Halitosis: Current concepts on etiology, diagnosis and management

Halitosis: Current concepts
on etiology, diagnosis
and management
E U R J D E N T 2 0 1 6 ; 1 0 : 2 9 2 - 3 0 0 .
Journal club : 12

PROLOGUE
An unpleasant or
offensive odour
emanating from the
breath regardless of
whether the odour
originates from oral
or non-oral sources.
G Campisi, A Musciotto. Halitosis: could it be more than mere bad breath?; Intern Emerg
Med (2011) 6:315–319.

AIM
Succinctly focuses on the
development of a systematic
flow of events to come to the
best management of the
halitosis from the primary care
practitioner’s point of view.

INTRODUCTION
It was described as a clinical entity
by HOWE (1874).
Halitosis should not be confused
with the generally temporary oral
odour caused by intake of certain
foods, tobacco, or medications.
Originates from two
Latin words
◦ Halitus → breath
◦ Osis → disease
Armstrong BL, Sensat ML, Stoltenberg JL. Halitosis: A review of
current literature. J Dent Hyg 2010;84:65-74.

SYNONYM
S
Bad or foul
breath
Breath
malodour
Oral
malodour
Foetor ex-
ore
Foetor oris
Stomato
dysodia
van den Broek AM, Feenstra L, de Baat C. A review of the current literature on aetiology
and measurement methods of halitosis. J Dent 2007;35:627-35

DEFINITIONS
Halitosis is the general
term used to describe a
foul odor emanating
from the oral cavity, in
which proteolysis,
metabolic products of
the desquamating cells
and bacterial
putrefaction are
involved.
• Marita et al., 2001
Halitosis is the general
term used to describe
any disagreeable odor in
expired air, regardless of
whether the odorous
substances originate
from oral or non-oral
sources.
• -Tangerman, 2002
Halitosis is also
termed as fetor ex
ore or fetor oris. It
is a foul or
offensive odor
emanating from
the oral cavity.
• Carranza(2003)
Unpleasant odor of
the expired air
whatever the origin
may be. Oral
malodor specifically
refers to such odor
originating from the
oral cavity itself.
• Jan Lindhe(2003)
J lindhe. Clinical periodontology and implant dentistry; vol 1: 5th edition
Newman ,Takei, Carranza. Clinical periodontology ; 10th and 11th edition

DEFINITION
S
Breath malodor, defined as foul or offensive odor of expired air, may be
caused by a number of factors, both intra-oral & extra-oral (gingivitis/
periodontitis, nasal inflammation, chronic sinusitis, diabetes mellitus, liver
insufficiency etc.,) & can be linked to more serious underlying medical
problems including primary biliary cirrhosis, uremia, lung carcinoma,
decompensated liver cirrhosis & trimethylaminuria.
Quirynen, Zhao, Avontroodt et al., 2003

HISTORY
The problem of halitosis has been
reported for many years.
References were found in papyrus
manuscripts dating back to 1550
BC.
During Christianity, the devil's
supreme malignant odor smelled
of sulfur & it was presumed that
sins produced a more or less bad
smell.
Rayman S, Almas K. Halitosis among racially diverse populations: An update. Int J Dent Hyg 2008;6:2-7

A treaty in Islamic
literature from the year
850 talked about
dentistry, referring to
the treatment of fetid
breath & recommended
the use of siwak when
breath had changed or
at any time when
getting out of bed.
Buddhist monks in
Japan also
recommended teeth
brushing & tongue
scraping before the first
morning prayers.
HISTORY

HISTORY
The Hindus consider the mouth as
the body's entry door and, therefore,
insist that it be kept clean, mainly
before prayers. The ritual is not
limited to teeth brushing, but
includes scraping the tongue with a
special instrument and using
mouthwash.

