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Halitosis: A Review of the Literature on Its Prevalence, Impact and Control

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 REVIEWAkaji
ARTICLE
et al

Halitosis: A Review of the Literature on Its Prevalence,

Impact and Control

Ezi A. Akajia/Nkiru Folaranmib/Olufunmilayo Ashiwajuc

Summary: Halitosis is the offensive or disagreeable odour that may emanate from the mouth. In 80%–90% of cases,
bacterial activities especially on the dorsum of the tongue are implicated. Current studies on halitosis accessed from
electronic databases were appraised in the light of prevalence, impact and control of halitosis. Halitosis has a world-
wide occurrence with a prevalence range of 22% to 50%. Due to the associated social and psychological effects, it
should be taken seriously in all affected patients. Oral healthcare professionals ought to be well informed, because
their office(s) are usually the first points of call for the affected patients.

Key words: control, halitosis, prevalence, prevention

Oral Health Prev Dent 2014;12:297-304 Submitted for publication: 17.08.13; accepted for publication:08.01.14
doi: 10.3290/j.ohpd.a33135

H alitosis is an offensive or disagreeable odour

emanating from the mouth or hollow cavities of
the nose, sinuses or pharynx.71,73,91 Other general
thyl mercaptan (CH3SH) and dimethyl sulfide
(CH3SCH3) as metabolites.2,18,24,57 Some micro-or-
ganisms and other conditions associated with hali-
terms used to describe this unpleasant condition tosis are listed in Table 1.
are fetor oris, fetor ex oris, oral malodour, foul Various sites in the oral cavity serve as niches
breath or bad breath.2,18 Halitosis can be classified for these bacteria, but the dorsum of the tongue
as genuine halitosis, pseudo-halitosis or as halito- with its characteristic fissures and grooves is their
phobia.35,94 Genuine halitosis is either physiologi- primary location.1,35,40,64,83,93,95 The tongue pro-
cal or pathological in origin, while pseudo-halitosis vides a suitable environment for the growth of
is the claim that halitosis exists when no objective these organisms, as favourable redox potentials
evidence can be found.35,94 In genuine halitosis, are found in the deep crypts associated with the
bacterial activities in the oral cavity are implicated structure of the tongue papillae.30 Quirynen et al61
in 80%–90% of cases.26,73 Researchers have de- demonstrated that tongue coating – whether pre-
tected over 600 species of microorganisms in the sent alone or with periodontal inflammation – was
oral microbiota.33,36 These operate mainly by their associated with halitosis in more than 1200 of
action on sulfur amino acids such as cysteine, cys- 2000 patients of a breath clinic. The aim of the
tine and methionine to produce volatile sulfur com- present study was to assess the prevalence of hal-
pounds (VSCs) such as hydrogen sulfide (H2S), me- itosis, impact on the individual and the wider soci-
ety and the available control measures for this pub-
a
Senior Lecturer and Consultant Public Health Dentist, Depart- lic health issue.20 This review may be useful to oral
ment of Preventive Dentistry, College of Medicine, University of healthcare professionals in treatment planning de-
Nigeria, Enugu Campus, Enugu, Nigeria. Study concept and de-
sign, the review of study materials, coordinated manuscript writ- cisions and in providing information to share with
ing, proofread manuscript. patients who are burdened with oral malodour.
b
Senior Lecturer and Consultant Orthodontist, Department of
Child Dental Health, College of Medicine, University of Nigeria,
Enugu Campus, Enugu, Nigeria. Reviewed study materials, proof-
read manuscript. DATA SOURCES AND STUDY SELECTION
c
Lecturer and Consultant Paediatric Dentist, Department of Child
Dental Health, College of Medicine, University of Lagos, Idi-Araba, Articles published between 1990 and 2012 from
Lagos, Nigeria. Provided technical support, proofread manuscript. the University of Nigeria electronic library and inter-
Correspondence: Dr. Ezi A. Akaji, Department of Preventive Den- net-based publications were retrieved. The words
tistry, College of Medicine, University of Nigeria, Enugu Campus,
Enugu 234, Nigeria. Tel: 234-806-956-5601. ‘halitosis’ and ‘oral malodour’ were used as key
Email: [email protected] words for the electronic data search. Available full

