Periodontopathogens, Candida spp. and immunological aspects in type 2 diabetes mellitus patients with chronic periodontitis

Authors

  • Gabriela Alessandra Da Cruz Galhardo Camargo Universidade Federal Fluminense
  • Natalia Linhares Coutinho Silva Universidade Federal do Rio de Janeiro
  • Ana Luísa Palhares de Miranda Universidade Federal do Rio de Janeiro
  • Jorge Luiz Mendonça Tributino Universidade Federal do Rio de Janeiro
  • Natália Helena Colombo Universidade Estadual Paulista
  • Cristiane Duque Universidade Estadual Paulista

DOI:

https://doi.org/10.20396/bjos.v15i3.8649993

Keywords:

Diabetes mellitus. Periodontal disease. Candida spp. TNF-α. Myeloperoxidase.

Abstract

This study aimed to evaluate clinical, microbiological and immunological parameters in type 2 diabetes mellitus (DM) in comparison with normoglycemic patients (NDM). Glycemic and lipid profiles and periodontal clinical status were determined for thirty-three patients (17 DM and 16 NDM). The presence of periodontopathogens and species of Candida in subgingival sites were determined by polymerase chain reaction and immunological parameters by ELISA assays. All glycemic and clinical parameters evaluated were higher in the DM group, with statistical difference for fasting glucose, glycated-hemoglobin, and periodontal parameters. Lipid profile (except triglycerides), levels of TNF-α and myeloperoxidase and the prevalence of the tested microorganisms were similar between the groups, except for Candida albicans and Candida glabrata, which was higher in the DM group. In conclusion, although microbiological and immunological parameters were similar in the DM and NDM groups, periodontitis and the levels of some species of Candida were more severe in DM patients.

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Author Biographies

Gabriela Alessandra Da Cruz Galhardo Camargo, Universidade Federal Fluminense

Professora Adjunto IV da Universidade Federal Fluminense, Instituto de Saúde de Nova Friburgo, Área de Periodontia. Bolsista do Ciências sem Fronteiras, bolsa de Pós Doutoramento na Universidade da Pensilvânia, UPENN, área de Periodontia (2014-2015).

Natalia Linhares Coutinho Silva, Universidade Federal do Rio de Janeiro

Farmacêutica generalista pelo Centro Universitário Augusto Motta (2009) e mestre em Ciências Farmacêuticas pela Universidade Federal do Rio de Janeiro (2012). Atualmente é doutoranda do Programa de Pós-graduação em Ciências Farmacêuticas (UFRJ) e afiliada da Sociedade Brasileira de Farmacologia e Terapêutica Experimental (SBFTE).

Ana Luísa Palhares de Miranda, Universidade Federal do Rio de Janeiro

Possui graduação em Farmácia pela Universidade Federal do Rio de Janeiro, concluiu o doutorado em Farmacologia pelo Institut National Polytechnique de Toulouse em 1986 e realizou pós-doutorado no Centro de Pesquisas da Sanofi Recherche - Toulouse(1988). Atualmente é Professor Associado IV da Faculdade de Farmácia da Universidade Federal do Rio de Janeiro, Vice-Diretora da Faculdade de Farmácia e Diretora Adjunta de Pós-Graduação, Faculdade de Farmácia, UFRJ, membro da Sociedade de Farmacologia e Terapêutica Experimental (SBFTE), membro da Sociedade Brasileira de Química (SBQ) e da Associação Brasileira de Ciências Farmacêuticas (ABCF).

Jorge Luiz Mendonça Tributino, Universidade Federal do Rio de Janeiro

Possui graduação em Farmácia pela Universidade Federal do Rio de Janeiro (2001), concluiu o mestrado (2002) e o doutorado (2008) pelo programa de Farmacologia e Química Medicinal do Instituto de Ciências Biomédicas (ICB) da Universidade Federal do Rio de Janeiro. Foi professor de Farmacologia e Fisiologia da Universidade Federal Fluminense - Pólo Universitário de Nova Friburgo e atualmente é Professor Adjunto II do Instituto de Ciências Biomédicas da Universidade Federal do Rio de Janeiro.

Natália Helena Colombo, Universidade Estadual Paulista

Graduada em Odontologia em 2009 pela Faculdade de Odontologia de Araçatuba, Universidade estadual paulista Júlio de Mesquita Filho (FOA/ UNESP). Mestrado em Ciências Fisiológicas concluído em 2012 (FOA/UNESP). Doutorado em Ciência Odontológica, Área de Saúde Bucal da Criança concluído em 2015 (FOA/UNESP).

