The Impact of Hyperbaric Oxygen Therapy on Serum C-Reactive Protein Levels, Osteoprotegerin Expression, and Osteoclast Numbers in Induced-Periodontitis Diabetic Rats

Abstract

Objectives This study aimed to examine the impact of hyperbaric oxygen therapy (HBOT) on serum C-reactive protein (CRP) levels, osteoclast numbers, and osteoprotegerin (OPG) expression in periodontitis-induced diabetic rats

Materials and Methods This study constituted an in vivo laboratory-based experiment incorporating a posttest only control group design. Thirty male Wistar rats were divided into three groups of research subjects: a healthy group (K0), periodontitis-induced diabetic group (K1), and periodontitis-induced diabetic group treated with HBOT for 7 days (K2). After treatment, the subjects were sacrificed to determine the level of serum CRP by the ELISA method. Immunohistochemical analysis was conducted to check the level of OPG expression, while a histological analysis was undertaken to quantify the number of osteoclasts.

Statistical Analysis The data was analyzed using a one-way ANOVA and Least Significant Difference (LSD) test on which a result of p < 0.05 was considered statistically significant.

Results HBOT appreciably decreased serum CRP levels, significantly enhancing OPG expression in periodontitis-induced diabetic (p < 0.05) and decreasing the number of osteoclasts in -periodontitis-induced diabetic (p > 0.05).

Conclusion HBOT reduced the serum CRP level, increased OPG expression, and decreased osteoclast numbers in periodontitis-induced diabetic rats.

Keywords

C-reactive protein - osteoprotegerin - osteoclast - diabetes mellitus - periodontitis

