Breathing out a virus

Intra-Oral Causes
Extra-Oral Causes
Psychological Causes
Psycho-Social Effects


Halitosis (oral malodour, bad breath, fetor oris) is defined as offensive breath odour, with the potential to cause personal discomfort and social embarrassment. 1 The condition has been reported since ancient times, with references dating back to 1550 BC. Hippocrates advised that ‘any girl should have pleasant breath, making sure to always wash her mouth with wine, anise and dill seeds’.2 The condition is common to all age groups, with an estimated global prevalence of between 15% and 50% in adult populations.3-6

Halitosis has a range of local oral and systemic causes and can indicate an underlying disease. However, most sources of malodour are intra-oral (~85%), including poor dental hygiene. An abnormal tongue coating accounts for 50%,7 periodontal conditions 15%, or a combination of the two comprise 25% of cases.8 The irregular dorsum of the tongue, with a surface area of 25cm2, provides an ideal habitat for bacteria9 thriving on the putrefaction occurring among desquamating epithelial cells and food debris.10-11 Strong evidence has demonstrated the positive correlation between the majority of cultured microorganisms responsible for halitosis and those found among tongue coating material and in periodontitis; with deeper periodontal pockets harbouring higher bacterial concentrations. 12-17

In around 5% of cases, causality is due to an extra-oral source, typically related to otolaryngeal, gastrointestinal or respiratory pathology.18 Systemic disease can also be attributable, such as diabetes, metabolic or hormonal changes, and renal or hepatic insufficiency.19 Transient halitosis can be due to dietary sources, or smoking. Pseudo-halitosis is defined as patient-perceived halitosis that is not apparent to either a healthcare professional, or any of the patient’s family, friends or close associates. The condition is common, affecting around 28% of patients presenting with halitosis. Patients are offered counselling, and those with persistent beliefs are categorised as having ‘halitophobia’.20-21

Identifying the cause of halitosis is important since this should direct appropriate medical management, with referral indicated in complicated or resistant cases.

Intra-oral causes


The  micro-organisms  implicated  in  oral  malodour  are  predominantly  Gram-negative  anaerobes,  which  include: Porphyromonasgingivalis; Prevotella intermedia; Fusobacterium nucleatum; Solobacterium moorei; Tannerella forsythia (Bacteroides forsythus) and Treponema denticola.22-24 Gram-positive bacteria are also involved and can denude available glycoproteins of their sugar chains, enabling the anaerobic Gram-negative proteolytic bacteria to break down the denuded proteins. Gram-negative bacteria produce chemicals that create malodour, including volatile sulphur compounds (VSCs) - mainly methyl mercaptan, hydrogen sulphide, and dimethyl sulphide, diamines (putrescine and cadaverine) - and short chain fatty acids (butyric, valeric and propionic).25-26 It is estimated that between 80% to 90% of halitosis odours of intra-oral origin are due to VSCs.1, 22, 27-28 In patients with chronic periodontitis higher levels of VSCs have been demonstrated.13, 29

The causative bacteria may be present in areas of periodontal disease, particularly in association with ulceration or necrosis, where they reside deep within pathological tissue recesses around teeth. Conversely, in the presence of healthy periodontal (gingival) tissues, such bacteria may proliferate on the dorsum of the tongue, the posterior area commonly the location of microbial activity associated with bad breath.30


Patients with xerostomia (dry mouth due to reduced salivary flow) lack saliva’s plethora of protective actions on the oral cavity, and will often show an increased volume of plaque on teeth and tongue.31 The lack of salivary flow and its associated antimicrobial activity leads to a transition from mainly Gram-positive bacteria to Gram-negative species,32 and an overall increase in the bacterial load.

Xerostomia can be due to salivary stagnation, salivary gland disease, post-radiotherapy to the head and neck, autoimmune diseases, such as Sjögren syndrome, or the use of salivation inhibiting anticholinergic, antihistamine or diuretic drugs. Further causes include chronic mouth breathing, dehydration and systemic illness such as diabetes mellitus, renal disease and thyroid dysfunction although more common in hyperthyroidism, dry mouth is also recognised in patients with hypothyroidism and is expected to improve with treatment of the underlying thyroid irregularity.

