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Oxidant/antioxidant balance and trace elements status in sheep with liver cystic echinococcosis

Comparative Clinical Pathology volume 22, pages 1043–1049 (2013)Cite this article

Abstract

This study aimed to determine the trace elements and oxidative stress markers as contributory factors causing liver injury and erythrocyte destruction in sheep with liver cystic echinococcosis. In comparison to healthy control, the index of serum lipid peroxidation assessed by the malonyldialdehyde (MDA) level was significantly (P < 0.001) higher and the concentrations of serum total antioxidant status (TAS) and trace elements (zinc, copper, and iron) were significantly (P < 0.001) lower in sheep with liver cystic echinoccocosis. No significant differences were observed for erythrocyte glutathione peroxidase (GPx) and superoxide dismutase activities between infected and healthy groups. In infected sheep, a significant positive correlation of MDA with aspartate transaminase (AST) (r = 0.636, P = 0.000) and erythrocyte GPx (r = 0.373, P = 0.043) was observed. By contrast, serum MDA concentration was negatively correlated with the values of TAS (r = −0.559, P = 0.001) and packed cell volume (PCV; r = −0.473, P = 0.008). On the other hand, there was a significant negative correlation between serum TAS concentration and the levels of AST (r = −0.433, P = 0.017) and MDA (r = −0.559, P = 0.001). By contrast, serum TAS was positively correlated with the value of PCV (r = 0.728, P = 0.000). From the present study, it was concluded that cystic echinococcosis in sheep is associated with oxidative stress. The resulting oxidative stress seems to have a role in the injury of hepatocytes and erythrocytes.

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References

  • Abo-Shousha S, Khalil S, Rashman E (1999) Oxygen free radicals and nitric oxide production in single or combined human schistosomiasis and fascioliasis. J Egypt Soc Parasitol 29:149–156

    PubMed  CAS  Google Scholar 

  • Aruoma OI (1998) Free radicals, oxidative stress, and antioxidants in human health and disease. J Am Chem Soc 75:199

    CAS  Google Scholar 

  • Boczon K, Hadas E, Wandurska-Nowak E, Derda M (1996) A stimulation of antioxidants in muscles of Trichinella spiralis infected rats. Acta Parasitologica 41:136–138

    CAS  Google Scholar 

  • Clemens MR, Waller HD (1987) Lipid peroxidation in erythrocytes. Chem Phys Lipids 45:251–268

    PubMed  Article  CAS  Google Scholar 

  • Deger Y, Ertekin A, Deger S, Mert H (2008) Lipid peroxidation and antioxidant potential of sheep liver infected naturally with distomatosis. Turkiye Parazitol Derg 32:23–26

    PubMed  Google Scholar 

  • Derda M, Wandurska-Nowak E, Hadas E (2004) Changes in the level of antioxidants in the blood from mice infected with Trichinella spiralis. Parasitol Res 93:207–210

    PubMed  Article  Google Scholar 

  • Dimri U, Ranjan R, Kumar N, Sharma MC, Swarup D, Sharma B, Kataria M (2008) Changes in oxidative stress indices, zinc and copper concentrations in blood in canine demodicosis. Vet Parasitol 154:98–102

    PubMed  Article  CAS  Google Scholar 

  • Dimri U, Sharma MC, Yamdagni A, Ranjan R, Zama MMS (2010) Psoroptic mange infestation increases oxidative stress and decreases antioxidant status in sheep. Vet Parasitol 168:318–322

    PubMed  Article  CAS  Google Scholar 

  • Eckert E, Deplazes P (2004) Biological, epidemiological, and clinical aspects of echinococcosis, a zoonosis of increasing concern. Clin Microbiol Rev 17:107–135

    PubMed  Article  Google Scholar 

  • Ergin S, Saribas S, Yuksel P, Zengin K, Midilli K, Adas G, Arikan S, Aslan M, Uysal H, Caliskan R, Oner A, Kucukbasmaci O, Kaygusuz A, Mamal Torun M, Kocazeybek B (2010) Genotypic characterisation of Echinococcus granulosus isolated from human in Turkey. Afr J Microbiol Res 4:551–555

    CAS  Google Scholar 

  • Ersayit D, Kilic E, Yazar S, Artis T (2009) Oxidative stress in patients with cystic echninococcosis: relationship between oxidant and antioxidant parameters. Saglık Bil Dergisi 18:159–166

    Google Scholar 

  • Evans P, Halliwell B (2001) Micronutrients: oxidant and antioxidant status. Br J Nutr 85:67–74

    Article  Google Scholar 

  • Fang YZ, Yang S, Wu G (2002) Free radicals, antioxidants and nutrition. Nutr 18:872–879

    Article  CAS  Google Scholar 

  • Galtier P, Cambon-Gros C, Fernandez Y, Deltour P, Eeckhoutte C, Hoellinger H (1994) Fasciola hepatica: liver microsomal membrane functions in host rat. Exp Parasitol 78:175–182

