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Clinical Oral Investigations

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01-12-2012 | Original Article

Quantitative analysis of microbiota in saliva, supragingival, and subgingival plaque of Chinese adults with chronic periodontitis

Authors: Jiayan He, Wujing Huang, Zhiwen Pan, Honghua Cui, Ganggang Qi, Xueping Zhou, Hui Chen

Published in: Clinical Oral Investigations | Issue 6/2012

Abstract

Objective

The aim of this study was to determine the profiles of periodontopathogenic bacteria in a Chinese population using quantitative real-time polymerase chain reaction (qRT-PCR).

Materials and methods

Twenty-four periodontally healthy Chinese subjects and 60 patients with chronic periodontitis (CP) were enrolled in this cross-sectional study. qRT-PCR was used to quantify Aggregatibacter actinomycetemcomitans, Fusobacterium nucleatum, Porphyromonas gingivalis, and Prevotella intermedia as well as total bacterial counts from 252 samples collected from the saliva, supragingival plaque, and subgingival plaque of all 84 subjects.

Results

The detection frequency of A. actinomycetemcomitans was less than 50%. F. nucleatum was detected in all subjects and CP patients had higher bacterial loads than healthy subjects. The median proportion of F. nucleatum was significantly higher in subgingival plaque than in supragingival plaque and saliva. P. gingivalis and P. intermedia had higher detection frequencies and bacterial loads in CP patients than in healthy subjects. The median proportion of P. gingivalis was significantly different among the three intraoral locations in the CP group and its proportion in subgingival plaque was 9.01%. Moreover, strong positive Spearman’s correlations were found in A. actinomycetemcomitans, P. gingivalis, and P. intermedia counts across the three intraoral locations.

Conclusion

The presence and bacteria loads of these four bacteria in this Chinese population are similar to those from other populations.

Clinical relevance

Examination of bacterial detection frequency and loads in Chinese adults may assist microbial studies of periodontal disease and will shed light on periodontal disease diagnosis and treatment using antibiotics in the Chinese population.

Corbet EF, Zee KY, Lo EC (2002) Periodontal diseases in Asia and Oceania. Periodontol 2000 29:122–152PubMedCrossRef

Demmer RT, Papapanou PN (2010) Epidemiologic patterns of chronic and aggressive periodontitis. Periodontol 2000 53:28–44PubMedCrossRef

Chen H, Zheng P, Zhu H, Zhu J, Zhao L, El Mokhtari NE, Eberhard J, Lins M, Jepsen S (2010) Platelet-activating factor levels of serum and gingival crevicular fluid in nonsmoking patients with periodontitis and/or coronary heart disease. Clin Oral Investig 14:629–636PubMedCrossRef

Zheng P, Chen H, Shi S, Jepsen S, Eberhard J (2006) Periodontal parameters and platelet-activating factor levels in serum and gingival crevicular fluid in a Chinese population. J Clin Periodontol 33:797–802PubMedCrossRef

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 42:80–87PubMedCrossRef

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

Socransky SS, Haffajee AD (2005) Periodontal microbial ecology. Periodontol 2000 38:135–187PubMedCrossRef

Armitage GC (2010) Comparison of the microbiological features of chronic and aggressive periodontitis. Periodontol 2000(53):70–88CrossRef

Slots J, Ting M (1999) Actinobacillus actinomycetemcomitans and Porphyromonas gingivalis in human periodontal disease: occurrence and treatment. Periodontol 2000 20:82–121PubMedCrossRef

10.

Teles RP, Haffajee AD, Socransky SS (2006) Microbiological goals of periodontal therapy. Periodontol 2000 42:180–218PubMedCrossRef

11.

Riep B, Edesi-Neuss L, Claessen F, Skarabis H, Ehmke B, Flemmig TF, Bernimoulin JP, Gobel UB, Moter A (2009) Are putative periodontal pathogens reliable diagnostic markers? J Clin Microbiol 47:1705–1711PubMedCrossRef

12.

