A phylogenetic contribution to understanding the panzootic spread of African swine fever: from the global to the local scale

Abstract

African Swine Fever virus has become a primary concern for veterinarian health agencies and pig producers worldwide. The current panzootic of the virus genotype II is having a devastating impact on pig production in Africa, Europe, Asia, Oceania and Hispaniola (Caribbean). Due to its high persistence and mortality rate, disease control policies require enhanced passive surveillance activities, wild boar depopulation, containment and other costly interventions, as a safe and effective vaccine is not currently available. Since 2007, several disease clusters have emerged far from both its original range, in South-Eastern Africa, and far from other affected suid populations. These transmissions were likely caused by anthropogenic movement of contaminated material, facilitated by the persistence of the virus in the environment and on contaminated material. The objective of this research is to understand the spatio-temporal dynamic of the African Swine Fever virus panzootic, with a specific focus on clusters from mainland Italy. We mapped and analysed the virus spread using 228 whole-genome sequences available from online repositories and from the Italian cases/outbreaks, combined with their metadata. We inferred the pathogen phylogenies using a Bayesian phylodynamic model, with which we obtained a time-scaled and spatially explicit maximum clade credibility tree. Our results showed a non-negligible number of long-distance transmissions across regions or continents, coupled with dense local dynamics, particularly in areas where the disease affected a naive population. The distribution of spatial distances inferred along the trees branches further highlighted these trends, and revealed how previously observed survival times in pork products could allow the virus to traverse distances up to 900km. Finally, from the available sequences, we identified at least seven separate introduction events in Europe, of which at least three caused new clusters on mainland Italy. This study provides important insights on the African Swine Fever virus introduction into many affected areas worldwide and highlights the crucial role of genomic surveillance to correctly track the pathogen spread, and to monitor the virus potential evolution.