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Early‐phase risk assessments during the first epidemic year of African swine fever outbreaks in Vietnamese pigs

Abstract Background African swine fever (ASF) is a notifiable viral disease of pigs and wild boars that could lead to serious economic losses for the swine industry. Objectives The aim of this study was to identify risk factors in the early phase of ASF outbreaks in Vietnamese swine herds during the first epidemic year. Methods The period of interest for this case–control study was February to July 2019. A questionnaire was administered in northern Vietnam where all early cases of ASF were reported. Producers of herds with reported cases were asked to provide information starting from the day of onset of clinical signs as well as 30 days prior to that day. The period of interest for controls was within the 6 months of the first outbreak in Vietnam (February 2019). Questionnaires included 55 questions; responses were received from 67 cases and 115 controls. Logistic regression analysis was used to identify factors associated with ASF status. Results Thirty‐seven variables of interest (among a total of 55 variables) were associated with ASF status in univariate analysis (p < 0.05). These 37 variables were assessed for inclusion in the multivariate analysis by backward stepwise selection. Six variables remained significant as ASF risk factors in the final model: distance to farm within 500 m, distance of irrigation systems within 200 m, total number of pigs (≤500), absence of dressing rooms for workers/visitors before entering the farm, poor hygienic practices for people within the farm, and poor hygienic practices at pig loading/unloading locations. Conclusions These results may help in understanding the epidemiology of ASF in Vietnam and provide a scientific basis for optimization of current interventions and development of new tools and strategies to reduce transmission of ASF.


INTRODUCTION
African swine fever (ASF) is one of the most complex viral diseases affecting pigs and imposes a significant socio-economic impact because of its high mortality rates approaching 100% (Galindo & Alonso, 2017).
The causative agent of ASF is the ASF virus (ASFV), a large, doublestranded DNA virus and the sole member of the Asfarviridae family (Dixon et al., 2005). ASF was first described in 1909 when the virus infected domestic pigs of European origin in Kenya (Eustace Montgomery, 1921). ASF has since spread to the Iberian Peninsula as well as several European and American countries, mainly through the movement of contaminated meat products .
More recently, in August 2018, ASFV first affected the world's largest pig producer, China. The virus is now spreading in several Asian countries (Blome et al., 2020). No vaccines or therapeutics against ASFV are available. Currently, disease control measures typically include culling large numbers of pigs and strict sanitary measures (Blome et al., 2020).
The continuing spread of ASF and ineffective control measures pose a serious threat to the global pig industry and food security. Each farming system has its own distinct risk factors (Dixon et al., 2019). Therefore, efforts to combat the spread of ASFV will require international cooperation.
Pigs of all ages are susceptible to virulent strains of ASFV (Arias et al., 2018). The virus is present in urine, nasal secretions, saliva, and other excreta. ASFV has complex and diverse transmission modes.
The virus can be spread through direct and indirect contact or via short-distance aerosols. Feed contaminated with the biological fluids of infected pigs has been identified as an efficient mode of viral transmission (Yuan et al., 2020). In addition, direct contact with contaminated surfaces, feed, faeces, or water can indirectly result in pig infection (Olesen et al., 2018). Pigs that recover from ASF infection become clinically healthy virus carriers and may represent sources of new acute infections (Olesen et al., 2018). The role of ticks widely distributed in South America in transmitting the disease to Europe has been confirmed (Pereira De Oliveira et al., 2020). Epidemiological studies of ASF outbreaks in China found that trans-regional transportation of live pigs and pork products, movement of vehicles and people, swill feeding, and human activities all play important roles in the transmission of ASFV (Wu et al., 2020). Poor management and husbandry practices significantly increase the risk of ASFV transmission (Dione et al., 2017).
Pig production is one of the main industries in Vietnam. There are approximately three million households, of which more than 70% were smallholders by small-and medium-sized farms with produc-