    PubMed  Article  CAS  Google Scholar 

  • Gurer H, Ozgunes H, Neal R, Spitzand DR, Ercal N (1998) Antioxidant effects of N-acetyl cysteine and succimer in red blood cells from lead exposed rats. Toxicol 128:181–189

    Article  CAS  Google Scholar 

  • Gutteridge JMC (1995) Lipid peroxidation and antioxidants as biomarkers of tissue damage. Clin Chem 41:1819–1828

    PubMed  CAS  Google Scholar 

  • Halliwell B (1988) Albumin, an important extracellular antioxidant. Biochem Pharmacol 37:569–571

    PubMed  Article  CAS  Google Scholar 

  • Halliwell B (1994) Free radicals, antioxidants, and human disease: curiosity, cause and consequence? Lancet 344:721–724

    PubMed  Article  CAS  Google Scholar 

  • Halliwell B, Chirico S (1993) Lipid peroxidation: its mechanism, measurement, and significance. Am J Clin Nutr 57:715–725

    Google Scholar 

  • Halliwell B, Gutteridge JMC (1999) Free radical biology and medicine, 3rd edn. Oxford University Press, Oxford

    Google Scholar 

  • Jain NC (1986) Schalm's veterinary hematology, 4th edn. Lea & Febiger, Philadelphia

    Google Scholar 

  • Kilic E, Yazar S, Baskol G, Artis T, Ersayit D (2010) Antioxidant and nitric oxide status in patients diagnosed with Echinococcus granulosus. Afr J Microbiol Res 4:2439–2443

    CAS  Google Scholar 

  • Klasing KC (1988) Nutritional aspects of leukocytic cytokines. J Nutr 118:1436–1446

    PubMed  CAS  Google Scholar 

  • Kolodziejczyk L, Siemieniuk E, Skrzydlewska E (2005) Antioxidant potential of rat liver in experimental infection with Fasciola hepatica. Parasitol Res 96:367–372

    PubMed  Article  CAS  Google Scholar 

  • Koltas IS, Yucebiligc G, Biligin R, Parsak CK, Sakman G (2006) serum malondialdehyde level in patients with cystic echinococcosis. Saudi Med J 27:1703–1705

    PubMed  Google Scholar 

  • Kosecik M, Erel O, Sevinc E, Selek S (2005) Increased oxidative stress in children exposed to passive smoking. Int J Cardiol 100:61–64

    PubMed  Article  Google Scholar 

  • Latif AA, Tanveer A, Maqbool A, Siddiqi N, Kyaw-Tanner M, Traub RJ (2010) Morphological and molecular characterisation of Echinococcus granulosus in livestock and humans in Punjab, Pakistan. Vet Parasitol 170:44–49

    PubMed  Article  CAS  Google Scholar 

  • Lilic A, Dencic S, Pavlovic SZ, Blagojevic DP, Spasic MB, Stankovic NS, Saicic ZS (2007) Activity of antioxidative defense enzymes in the blood of patients with liver echinococcosis. Vojnosanit Pregl 64:235–240

    PubMed  Article  Google Scholar 

  • Loban A, Kime R, Powers H (1997) Iron-binding antioxidant potential of plasma albumin. Clin Sci (Lond) 93:445–451

    CAS  Google Scholar 

  • May JM, Qu ZC, Mendiratta S (1998) Protection and recycling of alfa-tocopherol in human erythrocytes by intracellular ascorbic acid. Arch Biochem Biophys 349:281–289

    PubMed  Article  CAS  Google Scholar 

  • Munoz C, Rios E, Olivos J, Brunser O, Olivares M (2007) Iron, copper and immunocompetence. Br J Nutr 98:24–28

    Article  Google Scholar 

  • Oteiza PI, Olin KL, Fraga CG, Keen CL (1995) Zinc deficiency causes oxidative damage to proteins, lipids and DNA in rat testes. J Nutr 125:823–829

    PubMed  CAS  Google Scholar 

  • Panda D, Patra RC, Nandi S, Swarup D (2009) Oxidative stress indices in gastroenteritis in dogs with canine parvoviral infection. Res Vet Sci 86:36–42

    PubMed  Article  CAS  Google Scholar 

  • Pednekar RP, Gatne ML, Thompson RCA, Traub RJ (2009) Molecular and morphological characterisation of Echinococcus from food producing animals in India. Vet Parasitol 165:58–65

    PubMed  Article  Google Scholar 

  • Placer ZA, Cushman L, Johnson B (1966) Estimation of product of lipid peroxidation (malonyldialdehyde) in biochemical system. Anal Biochem 16:359–364

    PubMed  Article  CAS  Google Scholar 

  • Rush JW, Sandiford SD (2003) Plasma glutathione peroxidase in healthy young adults: influence of gender and physical activity. Clin Biochem 36:345–351

