ORIGINAL ARTICLE
Effect of Clinician’s Experience, Age, Gender and Calibration on the Assessment of Halitosis ùehrazat Evirgena/Kıvanç Kamburo÷lub/Ayse Gulsahic Purpose: To evaluate the diagnosis of halitosis in relation to the oral malodour judge’s experience, age, gender and calibration. Materials and Methods: This study included 38 dental patients who volunteered to participate. Patients were evaluated for halitosis by 6 clinicians using the organoleptic method and by measuring mouth exhaled air using a halimeter, which is considered the gold standard. Sensitivity, specificity, and positive and negative predictive values were calculated for each clinician. Consistency between clinicians was evaluated through a kappa test. Significance level was set at P < 0.05. Results: Out of the 38 patients, 14 were diagnosed with halitosis by 6 clinicians using a halimeter. The highest sensitivity (89%) was found for clinician No. 6, followed by clinician No. 5 (78%). Specificities were 57% for clinician No. 4 and 36% for clinician No. 1 and No. 5. The most correct positive predictive value (halitosis according to halimeter readings) was made by clinician No. 6 (65%), who also had the highest rates (83%) of negative predictive value (no halitosis according to halimeter readings). There were no statistically significant differences (P > 0.05) between the diagnoses of clinicians No. 1, 2, 3, 5, or 6; however, the diagnoses made by clinician No. 4 were statistically different (P < 0.05) than those of all other clinicians. The highest rate of agreement (44%) in diagnoses was between the two calibrated clinicians. However, there was no correlation between the halitosis diagnoses and the age, gender and years of experience of the clinicians. Conclusions: This study indicates that calibration of clinicians is a significant factor in the organoleptic evaluation of halitosis. Key words: bad breath, halitosis, oral clinician’s calibration, organoleptic method Oral Health Prev Dent 2013; 11: 17-22
H
alitosis, or oral malodour, is a common complaint among dental patients (Rosenberg and McCulloch, 1992; Iwakura et al, 1994; Al-Ansari et al, 2006). In the large majority of the cases, halitosis originates in the oral cavity as the result of microbial putrefaction (Rosenberg and McCulloch, 1992). Halitosis of oral aetiology may result from periodontal disease, poor saliva flow, improper den-
a
Researcher, Faculty of Dentistry, Oral Diagnosis and Radiology Department, Ankara, Ankara University, Turkey.
b
Associate Professor, Faculty of Dentistry, Oral Diagnosis and Radiology Department, Ankara, Ankara University, Turkey.
c
Associate Professor, Faculty of Dentistry, Oral Diagnosis and Radiology Department, Ankara, Baskent University, Turkey.
Correspondence: Dr. Sehrazat Evirgen, Medikal Park Izmir Hospital, Yeni Girne Bulvari 1825 St. No:12, Karsiyaka, Izmir, Turkey. Tel: +900532-516-8298. Email:
[email protected]
Vol 11, No 1, 2013
Submitted for publication 11.3.12; accepted for publication 28.4.12
tal restorations, excessive microbial colonisation of the tongue, or diet (Rosenberg and McCulloch, 1992; Lee et al, 2004). Non-oral aetiologies may include upper and lower respiratory tract conditions, neurologic and gastrointestinal disorders, various systemic diseases and use of certain drugs (Rosenberg and McCulloch, 1992). There are few studies evaluating the prevalence of oral malodour in the general population, with reported rates ranging from 22% to more than 50% (Yaegaki and Coil, 2000; Al-Ansari et al, 2006). According to the American Dental Association, approximately 50% of the adult population has had at the least an occasional complaint of oral malodour, while 25% appear to have a severe, chronic problem (ADA Council on Scientific Affairs, 2003). Consequently, this condition has recently begun to receive increased professional and commercial interest in terms of both aetiological factors and therapeutic measures
17
Evirgen et al
(ADA Council on Scientific Affairs, 2003; Al-Ansari et al, 2006). Halitosis is generally diagnosed by organoleptic examination and/or chromatographic analysis of the main source of halitosis, i.e. volatile sulphur compounds (VSC), such as hydrogen sulphide and methyl mercaptan in mouth air (Iwakura et al, 1994). Organoleptic, or ‘hedonic’ assessment consists of direct sniffing of expelled mouth air and is the simplest and most commonly used approach to sample and measure oral malodour. In one sense, this method may be considered a gold standard of oral malodour measurement (Rosenberg and McCulloch, 1992). Alternatively, VSC concentration in the oral cavity can be measured using a halimeter, a portable instrument that is sensitive to volatile compounds and which requires calibration to the background air before taking a reading (Lee et al, 2004). There is little information available on how examiners for bad breath assessment should be selected or excluded. Therefore, the aim of this study was to evaluate the diagnosis of halitosis in relation to the oral malodor clinician’s experience, age, gender and calibration.
