journal of dentistry 35 (2007) 627–635

available at www.sciencedirect.com

journal homepage: www.intl.elsevierhealth.com/journals/jden

Review

A review of the current literature on aetiology and

measurement methods of halitosis

Annemiek M.W.T. van den Broek a, Louw Feenstra b, Cees de Baat a,*
a
Department of Oral and Maxillofacial Surgery and Special Dental Care, Erasmus University Medical Centre, Rotterdam,
The Netherlands
b
Department of Otorhinolaryngology, Erasmus University Medical Centre, Rotterdam, The Netherlands

article info abstract

Article history: Objectives: This work reviews the current knowledge of aetiology and measurement meth-
Received 14 February 2007 ods of halitosis.
Received in revised form Data: Halitosis is an unpleasant or offensive odour emanating from the breath. The con-
5 April 2007 dition is multifactorial and may involve both oral and non-oral conditions.
Accepted 27 April 2007 Sources: A private, monthly with keywords halitosis, malodo(u)r, (a)etiology, measurement,
and management from Medline and Pubmed updated database of literature was reviewed.
Conclusions: In approximately 80–90% of all cases, halitosis is caused by oral conditions,
Keywords: defined as oral malodour. Oral malodour results from tongue coating, periodontal disease,
Halitosis peri-implant disease, deep carious lesions, exposed necrotic tooth pulps, pericoronitis,
Aetiology mucosal ulcerations, healing (mucosal) wounds, impacted food or debris, imperfect dental
Measurement restorations, unclean dentures, and factors causing decreased salivary flow rate. The basic
process is microbial degradation of organic substrates. Non-oral aetiologies of halitosis
include disturbances of the upper and lower respiratory tract, disorders of the gastrointest-
inal tract, some systemic diseases, metabolic disorders, medications, and carcinomas.
Stressful situations are predisposing factors. There are three primary measurement meth-
ods of halitosis. Organoleptic measurement and gas chromatography are very reliable, but
not very easily clinically implemented methods. The use of organoleptic measurement is
suggested as the ‘gold standard’. Gas chromatography is the preferable method if precise
measurements of specific gases are required. Sulphide monitoring is an easily used method,
but has the limitation that important odours are not detected. The scientific and practical
value of additional or alternative measurement methods, such as BANA test, chemical
sensors, salivary incubation test, quantifying b-galactosidase activity, ammonia monitor-
ing, ninhydrin method, and polymerase chain reaction, has to be established.
# 2007 Elsevier Ltd. All rights reserved.

Halitosis is a general term used to define an unpleasant or malodour, foetor ex-ore, and foetor oris. Halitosis should not
offensive odour emanating from the breath regardless of be confused with the generally temporary oral odour caused
whether the odour originates from oral or non-oral sources.1,2 by intake of certain foods, tobacco, or medications. Medica-
Other terms used are bad or foul breath, breath malodour, oral tions known or suspected of causing halitosis are suplatast

* Corresponding author at: Department of Preventive and Restorative Dentistry, Radboud University Nijmegen Medical Centre, P.O. Box
9101, 6500 HB Nijmegen, The Netherlands. Tel.: +31 24 3616410; fax: +31 24 3540265.
E-mail address: c.debaat@dent.umcn.nl (C. de Baat).
0300-5712/$ – see front matter # 2007 Elsevier Ltd. All rights reserved.
doi:10.1016/j.jdent.2007.04.009
628 journal of dentistry 35 (2007) 627–635
tosilate, cyclosporine, and a fish oil derivative in the treatment
of Crohn’s disease.3–5
Halitosis can be classified into categories of genuine
halitosis, pseudo-halitosis, and halitophobia.6 Genuine hali-
tosis is diagnosed if obvious malodour with intensity beyond
socially acceptable level is perceived. If obvious malodour is
not perceived by others, although the patient stubbornly
complains of its existence, it is diagnosed as pseudo-halitosis.
Should a patient, after treating either genuine or pseudo-
halitosis resulting in no objectively noticeable foul odour, still
believe that he or she has halitosis, very likely the diagnosis is
halitophobia.
Most adults suffer from genuine halitosis occasionally,
while an estimated 10–30% of the population suffers from this
problem regularly.7 Just a few studies have documented the
prevalence in population-wide samples. A group of 2672
Japanese governmental workers had in 14%, 23%, 6%, and 16%
of cases, respectively, early morning, late morning, early
afternoon, and late afternoon halitosis.8 In a sample of 20–60-
year-old Jordanian adults 25% reported to have halitosis.9 The
objectively measured prevalence of halitosis in a sample of
1000 men and 1000 women, aged 15–64 years, residing in urban
and rural areas in China, was 27.5%.10 In the Western societies,
discomfort and (psycho)social embarrassment are reasons for
seeking professional care for halitosis. This paper reviews and
discusses the current literature on aetiology and measure-
ment methods of genuine halitosis. The source of the
literature reviewed was a private, monthly with keywords
halitosis, malodo(u)r, (a)etiology, measurement, and manage-
ment from Medline and Pubmed updated database.
