Skip to main content
SpringerLink
Log in

The protective role of topical propolis on experimental keratitis via nitric oxide levels in rabbits

  • Published:
Molecular and Cellular Biochemistry Aims and scope Submit manuscript

Abstract

The aim of this study was to investigate antioxidant, anti-inflammatory, and antibacterial properties of propolis in the treatment of experimental Staphylococcus aureus keratitis. Twenty young New Zealand white rabbits were used in this experiment. Staphylococcus aureus were given by intrastromal injection to 16 rabbits and 4 rabbits were used as control group (Group 1). Group 2 was treated with phosphate-buffered solution drops; Group 3 was administered ethanolic extract of propolis drops; Group 4 received topical ciprofloxacin drops; Group 5 was treated with topical ciprofloxacin drops along with ethanolic extract of propolis drops. The eyes were examined by slit lamp to assess corneal opacity. And then, corneas were removed to determine nitric oxide (NO) levels and count bacteria. Corneas were also evaluated histologically. Corneal NO concentration in gruop 5, treated with a combination of propolis and ciprofloxacin was determined significantly lower (10.0± 1.8 μmol/g wet tissue) than in Group 4, treated with ciprofloxacin (24.0± 3.1 μmol/g wet tissue), from Group 3, treated with propolis (15.6± 1.8 μmol/g wet tissue), and treated with PBS (44.7± 7.8 μmol/g wet tissue). There were significantly fewer bacteria in eyes that received propolis plus ciprofloxacin than in eyes treated with ciprofloxacin (p = 0.0001) or propolis (p = 0.0001) or eyes treated with PBS (p = 0.0001). The light microscopic examination revealed that the control group showed normal corneal morphology. In the nontreated group, sections of the stromal infiltration revealed the presence of inflammatory cells, which were diffusely distributed (p < 0.05). Administrations of ciprofloxacin plus propolis resulted in a significantly reduced histological damage with fewer bacterial inoculation of the corneal stroma in comparison with the other groups (p < 0.05). Based on these findings, we suggest that ethanolic extract of propolis has antioxidant, anti-inflammatory, and antibacterial properties for S. aureus keratitis in rabbits.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Alexandrakis G, Alfonso EC, Miller D: Shifting trends in bacterial keratitis in south Florida and emerging resistance to fluoroquinolones. Ophthalmology 107: 1497–1502, 2000

    Article  PubMed  CAS  Google Scholar 

  2. Liesegang TJ: Bacterial and fungal keratitis. In: H. E. Kaufman (ed). The Cornea, 2nd edn. Butterworth-Heinemann, Boston, MA, 1998, pp. 159–219

    Google Scholar 

  3. Boston MA, Callegan MC, Engel LS, Hill JM, O'Callaghan RJ: Corneal virulence of Staphylococcus aureus: Roles of alpha-toxin and protein A in pathogenesis. Infect Immun 62: 2478–2482, 1994

    Google Scholar 

  4. Trinkaus-Randall V, Leibowitz HM, Ryan WJ, Kupferman A: Quantificationof stromal destruction in the inflamed cornea. Invest Ophthalmol Vis Sci 32: 603–609, 1991

    PubMed  CAS  Google Scholar 

  5. Leibowitz HM, Ryan WJ, Kupferman A, DeSantis L: Effect of concurrent topical corticosteroid and NSAID therapy of experimental keratitis. Invest Ophthalmol Vis Sci 27: 1226–1229, 1986

    PubMed  CAS  Google Scholar 

  6. Wilhelmus KR, Stulting RD, Sugar J, Khan MM: Primary corneal graft failure. A national reporting system. Medical Advisory Board of the Eye Bank Association of America. Arch Ophthalmol 113(12): 1497–1502, 1995

    Google Scholar 

  7. Goureau O, Bellot J, Thillaye B, Courtois Y, de Kozak Y: Increased nitric oxide production in endotoxin-induced uveitis: Reduction of uveitis by an inhibitor of nitric oxide synthase. J Immunol 154: 6518–6523, 1995

    PubMed  CAS  Google Scholar 

  8. Mandai M, Mittag TW, Kogishi J, Iwaki M, Hangai M, Yoshimura N: Role of nitric oxide synthase isozymes in endotoxin-induced uveitis. Invest Ophthalmol Vis Sci 37: 826–832, 1996

