|Year : 2016 | Volume
| Issue : 3 | Page : 94-98
Assessment of halitosis using the organoleptic method and volatile sulfur compounds monitoring
Mohammed Alasqah1, Shoyab Khan2, Mohammed Ali Elqomsan2, Khalid Gufran1, Zaheer Kola3, Mariam Omer Bin Hamza4
1 Department of Preventive Dental Sciences, College of Dentistry, Prince Sattam Bin Abdulaziz University, Al Kharj, Kingdom of Saudi Arabia
2 Department of Conservative Dental Sciences, College of Dentistry, Prince Sattam Bin Abdulaziz University, Al Kharj, Kingdom of Saudi Arabia
3 Department of Prosthodontics Dental Sciences, College of Dentistry, Prince Sattam Bin Abdulaziz University, Al Kharj, Kingdom of Saudi Arabia
4 Al Kharj Armed Forces Hospital, Al Kharj, Kingdom of Saudi Arabia
|Date of Web Publication||28-Nov-2016|
Department of Preventive Dental Sciences, College of Dentistry, Prince Sattam Bin Abdulaziz University, Al Kharj
Kingdom of Saudi Arabia
Source of Support: None, Conflict of Interest: None
Introduction: Halitosis can be tested using two main methods, organoleptic and assessment of volatile sulfur compounds (VSCs), using an electronic meter like Halimeter. Therefore, the present study was conducted to measure the oral malodor of volunteers by means of the organoleptic method and VSCs monitoring and to evaluate the diagnostic value of the Halimeter in the diagnosis of halitosis. Materials and Methods: A cross-sectional observational study was conducted to compare the two diagnostic aids for halitosis. The study population included 110 volunteers, all males, between the ages of 18 and 45 years selected from academic staff, students, and patients of college. Evaluation and comparison of two main methods for halitosis were done, namely, organoleptic and Halimeter. Specificity, positive predictive value (PPV), negative predictive value (NPV), and disease prevalence were calculated for the sulfide monitor test. Receiver operating characteristic (ROC) curve was used to determine the diagnostic values of Halimeter to differentiate individuals with and without halitosis. Results: The correlation coefficient between VSC grading and organoleptic score (Kendall's tau-b) was −0.1090, which was not significant (P = 0.2170). Sensitivity and specificity of sulfide monitor grades for detecting individuals with and without halitosis were 20.75% and 66.67%, respectively. The PPV for the Halimeter was 36.67%, and the NPV was 47.50%. A total of 48.18% of all subjects were accurately identified and differentiated. The area under the ROC curve was 0.5790 (95% confidence interval: 0.4600-0.6980). Conclusion: In the present study, the Halimeter was not found to have a good correlation with the organoleptic method. However, due to the diverse influencing factors, proof of halitosis should always be obtained with two different methods.
Keywords: Halimeter, halitosis, organoleptic, volatile sulfur compound
|How to cite this article:|
Alasqah M, Khan S, Elqomsan MA, Gufran K, Kola Z, Hamza MO. Assessment of halitosis using the organoleptic method and volatile sulfur compounds monitoring. J Dent Res Rev 2016;3:94-8
|How to cite this URL:|
Alasqah M, Khan S, Elqomsan MA, Gufran K, Kola Z, Hamza MO. Assessment of halitosis using the organoleptic method and volatile sulfur compounds monitoring. J Dent Res Rev [serial online] 2016 [cited 2020 Dec 1];3:94-8. Available from: https://www.jdrr.org/text.asp?2016/3/3/94/194833
| Introduction|| |
Halitosis is defined as breath that is offensive to others, caused by a variety of reasons including but not limited to periodontal disease, bacterial coating of the tongue, systemic disorders, and different types of food.  Halitosis also known as fetor oris or oral malodor or bad breath has an influence on the social interaction and confidence of the person.  The high prevalence of moderate halitosis is seen among world's population, whereas severe form of halitosis is restricted to less than 5% of the population. Main contributing factors for halitosis are local factors such as plaque, calculus, periodontal disease, dental caries, xerostomia, coating on tongue, tobacco usage, and other infections of oral cavity, followed by few systemic factors such as diabetes, upper respiratory infections, and type food. 
