See

discussions, stats, and author profiles for this publication at: https://www.researchgate.net/publication/227857137

Halitosis: The multidisciplinary approach

Article in International Journal of Oral Science · June 2012

DOI: 10.1038/ijos.2012.39 · Source: PubMed

CITATIONS READS

51 146

2 authors, including:

Curd Bollen
Mondcentrum dr. Bollen
38 PUBLICATIONS 3,074 CITATIONS

SEE PROFILE

Some of the authors of this publication are also working on these related projects:

HPV in dentistry View project

Zirconia implants View project

All content following this page was uploaded by Curd Bollen on 19 July 2015.

The user has requested enhancement of the downloaded file. All in-text references underlined in blue are added to the original document
and are linked to publications on ResearchGate, letting you access and read them immediately.
 International Journal of Oral Science (2012) 4, 55–63
ß 2012 WCSS. All rights reserved 1674-2818/12
www.nature.com/ijos

REVIEW

Halitosis: the multidisciplinary approach

Curd ML Bollen and Thomas Beikler

Halitosis, bad breath or oral malodour are all synonyms for the same pathology. Halitosis has a large social and economic impact. For the
majority of patients suffering from bad breath, it causes embarrassment and affects their social communication and life. Moreover,
halitosis can be indicative of underlying diseases. Only a limited number of scientific publications were presented in this field until
1995. Ever since, a large amount of research is published, often with lack of evidence. In general, intraoral conditions, like insufficient
dental hygiene, periodontitis or tongue coating are considered to be the most important cause (85%) for halitosis. Therefore, dentists
and periodontologists are the first-line professionals to be confronted with this problem. They should be well aware of the origin, the
detection and especially of the treatment of this pathology. In addition, ear–nose–throat-associated (10%) or gastrointestinal/
endocrinological (5%) disorders may contribute to the problem. In the case of halitophobia, psychiatrical or psychological problems
may be present. Bad breath needs a multidisciplinary team approach: dentists, periodontologists, specialists in family medicine, ear–
nose–throat surgeons, internal medicine and psychiatry need to be updated in this field, which still is surrounded by a large taboo.
Multidisciplinary bad breath clinics offer the best environment to examine and treat this pathology that affects around 25% of the whole
population. This article describes the origin, detection and treatment of halitosis, regarded from the different etiological origins.
International Journal of Oral Science (2012) 4, 55–63; doi:10.1038/ijos.2012.39; published online 22 June 2012

Keywords: halitosis; microbiology; periodontology

EPIDEMIOLOGY the incidence seemed to be around 28%.9 Bornstein et al.10 found

The amount of epidemiological research on bad breath is limited, nearly the same incidence in Swiss city of Bern. These results suggest
since this topic is still a large but underestimated taboo. A public that this oral malodour is caused by tongue coating in the younger gene-
investigation in 2005 in The Netherlands showed that halitosis was ration and by periodontitis with tongue coating in the older cohorts.
one of the 100 biggest human overall exasperations (TNS-NIPO). This large variety of data suggest that there are large shortcomings
There are several reasons for this lack of scientific data. First, there is in the methodology of the overall research projects.11 A standardized
the difference in cultural and racial appreciation of odours, as for evaluation protocol for halitosis studies is needed to compare epide-
patients as well as for investigators.1 Second, there is absence of uni- miological data. Therefore, a mechanical detection method should be
formity in evaluation methods, as for organoleptical as for mechanical used as golden standard for bad breath research.
measurements.
A cross-sectional Brazilian study among university students and ORIGIN
their families, showed a malodour incidence of 15%. Men suffered Microbial degradation in the oral cavity is the main cause of oral
more from the problem than women, especially when they were over malodour. Due to this process, volatile sulphur compounds (VSCs)
20 years.2 Japanese researchers investigated 33 000 adults. Fifteen per are formed. The most important VSCs involved in halitosis are
cent of them declared to suffer from bad breath, with a peak of more hydrogen sulphide (H2S), methyl mercaptan (CH3SH) and dimethyl
than 20% in the city of Tokyo.3 Moreover, 70% of the businessmen in sulphide (CH3)2S. These VSCs are mainly produced by Gram-negative
Tokyo detected regularly a personal halitosis. In China, more than anaerobic oral bacteria.12 Other molecules involved in this bacterial
25% of a population of 2 000 individuals seems to be suffering from degradation process are: diamines (indole and skatole) or polyamines
halitosis.4 Al-Ansari et al.5 showed also in 2006 the same incidence in a (cadverin and putrescin). They seem play a less important role in the
Kuwaiti population of 1 500 people. In general, nearly of 25% of the expression of bad breath.
population seems to suffer from bad breath on a regular basis. Most of these components are produced in the proteolytic degra-
Man and women seem to suffer in the same proportions, whereas dation process of peptides. The most predominant substrates in this
women seem to seek faster for professional help than men.6 Miyazaki VSC production are cysteine, cystine and methionine.13 The main
found that there is a clear correlation between age and oral malodour: substrate for skatole and indole production is tryptophan, whereas
the older one gets, the more intense the odour will become.7 In the lysine and ornithine are the basis for the putrescin/cadaverin produc-
United States, Loesche et al.8 found that 43% of people over 60 had tion. The involved bacteria in these metabolic processes are shown in
breath problems. Whereas in the same Group of Turkish individuals, Table 1.
Poliklinik für Zahnerhaltung, Parodontologie und Endodontologie, Westdeutsche Kieferklinik, Universitätsklinikum, Düsseldorf, Germany
Correspondence: Dr CML Bollen, Poliklinik für Zahnerhaltung, Parodontologie und Endodontologie, Department of Periodontology, Moorenstrabe 5, Düsseldorf 40225, Germany
E-mail: curd.bollen@med.uni-duesseldorf.de
Received 12 September 2011; accepted 16 March 2012
 Halitosis: the multidisciplinary approach
CML Bollen and T Beikler
56

Table 1 Bacteria responsible for VSC production Oral pathology, microbiology and xerostomia
Volatile sulphur compounds Bacteria In nearly 85% of all halitosis cases, the origin is found in the oral cavity.
A clinical evaluation of malodour on 2 000 patients in Belgium,
H2S from cysteine Peptosteptococcus anaerobius
showed that 76% of these patients had oral causes: tongue coating
Micros prevotii
Eubacterium limosum
(43%), gingivitis/periodontitis (11%) or a combination of the two
Bacteroides spp. (18%).18
Centipedia periodontii
H2S from serum Prevotella intermedia Tongue coating. This phenomenon is the most common cause of bad
Prevotella loescheii breath.19 The dorsum of the tongue, which is irregular and has a
Porphyromonas gingivalis (BANA positive) surface of 25 cm2 is an ideal niche for oral bacteria.20 Since desqua-
Treponema denticola (BANA positive)
mating epithelial cells and food remnants are available, putrefaction
Selenomonas artermidis
CH3SH from methionine Fusobacterium nucleatum
occurs. Hence, the tongue surface seems to be an important reservoir
Fusobacterium periodonticum in the recolonisation of tooth surfaces.21 Tongue coating is not easy to
Eubacterium spp. remove. Daily scraping or brushing of the tongue can help to reduce
Bacteroides spp. the substrata for putrefaction, rather than to reduce the bacterial load.
CH3SH from serum Treponema denticola (BANA positive) Moreover, tongue cleaning improves taste sensation.22
Porphyromonas gingivalis (BANA positive)
Porphyromonas endodontalis
Other Prevotella melaninogenica Morning breath. Due to the reduced saliva production during night,
Tanerella forsythensis anaerobic putrefaction will increase, causing the typical morning
Eikenella corrodens breath. This is a non-pathological form of halitosis. The problem will
Solobacterium moorei disappear as soon as oral hygiene measures are taken. Snel et al.23
Treponema forsythensis concluded that gender seems to play an unknown role in this
Centipeda periodontii phenomenon: women manifest higher VSC levels than men in the
Atopobium parvulum
morning. This phenomenon needs to be further investigated to
Adapted from Persson et al.120 understand its impact.

