African Swine Fever: An Emerging Threat to Piggery Industry in India
Dr. Amitava Paul, Dr. Hardeep Kalkal and Dr. Shikha Tamta
Introduction:
African swine fever (ASF) is a contagious, devastating, transboundary, haemorrhagic viral disease of domestic and wild pigs, with exceptionally high lethality i.e., 100 %. Despite its limited host range and absent zoonotic potential, its socioeconomic impact is very high and the disease is notifiable to the World Organisation for Animal Health (OIE). ASF was first detected in East Africa in the early 1900s and spread to Europe and South America in the 1950s and 1960s, where it was eradicated after many years and substantial effort. After the appearance of ASF in the Caucasian region in 2007, it has been spreading quickly to neighbouring countries and beyond, making its first appearance in China in 2018 and other Asian countries. In recent times pigs industry in India has been hit by acute outbreak of ASF in north-eastern region and subsequently spreading to the other states at a very high rate causing severe mortality and economic losses to pig farmers. ASF not only affecting the animal health and welfare but also has detrimental impacts on biodiversity and the livelihoods of farmers. Against this background the current article focuses on etiological agent, host range, clinical disease upon infection, diagnosis and control to have a basic idea about the disease and minimize the chances of future outbreaks.
Causative Agent
The causative agent of ASF is African swine fever virus (ASFV), a large double-stranded DNA virus of the genus Asfivirus within the Asfarviridae family.
Species Affected
African swine fever affects members of the pig family (Suidae). Species known to be susceptible to infection include domesticated swine and wild boar (both subspecies of Sus scrofa), warthogs (Phacochoerus spp.), bush pigs (Potamochoerus larvatus and Potamochoerus porcus) and giant forest hogs (Hylochoerus spp.). Most of these animals can develop clinical signs, although infections in warthogs seem to be subclinical or mild. Bushpigs and warthogs are natural reservoir hosts of ASFV, although other wild suids might also play a role. Domesticated pigs also maintain ASFV.
Transmission
African swine fever can be transmitted either with or without tick vectors as intermediaries. Domesticated pigs can shed ASFV in all secretions and excretions including oronasal fluid, urine and faeces. Significant virus shedding can begin 2 days before the onset of clinical signs. Blood contains large amounts of the virus, and massive environmental contamination may result if blood is shed during necropsies or pig fights, or if a pig develops bloody diarrhea. ASFV can most likely enter the body through various mucous membranes after direct (non-tickborne) contact with infected pigs or the environment, but most animals are thought to be infected by inhalation or ingestion. Aerosolized viruses may contribute to transmission within a building or farm, but current evidence suggests that this only occurs over relatively short distances. Because ASFV can persist in tissues after death, it can be spread by feeding uncooked or undercooked pig swill that contains tissues from infected animals. Cannibalism of dead pigs might be important in some outbreaks.
Vector-mediated transmission occurs through the bites of some members of the soft tick genus Ornithodoros. In some parts of Africa, The ASF virus is maintained through a natural cycle of transmission between the juvenile common warthogs (Phacochoerus africanus), bushpig (Potamchoerus porcus) and soft ticks of the Ornithodoros moubata complex, which live in their burrows. Warthogs may get infected early in life following the bite of an infected tick. Virus replicates in the warthog and produces a low degree of viraemia for a few weeks, which is sufficient to infect a proportion of ticks that feed on the viraemic young warthogs. Domestic pigs mainly acquire infection from wildlife reservoirs of the virus primarily by the bite of an infected tick. A similar cycle is thought to exist between domesticated pigs in Africa and the Ornithodoros moubata complex ticks that colonize their pens. Ornithodoros spp. ticks are long-lived, and colonies have been demonstrated to maintain ASFV for several years. However, they can eventually clear the virus if they are not reinfected. Other bloodsucking insects such as mosquitoes and biting flies might be able to transmit ASFV mechanically.
Clinical Presentation and Gross Pathology
The clinical presentation and the gross pathological lesions of ASF in domestic pigs are highly variable and depend on the virulence of the strain and the age and immune status of the animals. The clinical courses observed in ASF in domestic pigs can be described as (a) peracute (or hyperacute), (b) acute, (c) subacute, and (d) chronic.