Almost 25% of older persons (over 65 years) suffer from dry mouth33, and there is a positive correlation between dry mouth (which can also cause dysgeusia (an altered sense of taste), glossodynia (a sore or ‘burning’ mouth), sialadenitis (an infection of the salivary gland(s) - usually viral or bacterial, with associated pain, tenderness, redness, and localised swelling), cracking and fissuring of the oral mucosa) and halitosis.34-36

Odontogenic halitosis (poor oral hygiene)

Poor oral hygiene can allow accumulation of food debris, plaque and calculus around teeth, or under a neglected or poorly designed fixed prosthesis (a dental bridge, crown or implant, for example with gaps or spaces that inhibits adequate oral hygiene and permits collection of food debris), which can contribute to halitosis. Poorly maintained and ill-fitting dentures can also be a source of malodour, as can keeping dentures in place overnight, rather than removing and cleaning.

Periodontal disease (gingivitis and/or periodontitis), especially necrotizing gingivitis, can also cause bad breath and are indicated by sore, swollen gums and bleeding. Stomatitis, intra-oral neoplasia, exposed tooth pulps (with necrotic content), extraction wounds (with a blood clot or purulent discharge), or crowding of teeth (favouring food entrapment) are further sources of halitosis. Peri-implantitis (inflammation of the soft tissues surrounding the crown of a partially erupted tooth), recurrent oral ulcerations and herpetic gingivitis can also be involved. 21, 37-38

Oral intake

Following ingestion a number of foods and spices can release their odour to the lungs, which is then exhaled (transient blood-borne or haematogenic halitosis), for example, garlic is classically detectable on the breath for several hours after eating. Smoking can contribute to poor breath, as well as staining teeth, contribute to periodontal disease and reduce the senses of taste and smell. Alcohol can remain on the breath for several hours. Dieting schemes that focus on particular foods can cause malodour, as can crash dieting where the body will metabolise fats in the absence of ingested carbohydrates - producing ketones that are detectable on the breath.

Morning breath

Following overnight mouth breathing, lack of oral cleansing during sleep and physiologically low overnight salivary flow rates a degree of oral malodour is common on awakening (‘morning breath’)  and is generally of no significance. Subsequent to breakfast food/drink, attention to regular morning basic oral hygiene measures and resumption of normal daytime salivary flow, such malodour will dissipate.39

Extra-oral causes

Ear, nose and throat

Up to 10% of halitosis cases can originate from the ear, nose and throat (ENT) region – with 3% due to pathology at the tonsils.40 Tonsilloliths/ tonsil stones (small collections of microbial and cellular debris that form in the crevices/crypts of the tonsils) are associated with a 10-fold increased risk of abnormal VSC levels. 41 Mouth breathing can be a cause of halitosis and typically takes place when nasal obstruction impedes normal nasal breathing at rest.42 Postnasal drip (mucus of the paranasal sinuses) onto the dorsum of the tongue can cause halitosis.42-43

Bacterial sinusitis, often secondary to acute viral sinusitis, typically involving Streptococcus pneumonia and Haemophilus influenza, can produce malodour if purulent mucous is produced. Similarly, atrophic rhinitis with bacterial super-infection can lead to halitosis. In the case of chronic sinusitis, 50%–70% of patients complain about oral malodour.44 Foreign bodies in the nasal cavity can produce a foul odour and not uncommonly provide an infective nidus – this is particularly important to explore in children and susceptible psychiatric patients.


The gastrointestinal tract can only indirectly influence bad breath, with 0.5% of halitosis cases attributable.45 These limited cases include the chronic unpleasant odour of rare Zenker's diverticulum typically in patients over 65 years of age. Bleeding of the oesophagus can cause a musty odour, while regurgitation of gastric contents or reflux of gastric acid can cause halitosis – alongside the more frequent burning throat/mouth sensation and sour taste.47 In some cases of intestinal obstruction, a faecal oral odour may be detectable.48

Metabolic/organ failure

Chronic renal failure is associated with raised blood urea nitrogen levels, generating typically uraemic halitosis, together with low salivary flow rates leading to dry mouth with associated oral malodour.49 Liver impairment produces a musky or sometimes faintly sulfurous odour. Liver failure results in waste product elimination by diversion via the pulmonary circulation, producing ‘fetor hepticus’ - a sweet, excremental odour.50 Liver failure also inhibits detoxification systemically, causing unpleasant odours.51

Diabetics ketoacidosis can result in unusual smelling ketotic breath, sometimes compared to the sweet or fruity smell of acetone. In difficult to diagnose cases, it is worth considering that several metabolic disorders affect the bowels, such as trimethylaminuria - producing a specific fishy odour and is the largest cause of undiagnosed body odour.52 This rare disorder causes a defect in the normal production of flavin-containing monooxygenase 3 (FMO3). There is a corresponding loss in proper conversion of trimethylamine (TMA) from precursor compounds in food allowing an accumulation of TMA which is released in sweat, urine, and breath, giving off the strong odours.


