Table of Contents Author Guidelines Submit a Manuscript
Evidence-Based Complementary and Alternative Medicine
Volume 2014, Article ID 383482, 10 pages
http://dx.doi.org/10.1155/2014/383482
Research Article

Protective Effect of Repeatedly Preadministered Brazilian Propolis Ethanol Extract against Stress-Induced Gastric Mucosal Lesions in Rats

1Japan Beekeeping Co. Ltd., Gifu 500-8691, Japan
2Department of Chemistry, Fujita Health University School of Medicine, Toyoake, Aichi 470-1192, Japan
3Department of Clinical Biochemistry, Faculty of Medical Technology, Fujita Health University School of Health Sciences, Toyoake, Aichi 470-1192, Japan
4Faculty of Health and Nutrition, Shubun University, Ichinomiya, Aichi 491-0938, Japan

Received 5 November 2013; Accepted 20 December 2013; Published 3 February 2014

Academic Editor: Vassya Bankova

Copyright © 2014 Tadashi Nakamura et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. A. H. Banskota, Y. Tezuka, and S. Kadota, “Recent progress in pharmacological research of propolis,” Phytotherapy Research, vol. 15, no. 7, pp. 561–571, 2001. View at Publisher · View at Google Scholar · View at Scopus
  2. J. M. Sforcin, “Propolis and the immune system: a review,” Journal of Ethnopharmacology, vol. 113, no. 1, pp. 1–14, 2007. View at Publisher · View at Google Scholar · View at Scopus
  3. M. Vidda-Martos, Y. Ruìz-Navajas, J. Fernández-López, and J. A. Pérez-Álvarez, “Functional properties of honey, propolis, and royal jelly,” Journal of Food Science, vol. 273, no. 9, pp. R117–R123, 2008. View at Google Scholar
  4. M. Marcucci, “Propolis: chemical composition, biological properties and therapeutic activity,” Apidologie, vol. 26, no. 2, pp. 83–99, 1995. View at Google Scholar · View at Scopus
  5. K. Midorikawa, A. H. Banskota, Y. Tezuka et al., “Liquid chromatography-mass spectrometry analysis of propolis,” Phytochemical Analysis, vol. 12, no. 6, pp. 366–373, 2001. View at Publisher · View at Google Scholar · View at Scopus
  6. M. Lemos, M. P. De Barros, J. P. B. Sousa, A. A. Da Silva Filho, J. K. Bastos, and S. F. De Andrade, “Baccharis dracunculifolia, the main botanical source of Brazilian green propolis, displays antiulcer activity,” Journal of Pharmacy and Pharmacology, vol. 59, no. 4, pp. 603–608, 2007. View at Publisher · View at Google Scholar · View at Scopus
  7. M. P. de Barros, M. Lomos, E. L. Maistro, and S. F. de Amdrade, “Effect of Brazilian green propolis on experimental gastric ulcers in rats,” Journal of Ethnopharmacology, vol. 110, no. 3, pp. 372–377, 2007. View at Google Scholar
  8. M. P. D. Barros, M. Lemos, E. L. Maistro et al., “Evaluation of antiulcer activity of the main phenolic acids found in Brazilian Green Propolis,” Journal of Ethnopharmacology, vol. 120, no. 3, pp. 372–377, 2008. View at Publisher · View at Google Scholar · View at Scopus
  9. T. Yoshikawa, H. Miyagawa, N. Yoshida, S. Sugino, and M. Kondo, “Increase in lipid peroxidation in rat gastric mucosal lesions induced by water-immersion restraint stress,” Journal of Clinical Biochemistry and Nutrition, vol. 1, no. 3, pp. 271–277, 1986. View at Google Scholar
  10. K. Nishida, Y. Ohta, T. Kobayashi, and I. Ishiguro, “Involvement of the xanthine-xanthine oxidase system and neutrophils in the development of acute gastric mucosal lesions in rats with water immersion restraint stress,” Digestion, vol. 58, no. 4, pp. 340–351, 1997. View at Google Scholar · View at Scopus
