Effect of a Prior Exposure to a Low Pathogenic Avian Influenza Virus in the Outcome of a Heterosubtypic Low Pathogenic Avian Influenza Infection in Mallards (Anas platyrhynchos)

Costa, Teresa; Brown, Justin D.; Howerth, Elizabeth W.; Stallknecht, David E.

doi:10.1637/9480-072210-reg.1

Cited by 37 publications

(46 citation statements)

References 23 publications

(12 reference statements)

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“…In those studies, the time interval between the first and second inoculations was relatively short, ranging from 21 to 84 days. In contrast to our findings in BHGU, LPAIV infection induced partial (H5N3 followed by H7N2 and H3N8 followed by H5N2 and vice versa, respectively) (7, 9) to nearly complete (8) protection against subsequent infection with a heterologous virus in Pekin ducks (7) and mallards (8,9). The following differences in study design may play a role in this discrepancy.…”

Section: Discussioncontrasting

confidence: 99%

“…The following differences in study design may play a role in this discrepancy. Compared to our study, the LPAIV subtypes used in those studies were different (H5N3 and H7N2 [7], H7N7 and H5N2 [8], and H3N8 and H5N2 [9]); the time interval between the first and second inoculations, 14 (8) or 21 days (7, 9), was shorter; the inoculum dose, 4 ϫ 10 6 PFU (7) or 10 8.7 EID 50 (8), was higher; and there were two prior infections with a heterologous virus (8) rather than one. In free-living mallards, heterosubtypic LPAIV immunity has been described for different HA subtypes belonging to the same phylogenetic clade (19).…”

Section: Discussioncontrasting

confidence: 80%

“…For instance, LPAIV infections followed by exposure to the same (i.e., homologous) LPAIV HA subtype have been shown to induce strong protection in chickens (7) and mallards (Anas platyrhynchos) (8) but weak protection in Pekin ducks (7). 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).…”

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confidence: 99%

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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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Section: Discussioncontrasting

confidence: 99%

Section: Discussioncontrasting

confidence: 80%

mentioning

confidence: 99%

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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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“…B 281: 20140098 strain (homosubtypic immunity) [40,41]. In addition, the development of partial protection against other strains, defined as heterosubtypic or cross-protective immunity, may also occur [40,[42][43][44][45]. This seems to be true for sentinel mallards in nature [46].…”

Section: (B) What Is Governing the Seasonal Trends In Influenzamentioning

confidence: 99%

Long-term variation in influenza A virus prevalence and subtype diversity in migratory mallards in northern Europe

et al. 2014

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Data on long-term circulation of pathogens in wildlife populations are seldom collected, and hence understanding of spatial-temporal variation in prevalence and genotypes is limited. Here, we analysed a long-term surveillance series on influenza A virus (IAV) in mallards collected at an important migratory stopover site from 2002 to 2010, and characterized seasonal dynamics in virus prevalence and subtype diversity. Prevalence dynamics were influenced by year, but retained a common pattern for all years whereby prevalence was low in spring and summer, but increased in early autumn with a first peak in August, and a second more pronounced peak during October-November. A total of 74 haemagglutinin (HA)/neuraminidase (NA) combinations were isolated, including all NA and most HA (H1-H12) subtypes. The most common subtype combinations were H4N6, H1N1, H2N3, H5N2, H6N2 and H11N9, and showed a clear linkage between specific HA and NA subtypes. Furthermore, there was a temporal structuring of subtypes within seasons based on HA phylogenetic relatedness. Dissimilar HA subtypes tended to have different temporal occurrence within seasons, where the subtypes that dominated in early autumn were rare in late autumn, and vice versa. This suggests that build-up of herd immunity affected IAV dynamics in this system.

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“…In mallard and geese, previous exposure to homo-or heterosubtypic LPAI reduces the duration and concentration of virus shedding in consecutive infections (6,25). A negative trend in virus shedding duration in infected birds has been observed in migrating mallards during the progression of autumn (29).…”

Section: Discussionmentioning

confidence: 99%

Impact of Age, Season, and Flowingvs. Stagnant Water Habitat on Avian Influenza Prevalence in Mute Swan (Cygnus olor) in Belgium

et al. 2016

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Due to their probable role in the spread of Asian highly pathogenic avian influenza (HPAI) H5N1 virus, and in order to explore its implication in the low pathogenic avian influenza (LPAI) virus epidemiology, mute swans represent one particular wild bird species specifically targeted in the avian influenza (AI) surveillance elaborated in Belgium. A total of 640 individual mute swans have been sampled during a 4-yr AI surveillance program (2007-2010) to determine the AI seroprevalence and viroprevalence in this species; all were analyzed through age, temporal, and habitat (flowing and stagnant water) factors. Using a nucleoprotein (NP)-based ELISA, a global antibody prevalence of 35% has been found and was characterized by two peaks in the winter and the summer that might be indicative of a greater LPAI virus circulation in the autumn than in the spring. A significantly higher antibody prevalence was detected in adult swans (53.8%) as compared to juveniles (15.5%). In contrast, a low prevalence of infection (2.7%) was found, mainly in juvenile mute swans and only during the autumn migration period. Interestingly, an impact of water habitat was observed based on the comparison of the antibody prevalence and prevalence of infection from swan populations living on stagnant water vs. flowing water, suggesting that stagnant water provides a more-favorable environment for LPAI persistence and transmission.

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Effect of a Prior Exposure to a Low Pathogenic Avian Influenza Virus in the Outcome of a Heterosubtypic Low Pathogenic Avian Influenza Infection in Mallards (Anas platyrhynchos)

Cited by 37 publications

References 23 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

Long-term variation in influenza A virus prevalence and subtype diversity in migratory mallards in northern Europe

Impact of Age, Season, and Flowingvs. Stagnant Water Habitat on Avian Influenza Prevalence in Mute Swan (Cygnus olor) in Belgium

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