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Comparative oral health status of an adult Sudanese population using miswak
or toothbrush regularly
Article · January 2004
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29
Comparative oral health status of an adult Sudanese population
using miswak or toothbrush regularly
Ismail Abbas Darout, DDS, PhD and Nils Skaug, DDS, PhD
The objective of the present study was to conduct a systematic evaluation of miswak as an alternative tool to the modern toothbrush
in preventing oral diseases. This involved clinical, microbial and chemical assessment using modern scientific methods. An adult
Sudanese population using miswak or a modern toothbrush regularly was examined using clinical and microbial parameters. Freeze-
dried extract of miswak was analyzed for antimicrobial components. The results showed a lower caries experience in the miswak
users than in the subjects who used a modern toothbrush. There were no significant differences between the two groups in the
periodontal variables examined except for less calculus in the posterior sextants of miswak users. The results also indicated that
regular use of miswak had a significant inhibitory effect on the levels of some salivary and subgingival plaque bacteria. The chemical
analysis of miswak extracts showed that miswak contained a number of antimicrobial components including Cl-, SO42-, SCN-, NO3-.
These findings partially support the hypothesis that (1) adult Sudanese regular miswak users have better oral health and lower levels
of oral pathogens than have adult Sudanese who use a modern toothbrush regularly and (2) these beneficial effects may be due to
leachable SCN- in miswak.
Introduction procedure that includes brushing of teeth, gums
and tongue is completed, miswak is removed from
The use of miswak could be traced back at least to or may be left in the mouth for some additional
time. Left in the mouth, it will stimulate salivation
pre-Islamic times.1 Currently, many of the world
and thus, there may be a better cleansing effect.
populations in India, Pakistan, several African
countries, the Arab countries and most of the
Muslim world still use miswak.2 In geographical Mechanical Effect of Miswak
regions in which the Arak (Araak) shrub or tree
Miswak is generally used for a longer period of
(botanical name Salvadora persica L) grows,
time than is a modern toothbrush and the cleaning
miswak is interpreted as tooth sticks prepared
is usually implemented for 5 to 10 min each time.4
from this plant. Where S. persica is not growing,
T h e p l a n t f i b e r s re m o v e p l a q u e a n d
miswak is prepared from other suitable plants.
simultaneously massage the gum. Unlike a
Miswak is a pencil-sized stick 15-20 cm long and
modern toothbrush, the bristles of miswak are
with diameter 1-1.5 cm that is prepared from the
situated along the long axis of its handle.
root, stem, twigs or bark. The stick is chewed or
Consequently, the facial surfaces of the teeth can
tapered at one end until it becomes frayed into a
be reached more easily than the lingual surfaces
brush.
or the interdental spaces. Eid et al.5 reported that
the majority of miswak users applied miswak to
Cleansing Efficacy of Miswak
both aspects of their teeth and no significant
differences in facial plaque scores were noted
Various explanations3 for the cleansing
between the miswak and toothbrush users.
efficacy of miswak have been offered including (i)
Additional studies suggested that miswak efficacy
the mechanical effects of its fibers, (ii) its release
was comparable to that of the conventional
of beneficial chemicals and (iii) a combination of
(i) and (ii).3 Also, when the mouth cleaning Address reprint requests to:
Ismail A. Darout
Received 7 June 2003; Revised 7 November 2003 Laboratory of Oral Microbiology
Accepted 2 December 2003 Armauer Hansens Hus, Haukelandsvn. 28
Department of Odontology - Oral Microbiology N-5021 Bergen, Norway
Faculty of Dentistry and Centre for International Health Fax: 47-55974979
University of Bergen, Bergen, Norway E-mail:
[email protected] Saudi Dental Journal, Vol. 16, No. 1, January - April 2004
30 COMPARATIVE ORAL HEALTH STATUS OF AN ADULT SUDANESE
tootbrush6 or demonstrated plaque scores to be diet. Similar results were noted in Saudi children
significantly lower following the use of miswak aged 13 to 15 years when compared with children
when compared with the conventional toothbrush in western countries.15 Again, the main preventive
used without toothpaste.7 factor reported was miswak use by these children.
