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A Study on the Internal Oral Factors Affecting Components of Halitosis
Int J Clin Prev Dent 2020;16(4):165-169
Published online December 31, 2020;
© 2020 International Journal of Clinical Preventive Dentistry.

Hye-Jeong Bok, Eun-hee Lee

Department of Dental Hygiene, Busan Women's College, Busan, Korea
Correspondence to: Eun-hee Lee
Received December 10, 2020; Revised December 21, 2020; Accepted December 28, 2020.
This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License ( which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.
Objective: The present study aimed to investigate the relationship between internal oral factors and components of halitosis and prepare clinically applicable data for efficient prevention of halitosis and establishment of a halitosis control plan.
Methods: A hundred and one healthy adult men and women without systemic diseases were recruited in the present study. Values for each component of halitosis and internal oral factors, including oral hygiene index, using a disclosing agent and Quantitative light-induced fluorescence- device (AIOBIO, Seoul, Korea), salivary flow rate, oral humidity, and tongue plaque index, were measured, and a correlation analysis was performed for each figure.
Results: According to the results of the association analysis between halitosis components and internal oral factors, hydrogen sulfide had a statistically significant relationship with simulated saliva and the tongue coating index (p<0.05). Methyl mercaptan was found to have a significant relationship with the O’Leary index and the simple plaque score (p<0.05).
Conclusion: The above results suggest that of the internal oral factors studied, O’Leary index, simple plaque score, tongue coating index, stimulated saliva, etc., have associations with halitosis components.
Keywords : halitosis, methyl mercaptan, hydrogen sulfide

Oral malodor, halitosis has been influenced the human relationship at present days as one of the social problems. The etiology of the halitosis would be divided as systemic factor, oral factor Psychologic factor and physiologic factor and the main factor of them would be a host factor and it would be from the putrefaction of food debris by oral micro-organism [1]. Among them, volatile sulfur compound (VSC) as volatile sulfur compounds (VSCs) has been known as the main cause of oral malodor and it could be divided as 3 components as hydrogen sulfide (H2S), Methyl Mercaptan (CH3SH) and Dimethyl Sulfide (C2H6S) [2]. VSC has been known to be occurred from the metabolic process for the analysis of such components as epithelial cell, blood protein or food debris by Gram negative anaerobic oral micro-organisms [3,4]. Oral malodor would be relation with the tongue plaque and periodontal disease with their oral micro-organisms such Gram negative anaerobic bacteria as Treponema denticola, Porphyromonas gingivalis, Prevotella intermedia, Bacteroides forsytus, and Fusobacterium, and it could be find lots of production of H2S and CH3SH, to be estimated that the oral malodor could be related with periodontal disease [5
-7]. Moreover, oral malodor has been known as related with the salivary flow. In case of decreasing the salivary flow, the density of oral micro-organisms in oral cavity should be increased and it could be increased the oral malodor level through the longer time contact with Sulfur and fatty acid producing materials [8].

The malodor check method has been known as subjective method and objective one. The subjective examination is called as the organoleptic examination which the examiner smell patient’s malodor directly with closing their nose to patient’s mouth, and the objective method as using the malodor check machine. The subjective method is not general used in research method because of it’s the different by examiners [9]. On the other hands, one of the malodor check machine, Oral Chroma (CHM-1, Osaka, Japan) can be used not only for checking total amounts of VSCs, but also checking each sub components with Sulfur compounds as H2S, CH3SH and C2H6S, with separately and individually [10].

But there was rare to be studied as the relationship with each causing factor and oral malodor [11]. Oral malodor can be occurred with varies causing factors and composed with varies factors influence each other. So it needed for the comprehensive study about the relationship between each factor and real malodor components and amounts. This study has been performed to know which facto can be influenced to each oral malodor, in order to prepare the basic data for oral malodor control and prevention clinically in the future.

Materials and Methods

1. Subjects

The clinical study has been performed after receiving Institutional Review Board of the Dankook University (IRB no. 2020-04-021-001), and the volunteers were collected by use of community advertising board, using the community homepage and sharing the advertising papers from May in 2020. 101 volunteers were collected. 101 adult volunteers who had no problems with systemic disease or infection disease and good oral state without problem for oral malodor have been selected for this study. All subjects have been submitted the written agreement after understanding the objectives of the study. The general characteristics of subjects were shown in Table 1.

