J Clin Periodontol 2015; 42 (Suppl. 16): S303S316 doi: 10.1111/jcpe.

12378

Treatment of oral malodour.

Medium-term efficacy of
mechanical and/or chemical
agents:
a systematic review

Dagmar E. Slot1, Sophie De Geest2,

Fridus A. van der Weijden1 and Marc
Quirynen2
1

Department of Periodontology, Academic

Centre for Dentistry Amsterdam (ACTA),
Amsterdam, The Netherlands;
2
Periodontology, Department of Oral Health
Sciences, Katholieke Universiteit Leuven,
University Hospitals & Dentistry Leuven,
Leuven, Belgium

Slot DE, De Geest S, van der Weijden FA, Quirynen M. Treatment of oral
malodour. Medium-term efficacy of mechanical and/or chemical agents:
-a systematic review-. J Clin Periodontol 2015; 42 (Suppl. 16): S303S316. doi:
10.1111/jcpe.12378.

Abstract
Focused question: What is the effect of a dentifrice (DF), a mouthwash (MW),
tongue cleaning (TC), or any combination of these as adjunct to toothbrushing on
intra-oral malodour and tongue coating as compared to toothbrushing alone in systemically healthy patients, when used for a minimum follow-up period of 2 weeks?
Material and Methods: The MEDLINE-PubMed, Cochrane-CENTRAL and
EMBASE databases were searched up to August 2014. Measurements of Volatile
Sulphur Compounds and organoleptic scores of oral malodour were selected as
outcome variables. Data were extracted and a descriptive analysis was performed.
Results: Independent screening of 1054 unique papers resulted in 12 eligible clinical
trials with a medium-term (2 weeks) duration. The majority of studies provided a
significant reduction in oral malodour when evaluating products with an active
ingredient (incorporated into a DF or a MW) used adjunctively to toothbrushing.
The added value of tongue cleaning over a MW was evaluated in one study.
Conclusion: Due to very limited evidence, the potential effect of a specifically
formulated dentifrice, a mouthwash or a tongue scraper for treating oral malodour is, in general, unclear. For mouthwashes containing the active ingredients
chlorhexidine + cetylpyridinium chloride + zinc (CHX + CPC + Zn) and zinc
chloride + cetylpyridinium chloride (ZnCl + CPC) most evidence was available.
The strength of a recommendation to use these products was graded to be weak.

Key words: bad breath; dentifrice; halitosis;

intra-oral malodour; mouthrinse; mouthwash;
oral malodour; review; tongue cleaning;
toothpaste
Accepted for publication 4 February 2015

Conflict of interest and source of funding statement

The authors declare that they have no conflict of interest.
This study was self-funded by the authors and their institutions.
Ethical approval was not required.
This study was initiated by the European Federation of Periodontology (XI European Workshop) within the theme: Effective
Prevention of Periodontal and Peri-implant diseases, Organized November 2014 in Segovia, Spain.
Quirynen, Slot and Van der Weijden have formerly received either external advisor fees, lecturer fees or research grants from
companies that produce oral malodour products. Among these were: Procter & Gamble, Colgate, GABA, Sara Lee, Dentaid,
Lactona, and Unilever.
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Slot et al.

Individuals can suffer from persistent oral malodour (halitosis). In

many cases, the cause can be found
in the oral cavity in which case this
is referred to as intra-oral halitosis
or oral malodour (Delanghe et al.
1997, Dadamio et al. 2013a,b).
Quirynen et al. (2009) assessed the
aetiology and characteristics of 2000
patients with oral malodour complaints (often for several years) who
visited a multidisciplinary oral malodour clinic in Leuven (Belgium), In
75.8% of the patients, an intra-oral
cause for their complaints was
found. In 4.2% the cause was identified as originating from the ear,
nose, throat or other pathologies
(i.e. gastro-intestinal/respiratory tract
infections, systemic diseases). In
4.5% a combination of different
aetiologies was identified, and in
15.7% of the individuals the complaint was judged as being pseudohalitosis/halitophobia.
Oral malodour is primarily the
result of the degradation of organic
substrates by anaerobic bacteria of
the oral cavity. In those patients
with malodour originating from the
oral cavity, the distribution of
underlying aetiological factors was
tongue coating (57.3%), gingivitis/
periodontitis (14.7%) or a combination of the two (24.0%), xerostomia
(3.3%), candida infection (0.3%),
and overhanging restorations/caries
(0.4%; Quirynen et al. 2009). The
treatment is mostly done by eliminating the cause (bacteria and/or
their substrates) either mechanically,
chemically or a combination of both,
or by masking/capturing the odorous
compounds (Dadamio et al. 2013a,
b).
The first systematic reviews which
addressed the treatment of oral malodour were performed in collaboration with the Cochrane Oral Health
Group. Weak and unreliable evidence was found that tongue scrapers (cleaners) have a benefit over
toothbrushes in the reduction of
halitosis in adults (Outhouse et al.
2006). Mouthrinses containing antibacterial agents [i.e. chlorhexidine
(CHX) and cetylpyridinium chloride
(CPC)] may play a role in reducing
the levels of halitosis-producing bacteria on the tongue. Chlorine dioxide
and zinc-containing mouthrinses can
be effective in neutralization of
odouriferous sulphur compounds

