International Journal of Probiotics and Prebiotics Vol. 5, No. 4, pp.

221-228, 2010
ISSN 1555-1431 print, Copyright © 2010 by New Century Health Publishers, LLC
www.newcenturyhealthpublishers.com
All rights of reproduction in any form reserved

EFFECT OF CONSUMPTION OF LACTOBACILLUS RHAMNOSUS GG AND CALCIUM, IN

CARROT-PINEAPPLE JUICE ON DENTAL CARIES RISK IN CHILDREN
1
S. Pohjavuori, 1A.J. Ahola, 2H. Yli-Knuuttila, 3L. Piirainen, 4T. Poussa, 2,5
J.H. Meurman and 1,3
R. Korpela

1
Valio Ltd, R&D, FIN-00039 Valio, Helsinki, Finland; 2Institute of Dentistry, University of Helsinki, FIN-00014
University of Helsinki, Helsinki, Finland; 3Institute of Biomedicine, Pharmacology, University of Helsinki, FIN-00014
University of Helsinki, Helsinki, Finland; 4Stat-Consulting, FIN-33230 Tampere, Finland; 5Department of Oral and Dental
Diseases, Helsinki University Central Hospital, FIN-00029 HUCH, Helsinki, Finland

[Received Month Date, 2010; Accepted May 12, 2010]