Shaddox LM, Walker C (2009) Microbial testing in periodontics: value, limitations and future directions. Periodontol 2000 50:25–38PubMedCrossRef

13.

Herrera D, Contreras A, Gamonal J, Oteo A, Jaramillo A, Silva N, Sanz M, Botero JE, Leon R (2008) Subgingival microbial profiles in chronic periodontitis patients from Chile, Colombia and Spain. J Clin Periodontol 35:106–113PubMedCrossRef

14.

Psoter WJ, Ge Y, Russell SL, Chen Z, Katz RV, Jean-Charles G, Li Y (2010) PCR detection of Streptococcus mutans and Aggregatibacter actinomycetemcomitans in dental plaque samples from Haitian adolescents. Clin Oral Investig 15:461–469PubMedCrossRef

15.

Wara-aswapati N, Pitiphat W, Chanchaimongkon L, Taweechaisupapong S, Boch JA, Ishikawa I (2009) Red bacterial complex is associated with the severity of chronic periodontitis in a Thai population. Oral Dis 15:354–359PubMedCrossRef

16.

Yang HW, Huang YF, Chou MY (2004) Occurrence of Porphyromonas gingivalis and Tannerella forsythensis in periodontally diseased and healthy subjects. J Periodontol 75:1077–1083PubMedCrossRef

17.

Dahlen GG, Luan WM, Baelum V, Fejerskov O, Chen X (1995) Periodontopathogens in elderly Chinese with different periodontal disease experience. J Clin Periodontol 22:188–200PubMedCrossRef

18.

Meng S, Zhao L, Yang H, Wu Y, Ouyang Y (2009) Prevalence of Actinobacillus actinomycetemcomitans in Chinese chronic periodontitis patients and periodontally healthy adults. Quintessence Int 40:53–60PubMed

19.

Mombelli A, Gmur R, Frey J, Meyer J, Zee KY, Tam JO, Lo EC, Di Rienzo J, Lang NP, Corbet EF (1998) Actinobacillus actinomycetemcomitans and Porphyromonas gingivalis in young Chinese adults. Oral Microbiol Immunol 13:231–237PubMedCrossRef

20.

Papapanou PN, Baelum V, Luan WM, Madianos PN, Chen X, Fejerskov O, Dahlen G (1997) Subgingival microbiota in adult Chinese: prevalence and relation to periodontal disease progression. J Periodontol 68:651–666PubMedCrossRef

21.

Jervoe-Storm PM, AlAhdab H, Koltzscher M, Fimmers R, Jepsen S (2010) Quantification of periodontal pathogens by paper point sampling from the coronal and apical aspect of periodontal lesions by real-time PCR. Clin Oral Investig 14:533–541PubMedCrossRef

22.

Sakamoto M, Umeda M, Benno Y (2005) Molecular analysis of human oral microbiota. J Periodontal Res 40:277–285PubMedCrossRef

23.

Syed SA, Loesche WJ (1972) Survival of human dental plaque flora in various transport media. Appl Microbiol 24:638–644PubMed

24.

Novak MJ, Novak KF, Hodges JS, Kirakodu S, Govindaswami M, Diangelis A, Buchanan W, Papapanou PN, Michalowicz BS (2008) Periodontal bacterial profiles in pregnant women: response to treatment and associations with birth outcomes in the obstetrics and periodontal therapy (OPT) study. J Periodontol 79:1870–1879PubMedCrossRef

25.

Maeda H, Fujimoto C, Haruki Y, Maeda T, Kokeguchi S, Petelin M, Arai H, Tanimoto I, Nishimura F, Takashiba S (2003) Quantitative real-time PCR using TaqMan and SYBR Green for Actinobacillus actinomycetemcomitans, Porphyromonas gingivalis, Prevotella intermedia, tetQ gene and total bacteria. FEMS Immunol Med Microbiol 39:81–86PubMedCrossRef

26.

