Abstract
Objective: To assess the psychosomatically subjective symptoms of subjects with neurotic tendencies complaining of halitosis. Design: Breath malodour was measured in 368 patients using organoleptic test and gas chromatography. Neurotic tendency and subjective symptoms were assessed using the Cornell Medical Index (CMI). Results: Of the 79 subjects who met the criteria for neurotic tendencies according to CMI scores, 58 (73.4%) had oral malodour, whereas 21 (26.6%) did not. Coated tongue, periodontal pocket, and daily drinking were significantly more common in subjects with oral malodour. On the CMI questionnaire, subjects with no oral malodour more frequently responded ‘yes’ to questions about fatigue and psychological problems in their families. Additionally, many answered that they had perceived their own bad breath. Conclusions: Difficulties experienced by subjects with neurotic tendencies and oral malodour may manifest primarily in oral conditions, whereas those experienced by individuals with neurotic tendencies and no oral malodour may manifest primarily in psychosomatic symptoms.
Key words: Cornell Medical Index, neurotic tendency, oral malodour, organoleptic test, psychosomatic status
INTRODUCTION
Oral malodour, also known as bad breath, is a common complaint among the general population and is primarily associated with conditions in the oral cavity, including oral hygiene status and periodontal condition1., 2.. It is mainly the result of the microbial metabolism of amino acids in local debris3. Many of the major compounds that contribute to oral malodour are volatile sulphur compounds (VSCs) such as hydrogen sulphide (H2S), methyl mercaptan (CH3SH), and dimethyl sulphide (CH3SCH3)4., 5.. VSC levels have typically been measured, and an organoleptic test (OLT) given, to evaluate the level of oral malodour in patients complaining of halitosis6.
Clinically, some patients who complain of halitosis have actual malodour, whereas others have almost no malodour. Diagnosis and treatment of halitosis involves a simple classification into the categories of genuine halitosis, pseudo halitosis, and halitophobia2., 7.. The treatment of genuine halitosis primarily involves periodontal treatment, dental and oral care, oral hygiene instructions, and counselling, whereas that of pseudo halitosis involves counselling that includes education and explanations of examination results showing that the intensity of the patient’s malodour is not beyond socially acceptable levels2., 7., 8.. Halitophobia is characterised by a patient’s persistent belief that he or she has halitosis despite reassurance, treatment, and counselling. Patients with halitophobia should be referred to medical specialists2., 7..
It has been suggested that halitosis is a symptom related to both somatic and emotional status and that psychological disorders are strongly associated with the condition in some patients9. According to previous studies, patients complaining of halitosis who have psychological disorders, namely halitophobia do not generally demonstrate oral malodour10. However, patients with oral malodour as well as those with no oral malodour might have an accompanying psychological condition2. Therefore, differential diagnosis of halitophobia versus pseudo halitosis or genuine halitosis toward psychological symptoms can be difficult at times for most dentists. We hypothesised that the psychosomatic histories and dynamics of subjects with and without oral malodour might differ. The present study focused on patients who complained of halitosis and showed psychological symptom according to the Cornell Medical Index (CMI) Health Questionnaire11 and investigated the relationship among the presence of oral malodour, clinical condition, and the psychosomatic subjective symptoms of the subjects. The questionnaire was created to collect a large body of pertinent medical and psychiatric data with a minimal time expenditure12 and is often employed to evaluate the psychosomatic aspect of halitosis patients13., 14., 15..
METHODS
Subjects and study design
The study population was composed of 146 males and 222 females (45.4 ± 14.6 years) who complained of halitosis and presented to the Oral Malodour Clinic of Fukuoka Dental College Medical and Dental Hospital, Japan, between June 2005 and December 2009. At the initial visit, chief complaints, brief systemic and dental histories, and living habits were obtained from the patients. At the second visit, each subject was asked to fill out the Japanese CMI11 to evaluate his or her psychosomatic aspects and neurotic tendencies. In addition, a malodour assessment and clinical examination were performed. All of the subjects who participated understood the nature of the research project and provided informed consent.
