Susceptibility and intra-species transmission of the H9N2 G1 prototype lineage virus in Japanese quail and turkeys

Bonfante, Francesco; Patrono, Livia Victoria; Aiello, Roberta; Beato, Maria Serena; Terregino, Calogero; Capua, Ilaria

doi:10.1016/j.vetmic.2013.03.014

Cited by 19 publications

(20 citation statements)

References 24 publications

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“…Quail are experimentally susceptible to many subtypes of both mammalian and avian influenza viruses (22)(23)(24) and have been proposed to be a bridging species or disease amplifiers between wild waterfowl and domestic gallinaceous poultry (25)(26)(27)(28)(29). In this study, we demonstrate that quail are susceptible to even a lowdose challenge of the Chinese H7N9 virus.…”

Section: Discussionmentioning

confidence: 56%

Role of Poultry in the Spread of Novel H7N9 Influenza Virus in China

Pantin‐Jackwood

Miller

Spackman

et al. 2014

J Virol

135

145

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The recent outbreak of H7N9 influenza in China has resulted in many human cases with a high fatality rate. Poultry are the likely source of infection for humans on the basis of sequence analysis and virus isolations from live bird markets, but it is not clear which species of birds are most likely to be infected and shedding levels of virus sufficient to infect humans. Intranasal inoculation of chickens, Japanese quail, pigeons, Pekin ducks, Mallard ducks, Muscovy ducks, and Embden geese with 10 6 50% egg infective doses of the A/Anhui/1/2013 virus resulted in infection but no clinical disease signs. Virus shedding was much higher and prolonged in quail and chickens than in the other species. Quail effectively transmitted the virus to direct contacts, but pigeons and Pekin ducks did not. In all species, virus was detected at much higher titers from oropharyngeal swabs than cloacal swabs. The hemagglutinin gene from samples collected from selected experimentally infected birds was sequenced, and three amino acid differences were commonly observed when the sequence was compared to the sequence of A/Anhui/1/2013: N123D, N149D, and L217Q. Leucine at position 217 is highly conserved for human isolates and is associated with ␣2,6-sialic acid binding. Different amino acid combinations were observed, suggesting that the inoculum had viral subpopulations that were selected after passage in birds. These experimental studies corroborate the finding that certain poultry species are reservoirs of the H7N9 influenza virus and that the virus is highly tropic for the upper respiratory tract, so testing of bird species should preferentially be conducted with oropharyngeal swabs for the best sensitivity. IMPORTANCEThe recent outbreak of H7N9 influenza in China has resulted in a number of human infections with a high case fatality rate. The source of the viral outbreak is suspected to be poultry, but definitive data on the source of the infection are not available. This study provides experimental data to show that quail and chickens are susceptible to infection, shed large amounts of virus, and are likely important in the spread of the virus to humans. Other poultry species can be infected and shed virus but are less likely to play a role of transmitting the virus to humans. Pigeons were previously suggested to be a possible source of the virus because of isolation of the virus from several pigeons in poultry markets in China, but experimental studies show that they are generally resistant to infection and are unlikely to play a role in the spread of the virus. O n 1 April 2013, the People's Republic of China reported the first 3 human cases of a novel H7N9 subtype of influenza A virus. Over the subsequent days, the number of confirmed cases ballooned to over 82, with over 17 fatalities occurring in 6 different provinces (1). Sequence analysis of the virus showed the H7 and N9 genes to be those of avian influenza viruses (AIVs) of Eurasian lineage, but at only 95% similarity to other isolates in the public sequence databa...

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Section: Discussionmentioning

confidence: 56%

Role of Poultry in the Spread of Novel H7N9 Influenza Virus in China

Pantin‐Jackwood

Miller

Spackman

et al. 2014

J Virol

135

145

View full text Add to dashboard Cite

show abstract

“…Some studies suggest that certain gallinaceous species, such as ring-necked pheasants and Japanese quail, are more susceptible than chickens and turkeys to LPAI viruses from free-living aquatic birds (22,(28)(29)(30)(31)(32)(33)(34). In addition, Japanese quail and European quail (Coturnix coturnix) may support the replication of almost all LPAI virus subtypes (33,35).…”

Section: Discussionmentioning

confidence: 99%

“…Epidemiological and experimental data suggest that, among the gallinaceous poultry, Japanese quail play a crucial role in the genesis of AI viruses because (i) AI viruses have been isolated from Japanese quail in commercial flocks and LPMs in North America, Europe, and Asia (27,(53)(54)(55)(56)(57); (ii) Japanese quail are experimentally susceptible to and support replication of HPAI viruses (22); (iii) most AI subtypes are able to replicate in Japanese quail, primarily in the respiratory tract (22); (iv) Japanese quail facilitate the adaptation of AI viruses of wild origin to major poultry species and mammals (28,40,41,(57)(58)(59)(60)(61)(62); (v) Japanese quail carry sialic acid receptors functional for binding of both avian (␣-2,3) and human (␣-2,6) influenza viruses (63); and (vi) Japanese quail are able to support efficient replication and transmission of reassortant viruses (34,37,38,64,65). Collectively, these findings support the tenet that Japanese quail are optimal hosts for the adaptation of wild bird AI viruses.…”

