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Published in: Clinical Oral Investigations 11/2023

16-10-2023 | Halitosis | Review

Halitosis: etiology, prevention, and the role of microbiota

Authors: Zhengrui Li, Jing Li, Rao Fu, Ji’an Liu, Xutao Wen, Ling Zhang

Published in: Clinical Oral Investigations | Issue 11/2023

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Abstract

Objectives

This study aims to review halitosis research, discuss its various causes, and propose effective interventions based on the underlying etiologies and mechanisms. The main research question is to identify the primary factors contributing to halitosis and appropriate strategies to address them.

Materials and methods

A comprehensive literature review was conducted on halitosis and its associated causes, including oral pathological factors, oral microbial influences, microbial metabolic pathways, gastrointestinal diseases, and gut microbiota dysbiosis.

Results

Unhealthy eating habits and an imbalance of microorganisms in the oral cavity and gastrointestinal tract were identified as primary causes of halitosis. Dental caries, periodontal disease, xerostomia, and digestive disorders like gastritis and irritable bowel syndrome were also found to be related to the development of halitosis. Due to poor oral hygiene or antibiotic use, disruption of microbial communities can result in dysbiosis, inflammation, and halitosis.

Conclusions

Halitosis is a multifactorial condition with various underlying causes, including oral and systemic diseases. Effective interventions should be tailored based on the specific etiologies and mechanisms involved.

