The relationship between volatile sulfur compounds and major halitosis-inducing factors.

Lee CH, Kho HS, Chung SC, Lee SW, Kim YK.

Department of Oral Medicine and Oral Diagnosis, College of Dentistry, Seoul National University, Seoul, Korea.

J Periodontol. 2003 Jan;74(1):32-7.

http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&list_uids=12593593&dopt=Abstract

BACKGROUND: 
Although tongue coating and periodontal conditions have been reported to be major halitosis-inducing factors, the relationship between volatile sulfur compounds (VSC) and these 2 major factors is not yet fully understood. The aim of this study was to investigate the relationship of VSC concentrations to tongue coating and periodontal health. METHODS: Forty subjects (mean age 33.3 years, range 14 to 64 years) were enrolled in this study. Gas chromatography was performed to analyze each VSC component from the mouth air sampled prior to tongue scraping, after tongue scraping, and after a subsequent prophylaxis on the interdental spaces. 

RESULTS: 
CH3SH was the most malodorous component among the 3 major VSC from the mouth air. The high CH3SH group showed a significantly higher organoleptic rating (P < 0.01), gingival index (P < 0.01), bleeding index (P < 0.01), probing depth (P < 0.05), and VSC concentrations prior to tongue scraping (P < 0.01), except for the amount of tongue coating, compared to the low CH3SH group. All VSC concentrations were vastly reduced by tongue scraping in both groups, and the remaining contents were nearly all removed by the subsequent prophylaxis. The VSC contents produced by the tongue coating played a major role [H2S: 76%; CH3SH: 52%; (CH3)2S: 55%] in the low CH3SH group. In the high CH3SH group which had poor periodontal health, the tongue coating still played a major role [H2S: 67%; CH3SH: 59%; (CH3)2S: 48%], but the interdental spaces also contributed to VSC production [H2S: 26%; CH3SH: 32%; (CH3)2S; 36%]. 

CONCLUSIONS: 
The tongue coating was demonstrated to be a primary halitosis-inducing factor. Periodontal health was also shown to contribute to VSC production.

Variation in oral volatile sulphur compound formation.

Young A, Jonski G, Rolla G.

Department of Cariology, Oral Research Laboratory, Faculty of Dentistry, University of Oslo, Norway. alixr@odont.uio.no

Acta Odontol Scand. 2002 Dec;60(6):321-4.

http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&list_uids=12512879&dopt=Abstract

It has been suggested that the level of orally produced volatile sulphur compounds (VSCs) can be of use when monitoring oral malodour or in determining patients at risk of periodontal disease in longitudinal studies. It is not known, however, to what extent the level of VSC in mouth air is a stable, individual characteristic over time. 

AIM: 
The hypothesis to be tested was that the level of VSC in mouth air is an individual trait that is stable over time. 

METHODS:
Two groups of dental students participated in the study (n = 30 and n = 11). The amount of available substrate for VSC formation was standardized by rinses with 6 mM aqueous solutions of cysteine (pH 7.2). Part 1 used a Haliineter to measure 'morning breath' and response to cysteine rinses. Part 2 measured response to cysteine rinsing using a gas chromatograph. Repeated measurements provided information concerning the longitudinal intra-individual variations in level of oral VSC formation. 

RESULTS: 
Both groups showed large intra-individual variations in oral VSC. The differences were enhanced by cysteine rinses. 

CONCLUSION: 
The hypothesis was not supported. Oral VSC levels cannot be taken as diagnostic criteria in a normal population because of marked intra-individual variations over time.

Classification and examination of halitosis.

Murata T, Yamaga T, Iida T, Miyazaki H, Yaegaki K.

Department of Oral Health Science, Graduate School of Medical and Dental Sciences, Niigata University, Japan.

