Abstract
The haemato-biochemical indices and oxidative stress markers in horses naturally infected with Trypanosoma evansi were evaluated by analyzing the level of these parameters between T. evansi infected (microscopically positive patent group and PCR positive latent group) and infection free horses. To compare the hemato-biochemical indices and oxidative stress indicators, horses were divided into three categories based on diagnostic test employed and positive results obtained. These included Romanowsky stained slide positive group (Group I; n = 6), PCR positive group (group II; n = 28) and negative control group (group III, n = 30), revealing parasitologically positive patent, molecular positive latent and disease free status of horses. A significant reductions in total erythrocytes count (TEC, P = 0.01), haemoglobin (Hb, P = 0.01) and packed cell volume (PCV, P = 0.04) was noticed both in group I and group II while significant neutrophilia and lymphocytopenia was observed in group I when compared to negative control group. Substantial increase in creatinine (CRTN, P = 0.032) and gamma glutamyl transferase (GGT, P = 0.012) in group I while significant decrease in glucose (GLU, P = 0.04) and iron (Fe, P = 0.01) were noticed in both group I and group II in comparison to group III. A significant difference in lipid peroxides (LPO, P = 0.01) with highest level in patent group I (15.33 ± 0.53) followed by PCR positive latent group (14.09 ± 1.66) indicates higher lipid peroxidation in erythrocytes and oxidative stress in decreasing order when compared with infection free control horses (9.83 ± 0.97). Catalase (CAT, P = 0.01) was significantly lower in parasitological (0.82 ± 0.14) and molecular positive cases (1.27 ± 0.35) in comparison to control group (3.43 ± 0.96). The levels of superoxide dismutase (SOD, P = 0.01), reduced glutathione (GSH, P = 0.01) and ferric reducing antioxidant power (FRAP, P = 0.01) were significantly lower in parasito-molecular positive cases as compared to infection free control horses. An inverse correlation of RBC count with LPO and GSH and a direct correlation with catalase, SOD and FRAP was revealed. Overall, the observed substantial decreases in the oxidative parameters like catalase CAT, SOD, GSH and FRAP activities with remarkably elevated levels of LPO indicate high exposure of erythrocytes to oxidative damage in T.evansi infected horses.
Conflict of interest. None of the authors of this paper has a financial or personal relationship with other people or organizations that could in appropriately influence or bias the content of the paper.
Acknowledgements
Thanks are due to the Authorities of Guru Angad Dev Veterinary and Animal Sciences University for providing financial support to carry out the research work.
References
Abd El-Baky A. A., Salem S.I. 2011. Clinicopathological and cytological studies on naturally infected camels and experimentally infected rats with Trypanosoma evansi. World Applied Sciences Journal, 14, 42–50Search in Google Scholar
Abenga J.N., Anosa V.O. 2007. Serum biochemical changes in experimental gambian trypanosomosis. II. Assessing hepatic and renal dysfunction. Turkish Journal of Veterinary and Animal sciences, 31, 293–296Search in Google Scholar
Adejinmi J.O., Akinboade O.A. 2000. Serum biochemical changes in WAD goats with experimental mixed Trypanosoma brucei and Cowdria ruminantum infections. Tropical Veterinarian, 18, 111–120Search in Google Scholar
Aebi H.E. 1983. Catalase. In: Bergmeyer, H.U., Ed., Methods of enzymatic analysis, Verlag Chemie, Weinhem. 273–286. 10.1016/B978-0-12-091302-2.50032-3Search in Google Scholar
Akanji M.A., Adeyemi O.S., Oguntoye S.O., Suleiman F. 2009. Psidium guavaja extract reduces trypanosomosis associated lipid peroxidation and raised glutathione concentrations in infected animals. Excli Journal, 8,148–154Search in Google Scholar
Amanvermez R., Celik C. 2004. Superoxide dismutase, glutathione, vitamin C, total antioxidant and total thiol levels in hydatid cysts. Turkiye Klinikleri Journal of Medical Sciences, 24, pp. 2 13Search in Google Scholar
