African Swine Fever: the state of the art in Italy up to 11 September 2023
Introduction
African swine fever (ASF) is a contagious viral disease affecting pigs, characterized by haemorrhagic symptoms. It can infect both domestic pigs and wild boars (biologically of the same species, Sus scrofa). Unfortunately, no safe and effective vaccine is currently available, so control appears very complicated.
Although it is not a zoonosis, it is a serious question because of the high mortality rates in affected populations (90-100%). African swine fever is a highly contagious viral disease affecting domestic pigs and Eurasian wild boars, caused by African swine fever virus (ASFV). ASFV poses a significant economic threat because of its high lethality rate and severe impact on markets. The virus can spread through various cycles, including the African cycle, which involves wild reservoirs such as feral pigs, warthogs, and soft ticks (Ornithodoros spp.). The domestic cycle, in which the virus spreads among domestic pigs through various routes and includes direct and indirect contact (contaminated food or tools). Finally, the wild boar-habitat cycle observed in the Central and Eastern European outbreak.
ASFV is remarkably stable and resilient, remaining infectious for extended periods in carcasses and the environment. The virus was first reported in Kenya in 1921, and initially occurred in sub-Saharan African countries where it remains endemic. Genotypic differentiation of ASFV has identified 24 genotypes, with only five known as pig-adapted viruses, including genotype I and II responsible for outbreaks outside of Africa.
The disease emerged in Europe, Russia, the Caribbean, and South America between the late 1950s and early 1980s, leading to widespread outbreaks across the continent.
In Europe, genotype I ASFV emerged in the late 1950s and spread to various countries, including Portugal, Spain, France, and Italy. The Sardinia region (Italy), experienced an ASFV incursion in 1978, leading to endemicity on the island. A second epidemic wave in 2007 introduced genotype II ASFV to the Republic of Georgia, spreading to other countries, such as Poland, Latvia, and Estonia in 2014. The virus continued to spread, reaching countries like the Czech Republic, Romania, Belgium, Hungary, Serbia, and Slovakia in subsequent years. In 2022, ASFV spread to Italy, initially affecting wild boars.
Italy has faced different scenarios of ASF infections, including protecting ASF-free territories, managing ongoing epidemics among wild boars, and eradicating ASF in regions with coexisting domestic pigs and wild boars, such as Sardinia. The unique Italian experience in ASF control provides valuable insights into the effectiveness of strategies and measures adopted, identifying areas for improvement in disease management and control efforts.
The present paper aims to provide a comprehensive overview of ASF in Italy, describing the spread of ASF in wild boars and domestic pigs as an example of multiple concurring different scenarios.
The different italian scenarios
The current Italian epidemiological scenario (updated to the 11 of September 2023) is reported in Figure 1.
Figure 1. Current Italian epidemiological scenario updated to the 11 of September 2023 representing the protection and surveillance zone and the restricted zones I, II, and III that are listed in the Annex I of Commission Implementing Regulation (EU) 2023/594, as last amended by the Commission Implementing Regulation (EU) 2023/1485 on the 18th of July 2023
Sardinia: a step closer to ASF eradication
The text discusses the epidemiological scenario of African Swine Fever Virus in the Sardinia region, Italy, up to 11 September 2023. It outlines how ASFV genotype I has been present since 1978 due to factors such as the coexistence of domestic and wild pigs, backyard pig farming, and illegal free-ranging pig breeding. The cultural tradition of backyard pig raising for festivals and traditional dishes has contributed to the persistence of ASFV. To combat the disease, a tailored eradication strategy, known as EP-ASF-15-18, was implemented in 2015. This strategy focused on banning free-ranging pig rearing, enforcing biosecurity measures, and incentivizing farmers to adopt safer practices. This strategy gained support from local authorities and stakeholders and aimed to address the specific challenges of the Sardinian context.
The measures included financial support for farms to implement mandatory biosecurity measures, such as double fencing, and incentives for the breeding sector, such as individual bonuses for breeder pigs. Veterinary inspections were intensified throughout the pig production chain, while stricter regulations were enforced for hunting, including proper disposal of wild boar carcasses. These efforts were associated by extensive training and awareness campaigns targeting farmers, hunters, and the public.
To address the issue of free-ranging pig farming, approximately 5000 pigs were culled during military-style operations, resulting in enhanced biosecurity and fewer ASF outbreaks. The effective regional control structure, supported by central authorities, implemented expert recommendations, leading to ASFV eradication in Sardinia by 2018 in domestic pigs and 2019 in wild boars.
However, achieving ASF-free status at the European level requires further evidence of no ASFV circulation in wild boars. To this end, a surveillance strategy was implemented, encompassing active and passive monitoring of domestic animals and wild boars, with the development of tools such as the WBC-Counter Tool to standardize surveillance efforts.
Despite evidence of active ASFV circulation only in certain areas, Sardinia applied EU regulations rigorously, considering the entire region at the highest risk level initially. As the epidemiological situation improved, the restricted zone was gradually reduced.
Although ASFV seropositive animals were still occasionally detected during the implementation of the exit strategy, the decreasing number of cases suggests that ASFV eradication in Sardinia may be achieved in the near future, even if the ASF-free status cannot yet be declared.
At present, the last step that the European Commission requires in order to grant definitive indemnity to the region is the conclusive suppression of the remaining illegal grazing, which to a small extent persists, undermining the eradication process itself.
Piedmont–Liguria–Lombardy Regions: the challenge of tri-regional incursion
In early 2022, ASFV genotype II was detected in wild boars in the northwest of Italy, precisely between the provinces of Alessandria and Genoa (Liguria Region). The outbreak prompted the establishment of regional crisis units to manage surveillance, hunting activities, and biosecurity measures. Moreover, in accordance with EU regulations, restricted zones were defined, and movement restrictions were implemented to prevent the spread of the disease. In February 2022, a special Commissioner was appointed to coordinate actions effectively.
Despite of the efforts to contain the disease by erecting fencing around the affected areas, bureaucratic delays and challenging territories hindered the complete containment of the disease, resulting in an unstopped spread. By June 2023, ASFV had spread to Lombardy Region, marking a tri-regional incursion. Multiple cases were confirmed in wild boars, and the first outbreak in pigs was detected in August 2023. Prompt measures were taken, including culling and disposal of infected pigs, alongside the establishment of protection and surveillance zones. Despite intensive farming practices in Lombardy, gaps in biosecurity measures were identified on affected farms, highlighting the imperative for enhancing collaboration among authorities, veterinarians and farmers to fight the epidemic in Northern Italy.
Central Italy, Lazio Region: a re-emerging challenge
Lazio is a central Italian region that is characterised by the high wild boar population
(around 70,000 animals) living in rural, as well as in peri-urban and urban areas, and a poorly pigmeat sector that is predominantly composed by backyard pig farming and commercial farms, typically attaining no more than 50 animals.
In May 2022, Lazio region faced an outbreak of African Swine Fever Virus when an infected wild boar was found near Rome. Prompt notification to authorities and comprehensive territorial analysis facilitated the establishment of an infected area core and restriction zones, encompassing parks and reserves. Measures such as erecting fences, reinforcing passive surveillance, and ensuring strict carcass disposal were swiftly implemented to curtail virus spread.
Despite these proactive measures, ASFV was detected in an outdoor pig farm nearby in June 2022, evidently related to the present epidemic in wild boar. Actions, including movement restrictions, stamping out of infected farms, and epidemiological investigations, were promptly implemented. However, due to poor farm biosecurity and the presence of wild boars, containment efforts faced challenges.
Although no new cases were detected from September 2022 to May 2023, a resurgence occurred in May, marking a new epidemic phase. Despite setbacks, delays, and obstacles, maintaining rigorous surveillance efforts remains imperative to control the outbreak and prevent further spread.
At present, the wild boar population in the affected area is reduced to a minimum, both because the disease has decimated the population and because the competent authorities have depopulated the most frequented areas; this gives hope that the virus will soon be eradicated.
Calabria Region: a complex scenario
Calabria is a southern-Italian region characterised by a moderate/high wild boar population (around 60,000 animals) inhabiting rural and forested areas and a small pigmeat sector that primarily consists of small-scale familiar or wild and semi-free-range farming, typically with no more than 200 animals.
In May 2023, Calabria, experienced an ASFV outbreak when three dead wild boars tested positive in Cardeto (in the Reggio Calabria province) and Reggio Calabria province. Subsequently, another case was confirmed in Bagnara Calabra, 40 km away. Despite a moderate wild boar population, the presence of backyard and small commercial pig farms with inadequate biosecurity measures posed a significant risk for virus transmission.
The virus later spread to two small pig herds in Africo, 70 km from the initial outbreak, located in a rural forest area lacking adequate biosecurity measures. Approximately 80 animals were culled, and strict cleaning and disinfection procedures were implemented.
Despite the biosecurity measures put in place, new cases in wild boars continued to emerge and the infection is still spreading in all directions.
Challenges encountered included outdated farm registries, deficient farm biosecurity practices, animal movements escaped veterinary control and difficulty in controlling wild pig populations due to rugged and wide territory and logistical issues with carcass tracing.
The complex situation in Calabria posed significant management difficulties, highlighting the need for improved farm registries, enhanced biosecurity measures, and better coordination in wild pig population control and carcass tracing efforts compared to national contingency plans.
Campania region: newest cluster
Campania, a central-southern Italian region, is characterised by a moderate wild boar population of approximately 55,000 animals inhabiting rural and peri-urban areas. Its pigmeat sector consists primarily of familiar or wild and semi-free-range farming, typically attaining no more than 20 animals, although scattered commercial farming with more than 100 animals can also be found.
In May 2023, Campania faced an outbreak of African Swine Fever Virus when five decomposed wild boar carcasses tested positive in Sanza and Montesano on the Marcellana. The region promptly established an infected zone encompassing several municipalities in Salerno province, implementing additional measures near the border with Basilicata region.
With a wild boar density ranging from one to five animals per Km2, efforts focused on preventing ASFV spread and involving the domestic pig sector. A coordinated campaign employing targeted hunting and trapping with euthanasia was employed to reduce the wild boar population, to curb the outbreak and to prevent further ASFV spread to domestic pig sectors.
It is interesting to record that although the infection continues to be present in the area of origin, the cluster has not expanded in a relevant form, and the properly infected zone remains rather limited.
Discussion
African Swine Fever it is a highly fatal disease of domestic pigs and wild boars, with severe implications for the pig industry and livelihoods. Despite ongoing research into vaccines and therapeutics, no effective products are currently available, making the control of the disease challenging. Thus, minimizing the impact of ASF relies heavily on stringent biosecurity measures and effective preparedness planning.
Considering the international scenario characterised by several incursions of ASF in several European and non-European countries, since 2018, Italy has been proactive in preparing for ASF incursions, as well as be ready to face the emergency when an ASF incursion occurs.
These included the drafting of a contingency plan, an emergency manual for ASF in wild boars and an operative manual for ASF and classical swine fever (CSF) in domestic pigs. Furthermore, awareness campaigns and simulation exercises have been carried out to engage stakeholders and to improve preparedness, response capabilities, crisis management, and risk and crisis communication.
Despite these efforts, ASF genotype II was reported in several peninsular regions of Italy in 2022, while the Sardinia region was applying the exit strategy to obtain the ASF-free status from the European Commission (EC). The initial incursion occurred in Piedmont in January 2022, with subsequent outbreaks primarily affecting wild boars. However, challenges arose in implementing control measures due to institutional complexities and social factors affecting public compliance. Measures such as fencing systems and carcass removal were delayed or incomplete, contributing to ASF spread.
