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Halitology (breath odour: Aetiopathogenesis

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INVITED MEDICAL REVIEW
Halitology (breath odour: aetiopathogenesis and
management)
C Scully1, J Greenman2
1
Department of Oral Medicine, University of Bristol, Bristol, UK; 2Faculty of Health and Life Sciences, University of West of
England, Bristol, UK
This article reviews the aetiopathogenesis of halitosis (oral
malodour) and management. Halitosis is any disagreeable
breath odour. In most patients, the odour originates from
the oral cavity. In some patients, it has an extra-oral
aetiology and, in a few, metabolic anomalies are respon-
sible. In other patients complaining of malodour, this is
imagined rather than real. Volatile sulphur compounds
(VSCs) and other elements appear largely responsible for
the malodour. Predisposing factors include poor oral hy-
giene, hyposalivation, dental appliances, gingival and
periodontal disease and mucosal disease. The first step in
assessment is objective measurement to determine whe-
ther malodour is present. If present, the oral or extra-oral
origin should be determined, because the latter requires
medical investigation and support in therapy, as is also the
case where the malodour is imagined rather than real.
Oral malodour is managed largely by oral health
improvement, plus use of one or more of the wide range of
antimalodour therapies, and sometimes also with use of a
malodour counteractive. Emergent treatments include
probiotics and vaccines targeted against causal micro-
organisms or their products.
Oral Diseases (2012) 18, 333–345
Keywords: halitosis; malodor; volatile sulphur compounds; oral;
trimethylaminuria, psychoses, hypochondriasis, tongue, plaque
toothpastes; mouthwashes; tongue; probiotics, vaccines
Introduction
Humans can emit a variety of volatile and non-volatile
molecules in body fluids that are influenced by genetics,
diet, stress and disease. Oral malodour is an alternative
term used. This subject has been reviewed by a number
Correspondence: Crispian Scully, CBE, Bristol Dental Hospital,
University of Bristol, Bristol, BS1 2LY, UK. Tel: +44(0) 203 456
1170, Fax: +44(0) 117 923 0000, E-mail: Crispian.scully@ ucl.ac.uk
Based upon presentations at the CED-IADR, Budapest, 2011.
Received 23 November 2011; revised 7 December 2011; accepted 8
December 2011
Oral Diseases (2012) 18, 333–345 doi:10.1111/j.1601-0825.2011.01890.x
 2011 John Wiley & Sons A/S
All rights reserved
www.wiley.com
of authors (Rosenberg, 1996; Sanz et al, 2001; Nach-
nani, 2011), including us (Scully et al, 1994, 1997;
El-Maaytah et al, 1996; Scully and Rosenberg, 2003;
Porter and Scully, 2006; Scully and Porter, 2006; Scully
and Greenman, 2008) but, in view of several recent
advances, we review the subject here.
Prevalence of oral malodour
Oral malodour is a common complaint, analogous to
body odour (Lee et al, 2007), often causing embarrass-
ment and affecting interpersonal social communication
(Bosy, 1997).
The prevalence of oral malodour is unclear, not least
because available epidemiological data are based mainly
on subjective self-estimation of malodour, which is
limited in accuracy and sensitivity. However, studies
estimate that 30–50% of the population have oral
malodour (Tessier and Kulkarni, 1991; Sanz et al, 2001;
Liu et al, 2006; Outhouse et al, 2006). However, some
studies show a lower prevalence; for example, the
prevalence in a recent study was only 15%, but 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
(Nadanovsky et al, 2007). Oral malodour may rank only
behind dental caries and periodontal disease as the cause
of patient’s visits to the dentist, but the perception of
malodour is different in culturally diverse populations
(Rayman and Almas, 2008).
Types of breath odour
Several terms describe and characterise the different
aspects of oral malodour (Table 1). Causes are shown in
Figure 1.
Physiologic halitosis
Oral malodour is quite common on awakening (Ômorn-
ing breath’ also known as physiologic halitosis) and this
 Breath odour diagnosis and management
C Scully and J Greenman

334
Table 1 Terminology related to oral malodour

Terms used Definition

Halitosis Any disagreeable odour of expired air, regardless of origin

Bad breath Lay term for halitosis
Genuine halitosis Breath malodour that can be verified objectively

Physiologic halitosis, also termed transient halitosis e.g. morning breath or lifestyle malodours
Pathologic halitosis Subclassified into (i) oral and (ii) extra-oral

