Effect of Chlorhexidine and Probiotics on Halitosis.

OBJECTIVE: The purpose of this study was to analyze the effect of chemical method of oral hygiene practice, chlorhexidine (CHX) disinfection, and the followed consumption of probiotics on oral malodor in children. The effects of chemical and mechanical oral hygiene practice methods on the intensity of oral malodor were also evaluated.
MATERIALS AND METHODS: Organoleptic test (OLT) scores of 2 or more of 196 children were randomly allocated to four groups: 1: Conventional oral hygiene practices (COH) including flossing and tooth brushing, 2: COH + tongue scraping (TS), 3: COH + TS + CHX, and 4: COH + TS + CHX + probiotics. OLT was performed at 1-week and 3-month follow-ups.
RESULTS: A stable and significant number of individuals showed crucial and average levels of improvement in Group 4 OLT scores. The improvement of Group 3 OLT scores was also remarkable but not steady over the follow-ups. Neither remarkable nor steady improvements in the OLT scores was detected in Groups 1 and 2 through follow-ups.
CONCLUSION: Oral disinfection followed by probiotic therapy with CHX may decrease the severity of oral malodor over a long period of time. Copyright:

INTRODUCTION

Halitosis or oral malodor is any unpleasant odor from the mouth. Ninety percent of oral bad smell originates from the mouth itself. Several intraoral and extraoral factors causes imbalance of the normal microflora of the tongue, saliva, and periodontal pockets.[1] Many strategies have been developed for the reduction of halitosis.[2] These protocols typically require physical or chemical methods to be carried out on a daily basis. However, these can provide only short-term benefits.

Probiotics consist of live microbial dietary supplement which improves the intestinal microbial harmony of the host.[3] Therefore, it has a beneficial effect on the host as well as in the reduction of halitosis. Probiotics are also used in the treatment of gingivitis and periodontal disease and has an cariostatic effect by the inhibition of Streptococcus mutans. They work based on how they fight with pathogenic microorganisms for adhesion sites such as biofilm or dental plaque and to antagonize these microbes.[4]

Numerous studies were conducted to change bacteria responsible for malodor with probiotic bacteria such as Streptococcus salivarius, Lactobacillus salivarius, or Weissella cibaria.[56] The main purpose is to stop reestablishment of undesirable bacteria and hence preventing the mouth malodor. A research reported that the consumption of gum or lozenges containing S. salivarius causes the low levels of volatile sulfur compounds. However, these protocols can lead to recurrence of malodor.[7] Probiotic strains after exposure to an antimicrobial agent can cause long-lasting effect. Chlorhexidine (CHX) has an bactericidal effect on Gram-negative and Gram-positive microorganisms and hence widely used as chemical plaque control.[8]

The present study aims to find the effects of prophylactic use of CHX and subsequent use of probiotics on halitosis in children. The principle of competitive exclusion was the basis of the study design. The use of different mechanical and chemical methods of oral hygiene practices on oral malodor and comparing it with the effect of probiotic strains forms the focus of the study. The four sets of variables were analyzed to find out how mechanical or chemical oral hygiene practices along with the introduction of probiotic bacteria affect oral malodor in children. They were:

Decayed, Missing and Filled Teeth/decayed, missing and filled teeth (DMFT/dmft)

Mechanical and chemical oral hygiene practices

Mechanical and chemical oral hygiene practices + consumption of S. salivarius probiotics

Oral malodor, in addition to parental satisfaction about the treatment results.

A marked alteration in the balance between oral microflora and probiotic strains along with mechanical plaque control methods can lead to the removal of inherent pathogenic bacteria and increase in persistent colonization with probiotic strains and thereby the treatment of oral malodor.[910]

MATERIALS AND METHODS

Participants

A randomized clinical trial was conducted by selecting 290 children for the study period whose parents were reported decrease of oral malodor. A comprehensive medical and dental history was taken, and a treatment plan is decided for each patient.

Eligibility criteria

Children with no gingivitis and periodontal disease and no previous orthodontic therapy

No systemic conditions or developmental disturbances associated with oral malodor such as diabetes mellitus, renal disease, GI disorders, respiratory disease, chronic sinusitis, and local or systemic conditions affecting the quantity and quality of saliva

Not using medications affecting the quantity and quality of saliva for the past 6 months

Absence of habitual mouth breathing

No previous intake of probiotic products.