Suzuki N, Yoshida A, Saito T, Kawada M, Nakano Y (2004) Quantitative microbiological study of subgingival plaque by real-time PCR shows correlation between levels of Tannerella forsythensis and Fusobacterium spp. J Clin Microbiol 42:2255–2257PubMedCrossRef

27.

Sakamoto M, Takeuchi Y, Umeda M, Ishikawa I, Benno Y (2001) Rapid detection and quantification of five periodontopathic bacteria by real-time PCR. Microbiol Immunol 45:39–44PubMed

28.

Baumgartner JC, Watkins BJ, Bae KS, Xia T (1999) Association of black-pigmented bacteria with endodontic infections. J Endod 25:413–415PubMedCrossRef

29.

Nadkarni MA, Martin FE, Jacques NA, Hunter N (2002) Determination of bacterial load by real-time PCR using a broad-range (universal) probe and primers set. Microbiology 148:257–266PubMed

30.

Kuboniwa M, Amano A, Kimura KR, Sekine S, Kato S, Yamamoto Y, Okahashi N, Iida T, Shizukuishi S (2004) Quantitative detection of periodontal pathogens using real-time polymerase chain reaction with TaqMan probes. Oral Microbiol Immunol 19:168–176PubMedCrossRef

31.

Ledder RG, Gilbert P, Huws SA, Aarons L, Ashley MP, Hull PS, McBain AJ (2007) Molecular analysis of the subgingival microbiota in health and disease. Appl Environ Microbiol 73:516–523PubMedCrossRef

32.

Parahitiyawa NB, Scully C, Leung WK, Yam WC, Jin LJ, Samaranayake LP (2010) Exploring the oral bacterial flora: current status and future directions. Oral Dis 16:136–145PubMedCrossRef

33.

Lafaurie GI, Contreras A, Baron A, Botero J, Mayorga-Fayad I, Jaramillo A, Giraldo A, Gonzalez F, Mantilla S, Botero A, Archila LH, Diaz A, Chacon T, Castillo DM, Betancourt M, Aya MD, Arce R (2007) Demographic, clinical, and microbial aspects of chronic and aggessive periodontitis in Colombia: a multicenter study. J Periodontol 78:629–639PubMedCrossRef

34.

Nonnenmacher C, Dalpke A, Mutters R, Heeg K (2004) Quantitative detection of periodontopathogens by real-time PCR. J Microbiol Methods 59:117–125PubMedCrossRef

35.

Thiha K, Takeuchi Y, Umeda M, Huang Y, Ohnishi M, Ishikawa I (2007) Identification of periodontopathic bacteria in gingival tissue of Japanese periodontitis patients. Oral Microbiol Immunol 22:201–207PubMedCrossRef

36.

Fine DH, Kaplan JB, Kachlany SC, Schreiner HC (2006) How we got attached to Actinobacillus actinomycetemcomitans: a model for infectious diseases. Periodontol 2000 42:114–157PubMedCrossRef

37.

Koenoenen E, Paju S, Pussinen PJ, Hyvonen M, Di Tella P, Suominen-Taipale L, Knuuttila M (2007) Population-based study of salivary carriage of periodontal pathogens in adults. J Clin Microbiol 45:2446–2451CrossRef

38.

Hamlet SM, Cullinan MP, Westerman B, Lindeman M, Bird PS, Palmer J, Seymour GJ (2001) Distribution of Actinobacillus actinomycetemcomitans, Porphyromonas gingivalis and Prevotella intermedia in an Australian population. J Clin Periodontol 28:1163–1171PubMedCrossRef

39.

Bolstad AI, Jensen HB, Bakken V (1996) Taxonomy, biology, and periodontal aspects of Fusobacterium nucleatum. Clin Microbiol Rev 9:55–71PubMed

40.

van Winkelhoff AJ, Loos BG, van der Reijden WA, van der Velden U (2002) Porphyromonas gingivalis, Bacteroides forsythus and other putative periodontal pathogens in subjects with and without periodontal destruction. J Clin Periodontol 29:1023–1028PubMedCrossRef

41.

