The impact of metabolic disorders on management of periodontal health in children

Abstract

Periodontitis is a chronic inflammatory disease caused by plaque biofilm which shares risk factors with systemic chronic diseases such as diabetes, cardiovascular disease, and osteoporosis. Many studies have found increased prevalence and rate of progression of periodontal disease in children with common metabolic disorders. Although the causal relationship and specific mechanism between them has not been determined yet. The aim of this paper is to progress on the impact of metabolic disorders on periodontal health in children and the underlying mechanisms, which provides new evidences for the prevention and intervention of metabolic disorders and periodontitis in children.

Keywords

children / metabolic disorders / periodontal health

References

[1] Kinane DF, Stathopoulou PG, Papapanou PN. Periodontal diseases. Nat Rev Dis Prim. 2017;3(1):17038.

[2] Hajishengallis G, Chavakis T. Local and systemic mechanisms linking periodontal disease and inflammatory comorbidities. Nat Rev Immunol. 2021;21(7):426-440.

[3] Aldridge JP, Lester V, Watts TL, Collins A, Viberti G, Wilson R. Single-blind studies of the effects of improved periodontal health on metabolic control in type 1 diabetes mellitus. J Clin Periodontol. 1995;22(4):271-275.

[4] Preshaw PM, Alba AL, Herrera D, et al. Periodontitis and diabetes: a two-way relationship. Diabetologia. 2012;55(1):21-31.

[5] Wang C-WJ, McCauley Laurie K. Osteoporosis and periodontitis. Curr Osteoporos Rep. 2016;14(6):284-291.

[6] Genco RJ. Current view of risk factors for periodontal diseases. J Periodontol. 1996;67(10):1041-1049.

[7] Dai W, Liu X, Han S, Li X, Xu Y, Yu Y. Influence of adipose tissue immune dysfunction on childhood obesity. Cytokine Growth Factor Rev. 2022;65:27-38.

[8] Jacobs David R, Woo Jessica G, Sinaiko Alan R, et al. Childhood cardiovascular risk factors and adult cardiovascular events. N Engl J Med. 2022;386(20):1877-1888.

[9] Soskolne AW, Bimstein E. Histomorphological study of the shedding process of human deciduous teeth at various chronological ages. Archs Oral Biol. 1977;22(5):331-335.

[10] Bimstein E, Eidelman E. Morphological changes in the attached and keratinized gingiva and gingival sulcus in the mixed dentition period. A 5-year longitudinal study. J Clin Periodontol. 1988;15(3):175-179.

[11] Matsson L. Factors influencing the susceptibility to gingivitis during childhood-a review. Int J Paediatr Dent. 1993;3:119-127.

[12] Peretz B, Machtei EM, Bimstein E. Periodontal status in childhood and early adolescence: three year follow up. J Clin Pediatr Dent. 1996;20:226-232.

[13] Bailit HL, Baldwin DC, Hunt EE. The increasing prevalence of gingival Bacteroides melaninogenicus with age in children. Archs Oral Biol. 1964;9(4):435-438.

[14] Kelstrup J. The incidence of bacteroides melaninogenicus inhuman gingival sulci, and its prevalence in the oral cavity at different ages. Periodontics. 1966;4:14-18.

[15] Socransky SS, Manganiello SD. The oral microbiota of man from birth to senility. J Periodontol. 1971;42(8):485-496.

[16] Nakagawa S, Tonogi N, Kubo S, Machida Y, Okuda K, Takazoe I. Subgingival microflora in children of early childhood, school age and circumpuberty. The proportion and frequency of gram-negative bacteria in periodontally healthy and gingivitis groups. Shoni Shikagaku Zasshi. 1991;29:72-85.

[17] Katharina SA, Hollander Georg A, Andrew M. Evolution of the immune system in humans from infancy to old age. Proc Biol Sci. 2015;282:20143085.

[18] Bimstein E. Periodontal health and disease in children and adolescents. Pediatr Clin. 1991;38(5):1183-1207.

[19] Harokopakis-Hajishengallis E. Physiologic root resorption in primary teeth: molecular and histological events. J Oral Sci. 2007;49:1-12.

