THE EFFECT OF BISPHOSPHONATES AND LOW-DOSE DOXCYCLINE THERAPY IN DIABETICS WITH PERIODONTITIS: A REVIEW

Şeyma Bozkurt Doğan; Figen Özgöz Dede

doi:10.17567/ataunidfd.290572

THE EFFECT OF BISPHOSPHONATES AND LOW-DOSE DOXCYCLINE THERAPY IN DIABETICS WITH PERIODONTITIS: A REVIEW

Abstract

ABSTRACT

Diabetes mellitus and periodontal disease are chronic diseases affecting a large number of populations worldwide. The major component of soft and hard tissue destruction associated with periodontal disease is the result of activation of the host immuno-inflammatory response to the oral pathogens. Diabetes mellitus alters bacteria–host interactions by prolonging the inflammatory response and dysregu- lating cytokine production, and is among the primary risk factors for periodontal disease. Alveolar bone loss is one of the main outcomes of periodontitis. One of the important long-term complications associated with diabetes mellitus is changed bone metabolism. Recently, the therapeutic strategies for the treatment of periodontal disease have been directed towards to host modulation therapy. In this review, we will evaluate the effects of bisphosphonates and low dose doxcycline drugs as host modulation agents in the treatment of periodontal disease and in diabetics with periodontal disease.

Keywords: Periodontitis, diabetes mellitus, bisphosphonate, doxycycline, alveolar bone loss

DÜŞÜK-DOZ DOKSİSİKLİN VE BİFOSFONAT TEDAVİSİNİN PERİODONTİTİSLİ DİYABET HASTALARINDAKİ ETKİSİ: DERLEME

ÖZ

Diabetes mellitus ve periodontal hastalıklar, dünya popülasyonunun geniş bir kitlesini etkileyen kronik hastalıklardır. Periodontal hastalıklar ile ilişkili sert ve yumuşak doku yıkımı, oral patojenlere karşı konak im- muno-inflamatuvar cevabın aktivasyonu sonucu mey- dana gelmektedir. Diabetes mellitus, sitokin üretiminin düzenlenmesini bozarak ve inflamatuvar cevabı uzatarak bakteri-konak etkileşimini değiştirmektedir ve periodontal hastalıklar için başlıca risk faktörleri ara- sındadır. Periodontitisin temel klinik özelliklerinden biri alveoler kemik kaybıdır. Diabetes mellitus ile ilişkili önemli uzun-süreli komplikasyonlarından biri, kemik metabolizmasındaki değişimdir. Son zamanlarda pe- riodontal hastalığın tedavisi için uygulanan terapötik stratejiler konak modülasyon tedavisine doğru yönel- miştir. Bu derlemede, periodontal hastalıklı diyabet hastalarında ve periodontal hastalığın tedavisinde konak modülasyon ajanları olarak kullanılan bifosfo- natlar ve düşük-doz doksisiklin ilaçlarının etkilerini değerlendireceğiz.

Anahtar Kelimeler: Periodontit, diabetes mellitus, bifosfonat, doksisiklin, alveolar kemik kaybı

