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Rapid maxillary expansion in growing patients: Correspondence between 3-dimensional airway changes and polysomnography
International Journal of Pediatric Otorhinolaryngology 78 (2014) 23–27
Contents lists available at ScienceDirect
International Journal of Pediatric Otorhinolaryngology journal homepage: www.elsevier.com/locate/ijporl
Rapid maxillary expansion in growing patients: Correspondence between 3-dimensional airway changes and polysomnography Alberto Caprioglio a, Matteo Meneghel a, Rosamaria Fastuca a,*, Piero Antonio Zecca a, Riccardo Nucera b, Luana Nosetti c a b c
Department of Orthodontics, University of Insubria, Varese, Italy Department of Orthodontics, University of Messina, Messina, Italy Department of Pediatrics, University of Insubria, Varese, Italy
A R T I C L E I N F O
A B S T R A C T
Article history: Received 1 August 2013 Received in revised form 13 October 2013 Accepted 15 October 2013 Available online 25 October 2013
Objectives: The aim of the present prospective study was to investigate the effects of rapid maxillary expansion on the airway correlating airway volumes computed on cone beam computed tomography and polysomnography evaluation of oxygen saturation and apnea/hypopnea index. Methods: The study group comprised 14 caucasian patients (mean age 7.1 0.6 years) undergone to rapid maxillary expansion with Haas type expander banded on second deciduous upper molars. Cone beam computed tomography scans and polysomnography exams were collected before placing the appliance (T0) and after 12 months (T1). Landmarks localization and airway semiautomatic segmentation on cone beam computed tomography scans allowed airway volume computing and measurements. Results: Increases of total airway volume, oxygen saturation and apnea/hypopnea index were statistically significant. No correlation was found among total airway volume, oxygen saturation and apnea/hypopnea index changes between the examined timepoints. Conclusions: Computing airway volume on cone beam computed tomography allow to measure the amount of air that flows through nasal cavity, nasopharynx and oropharynx while oxygen saturation and apnea/hypopnea index could give information about functional parameters. In the present study all three variables investigated showed statistically significant differences between T0 and T1 but no correlation was found between increases of the different variables tested. ß 2013 Elsevier Ireland Ltd. All rights reserved.
Keywords: Maxillary expansion Polysomnography Mouth breathing Airway
1. Introduction Rapid maxillary expansion (RME) is a common orthodontic treatment to correct transverse maxillary discrepancy. It was suggested that RME might influence nasal morphology [1,2] and breathing pattern [3,4]. Wertz [5] investigated the advantages of RME in improving nasal airflow in patients with nasal stenosis. However, considering the Vshaped opening pattern of the midpalatal suture, he claimed that RME cannot be justified for the sole purpose of increasing nasal permeability unless the obstruction is in the lower anterior portion of the nasal cavity and bilateral maxillary arch-width deficiency. Several studies investigated nasal airway resistance finding reduction of resistances after RME [6,7]. These results were confirmed by Warren et al. [8] who reported 45% increase in nasal cross-sectional areas after expansion.
* Corresponding author at: C/O School of Dentistry, Department of Orthodontics, Via Giuseppe Piatti, 10 Velate, 21100 Varese, Italy. Tel.: +39 3803546218. E-mail address: [email protected] (R. Fastuca). 0165-5876/$ – see front matter ß 2013 Elsevier Ireland Ltd. All rights reserved. http://dx.doi.org/10.1016/j.ijporl.2013.10.011
Airway changes after RME have been studied with different means including acoustic rhinometry, 2d and 3d radiographic technique such as cone beam computed tomography (CBCT). Other diagnostic tool can be employed to investigate the effects of RME on airflow from a more functional point of view. The measurement of the volumes of airway compartments may be biased by several factors such as head and tongue position during CBCT scan acquisition, breathing, swallowing movements, repositioning of the tongue and the mandible after treatment. Moreover threshold-based segmentation of airway may not be standardized although, the method errors were acceptable for the present study. The combination of morphological recording with functional respiratory analyses is therefore recommended. Polysomnography examinations (PSG), often employed in obstructive sleep apnoea (OSA) patients [9], could give further information about breathing pattern, showing quantitative data such as oxygen saturation (SpO2) and apnea/hypopnea index (AHI). The aim of the present prospective study was to investigate the effects of RME on the airway correlating airway volumes computed on CBCT and PSG examinations (SpO2 and AHI).
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A. Caprioglio et al. / International Journal of Pediatric Otorhinolaryngology 78 (2014) 23–27
Table 1 Selection criteria. 1. Age (6–9 years) 2. CVS 1 skeletal maturation 3. Functional unilateral posterior crossbite 4. Early mixed dentition 5. Upper and lower first molars erupted 6. No systemic disease 7. No skeletal asymmetries 8. No previous orthodontic treatment 9. High risk of upper canine impaction
2. Methods Ethical approval for this study was obtained from the local Ethical Committee (no. 5184) and informed consent forms were signed by the parents of all patients. The sample consisted of patients treated at the dental clinic. The selection criteria for the present prospective study are shown in Table 1. The initial study group comprised 21 caucasian patients. 7 patients were considered drop out for low quality of the CBCT scans. The final study sample comprised 14 patients (mean age 7.1 0.6 years), who fully matched inclusion and exclusion criteria. The maxillary expander (Snap Lock Expander 10 mm A1671439, Forestadent, Pforzheim, Germany) used for all subjects was Haas type expander banded to the upper second deciduous molars (Fig. 1) as previously suggested [10]. The maxillary expanders were banded using glass ionomer cement (Multi-Cure Glass Ionomer Cement, Unitek, Monrovia, CA, USA) in accordance with the manufacturer’s instructions. The screw of the palatal expander was initially turned two times (0.45 mm initial transversal activation). Afterwards patients were instructed to turn the screw once per each following day (0.225 mm activation per day). The maxillary expansion was performed until dental overcorrection (2 mm) was achieved or when occlusion relationship evaluated at the first permanent molars was cusp to cusp. At the end of the active expansion period (32 5 days) the screw was locked with light-cure flow composite (Premise Flowable; Kerr Corporation, Orange, CA, USA). The palatal expander was removed 12 months after it was inserted, at the end of the retention period. During this period no other fixed orthodontic appliances were used in any patients. CBCT scans (i-CAT, Imaging Sc. Int., Hatfield, PA, USA) were performed in seated position before inserting the maxillary expander (T0) and at the end of retention (T1), 12 months later when the expander was removed.
