[en] Bad breath (halitosis) is an important social complaint. In most cases (≥90%), the cause of halitosis can be found within the oral cavity. Under this circumstance, the term oral malodor applies. It affects both healthy and periodontally diseased individuals. Oral malodor is mainly caused by a microbial degradation of both sulfur-containing and nonsulfur-containing amino acids into volatile, bad-smelling gases. Anaerobic gram-negative bacteria, the same species that have been linked to periodontal diseases, are especially involved in this process, explaining why clinicians often associate oral malodor with periodontitis. Some volatile organic compounds render patients more susceptible to periodontitis and this supports the malodor-periodontitis link. This review investigates the interaction between oral malodor and periodontal diseases. Pro and con arguments regarding the mechanisms of halitosis and clinical implications will be presented. In general, however, the impact of tongue coatings has been found to be the dominant factor, besides gingivitis and periodontitis. The last part of this review discusses the treatment of bad breath, with different options.
Research center :
d‐BRU - Dental Biomaterials Research Unit - ULiège [BE]
Disciplines :
Dentistry & oral medicine
Author, co-author :
De Geest, Sophie
Laleman, Isabelle ; Centre Hospitalier Universitaire de Liège - CHU > > Service de parodontologie, chirurgie bucco-dentaire et chirurgie implantaire
Teughels, Wim
Dekeyser, Christel
Quirynen, Marc
Language :
English
Title :
Periodontal diseases as a source of halitosis: a review of the evidence and treatment approaches for dentists and dental hygienists.
Addy M, Moran J, Wade W. Chemical plaque control in the prevention of gingivitis and periodontitis. In: Lang NP, Karring T, editors. Proceedings of the 1st European workshop in periodontology. London: Quintessence, 1994: 244-257.
Addy M, Moran J. Clinical indications for the use of chemical adjuncts to plaque control: chlorhexidine formulations. Periodontol 2000 1997: 15: 52-54.
Addy M, Renton-Harper P. The role of antiseptics in secondary prevention. In: Lang NP, Karring T, editors. Proceedings of the second European workshop in periodontology. London: Quintessence, 1997: 152-173.
Apatzidou AD, Bakirtzoglou E, Vouros I, Karagiannis V, Papa A, Konstantinidis A. Association between oral malodour and periodontal disease-related parameters in the general population. Acta Odontol Scand 2013: 71: 189-195.
Aung E, Ueno M, Zaitsu T, Furukawa S, Kawaguchi Y. Effectiveness of three oral hygiene regimens on oral malodor reduction: a randomized clinical trial. Trials 2015: 16: 31.
De Boever EH, Loesche WJ. Assessing the contribution of anaerobic microflora of the tongue to oral malodor. J Am Dent Assoc 1995: 126: 1384-1393.
Bollen C, Quirynen M. Microbiological response to mechanical treatment in combination with adjunctive therapy: a review of the literature. J Periodontol 1996: 67: 1143-1158.
Bosy A, Kulkarni GV, Rosenberg M, McCullough CAG. Relationship of oral malodor to periodontitis: evidence of independence in discrete subpopulations. J Periodontol 1994: 65: 37-46.
Brunette D, Proskin H, Nelson B. The effects of dentifrice systems on oral malodor. J Clin Dent 1998: 9: 76-82.
Calil C, Liberato FL, Pereira AC, de Castro Meneghim M, Goodson JM, Groppo FC. The relationship between volatile sulphur compounds, tongue coating and periodontal disease. Int J Dent Hyg 2009: 7: 251-255.
Carvalho M, Tabchoury C, Cury J, Toledo S, Nogueira-Filho GR. Impact of mouthrinses on morning bad breath in healthy subjects. J Clin Periodontol 2004: 31: 85-90.
Christensen G. Why clean your tongue? J Am Dent Assoc 1998: 129: 1605-1607.
Cicek Y, Orbak R, Tezel A, Orbak Z, Erciyas K. Effect of tongue brushing on oral malodor in adolescents. Pediatr Int 2003: 45: 719-723.
Clark G, Nachnani S, Messadi D. Detecting and treating oral and nonoral malodors. J Calif Dent Assoc 1997: 25: 133-144.
Coil J, Tonzetich J. Characterization of volatile sulfur compounds production at individual gingival cervicular sites in humans. J Clin Dent 1992: 3: 97-103.
