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Defining Normal Upper Airway Motion in Asymptomatic Children during Sleep by Means of Cine MR Techniques¹

¹ From the Departments of Radiology (L.F.D., K.A.C., B.L.K.) and Pediatrics (L.F.D., B.C., B.L.K.), Children’s Hospital Medical Center, 3333 Burnet Ave, Cincinnati, OH 45229-3039 and University of Cincinnati College of Medicine. Received June 11, 2001; revision requested July 10; revision received August 2; accepted September 17. Address correspondence to L.F.D. (e-mail: lane.donnelly@chmcc.org).

	ABSTRACT

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 
PURPOSE: To define normal upper airway motion in asymptomatic children during sleep by means of dynamic cine magnetic resonance (MR) techniques.

MATERIALS AND METHODS: In children referred for MR of the brain who required sedation, a sagittal midline cine MR sequence was performed. Motion of the nasopharynx, oropharynx, and hypopharynx was characterized as static patent, dynamic patent, intermittent collapse, or static collapsed; maximal diameter and greatest change in size were calculated in millimeters. Mouth position (open or closed) was determined. Parameters were compared with age (t test) and mouth position (Fisher exact test).

RESULTS: In the 148 subjects (mean age, 3.4 years), the nasopharynx showed dynamic motion in 53 (36%). The oropharynx was most commonly collapsed in 98 (66%) of the patients. The hypopharynx showed dynamic motion in 72 (49%) of the patients and was never collapsed. Vertical motion was present in 77 (52%) of the patients. The mouth was open in 96 (65%) of the patients. There was a statistically significant correlation between mouth position and dynamic motion in the oropharynx (P = .006) and in the nasopharynx (P < .006) but not in the hypopharynx (P = .655).

CONCLUSION: Dynamic changes in diameter were often seen in the nasopharynx and in the hypopharynx of asymptomatic sleeping children. However, collapse of the hypopharynx was not normally encountered.

Supplemental material: radiology.rsnajnls.org/cgi/content/full/2231011023/DC1.

© RSNA, 2002

Index terms: Children, respiratory system, 20.121419 • Infants, respiratory system, 20.121419 • Neck, MR, 28.121419

	INTRODUCTION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 
The importance of obstructive sleep apnea in the development of many childhood problems is being increasingly recognized. Recent evidence has suggested that obstructive sleep apnea in children can be associated with excessive daytime sleepiness, hyperactivity, attention deficit disorder, poor hearing, physical debilitation, and failure to thrive (1–6). It is estimated that up to 3% of all children, approximately 2 million in the United States alone, are affected by obstructive sleep apnea syndrome (7,8). In cases in which the cause of obstructive sleep apnea is related to phenomena other than the typical tonsil enlargement, dynamic sleep fluoroscopy has been shown to be a useful adjunct to endoscopic evaluation, affecting management decisions in over 50% of cases (9–13). It is particularly useful in the diagnosis of dynamic abnormalities of the airway such as glossoptosis and pharyngeal collapse (9–11). The diagnosis of such dynamic abnormalities is made with fluoroscopic detection of abnormal motion of the soft-tissue structures that make up the walls of the airway (9–11). Although severe cases are obviously abnormal at fluoroscopy, the differentiation between less severe cases and the upper limits of normal respiratory motion of the airway can be problematic. It has been assumed that the airway of a healthy child demonstrates little or no respiratory motion during sleep (9–11). However, the amount of motion that occurs within the normal airway during sleep has not been well established.

Cine magnetic resonance (MR) techniques have been described as being successful in demonstrating the motion abnormalities that cause obstructive sleep apnea in adults (14–17). It would be unethical to sedate healthy children for the purposes of studying normal respiratory motion. Children who are referred for MR of the brain and require sedation during the examination represent a potentially ideal population in which to study motion of the airway. They are already undergoing MR, are asleep, and do not typically have airway abnormalities. For these reasons, we elected to use a cine MR sequence to evaluate airway motion in children who were already sedated for MR studies of the brain. The purpose of this study was to define normal upper airway motion in asymptomatic children during sleep by means of dynamic cine MR techniques.

