Oral Diseases (2014) 20, 787–795 doi:10.1111/odi.12198 © 2013 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd All rights reserved www.wiley.com
ORIGINAL ARTICLE
Characteristics of patients complaining of halitosis and factors associated with halitosis H-X Lu1, C Tang1, X Chen1, MCM Wong2, W Ye1 1
Department of Preventive Dentistry, Ninth People’s Hospital, Shanghai Jiao Tong University, School of Medicine, Shanghai, China; Dental Public Health, Faculty of Dentistry, University of Hong Kong, Hong Kong, China
2
OBJECTIVES: To describe the characteristics of patients who visited halitosis clinic and to investigate the factors that may associate with halitosis. MATERIALS AND METHODS: Nine hundred and eleven patients, who visited halitosis clinic for consultations, underwent organoleptic tests and volatile sulfur compound (VSC) measurements with a portable sulfide monitor. The oral health of patients, including dental caries, oral hygiene, and gingival inflammation status, was assessed. Questionnaires were used to obtain information on demographics, oral hygiene practices, and dietary habits. RESULTS: Of the 911 patients, more females than males visited the clinic. Patients’ age ranged from 18 to 82 years (mean s.d.: 40.8 14.1). Almost 30% of patients had complained of halitosis for over 5 years before looking into treatments. Approximately half of the patients selfperceived that they were unable to get close to others. Around 77% of patients had halitosis. Results of multiple logistic regressions for organoleptic scores and VSC values showed that tongue coating and tongue scraping were significantly associated with halitosis (P < 0.05). CONCLUSIONS: Among these Chinese patients, over three-quarters of patients had halitosis, and negative impacts on social communications were observed. Tongue coating was the most important factor responsible for halitosis. Oral Diseases (2014) 20, 787–795 Keywords: halitosis; periodontal disease; tongue coating
Introduction Halitosis is an oral health condition defined as an unpleasant or offensive odor to others that emits from the oral cavity, either from intra-oral or extra-oral sources (Tonze-
Correspondence: Wei Ye, Department of Preventive Dentistry, Ninth People’s Hospital, School of Medicine, Shanghai Jiao Tong University, 639 Zhizaoju Road, Shanghai, China. Tel: 86 21 33183424; Fax: 86 21 33183424; E-mail: [email protected] Received 26 May 2013; revised 3 October 2013; accepted 11 October 2013
tich and Ng, 1976; Tonzetich, 1977). Other terms described for this health condition are bad breath, oral malodor, and breath malodor. Halitosis is one of the most common complaints from patients in the dental clinic, just behind dental caries and periodontal disease (Rayman and Almas, 2008). Halitosis may be a significant concern in social situations because it is not only a health condition, but also has psychological effects that result in social and personal isolation (Sanz et al, 2001). Approximately 80% to 90% of patients have halitosis, which originates from intra-oral causes that result from proteolytic degradation by predominantly anaerobic gram-negative oral microorganisms of various sulfur-containing substrates in food debris, saliva, blood, and epithelial cells. The prominent components of halitosis are volatile sulfide compounds (VSC), especially hydrogen sulfide (H2S), methyl mercaptan (CH3SH), and dimethylsulfide [(CH3)2S], or compounds such as butyric acid, propionic acid, putrescine, and cadaverine (Tonzetich, 1977). The prevalence of halitosis has been investigated in the world population. However, due to the different assessment methods (self-perceived halitosis or objective assessment) and diversity of cutoff points used in these studies, the precise estimation of the prevalence of halitosis has not been possible to obtain (Rosing and Loesche, 2011). Current available evidence states that its prevalence varies from 22% to over 50% (Sanz et al, 2001; Outhouse et al, 2006; Nadanovsky et al, 2007; Bornstein et al, 2009a,b). In China, a large-scale epidemiological study included 2000 participants aged 15–64 years, launched in 2002. Nearly 28% of the population had halitosis according to organoleptic scores, and 20.3% to 35.4% of the participants had VSC values greater than 110 ppb and 75 ppb, respectively (Liu et al, 2006). Given the undesirable condition of halitosis, it is of interest to investigate the characteristics of patients who complained of halitosis and who visited the halitosis clinic. Although several relatively large-scale studies have been carried out in this field, these have mainly been in the Caucasian population (Delanghe et al, 1997; Seemann et al, 2006; Quirynen et al, 2009). As one-fifth of the world’s population is Chinese, it is of great
Characteristics of patients with halitosis
H-X Lu et al
788
importance to report the characteristics of this population of patients who received consultations in an oral malodor clinic. In 2009, an outpatient oral malodor clinic was implemented in the Ninth People’s Hospital of Shanghai Jiao Tong University in Shanghai, China. Over 900 Chinese patients who complained of oral malodor were examined by the same dentists (W.Y.), leading to the accumulation of a relatively large amount of clinical data. The aims of this study were to describe the characteristics of patients who visited the oral malodor clinic and to investigate the factors that may associate with oral malodor condition.