Oral malodour Pathologic halitosis originating from the oral cavity Foetor oris
Foetor ex oris
Extra-oral malodour Pathologic halitosis originating from outwith the oral cavity
Pseudohalitosis Breath malodour that cannot be verified objectively (the patient initially thinks that they have malodour but
there is no objective evidence of it. Patient eventually accepts that they do not have malodour)
Halitophobia Breath malodour that can not be verified objectively (the patient persists in believing they have malodour
despite evidence to the contrary (a monosymptomatic delusional hypochondriasis)

smoke (Stedman, 1968) but tobacco also predisposes to

Malodour
Pseudohalitosis Genuine halitosis
Halitophobia Physiological Pathological
halitosis halitosis
Foods, Oral Extraoral
poor oral
hygiene
Respiratory Non-
etc
Respiratory
Metabolic Hepatic
Figure 1 Causes of oral malodour
malodour is transient, probably related to normal
nocturnal hyposalivation and is rarely of any special
significance. (Scully et al, 1994; Sanz et al, 2001; Out-
house et al, 2006; Porter and Scully, 2006; Fukui et al,
2008), probably resulting from increased microbial
metabolic activity during sleep. Malodour is also
aggravated by menstruation (Kawamoto et al, 2010).
Starvation can lead to a similar malodour.
Physiologic malodour forms can usually be readily
rectified by eating, toothbrushing and tongue brushing
or scraping and rinsing the mouth with fresh water
(Faveri et al, 2006). Tongue cleansing with a scraper
appears unable to prevent morning breath in the
absence of tooth cleaning in periodontally healthy
individuals (Haas et al, 2007; Allaker et al, 2008).
Lifestyle oral malodour
Oral malodour at other times may be the consequence of
lifestyle habits, such as smoking tobacco or drinking
alcohol, or the ingestion of odiferous food and drinks
(e.g. garlic, onion, durian or spices, cabbage, cauliflower
and radish (Suarez et al, 1999). Tobacco smoke contains
volatile sulphur compounds (VSC), which are at least
partly responsible for the oral malodour of people who
hyposalivation and periodontal disease – other causes of
malodour. Alcohol intake may predict oral malodour
(Rosenberg et al, 2007). The avoidance of these habits
and foods is the best prevention.
Pathologic malodour
Halitosis from oral causes
In most patients with persistent malodour (about 85%),
the odour originates from the oral cavity (Delanghe
et al, 1997; Eldarrat, 2011) mainly from bacterial
activity (Allaker, 2009). It is probable that several
bacterial species (mainly Gram-negative anaerobes) are
responsible, because no single-specific species has been
Renal
associated (Box 1). Solobacterium moorei has been
found to be present in all subjects with malodour but
not controls, suggesting some distinct bacterial species
are associated (Haraszthy et al, 2007). The tongue
dorsum is the location of many of the bacteria impli-
cated in oral malodour.
Bacterial interactions with specific substrates, such as
cysteine, methionine, tryptophan, arginine and lysine,
biotransforms them into odiferous hydrogen sulphide,
methylmercaptan, indole, putrescine and cadaverine,
respectively (Greenman, 1999). These, other amino acids
Box 1 Main micro-organisms associated with halitosis (in alphabetical
order only)
Bacteroides loescheii
Centipeda periodontii
Eikenella corrodens
Enterobacteriaceae
Fusobacterium nucleatum nucleatum
Fusobacterium nucleatum polymorphum
Fusobacterium nucleatum vincentii
Fusobacterium periodonticum
Porphyromonas endodontalis
Porphyromonas gingivalis
Prevotella (Bacteroides) melaninogenica
Prevotella intermedia
Solobacterium moorei
Tannerella forsythensis (Bacteroides forsythus)
Treponema denticola

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 Breath odour diagnosis and management
C Scully and J Greenman

