Halitosis: a New Definition and Classification

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Halitosis: a new definition IN BRIEF • Suggests previous halitosis classification RESEARCH systems omit some aetiologies, and their and classification diagnoses hinged on single occasion halitometric and organoleptic findings, which are unreliable. M. Aydin*1 and C. N. Harvey-Woodworth2 • Proposes halitosis diagnosis should focus more on the declarations of the patient and his/her social environment. • Suggests the new classification completely covers all possible aetiologies of halitosis.

Background There is no universally accepted, precise definition, nor standardisation in terminology and classification of halitosis. Objective To propose a new definition, free from subjective descriptions (faecal, fish odour, etc), one-time sulphide detector readings and organoleptic estimation of odour levels, and excludes temporary exogenous odours (for example, from dietary sources). Some terms previously used in the literature are revised. Results A new aetiologic classification is proposed, dividing pathologic halitosis into Type 1 (oral), Type 2 (airway), Type 3 (gastroesophageal), Type 4 (blood-borne) and Type 5 (subjective). In reality, any halitosis complaint is potentially the sum of these types in any combination, superimposed on the Type 0 (physiologic odour) present in health. Conclusion This system allows for multiple diagnoses in the same patient, reflecting the multifactorial nature of the complaint. It represents the most accurate model to understand halitosis and forms an efficient and logical basis for clinical management of the complaint.

LITERATURE REVIEW Previous definitions Halitophobia Intra-Oral Halitosis is receiving increasing scientific Pseudo-halitosis Halitosis interest, but still no accepted definition exists. In the literature, definitions include: Genuine halitosis Extra-Oral ‘the subjective perception after smelling someone’s breath, if unpleasant’,1 ‘noticeably unpleasant odours exhaled in breathing’,2 Pathologic Physiologic Blood borne Non-blood borne ‘an oral health condition characterised by halitosis halitosis unpleasant odours emanating consistently from oral cavity’,3 ‘general term to describe any disagreeable odour of breath, regardless Oral Extra-Oral of its origin’,4 and ‘an unpleasant odour (Miyazaki et al., 1999) (Tangerman et al., 2010) emanating from oral cavity.’5 Many definitions are inadequate, ignoring Fig. 1 Two previous classifications. Miyazakiet al . 1999 is generally the most widely used, but 5 the potential emanation of odours via the neither is universally accepted mouth and nose from the respiratory and gastroesophageal tracts, transfer of volatiles or the clinician by sulphide detectors to North American society with regards to from blood to breath during alveolar gas (halitometers)? Some refer to exogenous halitophobia, and appeared in publications exchange, and also self-perception of odorants (for example, garlic) as halitosis, a decade ago.7–9 This classification is inflex- halitosis by the patient. To varying degrees yet this is not pathologic. To distinguish ible since multiple diagnoses for one patient the breath always has odorant volatiles, normality from disease, a more precise are not enabled. The broad category ‘extra- originating orally or elsewhere. None set a definition and classification is needed. oral, pathologic halitosis’ does not aid clear boundary between normal, physiologic This paper reviews previous attempts at referral choice or help the receiving clini- breath odour and, pathologic halitosis. classification and definition of halitosis and cian, and is also poor for researchers who Negative identification of an odour requires forwards a new scheme. The diagnosis and need to precisely classify extra-oral halito- qualification. Who determines this? The treatment of halitosis according to this scheme sis according to aetiology. ‘Morning breath’ patient, the patient’s social environment, are discussed in a separate publication. is not placed in the oral category, despite manifesting orally. Inappropriately, two out 1Private practice, Turkey; 2Private practice, London Previous classifications of three categories (pseudo-halitosis and *Correspondence to: Dr Murat Aydin 6 Email: [email protected] Miyazaki et al. suggest genuine halitosis, halitophobia) have psychopathologic con- pseudo-halitosis and halitophobia (Fig. 1). notations and they are excluded from patho- Online article number E1 Genuine halitosis is divided into physiologi- logic halitosis. Subjective halitosis can be Refereed Paper - accepted 24 February 2014 DOI: 10.1038/sj.bdj.2014.552 cal or pathological, then the latter is split caused by psychologic or neurologic factors, ©British Dental Journal 2014; 217: E1 into oral and extra-oral. This was adapted which are technically extra-oral processes,

