REVIEW ARTICLE
Diagnostic Role of Magnetic Resonance Imaging in Obstructive Sleep Apnea Syndrome Ahmed Abdel Khalek Abdel Razek, MD Abstract: We aim to review the diagnostic role of magnetic resonance (MR) imaging in obstructive sleep apnea syndrome (OSAS). Basic background about sleep apnea, MR anatomy of the pharyngeal airway, and MR imaging sequences applied in obstructive sleep apnea are discussed. Static and dynamic MR imaging is used in the assessment of patients with OSAS. Magnetic resonance imaging can detect the level, degree, and cause of obstruction in the upper airway that guide the clinical diagnosis and treatment. Imaging is used for prediction of treatment outcome and monitoring and follow-up of patients with OSAS after therapy. Key Words: MR imaging, sleep, apnea, pharynx (J Comput Assist Tomogr 2015;39: 565–571)
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bstructive sleep apnea syndrome (OSAS) is a common disorder characterized by repetitive, partial, or complete obstruction of the upper airway during sleep resulting in episodic hypoxemia, arousal, and fragmented sleep. The most common complaints are snoring and excessive daytime sleepiness. Obstructive sleep apnea syndromes affect all age groups, and approximately 3% of all children are affected by OSAS. The lifetime incidence of OSAS in adults (30–45 years) is greater than that in men (9%–24%) compared with women (4%–9%) because men have inferiorly positioned hyoid bones, longer and thicker uvulas, and greater neck circumferences. The risk factors for OSAS include a family history of sleep apnea, a large neck, a recessed chin, any abnormalities in the structure of the upper airway, smoking, alcohol use, and age. Consequences of OSAS include neurocognitive impairment, stroke, and cardiovascular sequelae, including hypertension and myocardial infarction.1–3 Current theories on OSAS pathogenesis involve a combination of abnormalities in the anatomy of the pharynx and the physiology of the upper airway dilator muscles. Anatomical changes in OSAS include decreased anteroposterior, lateral, cross-sectional, and volumetric measurements at different pharyngeal levels. Inefficacy of the upper airway dilator muscles to maintain adequate airway despite the negative intraluminal pressure during inspiration has a role in the pathophysiology of OSAS.2–4 Although polysomnography is the gold standard for diagnosis of OSAS, it cannot actually detect the level, degree, and causes of obstruction. It is important to determine the level, degree, and causes of the obstruction so that appropriate conservative and surgical treatment planning can be undertaken. Different imaging modalities are used for assessment of patients with OSAS. Computed tomographic scan has a role in the assessment of patients with OSAS, but it is associated with radiation exposure and is
From the Department of Diagnostic Radiology, Mansoura Faculty of Medicine, Mansoura, Egypt. Received for publication January 26, 2015; accepted February 6, 2015. Reprints: Ahmed Abdel Khalek Abdel Razek, MD, Department of Diagnostic Radiology, Mansoura Faculty of Medicine, Mansoura 13351, Egypt (e‐mail: [email protected]). Presented as an educational exhibit at the assembly and annual meeting of Radiological Society of North America. The authors declare no conflict of interest. Copyright © 2015 Wolters Kluwer Health, Inc. All rights reserved.
inadequate for soft tissue differentiation. Cephalometry can assess craniofacial abnormalities, but of limited value in the evaluation of soft tissue structures. Different articles discuss the role of magnetic resonance (MR) imaging in the assessment of patients with OSAS.4–6 Magnetic resonance imaging can help for the determination of the degree of pharyngeal airway narrowing, volumetric assessment of soft tissues changes, and craniofacial abnormalities. Magnetic resonance imaging data increase our knowledge of the pathophysiology of OSAS and provide new insights into OSAS evaluation and treatment planning.5–8 The aim of this work is to review the diagnostic role of MR imaging in OSAS with illustration of potential causes of OSAS detected on MR imaging.
TECHNIQUE OF MR IMAGING Anatomical MR Imaging The anatomical subdivision of the upper airway is as follows: nasopharynx (region of airway between the skull base and the hard palate), velopharynx (region from the hard palate to the tip of the soft palate), retroglossal region of the oropharynx (region from the tip of the soft palate to the tip of the epiglottis), and hypopharynx (region from the tip of the epiglottis to the glottis level1–4 (Fig. 1). To image this anatomy, we use a midsagittal and axial sequential T1-weighted (repetition time, 650 milliseconds; echo time, 14 milliseconds) and T2-weighted (repetition time, 6,000 milliseconds; echo time, 90 milliseconds) images with 3-mm slice thickness. The sagittal planes are obtained from the midline laterally, and the axial planes are obtained from the skull base to the larynx. Patients are instructed to refrain from swallowing during scanning and to breathe through their nosewith their mouth closed. The image analysis is done on workstation with determination of the level and cause of obstruction. Two-dimensional distances and diameters of the upper airway or its related structures are measured. Researchers evaluatevolumes of soft tissue structures such as the tongue, the adenoids, the soft palate, or the pharyngeal walls or the remaining compromised or noncompromised airway spaces. To obtain 3dimensional data, volumes based on cross-sectional areas and slice thickness are established by various computerized models.4–9
Dynamic MR Imaging Dynamic MR imaging can obtain rapid images (1 image per second) that are temporally spaced a short time apart. Dynamic MR imaging can show dynamic motion of the upper airway, thereby allowing visualization of the changing shape and configuration of the airway during respiration and evaluation of the relationship between the soft tissue of the upper airway such as adenoid, palatine tonsils, and soft palate and the degree of airway compromise.10,11 Dynamic MR obtained during a normal sleeping state shows the patent nasopharynx and retroglossal airway (Fig. 1) with minimal airway motion. The degree of motion of the retroglossal airway is less than 5 mm. Dynamic MR in OSAS showed complete airway collapse at the level of the soft palate and base of the tongue during apneic events. Sedation is recommended in
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at different levels to calculate the volume is time-consuming, and there are interobserver and intraobserver variabilities. Automated software for volumetric assessment improves the accuracy of the results.4,6,14
Causes of Airway Obstruction
FIGURE 1. Anatomy of the pharyngeal airway. Sagittal T1-weighted image shows that the nasopharynx is the region between the skull base and the hard palate, velopharynx is the region from the hard palate to the tip of the soft palate, retroglossal region of the oropharynx is the region from the tip of the soft palate to the tip of the epiglottis, and hypopharynx is the region from the tip of the epiglottis to the glottis level. Figure 1 can be viewed online in color at www.jcat.org.
