Investigation of the Effect of Type 2 Diabetes Mellitus on Subgingival Plaque Microbiota by High-Throughput 16S rDNA Pyrosequencing

PLoS ONE

Volumn 8, Issue 4, 2013, Pages

  Zhou, Mi ^a   Rong, Ruichen ^b   Munro, Daniel ^b   Zhu, Chunxia ^a   Gao, Xiang ^b   Zhang, Qi ^a,c   Dong, Qunfeng ^b  

^a WUHAN UNIVERSITY   (China)

^b UNIVERSITY OF NORTH TEXAS   (United States)

^c TONGJI UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

DNA 16S; BACTERIAL DNA; RIBOSOME DNA;

ACTINOBACTERIA; ACTINOMYCES; ADULT; AGED; AGGREGATIBACTER; ARTICLE; BACTERIUM CULTURE; BACTERIUM ISOLATION; BIODIVERSITY; CHRONIC PERIODONTITIS; CLINICAL ARTICLE; CONTROLLED STUDY; DNA SEQUENCE; FEMALE; HIGH THROUGHPUT SEQUENCING; HUMAN; MICROBIAL COMMUNITY; MOLECULAR CLONING; MOUTH FLORA; MOUTH PLAQUE; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; POPULATION ABUNDANCE; PREVOTELLA; PROTEOBACTERIA; PSEUDOMONAS; PYROSEQUENCING; SPECIES COMPOSITION; SUBLINGUAL GLAND; TANNERELLA; BACTERIA; CLASSIFICATION; COMPLICATION; GENETICS; GINGIVA; MICROBIOLOGY; MICROFLORA; MIDDLE AGED; PERIODONTITIS;

ACTINOBACTERIA; ACTINOMYCES; BACTERIA (MICROORGANISMS); OTUS; PREVOTELLA; PROTEOBACTERIA; PSEUDOMONAS; TANNERELLA;

ADULT; AGED; BACTERIA; DIABETES MELLITUS, TYPE 2; DNA, BACTERIAL; DNA, RIBOSOMAL; GINGIVA; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; HUMANS; MICROBIOTA; MIDDLE AGED; PERIODONTITIS; SEQUENCE ANALYSIS, DNA;

EID: 84876427116     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0061516     Document Type: Article

References (80)

