Skip to main content

The relationship between physiologic halitosis and periodontopathic bacteria of the tongue and gingival sulcus

Odontology volume 98, pages 44–51 (2010)Cite this article

Abstract

To determine the influence of oral status on halitosis, the relationship between halitosis and periodontopathic bacteria present in plaque on the tongue and the subgingival sulcus was examined in 62 periodontally healthy adults. Halitosis indicators used were the organoleptic score; gas chromatography results [total volatile sulfur compounds (VSCs) = H2S + CH3SH + (CH3)2S]; Halimeter values; and the results of three clinical tests, plaque control record (PlCR), plaque index (PlI), and tongue coat status. Significant correlations with organoleptic scores was observed for PlCR, PlI, tongue coat status, VSC amounts, and Halimeter values, indicating that halitosis in periodontally healthy subjects tended to originate from tongue plaque deposits. Polymerase chain reaction analysis was used to detect six periodontopathic bacteria (Aggregatibacter actinomycetemcomitans, Fusobacterium nucleatum, Porphyromonas gingivalis, Prevotella intermedia, Tannerella forsythensis, and Treponema denticola) from the tongue and subgingival plaque. Significant effects on the organoleptic scores, tongue coat status, total VSC, H2S and CH3SH amounts, and Halimeter values were observed only for T. denticola and F. nucleatum and only in the tongue plaque, not in the subgingival plaque. Thus, therapies developed to inhibit the growth of these bacteria may lead to future treatments of halitosis.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

43,34 €

Price includes VAT (Finland)
Tax calculation will be finalised during checkout.

References

  1. Statistics and Information Department, Minister’s Secretariat, Ministry of Health, Labour and Welfare. In: Survey on trends of health and welfare 1999. Japan: Health and Welfare Statistics Association; 2001. p. 8–12.

    Google Scholar 

  2. Tonzetich J. Production and origin of oral malodor: a review of mechanisms and methods of analysis. J Periodontol 1977;48:13–20.

    PubMed  Google Scholar 

  3. Yaegaki K, Sanada K. Volatile sulfur compounds in mouth air from clinically healthy subjects and patients with periodontal disease. J Periodont Res 1992;27:233–238.

    Article  PubMed  Google Scholar 

  4. Tonzetich J. Oral malodor: an indicator of health status and oral cleanliness. Int Dent J 1973;28:309–319.

    Google Scholar 

  5. Saito S, Ohmori M, Katsuragi H. Factors in physiological breath odor. J Jpn Soc Periodontol 2002;44:168–177.

    Google Scholar 

  6. Bosy A, Kulkarni GV, Rosenberg M, McCulloch CAG. Relationship of oral malodor to periodontitis: evidence of independence in discrete subpopulations. J Periodontol 1994;65:37–46.

    PubMed  Google Scholar 

  7. Rosenberg M. Clinical assessment of bad breath. J Am Dent Assoc 1996;127:475–482.

    PubMed  Google Scholar 

  8. Rooth G, Ostenson S. Acetone in alveolar air, and the control of diabetes. Lancet 1996;19:1102–1105.

    Google Scholar 

  9. Simenhoff ML, Burke JF, Saukkonen JJ, Ordinario AT, Doty R. Biochemical profile of uremic breath. N Engl J Med 1977;297:132–135.

    PubMed  Article  Google Scholar 

  10. Tjoa S, Fennessey P. The identification of trimethylamine excess in man: quantitative analysis and biochemical origins. Anal Biochem 1991;197:77–82.

    Article  PubMed  Google Scholar 

  11. Messadi DV, Younai FS. Halitosis. Dermatol Clin 2003;21:147–155.

    Article  PubMed  Google Scholar 

  12. Miyazaki H, Sakao S, Katoh Y, Takehara T. Correlation between volatile sulphur compounds and certain oral health measurements in the general population. J Periodontol 1995;66:679–684.

    PubMed  Google Scholar 

  13. Ohmori M, Imai R, Satoh S, Hori R, Hasegawa A. A study of daily in physiological oral malodor. J Jpn Soc Periodontol 1999;42:43–48.

