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Update on ASF diagnosis and current circulating strains
Carmina Gallardo and Marisa Arias
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Summary
Knowledge of and attempts to control African swine fever (ASF) date back at least a century and it is now the first disease for which a viral etiology, ASF virus (ASFV), threatens the global swine industry in all over the world and affects the five continents. ASFV infects domestic and wild members of the Suidae family, causing a wide variety of symptoms, from chronic or persistent infection to acute haemorrhagic fever, causing up to 100% mortality in their sharper forms. There is no commercialized vaccine available against the ASFV, and current control measures consist of strict animal quarantine and culling procedures. The virus is very stable and spreads easily through infected pigs, contaminated pork products, and fomites, or by transmission by the Ornithodoros vector. The establishment of endemic ASFV infections in wild boar populations further complicates the control of the disease. Since its first description in Kenya in 1921, ASFV remained exclusively on the African continent until the end of the 1950s. It was in 1957 that ASFV emerged for the first time in Europe, spreading to South America, but was eradicated in mostly in the mid-1990s. In 2007, a highly virulent genotype II ASFV strain emerged in the Caucasus region and subsequently spread to the Russian Federation and Europe, where it has continued to circulate and spread. In 2018, ASFV jumped to China and spread to several neighbouring countries in Southeast Asia. More recently, and after 40 years of silence, the ASFV emerged in America, affecting the Dominican Republic and Haiti in 2021. The high morbidity and mortality associated with ASFV, the lack of an effective vaccine, and the complexity of the virus, as well as its epidemiology, make this pathogen a serious threat to the global swine industry and national economies. Topics covered by this review include the genetic characteristics of ASFV, its biological properties, with particular attention to the evolution of virulent to moderate and attenuated, strains, current and future diagnostic strategies, diagnostic gaps and their relevance.
ASFV genetics, epidemiology and genotype II epidemic history
The ASFV genome is approximately 170 to 190 kilobase (kb) pair and is divided into the left variable region (38 to 48 kb), the conserved central region (approximately 125 kb), and the right variable region (13 to 22 kb). The differences in size between the strains are due to insertions or deletions of the genes of the 5 multigene families (MGF), although variations in the conserved central region related to single nucleotide polymorphism (SNP) or to the presence of tandem repeat sequences (TRS) have been described. These variable regions are important for phylogenetic studies of ASFV. Comparative analysis of the C-terminal end of the B646L gene, which encodes the p72 protein, allows ASFV to be classified into 24 different genotypes (Quembo et al., 2019). This method, used internationally, allows relatively quick and easy typing of ASFV strains and remains the first approach to identify the origin of the virus in case of introduction into new territories. However, the genotyping method based on the B646L gene, it does not always provide adequate typing resolution or the ability to discriminate between viruses closely related. Analysis of the tandem repeats sequences (TRS) in the central variable region (CVR) of the B602L gene or the intergenic region (IGR) between the I73R and I329L genes at the right end of the genome (Gallardo et al., 2014) can be used to distinguish closely related ASFV isolates. The B602L gene is a particularly discriminative genetic marker whose sequencing has distinguished up to 31 subgroups of viruses with varying tetrameric amino acid repeats (Nix et al, 2006). Many other gene regions, such as the E183L, CP204L and EP402R encoding the p54, p30 and CD2v proteins, respectively, have also proved valuable in the analysis of ASFV from various locations to trace its spread (Qu et al., 2022).
The complex epidemiological pattern of ASFV is evident in sub-Saharan African that result in greater genetic variability of ASFV isolates from eastern and southern Africa with all 24 genotypes present (Penrith et al., 2022). In West African viruses are highly homogeneous, and outbreaks have historically been associated with genotype I, although different studies describe the spread of ASFV genotypes from East Africa to West Africa (Adedeji et al., 2021). In 1957, ASF genotype I was identified for the first time in Europe, in Lisbon coming from West Africa (Danzetta et al., 2021). In 1960 emerged in Lisbon and after that ASFV spread through the Iberian Peninsula (Spain and other areas of Portugal), and from there to other countries in Europe, the Caribbean and Brazil. Eradication was achieved in the mid-1990s, except in Sardinia, where the disease remains endemic. Genotype I was responsible for this first transcontinental spread.
In 2007, the second jump from the African to the European continent took place, when the ASFV emerged in the Republic of Georgia. The cause of this outbreak was a genotype II, which was circulating in Mozambique, Madagascar and Zambia (Rowlands et al, 2008). Subsequently, the disease continued to spread through the Caucasus region and later through the Russian Federation and Eastern Europe, until reaching the European Union (EU) in 2014. Since then, ASF has been reported by 13 EU countries, including Lithuania, Poland, Latvia and Estonia (2014), the Czech Republic and Romania (2017), Bulgaria and Hungary (2018), Belgium and Slovakia (2019), Greece and Germany in 2020, and most recently in January 2022, in the Piedmont region of north-western Italy. Two European countries have managed to eradicate the disease: Belgium (event resolved in March 2020) and the Czech Republic (event resolved in April 2018). In August 2018, the worst scenario happened when China reported the outbreak of ASF in the Liaoning province caused by a genotype II strain (Ge et al., 2018). Since then, the disease continued to spread in China, and by the end of February of 2022, ASFV was detected in 32 China provinces and in 13 Asian countries, being the latest Thailand in January 2022. In September 2019, the first occurrence of ASF in Oceania was reported by Timor-Leste, followed by Papua New Guinea (March 2020). In July 2021 the disease reappeared in the Americas after an absence of almost 40 years, having been introduced in Dominican Republic and later in Haiti (FAO situation update, www.fao.org).
The investigation of virus molecular evolution in combination with spatio-temporal data is an integral part of pathogen tracing and may help in the identification of potential routes of its spreading, therefore in disease prevention and control. With the introduction of ASF into Asia, place with the highest population of domestic pigs in the world, the world is now facing the worst pandemic of an animal disease seen to date, and new ASFV whole-genome sequences from Europe and Asia are being published with increasing frequency. Currently there are available 139 whole genome sequences from 13 out of the 24 genotypes described, and 41 corresponds to genotype II (figure 1). [...]
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