Materials and methods Study participants This study included patients who complained of oral malodor and visited an oral malodor clinic in the Department of Preventive Dentistry, Ninth People’s Hospital, School of Medicine, Shanghai Jiao Tong University (Shanghai, China) between 2009 and 2012. Exclusion criteria included age below 18 years, antibiotic therapy in the previous month, diabetes, kidney disease, chronic sinusitis or rhinitis, gastrointestinal tract disorders, chronic bronchitis, pharyngolaryngitis, anemia, and autoimmune disease. The Institutional Review Board of the Ninth People’s Hospital, School of Medicine, Shanghai Jiao Tong University, operates in accordance with the Helsinki Declaration. Ethical approval for this study was obtained from IRB of the Ninth People’s Hospital prior to implementation of the study, and written informed consent was obtained from all patients. Prior to examination, patients were given a letter with instructions: Garlic, onions, and spicy food were prohibited from being eaten 1 day before examination. Alcohol, coffee, and smoking were also to be refrained from 12 h before their appointment. To distinguish between breath malodor and morning breath, patients were allowed to brush their teeth and eat breakfast, but this had to be done 2 h before oral malodor assessment (Quirynen et al, 2009). All assessments were carried out between 8:00 and 11:30 AM. Each patient was given a clinical oral examination and a questionnaire. Questionnaire Prior to the clinical oral examination, patients were asked to complete a questionnaire. Information on oral malodor, including duration, daily patterns, self-reported halitosis, and whether they had eaten or brushed their teeth before visiting the clinic, was collected. Patients were also asked to describe what negative impacts they had experienced because of halitosis. Questions regarding demographics (gender and age), oral hygiene practices (toothbrushing frequency, use of dental floss and mouthrinse, tongue scraping habit, and utilization of dental services), and dietary habits (smoking and drinking habit, preference for meat and strong smelling foods) were also asked. Finally, medical history (i.e., diabetes, kidney disease, chronic sinusitis or rhinitis, gastrointestinal tract disorders, chronic bronchitis, pharyngolaryngitis, anemia, and autoimmune disease) and use of medication were recorded. Oral Diseases
Clinical oral examination Patients were examined by a trained and licensed dentist in regard to their dental caries experience, gingival inflammation, oral hygiene, plaque accumulation, and tongue coating. The dental caries experience of the patient was recorded by counting the number of teeth that are decayed (D), missing due to caries (M), and filled (F), for calculation of the DMFT score according to the criteria proposed by the World Health Organization (WHO, 1997). Dental caries was detected visually at the cavitation level and early caries was not recorded. Gingival inflammation and plaque accumulation were assessed using the Gingival Index (GI) and Plaque Index (PLI) at four sites per tooth (medial, distal, buccal, and lingual) for six index teeth (16, 11, 26, 36, 31, and 46) (Loe and Silness, 1963; Silness and Loe, 1964). Oral hygiene was assessed using the oral hygiene index-simplified (OHI-S), which includes the debris index-simplified (DI-S) and calculus index-simplified (CI-S), with 0 = no debris/calculus, 1 = debris/calculus less than 1/3 of the tooth surface, 2 = debris/ calculus between 1/3 and 2/3 of the tooth surface, 3 = debris/calculus more than 2/3 of the tooth surface (Greene and Vermillion, 1964). Tongue coating (TC) was scored by 0–4 measures, with 0 = no coating, 1 = thin coating less than 1/3 of the tongue, 2 = thin coating between 1/3 and 2/3 of the tongue or thick coating on 1/3 of the tongue, 3 = thin coating more than 2/3 of the tongue or thick coating between 1/3 and 2/3 of the tongue, 4 = thick coating more than 2/3 of the tongue (Rosenberg and McCulloch, 1992). Each examination was performed with a mouth-mirror and lightweight CPI probe under artificial light. To monitor intra-examiner reproducibility, 10% of patients were re-examined, and the degree of reproducibility was assessed using Cohen’s kappa statistics Intra-examiner reliability in regard to dental caries experience, plaque accumulation, and tongue coating, was 0.96, 0.85, and 0.80, respectively. Oral malodor assessment There were two measurements of oral malodor assessment: organoleptic and Halimeterâ measurements used in this study. Organoleptic scores (OS) were assessed by a trained and calibrated examiner (W.Y.) who was trained in distinguishing odors using the smell identification tests (Sensonics Inc., Haddon