ABSTRACT: Consumption of milk containing Lactobacillus
rhamnosus GG (LGG) has been shown to reduce caries risk in
children. We examined whether long-term consumption of
juice containing LGG and calcium lactate gluconate (CaLG)
affects the caries risk in a double-blind, placebo-controlled
setting. The study comprised 530 healthy children, aged 3-6
years. They consumed 5 days a week for 7 months either carrot-
pineapple juice containing LGG (Valio Ltd, Finland; 5x106
cfu/ml) and CaLG or control juice. The children’s oral health
status was assessed at the baseline and in the end of the study,
and salivary Streptococcus mutans counts four times during
the study. The caries risk and the need for dental care increased,
and high S. mutans counts decreased in both study groups. At
the end of the study, the caries risk was not lower (baseline-
adjusted OR=0.71, 95% CI 0.38-1.32, p=0.281), but the
need of dental care was smaller (baseline-adjusted OR=0.58;
95% CI 0.34-1.00; p=0.050), and there were more children
who had all the six sextants healthy (baseline-adjusted
OR=1.69, 95% CI 0.99-2.89; p=0.056) in the LGG-CaLG
juice group compared to the control juice group. To conclude,
supplementation of juice with LGG and CaLG might be
beneficial for dental health in children.
KEY WORDS: Calcium, Caries risk, Children, Lactobacillus GG
Corresponding Author: Prof. Riitta Korpela, Institute of
Biomedicine, Pharmacology, PO Box 63, FIN-00014
University of Helsinki, Finland; Fax: +358919125364;
E-mail: riitta.korpela@helsinki.fi
INTRODUCTION
Dental caries is a chronic infectious disease and common in
childhood. Although dental health of children in Finland and
other Western countries has improved markedly during the
past decades (Rytömaa et al., 1980; Seppä et al., 2002), the
children with caries are more severely affected than before
(Vehkalahti et al., 1997; Mattila et al., 2000). Use of probiotic
bacteria to reduce caries has been under increased interest in
recent years. Lactobacillus rhamnosus GG (LGG) is one of the
most studied probiotic bacteria and shown to have an inhibitory
activity against bacterial species including Steptococcus spp. (Silva
et al., 1987; Meurman et al., 1995). In laboratory studies LGG
has been shown to reduce or not to ferment sucrose and lactose
(Saxelin, 1997; Haukioja et al., 2008). In addition, LGG
reduces the adhesion of Streptococcus mutans to saliva-coated
hydroxyapatite beads (Wei et al., 1992; 2002), possibly by its
coaggregation in the dental biofilm (Twetman et al., 2009),
which confirms the anticariogenic effect of LGG.
We have previously shown that milk containing LGG reduces
caries risk in children (Näse et al., 2001). Furthermore, we
found that a short-term consumption of cheese containing LGG
and Lactobacillus rhamnosus LC 705 showed a trend towards
reduction of the risk of the highest level of S. mutans bacteria
(Ahola et al., 2002). Also other probiotic bacteria have shown
similar positive effects on dental caries (Caglar et al., 2005;
2006; 2008). However, cheese and milk themselves are known
to have positive effects on dental caries (Harper et al., 1986;
Krobicka et al., 1987; Vacca-Smith and Bowen, 2000;
Drummond et al., 2002). In the present study we assessed
whether the anticariogenic effects of probiotics could even be
seen when using sugar-containing juice, which itself has
cariogenic potential, as the vehicle of probiotic administration.
Excessive consumption of acid-containing drinks such as
soft drinks and juices is associated with an increased risk of
dental erosion (Jensdottir et al., 2004; Moazzez et al., 2000).
Although water and milk are considered better for dental health,
some children occasionally prefer juices. Therefore, formulating
sugar-containing acidic drinks with reduced cariogenic and
222 Probiotics and caries risk in children
erosive potential is a likely approach to support dental health.
Enrichment of acidic drinks with minerals such as calcium and
phosphorus to reduce their erosive potential has been under
increased interest in recent years (Attin et al., 2005; Jensdottir
et al., 2005; West et al., 2004). To our knowledge, formulation
of an acidic drink with both probiotic bacteria and minerals
has not been studied earlier. Therefore, the aim of this double-
blinded, placebo-controlled intervention study was to examine
whether long-term consumption of a juice enriched with LGG
and calcium lactate gluconate (CaLG) affects the development
of caries and caries risk in day care children.
MATERIALS AND METHODS
Subjects
Thirty day care centres, in similar socio-economic areas in
the cities of Espoo and Vantaa, Finland, participated in this
randomized, double-blind, placebo-controlled multi-centre
study. Altogether 530 healthy children aged 3-6 years
volunteered to take part. The parents gave their written
