The Complex Interrelationship between Diabetes Mellitus, Oral Diseases and General Health

Article ID: e220321192408 Pages: 15

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Abstract

There is emerging evidence that several oral diseases and conditions can be associated with DM. Dental caries, hyposalivation, fungal diseases and endodontics lesions may represent potential oral complications that can be aggravated by chronic hyperglycemia. Individuals with DM have a low perception of oral diseases which can lead to clinically important oral and systemic complications. This review aims to provide data on the most common oral signs and symptoms related to DM and to explore the mechanisms that might explain associations between DM and oral diseases in order to clarify the risks posed by poor oral health in DM. Since the linkage between oral diseases and DM is part of multifactorial aspects related to chronic hyperglycemic status and several common conditions affecting the whole body, both require rigorous self-control from patients and attention from medical and dental professionals.

Keywords: Diabetes mellitus, oral health, hyperglycemia, oral diseases, health care, dental diseases.

[1]
Lalla E. Periodontal infections and diabetes mellitus: when will the puzzle be complete? J Clin Periodontol 2007; 34(11): 913-6.
[http://dx.doi.org/10.1111/j.1600-051X.2007.01140.x] [PMID: 17935499]
[2]
Macpherson P. The effect of diabetes on oral and systemic health. 2014; 196-202: Corpus ID: 71585432.
[3]
GBD 2017 Disease and Injury Incidence and Prevalence Collaborators. Global, regional, and national incidence, prevalence, and years lived with disability for 354 diseases and injuries for 195 countries and territories, 1990-2017: a systematic analysis for the Global Burden of Disease Study 2017. Lancet 2018; 392(10159): 1789-858.
[http://dx.doi.org/10.1016/S0140-6736(18)32279-7] [PMID: 30496104]
[4]
Lin J, Thompson TJ, Cheng YJ, et al. Projection of the future diabetes burden in the United States through 2060. Popul Health Metr 2018; 16(1): 9.
[http://dx.doi.org/10.1186/s12963-018-0166-4] [PMID: 29903012]
[5]
Mauri-Obradors E, Estrugo-Devesa A, Jané-Salas E, Viñas M, López-López J. Oral manifestations of diabetes mellitus. A systematic review. Med Oral Patol Oral Cir Bucal 2017; 22(5): e586-94.
[http://dx.doi.org/10.4317/medoral.21655] [PMID: 28809366]
[6]
Löe H. Periodontal disease. The sixth complication of diabetes mellitus. Diabetes Care 1993; 16(1): 329-34.
[http://dx.doi.org/10.2337/diacare.16.1.329] [PMID: 8422804]
[7]
Kogawa EM, Grisi DC, Falcão DP, et al. Salivary function impairment in type 2 Diabetes patients associated with concentration and genetic polymorphisms of chromogranin A. Clin Oral Investig 2016; 20(8): 2083-95.
[http://dx.doi.org/10.1007/s00784-015-1705-z] [PMID: 26750135]
[8]
Genco RJ, Schifferle RE, Dunford RG, Falkner KL, Hsu WC, Balukjian J. Screening for diabetes mellitus in dental practices: a field trial. J Am Dent Assoc 2014; 145(1): 57-64.
[http://dx.doi.org/10.14219/jada.2013.7] [PMID: 24379330]
[9]
International Diabetes Federation IDF Diabetes Atlas, 9th edn 2019. Available at: https://www.diabetesatlas.org
[10]
Chinnasamy A, Moodie M. Prevalence of undiagnosed diabetes and prediabetes in the dental setting: a systematic review and meta-analysis. Int J Dent 2020; 2020: 2964020.
[http://dx.doi.org/10.1155/2020/2964020] [PMID: 32908510]
[11]
Borrell LN, Kunzel C, Lamster I, Lalla E. Diabetes in the dental office: using NHANES III to estimate the probability of undiagnosed disease. J Periodontal Res 2007; 42(6): 559-65.
[http://dx.doi.org/10.1111/j.1600-0765.2007.00983.x] [PMID: 17956470]
[12]
Lalla E, Kunzel C, Burkett S, Cheng B, Lamster IB. Identification of unrecognized diabetes and pre-diabetes in a dental setting. J Dent Res 2011; 90(7): 855-60.
[http://dx.doi.org/10.1177/0022034511407069] [PMID: 21531917]
[13]
AlGhamdi AST, Bukhari SMN, Elias WY, Merdad K, Sonbul H. Dental clinics as potent sources for screening undiagnosed diabetes and prediabetes. Am J Med Sci 2013; 345(4): 331-4.
[http://dx.doi.org/10.1097/MAJ.0b013e318287c96c] [PMID: 23531966]
[14]
Strauss SM, Rosedale MT, Pesce MA, et al. The potential for glycemic control monitoring and screening for diabetes at dental visits using oral blood. Am J Public Health 2015; 105(4): 796-801.