Section: Discussionmentioning

confidence: 99%

Pathobiology of Clade 2.3.4.4 H5Nx High-Pathogenicity Avian Influenza Virus Infections in Minor Gallinaceous Poultry Supports Early Backyard Flock Introductions in the Western United States in 2014-2015

Bertran

Lee

Pantin‐Jackwood

et al. 2017

J Virol

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In 2014 and 2015, the United States experienced an unprecedented outbreak of Eurasian clade 2.3.4.4 H5 highly pathogenic avian influenza (HPAI) virus. Initial cases affected mainly wild birds and mixed backyard poultry species, while later outbreaks affected mostly commercial chickens and turkeys. The pathogenesis, transmission, and intrahost evolutionary dynamics of initial Eurasian H5N8 and reassortant H5N2 clade 2.3.4.4 HPAI viruses in the United States were investigated in minor gallinaceous poultry species (i.e., species for which the U.S. commercial industries are small), namely, Japanese quail, bobwhite quail, pearl guinea fowl, chukar partridges, and ring-necked pheasants. Low mean bird infectious doses (<2 to 3.7 log10) support direct introduction and infection of these species as observed in mixed backyard poultry during the early outbreaks. Pathobiological features and systemic virus replication in all species tested were consistent with HPAI virus infection. Sustained virus shedding with transmission to contact-exposed birds, alongside long incubation periods, may enable unrecognized dissemination and adaptation to other gallinaceous species, such as chickens and turkeys. Genome sequencing of excreted viruses revealed numerous low-frequency polymorphisms and 20 consensus-level substitutions in all genes and species, but especially in Japanese quail and pearl guinea fowl and in internal proteins PB1 and PB2. This genomic flexibility after only one passage indicates that influenza viruses can continue to evolve in galliform species, increasing their opportunity to adapt to other species. Our findings suggest that these gallinaceous poultry are permissive for infection and sustainable transmissibility with the 2014 initial wild bird-adapted clade 2.3.4.4 virus, with potential acquisition of mutations leading to host range adaptation. IMPORTANCE The outbreak of clade 2.3.4.4 H5 highly pathogenic avian influenza (HPAI) virus that occurred in the United States in 2014 and 2015 represents the worst livestock disease event in the country, with unprecedented socioeconomic and commercial consequences. Epidemiological and molecular investigations can identify transmission pathways of the HPAI virus. However, understanding the pathogenesis, transmission, and intrahost evolutionary dynamics of new HPAI viruses in different avian species is paramount. The significance of our research is in examining the susceptibility of minor gallinaceous species to HPAI virus, as this poultry sector also suffers from HPAI epizootics, and identifying the biological potential of these species as an epidemiological link between the waterfowl reservoir and the commercial chicken and turkey populations, with the ultimate goal of refining surveillance in these populations to enhance early detection, management, and control in future HPAI virus outbreaks.

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“…Indeed, under experimental conditions, LPAIVs do not typically cause morbidity or mortality in gallinaceous birds (Alexander et al, 1986;Makarova et al, 2003;Perez et al, 2003a,b;Humberd et al, 2006Humberd et al, , 2007Bertran et al, 2011Bertran et al, , 2013Thontiravong et al, 2012a;). Nonetheless, some subtypes such as H9N2 or H10 may result in non-specific clinical signs including decreased activity, ruffled feathers, coughing and sneezing, diarrhoea, and fall in egg production as reported in J. quail (Makarova et al, 2003;Lavoie et al, 2007;Nili et al, 2007;Ebrahimi et al, 2011;Bonfante et al, 2013) and C. partridge (Nili et al, 2013).…”

Section: Pathobiology Of Lpaivs In Minor Gallinaceous Speciesmentioning

confidence: 99%

“…However, differences in viral shedding effectiveness have been observed among species and for different viruses. Therefore, J. quail (Makarova et al, 2003;Bonfante et al, 2013), E. quail (Bertran et al, 2013), and R. pheasants (Humberd et al, 2006(Humberd et al, , 2007 are recognized as efficient shedders of LPAIV, especially by the oral route but occasionally also by the cloacal route. In particular, inoculation of LPAIV representing subtypes H1 to H15 proved that J. quail may support the replication (predominantly in the respiratory tract) of almost all of them (Makarova et al, 2003).…”

Section: Pathobiology Of Lpaivs In Minor Gallinaceous Speciesmentioning

confidence: 99%