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BMC Medicine
Published in: BMC Medicine 1/2013

Open Access 01-12-2013 | Research article

Transmission potential of influenza A/H7N9, February to May 2013, China

Authors: Gerardo Chowell, Lone Simonsen, Sherry Towers, Mark A Miller, Cécile Viboud

Published in: BMC Medicine | Issue 1/2013

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Abstract

Background

On 31 March 2013, the first human infections with the novel influenza A/H7N9 virus were reported in Eastern China. The outbreak expanded rapidly in geographic scope and size, with a total of 132 laboratory-confirmed cases reported by 3 June 2013, in 10 Chinese provinces and Taiwan. The incidence of A/H7N9 cases has stalled in recent weeks, presumably as a consequence of live bird market closures in the most heavily affected areas. Here we compare the transmission potential of influenza A/H7N9 with that of other emerging pathogens and evaluate the impact of intervention measures in an effort to guide pandemic preparedness.

Methods

We used a Bayesian approach combined with a SEIR (Susceptible-Exposed-Infectious-Removed) transmission model fitted to daily case data to assess the reproduction number (R) of A/H7N9 by province and to evaluate the impact of live bird market closures in April and May 2013. Simulation studies helped quantify the performance of our approach in the context of an emerging pathogen, where human-to-human transmission is limited and most cases arise from spillover events. We also used alternative approaches to estimate R based on individual-level information on prior exposure and compared the transmission potential of influenza A/H7N9 with that of other recent zoonoses.

Results

Estimates of R for the A/H7N9 outbreak were below the epidemic threshold required for sustained human-to-human transmission and remained near 0.1 throughout the study period, with broad 95% credible intervals by the Bayesian method (0.01 to 0.49). The Bayesian estimation approach was dominated by the prior distribution, however, due to relatively little information contained in the case data. We observe a statistically significant deceleration in growth rate after 6 April 2013, which is consistent with a reduction in A/H7N9 transmission associated with the preemptive closure of live bird markets. Although confidence intervals are broad, the estimated transmission potential of A/H7N9 appears lower than that of recent zoonotic threats, including avian influenza A/H5N1, swine influenza H3N2sw and Nipah virus.

