Accepted: 16 July 2017

DOI: 10.1111/idh.12306

REVIEW ARTICLE

The effect of professional tooth cleaning or non-­surgical

periodontal therapy on oral halitosis in patients with
periodontal diseases. A systematic review

HCD Deutscher1  | SHM Derman1  | AG Barbe1  | R Seemann2 | MJ Noack1

1
Department of Operative Dentistry and
Periodontology, University of Cologne,
Cologne, Germany
2
Department of Preventive-, Restorative - and
Pediatric Dentistry, zmk Bern, University Bern,
Switzerland
Correspondence
Deborah Deutscher, Department of Operative
Dentistry and Periodontology, University of
Cologne, Cologne, Germany.
Email: deborah.deutscher@uk-koeln.de
Abstract
Objective: The aim of this systematic review was to give the best available evidence
on the impact of professional tooth cleaning (PTC) and scaling and root planing (SRP)
on oral halitosis in patients with periodontal diseases.
Material and methods: Three databases were screened for relevant studies. Only ran-
domized controlled trials (RCTs) or controlled clinical trials (CCT) were included.
The primary outcome in all included studies was volatile sulphur compounds (VSC)
measured by Halimeter or OralChroma and organoleptic scores as secondary out-
come. Only studies investigating healthy adults except for periodontitis or gingivitis
were included. The considered intervention strategies were professional tooth clean-
ing and non-­surgical periodontal treatment. For both strategies, additional oral hy-
giene instructions (OHI) were possible. Two independent reviewers performed the
study selection and quality assessment.
Search results: After abstract and title screening and subsequent full-­text reading of
potential papers, a placebo-­controlled RCT could not be found. However, eight studies
or particular arms used PTC or SRP as sole interventions and were included in this
review. All trials or study arms included showed a positive effect on VSC levels or or-
ganoleptic scores after intervention.
Conclusions: Based on best available evidence, PTC and SRP in combination with oral
hygiene instructions reduced VSC values in patients with oral halitosis and/or perio-
dontal diseases, independent of tongue cleaning and the use of mouth rinses.

KEYWORDS
bad breath, oral malodour, periodontal disease, periodontal treatment, volatile sulphur
compound

1 | INTRODUCTION
Periodontal diseases are frequently accompanied by halitosis,1-3
and periodontitis is known to be the second most common cause
for oral halitosis right after tongue coating.4,5 Bacteria associated
with gingivitis and/or periodontitis, such as Porphyromonas gingi-
valis or Prevotella intermedia, are able to produce volatile sulphur
6
compounds (VSCs). These VSCs including hydrogen sulphide (H2S)
and methyl mercaptan (CH3SH) are the main components of mal-
odour originating from the oral cavity.7 Both the bacteria causing
halitosis and periodontal pathogens are mostly gram-­negative and
anaerobic.8
In periodontal patients with probing depths more than 4 mm,
the concentrations of VSCs, particularly methyl mercaptan, were
found to be higher compared to healthy controls.9 In an in vitro
experiment, porcine epithelial tissues were treated with CH3SH,

