African swine fever (ASF) is a contagious and lethal hemorrhagic disease with a case fatality rate approaching 100% in domestic pigs (1). The disease causes huge economic losses to the pig industry and threatens food security around the world, and is classified as a notifiable disease by the World Organization for Animal Health (OIE). (2, 3). ASF has been endemic in most sub-Saharan African countries and has emerged in the Caucasus and some areas of Europe (4, 5). In Asia, the first case was reported in the northeast of China in August 2018, and then the virus was quickly spread to other countries in Asia, including Vietnam (6–8). In Vietnam, ASF outbreaks were first reported in February 2019 in Hung Yen province (250 km from the Chinese border and 50 km from Hanoi) and have rapidly spread across the entire county within a short period of time. As of Dec 2021, more than 6 million (>20% of pig production) have died and been culled across the country (7). Poor biosecurity (mainly smallholders, accounting for 65–70%) was one of the main risk factors to the rapid spread of ASF at the farm level, resulting in a huge economic impact for the pig industry in Vietnam (9, 10).

Cluster analysis is an important analytic technique in spatial or spatial-temporal epidemiology. It can detect space, time and space-time clusters of disease cases resulting from disease outbreaks. Together with remote sensing data, it is becoming popular to address the research questions in veterinary medicine (11, 12). In Vietnam, some studies have been carried out to identify the space-time clusters of Porcine reproductive and respiratory syndrome (PRRS) and Foot-and-mouth disease (FMD) (13, 14), and to estimate the spatial distribution of Culex mosquito abundance using remote sensing data (15). In addition, value chain assessment (VCA) is a systematic framework for describing and analyzing the inter-connected activities that transport a raw product from the producers to the final consumer (16, 17). The VCA can help us to develop cost-effective intervention strategies for the pig production system. In Vietnam, a few studies have been conducted in the livestock sector (mainly pig) (18–20).

To our knowledge, no studies have been conducted to evaluate the occurrence of ASF in space and time and to identify the potential risk factors. Therefore, the main objectives of this study were to describe the spatiotemporal analysis as well as to assess the potential risk factors along the pig value chain in Lao Cai province, Vietnam.

This research was the first attempt to assess the spatiotemporal analysis of ASF using local surveillance and remote sensing data, as well as to evaluate the risk factors in the pig value chain in Lao Cai, Vietnam. It was possible that ASF cases in the local surveillance system were likely to be underestimated because small-scale farms (accounting for 65−70% of the pig population in Vietnam) lacked knowledge about livestock diseases (including ASF) and were less reachable to veterinarians and animal health workers. Moreover, all pigs must be slaughtered when a new case is confirmed on the farm, which may have resulted in reluctance for reporting.

The primary, secondary and fifth clusters were observed near the Chinese border, which might be highly associated with the illegal movements between Chinese borders as the first ASF case was reported in China (6) and rapidly spread to other countries in Asia, including Vietnam (7). It was assumed that the ASF virus was transmitted through pig movements and pork products or infected fomite (29). One study found that the strain of the ASF virus in Vietnam was the same strain as the circulating virus in China (8). In addition, it showed similar outbreak patterns of the highly pathogenic porcine reproductive and respiratory syndrome (HP-PRRS) in 2007 (30). The HP-PRRS outbreak was first detected in China, then quickly jumped in Vietnam and other Southeast Asian countries (31, 32).

Our study found that the distance to the road and elevation were reversely associated with the ASF outbreaks, which was consistent with previous studies (25, 26). Actually, unregulated slaughtering and the proximity of pig slaughterhouses to the main road is common in Vietnam (33). In addition, it is possible that farms at low elevation have better accessibility for human movement (e.g., traders and feed companies), resulting in an increased risk of ASF.

Since the first case of ASF was detected in northern Vietnam in February 2019, the number of affected provinces rapidly were increased within a short period of time (<4–5 months). Some potential risk factors have been proposed, such as illegal trading activities; low biosecurity; feeding of food scraps to pigs; not fully culling all pigs in infected farms, disposal of pig carcasses to public areas. Moreover, increased human and animal movements during the Tet holiday (Vietnamese New Year in late January or early February) may have played a significant role in spreading the ASF virus across the country.

It has been well recognized that wild boars and soft tickets can play a significant role in the transmission of the virus (34–36). In Asia, ASF in wild boars has been detected in China and South Korea (37–39). However, no studies have been implemented to evaluate the possible roles of wild boars and soft tickets for spreading a virus among farms in Vietnam. Especially, Lao Cai province is a mountainous region that may provide favorable conditions for wild boar habitats. Therefore, more research is necessary to assess the main transmission route of the ASF virus at the farm level.