Clinical relevance

Understanding the factors contributing to halitosis is crucial for developing appropriate treatment strategies. Enhancing oral hygiene habits, using antimicrobial drugs, or administering probiotics may help regulate oral or intestinal flora, thereby improving halitosis and overall oral health.
Literature
1.
go back to reference Memon MA et al (2023) Aetiology and associations of halitosis: a systematic review. Oral Dis 29(4):1432–1438 Memon MA et al (2023) Aetiology and associations of halitosis: a systematic review. Oral Dis 29(4):1432–1438
3.
go back to reference Rosier BT et al (2022) The importance of nitrate reduction for oral health. J Dent Res 101(8):887–897PubMed Rosier BT et al (2022) The importance of nitrate reduction for oral health. J Dent Res 101(8):887–897PubMed
4.
go back to reference Graziani F, Tsakos G (2000) Patient-based outcomes and quality of life. Periodontol 83(1):277–294 Graziani F, Tsakos G (2000) Patient-based outcomes and quality of life. Periodontol 83(1):277–294
5.
go back to reference Springfield J et al (2001) Spontaneous fluctuations in the concentrations of oral sulfur-containing gases. J Dent Res 80(5):1441–1444PubMed Springfield J et al (2001) Spontaneous fluctuations in the concentrations of oral sulfur-containing gases. J Dent Res 80(5):1441–1444PubMed
6.
go back to reference De Lima PO et al (2020) Effects of academic stress on the levels of oral volatile sulfur compounds, halitosis-related bacteria and stress biomarkers of healthy female undergraduate students. J Breath Res 14(3):036005PubMed De Lima PO et al (2020) Effects of academic stress on the levels of oral volatile sulfur compounds, halitosis-related bacteria and stress biomarkers of healthy female undergraduate students. J Breath Res 14(3):036005PubMed
7.
go back to reference Kolokotronis A, Doumas S (2006) Herpes simplex virus infection, with particular reference to the progression and complications of primary herpetic gingivostomatitis. Clin Microbiol Infect 12(3):202–211PubMed Kolokotronis A, Doumas S (2006) Herpes simplex virus infection, with particular reference to the progression and complications of primary herpetic gingivostomatitis. Clin Microbiol Infect 12(3):202–211PubMed
8.
go back to reference Memon MA et al (2023) Aetiology and associations of halitosis: a systematic review. Oral Dis 29(4):1432–1438PubMed Memon MA et al (2023) Aetiology and associations of halitosis: a systematic review. Oral Dis 29(4):1432–1438PubMed
9.
go back to reference Wu J et al (2020) Halitosis: prevalence, risk factors, sources, measurement and treatment—a review of the literature. Aust Dent J 65(1):4–11PubMed Wu J et al (2020) Halitosis: prevalence, risk factors, sources, measurement and treatment—a review of the literature. Aust Dent J 65(1):4–11PubMed
10.
go back to reference Randall DA, Wilson Westmark NL, Neville BW (2022) Common oral lesions. Am Fam Physician 105(4):369–376PubMed Randall DA, Wilson Westmark NL, Neville BW (2022) Common oral lesions. Am Fam Physician 105(4):369–376PubMed
11.
go back to reference Renvert S et al (2020) The underestimated problem of intra-oral halitosis in dental practice: an expert consensus review. Clin Cosmet Investig Dent 12:251–262PubMedPubMedCentral Renvert S et al (2020) The underestimated problem of intra-oral halitosis in dental practice: an expert consensus review. Clin Cosmet Investig Dent 12:251–262PubMedPubMedCentral
12.
go back to reference Tay JRH et al (2022) The efficacy of probiotics in the management of intra-oral halitosis: a systematic review. Clin Oral Investig 26(7):4687–4700PubMed Tay JRH et al (2022) The efficacy of probiotics in the management of intra-oral halitosis: a systematic review. Clin Oral Investig 26(7):4687–4700PubMed
13.
go back to reference Harvey-Woodworth CN (2013) Dimethylsulphidemia: the significance of dimethyl sulphide in extra-oral, blood borne halitosis. Br Dent J 214(7):E20PubMed Harvey-Woodworth CN (2013) Dimethylsulphidemia: the significance of dimethyl sulphide in extra-oral, blood borne halitosis. Br Dent J 214(7):E20PubMed
14.
go back to reference Tsuruta M et al (2017) Relationships between pathologic subjective halitosis, olfactory reference syndrome, and social anxiety in young Japanese women. BMC Psychol 5(1):7PubMedPubMedCentral Tsuruta M et al (2017) Relationships between pathologic subjective halitosis, olfactory reference syndrome, and social anxiety in young Japanese women. BMC Psychol 5(1):7PubMedPubMedCentral
15.
go back to reference Falcao DP, Vieira CN, de Amorim RFB (2012) Breaking paradigms: a new definition for halitosis in the context of pseudo-halitosis and halitophobia. J Breath Res 6(1):017105PubMed Falcao DP, Vieira CN, de Amorim RFB (2012) Breaking paradigms: a new definition for halitosis in the context of pseudo-halitosis and halitophobia. J Breath Res 6(1):017105PubMed