Conclusion

Although uncertainty remains high in R estimates for H7N9 due to limited epidemiological information, all available evidence points to a low transmission potential. Continued monitoring of the transmission potential of A/H7N9 is critical in the coming months as intervention measures may be relaxed and seasonal factors could promote disease transmission in colder months.
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Literature
1.
Butler D: Mapping the H7N9 avian flu outbreaks. Nature. 2013, doi:10.1038/nature.2013.12863
2.
3.
4.
Li Q, Zhou L, Zhou M, Chen Z, Li F, Wu H, Xiang N, Chen E, Tang F, Wang D, Meng L, Hong Z, Tu W, Cao Y, Li L, Ding F, Liu B, Wang M, Xie R, Gao R, Li X, Bai T, Zou S, He J, Hu J, Xu Y, Chai C, Wang S, Gao Y, Jin L, et al: Preliminary report: epidemiology of the avian influenza A (H7N9) outbreak in China. N Eng J Med. in press
5.
Chen Y, Liang W, Yang S, Wu N, Gao H, Sheng J, Yao H, Wo J, Fang Q, Cui D, Li Y, Yao X, Zhang Y, Wu H, Zheng S, Diao H, Xia S, Zhang Y, Chan K-H, Tsoi HW, Teng JL, Song W, Wang P, Lau S-Y, Zheng M, Chan JF, To KK, Chen H, Li L, Yuen KY: Human infections with the emerging avian influenza A H7N9 virus from wet market poultry: clinical analysis and characterisation of viral genome. Lancet. 2013, 381: 1916-1925. 10.1016/S0140-6736(13)60903-4.CrossRefPubMed
6.
7.
Gao R, Cao B, Hu Y, Feng Z, Wang D, Hu W, Chen J, Jie Z, Qiu H, Xu K, Xu X, Lu H, Zhu W, Gao Z, Xiang N, Shen Y, He Z, Gu Y, Zhang Z, Yang Y, Zhao X, Zhou L, Li X, Zou S, Zhang Y, Li X, et al: Human infection with a novel avian-origin influenza A (H7N9) virus. N Engl J Med. 2013, 368: 1888-1897. 10.1056/NEJMoa1304459.CrossRefPubMed
8.
Zhu H, Wang D, Kelvin DJ, Li L, Zheng Z, Yoon S-W, Wong S-S, Farooqui A, Wang J, Banner D, Chen R, Zheng R, Zhou J, Zhang Y, Hong W, Dong W, Cai Q, Roehrl MH, Huang SS, Kelvin AA, Yao T, Zhou B, Chen X, Leung GM, Poon LL, Webster RG, Webby RJ, Peiris JS, Guan Y, Shu Y: Infectivity, transmission, and pathology of human H7N9 influenza in ferrets and pigs. Science. 2013, 341: 183-186. 10.1126/science.1239844.CrossRefPubMed
9.
From SARS to H7N9: will history repeat itself?. Lancet. 2013, 381: 1333-10.1016/S0140-6736(13)60865-X.
10.
11.
Bettencourt LM, Ribeiro RM: Real time bayesian estimation of the epidemic potential of emerging infectious diseases. PLoS One. 2008, 3: e2185-10.1371/journal.pone.0002185.CrossRefPubMedPubMedCentral
12.
Chowell G, Nishiura H, Bettencourt LM: Comparative estimation of the reproduction number for pandemic influenza from daily case notification data. J R Soc Interface. 2007, 4: 155-166. 10.1098/rsif.2006.0161.CrossRefPubMed
13.
Birrell PJ, Ketsetzis G, Gay NJ, Cooper BS, Presanis AM, Harris RJ, Charlett A, Zhang XS, White PJ, Pebody RG, De Angelis D: Bayesian modeling to unmask and predict influenza A/H1N1pdm dynamics in London. Proc Natl Acad Sci U S A. 2011, 108: 18238-18243. 10.1073/pnas.1103002108.CrossRefPubMedPubMedCentral
14.
Chowell G, Fenimore PW, Castillo-Garsow MA, Castillo-Chavez C: SARS outbreaks in Ontario, Hong Kong and Singapore: the role of diagnosis and isolation as a control mechanism. J Theor Biol. 2003, 224: 1-8. 10.1016/S0022-5193(03)00228-5.CrossRefPubMed
15.
Lipsitch M, Cohen T, Cooper B, Robins JM, Ma S, James L, Gopalakrishna G, Chew SK, Tan CC, Samore MH, Fisman D, Murray M: Transmission dynamics and control of severe acute respiratory syndrome. Science. 2003, 300: 1966-1970. 10.1126/science.1086616.CrossRefPubMedPubMedCentral
16.
Chowell G, Ammon CE, Hengartner NW, Hyman JM: Estimation of the reproductive number of the Spanish flu epidemic in Geneva, Switzerland. Vaccine. 2006, 24: 6747-6750. 10.1016/j.vaccine.2006.05.055.CrossRefPubMed
17.
Nishiura H, Castillo-Chavez C, Safan M, Chowell G: Transmission potential of the new influenza A(H1N1) virus and its age-specificity in Japan. Euro Surveill. 2009, 14.
18.
Mills CE, Robins JM, Lipsitch M: Transmissibility of 1918 pandemic influenza. Nature. 2004, 432: 904-906. 10.1038/nature03063.CrossRefPubMed
19.
Viboud C, Tam T, Fleming D, Handel A, Miller MA, Simonsen L: Transmissibility and mortality impact of epidemic and pandemic influenza, with emphasis on the unusually deadly 1951 epidemic. Vaccine. 2006, 24: 6701-6707. 10.1016/j.vaccine.2006.05.067.CrossRefPubMed