yet ‘extra-oral halitosis’ is again excluded compound (VSC) levels are normal. There clinically existent, self-producing odour; from pathologic halitosis. After treatment, is no local or systemic condition and no imaginary halitosis describes halitosis whether for genuine halitosis or pseudo- reliable, third party confidants confirming produced psychologically; and phantom halitosis, if the patients continue to believe the complaint. This scenario is generally halitosis is neurologic they have halitosis, reclassification to halito- ascribed to psychologic factors, termed • Morning breath is sometimes used phobia occurs. This categorises cases accord- imaginary halitosis,14 delusional halitosis,15 instead of physiologic halitosis, but these ing to treatment outcome, as halitophobia is pseudo-halitosis,7 non-genuine halitosis,16,17 are also dissimilar. Not all ‘morning diagnosed following a failed treatment. This chronic olfactory paranoid syndrome,18 breath’ is physiologic. scheme claims to provide treatment needs, anthropophobia (taijin kyofusho),19 but how can these be determined before- halitophobia,20 olfactory reference syndrome NEW DEFINITION OF HALITOSIS hand if they depend on results of treat- (ORS),21,22 and social anxiety disorder.23 These Objective halitosis has been defined ment? Pseudo-halitosis is misleading when terms may easily cause confusion. as ‘malodour with intensity beyond a considered alongside other medical terms, The term psychosomatic halitosis is socially acceptable level perceived’.7 This is for example, pseudo-Cushing’s syndrome, incorrectly used when referring to subjective independent from halitometric readings and intestinal pseudo-obstruction, pseudo-lym- halitosis complaints. Psychosomatic subjective odour descriptions. This should be a phoma or pseudo-Kaposi’s sarcoma. These disorders are disorders in which psychologic basic definition of objective halitosis, but must exist as physical entities that masquerade factors play a significant role and there be qualified with several important points: as their namesake. Pseudo-halitosis implies are physical symptoms that are detectable • A halitosis complaint may be objective, a genuine, physical condition mistaken for clinically. However, the term psychosomatic where there is an unpleasant odour non-existent halitosis. Similarly, halitopho- halitosis is used to describe an odour is that endogenously produced anywhere in bia suggests an irrational fear, but instead is clinically non-existent. the body, emitted from the mouth and/ refers to where the patients believe their Terms that refer to odour character or nose and detectable to others; or treatment unsuccessful. promote confusion for clinicians and subjective, where there is no detectable Tangerman and Winkel suggest intra- and patients, for example sulphurous/faecal, odour to others but the patient extra-oral halitosis, the latter then divided fruity, and ammoniacal/urine-like; complains of its presence into non-blood-borne and blood-borne.10 respectively attributed to VSC, acetone, • Anyone who complains of halitosis, An earlier publication divides extra-oral and ammonia with other amines.10 Sweet, objective or subjective, should be halitosis into blood-borne, upper respiratory musty or fishy are used to describe particular considered a ‘halitosis patient’ tract and lower respiratory tract.11 They list halitosis types. However, fish odour is non- • Evidence of objective halitosis is a four aetiologic mechanisms of blood-borne specific for trimethylaminuria (TMAU),24 clinical picture built of (i) reliable reports halitosis: systemic diseases, metabolic as is acetone for diabetes. All individuals from the patient’s social environment disorders, food and medications.10 These have detectable breath acetone >400 ppb,25,26 for example, family members or close authors use ‘pseudo-halitosis/halitophobia’ especially when fasting. Fish odour can be friends, (ii) patient’s self declaration to describe no measurable halitosis, perceived as musty and acetone as sweet. of halitosis, and to a lesser extent (iii) while retaining their own classification The sweet, musty aroma in liver failure has halitometric readings for measurable halitosis.12 In reality, this been termed fetor hepaticus.27 This is also • A lack of complaints from the patient’s classification focuses on oral and blood-borne described as faecal, ‘the smell of dead mice’ social environment including family halitosis, with insufficient categorisation of or ‘the breath of the dead’.28 members, suggests that there is no physiologic, sinonasal, laryngopharyngeal, Other terms include ‘denture odour’,29 objective halitosis. Furthermore, if gastroesophageal or psychologic causes. The ‘uraemic fetor’ in renal failure,30 and ‘rotten there are no complaints from either the significance of blood-borne halitosis relative egg’ in poor oral hygiene. All these terms are patient or his/her social environment, to other extra-oral mechanisms is unclear subjective and open to misinterpretation. There this usually implies that there is no need and a broad division into blood-borne and is no standardisation in terminology, which to diagnose halitosis or treat, even if non-blood-borne may be inappropriate. has led to discrepancies developing where halitometric measurements appear to Again, this system does not allow for some authors use a term with one definition indicate the presence of elevated VSC. multiple diagnoses, making accurate and others with different meaning. As a rule, halitometers measure VSC, not categorisation of some cases difficult, and • Oral malodour, oral halitosis, tongue halitosis there is no distinction between pathologic malodour, odontogenic halitosis, • Halitosis is considered unpleasant by the and physiologic halitosis. pathological halitosis, objective halitosis, patient and his/her social environment. Motta et al. suggest primary halitosis genuine halitosis and intra-oral halitosis If the odour is not perceived negatively, (‘respiration exhaled by the lungs’), and are used incorrectly as synonyms for it is not halitosis secondary halitosis (‘originates in mouth halitosis.31 For example, oral malodour • Halitosis is almost always chronic in or upper airways’).13 It is unclear if primary includes all odours originating orally, not nature, although