informed consent prior the study on behalf of their children.
The study was ethically conducted in accordance with the
Declaration of Helsinki and the Ethics Committee of the
Helsinki City Health Department approved the study
protocol.
Intervention
The intervention lasted seven months from September 2002
to May 2003. The children were randomised to the LGG-
CaLG juice group or to the control juice group according to a
computer generated randomly permuted block-method. In
randomisation the block size of four was used, and it was
stratified according to age (3-4 years or 5-6 years) and the S.
mutans count (0-1 or 2-3, where 0: no growth, 1: =103 CFU/
ml, 2: 104 CFU/ml, 3: =105 CFU/ml) from samples taken at
inclusion.
During the intervention the children drank either carrot-
pineapple juice (Gefilus®, Valio Ltd, Helsinki, Finland) enriched
with LGG (5 x 106 CFU/ml of strain LGG, ATCC 53103)
and calcium (CaLG 120 mg/100g), or control carrot-pineapple
juice without LGG and calcium. The juices were delivered to
the day care centres in cartons labelled as “M” and “R” juices.
The study personnel (unless T. P.), the day care personnel, the
study children and their families did not know which one was
the active product until the end of the study.
The day care personnel served the juices with afternoon
snacks five days a week and recorded the daily amount of juices
consumed by each child. The intended daily dose of study
juice was 200 ml. The use of other products containing
probiotic bacteria was prohibited for four weeks prior the
intervention and throughout the study.
Examination of oral health
Information about the children’s dental health and dietary
habits were collected using a structured questionnaire filled in
by the parents. The study coordinator checked the completed
questionnaires, and supplied missing data with help of the
parents. During the study, the parents recorded daily in a
symptom diary any illnesses, dental appointments, and
medications of the children.
The children’s oral health was clinically examined at baseline
and in the end of the study by an experienced dentist (H. Y.-K.)
according to the World Health Organisation criteria from 1987.
The use of fluoride varnish was forbidden during the
intervention, but all necessary dental treatment and fluoride
toothpaste were allowed.
The S. mutans counts were evaluated four times during the
study: at inclusion, at baseline (0 months), in the middle (3.5
months), and in the end of the study (7 months). The samples
were taken in the day care centres from all the children and always
at the same time, i.e. one hour after breakfast or lunch. The research
assistants took samples from the tongue surface by using the
Dentocult SM Strip mutans® slides (Orion Diagnostica, Espoo,
Finland). The S. mutans counts were measured using the following
categories: 0: no growth, 1: =103 CFU/ml, 2: 104 CFU/ml, 3:
=105 CFU/ml.
The caries risk was evaluated at baseline and in the end of the
study by using both clinical and microbiological data (S. mutans
counts). The sums of decayed, missing and filled teeth in the
primary (dmft) and permanent (DMFT) teeth were analysed.
The caries risk was considered “low” if no caries was detected and
the S. mutans count was <105 CFU/ml; “moderate” if the child
had either a dmft/DMFT or initial caries score >0 or the S. mutans
count >105 CFU/ml; and “high” if the child had a dmft/DMFT
or initial caries score >0 and S. mutans count >105 CFU/ml.
Lactobacillus rhamnosus GG measurements
Salivary LGG was analyzed at baseline and in the end of the
study in a subgroup of study children (total n=362, LGG-CaLG
juice group n=179, control juice group n=183). Saliva samples
were cultured on agar and LGG was identified by colony
morphology, lactose fermentation test and characteristic cell
shapes (Yli-Knuutila et al., 2006).
Statistical methods
Calculation of the sample size was based on the assumption
that the use of LGG-CaLG juice results in 44% reduction in
dental caries risk. As a reference data we used our previous study
which showed an odds ratio of 0.56 for LGG in preventing
caries (Näse et al., 2001). We assumed that after the intervention
period the proportion of moderate or high caries risk would be
27% in the LGG-CaLG juice group vs. 40% in the control juice
group. It was further estimated that with a two group continuity
corrected, Chi-square test with a 0.050 two-sided significance
level would show a 80% power in the detection of the difference
between the LGG-CaLG juice group and control juice group
(OR=0.56) when the sample size in each is 228. To take the
possible dropouts into consideration, 265 subjects per group
were randomized.
The primary outcome measure was the caries risk measured in the
 Probiotics and caries risk in children 223

