Molecular detection of porcine circovirus (PCV2 and PCV3), torque teno swine virus 1 and 2 (TTSuV1 and TTSuVk2), and histopathological findings in swine organs submitted to regular slaughter in Southeast, Brazil
PDF
XML

Keywords

Histopathology; nested PCR; coinfection; pig; asymptomatic infection

How to Cite

de Souza, A. E., Cruz, A. C. de M., Rodrigues, I. L., de Carvalho, E. C. Q., Varella, R. B., Medina, R. M., … de Castro, T. X. (2023). Molecular detection of porcine circovirus (PCV2 and PCV3), torque teno swine virus 1 and 2 (TTSuV1 and TTSuVk2), and histopathological findings in swine organs submitted to regular slaughter in Southeast, Brazil. Brazilian Journal of Veterinary Medicine, 45, e000623. https://doi.org/10.29374/2527-2179.bjvm000623

Abstract

Porcine circovirus 2 and 3 (PCV2 and PCV3) and torque teno sus virus 1 and 2 (TTSuV1 and TTSuVk2) are important pathogens in pig associated with post-weaning mortality, different clinical syndromes in adults (PCVAD), and a decrease of average daily weight gain (PCV2-SI) but little is known about the infection on asymptomatic pigs. The aim of this study was to evaluate the presence of PCV2, PCV3, TTSuV1, and TTSuVk2 in swine organ samples from asymptomatic pigs slaughtered in Espírito Santo State, Southeastern Brazil, through molecular detection and histopathological analysis. Nested PCR showed the presence of PCV2 DNA in 10% (14/140), PCV3 in 13.6% (19/140), TTSuV1 in 12.9% (18/140), and TTSuVk2 in 30% (42/140) of the tissue samples. All four viruses were detected in the lung, kidney, lymph node, and liver. TTSuVk2 was detecded in 30% (42/140), PCV3 in 13.6% (19/140), TTSuV1 in 12.9% (18/140), and PCV2 in 10% (14/140) of the samples. Single infections were observed in 30.7% (43/140), while co-detections in the same tissue occurred in 15.7% (22/140). The most frequent combinations were TTSuV1/TTSuVk2 in 31.8% (7/22), PCV2/TTSuVk2 in 18.1% (4/22), and PCV2/PCV3/TTSuVk2 in 13.6% (3/22). Lymphocyte depletion was associated with TTSuVk2 infection (p = 0.0041) suggesting that TTSuVK2 plays an induction of PMWS-like lymphoid lesions in pigs. The data obtained in this study show that PCV2, PCV3, TTSuV1, and TTSuVk2 are related to infection in asymptomatic animals with different tissue lesions, and the molecular diagnosis for these pathogens should be considered in the sanitary monitoring of herds.

https://doi.org/10.29374/2527-2179.bjvm000623
PDF
XML

References

Alarcon, P., Rushton, J., & Wieland, B. (2013). Cost of post- weaning multi-systemic wasting syndrome and porcine circovirus type- 2 subclinical infection in England - an economic disease model. Preventive Veterinary Medicine, 110(2), 88-102. http://dx.doi.org/10.1016/j.prevetmed.2013.02.010. PMid:23490147.

Aramouni, M., Kekarainen, T., Ganges, L., Tarradas, J., & Segalés, J. (2013). Increased viral load and prevalence of Torque teno sus virus 2 (TTSuV2) in pigs experimentally infected with classical swine fever virus (CSFV). Virus Research, 172(1-2), 81-84. http://dx.doi.org/10.1016/j.virusres.2012.12.010. PMid:23274109.

Aramouni, M., Segalés, J., Cortey, M., & Kekarainen, T. (2010). Age- related tissue distribuition of swine Torque teno sus virus 1 and 2. Veterinary Microbiology, 146(3-4), 350-353. http://dx.doi.org/10.1016/j.vetmic.2010.05.036. PMid:20646878.

Balestrin, E., Wolf, J. M., Wolf, L. M., Fonseca, A. S. K., Ikuta, N., Siqueira, F. M., & Lunge, V. R. (2022). Molecular detection of respiratory coinfections in pig herds with enzootic pneumonia: A survey in Brazil. Journal of Veterinary Diagnostic Investigation, 34(2), 310-313. http://dx.doi.org/10.1177/10406387211069552. PMid:35034523.