Enquiring into changes of medications or new drugs is important since some can cause bad breath (including amlodipine, phenothiazines and oral nitrates - isosorbide mononitrate), as can over the counter preparations – such as the starch-based multi-vitamin preparations.53

Psychological causes


A number of patients complain of halitosis, but objectively have no evidence of the condition and instead, are subjectively imagining such symptoms psychogenically. This can present a clinical challenge since no evidence of oral malodour can be detected even with objective testing and yet the patient belief remains steadfast. The oral malodour can be attributed to a form of delusion or monosymptomatic hypochondriasis (self-oral malodour; halitophobia). Such patients can often misinterpret other people’s behaviour as reactive to their perceived offensive breath, for example apparently covering the nose or averting the face.  Understanding, empathic communication and referral to specialist secondary care services is indicated in such situations. 19, 54-55


This is the fear of offending others through ones perceived bad breath and affects 0.5%–1% of the adult population. Convinced they have halitosis, they are not persuaded by negative test results during diagnosis and therapy. Such non-real halitosis is a form of compulsive disorder and can frustrate the patient and irritate those around them. 19, 54-55

Psycho-social effects

The effect of both genuine halitosis and pseudo-halitosis on patients is the frequent adoption of behaviour to try and minimise their problem/perceived problem - such as, covering the mouth when speaking, avoiding or keeping a distance from other people and avoiding social situations – all of which can create internal frustration and social tensions.

Further actions can include excessively using chewing gum,  mints, mouthwashes or sprays designed to reduce malodour, and frequent toothbrushing and tongue cleaning. Paradoxically in such patients, the level of oral hygiene may be superb, indeed their overzealousness can be damaging the oral tissue, and extra-oral sources of halitosis should be sought, with psychological support where indicated. The challenge with pseudo-halitosis patients is that the majority have poor insight and will, unfortunately, fail to recognise their psychological condition, convinced they have halitosis, and often reluctant to receive psychological input. 19, 54-55


Halitosis is a common condition, largely due to intra-oral sources, with a limited number of cases secondary to extra-oral conditions. The commonest intra-oral cause is the presence of anaerobic microorganisms in the tongue coating, followed by poor oral hygiene – once addressed through oral hygiene measures, the halitosis often significantly improves. Malodour due to gingivitis or periodontitis should receive the input of dental professionals.