  11. K. Nishida, Y. Ohta, and I. Ishiguro, “Role of gastric mucosal constitutive and inducible nitric oxide synthases in the development of stress-induced gastric mucosal lesions in rats,” Biochemical and Biophysical Research Communications, vol. 236, no. 2, pp. 275–279, 1997. View at Publisher · View at Google Scholar · View at Scopus
  12. K. Nishida, Y. Ohta, and I. Ishiguro, “Contribution of NO synthases to neutrophil infiltration in the gastric mucosal lesions in rats with water immersion restraint stress,” FEBS Letters, vol. 425, no. 2, pp. 243–248, 1998. View at Publisher · View at Google Scholar · View at Scopus
  13. K. Nishida, Y. Ohta, and I. Ishiguro, “Relation of inducible nitric oxide synthase activity to lipid peroxidation and nonprotein sulfhydryl oxidation in the development of stress-induced gastric mucosal lesions in rats,” Nitric Oxide, vol. 2, no. 4, pp. 215–223, 1998. View at Publisher · View at Google Scholar · View at Scopus
  14. K. Nishida, Y. Ohta, and I. Ishiguro, “Changes in nitric oxide production with lesion development in the gastric mucosa of rats with water immersion restraint stress,” Research Communications in Molecular Pathology and Pharmacology, vol. 100, no. 2, pp. 201–212, 1998. View at Google Scholar · View at Scopus
  15. M. Hamaguchi, T. Watanabe, K. Higuchi, K. Tominaga, Y. Fujiwara, and T. Arakawa, “Mechanisms and roles of neutrophil infiltration in stress-induced gastric injury in rats,” Digestive Diseases and Sciences, vol. 46, no. 12, pp. 2708–2715, 2001. View at Publisher · View at Google Scholar · View at Scopus
  16. K. Yasukawa, K. Kasazaki, F. Hyodo, and H. Utsumi, “Non-invasive analysis of reactive oxygen species generated in rats with water immersion restraint-induced gastric lesions using in vivo electron spin resonance spectroscopy,” Free Radical Research, vol. 38, no. 2, pp. 147–155, 2004. View at Publisher · View at Google Scholar · View at Scopus
  17. Y. Ohta, Y. Kamiya, Y. Imai, T. Arisawa, and H. Nakano, “Role of gastric mucosal ascorbic acid in gastric mucosal lesion development in rats with water immersion restraint stress,” Inflammopharmacology, vol. 13, no. 1–3, pp. 249–259, 2005. View at Publisher · View at Google Scholar · View at Scopus
  18. Y. Ohta, S. Chiba, Y. Imai, Y. Kamiya, T. Arisawa, and A. Kitagawa, “Ascorbic acid deficiency aggravates stress-induced gastric mucosal lesions in genetically scorbutic ODS rats,” Inflammopharmacology, vol. 14, no. 5-6, pp. 231–235, 2006. View at Publisher · View at Google Scholar · View at Scopus
  19. Y. Ohta, Y. Imai, S. Kaida, Y. Kamiya, M. Kawanishi, and I. Hirata, “Vitamin E protects against stress-induced gastric mucosal lesions in rats more effectively than vitamin C,” BioFactors, vol. 36, no. 1, pp. 60–69, 2010. View at Publisher · View at Google Scholar · View at Scopus
  20. T. Nakamura, Y. Ohta, M. Tada et al., “Protective effect of Brazilian propolis ethanol extract against stress-induced gastric mucosal lesions in rats. Its evaluation using oxidative stress markers,” Journal of Analytical Bio-Science, vol. 34, no. 2, pp. 135–146, 2011. View at Google Scholar
