The Laryngoscope C 2014 The American Laryngological, V
Rhinological and Otological Society, Inc.
Three-Dimensional Evaluation of Nasopharyngeal Airways of Unilateral Cleft Lip and Palate Patients Luiz Andre Pimenta, DDS, MS, PhD; Gabriella Lopes de Rezende Barbosa, DDS, MS; Henrique Pretti, DDS, MS, PhD; Omri Emodi, DMD; John van Aalst, MD, FACS; Paul Emile Rossouw, DDS, PhD; Donald Alton Tyndall, DDS, MS, PhD; Amelia Fischer Drake, MD, FACS Objectives/Hypothesis: The aim of this study was to compare the volume of nasopharyngeal airways of patients with unilateral cleft lip and palate (UCLP) with a control (noncleft) group of subjects. Study Design: Retrospective case-control study. Methods: The sample consisted of 45 subjects, 30 with UCLP who underwent cone beam computed tomography (CBCT) exams as part of their workups for alveolar bone graft and 15 noncleft subjects seeking orthodontic care who obtained CBCT for diagnostic purposes. The three-dimensional volumes of nasal (NV) and oropharyngeal (PV) airways of these subjects were assessed separately using Mimics software by one well-calibrated evaluator. The images were rendered, and the volumes were measured in cm3. Results: The mean PV of the UCLP subjects was 6.7 cm3 and the mean NV was 10.3 cm3. The control group presented with a mean PV of 8.1 cm3 and a mean NV of 11.6 cm3. Student t test showed no statistically significant difference for PV (P 5 0.10) or NV (P 5 0.23) when comparing cleft and noncleft subjects. Conclusion: Evaluation of the nasopharyngeal airways revealed that the NV and PV airways showed no difference between the cleft and noncleft subjects. It is interesting to postulate that the reported nasal abnormalities of the cleft patients do not produce a significant measurable effect on the overall volume, at least as shown in our study sample. In addition, the nasopharyngeal airways of patients are not larger than those of age-matched controls, at least at the ages that were sampled, after cleft palate repair. Key Words: Cone beam computed tomography, nasopharyngeal airways, unilateral cleft lip and palate patients. Level of Evidence: 3b. Laryngoscope, 00:000–000, 2014
INTRODUCTION
DOI: 10.1002/lary.24895
resistance to nasal breathing, and hinder nasal airflow.1,2 Moreover, constrictions and altered dimensions in the oropharyngeal airway are also reported in CLP patients.3 Several consequences of these obstructions may occur, such as alterations of the respiration mode, abnormal facial form, malocclusions, and disturbances in velopharyngeal function.4 Reports of initial symptoms of sleep-disordered breathing highlight the relation of the smaller upper airway of CLP patients and the development of obstructive sleep apnea. Signs such as the elevated incidence of mouth breathing, snoring, and hypopnea during sleep have been described.3,5 The development of the oral, nasal, and pharyngeal structures also has a direct influence on the production of speech, which may cause hypernasal or hyponasal speech.2,6 Previous studies evaluated the airways of CLP patients using different methods.7–9 Morphometric evaluations on cephalometric images have been used; linear measurements based on landmarks are defined in order to obtain dimensions of pharyngeal airways. However, with the advent of different imaging techniques such as cone beam computed tomography (CBCT), threedimensional (3D) evaluations are now present in dental practice, providing a more realistic assessment of airway volume and reducing the chances of distortions. In this
Laryngoscope 00: Month 2014
Pimenta et al.: 3D Airway Evaluation of Patients With Cleft
Subjects with cleft lip and palate (CLP) deformities frequently present with nasal airway deformities, leading to inadequate function and appearance of the nose.1 Frequently encountered abnormalities such as narrowing of the nasal airways due to septal deflections, as well as mucosal hypertrophy of the turbinates, tend to reduce the dimensions of the nasal cavity, increase
From the Department of Dental Ecology (L.A.P.); the Department of Orthodontics (P.E.R.); and the Department of Diagnostic Sciences (D.A.T.), School of Dentistry, University of North Carolina at Chapel Hill; the Division of Plastic and Reconstructive Surgery (J.V.A.); and the Department of Otolaryngology/Head and Neck Surgery (A.F.D.), School of Medicine, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina, U.S.A.; the Departament of Oral Diagnosis, Division of Oral Radiology, Piracicaba Dental School, University of Campinas (G.L.D.R.B.), Piracicaba, S~ ao Paulo; the Department of Orthodontics, School of Dentistry, Federal University of Minas Gerais (H.P.), Belo Horizonte, Minas Gerais, Brazil; the Rambam Health Care Campus (O.E.), Haifa, Israel. Editor’s Note: This Manuscript was accepted for publication July 29, 2014. The authors have no funding, financial relationships, or conflicts of interest to disclose. Send correspondence to Luiz Andr e Pimenta, School of Dentistry, Craniofacial Center, University of North Carolina at Chapel Hill, 001 Brauer Hall, Manning Dr. & Columbia St, Chapel Hill, 27516-7450. E-mail: [email protected]
