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Haemato-biochemical alterations and oxidative stress associated with naturally occurring porcine circovirus2 infection in pigs

Abstract

Porcine circovirus2 (PCV2) infection in pigs is one of the major causes of economic loss to the farmers in terms of low production, slow growth and increase post-weaning mortality rate. The effect of PCV2 infection on haemogram, serum biochemical profile and oxidant/anti-oxidant status is not well established in pigs. In the present study, haemogram, serum biochemical profile and oxidant/anti-oxidant status were assessed in pigs confirmed positive for PCV2 infections as evidenced by commercially available enzyme-linked immunosorbent assay kit (n = 151) and polymerase chain reaction (PCR) (n = 42) among a total of 306 number of pigs included in the study. Non-infected healthy pigs (n = 6) served as healthy control. The total erythrocyte count (TEC), haemoglobin (Hb), packed cell volume (PCV), total leukocyte count (TLC), differential leukocyte count (DLC) and thrombocyte count were measured. The levels of total protein, albumin, globulin, total bilirubin, direct bilirubin, blood urea nitrogen (BUN), creatinine and glucose and enzymes viz. alanine transaminase (ALT), aspartate transaminase (AST), gamma-glutamyl transferase (GGT) and alkaline phosphatase (ALP) were measured. Oxidative stress indicators such as plasma malondialdehyde (MDA) and total anti-oxidant activity (TAOA) were measured using commercially available kits. The mean values of TLC, lymphocytes and thrombocyte count were significantly (P < 0.05) low in PCV2-infected pigs. The levels of globulin, AST, GGT, BUN and creatinine were significantly increased (P < 0.05) whereas levels of albumin and glucose significantly (P < 0.05) decreased in PCV2-infected pigs. The significant increase (P < 0.05) in MDA level and significant decrease (P < 0.05) in TAOA level were noticed in PCV2-infected animals as compared with healthy control. The present study supports immunosuppression, possible multiple organ damage and oxidative stress associated with naturally occurring PCV2 infection in pigs. Timely vaccination and managemental practices can reduce PCV2 infection in farms. In spite of many research studies, there is still paucity of detailed systemic study on haemato-biochemical alteration and oxidative stress associated with PCV2 infection.

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References

  1. Afolabi, K.O., Iweriebor, B.C., Okoh, A.I., and Obi, L.C., 2017. Global Status of Porcine circovirus Type 2 and its Associated Diseases in Sub-Saharan Africa. Advances in Virology, 2017:1–16.

  2. Chen, X., Ren, F., Hesketh, J., Shi, X., Li, J., Gan, F. and Huang, 2012. Reactive oxygen species regulate the replication of porcine circovirus type 2 via, K NF-κB pathway. Virology, 426: 66–72.

  3. Chianini, F., Majo, N., Segale, S.J., Domínguez, J. and Domingo, M., 2003. Immunohistochemical characterisation of PCV2 associate lesions in lymphoid and non-lymphoid tissues of pigs with natural postweaning multisystemic wasting syndrome (PMWS). Veterinary Immunology and Immunopathology, 94: 63–75.

  4. Darwich, L., Balasch, M., Plana-Durá NJ., Segalé SJ., Domingo, M. and Mateu, E., 2003. Cytokine profiles of peripheral blood mononuclear cells from pigs with postweaning multisystemic wasting syndrome in response to mitogen, superantigen or recall viral antigens. Journal of General Virology, 84: 3453–3457.

  5. De, U.K., Mukherjee, R., Nandi, S., Patel, B.H.M., Dimri, U., Ravishankar, C. and Verma, A. K., 2014. Alterations in oxidant/antioxidant balance, high-mobility group box 1 protein and acute phase response in cross-bred suckling piglets suffering from rotaviral enteritis. Tropical Animal Health and Production, 46: 1127–1133.

  6. Dutton, T.L. and Larson, K.L., 2016. Porcine circovirus 3. Swine Health Information Center. Center for Food Security and Public Health. Iowa state University, 1-16.