	MATERIALS AND METHODS

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 
Children who were referred for MR of the brain and who required sedation to perform this examination were asked to participate in the study. In these children, a cine MR sequence of the airway was obtained after all clinically indicated image sequences were completed. In no case was additional sedation given to obtain the cine MR images of the airway. If the patient began to wake up during the investigational sequence, the sequence was aborted. The study was approved by our institutional review board, and informed consent was obtained in all cases.

Because all of the patients were referred for an MR imaging study of the brain, they in a sense do not represent a "normal" population. Efforts were made to exclude those patients who might have abnormalities of the airway from the study. Patients who had histories, signs, or symptoms of airway abnormalities (eg, previous airway surgery, tracheotomy, obstructive sleep apnea, snoring) detected during the presedation work-up were excluded from participation in the study. Patients and parents were asked if the child had a history of snoring, obstructive sleep apnea, previous airway surgery, or other airway diseases. At physical examination, stridor, wheezing, a tracheotomy, or scarring from previous airway surgery were noted. Also, those patients who experienced oxygen desaturation or noisy breathing (snoring) during sedation were excluded. Therefore, all subjects in the study were asymptomatic in terms of airway diseases. No exclusion criteria were based on the clinical indication for the brain MR examination. Patients were referred for MR of the brain for a variety of reasons, including seizure, headache, or follow-up of a brain tumor. The mean age and age range of the subjects enrolled in the study were reflective of those patients who required sedation to complete MR imaging of the brain.

All sedation procedures were performed and monitored in accordance with our departmental structured sedation program (18,19). The sedation nurse obtained a history and performed a physical examination immediately prior to each sedation procedure and was supervised by the pediatric radiologist in doing so. Patients were sedated with either oral chloral hydrate (50–100 mg/kg) or intravenous pentobarbital (3 mg/kg, with repeat dosing if the patient remained awake, for up to a total of 7 mg/kg). Drug choice was based on patient age (guideline: chloral hydrate for patients aged <1 year, pentobarbital for patients aged >1 year). During the entire procedure and each patient’s recovery from sedation, respiratory rate, heart rate and rhythm, and blood oxygen saturation were monitored by means of transcutaneous pulse oximetry. All children breathed spontaneously without any form of assisted ventilation.

The sequence used to create the cine MR images was a fast gradient-echo sequence. Technical parameters included flip angle of 80°, repetition time of 8.2 seconds, echo time of 3.6 seconds (8.2/3.6), and section thickness of 8 mm. One hundred twenty-eight consecutive images at the same midline sagittal location were obtained during an imaging time of approximately 2 minutes. Because each child was in a head coil so that the clinically indicated images of the brain could be obtained, the airway cine images were obtained with the patient in the head coil. In all children, the airway was visualized from the most superior portion of the nasopharynx to the midtrachea. In some smaller infants, the trachea could be visualized to the level of the carina. Images were obtained with one of two 1.5-T MR units (LX; GE Medical Systems, Milwaukee, Wis). The images were displayed in cine format, creating a real-time "movie" of airway motion. The images were evaluated by two reviewers (L.F.D., K.A.C.) simultaneously. Conclusions were reached through consensus.

Dynamic motion of the airway was evaluated in three anatomic locations. These included the nasopharynx, the oropharynx, and the hypopharynx. In each location, motion was categorized as static patent, dynamic patent, intermittently collapsed, or static collapsed. Static patent was defined as when the anatomic region of the airway was patent and motionless. Dynamic patent was defined as when the anatomic region of the airway demonstrated a measurable change in diameter but remained patent during the entire duration of the cine MR sequence. Intermittent collapse was defined as when the anatomic region of the airway demonstrated a measurable change in diameter, was patent at times during imaging, and was completely collapsed at other times. Static collapse was defined as when the anatomic region of the airway was collapsed during the entire duration of the cine MR sequence. For each anatomic area, the maximal diameter (in millimeters) of the airway from anterior to posterior was recorded. If there was dynamic motion, the maximal change in diameter (in millimeters) was also recorded.

For consistency, maximal diameters were measured in the following anatomic locations. The diameter of the nasopharynx was measured at the narrowest point between the adenoid tonsils posteriorly and the posterior aspect of the soft palate anteriorly. The diameter of the oropharynx was measured at the narrowest point between the superior surface of the tongue anteriorly and the inferior aspect of the soft palate posteriorly. 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).