Int Dent J. 2002 Jun;52 Suppl 3:181-6.

http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&list_uids=12090449&dopt=Abstract

In this paper, the classification of halitosis and the examination procedures used in diagnosing halitosis are outlined. Halitosis is classified into categories of genuine halitosis, pseudo-halitosis and halitophobia. Genuine halitosis is subclassified into physiologic halitosis and pathologic halitosis. Pathologic halitosis itself is subdivided into oral and extraoral halitosis. Patients diagnosed with pseudo-halitosis and halitophobia usually complain about having oral malodour that does not really exist. Pseudohalitosis can be treated by dental practitioners, but halitophobic patients must be referred to psychological specialists. Oral malodour can be measured using an organoleptic measurement or a gas chromatography analysis. The organoleptic measurement is the most practical procedure with which one can evaluate oral malodour. Gas chromatography (GC) analysis using a flame photometric detector has been shown to be the gold standard for measuring oral malodour, owing its reputation to its objectivity and reproducibility. Moreover, GC is specific for volatile sulphur compounds (VSC), which are the main causes of oral malodour. It has been demonstrated that there is a high correlation between the intensity of oral malodour and the VSC concentration as measured by GC.

Comparison of volatile sulfur compound concentrations measured with a sulfide detector vs. gas chromatography.

Furne J, Majerus G, Lenton P, Springfield J, Levitt DG, Levitt MD.

The Minneapolis Veterans Affairs Medical Center, MN 55417, USA.

J Dent Res. 2002 Feb;81(2):140-3.

http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&list_uids=11827259&dopt=Abstract

The accuracy of the Halimeter, an inexpensive, simple instrument that measures total breath volatile sulfur compounds (VSCs), has not been adequately tested. We compared Halimeter measurements with those obtained with a specific and sensitive gas chromatographic (GC) technique. The Halimeter gave different, biexponential responses to a constant concentration of different VSCs: The relative response rate and sensitivity were hydrogen sulfide > methyl mercaptan > dimethylsulfide. The transient peak VSC concentration of oral samples was reached long before the sulfide detector fully responded. The GC measurement of initial total VSCs in breath samples was 2.7+/-0.48 times greater than the peak concentration of the Halimeter. However, the plateau phase measurement of the Halimeter was 25% greater than that of GC. While GC and Halimeter measurements positively correlated, appreciable differences were observed. In studies where relatively precise VSC measurements are required, GC is the preferable technique.

Effect of initial periodontal therapy on sulcular/tongue sulfide level. A pilot study.

Morita M, Wang HL.

Department of Periodontics/Prevention/Geriatrics, University of Michigan School of Dentistry, Ann Arbor, MI, USA.E-mail: homlay@umich.edu

J Clin Periodontol. 2002 Sep;29(9):844-7.

http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&list_uids=12423298&dopt=Abstract

BACKGROUND: 
Volatile sulfur compounds (VSC), such as hydrogen sulfide, methyl mercaptan and dimethyl sulfide, are toxic metabolites produced by periodontal pathogens. These VSC are also released from the tongue dorsum. Currently, limited data are available on how periodontal treatments may affect sulcular/tongue sulfide level. The aim of this study was to determine effect of initial therapy including oral hygiene instruction and scaling and root planing (SRP) on sulcular/tongue sulfide level. 

METHODS: 
Thirteen subjects diagnosed with chronic periodontitis and having three representative periodontal pocket depth (PD) strata in one quadrant (PD <or= 3.0 mm: healthy, 4.0 mm <or= PD <or= 6.0 mm: moderate, and PD >or= 7.0 mm: severe disease sites) were selected. Clinical periodontal parameters were recorded at baseline and 3 weeks after completion of the initial therapy. The sulfide levels in three representative periodontal pockets (pS) and on three parts (anterior, middle, and posterior) of the tongue dorsum (tS) were measured using a commercial sulfide-monitoring device. 

RESULTS: 
The pS levels of the three representative sites were reduced significantly following the initial therapy (p < 0.05). However, there was no significant reduction of the tS level in all three parts of the tongue. 

CONCLUSIONS:
The initial periodontal therapy such as oral hygiene and SRP reduces the sulcular sulfide level but not the tongue sulfide level. This suggests that sulcular sulfide level may be a possible indicator for assessing the outcome of initial periodontal treatment.

Characteristics of patients complaining of halitosis and the usefulness of gas chromatography for diagnosing halitosis.

Oho T, Yoshida Y, Shimazaki Y, Yamashita Y, Koga T.

Department of Preventive Dentistry, Faculty of Dental Science, Kyushu University, 3-1-1 Maidashi, Higashi-ku, Fukuoka, 812-8582, Japan.

