- Email: [email protected]
or palate
Evaluation of oral and nasal halitosis parameters in patients with repaired cleft lip and/or palate Fla´vio Monteiro-Amado, DDS,a Luiz Eduardo Montenegro Chinellato, PhD,b and Maria Lu´cia Rubo de Rezende, DDS, PhD,c Bauru, Brazil ˜ O PAULO UNIVERSIDADE OF SA
Objective. The objective of this study was to investigate the relationship between halitosis parameters in patients with and without cleft lip and/or palate.
Study design. Forty-two subjects were examined. They were divided into group I, postgraduate students of Bauru Dental School (FOB); and group II, individuals with repaired cleft lip and/or palate. The concentration of volatile sulfur compounds (VSC) was assessed with a portable sulfide monitor and the values were correlated to the salivary flow rate and weight of tongue coating. Results. There was a relationship between the presence of tongue coating and VSC levels, as well as between salivary flow rate and VSC levels in group II. The same group also revealed a significant correlation between weight of tongue coating and salivary flow rate. There were no significant differences between groups as regards the Halimeter oral measurement. Conclusions. Individuals with repaired cleft lip and/or palate can have the same VSC levels as subjects without clefts. (Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2005;100:682-7)
The etiology of halitosis includes the following: (1) local factors of pathologic origin, (2) local factors of nonpathologic origin, (3) systemic factors of pathologic origin, (4) systemic factors of nonpathologic origin, (5) administration of systemic drugs, and (6) xerostomia.1 Studies on the etiology of breath malodor agree that hydrogen sulfide (H2S), dimethyl sulfide (CH3)2S, and methylmercaptan (CH3SH), collectively referred to as volatile sulfur compounds (VSC), which are gases originated from the anaerobic bacterial degradation of sulfur-containing amino acids within the oral cavity, are the main components of offensive breath.2-5 Although several microorganisms are capable of producing volatile sulfur compounds, Treponema denticola, Porphyromonas gingivalis, Prevotella intermedia, Bacteroides forsythus, and Fusobacterium can
Financial support was from Coordenac¸a˜o de Aperfeic¸oamento de Pessoal de Nı´vel Superior. These data were presented at the 82nd General Session and Exhibition of the International Association for Dental Research/American Association for Dental Research/ Canadian Association for Dental Research, Honolulu, Hawaii, 2004. a Specialist in Dental Implantology, Hospital for Rehabilitation of Craniofacial Anomalies, Universidade of Sa˜o Paulo, and Master of Science in Stomatology by Bauru Dental School, Universidade of Sa˜o Paulo, Bauru, Brazil. b Assistant Professor, Stomatology Department, Bauru Dental School, Universidade of Sa˜o Paulo, Bauru, Brazil. c Periodontist and Implantologist, Hospital for Rehabilitation of Craniofacial Anomalies, Universidade of Sa˜o Paulo, Bauru, Brazil. Received for publication Jan 12, 2005; returned for revision Mar 7, 2005; accepted for publication Mar 23, 2005. 1079-2104/$ - see front matter Ó 2005 Mosby, Inc. All rights reserved. doi:10.1016/j.tripleo.2005.03.019
682
produce significant amounts of hydrogen sulfide and methylmercaptan from serum proteins, cysteine, and methionine.6 Evaluation of tongue coating is of special interest in the study of halitosis, since the desquamated tongue epithelium provides an ideal environment for minute food particles and bacteria capable of emitting offensive odor.7 Poor oral hygiene is probably the most common factor leading to bad breath and tends to exacerbate other causes.8 The vast majority of cases of bad breath (90%) are of oral origin,9 and tongue coating shows a direct correlation with sulfide levels,6,10-15 being responsible for nearly 50% of VSC produced in the mouth.16 Much emphasis is reported in the literature about unpleasant breath from oral sources, but there are few reports concerning the bad odor because of nasal alterations.7,17 The general low level of knowledge as to the causes of halitosis and how it is self-managed among medical and dental practitioners9,18 can contribute to the lack of a better interaction between physicians and dental clinicians in the treatment of this problem. Airway passages are described as the second main source of halitosis.19 Tonsillitis, sinusitis, and rhinitis are believed to contribute to halitosis,20 as do polyps and foreign bodies in nasal odor.21 Nevertheless, Crohn and Drosd,22 in 1941, wrote that ‘‘unless pathologic oral or nasopharyngeal conditions exist, the mouth, teeth and pharynx play little or no part in the production of essential halitosis.’’ Finkelstein,23 in 1995, described several factors that may lead to the high incidence of sinusitis in patients with clefts and then to the increased frequency of
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halitosis in these patients, such as deviated nasal septum, deformed medium turbinate, underdeveloped maxillary sinuses, maxillary growth deficits, choanal stenosis or atresia, atresia of the nostrils, malformed external nasal valve, incompetent velopharyngeal valve, presence of pharyngeal flap, and impairment of mucociliary transport. The nasal cavity may also be contaminated by saliva and food that passes from the oral to the nasal cavity through oronasal fistulae. Patients with clefts can present with reduced nasal passage as a result of ostial obstruction, septal deviation, inferior turbinate hypertrophy, valvular collapse, and reduced airflow.24,25 Pathologic conditions as those previously mentioned, affecting the nose, pharynx, or tracheobronchial tree may result in the production of objectionable odors. Virtually any condition leading to the growth of gram-negative or anaerobic microorganisms will produce an unpleasant odor.7 A preliminary work showed that individuals with cleft lip and/or palate are prone to present higher nasal VSC measurements.26 The lack of information about halitosis in patients with cleft lip and palate encouraged accomplishment of this study. The purpose was to compare the VSC levels, amount of tongue coating, and salivary flow rate among postgraduate students of Bauru Dental School, University of Sa˜o Paulo, Brazil, and individuals with repaired cleft lip and/or palate from the Hospital for Rehabilitation of Craniofacial Anomalies, University of Sa˜o Paulo, in Bauru.
