Effect of rapid maxillary expansion on halitosis

Effect of rapid maxillary expansion on halitosis

ORIGINAL ARTICLE Effect of rapid maxillary expansion on halitosis Turkan Sezen Erhamzaa and Ferabi Erhan Ozdılerb Kirikkale and Ankara, Turkey Intro...

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Effect of rapid maxillary expansion on halitosis Turkan Sezen Erhamzaa and Ferabi Erhan Ozdılerb Kirikkale and Ankara, Turkey

Introduction: The objective of this study was to evaluate the effect of rapid maxillary expansion (RME) on halitosis. Methods: Thirty children (11-15 years old) were randomly divided into RME and control groups. The RME group consisted of 15 children treated with hyrax appliances, and the control group included 15 children without treatment. Halitosis was evaluated with the halimeter and the organoleptic method. Plaque index and gingival index scores were recorded. Acoustic rhinometry was used to measure the nasal volume. Measurements were obtained at 2 times: before RME, and after retention at 4 months. The Wilcoxon signed rank test and the paired t test were used for intragroup comparisons, and the Mann-Whitney U test and the Student t test were used for intergroup comparisons. Results: Halitosis (halimeter and organoleptic values) decreased significantly in the RME group (P \0.001). Insignificant changes of halitosis were observed in the control group. Intragroup and intergroup comparisons showed no statistically significant differences for the plaque index. Gingival index values were significantly decreased with RME (P #0.05). Nasal cavity volume increased significantly in the RME group (P \0.01). Conclusions: RME was shown to lower halitosis values. RME could be a treatment option for patients with maxillary transverse deficiency and halitosis. (Am J Orthod Dentofacial Orthop 2018;154:702-7)


alitosis is used to describe a bad or an unpleasant odor in the mouth. It is a condition that causes patients to feel insecure and embarrassed, thus reducing their quality of life.1 When halitosis is examined, volatile sulfur compounds (VSCs) are found to be the responsible for the odor. VSCs are formed by the proteolysis of sulfur-containing amino acids such as cysteine, cystine, methionine, and proteins by bacteria in saliva and gingival fluid, and on the tongue and other parts of the oral cavity.2 There are certain conditions for the formation of VSCs. Acidic or basic pH value of the saliva, decreased saliva amount and flow rate, gingivitis, periodontitis accompanied by an increase of gram-negative anaerobic bacteria, a diet supporting bacteria reproduction and

a Deparment of Orthodontics, Faculty of Dentistry, Kirikkale University, Kirikkale, Turkey. b Deparment of Orthodontics, Faculty of Dentistry, Ankara University, Ankara, Turkey. All authors have completed and submitted the ICMJE Form for Disclosure of Potential Conflicts of Interest, and none were reported. Supported by the Coordinatorship of Scientific Research Projects, Kirikkale University (grant number 2015/09). Address correspondence to: Turkan Sezen Erhamza, Kirikkale University, Faculty of Dentistry, Department of Orthodontics, Kirikkale, Turkey; e-mail, dt. [email protected]. Submitted, September 2017; revised and accepted, January 2018. 0889-5406/$36.00 Ó 2018 by the American Association of Orthodontists. All rights reserved. https://doi.org/10.1016/j.ajodo.2018.01.014


metabolism, low oxygen, and pharyngeal infections are some conditions leading to halitosis.2-4 Transverse maxillary deficiency, accompanied by a high palatal vault, is a symptom of a skeletally developed syndrome that causes some rhinologic disorders and has certain undesirable effects on the dentofacial pattern.5 Some features of this problem are a decrease in nasal permeability resulting from nasal stenosis, elevation of the nasal floor, bilateral dental maxillary crossbite, mouth breathing, and, because of enlargement of the nasal turbinates, a decrease in nasal airway size.5-7 Treatment for transverse maxillary constriction involves the use of rapid maxillary expansion (RME). It promotes the separation of the maxillary bones in a pyramidal shape in which maximum expansion is near the incisors, just below the nasal valves. This treatment expands the external walls of the nasal cavity to increase its capacity.8-10 This can result in improvement of the patient's ability to breathe through the nose.8 Gray11 found that RME could replace oral breathing over to nasal breathing in 80% of patients. Considering this information, we planned this study with the idea that changes in the nasal cavity obtained by RME treatment in patients with maxillary constriction might facilitate nasal breathing and decrease oral malodor. The effects of orthodontic treatment on oral malodor have been evaluated in several studies.10,12-17 Some