Cristiane Duque, Universidade Estadual Paulista

Possui graduação em Odontologia pela Universidade Estadual Paulista Júlio de Mesquita Filho - UNESP - Araraquara (1999), especialização em Odontopediatria pelo Hospital de Reabilitação de Anomalias Craniofaciais - USP - Bauru (2002) e doutorado em Ciências Odontológicas (Área - Odontopediatria) pela Universidade Estadual Paulista Júlio de Mesquita Filho - UNESP (2005). Realizou pós-doutoramento na área de Microbiologia e Imunologia na Faculdade de Odontologia de Piracicaba - UNICAMP, com estágio na Forsyth Institute (EUA) (2006-2009). Atualmente é professor assistente doutor de Odontopediatria da Faculdade de Odontologia de Araçatuba - UNESP.

References

American Diabetes Association. Diagnosis and classification of diabetes mellitus. Diabetes Care. 2007 Jan;30 Suppl 1:S42-47.

Fentoğlu O, Oz G, Taşdelen P, Uskun E, Aykaç Y, Bozkurt FY. Periodontal status in subjects with hyperlipidemia. J Periodontol. 2009 Feb;80(2):26773. doi: 10.1902/jop.2009.080104.

Whiting DR, Guariguata L, Weil C, Shaw J. IDF diabetes atlas: global estimates of the prevalence of diabetes for 2011 and 2030. 2011 Dec;94(3):311-21. doi: 10.1016/j.diabres.2011.10.029.

Lalla E, Lamster IB, Drury S, Fu C, Schmidt AM. Hyperglycemia, glycoxidation and receptor for advanced glycation endproducts: potential mechanisms underlying diabetic complications, including diabetesassociated periodontitis. Periodontol 2000. 2000 Jun;23:50-62.

Chávarry NG, Vettore MV, Sansone C, Sheiham A. The relationship between diabetes mellitus and destructive periodontal disease: a metaanalysis. Oral Health Prev Dent. 2009;7(2):107-27.

Ebersole JL, Holt SC, Hansard R, Novak MJ. Microbiologic and immunologic characteristics of periodontal disease in Hispanic Americans with type 2 diabetes. J Periodontol. 2008 Apr;79(4):637-46. doi: 10.1902/ jop.2008.070455.

Field CA, Gidley MD, Preshaw PM, Jakubovics N. Investigation and quantification of key periodontal pathogens in patients with type 2 diabetes. J Periodontal Res. 2012 Aug;47(4):470-8. doi: 10.1111/j.16000765.2011.01455.x.

Sardi JC, Duque C, Camargo GA, Hofling JF, Gonçalves RB. Periodontal conditions and prevalence of putative periodontopathogens and Candida spp. In insulin-dependent type 2 diabetic and non-diabetic patients with chronic periodontitis--a pilot study. Arch Oral Biol. 2011 Oct;56(10):1098105. doi: 10.1016/j.archoralbio.2011.03.017.

Salvi GE, Beck JD, Offenbacher S. PGE2, IL-1 beta, and TNF-alpha responses in diabetics as modifiers of periodontal disease expression. Ann Periodontol. 1998 Jul;3(1):40-50.

Preshaw PM, Alba AL, Herrera D, Jepsen S, Konstantinidis A, Makrilakis K, et al. Periodontitis and diabetes: a two-way relationship. Diabetologia. 2012 Jan;55(1):21-31. doi: 10.1007/s00125-011-2342-y.

Buduneli N, Kinane DF. Host-derived diagnostic markers related to soft tissue destruction and bone degradation in periodontitis. J Clin Periodontol. 2011 Mar;38 Suppl 11:85-105. doi: 10.1111/j.1600-051X.2010.01670.x.

Leppilahti JM, Hernández-Ríos PA, Gamonal JA, Tervahartiala T, Brignardello-Petersen R, Mantyla P, et al. Matrix metalloproteinases and myeloperoxidase in gingival crevicular fluid provide site-specific diagnostic value for chronic periodontitis. J Clin Periodontol 2014 Apr;41(4):348-56. doi: 10.1111/jcpe.12223.

Gonçalves D, Correa FO, Khalil NM, de Faria Oliveira OM, Orrico SR. The effect of non-surgical periodontal therapy on peroxidase activity in diabetic patients: a case-control pilot study. J Clin Periodontol. 2008 Sep;35(9):799806. doi: 10.1111/j.1600-051X.2008.01289.x.

Page RC, Eke PI. Case definitions for use in population-based surveillance of periodontitis. J Periodontol. 2007 Jul;78(7 Suppl):1387-99.

