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The effects of morus nigra on the alveolar bone loss in experimentally-induced periodontitis

Year 2019, Volume: 53 Issue: 3, 99 - 105, 01.10.2019

Abstract

Purpose The aim of this study is to evalute the anti-inflammatory effects of morus migra on experimentally-induced periodontitis in rats. Materials and Methods Twenty-four Wistar-albino rats were randomly divided into three groups: control group (C, n=8), experimental periodontitis (PER, n=8), experimental periodontitis and treated with Morus nigra (MN+PER, n=8) (50 mg/kg per day for 21 days). After 21 days, the rats were sacrificed, and alveolar bones were evaluated histopathologically and histometrically analyzed to obtain level of alveolar bone loss. The detection of RANKL and OPG were immunohistochemically performed. Serum and tissue levels of MMP-8 and MMP-13 were also analyzed. Results Morus nigra treatment decreased tissue MMP-8 and MMP-13 levels and there were significant differences in the case of tissue levels of MMP-8 and MMP-13 between groups PER and MN+PER (p=0.035, p=0.041). There were no significant differences among all the groups serum levels of MMP-8 and MMP-13 (p=0.067, p=0.082). In the histometric evaluation, alveolar bone loss was greater in the PER group compared to C and MN groups (p=0.035). Immuno-histochemical staining of RANKL activities were found significantly lower (p=0.037) and OPG activities were found significantly higher in MN+PER group when compared to PER group (p=0.021). Conclusion The present study reveals that systemic administration of Morus nigra significantly inhibited the regional alveolar bone resorption and contributes to periodontal healing in the rat experimental-periodontitis models.

Supporting Institution

This work was funded by the Firat University Scientific Research Project Coordinatorship (DHF.15.02) Elazığ, Turkey.