Organoleptic measurements Patients were instructed to close their mouths for 30 seconds and then exhaled briefly through the mouth at a distance of 10 to 20 cm from the nose of the clinician. Oral malodour was rated using a 6-point scale (Rosenberg et al, 1991a; Rosenberg et al, 1991b; Greenman et al, 2005) that rates odour intensity as follows: r r r r r r
0: No malodour (below the detectable threshold) 1: Barely noticeable odour 2: Slight odour 3: Moderate odour 4: Strong odour 5: Extremely strong odour
Prior to taking measurements from patients, two of the clinicians (No. 5 and No. 6) were calibrated by smelling test strips dipped in 0, 10, 50, 100, 500 and 1000 ppb concentration of methyl mercaptan (prepared at the Ankara University Faculty of Sciences, Department of Chemistry), as described in previous studies (Shimura et al, 1996).
Halimeter measurements
MATERIALS AND METHODS This study included voluntary participation of 38 patients referred to the Ankara University Faculty of Dentistry for dental treatment. Volunteers were asked to fill out a consent form after which they were evaluated for halitosis by 6 clinicians using the organoleptic method. Of the six clinicians, 3 were male and 3 were female with ages ranging from 25 to 46 years (Table 1).
Standardization of the patients Patients were asked to refrain from eating any food that might generate a strong odour on both the day before and the morning of the test. Patients were also asked to refrain from smoking, chewing gum, wearing scented personal care products, tooth brushing, oral rinsing and eating immediately before the visit.
18
Following organoleptic examination, VSC values for all patients were recorded using a halimeter (Model RH-17 Halimeter, Interscan; Simi Valley, CA, USA). Measurements were taken according to the manufacturer’s instructions. In order to provide adequate accumulation of VSCs, patients were instructed to close their mouths for 2 to 3 minutes and breathe from the nose before the initial measurement with the halimeter. The first measurement was performed after adjustment of the halimeter’s reset button. A value between -10 and +10 appearing on the digital screen of the device was considered acceptable (as per the instructions given in the manuel for the halimeter). Once an acceptable value was obtained, the subjects was asked to open his/her mouth slightly, and a straw probe (for RH-17 series Halimeter, Interscan) was placed 3 to 4 cm inside the mouth, taking care not touch teeth, mouth, or other tissues in the mouth. The patient was instructed not to close his/her lips, blow, or suck, and to breathe from the nose. Once the maximum value was reached, as indicated on the digital screen, the probe was removed from the mouth and the VSC value (ppb) appearing on the halimeter’s digital display monitor was recorded. This procedure was re-
Oral Health & Preventive Dentistry
Evirgen et al
Table 1 Distribution of oral malodor judges, gender, age and occupational experience Judge No
Gender
Age
Occupational experience (years)
1
Female
30
9
2
Female
46
24
3
Male
25
1
4
Male
37
16
5
Male
36
12
6
Female
35
12
Table 2 Evaluation of the organoleptic measurements performed by six different clinicians and halimeter measurements Clinician No
Sensitivity (%)
Specificity (%)
Positive predictive value (%)
Negative predictive value (%)
1
68
36
52
53
2
63
42
52
53
3
68
42
54
57
4
68
57
61
64
5
78*
36
55
63
6
89*
52
65
83
P < 0.05*
peated twice, and the average of the 3 recorded values was computed. After the probe was taken away from the mouth, the value on the indicator went down slowly to finally reach negative values. Halitosis was evaluated based on the same standard or definition mentioned in the previous reports (Miyazaki et al, 1995; Furne et al, 2002). Halitosis was diagnosed if the average level of VSC was ≥ 125 ppb and the organoleptic measurement using a 0 to 5 point scale was ≥ 2. Physiological halitosis was diagnosed if the average level of VSC was ≥ 75 ppb (Iwanicka-Grzegorek et al, 2005) and the organoleptic measurement using the 0 to 5 point scale was 1. The classification of halitosis proposed by Yaegaki and Coil (2000) was used in the present study. Results obtained by both methods were recorded. The sensitivity, specificity, and positive and negative predictive values were calculated and recorded for each clinician. The consistency between clinicians was evaluated through kappa test. Significance level was set at P < 0.05.
