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1 Department of Radiology, Children's Hospital Medical Center and the University
of Cincinnati College of Medicine, 3333 Burnet Ave., Cincinnati, OH
45229-3039.
2 Department of Pediatrics, Children's Hospital Medical Center and the
University of Cincinnati College of Medicine, Cincinnati, OH 45229-3039.
Received October 22, 2001;
accepted after revision February 11, 2002.
Address correspondence to L. F. Donnelly.
Abstract
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SUBJECTS AND METHODS. We performed sagittal midline cine MR imaging (fast gradient-echo series: TR/TE, 8.2/3.6 sec; flip angle, 80°; slice thickness, 8 mm; 128 consecutive images; imaging time, 2 min; displayed in cine mode) in children referred for MR imaging of the brain who required sedation. The largest transverse diameter of the adenoids was recorded. A subjective impression was made as to whether the adenoids were enlarged or normal in size. Palatine tonsils were considered enlarged when a soft-tissue mass was identified on the midline cine images, and maximum diameter was recorded. Enlarged and nonenlarged adenoid and palatine tonsil groups were compared using motion parameters (chi-square or Fisher's exact test): mouth position (opened or closed); vertical motion (present, absent); nasopharyngeal, oropharyngeal, and hypopharyngeal motion (static patent, dynamic patent, intermittent collapsed, or static collapsed, and greatest change in size).
RESULTS. We studied 148 subjects who had a mean age of 3.4 years. The adenoid tonsils were considered enlarged in 64 patients (43%), and the palatine tonsils were considered enlarged in 29 patients (20%). The mean size of the enlarged adenoid tonsils was 11.6 mm and of the nonenlarged adenoid tonsils was 6.2 mm. Enlarged adenoids correlated with the open mouth position (p = 0.0242) and increased dynamic motion of the oropharynx (p = 0.0413). A trend was also seen for increased dynamic motion of the nasopharynx (p = 0.0723). Enlarged palatine tonsils correlated with an increased frequency of dynamic motion of the oropharynx (p = 0.0006) and the nasopharynx (p = 0.0033) and a trend for increased frequency of the open mouth position (p = 0.0692).
CONCLUSION. Large adenoid and palatine tonsil size affects breathing dynamics of the upper airway even in asymptomatic children.
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MR imaging has been advocated as an accurate way to depict and measure the size of the adenoid and palatine tonsils [1, 2]. MR imaging does not share some of the problems associated with tonsillar measurement as performed with lateral radiography, such as superimposition of overlying structures, anatomic variants of adjacent structures, magnification issues, and radiation dose [1, 2]. In addition, children with obstructive sleep apnea typically show increased dynamic motion of the upper airway, such as hypopharyngeal collapse, as compared with children without obstructive sleep apnea [14,15,16,17]. Cine MR imaging techniques have been described as successful in showing the motion abnormalities that are associated with obstructive sleep apnea [18,19,20,21]. The combination of data concerning static anatomic structure and data concerning dynamic motion available from cine MR imaging provides the opportunity to evaluate the relationship between the size of the adenoid and palatine tonsils and the degree of airway motion. If enlarged adenoid and palatine tonsils do play a role in causing obstructive sleep apnea, it would be expected that a correlation would exist between increasing tonsillar size and increased dynamic motion of the airway. This correlation may hold true even in children who are asymptomatic.
Children who are referred for MR imaging of the brain and require sedation to undergo the study are a potentially ideal population to study motion of the airway during sleep. They are already undergoing MR imaging, are asleep, and do not typically have airway abnormalities. For these reasons, we elected to use a cine MR imaging sequence to evaluate tonsillar size and dynamic airway motion in children who were already sedated for MR imaging of the brain. The purpose of this study was to evaluate variations in size of the adenoid and palatine tonsils and the relationship between tonsillar enlargement and upper airway motion in asymptomatic children during sleep using cine MR imaging.
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Efforts were made to exclude from the study those patients who might have abnormalities of the airway. Patients who had histories, signs, or symptoms of airway abnormalities were excluded from participation, including patients with previous airway surgery (adenoidectomy, tracheotomy), obstructive sleep apnea, or snoring detected during the presedation workup. Patients and parents were asked if the child had a history of snoring, obstructive sleep apnea, previous airway surgery, or other airway disease. At physical examination, stridor, wheezing, a tracheotomy, and scars from previous airway surgery were noted. Also, patients who experienced oxygen desaturation (drop in blood oxygen saturation below 95%) or noisy breathing (snoring) during the sedation were excluded. Therefore, all subjects in the study were asymptomatic in terms of airway diseases. Patients were referred for brain MR imaging for a variety of reasons. No exclusion criterion was based on the clinical indication for the brain MR imaging. The mean age and age range of subjects enrolled in the study were reflective of those patients who required sedation to complete MR imaging of the brain.