36  |  wileyonlinelibrary.com/journal/idh
© 2017 John Wiley & Sons A/S. Int J Dent Hygiene. 2018;16:36–47.
Published by John Wiley & Sons Ltd
Deutscher et al.
T A B L E   1   The search strategy developed for PubMed-­MEDLINE
and then customized for the COCHRANE-­CENTRAL and Google
Scholar databases
The following terms were used in search strategy:
<(Intervention) AND (outcome)>
<(Intervention: Periodontal treatment OR Periodontal therapy OR
Scaling root planing OR Scaling and root planing OR Tooth cleaning
Or Professional tooth cleaning OR Non-­surgical periodontal
treatment OR Non-­surgical periodontal therapy OR Professional
mechanical tooth cleaning)
AND
(Outcome: Halitosis OR Bad breath OR Foul breath OR Foul smelling
OR Foeter ex ore OR Foul odour OR Rotten smell OR Rotten odor
OR Volatile sulphur compounds OR VSC)>
resulting in severe cell damage or apoptosis.9 Even extremely low
concentrations of VSCs proved to be toxic to the periodontal tis-
sues,10 and it is presumed that VSCs can facilitate bacterial invasion
into deeper tissues.3 Accordingly, not only do VSCs cause halitosis in
terms of a lifestyle problem, but are also regarded as a periodontal
pathogenic factor.
Scaling and root planing (SRP) and professional tooth cleaning
(PTC) are essential elements of both an anti-­infective therapy and a
periodontal supportive therapy, not only in periodontitis patients but
also in patients suffering from gingivitis.11,12 Taking into account that
periodontitis is an important source of oral halitosis, we would antici-
pate that an additional benefit of both SRP and PTC would be a reduc-
tion in oral levels of VSCs and in oral halitosis.
However, systematic literature reviews exist only for the effect
of tongue cleaning and mouth rinses on oral VSC concentrations
and organoleptic scores13,14 and show beneficial effects for both
measurements.
Therefore, the aim of this review was to elucidate the question
whether anti-­infective therapy independent from tongue cleaning and
mouth rinsing already shows a beneficial effect on halitosis in patients
with periodontal and gingival disease, and furthermore, whether or
not anti-­infective therapy is able to cure patients suffering from hali-
tosis caused by periodontal disease. Specifically, this review aimed at
the evaluation of the impact of PTC and SRP in addition to oral hy-
giene instructions (OHI) on oral halitosis in patients with periodontal
diseases. Primary outcomes were the VSC concentrations measured
by OralChroma (Abilit Corporation, Japan) or Halimeter (Interscan
Co., Chatsworth, CA, USA), and secondary outcome the organoleptic
scores.
2 | MATERIALS AND METHODS
2.1 | Search strategy
For this systematic review, three Internet databases were system-
atically screened to find all relevant studies up to January 2016.
Regarding the focused question, our databases were as follows:
PubMed-­
MEDLINE, Cochrane CENTRAL and Google Scholar. The
|
      37
search terms to evaluate the impact of preventive dentistry on halito-
sis are presented in Table 1.
2.2 | Study selection
Initially, two independent reviewers (H.C.D.D. and S.H.M.D.) read all
selected papers considering title and abstract. Solely included were
randomized clinical trials (RCTs) or controlled clinical trials (CCTs) pub-
lished in English with an a priori design.
Letters, case reports or historical articles as well as unpublished
data were excluded.
Inclusion criteria were as follows:
Population:
• Human subjects
• No systemic diseases affecting oral malodour except periodontitis
or gingivitis
• Individuals aged at least 18 years
Intervention in at least one study arm:
(a). Professional tooth cleaning; along with oral hygiene instructions.
(b). Periodontal treatment: non-surgical periodontal treatment; along
with oral hygiene instruction.
• No additional conscious intervention like tongue cleaning and use
of mouthwash during the evaluation period.
Control:
• No intervention like SRP or PTC in control group.
Outcome:
• Primary outcome: VSC concentrations (measured by sulphide mon-
itor: Halimeter or gas chromatograph: OralChroma).
• Secondary outcome: organoleptic scores.
2.3 | Assessment of heterogeneity
All included studies showed homogeneity regarding the primary out-
come (VSC levels), and some studies used additionally organoleptic
scores as secondary outcome. The considered intervention strategies
were non-­surgical periodontal therapy and professional tooth clean-
ing combined with oral hygiene instruction.
The heterogeneity between the included studies regarding
study design, subject selection and evaluation period is shown in
Table 2.
2.4 | Quality assessment
Two independent reviewers (HCDD and MJN) examined the meth-
odological quality of the included studies regarding characteristics of
subjects, number of subjects, gender, mean age, evaluation period, in-
tervention, outcome, authors’ conclusions and also the best available
evidence in the interest of this review (Table 2).
As for quality criteria, we followed the Cochrane Handbook and
the PRISMA statement.15
 |
38       Deutscher et al.

T A B L E   2   Overview of the included studies and single study arms and characteristics processes for data extraction

Study design No. of subjects

(particular arms/total Groups (selected for baseline (end) Gender Characteristics (inclusion, exclusion criteria,
No/Author/Year arms) review) Age (mean/range) etc.)

I Soares et al, CCT Generalized chronic ? No systemic diseases

2015a 28 Only test group without periodontitis f: ? m: ? Absence of dental decay
CHX and without 47.74 ± 14.26 (38-­66) No periodontal treatment in the previous 12 mo
tongue cleaning were No antibiotics within the last 6 mo
included No history of radiation therapy for neck or head
(1/4) No current smoking
II Eid 2014a 36 Cross-­sectional Case group and test group ? (60) No data about smoking status
comparison with chronic periodontal f: 30 m: 30 No systemic disease
(3/3) disease 31.35 ± 3.25 (25-­35) No antibiotics within the last 6 wk
Control group without
periodontal diseases

III Guentsch CCT Test group with periodontal 42 (30) No complain of halitosis
et al, 201337 (2/2) disease f: 18 m: 12 No systemic diseases
Control group periodontal Test: 52 (25-­72) No pregnant or lactating females
healthy Control: 26 (23-­39) No antibiotics within the last 6 mo
Analysed after first No smokers, no history of smoking
intervention (PTC) No TC

IV Ehizele et al, CCT Test group with periodontal ? (400) No systemic disease
201338 (2/2) disease ? No smokers
Control group without 20-­40 No orthodontic or prosthetic appliance
periodontal disease

