|Year : 2018 | Volume
| Issue : 5 | Page : 237-243
Effect of chewing gums containing probiotics and xylitol on oral health in children: A randomized controlled trial
Kanwardeep Kaur1, Sridhar Nekkanti1, Mridula Madiyal2, Prashant Choudhary3
1 Department of Pedodontics and Preventive Dentistry, Manipal College of Dental Sciences, Manipal, Karnataka, India
2 Department of Microbiology, Kasturba Medical College, Manipal, Karnataka, India
3 Faculty of Dentistry, SEGi University, Kota Damanasara, Petaling Jaya, Selengor, Malaysia
|Date of Web Publication||24-Oct-2018|
Prof. Sridhar Nekkanti
Department of Pedodontics and Preventive Dentistry, Manipal College of Dental Sciences, Manipal - 576 104, Karnataka
Source of Support: None, Conflict of Interest: None
Aims: Probiotics have been proven to be beneficial for general and systemic health. Many in vitro and in vivo studies have investigated the use of probiotics for the prevention or treatment of dental caries and gingival diseases. Lactobacillus reuteri is believed to possess anti-microbial and anti-inflammatory properties. The aim of our randomized controlled trial was to evaluate the effect of chewing gums containing probiotics and xylitol on the salivary Streptococcus mutans counts, plaque, and gingival scores after the intervention. Materials and Methods: In our 3-week, short-term trial, 40 healthy 7–12-year-old children consumed two commercially available chewing gums; Group 1 (BioGaia™ ProDentis) and Group 2 (Orbit®Gum, Wrigley's). Individuals consumed three chewing gums daily, immediately after major meals for 20 min each. The probiotic gum contained two strains of L. reuteri (ATCC 55730 and ATCC PTA 5282) along with artificial sweetener, sorbitol, and the xylitol gum consisted of both xylitol and sorbitol. Pre- and post-intervention whole unstimulated saliva samples were collected and cultured on Mitis Salivarius Bacitracin agar plates to check for colony forming units/ml of Streptococcus mutans. Plaque and gingival scores were also recorded at pre- and post-intervention appointments. Results: Following the intervention, the salivary Streptococcus mutans counts decreased in both groups. There was a significant reduction in plaque and gingival scores at postintervention examination. Conclusion: Probiotics can be used as an alternative to xylitol in the preventive regimen for dental caries or control in case of high caries risk.
Keywords: Dental caries, gingival index, plaque index, probiotics, xylitol
|How to cite this article:|
Kaur K, Nekkanti S, Madiyal M, Choudhary P. Effect of chewing gums containing probiotics and xylitol on oral health in children: A randomized controlled trial. J Int Oral Health 2018;10:237-43
|How to cite this URL:|
Kaur K, Nekkanti S, Madiyal M, Choudhary P. Effect of chewing gums containing probiotics and xylitol on oral health in children: A randomized controlled trial. J Int Oral Health [serial online] 2018 [cited 2020 Oct 1];10:237-43. Available from: http://www.jioh.org/text.asp?2018/10/5/237/243854
| Introduction|| |
The prevalence of dental caries has significantly reduced in the past few decades owing to the use of fluoride and popularity of dentifrices. While the developed nations have preventive protocols, organized dental homes, and awareness programs, industrialized nations such as India still face the burden of oral diseases.
Fejerskov and Nyvad, 2003 redefined dental caries as, “A complex microbiologic disease caused by an imbalance in the physiologic equilibrium between tooth mineral and biofilm fluid.” Based on studies conducted by various authors and data collected over the years, the American Academy of Pediatric Dentistry, 2016 has enumerated following risk factors for dental caries: High levels of salivary Streptococcus mutans obacilli, low buffering capacity of the saliva, low fluoride levels in plaque and saliva, presence of plaque on teeth, and low socioeconomic status.