(a) Peracute ASF: Clinical Signs and Lesions: clinical course, characterized by a very rapid clinical course, with high fever (up to 42◦C), anorexia, lethargy, and sometimes sudden death without signs of disease. This is often observed when the virus enters a naïve farm causing death of some animals before the explosion of clinical cases. Some animals can show respiratory distress due to the high fever, but no gross lesions are usually found at the post mortem examination.
(b) Acute ASF: Clinical Signs and Lesions: This clinical form is cause by highly or moderately virulent isolates and it is the typical course observed in naïve farms very quickly after the first fatal cases are reported. The clinical course is characterized by high fever, with temperatures of 40– 42◦C, lethargy, anorexia, and inactivity. The affected animals tend to bunch up together. Many affected animals show a centripetal cyanosis, easily found in the ears, snout, limbs, abdomen, tail, and perianal area. Respiratory distress is usually observed, with severe pulmonary oedema in animals affected by highly pathogenic isolates. Skin lesions are frequent, with presence of petechial hemorrhages or ecchymosis. Other clinical signs may include nasal discharges, sometimes stained with blood (epistaxis), vomiting, diarrhoea and display signs of abdominal pain; the diarrhea is initially mucoid and may later become bloody, causing black-colored stains in the perianal area of the animal. Pregnant animals frequently abort and the mortality rates may reach up to 100% in affected farms within 7 days of the onset of the disease.
At the post mortem examination, the most characteristic lesion of acute ASF is the haemorrhagic splenomegaly, with a much-enlarged spleen, dark in color and friable at sectioning, occupying a large space within the abdominal cavity. The second most important lesion described in acute ASF is a multifocal haemorrhagic lymphadenitis. Lymph nodes can have multifocal or extensive haemorrhages that can produce a marbled appearance. The most affected lymph nodes are the gastrohepatic, renal, and other abdominal lymph nodes as ileocaecal, and mesenteric. Haemorrhages may also be observed in other lymph nodes, such as submandibular, retropharyngeal, or inguinal. Petechial haemorrhages are often observed in the kidney surface and at sectioning. Other lesions can also be observed, mostly haemorrhages in the mucosa or the serosa of other organs, as the large and small intestine, the epicardium in the heart, or the urinary bladder. Haemorrhages on wall of gall bladder or oedematous and enlarged gall bladder, haemorrhages on epiglottis and tonsils also commonly seen in acute infection.
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(c) Subacute ASF: Clinical Signs and Lesions: This clinical form is usually observed in animals infected by moderately virulent isolates, with similar clinical signs as those observed in acute ASF but with less severe form. Affected pigs show moderate to high fever and the mortality rate ranges from 30 to 70%, with pigs dying at 7–20 days after infection. The vascular changes, mostly haemorrhages and oedema, in the subacute form of the disease can be more intense than the acute form.
At the post mortem examination, animals show hydropericardium, ascites, and multifocal oedema, very characteristic in the wall of the gall bladder or in the perirenal fat. Some animals may show haemorrhagic splenomegaly as described for the acute form of the disease, but many animals will show partial splenomegaly, with patches of spleen affected and other areas unaffected. A multifocal haemorrhagic lymphadenitis can also be observed with multiple lymph nodes in all areas of the body showing the haemorrhages and the “marble” appearance. Petechial haemorrhages can also be observed in the kidney. Multifocal pneumonia is also observed with patches of consolidation and dark colour in the lung. This lesion can also be attributed to secondary infections due to the state of immunosuppression induce by ASFV.
(d) Chronic ASF: Clinical Signs and Lesions: This clinical form is caused by the infection of low virulence isolates. Pigs with the chronic form have nonspecific signs such as an intermittent low fever, appetite loss and depression. Other signs may be limited to emaciation and stunting, but some pigs develop respiratory problems and swollen joints. Coughing is common; diarrhoea and occasional vomiting have been reported. Ulcers and reddened or raised necrotic skin foci may appear over body protrusions and other areas subject to trauma. Chronic African swine fever can be fatal. No vascular changes are observed in the chronic form of ASF, and many observed lesions are associated with bacterial secondary infections, inducing fibrinous polyserositis, necrotic, or chronic pneumonia, necrosis of the skin, tongue, and tonsils.