Oral Surg Oral Med Oral Pathol Oral Radiol Endod. 2001 May;91(5):531-4.

http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&list_uids=11346730&dopt=Abstract

OBJECTIVE: 
The purpose of this study was to examine the characteristics of patients complaining of halitosis and to evaluate the diagnostic accuracy of 3 methods of measuring halitosis.Study Design: The actual degree of halitosis was determined through use of an organoleptic test in 155 patients aged 46 +/- 17 years (mean +/- SD). The volatile sulfur compounds (VSCs) were determined with gas chromatography and with sulfide monitoring. 

RESULTS: 
The organoleptic test revealed that 55% of the subjects had either no mouth odor or slight mouth odor. There was a significant correlation between the organoleptic score and the total VSC level as determined through use of other methods. The critical discrimination value of the total VSC level was calculated to be 0.057 ppm for gas chromatography and 0.117 ppm for sulfide monitoring; high sensitivity and specificity were obtained when the gas chromatography value was used. The amount of tongue coating was significantly greater in the halitosis-positive group than in the halitosis-negative group, whereas there was no difference in salivary flow rate between the 2 groups. 

CONCLUSION: 
These results indicate that determining VSCs with gas chromatography is a useful means of diagnosing halitosis.

Effectiveness of mechanical tongue cleaning on oral levels of volatile sulfur compounds.

Seemann R, Kison A, Bizhang M, Zimmer S.

MEDLive GmbH, Fabeckstrasse 60-62, 14195 Berlin, Germany. seemann@medlive.de

J Am Dent Assoc. 2001 Sep;132(9):1263-7; quiz 1318.

http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&list_uids=11665351&dopt=Abstract

BACKGROUND: 
Mechanical tongue cleaning may be an effective method for decreasing oral levels of volatile sulfur compounds, or VSC, and oral malodor. The authors conducted a study to compare the effectiveness of a specially designed tongue cleaner (One Drop Only Tongue Cleaner, One Drop Only, Berlin), a tongue scraper and a toothbrush in reducing oral VSC levels. 

METHODS: 
In this balanced, crossover study, 30 subjects had four morning appointments each with a waiting period of one week between appointments. At each appointment, a dental professional performed a single standardized tongue cleaning procedure using one of the cleaning tools. The authors monitored the subjects' oral VSC values using a portable sulfide monitor until their baseline VSC values were reached. 

RESULTS: 
The baseline values showed no significant difference between the three groups. The tongue cleaner and the tongue scraper (42 percent and 40 percent, respectively) reduced oral VSC levels more than the toothbrush (33 percent) did. Reduced VSC values could be detected significantly longer after using the tongue cleaner than after using the tongue scraper or the toothbrush. The authors, however, could not detect a significant VSC reduction for more than 30 minutes in any of the subjects. 

CONCLUSIONS AND CLINICAL IMPLICATIONS: 
The tongue cleaner, a combination brush and scraper, was slightly more effective in reducing oral VSC levels than were the tongue scraper and a regular toothbrush. Because of the limited duration of the effect, however, the clinical efficacy on the reduction of oral malodor remains questionable.

Spontaneous fluctuations in the concentrations of oral sulfur-containing gases.

Springfield J, Suarez FL, Majerus GJ, Lenton PA, Furne JK, Levitt MD.

The Minneapolis Veterans Affairs Medical Center, MN 55417, USA.

J Dent Res. 2001 May;80(5):1441-4.

http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&list_uids=11437216&dopt=Abstract

Breath hydrogen sulfide (H2S) and methyl-mercaptan (CH3SH) concentrations are used as quantitative indicators of halitosis. However, measurements of these gases in duplicate oral samplings often show poor reproducibility. To determine if this poor reproducibility is an artifact of the collection/analytical procedure or a true biological phenomenon, we used a standardized technique to collect from 20 to 30 oral gas samples at two-minute intervals from 11 healthy subjects. The samples were analyzed for sulfur gases and CO2. Sizable variations in H2S and CH3SH concentrations were not associated with alterations in CO2, indicating that the variations did not reflect variable contamination with atmospheric or pulmonary gas. In addition, fluctuations in H2S and CH3SH were not identical and often were not random. We conclude that minute-to-minute variability in oral sulfur gas concentrations is a true biological phenomenon. This fluctuation complicates experimental studies designed to show that interventions alter halitosis.

Assessment of newly developed tongue sulfide probe for detecting oral malodor.