1. Aetiology of halitosis
Genuine halitosis is multifactorial and may involve both oral
and non-oral conditions. However, in approximately 80–90%
of all cases it is caused by oral conditions, defined as oral
malodour.8,11
1.1. Oral malodour
There is consensus that oral malodour results from tongue
coating, periodontal disease, peri-implant disease, deep
carious lesions, exposed necrotic tooth pulps, pericoronitis,
mucosal ulcerations, healing (mucosal) wounds, impacted
food or debris, imperfect dental restorations, unclean den-
tures, and factors causing decreased salivary flow rate.10,12–19
Oral malodour arises from microbial degradation of organic
substrates, such as glucose, mucins, peptides, and proteins
present in saliva, crevicular fluid, oral soft tissues, and
retained debris.2,20–23 Proteins containing the sulphurous
amino acids cysteine and methionine, as well as tryptophan
and lysine are causative substrates.24,25 Activity of the enzyme
b-galactosidase in saliva is an associated cause.26,27 Some
microbial degradation products are volatile sulphur-contain-
ing compounds. Hydrogen sulphide (H2S), methyl mercaptan
(CH3SH), and dimethyl sulphide ((CH3)2S) contribute to the
malodour.2,12,28 Methyl mercaptan is the major oral malodour
component associated with periodontal disease.12,29 In addi-
tion to volatile sulphur-containing compounds, a contribution
has been demonstrated or suggested from short-chain fatty
acids (butyrate, propionate, valerate), diamines (cadaverine,
putrescine), alcohols, phenyl compounds (indole, skatole,
pyridiene), alkines, ketones, and nitrogen-containing com-
pounds (urea, ammonia).30–32
Organisms responsible for the hydrolysis of peptides and
proteins, and the production of volatile sulphur-containing
compounds include proteolytic obligate anaerobes, especially
the Gram-negative species, mainly retained in tongue coating
and periodontal pockets.2,13,33–35 It has been suggested that the
primary sources of volatile sulphur production are the BANA
(benzoyl-DL-arginine-napthylamide)-hydrolysing pathogens
in the substrates.36 Bacteria known to produce volatile
sulphur-containing compounds include Aggregatibacter actino-
mycetemcomitans (formerly Actinobacillus actinomycetemcomi-
tans), Actinomyces species, Atopobium parvulum, Campylobacter
rectus, Desulfovibrio species, Eikenella corrodens, Eubacterium
sulci, Fusobacterium species, Peptostreptococcus micros, Porphyr-
omonas endodontalis, Porphyromonas gingivalis, Prevotella species,
Solobacterium moorei, Tannerella forsythia (formerly Bacteriodes
forsythus or Tannerella forsythensis), Treponema denticola, Veillo-
nella species, Vibrio species, a phylotype of Dialister, a
phylotype of the uncultivated phylum, and a phylotype of
Streptococcus, and as yet unidentified sulphur-reducing bac-
teria.22,33–35,37–46 The species diversity found in halitosis
samples suggests that halitosis may be the result of complex
interactions between several bacterial species. Also, the role of
uncultivable bacteria may be important in contributing to this
complex process.34
Among healthy individuals with no history of halitosis and
no periodontal disease, the tongue was the major site for
volatile sulphur compounds production.24 The substrate on
the dorsum of the tongue may be built up by post-nasal drip
and by extra-oesophageal reflux disease.47,48 Several studies
have shown a relationship between oral malodour and
periodontal disease. The potential importance of volatile
sulphur-containing compounds in the transition of period-
ontal tissues in developing periodontal disease has been
emphasized.14,15,49,50 However, it is still not well understood
how periodontal health relates to oral malodour.51–53 Medica-
tions which reduce salivary flow, such as antidepressants,
antipsychotics, and narcotics, may cause oral malodour.17,54
There are three areas of evidence to consider the bacteria
present in the oral cavity as the most likely origin of halitosis.
First, in vitro, oral organic substrates and bacteria produced the
odorous compounds.25,55 In vivo, production of volatile
sulphur-containing compounds was induced upon provision
of peptides and amino acids in the mouth.24,56,57 Second,
halitosis was immediately reduced by reduction of substrates
and micro-organisms, such as brushing the teeth and cleaning
the tongue, which would not have been possible if the halitosis
originated in non-oral regions, such as the nose, the tonsils,
the lungs, or the stomach.1,58,59 Third, antibacterial agents
reduce halitosis.60
1.2. Non-oral halitosis
Non-oral aetiologies of genuine halitosis may include distur-
bances of the upper and lower respiratory tract, disorders of the
gastrointestinal tract, some systemic diseases, metabolic
 journal of dentistry 35 (2007) 627–635 629

disorders, and carcinomas.61–64 Stressful situations are predis-
posing factors.65–67 Parasitosis is suggested as being a possible
cause of halitosis in children.68 Publications of fundamental
research are lacking. Reports are authors’ opinions or case-
reports or reports of small groups of patients. Reports
suggesting halitosis originating from the respiratory tract are
on chronic (rhino)sinusitis, chronic tonsillitis, tonsillithiasis,
nasal obstruction, a foreign body in the upper respiratory tract,
nasopharyngeal abscess, and a Zenker’s diverticle.69–76 Reports
suggesting halitosis originating from the gastrointestinal tract
and systemic diseases are on inflammatory bowel disease,
Helicobacter pylori infection, gastritis, (extra)oesophageal reflux
disease, and diabetes mellitus.48,73,77–80
155 patients complaining of halitosis. The results were
recorded as no appreciable odour, slight odour, clearly
noticeable malodour or strong malodour. The percentage of
agreement in scores exceeded 83%.86 Four experienced and
two inexperienced odour judges completed a sensory training
exercises protocol and conducted pre- and post-training odour
measurements. Overall, training reduced oral judges’ errors.
Previous experience was not associated with the size of the
errors, nor the improvement from pre- to post-training.87
The spoon test is a simple, albeit subjective, organoleptic
measurement method.88–90 Using a spoon or similar instru-
ment, the tongue dorsum is scraped and the scraped material
can be smelled.

2.2. Gas chromatography

2. Measurement methods of halitosis
With gas chromatography the concentration of volatile
The three primary measurement methods of genuine halitosis sulphur-containing compounds in samples of saliva, tongue
are organoleptic measurement, gas chromatography, and coating or expired breath is measured by producing mass
sulphide monitoring. Additional or alternative measurement spectra. Samples are analyzed by a gas chromatograph
methods are BANA test, chemical sensors, salivary incubation equipped with a flame photometric detector. The components
test, quantifying b-galactosidase activity, ammonia monitor- can be identified by comparing the mass spectra with those of
ing, ninhydrin method, and polymerase chain reaction. a computer based reference library.91 Gas chromatography
may be combined with mass spectrometry, enlarging the
2.1. Organoleptic measurement scope of the method.62
Low as well as high correlations were shown between the
Organoleptic or hedonic measurement is a simple commonly results of organoleptic measurements and gas chromatogra-
used measurement method of halitosis by an examiner. A phy (Table 1). The method is considered to be highly objective,
plastic tube is inserted into the patient’s mouth, preventing reproducible, and reliable.92 However, it cannot be easily
the dilution of mouth air with room air. While the patient is clinically implemented because of the relatively high cost, the
exhaling slowly, the examiner judges the odour at the other requirement of highly trained persons, and the extensive
end of the tube. A privacy screen with a hole for the straw or procedures.1,2,93–95 To eliminate discrepancies caused by