The oral cavity is home to over 250 microbial species and the dental hard tissue with its pits and fissures, and other inaccessible areas are the safe haven of these microbes. These species colonize the oral cavity in a methodical manner, from adhesion and succession to progression. Once the biofilms are formed, caries develop in those regions where they are allowed to mature and remain undisturbed for prolonged periods of time. Even among a plethora of microorganisms in the oral cavity, acidogenic organisms such as Streptococcus mutans have been found to play a major role in causing dental caries. These acidogenic organisms produce acid during metabolism of dietary carbohydrates. The acids thereby formed can dissolve the tooth mineral through a complex cycle of demineralization and remineralization and eventually take part in causing dental caries.
Over the past decade, scientists have been working on more conservative treatments and dentistry has seen a paradigm shift from its traditional “mechanics-based surgical” model to a “biologically-based medical” model. Although “drill and fill” still occupies a major place in our regimen, scientists are on the lookout for newer techniques to alter the oral environment and shift the balance toward protective factors. The new age treatment is aimed to be preventive rather than therapeutic.
Fluoride has remained as the mainstay of preventive dentistry since the past few decades. Other methods such as caries vaccine and remineralizing agents have been discussed in literature at length. At present, alternatives such as bacteriotherapy and use of sugar substitutes are being studied.
Among sugar substitutes, the role of natural sugar, xylitol in targeting oral microflora has been well established. Xylitol is known to inhibit the growth and metabolism of mutans Streptococcus group. Xylitol is not readily metabolized by bacteria and hence has been claimed to be anti-cariogenic. While the caries-preventive and cariostatic effect of xylitol is proven, its role in actively antagonizing caries is still controversial. Nevertheless, xylitol chewing gums are widely used commercially. Several in vivo trials have proven the effectiveness of xylitol in the reduction of Streptococcus mutans counts in plaque and saliva, but one of the latest systematic reviews has concluded that there is insufficient and low-quality evidence regarding its effectiveness.
Over the years, many more antimicrobials have been studied and the anti-cariogenic role of “probiotics” is now being thoroughly researched. As defined by International Scientific Association for Probiotics and Prebiotics, probiotics are “live microorganisms, which when administered in adequate amounts, confer a health benefit on the host.” Both in vitro and clinical studies have confirmed the positive association between Lactobacilli and oral health. Clinical trials have proven that probiotic bacterium, Lactobacillus reuteri can reduce salivary Streptococcus mutans levels. Probiotics may have many direct and indirect effects in the oral cavity such as competitive inhibition of streptococci by replacement and direct contact with the oral tissues. An in vitro study found out that probiotics interfere with Streptococcus mutans biofilm formation. Many more possible mechanisms have also been proposed.
Although the role of xylitol in caries prevention is still questionable, most commercially available caries preventing agents such as chewing gums widely employ it. Probiotic bacteriotherapy, on the other hand, is rather new, and although several studies have confirmed its effectiveness, there is insufficient literature regarding its success.
The aim of this study was to determine the effect of chewing gums containing Probiotic Bacteria, and Xylitol on salivary Streptococcus mutans counts in 7–12-year-old children and also to assess whether there is a change in plaque and gingival scores after chewing the aforementioned gums for 3 weeks.
Hypothesis: (1) Chewing gums containing Probiotics and Xylitol have no effect on the salivary Streptococcus mutans counts in 7–12-year-old children. (2) There is no difference between the plaque and gingival scores before and after intervention with chewing gums containing probiotics and xylitol.
| Materials and Methods|| |
To be able to detect a difference between the two groups, a sample size of 16 was calculated with the power of study being 80% at a significance level of 0.05. To allow for dropouts and anticipating a “loss of follow-up” of up to 25%, additional four individuals were recruited in each group, making it a total of 40 individuals (n = 20). This investigation was a double-blinded randomized controlled trial in accordance with Consolidated Standards of Reporting Trials and Helsinki Declaration of Human Rights [Figure 1].
