Interspecies transmission of porcine-originated G4P[6] rotavirus A between pigs and humans: a synchronized spatiotemporal approach

Valentina Kunić; Tina Mikuletič; Rok Kogoj; Tom Koritnik; Andrej Steyer; Silvija Šoprek; Goran Tešović; Vlatka Konjik; Ivana Roksandić Križan; Marina Prišlin; Lorena Jemeršić; Dragan Brnić

doi:10.3389/fmicb.2023.1194764

Interspecies transmission of porcine-originated G4P[6] rotavirus A between pigs and humans: a synchronized spatiotemporal approach

Front Microbiol. 2023 May 22:14:1194764. doi: 10.3389/fmicb.2023.1194764. eCollection 2023.

Authors

Affiliations

¹ Virology Department, Croatian Veterinary Institute, Zagreb, Croatia.
² School of Medicine, Institute for Microbiology and Immunology, University of Ljubljana, Ljubljana, Slovenia.
³ Public Health Microbiology Department, National Laboratory of Health, Environment, and Food, Ljubljana, Slovenia.
⁴ Department for Pediatric Infectious Diseases, University Hospital for Infectious Diseases "Dr. Fran Mihaljević", Zagreb, Croatia.
⁵ School of Medicine, University of Zagreb, Zagreb, Croatia.
⁶ Clinical Hospital Center Osijek, Osijek, Croatia.

Abstract

As a leading viral cause of acute gastroenteritis in both humans and pigs, rotavirus A (RVA) poses a potential public health concern. Although zoonotic spillover of porcine RVA strains to humans is sporadic, it has been detected worldwide. The origin of chimeric human-animal strains of RVA is closely linked to the crucial role of mixed genotypes in driving reassortment and homologous recombination, which play a major role in shaping the genetic diversity of RVA. To better understand how genetically intertwined porcine and zoonotic human-derived G4P[6] RVA strains are, the present study employed a spatiotemporal approach to whole-genome characterization of RVA strains collected during three consecutive RVA seasons in Croatia (2018-2021). Notably, sampled children under 2 years of age and weanling piglets with diarrhea were included in the study. In addition to samples tested by real-time RT-PCR, genotyping of VP7 and VP4 gene segments was conducted. The unusual genotype combinations detected in the initial screening, including three human and three porcine G4P[6] strains, were subjected to next-generation sequencing, followed by phylogenetic analysis of all gene segments, and intragenic recombination analysis. Results showed a porcine or porcine-like origin for each of the eleven gene segments in all six RVA strains. The G4P[6] RVA strains detected in children most likely resulted from porcine-to-human interspecies transmission. Furthermore, the genetic diversity of Croatian porcine and porcine-like human G4P[6] strains was propelled by reassortment events between porcine and porcine-like human G4P[6] RVA strains, along with homologous intragenotype and intergenotype recombinations in VP4, NSP1, and NSP3 segments. Described concurrent spatiotemporal approach in investigating autochthonous human and animal RVA strains is essential in drawing relevant conclusions about their phylogeographical relationship. Therefore, continuous surveillance of RVA, following the One Health principles, may provide relevant data for assessing the impact on the protectiveness of currently available vaccines.

Keywords: Croatia; G4P[6]; domestic pig; human; reassortment; recombination; rotavirus A; zoonosis.

Grants and funding

This research was funded by the Croatian Science Foundation installation research project Reco “Rotaviruses in Croatian Ecosystem: molecular epidemiology and zoonotic potential,” Grant No. HRZZ-UIP-2017-05-8580. The work of VK was funded by the Croatian Science Foundation project DOK-2021-02-3623.