Insights into cross-species infection: Porcine epidemic diarrhea virus infections in the rodent

Jianing Chen; Zemei Wang; Shengyu Lin; Mengling Gao; Yongheng Shao; Shuxian Li; Qingbo Chen; Yaru Cui; Yonghao Hu; Guangliang Liu

doi:10.1016/j.virs.2025.03.012

June 2025

Citation: Jianing Chen, Zemei Wang, Shengyu Lin, Mengling Gao, Yongheng Shao, Shuxian Li, Qingbo Chen, Yaru Cui, Yonghao Hu, Guangliang Liu. Insights into cross-species infection: Porcine epidemic diarrhea virus infections in the rodent .VIROLOGICA SINICA, 2025, 40(3) : 301-313. http://dx.doi.org/10.1016/j.virs.2025.03.012

Insights into cross-species infection: Porcine epidemic diarrhea virus infections in the rodent

Jianing Chen ^a ,
Zemei Wang ^a,b ,
Shengyu Lin ^a,c ,
Mengling Gao ^a ,
Yongheng Shao ^a,b ,
Shuxian Li ^a,d ,
Qingbo Chen ^a,d ,
Yaru Cui ^a ,
Yonghao Hu ^b ,
Guangliang Liu ^{a
,,}

a. State Key Laboratory for Animal Disease Control and Prevention, College of Veterinary Medicine, Lanzhou University, Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural Sciences, Lanzhou 730000, China;
b. College of Veterinary Medicine, Gansu Agricultural University, Lanzhou 730070, China;
c. College of Animal Sciences, Fujian Agriculture and Forestry University, Fuzhou 350002, China;
d. College of Veterinary Medicine, Xinjiang Agricultural University, Urumqi 830052, China

Corresponding author: Guangliang Liu, LiuGuangliang01@caas.cn
Received Date: 03 July 2024
Accepted Date: 25 March 2025
Available online: 27 March 2025

Abstract

The cross-species infection of coronaviruses has resulted in several major epidemics since 2003. Porcine epidemic diarrhea virus (PEDV) is a devastating swine enteric coronavirus, which targets pigs as the only natural reservoir. In this study, the nucleic acid of PEDV was detected in rat fecal samples collected from pig farms. Further animal tests showed that PEDV can cause systemic infections in neonatal mice and rats via intracranial inoculation. The brain, lung, intestine and spleen were all targets for PEDV in rodents in contrast to the intestine being targeted in pigs. Morbidity and mortality vary via different infection routes. PEDV was also detectable in feces after infection, suggesting that the infected rodents were potential infectious sources. Moreover, the cerebral tropism of PEDV was verified in piglets via orally inoculation, which had not been identified before. In conclusion, our findings demonstrate that PEDV could cross the species barrier to infect mice and rats through different routes in experimental settings. Although it is highly devastating to piglets, PEDV changes the target organs and turns to be milder when meeting with new hosts. Based on these findings, more attention should be paid to the potential cross-species infection of PEDV.
- Porcine epidemic diarrhea virus
- , Rodent
- , Cerebral tropism
- , Cross-species
- , Animal model

Electronic Supplementary Material

10.1016j.virs.2025.03.012-ESM.docx
References
1. Butler, N., Pewe, L., Trandem, K., Perlman, S., 2006. Murine encephalitis caused by HCoV-OC43, a human coronavirus with broad species specificity, is partly immune-mediated. Virology 347, 410-421.
2. Chen, J., Cui, Y., Wang, Z., Liu, G., 2020. Identification and characterization of PEDV infection in rat crypt epithelial cells. Vet. Microbiol. 249, 108848.
3. Chen, Y., Jiang, R. D., Wang, Q., Luo, Y., Liu, M. Q., Zhu, Y., Liu, X., He, Y. T., Zhou, P., Yang, X. L., Shi, Z. L., 2022. Lethal Swine Acute Diarrhea Syndrome Coronavirus Infection in suckling mice. J. Virol. 96, e0006522.
4. Chung, H.C., Lee, J.H., Nguyen, V.G., Huynh, T.M.L., Lee, G.E., Moon, H.J., Park, S.J., Kim, H.K., Park, B.K., 2016. New emergence pattern with variant porcine epidemic diarrhea viruses, South Korea, 2012-2015. Virus Res. 226, 14-19.
5. De Sabato, L., Ianiro, G., Monini, M., De Lucia, A., Ostanello, F., Di Bartolo, I., 2020. Detection of hepatitis E virus RNA in rats caught in pig farms from Northern Italy. Zoonoses Public Health 67, 62-69.
6. Han, Y., Du, J., Su, H., Zhang, J., Zhu, G., Zhang, S., Wu, Z., Jin, Q., 2019. Identification of diverse bat alphacoronaviruses and betacoronaviruses in China Provides new insights into the evolution and origin of coronavirus-related diseases. Front. Microbiol. 10, 1900.
7. Huang. X., Chen, J., Yao, G., Guo Q, Wang, J., Liu, G., 2019. A TaqMan-probe-based multiplex real-time RT-qPCR for simultaneous detection of porcine enteric coronaviruses. Appl. Microbiol. Biotechnol. 103, 4943-4952.
8. Joshi, L.R., Mohr, K.A., Clement, T., Hain, K.S., Myers, B., Yaros, J., Nelson, E.A., Christopher-Hennings, J., Gava, D., Schaefer. R., et al., 2016. Detection of the emerging Picornavirus Senecavirus A in pigs, mice, and houseflies. J. Clin. Microbiol. 54, 1536-1545.
9. Kotani, O., Shirato, K., Nagata, N., Ikeda, H., Takahashi, K., Taguchi, F., 2013. Neuropathogenesis of a mouse-adapted porcine epidemic diarrhea virus infection in suckling mice. J. Gen. Virol. 94, 831-836.
10. Lacroix, A., Duong, V., Hul, V., San, S., Davun, H., Omaliss, K., Chea, S., Hassanin, A., Theppangna, W., Silithammavong, S., et al., 2017. Genetic diversity of coronaviruses in bats in Lao PDR and Cambodia. Infect. Genet. Evol. 48, 10-18.
11. Lorincz, M., Csagola, A., Biksi, I., Szeredi, L., Dan, A., Tuboly, T., 2010. Detection of porcine circovirus in rodents - short communication. Acta Vet. Hung. 58, 265-268.
12. Lv, L., Luo, H., Yu, L., Tong, W., Jiang, Y., Li, G., Tong, G., Li, Y., Liu, C., 2022. Identification and characterization of cell lines HepG2, Hep3B217 and SNU387 as models for porcine epidemic diarrhea coronavirus infection. Viruses 14, 2754.
13. McIntosh, K., Becker, W.B., Chanock, R.M., 1967. Growth in suckling-mouse brain of "IBV-like" viruses from patients with upper respiratory tract disease. Proc. Natl. Acad. Sci. U S A 58, 2268-2273.
14. Mora-Diaz, J.C., Pineyro, P.E., Houston, E., Zimmerman, J., Gimenez-Lirola, L.G., 2019. Porcine Hemagglutinating Encephalomyelitis Virus: a review. Front. Vet. Sci. 6: 53.
15. Mora-Diaz, J.C., Pineyro, P.E., Rauh, R., Nelson, W., Sankoh, Z., Gregg, E., Carrillo-Avila, J.A., Shen, H., Nelli, R.K., Zimmerman, J.J., et al., 2021. Porcine hemagglutinating encephalomyelitis virus infection in vivo and ex vivo. J. Virol. 95, e02335-20.
16. Murphy, E.G., Williams, N.J., Bennett, M., Jennings, D., Chantrey, J., McElhinney, L.M., 2019. Detection of Seoul virus in wild brown rats (Rattus norvegicus) from pig farms in northern England. Vet. Rec. 184, 525.