Fig. 1. RME on deciduous second molars.
Fig. 2. 3d landmarks and planes. Po: porion right and left; Or: orbitale right and left; PNS: posterior nasal spine; PaF: palatal foramen right and left; OdP: middle point of odontoid process of second cervical vertebra; Epi: top of the epiglottis. Frankfort plane: plane passing through PoR-PoL-OrR-OrL; PNS plane: projection on PNS of plane perpendicular to Frankfort passing through PoR-PoL; odontoid plane: passing through OdP and parallel to Frankfort; epiglottis plane: passing through top of the epiglottis and parallel to Frankfort.
PSG examination (Embletta-EMBLA, Thornton, CO, USA) was performed for all subjects at T0 and T1 to collect SpO2 and AHI. 2.1. Image processing Dicom images were processed in two steps. 2.1.1. Landmarks localization and airway semiautomatic segmentation Dicom images were acquired in Mimics software (version 10.11, Materialise Medical Co, Leuven, Belgium). First a set of reproducible landmarks and planes was defined (Fig. 2). Distance between palatal foramens (PaF) right and left were used to assess total maxillary expansion (Fig. 2). Planes were used to obtain a reproducible position of head and to define airway compartments (Fig. 3). The airway was segmented using thresholding based segmentation manually corrected slice by slice. The upper limit of UPPER AIRWAY was set at the edge between nasal bones and etmoid bone.
Fig. 3. Airway compartments. Upper airway (green) from nares to PNS plane; middle airway (yellow) from PNS plane to OdP plane; lower airway (blue) from OdP plane to epiglottis plane; total airway (AIR) from nares to epiglottis plane. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of the article.)
A. Caprioglio et al. / International Journal of Pediatric Otorhinolaryngology 78 (2014) 23–27
Segmented airway and landmarks were then exported respectively in stereolitographic (.stl) and iges (.igs) files.
Table 2 The different recorded parameters at each time point (n = 14). Parameter
2.1.2. Volume computing The airway and landmarks files were imported in Rhinoceros Software (Robert McNeel & Associates, 3670 Woodland Park Ave, N Seattle, WA 98103, USA) where a logarithmic sequence built for this purpose automatically computed planes and volumes. 2.2. Sample size calculation and method error analysis A sample size of at least 10 subjects per group was necessary to detect an effect size (ES) coefficient [11] of 1.0 for each recorded parameter between the time points, with an alpha set at 0.05 and a power of 0.8. The ES coefficient is the ratio of the difference between the recordings of the two groups (T0 and T1), divided by the within-subject standard deviation (SD). An effect size of at least 0.8 is regarded to as a large effect [11], while a value of at least 1.0 is considered to be associated with good diagnostic potential [12]. With the aim of quantifying the full method error of the recordings for both of these palatal parameters, the method of moments (MME) variance estimator was used [13]. Therefore, the mean error and 95% confidence intervals (CIs) between the repeated recordings were calculated using the MME variance estimator, and were expressed as percentages [14]. The MME variance estimator has the advantages of not being affected by any unknown bias, i.e. systematic errors, between pairs of measurements [13]. 2.3. Data analysis The SPSS software, version 13.0 (SPSS1 Inc., Chicago, IL, USA) and Comprehensive Meta-Analysis, version 2 (BiostatTM, Englewood, NJ, USA) were used to perform the statistical analyses. Parametrical methods were used after having tested the existence of the assumptions though the Shapiro–Wilk test and Levene test for the normality of the distributions and equality of the variances between the time points, respectively. A paired sample t-test was employed to assess the significance of the difference of each parameter between the time points. Within each time point, the contribution of each airway compartment (upper, middle and lower) to the total volume was also calculated as percentage. The significance of the difference of each compartment contribution between the time point was also assessed through a paired sample t-test. Moreover, the ES coefficients for each recorded parameter along the 95% CIs, were calculated between the time points, as previously described [11]. In particular, the paired nature of the data was taken into account and, whenever negative, absolute values have been reported. Finally, a Pearson rho correlation coefficient was employed to evaluate the strength of the relationship between the intra-subject changes (scores at T1 scores at T0) in PF, AIR, SpO2 and AHI. A p value less than 0.05 was used in the rejection of the null hypothesis.
