Oral malodor. J Am Dent Assoc. 2003; 134:(2)209-214
Amir E, Shimonov R, Rosenberg M Halitosis in children. J Pediatr. 1999; 134:338-343
Tonzetich J, McBride BC Characterization of volatile sulphur production by pathogenic and non-pathogenic strains of oral Bacteroides. Arch Oral Biol. 1981; 26:963-969
Goldberg S, Kozlovsky A, Gordon D Cadaverine as a putative component of oral malodor. J Dent Res. 1994; 73:(6)1168-1172
Reingewirtz Y Halitose et parodontite; revue de littérature. J parodont d'implantol orale. 1999; 18:27-35
Bosy A, Kulkarni GV, Rosenberg M Relationship of oral malodor to periodontitis: evidence of independence in discrete subpopulations. J Periodontol. 1994; 65:(1)37-46
Lee H, Kho HS, Chung JW, Chung SC, Kim YK Volatile sulfur compounds produced by Helicobacter pylori. J Clin Gastroenterol. 2006; 40:421-426
De Boever EH, Loesche WJ Assessing the contribution of anaerobic microflora of the tongue to oral malodor. J Am Dent Assoc. 1995; 126:(10)1384-1393
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
Bollen CML, Beikler T Halitosis: the multidisciplinary approach. Int J Oral Sci. 2012; 4:55-63
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
Porter SR, Scully C Oral malodour (halitosis). Br Med J. 2006; 333:632-635
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Ratkay LG, Waterfield JD, Tonzetich J Stimulation of enzyme and cytokine production by methyl mercaptan in human gingival fibroblast and monocyte cell cultures. Arch Oral Biol. 1995; 40:337-344
Lancero H, Niu JJ, Johnson PW Exposure of periodontal ligament cells to methyl mercaptan reduces intracellular pH and inhibits cell migration. J Dent Res. 1996; 75:1994-2002
Miyazaki H, Arao M, Okamura K, Kawaguchi Y, Toyofuku A, Hoshi K, Yaegaki K Tentative classification of halitosis and its treatment needs. Niigata Dent J. 1999; 32:7-11
Oho T, Yoshida Y, Shimazaki Y, Yamashita Y, Koga T Characteristics of patients complaining of halitosis and the usefulness of gas chromatography for diagnosing halitosis. Oral Surg Oral Med Oral Pathol Oral Radiol Endod. 2001; 91:531-534
Rosenberg M, Septon I, Eli I, Bar-Ness R, Gelernter I, Brenner S Halitosis measurement by an industrial sulphide monitor. J Periodontol. 1991a; 62:487-489
Patil SH, Kulloli A, Kella M Unmasking oral malodor: a review. People's J Sci Res. 2012; 5:(1)61-67
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
Tanaka M, Anguri H, Nanaka A, Kotaoka K, Negata H, Kita J, Shizukuishi S Clinical assessment of oral malodor by the electronic nose system. J. 2004; 83:(4)317-321
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Mathew J, Vandana KL Detection and measurement of oral malodor in periodontitis patients. Ind J Dent Res. 2006; 17:(1)2-6
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Halitosis is an unpleasant condition that may be the origin of concern not only for a possible health condition but also for frequent psychological alterations which may lead to social and personal isolation. The most frequent sources of halitosis that exist in the oral cavity include bacterial reservoirs such as the dorsum of the tongue, saliva and periodontal pockets. Volatile sulphur compounds (VSCs) are the prominent elements of oral malodour. Genuine halitosis and pseudo-halitosis should be in the treatment realm of dental practitioners.
Clinical Relevance: Halitosis can be a symptom of underlying systemic disease, therefore the exact diagnosis and its source (oral or non-oral) is important in the proper approach to its management.