(Fedorowicz et al. 2008). More

recently another systematic review
demonstrated that tongue brushing
or tongue scraping of the dorsum of
the tongue, successfully reduced
breath odour and tongue coating.
However, the evidence for the beneficial effect of mechanical tongue
cleaning in real oral malodour
patients was weak since this could
only be confirmed in one included
study (Van der Sleen et al. 2010).
Recently Kuo et al. (2013) concluded that the use of toothbrushing
plus tongue cleaning compared with
toothbrushing alone significantly
reduced the indicators of halitosis.
However, there was insufficient evidence to recommend frequency,
duration, or delivery method of tongue cleaning.
Based on a recent systematic
review of Blom et al. (2012), nearly
all mouthwashes with active ingredients appear to be beneficial in
reducing oral malodour, both in
the short- and longer term. The
most compelling evidence was provided for CHX mouthwashes
(MW), and for those that contained
a combination of CHX, CPC and
zinc (Zn). The data with respect to
the reduction in tongue coating
were sparse and none of the
included studies showed a significant effect (Blom et al. 2012). A
recent review on dentifrices (DF)
concluded that antibacterial ingredients such as triclosan, and metal
ions like stannous and zinc appear
to be effective in controlling oral
malodour (Dadamio et al. 2013a).
Toothpaste formulations have been
modified to carry these antimicrobial agents. Moreover, oxidizing
agents were added in an attempt to
influence the process of oral malodour formation (Dadamio et al.
2013b).
All systematic reviews described
above selected for inclusion papers
without restrictions to the follow-up
time. The present systematic review
focussed on those studies reporting
on the medium-term effect of causerelated interventions, by analysing
the effect after a minimum follow-up
period of 2 weeks. In addition combinations of mechanical and chemical interventions were also reviewed.
A restriction was made to include
only those studies that evaluated the
treatment of patients with malodour

originating from the oral cavity,

because other cases of halitosis
(extra-oral causes such as systemic
diseases/gastro-intestinal/respiratory
tract infections) require a different,
pathology specific, approach.
Materials and Methods

The protocol of this systematic

review detailing the review method
was developed a priori following
initial discussion between members
of the research team. It was conducted in accordance with the Cochrane handbook (Higgins & Green
2009) for systematic reviews of interventions and with the guidelines of
Transparent Reporting of Systematic
Reviews and Meta-analyses (PRISMA
statement, Moher et al. 2009).
Focused PICO questions

Based on randomized controlled

clinical trials (RCT) with systemically healthy individuals (Copanitsanou & Valkeap
a
a 2014), what is the
effect of a dentifrice (DF), a mouthwash (MW), tongue cleaning (TC),
or any combination of these as
adjunct to toothbrushing on oral
malodour parameters assessed by
Volatile Sulphur Compounds (VSC)
levels or organoleptic scores (ORG)
as compared to toothbrushing alone
when used for a follow-up period
2 weeks?
Search strategy

Three Internet sources were queried

to search for appropriate papers.
These sources included the National
Library of Medicine, Washington,
DC
(MEDLINE-PubMed),
the
Cochrane Central Register of Controlled Trials (CENTRAL), and
EMBASE (Excerpta Medical Database by Elsevier). All three databases
were searched for eligible studies up
to September 2014. For details
regarding the search terms used, see
Box 1.
Screening and selection

Two reviewers (SDG and DES)

independently screened all titles and
abstracts for eligible papers. If eligibility aspects were present in the title
or abstract, the paper was selected
for further reading. After selection,

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Management of oral malodour

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Box 1. Search terms used for PubMed-MEDLINE, Cochrane-CENTRAL and EMBASE The search strategy [<products> AND
<outcome/disease>] was customized appropriately for each of the additional databases taking into account differences in controlled vocabulary and syntax rules.
The following terms were used in the search strategy:
[<Products: [MeSH terms/all subheadings] toothpastes OR dentifrices OR oral hygiene OR mouthwashes [textwords] OR gel OR
toothpaste OR toothpastes OR dentifrices OR dentifrice OR mouthwashes OR mouthwash OR mouthwash* OR mouthrinses OR
mouthrinse OR (tongue brushing) OR (tongue cleaning) OR (tongue scraping) OR (tongue scraper) OR (oral hygiene)>
AND
<Outcome/disease: [MeSH terms/all subheadings] halitosis OR [text words] halitosis OR (oral malodour) OR (oral malodor) OR
halimetry Or halimeter OR (oral chroma) OR (bad breath) OR (morning breath odour) OR (morning breath odor) OR (volatile sulphur
compounds) OR (volatile sulphur compounds) OR VSC OR (tongue coating) OR (foetor ex ore) OR (fetor ex ore) OR breath OR
(organoleptic score)>]
The asterisk (*) was used as a truncation symbol.

the full-text papers were read in

detail by two reviewers (SDG and
DES). Any disagreement between
the two reviewers was resolved after
additional discussion. If a disagreement persisted, the judgment of a
third reviewer (GAW) was decisive.
The papers that fulfilled all selection
criteria were processed for data
extraction. Only handsearching was
done as part of the Cochrane Worldwide Handsearching Programme
and uploaded to CENTRAL was
included (see the Cochrane Masterlist for details of journal issues
searched to date). All reference lists
of the selected studies were handsearched for additional papers that
could possibly meet the eligibility
criteria. Unpublished work was not
sought.
The eligibility criteria were as
follows:

Randomized Controlled clinical

Trials (RCTs).
Papers written in English.
Studies conducted in humans:
18 years,
in good general health,
Intervention: a dentifrice (DF), a
mouthwash (MW), tongue cleaning (TC), or a combination of
these to toothbrushing alone.
Comparison: toothbrushing alone
or toothbrushing combined with
the adjunctive use of a placebo
MW or a DF without active
ingredients.
Breath improvement evaluation
via one or more of the following
clinical parameters:
Organoleptic scores (ORG),
Volatile Sulphur Compound
(VSC) levels as assessed using
a Halimeter and/or Oral
Chroma.
Follow-up period of 2 weeks.

Assessment of heterogeneity

The heterogeneity of the outcome

variables across studies was explored
according to the following factors:

Study design, study population,

evaluation period.
Subjects
characteristics
and
smoking habits.
Intervention regimens and procedures.
Lost to follow-up, side effects,
and industry (commercial) funding.

