Australian Dental Journal

The official journal of the Australian Dental Association

Australian Dental Journal 2020; 65: 4–11

doi: 10.1111/adj.12725

Halitosis: prevalence, risk factors, sources, measurement

and treatment – a review of the literature
J Wu,* RD Cannon,* P Ji,† M Farella,* L Mei*
*Department of Oral Sciences, Faculty of Dentistry, Sir John Walsh Research Institute, University of Otago, Dunedin, New Zealand .
†Stomatological Hospital of Chongqing Medical University, Chongqing, China .

ABSTRACT
Halitosis, an offensive breath odour, has multiple sources and negative impacts on people’s social interactions and qual-
ity of life. It is important for health care professionals, including general physicians and dental professionals, to under-
stand its aetiology and risk factors in order to diagnose and treat patients appropriately. In this study, we have reviewed
the current literature on halitosis regarding its prevalence, classification, risk factors, sources, measurement and treat-
ment.
Keywords: Bad breath, halitosis, oral malodour.
Abbreviations and acronyms: BANA = benzoyl-DL-arginine-naphthylamide; VSC = volatile sulphur compound.
(Accepted for publication 9 October 2019.)

productivity of people in the community and the cor-

INTRODUCTION
Halitosis is commonly defined as an unpleasant or
offensive odour that is emitted from the oral cavity.1
The word halitosis is derived from Latin, where hali-
tus means breathed air and osis means pathologic
alteration. It is one of the most frequent complaints
patients present with to the dentist, after dental car-
ies and periodontal disease.2 Halitosis is mostly due
to putrefying bacteria living on the dorsum of the
tongue and the volatile sulphur compounds (VSCs)
produced from food remnants. The main compounds
thought to be the primary cause of halitosis are
hydrogen sulphide, methyl mercaptan and dimethyl
sulphide.3–5
The social and psychosocial effects of halitosis are
widely regarded to have the most significant impact
for the sufferer. Studies have shown that personal dis-
comfort and social embarrassment were the main con-
cerns for individuals affected by halitosis and also the
primary reason why patients sought professional assis-
tance.6,7 Some individuals, however, might be una-
ware of their bad breath, which creates a problem
when researchers try to estimate the prevalence of hal-
itosis in a population. The problem is accentuated
when these people start talking to others, resulting in
social isolation in the wider community.8,9 To a cer-
tain extent, halitosis can also affect the work
responding health care system.10
PREVALENCE OF HALITOSIS
There is little consensus in the literature about the
prevalence of halitosis. This is probably due to the
subjective nature of the information and measure-
ments gathered and the methodological differences
between studies.11–14 For example, the prevalence of
self-perceived halitosis for Polish university students
was found to be 24%, while a study in the US
reported that practising dentists diagnosed 41% of
their patients in 1 week had halitosis.14,15 For adoles-
cents, surveys in Korea, Brazil and Sweden indicate
that the prevalence of halitosis is approximately
25%.16–18 In a paediatric population where the mean
age was 12 years old, the reported prevalence was
37.6%.19 While there is a variation in the prevalences
in these studies, it appears generally true that there is
at least one halitosis sufferer for every four peo-
ple.20,21
It has been reported that dental students exhibit a
lower prevalence of halitosis than the general popula-
tion.14,22 This can probably be put down to their
greater motivation in maintaining their oral hygiene
gained from their dental education. Halitosis has been
found to be more common and of greater intensity in

