The authors have declared that no competing interests exist.
Conceived and designed the experiments: XPF. Performed the experiments: YZ. Analyzed the data: HXL. Contributed reagents/materials/analysis tools: XC. Wrote the paper: XC.
‡ These authors are joint first authors on this work.
To investigate the factors associated with halitosis in Chinese white-collar employees.
Subjects in three randomly selected office buildings in Shanghai, China, were enrolled in this cross-sectional study using cluster random sampling. Oral malodor was assessed by measuring volatile sulfur compounds (VSCs) with a portable sulfide monitor. Subjects’ oral health, including dental caries, periodontal status, and tongue coating, was evaluated clinically. A questionnaire was used to obtain information about participants’ demographic characteristics, oral hygiene habits, and health behaviors.
Of the 805 subjects invited to participate in this study, 720 were enrolled (89.4% response rate). Data from these subjects were used for statistical analyses. The prevalence of halitosis was 33.2%. In the final regression model, halitosis was significantly related to tongue coating thickness, periodontal pocket depth, no food consumption within 2 hours prior to oral examination, and less intake frequency of sweet foods.
In this Chinese white-collar population, tongue coating and periodontal disease were associated with halitosis. Oral hygiene education should be provided at the population level to encourage the maintenance of oral health and fresh breath. Consumption of sweet foods may reduce VSC production, although this finding requires further investigation.
The term “halitosis” refers to an unpleasant or offensive odor emanating from the mouth, regardless of whether its source is oral or non-oral[
Most cases of halitosis (80–90%) originate in the oral cavity as a result of proteolytic degradation by anaerobic Gram-negative oral bacteria of various sulfur-containing substrates in saliva, epithelial cells, blood, and food debris[
Compared to other workers, white-collar employees, including administrators, office workers, technicians, and commercial staff, may have more opportunities for interpersonal communication and, as a result, must pay more attention to their personal appearance. Many studies have examined aspects of health, such as mental health problems, sleep quality, and other illnesses, among this population [
The study was in compliance with Strengthening the reporting of observational studies in epidemiology (STROBE) statement guidelines.
This cross-sectional study was conducted in three randomly selected districts among the six districts with concentrations of office buildings in Shanghai, China. One office building in each district and two departments in each building were selected using cluster random sampling. All staff members in these departments were verbally invited to participate in the study by department directors who had been informed of the purpose and structure of the study. The sample size was calculated on the basis of a prevalence of halitosis of 20% in the general Chinese population, as determined by Halimter [
In each office building, we rented a room for several days for examination purposes. Subjects were asked to complete the questionnaire, and then oral malodor was assessed. Clinical oral examination was conducted with each subject seated in a portable dental chair. Three dentists were involved in the investigation, each of whom was responsible for one procedure. The examination procedure, which required about 2 hours for each subject, was conducted during the working hours of each office building. Subjects were not given specific instructions (e.g., to brush) or prohibitions (e.g., to not eat).
Oral malodor was assessed with a Halimeter (Interscan, Chatsworth, CA, USA) by measuring VSCs originating from the oral cavity. Each subject was asked to close his/her mouth for at least 1 minute. He/she was then instructed to hold a disposable tube above the posterior tongue dorsum, with the mouth slightly open while breathing through the nose. The peak value [in parts per billion (ppb)] displayed by the Halimeter was recorded. A VSC value of 110 ppb or greater was considered to indicate the presence of halitosis, according to the manufacturer’s instructions [
A trained and licensed dentist assessed participants’ dental caries status, gingival inflammation, periodontal status, plaque accumulation, and tongue coating. Oral examinations were conducted after oral malodor assessment to avoid the potential effect of possible gingival bleeding after probing on the accuracy of the latter. Decayed, missing, and filled tooth (DMFT) and decayed, missing, and filled surface (DMFS) indices were calculated. Dental caries status was assessed using the visual-tactile criteria proposed by the World Health Organization [
To assess intraexaminer reproducibility, 10% of subjects were reexamined. Cohen’s κ values for all clinical measurements (including dental caries status, gingival inflammation, periodontal status, plaque accumulation, and tongue coating evaluation) ranged from 0.87 to 0.98.