1
TABLE I. Comparison Between Demographic Data of the Groups Evaluated. Control (n 5 15)
Cleft (n 5 30)
861 7
9.1 6 1.06 7
Maximum
12
12
Gender n (%) Male
9 (60%)
19 (63.3%)
6 (40%)
13 (36.6%)
Age (years) Mean 6 SD Minimum
Female SD 5 standard deviation.
sense, 3D assessment of the airway can be performed without the inherent superimposition or magnification of 2D techniques as conventional lateral images. Furthermore, it has been demonstrated that the information obtained by the CBCT image is superior to that obtained by 2D techniques with regard to a decision for CLP treatment such as in cases of mesiodens—and even for a better understanding of tooth disposition in the arch for more precise surgical planning.10 Although the nasopharyngeal alterations of patients with clefts have been the subject of study of many different investigators, there is a paucity of studies using 3D exams to investigate the airway and its volume, especially in a young population. Therefore, the present study aimed to compare the nasopharyngeal airways of patients with unilateral cleft lip and palate (UCLP) with a control (noncleft) group of patients seeking orthodontic treatment ranging in age from 7 to 12 years old.
MATERIALS AND METHODS The present study included 30 CBCT images of subjects with UCLP (19 male/13 female) and 15 images from control subjects without clefts under orthodontic treatment (9 male/6 female) ranging from 7 to 12 years old (Table I). The inclusion criterion of the affected group was the presence of unilateral cleft. Patients with the presence of any syndrome, symptoms due to upper airway infections, and pharyngeal pathologies such as tonsillitis were excluded from the study. Subjects that had ever undergone palatal expansion at any time were also excluded. The institutional review board at the University of North Carolina/Chapel Hill (UNC/CH) (IRB#11-1560) approved the project, and the principles outlined in the Declaration of Helsinki were followed. The UCLP patients were referred to the radiology clinic for a CBCT exam for preoperative planning of reconstructive surgery with alveolar bone grafting. The images from control subjects were obtained during routine radiographic documentation prior to orthodontic treatment at the School of Dentistry– UNC orthodontic clinic. None of the referrals were related to the study. All CBCT images were acquired in the oral radiology clinic at UNC/CH using a CS9300 unit (Carestream Health, Rochester, NY) operating at 60 to 90 kVp; 2 to 15 mA; 0.5-mm slice thickness; 17 3 13 5-cm field of view; and 0,3 voxel size. All CBCT scans were acquired without sedation of the subjects. The obtained data were analyzed using Mimics software version 16.0 (Materialise Medical, Leuven, Belgium) by a wellcalibrated and trained evaluator. The nasal airway volume (NV)
Laryngoscope 00: Month 2014
2
and pharyngeal airway volume (PV) were assessed separately, excluding the sinus areas. The threshold was defined manually in an attempt to include the airway spaces and to remove any visible extraneous scatter, artifacts, and background. The volumetric region of interest (VOI) was cropped and narrowed to comprise only the structure that would be segmented. The PV was defined as the volume of the pharynx between the palatal plane and the parallel plane that intersects the most anteroinferior point of the second cervical vertebra, extending posteriorly to the wall of the pharynx (Fig. 1). For this PV volume, the superior and inferior limits were slightly modified from the ones used by Ogawa et al.11 The NV was characterized as the nasal airway without sinuses, with an inferior limit demarcated as the superior boundary of the PV airway (Fig. 1). The NV volume was rendered as a whole structure, including the nasopharynx and turbinates (Figs. 2 and 3).12 After the threshold selection and definition of the boundaries, a combination of manual slice editing and 3D editing was used to obtain refined surfaces of the segmentation of the airway. The resulting set of masks of the VOI was rendered into a shaded surface mesh in the same software; and according to the manufacturer’s recommendations, each segmented volume (cm3) was calculated (Fig. 3). The statistical analysis was performed using Stata software version 10.0 (StataCorp, TX). Student t test was used to determine the differences between the volumes of the cleft and control (noncleft) groups; P values < 0.05 were considered statistically significant.