Table 1 . General characteristics (n=101)

SexMale30 (29.7)
Female 71 (70.3)
Age (yr) 20-2985 (84.1)
30-395 (5.0)
40-495 (5.0)
>666 (5.9)
Total 101 (100.0)

Values are presented as number (%).

2. Method

Plaque index was checked by use of O’Leary index which has been used popularly. Disclosing agent as disclosing solution (Sultan chemists inc, Englewood, NJ, USA) was used and checked the coated area with 4 surfaces as Mesial, Distal Buccal and Lingual surfaces with all teeth by divided with line angle of each tooth, and recorded the score. Quantitative light-induced fluorescence (QLF) (AIOBIO, Seoul, Korea) was used without coating the disclosing agent on the tooth surface which can check the Porphyrin as red colored fluorescent materials secreted from the micro-organisms [12]. In order to check the dental plaque, QLF was used without use the disclosing agent in the dark environment of observation room and lye the subject with supine position on the dental unit chair and took pictures for frontal teeth areas.

Oral hygiene index was estimated as 0 to 5 points by use of QLF-D simple plaque score (SPS) at each surface and recorded it [13].

Tongue coating index (TCI) was checked by dividing the dorsum of the tongue with 9 parts as 3 parts for the width and 3 for the length as give 0 point for without plaque and 1 point for thin plaque deposition with showing the papilla.

Oral malodor check was checked by use of Oral Chroma (CHM-1, Osaka, Japan) which can find each component of halitosis analysis. The standardization for recognition for each component was H2S 112 ppb, CH3SH 28 ppb, C2H6S 8 ppb and let them limit the diet, smoking or tooth-brushing or mouth gaggle at 3 hours before checking malodor, in order to check malodor component accurately. The oral gas was collected with 1 ml Oral Chroma syringe (CHM-1, Osaka, Japan) biting the tip without touching with saliva after mouth closing for 5 minutes in order to collect the malodor components in the mouth.

Stimulated salivary flow was measured collecting the saliva flow for 5 minutes separating with the stimulated and unstimulated salivary flow and estimated it as a minute salivary flow. Oral humidity test was done by use of Mucus (Life Co., Saitama, Japan) and check 3 times on the dorsum of the tongue and record the average points.

3. Data analysis and statistical methods

PASW Statistics ver. 18.0 (IBM Co., Armonk, NY, USA) computer program was used to analyze the collected data. The average of the frequency and percentage were calculated for the general characteristics of subjects and oral factors. Mann-Whitney U test for oral malodor components according to the gender difference, and Spearman's rank correlation coefficient was done for the components according to the relationship between the oral factors.


It has been reported that there has been different of oral malodor through the gender different among the physiologic factors for causing the halitosis [13,14]. Mann-Whitney U test was done for the oral malodor components according to the gender difference in order to know the other factors without the oral factors. The results were shown in Table 2 as the similar as Lee et al. [15] who have reported as no different of malodor components in VSC. The average level of VSC was not so high for all subjects but high level as 34.44 ppb on C2H6S, shown in Table 3. It revealed the average level of oral hygiene index as 57.31 points and oral humidity level as 27.03 for all subject, otherwise the tongue plaque coating level was average 2.21 as low level. C2H6S as measured as 34.44 as high level for recognizing the malodor level, shown in Table 4.

Table 2 . Comparison of volatile sulfur compound components by sex

VariableAverage rankRank totalUZp-value
Hydrogen sulfide (H2S)Male47.381421.50956.500−0.8080.419
Female 52.533729.50
Methyl mercaptan (CH3SH)Male48.781463.50998.500−0.4980.618
Female 51.943687.50
Dimethyl sulfide (C2H6S)Male57.421722.50872.500−1.4420.149
Female 48.293428.50  

Table 3 . Analysis of volatile sulfur compound concentration level

Hydrogen sulfide (H2S)0-11198 (97.0)
≥1123 (3.0)
Methyl mercaptan (CH3SH)0-2588 (87.1)
≥2613 (12.9)
Dimethyl sulfide (C2H6S)0-758 (57.4)
≥843 (42.6)

Values are presented as number (%). a: Measurement by ppb (parts per billion).

Table 4 . Descriptive statistics for oral factor variables

Hydrogen sulfide24.85±76.86
Methyl mercaptan12.58±27.36
Dimethyl sulfide34.44±66.56
O’Leary index55.45±22.80
Stimulated saliva9.57±3.20
Unstimulated saliva3.09±0.62
Oral humidity27.06±1.84
Tongue coating index2.39±2.09
Simple plaque score0.77±1.15

Values are presented as mean±standard deviation.