  21. H. Izuta, Y. Narahara, M. Shimazawa, S. Mishima, S.-I. Kondo, and H. Hara, “1,1-diphenyl-2-picrylhydrazyl radical scavenging activity of bee products and their constituents determined by ESR,” Biological and Pharmaceutical Bulletin, vol. 32, no. 12, pp. 1947–1951, 2009. View at Publisher · View at Google Scholar · View at Scopus
  22. E. Szliska, A. Z. Kucharska, A. Sokół-Łętowska, A. Q. Mertas, Z. P. Czuba, and W. Król, “Chemical composition and anti-inflammatory effect of ethanolic extract of Brazilian green propolis on activated J1774A. 1 macrophages,” Evidence-Based Complementary and Alternative Medicine, vol. 2013, Article ID 976415, 13 pages, 2013. View at Publisher · View at Google Scholar
  23. Y. Nakajima, K. Tsuruma, M. Shimazawa S, Mishima, and H. Hara, “Comparison of bee products based on assays of antioxidant capacities,” BMC Complement Alternative Medicine, vol. 9, article 4, 2009. View at Publisher · View at Google Scholar
  24. L. E. Dowd, “Spectrophotometric determination of quercetin,” Analytical Chemistry, vol. 31, no. 7, pp. 1184–1187, 1959. View at Google Scholar · View at Scopus
  25. M.-R. Ahn, S. Kumazawa, T. Hamasaka, K.-S. Bang, and T. Nakayama, “Antioxidant activity and constituents of propolis collected in various areas of Korea,” Journal of Agricultural and Food Chemistry, vol. 52, no. 24, pp. 7286–7292, 2004. View at Publisher · View at Google Scholar · View at Scopus
  26. K. Takagi and S. Okabe, “The effects of drugs on the production and recovery processes of the stress ulcer,” Japanese Journal of Pharmacology, vol. 18, no. 1, pp. 9–18, 1968. View at Google Scholar · View at Scopus
  27. J. Sedlak and R. H. Lindsay, “Estimation of total, protein-bound, and nonprotein sulfhydryl groups in tissue with Ellman's reagent,” Analytical Biochemistry, vol. 25, pp. 192–205, 1968. View at Google Scholar · View at Scopus
  28. Y. Kamiya, Y. Ohta, Y. Imai, T. Arisawa, and H. Nakano, “A critical role of gastric mucosal ascorbic acid in the progression of acute gastric mucosal lesions induced by compound 48/80 in rats,” World Journal of Gastroenterology, vol. 11, no. 9, pp. 1324–1332, 2005. View at Google Scholar · View at Scopus
  29. V. Zannoni, M. Lynch, S. Goldstein, and P. Sato, “A rapid micromethod for the determination of ascorbic acid in plasma and tissues,” Biochemical Medicine, vol. 11, no. 1, pp. 41–48, 1974. View at Google Scholar · View at Scopus
  30. H. Ohkawa, N. Ohishi, and K. Yagi, “Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction,” Analytical Biochemistry, vol. 95, no. 2, pp. 351–358, 1979. View at Google Scholar · View at Scopus
  31. L. C. Green, D. A. Wagner, and J. Glogowski, “Analysis of nitrate, nitrite, and [15N]nitrate in biological fluids,” Analytical Biochemistry, vol. 126, no. 1, pp. 131–138, 1982. View at Google Scholar · View at Scopus
  32. S. Hashimoto, “A new spectrophotometric assay method of xanthine oxidase in crude tissue homogenate,” Analytical Biochemistry, vol. 62, no. 2, pp. 426–435, 1974. View at Google Scholar · View at Scopus
  33. K. Suzuki, H. Ota, and S. Sasagawa, “Assay method for myeloperoxidase in human polymorphonuclear leukocytes,” Analytical Biochemistry, vol. 132, no. 2, pp. 345–352, 1983. View at Google Scholar · View at Scopus
  34. R. Guillemin, G. W. Clayton, H. S. Lipscomb, and J. D. Smith, “Fluorometric measurement of rat plasma and adrenal corticosterone concentration. A note on technical details,” The Journal of Laboratory and Clinical Medicine, vol. 53, no. 5, pp. 830–832, 1959. View at Google Scholar · View at Scopus