Morita M, Musinski DL, Wang HL.

Department of Preventive Dentistry, Okayama University Dental School, Japan. Periodontics/Prevention/Geriatrics, University of Michigan School of Dentistry, Ann Arbor, Michigan 48109-1078, USA, E-mail: homlay@umich.edu

J Clin Periodontol. 2001 May;28(5):494-6.

http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&list_uids=11350515&dopt=Abstract

AIM: 
The present study examined the relationship between sulfide levels on tongue dorsum surfaces (pS levels) and oral malodor. METHOD: The pS levels of 20 systemically healthy volunteers were evaluated using an industrial device equipped with a newly-developed tongue sulfide probe. The pS levels on 3 parts of the tongue--anterior, middle and posterior along the median groove of the tongue dorsum--were determined for each subject. 

RESULTS: 
The device reported the pS level in a digital score ranging from 0.0 (< 10(-7) M of sulfide) to 5.0 (> or = 10(-2) M of sulfide) in increments of 0.5. Oral malodor was assessed by measuring the level of volatile sulfur compounds in mouth air, as well as by the organoleptic method. The pS levels were 0.03 +/- 0.11, 0.20 +/- 0.41 and 0.88 +/- 0.76 for the anterior, middle and posterior parts, respectively. This difference was significant (p<0.001). Both oral malodor measurements showed significant correlation (p<0.05) with the pS levels of middle and posterior parts of tongue. 

CONCLUSION: 
It was concluded that the tongue sulfide probe might be useful in management of subjects with oral malodor.

Association between oral malodor and adult periodontitis: a review.

Morita M, Wang HL.

Department of Preventive Dentistry, Hokkaido University Dental School, Sapporo, Japan.

J Clin Periodontol. 2001 Sep;28(9):813-9.

http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&list_uids=11493349&dopt=Abstract

BACKGROUND: 
Bad breath has a significant impact on our daily social life to those who suffer from it. The majority of bad breath originates within the oral cavity. However, it is also possible that it can come from other sources such as gastric-intestine imbalance. The term "oral malodor" is used to describe a foul or offensive odor emanating from the oral cavity, in which proteolysis, metabolic products of the desquamating cell, and bacterial putrefaction are involved. Recent evidence has demonstrated a link between oral malodor and adult periodontitis. The process of developing bad breath is similar to that noted in the progression of gingivitis/periodontitis. Oral malodor is mainly attributed to volatile sulfur compounds (VSC) such as hydrogen sulfide, methyl mercaptan and dimethyl sulfide. The primary causative microbes are gram-negative, anaerobic bacteria that are similar to the bacteria causing periodontitis. These bacteria produce the VSC by metabolizing different cells/tissues (i.e., epithelial cells, leukocytes, etc.) located in saliva, dental plaque, and gingival crevicular fluid. Tongue surface is composed of blood components, nutrients, large amounts of desquamated epithelial cells and bacteria, suggesting that it has the proteolytic and putrefactive capacity to produce VSC. One of the challenges in dealing with oral malodor is to identify a reliable test for detecting bad breath. 

AIMS: 
The purposes of this review article were: (1) to correlate the relationship between oral malodor and adult periodontitis; (2) to analyze current malodor tests and discuss available treatment regimens.

On the transformation of sulfur-containing amino acids and peptides to volatile sulfur compounds (VSC) in the human mouth.
Waler SM.

Dental Faculty, University of Oslo, Norway. smw@odont.uio.no

Eur J Oral Sci. 1997 Oct;105(5 Pt 2):534-7.

http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&list_uids=9395120&dopt=Abstract

Halitosis is most often caused by oral conditions. Volatile sulfur compounds (VSC), constituting the major components of oral malodor, are produced by anaerobic, gram-negative bacteria retained mainly in periodontal pockets or on the tongue dorsum. Sulfur-containing amino acids serve as substrate for these bacteria. VSC have also been found to have unfavorable effect on the tissue. The aim of this study was to examine whether normal, healthy individuals with no history of halitosis were able to produce VSC from cysteine, when applied as a mouthrinse. A further aim of the study was to investigate and compare the potential of other sulfur-containing amino acids and peptides as substrates for oral VSC production and to localize the odor-production sites. A portable sulfide monitor was used for VSC registration. Results showed that all test subjects produced high oral concentrations of VSC upon rinses with cysteine, which thus seems to be a major substrate for VSC production. The other sulfur-containing substrates had much less effect. It was found that the tongue was the major site for VSC production, and that saliva per se caused low VSC production.