MR imaging of the airway, especially in a dynamic study to simulate the phases of sleep as muscle tone of the pharynx varies between awake and asleep states. Children with OSAS are sedated successfully and safely for MR imaging. Sedation is used with caution in adults because of intermittent airway obstruction.2–4 Sleep MR is a real-time device that detects and characterizes the anatomical site, magnitude, and duration of airway obstruction simultaneously with MR-compatible physiologic measures of peripheral arterial tone, hemoglobin oxygen saturation, and pulse rate in patients with OSAS.10–12 Recently, real-time MR imaging platform for synchronous, multiplanar visualization of upper airway collapse in OSAS at 3 T was performed to promote natural sleep, with an emphasis on lateral pharyngeal wall visualization.12
ROLE OF MR IMAGING Level of Airway Obstruction The site of obstruction in OSAS may be at the nasopharynx, velopharynx, retroglossal region of the oropharynx, or hypopharynx, or at multiple combined levels of obstruction. The retropalatal and retroglossal regions of the pharynx are the most common sites of upper airway collapse in adult patients with OSAS.1,5 The most frequent sites of pharyngeal collapse are the soft palate, lateral pharyngeal walls, palatine tonsils, and base of the tongue. Determination of level of airway obstruction is important for treatment planning and patient outcome.9,13
Degree of Airway Obstruction Measuring the anteroposterior and transverse diameters and cross-sectional area, and volumetric assessment of the airway and soft tissue structures can help in the determination of the degree of airway obstruction in patients with OSAS. The measured soft tissues are adenoid tonsils, lingual tonsils, palatine tonsil, soft palate, tongue, lateral pharyngeal wall, and fat pad area. The measurement is usually done at the largest section of the soft tissue and narrowed section of the airway. The cross-sectional area of the soft tissues and the airway at different levels is calculated. Measurement of the upper airway revealed enlarged soft tissue structures and narrowed pharyngeal airway in patients with OSAS. Manually drawing the contour of the soft tissue and pharyngeal airway
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Obstructive sleep apnea syndrome is caused by obstruction anywhere in the upper airway, from the nasopharynx to the larynx. It may due to obstruction at multiple levels, either simultaneously or in an alternating pattern.3–6 It may due to enlargement of soft tissue structures and alterations of craniofacial structures. Enlargement of soft tissue includes an enlarged adenoid, the palatine tonsils, the lingual tonsils, the soft palate, and the tongue as well as accumulation of fat in the parapharyngeal walls. Alternations in craniofacial structures such as retroposition of maxilla and mandible and inferior positioned hyoid bone are reported in patients with OSAS.1–5 Table 1 shows the causes of OSAS according to the level of obstruction.
Enlarged Adenoid Tonsils Enlarged adenoid tonsils are usually obstructing the nasopharynx. Adenoids are absent at birth and then rapidly proliferate during infancy. They reach a maximum size between 2 and 10 years of age and then begin to decrease in size during puberty. The normal size of the adenoids is between 7 and 12 mm. Adenoids larger than 12 mm in size is abnormally enlarged (Fig. 2). The mean size of the adenoid tonsils was statistically larger in the patients with OSAS (13.46 mm) than that in those without this abnormality. There is increased dynamic motion of the airway with increased adenoid size at dynamic MR imaging. Children with enlarged adenoids and OSAS have larger volumes of deep cervical lymph nodes, denoting that enlarged adenoids are a part of larger spectrum of cervical lymphoid hypertrophy. Criteria for recurrent adenoids include regrowth of the adenoid tonsils greater than 12 mm in the midline sagittal plane and association of intermittent collapse of the posterior nasopharynx on dynamic MR imaging.3–6,15,16
Enlarged Palatine Tonsils The palatine tonsils, also referred to as faucial tonsils, are 2 prominent soft tissues, one on each side, located in between the glossopalatine and pharyngopalatine arches. Enlargement of the palatine tonsils is a common cause of OSAS in children. Criteria used for enlargement of the palatine tonsils include prominence of palatine tonsils associated with obstruction of the retroglossal
TABLE 1. Causes of OSAS According to the Level of Obstruction Level
Causes of OSAS
Nasopharynx Oropharynx
Tongue Hypopharynx Larynx Retropharyngeal space Parapharyngeal space Craniofacial structure Associated disorders
Enlarged adenoid tonsils, recurrent adenoid Enlarged palatine tonsil, enlarged lingual tonsils, elongated and/or thickened soft palate Macroglossia, glossoptosis Valecular cyst or mass, hypopharyngeal collapse Elongated epiglottis Infection, benign masses, malignancy Fatty deposition Mandibular hypoplasia, acromegaly Genetic and metabolic disorders
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FIGURE 2. Adenoid tonsil. A and B, Sagittal and axial T2-weighted images in another patient show an enlarged adenoid (arrow) that nearly completely obstructs the nasopharyngeal airway. C, Sagittal gradient–recalled echo MR image shows and enlarged adenoid that narrows the nasopharyngeal airway with prominent soft palate.
