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

Valentina Kunić1 Tina Mikuletič2 Rok Kogoj2 Tom Koritnik3 Andrej Steyer3 Silvija Šoprek4 Goran Tešović4,5 Vlatka Konjik6 Ivana Roksandić Križan6 Marina Prišlin1 Lorena Jemeršić1 Dragan Brnić1
Affiliations 6 institutions
  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.

Supporting text Virus Host Location
Croatia 5 domestic pig 2 G4P[6] 3 human 14 reassortment 36 recombination 40 rotavirus A 12 zoonosis 116

Evidence records

5 total
Zoonotic Surveillance
1 records · 1 evidence types
Evidence type
1 records
OVE7028
Key finding

G4P[6] rotavirus A was detected by RT-PCR and genotyping in diarrheal samples from children under 2 years of age and weanling piglets in Croatia.

Virus
Host
Location
Supporting text

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.

Method
real-time RT-PCR | genotyping | next-generation sequencing
Sample type
diarrheal samples
Geographic raw
Croatia
Country inferred
HRV
Transmission Evidence
1 records · 1 evidence types
Evidence type
1 records
OVE7029
Key finding

Human G4P[6] rotavirus A strains detected in children in Croatia most likely resulted from porcine-to-human transmission.

Virus
Host
Location
Supporting text

The G4P[6] RVA strains detected in children most likely resulted from porcine-to-human interspecies transmission. The present study employed a spatiotemporal approach to whole-genome characterization of RVA strains collected during three consecutive RVA seasons in Croatia (2018-2021).

Method
real-time RT-PCR | genotyping | next-generation sequencing | phylogenetic analysis | intragenic recombination analysis
Study design
genomic characterization and spatiotemporal analysis of porcine and human RVA strains
Transmission direction
animal-to-human
Geographic raw
Croatia
Country inferred
HRV
Genomic Evolution
3 records · 2 evidence types
Evidence type
2 records
OVE7030
Key finding

Croatian porcine and porcine-like human G4P[6] rotavirus A strains exhibited reassortment and homologous recombination involving VP4, NSP1, and NSP3 segments.

Virus
Host
Not specified
Location
Not specified
Supporting text

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.

Event type
reassortment
Genes or segments
VP4 | NSP1 | NSP3
OVE7031
Key finding

Homologous intragenotype and intergenotype recombinations occurred in VP4, NSP1, and NSP3 of Croatian porcine and porcine-like human G4P[6] rotavirus A strains.

Virus
Host
Not specified
Location
Not specified
Supporting text

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.

Event type
recombination
Genes or segments
VP4 | NSP1 | NSP3
Evidence type
1 records
OVE7032
Key finding

Phylogenetic analysis indicated that all six Croatian G4P[6] rotavirus A strains had genome segments of porcine or porcine-like origin.

Virus
Host
Location
Not specified
Supporting text

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.

Genes or proteins
eleven gene segments
Analysis methods
phylogenetic analysis