The Cleft Palate Craniofacial Journal 52(3) pp. 346 351 May 2015 Ó Copyright 2015 American Cleft Palate Craniofacial Association ORIGINAL ARTICLE Three-Dimensional Evaluation of Pharyngeal Airway in Complete Unilateral Cleft Individuals and Normally Growing Individuals Using Cone Beam Computed Tomography Rohan Diwakar, B.D.S., M.D.S., Maninder Singh Sidhu, B.D.S., M.D.S., DIBO, Saurabh Jain, Seema Grover, B.D.S., M.D.S., Mona Prabhakar, B.D.S., M.D.S. Aims: The aim of the present study was to evaluate pharyngeal airway in cleft individuals and normally growing individuals using cone beam computed tomography. Materials and Methods: Cone beam computed tomography scans of 22 individuals were obtained from the Department of Orthodontics and divided in two groups. Group 1 includes 11 cases with complete unilateral cleft lip and palate (mean age, 12 years) and group 2 includes 11 noncleft cases (mean age, 14 years). The oropharyngeal, nasopharyngeal, and oronasal pharyngeal airway was evaluated between the two groups. Results: In the cleft group, the volume of the nasopharyngeal airway was found to be 3.66 cm 3 ; of the oropharyngeal airway, 9.28 cm 3 ; and of the oronasal pharyngeal airway, 12.67 cm 3. The volume of the nasopharyngeal airway was found to be significantly reduced in the cleft palate group when compared with the noncleft group. Conclusion: The nasopharyngeal airway was found to be significantly smaller among the children with cleft palate than among those in the control group. KEY WORDS: cone beam computed tomography, pharyngeal airway, unilateral cleft Nonsyndromic orofacial cleft lip and palate presents multiple problems, including dental problems such as malocclusion, multiple impacted teeth, missing teeth, and deficient alveolar bone support. Problems such as nasality, difficulty in speech and hearing, and nasal deformities such as septal deviation, nasal atresia, and alar constriction are frequently associated with it (Drettner, 1960; Hairfield et al., 1988; Hairfield and Warren, 1989). These nasal deformities tend to decrease the size of the nasal airway, which in turn results in obligatory mouth breathing that can further affect development of facial and dental structures (Hairfield et al., 1988). Increased incidence of mouth breathing in patients with cleft lip and palate was shown in 1988 by Hairfield et al., who reported that 68% of individuals with cleft lip and palate have mouth breathing tendency. Similarly, Rose et al. (2002) found that children with cleft lip and palate had a significantly elevated incidence of mouth breathing, snoring, and sleep hypopnea. All Dr. Diwakar is Senior Lecturer, Dr. Sidhu is Professor and Head, Dr. Jain is postgraduate student, Dr. Grover is Professor, and Dr. Prabhakar is Professor, Department of Orthodontics, SGT Dental College, Gurgaon, India. Submitted November 2013; Revised February 2014; Accepted March 2014. Address correspondence to: Dr. Maninder Singh Sidhu, Professor and Head, Department of Orthodontics, SGT Dental College, Gurgaon, India. E-mail drmssidhu@hotmail.com. DOI: 10.1597/13-292 these nasal abnormalities cause a reduction in the size of the nasal cavity and reduce airway function (Warren, 1992). Earlier, two-dimensional (2D) evaluation of the airway was done using various radiological methods such as lateral cephalograms and functional methods such as rhinomanometry and plethysmography (Smahel et al., 1991; Drake et al., 1993; Imamura et al., 2002; Fukushiro and Trindade, 2005). Diagnosis of the airway using lateral cephalograms or 2D imaging techniques has the limitation of a view in only one plane. Lateral cephalogram-generated images are used to view in the sagittal plane only, and these images overlap structures, making it difficult to identify landmarks, and involve image enlargement (Waitzman et al., 1992). Hence, to get accurate information regarding the airway, axial images are required, which are not possible on lateral cephalograms (Isono et al., 1993). It is possible to visualize the airway in axial slices with the advent of various three-dimensional (3D) imaging techniques such as computed tomography (CT) or cone beam computed tomography (CBCT). However, use of a CT scan generates the potential risk of higher radiation exposure in the maxillofacial region. The radiation dose reported for maxillofacial imaging by conventional CT is approximately 2000 msv (Dula et al., 1996; Scaf et al., 1997; Schulze et al., 2004). Published data in the past indicate that the effective dose for CBCT devices ranges from 29 to 477 msv (Ludlow et al., 2006). For the present study, the radiation exposure from the CBCT scans was 346