[http://dx.doi.org/10.2105/AJPH.2014.302357] [PMID: 25713975]
[15]
Buset SL, Walter C, Friedmann A, Weiger R, Borgnakke WS, Zitzmann NU. Are periodontal diseases really silent? A systematic review of their effect on quality of life. J Clin Periodontol 2016; 43(4): 333-44.
[http://dx.doi.org/10.1111/jcpe.12517] [PMID: 26810308]
[16]
Chapple ILC, Bouchard P, Cagetti MG, et al. Interaction of lifestyle, behaviour or systemic diseases with dental caries and periodontal diseases: consensus report of group 2 of the joint EFP/ORCA workshop on the boundaries between caries and periodontal diseases. J Clin Periodontol 2017; 44(Suppl. 18): S39-51.
[http://dx.doi.org/10.1111/jcpe.12685] [PMID: 28266114]
[17]
Masood M, Newton T, Bakri NN, Khalid T, Masood Y. The relationship between oral health and oral health related quality of life among elderly people in United Kingdom. J Dent 2017; 56: 78-83.
[http://dx.doi.org/10.1016/j.jdent.2016.11.002] [PMID: 27825838]
[18]
Papapanou PN, Sanz M, Buduneli N, 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(Suppl. 1): S173-82.
[http://dx.doi.org/10.1002/JPER.17-0721] [PMID: 29926951]
[19]
Caton JG, Armitage G, Berglundh T, et al. A new classification scheme for periodontal and peri-implant diseases and conditions - Introduction and key changes from the 1999 classification. J Periodontol 2018; 89(Suppl. 1): S1-8.
[http://dx.doi.org/10.1002/JPER.18-0157] [PMID: 29926946]
[20]
Albandar JM, Susin C, Hughes FJ. Manifestations of systemic diseases and conditions that affect the periodontal attachment apparatus: Case definitions and diagnostic considerations. J Periodontol 2018; 89(Suppl. 1): S183-203.
[http://dx.doi.org/10.1002/JPER.16-0480] [PMID: 29926941]
[21]
Newman M, Takei H, Klokkevold P, et al. Carranza periodontia clínica.11th ed. Rio de Janeiro: Elsevier 2012.
[22]
Demmer RT, Squillaro A, Papapanou PN, et al. Periodontal infection, systemic inflammation, and insulin resistance: results from the continuous National Health and Nutrition Examination Survey (NHANES) 1999-2004. Diabetes Care 2012; 35(11): 2235-42.
[http://dx.doi.org/10.2337/dc12-0072] [PMID: 22837370]
[23]
Chapple ILC, Genco R. Working Grp 2 Joint EFPAAPW. Diabetes and periodontal diseases: consensus report of the Joint EFP/AAP Workshop on Periodontitis and Systemic Diseases. J Periodontol 2013; 84(4): S106-2.
[PMID: 23631572]
[24]
Sanz M, Ceriello A, Buysschaert M, et al. Scientific evidence on the links between periodontal diseases and diabetes: Consensus report and guidelines of the joint workshop on periodontal diseases and diabetes by the International Diabetes Federation and the European Federation of Periodontology. J Clin Periodontol 2018; 45(2): 138-49.
[http://dx.doi.org/10.1111/jcpe.12808] [PMID: 29280174]
[25]
Shlossman M, Knowler WC, Pettitt DJ, Genco RJ. Type 2 diabetes mellitus and periodontal disease. J Am Dent Assoc 1990; 121(4): 532-6.
[http://dx.doi.org/10.14219/jada.archive.1990.0211] [PMID: 2212346]
[26]
Nascimento GG, Leite FRM, Vestergaard P, Scheutz F, López R. Does diabetes increase the risk of periodontitis? A systematic review and meta-regression analysis of longitudinal prospective studies. Acta Diabetol 2018; 55(7): 653-67.
[http://dx.doi.org/10.1007/s00592-018-1120-4] [PMID: 29502214]
[27]
Genco RJ, Borgnakke WS. Diabetes as a potential risk for periodontitis: association studies. Periodontol 2000 2020; 83(1): 40-5.
[http://dx.doi.org/10.1111/prd.12270] [PMID: 32385881]
[28]
Mealey BL, Oates TW. American Academy of Periodontology. Diabetes mellitus and periodontal diseases. J Periodontol 2006; 77(8): 1289-303.
[http://dx.doi.org/10.1902/jop.2006.050459] [PMID: 16881798]
[29]
Ajita M, Karan P, Vivek G, S MA, Anuj M. Periodontal disease and type 1 diabetes mellitus: associations with glycemic control and complications: an Indian perspective. Diabetes Metab Syndr 2013; 7(2): 61-3.
[http://dx.doi.org/10.1016/j.dsx.2013.03.001] [PMID: 23680241]
[30]
Taylor GW, Burt BA, Becker MP, Genco RJ, Shlossman M, Knowler WC, et al. Severe periodontitis and risk for poor glycemic control in patients with non-insulin-dependent diabetes mellitus. J Periodontol 1996; 67(10)(Suppl.): 1085-93.