    Google Scholar 

  14. Yaegaki K, Coil JM. Examination, classification and treatment of halitosis. J Can Dent Assoc 2000;66:257–261.

    PubMed  Google Scholar 

  15. Tonzetich J. Direct gas chromatographic analysis of sulphur compounds in mouth air in man. Arch Oral Biol 1971;16:587–597.

    Article  PubMed  Google Scholar 

  16. Tonzetich J, Carpenter PA. Production of volatile sulphur compounds from cysteine, cystine and methionine by human dental plaque. Archs Oral Biol 1971;16:599–607.

    Article  Google Scholar 

  17. Yaegaki K, Sanada K. Biochemical and clinical factor influencing oral malodor periodontal patients. J Periodontol 1992;63:783–789.

    PubMed  Google Scholar 

  18. Persson S, Edlund MB, Claesson R, Carlsson J. The formation of hydrogen sulfide and methyl mercaptan by oral bacteria. Oral Microbiol Immunol 1990;5:195–201.

    Article  PubMed  Google Scholar 

  19. Loesche WJ, Lopatin DE, Giordano J, Alcoforado G, Hujoel P. Comparison of the benzoyl-DL-arginine-naphthylamide (BANA) test, DNA probes, and immunological reagents for ability to detect anaerobic periodontal infection due to Porphyromonas gingivalis, Treponema denticola, and Bacteroides forsythus. J Clin Microbiol 1992;30:427–433.

    PubMed  Google Scholar 

  20. Löe H. The gingival index, the plaque index and the retention index systems. J Periodontol 1967;38:610–616.

    PubMed  Google Scholar 

  21. Satoh S, Ohmori M, Murayama K, Nakamura T, Saitoh M, Imai R, Hori R, Hasegawa A. A study of measurement of oral malodor with a portable sulfide monitor Halimeter®. J Jpn Soc Periodontol 1999;41:195–200.

    Google Scholar 

  22. Rosenberg M, Kulkarni GV, Bosy A, McCulloch CA. Reproducibility and sensitivity of oral malodor measurements with a portable sulphide monitor. J Dent Res 1991;70:1436–1440.

    PubMed  Google Scholar 

  23. Tonzetich J, Ng SK. Reduction of malodor by oral cleansing procedures. Oral Surg Oral Med Oral Pathol 1976;42:172–181.

    Article  PubMed  Google Scholar 

  24. O’Leary TJ, Dranke RB, Naylor JE. The plaque control record. J Periodontol 1972;43:38.

    PubMed  Google Scholar 

  25. Silness J, Löe H. Periodontal disease in pregnancy. II. Correlation between oral hygiene and periodontal condition. Acta Odontol Scand 1964;22:121–135.

    Article  PubMed  Google Scholar 

  26. Kojima K. Clinical studies on the coated tongue. Jpn J Oral Maxillofac 1985;31:1659–1678.

    Google Scholar 

  27. Christersson LA, Albini B, Joseph JJ, Wikesjo UM, Genco RJ. Tissue localization of Actinobacillus actinomycetemcomitans in human periodontitis I. Light, immunofluorescence and electron microscopic studies. J Periodontol 1987;58:529–539.

    PubMed  Google Scholar 

  28. 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;11:266–273.

    Article  PubMed  Google Scholar 

  29. Baumgartner JC, Siqueira JF Jr, Xia T, Rocas IN. Geographical differences in bacteria in endodontic infections using polymerase chain reaction. J Endod 2004;30:141–144.

    Article  PubMed  Google Scholar 

  30. Moriya T, Kishi M, Aizawa F, Minami K, Yonemitsu M. Tongue coating score as a screening test for oral malodor. J Dent Health 2002;52:12–21.

    Google Scholar 

  31. Tonzetich J, Kestenbaum RC. Odor production by human salivary fractions and plaque. Arch Oral Biol 1969;14:815–827.

    Article  PubMed  Google Scholar 

  32. Solis-Gaffar MC, Niles HP, Rainieri WC, Kestenbaum RC. Instrumental evaluation of mouth odor in a human clinical study. J Dent Res 1975;54:351–357.