4 © 2019 Australian Dental Association


older people.5 There is no consensus on whether the
prevalence of halitosis is greater in males or
females.1,18,19,23 There are some papers that claim
that the condition is more prevalent among females
and have offered plausible reasons why. For example,
a Chinese study suggested that the prevalence in
women was greater due to their greater willingness to
consult health professionals about the problem.8
However, a self-administered questionnaire in India
indicated that female students had better oral hygiene
practices which resulted in a lower proportion of self-
reported halitosis.24
Most studies support the proposition that halitosis
is an underestimated oral health problem in the gen-
eral population.11,16 This is largely based on the fact
that many sufferers are either not aware of it or too
embarrassed about their condition to report it or seek
help.25,26
CLASSIFICATION OF HALITOSIS
The classification of halitosis generally includes genuine
halitosis (physiologic and pathologic halitosis), pseudo-
halitosis and halitophobia.27 Genuine halitosis is an
obvious oral malodour, with intensity beyond a socially
acceptable level. Genuine halitosis is further subclassified
into physiologic halitosis and pathologic halitosis. Physi-
ologic halitosis is described as malodour that arises
through putrefactive processes within the oral cavity,
without any specific disease or pathologic condition that
could cause halitosis. The origin of physiologic halitosis
is mainly the dorsoposterior region of the tongue. Patho-
logic halitosis is subclassified into oral pathologic halito-
sis (caused by oral diseases) and extra-oral pathologic
halitosis (e.g. originated from nasal, paranasal, laryngeal
regions, pulmonary tract and upper digestive tract).
Pseudo-halitosis is a condition in which patients
stubbornly complain of the existence of oral malodour
but it is not perceived by others. Usually the condition
is improved by counselling and simple oral hygiene
measures.
Halitophobia is the condition where patients persist
in believing that they have halitosis even after the
treatment of either genuine halitosis or pseudo-halito-
sis, without any physical or social evidence suggesting
the presence of halitosis.
RISK FACTORS FOR HALITOSIS
Dry mouth
Dry mouth has been found to be associated with oral
malodour, which can be explained by the reduced
salivary flow favouring anaerobic bacterial putrefac-
tion of food debris that remains in the oral cavity
after eating.24,28 Dry mouth also results in an
© 2019 Australian Dental Association
Halitosis
increased Gram-negative bacterial load, which
increases VSC production, the main contributor to
halitosis.29 This is especially evident in the morning as
salivary flow has decreased during the sleeping period;
as demonstrated in 70% of participants in a study in
Baghdad, Iraq.22
Smoking
A number of studies have found that smoking is associ-
ated with the increased incidence and severity of halito-
sis.16,24 This largely stems from the fact that cigarette
smoking is associated with the high levels of VSCs in
diseased periodontal pockets, as well as a harmful effect
on the periodontium.30 The believed cause is either
through the cigarette smoke altering the balance of the
microbial populations and niches in subgingival plaque
or through an increase in the absolute numbers of VSC-
producing bacteria.13,20. In addition, tobacco smoke
per se contains VSCs and smoking also predisposes
hyposalivation, which aggravates people’s perception
of their own breath malodour.
Dietary habits and alcohol consumption
Some foods, especially those containing volatile com-
pounds such as garlic, onions and spices, can cause
transient unpleasant oral malodour, but not all indi-
viduals would consider such alterations as ‘halitosis’
because this will be influenced by what people believe
is an acceptable breath smell.31 Durian, a fruit with a
very pungent odour, can also give rise to a profound
dietary-related halitosis.
Alcohol consumption is another potential risk fac-
tor for bad breath. It has been found that chronic
alcohol drinkers have a unique type of breath that
might result from oxidation of alcohol in the mouth
and liver, producing acetaldehyde and other odorous
byproducts. Alcohol might also cause hyposalivation
and dry mouth.32
SOURCES OF HALITOSIS
Halitosis can be classified as either primary, sometimes
termed extra-oral, which originates from the exhalation
by the lungs, or secondary, sometimes termed intra-oral,
which originates from the mouth or upper airways.33,34
The best way to differentiate between the two forms is
by comparing mouth breath with nose breath.34 Most
cases of halitosis are of the secondary form which is due
to the VSCs produced in the oral cavity.
Extra-oral sources
Although 90% of halitosis is intra-oral, it is still
important to consider potential extra-oral systemic
5
J Wu et al.
causes. The liver is one of the most important extra-
oral sources of bad breath, with its chronic infection
affecting approximately 400 million people around
the world. The term fetor hepaticus, referring to a
slightly sweet, musty and faecal breath is directly cor-