[http://dx.doi.org/10.1902/jop.1996.67.10s.1085]
[31]
Kocher T, König J, Borgnakke WS, Pink C, Meisel P. Periodontal complications of hyperglycemia/diabetes mellitus: Epidemiologic complexity and clinical challenge. Periodontol 2000 2018; 78(1): 59-97.
[http://dx.doi.org/10.1111/prd.12235] [PMID: 30198134]
[32]
Silvestre FJ, Miralles L, Llambes F, Bautista D, Solá-Izquierdo E, Hernández-Mijares A. Type 1 diabetes mellitus and periodontal disease: relationship to different clinical variables. Med Oral Patol Oral Cir Bucal 2009; 14(4): E175-9.
[PMID: 19300353]
[33]
Jimenez M, Hu FB, Marino M, Li Y, Joshipura KJ. Type 2 diabetes mellitus and 20 year incidence of periodontitis and tooth loss. Diabetes Res Clin Pract 2012; 98(3): 494-500.
[http://dx.doi.org/10.1016/j.diabres.2012.09.039] [PMID: 23040240]
[34]
Tsai C, Hayes C, Taylor GW. Glycemic control of type 2 diabetes and severe periodontal disease in the US adult population. Community Dent Oral Epidemiol 2002; 30(3): 182-92.
[http://dx.doi.org/10.1034/j.1600-0528.2002.300304.x] [PMID: 12000341]
[35]
Graziani F, Gennai S, Solini A, Petrini M. A systematic review and meta-analysis of epidemiologic observational evidence on the effect of periodontitis on diabetes An update of the EFP-AAP review. J Clin Periodontol 2018; 45(2): 167-87.
[http://dx.doi.org/10.1111/jcpe.12837] [PMID: 29277926]
[36]
Taylor JJ, Preshaw PM, Lalla E. A review of the evidence for pathogenic mechanisms that may link periodontitis and diabetes. J Periodontol 2013; 84(4)(Suppl.): S113-34.
[PMID: 23631573]
[37]
Miranda TS, Feres M, Retamal-Valdés B, Perez-Chaparro PJ, Maciel SS, Duarte PM. Influence of glycemic control on the levels of subgingival periodontal pathogens in patients with generalized chronic periodontitis and type 2 diabetes. J Appl Oral Sci 2017; 25(1): 82-9.
[http://dx.doi.org/10.1590/1678-77572016-0302] [PMID: 28198980]
[38]
Longo PL, Dabdoub S, Kumar P, et al. Glycaemic status affects the subgingival microbiome of diabetic patients. J Clin Periodontol 2018; 45(8): 932-40.
[http://dx.doi.org/10.1111/jcpe.12908] [PMID: 29742293]
[39]
Engebretson S, Kocher T. Evidence that periodontal treatment improves diabetes outcomes: a systematic review and meta-analysis. J Periodontol 2013; 84(4): S153-63.
[PMID: 23631575]
[40]
Borgnakke WS, Chapple IL, Genco RJ, et al. The multi-center randomized controlled trial (RCT) published by the journal of the American Medical Association (JAMA) on the effect of periodontal therapy on glycated hemoglobin (HbA1c) has fundamental problems. J Evid Based Dent Pract 2014; 14(3): 127-32.
[http://dx.doi.org/10.1016/j.jebdp.2014.04.017] [PMID: 25234213]
[41]
Cao R, Li Q, Wu Q, Yao M, Chen Y, Zhou H. Effect of non-surgical periodontal therapy on glycemic control of type 2 diabetes mellitus: a systematic review and Bayesian network meta-analysis. BMC Oral Health 2019; 19(1): 176.
[http://dx.doi.org/10.1186/s12903-019-0829-y] [PMID: 31387569]
[42]
Group UPDU. In: Intensive blood-glucose control with sulphonylureas or insulin compared with conventional treatment and risk of complications in patients with type 2 diabetes (UKPDS 33). 1998; pp. 837-53.
[43]
Ben-Aryeh H, Cohen M, Kanter Y, Szargel R, Laufer D. Salivary composition in diabetic patients. J Diabet Complications 1988; 2(2): 96-9.
[http://dx.doi.org/10.1016/0891-6632(88)90011-6] [PMID: 2458369]
[44]
Chavez EM, Taylor GW, Borrell LN, Ship JA. Salivary function and glycemic control in older persons with diabetes. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2000; 89(3): 305-11.
[http://dx.doi.org/10.1016/S1079-2104(00)70093-X] [PMID: 10710454]
[45]
Mata AD, Marques D, Rocha S, et al. Effects of diabetes mellitus on salivary secretion and its composition in the human. Mol Cell Biochem 2004; 261(1-2): 137-42.