Our research had some limitations in that it was likely that ASF surveillance data were underreported due to lack of awareness, animal health professionals and laboratory facilities in rural and mountainous areas. Especially, farmers were reluctant to report to the authorities because of low compensation rates and complicated/prolonged administrator procedures. In addition, it was assumed that the pig population did not rapidly change during the research period, which is very important for a space-time permutation model. Therefore, it was possible that our detected clusters may have been affected by the pig population at risk if the background population dramatically increased or decreased in one area compared to another.

During the stakeholder feedback workshop, participants discussed the risk factors for ASF transmission, especially the differences in risk levels between commercial farms and household farms. Although the risk of disease on any farm was tied to many factors, the human risk factors were lower on commercial farms because most of them applied high biosecurity procedures. In addition, they did not allow visitors, including traders, into the barn areas. However, for small-scale producers, the human movement was one of the most important risk factors as they applied fewer biosecurity practices and did not control their neighbors or traders who may move in and out of the production areas, which was consistent with a previous study (9). Mostly, livestock farmers considered producers to be high-risk actors as they visited many places, however, they rarely entered the pig stables of other farmers.

According to the interviewed pig producers, the greatest difficulties for restocking pig herds after ASF outbreaks on the farms and in the region were concerns about re-infection with ASF, high cost of breeding pigs and lack of capital for both household and commercial farms. In addition, for household farms, access to breeding pigs with known origin was also difficult. Restocking of breeding sows was slow due to difficulties in purchasing quality breeds, especially exotic breeds. Restocking fatteners was also slow due to the high price of commercial piglets. ASF outbreak reoccurred in the province in February 2020 and continued to spread across the province. However, large numbers of households still did not have a deep understanding of diseases and biosecurity. Currently, the majority of people believe that any sickness or death among pigs is caused by ASF, causing farmers to be hesitant about restocking.

Among the technical solutions discussed, both commercial and household pig producers considered minimizing the number of people going in and out of pig stables and improving healthcare and husbandry procedures to be both very important and feasible. The interviewees addressed the other most important practices were strengthening decontamination and disinfection (using lime and hormones with higher frequency), disinfection of transport vehicles and killing of mice, flies and mosquitoes. These solutions were also considered highly feasible for adoption on the ground. As for appropriate policies to overcome ASF, household farms suggested that they would expect compensation or support when their pigs are depopulated due to ASF, as well as support for purchasing disinfectants. In addition, the commercial farms expected support for purchasing disinfectants, farm materials and equipment. The priority for training needs in the context of ASF is quite similar between households and commercial farms. These include the detection and recognition of ASF and emerging diseases; understanding the risks of ASF infection and how to prevent it; training on breeds and controlled breeding practices; safe artificial insemination practices; and technical knowledge of sanitary and disease-free pig housing.

There was a high risk of ASF transmission from traders in the pig value chain, including collectors, slaughterers and retailers at the provincial, district and commune levels. These actors all participated in the sale and purchase of pigs that could be infected. Furthermore, live pigs and pork products were not subject to quarantine within the province, and their movement was not controlled. In addition, when an epidemic occurred, it took a long time to identify the disease due to the lack of resources and capacity among local animal husbandry actors and the inability to analyse samples locally for detecting the ASF virus. This allowed time for pathogens to spread through transportation and sales of sick pigs. Every year, Sub- DAH officers have been trained in disease prevention, control and surveillance. However, in-depth professional knowledge was still lacking. At the district level, some stations lack livestock and animal health specialized staff. In some districts, the specialized veterinary staff they have were sent to work other jobs. The veterinary officers at the provincial and district levels have limited resources and capacity for monitoring and surveillance of ASF. There is a need for compliance by all pig producers and other actors in the pig value chain to adopt biosecurity practices. Therefore, awareness, knowledge and understanding of infection and risks of ASF need to be improved. Veterinary officials at the provincial and district levels need to improve capacity and resources to perform laboratory analysis for ASF and need to coordinate with local actors on the control and prevention of ASF in the community.

The raw data supporting the conclusions of this article will be made available by the authors, without undue reservation.

The studies involving human participants were reviewed and approved by Hanoi University of Public Health. The patients/participants provided their written informed consent to participate in this study. The animal study was reviewed and approved by Hanoi University of Public Health.

HL designed and ran the statistical analyses, wrote the draft of the manuscript, and prepared all the figures and tables presented. TD and LH collected the data. All authors contributed to the conception and design of this study and editing and comprehensive revision of this manuscript.

This study was funded by the CGIAR Research Program on Livestock.

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

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