Subject recruitment

During the first visit, all the methodology and objectives were explained, and consent was obtained from the parents. It consists of two consecutive phases. In the first phase, 290 children were selected within the age group of 6–9 years who reported with halitosis. Organoleptic test (OLT) was conducted, and participants having score of two or more were selected after which all dental treatments such as restorations, pulp treatment, and extractions were performed. The second phase included 196 participants who completed their dental treatments and had an OLT score of 2 and above.

Study group and intervention

After the first phase, participants with OLT score of 2 and above were divided into four groups, with 49 members in each group.

Group 1 included conventional hygiene methods + tooth brushing + flossing

Group 2 consists of conventional oral hygiene (COH) + tooth brushing + flossing + tongue scraping (TS)

Group 3 consists of COH + tooth brushing + flossing + TS + CHX

Group 4 consists of COH + tooth brushing + flossing + TS + CHX + probiotics

Probiotic lozenge consists of 1 × 10

colony-forming units of S. salivarius. Tooth brushing was not allowed for at least 1 h after lozenge consumption for 2 weeks.

Oral malodor assessment

The OLT is the simplest gold standard method of oral malodor measurement.[811] The participants were asked to not to eat, drink, chew gum, smoke, brush, or rinse mouth for at least 5 h. Each participants asked to exhale through mouth with a distance of 9 cm from investigator, and scores were recorded 0–5 [Table 1].

Table 1

Organoleptic test score

Score	Description
0	Absence of odor
1	Questionable odor
2	Slight malodor
3	Moderate malodor
4	Strong malodor
5	Severe malodor

Two examiners with no history of chronic asthma or allergy and had a previous experience in the assessment were selected. On the day of examination, both examiners were restricted from having tea, coffee, smoking, and other cosmetic sprays. The measurements were carried out at 1 week and 3 months [Figure 1] after which satisfaction of parents were assessed through questionnaire like where you satisfied with the treatment of your child and parents were asked to rate their assessment with points like 1 (not satisfied), 2 (moderately satisfied), and 3 (complete satisfaction).

Figure 1

Flow chart of the participants

RESULTS

Out of 196 participants, 80 were female and 116 were male. They were grouped into four. Out of which, 8 were removed, because they did not cooperate. The baseline characteristics are shown in Table 2. OLT scores increased with the increase in DMFT/dmft levels, but these did not seem statistically significant [Table 3].

Table 2

Study sample - baseline characteristics

	Group 1 (n=46)	Group 2 (n=47)	Group 3 (n=48)	Group 4 (n=47)
Age	7.51±1.01	7.43±1.10	7.52±1.18	7.43±1.12
OLT score	3.01±0.13	3.84±0.83	3.03±0.68	3.01±0.83

OLT: Organoleptic test

Table 3

Organoleptic test scores based on individuals caries experience Level of caries experience

	DMFT=0/caries free dmft	DMFT=1/low dmft	DMFT ≤3/moderate 2≤ dmft	DMFT ≥4/high dmft
OLT score	2.8±0.2	2.11±0.7	3.2±0.5	3.2±0.4

DMFT: Decayed, Missing and Filled Teeth, dmft: decayed, missing, and filled teeth

Group 1 – after the first and second phases of assessment, the OLT score shows no or slight improvement

Group 2 – after the first and second phases, no improvement was noticed

Group 3 – after the first phase of assessment, a significant improvement was seen but were not noticed after the second phase

Group 4 – after the first and second phases of assessment, a major to moderate levels of improvement in OLT score was seen.

DISCUSSION

S. salivarius has great credentials in being an oral probiotic as it is not likely to accord halitosis.[6] Growth of numerous strains of bacteria has shown to be inhibited by S. salivarius (K12). Above all, this bacterial strain is a pioneer in colonizing the oral cavity and is a predominant member of oral microflora in healthy individuals. Because of its ability to yield bacteriocin that can reduce the number of production of bacterial species, it is also called as commensal probiotic of the oral cavity. The growth of black-pigmented bacteria is found to be inhibited by S. salivarius K12 strain (in vitro).[12] The usage of lozenges or gum consisting of S. salivarius has been found to reduce volatile sulfur compound levels in patients with oral malodor.[313]

Table 4 depicts a predominant reduction in halitosis in Groups 3 and 4 compared to Groups 1 and 2 were found. Consumption of antimicrobial products in combination with improvement of oral hygiene practices prevents halitosis due to reduction in the bacterial population.[214] CHX is reckoned to be the gold standard and key agent for managing gingivitis and plaque.[15] The antibacterial activity is dependent upon the cationic molecule on to which negatively charged bacterial surfaces are attracted. Bacterial cell membrane integrity is modified after adsorption resulting in low dosage causing reversible leakage of bacterial low-molecular-weight compounds or higher doses causing intense membrane damage. Long-term consumption of CHX, however, corresponds with excessive calculus formation, extrinsic staining of tongue and teeth, alteration in taste, burning sensation, and oral mucosal irritation.[816]