Carl and Zambon10 reported that dental caries was
Beneficial Substances in S. Persica Extracts relatively rare among Kenyan primary school
children who were using only miswak as an oral
A variety of chemical components have been hygiene tool. The authors concluded that caries in
identified in S. persica extracts. Some of these adults was mostly present in older persons and
have been suggested to contribute to the usually involved the maxillary and mandibular
cleansing efficacy of miswak. Miswak extracts second and first molars, which are difficult to
have also been shown to inhibit the growth of reach for cleaning with miswak. It has also been
different microorganisms. In addition, a decoction demonstrated that users of chewing sticks not
of S. persica has been used for the treatment of prepared from S. persica, had low caries
many diseases. These topics have been prevalence compared to modern toothbrush
extensively reviewed by others.8 It remains, users.16
however, to be shown that beneficial substances
are leaching out in saliva while miswak is kept in Rationales of our Study
the mouth in amounts that will benefit oral health.
Surprisingly, despite the widespread use of
Epidemiological Studies miswak since ancient times, relatively little
scientific attention has been paid to its oral health
Periodontal Disease beneficial effects. In 1987, the WHO17 encouraged
developing nations to use miswak for oral hygiene
Low periodontal treatment needs have been because of tradition, availability and low cost.
reported among Saudi adults who use miswak.9 Recently, it was concluded that chewing sticks may
Furthermore, Gazi et al . 7 compared the have a role to play in the promotion of oral hygiene
periodontal status of habitual users of miswak or and that evaluation of miswak effectiveness
toothbrush and showed that the former had lower warranted further research.18
gingival bleeding and interproximal bone height
than the toothbrush users. The same authors also Study Hypothesis
indicated that there were no significant
differences in plaque scores and pocket depths Based on our experience from the Sudan and
between the two groups. Carl and Zambon10 available information in the literature, we
suggested that in northern Kenya advanced formulated a working hypothesis that miswak
periodontal disease was very rare among persons users have a better oral health and lower levels of
over the age of 50 years who used miswak for oral pathogens than modern toothbrush users and
teeth brushing. Eid et al.11 reported that there that thiocyanate contributes to the oral health
were no significant differences in gingival or promoting effect of miswak.
bleeding indices between miswak and modern
toothbrush users. Objective and Aims of the Study
Caries The objective was to conduct a systematic
evaluation of miswak as an alternative to the
In a dental health survey in Sudan, Emslie12 modern toothbrush in preventing oral diseases by
using modern scientific methods of clinical,
reported for the first time less caries in people
microbial and chemical assessments. Specific aims
using chewing sticks than in those using a modern
were:
toothbrush. In a controlled clinical study,
Baghdady and Ghose13 compared the caries
1. To assess and compare in a population of adult
prevalence between Iraqi and Sudanese
Sudanese habitual miswak users and
schoolchildren using the WHO DMFT (diseased, toothbrush users: (a) their periodontal status
missing, filled teeth) index.14 They reported that using prevalence of gingival bleeding, dental
Sudanese schoolchildren showed lower caries calculus, probing pocket depth (PPD) and
prevalence due to the use of miswak and their clinical attachment level (CAL) as clinical
Saudi Dental Journal, Vol. 16, No. 1, January - April 2004
DAROUT and SKAUG 31
parameters; (b) salivary bacterial levels and and was defined as the distance from the
their relationships with the periodontal status cementenamel junction (CEJ) to the bottom of a
and experience of caries, respectively, of the pocket/sulcus. Caries experience was recorded as
test subjects; (c) levels and associations of present or absent according to the WHO caries
subgingival plaque bacteria with respect to oral criteria.20
hygiene and periodontal status at the sampled
sites. Selection of Subjects for Biological Sampling
2. To identify and quantify some potentially
antimicrobial anionic components of S. The inclusion criteria of this study group
persica root and stem aqueous extracts. required at least one maxillary and one
mandibular tooth with PPD >4 mm that showed
Materials and Methods gingival bleeding on probing. Using the
measurements of PPD, one maxillary and one
Study Group mandibular posterior tooth exhibiting 4-5 mm or
>6 mm PPD and bleeding on probing were
The participants were employees and students selected for bacterial sampling. If posterior teeth
at the Medical Sciences Campus, University of were missing, anterior teeth were used instead.
