UNIVERSIDADE ESTADUAL PAULISTA
“JÚLIO DE MESQUITA FILHO”
Instituto de Ciência e Tecnologia
Campus de São José dos Campos
LITERATURE REVIEW DOI: https://doi.org/10.4322/bds.2024.e4042
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This is an Open Access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in
any medium, provided the original work is properly cited.
Halitosis: a conceptual, etiologic and therapeutic approach
Halitose: uma abordagem conceitual, etiológica e terapêutica
Karolina Skarlet Silva VIANA1 , Esther Aranda Figueiredo SOUZA1 , Rafael Paschoal Esteves LIMA1 , Luis Otavio Miranda COTA1
1 - Universidade Federal de Minas Gerais, Faculdade de Odontologia, Departamento de Clínica, Patologia e Cirurgia Odontológicas. Belo
Horizonte, Brazil.
How to cite: Viana KSS, Souza EAF, Lima RPE, Cota LOM. Halitosis: a conceptual, etiologic and therapeutic approach. Braz Dent Sci.
2024;27(1):e4042. https://doi.org/10.4322/bds.2024.e4042
ABSTRACT
Objective: Halitosis is the offensive odor emanated by the oral and nasal cavities and perceived by the individual
and/or by other people. Halitosis is a symptom that directly impacts on the social aspects of an individual’s life
and may be a sign for a systemic disorder in some cases. Material and Methods: A search was conducted on the
literature in order to gather the main aspects about halitosis and make a review about the main features necessary
to the clinical practice when a professional deals with a patient with halitosis. Results: The information was
summarized and discussed with a focus on what clinicians should be aware of when dealing with a patient with
halitosis. Conclusion: Halitosis is a prevalent symptom that affects approximately 25% of the individuals. Its
classication takes into consideration the origin of the compounds producing the malodor. The diagnosis must
take into consideration the various etiological possibilities before dening the treatment. The treatment must
be focused on the cause and since there is a wide range of possible causes, halitosis needs a multidisciplinary
approach.
KEYWORDS
Dimethyl sulde; Halitosis; Hydrogen sulde; Odorants; Oral hygiene.
RESUMO
Objetivo: Halitose é um cheiro ofensivo expelido pela cavidade bucal e pela cavidade nasal e percebido pelo
indivíduo e/ou pelas outras pessoas. A halitose é um sintoma que impacta diretamente aspectos sociais da vida
de um indivíduo e pode ser um sinal de alguma desordem sistêmica em alguns casos. Material e Métodos: Uma
busca foi feita na literatura para reunir os principais aspectos da halitose e conduzir uma revisão sobre as principais
características necessárias à prática clínica quando um prossional lida com um paciente com a queixa de halitose.
Resultados: A informação disponível foi sumarizada e discutida com foco naquilo que um clínico deve estar
atento quando lida com um paciente com a queixa de halitose presente. Conclusão: A halitose é um sintoma
prevalente que afeta aproximadamente 25% dos indivíduos. Sua classicação leva em consideração a origem dos
compostos que produzem o mau hálito. O diagnóstico deve levar em conta as várias etiologias possíveis antes
de denir um tratamento. O tratamento deve ser focado na causa e, como há uma ampla variedade de possíveis
causas, a halitose é um sintoma que precisa de uma abordagem multidisciplinar.
PALAVRAS-CHAVE
Dimetil sulfeto; Halitose; Sulfeto de hidrogênio; Odorantes; Higiene bucal.
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Halitosis: a conceptual, etiologic and therapeutic approach
INTRODUCTION
Breath is the odor of the air exhaled
through the mouth during exhalation. When
this odor is unpleasant, it is denominated as bad
breath or halitosis [1,2]. Halitosis is described
as an unpleasant or offensive odor emanated
by the oral and nasal cavities and perceived
by the individual and/or by other people [3].
In most cases, its origin is related to oral cavity
conditions [4-6]. However, though seldom, it
can be associated with systemic pathological
conditions [7].
Halitosis is frequently associated to
important social, psychological and emotional
aspects, and sometimes it is an obstacle to
social interactions, creating discomfort and
embarrassment [8,9]. Individuals affected by
halitosis are more anxious and depressed than
those who are not affected, and consequently,
they have lower self-esteem and a decrease in
their quality of life and social interactions [10].
A recent study showed that more than half
of individuals with halitosis complaint feel
uncomfortable when they are close to another
person, hesitate to talk to other people and
report that their social and professional life was
negatively affected by bad breath [11].
Individuals affected by halitosis rarely look
for a professional to solve the problem [12,13].