Project Number

DHF.15.02

References

  • 1. Saglam M, Koseoglu S, Hatipoglu M, Esen HH, Koksal E. Effect of sumac extract on serum oxidative status, RANKL/OPG system and alveolar bone loss in experimental periodontitis in rats. J Appl Oral Sci 2015;23(1):33-41.
  • 2. Papageorgiou SN, Hagner M, Nogueira AV, Franke A, Jager A, Deschner J. Inflammatory bowel disease and oral health: systematic review and a meta-analysis. J Clin Periodontol 2017.
  • 3. Bostanci V, Toker H, Senel S, Ozdemir H, Aydin H. Effect of chronic periodontitis on serum and gingival crevicular fluid oxidant and antioxidant status in patients with familial Mediterranean fever before and after periodontal treatment. J Periodontol 2014;85(5):706-712.
  • 4. Arabaci T, Kermen E, Ozkanlar S, Kose O, Kara A, Kizildag A, Duman SB, Ibisoglu E. Therapeutic effects of melatonin on alveolar bone resorption after experimental periodontitis in rats: a biochemical and immunohistochemical study. J Periodontol 2015;86(7):874-881.
  • 5. Ozcan E, Isil Saygun N, Serdar MA, Umut Bengi V, Kantarci A. Non-Surgical Periodontal Therapy Reduces Saliva Adipokine and Matrix Metalloproteinase Levels in Periodontitis. J Periodontol 2016;87(8):934-943.
  • 6. Yang D, Wang J, Ni J, Shang S, Liu L, Xiang J, Li C. Temporal expression of metalloproteinase-8 and -13 and their relationships with extracellular matrix metalloproteinase inducer in the development of ligature-induced periodontitis in rats. J Periodontal Res 2013;48(4):411-419.
  • 7. Bassil J, Senni K, Changotade S, Baroukh B, Kassis C, Naaman N, Godeau G. Expression of MMP-2, 9 and 13 in newly formed bone after sinus augmentation using inorganic bovine bone in human. J Periodontal Res 2011;46(6):756-762.
  • 8. Karakan NC, Akpinar A, Goze F, Poyraz O. Investigating the effects of systemically administired strontium ranelate on alveolar bone loss histomorphometrically and histopathologically on experimental periodontitis in Rats. J Periodontol 2016;88(2):1-17.
  • 9. Silva N, Dutzan N, Hernandez M, Dezerega A, Rivera O, Aguillon JC, Aravena O, Lastres P, Pozo P, Vernal R, Gamonal J. Characterization of progressive periodontal lesions in chronic periodontitis patients: levels of chemokines, cytokines, matrix metalloproteinase-13, periodontal pathogens and inflammatory cells. J Clin Periodontol 2008;35(3):206-214.
  • 10. Padilha MM, Vilela FC, Rocha CQ, Dias MJ, Soncini R, dos Santos MH, Alves-da-Silva G, Giusti-Paiva A. Antiinflammatory properties of Morus nigra leaves. Phytother Res 2010;24(10):1496-1500.
  • 11. Naderi GA, Asgary S, Sarraf-Zadegan N, Oroojy H, Afshin-Nia F. Antioxidant activity of three extracts of Morus nigra. Phytother Res 2004;18(5):365-369.
  • 12. Volpato GT, Calderon IM, Sinzato S, Campos KE, Rudge MV, Damasceno DC. Effect of Morus nigra aqueous extract treatment on the maternal-fetal outcome, oxidative stress status and lipid profile of streptozotocin-induced diabetic rats. J Ethnopharmacol 2011;138(3):691-696.
  • 13. Ozan F, Tepe B, Polat ZA, Er K. Evaluation of in vitro effect of Morus rubra (red mulberry) on survival of periodontal ligament cells. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2008;105(2):e66-69.
  • 14. Aral CA, Kesim S, Greenwell H, Kara M, Cetin A, Yakan B. Alveolar bone protective and hypoglycemic effects of systemic propolis treatment in experimental periodontitis and diabetes mellitus. J Med Food 2015;18(2):195-201.