335
Table 2 Odiferous compounds that may cause or contribute towards The microbial degradation of cysteine produces H2S
oral malodour and the sufhydryl anion (HS)), a strong reducing agent
that drops the redox potential (Eh) within the tongue
Group of compounds Examples biofilm (Kleinberg and Codipilly, 2008), favouring the
Volatile sulphur Hydrogen sulphide growth of anaerobes (McNamara et al, 1972), and
compounds (VSCs) Methyl mercaptan activating thiol-dependent enzymes including trypsin-
Dimethyl sulphide like protease, important in the putrefaction process
Polyamines Cadaverine (Smalley et al, 1994) and cysteine desulfhydrase (the
Putrescine
Trimethylamine very same enzyme responsible for H2S ⁄ HS) production
(microbial generation) in the first place).
Short-chain fatty acids Acetic acid Acetone, 2-butanone, 2-pentanone and 1-propanol
Butyric acid are also common to all volunteers with halitosis and
Propionic acid
Valeric acid
appear in both alveolar and mouth air, and indole and
Indoles Indole dimethyl selenide are found in alveolar air (van den
Methyl-indole (skatole) Velde et al, 2007). Most of the VCs appear to be
Pyridiene produced endogenously and ⁄ or in the mouth (van den
Velde et al, 2007).
and sugars, can also be fermented into short-chain Persistent malodour because of oral causes usually
organic acids (Table 2). Salivary mucins may also be a originates from the posterior dorsum of tongue and ⁄ or
source of primary substrates and microbial deglycosy- oral ⁄ dental diseases, including periodontal disease,
lation may be a step prior to full proteolytic digestion being most likely where food and bacterial plaque ⁄ bio-
(Sterer et al, 2002) (Figure 2). film accumulate and anaerobic ecosystems develop.
Two theories of microbial aetiology include a Ôspecific Predisposing factors include poor oral hygiene, hypos-
theory’ (a few Ôsingle’ bacterial species are aetiological alivation, dental appliances, gingival and periodontal
and capable of causing malodour) and a Ônon-specific’ disease and mucosal disease (Table 3). (Scully et al,
theory – many species are involved. Anaerobes, pre- 1994; Yaegaki and Coil, 2000; Sanz et al, 2001; Koshi-
dominantly Gram-negative, are certainly important mune et al, 2003; Outhouse et al, 2006; Porter and
(Scully et al, 1994; Hartley et al, 1996, 1999; Yaegaki Scully, 2006; Sterer et al, 2008; Babacan et al, 2011).
and Coil, 2000; Sanz et al, 2001; Outhouse et al, 2006;
Porter and Scully, 2006). Tongue biofilm
These anaerobes produce malodorous volatile com-
pounds (VCs), which include (Krespi et al, 2006) Malodour of oral origin arises mainly from the resident
(Table 2): microbes on the dorsum of the tongue, and there is a
relationship between the quantity of microbes present
• VSCs, particularly hydrogen sulphide H2S and (biofilm amount) and the degree of odour (Hartley et al,
methyl mercaptan CH3SH, – the main contributors 1996, 1999). Methods to measure the amount of tongue
to oral malodour. Dimethyl sulphide CH3SCH3 is biofilm include (i) aerial density of microbes (cfu cm)2)
the main VSC contributing to extra-oral and blood- determined from tongue scrapes sampled from a mea-
borne halitosis (Tangerman and Winkel, 2007) but sured area of the surface and (ii) a tongue-coating index,
may also contribute to oral malodour. where a judge assesses the amount of Ôcoating’ by visual
• short-chain fatty acids (acetic, propionic, butyric inspection (Gomez et al, 2001; Winkel et al, 2003;
and valeric acids). Lundgren et al, 2007; Kim et al, 2009).
• polyamines (putrescine, cadaverine and [microbially
produced] trimethylamine).
• indoles (skatole and indole).
Table 3 Main oral causes of malodour
Volatile
products Tongue biofilm coating Poor hygiene, soft diet, appliances and
smoking
Bacteria Plaque-related gingival Gingivitis, periodontitis, acute necrotising
Hydrogen
sulphide and periodontal disease ulcerative gingivitis, pericoronitis and
abscesses
Aminoacids H2S
Ulceration Systemic disease (inflammatory ⁄ infectious
e.g. disorders, cutaneous, gastrointestinal and
cysteine, Microbial enzymes Volatile Methyl
Cysteine haematological disease),
cysƟne,
desulphydrase Sulphur mercaptan
methionine malignancy, local causes, aphthae and
Methionine lyase
Compounds
CH3SH drugs
Tryptophanase
Decarboxylases Hyposalivation E.g. from drugs, Sjögren syndrome and
Dimethyl
Microbial cancer therapy
hydrolases disulphide Wearing dental Poor hygiene and candidosis
Debris (CH3)2SH appliances
Blood
Dental conditions Food packing and dental abscesses
Amines, acids Bone diseases Dry socket, osteomyelitis, osteonecrosis
and malignancy
Figure 2 Pathogenesis of oral malodour

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 Breath odour diagnosis and management
C Scully and J Greenman