Khartoum, Khartoum, Sudan. A total of 213 Seventy-four subjects were sampled. These
individuals volunteered to participate in the study. included 38 miswak users (27 males and 11
Their age ranged between 19 and 65 years (mean
females) and 36 toothbrush users (35 males and 1
36.6 ± 8.7 years), and they included 201 males
(mean age 36.6 years) and 12 females (mean age female). Fifty-six of the subjects also donated
35.6 years). saliva samples; 30 were miswak users (19 males
and 11 females) and 26 toothbrush users (25 males
Inclusion Criteria and 1 female).
The selection criteria for inclusion in the study Collection of Biological Samples
were dentate subjects > 18 years of age who had
18 or more teeth present, had good general Collection of saliva from the study subjects has
health, and used either miswak or toothbrush been previously reported.21 Immediately after
regularly as their main oral hygiene tool. In saliva collection, the teeth of each individual
addition, a subject must not have used antibiotics selected for subgingival plaque sampling were
during the preceding 3 months and had no isolated with cotton rolls, carefully scaled
present or past history of smoking cigarettes or supragingivally with sterile Gracey curettes,
using other tobacco products. Regular users of cleaned with sterile cotton pellets and dried with
miswak or toothbrush were defined as individuals air. A sterile curette was then inserted into the
who reported using miswak or toothbrush, pocket and subgingival plaque was collected by
respectively, as their main oral hygiene method at multiple scaling strokes of the 6 probing sites per
least once a day for the past year. Consenting selected tooth. The plaque collected from one
subjects were then subjected to a structured maxillary and one mandibular tooth (totally 12
interview to assess their demographic profile and sites) of each subject was pooled and immediately
oral hygiene habits. In all, 109 subjects (age range transferred into one Eppendorf tube containing
20-61 years, mean 36.1 years), 11 females and 98 150 μl of sterile TE buffer (10 mM Tris-HCl, 1.0 mM
males were regular miswak users, and 104
EDTA, pH 7.6) and the plaque samples were then
subjects (age range 20-65 years, mean 35.7 years),
1 female and 103 males, used toothbrush suspended into the buffer by vigorous shaking.
regularly. The periodontal status of the study
group has been published elsewhere.19 Identification and Quantification of Bacteria
Clinical Examinations Handling of the biological samples and
identification and quantification of bacteria using
The periodontal status of the study subjects whole genomic DNA probes from 28 bacteria
was assessed using the Community Periodontal (plaque samples) or 25 bacteria (saliva samples)
Index (CPI).20 Each sextant was given the highest and checkerboard DNA-DNA hybridization22 have
score of examined teeth. CAL was then assessed been previously published.21
Saudi Dental Journal, Vol. 16, No. 1, January - April 2004
32 COMPARATIVE ORAL HEALTH STATUS OF AN ADULT SUDANESE
Chemical Analysis of S. Persica Freez-Dried with gingival bleeding and PPD 4-5 mm (P=0.03)
Extract and CAL >4 mm (P=0.02) than had the 30-39 year
group. The overall effect of the two oral hygiene
Aliquots of the powdered extracts were methods showed no marked differences as
reconstituted in sterile distilled water, filtered assessed by the periodontal variables (i.e. PPD and
through a 0.2 mm membrane (Millipore Corp.) CAL) used in this population. However, when the
and, used for identification and quantification of data were reanalyzed in order to test the effect of
potentially antimicrobial anionic components by tooth type, the results demonstrated that miswak
using capillary electrophoresis.23 users had significantly (P=0.002) lower numbers of
sextants with dental calculus in the posterior
Data Analysis sextants than had toothbrush users (Table 1).
The percentage of subjects and the mean Table 1. The mean number of sextants per subject with gingival
bleeding, supragingival calculus, probing depth, and clinical
number of sextants per subject with gingival attachment loss adjusted for age, by oral hygiene group and
bleeding, calculus, PPD 4-5 mm and PPD >6 mm, tooth type.