The individuals were screened from a group of children who visited the Department of Pedodontics and Preventive Dentistry, Manipal College of Dental Sciences, Manipal as a part of the institution's school health program initiative. Materials used for screening included mouth mirror, probe, tweezers, cotton and gauze piece, disposable gloves and mouth mask. Sterile graded cups for the collection of unstimulated saliva samples, 2 cc syringe to transport saliva sample, disposable gloves and mouth mask were among the materials used for sample collection. Culturing media used included Mitis Salivarius Bacitracin (MSB) Agar with Potassium Tellurite (Hi-Media®, Hi-Media laboratories, Mumbai, India), standard loop to streak the saliva sample on the culture plate, and MSB agar plate. Chewing gums used in the study were Probiotic Chewing Gums (BioGaia™ ProDentis, Sweden) containing L. reuteri DSM 17938 And L. reuteri ATCC PTA 5289 (L. reuteri Prodentis) and Xylitol Chewing Gums (Orbit® Gum, Wrigley's, India). This study was approved by Institutional Ethics Committee, Kasturba Hospital, Manipal (Registration number: ECR/146/INST/KA/2013) bearing number IEC 672/2015. The clinical trial was prospectively registered with Clinical Trials Registry of India bearing the registration number: CTRI/2017/05/008518.
A total of 200 children, 7–12-year-old children who visited the Department of Pedodontics and Preventive Dentistry, Manipal, as a part of the department's school health program were screened. Based on the inclusion and exclusion criteria, 40 children were selected for the study. Inclusion criteria: healthy children in the age group of 7–12 years, children with decayed, missing, and filled teeth/deft score more than 1, children with similar oral hygiene and dietary habits, and those having minimal or no crowding.
Exclusion Criteria: Children suffering from any long-term medical conditions, children under current anti-microbial therapy or those who had been on the same 1 month before the commencement of the study, children who had large fillings/open carious lesions on the smooth surfaces of teeth and those with severely crowded dentition. Before recruitment of the individuals and before the commencement of the study, a patient information sheet was given to all the students in English and the vernacular, Kannada. A written informed consent designed in accordance with the guidelines of Kasturba Hospital Ethics Committee, Manipal, was obtained from the parents of participating children. Cluster Randomization was done, and the students from each school were assigned a particular chewing gum.
Unstimulated saliva was used for the assessment of Streptococcus mutans counts before the intervention. Individuals were asked to expectorate the saliva into sterile graded cups which were transferred to the department of microbiology for analysis within 20 min of collection. The collected salivary samples were cultured on MSB Agar quantitatively. Commercial media from Hi-Media® (Hi-Media laboratories, Mumbai, India) was used for the preparation of the media with modifications adapted as per Gold et al., 1973 by adding 20% sucrose and 0.2 units/ml of bacitracin.
The samples were diluted in 100–10−2 dilutions using a standard loop. Plates were incubated at 37°C for 48 h in CO2 incubators. Streptococcus mutans was identified using the cultural characteristics. Doubtful isolates were identified using Vitak 2 identification system. The growth was quantified taking loop factor and dilution factor into account.
Each child in a particular school, i.e., cluster was instructed to consume three chewing gums every day, namely morning, afternoon, and night after the three major meals for 20 min throughout the study period of 21 days. In Group 1, probiotic chewing gums were given, and in Group 2 xylitol chewing gums were administered. The chewing gums were placed in similar white containers and coded by a third person who was not involved in the study.
Children were advised to continue their normal diet and tooth brushing. Before dispensing of chewing gums, a written assent of each subject was obtained, and a log sheet for each consumption was handed out to monitor consumption. The school teachers were requested to supervise consumption of chewing gums, and written notes were sent for the parents to supervise at home and on Sundays/holidays.
At the end of 3 weeks of the use of chewing gums, the salivary samples were taken again in a similar way as described for the baseline readings and subjected for microbiological analysis. Plaque and gingival scores were also recorded postintervention.
| Results|| |
The statistical analysis was done using SPSS version 18 (SPSS Inc, Illinois, Chicago, USA). A <0.05 was considered statistically significant. Colony forming units (CFU) values for pre- and post-intervention were transformed by Logarithmic transformation. Mann–Whitney U test was done to compare the log CFU/ml of Streptococcus mutans counts, plaque and gingival scores between the two groups preintervention [Table 1]. The mean Log CFU of the individuals in Group 1 and Group 2 was 3.81 (standard deviation [SD]−0.60) and 4.39 (SD −0.80), respectively. Statistically, there was no statistically significant difference in the Log CFU among the two groups. The mean plaque score in Group 1 and Group 2 was 1.49 (SD −0.26) and 1.72 (SD −0.26), respectively. No statistically significant difference was observed between the two groups. The mean gingival score in Group 1 and Group 2 was 1.37 (SD −0.30) and 1.12 (SD −0.41), respectively. Statistically significant difference was observed between the two groups.