  • 15. Akman S, Canakci V, Kara A, Tozoglu U, Arabaci T, Dagsuyu IM. Therapeutic effects of alpha lipoic acid and vitamin C on alveolar bone resorption after experimental periodontitis in rats: a biochemical, histochemical, and stereologic study. J Periodontol 2013;84(5):666-674.
  • 16. Cuzzocrea S, Zingarelli B, Hake P, Salzman AL, Szabo C. Antiinflammatory effects of mercaptoethylguanidine, a combined inhibitor of nitric oxide synthase and peroxynitrite scavenger, in carrageenan-induced models of inflammation. Free Radic Biol Med. 1998;24(3):450-459.
  • 17. Lucinda LM, de Oliveira TT, Salvador PA, Peters VM, Reis JE, Guerra Mde O. Radiographic evidence of mandibular osteoporosis improvement in Wistar rats treated with Ginkgo biloba. Phytother Res 2010;24(2):264-267.
  • 18. Remmele W, Stegner HE. [Recommendation for uniform definition of an immunoreactive score (IRS) for immunohistochemical estrogen receptor detection (ER-ICA) in breast cancer tissue]. Pathologe 1987;8(3):138-140.
  • 19. Zelova H, Hanakova Z, Cermakova Z, Smejkal K, Dall Acqua S, Babula P, Cvacka J, Hosek J. Evaluation of anti-inflammatory activity of prenylated substances isolated from Morus alba and Morus nigra. J Nat Prod 2014;77(6):1297-1303.
  • 20. Balli U, Cetinkaya BO, Keles GC, Keles ZP, Guler S, Sogut MU, Erisgin Z. Assessment of MMP-1, MMP-8 and TIMP-2 in experimental periodontitis treated with kaempferol. J Periodontal Implant Sci 2016;46(2):84-95.
  • 21. Mukherjee PK, Saha K, Das J, Pal M, Saha BP. Studies on the anti-inflammatory activity of rhizomes of Nelumbo nucifera. Planta Med 1997;63(4):367-369.
  • 22. Gupta MB, Nath R, Srivastava N, Shanker K, Kishor K, Bhargava KP. Anti-inflammatory and antipyretic activities of beta-sitosterol. Planta Med 1980;39(2):157-163.
  • 23. de Queiroz GT, Santos TR, Macedo R, Peters VM, Leite MN, de Cassia da Silveira e Sa R, de Oliveira Guerra M. Efficacy of Morus nigra L. on reproduction in female Wistar rats. Food Chem Toxicol 2012;50(3-4):816-822.
  • 24. Bastos MF, Tucci MA, de Siqueira A, de Faveri M, Figueiredo LC, Vallim PC, Duarte PM. Diabetes may affect the expression of matrix metalloproteinases and their inhibitors more than smoking in chronic periodontitis. J Periodontal Res 2016.
  • 25. Johnson N, Ebersole JL, Kryscio RJ, Danaher RJ, Dawson D, 3rd, Al-Sabbagh M, Miller CS. Rapid assessment of salivary MMP-8 and periodontal disease using lateral flow immunoassay. Oral Dis 2016;22(7):681-687.
  • 26. de Aquino SG, Guimaraes MR, Stach-Machado DR, da Silva JA, Spolidorio LC, Rossa C, Jr. Differential regulation of MMP-13 expression in two models of experimentally induced periodontal disease in rats. Arch Oral Biol 2009;54(7):609-617.
  • 27. Gorska R, Gregorek H, Kowalski J, Laskus-Perendyk A, Syczewska M, Madalinski K. Relationship between clinical parameters and cytokine profiles in inflamed gingival tissue and serum samples from patients with chronic periodontitis. J Clin Periodontol 2003;30(12):1046-1052.
  • 28. Dong Y, Huihui Z, Li C. Piperine inhibit inflammation, alveolar bone loss and collagen fibers breakdown in a rat periodontitis model. J Periodontal Res 2015;50(6):758-765.
  • 29. Behfarnia P, Saied-Moallemi Z, Javanmard SH, Naseri R. Serum, saliva, and GCF concentration of RANKL and osteoprotegerin in smokers versus nonsmokers with chronic periodontitis. Adv Biomed Res 2016;5:80.
  • 30. Garlet GP, Martins W, Jr., Fonseca BA, Ferreira BR, Silva JS. Matrix metalloproteinases, their physiological inhibitors and osteoclast factors are differentially regulated by the cytokine profile in human periodontal disease. J Clin Periodontol 2004;31(8):671-679.
Year 2019, Volume: 53 Issue: 3, 99 - 105, 01.10.2019