Dadamio J, Van Tornhout M, Teughels W. Efficacy of different mouthrinse formulations in reducing oral malodour: a randomized clinical trial. J Clin Periodontol 2013: 40: 505-513.
Delanghe G, Ghyselen J, van Steenberghe D, Feenstra L. Multidisciplinary breath-odor clinic. Lancet 1997: 350: 187.
Feng X, Chen X, Cheng R, Sun L, Zhang Y, He T. Breath malodor reduction with use of a stannous-containing sodium fluoride dentifrice: a meta-analysis of four randomized and controlled clinical trials. Am J Dent 2010: 23: 27B-31B.
Figueiredo LC, Rosetti EP, Marcantonio E Jr, Marcantonio RAC, Salvador SL. The relationship of oral malodor in patients with or without periodontal disease. J Periodontol 2002: 73: 1338-1342.
Frascella J, Gilbert R, Fernandez P, Hendler J. Efficacy of a chlorine dioxide-containing mouthrinse in oral malodor. Compend Contin Educ Dent 2000: 21: 241-244.
Gagari E, Kabani S. Adverse effects of mouthwash use: a review. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 1995: 80: 432-439.
Gerlach R, Hyde J, Poore C, Stevens D, Witt J. Breath effects of three marketed dentifrices: a comparative study evaluating single and cumulative use. J Clin Dent 1998: 9: 83-88.
Gilmore E, Bhaskar S. Effect of tongue brushing on bacteria and plaque formed in vitro. J Periodontol 1972: 43: 418-422.
Gilmore E, Gross A, Whitley R. Effect of tongue brushing on plaque bacteria. Oral Surg Oral Med Oral Pathol 1973: 36: 201-204.
Greenstein R, Goldberg S, Marku-Cohen S, Sterer N, Rosenberg M. Reduction of oral malodor by oxidizing lozenges. J Periodontol 1997: 68: 1176-1181.
Gross A, Barnes G, Lyon T. Effects of tongue brushing on tongue coating and dental plaque scores. J Dent Res 1975: 54: 1236.
Hoshi K, van Steenberghe D. The effect of tongue brushing or toothpaste application on oral malodour reduction. In: van Steenberghe D, Rosenberg M, editors. Bad breath, a multidisciplinary approach. Leuven: Leuven University Press, 1996: 255-264.
Hu D, Zhang Y, Petrone M, Volpe A, DeVizio W, Proskin H. Clinical effectiveness of a triclosan/copolymer/sodium-fluoride dentifrice in controlling oral malodor: a three-week clinical trial. Compend Contin Educ Dent 2003: 24: 34-41.
Jones C. Chlorhexidine: is it still the gold standard? Periodontol 2000 1997: 15: 55-62.
Kleinberg I, Wolff M, Codipilly DM. Role of saliva in oral dryness, oral feel and oral malodour. Int Dent J 2002: 52: 236-240.
Koshimune S, Awano S, Gohara K, Kurihara E, Ansai T, Takehara T. Low salivary flow and volatile sulfur compounds in mouth air. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2003: 96: 38-41.
Kozlovsky A, Goldberg S, Natour I, Rogatky-Gat A, Gerlenter I, Rosenberg M. Efficacy of a 2-phase oil: water mouthrinse in controlling oral malodor, gingivitis, and plaque. J Periodontol 1996: 67: 577-582.
Kozlovsky A, Gordon D, Gelernter I, Loesche WJ, Rosenberg M. Correlation between the BANA test and oral malodor parameters. J Dent Res 1994: 73: 1036-1042.
Kuyyakanond T, Quesnel L. The mechanism of action of chlorhexidine. FEMS Microbiol Lett 1992: 79: 211-215.
Liu XN, Shinada K, Chen XC, Zhang BX, Yaegaki K, Kawaguchi Y. Oral malodor-related parameters in the Chinese general population. J Clin Periodontol 2006: 33: 31-36.
Lopez-Lazaro M. Dual role of hydrogen peroxide in cancer: possible relevance to cancer chemoprevention and therapy. Cancer Lett 2007: 252: 1-8.
Menon M, Coykendall A. Effect of tongue scraping. J Dent Res 1994: 73: 1492.
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.
