Periodontics

Review Article
Periodontics

Halitosis: an overview of epidemiology,

etiology and clinical management

Cassiano Kuchenbecker Rösing(a) Abstract: Halitosis is an unpleasant condition that causes social re-
Walter Loesche(b) straint. Studies worldwide indicate a high prevalence of moderate halito-
sis, whereas severe cases are restricted to around 5% of the populations.

Department of Periodontology, Dental
(a) The etiological chain of halitosis relates to the presence of odoriferous
School, Universidade Federal do Rio substances in exhaled air, especially the volatile sulphur compounds
Grande do Sul, Porto Alegre, RS, Brazil.
(VSC) produced by bacteria. The organoleptic diagnosis is the gold stan-

Department of Microbiology and
(b)
dard and clinical management includes oral approaches, especially peri-
Immunology, School of Dentistry, University
odontal treatment and oral hygiene instructions, including the tongue.
of Michigan, Ann Arbor, MI, USA.
When oral strategies are not successful, referral to physicians is warrant-
ed.

Descriptors: Halitosis; Epidemiology; Microbiology; Review.

Introduction
Halitosis is defined as breath that is offensive to others, caused by a
variety of reasons including but not limited to periodontal disease, bacte-
rial coating of tongue, systemic disorders and different types of food.1 It
is one of the most frequent claims from patients to the dentist. 2
After the decline in the prevalence of oral diseases of major preva-
lence, Dentistry has given it a closer attention, which should not be con-
sidered a cosmetic problem. However, science behind the understand-
ing of halitosis is weak. Several clinical approaches are based strictly on
opinions. The present review will focus on different aspects of halitosis,
trying to demonstrate the most appropriate evidence to support the ap-
proach for its management.

Epidemiology
Declaration of Interests: The authors Descriptive studies
certify that they have no commercial or
associative interest that represents a conflict The prevalence of halitosis has been studied in groups of individu-
of interest in connection with the manuscript. als found in different parts of the world in convenience samples. Dif-
ferent assessments and cut-off points are presented. Therefore, precise
estimates of the prevalence of halitosis are not possible to obtain. Table
Corresponding author:
Cassiano Kuchenbecker Rösing 1 describes descriptive epidemiological studies that document the preva-
E-mail: [email protected] lence of halitosis. They indicate that moderate chronic halitosis affects
approximately one third of the groups, whereas severe halitosis may in-
volve less than 5% of the population. It is clear that halitosis is a preva-
lent problem, and that the dental profession needs to take its responsibil-
Received for publication on Jul 10, 2011
Accepted for publication on Sep 01, 2011 ity in managing it.

466 Braz Oral Res. 2011 Sep-Oct;25(5):466-71

 Rösing CK, Loesche W

Table 1 - Summary of descriptive epidemiological studies concerning halitosis.

Author/year Location N Sampling procedure Halitosis measurement Main results

2672 government
Miyazaki et al., Convenience Prevalence of moderate halitosis
Japan workers, VSC (Halimeter)
19953 sample (≥ 75 ppb) = 28%
18-64 years
Prevalence of self
Loesche et al., 270 adults, Convenience perception = 31%
USA Self-report
19964 60+ years sample Prevalence of halitosis informed
by others = 24%
Frexinos et al., 4815 individuals, Randomized, Prevalence of self-reported
France Self-report
19985 15+ years representative halitosis = 22%
Söder et al., Stockholm, 1681 adults, Randomized, Prevalence of severe halitosis
Organoleptic
20006 Sweden 30-40 years, representative (score 5) = 2.4%
Nalçaci et al., Middle Anatolia, 628 children, 7-11 Convenience Prevalence of
Organoleptic
20087 Turkey years sample halitosis = 14.5%
Prevalence of organoleptic
score 3+ = 11.5%
Self-report,
Bornstein et al., Bern, 419 adults, Randomized, Prevalence of self-reported
Organoleptic
20098 Switzerland 18-94 years 21% response halitosis = 32%
and VSC
Prevalence of
VSC 75+ ppb = 28%
Prevalence of detected chronic
626 male
Bornstein et al., Convenience Self-report and halitosis = 20%
Switzerland army recruits,
20099 sample clinical analysis Prevalence of individuals without
18-25 years
halitosis experience = 17%
Prevalence of halitosis
experience (anxiety or
Yokoyama et al., 474 senior high Convenience Self report and consciousness of the problem at
Japan
201010 school students sample clinical analysis least once) = 42%
Prevalence of clinically
detectable malodor = 39.6%