Odontogenic halitosis. Poor oral hygiene, dental plaque, dental caries,

Most of the responsible microorganisms in halitosis are involved in accumulation and putrefaction of food remnants and unclean acrylic
periodontitis. So, there is a positive correlation between bad breath dentures (worn at night or not regularly cleaned or with rough
and periodontitis: the depth of the periodontal pockets is positively surfaces) contribute to bad breath. The latter was recently concluded
correlated to the height of the VSC concentrations in the mouth.14 in a systematic review, stating that, although isolated reports, chemi-
When tongue coating is taken into account, the correlation is even cals and brushing appear to be more effective than placebo in the
more significant.15–16 Individuals with a healthy periodontium can reduction of plaque coverage and microbial counts of anaerobes and
show halitosis caused by the impaction of food, bacteria, leucocytes aerobes on complete denture bases.24
and desquamating epithelial cells on the dorsum of their tongue. This Gingivitis and periodontitis are the main causes of the problem.25 A
surface is large and has a high retention capacity due to the rough and positive correlation between the depth of the pockets and the concen-
papillary structure. The bacterial composition on the dorsum of the tration of the sulphur components has been shown.15 Necrotizing
tongue seems to be identical to the subgingival plaque.17 Table 2 shows gingivitis or periodontitis cause extreme soiled odours. This disease
the main volatile molecules contributing to oral malodour. is caused by opportunistic bacterial infections occurring in individuals
with stress, malnutrition, insufficient oral hygiene, smoking or sys-
temic diseases.26
Table 2 Volatile molecules contributing to oral malodour
Categories Compounds Xerostomia. Patients with a dry mouth (0.15 mL?min21 instead of
Volatile sulphur compounds Methyl mercaptan: CH3SH 0.25–0.50 mL?min21) often show an increased volume of plaque on
Hydrogen sulphide: H2S teeth and tongue.27 The lack of salivary flow, leads to the disappearance
Dimethyl sulphide: (CH3)2S of the antimicrobial activity of the saliva and the transition from
Diamines Putrescine: NH2(CH2)4NH2 Gram-positive bacteria to Gram-negative species.28 Hyposialy can
Cadaverine: NH2(CH2)5NH2 be caused by diabetes, Sjögren syndrome, stress, depression, medica-
Butyric acid: CH3CH2CH2COOH
tion, mouth breathing and alcohol abuse. Almost 25% of the
Propionic acid: CH3CH2COOH
elderly suffer from a dry mouth.29 Research groups of Kleinberg and
Valeric acid: C5H10O2
Phenyl compounds Indole: C8H7N Koshimune described properly the correlation between the dry mouth
Skatole: C9H9N and the increase of halitosis.30–31
Pyridine: C5H5N Moreover, other salivary factors can influence the development of
Alcohols 1-propoxy-2-propanol malodour: an increase of the salivary pH by the intake of amino acids,
Alkalines 2-methy-propane and a change in the oxygen depletion (a reduction stimulates the
Nitrogen-containing compounds Urea: (NH2)2CO metabolism of Gram-negative bacteria, responsible for higher VSC
Ammonia: NH3
production).32–33
Ketones
A recent study in elderly found the accumulation of bacterial
Adapted from Goldberg et al.,13 Greenman et al.17 and Claus et al.121 plaque on the tongue, oral dryness, burning mouth, overnight denture

International Journal of Oral Science

 Halitosis: the multidisciplinary approach
CML Bollen and T Beikler
57

wear, and lower educational levels to be significantly related to oral images, fading is perceived. When purulent mucous is produced, a
malodour.34 typical odour appears. In 10% of the sinusitis cases, a tooth or several
Although xerostomia is associated with aging, studies have demon- teeth are involved. In these cases, the spotted bacteria are: Peptostre-
strated that salivary gland function is well preserved in the healthy tococcus spp., Fusobacterium spp., Prevotella spp. and Porphyromonas
geriatric population. Therefore, dry mouth is probably a condition of spp. Since those bacteria are able to produce VSCs, a clear association
systemic or extrinsic origin. Saliva seems to undergo chemical changes to halitosis is available. The treatment of dentogenic problems (even-
with aging. As the amount of ptyalin decreases and mucin increases, tual with the additional use of antibiotics) decreases the anaerobic
saliva becomes thick and viscous and presents problems for the elderly. pathogens, even as the odour problem. In the case of chronic sinusitis,
One of the most prevalent causes of xerostomia is medication (anti- 50%–70% of the patients complain about oral malodour.46
cholinergics, antihistamines and diuretics dry the mucosa). Chronic
mouth breathing, radiation therapy, dehydration and autoimmune Pulmonary pathology. bronchiectasis, lung abscesses and other endo-
diseases (as Sjögren’s) can also diminish salivation, as can systemic brochial chronic disorders, i.e. necrotizing pulmonic neoplasias may
illness such as diabetes mellitus, nephritis and thyroid dysfunction. cause an unpleasant odour.47
Xerostomia can lead to dysgeusia, glossodynia, sialadenitis, crack-
ing and fissuring of the oral mucosa, and halitosis. Dry mouth
Gastro-intestinal pathology
symptom can be treated with hydration and sialagogues or with arti-
The gastro-intestinal tract can only indirectly (haematogenic) influ-
ficial saliva substitutes. In patients with Sjögren’s syndrome and in
ence bad breath. A majority of patients and physicians still abusively
those who have undergone radiation therapy, pilocarpine has been
believes that halitosis originates from the stomach. The latter is only
used with good results.35
correct in ,0.5% of the cases.
Other oral causes. Stomatitis, intra-oral neoplasia, exposed tooth
pulps (with necrotic content), extraction wounds (with blood cloth Oesophagus. Only in specific cases, this is the origin of malodour.
or purulent discharges), or crowding of teeth (favouring food entrap- When a Zenker’s diverticulum is present, a chronic unpleasant odour
ment) can also be involved.36 Moreover, peri-implantitis, peri-coronitis, appears.48 The incidence of this phenomenon is less than 0.1% and it is
recurrent oral ulcerations and herpetic gingivitis, are described as only diagnosed in patients over 65 years of age. Also bleeding of the
origin for bad breath.37 oesophagus can cause a musty odour. When severe regurgitation is
determined, halitosis will be present.49 Symptomatically, coughing,
postnasal drip, pyrosis, irritations and ulcerations of the oesophagus
ENT and pulmonary pathology
and halitosis will be detected. pH monitoring is used for diagnosis.
Maximally 10% of the oral malodour cases originate from the ears,
When the diagnosis is missed, carcinomatic deterioration can occur.
nose and throat (ENT) region, from which 3% finds its origin at the
tonsils.38 Very seldom the larynx is involved. Therefore, when a clinical
investigation is performed, attention should first be paid to the tonsils: Stomach. Infections with Helicobacter pylori can cause peptic ulcers.
size, structure (invaginations, coating and hyperaemia) and presence There is no 100% clear correlation found between these ulcers and
of tonsilloliths.39 halitosis.50–51 In vitro studies show significant VSC production by H.
pylori.52 More recent research by Lee et al.53 confirmed this statement.
Oral causes. Acute tonsillitis is the most important ENT origin. Moreover, it is suggested that H. pylori was detected in subjects with
Mostly, infections with streptococci play a role, but also viral infections periodontitis, suggesting that progression of periodontal pocket and
(e.g. mononucleosis infectiosa) are possible. When acute tonsillitis inflammation may favour colonization by this species and that
takes place more than three times a year, a tonsillectomy can be con- H. pylori infection may be indirectly associated with oral patho-
sidered.40 A Plaut-Vincent angina (caused by Fusobacterium Plaut- logical halitosis following periodontitis.54 Kinberg et al.55 showed
Vincenti and Borrelia Vincenti) is another ENT cause for halitosis.41 that halitosis has often been reported among the symptoms related
The presence of tonsilloliths represents a 10-fold increased risk of to H. pylori infection and gastroesophageal reflux disease. When
abnormal VSC levels.42 Anaerobic bacteria detected in tonsilloliths gastrointestinal pathology was treated, most of the halitosis com-
belonged to the species of Eubacterium, Fusobacterium, Porphyromonas, plaints disappeared. The latter suggests that halitosis can have a
Prevotella, Selenomonas and Tanerella, all of which appear to be gastro-intestinal origin. In a recent comparative study among children
associated with the production of VSCs.43 Tonsilliliths are asympto- in Turkey, it was concluded that there was a difference between the
matic phenomena and are therefore never a reason for tonsillectomy. rate of H. pylori infections among those with and without halitosis.
A tonsillectomy is only performed when oral hygiene measures do Eradication treatment was found beneficial in the treatment of
not result in improvement of the breath. children with halitosis and positive H. pylori stool antigen test. The
results, however, were not statistical significant.56
Nasal causes. Postnasal drip (caused by mucus of the paranasal In general, it can be concluded that more research has to be done
sinuses) contacting the dorsum of the tongue is largely involved.44 to clarify a clear correlation between stomach problems by H. pylori
Foreign bodies in the nasal cavity can produce a foul odour as well. infections and halitosis.
Also a cleft palate can be the origin of bad breath.45 Atrophic rhinitis
with bacterial surinfection causes malodour too. This can be caused by Intestines. In cases of intestinal obstruction, a faecal mouth odour may
tumor rescetions, radiotherapy or overuse of decongestives or cocaine. be detectable, as found in two siblings with extrinsic duodenal obstruc-
tion caused by congenital peritoneal bands.57 Attention was drawn to
Sinusitis. Bacterial sinusitis develops mostly out of acute viral sinu- the unusual physical sign of halitosis as a presenting feature. It was
sitis. Streptococcus pneumonia and Haemophilus influenza are the main suggested that this physical sign may be an indication for barium
responsible bacteria. On radiological or computed tomography (CT) studies.