1. Graves DT, Li J, Cochran DL, (2011) Inflammation and uncoupling as mechanisms of periodontal bone loss. J Dent Res 90: 143-153.
2. Pihlstrom BL, Michalowicz BS, Johnson NW, (2005) Periodontal diseases. Lancet 366: 1809-1820.
3. Socransky SS, Haffajee AD, (2005) Periodontal microbial ecology. Periodontol 2000 38: 135-187.
4. Griffen AL, Beall CJ, Campbell JH, Firestone ND, Kumar PS, et al. (2012) Distinct and complex bacterial profiles in human periodontitis and health revealed by 16S pyrosequencing. ISME J 6: 1176-1185.
5. Liu B, Faller LL, Klitgord N, Mazumdar V, Ghodsi M, et al. (2012) Deep sequencing of the oral microbiome reveals signatures of periodontal disease. PLoS One 7: e37919.
6. Taylor GW, (2001) Bidirectional interrelationships between diabetes and periodontal diseases: an epidemiologic perspective. Ann Periodontol 6: 99-112.
7. Nelson RG, Shlossman M, Budding LM, Pettitt DJ, Saad MF, et al. (1990) Periodontal disease and NIDDM in Pima Indians. Diabetes Care 13: 836-840.
8. Shlossman M, Knowler WC, Pettitt DJ, Genco RJ, (1990) Type 2 diabetes mellitus and periodontal disease. J Am Dent Assoc 121: 532-536.
9. Loe H, (1993) Periodontal disease. The sixth complication of diabetes mellitus. Diabetes Care 16: 329-334.
10. Lakschevitz F, Aboodi G, Tenenbaum H, Glogauer M, (2011) Diabetes and periodontal diseases: interplay and links. Curr Diabetes Rev 7: 433-439.
11. Taylor GW, Borgnakke WS, (2008) Periodontal disease: associations with diabetes, glycemic control and complications. Oral Dis 14: 191-203.
12. Mealey BL, Oates TW, (2006) Diabetes mellitus and periodontal diseases. J Periodontol 77: 1289-1303.
13. Taylor GW, Burt BA, Becker MP, Genco RJ, Shlossman M, et al. (1996) Severe periodontitis and risk for poor glycemic control in patients with non-insulin-dependent diabetes mellitus. J Periodontol 67: 1085-1093.
14. Lalla E, Papapanou PN, (2011) Diabetes mellitus and periodontitis: a tale of two common interrelated diseases. Nat Rev Endocrinol 7: 738-748.
15. Salvi GE, Collins JG, Yalda B, Arnold RR, Lang NP, et al. (1997) Monocytic TNF alpha secretion patterns in IDDM patients with periodontal diseases. J Clin Periodontol 24: 8-16.
16. Salvi GE, Yalda B, Collins JG, Jones BH, Smith FW, et al. (1997) Inflammatory mediator response as a potential risk marker for periodontal diseases in insulin-dependent diabetes mellitus patients. J Periodontol 68: 127-135.
17. Karima M, Kantarci A, Ohira T, Hasturk H, Jones VL, et al. (2005) Enhanced superoxide release and elevated protein kinase C activity in neutrophils from diabetic patients: association with periodontitis. J Leukoc Biol 78: 862-870.
18. Ohnishi T, Bandow K, Kakimoto K, Machigashira M, Matsuyama T, et al. (2009) Oxidative stress causes alveolar bone loss in metabolic syndrome model mice with type 2 diabetes. J Periodontal Res 44: 43-51.
19. Lalla E, Lamster IB, Drury S, Fu C, Schmidt AM, (2000) Hyperglycemia, glycoxidation and receptor for advanced glycation endproducts: potential mechanisms underlying diabetic complications, including diabetes-associated periodontitis. Periodontol 2000 23: 50-62.
20. Marette A, (2004) Pathogenic role of inflammatory cytokines in obesity: from insulin resistance to diabetes mellitus. Nestle Nutr Workshop Ser Clin Perform Programme 9: 141-150; discussion 151-143.
21. Alexandraki K, Piperi C, Kalofoutis C, Singh J, Alaveras A, et al. (2006) Inflammatory process in type 2 diabetes: The role of cytokines. Ann N Y Acad Sci 1084: 89-117.
22. Kardesler L, Buduneli N, Cetinkalp S, Lappin D, Kinane DF, (2011) Gingival crevicular fluid IL-6, tPA, PAI-2, albumin levels following initial periodontal treatment in chronic periodontitis patients with or without type 2 diabetes. Inflamm Res 60: 143-151.
23. King GL, (2008) The role of inflammatory cytokines in diabetes and its complications. J Periodontol 79: 1527-1534.
24. Preshaw PM, Alba AL, Herrera D, Jepsen S, Konstantinidis A, et al. (2012) Periodontitis and diabetes: a two-way relationship. Diabetologia 55: 21-31.
25. 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.
26. Ohlrich EJ, Cullinan MP, Leichter JW, (2010) Diabetes, periodontitis, and the subgingival microbiota. J Oral Microbiol 2.
27. Mashimo PA, Yamamoto Y, Slots J, Park BH, Genco RJ, (1983) The periodontal microflora of juvenile diabetics. Culture, immunofluorescence, and serum antibody studies. J Periodontol 54: 420-430.
28. Thorstensson H, Dahlen G, Hugoson A, (1995) Some suspected periodontopathogens and serum antibody response in adult long-duration insulin-dependent diabetics. J Clin Periodontol 22: 449-458.
