African Swine Fever: an emerging risk to pig health
African swine fever (ASF) is a highly contagious, viral disease manifesting differently in wild and domestic pigs. Its impact depends on the virus virulence, the infectious dose, and the infection route. African swine fever is not a health or foodborne risk to humans as it only affects wild and domestic pigs. Mortality rate of peracute and acute clinical forms of ASF can reach 100% and in subacute or chronic forms, ASF mortality ranges from 30-70% (Galindo-Cardiel et al., 2013; Sánchez-Vizcaíno et al., 2015). On average, clinically recovered animals can continue to shed the virus for 6 weeks or longer (Sánchez-Vizcaíno et al., 2015). Early diagnosis of ASF is crucial to assist with the rapid implementation of measures necessary to control and eradicate the disease (Oura et al. 2013). Once the presence of ASF is confirmed, corresponding regulatory authorities must be immediately notified. In the United States, this means reporting all suspected cases to the appropriate State Veterinarian.
This article will:
- define ASF
- discuss the impacts of ASF
- explain transmission and spread
- describe control and eradication
- discuss prevention of global spread
What is ASF?
African swine fever is a highly fatal viral disease of wild and domestic pigs in regions of Asia, Africa and Europe (OIE, 2021). African swine fever is caused by an infection with a complex DNA virus, the ASF virus (Dixon et al. 2019). Infection produces a wide range of clinical forms: peracute, acute, subacute, and chronic (Arias et al. 2008; see Table 1). Wild pigs and soft ticks of the Ornithodoros genus are natural hosts of the virus in which the infection is usually asymptomatic and persistent. In contrast, in domestic pigs it manifests as a hemorrhagic fever with a mortality rate up to 100% (Penrith & Vosloo, 2009). Currently, there is no effective, commercially available vaccine against ASF (Galindo & Alonso, 2017). However, recently, scientists with the U.S. Department of Agriculture’s Agricultural Research Service announced that a novel ASF vaccine candidate has been evaluated and conditionally approved for use in Vietnam.
Table 1: Characteristics of peracute, acute, subacute, and chronic forms of ASF. Adapted from (Sánchez-Vizcaíno et al., 2015).
|Peracute ASF||Acute ASF||Subacute ASF||Chronic ASF|
|Virus||Highly virulent||Highly virulent||Moderately virulent||Low virulent|
|Fever||41-42°C||40.5-42°C||Slight fever||Intermittent low fever|
|Lesion||Few or poorly developed lesions||Hemorrhagic lesions in spleen, lymph nodes, kidneys, and heart||Petechiae and cyanotic lesions||Ulcers, reddened and necrotic lesions of the skin and arthritis|
|Symptoms||Loss of appetite, inactivity, hyperpnea and cutaneous hyperemia.||Reddening of the skin, tips of ears, tail, distal extremities, ventral aspects of chest and abdomen. Anorexia, listlessness, cyanosis, and incoordination. Increased pulse and respiratory rate|
Vomiting, diarrhea, and eye discharges. Abortion in pregnant sows.
|Reduced appetite and depression. Abortion in pregnant sows.||Loss of weight, chronic skin ulcers, pericarditis, adhesions of lungs, swellings over joints, appetite loss and depression. emaciation and stunting, respiratory problems, and swollen joints. Coughing, diarrhea, and occasional vomiting.|
|Mortality rate||100%||100%||30–70%||Low mortality|
|Death||1-4 days after the onset of clinical signs||Within 6–13 days, or up to 20 days||Within 15–45 days||Few weeks to months|
Economic impact of ASF
African swine fever has a severe socio-economic impact, both in the areas where it is newly introduced and where it is endemic. This is due to the high mortality rates associated with the acute and peracute forms of the disease and its potential for extensive and rapid spread at international levels (Arias et al., 2008). The highest impact of ASF is in countries with a significant commercial pig industry (Costard et al., 2009) as it leads to immediate restrictions on the pig and pork trade, and the implementation of drastic and costly control strategies to eradicate the disease. These eradication techniques and restrictions on pork trade may limit the amount of pork supplied to many countries having serious implications for the human food supply. The U.S. is the world’s third largest pig producer, with over 11.5 million tons of pork produced per year, and the world’s second largest pork exporter, with exports in 2017 valued at 4.6 billion USD (FAO, 2018). It is estimated that the net benefit of preventing ASF introduction in the U.S. amounts to almost $4500 million annually, representing nearly 5% of the value of total sales of pork products (Rendleman & Spinelli, 1994). A new study conducted by agricultural economists at Iowa State University estimated that the economic impact of ASF outbreak in the U.S. could cost the swine industry as much as $50 billion over 10 years (Carriquiry et al., 2020).