end of the study. In the final analyses the classes TABLE 1. Characteristics of the study children, randomized to consume either juice enriched with
“moderate” and “high” were combined. Logis- Lactobacillus GG and calcium lactate gluconate (LGG-CaLG juice group, n=235) or control juice
tic regression analyses were performed to com- (control juice group, n=238). Figures are percentages or means (range).
pare the LGG-CaLG juice group to the con-
trol juice group with respect to moderate/high LGG-CaLG CONTROL
caries risk or other binary response variables mea- JUICE GROUP JUICE GROUP
sured in the end of the study. The correspond- Boys/girls, % 51/49 53/47
ing baseline status was included as a categorical Age, years 5.5 (3.4-6.9) 5.6 (3.3-6.9)
covariate. As the baseline-adjusted analysis re-
Oral health habits
quires complete data, the main analyses include
the subjects who participated in all study Brushing the teeth, % <1/day 3 4
phases (baseline, middle and end). The results 1/day 63 64
are given as odds ratios (OR) with 95% confi- 2/day 33 32
dence intervals (CI). Parental help with brushing, % 83 80
The baseline characteristics were analyzed
Age when tooth brushing started, months 11 (0-48) 11 (0-48)
using t-test for independent samples or Chi-
square test, when appropriate. The analyses Use of fluoride toothpaste, % 98 97
were performed using SPSS (Version 17.0, the Use of other fluoride products, % 18 14
SPSS Inc., Chicago, IL, USA). Use of xylitol-products, % 95 98
Using dummy, % 0 0
RESULTS
Age when dummy eating stopped, months 17 (0-48) 17 (0-48)
Baseline characteristics and compliance Using baby bottle, % 1.3 0.4
Of the 530 study children, 265 were Age when baby bottle use stopped, months 18 (0-48) 18 (0-72)
allocated to the LGG-CaLG juice group and Dietary habits
265 children to the control juice group (Figure Drink when thirsty, % Water 42 47
1). Thirty-seven children (14%) in the LGG-
Milk 31 26
CaLG juice group and 43 children (16%) in
the control juice group dropped out. Juice 27 25
The study groups were comparable with Sugar snacks, % 94 94
respect to the children’s oral health habits and Number of meals per day 5 (2-7) 5 (2-10)
dietary habits (Table 1). However, children in
the control juice group used slightly more xylitol TABLE
products (98% in the control juice group vs. 95% in the 2. The number of children with different Streptococcus mutans scores at the baseline,
LGG-CaLG juice group, p=0.061). in the middle and in the end of the study in groups consuming either juice enriched
The average daily consumption of juice in the LGG- with Lactobacillus GG and calcium lactate gluconate (LGG-CaLG juice group, n=211)
or control juice (control juice group, n=220). 1S. mutans scores 0-103 CFU/ml; 2S.
FIGURE 1. Flow-chart indicating the progress of mutans scores 104-105 LGG-CaLG
CFU/ml; 3S. mutans =105 CFU/ml CONTROL
participation in the different phases of the 7- month study. JUICE GROUP JUICE GROUP
Class 0-11 Class 22 Class 33 Class 0-1 Class 2 Class 3
Baseline 190 (90%) 10 (4.7%) 11 (5.2%) 199 (91%) 14 (6.4%) 7 (3.2%)
Middle 196 (93%) 10 (4.7%) 5 (2.4%) 202 (92%) 13 (5.9%) 5 (2.3%)
End 199 (94%) 8 (3.8%) 4 (1.9%) 207 (94%) 10 (4.5%) 3 (1.4%)