and CAL as well as the number and percentage of
Variables Oral hygiene Mean S.E. P-value
subjects with sound teeth or having teeth with group
caries experience were calculated according to
Darout et al.19,21 The mean values of pocket Anterior teeth
depths 4-5 mm and > 6 mm was computed for each
tooth and the teeth values were averaged for each Gingival bleeding miswak 0.30 0.05 0.5
toothbrush 0.34 0.05
subject. The analysis of variance for unbalanced Dental calculus miswak 0.22 0.04 0.4
data was used to compare the study subjects, and toothbrush 0.17 0.04
the model was adjusted for age groups (20-39 Probing depth > 4 mm miswak 0.04 0.01 0.05*
years and 40-65 years) as described by Darout toothbrush 0.009 0.01
et al.19. The percentages of subjects with various Attachment loss > 4 mm miswak 0.53 0.06 0.2
toothbrush 0.42 0.07
bacterial levels grouped by age, gender,
periodontal status, and oral hygiene were Posterior teeth
compared by the Wilcoxon Signed Rank test. The t
test was used to compare the percentages of Gingival bleeding miswak 0.94 0.12 0.09
subjects by caries status, as well as, the toothbrush 1.22 0.12
Dental calculus miswak 0.11 0.05 0.002*
concentrations of different anionic components in toothbrush 0.35 0.06
miswak extracts. The Spearman correlation Probing depth > 4 mm miswak 0.10 0.05 0.057
coefficient was utilized to assess the strength of toothbrush 0.23 0.05
correlation between cariogenic species (>105 Attachment loss > 4 mm miswak 0.64 0.04 0.20
cells) and the caries scores and between bacterial toothbrush 0.55 0.04
levels. P value <0.05 were considered statistically * Statistically significant
significant. A a value of 0.01 was used when
multiple comparisons were made, and this Salivary Bacteria
adjustment was in accordance with the method of
Hochberg. 24 The statistical analysis was Subjects with one or more sextants with PPD 4-
performed by the SAS statistical package (SAS 5 mm or two or more sextants with CAL >4 mm had
version 6.12, SAS Institute Inc., Cary, NC, USA). similar levels of most salivary bacteria compared to
subjects without attachment loss or deep >6 mm
Results PPD. Presence of >105 Lactobacilus acidophilus
bacterial cells in saliva was significantly correlated
Periodontal Status with the subject's caries score (P=0.02). The
percentages of subjects with detectable levels of
Fifty-four percent of the total study groups had Actinobacillus actinomycetemcomitans,
one or more sextants with gingival bleeding and Prevotella melaninogenica, Campylobacter
31.9% dental calculus in one or more sextants. rectus, Peptostreptococcus micros,
Approximately, 10% of the subjects had one or Veillonella parvula, Streptococcus mutans,
more sextants with PPD 4-5 mm and about 2% had Streptococcus anginosus, Actinomyces
sextants with PPD >6 mm. Fifty-one percent of the israelii, Capnocytophaga sputigena, and
subjects had CAL > 4 mm in one or more of the Capnocytophaga gingivalis were significantly
sextants. Subjects in the age group 40-65 years had higher in the miswak group whereas for
significantly (P=0.004) higher numbers of sextants Prevotella intermedia, Fusobacterium
Saudi Dental Journal, Vol. 16, No. 1, January - April 2004
DAROUT and SKAUG 33
nucleatum, Selenomonas sputigena, frequencies of the investigated species varied
Eikenella corrodens, Lactobacillus between 2.6% and 47.4% in the miswak group and
acidophilus, Streptococcus sanguis, between 2.8% and 36.1% in the toothbrush group.
Streptococcus salivarius, Streptococcus Similarly, the prevalences of periodontopathic
oralis, and Streptococcus mitis the species including Porphyromonas gingivalis,
percentages of subjects were significantly higher Treponema denticola, Tannerella
in the toothbrush group (Table 2). In the miswak forsythensis (Bacteriodes forsythus), P.
group, 16 (53.3%) subjects had one or more teeth intermedia, A. actinomycetemocmitans, and
with primary or recurrent caries score as compared V. parvula were between 10.5% and 36.8%, and
between 2.8% and 19.4% in the two groups. There
Table 2. Percentage of subjects showing detectable levels of were significantly (P=0.05) more miswak users
bacteria in saliva, by type of oral hygiene habit than toothbrush users harboring Streptococcus
intermedius, A. actinomycetemocmitans, V.