Article
The word halitosis is derived from the Latin word halitus, which means exhalation. Halitosis is a term used to refer to offensive or bad breath. Fetor exore, fetor oris and stomatodysodia (dysodia in Greek refers to stench) are other terms that have been used in literature to describe halitosis. Oral halitosis is the specific term used to describe halitosis that originates within the oral cavity.1,2 Breath malodour may be an important factor in social communication and, therefore, may be the origin of concern not only for a possible health condition but also for frequent psychological alterations leading to social and personal isolation. The importance of oral malodour goes beyond the knowledge of its cause, diagnosis and therapy because it interacts with other sociological issues such as culture, religion, race, sex and social taboos.
However, this condition was not studied scientifically until the 1940s and 1950s when Fosnick et al developed an instrument called the osmoscopy, which measures the sources of malodour. They demonstrated that this problem could be either physiologic or pathologic, and the source of bad breath could originate from the mouth, the nasopharynx, or various other parts of the body.
The ratio between female and male patients with oral malodour is almost the same; no gender-based differences have been found with regard to prevalence and severity of halitosis. However, it has been observed that women seek treatment more often than men.
Aetiology
The primary cause of halitosis is the release of volatile sulphur compounds (VSCs), which include hydrogen sulphide, dimethyl sulphide and methyl mercaptan. Methyl mercaptan (CH3SH) is believed to be the most malodorous component.3 Sulphur-containing amino acids [cysteine] are broken down by the anaerobic bacteria to release volatile sulphur compounds. Certain non-sulphur-containing substances like diamines [cadaverine4 (cadaver smell) and putrescine5 (rotting meat smell)], acetone and acetaldehyde also contribute to halitosis emanating from the oral cavity. Other potentially odour-producing substances include indole (used in small quantities in perfumes, however, large quantities can produce an offensive odour), skatole (faecal odour), short-chain carboxylic acids such as butyric and valeric acids (sweaty feet odour) and ammonia. The activity of bacteria is at its peak at a pH of 7.2 and inhibited at a pH of 6.5.6
Micro-organisms
Volatile sulphur compounds (VSCs) are believed to be produced by Gram-negative proteolytic anaerobes. These microbes are located in the stagnant areas of the mouth, such as the periodontal pockets, tongue surface, interproximal areas between the teeth and in the dental caries. The principal bacteria that are implicated in the creation of oral malodour include Fusobacterium nucleatum, Prevotella intermedia and Tannerella forsythensis. Other bacteria that have been implicated in the production of VSCs include Porphyromonas gingivalis, Porphyromonas endodontalis, Treponema denticola, Aggregatibacter actinomycetemcomitans, Atopobium parvulum, Campylobacter rectus, Desulfovibrio species, Eikenella corrodens, Eubacterium sulci, Fusobacterium species and Peptostreptococcus micros. Helicobacter pylori can produce VSCs and should also be considered as a possible cause of halitosis.7Klebsiella and Enterobacter are reported to have emitted foul odours in vitro which resembled bad breath in denture wearers.8
Exogenous (transient) causes of halitosis
The intake of food and drinks can either dry the mouth, such as alcohol-containing liquids (wine and some mouthwashes) and cigarettes, or provide high concentrations of protein or sugar. Dairy products are known to break down in the mouth and release amino acids that are rich in sulphur. Onion and garlic contain high concentrations of sulphur, which can pass through the lining of the intestine into the bloodstream, and subsequently be released into the lungs and then exhaled.
Smoking not only raises the concentration of volatile compounds in the mouth and lungs, but also further aggravates the situation because of its drying effect on the oral mucosa. Morning breath is related to the decreased saliva production and secretion resulting in the transient desiccation of the mouth.
Intra-oral causes of halitosis
Intra-oral causes of halitosis include:
Plaque-related gingival and periodontal disease, such as gingivitis, periodontitis, necrotizing ulcerative gingivitis, pericoronitis, abscesses;
Ulceration caused by malignancy, local causes, apthae, drugs;
Hyposalivation caused by drugs, radiotherapy, chemotherapy, Sjögren's syndrome;
Tongue coating resulting from poor oral hygiene;
Deposition of debris in dental appliances;
Bone disease such as osteomyelitis, osteonecrosis, dry socket and malignancy.