EPIDEMIOLOGY
Miyazaki concluded that
there was increased
correlation between older
age and malodour with
aging resulting in greater
intensity the of odor. In
above 60 years age group
of the Turkish individuals,
the incidence was around
28%.
A recent study had
revealed a prevalence
of self-reported
halitosis among Indian
dental students ranging
from 21.7% in males to
35.3% in females.
In the general
population, halitosis
has a prevalence
ranging from 50%
in the USA to
between 6% and
23% in china,

Japan study 2,672
Individuals 6-23% of
subjects had oral
malodour (VSC) as in
expired air at some period
during the day (Miyazaki
1996).
Another study in the
United States involving
individuals older than 60
years found 24% had oral
malodour (Rosenberg
1996).
Epidemiology
The prevalence of persistent oral malodor in a Brazilian study was reported to
be 15%, was nearly three times higher in men than in women (regardless of
age) and the risk was slightly more than three times higher in people over 20
years of age compared with those aged 20 years or under, controlling for
gender .

Genuine
halitosis
Physiologic
halitosis
Pathologic
halitosis
Intraoral Extraoral
CLASSIFICATIO
N

PHYSIOLOGIC
HALITOSIS
Morning
breath
odour
Decrease
in
frequent
liquid
intake
Stagnation of saliva
and putrefaction of
entrapped food
particles and
desquamated
epithelial cells by the
accumulation of
bacteria on the
dorsum of the
tongue,

poor oral hygiene,
dental caries,
periodontal
diseases in
particular NUG,
NUP,
periodontitis,
pericoronitis,dry socket
tongue coating
oral carcinoma.
Intra oral origin
Pathologic halitosis

OTHER ORIGINS OF
HALITOSIS
The resulting breath takes on a different odor that may last
several hours
Transient oral malodor
Porter SR, Scully C. Oral malodour (halitosis). BMJ 2006;333:632-5.

• 10-20%
• gastro intestinal diseases
• infections or malignancy in respiratory tract
• Chronic sinusitis and tonsillitis
• stomach, intestine, liver or kidney affected by
systemic diseases
Extra oral origin

Maximally 10% of the oral malodor cases originate from the ears, nose and throat (ENT)
region, from which 3% finds its origin at the tonsils.
The presence of acute/chronic tonsillitis and tonsilloliths represents a 10-fold increased
risk of abnormal VSC levels due to deep tonsillar crypts formation.
Foreign bodies in the nose can become a hub for bacterial degradation and hence
produce a striking odor to the breath

Examples of
systemic
pathological
conditions
that cause
halitosis

CLASSIFICATIO
N
Delusional
halitosis
Pseudo
halitosis
Halitophobia.

Condition in which a subject believes that their breath odor is
offensive and is a cause of social nuisance, however, neither
any clinician nor any other confidant can approve
of its existence
• Monosymptomatic
• Hypochondriasis
• Imaginary halitosis
Interestingly, advertisements of oral hygiene products are responsible for the
increase in a number of patients with delusional halitosis.
IMAGINARY OR
DELUSIONAL HALITOSIS

IMAGINARY OR
•Pseudo halitosis
– Apparently healthy individuals
•Haltophobia
– exaggerated fear of having halitosis
– also referred as delusional halitosis
– considered variant of monosymptomatic hypochondrial
psychosis.
Yaegaki K, Coil JM. Genuine halitosis, pseudo-halitosis and halitophobia: classification,
diagnosis, and treatment. Compend Cont Educ Dent 2000; 21(10A):880–886

Pseudo-halitosis patients complain of
having oral malodor without actually
suffering from the problem and
eventually gets convinced of a disease
free state during diagnosis and therapy
28% of patients
complaining of bad
breath did not show
signs of bad breath
IMAGINARY OR

Halitophobia is fear of having bad breath seen in at least 0.5–1% of adult
population
Such patients need psychological
counseling and should be given
enough time during
the consultation.
IMAGINARY OR

OLFACTORY REFERENCE
SYNDROME
 Psychological disorder in which there
is a preconceived notion about one
having foul mouth breath or emits
offensive body odor.

Halitosis generally arises as a result of the bacterial
decomposition of food particles, cells, blood and
some chemical compounds of the saliva.
Moss, 1998
Etiology
Yaegaki K, Sanada K. Volatile sulphur compounds in mouth air from clinically healthy
subjects and patients with periodontal disease. J Periodontol Res 1992;27:233-8.

Volatile sulphur compounds → hydrogensulphide [H2S,
rotten egg smell], dimethyl sulphide [(CH3)2S, rotten
cabbage smell, and methyl mercaptan [CH3SH, fecal smell].
Non - sulphur containing substances → diamines
[cadaverine (cadaver smell) and putrescine (rotten meat
smell), acetone and acetaldehyde
ETIOLOGY
Yaegaki K, Sanada K. Volatile sulphur compounds in mouth air from clinically healthy
subjects and patients with periodontal disease. J Periodontol Res 1992;27:233-8.