Quality assessment

Two reviewers (SDG and DES)

scored the methodological quality of
the included studies according to the
method described in detail by Keukenmeester et al. (2013, for scoring
items see Appendix S2). In short,
when random allocation, defined eligibility criteria, masking of examiners, masking of patients, balanced
experimental groups, identical treatment between groups (except for the
intervention), and reporting of followup were present, the study was
classified as having an estimated low
risk of bias. When one of these eight
criteria was missing, the study was
considered to have an estimated
moderate risk of bias. When two or
more of these criteria were missing,
the study was considered to have an
estimated high risk of bias, as previously proposed by Van der Weijden
et al. (2009).
Statistical analyses

Data extraction
The data from those papers that met
the selection criteria were extracted
and processed for further analysis.
For studies that presented an

2015 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd

intermediate outcome assessment,

only the baseline and final outcomes
were used. Two reviewers (SDG and
DES) evaluated the selected papers
for baseline-, end- and incremental
mean values, and standard deviation
(SD). Disagreements were resolved
by discussion, and if the disagreement persisted, the judgement of a
third reviewer (GAW) was decisive.
For those papers that provided
insufficient data to be included in
the analysis, the first or corresponding authors were contacted to determine if additional data could be
provided. To warrant a precise
estimate, any data approximation in
figures was avoided.
Data analysis
Data extraction revealed considerable heterogeneity in many aspects
of the included studies and, therefore, a meta-analysis could not be
carried out. Therefore, the data of
all studies were summarized and presented in a descriptive manner.
Grading the body of evidence

The Grading of Recommendations

Assessment, Development and Evaluation (GRADE) system, as proposed
by the GRADE working group, was
used to grade the evidence emerging
from this systematic review (Guyatt
et al. 2008, GRADE). Two reviewers
(DES & GAW) rated the quality of
the evidence as well as the strength of
the recommendations according to
the following aspects: study design,
estimated risk of bias of the individual studies; consistency and precision
among the study outcomes; directness
of the study results; detection of publication bias. and magnitude of the
effect. Any disagreement between the

Slot et al.
Cochrane-CENTRAL
190

PubMed-MEDLINE
1021

EMBASE
170

participants. Information regarding

the study characteristics is displayed
in detail in Table 1.
Study design, evaluation period, and
research groups

Excluded by title and

abstract
1008

Unique title
& abstracts

1054

Excluded after
full reading
32

Selected
for full-text
reading

46
Included from the
reference list
0
Final Selection
14*

Tongue cleaning
0 papers

Analyzed

Included

Eligibility

Screening

Identification

S306

Dentifrices
5 papers

Dentifrices
5 experiments

Mouthwashes
6 papers

Mouthwashes
5 experiments

Combinations
3 papers

Combinations
2 experiments

Fig. 1. Search, selection and analysis process.

*Three times two papers on the same experiment were included and one paper published two experiments.

two reviewers was resolved following

additional discussion. Grading was
performed in relation to active ingredients for which a minimum of two
experiments had been retrieved.
Results
Search and selection results

The searches resulted in 1054 unique

papers (for details, see Fig. 1). The
screening of titles and abstracts initially resulted in 46 papers. Based on
detailed reading of full texts, another
32 papers were excluded. The reasons for exclusion are explained in
Appendix S1. The reference lists of
the selected papers did not reveal
any additional suitable papers. Thus,
14 paper studies were identified as
eligible for inclusion in this systematic review, according to defined criteria for study design, participants,
intervention, and outcome. It is

noteworthy that three experiments

each were presented in two separate
papers: Roldan et al. (2003) and
Winkel et al. (2003); Hu et al. (2003,
2005) and Ademovski et al. (2012,
2013). Navada et al. (2008) published two experiments in a single
paper, resulting in a final total inclusion of 12 experiments. None of the
included studies evaluated the effect
on tongue cleaning as a primary
intervention. In total, five experiments evaluated the effect of a MW
on oral malodour. Five clinical
experiments evaluated the effect of
DF and two experiments evaluated
combinations of these interventions.
Assessment of heterogeneity

Considerable
heterogeneity
was
observed in the 12 included clinical
experiments with respect to study
design, evaluation period, study population, number, gender, and age of

All included studies were double

blind RCTs, mostly having a parallel
design with the exception of two
cross-over experiments (Peruzzo et al.
2007, Ademovski et al. 2012, 2013).
The evaluation period varied from
2 weeks to 6 months. Allocation
concealment procedures were not
described in any of the selected
studies. Two papers describing the
same experiment (Roldan et al. 2003,
Winkel et al. 2003) were from collaborating research groups. The research
group of Hu et al. (2003, 2005, 2013)
contributed to two included experiments in this systematic review. All
other papers were from different
research groups.
Subject characteristics and smoking
habits
All of the study participants of the
selected studies were in good general
health. The majority of the studies
used absence of periodontal disease
as an inclusion criteria. Rassamee
Masmaung et al. (2007) allowed for
mild to moderate chronic gingivitis
patients. Quirynen et al. (2005) specifically selected patients diagnosed
with moderate periodontitis (at least
two multi-rooted and two singlerooted teeth in the first quadrant with
probing depths 6 mm and radiographic evidence of bone loss 1/3 of
the root length). Seven studies
defined inclusion criteria for the oral
malodour status with cut-off points
for organoleptic scores ranging from
>1 up to 4, and/or VSC level measurement with a varying minimal
threshold of 80 ppb up to
>170 ppb. One experiment used the
presence of tongue coating as an additional inclusion criterion (Roldan
et al. 2003, Winkel et al. 2003). Hu
et al. (2003, 2005) mentioned existing
oral malodour, but it was unclear
how this was assessed, either professionally, by an apparatus or selfreported. Five studies enrolled only
non-smoking participants (Borden
et al. 2002, Peruzzo et al. 2007,
Rassameemasmaung
et al.
2007,
Wigger-Alberti et al. 2010, Ademovski
et al. 2012, 2013), for two others
there was no clear specification about

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 2015 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd

Codipilly
et al. (2004)

Rassameemasmaung
et al. (2007)

Wigger-Alberti
et al. (2010)

Mouthwashes

Authors (year)

: 144, : 32
Mean age: 43.1
Range: ?

No perio

Parallel
Double-blind

3 weeks

No perio
Oral malodour: 80
ppb VSC in
morning breath

4 weeks

Systemically healthy
Smokers: ?