Boom, R., Sol, C. J. A., Salimans, M. M., Jansen, C. L., Wertheim-van Dillen, P. M., & van der Noordaa, J. (1990). Rapid and simple method for purification of nucleic acids. Journal of Clinical Microbiology, 28(3), 495-503. http://dx.doi.org/10.1128/jcm.28.3.495-503.1990. PMid:1691208.

Brassard, J., Gagné, M. J., & Leblanc, D. (2013). Real-time PCR study of the infection dynamics of Torque teno sus viruses in naturally infected pigs from nursery to slaughterhouse. Veterinary Journal, 197(2), 506-508. http://dx.doi.org/10.1016/j.tvjl.2013.01.004. PMid:23395348.

Cortey, M., Pileri, E., Segalés, J., & Kekarainen, T. (2012). Globalisation and global trade influence molecular viral population genetics of Torque Teno Sus Viruses 1 and 2 in pigs. Veterinary Microbiology, 156(1-2), 81-87. http:// dx.doi.org/10.1016/j.vetmic.2011.10.026. PMid:22101091.

Cruz, A. C. M., Silveira, R. L., Baez, C. F., Varella, R. B., & Castro, T. X. (2016). Clinical aspects and weight gain reduction in swine infected with porcine circovirus type 2 and torque teno sus virus in Brazil. Veterinary Microbiology, 195, 154-157. http://dx.doi.org/10.1016/j.vetmic.2016.09.012. PMid:27771061.

Cruz, A. C., Rodrigues, I. L. F., Souza, A. E., Knackfuss, F. B., Silveira, R. L., & Castro, T. X. (2020). Molecular detection and clinical aspects of porcine circovirus 3 infection in pigs from Brazil. Arquivo Brasileiro de Medicina Veterinária, 72(5), 1731-1736. http://dx.doi.org/10.1590/1678-4162-11924.

Dal Santo, A. C., Cezario, K. C., Bennemann, P. E., Machado, S. A., & Martins, M. (2020). Full-genome sequences of porcine circovirus 3 (PCV3) and high prevalence in mummified fetuses from commercial farms in Brazil. Microbial Pathogenesis, 141, 104027. http://dx.doi.org/10.1016/j.micpath.2020.104027. PMid:32007620.

Ellis, J., Hassard, L., Clark, E., Harding, J., Allan, J., Willson, P., Strokappe, J., Martin, K., McNeilly, F., Meehan, B., Todd, D., & Haines, D. (1998). Isolation of circovirus from lesions of pigs with postweaning multisystemic wasting syndrome. The Canadian Veterinary Journal, 39(1), 44-51. PMid:9442952.

Kekarainen, T., & Segalés, J. (2012). Torque teno sus virus in pigs: An emerging pathogen? Transboundary and Emerging Diseases, 59(Suppl. 1), 103-108. http://dx.doi.org/10.1111/j.1865-1682.2011.01289.x. PMid:22252126.

Kim, J., & Chae, C. (2001). Optimized protocols for the detection of porcine circovirus 2 DNA from formalinfixed paraffin-embedded tissues using nested polymerase chain reaction and comparison of nested PCR with in situ hybridization. Journal of Virological Methods, 92(2), 105-111. http://dx.doi.org/10.1016/S0166- 0934(00)00255-X. PMid:11226557.

Ku, X., Chen, F., Li, P., Wang, Y., Yu, X., Fan, S., Qian, P., Wu, M., & He, Q. (2017). Identification and genetic characterization of porcine circovirus type 3 in China. Transboundary and Emerging Diseases, 64(3), 703-708. http://dx.doi.org/10.1111/tbed.12638. PMid:28317326.

Lee, S., Shin, J., Kim, C., & Lyoo, Y. S. (2012). Comparison of Torque Teno Sus Virus (TTSuV) viral load in Porcine Circovirus Type 2 vaccinated and non-vaccinated pig herds. Research in Veterinary Science, 93(2), 1039-1041. http://dx.doi.org/10.1016/j.rvsc.2011.10.021. PMid:22112638.

Lee, Y., Lin, C. M., Jeng, C. R., Chang, H. W., Chang, C. C., & Pang, V. F. (2015). The pathogenic role of torque teno sus virus 1 and 2 and their correlations with various viral pathogens and host immunocytes in wasting pigs. Veterinary Microbiology, 180(3-4), 186-195. http://dx.doi.org/10.1016/j.vetmic.2015.08.027. PMid:26390821.

Maes, D. (2012). Subclinical porcine circovirus infection: What lies beneath. Veterinary Journal, 194(1), 9. http:// dx.doi.org/10.1016/j.tvjl.2012.06.029. PMid:22819006.

Martínez-Guinó, L., Kekarainen, T., & Segalés, J. (2009). Evidence of Torque teno vírus (TTV) vertical transmission in swine. Theriogenology, 71(9), 1390-1395. http://dx.doi.org/10.1016/j.theriogenology.2009.01.010. PMid:19249089.

Molossi, F. A., Almeida, B. A., Cecco, B. S., Silva, M. S., Mósena, A. C. S., Brandalise, L., & Simão, G. M. R. (2022). A putative PCV3 associated disease in piglets from Southern Brazil. Brazilian Journal of Microbiology, 53(1), 491-498. http://dx.doi.org/10.1007/s42770-021-00644-7. PMid:34988935.

Oliver-Ferrando, S., Segalés, J., López-Soria, S., Callén, A., Merdy, O., Josiel, F., & Sibila, M. (2016). Evaluation of natural porcine circovirus type 2 (PCV2) subclinical infection and seroconversion dynamics in piglest vaccinated at different ages. Veterinary Research, 47(1), 121. http://dx.doi.org/10.1186/s13567-016-0405-2. PMid:27912792.

Opriessnig, T., Karuppannan, A. K., Castro, A. M. M. G., & Xiao, C. (2020). Porcine circoviruses: Current status, knowledge gaps and challenges. Virus Research, 286, 198044. http://dx.doi.org/10.1016/j.virusres.2020.198044. PMid:32502553.

Opriessnig, T., Meng, X. J., & Halbur, P. (2007). Porcine circovirus type 2- associated disease: Update on current terminology, clinical manifestations, pathogenesis, diagnosis, and intervention strategies. Journal of Veterinary Diagnostic Investigation, 19(6), 591-615. http://dx.doi.org/10.1177/104063870701900601. PMid:17998548.

Ouyang, T., Zhang, X., Liu, X., & Ren, L. (2019). Co- infection of swine with Porcine Circovirus Type 2 and other swine viruses. Viruses, 11(2), 185. http://dx.doi.org/10.3390/v11020185. PMid:30795620.

Paglis, J. R. (2013). Processamento de tecido em micro-ondas para o diagnóstico histopatológico e imunohistoquímico rápido de lesões em linfonodos de suínos na inspeção sanitária [Doctoral dissertation, Universidade Federal de Lavras, Faculdade de Veterinária].

Ramos, N., Mirazo, S., Botto, G., Teixeira, T. F., Cibulski, S. P., Castro, G., Cabrera, K., Roehe, P. M., & Arbiza, J. (2018). High frequency and extensive genetic heterogeneity of TTSuV1 and TTSuVk2a in PCV2 - infected and non-infected domestic pigs and wild boars from Uruguay. Veterinary Microbiology, 224, 78-87. http://dx.doi. org/10.1016/j.vetmic.2018.08.029. PMid:30269794.

Rodrigues, I. L. F., Cruz, A. C. M., Souza, A. E., Knackfuss, F. B., Costa, C. H. C., Silveira, R. L., & Castro, T. X. (2020). Retrospective study of porcine circovirus 3 (PCV3) in swine tissue from Brazil (1967–2018). Brazilian Journal of Microbiology, 51(3), 1391-1397. http://dx.doi.org/10.1007/s42770-020-00281-6. PMid:32347531.

Rogers, A. J., Huang, Y. W., Heffron, C. L., Opriessnig, T., Patterson, A. R., & Meng, X. J. (2017). Prevalence of the novel Torque teno Sus virus Species k2 from pigs in the United States and lack of association with postweaning multisystemic wastig sydrome or mulberry heart disease. Transboundary and Emerging Diseases, 64(6), 1877-1883. http://dx.doi.org/10.1111/tbed.12586. PMid:27878979.

Rosell, C., Segalés, J., & Domingo, M. (2000). Hepatitis and staging of hepatic damage in pigs naturally infected with Porcine Circovirus type 2. Veterinary Pathology, 37(6), 687-692. http://dx.doi.org/10.1354/vp.37-6-687. PMid:11105965.

Saraiva, G. L., Vidigal, P. M. P., Assao, V. S., Fajardo, M. L. M., Loreto, A. N. S., Fietto, J. L. R., Bressan, G. C., Lobato, Z. I. P., Almeida, M. R., & Silva-Junior, A. (2019). Retrospective detection and genetic characterization of porcine circovirus 3 (PCV-3) strains identified between 2006 and 2007 in Brazil. Viruses, 11(3), 201. http:// dx.doi.org/10.3390/v11030201. PMid:30818809.

Segalés, J. (2012). Porcine circovirus type 2 (PCV-2) infections: Clinical signs, pathology and laboratory diagnosis. Virus Research, 164(1-2), 10-19. http://dx.doi.org/10.1016/j.virusres.2011.10.007. PMid:22056845.

Shen, H., Liu, X., Zhang, P., Wang, L., Liu, Y., Zhang, L., Liang, P., & Song, C. (2018). Genome characterization of a porcine circovirus type 3 in South China. Transboundary and Emerging Diseases, 65(1), 264-266. http://dx.doi. org/10.1111/tbed.12639. PMid:28296271.

Sibila, M., Martinéz-Guinó, L., Huerta, E., Llorens, A., Mora, M., Grau-Roma, L., Kekarainen, T., & Segalés, J. (2009). Swine torque teno virus (TTV) infection and excretion dynamics in conventional pig farms. Veterinary Microbiology, 139(3-4), 213-218. http://dx.doi.org/10.1016/j.vetmic.2009.05.017. PMid:19559548.

Silva, M. S., Budaszewski, R. F., Weber, M. N., Cibulski, S. P., Paim, W. P., Mosena, A. C. S., Canova, R., Varela, A. P. M., Mayer, F. Q., Pereira, C. W., & Canal, C. W. (2020). Liver virome of healthy pigs reveals diverse small ssDNA viral genomes. Infection, Genetics and Evolution, 81, 104203. http://dx.doi.org/10.1016/j.meegid.2020.104203. PMid:32035977.

Webb, B., Rakibuzzaman, A. G. M., & Ramamoorthy, S. (2020). Torque teno viruses in health and disease. Virus Research, 285, 198013. http://dx.doi.org/10.1016/j.virusres.2020.198013. PMid:32404273.

Wilfred, E., Mutebi, F., Mwiine, F., James, O. A., & Lonzy, O. (2018). Porcine Circovirus type 2 - systemic disease on pig farms and associated knowledge of key players in the pig industry in Central Uganda. International Journal of Veterinary Science and Medicine, 6(2), 178-185. http://dx.doi.org/10.1016/j.ijvsm.2018.08.004. PMid:30564593.

Zanella, J. R. C., Morés, N., Simon, N. L., Oliveira, S. R., & Gava, D. (2006). Identification of porcine circovirus type 2 by polymerase chain reaction and immunohistochemistry on archived porcine tissues since 1988 in Brazil. Ciência Rural, 36, 1480-1485. http://dx.doi.org/10.1590/S0103-84782006000500021.

Zhai, S. L., Zhou, X., Zhang, H., Hause, B. M., Lin, T., Liu, R., Chen, Q. L., Wei, W. K., Lv, D. H., Wen, X. H., Li, F., & Wang, D. (2017). Comparative epidemiology of porcine circovirus type 3 in pigs with different clinical presentations. Virology Journal, 14(1), 222. http://dx.doi.org/10.1186/s12985-017-0892-4. PMid:29132394.

Creative Commons License

This work is licensed under a Creative Commons Attribution 4.0 International License.

Copyright (c) 2023 Amanda Eduarda de Souza, Ana Claudia de Menezes Cruz, Ingrid Lyrio Rodrigues, Eulógio Carlos Queiroz de Carvalho, Rafael Brandão Varella, Raphael Mansur Medina, Rachel Bittencourt Ribeiro Rodrigues, Renato Luiz Silveira, Tatiana Xavier de Castro