The same test was done to compare the log CFU/ml of Streptococcus mutans counts, plaque and gingival scores between the two groups postintervention [Table 2]. The mean Log CFU of the individuals in Group 1 and Group 2 was 1.91 (SD −1.89) and 2.39 (SD-2.27), respectively. Statistically, there was no statistically significant difference in the Log CFU among the two groups. The mean plaque score in Group 1 and Group 2 was 1.31 (SD −0.24) and 1.38 (SD −0.40), respectively. No statistically significant difference was observed between the two groups. The mean gingival score in Group 1 and Group 2 was 1.16 (SD −0.27) and 0.86 (SD −0.42), respectively. Statistically significant difference was observed between the two groups.
Intragroup comparison between pre- and post-intervention
Probiotic chewing gums
Wilcoxon Signed Rank test was done to compare the means of the given parameters pre- and post-intervention in each of the two groups. The P value obtained for the pre- and post- intervention Streptococcus mutans counts in probiotic group was 0.003 [Table 3]. The null hypothesis was rejected, implying that there was a statistically significant difference between the microbial counts pre- and post-intervention with probiotic chewing gums. The P value obtained for the pre- and post-intervention plaque score was <0.001. There was a statistically significant difference between the pre- and post-intervention plaque scores. The P value obtained for the pre- and post-intervention gingival score was <0.001. Hence, there was a statistically significant difference between the pre-and post-intervention gingival scores.
Xylitol chewing gums
The log CFU counts pre- and post-intervention for the xylitol group and the P value obtained was 0.001. The obtained P value suggests that there is a statistically significant difference before and after the intervention with xylitol-containing chewing gums. The P value obtained for the pre- and post-intervention plaque score was <0.001. There was a statistically significant difference between the pre- and post-intervention plaque scores. The P value obtained for the pre- and post-intervention gingival score was <0.002. Hence, there was a statistically significant difference between the pre- and post-intervention gingival scores.
| Discussion|| |
This randomized controlled trial was carried out to assess the effect of chewing gums containing probiotics and xylitol on salivary Streptococcus counts in 7–12-year-old children. As a secondary outcome measure, the clinical implications in terms of plaque and gingival scores were also measured before and after the intervention period of 21 days.
Chewing gums stimulate salivary flow which results in an increase in the buffering capacity of saliva. The masticatory and gustatory stimuli together, aid in increasing the flow rate by as much as 10–12 times more than unstimulated saliva. This counterbalances the drop in plaque pH that occurs after eating (Burt BA, 2006). Another anti-cariogenic action of chewing gums may be due to increase in bicarbonate ions, which also improve the buffering capacity of saliva. Moreover, this leads to an increase in the rate of clearance of sugars and food debris. While sugared gum is cariogenic, gums containing non-caloric substitutes have been used in the caries-control regimen since long. The most common components of commercially available polyol chewing gums are sorbitol and xylitol. Xylitol is a derivative of pentose sugar, xylose whereas sorbitol is derived from glucose. The mechanism of action of both involves stimulation of gustation and salivary flow. Most oral bacteria cannot metabolize either of the two to form acids. The ability of sorbitol in reducing demineralization was demonstrated by chewing a gum containing sorbitol for 5 min following a sucrose rinse. The fact that enhanced salivary stimulation and subsequent remineralization can result from mastication cannot be underestimated. Recent studies have also proven that xylitol not only decreases bacterial load but also aids in increasing pH of the oral cavity and has a remineralizing potential.