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researchers have found that brackets, ligatures, and other attachments used for orthodontic treatment cause plaque accumulation as well as periodontal inflammation, hyperemia, hyperplasia, and oral malodor because of their retentive properties.10,12 In contrast, some studies have reported that periodontal tissues are not affected by orthodontic treatment, and even plaque indexes might be lower as a result of increased oral hygiene motivation.18-20 Although several studies have evaluated the relationship between oral malodor and removable appliances and fixed orthodontic treatment, the effects of RME, an orthopedic treatment, have not been documented. Thus, this prospective randomized clinical study was performed to investigate the effect of RME on halitosis. MATERIAL AND METHODS

This study protocol was approved both by the Ethics Committee for Clinical Research of Kirikkale University (14/03-2015) and the Medicine and Medical Devices Agency of Turkey (2015-AC-CE-114). The Coordinatorship of Scientific Research Projects of Kirikkale University financially supported this study (grant number 2015/09). Thirty subjects with ages between 11 and 15 years were randomly selected. They were divided into 2 groups: the RME group (7 girls, 8 boys; mean age, 12.6 6 1.17 years) and the control group (10 girls, 5 boys; mean age, 13.06 6 1.22 years). The inclusion criteria were maxillary constriction, deep palatal vault, bilateral crossbite, and presence of first premolars and first molars. Patients were excluded if they had congenital or developmental deformities or systemic disorders, thumb sucking, tongue thrust, periodontal problems, or were using antibiotics or mouthwash, or were receiving orthodontic treatment. Orthodontic treatment of the control group subjects started after this study. We received informed consent from all patients. The block randomization method was used for selection of the patients. Details of the allocated groups were written on colored cards placed in sequentially numbered, opaque, sealed envelopes. All subjects received oral hygiene instructions to maintain their usual oral hygiene procedures at every appointment. Halitosis and organoleptic measurements, acoustic rhinometry results, and plaque and gingival index records were obtained before treatment (T0) and after retention of RME (T1). Hyrax appliances consisting of an expansion screw and stainless steel extensions (Dentaurum, Pforzheim, Germany) were used to expand the maxilla. The screw was positioned parallel to the occlusal plane and as close as possible to the palate. The appliance was cemented to the first premolars and first molars with glass ionomer


