Morphologic changes of the nasal cavity induced by rapid maxillary expansion: A study on 3-dimensional computed tomography models

Morphologic changes of the nasal cavity induced by rapid maxillary expansion: A study on 3-dimensional computed tomography models

ORIGINAL ARTICLE Morphologic changes of the nasal cavity induced by rapid maxillary expansion: A study on 3-dimensional computed tomography models ¨ ...

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ORIGINAL ARTICLE

Morphologic changes of the nasal cavity induced by rapid maxillary expansion: A study on 3-dimensional computed tomography models ¨ zkayae Adam Haralambidis,a Arzu Ari-Demirkaya,b Ahu Acar,c Nazan Ku¨c¸u¨kkelesx,d Mustafa Atesx,e and Selin O Istanbul, Turkey Introduction: The aim of this study was to evaluate the effect of rapid maxillary expansion on the volume of the nasal cavity by using computed tomography. Methods: The sample consisted of 24 patients (10 boys, 14 girls) in the permanent dentition who had maxillary constriction and bilateral posterior crossbite. Ten patients had skeletal Class I and 14 had Class II relationships. Skeletal maturity was assessed with the modified cervical vertebral maturation method. Computed tomograms were taken before expansion and at the end of the 3-month retention period, after active expansion. The tomograms were analyzed by Mimics software (version 10.11, Materialise Medical Co, Leuven, Belgium) to reconstruct 3-dimensional images and calculate the volume of the nasal cavities before and after expansion. Results and Conclusions: A significant (P 5 0.000) average increase of 11.3% in nasal volume was found. Sex, growth, and skeletal relationship did not influence measurements or response to treatment. A significant difference was found in the volume increase between the Class I and Class II patients, but it was attributed to the longer expansion period of the latter. Therefore, rapid maxillary expansion induces a significant average increase of the nasal volume and consequently can increase nasal permeability and establish a predominant nasal respiration pattern. (Am J Orthod Dentofacial Orthop 2009;136:815-21)

R

apid maxillary expansion (RME) is a commonly used orthodontic procedure for correcting transverse maxillary deficiency. This method was first described by Angell1 in 1860 and popularized by Haas2-5 100 years later. The concept of RME was extended to the nasal cavity,6 because it was suggested that, with expansion, increases in nasal width and volume are obtained.4,5,7-10 Wertz8 confirmed the advantages of RME in improving nasal airflow in patients with stenosis of the nasal airway. However, he stated that, since only the maxilla is gripped by the appliance and the midpalatal suture opens more anteriorly, RME for the sole purpose

From the Department of Orthodontics, Faculty of Dentistry, Marmara University, Istanbul, Turkey. a Former fellow; private practice, Thessalonicki, Greece. b Assistant professor. c Associate professor. d Professor and department chair. e Research assistant. Supported by the Scientific Research Projects Commission of Marmara University (BAPKO), project number SAG-BGS-060907-0173 The authors report no commercial, proprietary, or financial interest in the products or companies described in this article. Reprint requests to: Adam Haralambidis, Department of Orthodontics, Faculty of Dentistry, Marmara University, G}uzelbahc¸e B}uy}uk C¸iftlik Sk. No 6, Nisantasi, 34 367, Istanbul, Turkey; e-mail, [email protected]. Submitted and accepted, March 2008. 0889-5406/$36.00 Copyright Ó 2009 by the American Association of Orthodontists. doi:10.1016/j.ajodo.2008.03.020

of increasing nasal permeability can be justified only when the obstruction is in the lower anterior portion of the nasal cavity and accompanied by bilateral maxillary arch-width deficiency. RME effects on the reduction of nasal airway resistance were established by Linder-Aronson and Aschan11 and Hershey et al.12 Their findings were supported by Warren et al,13 who reviewed the nasal airway after expansion and reported 45% and 55% increases in nasal cross-sectional areas after RME and surgically assisted RME, respectively. RME altered the nasal valve area, reducing its resistance to airflow during breathing; this reduction was stable for at least a year.14 Previous methods for assessing nasal cavity volume included lateral and posteroanterior radiographs.15-19 Although those methods were useful in determining the obstruction of the nasal and pharyngeal areas, they were inadequate for measuring nasal resistance and nasal volume. Montgomery et al20 initially studied nasal airways in human cadavers using computed tomography (CT) and established that accurate volume measurements of the nasal airway from CT images were possible. The use of CT allows measurements with fewer projection, magnification, and distortion errors. Furthermore, CT confines the radiation to the plane of interest, minimizes blurring, and permits visualization of small variations in tissue density. Nevertheless, CT 815

