Pediatrics International (2003) 45, 719723

Original Article

Effect of tongue brushing on oral malodor in adolescents

YASIN IEK,1 RECEP ORBAK,1 ADNAN TEZEL,1 ZERRIN ORBAK2 AND KAMILE ERCIYAS1 Departments of 1Periodontology and 2Pediatrics, Faculty of Dentistry and Medicine, Atatrk University, Erzurum, Turkey
Abstract Background: Halitosis is a common problem in humans, and is a social and psychological handicap for those affected by it. Halitosis has a positive correlation with the accumulation of bacterial plaque in the oral cavity. Aims: The aim of the present study was to determine the effect of tongue brushing on oral malodor in adolescents. Methods: The subjects of the investigation were 28 adolescents who had oral malodor and whose average age was 16 0.12 years. Subjects were chosen to participate in the study if they had an established routine of oral care, and did not have systemic or periodontal disease or dentures (such as fixed prosthesis or partial and total dentures). The subjects with oral malodor were randomly assigned into two groups. Individuals in the first group received instructions regarding professional procedures of oral care from a periodontist. In addition, individuals in this group had the surface of their tongue cleaned using a hard toothbrush, wetted with 0.12% chlorhexidine gluconate. Individuals in the second group (control) underwent the same professional procedures of oral care executed by the same periodontist, however, they did not have their tongues cleaned. Oral malodor of individuals was then evaluated for all individuals using the organoleptic method. The pH of the subjects tongues were recorded before and after treatment. The results of the oral malodor test were compared between the two groups. Results: The results of the study found that oral malodor scores obtained by an organoleptic method was more severe in the second group than the first group, and statistical differences were found between the two groups (P < 0.001). Conclusion: These results revealed that accumulation of bacterial plaque on the tongue is an important factor for oral malodor in the adolescents. Oral malodor levels were significantly reduced after cleaning the surface of the tongue. Thus, tongue care shouldnt be neglected in order to avoid oral malodor. diagnosis, etiology, oral malodor, tongue, treatment. the anterior of the tongue dorsum; odor from the posterior of the tongue dorsum; nasal odor; denture odor and smokers odor.5 When considering this classification system, it is obvious that the tongue is an important factor in oral malodor. Although the mechanisms of bad oral breath, the influence of the periodontal situation on bad oral breath, and the effect of halitosis on social and psychologic development in humans have been widely discussed, we could not find any published literature about the effect of tongue brushing on halitosis in adolescents.1,612 The purpose of this study was to evaluate the effects of tongue brushing on halitosis in adolescents.

Key words

Bad oral breath is usually called halitosis, but it is more convenient that such malodors originating from the oral cavity are called oral malodor.1,2 Whichever name is used, bad oral breath is a social and psychological handicap for affected individuals.1 This condition is of particular concern in adolescents, as adolescence is a critical period for psychologic development.3,4 Halitosis is a common complaint that periodically affects most people.5 Although halitosis has a multifactorial etiology, localized factors play the major role in most cases and 90% of oral odor originates from oral sources. The study of Rosenberg and McCulloch divided oral malodors into six groups: odor typical of subgingival putrefaction; odor from
Correspondence: Recep Orbak, Atatrk niversitesi, Dis Hekimligi Fak, Periodontoloji Anabilim Dali, 25240, Erzurum/Turkey. Email: receporbak@yahoo.com Received 19 September 2002; revised 29 March 2003; accepted 11 April 2003.

Methods
Study population

A total of 40 adolescents aged 1217 years, who had presented to the Periodontology Department of Atatrk University

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Faculty of Dentistry with bad oral breath complaints were examined. Twelve subjects were excluded from the study for various reasons, and the investigation was carried out in 28 adolescent subjects with halitosis. All subjects signed consent forms prior to commencement of the study. The adolescent subjects with bad oral breath were randomly assigned into two equal groups using the envelope method. Individuals in the first group received professional procedures of oral care administered by a periodontist. In addition, individuals in this group had the surface of their tongue cleaned using a hard toothbrush wetted with 0.12% chlorhexidine gluconate (CHX). Individuals in the second group (control) received the same professional procedures of oral care executed by the same periodontist, however, they did not have their tongues cleaned. All subjects were of similar age, sex, socioeconomic and socio-cultural background, and did not suffer from an oral or systemic disease apart from oral malodor. The occlusal adaptation conditions, such as open bite on anterior teeth, tongue thrust, lip biting, occupation-related peculiarities (for example, holding nails or pins between the teeth) and tipping of adjacent teeth into an extraction site resulting in occlusal imbalances were considered. Individuals who had any of the following criteria were excluded: use of a drug to affect the mouth flora (for example, use of mouth wash or rinse); a periodontal treatment or systematic oral care procedures in the 6 months prior to the assessment; use of an oral prosthesis (such as fixed prosthesis or partial and full dentures); presence of fillings in teeth; having caries in teeth.