[20] Oh T-J, Eber R, Wang H-L. Periodontal diseases in the child and adolescent. J Clin Periodontol. 2002;29(5):400-410.

[21] Pinkham JR, Casamassimo PS, Fields HW, McTigue DJ, Nowak A. Pediatric Dentistry. Elsevier Saunders; 2005.

[22] Bimstein E, Matsson L. Growth and development considerations in the diagnosis of gingivitis and periodontitis in children. Pediatr Dent. 1999;21:186-191.

[23] Bimstein E, Soskolne AW. A radiographic study of interproximal alveolar bone crest between the primary molars in children. ASDC J Dent Child. 1988;55:348-350.

[24] Bishara SE. Facial and dental changes in adolescents and their clinical implications. Angle Orthod. 2000;70:471-483.

[25] Sjödin B, Matsson L. Marginal bone level in the normal primary dentition. J Clin Periodontol. 1992;19(9):672-678.

[26] Peres Marco A, Macpherson Lorna MD, Weyant Robert J, et al. Oral diseases: a global public health challenge. Lancet. 2019;394(10194):249-260.

[27] Broadbent Jonathan M, Murray TW, Boyens John V, Poulton R. Dental plaque and oral health during the first 32 years of life. J Am Dent Assoc. 2011;142(4):415-426.

[28] D’Mello GI. Long-term Oral and General Health Outcomes in Adolescents Who Had Extensive Decay in Early Childhood. Doctor of Clinical Dentistry Thesis. University of Otago; 2011.

[29] Armitage G. Development of a classification system for periodontal diseases and conditions. Ann Periodontol. 1999;4:1-6.

[30] Bimstein E, Huja PE, Ebersole Jeffrey L. The potential lifespan impact of gingivitis and periodontitis in children. J Clin Pediatr Dent. 2013;38(2):95-99.

[31] Saxén L. Juvenile periodontitis. J Clin Periodontol. 1980;7:1-19.

[32] Walker JD, MacKenzie IE. Periodontal diseases in children and adolescents. In: Stewart RE, Barber TK, Troutman KC, et al., eds. Dentistry. Scientific Foundations and Clinical Practice. CV Mosby Company; 1982: 62.

[33] American Academy of Periodontology-Research. Science and therapy committee, periodontal diseases of children and adolescents. Pediatr Dent. 2008;30:240-247.

[34] Albandar JM, Brown LJ, Brunelle JA, Loe H. Gingival state and dental calculus in early-onset periodontitis. J Periodontol. 1996;67(10):953-959.

[35] Albandar JM, Muranga MB, Rams TE. Prevalence of aggressive periodontitis in school attendees in Uganda. J Clin Periodontol. 2002;29(9):823-831.

[36] Gjermo P, Rosing CK, Susin C, Oppermann R. Periodontal diseases in central and South America. Periodontol 2000. 2002;29(1):70-78.

[37] Fi C, Wo W. Periodontal disease and systemic diseases: an overview on recent progresses. J Biol Regul Homeost Agents. 2021;35:1-9.

[38] Hajishengallis G. Interconnection of periodontal disease and comorbidities: evidence, mechanisms, and implications. Periodontol 2000. 2022;89(1):9-18.

[39] Loos Bruno G, Van Dyke Thomas E. The role of inflammation and genetics in periodontal disease. Periodontol 2000. 2020;83(1):26-39.

[40] Hajishengallis G. Periodontitis: from microbial immune subversion to systemic inflammation. Nat Rev Immunol. 2015;15(1):30-44.

[41] Reeves AF, Rees JM, Schiff M, Hujoel P. Total body weight and waist circumference associated with chronic periodontitis among adolescents in the United States. Arch Pediatr Adolesc Med. 2006;160(9):894-899.

[42] Zhao B, Jin C, Li L, Wang Y. Increased expression of TNF-α occurs before the development of periodontitis among obese Chinese children: a potential marker for prediction and prevention of periodontitis. Oral Health Prev Dent. 2016;14(1):71-75.

[43] Gregg EW, Shaw JE. Global health effects of overweight and obesity. N Engl J Med. 2017;377(1):80-81.