V Silveira et al, Clinical trial (without Subjects with periodontal ? (27) No systemic disease
201239 control group) disease and generalized f: 14 m: 13 No periodontal treatment in the last 6 mo
(1/1) gingivitis 47.7 ± 7 No antibiotic and anti-­inflammatory therapy in
the last 6 and 3 mo
No smokers
At least 12 teeth present
VI Pham et al, CCT Test group 1 with 229 (218) Diagnosed with oral halitosis
2011a 27 Only periodontal periodontitis f: 113  No systemic disease
treatment arms are Test group 2 with gingivitis m: 105 No periodontal treatment within the last 6 mo
included of the RCT 42.6 ± 8.5 (25-­60) No pregnant or lactating females
(2/4) No TC instruction

VII Seemann CCT Test group: patients from ? (40) No systemic diseases
et al, 200440 (2/2) dental students course test group: 30 No medication within 3 mo before and/or
without periodontitis control group 10 during the study
Control group: staff f: ? m: ? 23-­51 No mucosal lesions
member of dental school No active periodontitis
without periodontitis No complain of oral halitosis
No regular TC
No removable dentures
At least 24 teeth
VIII Seemann CCT Dental students ? (65) No complain of halitosis
et al, 200141 (2/2) f: ? m: ? No systemic disease
22-­31 No data about smoking status
No regular TC

CCT, clinical controlled trial; RCT, randomized controlled trial; ?, unknown/not given; PTC, professional tooth cleaning; OHI, oral hygiene instruction; SRP,
scaling and root planning; TC, tongue cleaning; HM, Halimeter; OC, OralChroma; ORG, organoleptic measurement; VAS, visual analogue scale; VSC,
volatile sulphur compound.
a
Only study arms with SRP or PTC or suitable study phases were included.
b
Post hoc analysis regarding tongue cleaning.
Deutscher et al. |
      39

Best available evidence (sole impact of SRP,

Evaluation period Intervention Measurement Selected authors conclusion PTC)

T0 baseline Non-­surgical HM After intervention, there is a For patients with generalized chronic periodonti-
T1 day 30 periodontal ORG reduction in VSC level measured by tis with moderate VSC levels at baseline
T2 day 60 treatment in Halimeter® and organoleptic scoring After non-­surgical periodontal treatment, the
T3 day 90 quadrants VSC level decreases and it is still low after 90 d

Baseline measure- No randomization HM The periodontal group has the Cross-­sectional comparison
ment for case and Test group: highest level of VSC with 230.8 ppb; For patients with periodontal diseases with
control group non-­surgical the treated group showed higher VSC levels than healthy controls
Test group first periodontal 124.5 ppb, and the periodontal After non-­surgical periodontal treatment,
measurement after treatment healthy group the VSC level is about patients have a lower VSC levels than patients
intervention Case and control: 102.35 ppb with untreated periodontitis patients, but still
no intervention higher than those without periodontitis
T0 baseline No randomization HM Statistically significant differences in For patients with and without periodontal
T1 after PTC PTC ORG the VSC of both groups were diseases with comparable VSC levels
OHI observed between baseline and T1. 1. The reduction in VSC concentration after the
However in patients with periodon- PTC is higher in periodontitis patients than in
tal diseases, a more complex healthy patients
treatment is necessary 2. VSC levels increase again in patients having a
periodontitis 14 d after intervention
T0 baseline No randomization HM At baseline VSC in no periodontal For patients with periodontal diseases with
T1 after intervention Test: non-­surgical disease is 91.5 ppb while group with double as high VSC levels than healthy control
T2 week 2 periodontal periodontal disease the VSC After SRP, VSC levels are reduced in patients
T3 week 6 treatment concentration is 228.5 ppb. with periodontal problems, but it is still higher
Control: tooth- Immediately after instituting the than in periodontal healthy patients
brushing, OHI treatment, 364 of 400 subjects have
a concentration less than 180 ppb
T0 baseline No randomization HM Supragingival plaque control is For patients with periodontal diseases and with
T1 day 30 PTC ORG effective in reduction of bad breath high VSC levels
T2 day 90 OHI (No change of VAS in patients with chronic periodontal 1. After PTC, the VSC concentration decreases,
T3 day 180 daily tongue disease but it is still high
cleaningb) 2. After 180 d, the VSC level increases again

