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DOI :10.26650/eor.20241248958   IUP :10.26650/eor.20241248958    Full Text (PDF)

Prophylactic and therapeutic effects of (6)–shogaol on alveolar bone loss in experimental periodontitis

Didem Bezirci, Meltem Karşıyaka Hendek, Gönen Özcan, Oğuz Kul, Tuğçe Anteplioğlu, Ebru Olgun

Purpose: (6)-Shogaol is the most prevalent bioactive compound in ginger. The aim of this study was to examine both the prophylactic and therapeutic effects of (6)-shogaol in an experimental periodontitis model.

Materials and Methods: Thirty-five male Wistar albino rats were divided into four groups. In the healthy group (n=5), no intervention was undertaken. In the periodontitis group (n=10), periodontitis was induced by ligature placement for 14 days. In the prophylaxis group (n=10), periodontitis was induced with ligature placement for 14 days, and during this time, 20 mg/kg/day of (6)-shogaol was administered via oral gavage. In the therapeutic group (n=10), periodontitis was induced with ligature placement for 14 days, and following the removal of the ligature, 20 mg/kg/day of (6)-shogaol was administered via oral gavage for 14 days. Alveolar bone loss was histometrically measured, and malondialdehyde (MDA), superoxide dismutase (SOD), glutathione peroxidase (GP), nuclear factor kappa B (NF-κB), receptor activator of nuclear factor kappa B ligand (RANKL), and osteoprotegerin (OPG) were immunohistochemically analyzed.

Results: Alveolar bone loss was significantly lower in the healthy group than in the remaining groups, as well as in the therapeutic group than in the periodontitis group (p<0.001). RANKL/OPG was significantly higher in the periodontitis group compared to the remaining groups and in the prophylaxis group compared to the therapeutic group (p<0.001). MDA was significantly lower in the healthy group than in the remaining groups (p<0.001). SOD was significantly lower in the periodontitis group than in the prophylaxis and therapeutic groups (p=0.039 and p=0.042, respectively). GP was significantly lower in the healthy group than in the prophylaxis and therapeutic groups (p=0.031 and p=0.002, respectively).

Conclusion: The administration of (6)-shogaol modulated the RANKL/OPG balance and antioxidant status in rats with ligature-induced periodontitis.

Keywords: Experimental periodontitis, ginger, oxidative stress, RANKL/OPG, shogaol

