J Periodontol • August 2008

Chlorine Dioxide and Chlorhexidine

Mouthrinses Compared in a 3-Day
Plaque Accumulation Model
Spiros Paraskevas,* Nanning A.M. Rosema,* Paula Versteeg,* Ubele Van der Velden,*
and G.A. Van der Weijden*

Background: The aim of this study was to investigate the

inhibiting effect of a chlorine dioxide mouthrinse as opposed
to a mouthrinse containing chlorhexidine (0.20%) during 3
days of plaque accumulation.
Methods: At baseline, all participants (N = 77) received a
professional prophylaxis and were randomly assigned to the
test (chlorine dioxide) or (positive) control (chlorhexidine)

P
laque is a biofilm with layers of
group. On the following 3 days, both groups rinsed twice daily microorganisms contained in a ma-
for 1 minute with 10 ml test or control solution. At the end of trix that forms on oral surfaces and
the experimental period, plaque was assessed, and the panel- is continuously bathed by saliva.1 The
ists filled out a questionnaire. relationship between plaque and peri-
Results: Chlorhexidine inhibited plaque growth significantly odontal inflammation was established
more than the mouthrinse containing chlorine dioxide (plaque decades ago.2,3 Furthermore, several stud-
index = 1.39 versus 1.96, respectively; P <0.001). The results ies4-6 demonstrated the importance of
of the questionnaire showed that the panelists found chlorhex- plaque as an etiologic factor of periodon-
idine easier to use and more effective. However, they preferred titis. This led to the concept that strict
the taste of the chlorine dioxide mouthrinse and experienced plaque control is a prerequisite for a sta-
less taste alterations. ble and healthy periodontal condition.7
Conclusion: Chlorine dioxide mouthrinse seems to be a Since that time, several approaches have
less potent plaque inhibitor than chlorhexidine. J Periodontol been developed to control plaque growth.
2008;79:1395-1400. Plaque removal by mechanical means
(mostly a toothbrush combined with den-
KEY WORDS
tifrice) seems to be a common way of
Chlorhexidine; chlorine dioxide; clinical trial; dental plaque. controlling plaque.8 However, factors,
such as dexterity and motivation, can limit
the effectiveness of daily self-performed
* Department of Periodontology, Academic Center for Dentistry Amsterdam, Amsterdam,
The Netherlands. oral hygiene.9
A chemical approach has been intro-
duced to deal with the potential defi-
ciencies of daily self-performed oral
hygiene.10 The challenge with chemical
plaque control is to develop an active
antiplaque agent that does not disturb
the natural flora of the oral cavity. The
use of an antibioticum could be a tempt-
ing idea to control the growth of microor-
ganisms, but it has severe limitations
(risks of bacterial resistance, hypersensi-
tivity reactions, or superinfections).11 Ad-
ditionally, the incorporation of a pathogen
in a biofilm can protect this organism
from concentrations of antimicrobials that

