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Differences in the subgingival microbial population of chronic periodontitis in subjects with and without type 2 diabetes mellitus—a systematic review

  • Linda Sun Liu
  • Nikolaos Gkranias
  • Bruna Farias
  • Dave Spratt
  • Nikolaos Donos
Review

Abstract

Objectives

The purpose of this systematic review was to evaluate the available evidence in the literature in regard to the subgingival microbial population of chronic periodontitis in subjects with type 2 diabetes mellitus (T2DM+PD) compared to non-diabetic subjects (NDM+PD).

Materials and methods

A literature search was conducted at Ovid MEDLINE and EMBASE database from 1980 to 2016, supplemented by hand searching as needed. Studies presenting with at least one of the primary outcomes (presence of any subgingival microorganisms, proportion and/or the amount of any subgingival plaque bacteria in T2DM+PD versus NDM+PD) were included. Screening, data extraction and quality assessment were conducted independently and in duplicate.

Results

From 611 citations, 19 full-text papers were screened and 11 articles were included for critical appraisal by both reviewers. Some evidence of a difference in the microbial profile between chronic PD subjects with and without T2DM was identified. The strength of evidence is strongest in Tannerella forthysia (T .forsythia) which was reported to be less frequent in the diabetic (T2DM+PD) group in five of the studies, followed by a weaker strength of evidence for other periodontal pathogens such as Porphyromonas gingivalis (P. gingivalis) and Aggregatibacter actinomycetemcomitans (A. actinomycetemcomitans), which were also found less frequent in the diabetic (T2DM+PD) group .

Conclusion

Only few studies have compared T2DM+PD with NDM+PD. It is therefore strongly recommended that further studies which include four distinct groups of participants (NDM+PD, T2DM+PD, NDM+NPD, T2DM+NPD) instead of using intra-subject comparisons between healthy and diseased sites of the same subjects.

Clinical relevance

Differences in bacterial populations of T2DM+PD in comparison to NDM+PD subjects may indicate the need of different protocols for the treatment of the diabetic patients with periodontal disease.

Keywords

Periodontitis Diabetes mellitus Systematic review Microbiological analyses 

Notes

Funding

The work was supported by the Department of Periodontology, UCL Eastman Dental Institute, London, UK.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors. For this type of study, ethical approval is not required.

Informed consent

For this type of study, formal consent is not required.

