Hostname: page-component-8448b6f56d-dnltx Total loading time: 0 Render date: 2024-04-24T04:49:20.184Z Has data issue: false hasContentIssue false
  • English
  • Français

Oxidative stress and changes in adenosine deaminase activity of cattle experimentally infected by Fasciola hepatica

Published online by Cambridge University Press:  20 January 2017

ALEKSANDRO S. DA SILVA ,
MATHEUS D. BALDISSERA ,
NATHIELI B. BOTTARI ,
MATHEUS E. GABRIEL ,
LEANDRO A. RHODEN ,
MANOELA M. PIVA ,
RICARDO CHRIST ,
FERNANDA A. STEDILLE ,
ANDERSON GRIS  and
VERA M. MORSCH
...Show all authors
ALEKSANDRO S. DA SILVA*
Affiliation:
Graduate Program in Animal Science, Universidade do Estado de Santa Catarina (UDESC), Chapecó, Brazil Department of Biochemistry and Molecular Biology and Department of Microbiology and Parasitology, Universidade Federal de Santa Maria (UFSM), Brazil
MATHEUS D. BALDISSERA
Affiliation:
Department of Microbiology and Parasitology, Universidade Federal de Santa Maria (UFSM), Brazil
NATHIELI B. BOTTARI
Affiliation:
Department of Biochemistry and Molecular Biology and Department of Microbiology and Parasitology, Universidade Federal de Santa Maria (UFSM), Brazil
MATHEUS E. GABRIEL
Affiliation:
Laboratory of Veterinary Pathology, Instituto Federal Catarinense (IFC), Concórdia, SC, Brazil
LEANDRO A. RHODEN
Affiliation:
Laboratory of Veterinary Pathology, Instituto Federal Catarinense (IFC), Concórdia, SC, Brazil
MANOELA M. PIVA
Affiliation:
Laboratory of Veterinary Pathology, Instituto Federal Catarinense (IFC), Concórdia, SC, Brazil
RICARDO CHRIST
Affiliation:
Laboratory of Veterinary Pathology, Instituto Federal Catarinense (IFC), Concórdia, SC, Brazil
FERNANDA A. STEDILLE
Affiliation:
Laboratory of Veterinary Pathology, Instituto Federal Catarinense (IFC), Concórdia, SC, Brazil
ANDERSON GRIS
Affiliation:
Laboratory of Veterinary Pathology, Instituto Federal Catarinense (IFC), Concórdia, SC, Brazil
VERA M. MORSCH
Affiliation:
Department of Biochemistry and Molecular Biology and Department of Microbiology and Parasitology, Universidade Federal de Santa Maria (UFSM), Brazil
MARIA ROSA SCHETINGER
Affiliation:
Department of Biochemistry and Molecular Biology and Department of Microbiology and Parasitology, Universidade Federal de Santa Maria (UFSM), Brazil
RICARDO E. MENDES*
Affiliation:
Laboratory of Veterinary Pathology, Instituto Federal Catarinense (IFC), Concórdia, SC, Brazil
*
*Corresponding authors: UDESC, Animal Science, Rua Beloni Trombeta Zanini, Chapecó 89805-030, Brazil. E-mail: aleksandro_ss@yahoo.com.br; ricardo.mendes@ifc-concordia.edu.br
*Corresponding authors: UDESC, Animal Science, Rua Beloni Trombeta Zanini, Chapecó 89805-030, Brazil. E-mail: aleksandro_ss@yahoo.com.br; ricardo.mendes@ifc-concordia.edu.br
Get access Rights & Permissions [Opens in a new window]

Summary

The aim of this study was to evaluate the oxidative stress in serum and liver and adenosine deaminase (ADA) activity of cattle experimentally infected by Fasciola hepatica. The group A consisted of five healthy animals (uninfected), and the group B was composed of five animals orally infected with 200 metacercariae of F. hepatica. On days 20, 40, 60 and 80 post-infection (PI) serum was collected to measure oxidative stress variables. On day 100 PI, animals were humanely euthanized and liver samples were collected. Infected animals showed lower (P < 0·05) seric ADA activities on days 40 and 60 PI but higher (P < 0·05) in the liver tissue compared with uninfected animals. Seric and hepatic reactive oxygen species (ROS) were higher (P < 0·05) in infected compared with uninfected animals. Hepatic thiobarbituric acid reactive substances were higher (P < 0·05) in infected animals. Catalase and glutathione S-transferase activities were lower in liver tissue of infected animals, while glutathione peroxidase was higher compared with uninfected (P < 0·05). In summary, we conclude that oxidative stress occurs in cattle experimentally infected by F. hepatica, mainly due to excessive ROS production in the course of fasciolosis, contributing to hepatic damage, and that increased in hepatic ADA activity may contribute to the inflammatory process.

