J Appl Biomed 13:161-167, 2015 | DOI: 10.1016/j.jab.2014.11.002

Systemic oxidative stress in victims of Bothrops snakebites

Juliana de Ornellas Strapazzona, Eduardo Benedetti Parisottoa, Ana Maria Moratellia, Thais Regina Garleta, Juliana Bastosb, Ivan Ricardo Zimermannc, Marlene Zaninc, Rodrigo Fagundeza, Manuel Rosa de Oliveira Linod, Tânia Silvia Frödee, Danilo Wilhelm Filhoa,*
a Department of Ecology and Zoology, Federal University of Santa Catarina, Florianópolis, Brazil
b Department of Chemistry, Federal University of Santa Catarina, Florianópolis, Brazil
c Center for Toxicological Information, Federal University of Santa Catarina, Florianópolis, Brazil
d Department of Informatics and Statistics, Federal University of Santa Catarina, Florianópolis, Brazil
e Department of Clinical Analysis, Federal University of Santa Catarina, Florianópolis, Brazil

The genus Bothrops is responsible for approximately 90% of snakebites in Brazil. In the present study biomarkers of oxidative stress (OS) were evaluated in the blood of victims of snakebites from Bothrops jararaca and Bothrops jararacussu. Patient monitoring started from the emergency entrance at the hospital up to 30 days, groups divided as follows: time 0 (t0), 24 hours (t24h), 7 days (t7d) and 30 days (t30d). The activities of catalase (CAT), superoxide dismutase (SOD), glutathione peroxidase (GPx), glutathione reductase (GR), glutathione S-transferase (GST), and myeloperoxidase (MPO), as well as the contents of reduced glutathione (GSH), vitamin E, lipid peroxidation (TBARS), protein carbonyls (PC) were examined in blood. Initial determinations revealed increased CAT, GR and GPx activities and decreased SOD and GST activities together with the depletion of GSH contents, while markers of oxidative damage showed increased TBARS levels and decreased PC concentrations in victims of snakebite compared to controls (blood donors). Regarding the temporal effect, no statistical differences among the groups were detected for the distinct parameters analyzed. The responses obtained in OS biomarkers in victims of snakebite compared to healthy subjects indicate that Bothrops envenomation promoted a pronounced and persistent systemic OS in the blood of those subjects.

Keywords: Snakebites; Bothrops; Ophidic accidents; Inflammation; Oxidative stress; Antioxidants

Received: August 8, 2014; Revised: November 13, 2014; Accepted: November 19, 2014; Published: May 1, 2015  Show citation

ACS AIP APA ASA Harvard Chicago Chicago Notes IEEE ISO690 MLA NLM Turabian Vancouver
de Ornellas Strapazzon J, Benedetti Parisotto E, Moratelli AM, Garlet TR, Bastos J, Zimermann IR, et al.. Systemic oxidative stress in victims of Bothrops snakebites. J Appl Biomed. 2015;13(2):161-167. doi: 10.1016/j.jab.2014.11.002.
Download citation