Conflict of interest: none declared


Dr Matthew West, Dr Iram Sofia Tawhid
GP, Herts Valley CCG 


Part two of this article will look at the management of halitosis



  1. Scully C & Greenman J. Halitology (breath odour: aetiopathogenesis and management). Oral Dis. 2012. 18:333–345
  2. Bosy A. Oral malodor: philosophical and practical aspects. J Can Dent Assoc. 1997.  63(3):196–201
  3. Nadanovsky P, Carvalho LB, Ponce de Leon A. Oral malodour and its association with age and sex in a general population in Brazil. Oral Dis. 2007. 13(1): 105–109
  4. Saito H, Kawaguchi Y. Halitosis prevention campaign: a report of oral health promotion activities in Japan. Int Dent J. 2002. 52( Suppl 3): 197–200
  5. Liu XN, Shinada K, Chen XC et al. Oral malodour-related parameters in the Chinese general population. J Clin Periodontol. 2006. 33(1): 27–31
  6. Al-Ansari JM, Boodai H, Al-Sumait N et al. Factors associated with the self-reported halitosis in Kuwaiti patients. J Dent. 2006. 34(7): 444–449
  7. Roldán S, Herrera D, Sanz M. Biofilms and the tongue: therapeutical approaches for the control of halitosis. Clin Oral Investig. 2003. 7(4): 189–197
  8. Quirynen M, Dadamio J, van den Velde S et al. Characteristics of 2000 patients who visited a halitosis clinic. J Clin Periodontol. 2009. 36(11): 970–975
  9. Collins LM, Dawes C. The surface area of the adult human mouth and thickness of the salivary film covering the teeth and oral mucosa. J Dent Res. 1987. 66(8): 1300–1302
  10. De Boever EH, Loesche WJ. Assessing the contribution of anaerobic microflora of the tongue to oral malodor. J Am Dent Assoc. 1995. 126(10):1384-93
  11. De Boever EH, Uzeda M, Loesche WJ. Role of tongue surface characteristics and tongue flora in halitosis. J Dent Res. 1995. 74:127  
  12. Calil C, Liberato FL, Pereira AC et al. The relationship between volatile sulphur compounds, tongue coating and periodontal disease. Int J Dent Hyg. 2009. 7(4): 251–255
  13. Yaegaki K, Sanada K. Volatile sulphur-compounds in mouth air from clinically healthy subjects and patients with periodontal disease. J Periodont Res. 1992. 27(4 Pt 1): 233–238
  14. Tanaka M, Yamamoto Y, Kuboniwa M et al. Contribution of periodontal pathogens on tongue dorsa analysed with real-time PCR to oral malodour. Microbes Infect. 2004. 6(12): 1078–1083
  15. Rosenberg M. Bad breath and periodontal disease: how related are they? J Clin Periodontol. 2006. 33(1):29-30
  16. 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 Suppl 3:212-6 
  17. Mantilla Gómez S, Danser MM, Sipos PM, Rowshani B, van der Velden U, van der Weijden GA. Tongue coating and salivary bacterial counts in healthy/gingivitis subjects and periodontitis patients. J Clin Periodontol. 2001. 28:970-8
  18. Tangerman A & Winkel EG. Extra-oral halitosis: an overview. J Breath Res. 2010. 4(1):017003
  19. Yaegaki K, Coil JM. Examination, Classification, and Treatment of Halitosis; Clinical Perspectives. J Can Dent Assoc. 2000. 66:257-6.
  20. National Institute for Health and Clinical Excellence (NICE). Clinical Knowledge Summaries: Halitosis. Available at: (accessed August 2018)
  21. Rosenberg M. Clinical assessment of bad breath: current concepts. J Amer Dent Assoc. 1996. 127:475–482 
  22. Loesche WJ, Kazor C. Microbiology and treatment of halitosis. Periodontol. 2000. 2002;28:256-79
  23. Donaldson A, McKenzie D, Riggio M, Hodge P, Rolph H, Flanagan A et al. Microbiological culture analysis of the tongue anaerobic microflora in subjects with and without halitosis. Oral Dis. 2005. 11 Suppl 1:61-3
  24. Riggio MP, Lennon A, Rolph HJ, Hodge PJ, Donaldson A, Maxwell AJ et al. Molecular identification of bacteria on the tongue dorsum of subjects with and without halitosis. Oral Dis. 2008. 14(3):251-8
  25. Kaizu T, Tsunoda M, Aoki H, Kimura K. Analysis of volatile sulphur compounds in mouth air by gas chromatography. Bull Tokyo Dent Coll. 1978. 19:43-52
  26. Goldberg S, Kozlovsky A, Gordon D, Gelernter I, Sintov A, Rosenberg M. Cadaverine as a putative component of oral malodor. J Dent Res. 1994. 73(6):1168-72
  27. Tsai CC, Chou HH, Wu TL, Yang YH, Ho KY, Wu YM et al. The levels of volatile sulfur compounds in mouth air from patients with chronic periodontitis. J Periodontal Res. 2008. 43:186-93