MATERIAL AND METHODS Study population Two groups of patients were evaluated concerning oral and nasal halimeter measurements: group I, 21 postgraduate students of Bauru Dental School, University of Sa˜o Paulo (FOB/USP), who were supposed to present good oral hygiene; and group II, 21 individuals with repaired clefts, from the Hospital for Rehabilitation of Craniofacial Anomalies of University of Sa˜o Paulo (HRAC/USP), who worked or lived near the hospital and were examined at the Stomatology Clinic of FOB/USP. Exclusion criteria were the existence of systemic disorders (sinusitis, rhinitis, or lung, kidney, liver, and intestinal disturbances) and local factors that could affect oral malodor (poor oral hygiene, visually noticed gingivitis, or visual loss of periodontal attachment). For odor measurements, a portable sulfide monitor was used (Halimeter, Interscan Corporation, Chatsworth, Calif). The protocol was approved by the Institutional Review Board of Bauru Dental School, University of Sa˜o Paulo, and all subjects signed a written informed consent term agreeing to participate in the study.
Monteiro-Amado, Chinellato, and de Rezende 683
On the day of examination, the participants were asked not to use personal scent products and to avoid all oral activities for 3 hours prior to the appointment, including eating, chewing, drinking (except water), and any other hygiene procedures. Clinical examination Concentration of volatile sulfur compounds. After being submitted to complete intraoral examination, each patient closed the mouth for 60 seconds prior to sampling. Measurements were made in triplicate using a portable sulfide monitor (Halimeter, Interscan Corporation), and the mean value was calculated. A plastic straw was inserted and positioned above the posterior part of the tongue dorsum, not touching the oral mucosa or tongue. No breathing was allowed during each sampling; the mouth was kept slightly opened and the peak value was recorded. Then, measurements of nasal values were accomplished by inserting another plastic straw 1 cm inside each nostril, only once, until the peak value was achieved. The concentration of mouth volatile sulfur compounds was obtained in the same manner after removal of tongue coating, and 1 measurement was performed during expiration, in order to exclude possible systemic causes of halitosis that could lead to liberation of VSC by the lungs. If this measurement was lower than the measurements without tongue coating, then it could be supposed that no VSC from the lungs were being detected. Tongue coating sampling and BANA test. Although there are several microorganisms capable of performing the process of VSCs production, three in particular—T. denticola, P. gingivalis, and B. forsythus—produce a ‘‘trypsin-like’’ enzyme that can be detected by the hydrolysis of the synthetic peptide, benzoyl-DLarginine-naphthylamide, known as BANA, and it can be monitored by the use of a test called the BANA test.27 Excessive moisture from the tongue dorsum was removed with gauze, tongue coating was removed with a tongue scraper, and new measurements of oral VSC were obtained, again in triplicate. The tongue coating was put on a filter paper, previously weighed, and allowed to dry for 24 hours at room temperature, when it was weighed with a precision balance (A&D Company, Limited, Tokyo, Japan). Salivary flow rate. Resting and stimulated saliva were obtained as follows. The patient kept his or her mouth slightly open for 5 minutes, without talking or spitting, and saliva was allowed to go down into a glass recipient. The volume of saliva was assessed. Then, the patient chewed a piece of silicone rubber for 5 minutes (Saudbucal, Sa˜o Paulo, Brazil) after which he or she expectorated all saliva formed in another glass recipient, where the volume of saliva was assessed. The volume
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684 Monteiro-Amado, Chinellato, and de Rezende
Table I. Results of the paired t test between the initial variable VSC levels, after removal of tongue coating and during expiration Variable Without cleft With cleft
Initial Initial Initial Initial
sulfide sulfide sulfide sulfide
level level level level
(ppb) (ppb) (ppb) (ppb)
Mean
SD
Variable
Mean
SD
P*
88.9523 88.9523 91.8095 91.8095
73.9624 73.9624 68.8764 68.8764
Sulfide level without tongue coating (ppb) Sulfide level during expiration (ppb) Sulfide level without tongue coating (ppb) Sulfhide level during expiration (ppb)
69.4761 56.2857 66.1428 65.9047
38.0928 25.0342 51.7003 68.8737
.047 .012 .025 .084
VSC, volatile sulfur compounds. *Boldface indicates statistical significance.
Table II. Results of the independent t test between the variables in Groups I and II With cleft Variables Initial sulfide level (ppb) Sulfide level without tongue coating (ppb) Weight of tongue coating (mg) Sulfide level during expiration (ppb) Resting salivary flow rate (mL/min) Stimulated salivary flow rate (mL/min) Nasal sulfide level (ppb)
Without cleft
Mean
SD
Mean
SD
Difference*
P**
91.8095 66.1428 0.0235 65.9047 0.1628 1.2466 47.6666
68.8764 51.7003 0.0150 68.8737 0.1395 0.9382 13.9044
88.9523 69.4761 0.0139 56.2857 0.1790 1.1695 62.0000
73.9624 38.0928 0.01332 25.0342 0.1275 0.7022 20.1940
ÿ2.8571 3.3333 ÿ0.0096 ÿ9.6190 0.01619 ÿ0.0771 14.3333
.898 .813 .036 .551 .697 .764 .011
*Represents the difference between the mean values of the variables in the two groups. **Boldface indicates statistical significance.