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PF (mm3) AIR (mm3) SpO2 (%) AHI (events)
Time point
ES (95% CI)
T0
T1
26.6 3.0 16 513.5 4554.8 89.8 1.1 5.7 1.2
29.1 3.2*** 21 754.8 8233.7* 95.5 1.6*** 1.4 0.6***
0.77 0.72 4.05 4.43
(0.48–1.06)*** (0.06–1.38)* (1.43–6.68)** (1.62–7.25)**
Data are shown as mean SD. PF, inter-PaF distance; AIR, total airway; SpO2, oxygen saturation; AHI, apnea/hypopnea index; ES, effect size; CI, confidence interval. Levels of significance: *p < 0.05; **p < 0.01; ***p < 0.001
Table 3 The volumes (in mm3) of each airway compartment at each time point (n = 14). Compartment
Time point T0
T1
Upper Middle Lower
7152.8 3074.0 5975.0 2423.7 3385.8 1450.7
9723.3 4329.4* 7067.5 3200.6 4964.1 2506.6
ES (95% CI)
0.62 (0.10–1.15)* 0.36 ( 0.30–1.02) 0.71 ( 0.00–1.43)
Data are shown as mean SD. ES, effect size; CI, confidence interval. Level of significance: *p < 0.05.
ranging from 0.72 to 4.43 for the total AIR volume and AHI, respectively. However, only for the SpO2 and AHI, the full 95% CI of the ES coefficients were above the threshold of 1.0. Regarding the individual airway compartment volumes (Table 3), only for the upper part a statistically significant increase after treatment was seen (p < 0.05), while for the middle and lower part volumes, the values did not change significantly over time. Similarly, only the ES coefficient for the upper airway compartment volume was significantly greater than zero even though lower than the threshold of 1.0 (0.62). The results on the contribution of each compartment to the total airway volume are showed in Fig. 4. The upper and lower compartments showed the greatest and lowest contributions, respectively. The contributions of the upper and lower compartments also underwent a slight increase at T1 as compared to the corresponding baseline values, although these changes did not reach the statistical significance. Results regarding the correlation analyses between the PF, AIR, SpO2 and AHI changes parameters are shown in Table 4. In particular, none of these correlations reached the statistical significance with Pearson’s r values ranging from 0.487 to 0.282 for PF and SpO2 and AHI changes, respectively.
3. Results Method errors as mean (95% CI) ranged from 0.3 (0.1–0.5) to 179.6 (84.2–298.9) for the inter-PaF distance (PF) and total airway (AIR), respectively. Descriptive statistics for each recorded parameter are shown in Table 2. The PF, AIR, SpO2 and AHI (Table 2) recorded at T1 were significantly greater than the corresponding baseline values (p < 0.05, at least). The ES coefficients retrieved for all these parameters were statistically significantly greater than zero and
Fig. 4. The percentage contribution of upper, middle and lower compartments to total airway volume at each time point (n = 14). Within each compartment, the differences between the time points are not statistically significant.
A. Caprioglio et al. / International Journal of Pediatric Otorhinolaryngology 78 (2014) 23–27
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Table 4 Correlation matrix between AIR, SPO and AHI changes (n = 14). Parameter PF AIR SpO2 AHI
PF 1 0.213 0.487 0.282
AIR 1 0.367 0.227
SPO
1 0.051
AHI
1
All the rho correlation coefficients are not statistically significant.
4. Discussion In the present study changes in airway volume, SpO2 and AHI in patients undergone RME were investigated. All three variables investigated showed statistically significant differences between T0 and T1 and the ES coefficients were significant for SpO2 and AHI both. PF variations between the two time points (Table 2) indicated the amount of expansion measured at the bone level (palatal foramens) which allowed to measure the efficiency of RME treatment. Computing airway volume on CBCT scans allow to measure the amount of air that flows through nasal cavity, nasopharynx and oropharynx while SpO2 and AHI could give information about functional parameters. Several studies [15–18] computed airway volume after RME dividing airway in segments in order to better understand changes at different levels. In the present study nasal cavity, middle and lower airway were examined and also the whole volume which comprises the three areas. Based on our results among the three airway compartments only nasal cavity had significant increase after RME. These findings agree with other studies [16,17], also when compared with a control group [18]. In relation to the pharyngeal airway volume, Zhao et al. [15] is the only one who compared the results to a control group and found no significant changes between treated and controls after RME. Matsumoto et al. [19] investigated long-term effects of RME on nasal cavity using acoustic rhinometry, computed rhinomanometry and posteroanterior cephalometric radiography demonstrating an increase in nasal osseous width with less significant increases in nasal area and nasal resistance; in agreement with other studies, he suggested that the effects of RME could be more evident at the bony level [20,21] than at the mucosal level and this might be due to compensatory hypertrophy of the nasal mucosa after expansion. We investigated nasal volume after 12 months finding an increase but we did not have a control group for ethical reasons, which could certainly be considered a limit of our study. The contributions of the upper and lower compartments also underwent a slight increase at T1 as compared to the corresponding baseline values, although these changes did not reach the statistical significance and it could be explained by growth that could have taken place in our patients because of the long interval between the two time points (1 year). SpO and AHI showed significant increase in our sample after RME, indicating an improvement in breathing pattern. Timms [4] reported that 82% of patients had fewer upper respiratory infections after expansion and Gray [3] found reduced by half the incidences of colds, respiratory illnesses, allergic rhinitis, and asthma. These studies supported clinically the improving of breathing function after RME. Villa et al. [22], in OSA patients, found after RME significant improvements in AHI, stable 24 months after treatment. OSA children showed particular cranio-facial features [23,24], associated with large adenoids and tonsils [25,26]. OSA have been found to have somatic growth impairment due to abnormal nocturnal growth hormone (GH) secretion; after adenotonsillectomy was found a significant increase in the serum levels of GH mediators and its binding protein with normalization and even catch-up of
somatic growth [25,26]. Even more, seems that the anabolic effects of GH on the masseter and medial pterygoid muscles increase endochondral bone formation in the condylar cartilage and bone apposition in the lower border of the mandible [27]. OSA showed a greater posterior face height growth (ramus growth), stable in 5 years after adenotonsillectomy (OSA children 5 mm, control children 3 mm) [28]. In patients with large adenoids and tonsils (classically, regarded as mouth breathing patients), Peltoma¨ki suggested an influence of the adenotonsillectomy on the craniofacial structure, not only caused by a mechanistic alteration due to the change in the mode of breathing but also by a more complex sequence of epigenetic events [29]. In some cases we could expect similar effects after RME, monitoring it by polysomnography (SpO2 and AHI) to better understand the individual answer. In the present study ES coefficients for AHI and SpO2 were above the threshold of 1.0 (Table 2), in favour of their reliable diagnostic use of the functional activity [12]. These data thus warrants further longitudinal study to better define diagnostic ranges and their accuracy. Results regarding the correlation analyses between the AIR, SpO2 and AHI changes showed no correlation of the examined parameters. To the best of our knowledge this is the first study, which evaluates the correlation between airway volume and functional parameters obtained by polysomnography exam as SpO2 and AHI. All the parameters showed significant increases when considered singularly, but they showed no correlations when compared. This result could be due to the exiguity of the sample, which, nevertheless satisfying good ES and study power, is one of the limits of the present study, then further studies are needed to confirm our findings. 5. Conclusions The main results of the present prospective study showed that increases of total airway volume, SpO2 and AHI were statistically significant but ES coefficients were significant only for SpO2 and AHI for our study sample; no correlation was found among total airway volume, SpO2 and AHI changes between the examined timepoints.