16.
go back to reference Lu HX et al (2017) Oral health impact of halitosis in Chinese adults. Int J Dent Hyg 15(4):e85–e92PubMed Lu HX et al (2017) Oral health impact of halitosis in Chinese adults. Int J Dent Hyg 15(4):e85–e92PubMed
17.
go back to reference Kandalam U et al (2018) Inhibition of methionine gamma lyase deaminase and the growth of Porphyromonas gingivalis: a therapeutic target for halitosis/periodontitis. Arch Oral Biol 90:27–32PubMed Kandalam U et al (2018) Inhibition of methionine gamma lyase deaminase and the growth of Porphyromonas gingivalis: a therapeutic target for halitosis/periodontitis. Arch Oral Biol 90:27–32PubMed
18.
go back to reference Ren W et al (2016) Supragingival plaque microbial community analysis of children with halitosis. J Microbiol Biotechnol 26(12):2141–2147PubMed Ren W et al (2016) Supragingival plaque microbial community analysis of children with halitosis. J Microbiol Biotechnol 26(12):2141–2147PubMed
19.
go back to reference Riggio MP et al (2008) Molecular identification of bacteria on the tongue dorsum of subjects with and without halitosis. Oral Dis 14(3):251–258PubMed Riggio MP et al (2008) Molecular identification of bacteria on the tongue dorsum of subjects with and without halitosis. Oral Dis 14(3):251–258PubMed
20.
go back to reference Zhang Y et al (2021) Dynamic alterations of oral microbiota related to halitosis in preschool children. Front Cell Infect Microbiol 11:599467PubMedPubMedCentral Zhang Y et al (2021) Dynamic alterations of oral microbiota related to halitosis in preschool children. Front Cell Infect Microbiol 11:599467PubMedPubMedCentral
21.
go back to reference Seemann R et al (2004) Reduction of oral levels of volatile sulfur compounds (VSC) by professional toothcleaning and oral hygiene instruction in non-halitosis patients. Oral Health Prev Dent 2(4):397–401PubMed Seemann R et al (2004) Reduction of oral levels of volatile sulfur compounds (VSC) by professional toothcleaning and oral hygiene instruction in non-halitosis patients. Oral Health Prev Dent 2(4):397–401PubMed
23.
go back to reference Lee CH et al (2003) The relationship between volatile sulfur compounds and major halitosis-inducing factors. J Periodontol 74(1):32–37PubMed Lee CH et al (2003) The relationship between volatile sulfur compounds and major halitosis-inducing factors. J Periodontol 74(1):32–37PubMed
24.
go back to reference Milella L (2015) The negative effects of volatile sulphur compounds. J Vet Dent 32(2):99–102PubMed Milella L (2015) The negative effects of volatile sulphur compounds. J Vet Dent 32(2):99–102PubMed
25.
go back to reference Hampelska K et al (2020) The role of oral microbiota in intra-oral halitosis. J Clin Med 9(8) Hampelska K et al (2020) The role of oral microbiota in intra-oral halitosis. J Clin Med 9(8)
26.
go back to reference Mogilnicka I, Bogucki P, Ufnal M (2020) Microbiota and malodor—etiology and management. Int J Mol Sci 21(8) Mogilnicka I, Bogucki P, Ufnal M (2020) Microbiota and malodor—etiology and management. Int J Mol Sci 21(8)
27.
go back to reference De Geest S et al (2016) Periodontal diseases as a source of halitosis: a review of the evidence and treatment approaches for dentists and dental hygienists. Periodontol 2000 71(1):213–227PubMed De Geest S et al (2016) Periodontal diseases as a source of halitosis: a review of the evidence and treatment approaches for dentists and dental hygienists. Periodontol 2000 71(1):213–227PubMed
28.
go back to reference Drmosh QA et al (2021) Zinc oxide-based acetone gas sensors for breath analysis: a review. Chem Asian J 16(12):1519–1538PubMed Drmosh QA et al (2021) Zinc oxide-based acetone gas sensors for breath analysis: a review. Chem Asian J 16(12):1519–1538PubMed
29.
go back to reference Stephen AS et al (2021) Interdental and subgingival microbiota may affect the tongue microbial ecology and oral malodour in health, gingivitis and periodontitis. J Periodontal Res 56(6):1174–1184PubMed Stephen AS et al (2021) Interdental and subgingival microbiota may affect the tongue microbial ecology and oral malodour in health, gingivitis and periodontitis. J Periodontal Res 56(6):1174–1184PubMed
30.
go back to reference Belay AS, Achimano AA (2022) Prevalence and risk factors for periodontal disease among women attending antenatal care in public hospitals, Southwest Ethiopia, 2022: a multicenter cross-sectional study. Clin Cosmet Investig Dent 14:153–170PubMedPubMedCentral Belay AS, Achimano AA (2022) Prevalence and risk factors for periodontal disease among women attending antenatal care in public hospitals, Southwest Ethiopia, 2022: a multicenter cross-sectional study. Clin Cosmet Investig Dent 14:153–170PubMedPubMedCentral
31.