29. Sbordone L, Ramaglia L, Barone A, Ciaglia RN, Iacono VJ, (1998) Periodontal status and subgingival microbiota of insulin-dependent juvenile diabetics: a 3-year longitudinal study. J Periodontol 69: 120-128.
30. Hintao J, Teanpaisan R, Chongsuvivatwong V, Ratarasan C, Dahlen G, (2007) The microbiological profiles of saliva, supragingival and subgingival plaque and dental caries in adults with and without type 2 diabetes mellitus. Oral Microbiol Immunol 22: 175-181.
31. Lalla E, Kaplan S, Chang SM, Roth GA, Celenti R, et al. (2006) Periodontal infection profiles in type 1 diabetes. J Clin Periodontol 33: 855-862.
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.
33. Yuan K, Chang CJ, Hsu PC, Sun HS, Tseng CC, et al. (2001) Detection of putative periodontal pathogens in non-insulin-dependent diabetes mellitus and non-diabetes mellitus by polymerase chain reaction. J Periodontal Res 36: 18-24.
34. Sardi JC, Duque C, Camargo GA, Hofling JF, Goncalves 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.
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.
36. Margulies M, Egholm M, Altman WE, Attiya S, Bader JS, et al. (2005) Genome sequencing in microfabricated high-density picolitre reactors. Nature 437: 376-380.
37. Human Microbiome Consortium (2012) Structure, function and diversity of the healthy human microbiome. Nature 486: 207-214.
38. Lazarevic V, Whiteson K, Hernandez D, Francois P, Schrenzel J, (2010) Study of inter- and intra-individual variations in the salivary microbiota. BMC Genomics 11: 523.
39. Dong Q, Nelson DE, Toh E, Diao L, Gao X, et al. (2011) The microbial communities in male first catch urine are highly similar to those in paired urethral swab specimens. PLoS One 6: e19709.
40. Dong Q, Brulc JM, Iovieno A, Bates B, Garoutte A, et al. (2011) Diversity of bacteria at healthy human conjunctiva. Invest Ophthalmol Vis Sci.
41. Wolfe AJ, Toh E, Shibata N, Rong R, Kenton K, et al. (2012) Evidence of uncultivated bacteria in the adult female bladder. J Clin Microbiol 50: 1376-1383.
42. Ahn J, Yang L, Paster BJ, Ganly I, Morris L, et al. (2011) Oral microbiome profiles: 16S rRNA pyrosequencing and microarray assay comparison. PLoS One 6: e22788.
43. Hooda S, Boler BM, Serao MC, Brulc JM, Staeger MA, et al. (2012) 454 pyrosequencing reveals a shift in fecal microbiota of healthy adult men consuming polydextrose or soluble corn fiber. J Nutr 142: 1259-1265.
44. Casarin RC, Barbagallo A, Meulman T, Santos VR, Sallum EA, et al. (2012) Subgingival biodiversity in subjects with uncontrolled type-2 diabetes and chronic periodontitis. J Periodontal Res.
45. Hartroth B, Seyfahrt I, Conrads G, (1999) Sampling of periodontal pathogens by paper points: evaluation of basic parameters. Oral Microbiol Immunol 14: 326-330.
46. Tanner AC, Goodson JM, (1986) Sampling of microorganisms associated with periodontal disease. Oral Microbiol Immunol 1: 15-22.
47. Paster BJ, Boches SK, Galvin JL, Ericson RE, Lau CN, et al. (2001) Bacterial diversity in human subgingival plaque. J Bacteriol 183: 3770-3783.
48. Kumar PS, Brooker MR, Dowd SE, Camerlengo T, (2011) Target region selection is a critical determinant of community fingerprints generated by 16S pyrosequencing. PLoS One 6: e20956.
49. Shumway M, Cochrane G, Sugawara H, (2010) Archiving next generation sequencing data. Nucleic Acids Res 38: D870-871.
50. Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, et al. (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75: 7537-7541.
51. Hawlena H, Rynkiewicz E, Toh E, Alfred A, Durden LA, et al. (2012) The arthropod, but not the vertebrate host or its environment, dictates bacterial community composition of fleas and ticks. ISME J.
52. Stackebrandt E, Goebel BM, (1994) A place for DNA-DNA reassociation and 16S rRNA sequence analysis in the present species definition in bacteriology. Int J Syst Bacteriol 44: 846-849.
53. Quince C, Lanzen A, Curtis TP, Davenport RJ, Hall N, et al. (2009) Accurate determination of microbial diversity from 454 pyrosequencing data. Nat Methods 6: 639-641.
54. Kunin V, Engelbrektson A, Ochman H, Hugenholtz P, (2010) Wrinkles in the rare biosphere: pyrosequencing errors can lead to artificial inflation of diversity estimates. Environ Microbiol 12: 118-123.
55. Fettweis JM, Serrano MG, Sheth NU, Mayer CM, Glascock AL, et al. (2012) Species-level classification of the vaginal microbiome. BMC Genomics 13 Suppl 8: S17.
