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J Dent Res 82(7): 518-522, 2003
© 2003 International and American Associations for Dental Research

RESEARCH REPORT
Clinical

Reliability of Clinical Parameters for Predicting the Outcome of Oral Malodor Treatment

M. Tanaka, H. Anguri, N. Nishida, M. Ojima, H. Nagata, and S. Shizukuishi*

Department of Preventive Dentistry, Graduate School of Dentistry, Osaka University, 1-8, Yamadaoka, Suita, Osaka 565-0871, Japan;

*corresponding author, shizuku{at}dent.osaka-u.ac.jp


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 SUBJECTS & METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
We conducted the present study to determine which clinical parameters for diagnosing halitosis are most reliable in the development of an accurate prognosis for oral malodor treatment. Clinical evaluation included a questionnaire, oral examination and volatile sulfur compounds (VSC) measurement, and organoleptic test (OLT) at baseline. Ninety-two patients classified with oral pathologic halitosis were treated in a similar manner. Improved treatment outcome was defined as < 0.25 ppm of total VSC, ≤ 2 OLT score, and < 30 on the "sad feeling" scale as subjective stress level by oral malodor 6 months after baseline. Thirty-four patients demonstrated improvement due to the treatment. In a multiple logistic model, pocket depth, OLT score, intra-oral discomfort, and self-perception of oral malodor at baseline displayed significant association with "not improved outcome". These results suggest that malodor- and periodontal-disease-related parameters and self-estimation of malodor at baseline are effective for prediction of outcome.

KEY WORDS: oral malodor • treatment outcome • prognosis • clinical parameters


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
SUBJECTS & METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Most oral malodor originates within the oral cavity itself (Delanghe et al., 1999), primarily as a result of microbial metabolism, in which volatile sulfur compounds (VSC) and other volatile compounds are produced through deglycosylation, proteolysis, and putrefaction of glycoproteins and proteins (Scully et al., 1997; Sterer et al., 2002). Furthermore, cleaning of the teeth and tongue (Tonzetich and Ng, 1976), rinsing with mouthwash, and periodontal therapy (Quirynen et al., 1998) can control oral malodor. However, it has also been reported that these treatments are often deemed unsuccessful by patients who are extremely sensitive to and often delusional about the behavior of others toward their imagined oral malodor and who suffer from oral malodor with accompanying psychosomatic tendencies (Yaegaki and Coil, 1999). Patients displaying psychosomatic halitosis may continue to complain about oral malodor despite the reduction or elimination of their oral malodor following treatment. Therefore, the practitioner must consider many factors regarding oral hygiene, dentition, and systemic and mental status of patients before arriving at an accurate prognosis for oral malodor treatment.

For halitosis to be diagnosed, oral malodor can be measured with the organoleptic test (OLT) and/or gas chromatography; moreover, additional information can be obtained from a questionnaire regarding patient history of halitosis and symptoms. Recently, based on this information, halitosis has been classified into categories of genuine halitosis, pseudo-halitosis, and halitophobia. Genuine halitosis is sub-classified into physiologic halitosis and pathologic halitosis (Miyazaki et al., 1999; Yaegaki and Coil, 2000). However, it is unclear whether this simple classification can establish the appropriate management of patients with halitosis. Assignment of prognosis may be one of the most important functions undertaken in oral malodor treatment (Newman et al., 1994). The purpose of the present investigation was to determine which clinical parameters with respect to diagnosis of halitosis are most reliable in the development of an accurate prognosis for oral malodor treatment.


   SUBJECTS & METHODS
TOP
 ABSTRACT
 INTRODUCTION
 SUBJECTS & METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Subjects and Study Design
Between April, 1999, and October, 1999, 156 patients complaining of oral malodor visited the Oral Malodor Clinic at Osaka University Dental Hospital. At the initial visit, chief complaint and brief systemic and dental histories were obtained from patients. Preliminary oral examinations were also conducted. During the second visit, bad breath history, medical history related to bad breath, and psychosocial history, including the Cornell Medical Index Health Questionnaire (Lowe, 1975), were obtained by direct interview. Extra-oral, intra-oral, and periodontal examinations were performed. At the time of the third visit, bad breath was assessed via VSC measurement with gas chromatography and OLT. Patients were diagnosed according to the clinical classification with corresponding treatment needs, as developed at the Niigata Workshop in 1998 (Miyazaki et al., 1999). Permission for this study was obtained from the Ethical Committee for Clinical Research of Osaka University Graduate School of Dentistry.