References

  1. 1.
    Jenkinson HF, Dymock D (1999) The microbiology of periodontal disease. Dent Update 26:191–197CrossRefPubMedGoogle Scholar
  2. 2.
    Van Der Velden U (2005) Purpose and problems of periodontal disease classification. Periodontol 39:13–21.  https://doi.org/10.1111/j.1600-0757.2005.00127.x CrossRefGoogle Scholar
  3. 3.
    Pérez-Chaparro PJ, Gonçalves C, Figueiredo LC, Faveri M, Lobão E, Tamashiro N, Duarte P, Feres M (2014) Newly identified pathogens associated with periodontitis: a systematic review. J Dent Res 93:846–858.  https://doi.org/10.1177/0022034514542468 CrossRefPubMedPubMedCentralGoogle Scholar
  4. 4.
    Dzink JL, Socransky SS, Haffajee AD (1988) The predominant cultivable microbiota of active and inactive lesions of destructive periodontal diseases. J Clin Periodontol 15:316–323CrossRefPubMedGoogle Scholar
  5. 5.
    Socransky SS, Haffajee AD (2005) Periodontal microbial ecology. Periodontol 38:135–187.  https://doi.org/10.1111/j.1600-0757.2005.00107.x CrossRefGoogle Scholar
  6. 6.
    Socransky SS, Haffajee AD, Smith C, Duff GW (2000) Microbiological parameters associated with IL-1 gene polymorphisms in periodontitis patients. J Clin Periodontol 27:810–818.  https://doi.org/10.1034/j.1600-051x.2000.027011810.x CrossRefPubMedGoogle Scholar
  7. 7.
    Trevilatto PC, Scarel-Caminaga RM, de Brito RB, de Souza AP, Line SRP (2003) Polymorphism at position- 174 of IL-6 gene is associated with susceptibility to chronic periodontitis in a Caucasian Brazilian population. J Clin Periodontol 30:438–442.  https://doi.org/10.1034/j.1600-051X.2003.20016.x CrossRefPubMedGoogle Scholar
  8. 8.
    Babel N, Cherepnev G, Babel D, Tropmann A, Hammer M, Volk HD, Reinke P (2006) Analysis of tumor necrosis factor-alpha, transforming growth factor-beta, interleukin-10, IL-6, and interferon-gamma gene polymorphisms in patients with chronic periodontitis. J Periodontol 77:1978–1983.  https://doi.org/10.1902/jop.2006.050315 CrossRefPubMedGoogle Scholar
  9. 9.
    Toomes C, James J, Wood AJ, Wu CL, McCormick D, Lench N, Hewitt C, Moynihan L, Roberts E, Woods CG, Markham A, Wong M, Widmer R, Ghaffar KA, Pemberton M, Hussein IR, Temtamy SA, Davies R, Read AP, Sloan P, Dixon MJ, Thakker NS (1999) Loss-of-function mutations in the cathepsin C gene result in periodontal disease and palmoplantar keratosis. Nat Genet 23:421–424.  https://doi.org/10.1038/70525 CrossRefPubMedGoogle Scholar
  10. 10.
    Nibali L, Donos N, Henderson B (2009) Periodontal infectogenomics. J Med Microbiol 58:1269–1274.  https://doi.org/10.1099/jmm.0.012021-0 CrossRefPubMedGoogle Scholar
  11. 11.
    Grossi SG, Genco RJ (1998) Periodontal disease and diabetes mellitus: a two-way relationship*. Ann Periodontol 3:51–61CrossRefPubMedGoogle Scholar
  12. 12.
    Chapple ILC, Genco R (2013) And on behalf of working group 2 of the joint EFP/AAP workshop. Diabetes and periodontal diseases: consensus report of the joint EFP/AAP workshop on periodontitis and systemic diseases. J Clin Periodontol 40(Suppl. 14):S106–S112.  https://doi.org/10.1111/jcpe.12077 CrossRefPubMedGoogle Scholar
  13. 13.
    Seppälä B, Seppälä M, Ainamo J (1993) A longitudinal study on insulin-dependent diabetes mellitus and periodontal disease. J Clin Periodontol 20:161–165CrossRefPubMedGoogle Scholar
  14. 14.
    Taylor GW, Burt BA, Becker MP, Genco RJ, Shlossman M, Knowler WC, Pettitt DJ (1998) Non-insulin dependent diabetes mellitus and alveolar bone loss progression over 2 years. J Periodontol 69:76–83.  https://doi.org/10.1902/jop.1998.69.1.76 CrossRefPubMedGoogle Scholar
  15. 15.
    Lalla E, Papapanou PN (2011) Diabetes mellitus and periodontitis: a tale of two common interrelated diseases. Nat Rev Endocrinol 7:738–748CrossRefGoogle Scholar
  16. 16.
    Taylor JJ, Preshaw PM, Lalla E (2013) A review of the evidence for pathogenic mechanisms that may link periodontitis and diabetes. J Clin Periodontol 40(Suppl. 14):S113–S134.  https://doi.org/10.1111/jcpe.12059 CrossRefPubMedGoogle Scholar
  17. 17.
