Original Article

Relationships between Oxidative Stress, Liver, and Erythrocyte Injury, Trace Elements and Parasite Burden in Sheep Naturally Infected with Dicrocoelium dendriticum


Background: The aim of this study was to investigate the role of oxidative stress in the pathology of ovine dicrocoeliasis.

Methods: During Dec 2013 - Oct 2014, seventy-two sheep (1-3 years) with liver dicrocoeliasis along with 47 healthy sheep were selected from animals admitted for slaughtering at slaughterhouse located in Neyshabour, Razavi Khorasan Province, Iran.

Results: In comparison to healthy control, the malondialdehyde (MDA) level and serum total antioxidant capacity were significantly higher in the parasitized group (P<0.05). A significant increase in liver MDA concentration (P<0.05) of parasitized group was also observed. Packed cell volume (PCV), zinc, iron, total bilirubin and albumin sera levels were significantly lower in the parasitized group (P<0.05). In parasitized sheep, a significant positive correlation was seen between serum MDA concentration and the activity of aspartate aminotransferase (AST). On the other hand, the concentration of serum MDA was inversely correlated with the value of PCV. No significant differences were observed for MDA concentration and total antioxidant capacity between normal and abnormal hepatic lobes in the parasitized animals. Oxidative stress markers (MDA and total antioxidant capacity in serum and liver samples) showed no significant correlations with the extent of pathological lesions and serum variables of liver injury in the parasitized sheep. No significant correlation was observed between oxidative stress markers and the fluke’s number in the parasitized animals.

Conclusion: Oxidative stress may play an important role in the erythrocyte destruction in sheep naturally infected with D. dendriticum. However, no clear relationships were observed between the oxidative stress, hepatic damage and parasite burden.

Manga-González MY, Ferreras MC. Dicrocoeliidae family: major species causing veterinary diseases. Adv Exp Med Biol. 2014; 766: 393-428.

Otranto D, Traversa D. A review of dicrocoeliosis of ruminants including recent advances in the diagnosis and treatment. Vet Parasitol. 2002; 107(4): 317–35.

Jithendran KP, Bhat TK. Prevalence of dicrocoeliosis in sheep and goats in Himachal Pradesh. India. Vet Parasitol. 1996; 61(3-4):265–71.

Manga-González MY, Ferreras MC, Campo R, González-Lanza C, PérezV, García-Marín JF. Hepatic marker enzymes, biochemical parameters and pathological effects in lambs experimentally infected with Dicrocoelium dendriticum. Parasitol Res. 2004; 93(5): 344–55.

Bakır S, Çeliksöz A, Çelik VK, Sari I, Aydın H. Antioxidant-oxidant status in patients with hydatid cyst. Turk J Biochem. 2012; 37(1): 29–34.

Luszczak JM, Ziaja-Sołtys M, Rzymowska J. Anti-oxidant activity of superoxide dismutase and glutathione peroxidase enzymes in skeletal muscles from slaughter cattle infected with Taenia saginata. Exp Parasitol. 2011; 128(2): 163–5.

Kolodziejczyk L, Siemieniuk E, Skrzydlewska E. Antioxidant potential of rat liver in experimental infection with Fasciola hepatica. Parasitol Res. 2005; 96(6): 367–72.

Saleh MA, Mahran OM, Bassam Al-Salahy M. Circulating oxidative stress status in dromedary camels infested with sarcoptic mange. Vet Res Commun. 2011; 35(1): 35–45.

Poli G. Pathogenesis of liver fibrosis: role of oxidative stress. Mol Aspects Med. 2000; 21(3): 49–98.

Dimri U, Sharma MC, Yamdagni A, Ranjan R, Zama MM. Psoroptic mange infestation increases oxidative stress and decreases antioxidant status in sheep. Vet Parasitol. 2010; 168(3-4): 318–22.

Evans P, Halliwell B. Micronutrients: oxi-dant/antioxidant status. Br J Nutr. 2001; 85(Suppl 2): 67-74.

Şimşek S, Yüce A, Ütük AE. Determina-tion of serum malondialdehyde levels in sheep naturally infected with Dicrocoelium dendriticum. F U Saglık Bil Dergisi. 2006; 20(3): 217–20.