All sedations were performed and monitored in accordance with our departmental structured sedation program. Immediately before each sedation, the sedation nurse obtained a history and physical examinatioin that was supervised by the pediatric radiologist. Patients were sedated with either oral chloral hydrate (50-100 mg/kg of body weight) or IV pentobarbital (3 mg/kg, with repeated dosing if patient remained awake, up to a total of 7 mg/kg). Drug choice was based on patient age (chloral hydrate for patients < 1 year old, pentobarbital for patients > 1 year old). During the entire procedure and sedation recovery, respiratory rate, heart rate and rhythm, and blood oxygen saturation were monitored using transcutaneous pulse oximetry. All children were breathing spontaneously without any form of assisted ventilation.
The sequence used to perform the cine MR imaging was a fast gradient-echo sequence. Technical parameters included a TR/TE of 8.2/3.6 sec, a flip angle of 80°, and a slice 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 min. In all patients, sagittal T1-weighed images and axial T2-weighted images that included the nasopharynx were obtained as part of the clinical MR imaging brain protocol. These images were used, as well as initial localization images, to document that the cine MR imaging sequence was truly obtained in the sagittal midline plane. The images were used both during the performance of the study—the sequence was repeated if it was not in the true midline plane—and during interpretation of the cine MR images.
Because the children were in the head coil to obtain the clinically indicated brain images, cine MR imaging of the airway was performed with the patient in the head coil. In all children, the airway was visualized from the most superior portion of the nasopharynx to the mid trachea. Images were obtained on one of two 1.5-T MR scanners (General Electric Medical Systems, Milwaukee, WI). The obtained images were displayed in cine format, creating a real time "movie" of airway motion. The images were evaluated by two reviewers simultaneously. Conclusions were reached by consensus.
In each case, the maximal diameter of the adenoid tonsils was recorded in a manner similar to that used by Jaw et al. [2] and Vogler et al. [1]. Using the midline image, the thickness of the adenoid tonsil was measured at the maximal convexity of the adenoid in a line perpendicular to the anterior clival surface.
In our clinical practice, lateral digital radiographs are often obtained in children with obstructive sleep apnea or snoring to evaluate potentially enlarged adenoid tonsils. The pediatric radiologist interpreting the study makes a subjective impression (often without measurements) as to whether the tonsils are enlarged on the basis of the relative size of the adenoid compared with the size of the nasopharynx and whether the adenoid tonsils encroach on or obstruct the nasopharynx. In an attempt to determine the value of such subjective impressions, the reviewers, independently and before performing measurements, rendered a subjective impression as to whether the adenoid was enlarged or normal in size.
The palatine tonsils were judged to be enlarged or not enlarged. Palatine tonsils met criteria for enlargement when they were large enough that a soft-tissue mass was identified extending into the midline cine images. In most such cases, the palatine tonsils were grossly enlarged. If the palatine tonsils were enlarged, the maximum diameter was recorded. All measurements were made with electronic calipers.
Dynamic motion of the airway was evaluated in three anatomic locations: the nasopharynx, the oropharynx, and the hypopharynx. For anatomic consistency, the 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, and between the soft palate superiorly and the superior tip of the epiglottis inferiorly. In each location, motion was categorized as static patent, dynamic patent, intermittently collapsed, or static collapsed. Static patent was defined as the anatomic region of the airway being patent and motionless. Dynamic patent was defined as the anatomic region of the airway showing a measurable change in diameter but remaining patent during the entire duration of the cine MR imaging. Intermittent collapse was defined as the anatomic region of the airway showing a measurable change in diameter, at times during imaging being patent and at times, completely collapsed. Static collapse was defined as the anatomic region of the airway being collapsed during the entire duration of the cine MR imaging. For each anatomic area, the maximal diameter (in millimeters) of the airway from anterior to posterior was recorded. If dynamic motion was seen, the maximal change in diameter (in millimeters) was also recorded. The mouth position was noted as open or closed during the cine MR imaging. If the subject had a pacifier in place during the study, the mouth position was considered closed. Vertical motion was noted as present or absent. Vertical motion was defined as repetitive motion of the pharynx in a superior to inferior direction during the respiratory cycle.
Enlarged and nonenlarged adenoid and palatine tonsil groups were compared using parameters of airway motion for statistical correlation: mouth position (opened or closed); vertical motion (present or absent); and type and degree of nasopharyngeal, oropharyngeal, and hypopharyngeal motion (static patent, dynamic patent, intermittent collapsed, or static collapsed, and greatest change in size [in millimeters]). The chi-square test was used except for parameters for which numbers were small. In such cases, the Fisher's exact test was used. Adenoid size was compared by age group for statistical correlation using an analysis of variance test.