Malodour assessment
Before the appointment for malodour assessment, each subject was asked to refrain from eating, drinking, chewing, smoking, brushing, or rinsing the mouth for at least five hours. The severity of oral malodour in each individual was determined using an OLT and gas chromatography (model GC14B; Shimadzu Works, Kyoto, Japan). For the OLT, two of the three evaluators with training and experience in calibration tests estimated the odour at a distance of 10 cm from a sampling bag (GL Science, Tokyo, Japan) containing exhaled air from the patient. The OLT scores were estimated on a scale of 0 to 5 (0, absence of odour; 1, questionable odour; 2, slight malodour; 3, moderate malodour; 4, strong malodour; 5, severe malodour)2, and mean scores given by the different judges were used. The percentage agreement in the OLT scores were among the three evaluators always exceeded 75.0% (κ = 0.50). For the gas chromatographic measurements, the concentration of each VSC was determined based on the values for standard H2S, CH3SH, and CH3SCH3 gas prepared with a PD-1B permeater (GL Science). The level of total VSCs was defined as the total concentrations of H2S, CH3SH, and CH3SCH3. The threshold levels for genuine halitosis were defined as a ≥3 OLT score and/or ≥0.25 ppm total VSCs in mouth air by gas chromatography according to previous report15. A significant correlation was observed between OLT scores and the total levels of VSC as determined by gas chromatography (r = 0.62). The OLT score was given priority over the VSC levels for the evaluation of malodour. Eight patients, who scored 3 on the OLT and measured <0.25 ppm total VSC in mouth air, were judged as having genuine halitosis.
Clinical examinations
The oral health of each patient was evaluated based on the number of teeth, number of carious teeth, number of fillings, poor margins on restorations, mobility of the teeth, periodontal pocket depth (PPD), degree of tongue coating, volume of stimulated salivary flow and the presence of occult blood in the saliva. PPD was measured at six points around each tooth in all of the subjects. Each subject’s periodontal status was determined based on the presence of teeth with PPD ≥5 mm. The tongue coating score (TCS) was assessed based on conventional criteria, with simple modification: 0, no tongue coating; 1, thin and area <1/3; 2, thin and area = 1/3–2/3 or thick and area <1/3; 3, thin and area >2/3 or thick and area = 1/3–2/3; 4, thick and area >2/3)14., 16., 17.. The volume of stimulated salivary flow was measured using the chewing gum test14., 16., 17.. Testing for the presence of occult blood in the saliva was performed using Perioscreen (Sunstar, Osaka, Japan). Data about the presence of systemic illness, bad-breath history, smoking habits, and drinking habits were obtained by direct interview.
Questionnaire
The subjects’ psychosomatic characteristics and neurotic tendencies were evaluated using the Japanese CMI Health Questionnaire11. This questionnaire contains simply worded questions that cover a broad range of somatic and emotional statuses; all questions, totalling 211 for male and 213 for female subjects, are answered ‘yes’ or ‘no’. For the evaluation of somatic symptoms and habits, the CMI questionnaire asks about the condition of the eyes and ears (A), upper respiratory system (B), cardiovascular system (C), digestive tract (D), musculoskeletal system (E), skin (F), nervous system (G), genitourinary systems (H), fatigability (I), frequency of illness (J), miscellaneous diseases (K), and habits (L). For the evaluation of emotional status, questions concerning inadequacy (M), depression (N), anxiety (O), sensitivity (P), anger (Q), and tension (R) are included. Previous studies have reported that neurotic subjects obtain high scores on somatic questions, including those pertaining to the cardiovascular system (C), fatigability (I), and frequency of illness (J), as well as on emotional questions (M to R); these sections of the CMI questionnaire have been established as significant contributors to the identification of individuals with neurotic tendencies.
Therefore, following Kaneshita et al.11, the neurotic tendencies of patients were divided into four classes (1–4) based on the total number of ‘yes’ responses to items C, I, and J and the total number of ‘yes’ responses to questions about their emotional status (M–R). Class 1 was diagnosed as normal and class 4 was diagnosed as neurotic. Classes 2 and 3 occupy a boundary state between normal and neurotic. Class 2 has a higher likelihood of being normal, resulting in a provisional diagnosis as normal; class 3 has a lesser likelihood of being normal, resulting in a provisional diagnosis as neurotic.
Statistical analysis
The raw data from the questionnaires were entered into a computer database. The chi-square and unpaired t-tests were used to identify differences between the subjects with and without oral malodour who had neurotic tendencies in terms of the frequency of ‘yes’ responses to the CMI questionnaire and the clinical parameters. The SPSS statistical software package was used for all analyses (release 11.0 J; SPSS, Tokyo, Japan).
