One Year of African Swine Fever Outbreak in China

Background: African swine fever (ASF) is a major threat to domestic pigs and wild boars. Since 2018, ASF outbreak has been ongoing in China. As of August 3, 2019, a total of 151 ASF outbreaks reported in China have caused severe economic losses for many pig farmers and pork producers. The present study is to analyze the epidemiologic characteristics of ASF outbreak that occurred in several regions across China during the period August 2018- August 2019. Particularly focusing on the epidemic distribution, main transmission routes, incidence/fatality, impact on pig production capacity, and the main preventive measures adopting to mitigate the risk of ASF spread in pig farming systems by Chinese government. Results: The data show that the importance of seasonality effect, spatial distribution and the anthropogenic factors on the transmission of ASF, and further suggest that effective ASF risk management in China will require a comprehensive and integrated approach linking science and policy and will need to involve all relevant stakeholders to develop realistic policies. Conclusions: This provides an improved scientic basis to optimize current interventions as well as develop new tools and strategies to reduce the risk of African swine fever virus (ASFV) transmission to domestic pigs and wild boars. ASF cases/numbers of susceptible animals/K, and generally fatality rate = numbers of deaths/numbers of animals suffering from ASF infection/K, K = 100%.


Background
African swine fever (ASF) is a highly contagious disease that currently has no great economic losses to animal husbandry economy. Since ASF was rst identi ed in Kenya in the 1921, 68 countries have suffered from ASF at present [1,2]. Especially, more than 3900 ASF epidemics were reported worldwide merely in 2018 with the numbers of cases having increased by 25% compared to that of 2017 [3]. Most of concern is that ASF outbreaks have reemerged in some countries such as Hungary, Bulgaria and Belgium 30 years after eradication [4]. More than that ASF outbreaks have occurred in Mongolia and Vietnam along the border of China in 2019 [5,6]. Since the con rmation of the ASF entered China in August 3 2018, a total of 151 ASF outbreaks have been reported in 31 provinces as of August 3, 2019. The experiences in a variety of prevention and surveillance measures against ASF indicate that it is di cult to eradicate ASF in a short period once outbreak [7,8]. The disease can have great impact on global trade of pigs and pork products which threaten the global food security [9]. This study focuses on the characteristics of ASF outbreak that occurred in the infected regions in China one year on. This work presents ASF risk zones in China and may provide useful information for the development of effective strategies for the prevention and control of ASF outbreak. Furthermore, the data will bene t to assess the potential public health risks posed by ASFV infections.

Geographical distribution of ASF outbreak in China
Outbreak analysis of geographical distribution showed that since August 3, 2018, the rst ASF outbreak occurred in Shenyang in China, ASF continued spreading among domestic pigs and wild boars in country. As of August 3, 2019, almost geographical regions total of 31 provinces in China have reported ASF outbreaks except Hong Kong, Macao, and Taiwan ( Figure 1A). Outbreak rates of ASF in each province are shown in Figure 1B and Table 1. Apparently, the Liaoning province has the largest cumulative ASF outbreaks, showing 13.9% of cases (21/151), followed by Guizhou with 6.6% (10/151), Anhui and Guangxi both with 5.9%(9/151), subsequently, Hunan, Hubei and Sichuan at 5.2% (8/151), and the other 24 provinces, this ratio is between 4.6-0.6%. Comparison the epidemic tendency among provinces showed that the spread of ASF outbreaks mainly located along the Northeast, Eastern China, and then reached Southern and Southwest, showing an increasing southward in general. Notably, Xinjiang, Tibet and Hainan, were con rmed ASF for the rst time in April 2019. Nine months had elapsed since the rst ASF outbreak had occurred in China in August 2018 (Appendix Table 1). In this regard, preliminary speculation is that Xinjiang, Tibet and Hainan, different from Eastern China and other areas, of geographical locations are far away from major economic transport routes and of population densities are at a relatively low level, slowing down the spread of ASF. In addition, Xinjiang and Tibet are the major residential areas of ethnic minorities [10]. The consumptions of beef and mutton occupy the major part of the market because of religious practices [11].Therefore, the impacts of ASF on these regions are relatively delayed.  Figure   2A,Table2).Which of them are also the main residential areas of Hui nationals in China [10]. Thus, live pig stocks and pork consumption are keeping at relatively lower level because of religious practice , and then reducing the number of susceptible pigs [11]. In brief, the spread of the ASF epidemics are associated with anthropogenic factors, such as trade of animals, processed meat products and ethnic culture.