Table 4

Organoleptic test score improvement in phase 1 and phase 2

Level of improvement	Group 1 (n=46)		Group 2 (n=47)		Group 3 (n=48)		Group 4 (n=47)
	Phase 1 (%)	Phase 2 (%)	Phase 1 (%)	Phase 2 (%)	Phase 1 (%)	Phase 2 (%)	Phase 1 (%)	Phase 2 (%)
Major	4 (8.7)	3 (6.5)	11 (23.4)	8 (17)	20 (41.7)	12 (25)	19 (40.4)	17 (36.2)
Moderate	6 (13)	5 (10.9)	14 (29.8)	12 (25.5)	11 (22.9)	10 (20.8)	14 (29.8)	17 (36.2)
Slight	19 (41.3)	23 (50)	10 (21.3)	15 (31.9)	15 (31.3)	14 (29.2)	12 (25.5)	11 (23.4)
No improvement	17 (37)	15 (32.6)	12 (25.5)	12 (25.5)	2 (4.2)	12 (25)	2 (4.3)	2 (4.3)

Even though the oral hygiene practice by chemical methods in Group 3 resulted in a prominent reduction halitosis score after the first follow-up session, oral malodor recurred at the second follow-up session confirming the prime concern of earlier studies on reducing halitosis with CHX. To the contrary, halitosis score in Group 4 did not indicate notable variation between the follow-ups. As a result, the outcome seen in Group IV verifies the hypothesis that oral disinfection followed by probiotic therapy could be a desired approach for the long-term management of oral malodor.

Competitive exclusion principle supporting the growth of probiotics followed by the suppression of oral bacteria by using CHX seems to account to this finding. In point of fact, based on the concept of competitive exclusion, easy colonization with probiotic strain is made possible with decrease in oral microbial numbers.[917] Oral malodor was primarily improved by probiotic lactobacilli being administered orally.[4] The results obtained agree with the same. Nevertheless, due to short follow-up period and less participants, a suggestion was made to further work to enhance the stability and preserve the activity of L. salivarius in the complex oral microbiota.

Improvement in Group 2 was seen when compared to Group 1 as halitosis particularly arises from the resident microbes mainly anaerobic ecosystem situated on the dorsum of the tongue. Papillary structure of the dorsum of the tongue offers a huge surface area that aids in the accumulation of plaque and microorganisms.[2]

OLT scores stated by the various levels of DMFT/dmft did not vary significantly, although the outcome of the primary phase of study exhibited an association between DMFT/dmft and oral malodor. Evirgen et al. suggested that there is no remarkable association between DMFT/dmft and oral malodor. Young children with halitosis were reported to be caries free, whereas age-matched children with halitosis were found to have moderate-to-severe caries activity.[9] Conversely, the results may be due to the reason that the etiology of periodontal disease, caries and halitosis is usually associated with the accumulation of bacteria and composition of plaque.[11]

Porphyromonas sp. and Lactobacillus sp. that cause caries have found to be responsible for causing halitosis.[211] Recent studies show that an increase in pH and buffering capacity of saliva and decrease in viscosity of saliva is linearly proportional to the number of excluded carious surfaces of teeth.[18] Henceforth, it seems rational to presume that decrease in the accumulation of carbohydrate and plaque removal, viscosity of saliva, increased buffering capacity, and pH result in eradication of cariogenic microorganisms and caries and hence decreased halitosis.[19]

Providing treatment with quality outcomes and patient satisfaction is the priority and supreme competitive lead in most health-care systems.[20] Hence, we evaluated the difference between the patient's satisfaction and health-care practitioners in the improvement of halitosis. A patient-oriented approach takes into consideration the patient's requirement, belief and assessment for the motive of quality improvement.

CONCLUSION

According to the current study, it is inferred that the first step in controlling oral malodor is the mechanical elimination of biofilm and microorganisms responsible for the same. It is recommended that TS as a major mechanical measure to prevent malodor. Chemical methods can be used as an adjunct in eradicating biofilm. Based on the current results, oral disinfection followed by probiotic therapy is found to alter the oral microbiota and surpass malodor.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.