[http://dx.doi.org/10.1023/B:MCBI.0000028748.40917.6f] [PMID: 15362496]
[46]
Bernardi MJ, Reis A, Loguercio AD, Kehrig R, Leite MF, Nicolau J. Study of the buffering capacity, pH and salivary flow rate in type 2 well-controlled and poorly controlled diabetic patients. Oral Health Prev Dent 2007; 5(1): 73-8.
[PMID: 17366764]
[47]
Kogawa EM, Grisi DC, Falcão DP, et al. Impact of glycemic control on oral health status in type 2 diabetes individuals and its association with salivary and plasma levels of chromogranin A. Arch Oral Biol 2016; 62: 10-9.
[http://dx.doi.org/10.1016/j.archoralbio.2015.11.005] [PMID: 26605682]
[48]
Navea Aguilera C, Guijarro de Armas MG, Monereo Megías S, Merino Viveros M, Torán Ranero C. The relationship between xerostomia and diabetes mellitus: a little known complication. Endocrinol Nutr 2015; 62(1): 45-6.
[http://dx.doi.org/10.1016/j.endonu.2014.09.004] [PMID: 25458402]
[49]
Aitken-Saavedra J, Rojas-Alcayaga G, Maturana-Ramírez A, et al. Salivary gland dysfunction markers in type 2 diabetes mellitus patients. J Clin Exp Dent 2015; 7(4): e501-5.
[http://dx.doi.org/10.4317/jced.52329] [PMID: 26535097]
[50]
von Bültzingslöwen I, Sollecito TP, Fox PC, et al. Salivary dysfunction associated with systemic diseases: systematic review and clinical management recommendations. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2007; 103 Suppl: S57.e1-S57.e15.
[http://dx.doi.org/10.1016/j.tripleo.2006.11.010]
[51]
Guggenheimer J, Moore PA. Xerostomia: etiology, recognition and treatment. J Am Dent Assoc 2003; 134(1): 61-9.
[http://dx.doi.org/10.14219/jada.archive.2003.0018] [PMID: 12555958]
[52]
Verhulst MJL, Loos BG, Gerdes VEA, Teeuw WJ. Evaluating all potential oral complications of diabetes mellitus. Front Endocrinol (Lausanne) 2019; 10: 56.
[http://dx.doi.org/10.3389/fendo.2019.00056] [PMID: 30962800]
[53]
Villa A, Connell CL, Abati S. Diagnosis and management of xerostomia and hyposalivation. Ther Clin Risk Manag 2014; 11: 45-51.
[http://dx.doi.org/10.2147/TCRM.S76282] [PMID: 25653532]
[54]
Negrato CA, Tarzia O. Buccal alterations in diabetes mellitus. Diabetol Metab Syndr 2010; 2: 3.
[http://dx.doi.org/10.1186/1758-5996-2-3] [PMID: 20180965]
[55]
Xiang RL, Huang Y, Zhang Y, et al. Type 2 diabetes-induced hyposalivation of the submandibular gland through PINK1/Parkin- mediated mitophagy. J Cell Physiol 2020; 235(1): 232-44.
[http://dx.doi.org/10.1002/jcp.28962] [PMID: 31190343]
[56]
Silva MF, Barbosa KG, Pereira JV, Bento PM, Godoy GP, Gomes DQ. Prevalence of oral mucosal lesions among patients with diabetes mellitus types 1 and 2. An Bras Dermatol 2015; 90(1): 49-53.
[http://dx.doi.org/10.1590/abd1806-4841.20153089] [PMID: 25672299]
[57]
López-Pintor RM, Casañas E, González-Serrano J, et al. Xerostomia, hyposalivation, and salivary flow in diabetes patients. J Diabetes Res 2016; 2016: 4372852.
[http://dx.doi.org/10.1155/2016/4372852] [PMID: 27478847]
[58]
Panchbhai AS, Degwekar SS, Bhowte RR. Estimation of salivary glucose, salivary amylase, salivary total protein and salivary flow rate in diabetics in India. J Oral Sci 2010; 52(3): 359-68.
[http://dx.doi.org/10.2334/josnusd.52.359] [PMID: 20881327]
[59]
Berti-Couto SdA, Couto-Souza PH, Jacobs R, et al. Clinical diagnosis of hyposalivation in hospitalized patients. J Appl Oral Sci 2012.
[60]
Li YH, Sun P, Guo JC. Clinical analysis of diabetic combined pulmonary mucormycosis. Mycopathologia 2017; 182(11-12): 1111-7.
[http://dx.doi.org/10.1007/s11046-017-0167-z] [PMID: 28667347]
[61]
Simões RJ, Fonseca P, Figueiral MH. Infecções por candida spp na cavidade oral. OdontolClín-Cien 2013; 12(1) (online)
[62]
Yamashita JM. Moura-grec pgd, capelari mm, sales-peres a, sales-peres shdc. manifestações bucais em pacientes portadores de diabetes mellitus: uma revisão sistemática. Rev Odontol UNESP 2013; 43(3): 211-20.