Mean age: 40.2a

Range: 2169a

Double-blind

RCT
Parallel

Systemically healthy
Smoking: no
50 (48) subjects
: 28a, : 20a

Mean age: 26.15

Range: 1737
Mild to moderate
chronic gingivitis
Oral malodour: 80
ppb VSC in
morning breath

Double-blind

2 weeks

60 (60)
: 48, : 12

RCT
Parallel

OLS: >2
Systemically healthy
Smokers: no

? (174)

No. of participants
baseline (end), gender, age
(mean/range), characteristics

RCT

Study design,
duration

Table 1. Overview of the studies processed for data extraction

a: ZnC + NaClO2 MW (TriOral

triumph pharmaceuticals Inc.,
St. Louis, MO, USA)
b: ZnC MW (BreathRx
Discus Dental, Inc.,
Los Angeles, CA, USA)
c: Placebo MW

a: Herbal MW
(prepared by the
Faculty of Pharmacy,
Mahidol University,
Bangkok, Thailand)
b: Placebo MW

a: 250 ppm AmF/SnF + 0.2%

Zn-la MW
b: 0.05% CHX + 0.05%
CPC + 0.14%
Zn-la MW (Halita,
Dentaid, S.A.,
Barcelona, Spain)
c: 0.12% CHX MW
(Perio-Aid
Maintenance; Dentaid)
d: Placebo MW

Groups

OP: No
OH instructions: ?
Standardized
OH products: TB + DF
Other devices: ?

29 daily

20 mL
30 s

OP: No (a) & Yes

(b) (2 experiments)
OH instructions: No
Standardized
OH products: ?
Other devices: ?

29 daily

OP: No
OH instructions: ?
Standardized OH
products: TB + DF
Other devices: ?
15 mL
60 s

No gargling

29 daily

60 s

15 mL

Regimen: use and instruction

Oral prophylaxis (OP)

Zinc chloride plus

sodium chlorite
mouthrinse
is more effective in
reducing oral
malodour than a
zinc chloride alone
mouthrinse

Herbal mouthwash
that contained the
pericarp extract of
Garcinia mangostana
may be used as an
adjunct in treating
oral malodour

All 3 CHX rinses were

able to significantly
reduce oral malodour
in patients with increased
OLS or VSC values

Conclusions of the
authors of the original
papers

Management of oral malodour

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Hu et al. (2013)

Dentifrices

Borden
et al. (2002)

Mean age: 43.8

Range: 2184
No perio
Oral malodour:
oral origin,
OLS > 1, VSC > 170
ppb, TCI > 4.

Double-blind

6 months

RCT
Parallel
Double-blind

No perio

4 weeks

Systemically healthy
Smokers: ?

? (119)
: 64, : 55
Range: 2170
Mean age: 50.62a
No perio
Oral malodour: ?

Systemically healthy
Smokers: no

OLS 4.

Mean age: ?
Range: 1965

Double-blind

RCT
Parallel

Systemically healthy
Smokers: included
(not 12 h before
examination)
95 (84)
: 66, : 29

40 (40)
: 19, : 21

RCT
Parallel

Roldan
et al. (2003)
and Winkel
et al. (2003)

2 weeks

No. of participants
baseline (end), gender, age
(mean/range), characteristics

Study design,
duration

Authors (year)

Table 1. (continued)

a: 1.5% arginine, 1450 ppm

fluor (NaMPF) dical base
b: 8% arginine, 1450 ppm fluor
(NaMPF) Ca. carbonate base
c: 1450 ppm fluor (NaMPF) dical base

a: 0.064% Thm, 0.09%

Euc + 0.042% Men MW (Listerine
Antiseptic, Pfizer, Inc.,
Morris Plains, NJ, USA)
b: 0.075% CPC MW (BreathRx
Discus Dental, Inc.,
Culver City, CA, USA)
c: ClO2 + Zn-ac MW (Oxygene,
Oxyfresh Worldwide, Inc.,
Spokane, WA, USA)
d: Placebo MW

a: 0.05% CHX + 0.05%

CPC + 0.14% Zn-la MW
(Halita, Dentaid, S.L.,
Barcelona, Spain)
b: Placebo MW

Groups

OP: No
OH instructions: No
Other devices: ?

1 min
29 daily
TB: ?

OP: ?
OH instructions: ?
Standardized
OH products:
TB + DF
Other devices:
Not allowed

29 daily

? mL
?s

OP: No
OH instructions: No
Standardized
OH products: DF
Other devices:
No other DF
or MW, avoid TC

29 daily

15 mL
60 s gargling

Regimen: use and instruction

Oral prophylaxis (OP)

No statistical
significant difference
in oral malodour
among subjects
using the 3 different
DF after 6 months of use

The four mouth rinses

reduced oral malodour
within 4 hours of
single usage. CPC
was the most effective,
and the placebo was
the least effective
CPC was the only
mouthrinse that
reduced oral malodour
from baseline values
after 2 and 4 weeks
of daily use

The tested mouthrinse

was effective for
the treatment of
oral malodour

Conclusions of the
authors of the original
papers

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 2015 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd

Hu et al. (2003) +
Hu et al. (2005)

Navada
et al. (2008)

RCT
Cross-over
Double blind

Peruzzo
et al. (2007)

Double-blind
3 weeks

RCT
Parallel

RCT
Parallel
Double-blind
4 weeks

RCT
Parallel
Double-blind
4 weeks

30 days

Study design,
duration

Authors (year)

Table 1. (continued)

Oral Malodour: ?
Smokers: included
(not on morning
of examination)

No perio
Systemically healthy

General health: ?
Smokers: included(not
on morning of examination)
190 (187)
Range: 1845
: ?, : ?
No perio
OLS 3
General health: ?
Smokers: included
(not on morning
of examination)
? (81)
Range: 2270
Mean age: 44.73a

Systemically healthy
Smokers: no
190 (188)
Range: 1845
: ?, : ?
No perio
Oral malodour:
VSC 120-250 ppb

25 (25)
: 12, : 13
Range: 2535
Mean age: 27
Oral malodour: ?
No perio

No. of participants
baseline (end), gender, age
(mean/range), characteristics

a: 0.3% triclosan, 2%
copolymer, 0.243% sodium
fluoride in a silica base
(Colgate Total Advanced Frech;
Colgate-Palmolive Company,
New York, NY, USA)
b: 0.243% sodium fluoride
in a silica base (Colgate
Cavity Protection
Winterfresh Gel;
Colgate-Palmolive Company)

a: Silica gel DF containing

1000 ppm Fluoride with 0.2% Zinc
b: Placebo DF (1000 ppm Fluoride)

a: SLS DF (SLS-Close Up
Red Unilever, Sao Paulo, Brazil)
b: SLS free DF (Unilever)

Groups

TB: provided
OP: ?
OH instructions: No
Other devices: ?