Keywords

Periodontitis,diabetes mellitus,bisphosphonate,doxycycline

References

.Listgarten MA. Pathogenesis of periodontitis. J Clin Periodontol 1986;13:418-30.
2.Çanakçı CF, Doğan GE. Role of nitric oxide in inflammatory periodontal diseases: a revıew. J Dent Fac Atatürk Uni 2014; 9:74-84.
3.Mealey BL, Oates TW. Diabetes mellitus and periodontal diseases. J Periodontol 2006;77:1289-303.
4.Saito T, Shimazaki Y, Kiyohara Y, Kato I, Kubo M, Iida M, Koga T. The severity of periodontal disease is associated with the development of glucose intolerance in non-diabetics: the Hisayama study. J Dent Res 2004;83:485-90.
5.Loe H. Periodontal disease. The sixth complication of diabetes mellitus. Diabetes Care 1993;16:329-334.
6.Campus G, Salem A, Uzzau S, Baldoni E, Tonolo G. Diabetes and periodontal disease: a case-control study. J Periodontol 2005;76:418-25.
7.Ozdemir SP, Kurtis B, Tuter G, Bozkurt Ş, Gültekin SE, Sengüven B, Watanabe K, Aydın S. Effects of low-dose doxycycline and bisphosphonate clodronate on alveolar bone loss and gingival levels of matrix metalloproteinase-9 and interleukin-1beta in rats with diabetes: a histomorphometric and immunohistochemical study. J Periodontol 2012;83:1172-82.
8.Duarte PM, Neto JB, Casati MZ, Sallum EA, Nociti FH, Jr. Diabetes modulates gene expression in the gingival tissues of patients with chronic periodontitis. Oral Dis 2007;13:594-9.