Sanchez-Campos S, Tunon MJ, Gonzales P, Gonzales-Gallego J. Oxidative stress and changes in liver antioxidant enzymes induced by experimental dicrocoeliosis in hamsters. Parasitol Res. 1999; 85(6): 468–74.

Saleh MA. Circulating oxidative stress status in desert sheep naturally infected with Fasciola hepatica. Vet Parasitol. 2008; 154(3-4): 262–9.

Heidarpour M, Mohri M, Borji H, Mogh-dass E. Oxidant/antioxidant status in cattle with liver cystic echinococcosis. Vet Parasitol. 2013; 195(1-2): 131–5.

Heidarpour M, Mohri M, Borji H, Mogh-dass E. Oxidative stress and trace elements in camel (Camelus dromedarius) with liver cystic echinococcosis. Vet Parasitol. 2012; 187(3-4): 459–63.

Heidarpour M, Mohri M, Borji H, Mogh-dass E. Oxidant/ antioxidant balance and trace elements status in sheep with liver cystic echinococcosis. Comp Clin Pathol. 2013; 22(6): 1043–9.

Sánchez-Campos S, González P, Ferreras C, García-Iglesias MJ, González-Gallego J, Tuñón MJ. Morphologic and biochemical changes caused by experimentally induced dicrocoeliosis in hamsters (Mesocricetus au-ratus). Comp Med. 2000; 50(2): 147–52.

Jain NC. Hematologic techniques. In: Jain NC editor. Schalm’s Veterinary Hematology. 4th ed. Philadelphia: Lea and Febiger; 1986. p. 20–86.

Sanz F, Tarazana JM, Jurado R, Friag J, Tarozana JV, Duncan JC. An evaluation of the efficacy of netobimin against Dicrocoelium dendriticum in sheep. Vet Rec. 1987; 120(3): 57-8.

Placer ZA, Cushman LL, Johnson BC. Estimation of product of lipid peroxidation (malonyldialdehyde) in biochemical systems. Anal Biochem. 1966; 16(2): 359–64.

Benzie IF, Strain JJ. The ferric reducing ability of plasma (FRAP) as a measure of “antioxidant power”: the FRAP assay. Anal Biochem. 1996; 239(1): 70–6.

Kolodziejczyk L, Siemieniuk E, Skrzydlewska E. Fasciola hepatica: effects on the antioxidative properties and lipid peroxidation of rat serum. Exp Parasitol. 2006; 113(1): 43–8.

Kaya S, Sutcu R, Cetin ES, Arıdogan BC, Delibas N, Demirci M. Lipid peroxidation level and antioxidant enzyme activities in the blood of patients with acute and chronic fascioliasis. Int J Infect Dis. 2007; 11(3): 251–5.

Gabrashanska M, Teodorova SE, Anisimova M. Oxidative-antioxidant status of Fasciola hepatica-infected rats supplemented with zinc. A mathematical model for zinc bioaccumulation and host growth. Parasitol Res. 2008; 104(1): 69–78.

Kilic E, Yazar S, Baskol G, Artis T, Ersayit D. Antioxidant and nitric oxide status in patients diagnosed with Echinococcus granulosus. Afr J Microbiol Res. 2010; 4(22): 2439–43.

Heidarpour M, Soltani S, Mohri M, Khoshnegah J. Canine visceral leishmaniasis: relationships between oxidative stress, liver and kidney variables, trace elements, and clinical status. Parasitol Res. 2012; 111(4): 1491–6.

Bahrami B, Razi Jalali MH, Jafari A. Evaluation of hepatic antioxidant changes in ovine dicrocoeliosis. J Parasit Dis. 2015; 39(4): 766–9.

Uner N, Oruç EO, Canli M, Sevgiler Y. Effects of cypermethrin on antioxidant enzyme activities and lipid peroxidation in liver and kidney of the freshwater fish. Oreochromis niloticus and Cyprinus carpio (L.). Bull Environ Contam Toxicol. 2001; 67(5): 657–64.

Panda D, Patra RC, Nandi S, Swarup D. Oxidative stress indices in gastroenteritis in dogs with canine parvoviral infection. Res Vet Sci. 2009; 86(1): 36–42.

