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Pediatric Imaging |
1 From the Department of Radiology (L.F.D., K.A.C.), Division of Pulmonary Medicine (V.S., B.A.C., R.S.A.), and Department of Pediatrics (L.F.D., V.S., B.A.C., S.A.P., R.S.A.), Children’s Hospital Medical Center, 3333 Burnet Ave, Cincinnati, OH 45229-3039. Received March 14, 2002; revision requested May 2; final revision received October 3; accepted October 4. Address correspondence to L.F.D. (e-mail: lane.donnelly@cchmc.org).
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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MATERIALS AND METHODS: Fast gradient-echo sequences were performed in the sagittal midline by using a 1.5-T unit to create cine MR images. Cine MR images obtained during sleep in 16 young patients with OSA were compared with those obtained in 16 young patients with no airway symptoms of airway disease. The nasopharynx, oropharynx, and hypopharynx were characterized in terms of airway motion as static patent (SP), dynamic patent, intermittent collapsed (IC), or static collapsed (SC); and the maximal diameter and greatest change in diameter (in millimeters) of these airways were calculated. Adenoid tonsil size and mouth position (ie, opened or closed) were determined. Differences in the frequency of MR imaging parameters in the different anatomic regions were evaluated by using Fisher exact, 
2, and sample t tests.
RESULTS: There were statistically significant differences in the following parameters between the two groups: nasopharynx SP (P < .001) and IC (P < .001); hypopharynx SP (P < .001) and IC (P < .001); and mean change in airway diameter of the nasopharynx (P < .001) and hypopharynx (P < .001). The mean adenoid tonsil size in the patients with OSA was larger (P = .006).
CONCLUSION: There are significant differences in the patterns of dynamic airway motion between young patients with and those without OSA.
© RSNA, 2003
Index terms: Magnetic resonance (MR), cine study, 262.121412, 262.121416, 263.121412, 263.121416 • Magnetic resonance (MR), in infants and children, 262.121411, 262.121412, 262.121416, 263.121411, 263.121412, 263.121416 • Nasopharynx, abnormalities, 262.827, 263.827 • Sleep apnea, 262.827, 263.827 • Small airways disease, 262.827, 263.827
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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In much of the literature addressing the potential uses of imaging in the evaluation of patients with obstructive sleep apnea, the emphasis has been on the evaluation of static anatomic measurements (9–13). This evaluation includes cephalometrics, in which specific anatomic landmarks identified on radiographs of the skull and airway are used to calculate static measurements that are used to differentiate asymptomatic populations from populations with anatomic factors indicating risk of obstructive sleep apnea (9–12).Cross-sectional imaging examinations such as MR imaging have likewise been used to measure soft-tissue and bone anatomic landmarks for evaluations of differences between asymptomatic subjects and those with obstructive sleep apnea (13).
To our knowledge, comparisons of the patterns of dynamic airway motion during sleep in children with and without obstructive sleep apnea have not been emphasized. Diagnoses of airway abnormalities in pediatric patients, such as glossoptosis and pharyngeal collapse, are based on the identification of abnormal dynamic motion on images (14–18). The identification of patterns of dynamic airway motion in pediatric patients while they are sleeping may be helpful not only in identifying specific diagnoses but also potentially in predicting which children will and will not benefit from therapies such as tonsillectomy. Cine MR imaging techniques have been reported to be successful in depicting airway motion abnormalities that are related to obstructive sleep apnea in adults (19–23). These examinations yield detailed information on both anatomy and dynamic airway motion (19–23). For research purposes, MR imaging is also optimal because it does not involve the use of ionizing radiation, which is required for computed tomography and fluoroscopy. The purpose of this study was to compare the patterns of dynamic airway motion depicted on cine MR images obtained during sleep between young patients with and those without obstructive sleep apnea.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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The review of data regarding these patients was approved by our institutional review board. Because our study data were obtained by means of retrospective review of existing clinical data on these patients with obstructive sleep apnea, informed consent was waived by our institutional review board.
The 16 subjects in the age-matched control group were recruited from a population of patients who were referred for MR imaging of the brain. All of these subjects required sedation at MR imaging. The mean age of these patients was 8.7 years (age range, 6 months to 19 years). The examination of patients in the control group was approved by our institutional review board, and informed consent was obtained from either the parents or the patient in all cases. We excluded from the control group those patients who might have had airway abnormalities. Patients in whom histories, signs, or symptoms of airway abnormalities (eg, previous airway surgery, tracheotomy, obstructive sleep apnea, snoring) were identified at the presedation work-up were excluded from participation in the study. Those patients who experienced oxygen desaturation or breathed noisily during the sedation also were excluded. Thus, all of the control subjects in this study were asymptomatic in terms of airway disease. These patients were sedated according to the same guidelines used to induce sedation in the obstructive sleep apnea group.