was divided by 5 and the salivary flow rate was obtained (mL/min). Statistical analysis Results were analyzed by means of the dependent and independent t test for the following scalar quantitative variables: halitosis, salivary flow rate, and weight of tongue coating, between the 2 groups. The paired t test was used to verify the relationship between initial VSC values after removal of tongue coating and VSC values during forced expiration. The relationship between VSC measurements, tongue coating’s dry weight, and salivary flow rate was obtained by the Pearson correlation. The significance level was set at 5%. RESULTS A total of 42 individuals were evaluated, divided into 2 groups of 21 individuals each: group I, without cleft lip and/or palate, post-graduation students of Bauru Dental School; and group II, with repaired cleft lip and/or palate. Group I was composed of 13 males and 8 females with a mean age 26.2 years (range 21 to 30 years). Group II was composed of 13 males and 8 females with a mean age 24.2 years (range 19 to 33 years). Data on the parameters investigated are presented in the tables. Statistically significant values are displayed in bold letters. Table I shows that reduction in VSC levels after removal of tongue coating was statistically significant for groups I and II. Although there was reduction in VSC levels during expiration in both groups, it was only
statistically significant for group I. Group I had less tongue coating than group II, but higher nasal VSC levels (Table II). Only group II showed statistically significant correlations for the variables studied, although these correlations were all mild (Table III). DISCUSSION Persistent oral malodor affects at least 50% of the population,21 and the vast majority of cases of bad breath (90%) are of oral origin.9 It may result from microbial metabolism on the tongue dorsum and periodontium, and is modulated by low salivary flow at certain times during the day, food impaction, and diet.5,28 Its intensity is significantly related to increased oral levels of VSC,29 which are likely to arise mainly from the breakdown of cysteine, cystine, and methionine, peptides and amino acids found free in gingival crevicular fluid, in saliva, or produced as a result of proteolysis of protein substrates.30 Cadaverine, produced from the decarboxylation of lysine, may also be of some importance in malodor.31 Factors involved in the production, release, and detection of odors are reduced salivary flow rate; accumulation and putrefaction of oral epithelial debris, food, and saliva; low oxygen concentration; reduced availability of carbohydrates as bacterial substrate; and high oral pH.5,7 There are 3 main methods to evaluate exhaled air: organoleptic scales; gas chromatography; and portable sulfide monitor, which detects mainly hydrogen sulfide,
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but also, and to a lesser extent, dimethyl sulfide and methylmercaptan.4 Even though the use of gas chromatography is the most accurate method for detecting the products involved in the process of halitosis, the sulfide monitor presents other advantages, such as no need for skilled personnel, noninvasive procedures,32 low possibility of cross-infection, portability, relatively inexpensive, and rapid turnaround time of 1 to 2 minutes between measurements.4 Figueiredo et al33 reported, in 2002, that absolute levels of VSC may vary between different population groups, and this indicates that studies on VSC production and malodor should include a control population that either has no periodontal disease or no complaints of malodor. In the present study, none of the individuals evaluated had complaints about bad breath, as the aim was to assess the difference between healthy individuals with clefts and the general population. Although not statistically significant, group II showed higher values of oral halimeter measurements than group I. The reason for this finding could not be confirmed, as the periodontal status of the patients was not evaluated in this study, despite the fact that there is a straight relation between periodontal disease and halitosis.5,9,12,14,34-39 It can only be assumed that periodontal involvement was not visually evident in any of the groups. Published data addressing nasal halitosis and its causes could not be found. Moreover, reports about bad breath in patients with facial deformities are not based on a scientific prospective study, but rather on clinical observations and assumptions. Few authors assume that the malformation itself leads to the development of malodor.23,40,41 Craniofacial anomalies, such as palatal clefts, lateral choanal atresia, and tumors of the nasal cavity represent an altered environment, susceptible to infections and production of malodor.40 Patients with cleft lip and/or palate can also present with severe impairment of airflow, as a result of a smaller transverse section of the nasal airway.25 This fact led us to imply that an impaired airflow in those patients would favor the growth of proteolytic gram-negative VSC-producing microorganisms, because of the low oxygen level. Nevertheless, slightly higher halimeter nasal measurements were observed in group I, although no reasons could be found for this fact. These data conflict with our own previous observations,26 in which higher nasal VSC values were observed in individuals with clefts. Even in group I, the slightly higher values were maintained within normal values. Maybe this can be attributed to the fact that in the present study individuals with repaired clefts were selected according to their hygiene status and easy access to the hospital, so that they could be compared to postgraduate students.
Monteiro-Amado, Chinellato, and de Rezende 685
Table III. Pearson correlation coefficients (r) between the variables with possible causal relations with halitosis, in Groups I and II Group I r Initial sulfide level 3 Weight of tongue coating Initial sulfide level 3 Resting salivary flow rate Initial sulfide level 3 Stimulated salivary flow rate Weight of tongue coating 3 Resting salivary flow rate Weight of tongue coating 3 Stimulated salivary flow rate
Group II P
r
P*
0.3104
.1707
0.6924
.001
ÿ0.0283
.9030
0.4523
.040
ÿ0.1258
.5868
0.5595
.008
ÿ0.2051
.3724
0.4470
.042
ÿ0.0666
.7742
0.7215
.000
*Boldface indicates statistical significance.
Waler42 showed that the great production of VSC occurs on the tongue dorsum. De Boever and Loesche6 visually evaluated the amount of tongue coating and noticed that the oral breath score was highly associated with tongue odor and the presence and extension of tongue coating. However, in agreement with the method used by Yaegaki and Sanada16 who quantitatively evaluated the amount of tongue coating, the present data support the idea that adequate cleaning procedures should be a part of daily routine,19 since removal of tongue coating diminished the levels of VSCs in both groups. Also, the fact that VSC values were lower during expiration suggests that the mouth, more than the lung, is the main cause of halitosis, as previously stated elsewhere.9 Volatile compounds are strongly expressed after evaporation of the solution where they are included,43,44 which makes breath stronger when the mouth is dry.19 Mastication improves salivary flow rate, cleans the mouth and reduces bad breath,5 as demonstrated by the inverse correlation between breath and salivary flow rate.45 A medium, statistically significant correlation was found between salivary flow rate and halimeter measurements in group II, also showing a direct relation between salivary flow rate and tongue coating’s dry weight. Taking into account that the subjects in this study did not have complaints of bad breath, the VSC levels were low, and the amount of tongue coating was small, it could be implied that the inhibitory effect of salivary flow rate on the formation of tongue coating is not as evident as it could be if the amount of tongue coating was greater. CONCLUSIONS The present observations suggest that individuals with cleft lip and/or palate, since adequately treated,
686 Monteiro-Amado, Chinellato, and de Rezende can present the same VSC levels when compared with individuals without clefts, as long as hygiene conditions are controlled, as observed in both groups. This highlights the importance of follow-up for patients with clefts during treatment for maintenance of oral and nasal health, thereby avoiding halitosis. It should be considered that this study was conducted on subjects with good knowledge of oral hygiene procedures and easy access to dental treatment. The weak relation between the parameters studied and halitosis does not indicate, at any circumstances, the inexistence of these relations in the population groups. As halitosis becomes more evident, the relationship between the parameters studied and breath would be stronger. This study included patients with no complaints of bad breath, so that any differences related to the cleft itself and to the parameters investigated could be identified. However, the differences related to the cleft were irrelevant. We thank Rodrigo Hermont Canc¸ado for his assistance.