Vol 11, No 1, 2013
RESULTS Of the total 38 subjects participating in this study, 14 were diagnosed with halitosis using a halimeter by 6 dentists. Organoleptic measurements performed by 6 different dentists were evaluated by the validity of halimeter readings test, which is considered the gold standard. The results are presented in Table 2. The sensitivity (89%) made by clinician No. 6 was followed by clinician No. 5 (78%). Specificities were (57%) for clinician No. 4 and (36%) for clinicians No. 1 and No. 5. The most correct positive predictive value (halitosis according to halimeter readings) was made by clinician No. 6 (65%), who also had the highest rates (83%) of negative predictive value (no halitosis according to halimeter readings). Agreement between the organoleptic measurements of the dentists was evaluated by the Kappa coefficient (Table 3). There were no statistically significant differences between the diagnoses of clinicians No. 1, 2, 3, 5, or 6; however, the diagnoses
19
Evirgen et al
Table 3 Consistency test of the organoleptic measurements performed by six different clinicians (Kappa Test)
Clinician No. 1 Clinician No. 2
Clinician No. 2
Clinician No. 3
Clinicain No. 4
Clinician No. 5
Clinician No. 6
%
%
%
%
%
21
37*
24
39*
23
28
14
42*
37*
30
47*
42*
23
40*
Clinician No. 3 Clinician No. 4 Clinician No. 5
44*
*P < 0.05
made by clinician No. 4 were statistically different than those of all other clinicians. This shows that organoleptic calibration removes the difference between the clinicians with regard to specificity. The highest rate of agreement (44%) in diagnoses was between the two calibrated dentists, clinician No. 6 and clinician No. 5, despite the fact that they were of different sex and had different occupational experiences. In addition, there was no correlation between halitosis diagnosis and the age, gender and experience of the clinicians.
DISCUSSION The simplest and most commonly used approach to sampling and measuring oral malodour is direct nasal sniffing of expelled mouth air. This is often referred to as organoleptic or ‘hedonic’ assessment. While researchers generally agree that the human sense of smell is capable of detecting differences in strengths and concentrations of odour molecules, different groups of researchers have used different descriptions and different scales to measure oral malodour. This study used a 0 to 5 intensity scale that is commonly used in oral malodour research (Rosenberg et al, 1991a; Rosenberg et al, 1991b). Use of the halimeter in combination with the organoleptic method has been shown to be an effective method of diagnosing halitosis, which has been confirmed by many researchers (Rosenberg, 1996; Nachnani et al, 2005). The halimeter, along with the gas chromatograph, are the instruments currently used to provide objective measurements with which to assess oral malodour. However, high-performance liquid chromatography, which is used to
20
detect polyamines, is relatively expensive and time consuming, which prohibits its use in the examination of a large subject population (Goldberg et al, 1994; Murata et al, 2002). In contrast, the halimeter, which monitors sulphide levels, is a fast, simple and inexpensive method of diagnosis (Iwanicka-Grzegorek et al, 2005). A study (Furne et al, 2002) demonstrated that the halimeter’s sulphide detector responds linearly to H2S and CH3SH, the primary VSCs in breath gas, and that the peak and plateau concentrations recorded by the halimeter correlate significantly with data obtained with gas chromatography. Thus, they concluded that the halimeter, while lacking perfect accuracy, provides useful data for the clinical study of oral malodour. In line with the above, this study used a halimeter to provide objective measurements of the oral malodour levels of patients with which to compare the subjective evaluations of the clinicians. In order to test the effects of calibration of clinicians on their ability to organoleptically assess halitosis, two of the clinicians in this study (Nos. 5 and 6) were provided with training in smelling various concentrations of methyl mercaptan. Methyl mercaptan was used both because of its very close correlation with organoleptic measurements and because it is an important component of VSC (Awano et al, 2004). Calibration is significant in organoleptic measurements in the training of the odour judges, in the recognition of oral malodour by these individuals and in providing reliability and reproducibility of the organoleptic measurements. Two of the odour judges included in the study (No. 5 and 6) were trained by smelling methyl mercaptan concentrations, thus were calibrated with each other.