Despite the low rate of reports, studies show
that halitosis is a prevalent condition, estimating
that 10% to 30% of individuals have bad
breath [14,15]. Therefore, halitosis prevalence on
the population is underestimated [16,17] due to
a lack of knowledge by patients about their own
condition or embarrassment about reporting it.
As halitosis is a symptom, it reects an intra or
extraoral disorder and might be related to serious
health conditions [1]. Health professionals,
especially dentists, must know about the etiology,
diagnosis and therapeutic approach for these
individuals, in order to be able to identify the
symptom and provide the necessary support,
referring the patient to proper treatment of the
causes.
This review makes a conceptual, etiologic
and therapeutic approach of halitosis, aiming
to understand its epidemiology and population
impact, its main causes and diagnostic means,
to guide the dentist to the adequate treatment
options for each specic case.
METHODOLOGY
Different searches were conducted in
PubMed to identify studies discussing different
aspects of halitosis: the classification and
diagnosis, the etiology and the treatment.
For each aspect of interest, a search strategy
was elaborated. To discuss classication and
diagnosis of halitosis the following MeSH terms
and free terms were combined:
halitosis AND
(classification OR “delusional halitosis” OR
halitophobia OR diagnosis OR organoleptic
OR OralChroma OR “gas chromatography” OR
Halimeter OR “sulde monitors” OR “self-report”
OR “volatile sulfur compounds” OR prevalence)
.
In order to retrieve articles discussing the
etiology of halitosis considering its different
sources, the following keywords were combined:
halitosis AND (tongue coating OR periodontitis
OR “periodontal diseases” OR xerostomia
OR “dry mouth” OR oral hygiene OR “dental
flossing” OR toothbrushing OR “respiratory
disorders” OR “gastrointestinal disorders” OR
“gastroesophageal reux disease” OR GERD OR
reux OR “Helicobacter pylori” OR “H. pylori”
OR “inammatory bowel diseases” OR “Crohn’s
disease” OR “ulcerative colitis” OR “diabetes
mellitus” OR hepatitis OR “renal failure” OR
“kidney failure” OR infections OR smoking OR
smoker OR tobacco OR alcohol OR alcoholism
OR medication OR drugs OR medicine)
. Lastly,
to discuss the treatment of halitosis, another
search was performed using the terms
halitosis
AND (treatment OR mouthwash OR toothpaste)
.
A manual search within the reference list of the
included studies were also performed to identify
studies that the electronic search might have
missed.
The search was conducted without restriction
of date and language. This review included
primary studies, systematic reviews and other
reviews bringing relevant insights to the eld.
Book chapters, letters, personal opinions, meeting
abstracts and case reports were excluded.
Classication
Halitosis is normally classied in two main
categories: genuine halitosis and delusional
halitosis, according to the classication adopted
by the
International Society for Breath Odor
Research
(ISBOR), based on the origin of the
compounds responsible for the malodor [18].
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Genuine halitosis is the obvious malodor,
exhaled by the mouth, in a level above the
level considered as socially acceptable. Genuine
halitosis can be physiological or pathological.
Physiological halitosis is the morning bad breath,
which occurs during the night due to reduction
of salivary flow rate and increasing of the
putrefaction processes by the microorganisms
inside the oral cavity [19]. This is a transient
malodor, that disappears when eating or brushing
the teeth [20,21]. Physiological halitosis can
also be caused by some specific food capable
of modifying the smell of the exhaled air and
for long starvation periods. As the morning
bad breath, this type of halitosis is transient,
therefore, physiological [22].
Pathological halitosis is the true bad breath,
which occurs as a symptom associated to various
disorders. Pathological halitosis is chronic and
classied according to its origin in intraoral or
extraoral halitosis [19]. In intraoral halitosis, the
malodor originates from factors and processes
that occur inside the mouth. In extraoral halitosis,
the origin of the bad breath might be the
respiratory tract, the gastrointestinal tract,
the liver, kidneys or metabolic disorders [23].
Extraoral halitosis is divided into bloodborne
halitosis or non-bloodborne halitosis, considering
how the molecules of malodorous gases leave
the site where they are produced and reach the
oral cavity, from where they are exhaled to the
exterior as bad breath [24,25].
There are two situations in which halitosis
might have a psychological origin. One situation,
classied as pseudo halitosis, happens when the
individual reports a bad breath, but this cannot be
clinically diagnosed. The other situation, dened
as halitophobia, happens when the individual has
an excessive fear of having bad breath, even after
the treatment and a negative diagnosis made by
a professional [26]. Both situations are dened
on the literature as delusional halitosis [27,28].
The classication of the halitosis categories can
be found on Figure 1.
