ODOVTOS

Quispe et al: Complicaciones quirúrgicas de la elevación de seno maxilar en implantología

BASIC RESEARCH DOI: https://doi.org/10.15517/ijds.v0i0.34573

Received:
1-VIII-2018
Remineralizing Effect of Xilitol, Juniperus Communis and Camellia
Accepted:
Sinensis Added to a Toothpaste: An In Vitro Study
11-IX-2018

Published Online:
Efecto remineralizante del Xilitol, Juniperus Communis y Camellia
18-IX-2018 Sinensis adicionados en pastas dentales: Estudio in vitro

Sandra I. Jiménez-Gayosso DDS¹,²; Edith Lara-Carrillo DDS, MSc, PhD¹;

Rogelio J. Scougall-Vilchis DDS, MSc, PhD¹; Raúl A. Morales-Luckie BS Chem, PhD³;
Carlo E. Medina Solís DDS, MSc¹,²; Ulises Velázquez-Enríquez DDS, MSc, PhD¹;
Gerardo Maupomé DDS, MsC, PhD⁴,⁵; Brenda Herrera-Serna DDS, MSc¹,⁶

1. Advanced Studies and Research Centre in Dentistry "Dr. Keisaburo Miyata" of Faculty of Dentistry
at Autonomous University State of Mexico, Toluca, Mexico.
2. Academic Area of Dentistry of Health Sciences Institute at Autonomous University of Hidalgo State,
Pachuca, Mexico.
3. Sustainable Chemistry UAEMex-UNAM Research Center of Faculty of Chemistry at Autonomous
University State of Mexico, Toluca, Mexico.
4. Richard M. Fairbanks School of Public Health, Indiana University/Purdue University in Indianapolis.
Indianapolis, USA.
5. Indiana University Network Science Institute. Bloomington, USA.
6. Autonomous University of Manizales, Colombia.

Correspondence to: Dra. Edith Lara-Carrillo - [email protected]

ABSTRACT: The aim of this study was to explore the remineralizing effect of toothpastes
based on Xilitol, Camellia Sinensis and Juniperus Communis. An in vitro experimental
study was carried out in an 18 human premolars sample, which were treated with one
of the 3 evaluated toothpastes and a control fluoride one. The atomic percentages of
Ca and P were evaluated by Energy Dispersive X-ray Spectroscopy (EDS). In addition,
the enamel surface of treated teeth was visualized by Scanning Electron Microscopy
(SEM). The evaluations were carried out in three stages: pre-treatment, after an
artificial demineralization process and after the treatment with the toothpastes. In the
statistical analysis, the one-way ANOVA and Pearson correlation tests were used. Xilitol
and Juniperus Communis showed the greatest gain of P ions compared to the control
group (p<0.01). As for Ca, the group treated with xylitol-based toothpaste showed
more ion gain compared with the control group (p<0.01). In the Pearson correlation
test between Ca and P, statistically significant correlations were observed in all groups
(p<0.01), ranging between r=0.7413 (Xylitol Group) and r=0.9510 (Control Group).
We concluded that Xylitol paste showed the highest remineralizing property, both in
the EDS analysis and in the SEM images.

JIMÉNEZ S., LARA E., SCOUGALL R., MORALES R., MEDINA C., VELÁZQUEZ U., MAUPOMÉ G., HERRERA B., 2020: Remineralizing Effect of Xilitol,
Juniperus Communis and Camellia Sinensis Added to a Toothpaste: An In Vitro Study.-ODOVTOS-Int. J. Dental Sc., 22-1 (January-April): 71-79.
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 ODOVTOS-International Journal of Dental Sciences

KEYWORDS: Remineralization; Xylitol; Juniperus Communis; Camellia Sinensis;

Toothpaste; In Vitro Techniques.

