Abstract
Purpose of Review
Metabolic syndrome is a systemic condition that has components such as obesity, dyslipidemia, hyperglycemia, and hypertension and is associated with an increased risk of cardiovascular disease and type 2 diabetes. Periodontitis is a chronic inflammatory disease characterized by progressive attachment loss that develops as a result of the host response to the dysbiotic plaque microbiome. Periodontal diseases can jeopardize systemic health through various mechanisms as well as be detrimental to oral health. The interlinks of these mechanisms and the pathogenesis of metabolic syndrome cause a bidirectional interaction between the two diseases. This review aimed to evaluate studies focusing on potential interaction mechanisms between periodontal disease and metabolic syndrome and present the clinical implications of these interactions.
Recent Findings
Studies dealing with the relationship between metabolic syndrome and components of metabolic syndrome and periodontal disease are available in the literature, and it is reported that the two conditions are generally related. According to literature findings, inflammation is a common pathway in metabolic syndrome and periodontal disease. While both diseases can exacerbate the inflammation and affect the other, it is also seen that the severity of the disease increases by being affected by the increasing chronic inflammation itself. The fact that they have common risk factors other than the intersecting pathways in the two diseases in the host inflammatory response strengthens their relationship but prevents the understanding of causality and the visibility of the initiating factor. Although these common risk factors affect the prevalence studies, the immune mechanisms identified to date and the results of longitudinal studies show that this relationship is bidirectional. Fewer data describing the relationship between metabolic syndrome and periodontal disease, which is significant for systemic disease risk. This is explained by the factors that make the standardization of studies difficult. The use of different disease definitions, the existence of different forms of periodontal disease, the multi-component of metabolic syndrome, and different study plans prevent standardization and reduce the number of studies to be included in compilations and meta-analyses that will reveal essential information on the subject.
Summary
It is thought that the data of longitudinal studies, which have a standardized study design and use common diagnostic criteria, can more clearly reveal the relationship between periodontal disease and metabolic syndrome. Thus, the direction of the relationship between the two diseases (bidirectional or unidirectional), cause-effect relationship, dose-response relationship, and treatment approaches can be obtained.
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References
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Papapanou PN, Sanz M, Buduneli N, Dietrich T, Feres M, Fine DH, et al. Periodontitis: consensus report of workgroup 2 of the 2017 World Workshop on the classification of periodontal and peri-implant diseases and conditions. J Periodontol. 2018;89:S173–S82.
Petersen P. The World Oral Health Report 2003: continuous improvement of oral health in the 21st century - the approach of the WHO Global Oral Health Programme. Community Dent Oral Epidemiol. 2004;31(Suppl 1):3–23. https://doi.org/10.1046/j..2003.com122.x.
Tonetti MS, Jepsen S, Jin L, Otomo-Corgel J. Impact of the global burden of periodontal diseases on health, nutrition and wellbeing of mankind: a call for global action. J Clin Periodontol. 2017;44(5):456–62.
Pirih FQ, Monajemzadeh S, Singh N, Sinacola RS, Shin JM, Chen T, et al. Association between metabolic syndrome and periodontitis: the role of lipids, inflammatory cytokines, altered host response, and the microbiome. Periodontol 2000. 2021;87(1):50–75.
Day C. Metabolic syndrome, or What you will: definitions and epidemiology. Diab Vasc Dis Res. 2007;4(1):32–8.
Stone NJ, Bilek S, Rosenbaum S. Recent national cholesterol education program adult treatment panel III update: adjustments and options. Am J Cardiol. 2005;96(4):53–9.
Alberti KG, Eckel RH, Grundy SM, Zimmet PZ, Cleeman JI, Donato KA, et al. Harmonizing the metabolic syndrome: a joint interim statement of the international diabetes federation task force on epidemiology and prevention; national heart, lung, and blood institute; American heart association; world heart federation; international atherosclerosis society; and international association for the study of obesity. Circulation. 2009;120(16):1640–5.
Grundy SM, Bilheimer D, Chait A, Clark LT, Denke M, Havel RJ, et al. Summary of the second report of the National Cholesterol Education Program (NCEP) Expert Panel on detection, evaluation, and treatment of high blood cholesterol in adults (Adult Treatment Panel II). Jama. 1993;269(23):3015–23.
Caton JG, Armitage G, Berglundh T, Chapple IL, Jepsen S, Kornman KS, et al. A new classification scheme for periodontal and peri-implant diseases and conditions–introduction and key changes from the 1999 classification. J Clin Periodontol. 2018;89:S1–8.
Tonetti MS, Greenwell H, Kornman KS. Staging and grading of periodontitis: framework and proposal of a new classification and case definition. J Periodontol. 2018;89:S159–S72.