Through Spearman's rank correlation coefficient, because of not normal distribution in statistically, H2S and stimulated saliva and TCI were significantly different statistically (p<0.05). CH3SH was related with O’Leary index, H2S and simplified plaque score (p<0.05), shown in Table 5.

Table 5 . The correlation between malodor components and oral factors (n=101)

O’Leary indexStimulated salivaUnstimulated salivaOral humidityHydrogen sulfideMethyl mercaptanDimethyl sulfideTongue coating indexSimple plaque score
O’Leary index1
Stimulated saliva−0.0161
Unstimulated saliva0.1160.493**1
Oral humidity0.1510.1590.0211
Hydrogen sulfide−0.028−0.198*−0.112−0.1551
Methyl mercaptan0.236*−0.177−0.062−0.0720.335*1
Dimethyl sulfide0.066−0.063−0.136−0.104−0.0720.0661
Tongue coating index0.340**−0.135−0.046−0.0370.224*0.119−0.0591
Simple plaque score0.1160.0350.082−0.0050.0480.231*−0.1180.320*1

*p<0.05, **p<0.01.


It has been studied that how the causes of oral malodor related with each other, through the analysis of the causes of the oral malodor and each malodor component. Many studies with such causes as caries experience (i.e., the number of decayed, missing, filled teeth, DMFT), salivary flow, plaque index, salivary pH, tongue plaque index or periodontal index have been considered for the relationship with halitosis [16
-18]. But the halitosis with sulfuric compound has been known as composed with such components as H2S, CH3SH, C2H6S, and multi causative, so it could be hard to indicate for one cause directly [19]. In this study, it has been done to know the relationship between each causative factor. It has been resulted that H2S had been increased by the increasing of CH3SH component and TCI, otherwise, H2S would be increased according to decrees the stimulated salivary flow (p<0.05).

Moreover, the more increase the O’Leary index, H2S and SPS, the more increase the amounts of CH3SH (p<0.05). It revealed the positive relationship between H2S and CH3SH (p<0.01). Lee et al. [20] have reported that C2H6S could be increased in gastric troubled patient or lung problem patient, and it might be originated from systemic disease other than oral or local factor origin. In this study, the average amount of C2H6S was not high as low level and there was no relationship with the oral factors (p>0.05). This meant that the volunteers had been collected with the sound for systemic conditions and minimize the influence from the outside of the oral factor.

The former studies about the periodontal disease and oral malodor had announced that the saliva from the periodontal patients had enough amino acid which could be occurred the oral malodor [21,22]. Miyazaki et al. [23] repoeted that the patients who had periodontal disease and tongue plaque coating have increased the oral malodor. So, in this study, the higher O’Leary index and simplified oral hygiene index, the more producing the CH3SH (p<0.05), and it revealed the significant relation between in TCI and H2S (p<0.05). This result said that dental plaque, the causative factors for periodontal disease increased, it could influence to increase the VSC. But in this study, there was no consideration about the dental caries, or oral micro-organisms related with the producing the VSC, and it needed more studies about the relation with the more and variety causative factors and oral malodor in the future.


The aims of the study were to observe the relationship between the intrinsic factors and oral malodor components and to find the basic way for prevention and the control of oral malodor for clinical use.

101 adult volunteers who have no systemic disease were chosen for clinical test. Oral malodor was checked to analyze each component and checked such items as the plaque index by use of the disclosing solution and QLF-D, salivary flow, oral humidity test and tongue plaque index, to analyze the correlation coefficient. The obtained results were as followings.

1. There was a relationship between H2S and stimulated salivary flow and TCI, with significantly different statistically (p<0.05).

2. It revealed also relationship between CH3SH and O’Leary index and simplified plaque index with statistically significant (p<0.05).

3. It would be considered as certain that O’Leary index and simplified plaque index as plaque deposition, and tongue coating plaque and the stimulated salivary flow were related with the oral malodor.

4. H2S and CH3SH has been relationship (p<0.01).

And then from the above, the causative factors for oral factor were related with salivary flow and oral hygiene index. The more and detailed study to reveal the mechanism of oral malodor should be needed because the oral malodor can be occurred with variety cause with related factors together.

Conflict of Interest

No potential conflict of interest relevant to this article was reported.