[44] GBD 2015 Obesity Collaborators, Afshin A, Forouzanfar Mohammad H, et al. Health effects of overweight and obesity in 195 countries over 25 years. N Engl J Med. 2017;377(1):13-27.

[45] Pan X-F, Wang L, Pan A. Epidemiology and determinants of obesity in China. Lancet Diabetes Endocrinol. 2021;9(6):373-392.

[46] Lundin M, Yucel-Lindberg T, Dahllöf G, Marcus C, Modéer T. Correlation between TNFalpha in gingival crevicular fluid and body mass index in obese subjects. Acta Odontol Scand. 2004;62(5):273-277.

[47] Janem WF, Scannapieco FA, Sabharwal A, et al. Salivary inflammatory markers and microbiome in normoglycemic lean and obese children compared to obese children with type 2 diabetes. PLoS One. 2017;12(3):e0172647.

[48] Lehmann-KalataSurdacka APA, Ciężka-Hsiao E, Swora-Cwynar E, Grzymisławski M. Clinical parameters of oral cavity, physical and microbiological properties of saliva in patients with obesity [in Polish]. Dent Med Probl. 2015;52(4):415-423.

[49] Scorzetti L, Marcattili D, Pasini M, Mattei A, Marchetti E, Marzo G. Association between obesity and periodontal disease in children. Eur J Paediatr Dent. 2013;14(3):181-184.

[50] Weng J, Zhou Z, Guo L, et al. Incidence of type 1 diabetes in China, 2010–13: population based study. BMJ. 2018;360:j5295.

[51] Diamond Project Group. Incidence and trends of childhood type 1 diabetes worldwide 1990–1999. Diabet Med. 2006;23(8):857-866.

[52] Patterson CC, Harjutsalo V, Rosenbauer J, et al. Trends and cyclical variation in the incidence of childhood type 1 diabetes in 26 European centres in the 25 year period 1989–2013: a multicentre prospective registration study. Diabetologia. 2019;62(3):408-417.

[53] Gale EA. The rise of childhood type 1 diabetes in the 20th century. Diabetes. 2002;51(12):3353-3361.

[54] Dabelea D, Mayer-Davis EJ, Saydah S, et al. Prevalence of type 1 and type 2 diabetes among children and adolescents from 2001 to 2009. JAMA. 2014;311(17):1778-1786.

[55] Fu J, Prasad HC. Changing epidemiology of metabolic syndrome and type 2 diabetes in Chinese youth. Curr Diabetes Rep. 2014;14(1):447.

[56] Shimazaki Y, Egami Y, Matsubara T, et al. Relationship between obesity and physical fitness and periodontitis. J Periodontol. 2010;81(8):1124-1131.

[57] Chaffee Benjamin W, Weston Scott J. Association between chronic periodontal disease and obesity: a systematic review and meta-analysis. J Periodontol. 2010;81(12):1708-1724.

[58] Kim E-J, Jin B-H, Bae K-H. Periodontitis and obesity: a study of the Fourth Korean national health and nutrition examination survey. J Periodontol. 2011;82(4):533-542.

[59] Jepsen S, Suvan J, Deschner J. The association of periodontal diseases with metabolic syndrome and obesity. Periodontol 2000. 2020;83(1):125-153.

[60] Timonen P, Niskanen M, Suominen-Taipale L, Jula A, Knuuttila M, Ylöstalo P. Metabolic syndrome, periodontal infection, and dental caries. J Dent Res. 2010;89(10):1068-1073.

[61] Morita T, Yamazaki Y, Mita A, et al. A cohort study on the association between periodontal disease and the development of metabolic syndrome. J Periodontol. 2010;81(4):512-519.

[62] Ka K, Rousseau MC, Lambert M, et al. Metabolic syndrome and gingival inflammation in Caucasian children with a family history of obesity. J Clin Periodontol. 2013;40(11):986-993.

[63] Lalla E, Cheng B, Lal S, et al. Diabetes-related parameters and periodontal conditions in children. J Periodontal Res. 2007;42(4):345-349.

[64] Recep O, Simsek Sera, Zerrin O, et al. The influence of type-1 diabetes mellitus on dentition and oral health in children and adolescents. Yonsei Med J. 2008;49:357-365.