Rushmore TH, Morton MR, Pickett CB. The antioxidant responsive element. Activation by oxidative stress and identification of the DNA consensus sequence required for functional activity. J Biol Chem. 1991; 266(18): 11632–9.

Thomas JS. Overview of plasma proteins. In: Feldman BF, Zinkl JG, Jain NC, editors. Schalm’s Veterinary Hematology. Philadelphia: Lippincott Williams & Wilkins: 2000. p. 891–8.

Halliwell B. Albumin, an important extracellular antioxidant. Biochem Pharmacol. 1988; 37(4): 569–71.

Klotz LO, Kroncke KD, Buchczyk DP, Sies H. Role of copper, zinc, selenium and tellurium in the cellular defense against oxidative and nitrosative stress. J Nutr. 2003; 133(5 Suppl 1): 1448–51.

Munoz C, Rios E, Olivos J, Brunser O, Olivares M. Iron, copper and immunocompetence. Br J Nutr. 2007; 98(Suppl 1): 24–8.

Tasci S, Sengil AZ, Altindis M, Arisoy K. The effect of zinc supplementation in experimentally induced Toxoplasma gandii infection. J Egypt Soc Parasitol. 1995; 25(3): 745–51.

Beisel WR. Nutrition and infection. In: Linder MC. editor. Nutritional biochemistry and metabolism with clinical application. 2nd ed. New York: Elsevier; 1991. p. 507–42.

Corrigall W, Dalgarno AC, Ewen LA, Williums RB. Modulation of plasma copper and zinc concentrations by disease status in ruminants. Vet Rec. 1976; 99(20): 396–7.

Wegner TN, Ray DE, Lox CD, Stott GH. Effect of stress on serum zinc and plasma corticoids in dairy cattle. J Dairy Sci. 1973; 56(6): 758–62.

Ranjan R, Swarup D, Naresh R, Patra RC. Enhanced erythrocytic lipid peroxides and reduced plasma ascorbic acid and alteration in blood trace elements level in dairy cows with mastitis. Vet Res Commun. 2005; 29(1): 27–34.

Saleh MA, Al-Salahy MB, Sanousi SA. Oxidative stress in blood of camels (Camelus dromedaries) naturally infected with Trypanosoma evansi. Vet Parasitol. 2009; 162(3-4): 192–9.

Sheridan AM, Fitzpatrick S, Wang C, Wheeler DC, Lieberthal W. Lipid peroxidation contributes to hydrogen peroxide induced cytotoxicity in renal epithelial cells. Kidney Int.1996; 49(1): 88–93.

Derda M, Wandurska-Nowak E, Hadas E. Changes in the level of antioxidants in the blood from mice infected with Trichinella spiralis. Parasitol Res. 2004; 93(3): 207–10.

Hoffmann WE, Solter PF. Diagnostic enzymology of domestic animals. In: Kaneko, JJ, Harvey, JW, Bruss ML, editors. Clinical biochemistry of domestic animals. 6th ed. San Diego: Academic press; 2008. p. 351-78.

Cunha GM, Silva VM, Bessa KD, Bitencourt MA, Macêdo UB, Freire-Neto FP, Martins RR, Assis CF, Lemos TM, Almeida MG, Freire AC. Levels of oxidative stress markers: correlation with hepatic function and worm burden pa-tients with schistosomiasis. Acta Parasitol. 2012; 57(2): 160-6.

Sorci G, Faivre B. Inflammation and oxidative stress in vertebrate host–parasite systems. Philos Trans R Soc Lond B Biol Sci. 2009; 364(1513): 71–83.

IssueVol 12 No 1 (2017) QRcode
SectionOriginal Article(s)
Ovine dicrocoeliasis Oxidative stress Parasite burden

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How to Cite
SAMADIEH H, MOHAMMADI G-R, MALEKI M, BORJI H, AZIZZADEH M, HEIDARPOUR M. Relationships between Oxidative Stress, Liver, and Erythrocyte Injury, Trace Elements and Parasite Burden in Sheep Naturally Infected with Dicrocoelium dendriticum. Iran J Parasitol. 2017;12(1):46-55.