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References

  • 1. Kinane DF, Stathopoulou PG, Papapanou PN. Periodontal diseases. Nat Rev Dis Primers 2017;3:17038. google scholar
  • 2. Belibasakis GN, Bostanci N. The RANKL-OPG system in clinical periodontology. J Clin Periodontol 2012;39:239-48. google scholar
  • 3. Chapple IL, Matthews JB. The role of reactive oxygen and antioxidant species in periodontal tissue destruction. Periodontol 2000 2007;43:160-232. google scholar
  • 4. Kubra IR, Rao LJ. An impression on current developments in the technology, chemistry, and biological activities of ginger (Zingiber officinale Roscoe). Crit Rev Food Sci Nutr 2012;52;651-88. google scholar
  • 5. Kou X, Wang X, Ji R, Liu L, Qiao Y, Lou Z, et al. Occurrence, biological activity and metabolism of (6) shogaol. Food Funct 2018;9:1310-27. google scholar
  • 6. Butt MS, Sultan MT. Ginger and its health claims: molecular aspects. Crit Rev Food Sci Nutr 2011;51:383-93. google scholar
  • 7. Dugasani S, Pichika MR, Nadarajah VD, Balijepalli MK, Tandra S, Korlakunta JN. Comparative antioxidant and anti-inflammatory effects of [6]-gingerol, [8]-gingerol, [10] gingerol and [6]-shogaol. J Ethnopharmacol 2010;127:515-20. google scholar
  • 8. Park G, Kim HG, Ju MS, Ha SK, Park Y, Kim SY, et al. (6)-Shogaol, an active compound of ginger, protects dopaminergic neurons in Parkinson's disease models via anti-neuroinflammation. Acta Pharmacol Sin 2013;34:1131-9. google scholar
  • 9. Na JY, Song K, Lee JW, Kim S, Kwon J. 6-Shogaol has anti-amyloidogenic activity and ameliorates Alzheimer's disease via CysLT1R-mediated inhibition of cathepsin B. Biochem Biophys Res Commun 2016;477:96-102. google scholar
  • 10. Na JY, Song K, Lee JW, Kim S, Kwon J. Pretreatment of 6-shogaol attenuates oxidative stress and inflammation in middle cerebral artery occlusion-induced mice. Eur J Pharmacol 2016;788:241-7. google scholar
  • This article has been accepted for publication and undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record google scholar
  • 11. Park G, Oh DS, Lee MG, Lee CE, Kim YU. 6-Shogaol, an active compound of ginger, alleviates allergic dermatitis-like skin lesions via cytokine inhibition by activating the Nrf2 pathway. Toxicol Appl Pharmacol 2016;310:51-9. google scholar
  • 12. Annamalai G, Suresh K. (6)-Shogaol attenuates inflammation, cell proliferation via modulate NF-kappaB and AP-1 oncogenic signaling in 7,12-dimethylbenz[a]anthracene induced oral carcinogenesis. Biomed Pharmacother 2018;98:484-90. google scholar
  • 13. Yi JK, Ryoo ZY, Ha JJ, Oh DY, Kim MO, Kim SH. Beneficial effects of 6-shogaol on hyperglycemia, islet morphology and apoptosis in some tissues of streptozotocin-induced diabetic mice. Diabetol Metab Syndr 2019;11:15. google scholar
  • 14. Kilkenny C, Browne W, Cuthill IC, Emerson M, Altman DG. NC3Rs Reporting Guidelines Working Group. Animal research: reporting in vivo experiments: the ARRIVE guidelines. Br J Pharmacol 2010;160:1577-9. google scholar
  • 15. Rahmani AH, Shabrmi FMA, Aly SM. Active ingredients of ginger as potential candidates in the prevention and treatment of diseases via modulation of biological activities. IJPPP 2014;6:125-36. google scholar
  • 16. Wu H, Hsieh MC, Lo CY, Liu CB, Sang S, Ho CT, et al. 6-Shogaol is more effective than 6-gingerol and curcumin in inhibiting 12- Otetradecanoylphorbol 13-acetate induced tumor promotion in mice. Mol Nutr Food Res 2010;54: 1296-306. google scholar
  • 17. Pan MH, Hsieh MC, Hsu PC, Ho SY, Lai CS, Wu H, et al. 6-shogaol suppressed lipopolysaccharide-induced up-expression of iNOS and COX-2 in murine macrophages. Mol Nutr Food Res 2008;52:1467-77. google scholar
  • 18. Ahn SI, Lee JK, Youn HS. Inhibition of homodimerization of toll-like receptor 4 by 6-shogaol. Mol Cells 2009;27:211-5. google scholar
  • 19. Sohn Y, Han NY, Lee MJ, Cho HJ, Jung HS. [6]-shogaol inhibits the production of proinflammatory cytokines via regulation of NF-kB and phosphorylation of JNK in HMC-1 cells. Immunopharmacol Immunotoxicol 2013;35:462-70. google scholar