the tube can be used to separate the examiner from the variations in operator sampling or breath injection techni-
patient. Nasal-breath odour can be measured with a tube ques, an automated system aspirating breath samples directly
inserted into one of the nostrils, while the other nostril is into the gas chromatograph was developed.96 In order to
closed by a finger.6 overcome the practical drawbacks, portable gas chromato-
Various scoring systems can be used for estimating the graphs were developed to measure sulphur-containing com-
intensity of the odour. The most widely used scale is ranging pound levels inside the mouth.45,97 The scientific and practical
from 0 to 5: 0 = no odour, 1 = barely noticeable odour, 2 = slight
but clearly noticeable odour, 3 = moderate odour, 4 = strong
odour, 5 = extremely foul odour.81 However, the reliability and
Table 1 – Correlations between organoleptic scores and
reproducibility of the method are problematic and research
gas chromatography measurements, directly taken from
projects are carried out attempting to improve the method.82 the source articles
Measurement by a panel of judges is considered to improve the
Study Correlation p-Value
reliability.6,83 Agreement among judges may be increased by
coefficient
standardisation of the sense of smell, using an odour solution
kit for measuring the olfactory sense and previously assigned Schmidt et al.28
scores.84 The use of n-butanol as a suitable odorant for use in Study I r = 0.28 p < 0.05
Study II r = 0.35 p < 0.001
organoleptic training of breath odour judges could not be
assessed as a helpful method. The scores did not correlate with Shimura et al.107 r = 0.71 p < 0.01
gas chromatography scores at all and the use of n-butanol could Oho et al.86 r = 0.69 p < 0.0001
Amano et al.31 r = 0.47 p < 0.01
not be recommended because of its irritant nature.85 For a good
Tanaka et al.109 r = 0.63 p < 0.05
agreement between judges, patients must abstain from hygiene
Nonaka et al.110 r = 0.73 p < 0.05
practises, smoking, antibiotics, and foods containing garlic,
Hunter et al.96
onion, and spices prior to the examination.6 Furthermore, the
H2S r = 0.63 p < 0.001
agreement between judges may be increased if they themselves
CH3SH r = 0.61 p < 0.001
avoid drinking coffee, tea, and juice, smoking, and using (CH3)2S r = 0.46 p < 0.001
scented cosmetics before the organoleptic measurements.6 Total sulphur compounds r = 0.65 p < 0.001
Three dentists, who were trained in performing a stan-
Iwanicka-Grzegorek et al.114 r = 0.78 p < 0.001
dardized organoleptic measurement, conducted a test among
630 journal of dentistry 35 (2007) 627–635

value of portable gas chromatographs has to be elucidated by Table 3 – Correlations between gas chromatography and
future research projects. sulphide monitor (peak values) measurements, directly
taken from the source articles
2.3. Sulphide monitoring Study Correlation coefficient p-Value
86
Oho et al. r = 0.84 p < 0.0001
A portable monitor has been developed for measuring volatile Furne et al.95 r = 0.73 p < 0.01
sulphur compounds. Patients are asked to refrain from talking
Sopapornamorn et al.102
5 min prior to measurement. The monitor is zeroed on
H 2S r = 0.79 p < 0.01
ambient air. Measurement is performed by inserting a CH3SH r = 0.67 p < 0.01
disposable tube into the patient’s mouth and connecting this (CH3)2S r = 0.63 p < 0.01
to the monitor, while the patient is breathing through the
Sopapornamorn et al.103
nose. Electrochemical reactions with the sulphur-containing H 2S r = 0.73 p < 0.01
compounds in the breath generate an electric current, which is CH3SH r = 0.63 p < 0.01
directly proportional to the levels of volatile sulphur-contain- (CH3)2S r = 0.55 p < 0.01
ing compounds.98,99
Sulphide monitor measurements correlated significantly
for mainly low correlation coefficients with organoleptic Although several studies demonstrated that gas chroma-
scores (Table 2). Patients may produce normal sulphide tography and sulphide monitor measurements are highly
monitor measurements, whereas organoleptic scores are significant correlated, appreciable differences were observed
high. The reason for this discrepancy is that in addition to (Table 3). The sensitivity and specificity of gas chromatogra-
volatile sulphide-containing compounds other odorants con- phy (0.79 and 0.83, respectively) appeared higher than the
tribute to halitosis, such as volatile short-chain fatty acids, sensitivity and specificity of sulphide monitoring (0.76 and
polyamines, alcohols, phenyl compounds, alkanes, ketones, 0.78, respectively).86 When relatively precise measurements
and nitrogen-containing compounds.30,90,95,100,101 These odor- are required, gas chromatography is the preferable method.95
ants are not detectable by a sulphide monitor. Recently, a new sulphide monitor was developed. The
monitor’s sensitivity and specificity was, respectively, more
than 0.79 and between 0.61 and 0.73. Because this monitor has
Table 2 – Correlations between organoleptic scores and a low specificity in periodontal disease patients, it should be
sulphide monitor measurements, directly taken from the used cautiously for measuring volatile sulphur-containing
source articles compounds related to periodontal disease.102,103
Study Correlation p-Value
coefficient 2.4. BANA test
Rosenberg et al.98
Judge A r = 0.60 p < 0.05 Proteolytic obligate Gram-negative anaerobes and short-chain
Judge B r = 0.52 p < 0.05 fatty acids colonizing the subgingival plaque and the dorsum
of the tongue, can be detected by the presence of an enzyme
Rosenberg et al.83 r = 0.60 p < 0.001
degrading benzoyl-DL-arginine-a-naphthylamide (BANA), a
36
De Boever et al. synthetic trypsin substrate, and forming a coloured com-
Sulphide monitor measurement
pound. The name of the halitosis measurement method is
After 30 s r = 0.53 p < 0.001
After 60 s r = 0.63 p < 0.001
BANA test. The BANA test is a very practical and easy to use
method. Disadvantage is that it cannot determine the specific
Greenstein et al.90
role of the different bacterial species in the production of
Judge A, before treatment r = 0.27 p = 0.003
halitosis.30,36,88,104,105 BANA scores correlated significantly
Judge A, after treatment r = 0.27 p = 0.003
Judge B, before treatment r = 0.39 p < 0.001 with organoleptic measurements (r = 0.40; p = 0.003), but were
Judge B, after treatment n.s. poorly related to sulphide monitor measurements (r < 0.30).
However, multiple-regression analysis with organoleptic
Willis et al.119 r = 0.41 p = 0.027
Oho et al.86 r = 0.66 p < 0.0001 measurements as the independent variable, both peak
sulphide measurement levels and BANA scores factored into
Sterer et al.26
the regression, yielding highly significant associations
Judge A, whole-mouth r = 0.37 p = 0.002
Judge A, tongue dorsum r = 0.26 p = 0.036
(r = 0.50–0.59; p < 0.001). Probably, micro-organisms asso-
Judge B, whole-mouth r = 0.46 p < 0.001 ciated with BANA assay contribute malodorous components
Judge B, tongue dorsum r = 0.38 p = 0.002 to the breath air other than sulphur-containing compounds,
such as cadaverine.30,88 In patients with periodontal disease, a
Iwanicka-Grzegorek et al.114 r = 0.78 p < 0.001
Stamou et al.52 r = 0.55 p < 0.001 stronger correlation between BANA test and sulphide monitor
measurements was found (r = 0.55; p < 0.01).106
Sopapornamorn et al.102
Periodontal disease group r = 0.42 p < 0.05
Non-periodontal disease group r = 0.61 p < 0.01 2.5. Chemical sensors
Total group r = 0.56 p < 0.01
Chemical sensors for volatile sulphur-containing compounds
Sopapornamorn et al.103 r = 0.64 p < 0.01
have been integrated into a probe for measuring directly in
 journal of dentistry 35 (2007) 627–635
periodontal pockets and on the tongue. A sulphide-sensing
element in the probe generates an electrochemical voltage
proportional to the concentration of sulphide ions present.