Diwakar et al., AIRWAY EVALUATION WITH CBCT 347 FIGURE 1 The rendering window, which allows simultaneous viewing of the X, Y, and Z sections (axial, coronal, sagittal) and custom sections of a 3D view. 130 msv. Thus, the use of CBCT has many advantages over conventional radiographic technique and other 3D imaging techniques such as CT scans. Cone beam computed tomography generates images in all the three planes: coronal, sagittal, and axial (Waitzman et al., 1992). In addition, CBCT have been helpful in getting information regarding the position of the impacted teeth, prognosis for the bone grafting, and future pathways for erupting canines. The aim of the present study was to conduct a 3D evaluation of the pharyngeal airway volume in children TABLE 1 Boundaries of the Nasopharyngeal, Oropharyngeal, and Oronasal Pharyngeal Airway with complete unilateral cleft lip and palate (UCLP) and compare with normally growing children using CBCT. MATERIAL AND METHODS The sample size consisted of 22 individuals divided into two groups. Group 1 comprised 11 cases with complete UCLP (12 to 14 years) and group 2 constituted 11 normally growing individuals (12 to 14 years) who served as the controls. The inclusion criteria for the cleft lip and palate group was (1) presence of complete UCLP, (2) nonsyndromic UCLP, and (3) no history of previous orthodontic treatment. The inclusion criteria for the control group included (1) no prior orthodontic treatment Airway Landmarks* Nasopharyngeal airway Oropharyngeal airway Oronasal airway The inferior limit of the nasopharyngeal airway was taken as a line joining the ANS-PNS and extending to the posterior pharyngeal wall, which is also the superior boundary of the oropharyngeal airway. The anterior border of nasopharyngeal airway was selected as a line perpendicular to the palatal plane drawn from the PNS. The superior limit of oropharyngeal airway was taken as a line joining the ANS-PNS and extending to the posterior pharyngeal wall. The inferior limit was taken as a line parallel to the ANS-PNS plane passing through the antero-inferior border of the second cervical vertebrae. The anterior border of the total pharyngeal airway was selected as a line perpendicular to the palatal plane drawn from the PNS, which was also the anterior boundary of the nasopharyngeal airway. The inferior limit was taken as a line parallel to the ANS-PNS plane passing through the antero-inferior border of the second cervical vertebrae, which was also the inferior border of the oropharyngeal airway. * ANS ¼ anterior nasal spine; PNS ¼ posterior nasal spine. FIGURE 2 Boundaries of the nasopharyngeal, oropharyngeal, and oronasal pharyngeal airway.
348 Cleft Palate Craniofacial Journal, May 2015, Vol. 52 No. 3 FIGURE 3 Comparison of the nasopharyngeal airway between cleft group and the controls. and (2) no history of adenoidectomy or tonsillectomy. For the control group, the CBCT scans were selected from the data bank of the department. These CBCT scans were mainly done for patients (1) with impacted teeth, (2) with a single missing tooth prior to implant placement, or (3) in whom it was important to assess the bone level in the maxilla or the mandible. Each volumetric data set was acquired with a 20-second scan time with a 13 3 16-cm field of view (diameter and height, respectively) and at a resolution of 0.25 mm voxels. All the images were collected at 120 kvp and 5 ma, based on the manufacturer s specifications. The acquired digital axial images were transferred directly to a personal computer in the Digital Imaging and Communications in Medicine format. Volume-rendering software (Invivo5.1, Anatomage, San Jose, CA) was used to create the 3D images. The slice data sets were reoriented as follows: (1) the axial plane was parallel to the Frankfort horizontal plane, which was defined by the right and left poria and the center of the right and left orbitales; (2) the frontal plane was perpendicular to the Frankfort horizontal plane, passing through the right and left poria; and (3) the sagittal plane was perpendicular to the