Associated factors logical factors; however, in order not to undertake

A study in Sweden6 observed that calculus, the responsibility for treatment, it would sometimes
plaque and scarce dental visits were significantly emphasize non-oral causes of halitosis. Thus, the
correlated to severe halitosis. A Japanese study3 cor- stomach was, for years, blamed for the presence of
related periodontitis and tongue coating to VSC halitosis. Several studies have demonstrated that the
scores. Also, severe periodontitis patients presented mouth is the origin for the majority of halitosis. 2,11
higher halitosis scores than non-periodontal pa- Eighty-seven percent of the incoming patients with
tients. In the two Swiss studies8,9 tongue coating was severe malodor who attended a specialized clinic for
considered an influencing factor for halitosis. Smok- halitosis in Belgium11 had their problem related to
ing and periodontal disease were associated with oral factors. Gingivitis and periodontitis accounted
higher halitosis rankings.8 Plaque and tongue coat- for approximately 60% of the oral factors and the
ing were associated with halitosis.10 In children, car- tongue accounted for the other 40%. A subsequent
ies experience and age were associated to malodor.7 report by the same group12 found oral factors as
Whether these associations are causal is not clear. responsible for halitosis in 76% of 2000 patients.
Therefore, Dentistry is responsible for diagnosing
Etiology and treating halitosis.
The etiology of halitosis has been subject to a
historical controversy. 2 Dentistry claimed oral etio-

Braz Oral Res. 2011 Sep-Oct;25(5):466-71 467

 Halitosis: an overview of epidemiology, etiology and clinical management

Periodontal inflammation treatment improves halitosis measurements. Stressful

The presence of microorganisms and the inflam- situations also might contribute to increase halito-
matory products present in gingivitis/periodontitis sis.23 In some individuals, the complaint of halitosis
are capable of producing odoriferous substances. cannot be associated with either the ability of the
Cross-sectional studies associated halitosis to the clinician to detect odors or with the demonstration
presence of either gingivitis or periodontitis.3,8,9,11,12 of VSC in the exhaled air. This paradoxical situation
In vitro and in vivo studies demonstrated the ability has been classified as halitophobia, an important
of putative periodontal pathogens and products of psychological problem that needs to be addressed
inflammation to produce volatile odoriferous com- with non-oral clinical strategies.6,12
pounds.13,14,15,16 Therefore, the presence of periodon-
tal inflammation needs to be considered in the man- Clinical management
agement of halitosis. Diagnosis
Self-assessment
Tongue coating The patient cannot smell his own breath and re-
Tongue coating, including bacteria, desquamated lies upon others for this information. It should be
cells, and saliva, among others, is one of the impor- emphasized that it is a difficult task to tell someone
tant etiological factors of halitosis. A study12 demon- that he has bad breath. Thus, results from this kind
strated that tongue coating was associated with hali- of diagnosis should be interpreted with care. In a
tosis in more than 60% of 2000 patients of a breath breath clinic,11 more than 70% of the patients were
clinic, whether present alone, or with periodontal advised by others to seek treatment, whereas in an-
inflammation. Most studies implicate the coating on other study,4 only 24% of the elders were informed
the posterior area of the tongue which is consistent that they harbored bad breath. Of course, differences
with the presence of billions of bacteria, including from study populations might explain the dispar-
anaerobes that live there and are capable of produc- ity in results (the former being from a breath clinic
ing odoriferous substances.17 and the latter from a convenience sample of older
individuals). In the study by Bornstein et al.,8 a weak
Microbiology of halitosis correlation was observed between self-reported hali-
Bacteria from the saliva,18 from plaque removed tosis and clinical measurements.
from gingivitis/periodontitis16 as well as from the
tongue17 produce odoriferous substances in vitro. In- Organoleptic measurements
tervention studies which achieve a clinically signifi- The human nose remains the “Gold Standard” in
cant effect in reducing halitosis exhibit a reduction detecting oral halitosis. The most widely used scor-
in these bacteria.19,20 Therefore, the clinical manage- ing system for ranking halitosis is the Organoleptic
ment should also include microbiological targets, Score popularized by Rosenberg and McCulloch.24
with antimicrobial approaches – mechanical and The organoleptic measurement depends on a trained
chemical – being part of the strategy. examiner that has demonstrated reliability in smell-
ing halitosis. The study by Haas et al.25 has demon-
Non-oral causes of halitosis strated good levels of reproducibility of breath odor
Ear-nose-throat problems such as tonsillitis, si- measurements, under a blind evaluation. The reason
nusitis, the presence of out-of-body material and rhi- by which the organoleptic score has been the gold
nitis were frequently associated with non-oral halito- standard for breath measurements rely on the fact
sis in breath clinics.11,12 These studies were unable to that the human nose is capable of smelling and de-
find clinically relevant associations of halitosis with fining as pleasant/unpleasant not only the VSC, but
gastroenterological problems. However, two stud- also other organic compounds that come from exha-
ies21,22 demonstrated a possible association between lation and are identified as unpleasant.2
gastrointestinal problems and halitosis and that their