Keywords

ADAfasciolosisoxidative stresszoonosis
Type
Research Article
Information
Parasitology , Volume 144 , Issue 4 , April 2017 , pp. 520 - 526
Check for updates
Copyright
Copyright © Cambridge University Press 2017 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Abbracchio, M. P. and Ceruti, S. (2007). P1 receptors and cytokine secretion. Purinergic Signalling 3, 13–25.CrossRefGoogle ScholarPubMed
Aebi, H. (1984). Catalase in vitro . Methods in Enzymology 105, 121–126.Google Scholar
Baldissera, M. D., Bottari, N. B., Mendes, R. E., Schwertz, C. I., Lucca, N. J., Dalenogare, D., Bochi, G. V., Moresco, R. N., Morsch, V. M., Schetinger, V. M., Rech, V. C., Jaques, J. A. and Da Silva, A. S. (2015). Activity of cholinesterases, pyruvate kinase and adenosine deaminase in rats experimentally infected by Fasciola hepatica: influence of these enzymes on inflammatory response and pathological findings. Pathology – Research and Practice 211, 871–876.Google Scholar
Baldissera, M. D., Mendes, R. E., Doleski, P. H., Bottari, N. B., Casali, E. A., Cardoso, V. V., Henker, L. C., Christ, R., Stedille, F. A., Stefani, L. M. and Da Silva, A. S. (2016). Hepatic and seric levels of purines in rats experimentally infected by Fasciola hepatica . Parasitology Research 115, 2363–2369.Google Scholar
Bottari, N. B., Mendes, R. E., Lucca, N. J., Schwertz, C. I., Henker, L. C., Olsson, D. C., Piva, M. M., Sangoi, M., Campos, L. P., Moresco, R. N., Jaques, J. A. and Da Silva, A. S. (2015). Oxidative stress associated with pathological lesions in the liver of rats experimentally infected by Fasciola hepatica . Experimental Parasitology 159, 24–28.Google Scholar
Bottari, N. B., Mendes, R. E., Baldissera, M. D., Bochi, G. V., Moresco, R. N., Schetinger, M. R., Christ, R., Gheller, L., Marques, E. J. and Da Silva, A. S. (2016). Relation between iron metabolism and antioxidants enzymes and δ-ALA-D activity in rats experimentally infected by Fasciola hepatica . Experimental Parasitology 165, 58–63.Google Scholar
Box, G. E. P. (1953). Non-normality and tests on variances. Biometrika 40, 318–335.CrossRefGoogle Scholar
Bradford, M. (1976). A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein – dye binding. Analytical Biochemistry 72, 248–254.CrossRefGoogle Scholar
Carlberg, I. and Mannervik, B. (1985). Glutathione reductase. Methods in Enzymology 113, 484–490.Google Scholar
Choi, C. Y., An, K. W. and An, M. I. (2008). Molecular characterization and mRNA expression of glutathione peroxidase and glutathione S-transferase during osmotic stress in olive flounder (Paralichthys olivaceus). Comparative Biochemistry and Physiology Part A: Molecular Integrative Physiology 149, 330–337.Google Scholar
Colpo, E., de Bem, A. F., Pieniz, S., Schettert, S. D., dos Santos, R. M., Farias, I. L., Bertoncello, I., Moreira, C. M., Barbosa, N. V., Moretto, M. B. and Rocha, J. B. (2008). A single high dose of ascorbic acid and iron is not correlated with oxidative stress in healthy volunteers. Annals of Nutrition & Metabolism 53, 79–85.Google Scholar
De Oliveira, R. B., Senger, M. R., Vasques, L. M., Gasparotto, J., Dos Santos, J. P., Pasqualli, M. A., Moreira, J. C. F., Silva, F. P. and Gelain, D. P. (2013). Schistosoma mansoni infection causes oxidative stress and alters receptor for advanced glycation endproducts (RAGE) and tau levels in multiple organs in mice. International Journal for Parasitology 43, 371–379.Google Scholar