cement (3M Unitek, Monrovia, Calif). The screw was activated 0.5 mm per day until the midpalatal suture was opened. The opening of the midpalatal suture was determined with an occlusal radiograph and midline diastema of the maxilla. Then it was activated 0.25 mm per day until the palatal cusps of the maxillary molars were in contact with the buccal cusps of the mandibular first molars. RME appliances were used as retainers without debanding for 4 months. The amount of VSCs representing halitosis was measured with a halimeter device (Interscan, Chatsworth, Calif) at T0 and T1. Halitosis scores were divided into 4 categories and classified as normal (0-100 ppb), weak (101-150 ppb), strong (151-300 ppb), or very strong ($301 ppb).21 The patients were asked to breathe through their noses for 3 minutes before sampling. Then they were instructed to place the disposable straw at the posterior dorsum of the tongue and not to touch the oral mucosa or the tongue. They were told to keep their lips 1.5 cm apart during the measurements. Measurements were repeated 3 times at 3-minute intervals. The mean value was calculated in parts per billion for each patient. Another method for the evaluation of oral malodor was the organoleptic method with scores in 5 categories: 0, no malodor; 1, slight malodor; 2, clearly noticeable malodor; 3, moderate malodor; 4, strong malodor; and 5, very strong oral malodor.22 The organoleptic measurements of breath were taken at a distance of 10 cm from the oral cavity and scored. All subjects were requested to avoid eating onions, garlic, and spices for 2 days before the halitosis measurements. They were instructed to brush their teeth after dinner on the evening before the measurements and to refrain from eating, drinking, toothbrushing, mouthwashing, and gum chewing before the appointment the next morning. All measurements were made in the morning before breakfast. No antibiotics were used for 2 months before the measurements. In addition, the measurements from the girls were taken when they were not menstruating. The assessments were made by the same examiner (T.S.E.) throughout the study. The examiner avoided tea, coffee, orange juice, fragrances, and cosmetics before the organoleptic evaluation. The measurements were carried out using an acoustic rhinometry device (SRE 2000, Rhinoscan 2.5; RhinoMetrics, Lynge, Denmark), which produces an acoustic signal in the form of discrete impulses, according to the criteria determined and recommended by the Standardization Committee on Acoustic Rhinometry guidelines. The room where the acoustical rhinometry measurements were taken was silent, with an approximate

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Table I. Comparison of halimeter and organoleptic values of groups and changes between T0 and T1 T0 Halimeter RME group Control group Between groups Organoleptic RME group Control group Between groups

128 6 85.44 89.56 6 26.22 Z 5 –1.72c 3 (2-3) 1 (1-3) Z 5 –3.66*c



Mean 6 SD 17.6 6 12.49 82.43 6 30.05 Z 5 –4.53*c Median (minimum-maximum) 1 (0-2) 2 (1-3) Z 5 –4.53*c

110.86 6 82.10 7.12 6 14.96 Z 5 –4.68*c 2 (–3-[–1]) 0 (0-1) Z 5 –4.98*c

P \0.001*b 0.076b

\0.001*a 0.056a

a, Wilcoxon signed rank test; b, paired t test; c, Mann-Whitney U test. *Significant at P #0.001.

temperature of 22 C and humidity of 50% to 60%.23,24 The subjects were seated in a stable position during the measurement, facing up, with glasses removed to prevent pressure on the nose and possible change of nose shape. Before each measurement, the system was calibrated. The most suitable nose adapter was chosen, and gel was applied to the tip of the nose adapter to prevent sound wave loss. It was set at an angle of 45 so as not to disturb the nostril anatomy. Measurements were carried out after cleaning the subject's nose and without using decongestant to ensure standardization.25-27 The nasal volume was computed separately for each nostril as the volume of the nasal cross-section 5 cm from the nasal inlet. The total volume of the nasal cavity was calculated by summing the volumes of each nostril (total nasal volume 5 volume right 1 volume left).28,29 Plaque index30 and gingival index31 values were measured at 6 sites (mesiobuccal, distobuccal, midbuccal, mesiolingual, midlingual, distolingual) for all teeth with a Williams probe. Periodontal measurements were calculated as the sum of the mean scores of each examined tooth divided by the number of evaluated teeth. Scores for the plaque index were defined as follows: 0, no plaque in the gingival area; 1, a film of plaque adhering to the free gingival margin and adjacent area of the tooth that could be recognized only by running a probe across the tooth surface; 2, moderate accumulation of soft deposits in the gingival pocket and on the gingival margin and adjacent tooth surface that could be seen by the naked eye; and 3, abundance of soft matter in the gingival pocket and on the gingival margin and adjacent tooth surface. Scores for the gingival index were defined as follows: 0, normal gingiva; 1, mild inflammation, slight change in color, slight edema, and no bleeding on palpation; 2, moderate inflammation, redness, edema, glazing,

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and bleeding on probing; and 3, severe inflammation, marked redness and edema, ulceration, and tendency to spontaneous bleed. Statistical analysis