FIGURE 3. Palatine tonsil. A, Axial T1-weighted image shows both enlarged palatine tonsils (arrows) with marked narrowing of the pharyngeal airway. B, Parasagittal T2-weighted image in another patient shows an enlarged hyperintense palatine tonsil (arrow) that compromises along the pharyngeal airway.
airway (Fig. 3). The palatine tonsils are an encapsulated organ that is easily surgically removed. There is no recurrent palatine tonsil after palatine tonsillectomy.4–8
Enlarged Lingual Tonsils Normally, the lingual tonsil appears as a small disk of high T2-weighted signal at the posterior aspect of the inferior tongue. When the lingual tonsils enlarged, they appear as a large high T2-signal mass posterior to the tongue often obstructing the velopharynx. Often when they enlarge, the tonsils appear as one large dumbbell-shaped mass rather than 2 discrete lingual tonsils (Fig. 4). The lingual tonsils were noted as markedly enlarged if the anteroposterior diameter is more than 10 mm.17,18
Enlarged and Elongated Soft Palate Normally, the soft palate is isointense to tongue musculature on T2-weighted images. When the soft palate becomes edematous, it becomes high in signal on T2 weighted and thickens (>1 cm). The soft palate thickens in OSAS because of microtrauma from fluttering during snoring. Thickened soft palate contributes to worsening of OSAS by taking up more potential airway space. Criteria to consider a soft palate to be “elongated” include when the soft palate draped over abutting the tongue or soft palate
FIGURE 4. Lingual tonsil. Axial T2-weighted image shows that enlarged lingual tonsils (arrows) appear as a large high T2-signal mass obstructing the retroglossal region of the oropharynx.
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FIGURE 5. Enlarged and elongated soft palate. A, Sagittal T1-weighted image shows an enlarged and prominent soft palate that hangs and abuts the posterior pharyngeal airway with subsequent narrowing. B, Sagittal T2-weighted image in another patient shows an elongated soft palate (long arrow) that reaches to the epiglottis. Note the associated enlarged adenoid (short arrow).
posteriorly positioned abutting the adenoids and obstructing the nasopharynx, and when the soft palate hangs inferiorly, below the midtongue or touches the epiglottis (Fig. 5). These patients are treated with uvulopalatoplasty.4–8,19
Macroglossia Macroglossia is defined as a resting tongue that protrudes beyond the alveolar ridge and the posterior aspect of the tongue sits near the posterior wall of the retroglossal airway, resulting in a consistently narrowed airway. Common causes include hypothyroidism, idiopathic hyperplasia, mucopolysaccharidosis, and chromosomal abnormalities, such as the Beckwith-Wiedeman syndrome and Down syndrome. The tongue may be relatively large in patients who have a small mandible (micrognathia), which is termed as relative macroglossia. An enlarged tongue can fall posteriorly during sleep, obstructing the retroglossal airway. Magnetic resonance imaging is useful in assessing the size of the tongue and the degree of compression along the retroglossal
airway (Fig. 6). Reduction glossectomy has been the main surgical treatment for patients with symptomatic macroglossia.7,8,20
Glossoptosis Glossoptosis is defined as posterior motion of the tongue during sleep. With glossoptosis, the posterior border of the tongue intermittently moves posteriorly and abuts the posterior pharyngeal wall causing obstruction of the retroglossal airway. The presence of glossoptosis is associated with macroglossia, micrognathia, or decreased muscular tone. Populations at risk include those with Down syndrome, cerebral palsy, and PierreRobin syndrome. Dynamic sagittal MR imaging demonstrates the tongue to “fall” posteriorly, abutting the velum and the posterior wall of the pharynx, which causes upper airway obstruction (Fig. 7). In severe glossoptosis, the tongue can also push the soft palate posteriorly, causing intermittent obstruction of the nasopharynx. On axial images obtained at the level of the middle portion of the tongue, the predominant motion is anterior to posterior
FIGURE 6. Macroglossia. A, Axial T1-weighted image shows an enlarged tongue that narrows the pharyngeal airway. B, Sagittal T2-weighted image shows an enlarged tongue that is associated with enlarged adenoids (arrow head) that narrow the nasopharynx, and enlarged soft palate (short arrow) and lingual tonsils (long arrow) that narrow the velopharynx.
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FIGURE 7. Glossoptosis. A, Sagittal gradient–recalled echo MR image during expiration shows the retroglossal airway. B, Sagittal gradient–recalled echo MR image during inspiration shows the posterior aspect of the tongue that moves posteriorly and narrows the retroglossal airway. Note that there are prominent adenoid and soft palate.
motion of the tongue intermittently obstructing the retroglossal airway, whereas the lateral and the posterior aspects of the retroglossal airway remain stable in position.8–21
Hypopharyngeal Collapse Hypopharyngeal collapse is the term given to the collapse of the retroglossal airway that is related to decreased muscular tone. In contrast to glossoptosis where there is abnormal posterior motion of the tongue during sleep, the hypopharyngeal collapse shows the tongue moving posteriorly and the posterior wall of the pharynx moving anteriorly. Certain patients, particularly those with Down syndrome, will have both components of glossoptosis and a floppy airway at risk for hypopharyngeal collapse.7,8
Mandibular hypoplasia may be idiopathic but more commonly associated with certain inherited disorders and syndromes, such as Treacher Collins syndrome, Nager syndrome, Goldenhar syndrome, hemifacial microsomia, trisomies 17-18 and 13-15, Cri Du Chat syndrome, and Pierre Robin sequence. Magnetic resonance imaging is helpful in establishing the size and position of the tongue in relation to the hypoplastic mandible and degree of airway compromise.10,11
Associated Disorders In Down syndrome, there is no true or absolute macroglossia but a relative macroglossia in relation to the size of the oral cavity. Obstructive sleep apnea syndrome occurs in 30% to 60% of patients
Hypopharyngeal and Laryngeal Lesions Valecular cysts of the hypopharynx (Fig. 8) and other soft tissue tumors such as lipoma in the hypopharyngeal region have been associated with OSAS. The larynx can be involved as a site of obstruction, at epiglottis level in most cases. Edema and granulomatous lesions of the epiglottis as scleroma may be associated with OSAS.3,7,9
Fat Deposition in Parapharyngeal Space Excess adipose fatty tissue deposition in the parapharyngeal space may be associated with OSAS.6,8
Retropharyngeal Lesions Soft tissue tumors of the retropharyngeal space such as lipoma and schwannoma (Fig. 9) usually narrow the airway with OSAS. Retropharyngeal abscess associated with bacterial or tuberculous infection may be associated with OSAS. Lastly, bony tumor such as exostosis from the cervical spine may be associated with OSAS.1–7,22
Craniofacial Abnormalities Craniofacial abnormalities such as retrognathia, inferiorly positioned hyoid bone, and maxillary and mandibular retroposition are associated with OSAS. Cephalometry and computed tomographic scan are important for detection of osseous changes; however, MR has a role but of limited value. There is a relationship between surface facial dimensions and upper airway structures measured at MR imaging in patients with OSAS.23,24
FIGURE 8. Valecular cyst. Sagittal T2-weighted image shows a large hyperintense valecular cyst (long arrow) that narrows the hypopharyngeal airway. Note that there are an associated enlarged lingual tonsil (short arrow) that narrows the velopharynx and adenoids (arrow head) that narrow the nasopharyngeal airway.
