Skip to main content
Log in

Evaluation of erythrocyte antioxidant mechanisms: antioxidant enzymes, lipid peroxidation, and serum trace elements associated with progressive anemia in ovine malignant theileriosis

  • Original Paper
  • Published:
Parasitology Research Aims and scope Submit manuscript

Abstract

Ovine malignant theileriosis is a fatal disease that is characterized by severe progressive anemia. In order to elucidate the underlying mechanisms involved in anemia, this study was designed to assess the antioxidant status and erythrocyte oxidative injuries in Iranian fat-tailed sheep that suffered from malignant theileriosis. The infected animals (infected group), composed of 50 Iranian sheep about 1–2 years old, naturally infected with Theileria sp., were divided into three subgroups according to parasitemia rates (<1%, 1–3%, 3–5%), and ten non-infected animals were also selected as the control group. Blood samples were taken and hematological parameters, the activities of antioxidant enzymes including superoxide dismutase (SOD), glutathione peroxidase (GPX) and catalase, erythrocyte osmotic fragility, and serum concentrations of some trace elements (copper, iron, zinc, manganese, and selenium), were measured. As an index of lipid peroxidation, the level of malondialdehyde (MDA) was also determined. According to the results, a significant decrease in red blood cell (RBC) count, packed cell volume, the activities of SOD, GPX, and catalase (P < 0.001), and also serum concentrations of Cu, Zn, Mn, and Se (P < 0.05) were evident in the infected sheep. In contrast, significantly increased levels of MDA and erythrocyte osmotic fragility (P < 0.001) as well as serum concentration of iron (P < 0.05) were recorded in the infected animals. The significant decrease in antioxidant enzyme activities and substantial elevated levels of lipid peroxidation and erythrocyte osmotic fragility associated with the increase in parasitemia indicate increased exposure of RBCs to oxidative damage. Also, it appears that disturbed antioxidant defense mechanisms can promote the development of anemia in ovine theileriosis.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Aihara K, Nishi Y, Hatano S, Kihara M, Yoshimitsu K, Takeichi N, Ito H, Ezaki H, Usui T (1984) Zinc, copper, manganese, and selenium metabolism in thyroid disease. Am J Clin Nutr 40:26–35

    PubMed  CAS  Google Scholar 

  • Asri Rezaei S, Dalir-Naghadeh B (2006) Evaluation of antioxidant status and oxidative stress in cattle infected with Theileria annulata. Vet Parasitol 142:179–186

    Article  PubMed  CAS  Google Scholar 

  • Bouman AA, Platenkamp AJ, Posma FD (1986) Determination of cobalt in urine by flameless atomic absorption spectroscopy. Comparison of direct analysis using Zeeman background correction and indirect analysis using extraction in organic solution. Ann Clin Biochem 23:346–350

    PubMed  CAS  Google Scholar 

  • Brown CGD, Hunter AG, Luckins AG (1990) Diseases caused by protozoa. In: Sewell MMH, Brocklesby DW (eds) Handbook on animal diseases in the tropics. Bailliere Tindall, London, pp 161–226

    Google Scholar 

  • Chanarin I (1989) Laboratory haematology: an account of laboratory techniques. Churchill Livingstone, New York

    Google Scholar 

  • Chance B, Sies H, Boveris A (1979) Hydroperoxide metabolism in mammalian organs. Physiol Rev 59:527–605

    PubMed  CAS  Google Scholar 

  • Davies KJA, Goldberg AL (1987) Oxygen radicals stimulate intracellular proteolysis and lipid peroxidation by independent mechanisms in erythrocytes. J Biol Chem 262:8220–8226

    PubMed  CAS  Google Scholar 

  • Esterbauer H (1996) Estimation of peroxidative damage. A critical review. Pathol Biol 44:25–28

    PubMed  CAS  Google Scholar 

  • Evans P, Halliwell B (2001) Micronutrients: oxidant/antioxidant status. Br J Nutr 85:s57–s74

    Article  Google Scholar 

  • Flohe L (1971) Glutathione peroxidase: enzymology and biological aspects. Klin Wochenschr 49:669–683

    Article  PubMed  CAS  Google Scholar 

  • Friedman MI (1979) Oxygen damage mediates variant red cell resistance to malaria. Nature 280:245–247

    Article  PubMed  CAS  Google Scholar 

  • Grewal A, Ahuja CS, Singh SP, Chaudhary KC (2005) Status of lipid peroxidation, some antioxidant enzymes and erythrocytic fragility of crossbred cattle naturally infected with Theileria annuluta. Vet Res Commun 29:387–394

    Article  PubMed  CAS  Google Scholar 

  • Hafeman DG, Sunde RA, Hoekstra WG (1974) Effect of dietary selenium on erythrocyte and liver glutathione peroxidase in rat. J Nutr 104:580–587

    PubMed  CAS  Google Scholar 

  • Halliwell B, Chirico S (1993) Lipid peroxidation: its mechanism, measurement, and significance. Am J Clin Nut 57:715S–724S