doi: 10.1902/jop.2008.070630

1395
Chlorine Dioxide and Chlorhexidine Mouthrinses
would normally kill or inhibit those organisms freely
suspended in water (planktonic bacteria). The effective-
ness of antimicrobials, as measured with in vitro tests, is
dramatically reduced in vivo because of the properties
of the microbial community.12,13 Mature, intact biofilms
are less sensitive to such agents because the exopoly-
mer matrix, bacterial enzymes, and low growth rate
hinder the action of chemotherapeutic agents.14
For many years, researchers have searched for
an effective chemical agent that would prevent oral
plaque growth and, thereby, could replace mechani-
cal plaque control. Chlorhexidine (CHX) seems to be
the most effective chemical agent in short- and long-
term use.15 Because of its established use and efficacy,
CHX is the gold standard against which other chemical
factors should be compared when claims of efficacy
are attempted.
Although CHX has a relatively low toxic effect fol-
lowing oral use,16 it is not without side effects. The
most common are staining of the tooth surfaces and
taste alteration,17,18 but dryness, bitter taste, sore-
ness, burning sensation, and numbness are also re-
ported.17,19 Taste impairment may occur as soon as
after the first day of rinsing and can last as long as reg-
ular rinses are applied. These are reversed after ces-
sation of the CHX rinses.20 It is not uncommon for
patients, particularly children and poorly motivated
adults, to refrain from using CHX for this reason.21
A study by Helms et al.22 indicated that CHX re-
duced the perceptual intensity of sodium chloride
and quinine-HCl solutions. This was also found in a
study by Marinone and Savoldi,23 who reported that
hypogeusia induced by CHX concerns specifically
the salt and bitter taste components. Such side ef-
fects may negatively influence the compliance of
patients.
Because of the side effects reported, new chemical
agents that would exert the same efficacy as CHX
without its side effects are being researched. Chlorine
dioxide (ClO2) is a chemical agent with known antimi-
crobial properties. It is increasingly used in different
industries, including the dairy, beverage, and food in-
dustries, to control microbiologic growth and for the
removal of biofilms.24 It is an oxidizing biocide, impli-
cating that it kills microorganisms by disruption of the
transport of nutrients across the cell wall. ClO2 is a gas
at room temperature. The relatively stable free radical
species ClO2 is a chemical oxidant with powerful
bactericidal, viricidal, sporicidal, cysticidal, algicidal,
and fungicidal properties. The oxidative consumption
of critical biomolecules by ClO2 is primarily responsi-
ble for its wide range of biocidal activity, and its single-
electron reduction product (ClO2-) can also act as a
reactive oxidant toward many electron-donating bio-
molecules (e.g., methionine, pyruvate, urate, and en-
dogenous thiols, such as cysteine).16
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Volume 79 • Number 8
Therefore, the aim of the present study was to as-
sess the plaque growth inhibition of a ClO2-containing
mouthrinse compared to a CHX-containing mouthrinse
during a 3-day de novo plaque-accumulation model.
MATERIALS AND METHODS
Study Population
The study population consisted mainly of university
students from Amsterdam and surrounding areas.
The subjects were recruited by advertisements. All
candidates were screened for suitability by the re-
search team. Seventy-seven healthy subjects (43 fe-
males and 34 males; age range, 18 to 48 years; mean
age: 23.2 years) participated in the study. Selection
criteria were a dentition with ‡20 evaluable teeth
(minimum of five teeth per quadrant), no oral lesions,
no severe periodontal problems (no probing depth
‡5 mm), and no removable prostheses or orthodon-
tic bands or appliances. Persons allergic to several
mouthrinse components were excluded from the study.
All eligible subjects were given oral and written in-
formation about the products and the purpose of the
study and were asked to sign an informed consent.
The study was conducted from June 10, 2004 to July
15, 2005 in the Department of Periodontology, Aca-
demic Center for Dentistry Amsterdam, in accor-
dance with the ethical principles originating in the
Declaration of Helsinki and consistent with good clin-
ical practices.
Study Design
The study was designed as an examiner-masked,
two-group parallel experiment. At baseline, plaque
was disclosed, and all participants received a thor-
ough supragingival scaling and polishing to remove
all plaque, stain, and calculus. This was performed us-
ing hand instruments, mechanical scalers, and rotat-
ing brushes with polishing paste. Special attention
was paid at interproximal areas where dental floss
was used. To ensure that all deposits had been re-
moved, a second disclosing episode was carried out
after which any remaining plaque was removed.
Subjects were randomly assigned to the test or con-
trol group. Randomization was performed using com-
puter-generated random numbers. The allocation of
test or control products was carried out by a person
not directly involved in the research project.
During a 3-day experimental non-brushing period,
subjects in the test group used a ClO2 mouthrinse†
twice daily, whereas subjects of the (positive) control
group used a 0.2% CHX mouthrinse.‡ All participants
† 10 Quist-forte (containing 100-ppm free ClO2). The rinse is activated
when 5 ml base solution is mixed with 5 ml activator solution. De Witte
Tanden Winkel, Rotterdam, The Netherlands.
‡ Corsodyl (containing 0.20% chlorhexidine digluconate, ethanol, polyoxyl