related with hepatitis and liver failure. A defining fea-
ture of fetor hepaticus is the VSC methyl mercaptan,
and its association with halitosis is substantial, espe-
cially when combined with known attenuating factors
such as periodontitis, xerostomia and smoking.35,36
Extra-oral halitosis can also be caused by respiratory
tract infections causing nasal or sinus secretions pass-
ing into the pharynx, gastrointestinal disease, haema-
tological or endocrine system disorders.37 The main
VSC associated with extra-oral halitosis is dimethyl
sulphoxide whereas the main VSCs contributing to
intra-oral halitosis are methyl mercaptan and hydro-
gen sulphide.34,37
Intra-oral sources
It has been well demonstrated that in 90% of halitosis
cases the source of the malodour is the oral cav-
ity.2,24,38,39 The humid conditions and temperature of
up to 37°C inside the oral cavity provide an ideal
environment for bacteria to flourish and efficiently
metabolize sulphur-containing amino acids (L-cys-
teine + L-methionine) to generate hydrogen sulphide
and methyl mercaptan.20,37,40
Tongue coating
Tongue coating is considered the most important con-
tributor to halitosis levels.3,41,42 This is probably
because the dorsum of the tongue is a reservoir for
anaerobic bacteria: a single epithelial cell on the dor-
sum of the tongue can harbour up to 100 bacteria,
more than anywhere else in the oral cavity.43,44 This
is mainly due to the ‘cratered’ surface of the tongue
consisting of a complex papillary structure that sup-
ports the retention of considerable quantities of bacte-
ria. These microbes, especially Gram-negative and
proteolytic nitrate-producing anaerobes, for example,
Veillonella and Actinomyces, are proficient at produc-
ing odiferous substances from epithelial cell debris
and food remnants.2,5,36,38,45,46 There is also high
bacterial species diversity on the dorsum of the ton-
gue, suggesting that oral malodour is created by inter-
actions between several bacterial species rather than a
few dominant ones.46 Clinically, there is a correlation
between more severe halitosis and greater tongue
coating scores. Tongue coating is most commonly
classified using the Kojima scoring criteria.11,36
The association between halitosis and tongue coat-
ing is particularly strong in the region posterior to the
circumvallate papillae. These surfaces have been
6 © 2019 Australian Dental Association
shown to carry the highest load of the Gram-negative
bacteria that contribute to oral malodour.38 To com-
pound the issue, these regions are also less accessible
to routine oral hygiene procedures, allowing a greater
build-up of bacteria. Other studies propose that it is
the composition of the coating rather than the amount
that has the greatest impact on halitosis.45 For exam-
ple, halitosis has been related simply to the presence
of Porphyromonas gingivalis on the dorsum of the
tongue, rather than the thickness of the coating.45 In
addition to the important role of Gram-negative bac-
teria in VSC production, the b-galactosidase of Gram-
positive bacteria is also considered to play a role,
especially in tongue coating-associated malodor.47
Periodontal disease
Many studies have put forward a compelling case sup-
porting a direct correlation between periodontal
health and halitosis.3,27 Bollepalli’s study, for exam-
ple, showed that all the clinical parameters for mea-
suring periodontal disease were significantly related to
oral malodour.23
A proposed microbiological link between halitosis
and periodontal disease is through a property of the
main microbially generated VSCs, whereby hydrogen
sulphide and methyl mercaptan facilitate the penetra-
tion of lipopolysaccharide into the gingival epithe-
lium, inducing inflammation.41 The VSCs also aid
bacterial invasion of the connective tissue by their
toxic effects on epithelial cells, while methyl mercap-
tan hinders epithelial cell growth and proliferation.48
This is accentuated by decreasing oxygen tension aris-
ing from an increase in periodontal pocket depth,
with a concomitant decrease in pH, which is neces-
sary for the putrefaction of amino acids that create
VSCs.29 It has also been suggested that saliva from
patients that suffer from periodontal disease might
produce increased amounts of VSCs.20
Another theory supporting the connection between
halitosis and periodontal disease originates from the
fact that patients with periodontitis have markedly
increased tongue coating.27 It is suggested that the
anaerobic bacteria present on the tongues of these
patients are responsible for their halitosis rather than
the bacteria associated with the periodontal disease.
Other studies have postulated that halitosis might be
due to an increased concentration of VSCs in gingival
crevicular sites, which are quite deep in periodontally
compromised patients.45 Some studies, however, con-
sider the periodontal pocket to be a closed environ-
ment and that only a small fraction of malodorous
gases is able to escape into the mouth. This might
explain why some studies have failed to find a correla-
tion between periodontal health and halito-
sis.20,45,49,50 Besides periodontal conditions, untreated