Morita M, Wang HL. Association between oral malodor and adult periodontitis: a review. J Clin Periodontol 2001: 28: 813-819.
Morita M, Wang HL. Relationship between sulcular sulfide level and oral malodor in subjects with periodontal disease. J Periodontol 2001: 72: 79-84.
Murata M, Mizutani M, Oikawa S, Hiraku Y, Kawanishi S. Oxidative DNA damage by hyperglycemia-related aldehydes and its marked enhancement by hydrogen peroxide. FEBS Lett 2003: 554: 138-142.
Ng W, Tonzetich J. Effect of hydrogen sulfide and methyl mercaptan on the permeability of oral mucosa. J Dent Res 1984: 63: 994-997.
Niles H, Gaffar A. Advances in mouth odor research. In: Rosenberg M, editor. Bad breath: research perspectives. Tel Aviv: Ramot Publishing, 1995: 55-69.
Niles H, Hunter C, Vazquez J, Williams M, Cummins D. The clinical comparison of a triclosan/copolymer/fluoride dentifrice vs a breath-freshening dentifrice in reducing breath odor overnight: a crossover study. Oral Dis 2005: 11: 54-56.
Niles H, Vazquez J, Rustogi K, Williams M, Gaffar A, Proskin H. The clinical effectiveness of a dentifrice containing triclosan and a copolymer for providing long-term control of breath odor measured chromatographically. J Clin Dent 1999: 10: 135-138.
Outhouse T, Al-Alawi R, Fedorowicz Z, Keenan J. Tongue scraping for treating halitosis. Cochrane Database Syst Rev 2006: 19: CD005519.
Pedrazzi V, Sato S, de Mattos Mda G, Lara E, Panzeri H. Tongue-cleaning methods: a comparative clinical trial employing a toothbrush and a tongue scraper. J Periodontol 2006: 75: 1009-1012.
Persson S, Edlund M-B, Claesson R, Carlsson J. The formation of hydrogen sulfide and methyl mercaptan by oral bacteria. Oral Microbiol Immunol 1990: 5: 195-201.
Persson S. Hydrogen sulfide and methylmercaptan in periodontal pockets. Oral Microbiol Immunol 1992: 7: 378-379.
Pham T, Ueno M, Zaitsu T, Takehara S, Shinada K, Lam P, Kawaguchi Y. Clinical trial of oral malodor treatment in patients with periodontal diseases. J Periodontal Res 2011: 46: 722-729.
Pitts G, Brogdon C, Hu L, Masurat T, Pianotti R, Schumann P. Mechanism of action of an antiseptic, anti-odor mouthwash. J Dent Res 1983: 62: 738-742.
Putt M, Milleman K, Ghassemi A, Vorwerk L, Hooper W, Soparkar P, Winston A, Proskin H. Enhancement of plaque removal efficacy by tooth brushing with baking soda dentifrices: results of five clinical studies. J Clin Dent 2008: 19: 111-119.
Quirynen M, Avontroodt P, Soers C, Zhao H, Pauwels M, Coucke W, van Steenberghe D. The efficacy of amine fluoride/stannous fluoride in the suppression of morning breath odour. J Clin Periodontol 2002: 29: 944-954.
Quirynen M, Avontroodt P, Soers C, Zhao H, Pauwels M, van Steenberghe D. Impact of tongue cleansers on microbial load and taste. J Clin Periodontol 2004: 31: 506-510.
Quirynen M, Dadamio J, Van de Velde S, De Smet M, Dekeyser C, Van Tornhout M, Vandekerckhove B. Characteristics of 2000 patients who visited a halitosis clinic. J Clin Periodontol 2009: 36: 970-975.
Quirynen M, Mongardini C, van Steenberghe D. The effect of a 1-Stage Full-mouth disinfection on oral malodor and microbial colonization of the tongue in periodontitis patients. A pilot study. J Periodontol 1998: 69: 374-382.
Quirynen M, Zhao H, Soers C, Dekeyser C, Pauwels M, Coucke W, van Steenberghe D. The impact of periodontal therapy and the adjunctive effect of antiseptics on breath odor-related outcome variables: a double-blind randomized study. J Periodontol 2005: 76: 705-712.
Quirynen M, Zhao H, van Steenberghe D. Review of the treatment strategies for oral malodour. Clin Oral Investig 2002: 6: 1-10.