A study in the elderly found the accumulation of bacterial plaque on the tongue, oral dryness, burning mouth, overnight denture wear, and lower educational levels to be significantly related to oral malodour.9 Saliva seems to undergo chemical changes with ageing. As the amount of ptyalin decreases and mucin increases, saliva becomes thick and viscous and presents problems for the elderly.10
Patients with deep periodontal pockets are associated with increased levels of VSCs.11 Deep periodontal pockets are associated with low oxygen tension and low pH, which activates the decarboxylation of the amino acids (eg lysine, ornithine) to cadaverine and putrescine, which is a malodorous diamine. The presence of active periodontal inflammation has also been suggested to be more important for the production of oral malodour than just these periodontal pockets.11
Other causes of halitosis
Drug-induced
Amphetamine, chloral hydrate, cytotoxic drug, dimethyl sulphoxide, disulfiram, nitrate and nitrite, phenothiazine and solvent abuse are some drugs associated with halitosis.12
Systemic
Nasal sepsis (eg sinusitis, postnasal drip), diabetic ketosis, gastro-intestinal disease, hepatic failure, renal failure, respiratory infection and sinusitis, hiatus hernia, trimethylaminuria, fish-odour-syndrome (rare, smells of rotten fish due to insufficient enzyme to break down trimethylamine), post-irradiation therapy, Sjögren's syndrome.13,14
Hormonal
With increased progesterone15 levels during the menstrual cycle, a typical breath odour can develop. Evidence also indicates that VSC levels in the expired air are increased two-fold to four-fold about the day of ovulation and in the premenstrual period.
Effects of VSCs on gingivitis and periodontitis
Volatile sulphur compounds (VSCs) are potentially capable of altering permeability of the gingival tissues, inducing inflammatory responses, and modulating functions of gingival fibroblasts. VSCs penetrate deeply into the tissues where they can induce deleterious changes in the non-keratinized epithelium, basement membrane and underlying lamina propria, which can be demonstrated in histologic sections. VSCs are not only directly toxic to tissues, but they may also facilitate entry of other bacterial antigens, such as lipopolysaccharides (LPS), into the underlying lamina propria.16
Gingivitis results from the induction of an immune response accompanied by alterations in fibroblast function. CH3SH has been shown to induce secretion of IL-1ß from mononuclear cells in culture.17 Methyl mercaptan has also been shown to act synergistically with both LPS and IL-1ß to increase secretion of prostaglandin E2 and collagenase (important mediators of inflammation and tissue destruction). The effects of CH3SH on collagen metabolism are a reflection of both decreased synthesis and increased degradation of protein. Studies have shown that periodontal ligament (PDL) cells exposed to methyl mercaptan in culture alter their intracellular pH and become more acidic. In addition, they exhibit decreased motility, lowered protein synthesis and alterations in collagen metabolism. These changes are predominantly detrimental to the ability of these cells to maintain or regenerate mineralized tissues.18
Classification of halitosis
Miyazaki et al19 proposed a simple classification (Table 1) with corresponding treatment need (TN) of halitosis which includes the categories of genuine halitosis, pseudo-halitosis and halitophobia. Five classes (Table 2)19 of treatment need for halitosis have been categorized to provide guidelines for clinicians. Dental practitioners are responsible for the management of physiologic halitosis (TN-1), oral pathologic halitosis (TN-1 and TN-2) and pseudo-halitosis (TN-1 and TN-4), physician or medical specialist would manage the extra-oral pathologic halitosis (TN-3), and halitophobia (TN-5) would be managed by a physician, psychiatrist or psychological specialist.
Classification
Treatment Needs
Description
I. Genuine halitosis
Obvious malodour, with intensity beyond socially acceptable level, is perceived.
A. Physiologic halitosis
TN-1
Malodour arises through putrefactive process within the oral cavity. Neither specific disease nor pathologic condition that could cause halitosis is found.
Origin is mainly the dorso-posterior region of the tongue.