Vol 12, No 4, 2014 297

Akaji et al

Table 1 Aetiological agents/conditions associated with halitosis

Other oral
contributory
Bacteria in oral cavity factors Consumables (food and drugs) Non-oral sources

Drugs causing dry mouth Non-oral sources of halitosis

Treponema denticola, Porphyr- Tooth decay,
(xerostomia) – anti-cholinergics, include ENT infections (acute
omonas gingivalis, Porphyromonas gingival
e.g. atropine, anti-depressants; pharyngitis, purulent sinusitis, and
endodontalis, Prevotella interme- inflammation,
diuretics, e.g. furosemide; postnasal drip); bronchial and lung
dia, Bacteroides loescheii, poor oral
anti-hypertensives, e.g. methyl- disease (chronic bronchitis,
Enterobacteriaceae, Tannerella hygiene,
dopa and captopril; analgesics, bronchiectasis, bronchial carci-
forsythia, Centipeda periodontii, dental
e.g. codeine, methadone, noma), liver diseases (cirrhosis),
Eikenella corrodens, Fusobacte- abscesses
ibuprofen and piroxicam; anti- kidney disorders (chronic renal
rium nucleatum, Micromonas and presence
histamines, e.g. brompheniramine failure), metabolic disorders
micros, Campylobacter rectus, of dental
and diphenhydramin; some (diabetes/diabetic ketoacidosis),
Desulfovibrio and Eubacterium prosthe-
cytotoxic agents, solvent GIT disorders, e.g.
spp.8,16,37,43,58 ses6,55
abuse45,58 GERD11,45,58,84,91

Peptostreptococcus anaerobius, Other conditions linked with

Collinsella aerofaciens, Veillonella Dry mouth,
halitosis: dehydration, old age,
spp., Selenomonas flueggei, and food impac-
anaemia, hypovitaminosis,
Proteus mirabilis89 tion areas in
emotional stress, inflammatory
between Onions, garlic, coffee, alcohol,
autoimmune diseases and
Atopobium pavulum, Eubacterium teeth, oral cigarettes14,35,38,68,74
sulci, Fusobacterium periodonti- obstruction of salivary glands,
ulcerations,
cum, Dialister spp., Solobacterium malignancy and irradiation for
oral malignan-
head and neck cancers, multiple
moorei, certain uncharacterised cies6,24,39,58,87
Streptococcus species29,33 sclerosis, menopause45,58

