This is the first study compared the effectiveness of LPMs closure in cities that implemented the various scale and duration measure from first to fifth epidemics waves, for preventing human exposure to avian influenza H7N9 virus. Our study suggests that long-termed and fully closed such as Shanghai and Shenzhen (last two waves) have a most significant effect, while short-term closure has a limited effect such as Guangzhou, but partly closed even if long-termed closure was not significant such as Hangzhou and Suzhou. The results of classification tree analysis suggest that LPMs closure rather than environmental factors had the predominant role in reducing incidence for Shanghai and Shenzhen, which substantially controlled the H7N9 virus exposure to human.
How does the scope of LPMs closure affect? Yu and colleagues demonstrated that closure of LPMs in four cities reduced the risk of human infections by 97%-99% in June of 2013. It has indicated that LPMs closures were effective in controlling the human risk of H7N9 infection at that early time of H7N9 outbreak. But their study suggested that LPMs closure should be sustained in at-risk areas and implemented in any urban areas. Our study’s results of Hangzhou and Suzhou city indicated if only urban area implemented the LPMs closure would not be effective to reduce the risk for human H7N9 infected, may due to the people who have the habit of eating live poultry are still willing to the suburb or rural area to purchase the live poultry. In one investigated study convincingly demonstrated this fact that all respondents were asked about, without consideration of other factors, which type of the chicken they preferred most among the four types of chicken (i.e. live, freshly slaughtered, chilled or frozen). A significant portion of 47% of respondents indicated that they preferred live chicken above other forms of chicken, while 32% expressed “indifferent”. Live poultry is a necessity for many residents and related workers, that may explain why partial closure does not cause have an ideal controlling consequent. The separate area to conducted LPMs closure in a city cannot really block the exposure of live poultry.
How does the duration of LPMs closure affect? Many published studies agreed that the government would play a crucial role to implement the policy of LPMs closure timely once a confirmed case has occurred in this city. Some even suggested that LPMs should be closed immediately in areas where H7N9 virus is detected in LPMs. From a public health standpoint, LPMs should remain closed in all affected areas until the current influenza A(H7N9) epizootic and epidemic are declared definitively over by national authorities. Moreover, one study suggested that A(H7N9) virus activity peaked around March in both retail and wholesale LPMs, while A(H5N1) virus peaked around in December to January in China. Based on the evidence of our results, control measures (e.g. LPMs all closure) for avoiding exposure from live poultry to human and surveillance in LPMs should be maintained over spring.
We adjusted the influence of meteorological factors in generalized linear regression, and added temperature and relative humidity as predictors in the regression tree because meteorological factors are also one of the factors that affect the incidence of H7N9. Previous studies have indicated that odds ratio of precipitation (49.19-115.60 mm), sunshine (22-9.25h), temperature (<9.33 °C)  and wind speed (2.1-3.0 m/s or 6.3-7.1 m/s)  was statistically significant for H7N9 incidence. Both daily minimum and daily maximum temperature contributed significantly to human infection with the influenza A H7N9 virus, and the temperature range is similar to our study. Other study shown the risky windows of H7N9 infection were different in the northern and southern areas. This point is consistent with our study. The temperature and humidity ranges that increase the risk of H7N9 vary from city to city.
However, Whether LPMs can be reopened to satisfy the Chinese tradition of buying live poultry when there is no H7N9 outbreak, this issue is still worth discussing. Related study demonstrated the poultry industry loosed amounted to ¥7.75 billion (USD$1.24 billion) in 10 affected provinces and ¥3.68 billion (USD$0.59 billion) in eight non-affected adjacent provinces in only three months from March to May, 2013, included cost of poultry slaughter, cost of closing LPMs, cost of live poultry sales and cost of market-stall leases. After the H7N9 outbreak in whole of China, reduced to 6% of the household had experience of purchasing poultry. Meanwhile, the proportion of direct medical losses and DALYs losses in the estimate of H7N9 burden was small, but the medical costs per case were extremely high (mean cost for each patient was ¥10 117 (USD$1619) for mild patients, and ¥205 976 (USD$32 956) for severe cases with death).
Besides the serious agriculture losses, the effectiveness of LPMs needs further evaluation. One field study demonstrated that during the closure, H7N9 viral RNA detection and isolation rates in retail markets decreased by 79% and 92%, respectively. However, viable H7N9 virus could be cultured from wastewater samples collected up to 2 days after the market closure began. Overall, LPMs reopen and temporary interventions cannot completely halt A(H7N9) virus persistence and dissemination. In order to balance the interests of agriculture economics and public health, government encourages residence purchase chilled chicken instead of live poultry. Chilled chickens are slaughtered and packaged chicken stored at between 0°C and 4°C after going through a chilling process and has a shelf-life of 5-7 days, which can highly reduce the risk of virus transmission from live poultry to human. Since the outbreaks of H7N9, many cities that reported the cases have launched a pilot program (named “Centralized Slaughtering, Cold Chain Delivery, Chilled Poultry Supply”) in designated areas, such as 2013 in Shanghai, 2014 in Guangzhou and Shenzhen. Furthermore, the long-lasting circulation of the H7N9 virus in market poultry has often preceded the emergence of H7N9 outbreaks. Based on the above considerations, on 1st June 2016, Shenzhen was the first city in China implemented the LPMs all closure in the whole city and sold chilled poultry instead of live poultry in urban and suburb areas. This policy of live poultry ban in the whole city can prevent any type of avian influenza not only H7N9. It is an optimal measure with long-term effectiveness to block the avian infected virus transmit to human, our results proved that as well.
Furthermore, in September 2017, an H5/H7 bivalent inactivated vaccine for chickens was introduced, and the H7N9 virus isolation rate in poultry dropped by 93.3% after vaccination. Only three H7N9 human cases were reported between October 1, 2017 and September 30, 2018 (the sixth epidemics period), indicating that vaccination of poultry successfully eliminated human infection with H7N9 virus. Recently, however, there are thousands of pneumonia patients in Wuhan, a city in central China. The symptoms are very similar to SARS in 2013. A Novel coronavirus was isolated from the patients which denoted 2019-nCoV by the WHO. At first, the common point of the sick patients was that they had been to the Huanan Seafood Wholesale Market in Wuhan, which also sold live wild animals. This market was later identified as the center of a respiratory illness outbreak by health authorities. This incident further reminds us that the sale of live wild animals or poultry and animals poses a great threat to public health.
Our study has some limitations. As an ecologic study, our findings might be affected by other potential confounding (e.g., human movement etc.). If we were able to collect the samples from the environment around the live poultry markets to detect the positive rate of virus of LPMs in every city, it can be a piece of strong evidence to support our results. Despite poultry immunity has been controlled, it does not rule out that the evolutionary genes transmit into human beings or emerge other types of avian influenza. It is necessary to adopt long-term, large-scale LPMs closure or even permanent ban on the sale of live poultry and wild animal in high-risk area and densely populated cities.