Doleski, P. H., Mendes, R. E., Leal, D. B., Piva, M. M., Da Silva, E. S., Gabriel, M. E., Lucca, N. J., Schwertz, C. I., Giacomim, P., Morsch, V. M., Schetinger, M. R., Baldissera, M. D. and Da Silva, A. S. (2016). Seric and hepatic NTPDase and 5′-nucleotidase activities of rats experimentally infected by Fasciola hepatica . Parasitology 143, 551–556.CrossRefGoogle ScholarPubMed
Fiss, L., Adrien, M. A., Marcolongo-Pereira, C., Assis-Brasil, N. D., Sallis, E. S. V., Riet-Correa, F., Ruas, J. L. and Schild, A. L. (2013). Subacute and acute fasciolosis in sheep in Southern Brazil. Parasitology Research 112, 883–887.Google Scholar
Fredholm, B. B., Johansson, S. and Wang, Y. W. (2011). Adenosine and the regulation of metabolism and body temperature. Advances in Pharmacology 61, 77–94.Google Scholar
Fujita, T. (2002). Formation and removal of reactive oxygen species, lipid peroxidation and free radicals, and their biological effects. Yakugaku Zasshi 122, 203–218.Google Scholar
Giusti, G. and Gakis, C. (1971). Temperature conversion factors, activation energy, relative substrate specificity and optimum pH of adenosine deaminase from human serum and tissues. Enzyme 12, 417–425.Google Scholar
Giusti, G. and Galanti, B. (1984). Colorimetric method. In Berg-meyer, H.U. Methods of Enzymatic Analysis, 3rd ed., Verlag Chemie, Weinheim, p. 315–323.Google Scholar
Habig, W. H., Pabst, M. J. and Jakoby, W. B. (1974). Glutathione S-transferases. The first enzymatic step in mercapturic acid formation. Journal of Biological Chemistry 249, 7130–7139.CrossRefGoogle ScholarPubMed
Halliwell, B. and Gutteridge, J. M. (1999). Free Radicals in Biology and Medicine. Clarendon Press, Oxford, pp. 1–543.Google Scholar
Halliwell, B. and Gutteridge, J. M. C. (2007) Free Radicals in Biology and Medicine, 4th Edn. Oxford University Press, New York.Google Scholar
Jentzsch, A. M., Bachmann, H., Furts, P. and Biesalski, H. K. (1996). Improved analysis of malondialdehyde in human body fluids. Free Radical Biology and Medicine 20, 251–256.Google Scholar
Kamel, H. H., Sarhan, R. M. and Saad, G. A. (2015). Biochemical assessment of oxidative stress versus liver enzymes in patients with chronic fascioliasis. Journal of Parasitic Diseases 39, 628–633.Google Scholar
Khadija, A. A., Mohammed, S., Saad, A. M. and Mohamed, H. E. (2009). Response of broiler chicks to dietary monosodium glutamate. Pakistan Veterinary Journal 29, 165–168.Google Scholar
Kilic, E., Yazar, S., Saraymen, R. and Ozbilge, H. (2003). Serum malondialdehyde level in patients infected with Ascaris lumbricoides . World Journal of Gastroenterology 9, 2332–2334.Google Scholar
Kolodziejczyk, L., Siemieniuk, E. and Skrzydlewska, E. (2005). Antioxidant potential of rat liver in experimental infection with Fasciola hepatica . Parasitology Research 96, 367–372.Google Scholar
Kolodziejczyk, L., Siemieniuk, E. and Skrzydlewska, E. (2006). Fasciola hepatica: effects on the antioxidant properties and lipid peroxidation of rat serum. Experimental Parasitology 113, 43–48.Google Scholar
Kolodziejczyk, L., Laszczynska, M., Masiuk, M., Grabowska, M. and Skrzydlewska, E. (2015). Immunoexpression of intermediate filaments and morphological changes in the liver and bile ducts of rats infected with Fasciola hepatica . Biotechnic and Histochemistry 90, 477–485.Google Scholar
Lopaczyski, W. and Zeisel, S. H. (2001). Antioxidants, programmed cell death and cancer. Nutrition Research 21, 295–307.Google Scholar