    Mealey BL, Oates TW (2006) Diabetes mellitus and periodontal diseases. J Periodontol 77:1289–1303.  https://doi.org/10.1902/jop.2006.050459 CrossRefPubMedGoogle Scholar
  18. 18.
    Ficara AJ, Levin MP, Grower MF, Kramer GD (1975) A comparison of the glucose and protein content of gingival fluid from diabetics and nondiabetics. J Periodontal Res 10:171–175.  https://doi.org/10.1111/j.1600-0765.1975.tb00022.x CrossRefPubMedGoogle Scholar
  19. 19.
    Anestis M (2006) AP biology, 2nd edn. McGraw-Hill Professional, New YorkGoogle Scholar
  20. 20.
    Walker AW, Duncan SH, McWilliam Leitch EC et al (2005) pH and peptide supply can radically alter bacterial populations and short-chain fatty acid ratios within microbial communities from the human colon. Appl Environ Microbiol 71:3692–3700.  https://doi.org/10.1128/AEM.71.7.3692-3700.2005 CrossRefPubMedPubMedCentralGoogle Scholar
  21. 21.
    Ciantar M, Gilthorpe MS, Hurel S et al (2005) Capnocytophaga spp. in periodontitis patients manifesting diabetes mellitus. J Periodontol 76:194–203.  https://doi.org/10.1902/jop.2005.76.2.194 CrossRefPubMedGoogle Scholar
  22. 22.
    Sastrowijoto SH, Hillemans P, van Steenbergen TJ et al (1989) Periodontal condition and microbiology of healthy and diseased periodontal pockets in type 1 diabetes mellitus patients. J Clin Periodontol 16:316–322CrossRefPubMedGoogle Scholar
  23. 23.
    Zambon JJ, Reynolds H, Fisher JG, Shlossman M, Dunford R, Genco RJ (1988) Microbiological and immunological studies of adult periodontitis in patients with noninsulin-dependent diabetes mellitus. J Periodontol 59:23–31CrossRefPubMedGoogle Scholar
  24. 24.
    Spratt D (2004) Significance of bacterial identification by molecular biology methods. Endod Top 9:5–14.  https://doi.org/10.1111/j.1601-1546.2004.00106.x CrossRefGoogle Scholar
  25. 25.
    Weisburg WG, Barns SM, Pelletier DA, Lane DJ (1991) 16S ribosomal DNA amplification for phylogenetic study. J Bacteriol 173:697–703CrossRefPubMedPubMedCentralGoogle Scholar
  26. 26.
    Coenye T, Vandamme P (2003) Intragenomic heterogeneity between multiple 16S ribosomal RNA operons in sequenced bacterial genomes. FEMS Microbiol Lett 228:45–49.  https://doi.org/10.1016/S0378-1097(03)00717-1 CrossRefPubMedGoogle Scholar
  27. 27.
    Higgins GS (editors). (2011) Cochrane Handbook for Systematic Reviews of Interventions Version 5.1.0 [updated March 2011]. The Cochrane collaboration. In: Cochrane Collab. 2011. http://www.cochrane.org/training/cochrane-handbook. Accessed 16 Apr 2012
  28. 28.
    Wells G, Shea B, O’Connell D et al (2000) The Newcastle-Ottawa Scale (NOS) for assessing Available, quality if nonrandomized studies in meta-analysesGoogle Scholar
  29. 29.
    Collin HL, Uusitupa M, Niskanen L, Kontturi-Närhi V, Markkanen H, Koivisto AM, Meurman JH (1998) Periodontal findings in elderly patients with non-insulin dependent diabetes mellitus. J Periodontol 69:962–966CrossRefPubMedGoogle Scholar
  30. 30.
    Davila-Perez C, Amano A, Alpuche-Solis AG, Patiño-Marin N, Pontigo-Loyola AP, Hamada S, Loyola-Rodriguez JP (2007) Distribution of genotypes of Porphyromonas gingivalis in type 2 diabetic patients with periodontitis in Mexico. J Clin Periodontol 34:25–30.  https://doi.org/10.1111/j.1600-051X.2006.01011.x CrossRefPubMedGoogle Scholar
  31. 31.
    Sardi JCO, Duque C, Camargo GACG, Hofling JF, Gonçalves RB (2011) 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 56:1098–1105.  https://doi.org/10.1016/j.archoralbio.2011.03.017 CrossRefPubMedGoogle Scholar
  32. 32.
    Ebersole JL, Holt SC, Hansard R, Novak MJ (2008) Microbiologic and immunologic characteristics of periodontal disease in Hispanic americans with type 2 diabetes. J Periodontol 79:637–646.  https://doi.org/10.1902/jop.2008.070455 CrossRefPubMedGoogle Scholar
  33. 33.
    Novaes AB, Gonzalez Gutierrez F, Grisi MF (1997) Periodontal disease progression in type II non-insulin-dependent diabetes mellitus patients (NIDDM). Part II--microbiological analysis using the BANA test. Braz Dent J 8:27–33PubMedGoogle Scholar
  34. 34.