  • This article has been accepted for publication and undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record google scholar
  • 20. Villalvilla A, DaSilva JA, Largo R, Gualillo O, Vieira PC, Herrero-Beaumont G, et al. 6-shogaol inhibits chondrocytes’ innate immune responses and cathepsin-K activity. Mol Nutr Food Res 2014;58:256-66. google scholar
  • 21. Levy AS, Simon OR. Six-shogaol inhibits production of tumour necrosis factor alpha, interleukin-1 beta and nitric oxide from lipopolysaccharide-stimulated RAW 264.7 macrophages. West Indian Med J 2009;58:295-300. google scholar
  • 22. Kuhr A, Popa-wagner A, Schmoll H, Schwahn C, Kocher T. Observations on experimental marginal periodontitis in rats. J Periodontal Res 2004;39:101-6. google scholar
  • 23. Kantarcı A, Hasturk H, Van Dyke TE. Animal models for periodontal regeneration and peri-implant responses. Periodontol 2000 2015;68;66-82. google scholar
  • 24. Schwarz JM, Nugent BM, Mccarthy MM. Developmental and hormone-induced epigenetic changes to estrogen and progesterone receptor genes in brain are dynamic across the life span. Endocrinology 2010;151:4871-81. google scholar
  • 25. Cochran DL. Inflammation and bone loss in periodontal disease. J Periodontol 2008;79:1569-76. google scholar
  • 26. Barbato L, Francioni E, Bianchi M, Mascitelli E, Marco LB, Tonelli DP. Periodontitis and bone metabolism. Clin Cases Miner Bone Metab 2015;12:174-7. google scholar
  • 27. Bartold PM, Cantley MD, Haynes DR. Mechanisms and control of pathologic bone loss in periodontitis. Periodontol 2000 2010;53:55-69. google scholar
  • 28. Kim YG, Kim MO, Kim SH, Kim HJ, Pokhrel NK, Lee JH, et al. 6-Shogaol, an active ingredient of ginger, inhibits osteoclastogenesis and alveolar bone resorption in ligature-induced periodontitis in mice. J Periodontol 2020;91:809-18. google scholar
  • 29. Yeh IJ, Chen SC, Yen MC, Wu YH, Hung CH, Kuo PL. 6-Shogaol Suppresses 2-Amino-1-Methyl-6-Phenylimidazo [4,5-b] Pyridine (PhIP)-Induced Human 786-O Renal Cell Carcinoma Osteoclastogenic Activity and Metastatic Potential. Nutrients 2019;11:2306. google scholar
  • 30. Dahiya P, Kamal R, Gupta R, Bhardwaj R, Chaudhary K, Kaur S. Reactive oxygen species in periodontitis. J Indian Soc Periodontol 2013;17:411-6. google scholar
  • 31. Chapple IL. Oxidative stress, nutrition and neutrogenomics in periodontal health and disease. Int J Dent Hyg 2006;4:15-21. google scholar
  • 32. Lee NK, Choi YG, Baik JY, Han SY, Jeong DW, Bae YS, et al. A crucial role for reactive oxygen species in RANKL-induced osteoclast differentiation. Blood 2005;106:852-9. google scholar
  • 33. Tsikas D. Assessment of lipid peroxidation by measuring malondialdehyde (MDA) and relatives in biological samples: Analytical and biological challenges. Anal Biochem 2017;524:13-30. google scholar
  • 34. Halliwell B. Reactive species and antioxidants. Redox biology is a fundamental theme of aerobic life. Plant Physiol 2006;141:312-22. google scholar
  • 35. Kim JK, Jang HD. 6-shogaol attenuates H2O2-induced oxidative stress via upregulation of Nrf2-mediated Y-glutamylcysteine synthetase and heme oxygenase expression in HepG2 cells. Food Sci Biotechnol 2016;25:319-27. google scholar
  • 36. Wang YK, Hong YJ, Yao YH, Huang XM, Liu XB, Zhang CY, et al. 6-Shogaol protects against oxidized LDL-induced endothelial injuries by inhibiting oxidized LDL-evoked LOX-1 signaling. Evid Based Complement Alternat Med 2013;2013:503521. google scholar
  • 37. Qi HY, Han B. Protective effect of 6-shogaol against endotoxin-induced periodontitis in rats. Acta Poloniae Pharmaceutica 2018;75:1391-8. google scholar
  • 38. Nonaka K, Bando M, Sakamoto E, Inagaki Y, Naruishi K, Yumoto H, et al. 6-Shogaol Inhibits Advanced Glycation End-Products-Induced IL-6 and ICAM-1 Expression by Regulating Oxidative Responses in Human Gingival Fibroblasts. Molecules 2019;24: 3705. google scholar
  • 39. Han SJ, Kim M, D'Agati VD, Lee HT. 6-Shogaol protects against ischemic acute kidney injury by modulating NF-kB and heme oxygenase-1 pathways. Am J Physiol Renal Physiol 2019;317:743-56. google scholar