[http://dx.doi.org/10.1590/S1807-25772013000300011]
[63]
Prado BN, Vaccarezza GF. Alterações Bucais em Pacientes Diabéticos.Rev Odontol Univ Cid São Paulo. 2013; pp. 147-53.
[64]
Vernillo AT. Dental considerations for the treatment of patients with diabetes mellitus. J Am Dent Assoc 2003; 134(Spec No): 24S-33S.
[http://dx.doi.org/10.14219/jada.archive.2003.0366] [PMID: 18196670]
[65]
Bremenkamp RM, Caris AR, Jorge AO, et al. Prevalence and antifungal resistance profile of Candida spp. oral isolates from patients with type 1 and 2 diabetes mellitus. Arch Oral Biol 2011; 56(6): 549-55.
[http://dx.doi.org/10.1016/j.archoralbio.2010.11.018] [PMID: 21183157]
[66]
Trentin MS, Verardi G, De C Ferreira M, et al. Most frequent oral lesions in patients with type 2 diabetes mellitus. J Contemp Dent Pract 2017; 18(2): 107-11.
[http://dx.doi.org/10.5005/jp-journals-10024-1999] [PMID: 28174362]
[67]
Vasconcelos BCdE. Prevalência das alterações da mucosa bucal em pacientes diabéticos: estudo preliminar. Rev Bras Otorrinolaringol 2008; 423-8.
[68]
Gome SCC, Guimarã ESLS, Pinto LCC. Camargo Gadcg, Valente MIB, Sarquis MIdM. Investigations of the prevalence and virulence of Candida albicans in periodontal and endodontic lesions in diabetic and normoglycemic patients. J Appl Oral Sci 2017; 25(3): 274-81.
[69]
Contaldo M, Romano A, Mascitti M, Fiori F, Della Vella F, Serpico R, et al. Association between denture stomatitis, cândida species and diabetic status.J Biol Regul Homeost Agent 2019; 35-41.
[70]
Dorko E, Jenca A, Pilipcinec E, Danko J, Svický E, Tkáciková L. Candida-associated denture stomatitis. Folia Microbiol (Praha) 2001; 46(5): 443-6.
[http://dx.doi.org/10.1007/BF02814436] [PMID: 11899479]
[71]
Olczak-Kowalczyk D, Pyrżak B, Dąbkowska M, et al. Candida spp. and gingivitis in children with nephrotic syndrome or type 1 diabetes. BMC Oral Health 2015; 15: 57.
[http://dx.doi.org/10.1186/s12903-015-0042-6] [PMID: 25952029]
[72]
Nezafati S, Kazemi A, Asgari K, Bahrami A, Naghili B, Yazdani J. Rhinocerebral mucormycosis, risk factors and the type of oral manifestations in patients referred to a University Hospital in Tabriz, Iran 2007-2017. Mycoses 2018; 61(10): 764-9.
[http://dx.doi.org/10.1111/myc.12802] [PMID: 29896908]
[73]
Saravia-Flores M, Guaran DM, Argueta V. Invasive cutaneous infection caused by Apophysomyces elegans associated with a spider bite. Mycoses 2010; 53(3): 259-61.
[http://dx.doi.org/10.1111/j.1439-0507.2009.01698.x] [PMID: 19389070]
[74]
Kassebaum NJ, Bernabé E, Dahiya M, Bhandari B, Murray CJ, Marcenes W. Global burden of untreated caries: a systematic review and metaregression. J Dent Res 2015; 94(5): 650-8.
[http://dx.doi.org/10.1177/0022034515573272] [PMID: 25740856]
[75]
Garton BJ, Ford PJ. Root caries and diabetes: risk assessing to improve oral and systemic health outcomes. Aust Dent J 2012; 57(2): 114-22.
[http://dx.doi.org/10.1111/j.1834-7819.2012.01690.x] [PMID: 22624749]
[76]
Naseri R, Mozaffari HR, Ramezani M, Sadeghi M. Effect of diabetes mellitus type 2 on salivary glucose, immunoglobulin A, total protein, and amylase levels in adults: A systematic review and meta-analysis of case-control studies. J Res Med Sci 2018; 23: 89.
[http://dx.doi.org/10.4103/jrms.JRMS_135_18] [PMID: 30505327]
[77]
Goodson JM, Hartman ML, Shi P, et al. The salivary microbiome is altered in the presence of a high salivary glucose concentration. PLoS One 2017; 12(3): e0170437.
[http://dx.doi.org/10.1371/journal.pone.0170437] [PMID: 28249034]
[78]
Jawed M, Shahid SM, Qader SA, Azhar A. Dental caries in diabetes mellitus: role of salivary flow rate and minerals. J Diabetes Complications 2011; 25(3): 183-6.
[http://dx.doi.org/10.1016/j.jdiacomp.2010.07.001] [PMID: 20801061]
[79]
Albrecht M, Bánóczy J, Tamás G Jr. Dental and oral symptoms of diabetes mellitus. Community Dent Oral Epidemiol 1988; 16(6): 378-80.