T0 baseline Test group 1: OC Periodontal therapy impacted an oral For patients with periodontal diseases with higher
T1 after intervention Randomization ORG malodour reduction; however, the VSC levels than patients with gingivitis (CH3SH)
1 1. SRP degrees of effect depending on SRP resulted more improvement of halitosis in
Test group 2: periodontal status patients with periodontitis than in patients with
Randomization gingivitis especially regarding methyl mercaptan
1. SRP values
T0 baseline No randomization HM Patients having PTC and OHI show For patients without periodontal diseases
T1 after PTC Test: PTC, OHI immediately after intervention and 1. Directly after PTC, the VSC concentration
T2 week 1 Control: no after 1 and 4 wk lower VSC decreased compared with baseline
T3 week 4 intervention concentrations compared to baseline. 2. After 1 and especially after 4 wk, the VSC
In patients without any intervention, levels increase again, but it is still lower than in
there was no significant change patients without any treatment
regarding VSC level over the study
period

T0 baseline No randomization HM In patients after PTC, the VSC values For patients without periodontal diseases
T1 week 1 Test: plaque-­free were significant lower 1 wk after 1. There are no changes regarding VSC levels
T2 plaque-­free status status (week 2), PTC and at the end of the study after self-­accomplished plaque-­free status
(week 2) PTC (week 6) compared to the untreated patients 2. The VSC concentrations decrease after PTC
T3 after PTC (week 6) Control: no and baseline values. 3. VSC concentration increases again 4 wk after
T4 week 10 intervention PTC, but is still lower than in patients
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40       Deutscher et al.
2.5 | Data extraction and analysis
After abstract and full-­text reading of the potentially relevant stud-
ies by two independent reviewers (HCDD and MJN) regarding the
review’s objective, the studies that met the inclusion criteria were fil-
tered out. The impact of the SRP and PTC on VSC levels and organo-
leptic scores was extracted.
A meta-­analysis could not be performed with the included stud-
ies/study arms. Even if all studies reported VSC levels, they differed
tremendously regarding included subjects and evaluation period.
Therefore, a subgrouping focussing professional tooth cleaning or SRP
was not possible, too.
2.6 | Grading the “body of evidence”
A GRADE evidence profile was performed as recommended by the
GRADE working group regarding scaling and root planing and pro-
fessional tooth cleaning.16 Two reviewers (HCDD and MJN) inde-
pendently evaluated the quality of the evidence regarding study
outcomes and the strength of the recommendation according to
the following issues: risk of bias of the included studies/single
study arms, precision and consistency among the studies, direct-
ness of the results and detection of potential publication bias. Any
inhomogeneity between the reviewers was resolved after further
discussion.
3 |  RESULTS
3.1 | Search and selection results
In three databases (PubMed-­
MEDLINE, Cochrane CENTRAL and
Google Scholar), a total of 339 unique titles and abstracts were found.
After screening, the papers by title and abstract, 15 full-­text articles
remained, seven of which did not meet the inclusion criteria. In total,
eight trials were included in this review (Fig. 1). After searching by
hand, no additional papers were found. To collect more in-­
depth
data, we also contacted various authors who had published the cited
studies.
3.2 | Study design
Up to now, no classically designed RCT (parallel groups, control group
without intervention) could be found related to the questions of this
review. There are a number of clinical trials and several study arms
that were used to answer the question by proving the best available
evidence.
Five of the eight investigated studies were CCTs (#I, III, IV, VII and
VIII). Study #II used a cross-­sectional comparison, and study #V used
a clinical trial without any control group. Only study VI was a RCT de-
sign; however, two of the four study arms were excluded because of
additional intervention (tongue cleaning). In Study #I, also only one of
the four study arms was included, and the other arms used additional
interventions (eg, tongue cleaning or mouthwash) and therefore were
excluded.
3.3 | Industry funding and side effects
None of the eight studies reported support by industrial funding or
non-­commercial grants. Moreover, no kind of side effects has been
declared.
3.4 | Assessment of heterogeneity
Regarding characteristics of subjects, evaluation period, inclu-
sion criteria and intervention, the eight selected studies we uti-
lized had strong heterogeneity (Table 2). All studies, except #II,
measured the VSC concentrations levels before after interven-
tion and included only healthy subjects except for their diagnosis
of periodontitis or gingivitis who were aged at least 18 years of
age.
3.5 | Quality assessment
The main problem comparing the included studies was the wide va-
riety of subjects (both overall and within the single studies). Hence,
there is a selection bias regarding the focused question in all of the
eight studies (Table 3).
3.6 | Grading the “body of evidence”
The quality of evidence was rated by the GRADE system. Table 4
shows an overview of the quality of evidence as well as strength and
direction of recommendation according to GRADE16,17 and also the
level of certainty.18
We included single study arms in mainly control trials and CCTs,
which might indicate a high risk of bias (Table 3). Publication bias how-
ever is unlikely.
Regarding VSC-­levels, the direction of recommendation favours
SRP over PTC in patients suffering periodontal disease. Organoleptic
scores showed similar direction of recommendation.
3.7 | Characteristics of subjects
3.7.1 | Periodontal status
Studies #II, III and VI compared patients diagnosed with periodontal
disease with subjects without periodontitis or gingivitis. In studies
#I and V, all subjects suffered from periodontal or gingival diseases.
Study #VI included two intervention groups, one with gingivitis and
one with periodontitis. In study #VII, the control group consisted of
staff members of dental clinic and study #VIII only investigated den-
tal students. None of the study populations in trials #VII and #VIII
showed any periodontal problems.
Deutscher et al. |
      41