Fig. 1 Distribution of times at which patients had halitosis.

Oral malodor measurements

Study Design

Subjects and parents were informed about the study, and were required to fill out a consent form and a medical history questionnaire. Subjects were asked to refrain from oral activities including eating (especially onion and garlic), drinking (especially alcohol), chewing, brushing, and mouth rinsing for 2 h prior to each appointment. Subjects were also asked not to use commercial mouthwash for 1 day prior to their appointment. All subjects were evaluated at the first appointment in order to establish their baseline measurements. After the subjects had conducted their own oral care for 4 weeks, the measurements were taken again. Measurements from the second appointment were compared with those from the first appointment. Subjects were assessed by one of two evaluators who had been calibrated previously for organoleptic and clinical measurements over a period of several clinical sessions prior to the study. To evaluate any differences in assessment, each evaluator examined the same subjects independently over several clinical appointments and the results were compared and the examiners calibrated.

Subjects were asked to complete a questionnaire regarding their usual diet (such as consumption of alcohol, onion and garlic) and general health (such as dehydration, diabetes, disease of digestive organs). Halitosis was then examined in order to determine whether or not the halitosis originated from an oral source, using the organoleptic method described in the study of Rosenberg.10 In this organoleptic evaluation, the examiner is positioned 10 cm from the subject, and instructs the subject to keep his/her mouth closed for a period of 2 min and to breathe through his/her nose. If the odor emanated from the nose while the mouth was closed, the odor was accepted as existing for systemic reasons and the patient was excluded from the study. Individuals were included in the study if the odor was only present when the mouth was open. The measurements were taken in the Department of Periodontology, Atatrk University. The oral malodor scores were recorded by the organoleptic methods.10 The results of the organoleptic method were scored on a scale of 05 as follows: 0, no odor; 1, barely noticeable odor; 2, slight but clearly noticeable odor; 3, moderate odor; 4, strong odor; 5, Extremely foul odor. In addition, each patient was measured for halitosis at a range of times throughout the day, and whether halitosis was present in the morning, night, or every hour was recorded (Fig. 1).
Clinical evaluation

Clinical evaluation of oral hygiene status was performed before and after treatment, using the plaque index, the gingival index, and saliva pH of patients was determined with litmus indicator paper.13,14 Plaque index scores were recorded on four tooth surfaces (mesial, distal, buccal, and lingual) and the quantity of supragingival plaque was assessed at the cervical area of every tooth.

Tongue brushing and oral malodor

Table 1 Numerical scale indicating degree of improvement of halitosis in adolescents Decrease in degree of halitosis 5 0 5 4 5 5 4 0 4 3 4 4 3 0 3 2 3 3 2 0 2 1 2 2 1 0 1 1

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Evaluation Full improvement Slight improvement No improvement

Table 2

Statistical analysis of halitosis scores obtained after oral care procedures in both groups First group n Total relief (%) 9 (64.3) 4 (28.6) 1 (7.1) n 14 14 14 Second group Total relief (%) 1 (7.1) 3 (21.4) 10 (71.5) Z Value 3.16* 0.43 3.48*