RESULTS The sample of the present study consisted of a total of 45 CBCT images, including 15 control subjects and 30 unilateral cleft subjects. The volumes of nasal and pharyngeal airways are shown in Table II. The mean PV of the patients with cleft was 6,7 cm3; whereas the control group was 8,1 cm3. In relation to the mean value of NV, the UCLP group presented with a mean of 10,3 cm3 and the control group with a mean of
Fig. 1. Definition of the orientation planes for characterization of the nasal (red contour) and oropharyngeal (blue contour) airways.
Pimenta et al.: 3D Airway Evaluation of Patients With Cleft
Fig. 2. Multiplanar reconstruction from core beam computed tomography images of a patient with cleft demonstrating the nasal (red contour) and oropharyngeal (blue contour) airways.
11,6 cm3. Although the reported volumes appear to differ, the student t test was performed to evaluate differences between the groups and no statistically significant differences were observed, neither in the PV (P 5 0.10) nor in the NV (P 5 0.23).
DISCUSSION Originally, diagnostic measurement of the nasal cavity and airway changes was performed by acoustic rhinometry, a well-established and noninvasive technique suitable for the assessment of all patients, including ones with a cleft.13 However, with the introduction of 3D imaging modalities, different approaches are now possible. According to Yamashina et al.,14 CBCT images provide accurate measurement of the air space surrounded by soft tissues, being a close representation of the real volume. Based on this, the present study performed 3D evaluations in CBCT images to calculate the
volume of the nasal and pharyngeal airway of nonsyndromic patients with cleft, which was compared to that of age-matched controls. CBCT was chosen due to its significant reduction of the effective dose of radiation of up to 12.3 times when compared to the multislice CT system,15 avoiding exposure of the patient to unnecessary higher doses as in previous studies, especially younger patients.4 The introduction of CBCT led to a more accessible 3D evaluation of the patient, and as a consequence, a large number and variety of software is emerging for different clinical purposes. Regarding the segmentation of the airway, the programs may have manual and/or automatic segmentation; and even if several programs allow automatic segmentation, it does not mean that the same method is used by all of them. In our study, Mimics software was chosen due to its accuracy and possibility of a detailed individualization of the VOI after the selection of the density values in the threshold. Additionally, as stated by Weissheimer et al., the software is simple to work with and allows quick and easy airway segmentation.16 It is worth highlighting that most programs miss regions with narrow spaces, and some others do not allow for the exclusion of the sinuses because their density is the same as the region of interest, resulting in an erroneous inclusion as part of the airway segmentation. When Mimics software is used, the possibility of editing the VOI, even in 2D slices, avoids these types of errors, leading to a more accurate volumetric measurement of airway only.
TABLE II. Mean and Standard Deviation of Nasal and Pharyngeal Airways (Cm3).
Fig. 3. Three-dimensional segmentation of the nasal (red) and oropharyngeal (blue) airways superimposed to the core beam computed tomography sagittal slice.
Laryngoscope 00: Month 2014
Nasal Airway
Pharyngeal Airway
Control n 5 15
11,6 (2,5)
8,1 (3,3)
Cleft n 5 30
10,3 (3,8)
6,7 (2,2)
No statistical significant differences observed.
