SHIC Monitors Recombinant ASFV Genotype I/II Strain Emergence Globally

The US swine industry is vulnerable to the introduction of emerging pathogens and routine swine disease monitoring provides early warnings of global challenges that could negatively impact US swine producers. As part of its mission to identify emerging disease threats, SHIC funds Global Swine Disease Monitoring Reports led by Dr. Maria Sol Perez Aguirreburualde at the University of Minnesota. Recent reporting on African swine fever virus strain circulation has highlighted a concerning expansion of the ASFV Recombinant Genotype I/II strains being detected in Asia and now the Russian Far East. Evolving changes in globally circulating ASFV genotypes continue to pose risks for US introduction and inform ongoing prevention and preparedness activities to protect the health of US swine.

Background

Since first being reported in August 2018 on a pig farm near Shenyang, China, 19 additional countries have reported ASF outbreaks in the Asia and Pacific region as of October 2024. The first ASFV genotype occurring in Asia was genotype II, characterized by highly pathogenic strains causing high mortality in domestic pigs. Genotype II is the predominant virus in Europe, Russia, Asia, and the Americas. Ongoing changes in ASFV circulating genotypes are being monitored by the Swine Health Information Center and reported via its Global Swine Disease Monitoring Reports.

Key events altering the ASF epidemiological landscape in Asia

Between 2019 and 2020, there were reports of low pathogenic strains of ASFV genotype II in China and other Asian countries. These low pathogenic genotype II strains were detected during various surveillance activities. Later, in 2021, ASFV genotype I was reported in China which further complicated the epidemiology of the disease in the country and Asia-Pacific region. Prior to this report, ASFV genotype I was only known to be present in Sardinia, Italy, and on the African continent. In 2021, China also reported the discovery of ASF viruses that were a mix between the two genotypes (recombinant viruses).

The recombinant viruses in China were a mix of genetic types, genotypes I and II. These new strains were found in pigs from Jiangsu, Henan, and Inner Mongolia. The viruses were identified as genotype I based on one gene (B646L). However, they showed an unexpected characteristic—they were “HAD-positive” and caused red blood cells to clump together, something not seen in previous genotype I strains in China. This trait is linked to a specific protein, CD2v, encoded by another gene (EP402R). When the researchers sequenced the EP402R gene, they found that it matched genotype II viruses, suggesting a mix between the two genotypes.

In 2023, researchers in Vietnam reported the detection of the recombinant ASFV genotype I and II viruses in domestic pig farms in Northern Vietnam. The recombinant viruses found in Vietnam matched the corresponding sequences of recombinant ASFV I/II strains from China, except for one genetic region, the Central Variable Region. Further molecular analysis of the recombinant strains from Vietnam indicates three possible independent introductions into the country.

ASFV recombinant virus strains reported in Russia

Also in 2023, an ASFV isolate obtained from a domestic pig in the Primorsky Region, a Russian region bordering China, was found to be a recombinant strain. The recombinant genotype I/II virus found in Primosky shares similarities with the recombinant strains from China and has a 99.9% sequence identity, although it does not share identical viral gene sequences. This means the Primosky isolate may be part of a wider transmission network and has undergone minor evolutionary changes as it spread from China. The Primosky recombinant strain presented acute disease in domestic pigs when infected experimentally, which suggests similar characteristics to the Recombinant strains from China.

Timeline of ASFV strain discovery in Asia and the Russian Far East

August 2018 – ASFV emergence in Asia (China) – ASFV genotype II (highly pathogenic strains)
January 2019 – ASFV continues in China and other Asian countries – ASFV genotype II (low pathogenic strains)
December 2020 – ASFV continues in Asia – ASFV genotype II (low pathogenic gene deleted strains)
March 2021 – New outbreak in China – ASFV genotype I (low pathogenic strains)
December 2021 – New outbreak in China – ASFV recombinant genotype I/II
2023 – New outbreaks in Vietnam and Russia – ASFV recombinant genotype I/II

Characteristics of ASFV recombinant strain

Genotype I/II strains from China:

  • The genomes are 56.5% genotype II virus and 43.5% genotype I virus, with 10 gene fragments transferred from the genome of ASFV genotype II.
  • Animal studies with one of the recombinant viruses indicate high lethality and transmissibility in domestic pigs.
  • Deletion of the virulence-related genes MGF_505/360 and EP402R derived from the virulent genotype II virus highly attenuates the virulence of the recombinant strain.
  • Immunological studies on these three recombinant viruses showed that the recombinant virus was highly lethal and transmissible in pigs and evaded the immunity induced by vaccination with a live attenuated vaccine.