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is an expensive, time-consuming method that delivers a higher dose of radiation than any other type of radiography.21 Therefore, its application should be considered with regard to the radiation dose and the need for more detailed information. The development of new computer software in the field of fast and precise axial acquisition of many thin slices and the potential for multiplanar, 3-dimensional (3D) reconstruction contribute to extending the possibilities in diagnosis. The purposes of this study were to develop a technique to use 3D modeling of CT data for nasal airway assessment and to evaluate the effects of RME on the change in nasal volume with CT. MATERIAL AND METHODS

This project was approved by the ethics committee of the Institute of Health Sciences of Marmara University, Istanbul, Turkey, and informed consent forms were signed by the parents of all patients. The sample consisted of patients who sought orthodontic treatment at the Department of Orthodontics of Marmara University. The selection criteria were age (10-17 years), transverse maxillary deficiency with bilateral posterior crossbite, complete permanent dentition, no systemic disease, and no previous orthodontic treatment. The study group comprised 24 patients (mean age, 14.5 years), 10 boys (mean age, 15.2 years) and 14 girls (mean age, 14.0 years). Ten had a Class I skeletal relationship, and 14 had a Class II skeletal relationship. The patients’ skeletal maturity was determined by using the improved cervical vertebral maturation method, developed by Baccetti et al.22 Table I shows the distribution of the 2 malocclusion groups according to sex and skeletal maturation. RME was accomplished by using the cemented acrylic cap splint appliance (hyrax screw, GH Wire Company, Hannover, Germany). After cementation, the screw was turned by the clinician twice, and instructions were given to the patients’ parents to activate the appliance a quarter turn of the screw twice a day. In all patients, expansion was terminated just before reaching buccal crossbite, without any discomfort or failure of the appliance. The screw was secured with a stainless steel ligature wire, and the RME appliance was left in place for 3 months as a retention appliance. Then it was removed, and a soldered transpalatal arch with arms extending along the palatal aspects of the premolars was placed. Comprehensive orthodontic treatment began soon after the retention period. CT images of the head were obtained before treatment. At the end of the 3-month retention period, after

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Sex, dental relationship, and skeletal maturation distribution of the sample

Table I.

Class I Sex Male Female Growth stage (CVM) 3 4 5

Class II

5 5

50.0% 50.0%

5 9

35.7% 64.3%

4 4 2

40.0% 40.0% 20.0%

5 5 4

35.7% 35.7% 28.6%

removal of the acrylic cap splint, the records were repeated. It was essential to perform the second CT scanning before the placement of the transpalatal arch, because metal causes artefacts that influence imaging quality and diagnostic accuracy. A spiral CT machine (Siemens Sensation 40, Siemens Medical Solutions, Erlangen, Germany) was used at 120 KV and 80 mAs. A scanning filter with a field of view of 12.6 3 12.6 cm and a matrix of 512 3 512 pixels was used. Axial sections with a slice increment of 0.3 mm were made, including the patient’s entire head. The data from the CT images were transferred to a network computer workstation on which 2-dimensional reformatted images were generated and measured. The software was Mimics (version 10.11, Materialise Medical Co, Leuven, Belgium). Mimics imports 2-dimensional stacked images, such as CT or magnetic resonance images, and displays the data in several ways, by dividing the screen into 4 views: original axial view, coronal view (made up of resliced data), sagittal view (made up of resliced data), and 3D view (Fig 1). Initially, while going through the sliced images in the axial view, points and planes were drawn as reference guides for the borders of the apertures of the nares (Fig 2). In the coronal view, the connection with the outer air was cropped slice by slice with the segmentation tools of the software, by using as references the 2 planes drawn previously. Consequently, any connection with the outer air was eliminated for the nasal airway to be depicted (Fig 3). With the patient’s airway isolated (Fig 4), a 3D object of the airway is created through the flexible interface provided by the software (Fig 5). To separate the anterior nasal cavity from the entire airway, 3 reference points were selected on the 3D object: the most posterior point along the anterior border, immediately behind the soft-tissue nasion on the lateral view, and the 2 most lateral and inferior points corresponding to the soft-tissue contour of the nares on the frontal view. The area bounded by these points was highlighted (Fig 5), and the volume was calculated by the software.