Frankfort horizontal and frontal planes, passing through the center of the right and left orbitales (Fig. 1). The definition of the planes used for pharyngeal measurements are described in Table 1 and illustrated in Figure 2. Measuring Nasopharyngeal Airway Volume The boundaries of the nasopharyngeal airway were slightly modified from those taken by Aboudara et al. (2009). The inferior limit of the nasopharyngeal airway was taken as a line joining the anterior nasal spine and the posterior nasal spine (ANS-PNS) and extending to the posterior pharyngeal wall, which is also the superior boundary of the oropharyngeal airway. The anterior border of the nasopharyngeal airway was selected as a line perpendicular to the palatal plane drawn from the PNS. Figure 3 presents a comparison of the nasopharyngeal airway of the cleft group with the controls. Measuring Oropharyngeal Airway The superior limit of the oropharyngeal airway was taken as a line joining the ANS-PNS and extending to the posterior pharyngeal wall. The inferior limit was taken as a line parallel to the ANS-PNS plane, passing through the antero-inferior border of the second cervical vertebrae. For the oropharyngeal airway, the superior and inferior limits are similar to those taken by El and Palomo (2011). Figure 4 presents a comparison of the oropharyngeal airway of the cleft group with that of the controls. Measuring Oronasal Pharyngeal Airway Volume The anterior border of the oronasal pharyngeal airway was selected as a line perpendicular to the palatal plane drawn from PNS, which was also the anterior boundary of the nasopharyngeal airway. The inferior limit was taken as a line parallel to the ANS- PNS plane and passing through the antero-inferior border of the second cervical vertebrae, which was also the inferior border of the oropharyngeal airway. Figure 5 presents a comparison of the oronasal FIGURE 4 Comparison of the oropharyngeal airway between cleft group and the controls.
Diwakar et al., AIRWAY EVALUATION WITH CBCT 349 FIGURE 5 Comparison of the oronasal pharyngeal airway between cleft group and the controls. pharyngeal airway volume of the cleft group with the controls. RESULTS All the patients in the cleft group had unilateral cleft of the lip, hard palate, and soft palate. All statistical analyses were performed with SPSS software (version 15.0J for Windows; SPSS, Inc., Chicago, IL). Table 2 shows the individual measurements of pharyngeal airway volume of complete unilateral cleft patients. The mean value and standard deviation between the groups were calculated by using paired t tests. Table 3 and Figure 6 show the comparison of the oropharyngeal, nasopharyngeal, and oronasal pharyngeal airway volume between the cleft palate and noncleft individuals using a paired t test. The nasopharyngeal airway was found to be statistically different in the two groups, with the value being less in the cleft palate group compared with the controls. Oropharyngeal and oronasal airway volume was not found to be statistically different between the two groups. DISCUSSION The main aim of the study was to develop a reliable 3D analysis to measure certain characteristics of the pharyngeal airway in children with complete UCLP and compare the findings with a noncleft control group. The present study was conducted to evaluate the oropharyngeal, nasopharyngeal, and oronasal pharyngeal airway volume in three dimensions using CBCT. The study reveals that the volume of the nasopharyngeal airway was found to be 3.66 cm 3 in cleft group and 6.40 cm 3 in noncleft group. The volume of the oropharyngeal airway was found to be 9.28 cm 3 in cleft group and 11.38 cm 3 in the noncleft group. The oronasal pharyngeal airway was found to be 12.67 cm 3 in the cleft group and 17.71 cm 3 in the noncleft group. The volume of the nasopharyngeal airway was found to be significantly reduced in the cleft palate group as compared with the noncleft group. The findings were in agreement with the findings of Wermker et al. (2012), who reported a decrease in the anterior nasopharyngeal height when lateral cephalograms of individuals with complete cleft lip and palate were measured and compared retrospectively with the cephalograms of healthy individuals. Imamura et al. (2002) reported a significantly smaller upper airway in their cleft lip and palate (CLP) juvenile group than in the control