Relationship between volatile sulfur compounds, BANA-hydrolyzing bacteria and gingival health in patients with and without complaints of oral malodor.

De Boever EH, De Uzeda M, Loesche WJ.

Department of Biological and Materials Sciences, University of Michigan School of Dentistry, Ann Arbor.

J Clin Dent. 1994;4(4):114-9.

http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&list_uids=8031479&dopt=Abstract

The aim of this study was to obtain measurements of oral malodor, as measured by volatile sulfur compounds (VSC), in periodontally healthy individuals without any complaints of bad breath, and to compare the results with data obtained from patients with complaints of oral malodor. The quality of the mouth air was assessed organoleptically and a portable sulfide monitor was used to measure the concentration of VSC in mouth air. The gingival health of 35 individuals (21 M, 14 F; ages 18-57 years) without any malodor complaints was evaluated according to the Papillary Bleeding Score (PBS). Pocket depths and Bleeding upon Probing (BOP) were also recorded in 20 patients (11 females and 9 males ranging in age from 14 to 71 years) who complained of oral malodor. Scrapings of the dorsal surface of the tongue and each of 6 plaque samples per patient were evaluated for the presence of BANA-positive species, such as T. denticola, P. gingivalis, and B. forsythus. The organoleptic ratings and VSC values were significantly higher in the complaint group (p < 0.05). Subjects in the complaint group had a significantly higher percentage of bleeding sites (p < 0.005) and had significantly more plaques that tested positive for the presence of BANA-hydrolyzing species (p < 0.05). Tongue scrapings of subjects with a high organoleptic score consistently yielded a positive BANA reaction suggesting that the dorsal surface of the tongue is an important niche for BANA-positive, VSC-producing bacteria. This study suggests that the primary sources of VSC production are BANA-hydrolyzing bacteria in the plaque and on the dorsal surface of the tongue.

Volatile sulfur compounds in mouth air from clinically healthy subjects and patients with periodontal disease.

Yaegaki K, Sanada K.

Department of Preventive and Community Dentistry, School of Dentistry, Niigata, Japan.

J Periodontal Res. 1992 Jul;27(4 Pt 1):233-8.

http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&list_uids=1640345&dopt=Abstract

Volatile sulfur compounds (VSC) in mouth air were estimated by gas chromatography. The amount of VSC and the methyl mercaptan/hydrogen sulfide ratio were significantly increased in patients with periodontal disease. These two parameters also increased in proportion to the bleeding index and probing depth. A study was also done on the effect of removal of tongue coating on VSC concentrations in mouth air from patients with periodontal involvement. VSC and the methyl mercaptan/hydrogen sulfide ratio were reduced to 49% and 35%, respectively, by removal of the tongue coating. The average amount of tongue coating removed from patients with periodontal disease was significantly higher than from controls (90.1 mg vs. 14.6 mg, p less than 0.01). Estimated production of VSC from tongue coating was 4 times higher than the control value, and the methyl mercaptan/hydrogen sulfide ratio was also markedly increased. However, a saliva putrefaction study suggested that saliva does not contribute to the elevated ratio of methyl mercaptan in mouth air. These results strongly suggest that, in addition to periodontal pockets, tongue coating has an important role in VSC production, in particular leading to an elevated concentration of methyl mercaptan, which is more pathogenic than hydrogen sulfide.

The correlation between organoleptic mouth-odor ratings and levels of volatile sulfur compounds.

Schmidt NF, Missan SR, Tarbet WJ.

Oral Surg Oral Med Oral Pathol. 1978 Apr;45(4):560-7.

http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&list_uids=273847&dopt=Abstract

An organoleptic rating (OR) technique and gas-liquid chromatography were employed to study the relationship between oral-malodor ratings and the corresponding concentrations of oral volatile sulfur compounds (VSC) in a total of 102 subjects in two separate studies. Both studies demonstrated a statistically significant positive correlation between the intensity of perceived oral malodor and the concentration of VSC (H2S + CH3SH) emitted by individual subjects.