Ralph W. Oral hygiene-why neglect the tongue? Aust Dent J 1988: 33: 224-225.
Ratcliff PA, Johnson PW. The relationship between oral malodor, gingivitis, and periodontitis: A review. J Periodontol 1999: 70: 485-489.
Raven S, Matheson J, Huntington E. The efficacy of combined zinc and triclosan system in the prevention of oral malodour. In: van Steenberghe D, Rosenberg M, editors. Bad breath: a multidisciplinary approach. Leuven: Leuven University Press, 1996: 247-254.
Rees T, Orth C. Oral ulcerations with use of hydrogen peroxide. J Periodontol 1986: 57: 689-692.
Reingewirtz Y, Girault O, Reingewirtz N, Senger B, Tenenbaum H. Mechanical effects and volatile sulfur compound-reducing effects of chewing gums: comparison between test and base gums and a control group. Quintessence Int 1999: 30: 319-323.
Reiter M, Sawicka A, Baumeister P, Welz C, Schwenk-Zieger S, Harréus U. Chromosomal alterations in mini organ cultures of human oropharyngeal mucosa cells caused by hydrogen peroxide. Cancer Genomics Proteomics 2009: 6: 275-280.
Replogle W, Beebe D. Halitosis. Am Fam Physician 1996: 53: 1215-1218.
Rizzo A. The possible role of hydrogen sulfide in human periodontal disease. 1. Hydrogen sulfide production in periodontal pockets. Periodontics 1967: 5: 233-236.
Rosenberg M, Gerlenter I, Barki M, Bar-Ness R. Day-long reduction of oral malodor by a two-phase oil:water mouthrinse as compared to chlorhexidine and placebo rinses. J Periodontol 1992: 63: 39-43.
Rosenberg M, Kulkarni G V, Bosy A, McCulloch C a. Reproducibility and sensitivity of oral malodor measurements with a portable sulphide monitor. J Dent Res 1991: 70: 1436-1440.
Rosenberg M, Leib E. Experiences of an Israeli malodor clinic. In: Rosenberg M, editor. Bad breath: research perspectives. Tel Aviv: Ramot Publishing, 1995: 137-148.
Rosenberg M, Septon I, Eli I, Bar-ness R, Gelernter I, Brenner S, Gabbay J. Halitosis measurement by an Industrial Sulphide Monitor. J Periodontol 1991: 62: 487-489.
Rosenberg M. Bad breath and periodontal disease: how related are they? J Clin Periodontol 2006: 33: 29-30.
Rowley E, Schuchman L, Tishk M, Carlson H. Tongue brushing versus tongue scraping. Clin Prev Dent 1987: 9: 13-16.
Schmidt N, Tarbet W. The effect of oral rinses on organoleptic mouth odor ratings and levels of volatile sulfur compounds. Oral Surg Oral Med Oral Pathol 1978: 45: 876-883.
Schroeder H, Münzel-Pedrazzoli S, Page R. Correlated morphometric and biochemical analysis of gingival tissues in early chronic gingivitis in men. Arch Oral Biol 1973: 18: 899-923.
Sharma N, Galustians H, Qaquish J, Galustians A, Rustogi K, Petrone M, Chaknis P, Garcia L, Volpe A, Proskin H. The clinical effectiveness of a dentifrice containing triclosan and a copolymer for controlling breath odor measured organoleptically twelve hours after toothbrushing. J Clin Dent 1999: 10: 131-134.
Sharma N, Galustians H, Qaquish J, Galustians A, Rustogi K, Petrone M, Chaknis P, Garcia L, Volpe A, Proskin H. Clinical effectiveness of a dentifrice containing triclosan and a copolymer for controlling breath odor. Am J Dent 2007: 20: 79-82.
Shinada K, Ueno M, Konishi C, Takehara S, Yokoyama S, Kawaguchi Y. A randomized double blind crossover placebo-controlled clinical trial to assess the effects of a mouthwash containing chlorine dioxide on oral malodor. Trials 2008: 9: 71.
Söder B, Johansson B, Söder P. The relation between foeter ex ore, oral hygiene and periodontal disease. Swed Dent J 2000: 24: 73-82.