Temporary halitosis due to dietary factors (eg garlic) should be excluded.
B. Pathologic halitosis
(i) Oral
TN-1 and TN-2
Halitosis caused by disease, pathologic condition or malfunction of oral tissues.
Halitosis derived from tongue coating, modified by pathologic condition (eg periodontal disease, xerostomia) is included in this subdivision.
(ii) Extra-oral
TN-1 and TN-3
Malodour originates from nasal, paranasal and/or laryngeal regions.
Malodour originates from pulmonary tract or upper digestive tract.
Malodour originates from disorders anywhere in the body whereby the odour is blood-borne and emitted via the lungs (eg diabetes mellitus, hepatic cirrhosis, uremia, internal bleeding).
II. Pseudo-halitosis
TN-1 and TN-4
Obvious malodour is not perceived by others, although the patient stubbornly complains of its existence.
Condition is improved by counselling (using literature support, education and explanation of examination results) and simple oral hygiene measures.
III. Halitophobia
TN-1 and TN-5
After treatment for genuine halitosis or pseudo-halitosis, the patient persists in believing that he/she has halitosis.
No physical or social evidence exists to suggest that halitosis is present.
Category
Description
TN-1
Explanation of halitosis and instructions for oral hygiene (support and reinforcement of a patient's own self-care for further improvement of his/her oral hygiene).
TN-2
Oral prophylaxis, professional cleaning and treatment for oral diseases, especially periodontal diseases.
TN-3
Referral to a physician or medical specialist.
TN-4
Explanation of examination data, further professional instruction, education and reassurance.
TN-5
Referral to a clinical psychologist, psychiatrist or other psychological specialist.
Diagnosis
Oral malodour can be assessed by the following methods.
Patient history
There is a saying ‘Listen to the patient and he will tell you the diagnosis’. This is true for patients with breath odour complaints.
Besides what is spontaneously told, the clinician should also ask the following questions:
The frequency of odour (eg does it happen only some weeks);
The time of appearance within the day (eg after meals, which can indicate a hernia);
Whether others (non-confidants) have identified the problem (imaginary breath odour?);
What kind of medications are taken;
Whether dryness of the mouth is noticed, etc.
Medical history
A detailed history of the condition, duration, the severity, and the impact on the patient's everyday life should be taken, any predisposing and modifying factors investigated and concerns from the patient's family members also noted.
Clinical examination
A clinical examination should be carried out checking the patient's oral hygiene, caries, periodontal status, tongue coating and also plaque retention; all these factors should be recorded.
Radiographical examination
A radiographical examination could be used to look for evidence of dental caries, alveolar bone defects and defective restorations.
Self examination
A self examination could involve the following:
Smelling a sterile metallic or non-odorous plastic spoon after scraping the posterior part of the dorsum of the tongue.20 After about 5 seconds, the odour from the contents of the spoon is assessed, holding the spoon about 5 cm away from the nose.
Smelling a toothpick/dental floss after introducing it in an interdental area. The odour is assessed by holding the toothpick/floss about 3 cm from the nose.
Smelling saliva spit in a small cup or spoon.
Licking the wrist and allowing it to dry (reflecting the saliva contribution to malodour).
A subjective test scored on the basis of the examiner's perception of a subject's oral malodour. This is carried out simply by sniffing the patient's breath and scoring the level of oral malodour. A translucent tube (2.5 cm D, 50–70 cm L) is placed through the privacy screen, inserted into the patient's mouth. The patient then exhales slowly and the breath, undiluted by room air, can be evaluated and assigned an organoleptic score. The use of a privacy screen allows the patient to believe that he/she has undergone a specific malodour examination rather than the direct-sniffing procedure.
An organoleptic test19 should be carried out on two or three different days and recorded on the organoleptic scale:
Patients are given the following instructions before the assessment:
To abstain from taking antibiotics for three weeks;
To abstain from eating garlic, onion and spicy foods for 48 hours;
To abstain from ingesting any food or drink;
To omit their usual oral hygiene practices, using oral rinse and breath fresheners;
To abstain from smoking for 12 hours before the assessment;
To avoid using scented cosmetics for 24 hours.