hydrogenated castor oil, sorbitol, E-125, purified water), GlaxoSmithKline,
Zeist, The Netherlands.
J Periodontol • August 2008
were instructed to refrain from using any other means
of oral hygiene during the experimental period.
The subjects in the test group received two bottles
(5 ml in each bottle) of mouthrinse that had to be
freshly mixed for each rinsing episode. The positive
control group received one bottle of mouthrinse con-
taining 200 ml 0.2% CHX. All subjects were instructed
to rinse twice a day, in the morning and in the evening,
with 10 ml solution for 60 seconds, after which they
expectorated. Subsequent rinsing with water was
not allowed. Written instructions were provided ex-
plaining how to use the mouthrinse. Rinsing was per-
formed at home without supervision. To check for
compliance, subjects were asked to note the times
of day when they rinsed.
After 3 days, subjects returned to the clinic for the
plaque assessments. The dentition was disclosed with
a disclosing solution.§ Subsequently, the level of
plaque was assessed at six sites per tooth using the
Quigley and Hein25 index as modified by Turesky
et al.26 and further modified by Lobene et al.27 All
measurements were carried out under the same con-
ditions by the same investigator (PAV) who was un-
aware of the allocation of the mouthrinse to the
participants. Finally, after plaque scoring, all subjects
received a questionnaire using a visual analog scale
(VAS) designed to evaluate their attitudes with regard
to the product used. Subjects marked a point on a
10-cm-long uncalibrated line with the negative ex-
treme response (0) at the left end and the positive
extreme response (10) at the right end.
Statistical Analysis
The study population size was calculated a priori. Us-
ing a power calculator, it was determined that ‡60
subjects were necessary so that a difference of 0.26 –
0.4 of the mean plaque index could be identified with
an a error level of 0.05 and ‡80% power.
The plaque scores were used as the main response
variable. Mean plaque values were calculated at
the subject level. By definition, those values are arith-
metic means of a series of ordinal scales units. A dis-
tribution of those mean values that approximates a
normal distribution is not uncommon. Nevertheless,
the problem remains that plaque indices are not
proportional scales. Although some parametric sta-
tistics (t test) were proven to be robust with respect
to the assumption of normality of the distribution
within the treatment populations, non-parametric sta-
tistics (Mann-Whitney U-test) are more powerful
when data show skewed distributions. Thus, it was de-
cided that non-parametric tests (Mann-Whitney test)
would be more appropriate to compare the differ-
ences between the two groups. Explorative analysis
was performed to investigate the origin of the overall
differences. Data were categorized according to upper
Paraskevas, Rosema, Versteeg, Van der Velden, Van der Weijden
and lower jaw, tooth types, and surfaces. P values
<0.05 were accepted as statistically significant.
RESULTS
All subjects (N = 77) completed the 3-day experimen-
tal period. The plaque scores for the test and control
groups at the end of the experimental period are dis-
played in Table 1. There was a significant difference in
plaque levels between the two groups. In the control
group, the mean overall mouth plaque index was
1.39 compared to 1.96 in the test group. This differ-
ence of 0.57 between the two groups was statistically
significant (P <0.001). Exploratory analysis was car-
ried out to assess the origin of this difference (Table1).
This analysis showed that the difference in plaque re-
duction between the two groups was maintained when
plaque levels for different jaws, surfaces, or tooth
types were examined.
The results of the questionnaire are shown in Table 2.
With regard to subjects’ rating of the rinsing time
(question 5), the results demonstrated no difference
between the test and control groups (5.3 and 5.7, re-
spectively). However, with respect to the other ques-
tions (taste perception, duration of taste, alteration in
taste perception, convenience, and plaque-control
efficiency), statistically significant differences were
noted between groups. More specifically, subjects
preferred the taste of ClO2 mouthrinse (VAS 5.5) over
the taste of CHX (VAS 3.6; P <0.001). They also expe-
rienced that the taste duration (aftertaste) in their
mouth after rinsing with ClO2 (VAS 6.4) was much less
than after rinsing with CHX (VAS 3.8; P <0.001). Also,
they preferred ClO2 (VAS 4.6) to CHX (4.0) with re-
spect to alterations in taste perception (P = 0.048).
The subjects were also asked to evaluate the conve-
nience of use and the plaque-reduction efficacy. Sub-
jects found CHX more convenient to use (VAS 5.7)
than ClO2 (VAS 5.3; P <0.001). They also considered
CHX (VAS 6.8) more effective in reducing plaque in the
mouth compared to the ClO2 mouthrinse (VAS 4.0;
P <0.001).
DISCUSSION
The present study was designed to determine the plaque-
inhibiting effect of ClO2 compared to 0.2% CHX. It
used a 3-day non-brushing model that allowed for
plaque accumulation. This design was previously used
to assess the effect of various mouthwashes.19,28,29
Zee et al.30 and Simonsson31 also used this 3-day
model to discern between ‘‘rapid’’ and ‘‘slow’’ plaque
formers. It was a convenient model with which to as-
sess the plaque-inhibitory capacity of the test product
per se and determine its relative activity in relation to
the well-established action of CHX. Using such a 3-day
§ Mira-2-Tone, Hager & Werken, Duisburg, Germany.
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Chlorine Dioxide and Chlorhexidine Mouthrinses Volume 79 • Number 8