    Casarin RCV, Barbagallo A, Meulman T, Santos VR, Sallum EA, Nociti FH, Duarte PM, Casati MZ, Gonçalves RB (2013) Subgingival biodiversity in subjects with uncontrolled type-2 diabetes and chronic periodontitis. J Periodontal Res 48:30–36.  https://doi.org/10.1111/j.1600-0765.2012.01498.x CrossRefPubMedGoogle Scholar
  35. 35.
    Field CA, Gidley MD, Preshaw PM, Jakubovics N (2012) Investigation and quantification of key periodontal pathogens in patients with type 2 diabetes. J Periodontal Res 47:470–478.  https://doi.org/10.1111/j.1600-0765.2011.01455.x CrossRefPubMedGoogle Scholar
  36. 36.
    Zhou M, Rong R, Munro D, Zhu C, Gao X, Zhang Q, Dong Q (2013) Investigation of the effect of type 2 diabetes mellitus on subgingival plaque microbiota by high-throughput 16S rDNA pyrosequencing. PLoS One 8:e61516.  https://doi.org/10.1371/journal.pone.0061516 CrossRefPubMedPubMedCentralGoogle Scholar
  37. 37.
    Christgau M, Palitzsch KD, Schmalz G, Kreiner U, Frenzel S (1998) Healing response to non-surgical periodontal therapy in patients with diabetes mellitus: clinical, microbiological, and immunologic results. J Clin Periodontol 25:112–124CrossRefPubMedGoogle Scholar
  38. 38.
    Armitage GC (1999) Development of a classification system for periodontal diseases and conditions. Ann Periodontol 4:1–6.  https://doi.org/10.1902/annals.1999.4.1.1 CrossRefPubMedGoogle Scholar
  39. 39.
    Stone MA, Camosso-Stefinovic J, Wilkinson J, de Lusignan S, Hattersley AT, Khunti K (2010) Incorrect and incomplete coding and classification of diabetes: a systematic review. Diabet Med 27:491–497.  https://doi.org/10.1111/j.1464-5491.2009.02920.x CrossRefPubMedGoogle Scholar
  40. 40.
    Rylev M, Kilian M (2008) Prevalence and distribution of principal periodontal pathogens worldwide. J Clin Periodontol 35:346–361.  https://doi.org/10.1111/j.1600-051X.2008.01280.x CrossRefPubMedGoogle Scholar
  41. 41.
    Bizzarro S, Loos BG, Laine ML, Crielaard W, Zaura E (2013) Subgingival microbiome in smokers and non-smokers in periodontitis: an exploratory study using traditional targeted techniques and a next-generation sequencing. J Clin Periodontol 40:483–492.  https://doi.org/10.1111/jcpe.12087 CrossRefPubMedGoogle Scholar
  42. 42.
    Smith S, Morin PA (2005) Optimal storage conditions for highly dilute DNA samples: a role for trehalose as a preserving agent. J Forensic Sci 50:1101–1108CrossRefPubMedGoogle Scholar
  43. 43.
    Jervøe-Storm P-M, Alahdab H, Koltzscher M et al (2007) Comparison of curet and paper point sampling of subgingival bacteria as analyzed by real-time polymerase chain reaction. J Periodontol 78:909–917.  https://doi.org/10.1902/jop.2007.060218 CrossRefPubMedGoogle Scholar
  44. 44.
    Yang MCK, Marks RG, Clark WB, Magnusson I (1991) Evaluation of statistical methods for monitoring periodontal disease. Stat Med 10:1089–1097.  https://doi.org/10.1002/sim.4780100709 CrossRefPubMedGoogle Scholar
  45. 45.
    Abusleme L, Dupuy AK, Dutzan N, Silva N, Burleson JA, Strausbaugh LD, Gamonal J, Diaz PI (2013) The subgingival microbiome in health and periodontitis and its relationship with community biomass and inflammation. ISME J 7:1016–1025.  https://doi.org/10.1038/ismej.2012.174 CrossRefPubMedPubMedCentralGoogle Scholar
  46. 46.
    Saunders NA, Martin A. Lee (2009) Real-time PCR: current technology and applicationsGoogle Scholar
  47. 47.
    Boutaga K, van Winkelhoff AJ, Vandenbroucke-Grauls CMJE, Savelkoul PHM (2005) Periodontal pathogens: a quantitative comparison of anaerobic culture and real-time PCR. FEMS Immunol Med Microbiol 45:191–199.  https://doi.org/10.1016/j.femsim.2005.03.011 CrossRefPubMedGoogle Scholar
  48. 48.
    Boutaga K, van Winkelhoff AJ, Vandenbroucke-Grauls CMJE, Savelkoul PHM (2003) Comparison of real-time PCR and culture for detection of Porphyromonas gingivalis in subgingival plaque samples. J Clin Microbiol 41:4950–4954CrossRefPubMedPubMedCentralGoogle Scholar
  49. 49.
    Boutaga K, van Winkelhoff AJ, Vandenbroucke-Grauls CMJE, Savelkoul PHM (2006) The additional value of real-time PCR in the quantitative detection of periodontal pathogens. J Clin Periodontol 33:427–433.  https://doi.org/10.1111/j.1600-051X.2006.00925.x CrossRefPubMedGoogle Scholar