Camargo GA, Lima M A, Fortes TV, de Souza CS, de Jesus AM, de Almeida RP. Effect of periodontal therapy on metabolic control and levels of IL-6 in the gingival crevicular fluid in type 2 diabetes mellitus. Indian J Dent Res. 2013 Jan-Feb;24(1):110-6. doi: 10.4103/0970-9290.114953.

Ainamo J, Bay I. Problems and proposals for recording gingivitis and plaque. Int Dent J. 1975 Dec;25(4):229-35.

Ashimoto A, Chen C, Bakker I, Slots J. Polymerase chain reaction detection of 8 putative periodontal pathogens in subgingival plaque of gingivitis and advanced periodontitis lesions. Oral Microbiol Immunol. 1996 Aug;11(4):266-73.

Correa FO, Gonçalves D, Figueredo CM, Bastos AS, Gustafsson A, Orrico SR. Effect of periodontal treatment on metabolic control, systemic inflammation and cytokines in patients with type 2 diabetes. J Clin Periodontol. 2010 Jan;37(1):53-8. doi: 10.1111/j.1600-051X.2009.01498.x.

Abbass MM, Korany NS, Salama AH, Dmytryk JJ, Safiejko-Mroczka B. The relationship between receptor for advanced glycation end products expression and the severity of periodontal disease in the gingiva of diabetic and non diabetic periodontitis patients. Arch Oral Biol. 2012 Oct;57(10):1342-54. doi: 10.1016/j.archoralbio.2012.06.007.

Garcia D, Tarima S, Okunseri C. Periodontitis and glycemic control in diabetes: NHANES 2009 to 2012. J Periodontol. 2015 Apr;86(4):499-506. doi: 10.1902/jop.2014.140364.

Radoi V, Lixandru D, Mohora M, Virgolici B. Advance glycation and products in diabetes mellitus: mechanism of action and focused treatment. Proc Rom Acad. 2012;1:9-19.

Machado AC, Quirino MR, Nascimento LF. Relation between chronic periodontal disease and plasmatic levels of triglycerides, total cholesterol and fractions. Braz Oral Res. 2005 Oct-Dec;19(4):284-9.

Banihashemrad SA, Moeintaghavi A, Rafighdoost A. Relationship between cholesterol and triglyceride blood values and periodontal parameters in patients of Mashhad health center. N Y State Dent J. 2008 AugSep;74(5):65-6.

Tu YK, D'Aiuto F, Lin HJ, Chen YW, Chien KL. Relationship between metabolic syndrome and diagnoses of periodontal diseases among participants in a large Taiwanese cohort. J Clin Periodontol. 2013 Nov;40(11):994-1000. doi: 10.1111/jcpe.12157.

Sora ND, Marlow NM, Bandyopadhyay D, Leite RS, Slate EH, Fernandes JK. Metabolic syndrome and periodontitis in Gullah African Americans with type 2 diabetes mellitus. J Clin Periodontol. 2013 Jun;40(6):599-606. doi: 10.1111/jcpe.12104.

Almeida Abdo J, Cirano FR, Casati MZ, Giampaoli V, Viana Casarin RC, Pimentel SP. Influence of dyslipidemia and diabetes mellitus on chronic periodontal disease. J Periodontol. 2013 Oct;84(10):1401-8. doi: 10.1902/ jop.2012.120366.

Casarin RC, Barbagallo A, Meulman T, Santos VR, Sallum EA, Nociti FH, et al. Subgingival biodiversity in subjects with uncontrolled type-2 diabetes and chronic periodontitis. J Periodontal Res. 2013 Feb;48(1):30-6. doi: 10.1111/j.1600-0765.2012.01498.x.

Yuan K, Chang CJ, Hsu PC, Sun HS, Tseng CC, Wang JR. Detection of putative periodontal pathogens in non-insulin-dependent diabetes mellitus and non-diabetes mellitus by polymerase chain reaction. J Periodontal Res. 2001 Feb;36(1):18-24.

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 Jun;22(3):175-81.

Aemaimanan P, Amimanan P, Taweechaisupapong S. Quantification of key periodontal pathogens in insulin-dependent type 2 diabetic and nondiabetic patients with generalized chronic periodontitis. Anaerobe. 2013 Aug;22:64-8. doi: 10.1016/j.anaerobe.2013.06.010.