ROLE OF VOLATILE SULPHUR COMPOUNDS
IN THE PATHOGENESIS OF HALITOSIS
MAJOR COMPOUNDS IMPLICATED IN HALITOSIS
VSC’s - Methylmercaptan, Hydrogen sulfide, dimethyl sulfide
& Dimethyl disulfide.
Polyamides - Putrescein, Cadaverine, Skatole, Indole.
Short chain FA - Butyric, Propionic, Valeric & Isovaleric acid.
Others - Acetone, Acetaldehyde, Ethanol diacyl.
Miyazaki H, Sakao S, Katoh Y, Takehara T. Correlation between volatile sulphur compounds
and certain oral health measurements in the general population. J Periodontol 1995;66:679-84

It increases the permeability of oral mucosa and crevicular epithelium. It
impairs oxygen utilization by host cells, and reacts with cellular proteins, and
interferes with collagen maturation.
It also increases the collagen solubility.
It decrease the DNA synthesis.
It increases the secretion of collagenases, prostaglandins from
fibroblasts.
VSC reduce the intracellular pH; inhibit cell growth, and
periodontal cell migration.
Miyazaki H, Sakao S, Katoh Y, Takehara T. Correlation between volatile sulphur compounds
and certain oral health measurements in the general population. J Periodontol 1995;66:679-84

Pathogenesis of oral malodor
Marawar PP, Sodhi NA, Pawar BR, Mani AM. Halitosis: A silent affliction!. Chron Young Sci 2012;3:251-7.

The role of tongue coatings in the
aetiology of oral malodour has been
extensively documented.
Tongue coatings include desquamated
epithelial cells, food debris, bacteria
and salivary proteins and provide an
ideal environment for the generation
of VSCs and other compounds that
contribute to malodour

The purulent discharge from the paranasal sinuses, seen in regurgitation
esophagitis, gets collected at the dorsum of the tongue resulting in halitosis.
Atrophic rhinitis is caused by Klebsiella ozenae, which inhibits the self-cleaning
property of nasal mucosa. Acute pharyngitis and sinusitis, caused by streptococcal
species, are also responsible for producing halitosis.
Carcinoma of the larynx, nasopharyngeal abscess, and lower respiratory tract
infections such as bronchiectasis, chronic bronchitis, lung abscess, asthma, cystic
fibrosis, bronchiectasis, interstitial lung diseases, and pneumonia have been known
to cause halitosis

Kinberg et al. published a review in 2010, in which they examined 94 patients having
halitosis out of which 54 had gastrointestinal pathology suggesting that gastrointestinal
is one of the common extra oral causes of halitosis.
Gastrointestinal causes like Zenker’s diverticulum, Gastro-esophageal reflux disease
(GERD),Gastric and peptic ulcers have been known to cause halitosis.
Helicobacter pylori is known to cause a gastric and peptic ulcer and is recently
associated with oral malodor.
Congenital broncho esophageal fistula, gastric cancer, hiatus hernia, pyloric stenosis,
enteric infections, dysgeusia, duodenal obstruction, and steatorrhea are some of the
sources of pathological mouth odor

Metabolic disorders like Trimethylaminuria (fish odor syndrome) is characterized by the
presence of trimethylamine (TMA), whose odor resembles of rotting fish in the urine,
sweat and expired air.
Individuals with TMAuria have diminished the capacity to oxidize the dietary-derived
amines TMA to its odorless metabolite TMA N-oxide resulting in an increased excretion
of large amounts of TMA in body fluids.
In hypermethioninemia the body produces a peculiar odor, which resembles that of,
boiled cabbage and is emanated through sweat, breath and urine.
If this condition is present, the extraoral origin should be determined, because the latter
requires medical investigation and support in therapy.