1 min.
29 daily

2 min
29 daily
TB: ?
OP: No
OH instructions: No
Other devices:
No instruction

OP: Yes (7 days prior baseline)

OH instructions: Yes
Other devices:
Dental floss allowed,
no TC or MW

? min.
39 daily
TB: provided

Regimen: use and instruction

Oral prophylaxis (OP)

A DF-containing
triclosan/copolymer/NaF
provides effective
control of oral
malodour up to 12 h

DF with 0.2% Zinc

sulphate is effective in
reducing oral malodour,
compared to a
toothpaste without zinc

SLS-containing DF
reduces the VSC
formation in morning
bad breath in healthy subjects

Conclusions of the
authors of the original
papers

Management of oral malodour

S309

2 weeks

RCT
Cross-over
Double-blind

27, 18
Moderate perio

Double-blind
6 months

c: Placebo MW + TS (Dentaid)
d: Placebo MW

No perio
Oral malodour:
oral origin, OLS 2,
VSC 160 ppb
Systemically healthy
Smokers: no

a: CHX 0.2% MW + TS
b: CHX 0.05% + CPC
0.05% MW + TS
c: Placebo MW + TS

Groups

a: Zn acetate (0.3%), CHX

diacetate (0.025%), Sodium
fluoride (0.05%) MW (SB12
Antula Health Care AB,
Stockholm, Sweden) + TS (Dentaid)
b: Zn acetate (0.3%), CHX
diacetate (0.025%), Sodium
fluoride (0.05%) MW (SB12
Antula Health Care AB)

Oral Malodour: ?
Systemically healthy
Smokers: included
21 21
10, 11
Mean 45.7 years
Range 2166 years

45 ?
Mean age: 47.5

No. of participants
baseline (end), gender, age
(mean/range), characteristics

RCT
Parallel

Study design,
duration

OP: ?
OH instructions:
Yes (TS + MW)
Standardizes OH products: ?
Other devices: ?

Rinse: 10 mL, 1 min, 29 daily

TS: 5 strokes, as far as possible
29/day, before rinsing

OP: Yes (OSFMD + CHX-gel)

OH instructions: Yes
Standardizes OH products: ?
Other devices:
inter-dental brushes

MW: 1 min, 29 daily

Regimen: use and instruction

Oral prophylaxis (OP)

Rinsing with the active rinse

resulted in clinically relevant reductions.
The use of a tongue scraper did not
provide additional benefits
to the active rinse

Mechanical debridement in combination

with improved oral hygiene (including
tongue scraping) reduces the VSC levels
in the oral cavity. A CHX 0.2% solution
or a CHX 0.05% + CPC 0.05% solution
offers a beneficial adjunctive effect

Conclusions of the
authors of the original
papers

TB, Toothbrush; TS, Tongue scraper; MW, Mouthwash; DF, Dentifrice; TC, Tongue coating; TCI, Tongue coating Index; OLS, Organoleptic Score; VSC, Volatile Sulphur Compounds;
OH, Oral Hygiene; OP, At initial appointment all teeth were thoroughly scaled and polished; ?, unknown/not given.
a
Calculated by the authors of this review based on the presented data in the selected paper.

Ademovski
et al. (2012) +
Ademovski
et al. (2013)

Quirynen
et al. (2005)

Combination

Authors (year)

Table 1. (continued)

S310
Slot et al.

2015 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd

TS
0
+

Zn acetate (0.3%),
CHX diacetate (0.025%),
Sodium fluoride (0.05%)
Placebo MW TS
?
Zn acetate (0.3%), CHX diacetate (0.025%), Sodium fluoride (0.05%) + TS

0
0

+
?
CHX 0.2% MW + TS
CHX 0.05% + CPC 0.05% MW + TS
Zn acetate (0.3%), CHX diacetate (0.025%), Sodium fluoride (0.05%)
TS
Zn acetate (0.3%), CHX diacetate (0.025%), Sodium fluoride (0.05%) + TS

Placebo MW + TS

+
+

Ademovski et al.
(2012, 2013)

Quirynen et al. (2005)

Hu et al. (2005, 2003)

Navada et al. (2008)

Peruzzo et al. (2007)

Hu et al. (2013)

Borden et al. (2002)

Roldan et al. (2003)

and Winkel et al. (2003)

Codipilly et al. (2004)

Rassameemasmaung
et al. (2007)

250 ppm AmF/SnF + 0.2% Zn-la MW

0.05% CHX + 0.05% CPC + 0.14% Zn-la MW
0.12% CHX MW
Herbal MW
Herbal MW + OP
ZnC + NaClO2 MW
ZnC MW
0.05% CHX + 0.05% CPC + 0.14% Zn-la MW
Wigger-Alberti et al. (2010)

2015 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd

+, Significant difference in favour of test group; , significant difference in favour of control group; 0, no significant difference; , no data available; ?, inconclusive data which does not
allow to draw conclusions concerning statistical significance; NaF, sodium fluoride.

Tongue scraper

Mouthwash
Placebo MW TS
Placebo MW + TS

0
0
+

+
+
1.5% arginine, 1450 ppm fluor (NaMPF) dical base
8% arginine, 1450 ppm fluor (NaMPF) Ca. carbonate base
SLS DF
Silica gel DF containing 1000 ppm Fluoride with 0.2% Zinc
Silica gel DF containing 1000 ppm Fluoride with 0.2% Zinc
0.3% triclosan, 2% copolymer, 0.243% sodium fluoride in a silica base

?
?