20.
Cauchemez S, Epperson S, Biggerstaff M, Swerdlow D, Finelli L, Ferguson NM: Using routine surveillance data to estimate the epidemic potential of emerging zoonoses: application to the emergence of US swine origin influenza A H3N2v virus. PLoS Med. 2013, 10: e1001399-10.1371/journal.pmed.1001399.CrossRefPubMedPubMedCentral
21.
Luby SP, Hossain MJ, Gurley ES, Ahmed BN, Banu S, Khan SU, Homaira N, Rota PA, Rollin PE, Comer JA, Kenah E, Ksiazek TG, Rahman M: Recurrent zoonotic transmission of Nipah virus into humans, Bangladesh, 2001–2007. Emerg Infect Dis. 2009, 15: 1229-1235. 10.3201/eid1508.081237.CrossRefPubMedPubMedCentral
22.
Nishiura H, Mizumoto K, Ejima K: How to interpret the transmissibility of novel influenza A(H7N9): an analysis of initial epidemiological data of human cases from China. Theor Biol Med Model. 2013, 10: 30-10.1186/1742-4682-10-30.CrossRefPubMedPubMedCentral
23.
Bettencourt LM, Ribeiro RM, Chowell G, Lant T, Castillo-Chavez C: Towards real time epidemiology: data assimilation, modeling and anomaly detection of health surveillance data streams. Intelligence and security informatics: biosurveillance. Lecture Notes in Comput Sci. 2007, 4506: 79-90. 10.1007/978-3-540-72608-1_8.CrossRef
24.
Yang F, Yuan L, Tan X, Huang C, Feng J: Bayesian estimation of the effective reproduction number for pandemic influenza A H1N1 in Guangdong Province, China. Ann Epidemiol. 2013, 23: 301-306.CrossRefPubMed
25.
Ferguson NM, Cummings DA, Cauchemez S, Fraser C, Riley S, Meeyai A, Iamsirithaworn S, Burke DS: Strategies for containing an emerging influenza pandemic in Southeast Asia. Nature. 2005, 437: 209-214. 10.1038/nature04017.CrossRefPubMed
26.
Gao HN, Lu HZ, Cao B, Du B, Shang H, Gan JH, Lu SH, Yang YD, Fang Q, Shen YZ, Xi XM, Gu Q, Zhou XM, Qu HP, Yan Z, Li FM, Zhao W, Gao ZC, Wang GF, Ruan LX, Wang WH, Ye J, Cao HF, Li XW, Zhang WH, Fang XC, He J, Liang WF, Xie J, Zeng M, et al: Clinical findings in 111 cases of influenza A (H7N9) virus infection. N Engl J Med. 2013, 368: 2277-2285. 10.1056/NEJMoa1305584.CrossRefPubMed
27.
Cowan G: Statistical Data Analysis. 1998, Oxford: Oxford University Press
28.
29.
Pitzer VE, Olsen SJ, Bergstrom CT, Dowell SF, Lipsitch M: Little evidence for genetic susceptibility to influenza A (H5N1) from family clustering data. Emerg Infect Dis. 2007, 13: 1074-1076. 10.3201/eid1307.061538.CrossRefPubMedPubMedCentral
30.
Lindstrom S, Garten R, Balish A, Shu B, Emery S, Berman L, Barnes N, Sleeman K, Gubareva L, Villanueva J, Klimov A: Human infections with novel reassortant influenza A(H3N2)v viruses, United States, 2011. Emerg Infect Dis. 2012, 18: 834-837. 10.3201/eid1805.111922.CrossRefPubMedPubMedCentral
31.
Andreasen V, Viboud C, Simonsen L: Epidemiologic characterization of the 1918 influenza pandemic summer wave in Copenhagen: implications for pandemic control strategies. J Infect Dis. 2008, 197: 270-278. 10.1086/524065.CrossRefPubMedPubMedCentral
32.
Chowell G, Viboud C, Simonsen L, Miller MA, Acuna-Soto R, Diaz JM, Martinez-Martin AF: The 1918–19 influenza pandemic in Boyaca, Colombia. Emerg Infect Dis. 2012, 18: 48-56. 10.3201/eid1801.101969.CrossRefPubMedPubMedCentral
33.
Viboud C, Tam T, Fleming D, Miller MA, Simonsen L: 1951 influenza epidemic, England and Wales, Canada, and the United States. Emerg Infect Dis. 2006, 12: 661-668. 10.3201/eid1204.050695.CrossRefPubMedPubMedCentral
34.
Boëlle P-Y, Ansart S, Cori A, Valleron A-J: Transmission parameters of the A/H1N1 (2009) influenza virus pandemic: a review. Influenza Other Respi Viruses. 2011, 5: 306-316. 10.1111/j.1750-2659.2011.00234.x.CrossRef
35.
Fraser C, Donnelly CA, Cauchemez S, Hanage WP, Van Kerkhove MD, Hollingsworth TD, Griffin J, Baggaley RF, Jenkins HE, Lyons EJ, Jombart T, Hinsley WR, Grassly NC, Balloux F, Ghani AC, Ferguson NM, Rambaut A, Pybus OG, Lopez-Gatell H, Alpuche-Aranda CM, Chapela IB, Zavala EP, Guevara DM, Checchi F, Garcia E, Hugonnet S, Roth C, WHO Rapid Pandemic Assessment Collaboration: Pandemic potential of a strain of influenza A (H1N1): early findings. Science. 2009, 324: 1557-1561. 10.1126/science.1176062.CrossRefPubMedPubMedCentral