Pimenta et al.: 3D Airway Evaluation of Patients With Cleft
3
Our results demonstrated no significant differences between the NV of patients with unilateral clefts compared to the control group, which differs from previous studies that reported smaller nasal volumes in the cleft group.4 This may be due to the fact that different landmarks based on cephalometric images were established, and the delimited nasal volume does not cover the entire nasal cavity, missing the anterior part. Further studies are needed to compare the NV of the cleft side with the normal side in CBCT images, as assessed by Mani et al. using acoustic rhinometry, who reported smaller values for NV in the affected side.1 In relation to the PV, there were no differences between the cleft and noncleft control groups, in agreement with Aras et al. and Cheung and Oberoi, who similarly found that the pharyngeal airway is not compromised in individuals with cleft.4,17 Contrarily, Yoshihara et al. reported reduced pharyngeal airway spaces in the cleft group when compared to the control.3 This similarity between the observed groups in our study might have been due to the comparable dimensions among a juvenile sample, which does not occur when adolescents were evaluated.3 Age-related changes in the dimensions of the nasopharyngeal airway are still unclear,3 as well as the influence of alveolar bone graft that was likely done in older age groups. It can be presumed that these differences between individuals with and without cleft increase with growth, or even represent a compensatory phenomenon in the patients with clefts. It can be postulated that there is an increase in the airway volume of patients with clefts, based on the findings of Wermker et al., who described a reduced antero–posterior dimension of nasopharyngeal complex in favor of a more accentuated vertical development in patients with cleft.18 Differences among the studies regarding the airway volume of patients can be affected by the delimitation of the VOI, selection of landmarks, and even the software used. In this sense, a cautious evaluation of the airway using a program that allows for automatic segmentation and posterior manual edition is recommended. Further studies are necessary to better understand the relation and morphology of surrounding structures with the nasopharyngeal airway of patients with cleft.
CONCLUSION Evaluation of the nasopharyngeal airways showed that the NV and PV airways showed no difference
Laryngoscope 00: Month 2014
4
between the cleft and noncleft subjects. It is interesting to postulate that the reported septal and nasal abnormalities of the cleft patients do not have a significant effect on the overall volume, at least as shown in our study sample.
BIBLIOGRAPHY 1. Mani M, Moren S, Thorvardsson O, Jakobsson O, Skoog V, Holmstrom M. EDITOR’S CHOICE: objective assessment of the nasal airway in unilateral cleft lip and palate—a long-term study. Cleft Palate Craniofac J 2010;47:217–224. 2. Trindade IE, Bertier CE, Sampaio-Teixeira AC. Objective assessment of internal nasal dimensions and speech resonance in individuals with repaired unilateral cleft lip and palate after rhinoseptoplasty. J Craniofac Surg 2009;20:308–314. 3. Yoshihara M, Terajima M, Yanagita N, Hyakutake H, Kanomi R, Kitahara T, Takahashi I. Three-dimensional analysis of the pharyngeal airway morphology in growing Japanese girls with and without cleft lip and palate. Am J Orthod Dentofacial Orthop 2012;141(suppl 4):S92–S101. 4. Aras I, Olmez S, Dogan S. Comparative evaluation of nasopharyngeal airways of unilateral cleft lip and palate patients using three-dimensional and two-dimensional methods. Cleft Palate Craniofac J 2012;49:e75– e81. 5. Rose E, Staats R, Thissen U, Otten JE, Schmelzeisen R, Jonas I. Sleeprelated obstructive disordered breathing in cleft palate patients after palatoplasty. Plast Reconstr Surg 2002;110:392–396. 6. Kummer AW. Speech therapy for errors secondary to cleft palate and velopharyngeal dysfunction. Semin Speech Lang 2011;32:191–198. 7. Imamura N, Ono T, Hiyama S, Ishiwata Y, Kuroda T. Comparison of the sizes of adenoidal tissues and upper airways of subjects with and without cleft lip and palate. Am J Orthod Dentofacial Orthop 2002;122:189– 194. 