Identification
Pubmed, Cochrane, Google Scholar Additional records identified
(n = 339) through other sources

Unique Excluded by title and

Screening
title &
abstract
abstract
(n = 227) (n = 212)

Selected
Eligibility for full-text Excluded after full-text
reading reading, because of
(n = 15) additional treatment (n = 7)
Included

Final selection
8 papers

Descriptive analysis
8
Analysed

VSC 8 Org. 4

F I G U R E   1   PRISMA flow diagram

other studies (#I, II and IV) did not report any information regarding
3.7.2 | Halitosis
tongue cleaning habits of the participants. Only trial #V did a post hoc
Subjects in studies #III and VIII had no complaints of obvious oral hali- analysis if there was a difference in VSC levels as a result of tongue
tosis. In study VII, oral malodour could not be detected by organolep- cleaning performed.
tic measurement at baseline.
Only one study included patients diagnosed with halitosis (#VI).
3.7.5 | Mouthwashes
However, no explanation was provided whether the diagnosis was
based on organoleptic or instrumentally scores, or whether the pa- None of the eight investigated studies state whether or not mouth
tients had diagnosed halitosis themselves. In the studies #I, II, IV and rinses were used during or prior to SRP or PTC.
V, the presence or absence of oral malodour was not considered as an
inclusion criterion.
3.8 | Bias
The different types of bias are shown in Table 3. The evaluation of
3.7.3 | Smoking status
bias in the studies refers to the review’s objective and was based on
Only one trial (#VII) included smokers in the test group, but there were Cochrane Handbook.15
no smokers in the control group. Smoking was an exclusion criterion
for trials #I, III, IV and V. The other three studies (#II, VI, VIII) were not
3.9 | Outcome
explicit regarding patient selection and smoking status.

3.9.1 | Comparison of VSC levels at baseline and

3.7.4 | Tongue cleaning after intervention
For the majority of the included trials, tongue cleaning performed by All investigated types of intervention showed a beneficial effect on hal-
the participants was an exclusion criterion (#III, VI, VII and VIII). The itosis (Table 5). Because of the different measurements (OralChroma,
 |
42      

T A B L E   3   Bias profile of included studies regarding review’s objective, detection bias was not found in any study

Study no., Author/

Date Selection bias Performance bias Possible Confounding factors Attrition bias Reporting bias

I Soares et al, 2015 No No • Removable dentures not No data about dropouts No

reported reported
II Eid 2014 • Three groups: 1 intervention, 2 control groups Two control groups • Smoking status not reported Unclear, no information No data provided regarding
• No randomization without intervention •­TC not reported provided baseline VSC in test group
•­Removable dentures not
reported
•­No instruction before
measurement
III Guentsch et al • Two intervention groups No •­Removable dentures not No Additional long term in periodon-
2013 • No randomization reported tal group not comparable, data in
healthy group missing
IV Ehizele et al, 2013 •­Two intervention groups Two different •­TC not reported No data about dropouts No subgrouping of test group into
interventions •­Intake of antibiotics not reported reported gingivitis and periodontitis
V Silveira et al, 2012 •­Inhomogeneous diseased group No •­Removable dentures not No data about dropouts No
•­No control group reported reported
•­No randomization
•­Post hoc subgrouping by self-­performance of
TC
VI Pham et al, 2011 •­Two intervention groups No •­Smoking status not reported No Per-­protocol analysis reported, no
•­Removable dentures not information about intention-­to-­
reported treat analysis
VII Seemann et al, •­No randomization No •­Control group of dental No data about dropouts No
2004 professionals reported
•­Smokers only in the intervention
group
VIII Seemann et al, • No randomization No •­Smoking status not reported No data about dropouts No
2001 •­All participants dental students reported
•­Absence of including criteria
Deutscher et al.
Deutscher et al. |
      43

T A B L E   4   GRADE evidence profile for impact of SRP and PTC on gingivitis with mean baseline values around 450 ppb and a maximum
halitosis parameters close to 2000 ppb.