The power analysis showed that for a power of 0.80, with an a error of 0.05 (effect size 1.1), 15 patients were required for each group. Statistical analysis was performed with SPSS software (version 20.0; IBM, Armonk, NY). The distribution of variables was evaluated by the Shapiro-Wilk test. The Wilcoxon signed rank test and the paired t test were performed for intragroup comparisons. The Mann-Whitney U test and the Student t test were used for intergroup comparisons. The Spearman rank order correlation was applied to measure the association between halitosis and nasal cavity volume. P values equal to or less than 0.05 were considered statistically significant. RESULTS

The changes in mean intercanine and intermolar width were 2.33 6 1.54 mm and 6.33 6 1.54 mm, respectively (T0-T1). The mean and median values of halitosis, periodontal scores, and nasal cavity measurements are given in Tables I through III. For the halimeter measurements (T0-T1), the intragroup evaluation showed that, in the RME group, the measurements decreased significantly (P \0.001); however, there were no statistically significant differences in the control group. Intergroup analysis showed significant differences (P \0.001) (Table I). For the organoleptic measurements (T0-T1), the organoleptic values and the intragroup and intergroup comparisons showed significant differences in the RME

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Table II. Comparison of total nasal volume of groups and changes between T0 and T1

Nasal total volume RME group Control group Between groups




7.36 (4.81-9.33) 9.26 (5.55-13.65) Z 5 –2.64yb

Median (minimum-maximum) 10.69 (7.99-15.07) 9.27 (5.53-14.02) Z 5 –1.93b

3.31 (0.04-6.30) 0.06 (–0.59-0.89) Z 5 –4.41yb

P 0.001ya 0.267a

a, Wilcoxon signed rank test; b, Mann-Whitney U test. Significance: *P #0.01; yP #0.001.

Table III. Comparison of plaque and gingival index records of groups and changes between T0 and T1 T0



Plaque index RME group Control group Between groups

1.08 6 0.55 0.60 6 0.43 0.252d

Mean 6 SD 0.87 6 0.24 0.73 6 0.24 0.252d

0.21 6 0.59 0.12 6 0.42 0.115d

Gingival index RME group Control group Between groups

0.25 (0-1.5) 0 (0-1.31) Z 5 0.00c

Median (minimum-maximum) 0 (0-1.25) 0 (0-1) Z 5 –1.58c

P 0.195b 0.280b

0.09 (–1.5-0.44) 0 (–1.08-0.25) Z 5 –1.18c

0.05*a 0.263a

a, Wilcoxon signed rank test; b, paired t test; c, Mann-Whitney U test; d, Student t test. *Significant at P #0.05.

group (P \0.001). Nevertheless, no significant difference was found in the control group (Table I). A significant positive correlation was found between the halimeter and organoleptic methods (r 5 0.725; P #0.001). For the nasal measurements (T0-T1), although significant differences were observed in total nasal volume values in the RME group (P\0.01), no significant difference was found in the control group. Intergroup analysis showed significant differences (P \0.001) (Table II). For the plaque ındex records (T0-T1), intragroup and intergroup comparisons showed no significant differences (Table III). For the gingival ındex records (T0-T1), the intragroup evaluation showed a significant decrease in measurement values (P #0.05) in the RME group, however, there were no statistical differences in the control group. Intergroup comparisons showed no significant differences (Table III). The Spearman rank order correlation coefficients between the nasal cavity volume and the halitosis measurements are shown in Table IV. Total nasal volume showed statistically significant negative correlations with the halimeter and organoleptic measurements (r 5 0.598, P \0.001; and r 5 0.716, P \0.001, respectively).

Table IV. Correlation coefficients between total nasal

cavity volume and halitosis Correlation coefficients r 0.598 0.716

Halimeter Organoleptic

P \0.001* \0.001*

*Significant at P #0.001.