Ghasemi et al., 2017 in their study used xylitol chewing gums and probiotic yogurt as vehicles. While they concluded that both were equally effective in reducing the salivary Streptococcus mutans counts, the use of a similar vehicle in both groups would have eliminated the bias of salivary stimulation on bacterial counts in the chewing gum group as compared to the yogurt group. Mitrakul et al.,2017 compared xylitol chewing gum and maltitol spray, thus creating a bias due to the difference in vehicles. Van Loveren, 2004 stated that xylitol induced reduction of dental caries could be confounded by increased salivation due to the chewing effect. Mäkinen et al., 1995 in their 40-month cohort trial used different formulations of non-sugar gums (xylitol/sorbitol) in all the nine study groups.
The beneficial effects of probiotics for the treatment of oral diseases such as caries, gingivitis, or periodontitis have been proven in vitro. Many in vivo studies,,,,, have also attempted to study the short-term and long-term effects of probiotics in the oral cavity. Different vehicles such as curd, ice creams, yogurt, or non-dairy products such as drops, straws, lozenges, tablets, and candies were used in different studies. Caglar et al., 2007 also compared chewing gums containing probiotics (L. reuteri) and xylitol in their study and concluded that both had a significant effect on Streptococcus mutans counts in saliva. Moreover, chewing gum as a vehicle is attractive and acceptable for children as compared to lozenges, yogurt, or milk.
Taking into consideration the previous studies, chewing gums were chosen as a vehicle in our study to eliminate the confounding bias as well as to have a similar amount of salivary stimulation in both groups. Most of the previous studies either compared xylitol with other polyols or with placebo. Ours is one of the first studies in children to compare xylitol and probiotic chewing gums.
Each subject was given an equal number of chewing gum pellets of probiotics and xylitol. All the individuals had healthy, adequate amount of saliva and were asked to chew the gum pellets thrice daily for 20 min each. The school teachers were explained the whole process and were requested to supervise and monitor the children. Written forms with instructions and daily checklists were given to all the children to check compliance. Similar compliance calendars were followed by Pahumunto et al., 2017 and Alamoudi et al., 2018.
The possible effect of the duration of chewing gum on the overall outcome of the intervention cannot be overlooked. Edgar et al. (1975) concluded that a 5-min duration of chewing sugar-free gum had little effect on the pH of plaque. A smaller fall in the pH and a more rapid rise of the pH back to its resting levels was noticed after a 10-min chewing duration by Park et al. Following an acidogenic challenge, the rise in resting pH levels was more rapid and took substantially lesser time when a sugarless gum was chewed for at least 20 min. Park et al., determined the optimal initiation time and duration of chewing to achieve maximum salivary stimulation and benefits of a chewing gum containing sorbitol. The authors concluded that chewing a sugarless gum within the first 5 min of eating and continuing it for a minimum of 15 min would confer the maximum benefits. Caglar et al., 2007 in their study on healthy adults used a chewing duration of 10 min and reported a significant reduction in salivary Streptococcus counts with both probiotics and xylitol. The European Food Safety Authority, 2010 reviewed a plethora of scientific research papers and recommended the use of 2–3 g of sugar-free gum for 20 min after meals. Therefore, keeping in mind the recommendations of the European Food Safety Authority, manufacturer recommendations, as well as the American Dental Association guidelines, a chewing duration of 20 min, was kept standard for both groups. Our results showed that both probiotics and xylitol significantly reduced the levels of Streptococcus mutans in saliva after 3 weeks of intervention. These results are consistent with the study conducted by Caglar et al., 2007. However, the mechanism of action of both the gums is different, and because the bias of salivary stimulation was eliminated, both groups were comparable. While probiotics, in general, may act through several mechanisms such as host modulation, prevention of cellular adhesion, competitive inhibition and coaggregation, L. reuteri particularly is known to secrete two antimicrobial agents called “Reuterin” and “Reutericyclin.” Our results revealed a statistically significant difference in the pre- and post-intervention values of Log CFU in case of probiotic chewing gums, which can be attributed to the action of saliva and the presence of “Reuterin” and “Reutericyclin” in the gum formulation.