[65] Weintraub JA, Lopez Mitnik G, Dye BA. Oral diseases associated with nonalcoholic fatty liver disease in the United States. J Dent Res. 2019;98(11):1219-1226.

[66] Cornier M-A, Dabelea D, Hernandez Teri L, et al. The metabolic syndrome. Endocr Rev. 2008;29(7):777-822.

[67] Zimmet P, Alberti G, Kaufman F, et al. The metabolic syndrome in children and adolescents. Lancet. 2007;369(9579):2059-2061.

[68] Olza J, Gil-Campos M, Leis R, et al. Presence of the metabolic syndrome in obese children at prepubertal age. Ann Nutr Metab. 2011;58(4):343-350.

[69] Reinehr T, de Sousa G, Toschke AM, Andler W. Comparison of metabolic syndrome prevalence using eight different definitions: a critical approach. Arch Dis Child. 2007;92(12):1067-1072.

[70] Baroncelli GI, Angiolini M, Ninni E, et al. Prevalence and pathogenesis of dental and periodontal lesions in children with X-linked hypophosphatemic rickets. Eur J Paediatr Dent. 2006;7:61-66.

[71] Chen Y, Yang Y-C, Zhu B-L, Wu C, Lin R, Zhang X. Association between periodontal disease, tooth loss and liver diseases risk. J Clin Periodontol. 2020;47(9):1053-1063.

[72] Lee K-S, Lee SG, Kim E-K, et al. Metabolic syndrome parameters in adolescents may be determinants for the future periodontal diseases. J Clin Periodontol. 2015;42(2):105-112.

[73] Holick Michael F. Resurrection of vitamin D deficiency and rickets. J Clin Invest. 2006;116(8):2062-2072.

[74] Miller Walter L, Imel Erik A. Rickets, vitamin D, and Ca/P metabolism. Horm Res Paediatr. 2022;95(6):579-592.

[75] Prentice A. Nutritional rickets around the world. J Steroid Biochem Mol Biol. 2013;136:201-206.

[76] Thacher Tom D, Fischer Philip R, Tebben Peter J, et al. Increasing incidence of nutritional rickets: a population-based study in Olmsted County, Minnesota. Mayo Clin Proc. 2013;88(2):176-183.

[77] Baroncelli Giampiero I, Toschi B, Bertelloni S. Hypophosphatemic rickets. Curr Opin Endocrinol Diabetes Obes. 2012;19(6):460-467.

[78] Beck-Nielsen SS, Brock-Jacobsen B, Gram J, Brixen K, Jensen TK. Incidence and prevalence of nutritional and hereditary rickets in southern Denmark. Eur J Endocrinol. 2009;160(3):491-497.

[79] Endo I, Fukumoto S, Ozono K, et al. Nationwide survey of fibroblast growth factor 23 (FGF23)-related hypophosphatemic diseases in Japan: prevalence, biochemical data and treatment. Endocr J. 2015;62(9):811-816.

[80] Rafaelsen S, Johansson S, Raeder H, Bjerknes R. Hereditary hypophosphatemia in Norway: a retrospective population-based study of genotypes phenotypes, and treatment complications. Eur J Endocrinol. 2016;174(2):125-136.

[81] Darveau Richard P. Periodontitis: a polymicrobial disruption of host homeostasis. Nat Rev Microbiol. 2010;8(7):481-490.

[82] Lalla E, Papapanou Panos N. Diabetes mellitus and periodontitis: a tale of two common interrelated diseases. Nat Rev Endocrinol. 2011;7(12):738-748.

[83] Stevenson David A, Carey John C, Byrne Janice LB, et al. Analysis of skeletal dysplasias in the Utah population. Am J Med Genet A. 2012;158(5):1046-1054.

[84] Rauch F, Glorieux Francis H. Osteogenesis imperfecta. Lancet. 2004;363(9418):1377-1385.

[85] Thomas Inas H, DiMeglio Linda A. Advances in the classification and treatment of osteogenesis imperfecta. Curr Osteoporos Rep. 2016;14:1-9.