MR Imaging
All of the MR imaging examinations were performed while the subjects were asleep. MR imaging was performed in two study patients who had fallen asleep spontaneously after sleep deprivation; the remaining patients were sedated. All sedations were performed and monitored in accordance with the structured sedation program of our department of radiology (24,25). A sedation nurse, pediatric radiologist, and respiratory therapist who was equipped with positive pressure breathing equipment were present during sedation and MR imaging. Sedation was induced in the patients with either orally administered chloral hydrate (50–100 mg/kg) or intravenously administered pentobarbital (3 mg/kg, with repeat doses up to a total of 7 mg/kg if patient remains awake). The drug chosen for sedation was based on patient age: Chloral hydrate was administered to patients younger than 1 year and pentobarbital to patients older than 1 year. During the entire MR imaging procedure and recovery from sedation (if applicable), respiratory rate, heart rate and rhythm, and blood oxygen saturation were monitored by using transcutaneous pulse oximetry. No sedated patients had complications.
Midline sagittal fast gradient-echo cine, transverse fast gradient-echo cine, transverse fast spin-echo T2-weighted, and sagittal T1-weighted MR images were obtained in each patient once he or she was asleep. These images were obtained with one of two 1.5-T MR imaging units (GE Medical Systems, Milwaukee, Wis). A head-neck vascular coil was used. The patients were imaged while in the supine position with the neck in a neutral position. The airway was imaged from the most superior aspect to the level of the lower cervical trachea.
A fast gradient-echo sequence was used to create the cine MR images. Technical parameters included 8.2/3.6 (repetition time msec/echo time msec), an 80° flip angle, and an 8-mm section thickness. One hundred twenty-eight consecutive cine MR images were obtained at the same midline sagittal location in approximately 2 minutes. These images were obtained in the midline sagittal plane and in the transverse plane at the base of the tongue and displayed in a cine format to create a real-time "movie" of airway motion. The midline plane was determined from the localizer images and the static transverse and sagittal MR images.
In the control group, midline sagittal cine MR images of the airway were obtained after all clinically indicated imaging examinations were completed. The same technical parameters that were used to image the patients with obstructive sleep apnea were used. In no case was additional sedation induced to obtain the cine MR images of the airway. If the patient began to wake up during the investigational (ie, cine) sequence, the acquisition was aborted.
MR Image Evaluation
The midline sagittal cine MR images obtained in the obstructive sleep apnea and control groups were compared. Dynamic motion of the airway was evaluated in three anatomic locations—the nasopharynx, the oropharynx, and the hypopharynx—each of which was categorized as static patent, dynamic patent, intermittent collapsed, or static collapsed. When the anatomic region of the airway was patent and motionless, it was considered to be static patent. When the anatomic region of the airway demonstrated a measurable change in diameter but remained patent during the duration of the cine MR imaging sequence, it was considered to be dynamic patent. When the anatomic region of the airway demonstrated a measurable change in diameter and during imaging was patent at times and completely collapsed at other times, it was considered to be intermittent collapsed. When the anatomic region of the airway was collapsed during the duration of the cine MR imaging sequence, it was considered to be static collapsed.
The maximal anterior-to-posterior diameter (in millimeters) of the airway in each anatomic area was recorded. Measurements were made with electric calibers on a picture archiving and communication system, or PACS, workstation (GE Medical Systems). If there was dynamic motion, the maximal change in diameter (in millimeters) also was recorded. If the diameter was static, the change in diameter was considered to be zero. The mouth position was noted to be open or closed during cine MR imaging. The images were reviewed simultaneously by two authors (L.F.D., K.A.C.), and conclusions were reached by consensus.
For consistency of anatomic measurements, the maximal diameters were measured as follows: The diameter of the nasopharynx was measured at the narrowest point between the adenoid tonsils (or the posterior pharyngeal soft tissues in patients without recurrent adenoid tonsils after adenoidectomy) posteriorly and the posterior aspect of the soft palate anteriorly. The diameter of the oropharynx was measured between the superior surface of the tongue anteriorly and the inferior aspect of the soft palate posteriorly, at the level of the middle portion of the soft palate. The diameter of the hypopharynx was measured at the narrowest point between the posterior aspect of the tongue anteriorly and the posterior wall of the pharynx posteriorly, between the soft palate superiorly and the superior tip of the epiglottis inferiorly. In each case, the maximal diameter of the adenoid tonsils was recorded in a manner similar to that used by Vogler et al (26) and Jaw et al (27). By using the midline image, the diameter of the adenoid tonsil was measured at the maximal convexity of the adenoid tonsil in a line perpendicular to the anterior clival surface. If the adenoid tonsils had been surgically removed and were absent, the diameter was considered to be zero.