Suvan J, D’Aiuto F, Moles DR, Petrie A, Donos N. Association between overweight/obesity and periodontitis in adults. A systematic review. Obes Rev. 2011;12(5):e381–404.
Jepsen S, Caton JG, Albandar JM, Bissada NF, Bouchard P, Cortellini P, et al. Periodontal manifestations of systemic diseases and developmental and acquired conditions: consensus report of workgroup 3 of the 2017 World Workshop on the classification of periodontal and peri-implant diseases and conditions. J Clin Periodontol. 2018;45:S219–S29.
• Campos JR, Martins CC, Faria SFS, Carvalho AP, Pereira AG, Costa FO, et al. Association between components of metabolic syndrome and periodontitis: a systematic review and meta-analysis. Clin Oral Investig. 2022;26(9):5557–74. This current meta-analysis and systematic review evaluated the effects of metabolic syndrome and its components in the association with periodontal disease.
Koo HS, Hong SM. Prevalence and risk factors for periodontitis among patients with metabolic syndrome. Metab Syndr Relat Disord. 2018;16(7):375–81.
Pham T. The association between periodontal disease severity and metabolic syndrome in Vietnamese patients. Int J Dent Hyg. 2018;16(4):484–91.
Lamster IB, Pagan M. Periodontal disease and the metabolic syndrome. Int Dent J. 2017;67(2):67–77.
Nibali L, Tatarakis N, Needleman I, Tu Y-K, D'Aiuto F, Rizzo M, et al. Association between metabolic syndrome and periodontitis: a systematic review and meta-analysis. J Clin Endocrinol Metabol. 2013;98(3):913–20.
Daudt LD, Musskopf ML, Mendez M, Remonti LLR, Leitão CB, Gross JL, et al. Association between metabolic syndrome and periodontitis: a systematic review and meta-analysis. Braz Oral Res. 2018:32.
Morita T, Yamazaki Y, Mita A, Takada K, Seto M, Nishinoue N, et al. A cohort study on the association between periodontal disease and the development of metabolic syndrome. J Periodontol. 2010;81(4):512–9.
Morita I, Okamoto Y, Yoshii S, Nakagaki H, Mizuno K, Sheiham A, et al. Five-year incidence of periodontal disease is related to body mass index. J Dent Res. 2011;90(2):199–202.
Tanaka A, Takeuchi K, Furuta M, Takeshita T, Suma S, Shinagawa T, et al. Relationship of toothbrushing to metabolic syndrome in middle-aged adults. J Clin Periodontol. 2018;45(5):538–47.
Garrow JS, Webster J. Quetelet's index (W/H2) as a measure of fatness. Int J Obes (Lond). 1985;9(2):147–53.
Kissebah AH, Vydelingum N, Murray R, Evans DJ, Kalkhoff RK, Adams PW. Relation of body fat distribution to metabolic complications of obesity. J Clin Endocrinol Metabol. 1982;54(2):254–60.
Klein S, Allison DB, Heymsfield SB, Kelley DE, Leibel RL, Nonas C, et al. Waist circumference and cardiometabolic risk: a consensus statement from shaping America’'s health: association for weight management and obesity prevention; NAASO, the Obesity Society; the American Society for Nutrition; and the American Diabetes Association. Am J Clin Nutr. 2007;85(5):1197–202.
Goodpaster BH. Measuring body fat distribution and content in humans. Curr Opin Clin Nutr Metab Care. 2002;5(5):481–7.
Bays H. Central obesity as a clinical marker of adiposopathy; increased visceral adiposity as a surrogate marker for global fat dysfunction. Curr Opin Endocrinol Diabetes Obes. 2014;21(5):345.
Perlstein MI, Bissada NF. Influence of obesity and hypertension on the severity of periodontitis in rats. Oral Surg Oral Med Oral Pathol. 1977;43(5):707–19.
Saito T, Shimazaki Y, Sakamoto M. Obesity and periodontitis. N Engl J Med. 1998;339(7):482–3.
Wood N, Johnson RB, Streckfus CF. Comparison of body composition and periodontal disease using nutritional assessment techniques: Third National Health and Nutrition Examination Survey (NHANES III). J Clin Periodontol. 2003;30(4):321–7.
• Ganesan SM, Vazana S, Stuhr S. Waistline to the gumline: relationship between obesity and periodontal disease-biological and management considerations. Periodontol 2000. 2021;87(1):299–314. This review evaluates the biological interlinks between obesity and periodontal disease and delineates practical considerations for managing these patients in an everyday periodontal practice setting.
Fantuzzi G. Adipose tissue, adipokines, and inflammation. J Allergy Clin Immunol. 2005;115(5):911–9.
Tomofuji T, Yamamoto T, Tamaki N, Ekuni D, Azuma T, Sanbe T, et al. Effects of obesity on gingival oxidative stress in a rat model. J Periodontol. 2009;80(8):1324–9.