International Journal of Oral Science

 Halitosis: the multidisciplinary approach
CML Bollen and T Beikler
58

Metabolic disorders Table 3 Odours in the case of metabolic or endocrinological problems

Preti et al.58 discussed already in 1992 a number of non-oral causes Odours Metabolic or endocrinological problems
for oral malodour. Several well-documented aetiologies for non-oral
Fruity odour Type-1-diabetes in children
malodour include renal failure, cirrhosis of the liver and diabetes
Type-2-diabetes in adults
mellitus. In addition, there appeared to be several other metabolic
Alcoholic ketoacidosis
conditions involving enzymatic and transport anomalies (such as tri- Faecal odour Intestinal obstruction
methylaminuria) which lead to the systemic production of volatile Ammonia of fishy odour Kidney-insufficiency
malodours that manifest themselves as halitosis and/or altered che- Trimethylaminuria
moreception. Mouse odour Phenylketonuria
Renal disease in the form of chronic renal failure is associated with Cooked cabbage odour Methionine adenosyl transferase deficiency
high blood urea nitrogen levels and low salivary flow rates. Peritoneal Sweating feet odour Isovaleriaan acidity
Deficiency on chromosome 15
dialysis decreased the problem.59 The dispersed odour is a typical
Burned sugar odour Maple syrup urine disease
uremic odour in combination with a dry mouth. Also pancreatic
Sweet musty odour Homocystinuria
insufficiencies can cause oral bad odours as found by Feller and Rotten eggs odour Disease of Lignac
Blignaut in 2005.60
Diabetic ketoacidosis leads to a typical breath odour.61 Diabetes Adapted from van Steenberge.62
type 2 demonstrates a typical sweet and fruity odour.62 Due to gas
chromatography–mass spectrometry, it seems possible to detect dif- Medication
ferent extra-oral causes of halitosis such as diabetes.63 Next to medication resulting in a dry mouth (see above); recently the
Several metabolic disorders in the bowels, like trimethylaminuria use of bisphosphonates can contribute to oral malodour. Bisphospho-
cause a specific fishy odour. According to Whittle et al.,64 this genetic nate-induced osteonecrosis is since 2003 a common problem.71 The
disease is the largest cause of undiagnosed body odour. Trimethyl- product is used systemically in cases of malignant bone tumours and
aminuria is a disorder in which the volatile, fish-smelling compound, their metastases. Often this results in jawbone necrosis, a clear origin
trimethylamine accumulates and is excreted in the urine, but it is also for a filthy odour. The necrotic sequesters should be removed and it is
found in the sweat and breath. Because many patients have associated tried to cover up the necrotic area with a steeled flap.72
body odours or halitosis, trimethylaminuria sufferers can meet serious
difficulties in their social context, leading to isolation and even depres- DETECTION
sion. Trimethylamine is formed by bacteria in the mammalian gut The gold standard is the organoleptic scoring, i.e., smelling the odour
from reduction of compounds such as trimethylamine-N-oxide and of the patient. A more objective method is the analysis of breath
choline. Primary trimethylaminuria sufferers have an inherited samples by gas chromatography or by means of portable VSC
enzyme deficiency where trimethylamine is not efficiently converted analysers.
to the non-odorous trimethylamine-N-oxide in the liver. Diagnosis
of trimethylaminuria requires the measurement of trimethylamine
Organoleptic scoring
and trimethylamine-N-oxide in urine, which should be collected
In expired air, more than 150 different components have been
after a high substrate meal in milder or intermittent cases, a marine-
detected. The perception of these molecules is dependent of the olfac-
fish meal. The symptoms of trimethylaminuria can be improved by
tory response, the threshold concentration, the strength of the odour
changes in the diet to avoid precursors, in particular trimethylamine-
and the volatility of the molecules. When organoleptical scoring is
N-oxide which is found in high concentrations in marine fish.
performed, a well-trained clinician determines if the odour samples
Treatment with antibiotics to control bacteria in the gut, or activated
smells bad or not, giving a score to the intensity. Theses scores go from
charcoal to sequester trimethylamine, may also be beneficial.65
0 up to 5 (Table 4).
Recently, an article by Scully and Greenman66 reviewed the
From every patient, different samples are analysed:
aetiopathogenesis of halitosis. They stated that only in a few
patients, metabolic anomalies are responsible. If this condition is pre- . mouth odour (smelled at 10 cm form the oral cavity: while the
sent, the extra-oral origin should be determined, because the latter patient normally breaths and while the patient counts loudly to
requires medical investigation and support in therapy. 10);
. saliva odour (measured by the wrist-lick test: the patient licks at
Hepathology and endocrinology the wrist, and after 10 s of drying, a score is given to this sample);
The liver can be involved in oral malodour. Due to a reduced liver . tongue coating (a score is given to debris, scraped from the dorsum
function, waste products are eliminated through the lungs, causing the of the tongue with a periodontal probe);
‘fetor hepticus’: a sweet, excremental odour (the breath of death).
Fetor hepaticus is an expression of hepatic encephalopathy.67 Liver
Table 4 Organoleptical scoring scale
failure inhibits the detoxification in the whole body, causing unplea-
sant odours.68 Also some hereditary disorders can influence the Rosenberg & McCulloch scale Description
breath: tyrosinemy is the most important example (cabbage odour). 0 No detectable odour
Endocrinology can also contribute to halitosis. Not only the hor- 1 Hardly detectable odour
monal cycle seems to influence the mouth odour, but also a lot of other 2 Light odour
intestinal diseases.69–70 3 Moderate odour
4 Strong odour
Recently, van Steenberghe mentioned a whole list of metabolic and
5 Extremely strong odour
endocrinological aspects in correlation to oral malodour.62 This list is
resumed in Table 3. Adapted from Rosenberg and McCulloch.75