Etiologic mechanisms
Halitosis is not a disease, but a sign that
there is a disorder in the body, characterizing
a symptom. The causes of bad breath are
multifactorial. However, studies show that
approximately 80% of bad breath is originated
on the mouth [4,5,29,30].
Some intraoral sites favor the accumulation
of bacteria and the putrefaction of organic
compounds. The humidity and temperature inside
the mouth facilitate the microbial degradation of
amino acids containing sulfur, such as cystine,
cysteine and methionine. The unpleasant
odors usually originate from these sites [31].
Figure 1 - Halitosis classification according to the origin of VSCs. Halitosis is divided in two main categories: genuine halitosis and delusional
halitosis. Delusional halitosis can be defined as pseudohalitosis or halitophobia. Genuine halitosis can be physiological or pathological.
Pathological halitosis can be of intra or extra oral origin, and extra oral halitosis can be divided into blood borne and non blood borne halitosis.
Adapted from Izidoroetal. [18].
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Proteolytic Gram-negative bacteria are capable
of degrading these organic compounds and
metabolizing such amino acids, releasing gaseous
molecules containing sulfur, called volatile sulfur
compounds (VSCs) [6,32]. Almost 90% of the
composition of the malodor exhaled by the oral
cavity is composed by hydrogen sulde (HS),
dimethyl sulde (DMS) and methyl mercaptan
(MM), released on this process [18]. Other
VSCs molecules can be found, but in very lower
concentrations [25].
Extraoral pathological halitosis is also
mostly caused by the presence of VSCs in the
exhaled air. In bloodborne extraoral halitosis,
VSCs produced in distant sites are adsorbed into
the blood and circulate to the lungs. In the lungs
they are released during gaseous exchanges and
volatilized with the exhaled air. The main VSCs
responsible for the malodor in these cases is DMS.
MM and SH immediately reacts with the blood and
undergo irreversible oxidization, preventing them
from reaching lungs. DMS is a neutral molecule,
stable on the blood and can be transported to the
alveolus in an intact form [25]. Hepatic, renal,
intestinal and metabolic pathologies can give
rise to bloodborne halitosis. Non-bloodborne
extraoral halitosis is originated mainly on the
superior and inferior respiratory tract, and a
small part has gastric origin. Its occurrence is
explained by the anatomical proximity between
the site where the VSCs are produced and the oral
cavity, allowing VSCs to reach the mouth and to
be exhaled within the air [24,25]. A scheme for
bloodborne halitosis can be found on Figure 2.
Despite the importance of VSCs on the
halitosis etiology, its absence does not imply on
the absence of halitosis. Approximately 15% of
halitosis cases can be caused by other volatile
organic compounds (VOCs), without sulfur on
their composition. It is the case of extraoral
bloodborne halitosis caused by renal disorders
and Diabetes Mellitus, where the VOCs with a
structure different from that of VSCs are adsorbed
into the blood and released by the lungs, being
exhaled through the mouth [25].
Epidemiological aspects
Halitosis is a prevalent condition in the
population. However, literature brings inconsistent
data about its prevalence, possibly as a result from
different diagnostic methods and different criteria
to dene and measure bad breath on the individuals
in different studies [33]. Different studies suggest
that the variation on the prevalence of halitosis is
from approximately 2.4% to 78% [16,17,33-36],
and according to a systematic review this prevalence
would be of 31.8% [36]. Despite the fact that
Figure 2 - Bloodborne halitosis. VSCs are produced in sites far from the mouth, such as liver, kidneys, intestines or pancreas, and transported
through the blood to the lungs. Then, they are exhaled withing the air as bad breath. Figure inspired by the BioRender.com element designs.
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there is no consensus on the literature regarding
the prevalence rate of halitosis or which gender is
more affected [33,37], if we consider prevalence
rates available on the literature, we could estimate
that at least one out of every four people has
halitosis [38,39] and that it is more common and
intense in elderly people [40]. Halitosis prevalence
increases with age increasing. For elderly people,
halitosis is more severe and common. It has been
reported that above the age of 65, the prevalence
is twice the prevalence that of individuals in their
twenties [12].
Furthermore, the perception of bad breath
varies among different cultures [41,42].
For example, the self-reported prevalence of
halitosis on individuals above 16 years-old in the
Netherlands was 43.7% [43], while in individuals
above 15 years-old in France was 22% [44]. In an
infant population, with an average of 12 years-
old, the reported prevalence was 37.6% [37].
In Brazil, the self-reported halitosis represented
a prevalence of 16.6% in adults [45].