[86] Sillence DO, Senn A, Danks DM. Genetic heterogeneity in osteogenesis imperfecta. J Med Genet. 1979;16(2):101-116.

[87] Holick MF, Hossein-Nezhad A, Tabatabaei F. Multiple fractures in infants who have Ehlers-Danlos/hypermobility syndrome and or vitamin D deficiency: a case series of 72 infants whose parents were accused of child abuse and neglect. Dermatoendocrinol. 2017;9(1):e1279768.

[88] Judge Daniel P, Dietz Harry C. Marfan's syndrome. Lancet. 2005;366(9501):1965-1976.

[89] Alterio A, Alisi A, Liccardo D, Nobili V. Non-alcoholic fatty liver and metabolic syndrome in children: a vicious circle. Horm Res Paediatr. 2014;82(5):283-289.

[90] Nobili V, Svegliati-Baroni G, Alisi A, Miele L, Valenti L, Vajro P. A 360-degree overview of paediatric NAFLD: recent insights. J Hepatol. 2013;58(6):1218-1229.

[91] Alisi A, Manco M, Vania A, Nobili V. Pediatric nonalcoholic fatty liver disease in 2009. J Pediatr. 2009;155(4):469-474.

[92] Zambrano M, Nikitakis NG, Sanchez-Quevedo MC, Sauk JJ, Sedano H, Rivera H. Oral and dental manifestations of vitamin D-dependent rickets type I: report of a pediatric case. Oral Surg Oral Med Oral Pathol Oral Radiol Endod. 2003;95(6):705-709.

[93] Kaye EK, Chen N, Cabral HJ, Vokonas P, Garcia RI. Metabolic syndrome and periodontal disease progression in men. J Dent Res. 2016;95(7):822-828.

[94] Blasco-Baque V, Garidou L, Pomié C, et al. Periodontitis induced by Porphyromonas gingivalis drives periodontal microbiota dysbiosis and insulin resistance via an impaired adaptive immune response. Gut. 2017;66(5):872-885.

[95] Singer K, Lumeng CN. The initiation of metabolic inflammation in childhood obesity. J Clin Investig. 2017;127(1):65-73.

[96] Nieman DC, Henson DA, Nehlsen-Cannarella SL, et al. Influence of obesity on immune function. J Am Diet Assoc. 1999;99(3):294-299.

[97] Blüher M. Obesity: global epidemiology and pathogenesis. Nat Rev Endocrinol. 2019;15(5):288-298.

[98] Zheng Y, Ley Sylvia H, Hu Frank B. Global aetiology and epidemiology of type 2 diabetes mellitus and its complications. Nat Rev Endocrinol. 2018;14:88-98.

[99] Cawley J. The economics of childhood obesity. Health Aff. 2013;29(3):364-371.

[100] Van den Bossche J, O'Neill LA, Menon D. Macrophage immunometabolism: where are we (going)?Trends Immunol. 2017;38(6):395-406.

[101] Orr JS, Puglisi MJ, Ellacott KL, Lumeng CN, Wasserman DH, Hasty AH. Toll-like receptor 4 deficiency promotes the alternative activation of adipose tissue macrophages. Diabetes. 2012;61(11):2718-2727.

[102] Bruun JM, Lihn AS, Pedersen SB, Richelsen B. Monocyte chemoattractant protein-1 release is higher in visceral than subcutaneous human adipose tissue (AT): implication of macrophages resident in the AT. J Clin Endocrinol Metab. 2005;90(4):2282-2289.

[103] Feingold KR, Soued M, Staprans I, et al. Effect of tumor necrosis factor (TNF) on lipid metabolism in the diabetic rat. Evidence that inhibition of adipose tissue lipoprotein lipase activity is not required for TNF-induced hyperlipidemia. J Clin Invest. 1989;83(4):1116-1121.

[104] Hotamisligil GS, Shargill NS, Spiegelman BM. Adipose expression of tumor necrosis factor-alpha: direct role in obesity-linked insulin resistance. Science. 1993;259(5091):87-91.

[105] Breslin WL, Johnston CA, Strohacker K, et al. Obese Mexican American children have elevated MCP-1, TNF-alpha, monocyte concentration, and dyslipidemia. Pediatrics. 2012;129(5):e1180-e1186.