International Journal of Oral Science

 Halitosis: the multidisciplinary approach
CML Bollen and T Beikler
59

. interdental ‘floss’ (after flossing with dental tape, the odour of the differential diagnosis of halitosis, with the possibility to detect extra-
floss is scored); oral causes, which often remain undetected unless characterized by a
. nasal odour (while the patient is breathing through the nose specific smell.
(mouth closed), a score is given to the exhaled air);
. prosthesis odour (if the patient wears a partial or full removable
THERAPY
denture, scoring of the odour of this prosthetic is noted).
Oral causes
Since the oral causes are related to microorganisms, the therapy can
To gather optimal test results several precautions should be taken
consist of: (i) mechanical reduction of the intra-oral nutrients and
before the examinations: the patient should refrain from spicy foods,
micro-organisms; (ii) chemical reduction of microorganisms; (iii)
garlic or onions the day before the examination. At least 12 h before the
inverting volatile fragrant gasses into non-volatile components or
consultation, teeth should not be cleaned or rinsed, perfumes should
(iv) masking of the malodour.80
be avoided and at least 6 h before the examination, the intake of food
or liquids should be avoided. Smoking should be stopped at least 24 h
before any examination.73 Mechanical reduction. Tongue coating is the most prominent factor
The advantages of organoleptical scoring are: inexpensive, no and therefore, extensive tongue cleaning is of utmost importance. The
equipment needed and a wide range of odours is detectable. As dis- scraping of the dorsum of the tongue reduces the available nutrients
advantages, the extreme subjectivity of the test, the lack of quantifi- even as the available microorganisms, leading to an improvement of
cation, the saturation of the nose and the reproducibility can be the odour.81 Home tongue cleaning can be performed with a regular
mentioned.74 Still, organoleptic scoring is considered as the gold toothbrush, but a specific tongue scraper is advised. A brush is less
standard in the detection of oral bad breath. aggressive on the soft tissues.82 Since the largest amount of coating is
found on the dorsal part of the tongue surface, a cleaning as posterior
Portable gas analysis as possible is advised. To prevent from vomiting, it is counselled to
The Halimeter (Interscan corporation, Chatsworth, CA, USA) and pull out the tongue when scraping.
OralChroma (Abimedical corporation, Miyamae-ku Kawasaki-shi, A systemic review by van der Sleen et al.83 demonstrated that tongue
Kanagawa, Japan) are electronic devices available to detect some of brushing or tongue scraping have the potential to successfully reduce
the volatile sulphur components in expired air. The OralChroma is a breath odour and tongue coating. Due to tongue cleaning, the taste
portable gas chromatograph offering lower cost, higher performance seems to improve again.84 Interdental cleaning and toothbrushing are
and more user-friendly operations than conventional gas chromato- also necessary to control plaque and oral microorganisms.
graphs by limiting the target gases to three types: H2S, CH3SH and A Cochrane review from 2006, compared randomized controlled
(CH3)2S. Also, an interpretation of the results can be shown to the trials for different methods of tongue cleaning to reduce mouth odour
patients. in adults with halitosis.85 Only two trials were included, involving 40
The Halimeter can only give an idea of the total amount of VSCs, participants. Due to the clinical heterogeneity between these two
present in a sample. In the Halimeter, the total amount ppb (parts studies, only a descriptive summary could be made. It is concluded
per billion) of VSCs in the sample is marked. In normal situations that there is a weak and unreliable evidence to show that there is a
this value is less than 100 ppb. When 300–400 ppb are detected in the small but statistically significant difference in reduction of VSC levels
mouth air, a persistent oral odour can be concluded.15,75 when scrapers or cleaners rather than toothbrushes are used to reduce
These portable machines have a lot of advantages: easy to handle, halitosis in adults. More coherent studies are required to come to
fast results, portable and reproducible. Furthermore, they are rather clear conclusions.
inexpensive and can be controlled by untrained staff. As disadvantage, Since periodontitis is one of the main causes of oral malodour, a
the limited diversity in the explored gasses should be stated. Recently, professional periodontal therapy should be performed. A one-stage
it was shown that the OralChroma may produce a more comprehen- full-mouth disinfection, as described by Bollen et al.,86 combining
sive assessment of VSC production by oral microflora than the scaling and rootplaning in combination with chlorhexidine, has a
Halimeter.76 It would desirable to select one machine as gold standard significant microbiological improvement up to 2 months and reduces
to make different studies comparable in the future. the organoleptical scores, in particular for saliva samples, who seems
to be representative for organoleptical scoring.87
Gas chromatography When patients’ response to treatments at a multidisciplinary breath
In halitosis research, the gas chromatography (GC) analysis can be odour clinic was considered, it was concluded that education of the
performed on breath, saliva and tongue debris. Almost all different air public and dental professionals in a more consequent general oral
components can be detected. In expired air, almost 500 different sub- hygiene might elevate the level of compliance and could cause thereby
stances can be demonstrated.77 GC in malodour research is still in an an amelioration of the problem.88
experimental stage, although used since the late 1960s.78 VSCs can be
well detected, but the challenge will be to analyse the other contribu- Chemical reduction. Rinsing is a common practice in the approach of
ting components of oral malodour. Also the associations of different oral malodour. The most used rinsing components are:
odours with specific systemic disease can and should be investigated.
GC has several advantages: an analysis of almost all components . chlorhexidine (CHX): CHX is the most efficient molecule against
with high sensitivity and specificity. The method is non-invasive, but plaque. Rosenberg showed that rinsing with 0.2% CHX causes a
expensive and a well-trained staff is needed. The progression of the reduction of 43% in VSCs and of 50% in the organoleptical scores
method takes much more time and the machine cannot be used in on a day-long basis.89
daily practice.79 . essential oils: these products give only a short-term and restricted
Recently, trailblazing research was performed by van den Velde effect (25% reduction) for 3 h. Also, the reduction in odour-
et al.63,68 with gas chromatography–mass spectrometry as a tool for producing bacteria is limited.90