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Fig 1. The Mimics screen.

Fig 3. Coronal slice. Cropping tool (black) cutting off the connection between the nasal airway and the outer air.

Fig 2. Axial slice. Reference planes drawn on the slice with the largest cross-sectional area of the nares.

For assessment of intraobserver method error, 10 randomly selected CT images were reanalyzed 3 weeks later with the same conditions. Intraclass correlation coefficients of the repeated volumetric values were calculated.

Statistical analysis was performed with software for Windows (version 2007, NCSS Statistical & Power Analysis Software, Kaysville, Utah). The Wilcoxon signed rank test was used to assess preexpansion and postexpansion values in the groups, and the Mann-Whitney U test was used to compare the Class I and Class II groups and the sex differences. The Kruskal-Wallis test was used to compare groups defined by the patients’ growth stages and groups defined by the patients’

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Fig 4. Sagittal slice. Isolation of the nasal airway verified in the sagittal view.

expansion durations. All results were evaluated within a 95% confidence interval, and the level of statistical significance was established at P \0.05. RESULTS

The intraclass correlation coefficient for the entire group of volumetric values was 0.999, with a 0.992 to 0.999 confidence interval, demonstrating a high rate of consonance between measurements and confirming the reliability and the reproducibility of the method. In both malocclusion groups, and in the entire sample, a statistically significant increase in the volume of the nasal cavity was observed (Table II). A significant difference (P 5 0.000) was found when the expansion durations of the Class I and Class II patients were compared, resulting in a significant difference (P 5 0.046) in the nasal-volume increase between these groups (Table II). This difference was also reflected when patients were divided into groups according to the duration of the expansion (Table III). Patients expanded for less than 21 days were all Class I, whereas patients expanded longer were all Class II. Tables IV and V show that skeletal maturity and sex did not influence the response to treatment or the measurements in a statistically significant manner. Table VI compares the changes in the Class I and Class II groups. DISCUSSION

RME is a recognized treatment modality indicated for constricted maxillary arches. Doubt had been expressed as to whether RME results in movement of the nontooth-bearing bones of the maxillary complex

Fig 5. 3D appearance of the nasal airway isolated. Landmarks (pink) depict the borders chosen to calculate the volume of the anterior nasal cavity (light brown). A, Lateral view; B, frontal view.

because of their articulations with cranial and facial bones, buttressing, and sutural slippage.9 Timms,23 however, showed that lateral walls of the nasal cavity move outward, increasing the nasal cavity’s width, volume, and minimal cross-sectional area. There are also some downward and forward movements of the palate, but, because of the triangular opening of the suture, the greatest increase is in the width of the nasal floor.24 Since the nasal cavity is high and narrow, a small increase in width will produce a great increase in crosssectional area; this is the primary determinant of the magnitude of the nasal airway resistance and will permit the passage of a vastly increased volume of air. Acoustic rhinometry was introduced as a useful tool for measuring nasal cavity dimensions by Hilberg et al,25 because it analyzes sound waves reflected in the nasal cavity and is potentially useful for characterizing the geometry of the nasal cavity. Hahn et al26 reported an increase of 10.13% in the volume of the nasal cavity after RME, evaluated and calculated with acoustic rhinometry. Babacan et al,27 also using acoustic rhinometry, reported a 13.8% increase

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Table II.