REFERENCES 1. Lu DP. Halitosis: an etiologic classification, a treatment approach, and prevention. Oral Surg Oral Med Oral Pathol 1982;54:521-67. 2. Richter JL. Diagnosis and treatment of halitosis. Compend Contin Educ Dent 1996;17:370-6. 3. Richter VJ, Tonzetich J. The application of instrumental technique for the evaluation of odoriferous volatiles from saliva and breath. Arch Oral Biol 1964;16:47-53. 4. 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. 5. Tonzetich J. Production and origin of oral malodor: a review of mechanisms and methods of analysis. J Periodontol 1977;48: 13-20. 6. De Boever EH, Loesche WJ. Assessing the contribution of anaerobic microflora of the tongue to oral malodor. J Am Dent Assoc 1995;126:1384-93. 7. Bogdasarian RS. Halitosis. Otolaryngol Clin North Am 1986;19: 111-7. 8. Young K, Oxtoby A, Field EA. Halitosis: a review. Dent Update 1993;20:57-61. 9. Tessier JF, Kulkarni GV. Bad breath: etiology, diagnosis and treatment. Oral Health 1991;81:19-24. 10. Chaim LAF. Comparison between the use of a simplified tongue scraper and a toothbrush for tongue cleaning [Portuguese]. Rev ABO Nac 2001;9:242-6. 11. Christensen GJ. Why clean your tongue? J Am Dent Assoc 1998; 129:1605-7. 12. Kozlovsky A, Gordon D, Gelernter I, Loesche WJ, Rosenberg M. Correlation between the BANA test and oral malodor parameters. J Dent Res 1994;73:1036-42. 13. Menon MV, Coykendall AL. Effect of tongue scraping. J Dent Res 1994;73:1492. 14. Morita M, Musinsky DL, Wang HL. Assessment of newly developed tongue sulfide probe for detecting oral malodor. J Clin Periodontol 2001;28:494-6. 15. Seemann R, Kison A, Bizhang M, Zimmer S. Effectiveness of tongue cleaning on oral levels of volatile sulfur compounds. J Am Dent Assoc 2001;132:1263-7.
OOOOE December 2005 16. Yaegaki K, Sanada K. Volatile sulfur compounds in mouth air from clinically healthy subjects and patients with periodontal disease. J Periodontol Res 1992;27:233-8. 17. Bennett JD. An unexpected cause of halitosis. J R Army Med Corps 1988;134:151-2. 18. Clark GT, Nachnani S, Messadi DV. Detecting and treating oral and nonoral malodors. J Calif Dent Assoc 1997;25:133-44. 19. Rosenberg M. Clinical assessment of bad breath: current concepts. J Am Dent Assoc 1996;127:475-82. 20. Hine MK. Halitosis. J Am Dent Assoc 1957;55:37-46. 21. Bosy A. Oral malodor: philosophical and practical aspects. J Can Dent Assoc 1997;63:196-201. 22. Crohn BB, Drosd R. Halitosis. J Am Med Assoc 1941;117: 2242-5. 23. Finkelstein Y. Halitosis in patients with craniofacial anomalies. In: Rosenberg M, editor. Bad breath: research perspectives. Tel Aviv Israel: Ramot Publishing, Tel Aviv University; 1995. p. 189-200. 24. Anastassov GE, Joos U, Zo¨llner B. Evaluation of the results of delayed rhinoplasty in cleft lip and palate patients. Functional and aesthetic implications and factors that affect successful nasal repair. Br J Oral Maxillofac Surg 1998;36:416-24. 25. Warren DW, Hairfield M, Dalston ET. Nasal airway impairment: the oral response in cleft palate patients. Am J Orthod Dentofacial Orthop 1991;99:346-53. 26. Monteiro-Amado F, Chinellato LE, Tarzia O, Rezende ML. Evaluation of oral and nasal odor in patients with and without cleft lip and palate: preliminary report. Cleft Palate Craniofac J 2004;41:661-3. 27. Brefz WA, Loesch WJ. Characteristics of trypsin-like activity in subgingival plaque sample. J Dent Res 1987;66:1668-72. 28. McNamara TF, Alexander JF, Lee M. The role of microorganisms in the production of oral malodor. Oral Surg Oral Med Oral Pathol 1972;34:41-8. 29. Rosenberg M, McCulloch CA. Measurement of oral malodor: current methods and future prospects. J Periodontol 1992;63: 776-82. 30. Scully C, el-Maaytah M, Porter SR, Greenman J. Breath odor: etiopatogenesis, assessment and management. Eur J Oral Sci 1997;105:287-93. 31. Goldberg S, Kozlovsky A, Gordon D, Gelernter I, Sintov A, Rosenberg M. Cadaverine as a putative component of oral malodor. J Dent Res 1994;73:1168-72. 32. Astor FC, Hanft KL, Ciocon JO. Xerostomia: a prevalent condition in the elderly. Ear Nose Throat J 1999;78:476-9. 33. 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. 34. Berg M, Fosdick LS. Studies in periodontal disease. J Dent Res 1946;25:73-81. 35. Cohen M. A new era in halitosis and periodontal treatment. Dent Today 1998;17:88-9. 36. Klokkevold PR. Oral malodor: a periodontal perspective. J Calif Dent Assoc 1997;25:153-9. 37. Messadi DV. Oral and nonoral sources of halitosis. J Calif Dent Assoc 1997;25:127-31. 38. Ratcliff PA, Johnson PW. The relationship between oral malodor, gingivitis, and periodontitis. A review. J Periodontol 1999;70: 485-9. 39. Tanaka M, Yamamoto Y, Kuboniwa M, Nonaka A, Nishida N, Maeda K, et al. Contribution of periodontal pathogens on tongue dorsa analyzed with real-time PCR to oral malodor. Microbes Infect 2004;6:1078-83. 40. Ayers KM, Colquhoun AN. Halitosis: causes, diagnosis, and treatment. N Z Dent J 1998;94:156-60. 41. ADA Council on Scientific Affairs. Oral malodor. J Am Dent Assoc 2003;134:209-14. 42. Waler SM. On the transformation of sulfur-containing amino acids and peptides to volatile sulfur compounds (VSC) in the human mouth. Eur J Oral Sci 1997;105:534-7.