Transmission and spread
The hosts of ASF include domestic pigs and wild pigs. The virus transmits between domestic pigs, between wild pigs, from wild pigs to domestic pigs, by various forms of human activity and byfeed and feed ingredients (Dixon et al. 2019). Pigs recovering from infection with moderate or low virulence isolates may remain persistently infected and may spread infection to pigs via direct contact. However, the frequency and duration of virus persistence and their potential role in the spread of ASF is unknown. Furthermore, soft ticks of the genus Ornithodoros play a role in the disease transmission as biological vectors. African swine fever is not infectious to humans, nor can it be transmitted to humans through consumption of pork products. Although, in East Africa, the soft tick vector is present in some villages and can play a role in maintaining a reservoir of ASF, they are currently not thought to be involved elsewhere.
Transmission between domestic pigs
The ASF virus can be transmitted between infected pigs by direct contact through the oral-nasal route or through skin abrasions. The virus is present in bodily fluids including urine, feces, saliva, and semen. Aerosol transmission is thought to occur only over short distances (i.e. 1 m or 3.281 ft) (Olesen et al., 2017). Ingestion of infected material on contaminated surfaces, feed or water can also result in pigs getting infected by virus (Petrov et al., 2018).
Transmission between wild pigs
Wild pigs in Africa can be persistently infected and develop few if any clinical signs. Wild pigs develop a transient increase in circulating virus that is sufficient to infect soft ticks that feed on them. Soft ticks play an important role in virus transmission between wild pig hosts. Transmission of virus between wild pigs also occurs by direct or indirect contact with infected animals or contaminated surfaces, feed, or water. An additional route of infection between wild pigs is thought to be contact with infected carcasses (Berg et al., 2015; Probst et al., 2017).
Transmission from wild pigs to domestic pigs
Disease transmission from wild pigs to domestic pigs is thought to take place when wild pigs and domestic pigs share the same feeding area and soft ticks from wild pigs bite domestic pigs (Jori & Bastos, 2009). Domestic pigs may be readily infected by wild pigs, either by direct or indirect contact. This is particularly important in areas with a high density of wild pigs where the contact with domestic pigs is more likely, particularly with domestic pigs raised in establishments with insufficient biosecurity or where pigs are allowed outdoors to forage during the day (Dixon et al. 2019).
Transmission by various forms of human activity
Various human activities can increase the risk of ASF spread within an infected country, or from an infected area to ASF-free area or country. Imported pork products pose a high risk as the virus can survive for years in processed items or indefinitely in frozen products. Fomites including clothing, boots, transport vehicles and hunting knives, can also be a source of infection through indirect transmission (Guinat et al., 2016; Sánchez-Vizcaíno et al., 2015). Feeding pigs contaminated garbage, garbage containing pork products, or materials such as grass contaminated by infected wild pigs excretions can also result in infection (Dixon et al. 2019). In addition, administration of non-approved attenuated ASF vaccines in China has contributed to ASF spread through Chinese swine industry throughout 2019.
Transmission by feed and feed ingredients
The ability of feed and feed ingredients to serve as vehicles for the transport and transmission of viral pathogens is a new discovery, previously thought not to occur (Dee et al., 2020). The original hypothesis surrounding the risk of feed was based on observations following the introduction of Porcine Epidemic Diarrhea Virus into the US in 2013-2014. The rapid movement of a previously unidentified viral pathogen across long distances, simultaneously infecting unrelated swine populations housed under conditions of high biosecurity raised awareness to the possibility of contaminated feed. Following proof of this hypothesis (Dee et al., 2014), scientific evidence evaluating the survival of ASF virus, as well as Classical Swine Fever virus, Foot and Mouth Disease virus, Seneca virus A, and Pseudorabies virus in feed and feed ingredients has been published (Caserta et al., 2022; Dee et al., 2018; Stenfeldt et al., 2022; Stoian et al., 2020). In regard to ASFV, transmission of the virus by feed and water and the infectious oral dose by feed and water consumption has been published (Niederwerder et al., 2019) and the T ½ of the virus in feed has been calculated (Stoian et al., 2019).