  50. 50.
    Szafrański SP, Deng Z-L, Tomasch J, Jarek M, Bhuju S, Meisinger C, Kühnisch J, Sztajer H, Wagner-Döbler I (2015) Functional biomarkers for chronic periodontitis and insights into the roles of Prevotella nigrescens and fusobacterium nucleatum; a metatranscriptome analysis. npj Biofilms Microbiomes 1:15017.  https://doi.org/10.1038/npjbiofilms.2015.17 CrossRefPubMedPubMedCentralGoogle Scholar
  51. 51.
    Vartoukian SR, Palmer RM, Wade WG (2010) Cultivation of a Synergistetes strain representing a previously uncultivated lineage. Environ Microbiol 12:916–928.  https://doi.org/10.1111/j.1462-2920.2009.02135.x CrossRefPubMedPubMedCentralGoogle Scholar
  52. 52.
    Griffen AL, Beall CJ, Campbell JH, Firestone ND, Kumar PS, Yang ZK, Podar M, Leys EJ (2012) Distinct and complex bacterial profiles in human periodontitis and health revealed by 16S pyrosequencing. ISME J 6:1176–1185.  https://doi.org/10.1038/ismej.2011.191 CrossRefPubMedGoogle Scholar
  53. 53.
    Kumar PS, Griffen AL, Moeschberger ML, Leys EJ (2005) Identification of candidate periodontal pathogens and beneficial species by quantitative 16S clonal analysis. J Clin Microbiol 43:3944–3955.  https://doi.org/10.1128/JCM.43.8.3944-3955.2005 CrossRefPubMedPubMedCentralGoogle Scholar
  54. 54.
    Mardis ER (2011) A decade’s perspective on DNA sequencing technology. Nature 470:198–203.  https://doi.org/10.1038/nature09796 CrossRefPubMedGoogle Scholar
  55. 55.
    Liu B, Faller LL, Klitgord N, Mazumdar V, Ghodsi M, Sommer DD, Gibbons TR, Treangen TJ, Chang YC, Li S, Stine OC, Hasturk H, Kasif S, Segrè D, Pop M, Amar S (2012) Deep sequencing of the oral microbiome reveals signatures of periodontal disease. PLoS One 7:e37919.  https://doi.org/10.1371/journal.pone.0037919 CrossRefPubMedPubMedCentralGoogle Scholar
  56. 56.
    Mardis ER (2008) The impact of next-generation sequencing technology on genetics. Trends Genet 24:133–141.  https://doi.org/10.1016/j.tig.2007.12.007 CrossRefPubMedGoogle Scholar
  57. 57.
    Décaillet F, Giannopoulou C, Cionca N et al (2012) Microbial profiles of patients seeking treatment for periodontitis. Influence of origin, smoking and age? Schweiz Monatsschr Zahnmed 122:198–204PubMedGoogle Scholar
  58. 58.
    Buchwald S, Kocher T, Biffar R, Harb A, Holtfreter B, Meisel P (2013) Tooth loss and periodontitis by socio-economic status and inflammation in a longitudinal population-based study. J Clin Periodontol 40:203–211.  https://doi.org/10.1111/jcpe.12056 CrossRefPubMedGoogle Scholar
  59. 59.
    Lafaurie GI, Contreras A, Barón A, Botero J, Mayorga-Fayad I, Jaramillo A, Giraldo A, González F, Mantilla S, Botero A, Archila LH, Díaz A, Chacón T, Castillo DM, Betancourt M, del Rosario Aya M, Arce R (2007) Demographic, clinical, and microbial aspects of chronic and aggressive periodontitis in Colombia: a multicenter study. J Periodontol 78:629–639.  https://doi.org/10.1902/jop.2007.060187 CrossRefPubMedGoogle Scholar
  60. 60.
    Kim TS, Kang NW, Lee S-B, Eickholz P, Pretzl B, Kim CK (2009) Differences in subgingival microflora of Korean and German periodontal patients. Arch Oral Biol 54:223–229.  https://doi.org/10.1016/j.archoralbio.2008.10.005 CrossRefPubMedGoogle Scholar
  61. 61.
    Persson GR (2005) Site-based versus subject-based periodontal diagnosis. Periodontol 39:145–163.  https://doi.org/10.1111/j.1600-0757.2005.00130.x CrossRefGoogle Scholar
  62. 62.
    Röder B, Frühwirth K, Vogl C et al (2010) Impact of long-term storage on stability of standard DNA for nucleic acid-based methods. J Clin Microbiol 48:4260–4262.  https://doi.org/10.1128/JCM.01230-10 CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Periodontology UnitUCL Eastman Dental InstituteLondonUK
  2. 2.Centre for Oral Clinical Research, Institute of Dentistry, Barts & The London School of Medicine & DentistryQueen Mary University of London (QMUL)LondonUK
  3. 3.Postgraduate DepartmentFederal University of PernambucoRecifeBrazil
  4. 4.Microbiology DepartmentUCL Eastman Dental InstituteLondonUK

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