OOOOE Volume 100, Number 6 43. Van Steenberghe D. Breath malodor. Curr Opin Periodontol 1997;4:137-43. 44. Van Steenberghe D, Avontroodt P, Peeters W, Pauwels M, Coucke W, Lijnen A, et al. Effect of different mouthrinses on morning breath. J Periodontol 2001;72:1183-91. 45. Tonzetich J. Oral malodour: an indicator of health status and oral cleanliness. Int Dent J 1978;28:309-19.
Monteiro-Amado, Chinellato, and de Rezende 687 Reprint requests: Fla´vio Monteiro-Amado, DDS Rua Jose´ Gonc¸alves da Mota Ju´nior, 103 - CEP 11390-050 Vila Valenc¸a Sa˜o Vicente, SP, Brazil [email protected]
Objective. The objective of this study was to investigate the relationship between halitosis parameters in patients with and without cleft lip and/or palate.
Study design. Forty-two subjects were examined. They were divided into group I, postgraduate students of Bauru Dental School (FOB); and group II, individuals with repaired cleft lip and/or palate. The concentration of volatile sulfur compounds (VSC) was assessed with a portable sulfide monitor and the values were correlated to the salivary flow rate and weight of tongue coating. Results. There was a relationship between the presence of tongue coating and VSC levels, as well as between salivary flow rate and VSC levels in group II. The same group also revealed a significant correlation between weight of tongue coating and salivary flow rate. There were no significant differences between groups as regards the Halimeter oral measurement. Conclusions. Individuals with repaired cleft lip and/or palate can have the same VSC levels as subjects without clefts. (Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2005;100:682-7)
The etiology of halitosis includes the following: (1) local factors of pathologic origin, (2) local factors of nonpathologic origin, (3) systemic factors of pathologic origin, (4) systemic factors of nonpathologic origin, (5) administration of systemic drugs, and (6) xerostomia.1 Studies on the etiology of breath malodor agree that hydrogen sulfide (H2S), dimethyl sulfide (CH3)2S, and methylmercaptan (CH3SH), collectively referred to as volatile sulfur compounds (VSC), which are gases originated from the anaerobic bacterial degradation of sulfur-containing amino acids within the oral cavity, are the main components of offensive breath.2-5 Although several microorganisms are capable of producing volatile sulfur compounds, Treponema denticola, Porphyromonas gingivalis, Prevotella intermedia, Bacteroides forsythus, and Fusobacterium can
Financial support was from Coordenac¸a˜o de Aperfeic¸oamento de Pessoal de Nı´vel Superior. These data were presented at the 82nd General Session and Exhibition of the International Association for Dental Research/American Association for Dental Research/ Canadian Association for Dental Research, Honolulu, Hawaii, 2004. a Specialist in Dental Implantology, Hospital for Rehabilitation of Craniofacial Anomalies, Universidade of Sa˜o Paulo, and Master of Science in Stomatology by Bauru Dental School, Universidade of Sa˜o Paulo, Bauru, Brazil. b Assistant Professor, Stomatology Department, Bauru Dental School, Universidade of Sa˜o Paulo, Bauru, Brazil. c Periodontist and Implantologist, Hospital for Rehabilitation of Craniofacial Anomalies, Universidade of Sa˜o Paulo, Bauru, Brazil. Received for publication Jan 12, 2005; returned for revision Mar 7, 2005; accepted for publication Mar 23, 2005. 1079-2104/$ - see front matter Ó 2005 Mosby, Inc. All rights reserved. doi:10.1016/j.tripleo.2005.03.019
682
produce significant amounts of hydrogen sulfide and methylmercaptan from serum proteins, cysteine, and methionine.6 Evaluation of tongue coating is of special interest in the study of halitosis, since the desquamated tongue epithelium provides an ideal environment for minute food particles and bacteria capable of emitting offensive odor.7 Poor oral hygiene is probably the most common factor leading to bad breath and tends to exacerbate other causes.8 The vast majority of cases of bad breath (90%) are of oral origin,9 and tongue coating shows a direct correlation with sulfide levels,6,10-15 being responsible for nearly 50% of VSC produced in the mouth.16 Much emphasis is reported in the literature about unpleasant breath from oral sources, but there are few reports concerning the bad odor because of nasal alterations.7,17 The general low level of knowledge as to the causes of halitosis and how it is self-managed among medical and dental practitioners9,18 can contribute to the lack of a better interaction between physicians and dental clinicians in the treatment of this problem. Airway passages are described as the second main source of halitosis.19 Tonsillitis, sinusitis, and rhinitis are believed to contribute to halitosis,20 as do polyps and foreign bodies in nasal odor.21 Nevertheless, Crohn and Drosd,22 in 1941, wrote that ‘‘unless pathologic oral or nasopharyngeal conditions exist, the mouth, teeth and pharynx play little or no part in the production of essential halitosis.’’ Finkelstein,23 in 1995, described several factors that may lead to the high incidence of sinusitis in patients with clefts and then to the increased frequency of
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halitosis in these patients, such as deviated nasal septum, deformed medium turbinate, underdeveloped maxillary sinuses, maxillary growth deficits, choanal stenosis or atresia, atresia of the nostrils, malformed external nasal valve, incompetent velopharyngeal valve, presence of pharyngeal flap, and impairment of mucociliary transport. The nasal cavity may also be contaminated by saliva and food that passes from the oral to the nasal cavity through oronasal fistulae. Patients with clefts can present with reduced nasal passage as a result of ostial obstruction, septal deviation, inferior turbinate hypertrophy, valvular collapse, and reduced airflow.24,25 Pathologic conditions as those previously mentioned, affecting the nose, pharynx, or tracheobronchial tree may result in the production of objectionable odors. Virtually any condition leading to the growth of gram-negative or anaerobic microorganisms will produce an unpleasant odor.7 A preliminary work showed that individuals with cleft lip and/or palate are prone to present higher nasal VSC measurements.26 The lack of information about halitosis in patients with cleft lip and palate encouraged accomplishment of this study. The purpose was to compare the VSC levels, amount of tongue coating, and salivary flow rate among postgraduate students of Bauru Dental School, University of Sa˜o Paulo, Brazil, and individuals with repaired cleft lip and/or palate from the Hospital for Rehabilitation of Craniofacial Anomalies, University of Sa˜o Paulo, in Bauru.