  1. Tonzetich J. Production and origin of oral malodor: a review of mechanisms and methods of analysis. J Periodontol. 1977 ; 48 : 13-20.
    Pubmed CrossRef
  2. Tonzetich J. Oral malodour: an indicator of health status and oral cleanliness. Int Dent J. 1978 ; 28 : 309-19.
  3. Kleinberg I, Westbay G. Salivary and metabolic factors involved in oral malodor formation. J Periodontol. 1992 ; 63 : 768-75.
    Pubmed CrossRef
  4. Persson S, Edlund MB, Claesson R, Carlsson J. The formation of hydrogen sulfide and methyl mercaptan by oral bacteria. Oral Microbiol Immunol. 1990 ; 5 : 195-201.
    Pubmed CrossRef
  5. Rosenberg M. Clinical assessment of bad breath: current concepts. J Am Dent Assoc. 1996 ; 127 : 475-82.
    Pubmed CrossRef
  6. Persson S, Claesson R, Carlsson J. The capacity of subgingival microbiotas to produce volatile sulfur compounds in human serum. Oral Microbiol Immunol. 1989 ; 4 : 169-72.
    Pubmed CrossRef
  7. Loesche WJ. The identification of bacteria associated with periodontal disease and dental caries by enzymatic methods. Oral Microbiol Immunol. 1986 ; 1 : 65-72.
    Pubmed CrossRef
  8. Brunette DM. Introduction to the proceedings of the Fifth International Conference on Breath Odour Research. Int Dent J. 2002 ; 52 Suppl 3 : 177-80.
    Pubmed CrossRef
  9. Greenman J, Duffield J, Spencer P, Rosenberg M, Corry D, Saad S, et al. Study on the organoleptic intensity scale for measuring oral malodor. J Dent Res. 2004 ; 83 : 81-5.
    Pubmed CrossRef
  10. Jo ED, Han GS. Influencing factors in the halitosis. J Korean Acad Oral Health. 2012 ; 36 : 272-81.
  11. Kim BI. QLF concept and clinical implementation. J Korean Dent Assoc. 2011 ; 49 : 443-50.
  12. Yeo AN, Lee SY. The convergent effects of oral health education feedback using QraycamTM. J Korea Converg Soc. 2017 ; 8 : 63-70.
  13. Tonzetich J, Preti G, Huggins GR. Changes in concentration of volatile sulphur compounds of mouth air during the menstrual cycle. J Int Med Res. 1978 ; 6 : 245-54.
    Pubmed CrossRef
  14. Kawamoto A, Sugano N, Motohashi M, Matsumoto S, Ito K. Relationship between oral malodor and the menstrual cycle. J Periodontal Res. 2010 ; 45 : 681-7.
    Pubmed CrossRef
  15. Lee EH, Lee MG, Lee KH. Mineral salt and oriental medicine extracts contained mouth rinse influence to the dryness of the mouth and the oral malodor. Int J Clin Prev Dent. 2017 ; 13 : 81-6.
  16. Tonzetich J, Richter VJ. Evaluation of volatile odoriferous components of saliva. Arch Oral Biol. 1964 ; 9 : 39-46.
    Pubmed CrossRef
  17. Jung HY, Shin SC, Cho JW, Kim IS. A clinical study on oral malodor related to saliva and tongue plaque. Int J Clin Prev Dent. 2005 ; 1 : 54-63.
  18. Jee YJ, Shin SC, Song HJ, Cho JW. Correlation coefficiency between the oral malodour and the critical periodontal index. Int J Clin Prev Dent. 2006 ; 2 : 42-52.
  19. Kwon JH, Chang MT, Ryu SH, Kim HS. A study on the relationship between oral malodor and periodontal disease. J Korean Acad Periodontol. 2000 ; 30 : 203-12.
  20. Lee DN, Ahn YW, Ko MY, Park JS. A study for the relationship between systemic diseases and oral malodor. J Oral Med Pain. 2004 ; 29 : 119-26.
  21. Jee YJ, Kim JS, Lee JH, Jeon ES. A study on the relationship between halitosis developments and oral environmental. J Dent Hyg Sci. 2010 ; 10 : 101-7.
  22. Bae SM, Lee JY, Choi JI, Kim SJ. The effect of a full mouth disinfection on oral malodor in chronic periodontitis patients. J Korean Acad Periodontol. 2006 ; 36 : 829-37.
  23. Miyazaki H, Sakao S, Katoh Y, Takehara T. Correlation between volatile sulphur compounds and certain oral health measurements in the general population. J Periodontol. 1995 ; 66 : 679-84.
    Pubmed CrossRef

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