This voltage is measured relative to the operating point of a
reference element. The electrochemical voltages generated by
sulphide ions are measured by an electronic unit and
displayed in a digital score.14–16,105 Measurements by a
monitor with a zinc-oxide, thin film, semiconductor sensor
demonstrated highly significant correlations with organolep-
tic measurements (r = 0.76–0.82; p < 0.01).107,108 With a
recently developed chemical sensor system, the so-called
electronic nose, high correlations have been found with
organoleptic (r = 0.71–0.81; p < 0.05) as well as gas chromato-
graphy measurements (r = 0.63; p < 0.05).109,110
Other promising chemical sensors for measuring ammonia
and methyl mercaptan in breath air have been introduced
lately.111,112 Recently, a compact gas chromatograph with an
indium oxide semiconductor gas sensor was developed. The
apparatus measures each volatile sulphur-containing com-
pound separately. Strong measurement correlations have
been demonstrated between this apparatus and a conven-
tional gas chromatograph (r = 0.77–0.87; p < 0.0001).113
2.6. Quantifying b-galactosidase activity
Deglycosylation of glycoproteins was considered as an initial
step on oral malodour production. b-Galactosidase is one of
the important enzymes in deglycosylation. The activity of b-
galactosidase can be easily quantified with the use of a
chromogenic substrate absorbed onto a chromatography
paper disc. Saliva applied to the paper disc, may induce a
colour chance of the paper, which can be recorded by an
examiner: 0 = no colour; 1 = faint blue colour; 2 = moderate to
dark blue colour. b-Galactosidase assay scores were signifi-
cantly associated with organoleptic scores for whole-mouth
and tongue malodour (r = 0.47–0.49; p < 0.001). b-Galactosi-
dase activity and sulphide monitor measurements both
factored significantly into multiple regression equations for
organoleptic scores, yielding multiple r-values ranging from
0.47 ( p = 0.0007) to 0.60 ( p < 0.0001).26,27
2.7. Salivary incubation test
The salivary incubation test is using saliva collected in a glass
tube. After incubating the tube at 37 8C in an aerobic chamber
under an atmosphere of 80% nitrogen, 10% carbon dioxide,
and 10% hydrogen for several hours, the odour can be
measured by an examiner. A strong correlation between the
salivary incubation test and organoleptic (r = 0.39–0.54;
p = 0.000–0.013) as well as sulphide monitor measurements
(r = 0.58–0.60; p = 0.000) was demonstrated. The salivary
incubation test is much less influenced by external para-
meters, such as subjectivity, smoking, drinking coffee, eating
garlic, onion, spicy food, and scented cosmetics, than
organoleptic measurements.100
2.8. Ammonia monitoring
On the basis of the hypothesis that ammonia produced by oral
bacteria reflects halitosis, a portable monitor for measuring
631
ammonia has been developed. Patients are instructed to rinse
with a urea solution during 30 s and to keep their mouth closed
for 5 min. The instrument contains a pump, which can draw
air through an ammonia gas detector tube connected to a
disposable mouthpiece placed inside a patient’s mouth. The
concentrations of ammonia produced by oral bacteria can be
read directly from a scale. Levels of volatile sulphur-contain-
ing compounds and ammonia were determined in 25 patients
by gas chromatography and ammonia monitoring. A signifi-
cant correlation existed between the two measurement
methods (r = 0.39; p < 0.01). Bacteria in dental plaque and
tongue coating produced ammonia in a concentration-
dependent manner. The ammonia level decreased after the
removal of tongue coating and dental plaque.31
2.9. Ninhydrin method
Amines or polyamines cannot be measured by using sulphide
monitoring. In a recent study, the ninhydrin method was used
for detecting low-molecular-weight amines in breath. A
sample of saliva and isopropanol was mixed and centrifuged.
The supernatant was diluted with isopropanol, buffer solution
(pH 5), and ninhydrin reagent. The mixture was refluxed in a
water bath for 30 min, cooled to 21 8C, and diluted with
isopropanol to a total volume of 10 ml. Light absorbance
readings were determined using a spectrometer. The ninhy-
drin colorimetric reaction is a simple, rapid, and inexpensive
method. Salivary amine levels measured by the ninhydrin
method significantly correlated with organoleptic scores
(r = 0.60; p  0.001) and sulphide monitor measurements
(r = 0.54; p  0.001) in halitosis patients and control subjects.114
2.10. Polymerase chain reaction
Real-time polymerase chain reaction (PCR) using the TaqMan
system can be used for quantitative analysis of volatile
sulphur-containing compounds-producing oral bacteria.
Briefly, an oligonucleotide probe with a reporter fluorescent
dye attached to its 50 -end and a quencher dye attached to its 30 -
end is designed to hybridize to the target gene. During PCR
amplification, the quencher dye of the probe is cleaved by the
50 -nuclease activity of Taq polymerase, resulting in the
accumulation of reporter fluorescence. The release of the
fluorescent dye during amplification allows for the rapid
detection and quantification of oral bacteria DNA.33,115
Using the polymerase chain reaction, a strong correlation
was found between the presence of Bacteroides forsythus in
saliva of subjects with periodontitis and the concentration of
volatile sulphur-containing compounds in breath air mea-
sured using gas chromatography.42
3. Discussion
Halitosis seems an important negative factor in social
communication. Just a few studies are reporting the pre-
valence of halitosis in the general population. Because of the
important health and social implications of halitosis, epide-
miologic, aetiologic and measurement studies are needed to
assess the prevalence of halitosis in the general population
632 journal of dentistry 35 (2007) 627–635
world-wide, to identify factors associated with this condition,
such as age, gender, socioeconomic factors, oral health status,
and (oral) health behaviour, and to evaluate halitosis
measurement methods. The ultimate goal of halitosis
research should be to control this condition in the world-
wide population by effective preventive measurements and
treatment.
Since approximately 80–90% of all halitosis cases have an
oral aetiology, in research and management of halitosis
attention should primarily be paid to all forms of microbial
degradation of organic substrates in the oral cavity. Never-
theless, since non-oral halitosis might be a manifestation of a
serious disease or problem, the importance of non-oral
halitosis should not be underexposed.
The three primary measurement methods of genuine
halitosis, organoleptic measurement, gas chromatography,
and sulphide monitoring, showed statistically significant, but
not generally consistent correlations (Tables 1–3). The dis-
parity in correlation coefficients, which were directly taken
from the research articles, may be explained by the following
factors: variability in patient groups (age, race, intensity of
halitosis), variability in equipment used (calibration), differ-
ences between judges (calibration, sniffing capacity), and
variability in breath gases exhaled by patient groups in
combination with variable susceptibility of the measurement
methods to these gases.