More than 85 million people worldwide experience oral malodor problems, and they spend over $2 billion each year to mask their malodors.1 This situation poses problems in their social lives, and makes people isolate themselves from society and consume millions of prescribed or unprescribed drugs each year for the solution.32 Therefore, it is important to carry out studies related to this subject. Detection of the VSCs responsible for the malodor was done with the halimeter device. It is a handy, lowcost, and objective method,33 but measuring VSCs is not adequate for determining oral malodor. The organoleptic method might be used to diagnose malodor stemming from other gases.34 This method gives more

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subjective results than does the halimeter measurement. Hence, it was thought that more reliable results would be obtained by using both methods. Several methods are used for nasal cavity measurements: tomography, rhinomanometry, acoustic rhinometry, and cephalograms.25 Acoustic rhinometry is a noninvasive, painless, and handy method that does not require patient cooperation.35 It is widely accepted in clinical practices; however, there are some differences in practice.8,24-27,36 In this study, acoustic rhinometry measurements were taken each nostril under basal conditions (no nasal decongestants). Measurements under basal condition is more realistic when determining anatomic and functional variabilities26,27 In addition, Doruk et al25 reported that reliable results can be obtained without using nasal decongestants. RME could also result in various alterations in addition to dental and skeletal effects such as changes in urinary incontinence rates,37 improvement in transmission type hearing loss,9 and reductions in rhinitis and asthma.38 Furthermore, our results suggest that a decrease in oral malodor can also be a consequence of RME. In previous studies, it is reported that braces, ligatures and orthodontic appliances often cause plaque accumulation, and in case of insufficient oral hygiene; periodontal inflammation, hyperemia and hyperplasia may occur.12,14,16 This situation may induce periodontal problem and halitosis. The stability of the plaque index could only be explained by the hygienic motivation provided to the subjects at the beginning of the treatment, the hygienic nature of the hyrax appliance,39 and the involvement of the first premolars and first molars rather than fixed orthodontic attachments. In agreement these findings, studies have suggested that plaque index values decrease immediately after the application of orthodontic attachments.18 RME separates the walls of the nasal cavity laterally. This situation increases intranasal capacity and improves breathing.36 The increase in the volume of the nasal cavity in our study may have improved our subjects' breathing. This may have facilitated nasal breathing and reduced periodontal inflammation caused by oral breathing, leading to a decrease in the gingival index.40 However, these differentiations may not consistently and predictably relate to changes in the mode of breathing. Oral breathing is a complex phenomenon and cannot be explained simply.8 Thus, it would be helpful to use a method that can objectively evaluate the respiratory mode in studies about this topic. RME, unlike fixed orthodontic treatment, makes a dentofacial orthopedic change. Orthopedic effects could result in greater intranasal capacity and improved

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breathing.36 Consequently, the flow rate and quantity of saliva could be increased, and the reproduction of gram-negative anaerobic bacteria could be prevented by higher oxygen intake.2,3 This information supports the decrease in oral malodor. CONCLUSIONS

Halitosis is a common complaint of many people. It occurs worlwide and has a multifactorial etiology. Our study showed that RME could be an alternative treatment for patients suffering from maxillary constriction and halitosis. Further studies on halitosis and the factors related to its etiology are needed. ACKNOWLEDGMENT