RESULTS
Presence of oral malodour and psychological status
For the 368 subjects, the CMI estimates for neurotic tendencies placed 174 (47.3%), 115 (31.3%), 73 (19.8%), and 6 (1.63%) subjects in classes 1 to 4, respectively. Of the 289 subjects in classes 1 and 2, classified as normal according to the CMI, 225 (61.1%) met criteria for oral malodour (≥3 OLT score and/or ≥0.25 ppm mouth air of total VSCs), and 64 (17.4%) did not (<3 OLT score and/or <0.25 ppm mouth air of total VSCs). The former were diagnosed with simple genuine halitosis and the latter with simple pseudo halitosis, and the treatment of these patients followed the conventional standard protocol2., 7.. On the other hand, the 79 subjects in classes 3 and 4, classified as having neurotic tendencies, could be diagnosed with halitophobia per se, or genuine- or pseudo-halitosis with psychosomatic symptoms. Fifty-eight patients (15.8%) had oral malodour, and 21 (5.7%) did not. Table 1 shows demographic information, VSC levels, and oral health conditions of the study population. There was a high proportion of females in the group with neurotic tendencies and no oral malodour (81.0%); this figure was significantly (P = 0.004) higher than that for the group with neurotic tendencies and oral malodour (44.8%). All of the subjects had good oral mucosal and salivary gland health. Table 2 shows clinical parameters associated with oral malodour and living habits among subjects with and without oral malodour and with neurotic tendencies. A TCS ≥3, a PPD ≥5 mm, and daily alcohol consumption were significantly more common in the subjects with oral malodour. There was no significant difference in the smoking status among the subjects with and without oral malodour.
Table 1.
Demographics, oral malodour levels, and baseline oral health conditions of subjects
| Parameter | Normal mental status (n = 289) | Neurotic mental status (n = 79) | ||
|---|---|---|---|---|
| Subjects without oral malodour (n = 64) | Subjects with oral malodour (n = 225) | Subjects without oral malodour (n = 21) | Subjects with oral malodour (n = 58) | |
| Age (years) (average ± SD) | 43.3 ± 15.6 | 47.0 ± 14.4 | 40.1 ± 11.5 | 43.3 ± 14.7 |
| Females (%) | 57.8 (37/64) | 63.1 (142/225) | 81.0 (17/21) | 44.8 (26/58) |
| Males (%) | 42.2 (27/64) | 36.9 (83/225) | 19.0 (4/21) | 55.2 (32/58) |
| Oral malodour levels | ||||
| H2S (ppm) | 0.07 ± 0.05 | 0.50 ± 0.35 | 0.07 ± 0.04 | 0.56 ± 0.42 |
| CH3SH (ppm) | 0.03 ± 0.03 | 0.36 ± 0.28 | 0.04 ± 0.03 | 0.35 ± 0.32 |
| CH3SCH3 (ppm) | 0.01 ± 0.02 | 0.10 ± 0.08 | 0.01 ± 0.02 | 0.10 ± 0.10 |
| Total VSCs (ppm) | 0.11 ± 0.08 | 0.96 ± 0.66 | 0.12 ± 0.07 | 1.01 ± 0.78 |
| Baseline of oral health condition | ||||
| Number of teeth | 26.3 ± 5.03 | 26.7 ± 3.46 | 26.3 ± 4.87 | 25.9 ± 6.37 |
| Number of caries | 0.68 ± 2.33 | 0.50 ± 1.41 | 0.38 ± 0.74 | 0.43 ± 0.86 |
| Number of fillings | 12.7 ± 5.60 | 12.8 ± 5.77 | 14.6 ± 5.33 | 12.1 ± 6.10 |
| Stimulated salivary flow (ml per 5 minutes) | 5.88 ± 2.74 | 6.67 ± 3.34 | 5.09 ± 2.64 | 7.11 ± 3.70 |
Table 2.