Measurement of halitosis is complicated by a variety of
parameters and each method has specific advantages and
shortcomings with respect to these parameters. Organoleptic
measurement by a panel of sensory judges and gas chroma-
tography are very reliable, but expensive and not very practical
methods. Nevertheless, the use of organoleptic measurement
is suggested as the ‘gold standard’ or primary indicator of
halitosis.116,117 This statement is corroborated by research
findings with the comment that because of the inherent
subjectivity it should not be the sole measurement method in
defining patients with halitosis.118 Gas chromatography is the
preferable method if precise measurements of specific gases
are required, but the method can not be easily clinically
implemented since it requires relatively high cost, highly
trained persons, and extensive procedures. Sulphide monitor-
ing is a relatively inexpensive and easily used method, but has
the limitation that important odours are not detected. Further
improvement of the three primary measurement methods of
halitosis should be one of the aims of halitosis research.
The scientific and practical value of the additional or
alternative measurement methods of halitosis presented in
this review has still to be established by scientific evaluation of
the methods. The most promising additional or alternative
method for both research and clinical purposes seem to be the
use of chemical sensors.
4. Concluding remarks
Most adults suffer from genuine halitosis occasionally, while
an estimated 10–30% of the population suffers from this
problem regularly. In approximately 80–90% of all cases
halitosis is caused by oral conditions, defined as oral
malodour. Oral malodour arises from microbial degradation
of organic substrates. Non-oral aetiologies of genuine halitosis
may include disturbances of the upper and lower respiratory
tract, disorders of the gastrointestinal tract, some systemic
diseases, metabolic disorders, and carcinomas. Stressful
situations are predisposing factors. Organoleptic measure-
ment by a panel of sensory judges and gas chromatography
are very reliable, but expensive and not very easily clinically
implemented measurement methods of halitosis. Gas chro-
matography is the preferable method if precise measurements
of specific gases are required. Sulphide monitoring is a
relatively inexpensive and easily used method, but has the
limitation that important odours are not detected. The
scientific and practical value of the presented additional or
alternative measurement methods has to be established by
scientific evaluation.
references
1. Tonzetich J, Ng SK. Reduction of malodor by oral cleansing
procedures.. Oral Surgery Oral Medicine and Oral Pathology
1976;42:172–81.
2. Tonzetich J. Production and origin of oral malodor: a review
of mechanisms and methods of analysis. Journal of
Periodontology 1977;48:13–20.
3. Belluzzi A, Brignola C, Campieri M, Camporesi EP,
Gionchetti P, Rizzello F, et al. Effects of new fish oil
derivative on fatty acid phospholipid-membrane pattern in
a group of Crohn’s disease patients. Digestive Diseases
Sciences 1994;39:2589–94.
4. Murata T, Fujiyama Y, Yamaga T, Miyazaki H. Breath
malodor in an asthmatic patient caused by side-effects of
medication: a case report and review of the literature. Oral
Diseases 2003;9:273–6.
5. Steinberg SM, Venuto RC, Kuruvila CK, Taylor DO, Anil
Kumar MS, Groothuis JR, et al. Randomized, open-label
preference study of two cyclosporine capsule formulations
(USP modified) in stable solid-organ transplant recipients.
Clinical Therapeutics 2003;25:2037–52.
6. Yaegaki K, Coil JM. Examination classification and
treatment of halitosis; clinical perspectives. Journal of the
Canadian Dental Association 2000;66:257–61.
7. Meskin LH. A breath of fresh air. Journal of the American
Dental Association 1996;127:1282–6.
8. Miyazaki H, Sakao S, Katoh Y, Takehara T. Correlation
between volatile sulphur compounds and certain oral
health measurements in the general population. Journal of
Periodontology 1995;66:679–84.
9. Taani DQ. Periodontal awareness and knowledge, and
pattern of dental attendance among adults in Jordan.
International Dental Journal 2002;52:94–8.
10. Liu XN, Shinada K, Chen XC, Zhang BX, Yaegaki K,
Kawaguchi Y. Oral malodor-related parameters in the
Chinese general population. Journal of Clinical Periodontology
2006;33:31–6.
11. Delanghe G, Ghyselen J, van Steenberghe D. Experiences of
a Belgian multidisciplinary breath odour clinic. Acta
Otorhinolaryngology Belgica 1997;51:43–8.
12. Yaegaki K, Sanada K. Volatile sulfur compounds in mouth
air from clinically healthy subjects and patients with
periodontal disease. Journal of Periodontal Research
1992;27:233–8.
13. Yaegaki K, Sanada K. Biochemical and clinical factors
influencing oral malodor in periodontal patients. Journal of
Periodontology 1992;63:783–9.
 journal of dentistry 35 (2007) 627–635
14. Morita M, Wang H-L. Relationship of sulcular sulfide level
to severity of periodontal disease and BANA test. Journal of
Periodontology 2001;72:74–8.
15. Morita M, Wang H-L. Relationship between sulcular sulfide
level and oral malodor subjects with periodontal disease.
Journal of Periodontology 2001;72:79–84.
16. Morita M, Musinski DL, Wang H-L. Assessment of newly
developed tongue sulfide probe for detecting oral malodor.
Journal of Clinical Periodontology 2001;28:494–6.
17. Kleinberg I, Wolff MS, Codipilly DM. Role of saliva in oral
dryness, oral feel and oral malodour. International Dental
Journal 2002;52:236–40.
18. Hinode D, Fukui M, Yokoyama N, Yokoyama M, Yoshioka
M, Nakamura R. Relationship between tongue coating and
secretory-immunoglobulin A level in saliva obtained from
patients complaining of oral malodour. Journal of Clinical
Periodontology 2003;30:1017–23.
19. van Steenberghe D. Breath malodour: a step by step
approach. Copenhagen: Quintessence Publishing; 2004.
20. McNamara TF, Alexander JF, Lee M, Plains M. The role of
microorganisms in the production of oral malodor. Oral
Surgery Oral Medicine and Oral Pathology 1972;34:41–8.
21. Persson S, Claesson R, Carlsson J. The capacity of
subgingival microbiotas to produce volatile sulfur
compounds in human serum. Oral Microbiology and
Immunology 1989;4:169–72.
22. Persson S, Edlund MB, Claesson R, Carlsson J. The
formation of hydrogen sulfide and methyl mercaptan by
oral bacteria. Oral Microbiology and Immunology 1990;5:195–
201.
23. Kleinberg I, Westbay G. Salivary and metabolic factors
involved in oral malodor formation. Journal of Periodontology
1992;63:768–75.