8. Oosterkamp BCM, Remmelink HJ, Pruim GJ, Hoekema A, Dijkstra PU. Craniofacial, craniocervical, and pharyngeal morphology in bilateral cleft lip and palate and obstructive sleep apnea patients. Cleft Palate Craniofac J 2007;44:1–7. 9. Martin O, Muelas L, Vinas MJ. Nasopharyngeal cephalometric study of ideal occlusions. Am J Orthod Dentofacial Orthop 2006;130:436.e1–e9. 10. Wortche R, Hassfeld S, Lux CJ, et al. Clinical application of cone beam digital volume tomography in children with cleft lip and palate. Dentomaxillofac Radiol 2006;35:88–94. 11. Ogawa T, Enciso R, Shintaku WH, Clark GT. Evaluation of cross-section airway configuration of obstructive sleep apnea. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2007;103:102–108. 12. El H, Palomo JM. Airway volume for different dentofacial skeletal patterns. Am J Orthod Dentofacial Orthop 2011;139:e511–e521. 13. Cakmak O, Celik H, Cankurtaran M, Ozluoglu LN. Effects of anatomical variations of the nasal cavity on acoustic rhinometry measurements: a model study. Am J Rhinol 2005;19:262–268. 14. Yamashina A, Tanimoto K, Sutthiprapaporn P, Hayakawa y. The reliability of computed tomography (CT) values and dimensional measurements of the oropharyngeal region using cone beam CT: comparison with multidetector CT. Dentomax-Illofac Radiol 2008;37:245–251. 15. Ludlow JB, Ivanovic M. Comparative dosimetry of dental CBCT devices and 64-slice CT for oral and maxillofacial radiology. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2008;106:106–114. 16. Weissheimer A, Menezes LM, Sameshima GT, Enciso R, Pham J, Grauer D. Imaging software accuracy for 3-dimensional analysis of the upper airway. Am J Orthod Dentofacial Orthop 2012;142:801–813. 17. Cheung T, Oberoi S. Three dimensional assessment of the pharyngeal airway in individuals with non-syndromic cleft lip and palate. PLoS One 2012;7:e43405. 18. Wermker K, Jung S, Joos U, Kleinheinz J. Nasopharyngeal development in patients with cleft lip and palate: a retrospective case-control study. Int J Otolaryngol 2012;2012:458507.
Pimenta et al.: 3D Airway Evaluation of Patients With Cleft
Rhinological and Otological Society, Inc.
Three-Dimensional Evaluation of Nasopharyngeal Airways of Unilateral Cleft Lip and Palate Patients Luiz Andre Pimenta, DDS, MS, PhD; Gabriella Lopes de Rezende Barbosa, DDS, MS; Henrique Pretti, DDS, MS, PhD; Omri Emodi, DMD; John van Aalst, MD, FACS; Paul Emile Rossouw, DDS, PhD; Donald Alton Tyndall, DDS, MS, PhD; Amelia Fischer Drake, MD, FACS Objectives/Hypothesis: The aim of this study was to compare the volume of nasopharyngeal airways of patients with unilateral cleft lip and palate (UCLP) with a control (noncleft) group of subjects. Study Design: Retrospective case-control study. Methods: The sample consisted of 45 subjects, 30 with UCLP who underwent cone beam computed tomography (CBCT) exams as part of their workups for alveolar bone graft and 15 noncleft subjects seeking orthodontic care who obtained CBCT for diagnostic purposes. The three-dimensional volumes of nasal (NV) and oropharyngeal (PV) airways of these subjects were assessed separately using Mimics software by one well-calibrated evaluator. The images were rendered, and the volumes were measured in cm3. Results: The mean PV of the UCLP subjects was 6.7 cm3 and the mean NV was 10.3 cm3. The control group presented with a mean PV of 8.1 cm3 and a mean NV of 11.6 cm3. Student t test showed no statistically significant difference for PV (P 5 0.10) or NV (P 5 0.23) when comparing cleft and noncleft subjects. Conclusion: Evaluation of the nasopharyngeal airways revealed that the NV and PV airways showed no difference between the cleft and noncleft subjects. It is interesting to postulate that the reported nasal abnormalities of the cleft patients do not produce a significant measurable effect on the overall volume, at least as shown in our study sample. In addition, the nasopharyngeal airways of patients are not larger than those of age-matched controls, at least at the ages that were sampled, after cleft palate repair. Key Words: Cone beam computed tomography, nasopharyngeal airways, unilateral cleft lip and palate patients. Level of Evidence: 3b. Laryngoscope, 00:000–000, 2014