One hundred one patients who were classified with oral pathologic halitosis of ≥ 0.25 ppm of total VSC level and/or ≥ 3 OLT score and the presence of periodontal pockets of ≥ 4 mm and/or tongue-coating scores of > 3 and who were treated on more than 4 occasions within 6 mos were selected for this investigation. Informed consent was obtained from all subjects. Within this period, nine patients did not return after their appointment. The subject population was comprised of 15 males and 77 females aged 17-76 yrs. The mean age of patients was 44.9 yrs. Mean frequency of visits was 7.5 times, and mean period between visits was 7.2 mos. At the initial 3 visits, we attempted to establish rapport with halitosis patients through the examinations, the questionnaire, and malodor measurement. Subsequently, patients were treated in a similar manner with respect to oral hygiene instruction, tongue cleaning, and periodontal treatment. During the treatment, patients were informed regarding improvement in their oral health status. One of three dentists examined and treated the same patients from the second to the final visits. Improved outcome of oral malodor treatment was defined as < 0.25 ppm of total VSC, ≤ 2 OLT score, and < 30 on the "sad feeling" scale by oral malodor 6 mos after the initial visit.

Questionnaire
Patients completed a questionnaire involving a "sad feeling" scale, intra-oral discomfort, and self-perception for malodor. A "sad feeling" scale, which was assessed as subjective mental stress by oral malodor and which was derived based on a single-item response, was scored on a scale of 0-100 by the modified method of Aitken (1969). This subjective stress level was separated into a "high or middle" levels with ≥ 30 and a "low" level with < 30 "sad feeling" scale as above or below the lower 10th percentile of the distribution (Orr et al., 2002). In addition, the Cornell Medical Index at baseline was utilized. This questionnaire contains simply worded questions that cover a broad range in terms of somatic and emotional status of subjects; each question can be answered "yes" or "no". Patients were divided into 4 categories (scale, 1-4) based on whether subjects exhibited a tendency toward neurosis.

Malodor Assessment
Prior to the appointment for odor assessment, patients were asked to refrain from oral activities, including eating, drinking, and chewing, for 4 hrs, and from brushing and mouthrinsing for one half-day. For OLT, patients remained quiet and maintained a closed mouth for a period of 30 sec. Subjects were then requested to exhale through the mouth with moderate force into a sampling bag (GL Science Inc., Tokyo, Japan) for 2 to 3 sec to prevent the dilution of odor with lung and room air. This procedure was repeated three or four times. Three evaluators, who were trained to perform an examination standardized by the Japan Bureau of Environmental Health, estimated the odor at a distance of approximately 10 cm from the sampling bag (Shimura et al., 1997). OLT scores were estimated on a scale of 0 to 5, and the mean values of the three judges were used. The percentage of agreement in OLT scores among the three examiners always exceeded 71% ({kappa} = 0.77; Aickin, 1990).

VSC level was analyzed with a Shimadzu GC-14B gas chromatograph (Shimadzu Ltd., Kyoto, Japan) equipped with a flame photometric detector system (Oho et al., 2001). Mouth air (10 mL) was aspirated with a gas-tight syringe; subsequently, samples were injected onto the gas chromatograph column at 70°C. A glass column was packed with 25% ßß-oxydipropionitrile on a 60- to 80-mesh Chromosorb W AW-DMCS-ST support system (Shimadzu Ltd.); the glass was treated with phosphoric acid. The concentration of each sulfur compound was determined with standard gas of hydrogen sulfide, methylmercaptan, or dimethyl sulfide prepared with a PD-1B permeater (Gastec Co., Ltd., Kanagawa, Japan). The level of VSC was defined as ppm of the total concentrations of hydrogen sulfide, methylmercaptan, and dimethyl sulfide.

Periodontal and Dental Examinations
Periodontal pocket depth (PPD) was measured at two points on each tooth within the patient’s mouth. Periodontal status was evaluated as percentage of teeth characterized by ≥ 4 mm of PPD. Plaque control record (O’Leary et al., 1972) was used for the determination of oral hygiene status. We calculated the tongue-coating score by multiplying the thickness score by the area score (Oho et al., 2001). The area was reported as a score of 0 to 3 (0, no tongue coating; 1, tongue coating covering less than 1/3 of tongue dorsum; 2, tongue coating covering 1/3 ~ 2/3 of tongue dorsum; and 3, tongue coating covering greater than 2/3 of tongue dorsum). Thickness was reported as a score of 0 to 2 (0, no tongue coating; 1, thin coating with tongue papillae visible; 2, moderate coating with tongue papillae invisible; and 3, thick tongue papillae invisible). The percentage of agreement in tongue-coating scores among the three examiners always exceeded 72% ({kappa} = 0.72).