Furthermore the present investigation suggests SpO2 and AHI as reliable diagnostic tools to assess RME in growing subjects in terms of respiratory performance. Lacking of a control group because of the ethical complexity to postpone from treating children with functional crossbite is certainly a limitation of our study, therefore also growth and not only treatment might have played a role in gaining our results. References [1] G.V.I. Brown, The application of orthodontic principles to nasal disease, Iowa State Dent. Soc. Trans. (1902) 67–79. [2] F. Ballanti, R. Lione, T. Baccetti, L. Franchi, P. Cozza, Treatment and posttreatment skeletal effects of rapid maxillary expansion investigated with low-dose computed tomography in growing subjects, Am. J. Orthod. Dentofacial Orthop. 138 (2010) 311–317. [3] L.P. Gray, Results of 310 cases of rapid maxillary expansion selected for medical reasons, J. Laryngol. Otol. 89 (1975) 601–614. [4] D.J. Timms, Rapid maxillary expansion in the treatment of nasal obstruction and respiratory disease, Ear Nose Throat J. 66 (1987) 242–247. [5] R.A. Wertz, Skeletal and dental changes accompanying rapid midpalatal suture opening, Am. J. Orthod. 58 (1970) 41–66. [6] S. Linder-Aronson, G. Aschan, Nasal resistance to breathing and palatal height before and after expansion of the median palatal suture, Odont. Revy 14 (1963) 254–270. [7] H.G. Hershey, B.L. Stewart, D.W. Warren, Changes in nasal airway resistance associated with rapid maxillary expansion, Am. J. Orthod. 69 (1976) 274–284.
A. Caprioglio et al. / International Journal of Pediatric Otorhinolaryngology 78 (2014) 23–27 [8] D.W. Warren, H.G. Hershey, T.A. Turvey, V.A. Hinton, W.M. Hairfield, The nasal airway following maxillary expansion, Am. J. Orthod. Dentofacial Orthop. 91 (1987) 111–116. [9] A. Caprioglio, L. Levrini, L. Nosetti, J. Berini, A. Macchi, A. Tagliabue, et al., Prevalence of malocclusion in preschool and primary school children with habitual snoring and sleep-disordered breathing, Eur. J. Paediatr. Dent. 12 (2011) 267– 271. [10] M. Cozzani, M. Rosa, P. Cozzani, G. Siciliani, Deciduous dentition-anchored rapid maxillary expansion in crossbite and non-crossbite mixed dentition patients: reaction of the permanent first molar, Prog. Orthod. 4 (2003) 15–22. [11] J. Cohen, A power primer, Psychol. Bull. 112 (1992) 155–159. [12] G. Perinetti, L. Contardo, Posturography as a diagnostic aid in dentistry: a systematic review, J. Oral Rehabil. 36 (2009) 922–936. [13] S.D. Springate, The effect of sample size and bias on the reliability of estimates of error: a comparative study of Dahlberg’s formula, Eur. J. Orthod. 34 (2012) 158– 163. [14] G. Perinetti, L. Marsi, A. Castaldo, L. Contardo, Is postural platform suited to study correlations between the masticatory system and body posture?. A study of repeatability and a meta-analysis of reported variations, Prog. Orthod. 13 (2012) 273–280. [15] Y. Zhao, M. Nguyen, E. Gohl, J.K. Mah, G. Sameshima, R. Enciso, Oropharyngeal airway changes after rapid palatal expansion evaluated with cone-beam computed tomography, Am. J. Orthod. Dentofacial Orthop. 137 (2010) S71–S78. [16] S. Go¨rgu¨lu¨, S.M. Gokce, H. Olmez, D. Sagdic, F. Ors, Nasal cavity volume changes after rapid maxillary expansion in adolescents evaluated with 3-dimensional simulation and modeling programs, Am. J. Orthod. Dentofacial Orthop. 140 (2011) 633–640. [17] T. Smith, A. Ghoneima, K. Stewart, S. Liu, G. Eckert, S. Halum, et al., Threedimensional computed tomography analysis of airway volume changes after rapid maxillary expansion, Am. J. Orthod. Dentofacial Orthop. 141 (2012) 618– 626. [18] H. El, J.M. Palomo, Three-dimensional evaluation of upper airway following rapid maxillary expansion, Angle Orthod. (2013) 18.