it may be intermittent halitosis refers to blood-borne halitosis, just the tongue; but not all pathologic/ • Some diseases (tonsillitis, pharyngitis, odour from the lower respiratory tract objective halitosis originates orally etc) or transient oral flora or metabolic itself, or both. This is seldom used, perhaps • Pseudo-halitosis, psychosomatic changes in the body may cause bad because the clinical utility is limited by halitosis, halitophobia, self-halitosis, odour in the short term (<2 months), not addressing subjective halitosis or imaginary halitosis non-genuine which disappears when the condition gastroesophageal halitosis. halitosis, delusional halitosis and resolves. Such bad odours are called phantom halitosis are also sometimes temporary halitosis Previous terminology used interchangeably,32 but they not • Some volatile foodstuffs possess specific In some cases, odour is not detected synonymous, for example, halitophobia odours (for example, garlic, onion) and organoleptically and volatile sulphur describes a fear; self-halitosis describes may cause short term halitosis (‘dietary

exchange in pulmonary alveoli. Therefore, minimal amounts of Types 1‑5 potentially Type 1 - oral exist in health. The total level of odour and the relative contributions of these different sources of physiologic odour is Type 2 - airway subject to both interpersonal variation, and also variation in the same individual from one occasion to the next. One or multiple Type 3 - gastroesophageal types may exist in any combination at any time, varying according to many different factors, including hydration, oral hygiene,

HALITOSIS microbiota, salivary flow rate, nature of last Type 4 - blood borne food consumption, biochemical, hormonal, mechanic activity of the body, fasting, sleep, digestive enzyme profile in gut, momentarily Type 5 - subjective amino acid and electrolyte profile in serum etc. It is distinguished from oral halitosis (Table 1). Type 0 Type 1 halitosis: oral halitosis

Physiologic Pathological halitosis The gases that contribute to Type 1 (oral) halitosis halitosis are (greatest to least): VSC, volatile organic compounds (VOC) and nitrogen Fig. 2 New etiologic classification proposed containing gases (amines).33 The main VSC

involved are hydrogen sulphide (H2S), methyl Table 1 Outlines the differences between Type 0 and Type 1 halitosis. Physiologic halitosis sulphide (CH3SH, or methyl mercaptan, should not be confused with a low level of oral (Type 1) halitosis since there are differences MM), and dimethyl sulphide [(CH3)2S, DMS]. Type 0 Type 1 Nearly 700 different compounds have been detected orally,34 including indole, skatole, Duration Always present; fluctuating While a cause exits acetic acid and short chain acids (for Originates Mouth + elsewhere Mouth only example, butyric, valeric, isovaleric, lactic, caproic, propionic and succinic acids). In Detectable on Mouth air + breath Mouth air halitosis patients, the 30 most abundant Offensive Possibly Yes VOC in mouth air are alkanes or alkane derivatives, and of these the most common Treatable No Yes are methyl benzene, tetramethyl butane, and Preventable No Yes ethanol.35 Alkanes are aromatic breakdown products from reactive oxygen species Detectable by halitometer Yes Yes acting on inflamed tissues.35 Others report acetone, methenamine, isoprene, phenol, odour’), as with certain medications or low as to give negligible contributions to the and D‑ limonene are the most abundant intoxications. All are called temporary overall complaint, or there may be multiple organic compounds in mouth air in oral halitosis, managed with reassurance contributing factors in the same patient. This halitosis patients. The organoleptic level and advice, and further diagnosis or can be recorded as Type 1 + 3, Type 2 + 4, of oral halitosis correlates with VSC,34 and treatment is unnecessary. Type 1 + 4 + 5 halitosis, etc. Previous amines (such as putrescine, cadaverine, classifications oversimplify halitosis, and this and trimethylamine).36 NEW CLASSIFICATION new classification is the most representative The gases responsible for oral halitosis OF HALITOSIS model proposed. are by-products of protein and glycoprotein Types 1‑5 (Fig. 2) represent different odour putrefaction by the oral microbiota. The mechanisms, which may be present in any Type 0 halitosis: dorso-posterior tongue is the most important combination at any time. Potentially, each physiologic halitosis halitogenic site, by virtue of having both the type of pathologic halitosis (Type 1‑5) is Type 0 halitosis represents the sum of largest surface area and the highest bacterial superimposed on physiologic odour (Type the physiologic contributions of oral, load, within a densely populated biofilm.37–39 0). At any given time, pathologic halitosis is airway, gastroesophageal, blood-borne About 85% of oral halitosis cases are caused the sum of the all these types sources, as well and subjective halitosis that are potentially by poor oral hygiene, plaque stagnation as their respective underlying physiologic present in every healthy person, in any areas, gingivitis, and tongue coating.31 contributions. combination. All healthy individuals However, a degree of oral bacterial action The relative contributions of these have a certain level of bacterial activity is continuously present in health, even with different physiologic and pathologic in the mouth and on respiratory tract impeccable oral hygiene, and this constitutes aetiologies is subject to interpersonal mucosae. In addition there is a potentially the physiologic part of Type 1 halitosis. variation and may fluctuate even within a negligible amount of gas leakage from the Specific bacteria, especially anaerobes, hours in the same individual. Sometimes gastroesophageal tract, and blood gases are are suggested to cause oral halitosis.40,41 In the level of one or more types may be so transferred to the exhaled breath during gas reality, most oral bacteria are potentially