The examiner, who should have a normal sense of smell, is required to refrain from drinking coffee, tea or juice, and to refrain from smoking and using scented cosmetics before the assessment.
Gas chromatography is a highly sensitive technique to assess breath malodour. This is considered the gold standard for measuring oral malodour since it is specific for VSCs, the main cause of oral malodour. Traditional laboratory gas chromatography or gas chromatography–mass spectrometry are cumbersome, need inert column carrier gas (gas cylinders of nitrogen or helium) and require technicians or specialists with adequate training, and are thus clinically impractical.10 The GC equipment is expensive, bulky and the procedure requires a skilful operator. Therefore, this technology has been confined to research and not to clinical use. However, a newly developed portable gas chromatograph (Oral ChromaTM, Abimedical, Osaka) has now been described, which does not use a special carrier gas (using air instead) and is highly sensitive yet relatively low cost compared with a standard gas chromatograph.10 The Oral ChromaTM analyses individual concentrations of volatile sulphur compounds, such as hydrogen sulphide, methyl mercaptan and dimethyl sulphide and displays the concentrations on a display panel.
Sulphide monitors analyse for total sulphur content of the subject's mouth air. Although compact sulphide monitors are inexpensive, portable and easy to use, most of them are not able to distinguish between the VSCs. For example, the Halimeter® analyses the total sulphur content of the individual's breath but cannot differentiate between various sulphides. The instrument measures parts per billion levels of hydrogen sulphide and, to a lesser extent, methyl mercaptan. A measurement is taken once a peak reading has been reached:23
Less than 100 is normal;
100–180 is minor halitosis;
Greater than 250 is chronic halitosis.
There may be false positive results due to other volatile vapours, such as acetone, ethanol and methanol that do not contribute to oral halitosis.
BANA (Benzyl D L arginine α naphthylamide) test
A BANA test6 is a chairside colorimetric assay that assesses the proteolytic activity of anaerobic bacteria. It is a rapid chairside test for the evaluation of non-sulphurous malodorous compounds. The BANA test correlates significantly with the organoleptic score.
Electronic nose
The FF-1 odour discrimination analyser (Electronic nose, Shimadzu Corporation) was used by Tanaka et al.24 Electronic noses25 are chemical sensors that have been used in recent times for the quantitative assessment of malodour associated with food and beverages. These electronic noses clinically assess oral malodour and examine the association between oral malodour strength and oral health status. The set-up comprises a pre-concentrator, an array of six metal oxide semiconductor sensors selected for their different sensitivities and selectivities to fragrant substances, and a pattern recognition software. The instrument can be set to various modes such as the ‘allnote measurement mode’ which is the standard setting used for measuring all volatile substances and the ‘topnote measurement mode’, which primarily measures volatile substances with a low boiling point. The results of a preliminary study showed that the main compounds related to oral malodour were volatile substances with a low boiling point.26
There are many other portable VSC monitors that are compact and relatively inexpensive, eg Tanita breath alert, Osmoscope, Halimeter and diamond probe. Another chairside test kit (Halitox reagent kit) measures halitosis-linked toxins. It is a quick, simple colorimetric test that detects both volatile sulphur compounds, as well as polyamines.27 A recent study using Tanita breath alert, BANA and a Halitox reagent kit, has shown that Tanita breath alert can be a useful tool in self assessment of malodour, but it is currently not available in India.28 The diamond probe/Perio 2000 system is a dental device designed to detect sulphide concentration of various forms (S, HS, H2S and CH3SH) in gingival sulci. The micro-sulphide sensor responds to sulphide ions and measures metabolic products of many anaerobic bacteria and, indirectly, bacterial activity. The reaction of the sulphide ions with the sensor generates a measurable voltage that is proportional to the sulphide concentration. Since sulphides are continually cleared from the pockets by crevicular fluid flow, the presence of high sulphide levels indicates a higher level of anaerobic bacterial activity.29 If the presence of sulphide was indicated above threshold (>0.5), the light on the front of the display panel would change colour, depending on the sulphide concentration, and an audible tone would sound.29
The management of halitosis
The available methods30 leading to a lowering of oral malodour level can be divided into:
The usage of masking products;
Mechanical reduction of micro-organisms and their substrates;
Chemical reduction of micro-organisms;
Chemical neutralization of odorous compounds, including volatile sulphur-containing compounds.