468 Braz Oral Res. 2011 Sep-Oct;25(5):466-71

 Rösing CK, Loesche W

VSC monitoring on compounds other than the VSC that contribute

Objective measurements have always been de- to halitosis. Kozlovsky et al.26 found that the BANA
sired for breath assessments. The most common mal- Test correlated significantly with the organoleptic
odorants detected in halitosis are VSC which include scores obtained from the whole mouth, the tongue
hydrogen sulfide and methyl mercaptans, among and saliva, but not with the VSC. When multiple-
others. VSC monitors have been developed, such as regression analyses were performed with the organ-
the Halimeter (Interscan, Chatsworth, USA) which is oleptic scores as the dependent variable, both peak
used chairside and provides both the patient and the VSC and the BANA scores factored into the regres-
professional an idea of the breath situation. A halim- sion, yielding significant associations. They conclude
eter score of ≥ 75 ppb is recognized as clearly detect- that the “BANA test may be a simple, adjunct assay
ed halitosis. It is important to understand that VSC together with volatile sulphide determination in or-
assessment, as well as other breath diagnostic tools der to provide additional quantitative data which
are subjected to great variation, especially between contribute to the overall association with odor-judge
different hours of the day, and are strongly affected estimation.”
by confounders.16 A connection between BANA-positive bacteria
and malodor was observed in English subjects27 us-
Microbiologic tests ing BAPNA as the trypsin-like substrate. Seventy
The VSC monitors detect from 18% to 67% of eight percent of the isolates from 23 subjects with
the odors represented by the organoleptic score. This organoleptic scores ≥ 3 were BAPNA positive, com-
is because the nose is detecting odors due to many pared with 35% to 40% BAPNA positive isolates
other compounds that are in the intra-oral air as a in the subjects with organoleptic scores of 2. Sub-
result of microbial metabolism. Most of these com- sequently, Stomatococcus mucilaginus, a gram-pos-
pounds cannot be easily measured, and some such itive, facultative, cocco-bacillus, was identified as
as volatile fatty acids (butyrate, propionate, etc.), a BAPNA-positive species that is indigenous to the
diamines (cadaverine, putrescine) and other foul- tongue. This indicates that a BANA-positive reaction
smelling products can only be measured by labora- in the tongue, while indicative of halitosis, is due to
tory based assays. the presence of a bacterial flora that may be unique
An alternative strategy would be to detect in to it.
plaque, or in the tongue coating, taken from individ-
uals with halitosis, those bacteria or their enzyme(s) Treatment
that can produce these compounds. Three species Periodontal therapy
associated with periodontal disease, Treponema Periodontal treatment decreases halitosis. How-
denticola, Porphyromonas gingivalis and Tanner- ever, studies concerning response to periodontal
ella forsythia, produce both VSC and volatile fatty therapy as the only therapeutic approach for halito-
acids. The detection of these bacteria might provide sis are scarce and sometimes the effects are limited,
additional information concerning factors contrib- especially because other sources of halitosis are not
uting to the individual’s malodor. These organisms considered. A study by Silveira et al.28 demonstrated
can be detected by the presence of an enzyme(s) that a strict supragingival plaque control is able to
that degrades benzoyl-DL-arginine-naphthylamide reduce VSC and organoleptic scores in periodonti-
(BANA), a synthetic trypsin substrate, forming a col- tis patients. The studies performed in breath clinics
ored compound. We have adapted this enzyme assay have also demonstrated the ability of periodontal
to a 5- to 10-minute chairside test – the BANA Test treatment measurements to reduce halitosis.11,12
(BANAMet LLC, Ann Arbor, USA) – that detects
the presence of this enzyme(s) in plaque and tongue Approaches directed to tongue coating
samples. Several studies have demonstrated that reducing
The BANA test provides additional information bacteria on the dorsum of the tongue will dimin-

