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.
Similar content being viewed by others
References
Memon MA et al (2023) Aetiology and associations of halitosis: a systematic review. Oral Dis 29(4):1432–1438
Bollen CM, Beikler T (2012) Halitosis: the multidisciplinary approach. Int J Oral Sci 4(2):55–63
Rosier BT et al (2022) The importance of nitrate reduction for oral health. J Dent Res 101(8):887–897
Graziani F, Tsakos G (2000) Patient-based outcomes and quality of life. Periodontol 83(1):277–294
Springfield J et al (2001) Spontaneous fluctuations in the concentrations of oral sulfur-containing gases. J Dent Res 80(5):1441–1444
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):036005
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):202–211
Memon MA et al (2023) Aetiology and associations of halitosis: a systematic review. Oral Dis 29(4):1432–1438
Wu J et al (2020) Halitosis: prevalence, risk factors, sources, measurement and treatment—a review of the literature. Aust Dent J 65(1):4–11
Randall DA, Wilson Westmark NL, Neville BW (2022) Common oral lesions. Am Fam Physician 105(4):369–376
Renvert S et al (2020) The underestimated problem of intra-oral halitosis in dental practice: an expert consensus review. Clin Cosmet Investig Dent 12:251–262
Tay JRH et al (2022) The efficacy of probiotics in the management of intra-oral halitosis: a systematic review. Clin Oral Investig 26(7):4687–4700
Harvey-Woodworth CN (2013) Dimethylsulphidemia: the significance of dimethyl sulphide in extra-oral, blood borne halitosis. Br Dent J 214(7):E20
Tsuruta M et al (2017) Relationships between pathologic subjective halitosis, olfactory reference syndrome, and social anxiety in young Japanese women. BMC Psychol 5(1):7
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):017105
Lu HX et al (2017) Oral health impact of halitosis in Chinese adults. Int J Dent Hyg 15(4):e85–e92
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 90:27–32
Ren W et al (2016) Supragingival plaque microbial community analysis of children with halitosis. J Microbiol Biotechnol 26(12):2141–2147
Riggio MP et al (2008) Molecular identification of bacteria on the tongue dorsum of subjects with and without halitosis. Oral Dis 14(3):251–258
Zhang Y et al (2021) Dynamic alterations of oral microbiota related to halitosis in preschool children. Front Cell Infect Microbiol 11:599467
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):397–401
Bicak DA (2018) A current approach to halitosis and oral malodor—a mini review. Open Dent J 12:322–330
Lee CH et al (2003) The relationship between volatile sulfur compounds and major halitosis-inducing factors. J Periodontol 74(1):32–37
Milella L (2015) The negative effects of volatile sulphur compounds. J Vet Dent 32(2):99–102
Hampelska K et al (2020) The role of oral microbiota in intra-oral halitosis. J Clin Med 9(8)
Mogilnicka I, Bogucki P, Ufnal M (2020) Microbiota and malodor—etiology and management. Int J Mol Sci 21(8)
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):213–227
Drmosh QA et al (2021) Zinc oxide-based acetone gas sensors for breath analysis: a review. Chem Asian J 16(12):1519–1538
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):1174–1184
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 14:153–170
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):359–375
Mokeem SA (2014) Halitosis: a review of the etiologic factors and association with systemic conditions and its management. J Contemp Dent Pract 15(6):806–811
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):748–755
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):2487
Suzuki N et al (2019) Induction and inhibition of oral malodor. Mol Oral Microbiol 34(3):85–96
Yu WW et al (2022) Prevalence of halitosis among young adults in Dunedin. New Zealand. Int J Dent Hyg 20(4):700–707
Jo JK et al (2021) Identification of salivary microorganisms and metabolites associated with halitosis. Metabolites 11(6)
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):90–94
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):1996755
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):e32507
Izidoro C et al (2023) Non-surgical periodontal treatment impact on subgingival microbiome and intra-oral halitosis. Int J Mol Sci 24(3)
Amou T et al (2014) Relationship between halitosis and periodontal disease—associated oral bacteria in tongue coatings. Int J Dent Hyg 12(2):145–151
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):36–47
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
Kumar R et al (2022) Exploring the potential of natural product-based nanomedicine for maintaining oral health. Molecules 27(5)
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):483–490
Moshkowitz M et al (2007) Halitosis and gastroesophageal reflux disease: a possible association. Oral Dis 13(6):581–585
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):34–40
Nakhleh MK, Quatredeniers M, Haick H (2018) Detection of halitosis in breath: between the past, present, and future. Oral Dis 24(5):685–695
Poniewierka E et al (2022) Halitosis as a symptom of gastroenterological diseases. Prz Gastroenterol 17(1):17–20
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 2:777442
Prabhu RV et al (2014) Areca nut and its role in oral submucous fibrosis. J Clin Exp Dent 6(5):e569–e575
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):592–594
Scully C (2014) Halitosis. BMJ Clin Evid 2014:1305
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)
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):316–320
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):775–783
Han HS et al (2023) Improvement of halitosis by probiotic bacterium Weissella cibaria CMU: a randomized controlled trial. Front Microbiol 14:1108762
Funding
The work was supported by the National Natural Science Foundation of China (81771127), the Natural Science Foundation of Xinjiang Uygur Autonomous Region (2022D01C15), the Medical Engineering Cross Foundation of Shanghai Jiao Tong University (YG2015MS06), and the Seed Foundation of the Ninth People’s Hospital, Shanghai Jiao Tong University School of Medicine (JYZZ196). Stomatology Clinical Research Project of Nation Clinical Center for Oral Diseases (NCRCO202330).
Ethics declarations
Ethics approval and consent to participate
Not applicable.
Conflict of interest
The authors declare no competing interests.
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Li, Z., Li, J., Fu, R. et al. Halitosis: etiology, prevention, and the role of microbiota. Clin Oral Invest 27, 6383–6393 (2023). https://doi.org/10.1007/s00784-023-05292-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00784-023-05292-9