MICROBIOLOGY AND BREATH
MALODOR
Fusobacterium
nucleatum,
Treponema
denticola,
Prevotella
intermedia,
Porphyromonas
gingivalis,
Bacteroides
forsythus,
Eubacterium.
Some of the evidence in support of periodontal disease is indirect, as it is based on the
in vitro ability of species indigenous to the sub-gingival plaque to produce VSC’s.
produce large
amounts of CH3
SH and H2 S from
methionine,
cysteine, or serum
proteins

DRUGS ASSOCIATED WITH
HALITOSIS

DIAGNOSIS
Complaint,
Medical, dental and
halitosis history,
Information about
diet and habits,
Confirming an
objective basis to the
complaint

Discretely and intermittently recorded.
Questions such as frequency, duration, time of appearance within a day,
Whether others have identified the problem (excludes pseudo-halitosis
from genuine halitosis),
List of medications taken,
Habits (smoking, alcohol consumption)
Other Symptoms (nasal discharge, anosmia, cough, pyrexia, and weight
loss) should be carefully recorded
DIAGNOSIS

DIRECT
1. By directly sniffing the bad breath
2. Determination of odoriferous sulfur
containing substances by gas
chromatography or halimetry and other
methods
INDIRECT
These methods assess the products
produced by microorganisms in vitro or
identify odor producing microorganisms.

1. Self-assessment,
2. Whole mouth
breath test,
3. Spoon test,
4. Dental floss odor
test,
5. Saliva odor test.
Direct tests - Organoleptic
Direct sniffing of the expired air
(“organoleptic” and “hedonic”
assessment) is the simplest, most
common method to evaluate oral
malodor. An organoleptic
examination involves the dentist
assessing the odor at a range of
distances from the patient
Organoleptic measurement is highly recommended for initial diagnosis.
One potential risk of the organoleptic measurement is the transmission of
diseases via the expelled air

ORGANOLEPTIC MEASUREMENT
(SNIFF TEST)
Organoleptic measurement is a sensory test scored on the
basis of the examiner’s perception of a subject’s oral
malodor.
Organoleptic measurement can be carried out simply by
sniffing the patient’s breath and scoring the level of oral
malodor.
By inserting a translucent tube (2.5 cm diameter, 10 cm length) into the patient’s mouth and having the
person exhale slowly, the breath, undiluted by room air, can be evaluated and assigned an organoleptic
score.
The tube is inserted through a privacy screen (50cm-70cm) that separates the examiner and the patient.
The use of a privacy screen allows the patient to believe that they have undergone a specific malodor
examination rather than the direct-sniffing procedure.

Organoleptic Scores
(0- 5)
0 - No appreciable odor
1 - Barely noticeable odor
2 - Slight but noticeable odor
3 - Moderate odor
4 - Strong odor
5- Extremely
foul odor
By Rosenberg ,
Mulloch Et Al
1991.

DIAGNOSIS
The subjects are instructed to smell the
odor emanating from their entire mouth
by cupping their hands over their
mouth and breathing through the nose.
The presence or absence of malodor can
be evaluated by the patient
himself/herself.
SELF ASSESSMENT TESTS
Whole mouth malodor (Cupped breath)

Subjects are asked to
extend their tongue
and lick their wrist
in a perpendicular
fashion.
The presence of odor
is judged by
smelling the wrist
after 5 seconds at a
distance of about 3
cm.
Wrist lick test

Plastic spoon is used to
scrape and scoop material
from the back region of
the tongue.
The odor is judged by smelling
the spoon after 5 seconds at a
distance of about 5 cm
organoleptically.
Spoon test

Unwaxed floss is passed through interproximal contacts.
Dental floss test

Involves having the subject
expectorate approx. 1-2 ml of
saliva into a petridish.
The dish is covered immediately,
incubated at 370 C for five
minutes and then presented for
odor evaluation at a distance of
4 cm from the examiner’s nose.
Saliva odor test

BANA TEST
If any of the these species are present, they hydrolyze the BANA
enzyme-producing B-naphthylamide which in turn reacts with
imbedded diazo dye to produce a permanent blue color indicating a
positive test
It is a chair side, enzyme-based assay, which is
used to determine the proteolytic activity of
certain oral anaerobes that contribute to oral
malodor and which are considered as active
H2 SO4 producers.

VOLATILE SULFIDE MONITOR
This electronic (Haiimeter,
InterScan, Chatsworth, Calif)
analyzes concentration of hydrogen
sulfide and methyl-mercaptan , but
without discriminating between
them.