To supplement the oral examinations and obtain information about factors associated with halitosis, participants were asked to complete a 52-item self-administered questionnaire. This instrument has been used in halitosis clinics [
Descriptive statistics (means, standard deviations, and percentages) were calculated for subjects’ sociodemographic characteristics and VSC measurements. Chi-squared tests were performed to examine differences in VSC values [dichotomized as 0 (VSC < 110 ppb) and 1 (VSC ≥ 110 ppb)] according to clinical and lifestyle factors. Student’s
Of the 805 white-collar workers invited to participate in the study, 720 [347 men, 373 women; mean age, 30.4 (range, 22–70) years] were enrolled (89.4% response rate). Subjects who were absent on the examination days due to business trips or illness and those unwilling to undergo dental examination were excluded from the study. Clinical and survey data from the 720 subjects were included in the final analyses. No difference in age or gender distribution was noted between subjects who did and did not participate in the study.
The mean VSC value was 117 ± 103 ppb. VSC values exceeded 110 ppb, the cutoff value for halitosis, in 33.2% of subjects. Halitosis was more prevalent in men than in women (
% with VSC ≥ 110 ppb | VSC value (mean ± SD) | ||||
---|---|---|---|---|---|
Age (years) | 0. 420 | 0.190 | |||
21–30 | 479 | 40.3 | 111 ± 97 | ||
31–40 | 179 | 39.1 | 136 ± 120 | ||
>40 | 62 | 40.3 | 115 ± 82 | ||
Gender | 0.003 | 0.002 | |||
Male | 347 | 38.6 | 130 ± 117 | ||
Female | 373 | 28.2 | 106 ± 86 | ||
Place of birth | 0.941 | 0.304 | |||
Shanghai region | 387 | 33.1 | 114 ± 96 | ||
Other | 333 | 33.3 | 122 ± 110 | ||
BMI (kg/m2) |
0.170 | 0.015 | |||
<18 | 52 | 30.8 | 111 ± 101 | ||
18–24 | 521 | 31.7 | 112 ± 96 | ||
>24 | 143 | 39.9 | 140 ± 124 | ||
Education level |
0.067 | 0.841 | |||
High school or less | 154 | 39.6 | 121 ± 83 | ||
Undergraduate | 404 | 33.2 | 118 ± 101 | ||
Master's degree or more | 158 | 27.2 | 114 ± 122 | ||
Monthly income (RMB) |
0.773 | 0.539 | |||
0–3000 | 86 | 36.0 | 115 ± 83 | ||
3001–6000 | 162 | 32.1 | 114 ± 93 | ||
6001–9000 | 135 | 28.9 | 112 ± 97 | ||
9001–12000 | 115 | 33.0 | 112 ± 85 | ||
>12000 | 121 | 35.5 | 130 ± 120 |
#Obtained by Chi-squared test, Student’s
*Some data are missing for these variables.
VSC: volatile sulfur compound; SD: standard deviation; BMI: body mass index; RMB: Ren Min Bi (name of the currency in China).
Relationships between oral malodor measures and clinical factors are shown in
% with VSC ≥ 110 ppb | VSC value (mean ± SD) | ||||
---|---|---|---|---|---|
Tongue coating thickness | 0.007 | 0.003 | |||
None | 344 | 27.6 | 106 ± 93 | ||
Thin | 260 | 36.9 | 122 ± 96 | ||
Thick | 116 | 41.4 | 142 ± 135 | ||
Tongue coating area | 0.005 | 0.009 | |||
None | 342 | 27.2 | 105 ± 92 | ||
≤1/3 | 80 | 36.3 | 124 ± 97 | ||
1/3–2/3 | 154 | 35.7 | 123 ± 101 | ||
≥2/3 | 144 | 43.1 | 138 ± 125 | ||
Gingival index | 0.091 | 0.143 | |||
<1 | 610 | 31.7 | 115 ± 100 | ||
1–1.5 | 67 | 42.6 | 139 ± 134 | ||
>1.5 | 43 | 44.2 | 135 ± 98 | ||
Plaque index | 0.251 | 0.629 | |||
<2 | 593 | 32.7 | 117 ± 106 | ||
2–3 | 85 | 40.0 | 124 ± 94 | ||
>3 | 42 | 26.2 | 105 ± 66 | ||
Periodontal probing depth | <0.001 | <0.001 | |||
<3.5 mm | 682 | 31.7 | 114 ± 98 | ||
≥3.5 mm | 38 | 60.5 | 175± 153 |
#Obtained by Chi-squared test, Student’s
VSC: volatile sulfur compound; SD: standard deviation.