Li C, Liu J, Tan L, Yu N, Lin L, Geng F, et al. The sociodemographic characteristics, periodontal health status, and subgingival microbiota of patients with chronic periodontitis and type 2 diabetes mellitus: a casecontrol study in a Chinese population. J Periodontol. 2013 Aug;84(8):105866. doi: 10.1902/jop.2012.120282.

Zhou M1, Rong R, Munro D, Zhu C, Gao X, Zhang Q, et al. Investigation of the effect of type 2 diabetes mellitus on subgingival plaque microbiota by high-throughput 16S rDNA pyrosequencing. PLoS One. 2013 Apr 22;8(4):e61516. doi: 10.1371/journal.pone.0061516.

Haffajee AD, Bogren A, Hasturk H, Feres M, Lopez NJ, Socransky SS. Subgingival microbiota of chronic periodontitis subjects from different geographic locations. J Clin Periodontol. 2004 Nov;31(11):996-1002.

Javed F, Klingspor L, Sundin U, Altamash M, Klinge B, Engström PE. Periodontal conditions, oral Candida albicans and salivary proteins in type 2 diabetic subjects with emphasis on gender. BMC Oral Health. 2009 May 12;9:12. doi: 10.1186/1472-6831-9-12.

Hammad MM, Darwazeh AM, Idrees MM. The effect of glycemic control on Candida colonization of the tongue and the subgingival plaque in patients with type II diabetes and periodontitis. Oral Surg Oral Med Oral Pathol Oral Radiol. 2013 Sep;116(3):321-6. doi: 10.1016/j.oooo.2013.05.013.

Melton JJ, Redding SW, Kirkpatrick WR, Reasner CA, Ocampo GL, Venkatesh A, et al. Recovery of Candida dublinienses and other Candida species from the oral cavity of subjects with periodontitis who had well controlled and poorly controlled type 2 diabetes: a pilot study. Spec Care Dent. 2010 Nov-Dec;30(6):230-4. doi: 10.1111/j.1754-4505.2010.00159.x.

Fidel PL Jr, Vazquez JA, Sobel JD. Candida glabrata: review of epidemiology, pathogenesis, and clinical disease with comparison to C. albicans. Clin Microbiol Rev. 1999 Jan;12(1):80-96.

Javed F, Al-Askar M, Al-Hezaimi K. Cytokine profile in the gingival crevicular fluid of periodontitis patients with and without type 2 diabetes: a literature review. J Periodontol. 2012 Feb;83(2):156-61. doi: 10.1902/ jop.2011.110207.

Geisinger ML, Michalowicz BS, Hou W, Schoenfeld E, Gelato M, Engebretson SP, et al. Systemic Inflammatory Biomarkers and Their Association With Periodontal and Diabetes-Related Factors in the Diabetes and Periodontal Therapy Trial, A Randomized Controlled Trial. J Periodontol. 2016 Aug;87(8):900-13. doi: 10.1902/jop.2016.150727.

Yamalik N, Cağlayan F, Kilinç K, Kilinç A, Tümer C. The importance of data presentation regarding gingival crevicular fluid myeloperoxidase and elastase-like activity in periodontal disease and health status. J Periodontol. 2000 Mar;71(3):460-7.

Tenovuo J, Lehtonen OP, Viikari J, Larjava H, Vilja P, Tuohimaa P. Immunoglobulins and innate antimicrobial factors in whole saliva of patients with insulin-dependent diabetes mellitus. J Dent Res. 1986 Jan;65(1):62-6.

Benkirane RM, Guillot E, Mouton C. Immunomagnetic PCR and DNA probe for detection and identification of Porphyromonas gingivalis. J Clin Microbiol 1995;33(11):2908-12.

Slots J, Ashimoto A, Flynn MJ, Li G, Chen C. Detection of putative periodontal pathogens in subgingival specimens by 16S ribosomal DNA amplification with the polymerase chain reaction. Clin Infect Dis 1995;20(Suppl):S304-7.

Donnelly SM, Sullivan DJ, Shanley DB, Coleman DC. Phylogenetic analysis and rapid identification of Candida dubliniensis based on analysis of ACT1 intron and exon sequences. Microbiology 1999;145(Pt 8):1871182.

Published

2017-08-11

How to Cite

1.
Camargo GADCG, Silva NLC, Miranda ALP de, Tributino JLM, Colombo NH, Duque C. Periodontopathogens, Candida spp. and immunological aspects in type 2 diabetes mellitus patients with chronic periodontitis. Braz. J. Oral Sci. [Internet]. 2017Aug.11 [cited 2021Mar.8];15(3):226-33. Available from: https://periodicos.sbu.unicamp.br/ojs/index.php/bjos/article/view/8649993

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