Abstract
Over the years four porcine circoviruses (PCVs) species have been discovered, which apparently share common epidemiological trajectories. In particular, PCV-2 and PCV-3 species, better known for their pathogenicity and economic impact, despite being reported as emerging new viruses, were thereafter proved to have been circulating undetected over several decades in domestic pigs.
The detection of PCV-4 in China in 2019 (Zhang et al., 2019) and retrospectively in samples from 2012, demonstrates a circulation for at least 10 years in Chinese domestic pigs, reminding PCV-2 and -3 scenarios. However, the current restricted distribution in China, South Korea, Malaysia and Thailand, and the lack of detection in Italy, Spain and Colombia (Franzo et al., 2020, Vargas-Bermudez et al., 2022), apparently suggest a recent origin, thus conflicting with what demonstrated for the ubiquitous PCVs-2 and -3.
The present study aims to investigate PCV-4 apparent geographical confinement and address questions about its actual epidemiology and emergence.
Phylogenetic, phylodynamic, and phylogeographic analyses were performed on PCV-4 sequences with adequate metadata available in GenBank to reconstruct its history, migration paths and evolution.
A total of 97 sequences were included in the data set: 88 were detected in 10 different Chinese provinces, 4 in South Korea, 3 in Thailand, and 2 in Malaysia. The achieved alignment and phylogenetic trees showed a certain genetic stability between strains over time, and congruent results were obtained for different genomic regions. Additionally, the evolutionary rate is of the same order of magnitude of PCV-3. The analysis of viral population dynamics, similarly to other PCVs, suggests an ancient origin followed by persistent but undetected circulation in the swine population. Based on these results and others PCVs history/epidemiology a wider distribution than the one currently shown in literature was expected. On the contrary the geographical clustering, and the low number of clearly supported migration rates among Chinese provinces respectively showed by phylogenetic and phylogeographic analysis are compatible with the geographical isolation suggested by the detection of PCV-4 in Asia only and its absence in pivotal swine farming countries such as Italy and Spain. The contradiction with the hypothesis of an ancient viral origin is challenging to be explained, although the currently scarce number of available sequences, the limited number of studies performed outside Asia and the short timespan considered may be also involved.
This study provides an example of the application of genetic methods as instrumental tools to improve the understanding of pathogens' epidemiology, geographical relations, and emergence. In presence of larger-scale geographical data, genetic and spatial methods may act in synergy to better investigate the presence of spatial patterns, and to monitor, predict and thus better control the spreading of animal infectious diseases.
References
Zhang, H. H., Hu, W. Q., Li, J. Y., Liu, T. N., Zhou, J. Y., Opriessnig, T., & Xiao, C. T. (2019). Novel circovirus species identified in farmed pigs designated as Porcine circovirus 4, Hunan province, China. Transboundary and Emerging Diseases, 67(3), 1057–1061. https://doi.org/10.1111/tbed.13446
Franzo, G., Ruiz, A., Grassi, L., Sibila, M., Drigo, M., & Segalés, J. (2020). Lack of Porcine circovirus 4 genome detection in pig samples from Italy and Spain. Pathogens, 9(6), . https://doi.org/10.3390/pathogenS9060433
Vargas-Bermudez, D.S., Mogollón, J.D. & Jaime, J. (2022). The Prevalence and Genetic Diversity of PCV3 and PCV2 in Colombia and PCV4 Survey during 2015–2016 and 2018–2019. Pathogens, 11, 633. https://doi.org/10.3390/ pathogens11060633