INTRODUCTION
DOI: 10.1002/lary.24895
resistance to nasal breathing, and hinder nasal airflow.1,2 Moreover, constrictions and altered dimensions in the oropharyngeal airway are also reported in CLP patients.3 Several consequences of these obstructions may occur, such as alterations of the respiration mode, abnormal facial form, malocclusions, and disturbances in velopharyngeal function.4 Reports of initial symptoms of sleep-disordered breathing highlight the relation of the smaller upper airway of CLP patients and the development of obstructive sleep apnea. Signs such as the elevated incidence of mouth breathing, snoring, and hypopnea during sleep have been described.3,5 The development of the oral, nasal, and pharyngeal structures also has a direct influence on the production of speech, which may cause hypernasal or hyponasal speech.2,6 Previous studies evaluated the airways of CLP patients using different methods.7–9 Morphometric evaluations on cephalometric images have been used; linear measurements based on landmarks are defined in order to obtain dimensions of pharyngeal airways. However, with the advent of different imaging techniques such as cone beam computed tomography (CBCT), threedimensional (3D) evaluations are now present in dental practice, providing a more realistic assessment of airway volume and reducing the chances of distortions. In this
Laryngoscope 00: Month 2014
Pimenta et al.: 3D Airway Evaluation of Patients With Cleft
Subjects with cleft lip and palate (CLP) deformities frequently present with nasal airway deformities, leading to inadequate function and appearance of the nose.1 Frequently encountered abnormalities such as narrowing of the nasal airways due to septal deflections, as well as mucosal hypertrophy of the turbinates, tend to reduce the dimensions of the nasal cavity, increase
From the Department of Dental Ecology (L.A.P.); the Department of Orthodontics (P.E.R.); and the Department of Diagnostic Sciences (D.A.T.), School of Dentistry, University of North Carolina at Chapel Hill; the Division of Plastic and Reconstructive Surgery (J.V.A.); and the Department of Otolaryngology/Head and Neck Surgery (A.F.D.), School of Medicine, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina, U.S.A.; the Departament of Oral Diagnosis, Division of Oral Radiology, Piracicaba Dental School, University of Campinas (G.L.D.R.B.), Piracicaba, S~ ao Paulo; the Department of Orthodontics, School of Dentistry, Federal University of Minas Gerais (H.P.), Belo Horizonte, Minas Gerais, Brazil; the Rambam Health Care Campus (O.E.), Haifa, Israel. Editor’s Note: This Manuscript was accepted for publication July 29, 2014. The authors have no funding, financial relationships, or conflicts of interest to disclose. Send correspondence to Luiz Andr e Pimenta, School of Dentistry, Craniofacial Center, University of North Carolina at Chapel Hill, 001 Brauer Hall, Manning Dr. & Columbia St, Chapel Hill, 27516-7450. E-mail: [email protected]
1
TABLE I. Comparison Between Demographic Data of the Groups Evaluated. Control (n 5 15)
Cleft (n 5 30)
861 7
9.1 6 1.06 7
Maximum
12
12
Gender n (%) Male
9 (60%)
19 (63.3%)
6 (40%)
13 (36.6%)
Age (years) Mean 6 SD Minimum
Female SD 5 standard deviation.
sense, 3D assessment of the airway can be performed without the inherent superimposition or magnification of 2D techniques as conventional lateral images. Furthermore, it has been demonstrated that the information obtained by the CBCT image is superior to that obtained by 2D techniques with regard to a decision for CLP treatment such as in cases of mesiodens—and even for a better understanding of tooth disposition in the arch for more precise surgical planning.10 Although the nasopharyngeal alterations of patients with clefts have been the subject of study of many different investigators, there is a paucity of studies using 3D exams to investigate the airway and its volume, especially in a young population. Therefore, the present study aimed to compare the nasopharyngeal airways of patients with unilateral cleft lip and palate (UCLP) with a control (noncleft) group of patients seeking orthodontic treatment ranging in age from 7 to 12 years old.