RESUMEN: El objetivo de este studio fue explorer el efecto remineralizante de las cremas
dentales compuestas de Xilitol, Camelia Sinensis y Juniperus Communis. Se llevó a
cabo un estudio experimental in vitro en una muestra de 18 premolares humanos, los
cuales fueron tratados con una de las tres pastas dentales evaluadas y una fluorada.
Los porcentajes atomicos de Ca y P fueron evaluados por Espectroscopia de rayos X
de energía dispersive (EDS). Además, la superficie del esmalte de los dientes tratados
fue examinada por Microscopia Electronica de Barrido (SEM). Las evaluaciones fueron
llevadas a cabo en tres etapas: pre-tratamiento, despues de un proceso artificial de
desmineralizacion y después del tratamiento con las pastas dentales. Se usaron ANOVA
de una via y correlacion de Pearson para el analisis estadistico. Xilitol y Juniperus
Communis mostraron la mayor ganancia de iones P comparados con el grupo control
(p<0.01), con rangos entre r=0.7413 (Grupo con Xylitol) and r=0.9510 (Group Control).
Se concluyó que la pasta con Xilitol mostró las mayores propiedades remineralizantes,
tanto en el analisis EDS y las imágenes SEM.

PALABRAS CLAVE: Remineralizacion; Xylitol; Juniperus communis; Camellia sinensis;

Pasta dental; Técnicas in vitro.

INTRODUCTION prevent the disease in its incipient stages (1-

3). The importance of fluoride is indisputable
The balance of demineralization and as a viable and economical method; most likely,
remineralization in dental caries is fundamental it will continue to lead the prevention of dental
to understand the presence and progress of initial caries. However, there are compounds that serve
or subclinical lesions (1-3). These cycles are a as adjuvants in the remineralization process (11).
complex series of events on the tooth surface, Currently there is a growing interest in options
which take place in ecological changes within that do not contain fluoride. These compounds are
the dental biofilm (4,5). At the beginning they are biologically active, mainly derived from natural
observed clinically as a small demineralized area. products such as tea (eg, Camellia Sinensis or
Remineralization is a net gain of ions towards the green tea), coffee, grapes, propolis, as well as
dental tissues, which replaces the loss due to the some Asian herbs and mushrooms (12), synthetics
demineralization process. This occurs through products such as amorphous calcium phosphate,
a physical-chemical process that includes the casein and xylitol (13-15). Xylitol [(CHOH) 3(CH2OH) 2]
supersaturation of ions in the solution in relation is a non-acidic sweetener; it is associated with
to enamel, the formation of nucleus and crystals Ca in aqueous solution to inhibit the dissolution
(6,7). Since the control of dental caries remains of enamel’s calcium or phosphate ions, thus acting
a challenge (8) as one of the main public health as a calcium transporter required for enamel
problems in the world, its negative impacts should remineralization (16).
not be underestimated. Among other effects,
dental pain, tooth loss, effects on general well- The objective of this article was to evaluate
being and quality of life must be mentioned (9,10). the remineralizing effect of toothpastes based on
It is important to look for effective treatments to Xylitol, and of two biologically active natural botanical

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 Jiménez et al: Remineralization with Xylitol, Juniperus Communis and Camellia Sinensis

agents, Camellia sinensis and Juniperus communis. CYCLIC PH MODEL

This exploration of its remineralizing potential was
compared against a fluoridated toothpaste. The specimens were exposed to a cyclic pH
model for 15 days at 37°C in order to simulate the
MATERIALS AND METHODS conditions of the oral environment.