Chapple IL, Matthews JB. The role of reactive oxygen and antioxidant species in periodontal tissue destruction. Periodontol 2000. 2007;43(1):160–232.
Karthikeyan B, Pradeep A. Gingival crevicular fluid and serum leptin: their relationship to periodontal health and disease. J Clin Periodontol. 2007;34(6):467–72.
Furugen R, Hayashida H, Yamaguchi N, Yoshihara A, Ogawa H, Miyazaki H, et al. The relationship between periodontal condition and serum levels of resistin and adiponectin in elderly Japanese. J Periodontal Res. 2008;43(5):556–62.
Yılmaz G, Kırzıoğlu FY, Doğuç DK, Koçak H, Orhan H. Ghrelin levels in chronic periodontitis patients. Odontology. 2014;102(1):59–67.
Pasare C, Medzhitov R. Toll-like receptors: linking innate and adaptive immunity. Adv Exp Med Biol. 2005;560:11–8.
Medvedev AE, Sabroe I, Hasday JD, Vogel SN. Invited review: Tolerance to microbial TLR ligands: molecular mechanisms and relevance to disease. J Endotoxin Res. 2006;12(3):133–50.
Fentoğlu Ö, Köroğlu BK, Hiçyılmaz H, Sert T, Özdem M, Sütçü R, et al. Pro-inflammatory cytokine levels in association between periodontal disease and hyperlipidaemia. J Clin Periodontol. 2011;38(1):8–16.
Haffajee AD, Socransky SS. Relation of body mass index, periodontitis and Tannerella forsythia. J Clin Periodontol. 2009;36(2):89–99.
Tam J, Hoffmann T, Fischer S, Bornstein S, Gräßler J, Noack B. Obesity alters composition and diversity of the oral microbiota in patients with type 2 diabetes mellitus independently of glycemic control. PloS One. 2018;13(10):e0204724.
Lin JH, Duffy JL, Roginsky MS. Microcirculation in diabetes mellitus: a study of gingival biopsies. Hum Pathol. 1975;6(1):77–96.
Gümüş P, Nizam N, Lappin DF, Buduneli N. Saliva and serum levels of B-cell activating factors and tumor necrosis factor-α in patients with periodontitis. J Periodontol. 2014;85(2):270–80.
Parameswaran K, Todd DC, Soth M. Altered respiratory physiology in obesity. Can Respir J. 2006;13(4):203–10.
• Jepsen S, Suvan J, Deschner J. The association of periodontal diseases with metabolic syndrome and obesity. Periodontol 2000. 2020;83(1):125–53. This is a recently published review that follows highlights the current evidence from epidemiologic studies reporting on the association between periodontal disease, metabolicm syndrome, and obesity.
Nakajima M, Arimatsu K, Kato T, Matsuda Y, Minagawa T, Takahashi N, et al. Oral administration of P. gingivalis induces dysbiosis of gut microbiota and impaired barrier function leading to dissemination of enterobacteria to the liver. PloS One. 2015;10(7):e0134234.
Lianhui Y, Meifei L, Zhongyue H, Yunzhi F. Association between chronic periodontitis and hyperlipidemia: a meta-analysis based on observational studies. Hua xi kou Qiang yi xue za zhi= Huaxi Kouqiang Yixue Zazhi= West China Journal of Stomatology. 2017;35(4):419–26.
Nepomuceno R, Pigossi SC, Finoti LS, Orrico SR, Cirelli JA, Barros SP, et al. Serum lipid levels in patients with periodontal disease: a meta-analysis and meta-regression. J Clin Periodontol. 2017;44(12):1192–207.
Khovidhunkit W, Kim M-S, Memon RA, Shigenaga JK, Moser AH, Feingold KR, et al. Effects of infection and inflammation on lipid and lipoprotein metabolism: mechanisms and consequences to the host. J Lipid Res. 2004;45(7):1169–96.
Feingold K, Hardardottir I, Grunfeld C. Beneficial effects of cytokine induced hyperlipidemia. Z Ernahrungswiss. 1998;37:66–74.
Chen S, Lin G, You X, Lei L, Li Y, Lin M, et al. Hyperlipidemia causes changes in inflammatory responses to periodontal pathogen challenge: implications in acute and chronic infections. Arch Oral Biol. 2014;59(10):1075–84.
Ohgi K, Kajiya H, Goto-T K, Okamoto F, Yoshinaga Y, Okabe K, et al. Toll-like receptor 2 activation primes and upregulates osteoclastogenesis via lox-1. Lipids Health Dis. 2018;17(1):1–9.
Borgnakke WS, Yl€ ostalo PV, Taylor GW, Genco RJ. Effect of periodontal disease on diabetes: systematic review of epidemiologic observational evidence. J Periodontol. 2013;84:S135–S52.