MATERIALS AND METHODS The present study included 30 CBCT images of subjects with UCLP (19 male/13 female) and 15 images from control subjects without clefts under orthodontic treatment (9 male/6 female) ranging from 7 to 12 years old (Table I). The inclusion criterion of the affected group was the presence of unilateral cleft. Patients with the presence of any syndrome, symptoms due to upper airway infections, and pharyngeal pathologies such as tonsillitis were excluded from the study. Subjects that had ever undergone palatal expansion at any time were also excluded. The institutional review board at the University of North Carolina/Chapel Hill (UNC/CH) (IRB#11-1560) approved the project, and the principles outlined in the Declaration of Helsinki were followed. The UCLP patients were referred to the radiology clinic for a CBCT exam for preoperative planning of reconstructive surgery with alveolar bone grafting. The images from control subjects were obtained during routine radiographic documentation prior to orthodontic treatment at the School of Dentistry– UNC orthodontic clinic. None of the referrals were related to the study. All CBCT images were acquired in the oral radiology clinic at UNC/CH using a CS9300 unit (Carestream Health, Rochester, NY) operating at 60 to 90 kVp; 2 to 15 mA; 0.5-mm slice thickness; 17 3 13 5-cm field of view; and 0,3 voxel size. All CBCT scans were acquired without sedation of the subjects. The obtained data were analyzed using Mimics software version 16.0 (Materialise Medical, Leuven, Belgium) by a wellcalibrated and trained evaluator. The nasal airway volume (NV)
Laryngoscope 00: Month 2014
2
and pharyngeal airway volume (PV) were assessed separately, excluding the sinus areas. The threshold was defined manually in an attempt to include the airway spaces and to remove any visible extraneous scatter, artifacts, and background. The volumetric region of interest (VOI) was cropped and narrowed to comprise only the structure that would be segmented. The PV was defined as the volume of the pharynx between the palatal plane and the parallel plane that intersects the most anteroinferior point of the second cervical vertebra, extending posteriorly to the wall of the pharynx (Fig. 1). For this PV volume, the superior and inferior limits were slightly modified from the ones used by Ogawa et al.11 The NV was characterized as the nasal airway without sinuses, with an inferior limit demarcated as the superior boundary of the PV airway (Fig. 1). The NV volume was rendered as a whole structure, including the nasopharynx and turbinates (Figs. 2 and 3).12 After the threshold selection and definition of the boundaries, a combination of manual slice editing and 3D editing was used to obtain refined surfaces of the segmentation of the airway. The resulting set of masks of the VOI was rendered into a shaded surface mesh in the same software; and according to the manufacturer’s recommendations, each segmented volume (cm3) was calculated (Fig. 3). The statistical analysis was performed using Stata software version 10.0 (StataCorp, TX). Student t test was used to determine the differences between the volumes of the cleft and control (noncleft) groups; P values < 0.05 were considered statistically significant.
RESULTS The sample of the present study consisted of a total of 45 CBCT images, including 15 control subjects and 30 unilateral cleft subjects. The volumes of nasal and pharyngeal airways are shown in Table II. The mean PV of the patients with cleft was 6,7 cm3; whereas the control group was 8,1 cm3. In relation to the mean value of NV, the UCLP group presented with a mean of 10,3 cm3 and the control group with a mean of
Fig. 1. Definition of the orientation planes for characterization of the nasal (red contour) and oropharyngeal (blue contour) airways.
Pimenta et al.: 3D Airway Evaluation of Patients With Cleft
Fig. 2. Multiplanar reconstruction from core beam computed tomography images of a patient with cleft demonstrating the nasal (red contour) and oropharyngeal (blue contour) airways.
11,6 cm3. Although the reported volumes appear to differ, the student t test was performed to evaluate differences between the groups and no statistically significant differences were observed, neither in the PV (P 5 0.10) nor in the NV (P 5 0.23).