An experimental in vitro study was carried Each specimen was immersed in a

out. The protocol was reviewed and approved demineralizing solution (2.2Mm CaCl2, 2.2Mm
by the Research and Ethics Committee of the NaH2PO4, 0.05 Mm CH3COOH, 1M KOH, pH 4.4,
Autonomous University State of Mexico. 10 mL/specimen) twice a day for 3 hours and for 2
hours in the remineralizing solution (1.5Mm CaCl2,
We included 18 human premolars extracted 0.9Mm NaH2PO4, 0.15Mm KCl, pH 7.0, 10mL /
for orthodontic reasons. All the patients signed an specimen) between the demineralization cycles.
informed consent.
The specimens treated with the toothpastes
Bicuspids had no restorations, fractures or were embedded in suspension of toothpaste
decay on the vestibular face. The teeth were stored according to their group (5 mL per specimen) for 60s
in 0.2% thymol after extraction. Teeth were randomly before the onset of the first demineralization cycle
assigned to one of six groups. Control group, which and before and after the second demineralization
was not exposed to any procedure; Demineralization cycle. Then, they were stored in remineralizing
only group, exposed to an artificial demineralization solution in an incubator at 37ºC for 16 hours to
process; Xilitol group, exposed to 100% Natural complete 24 hours of a cycle (17).
Dentiste toothpaste (Bangkok, Thailand); Camelia
sinensis group, exposed to Fluocaril toothpaste TEETH PREPARATION FOR ANALYSIS BY SEM AND EDS
(Bangkok, Thailand); Juniperus communis group,
exposed to Splat Special Blackwood toothpaste We obtained 3x3 mm blocks of enamel from
(Moscow, Russia); and Toothpaste Control Group, the vestibular surface of the teeth. They were cut
exposed to Colgate Triple Action toothpaste (San with a carbide disc, then we cleaned of specimens
Jose Iturbide, Guanajuato, Mexico). for 5 minutes in separate containers, filled with
tri-distilled water in an ultrasonic bath (Quantrex
ALL THE TEETH WERE SUBJECTED TO THE Q140, L & R Ultrasonics, NJ, USA). Next, the blocks
FOLLOWING PROCESSES FOR FURTHER ANALYSIS were fixed to an aluminum specimen holder with
carbon adhesive tape (SPI Supplies, USA).
ARTIFICIAL DEMINERALIZATION PROCESS
The atomic percentages of Ca and P were
An artificial demineralization process was evaluated, which were analyzed with EDS. In
performed, for which the specimens were immersed addition, the enamel surface was visualized by SEM.
in a demineralizing solution (2.2 Mm CaCl2, 2.2
Mm NaH2PO4, 0.05 Mm CH3COOH and 1M KOH) The SEM analysis was performed using a
adjusting the pH to 4.4 during 96 hours at 37 ° C scanning electron microscope (JEOL, JSM-6510LV,
in an incubator (17). Japan) in the low vacuum mode at 10 Pa of pressure

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 ODOVTOS-International Journal of Dental Sciences