MATERIAL AND METHODS Study population Two groups of patients were evaluated concerning oral and nasal halimeter measurements: group I, 21 postgraduate students of Bauru Dental School, University of Sa˜o Paulo (FOB/USP), who were supposed to present good oral hygiene; and group II, 21 individuals with repaired clefts, from the Hospital for Rehabilitation of Craniofacial Anomalies of University of Sa˜o Paulo (HRAC/USP), who worked or lived near the hospital and were examined at the Stomatology Clinic of FOB/USP. Exclusion criteria were the existence of systemic disorders (sinusitis, rhinitis, or lung, kidney, liver, and intestinal disturbances) and local factors that could affect oral malodor (poor oral hygiene, visually noticed gingivitis, or visual loss of periodontal attachment). For odor measurements, a portable sulfide monitor was used (Halimeter, Interscan Corporation, Chatsworth, Calif). The protocol was approved by the Institutional Review Board of Bauru Dental School, University of Sa˜o Paulo, and all subjects signed a written informed consent term agreeing to participate in the study.
Monteiro-Amado, Chinellato, and de Rezende 683
On the day of examination, the participants were asked not to use personal scent products and to avoid all oral activities for 3 hours prior to the appointment, including eating, chewing, drinking (except water), and any other hygiene procedures. Clinical examination Concentration of volatile sulfur compounds. After being submitted to complete intraoral examination, each patient closed the mouth for 60 seconds prior to sampling. Measurements were made in triplicate using a portable sulfide monitor (Halimeter, Interscan Corporation), and the mean value was calculated. A plastic straw was inserted and positioned above the posterior part of the tongue dorsum, not touching the oral mucosa or tongue. No breathing was allowed during each sampling; the mouth was kept slightly opened and the peak value was recorded. Then, measurements of nasal values were accomplished by inserting another plastic straw 1 cm inside each nostril, only once, until the peak value was achieved. The concentration of mouth volatile sulfur compounds was obtained in the same manner after removal of tongue coating, and 1 measurement was performed during expiration, in order to exclude possible systemic causes of halitosis that could lead to liberation of VSC by the lungs. If this measurement was lower than the measurements without tongue coating, then it could be supposed that no VSC from the lungs were being detected. Tongue coating sampling and BANA test. Although there are several microorganisms capable of performing the process of VSCs production, three in particular—T. denticola, P. gingivalis, and B. forsythus—produce a ‘‘trypsin-like’’ enzyme that can be detected by the hydrolysis of the synthetic peptide, benzoyl-DLarginine-naphthylamide, known as BANA, and it can be monitored by the use of a test called the BANA test.27 Excessive moisture from the tongue dorsum was removed with gauze, tongue coating was removed with a tongue scraper, and new measurements of oral VSC were obtained, again in triplicate. The tongue coating was put on a filter paper, previously weighed, and allowed to dry for 24 hours at room temperature, when it was weighed with a precision balance (A&D Company, Limited, Tokyo, Japan). Salivary flow rate. Resting and stimulated saliva were obtained as follows. The patient kept his or her mouth slightly open for 5 minutes, without talking or spitting, and saliva was allowed to go down into a glass recipient. The volume of saliva was assessed. Then, the patient chewed a piece of silicone rubber for 5 minutes (Saudbucal, Sa˜o Paulo, Brazil) after which he or she expectorated all saliva formed in another glass recipient, where the volume of saliva was assessed. The volume
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684 Monteiro-Amado, Chinellato, and de Rezende
Table I. Results of the paired t test between the initial variable VSC levels, after removal of tongue coating and during expiration Variable Without cleft With cleft
Initial Initial Initial Initial
sulfide sulfide sulfide sulfide
level level level level
(ppb) (ppb) (ppb) (ppb)
Mean
SD
Variable
Mean
SD
P*
88.9523 88.9523 91.8095 91.8095
73.9624 73.9624 68.8764 68.8764
Sulfide level without tongue coating (ppb) Sulfide level during expiration (ppb) Sulfide level without tongue coating (ppb) Sulfhide level during expiration (ppb)
69.4761 56.2857 66.1428 65.9047
38.0928 25.0342 51.7003 68.8737
.047 .012 .025 .084
VSC, volatile sulfur compounds. *Boldface indicates statistical significance.
Table II. Results of the independent t test between the variables in Groups I and II With cleft Variables Initial sulfide level (ppb) Sulfide level without tongue coating (ppb) Weight of tongue coating (mg) Sulfide level during expiration (ppb) Resting salivary flow rate (mL/min) Stimulated salivary flow rate (mL/min) Nasal sulfide level (ppb)
Without cleft
Mean
SD
Mean
SD
Difference*
P**
91.8095 66.1428 0.0235 65.9047 0.1628 1.2466 47.6666
68.8764 51.7003 0.0150 68.8737 0.1395 0.9382 13.9044
88.9523 69.4761 0.0139 56.2857 0.1790 1.1695 62.0000
73.9624 38.0928 0.01332 25.0342 0.1275 0.7022 20.1940
ÿ2.8571 3.3333 ÿ0.0096 ÿ9.6190 0.01619 ÿ0.0771 14.3333
.898 .813 .036 .551 .697 .764 .011
*Represents the difference between the mean values of the variables in the two groups. **Boldface indicates statistical significance.