articles were accessed and stored on a CD-ROM. Tangerman and Winkel,88 in their assessment of
Sorting was done to exclude all publications before 58 subjects without periodontal disease but with
1990 while those from 1990 and 2012 were includ- complaint of malodour, found 10.4% of them with
ed. The authors read the articles and extracted data halitosis from non-oral sources. They also reported
on prevalence, impact and control of halitosis. If any dimethyl sulfide (CH3SCH3) and methyl mercaptan
author had more than one article on halitosis or its (CH3SH) as the main VSCs associated with extra-
correlates, the most suitable for each subheading oral and intra-oral halitosis, respectively.12 In their
under focus was selected; this was done to accom- study on daily variation of oral malodour and related
modate as many authors’ views as possible. factors in community-dwelling elderly subjects, Sam-
nieng et al72 found a significant association between
the concentration of CH3SCH3 with systemic diseas-
PREVALENCE OF HALITOSIS es and routine intake of medications at all times of
measurements. Subjects with systemic disease and
Halitosis is a problem that has plagued people for routine intake of medicines (80.7%) tended to have
thousands of years; it ranks third amongst the rea- a higher concentration of CH3SCH3 than their coun-
sons for patients’ visit to the dentist.14,24 It can be terparts. Although halitosis from non-oral sources is
detected organoleptically (i.e. by nose) and instru- generally not common, records from a multidisciplin-
mentally using sulfide monitors or gas chromatogra- ary breath clinic show that the most frequent non-
phy,57,66,68,96 although results of these different oral source is in the ear, nose and throat area.21,22
methods do not always agree.15 The prevalence of
halitosis differs across the globe due to variations
in the perception of odours among people of differ- IMPACT OF HALITOSIS ON THE INDIVIDUAL
ent races and cultures, absence of uniformity in AND SOCIETY
evaluation as well as a disparity between self-per-
ceived and clinically detected halitosis re- Halitosis has both medical and social aspects, the
ports.11,44,63 However, the overall prevalence ranges latter being responsible for most of the concern in
from 22% to 50%, being higher when self-reported recent times.9,19,73 Some phrases used to describe
than clinically detected.18,71 Table 2 shows the prev- it in the literature include social stigma,6 social
alences of halitosis extracted from some studies. health problem,63 universal medico-social prob-

298 Oral Health & Preventive Dentistry

 Akaji et al

Table 2 Prevalence of halitosis extracted from some studies

Authors / Type of Other observations /
year Location Subjects/N assessment Prevalence report conclusion

41 consecutive The most affected

Odai et al, Benin city, Organoleptic 80.5% with genuine
patients attending a population was the age
201055 Nigeria assessment halitosis
halitosis clinic group 60–69

498 student volun-

Eldarrat et 44.4% in males and Halitosis was perceived
Libya teers and office Self-perceived
al, 200824 54.2% in females mostly upon awakening
workers

Smoking, dry mouth and

Almas et 481 dental students 44% in males and 32% in
Riyadh Self-perceived tea consumption were
al, 20036 (19–24 years) females
the other features

35.4% for all cases: Mean VSC level 157.7 ±

Measurement
Mbodj et 62 dental prostheses 72.2% for fixed denture 152.6 ppb was much
Senegal of VSCs using
al, 201147 users users and 27.3% for users higher than the cut-off
halimeter
of removable dentures point VSC ≥ 152.6

Significant differences
Arowojolu were found in the
14.5% among attendees
and Ibadan, 255 consecutive Organoleptic prevalence of halitosis
of the periodontology
Dosunmu, Nigeria patients (16–74 years) assessment according to age group,
clinic
20047 oral hygiene status and
social class

Tongue coating, peri-

Organoleptic
odontal status and
Liu et al, assessment 27.5% by organoleptic
China 2000 (15–64 years) plaque index had positive
200642 and with score
associations with level of
sulfide monitor
oral malodour

Organoleptic Weak correlation

Bornstein 419 individuals 28% had readings of ≥
Switzer- assessment between self-reported
et al, from Bern, 75 ppb VSCs in their
land and VSC with either organoleptic
2009a12 (18–94 years) breath (halimeter)
measurement or VSC measurement

Compared No correlation between

Bornstein
Switzer- 625 Army recruits self-perceived 20% prevalence of self-reported halitosis
et al,
land (18–25 years) halitosis with halitosis and clinical measure-
2009b13
clinical data ment was detected

Significantly higher
Söder et Clinically rated
Sweden Swedish men/ 1681 41 (2.4%) prevalence probing depth and
al, 200080 halitosis
gingival index