For cases in which the hypopharynx demonstrated dynamic motion (ie, dynamic patent motion or intermittent collapse), the predominant anatomic structure causing dynamic motion was categorized as the tongue, the posterior wall of the pharynx, or both. The mouth position was noted to be open or closed during the cine MR examination. If the patient had a pacifier in place during the study, his or her mouth position was considered to be closed. Vertical motion was noted to be present or absent. Vertical motion was defined as repetitive motion of the pharynx in a superior-to-inferior direction during the respiratory cycle.

All dynamic and static airway parameters were compared with age (t test) and with mouth position (Fisher exact test) for statistically significant trends (P < .05).

	RESULTS

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The number of subjects studied with cine MR was 148. The mean age was 3.4 years, and the age range was 10 days to 19 years. There were 97 boys and 51 girls. The results of the evaluation of static and dynamic motion are summarized in Table 1 and are illustrated in Figures 1–3 and Movies 1–3 (radiology.rsnajnls.org/cgi/content/full/2231011023/DC1). Dynamic motion of the airway was commonly encountered. There was dynamic motion (dynamic patent or intermittent collapse) of the nasopharynx in 53 (36%) of the subjects (Figs 1, 2; Movies 1, 2 [radiology.rsnajnls.org/cgi/content/full/2231011023/DC1]). The hypopharynx showed dynamic motion in 72 (49%) of the subjects but was never collapsed (intermittently or statically). The oropharynx was most commonly collapsed; this occurred in 98 (66%) of the subjects.

View larger version (145K): [in this window] [in a new window] [Download PPT slide]   Figure 1a. Cine MR images (fast gradient echo, 80° flip angle, 8.2/3.6, 8-mm section thickness, 128 consecutive midline sagittal images, 2-minute image time) in a 5-year-old girl with no airway symptoms show dynamic hypopharyngeal and nasopharyngeal motion. (a) Cine MR image obtained at one point during the respiratory cycle shows a patent hypopharynx (arrows) and nasopharynx (white arrowhead). The oropharynx (black arrowheads) is collapsed between the tongue and soft palate. The mouth is closed. (b) Cine MR image obtained at another point during the respiratory cycle shows decreased diameter of the hypopharynx (arrows) and collapse of the nasopharynx (arrowhead) between the soft palate and the adenoids. The oropharynx remains collapsed.

View larger version (146K): [in this window] [in a new window] [Download PPT slide]   Figure 1b. Cine MR images (fast gradient echo, 80° flip angle, 8.2/3.6, 8-mm section thickness, 128 consecutive midline sagittal images, 2-minute image time) in a 5-year-old girl with no airway symptoms show dynamic hypopharyngeal and nasopharyngeal motion. (a) Cine MR image obtained at one point during the respiratory cycle shows a patent hypopharynx (arrows) and nasopharynx (white arrowhead). The oropharynx (black arrowheads) is collapsed between the tongue and soft palate. The mouth is closed. (b) Cine MR image obtained at another point during the respiratory cycle shows decreased diameter of the hypopharynx (arrows) and collapse of the nasopharynx (arrowhead) between the soft palate and the adenoids. The oropharynx remains collapsed.

View larger version (144K): [in this window] [in a new window] [Download PPT slide]   Figure 2a. Cine MR images (fast gradient echo, 80° flip angle, 8.2/3.6, 8-mm section thickness, 128 consecutive midline sagittal images, 2-minute image time) in a 9-year-old boy with no airway symptoms show dynamic hypopharyngeal and nasopharyngeal motion. (a) Cine MR image obtained at one point during the respiratory cycle shows a patent hypopharynx (arrows) and nasopharynx (white arrowhead). The oropharynx (black arrowheads) is collapsed between the tongue and soft palate. The mouth is open. (b) Cine MR image obtained at another point during the respiratory cycle shows decreased diameter of the hypopharynx (arrows) and of the nasopharynx (arrowhead) between the soft palate and adenoids.