was divided by 5 and the salivary flow rate was obtained (mL/min). Statistical analysis Results were analyzed by means of the dependent and independent t test for the following scalar quantitative variables: halitosis, salivary flow rate, and weight of tongue coating, between the 2 groups. The paired t test was used to verify the relationship between initial VSC values after removal of tongue coating and VSC values during forced expiration. The relationship between VSC measurements, tongue coating’s dry weight, and salivary flow rate was obtained by the Pearson correlation. The significance level was set at 5%. RESULTS A total of 42 individuals were evaluated, divided into 2 groups of 21 individuals each: group I, without cleft lip and/or palate, post-graduation students of Bauru Dental School; and group II, with repaired cleft lip and/or palate. Group I was composed of 13 males and 8 females with a mean age 26.2 years (range 21 to 30 years). Group II was composed of 13 males and 8 females with a mean age 24.2 years (range 19 to 33 years). Data on the parameters investigated are presented in the tables. Statistically significant values are displayed in bold letters. Table I shows that reduction in VSC levels after removal of tongue coating was statistically significant for groups I and II. Although there was reduction in VSC levels during expiration in both groups, it was only
statistically significant for group I. Group I had less tongue coating than group II, but higher nasal VSC levels (Table II). Only group II showed statistically significant correlations for the variables studied, although these correlations were all mild (Table III). DISCUSSION Persistent oral malodor affects at least 50% of the population,21 and the vast majority of cases of bad breath (90%) are of oral origin.9 It may result from microbial metabolism on the tongue dorsum and periodontium, and is modulated by low salivary flow at certain times during the day, food impaction, and diet.5,28 Its intensity is significantly related to increased oral levels of VSC,29 which are likely to arise mainly from the breakdown of cysteine, cystine, and methionine, peptides and amino acids found free in gingival crevicular fluid, in saliva, or produced as a result of proteolysis of protein substrates.30 Cadaverine, produced from the decarboxylation of lysine, may also be of some importance in malodor.31 Factors involved in the production, release, and detection of odors are reduced salivary flow rate; accumulation and putrefaction of oral epithelial debris, food, and saliva; low oxygen concentration; reduced availability of carbohydrates as bacterial substrate; and high oral pH.5,7 There are 3 main methods to evaluate exhaled air: organoleptic scales; gas chromatography; and portable sulfide monitor, which detects mainly hydrogen sulfide,
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but also, and to a lesser extent, dimethyl sulfide and methylmercaptan.4 Even though the use of gas chromatography is the most accurate method for detecting the products involved in the process of halitosis, the sulfide monitor presents other advantages, such as no need for skilled personnel, noninvasive procedures,32 low possibility of cross-infection, portability, relatively inexpensive, and rapid turnaround time of 1 to 2 minutes between measurements.4 Figueiredo et al33 reported, in 2002, that absolute levels of VSC may vary between different population groups, and this indicates that studies on VSC production and malodor should include a control population that either has no periodontal disease or no complaints of malodor. In the present study, none of the individuals evaluated had complaints about bad breath, as the aim was to assess the difference between healthy individuals with clefts and the general population. Although not statistically significant, group II showed higher values of oral halimeter measurements than group I. The reason for this finding could not be confirmed, as the periodontal status of the patients was not evaluated in this study, despite the fact that there is a straight relation between periodontal disease and halitosis.5,9,12,14,34-39 It can only be assumed that periodontal involvement was not visually evident in any of the groups. Published data addressing nasal halitosis and its causes could not be found. Moreover, reports about bad breath in patients with facial deformities are not based on a scientific prospective study, but rather on clinical observations and assumptions. Few authors assume that the malformation itself leads to the development of malodor.23,40,41 Craniofacial anomalies, such as palatal clefts, lateral choanal atresia, and tumors of the nasal cavity represent an altered environment, susceptible to infections and production of malodor.40 Patients with cleft lip and/or palate can also present with severe impairment of airflow, as a result of a smaller transverse section of the nasal airway.25 This fact led us to imply that an impaired airflow in those patients would favor the growth of proteolytic gram-negative VSC-producing microorganisms, because of the low oxygen level. Nevertheless, slightly higher halimeter nasal measurements were observed in group I, although no reasons could be found for this fact. These data conflict with our own previous observations,26 in which higher nasal VSC values were observed in individuals with clefts. Even in group I, the slightly higher values were maintained within normal values. Maybe this can be attributed to the fact that in the present study individuals with repaired clefts were selected according to their hygiene status and easy access to the hospital, so that they could be compared to postgraduate students.
Monteiro-Amado, Chinellato, and de Rezende 685
Table III. Pearson correlation coefficients (r) between the variables with possible causal relations with halitosis, in Groups I and II Group I r Initial sulfide level 3 Weight of tongue coating Initial sulfide level 3 Resting salivary flow rate Initial sulfide level 3 Stimulated salivary flow rate Weight of tongue coating 3 Resting salivary flow rate Weight of tongue coating 3 Stimulated salivary flow rate
Group II P
r
P*
0.3104
.1707
0.6924
.001
ÿ0.0283
.9030
0.4523
.040
ÿ0.1258
.5868
0.5595
.008
ÿ0.2051
.3724
0.4470
.042
ÿ0.0666
.7742
0.7215
.000
*Boldface indicates statistical significance.