Level of improvement

Full improvement Little improvement No improvement *P < 0.001

14 14 14

The scores for the plaque index were defined as follows: 0, no plaque in the gingival area; 1, a film of plaque adhering to the free gingival margin and adjacent area of the tooth, the plaque can be recognized only by running a probe across the tooth surface; 2, moderate accumulation of soft deposits within the gingival pocket and on the gingival margin and/or adjacent tooth surface that can be seen by the naked eye; 3, abundance of soft matter within the gingival pocket and/or on the gingival margin and adjacent tooth surface. The gingival index was recorded for the mesial, distal, buccal and lingual surfaces with a manual periodontal probe (Williams periodontal probe, Hu-Friedy, Michigan, USA) for the area adjacent to every tooth. Bleeding was recorded if it occurred within 30 s of probing. The scores for the gingival index were defined as follows: 0, normal gingival; 1, mild inflammation, slight change in color, slight edema no bleeding on palpation; 2, moderate inflammation, redness, edema and glazing, bleeding on probing; 3, severe inflammation, marked redness and edema, ulceration, tendency to spontaneous bleeding. The numerical scores of the plaque and gingival indexes were obtained according to the formula: Per person = sum of individual scores/number of teeth present for each person. and a group score was subsequently calculated by adding together the individual scores and dividing the total into the number of patients included.
Treatment procedures

instruction and were monitored for 4 weeks by a periodontist (YC) for maintenance of adequate oral hygiene. Adolescents in the first group were taught how to brush their teeth correctly (at least twice a day), and how to clean the surface of tongue using a hard toothbrush wetted with CHX. Adolescents in this group were informed about the importance of cleaning the surface of tongue for protection against oral malodor. Adolescents in the second group (control group) received the same oral hygiene instructions except for the tongue cleaning procedures, from the same experienced periodontist.
Statistical analysis

The test for the difference between the two populations was used for statistical analysis. In addition, the two groups were compared using the Students t-test.

Results
The investigation was carried out in 28 adolescent subjects with oral malodor. Group I consisted of 14 patients with oral malodor (six females, nine males), with a mean age of 16 0.14 years; group II consisted of 14 patients with oral malodor (seven females, seven males), with a mean age of 16 0.11 years. The distribution of times at which patients exhibited oral malodor is shown in Figure 1. Oral malodor was mostly detected in the morning (76.80%). Improvements in numerical evaluations are shown in Table 1; the distribution of subjective improvement is shown in Table 2. After 4 weeks of self-administered oral care, the type of improvement experienced by each subject was investigated. Full improvement in the first group was observed in 64.3% of subjects, and in the second group full improvement was observed in 7.1% of subjects. The rate of full improvement

Subjects were selected from individuals who followed routine oral care procedures, did not have systemic and periodontal disease, and did not have dentures (fixed prosthesis or partial and full dentures). Therefore, treatment for the prevention of oral malodor was mostly based on providing oral hygiene education to subjects and their families. All patients received

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Comparison of plaque index and gingival index values obtained before and after treatment in both groups First group Plaque index (mean SD) Gingival index (mean SD) 0.85 0.39 0.84 0.37 >0.05 Plaque index (mean SD) 0.92 0.23 0.88 0.25 >0.05 Second group Gingival index (mean SD) 0.86 0.38 0.82 0.31 >0.05

Table 3 Phases

Before treatment After treatment P

0.93 0.23 0.89 0.19 >0.05

Table 4 The pH values of the tongue before and after treatment according to the litmus indicator method First group n Before treatment After treatment 14 14 Mean SD 7.6 0.12 7.5 0.16 Second group Mean SD 7.6 0.12 7.5 0.18 P >0.05 >0.05

was higher in the first group than in the second group, and statistical differences were found to be significant between the groups (P < 0.001). The clinical evaluation of oral hygiene status and statistical comparisons are shown in Table 3. According to the mean gingival index, no significant relationship was found between before and after systematic oral care in the two groups (P > 0.05); the same relationship was observed using the plaque index (P > 0.05). However, it was determined that tongue brushing reduced the pH of the tongue more than brushing teeth alone; however, this was not found to be statistically significant (P > 0.05) (Table 4).

Discussion
The effects of tongue brushing on oral malodor in adolescents were evaluated using organoleptic measurements and clinical findings. Volatile compounds come into existence as a result of food putrefaction, mostly in the form of gram-negative bacteria. These compounds are divided into two groups: volatile sulfur compound (VSC) such as hydrogen sulfide, methyl mercaptan, dimethyl sulfide; and volatile organic compounds (VOC) such as ethyl alcohol, acetaldehyde and acetone. These compounds are indicators of odor in the breath and 90% of these compounds make up hydrogen sulfate and methyl mercaptan.15 There are two main methods used in the evaluation of halitosis: subjective evaluation (organoleptic), and objective evaluation (quantitative measure of VSC, gas chromatography and monitor analysis).13 While most researchers use a combination of both methods, some researchers prefer the objective method in order to obtain a numeric value.5,15