[106] Olefsky JM, Glass CK. Macrophages, inflammation, and insulin resistance. Annu Rev Physiol. 2010;72(1):219-246.

[107] Rathinam Vijay AK, Fitzgerald Katherine A. Inflammasome complexes: emerging mechanisms and effector functions. Cell. 2016;165(4):792-800.

[108] Lamkanfi M, Dixit Vishva M. Mechanisms and functions of inflammasomes. Cell. 2014;157(5):1013-1022.

[109] Yang H, Youm Y-H, Vandanmagsar B, et al. Obesity accelerates thymic aging. Blood. 2009;114(18):3803-3812.

[110] Kawai T, Autieri MV, Scalia R. Adipose tissue inflammation and metabolic dysfunction in obesity. Am J Physiol Cell Physiol. 2021;320(3):C375-C391.

[111] Wolf Anna M, Wolf D, Rumpold H, Enrich B, Tilg H. Adiponectin induces the anti-inflammatory cytokines IL-10 and IL-1RA in human leukocytes. Biochem Biophys Res Commun. 2004;323(2):630-635.

[112] Ziegler-Heitbrock HW, Wedel A, Schraut W, et al. Tolerance to lipopolysaccharide involves mobilization of nuclear factor kappa B with predominance of p50 homodimers. J Biol Chem. 1994;269(25):17001-17004.

[113] de Candia P, Prattichizzo F, Garavelli S, Alviggi C, La Cava A, Matarese G. The pleiotropic roles of leptin in metabolism, immunity, and cancer. J Exp Med. 2021;218(5):e20191593.

[114] Papathanassoglou E, El-Haschimi K, Li Xian C, Matarese G, Strom T, Mantzoros C. Leptin receptor expression and signaling in lymphocytes: kinetics during lymphocyte activation, role in lymphocyte survival, and response to high fat diet in mice. J Immunol. 2006;176(12):7745-7752.

[115] Loffreda S, Yang SQ, Lin HZ, et al. Leptin regulates proinflammatory immune responses. FASEB J. 1998;12(1):57-65.

[116] Caldefie-Chezet F, Poulin A, Vasson MP. Leptin regulates functional capacities of polymorphonuclear neutrophils. Free Radic Res. 2003;37(8):809-814.

[117] Zhao Y, Sun R, You L, Gao C, Tian Z. Expression of leptin receptors and response to leptin stimulation of human natural killer cell lines. Biochem Biophys Res Commun. 2003;300(2):247-252.

[118] Karlsson EA, Sheridan PA, Beck MA. Diet-induced obesity impairs the T cell memory response to influenza virus infection. J Immunol. 2010;184(6):3127-3133.

[119] Suriano F, Vieira-Silva S, Falony G, et al. Novel insights into the genetically obese (ob/ob) and diabetic (db/db) mice: two sides of the same coin. Microbiome. 2021;9(1):147.

[120] Ilonen J, Lempainen J, Veijola R. The heterogeneous pathogenesis of type 1 diabetes mellitus. Nat Rev Endocrinol. 2019;15(11):635-650.

[121] Salvi GE, Collins JG, Yalda B, Arnold RR, Lang NP, Offenbacher S. Monocytic TNF alpha secretion patterns in IDDM patients with periodontal diseases. J Clin Periodontol. 1997;24(1):8-16.

[122] Karima M, Kantarci A, Ohira T, et al. Enhanced superoxide release and elevated protein kinase C activity in neutrophils from diabetic patients: association with periodontitis. J Leukoc Biol. 2005;78(4):862-870.

[123] Ighbariya A, Weiss R. Insulin resistance, prediabetes, metabolic syndrome: what should every pediatrician know?J Clin Res Pediatr Endocrinol. 2017;9:49-57.

[124] Kotnik P, Fischer PP, Wabitsch M. Endocrine and metabolic effects of adipose tissue in children and adolescents. Zdr Varst. 2015;54(2):131-138.

[125] Hand Timothy W, Vujkovic-Cvijin I, Ridaura Vanessa K, Belkaid Y. Linking the microbiota, chronic disease, and the immune system. Trends Endocrinol Metabol. 2016;27(12):831-843.