In accordance with a study conducted by Krasse et al., 2006, we also observed a significant reduction (P < 0.001) in plaque and gingival scores (P < 0.001). Our results are consistent with Vivekananda et al., 2010 who conducted a split-mouth trial in which two quadrants were treated with scaling and root planing and the other two were left untreated. The individuals were then given probiotic lozenges for 2 weeks and a significant reduction in plaque and gingival scores was noticed. The reduction of plaque and gingival scores in our study would have been more if we had performed oral prophylaxis and root planing before administration of probiotic chewing gums.
It can thus be hypothesized that the gingival and plaque scores decreased partly because of the anti-inflammatory action of L. reuteri as supported by Cabana et al., 2006 in their in vitro study. L. reuteri inhibits the pro-inflammatory cytokine, IL-8 and upregulates Nerve Growth Factor. Second, the presence of reuterin and reutericyclin contributes toward the antimicrobial effects of L. reuteri. Finally, it can also be assumed that some reduction might be seen due to the daily chewing action which increases the overall oral clearance.
Our study, therefore, confirms the anti-inflammatory and plaque inhibitory actions of probiotic chewing gums, although the exact mechanism is still unclear.
In case of xylitol group, a small but significant reduction in plaque scores was noticed in our study. This is in accordance with the systematic review by Kukenmeester et al., 2013 where plaque scores were lowered after using polyol chewing gums. Mitrakul et al., 2017 also observed a reduction in plaque index after a 4-week intervention with xylitol gum. These results could be an effect of normal tooth brushing along with a psychological component wherein children might have been encouraged to brush their teeth more frequently and effectively because of frequent contact with the doctor. Alamoudi et al., 2018 reported a similar Hawthorne Effect. Nevertheless, the reduction in gingival scores in case of xylitol group is a controversial.
Steinberg et al.,1992 carried out a 6-week single-blinded, crossover trial wherein the study individuals chewed five xylitol gums daily in addition to maintaining normal oral hygiene. They reported that there was a reduction in plaque score and gingival inflammation after the intervention period. However, the systematic review by Keukenmeester et al., 2013 could not corroborate strong evidence for the same and questioned the validity of the previous studies. The significant reduction of gingival scores in the xylitol group as compared to the probiotic group in our study is unlikely to be due to polyols alone. It might have to do with the fact that children may not have followed instructions of avoiding all other measures of oral hygiene except for regular tooth brushing. Moreover, the different tooth brushing habits of children could have played a role in reducing gingival scores in the xylitol group more than the probiotic group despite the anti-inflammatory properties of probiotics being more pronounced than that of xylitol.
Among since the children were from lower socioeconomic strata; the compliance was questionable. Despite taking consent, assent and daily checklists, four children in the xylitol group dropped out of the study and were not available for postintervention records. Only one child reported of discomfort due to probiotic chewing gum, which might have been due to its taste and was immediately asked to discontinue intake and was withdrawn from the study.
Further long-term studies with larger a sample size are needed to compare the efficacy of probiotic and xylitol chewing gums in caries-control regimen.
| Conclusion|| |
The effect of chewing gums containing probiotics (ProDentis, BioGaia™, Sweden) and xylitol (Orbit® Gum, Wrigley's, India) on salivary Streptococcus mutans counts and plaque and gingival scores was evaluated.
The following conclusions can be drawn from this study:
- Both probiotic and xylitol containing gums are equally effective in reducing Streptococcus mutans counts in children
- There was a small but significant reduction in plaque deposition when regular home care hygiene methods were continued in both, xylitol and probiotic groups
- There was more reduction of gingival scores in case of xylitol group
- Chewing gums containing probiotics and xylitol can be an alternative regimen for prevention of caries in children in addition to fluoride supplements.
Declaration of patient consent
The authors certify that they have obtained all appropriate patient consent forms. In the form the patient(s) has/have given his/her/their consent for his/her/their images and other clinical information to be reported in the journal. The patients understand that their names and initials will not be published and due efforts will be made to conceal their identity, but anonymity cannot be guaranteed.
Financial support and sponsorship
The authors would like to thank Sebastian Nummelin (Bio Gaia, Stockholm, Sweden) for supplying the probiotic gums for this trial.
Conflicts of interest
There are no conflicts of interest.
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[Table 1], [Table 2], [Table 3]
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