Significant link between

Miyazaki et 2672 individuals aged VSCs scores VSC values and tongue
Japan 6%–23%
al, 199551 18 to 64 years with halimeter coating status; periodontal
conditions were observed

lem63 and social-life killer.9 Hence, it could consti- es such as use of mints and chewing gum, mouth-
tute a handicap leading to withdrawal from social wash, sprays and dental floss, increased frequency
circles by affected individuals.24,34 Data analysed of toothbrushing and toothbrushing force were ap-
from 465 patients who attended the halitosis clinic plied to mask bad breath.10,14,49,58 Thus, proper pro-
at the University of Basel over a 7-year period re- fessional guidance in employing some of these
vealed that social life was affected in about 388 of practices is strongly encouraged to avoid unwanted
them.97 Sufferers of halitosis can also be plagued side effects, such as tooth-wear lesions and caries.
with anxiety regardless of whether the condition is Other challenges that can ensue from halitosis
real or imagined.4,75,90 Anxiety in this context is are low self-esteem and self-confidence, hampered
more or less phobia-mediated, leading to avoidance intimate relationships such as dating and marriage,
of dental visits, poorer oral health and ultimately to decreased quality of life, unfulfilled career aspira-
a heightened or real oral malodour.75 Clinicians ob- tions, loneliness, depression, substance abuse,
served a trend among victims: behavioural practic- dropping out of school, suicidal tendencies and di-

Vol 12, No 4, 2014 299

Akaji et al

vorce.3,4,9 Ancient Hebraic texts (the Talmud) pro- • TN-2: Oral prophylaxis, professional cleaning and
vided legal backing to broken marriages if one part- treatment of oral diseases, especially periodon-
ner had oral malodour and similar references were tal diseases.
found in writings from Greek, Roman, early Chris- • TN-3: Referral to a physician or medical specialist.
tian and Islamic cultures.73 • TN-4: Explanation of examination data, further pro-
The effect of halitosis goes beyond the immedi- fessional instruction, education and reassurance.
ate sufferer as relatives and friends also share in • TN-5: Referral to a clinical psychologist, psychia-
the burden.9,19 Apart from the awkward scenario trist or other psychological specialist.
created by the condition, relatives may need to re-
assure or counsel the sufferers about their bad Dental clinicians may implement the TN-1 modality
breath.9,55 Delanghe et al22 reported that more than as treatment of physiologic halitosis; TN-1 and TN-2
70% of the attendees at a Belgian breath clinic were apply to oral pathological halitosis, while TN-1 and
advised by others to seek treatment; in a suburban TN-4 would suffice for pseudo-halitosis.50,94 Treat-
health facility in Nigeria, 31.7% and 24.4% were in- ment of extraoral halitosis should be performed by
formed of the symptoms by friends and spouses, a physician or medical specialist in line with TN-3,
respectively, before they visited the clinic.55 From while treatment of halitophobia should be by a clin-
an economic point of view, productive hours are lost ical psychologist, psychiatrist or psychologist (TN-
while sufferers seek solutions to their predicament, 5).50,94 TN-2 procedures entail mechanical reduc-
with a concurrent boom in the mouthwash indus- tion of tongue coating as well as gingivitis and
try.9,55 This is evidenced by the $700 million dollars periodontitis therapy.50,59 Some clinicians have ad-
spent on mouthwashes by Americans in 2000 and vised adequate oral hygiene at home: toothbrush-
more than $850 million dollars in the previous ing, flossing and moderate tongue scraping or
years.52,67 Meningaud et al49 reported over 2 billion brushing using an infant toothbrush or a small
dollars spent annually on products to mask halito- tongue brush to remove the microbial causal
sis. It can be concluded that a great deal of social, agent(s).53,54,85 Chemical agents and use of natural
psychological and economic resources are devoted ingredients such as mouthrinses containing chlor-
to halitosis both at the individual and community hexidine, triclosan, cetylpyridinium chloride, essen-
levels, since its impact cuts across culture, religion, tial oils or hydrogen peroxide could also be pre-
race, sex and social taboos.63,73 scribed.18,35,64 Metal ions, e.g. stannous, zinc and
copper ions, are useful in controlling halitosis
through their anti-plaque properties, that is, by the
PREVENTION AND CONTROL OF HALITOSIS oxidation of either thiol groups in the sulfur-contain-
ing precursors of VSCs or the odoriferous substanc-
Halitosis, a condition with known microbial and bio- es themselves to non-volatile substances.35 Chlor-
chemical parameters, can be prevented and/or ine dioxide is another antibacterial mouthwash that
controlled.2,41,44,85 Each case is treated differently may be used against oral malodour.28,79 Two sepa-
depending on its origin, making a holistic approach rate clinical trials by the same research group found
necessary.53 Before a treatment plan can be devel- it effective as an oxidant in both healthy and af-
oped for any patient, an accurate diagnosis based fected subjects for the control of oral malodour.77,78
on the patient’s history, physical examination, or- Other agents against halitosis include bacterio-
ganoleptic assessment and evaluation of any la- cin-producing microorganisms (probiotics) such as
boratory tests must be made.48 Also, a review of Streptococcus salivarius K12 and Lactobacillus sali-
significant aspects of the patient’s family and so- varius WB21.16,32,46 Here, the objective is to pre-
cial history (such as dietary and smoking habits), vent re-establishment of undesirable bacteria,
drug histories, illnesses, hospitalisations and sur- thereby limiting the re-occurrence of oral malodour
geries are invaluable in reaching an appropriate di- over a prolonged period, since probiotics are keen
agnosis.48 In 1999, Miyazaki et al50 established competitors of oral malodour bacteria.11 Herbal
the recommended classification for halitosis with and natural products have also been advocated for
the corresponding treatment needs: the control of halitosis.31,62,76,81,82,86 Green tea
• TN-1: Explanation of halitosis and instructions mouthwash containing green tea extracts demon-
for oral hygiene (support and reinforcement of a strated an appreciable effect among 60 patients
patient’s own self-care for further improvement with gingivitis who had at least 80 ppb VSCs in
of his/her oral hygiene). mouth air. The reduction in malodour observed was