Lushchak, V. I. (2011). Environmentally induced oxidative stress in aquatic animals. Aquatic Toxicology 101, 13–30.Google Scholar
Mas-Coma, S., Bargues, M. D. and Valero, M. A. (2005). Fascioliasis and other plant-borne trematode zoonoses. International Journal for Parasitology 35, 1255–1278.CrossRefGoogle ScholarPubMed
Mas-Coma, S., Bargues, M. D. and Valero, M. A. (2014). Diagnosis of human fascioliasis by stool and blood techniques: update for the present global scenario. Parasitology 141, 1918–1946.Google Scholar
Mills, J. H., Kim, D. G., Krenz, A., Chen, J. F. and Boyne, M. S. (2012). A2A adenosine receptor signaling in lymphocytes and the central nervous system regulates inflammation during experimental autoimmune encephalomyelitis. Journal of Immunology 188, 5713–5722.Google Scholar
Misra, H. P. and Fridovich, I. (1972). The role of superoxide anion in the autoxidation of epinephrine and a simple assay for superoxide dismutase. Journal of Biological Chemistry 247, 3170–3175.Google Scholar
Murphy, M. P., Holmgren, A., Larsson, N.G., Halliwell, B., Chang, C. J., Kalyanaraman, B., Rhee, S. G., Thornalley, P. J., Partridge, L., Gems, D., Nyström, T., Belousov, V., Schumacker, P. T. and Winterbourn, C. C. (2011). Unravelling the biological roles of reactive oxygen species. Cell Metabolism 13, 361–366.Google Scholar
Nelson, D. P. and Kiesow, L. A. (1972). Enthalpy of the composition of hydrogen peroxide by catalase at 25 °C. Analytical Biochemistry 49, 474–479.Google Scholar
Ohkawa, H., Ohishi, N. and Yagi, K. (1979). Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Analytical Biochemistry 95, 351–358.Google Scholar
Paglia, D. E. and Valentine, W. N. (1967). Studies on the quantitative and qualitative characterization of erythrocytes glutathione peroxidase. Journal of Laboratory and Clinical Medicine 70, 158–169.Google Scholar
Piedrafita, D., Spithill, T. W., Smith, R. E. and Raadsma, H. W. (2010). Improving animal and human health through understanding liver fluke immunology. Parasite Immunology 32, 572–581.Google Scholar
Salimi-Bejestani, M. R., McGarry, J. W., Felstead, S., Ortiz, P., Akca, A. and Williams, D. J. L. (2005). Development of an antibody-detection ELISA for Fasciola hepatica and its evaluation against a commercially available test. Research in Veterinary Science 78, 177–181.Google Scholar
Sarin, K., Kumar, A., Prakash, A. and Sharma, A. (1993). Oxidative stress and antioxidant defense mechanism in Plasmodium vivax malaria before and after chloroquine treatment. Indian Journal of Malariology 30, 127–133.Google Scholar
Sena, L. A. and Chandel, N. S. (2012). Physiological roles of mitochondrial reactive oxygen species. Molecular and Cellular Biochemistry 48, 158–167.Google Scholar
Shao, B., Zhu, L. S., Dong, M., Wang, J., Wang, J., Xie, H., Zhang, Q., Du, Z. and Zhu, S. (2012). DNA damage and oxidative stress induced by endosulfan exposure in zebrafish (Danio rerio). Ecotoxicology 21, 1533–1540.CrossRefGoogle ScholarPubMed
Thrall, M. A., Weiser, G., Allison, R. W. and Campbell, T. W. (2012). Veterinary Hematology and Clinical Chemistry, 2nd edn. Wiley-Blackwell, State Avenue, Ames, Iowa. 762p.Google Scholar
Ueno, H. and Gonçalves, P. C. (1994). Manual for the Diagnosis of Helminths of Ruminants, 3nd edn. JICA, Porto Alegre, 62p.Google Scholar
Winterbourne, C. C. (2015). Are free radicals involved in thiol-based redox signaling? Free Radical Biology and Medicine 80, 164–170.CrossRefGoogle Scholar