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Associations between Salivary Levels of

Streptococcus mutans, Streptococcus
sobrinus, Lactobacilli and caries experience
in Kenyan Adolescents

ARTICLE in JOURNAL OF DENTAL RESEARCH · SEPTEMBER 1989

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Associations between Salivary Levels of Streptococcus mutans, Streptococcus sobrinus,

Lactobacilli, and Caries Experience in Kenyan Adolescents
D. Beighton, F. Manji, V. Baelum, O. Fejerskov, N.W. Johnson and J.M.A. Wilton
J DENT RES 1989 68: 1242
DOI: 10.1177/00220345890680080601

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Associations between Salivary Levels
of Streptococcus mutans, Streptococcus sobrinus, Lactobacilli,
and Caries Experience in Kenyan Adolescents
D. BEIGHTON', F. MANJI2, V. BAELUM3, 0. FEJERSKOV3, N.W. JOHNSON' 4, and J.M.A. WILTON4
'Dental Research Unit, Royal College of Surgeons of England, Downe, Kent, United Kingdom BR6 7JJ; 2Oral Health Research Unit, KEMRI,
Nairobi, Kenya; 3Royal Dental School, Aarhus, Denmark; and 'MRC, Dental Research Unit, Periodontal Diseases Programme, London Hospital
Medical College, London, England