The incidence and fatality in different regions of China
This comprehensive analysis has highlighted that in one year period, Shandong province reported 17 infected pigs, substantially fewer than the 5123 infected cases reported in Heilongjiang province, followed by Jiangsu with 3079 cases and Liaoning with 2378 cases. Similarly, the provinces with the highest number of dead pigs are Heilongjiang (4158). Liaoning (2087) and Jiangsu (1466). The lowest number of dead pigs is only 3 in Shandong (Figure1 A, Figure   2B, Table 2). However, it is worth noting that the highest fatality rate of 97.6%(204/209) is in Jilin province, followed by Tibet with 91.7%(55/60). The previous provinces of Heilongjiang, Jiangsu and Liaoning, in which there are the maximum cumulative cases of infected and dead pigs, conversely, showing fatality rates with 81.2%(4128/5123), 47.6%(1466/3079), and 87.8%(2087/2378) respectively ( Figure 2B, Table2). Meanwhile, as for incidence, Gansu province has the highest pig incidence rate of 62.5%(187/299), followed by Tibet and Qinghai with the incidence values are 46.5%(60/129) and 45.5%(46/101) respectively. These indicate that there is no consistent tendency between the incidence and fatality ( Figure 2B, Table2). For this, it seems that the appropriate prevention and control measures applied in time are fully effective in protecting against ASFV incursion and decreasing the fatality rate.
Characteristics of ASF epidemic in suburban and rural areas As shown in Figure 3A-3B, the pig numbers of susceptibility, incidence and death in rural areas exceed that of in suburban areas. This can partly be explained that most of commercial pig farms are mainly located in the urban suburbs, they can effectively control the ASF epidemics together with higher level biosecurity and various management measures [12,13]. Meanwhile, the majority of backyard pig farms with either a low or very low biosecurity level are scattered, correspondingly, the management measures of various norms are relatively primitive resulting in a delayed response to the epidemic, which increases the pig numbers of susceptibility, incidence and death.
It is generally assumed that low level biosecurity farms are at higher risk of introduction the infections. Also, we note that the pig numbers of susceptibility, incidence and death showed an "explosive" increase during the December 2018-February 2019, reaching the peak in January 2019. Despite a small increase during September 2018-November 2018( Figure 3A-3B, Table3). This is likely the result to coincide with the Chinese New Year, which stimulated the nationwide trades of animals and processed meat products due to an increased demand for various pork products across the country, accelerating the incursion of ASFV and the frequency of ASF outbreaks. And subsequently, the pig numbers of susceptibility, incidence and death varied between different month together with a decreasing trend in general during the period March 2019-August 2019 ( Figure 3A-3B, Table3), although there were marginal uctuations within some months.

