Elsevier

The Lancet

Volume 383, Issue 9916, 8–14 February 2014, Pages 541-548
The Lancet

Articles
Effect of closure of live poultry markets on poultry-to-person transmission of avian influenza A H7N9 virus: an ecological study

https://doi.org/10.1016/S0140-6736(13)61904-2Get rights and content

Summary

Background

Transmission of the novel avian influenza A H7N9 virus seems to be predominantly between poultry and people. In the major Chinese cities of Shanghai, Hangzhou, Huzhou, and Nanjing—where most human cases of infection have occurred—live poultry markets (LPMs) were closed in April, 2013, soon after the initial outbreak, as a precautionary public health measure. Our objective was to quantify the effect of LPM closure in these cities on poultry-to-person transmission of avian influenza A H7N9 virus.

Methods

We obtained information about every laboratory-confirmed human case of avian influenza A H7N9 virus infection reported in the four cities by June 7, 2013, from a database built by the Chinese Center for Disease Control and Prevention. We used data for age, sex, location, residence type (rural or urban area), and dates of illness onset. We obtained information about LPMs from official sources. We constructed a statistical model to explain the patterns in incidence of cases reported in each city on the basis of the assumption of a constant force of infection before LPM closure, and a different constant force of infection after closure. We fitted the model with Markov chain Monte Carlo methods.

Findings

85 human cases of avian influenza A H7N9 virus infection were reported in Shanghai, Hangzhou, Huzhou, and Nanjing by June 7, 2013, of which 60 were included in our main analysis. Closure of LPMs reduced the mean daily number of infections by 99% (95% credibility interval 93–100%) in Shanghai, by 99% (92–100%) in Hangzhou, by 97% (68–100%) in Huzhou, and by 97% (81–100%) in Nanjing. Because LPMs were the predominant source of exposure to avian influenza A H7N9 virus for confirmed cases in these cities, we estimated that the mean incubation period was 3·3 days (1·4–5·7).

Interpretation

LPM closures were effective in the control of human risk of avian influenza A H7N9 virus infection in the spring of 2013. In the short term, LPM closure should be rapidly implemented in areas where the virus is identified in live poultry or people. In the long term, evidence-based discussions and deliberations about the role of market rest days and central slaughtering of all live poultry should be renewed.

Funding

Ministry of Science and Technology, China; Research Fund for the Control of Infectious Disease; Hong Kong University Grants Committee; China–US Collaborative Program on Emerging and Re-emerging Infectious Diseases; Harvard Center for Communicable Disease Dynamics; and the US National Institutes of Health.

Introduction

On March 31, 2013, the first laboratory-confirmed human infection with avian influenza A H7N9 virus was officially announced in Shanghai. Phylogenetic analysis showed that the virus was a novel triple reassortant of avian influenza A H7N3, A H7N9, and A H9N2 viruses,1, 2 and seems to have spread widely with low pathogenicity in poultry in the Yangtze river delta.3 By June 7, 2013, influenza A H7N9 virus had been associated with typically serious disease in 130 individuals,4 and has also seemingly caused mild human infections.5, 6 Because no evidence of sustained or efficient person-to-person transmission is available as yet,2, 4, 7 the focus of prevention remains at the interface between people and poultry.8, 9, 10

Live poultry markets (LPMs) are common in China and many other countries (eg, Thailand, Laos, and Singapore), primarily in urban areas. A 2006 survey in Guangzhou—the provincial capital of Guangdong Province, which borders the Hong Kong Special Administrative Region in southern China—showed that 80% of households reported purchasing poultry at LPMs at least once a year, and more frequent purchases were common.11 LPMs therefore pose an important potential zoonotic risk if the flocks are infected with avian influenza viruses.12 Moreover, transmission of the virus between birds can be increased in LPMs, because many birds are kept together in a small area, thereby increasing the risk of transmission to people.13

The first human outbreak of avian influenza A H5N1 virus infection was in Hong Kong in 1997, with 18 cases and six deaths.14 The epidemic was quickly contained after territory-wide LPM closure and depopulation of all local poultry farms.15 Since 2003, avian influenza A H5N1 viruses have continued to infect people; as of Aug 29, 2013, 45 cases have been confirmed in mainland China and 637 worldwide,16 with some infections directly attributable to LPM exposure.4, 17

LPM closure in urban areas of some cities in eastern China has coincided with reductions in human cases of influenza A H7N9 virus infection,4 although only the qualitative effect of LPM closures on poultry-to-people transmission has been investigated in previous studies, without a formal causal inferential framework.10, 18, 19 Although the conclusions of the previous studies are persuasive, without robust evidence to define and quantify such effect, policy makers would struggle to justify the continued closure of LPMs because of the millennia-old culture of trading of live birds and the potential economic implications.20 On the basis of previous reports of influenza viral zoonoses of H5, H7, and H9, autumn could bring a new wave of infections after a quiet summer period.4 The new wave will test the tenet advocated by the Food and Agriculture Organization, World Organisation for Animal Health, WHO, UN, UNICEF, and World Bank to “diminish the risk and minimize the global impact of epidemics and pandemics due to emerging infectious disease”.21 We developed a statistical model to quantify the effect of LPM closure on poultry-to-person transmission of avian influenza A H7N9 virus in the major Chinese cities of Shanghai, Hangzhou, Huzhou, and Nanjing.

Section snippets

Data sources

We investigated incidence of avian influenza A H7N9 virus infection until June 7, 2013. The Chinese Center for Disease Control and Prevention (China CDC) has built an integrated dataset with detailed demographic, epidemiological, and geographical information about every reported laboratory-confirmed human case of avian influenza A H7N9 virus infection.4 In our analysis, we used information about age, sex, location, residence type (rural or urban area), and dates of illness onset. Case

Results

Of the 130 individuals with avian influenza A H7N9 virus infection reported by June 7, 2013, 123 (95%) had serious disease with pneumonia and 44 (34%) had died. 85 (65%) were identified in Shanghai, Hangzhou, Huzhou, and Nanjing. Although 88 of the 95 cases with illness onset confirmed by April 12 were identified in this area, from April and May, cases spread away from the epicentre to surrounding provinces.4

Local authorities closed the 460 LPMs in Shanghai on April 6, and the 92 in Nanjing on

Discussion

Our findings show that LPM closure in the Chinese cities of Nanjing, Huzhou, Hangzhou, and Shanghai substantially reduced the incidence of human infection with avian influenza A H7N9 virus (panel). Incidence fell substantially within 2–3 days of LPM closure. Two points raised by our findings are important. First, they support the idea that LPM exposure has a major role in human risk of avian influenza A H7N9 virus infection in urban areas.18, 19, 34 Although a previous study4 showed that 75% of

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