Anosa V.O. 1988. Haematological and biochemical changes in human and animal trypanosomosis. Part I. Revue d’élevage et de Médecine Vétérinaire des pays Tropicaux, 41, 65–78Search in Google Scholar
Auten R.L., Davis J.M. 2009. Oxygen toxicity and reactive oxygen species: the devil is in the details. Pediatric Research, 66, 121–127. 10.1203/PDR.0b013e3181a9eafbSearch in Google Scholar
Bal M.S., Sharma A., Ashuma Bath B.K., Kaur P., Singla L.D. 2014. Detection and management of latent infection of Trypanosoma evansi in a cattle herd. Indian Journal of Animal Research, 48, 31–37. 10.5958/j.0976-0555.48.1.007Search in Google Scholar
Benzie I.F.F., Strain J.J. 1999. Ferric reducing/antioxidant power assay: direct measure of total antioxidant activity of biological fluids and modified version for simultaneous measurement of total antioxidant power and ascorbic acid concentration. Methods in Enzymology, 299, 15–27. 10.1016/S00766879 (99)99005-5Search in Google Scholar
Brun R., Hecker H., Lun Z., 1998. Trypanosoma evansi and T. equiperdum: distribution, biology, treatment and phylogenetic relationship. Veterinary Parasitology, 79, 95–107. 10.1016/S0304-4017 (98)00146-0Search in Google Scholar
Bulger E.M., Maier R.V. 2001. Antioxidants in critical illness. Archives of Surgery, 136, 1201–1207. 10.1001/archsurg.136.10.1201Search in Google Scholar
Cadioli F.A., Marques L.C., Machado R.Z., Alessi A.C., Aquino L.P.C.T., Barnabé P.A. 2006. Experimental Trypanosoma evansi infection in donkeys: hematological, biochemical and histopathological changes. Arquivo Brasileiro de Medicina Veterinária e Zootecnia, 58, 749–756. 10.1590/S010209352006000500008Search in Google Scholar
Chaudhary Z.I., Iqbal J. 2000. Incidence and haematological alterations induced by natural trypanosomiasis in racing dromedary camels. Acta Tropica, 77, 209–213. DOI.org/10.1016/S0001-706X(00)00142-X10.1016/S0001-706X(00)00142-XSearch in Google Scholar
Chaudhuri S., Varshney J.P., Patra R.C. 2008. Erythrocytic antioxidant defense, lipid peroxides level and blood iron, zinc and copper concentrations in dogs naturally infected with Babesia gibsoni. Research in Veterinary Science, 85, 120–124. 10.1016/j.rvsc.2007.09.001Search in Google Scholar PubMed
Dargie J.D., Murray P.K., Murray M., Grimshaw W.R.T., McIntyre W.I.M. 1979. Bovine trypanosomiasis: the red cell kinetics of Ndama and Zebu cattle infected with Trypanosoma congolense. Parasitology International, 78, 271–286. 10.1017/S0031182000051143Search in Google Scholar PubMed
De U.K., Dey S., Banerjee P.S., Sahoo M. 2012. Correlations among Anaplasma marginale parasitemia and markers of oxidative stress in crossbred calves. Tropical Animal Health and Production, 44, 385–8. 10.1007/s11250-011-9938-6Search in Google Scholar
Demerdash F.M., Jebur A.B., Nasr H.M. 2013. Oxidative stress and biochemical perturbations induced by insecticides mixture in rat testes. Journal of Environmental Science and Health, 48, 593–599. 10.1080/03601234.2013.774998Search in Google Scholar
Dimri U., Sharma M.C., Yamdagni A., Ranjan R., Zama M.M.S. 2010. Psoroptic mange infestation increases oxidative stress and decreases antioxidant status in sheep. Veterinary Parasitology, 168, 318–322. 10.1016/j.vetpar.2009.11.013Search in Google Scholar
Dobson R.J., Dargantes A.P., Mercado R.T., Reid S.A. 2009. Models for Trypanosoma evansi (surra), its control and economic impact on small-hold livestock owners in the Philippines. International Journal for Parasitology, 39, 1115–1123. 10.1016/j.ijpara.2009.02.013Search in Google Scholar
Egbu F.M.I., Ubachukwu P.O., Okoye I.C. 2013. Haematological changes due to bovine fasciolaisis. African Journal of Biotechnology, 12, 1828–1835. 10.5897/AJB12.2716.Search in Google Scholar
Esmaeilnejad B., Tavassoli M., Asri-Rezaei S., Dalir-Naghadeh B. 2012. Evaluation of antioxidant status and oxidative stress in sheep naturally infected with Babesia ovis. Veterinary Parasitology, 185, 124–30. 10.1016/j.vetpar.2011.10.001Search in Google Scholar
