Ahead of Print -Possible Role of Songbirds and Parakeets in Transmission of Influenza A(H7N9) Virus to Humans - Volume 20, Number 3—March 2014 - Emerging Infectious Disease journal - CDC

full-text ►

Ahead of Print -Possible Role of Songbirds and Parakeets in Transmission of Influenza A(H7N9) Virus to Humans - Volume 20, Number 3—March 2014 - Emerging Infectious Disease journal - CDC

Volume 20, Number 3—March 2014

Research

Possible Role of Songbirds and Parakeets in Transmission of Influenza A(H7N9) Virus to Humans

Article Contents

• Methods
• Results
• Discussion
• Acknowledgments
• References
• Figure
• Table 1
• Table 2
• Table 3
• Table 4
• Suggested Citation

Jeremy C. Jones, Stephanie Sonnberg, Zeynep A. Koçer, Karthik Shanmuganatham, Patrick Seiler, Yuelong Shu, Huachen Zhu, Yi Guan, Malik Peiris, Richard J. Webby, and Robert G. Webster 

Author affiliations: St. Jude Children’s Research Hospital, Memphis, Tennessee, USA (J.C. Jones, S. Sonnberg, Z.A. Kocer, K. Shanmuganatham, P. Seiler, R.J. Webby, R.G. Webster); Chinese Center for Disease Control and Prevention, Beijing, China (Y. Shu); Shantou University Medical College, Shantou, China (H. Zhu, Y. Guan); State Key Laboratory of Emerging Infectious Diseases, Shenzhen Third People's Hospital, Shenzhen, China (H. Zhu, Y. Guan, M. Peiris); The University of Hong Kong, Hong Kong, China (H. Zhu, Y. Guan, M. Peiris)

Suggested citation for this article

Abstract

Avian-origin influenza A(H7N9) recently emerged in China, causing severe human disease. Several subtype H7N9 isolates contain influenza genes previously identified in viruses from finch-like birds. Because wild and domestic songbirds interact with humans and poultry, we investigated the susceptibility and transmissibility of subtype H7N9 in these species. Finches, sparrows, and parakeets supported replication of a human subtype H7N9 isolate, shed high titers through the oropharyngeal route, and showed few disease signs. Virus was shed into water troughs, and several contact animals seroconverted, although they shed little virus. Our study demonstrates that a human isolate can replicate in and be shed by such songbirds and parakeets into their environment. This finding has implications for these birds’ potential as intermediate hosts with the ability to facilitate transmission and dissemination of A(H7N9) virus.

The emergence of novel influenza strains from the avian reservoir remains a constant threat to human and animal health, as was recently illustrated by human infections with novel and wholly avian influenza A(H7N9) viruses in China. These viruses show little virulence in birds but can cause severe illness in humans (1,2). Of the 134 confirmed human cases, >30% have been fatal (3,4). In the 3 index case-patients, the illness progressed to acute respiratory distress syndrome and death (1), and most persons with confirmed infections required hospital care (2,5). Retrospective epidemiologic analyses showed >75% of affected patients had had contact with domestic poultry (6,7), a common source of zoonotic transmission of influenza (8). Several of the A(H7N9) virus internal genes (polymerase basic protein [PB] 1, matrix, nonstructural protein, and nucleoprotein) originated from the H9N2 subtype commonly found in chickens. When chickens and quail were inoculated with A(H7N9) isolated from humans, they shed the viruses to high titers but had little or no clinical disease (9,10). Thus, poultry appears to be a reservoir for A(H7N9) viruses and a source of human infections. Yet, multiple lines of evidence suggest avian species other than the usual suspects (waterfowl and poultry) contributed to the emergence of these novel H7N9 viruses: first, H7N9 has been isolated from nonpoultry birds (pigeons) in Chinese live-bird markets (11); second, 2 genes (PA, PB2) in an initially characterized human isolate (A/Anhui/1/2013) were most closely related to viruses isolated from bramblings (finch-like birds of the large order Passeriformes) (12); and third, the matrix, polymerase acidic protein [PA], PB1 and PB2 gene segments from additional human isolates appear to have been donated by A/brambling/Beijing/16/2012 (H9N2)-like virus(es) (13). Therefore, songbirds and other small, terrestrial birds could have been directly involved in the genesis of novel A(H7N9) viruses and subsequent infection in humans.