GRADE SRP PTC For patients without any periodontal diseases (#VII and #VIII),
the VSC levels for test and control groups at baseline were similar
Study design CCT CCT
and accounted for 110 ppb (trial #VII) and 130 ppb (trial #VIII).
Studies No. 4 4
In three studies (#II, III, IV), the test group members suffered
Comparison No. 5 4
from periodontal disease while subjects of the control groups
Risk of bias High High were periodontally healthy or had gingivitis. In all of these trials,
Consistency Inconsistent Inconsistent Halimeter measurements were taken. The VSC baseline levels in
Directness Generalized Generalized periodontal groups in studies #II and IV were approximately 230
Precision Rather imprecise Rather imprecise and 100 ppb in the accordant control groups. In study #III, there
Publication bias Undetected Undetected is almost no difference at baseline with approximately 70 ppb in
subjects with periodontitis and the healthy control group.
Level of certainty Low Low
Regarding the different VSC concentrations measured by
Magnitude of the Moderate Small
OralChroma, mean hydrogen sulphide levels were above 500 ppb
effect
in the periodontal group and approximately 400 ppb in the gin-
Direction of the Strong recommenda- Weak recommenda-
recommendation tion for patients with tion for patients givitis group. For methyl mercaptan, the mean concentration
untreated periodon- with untreated at baseline was approximately 450 ppb in patients suffering
titis and bad breath periodontitis and from periodontitis and approximately 150 ppb for patients with
bad breath
gingivitis.
CCT, clinical controlled trial; PTC, professional tooth cleaning; SRP, scaling
and root planing.

Halimeter, organoleptic measurement and visual analogue scale), an
all-­over comparison or meta-­analysis could not be performed.
Regarding Halimeter measurements (# I, III, IV, V, VII and VIII), the
mean VSC concentration decreased after intervention (values at base-
line (T0) between below 100 ppb and over 450 ppb; values after inter-
vention (T1) between below 50 ppb up to 320 ppb).
In study #II, there was a lower VSC concentration in the group with
periodontal treatment compared to the untreated group. The size of
effect could not be determined because of missing pretreatment data.
Authors reported a cross-­sectional comparison.
In trial #VI, the VSC concentrations measured by OralChroma
regarding methyl mercaptan decreased from over 450 ppb to below
100 ppb for patients with periodontitis. In patients suffering from
gingivitis, the mean concentration was 150 ppb at baseline and about
100 ppb after intervention. Concerning hydrogen sulphide, the VSC
levels decreased after intervention from over 500 ppb to below
200 ppb in patients with periodontitis and from over 400 ppb to
below 350 ppb in patients with gingivitis.
In total, four trials (# I, III, V, VI) used additional organoleptic scores
for halitosis detection, which were also positively influenced by inter-
vention. The different organoleptic scores are shown in Table 5.
Only trial #V used a visual analogue scale (patient-­based) to offer
a subjective outcome after intervention (7 at baseline and 5 at T1).
3.9.2 | Comparison of VSC levels at baseline
Except for trial VI, all studies used the Halimeter.
In trial #I, all subjects suffered from periodontitis and showed a
mean baseline value of approximately 100 ppb VSCs. In trial #V, mem-
bers of both test and control groups suffered from periodontitis or
4 | DISCUSSION
Based on best available evidence, this review revealed the re-
duction in oral volatile sulphur compounds after periodontal
therapy with SRP or PTC in patients with periodontitis or gingivi-
tis. However, the extent of this reduction could not be assessed
quantitatively due to the lack of RCTs and randomized control
groups. Performing meta-­analysis was not possible as VSC lev-
els were scored by different types of equipment (OralChroma and
Halimeter). Moreover, the various methods of intervention (SRP
and PTC) and differences in selection of subjects, that is healthy
patients vs patients suffering from gingivitis and periodontitis,
made any comparison impossible.
Scaling and root planing in conjunction with supragingival
plaque control (PTC) is the current method to treat patients suf-
fering from chronic periodontitis. 19,20
In general, patients with periodontitis showed more VSC re-
duction after SRP than healthy controls or those with gingivi-
tis after PTC. The beneficial effect could be estimated, but the
rated impact in comparison with other interventions like tongue
cleaning 13 or use of mouthwashes 14 could not be determined. In
gingivitis patients where PTC and mouthwashes or tongue clean-
ing are competitive approaches for halitosis treatment, the rated
impact of each option would be important in the decision-­m aking
process, not only from a medical point of view but also under the
aspect of a reasonable health economy.
However, of the eight included studies, none describes
whether or not mouthwashes as an addition to SRP or PTC were
used or recommended. This leaves room for discussion as the use
of mouthwashes during the treatment of halitosis was stated to be
beneficial.14 If mouth rinses were used, the magnitude of impact
 |
44      

T A B L E   5   Effectiveness of intervention regarding VSC levels, organoleptic scores and VAS

Organoleptic
VSC level (mean) scores (mean) Odour
Subjects characteristics in Significant self-­assessment
Study/Year test and control group(s) Intervention Measurement Baseline T1 difference Baseline T1 Significant difference VAS