Patients diagnosed as suffering from non-oral halitosis should be referred to a clinic for otorhinolaryngology or internal medicine for appropriate treatment.
Masking products
The usage of masking products only is never an effective management of halitosis. Nevertheless, some commercially available products, such as mints, toothpastes, mouthrinses, sprays and chewing gums, attempt to control halitosis with pleasant flavours and fragrances. A short-term masking effect can be gained with menthol-containing gum and may be the result of the menthol.31
Mechanical reduction of micro-organisms and their substrates
Mechanical reduction of micro-organisms and their substrates can be achieved by taking a solid breakfast, improving hyposalivation, using chewing gum, brushing the teeth, flossing, using toothpicks, tongue cleaning and professional oral healthcare. The passage of solid food over the surface of the tongue may remove the tongue coating.3 Extreme hyposalivation increases the production of volatile sulphur-containing compounds.30 Salivary stimulation by eating breakfast, chewing or consuming acid food and saliva substitutes diminishes the effect of hyposalivation.22 Levels of VSCs could be reduced for at least 1 hour by brushing the teeth and the tongue, and then rinsing the mouth with water.27
Chemical reduction of micro-organisms
Toothpastes and mouthrinses with antimicrobial properties can reduce oral malodour by reducing the number of micro-organisms chemically.28 Often used active ingredients in these product are chlorhexidine,29 triclosan,24 essential oils15 and cetylpyridinium chloride.9 Other effective chemical agents are allylpyrocatechol, L-trifluoromethionine and dehydroascorbic acid.
Chemical neutralization of odorous compounds
Toothpastes, mouthrinses, lozenges and other products can reduce halitosis by chemically neutralizing odorous compounds, including VSCs. Often used active ingredients of these products are metal ions and oxidizing agents. Metals, such as zinc, sodium, stannous and magnesium are thought to interact with sulphur. This interaction forms insoluble sulphides. The mechanism proposed is that metal ions oxidize the thiol groups in the precursors of volatile sulphur-containing compounds.10 Oxidizing agents may reduce halitosis by reducing conditions necessary for metabolizing sulphur-containing amino acids to volatile sulphur-containing compounds.
Probiotics
The objective of probiotics10 is to prevent the re-establishment of non-desirable bacteria and thereby limit the re-occurrence of oral malodour over a prolonged period. Recently, several studies were performed to replace bacteria responsible for halitosis with probiotics such as Streptococcus salivarius (K12), Lactobacillus salivarius or Weissella cibaria. Several studies conclude that probiotic bacterial strains, originally sourced from the indigenous oral microbiotas of healthy humans, may have potential application as adjuncts for the prevention and treatment of halitosis.32 The oral administration of the probiotic lactobacilli not only seemed to improve the physiologic halitosis, but also showed beneficial effects on bleeding on probing from the periodontal pockets.33
Conclusion
Malodour should not be considered as just cosmetic therapy, since the available evidence indicates that many VSCs are toxic to periodontal tissues, even when present at extremely low concentrations. Periodontal tissues, unlike the tongue and alveolar mucosa, are not protected by a keratinized layer and may be particularly susceptible in injury. Traditional procedures of scaling, root planing and the practice of oral hygiene, combined with tongue-scraping, are effective at reducing levels of these compounds in mouth air and are satisfactory as cosmetic treatment. Underlying systemic disease should also be considered as a possible source of aetiology and appropriately management accordingly.