[http://dx.doi.org/10.1111/j.1600-0528.1988.tb00586.x] [PMID: 3203498]
[80]
Blanco JJA, Villar BB, Martinez EJ. Pilar, Vallejo S, Blanco FJA. Problemas bucodentales en pacientes con diabetes mellitus. I: Índice de placa y caries dental. Med Oral 2003; 97-109.
[81]
Iqbal S, Kazmi F, Asad S, Mumtaz M, Khan AA. Dental caries and diabetes mellitus. Pak Oral Dent J 2011; 31(3): 60-3.
[82]
Bacić M, Ciglar I, Granić M, Plancak D, Sutalo J. Dental status in a group of adult diabetic patients. Community Dent Oral Epidemiol 1989; 17(6): 313-6.
[http://dx.doi.org/10.1111/j.1600-0528.1989.tb00645.x] [PMID: 2591185]
[83]
Bharateesh J, Ahmed M, Kokila G. Diabetes and oral health: a case-control study. Int J Prev Med 2012; 3(11): 806-9.
[PMID: 23189233]
[84]
Lin BP, Taylor GW, Allen DJ, Ship JA. Dental caries in older adults with diabetes mellitus. Spec Care Dentist 1999; 19(1): 8-14.
[http://dx.doi.org/10.1111/j.1754-4505.1999.tb01361.x] [PMID: 10483454]
[85]
Seethalakshmi C, Reddy RC, Asifa N, Prabhu S. Correlation of salivary pH, incidence of dental caries and periodontal status in diabetes mellitus patients: A cross-sectional study. J Clin Diagn Res 2016; 10(3): ZC12-4.
[http://dx.doi.org/10.7860/JCDR/2016/16310.7351] [PMID: 27134992]
[86]
Ramana DPV, Rao VUM. Status of periodontal diseases and dental caries among type -2 diabetic and non-diabetic patients. Res J Pharm Biol Chem Sci 2014; 5: 1251-60.
[87]
Tanriverdi O, Ayman D, Turker NBK. Investigation of prosthesis complications in diabetics and determination of prognosis of gingival diseases and dental caries.2006; 50-4.
[88]
Hintao J, Teanpaisan R, Chongsuvivatwong V, Ratarasan C, Dahlen G. The microbiological profiles of saliva, supragingival and subgingival plaque and dental caries in adults with and without type 2 diabetes mellitus. Oral Microbiol Immunol 2007; 22(3): 175-81.
[http://dx.doi.org/10.1111/j.1399-302X.2007.00341.x] [PMID: 17488443]
[89]
Cherry-Peppers G, Ship JA. Oral health in patients with type II diabetes and impaired glucose tolerance. Diabetes Care 1993; 16(4): 638-41.
[http://dx.doi.org/10.2337/diacare.16.4.638] [PMID: 8462394]
[90]
Soni S, Mehta M, M AD, et al. Root caries among type 2 diabetes mellitus patients visiting a hospital. Spec Care Dentist 2014; 34(6): 273-7.
[http://dx.doi.org/10.1111/scd.12065] [PMID: 24612224]
[91]
Do T, Damé-Teixeira N, Naginyte M, Marsh PD. Root Surface Biofilms and Caries. Monogr Oral Sci 2017; 26: 26-34.
[http://dx.doi.org/10.1159/000479304] [PMID: 29050018]
[92]
Machado D, Coelho A, Paula A, et al. Prevalência de Lesões de Cárie de Doentes com Diabetes Mellitus Tipo 1 Tratados com Múltiplas Administrações de Insulina e de Indivíduos sem Diabetes. Acta Med Port 2017; 30(5): 402.
[http://dx.doi.org/10.20344/amp.8050]
[93]
Malvania EA, Sheth SA, Sharma AS, Mansuri S, Shaikh F, Sahani S. Dental caries prevalence among type II diabetic and nondiabetic adults attending a hospital. J Int Soc Prev Community Dent 2016; 6(Suppl. 3): S232-6.
[http://dx.doi.org/10.4103/2231-0762.197202] [PMID: 28217542]
[94]
Malicka B, Kaczmarek U. Periodontal condition in adult patients with diabetes mellitus type 1 and 2. Dental and Medical Problems 2011; 48(2): 198-207.
[95]
Mohamed HG, Idris SB, Ahmed MF, et al. Association between oral health status and type 2 diabetes mellitus among Sudanese adults: a matched case-control study. PLoS One 2013; 8(12): e82158.
[http://dx.doi.org/10.1371/journal.pone.0082158] [PMID: 24349205]
[96]
Pachoński M, Jarosz-Chobot P, Koczor-Rozmus A, Łanowy P, Mocny-Pachońska K. Dental caries and periodontal status in children with type 1 diabetes mellitus. Pediatr Endocrinol Diabetes Metab 2020; 26(1): 39-44.