Halitosis occurs when pathogens in the oral cavity due to periodontal disease or coating on the tongue produce odoriferous substance. Halitosis can be tested using two main methods, organoleptic and assessment of volatile sulfur compounds (VSCs), using an electronic meter like Halimeter. ,,,, In the organoleptic method, oral malodor is assessed by the investigator at a fixed distance by smell and severity grades which are assigned on the basis of that. , VSCs are measured from sulfide monitors that detect compounds such as hydrogen sulfide, methyl mercaptan, and dimethyl sulfide which are contributing compounds for halitosis. 
Oral malodor, as perceived by the human nose, is considered to be the gold-standard halitosis test. ,, However, tests employing human olfaction are not always considered reliable as they are based on a subjective judgment by the examiner (operator). Hence, comparison of the test results between before and after treatment is difficult. Furthermore, the test cannot be considered persuasive enough for explaining the level of oral malodor. , Therefore, to judge the oral malodor level, generally, the measurement of oral malodor-producing substances using an oral malodor-analyzing device that provides objective measurement is usually employed to complement the results of a subjective organoleptic test.
The role of dentists in identifying the problem and giving effective solutions depends on the accuracy of the diagnosis made. Through an understanding of the prevalence, etiology and best available evidence on diagnostic aids for halitosis are a must. Hence, the purpose of the present study was to measure the oral malodor of volunteers by means of a subjective organoleptic method and VSCs monitoring as well as to evaluate the diagnostic value of the Halimeter in the diagnosis of halitosis.
| Materials and Methods|| |
A cross-sectional observational study was conducted to compare the two diagnostic aids for halitosis. The sample size was calculated using the previously available literature.  The ethical clearance for the study was obtained from the Institutional Review Board. One hundred and ten male volunteers were recruited from the study population, between the ages of 18 and 45 years selected from academic staff, students, and patients of College of Dentistry, Prince Sattam Bin Abdulaziz University, Al Kharj, Saudi Arabia, who responded to local recall program and agreed to take part in this study. Exclusion criteria were individuals with self-reporting systemic diseases, affecting breath odor such as hepatic cirrhosis, diabetes mellitus, uremia, and sinusitis.
All the study participants were asked to avoid any kind of food and drinks 8 h before the test. They were also asked to refrain from eating garlic or onions for 24 h before assessment. They were also asked to abstain from toothbrushing, using toothpaste, mouthwash, breath fresheners, and scented cosmetics, the morning of testing. On the day of examination in morning hours, participants were first assessed using the organoleptic method and then the sulfide monitor. The organoleptic evaluation was done by two different investigators who were trained and calibrated with a kappa value of 0.92.
The organoleptic measurement of breath was taken at distances of 10 cm and 1.5 m from the oral cavity. Severity grades were assigned as follows: 0: No oral malodor; 1: Slight oral malodor; 2: Moderate oral malodor; 3: Strong oral malodor; 4: Very strong oral malodor. 
Organoleptic scores were then recorded independently by each investigator on an ordinal scale as follows:
0: No malodor
1: Slight malodor
2: Clearly noticeable malodor
3: Strong malodor.
Each subject was then evaluated with a sulfide monitor (Halimeter) test. Patients were asked to keep their mouths closed for 3 min before testing while breathing through the nose. After 3 min, a disposable suction tip was mounted on the handpiece of Halimeter and inserted into the subject's mouth and the subjects were asked to exhale briefly through the suction tip for 30 s. The procedure was repeated in three trials for each subject, and in each turn, the peak value was recorded by the Halimeter. Then, the mean value of the peak recordings was calculated, and the final value for the VSCs for each patient was recorded in parts per billion (ppb) sulfide equivalents. According to the manufacturer's instructions, Halimeter measurements were divided into three categories as follows: 
- Normal: 80-160 ppbs
- Weak: 160-250 ppbs
- Strong: >250 ppbs.