36.
Yang Y, Sugimoto JD, Halloran ME, Basta NE, Chao DL, Matrajt L, Potter G, Kenah E, Longini IM: The transmissibility and control of pandemic influenza A (H1N1) virus. Science. 2009, 326: 729-733. 10.1126/science.1177373.CrossRefPubMedPubMedCentral
37.
Munayco CV, Gomez J, Laguna-Torres VA, Arrasco J, Kochel TJ, Fiestas V, Garcia J, Perez J, Torres I, Condori F, Nishiura H, Chowell G: Epidemiological and transmissibility analysis of influenza A(H1N1)v in a southern hemisphere setting: Peru. Euro Surveill. 2009, 14.
38.
White LF, Wallinga J, Finelli L, Reed C, Riley S, Lipsitch M, Pagano M: Estimation of the reproductive number and the serial interval in early phase of the 2009 influenza A/H1N1 pandemic in the USA. Influenza Other Respi Viruses. 2009, 3: 267-276. 10.1111/j.1750-2659.2009.00106.x.CrossRefPubMedCentral
39.
Nishiura H, Chowell G, Safan M, Castillo-Chavez C: Pros and cons of estimating the reproduction number from early epidemic growth rate of influenza A (H1N1) 2009. Theor Biol Med Model. 2010, 7: 1-10.1186/1742-4682-7-1.CrossRefPubMedPubMedCentral
40.
Katriel G, Yaari R, Huppert A, Roll U, Stone L: Modelling the initial phase of an epidemic using incidence and infection network data, H1N1 pandemic in Israel as a case study. J R Soc Interface. 2009, 2011: 856-867.
41.
Chowell G, Miller MA, Viboud C: Seasonal influenza in the United States, France, and Australia: transmission and prospects for control. Epidemiol Infect. 2007, 136: 852-864.PubMedPubMedCentral
42.
Chowell G, Viboud C, Simonsen L, Miller M, Alonso WJ: The reproduction number of seasonal influenza epidemics in Brazil, 1996–2006. Proc Biol Sci. 2010, 277: 1857-1866. 10.1098/rspb.2009.1897.CrossRefPubMedPubMedCentral
43.
Parashar UD, Sunn LM, Ong F, Mounts AW, Arif MT, Ksiazek TG, Kamaluddin MA, Mustafa AN, Kaur H, Ding LM, Othman G, Radzi HM, Kitsutani PT, Stockton PC, Arokiasamy J, Gary HE, Anderson LJ: Case–control study of risk factors for human infection with a new zoonotic paramyxovirus, Nipah virus, during a 1998–1999 outbreak of severe encephalitis in Malaysia. J Infect Dis. 2000, 181: 1755-1759. 10.1086/315457.CrossRefPubMed
44.
Riley S, Fraser C, Donnelly CA, Ghani AC, Abu-Raddad LJ, Hedley AJ, Leung GM, Ho LM, Lam TH, Thach TQ, Chau P, Chan KP, Lo SV, Leung PY, Tsang T, Ho W, Lee KH, Lau EM, Ferguson NM, Anderson RM: Transmission dynamics of the etiological agent of SARS in Hong Kong: impact of public health interventions. Science. 2003, 300: 1961-1966. 10.1126/science.1086478.CrossRefPubMed
45.
46.
47.
Shaman J, Kohn M: Absolute humidity modulates influenza survival, transmission, and seasonality. Proc Natl Acad Sci USA. 2009, 106: 3243-3248. 10.1073/pnas.0806852106.CrossRefPubMedPubMedCentral
48.
Shaman J, Pitzer VE, Viboud C, Grenfell BT, Lipsitch M: Absolute humidity and the seasonal onset of influenza in the continental United States. PLoS Biol. 2010, 8: e1000316-10.1371/journal.pbio.1000316.CrossRefPubMedPubMedCentral
49.
Breban R, Riou J, Fontanet A: Interhuman transmissibility of Middle East respiratory syndrome coronavirus: estimation of pandemic risk. Lancet. 2013, 382: 694-699. 10.1016/S0140-6736(13)61492-0.CrossRefPubMed
50.
Bai T, Zhou J, Shu Y: Serologic study for influenza A (H7N9) among high-risk groups in China. N Engl J Med. 2013, 368: 2339-2340. 10.1056/NEJMc1305865.CrossRefPubMed
51.
Boni MF, Chau NV, Dong N, Todd S, Nhat NT, de Bruin E, van Beek J, Hien NT, Simmons CP, Farrar J, Koopmans M: Population-level antibody estimates to novel influenza A/H7N9. J Infect Dis. 2013, 208: 554-558. 10.1093/infdis/jit224.CrossRefPubMedPubMedCentral
52.
Xu C, Havers F, Wang L, Chen T, Shi J, Wang D, et al: Monitoring avian influenza A(H7N9) virus through national influenza-like illness surveillance, China. Emerg Infect Dis. 2013, 19: doi:10.3201/eid1908.130662
Metadata
Title
Transmission potential of influenza A/H7N9, February to May 2013, China
Authors
Gerardo Chowell
Lone Simonsen
Sherry Towers
Mark A Miller
Cécile Viboud
Publication date
01-12-2013
Publisher
BioMed Central
Published in
BMC Medicine / Issue 1/2013
Electronic ISSN: 1741-7015
DOI
https://doi.org/10.1186/1741-7015-11-214

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