References

  1. Aebi, H., 1984. Catalase in vitro. Methods Enzymol. 204, 234-254. Go to original source... Go to PubMed...
  2. Albuquerque, P.L., Jacinto, C.N., Silva Junior, G.B., Lima, J.B., Veras Mdo, S., Daher, E.F., 2013. Acute kidney injury caused by Crotalus and Bothrops snake venom: a review of epidemiology, clinical manifestations and treatment. Rev. Inst. Med. Trop. Sao Paulo 55 (5), 295-301. Go to original source... Go to PubMed...
  3. Beutler, E., Duron, O., Kelly, B.M., 1963. Improved method for the determination of blood glutathione. J. Lab. Clin. Med. 61, 882-890.
  4. Bernarde, P.S., 2014. Serpentes Peçonhentas e Acidentes Ofídicos no Brasil. Anolis Books, Curitiba, Brasil230.
  5. Bird, R.P., Draper, A.H., 1984. Comparative studies on different methods of malondialdehyde determination. Methods Enzymol. 90, 105-110. Go to original source... Go to PubMed...
  6. Boveris, A., Cadenas, E., 1997. Cellular sources and steady-state levels of reactive oxygen species. In: Clerçk, L., Massaro, D. (Eds.), Oxygen, Gene Expression and Cellular Function, vol. 105. Marcel Dekker, New York, pp. 1-25.
  7. Calberg, I., Mannervik, B., 1985. Glutathione reductase from rat liver. Methods Enzymol. 113, 484-490. Go to original source... Go to PubMed...
  8. Cardoso, J.L.C., França, F.O.S., Fan, H.W., Málaque, C.M.S., Vidal, H.J., 2003. Animais Peçonhentos no Brasil: Biologia, Clínica e Terapêutica dos Acidentes. Sarvier, Cap: 2-6.
  9. Castro, I., Burdmann, E.A., Seguro, A.C., Yu, L., 2003. Bothrops venom induces direct renal tubular injury: role for lipid peroxidation and prevention by antivenom. Toxicon 43, 833-839. Go to original source... Go to PubMed...
  10. Clissa, P.B., Laing, G.D., Davis, R., Theakston, G., Mota, I., Taylor, M.J., Moura da Silva, A.M., 2001. The effect of jararhagin, a metalloproteinase from Bothrops jararaca venom, on proinflammatory cytokines released by murine peritoneal adherent cells. Toxicon 39, 1567-1573. Go to original source... Go to PubMed...
  11. Costa, E.P., Clissa, P.B., Teixeira, C.F., Moura-da-Silva, A.M., 2002. Importance of metalloproteinases and macrophages in viper snake envenomation-induced local inflammation. Inflammation 26 (1), 13-17. Go to original source... Go to PubMed...
  12. Farias, M.S., Budni, P., Ribeiro, C.M., Parisotto, E.B., Santos, C.E., Dias, J.F., Dalmarco, E.M., Fröde, T.S., Pedrosa, R.C., Wilhelm Filho, D., 2012. Antioxidant supplementation attenuates oxidative stress in chronic hepatitis C patients. Gastroenterol. Hepatol. 35, 386-394. Go to original source... Go to PubMed...
  13. Ferreira, A.L.A., Matsubara, L.S., 1997. Radicais livres: conceitos, doenças relaciondas, sistema de defesa e estresse oxidativo. Revista da Associação Médica Brasileira 43, 61-68. Go to original source... Go to PubMed...
  14. Flohé, L., Gunzler, W.A., 1984. Assays of glutathione peroxidase. Methods Enzymol. 105, 114-121. Go to original source... Go to PubMed...
  15. França, F.O.S., Málaque, C.M.S., 2003. Acidente botrópico. In: Animais peçonhentos no Brasil: biologia, clínica e terapêutica dos acidentes. Cardoso et al. (Orgs.). Sarvier, São Paulo, SP72-86.
  16. Habig, W.H., Pabst, M.J., Jacoby, W.B., 1976. Glutathione S-transferases: the first enzymatic step in mercapturic acid formation. J. Biol. Chem. 249, 7130-7139. Go to original source...
  17. Halliwell, B., Gutteridge, J.M.C., 2007. Free Radicals in Biology and Medicine, 4th ed. Clarendon Press, Oxford.
  18. Ishii, Y., Partridge, C.A., Del Vecchio, P.J., Malik, A.B., 1992. Tumor necrosis factor-a-mediated decrease in glutathione increase the sensitivity of pulmonary vascular endothelial cells to H2O2. J. Clin. Invest. 89, 794-802. Go to original source... Go to PubMed...
  19. Izidoro, I.L.F.M., Sobrinho, J.C., Mendes, M.M., Costa, T.R., Grabner, A.N., Rodrigues, V.M., da Silva, S.L., Zanchi, F.B., Zuliani, J.P., Fernandes, C.F.C., Calderon, L.A., Stábeli, R.G., Soares, A.M., 2014. Snake venom L-amino acid oxidases: trends in pharmacology and biochemistry. Biomed. Res. Int. 1-19. Go to original source...
  20. Kuebler, W.M., Abels, C., Schuerer, L., Goetz, A.E., 1996. Measurement of neutrophil content in brain and lung tissue by a modified myeloperoxidase assay. Int. J. Microcirc. Clin. Exp. 16, 89-97. Go to original source... Go to PubMed...