Table 1. When ClO2 is photo-oxidized by sunlight, it falls apart.

The end products of ClO2 reactions are chloride (Cl-),
Total Plaque Index (mean – SD) for the
chlorite (ClO-), and chlorate (ClO3-).
Test and Control Groups and Exploratory The existing literature provides information on
Analysis for Different Jaws, Surfaces, mouthrinses containing acidified sodium chlorite so-
and Tooth Categories lution (ASC) that can be activated at low pH by mixing
it with a certain acid. A reaction by-product is ClO2,
0.2% CHX P ClO2 which is probably present at a low concentration.
(n = 37) Value* (n = 40) Conversion rates for ClO2 range from 1% to 10%
and are typically proportional to the amount and
Overall 1.39 – 0.42 <0.001 1.98 – 0.40
strength of the acid added to the sodium chlorite so-
All upper 1.32 – 0.47 <0.001 1.94 – 0.42 lution. ClO2 has been used in mouthrinse form for
the treatment of oral malodor. The ability of ClO2 to
All lower 1.48 – 0.44 <0.001 2.01 – 0.44
reduce malodor is well documented.34 A single use
All vestibular 1.59 – 0.48 <0.001 2.43 – 0.46 of ClO2-containing mouthrinse significantly improved
mouth odor pleasantness and reduced mouth odor in-
All lingual 1.19 – 0.42 0.002 1.49 – 0.41
tensity and volatile sulfur compound concentrations
All approximal vestibular 1.80 – 0.44 <0.001 2.54 – 0.42 in mouth air for ‡8 hours after use.35 ClO2 substan-
tially reduced salivary Streptococcus mutans and lac-
All mid-vestibular 1.18 – 0.61 <0.001 2.21 – 0.59
tobacilli levels; as expected, mineral water exerted no
All mid-lingual 0.70 – 0.52 0.007 1.02 – 0.50 influence on the salivary levels of each of these micro-
organisms.16
Front 1.27 – 0.42 <0.001 1.88 – 0.40
Little is known about the influence of ClO2 on
Premolars 1.35 – 0.48 <0.001 1.92 – 0.40 plaque accumulation. A pilot double-masked, cross-
over study36 examined the effect of a metastabilized
Molars 1.62 – 0.46 <0.001 2.13 – 0.48
chlorous acid/ClO2 mouthrinse on plaque accumula-
* Mann-Whitney test. tion and salivary bacteria. Eighteen subjects were re-
cruited and rinsed twice daily with the test (high or low
plaque accumulation model provides a general indica- concentration of ASC)i or placebo mouthrinse for
tion of how the product in question would perform under 5-day periods separated by washout periods of 9
actual conditions, insofar as significant plaque reduc- days. The results demonstrated significant plaque re-
tion is a prerequisite for the reduction in gingivitis.32 ductions for the test (high and low concentrations of
ClO2 exists as synthetic greenish-yellow to orange ASC) mouthrinses compared to the placebo product.
gas with a characteristic pungent chlorine-like odor at These reductions in plaque were not accompanied by
room temperature. It is a neutral chlorine compound. significant reductions in salivary bacterial counts. Ac-
ClO2 is different from elementary chlorine in its chem- cording to the investigators, this may be the result of
ical structure and behavior. ClO2 is a small, volatile, the low substantivity of ClO2 as opposed to CHX.
and very strong molecule. It was discovered in 1814 However, the outcomes of another study37 are not
by Humphrey Davy.24 He first produced this gas by in concordance to this. This particular study was also
pouring sulfuric acid (H2SO3) on potassium chlorate designed in a double-masked, cross-over manner and
(KClO3). Next, he replaced sulfuric acid with hypo- tested the effect of three different formulations of
chlorous acid (HOCl). This reaction is used to produce ASC¶ compared to the CHX and placebo mouthrinses.
large quantities of ClO2. Sodium chlorate (NaClO3) is The three test solutions demonstrated equivalent anti-
now used most frequently instead of KClO3. The fol- bacterial activity to CHX for plaque as well as for bac-
lowing reaction takes place: 2NaClO3 + 4HCl / terial salivary counts. The investigators concluded
2ClO2 + Cl2 + 2NaCl + 2H2O. that the test products had comparable substantivity
ClO2 is an unstable gas that dissociates into chlo- to CHX. These outcomes are not in line with the results
rine gas (Cl2), oxygen gas (O2), and heat. One of of the present study, in which CHX was more effective
the most important qualities of ClO2 is its high water in reducing plaque levels than was ClO2. The reason
solubility, especially in cold water. It is ;10 times may be attributed to differences in study methodol-
more soluble in water than chlorine. ClO2 is a free rad- ogy, such as the rinsing time (30 seconds versus 60
ical in diluted, watery solutions but is quite stable if seconds) and supervised versus unsupervised rins-
kept cool and in the dark. Once the gas is absorbed ing. Certainly, more research is necessary to gain
in water, it has a low volatility. For this reason, inha-
lation exposure is anticipated to be minimal.33 At high i Alcide, Redmond, WA.
concentrations it reacts strongly with reducing agents. ¶ Alcide.