    PubMed  CAS  Google Scholar 

  9. Moncada S, Palmer RMJ, Higgs EA: Nitric oxide: physiology, pathophysiology and pharmacology. Pharmacol Rev 43: 109–141, 1991

    PubMed  CAS  Google Scholar 

  10. Knowles RG, Moncada S: Nitric oxide synthase in mammals. Biochem J 298: 249–258, 1994

    PubMed  CAS  Google Scholar 

  11. Kröncke KD, Fehsel K, Kolb-Bachofen V: Inducible nitric oxide synthase and its product nitric oxide, a small molecule with complex biological activities. Biol Chem Hoppe-Seyler 376: 327–343, 1995

    PubMed  Google Scholar 

  12. De Castro SL: Propolis: biological and pharmacological activities. Therapeutic uses of this bee-product. Annu Rev Biol Sci 3: 49–83, 2001

    CAS  Google Scholar 

  13. Banskota AH, Tezuka Y, Kadota S: Recent progress in pharmacological research of propolis Phytother Res 15: 561–571, 2001

    Article  PubMed  CAS  Google Scholar 

  14. Dobrowolski JW, Vohora SB, Sharma K, Shah SA, Naqvi SA, Dandiya PC: Antibacterial, antifungal, antiamoebic, anti-inflammatory, and antipyretic studies on propolis bee products. J Ethnopharmacol 35: 77–82, 1991

    Article  PubMed  CAS  Google Scholar 

  15. Khayyal MT, el-Ghazaly MA, el-Khatip AS: Mechanisms involved in the anti-inflammatory effect of propolis extract. Drugs Exp Clin Res 19: 197–203, 1993

    PubMed  CAS  Google Scholar 

  16. Bankova VS, de Castro SL, Marcucci MC: Propolis: Recent advances in chemistry and plant origin. Apidologie 31: 3–15, 2000

    Article  CAS  Google Scholar 

  17. Song YS, Park EH, Hur GM, Ryu YS, Lee YS, Lee JY, Kim YM, Jin C: Caffeic acid phenethyl ester inhibits nitric oxide synthase gene expression and enzyme activity. Cancer Lett 175: 53–61, 2002

    Article  PubMed  CAS  Google Scholar 

  18. National Committee for Clinical Laboratory Standards (NCCLS): Methods for dilution antimicrobial susceptibility tests for bacteria that grow aerobically. Approved Standard M7-A4, Viallanova, PA, 1997

  19. Beisel KW, Hazlett LD, Berk RS: Dominant susceptibility effect on the murine corneal response to Pseudomonas aeruginosa. Proc Soc Exp Med 172: 488–491, 1983

    CAS  Google Scholar 

  20. Cortas NK, Wakid NW: Determination of inorganic nitrate in serum and urine by a kinetic cadmium-reduction metod. Clin Chem 36: 1440–1443, 1990

    PubMed  CAS  Google Scholar 

  21. Chusid MJ, Davis SD: Experimental keratitis in neutropenic guinea pigs: Polymorphonuclear leukoytes in corneal host defense. Infect Immun 24: 948–952, 1979

    PubMed  CAS  Google Scholar 

  22. Vajpayee RB, Sharma N, Chand M, Tabin GC, Vajpayee M, Anand JR: Corneal superinfection in acute hemorrhagic conjunctivitis. Cornea 17: 614–617, 1998

    Article  PubMed  CAS  Google Scholar 

  23. Elgebaly SA, Miano DC, Kreutzer DL, Fishman JB: Cornea derived neutrophil chemotactic factors: Intracellular synthesis and release. Curr Eye Res 9: 839–845, 1990

    Article  PubMed  CAS  Google Scholar 

  24. MacMicking J, Xie Q, Nathan C: Nitric oxide and macrophage function. Ann Rev Immunol 15: 323–350, 1997

    Article  CAS  Google Scholar 

  25. Mandai M, Yoshimura N, Yoshida M, Iwaki M, Honda Y: The role of nitric oxide synthase in endotoxin-induced uveitis: Effects of NG-nitro l-arginine. Invest Ophthalmol Vis Sci 35: 3673–3679, 1994