17. Niu, Z., Zhang, S., Xu, S., Wang, J., Wang, S., Hu, X., Zhang, L., Ren, L., Zhang, J., Liu, X., et al., 2023. Porcine epidemic diarrhea virus replication in human intestinal cells reveals potential susceptibility to cross-species infection. Viruses 15, 956.
18. Park, J.E., Park, E.S., Yu, J.E., Rho, J., Paudel, S., Hyun, B.H., Yang, D.K., Shin, H.J., 2015. Development of transgenic mouse model expressing porcine aminopeptidase N and its susceptibility to porcine epidemic diarrhea virus. Virus Res. 197, 108-115.
19. Pensaert, M.B., de Bouck, P., 1978. A new coronavirus-like particle associated with diarrhea in swine. Arch. Virol. 58, 243-247.
20. Pinheiro, A.L., Bulos, L.H., Onofre, T.S., de Paula, Gabardo.M., de Carvalho, OV., Fausto, M.C,, Guedes, R.M., de Almeida, M.R., Silva, Junior.A., 2013. Verification of natural infection of peridomestic rodents by PCV2 on commercial swine farms. Res. Vet. Sci. 94, 764-768.
21. Sanford, B.J., Opriessnig, T., Kenney, S.P., Dryman, B.A., Cordoba, L., Meng, XJ., 2012. Assessment of the cross-protective capability of recombinant capsid proteins derived from pig, rat, and avian hepatitis E viruses (HEV) against challenge with a genotype 3 HEV in pigs. Vaccine 30, 6249-6255.
22. Simas, P.V., Barnabe, A.C., Duraes-Carvalho, R., Neto, D.F., Caserta, L.C., Artacho, L., Jacomassa, F.A., Martini, M.C., Bianchi, Dos, Santos, M.M., et al., 2015. Bat coronavirus in Brazil related to appalachian ridge and porcine epidemic diarrhea viruses. Emerg. Infect. Dis. 21, 729-731.
23. Stevenson, G.W., Hoang, H., Schwartz, K.J., Burrough, E.R., Sun, D., Madson, D., Cooper, V.L., Pillatzki, A., Gauger, P., Schmit, B.J., et al., 2013. Emergence of Porcine epidemic diarrhea virus in the United States: clinical signs, lesions, and viral genomic sequences. J. Vet. Diagn. Invest. 25, 649-654.
24. Sun, R., Cai, R., Chen, Y., Liang, P., Chen, D., Song, C., 2012. Outbreak of porcine epidemic diarrhea in suckling piglets, China. Emerg. Infect. Dis. 18, 161-163.
25. Sun, Y., Chen, Y., Han, X., Yu, Z., Wei, Y., Zhang, G., 2019. Porcine epidemic diarrhea virus in Asia: an alarming threat to the global pig industry. Infect. Genet. Evol. 70, 24-26.
26. Tonietti, Pde, O., da Hora, A.S., Silva, F.D., Ferrari, K.L., Brandao, P.E., Richtzenhain, L.J., Gregori, F., 2013. Simultaneous detection of group a rotavirus in swine and rat on a pig farm in Brazil. ScientificWorldJournal 2013, 648406.
27. Wang, B., Meng, XJ., 2021. Hepatitis E virus: host tropism and zoonotic infection. Curr. Opin. Microbiol. 59, 8-15.
28. Wang, X., Fang, L., Liu, S., Ke, W., Wang, D., Peng, G., Xiao, S., 2019. Susceptibility of porcine IPI-2I intestinal epithelial cells to infection with swine enteric coronaviruses. Vet. Microbiol. 233, 21-27.
29. Wood, E.N., 1977. An apparently new syndrome of porcine epidemic diarrhoea. Vet. Rec. 100, 243-244.
30. Zhai, S., Chen, S., Liu, W., Li, X., Deng, S., Wen, X., Luo, M., Lv, D., Wei, W., Chen, R., 2016. Molecular detection and genome characterization of porcine circovirus type 2 in rats captured on commercial swine farms. Arch. Virol. 161, 3237-3244.
31. Zhang, J., Guo, L., Xu, Y., Yang, L., Shi, H., Feng, L., Wang, Y., 2017. Characterization of porcine epidemic diarrhea virus infectivity in human embryonic kidney cells. Arch. Virol. 162, 2415-2419.
32. Zhao, S., Gao, J., Zhu, L., Yang. Q., 2014. Transmissible gastroenteritis virus and porcine epidemic diarrhoea virus infection induces dramatic changes in the tight junctions and microfilaments of polarized IPEC-J2 cells. Virus Res. 192, 34-45.
Proportional views