaceted interdisciplinary approach offers promising opportunities to elucidate the role of migratory and resident hosts in infectious disease dynamics in wildlife.

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Tissue tropism and pathology of natural influenza virus infection in black-headed gulls (Chroicocephalus ridibundus)

Cited by 31 publications

References 24 publications

Epidemiology of Influenza A Virus among Black-headed Gulls, the Netherlands, 2006–2010

Epidemiology of Influenza A Virus among Black-headed Gulls, the Netherlands, 2006–2010

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

Migratory Birds Reinforce Local Circulation of Avian Influenza Viruses

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