[http://dx.doi.org/10.5114/pedm.2020.93249] [PMID: 32272827]
[97]
de Lima AKA, Amorim Dos Santos J, Stefani CM, Almeida de Lima A, Damé-Teixeira N. Diabetes mellitus and poor glycemic control increase the occurrence of coronal and root caries: a systematic review and meta-analysis. Clin Oral Investig 2020; 24(11): 3801-12.
[http://dx.doi.org/10.1007/s00784-020-03531-x] [PMID: 32829477]
[98]
Arya S, Duhan J, Tewari S, Sangwan P, Ghalaut V, Aggarwal S. Healing of apical periodontitis after nonsurgical treatment in patients with type 2 diabetes. J Endod 2017; 43(10): 1623-7.
[http://dx.doi.org/10.1016/j.joen.2017.05.013] [PMID: 28803674]
[99]
Segura-Egea JJ, Martín-González J, Cabanillas-Balsera D, Fouad AF, Velasco-Ortega E, López-López J. Association between diabetes and the prevalence of radiolucent periapical lesions in root- filled teeth: systematic review and meta-analysis. Clin Oral Investig 2016; 20(6): 1133-41.
[http://dx.doi.org/10.1007/s00784-016-1805-4] [PMID: 27055847]
[100]
Sasaki H, Hirai K, Martins CM, Furusho H, Battaglino R, Hashimoto K. Interrelationship between periapical lesion and systemic metabolic disorders. Curr Pharm Des 2016; 22(15): 2204-15.
[http://dx.doi.org/10.2174/1381612822666160216145107] [PMID: 26881444]
[101]
Segura-Egea JJ, Castellanos-Cosano L, Machuca G, et al. Diabetes mellitus, periapical inflammation and endodontic treatment outcome. Med Oral Patol Oral Cir Bucal 2012; 17(2): e356-61.
[http://dx.doi.org/10.4317/medoral.17452] [PMID: 22143698]
[102]
Nayak M, Kotigadde S, Shetty H. R V DV, Antony B. Impact of peptostreptococcus on type 2 diabetes mellitus related secondary root canal infections. Int J Pharm Sci Res 2013; 4: 4001-9.
[103]
Fouad AF. Diabetes mellitus as a modulating factor of endodontic infections. J Dent Educ 2003; 67(4): 459-67.
[http://dx.doi.org/10.1002/j.0022-0337.2003.67.4.tb03647.x] [PMID: 12749575]
[104]
Pishipati V. Diabetes mellitus: An endodontic perspective. Eur J Gen Dent 2013; 2: 241.
[http://dx.doi.org/10.4103/2278-9626.115996]
[105]
Lima SMF, Grisi DC, Kogawa EM, et al. Diabetes mellitus and inflammatory pulpal and periapical disease: a review. Int Endod J 2013; 46(8): 700-9.
[http://dx.doi.org/10.1111/iej.12072] [PMID: 23442003]
[106]
Marotta PS, Fontes TV, Armada L, Lima KC, Rôças IN, Siqueira JF Jr. Type 2 diabetes mellitus and the prevalence of apical periodontitis and endodontic treatment in an adult Brazilian population. J Endod 2012; 38(3): 297-300.
[http://dx.doi.org/10.1016/j.joen.2011.11.001] [PMID: 22341063]
[107]
Limeira FIR, Arantes DC, de Souza Oliveira C, de Melo DP, Magalhães CS, Bento PM. Root canal treatment and apical periodontitis in a brazilian population with type 1 diabetes mellitus: a cross-sectional paired study. J Endod 2020; 46(6): 756-62.
[http://dx.doi.org/10.1016/j.joen.2020.02.010] [PMID: 32299700]
[108]
López-López J, Jané-Salas E, Estrugo-Devesa A, Velasco-Ortega E, Martín-González J, Segura-Egea JJ. Periapical and endodontic status of type 2 diabetic patients in Catalonia, Spain: a cross-sectional study. J Endod 2011; 37(5): 598-601.
[http://dx.doi.org/10.1016/j.joen.2011.01.002] [PMID: 21496655]
[109]
Ruiz XF, Duran-Sindreu F, Shemesh H, et al. Development of periapical lesions in endodontically treated teeth with and without periodontal involvement: a retrospective cohort study. J Endod 2017; 43(8): 1246-9.
[http://dx.doi.org/10.1016/j.joen.2017.03.037] [PMID: 28606666]
[110]
Vasconcelos AC, Soares MS, Almeida PC, Soares TC. Comparative study of the concentration of salivary and blood glucose in type 2 diabetic patients. J Oral Sci 2010; 52(2): 293-8.
[http://dx.doi.org/10.2334/josnusd.52.293] [PMID: 20587956]
[111]
Damé-Teixeira N, Parolo CCF, Maltz M. Spec2367. Monogr Oral Sci 2017; 26: 15-25.