GAS CHROMATOGRAPHY (GC):
GC, performed
with apparatus
equipped with a
flame photometric
detector, is specific
for detecting
sulphur in mouth
air.
It measures
directly the three
VSC methyl
mercaptan,
hydrogen sulfide
and dimethyl
sulfide.
GC is considered
the GOLD
STANDARD for
measuring oral
malodor.
This device can
analyze air, saliva,
crevicular fluid for
a volatile
component.

DIAMOND PROBE
 The Probe is placed directly into the
periodontal pocket or tongue.
 The sulfide-sensing element
generates an electrochemical voltage
proportional to the concentration of
sulfide ions present.
 The control unit reports the sulfide
level at each site in a digital score
from: 0.0 to 5.0

NINHYDRIN METHOD OF
DETECTING AMINE
COMPOUNDS
Iwanicka et al (2005)
showed that amine levels
were higher in the saliva of
subjects suffering from
halitosis and lower in
healthy controls.
Tanaka M et al used these electronic
noses to clinically assess oral malodor and
examined the association between oral
malodor strength and oral health status.
ELECTRONIC NOSE

HALITOX SYSTEM
Quick and simple
Detects VSCs and poly
amines

TOPAS
It detects both VSC and
polyamines in the
sample.
The absorbent point
given with the kit is
inserted into the pocket.
Left in place for 1
minute.
Submerge the absorbent
point tip in the toxin
reagent .
Wait for 5 minutes and
see for yellow color in
the specimen on the
scale of 0-5, which is
directly proportional to
the level of toxins in the
sample.

PREVENTIVE MEASURES
Visit dentist regularly
Periodical tooth cleaning by dental
professional.
Brushing of teeth twice daily with
appropriate brushing techniques and
for a duration of 2-3 mins.
Use of a tongue scraper to get rid of
the lurking odour causing bacteria in
the tongue surface.
Preventive measures rather than curative aspects are highly recommended.

Flossing after brushing to remove food particles
stuck in between the tooth surfaces.
Limit intake of strong odour species.
Limit sugar and caffeine intake.
Drink plenty of liquids.
Chew sugar free gum for a minute when mouth
feels dry.
Eat fresh fibrous vegetables such as carrots.

MANAGEMENT AND
TREATMENT
1. Confirm the diagnosis,
2. Identify and eliminate the predisposing and modifying factors,
3. Identify any contributing medical conditions and refer for management,
4. Review and reassure.
The management of halitosis entails four steps:

MANAGEMENT
Treatment needs (TN) for halitosis have been categorized into 5 classes in order to provide guidelines
for clinicians in treating halitosis patients:
Rosenberg M, McCulloch CA. Measurement of oral malodor: Current methods and future prospects. J Periodontol
1992;63:776-82.
Category Description
TN- 1 Explanation of halitosis and instruction of
oral hygiene
TN- 2 Oral prophylaxis, Professional cleaning and
treatment for oral diseases
TN- 3 Referral to a physician or medical specialist
TN- 4 Explanation of examination data, further professional instruction,
education and reassurance
TN- 5 Referral to a clinical psychologist , a psychiatrist or other
psychology specialist

Mechanical
reduction of
intraoral
nutrients and
micro-organisms
Chemical
reduction of oral
microbial load
Conversions of
VSCs
Masking the
malodor.
MANAGEMENT

Mechanical reduction of intraoral nutrients and micro-organisms
- Tongue cleaning
- Tooth brush
- Inter-dental cleaning
- Professional periodontal therapy
- Chewing gum
MANAGEMENT

2. Chemical reduction of oral microbial load
- Chlorhexidine
- Essential oils
- Chlorine dioxide
- Two-phase oilwater rinse
- Triclosan
- Aminefluoride/ Stannous fluoride
- Hydrogen peroxide
- Oxidising lozenges
-Roldan S 2005,2004,2003 scully 2006
MANAGEMENT