CaLG juice and control juice groups were 92 (SD 0.33) and 95 (SD
0.31) ml with no difference in the compliance (46% and 47%).
Salivary LGG was analyzed twice in a subgroup of study children
(total n=362, LGG-CaLG juice group n=179, control juice group
n=183). At baseline, 9.5% of subjects in the LGG-CaLG juice group
and 12.0% in the control juice group had detectable amounts of
LGG in saliva. At the end of the study the figures were 42.5% versus
17.5% (baseline-adjusted OR=4.09; 95% CI 2.44 to 6.86; p<0.001).

Streptococcus mutans counts

Only few children showed S. mutans infection (Table 2). During
224 Probiotics and caries risk in children

the intervention, the number of children with high S. mutans counts Results on clinical dental examination
(score 3) decreased from 5.2% to 1.9% in the LGG-CaLG juice group According to the S. mutans counts and clinical examination in the
and from 3.2% to 1.4% in the control juice group. We combined end of the study, the combined high to moderate caries risk increased
moderate and high S. mutans count groups (scores 2 to 3) for further in both groups during the study, from 27% to 32% in the LGG-
analyses. In the middle of the study, the number of children in moderate CaLG juice group and from 29% to 37% in the control juice group
and high count groups had decreased from 10.0% to 7.1% in the (Table 3). At the end of the study the corresponding percentage was
LGG-CaLG juice group and from 9.5% to 8.2% in the control juice 31% in the LGG-CaLG juice group and 37% in the control juice
group (baseline-adjusted OR 0.75; 95% CI 0.30 to 1.87; p=0.537). group, that is, caries risk was non-significantly 29% lower in the
In the end of the study the percentage had decreased to 5.7% in the LGG-CaLG juice group compared to control juice group (baseline-
LGG-CaLG juice group and to 5.9% in the control juice group (baseline- adjusted OR=0.71; 95% CI 0.38-1.32; p=0.281).
adjusted OR 0.71; 0.27 to 1.87; p=0.490). The odds ratios indicate a The need of dental care increased in both study groups during the
non-significant risk reduction, 25% in the middle of the study and intervention, from 86 (43%) to 91 (46%) in the LGG-CaLG juice
29% in the end of the study, in favor of the LGG-CaLG group. group and from 99 (50%) to 114 (58%) in the control juice group
(Figure 2). Thus, at the end of the study,
TABLE 3. Dental caries risk at baseline and in the end of the study in groups consuming either juice the need of dental care was smaller in the
enriched with Lactobacillus GG and calcium lactate gluconate (LGG-CaLG juice group, n=197) or LGG-CaLG juice group compared to the
control juice (control juice group, n=197). 1no caries and S. mutans count <105 CFU/ml; 2decayed, controls (baseline-adjusted OR=0.58; 95%
missing or filled teeth or initial caries score >0 or S. mutans count >105 CFU/ml; 3decayed, missing or filled
CI 0.34-1.00; p=0.050). At the end of the
teeth or initial caries score >0 and S. mutans count >105 CFU/ml.
intervention there were slightly more
LGG-CaLG CONTROL children in the LGG-CaLG juice group
JUICE GROUP JUICE GROUP than in the control juice group who had all
Low1 Moderate2 High3 Low Moderate High the six mouth sextants healthy (baseline-
Baseline 144 (73%) 44 (22%) 9 (4.6%) 140 (71%) 51 (26%) 6 (3.0%) adjusted OR=1.69, 95% CI 0.99-2.89;
End 135 (69%) 58 (29%) 4 (2.0%) 125 (64%) 69 (35%) 3 (1.5%) p=0.056, Table 4).
TABLE 4. The number of healthy sextants at baseline and in the end of the study in the groups
DISCUSSION
consuming either juice enriched with Lactobacillus GG and calcium lactate gluconate (LGG-
In the present study we examined, for the
CaLG juice group, n=197) or control juice (control juice group, n=197).
first time, whether long-term consumption of
NUMBER BASELINE END a juice enriched with LGG and CaLG affects
LGG-CaLG Control p-value LGG-CaLG Control p-value the development of caries in children. At the
juice group juice group juice group juice group end of the 7-month study, the need for dental
0 8 (4.0%) 10 (5.1%) 11 (5.5%) 11 (5.6%) care was smaller and there were more children
1 0 (0.0%) 1 (0.5%) 1 (0.5%) 0 (0.0%) who had all the six sextants healthy in the
2 7 (3.5%) 5 (2.5%) 4 (2.0%) 9 (4.5%) LGG-CaLG juice group compared with the
3 12 (6.0%) 18 (9.1%) 8 (4.0%) 15 (7.6 %) control juice group. However, no statistically
4 33 (17%) 35 (28%) 39 (20%) 39 (20%) significant differences were found between
5 27 (14%) 30 (15%) 29 (15%) 40 (20%) the study groups in the caries risk and salivary
6 112 (56%) 99 (50%) 0.210 107 (54%) 84 (42%) 0.056 S. mutans counts. Hence a functional mixture
of LGG and calcium was able to
FIGURE 2. Number of children at baseline and in the end of the study needing dental care in the
slightly protect the children’s teeth
groups consuming either juice enriched with Lactobacillus GG and calcium lactate gluconate (LGG-
even in a sugar containing juice
CaLG juice group, n=199) or control juice (control juice group, n=198).
confirming earlier positive findings
on reducing the risk of dental caries
with probiotic milk, cheese, yoghurt,
lozenge, straws and tablets (Näse et
al., 2001; Ahola et al., 2002; Caglar
et al., 2005, 2006, 2008). Children
commonly consume juices even
though their excessive consumption
is related to an increased risk of dental
erosion and caries (Moazzez et al.,
2000; Jensdottir et al., 2004).
Therefore, we aimed to formulate
juice to reduce its cariogenic and
erosive potential.