The substantial variation in halitosis
prevalence is a consequence of methodological
variations in research, including the lack of well-
dened diagnostic criteria and the use of different
methods and instruments [46]. Some studies use the
self-report as a diagnostic measurement [17,35],
while others use the organoleptic method [5,16]
or automatic method as the sulde monitors or
gas chromatography [37]. In a cross-sectional
study from New-Zealand, different prevalence
rates were found for the same population with
different diagnostic methods: 31.2% for sulde
monitors, 14.3% and 25.6% self-report [47]. These
differences demonstrate that the prevalence of
halitosis can vary depending on the classication
adopted and the diagnostic method applied [46].
Diagnosis
Considering that halitosis has a multifactorial
feature [34], in addition to the intraoral clinical
examination, the analysis of the individual’s
medical and dental history should be included
as a protocol for every person complaining of
bad breath. In some situations, considering that
systemic diseases might be associated to halitosis,
a medical evaluation might be necessary.
At the rst moment, evaluating the presence
or absence of genuine halitosis is essential, as the
majority of patients are not good judges of their
own breath [48]. This diagnosis can be made
through tests capable of detecting malodor or
the involved gases. The main available methods
include the organoleptic method, the sulfide
quantication, the gas chromatography [27] and
patient self-report [45].
The organoleptic method is a simple exam
and considered as the gold standard for the
diagnosis of halitosis on the clinical practice [5],
once it reects the presence of an unpleasant odor
detected by an observer [49]. The organoleptic
measurement is a sensorial test based on the
perception of bad breath by an examiner properly
trained and calibrated. As this method does not
need sophisticated equipment or technique, this
methodology is more accessible and practical for
clinical use. The technique consists in classifying
the odor exhaled through the nose and the mouth
using a scoring system that measures the intensity
of malodor [50].
Once it depends on the olfactory accuracy
from the examiner, the organoleptic method
is considered subjective and a good qualitative
method, but without quantitative accuracy [51],
and might be uncomfortable for the examiner and
the examined individual [49]. It is recommended
that the patients avoid consuming strongly scented
foods before the appointment test, for at least
24h. The patient and the examiner should refrain
from drinking coffee, tea, juice, smoke and using
cosmetics and perfume [27]. The examiner instructs
the patient to inhale through the nose and exhale
slowly through the mouth, while the examiner
stands at a distance of approximately 20 cm from
the patient and classies the exhaled odor [50,51].
This classication is made in a scale from 0 to 5:
0) undetectable odor; 1) questionable odor, barely
detectable; 2) discrete odor, exceeds the threshold
for recognizing malodor; 3) malodor detected; 4)
strong malodor; 5) very strong malodor. Patient
classied on score 2 and above has clinical halitosis
(clinically perceived). On scores 4 and 5, the patient
is classied as severe halitosis [49].
Sulfide monitors (Halimeter®) are
electrochemical devices that measure the level
of VSCs in expired air [52]. It is a non-selective
volumetric method that only measures the total
volume of VSCs in the sample [23], and it is
not able to distinguish the gases HS, MM and
DMS [20]. This is a good diagnostic method for the
presence or absence of halitosis caused by VSCs.
But for extraoral halitosis caused by VOCs other
than the three above mentioned, this method is not
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recommended [22,53,54]. Halimeter is more sensible
to HS and have a lower response for MM and DMS.
When Halimeter is used, the DMS concentrations
are underestimated in almost 70% [55].
Gas chromatography has the ability to
quantify and distinguish the different VSC present
on the breath, allowing the differentiation between
intraoral and extraoral halitosis [53]. The most
known device of gas chromatography is the
compact OralChroma®, which is able to provide a
quick evaluation of the VSC, capable of measuring
and distinguishing the key compounds of bad
breath (DMS, MM e SH) and distinguish halitosis
subtypes based on their origin [56]. Despite
having a high sensitivity and accuracy being able
to measure extremely low concentrations of VSC,
the gas chromatography is an expensive device
which requires trained professionals to perform
the exam. This makes it less appropriate to the
routine diagnosis [23]. Furthermore, the accuracy
and precision of this device depends on constant
update of its software and on its calibration [56].
Diagnostic tests should be applied to evaluate
the exhaled air through the mouth and the nose
separately, aiming to distinguish intraoral from
extraoral halitosis. Patients with intraoral halitosis
will have the malodor exhaled only through the
mouth, while patients with extraoral halitosis will
have the bad breath exhaled through mouth and
nose [54]. If a malodor cannot be identied during
the exams, these should be repeated after two or
three distinct days and if their absence is persistent,
a pseudohalitosis diagnosis should be considered.