The data were subjected to statistical analysis using the Statistical Package for Social Sciences 19.0 (SPSS version 19.0, IBM, Chicago, IL, USA). The correlation between the organoleptic score and the sulfide monitor score was determined using Kendall's tau-b correlation coefficient. Specificity, positive predictive value (PPV), negative predictive value (NPV), and disease prevalence were calculated for the sulfide monitor test. Receiver operating characteristic (ROC) curve was used to determine the diagnostic values of sulfide monitor grades to differentiate individuals with and without halitosis. The area under the ROC curve was calculated. Kappa statistics was used to check the inter- and intra-examiner calibration. The statistical significance was set at 5% level of significance (P < 0.05).
| Results|| |
The study population included 110 volunteers between the ages of 18 and 45 years. All the participants were male. [Table 1] shows the organoleptic score and sulfide monitor grades for the study participants. Among the participants, the organoleptic scores were as follows: 57 (51.82%) participants were assigned Score 0, 33 (30%) participants were assigned Score 1, 12 (10.91%) were assigned Score 2, and 8 (7.27%) participants were assigned Score 3. According to the manufactures' guide, 83 subjects (75.45%) had a sulfide monitor value of the normal range (80-160 ppb or below). Twenty-two (20.00%) had slight (160-250 ppb), and 5 (4.55%) had a strong halitosis (>250 ppb). The Kendall's tau-b correlation coefficient between Halimeter grading and the organoleptic score was −0.1090, which was not statistically significant (P = 0.2170).
|Table 1: Association between organoleptic score and sulfide monitor grades for 110 patients|
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The subjects were divided into four groups based on the organoleptic score (0 as without halitosis and >1 as with halitosis) and the degree of halitosis estimated by sulfide monitor values (<160 ppb as normal and >160 ppb as abnormal) as depicted in [Table 2]. Sensitivity, specificity, PPV, NPV, and disease prevalence were calculated for the sulfide monitor test as shown in [Table 3].
|Table 2: Characterizing individual's organoleptic score and sulfide monitor grades|
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Sensitivity and specificity of sulfide monitor grades for detecting individuals with and without halitosis were 20.75% and 66.67%, respectively. The PPV for the Halimeter was 36.67%, and the NPV was 47.50%. A ratio of 48.18% of all subjects was differentiated accurately. The area under the ROC curve was 0.5790 (95% confidence interval: 0.4600-0.6980), and the estimated curve was defined as Y = −0.6930-0.647 (X) [Figure 1].
|Figure 1: Receiver operating characteristic curves to determine the diagnostic values of sulfide monitor grades which differentiate individuals with and without halitosis|
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| Discussion|| |
The present study was conducted to measure the oral malodor of volunteers by means of a subjective organoleptic method and VSCs monitoring as well as to evaluate the diagnostic value of the Halimeter in the diagnosis of halitosis. When an attempt was made to establish a correlation between the qualitative, i.e., organoleptic measurements, and quantitative, i.e. Halimeter readings, we found a nonsignificant correlation (Kendall's tau = −0.109). This observation was similar to those by Grover et al.,  Figueiredo et al.,  Quirynen et al.,  and in contrast to the studies done by Baharvand et al. 2008,  Bosy et al.,  Rosenberg et al. 1991a,  Rosenberg et al. 1991b,  Shimura et al. 1997,  and Oho et al., 2001,  where they found significant correlation between the organoleptic and the VSC score with the extent of this correlation expressed as Spearman's rho ranging 0.49-0.82.18. In the present study, the sensitivity and specificity of sulfide monitor grades for detecting individuals with and without halitosis were 20.75% and 66.67%, respectively. These values were lower than those reported by Baharvand et al. 2008  and Oho et al. 2001.  The contrasting results of the various studies may be attributed to the difference in the sample size, variation in the characteristics of the study participants, variation in the method of calibration of the examiners, the inability of the participants to follow instructions of using Halimeter, and difference in the calibration of the Halimeter instrument.