Abstract

Project Number

DHF.15.02

References

  • 1. Saglam M, Koseoglu S, Hatipoglu M, Esen HH, Koksal E. Effect of sumac extract on serum oxidative status, RANKL/OPG system and alveolar bone loss in experimental periodontitis in rats. J Appl Oral Sci 2015;23(1):33-41.
  • 2. Papageorgiou SN, Hagner M, Nogueira AV, Franke A, Jager A, Deschner J. Inflammatory bowel disease and oral health: systematic review and a meta-analysis. J Clin Periodontol 2017.
  • 3. Bostanci V, Toker H, Senel S, Ozdemir H, Aydin H. Effect of chronic periodontitis on serum and gingival crevicular fluid oxidant and antioxidant status in patients with familial Mediterranean fever before and after periodontal treatment. J Periodontol 2014;85(5):706-712.
  • 4. Arabaci T, Kermen E, Ozkanlar S, Kose O, Kara A, Kizildag A, Duman SB, Ibisoglu E. Therapeutic effects of melatonin on alveolar bone resorption after experimental periodontitis in rats: a biochemical and immunohistochemical study. J Periodontol 2015;86(7):874-881.
  • 5. Ozcan E, Isil Saygun N, Serdar MA, Umut Bengi V, Kantarci A. Non-Surgical Periodontal Therapy Reduces Saliva Adipokine and Matrix Metalloproteinase Levels in Periodontitis. J Periodontol 2016;87(8):934-943.
  • 6. Yang D, Wang J, Ni J, Shang S, Liu L, Xiang J, Li C. Temporal expression of metalloproteinase-8 and -13 and their relationships with extracellular matrix metalloproteinase inducer in the development of ligature-induced periodontitis in rats. J Periodontal Res 2013;48(4):411-419.
  • 7. Bassil J, Senni K, Changotade S, Baroukh B, Kassis C, Naaman N, Godeau G. Expression of MMP-2, 9 and 13 in newly formed bone after sinus augmentation using inorganic bovine bone in human. J Periodontal Res 2011;46(6):756-762.
  • 8. Karakan NC, Akpinar A, Goze F, Poyraz O. Investigating the effects of systemically administired strontium ranelate on alveolar bone loss histomorphometrically and histopathologically on experimental periodontitis in Rats. J Periodontol 2016;88(2):1-17.
  • 9. Silva N, Dutzan N, Hernandez M, Dezerega A, Rivera O, Aguillon JC, Aravena O, Lastres P, Pozo P, Vernal R, Gamonal J. Characterization of progressive periodontal lesions in chronic periodontitis patients: levels of chemokines, cytokines, matrix metalloproteinase-13, periodontal pathogens and inflammatory cells. J Clin Periodontol 2008;35(3):206-214.
  • 10. Padilha MM, Vilela FC, Rocha CQ, Dias MJ, Soncini R, dos Santos MH, Alves-da-Silva G, Giusti-Paiva A. Antiinflammatory properties of Morus nigra leaves. Phytother Res 2010;24(10):1496-1500.
  • 11. Naderi GA, Asgary S, Sarraf-Zadegan N, Oroojy H, Afshin-Nia F. Antioxidant activity of three extracts of Morus nigra. Phytother Res 2004;18(5):365-369.
  • 12. Volpato GT, Calderon IM, Sinzato S, Campos KE, Rudge MV, Damasceno DC. Effect of Morus nigra aqueous extract treatment on the maternal-fetal outcome, oxidative stress status and lipid profile of streptozotocin-induced diabetic rats. J Ethnopharmacol 2011;138(3):691-696.
  • 13. Ozan F, Tepe B, Polat ZA, Er K. Evaluation of in vitro effect of Morus rubra (red mulberry) on survival of periodontal ligament cells. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2008;105(2):e66-69.
  • 14. Aral CA, Kesim S, Greenwell H, Kara M, Cetin A, Yakan B. Alveolar bone protective and hypoglycemic effects of systemic propolis treatment in experimental periodontitis and diabetes mellitus. J Med Food 2015;18(2):195-201.
  • 15. Akman S, Canakci V, Kara A, Tozoglu U, Arabaci T, Dagsuyu IM. Therapeutic effects of alpha lipoic acid and vitamin C on alveolar bone resorption after experimental periodontitis in rats: a biochemical, histochemical, and stereologic study. J Periodontol 2013;84(5):666-674.
  • 16. Cuzzocrea S, Zingarelli B, Hake P, Salzman AL, Szabo C. Antiinflammatory effects of mercaptoethylguanidine, a combined inhibitor of nitric oxide synthase and peroxynitrite scavenger, in carrageenan-induced models of inflammation. Free Radic Biol Med. 1998;24(3):450-459.