300 Oral Health & Preventive Dentistry

 Akaji et al

Table 3 Summary of some interventional data on prevention and control of halitosis

Authors/ Effectiveness of the
year Study design Strategy used Results method
Prospective study of 41
Scaling and polishing;
Odai et al, consecutive patients Reduced bacterial load in Satisfactory outcome in 90.2%
restorations of cavities and
201055 given clinical interven- patients’ mouth of cases
replacement of dentures
tions

VSCs production diminished

Double blind crossover Use of 2 chewing gums as
VSCs production was same for after chewing gum; reduction
study involving 14 masking agents measured in 2
Rösing et both over time in the 2 series, enhanced by cysteine rinses.
subjects (20–35 years) series: 1st without and 2nd
al, 200970 largest reduction (71% to 52%) Effect was not sustained; only
with healthy periodon- after a mouthrinse containing
observed after 5 and 15 min served as a temporary
tium cysteine
measure

In periodontally healthy
Blinded crossover Tongue scraping and interdental Reduced VSCs in morning
Faveri et subjects, tongue scraping was
study involving 19 cleaning done thrice a day for 7 breath in subjects with healthy
al, 200625 an important method of
volunteers days, then washouts periodontium
reducing halitosis

Efficacy of 2 methods for tongue The tongue scraper yielded a

Pedrazzi Crossover trial Tongue scraper performed
cleaning – toothbrush and tongue 75% reduction in VSCs, while
et al, involving 10 healthy better in reducing the
scraper were compared through the toothbrush only achieved a
200456 subjects (20–50 years) production of VSCs
a handheld sulfide monitor 45% reduction in VSCs

Experimental study
Zinc cations added to CHX
involving 16 dental
Quirynen Rinsing with CHX-Alc, CHX-CPC- mouthrinse yielded 40% Sulfur binding to zinc produced
students who rinsed
et al, Zn, or AmF/SnF 2 mouthrinse, reduction in VSC, 80% an enhanced effect of halitosis
with one of the 3
200260 used twice daily for 1 week reduction in organoleptic reduction
solutions in a
expired ratings
randomised order