Braz Oral Res. 2011 Sep-Oct;25(5):466-71 469

 Halitosis: an overview of epidemiology, etiology and clinical management

ish halitosis. A study concluded that tongue clean- chiatrist should be included.11,12,21,22,34
ing was one of the most important approaches for
halitosis.29 A systematic review30 demonstrated the Masking agents
potential of tongue cleaning, however the evidence When it is not possible to direct the treatment ap-
was not convincing. Also, a Cochrane systematic re- proach to the cause, masking agents have been devel-
view31 demonstrated that there is a little superiority oped to decrease the odor. The use of chewing gum
of tongue scrapers as compared to brushing in re- may decrease halitosis, especially through increasing
ducing halitosis. Therefore, tongue cleansing is one salivary secretion.35 Mouthrinses containing chlorine
of the components and should never be a sole treat- dioxide and zinc salts have a substantial effect in
ment for halitosis. masking halitosis, not allowing the volatilization of
the unpleasant odor.20,35 These approaches should be
Antimicrobials only used temporarily in order to improve satisfac-
Since the presence of microorganisms from oral tion of the patient.
biofilms is responsible for producing malodor, any
type of treatment approach that has impact in the Summary and Conclusions
oral microbiota has the potential of reducing halito- The present review demonstrated that halitosis is
sis. Mouthrinses, especially chlorhexidine and cetil- a common problem impacting individuals at all ages.
pyridinium chloride have been effective in reducing The main etiological factors include bacteria in the
halitosis.20,32 In addition, the use of dentifrices has oral cavity related especially to periodontal diseases
also been studied. Triclosan containing dentifrices, and the dorsum of the tongue. Medical aspects in-
for example, have demonstrated an interesting po- clude ear-nose-throat and gastroenterological prob-
tential in reducing VSC.33 lems. Since the majority of halitosis is related to the
mouth, the dental team should lead the treatment,
Medical approaches performing dental/periodontal treatment and per-
If oral approaches are not successful in reducing/ sonalized oral hygiene instructions. Antimicrobials
eliminating halitosis, patients should be referred to a have the potential of reducing halitosis and masking
physician. If the medical causes cannot be suspected, agents should be used temporarily. The literature, es-
the first professional to be referred is the otorhino- pecially with randomized clinical trials, is scarce and
laryngologist, followed by the gastroenterologist. If additional studies are needed.
halitophobia is considered, a psychologist or phsy-

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