International Journal of Oral Science

 Halitosis: the multidisciplinary approach
CML Bollen and T Beikler
60

. chlordioxide: chlordioxide is a strong oxidizing product that can The treatment of chronic sinusitis is depending on the underlying
reduce oral malodour by the oxidation of H2S, CH3SH, cysteine cause. The problem will be treated by medications containing vaso-
and methionine. A reduction of 29% in odour after 4 h was constrictors associated or not with H1 antihistaminic, rinsing of the
reported.91 sinuses or even surgical removal of the inflamed mucosa and polyps.102
. triclosan: triclosan is effective against the majority of oral bacteria. In the case of chronic tonsillitis, the elimination of the deep crypts,
An 84% reduction of VSCs after 3 h is proved.92 which harbour exfoliated cells, debris and bacteria, is important.
. aminefluoride/tinfluoride: the combination of AmF/SnF2 can Prescribing antibiotics like metronidazole has only a short-term
cause an 83% reduction in the morning halitosis.84 effect. Cryptolysis by means of CO2 laser is another option.103 Ozena
. H2O2: a concentration of 3% of this product can result in a 90% seems to respond well to a prolonged treatment of fluoroquiolone,
VSC reduction after 8 h.93 which are highly effective against Gram-negative bacteria including
Heamophilus influenza. Prolonged treatment can produce however
some side effects as photosensibilisation or tendinitis.104
Toothpastes, containing stannous fluoride, zinc or triclosan, seem In the case of tonsilloliths, a proper hygiene can be instructed by
to have proved their beneficial effect in reducing the oral malodour squeezing out the debris out of the cryptic tonsils. This handling
for a limited period of time.94–96 requires exercising.
In a recent Cochrane review by Fedorowicz, only five randomized
controlled trials could be found, involving 293 participants.97 In view Gastro-intestinology
of the clinical heterogeneity between the trials, pooling of the results In the case of regurgitation esophagitis, the treatment mostly consist
and a meta-analysis of the extracted data was not feasible. Compared of weight reduction, prohibition of coffee and tobacco, avoidance of
to placebo, 0.05% chlorhexidine10.05% cetylpyridinium chloride1 extensive meals in the evening, placing the head of the bed in a slightly
0.14% zinc lactate mouthrinse significantly reduced the organoleptic higher position. H2 anatgonists can be prescribed.105 When H. pylori
scores, but showed significantly more tongue and tooth staining. It is infections are noticed, the therapy consists of the intake of omeprazol,
concluded that this mouthrinse plays an important role in reducing amoxicillin en clarithromycin.106
the levels of halitosis producing bacteria on the tongue and can be A Zenker diverticle must be surgically removed. For a stomach
effective in neutralization of odoriferous sulphur compounds. But hernia, generally a surgical intervention will be necessary.
well-designed, randomized controlled trials with larger sample size,
a longer intervention and follow-up period are still needed to confirm
Hepathology and endocrinology
these results.
In severe hepatologic problems, a liver transplantation can be neces-
sary. In less life-threatening situations, a liver dialysis can be sufficient
Transformation of volatile sulphur components. Metal ions with affi- to treat the problems. In more simple pathology, cortisone therapy
nity for sulphur, pick up sulphur-containing gasses. Zinc, mercury and a stringent diet can be enough.107
and copper are the most important metals.98 A commercial rinse In the endocrinological range of problems, the underlying diseases
(containing 0.005% CHX, 0.05% cetylpyridinium chloride (CPC) should be treated. The detailed approach of these therapies falls out-
and 0.14% zinc lactate) seems to be much more efficient than CHX side the scope of this article.
alone, due to the effect of zinc. Zinc plus CHX seem to have a syn-
ergistic effect as Young et al.99 proved. Probiotics
Recently several studies were performed to replace bacteria respon-
Masking effect. Rinsing products, sprays, mint tablets or chewing gum sible for halitosis with probiotics as Streptococcus salivarius (K12),
only have a short-term masking effect.100 Mostly, they increase the Lactobacillus salivarius or Weissella cibaria. The objective is to prevent
saliva production, thereby retaining more soluble sulphur compo- re-establishment of non-desirable bacteria and thereby limit the re-
nents for a short period of time.30 occurrence of oral malodour over a prolonged period. Several studies
conclude that probiotic bacterial strains, originally sourced from the
ENT and pulmonology indigenous oral microbiotas of healthy humans, may have potential
When problems in this area are considered, patients should be referred application as adjuncts for the prevention and treatment of hali-
to an ENT specialist or a pulmonologist. Acute pharyngitis can be tosis.108 The oral administration of the probiotic lactobacilli not only
treated symptomatically, when a viral infection is at stake. A salicylic seemed to improve the physiologic halitosis, but also showed bene-
intake seems efficient when started from the prodromal stage onwards. ficial effects on bleeding on probing from the periodontal pockets.109
Chlorhexidine sprays can prevent bacterial overgrowth and reduce the Moreover, Weisella cibaria isolates possess the ability to inhibit VSC
breath malodour. If pharyngitis is of bacterial origin, group A strep- production under both in vitro and in vivo conditions, demonstrating
tococci are mostly responsible. The infection can be confirmed by that they bear the potential for development into novel probiotics
bacterial culturing or by antigen tests. Treatment with penicillin is for use in the oral cavity.110 Gut-caused halitosis, although rarely
imperative to prevent rheumatic fever. The breath malodour will soon occurring, can be successfully treated with a suspension of living
disappear.101 Foreign objects in the nose should be removed. non-pathogenic Escherichia coli bacteria.111 Scully and Greenman66
Acute infective sinusitis can be treated by an appropriate antimi- showed that emergent halitosis treatments include probiotics and
crobial. Broad-spectrum penicillin or cephalosporin is the choice. vaccines targeted against causal microorganisms or their products.
Sometimes, a surgical widening of the ostia is needed, especially if
recurrences are observed. If the problem is of dental origin, this infec- PSYCHOLOGICAL ASPECTS
tion should be treated first. Periapical tooth infections, particularly In general, humans cannot detect their own bad breath. Therefore, it
of second molars are mostly responsible. Endodontic treatment or is unusual that patients can detect their halitosis, although there is
extraction of the tooth is the options. nothing wrong. This kind of patients often frequents a halitosis clinic.

International Journal of Oral Science

 Halitosis: the multidisciplinary approach
CML Bollen and T Beikler
61

Halitophobia be the sign of an underlying systemic disease. Therefore, it is substan-