At a later stage, the professional’s role is
to associate the information obtained during
anamnesis with the results of the sensitive
and objective tests conducted. Halitosis has a
predominantly clinical diagnosis which is based
on the patient’s medical and dental history.
A well-dened diagnosis is determinant for future
treatments. When the professional suspects a
systemic cause, it is important to assemble a
multidisciplinary team to conduct this investigation,
which may require additional tests [45].
Self-reporting has been used in various health
specialties to understand the prevalence and
risk factors of some systemic conditions [45].
Halitosis self-report has a good accuracy with the
clinical measures for severe halitosis (75%), but
a lower accuracy for clinical halitosis (50%) [46].
Nevertheless, it shows a good general correspondence
with the organoleptic method [57]. The self-report
is a good sorting method [46]. At the population
level, it has the ability to detect potential problems
in groups of affected individuals, reducing the costs
with tests and the time employed on research. In a
research scenario it would be impossible for the
researcher to individually test each participant [45].
At the individual level, it has the ability to detect
individuals with halitosis complaints and to guide
them to the correct treatment.
Causes
Oral cavity is responsible for 85% to 90%
of halitosis cases. The oral environment is humid
and has an ideal temperature for growth of many
microorganisms capable of metabolizing aminoacids
and producing VSCs [18].
In vitro,
many oral
bacteria produce VSCs, especially MM and HS [49].
The main intraoral factors capable of causing
halitosis are the tongue coating, periodontitis,
bad oral hygiene and the presence of infections,
caries and mucosal wounds [31]. Especially in a
post-pandemic reality, where people spent several
months without proper dental assistance due to
fear of contraction of COVID-19, intraoral factors
should be carefully evaluated [58].
Tongue coating
Tongue is the main site of malodor production
and bad breath is associated with the presence of
bacteria on the dorsum of the tongue, mostly
Gram negative [49,59]. The supercial anatomy
of the tongue dorsum with papilae and ssures is a
retentive structure for the microorganisms [60,61],
and an anatomic niche, where the environment
relatively inaccessible to saliva and oxygen favors
the growth of an anaerobic microbiota [60].
This microbiota adheres to the coating
on the dorsum of the tongue that comprises
desquamated epithelial cells, blood cells,
nutrients and bacteria, and this composition
can change from one individual to another [60].
Data on the literature shows that there is not
a specific specie responsible for the malodor,
in fact what happens is an abnormal growth
of many bacteria, especially the proteolytic
ones [49,62]. Microorganisms, especially Gram
negative, are able to produce VSCs using food
debris and desquamated epithelial cells from
tongue coating [18]. The dorsum of the tongue
is responsible for almost 60% of the VSCs
production [63], and the area posterior to the
circumvallate papilla is the region with the
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greatest capacity to harbor Gram negative bacteria
and produce VSCs with greater intensity [18].
Periodontitis
There is a positive correlation between VSCs
concentration and periodontitis severity, once
periodontal pathogens (mainly
Porphyromonas
gingivalis)
are capable of producing these
compounds [3]. Subgingival biolm is primarily
composed by Gram-negative anaerobic
microorganisms, with a proteolytic nature and
ability to produce VSCs [18].
It was demonstrated that approximately
82% of the patients diagnosed with periodontitis
presented halitosis, and that periodontitis patients
had a greater risk of having halitosis when
compared to patients without periodontitis [3].
A positive correlation between halitosis and
periodontal clinical parameters, especially probing
pocket depth higher than 4 mm, was demonstrated.
As PPD increases, the VSCs concentration on
breath also increases [6,27,63-65]. Furthermore,
on periodontitis patients there is a trend to an
increased volume of tongue coating, contributing
to the increase of malodor [63].
Bad oral hygiene
Tooth brushing is an important factor on
the reduction of severe halitosis risk, because it
reduces the substrate and the bacterial load on the
mouth [17]. A lower oral hygiene index and less
adherence to the use of dental oss are associated to
a higher severity of halitosis [46]. It is also possible
to observe that lower education level and higher age
are associated to worse oral hygiene index [66,67],
directly contributing to halitosis occurrence.
Infections and intraoral wounds
All factors creating food or plaque
retention, and allowing the bacterial aminoacids
putrefaction, could cause halitosis [18]. Tongue
coating, periodontitis and bad oral hygiene are
the main intraoral factors associated to halitosis,
but less frequent causes of halitosis include caries,
ulcers, food impaction, nocturnal use of prothesis
or bad prothesis hygiene, neoplastic wounds and
a low salivary rate [23].
Respiratory disorders
Due to the proximity between the oral cavity
and the airways, there is a signicant increase
in VSCs in exhaled breath during episodes of
pathologic airways disorders [23].