Publikationsverlauf

Artikel online veröffentlicht:
24. Mai 2020

• References

• 1 Fitzsimmons TR, Sanders AE, Slade GD, Bartold PM. Biomarkers of periodontal inflammation in the Australian adult population. Aust Dent J 2009; 54 (02) 115-122
• 2 Bansal T, Pandey A, D. D, Asthana AK. Asthana. AK. C-reactive protein (CRP) and its association with periodontal disease: a brief review. J Clin Diagn Res 2014; 8 (07) ZE21-ZE24
• 3 Salvi GE, Carollo-Bittel B, Lang NP. Effects of diabetes mellitus on periodontal and peri-implant conditions: update on associations and risks. J Clin Periodontol 2008; 35 (08) (Suppl) 398-409
• 4 Chávarry NG, Vettore MV, Sansone C, Sheiham A. The relationship between diabetes mellitus and destructive periodontal disease: a meta-analysis. Oral Health Prev Dent 2009; 7 (02) 107-127
• 5 Khader YS, Dauod AS, El-Qaderi SS, Alkafajei A, Batayha WQ. Periodontal status of diabetics compared with nondiabetics: a meta-analysis. J Diabetes Complications 2006; 20 (01) 59-68
• 6 Demmer RT, Holtfreter B, Desvarieux M. et al. The influence of type 1 and type 2 diabetes on periodontal disease progression: prospective results from the Study of Health in Pomerania (SHIP). Diabetes Care 2012; 35 (10) 2036-2042
• 7 Lalla E, Papapanou PN. Diabetes mellitus and periodontitis: a tale of two common interrelated diseases. Nat Rev Endocrinol 2011; 7 (12) 738-748
• 8 Taylor GW, Borgnakke WS. Periodontal disease: associations with diabetes, glycemic control and complications. Oral Dis 2008; 14 (03) 191-203
• 9 Mealey BL, Ocampo GL. Diabetes mellitus and periodontal disease. Periodontol 2000 2007; 44: 127-153
• 10 Gomes-Filho IS, Freitas Coelho JM, da Cruz SS. et al. Chronic periodontitis and C-reactive protein levels. J Periodontol 2011; 82 (07) 969-978
• 11 Silva JA, Lopes Ferrucci D, Peroni LA. et al. Periodontal disease-associated compensatory expression of osteoprotegerin is lost in type 1 diabetes mellitus and correlates with alveolar bone destruction by regulating osteoclastogenesis. Cells Tissues Organs 2012; 196 (02) 137-150
• 12 Collin-Osdoby P, Rothe L, Anderson F, Nelson M, Maloney W, Osdoby P. Receptor activator of NF-kappa B and osteoprotegerin expression by human microvascular endothelial cells, regulation by inflammatory cytokines, and role in human osteoclastogenesis. J Biol Chem 2001; 276 (23) 20659-20672
• 13 Crotti T, Smith MD, Hirsch R. et al. Receptor activator NF kappaB ligand (RANKL) and osteoprotegerin (OPG) protein expression in periodontitis. J Periodontal Res 2003; 38 (04) 380-387
• 14 Santos VR, Lima JA, Gonçalves TE. et al. Receptor activator of nuclear factor-kappa B ligand/osteoprotegerin ratio in sites of chronic periodontitis of subjects with poorly and well-controlled type 2 diabetes. J Periodontol 2010; 81 (10) 1455-1465
• 15 Ribeiro FV, de Mendonça AC, Santos VR, Bastos MF, Figueiredo LC, Duarte PM. Cytokines and bone-related factors in systemically healthy patients with chronic periodontitis and patients with type 2 diabetes and chronic periodontitis. J Periodontol 2011; 82 (08) 1187-1196
• 16 Al-Ghurabi BH, Mohsen SM. Salivary level of RANKL and OPG in chronic periodontitis. J Bagh College Dentistry 2015; 27 (01) 189-194
• 17 Chen TL, Lin SL, Liu GQ. et al. [Effects and holding time of hyperbaric oxygen on human severe periodontitis]. Shanghai Kou Qiang Yi Xue 2003; 12 (06) 403-405
• 18 Rabkin JM, Hunt TK. Local heat increases blood flow and oxygen tension in wounds. Arch Surg 1987; 122 (02) 221-225
• 19 King AJS. The use of animal models in diabetes research. Br J Pharmacol 2012; 166 (03) 877-894
• 20 Guvva S, Patil MB, Mehta DS. Review Article. Rat as laboratory animal model in periodontology. International Journal of Oral Health Sciences 2017; 7 (02) 68-75
• 21 Straka M. Oral manifestations of diabetes mellitus and influences of periodontological treatment on diabetes mellitus. Bratisl Lek Listy 2011; 112 (07) 416-420
• 22 Al H Hadi, Smerdon GR, Fox SW. Hyperbaric oxygen therapy accelerates osteoblast differentiation and promotes bone formation. J Dent 2015; 43 (03) 382-388
• 23 Wu YY, Xiao E, Graves DT. Diabetes mellitus related bone metabolism and periodontal disease. Int J Oral Sci 2015; 7 (02) 63-72
• 24 Joseph R, Narayan V, Krishnan R, Melemadathil S. Non-surgical periodontal therapy improves serum levels of C-reactive protein and edematous states in female patients with idiopathic edema. J Periodontol 2011; 82 (02) 201-209
• 25 Taylor JJ, Preshaw PM, Lalla E. A review of the evidence for pathogenic mechanisms that may link periodontitis and diabetes. J Clin Periodontol 2013; 40 (Suppl 14) S113-S134
• 26 Cochran DL. Inflammation and bone loss in periodontal disease. J Periodontol 2008; 79 (08) (Suppl) 1569-1576
• 27 Ioannidou E, Malekzadeh T, Dongari-Bagtzoglou A. Effect of periodontal treatment on serum C-reactive protein levels: a systematic review and meta-analysis. J Periodontol 2006; 77 (10) 1635-1642
• 28 Nogueira-Filho GR, Rosa BT, David-Neto JR. Effects of hyperbaric oxygen therapy on the treatment of severe cases of periodontitis. Undersea Hyperb Med 2010; 37 (02) 107-114
• 29 Chen T, Zhou Y, Liu J, Xu B, Wu Z, Li D. Biological effects of hyperbaric oxygen on human severe periodontitis. Undersea Hyperb Med 2002; 29 (03) 159-166
• 30 Zhang L, Ding Y, Rao GZ, Miao D. Effects of IL-10 and glucose on expression of OPG and RANKL in human periodontal ligament fibroblasts. Braz J Med Biol Res 2016; 49 (04) e4324
• 31 Reinhard H, Lajer M, Gall MA. et al. Osteoprotegerin and mortality in type 2 diabetic patients. Diabetes Care 2010; 33 (12) 2561-2566
• 32 Theoleyre S, Wittrant Y, Tat SK, Fortun Y, Redini F, Heymann D. The molecular triad OPG/RANK/RANKL: involvement in the orchestration of pathophysiological bone remodeling. Cytokine Growth Factor Rev 2004; 15 (06) 457-475
• 33 Liu C, Walter TS, Huang P. et al. Structural and functional insights of RANKL-RANK interaction and signaling. J Immunol 2010; 184 (12) 6910-6919
• 34 Vezzani G, Quartesan S, Cancellara P. et al. Hyperbaric oxygen therapy modulates serum OPG/RANKL in femoral head necrosis patients. J Enzyme Inhib Med Chem 2017; 32 (01) 707-711
• 35 Pacios S, Kang J, Galicia J. et al. Diabetes aggravates periodontitis by limiting repair through enhanced inflammation. FASEB J 2012; 26 (04) 1423-1430
• 36 Lappin DF, Eapen B, Robertson D, Young J, Hodge PJ. Markers of bone destruction and formation and periodontitis in type 1 diabetes mellitus. J Clin Periodontol 2009; 36 (08) 634-641
• 37 Mogi M, Otogoto J, Ota N, Togari A. Differential expression of RANKL and osteoprotegerin in gingival crevicular fluid of patients with periodontitis. J Dent Res 2004; 83 (02) 166-169
• 38 Musurlieva NM, Bratoycheva MS. Diabetes - A systemic risk factor for the development of chronic periodontitis in Bulgarian patients. Int J Diabetes Clin Res 2015; 2: 2