Control and eradication
Avoiding introduction of the disease is the primary focus for countries currently free of ASF. Several strategies have been studied to develop vaccines; however, the lack of neutralizing antibodies, genetic variability, and knowledge gaps relating to pathogenesis and the immune response make discovery-based approaches difficult (Sánchez-Vizcaíno et al., 2015). Disease control is best approached through implementation of on-farm biosecurity practices (Chenais et al., 2019).Although, recent vaccine development is Vietnam is promising, there is still lack of field data to support vaccine efficacy.
The most critical tool for preventing ASF is an adequate farm biosecurity plan which should describe all available interventions and strategies for how each item such as supplies needed, changes in management practices, etc. could be implemented (Bellini et al. 2016). Biosecurity practices include all measures aiming to minimize the risk of introducing new pathogens (i.e. external biosecurity) to the farm (Dewulf 2014). In recent years, risk-based scoring indexes such as UGhent Bio check (Laanen et al., 2009) and Secure Pork Supply biosecurity self-assessment checklist (SPS, 2021) have been developed to provide an objective way to quantify biosecurity status and harmonize recommendations. These scoring systems group different internal and external biosecurity practices into several sections and each section receives a weighted score. Such scoring systems are good for benchmarking, and they provide useful information to farmers, veterinarians and pig advisors on which areas biosecurity could be improved. Although some biosecurity principles apply to all farming systems and infectious diseases, biosecurity plans tailored for specific farming systems are important to target particular diseases (Calderón Díaz et al. 2020). Secure Pork Supply offers a self-assessment checklist for enhanced pork production biosecurity for animals raised indoors (SPS, 2021). Below are the checklist components.
- Biosecurity manager and written plan: A biosecurity manager needs to be identified for the site who is responsible for developing the biosecurity plan with the assistance of the herd veterinarian. Then, a site-specific, written, enhanced biosecurity plan needs to be developed and implemented.
- Training: The biosecurity manager and essential personnel need to be trained at least annually about the biosecurity measures necessary to keep ASF out of the herd.
- Testing: The biosecurity manager and essential personnel need to be tested at least annually to make sure the training was learned properly.
- Protecting the pig herd: it is implemented through the following areas.
- Site entry: a barrier must be present restricting access of unauthorized vehicles to the pork production facilities within the site.
- Designated parking area: There is a clearly marked, designated parking area outside of the perimeter buffer area, away from animal areas, for vehicles that have not been cleaned and disinfected.
- Perimeter buffer area: This area is established to serve as an outer control boundary around the buildings to limit virus transmission.
- Perimeter buffer area access point: Vehicles moving through the perimeter buffer area access point must be cleaned to remove visible contamination and then disinfected.
- Cleaning and disinfection station: There is an operational, clearly marked, and equipped cleaning and disinfection station with the means to remove visible contamination and then disinfect vehicles, equipment, and items needing to enter the perimeter buffer area.
- Line of separation: Line of separation is established as a control boundary to prevent virus transmission into areas where susceptible animals can be exposed.
- Line of separation access point: Equipment, people, and items crossing through the line of separation access point follow specific biosecurity measures.
- Securing the buildings: Buildings are locked when no one is present.
- Vehicles and equipment: All vehicles and equipment are cleaned and effectively disinfected prior to entering the perimeter buffer area. Disinfectants proven to be effective at eliminating the ASFV virus include potassium peroxymonosulfate, sodium hypochlorite, products consisting of Quaternary Ammonium with Glutaraldehyde, and …
- Personnel: Access is limited to individuals who are essential to the operation of the production site. Everyone crossing the line of separation arrives at the site having showered and wearing clean clothing and footwear.