The organoleptic method employing olfaction remains the gold-standard in detecting oral halitosis. The reason for this is the fact that in contrast to the Halimeter, which identifies only VSCs, the human nose is capable of smelling not only the VSCs but also the other organic compounds that come from exhalation and defining them as pleasant/unpleasant. Rosenberg and McCulloch have authored the most widely used organoleptic scoring system for ranking halitosis. , The organoleptic measurement depends on a trained examiner that has demonstrated reliability in smelling halitosis. Haas et al.  have demonstrated, under a blind evaluation, good levels of reproducibility of organoleptic oral malodor measurements. In the present study, a kappa value of 0.92 was obtained indicating an excellent inter-examiner reliability for the organoleptic method. However, the subjectivity of organoleptic ratings may undermine the reliability of this approach. ,
Owing to the limitations of the organoleptic method, objective assessment has always been desired for measuring oral malodor. The most commonly detected malodorants in halitosis are VSCs, such as hydrogen sulfide and methyl mercaptan and a few others. The Halimeter (Interscan, Chatsworth, USA) is a chairside instrument which provides both the patient and the professional an idea regarding the halitosis. A Halimeter score of ≥75 ppb is recognized as clearly detected halitosis. It is imperative for the clinician to understand that VSC assessment is affected by a number of confounding factors, such as circadian variation and environmental conditions. , In addition, it has been established that Halimeter can detect no other odoriferous compounds than VSCs. In addition, the sensitivity of the instrument reduces over time and has to recalibrate periodically.  Furthermore, the equipment reading may be biased by ambient conditions, such as local winds, humid environment, and presence of pollution in the air. Variability in the patients' force of breathing the air on the breath checker may also be an issue as multiple air exhausts on the equipment may be required. The number of VSCs in the breath reduces with each successive exhaust, thereby leading to very low or zero reading on the Halimeter which will lead to an incorrect assessment of the halitosis. 
Among the various quantitative measures available, Halimeter is the only device which presents the concentration of VSCs in ppb. It is, therefore, very useful for monitoring the progress of the treatment of halitosis.  Other methods, such as organoleptic examination, Halitox, or Fresh Kiss, only allow a classification into categories. Some authors have reported Halimeter values under 100 ppb VSCs as the normal range;  however, the manufacturer of the Halimeter describes the normal range as 50-150 ppb VSC. Still, other authors give normal values ranging between 70 and 110 ppb VSC. ,
Halitosis is a crippling social problem affecting a large number of people, but still neglected by dental professionals. The most common cause of halitosis is related to microbiota of oral cavity.  Several methods are available in the market for the measurement of halitosis, but more than an objective assessment, halitosis is a subjective perception of people. Oral malodor resulting from intraoral causes can be easily and effectively treated with proper maintenance of oral hygiene. However, halitosis originating from extraoral causes needs to be thoroughly explored and can provide clues regarding the underlying systemic condition of the patient. Hence, halitosis may seem to be a minor problem, but it may have the wider implications that warrant its treatment at a priority basis. 
| Conclusion|| |
The combination of Halimeter and organoleptic approaches enables simple, reliable, and fast diagnosis of halitosis. To eliminate confounding factors, it is very important to standardize the procedural methods and properly instruct the patients before measurements are taken.
Financial support and sponsorship
Conflicts of interest
There are no conflicts of interest.
| References|| |
American Academy of Periodontology. Glossary of Periodontal Terms. 4 th
ed. Chicago: American Academy of Periodontology; 2001. p. 56.
Sanz M, Roldán S, Herrera D. Fundamentals of breath malodour. J Contemp Dent Pract 2001;2:1-17.
Rösing CK, Loesche W. Halitosis: An overview of epidemiology, etiology and clinical management. Braz Oral Res 2011;25:466-71.
Yoneda M, Masuo Y, Suzuki N, Iwamoto T, Hirofuji T. Relationship between the ß-galactosidase activity in saliva and parameters associated with oral malodor. J Breath Res 2010;4:017108.
Kleinberg I, Codipilly M. Modeling of the oral malodor system and methods of analysis. Quintessence Int 1999;30:357-69.
Salako NO, Philip L. Comparison of the use of the Halimeter and the Oral Chroma™ in the assessment of the ability of common cultivable oral anaerobic bacteria to produce malodorous volatile sulfur compounds from cysteine and methionine. Med Princ Pract 2011;20:75-9.
De Boever EH, De Uzeda M, Loesche WJ. Relationship between volatile sulfur compounds, BANA-hydrolyzing bacteria and gingival health in patients with and without complaints of oral malodor. J Clin Dent 1994;4:114-9.