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[19] M.A. Matsumoto, C.E. Itikawa, F.C. Valera, G. Faria, W.T. Anselmo-Lima, Long-term effects of rapid maxillary expansion on nasal area and nasal airway resistance, Am. J. Rhinol. Allergy 24 (2010) 161–165. [20] G. Matarese, M. Portelli, M. Mazza, A. Militi, R. Nucera, E. Gatto, et al., Evaluation of skin dose in a low dose spiral CT protocol, Eur. J. Paediatr. Dent. 7 (June (2)) (2006) 77–80. [21] G. Cordasco, R. Nucera, R. Fastuca, G. Matarese, S.J. Lindauer, P. Leone, et al., Effects of orthopedic maxillary expansion on nasal cavity size in growing subjects: a low dose computer tomography clinical trial, Int. J. Pediatr. Otorhinolaryngol. 76 (2012) 1547–1551. [22] M.P. Villa, A. Rizzoli, S. Miano, C. Malagola, Efficacy of rapid maxillary expansion in children with obstructive sleep apnea syndrome: 36 months of follow-up, Sleep Breath. 15 (2011) 179–184. [23] A. Caprioglio, M. Zucconi, G. Calori, V. Troiani, Habitual snoring. OSA and craniofacial modification. Orthodontic clinical and diagnostic aspects in a case control study, Minerva Stomatol. 48 (1999) 125–137. [24] M. Zucconi, A. Caprioglio, G. Calori, L. Ferini-Strambi, A. Oldani, C. Castronovo, et al., Craniofacial modifications in children with habitual snoring and obstructive sleep apnoea: a case–control study, Eur. Respir. J. 13 (1999) 411–417. [25] A. Bar, A. Tarasiuk, Y. Segev, M. Phillip, A. Tal, The effect of adenotonsillectomy on serum insulin-like growth factor-I and growth in children with obstructive sleep apnea syndrome, J. Pediatr. 135 (1999) 76–80. [26] P. Nieminen, T. Lo¨ppo¨nen, U. Tolonen, P. Lanning, M. Knip, H. Lo¨ppo¨nen, Growth and biochemical markers of growth in children with snoring and obstructive sleep apnea, Pediatrics 109 (2002) e55. [27] C. Vogl, W.R. Atchley, D.E. Cowley, P. Crenshaw, J.D. Murray, D. Pomp, The epigenetic influence of growth hormone on skeletal development, Growth Dev. Aging 57 (1993) 163–182. [28] L. Zettergren-Wijk, C.M. Forsberg, S. Linder-Aronson, Changes in dentofacial morphology after adeno-/tonsillectomy in young children with obstructive sleep apnoea – a 5-year follow-up study, Eur. J. Orthod. 28 (2006) 319–326. [29] T. Peltoma¨ki, The effect of mode of breathing on craniofacial growth—revisited, Eur. J. Orthod. 29 (2007) 426–429.
Contents lists available at ScienceDirect
International Journal of Pediatric Otorhinolaryngology journal homepage: www.elsevier.com/locate/ijporl
Rapid maxillary expansion in growing patients: Correspondence between 3-dimensional airway changes and polysomnography Alberto Caprioglio a, Matteo Meneghel a, Rosamaria Fastuca a,*, Piero Antonio Zecca a, Riccardo Nucera b, Luana Nosetti c a b c
Department of Orthodontics, University of Insubria, Varese, Italy Department of Orthodontics, University of Messina, Messina, Italy Department of Pediatrics, University of Insubria, Varese, Italy
A R T I C L E I N F O
A B S T R A C T
Article history: Received 1 August 2013 Received in revised form 13 October 2013 Accepted 15 October 2013 Available online 25 October 2013
Objectives: The aim of the present prospective study was to investigate the effects of rapid maxillary expansion on the airway correlating airway volumes computed on cone beam computed tomography and polysomnography evaluation of oxygen saturation and apnea/hypopnea index. Methods: The study group comprised 14 caucasian patients (mean age 7.1 0.6 years) undergone to rapid maxillary expansion with Haas type expander banded on second deciduous upper molars. Cone beam computed tomography scans and polysomnography exams were collected before placing the appliance (T0) and after 12 months (T1). Landmarks localization and airway semiautomatic segmentation on cone beam computed tomography scans allowed airway volume computing and measurements. Results: Increases of total airway volume, oxygen saturation and apnea/hypopnea index were statistically significant. No correlation was found among total airway volume, oxygen saturation and apnea/hypopnea index changes between the examined timepoints. Conclusions: Computing airway volume on cone beam computed tomography allow to measure the amount of air that flows through nasal cavity, nasopharynx and oropharynx while oxygen saturation and apnea/hypopnea index could give information about functional parameters. In the present study all three variables investigated showed statistically significant differences between T0 and T1 but no correlation was found between increases of the different variables tested. ß 2013 Elsevier Ireland Ltd. All rights reserved.
Keywords: Maxillary expansion Polysomnography Mouth breathing Airway
1. Introduction Rapid maxillary expansion (RME) is a common orthodontic treatment to correct transverse maxillary discrepancy. It was suggested that RME might influence nasal morphology [1,2] and breathing pattern [3,4]. Wertz [5] investigated the advantages of RME in improving nasal airflow in patients with nasal stenosis. However, considering the Vshaped opening pattern of the midpalatal suture, he claimed that RME cannot be justified for the sole purpose of increasing nasal permeability unless the obstruction is in the lower anterior portion of the nasal cavity and bilateral maxillary arch-width deficiency. Several studies investigated nasal airway resistance finding reduction of resistances after RME [6,7]. These results were confirmed by Warren et al. [8] who reported 45% increase in nasal cross-sectional areas after expansion.