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Volumetric changes of the sample

Malocclusion Class I Mean SD Minimum Maximum Class II Mean SD Minimum Maximum Total Mean SD Minimum Maximum Intergroup comparison with Mann-Whitney U test, P value

Intragroup comparison with Wilcoxon test, P value

V1 (mm3)

V2 (mm3)

Increase (%)

18.7 2.4 15 21

5522.81 1304.20 3004.92 7144.51

5933.51 1408.31 3137.30 7690.49

7.59 8.51 0.34 27.28

0.005

27.2 4.1 23 35

5376.33 970.78 4122.05 7413.98

6125.84 1167.42 4551.70 8503.01

13.95 6.60 0.64 22.03

0.001

23.7 5.5 15 35 0.0001

5437.36 1097.13 3004.92 7413.98 0.639

6045.70 1247.31 3137.30 8503.01 0.861

11.30 7.95 0.64 27.28 0.046

0.0001

ED (days)

ED, Expansion duration; V1, nasal volume before expansion; V2, nasal volume after retention. Table III.

Comparison of volumetric changes between groups defined by the expansion duration Expansion duration (days)

3

V1 (mm ) V2 (mm3) Increase (%)

\21 (n 5 9)

21-25 (n 5 8)

.25 (n 5 7)

Kruskal-Wallis test, P value

5374.92 6 1291.32 5788.70 6 1412.57 7.82 6 8.99

5640.93 6 942.84 6467.70 6 922.85 15.20 6 5.64

5285.00 6 1124.96 5893.85 6 1395.12 11.33 6 7.67

0.832 0.434 0.105

V1, Nasal volume before expansion; V2, nasal volume after retention. Table IV.

Comparison of volumetric changes in skeletal maturation groups Growth stage

3

V1 (mm ) V2 (mm3) Increase (%)

CVM 3 (n 5 9)

CVM 4 (n 5 9)

CVM 5 (n 5 6)

Kruskal-Wallis test, P value

5115.50 6 1336.33 5629.48 6 1412.73 10.33 6 7.91

5837.57 6 1015.98 6516.99 6 1293.28 11.47 6 9.12

5319.85 6 732.7 5963.11 6 753.24 12.50 6 7.35

0.363 0.244 0.895

V1, Nasal volume before expansion; V2, nasal volume after retention; CVM, cervical vertebral maturation.

in nasal volume. Oliveira28 evaluated the nasal-volume changes induced by RME with acoustic rhinometry and reported an increase in nasal volume of 17.5%, higher than any other; this difference could be attributed to the age range of the patients (8-16 years) and to expansion duration (longer than in any other study). Previous investigations compared results from acoustic rhinometry with those from CT.29,30 Technical advances in CT and computer technology have made it possible to create a 3D reconstruction of the nasal airway, through which the nasal cavity was visualized, and its volume was calculated by computer software such as that we used in this study.

Doruk et al31 demonstrated reasonably good agreement between results from acoustic rhinometry and CT. The increases in nasal volume after RME were reported to be 13.28% and 11.16%, respectively. Those results are similar to our results (nasal-volume increase of 11.3%), although there were differences in the RME appliance, expansion protocol, retention period, and measurement method. The agreement among the results of this study with CT and previous ones with acoustic rhinometry suggests that both measurement methods are scientifically reliable, reproducible, and capable of quantifying the nasal-volume increase after RME. In our study, we tried

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Table V.

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Comparison of volumetric changes between the sexes

3

V1 (mm ) V2 (mm3) Increase (%)

Male (n 5 10)

Female (n 5 14)

Mann-Whitney U test, P value

6017.21 6 891.32 6724.58 6 802.69 12.44 6 7.75

5023.19 6 1065.94 5560.79 6 1303.35 10.49 6 8.28

0.019 0.022 0.682

V1, Nasal volume before expansion; V2, nasal volume after retention. Table VI. Comparison of volumetric changes within groups defined by skeletal relationship V1 (mm3)

V2 (mm3)