odorigenic, releasing VSC, VOC and/or Obstructive nasal pathology causes gastroesophageal reflux disease (GERD), amines. Depending upon the constituents mouthbreathing, possibly resulting in ii) Helicobacter pylori related gastritis, or of the gas produced by oral bacteria and xerostomia and halitosis.13,55 iii) other causes for example, gastrocolic ecologic factors in the mouth (for example, Tonsillitis causes oedema and hypertrophy, fistulae, Zenker diverticulum and microbiota compositional fluctuations, which may obstruct orifices on tonsillar hypopharyngeal diverticulae.66 Falcao et al. available nutritional substrate, bacterial surface. This disrupts the cleansing flow of argued that certain GI disorders can cause metabolism) momentarily determine the secretions, and desquamated epithelial and taste disturbance. Taste receptor cells are composition and level of odour. Therefore, bacterial cells, extracellular matrix and food associated with lingual papillae, but also the diagnostic value of the odour character debris become trapped, leading to stagnation. present on the palate, epiglottis and upper at any one time is questionable. To consider Bacteria putrefy local substrate and release oesophagus. Low intensity acid reflux can some bacteria as odorigenic and others as VOC and VSC, expressed on the breath as cause phantom taste sensations, which may non-odorigenic is oversimplification. In halitosis with a similar mechanism that manifest as subjective halitosis.16 reality every bacterium is odorigenic, and operates on the tongue surface. Crypt debris Evidence for GERD-related halitosis is there is a continuous spectrum from low to may mineralise, similar to the transformation contradictory. Some studies report self- high degree of odour formation capability.33,42 of dental plaque to dental calculus. These reported/subjective halitosis complaints Other possible origins of oral halitosis mineralised deposits are termed tonsilloliths are associated with GERD.68–71 One study include: periodontal disease, acute necrotising (tonsil stones). The presence of tonsilloliths reported gastroesophageal pathology in ulcerative gingivitis, osteoradionecrosis, is strongly associated with abnormal VSC less than 50% of patients complaining large carious cavities, blood/thrombi (for levels.46 They are asymptomatically present of halitosis,72 while others report that GI example, extraction sockets), ulceration, in up to 10% of the general population.56 disorders may account for up to 5% of interdental food packing, oral prostheses Anaerobic bacteria detected in tonsilloliths objective halitosis complaints.31 A systematic (dentures, orthodontic appliances, bridges). include Eubacterium, Fusobacterium, review investigated the relationship between Porphyromonas, Prevotella, Selenomonas GERD and halitosis (among other things). Type 2 halitosis: airway halitosis and Tanerella spp., all associated with the Three studies were included, and the authors Type 2 halitosis originates from the production of VSCs.57 concluded halitosis is a possible extra- respiratory tract itself (rhinosinusitis, Odorous gases from the mouth or present oesophageal symptom of GERD,73 however, tonsillitis, pharyngitis, laryngitis, in oronasal secretions can excite olfactory two of these studies utilised questionnaires bronchitis, pneumonia), anywhere from receptors and be perceived as halitosis,58 (that is, subjective halitosis). Yoo et al. report nose to alveoli. Odorous gases produced by even if no halitosis can be detected H. pylori infection correlated with elevated various respiratory pathoses are held in the halitometrically. This is retronasal olfaction VSC in mouth and mucosal erosions,74 exhaled breath and expressed via the nose and is usually misdiagnosed. posing halitosis as a potential biomarker or mouth. This should be distinguished ‘Airway reflux’ describes gaseous or liquid to distinguish between erosive (200 ppb) from Type 4 (blood-borne) halitosis, where gastric contents refluxing to the pharynx, and (75 ppb) non-erosive GERD.75 Gas volatiles from the systemic circulation are oral cavity, nasal cavity, paranasal sinuses or chromatography on gastric juice and biopsies transferred during gas exchange to the even the middle ear,59 and is sometimes said in these subjects found resolved 7.5 ppm breath. Some studies report the proportion to be a cause of halitosis, however, there is significantly higher 2H S and expression of of halitosis cases that are due to upper little credible evidence for this mechanism. VSC-releasing enzymatic activity in the respiratory tract pathology to be between Other respiratory tract causes of halitosis erosive group, and 0.5 ppm in the non-erosive 2.9 and 10%.31,43–47 include: laryngitis, tracheitis, bronchitis, group.74 However, another study reported no Halitosis is considered a regional symptom bronchiectasis, pneumonia, tuberculosis, significant difference in halitosis parameters of chronic rhinosinusitis, and some report nasal foreign bodies, rhinoliths, atrophic when comparing erosive and nonerosive as many as 50‑70% will complain of rhinitis (ozena), abscesses (peritonsillar, GERD.76 Others have suggested the stomach halitosis.48,49 In