deep carious lesions also create deep sites that can
retain food debris and dental plaque and result in hal-
itosis.
Other intra-oral sources
Other factors contributing to intra-oral halitosis
include exposed tooth pulps, non-vital teeth, healing
wounds and fixed orthodontic appliances. All of these
factors create a food or plaque retention site which
enables putrefaction of amino acids by bacteria, caus-
ing halitosis.51 A number of acute conditions can also
cause oral malodour through the production of a
characteristic fetor oris. Pericoronal infections, oral
ulcerations and acute necrotizing ulcerative gingivitis
are such examples but intra-oral halitosis still mostly
arises through the action of bacteria on the dorsum of
the tongue and bacteria associated with periodontal
disease.20
There are also cases of temporary halitosis that lasts
for only several hours. For example, the period after
someone has eaten foods containing VSCs like garlic
or fast food.6 In contrast, foods with high-fibre con-
tents such as fruit and vegetables or green tea pro-
mote gastric emptying and have been reported to
effectively reduce VSC levels for a period of time.52,53
Delusional halitosis
In addition to conventional halitosis, approximately
5% of cases are termed ‘delusional halitosis’ or
‘monosymptomatic hypochondriasis’. These are situa-
tions where the patient complains of persistent malo-
dour but there are no subjective or objective signs
from examination and further investigations. This can
occur either because the patient is convinced they
have a problem (pseudo-halitosis) or because they are
so afraid they might develop the condition that they
believe they have it already (halitophobia). These
cases are very rare but should not be disregarded
when a patient sits in the dental chair. Interestingly,
advertisements of oral hygiene products have shown
to be responsible for the increase in the number of
patients with halitophobia.31 In terms of treatment,
the recommendation for delusional halitosis is to care-
fully explain the actual situation to the patient and
send them for psychological or psychiatric support as
soon as possible.54 A multidisciplinary approach
involving dentists, health care practitioners, psycholo-
gists and psychiatrists is thus necessary for these con-
ditions.29
MEASUREMENT OF HALITOSIS
There are many different methods for measuring hali-
tosis. Organoleptic measurement, which involves
© 2019 Australian Dental Association
Halitosis
using the human nose to score the intensity of odours
emanating from the patient’s mouth at varying dis-
tances,39 is considered the gold standard for halitosis
measurement.24 Testing should be undertaken in the
morning before eating and hygiene procedures are
performed to obtain the correct measurement of the
condition.55 The patient should also count aloud from
1 to 10 before measurement commences to promote
drying of the palate and tongue mucosa and facilitate
the release of VSCs.29 The use of a panel of judges is
likewise recommended to improve the reliability of
the results but this can increase cost for the test and
might be difficult in a practice setting. The most com-
mon reason why this method is not used is the unap-
pealing method of measurement for the examiner(s)
and socially uncomfortable position in which the
patient is placed. Moreover, the patient needs to avoid
consuming any odiferous foods or liquids for 48 h
that could affect the clinical reading, prior to the mea-
surement, to ensure that the results collected with the
Organoleptic Score method are accurate.27,56
Objective measurements of halitosis can be obtained
with an electrochemical meter or gas chromatography.
Electrochemical meter such as the Halimeter (Interscan
Corp., Chatsworth, LA, USA) and BreathtronTM (New
Cosmos Electric, Osaka, Japan) directly measure the
level of VSCs in breath samples.24,42 The sensitivity
and specificity of the Halimeter have been reported to
be 92.2% and 91.7% respectively.23,41 An electro-
chemical reaction with sulphur-containing compounds
generates an electric current that is proportional to the
concentration of VSCs. These portable sulphide moni-
tors are currently being employed in many clinical
practices, mainly due to their ease of use in generating
a quantitative measure of VSCs chairside.57 It must be
noted though, that this method of sulphide monitoring
has a major disadvantage in not being able to measure
dimethyl sulphide accurately.29,55 In addition, the pres-
ence of compounds like alcohols and phenyl com-
pounds and polyamines can interfere with readings.42
With recent technological advancements, the use of
gas chromatography to measure VSCs has become
more popular. It separates and analyses compounds
that are vaporized using a gas chromatograph
equipped with a flame photometric detector. This gives
the ability to distinguish between different compounds
that cause halitosis. It is therefore one of the most
accurate tests currently available, both in terms of its
objectivity and sensitivity in detecting low concentra-
tions of molecules.11,42,58,59 However, this technique is
not easily implemented clinically using traditional
chromatographs because of the relatively high cost of
the equipment, the requirement for highly trained
operators, and the extensive procedures involved.
More recently, portable gas chromatographs such as
the OralChromaTM (Abilit Corporation, Osaka, Japan)
7
J Wu et al.
and the Twin-BreasorTM (GC, Tokyo, Japan) have
become available and compare favourably to tradi-
tional GC machines.60 Currently, the most promising
