International Trades of Pigs and Pork Products Accelerate the Global Spread of African Swine Fever

Background: The global spread of African swine fever (ASF) has affected nearly half of the world pork market and caused great economic loss. Current studies have identified fairly complex transmission routes of this infectious disease. However, some evidences indicate that international trade of domestic pigs and their products may be another important factor facilitating the spatial spread of ASFV, but studies targeting the impact of international trade worldwide are limited. Methods: To investigate the possible global spreading routes of ASF, the nearest neighbor approach (NNA) was applied. Phylogenetic analyses based on all the publicly available ASFV DNA sequences were further conducted to estimate the genetic homology of sequences isolated in different countries. To evaluate the impacts of environmental conditions and human activities on ASF epidemics and to identify high-risk regions, we used ecological niche model (ENM). To simulate the global diffusion of AFSV facilitated by the international trade of domestic pigs and products, we constructed Susceptible-Infectious (S-I) epidemiological metapopulation models. Findings: We identified 24 genotypes and estimated the global spreading patterns of ASFV using NNA method. ASFV spread from Southern Africa to Eastern Europe and then most likely spread from Russia to China and Mongolia. According to the results of ENMs, the spreading cycle of ASFV could be divided into spreading via human transportation, such as trading of domestic pigs or pork, and spreading via natural processes, such as in wild boar populations. Furthermore, the established epidemiological metapopulation models showed that some countries, regardless of their geographic distance, shared similar changing patterns of yearly transmission rate over time, indicated that the international transportation and trades of live pigs and products may synchronize the ASF epidemics in countries with trade exchanges. Interpretation: The international trades of pigs and products probably accelerated the global spread of ASFV among domestic pigs. In dealing with ongoing and future epidemics, an understanding of both the conditions favorable for ASFV and the mechanism of its transmission dynamics will help policy-makers to take effective prevention and control measures. Funding Statement: This work was supported by Grants from the National Key R&D Program of China5 (No: 2018YFC0840402, 2016YFA0600104), Research Project of African Swine Fever of Chinese Academy of Sciences (No: KJZD-SW-L06-02), and donations from Delos Living LLC and the Cyrus Tang Foundation to Tsinghua University. Bo Xu was also partially supported by Scholarship of China Scholarship Council. W.L. is the principal investigator of the Innovative Research Group of the National Natural Science Foundation of China (Grant No. 81621091). J.L. is supported by Youth Innovation Promotion Association of CAS (2019091). Declaration of Interests: All authors declare that they have no conflict of interest. Ethics Approval Statement: Not required.