Statistical Analysis
Data were analyzed with use of the Stat View for Macintosh ver. 5.0 (SAS Institute Inc., Cary, NC, USA). Relationships between malodor measurement and clinical indicators of oral health at the baseline were assessed by the Spearman signed-rank test. Changes in clinical data prior to and after malodor treatment were examined by means of a paired t test or Wilcoxon rank-sum test. Association between clinical parameters at baseline and outcome of oral malodor treatment was evaluated by bivariate analyses with the Wilcoxon rank-sum test, Chi-square test, odds ratios, and their respective 95% confidence intervals. We used logistic regression analyses to determine which variables demonstrated significant independent effects on outcome of malodor treatment.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 SUBJECTS & METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
In the correlation analysis between malodor and oral health measurements at baseline (Table 1Go), total VSC level positively correlated with OLT and tongue-coating scores; the correlation coefficients were 0.53 and 0.32, respectively. OLT score also correlated positively with tongue-coating score. No significant correlation was evident between %PPD and the parameters of oral malodor. Additionally, no correlation was observed between the "sad feeling" scale and intra-oral discomfort or self-perception of oral malodor. In total, strong associations were not observed among these parameters.


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  		Table 1. Correlation Analysis between Malodor and Oral Health Measurements at Baseline (N = 92)
 
At baseline, mean total VSC was 0.57 ppm, and the range was 5.6 ppm. Following treatment, mean total VSC was 0.10 ppm, and the range was 1.1 ppm. Changes in VSC as a result of treatment were significantly different. Similar improvements were also observed in OLT score and "sad feeling" scale for oral malodor. Moreover, mean %PPD declined from 10.4 to 4.1 due to treatment. Plaque control record and tongue-coating score also decreased significantly. However, wide variation was evident in all clinical parameters (Table 2Go).


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  		Table 2. Changes in Mean Patient-based Clinical and Malodor Measurements before and after Treatments (N = 92)
 
Thirty-four patients displayed improvement in all parameters of total VSC, OLT score, and "sad feeling" scale for malodor. Forty-four subjects demonstrated no improvement on the "sad feeling" scale only; however, 14 patients failed to improve with respect to total VSC and/or OLT score. This result suggests that approximately half of patients with oral pathologic halitosis may be classified with psychosomatic halitosis. Consequently, 34 and 58 patients were defined as having improved and as not having improved, respectively.

Bivariate analyses were conducted between age, gender, and these initial clinical parameters and percentage of subjects failing to improve (Table 3Go). No significant association was evident between variables such as age, gender, smoking habit, the Cornell Medical Index, plaque control record, tongue-coating score, and percentage of subjects displaying no improvement following treatment. However, high scores of %PPD, total VSC, OLT score, "sad feeling" scale, intra-oral discomfort, and self-perception of malodor demonstrated a significantly higher percentage of subjects failing to improve. These odds ratios were 2.4, 4.7, 4.4, 3.2, 14.9, and 3.5, respectively.


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  		Table 3. Association between Initial Clinical Parameters and Treatment Outcome (N = 92)
 
Furthermore, the independent effects of variables exhibiting associations with treatment outcome were analyzed by multivariate logistic regression (Table 4Go). Significant variables in the logistic regression model were %PPD, OLT score, intra-oral discomfort, and self-perception of oral malodor. Odds ratios were 4.4, 4.3, 13.2, and 6.3, respectively. Intra-oral discomfort and self-perception of oral malodor tend to display higher odds ratio than did %PPD and OLT score. These results suggest that periodontal status and OLT score may be available for prediction of treatment outcome of malodor; moreover, self-perception related to malodor may also affect the prediction of outcome.