?
?
?
0
+
0
0.064% Thm, 0.09% Euc + 0.042% Men MW
0.075% CPC MW
ClO2 + Zn-ac MW

+
+

+
+
+
+
+
+
+
+
+
+
+

+
+

Placebo MW + TS

SLS free DF
Placebo DF (1000 ppm Fluoride)
Placebo DF (1000 ppm Fluoride)
0.243% sodium fluoride in a silica base

Placebo MW

1450 ppm fluor (NaMPF) dical base

Dentifrice

Mouthwash
Placebo MW

Placebo MW
Placebo MW + OP
Placebo MW

Placebo (tap water)

VSC
ORG
Intervention
Study

Table 2. A descriptive summary of statistical significance between treatment groups

Comparison

Evaluating

Management of oral malodour

S311

smoking status of the participants

(Codipilly et al. 2004, Hu et al.
2013). The other studies did allow for
inclusion of smokers although four
papers (Hu et al. 2003, 2005, Roldan
et al. 2003, Winkel et al. 2003, Quirynen et al. 2005, and Navada et al.
2008) mentioned that a non-smoking
period was taken into account prior
to the moment of breath odour
assessment. The effect of smoking
status on the outcome parameters
was not (sub)analysed in any of the
included studies.
Intervention regimens and procedures
Different active ingredients were
used in the MW or DF. There was a
variance with respect to mouthwash
volume used, duration of rinsing,
and daily frequency. Also for dentifrice, a variation was seen in how
often and how long participants
brushed and for the type of toothbrush provided. In the selected studies, oral hygiene instruction was not
provided consistently on a structured
basis. Neither was a baseline professional prophylaxis regularly part of
the study protocol.
Side effects & industry funding
The majority of papers did not
report on adverse events during the
follow-up period. The reported side
effects mainly focused on tooth
staining, evaluated by an index/score
(Roldan et al. 2003, Winkel et al.
2003, Quirynen et al. 2005, WiggerAlberti et al. 2010) or on subjective
perception
(Rassameemasmaung
et al. 2007). Results indicate that
products can cause staining, but not
to a level that will influence the compliance. Study funding by use of
material or as a grant was mentioned in the majority of the studies.
Some studies involved various industry partners. Four studies were written in collaboration with authors
affiliated to a product for the management of oral malodour (Borden
et al. 2002, Hu et al. 2003, 2005,
2013, Navada et al. 2008).
Quality assessment

Quality assessment outcomes, including external, internal, and statistical

validity, are presented in Appendix S2. Based on a summary of these
criteria, the estimated potential risk
of bias was considered to be low

S312

Slot et al.

Table 3. GRADE evidence profile for impact of the adjunctive effect on oral malodour mouthwash products in combination, with toothbrushing in general healthy patients when used 2 weeks
Product
GRADE items
Study design
Potential risk of bias
Consistency
Directness
Precision
Publication bias
Magnitude of the effect
Body of evidence and
strength of the recommendation

for four included studies (Borden

et al. 2002, Roldan et al. 2003, Winkel et al. 2003, Codipilly et al. 2004,
Rassameemasmaung et al. 2007),
moderate for six (Hu et al. 2003,
2005, 2013, Quirynen et al. 2005,
Peruzzo et al. 2007, Navada et al.
2008), and high for one study
(Wigger-Alberti et al. 2010).
Study outcomes

The Appendix S3 shows the results

from data extraction. Different indices and their modifications have
been used. Information regarding
the changes within each intervention
group for the various indices is presented. Analyses of within group
changes
were
not
commonly
reported in the studies included in
this review.
Between groups
Data did not allow for a metaanalysis due to the observed heterogeneity in study designs, products
and ingredients used, and outcome
measures and/or data presentation.
Table 2 provides a descriptive analysis of the individual studies summarizing the significant differences
observed between the treatment
groups, clustered by intervention
mouthwash (MW), dentifrice (DF)
or combinations (MW + TC). All
studies provided significant differences in VSC levels, organoleptic
scores or both, favouring all investigated products MW or DF with an
active ingredient, and used as an
adjunct to tooth brushing. The additional effect of tongue cleaning over
a MW was evaluated in only one
study.

CHX + CPC + Zn

ZnCl + CPC

Randomized Controlled Clinical Trial

n=2
Low to high
Inconsistent
Direct
High
Possible
Moderate
Weak

Randomized Controlled Clinical Trial

n=2
Low
Inconsistent
Direct
High
Possible
Small to moderate
Weak

Evidence profile

Table 3 shows a summary of the various factors used to rate the quality of
evidence and strength of recommendations according to GRADE
(Guyatt et al. 2008). Grading was
only possible for the combination of
ingredients CHX + CPC +Zn and
ZnCl + CPC in mouthwashes because
for both combinations at least two
studies were retrieved. Data were
found to be inconsistent and a publication bias was considered to be possible. The estimated potential risk of
bias varied from low to high for
CHX + CPC + Zn studies and the
magnitude of the effect for
ZnCl + CPC varied from moderate
to small. Taken all items together,
the body of evidence and the strength
of the recommendation emerging
from this review is considered to be
weak with respect to impact on oral
malodour.

Discussion

Oral malodour is a common complaint with significant socio-cultural

impact such as personal discomfort
and social embarrassment. Epidemiological research on oral malodour is
limited. The prevalence of oral malodour is unclear because epidemiological data are based mainly on
subjective self-estimation, which is
limited in accuracy and sensitivity.
Studies are also complicated by a difference in cultural and racial appreciation of odours, which implies for
patients as well as for investigators.
There is also an absence of uniformity in diagnostic methods, both for
organoleptic measurements and for