56. Wang Q, Garrity GM, Tiedje JM, Cole JR, (2007) Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73: 5261-5267.
57. Johnson M, Zaretskaya I, Raytselis Y, Merezhuk Y, McGinnis S, et al. (2008) NCBI BLAST: a better web interface. Nucleic Acids Res 36: W5-9.
58. Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, et al. (2013) The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res 41: D590-596.
59. Chen T, Yu WH, Izard J, Baranova OV, Lakshmanan A, et al. (2010) The Human Oral Microbiome Database: a web accessible resource for investigating oral microbe taxonomic and genomic information. Database (Oxford) 2010: baq013.
60. McMurdie PJ, Holmes S, (2012) Phyloseq: a bioconductor package for handling and analysis of high-throughput phylogenetic sequence data. Pac Symp Biocomput pp. 235-246.
61. Oksanen J, Kindt R, Legendre P, O'Hara RB, Simpson GL, et al. (2012) vegan: Community Ecology Package. R package version 20-5.
62. Lozupone C, Lladser ME, Knights D, Stombaugh J, Knight R, (2011) UniFrac: an effective distance metric for microbial community comparison. ISME J 5: 169-172.
63. Kumar PS, Griffen AL, Barton JA, Paster BJ, Moeschberger ML, et al. (2003) New bacterial species associated with chronic periodontitis. J Dent Res 82: 338-344.
64. 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.
65. Ashimoto A, Chen C, Bakker I, Slots J, (1996) Polymerase chain reaction detection of 8 putative periodontal pathogens in subgingival plaque of gingivitis and advanced periodontitis lesions. Oral Microbiol Immunol 11: 266-273.
66. Socransky SS, Haffajee AD, Cugini MA, Smith C, Kent RL Jr, (1998) Microbial complexes in subgingival plaque. J Clin Periodontol 25: 134-144.
67. Holt SC, Ebersole JL, (2005) Porphyromonas gingivalis, Treponema denticola, and Tannerella forsythia: the "red complex", a prototype polybacterial pathogenic consortium in periodontitis. Periodontol 2000 38: 72-122.
68. Moter A, Hoenig C, Choi BK, Riep B, Gobel UB, (1998) Molecular epidemiology of oral treponemes associated with periodontal disease. J Clin Microbiol 36: 1399-1403.
69. Colombo AP, Boches SK, Cotton SL, Goodson JM, Kent R, et al. (2009) Comparisons of subgingival microbial profiles of refractory periodontitis, severe periodontitis, and periodontal health using the human oral microbe identification microarray. J Periodontol 80: 1421-1432.
70. Colombo AP, Bennet S, Cotton SL, Goodson JM, Kent R, et al. (2012) Impact of periodontal therapy on the subgingival microbiota of severe periodontitis: comparison between good responders and individuals with refractory periodontitis using the human oral microbe identification microarray. J Periodontol 83: 1279-1287.
71. Shaddox LM, Huang H, Lin T, Hou W, Harrison PL, et al. (2012) Microbiological characterization in children with aggressive periodontitis. J Dent Res 91: 927-933.
72. Nadkarni MA, Browne GV, Chhour KL, Byun R, Nguyen KA, et al. (2012) Pattern of distribution of Prevotella species/phylotypes associated with healthy gingiva and periodontal disease. Eur J Clin Microbiol Infect Dis 31: 2989-2999.
73. Holdeman LV, Moore WE, Cato EP, Burmeister JA, Palcanis KG, et al. (1985) Distribution of capnocytophaga in periodontal microfloras. J Periodontal Res 20: 475-483.
74. Socransky SS, Holt SC, Leadbetter ER, Tanner AC, Savitt E, et al. (1979) Capnocytophaga: new genus of gram-negative gliding bacteria. III. Physiological characterization. Arch Microbiol 122: 29-33.
75. Campus G, Salem A, Uzzau S, Baldoni E, Tonolo G, (2005) Diabetes and periodontal disease: a case-control study. J Periodontol 76: 418-425.
76. Li C, Liu J, Tan L, Yu N, Lin L, et al. (2012) The Sociodemographic Characteristics, Periodontal Health Status, and Subgingival Microbiota of Chronic Periodontitis Patients With Type 2 Diabetes Mellitus: A Case Control Study in a Chinese Population. J Periodontol.
77. Haffajee AD, Bogren A, Hasturk H, Feres M, Lopez NJ, et al. (2004) Subgingival microbiota of chronic periodontitis subjects from different geographic locations. J Clin Periodontol 31: 996-1002.
78. Kim TS, Kang NW, Lee SB, Eickholz P, Pretzl B, et al. (2009) Differences in subgingival microflora of Korean and German periodontal patients. Arch Oral Biol 54: 223-229.
79. Liljemark WF, Bloomquist C, (1996) Human oral microbial ecology and dental caries and periodontal diseases. Crit Rev Oral Biol Med 7: 180-198.
80. Paster BJ, Olsen I, Aas JA, Dewhirst FE, (2006) The breadth of bacterial diversity in the human periodontal pocket and other oral sites. Periodontol 2000 42: 80-87.