This is the fear of having bad breath that other people find offensive. tiated to organize halitosis consultations in a multidisciplinary setting,
Moreover, 0.5%–1% of the adult population is affected with this assembling periodontologists, ENT specialists, specialists in internal
problem in their social live. These patients consider having bad breath, medicine and psychologists or even psychiatrists.
do not have it, but get not convinced during diagnosis and therapy. Although oral malodour is mostly associated with poor oral hygiene
Non-real halitosis or halitophobia is understood by the compulsive and the presence of gingivitis or even periodontitis, evidence suggests
idea to suffer from bad breath and to irritate others by this. that anaerobic microorganisms present in the tongue coating, are the
Nagel mentions that consultation hours for halitosis should be overwhelming cause of this condition. A limited number of successful
prepared for patients with non-real halitosis and build up correspond- treatment regimens have been described, but more research on the
ing interdisciplinary contacts.112 The ‘treatment’ of these patients is long-term outcomes of these therapies will be required. Also new and
impossible, since they are not into the arguments stated by a physician. more long lasting in-office treatments should be developed and tested.
Mostly, these patients hop from clinic/specialist to clinic/specialist to
find an argument for their self-esteemed problem. Imagined halitosis
is poorly documented in the psychiatric literature.113 Many of the
cases with imagined halitosis described in the literature resemble the 1 Rayman S, Almas K. Halitosis among racially diverse populations: an update. Int J
Dent Hyg 2008; 6(1): 2–7.
psychiatric syndrome of social phobia.114 2 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.
3 Saito H, Kawaguchi Y. Halitosis prevention campaign: a report of oral health promotion
Olfactory reference syndrome activities in Japan. Int Dent J 2002; 52(Suppl 3): 197–200.
Olfactory reference syndrome (ORS) is defined as the psychiatric con- 4 Liu XN, Shinada K, Chen XC et al. Oral malodour-related parameters in the Chinese
dition characterized by persistent preoccupation about body odour general population. J Clin Periodontol 2006; 33(1): 27–31.
5 Al-Ansari JM, Boodai H, Al-Sumait N et al. Factors associated with the self-reported
accompanied by shame, embarrassment, significant distress, avoid- halitosis in Kuwaiti patients. J Dent 2006; 34(7): 444–449.
ance behaviour and social isolation.115 ORS has, however, not been 6 Rosenberg M, Kulkarni GV, Bosy A et al. Reproducibility and sensitivity of oral
malodour measurements with a portable sulphide monitor. J Dent Res 1991;
included in the Diagnostic and Statistical Manual of Mental Disorders
70(11): 436–440.
and, given that it is primary symptoms may be found in various other 7 Miyazaki H, Sakao S, Katoh Y et al. Correlation between volatile sulphur compounds
disorders, differential diagnosis can be problematic. ORS seems to and certain oral health measurements in the general population. J Periodontol 1995;
66(8): 679–684.
represent a unique cluster of symptoms that can be delineated as a 8 Loesche WJ, Grossman N, Dominguez L et al. Oral malodour in the elderly. In: van
separate diagnostic entity, and ORS falls on a spectrum of social Steenberghe D, Rosenberg M, editors. Bad breath: A multi-disciplinary approach.
anxiety disorders that includes social anxiety disorder, taijin kyofusho Leuven: Leuven University Press, 1996: 181–194.
9 Avcu N, Ozbek M, Kutoglu D et al. Oral findings and health status among hospitalized
and body dysmorphic disorder.116 patients with physical disabilities, aged 60 or above. Arch Gerontol Geriatr 2005;
41(1): 69–79.
10 Bornstein MM, Kislig K, Hoti BB et al. Prevalence of halitosis in the population of the
Pseudo-halitosis city of Bern, Switzerland: a study comparing self-reported and clinical data. Eur J Oral
These are patients who consider to have bad breath, but who does Sci 2009; 117(3): 261–267.
not have it, and finally get convinced during diagnosis and therapy. 11 Vandekerckhove B, Bollen C. Epidemiology in the general population, specific
populations and in a multidisciplinary halitosis consultation. In: van Steenberghe
Seemann describes data collected from a multidisciplinary breath D, editor. Ademgeur. Houten: Prelum Uitgevers, 2009: 3–10.
consultation in Germany.73 According to this research, 28% of these 12 Krespi YP, Shrime MG, Kacker A. The relationship between oral malodour and volatile
sulphur compound producing bacteria. Otolaryngol Head Neck Surg 2006; 135(5):
patients complaining of bad breath did not show signs of bad breath— 671–676.
meaning that their concern of halitosis was exaggerated. Within this 13 Goldberg S, Kozlovsky A, Gordon D et al. Cadaverine as a putative component of oral
group, 76% received prior treatments for bad breath, 36% received malodour. J Dent Res 1994; 73(6): 116821172.
14 Calil C, Liberato FL, Pereira AC et al. The relationship between volatile sulphur
gastroscopies and 14% underwent an ENT operation—all without compounds, tongue coating and periodontal disease. Int J Dent Hyg 2009; 7(4):
having detectable signs of bad breath. Only 9% of these patients 251–255.
went through an organoleptic evaluation before they underwent these 15 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):
medical procedures. Patients with pseudo-halitosis show more often 233–238.
symptoms of depression.117 16 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.
Therapy 17 Greenman J, Duffield J, Spencer P et al. Study on the organoleptic intensity scale for
measuring oral malodour. J Dent Res 2004; 83(1): 81285.
Selective Serotonin Reuptake Inhibitor, which increases the concen- 18 Quirynen M, Dadamio J, van den Velde S et al. Characteristics of 2000 patients who
tration of serotonin in the brain, can help to treat this phenomenon.118 visited a halitosis clinic. J Clin Periodontol 2009; 36(11): 970–975.
When tricyclic antidepressant medication is used, xerostomia can 19 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.
appear, leading to an increase of halitosis awareness.119 Patients with 20 Collins LM, Dawes C. The surface area of the adult human mouth and thickness of the
symptoms of halitophobia or ORS, should not be treated by dental salivary film covering the teeth and oral mucosa. J Dent Res 1987; 66(8): 1300–
practitioners or by ENT specialists, but should be referred to psycho- 1302.
21 Faveri M, Feres M, Shibli JA et al. Microbiota of the dorsum of the tongue after plaque
logists or even to psychiatrists. accumulation: an experimental study in humans. J Periodontol 2006; 77(9): 1539–
1546.
22 Quirynen M, Avontroodt P, Soers C et al. Impact of tongue cleansers on microbial load
CONCLUDING REMARKS and taste. J Clin Periodontol 2004; 31(7): 506–510.
Halitosis is a common condition, affecting around 25% of the general 23 Snel J, Burgering M, Smit B et al. Volatile sulphur compounds in morning breath of
human volunteers. Arch Oral Biol 2011; 56(1): 29–34.
population. The origin of the problem largely arises from intra-oral 24 de Suza RF, de Freitas Oliveira Paranhos H, Lovato da Silva CH et al. Interventions for
causes, whereas only a limited number of cases are the result of extra cleaning dentures in adults. Cochrane Database Syst Re 2009; (4): CD007395.
oral or systemic problems. Nevertheless, proper investigation and 25 Morita M, Wang HL. Association between oral malodour and adult periodontitis: a
review. J Clin Periodontol 2001; 28(9): 813–819.
management of these extra oral causes is important for the total under- 26 Horning GM. Necrotizing gingivostomatitis: NUG to noma. Compend Contin Educ
standing of this phenomenon. Halitosis from an extra-oral origin can Dent 1996; 17(10): 951–958.