336
Comparison of these two approaches (Saad and malodour. Tonsilloliths can cause malodour (Castellani,
Greenman, 2008) shows no correlation (R2 < 0.02) 1930; Rio et al, 2008). Cleft lip ⁄ palate may predispose
and biofilms of similar population densities (ca. log to malodour (Doruk et al, 2008). In adults, particularly,
7.5 cm)2) had widely different opacities depending on respiratory infections, such as tonsillitis, bronchitis or
the species present. Thus, some individuals can have a bronchiectasis, or neoplasms may be responsible:
high aerial density, but if most species present are 2-aminoacetophenone in the breath may reflect the
translucent, the biofilm does not appear as a coating. presence of Pseudomonas aeruginosa (Scott-Thomas
Others may have the same density of microbes, but et al, 2010).
because of the presence of more pigmented species (or
staining from exogenous sources such as coffee or Gastrointestinal disorders. Oral malodour is also a fre-
tobacco), they can be observed to have a thick coating quent symptom of gastro-oesophageal reflux disease
index. Therefore, the coating index is poor at estimating (GORD) (Moshkowitz et al, 2007; Struch et al, 2008).
the quantity of microbes and the degree of malodour. Bacteria such as Enterococcus faecalis and Helicobacter
Prevention and treatment of infective processes, pylori may be found in periodontal pockets (Souto and
improvement of oral hygiene and sometimes the use of Colombo, 2008) and H. pylori in particular should be
antimicrobial products therapy if necessary can usually considered as a possible cause of malodour (Adler et al,
prevent or manage this type of malodour (see below). 2005; Lee et al, 2006; Suzuki et al, 2008a). Although
some have not found an association between functional
Halitosis from extra-oral causes dyspepsia, peptic ulcer disease and H. pylori infection
Malodour only infrequently has extra-oral causes (Tan- with malodour occurrence or severity (Moshkowitz
german and Winkel, 2010), typically from respiratory, et al, 2007), H. pylori can produce VSCs (Lee et al,
gastrointestinal or metabolic causes (Table 4) 2006), and treatments have improved the malodour
(Kinberg et al, 2010). In one study, triple drug eradica-
Respiratory disorders. Respiratory disorders can result tion of H. pylori infection resulted in sustained resolu-
in odourous gases in the air expelled from the oral cavity tion of halitosis during long-term follow-up in the
and the nose (Table 4), (Castellani, 1930; Scully et al, majority (Katsinelos et al, 2007).
1994; Yaegaki and Coil, 2000; Sanz et al, 2001; Porter
and Scully, 2006; Rio et al, 2008). Children sometimes Metabolic disorders. Metabolic disorders which may result
insert foreign bodies such as small toys into the nose, in odiferous agents circulating in the bloodstream and
and the subsequent sepsis is a common cause of being exhaled into the breath causing malodour (also
known as blood-borne halitosis) are shown in Box 2.
Table 4 Extra-oral causes of halitosis
A number of VCs may be present in breath (Table 5),
but dimethyl sulphide appears to be the main
Respiratory system Antral malignancy
(microbial aetiology) Bronchiectasis
Bronchitis
Cleft palate Box 2 Metabolic disorders which may result in oral malodour
Foreign bodies in the nose
Lung infections Diabetes
Lung malignancy Hepatic disease
Nasal malignancy Renal disease
Pharyngeal malignancy Trimethylaminuria
Sinusitis Dimethylglycinuria
Tonsillitis Cystinosis
Tonsilloliths Hypermethioninaemia
Gastrointestinal tract Gastro-oesophageal reflux disease
Malignancy
Oesophageal diverticulum
Metabolic disorders Diabetes
Table 5 Volatile compounds in breath in metabolic disorders
(blood borne) Liver disease
Renal failure
Trimethylaminuria Condition Main volatiles
(fish odour syndrome)
Dimethylglycinuria Diabetes Ketone bodies e.g.
Hypermethioninaemia Acetone
Cystinosis Aniline
Drugs (blood borne) Amphetamines Methylacetone
Chemotherapy Propanol
Chloral hydrate Toluidine
Dimethyl sulphoxide Liver failure Hydrogen sulphide
Disulfiram Aliphatic acids
Nitrates and nitrites Ketones
Phenothiazines Methionine
Solvent abuse Renal failure Methyl mercaptan
Psychogenic causes Depression Dimethyl sulphide
Hypochondriasis Trimethylamine
Obsessive compulsive disorder Trimethylaminuria Trimethylamine