9.Llavaneras A, Ramamurthy NS, Heikkila P, Teronen O, Salo T, Rifkin BR, Ryan ME, Golub LM, Sorsa T. A combination of a chemically modified doxycycline and a bisphosphonate synergistically inhibits endotoxin-induced periodontal breakdown in rats. J Periodontol 2001;72:1069-1077.
10.Sharma A, Pradeep AR. Clinical efficacy of 1% alendronate gel as a local drug delivery system in the treatment of chronic periodontitis: a randomized, controlled clinical trial. J Periodontol 2012;83:11-8.
21.Russell RG. Bisphosphonates: the first 40 years. Bone 2011;49:2-19.
22.Maruotti N, Corrado A, Neve A, Cantatore FP. Bisphosphonates: effects on osteoblast. Eur J Clin Pharmacol 2012;68:1013-8.
23.Fleisch H. Bisphosphonates in osteoporosis. Eur Spine J 2003;Supplement 12 2:S142-6.
24.Goya JA, Paez HA, Mandalunis PM. Effect of topical administration of monosodium olpadronate on experimental periodontitis in rats. J Periodontol 2006;77:1-6.
25.Rocha ML, Malacara JM, Sanchez-Marin FJ, Vazquez de la Torre CJ, Fajardo ME. Effect of alendronate on periodontal disease in postmenopausal women: a randomized placebo-controlled trial. J Periodontol 2004;75:1579-85.
26.Lane N, Armitage GC, Loomer P, Hsieh S, Majumdar S, Wang HY, Jeffcoat M, Munoz T. Bisphosphonate therapy improves the outcome of conventional periodontal treatment: results of a 12-month, randomized, placebo-controlled study. J Periodontol 2005;76:1113-22.
27.Yamashita J, McCauley LK, Van Poznak C. Updates on osteonecrosis of the jaw. Curr Opin Support Palliat Care 2010;4:200-6.
28.Skoglund B, Holmertz J, Aspenberg P. Systemic and local ibandronate enhance screw fixation. J Orthop Res 2004;22:1108-13.
29.Peter B, Ramaniraka N, Rakotomanana LR, Zambelli PY, Pioletti DP. Peri-implant bone remodeling after total hip replacement combined with systemic alendronate treatment: a finite element analysis. Comput Methods Biomech Biomed Engin 2004;7:73-8.
30.Adachi H, Igarashi K, Mitani H, Shinoda H. Effects of topical administration of a bisphosphonate (risedronate) on orthodontic tooth movements in rats. J Dent Res 1994;73:1478-86.
41.de Almeida JM, Ervolino E, Bonfietti LH, Novaes VC, Theodoro LH, Fernandes LA, Martins TM, Faleiros PL, Garcia VG. Adjuvant Therapy With Sodium Alendronate for the Treatment of Experimental Periodontitis in Rats. J Periodontol 2015:1-18.
42.Goes P, Melo IM, Dutra CS, Lima AP, Lima V. Effect of alendronate on bone-specific alkaline phosphatase on periodontal bone loss in rats. Arch Oral Biol 2012;57:1537-44.
43.Sharma A, Pradeep AR. Clinical efficacy of 1% alendronate gel in adjunct to mechanotherapy in the treatment of aggressive periodontitis: a randomized controlled clinical trial. J Periodontol 2012;83:19-26.
44.Alencar VB, Bezerra MM, Lima V, Abreu AL, Brito GA, Rocha FA, Ribeiro RA. Disodium chlodronate prevents bone resorption in experimental periodontitis in rats. J Periodontol 2002;73:251-6.
45.Mitsuta T, Horiuchi H, Shinoda H. Effects of topical administration of clodronate on alveolar bone resorption in rats with experimental periodontitis. J Periodontol 2002;73:479-86.
46.Shibutani T, Inuduka A, Horiki I, Luan Q, Iwayama Y. Bisphosphonate inhibits alveolar bone resorption in experimentally-induced peri-implantitis in dogs. Clin Oral Implants Res 2001;12:109-14.
47.Takaishi Y, Ikeo T, Miki T, Nishizawa Y, Morii H. Suppression of alveolar bone resorption by etidronate treatment for periodontal disease: 4- to 5-year follow-up of four patients. J Int Med Res 2003;31:575-84.
48.Takaishi Y, Miki T, Nishizawa Y, Morii H. Clinical effect of etidronate on alveolar pyorrhoea associated with chronic marginal periodontitis: report of four cases. J Int Med Res 2001;29:355-65.
49.Cetinkaya BO, Keles GC, Ayas B, Gurgor P. Effects of risedronate on alveolar bone loss and angiogenesis: a stereologic study in rats. J Periodontol 2008;79:1950-1961.