Salivary levels of mutans streptococci (S. mutans and S. sobrinus) and lactobacilli, we conducted a study in an adolescent pop-
and lactobacilli were determined in a random sample of rural Kenyans ulation in a rural area of Kenya, in which access to dental care
between 15 and 19 years of age (n = 149). It is possible for the is minimal, and in which there are on-going longitudinal stud-
natural history of dental caries in this population to be studied since ies on dental caries and periodontal diseases (the Primary Oral
it is characterized by a limited access to conventional dental treat- Health Care Project-Kenya).
ment. Using a short set of biochemical tests, we identified from seven
to ten presumptive mutans streptococcus colonies -cultured from the
saliva of each individual-to differentiate between S. mutans and S.
sobrinus. No colonies resembling S. rattus (S. mutans serotype b) Materials and methods.
were isolated. Lactobacilli were identified as Gram-positive, catalase-
negative rods. The mean DJ4MFS and D3-4MFS were 7.03 + 6.43 Study population. -The study was conducted in a rural area
and 1.46 + 3.44, respectively. The mean mutans streptococcus and of Kenya, in the Northern Division of the Machakos District.
lactobacillus levels were 8. 7 x 104 and 6. 7 x 104, respectively. The The sample included 183 persons (15 to 19 years of age),
salivary mutans streptococcus and lactobacillus levels were signifi- selected on the basis of a complex random-cluster sampling
cantly correlated (p<0.01). Of the subjects, 64% harbored only S. method that has been previously described (Manji et al., 1988a).
mutans, 4% only S. sobrinus, 30% both species, and 2% neither. In February, 1986, saliva samples were obtained from 149
Lactobacilli were ubiquitous. The caries experience of the group was
subjects from the total sample.
significantly (p <0. 001) correlated with both the total salivary level Dental caries examinations. -Three examiners (FM, VB,
of mutans streptococci and the salivary S. mutans levels, but not with OF) performed examinations in a shaded area, with use of
the salivary S. sobrinus level.
mouth mirrors and probes in natural daylight. All tooth sur-
J Dent Res 68(8):1242-1246, August, 1989 faces were examined and classified-according to the clinical
features of each surface-as sound, or as having lesions in-
volving only the enamel (D, and D2), lesions involving the
Introduction. dentin (D3), and those which either definitely or probably in-
volved the pulpal tissues (D4), as described previously (Manji
Streptococcus mutans and Streptococcus sobrinus, the mutans et al., 1988b).
streptococci most frequently isolated from human dental plaque, Collection and processing of saliva. -From each subject, a
are believed to be the major etiological agents of tooth decay 2-to-5-mL sample of unstimulated whole saliva was collected
(Hamada and Slade, 1980; Emilson and Krasse, 1985; Loesche, into a sterile bottle, stored in a cool place, and processed within
1986). Such evidence comes from both human cross-sectional 60 min. Each saliva sample was diluted 1:100 in sterile phos-
(Clarke, 1924) and longitudinal studies (Kristoffersson et al., phate-buffered saline. Duplicate 0.1-mL volumes of the neat
1985; Loesche et al., 1984), and from studies in animals (Fitz- and the diluted saliva were plated onto mitis-salivarius agar
gerald, 1968). Since the salivary levels of mutans streptococci (Oxoid, Ltd., Hampshire, UK), modified as described by Gold
are directly related to the number of tooth sites colonized (To-
et al. (1973), and onto Lactobacillus Selective Agar (Oxoid)
gelius et al., 1984) and to their proportion in dental plaque (Rogosa et al., 1951). The detection level for mutans strep-
(van Houte and Green, 1974), saliva has frequently been used tococci and lactobacilli was therefore five colony-forming units
to monitor the oral load of these micro-organisms (Matee et (cfu) per milliliter of saliva. All plates were incubated in can-
al., 1985; Beighton et al., 1987). dle jars for three days at 37TC.
In populations with a relatively high caries experience, pos- A new medium, TYCSB, for the isolation of mutans strep-
itive associations between caries experience and salivary levels tococci has been described (van Palenstein-Helderman et al.,
of mutans streptococci and lactobacilli (Crossner, 1981) have 1983). Since it is claimed to be superior to MSB for the iso-
frequently been reported (Emilson and Krasse, 1985). How- lation of mutans streptococci, we compared the recovery of
ever, relatively high levels of these micro-organisms have been
found in populations exhibiting a very low caries experience mutans streptococci from Kenyan saliva samples on these two
(Carlsson et al., 1985; Matee et al., 1985; Carlsson et al., media.
1987). Although the rate of caries progression in such popu- Identification and enumeration of mutans streptococci and
lations is apparently slow, it has recently been shown that, lactobacilli.-We counted the number of mutans streptococ-
with increasing age, such populations do experience disease to cus-like colonies growing on the MSB agar. Up to ten colonies
an extent which hitherto has not been appreciated (Manji et were picked from the medium and stored individually frozen
al., 1988a,b). in sterile tubes in 1 -mL volumes of Todd-Hewitt Broth (Oxoid)
To increase our knowledge of the associations between and plus 16% (V/V) glycerol, and flown back to England in liquid
among dental caries, salivary levels of mutans streptococci, nitrogen for subsequent identification. In all, 1100 colonies
presumptively identified as mutans streptococci were subcul-
tured for identification. The identity of the presumptive mutans
Received for publication August 4, 1988 streptococcus isolates was established by means of a short set
Accepted for publication April 26, 1989 of biochemical tests (Beighton, 1985) which, when necessary,
1242
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Vol. 68 No. 8 CARIES EXPERIENCE IN RURAL KENYANS 1243

were supplemented by serological (Bratthall, 1970; Perch et TABLE 2

al., 1974; Beighton et al., 1981) and electrophoretic methods CORRELATION COEFFICIENTS BETWEEN DENTAL CARIES
(Beighton et al., 1984). The lactobacilli were identified as EXPERIENCE AND SALIVARY LEVELS OF MUTANS
regular or curved Gram-positive, catalase-negative rods. No STREPTOCOCCI, S. mutans, S. sobrinus, AND LACTOBACILLI
further tests were performed to speciate these organisms. For Mutans
the comparison of MSB and TYCSB, only the total number streptococci S. mutans S. sobrinus Lactobacilli
of mutans streptococcus-like colonies growing on each me- DJ-4MFS 0.427** 0.433** 0.079 0.238*
dium was determined; no attempt was made to confirm the D3-4MFS 0.312** 0.339** -0.029 0.137
identity of these organisms. D3 4S 0.380** 0.384** 0-015 0.179
Statistical analysis.-The D component of the DMFS index *P<0.02; **P<0.001.
is presented in two forms: D1-4 includes all forms of caries,
while D3o4 excludes surfaces exhibiting merely enamel lesions
in which there was judged to be no dentinal or pulpal involve-
ment. The distribution of the salivary levels of S. mutans in A
the sample of individuals was divided into three parts, in such
a way that approximately the same number of individuals oc-
curred in each group. The lowest third of the distribution has
been designated the "low" group, the middle third the "me-
dium" group, and the upper third the "high" group. The dis-
tribution of the lactobacilli among the population was treated
in a similar manner.