Approximately 3% of extraoral halitosis
cases are originated on the tonsils, which
accumulate a white material, called caseum,
on their crypts [46,65,68]. The crypts system is
an ideal environment to the anaerobic bacterial
activity [68]. Caseums have a morphology similar
to the dental biolm, with desquamated epithelial
cells, keratin and food debris [69] colonized
by anaerobic bacteria that produces VSCs, very
similar to the tongue coating microbiota [68].
Caseum presence means a 10-fold increased
risk of changes in the VSCs exhaled pattern, and
consequently, on halitosis. The caseum chronic
formation is frequently related to halitosis and
77% of people who have caseum also have
halitosis. The main cause of bad breath in these
individuals is the decomposition of organic debris
forming caseum by proteolytic bacteria [69].
Bacterial sinusitis is the main cause of
malodor exhaled though nasal cavity. It presents a
characteristic malodor, especially when a purulent
mucus is present. Bacteria involved in mucus
production are capable of directly producing VSCs.
This purulent material, due to the anatomical
proximity, drips from the nasopharynx to the
oropharynx and may reach the base of the tongue.
This phenomenon is called postnasal dripping and
promotes an increase in the number of bacteria
that form the existing tongue coating, as well as an
increase in the nutrients utilized by these bacteria
in their metabolism. This mechanism increases the
production of VSCs [18].
Other respiratory tract conditions are less
frequently associated to halitosis, as pulmonary
abscess, necrotizing pneumonia, emphysema,
pulmonary carcinoma, bronchiectasis and
tuberculosis [18].
Gastrointestinal disorders
Despite the recurrent halitosis complaint
among patients with gastrointestinal disorders,
these represent the origin of only 0.5% of
halitosis cases [18]. Biological plausibility of the
involvement of gastrointestinal disorders with
halitosis can be explained through two distinct
mechanisms: a) the release of VSC produced in the
stomach through the esophagus; b) the adsorption
of VSC from gastrointestinal tract (GTI) to the
bloodstream and subsequently diffusion on the
lungs and release with the exhaled air [23].
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Helicobacter pylori
is a bacterium that
demonstrated ability to produce MM and HS
in
vitro
, what suggests its direct involvement on
halitosis development. These VSC are absorbed,
carried by the blood to the lungs where they are
diffused and exhaled within the air [70]. It was
demonstrated that the
H. pylori
eradication
results in halitosis resolution [71-74].
Gastroesophageal reflux disease is
characterized by the retrograde flux of gastric
contents from stomach to esophagus, bringing
unpleasant symptoms, halitosis among them [75].
Gastroesophageal reux may cause halitosis through
3 distinct mechanisms: 1) postnasal dripping of the
stomach contents, that reach the nasopharynx
through the esophagus, irritates the nasopharynx
mucosa and leads to the mucus dripping on the
tongue basis, increasing the tongue coating volume;
2) altered function of the esophagus sphincter that
could allow the gastric contents to return to the
mouth; 3) direct damage of the peptic acid on the
supraesophageal mucosa [76].
Inflammatory bowel diseases (IBD) are
chronic conditions that affects the colon and the
small intestine. Crohn’s disease and the ulcerative
colitis are part of this group of diseases [77].
Studies show a signicant prevalence of halitosis
among the patients carrying IBD [78] and this
prevalence increases with the severity of the IBD
clinical condition [79].
Diabetes mellitus
Individuals with type II diabetes mellitus
(T2DM) may present a characteristic breath
malodor, described as a “sweet and fruity
smell” [18]. On diabetic ketoacidosis, the
decarboxylation of acetyl coenzyme A in starvation
situations produces an excess of ketonic bodies
which circulate through the bloodstream until
reaching the lungs where they are volatilized
within the exhaled air, producing a breath with
the characteristic diabetes ketoacidosis sweet
smell [23].
Hepatic disorders
Bad breath caused by hepatic conditions is
denominated
foetor hepaticus
and is related to
DMS volatilized within the pulmonary air. DMS is
originated on the intestines, however, the altered
hepatic function results in higher concentration
of this compound in the bloodstream, once the
liver is unable to eliminate it. Consequently, DMS
concentration is elevated within the exhaled air
through the mouth and through the nose [25].
Renal disorders
Renal disorders are associated with an
ammoniac breath, called
uremic fetor.
Patients with
renal failure have elevated levels of ammonia, urea,
isoprene and other compounds, once the kidneys
are not able to eliminate them [23]. The malodor
is typically uremic and associated to hyposalivation,
common in patients with renal disorders [18].