International Journal of Oral Science

 Halitosis: the multidisciplinary approach
CML Bollen and T Beikler
62

27 Albuquerque DF, de Souza Tolentino E, Amado FM et al. Evaluation of halitosis and 63 van den Velde S, Quirynen M, van Hee P et al. Halitosis associated volatiles in breath of
sialometry in patients submitted to head and neck radiotherapy. Med Oral Pathol Oral healthy subjects. J Chromatogr B Analyt Technol Biomed Life Sci 2007; 853(1/2):
Cir Bucal 2010; 15(6): e850–e854. 54–61.
28 Almståhl A, Wikström M. Oral microflora in subjects with reduced salivary secretion. 64 Whittle CL, Fakharzadeh S, Eades J et al. Human breath doors and their use in
J Dent Res 1999; 78(8): 1410–1416. diagnosis. Ann N Y Acad Sci 2007; 1098: 252–266.
29 Pajukoski H, Meurman JH, Halonen P et al. Prevalence of subjective dry mouth and 65 Mackay RJ, McEntyre CJ, Henderson C et al. Trimethylaminuria: causes and diagnosis
burning mouth in hospitalized elderly patients and outpatients in relation to saliva, of a socially distressing condition. Clin Biochem Rev 2011; 32(1): 33–43.
medication, and systemic diseases. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 66 Scully C, Greenman J. Halitology (breath odour: aetiopathogenesis and management).
2001; 92(6): 641–649. Oral Dis 2012; 18(4): 333–345.
30 Kleinberg I, Wolff MS, Codipilly DM. Role of saliva in oral dryness, oral feel and oral 67 Tangerman A, Meuwese-Arends MT, Jansen JB. Foetor hepaticus. Lancet 1994;
malodour. Int Dent J 2002; 52(Suppl 3): 236–240. 343(8912): 1569.
31 Koshimune S, Awano S, Gohara K et al. Low salivary flow and volatile sulphur 68 van den Velde S, Nevens F, van Hee P et al. GC-MS analysis of breath odor compounds
compounds in mouth air. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2003; in liver patients. J Chromatogr B Analyt Technol Biomed Life Sci 2008; 875(2): 344–
9(1): 38–41. 348.
32 Iwanicka-Grzegorek K, Lipkowska E, Kepa J et al. Comparison of ninhydrin method of 69 Kawamoto A, Sugano N, Motohashi M et al. Relationship between oral malodour and
detecting amine compounds with other methods of halitosis detection. Oral Dis 2005; the menstrual cycle. J Periodontal Res 2010; 45(5): 681–687.
11(Suppl 1): 37–39. 70 Calil CM, Lima PO, Bernardes CF et al. Influence of gender and menstrual cycle on
33 Traudt M, Kleinberg I. Stoichiometry of oxygen consumption and sugar, organic acid volatile sulphur compounds production. Arch Oral Biol 2008; 53(12): 1107–1112.
and amino acid utilization in salivary sediment and pure cultures of oral bacteria. Arch 71 Marx RE. Pamidronate (Aridea) and zoledronateinduced avascular necrosis of the
Oral Biol 1996; 41(10): 965–978. jaws: a growing epidemic. J Oral Maxillofac Surg 2003; 61(9): 1115–1118.
34 Nalcaci R, Baran I. Oral malodor and removable complete dentures in the elderly. Oral 72 Stockmann P, Vairaktaris E, Wehrhan F et al. Osteotomy and primary wound closure in
Surg Oral Med Oral Pathol Oral Radiol Endod 2008; 105(6): e5–e9. bisphosphonate-associated osteonecrosis of the jaw: a prospective clinical study with
35 Astor FC, Hanft KL, Ciocon JO. Xerostomia: a prevalent condition in the elderly. Ear 12 months follow-up. Support Care Cancer 2010; 18(4): 449–460.
Nose Throat J 1999; 78(7): 476–479. 73 Seemann R. Organoleptische Beurteilung. In: Seemann R, editor. Halitosis-
36 Prahabita PK, Bhat KM, Bhat GS. Oral malodor: a review of the literature. J Dent Hyg management in der Zahnärztlichen praxis. Balingen: Spitta, 2006.
2006; 80(3): 8. 74 Tonzetich J. Production and origin of oral malodour: a review of mechanisms and
37 Delanghe G, Ghyselen J, van Steenberghe D et al. Multidisciplinary breath-odour methods of analysis. J Periodontol 1977; 48(1): 13–20.
clinic. Lancet 1997; 350(9072): 187. 75 Rosenberg M, McCulloch CA. Measurement of oral malodour: current methods and
38 van den Broek AM, Feenstra L, de Baat C. A review of the current literature on aetiology future prospects. J Periodontol 1992; 63(9): 776–782.
and measurement methods of halitosis. J Dent 2007; 35(8): 627–635. 76 Salako NO, Philip L. Comparison of the use of the Halimeter and the OralChroma2 in
39 Ansai T, Takehara T. Tonsilloliths as a halitosis-inducing factor. Br Dent J 2005; the assessment of the ability of common cultivable oral anaerobic bacteria to produce
198(5): 263–264. malodorous volatile sulphur compounds from cysteine and methionine. Med Princ
40 Mulwafu W, Fagan JJ, Isaacs S. Adult tonsillectomy—are long waiting lists putting Pract 2011; 20(1): 75–79.
patients at risk? S Afr J Surg 2006; 44(2): 66–68. 77 Tonzetich J. Direct gas chromatographic analysis of sulphur compounds in mouth air
41 Attia EL, Marshall KG. Halitosis. Can Med Assoc J 1982; 126(11): 1281–1285. in man. Arch Oral Biol 1971; 16(6): 587–597.
42 Fletcher SM, Blair PA. Chronic halitosis from tonsilloliths: a common aetiology. J La 78 Larsson BT, Widmark G. A gas chromatographic method for analysis of volatiles in
State Med Soc 1988; 140(6): 7–9. saliva samples. Acta Pharm Sued 1969; 6(4): 479–488.
43 Tsuneishi M, Yamamoto T, Kokegucji S et al. Composition of the bacterial flora in 79 Tonzetich J, Coil JM, Ng W. Gas chromatographic method for trapping and detection of
tonsilloliths. Microbes Infect 2006; 8(9/10): 2384–2389. volatile organic compounds from human mouth air. J Clin Dent 1991; 2(3): 79–82.
44 Amir E, Shimonov R, Rosenberg M. Halitosis in children. J Pediatr 1999; 134(4): 80 Bradshaw DJ, Perring KD, Cawkill PM et al. Creation of oral care flavours to deliver
338–343. breath-freshening benefits. Oral Dis 2005; 11(Suppl 1): 75–79.
45 Monteiro-Amado F, Chinellato LE, de Rezende ML. Evaluation of oral and nasal 81 Menon MV, Coykendall AL. Effect of tongue scraping. J Dent Res 1994; 73(9): 1492.
halitosis parameters in patients with repaired cleft lip and/or palate. Oral Surg Oral 82 Outhouse TL. A platinum standard of effectiveness in oral health care interventions:
Med Oral Pathol Oral Radiol Endod 2005; 100(6): 682–687. the Cochrane systemic review. Gen Dent 2006; 54(4): 228–229.
46 Lanza DC. Diagnosis of chronic rhinosinusitis. Ann Otol Rhinol Laryngol 2004; 83 van der Sleen MI, Slot DE, van Trijffel E et al. Effectiveness of mechanical tongue
193(Suppl 1): 10–14. cleaning on breath odour and tongue coating: a systematic review. Int J Dent Hyg
47 Mazzone PJ. Analysis of volatile organic compounds in the exhaled breath for the 2010; 8(4): 258–268.
diagnosis of lung cancer. J Thorac Oncol 2008; 3(7): 774–780. 84 Quirynen M, Zhao H, van Steenberghe D. Review of the treatment strategies for oral
48 Stoeckli SJ, Schmid S. Endoscopic stapler-assisted diverticuloesophagostomy for malodour. Clin Oral Investig 2002; 6(1): 1–10.
Zenker’s diverticulum: patient satisfaction and subjective relief of symptoms. 85 Outhouse TL, Al-Alawi R, Fedorowicz Z et al. Tongue scraping for treating halitosis.
Surgery 2002; 131(2): 158–162. Cochrane Database Syst Rev 2006; (2): CD005519.
49 Struch F, Schwahn C, Wallaschofski H et al. Self-reported halitosis and gastro- 86 Bollen CM, Vandekerckhove BN, Papaioannou W et al. Full- versus partial-mouth
oesophageal reflux disease in the general population. J Gen Intern Med 2008; disinfection in the treatment of periodontal infections. A pilot study: long-term
23(3): 260–266. microbiological observations. J Clin Periodontol 1996; 23(10): 960–970.
50 Werdmuller BF, van der Putten TB, Balk TG et al. Clinical presentation of Helicobacter 87 Quirynen M, Zhao H, Soers C et al. The impact of periodontal therapy and the
pylori-positive and -negative functional dyspepsia. J Gastroenterol Hepatol 2000; adjunctive effect of antiseptics on breath odour-related outcome variables: a
15(5): 498–502. double-blind randomized study. J Periodontol 2005; 76(5): 705–712.
51 Moshkowitz M, Horowitz N, Leshno M et al. Halitosis and gastroesophageal reflux 88 Delanghe G, Ghyselen J, Bollen C et al. An inventory of patients’ response to treatment
disease: a possible association. Oral Dis 2007; 13(6): 581–585. at a multidisciplinary breath odor clinic. Quint Int 1999; 70(3): 307–310.
52 Hoshi K, Yamano Y, Mitsunaga A et al. Gastrointestinal diseases and halitosis: 89 Rosenberg M, Gelernter I, Barki M et al. Day-long reduction of oral malodour by a two-
association of gastric Helicobacter pylori infection. Int Dent J 2002; 52(Suppl 3): phase oil: water mouthrinse as compared to chlorhexidine and placebo rinses. J
207–211. Periodontol 1992; 63(1): 39–43.
53 Lee H, Kho HS, Chung JW et al. Volatile sulphur compounds produced by Helicobacter 90 Pitts G, Brogdon C, Hu L et al. Mechanism of action of an antiseptic, antiodor
pylori. J Clin Gastroenterol 2006; 40(5): 421–426. mouthwash. J Dent Res 1983; 62(6): 738–742.
54 Suzuki N, Yoneda M, Naito T et al. Detection of Helicobacter pylori DNA in the saliva of 91 Frascella J, Gilbert R, Fernandez P. Door reduction potential of a chlorine dioxide
patients complaining of halitosis. J Med Microbiol 2008; 57(Pt 12): 1553–1559. mouthrinse. J Clin Dent 1998; 9(1): 39–42.
55 Kinberg S, Stein M, Zion N et al. The gastrointestinal aspects of halitosis. Can J 92 Raven S, Matheson J, Huntington E et al. The efficacy of a combined zinc and triclosan
Gastroenterol 2010; 24(9): 552–556. system in the prevention of oral malodour. In: van Steenberghe D, Rosenberg M,
56 Yilmaz AE, Bilici M, Tonbul A et al. Paediatric halitosis and Helicobacter editors. Bad breath: a multidisciplinary approach. Leuven: Leuven University Press,
pylori infection. J Coll Physicians Surg Pak 2012; 22(1): 27–30. 1996: 241–254.
57 Stephenson BM, Rees BI. Extrinsic duodenal obstruction and halitosis. Postgrad Med 93 Suarez FL, Furne JK, Springfield J et al. Morning breath odour: influence of treatments
J 1990; 66(777): 568–570. on sulphur-gases. J Dent Res 2000; 79(10): 1773–1777.
58 Preti G, Clark L, Cowart BJ et al. Non-oral aetiologies of oral malodour and altered 94 Navada R, Kumari H, Le S et al. Oral malodour reduction from a zinc-containing
chemosensation. J Periodontol 1992; 63(9): 790–796. toothpaste. J Clin Dent 2008; 19(2): 69–73.
59 Keles M, Tozoglu U, Uyanik A et al. Does peritoneal dialysis affect halitosis in patients 95 Feng X, Chen X, Cheng R et al. Breath malodour reduction with use of a stannous
with end-stage renal disease? Perit Dial Int 2011; 31(2): 168–172. containing sodium fluoride dentifrice: a meta-analysis of four randomized and
60 Feller L, Blignaut E. Halitosis: a review. J South African Den Assoc 2005; 60(1): 17– controlled clinical trials. Am J Dent 2010; 23(Spec No B): 27B–31B.
19. 96 Sharma NC, Galustians HJ, Qaqish J et al. Clinical effectiveness of a dentifrice
61 Bollen CM, Rompen EH, Demanez JP. Halitosis: a multidisciplinary problem. Rev Med containing triclosan and a copolymer for controlling breath odour. Am J Dent 2007;
Liege 1999; 54(1): 32–36. French. 20(2): 79–82.
62 van Steenberge D. Endocrinological aspects. In: van Steenberghe D, editor. 97 Fedorowicz Z, Aljufairi H, Nasser M et al. Mouthrinses for the treatment of halitosis.
Ademgeur. Houten: Prelum Uitgevers, 2009: 107–115. Cochrane Database Syst Rev 2008; (4): CD006701.