No oral hygiene habit was related to oral malodor (
% with VSC ≥ 110 ppb | VSC value (mean ± SD) | ||||
---|---|---|---|---|---|
Brushing < 2 hours before examination | 0.649 | 0.278 | |||
Yes | 24 | 37.5 | 140 ± 126 | ||
No | 696 | 33.0 | 117 ± 102 | ||
Toothbrushing frequency |
0.930 | 0.961 | |||
≥2×/day | 568 | 32.9 | 117 ± 103 | ||
1×/day | 145 | 33.8 | 119 ± 101 | ||
Never or seldom | 5 | 40.0 | 120 ± 60 | ||
Dental floss use |
0.934 | 0.357 | |||
Yes | 116 | 33.6 | 110 ± 71 | ||
No | 602 | 33.2 | 119 ± 108 | ||
Mouthwash use | 0.115 | 0.199 | |||
Yes | 236 | 29.2 | 110 ± 99 | ||
No | 484 | 35.1 | 121 ± 104 | ||
Gum chewing |
0.212 | 0.992 | |||
Yes | 506 | 31.8 | 117 ± 106 | ||
No | 213 | 36.6 | 118 ± 95 | ||
Tongue scraping | 0.518 | 0.192 | |||
Yes | 210 | 31.4 | 110 ± 86 | ||
No | 510 | 33.9 | 121 ± 108 |
#Obtained by Chi-squared test, Student’s
*Some data are missing for these variables.
VSC: volatile sulfur compound; SD: standard deviation.
% with VSC≥ 110 ppb | VSC value (mean ± SD) | ||||
---|---|---|---|---|---|
Food intake < 2 hours before examination |
<0.001 | <0.001 | |||
Yes | 407 | 24.3 | 96 ± 71 | ||
No | 312 | 44.9 | 146 ± 128 | ||
Fruit intake | 0.031 | 0.046 | |||
≥4×/week | 482 | 30.7 | 113 ± 99 | ||
≤3×/week | 164 | 34.8 | 120 ± 103 | ||
Seldom/never | 74 | 45.9 | 144 ± 121 | ||
Sweet food intake |
0.202 | <0.001 | |||
≥4×/week | 269 | 31.6 | 106 ± 77 | ||
≤3×/week | 369 | 32.5 | 117 ± 96 | ||
Seldom/never | 81 | 42.0 | 160 ± 172 | ||
Pungent food intake |
0.145 | 0.418 | |||
≥4×/week | 260 | 30.4 | 113 ± 102 | ||
≤3×/week | 228 | 31.1 | 116 ± 106 | ||
Seldom/never | 231 | 38.1 | 125 ± 101 | ||
Seafood intake | 0.398 | 0.333 | |||
≥4×/week | 127 | 31.5 | 112 ± 96 | ||
≤3×/week | 236 | 30.5 | 112 ± 100 | ||
Seldom/never | 357 | 35.6 | 123 ± 106 | ||
Fried food intake |
0.992 | 0.790 | |||
≥4×/week | 215 | 35.5 | 115 ± 99 | ||
≤3×/week | 261 | 33.0 | 117 ± 102 | ||
Seldom/never | 243 | 33.3 | 121 ± 106 | ||
Meat intake |
0.136 | 0.618 | |||
≥4×/week | 483 | 31.3 | 115 ± 102 | ||
≤3×/week | 120 | 40.8 | 123 ± 96 | ||
Seldom/never | 115 | 33.9 | 123 ± 113 | ||
Vegetable intake | 0.610 | 0.388 | |||
≥4×/week | 597 | 32.7 | 115 ± 96 | ||
≤3×/week | 86 | 33.7 | 129 ± 140 | ||
Seldom/never | 37 | 40.5 | 127 ± 104 | ||
Tea intake | 0.082 | 0.003 | |||
≥4×/week | 411 | 30.2 | 106 ± 80 | ||
≤3×/week | 124 | 33.9 | 127 ± 122 | ||
Seldom/never | 185 | 39.5 | 135 ± 127 | ||
Work stress | 0.043 | 0.231 | |||
Heavy | 255 | 52.4 | 111 ± 46 | ||
Medium | 400 | 36.8 | 127 ± 118 | ||
Low | 65 | 30.5 | 113 ± 96 | ||
Regular physical activity |
0.132 | 0.545 | |||
Yes | 361 | 30.5 | 120 ± 113 | ||
No | 358 | 35.8 | 115 ± 91 | ||
Current smoker |
0.568 | 0.287 | |||
Yes | 89 | 36.0 | 128 ± 115 | ||
No | 629 | 32.9 | 116 ± 101 | ||
Current alcohol consumption |
0.678 | 0.604 | |||
Yes | 174 | 34.5 | 121 ± 107 | ||
No | 543 | 32.8 | 117 ± 101 |
#Obtained by Chi-squared test, Student’s
*Some data are missing for these variables.