juvenile group, and the airway in the CLP adult group was also significantly smaller than that in the control adult group. One possible reason for this could be that the size of the adenoidal tissue was found to be greater in the adult and juvenile cleft group when compared with the adult and juvenile controls. Aras et al. (2012) compared the nasopharyngeal airway three dimensionally in UCLP individuals with the controls and concluded that the nasal volume was lower in the cleft individuals when compared with the healthy individuals. Given that the CLP TABLE 2 Individual Measurement of the Nasopharyngeal, Oropharyngeal, and Total Pharyngeal Airway in Children With Complete Unilateral Cleft Lip and Palate Subject No. Name Age (y)/sex Type of Cleft Nasopharyngeal Airway, cm 3 Oropharyngeal Airway, cm 3 Oronasal Airway, cm 3 1 RO 9/M Complete unilateral cleft lip and palate 5 12.1 17.1 2 DE 10/M Complete unilateral cleft lip and palate 3 5.3 8.3 3 MA 13/M Complete unilateral cleft lip and palate 3.2 10.7 13.9 4 RA 12/M Complete unilateral cleft lip and palate 2.5 8.4 10.9 5 RA 15/M Complete unilateral cleft lip and palate 5.8 18 23.8 6 SH 15/M Complete unilateral cleft lip and palate 3.8 7.5 11.3 7 DH 13/M Complete unilateral cleft lip and palate 3.1 10.4 13.5 8 SU 13/F Complete unilateral cleft lip and palate 3.5 7.8 11.3 9 KI 9/F Complete unilateral cleft lip and palate 4 4 8 10 MH 11/M Complete unilateral cleft lip and palate 3 14.4 17.4 11 LA 11/M Complete unilateral cleft lip and palate 3.4 3.5 6.9
350 Cleft Palate Craniofacial Journal, May 2015, Vol. 52 No. 3 TABLE 3 Comparison of the Oropharyngeal, Nasopharyngeal, and Oronasal Pharyngeal Airway Volume in Cleft and Noncleft Patients Airway Group 1 (Cleft Group) n ¼ 11 Group 2 (Noncleft Group) n ¼ 11 Mean 6 SD Mean 6 SD t Value P Value FIGURE 6 Comparison of the oropharyngeal, nasopharyngeal, and oronasal pharyngeal airway volume in cleft children and controls. patients mostly exhibit a retrusive and vertically deficient maxilla, there is greater likelihood for reduction in the volume of the bony nasopharyngeal airway. Because the landmarks used for measuring the nasopharyngeal airway in the study were bony and the size of the adenoids was not taken into consideration for determining the volume of the nasopharyngeal airway passage, we conclude that this defect could be due to the reduced bony framework in the cleft individuals as compared with the controls. However, adenoid enlargement may be an important factor in causing reduced nasopharyngeal airway patency in cleft individuals owing to the recurrent respiratory infections they experience. It would definitely be recommended that future studies are carried out to determine whether the reduced volume of the nasopharynx is due to the enlarged soft tissue, a smaller bony framework, or both. The oropharyngeal and oronasal pharyngeal airway volumes were not found to be significantly different between the cleft palate group and the noncleft group. The available literature (Solow et al., 1984; Muto et al., 2006) has amply shown that the sagittal position of the mandible is significantly correlated with the volume of the oropharynx. Because cleft individuals have a normally growing mandible, this could account for the insignificant difference of oropharyngeal airway between the two groups in our study. The findings of the present study were in agreement with the findings of Yoshihara et al. (2012), who also found that the oropharyngeal and the oronasal pharyngeal airway volumes did not differ significantly when the cleft palate juvenile group was compared with the control juvenile group. Cheung and Oberoi (2012) found that the pharyngeal airway volume was not significantly different between the cleft group and the noncleft group. Rather, a longer airway length was seen in the cleft group when compared with the noncleft group. One possible reason for this could be that the volume was measured after maxillary expansion, which could have resulted in an increase in the oronasal volume. To date, most studies evaluating the pharyngeal airway have been 2D. Use of lateral cephalograms has been extensively used in the past to measure the pharyngeal airway.incontrast,cbctcouldbeusedtoaccurately Nasopharyngeal airway (cm 3 ) 3.66 6 0.97 6.40 6 2.28 3.665.002** Oropharyngeal airway (cm 3 ) 9.28 6 4.44 11.38 6 5.92 0.941.358 