Results.
Isolation of mutans streptococci. -S. mutans was recovered NUMBEROF SIJRFACES WITH D,, LESIONS. LOGILACTOBACILLI PER ML).
from 94% of the subjects, S. sobrinus was isolated-in the
absence of S. mutans-from four percent of the subjects, and
both organisms were isolated together from 30% of individ-
uals. Only two percent of individuals harbored undetectable
levels of either organism. No organisms with the biochemical
properties of S. rattus (S. mutans serotype b) were isolated
from among the 1100 isolates from the MSB.
The recovery of mutans streptococci from saliva samples
was similar on each of the two media tested: 1.20 (+ 2.3) x
105 and 1.18 (+ 2.24) x 105 on MSB and TYCSB, respec-
tively (p>0.50). The recovery of mutans streptococci on each
medium was significantly correlated (r = 0.748; p<0.001).
The salivary concentrations of mutans streptococci and lac- D0, LESIONS
NUMBER OF SURFACES WITH IOG(LACTOBACILLI PER ML)

tobacilli are shown in Table 1. The salivary concentrations of Fig. I -(A) Cumulative frequency distribution of the percentage of
S. mutans and S. sobrinus were significantly, but not strongly, individuals by the number of D,4 caries lesions, categorized according to
correlated with the salivary lactobacillus concentration: r = their salivary S. mutans level (A = low, * -- medium, * = high). (B)
0.191 (p<0.02) and r = 0.332 (p<0.001), respectively. Cumulative frequency distribution of the percentage of individuals by the
Dental caries experience.-The mean D, 4MFS score was log (S. mutans per mL of saliva), categorized according to the number of
7.03 ± 6.43, with 89% having one or more surfaces affected. D, caries lesions (A = low, * = medium, * = high). (C) Cumulative
The mean D3 4MFS score was 1.46 + 3.44, with 66.4% of frequency distribution of the percentage of individuals by the number of
subjects having a score of zero. No individual had any fillings, D,-4 caries lesions, categorized according to the salivary S. mutans level
(A = low, v = medium, 0 = high). (D) Cumulative frequency distri-
and only eight subjects had any teeth missing because of caries bution of the percentage of individuals by the log (S. mutans per mL of
(MS = 0.44 ± 2.09). The mean D3-4S was 1.02 + 2.51. saliva), categorized according to the number of D3.4 caries lesions (A =
Salivary mutans streptococcal counts and dental caries ex- low, * = medium, 0 = high). [Note: "low", "medium", and "high"
perience.-Taken together, mutans streptococci were signifi- criteria are defined in "Materials and methods".]
cantly and positively associated with caries experience (where
enamel lesions were either included or excluded, or when the
missing component was excluded) (Table 2). On their own, The distribution of D1 among those harboring low and me-
however, salivary levels of S. sobrinus were not associated dium levels of S. mutans was similar (Fig. 1A). In these in-
with caries experience, the strength of the association of mu- dividuals and in the high-S. mutans group, approximately 90%
tans streptococci being caused entirely by S. mutans. of individuals had at least one lesion (D,14), and in all three
groups, the distribution of caries was markedly skewed. In the
TABLE 1 high-S. mutans group, a greater proportion of individuals tended
SUMMARY OF THE SALIVARY CONCENTRATIONS OF MUTANS to have more surfaces affected than in either of the other groups.
STREPTOCOCCI, S. mutans, S. sobrinus, AND LACTOBACILLI The two individuals who had more than 25 surfaces affected
(EXPRESSED AS COLONY-FORMING UNITS per mL OF SALIVA harbored high S. mutans levels. Excluding these "outliers"
X 10 4)
from the calculation of the correlation coefficient resulted in a
Mean SD Median Range value of r - 0.348 (p<0.001) (cf. Table 2). When the indi-
Mutans streptococci 8.68 19.7 1.55 <5-100 viduals were grouped according to the levels of caries (Fig.
S. inutans 7.72 18.5 1.35 <5-100 1B), it was apparent that the distribution of S. mutans in those
S. sobrinuis 0.96 5.0 < 0.05 <5- 56.6 with no caries, those with from one to five lesions (medium-
Lactobacilli 6.70 13.2 0.46 <5- 77
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personal use andusesthose
only. No other with six or more lesions (high-caries
without permission.
1244 BEIGHTON et al. J Dent Res August 1989