paediatric patients, one of nasopharnygeal, lung), and carcinomas rarely causes halitosis10 and gastroscopy in most frequent symptoms is halitosis together (nasal, sinuses, pharyngeal, lung).10,60–65 halitosis patients is entirely unnecessary,12 as with cough, rhinorrhoea and sniffling,50 even the findings do not correlate with halitosis.77 when nasal obstruction, post-nasal exudate, Type 3 halitosis: It has also been argued that there is no pain, sneezing and secretion are clinically gastroesophageal halitosis evidence that odorous substances are formed absent.51 Sinonasal anatomic variations (for Type 3 halitosis is leakage of odorant volatiles in the stomach.12 Another study reported no example, agger nasi cells, pneumatisation of from the stomach via the oesophagus to the statistically significant difference in the turbinates or septum; deviated nasal septum) mouth and nose. This should be distinguished prevalence of halitosis symptoms between are very commonly found together with from volatiles in the GI tract being absorbed children with GERD and those without.78 mucosal pathoses including rhinosinusitis.52 into the systemic circulation and exhaled H. pylori infection also has a controversial Post nasal drip is where mucus drains onto (Type 4, blood-borne halitosis). A degree of role. H pylori possesses a strain-dependent 53 the dorsal tongue via the nasopharynx. gastroesophageal reflux is considered normal, ability to synthesise H2S and MM from This is related to allergic rhinitis, however, occurring in almost all individuals several combined cysteine-methionine substrate the existence of post-nasal drip as a clinical times per day.66 In a study of 14 healthy in vitro.79 Elevated levels of both hydrogen entity is disputed as this occurs in health and individuals, 1.2 ml/10 min gas leakage from cyanide and hydrogen nitrate were there is no agreed definition or pathologic the stomach to the oesophagus while lying detected on the breath of H. pylori infected changes.54 Mucus stagnation provides a horizontal and 6.8 ml/10 min while sitting was patients compared to healthy controls;80 proteinaceous medium for more bacterial demonstrated.67 If odorous, this constitutes the however, whether this represents Type 3 or putrefaction, but the relationship between physiologic part of gastroesophageal halitosis. Type 4 (blood-borne) halitosis is unknown. halitosis and post-nasal drip has not been Pathologic level of gastroesophageal Oral H. pylori colonisation without gastritis formally investigated. halitosis is said to occur due to i) may cause Type 1 (oral) halitosis. PCR detected

Table 2 Example of aromatic gases exhaled in healthy individuals breath. Every exhaled odorant gas should be suspected as potentially contributing, by Breath gas Normal level (ppb) Reference Associated with varying degrees, to the overall perception of breath odour. 833 25 Protein or amino acid metabolism, nitrogen Ammonia 422‑2390 96 In pathologic Type 4 halitosis the metabolism 688 97 concentrations and profile of exhaled gases is significantly different to those seen 477 25 661.3 98 in health, depending on the pathology. Acetone Lipid metabolism 462 26 Exhaled breath volatiles are reported in 293‑870 96 diabetes mellitus, sleep apnea, H. pylori 461 25 Abnormal gut flora, renal or pancreatic infection, sickle cell disease, asthma, breast Methanol 32‑1684 99 insufficiency, carbohydrate malabsorption cancer, lung carcinoma, chronic obstructive 112 25 pulmonary disease, cystic fibrosis, liver Ethanol 27‑153 96 Bacterial overload in gut diseases, cirrhosis, uraemia, kidney failure 184 (7‑18 age) 26 and TMAU.24,94 106 25 Breath alkanes have a pungent odour and Isoprene 117.6 98 Cholesterol synthesis are elevated in intestinal inflammation,110 212 100 for example, ulcerative colitis,111,112 Crohn’s 18 25 112 113 Propanol Pancreatic insufficiency disease, in pulmonary tuberculosis, 20 26 schizophrenia,114 pneumonia,115 asbestos- 22 25 related disorders,116 stomach cancer,117 and Acetaldehyde 10 100 Alcohol metabolism angina pectoris.118 Pregnant females or pre- 24 101 eclampsia patients have a specific breath gas Butane 2.4 102 Protein oxidation/colonic bacteria profile, including undecane, ‑6 methyltridecane, 2‑methylpentane, 5‑methyltetradecane and Alkanes C13‑C20 1.5 x10–10 M/l 103 Oxidative stress 2‑methylnonane.119 DMS, acetone, 2‑butanone Dimethyl sulphide 0.2 nMol/l 12,104 Hepatic metabolism and 2‑pentanone are reported in liver failure, including cirrhosis.27 Hydrogen* <10 ppm 105 Carbohydrate metabolism in gut The ‘fetor hepaticus’ of hepatic failure *Hydrogen is odourless, but its elevation >10 ppm in breath may indicate small intestinal bacterial overgrowth syndrome, ileocaecal valve 28 syndrome, ileitis, or carbohydrate malabsorption/intolerance.106,107 Along with methane, hydrogen is an indicator gas used in disaccharide is largely caused by DMS, not ammonia. malabsorption tests to detect intestinal gases exhaled in breath.105 Odorous breath gases (Type 4 halitosis) are potentially present when breath Elevated blood DMS (‘dimethylsulphidemia’),28 hydrogen is elevated33 was reported to be responsible for the majority of cases of blood borne halitosis.12 H. pylori in 6.4% (21/326) of saliva samples constituting the phsyologic aspect of Body odour may accompany from non-dyspeptic individuals complaining Type 4 halitosis (Table 2). Type 4 halitosis as the same volatiles are of halitosis. H. pylori was associated with Methylated or low carbon containing also excreted during perspiration. This is higher MM concentration.81 alkanes, cyclic hydrocarbons, alcohols