VSC: volatile sulfur compound; SD: standard deviation.
Regression models indicated that the percentage of subjects with VSCs ≥ 110 ppb was associated significantly with tongue coating thickness, PPD, and no food consumption within 2 hours prior to assessment (
Odds ratio | 95% CI | ||
---|---|---|---|
Tongue coating thickness | 0.005 | ||
None |
|||
Thin | 1.60 | 1.11–2.28 | |
Thick | 1.90 | 1.21–3.00 | |
PPD | 0.003 | ||
<3.5 mm |
|||
≥3.5 mm | 2.90 | 1.45–5.80 | |
Food consumption < 2 hours before examination | <0.001 | ||
No |
|||
Yes | 0.40 | 0.29–0.55 | |
(Intercept) | 0.012 | <0.001 |
#Obtained by multiple logistic regression.
aReference group.
CI: confidence interval; PPD: periodontal probing depth.
Tongue coating thickness | 6.026 | 0.003 | |
None |
0 | ||
Thin | 18.955 | ||
Thick | 35.242 | ||
PPD | 8.185 | 0.004 | |
<3.5 mm |
0 | ||
≥3.5 mm | 46.604 | ||
Food consumption <2 hours before examination | 43.558 | <0.001 | |
Yes |
0 | ||
No | 48.385 | ||
Intake frequency of sweet food | 9.587 | <0.001 | |
≥4×/week |
0 | ||
≤3×/week | 45.706 | ||
Seldom/never | 55.071 | ||
(Intercept) | 308.004 | <0.001 |
#Obtained by analysis of covariance.
aReference group.
PPD: periodontal probing depth.
This is the first study to evaluate the prevalence and factors related to halitosis in the specific population of white-collar employees in Shanghai, China. More than one-third (33.2%) of VSC values in the study population exceeded 110 ppb, similar to the results of previous studies [
In the present study, more men than women had VSCs ≥ 110 ppb and higher VSC values in bivariate analysis, consistent with the results of a study conducted in Brazil [
The finding that VSC values were higher in subjects with BMIs > 24 in bivariate analysis is similar to the results of a study conducted in Israel [
The dorsum of the tongue has long been considered the most important site for the development of halitosis, as abundant desquamated cells and leukocytes are retained and anaerobic bacteria grow on its irregular surface [
Several studies have indicated that periodontal disease is also a source of halitosis [
In analyses controlling for confounding factors, such as age and gender, we found that more frequent intake of sweet foods reduced VSC concentrations. The presence of carbohydrates, such as glucose and sucrose, has been reported to inhibit the expression and activity of trypsin-like enzyme, which is capable of degrading peptides that may produce malodorous compounds by producing an acidic environment [
Tea is a very popular beverage in China. Green tea has been reported to reduce VSC levels immediately after consumption
More than 90% of the subjects in this study complained of moderate to severe work stress. A greater proportion of participants with heavy work stress had VSCs ≥ 110 ppb in the bivariate analysis. One animal experiment showed that rats under stress produced more VSCs [
This study was an epidemiological study of halitosis in a specific population rather than the general population. Thus, the results may only be applicable to individuals with similar backgrounds and working conditions. Caution should be taken when seeking to apply the results to other populations.
In the present study, tongue coating thickness and PPD were significantly related to measures of oral malodor. As most cases of halitosis originate from the oral cavity, tongue cleaning and periodontal health maintenance may help to reduce oral malodor. The results of our study suggest that appropriate intake of sweet foods, while controlling for the risk of caries development, can reduce VSC production. However, the relationship between halitosis and sweet food consumption, as well as the appropriate amount of such foods to control VSC production without causing caries, requires further investigation.
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