Miswak Toothbrush
(n=30) (n=26) parvula, A. israelii and C. gingivalis, and
No. of No. of significantly fewer of the former group harboring
bacteria bacteriap S. sputigena, S. salivarius, Actinomyces
Bacterial species* 105 >106 105 >106 P naeslundii and S. oralis. Significantly more
subjects with PPD >6mm harbored P. gingivalis,
P. gingivalis 56.7 0 50.0 7.7 0.7 T. denticola, T. forsythensis, F. nucleatum
A.actinomycetemcomit 33.3 30.0 11.5 0 0.0001
ans 56.7 3.3 50.0 26.9 0.03
and V. parvula than did the subjects with PPD 4-5
P. intermedia 40.0 30.0 0.0 0 0.0001 mm.
P. melaninogenica 20.0 0 42.3 15.4 0.002
F. nucleatum
T. denticola
20.0 0 8.0 4.0 0.5 Correlations Between Salivary and
C. rectus 73.3 13.3 23.1 11.5 0.001 Subgingival Bacteria in Autologous Samples
P. micros 53.3 0 0.0 0 0.0001
S. sputigena 60.0 10.0 34.6 57.7 0.0002
S. intermedius 26.7 0 34.6 0 0.5 There were significantly higher percentages of
E. corrodens 40.0 0 34.6 30.8 0.01 subjects with > 10 5 bacterial cells of P.
V. parvula 60.0 13.3 11.5 3.9 0.0001 intermedia, C. rectus, V. parvula, S. mutans,
S. mutans L. acidophilus, S. anginosus, S. salivarius,
26.7 0 3.9 0 0.03
S. sobrinus 3.3 0 0.0 0 0.4
and L. buccalis, and significantly lower
L. acidophilus 13.3 0 46.2 0 0.01 percentages of subjects with T. denticola in saliva
S. anginosus
than in subgingival plaque (p£ 0.01). Significantly
S. sanguis 50.0 46.7 19.2 19.2 0.0001 higher percentages of subjects demonstrated >
S. salivarius 53.3 3.3 30.8 57.7 0.0001 10 6 bacterial cells of S. sputigena, S.
S. oralis 70.0 3.3 57.7 34.6 0.002
S. mitis 20.0 0 57.7 7.7 0.0005 anginosus, S. sangius and S. salivarius while
A. israelii 0 0 19.2 0 0.02 significantly lower percentages of subjects
C. sputigena 50.0 0 7.7 0 0.001 showed P. gingivalis in saliva than in subgingival
C. gingivalis 73.3 3.3 11.5 0 0.0001
C. gracilis plaque (P < 0.01). Significant correlations between
66.7 0 7.7 0 0.0001
L. buccalis 46.7 0 26.9 7.7 0.6
the levels of salivary and subgingival plaque
30.0 0 19.2 0 0.4 bacteria were exhibited between P. gingivalis, F.
*Subdivided into 3 categories of bacteria: periodontitis- nucleatum, S. sputigena, S. sangius, and
associated (n=12), cariogenic species (n=3), and species Streptococcus mitis (P<0.05) as seen in Table 3.
associated with dental health (n=10). When such correlations were made separately for
P<0.05 = statistically significant. miswak users and toothbrush users, the former
group demonstrated significant correlation
to 36 (76.9%) subjects among the toothbrush users between the levels of F. nucleatum and S. oralis
(P=0.03). (P<0.01). No significant correlations were shown
Subgingival Bacteria between these bacterial levels in the toothbrush
users.
The detection frequencies of the 28 Identification and Quantification of Some
investigated species at <105, 105 and > 106 Potentially Antimicrobial Anionic
bacterial cells varied between 33.8% and 100%,
Components of Miswak Extracts
1.4% and 37.8%, and 1.4 and 41.9%, respectively.
Small percentages of subjects had 105 bacterial The results showed that S. persica root and
cells of S. mutans (1.4%) and S. sobrinus (5.4%). stem deionized distilled water extracts contained
At 105 bacterial cells threshold, the detection
Saudi Dental Journal, Vol. 16, No. 1, January - April 2004
34 COMPARATIVE ORAL HEALTH STATUS OF AN ADULT SUDANESE
Cl-, SO42-, SCN-, and NO3-. However, the showed no significant differences regarding the
concentrations of these four anionic components periodontal variables assessed in this Sudanese
differed considerably; stem extract contained population. However, in order to see if tooth type
more chloride (6.84%), sulphate (20.1%), and may have influenced the results, the data were re-
thiocyanate (0.38%) than did the root extracts analyzed using a bi-variate table, which is
(chloride 4.64%, sulphate 19.85%, thiocyanate somewhat similar to the analysis of co-variance.