Discussion
Due to the ASF epidemic, ever since the second half of 2018, the swine industry in China, especially the basic production capacity has been declining [14]. Moreover, as seen in January 2019, compared with the same period last year, the stocks of both live pigs and sows have signi cantly reduced reaching the lowest level in the decade. This to the same extent will affect the supply of pork in the market mostly during the second half of the year. It is expected that there will be a large increase in the price of pigs after the third quarter, particularly in the fourth quarter [14]. Additionally, several other factors in uence domestic pig production. Firstly, the uncertainty about the epidemic situation results in farmers and breeding enterprises giving up increasing the number of live pigs in stock, where epidemics have occurred. Secondly, because of the in uence of economic factors, pig farmers experience nancial di culties, consequently, they have to adjust or reduce their production capacity in some areas. Finally, the Chinese swine industries are being transformed and upgraded, some free-range farmers have gradually withdrawn from the industry during the outbreak of ASF [13]. To sum up, these factors are also accountable for the current decline in the pig production capacity.
After the outbreak of ASF, the MARA of China has issued several policies and regulations to prevent and control ASF outbreak. Firstly, more stringent surveillances, monitoring programs and enhancing the ful llment of legal requirements on biosecurity have been established for early detection and eradication of ASF.Currently, all 151 cases have been effectively dealt in time and no secondary spread occurred, with 90% of the affected areas have been identi ed to lift the blockade according to relevant regulation [15]. Additionally, the off-site transportation of live pigs is an important factor contributing to the spread of ASF. Therefore, the MARA of China has strengthened the supervision and regulation of live pigs transports and their products. Based on the epidemiological information, the proportion of outbreaks has declined around 35-15% at a national level compared to the previous period of ASF outbreaks [15].
Furthermore, among the 151 reports of ASF, 148 of which had been con rmed in domestic pigs and 3 ASF outbreaks were from wild boars (Appendix Table 1). Interestingly, there is no obvious evidence that direct association between domestic herds and wild herds. For this reason, contact between hunters and pig producers may be a major factor causing ASF transmission among them. Besides, another explanation for this might be tick-to-pig transmission. Soft ticks of the genus Ornithodoros have been identi ed as competent vectors of ASFV to domestic pigs [16,17].
Additionally, feeding of contaminated swill has been generally considered one of the main risk factors for indirect transmission of ASFV. Some pig farms especially on backyard farms, the feeding of kitchens leftovers could not be excluded [4,18,19]. Thus, most likely, the virus has entered and affected herds by means of contaminated fomites, clothing, vehicles, feed and bedding material due to inadequate biosecurity measures or errors in the implementation of these measures. Accordingly, the MARA of China has banned feeding food scraps to pigs. By comparison, the proportion of nationwide ASF outbreaks caused by feeding pigs with kitchen scraps has dropped around 50-44% [19,20]. In addition to these measures, the registration of pig transport vehicles, inspection of transportation and regulations for slaughtering pigs have been implemented to combat illegal cross-border movement of pigs or meat.

Conclusion
In summary, the ASF epidemic situation in China can be controlled with the gradual improvement in the prevention and control programs. However, the risk of ASF outbreak and transmission in China is still high. Further strengthened active surveillance is needed to control the transmission and evolution of ASFV. Also, the study is useful to detect trends and to evaluate the impact on the already implemented measures at regional or even at a national level. The control of ASF in China is a challenging and long-lasting battle that needs the participation and coordination of all national and international stakeholders. Particularly on developing models to forecast the epidemiological dynamics of ASF. More broadly, the international community should support research and policy in ASF-free countries that are at risk of exposure to the virus.

Methods
The regional distribution of ASF nationwide

ASF incidence and fatality
Thereafter, the rates of case fatality and incidence for ASF in different provinces were calculated with SPSS 22 by using epidemically and population data sourced from the China MAFA database presented in Appendix Table 1.
Incidence was de ned as numbers of new ASF cases/numbers of susceptible animals/K, and generally fatality rate = numbers of deaths/numbers of animals suffering from ASF infection/K, K = 100%.

Numbers of dead, infected and susceptible pigs in the suburban and rural areas
Similarly, the numbers of dead, infected and susceptible pigs in suburban and rural areas in China were calculated with SPSS 22, respectively. The time range was from August 2018 to August 2019; the retrospective analysis metrics was space-time; and the maximum temporal cluster size was one month.     The distribution characteristics of ASF outbreak in China in one year. (A)The cartographical analysis of the ASF outbreaks was performed using the geographic information system ArcGIS ArcMap 10.6.3 based on Appendix Table 1.
The yellow color represents the cumulative number of death cases in each province. The shades of red color on the map vary with the number of infected cases. (B)The percentage of ASF outbreaks in different provinces in China. Different color represents the percentage of ASF outbreaks for each province.

Figure 2
The characteristics of incidence, fatality and the number of susceptible pigs for ASF in China in one year. (A)The cumulative numbers of susceptible pigs in different provinces by using epidemiology and population data sourced from the China MAFA database presented in Appendix Table 1 and Table 2