Clinical parameters associated with oral malodour in and living habits of subjects with neurotic tendencies (n = 79)
| Parameter | Subjects without oral malodour (n = 21) | Subjects with oral malodour (n = 58) | P-value |
|---|---|---|---|
| Clinical parameters associated with oral malodour | |||
| Tongue coating score | |||
| ≥3 | 0 (0/21) | 20.7 (12/58) | <0.05 |
| <3 | 100 (21/21) | 79.3 (12/58) | |
| Caries | |||
| Presence | 23.8 (5/21) | 24.1 (14/58) | NS |
| Absence | 76.2 (16/21) | 75.9 (44/58) | |
| No-good margin | |||
| Presence | 4.76 (1/21) | 8.62 (5/58) | NS |
| Absence | 95.2 (20/21) | 91.4 (53/58) | |
| Tooth mobility | |||
| Presence | 14.3 (3/21) | 12.1 (7/58) | NS |
| Absence | 85.7 (18/21) | 87.9 (51/58) | |
| PPD | |||
| ≥5 mm | 4.76 (1/21) | 41.4 (24/58) | <0.01 |
| <5 mm | 95.2 (20/21) | 58.6 (34/58) | |
| Occult blood in the saliva | |||
| Presence | 19.0 (4/21) | 36.2 (21/56)* | NS |
| Absence | 81.0 (17/21) | 62.5 (21/56)* | |
| Living habits | |||
| Smoking | |||
| Current | 19.0 (4/21) | 12.1 (7/58) | NS |
| Non- or former | 81.0 (17/21) | 87.9 (51/58) | |
| Alcohol consumption | |||
| Daily | 0 (0/21) | 27.6 (16/58) | <0.01 |
| Not daily | 100 (21/21) | 72.4 (42/58) | |
Tests of occult blood in the saliva were not performed in two samples obtained from the subjects with oral malodour.
Psychological characteristics in the patients with neurotic tendencies
Table 3 shows the average of ‘yes’ responses to sections C, I, J and M–R of the CMI for subjects with and without oral malodour and with neurotic tendencies according to the CMI test. The 289 subjects classified as normal showed significantly lower scores in all sections than did the 79 subjects with neurotic tendencies (data not shown). The subjects without oral malodour scored significantly (P < 0.01) higher on the section addressing fatigability (I) with regard to somatic status. We found no significant difference in emotional status between the subjects with and those without oral malodour.
Table 3.
The average numbers of ‘yes’ responses among the subjects with and without oral malodour on Sections C, I, J and M–R of the CMI questionnaire
| Subjects without oral maloduor (n = 21) | Subjects with oral malodour (n = 58) | P-value | |
|---|---|---|---|
| Somatic Status | |||
| C (cardiovascular system) | 2.48 ± 1.78 | 3.05 ± 2.02 | NS |
| I (fatigability) | 3.57 ± 0.68 | 2.12 ± 1.45 | <0.01* |
| J (frequency of illness) | 1.33 ± 1.32 | 1.29 ± 1.51 | NS |
| Emotional Status | |||
| M (inadequacy) | 4.43 ± 2.62 | 4.78 ± 2.93 | NS |
| N (depression) | 1.10 ± 1.61 | 0.79 ± 1.22 | NS |
| O (anxiety) | 2.81 ± 1.89 | 2.22 ± 1.52 | NS |
| P (sensitivity) | 2.90 ± 1.34 | 2.74 ± 1.49 | NS |
| Q (anger) | 3.33 ± 2.01 | 3.48 ± 2.19 | NS |
| R (tension) | 1.86 ± 1.62 | 2.16 ± 1.58 | NS |
Significant difference between the subjects with and without oral malodour at P < 0.01 (unpaired t-test).
Further exploratory analysis was subsequently performed to identify the questions that were most effective for understanding the mental status of halitosis patients. Table 4 shows questions that comprised sections C, I, J and M–R and elicited significantly different answers from subjects with and without oral malodour at P < 0.05. The subjects with no oral malodour more frequently responded ‘yes’ to questions about morning tiredness and job-related exhaustion (question nos. 109–111 in item I [fatigability]). In addition, they more frequently responded ‘yes’ to questions about psychological problems in their families with regard to emotional symptoms compared to subjects with oral malodour (question nos. 169 and 171 in item O [anxiety]). They also frequently responded ‘yes’ to the question of ‘Does worrying run in your family?’ (question no. 164 in item O [anxiety]) compared with the subjects with oral malodour (P = 0.051). Furthermore, in the interviews asking about the bad-breath history of the patients, 12 (57.1%) of the subjects without oral malodour answered that they had perceived their own ‘bad breath’ (vs. 27.6% of the subjects with oral malodour, P < 0.05).
Table 4.
Questions included C, I, J and M–R showing significant differences between subjects with and without oral malodour (P < 0.05)
| Questionnaire | Subjects without oral malodour (n = 21) | Subjects with oral malodour (n = 58) | P-value* |
|---|---|---|---|
| Somatic status | |||
| I109 Does working tire you out completely? | 95.2 (20/21) | 69.0 (40/58) | 0.016 |
| 110 Do you usually get up tired and exhausted in the morning? | 66.7 (14/21) | 32.8 (19/58) | 0.007 |
| 111 Does every little effort wear you out? | 85.7 (18/21) | 25.9 (15/58) | <0.001 |
| Emotional status | |||
| O169 Did anyone in your family ever have a nervous breakdown? | 33.3 (7/21) | 8.62 (5/58) | 0.007 |
| 171 Was anyone in your family ever a patient in a mental hospital (for their nerves)? | 23.8 (5/21) | 1.72 (1/58) | 0.001 |
| R193 Do frightening thoughts keep coming into your mind? | 23.8 (5/21) | 6.90 (4/58) | 0.037 |
Chi-square test.