sometimes termed blood-borne body odour Improvements in halitosis (defined by and aldehydes has an especially pungent and halitosis. An example is TMAU, a rare various methodologies) following eradication odour when they exceed specific odour condition, classically characterised by fish therapy are reported.82–87 Positive correlation thresholds for the individual or his/her odour in urine, sweat and breath. between H. pylori and halitosis is reported social environment, constituting pathologic When odorous chemical in blood circulation by some studies,88–90 however, some of these Type 4 halitosis. The threshold concentration exceeds a critical level then it is secreted to can be criticised for relying on self-reported for any given chemical depends on the breath, urine, tear, saliva and sweat. In such halitosis rather than semi-objective breath change in intensity (odour strength) with conditions body odour appears. In other analysis.91 Others report no statistically concentration and the odour character. There circumstances, breath odour (Type 4 halitosis) significant correlation.69,77,91–93 is also interpersonal variation in emotional is detected without body odour. This mechanism is rarely responsible for reactions to detected odour; some may Another potential blood-borne mechanism halitosis, but cannot presently be dismissed react positively and others negatively.108 A may contribute to a halitosis complaint when due to several studies that support the idea single volatile chemical can be perceived at blood-borne odorants stimulate olfactory that GI disease may cause halitosis. lower concentrations than expected when receptors via their blood supply.16,120 it is combined in a mixture of thousands Strong olfactory receptor responses can Type 4 halitosis: of VOC like the breath by interaction with be triggered by intravascular injection of blood-borne halitosis other odorants and collective stimulation of odorants in tracheotomised animals. Such Type 4 (blood-borne) halitosis is where olfactory receptors. odour perceptions are not occurring by the volatile chemicals in the systemic circulation Artificial systems containing chemical normal air-borne route, so there may not be can transfer to exhaled breath during sensor arrays for the detection of breath measurable halitosis. alveolar gas exchange and cause halitosis.94 volatiles allow for profile readings of multiple Volatiles are endogenously produced, compounds instead of single sensors for a Type 5 halitosis: subjective halitosis mostly by-products of biochemical single volatile.109 This is more favourable as Subjective halitosis is a halitosis complaint metabolic processes.11 The concentration of breath odours are not limited to a single or without objective confirmation of halitosis by volatiles on the exhaled breath reflects their a handful of gasses describable according others or halitometer readings. Type 5 halitosis respective arterial concentrations.24 Healthy to their individual threshold levels. Rather, can be misdiagnosed if there are measurement subjects’ breath contains 3,481 VOCs,95 breath odours are ‘olfactory spectra’ of errors or transient symptoms.

It can be considered normal for even Olfaction and gustation are intimately Type 1 and 2 halitosis. Increased breath mentally healthy individuals to worry interlinked at the neuronal level in the ammonia, acetone,97,129 and isoprene,127 occasionally about to be having halitosis.121 brain. The definition of subjective halitosis occur after overnight fasting. Intestinal Such halitosis concern can be rationally (pseudo-halitosis) has been broadened: ‘the gas builds up in the colon during dismissed by most healthy people who have perception of an alteration in the quality sleep,130 possibly due to immobility and a degree of psychological resilience that of expired odour air, a symptom perceived microbial fermentation of intestinal is capable of compensating for stressors. only by the patient.’16 Many patients fail to contents. More Type 4 halitosis might This normal level of concern for halitosis distinguish between bad taste and bad odour. result, or possibly, more gas leakage constitutes the ‘physiologic’ aspect of Gustatory stimuli may influence orthonasal from the gastroesophageal valve (that Type 5 halitosis. and retronasal odorant perception.58 is, Type 3). All the above mechanisms Pathologic subjective halitosis can be Side effects of medication, hypothyroidism, may operate during sleep. The resultant categorised as psychologic or neurologic. hyposalivation (another extensive halitosis upon waking can be termed differential), nutrient deficiency (zinc, copper, morning breath, in reality an enhanced Psychologic causes iron, and vitamins A and B12), trauma and form of Type 0 halitosis Psychologic factors can cause subjective tumours involving the olfactory centre in the • Psychosomatic halitosis should be halitosis. This is termed monosymptomatic brain, or nerve damage (glossopharyngeal, retained, but the term should not be hypochondriacal psychosis,16 a type of vagus, chorda tympani, olfactory), misused. Some hypothesise that anxiety obsessive-compulsive spectrum disorder,121 neurodegenerative diseases (Parkinson’s, enhances oral VSC production.131 or olfactory reference syndrome (ORS). Alzheimer’s and Huntington’s disease), This mechanism is correctly termed Seventy-five percent of ORS patients present environmental pollutants (for example, psychosomatic, since a physical with halitosis complaints,122 but obsession smoking), drug abuse, certain oral hygiene symptom is being influenced by over other non-existent