For the obstructive sleep apnea group, transverse MR images obtained at the level of the middle portion of the hypopharynx were available. On these images, the transverse left-to-right and transverse anterior-to-posterior airway diameters were recorded. In the cases with dynamic motion, we determined whether there was dynamic motion in just the anterior-to-posterior plane or also in the left-to-right plane. Changes in airway diameters were recorded.
Statistical Analysis
Differences in the frequency of imaging parameters between the obstructive sleep apnea and control groups were evaluated for statistical significance. The frequencies of the nasopharynx, oropharynx, and hypopharynx being static patent, dynamic patent, intermittent collapsed, or static collapsed were analyzed by using the Fisher exact or 2 test. Differences in the mean change in diameter of the nasopharynx, oropharynx, and hypopharynx were evaluated with a two-sample t test. Significant differences in mean adenoid tonsil size and mouth position between the two groups were analyzed by using the two-sample t test and the 2 test, respectively. Statistical significance was defined by P 
.05, except when adjustments were made for multiple comparisons, in which case statistical significance was defined by P .012. Analyses were performed by using a computer software program.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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In the 16 patients with obstructive sleep apnea, the transverse cine MR images obtained at the level of the hypopharynx were evaluated for changes in both the transverse anterior-to-posterior diameter and the transverse left-to-right diameter (Fig 3). Fifteen of these patients demonstrated dynamic airway motion at cine MR imaging: Three of these patients had a dynamically patent airway and 12 an intermittently collapsed airway. One patient had a static collapsed airway. In all 15 patients with dynamic airway motion, motion was detected in the anterior-to-posterior direction. In 14 of the 15 subjects, motion was detected in the left-to-right direction also. On the basis of transverse cine MR image findings, the mean change in anterior-to-posterior diameter was 11.5 mm (range, 2–22 mm). The mean change in left-to-right diameter was 14.7 mm (range, 0–30 mm). Therefore, there was a greater mean change in the left-to-right diameter than in the anterior-to-posterior diameter.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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In some children who have obstructive sleep apnea with underlying causes other than enlarged adenoid and palatine tonsils, evaluation with dynamic sleep fluoroscopy (14–18) or MR imaging (19–23,27,28) has been shown to yield information that affects management decisions (14). Such underlying causes of obstructive sleep apnea include craniofacial anomalies, congenital syndromes (particularly Down syndrome and achondroplasia), mucopolysaccharidosis, and history of airway surgery (14–16). Many of these patients are predisposed to developing airway obstruction at multiple sites (14–16). Polysomnography is helpful in differentiating central from obstructive causes of sleep apnea (5,29). However, it does not yield accurate information about the anatomic level of obstruction or as to whether there are multiple levels of obstruction in children with obstructive sleep apnea. In cases of obstructive sleep apnea in which there is a complicated medical history or persistent breathing abnormality during sleep following a surgical procedure performed to treat sleep apnea, dynamic sleep fluoroscopy with sedation has been shown to be useful, affecting management decisions in up to 50% of cases (14).
Imaging with fluoroscopic or cine MR techniques is particularly suited for diagnosing both anatomic abnormalities such as enlarged adenoid tonsils and dynamic abnormalities of the airway such as glossoptosis and pharyngeal collapse (14–18). Glossoptosis is defined as an abnormal posterior motion of the tongue during sleep (16). It is seen most commonly in children with neuromuscular abnormalities because of an abnormal decrease in muscular tone, macroglossia, or micrognathia (16,30). At imaging, the tongue "falls" posteriorly during sleep, abutting the velum (ie, soft palate) and the posterior wall of the pharynx and obstructing the airway (16,30). Surgical interventions to either reduce the volume of the tongue or reposition the mandible have been described for those cases that are refractory to medical management such as the use of positive pressure airway devices during sleep (31,32).
The identification of different patterns of dynamic airway motion in the young patients with and without obstructive sleep apnea in this study supports the theory that certain patterns of motion, such as those in glossoptosis and pharyngeal collapse, are pathologic. None of the control subjects demonstrated collapse of the hypopharynx; in contrast, 13 of the 16 patients with obstructive sleep apnea demonstrated a collapsed airway in this region. Also, the mean change in diameter of the hypopharyngeal airway was much greater in the patients with obstructive sleep apnea (11.98 mm) than in the age-matched control group (0.81 mm). These findings suggest that while small degrees of motion of the hypopharynx should be considered normal, larger degrees of motion should be considered abnormal.