DISCUSSION
The CMI estimates for 79 (21.5%) of the 368 subjects placed them in the group with neurotic tendencies. Although the diagnosis and treatment of the 289 subjects in the normal group proceeded according to conventional protocol7, the diagnosis and treatment of the patients with neurotic tendencies were frequently difficult because differentiation among halitophobia and genuine- and pseudo-halitosis with psychosomatic symptoms is problematic. As a result, more detailed data on the clinical and psychosomatic characteristics of subjects with neurotic tendencies were collected in the present study.
Studies dating from 20 years ago reported a predominance of females in the patient populations at breath odour clinics18. Our clinic also had a higher proportion of females (60.3%) during the research; however, there was no significant difference between males and females. Recently, there has been an increase in the annual number of male patients. Nevertheless, most of the subjects with neurotic tendencies and no oral malodour were female (81.0%). Al-Ansari et al.19 reported that significant factors associated with self-reported halitosis in Kuwaiti patients included inadequate oral hygiene practices, female gender, older age, history of gastrointestinal tract disorders, chronic sinusitis, and lower education levels, suggesting that females tend to be more anxious about their bad breath than do males.
Among the subjects who exhibited neurotic tendencies as evaluated by CMI, a TCS ≥3, a PPD ≥5 mm, and daily alcohol consumption were significant factors associated with actual oral malodour. Coating of the tongue and marginal periodontitis are the most frequent oral causes of oral malodour2. Our previous study found an association between daily alcohol consumption and strong malodour, especially related to periodontal disease17. Other research has also reported that alcohol intake and body mass index may be factors that help predict oral malodour20.
The psychosomatic features of patients with no oral malodour might derive primarily from psychological problems involving social and interpersonal relationships. Although halitosis is not a self-evident symptom21, many patients with neurotic tendencies and with no oral malodour told the interviewer that they had perceived their own ‘bad breath.’ This may reflect a characteristic of psychosomatic conditions. These individuals more frequently responded ‘yes’ to questions about psychological problems in their families (Table 4). Numerous studies have reported increased rates of psychiatric disorders in children from homes with affectively ill parents, relative to children with non-ill parents22., 23.. Meta-analytic findings indicate that the offspring of parents with major depressive disorder will develop a psychiatric disorder during childhood or adolescence and are four times more likely to develop an affective disorder than are children with non-ill parents24. Many recent reports have emphasised the need to consider prevention for children of depressed parents. The patients with neurotic tendencies and no oral malodour also showed significantly greater symptoms of obsessive-compulsive disorder (question no. 193 in item R [tension]; P < 0.05), but not significantly higher scores for items regarding depression (N), anxiety (O), and sensitivity (P) compared with the patients having neurotic tendencies and oral malodour. Eli et al.25 reported that patients suffering from halitosis showed significant elevations in their scores for obsessive-compulsive symptoms, depression, anxiety, phobic anxiety, and paranoid ideation compared with a reference group of dental patients who did not complain of halitosis. Previous studies of the relationship between the actual degree of halitosis and the psychological condition of the subjects who complained of halitosis found, using the CMI test, that representative somatic symptoms (C, I, J), anger (Q), inadequacy (M), and sensitivity (P) were more often observed in subjects with no or slight oral malodour13., 14..
However, there have been no reports on the relationship between the actual degree of halitosis and the psychological condition of subjects who complain of halitosis and have neurotic tendencies according to the CMI test. Such different approaches using the CMI Health Questionnaire might be helpful for further sub-classification of subjects complaining of halitosis. Most malodour studies, including the present investigation, have been based on groups containing both males and females, with a broad range of ages. Further investigations are needed to develop prevention and treatment strategies fit to gender and/or age groups.
Acknowledgements
This study was supported by Grants-in-Aid for Scientific Research (C) 20592249 (to M.Y.) and 20592444 (to T.N.); and Grants-in-Aid for Advanced Science Research from the Ministry of Education, Culture, Sports, Science and Technology, Japan; and a research grant from the Mitsui Sumitomo Insurance Welfare Foundation.
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