* Corresponding author at: C/O School of Dentistry, Department of Orthodontics, Via Giuseppe Piatti, 10 Velate, 21100 Varese, Italy. Tel.: +39 3803546218. E-mail address: [email protected] (R. Fastuca). 0165-5876/$ – see front matter ß 2013 Elsevier Ireland Ltd. All rights reserved. http://dx.doi.org/10.1016/j.ijporl.2013.10.011
Airway changes after RME have been studied with different means including acoustic rhinometry, 2d and 3d radiographic technique such as cone beam computed tomography (CBCT). Other diagnostic tool can be employed to investigate the effects of RME on airflow from a more functional point of view. The measurement of the volumes of airway compartments may be biased by several factors such as head and tongue position during CBCT scan acquisition, breathing, swallowing movements, repositioning of the tongue and the mandible after treatment. Moreover threshold-based segmentation of airway may not be standardized although, the method errors were acceptable for the present study. The combination of morphological recording with functional respiratory analyses is therefore recommended. Polysomnography examinations (PSG), often employed in obstructive sleep apnoea (OSA) patients [9], could give further information about breathing pattern, showing quantitative data such as oxygen saturation (SpO2) and apnea/hypopnea index (AHI). The aim of the present prospective study was to investigate the effects of RME on the airway correlating airway volumes computed on CBCT and PSG examinations (SpO2 and AHI).
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A. Caprioglio et al. / International Journal of Pediatric Otorhinolaryngology 78 (2014) 23–27
Table 1 Selection criteria. 1. Age (6–9 years) 2. CVS 1 skeletal maturation 3. Functional unilateral posterior crossbite 4. Early mixed dentition 5. Upper and lower first molars erupted 6. No systemic disease 7. No skeletal asymmetries 8. No previous orthodontic treatment 9. High risk of upper canine impaction
2. Methods Ethical approval for this study was obtained from the local Ethical Committee (no. 5184) and informed consent forms were signed by the parents of all patients. The sample consisted of patients treated at the dental clinic. The selection criteria for the present prospective study are shown in Table 1. The initial study group comprised 21 caucasian patients. 7 patients were considered drop out for low quality of the CBCT scans. The final study sample comprised 14 patients (mean age 7.1 0.6 years), who fully matched inclusion and exclusion criteria. The maxillary expander (Snap Lock Expander 10 mm A1671439, Forestadent, Pforzheim, Germany) used for all subjects was Haas type expander banded to the upper second deciduous molars (Fig. 1) as previously suggested [10]. The maxillary expanders were banded using glass ionomer cement (Multi-Cure Glass Ionomer Cement, Unitek, Monrovia, CA, USA) in accordance with the manufacturer’s instructions. The screw of the palatal expander was initially turned two times (0.45 mm initial transversal activation). Afterwards patients were instructed to turn the screw once per each following day (0.225 mm activation per day). The maxillary expansion was performed until dental overcorrection (2 mm) was achieved or when occlusion relationship evaluated at the first permanent molars was cusp to cusp. At the end of the active expansion period (32 5 days) the screw was locked with light-cure flow composite (Premise Flowable; Kerr Corporation, Orange, CA, USA). The palatal expander was removed 12 months after it was inserted, at the end of the retention period. During this period no other fixed orthodontic appliances were used in any patients. CBCT scans (i-CAT, Imaging Sc. Int., Hatfield, PA, USA) were performed in seated position before inserting the maxillary expander (T0) and at the end of retention (T1), 12 months later when the expander was removed.
Fig. 1. RME on deciduous second molars.
Fig. 2. 3d landmarks and planes. Po: porion right and left; Or: orbitale right and left; PNS: posterior nasal spine; PaF: palatal foramen right and left; OdP: middle point of odontoid process of second cervical vertebra; Epi: top of the epiglottis. Frankfort plane: plane passing through PoR-PoL-OrR-OrL; PNS plane: projection on PNS of plane perpendicular to Frankfort passing through PoR-PoL; odontoid plane: passing through OdP and parallel to Frankfort; epiglottis plane: passing through top of the epiglottis and parallel to Frankfort.
PSG examination (Embletta-EMBLA, Thornton, CO, USA) was performed for all subjects at T0 and T1 to collect SpO2 and AHI. 2.1. Image processing Dicom images were processed in two steps. 2.1.1. Landmarks localization and airway semiautomatic segmentation Dicom images were acquired in Mimics software (version 10.11, Materialise Medical Co, Leuven, Belgium). First a set of reproducible landmarks and planes was defined (Fig. 2). Distance between palatal foramens (PaF) right and left were used to assess total maxillary expansion (Fig. 2). Planes were used to obtain a reproducible position of head and to define airway compartments (Fig. 3). The airway was segmented using thresholding based segmentation manually corrected slice by slice. The upper limit of UPPER AIRWAY was set at the edge between nasal bones and etmoid bone.
Fig. 3. Airway compartments. Upper airway (green) from nares to PNS plane; middle airway (yellow) from PNS plane to OdP plane; lower airway (blue) from OdP plane to epiglottis plane; total airway (AIR) from nares to epiglottis plane. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of the article.)
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Segmented airway and landmarks were then exported respectively in stereolitographic (.stl) and iges (.igs) files.