In this series, the mean size of the adenoid tonsils was statistically larger in the patients with obstructive sleep apnea (13.46 mm) than in those without this abnormality (7.36 mm) (P = .006). We believe that this is particularly interesting because nine of the 16 children with obstructive sleep apnea had undergone adenoidectomy, and six of these nine patients had regrowth of the adenoid tonsils following adenoidectomy. There were no significant differences in mouth position between the obstructive sleep apnea and control groups. With regard to the oropharynx, there was a statistically significant difference in the frequency of intermittent collapse only. This may have been related in part to the relatively small size of the oropharynx between the superior surface of the tongue anteriorly and the inferior aspect of the soft palate posteriorly. Accurately measuring such a small diameter (ie, several millimeters) to determine significant differences is more difficult than measuring larger diameters, such as those of the nasopharynx or hypopharynx.
The reference standard for dynamic imaging of the airway has been dynamic sleep fluoroscopy (14–18). With dynamic sleep fluoroscopy, the airway is visualized only in the lateral view (14–18). One of the advantages of MR imaging, as compared with sleep fluoroscopy, is that, in addition to involving no ionizing radiation, it enables one to view the airway in multiple planes. On the transverse cine MR images obtained in the patients with obstructive sleep apnea in this study, the mean change in airway diameter in the left-to-right plane was greater than that in the anterior-to-posterior plane. This large component of left-to-right motion in the hypopharynx cannot be detected in the lateral projection and thus may be missed at lateral fluoroscopy. Traditional concepts of glossoptosis and pharyngeal collapse as predominantly anterior-to-posterior processes may have to be reconsidered.
Our study had limitations: the small number of children in the obstructive sleep apnea group and the heterogeneous cases of obstructive sleep apnea in this group. Also, the control group may not have completely represented healthy children, because these patients were referred for MR imaging of the brain on the basis of clinical findings. However, efforts were made to ensure that none of these patients had signs or symptoms of sleep apnea or other airway abnormalities. Finally, most of the patients in the apnea and control groups in this study were sedated. Some might argue that sedation may not completely mimic the physiologic state of sleep. The physicians at our institution have been using the results of imaging studies performed with sedation to make clinical decisions concerning children with obstructive sleep apnea for nearly 2 decades. Although this is a point of debate, it is our opinion that although the physiologic state of airway motion in a sedated child may not be identical to that in a naturally sleeping child, it is very similar. The patients in both the obstructive sleep apnea group and the control group were sedated according to identical protocols, and, thus, we believe that the described comparisons between the two groups were legitimate.
In conclusion, there were significant differences in the patterns of dynamic airway motion between the young patients with and those without obstructive sleep apnea.
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FOOTNOTES |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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This article has been cited by other articles:
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  E. S. Katz and C. M. D'Ambrosio Pathophysiology of Pediatric Obstructive Sleep Apnea Proceedings of the ATS, February 15, 2008; 5(2): 253 - 262. [Abstract] [Full Text] [PDF]
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 J. J. Armstrong, M. S. Leigh, D. D. Sampson, J. H. Walsh, D. R. Hillman, and P. R. Eastwood Quantitative Upper Airway Imaging with Anatomic Optical Coherence Tomography Am. J. Respir. Crit. Care Med., January 15, 2006; 173(2): 226 - 233. [Abstract] [Full Text] [PDF]
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 L. F. Donnelly Obstructive Sleep Apnea in Pediatric Patients: Evaluation with Cine MR Sleep Studies Radiology, September 1, 2005; 236(3): 768 - 778. [Abstract] [Full Text] [PDF]
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R. Arens, S. Sin, J. M. McDonough, J. M. Palmer, T. Dominguez, H. Meyer, D. M. Wootton, and A. I. Pack Changes in Upper Airway Size during Tidal Breathing in Children with Obstructive Sleep Apnea Syndrome Am. J. Respir. Crit. Care Med., June 1, 2005; 171(11): 1298 - 1304. [Abstract] [Full Text] [PDF]
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M. B. Abbott, L. F. Donnelly, B. J. Dardzinski, S. A. Poe, B. A. Chini, and R. S. Amin Obstructive Sleep Apnea: MR Imaging Volume Segmentation Analysis Radiology, September 1, 2004; 232(3): 889 - 895. [Abstract] [Full Text] [PDF]
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M. B. Abbott, B. J. Dardzinski, and L. F. Donnelly Using Volume Segmentation of Cine MR Data to Evaluate Dynamic Motion of the Airway in Pediatric Patients Am. J. Roentgenol., September 1, 2003; 181(3): 857 - 859. [Full Text] [PDF]
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