International Journal of Oral Science

 Halitosis: the multidisciplinary approach
CML Bollen and T Beikler
63

98 Young A, Jonski G, Rölla G et al. Effects of metal salts on the oral production of 111 Henker J, Schuster F, Nissler K. Successful treatment of gut-caused halitosis with a
volatile sulphur containing compounds (VSC). J Clin Periodontol 2001; 28(8): suspension of living non-pathogenic Escherichia coli bacteria—a case report. Eur J
776–781. Pediatr 2001; 160(10): 592–594.
99 Young A, Jonski G, Rölla G. Inhibition of orally produced volatile sulphur compounds 112 Nagel D, Lutz C, Filippi A. Halitophobia—an under-recognized clinical picture.
by zinc, chlorhexidine or cetylpyridinium chloride—effect of concentration. Eur J Oral Schweiz Monatsschr Zahnmed 2006; 116(1): 57–64.
Sci 2003; 111(5): 400–404. 113 Malasi TH, El-Hilu SM, Mirza IA et al. Olfactory delusional syndrome with various
100 Sterer N, Rubinstein Y. Effect of various natural medicinals on salivary protein aetiologies. Br J Psychiatry 1990; 156: 256–260.
putrefaction and malodour production. Quint Int 2006; 37(8): 653–658. 114 Bohn P. Imagined halitosis: a social phobia symptom? J Calif Dent Assoc 1997; 25(2):
101 Grandis JR, Johnson JT, Vickers RM et al. The efficacy of perioperative antibiotic 161–164.
therapy on recovery following tonsillectomy in adults: randomized double-blind 115 Eli I, Koriat H, Baht R et al. Self-perception of breath odor: role of body image and
placebo-controlled trial. Otolaryngol Head Neck Surg 1992; 106(2): 137–142. psychopathologic traits. Percept Mot Skills 2000; 91(3 Pt 2): 1993–2001.
102 Bunzen DL, Campos A, Leão FS et al. Efficacy of functional endoscopic sinus 116 Lochner C, Stein DJ. Olfactory reference syndrome: diagnostic criteria and differential
surgery for symptoms in chronic rhinosinusitis with or without polyposis. Braz J diagnosis. J Postgrad Med 2003; 49(4): 328–331.
117 Suzuki N, Yoneda M, Naito T et al. Relationship between halitosis and psychologic
Otorhinolaryngol 2006; 72(2): 242–246.
status. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2008 Oct;106(4): 542–547.
103 Dal Rio AC, Passos CA, Nicola JH et al. CO2 laser cryptolysis by coagulation for the
118 Adams KH, Hansen ES, Pinborg LH et al. Patients with obsessive/compulsive disorder
treatment of halitosis. Photomed Laser Surg 2006; 24(5): 630–636.
have increased 5-HT2A receptor binding in caudate nuclei. Int J Neuropsycho-
104 Shortt P, Wilson R, Erskine I. Tendinitis: the Achilles heel of quinolones! Emerg Med J
pharmacol 2005; 8(3): 391–401.
2006; 23(12): e63.
119 Uher R, Farmer A, Henigsberg N et al. Adverse reactions to antidepressants. Br J
105 Labenz J, Morgner-Miehlke A. An update on the available treatments for non-erosive Psychiatry 2009; 195(3): 202–210.
reflux disease. Expert Opin Pharmacother 2006; 7(1): 47–56. 120 Persson S, Edlund MB, Claesson R et al. The formation of hydrogen sulphide and
106 Bytzer P, Dahlerup JF, Eriksen JR et al. Diagnosis and treatment of Helicobacter pylori methylmercaptan by oral bacteria. Oral Microbiol Immunol 1990; 5(4): 195–201.
infection. Dan Med Bull 2011; 58(4): C4271. 121 Claus D, Geypens B, Rutgeerts P et al. Where gastroenterology and periodontology
107 Malaguarnera M, Restuccia S, Motta M et al. Interferon, cortisone, and antivirals meet: determination of oral volatile organic compounds using closed-loop trapping
in the treatment of chronic viral hepatitis: a review of 30 years of therapy. and high-resolution gas chromatography-ion trap detection. In: van Steenberghe D,
Pharmacotherapy 1997; 17(5): 998–1005. Rosenberg M, editors. Bad breath: a multidisciplinary approach. Leuven: Leuven
108 Burton JP, Chilcott CN, Moore CJ et al. A preliminary study of the effect of probiotic University Press, 1996: 15–28.
Streptococcus salivarius K12 on oral malodour parameters. J Appl Microbiol 2006;
100(4): 754–764.
109 Iwamoto T, Suzuki N, Tanabe K et al. Effects of probiotic Lactobacillus salivarius This work is licensed under a Creative Commons
WB21 on halitosis and oral health: an open-label pilot trial. Oral Surg Oral Med Oral Attribution-NonCommercial-NoDerivative Works 3.0
Pathol Oral Radiol Endod 2010; 110(2): 201–208.
110 Kang MS, Kim BG, Chung J et al. Inhibitory effect of Weissella cibaria isolates on the Unported License. To view a copy of this license, visit http://
production of volatile sulphur compounds. J Clin Periodontol 2006; 33(3): 226–232. creativecommons.org/licenses/by-nc-nd/3.0

International Journal of Oral Science

View publication stats