Table 3. The correlations between the levels of autologous The results demonstrated that miswak users had
bacteria in intra-subject subgingival plaque and saliva samples. significantly lower numbers of sextants with
dental calculus in the posterior sextants than the
Bacterial species r-values P-values
modern toothbrush users had. This is in line with
Opportunistic bacteria Almas and Al-Lafi.25 Miswak extracts contains high
amounts of chloride25 and substantial amounts of
P. gingivalis 0.27 0.04* silica.26 Recently, it has been shown that the
A . 0.16 0.22
actinomycetemcomitans 0.25 0.06 commercially available dentifrice (Whitening
P. intermedia 0.23 0.08 Toothpaste, Colgate) which contains 10% silica is
P. melaninogenica 0.29 0.03* efficacious for control of supragingival calculus
F. nucleatum
T. denticola
0.10 0.46 formation.27 Furthermore, miswak is generally
C. rectus 0.05 0.71
-0.04 0.78 used for a longer period of time than is the modern
P. micros
S. sputigena 0.31 0.02* toothbrush, the cleaning is usually done for 5 to 10
S. intermedius 0.26 0.06 min each time,4 and the plant fibers remove
E. corrodens -0.12 0.38 plaque and simultaneously massage the gum.
V. parvula -0.12 0.39
C. sputigena -0.14 0.29 Thus, our finding that miswak users had lower
C. gingivalis -0.10 0.45 numbers of posterior sextants with dental calculus
S. mutans N.c. N.c. than toothbrush users had may be attributed to
S. sobrinus N.c. N.c.
L. acidophilus miswak`s chemical components and/or the
-0.02 0.89
differences in frequency and duration of brushing
Commensal bacteria
between the two methods.
S. anginosus It has been suggested that the level of
S. sanguis 0.23 0.09 supragingival calculus is a fairly good measure of
S. salivarius 0.30 0.02*
S. oralis N.c. N.c. the oral hygiene level and the frequency of
S. mitis 0.25 0.07 professional dental care in a population.28 Our
A. israelii 0.26 0.05* observation that there were no significant
L. buccalis -0.02 0.89
-0.03 0.81
differences in the pocket depths between habitual
miswak and toothbrush users is consistent with
N.c.= no correlation previous reports. Gazi et al.7 had demonstrated
*Statistically significant
that there were no significant differences in
0.28%). Nitrate concentration was 0.05% in both plaque scores and PPD measurements between
extracts. The % values express w/w % of habitual miswak and toothbrush users. Eid et al.11
reconstituted freeze-dried extract.
also indicated that there were no significant
Discussion
differences in plaque scores and attachment loss
between habitual miswak and toothbrush users.
Resources for oral health care are limited in
The lower caries experience in miswak users21
many developing countries and the need to
partially supports our working hypothesis of better
explore and test easily available and inexpensive
oral health in the miswak group. This is also in
traditional preventive measures is recognized and
agreement with previous epidemiological
supported by the WHO.17 This is also in line with a
studies.10,13,15,16 The lower caries experience in
recent consensus18 stating that "chewing sticks
the miswak users may possibly be explained by the
may have a role to play in the promotion of oral
results of a previous study,23 which demonstrated
hygiene" and that "evaluation of their
that miswak extract contained thiocyanate (SCN-).
effectiveness warrants further research". Our
hypothesis that habitual miswak users have better Tenovuo et al.29 showed in vitro that acid
oral health and lower levels of oral pathogens than production by S. mutans in human dental plaque
individuals who use modern toothbrush regularly was almost totally inhibited when supplementing
was not fully supported by the results of this study. saliva with SCN- and hydrogen peroxide. The
The overall effect of the two oral hygiene methods finding of a lower caries experience of miswak
Saudi Dental Journal, Vol. 16, No. 1, January - April 2004
DAROUT and SKAUG 35
users may also be referred to the cleansing effect A. naeslundii and S. oralis were found in
of miswak. For example, when the mouth cleaning significantly lower numbers in the miswak group.
procedure is completed, miswak is often left in the When we used 106 bacterial cells threshold, P.
mouth for some additional time. Left in the mouth, intermedia and S. mitis were significantly
it will stimulate salivation and thus promoting a higher in the toothbrush group than in the miswak
better cleansing and anti-cariogenic effect. group. The results comply with the levels of 25 of
Darout et al.36 is the first reported applying the these bacterial species in salivary samples from
checkerboard DNA-DNA hybridization method22 to the same individuals.