Questionnaire
A questionnaire was developed based on known risk factors for ASF and other infectious diseases of pigs described in previous studies (Bisimwa et al., 2021;Cappai et al., 2018;Dione et al., 2017;Mai et al., 2020;Martínez-López et al., 2015;Olesen et al., 2018;Wu et al., 2020) and in consultation with veterinarians involved in the 2019 ASF outbreaks. The questionnaire was pre-tested with five experience veterinarians in the veterinary epidemiology field for the clarity and appropriateness of its content, questions, and responses in terms of the local situation, before the start of the study to ensure that risk factors were appropriate; based on these validation efforts, an additional risk factor (use of transit trucks at the farm gate) was added.
Questionnaires were distributed to veterinarians who were present during the 2019 outbreaks and were involved in the pre-testing. The vehicles. Each category is described in more detail below.
The category of demographic characteristics of pig keepers included four questions regarding number of years spent pig raising, pig husbandry training, primary activity, and veterinary responsibility.
The category of farm location included seven questions related to the farm's proximity to other farms, irrigation systems, main roads, residential area, distances from the barn to the pig loading/unloading location and to the living room, and distance from the isolation barn to the living room.
The category of farm management included 25 questions on farm information such as farm production system (farrow-to-finish; nucleus; farrow-to-wean; and wean-to-finish), breed, total number of pigs, farm status (company or private farm), pig movements (all-in/all-out in each barn; type of pig movement; and separate location for pig movement), type of barn, water source, swill feeding, workers, equipment sharing, manure application, insect nets, fence surrounding the premises, dressing rooms for workers, visitor quarantine for 24 h before entering the farm, wearing of work clothes outside the piggery, and sources of human food.
The category of biosecurity practices and health management included seven questions assessing the disinfection items used by workers (six items), visitors (seven items), and vehicles (11 items The category of contact with people, animals, and vehicles contained three parts and 12 questions focusing on contacts with people, animals, and vehicles.

Statistical analysis
The questionnaire was administered by nine experienced veterinari-  (Whittemore, 1982). Because controls were not matched to cases by location in this study, farm location was treated as a random effect.
TA B L E 1 Demographic characteristics of pig keepers and associations with African swine fever (ASF) outbreak

Number of controls OR (95% CI) p-Value
The number of years in pig raising

Univariate associations
In fact, we got responses more than expected in the study design (60 cases and 60 control farms). Therefore, we included all in the analysis to reduce the bias. A total of 182 swine farms in north Vietnam (115 controls and 67 case farms) were included in this study. Some variables were excluded because we were unable to collect the required data from all respondents. A total of 55 variables were considered as potential risk factors for ASF status. Univariate associations for the five major categories of variables are presented in Tables 1-5. 3.1.1 Demographic characteristics of pig keepers Table 1 shows the relationships between ASF-infected farms and the demographic characteristics of pig keepers. Farms whose operators had more than 10 years of pig raising experience had 2.83 times greater odds of ASF outbreak than those with 5 to 10 years of experience.
Farms where farmers or agro-vet drug store employees were responsible for veterinary care had 5.33 and 5.70 times greater odds of ASF outbreak, respectively, compared with farms where a veterinarian was in charge.

3.1.2
Risks associated with farm location ASF was associated with farms located less than 500, 200, and 200 m from the nearest farm, residential area, and irrigation system, respectively (p < 0.05). We could not get the data from respondents regarding distances from the farm to the nearest farm with an ASF outbreak, forest, slaughterhouse, local market, and refuse dumpsite. Therefore, these variables were excluded from the analysis. In addition, barns that were less than 10 m from the living room were associated with 11.14 times increased odds of ASF outbreak compared with barns more than 50 m from the living room (Table 2). The living room of the workers had a kitchen area that could be related to the risk of ASFV contamination through near distance to the living room by food for workers may include the pork products. Abbreviations: CI, confidence interval; OR, odds ratio. *p < 0.05. These variables were evaluated in multivariate analyses.

3.1.5
Risks associated with people, animal, and vehicle contact Table 5 shows the univariate relationships between ASF-infected farms and people, animal, and vehicle contacts. In farms with ASF outbreaks, the presence of rodents, other animals, and ticks was strongly associated with the presence of ASF (p < 0.001). Vehicle visits to another farm on the same day or trips and high contacts with vehicles (more than six times per month) were also associated with ASF outbreaks (p < 0.05).

Risk factors for ASF outbreaks in multivariate analysis
Among a total of 55 variables, 37 variables of interest were associated with ASF status (p < 0.05) (Tables 1-5). These variables were included in the multivariate model, and backward stepwise selection was performed until the p-values for all remaining variables (by Wald test) were less than 0.05. The results for the final model are shown in Table 6. The multivariate analysis indicated that six variables (two each from the categories of farm location, farm management practices, and biosecurity practices and health management) were strongly associated with ASF outbreaks (p < 0.05) (AIC = 95.4). No multicollinearity and no interactions between variables were detected.