24. Wåler SM. On the transformation of sulfur-containing
amino acids and peptides to volatile sulfur compounds
(VSC) in the human mouth. European Journal of Oral Sciences
1997;105:534–7.
25. Kleinberg I, Codipilly M. Modeling of the oral malodor
system and methods of analysis. Quintessence International
1999;30:357–69.
26. Sterer N, Greenstein RB-N, Rosenberg M. b-Galactosidase
activity in saliva is associated with oral malodor. Journal of
Dental Research 2002;81:182–5.
27. Sterer N, Rosenberg M. Effect of deglycosylation of salivary
glycoproteins on oral malodour production. International
Dental Journal 2002;52:229–32.
28. Schmidt NF, Missan SR, Tarbet WJ, Cooper AD. The
correlation between organoleptic mouth-odor ratings and
levels of volatile sulfur compounds. Oral Surgery Oral
Medicine and Oral Pathology 1978;45:560–7.
29. Tonzetich J, Coil JM, Ng W. Gas chromatographic method
for trapping and detection of volatile gas compounds from
human mouth air. Journal of Clinical Dentistry 1991;2:79–82.
30. Goldberg S, Kozlovsky A, Gordon D, Gelernter I, Sintov A,
Rosenberg M. Cadaverine as a putative component of oral
malodor. Journal of Dental Research 1994;73:1168–72.
31. Amano A, Yoshida Y, Oho T, Koga T. Monitoring ammonia
to assess halitosis. Oral Surgery Oral Medicine Oral Pathology
Oral Radiology and Endodontology 2002;94:692–6.
32. Loesche WJ, Kazor C. Microbiology and treatment of
halitosis. Periodontology 2000 2002;28:256–79.
33. Kato H, Yoshida A, Awano S, Ansai T, Takehara T.
Quantitative detection of volatile sulphur compound-
producing microorganisms in oral specimens using real-
time PCR. Oral Diseases 2005;11:67–71.
34. Donaldson AC, McKenzie D, Riggio MP, Hodge PJ, Rolph H,
Flanagan A, et al. Microbiological culture analysis of the
tongue anaerobic microflora in subjects with and without
halitosis. Oral Diseases 2005;11:61–3.
633
35. Washio J, Sato T, Koseki T, Takahashi N. Hydrogen sulfide-
producing bacteria in tongue biofilm and their relationship
with oral malodour. Journal of Medical Microbiology
2005;54:889–95.
36. De Boever EH, De Uzeda M, Loesche WJ. Relationship
between volatile sulfur compounds. BANA-hydrolizing
bacteria and gingival health in patients with and without
complaints of oral malodor. The Journal of Clinical Dentistry
1994;4:114–9.
37. Claesson R, Edlund MB, Persson S, Carlsson J. Production of
volatile sulfur compounds by various Fusobacterium
species. Oral Microbiology and Immunology 1990;5:137–42.
38. Tang-Larsen J, Claesson R, Edlund MB, Carlsson J.
Competition for peptides and amino acids among
periodontal bacteria. Journal of Periodontal Research
1995;30:390–5.
39. Turng BF, Guthmiller JM, Minah GE, Falkler Jr WA.
Development and evaluation of a selective and differential
medium for the primary isolation of Peptostreptococcus
micros. Oral Microbiology and Immunology 1996;11:356–61.
40. Higuchi Y, Yagi T. Liberation of hydrogen sulfide during the
catalytic action of desulfovibrio hydrogenase under the
atmosphere of hydrogen. Biochemical and Biophysical
Research Community 1999;255:295–9.
41. Langendijk PS, Hagemann J, van der Hoeven JS. Sulfate-
reducing bacteria in periodontal pockets and in healthy
oral sites. Journal of Clinical Periodontology 1999;26:596–9.
42. Awano S, Gohara K, Kurihara E, Ansai T, Takehara T. The
relationship between the presence of
periodontopathogenic bacteria in saliva and halitosis.
International Dental Journal 2002;52:212–6.
43. Nakano Y, Yoshimura M, Koga T. Methyl mercaptan
production by periodontal bacteria. International Dental
Journal 2002;52:217–20.
44. Kazor CE, Mitchell PM, Lee AM, Stokes LN, Loesche WJ,
Dewhirst E, et al. Diversity of bacterial populations on the
tongue dorsa of patients with halitosis and healthy
patients. Journal of Clinical Microbiology 2003;41:558–63.
45. Senpuku H, Tada A, Yamaga T, Hanada N, Miyazaki H.
Relationship between volatile sulphide compounds
concentration and oral bacteria species detection in the
elderly. International Dental Journal 2004;54:149–53.
46. Krespi YP, Shrime MG, Kacker A. The relationship between
oral malodor and volatile sulfur compound-producing
bacteria. Otolaryngology-Head and Neck Surgery
2006;135:671–6.
47. Amir E, Shimonov R, Rosenberg M. Halitosis in children.
The Journal of Pediatrics 1999;134:338–43.
48. Poelmans J, Tack J, Feenstra L. Prospective study on the
incidence of chronic ear complaints related to
gastroesophageal reflux and on the outcome of antireflux
therapy. Annals of Otology Rhinology & Laryngology
2002;111:933–8.
49. Ratcliff PA, Johnson PW. The relation between oral
malodor, gingivitis, and periodontitis. A review. Journal of
Periodontology 1999;70:485–9.
50. Söder B, Johansson B, Söder PO. The relationship between
foetor ex ore, oral hygiene and periodontal disease. Swedish
Dental Journal 2000;24:73–82.
51. Bosy A, Kulkarni GV, Rosenberg M, McCulloch CA.
Relationship of oral malodor to periodontitis: evidence of
independence in discrete subpopulations. Journal of
Periodontology 1994;65:37–46.
52. Stamou E, Kozlovsky A, Rosenberg M. Association between
oral malodour and periodontal disease-related parameters
in a population of 71 Israelis. Oral Diseases 2005;11:72–4.
53. Rosenberg M. Bad breath and periodontal disease: how
related are they? Journal of Clinical Periodontology 2006;33:
29–30.
634 journal of dentistry 35 (2007) 627–635
54. Koshimune S, Awano S, Gohara K, Kurihara E, Ansai T,
Takehara T. Low salivary flow and volatile sulfur
compounds in mouth air. Oral Surgery Oral Medicine Oral
Pathology Oral Radiology and Endodontology 2003;96:38–41.
55. Quirynen M, van Eldere J, Pauwels M, Bollen CM, van
Steenberghe D. In vitro volatile sulfur compound
production of oral bacteria in different culture media.
Quintessence International 1999;30:351–6.
56. Kleinberg I, Codipilly DM. Cysteine challenge testing: a
powerful tool for examining oral malodour processes and
treatments in vivo. International Dental Journal 2002;52:221–8.
