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

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.

Human transmission and outbreaks of feline‐like G6 rotavirus revealed with whole‐genome analysis of G6P[9] feline rotavirus

“…RVA G6 strains have been documented in humans even earlier than the cases described above. 21,36,[38][39][40][41][42][43][44] In Hungary and Bulgaria in 1990s-2010s, G6P [8] and G6P [9] strains (e.g., Hun7, BP108, BG76, and BG1506) were identified in individuals with symptoms of gastroenteritis. 40,44 Furthermore, in the early 2010s, G6P [6] strains (e.g., BA346, ES298, 265-BF, and BF98) were circulating in children with acute diarrheal illness in African countries, including Cameroon and Burkina Faso.…”

“…Among the 61 samples collected from asymptomatic cats, three RVA G6P [9] strains and two G3P [9] strains were identified. The partial nucleotide sequences of Mie20120022f/G6P [9] and Mie20120049f/ G6P [9] were obtained by directly sequencing the RT-PCR products (Table 1). The whole nucleotide sequences of Mie20120017f/G6P [9], Mie20120003f/G3P [9], and Mie20120016f/G3P [9] were determined using NGS.…”

“…No gene segments of the representative G3P [9] feline/humanlike (FRV-1/AU-1-like) or G3P [3] feline/canine-like (Cat97/CU-1like) strains shared > 98% nucleotide identity with those of Mie20120017f (Table 1). Among other feline strains, G3P [9] strain T A B L E 1 Complete genotype constellations and nucleotide identities (%) of representative cat, human, and other animal strains with the Mie20120017f strain. THA/Meesuk/2021 most closely resembled Mie20120017f, sharing > 95% nucleotide identity across seven genetic segments (VP4, VP1, and NSP1-5).…”

“…In the VP6 (I3) tree, strains Mie20120003f/G3P [9] and Mie20120016f/G3P [9] belong to lineage I, forming a cluster with feline/human P [9] strains (Supporting Information: Figure 1B).…”

“…On the NSP2 (N2) tree, Mie20120017f clustered with feline strain THA/Meesuk/2021/G3P [9], canine G3P [3] strains, and bovine strains in lineage I (with nucleotide identities of 92.2%-100%) (Figure 3E).…”