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FIGURE 9. Retropharyngeal schwannoma. Sagittal contrast T1-weighted image shows a large intense, enhanced oblong solid mass (arrow) obstructing the hypopharyngeal and oropharyngeal airway.
with Down syndrome.25 Congenital conditions affecting craniofacial development such as Chiari, Marfan, Down, and the Pierre Robin syndrome predispose to OSAS.7,8 Endocrinologic conditions such as acromegaly and hypothyroidism are associated with a higher prevalence of OSAS.26
Predictors of Treatment Response and Posttreatment Conservative therapy is usually recommended first because it is noninvasive. Medical sleep centers provide several treatment methods for OSAS such as sleep hygiene, dental splints, and continuous positive airway pressure devices. Although the continuous
positive airway pressure device is the preferred treatment, poor compliance is common. Patients intolerant of conventional medical treatment may benefit from surgical therapy to alleviate pharyngeal obstruction. Tongue reduction surgery included genioglossus advancement, mandibular advancement, and hyoid suspension surgery, which are usually done in patients with retroglossal obstruction. Uvulopalatopharyngoplasty is the surgery usually done in patients with retropalatal obstruction. Maxillomandibular advancement has the highest surgical efficacy (86%) and cure rate (43%). The success of genioglossus advancement ranges from 23% to 77%. Soft palate surgical techniques are less successful, with uvulopalatopharyngoplasty having an OSAS surgical success rate of 50% and a cure rate of 16%.1,4,27 Magnetic resonance imaging is used to predict treatment response and to assess the potential effects or adverse effects of various therapeutic interventions, including surgical and nonsurgical strategies on the upper airway anatomy.1–4,27 Magnetic resonance imaging shows a decrease in the tongue volume in successful medical treatment for patients with OSAS and acromegaly26 and the effect of oral appliance on pharyngeal airway in patients with OSAS28 (Fig. 10). Magnetic resonance imaging demonstrated that the mandibular advancement surgery increases the airway by forward displacement of the entire tongue, and it produces lateral airway expansion via a direct connection between the lateral walls and the ramus of the mandible. Two MR biomarkers that predict response to genioglossus advancement are the relative size of the tongue and adenoid anteroposterior diameter. These findings may help to identify patients with OSA who most likely would benefit from genioglossus advancement surgery. Magnetic resonance imaging assesses changes in the airway after hyoid surgery. In radiofrequency surgery, MR imaging visualizes immediate postoperative effects on the soft tissue of the soft palate and the tongue base.29,30
ADVANTAGE AND LIMITATIONS Magnetic resonance imaging provides an image with excellent contrast of the soft tissue structures in patients with OSAS. A fast MR imaging is able to show the anatomical obstruction dynamically during apnea. Magnetic resonance imaging does not expose patients to ionizing radiation, and it allows imaging in multiple planes. The major limitations of MR imaging are as
FIGURE 10. Obstructive sleep apnea syndrome pretreatment and posttreatment. A, Sagittal T2-weighted image before treatment shows an enlarged and elongated soft palate that narrows the velopharynx (arrow). B, Sagittal T2-weighted image after oral appliance shows a widened velopharynx (arrow).
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follows: long examination time, noisy scanning, claustrophobic effects experienced by many people while in the gantry tube, and high cost. The lack of a comfortable sleep environment also limits the ability to use MR imaging during sleep.4–8
SUMMARY AND CONCLUSION Magnetic resonance imaging is essential for diagnosis and treatment planning of OSAS because it can detect the level, degree, and causes of the upper airway obstruction. It has a role in prediction treatment response and monitoring of patients with OSAS after therapy. REFERENCES 1. Kendzerska T, Mollayeva T, Gershon AS, et al. Untreated obstructive sleep apnea and the risk for serious long-term adverse outcomes: a systematic review. Sleep Med Rev. 2014;18:49–59. 2. Mannarino M, Di Filippo F, Pirro M. Obstructive sleep apnea syndrome. Eur J Intern Med. 2012;23:586–593. 3. Simon S, Collop N. Latest advances in sleep medicine: obstructive sleep apnea. Chest. 2012;142:1645–1651. 4. Strauss R, Burgoyne C. Diagnostic imaging and sleep medicine. Dent Clin North Am. 2008;52:891–915. 5. Junior C, Filho H, Gomes C, et al. Radiological findings in patients with obstructive sleep apnea. J Bras Pneumol. 2013;39:98–101.