Oral Diseases

Trimethylaminuria
Liver flavin
monoxygenase
FMO3
TMA
Gastrointestinal TMA
Oxide
(odour)
(no odour)
Saliva
Food
Urine
Figure 3. Pathogenesis of trimethylaminuria
contributor to blood-borne halitosis (Tangerman and
Winkel, 2007). Patients with severe or end-stage meta-
bolic disorders may also have malodour because of
complicating oral or periodontal disease.
Trimethylaminuria (TMAU; fish odour syndrome) is
the main genetic cause of undiagnosed body odour,
characterised by excessive blood levels of trimethyl-
amine (TMA) as a consequence of an autosomal
recessive mutation in the enzyme flavin mono-oxygenase
3 (FMO3) (Mackay et al, 2011). TMA is excreted into
body fluids and breath, which leads to the persistent oral
and body malodour similar to that of rotting fish
(Figure 3). Many individuals affected with this rare
condition present with oral as well as body malodour,
and with dysguesia (Whittle et al, 2007).
Diagnosis of trimethylaminuria is by a random urine
TMA and TMA-N-oxide level assay; choline or marine
fish load test; and FMO3 mutational analysis. Manage-
ment is by
• Diet (avoiding eggs, fish and brassica)
• Riboflavin (increases FMO3 levels)
• Clearing the gut, using
s Antimicrobials (e.g. metronidazole)
s Lactulose
s Activated charcoal and copper chlorophyllin.
TMA levels are also increased in some women around
the time of menstruation (Shimizu et al, 2007) and in a
range of other conditions (Box 3).
Other rare metabolic disorders that can lead to oral
malodour include dimethylglycinuria, cystinosis and
Box 3 Conditions in which TMA may be increased
Anxiety and stress
Deficient nicotine N-oxidation
Disorders of carnitine and choline intake
Haematological abnormalities
Hepatic disease
Noonan syndrome
Prader–Willi syndrome
Renal disease
Turner syndrome
Breath odour diagnosis and management
C Scully and J Greenman
337
hypermethioninaemia. Dimethylglycinuria is character-
ised by homozygous mutation in dimethylglycine dehy-
drogenase (DMGDH) gene, deficiency of DMGDH, a
high concentration of DMG and increased serum
creatinine kinase (Moolenaar et al, 1999).
Cystinosis is another rare autosomal recessive disor-
der characterised by the intralysosomal accumulation of
cystine. Cysteamine removes cystine from the lysosomes
and slows down the progression of the disease but one of
its adverse effects is halitosis as it is converted to
dimethyl sulphide and methanethiol. The expired air of
cystinotic patients then contains raised levels of
dimethyl sulphide and methanethiol (Besouw et al,
2007).
Malodour can also arise as a side effect of drugs
containing a dimethyl sulphide structure (Murata et al,
2003). Hypermethioninaemia may arise in a range of
conditions (Mudd, 2011), including genetic and acquired
disorders (Table 6).
Psychogenic malodour
Psychogenic or psychosomatic factors may be at play in
some patients complaining of malodour. Anxiety
increases TMA and VSC levels (Calil and Marcondes,
2006). Neurotic patients may often complain of halitosis
(Suzuki et al, 2011), and depression may be seen in
pathological malodour (Suzuki et al, 2008b).
Not all persons who believe they have halitosis
actually have any objective malodour, and this Ôpseu-
do-halitosis’ can be a real clinical dilemma (Seemann
et al, 2006). In those in whom no objective evidence of
malodour can be detected, but the complaint persists, it
may then be attributed to a delusion or monosymptom-
atic hypochondriasis (self-halitosis, halitophobia).
Many such patients fail to recognise their psychological
condition and never doubt that they have oral mal-
odour. Other people’s behaviour or perceived behav-
iour, such as apparently covering the nose or averting
the face, is typically misinterpreted by these patients as
an indication that their breath is indeed offensive. Many
patients adopt behaviour to minimise their perceived
problem, such as covering the mouth when talking,
avoiding or keeping a distance from other people, using
products designed to reduce malodour or excessively
cleaning their tongue and ⁄ or mouth.
Table 6 Conditions associated with hypermethioninaemia
Genetic deficiency Acquired
Citrin –
Cystathionine b-synthase Liver disease
(homocystinuria)
Fumarylacetoacetate –
hydrolase (tyrosinaemia type I)
Glycine N-methyltransferase Ingestion of large amounts
of methionine.
Methionine adenosyltransferase Low-birthweight and ⁄ or
I and III prematurity
S-adenosylhomocysteine hydrolase –
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 Breath odour diagnosis and management
C Scully and J Greenman
338
Diagnosis
In view of the range of conditions that may give rise to a
complaint of malodour, a full history and oral exami-
nation are required in all cases, and in some, a medical
opinion and investigations may be in order.
The first step in assessment is an objective measure-
ment of breath odour to determine whether malodour is
actually present, because most individuals are poor
judges of their own breath odour (Eli et al, 2001). Three
objective methods of breath malodour measurement are
available viz, gas chromatography, halimetry (sulphide
monitoring) and organoleptic (hedonic) measurements.
Gas chromatography (GC) is preferred if precise
measurements of specific gases are required and is
considered by many to be the method of choice for
differentiating and quantifying the VSC and (especially
if it runs with a Mass Spectrometer [MS] Detector) can
also distinguish other classes of compound (e.g. indole).
Traditional laboratory GC or GC-MS machines, how-
ever, are cumbersome, need inert column carrier gas (gas
cylinders of nitrogen or helium) and require technicians
or specialists with adequate training–and are thus
clinically impractical (Yaegaki and Coil, 2000). How-
ever, a newly developed portable GC (OralChromaTM,
Abilit, Osaka, Japan; Envin Scientific Ltd. Technology
House, Chowley Oak, Tattenhall, Chester, Cheshire,
UK) to measure VSCs (Tangerman and Winkel, 2007),
which does not use special carrier gas (using air instead)
and is highly sensitive yet relatively low cost compared
with a standard gas chromatograph, is now available.
This can differentiate the three major sulphides. Some
centres are able to objectively measure VSCs using a
halimeter (Interscan Corp., Chatsworth, CA, USA), a
portable sulphide monitor, but this cannot differentiate
between the different sulphides and cannot detect other
classes of volatile compounds.
Assessment is thus generally based upon organoleptic
assessment of exhaled air, namely the clinician sniffs the
air exhaled from the mouth and nose and subjectively
confirms or denies the presence of malodour (Donald-
son et al, 2007). The intensity of breath odour is often
rated as follows (Rosenberg, 1996):
0 – Odour cannot be detected.
1 – Questionable malodour, barely detectable.
2 – Slight malodour, exceeds the threshold of mal-
odour recognition.
3 – Malodour is definitely detected.
4 – Strong malodour.
5 – Very strong malodour.
Smelling both nose and mouth air is important as
malodour detectable from the nose alone (asking the
patient to breath while the mouth is closed) is most
likely to originate from nose or sinuses, or elsewhere
in the respiratory tract or from the gastrointestinal
tract.
For the purposes of fine quantification (for example,
in clinical trials of the efficacy of antimalodour com-
pounds), it has been suggested that organoleptic assess-
ments should be performed by two or more different
examiners (Wozniak, 2005) and that both the subject
Oral Diseases
and the examiners should adhere to some instructions to
obtain more reliable results (Yaegaki and Coil, 2000).
However, a panel increases the standard deviation of
mean determinations (because on absolute terms one
judge is often different from another), but they both
maintain a good enough relative scale.
As a general rule, before the assessment, it is advisable
that the patient abstains from eating odiferous foods for
48 h before the assessment and that both the patient and
the examiner refrain from drinking coffee, tea or juice,
smoking and using scented cosmetics (Yaegaki and Coil,
2000).
Halimetry and gas chromatography are very reliable,
but not very easily clinically implemented methods, and
usually, the organoleptic measurement is suggested as
the Ôgold standard’.
Additional or alternative measurement methods, such
as BANA (benzoyl–arginine–naphthyl–amide) test,
chemical sensors, salivary incubation test, quantifying
beta-galactosidase activity, ammonia monitoring, nin-
hydrin method and polymerase chain reaction are
infrequently employed (van den Broek et al, 2007,
2008).
If no malodour can be found during the initial
examination, the assessment for halitosis should be
repeated on two or three different days. Thereafter, if
malodour is still not present, the patient can be
considered to be affected by imaginary (pseudohalitosis)
(Yaegaki and Coil, 2000).
To summarise, therefore, diagnosis of oral malodour
is mainly clinical made from a full history; examination;
objective assessment of halitosis, usually by simply
smelling the exhaled air (organoleptic method) first from
the mouth (with nose closed by pinching nostrils) then
from the nose (with patient’s mouth closed) or objective
measurements of the agents responsible, using a hali-
meter (Interscan Corp) or a portable gas chromatograph
(OralChroma; Envin Scientific Ltd).
Systemic causes if suspected need the opinion of the
relevant specialist and possibly, investigations such as
nasendoscopy, chest imaging, H. pylori serum antibody
or endoscopy and rapid urease test or biopsy, liver and
renal function tests and urinalysis for the ratio of
trimethylamine to trimethylamine oxide.
Management of halitosis owing to oral causes
The management of malodour depends largely on the
cause but avoiding smoking, drugs and foods that might
be responsible is always sensible. Eating regular meals is
important and finishing with a fibrous fruit or vegetable
may help.
In most patients, treatment is primarily directed
towards treating oral ⁄ dental diseases, reducing accumu-
lation of food debris and biofilm, and malodour-
producing oral bacteria by improving oral hygiene and
reducing the tongue coating and using oral malodour
counteractives (OMCs). The patient should use appro-
priate regular oral hygiene procedures which include
tooth cleaning (brushing and interdental flossing) and
tongue cleaning and use of antimicrobial toothpastes