57. Rösing CK, Jonski G, Rølla G. Comparative analysis of some
mouthrinses on the production of volatile sulfur-
containing compounds. Acta Odontologica Scandinavica
2002;60:10–2.
58. Kostelc JG, Preti G, Zelson PR, Brauner L, Baehni P. Oral
odors in early experimental gingivitis. Journal of Periodontal
Research 1984;19:303–12.
59. Quirynen M, Zhao H, van Steenberge D. Review of the
treatment strategies for oral malodour. Clinical Oral
Investigations 2002;6:1–10.
60. van den Broek AMWT, Feenstra L, de Baat C. A review of
the current literature on management of halitosis. Oral
Diseases 2007; 13, in press.
61. Attia EL, Marshall KG. Halitosis. Canadian Medical Association
Journal 1982;126:1281–5.
62. Preti G, Clark L, Cowart BJ, Feldman RS, Lowry LD, Weber E,
et al. Non-oral etiologies of oral malodor and altered
chemosensation. Journal of Periodontology 1992;63:790–6.
63. Tomas Carmona I, Limeres Posse J, Diz Dios P, Fernandez
Feijoo J, Vazquez Garcia E. Extraoral etiology of halitosis.
Medicina Oral 2001;6:40–7.
64. Tangerman A. Halitosis in medicine: a review. International
Dental Journal 2002;52:201–6.
65. Kurihara E, Marcondes FK. Oral concentration of volatile
sulphur compounds in stressed rats. Stress 2002;5:295–8.
66. Queiroz CS, Hayacibara MF, Tabchoury CPM, Marcondes
FK, Cury JA. Relationship between stressful situations,
salivary flow rate and oral volatile sulfur-containing
compounds. European Journal of Oral Sciences 2002;110:337–
40.
67. Calil CM, Marcondes FK. Influence of anxiety on the
production of oral volatile sulphur compounds. Life Sciences
2006;79:660–4.
68. Ermis B, Aslan T, Beder L, Unalacak M. A randomized
placebo-controlled trial of mebendazole for halitosis.
Archives of Pediatric and Adolescent Medicine 2002;156:995–8.
69. Finkelstein Y, Talmi YP, Zohar Y, Ophir D. Endoscopic
diagnosis and treatment of persistent halitosis after
pharyngeal flap surgery. Plastic Reconstructive Surgery
1993;92:1176–8.
70. Miyahara H, Matsunaga T. Tornwaldt’s disease. Acta
Otolaryngology Supplement 1994;517:36–9.
71. Lewis M, McClay JE, Schochet P. Lingual tonsillectomy for
refractory paroxysmal cough. International Journal of
Pediatric Otorhinolaryngology 2000;53:63–6.
72. Tatli MM, San I, Karaoglanoglu M. Paranasal sinus
computed tomographic findings of children with chronic
cough. International Journal of Pediatric Otorhinolaryngology
2001;60:213–7.
73. Kurul S, Kandogan T. Pharyngeal foreign body in a child
persisting for three years. Emergency Medicine Journal
2002;19:361–2.
74. Stoeckli SJ, Schmid S. Endoscopic stapler-assisted
diverticuloesophagostomy for Zenker’s diverticulum:
patient satisfaction and subjective relief of symptoms.
Surgery 2002;131:158–62.
75. Candelli M, Rigante D, Marietti G, Nista EC, Crea F,
Bartolozzi F, et al. Helicobacter pylori, gastrointestinal
symptoms, and metabolic control in young type 1 diabetes
mellitus patients. Pediatrics 2003;111:800–3.
76. Ansai T, Takehara T. Tonsillolith as a halitosis-inducing
factor. British Dental Journal 2005;198:263–4.
77. Katz J, Shenkman A, Stavropoulos F, Melzer E. Oral signs
and symptoms in relation to disease activity and site of
involvement in patients with inflammatory bowel disease.
Oral Diseases 2003;9:34–40.
78. Santarelli L, Gabrielli M, Candelli M, Cremonini F, Nista EC,
Cammarota G, et al. Post-cholecystectomy alkaline reactive
gastritis: a randomized trial comparing sucralfate versus
rabeprazole or no treatment. European Journal of
Gastroenterology & Hepatology 2003;15:975–9.
79. Adler I, Denninghoff VC, Alvarez MI, Avagnina A, Yoshida
R, Elsner B. Helicobacter pylori associated with glossitis and
halitosis. Helicobacter 2005;10:312–7.
80. Gebara ECE, Faria CM, Pannuti C, Chehter L, Mayer MPA,
Lima LAPA. Persistence of Helicobacter pylori in the oral
cavity after systemic eradication therapy. Journal of Clinical
Periodontology 2006;33:329–33.
81. Rosenberg M, Gelernter I, Barki M, Bar-Ness R. Day-long
reduction of oral malodor by a two-phase oil:water
mouthrinse as compared to chlorhexidine and placebo
rinses. Journal of Periodontology 1992;63:39–43.
82. Greenman J, El-Maaytah M, Duffield J, Spencer P, Rosenberg
M, Corry D, et al. Assessing the relationship between
concentrations of malodor compounds and odor scores
from judges. Journal of the American Dental Association
2005;136:749–57.
83. Rosenberg M, Septon I, Eli I, Bar-Ness R, Gelernter I,
Brenner S, et al. Halitosis measurement by an industrial
sulphide monitor. Journal of Periodontology 1991;62:
487–9.
84. Zusho H, Asaka H, Okamoto M. Diagnosis of olfactory
disturbance. Auris Nasus Larynx 1981;8:19–26.
85. Saad S, Greenman J, Duffield J, Sudlow K. Use of n-butanol
as an odorant to standardize the organoleptic scale of
breath odour judges. Oral Diseases 2005;11:45–7.
86. Oho T, Yoshida Y, Shimazaki Y, Yamashita Y, Koga T.
Characteristics of patients complaining of halitosis and the
usefulness of gas chromatography for diagnosing halitosis.
Oral Surgery Oral Medicine Oral Pathology Oral Radiology and
Endodontology 2001;91:531–4.
87. Nachnani S, Majerus G, Lenton P, Hodges J, Magallanes E.
Effects of training on odor judges scoring intensity. Oral
Diseases 2005;11:40–4.
88. Kozlovsky A, Gordon D, Gelernter I, Loesche WJ, Rosenberg
M. Correlation between the BANA test and oral malodor
parameters. Journal of Dental Research 1994;73:1036–42.
89. Rosenberg M. Clinical assessment of bad breath: current
concepts. Journal of the American Dental Association
1996;127:475–82.
90. Greenstein RB-N, Goldberg S, Marku-Cohen S, Sterer N,
Rosenberg M. Reduction of oral malodor by oxidizing
lozenges. Journal of Periodontology 1997;68:1176–81.