Songbirds are common household pets and are in close contact with humans and domesticated animals. Their wild counterparts also are likely to interact with poultry in backyard farms and in many farming sectors (14,15). Consequently, we examined the replication and transmission of the human isolate A/Anhui/1/2013 (H7N9) in wild and domesticated small birds. A/Anhui/1/2013 was isolated from one of the initially reported human case-patients (1) and is closely related to many of the avian isolates that have been recovered (12). For this study, we chose 3 species of Passeriformes (zebra finches, society finches, and sparrows), which are related to the bramblings described previously. We also studied the parakeet (budgerigar; order Psittaciformes), a bird found in the wild and in households as a pet, that is known to support the replication of other subtypes of influenza (16–18). The study was conducted during June and July 2013 at St. Jude Children’s Research Hospital (Memphis, TN, USA).

Acknowledgments

We thank Lisa Kercher, Gregory Charlton, Jim Coleman, David Carey, Beth Little, and Angela Danner for assistance with animal experiments; Sharon Naron and Kimberly Friedman for editing the manuscript; and James Knowles for administrative assistance.

This work was supported by contract no. HHSN266200700005C from the US National Institute of Allergy and Infectious Disease, National Institutes of Health, US Department of Health and Human Services; and by the American Lebanese Syrian Associated Charities.

References

1. Gao R, Cao B, Hu Y, Feng Z, Wang D, Hu W, Human infection with a novel avian-origin influenza A (H7N9) virus. N Engl J Med. 2013;368:1888–97 . DOIPubMed
2. Yang S, Chen Y, Cui D, Yao H, Lou J, Huo Z, Avian-origin H7N9 virus infection in H7N9-affected areas of China: a serological study. J Infect Dis. 2013; Epub ahead of print.PMID: 23935201
3. World Health Organization. Number of confirmed human cases of avian influenza A(H7N9) reported to WHO 2013 [2013 Aug 16].http://www.who.int/influenza/human_animal_interface/influenza_h7n9/08_ReportWebH7N9Number.pdf 
4. World Health Organization. Human infection with avian influenza A(H7N9) virus—update. Global Alert and Response (GAR) 2013. 7.20.2013 [cited 2013 Aug 8].http://www.who.int/csr/don/2013_07_20/en/
5. Yu H, Cowling BJ, Feng L, Lau EH, Liao Q, Tsang TK, Human infection with avian influenza A H7N9 virus: an assessment of clinical severity. Lancet. 2013;382:138–45 . DOIPubMed
6. World Health Organization. WHO risk assessment: Human infections with influenza A (H7N9) virus. Geneva: The Organization; 2013.
7. Lee SS, Wong NS, Leung CC. Exposure to avian influenza H7N9 in farms and wet markets. Lancet. 2013;381:1815 and. DOIPubMed
8. de Wit E, Fouchier RA. Emerging influenza. J Clin Virol. 2008;41:1–6. DOIPubMed
9. Kahn RE, Richt JA. The novel H7N9 influenza a virus: its present impact and indeterminate future. Vector Borne Zoonotic Dis. 2013;13:347–8 . DOIPubMed
10. Branswell H. Chicken, quail catch and shed high volumes of new H7N9 flu, study shows. The Canadian Press. Toronto: Shaw Media; 2013 [cited 2013 Aug 16].http://globalnews.ca/news/619005/chicken-quail-catch-and-shed-high-volumes-of-new-h7n9-flu-study-shows/
11. Centers for Disease Control and Prevention. Emergence of avian influenza A(H7N9) virus causing severe human illness—China, February–April 2013. MMWR Morb Mortal Wkly Rep. 2013;62:366–71 .PubMed
12. Kageyama T, Fujisaki S, Takashita E, Xu H, Yamada S, Uchida Y, Genetic analysis of novel avian A(H7N9) influenza viruses isolated from patients in China, February to April 2013.Euro Surveill. 2013;18:20453 .PubMed
13. Zhang L, Zhang Z, Weng Z. Rapid reassortment of internal genes in avian influenza A H7N9 virus. Clin Infect Dis. 2013;57:1059–61. DOIPubMed
14. Brown JD, Stallknecht DE, Berghaus RD, Swayne DE. Infectious and lethal doses of H5N1 highly pathogenic avian influenza virus for house sparrows (Passer domesticus) and rock pigeons (Columbia livia). J Vet Diagn Invest. 2009;21:437–45. DOIPubMed
15. Forrest HL, Kim JK, Webster RG. Virus shedding and potential for interspecies waterborne transmission of highly pathogenic H5N1 influenza virus in sparrows and chickens. J Virol. 2010;84:3718–20. DOIPubMed