50.Shoji K, Horiuchi H, Shinoda H. Inhibitory effects of a bisphosphonate (risedronate) on experimental periodontitis in rats. J Periodontal Res 1995;30:277-84
61.Buduneli E, Buduneli N, Vardar-Sengul S, Kardeşler L, Atilla G, Lappin D, Kinane DF. Systemic low-dose doxycycline and alendronate administration and serum interleukin-1beta, osteocalcin, and C-reactive protein levels in rats. J Periodontol 2005;76:1927-33.
62.Shi F, Yu S, Xu L. Analysis of serum osteocalcin of patients with periodontitis. Zhonghua Kou Qiang Yi Xue Za Zhi 1996;31:300-2.
63.Lee NK, Sowa H, Hinoi E, Ferron M, Ahn JD, Confavreux C, Dacquin R, Mee PJ, McKee MD, Jung DY, Zhang Z, Kim JK, Mauvais-Jarvis F, Ducy P, Karsenty G. Endocrine regulation of energy metabolism by the skeleton. Cell 2007;130:456-69.
64.Chan DC, Yang RS, Ho CH, Tsai YS, Wang JJ, Tsai KT. The use of alendronate is associated with a decreased incidence of type 2 diabetes mellitus--a population-based cohort study in Taiwan. PLoS One 2015;10:e0123279.
65.Schafer AL, Sellmeyer DE, Schwartz AV, Rosen CJ, Vittinghoff E, Palermo L, Bilezikian JP, Shoback DM, Black DM. Change in undercarboxylated osteocalcin is associated with changes in body weight, fat mass, and adiponectin: parathyroid hormone (1-84) or alendronate therapy in postmenopausal women with osteoporosis (the PaTH study). J Clin Endocrinol Metab 2011;96:E1982-9.
66.Ferron M, Wei J, Yoshizawa T, Del Fattore A, DePinho RA, Teti A, Ducy P, Karsenty G. Insulin signaling in osteoblasts integrates bone remodeling and energy metabolism. Cell 2010;142:296-308.
67.Schwartz AV, Schafer AL, Grey A, Vittinghoff E, Palermo L, Lui LY, Wallace RB, Cummings SR, Black DM, Bauer DC, Reid IR. Effects of antiresorptive therapies on glucose metabolism: results from the FIT, HORIZON-PFT, and FREEDOM trials. J Bone Miner Res 2013;28:1348-54.
68.Pittas AG, Harris SS, Eliades M, Stark P, Dawson-Hughes B. Association between serum osteocalcin and markers of metabolic phenotype. J Clin Endocrinol Metab 2009;94:827-32.
69.Shea MK, Gundberg CM, Meigs JB, Dallal GE, Saltzman E, Yoshida M, Jacques PF, Booth SL. Gamma-carboxylation of osteocalcin and insulin resistance in older men and women. Am J Clin Nutr 2009;90:1230-5.
70.Ngarmukos C, Chailurkit LO, Chanprasertyothin S, Hengprasith B, Sritara P, Ongphiphadhanakul B. A reduced serum level of total osteocalcin in men predicts the development of diabetes in a long-term follow-up cohort. Clin Endocrinol (Oxf) 2012;77:42-6
81.Anavi-Lev K, Anavi Y, Chaushu G, Alon DM, Gal G, Kaplan I. Bisphosphonate related osteonecrosis of the jaws: clinico-pathological investigation and histomorphometric analysis. Oral Surg Oral Med Oral Pathol Oral Radiol 2013;115:660-6.
82.Ficarra G, Beninati F, Rubino I, Vannucchi A, Longo G, Tonelli P, Pini Prato G. Osteonecrosis of the jaws in periodontal patients with a history of bisphosphonates treatment. J Clin Periodontol 2005;32:1123-8.
83.Saussez S, Javadian R, Hupin C, Magremanne M, Chantrain G, Loeb I, Decaestecker C. Bisphosphonate-related osteonecrosis of the jaw and its associated risk factors: a Belgian case series. Laryngoscope 2009;119:323-9.
84.Marx RE, Cillo JE, Jr., Ulloa JJ. Oral bisphosphonate-induced osteonecrosis: risk factors, prediction of risk using serum CTX testing, prevention, and treatment. J Oral Maxillofac Surg 2007;65:2397-410.
85.Deng X, Tamai R, Endo Y, Kiyoura Y. Alendronate augments interleukin-1beta release from macrophages infected with periodontal pathogenic bacteria through activation of caspase-1. Toxicol Appl Pharmacol 2009;235:97-104.
86.Makkonen N, Salminen A, Rogers MJ, Frith JC, Urtti A, Azhayeva E, Mönkkönen J. Contrasting effects of alendronate and clodronate on RAW 264 macrophages: the role of a bisphosphonate metabolite. Eur J Pharm Sci 1999;8:109-18.