Heights, NJ, USA). The examiner was instructed to detect olfactory sensitivity using a series of low concentrations dilutions of the following substances: skatole, putrescine, isovaleric acid, and dimethyl disulfide. A plastic tube was inserted into the patient’s mouth, after which the patient was instructed to exhale slowly, and the dentist rated the odor at the other end of tube. OS was rated on a ‘Rosenberg Scale’ of 0–5, with 0 = absence of odor, 1 = barely noticeable odor, 2 = slight malodor, 3 = moderate malodor, 4 = strong malodor, and 5 = severe malodor (Rosenberg and McCulloch, 1992). The OS was measured twice in onetenth of patients to assess intra-examiner reproducibility. Kappa value on OS was 0.62. According to a review article by Murata et al, OS with 2 or greater is diagnosed as halitosis (Murata et al, 2002). While in some other literature, a cutoff value of 3 was used (Quirynen et al, 2009). Both cutoff values were adopted and reported in the present study.
Characteristics of patients with halitosis
H-X Lu et al
Oral malodor was also assessed using a VSC monitor termed ‘Halimeterâ’ (Interscan, Chatsworth, CA, USA). Prior to assessment, patients were asked to keep their mouth closed for at least 1 min. During the assessment, patients held a disposable tube above the posterior part of the dorsum of the tongue in their slightly opened mouth without reaching the oral mucosa or the tongue and kept breathing through their nose. The peak value displayed in parts per billion (ppb) was recorded. Data analysis Descriptive statistics (mean, standard deviation, and percentage) of general characteristics and oral malodor assessments (OS and VSC values) were presented. Chisquare tests were performed to compare general characteristics and oral malodor assessments between males and females. These tests were also used to compare oral malodor assessments (OS and VSC values) between different groups. Multiple factor analyses were performed to explore the associated factors with halitosis. OS and VSC values were dichotomized into 0 (OS < 2, OS < 3 or VSC values
ORIGINAL ARTICLE
Characteristics of patients complaining of halitosis and factors associated with halitosis H-X Lu1, C Tang1, X Chen1, MCM Wong2, W Ye1 1
Department of Preventive Dentistry, Ninth People’s Hospital, Shanghai Jiao Tong University, School of Medicine, Shanghai, China; Dental Public Health, Faculty of Dentistry, University of Hong Kong, Hong Kong, China
2
OBJECTIVES: To describe the characteristics of patients who visited halitosis clinic and to investigate the factors that may associate with halitosis. MATERIALS AND METHODS: Nine hundred and eleven patients, who visited halitosis clinic for consultations, underwent organoleptic tests and volatile sulfur compound (VSC) measurements with a portable sulfide monitor. The oral health of patients, including dental caries, oral hygiene, and gingival inflammation status, was assessed. Questionnaires were used to obtain information on demographics, oral hygiene practices, and dietary habits. RESULTS: Of the 911 patients, more females than males visited the clinic. Patients’ age ranged from 18 to 82 years (mean s.d.: 40.8 14.1). Almost 30% of patients had complained of halitosis for over 5 years before looking into treatments. Approximately half of the patients selfperceived that they were unable to get close to others. Around 77% of patients had halitosis. Results of multiple logistic regressions for organoleptic scores and VSC values showed that tongue coating and tongue scraping were significantly associated with halitosis (P < 0.05). CONCLUSIONS: Among these Chinese patients, over three-quarters of patients had halitosis, and negative impacts on social communications were observed. Tongue coating was the most important factor responsible for halitosis. Oral Diseases (2014) 20, 787–795 Keywords: halitosis; periodontal disease; tongue coating
Introduction Halitosis is an oral health condition defined as an unpleasant or offensive odor to others that emits from the oral cavity, either from intra-oral or extra-oral sources (Tonze-
Correspondence: Wei Ye, Department of Preventive Dentistry, Ninth People’s Hospital, School of Medicine, Shanghai Jiao Tong University, 639 Zhizaoju Road, Shanghai, China. Tel: 86 21 33183424; Fax: 86 21 33183424; E-mail: [email protected] Received 26 May 2013; revised 3 October 2013; accepted 11 October 2013