in the chamber, with an electron acceleration voltage test between Ca and P, statistically significant
of 15 kV and detecting backscattered electrons. correlations were observed in all groups (p <0.01),
ranging from r=0.7413 (Xylitol Group) to r=
The morphology of the enamel surface 0.9510 (Control Group).
was observed at a magnification of 500x at a
working distance of 50 mm. We determined the When performing the one-way ANOVA test
atomic percentages (% at) of Ca and P using for the comparison of P, statistically significant
an X-ray detector system (Oxford Instruments, differences were found between the Control
7582, United Kingdom) coupled to the scanning Toothpaste Group vs the Xylitol Group (p<0.001),
electron microscope. the Control Toothpaste Group vs the Camelia
Sinensis Group (p=0.003) and between the Control
STATISTICAL ANALYSIS Toothpaste Group vs Juniperus Communis Group
(p<0.001). With respect to Ca, statistically
Data were analyzed using the statistical significant differences were obtained between
package SPSS 23.0 (SPSS Inc., Chicago, USA). the Xylitol Group vs. the Demineralization Group
The one-way ANOVA test was performed with (p=0.001) and between the Control Toothpaste
Bonferroni’s correction for multiple comparisons Group vs the Xylitol Group (p <0.001) (Table 2 and 3).
of atomic percentages of Ca and P; the value of
p was adjusted to 0.001667. We also used the QUALITATIVE ANALYSIS WITH SEM OF THE
Pearson Correlation test between Ca and P, with a SPECIMENS’ SURFACES
significance of p≤0.05.
In Fig. 1 we observe the microphotographs
RESULTS representative of the SEM enamel surfaces analysis
for the groups. In the pretreatment analysis of the
QUANTITATIVE EVALUATION OF CHEMICAL enamel surface morphology, shown in Fig.1a),
COMPOSITION WITH EDS we observe the prisms exposed in a “key hole”
shape, as well as in a circular form. On the enamel
The chemical composition of the enamel surface after artificial demineralization we can
surface was determined before treatment, after a observe a smooth appearance without perikymata
demineralization process and after the treatment pattern, with irregular fissures, as well as small
with each of the remineralizing toothpastes, which defects in its periphery and presence of numerous
were presented in at%. irregular holes (Fig.1b). In the enamel surfaces
treated with the toothpastes studied, smooth
Table 1 shows the results of the atomic surfaces with various porosities and grooves were
percentage analysis of the Ca and P elements found in the goups treated with Camellia Sinensis
of each study group. In the Pearson correlation and Juniperus Communis toothpastes (Fig.1c-f).

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 Jiménez et al: Remineralization with Xylitol, Juniperus Communis and Camellia Sinensis

Table 1. Analysis of the Ca and P element atomic percentage.

Chemical Control Group Demineralization Xylitol Group Camelia Juniperus Control F p

element Group sinensis Group communis Toothpaste value*
at% Group Group
Ca 16.96±3.56 15.22±1.57 21.01±3.05 17.19±4.48 17.77±1.67 14.66±4.70 6.8 0.000
P 11.38±2.33 11.15±1.10 12.93±1.56 12.26±2.02 13.03±1.00 9.31±2.51
Correlation† r= 0.9510 r= 0.9161 r=0.7413 r=0.9371 r=0.9161 0.7626
p<0.0010 p<0.0010 p=0.0058 p<0.0010 p<0.0010 p<0.0012

* Analysis of variance (ANOVA)

† Pearson correlation of Ca y P

Table 2. Multiple comparisons of Bonferroni for P.

Control Group Demineralization Xylitol Group Camelia sinensis Juniperus

Group Group communis Group
Demineralization -0.2325
Group 1.000
Xylitol Group 1.5525 1.785
0.662 0.319
Camelia sinensis .8775 1.11 -0.675
Group 1.000 1.000 1.000
Juniperus communis 1.65 1.8825 0.0975 0.7725
Group 0.491 0.231 1.000 1.000
Control Toothpaste -2.0725 -1.84 -3.625 -2.95 -3.7225
Group 0.119 0.266 0.000 0.003 0.000
*The p value was adjusted to a significance of 0.001667.

Table 3. Multiple Bonferroni comparisons for Ca.

Control Group Demineralization Xylitol Group Camelia sinensis Juniperus

Group Group communis Group
Demineralization -1.74
Group 1.000
Xylitol Group 4.04583 5.78583
0.074 0.001
Camelia sinensis .224167 1.96417 -3.82167
Group 1.000 1.000 0.116
Juniperus communis .811666 2.55167 -3.23417 .5875
Group 1.000 1.000 0.347 1.000
Control Toothpaste -2.29833 -.558333 -6.34417 -2.5225 -3.11
Group 1.000 1.000 0.000 1.000 0.431
*The p value was adjusted to a significance of 0.001667.

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 ODOVTOS-International Journal of Dental Sciences

A B

C D

E F

Figure 1. a) Pretreatment enamel surface morphology, b) Enamel surface after an artificial demineralization process,
c) Enamel surface after treatment with xylitol toothpaste, d) Enamel surface after Camellia sinensis.