91. Tonzetich J. Direct gas chromatographic analysis of
sulphur compounds in mouth air in man. Archives of Oral
Biology 1971;16:587–97.
92. Murata T, Yamaga T, Iida T, Miyazaki H, Yaegaki K.
Classification and examination of halitosis. International
Dental Journal 2002;52:181–6.
93. Solis-Gaffar MC, Niles HP, Rainieri WC, Kestenbaum RC.
Instrumental evaluation of mouth odor in a human clinical
study. Journal of Dental Research 1975;54:351–7.
94. Persson S. Hydrogen sulfide and methyl mercaptan in
periodontal pockets. Oral Microbiology and Immunology
1992;7:378–9.
95. Furne J, Majerus G, Lenton P, Springfield J, Levitt DG, Levitt
MD. Comparison of volatile sulfur compound
 journal of dentistry 35 (2007) 627–635
concentrations measured with a sulfide detector vs. gas
chromatography. Journal of Dental Research 2002;81:140–3.
96. Hunter CM, Niles HP, Vazquez J, Kloos C, Subramanyam R,
Williams MI, et al. Breath odor evaluation by detection of
volatile sulphur compounds—correlation with
organoleptic odor ratings. Oral Diseases 2005;11:48–50.
97. Aizawa F, Kishi M, Moriya T, Takahashi M, Inaba D,
Yonemitsu M. The analysis of characteristics of elderly
people with high VSC level. Oral Diseases 2005;11:80–2.
98. Rosenberg M, Kulkarni GV, Bosy A, McCulloch CAG.
Reproducibility and sensitivity of oral malodor
measurements with a portable sulphide monitor. Journal of
Dental Research 1991;70:1436–40.
99. Kozlovsky A, Goldberg S, Natour I, Rogatky-Gat A, Gelernter
I, Rosenberg M. Efficacy of a 2-phase oil:water mouthrinse
in controlling oral malodour, gingivitis, and plaque. Journal
of Periodontology 1996;67:577–82.
100. Quirynen M, Zhao H, Avondtroodt P, Soers C, Pauwels M,
Coucke W, et al. A salivary incubation test for evaluation of
oral malodor: a pilot study. Journal of Periodontology
2003;74:937–44.
101. Phillips M, Cateneo RN, Greenberg J, Munawar MI,
Nachnani S, Samtani S. Pilot study of a breath test for
volatile organic compounds associated with oral malodor:
evidence for the role of oxidative stress. Oral Diseases
2005;11:32–4.
102. Sopapornamorn P, Ueno M, Shinada K, Vachirarojpisan T,
Kawaguchi Y. Clinical application of a VSCs monitor for
oral malodour assessment. Oral Health & Preventive Dentistry
2006;4:91–7.
103. Sopapornamorn P, Ueno M, Shinada K, Vachirarojpisan T,
Shinada K, Kawaguchi Y. Association between oral
malodor and measurements obtained using a new sulfide
monitor. Journal of Dentistry 2006;34:770–4.
104. Loesche WJ, Bretz WA, Kerschensteiner D, Stoll J,
Socransky SS, Hujoel P, et al. Development of a diagnostic
test for anaerobic periodontal infections based on plaque
hydrolysis of benzoyl-DL-arginine-naphthylamide. Journal
of Clinical Microbiology 1990;28:1551–9.
105. Loesche WJ, Lopatin DE, Giordano J, Alcoforado G, Hujoel P.
Comparison of the benzoyl-DL-arginine-naphthylamide
(BANA) test, DNA probes, and immunological reagents for
ability to detect anaerobic periodontal infections due to
Porphyromonas gingivalis, Treponema denticola and Bacteroides
forsythus. Journal of Clinical Microbiology 1992;30:427–33.
106. Figueiredo LC, Rosetti EP, Marcantonio Jr E, Marcantonio
RAC, Salvador SL. The relationship of oral malodor in
patients with or without periodontal disease. Journal of
Periodontology 2002;73:1338–42.
635
107. Shimura M, Yasuno Y, Iwakura M, Shimada Y, Sakai S,
Suzuki K, et al. A new monitor with a zinc-oxide thin film
semiconductor sensor for the measurement of volatile
sulfur compounds in mouth air. Journal of Periodontology
1996;67:396–402.
108. Shimura M, Watanabe S, Iwakura M, Oshikiri Y, Kusumoto
M, Ikawa K, et al. Correlation between measurements using
a new halitosis monitor and organoleptic assessment.
Journal of Periodontology 1997;68:1182–5.
109. Tanaka M, Anguri H, Nonaka A, Kataoka K, Nagata H, Kita J,
et al. Clinical assessment of oral malodor by the
electronic nose system. Journal of Dental Research
2004;83:317–21.
110. Nonaka A, Tanaka M, Anguri H, Nagata H, Kita J,
Shizukuishi S. Clinical assessment of oral malodour
intensity expressed as absolute value using an electronic
nose. Oral Diseases 2005;11:35–6.
111. Minamide T, Mitsubayashi K, Jaffrezic-Renault N, Hibi K,
Endo H, Saito H. Bioelectronic detector with monoamine
oxidase for halitosis monitoring. The Analyst
2005;130:1490–4.
112. Toda K, Li J, Dasgupta PK. Measurement of ammonia in
human breath with a liquid-film conductivity sensor.
Analytical Chemistry 2006;78:7284–91.
113. Murata T, Rahardjo A, Fujiyama Y, Yamaga T, Hanada M,
Yaegaki K, et al. Development of a compact and simple gas
chromatography for oral malodor measurement. Journal of
Periodontology 2006;77:1142–7.
114. Iwanicka-Grzegorek K, Lipkowska E, Kepa J, Michalik J,
Wierzbicka M. Comparison of ninhydrin method of
detecting amine compounds with other methods
of halitosis detection. Oral Diseases 2005;11:
37–9.
115. Suzuki N, Yoshida A, Nakano Y. Quantitative analysis of
multi-species oral biofilms by TaqMan real-time PCR.
Clinical Medicine & Research 2005;3:176–85.
116. American Dental Association. Products used in the
management of oral malodor. Chicago: American Dental
Association, Council on Scientific Affairs; 2003.
117. Greenman J, Rosenberg M. Proceedings of the sixth
international conference on breath odor. Oral Diseases
2005;11:5–6.
118. Donaldson AC, Riggio MP, Rolph HJ, Bagg J, Hodge PJ.
Clinical examination of subjects with halitosis. Oral
Diseases 2007;13:63–70.
119. Willis CL, Gibson GR, Holt J, Allison C. Negative correlation
between oral malodour and numbers and activities of
sulphate-reducing bacteria in the human mouth. Archives
of Oral Biology 1999;44:665–70.