Oral Health & Preventive Dentistry
Evirgen et al
In a sense, organoleptic assessment may be considered a kind of reference standard of oral malodour measurement, as it closely simulates everyday situations in which bad breath is detected. However, there are a number of problems related to this approach (Rosenberg and McCulloch, 1992). While general olfactory tests are available for selecting odour clinicians, little information is available on how clinicians for bad breath assessment should be selected. Considering that odour perception is purportedly more developed among females, it is possible that they may be better judges than males (Rosenberg and McCulloch, 1992). In one study (Doty et al, 1982), women were shown to have a more advanced sensitivity to odours compared to men. However, this study found no differences in the diagnosis of halitosis in male and female clinicians. Ability to perceive odours is known to decline with increasing age (Doty et al, 1982; Rosenberg and McCulloch, 1992). However, the present study found no correlation between halitosis diagnosis and the age of the clinician. It is also possible that individuals may become adapted to their own oral malodour and therefore be unable to diagnose halitosis in patients. Previous studies have considered individuals with mouth gas over 75 ppb as measured by a halimeter to be unsuitable judges of oral malodour (Awano et al, 2004; Iwanicka-Grzegorek et al, 2005). This study also used a halitosis value under 75 ppb as measured by a halimeter as a criterion for the selection of judges. Experience may have contradictory effects on a clinician’s subjective ability to diagnose halitosis. On the one hand, experience may be expected to improve a clinician’s ability to judge oral malodour; on the other hand, a clinician’s skills in distinguishing malodour may deteriorate as he or she becomes adapted to odours throughout their occupational experience. Just as workers in other foul-smelling environments become accustomed to workplace odours, dental professionals who are called upon to diagnose and treat halitosis in the clinical setting may become habituated to oral malodour and may therefore have a reduced ability to recognise and assess halitosis (Rosenberg and McCulloch, 1992). Periodontologists were found to be less sensitive to detection of oral malodour compared to other clinicians (Markovich et al, 1997). However, in a recent study comparing an experienced and a novice oral malodour judge, odour scores of the former were more reproducible and gave higher cor-
Vol 11, No 1, 2013
relations with instrumental sulphide analysis (Rosenberg et al, 1991a; Rosenberg et al, 1991b). In contrast, the current study found that differences in the length of occupational experience of clinicians did not result in significant differences in their organoleptic evaluation of halitosis, unless they were calibrated. Furthermore, instruction in assigning ratings to given levels of odour stimuli can improve the consistency with which clinicians diagnose halitosis. Such calibration has been found to be significant in organoleptic measurements in the training of the odour judges, in the recognition of oral malodour by these individuals and in providing reliability and reproducibility of the organoleptic measurements. Some authors (Nachnani et al, 2005) found that mistakes by oral judges decreased in a statistically significant manner with training in assessing halitosis. In an in vitro study (Markovich et al, 1997) where 37 clinicians, 33 researchers and 31 nonclinician and non-researcher individuals sniffed various artificial saliva combinations, no statistically significant difference between these 3 groups of participants was found. Differences in gender and age distribution among the 3 groups were not significant. This study also supports our results regarding different sex and occupational experiences as not being influential in malodour diagnosis. In this study, the diagnoses of the two clinicians who received training (Nos. 5 and 6) agreed most consistently with each other and with halimeter data.
CONCLUSION In conclusion, this study indicates that calibration of judges is a significant factor in the organoleptic evaluation of halitosis. No statistically significant differences were detected between the oral malodour assessment of clinicians of different gender, age and years of occupational experience. It is therefore suggested that in order to improve the diagnosis of halitosis and to evaluate the effectiveness of therapy, clinicians be calibrated to improve their consistency in assessing oral malodour. Alternatively, uncalibrated clinicians should use an objective measurement technique such as gas chromatography or halimeter in conjunction with an organoleptic assessment of malodour.