Waler42 showed that the great production of VSC occurs on the tongue dorsum. De Boever and Loesche6 visually evaluated the amount of tongue coating and noticed that the oral breath score was highly associated with tongue odor and the presence and extension of tongue coating. However, in agreement with the method used by Yaegaki and Sanada16 who quantitatively evaluated the amount of tongue coating, the present data support the idea that adequate cleaning procedures should be a part of daily routine,19 since removal of tongue coating diminished the levels of VSCs in both groups. Also, the fact that VSC values were lower during expiration suggests that the mouth, more than the lung, is the main cause of halitosis, as previously stated elsewhere.9 Volatile compounds are strongly expressed after evaporation of the solution where they are included,43,44 which makes breath stronger when the mouth is dry.19 Mastication improves salivary flow rate, cleans the mouth and reduces bad breath,5 as demonstrated by the inverse correlation between breath and salivary flow rate.45 A medium, statistically significant correlation was found between salivary flow rate and halimeter measurements in group II, also showing a direct relation between salivary flow rate and tongue coating’s dry weight. Taking into account that the subjects in this study did not have complaints of bad breath, the VSC levels were low, and the amount of tongue coating was small, it could be implied that the inhibitory effect of salivary flow rate on the formation of tongue coating is not as evident as it could be if the amount of tongue coating was greater. CONCLUSIONS The present observations suggest that individuals with cleft lip and/or palate, since adequately treated,
686 Monteiro-Amado, Chinellato, and de Rezende can present the same VSC levels when compared with individuals without clefts, as long as hygiene conditions are controlled, as observed in both groups. This highlights the importance of follow-up for patients with clefts during treatment for maintenance of oral and nasal health, thereby avoiding halitosis. It should be considered that this study was conducted on subjects with good knowledge of oral hygiene procedures and easy access to dental treatment. The weak relation between the parameters studied and halitosis does not indicate, at any circumstances, the inexistence of these relations in the population groups. As halitosis becomes more evident, the relationship between the parameters studied and breath would be stronger. This study included patients with no complaints of bad breath, so that any differences related to the cleft itself and to the parameters investigated could be identified. However, the differences related to the cleft were irrelevant. We thank Rodrigo Hermont Canc¸ado for his assistance.
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OOOOE December 2005 16. Yaegaki K, Sanada K. Volatile sulfur compounds in mouth air from clinically healthy subjects and patients with periodontal disease. J Periodontol Res 1992;27:233-8. 17. Bennett JD. An unexpected cause of halitosis. J R Army Med Corps 1988;134:151-2. 18. Clark GT, Nachnani S, Messadi DV. Detecting and treating oral and nonoral malodors. J Calif Dent Assoc 1997;25:133-44. 19. Rosenberg M. Clinical assessment of bad breath: current concepts. J Am Dent Assoc 1996;127:475-82. 20. Hine MK. Halitosis. J Am Dent Assoc 1957;55:37-46. 21. Bosy A. Oral malodor: philosophical and practical aspects. J Can Dent Assoc 1997;63:196-201. 22. Crohn BB, Drosd R. Halitosis. J Am Med Assoc 1941;117: 2242-5. 23. Finkelstein Y. Halitosis in patients with craniofacial anomalies. In: Rosenberg M, editor. Bad breath: research perspectives. Tel Aviv Israel: Ramot Publishing, Tel Aviv University; 1995. p. 189-200. 24. Anastassov GE, Joos U, Zo¨llner B. Evaluation of the results of delayed rhinoplasty in cleft lip and palate patients. Functional and aesthetic implications and factors that affect successful nasal repair. Br J Oral Maxillofac Surg 1998;36:416-24. 25. Warren DW, Hairfield M, Dalston ET. Nasal airway impairment: the oral response in cleft palate patients. Am J Orthod Dentofacial Orthop 1991;99:346-53. 26. Monteiro-Amado F, Chinellato LE, Tarzia O, Rezende ML. Evaluation of oral and nasal odor in patients with and without cleft lip and palate: preliminary report. Cleft Palate Craniofac J 2004;41:661-3. 27. Brefz WA, Loesch WJ. Characteristics of trypsin-like activity in subgingival plaque sample. J Dent Res 1987;66:1668-72. 28. McNamara TF, Alexander JF, Lee M. The role of microorganisms in the production of oral malodor. Oral Surg Oral Med Oral Pathol 1972;34:41-8. 29. Rosenberg M, McCulloch CA. Measurement of oral malodor: current methods and future prospects. J Periodontol 1992;63: 776-82. 30. Scully C, el-Maaytah M, Porter SR, Greenman J. Breath odor: etiopatogenesis, assessment and management. Eur J Oral Sci 1997;105:287-93. 31. Goldberg S, Kozlovsky A, Gordon D, Gelernter I, Sintov A, Rosenberg M. Cadaverine as a putative component of oral malodor. J Dent Res 1994;73:1168-72. 32. Astor FC, Hanft KL, Ciocon JO. Xerostomia: a prevalent condition in the elderly. Ear Nose Throat J 1999;78:476-9. 33. 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. 34. Berg M, Fosdick LS. Studies in periodontal disease. J Dent Res 1946;25:73-81. 35. Cohen M. A new era in halitosis and periodontal treatment. Dent Today 1998;17:88-9. 36. Klokkevold PR. Oral malodor: a periodontal perspective. J Calif Dent Assoc 1997;25:153-9. 37. Messadi DV. Oral and nonoral sources of halitosis. J Calif Dent Assoc 1997;25:127-31. 38. Ratcliff PA, Johnson PW. The relationship between oral malodor, gingivitis, and periodontitis. A review. J Periodontol 1999;70: 485-9. 39. Tanaka M, Yamamoto Y, Kuboniwa M, Nonaka A, Nishida N, Maeda K, et al. Contribution of periodontal pathogens on tongue dorsa analyzed with real-time PCR to oral malodor. Microbes Infect 2004;6:1078-83. 40. Ayers KM, Colquhoun AN. Halitosis: causes, diagnosis, and treatment. N Z Dent J 1998;94:156-60. 41. ADA Council on Scientific Affairs. Oral malodor. J Am Dent Assoc 2003;134:209-14. 42. Waler SM. On the transformation of sulfur-containing amino acids and peptides to volatile sulfur compounds (VSC) in the human mouth. Eur J Oral Sci 1997;105:534-7.
OOOOE Volume 100, Number 6 43. Van Steenberghe D. Breath malodor. Curr Opin Periodontol 1997;4:137-43. 44. Van Steenberghe D, Avontroodt P, Peeters W, Pauwels M, Coucke W, Lijnen A, et al. Effect of different mouthrinses on morning breath. J Periodontol 2001;72:1183-91. 45. Tonzetich J. Oral malodour: an indicator of health status and oral cleanliness. Int Dent J 1978;28:309-19.
Monteiro-Amado, Chinellato, and de Rezende 687 Reprint requests: Fla´vio Monteiro-Amado, DDS Rua Jose´ Gonc¸alves da Mota Ju´nior, 103 - CEP 11390-050 Vila Valenc¸a Sa˜o Vicente, SP, Brazil [email protected]