1398
J Periodontol • August 2008
Table 2.
Questionnaire Responses (mean – SD) Determined by VAS
Question
1) How was the taste of the product? Very bad
2) How long did the taste remain in the mouth after Very long
rinsing?
3) How was your taste of food and drinks affected? Negative change
4) Was the use of the mouthrinse convenient? Not convenient
5) What is your opinion about the rinsing time? Very long
6) What was your perception of the plaque reduction? Insufficient
* Mann-Whitney test.
more insight into the level of plaque inhibition
achieved with this chemical agent. Studies of longer
duration, in which the product in question is compared
to other control (positive or negative) or placebo pro-
ducts and where the safety and microbiological pa-
rameters will be assessed, are necessary to establish
the effectiveness of this product and its place among
the other agents used for chemical support of daily
mechanical plaque removal.
CONCLUSIONS
ClO2 mouthrinse was a less potent plaque inhibitor
than CHX. However, subjects preferred the taste of
the ClO2 mouthrinse and experienced less taste alter-
ations compared to CHX.
ACKNOWLEDGMENTS
The authors express their appreciation to Cor Quist,
De Witte Tanden Winkel, Rotterdam, The Netherlands,
for providing the test mouthrinse; Gerben Dreijer,
GlaxoSmithKline, Zeist, The Netherlands, for provid-
ing the chlorhexidine mouthrinse; and A.T. Klitsie and
E.M. Oud, Academic Center for Dentistry Amsterdam
(ACTA), for their help in the realization of this project.
This study was supported by university funds (Depart-
ment of Periodontology, ACTA). The authors report
no conflicts of interest related to this study.
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Correspondence: Dr. S. Paraskevas, Department of Peri-
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Submitted December 7, 2007; accepted for publication
February 6, 2008.