Stamou E, Kozlovsky A, Rosenberg M. Association between oral malodour and periodontal disease-related parameters in a population of 71 Israelis. Oral Dis 2005: 11(Suppl 1): 72-74.
Van Steenberghe D, Avontroodt P, Peeters W, Pauwels M, Coucke W, Lijnen A, Quirynen M. Effect of different mouthrinses on morning breath. J Periodontol 2001: 72: 1183-1191.
Suarez F, Furne J, Springfield J, Levitt M. Morning breath odor: influence of treatments on sulfur gases. J Dent Res 2000: 79: 1773-1777.
Takeuchi H, Machigashira M, Yamashita D, Kozono S, Nakajima Y, Miyamoto M, Takeuchi N, Setoguchi T, Noguchi K. The association of periodontal disease with oral malodour in a Japanese population. Oral Dis 2010: 16: 702-726.
Tangerman A, Winkel E. Extra-oral Halitosis: a review. J Breath Res 2010: 4: 017003.
Tonzetich J, Kestenbaum R. Odour production by human salivary fractions and plaque. Arch Oral Biol 1969: 14: 815-827.
Tonzetich J, Ng S. Reduction of malodor by oral cleansing procedures. Oral Surg Oral Med Oral Pathol 1976: 42: 172-181.
Tonzetich J. Production and origin of oral malodor: a review of mechanisms and methods of analysis. J Periodontol 1977: 48: 13-20.
Tonzetich J. Oral malodour: an indicator of health status and oral cleanliness. Int Dent J 1978: 28: 309-319.
Van Tornhout M, Dadamio J, Coucke W, Quirynen M. Tongue coating: related factors. J Clin Periodontol 2013: 40: 180-185.
Tsai C-C, Chou H-H, Wu T-L, Yang Y-H, Ho K-Y, Wu Y-M, Ho Y-P. The levels of volatile sulfur compounds in mouth air from patients with chronic periodontitis. J Periodontal Res 2008: 43: 186-193.
Tsunoda M, Yamada S, Yasuda H. Deodorizing mechanism of epigallocatechin and chewing gum containing tea extracts. In: van Steenberghe D, Rosenberg M, editors. Bad breath: a multidisciplinary approach. Leuven: Leuven University Press, 1996: 275-284.
Waler S. The effect of zinc-containing chewing gum on volatile sulfur-containing compounds in the oral cavity. Acta Odontol Scand 1997: 55: 198-200.
Weitzman S, Weitberg A, Stossel T, Schwartz J, Shklar G. Effect of hydrogen peroxide on oral carcinogenesis in hamsters. J Periodontol 1986: 57: 685-688.
Wigger-Alberti W, Gysen K, Axmann E, Wilhelm K. Efficacy of a new mouthrinse formulation on the reduction of oral malodour in vivo. A randomized, double-blind, placebo-controlled, 3 week clinical study. J Breath Res 2010: 4: 017102.
Wilhelm D, Gysen K, Himmelmann A, Krause C, Wilhelm K. Short-term effect of a new mouthrinse formulation on oral malodour after single use in vivo: a comparative, randomized, single-blind, parallel-group clinical study. J Breath Res 2010: 4: 036002.
Winkler S, Garg A, Mekayarajjananonth T, Bakaeen L, Khan E. Depressed taste and smell in geriatric patients. J Am Dent Assoc 1999: 130: 1759-1765.
Yaegaki K, Sanada K. Volatile sulfur compounds in mouth air from clinically healthy subjects and patients with periodontal disease. J Periodontal Res 1992: 27: 233-238.
Yaegaki K, Sanada K. Biochemical and clinical factors influencing oral malodor in periodontal patients. J Periodontol 1992: 63: 783-789.
Young A, Jonski G, Rolla G, Waler S. Effects of metal salts on the oral production of volatile sulfur-containing compounds (VSC). J Clin Periodontol 2001: 28: 776-781.
Young A, Jonski G, Rolla G. A study of triclosan and its solubilizers as inhibitors of oral malodour. J Clin Periodontol 2002: 12: 1078-1081.
Young A, Jonski G, Rolla G. Inhibition of orally produced volatile sulfur compounds by zinc, chlorhexidine or cetylpyridinium chloride: effect of concentration. Eur J Oral Sci 2003: 111: 400-404.