[126] Esser N, Legrand-Poels S, Piette J, Scheen AJ, Paquot N. Inflammation as a link between obesity, metabolic syndrome and type 2 diabetes. Diabetes Res Clin Pract. 2014;105:141-150.

[127] Desta T, Li J, Chino T, Graves D. Altered fibroblast proliferation and apoptosis in diabetic gingival wounds. J Dent Res. 2010;89(6):609-614.

[128] Gao L, Xu T, Huang G, Jiang S, Gu Y, Chen F. Oral microbiomes: more and more importance in oral cavity and whole body. Protein Cell. 2018;9(5):488-500.

[129] Feres M, Teles F, Teles R, Figueiredo LC, Faveri M. The subgingival periodontal microbiota of the aging mouth. Periodontol 2000. 2016;72(1):30-53.

[130] Hotamisligil Gökhan S. Inflammation and metabolic disorders. Nature. 2006;444(7121):860-867.

[131] Socransky SS, Haffajee AD, Cugini MA, Smith C, Kent RL. Microbial complexes in subgingival plaque. J Clin Periodontol. 1998;25(2):134-144.

[132] Socransky Sigmund S, Haffajee Anne D. Periodontal microbial ecology. Periodontol 2000. 2005;38(1):135-187.

[133] Jensen Emilija D, Selway Caitlin A, Allen G, et al. Early markers of periodontal disease and altered oral microbiota are associated with glycemic control in children with type 1 diabetes. Pediatr Diabetes. 2021;22(3):474-481.

[134] Mashimo PA, Yamamoto Y, Slots J, Park BH, Genco RJ. The periodontal microflora of juvenile diabetics: culture, immunofluorescence, and serum antibody studies. J Periodontol. 1983;54(7):420-430.

[135] Campus G, Salem A, Uzzau S, Baldoni E, Tonolo G. Diabetes and periodontal disease: a case-control study. J Periodontol. 2005;76(3):418-425.

[136] da Cruz GA, de Toledo S, Sallum EA, et al. Clinical and laboratory evaluations of non-surgical periodontal treatment in subjects with diabetes mellitus. J Periodontol. 2008;79(7):1150-1157.

[137] Ganesan SM, Joshi V, Fellows M, et al. A tale of two risks: smoking, diabetes and the subgingival microbiome. ISME J. 2017;11(9):2075-2089.

[138] Khader Y, Khassawneh B, Obeidat B, et al. Periodontal status of patients with metabolic syndrome compared to those without metabolic syndrome. J Periodontol. 2008;79(11):2048-2053.

[139] Pirih Flavia Q, Monajemzadeh S, Singh N, et al. Association between metabolic syndrome and periodontitis: the role of lipids, inflammatory cytokines, altered host response, and the microbiome. Periodontol 2000. 2021;87(87):50-75.

[140] Vallianou N, Christodoulatos GS, Karampela I, et al. Understanding the role of the gut microbiome and microbial metabolites in non-alcoholic fatty liver disease: current evidence and perspectives. Biomolecules. 2021;12(1):56.

[141] Albillos A, de Gottardi A, Rescigno M. The gut-liver axis in liver disease: pathophysiological basis for therapy. J Hepatol. 2020;72(3):558-577.

[142] Aron-Wisnewsky J, Vigliotti C, Witjes J, et al. Gut microbiota and human NAFLD: disentangling microbial signatures from metabolic disorders. Nat Rev Gastroenterol Hepatol. 2020;17(5):279-297.

[143] Kozarov Emil V, Dorn Brian R, Shelburne Charles E, Dunn WA, Progulske-Fox A. Human atherosclerotic plaque contains viable invasive Actinobacillus actinomycetemcomitans and Porphyromonas gingivalis. Arterioscler Thromb Vasc Biol. 2005;25(3):e17-e18.

[144] Kholy KE, Genco Robert J, Van Dyke TE. Oral infections and cardiovascular disease. Trends Endocrinol Metabol. 2015;26(6):315-321.