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15. Parikh SR, Sadoughi B, Sin S, et al. Deep cervical lymph node hypertrophy: a new paradigm in the understanding of pediatric obstructive sleep apnea. Laryngoscope. 2013;123:2043–2049. 16. Nandalike K, Shifteh K, Sin S, et al. Adenotonsillectomy in obese children with obstructive sleep apnea syndrome: magnetic resonance imaging findings and considerations. Sleep. 2013;36:841–847. 17. Sedaghat A, Flax-Goldenberg R, Gayler B, et al. A case–control comparison of lingual tonsillar size in children with and without Down syndrome. Laryngoscope. 2012;122:1165–1169. 18. Fricke BL, Donnelly LF, Shott SR, et al. Comparison of lingual tonsil size as depicted on MR imaging between children with obstructive sleep apnea despite previous tonsillectomy and adenoidectomy and normal controls. Pediatr Radiol. 2006;36:518–523. 19. Song CM, Lee CH, Rhee CS, et al. Analysis of genetic expression in the soft palate of patients with obstructive sleep apnea. Acta Otolaryngol. 2012;132(Suppl 1): S63–S68. 20. Guimaraes CV, Donnelly LF, Shott SR, et al. Relative rather than absolute macroglossia in patients with Down syndrome: implications for treatment of obstructive sleep apnea. Pediatr Radiol. 2008;38:1062–1067. 21. Donnelly LF, Strife JL, Myer CM3rd. Glossoptosis (posterior displacement of the tongue) during sleep: a frequent cause of sleep apnea in pediatric patients referred for dynamic sleep fluoroscopy. AJR Am J Roentgenol. 2000;175:1557–1560. 22. Zafereo ME Jr, Pereira KD. Chronic retropharyngeal abscess presenting as obstructive sleep apnea. Pediatr Emerg Care. 2008;24:382–384.
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27. Freedman N. Treatment of obstructive sleep apnea syndrome. Clin Chest Med. 2010;31:187–201. 28. Fleck RJ, Mahmoud M, McConnell K, et al. An adverse effect of positive airway pressure on the upper airway documented with magnetic resonance imaging. JAMA Otolaryngol Head Neck Surg. 2013;139: 636–638. 29. Choudhury M, Padmanabhan TV. A preliminary report on the effect of a mandibular advancement device on obstructive sleep apnea using magnetic resonance imaging and polysomnography. Int J Prosthodont. 2012;25: 613–618. 30. Schaaf W, Wootten C, Donnelly L, et al. Findings on MR sleep studies as biomarkers to predict outcome of genioglossus advancement in the treatment of obstructive sleep apnea in children and young adults. AJR Am J Roentgenol. 2010;194:1204–1209.
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Diagnostic Role of Magnetic Resonance Imaging in Obstructive Sleep Apnea Syndrome Ahmed Abdel Khalek Abdel Razek, MD Abstract: We aim to review the diagnostic role of magnetic resonance (MR) imaging in obstructive sleep apnea syndrome (OSAS). Basic background about sleep apnea, MR anatomy of the pharyngeal airway, and MR imaging sequences applied in obstructive sleep apnea are discussed. Static and dynamic MR imaging is used in the assessment of patients with OSAS. Magnetic resonance imaging can detect the level, degree, and cause of obstruction in the upper airway that guide the clinical diagnosis and treatment. Imaging is used for prediction of treatment outcome and monitoring and follow-up of patients with OSAS after therapy. Key Words: MR imaging, sleep, apnea, pharynx (J Comput Assist Tomogr 2015;39: 565–571)
O
bstructive sleep apnea syndrome (OSAS) is a common disorder characterized by repetitive, partial, or complete obstruction of the upper airway during sleep resulting in episodic hypoxemia, arousal, and fragmented sleep. The most common complaints are snoring and excessive daytime sleepiness. Obstructive sleep apnea syndromes affect all age groups, and approximately 3% of all children are affected by OSAS. The lifetime incidence of OSAS in adults (30–45 years) is greater than that in men (9%–24%) compared with women (4%–9%) because men have inferiorly positioned hyoid bones, longer and thicker uvulas, and greater neck circumferences. The risk factors for OSAS include a family history of sleep apnea, a large neck, a recessed chin, any abnormalities in the structure of the upper airway, smoking, alcohol use, and age. Consequences of OSAS include neurocognitive impairment, stroke, and cardiovascular sequelae, including hypertension and myocardial infarction.1–3 Current theories on OSAS pathogenesis involve a combination of abnormalities in the anatomy of the pharynx and the physiology of the upper airway dilator muscles. Anatomical changes in OSAS include decreased anteroposterior, lateral, cross-sectional, and volumetric measurements at different pharyngeal levels. Inefficacy of the upper airway dilator muscles to maintain adequate airway despite the negative intraluminal pressure during inspiration has a role in the pathophysiology of OSAS.2–4 Although polysomnography is the gold standard for diagnosis of OSAS, it cannot actually detect the level, degree, and causes of obstruction. It is important to determine the level, degree, and causes of the obstruction so that appropriate conservative and surgical treatment planning can be undertaken. Different imaging modalities are used for assessment of patients with OSAS. Computed tomographic scan has a role in the assessment of patients with OSAS, but it is associated with radiation exposure and is
From the Department of Diagnostic Radiology, Mansoura Faculty of Medicine, Mansoura, Egypt. Received for publication January 26, 2015; accepted February 6, 2015. Reprints: Ahmed Abdel Khalek Abdel Razek, MD, Department of Diagnostic Radiology, Mansoura Faculty of Medicine, Mansoura 13351, Egypt (e‐mail: [email protected]). Presented as an educational exhibit at the assembly and annual meeting of Radiological Society of North America. The authors declare no conflict of interest. Copyright © 2015 Wolters Kluwer Health, Inc. All rights reserved.
inadequate for soft tissue differentiation. Cephalometry can assess craniofacial abnormalities, but of limited value in the evaluation of soft tissue structures. Different articles discuss the role of magnetic resonance (MR) imaging in the assessment of patients with OSAS.4–6 Magnetic resonance imaging can help for the determination of the degree of pharyngeal airway narrowing, volumetric assessment of soft tissues changes, and craniofacial abnormalities. Magnetic resonance imaging data increase our knowledge of the pathophysiology of OSAS and provide new insights into OSAS evaluation and treatment planning.5–8 The aim of this work is to review the diagnostic role of MR imaging in OSAS with illustration of potential causes of OSAS detected on MR imaging.