  21. Levine, R.L., Garland, D., Oliver, C.N., Amici, A., Climent, I., Lenz, A.G., Ahn, B.W., Shaltiel, S., Stadtman, E.R., 1990. Determination of carbonyl content in oxidatively modified proteins. Methods Enzymol. 186, 464-478. Go to original source... Go to PubMed...
  22. Maçao, L.B., Wilhelm Filho, D., Pedrosa, R.C., Pereira, A., Backes, P., Torres, M.A., Fröde, T.S., 2007. Antioxidant therapy attenuates oxidative stress in chronic cardiopathy associated with Chagas' disease. Int. J. Cardiol. 123, 43-49. Go to original source... Go to PubMed...
  23. Mingjian, Z., Qifang, W., Lanxing, G., Hong, J., Zongyin, W., 1992. Comparative observation of the changes in serum lipid peroxides influenced by the supplementation of vitamin E in burn patients and healthy controls. Burns 18 (1), 19-21. Go to original source... Go to PubMed...
  24. Misra, H.P., Fridovich, I., 1972. The role of superoxide anion in the autoxidation of epinephrine and a simple assay for superoxide dismutase. J. Biol. Chem. 247, 188-192. Go to original source...
  25. Moreno, S.N.J., Palmero, D.J., Palmero, K.E., Docampo, R., Stoppani, A.O.M., 1980. Stimulation of lipid peroxidation and ultrastructural alterations induced by nifurtimox in mammalian tissues. Medicina 40, 553-559.
  26. Nicoletti, G., Crescibene, L., Scornaienchi, M., Bastone, L., Bagalà, A., Napoli, I.D., Caracciolo, M., Quattroneb, A., 2001. Plasma levels of vitamin E in Parkinson's disease. Arch. Gerontol. Geriatr. 37, 7-12. Go to original source... Go to PubMed...
  27. Oliveira, A.L., Burdmann, E.A., Seguro, A.C., Yua, L., 2008. Avaliação epidemiológica e laboratorial de pacientes que sofreram acidente ofidico na cidade de Miracatu (Vale do Ribeira, São Paulo). Rev. Patol. Tropic. 37, 268-274. Go to original source...
  28. Oliveira Junior, E.A.B., 2004. Alpha glutationa S-Transferase: marcador de lesão hepática em pacientes com hepatite pelo vírus C? (148 f. Tese)Faculdade de Medicina da Universidade de São Paulo, São Paulo.
  29. Oury, T.D., Schaefer, L.M., Fattman, C.L., Choi, A., Weck, K.E., Watkins, S.C., 2002. Depletion of pulmonary EC-SOD after exposure to hyperoxia. Am. J. Physiol. Lung Cell. Mol. Physiol. 283, 777-784. Go to original source... Go to PubMed...
  30. Parisotto, E.B., Garlet, T.R., Cavalli, V.L.L.O., Zamoner, A., Rosa, J. S., Bastos, J., Micke, G.A., Frode, T.S., Pedrosa, R.C., Wilhelm Filho, D., 2014. Antioxidant intervention attenuates oxidative stress in children and teenagers with Down syndrome. Res. Dev. Disabil. 35, 1228-1236. Go to original source... Go to PubMed...
  31. Petrecevich, V.L., Teixeira, C.F.P., Tambourgi, D.V., Gutiérrez, J. M., 2000. Increments in cytokine and nitric oxide serum levels in mice injected with Bothrops asper and Bothrops jararaca snake venoms. Toxicon 38, 1253-1266. Go to original source... Go to PubMed...
  32. Phelps, D.T., Ferro, T.J., Higgins, P.J., Shankar, R., Parker, D.M., Johnson, A., 1995. TNF-a induces peroxynitrite-mediated depletion of lung endothelial glutathione via protein kinase C. Am. J. Physiol. 269, 551-559. Go to original source... Go to PubMed...
  33. Rao, T.S., Currie, J.L., Shaffer, A.F., Isakson, P.C., 1993. Comparative evaluation of arachidonic acid (AA)- and tetradecanoylphorbol acetate (TPA)-induced dermal inflammation. Inflammation 17, 723-741. Go to original source... Go to PubMed...
  34. Sies, H., 1991. Oxidative Stress. Oxidants and Antioxidants. Academic Press, 650.
  35. Ueda, J., Starr, M.E., Takahashi, H., Du, J., Chang, Y.L., Crapo, J.D., Evers, M.B., Saito, H., 2008. Decreased pulmonary extracellular superoxide dismutase during systemic inflammation. Free Radic. Biol. Med. 45, 897-904. Go to original source... Go to PubMed...
  36. Wüster, W., Thorpe, R., Salomão, M.G., Thomas, L., Puorto, G., Theakston, R.D.G., Warrel, D.A., 2002. Origin and phylogenetic position of the Lesser Antillean species of Bothrops (Serpentes, Viperidae): biogeographical and medical implications. Bull. Nat. Hist. Mus. London 68, 101-106. Go to original source...
  37. Yadav, D., Hertan, H.I., Schweitzer, P., Norkus, E.P., Pitchumoni, C.S., 2002. Serum and liver micronutrient antioxidants and serum oxidative stress in patients with chronic hepatitis C. Am. J. Gastroenterol. 97, 2634-2639. Go to original source... Go to PubMed...
  38. Zamuner, S.R., Gutierrez, J.M., Muscara, M.N., Teixeira, A.S., Teixeira, C.F., 2001. Bothrops asper and Bothrops jararaca snake venoms trigger microbicidal functions of peritoneal leukocytes in vivo. Toxicon 39, 1505-1513. Go to original source... Go to PubMed...