21
Evirgen et al
REFERENCES 1. ADA Council on Scientific Affairs. Oral malodor. JADA 2003;134:209–214. 2. Al-Ansari JM, Boodai H, Al-Sumait N, Al-Khabbaz AK, AlShammari KF, Salako N. Factors associated with self-reported halitosis in Kuwaiti patients. J Dent 2006;34:444–449. 3. Awano S, Koshimune E, Kurihara E, Gohara K, Sakai A, Soh I, et al. The assessment of methyl mercaptan, an important clinical marker for the diagnosis of oral malodor. J Dent 2004;32:555–559. 4. Doty RL, Gren PA, Ram C, Yankell SL. Communication of gender from human breath odors: Relationship to perceived intensity and pleasantness. Horm Behav 1982;16:13–22. 5. Furne J, Majerus G, Lenton P, Springfield J, Levitt DG, Levitt MD. Comparison of volatile sulfur compound concentrations measured with a sulfide detector vs. gas chromatography. J Dent Res 2002;81:140–143. 6. Goldberg S, Kozlovsky A, Gordon D, Gelernter I, Sintov A, Rosenberg M. Cadaverine as a putative component of oral malodor. J Dent Res 1994;73:1168–1172. 7. Greenman J, El-Maaytah M, Duffield J, Spencer P, Rosenberg M, Corry D, Saad S, Lenton P, Majerus G, Nachnani S. Assessing the relationship between concentrations of malodor compounds and odor scores from judges. JADA 2005;136:749–757. 8. Iwakura M, Yasuno Y, Shimura M, Sakamoto S. Clinical characteristics of halitosis: differences in two patient groups with primary and secondary complaints of halitosis. J Dent Res 1994;73:1568–1574. 9. Iwanicka-Grzegorek K, Lipkowska E, Kepa J, Michalik J, Wierzbicka M. Comparison of ninhydrin method of detecting amine compounds with other methods of halitosis detection. Oral Dis 2005;11(suppl 1):37–39. 10. Lee PP, Mak WY, Newsome P. The aetiology and treatment of oral halitosis: an update. Hong Kong Med J 2004;10: 414–418.
22
11. Markovich D, Goldberg S, Eli I, Rosenberg M. In vitro oral malodor assessment: are dentists different. In: Rosenberg M (ed). Bad Breath: Research Perspectives. Ramat Aviv, Tel Aviv: Ramot Publishing, 1995. 12. 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;66:679–684. 13. Murata T, Yamaga T, Lida T, Miyazaki H, Yaegaki K. Classification and examination of halitosis. Int Dent J 2002;52 Suppl 3:181–186. 14. Nachnani S, Majerus G, Lenton P, Hodges J, Magallanes E. Effects of training on odour judges scoring intensity. Oral Dis 2005;11(suppl 1):40–44. 15. Rosenberg M. Clinical assessment of bad breath: current concepts. JADA 1996;27:475–482. 16. Rosenberg M, Kulkarni GV, Bosy A, McCulloch CA. Reproducibility and sensitivity of oral malodor measurements with a portable sulphide monitor. J Dent Res 1991a;70:1436– 1440. 17. Rosenberg M, McCulloch CA. Measurement of oral malodour: current methods and future prospects. J Periodontol 1992;63:776–782. 18. Rosenberg M, Septon I, Eli H, Bar-Ness R, Gelernter I, Brenner S et al. Halitosis measurement by an industrial sulphide monitor. J Periodontol 1991b;62:487–489. 19. Shimura M, Yasuno Y, Iwakura M, Shimada Y, Sakai K, Suzuki K, Sakamoto S. A new monitor with a zinc-oxide thin film semiconductor sensor for the measurement of volatile sulfur compounds in mouth air. J Periodontol 1996;67:396–402. 20. Yaegaki K, Coil JM. Examination, classification, and treatment of halitosis; clinical perspectives. J Can Dent Assoc 2000;66:257–261.
Oral Health & Preventive Dentistry