TECHNIQUE OF MR IMAGING Anatomical MR Imaging The anatomical subdivision of the upper airway is as follows: nasopharynx (region of airway between the skull base and the hard palate), velopharynx (region from the hard palate to the tip of the soft palate), retroglossal region of the oropharynx (region from the tip of the soft palate to the tip of the epiglottis), and hypopharynx (region from the tip of the epiglottis to the glottis level1–4 (Fig. 1). To image this anatomy, we use a midsagittal and axial sequential T1-weighted (repetition time, 650 milliseconds; echo time, 14 milliseconds) and T2-weighted (repetition time, 6,000 milliseconds; echo time, 90 milliseconds) images with 3-mm slice thickness. The sagittal planes are obtained from the midline laterally, and the axial planes are obtained from the skull base to the larynx. Patients are instructed to refrain from swallowing during scanning and to breathe through their nosewith their mouth closed. The image analysis is done on workstation with determination of the level and cause of obstruction. Two-dimensional distances and diameters of the upper airway or its related structures are measured. Researchers evaluatevolumes of soft tissue structures such as the tongue, the adenoids, the soft palate, or the pharyngeal walls or the remaining compromised or noncompromised airway spaces. To obtain 3dimensional data, volumes based on cross-sectional areas and slice thickness are established by various computerized models.4–9
Dynamic MR Imaging Dynamic MR imaging can obtain rapid images (1 image per second) that are temporally spaced a short time apart. Dynamic MR imaging can show dynamic motion of the upper airway, thereby allowing visualization of the changing shape and configuration of the airway during respiration and evaluation of the relationship between the soft tissue of the upper airway such as adenoid, palatine tonsils, and soft palate and the degree of airway compromise.10,11 Dynamic MR obtained during a normal sleeping state shows the patent nasopharynx and retroglossal airway (Fig. 1) with minimal airway motion. The degree of motion of the retroglossal airway is less than 5 mm. Dynamic MR in OSAS showed complete airway collapse at the level of the soft palate and base of the tongue during apneic events. Sedation is recommended in
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at different levels to calculate the volume is time-consuming, and there are interobserver and intraobserver variabilities. Automated software for volumetric assessment improves the accuracy of the results.4,6,14
Causes of Airway Obstruction
FIGURE 1. Anatomy of the pharyngeal airway. Sagittal T1-weighted image shows that the nasopharynx is the region between the skull base and the hard palate, velopharynx is the region from the hard palate to the tip of the soft palate, retroglossal region of the oropharynx is the region from the tip of the soft palate to the tip of the epiglottis, and hypopharynx is the region from the tip of the epiglottis to the glottis level. Figure 1 can be viewed online in color at www.jcat.org.
MR imaging of the airway, especially in a dynamic study to simulate the phases of sleep as muscle tone of the pharynx varies between awake and asleep states. Children with OSAS are sedated successfully and safely for MR imaging. Sedation is used with caution in adults because of intermittent airway obstruction.2–4 Sleep MR is a real-time device that detects and characterizes the anatomical site, magnitude, and duration of airway obstruction simultaneously with MR-compatible physiologic measures of peripheral arterial tone, hemoglobin oxygen saturation, and pulse rate in patients with OSAS.10–12 Recently, real-time MR imaging platform for synchronous, multiplanar visualization of upper airway collapse in OSAS at 3 T was performed to promote natural sleep, with an emphasis on lateral pharyngeal wall visualization.12
ROLE OF MR IMAGING Level of Airway Obstruction The site of obstruction in OSAS may be at the nasopharynx, velopharynx, retroglossal region of the oropharynx, or hypopharynx, or at multiple combined levels of obstruction. The retropalatal and retroglossal regions of the pharynx are the most common sites of upper airway collapse in adult patients with OSAS.1,5 The most frequent sites of pharyngeal collapse are the soft palate, lateral pharyngeal walls, palatine tonsils, and base of the tongue. Determination of level of airway obstruction is important for treatment planning and patient outcome.9,13
Degree of Airway Obstruction Measuring the anteroposterior and transverse diameters and cross-sectional area, and volumetric assessment of the airway and soft tissue structures can help in the determination of the degree of airway obstruction in patients with OSAS. The measured soft tissues are adenoid tonsils, lingual tonsils, palatine tonsil, soft palate, tongue, lateral pharyngeal wall, and fat pad area. The measurement is usually done at the largest section of the soft tissue and narrowed section of the airway. The cross-sectional area of the soft tissues and the airway at different levels is calculated. Measurement of the upper airway revealed enlarged soft tissue structures and narrowed pharyngeal airway in patients with OSAS. Manually drawing the contour of the soft tissue and pharyngeal airway
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Obstructive sleep apnea syndrome is caused by obstruction anywhere in the upper airway, from the nasopharynx to the larynx. It may due to obstruction at multiple levels, either simultaneously or in an alternating pattern.3–6 It may due to enlargement of soft tissue structures and alterations of craniofacial structures. Enlargement of soft tissue includes an enlarged adenoid, the palatine tonsils, the lingual tonsils, the soft palate, and the tongue as well as accumulation of fat in the parapharyngeal walls. Alternations in craniofacial structures such as retroposition of maxilla and mandible and inferior positioned hyoid bone are reported in patients with OSAS.1–5 Table 1 shows the causes of OSAS according to the level of obstruction.