go back to reference Foo LH et al (2021) Role of the oral microbiome, metabolic pathways, and novel diagnostic tools in intra-oral halitosis: a comprehensive update. Crit Rev Microbiol 47(3):359–375PubMed Foo LH et al (2021) Role of the oral microbiome, metabolic pathways, and novel diagnostic tools in intra-oral halitosis: a comprehensive update. Crit Rev Microbiol 47(3):359–375PubMed
32.
go back to reference Mokeem SA (2014) Halitosis: a review of the etiologic factors and association with systemic conditions and its management. J Contemp Dent Pract 15(6):806–811PubMed Mokeem SA (2014) Halitosis: a review of the etiologic factors and association with systemic conditions and its management. J Contemp Dent Pract 15(6):806–811PubMed
33.
go back to reference Tangerman A, Winkel EG (2007) Intra- and extra-oral halitosis: finding of a new form of extra-oral blood-borne halitosis caused by dimethyl sulphide. J Clin Periodontol 34(9):748–755PubMed Tangerman A, Winkel EG (2007) Intra- and extra-oral halitosis: finding of a new form of extra-oral blood-borne halitosis caused by dimethyl sulphide. J Clin Periodontol 34(9):748–755PubMed
34.
go back to reference Lee YH et al (2023) Volatile sulfide compounds and oral microorganisms on the inner surface of masks in individuals with halitosis during COVID-19 pandemic. Sci Rep 13(1):2487PubMedPubMedCentral Lee YH et al (2023) Volatile sulfide compounds and oral microorganisms on the inner surface of masks in individuals with halitosis during COVID-19 pandemic. Sci Rep 13(1):2487PubMedPubMedCentral
35.
go back to reference Suzuki N et al (2019) Induction and inhibition of oral malodor. Mol Oral Microbiol 34(3):85–96PubMed Suzuki N et al (2019) Induction and inhibition of oral malodor. Mol Oral Microbiol 34(3):85–96PubMed
36.
go back to reference Yu WW et al (2022) Prevalence of halitosis among young adults in Dunedin. New Zealand. Int J Dent Hyg 20(4):700–707PubMed Yu WW et al (2022) Prevalence of halitosis among young adults in Dunedin. New Zealand. Int J Dent Hyg 20(4):700–707PubMed
37.
go back to reference Jo JK et al (2021) Identification of salivary microorganisms and metabolites associated with halitosis. Metabolites 11(6) Jo JK et al (2021) Identification of salivary microorganisms and metabolites associated with halitosis. Metabolites 11(6)
38.
go back to reference Tolentino Ede S, Chinellato LE, Tarzia O (2011) Saliva and tongue coating pH before and after use of mouthwashes and relationship with parameters of halitosis. J Appl Oral Sci 19(2):90–94PubMed Tolentino Ede S, Chinellato LE, Tarzia O (2011) Saliva and tongue coating pH before and after use of mouthwashes and relationship with parameters of halitosis. J Appl Oral Sci 19(2):90–94PubMed
39.
go back to reference Botelho Dinis M et al (2021) Pilot study on selective antimicrobial effect of a halitosis mouthrinse: monospecies and saliva-derived microbiome in an in vitro model system. J Oral Microbiol 13(1):1996755PubMedPubMedCentral Botelho Dinis M et al (2021) Pilot study on selective antimicrobial effect of a halitosis mouthrinse: monospecies and saliva-derived microbiome in an in vitro model system. J Oral Microbiol 13(1):1996755PubMedPubMedCentral
40.
go back to reference Bhatia S et al (2022) Self-perceived halitosis and related factors among the mask-wearing population during the COVID-19 pandemic in Delhi, India: a cross-sectional study. Cureus 14(12):e32507PubMedPubMedCentral Bhatia S et al (2022) Self-perceived halitosis and related factors among the mask-wearing population during the COVID-19 pandemic in Delhi, India: a cross-sectional study. Cureus 14(12):e32507PubMedPubMedCentral
41.
go back to reference Izidoro C et al (2023) Non-surgical periodontal treatment impact on subgingival microbiome and intra-oral halitosis. Int J Mol Sci 24(3) Izidoro C et al (2023) Non-surgical periodontal treatment impact on subgingival microbiome and intra-oral halitosis. Int J Mol Sci 24(3)
42.
go back to reference Amou T et al (2014) Relationship between halitosis and periodontal disease—associated oral bacteria in tongue coatings. Int J Dent Hyg 12(2):145–151PubMed Amou T et al (2014) Relationship between halitosis and periodontal disease—associated oral bacteria in tongue coatings. Int J Dent Hyg 12(2):145–151PubMed
43.
go back to reference Deutscher H et al (2018) The effect of professional tooth cleaning or non-surgical periodontal therapy on oral halitosis in patients with periodontal diseases. A systematic review. Int J Dent Hyg 16(1):36–47PubMed Deutscher H et al (2018) The effect of professional tooth cleaning or non-surgical periodontal therapy on oral halitosis in patients with periodontal diseases. A systematic review. Int J Dent Hyg 16(1):36–47PubMed
44.