We thank Serkan Erat for his support and guidance in the statistical assessments. REFERENCES 1. Rio D, Coelho AC, Nicola EM, Teixeira AR. Halitosis: an assessment protocol proposal. Braz J Otorhinolaryngol 2007;73:835-42. 2. Sanz M, Roldan S, Herrera D. Fundamentals of breath malodour. J Contemp Dent Pract 2001;2:1-17. 3. McDowell JD, Kassebaum DK. Diagnosing and treating halitosis. J Am Dent Assoc 1993;124:55-64. 4. Porter SR, Scully C. Oral malodour (halitosis). BMJ 2006;333: 632-5. 5. Laptook T. Conductive hearing loss and rapid maxillary expansion: report of a case. Am J Orthod 1981;80:325-31. 6. Mitsuda ST, Pereira MD, Passos AP, Hino CT, Ferreira LM. Effects of surgically assisted rapid maxillary expansion on nasal dimensions using acoustic rhinometry. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2010;109:191-6. 7. Zambon C, Ceccheti M, Utumi E, Pinna F, Machado G, Peres M, et al. Orthodontic measurements and nasal respiratory function after surgically assisted rapid maxillary expansion: an acoustic rhinometry and rhinomanometry study. Int J Oral Maxillofac Surg 2012;41:1120-6. 8. De Felippe NL, Da Silveira AC, Viana G, Kusnoto B, Smith B, Evans CA. Relationship between rapid maxillary expansion and nasal cavity size and airway resistance: short- and long-term effects. Am J Orthod Dentofacial Orthop 2008;134:370-82. 9. Kilic N, Kiki A, Oktay H, Selimoglu E. Effects of rapid maxillary expansion on conductive hearing loss. Angle Orthod 2008;78:409-14. 10. Sokucu O, Akpinar A, Ozdemir H, Birlik M, Calisir M. The effect of fixed appliances on oral malodor from beginning of treatment till 1 year. BMC Oral Health 2016;16:14. 11. Gray LP. Results of 310 cases of rapid maxillary expansion selected for medical reasons. J Laryngol Otol 1975;89:601-14. 12. Babacan H, Sokucu O, Marakoglu I, Ozdemir H, Nalcaci R. Effect of fixed appliances on oral malodor. Am J Orthod Dentofacial Orthop 2011;139:351-5. 13. Doruk C, Ozturk F, Ozdemir H, Nalcaci R. Oral and nasal malodor in patients with and without cleft lip and palate who had undergone orthodontic therapy. Cleft Palate Craniofac J 2008; 45:481-4.

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27. Roithmann R, Cole P, Chapnik J, Shpirer I, Hoffstein V, Zamel N. Acoustic rhinometry in the evaluation of nasal obstruction. Laryngoscope 1995;105:275-81. 28. Millqvist E, Bende M. Reference values for acoustic rhinometry in subjects without nasal symptoms. Am J Rhinol 1998;12: 341-3. 29. Hilberg O, Pedersen O. Acoustic rhinometry: recommendations for technical specifications and standard operating procedures. Rhinol Suppl 2000;16:3-17. 30. Silness J, Loe H. Periodontal disease in pregnancy II. Correlation between oral hygiene and periodontal condition. Acta Odontol Scand 1964;22:121-35. 31. Loe H. The gingival index, the plaque index and the retention index systems. J Periodontol 1967;38:610-6. 32. Scully C, Greenman J. Halitosis (breath odor). Periodontol 2000 2008;48:66-75. 33. Van den Broek AM, Feenstra L, de Baat C. A review of the current literature on aetiology and measurement methods of halitosis. J Dent 2007;35:627-35. 34. Loesche WJ, Kazor C. Microbiology and treatment of halitosis. Periodontol 2000 2002;28:256-79. 35. Terheyden H, Maune S, Mertens J, Hilberg O. Acoustic rhinometry: validation by three-dimensionally reconstructed computer tomographic scans. J Appl Physiol (1985) 2000;89:1013-21. 36. Hershey HG, Stewart BL, Warren DW. Changes in nasal airway resistance associated with rapid maxillary expansion. Am J Orthod 1976;69:274-84. 37. Schutz-Fransson U, Kurol J. Rapid maxillary expansion effects on nocturnal enuresis in children: a follow-up study. Angle Orthod 2008;78:201-8. 38. Schuster G, Borel-Scherf I, Schopf PM. Frequency of and complications in the use of RPE appliances results of a survey in the Federal State of Hesse, Germany. J Orofac Orthop 2005;66: 148-61. 39. Biederman W. A hygienic appliance for rapid expansion. JPO J Pract Orthod 1968;2:67-70. 40. Gulati M, Grewal N, Kaur A. A comparative study of effects of mouth breathing and normal breathing on gingival health in children. J Indian Soc Pedod Prev Dent 1998;16:72-83.

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