Oronasal airway (cm 3 ) 12.67 6 5.33 17.71 6 6.95 1.907.071 **P,.01. assess the pharyngeal airway three dimensionally in all the three planes (i.e., sagittal, coronal, and axial). The results obtained in our study may not be representative of the airway volumes of a large cleft population because our sample size was small. However, we took care to include clefts of a similar nature, and this sample was matched with controls of similar age to alleviate the effect of growth on pharyngeal airway volume. CONCLUSION Cone beam computed tomography allows accurate measurement of the pharyngeal airway volume in 3D. Using the 3D technique, we could evaluate that the volume of the nasopharyngeal airway was found to be significantly reduced in the cleft palate groupwhencomparedwiththe noncleft group. The oropharyngeal and oronasal pharyngeal airway volume did not differ between the two groups. Further studies are required to validate these results with a larger sample size. REFERENCES Aboudara C, Neilsen I, Huang JC, Maki K, Miller AJ, Hatcher D. Comparison of airway space with conventional lateral headfilms and 3-dimensional reconstruction from cone beam computed tomography. Am J Orthod Dentofacial Orthop. 2009;135:468 479. Aras I, Olmez S, Dogan S. Comparative evaluation of nasopharyngeal airways of unilateral cleft lip and palate patients using threedimensional and two-dimensional methods. Cleft Palate Craniofac J. 2012:49:75 81. 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. Drake AF, Davis JU, Warren DW. Nasal airway size in cleft and noncleft children. Laryngoscope. 1993;103:915 917. Drettner B. The nasal airway and hearing in patients with cleft palate. Acta Otolaryngol. 1960;57:131 142. Dula K, Mini R, van der Stelt PF, Lambrecht JT, Schneeberger P, Buser D. Hypothetical mortality risk associated with spiral computed tomography of the maxilla and mandible. Eur J Oral Sci. 1996;104:503 510. El H, Palomo JM. Airway volume for different dentofacial skeletal patterns. Am J Orthod Dentofacial Orthop. 2011;139:e511 e521. Fukushiro AP, Trindade IE. Nasal airway dimensions of adults with cleft lip and palate: differences among cleft types. Cleft Palate Craniofac J. 2005;42:396 402.
Diwakar et al., AIRWAY EVALUATION WITH CBCT 351 Hairfield WM, Warren DW. Dimensions of the cleft nasal airway in adults: a comparison with subjects without cleft. Cleft Palate J. 1989;26:9 13. Hairfield WM, Warren DW, Seaton DL. Prevalence of mouth breathing in cleft lip and palate. Cleft Palate J. 1988;25:135 138. 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. Isono S, Morrison DL, Launois SH, Feroah TR, Whitelaw WA, Remmers JE. Static mechanics of the velopharynx of patients with obstructive sleep apnea. J Appl Physiol. 1993;75:148 154. Ludlow JB, Davies-Ludlow LE, Brooks SL, Howerton WB. Dosimetry of 3 CBCT devices for oral and maxillofacial radiology: CB Mercuray, NewTom 3G and i-cat. Dentomaxillofac Radiol. 2006;35:219 226. Muto T, Yamazaki A, Takeda S. Relationship between the pharyngeal airway space and craniofacial morphology, taking into account head posture. Int J Oral Maxillofac Surg. 2006;35:132 136. 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. Scaf G, Lurie AG, Mosier KM, Kantor ML, Ramsby GR, Freedman ML. Dosimetry and cost of imaging osseointegrated implants with film-based and computed tomography. Oral Surg Oral Med Oral Pathol Oral Radiol Endod. 1997;83:41 48. Schulze D, Heiland M, Thurmann H, Adam G. Radiation exposure during midfacial imaging using 4- and 16-slice computed tomography, cone beam computed tomography systems and conventional radiography. Dentomaxillofac Radiol. 2004;33:83 86. Smahel Z, Kasalova P, Skvarilova B. Morphometric nasopharyngeal characteristics in facial clefts. J Craniofac Genet Dev Biol. 1991;11:24 32. Solow B, Siersbzek-Nielsen S, Greve E. Airway adequacy, head posture, and craniofacial morphology. Am J Orthod. 1984;86:214 223. Waitzman AA, Posnick JC, Armstrong DC, Pron GE. Craniofacial skeletal measurements based on computed tomography: part I. Accuracy and reproducibility. Cleft Palate Craniofac J. 1992;29:112 117. Warren DW, Davis J, Drake A, Dalston E. The nasal airway in BCLP: a pattern of abnormal development? J Dent Res. 1992a;71:746. 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;2012:458 507. 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:S92 S101.