the use of devices. Irrespective of the

method used to assess oral malodour, and independent of the study
population, large-scale studies seem
to indicate that one in four subjects
(25%) really suffers from persistent
oral malodour (Miyazaki et al. 1995,
S
oder et al. 2000, Liu et al. 2006).
Van den Broek et al. (2007) evaluated in their review the current
knowledge concerning the aetiology
of
oral
malodour.
Microbial
degradation of proteins present in
saliva, food debris, gingival crevicular fluid, inter-dental plaque, shed
epithelial cells, post-nasal drip, and/
or blood are the main causes of oral
malodour (Laleman et al. 2014). Due
to this process of metabolic degradation, malodourous gases are formed.
The most important volatile sulphur
compounds (VSCs) involved in halitosis are hydrogen sulphide (H2S),
methyl mercaptan (CH3SH) and
dimethyl sulphide (CH3)2S. These
VSCs are mainly produced by Gramnegative anaerobic oral bacteria. In
general, intra-oral conditions, like
insufficient oral hygiene, periodontitis or tongue coating are considered
to be the most important causes (80
90%; Bollen & Beikler 2012). Therefore, dental professionals are the first
in line to be confronted with this
problem. A cause-related therapy can
be directed either to (i) the involved
bacteria, (ii) the substrate used by
these bacteria, and/or (iii) the bad
smelling volatile compounds. As
such, the following treatment strategies can be applied: mechanical
reduction in intra-oral microorganisms and/or their nutrients (substrates), chemical reduction in the
oral microbial load, and/or rendering

2015 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd

Management of oral malodour

malodourous gases non-volatile. The
malodourous gases can be masked
(e.g. mint-containing lozenges or aromas). The latter can be considered as
a non-cause related (deodorizing)
therapy, with improvements of only
short duration (hours). Their temporary effect is explained by flushing
away oral debris, diminishing the
bacterial load, and leaving a pleasant, refreshing taste (via the aromas).
Such mouthrinses should be marketed as oral deodorants, this in
analogy to deodorant soaps (the latter used to control and/or eliminate
body malodours (Loesche 1999).

Mechanical

The basic management of oral malodour is a mechanical reduction in

the amount of microorganisms and
substrates in the oral cavity (Van
den Broek et al. 2008). Guidelines
for the management of oral malodour typically emphasize the need
for tongue cleaning using brushes
or tongue scrapers. The dorsum of
the tongue, with a surface profile
that allows accumulation of VSC
producing bacteria, is a significant
contributor to oral malodour.
Indeed several studies confirmed a
positive relationship between tongue
coating and oral malodour (Van
Tornout et al. 2013). A number of
clinical trials confirmed that tongue
cleaning reduces both the amount
of coating (and thus bacterial nutrients) as well as the number of bacteria, and thereby reduces oral
malodour effectively (Gilmore et al.
1973, Gross et al. 1975, Ralph
1988, De Boever & Loesche 1995).
However, others indicated that the
reduction in the microbial load on
the tongue after cleaning is negligible and that the malodour reduction
probably results from the reduction
in the bacterial nutrients (Menon &
Coykendall 1994, Quirynen et al.
2004). A systematic review from
Van der Sleen et al. (2010) stated
that tongue cleaning has the potential to successfully reduce breath
odour and tongue coating. However, data concerning the effect on
chronic oral malodour were found
to be insufficient. Also the current
review failed to identify a single
randomized controlled clinical trial
particularly exploring the effect of

tongue cleaning
follow-up.

with

2 weeks

Chemical

The chemical reduction in VSCproducing bacteria forms another

therapeutic strategy. A range of
over-the-counter mouthrinses for
controlling mouth odour has been
available for some time. The optimal
antiseptic agent against oral malodour would be a product with proven, long-lasting efficacy in reducing
organoleptic scores and VSC levels
(Blom et al. 2012). Furthermore,
such a product should have little or
no side effects because it may be
necessary to use it over longer periods of time. The effectiveness of the
active ingredients in oral health care
products is dependent on their concentration and above a certain concentration the ingredients have
unwanted side effects (Van den
Broek et al. 2008). The studies in the
present review unfortunately showed
a strong heterogeneity, not only in
the active ingredients tested but also
in their use, as well as in the selection of volunteers and outcome variables. As such it prevented a
meaningful meta-analysis. However,
descriptive analysis of the data
(Table 2) indicated that nearly all
products with active ingredients
showed beneficial effects in reducing
oral malodour. Mouthwashes containing AmF, SnF2, Zn, CHX, or
CPC, all reduced organoleptic
scores. The present observation is in
support of a recent systematic review
with broader inclusion criteria allowing for short-term (multiple use)
data (Blom et al. 2012). These
review authors concluded that the
most compelling evidence for a
mouthwash in reducing oral malodour was provided for CHX, especially when combined with CPC and
Zn. A recent review, also including
short-term data (Dadamio et al.
2013b), concluded that antibacterial
ingredients in toothpastes such as
triclosan and metal ions like stannous and zinc appear to be effective
in the control of oral malodour.
Based on organoleptic assessments, the present review supported
the effect of active ingredients such
as triclosan and Zn (Table 2).
Recently, encouraging short-term
(1 week) data were published for

2015 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd

S313

rinses with antimicrobial ingredients

in combination with zinc (CHX +
CPC + Zn and AmF + SnF2 + Zn;
Dadamio et al. 2013a). Zinc is an
ion with two positive charges
(Zn++), which will bind to the
twice-negatively loaded sulphur radicals, and thus can reduce the expression of the VSCs. It basically
converts, for example, H2S and
CH3SH into non-volatile sulphides.
The same applies for other metal
ions such as stannous, mercury, and
copper (Young et al. 2001). Another
therapeutic approach could be
the direct inhibition of bacterial
enzymes (involved in the production
of malodourous gases). The bacterial
enzyme methionine-(gamma)-lyase,
for example, is responsible for VSC
formation by cleaving methionine
into methyl-mercaptan, ammonium,
and (alpha)-keto butyrate and can
be inhibited by oral malodour counter-actives (Givaudan 2007).
Microbiology

An evaluation of the impact on the

supra- or subgingival microbial load
or composition was not the focus of
this systematic review. However,
four studies included in addition to
the clinical data also a microbiological assessment (Roldan et al. 2003 &
Winkel et al. 2003, Quirynen et al.
2005, Peruzzo et al. 2007, Ademovski
et al. 2012). Experiment by Roldan
& Winkel (2003) and Quirynen et al.
(2005) evaluated a mouthwash containing CHX + CPC + Zn for which
they collected tongue samples,
unstimulated saliva and subgingival
plaque samples. It was concluded
that there was no significant microbiological difference between the test
and control product. Ademovski
et al. (2012) assessing mouthwashes
with a combination of Zn and CHX,
sampled the dorsum of the tongue
but failed to demonstrate differences
in bacterial counts and changes of
bacterial load. Peruzzo et al. (2007)
assessed toothpaste with and without
SLS and also found no antibacterial
effect in tongue coating samples.