16. Edmunds K, Roberton SI, Few R, Mahood S, Bui PL, Hunter PR, Investigating Vietnam's ornamental bird trade: implications for transmission of zoonoses. EcoHealth.2011;8:63–75. DOIPubMed
17. Perkins LE, Swayne DE. Varied pathogenicity of a Hong Kong–origin H5N1 avian influenza virus in four passerine species and budgerigars. Vet Pathol. 2003;40:14–24. DOIPubMed
18. Isoda N, Sakoda Y, Kishida N, Bai GR, Matsuda K, Umemura T, Pathogenicity of a highly pathogenic avian influenza virus, A/chicken/Yamaguchi/7/04 (H5N1) in different species of birds and mammals. Arch Virol. 2006;151:1267–79. DOIPubMed
19. Reed LJ, Muench H. A simple method for estimating fifty percent endpoints. Am J Hyg.1938;27:493–7.
20. Boon AC, Sandbulte MR, Seiler P, Webby RJ, Songserm T, Guan Y, Role of terrestrial wild birds in ecology of influenza A virus (H5N1). Emerg Infect Dis. 2007;13:1720–4. DOIPubMed
21. Palmer DFDW, Coleman MT, Schild GC. Hemagglutination inhibition test. Advanced laboratory techniques for influenza diagnosis. Atlanta: US Department of Health. Education, and Welfare; 1975.
22. Brown JD, Swayne DE, Cooper RJ, Burns RE, Stallknecht DE. Persistence of H5 and H7 avian influenza viruses in water. Avian Dis. 2007;51:285–9. DOIPubMed
23. Nestorowicz A, Kawaoka Y, Bean WJ, Webster RG. Molecular analysis of the hemagglutinin genes of Australian H7N7 influenza viruses: role of passerine birds in maintenance or transmission? Virology. 1987;160:411–8 . DOIPubMed
24. Nemeth NM, Thomas NO, Orahood DS, Anderson TD, Oesterle PT. Shedding and serologic responses following primary and secondary inoculation of house sparrows (Passer domesticus) and European starlings (Sturnus vulgaris) with low-pathogenicity avian influenza virus. Avian Pathol. 2010;39:411–8. DOIPubMed
25. Gutiérrez RA, Sorn S, Nicholls JM, Buchy P. Eurasian tree sparrows, risk for H5N1 virus spread and human contamination through Buddhist ritual: an experimental approach.PLoS ONE. 2011;6:e28609. DOIPubMed
26. Boseret G, Losson B, Mainil JG, Thiry E, Saegerman C. Zoonoses in pet birds: review and perspectives. Vet Res. 2013;44:36. DOIPubMed
27. Rivers C, Lum K, Lewis B, Eubank S. Estimating human cases of avian influenza A(H7N9) from poultry exposure. PLoS Curr. 2013;5: pii: ecurrents.outbreaks.264e737b489bef383fbcbaba60daf928.
28. Driedger M. Hong Kong's bird garden 2011 [cited 2013 Jul 23].http://www.thingsasian.com/stories-photos/36899
29. Cheng J. Pet birds a boon to Beijing's elderly. 2013 [cited 2013 Jul 23].http://gbtimes.com/culture/customs/pet-birds-boon-beijings-elderly
30. Delogu M, De Marco MA, Di Trani L, Raffini E, Cotti C, Puzelli S, Can preening contribute to influenza A virus infection in wild waterbirds? PLoS ONE. 2010;5:e11315 . DOIPubMed
31. Cowling BJ, Jin L, Lau EH, Liao Q, Wu P, Jiang H, Comparative epidemiology of human infections with avian influenza A H7N9 and H5N1 viruses in China: a population-based study of laboratory-confirmed cases. Lancet. 2013;382:129–37 . DOIPubMed
32. Du Ry van Beest Holle M, Meijer A, Koopmans M, de Jager CM. Human-to-human transmission of avian influenza A/H7N7, the Netherlands, 2003. Euro Surveill.2005;10:264–8 .PubMed
33. Liu D, Shi W, Shi Y, Wang D, Xiao H, Li W, Origin and diversity of novel avian influenza A H7N9 viruses causing human infection: phylogenetic, structural, and coalescent analyses. Lancet. 2013;381:1926–32 . DOIPubMed

Figure

• Figure. . Virus shedding into water trough. A 500-μL sample of water was collected daily for 6 days, and virus was titrated in chicken eggs. The lower limit of detection was...

Tables

• Table 1. Oropharyngeal and cloacal virus titers in birds inoculated with influenza A(H7N9) virus
• Table 2. Shedding of influenza A(H7N9) virus by direct contact among birds
• Table 3. Influenza A(H7N9) virus replication in organs of inoculated birds
• Table 4. Seroconversion of birds to influenza A(H7N9)

Suggested citation for this article: Jones JC, Sonnberg S, Koçer ZA, Shanmuganatham K, Seiler P, Shu Y, et al. Possible role of songbirds and parakeets in transmission of influenza A(H7N9) virus to humans. Emerg Infect Dis [Internet]. 2014 Mar [date cited].http://dx.doi.org/10.3201/eid2003.131271

DOI: 10.3201/eid2003.131271