Ziukaite L, Slot DE, Van der Weijden FA. Prevalence of diabetes mellitus in people clinically diagnosed with periodontitis: a systematic review and meta-analysis of epidemiologic studies. J Clin Periodontol. 2018;45(6):650–62.
Chávarry NGM, Vettore MV, Sansone C, Sheiham A. The relationship between diabetes mellitus and destructive periodontal disease: a meta-analysis. Oral Health Prev Dent. 2009;7(2):107–27.
Lackey DE, Olefsky JM. Regulation of metabolism by the innate immune system. Nat Rev Endocrinol. 2016;12(1):15–28.
Monnier VM, Glomb M, Elgawish A, Sell DR. The mechanism of collagen cross-linking in diabetes: a puzzle nearing resolution. Diabetes. 1996;45(Supplement_3):S67–72.
Manouchehr-Pour M, Spagnuolo P, Rodman H, Bissada N. Impaired neutrophil chemotaxis in diabetic patients with severe periodontitis. J Dent Res. 1981;60(3):729–30.
Naguib G, Al-Mashat H, Desta T, Graves DT. Diabetes prolongs the inflammatory response to a bacterial stimulus through cytokine dysregulation. J Investig Dermatol. 2004;123(1):87–92.
Hq FAN, Gu N, Liu F, Fei L, Xq PAN, Guo M, et al. Prolonged exposure to resistin inhibits glucose uptake in rat skeletal muscles 4. Acta Pharmacol Sin. 2007;28(3):410–6.
Sweeney G, Keen J, Somwar R, Konrad D, Garg R, Klip A. High leptin levels acutely inhibit insulin-stimulated glucose uptake without affecting glucose transporter 4 translocation in l6 rat skeletal muscle cells. Endocrinology. 2001;142(11):4806–12.
Martin-Cabezas R, Seelam N, Petit C, Agossa K, Gaertner S, Tenenbaum H, et al. Association between periodontitis and arterial hypertension: a systematic review and meta-analysis. Am Heart J. 2016;180:98–112.
Roth GA, Ankersmit HJ, Brown VB, Papapanou PN, Schmidt AM, Lalla E. Porphyromonas gingivalis infection and cell death in human aortic endothelial cells. FEMS Microbiol Lett. 2007;272(1):106–13.
Gonçalves TED, Zimmermann GS, Figueiredo LC, Souza MC, da Cruz DF, Bastos MF, et al. Local and serum levels of adipokines in patients with obesity after periodontal therapy: one-year follow-up. J Clin Periodontol. 2015;42(5):431–9.
Akram Z, Baharuddin NA, Vaithilingam RD, Rahim ZH, Chinna K, Krishna VG, et al. Effect of nonsurgical periodontal treatment on clinical periodontal variables and salivary resistin levels in obese Asians. J Oral Sci. 2017;59(1):93–102.
Al-Hamoudi N, Abduljabbar T, Mirza S, Al-Sowygh ZH, Vohra F, Javed F, et al. Non-surgical periodontal therapy reduces salivary adipocytokines in chronic periodontitis patients with and without obesity. J Investig Clin Dent. 2018;9(2):e12314.
Suresh S, Mahendra J, Singh G, Kumar ARP, Thilagar S, Rao N. Effect of nonsurgical periodontal therapy on plasma-reactive oxygen metabolite and gingival crevicular fluid resistin and serum resistin levels in obese and normal weight individuals with chronic periodontitis. J Indian Soc Periodontol. 2018;22(4):310.
López NJ, Quintero A, Casanova PA, Ibieta CI, Baelum V, López R. Effects of periodontal therapy on systemic markers of inflammation in patients with metabolic syndrome: a controlled clinical trial. J Periodontol. 2012;83(3):267–78.
Torumtay G, Kırzıoğlu F, Öztürk Tonguç M, Kale B, Calapoğlu M, Orhan H. Effects of periodontal treatment on inflammation and oxidative stress markers in patients with metabolic syndrome. J Periodontal Res. 2016;51(4):489–98.
Bizzarro S, van der Velden U, Teeuw WJ, Gerdes VE, Loos BG. Effect of periodontal therapy with systemic antimicrobials on parameters of metabolic syndrome: a randomized clinical trial. J Clin Periodontol. 2017;44(8):833–41.
Fontanille I, Boillot A, Range H, Carra MC, de Carvalho Sales-Peres SH, Czernichow S, et al. Bariatric surgery and periodontal status: a systematic review with meta-analysis. Surg Obes Relat Dis. 2018;14(10):1618–31.
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Velioğlu, E.M., Aydındoğan, S. & Hakkı, S.S. Metabolic Syndrome and Periodontal Disease. Curr Oral Health Rep 10, 43–51 (2023). https://doi.org/10.1007/s40496-023-00334-3
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DOI: https://doi.org/10.1007/s40496-023-00334-3