    PubMed  Article  CAS  Google Scholar 

  • Saleh MA (2008) Circulating oxidative stress status in desert sheep naturally infected with Fasciola hepatica. Vet Parasitol 154:262–269

    PubMed  Article  CAS  Google Scholar 

  • Saleh MA, Al-Salahy MB, Sanousi SA (2009) Oxidative stress in blood of camels (Camelus dromedaries) naturally infected with Trypanosoma evansi. Vet Parasitol 162:192–199

    PubMed  Article  CAS  Google Scholar 

  • Sanchez-Campos S, Tunon MJ, Gonzales P, Gonzales-Gallego J (1999) Oxidative stress and changes in liver antioxidant enzymes induced by experimental dicrocoeliosis in hamsters. Parasitol Res 85:468–474

    PubMed  Article  CAS  Google Scholar 

  • Sato Y, Kanazawa S, Sato K, Suzuki Y (1998) Mechanism of free radical induced hemolysis of human erythrocytes: II. Hemolysis by lipid soluble radical initiator. Biol Pharm Bull 21:250–256

    PubMed  Article  CAS  Google Scholar 

  • Seyrek K, Karagenc T, Pasa S, Kıral F, Atasoy A (2009) Serum zinc, iron and copper concentrations in dogs infected with Hepatozoon canis. Acta Vet Brno 78:471–475

    Article  CAS  Google Scholar 

  • Simsek S, Yuce A, Utuk AE (2006) Determination of serum malondialdehyde levels in sheep naturally infected with Dicrocoelium dendriticum. F U Saglık Bil Dergisi 20:217–220

    Google Scholar 

  • Sobolewski P, Gramaglia I, Frangos J, Intaglietta M, van der Heyde HC (2005) Nitric oxide bioavailability in malaria. Trends Parasitol 21:415–422

    PubMed  Article  CAS  Google Scholar 

  • Tasci S, Sengil AZ, Altindis M, Arisoy K (1995) The effect of zinc supplementation in experimentally induced Toxoplasma gandii infection. J Egypt Soc Parasitol 25:745–751

    PubMed  CAS  Google Scholar 

  • Wanger HM, Buesher HU, Rollinghoff M, Solbach W (1991) Interferon-gamma inhibits the efficacy of interleukin-1 to generate a Th2-cell biased immune response induced by Leishmania major. Immunobiology 182:292–306

    Article  Google Scholar 

  • Weinberg JB, Lopansri BK, Mwaikambo E, Granger DL (2008) Arginine, nitric oxide, carbon monoxide, and endothelial function in severe malaria. Curr Opin Infect Dis 21:468–475

    PubMed  Article  CAS  Google Scholar 

  • Zaki MH, Akuta T, Akaike T (2005) Nitric oxide-induced nitrative stress involved in microbial pathogenesis. J Pharmacol Sci 98:117–129

    PubMed  Article  CAS  Google Scholar 

  • Zeghir-Bouteldja R, Amri M, Aitaissa S, Bouaziz S, Mezioug D, Touil-Boukoffa C (2009) In vitro study of nitric oxide metabolites effects on human hydatid of Echinococcus granulosus. J Parasitol Res. doi:10.1155/2009/624919

  • Zelko IN, Mariani TJ, Folz RJ (2002) Superoxide dismutase multigene family. a comparison of the CuZn-SOD (SOD1), Mn-SOD (SOD2), and EC-SOD (SOD3) gene structures, evolution, and expression. Free Radic Biol Med 33:337–349

    PubMed  Article  CAS  Google Scholar 

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Acknowledgments

This study was supported by research fund of Ferdowsi University of Mashhad (project no. 17026/2). The authors wish to thank technicians who kindly helped us for sample collection of this study

Conflict of interest statement

The authors declare that they have no conflict of interest.

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Authors and Affiliations

  1. Department of Clinical Sciences, School of Veterinary Medicine, Ferdowsi University of Mashhad, Mashhad, Iran, PO Box 91775-1793

    M. Heidarpour & M. Mohri

  2. Center of Excellence in Ruminant Abortion and Neonatal Mortality, School of Veterinary Medicine, Ferdowsi University of Mashhad, Mashhad, Iran, PO Box 91775-1793

    M. Mohri

  3. Department of Pathobiology, School of Veterinary Medicine, Ferdowsi University of Mashhad, Mashhad, Iran, PO Box 91775-1793

    H. Borji & E. Moghaddas

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  1. M. Heidarpour
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  2. M. Mohri
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  3. H. Borji
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  4. E. Moghaddas
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Correspondence to M. Heidarpour.

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Heidarpour, M., Mohri, M., Borji, H. et al. Oxidant/antioxidant balance and trace elements status in sheep with liver cystic echinococcosis. Comp Clin Pathol 22, 1043–1049 (2013). https://doi.org/10.1007/s00580-012-1523-5

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  • DOI: https://doi.org/10.1007/s00580-012-1523-5

Keywords

  • Oxidative stress
  • Trace elements
  • Sheep
  • Echinococcosis