group) was similar, and no clear systematic differences be- dividuals (67%) with either medium or high lactobacilli counts
tween these groups could be identified. The distribution of had five or more lesions, whereas only 38% of those in the
D3-4 caries in the medium- and low-S. mutans groups was low group were affected. In general, those with high levels of
remarkably similar, and it was apparent that the strength of lactobacilli tended to have more surfaces affected by caries
the association between S. mutans and caries experience was than those with lower levels of the micro-organism, and con-
primarily a result of the greater proportion of individuals in versely, those with more caries tended to harbor greater levels
the high-S. mutans group also being in the high-caries group of lactobacilli than those with few or no lesions (Fig. 2B).
(Fig. iC). Excluding the two "outliers", the recalculated cor- When enamel lesions were excluded (Fig. 2C), there were
relation coefficient was not significantly different from zero (r almost no differences in the distribution of caries among those
= 0.099, p < 0.20). Nevertheless, the proportion of individuals with low or medium levels of lactobacilli, whereas those with
with one or more lesions (D3 -) increased from 27% in the low high lactobacilli counts tended to have more caries. The dis-
group, to 36% in the medium group, and to 49% in the high tribution of lactobacilli counts in those with either no frank
group. When the groups were defined according to their caries cavitation (D, -) or with one or two such lesions was similar,
experience (Fig. ID), the distribution of S. mutans in each whereas those with three or more lesions tended to harbor more
group was similar, except that a greater proportion of individ- lactobacilli (Fig. 2D).
uals with three or more lesions harbored between 10- and 105
S. mutans cfu/mL saliva, unlike either of the other groups.
However, approximately the same proportion of individuals in Discussion.
each group had more than 105 S. mutans cfu/mL saliva. The results of this study are of particular interest because
Salivary lactobacilli and dental caries experience.-Sali- they originate from a rural African population in which the
vary levels of lactobacilli were only significantly associated prevalence of dental caries was over 90%, with approximately
with caries where enamel lesions were included; otherwise, 40% of the individuals exhibiting frank cavitation. Previous
the correlation coefficients were not significantly different from studies dealing with populations having a relatively high caries
zero (Table 2). experience have been conducted in industrialized countries,
The distribution of D,4 lesions at each lactobacilli level is and in most of these studies, as in this one, a positive asso-
shown in Fig. 2A. Approximately the same proportion of in- ciation between S. mutans and dental caries experience has
been found (Hamada and Slade, 1980; Emilson and Krasse,
1985; Loesche, 1986). The results of the present study cannot,
however, be directly compared with those from such studies,
for a number of important reasons. In populations in indus-
A trialized countries, there is often extensive interference with
the disease process, either through the use of various prophy-
lactic regimens, or by the provision of treatment. The insertion
of fillings into cavities, for example, may result in the elimi-
nation of a source of micro-organisms to the saliva, or the
margins of the restorations may subsequently harbor microbial
colonies (Schaeken et al., 1984). In either case, the true re-
lationship between salivary micro-organisms and caries expe-
rience may be masked. Such is not, however, the case in the
population studied here. This population has minimal access
to formal dental care (Manji et al., 1988b), and this is reflected
SURFACES WITH
D,-4 LESIONS. LOG IS.MUTANS PER ML).
in the total absence of fillings and the very small number of
teeth extracted from these adolescents because of caries. Thus,
c few individuals, if any, were likely to have experienced pro-
phylactic interventions-such as the application of topical fluo-
rides or chlorhexidine-and few had received treatment.
Moreover, this population is characterized by rather poor oral
hygiene (Baelum et al., 1989) and, at the same time, by a
slow rate of progression of caries with age (Manji et al., 1988).
The findings here may be interpreted, therefore, as indicative
of the relationships between salivary micro-organisms and den-
tal caries experience in its undisturbed state, but do not neces-
sarily imply a causative role for these bacteria in the etiology
of caries in this population.
NUMBER SURFACES
D,,
WITH LESIONS, LOG
(SMUTANS
PER ML)
Although the recovery of mutans streptococci with use of
Fig. 2-(A) Cumulative frequency distribution of the percentage of MSB has been reported to be inferior to TYCSB (van Palen-
individuals by the number of D, caries lesions, categorized according to stein-Helderman, 1983; Matee et al., 1985), this was not the
the salivary lactobacillus level (A = low, * = medium, * = high). (B) case either in this or in a previous study (Beighton, 1986). The
Cumulative frequency distribution of the percentage of individuals by log recovery of these bacteria on both media was similar, and we
(lactobacilli per mL of saliva), categorized according to the number of can offer no explanation as to why others have been unable to
D, caries lesions (A = low, * = medium, - high). (C) Cumulative
0
obtain comparable results from both types of media. Exami-
frequency distribution of the percentage of individuals by the number of nation of both the distribution of caries according to the levels
D, caries lesions, categorized according to the salivary lactobacillus level
of micro-organism, and the distribution of the salivary levels
(A = low, * = medium, * = high). (D) Cumulative frequency distri-
bution of the percentage of individuals by log (lactobacilli per mL of of micro-organism according to caries experience, indicated
saliva), categorized according to the number of D3 caries lesions (A = that the nature of the relationship between these variables was
low, * medium,
= 0
high). [Note: "low", "medium", and "high"
= more complex than was at first appreciated. Furthermore, it
criteria are defined in "Materials and methods".] was apparent that for both S. mutans and lactobacilli, the re-
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Vol. 68 No. 8 CARIES EXPERIENCE IN RURAL KENYANS 1245