and ⁄ or mouthwashes. Toothbrushing can reduce mal-
odour (Table 7). Gentle and regular tongue cleaning
(Danser et al, 2003) aimed at dislodging trapped food,
cells and bacteria from between the filiform papillae can
decrease VSC concentration and should be done at night
using a tongue scraper or a hard toothbrush and cold
water (as done early during the day may induce
retching). There is weak and unreliable evidence of a
small but statistically significant greater short-term
reduction of VSC levels when tongue scrapers or
cleaners are used rather than toothbrushes (Outhouse
et al, 2006).
A wide range of antimalodour therapies is available,
and Table 7 shows a comparison of various oral
malodour therapies or treatments made on the basis of
objective reduction of VSC or component gases (by gas
chromatography, halimeter or sensor) in comparison
with appropriate controls (trials where N > 10 sub-
jects).
The effectiveness of active antimalodour ingredients
in oral healthcare products is dependent on their
concentration, and above a certain concentration, the
ingredients can occasionally have unpleasant adverse
effects (van den Broek et al, 2007, 2008).
Toothpastes. Toothpastes containing triclosan and a
copolymer (Colgate Total Toothpaste; Colgate, Man-
chester, UK) provide effective control of breath odour at
12 h after brushing the teeth (Niles et al, 1999; Sharma
et al, 2007). Stannous-containing sodium fluoride denti-
frices can also reduce malodour (Feng et al, 2010).There
is significant immediate antimalodour activity for a
0.454% stabilised stannous fluoride sodium hexameta-
phosphate dentifrice (Farrell et al, 2007; Chen et al,
2010).
Mouthwashes. Mouthwashes are also widely available
and contain a range of ingredients. Generally, it is
recommended that mouthwashes should be used two or
three times daily for at least 30 s. Mouthwashes
containing chlorhexidine gluconate (CHX), cetylpyrid-
inium chloride (CPC) or triclosan, or a two-phase oil:
water chlorhexidine, cetylpyridinium chloride mouth-
wash may be beneficial against malodour (Pitts et al,
1981, 1983; Kozlovsky et al, 1996; Roldán et al, 2003,
2004, 2005; Scully and Porter, 2005, 2006). Good short-
term results have been reported with CHX, essential oils
and CPC for up to 2 or 3 h.
Metal ions and oxidising agents, such as hydrogen
peroxide, chlorine dioxide and iminium chloride, are
active in neutralising VSCs. Zinc chloride appears to
make VSCs non-volatile and also inhibits bacterial
cysteine proteases, hindering the breakdown of exfoli-
ated epithelial cells, which are partly responsible for
the production of VSCs (Yaegaki and Suetaka, 1989).
Zinc seems to be an effective safe metal at concentra-
tions of at least 1%: a combination of zinc and CHX
in low concentrations seems an efficient way to remove
the VSC (Thrane et al, 2007). Antimalodour agents
containing oxidising agents, such as zinc (Zn2+) and
stannous ions (Sn2+), chlorine dioxide (ClO2) and
Breath odour diagnosis and management
C Scully and J Greenman
339
sodium chlorate (NaClO2), are effective in the inhibition
of both H2S and Eh (Kleinberg and Codipilly, 2008).
Oral malodour counteractives. Cosmetic non-pharmaco-
logical methods, such as chewing gums may reduce
maldour (Tanaka et al, 2010) and have the added
advantage of stimulating salivation.
Parsley, mint, cloves or fennel seeds and the use of
proprietary Ôfresh breath’ preparations, usually merely
provide a temporary odour to mask the malodour (oral
malodour counteractives) (Outhouse et al, 2006).
Antibiotics. In recalcitrant cases, the specialist empirically
may use a 1-week course of metronidazole 200 mg three
times daily in an effort to eliminate unidentified anaer-
obic infections; this may reduce tongue microbiota and
malodour levels (Hartley et al, 1999).
To summarise, the management of oral malodour
includes:
• Patient education.
• Treatment of the cause: medical help may be
required to manage patients with a systemic
background to the complaint.
• Avoiding habits such as smoking, and foods such
as onions, garlic, durian, cabbage, cauliflower and
radish.
• Eating regular meals and finishing meals with
fibrous fruits ⁄ vegetables (e.g. carrots and pineap-
ple).
s Ensuring good oral hygiene – dental prophylaxis,
toothbrushing, flossing and tongue cleaning.
s Using oral healthcare products; there is evidence
of benefit mainly from the use of toothpastes and
mouthwashes.
s Using chewing gum and oral deodorants (oral
malodour counteractives [OMC]).
s In recalcitrant cases, the specialist empirically
may use a 1-week course of metronidazole
200 mg three times daily.
A combination of treatments typically helps (Scully
et al, 1994; Roldán et al, 2003, 2004, 2005; Scully and
Rosenberg, 2003; Scully and Felix, 2005; Farrell et al,
2006; Porter and Scully, 2006; Scully and Porter, 2006;
Farrell et al, 2007).
Emergent treatments. Emergent treatments include pro-
biotics (Teughels et al, 2008), Fusobacterium nucleatum
vaccines (Liu et al, 2009, 2010), myrsinoic acid – a
methionase inhibitor which inhibits VSC production
(Ito et al, 2010) and tea catechins which inhibit Por-
phyromonas gingivalis and VSC production (Xu et al,
2010).
Management of halitosis as a result of
extra-oral causes
Halitosis as a result of extra-oral causes is managed
through the treatment of the underlying cause and, as
discussed, medical help may be required.
Oral Diseases
 Table 7 Comparison of various oral malodour therapies or treatments made on the basis of reduction of VSC or component gases (by gas chromatography, halimeter or sensor) in comparison with 340