I Soares et al, 2015 Periodontitis SRP HM 108 54 + 1.9 0.5 n.s. (Falcoa: 0-­4) /
II Eid, 2014 Periodontitis SRP HM / 124 n. s. / / /
Periodontitis / 230 /
Periodontal healthy / 102 /
III Guentsch et al, 2013 Periodontitis PTC + OHI HM 77 47 + n.a. + (Seemann: 0-­3) /
Periodontal healthy PTC + OHI 76 51
IV Ehizele et al, 2013 Periodontitis SRP HM 228 106 n. s. / / /
Periodontal healthy OHI 92 47
V Silveira et al, 2012 Periodontitis and Gingivitis PTC + OHI HM 463 312 + n.a. n.s. (Rosenberg: 0-­5) 6.56 4.88
VI Pham et al, 2011 Periodontitis SRP OC H2S: 535 186 + 2.86 1.45 + (Rosenberg: 0-­5) /
MM: 458 95 +
Gingivitis SRP H2S: 404 322 + 2.26 1.98 + (Rosenberg: 0-­5)
MM: 150 109 +
VII Seemann et al, 2004 Periodontal PTC HM 130A 80A + / / /
healthy
Staff member of dental / 130A 120A
school
VIII Seemann et al, Periodontal healthy PTC HM 110A 80A + / / /
2001 A
Periodontal healthy / 110 105A