Genotype I/II strains from Vietnam:

  • Genetically similar to the genotype I/II recombinant virus from China, when compared across 13 different genes.
  • It is only different at the Central Variable Region
  • It can be grouped into three sub-groups based on CVR analysis, which suggests three possible introductions to Vietnam from China.

Conclusions
The ASFV genotype I/II recombinant strains are circulating in swine and have likely spread to neighboring countries of China, not just Vietnam and Russia. Still, to confirm this assumption, molecular surveillance efforts are lacking in many countries in the region.

The recombinant strains are highly lethal and transmissible in pigs. Based on preliminary evidence, current live-attenuated vaccines based on ASFV genotype II, such as those being implemented in countries such as Vietnam and the Philippines, are most likely not protective against these recombinant genotype I/II strains.

References
1. Zhao, D., Sun, E., Huang, L. et al. Highly lethal genotype I and II recombinant African swine fever viruses detected in pigs. Nat Commun 14, 3096 (2023). https://doi.org/10.1038/s41467-023-38868-w
2. Le, V., Nguyen, V., Le, T., Mai, N., Nguyen, V., Than, T….Ambagala, A. (2024). Detection of Recombinant African Swine Fever Virus Strains of p72 Genotypes I and II in Domestic Pigs, Vietnam, 2023. Emerging Infectious Diseases, 30(5), 991-994. https://doi.org/10.3201/eid3005.231775.
3. Sun E, Huang L, Zhang X, Zhang J, Shen D, Zhang Z, Wang Z, Huo H, Wang W, Huangfu H, Wang W, Li F, Liu R, Sun J, Tian Z, Xia W, Guan Y, He X, Zhu Y, Zhao D, Bu Z. Genotype I African swine fever viruses emerged in domestic pigs in China and caused chronic infection. Emerg Microbes Infect. 2021 Dec;10(1):2183-2193. doi: 10.1080/22221751.2021.1999779. PMID: 34709128; PMCID: PMC8635679.
4. Shi K, Liu H, Yin Y, Si H, Long F and Feng S (2022) Molecular Characterization of African Swine Fever Virus From 2019-2020 Outbreaks in Guangxi Province, Southern China. Front. Vet. Sci. 9:912224. doi: 10.3389/fvets.2022.912224
5. Wang X, Wang X, Zhang X, He S, Chen Y, Liu X, Guo C. Genetic Characterization and Variation of African Swine Fever Virus China/GD/2019 Strain in Domestic Pigs. Pathogens. 2022 Jan 14;11(1):97. doi: 10.3390/pathogens11010097. PMID: 35056045; PMCID: PMC8780551.
6. Igolkin, A., Mazloum, A., Zinyakov, N. et al. Detection of the first recombinant African swine fever virus (genotypes I and II) in domestic pigs in Russia. Mol Biol Rep 51, 1011 (2024). https://doi.org/10.1007/s11033-024-09961-0

The Swine Health Information Center, launched in 2015 with Pork Checkoff funding, protects and enhances the health of the US swine herd by minimizing the impact of emerging disease threats through preparedness, coordinated communications, global disease monitoring, analysis of swine health data, and targeted research investments. As a conduit of information and research, SHIC encourages sharing of its publications and research. Forward, reprint, and quote SHIC material freely. For more information, visit http://www.swinehealth.org or contact Dr. Megan Niederwerder at mniederwerder@swinehealth.org or Dr. Lisa Becton at lbecton@swinehealth.org.