Kazor CE, Mitchell PM, Lee AM, Stokes LN, Loesche WJ, Dewhirst FE, et al.
Diversity of bacterial populations on the tongue dorsa of patients with halitosis and healthy patients. J Clin Microbiol 2003;41:558-63.
Rosenberg M, Septon I, Eli I, Bar-Ness R, Gelernter I, Brenner S, et al
. Halitosis measurement by an industrial sulphide monitor. J Periodontol 1991;62:487-9.
Rosenberg M, Kulkarni GV, Bosy A, McCulloch CA. Reproducibility and sensitivity of oral malodor measurements with a portable sulphide monitor. J Dent Res 1991;70:1436-40.
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.
Kameyama A, Ishii K, Tomita S, Tatsuta C, Sugiyama T, Ishizuka Y, et al.
Correlations between perceived oral malodor levels and self-reported oral complaints. Int J Dent 2015;2015:343527.
Nalçaci R, Sönmez IS. Evaluation of oral malodor in children. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2008;106:384-8.
Aylikci BU, Colak H. Halitosis: From diagnosis to management. J Nat Sci Biol Med 2013;4:14-23.
Bollen CM, Beikler T. Halitosis: The multidisciplinary approach. Int J Oral Sci 2012;4:55-63.
Baharvand M, Maleki Z, Mohammadi S, Alavi K, Moghaddam EJ. Assessment of oral malodor: A comparison of the organoleptic method with sulfide monitoring. J Contemp Dent Pract 2008;9:76-83.
Grover HS, Blaggana A, Jain Y, Saini N. Detection and measurement of oral malodor in chronic periodontitis patients and its correlation with levels of select oral anaerobes in subgingival plaque. Contemp Clin Dent 2015;6 Suppl 1:S181-7.
Figueiredo LC, Rosetti EP, Marcantonio E Jr., Marcantonio RA, Salvador SL. The relationship of oral malodor in patients with or without periodontal disease. J Periodontol 2002;73:1338-42.
Quirynen M, Mongardini C, van Steenberghe D. The effect of a 1-stage full-mouth disinfection on oral malodor and microbial colonization of the tongue in periodontitis. A pilot study. J Periodontol 1998;69:374-82.
Bosy A, Kulkarni GV, Rosenberg M, McCulloch CA. Relationship of oral malodor to periodontitis: Evidence of independence in discrete subpopulations. J Periodontol 1994;65:37-46.
Shimura M, Watanabe S, Iwakura M, Oshikiri Y, Kusumoto M, Ikawa K, et al.
Correlation between measurements using a new halitosis monitor and organoleptic assessment. J Periodontol 1997;68:1182-5.
Oho T, Yoshida Y, Shimazaki Y, Yamashita Y, Koga T. Characteristics of patients complaining of halitosis and the usefulness of gas chromatography for diagnosing halitosis. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2001;91:531-4.
Rosenberg M, McCulloch CA. Measurement of oral malodor: Current methods and future prospects. J Periodontol 1992;63:776-82.
Haas AN, Silveira EM, Rösing CK. Effect of tongue cleansing on morning oral malodour in periodontally healthy individuals. Oral Health Prev Dent 2007;5:89-94.
Loesche WJ, Kazor C. Microbiology and treatment of halitosis. Periodontol 2000 2002;28:256-79.
ADA Council on Scientific Affairs. Oral malodor. J Am Dent Assoc 2003;134:209-14.
Stassinakis A, Hugo B, Hotz P. Halitosis: Causes, diagnosis and treatment. Schweiz Monatsschr Zahnmed 2002;112:226-37.
Seemann R. Wenn der atem stinkt. Zahnärztl Mitt 2000;90:502-5.
Filippi A. Patienten mit mundgeruch in der zahnärztlichen praxis. 1. Berlin: Aufl., Quintessenz; 2005.
Veeresha KL, Bansal M, Bansal V. Halitosis: A frequently ignored social condition. J Int Soc Prev Community Dent 2011;1:9-13.
[Table 1], [Table 2], [Table 3]
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