Smoking
Cigarette smoke contains VSCs that can be
detected by a sulde monitor [18]. However, this
concentration depends directly on the period of
time that has passed since the individual’s last
cigarette [66]. Furthermore, when oral hygiene
and halitosis levels between smokers and non-
smokers was compared, it was observed a worse
oral hygiene and a higher occurrence of severe
halitosis among smokers [66].
The decrease of salivary ow rate in smokers
favors the deposits accumulation, especially on
the tongue, increasing the tongue coating which
is one of the main factors causing intraoral
halitosis [18,66].
Halitosis in smokers is also closely related
to periodontal issues since smoking is one of
the main risk factors for the progression of
periodontitis and destruction of the supporting
structures [66]. Cigarette smoke can change the
subgengival ecosystem, increasing the absolute
number of proteolytic Gram-negative bacteria,
periodontal pathogens, directly producers of
VSCs [18]. It also changes important cellular and
endothelial functions promoting the progression
of periodontitis and tissue destruction [80].
Alcoholism
Alcohol consumption is a risk factor for
halitosis because the alcohol oxidation in the
mouth and the liver produces acetaldehyde
and other volatile products with a strong odor.
Furthermore, alcohol intake is associated to a
lower salivary ow rate and xerostomia, both
risk factors for halitosis [18].
Xerostomia
Saliva is responsible for promoting the
cleanliness of mouth tissues, removing debris
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Viana KSS et al.
Halitosis: a conceptual, etiologic and therapeutic approach
Viana KSS et al.
Halitosis: a conceptual, etiologic and therapeutic approach
and microorganisms. This is the reason why
hyposalivation may promote anaerobic bacterial
growth and the putrefaction of debris that remains
on the oral cavity after food intake. This process
increases the production of VSCs in the mouth [18].
Medicines
The use of medicines is a common cause
of hyposalivation [18], and this is the most
common adverse effect of medicines affecting the
oral cavity [81]. In individuals with a complaint
of xerostomia, the main cause was the use of
medicines [82,83].
In a recent systematic review, the main
medicines capable of causing halitosis were
evaluated. Cysteamine, used to the nephropathic
cystinosis treatment or Huntington’s disease,
was the halitosis most associated medicine.
Other medicines associated were anticholinergic
oxybutynin and glycopyrrolate. Less frequently,
the antidepressant imipramine, antihistamine and
steroids. Medicines for neoplasia treatment was also
associated to halitosis, as the PX-12 chemotherapy
and with a lower intensity silibinin. A study
demonstrated that cysteamine and PX-12 caused
halitosis in 100% of the individuals [81].
Dietary intake
There are some foods with a high amount
of sulfur. These foods, when suffer degradation
on the intestines trigger a process similar to what
happens when DMS is excessively produced on
the intestine [25]. Onion and garlic are foods
associated with this phenomenon. Garlic releases
allyl methyl sulfide and onion releases methyl
propyl sulde [82]. The intake of these can increase
the DMS concentration within the exhaled air [25].
Treatment
The rst step on halitosis management is a
detailed examination of the patient to identify the
cause and drive the treatment to the identied
causes [70]. An accurate diagnosis is essential to
solve the issue.
To intraoral halitosis, the course of the
treatment must be determined after a detailed
intraoral examination, including teeth and soft
tissues [18]. When the identified cause is the
tongue coating, periodontitis or caries, the primary
way to reduce intraoral halitosis is to eliminate
the bacteria synthetizing the chemical compounds
responsible for malodor [46,84] through a
mechanical reduction of the microorganisms [18].
Patients must receive guidance about brushing their
teeth, mechanical cleanliness of the tongue [84]
and ossing or interdental cleaning devices such as
interdental brushes [15,85-87]. Even though oral
hygiene practices are a daily issue, some people
have a lack of proper knowledge about the correct
execution and frequency of such practices [88].
These hygiene habits must be incorporated on
the individual’s oral hygiene routine [89] and
should be individualized, considering that some
individuals may have some risk factor for plaque
retention, such as orthodontic devices [90].
When the origin of halitosis is identied as
periodontitis, the patient must receive the proper
periodontal treatment and follow up, referred
to a specialist able to conduct this therapy. Oral
hygiene guidance previously mentioned are
fundamental for patients with periodontitis,
once the treatment’s success depends on the
cooperation of the patient and their adherence
to a daily routine of oral hygiene. When necrosis
and pericoronitis are identied, treatment must
be performed aiming to solve these problems and
re-establish the health status in the mouth [89].
As a complement to the treatment of
intraoral causes, we can use some oral hygiene
products which can reduce microorganisms
or have the ability to mask the malodor.