DISCUSSION Originally, diagnostic measurement of the nasal cavity and airway changes was performed by acoustic rhinometry, a well-established and noninvasive technique suitable for the assessment of all patients, including ones with a cleft.13 However, with the introduction of 3D imaging modalities, different approaches are now possible. According to Yamashina et al.,14 CBCT images provide accurate measurement of the air space surrounded by soft tissues, being a close representation of the real volume. Based on this, the present study performed 3D evaluations in CBCT images to calculate the
volume of the nasal and pharyngeal airway of nonsyndromic patients with cleft, which was compared to that of age-matched controls. CBCT was chosen due to its significant reduction of the effective dose of radiation of up to 12.3 times when compared to the multislice CT system,15 avoiding exposure of the patient to unnecessary higher doses as in previous studies, especially younger patients.4 The introduction of CBCT led to a more accessible 3D evaluation of the patient, and as a consequence, a large number and variety of software is emerging for different clinical purposes. Regarding the segmentation of the airway, the programs may have manual and/or automatic segmentation; and even if several programs allow automatic segmentation, it does not mean that the same method is used by all of them. In our study, Mimics software was chosen due to its accuracy and possibility of a detailed individualization of the VOI after the selection of the density values in the threshold. Additionally, as stated by Weissheimer et al., the software is simple to work with and allows quick and easy airway segmentation.16 It is worth highlighting that most programs miss regions with narrow spaces, and some others do not allow for the exclusion of the sinuses because their density is the same as the region of interest, resulting in an erroneous inclusion as part of the airway segmentation. When Mimics software is used, the possibility of editing the VOI, even in 2D slices, avoids these types of errors, leading to a more accurate volumetric measurement of airway only.
TABLE II. Mean and Standard Deviation of Nasal and Pharyngeal Airways (Cm3).
Fig. 3. Three-dimensional segmentation of the nasal (red) and oropharyngeal (blue) airways superimposed to the core beam computed tomography sagittal slice.
Laryngoscope 00: Month 2014
Nasal Airway
Pharyngeal Airway
Control n 5 15
11,6 (2,5)
8,1 (3,3)
Cleft n 5 30
10,3 (3,8)
6,7 (2,2)
No statistical significant differences observed.
Pimenta et al.: 3D Airway Evaluation of Patients With Cleft
3
Our results demonstrated no significant differences between the NV of patients with unilateral clefts compared to the control group, which differs from previous studies that reported smaller nasal volumes in the cleft group.4 This may be due to the fact that different landmarks based on cephalometric images were established, and the delimited nasal volume does not cover the entire nasal cavity, missing the anterior part. Further studies are needed to compare the NV of the cleft side with the normal side in CBCT images, as assessed by Mani et al. using acoustic rhinometry, who reported smaller values for NV in the affected side.1 In relation to the PV, there were no differences between the cleft and noncleft control groups, in agreement with Aras et al. and Cheung and Oberoi, who similarly found that the pharyngeal airway is not compromised in individuals with cleft.4,17 Contrarily, Yoshihara et al. reported reduced pharyngeal airway spaces in the cleft group when compared to the control.3 This similarity between the observed groups in our study might have been due to the comparable dimensions among a juvenile sample, which does not occur when adolescents were evaluated.3 Age-related changes in the dimensions of the nasopharyngeal airway are still unclear,3 as well as the influence of alveolar bone graft that was likely done in older age groups. It can be presumed that these differences between individuals with and without cleft increase with growth, or even represent a compensatory phenomenon in the patients with clefts. It can be postulated that there is an increase in the airway volume of patients with clefts, based on the findings of Wermker et al., who described a reduced antero–posterior dimension of nasopharyngeal complex in favor of a more accentuated vertical development in patients with cleft.18 Differences among the studies regarding the airway volume of patients can be affected by the delimitation of the VOI, selection of landmarks, and even the software used. In this sense, a cautious evaluation of the airway using a program that allows for automatic segmentation and posterior manual edition is recommended. Further studies are necessary to better understand the relation and morphology of surrounding structures with the nasopharyngeal airway of patients with cleft.
CONCLUSION Evaluation of the nasopharyngeal airways showed that the NV and PV airways showed no difference
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between the cleft and noncleft subjects. It is interesting to postulate that the reported septal and nasal abnormalities of the cleft patients do not have a significant effect on the overall volume, at least as shown in our study sample.
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Pimenta et al.: 3D Airway Evaluation of Patients With Cleft