assess bacterial levels in saliva, in which they Darout et al.23,36 showed that species
showed that several bacterial species including including P. gingivalis, T. denticola, C. rectus,
periodontitis-associated ones were detectable. F. nucleatum and L. buccalis did not seem to be
This was in agreement with previous reports influenced by the type of oral hygiene used. This
which used different methods to detect various may suggest that the two oral hygiene methods
bacterial species including periodontitis- had similar effects on the levels of these species.
associated species in saliva.30,31 Our results also This is consistent with the findings of studies
showed that the method of oral hygiene had a which showed that supragingival plaque control
significant effect on the salivary levels of 19 out of had little or no effect on the levels of subgingival
the 25 bacterial species investigated. Ten of these species, at least in sites with deeper probing
species were present in significantly higher depths.34, 35
numbers, and 9 were found in significantly lower Darout et al.36 was the first to report the use of
numbers in the saliva of miswak users than of the checkerboard DNA-DNA hybridization method
toothbrush users. These microbial differences may to assess bacterial levels and their correlations in
be due to release of antimicrobial substances of autologous saliva and subgingival plaque
miswak or other factors. samples. Previously, Kononen et al.37 correlated
Our finding that four out of the six gram-negative anaerobes recovered by culture in
Streptococcus spp. examined were detectable in saliva and subgingival samples of a group of young
significantly lower levels in the miswak group can women. A relatively high percentage of the study
be explained by the results reported by Darout group had detectable levels of several of the
et al.23 Several of the anionic components examined opportunistic and commensal bacteria
detected in miswak extract are known to have in their paired saliva and subgingival plaque
antimicrobial effects. The higher levels of some samples. The results of Darout et al.36 showed
periodontal pathogens in the saliva of miswak that species including P. intermedia, T.
users21 may be due to a microbial shift from more denticola and P. gingivalis were more
streptococci to more periodontitis-associated frequently detected in saliva than in subgingival
species. If so, this would be in line with the plaque. This was consistent with a study that used
ecological plaque hypothesis.32 This may explain PCR to assess the frequencies of six oral bacteria in
the weak effect of miswak use on some oral paired samples of unstimulated saliva and
anaerobic (P. gingivalis, E. corrodens, S. subgingival plaque of adult subjects in the USA.30
sputigena P. micros, T. denticola, C. rectus) The latter study showed that P. gingivalis, P.
and facultative (C. sputigena, C. gingivalis, intermedia, P. nigrescens, and T. denticola
A. actinomy-cetemcomitans) species. were detected more frequently in saliva than in
This is the first report on detection frequencies periodontal pockets. The cariogenic bacteria S.
and levels of subgingival bacteria and their mutans and L. acidophilus were demonstrated
associations in adult Sudanese habitual miswak at detectable (105 bacterial cells) levels but not at
users and toothbrush users.33 The results showed high (106 bacterial cells) levels.21 Usually, high S.
that the type of oral hygiene practice had a
mutans and L. acidophilus counts indicate
significant effect on the subgingival plaque levels
active caries or a high caries risk. This may not
of 11 out of the 28 bacterial species investigated.
always be valid for Sudanese subjects who have
Using 10 5 bacterial cells threshold, S. been shown to have high counts of mutans
intermedius, A. actinomycetemcomitans, V. streptococci even in populations with extremely
parvula, A. israelii and C. gingivalis were low prevalence of dental caries.38
present in significantly higher numbers in The results of Darout et al.36 showed that S.
subgingival plaque of the miswak than of the mutans and L. acidophilus occurred
toothbrush group. S. sputigena, S. salivarius, significantly more frequently in saliva than in
Saudi Dental Journal, Vol. 16, No. 1, January - April 2004
36 COMPARATIVE ORAL HEALTH STATUS OF AN ADULT SUDANESE
subgingival plaque. This was in agreement with bound forms and for which we postulate their
the previous studies.39,40 The lower detection possible mode of action against oral bacteria. If
frequencies of mutans streptococci reported in a our working hypothesis on the contribution of
study36 may be attributed to the difference in the endogenous SCN- to the antimicrobial effect of
threshold levels of detection frequencies used in miswak were correct, this implies that miswak,
the two studies as well as to ethnic differences. when in the mouth, may represent an external
Darout et al.36 showed significant positive source of leachable SCN-. However, it remains to
correlations between levels of P. gingivalis, F. be shown in vivo that saliva extracts SCN- from
nucleatum, S. sputigena, S. sanguis and S. miswak in adequate amounts and that such
mitis. Umeda et al.30 used kappa statistics to additional SCN- really results in a more efficient
estimate the agreement between bacterial levels peroxidase-thiocyanate and hydrogen peroxide
in paired samples of saliva and pooled subgingival antimicrobial system.