    PubMed  CAS  Google Scholar 

  26. Croen K: Evidence for an antiviral effect of nitric oxide J Clin Invest 91: 2446–2452, 1993

    Article  PubMed  CAS  Google Scholar 

  27. Bredt DS, Snyder SH: Nitric oxide: a physiological messenger molecule. Ann Rev Biochem 63: 175–195, 1994

    Article  PubMed  CAS  Google Scholar 

  28. Geyer O, Almong J, Lupu-Meiri M: Nitric oxide synthase inhibitors protect rat retina against ischemic injury. FEBS Lett 374: 399–402, 1995

    Article  PubMed  CAS  Google Scholar 

  29. Nathanson JA, Mckee M: Alternation of human nitric oxide synthase in human glaucoma Invest Ophthalmol Vis Sci 36: 1774–1784, 1995

    Google Scholar 

  30. Courtois BY, Goureau O: Nitric oxide in the eye: Multifaceted roles and diverse outcomes Surv Ophthalmol 42: 71–82, 1997

    Article  PubMed  Google Scholar 

  31. Castaldo S, Capasso F: Propolis, an old remedy used in modern medicine. Fitoterapia 73: S1–S6, 2002

    Article  PubMed  CAS  Google Scholar 

  32. Pascual C, Gonzalez R, Torricella RG: Scavenging action of propolis extract against oxygen radicals. J Ethnopharmacol 41: 9–13, 1994

    Article  PubMed  CAS  Google Scholar 

  33. Ichikawa H, Satoh K, Tobe T, Yasuda I, Ushio F, Matsumoto K, Endo K, Ookubo C: Free radical scavenging activity of propolis. Redox Rep 7: 347–350, 2002

    Article  PubMed  Google Scholar 

  34. Krol W, Scheller S, Czuba Z, Matsuno T, Zydowicz G, Shani J, Mos M: Inhibition of neutrophils chemiluminescence by ethanolic extract of propolis (EEP) and its phenolic components. J Ethnopharmacol 55: 19–25, 1996

    Article  PubMed  CAS  Google Scholar 

  35. Strehl E, Volpert R, Elstner EF: Biochemical activities of propolis extracts: III Inhibition of dehydrofolate reductase. Z Naturforsch 49: 39–43, 1994

    CAS  Google Scholar 

  36. Callegan MC, Hobden JA, Hill JM, Insler MS, O'Callaghan RJ: Topical antibiotic therapy for the treatment of experimental Staphylococcus aureus keratitis. Invest Ophthalmol Vis Sci 33: 3017–3023, 1992

    PubMed  CAS  Google Scholar 

  37. Huang Y, Meek KM, Ho MW, Paterson CA: Anaylsis of birefringence during wound healing and remodeling following alkali burns in rabbit cornea. Exp Eye Res 73: 521–532, 2001

    Article  PubMed  CAS  Google Scholar 

  38. Oksuz H, Duran N, Koc A, Tamer C, Akaydı n Y, Cetin M, Silici S: Effect of propolis for treatment of experimental Staphylococcus aureus keratitis in rabbits. Ophthalmic Res (in press)

Download references

Author information

Authors and Affiliations

  1. Department of Microbiology, Faculty of Medicine, Mustafa Kemal University, Hatay, Turkey

    N. Duran

  2. Department of Histology, Mustafa Kemal University, Faculty of Veterinary, Hatay, Turkey

    A. Koc, Y. Akaydin & T. Kozlu

  3. Department of Ophthalmology, Mustafa Kemal University, Faculty of Medicine, Hatay, Turkey

    H. Oksuz & C. Tamer

  4. Department of Biochemistry, Osmaniye State Hospital, Osmaniye, Turkey

    M. Çelik

  5. Silahli Kuvvetler Caddesi, Gullu Bahce Mahallesi, Buket Apt. Kat: 1, No: 1, Antakya-Hatay, Turkey

    N. Duran

Authors
  1. N. Duran
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. A. Koc
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. H. Oksuz
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. C. Tamer
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Y. Akaydin
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. T. Kozlu
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. M. Çelik
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to N. Duran.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Duran, N., Koc, A., Oksuz, H. et al. The protective role of topical propolis on experimental keratitis via nitric oxide levels in rabbits. Mol Cell Biochem 281, 153–161 (2006). https://doi.org/10.1007/s11010-006-0720-4

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11010-006-0720-4

Keywords

Search

Navigation