87.Tsao C, Darby I, Ebeling PR, Walsh K, O'Brien-Simpson N, Reynolds E, Borromeo G. Oral health risk factors for bisphosphonate-associated jaw osteonecrosis. J Oral Maxillofac Surg 2013;71:1360-6.
88.Urade M. [Diabetes mellitus and bisphosphonate-related osteonecrosis of the jaws]. Clin Calcium 2009;19:1332-8.
89.Molcho S, Peer A, Berg T, Futerman B, Khamaisi M. Diabetes microvascular disease and the risk for bisphosphonate-related osteonecrosis of the jaw: a single center study. J Clin Endocrinol Metab 2013;98:E1807-12.
90.Berti-Couto SA, Vasconcelos AC, Iglesias JE, Figueiredo MA, Salum FG, Cherubini K. Diabetes mellitus and corticotherapy as risk factors for alendronate-related osteonecrosis of the jaws: a study in Wistar rats. Head Neck 2014;36:84-93
101.Sgolastra F, Petrucci A, Gatto R, Giannoni M, Monaco A. Long-term efficacy of subantimicrobial-dose doxycycline as an adjunctive treatment to scaling and root planing: a systematic review and meta-analysis. J Periodontol 2011;82:1570-1581.
102.Tsalikis L, Sakellari D, Dagalis P, Boura P, Konstantinidis A. Effects of doxycycline on clinical, microbiological and immunological parameters in well-controlled diabetes type-2 patients with periodontal disease: a randomized, controlled clinical trial. J Clin Periodontol 2014;41:972-80.
103.Martorelli de Lima AF, Cury CC, Palioto DB, Duro AM, da Silva RC, Wolff LF. Therapy with adjunctive doxycycline local delivery in patients with type 1 diabetes mellitus and periodontitis. J Clin Periodontol 2004;31:648-3.
104.Preshaw PM, Hefti AF, Jepsen S, Etienne D, Walker C, Bradshaw MH. Subantimicrobial dose doxycycline as adjunctive treatment for periodontitis. A review. J Clin Periodontol 2004;31:697-707.
105.Tella E, Aldahlawi S, Eldeeb A, El Gazaerly H. The Effect of Systemic Delivery of Aminoguanidine versus Doxycycline on the Resorptive Phase of Alveolar Bone Following modified Widman Flap in Diabetic Rats: A Histopathological and Scanning Electron Microscope (SEM) study. Int J Health Sci (Qassim) 2014;8:275-85.
106.Agarwal A, Bhattacharya HS, Srikanth G, Singh A. Comparative evaluation of decalcified freeze dried bone allograft with and without local doxycycline in non-contained human periodontal infrabony defects. J Indian Soc Periodontol 2013;17:490-4.
107.Llambes F, Silvestre FJ, Hernandez-Mijares A, Guiha R, Caffesse R. Effect of non-surgical periodontal treatment with or without doxycycline on the periodontium of type 1 diabetic patients. J Clin Periodontol 2005;32:915-20.
108.Bettany JT, Peet NM, Wolowacz RG, Skerry TM, Grabowski PS. Tetracyclines induce apoptosis in osteoclasts. Bone 2000;27:75-80.
109.Holmes SG, Still K, Buttle DJ, Bishop NJ, Grabowski PS. Chemically modified tetracyclines act through multiple mechanisms directly on osteoclast precursors. Bone 2004;35:471-8.
110.Caton JG, Ciancio SG, Blieden TM, Bradshaw M, Crout RJ, Hefti AF, Massaro JM, Polson AM, Thomas J, Walker C. Treatment with subantimicrobial dose doxycycline improves the efficacy of scaling and root planing in patients with adult periodontitis. J Periodontol 2000;71:521-32
131.Sasaki T, Kaneko H, Ramamurthy NS, Golub LM. Tetracycline administration restores osteoblast structure and function during experimental diabetes. Anat Rec 1991;231:25-34.
132.Fowlkes JL, Nyman JS, Bunn RC, Cockrell GE, Wahl EC, Rettiganti MR, Lumpkin CK Jr, Thrailkill KM. Effects of long-term doxycycline on bone quality and strength in diabetic male DBA/2J mice. Bone Rep 2015;1:16-9.
133.Yaffe A, Herman A, Bahar H, Binderman I. Combined local application of tetracycline and bisphosphonate reduces alveolar bone resorption in rats. J Periodontol 2003;74:1038-42.
134.Buduneli E, Vardar S, Buduneli N, Berdeli AH, Türkoğlu O, Başkesen A, Atilla G. Effects of combined systemic administration of low-dose doxycycline and alendronate on endotoxin-induced periodontitis in rats. J Periodontol 2004;75:1516-23.