- Pig movement: Incoming pigs come from sources with documented, enhanced biosecurity practices and no current or recent evidence of ASF infection. No animals from a regulatory control area are introduced onto the site for at least 7 days prior to moving any animals to another pork production site with susceptible animals.
- Carcass disposal: Dead animals are disposed of in a manner that prevents the attraction of wildlife, rodents, and other scavengers. Rendering trucks and other vehicles hauling dead animals to a common disposal site do not enter the perimeter buffer area.
- Manure management: Manure is stored and removed in a manner that prevents exposure of susceptible animals to disease agents and meets state, local, and Responsible Regulatory Officials’ requirements.
- Feed: Feed and feed ingredients are a potential source of infection introduction to swine farms and to pigs’ post-consumption of contaminated feed (Caserta et al., 2022). The data on feed risk ushers in the concept of “Next Generation Biosecurity”, changing human behavior regarding the need to biosecure feed and feed ingredients as they move between countries and between farms (Dee & Spronk, 2022). Principles of Responsible Imports, employing extended storage times following arrival of feed and feed ingredients from countries of high risk are being applied across North America (Calvin et al., 2022; Patterson et al., 2019). In addition, the use of feed additives previously demonstrated to have anti-viral properties help biosecure feed at the level of the mill and the farm (Dee et al., 2020; Niederwerder et al., 2021). Grain and feed are delivered, stored, mixed, and fed in a manner that minimizes contamination. Feed spills are cleaned up promptly and disposed of to avoid attracting wildlife.
Common Swine Industry Audit
Many farms have established biosecurity protocols that must be adhered to by the auditor. This includes required hours of downtime, personnel entry procedures, and if and how external equipment/materials can be brought into the site. The following questions in the common swine industry audit cover the biosecurity of the farm (National Pork Board, 2022). It must be noted that the Common Swine Industry Audit biosecurity protocol improves farm biosecurity, and it is not a guaranty to secure farm against ASF.
- Q90. Does the site have a written biosecurity SOP that contains information covering barn sanitation, rodent control, worker and visitor entry policies, and general farm security measures?
- Q91. Is there evidence that the site’s rodent control protocol is being followed?
- Q92. Does the site have a log for visitors?
- Q93. Does the site have signage or other methods around the facility to control and restrict access for biosecurity compliance?
Prevention of global spread
To combat ASF globally, surveillance and control methods need to be managed at the following three levels (Costard et al., 2009):
- Locally at points of occurrence in the swine farm: For local control in countries with a large, small-scale swine population, outreach efforts to increase disease awareness and improved access to animal health services are required to be implemented in the swine farms.
- Regional level in endemic and adjoining areas: For the implementation of control programs in endemic or epidemic areas, tools for rapid detection would allow a timely diagnosis and ensure involvement at the local level in control of the disease. Additionally, in the absence of an effective vaccine, direct and indirect transmission and contact with wildlife reservoirs need to be limited to reduce disease burden.
- Globally by preventing transboundary and transcontinental spread through animal movement and products: To prevent the spread of ASF at a global level through movement of livestock, livestock products or other agriculture commodities, countries are advised to follow international standards as outlined by the World Organization for Animal Health (Costard et al., 2009).
African swine fever is a contagious disease with severe socio-economic impacts within the swine industry. It has no direct impacts on human health; however, it is highly contagious and detrimental to domestic pigs. The disease has a high potential for expansion to new areas globally where it can then rapidly spread and persist if early detection and strict control measures are not implemented. Current control strategies rely on rapid detection and implementation of quarantine and slaughter policies. Detection of ASF virus antigen enables testing samples on a large scale; however, it is not sensitive enough in detecting early-stage infection. Therefore, quantitative PCR and conventional PCR are used as fast and sensitive methods to detect virus. Furthermore, to combat ASF globally, surveillance and control methods need to be managed (a) at points of occurrence in the swine farm level, (b) in endemic and adjoining areas, and (c) globally by preventing transboundary and transcontinental spread through animal movement and products. In addition, development of a safe and effective vaccine would be a critical tool to control and eradicate the virus from wild and domestic pigs. Although further work is needed before these could be used in the field.
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