go back to reference Tambe A et al (2014) Andrew’s bridge system: an aesthetic and functional option for rehabilitation of compromised maxillary anterior dentition. BMJ Case Rep 2014:bcr2014203988 Tambe A et al (2014) Andrew’s bridge system: an aesthetic and functional option for rehabilitation of compromised maxillary anterior dentition. BMJ Case Rep 2014:bcr2014203988
45.
go back to reference Kumar R et al (2022) Exploring the potential of natural product-based nanomedicine for maintaining oral health. Molecules 27(5) Kumar R et al (2022) Exploring the potential of natural product-based nanomedicine for maintaining oral health. Molecules 27(5)
46.
go back to reference Lee HJ et al (2014) Association between halitosis diagnosed by a questionnaire and halimeter and symptoms of gastroesophageal reflux disease. J Neurogastroenterol Motil 20(4):483–490PubMedPubMedCentral Lee HJ et al (2014) Association between halitosis diagnosed by a questionnaire and halimeter and symptoms of gastroesophageal reflux disease. J Neurogastroenterol Motil 20(4):483–490PubMedPubMedCentral
47.
go back to reference Moshkowitz M et al (2007) Halitosis and gastroesophageal reflux disease: a possible association. Oral Dis 13(6):581–585PubMed Moshkowitz M et al (2007) Halitosis and gastroesophageal reflux disease: a possible association. Oral Dis 13(6):581–585PubMed
48.
go back to reference Katz J et al (2003) Oral signs and symptoms in relation to disease activity and site of involvement in patients with inflammatory bowel disease. Oral Dis 9(1):34–40PubMed Katz J et al (2003) Oral signs and symptoms in relation to disease activity and site of involvement in patients with inflammatory bowel disease. Oral Dis 9(1):34–40PubMed
49.
go back to reference Nakhleh MK, Quatredeniers M, Haick H (2018) Detection of halitosis in breath: between the past, present, and future. Oral Dis 24(5):685–695PubMed Nakhleh MK, Quatredeniers M, Haick H (2018) Detection of halitosis in breath: between the past, present, and future. Oral Dis 24(5):685–695PubMed
50.
51.
go back to reference Zanetti F et al (2021) A literature review and framework proposal for halitosis assessment in cigarette smokers and alternative nicotine-delivery products users. Front Oral Health 2:777442PubMedPubMedCentral Zanetti F et al (2021) A literature review and framework proposal for halitosis assessment in cigarette smokers and alternative nicotine-delivery products users. Front Oral Health 2:777442PubMedPubMedCentral
53.
go back to reference Henker J, Schuster F, Nissler K (2001) Successful treatment of gut-caused halitosis with a suspension of living non-pathogenic Escherichia coli bacteria—a case report. Eur J Pediatr 160(10):592–594PubMed Henker J, Schuster F, Nissler K (2001) Successful treatment of gut-caused halitosis with a suspension of living non-pathogenic Escherichia coli bacteria—a case report. Eur J Pediatr 160(10):592–594PubMed
54.
go back to reference Scully C (2014) Halitosis. BMJ Clin Evid 2014:1305 Scully C (2014) Halitosis. BMJ Clin Evid 2014:1305
55.
go back to reference Wyszynska M et al (2021) The problem of halitosis in prosthetic dentistry, and new approaches to its treatment: a literature review. J Clin Med 10(23) Wyszynska M et al (2021) The problem of halitosis in prosthetic dentistry, and new approaches to its treatment: a literature review. J Clin Med 10(23)
56.
go back to reference Lau P et al (2021) Say ahhh: experience and views on halitosis management in the general public in Victoria, Australia. Int Dent J 71(4):316–320PubMedPubMedCentral Lau P et al (2021) Say ahhh: experience and views on halitosis management in the general public in Victoria, Australia. Int Dent J 71(4):316–320PubMedPubMedCentral
57.
go back to reference Mousquer CR et al (2020) Are Lactobacillus salivarius G60 and inulin more efficacious to treat patients with oral halitosis and tongue coating than the probiotic alone and placebo? A randomized clinical trial. J Periodontol 91(6):775–783PubMed Mousquer CR et al (2020) Are Lactobacillus salivarius G60 and inulin more efficacious to treat patients with oral halitosis and tongue coating than the probiotic alone and placebo? A randomized clinical trial. J Periodontol 91(6):775–783PubMed
58.
go back to reference Han HS et al (2023) Improvement of halitosis by probiotic bacterium Weissella cibaria CMU: a randomized controlled trial. Front Microbiol 14:1108762PubMedPubMedCentral Han HS et al (2023) Improvement of halitosis by probiotic bacterium Weissella cibaria CMU: a randomized controlled trial. Front Microbiol 14:1108762PubMedPubMedCentral
Metadata
Title
Halitosis: etiology, prevention, and the role of microbiota
Authors
Zhengrui Li
Jing Li
Rao Fu
Ji’an Liu
Xutao Wen
Ling Zhang
Publication date
16-10-2023
Publisher
Springer Berlin Heidelberg
Published in
Clinical Oral Investigations / Issue 11/2023
Print ISSN: 1432-6981
Electronic ISSN: 1436-3771
DOI
https://doi.org/10.1007/s00784-023-05292-9

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