However, some researchers use only the organoleptic method because it is economical and easier to perform.10 We used subjective evaluation in our study because of these advantages. Hunger and morning breath are causes of temporary oral malodor. The study of Morita and Wang reported that this state is the result of stagnation of epithelial and food debris.16 We evaluated the degree of oral malodor in subjects at a range of times, in order to investigate whether the time of day affected the degree of oral malodor. Oral malodor was most often present in subjects in the morning; it is therefore likely that the primary cause of this odor is oral dryness which occurs during sleep. This finding is consistent with other studies indicating that oral dryness is an important source of oral malodor.17,18 The influence of gingivitis and periodontitis on the risk of developing oral malodor has been the subject of much discussion in the literature. According to a majority of authors, individuals suffering from periodontal disease are at increased risk for the development of oral malodor.2,6,19 There is, however, a small group of researchers who did not find an increased risk.11 Currently, the most widely accepted theory is that the influence of gingivitis and periodontitis on oral malodor is high. Therefore, the present study was carried out in periodontally healthy adolescent subjects, in order to isolate the effects of the tongue on oral malodor. According to a majority of authors, oral malodor is more closely associated with tongue coating than with the severity of periodontal disease.11,20 This is attributed to the large surface area of the tongue which enables the accumulation of food and debris, the presence of bacteria and many microorganisms, and the presence of desquamated epithelial cells and dead leukocytes.1,2,17,21,22 The results of the present study indicated that accumulation of bacterial plaque on the surface of the tongue contributed to oral malodor, which further supports the theory that microbial accumulation often contributes to malodor production.20 The role of specific bacteria found on the tongue surface in malodor production has not been fully elucidated. However, the study of Rosenberg found that certain microorganisms (such as Treponema Denticola, Porphyromonas gingivalis and Bacteroides forsythus) that are commonly present in the tongue dorsum cause oral malodor.10 In the study of Yaegaki and Sanada, it was found that 60% of VSC were produced on the tongue surface.21

Tongue brushing and oral malodor

There are no accepted standards of care for treating oral malodor, and clinical protocols for the diagnosis and treatment of this problem vary widely. However, before commencing treatment, a clinician must determine the source of the malodor.16 The simplest way to distinguish an oral from nonoral origin is to compare the smell emanating from mouth and nose.10 If the origin is from nasal passages, or if the patient has a potentially related medical etiology, they must be referred to a physician for further evaluation and treatment.16 Effective methods for treating malodor reduce anaerobes by improving oral hygiene and periodontal health through basic dental care.22 Therefore, in our study all patients were instructed in oral care and monitored for 4 weeks by a periodontist, to ensure maintenance of adequate oral hygiene. When a patients conventional hygiene is adequate but an oral malodor problem exists, tongue brushing is often an effective form of treatment.23 The study of Tonzetich and Ng reported that tongue brushing is twice as effective as tooth brushing in reducing oral malodor.22 In our study, oral malodor scores obtained using the organoleptic method were higher, and thus oral mlodor was more severe in the second group than the first group, and statistical differences were found between the groups (P < 0.001). The first group in our study performed mechanical cleaning of the tongue using a hard tooth brush wetted with CHX 0.2%. If the patients still suffer from oral malodor after maintaining good oral hygiene, rinsing or gargling with an effective mouthwash might be advised.16 One method of treating periodontal patients with oral malodor is to use a combination of regular periodontal treatment and a chlorhexidine mouth rinse.11 The purpose of tooth brushing and oral antiseptic is to reduce the number of oral microorganisms present and to eliminate food debris.6,24 In the study carried out by Tonzetich, it was determined that halitosis could be reduced by using tooth brushing, tongue brushing, the combination of tooth and tongue brushing, and the use of antiseptic oral rinse after meals. Antiseptic rinses have also been used to remove halitosis.1 It is known that antiseptic rinses have an important effect on the qualitative and quantitative structure of microorganisms.10 The accumulation of bacterial plaque on the tongue is an important factor contributing to oral malodor in adolescents. Oral malodor levels were significantly reduced after cleaning the surface of the tongue. Thus, tongue care shouldnt be neglected in avoidance of oral malodor. Tongue brushing should be a part of daily home oral hygiene procedures.

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References
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