  • 17. Lucinda LM, de Oliveira TT, Salvador PA, Peters VM, Reis JE, Guerra Mde O. Radiographic evidence of mandibular osteoporosis improvement in Wistar rats treated with Ginkgo biloba. Phytother Res 2010;24(2):264-267.
  • 18. Remmele W, Stegner HE. [Recommendation for uniform definition of an immunoreactive score (IRS) for immunohistochemical estrogen receptor detection (ER-ICA) in breast cancer tissue]. Pathologe 1987;8(3):138-140.
  • 19. Zelova H, Hanakova Z, Cermakova Z, Smejkal K, Dall Acqua S, Babula P, Cvacka J, Hosek J. Evaluation of anti-inflammatory activity of prenylated substances isolated from Morus alba and Morus nigra. J Nat Prod 2014;77(6):1297-1303.
  • 20. Balli U, Cetinkaya BO, Keles GC, Keles ZP, Guler S, Sogut MU, Erisgin Z. Assessment of MMP-1, MMP-8 and TIMP-2 in experimental periodontitis treated with kaempferol. J Periodontal Implant Sci 2016;46(2):84-95.
  • 21. Mukherjee PK, Saha K, Das J, Pal M, Saha BP. Studies on the anti-inflammatory activity of rhizomes of Nelumbo nucifera. Planta Med 1997;63(4):367-369.
  • 22. Gupta MB, Nath R, Srivastava N, Shanker K, Kishor K, Bhargava KP. Anti-inflammatory and antipyretic activities of beta-sitosterol. Planta Med 1980;39(2):157-163.
  • 23. de Queiroz GT, Santos TR, Macedo R, Peters VM, Leite MN, de Cassia da Silveira e Sa R, de Oliveira Guerra M. Efficacy of Morus nigra L. on reproduction in female Wistar rats. Food Chem Toxicol 2012;50(3-4):816-822.
  • 24. Bastos MF, Tucci MA, de Siqueira A, de Faveri M, Figueiredo LC, Vallim PC, Duarte PM. Diabetes may affect the expression of matrix metalloproteinases and their inhibitors more than smoking in chronic periodontitis. J Periodontal Res 2016.
  • 25. Johnson N, Ebersole JL, Kryscio RJ, Danaher RJ, Dawson D, 3rd, Al-Sabbagh M, Miller CS. Rapid assessment of salivary MMP-8 and periodontal disease using lateral flow immunoassay. Oral Dis 2016;22(7):681-687.
  • 26. de Aquino SG, Guimaraes MR, Stach-Machado DR, da Silva JA, Spolidorio LC, Rossa C, Jr. Differential regulation of MMP-13 expression in two models of experimentally induced periodontal disease in rats. Arch Oral Biol 2009;54(7):609-617.
  • 27. Gorska R, Gregorek H, Kowalski J, Laskus-Perendyk A, Syczewska M, Madalinski K. Relationship between clinical parameters and cytokine profiles in inflamed gingival tissue and serum samples from patients with chronic periodontitis. J Clin Periodontol 2003;30(12):1046-1052.
  • 28. Dong Y, Huihui Z, Li C. Piperine inhibit inflammation, alveolar bone loss and collagen fibers breakdown in a rat periodontitis model. J Periodontal Res 2015;50(6):758-765.
  • 29. Behfarnia P, Saied-Moallemi Z, Javanmard SH, Naseri R. Serum, saliva, and GCF concentration of RANKL and osteoprotegerin in smokers versus nonsmokers with chronic periodontitis. Adv Biomed Res 2016;5:80.
  • 30. Garlet GP, Martins W, Jr., Fonseca BA, Ferreira BR, Silva JS. Matrix metalloproteinases, their physiological inhibitors and osteoclast factors are differentially regulated by the cytokine profile in human periodontal disease. J Clin Periodontol 2004;31(8):671-679.
There are 30 citations in total.

Details

Primary Language English
Subjects Dentistry
Journal Section Original Research Articles
Authors

Tuba Talo Yildirim This is me

Gonca Ozan This is me

Alihan Bozoglan This is me

Tahir Karaman This is me

Neval Dildes This is me

Can Ayhan Kaya This is me

Nalan Kaya This is me

Elif Erdem This is me

Project Number DHF.15.02
Publication Date October 1, 2019
Submission Date August 31, 2018
Published in Issue Year 2019 Volume: 53 Issue: 3

Cite

EndNote Talo Yildirim T, Ozan G, Bozoglan A, Karaman T, Dildes N, Kaya CA, Kaya N, Erdem E (October 1, 2019) The effects of morus nigra on the alveolar bone loss in experimentally-induced periodontitis. European Oral Research 53 3 99–105.