View larger version (144K): [in this window] [in a new window] [Download PPT slide]   Figure 2b. Cine MR images (fast gradient echo, 80° flip angle, 8.2/3.6, 8-mm section thickness, 128 consecutive midline sagittal images, 2-minute image time) in a 9-year-old boy with no airway symptoms show dynamic hypopharyngeal and nasopharyngeal motion. (a) Cine MR image obtained at one point during the respiratory cycle shows a patent hypopharynx (arrows) and nasopharynx (white arrowhead). The oropharynx (black arrowheads) is collapsed between the tongue and soft palate. The mouth is open. (b) Cine MR image obtained at another point during the respiratory cycle shows decreased diameter of the hypopharynx (arrows) and of the nasopharynx (arrowhead) between the soft palate and adenoids.

View larger version (144K): [in this window] [in a new window] [Download PPT slide]   Figure 3. Cine MR image (fast gradient echo, 80° flip angle, 8.2/3.6, 8-mm section thickness, 128 consecutive midline sagittal images, 2-minute image time) in a 2-year-old boy without airway symptoms shows vertical motion without other dynamic motion. The image shows the diameters and anatomic landmarks of the hypopharynx (arrows), nasopharynx (white arrowheads), and oropharynx (black arrowhead). All are patent and did not demonstrate dynamic motion or interval change in diameter during the cine. There was superior-to-inferior vertical motion of the entire airway, which is difficult to demonstrate on two static images. The mouth is open.

Vertical motion was present in 77 (52%) of the 148 patients and was absent in 71 (48%). There was high correlation between the presence of vertical motion and younger age (P < .001). The mean age of patients with vertical motion was 2.5 years; the mean age of those without vertical motion was 4.4 years. There was no statistically significant correlation between age and any of the other airway parameters evaluated (P > .05), including mouth position (P = .188), motion in the nasopharynx (P = .188), motion in the oropharynx (P = .279), and motion in the hypopharynx (P = .798).

Of the 148 patients, the mouth was open in 96 (65%) and was closed in 52 (35%). Data concerning the relationship between mouth position and airway motion are summarized in Table 2. There was no statistically significant relationship between mouth position and dynamic motion (ie, dynamic patency or intermittent collapse) in the hypopharynx (P = .655). The hypopharynx showed dynamic motion in 48 (50%) of 96 patients with open mouths and in 24 (46%) of 52 patients with closed mouths. There was a statistically significant increase in the number of patients with open mouths and dynamic motion of the oropharynx (P = .006) and/or the nasopharynx (P = .006). The oropharynx showed dynamic motion (ie, dynamic patency or intermittent collapse) in one (1%) of 96 patients with open mouths and in 12 (73%) of 52 patients with closed mouths. The nasopharynx showed dynamic motion in 41 (43%) of 96 patients with open mouths and in 12 (23%) of 52 patients with closed mouths.

	DISCUSSION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

In this series, dynamic motion of the airway was commonly encountered in asymptomatic sleeping children. Dynamic motion of the hypopharynx was encountered in 49% of subjects, and dynamic motion of the nasopharynx was encountered in 36% of subjects. The previous assumption that the airway of a healthy child demonstrates little or no respiratory motion during sleep (9–11) should be reconsidered. Some degree of motion of the pediatric airway should be considered normal in children. Concerning how much motion should be considered abnormal, in this series, the mean change in diameter was relatively small for each anatomic area studied: hypopharynx, 2.6 mm; nasopharynx, 2.2 mm; and oropharynx, 2.9 mm. The upper limit of the range of changes in diameter was 7.4 mm for the hypopharynx and 5.0 mm for both the oropharynx and the nasopharynx. It might be reasonable to consider anatomic regions that have motion measurements greater than 5 mm with greater suspicion for abnormality. With 5 mm for the criterion, most physiologic motion will not be considered abnormal.