alternative method for both research and clinical pur-
poses revolves around the use of chemical sensors.
These measure compounds inside the periodontal
pockets and dorsum of the tongue directly and have
demonstrated results very comparable to organoleptic
readings and gas chromatography measurements.61
There are also a number of indirect methods for
measuring halitosis. For example, the benzoyl-DL-argi-
nine-naphthylamide (BANA) test,62 which utilizes a
test strip containing the synthetic trypsin substrate
benzoyl-DL-arginine-2-naphthylamide. This enables the
detection of proteolytic obligate Gram-negative anaer-
obic bacteria, such as Treponema denticola, Porphy-
romonas gingivalis or Bacteroides forsythus, which
produce enzymes that hydrolyse the substrate and gen-
erate a blue colour.37 Test results, have been demon-
strated to show a strong positive correlation with
periodontal disease activity. However, the specific role
of the different types of bacteria present cannot be
fully determined.42 Salivary incubation is another indi-
rect method to measure halitosis. Saliva samples are
incubated in sealed containers at 37 °C and the head-
spaces of the containers analysed for VSCs by chemical
detection or organoleptic scoring.7,63 The method has
been demonstrated to produce results that are extre-
mely accurate when compared with results from the
‘gold standard’ organoleptic method.7,63
TREATMENT OF HALITOSIS
Halitosis is a significant clinical condition that should be
identified and treated by dentists in their daily practise.
First, the aetiology must be pinpointed correctly through
detailed clinical examination to tailor the correct treat-
ment for the patient. This includes a thorough medical
history complete with dietary analysis and identification
of personal habits to ensure that an extra-oral cause is
not missed.42 When dental issues are identified as the
major cause of halitosis, appropriate treatment usually
achieves complete resolution.12,24 Mechanical dental
treatment procedures include scaling, root planing and
detailed oral hygiene instructions.37,63 Any plaque and
food traps such as faulty restorations or open cavitated
lesions and infections such as pericoronitis should also
be addressed. It is crucial that individualized therapeutic
treatment plans are given for each patient to combat hal-
itosis as there is no generalized treatment.29
A critical issue in the treatment planning of a hali-
tosis sufferer revolves around their diet. Instructions
to quit smoking and use of baking soda dentifrices
have been recommended.29 One home care procedure
that has plenty of support in the literature is tongue
brushing with specialized tongue scrapers.35,51,64,65
8 © 2019 Australian Dental Association
These instruments are thought to be more effective at
reducing the biofilm on the dorsum of the tongue
compared to simple toothbrush bristles. However, one
study has shown, using a Halimeter, that outcomes
with a tongue scraper were comparable to those
obtained by brushing the tongue with tongue cleans-
ing devices on the back of a toothbrush.66 Also there
is debate as to how long the effects of tongue scraping
last. According to a Cochrane review, tongue brushing
in any form only conveys relief from halitosis for a
period of up to 30 min, with no significant long-term
effects.67 In fact, there is little evidence for the long-
term efficacy of any halitosis treatment method,
although tongue brushing does appear to be the best
option at the present time.
There are many forms of chemotherapeutic treat-
ment that might be recommended by the dentist as
part of the treatment as an adjunct to mechanical
therapy. Peppermint mouth rinses are safe formulation
to use at home and have been shown to be successful
in improving halitosis measures over a 1-week obser-
vation period.6,68,69 The zinc component of mouth-
wash has been shown to be effective in reducing
halitosis, by inhibiting bacterial breakdown of pro-
teins, hence VSC production.26 Chlorhexidine is
another valuable antiseptic agent which inhibits a
wide spectrum of microbes, controls plaque accumula-
tion and hence reduces halitosis. Its method of action
is by penetrating the cell membrane of oral bacteria,
causing cell leakage and disruption of bacterial meta-
bolism thus inhibiting cell growth.70 This treatment is
not without side effects, however, such as causing
abnormal taste sensation and long-term use can result
in reversible staining of teeth and mucosal surfaces. A
study using a dog model indicated that cetylpyri-
dinium chloride could be used to effectively control
plaque and calculus, but these results should be inter-
preted with caution because human tolerance of
chemicals might differ from that of animals.70
Chlorhexidine and cetylpyridinium chloride are
both compounds effective in reducing halitosis. A
Cochrane review has found that mouthwashes with
formulations of both compounds attained the best
results in reducing the concentrations of VSCs found
in expelled air and salivary bacterial counts.71 There-
fore, the potential benefit of these mouthwashes
should be considered in the light of the potential side
effects discussed above. Triclosan, which is present in
some toothpastes is another compound shown to have
broad-spectrum effects on Gram-negative bacteria. Its
effects on both soft and hard tissues are known to last
up to 12 h from the time of application.55,72
The use of probiotics has also been shown to reduce
the counts of bacteria that lead to caries and peri-
odontal disease. For example, daily consumption of
tablets containing probiotic Lactobacillus salivarius