  28. Krespi YP, Shrime MG, Kacker A. The relationship between oral malodor and volatile sulfur compound-producing bacteria. Otolaryngol Head Neck Surg. 2006. 135(5):671-6 
  29. Bosy A, Kulkarni GV, Rosenberg M, McCulloch CA. Relationship of oral malodor to periodontitis: evidence of independence in discrete subpopulations. J Periodontol. 1994. 65(1):37-46
  30. Yaegaki K, Sanada K. Biochemical and clinical factors influencing oral malodor in periodontal patients. J Periodontol. 1992. 63:783-9
  31. Albuquerque DF, de Souza Tolentino E, Amado FM et al.Evaluation of halitosis and sialometry in patients submitted to head and neck radiotherapy. Med Oral Pathol Oral Cir Bucal. 2010. 15(6): e850–e854   
  32. Almståhl A, Wikström M. Oral microflora in subjects with reduced salivary secretion. J Dent Res. 1999. 78(8): 1410–1416
  33. Pajukoski H, Meurman JH, Halonen P et al. Prevalence of subjective dry mouth and burning mouth in hospitalized elderly patients and outpatients in relation to saliva, medication, and systemic diseases. Oral Surg Oral Med Oral Pathol Oral Radiol Endod. 2001. 92(6): 641–649 
  34. Kleinberg I, Wolff MS, Codipilly DM. Role of saliva in oral dryness, oral feel and oral malodour. Int Dent J. 2002. 52(Suppl 3): 236–240
  35. Koshimune S, Awano S, Gohara K et al. Low salivary flow and volatile sulphur compounds in mouth air. Oral Surg Oral Med Oral Pathol Oral Radiol Endod. 2003. 9(1): 38–41
  36. Nalcaci R Baran I. Oral malodor and removable complete dentures in the elderly. Oral Surg Oral Med Oral Pathol Oral Radiol Endod. 2008. 105(6): e5–e9
  37. Prahabita PK Bhat KM Bhat GS. Oral malodor: a review of the literature. J Dent Hyg. 2006.  80(3): 8
  38. Delanghe G, Ghyselen J, van Steenberghe D et al. Multidisciplinary breath-odour clinic. Lancet. 1997. 350(9072): 187
  39. Faveri M, Hayacibara MF, Pupio GC, Cury JA, Tsuzuki CO, Hayacibara RM. A cross-over study on the effect of various therapeutic approaches to morning breath odour. J Clin Periodontol. 2006. 33(8):555-60
  40. van den Broek AM, Feenstra L, de Baat C. A review of the current literature on aetiology and measurement methods of halitosis. J Dent. 2007. 35(8): 627–635 
  41. Fletcher SM, Blair PA. Chronic halitosis from tonsilloliths: a common aetiology. J La State Med Soc. 1988. 140(6): 7–9
  42. Ng DK, Chow PY, Kwok KL. Halitosis and the nose. Hong Kong Med J. 2005. 11(1):71–72
  43. Amir E, Shimonov R, Rosenberg M. Halitosis in children. J Pediatr. 1999. 134(4): 338–343 
  44. Lanza DC. Diagnosis of chronic rhinosinusitis. Ann Otol Rhinol Laryngol. 2004. 193(Suppl 1): 10–14
  45. Bollen CML,  Beikler T. Halitosis: the multidisciplinary approach Int J Oral Sci. 2012. Jun; 4(2): 55–63
  46. Stoeckli SJ, Schmid S. Endoscopic stapler-assisted diverticuloesophagostomy for Zenker's diverticulum: patient satisfaction and subjective relief of symptoms. Surgery. 2002. 131(2): 158–162
  47. Struch F, Schwahn C, Wallaschofski H et al. Self-reported halitosis and gastro-oesophageal reflux disease in the general population. J Gen Intern Med. 2008. 23(3): 260–266 
  48. Stephenson BM, Rees BI. Extrinsic duodenal obstruction and halitosis. Postgrad Med J. 1990. 66(777): 568–570
  49. Keles M Tozoglu U Uyanik A et al. Does peritoneal dialysis affect halitosis in patients with end-stage renal disease? Perit Dial Int. 2011. 31(2): 168–172  
  50. Tangerman A, Meuwese-Arends MT, Jansen JB. Foetor hepaticus. Lancet. 1994. 343(8912): 1569
  51. van den Velde S, Nevens F, van Hee P et al. GC-MS analysis of breath odor compounds in liver patients. J Chromatogr B Analyt Technol Biomed Life Sci. 2008. 875(2): 344–348  
  52. Whittle CL Fakharzadeh S Eades J et al. Human breath doors and their use in diagnosis. Ann N Y Acad Sci 2007. 1098: 252–266
  53. Porter SR, Scully C. Oral malodour (halitosis). BMJ 2006; 23; 333(7569): 632-5.
  54. Lee SS, Zhang W, Li Y. Halitosis update: a review of causes, diagnoses, and treatments. J Calif Dent Assoc 2007; 35(4): 258-60
  55. Lee PP, Mak WY, Newsome P. The aetiology and treatment of oral halitosis: an update. Hong Kong Med J 2004; 10(6): 414- 8