    Google Scholar 

  • Hooshmand-Rad P (1976) The pathogenesis of anemia in Theileria annulata infection. Res Vet Sci 20:324–329

    PubMed  CAS  Google Scholar 

  • Hooshmand-Rad P (1974) Blood protozoan disease of ruminants. Bull Int Epiz 81(9–10):779–792

    Google Scholar 

  • Jain NC (1993) Essentials of veterinary hematology. Williams & Wilkins, Media, pp 389–396

    Google Scholar 

  • Lykkesfeldt J (2001) Determination of malondialdehyde as dithiobarbituric acid adduct in biological samples by HPLC with fluorescence detection: comparison with ultraviolet-visible spectrophotometry. Clin Chem 47:1725–1727

    PubMed  CAS  Google Scholar 

  • McCord JM, Fridovich I (1969) Superoxide dismutase: an enzymic function for erythrocuprein (hemocuprein). J Biol Chem 244:6049–6055

    PubMed  CAS  Google Scholar 

  • Moore K, Roberts LJ (1998) Measurement of lipid peroxidation. Free Radic Res 28:659–671

    Article  PubMed  CAS  Google Scholar 

  • Morel C, Uilenberg G (1981) The nomenclature of some Theileria species (Sporozoa, Babesoidea) of domestic ruminants. Rev Élev Méd Vét Pays Trop 34:139–143

    PubMed  CAS  Google Scholar 

  • Nazifi S, Razavi SM, Mansourian M, Nikahval B, Moghaddam M (2008) Studies on correlation among parasitemia and some hemolytic indices in two tropical diseases (theileriosis and anaplasmosis) in Fars province of Iran. Trop Anim Health Prod 40:47–53

    Article  PubMed  CAS  Google Scholar 

  • Nazifi S, Razavi SM, Hasanshahi F, Esmailnezhad Z (2009) Effect of the severity of Theileria annulata infection on some hematological parameters and antioxidant enzymes in naturally infected cattle. Bulgarian J Vet Med 12:63–71

    Google Scholar 

  • Paglia DE, Valentine WN (1967) Studies on the quantitative and qualitative characterization of erythrocyte glutathione peroxidase. J Lab Clin Med 70:158–169

    PubMed  CAS  Google Scholar 

  • Rayula V, Hafeez MD (1995) Hematological values in cattle infected with Theileria annulata. Indian J Anim Sci 56:1202–1203

    Google Scholar 

  • Razavi SM, Nazifi S, Vosoughi F, Masoudian M, Nowroozi Asl A, Rakhshandehroo E (2010) Alterations of serum tumor necrosis factor-α (TNF-α), interferon-γ (IFN-γ), and sialic acids in malignant ovine theileriosis. Comp Clin Pathol 19:503–509

    Article  CAS  Google Scholar 

  • Saluja PS, Gupta SL, Malhotra DV, Ambawat HK (1999) Plasma malondialdehyde in experimental Theileria annulata infected cross bred bovine calves. Indian Vet J 76:379–381

    CAS  Google Scholar 

  • Schnittger L, Yin H, Jianxun L, Lugwing W, Shayan P, Rahbari S, Voss-Holtmann A, Ahmed JS (2000) Ribosomal small-subunit RNA gene-sequence analysis of Theileria lestoquardi and a Theileria species highly pathogenic for small ruminants in China. Parasitol Res 86:352–358

    Article  PubMed  CAS  Google Scholar 

  • Shiono H, Yagi Y, Chikayama Y, Miyazaki S, Nakamura I (2003) Oxidative damage and phosphatidylserine expression of red blood cells in cattle experimentally infected with Theileria sergenti. Parasitol Res 89:228–234

    PubMed  Google Scholar 

  • Singh A, Singh J, Grewal AS, Brar RS (2001) Studies on some blood parameters of crossbred calves with experimental Theileria annulata infections. Vet Res Commun 25:289–300

    Article  PubMed  CAS  Google Scholar 

  • Slaughter MR, O'Brien PJ (2000) Fully-automated spectrophotometric method for measurement of antioxidant activity of catalase. Clin Biochem 33:525–534

    Article  PubMed  CAS  Google Scholar 

  • Soulsby EJL (1982) Helminthes, arthropods and protozoa of domesticated animals. Williams & Wilkins, London, pp 728–739

    Google Scholar 

  • Stockham SL, Scott MA (2002) Fundamentals of veterinary clinical pathology. Iowa State University Press, Ames, pp 433–467

    Google Scholar 

  • Weisiger RA, Fridovich I (1973) Mitochondrial superoxide dismutase. Site of synthesis and intramitochondrial localisation. J Biol Chem 248:4793–4796

    PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to S. Nazifi.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Nazifi, S., Razavi, S.M., Kianiamin, P. et al. Evaluation of erythrocyte antioxidant mechanisms: antioxidant enzymes, lipid peroxidation, and serum trace elements associated with progressive anemia in ovine malignant theileriosis. Parasitol Res 109, 275–281 (2011). https://doi.org/10.1007/s00436-010-2248-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00436-010-2248-5

Keywords

Navigation