DISCUSSION
In Vietnam, pig production occurs mainly on small-scale farms with unique sociological and cultural practices in the northern part of the country. This study concluded that distance to farm within 500 m, dis-  of cross-contamination from animals, vehicles, and human contacts and movements as well as aerosol transmission. Proximity of farms to irrigation systems also showed a significant positive relationship with ASF outbreak (OR = 2.89). This finding could relate to typical farming practices in Vietnam that takes advantage of proximity to irrigation systems; some farmers have built fishponds next to irrigation systems to simplify adding or draining water for fish culture as required. During the epidemic period, because of a lack of biosecurity awareness, some farmers discarded dead pigs into the irrigation system. This practice likely incurred a significant risk of introducing ASFV into the irrigation system or groundwater, where it could then be spread by water flow. In addition, water for pig rearing could be driven from the irrigation systems surrounding the farms, drill wells, or fish ponds (Mai et al., 2020).
In this study, water source (direct from drill well or irrigation system) was not included in the final model although this variable showed an association with ASF outbreak in the univariate analysis (p < 0.001).
The use of irrigation systems was identified as a significant risk fac-tor for porcine reproductive and respiratory syndrome in Vietnam (V. M. Truong & Gummow, 2014). Use of contaminated water from the Danube River was implicated in introducing ASF to farms (Houghton, 2018 to one another and it is exceedingly rare for pigs from private farms to move to company farms (A. D. Truong et al., 2020). Previous studies indicate that farms in northern provinces were highly connected through pig movements by pig purchases, especially in small farms (Baudon et al., 2017;Lee et al., 2021). In addition, boar hiring is the most common in these farms (Baudon et al., 2017). As a result of high connectivity between private farms through animal, vehicle, and human contacts, there was a higher risk of cross-contamination for private farms than for company farms. Moreover, biosecurity measures were less strictly applied in small farms compared with the large-scale industrial farms. A previous study indicated that ASF control measures mainly rely on strict sanitary interventions (Blome et al., 2020). In this study, 11/12 farms that did not have dressing rooms were case farms; all of 12 these farms were private farms. Two variables related to biosecurity practices were strongly associated with ASF outbreak. Applying less than six and 11 practice items to individuals inside the farm and at pig movement locations increased the odds of ASF outbreak by 5.20 and 5.86 times, respectively, compared with farms applying all practice items. Absence of dressing rooms for workers or visitors and lower biosecurity practices could be the potential risks for spreading ASF because of the high environmental resistance of ASFV. ASFV is able to persist for long periods in contaminated fomites or meat (Mazur-Panasiuk et al., 2019). Poor management and biosecurity practices were identified as crucial factors in increasing the risk of transmission of ASF in Uganda (Dione et al., 2017). According to a previous study, the limited biosecurity level of small domestic farms had the most significant contribution to the introduction of ASF into domestic farms (Boklund et al., 2018). Low biosecurity at pig movement locations, along with high environmental resistance of ASFV, could lead to rapid ASFV spread via transport vehicles. This finding may partially explain why ASF quickly spread to all 63 provinces in Vietnam and mainly to private farms. The spread of ASF may be associated with small private farms, which generally have lower biosecurity standards than larger commercial operations.
The major limitation of the study was bias introduced by the selection of control farms, which may have affected the risk factor analysis.
During the study period, more control farms culled their entire herds in the early stages of the outbreak. In addition, control farms were not geographically matched with case farms. Therefore, a location variable was included in the model as a random effect. A strength of this study was that study farms represented areas with high levels of pig production, and the questionnaires were administered by experienced veterinarians. In addition, there is a possibility that our results were affected by recall bias which is one of the most important problems for the case-control study. In this study, only eight of 182 responded farms did not have any written records, so that veterinarians questioned carefully as much as possible to reduce recall bias.
In conclusion, proximity to other farms and irrigation systems, poor hygienic management, and lower levels of biosecurity practices were

DATA AVAILABILITY STATEMENT
The data that support the findings of this study are included in the article and Supporting Information.