Oral Diseases
appropriate controls (trials where N > 10 subjects)

Statistical
significance of
malodour
Subjects reduction
Treatments Refs per group Comment Outcomes (measurement method) P

Professional oral health care (POHC)

POHC Adachi et al, 2002 37 Two-year study; test group received 60% CH3SH reduction (electronic sensor) <0.05
POHC every week including tongue
cleaning. Control group (n = 30) did not
POHC Tanaka et al, 2003a, 92 Before versus after clinical treatment at 80% VSC reduction (GC) <0.0001
2003b breath clinic
POHC and mouthwash Richter, 1996 923 Posttreatment assessments following visits 98% showed VSC reductions from NA
to bad breath clinic >180 ppb to <180 (halimeter)
Tongue cleaning Seemann et al, 2001 N = 30 Three hour, randomised crossover study 42% reduction in VSC immediately after <0.001
(3 groups) treatment and still significantly reduced
up to 25 min but not significant
thereafter (halimeter)
Short-term (0–8 h) effects of antimalodour product (single use)
Mouthrinse Zn2+ Schmidt and Tarbet, 62 Three hour, parallel study (3 groups), 70–80% VSC reduction at 1, 2 and 3 h <0.05
1978 Zn2+ versus controls (GC)
2
Toothpaste Zn + Brunette et al, 1998 11 Three hour, crossover study; five treat 40–70% H2S & CH3SH reduction in the <0.05
ments (+ 1-week washout periods) Zn pastes compared to controls at 1, 2 &
C Scully and J Greenman
Breath odour diagnosis and management

(Silica base dentrifice with 2% Zn) 3 h post-treatment (GC)

Mouthwash ClO2 Frascella et al, 2000 16 96 h, parallel study with 2 groups: Test 21% and 19% VSC reduction at 2 and <0.01
(ClO2 at 0.1%) and control (water; 4 h, respectively (halimeter)
n = 15)
Mouthwash Rosenberg et al, 1992 19 One day, parallel study with three groups For two-phase rinse, 38% VSC reduction <0.05
Two-phase (essential oils plus (two-phase mouthwash, CHX and at 8–10 h compared with placebo. <0.05
aqueous CPC) placebo) (halimeter)
CHX (0.2%) For CHX, 50% VSC reduction at 8–10 h
compared with placebo
Mouthrinses Carvalho et al, 2004 12 Six-step double-blind, crossover, For CHX (0.12%), a 63% VSC reduction =0.01
CHX (0.4%) randomised study on morning breath in For CHX (0.2%) a 70% VSC reduction. =0.001
CHX (0.05%) volunteers with healthy periodontium For CPC and triclosan, no significantVSC
Triclosan (0.03%) (4-day non-brushing). reductions (halimeter)
CPC (0.05%)
Mouthwashes (5 types of OTC Saad et al, 2011 14 Six-step double-blind crossover For both Listerine, and SB12, marked <0.05
plus 1 control) randomised study in orally healthy VSC reduction at 30, 60, 90 and 180 min
Listerine, volunteers (Odour judge, Halimetry, OralChro-
SB12 maGC)
Zn2+ (0.3%),
CHX (0.025%)
Mouthrinses (5 types containing Roldán et al, 2004 10 Six-step double-blind, crossover, VSC no significant differences at baseline <0.05
CHX and one negative randomised study in orally healthy All significantly different to negative
control) volunteers control at 1 and 5 h
0.12% CHX (CHX), plus At 5 h, CHX + CPC and CHX + Zn
alcohol (CHX + ALC), plus significantly different than other CHX
0.05% CPC (CHX + CPC), formulations (halimeter)
plus NaF (CHX + NaF),
plus 0.05% CPC and 0.14%
Zn2+ (CHX + Zn)
 Table 7 (Continued).