[http://dx.doi.org/10.1159/000479303] [PMID: 29050017]
[112]
Marsh PD, Do T, Beighton D, Devine DA. Influence of saliva on the oral microbiota. Periodontol 2000 2016; 70(1): 80-92.
[http://dx.doi.org/10.1111/prd.12098] [PMID: 26662484]
[113]
IDF. International Diabetes Federation. Diabetes Mellitus 2014.
[114]
Sonnenschein SK, Meyle J. Local inflammatory reactions in patients with diabetes and periodontitis. Periodontol 2000 2015; 69(1): 221-54.
[http://dx.doi.org/10.1111/prd.12089] [PMID: 26252411]
[115]
Hasturk H, Kantarci A. Activation and resolution of periodontal inflammation and its systemic impact. Periodontol 2000 2015; 69(1): 255-73.
[http://dx.doi.org/10.1111/prd.12105] [PMID: 26252412]
[116]
Singh VP, Bali A, Singh N, Jaggi AS. Advanced glycation end products and diabetic complications. Korean J Physiol Pharmacol 2014; 18(1): 1-14.
[http://dx.doi.org/10.4196/kjpp.2014.18.1.1] [PMID: 24634591]
[117]
Katz J, Bhattacharyya I, Farkhondeh-Kish F, Perez FM, Caudle RM, Heft MW. Expression of the receptor of advanced glycation end products in gingival tissues of type 2 diabetes patients with chronic periodontal disease: a study utilizing immunohistochemistry and RT-PCR. J Clin Periodontol 2005; 32(1): 40-4.
[http://dx.doi.org/10.1111/j.1600-051X.2004.00623.x] [PMID: 15642057]
[118]
Brandão DFLMO, Silva APG, Penteado LAM. Relação bidirecional entre a doença periodontal e a diabetes mellitus. Odontol Clín Cient 2011. (Online)
[119]
Ross R. The pathogenesis of atherosclerosis-an update. N Engl J Med 1986; 314(8): 488-500.
[http://dx.doi.org/10.1056/NEJM198602203140806] [PMID: 3511384]
[120]
Lloyd AR, Oppenheim JJ. Poly’s lament: the neglected role of the polymorphonuclear neutrophil in the afferent limb of the immune response. Immunol Today 1992; 13(5): 169-72.
[http://dx.doi.org/10.1016/0167-5699(92)90121-M] [PMID: 1642755]
[121]
Delamaire M, Maugendre D, Moreno M, Le Goff MC, Allannic H, Genetet B. Impaired leucocyte functions in diabetic patients. Diabet Med 1997; 14(1): 29-34.
[http://dx.doi.org/10.1002/(SICI)1096-9136(199701)14:1<29::AID-DIA300>3.0.CO;2-V] [PMID: 9017350]
[122]
Wilson RM. Neutrophil function in diabetes. Diabet Med 1986; 3(6): 509-12.
[http://dx.doi.org/10.1111/j.1464-5491.1986.tb00806.x] [PMID: 2951206]
[123]
Nielson CP, Hindson DA. Inhibition of polymorphonuclear leukocyte respiratory burst by elevated glucose concentrations in vitro. Diabetes 1989; 38(8): 1031-5.
[http://dx.doi.org/10.2337/diabetes.38.8.1031] [PMID: 2753233]
[124]
Wilson RM, Tomlinson DR, Reeves WG. Neutrophil sorbitol production impairs oxidative killing in diabetes. Diabet Med 1987; 4(1): 37-40.
[http://dx.doi.org/10.1111/j.1464-5491.1987.tb00825.x] [PMID: 2951217]
[125]
Leite MF, De Lima A, Massuyama MM, Otton R. In vivo astaxanthin treatment partially prevents antioxidant alterations in dental pulp from alloxan-induced diabetic rats. Int Endod J 2010; 43(11): 959-67.
[http://dx.doi.org/10.1111/j.1365-2591.2010.01707.x] [PMID: 20546046]
[126]
West IC. Radicals and oxidative stress in diabetes. Diabet Med 2000; 17(3): 171-80.
[http://dx.doi.org/10.1046/j.1464-5491.2000.00259.x] [PMID: 10784220]
[127]
Russell BG. The dental pulp in diabetes mellitus. Acta Pathol Microbiol Scand 1967; 70(2): 319-20.
[http://dx.doi.org/10.1111/j.1699-0463.1967.tb01299.x] [PMID: 6050387]
[128]
Bissada NF, Sharawy AM. Histologic study of gingival and pulpal vascular changes in human diabetics. Egypt Dent J 1970; 16(4): 283-96.
[PMID: 5278447]
[129]
Persson GR. Diabetes and periodontal disease: An update for health care providers. Diabetes Spectr 2011; 24(4): 195-8.
[http://dx.doi.org/10.2337/diaspect.24.4.195]
[130]
Lang NP, Bartold PM. Periodontal health. J Clin Periodontol 2018; 45(Suppl. 20): S9-S16.
[http://dx.doi.org/10.1111/jcpe.12936] [PMID: 29926485]