body odours, products (for example, mouthwashes) and psychologic factors. This is the uniquely often in combination, are included. Others’ certain foodstuffs can all be potentially correct usage of the term ‘psychosomatic behaviour (for example, opening windows, involved in subjective halitosis complaints halitosis’, rather than previous meanings sniffing, touching noses etc) is misinterpreted by various mechanisms.16,125 As described (see ‘Previous terminology’) as evidence of halitosis. Employment loss, previously, diabetes mellitus, GERD and • Self-halitosis has been used to describe divorce or suicidal ideation are reported.123 blood-borne stimulation of taste and smell a lack of objective halitosis even though ‘Doctor shopping’ to find clinicians to treat the receptors via the blood circulation may also the patient believes themselves to have non-existent odour may occur. However, some contribute to subjective halitosis.16,126 halitosis,32 but it is better used to define report that TMAU or other genuine odour endogenously produced, self-perceived symptoms can be misdiagnosed as ORS.124 NEW TERMINOLOGY odour, which is not a detectable odour to It may be the case that the previously black Unhelpful terms no longer needed: others. By true description, self-halitosis and white thinking of objective halitosis on appears in three forms: retronasal the one hand and psychologic halitosis on • Many of the confusing array olfaction, olfactory receptor responses the other is an oversimplification. Instead, of synonyms used to describe a triggered by blood-borne odorants, and it might be more accurate to consider a psychologic, subjective halitosis phantom tastes/odours spectrum, with entirely subjective halitosis at complaint (which would fall within • Halitophobia should be retained with one extreme and entirely objective halitosis Type 5 halitosis) are unneeded, including correct meaning. It refers to ‘fear of with no psychologic concern at the other. pseudo-halitosis, non-genuine halitosis, having halitosis’ but not ‘untreated Most patients will fall somewhere between delusional halitosis, olfactory obsession, halitosis’. these two points. psico-olfactory sensitivity, olfactory When objective halitosis has not been depression, halitosis anxiety and New terms treated it may cause the patient distress or imaginary halitosis • Exogenous odour results from social isolation and eventually over-concern • Subjective, descriptive terms such as consumption of aromatic foodstuffs (for about halitosis may develop. Even after sulphurous, ammoniacal, faecal, fishy example, garlic, onion, spicy foods), the odour is reduced to physiologic levels, or similar should be discontinued since beverages (for example, alcohol) or the negative psychosocial sequelae may they invite misunderstanding. tobacco. Exogenous volatiles may be persist, making these cases difficult to treat. released transiently from residues of Conversely, oversensitivity to physiologic Useful terms that are retained: food or drink in the mouth, or released odour may be the basis of a subjective • Objective halitosis refers to any unchanged via the blood-borne halitosis with no history of objective combination of Types 1‑4, but should not mechanism after being absorbed. Such halitosis. refer to Type 1 (oral) halitosis exclusively odours are distinguished from pathologic • Morning breath is a temporarily halitosis, for example, garlic smells like Neurogenic causes increased physiologic halitosis garlic. The terms garlic odour, spice Traditionally, subjective halitosis complaints during sleep and disappears soon odour, etc seem suitable. Dietary or are attributed to psychologic factors, after waking.127 Xerostomia is largely temporary halitosis are also terms that but at least some are neurologic. Nearly responsible,128 resulting from diminished could be argued to be useful 200 disorders can cause chemosensory salivary and respiratory secretion • Halitosis is an endogenous odour dysfunction (CSD).16 Dysosmia (disordered during sleep, especially when the because it is produced in the body. olfaction including parosmia and mouth remains open. Proteinaceous phantosmia) and dysgeusia (disordered substrates in saliva allows for microbial DISCUSSION gustation) present extensive differential action, and release of VSC and The new definition places less importance diagnoses. other volatiles, thereby enhancing on organoleptic examination and single

occasion halitometric reading, and instead Table 3 Variation in the ‘halitosis threshold’ reported in the literature places more emphasis on the declarations of the patient and his/her social environment. Halitosis threshold (VSC ppb) *organoleptic score Reference The reasoning for this follows. 75 156 Organoleptic examination 100 (2*) 7, 31, 157, 158 Organoleptic measurement is carried out by 110 12 smelling the patient’s breath then scoring 125 40 the level of halitosis.7 However, the examiner does not smell a pure sample of mouth 150 14, 35, 94, 159 air, but rather a mixture of mouth air and 250 (3*) 81, 160, 161 alveolar air. The organoleptic examination does not distinguish between these, only Total: VSC 250 81 H S, CH SH, (CH ) S: 150, 50, 20 respectively (3*) subjectively assesses the overall odour level. 