Statistical
significance of
malodour
Subjects reduction
Treatments Refs per group Comment Outcomes (measurement method) P

Mouthwashes Wilhelm et al, 2010 42 Single use, single-blind, parallel-group. Significant VSC and H2S reductions after <0.01
1. Amine fluoride ⁄ Measurements at baseline, 30 min and 4 h both ASF and CHX-CPC at 30 min and
stannous fluoride at 4 h. (organoleptic judge & OralChro-
(ASF) plus Zn2+ ma )
2. CHX (0.05%) +
CPC (0.05%) +
Zn2+
3. Water (negative
control)
Long-term or cumulative effects (regular use)
Tongue cleaning plus Faveri et al, 2006 19 Double-blind, randomised crossover study VSC reduction from tongue cleaning <0.05
interdental flossing (4 groups) (Halimeter organoleptic assessments)
on morning breath Interdental flossing had less effect
(halimetry)
Toothpaste Zn2+ + Payne et al, 2011 78 Examiner blind, two way crossover on H2S, methyl mercaptan and total VSC, <0.0001
o-cymen-5-ol healthy adult volunteers. Test toothpaste reduction compared with placebo, up to
ZnCl2 (0.6% w ⁄ v) used twice a day for 1 week: Pre- and 12 h (GC)
o-cymen-5-ol post- single treatment measurements
(0.1%w ⁄ v) taken on day 8
(7 day effect)
Toothpaste Sn2+ Gerlach et al, 1998 96 in each Five-day, randomised, controlled, 50–60% VSC reduction for Sn-containing <0.05
(5-day effect) group examiner blind, parallel study paste compared with control (halimeter
Mouthwash Winkel et al, 2003 40 Two-week double-blind parallel study of 45% VSC reduction (halimeter) <0.01
CHX + CPC + test (CHX + CPC + Zn) versus pla-
Zn2+ (14-day effect) cebo control
C Scully and J Greenman

Mouthwashes Wigger-Alberti et al, 174 Three-week, double-blind, placebo Significant VSC reductions after single <0.05
1. Amine 2010 controlled, parallel groups. VSC application and at days 7 and 21 for all
fluoride ⁄ stannous measured at baseline, days 1, 7, 14 and products against water negative control
fluoride (ASF) 21 days (organoleptic & OralChroma)
plus Zn2+
Breath odour diagnosis and management

2. CHX (0.05%) +
CPC (0.05%) +
Zn2+
3. CHX (0.12%)
4. Water (negative
control) 21 day
effect)

Exclusions: Trials that have <n = 10 subjects; those that only use organoleptic or hedonic methods; and those where subjects have known inflammatory periodontal disease. OTC, over the
counter; SB12 = Zn, CHX, NaF and acesulfame. Zn, zinc; ClO2, chlorine dioxide; CHX, chlorhexidine; CPC, cetyl pyridinium chloride; VSC, volatile sulphur compounds; CH3SCH3, dimethyl
sulphide; GC, gas chromatography; Sn, stannous.

Oral Diseases
341
 Breath odour diagnosis and management
C Scully and J Greenman
342
Experienced and intuitive clinicians may well have
already suspected psychogenic causes. In general, obses-
sive behaviour, depression, phobic anxiety, paranoid
ideation, reduced social interactions and the wrong
interpretation of people’s actions as an indication that
their breath is offensive (e.g. opening windows and
covering their nose) are warning signs (Iwu and Akpata,
1990; Sanz et al, 2001; Porter and Scully, 2006) but these
features are not sufficient alone to categorise a patient
under the label of pseudohalitosis as this remains a
diagnosis of exclusion.
Pseudohalitosis almost always requires referral for
clinical psychologist management. In these patients and
those with halitophobia, the involvement of a third
party (e.g. a confidant such as close family member or
trusted friend) in the management may provide the
patient with additional psychological support to con-
sider the problem in a more objective manner (Rosen-
berg, 1996). Psychiatric help and medications such as
paroxetine may be indicated (Hayashi et al, 2010).
Acknowledgement
GABA International provided support to give the IADR
presentations.
Author contributions
Both authors compiled and corrected this work.
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