Class I 5522.81 6 1304.2 5933.51 6 1408.31 Class II 5376.33 6 970.78 6125.84 6 116742 All groups 5437.36 6 1097.13 6045.7 6 1247.31

t

P

2.8 0.005 3.23 0.001 4.22 0.0001

capacity and nasal permeability, and establish a predominant nasal respiration pattern. A follow-up study of our subjects is already underway, because it will provide valuable long-term results regarding the stability of the nasal-volume increase. CONCLUSIONS

V1, Nasal volume before expansion; V2, nasal volume after retention.

to establish a standardized method that could be used reliably, in spite of the variability of subjects. The precision of this technique depends greatly on the accuracy of selecting points and planes on the single views and on the 3D object because of the features of Mimics. The high reproducibility of the method, demonstrated by the high rate of consonance between repeated measurements, the ease of use, and the small amount of time required for an analysis, make it valuable for future investigations. Statistical analysis of our results showed no correlations between the volume increase and sex or skeletal maturation stage of the patients. The latter can be attributed to the fact that growth was not an important factor in the volume increase because of the limited 3-month retention period. However, a significantly smaller increase in the volume of the nasal cavity was observed in the Class I group, almost half that in the Class II group. The patient’s dental and skeletal relationship should not be a determining factor in nasal cavity volume increase; however, the difference observed can be explained by the significantly shorter expansion duration in the Class I group. This fact was corroborated through comparison of volume increases of patients, grouped according to expansion durations (the group expanded for \21 days consisted of Class I patients). The relatively smaller volume increase in the group that was expanded the longest (.26 days) was unexpected, when viewed at first. This could be attributed to the great individual variations, but also because some patients who had difficulties in following expansion instructions that delayed the expansion procedure, were included in this group. Therefore, expansion duration proved to be a determining factor in the amount of nasal cavity volume increase. Consequently, since RME induces a significant average increase of nasal volume, it might increase intranasal

1.

2.

3.

Within the limitations of this study, the results suggest an average increase of 11.3% in the volume of the anterior nasal cavity induced by RME, but there were wide individual variations. Therefore, RME should not be advocated solely to increase the volume of the nasal cavity and improve nasal respiration, unless there is also a transverse maxillary deficiency. The significant difference in volume increases between malocclusion groups was attributed to the differences in expansion duration. Sex and growth were not determining factors in the amounts of nasal cavity volume increase. The method developed to use 3D reconstruction of the nasal airway with Mimics software on CT data proved to be precise, efficient, and reliable. Longterm stability of the nasal-volume increase should be investigated.

We thank Kutsal Tuac¸, general manager of 4C Medikal, for allowing us to use Mimics 10.11 and Erdem Okc¸uog˘lu for his valuable insights. REFERENCES 1. Angell EC. Treatment of irregularities of the permanent or adult teeth. Dent Cosmos 1860;1:540-4. 2. Haas AJ. Rapid expansion of the maxillary dental arch and nasal cavity by opening the midpalatal suture. Angle Orthod 1961;31: 73-90. 3. Haas AJ. The treatment of maxillary deficiency by opening the midpalatal suture. Angle Orthod 1965;35:200-17. 4. Haas AJ. Palatal expansion: just the beginning of dentofacial orthopedics. Am J Orthod 1970;57:219-55. 5. Haas AJ. Long-term posttreatment evaluation of rapid palatal expansion. Angle Orthod 1980;50:189-217. 6. Brown GVI. The application of orthodontic principles to nasal disease. Iowa State Dent Soc Trans 1902;67-79. 7. Derichsweiler H. Die gaumennahtsprengung. Fortschr Kieferorthop 1953;14:5-23.