There are mouthwashes and toothpastes with
antiseptic activity [87] and there are also
products with oxidizing potential available [46],
which will perform a chemical reduction of
the microorganisms and VSC neutralization
respectively [18]. Besides these, there are
products acting only by masking the malodor [62].
Antiseptic products available for
use are chlorhexidine, essential oils and
cetylpyridinium [18,62]. They have a
demonstrated effect on the reduction of the
production of VSCs through the reduction of the
microbial load on the mouth cavity, performed
by the antibacterial effect [62,91].
Chlorhexidine is nowadays considered
as the gold standard of the antiseptics and
an excellent supporting product on halitosis
treatment [18]. Chlorhexidine containing
mouthwashes show success on the reduction of
the supragingival plaque antimicrobial activity,
as well as on the tongue coating microbial
load [92]. However, chlorhexidine is associated
10
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Viana KSS et al.
Halitosis: a conceptual, etiologic and therapeutic approach
Viana KSS et al.
Halitosis: a conceptual, etiologic and therapeutic approach
to teeth and tongue staining as well as taste
changing, which limits its use for extended
periods of time [12]. Cetylpyridinium is a
quaternary compound that has bacteriostatic
effect on the VSC producing bacteria [93],
reducing the intensity of the malodor. However,
cetylpyridinium is unstable in solution and
has a small effect on dental biolm reduction,
especially when compared to chlorhexidine,
which performs a greater effect on biolm [94].
Mouthwashes based on essential oils are
used for their reported ability of rupturing
the bacterial cell membranes. However,
literature is scarce when we search for their
ability on reducing VSCs. Essential oils may
act masking the malodor due to its naturally
strong smell [62].
Zinc containing toothpaste are a good auxiliary
method on halitosis treatment, due to their
demonstrated ability to reduce VSC [70]. Zinc
is a metal ion and interacts with sulfur on VSC
precursors, neutralizing these molecules and
reducing the bad breath intensity [91].
When the individual presents some associated
cause as cigarette, alcohol and dietary habits that
may contribute to the bad breath occurrence,
we must guide the patient and when possible,
try to institute a habit modication [89]. When
halitosis is associated to the use of medicines or
a systemic condition, the patient must be referred
to the doctor to the proper treatment or replacing
the medicine when possible.
Patients with delusional halitosis should be
properly guided. Oral hygiene instruction and
the explanation about halitosis causes and risk
factors are valid for every patient. Sometimes
halitophobic patients are difcult to manage and
should be addressed with discretion, normally
with a carefully referral to a physician [49]. A tree
of decision regarding the clinical assessment of
the patient is represented on gure 3, in order to
guide the steps for correct diagnosis.
Figure 3 - Tree of decisions suggesting the steps a professional must follow to identify the correct cause of halitosis before deciding the
treatment. Information adapted from the paper from Campisietal. [89] and Seemanetal. [95].
11
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Viana KSS et al.
Halitosis: a conceptual, etiologic and therapeutic approach
Viana KSS et al.
Halitosis: a conceptual, etiologic and therapeutic approach
CONCLUSION
Halitosis is a prevalent health issue and
may affect the social life of people carrying this
symptom. Halitosis is mostly caused by oral health
issues, mainly tongue coating accumulation
and periodontitis. But halitosis might also
be a symptom of a wide range of systemic
conditions, including respiratory, renal, hepatic
and endocrine disorders. A correct diagnosis and
a multiprofessional approach are fundamental
for the clinical management and the treatment
of this condition, aiming a better prognostic for
the individual.
Acknowledgements
Conselho Nacional de Desenvolvimento
Científico e Tecnológico (CNPq, Ministério
da Educação, Brasil) and Coordenação de
Aperfeiçoamento de Pessoal de Nível Superior -
Brasil (CAPES) - Finance Code 001.
Author’s Contributions
KSSV, EAFS, RPEL, LOMC: Conceptualization,
Methodology, Writing – Review & Editing. KSSV:
Formal Analysis, Investigation, Data Curation.
KSSV, RPEL, LOMC: Writing – Original Draft
Preparation.
Conict of Interest
No conicts of interest declared concerning
the publication of this article.
Funding
This research did not receive any specic
grant from funding agencies in the public,
commercial, or not-for-prot sectors.
Regulatory Statement
Not applicable considering this is a review
paper.
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Karolina Skarlet Silva Viana
(Corresponding address)
Universidade Federal de Minas Gerais, Faculdade de Odontologia,
Departamento de Clínica, Patologia e Cirurgia Odontológicas. Belo
Horizonte, Brazil.
Email: karolinasilvaviana@gmail.com
Date submitted: 2023 Sept 15
Accept submission: 2024 Jan 24