Our positive post-treatment effect confirms earlier observations
that LGG may inhibit the colonization of Streptococcus sobrinus
(Meurman et al., 1995), a member of the mutans streptococci
family. It has also been shown that LGG ferments sucrose very
slowly indicating that this bacterium is not cariogenic (Saxelin,
1997; Haukioja et al., 2008). Some probiotic strains seem to inhibit
S. mutans in human saliva (Näse et al., 2001; Caglar et al., 2005,
2006, 2008). There are also critical reports (Montalto et al., 2004)
and some lactobacilli and bifidobacteria are actually cariogenic
(Aas et al., 2008) which emphasizes that the effects are strain
specific. In two recent studies LGG is found to ferment glucose
(Haukioja et al., 2008; Hedberg et al. 2008). However, amount of
glucose in saliva is rather low and LGG did not ferment or
fermented only slowly sucrose and lactose in these studies. This
characteristic could be one reason why we found stronger positive
effects with probiotic milk (Näse et al., 2001) while only a trend
with probiotic juice was seen in the present study.
Seven-month intervention is a short time for caries lesions to
develop. Therefore we assessed the caries risk with both clinical
and microbiological data (S. mutans counts) as has been found
practical in our earlier study (Näse et al., 2001). The risk of dental
caries was classified as low, moderate or high. The high caries risk
decreased in both study groups while the moderate caries risk
increased during the intervention. At the end of the study the
combined moderate to high caries risk was 31% in the LGG-
CaLG juice group and 37% in the control juice group which
accords with earlier Finnish studies reporting caries prevalence of
28-41% in this age group (Alaluusua et al., 1983; Mattila et al.
1998). Nevertheless, in the end of the present study the need of
dental care was smaller and there were more children who had all
the six sextants healthy in the LGG-CaLG juice group compared
to the control juice group.
The S. mutans counts from saliva were assessed from samples
taken from the upper surface of the tongue as reported by
Meurman and Rantonen (1994) from adult population and
now found practical also in the present study with children. The
moderate and high S. mutans levels decreased in both study
groups, although no statistically significant difference was found
between the groups. One explanation might be that there were
only few children that had caries and S. mutans infection at all.
At baseline, high S. mutans counts were detected in 11 out of
211 children (5.2%) in the LGG-CaLG juice group and only in
7 out of 220 children (3.2%) in the control juice group.
Corresponding S. mutans counts in our earlier study were 13%
in the LGG milk group and 8.6% in the placebo milk group
(Näse et al., 2001). Our study juices contained sucrose because
the taste of calcium needed to be covered with flavor and sugar
is the natural ingredient of juice. The sugar content might be
one reason why no statistically significant decrease in the S. mutans
counts could be detected during the study.
The high intake of sucrose has been shown to increase the risk
of dental caries in children (Ruottinen et al., 2004). In that study
the most frequently used food rich in sugar was sweetened dairy
products. On the other hand, it has been shown that brushing the
teeth twice a day with fluoride toothpaste may have greater impact
Probiotics and caries risk in children 225
on caries in young children than restricting sugary foods (Gibson
and Williams, 1999). In the present study we found that only
33% of the children brushed their teeth twice a day and 64%
brushed once a day. According to a Finnish study only 18% of the
5-year-olds Finns brushes their teeth twice a day (Mattila et al.,
1998) which is remarkable less than, for example in the UK,
where about 50% of the children brushes their teeth more than
once a day (Gibson and Williams, 1999).
In addition to probiotics, our study juice also contained calcium
in the form of CaLG. This may explain some of the positive effects.
The dissolution of mineral from enamel to the surrounding
environment is proportionate to the concentration of calcium and
phosphorus. Consequently, the addition of calcium and phosphate
to a drink in amounts corresponding to the enamel content can
prevent enamel from dissolving (Attin et al., 2005; Jensdottir et
al., 2005; West et al., 2004).
The results of the present study showed that consumption of
juice containing LGG and calcium might reduce the need for
dental care in children. However, no statistically significant
differences were observed between the study groups in the caries
risk and salivary S. mutans counts. Nevertheless, in the LGG-
CaLG juice group there were more children who had all the six
sextants healthy, indicating a post-treatment effect that
supplementation of juice with probiotics and calcium might be
beneficial for dental health in children.
CONFLICT OF INTEREST
S. Pohjavuori, A.J. Ahola and R. Korpela were employees of
Valio Ltd, sponsoring the study.
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