  7. Duy, D.T., Huong, L.T.T. and Bryant, J.E., 2015. Porcine circovirus type 2 in Vietnam: Ruminations on a puzzling swine virus. Vietnam Journal of Preventive Medicine, XXV, 2: 8–22.

  8. Ellis, J., 2014. Porcine circovirus: a historical perspective. Veterinary Pathology, 51: 315–327.

  9. Ellis, J., Krakowka, S., Lairmore, M., Haines, D., Bratanich, A., Clark, E., Allan, G., Konoby, C., Hassard, L., Meehan, B. and Martin, K., 1999. Reproduction of lesions of postweaning multisystemic wasting syndrome in gnotobiotic piglets. Journal of Veterinary Diagnostic Investigation, 11: 3–14.

  10. Fenaux, M., Opriessnig, T., Halbur, P., Elvinger, F. and Meng, X-J., 2004. A Chimeric Porcine Circovirus (PCV) with the Immunogenic Capsid Gene of the Pathogenic PCV Type 2 (PCV2) Cloned into the Genomic Backbone of the Nonpathogenic PCV1 Induces Protective Immunity against PCV2 Infection in Pigs, Journal of Virology, 78: 6297–6303.

  11. Fu, Y., Jiang, L., Zhao, W., Xinan, M., Huang, S., Hu, T. and Chen, H., 2017. Immuno-modulatory and antioxidant effects of total flavonoids of Spatholobus suberectus Dunn on PCV2 infected mice, Scientific Reports, 7: 8676.

  12. Hou, X., Zhang, J., Ahmad, H., Zhang, H., Xu, Z. and Wang, T., 2014. Evaluation of antioxidant activities of ampelopsin and its protective effect in lipopolysaccharide-induced oxidative stress piglets. PloS one, 9: e108314.

  13. Huang, Y.Y., Walther, I., Martinson, S.A., López, A., Yason, C., Godson, D.L., Clark, E. G. and Simko, E., 2008. Porcine Circovirus 2 Inclusion Bodies in Pulmonary and Renal Epithelial Cells, Veterinary Pathology, 45: 640–644.

  14. Jiang, H., Wang, D., Wang, J., Zhu, S., She, R., Ren, X., Tian, J., Quan, R., Hou, L., Li, Z. and Chu, J., 2019. Induction of porcine dermatitis and nephropathy syndrome in piglets by infection with porcine circovirus type 3. Journal of virology, 93: e02045–18.

  15. Kikon, L.J., Rajkhowa T.K., Arya, R.S., Singh, Y.D. and Ravindran, R., 2017. Seroprevalence of porcine circovirus type-2 (PCV2) and molecular diagnosis of PCV2 associated reproductive failure in pig population of Nagaland. Indian Journal of Veterinary Pathology, 41: 79–83.

  16. Kim, Y.J., Kim, E.H. and Hahm, K.B., 2012. Oxidative stress in inflammation-based gastrointestinal tract diseases: Challenges and opportunities. Journal of Gastroenterology and Hepatology, 27: 1004–1010.

  17. Krakowka, S., Ellis, J., McNeilly, F., Meehan, B., Oglesbee, M., Alldinger, S. and Allan, G., 2004. Features of cell degeneration and death in hepatic failure and systemic lymphoid depletion characteristic of porcine circovirus-2-associated postweaning multisystemic wasting disease. Veterinary Pathology, 41: 471–481.

  18. Kumar, S.K., Selvaraj, R., Hariharan, T., Chanrahassan, C. and Reddy, Y.K.M., 2014. Porcine Circovirus - 2 An Emerging Disease of Crossbred Pigs in Tamil Nadu, India. International Journal of Science, Environment and Technology, 3: 1268–1272.

  19. Liu, D., Lin, J., Su, J., Chen, X., Jiang, P. and Huang, K., 2018. Glutamine deficiency promotes PCV2 infection through induction of autophagy via activation of ROS-mediated JAK2/STAT3 signaling pathway. Journal of agricultural and food chemistry, 66: 11757–11766.