Boutaga K, Winkelhoff AJv, Vandenbroucke-Grauls CMJE, Savelkoul PHM (2006) The additional value of real-time PCR in the quantitative detection of periodontal pathogens. J Clin Periodontol 33:427–433PubMedCrossRef

42.

Ximenez-Fyvie LA, Almaguer-Flores A, Jacobo-Soto V, Lara-Cordoba M, Sanchez-Vargas LO, Alcantara-Maruri E (2006) Description of the subgingival microbiota of periodontally untreated Mexican subjects: chronic periodontitis and periodontal health. J Periodontol 77:460–471PubMedCrossRef

43.

Nonnenmacher C, Dalpke A, Rochon J, Flores-de-Jacoby L, Mutters R, Heeg K (2005) Real-time polymerase chain reaction for detection and quantification of bacteria in periodontal patients. J Periodontol 76:1542–1549PubMedCrossRef

44.

Lovegrove JM (2004) Dental plaque revisited: bacteria associated with periodontal disease. J N Z Soc Periodontol 87:7–21PubMed

45.

Ximenez-Fyvie LA, Haffajee AD, Socransky SS (2000) Comparison of the microbiota of supra- and subgingival plaque in health and periodontitis. J Clin Periodontol 27:648–657PubMedCrossRef

46.

Ali RW, Johannessen AC, Dahlen G, Socransky SS, Skaug N (1997) Comparison of the subgingival microbiota of periodontally healthy and diseased adults in northern Cameroon. J Clin Periodontol 24:830–835PubMedCrossRef

47.

Braga RR, Carvalho MA, Bruna-Romero O, Teixeira RE, Costa JE, Mendes EN, Farias LM, Magalhaes PP (2010) Quantification of five putative periodontal pathogens in female patients with and without chronic periodontitis by real-time polymerase chain reaction. Anaerobe 16:234–239PubMedCrossRef

48.

Mager DL, Ximenez-Fyvie LA, Haffajee AD, Socransky SS (2003) Distribution of selected bacterial species on intraoral surfaces. J Clin Periodontol 30:644–654PubMedCrossRef

49.

Boutaga K, Savelkoul PHM, Winkel EG, van Winkelhoff AJ (2007) Comparison of subgingival bacterial sampling with oral lavage for detection and quantification of periodontal pathogens by real-time polymerase chain reaction. J Periodontol 78:79–86PubMedCrossRef

50.

Umeda M, Contreras A, Chen C, Bakker I, Slots J (1998) The utility of whole saliva to detect the oral presence of periodontopathic bacteria. J Periodontol 69:828–833PubMedCrossRef

51.

Matto J, Saarela M, von Troil-Linden B, Alaluusua S, Jousimies-Somer H, Asikainen S (1996) Similarity of salivary and subgingival Prevotella intermedia and Prevotella nigrescens isolates by arbitrarily primed polymerase chain reaction. Oral Microbiol Immunol 11:395–401PubMedCrossRef

Title: Quantitative analysis of microbiota in saliva, supragingival, and subgingival plaque of Chinese adults with chronic periodontitis
Authors: Jiayan He
Wujing Huang
Zhiwen Pan
Honghua Cui
Ganggang Qi
Xueping Zhou
Hui Chen
Publication date: 01-12-2012
Publisher: Springer-Verlag
Published in: Clinical Oral Investigations / Issue 6/2012
Print ISSN: 1432-6981
Electronic ISSN: 1436-3771
DOI: https://doi.org/10.1007/s00784-011-0654-4

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Quantitative analysis of microbiota in saliva, supragingival, and subgingival plaque of Chinese adults with chronic periodontitis

Abstract

Objective

Materials and methods

Results

Conclusion

Clinical relevance

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Abstract

Objective

Materials and methods

Results

Conclusion

Clinical relevance

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