Present scenario in India
India was considered to be free from African swine fever (ASF) till 2019. The first occurrence of African swine fever (ASF) in domestic pigs in India was recorded from two states of northeast India, namely Arunachal Pradesh and Assam in early 2020. Considering the geographical location and widespread on-going ASF outbreaks in China since 2018, the possible source of ASF into Arunachal Pradesh and subsequently to Assam state of India was considered as through China. Subsequently, the outbreak of ASF was reported from Mizoram state in the year 2022. Apart from these states, ASF outbreak has been reported from Tripura, Sikkim, Meghalaya, Manipur, Nagaland, Uttarakhand, Haryana, Kerala, Madhya Pradesh, Jharkhand and Punjab [Fig. B]. Though ASF is not a danger to human health as the virus can’t be transmitted from pigs to human, but it has devastating effects on pig populations and the pig’s farmer’s economy. Neither direct contact with infected pigs nor eating pork originating from infected pigs can transmit the virus to human. As the ASF has now being spread to several states of the country it has become a major crisis for the pork industry due to massive losses in pig population and drastic economic consequences. The outbreaks have serious economic impact, particularly on farmers whose livelihood depends on pig farming and for consumers who are faced with the brunt of increasing pork prices. Pork meat is one of the primary sources of animal protein for more than 35% of the global meat intake including in India. Hence, the disease poses a serious problem for food security worldwide.
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Diagnosis
Rapid and reliable diagnosis is of paramount importance when it comes to early warning, timely intervention, and monitoring of ASF. Clinical samples like blood, spleen, kidney, lymph nodes and tonsil in particular should be collected for virus isolation, detection of antigen or PCR testing for viral DNA. Methods for early diagnosis of the disease includes an immunoblotting assay, sandwich ELISA, polymerase chain reaction (PCR), nested-PCR, hot-start multiplex PCR real-time PCR, cross-priming amplification (CPA) and loop-mediated isothermal amplification (LAMP) assay.
Control
A quick response is vital for containing outbreaks in ASFV-free regions. Veterinarians who encounter or suspect African swine fever should follow their national and/or local guidelines for disease reporting. Biosecurity measures (e.g., fences, restricted visitor access, good hygiene, disinfection of footwear or the use of dedicated footwear, closed herds, quarantines of new animals) help prevent virus introduction onto farms. Separation of the herd from wild suids, their environments and carcasses, as well as measures to prevent accidental human transport of ASFV, must be considered. Some areas have successfully eradicated African swine fever outbreaks by standard stamping out measures (e.g., slaughter of infected and in–contact animals, sanitation, disinfection, movement controls and quarantines), but more complex measures were needed in some regions. Current regulations in the EU allow pig farms to be restocked as soon as 40 days after proper cleaning and disinfection, if an African swine fever outbreak occurs in the absence of vectors, but the minimum quarantine is 6 years if vectors are thought to be involved in transmission. Current control measures in wild boar mainly focus on reducing their numbers, as higher population densities are thought to facilitate maintenance of the virus, and attempting to discourage the movements of infected animals.
Outlook: The future fight against African swine fever must even more focus on enhanced classical control measures like timely and reliable diagnosis, strict hygiene and biosecurity measures, culling of infected farms, compensation of losses, stand still measures, epidemiological tracing, establishment of restriction zones and wild boar control programs. This is particularly necessary since an applicable, safe and effective vaccine that could be produced in large quantities and also be used in the wild animal reservoir will probably not be available in the short term. Therefore, future research should concentrate on development of sustainable vaccine. For the India’s a strategic research plan on surveillance and sero-epidemiology of ASF on domestic and wild pig population in the state will help to implement immediate containment measures to prevent further spread of the disease. Studies on the involvement of biological vectors in the perpetuation and transmission of ASFV are also important to estimate the risks more accurately in the Indian scenario.
CORRESPONDING AUTHOR-