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8. Wertz RA. Changes in nasal airflow incident to rapid maxillary expansion. Angle Orthod 1968;38:1-11. 9. Wertz RA. Skeletal and dental changes accompanying rapid midpalatal suture opening. Am J Orthod 1970;58:41-66. 10. White BC, Woodside DG, Cole P. The effect of rapid maxillary expansion on nasal airway resistance. J Otolaryngol 1989;18: 137-43. 11. Linder-Aronson S, Aschan G. Nasal resistance to breathing and palatal height before and after expansion of the median palatal suture. Odont Rev 1963;14:254-70. 12. Hershey HG, Stewart BL, Warren DW. Changes in nasal airway resistance associated with rapid maxillary expansion. Am J Orthod 1976;69:274-84. 13. Warren DW, Hershey HG, Turvey TA, Hinton VA, Hairfield WM. The nasal airway following maxillary expansion. Am J Orthod Dentofacial Orthop 1987;91:111-6. 14. Warren DW. Aerodynamic studies of upper airway: implication for growth, breathing and speech. In: McNamara JA, editor. Nasorespiratory function and craniofacial growth. Craniofacial Growth Series. Ann Arbor: Center for Human Growth and Development; University of Michigan; 1979. 15. Cross DL, McDonald JP. Effect of rapid maxillary expansion on skeletal, dental and nasal structures: a postero-anterior cephalometric study. Eur J Orthod 2000;25:519-28. 16. Chung CH, Font B. Skeletal and dental changes in the sagittal, vertical, and transverse dimensions after rapid palatal expansion. Am J Orthod Dentofacial Orthop 2004;126:569-75. 17. Basciftci FA, Mutlu N, Karaman AI, Malkoc S, Ku¨c¸u¨kkolbasi H. Does the timing and method of rapid maxillary expansion have an effect on the changes in nasal dimensions? Angle Orthod 2002;72: 118-23. 18. Handelman CS, Osborne G. Growth of the nasopharynx and adenoid development from one to eighteen years. Angle Orthod 1976; 46:243-59. 19. Behfelt K, Linder-Aronson S, Neander P. Posture of the head, the hyoid bone, and the tongue in children with and without enlarged tonsils. Eur J Orthod 1990;12:458-67.

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20. Montgomery WM, Vig PS, Staab EU, Matteson SR. Computed tomography: a three-dimensional study of the nasal airway. Am J Orthod 1979;76:363-75. 21. Clark DE. Radiation absorbed from dental implant radiography: a comparison of linear tomography, CT scan, and panoramic and intra-oral techniques. J Oral Implantol 1990;16: 156-64. 22. Baccetti T, Franchi L, McNamara JA Jr. An improved version of the cervical vertebral maturation (CVM) method for the assessment of mandibular growth. Angle Orthod 2002;72:316-23. 23. Timms DJ. A study on basal movement with rapid maxillary expansion. Am J Orthod 1980;77:500-7. 24. McDonald JP. Airway problems in children: can the orthodontist help? Ann Acad Med Singapore 1995;24:158-62. 25. Hilberg O, Jackson AC, Swift DL, Pedersen OF. Acoustic rhinometry: evaluation of nasal cavity geometry by acoustic reflection. J Appl Physiol 1989;66:295-303. 26. Hahn L, Marchioro EM, Rizzatto SD, Roithmann R, Costa NP. Avaliacao do volume da cavidade nasal antes e apos expansao rapida da maxilla por meio da rinometria acoustica. Ortodontia Gaucha 1999;III:85-96. 27. Babacan H, So¨ku¨cu¨ O, Doruk C, Ay S. Rapid maxillary expansion and surgically assisted rapid maxillary expansion effects on nasal volume. Angle Orthod 2006;76:66-71. 28. Oliveira NL. Assessment of rapid maxillary expansion and its effects on the nasal cavity’s size and airway resistance [thesis]. Chicago: University of Illinois at Chicago; 2005. 29. Hilberg O, Jensen FT, Pedersen OF. Nasal airway geometry: comparison between acoustic reflection and magnetic resonance scanning. J Appl Physiol 1993;75:2811-9. 30. Cakmak O, Coskun M, Celik H, Buyuklu F, Ozluoglu LN. Value of acoustic rhinometry for measuring nasal valve area. Laryngoscope 2003;113:295-302. 31. Doruk C, So¨ku¨cu¨ O, Bicakci AA, Yilmaz U, Tas x F. Comparison of nasal volume changes during rapid maxillary expansion using acoustic rhinometry and computed tomography. Eur J Orthod 2007;29:251-5.