Enlarged Adenoid Tonsils Enlarged adenoid tonsils are usually obstructing the nasopharynx. Adenoids are absent at birth and then rapidly proliferate during infancy. They reach a maximum size between 2 and 10 years of age and then begin to decrease in size during puberty. The normal size of the adenoids is between 7 and 12 mm. Adenoids larger than 12 mm in size is abnormally enlarged (Fig. 2). The mean size of the adenoid tonsils was statistically larger in the patients with OSAS (13.46 mm) than that in those without this abnormality. There is increased dynamic motion of the airway with increased adenoid size at dynamic MR imaging. Children with enlarged adenoids and OSAS have larger volumes of deep cervical lymph nodes, denoting that enlarged adenoids are a part of larger spectrum of cervical lymphoid hypertrophy. Criteria for recurrent adenoids include regrowth of the adenoid tonsils greater than 12 mm in the midline sagittal plane and association of intermittent collapse of the posterior nasopharynx on dynamic MR imaging.3–6,15,16
Enlarged Palatine Tonsils The palatine tonsils, also referred to as faucial tonsils, are 2 prominent soft tissues, one on each side, located in between the glossopalatine and pharyngopalatine arches. Enlargement of the palatine tonsils is a common cause of OSAS in children. Criteria used for enlargement of the palatine tonsils include prominence of palatine tonsils associated with obstruction of the retroglossal
TABLE 1. Causes of OSAS According to the Level of Obstruction Level
Causes of OSAS
Nasopharynx Oropharynx
Tongue Hypopharynx Larynx Retropharyngeal space Parapharyngeal space Craniofacial structure Associated disorders
Enlarged adenoid tonsils, recurrent adenoid Enlarged palatine tonsil, enlarged lingual tonsils, elongated and/or thickened soft palate Macroglossia, glossoptosis Valecular cyst or mass, hypopharyngeal collapse Elongated epiglottis Infection, benign masses, malignancy Fatty deposition Mandibular hypoplasia, acromegaly Genetic and metabolic disorders
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FIGURE 2. Adenoid tonsil. A and B, Sagittal and axial T2-weighted images in another patient show an enlarged adenoid (arrow) that nearly completely obstructs the nasopharyngeal airway. C, Sagittal gradient–recalled echo MR image shows and enlarged adenoid that narrows the nasopharyngeal airway with prominent soft palate.
FIGURE 3. Palatine tonsil. A, Axial T1-weighted image shows both enlarged palatine tonsils (arrows) with marked narrowing of the pharyngeal airway. B, Parasagittal T2-weighted image in another patient shows an enlarged hyperintense palatine tonsil (arrow) that compromises along the pharyngeal airway.
airway (Fig. 3). The palatine tonsils are an encapsulated organ that is easily surgically removed. There is no recurrent palatine tonsil after palatine tonsillectomy.4–8
Enlarged Lingual Tonsils Normally, the lingual tonsil appears as a small disk of high T2-weighted signal at the posterior aspect of the inferior tongue. When the lingual tonsils enlarged, they appear as a large high T2-signal mass posterior to the tongue often obstructing the velopharynx. Often when they enlarge, the tonsils appear as one large dumbbell-shaped mass rather than 2 discrete lingual tonsils (Fig. 4). The lingual tonsils were noted as markedly enlarged if the anteroposterior diameter is more than 10 mm.17,18
Enlarged and Elongated Soft Palate Normally, the soft palate is isointense to tongue musculature on T2-weighted images. When the soft palate becomes edematous, it becomes high in signal on T2 weighted and thickens (>1 cm). The soft palate thickens in OSAS because of microtrauma from fluttering during snoring. Thickened soft palate contributes to worsening of OSAS by taking up more potential airway space. Criteria to consider a soft palate to be “elongated” include when the soft palate draped over abutting the tongue or soft palate
FIGURE 4. Lingual tonsil. Axial T2-weighted image shows that enlarged lingual tonsils (arrows) appear as a large high T2-signal mass obstructing the retroglossal region of the oropharynx.
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FIGURE 5. Enlarged and elongated soft palate. A, Sagittal T1-weighted image shows an enlarged and prominent soft palate that hangs and abuts the posterior pharyngeal airway with subsequent narrowing. B, Sagittal T2-weighted image in another patient shows an elongated soft palate (long arrow) that reaches to the epiglottis. Note the associated enlarged adenoid (short arrow).
posteriorly positioned abutting the adenoids and obstructing the nasopharynx, and when the soft palate hangs inferiorly, below the midtongue or touches the epiglottis (Fig. 5). These patients are treated with uvulopalatoplasty.4–8,19
Macroglossia Macroglossia is defined as a resting tongue that protrudes beyond the alveolar ridge and the posterior aspect of the tongue sits near the posterior wall of the retroglossal airway, resulting in a consistently narrowed airway. Common causes include hypothyroidism, idiopathic hyperplasia, mucopolysaccharidosis, and chromosomal abnormalities, such as the Beckwith-Wiedeman syndrome and Down syndrome. The tongue may be relatively large in patients who have a small mandible (micrognathia), which is termed as relative macroglossia. An enlarged tongue can fall posteriorly during sleep, obstructing the retroglossal airway. Magnetic resonance imaging is useful in assessing the size of the tongue and the degree of compression along the retroglossal
airway (Fig. 6). Reduction glossectomy has been the main surgical treatment for patients with symptomatic macroglossia.7,8,20
Glossoptosis Glossoptosis is defined as posterior motion of the tongue during sleep. With glossoptosis, the posterior border of the tongue intermittently moves posteriorly and abuts the posterior pharyngeal wall causing obstruction of the retroglossal airway. The presence of glossoptosis is associated with macroglossia, micrognathia, or decreased muscular tone. Populations at risk include those with Down syndrome, cerebral palsy, and PierreRobin syndrome. Dynamic sagittal MR imaging demonstrates the tongue to “fall” posteriorly, abutting the velum and the posterior wall of the pharynx, which causes upper airway obstruction (Fig. 7). In severe glossoptosis, the tongue can also push the soft palate posteriorly, causing intermittent obstruction of the nasopharynx. On axial images obtained at the level of the middle portion of the tongue, the predominant motion is anterior to posterior
FIGURE 6. Macroglossia. A, Axial T1-weighted image shows an enlarged tongue that narrows the pharyngeal airway. B, Sagittal T2-weighted image shows an enlarged tongue that is associated with enlarged adenoids (arrow head) that narrow the nasopharynx, and enlarged soft palate (short arrow) and lingual tonsils (long arrow) that narrow the velopharynx.