Eyob E., Matios L. 2013. Review on camel trypanosomosis (surra) due to Trypanosoma evansi: Epidemiology and host response. Journal of Veterinary Medicine and Animal Health,5, 334– 343. DOI. 10.5897/JVMAH2013.023610.5897/JVMAH2013.0236Search in Google Scholar
Fang Y.Z., Yang S., Wu G. 2002. Free radicals, antioxidants, and nutrition. Nutrition, 18, 872–879. 10.1016/S0899-9007(02) 00916-4Search in Google Scholar
Fridovich I. 1995. Superoxide radical and superoxide dismutases. Annual Review of Biochemistry, 64, 97–112. 10.1146/annurev.bi.64.070195.000525Search in Google Scholar PubMed
Gill B.S. 1977. Trypanosomes and trypanosomiases of Indian livestock. Information Division Indian Council of Agricultural Research; New DelhiSearch in Google Scholar
Gurbay A., Hıncal F.2004. Ciprofloxacin-induced glutathione redox status alterations in rat tissues. Drug and Chemical Toxicology, 27, 233–42. 10.1081/DCT-120037504Search in Google Scholar PubMed
Gutierrez C., Corbera J. A., Juste M.C., Doreste F., Morales I. 2005. An outbreak of abortions and high neonatal mortality associated with Trypanosoma evansi infection in dromedary camels in the Canary Islands. Veterinary Parasitology, 30, 163–168. 10.1016/j.vetpar.2005.02.009Search in Google Scholar
Gutteridge J.M. 1995. Lipid peroxidation and antioxidants as biomarkers of tissue damage. Clinical Chemistry, 41,1819–182810.1093/clinchem/41.12.1819Search in Google Scholar
Gutteridge J., Halliwell B. 2000. Free radicals and antioxidants in the year 2000: a historical look to the future. Annals of the New York Academy of Sciences, 899, 136–147. 10.1111/j.1749-6632.2000.tb06182.xSearch in Google Scholar
Jatkar P.R., Singh M. 1974. Pathogenesis of anemia in trypanosome infection. IV. Blood glucose studies. Indian Veterinary Journal, 51, 710–714Search in Google Scholar
Kahn C.M., Line S. 2010. The Merck Veterinary Manual, 10th ed. Merck & Co. Inc 2584–89Search in Google Scholar
Kaplowitz N. 2000. Mechanisms of liver cell injury. Journal of Hepatology, 32, 39–47. 10.1016/S0168-8278(00)80414-6Search in Google Scholar
Kumar R., Jain S., Kumar S., Sethi K., Kumar S., Tripathi B. N. 2017. Impact estimation of animal trypanosomosis (surra) on livestock productivity in India using simulation model: Current and future perspective. Veterinary Parasitology: Regional Studies and Reports, 10, 1–12. 10.1016/j.vprsr.2017. 06.008Search in Google Scholar
Kurt O., Ok U.Z., Ertan P., Yuksel H. 2002. Antioxidant substances and malaria. Acta Parasitologica Turcica. 26, 108–12Search in Google Scholar
Li M., You T.Z., Zhu, W.Z., Qu J.P., Liu C., Zhao B., et al. 2013. Antioxidant response and histopathological changes in brain tissue of pigeon exposed to avermectin. Ecotoxicology, 22, 1241–1254. 10.1007/s10646-013-1112-7Search in Google Scholar
Luckins A.G. 1988. Trypanosoma evansi in Asia. Parasitology Today 4, 137–142. 10.1016/0169-4758 (88)90188-3Search in Google Scholar
Marklund S., Marklund G. 1974. Involvement of the superoxide anion radical in the autooxidation of pyrogallol and a convenient assay for superoxide dismutase. European Journal of Biochemistry, 47, 469–47410.1111/j.1432-1033.1974.tb03714.xSearch in Google Scholar
Masiga D.K., Smyth A.J., Hayes P., Bromidge T.J., Gibson W.C. 1992. Sensitive detection of trypanosomes in tsetse flies by DNA amplification. International Journal of Parasitology, 22, 909–918. 10.1016/0020-7519(92)90047-OSearch in Google Scholar
Mates J.M., Perez-Gomez C., De Castro I.N. 1999. Antioxidant enzymes and human diseases. Clinical Biochemistry, 32, 595– 603. 10.1016/S0009-9120(99)00075-2Search in Google Scholar
Meister A., Anderson M.E. 1983. Glutathione. Annual Review of Biochemistry, 52, 711–76010.1146/annurev.bi.52.070183.003431Search in Google Scholar PubMed
Mijares A., Vivas J., Abad C., Betancourt M., Piñero S., Proverbio F., Marín R., Portillo R. 2010. Trypanosoma evansi: Effect of experimental infection on the osmotic fragility, lipid peroxidation and calcium- ATPase activity of rat red blood cells. Experimental Parasitology, 124, 301–305. 10.1016/j.exppara.2009.11.002Search in Google Scholar PubMed