    PubMed  Google Scholar 

  33. Dahlen G, Manji F, Baelum V, Fejerskov O. Putative periodontopathogens in diseased and non-diseased persons exhibiting poor oral hygiene. J Clin Periodontol 1992;19:35–42.

    Article  PubMed  Google Scholar 

  34. Kishi M, Kimura S, Ohara Y, Kishi K, Aizawa F, Moriya T, Yonemitsu M. Oral malodor and periodontopathic microorganisms in tongue coat of periodontally healthy subjects. Dent Japan 2002;38:24–28.

    Google Scholar 

  35. Takahashi M, Kishi M. Relationship between dental pathogenic bacteria in tongue coat and clinical oral status. J Dent Health 2006;56:137–147.

    Google Scholar 

  36. Tonetti MS, Mombelli A. Clinical periodontology and implant dentistry. In: Lindhe J, Karring T, Lang NP, editors. Aggressive periodontitis. 9th ed. Oxford: Blackwell Munksgaard; 2003. p. 216–242.

    Google Scholar 

  37. Palmer R, Soory M. Clinical periodontology and implant dentistry. In: Lindhe J, Karring T, Lang NP, editors. Modifying factors: diabetes, puberty, pregnancy and the menopause and tobacco smoking. 6th ed. Oxford: Blackwell Munksgaard; 2003. p.179–197.

    Google Scholar 

  38. Tonzetich J, Preti G, Huggins GR. Changes in concentration of volatile sulphur compounds of mouth air during the menstrual cycle. J Int Med Res 1978;6:245–254.

    PubMed  Google Scholar 

  39. Claesson R, Edlund MB, Persson S, Carlsson J. Production of volatile sulfur compounds by various Fusobacterium species. Oral Microbiol Immunol 1990;5:137–142.

    Article  PubMed  Google Scholar 

  40. Shibuya K. Constituents and origins of physiological malodor. J Dent Health 2001;51:778–792.

    Google Scholar 

  41. Goldberg S, Kozlovsky A, Gordon D, Gelenter I, Sintov A, Rosenberg M. Cadaverine as putative component of oral malodor. J Dent Res 1994;73:1168–1172.

    PubMed  Google Scholar 

  42. Tonzetich J, Coil JM, Ng W. Gas chromatographic method for trapping and detection of volatile organic compounds from human mouth air. J Clin Dent 1991;2:79–82.

    PubMed  Google Scholar 

  43. Tanaka M, Yamamoto Y, Kuboniwa M, Nonaka A, Nishida N, Maeda K, Kataoka K, Nagata H, Shizukuishi S. Contribution of periodontal pathogens on tongue dorsa analyzed with real-time PCR to oral malodor. Microbes Infect 2004;6:1078–1083.

    Article  PubMed  Google Scholar 

  44. Awano S, Gohara K, Kurihara E, Ansai T, Takehara T. The relationship between the presence of periodontopathogenic bacteria in saliva and halitosis. Int Dent J 2002;52:212–216.

    PubMed  Google Scholar 

Download references

Author information

Affiliations

  1. Department of Periodontology, The Nippon Dental University School of Life Dentistry at Niigata, 1-8 Hamaura-cho, Chuo-ku, Niigata, 951-8580, Japan

    Toshiyuki Yasukawa & Soh Sato

  2. Comprehensive Dental Care, The Nippon Dental University Niigata Hospital, Niigata, Japan

    Misaki Ohmori

Authors
  1. Toshiyuki Yasukawa
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Misaki Ohmori
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Soh Sato
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Toshiyuki Yasukawa.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Yasukawa, T., Ohmori, M. & Sato, S. The relationship between physiologic halitosis and periodontopathic bacteria of the tongue and gingival sulcus. Odontology 98, 44–51 (2010). https://doi.org/10.1007/s10266-009-0114-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10266-009-0114-7

Key words

  • Physiologic halitosis
  • Periodontopathic bacteria
  • Gas chromatography
  • Tongue plaque
  • Subgingival plaque