[145] Jain A, Batista Eraldo L, Serhan C, Stahl GL, Van Dyke TE. Role for periodontitis in the progression of lipid deposition in an animal model. Infect Immun. 2003;71(10):6012-6018.

[146] Hayashi C, Viereck J, Hua N, et al. Porphyromonas gingivalis accelerates inflammatory atherosclerosis in the innominate artery of ApoE deficient mice. Atherosclerosis. 2011;215(1):52-59.

[147] Miyamoto T, Yumoto H, Takahashi Y, Davey M, Gibson FC, Genco CA. Pathogen-accelerated atherosclerosis occurs early after exposure and can be prevented via immunization. Infect Immun. 2006;74(2):1376-1380.

[148] Graves DT, Corrêa JD, Silva TA. The oral microbiota is modified by systemic diseases. J Dent Res. 2019;98(2):148-156.

[149] De Luca F, Shoenfeld Y. The microbiome in autoimmune diseases. Clin Exp Immunol. 2019;195(1):74-85.

[150] Carrizales-Sepúlveda EF, Ordaz-Farías A, Vera-Pineda R, Flores-Ramírez R. Periodontal disease, systemic inflammation and the risk of cardiovascular disease. Heart Lung Circ. 2018;27(11):1327-1334.

[151] Bartova J, Sommerova P, Lyuya-Mi Y, et al. Periodontitis as a risk factor of atherosclerosis. J Immunol Res. 2014;2014:636893-636899.

[152] Chaves IdeM, Zicker MC, Laranjeira AdeO, et al. Dysbiotic oral microbiota contributes to alveolar bone loss associated with obesity in mice. J Appl Oral Sci. 2022;30:e20220238.

[153] Botero JE, Rodriguez C, Agudelo-Suarez AA. Periodontal treatment and glycaemic control in patients with diabetes and periodontitis: an umbrella review. Aust Dent J. 2016;61(2):134-148.

[154] Scheithauer Torsten PM, Rampanelli E, Nieuwdorp M, et al. Gut microbiota as a trigger for metabolic inflammation in obesity and type 2 diabetes. Front Immunol. 2020;11:571731.

[155] Simpson TC, Weldon JC, Worthington HV, et al. Treatment of periodontal disease for glycaemic control in people with diabetes mellitus. Cochrane Database Syst Rev. 2015;11(3):CD004714.

[156] Faggion CM, Jr, Cullinan MP, Atieh M. An overview of systematic reviews on the effectiveness of periodontal treatment to improve glycaemic control. J Periodontal Res. 2016;51(6):716-725.

[157] Wang TF, Jen IA, Chou C, Lei YP. Effects of periodontal therapy on metabolic control in patients with type 2 diabetes mellitus and periodontal disease: a meta-analysis. Medicine. 2014;93(28):e292.

[158] Di Paola R, Mazzon E, Maiere D, et al. Rosiglitazone reduces the evolution of experimental periodontitis in the rat. J Dent Res. 2006;85(2):156-161.

[159] Hassumi MY, Silva-Filho VJ, Campos-Junior JC, et al. PPAR-gamma agonist rosiglitazone prevents inflammatory periodontal bone loss by inhibiting osteoclastogenesis. Int Immunopharm. 2009;9(10):1150-1158.

[160] Mackler SB, Crawford JJ. Plaque development and gingivitis in the primary dentition. J Periodontol. 1973;44(1):18-24.

[161] Matsson L. Development of gingivitis in the preschool children and young adults. J Clin Periodontol. 1978;5(1):24-34.

[162] Bimstein E, Matsson L, Soskolne AW, Lustmann J. Histologic characteristics of the gingiva associated with the primary and permanent teeth of children. Pediatr Dent. 1994;3:206-210.

[163] Tonetti MS, Mombelli A. Early-onset periodontitis. Ann Periodontol. 1999;4(1):39-52.

[164] Watanabe K. Prepubertal periodontitis: a review of diagnostic criteria, pathogenesis, and differential diagnosis. J Periodontal Res. 1990;25(1):31-48.

[165] Burcham Zachary M, Garneau Nicole L, Comstock Sarah S, et al. Patterns of oral microbiota diversity in adults and children: a crowdsourced population study. Sci Rep. 2020;10(1):2133.

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