Details

Primary Language

Turkish

Subjects

-

Journal Section

-

Authors

Şeyma Bozkurt Doğan This is me

Figen Özgöz Dede This is me

Publication Date

November 24, 2016

Submission Date

February 7, 2017

Acceptance Date

March 16, 2016

Published in Issue

Year 2016

DOI

https://doi.org/10.17567/ataunidfd.290572

IZ

https://izlik.org/JA45DP78WB

Cite

RIS / Bibtex

APA

Bozkurt Doğan, Ş., & Özgöz Dede, F. (2016). THE EFFECT OF BISPHOSPHONATES AND LOW-DOSE DOXCYCLINE THERAPY IN DIABETICS WITH PERIODONTITIS: A REVIEW. Atatürk Üniversitesi Diş Hekimliği Fakültesi Dergisi, 65-79. https://doi.org/10.17567/ataunidfd.290572

AMA

1.Bozkurt Doğan Ş, Özgöz Dede F. THE EFFECT OF BISPHOSPHONATES AND LOW-DOSE DOXCYCLINE THERAPY IN DIABETICS WITH PERIODONTITIS: A REVIEW. Atatürk Üniversitesi Diş Hekimliği Fakültesi Dergisi. Published online November 1, 2016:65-79. doi:10.17567/ataunidfd.290572

Chicago

Bozkurt Doğan, Şeyma, and Figen Özgöz Dede. 2016. “THE EFFECT OF BISPHOSPHONATES AND LOW-DOSE DOXCYCLINE THERAPY IN DIABETICS WITH PERIODONTITIS: A REVIEW”. Atatürk Üniversitesi Diş Hekimliği Fakültesi Dergisi, November 1, 65-79. https://doi.org/10.17567/ataunidfd.290572.

EndNote

Bozkurt Doğan Ş, Özgöz Dede F (November 1, 2016) THE EFFECT OF BISPHOSPHONATES AND LOW-DOSE DOXCYCLINE THERAPY IN DIABETICS WITH PERIODONTITIS: A REVIEW. Atatürk Üniversitesi Diş Hekimliği Fakültesi Dergisi 65–79.

IEEE

[1]Ş. Bozkurt Doğan and F. Özgöz Dede, “THE EFFECT OF BISPHOSPHONATES AND LOW-DOSE DOXCYCLINE THERAPY IN DIABETICS WITH PERIODONTITIS: A REVIEW”, Atatürk Üniversitesi Diş Hekimliği Fakültesi Dergisi, pp. 65–79, Nov. 2016, doi: 10.17567/ataunidfd.290572.

ISNAD

Bozkurt Doğan, Şeyma - Özgöz Dede, Figen. “THE EFFECT OF BISPHOSPHONATES AND LOW-DOSE DOXCYCLINE THERAPY IN DIABETICS WITH PERIODONTITIS: A REVIEW”. Atatürk Üniversitesi Diş Hekimliği Fakültesi Dergisi. November 1, 2016. 65-79. https://doi.org/10.17567/ataunidfd.290572.

JAMA

1.Bozkurt Doğan Ş, Özgöz Dede F. THE EFFECT OF BISPHOSPHONATES AND LOW-DOSE DOXCYCLINE THERAPY IN DIABETICS WITH PERIODONTITIS: A REVIEW. Atatürk Üniversitesi Diş Hekimliği Fakültesi Dergisi. 2016;:65–79.

MLA

Bozkurt Doğan, Şeyma, and Figen Özgöz Dede. “THE EFFECT OF BISPHOSPHONATES AND LOW-DOSE DOXCYCLINE THERAPY IN DIABETICS WITH PERIODONTITIS: A REVIEW”. Atatürk Üniversitesi Diş Hekimliği Fakültesi Dergisi, Nov. 2016, pp. 65-79, doi:10.17567/ataunidfd.290572.

Vancouver

1.Şeyma Bozkurt Doğan, Figen Özgöz Dede. THE EFFECT OF BISPHOSPHONATES AND LOW-DOSE DOXCYCLINE THERAPY IN DIABETICS WITH PERIODONTITIS: A REVIEW. Atatürk Üniversitesi Diş Hekimliği Fakültesi Dergisi. 2016 Nov. 1;65-79. doi:10.17567/ataunidfd.290572