WB21 was shown to help in controlling oral malo-
dour.73 In another study, consumption of two tablets
per day of probiotic Streptococcus salivarius M18 for
1 month by patients wearing orthodontic brackets
decreased VSC levels at the 3-month follow-up signifi-
cantly.74 Despite the potential advantages of probiotic
treatment, there is still a lack of high-quality evidence
regarding its clinical efficacy in humans and any long-
term consequences.75–77 Odour masking agents like
generic rinsing products, flavoured toothpastes and
mint tablets from the supermarket have also shown
promise in reducing halitosis symptoms but only have
a very restricted short-term effect.77 Patients with oral
malodour but showing no oral cause of halitosis (e.g.
periodontal disease, abnormal tongue coating and
poor oral health) are usually classified as having
extra-oral halitosis, and they should be referred to
medical specialists. Patients with pseudo-halitosis need
to be counselled, with an explanation of the examina-
tion results. Overall, there are many home treatment
measures available to fight halitosis but professional
advice should always be consulted to avoid misdiag-
nosis and unwanted side effects.
SUMMARY
Halitosis, an offensive breath odour, has multiple
sources and negative impacts on people’s social inter-
actions and quality of life. It is important for health
care professionals, including general physicians and
dental professionals, to understand its aetiology and
risk factors in order to diagnose and treat patients
appropriately.
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