Table 2 The different recorded parameters at each time point (n = 14). Parameter
2.1.2. Volume computing The airway and landmarks files were imported in Rhinoceros Software (Robert McNeel & Associates, 3670 Woodland Park Ave, N Seattle, WA 98103, USA) where a logarithmic sequence built for this purpose automatically computed planes and volumes. 2.2. Sample size calculation and method error analysis A sample size of at least 10 subjects per group was necessary to detect an effect size (ES) coefficient [11] of 1.0 for each recorded parameter between the time points, with an alpha set at 0.05 and a power of 0.8. The ES coefficient is the ratio of the difference between the recordings of the two groups (T0 and T1), divided by the within-subject standard deviation (SD). An effect size of at least 0.8 is regarded to as a large effect [11], while a value of at least 1.0 is considered to be associated with good diagnostic potential [12]. With the aim of quantifying the full method error of the recordings for both of these palatal parameters, the method of moments (MME) variance estimator was used [13]. Therefore, the mean error and 95% confidence intervals (CIs) between the repeated recordings were calculated using the MME variance estimator, and were expressed as percentages [14]. The MME variance estimator has the advantages of not being affected by any unknown bias, i.e. systematic errors, between pairs of measurements [13]. 2.3. Data analysis The SPSS software, version 13.0 (SPSS1 Inc., Chicago, IL, USA) and Comprehensive Meta-Analysis, version 2 (BiostatTM, Englewood, NJ, USA) were used to perform the statistical analyses. Parametrical methods were used after having tested the existence of the assumptions though the Shapiro–Wilk test and Levene test for the normality of the distributions and equality of the variances between the time points, respectively. A paired sample t-test was employed to assess the significance of the difference of each parameter between the time points. Within each time point, the contribution of each airway compartment (upper, middle and lower) to the total volume was also calculated as percentage. The significance of the difference of each compartment contribution between the time point was also assessed through a paired sample t-test. Moreover, the ES coefficients for each recorded parameter along the 95% CIs, were calculated between the time points, as previously described [11]. In particular, the paired nature of the data was taken into account and, whenever negative, absolute values have been reported. Finally, a Pearson rho correlation coefficient was employed to evaluate the strength of the relationship between the intra-subject changes (scores at T1 scores at T0) in PF, AIR, SpO2 and AHI. A p value less than 0.05 was used in the rejection of the null hypothesis.
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PF (mm3) AIR (mm3) SpO2 (%) AHI (events)
Time point
ES (95% CI)
T0
T1
26.6 3.0 16 513.5 4554.8 89.8 1.1 5.7 1.2
29.1 3.2*** 21 754.8 8233.7* 95.5 1.6*** 1.4 0.6***
0.77 0.72 4.05 4.43
(0.48–1.06)*** (0.06–1.38)* (1.43–6.68)** (1.62–7.25)**
Data are shown as mean SD. PF, inter-PaF distance; AIR, total airway; SpO2, oxygen saturation; AHI, apnea/hypopnea index; ES, effect size; CI, confidence interval. Levels of significance: *p < 0.05; **p < 0.01; ***p < 0.001
Table 3 The volumes (in mm3) of each airway compartment at each time point (n = 14). Compartment
Time point T0
T1
Upper Middle Lower
7152.8 3074.0 5975.0 2423.7 3385.8 1450.7
9723.3 4329.4* 7067.5 3200.6 4964.1 2506.6
ES (95% CI)
0.62 (0.10–1.15)* 0.36 ( 0.30–1.02) 0.71 ( 0.00–1.43)
Data are shown as mean SD. ES, effect size; CI, confidence interval. Level of significance: *p < 0.05.
ranging from 0.72 to 4.43 for the total AIR volume and AHI, respectively. However, only for the SpO2 and AHI, the full 95% CI of the ES coefficients were above the threshold of 1.0. Regarding the individual airway compartment volumes (Table 3), only for the upper part a statistically significant increase after treatment was seen (p < 0.05), while for the middle and lower part volumes, the values did not change significantly over time. Similarly, only the ES coefficient for the upper airway compartment volume was significantly greater than zero even though lower than the threshold of 1.0 (0.62). The results on the contribution of each compartment to the total airway volume are showed in Fig. 4. The upper and lower compartments showed the greatest and lowest contributions, respectively. The contributions of the upper and lower compartments also underwent a slight increase at T1 as compared to the corresponding baseline values, although these changes did not reach the statistical significance. Results regarding the correlation analyses between the PF, AIR, SpO2 and AHI changes parameters are shown in Table 4. In particular, none of these correlations reached the statistical significance with Pearson’s r values ranging from 0.487 to 0.282 for PF and SpO2 and AHI changes, respectively.
3. Results Method errors as mean (95% CI) ranged from 0.3 (0.1–0.5) to 179.6 (84.2–298.9) for the inter-PaF distance (PF) and total airway (AIR), respectively. Descriptive statistics for each recorded parameter are shown in Table 2. The PF, AIR, SpO2 and AHI (Table 2) recorded at T1 were significantly greater than the corresponding baseline values (p < 0.05, at least). The ES coefficients retrieved for all these parameters were statistically significantly greater than zero and
Fig. 4. The percentage contribution of upper, middle and lower compartments to total airway volume at each time point (n = 14). Within each compartment, the differences between the time points are not statistically significant.
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Table 4 Correlation matrix between AIR, SPO and AHI changes (n = 14). Parameter PF AIR SpO2 AHI
PF 1 0.213 0.487 0.282
AIR 1 0.367 0.227
SPO
1 0.051
AHI
1
All the rho correlation coefficients are not statistically significant.