  35. Y. Ohta, S. Kaida, S. Chiba et al., “Involvement of oxidative stress in increases in the serum levels of various enzymes and components in rats with water-immersion restraint stress,” Journal of Clinical Biochemistry and Nutrition, vol. 45, no. 3, pp. 347–354, 2009. View at Publisher · View at Google Scholar · View at Scopus
  36. S. C. Boyd, H. A. Sasame, and M. R. Boyd, “High concentrations of glutathione in glandular stomach: possible implications for carcinogenesis,” Science, vol. 205, no. 4410, pp. 1010–1012, 1979. View at Google Scholar · View at Scopus
  37. K. Yoshizumi, N. Nishioka, and T. Tsuji, “The xanthine oxidase inhibitory activity and hypouricemia effect of the propolis in rats,” Yakugaku Zasshi, vol. 125, no. 3, pp. 315–321, 2005. View at Publisher · View at Google Scholar · View at Scopus
  38. R. Shinohara, Y. Ohta, T. Hayashi, and T. Ikeno, “Evaluation of antilipid peroxidative action of propolis ethanol extract,” Phytotherapy Research, vol. 16, no. 4, pp. 340–347, 2002. View at Publisher · View at Google Scholar · View at Scopus
  39. F. D. Marquele, V. M. Di Mambro, S. R. Georgetti, R. Casagrande, Y. M. L. Valim, and M. J. V. Fonseca, “Assessment of the antioxidant activities of Brazilian extracts of propolis alone and in topical pharmaceutical formulations,” Journal of Pharmaceutical and Biomedical Analysis, vol. 39, no. 3-4, pp. 455–462, 2005. View at Publisher · View at Google Scholar · View at Scopus
  40. K. Shimizu, H. Ashida, Y. Matsuura, and K. Kanazawa, “Antioxidative bioavailability of artepillin C in Brazilian propolis,” Archives of Biochemistry and Biophysics, vol. 424, no. 2, pp. 181–188, 2004. View at Publisher · View at Google Scholar · View at Scopus
  41. D. Lamarque and B. J. R. Whittle, “Involvement of peroxynitrite in the lipid peroxidation induced by nitric oxide in rat gastric mucosa,” European Journal of Pharmacology, vol. 313, no. 1-2, pp. R5–R7, 1996. View at Publisher · View at Google Scholar · View at Scopus
  42. K. Tan-No, T. Nakajima, T. Shoji et al., “Anti-inflammatory effect of propolis through inhibition of nitric oxide production on carrageenin-induced mouse paw edema,” Biological and Pharmaceutical Bulletin, vol. 29, no. 1, pp. 96–99, 2006. View at Publisher · View at Google Scholar · View at Scopus
  43. N. Paulino, C. Teizeria, R. Martins et al., “Evaluation of the analgestic and anti-inflmmatory effects of Brazilian green propolis,” Planta Medica, vol. 72, no. 10, pp. 899–906, 2006. View at Google Scholar
  44. N. Paulino, S. R. L. Abreu, Y. Uto et al., “Anti-inflammatory effects of a bioavailable compound, Artepillin C, in Brazilian propolis,” European Journal of Pharmacology, vol. 587, no. 1–3, pp. 296–301, 2008. View at Publisher · View at Google Scholar · View at Scopus
  45. H. Ichikawa, K. Satoh, T. Tobe et al., “Free radical scavenging activity of propolis,” Redox Report, vol. 7, no. 5, pp. 347–350, 2002. View at Publisher · View at Google Scholar · View at Scopus
  46. L. M. C. Simões, L. E. Gregório, A. A. Da Silva Filho et al., “Effect of Brazilian green propolis on the production of reactive oxygen species by stimulated neutrophils,” Journal of Ethnopharmacology, vol. 94, no. 1, pp. 59–65, 2004. View at Publisher · View at Google Scholar · View at Scopus