The anatomic region with the greatest clinical relevance in the evaluation of dynamic abnormalities of the upper airway related to obstructive sleep apnea is the hypopharynx. Glossoptosis and hypopharyngeal collapse are two of the more common diagnoses made at dynamic sleep fluoroscopy (9–11,21), and each is defined by the type of motion that occurs. Glossoptosis is defined as abnormal posterior motion of the tongue during sleep. It is seen most commonly in children with neuromuscular abnormalities because of an abnormal decrease in muscular tone (11). It can also be associated with macroglossia and micrognathia. At fluoroscopy, the tongue "falls" posteriorly during sleep, abutting the velum (soft palate) and the posterior wall of the pharynx and obstructing the airway (11). Surgical interventions aimed at either reducing the volume of the tongue or repositioning the mandible have been described for those cases refractory to medical management techniques such as the use of positive pressure airway devices during sleep (22,23). In contrast, in pharyngeal collapse, the tongue moves posteriorly and the posterior wall of the pharynx moves anteriorly. This differs from glossoptosis, in which only the tongue moves posteriorly. In pharyngeal collapse, the posterior pharyngeal wall, the velum, and the tongue oppose each other, causing naso- and oropharyngeal obstruction. Pharyngeal collapse can be a primary problem or can occur secondary to an obstruction at another anatomic level. In this series, although dynamic motion was seen in the hypopharynx in nearly one-half of subjects, no asymptomatic subjects ever experienced hypopharyngeal collapse, either static or intermittent. Intermittent or static collapse of the hypopharynx should always be considered abnormal. In our group of asymptomatic subjects who had dynamic motion of the hypopharynx, motion of the posterior wall of the pharynx was much more common (86%), either alone (42%) or in conjunction with posterior motion of the tongue (44%), than was isolated posterior motion of the tongue without posterior pharyngeal wall motion (14%). Therefore, isolated posterior motion of the tongue should perhaps be considered with greater suspicion as possibly indicating an abnormality than should other patterns of hypopharyngeal motion. Any degree of hypopharyngeal motion with a change in diameter greater than 5 mm should also be considered with increasing suspicion for abnormality.

In evaluating these cine MR studies, we were impressed by the degree of vertical motion in many of the subjects. Vertical motion was noted in 52% of patients. It was often most striking in infants. There was a statistically significant correlation between younger age and presence of vertical motion (P < .001). We speculate that in infants, who have both very short necks and more elastic thoracic tissues (related to the fact that they have a higher degree of cartilage than do older children and adults), the "up and down" motion of the diaphragm is more often transferred to the neck and upper airway. Vertical motion should be considered a normal pattern of airway motion.

None of the airway parameters studied other than vertical motion had a statistically significant correlation between incidence and subject age. Because infants are thought to be obligate nasal breathers, we had suspected that there may be correlation between those parameters reflective of mouth breathing and age. However, neither the incidence of patent oropharynx nor the incidence of open mouth was related to age. Thirty-seven (25%) of the subjects in this study did have a static patent oropharynx, suggesting that they were "mouth breathers." The fact that a greater percentage than that (65%) had their mouths open during sleep raises the possibility that a child sleeping with his or her mouth open may not always be mouth breathing, because many of the children with open mouths did not have a patent oropharynx during sleep. There was no difference in the frequency of dynamic motion of the hypopharynx in those with open mouths versus those with closed mouths. It is unclear why there would be more motion of the oropharynx in those with closed mouths and more motion of the nasopharynx in those with open mouths. The nasopharynx may be more apt to be in motion in those breathing through the mouth.

One of the major disadvantages of dynamic sleep fluoroscopy in the evaluation of children with obstructive sleep apnea is the associated radiation dose. If cine MR techniques could adequately reveal patients with obstructive sleep apnea, the issue of radiation exposure would be eliminated. One of our other motivations in this trial was to gain experience in using cine MR techniques in the evaluation of the airway. The images obtained in these 148 subjects suggest that it may be technically feasible to use cine MR techniques in the evaluation of abnormal airway motion in children with obstructive sleep apnea. This issue needs to be further addressed.

In conclusion, dynamic motion of the airway often occurs in asymptomatic children during sleep. A certain degree of airway motion is common and should be considered normal. In the interpretation of images obtained in children with obstructive sleep apnea, changes in the diameter of the upper airway greater than 5 mm should be considered with increased suspicion as indicative of an abnormal pattern of airway motion. Static or intermittent collapse of the hypopharynx should always be considered abnormal.

	FOOTNOTES

 
Author contributions: Guarantor of integrity of entire study, L.F.D.; study concepts and design, L.F.D.; literature research, L.F.D.; clinical studies, L.F.D., K.A.C., B.L.K.; data acquisition, L.F.D., B.L.K.; data analysis/interpretation, all authors; statistical analysis, B.C.; manuscript preparation, L.F.D.; manuscript definition of intellectual content, editing, and revision/review, all authors; manuscript final version approval, L.F.D.

	REFERENCES

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