tich and Ng, 1976; Tonzetich, 1977). Other terms described for this health condition are bad breath, oral malodor, and breath malodor. Halitosis is one of the most common complaints from patients in the dental clinic, just behind dental caries and periodontal disease (Rayman and Almas, 2008). Halitosis may be a significant concern in social situations because it is not only a health condition, but also has psychological effects that result in social and personal isolation (Sanz et al, 2001). Approximately 80% to 90% of patients have halitosis, which originates from intra-oral causes that result from proteolytic degradation by predominantly anaerobic gram-negative oral microorganisms of various sulfur-containing substrates in food debris, saliva, blood, and epithelial cells. The prominent components of halitosis are volatile sulfide compounds (VSC), especially hydrogen sulfide (H2S), methyl mercaptan (CH3SH), and dimethylsulfide [(CH3)2S], or compounds such as butyric acid, propionic acid, putrescine, and cadaverine (Tonzetich, 1977). The prevalence of halitosis has been investigated in the world population. However, due to the different assessment methods (self-perceived halitosis or objective assessment) and diversity of cutoff points used in these studies, the precise estimation of the prevalence of halitosis has not been possible to obtain (Rosing and Loesche, 2011). Current available evidence states that its prevalence varies from 22% to over 50% (Sanz et al, 2001; Outhouse et al, 2006; Nadanovsky et al, 2007; Bornstein et al, 2009a,b). In China, a large-scale epidemiological study included 2000 participants aged 15–64 years, launched in 2002. Nearly 28% of the population had halitosis according to organoleptic scores, and 20.3% to 35.4% of the participants had VSC values greater than 110 ppb and 75 ppb, respectively (Liu et al, 2006). Given the undesirable condition of halitosis, it is of interest to investigate the characteristics of patients who complained of halitosis and who visited the halitosis clinic. Although several relatively large-scale studies have been carried out in this field, these have mainly been in the Caucasian population (Delanghe et al, 1997; Seemann et al, 2006; Quirynen et al, 2009). As one-fifth of the world’s population is Chinese, it is of great
Characteristics of patients with halitosis
H-X Lu et al
788
importance to report the characteristics of this population of patients who received consultations in an oral malodor clinic. In 2009, an outpatient oral malodor clinic was implemented in the Ninth People’s Hospital of Shanghai Jiao Tong University in Shanghai, China. Over 900 Chinese patients who complained of oral malodor were examined by the same dentists (W.Y.), leading to the accumulation of a relatively large amount of clinical data. The aims of this study were to describe the characteristics of patients who visited the oral malodor clinic and to investigate the factors that may associate with oral malodor condition.
Materials and methods Study participants This study included patients who complained of oral malodor and visited an oral malodor clinic in the Department of Preventive Dentistry, Ninth People’s Hospital, School of Medicine, Shanghai Jiao Tong University (Shanghai, China) between 2009 and 2012. Exclusion criteria included age below 18 years, antibiotic therapy in the previous month, diabetes, kidney disease, chronic sinusitis or rhinitis, gastrointestinal tract disorders, chronic bronchitis, pharyngolaryngitis, anemia, and autoimmune disease. The Institutional Review Board of the Ninth People’s Hospital, School of Medicine, Shanghai Jiao Tong University, operates in accordance with the Helsinki Declaration. Ethical approval for this study was obtained from IRB of the Ninth People’s Hospital prior to implementation of the study, and written informed consent was obtained from all patients. Prior to examination, patients were given a letter with instructions: Garlic, onions, and spicy food were prohibited from being eaten 1 day before examination. Alcohol, coffee, and smoking were also to be refrained from 12 h before their appointment. To distinguish between breath malodor and morning breath, patients were allowed to brush their teeth and eat breakfast, but this had to be done 2 h before oral malodor assessment (Quirynen et al, 2009). All assessments were carried out between 8:00 and 11:30 AM. Each patient was given a clinical oral examination and a questionnaire. Questionnaire Prior to the clinical oral examination, patients were asked to complete a questionnaire. Information on oral malodor, including duration, daily patterns, self-reported halitosis, and whether they had eaten or brushed their teeth before visiting the clinic, was collected. Patients were also asked to describe what negative impacts they had experienced because of halitosis. Questions regarding demographics (gender and age), oral hygiene practices (toothbrushing frequency, use of dental floss and mouthrinse, tongue scraping habit, and utilization of dental services), and dietary habits (smoking and drinking habit, preference for meat and strong smelling foods) were also asked. Finally, medical history (i.e., diabetes, kidney disease, chronic sinusitis or rhinitis, gastrointestinal tract disorders, chronic bronchitis, pharyngolaryngitis, anemia, and autoimmune disease) and use of medication were recorded. Oral Diseases