2 3 3 2 The perception of odorants depends upon several factors, including constant detection (1‑10 ppb). Nevertheless, routine In order to investigate the Halimeter’s fluctuations in the clinician’s individual application of these clinically is impractical ability to distinguish between VSC and threshold level for that specific odour, what given the expense and complexity, and the other gases, having calibrated the Halimeter was last smelled before the examination, the expertise required.94 More practical methods to ambient air, the aspirating tube was concentration and volatility of the molecules utilise colorimetric hydrogen sulphide inserted into the headspace of some 250 ml themselves, room temperature (gases are less sensors engineered both as an optical commercial juice cartons immediately after volatile in lower temperatures), humidity of fibre, capable of measuring reflectance opening. The Halimeter readings for apricot, exhaled breath, how strongly the breath change of an immobilized reagent,137 and apple, peach, cherry juices, buttermilk, is blown into the examiner’s nose (less as thin reactive films of chromophores.138 soda, were 114, 352, 91, 48, 39, 47 ppb VSC forcefully expired breath will consist of less A bio-electronic nose capable of detecting respectively. In a similar experiment, the volume of air, and less odorant molecules the oxygen consumption induced by an Halimeter reported VSC as if H2S is emitted will be carried to the examiner’s olfactory enzymatic reaction with methyl sulphide from various flowers: daffodil, rose, jasmine epithelia), and lastly the examiner’s has also been developed.139 The Halimeter140 were 255, 42, 73 ppb while 104 ppb was concentration at that moment. All these contains an electrochemical sensor for VSC. read near a sump, and 417 ppb near hand parameters vary from one hour to the The semiconductor gas sensors Breathtron,141 soap. When using another gas detector in next and from one individual to the next, constructed as a zinc oxide film with specificity the same conditions, all these flowers read making this a subjective measure that does to hydrogen sulphide and mercaptans.142 with different percentages of VOC, not not reflect the actual level of odour. It can The GC‑based OralChroma,143 is portable VSC.153 Such simple experiments show that be suggested that self-applied organoleptic equipment capable of determining combined the Halimeter seems to confuse VSC with scoring (self-assessment) should be evaluated H2S, MM and DMS levels, with a 10 min other odorants, and may not be selective to monitorise prognosis. response time and a detection limit of a few enough for halitosis. The OralChroma gives Organoleptic examination is problematic,132 ppb. Twin Breasor,144 Diamond Probe/Perio more comprehensive VSC level readings and objectionable to both dentists and to 2000,145 Cyranose 320,146 and B/B Checker,147 than the Halimeter,41 but it shares the VSC patients. Dislike or shame is experienced are portable devices for detecting several exclusivity limitation and therefore cannot by 50% of patients with this examination gases including VSC and other odorous gases fully determine the actual level of breath (n = 283).133 Some use a privacy screen to in mouth or breath air.148,149 Their accuracy is odour due to potential minor contributions prevent the patient from seeing the examiner poor compared to GC and MS. They cannot from non-VSC gases. during the examination.7 Examiners find it distinguish one odour from another, and New gas detectors capable of detecting repulsive to smell a halitosis patient’s breath. they have difficulty distinguishing individual sulphur and nitrogen containing gases, as Self-detection of halitosis correlated compounds from the family of VSC.132 well as VOCs should be developed for use positively with actual halitosis only when Almost all halitosis researchers and in halitosis detection. There are industrial, subjects smelt their own saliva isolated specialists use portable sulphide monitors portable gas detectors that are capable of from their mouth. Other methods did not (for example, Halimeter) to detect oral detect more than four gas groups including 134 14 correlate. Another study reported less VSC. Good correlation exists between VSC, NH3, or VOC that could potentially be correlation between self-detection of halitosis Halimeter readings and VSC concentration,35 utilised at one reading. A sensor system for 150 and clinical findings. The sensitivity and and sulphur-producing bacteria levels. monitoring the simple gases H2, CO, H2S, 154 specificity of self-perceived oral malodour However, Halimeter readings are imprecise NH3, VOC and ethanol, and breath test were 47.2% and 59.2%, respectively.135 The and misdiagnosis may result.151 The kits including instruments to detect breath 155 same author later compared 252 halitosis Halimeter has biexponential response to a H2 and methane are available. patients’ self-estimation, organoleptic and constant concentration of VSC. Rapid (peak) halitometric results and found that self- and slow (plateau) responses differed. The Perturbation on threshold estimated corresponded significantly with total VSC in air samples was 2.7 times of halitosis clinical oral malodour.136 greater than at its peak concentration, but its There is no consensus regarding what VSC plateau phase measurement is 25% greater reading corresponds to clinically present Halitometers than the actual concentration. A modified halitosis (Table 3). Gas chromatography (GC), alone or combined protocol measuring plateau instead of peak Besides these data, some describe ranges with mass spectrometry (MS), is most values is available, yielding more favorable of VSC readings, eg: 0‑40, healthy; 41‑60, frequently utilised for highly sensitive VSC correlation with the actual level of VSC.152 physiologic; 61‑80, slight; 81‑110, moderate;

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