Murray R.K., Granner D.K., Mayes P.A, Rodwell V.W. 2003. Harper’s Illustrated Biochemistry a Lange Medical Book, 26th ed. The McGraw-Hill Companies, Inc., United States of America, pp. 622–701Search in Google Scholar
Omer O.H., Mousa H.M., Al-Wabel N. 2007. Study on the antioxidant status of rats experimentally infected with Trypanosoma evansi. Veterinary Parasitology, 145, 142–145. 10. 1016/j.vetpar.2006.11.007Search in Google Scholar
Ozden S., Catalgol B., Gezginci-Oktayoglu S., Arda-Pirincci P., Bolkent S., Alpeortunga B. 2009. Methiocarb-induced oxidative damage following subacute exposure and the protective effects of vitamin E and taurine in rats. Food and Chemical Toxicology, 47, 1676–1684. 10.1016/j.fct. 2009.04.018Search in Google Scholar
Padmaja K. 2012. Haemato-biochemical studies and therapy of trypanosomosis in camels. Veterinary World, 5, 356–35810.5455/vetworld.2012.356-358Search in Google Scholar
Pamplona R., Costantini D. 2011. Molecular and structural antioxidant defenses against oxidative stress in animals. American Journal of Physiology-Regulatory, Integrative and Comparative Physiology, 301, R843–R863. 10.1152/ajpregu. 00034.2011Search in Google Scholar
Pandey V., Nigam R., Jaiswal A.K., Sudan V., Singh R.K., Yadav P.K. 2015. Haemato–biochemical and oxidative status of buffaloes naturally infected with Trypanosoma evansi. Veterinary Parasitology, 212,118–122. 10.1016/j.vetpar.2015.07.025Search in Google Scholar PubMed
Parashar R. 2014. Prevalence of trypanosomiosis, its clinicohaemato-biochemical impact and PCR based detection in buffaloes. MVSc Thesis, DUVASU MathuraSearch in Google Scholar
Prins H.K., Loos J.A. 1969. Glutathione In: Biochemical Methods in Red Cell Genetics. (Edited byYunis, J.J.), Academic Press, New York. pp. 115–137Search in Google Scholar
Ranjithkumar M., Kamili N.M., Saxena A., Dan A., Dey S., Raut S.S. 2011. Disturbance of oxidant/antioxidant equilibrium in horses naturally infected with Trypanosoma evansi. Veterinary Parasitology, 180, 349–353. 10.1016/j.vetpar. 2011.03.029Search in Google Scholar
RehmanS., Chandra O., Abdulla M. 1995. Evaluation of malondialdehyde as an index of lead damage in rat brain homogenates. Biometals, 8, 275–27910.1007/BF00141599Search in Google Scholar PubMed
Rezai S.A., Dalir-NaghadehB. 2006. Evaluation of antioxidant status and oxidative stress in cattle naturally infected with Theileria annulata. Veterinary Parasitology, 142:179–18610.1016/j.vetpar.2006.05.033Search in Google Scholar PubMed
Saker K.E. 2006. Nutrition and immune function. Veterinary Clinics of North America: Small Animal Practice, 36, 1199–1224. 10.1016/j.cvsm.2006.09.001Search in Google Scholar PubMed
Saleh M.A., Al-Salahy M.B., Sanousi S.A. 2009. Oxidative stress in blood of camels (Camelus dromedaries) naturally infected with Trypanosoma evansi. Veterinary Parasitology, 162, 192– 199. 10.1016/j.vetpar.2009.03.035Search in Google Scholar PubMed
Sarror D.I. 1976. Plasma copper levels in bovine trypanosomosis. Veterinary Record, 98, pp.19610.1136/vr.98.10.196Search in Google Scholar PubMed
SAS. 2002. Statistical Analysis System. User’s Guide. SAS Institute Inc., Cary, USASearch in Google Scholar
Sharma A., Singla L.D., Tuli A., Kaur P., Bal M.S. 2015. Detection and assessment of risk factors associated with natural concurrent infection of Trypanosoma evansi and Anaplasma marginale in dairy animals by duplex PCR in eastern Punjab. Tropical Animal Health and Production, 47, 251–257. 10.1007/s11250-014-0710-6Search in Google Scholar PubMed
Sharma P., Juyal P.D., Singla L.D., Chachra D., Pawar H. 2012. Comparative evaluation of real time PCR assay with conventional parasitological techniques for diagnosis of Trypanosoma evansi in cattle and buffaloes. Veterinary Parasitology, 190, 375–382. DOI.org/10.1016/j.vetpar.2012.07.00510.1016/j.vetpar.2012.07.005Search in Google Scholar PubMed