lationship with caries experience was non-linear. Expression Further studies are presently being undertaken to study how
of the relationship in terms of the correlation coefficients was diet influences the propensity of individuals to be colonized
thus an inadequate or even misleading indicator of the nature by mutans streptococci and lactobacilli and to develop dental
and strength of the relationship between the variables. The caries.
strength of the correlation coefficients was, moreover, influ-
enced by the inclusion of data from a few outliers.
Previous studies (Kloch and Krasse, 1977; Bader et al., Acknowledgments.
1986) have suggested that relating combinations of micro-or- We acknowledge the assistance of the following: The Min-
ganisms (rather than considering each individually) to caries istry of Health (Kenya); Colgate-Palmolive (East Africa) Ltd.;
experience may be a more powerful (and perhaps more mean- East African Industries Ltd.; The Kenyan Army; James Simwa;
ingful) method of identifying high-risk individuals. However, Dr. Peter Wanzala; Joan Sawe; and the many others who made
more recent studies have suggested that it is the non- or low- this project possible. This paper constitutes a report of the
risk individuals who are better identified when both organisms Primary Oral Health Care Project-Kenya, a joint project of the
are considered together (Stecksen-Blicks, 1985; Kingman et
Kenya Medical Research Institute (KEMRI) and the Royal
al., 1988). Salivary levels of S. sobrinus were not associated Dental College, Aarhus, Denmark, supported by the Danish
with caries experience, and in combination with S. mutans, International Development Agency (DANIDA). Our thanks to
resulted in weaker associations than when the latter were con- Dr. P. Waiyaki [Director, Center for Microbiological Research
sidered alone. The value of determining salivary levels of in- (KEMRI)] and his staff for assisting with laboratory facilities
dividual mutans streptococcal species to examine their in Kenya, and to the Director of KEMRI for permission to
associations, individually, with caries experience, must there- publish these findings. The British participation was assisted
fore be carefully considered. by a grant from the Oral Health Unit of the World Health
The high frequency of isolation of mutans streptococci we Organization.
found was similar to that found in populations from both in-
dustrialized and non-industrialized countries (Loesche, 1986;
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