Randomised double- Reduced VSCs formation. Best Beneficial impact of mouth

Carvalho Use of 4 different mouth rinses
blind crossover study result using 0.2% CHX, then rinses on VSCs even in
et al, twice daily without mechanical
involving 12 dental 0.12% CHX + triclosan+ absence of mechanical plaque
200417 plaque control
students essential oils then CPC control

Double-blind ran-
Van CHX-CPC-Zn was more
domised study Randomised daily rinse with 1 Beneficial effect on halitosis
Steen- effective in reducing organo-
involving 12 (aged of the following: CHX, CHX- NaF although the mode of action
berghe et leptic scores and sulfide
21–23 years) medical or HX-CPC-Zn was unclear
al, 200192 monitoring readings
student volunteers

Randomised double- Divided subjects into 2 groups Concentrations of VSCs Further investigations on
Shinada blind crossover, that rinsed with either mouth- decreased for those who used long-term effects of ClO2 and
et al, placebo-controlled trial wash containing chlorine dioxide the experimental mouthwash its effect on periodontal
201078 involving 15 male volun- (ClO2) or placebo mouthwash for 7 days; plaque and tongue diseases and plaque accumula-
teers (19–38 years) without ClO2 for 7 days coating also decreased tion are needed

Randomised con- The stannous-containing NaF Halitosis reduced at all three

trolled, single-blind, Brushing with stannous-contain- dentifrice showed greater points analysed, stannous-
Feng et 3- or 4-period ing sodium fluoride (NaF) breath benefits through containing NaF dentifrice
al, 201027 crossover investigation dentifrice in 4 independent reduction of VSCs compared provided additional, simultane-
involving 100 subjects trials to the negative control ous cosmetic and therapeutic
aged 19–62 years dentifrice oral health benefits

Replacement of bacteria implicat- Bacteriocin-producing S.

Recruitment of 23 85% and 30% of S. salivarius
ed in halitosis by S. salivarius salivarius given after mouth-
subjects (18–69 years) and placebo groups,
Burton et K12. A 3-day CHX mouthrinsing wash treatment reduced VSCs
from a population who respectively, showed
al, 200616 followed at intervals with levels – randomised clinical
asserted they had substantial reduction of the
lozenges containing S. salivarius studies needed to validate the
halitosis implicated bacteria.
or a placebo result

Oral malodour parameters

2.01 x 109 Lactobacillus significantly decreased at 2
Oral administration of probiotic
Recruitment of 20 salivarius WB21 and 840mg weeks in the subjects with
lactobacilli primarily improved
Iwamoto patients who xylitol tablets were dissolved in physiological halitosis. The
physiological halitosis and also
et al, complained of halitosis the mouth daily. Evaluation after scores of an organoleptic test
showed beneficial effects on
201032 at the clinic within a 2 to 4 weeks was done at the and bleeding on probing
bleeding on probing from the
period of 14 months same time of day for each decreased at 4 weeks the
periodontal pocket
subject subjects with oral pathologic
halitosis

Abbreviations: CHX = chlorhexidine (0.2%); CHX-Alc = 0.2% chlorhexidine-alcohol mouthrinse; CHX-CPC-Zn = 0.05% CHX + 0.05% cetylpyridinium
chloride + 0.14% zinc lactate mouthrinse; AmF/SnF = an amine fluoride/stannous fluoride (125 ppm F-/125 ppm F-) containing mouthrinse; CPC
= cetylpyridinium chloride; CHX-NaF = 0.12% chlorhexidine + 0.05% sodium fluoride; CHX-CPC-Zn = 0.05% chlorhexidine + 0.05 cetylpyridinium
+ 0.14% zinc lactate; VSCs = volatile sulfur compounds.

Vol 12, No 4, 2014 301

Akaji et al

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