plaque. They found a fair agreement between
saliva and plaque samples for P. gingivalis, P. Conclusions
intermedia and T. denticola, and a poor
agreement for A. actinomycetemcomitans, B. 1. The periodontal status of miswak users in this
forsythus and P. nigrescens. Except for P. Sudanese population was similar to that of the
gingivalis, our data did not support their toothbrush users, suggesting that the efficacy
findings. of miswak use for oral hygiene was comparable
Miswak aqueous extracts contain potentially to that of the modern toothbrush.
antimicrobial anionic components including Cl-, 2. The miswak users had significantly less
SO42-, NO3- and SCN-. The antibacterial and weak calculus in their posterial sextants than had the
anti-inflammatory effects of S. persica root and toothbrush users which may be due to anti-
twig extracts have been attributed to their content calculus effect of miswak.
of beta-sitosterol, SO42- compounds and Cl-.43 In 3. The findings suggested that miswak may also
addition, Cl-, I- and SCN- (pseudohalides) are have a selective inhibitory effect on the level of
certain bacteria in saliva, particularly several
substrates for salivary peroxidase and/or the
oral Streptococcus species.
myeloperoxidase hydrogen peroxide antimicrobial
4. The results indicated that the type of oral
system. The lower levels of P. intermedia and F. hygiene method used had a significant effect
nucleatum in the miswak users24 may be on the levels of 11 out of the 28 species
attributed to its Cl- and SCN- content. investigated and that the effect was also
NO3- in S. persica root and stem water extracts dependent on type of bacteria and probing
may be released from the residual nitrate ions pocket depth.
taken up by the S. persica plant or from the 5. This study indicated that the levels of P.
oxidation of ammonia and other nitrogen gingivalis, F. nucleatum, S. sputigena, S.
compounds. Recently, Allaker et al.44 reported sanguis and S. mitis are correlated
that acidified nitrite exhibited growth-inhibitory significantly in autologous saliva and
effect on F. nucleatum, E. corrodens and P. subgingival plaque.
gingivalis. Furthermore, SCN- leaching out from 6. Miswak users showed lower caries experience
miswak while in the oral cavity may lead to an and lower levels of some oral pathogens (P.
elevated level of salivary SCN-. This in turn may intermedia, F. nucleatum, S. sputigena,
enhance the efficacy of the salivary peroxidase- E. corrodens, L. acidophilus, S. sanguis,
thiocyanate and hydrogen peroxide system, a S. salivarius, S. oralis, and S. mitis). This is
known innate antimicrobial component of human in support of our hypothesis of better oral
saliva. There are data showing that the most health and lower levels of oral pathogens in
susceptible bacteria to this antimicrobial system miswak users than modern toothbrush users.
are the oral streptococci, whereas other anaerobic 7. Demonstration of high levels of thiocyanate in
oral bacteria (C. sputigena, C. gingivalis, P. aqueous miswak extracts complies with our
gingivalis, E. corrodens, S. sputigena P. hypothesis that antimicrobial effect of miswak
micros, T. denticola, and C. rectus) were less may be due to its thiocyanate content.
affected.45
Our study showed for the first time that miswak Acknowledgements
aqueous extracts contain potential anionic
components including SCN- in both free and We would like to thank Professor Jasim
Saudi Dental Journal, Vol. 16, No. 1, January - April 2004
DAROUT and SKAUG 37
Albandar and Professor Alfred Christy for their 17. World Health Organization. Prevention of diseases.
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Research Center, Khartoum, Sudan for facilitating sticks or toothbrushes. Acta Odontol Scand
the clinical examinations. 2000;58:25-30.
20. World Health Organization. Oral health surveys.
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