nach oben

Clinical Oral Investigations

Erschienen in:

10.10.2018 | Review

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

verfasst von: Linda Sun Liu, Nikolaos Gkranias, Bruna Farias, Dave Spratt, Nikolaos Donos

Erschienen in: Clinical Oral Investigations | Ausgabe 8/2018

Einloggen, um Zugang zu erhalten

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.

Nur mit Berechtigung zugänglich

Jenkinson HF, Dymock D (1999) The microbiology of periodontal disease. Dent Update 26:191–197CrossRefPubMed

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 CrossRef

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 CrossRefPubMedPubMedCentral

Dzink JL, Socransky SS, Haffajee AD (1988) The predominant cultivable microbiota of active and inactive lesions of destructive periodontal diseases. J Clin Periodontol 15:316–323CrossRefPubMed

Socransky SS, Haffajee AD (2005) Periodontal microbial ecology. Periodontol 38:135–187. https://doi.org/10.1111/j.1600-0757.2005.00107.x CrossRef

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 CrossRefPubMed

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 CrossRefPubMed

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 CrossRefPubMed

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 CrossRefPubMed

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 CrossRefPubMed

11.

Grossi SG, Genco RJ (1998) Periodontal disease and diabetes mellitus: a two-way relationship*. Ann Periodontol 3:51–61CrossRefPubMed

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 CrossRefPubMed

13.

Seppälä B, Seppälä M, Ainamo J (1993) A longitudinal study on insulin-dependent diabetes mellitus and periodontal disease. J Clin Periodontol 20:161–165CrossRefPubMed

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 CrossRefPubMed

15.

Lalla E, Papapanou PN (2011) Diabetes mellitus and periodontitis: a tale of two common interrelated diseases. Nat Rev Endocrinol 7:738–748CrossRefPubMed

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 CrossRefPubMed

17.

Mealey BL, Oates TW (2006) Diabetes mellitus and periodontal diseases. J Periodontol 77:1289–1303. https://doi.org/10.1902/jop.2006.050459 CrossRefPubMed

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 CrossRefPubMed

19.

Anestis M (2006) AP biology, 2nd edn. McGraw-Hill Professional, New York

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 CrossRefPubMedPubMedCentral

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 CrossRefPubMed

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 16:316–322CrossRefPubMed

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 59:23–31CrossRefPubMed

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 CrossRef

25.

Weisburg WG, Barns SM, Pelletier DA, Lane DJ (1991) 16S ribosomal DNA amplification for phylogenetic study. J Bacteriol 173:697–703CrossRefPubMedPubMedCentral

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 CrossRefPubMed

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.

Wells G, Shea B, O’Connell D et al (2000) The Newcastle-Ottawa Scale (NOS) for assessing Available, quality if nonrandomized studies in meta-analyses

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 69:962–966CrossRefPubMed

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 CrossRefPubMed

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 CrossRefPubMed

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 CrossRefPubMed

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 8:27–33PubMed

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 CrossRefPubMed

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 CrossRefPubMed

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 CrossRefPubMedPubMedCentral

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 25:112–124CrossRefPubMed

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 CrossRefPubMed

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 CrossRefPubMed

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 CrossRefPubMed

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 CrossRefPubMed

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 50:1101–1108CrossRefPubMed

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 CrossRefPubMed

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 CrossRefPubMed

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 CrossRefPubMedPubMedCentral

46.

Saunders NA, Martin A. Lee (2009) Real-time PCR: current technology and applications

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 CrossRefPubMed

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 41:4950–4954CrossRefPubMedPubMedCentral

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 CrossRefPubMed

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 CrossRefPubMedPubMedCentral

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 CrossRefPubMedPubMedCentral

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 CrossRefPubMed

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 CrossRefPubMedPubMedCentral

54.

Mardis ER (2011) A decade’s perspective on DNA sequencing technology. Nature 470:198–203. https://doi.org/10.1038/nature09796 CrossRefPubMed

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 CrossRefPubMedPubMedCentral

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 CrossRefPubMed

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 122:198–204PubMed

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 CrossRefPubMed

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 CrossRefPubMed

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 CrossRefPubMed

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 CrossRef

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 CrossRefPubMedPubMedCentral

Titel: Differences in the subgingival microbial population of chronic periodontitis in subjects with and without type 2 diabetes mellitus—a systematic review
verfasst von: Linda Sun Liu
Nikolaos Gkranias
Bruna Farias
Dave Spratt
Nikolaos Donos
Publikationsdatum: 10.10.2018
Verlag: Springer Berlin Heidelberg
Erschienen in: Clinical Oral Investigations / Ausgabe 8/2018
Print ISSN: 1432-6981
Elektronische ISSN: 1436-3771
DOI: https://doi.org/10.1007/s00784-018-2660-2

Neu im Fachgebiet Zahnmedizin

19.04.2024 | Vorhofflimmern | Nachrichten

Newsletter bestellen

Live-Webinar: Aktuelle Leitlinien bei Herz-Kreislauf-Erkrankungen

Springer Medizin

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

Abstract

Objectives

Materials and methods

Results

Conclusion

Clinical relevance

Neu im Fachgebiet Zahnmedizin

Parodontalbehandlung verbessert Prognose bei Katheterablation

Invasive Zahnbehandlung: Wann eine Antibiotikaprophylaxe vor infektiöser Endokarditis schützt

Zell-Organisatoren unter Druck: Mechanismen des embryonalen Zahnwachstums aufgedeckt

Die Oralprophylaxe & Kinderzahnheilkunde umbenannt

Newsletter

Live-Webinar: Aktuelle Leitlinien bei Herz-Kreislauf-Erkrankungen

Springer Medizin

Abstract

Objectives

Materials and methods

Results

Conclusion

Clinical relevance

Bitte loggen Sie sich ein, um Zugang zu diesem Inhalt zu erhalten

Weitere Artikel der Ausgabe 8/2018

Treatment of intrabony defects with modified perforated membranes in aggressive periodontitis: a 12-month randomized controlled trial

Ten-year survival and chipping rates and clinical quality grading of zirconia-based fixed dental prostheses

Dental radiographic findings in 18 individuals with SATB2-associated syndrome

N-acetyl-l-cysteine protects dental tissue stem cells against oxidative stress in vitro

Neu im Fachgebiet Zahnmedizin

Parodontalbehandlung verbessert Prognose bei Katheterablation

Invasive Zahnbehandlung: Wann eine Antibiotikaprophylaxe vor infektiöser Endokarditis schützt

Zell-Organisatoren unter Druck: Mechanismen des embryonalen Zahnwachstums aufgedeckt

Die Oralprophylaxe & Kinderzahnheilkunde umbenannt

Newsletter