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APA

Bezirci, D., Karşıyaka Hendek, M., Özcan, G., Kul, O., Anteplioğlu, T., & Olgun, E. (2023). Prophylactic and therapeutic effects of (6)–shogaol on alveolar bone loss in experimental periodontitis. European Oral Research, 58(1), 37-43. https://doi.org/10.26650/eor.20241248958


AMA

Bezirci D, Karşıyaka Hendek M, Özcan G, Kul O, Anteplioğlu T, Olgun E. Prophylactic and therapeutic effects of (6)–shogaol on alveolar bone loss in experimental periodontitis. European Oral Research. 2023;58(1):37-43. https://doi.org/10.26650/eor.20241248958


ABNT

Bezirci, D.; Karşıyaka Hendek, M.; Özcan, G.; Kul, O.; Anteplioğlu, T.; Olgun, E. Prophylactic and therapeutic effects of (6)–shogaol on alveolar bone loss in experimental periodontitis. European Oral Research, [Publisher Location], v. 58, n. 1, p. 37-43, 2023.


Chicago: Author-Date Style

Bezirci, Didem, and Meltem Karşıyaka Hendek and Gönen Özcan and Oğuz Kul and Tuğçe Anteplioğlu and Ebru Olgun. 2023. “Prophylactic and therapeutic effects of (6)–shogaol on alveolar bone loss in experimental periodontitis.” European Oral Research 58, no. 1: 37-43. https://doi.org/10.26650/eor.20241248958


Chicago: Humanities Style

Bezirci, Didem, and Meltem Karşıyaka Hendek and Gönen Özcan and Oğuz Kul and Tuğçe Anteplioğlu and Ebru Olgun. “Prophylactic and therapeutic effects of (6)–shogaol on alveolar bone loss in experimental periodontitis.” European Oral Research 58, no. 1 (Nov. 2024): 37-43. https://doi.org/10.26650/eor.20241248958


Harvard: Australian Style

Bezirci, D & Karşıyaka Hendek, M & Özcan, G & Kul, O & Anteplioğlu, T & Olgun, E 2023, 'Prophylactic and therapeutic effects of (6)–shogaol on alveolar bone loss in experimental periodontitis', European Oral Research, vol. 58, no. 1, pp. 37-43, viewed 22 Nov. 2024, https://doi.org/10.26650/eor.20241248958


Harvard: Author-Date Style

Bezirci, D. and Karşıyaka Hendek, M. and Özcan, G. and Kul, O. and Anteplioğlu, T. and Olgun, E. (2023) ‘Prophylactic and therapeutic effects of (6)–shogaol on alveolar bone loss in experimental periodontitis’, European Oral Research, 58(1), pp. 37-43. https://doi.org/10.26650/eor.20241248958 (22 Nov. 2024).


MLA

Bezirci, Didem, and Meltem Karşıyaka Hendek and Gönen Özcan and Oğuz Kul and Tuğçe Anteplioğlu and Ebru Olgun. “Prophylactic and therapeutic effects of (6)–shogaol on alveolar bone loss in experimental periodontitis.” European Oral Research, vol. 58, no. 1, 2023, pp. 37-43. [Database Container], https://doi.org/10.26650/eor.20241248958


Vancouver

Bezirci D, Karşıyaka Hendek M, Özcan G, Kul O, Anteplioğlu T, Olgun E. Prophylactic and therapeutic effects of (6)–shogaol on alveolar bone loss in experimental periodontitis. European Oral Research [Internet]. 22 Nov. 2024 [cited 22 Nov. 2024];58(1):37-43. Available from: https://doi.org/10.26650/eor.20241248958 doi: 10.26650/eor.20241248958


ISNAD

Bezirci, Didem - Karşıyaka Hendek, Meltem - Özcan, Gönen - Kul, Oğuz - Anteplioğlu, Tuğçe - Olgun, Ebru. “Prophylactic and therapeutic effects of (6)–shogaol on alveolar bone loss in experimental periodontitis”. European Oral Research 58/1 (Nov. 2024): 37-43. https://doi.org/10.26650/eor.20241248958



TIMELINE


Submitted08.02.2023
Accepted09.05.2023
Published Online10.11.2023

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