4. Discussion In the present study changes in airway volume, SpO2 and AHI in patients undergone RME were investigated. All three variables investigated showed statistically significant differences between T0 and T1 and the ES coefficients were significant for SpO2 and AHI both. PF variations between the two time points (Table 2) indicated the amount of expansion measured at the bone level (palatal foramens) which allowed to measure the efficiency of RME treatment. Computing airway volume on CBCT scans allow to measure the amount of air that flows through nasal cavity, nasopharynx and oropharynx while SpO2 and AHI could give information about functional parameters. Several studies [15–18] computed airway volume after RME dividing airway in segments in order to better understand changes at different levels. In the present study nasal cavity, middle and lower airway were examined and also the whole volume which comprises the three areas. Based on our results among the three airway compartments only nasal cavity had significant increase after RME. These findings agree with other studies [16,17], also when compared with a control group [18]. In relation to the pharyngeal airway volume, Zhao et al. [15] is the only one who compared the results to a control group and found no significant changes between treated and controls after RME. Matsumoto et al. [19] investigated long-term effects of RME on nasal cavity using acoustic rhinometry, computed rhinomanometry and posteroanterior cephalometric radiography demonstrating an increase in nasal osseous width with less significant increases in nasal area and nasal resistance; in agreement with other studies, he suggested that the effects of RME could be more evident at the bony level [20,21] than at the mucosal level and this might be due to compensatory hypertrophy of the nasal mucosa after expansion. We investigated nasal volume after 12 months finding an increase but we did not have a control group for ethical reasons, which could certainly be considered a limit of our study. The contributions of the upper and lower compartments also underwent a slight increase at T1 as compared to the corresponding baseline values, although these changes did not reach the statistical significance and it could be explained by growth that could have taken place in our patients because of the long interval between the two time points (1 year). SpO and AHI showed significant increase in our sample after RME, indicating an improvement in breathing pattern. Timms [4] reported that 82% of patients had fewer upper respiratory infections after expansion and Gray [3] found reduced by half the incidences of colds, respiratory illnesses, allergic rhinitis, and asthma. These studies supported clinically the improving of breathing function after RME. Villa et al. [22], in OSA patients, found after RME significant improvements in AHI, stable 24 months after treatment. OSA children showed particular cranio-facial features [23,24], associated with large adenoids and tonsils [25,26]. OSA have been found to have somatic growth impairment due to abnormal nocturnal growth hormone (GH) secretion; after adenotonsillectomy was found a significant increase in the serum levels of GH mediators and its binding protein with normalization and even catch-up of
somatic growth [25,26]. Even more, seems that the anabolic effects of GH on the masseter and medial pterygoid muscles increase endochondral bone formation in the condylar cartilage and bone apposition in the lower border of the mandible [27]. OSA showed a greater posterior face height growth (ramus growth), stable in 5 years after adenotonsillectomy (OSA children 5 mm, control children 3 mm) [28]. In patients with large adenoids and tonsils (classically, regarded as mouth breathing patients), Peltoma¨ki suggested an influence of the adenotonsillectomy on the craniofacial structure, not only caused by a mechanistic alteration due to the change in the mode of breathing but also by a more complex sequence of epigenetic events [29]. In some cases we could expect similar effects after RME, monitoring it by polysomnography (SpO2 and AHI) to better understand the individual answer. In the present study ES coefficients for AHI and SpO2 were above the threshold of 1.0 (Table 2), in favour of their reliable diagnostic use of the functional activity [12]. These data thus warrants further longitudinal study to better define diagnostic ranges and their accuracy. Results regarding the correlation analyses between the AIR, SpO2 and AHI changes showed no correlation of the examined parameters. To the best of our knowledge this is the first study, which evaluates the correlation between airway volume and functional parameters obtained by polysomnography exam as SpO2 and AHI. All the parameters showed significant increases when considered singularly, but they showed no correlations when compared. This result could be due to the exiguity of the sample, which, nevertheless satisfying good ES and study power, is one of the limits of the present study, then further studies are needed to confirm our findings. 5. Conclusions The main results of the present prospective study showed that increases of total airway volume, SpO2 and AHI were statistically significant but ES coefficients were significant only for SpO2 and AHI for our study sample; no correlation was found among total airway volume, SpO2 and AHI changes between the examined timepoints.
Furthermore the present investigation suggests SpO2 and AHI as reliable diagnostic tools to assess RME in growing subjects in terms of respiratory performance. Lacking of a control group because of the ethical complexity to postpone from treating children with functional crossbite is certainly a limitation of our study, therefore also growth and not only treatment might have played a role in gaining our results. References [1] G.V.I. Brown, The application of orthodontic principles to nasal disease, Iowa State Dent. Soc. Trans. (1902) 67–79. [2] F. Ballanti, R. Lione, T. Baccetti, L. Franchi, P. Cozza, Treatment and posttreatment skeletal effects of rapid maxillary expansion investigated with low-dose computed tomography in growing subjects, Am. J. Orthod. Dentofacial Orthop. 138 (2010) 311–317. [3] L.P. Gray, Results of 310 cases of rapid maxillary expansion selected for medical reasons, J. Laryngol. Otol. 89 (1975) 601–614. [4] D.J. Timms, Rapid maxillary expansion in the treatment of nasal obstruction and respiratory disease, Ear Nose Throat J. 66 (1987) 242–247. [5] R.A. Wertz, Skeletal and dental changes accompanying rapid midpalatal suture opening, Am. J. Orthod. 58 (1970) 41–66. [6] S. Linder-Aronson, G. Aschan, Nasal resistance to breathing and palatal height before and after expansion of the median palatal suture, Odont. Revy 14 (1963) 254–270. [7] H.G. Hershey, B.L. Stewart, D.W. Warren, Changes in nasal airway resistance associated with rapid maxillary expansion, Am. J. Orthod. 69 (1976) 274–284.
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