Wide spread incidences of vaccine-like strains of lumpy skin disease virus (LSDV) have recently been reported in a Russian region with a neighboring country that actively vaccinate with a live attenuated LSD vaccine. The use of live-attenuated viruses (LAVs) as vaccines during an active outbreak, creates potential ground for coinfection of hosts and emergence of a strain combining genetic fragments of both parental vaccine and field strains. In this study, we analyse the vaccine-like strain LSDV RUSSIA/Saratov/2017 detected in Saratovskaya oblast, a region sharing border with Kazakhstan. To gain insight into possible recombination signals, a full-genome next-generation sequencing of the viral genome was performed using the Illumina platform. The genome contains the backbone of a live-attenuated vaccine with a patchwork of wild-type field virus DNA fragments located throughout. A total of 27 recombination events were identified. The average distance between the recombination sites was 3400 base pairs (bp). The impact of the recombination events on the virulence and transmission capacity of the identified virus remains to be clarified. These findings provide evidence for the first time of genetic exchanges between closely related strains of capripoxviruses in the field and a vaccine strain, and prompt a revisiting of the vaccination issue for a safe and efficacious prevention and control strategy of LSD.

Lumpy skin disease is recognized as a transboundary and emerging disease of cattle, buffaloes and other wild ruminants. Being initially restricted to Africa, and since 1989 the Middle East, the unprecedented recent spread across Eurasia demonstrates how underestimated and neglected this disease is. The initial identification of the causative agent of LSD as a poxvirus called LSD virus, was well as findings on LSDV transmission and epidemiology were pioneered at Onderstepoort, South Africa, from as early as the 1940s by researchers such as Weiss, Haig and Alexander. As more data emerges from an ever-increasing number of epidemiological studies, previously emphasized research gaps are being revisited and discussed. The currently available knowledge is in agreement with the previously described South African research experience that LSDV transmission can occur by multiple routes, including indirect contact, shared water sources and arthropods. The virus population is prone to molecular evolution, generating novel phylogenetically distinct variants resulting from a diverse range of selective pressures, including recombination between field and homologous vaccine strains in cell culture that produce virulent recombinants which pose diagnostic challenges. Host restriction is not limited to livestock, with certain wild ruminants being susceptible, with unknown consequences for the epidemiology of the disease.

Vaccination against lumpy skin disease (LSD) is crucial for maintaining the health of animals and the economic sustainability of farming. Either homologous vaccines consisting of live attenuated LSD virus (LSDV) or heterologous vaccines consisting of live attenuated sheeppox or goatpox virus (SPPV/GPPV) can be used for control of LSDV. Although SPPV/GTPV-based vaccines exhibit slightly lower efficacy than live attenuated LSDV vaccines, they do not cause vaccine-induced viremia, fever, and clinical symptoms of the disease following vaccination, caused by the replication capacity of live attenuated LSDVs. Recombination of capripoxviruses in the field was a long-standing hypothesis until a naturally occurring recombinant LSDV vaccine isolate was detected in Russia, where the sheeppox vaccine alone is used. This occurred after the initiation of vaccination campaigns using LSDV vaccines in the neighboring countries in 2017, when the first cases of presumed vaccine-like isolate circulation were documented with concurrent detection of a recombinant vaccine isolate in the field. The follow-up findings presented herein show that during the period from 2015 to 2018, the molecular epidemiology of LSDV in Russia split into two independent waves. The 2015–2016 epidemic was attributable to the field isolate. Whereas the 2017 epidemic and, in particular, the 2018 epidemic represented novel disease importations that were not genetically linked to the 2015–2016 field-type incursions. This demonstrated a new emergence rather than the continuation of the field-type epidemic. Since recombinant vaccine-like LSDV isolates appear to have entrenched across the country’s border, the policy of using certain live vaccines requires revision in the context of the biosafety threat it presents.