Strength of the recommendation

Various products were tested in the

studies retrieved for this review. Only
for CHX + CPC + Zn and ZnCl2 +

S314

Slot et al.

CPC some evidence emerged which

allowed for a weak strength of a
recommendation for use. For all
other products the evidence is insufficiently reliable to make informed
decisions. It is undoubtedly clear that
more high quality trials are needed to
provide definitive answers to this
problem. At present there is no consensus about how to assess oral malodour (Laleman et al. 2014). With
this in mind it would be helpful to
standardize assessments of oral malodour in order to allow future systematic reviewers to combine trials
from different research groups more
easily.

Limitations

This review identified a number of

additional
potential
limitations,
which render a comparison between
studies very difficult:

Organoleptic scores were used as

outcome variables for oral malodour. The odour judge (sniffer)
is still the gold standard since
the human nose can smell 10,000
different odours (Hatt 2004). The
most important disadvantage of
the organoleptic assessment is its
subjectivity, which explains its
low intra- and inter-examiner reliability (Laleman et al. 2014).
Researchers are trying to improve
the reliability and reproducibility
(Greenman et al. 2005), for example, by involving a panel of odour
judges (Yaegaki & Coil 2000) and
training and calibrating the panel
prior to the start of the study
(Nachnani et al. 2005). To date,
there are several simple portable
devices available to quantify certain VSCs (e.g. Halimeter, Oral
Chroma, Breathtron ). Unfortunately, these devices have a
number of shortcomings (e.g.
specificity, confounding factors,
stability), which translate into
moderate correlations between
their readings and the organoleptic outcomes (Laleman et al.
2014). These aspects have to be
taken into consideration when
reading this review.
No inclusion criteria were set
regarding the diagnosis of halitosis nor a threshold of its measurements.

In this systematic review study by

Rassameemasmaung et al. (2007)
included participants with mild to
chronic gingivitis, they were
referred to the clinic for gingivitis. Quirynen et al. (2005) conducted the study in moderate
periodontitis patients but these
were treated for their periodontal
problems as part of the study protocol using a one stage full-mouth
disinfection approach. The data
emerging from this systematic
review are therefore applicable for
those patients with gingivitis is
succesfully treated periodontitis.
A cost effective analysis could
not be performed because the
aspect of costs in relation to the
effectiveness of the anti-malodour
products was not reported by
any of the included studies.
Publication bias: Papers included
in the present review primarily
reported on the beneficial effects
of the active ingredients. Publication of studies with positive outcomes and statistically significant
results may represent publication
bias. Although no formal test
could be performed, the risk of
publication bias must be considered as potentially possible.
Language bias: The restricted use
of studies written in the English
language may be another limitation.

Conclusion

The collective evidence regarding the

adjunctive use of products such
as dentifrices, mouthwashes, and
tongue scrapers for reducing oral
malodour is, in general, unclear. For
mouthwashes
containing
active
ingredients such as CHX + CPC +
Zn and ZnCl + CPC, the strength of
the recommendation with respect to
the potential efficacy to reduce oral
malodour is considered to be weak.
More profound research is needed to
assess the effect of oral malodour
products particularly in halitosis
populations.
Acknowledgements

The authors acknowledge the support of Joost Bouwman, head librarian of the Academic Center for
Dentistry Amsterdam and Stephen

Siegel from the Journal of Clinical

Dentistry, who helped in the retrieval of the full-text articles. The
authors also thank the following
authors who responded to Blom
et al. (2011) on a request for additional data: W. Wigger-Alberti and
D.P. Codipilly.
Recommendations for further
research

The ADA has established Acceptance Program Guidelines that apply

to products that have been designed
for the management of oral malodour of a non-systemic origin.
These include products that are
active chemical agents as well as
mechanical products. Newly developed products should be evaluated
using study protocols satisfying the
criteria as formulated by the ADA.
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Studies

selected for this review.

Supporting Information

Additional Supporting Information

may be found in the online version
of this article:
Appendix S1. Overview of the studies
and reason for rejection after fulltext reading.

S316

Slot et al.

Appendix S2. Methodological quality

and estimated potential risk of bias
scores of the included studies.
Appendix S3. Mean (SD) scores for
the different intervention groups
with various indices and their modifications. Within groups analysis are
Clinical Relevance

Scientific rationale for the study:

Systematic reviews on the treatment of oral malodour have evaluated experiments irrespective of the
follow-up time. In the current systematic review the prolonged
effects (2 weeks) of the adjunctive
use of mechanical and/or chemical
products are reviewed.
Principal findings: This systematic
review demonstrates improvements

presented. (a) ORG scores and (b)

Total VSC measures.
Address:
Dagmar Else Slot
Department of Periodontology
Academic Centre for Dentistry Amsterdam
(ACTA)

of the level of volatile sulphur compounds and organoleptic scores

favoring the adjunctive use of dentifrices and mouthwashes with specific
active ingredients. Also when used in
a combination with tongue cleaning,
most products provided beneficial
effects of varying magnitudes.
Practical implications: Within the
limitations of this systematic review
various active ingredients appear to
have a beneficial effect. For mouth-

University of Amsterdam and VU University

Amsterdam
Gustav Mahlerlaan 3004
NL-1081 LA Amsterdam
The Netherlands
E-mail: d.slot@acta.nl

washes containing chlorhexidine in

combination with cetylpyridinium
chloride (CPC) and zinc, as well as
CPC in combination with zinc
chloride, most evidence (2 experiments) was retrieved. The recommendation emerging from the
collective evidence to use these
products was graded to be weak.

2015 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd