Live Poultry Markets Closure Research Articles

Live poultry markets beyond health risks: Understanding consumer preferences for live poultry in South China

Live poultry markets (LPMs) are veterinary and public health risks because of potential for zoonotic spillover of pathogens from diseased animals to humans. To control these health risks, veterinary and public health authorities in Asia, including China, have closed or restricted LPMs. In south China, however, LPM closure has been opposed or rendered infeasible by consumers who prefer to purchase live poultry. Previous scholarship has suggested this preference is due to cultural values of freshness. In this study, we present results from detailed interviews with shoppers in south China, including those who prefer live poultry and those who prefer pre-slaughtered poultry. We argue that broader concerns about food safety and quality, rather than freshness alone, drive the demand for LPMs. Live poultry provide sensory information that enable shoppers to evaluate safety and quality in ways that are not possible with pre-slaughtered, refrigerated meat. Based on these findings, we suggest that hygienic interventions into LPMs should recognize that not only freshness, but also trust, must be constructed and maintained in any intervention.

Transmission dynamics and optimal control of H7N9 in China

H7N9 avian influenza is a highly pathogenic zoonotic disease. In order to control the disease, many strategies have been adopted in China such as poultry culling, the closure of live poultry markets (LPMs), the vaccination of poultry, and the treatment for humans. Due to the limited resource, it is of paramount significance to achieve the optimal control. In this paper, an epidemic model incorporating the selective culling rate is formulated to investigate the transmission mechanism of H7N9. The threshold dynamics and bifurcation analyses of the model are well investigated. Furthermore, the problem of optimal control is explored in line with Pontryagin’s Maximum Principle, with consideration given to the comprehensive measures. The numerical simulations suggest that the vaccination of poultry and the closure of LPMs are the two most economical and effective measures.

Different intervention strategies toward live poultry markets against avian influenza A (H7N9) virus: Model-based assessment

BackgroundDifferent interventions targeting live poultry markets (LPMs) are applied in China for controlling avian influenza A (H7N9), including LPM closure and “1110” policy (i.e., daily cleaning, weekly disinfection, monthly rest day, zero poultry stock overnight). However, the interventions’ effectiveness has not been comprehensively assessed. MethodsBased on the available data (including reported cases, domestic poultry volume, and climate) collected in Guangdong Province between October 2013 and June 2017, we developed a new compartmental model that enabled us to infer H7N9 transmission dynamics. The model incorporated the intrinsic interplay among humans and poultry as well as the impacts of absolute humidity and LPM intervention, in which intervention strategies were parameterized and estimated by Markov chain Monte Carlo method. ResultsThere were 258 confirmed human H7N9 cases in Guangdong during the study period. If without interventions, the number would reach 646 (95%CI, 575–718) cases. Temporal, seasonal and permanent closures of LPMs can substantially reduce transmission risk, which might respectively reduce human infections by 67.2% (95%CI, 64.3%–70.1%), 75.6% (95%CI, 73.8%–77.5%), 86.6% (95%CI, 85.7–87.6%) in total four epidemic seasons, and 81.9% (95%CI, 78.7%–85.2%), 91.5% (95%CI, 89.9%–93.1%), 99.0% (95%CI, 98.7%–99.3%) in the last two epidemic seasons. Moreover, implementing the “1110” policy from 2014 to 2017 would reduce the cases by 34.1% (95%CI, 20.1%–48.0%), suggesting its limited role in preventing H7N9 transmission. ConclusionsOur study quantified the effects of different interventions and execution time toward LPMs for controlling H7N9 transmission. The results highlighted the importance of closing LPMs during epidemic period, and supported permanent closure as a long-term plan.

Live poultry market closure and avian influenza A (H7N9) infection in cities of China, 2013\u20132017: an ecological study

BackgroundPrevious studies have proven that the closure of live poultry markets (LPMs) was an effective intervention to reduce human risk of avian influenza A (H7N9) infection, but evidence is limited on the impact of scale and duration of LPMs closure on the transmission of H7N9.MethodFive cities (i.e., Shanghai, Suzhou, Shenzhen, Guangzhou and Hangzhou) with the largest number of H7N9 cases in mainland China from 2013 to 2017 were selected in this study. Data on laboratory-confirmed H7N9 human cases in those five cities were obtained from the Chinese National Influenza Centre. The detailed information of LPMs closure (i.e., area and duration) was obtained from the Ministry of Agriculture. We used a generalized linear model with a Poisson link to estimate the effect of LPMs closure, reported as relative risk reduction (RRR). We used classification and regression trees (CARTs) model to select and quantify the dominant factor of H7N9 infection.ResultsAll five cities implemented the LPMs closure, and the risk of H7N9 infection decreased significantly after LPMs closure with RRR ranging from 0.80 to 0.93. Respectively, a long-term LPMs closure for 10–13 weeks elicited a sustained and highly significant risk reduction of H7N9 infection (RRR = 0.98). Short-time LPMs closure with 2 weeks in every epidemic did not reduce the risk of H7N9 infection (p > 0.05). Partially closed LPMs in some suburbs contributed only 35% for reduction rate (RRR = 0.35). Shenzhen implemented partial closure for first 3 epidemics (p > 0.05) and all closure in the latest 2 epidemic waves (RRR = 0.64).ConclusionOur findings suggest that LPMs all closure in whole city can be a highly effective measure comparing with partial closure (i.e. only urban closure, suburb and rural remain open). Extend the duration of closure and consider permanently closing the LPMs will help improve the control effect. The effect of LPMs closure seems greater than that of meteorology on H7N9 transmission.

Effectiveness of Live Poultry Market Interventions on Human Infection with Avian Influenza A(H7N9) Virus, China.

Various interventions for live poultry markets (LPMs) have emerged to control outbreaks of avian influenza A(H7N9) virus in mainland China since March 2013. We assessed the effectiveness of various LPM interventions in reducing transmission of H7N9 virus across 5 annual waves during 2013–2018, especially in the final wave. With the exception of waves 1 and 4, various LPM interventions reduced daily incidence rates significantly across waves. Four LPM interventions led to a mean reduction of 34%–98% in the daily number of infections in wave 5. Of these, permanent closure provided the most effective reduction in human infection with H7N9 virus, followed by long-period, short-period, and recursive closures in wave 5. The effectiveness of various LPM interventions changed with the type of intervention across epidemics. Permanent LPM closure should be considered to maintain sufficient effectiveness of interventions and prevent the recurrence of H7N9 epidemics.

Effect of closure of live poultry markets in China on prevention and control of human infection with H7N9 avian influenza: a case study of four cities in Jiangsu Province.

As of August 2017, China had encountered five seasonal epidemics of H7N9 avian influenza. To prevent people from contracting H7N9 avian influenza, most cities closed live poultry markets (LPMs) to cut off the source of H7N9 virus. The objective of this study is to assess the impact of LPMs closure on reducing zoonotic transmission of avian influenza A (H7N9) virus and to make specific recommendations on the duration of closing the LPMs. Results show that the closure of LPMs can effectively control the spread of H7N9 avian influenza and reduce the incidence of human infection with H7N9. If cases of H7N9 avian influenza continue to occur, LPMs should close for at least 3-4weeks in susceptible areas to control the spread of infection.

Comparison of the three waves of avian influenza A(H7N9) virus circulation since live poultry markets were permanently closed in the main urban areas in Zhejiang Province, July 2014-June 2017.

BackgroundThe sudden increase in the number of human cases infected with avian influenza A(H7N9) virus after September 2016 raised global concern.ObjectivesTo assess the changes in epidemiological characteristics of H7N9 cases since the massive closure of live poultry markets (LPMs) in the main urban areas in Zhejiang province.MethodsWe used descriptive statistics to compare epidemiological characteristics of the three distinct waves of H7N9 cases in Zhejiang province. The rural or urban cases were defined according to the location where the patients had exposure within 2 weeks before illness onset.ResultsBetween July 2014 and June 2017, 166 H7N9 cases were reported in Zhejiang province, with 45, 34, and 87 cases reported in the third, fourth, and fifth wave, respectively. Across the three waves, most reported cases were from rural areas. A similar percentage of cases in all three waves reported exposure to LPMs, raising poultry at home or around the house, as well as occupational exposure. Compared to the third (80.00%) and fourth wave (70.59%), a significantly larger proportion of cases from the non‐LPMs closure areas were observed in the fifth wave (89.66%) (P = .034).ConclusionEpidemiological characteristics of human cases infected with avian influenza A(H7N9) virus had generally remained unchanged since the massive closure of LPMs in the main urban area of Zhejiang province. The sudden increase in the number of H7N9 cases in the fifth wave was mainly attributed to the excessive cases reported from areas where LPMs were not permanently closed.

An increasing trend of rural infections of human influenza A (H7N9) from 2013 to 2017: A retrospective analysis of patient exposure histories in Zhejiang province, China.

BackgroundAlthough investigations have shown that closing live poultry markets (LPMs) is highly effective in controlling human influenza A (H7N9) infections, many of the urban LPMs were shut down, but rural LPMs remained open. This study aimed to compare the proportional changes between urban and rural infections in the Zhejiang province from 2013 to 2017 by analyzing the exposure histories of human cases.MethodsAll laboratory-confirmed cases of H7N9 from 2013 (the first wave) to 2017 (the fifth wave) in the Zhejiang province of China were analyzed. Urban and rural infections were defined based on the locations of poultry exposure (direct and indirect) in urban areas (central towns) and rural areas (towns and villages on the outskirts of cities). A Chi-square trend test was used to compare the proportional trend between urban and rural infections over time and logistic regression was used to obtain the odds ratio by years.ResultsFrom 2013 to 2017, a statistically significant trend in rural infections was observed (p <0.01). The incremental odds ratio by years of rural infections was 1.59 with 95% confidence intervals of 1.34 to 1.86. Each year, significant increases in the proportion of live poultry transactions in LPMS and poultry processing plants were detected in conjunction with an increased proportion of urban and rural infections.ConclusionThe empirical evidence indicated a need for heightened infection control measures in rural areas, such as serving rural farms and backyards as active surveillance points for the H7N9 virus. Other potential interventions such as the vaccination of poultry and extending the closure of LPMs to the provincial level require further careful investigations.

Contact reductions from live poultry market closures limit the epidemic of human infections with H7N9 influenza

An early steep increase in the number of humans infected with avian influenza A(H7N9) virus was observed in China, raising great public concern domestically and internationally. Little is known about the dynamics of the transmission contacts between poultry and human populations, although such understanding is essential for developing effective strategies to control this zoonosis. In this study, we evaluated the effects of contact reductions from live poultry markets (LPMs) closures on the transmission of H7N9 virus during epidemics in Guangdong Province, China. A mathematical model of the poultry-to-person transmission dynamics of H7N9 virus was constructed. The parameters in the model were estimated from publicly available data on confirmed cases of human infection and information on LPMs closure during 2013–2017. By fitting the model, we measured the time-dependent contact quantity of the susceptible population to LPMs. The results showed that periodic intervention strategies can greatly reduce the magnitude of outbreaks, and the earlier interventions for policy are implemented, the smaller is the outbreak. The control efforts for LPMs to decrease the contact quantity are critical in preventing epidemics in the long term. This model should provide important insights for the development of a national intervention strategy for the long-term control of avian influenza virus epidemics.

Evaluation of animal-to-human and human-to-human transmission of influenza A (H7N9) virus in China, 2013\u201315

A novel avian-origin influenza A(H7N9) virus emerged in China in March 2013 and by 27 September 2017 a total of 1533 laboratory-confirmed cases have been reported. Occurrences of animal-to-human and human-to-human transmission have been previously identified, and the force of human-to-human transmission is an important component of risk assessment. In this study, we constructed an ecological model to evaluate the animal-to-human and human-to-human transmission of H7N9 during the first three epidemic waves in spring 2013, winter/spring 2013–2014 and winter/spring 2014–2015 in China based on 149 laboratory-confirmed urban cases. Our analysis of patterns in incidence in major cities allowed us to estimate a mean incubation period in humans of 2.6 days (95% credibility interval, CrI: 1.4–3.1) and an effective reproduction number Re of 0.23 (95% CrI: 0.05–0.47) for the first wave, 0.16 (95% CrI: 0.01–0.41) for the second wave, and 0.16 (95% CrI: 0.01–0.45) for the third wave without a significant difference between waves. There was a significant decrease in the incidence of H7N9 cases after live poultry market closures in various major cities. Our analytic framework can be used for continued assessment of the risk of human to human transmission of A(H7N9) virus as human infections continue to occur in China.

The effects of closure to live poultry markets on Avian influenza A (H7N9) epidemics in China

Since March 2013, China had experienced five seasonal epidemics related to Avian influenza A (H7N9). An unprecedented outbreak of H7N9 epidemic started from September 2016, with 730 cases reported till June 30(th) 2017, in mainland China that caused profound influences on both social development and health of the people. As an emerging infectious disease, information on pathogenic characteristics, transmission patterns and other epidemiological features of H7N9 virus somehow remained unclear. Data from previous studies suggested that the live poultry market (LPM) seemed to have served as main places where H7N9 virus got originated, mutated, spread and thus infected the human beings. Hence, closure of LPMs was suggested a major measure to control and prevent H7N9 epidemics in China. However, the effectiveness of different ways of LPM closures on H7N9 epidemics had been controversial. This study systemically summarized the effects of different ways of LPM closures on H7N epidemics from previous studies, aiming to provide references for developing a better program on H7N9 control and prevention in the country.

Sudden increase in human infection with avian influenza A(H7N9) virus in China, September-December 2016.

Since the first outbreak of avian influenza A(H7N9) virus in humans was identified in 2013, there have been five seasonal epidemics observed in China. An earlier start and a steep increase in the number of humans infected with H7N9 virus was observed between September and December 2016, raising great public concern in domestic and international societies. The epidemiological characteristics of the recently reported confirmed H7N9 cases were analysed. The results suggested that although more cases were reported recently, most cases in the fifth epidemic were still highly sporadically distributed without any epidemiology links; the main characteristics remained unchanged and the genetic characteristics of virus strains that were isolated in this epidemic remained similar to earlier epidemics. Interventions included live poultry market closures in several cities that reported more H7N9 cases recently.

Sustained live poultry market surveillance contributes to early warnings for human infection with avian influenza viruses

Sporadic human infections with the highly pathogenic avian influenza (HPAI) A (H5N6) virus have been reported in different provinces in China since April 2014. From June 2015 to January 2016, routine live poultry market (LPM) surveillance was conducted in Shenzhen, Guangdong Province. H5N6 viruses were not detected until November 2015. The H5N6 virus-positive rate increased markedly beginning in December 2015, and viruses were detected in LPMs in all districts of the city. Coincidently, two human cases with histories of poultry exposure developed symptoms and were diagnosed as H5N6-positive in Shenzhen during late December 2015 and early January 2016. Similar viruses were identified in environmental samples collected in the LPMs and the patients. In contrast to previously reported H5N6 viruses, viruses with six internal genes derived from the H9N2 or H7N9 viruses were detected in the present study. The increased H5N6 virus-positive rate in the LPMs and the subsequent human infections demonstrated that sustained LPM surveillance for avian influenza viruses provides an early warning for human infections. Interventions, such as LPM closures, should be immediately implemented to reduce the risk of human infection with the H5N6 virus when the virus is widely detected during LPM surveillance.Emerging Microbes & Infections (2016) 5, e79; doi:10.1038/emi.2016.75; published online 3 August 2016

Effects of closing and reopening live poultry markets on the epidemic of human infection with avian influenza A virus.

Live poultry markets (LPMs) are crucial places for human infection of influenza A (H7N9 virus). In Yangtze River Delta, LPMs were closed after the outbreak of human infection with avian influenza A (H7N9) virus, and then reopened when no case was found. Our purpose was to quantify the effect of LPMs’ operations in this region on the transmission of influenza A (H7N9) virus. We obtained information about dates of symptom onset and locations for all human influenza A (H7N9) cases reported from Shanghai, Jiangsu and Zhejiang provinces by May 31, 2014, and acquired dates of closures and reopening of LPMs from official media. A two-phase Bayesian model was fitted by Markov Chain Monte Carlo methods to process the spatial and temporal influence of human cases. A total of 235 cases of influenza A (H7N9) were confirmed in Shanghai, Jiangsu and Zhejiang by May 31, 2014. Using these data, our analysis showed that, after LPM closures, the influenza A (H7N9) outbreak disappeared within two weeks in Shanghai, one week in Jiangsu, and one week in Zhejiang, respectively. Local authorities reopened LPMs when there was no outbreak of influenza A (H7N9), which did not lead to reemergence of human influenza A (H7N9). LPM closures were effective in controlling the H7N9 outbreak. Reopening of LPM in summer did not increase the risk of human infection with H7N9. Our findings showed that LPMs should be closed immediately in areas where the H7N9 virus is confirmed in LPM. When there is no outbreak of H7N9 virus, LPMs can be reopened to satisfy the Chinese traditional culture of buying live poultry. In the long term, local authorities should take a cautious attitude in permanent LPM closure.

Surveillance of Avian H7N9 Virus in Various Environments of Zhejiang Province, China before and after Live Poultry Markets Were Closed in 2013-2014.

BackgroundTo date, there have been a total of 637 laboratory-confirmed cases of human infection with avian influenza A (H7N9) virus across mainland China, with 28% (179/637) of these reported in Zhejiang Province. Surveillance of avian H7N9 virus was conducted to investigate environmental contamination during H7N9 outbreaks. We sought to evaluate the prevalence of H7N9 in the environment, and the effects of poultry market closures on the incidence of human H7N9 cases.MethodsWe collected 6740 environmental samples from 751 sampling sites across 11 cities of Zhejiang Province (China) between January 2013 and March 2014. The presence of H7N9 was determined by reverse transcription polymerase chain reaction, with prevalence compared between sites and over time. The relationship between environmental contamination and human cases of H7N9 infection were analyzed using Spearman’s ranked correlation coefficient.ResultsOf the 6740 samples, 10.09% (680/6740) were H7N9-positive. The virus was found to circulate seasonally, and peaked during the spring and winter of 2013–2014. The prevalence of the virus decreased from the north to the southeast of the province, coinciding with the geographical distribution of human H7N9 cases. Compared with other sampling sites, live poultry markets (LPMs) had the highest prevalence of H7N9 virus at 13.94% (667/4784). Of the various sample types analyzed, virus prevalence was highest for chopping board swabs at 15.49% (110/710). The prevalence of the virus in the environment positively correlated with the incidence of human H7N9 cases (r2 = 0.498; P < 0.01). Cities with a higher incidence of human H7N9 cases also had a higher prevalence of H7N9 among samples and at sampling sites. Following the closure of LPMs at the end of January 2014, the prevalence of H7N9 decreased from 19.18% (487/2539) to 6.92% (79/1141). This corresponded with a decrease in the number of human H7N9 cases reported.ConclusionsThe prevalence of H7N9 virus in environmental samples oscillated seasonally, regardless of whether LPMs were open. The presence of H7N9 in environmental samples positively correlated with the number of human H7N9 cases, indicating that eradication of the virus from the environment is essential in reducing the numbers of H7N9 cases and halting the spread of the virus.

Public risk perception and attitudes towards live poultry markets before and after their closure due to influenza A(H7N9), Hong Kong, January-February 2014.

The study investigated public risk perception regarding influenza A(H7N9) and attitudes towards closure of live poultry markets (LPMs) before and after LPMs closed in Hong Kong. Two population-based surveys were conducted before and after LPMs closed in January-February 2014, respectively. Adults were recruited using random digital dialing. In total, 670 and 1011 respondents completed the survey before and after closure of LPMs, respectively. Perceived susceptibility to H7N9 infection was low across surveys. Among respondents who completed the survey after LPMs closed, only 14.6% agreed that temporary closure of LPMs caused inconvenience to the daily life; 38.7% valued the Chinese tradition of live poultry consumption more than controlling the risk of avian influenza; 54.6% recognized greater risk of influenza epidemic associated with LPMs. Support for permanent closure of LPMs which was comparably low across surveys was strongly associated with perceived risk of avian influenza related to LPMs, the effectiveness of LPM closure in control of avian influenza and the inconvenience caused by closure. Risk communication that promotes people's perceived risk of avian influenza associated with LPMs and the effectiveness of LPM closure in control of avian influenza outbreaks may improve support for permanent closure of LPMs.

Use of National Pneumonia Surveillance to Describe Influenza A(H7N9) Virus Epidemiology, China, 2004–2013

In mainland China, most avian influenza A(H7N9) cases in the spring of 2013 were reported through the pneumonia of unknown etiology (PUE) surveillance system. To understand the role of possible underreporting and surveillance bias in assessing the epidemiology of subtype H7N9 cases and the effect of live-poultry market closures, we examined all PUE cases reported from 2004 through May 3, 2013. Historically, the PUE system was underused, reporting was inconsistent, and PUE reporting was biased toward A(H7N9)-affected provinces, with sparse data from unaffected provinces; however, we found no evidence that the older ages of persons with A(H7N9) resulted from surveillance bias. The absolute number and the proportion of PUE cases confirmed to be A(H7N9) declined after live-poultry market closures (p<0.001), indicating that market closures might have positively affected outbreak control. In China, PUE surveillance needs to be improved.

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

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. 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. 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). 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. 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.

Can closure of live poultry markets halt the spread of H7N9?

After isolation of avian influenza A H7N9 virus from live poultry markets (LPMs), and reports that several people who were infected with the virus had visited such markets a few days before disease onset, LPMs were suspected to be a main source of human exposure to H7N9 in China.1 After LPM closure was enforced in several Chinese cities, the incidence of H7N9 human cases rapidly reduced.2 In The Lancet, Hongjie Yu and colleagues3 quantify the risk of human infections before and after LPM closure in the Chinese cities of Nanjing, Shanghai, Hangzhou, and Huzhou.