CHLORHEXIDINE (CHX)
Mouth rinses containing antibacterial agents such as CHX and cetylpyridinium chloride (CPC) may
play an important role in reducing the levels of halitosis producing bacteria on the tongue.
Chlorine dioxide and zinc containing mouth rinses can be effective in neutralization of odoriferous
sulfur compounds.
Roldan. S et al. evaluated five different commercial mouth rinses with respect to their anti-halitosis
effect and anti-microbial activity on salivary bacterial counts.
Formulations that combine CHX and CPC achieved the best results, and a formulation combining CHX
with NaF resulted in the poorest.
Essential oils: Listerine was found to be only relatively effective against oral malodor (±25% reduction
vs. 10% of placebo) and caused a sustained reduction in level of odorigenic bacteria
Chlorine dioxide: It is a powerful oxidizing agent that oxidizes the sulfides of the VSC’s to nonodorous
sulfates and raises the oxidation/reduction ratio of the saliva toward the more oxidizing state.

TWO-PHASE
OILWATER
RINSE: The
efficacy of
oilwater CPC
formulation is
thought to result
from the
adhesion of a
high proportion
of
microorganisms
to the oil droplet
which is further
enhanced by the
CPC.
TRICLOSAN: A
broad-spectrum
antibacterial
agent, has been
found to be
effective against
most oral
bacteria and has
a good
compatibility
with other
compounds used
for oral home
care
AMINEFLUORID
E/STANNOUS
FLUORIDE
(AMF/SNF2 ): The
association of
AmF/SnF2
resulted in
encouraging
reduction of
morning breath
odor, even when
oral hygiene is
insufficient
HYDROGEN
PEROXIDE:
Suarez et al.
reported that
rinsing with 3%
H2 O2 produced
impressive
reductions
(±90%) in sulfur
gas that persisted
for 8 h.
OXIDIZING
LOZENGES: The
anti-malodor effect
of lozenges may be
caused by the
activity of
dehydroascorbic
acid which is
generated by
peroxide-mediated
oxidation of
ascorbate present in
the lozenges.
MANAGEMENT

3.Conversion of volatile sulfide compounds
- Metal salt solutions
- Toothpastes
- Chewing gum
MANAGEMENT

Metal salt solutions: Metal ions with affinity for sulfur are rather efficient
in capturing the sulfur-containing gases. Zinc is nontoxic,
noncumulative, and gives no visible discoloration
Tooth paste: Baking soda dentifrices have been shown to be effective,
with a 44% reduction of VSCs level 3 h after tooth brushing versus a
31% reduction for fluoride dentifrices (Brunnet et al. 1998)
Chewing gums: Tsunoda et al. (1996) investigated the beneficial effects
of chewing gums containing tea extract for its deodorizing mechanism.
MANAGEMENT

4. Masking the malodor
-Rinses
-Mouth sprays
-Lozenges containing volatiles
-Chewing gum
MANAGEMENT

Herbs and essential
oils can be made into very
effective mouthwash
remedies to sweeten
breath and help
keep gums and teeth
healthy fennel not only
improves digestion, but
also can reduce bad
breath and body odor that
originates in the intestines.
Give raw carrots as a
midday treat to help scour
teeth of bacteria-laden
plaque, a common cause
of bad breath.
Cardamom tea contains
cineole, a potent antiseptic
that kills bad-breath
bacteria and sweetens
breath.
Herbal treatment: MANAGEMENT

Thymol, one of the
constituents of thyme, is
contained in antiseptic
mouthwashes.
Neem leaf powder can be used
as an effective tooth powder to
fight plaque and gingivitis
when mixed with astringent
herb powders and/or baking
soda.
A few drops of Tea tree oil
, lemon or peppermint
essential oils can be added to
warm water for an
effective mouth
rinse to freshen breath
Herbal treatment: MANAGEMENT

CONCLUSION
It’s a common complaint that may periodically affect most of the
adult population.
Oral maldor, which is commonly noticed by patients, is an
important clinical sign and symptom that has many etiologies
which include local and systemic factors.
It is often difficult for the clinician to find the underlying
pathologies.
Although consultation and treatment may result in dramatic
reduction in bad breathe, patients may find it difficult to sense the
improvement themselves
The field of halitosis research would benefit from: • More
reliable, portable instruments for measuring VSC’s, • A
standard scale for assessing oral malodor, • Further studies
with larger sections of the population, and • Development of
site-specific measurements.

REASON FOR
CHOOSING THIS
ARTICLE?

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