To date, approximately 650 confirmed ASF cases have been reported in northern Italy (Piedmont, Liguria, and Lombardy), resulting in significant economic losses in Italian pig meat industry. However, the disease continues to spread in peninsular Italy, with outbreaks detected in domestic pigs too. Surveillance and eradication efforts prioritize passive surveillance of wild boars, intensified biosecurity measures and movement restrictions in affected regions, and strengthening veterinary supervision.
In addition to local endemic persistence, the virus has spread to new areas, including Central and Southern Italy (Lazio, Calabria, and Campania), through wild boar populations and human activities such as the illegal trade of animals. Despite efforts to contain the disease, challenges persist, exacerbated by opposition from animal rights activists.
Furthermore, eradication efforts have been complicated by social factors, bureaucratic inefficiencies, and geographical challenges. In some regions, ASF has become endemic, requiring careful epidemiological monitoring and control measures.
In southern Italy, ASF outbreaks in domestic pigs were linked to small farms with inadequate biosecurity measures, stressing the need for better control and awareness measures.
In Sardinia, ASF eradication efforts have shown promising results, with a marked decrease in outbreaks following strict biosecurity regulations and exit strategy implementation. However, in the recent past, scattered seropositive animals persist, delaying ASF-free status achievement. Efforts are underway to eliminate the residual and minimal presence of illegally grazing animals in order to calculate this important risk factor.
Overall, ASF remains a significant challenge for Italy, requiring comprehensive strategies tailored to regional contexts, public cooperation, and addressing socio-economic and institutional factors influencing control efforts. Ongoing surveillance (active and passive), and containment energies are crucial to mitigating the spread of the disease, to safeguard both animal and human health and achieving ASF-free status.
Conclusions
The management of African Swine Fever in Italy presents a multifaceted challenge, encompassing the eradication of genotype I in Sardinia and the emergence of four new incursions of genotype II in peninsular Italy. While ASF spreads across Europe, its extent and impact in Italy were unforeseen. The country's approach to disease control is in line with EFSA and FAO international guidelines, but success depends on the rigorous and effective implementation of measures by each country.
Past experiences reveal varying success levels in fighting ASF, with some countries achieving eradication, such as Belgium and the Czech Republic, while others, like Italy, grapple with ongoing containment challenges.
African swine fever's complexity arises from its intersection with health, economic, environmental, political, sociological, and cultural factors, requiring collaboration among stakeholders (farmers, hunters, forest rangers, and citizens) at national, regional, and local levels.
Costly control measures, including preparedness and eradication phases, require timely implementation, as proved by lessons learned from fence construction in Piedmont region. Moreover, communication failures and conflicts of interest have delayed progress. Media attention on wild boar overpopulation often overshadows the urgency of addressing ASF, leading to confusion in addressing both issues simultaneously.
Addressing ASF in wild boars requires tailored intervention plans linked to specific territories. While reducing wild boar density aids in preventing ASF, it also benefits farmers. As ASF becomes endemic in Italian clusters and spread in the northwest, defending productive areas, becomes crucial, with biosecurity playing a central role, particularly in intensive pig farming, alongside strict control of the entire supply chain to ensure export guarantees.
References
- Pavone, S.; Iscaro, C.; Dettori, A.; Feliziani, F. African Swine Fever: The State of the Art in Italy. Animals 2023, 13, 2998.
Francesca Dall’Acqua1, Silvia Pavone2, Francesco Feliziani2
1 National Reference Centre for Veterinary Epidemiology, Programming, Information and Risk Analysis (COVEPI).
Istituto Zooprofilattico Sperimentale dell'Abruzzo e del Molise "G. Caporale", Teramo, Italy
2 National Reference Laboratory for Pestivirus and Asfivirus. Istituto Zooprofilattico Sperimentale dell’Umbria e delle Marche “Togo Rosati”, Perugia, Italy
Correspondig author: f.dallacqua@izs.it