SRP, scaling and root planing; PTC, professional tooth cleaning; OHI, oral hygiene instruction; HM, Halimeter; OC, OralChroma; MM, methyl mercaptan; VAS, visual analogue scale; VSC, volatile sulphur
compound.
/, not performed; +, significant difference; n.s., not significant; n.a., not available, A, contacted the author, all VSC samples were measured in ppb.
Deutscher et al.
Deutscher et al.
of either SRP/PTC or mouthwashes would be questionable as both
treatments evidently lead to a reduction in halitosis parameters.
Incongruent data concerning the cut-­off points for the definition
of halitosis are described in the literature: studies correlating organ-
oleptic scoring with Halimeter levels defined levels between 75 and
107 ppb as a threshold span, 21
while the manufacturer of the device
proposed 160 ppb (http://www.halimeter.com). OralChroma validity
was not influenced by reducing the manufacturer’s proposed detec-
tion limits, so the threshold levels were kept with 112 ppb for hy-
21
drogen sulphide and 26 ppb for methyl mercaptan. Not all studies
showed a VSC reduction below the above-­mentioned threshold val-
ues after intervention. Therefore, it remains questionable, whether
or not the VSC reduction achieved is satisfying from the patient’s
perspective. For the individual patient, it still has to be considered
if the PTC or SRP alone reached the treatment goal or if additional
interventions (eg, tongue cleaning or mouthwashes) are needed to
22,23
“cure” the halitosis.
4.1 | Sustainability
Five studies reported the long-­
term effect on VSC reduction
(#I 90 days, #V 180 days, #IV 6 weeks, #VII 4 weeks and #VIII
10 weeks). After the first measurement (post-­intervention) in four
studies (#I, V, VII and VIII), the VSC levels increased steadily, but
remained below the pretreatment values. Only in study #IV, the
VSC levels decreased steadily, reaching values lower than 10 ppb
without further intervention. Currently, there is no sufficient data
available to define when a retreatment or additional interventions
would be necessary.
4.2 | Study design
Up to now, no classically designed RCT (parallel groups, control group
without intervention) regarding this review’s objective could be found
and therefore the overall “body of evidence” is low,24 even we pointed
out the best available evidence.
From the classically designed RCTs,25-28 only one study arm could
be included and two were excluded completely, as they examined the
effect of SRP or PTC with additional use of antiseptics and/or tongue
cleaning.
However, the included clinical trials and the single arms of
studies performed could be interpreted as observational studies
regarding the effect of PTC, SRP and/or oral hygiene instructions
on halitosis. A recent methodological review proved the value of
observational studies (OS).29 No significant differences between
effects in trials with RCT design in comparison with observa-
tional studies were found.29 Conflicting data were not a result of
the study design (RCT vs. OS) but could be attributed to others
confounding factors.
The lack of classically designed RCTs should not lead to the con-
clusion that there is no evidence for an implication. The sum of the
observational studies and study arms points at a conclusion in terms
of best available evidence.
|
      45
4.3 | Measurement/halitosis evaluation
4.3.1 | Instruments
Even if the organoleptic measurement is still the gold standard for hali-
tosis evaluation,21,30,31 the use of Halimeter and/or OralChroma is more
specific for this review’s objective. Both devices measure the VSCs. The
Halimeter gives an overall VSC value whereas the OralChroma distin-
guishes between the three main components of bad breath hydrogen
sulphide, dimethyl sulphide and methyl mercaptan. Most of the in-
cluded studies used the Halimeter7,8; OralChroma was utilized in one
study. As methyl mercaptan showed an association with periodontal
diseases,9 the OralChroma measurements offer the most specific re-
sults for this review’s topic, in particular because of the Halimeter’s
sensitivity, which is lower for methyl mercaptan than for hydrogen
sulphide.32 The regularly demanded calibration of the OralChroma and
Halimeter was not reported in any study. That may be an explanation
for the tremendous differences between reported VSC values.
4.3.2 | Organoleptic scores
Regarding current literature, there are two main methods to assess halito-
sis. The comparison of both procedures however is almost impossible as
both methods have highly different approaches. Rosenberg established a
scoring system from 0 to 5 classifying the intensity of oral malodour.33,34
Reviewing Rosenberg’s system critically the reproducibility of scoring bad
breath by intensity might be questionable, as this method seems to be
fairly dependent on the investigator. Later, Seemann developed a scor-
ing system determining the distance in which oral malodour can be per-
ceived.35 Seemann’s procedure might lead to better reproducibility, as it
seems to be less dependent on the investigator’s subjective opinion.
4.3.3 | VSC values
Volatile sulphur compound values at baseline showed a wide range.
Using Halimeter, a differentiation between periodontal diseases and
healthy patients regarding VSC values was not possible. Baseline mean
values in periodontally diseased groups ranged from 66 to 1976 ppb,
while healthy controls showed 77 to 102 ppb. This may be attributed
to the fact that the Halimeter measures an overall VSC value, being
less sensitive for the periodontal-­related methyl mercaptan. Using the
OralChroma, periodontal patients showed three times higher mean
baseline values of methyl mercaptan than patients with gingivitis.
Regarding changes after SRP in periodontal patients, methyl
mercaptan levels were decreased (80% reduction), as was hydrogen
sulphide (related to tongue coating, 65% reduction). Again it should
be highlighted that the OralChroma measurements offer the most
specific results for this review’s topic.
4.4 | Limitations
The overall body of evidence is low for this review because of the
lack of RCTs focusing our question. Therefore, we present the best
 |
46       Deutscher et al.
available evidence regarding the impact of PTC or SRP on oral
halitosis.
Due to the heterogeneity of the included studies, no meta-­analysis
was performed. Most of these studies lack a classical control group
(selection bias) and compare different kinds of intervention (perfor-
mance bias).
Furthermore, there are known confounding factors such as smok-
ing habits and regular tongue cleaning, which can influence and might
alter instrumental measuring of sulphur compounds as well as organ-
oleptic staging.
5 |  CONCLUSION
Based on best available evidence, professional tooth cleaning or
non-­surgical periodontal therapy (scaling and root planning) in com-
bination with oral hygiene instructions reduced oral halitosis rep-
resented by VSC values and organoleptic scores in patients with
periodontal disease, independently of tongue cleaning and use of
mouthwashes.
For patients with oral halitosis, a treatment plan should include a
cause-­related strategy. In cases of enhanced methyl mercaptan levels
(indicating periodontal diseases), a treatment should start with pro-
fessional tooth cleaning or scaling and root planning. If patients show
increased hydrogen sulphide values that indicate tongue coating, this
problem should be targeted first. Patients treated for periodontitis
show reduced VSC levels and therefore might profit from the addi-
tional benefit of preventing or treating oral halitosis.
CLINICAL RELEVANCE
Scientific rationale for the study
Periodontal diseases are the second most common cause for oral
halitosis. Periodontal pathogenic germs produce VSCs and are known
to generate oral halitosis. Therefore, this review aimed to explore
whether reducing such bacteria by professional tooth cleaning and/
or scaling and root planing is able to cure oral halitosis in patients with
periodontal disease.
Principle findings
Both mechanical plaque removal and scaling and root planning reduce
oral halitosis. In patients suffering from periodontitis, the measured
VSC concentrations are more elevated than in patients with gingivitis
or periodontal healthy subjects. It is not possible to reduce halitosis
parameters below the thresholds in all described cases.
Practical implications
Within the limitation of this review (body of evidence is low), PTC and
SRP in healthy, gingivitis and periodontitis patients reduce VSC values
as well as organoleptic scores. The beneficial effect of PTC and SRP is
independent of the already proven tongue cleaning and use of mouth
rinses that should be need related combined in individual cases.
CO NFL I C T O F I NT ER ES T
The authors declare that they have no conflict of interests.
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How to cite this article: Deutscher HCD, Derman SHM,
Barbe AG, Seemann R, Noack MJ. The effect of professional
tooth cleaning or non-­surgical periodontal therapy on
oral halitosis in patients with periodontal diseases. A systematic
review. Int J Dent Hygiene. 2018;16:36–47. https://doi.
org/10.1111/idh.12306