SinghV., Tiwari A.K. 2012. Bovine Surra in India: an update. Ruminant Science, 1,1–7Search in Google Scholar
Singla L.D., Juyal P.D., Ahuja S.P. 1998. Blood brain barrier status in experimental Trypanosoma evansi infected and levamisole treated cow-calves. Indian Veterinary Journal, 75, 109–12Search in Google Scholar
Singla L.D., Juyal P.D., Roy K.S., Kalra I.S. 1997. Host responses of cow-calves against Trypanosoma evansi infection: Haematopathological study. Journal of Veterinary Parasitology 11, 55–63Search in Google Scholar
Singla L.D., Sharma A., Kaur P., Bal M.S. 2015. Comparative evaluation of agglutination assay with microscopy and polymerase chain reaction for detection of Trypanosoma evansi in bovines of Punjab. Indian Journal of Animal Sciences, 85, 1164–1166Search in Google Scholar
Sivajothi S., Rayulu V.C., Reddy B.S. 2013. Haematological and biochemical changes in experimental Trypanosoma evansi infection in rabbits. Journal of Parasitic Diseases. 10.1007/s12639-013-0321-6Search in Google Scholar PubMed PubMed Central
Sivajothi S., Rayulu V.C., Reddy B.S., Kumari K.N. 2015. Trypanosoma evansi causes thyroxin imbalance with biochemical alterations in wistar rats. Journal of Advanced Veterinary and Animal Research, 2, 205–209. 10.5455/javar. 2015.b68Search in Google Scholar
Spickett C.M., Jerlich A., Panasenko O.M., Arnhold J., Pitt A.R., Stelmaszyñska T., Schaur R.J. 2000. The reactions of hypochlorous acid, the reactive oxygen species produced by myeloperoxidase, with lipids. Acta Biochimica Polonica, 47, 889–90010.18388/abp.2000_3944Search in Google Scholar
Sumbria D., Singla L.D., Sharma A., Moudgil A.D., Bal M.S. 2014. Equine trypanosomosis in central and western Punjab: Prevalence, haemato-biochemical response and associated risk factors. Acta Tropica, 138, 44–50. 10.1016/j.actatropica. 2014.06.003Search in Google Scholar
Sumbria D., Singla L.D., Sharma A., Bal M.S., Kumar S. 2015. Multiplex PCR for detection of Trypanosoma evansi and Theileria equi in equids of Punjab, India. Veterinary Parasitology, 211, 293–99. 10.1016/j.vetpar.2015.05.018Search in Google Scholar PubMed
Taiwo V.O., Olaniyi M.O. and Ogunsanmi A.O. 2003. Comparative plasma biochemical changes and susceptibility of erythrocytes to in vitro peroxidation during experimental Trypanosoma congolense and T. brucei infections in sheep. Israel Journal of Veterinary Medicine, 112–117Search in Google Scholar
Takeet M.I., Adeleye A.I., Adebayo O.O., Akande F.A. 2009. Haematology and serum biochemical alteration in stress induced equine theileriosis. A case report. The Scientific World Journal, 4, 19–21. 10.4314/swj.v4i2.51840Search in Google Scholar
Takeet M.I., Fagbemi B.O. 2009. Haematological, pathological and plasma biochemical changes in rabbits experimentally infected with Trypanosoma congolense. The Scientific World Journal, 4. 10.4314/swj.v4i2.51843Search in Google Scholar
Weinberg E.D. 1978. Iron and infection. Microbiological Reviews. 42, 45–6610.1128/mr.42.1.45-66.1978Search in Google Scholar PubMed PubMed Central
Wolkmer P., da Silva A.S., Traesel C.K., Paim F.C., Cargnelutti J.F., Pagnoncelli M., Picada M.E., Monteiro S.G., dos Anjos Lopes S.T. 2009. Lipid peroxidation associated with anemia in rats experimentally infected with Trypanosoma evansi. Veterinary Parasitology, 165, 41–46. 10.1016/j.vetpar.2009.06.032Search in Google Scholar PubMed
Wolkmer P., Schafer da Silva A., Felipetto Cargnelutti J., Machado Costa M., Kist Traesel C., dos Anjos Lopes S., Gonzalez Monteiro S. 2007. Resposta eritropoética de ratos em diferentes graus de parasitemia por Trypanosoma evansi. Ciencia Rural. 37, 1682–168710.1590/S0103-84782007000600027Search in Google Scholar
Xing H., Li S., Wang Z., Gao X., Xu S., Wang X. 2012. Oxidative stress response and histopathological changes due to atrazine and chlorpyriphos exposure in common carp. Pesticide Biochemistry and Physiology, 103, 74–80. 10.1016/j.pestbp.2012.03.007Search in Google Scholar
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