DISCUSSION higher atomic percentage of P; however, it cannot

be definitively concluded if this result is due to
In the present study, the remineralizing the active component of Juniperus communis,
effect of Xylitol, Camellia sinensis and Juniperus since pyrophosphates are found within the
communis added to dentifrices was evaluated, ingredients of this toothpaste. On the other hand,
using a fluoride toothpaste as a control. We when analyzing the atomic percentages of Ca,
studied the morphological and chemical changes statistically significant differences were observed
of human premolars enamel surface after between the group treated with the Xylitol
their treatment with the toothpastes previously toothpaste and the control group. This ion gain
mentioned. It was found that specimens treated benefits the remineralization process by the net
with the Juniperus communis toothpaste had a addition into the enamel structure, which replaces

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 Jiménez et al: Remineralization with Xylitol, Juniperus Communis and Camellia Sinensis

what was previously lost by demineralization. to prevent oxidative damage to biological systems
It should be mentioned that this occurs through by reactive forms of oxygen H2, O2, O2- and OH)
a physical-chemical process that includes the that are produced during cellular metabolism in
ions supersaturation of the solution respecting organisms (29,30). It is worth mentioning that, in
to enamel, the formation of nucleus and crystal the present study, an almost perfect correlation
growth (18,19). was found between the amount of calcium and
phosphate ions when applying the Juniperus
It is well known that Xylitol in high communis toothpaste (28). For these reasons it
concentrations has the ability to form compounds is advisable to perform in vivo studies to evaluate
with calcium ions and penetrate the demineralized these effects - both the effects of the different types
enamel, where it can contribute to transporting of Juniperus by themselves, and in conjunction
dissolved ions by decreasing the calcium and with pyrophosphates in the toothpaste.
phosphate diffusion coefficient (15,20). Studies
have shown greater remineralizing effect in both Although the use of fluorides is essential
varnishes (15) and in toothpastes (21) when in the prevention of dental caries, it is important
xylitol is added to fluoride. In our study we found to explore the value of available alternatives. The
a positive correlation between the presence of present research aims to expand the knowledge
calcium and phosphorus; however, this was the about remineralizing substances that are not
weakest correlation, even compared with the based on fluoride. These have become attractive
control toothpaste group. In vivo studies have for patients interested in using products that are
shown that the remineralization process can be perceived to be biologically natural alternatives, or
accelerated because xylitol reduces the acidity of with fluorides excluded in their formulation. The
the bacterial biofilm, allowing fluoride to act under cultural tendency to exclude fluorides from water-
more favorable conditions (22). manifested in multiple votes in developed countries
in which local populations reject the addition of
Recent studies have shown the remineralizing fluorides to drinking water-makes it necessary
effect of Camellia sinensis (23,24) Likewise, it to evaluate the different options available in the
has been shown that its addition to carbonated market for prevention of dental caries.
drinks reduces the demineralization they cause
(25). In this study we found that the addition of This study has the limitation that it was
this compound to toothpastes helps to increase undertaken in a small sample. Despite its
calcium and phosphate ions, obtaining a strong exploratory nature, our results confirm some past
correlation. These results are not definitive: literature reports, and provide new evidence. Xylitol
in a dynamic environment such as the mouth, toothpaste showed the highest remineralizing
antibacterial effects should be evaluated (26). It property, both in the EDS analysis and in the SEM
should be determined whether remineralization images. Although the Camelia sinensis toothpaste
is influenced by the variable fluoride levels in the showed positive results by EDS, the SEM
Camellia sinensis leaves (27). images showed a smooth surface, similar to the
demineralized surface. The Juniperus communis
Reviewing the literature, no evidence was toothpaste was associated with a high percentage
found of the Juniperus communis remineralizing of phosphate; this may be due to the fact that its
effect (28) However, its antioxidant effect has been composition includes pyrophosphates, which can
proven, which is directly related to its application form synthetic phosphates.

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