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The palatine tonsils were considered enlarged in 29 subjects (20%) (Fig. 1A,1B). The mean maximum diameter of the palatine tonsils considered enlarged was 22 mm. Data from comparison of enlarged and nonenlarged palatine tonsil groups with parameters of dynamic airway motion are presented in Table 2. Enlarged palatine tonsils correlated with both nasopharynx (p = 0.0033) and oropharynx (p = 0.0006) motion status. The data revealed a decreased probability of a static patent nasopharynx (38% vs 69%), an increased probability of a dynamic patent nasopharynx (45% vs 24%), an increased probability of a static patent oropharynx (48% vs 19%), and a decreased probability of a static collapsed oropharynx (38% vs 73%) in the enlarged palatine tonsil group. No parameters of hypopharyngeal motion showed statistically significant correlation with enlargement of the palatine tonsils.
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Dynamic imaging techniques, such as sleep fluoroscopy or cine MR imaging, are often used to evaluate anatomic causes of obstructive sleep apnea in patients when treatment is not precisely determined on the basis of physical examination, lateral radiography, and polysomnography alone [14,15,16,17]. Such patients are often complex in regard to airway issues and have a predisposition to airway obstruction at multiple sites or persistent obstructive sleep apnea despite previous airway surgery [14,15,16,17, 27]. A relatively smaller degree of airway motion is seen in asymptomatic children than in those with obstructive sleep apnea [14,15,16,17, 27]. When evaluating a patient with dynamic imaging techniques, the presence of abnormal, increased motion of the airway establishes the diagnosis of such abnormalities as pharyngeal collapse or glossoptosis [14,15,16,17].
In our study, statistically significant increases in airway motion dynamics were greater in patients with large adenoid and palatine tonsils. This finding was true despite the fact that the study population was asymptomatic. That increased tonsillar volume is associated with increased airway dynamics supports the notion that enlarged adenoid and palatine tonsils can contribute to airway compromise and the development of obstructive sleep apnea. The findings suggest that as adenoid tonsils enlarge, they can encroach on and obstruct the nasopharyngeal airways. Large adenoid size was associated with a statistically significant increase in occurrence of dynamic motion in the oropharynx and an increased likelihood of the mouth being open. A trend for increased dynamic motion in the nasopharynx was also noted. These findings suggest that with large adenoid tonsils, the tendency is to breathe through the mouth as a result of the compromised air flow through the nasopharynx. Likewise, enlargement of the palatine tonsils was associated with increased dynamic airway motion. With enlargement of the palatine tonsils, the oropharynx is in the typical static closed position less frequently and dynamic motion in the nasopharynx is increased, again suggesting increased involvement of the oropharynx in breathing.
The hypopharynx is the anatomic area in which the most common dynamic motion abnormalities, such as glossoptosis or pharyngeal collapse, are diagnosed [14,15,16,17]. Glossoptosis is defined as abnormal posterior motion of the tongue during sleep [15]. In contrast, with pharyngeal collapse the tongue moves posteriorly and the posterior wall of the pharynx moves anteriorly [15, 17]. In this series, no significant difference was seen in the dynamic motion of the hypopharynx between the enlarged and nonenlarged adenoid and palatine tonsillar groups. This finding may reflect the fact that our patient population was asymptomatic. The amount of airway obstruction needed to create a dynamic hypopharynx may be great enough to typically result in airway symptoms.
Our study has several limitations. The study was intended to evaluate the relationship of adenoid and palatine tonsil size to the degree of airway motion in asymptomatic children. This study does not yield further information concerning the airway dynamics of patients with obstructive sleep apnea, nor does it yield information supporting the use of cine MR imaging in the evaluation of children with obstructive sleep apnea. Second, because of the constraints of adding research imaging at the end of a clinically indicated brain imaging study, airway motion was evaluated only in the sagittal plane. Motion of the lateral pharyngeal walls, which may be a significant component of airway dynamics, was not evaluated by obtaining axial or coronal images. Third, the children imaged in this study were all referred for MR imaging of the brain for clinical reasons and thus may not completely reflect a normal population. However, efforts were made to exclude any patients with a history of physical findings of airway compromise. Finally, the patients in this study were sedated. Whether the airway dynamics that are present in sedation reflect what occurs in children during natural sleep is much debated. Relaxation of the pharyngeal musculature may occur during sedation. However, we, as well as many experts, believe that the airway dynamics of the sedated child, although not being precisely physiologic, are most likely closely representative of those during natural sleep. For years, physicians have relied, with good success, on information obtained during dynamic sleep fluoroscopy studies performed on sedated patients to make management decisions concerning patients with complex causes of obstructive sleep apnea [14, 15]. MR imaging evaluation of airway dynamics during sedation may be the best imaging tool that we have considering the difficulties in achieving natural sleep during MR imaging in children.
In conclusion, large adenoid and palatine tonsil size affects breathing dynamics of the upper airway, even in asymptomatic children. A statistically significant correlation exists between large adenoid and palatine tonsils and an increase in a number of parameters for dynamic motion of the upper airway. These findings may support the concept that enlarged tonsils contribute to airway obstruction and the development of obstructive sleep apnea.
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