  20. Marks, F.S., Reck, J Jr., Almeida, L.L., Berger, M., Correa, A.M., Driemeier, D., Barcellos, D.E., Guimaraes J.A., Termignoniet C. and Canal, C. W., 2010. Porcine circovirus 2 (PCV2) induces a procoagulant state in naturally infected swine and in cultured endothelial cells. Veterinary Microbiology, 141: 22–30.

  21. Meng, X.J., 2012. Spread like a wildfire--the omnipresence of porcine circovirus type 2 (PCV2) and its ever-expanding association with diseases in pigs. Virus Research, 164: 1–3.

  22. Meng, X.J., 2013. Porcine circovirus type 2 (PCV2): pathogenesis and interaction with the immune system. Annual Review of Animal Biosciences, 1: 43–64.

  23. Mukherjee, P., Karam, A., Singh, U., Chakraborty, A.K., Huidrom, S., Sen, A. and Sharma I., 2018. Seroprevalence of selected viral pathogens in pigs reared in organized farms of Meghalaya from 2014 to 16. Veterinary World, 11: 42–47.

  24. Nielsen, J., Vincent, I.E., Bøtner, A., Ladekjær-Mikkelsen, A.S., Allan, G., Summerfield, A. and McCullough, K.C., 2003. Association of lymphopenia with porcine circovirus type 2 induced postweaning multisystemic wasting syndrome (PMWS). Veterinary immunology and immunopathology, 92: 97–111.

  25. João X. Oliveira Filho, Daphine A.J. de Paula, Nelson Morés, Caroline A. Pescador, Janice R. Ciacci-Zanella, Arlei Coldebella, Valéria Dutra, Luciano Nakazato, 2012. Interstitial nephritis of slaughtered pigs in the state of Mato Grosso, Brazil. Pesquisa Veterinária Brasileira, 32: 313–318.

  26. Opriessnig, T.I., 2006. Understanding the pathogenesis of porcine circovirus type 2 (PCV2) associated diseases, Thesis, PhD. Iowa State University, United States, 18–22.

  27. Ouyang, T., Zhang, X., Liu, X. and Ren, L., 2019. Co-Infection of Swine with Porcine Circovirus Type 2 and Other Swine Viruses. Viruses, 11: 185.

  28. Parra, M. D., Fuentes, P., Tecles, F., Martínez-Subiela, S., Martínez, J. S., Muñoz, A. and Cerón, J. J., 2006. Porcine Acute Phase Protein Concentrations in Different Diseases in Field Conditions. Journal of Veterinary Medicine, 53: 488–493.

  29. Patterson, A.R., Madson, D.M., Halbur, P.G. and Opriessnig, T., 2011. Shedding and infection dynamics of porcine circovirus type 2 (PCV2) after natural exposure. Veterinary Microbiology, 149: 225–29.

  30. Plagemann, P.G.W., Rowland, R.R.R. and Cafruny, W.A., 2005. Polyclonal hypergamaglobulinaemia and formation of hydrophobic immune complexes in porcine reproductive and respiratory syndrome virus-infected and uninfected pigs, Viral Immunology, 18: 138–147.

  31. Qian, G., Liu, D., Hu, J., Gan, F., Hou, L., Chen, X. and Huang, K., 2017. Ochratoxin A-induced autophagy in vitro and in vivo promotes porcine circovirus type 2 replication. Cell death & disease, 8: e2909.

  32. Rajesh, J.B., Rajkhowa, S., Dimri, U., Prasad, H., Pegu, S.R., Saikia, P., Chethan, G.E., Zosangpuii, Choudhury M. and Ajith, Y., 2019. Seroprevalence of PCV2 in north eastern hill states of India. Indian Journal of Animal Sciences, 89: 119–122.

  33. Resendes, A.R., Majo, M., Ingh, T.S.G.A.M., Mateu, E., Domingo, M., Calsaminglia, M. and Segalés, J., 2011. Apoptosis in postweaning multisystemic wasting syndrome (PMWS) hepatitis in pigs naturally infected with porcine circovirus type 2 (PCV2). Veterinary Journal, 189: 72–76.