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  		Table 4. Multiple Logistic Regression Analysis of Initial Clinical Parameters and Treatment Outcome (N = 92)
 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 SUBJECTS & METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
If an accurate system is to be developed for the assignment of prognosis to oral malodor, the determination of not only oral health parameters, i.e., OLT score and PPD, but also initial self-estimation of malodor, such as intra-oral discomfort and self-perception of malodor, were deemed necessary. In this investigation, most of the patients were female. It appears likely that females tend to be more anxious with respect to bad breath in comparison with males (Oho et al., 2001). The participants consisted of patients classified with oral pathologic malodor by OLT score and total VSC levels measured via gas chromatography. A significant correlation was observed between OLT score and the total level of VSC as determined by gas chromatography (r = 0.53), when the data acquired from subjects with ≥ 0.25 ppm of total VSC level and/or ≥ 3 OLT score were analyzed. Several studies also demonstrated a significant correlation between OLT score and total VSC levels determined by gas chromatography testing (Schmidt et al., 1978; Niles and Gaffar, 1997; Oho et al., 2001). Significant correlation was apparent between the parameters of oral malodor and tongue coating. These results support the important role of tongue coating in VSC production (Yaegaki and Sanada, 1992; Miyazaki et al., 1995). No significant correlation was evident between %PPD and the parameters of oral malodor. Bosy et al. (1994) also reported that oral malodor did not associate with periodontitis. However, when subjects were divided into two groups with and without periodontal pockets (N = 71 and 21, respectively), patients exhibiting periodontal pockets revealed significantly higher OLT scores (mean 3.2, mean rank 50.7) and total VSC levels (0.64 ± 1.04 ppm) in comparison with those subjects lacking periodontal pockets (OLT score; mean 2.7, mean rank 32.4 and total VSC level; 0.19 ± 0.43 ppm) (p < 0.05).

Oral pathologic halitosis patients were selected in this investigation to achieve treatment in a similar manner with respect to oral hygiene instruction and periodontal treatment. Sixty-two percent of the study population displayed both PPD of ≥ 4 mm and tongue-coating scores of > 3. Patients presenting with either PPD of ≥ 4 mm or tongue-coating scores of > 3 were 15% and 23%, respectively. We attempted to establish rapport with halitosis patients through the examinations, the questionnaire, and malodor measurement during the initial three visits. These patients were treated in a nearly identical manner with respect to toothbrushing instruction, tongue-cleaning instruction, and professional tooth and tongue cleaning and scaling during a period of approximately 6 mos. During the treatment, patients were informed regarding improvement in their oral health status. Significant improvement was observed in mean patient-based clinical and malodor measurements such as PPD, plaque control record, tongue-coating score, total VSC level, and OLT score.

Few studies exist regarding improvement of patients with malodor by treatment. Quirynen et al. (1998) reported that the standard periodontal treatment of patients with severe periodontitis during a two-month period resulted in improvement in OLT score but not in VSC values measured by a portable sulfide monitor. This finding might be explained by involvement of non-sulfur gaseous compounds, deterioration of the sensor of VSC monitor (Rosenberg and McCulloch, 1992), and the measurement for only peak values in non-steady state (Furne et al., 2002). Delanghe et al.(1999) noted that 86% of malodor cases at a multi-disciplinary oral malodor clinic were caused by an oral problem. Self-reported results of treatment for oral malodor indicated that 42% of patients believed that they had been cured; however, 26% of respondents believed that there had been no improvement. It is difficult to compare the present data regarding improvement of malodor patients with data of other investigators, due to methodological differences; moreover, patient selection and treatment outcomes appear not to differ markedly from those reported in other findings.

No widely accepted definition of improvement by oral malodor treatment exists. Patients displaying < 0.25 ppm of total VSC level, ≤ 2 of OLT score, and < 30 on the "sad feeling" scale by oral malodor may be considered acceptable in terms of clinical improvement following treatment for approximately 6 mos. Tonzetich and Ng (1976) have demonstrated that the threshold of objectionability for CH3SH and H2S is 0.05 ppm and 0.15 ppm, respectively. Although the olfactory threshold of dimethyl sulfide is not clear, we considered the olfactory threshold levels of total VSC as 0.25 ppm. Moreover, a score of 2 on the OLT was the recognizable threshold; however, this level was not the detectable threshold. Improvement was defined as low-level with < 30, which was below the lower 10th percentile of the distribution on the "sad feeling" scale.

Significant variables in the logistic regression model were %PPD, OLT score, intra-oral discomfort, and self-perception of oral malodor. These results suggest that periodontal status and OLT score may be available for prediction of treatment outcome of malodor. Furthermore, patients with severe periodontitis and/or high OLT scores must be considered in terms of closer, more frequent treatment if treatment outcome is to be improved. Self-perception related to malodor may affect the prediction of outcome more strongly than it affects oral physiological status. Thus, patients’ mental health status must be examined if an accurate prognosis is to be arrived at, even for oral pathologic halitosis patients. Oral pathologic patients exhibiting psychosomatic tendencies might be positively treated via a psychological approach, including explanations, education, and counseling for oral malodor.


   ACKNOWLEDGMENTS
 
This work was supported by a Grant-in-Aid for Scientific Research from the Ministry of Education, Science, Sports, and Culture of Japan (No. 13557182).

Received August 26, 2002; Last revision April 7, 2003; Accepted April 17, 2003


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 ABSTRACT
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 SUBJECTS & METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
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