Clinical oral examination Patients were examined by a trained and licensed dentist in regard to their dental caries experience, gingival inflammation, oral hygiene, plaque accumulation, and tongue coating. The dental caries experience of the patient was recorded by counting the number of teeth that are decayed (D), missing due to caries (M), and filled (F), for calculation of the DMFT score according to the criteria proposed by the World Health Organization (WHO, 1997). Dental caries was detected visually at the cavitation level and early caries was not recorded. Gingival inflammation and plaque accumulation were assessed using the Gingival Index (GI) and Plaque Index (PLI) at four sites per tooth (medial, distal, buccal, and lingual) for six index teeth (16, 11, 26, 36, 31, and 46) (Loe and Silness, 1963; Silness and Loe, 1964). Oral hygiene was assessed using the oral hygiene index-simplified (OHI-S), which includes the debris index-simplified (DI-S) and calculus index-simplified (CI-S), with 0 = no debris/calculus, 1 = debris/calculus less than 1/3 of the tooth surface, 2 = debris/ calculus between 1/3 and 2/3 of the tooth surface, 3 = debris/calculus more than 2/3 of the tooth surface (Greene and Vermillion, 1964). Tongue coating (TC) was scored by 0–4 measures, with 0 = no coating, 1 = thin coating less than 1/3 of the tongue, 2 = thin coating between 1/3 and 2/3 of the tongue or thick coating on 1/3 of the tongue, 3 = thin coating more than 2/3 of the tongue or thick coating between 1/3 and 2/3 of the tongue, 4 = thick coating more than 2/3 of the tongue (Rosenberg and McCulloch, 1992). Each examination was performed with a mouth-mirror and lightweight CPI probe under artificial light. To monitor intra-examiner reproducibility, 10% of patients were re-examined, and the degree of reproducibility was assessed using Cohen’s kappa statistics Intra-examiner reliability in regard to dental caries experience, plaque accumulation, and tongue coating, was 0.96, 0.85, and 0.80, respectively. Oral malodor assessment There were two measurements of oral malodor assessment: organoleptic and Halimeterâ measurements used in this study. Organoleptic scores (OS) were assessed by a trained and calibrated examiner (W.Y.) who was trained in distinguishing odors using the smell identification tests (Sensonics Inc., Haddon Heights, NJ, USA). The examiner was instructed to detect olfactory sensitivity using a series of low concentrations dilutions of the following substances: skatole, putrescine, isovaleric acid, and dimethyl disulfide. A plastic tube was inserted into the patient’s mouth, after which the patient was instructed to exhale slowly, and the dentist rated the odor at the other end of tube. OS was rated on a ‘Rosenberg Scale’ of 0–5, with 0 = absence of odor, 1 = barely noticeable odor, 2 = slight malodor, 3 = moderate malodor, 4 = strong malodor, and 5 = severe malodor (Rosenberg and McCulloch, 1992). The OS was measured twice in onetenth of patients to assess intra-examiner reproducibility. Kappa value on OS was 0.62. According to a review article by Murata et al, OS with 2 or greater is diagnosed as halitosis (Murata et al, 2002). While in some other literature, a cutoff value of 3 was used (Quirynen et al, 2009). Both cutoff values were adopted and reported in the present study.
Characteristics of patients with halitosis
H-X Lu et al
Oral malodor was also assessed using a VSC monitor termed ‘Halimeterâ’ (Interscan, Chatsworth, CA, USA). Prior to assessment, patients were asked to keep their mouth closed for at least 1 min. During the assessment, patients held a disposable tube above the posterior part of the dorsum of the tongue in their slightly opened mouth without reaching the oral mucosa or the tongue and kept breathing through their nose. The peak value displayed in parts per billion (ppb) was recorded. Data analysis Descriptive statistics (mean, standard deviation, and percentage) of general characteristics and oral malodor assessments (OS and VSC values) were presented. Chisquare tests were performed to compare general characteristics and oral malodor assessments between males and females. These tests were also used to compare oral malodor assessments (OS and VSC values) between different groups. Multiple factor analyses were performed to explore the associated factors with halitosis. OS and VSC values were dichotomized into 0 (OS < 2, OS < 3 or VSC values