  34. Rigobelo, E. C. and Ávila, F. A., 2011. Hypoglycemia Caused by Septicemia in Pigs. Hypoglycemia - Causes and Occurrences, (In Tech Europe: Croatia), 221-238.

  35. Rosell, C., Segalés, J. and Domingo, M., 2000. Hepatitis and Staging of Hepatic Damage in Pigs Naturally Infected with Porcine Circovirus Type 2, Veterinary Pathology, 37: 687–692.

  36. Sarli, G., Mandrioli, L., Panarese, S., Brunetti, B., Segalés, J., Domínguez, J. and Marcato, P. S., 2008. Characterization of Interstitial Nephritis in Pigs with Naturally Occurring Postweaning Multisystemic Wasting Syndrome, Veterinary Pathology, 45: 12–18.

  37. Segales, J., 2012. Porcine circovirus type 2 (PCV2) infections: clinical signs, pathology and laboratory diagnosis. Virus research, 164: 10–19.

  38. Segales, J. and Domingo, M., 2002. Postweaning multisystemic wasting syndrome (PMWS) in pigs. A review. Veterinary Quarterly, 24: 109–124.

  39. Segales, J., Rosell, C. and Domingo, M., 2004. Pathological findings associated with naturally acquired porcine circovirus type 2 associated disease. Veterinary Microbiology, 98: 137–149.

  40. Sorden, S.D., 2000. Diagnostic notes. Update on porcine circovirus and postweaning multisystemic wasting syndrome (PMWS). Swine Health Production. 8: 133–136.

  41. Stukelj, M., Toplak, I. and Nemec, S.A., 2013. Antioxidant enzymes (SOD, GPX), biochemical and haematological parameters in pigs naturally infected with porcine reproductive and respiratory syndrome virus. Polish Journal of Veterinary Science, 16: 369–376.

  42. Valyi-Nagy, T. and Dermody, T.S., 2005. Role of oxidative damage in the pathogenesis of viral infections of the nervous system. Histology and Histopathology, 20: 957–967.

  43. Wang, J., Sun, Z., Jiang, J., Wu, D., Liu, X., Xie, Z., Chen, E., Zhu, D., Ye, C., Zhang, X., Chen, W., Cao, H. and Li, L., 2017. Proteomic Signature of Acute Liver Failure: From Discovery and Verification in a Pig Model to Confirmation in Humans. Molecular & Cellular Proteomics, 16: 1188–1199.

  44. Wei, Y.Y., Hu, T.J., Su, Z.J., Zeng, Y., Wei, X.J. and Zhang, S.X., 2012. Immunomodulatory and antioxidant effects of carboxymethylpachymaran on the mice infected with PCV2. International Journal of Biological Macromolecules. 50: 713–719.

  45. Yang, Y., Shi, R., She, R., Mao, J., Zhao, Y., Du, F., Liu, C., Liu, J., Cheng, M., Zhu, R. and Li, W., 2015. Fatal disease associated with Swine Hepatitis E virus and Porcine circovirus 2 co-infection in four weaned pigs in China. BMC Veterinary Research, 11: 77.

  46. Zhai, N., Liu, K., Li, H., Liu, Z., Wang, H., Korolchuk, V.I., Carroll, B., Pan, C., Gan, F., Huang, K. and Chen, X., 2019. PCV2 replication promoted by oxidative stress is dependent on the regulation of autophagy on apoptosis. Veterinary Research, 50: 19.

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Correspondence to J. B. Rajesh.

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Rajesh, J.B., Rajkhowa, S., Dimri, U. et al. Haemato-biochemical alterations and oxidative stress associated with naturally occurring porcine circovirus2 infection in pigs. Trop Anim Health Prod (2020). https://doi.org/10.1007/s11250-020-02247-0

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Keywords

  • PCV2
  • ELISA
  • PCR
  • Haemogram
  • MDA
  • TAOA