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FIGURE 7. Glossoptosis. A, Sagittal gradient–recalled echo MR image during expiration shows the retroglossal airway. B, Sagittal gradient–recalled echo MR image during inspiration shows the posterior aspect of the tongue that moves posteriorly and narrows the retroglossal airway. Note that there are prominent adenoid and soft palate.
motion of the tongue intermittently obstructing the retroglossal airway, whereas the lateral and the posterior aspects of the retroglossal airway remain stable in position.8–21
Hypopharyngeal Collapse Hypopharyngeal collapse is the term given to the collapse of the retroglossal airway that is related to decreased muscular tone. In contrast to glossoptosis where there is abnormal posterior motion of the tongue during sleep, the hypopharyngeal collapse shows the tongue moving posteriorly and the posterior wall of the pharynx moving anteriorly. Certain patients, particularly those with Down syndrome, will have both components of glossoptosis and a floppy airway at risk for hypopharyngeal collapse.7,8
Mandibular hypoplasia may be idiopathic but more commonly associated with certain inherited disorders and syndromes, such as Treacher Collins syndrome, Nager syndrome, Goldenhar syndrome, hemifacial microsomia, trisomies 17-18 and 13-15, Cri Du Chat syndrome, and Pierre Robin sequence. Magnetic resonance imaging is helpful in establishing the size and position of the tongue in relation to the hypoplastic mandible and degree of airway compromise.10,11
Associated Disorders In Down syndrome, there is no true or absolute macroglossia but a relative macroglossia in relation to the size of the oral cavity. Obstructive sleep apnea syndrome occurs in 30% to 60% of patients
Hypopharyngeal and Laryngeal Lesions Valecular cysts of the hypopharynx (Fig. 8) and other soft tissue tumors such as lipoma in the hypopharyngeal region have been associated with OSAS. The larynx can be involved as a site of obstruction, at epiglottis level in most cases. Edema and granulomatous lesions of the epiglottis as scleroma may be associated with OSAS.3,7,9
Fat Deposition in Parapharyngeal Space Excess adipose fatty tissue deposition in the parapharyngeal space may be associated with OSAS.6,8
Retropharyngeal Lesions Soft tissue tumors of the retropharyngeal space such as lipoma and schwannoma (Fig. 9) usually narrow the airway with OSAS. Retropharyngeal abscess associated with bacterial or tuberculous infection may be associated with OSAS. Lastly, bony tumor such as exostosis from the cervical spine may be associated with OSAS.1–7,22
Craniofacial Abnormalities Craniofacial abnormalities such as retrognathia, inferiorly positioned hyoid bone, and maxillary and mandibular retroposition are associated with OSAS. Cephalometry and computed tomographic scan are important for detection of osseous changes; however, MR has a role but of limited value. There is a relationship between surface facial dimensions and upper airway structures measured at MR imaging in patients with OSAS.23,24
FIGURE 8. Valecular cyst. Sagittal T2-weighted image shows a large hyperintense valecular cyst (long arrow) that narrows the hypopharyngeal airway. Note that there are an associated enlarged lingual tonsil (short arrow) that narrows the velopharynx and adenoids (arrow head) that narrow the nasopharyngeal airway.
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FIGURE 9. Retropharyngeal schwannoma. Sagittal contrast T1-weighted image shows a large intense, enhanced oblong solid mass (arrow) obstructing the hypopharyngeal and oropharyngeal airway.
with Down syndrome.25 Congenital conditions affecting craniofacial development such as Chiari, Marfan, Down, and the Pierre Robin syndrome predispose to OSAS.7,8 Endocrinologic conditions such as acromegaly and hypothyroidism are associated with a higher prevalence of OSAS.26
Predictors of Treatment Response and Posttreatment Conservative therapy is usually recommended first because it is noninvasive. Medical sleep centers provide several treatment methods for OSAS such as sleep hygiene, dental splints, and continuous positive airway pressure devices. Although the continuous
positive airway pressure device is the preferred treatment, poor compliance is common. Patients intolerant of conventional medical treatment may benefit from surgical therapy to alleviate pharyngeal obstruction. Tongue reduction surgery included genioglossus advancement, mandibular advancement, and hyoid suspension surgery, which are usually done in patients with retroglossal obstruction. Uvulopalatopharyngoplasty is the surgery usually done in patients with retropalatal obstruction. Maxillomandibular advancement has the highest surgical efficacy (86%) and cure rate (43%). The success of genioglossus advancement ranges from 23% to 77%. Soft palate surgical techniques are less successful, with uvulopalatopharyngoplasty having an OSAS surgical success rate of 50% and a cure rate of 16%.1,4,27 Magnetic resonance imaging is used to predict treatment response and to assess the potential effects or adverse effects of various therapeutic interventions, including surgical and nonsurgical strategies on the upper airway anatomy.1–4,27 Magnetic resonance imaging shows a decrease in the tongue volume in successful medical treatment for patients with OSAS and acromegaly26 and the effect of oral appliance on pharyngeal airway in patients with OSAS28 (Fig. 10). Magnetic resonance imaging demonstrated that the mandibular advancement surgery increases the airway by forward displacement of the entire tongue, and it produces lateral airway expansion via a direct connection between the lateral walls and the ramus of the mandible. Two MR biomarkers that predict response to genioglossus advancement are the relative size of the tongue and adenoid anteroposterior diameter. These findings may help to identify patients with OSA who most likely would benefit from genioglossus advancement surgery. Magnetic resonance imaging assesses changes in the airway after hyoid surgery. In radiofrequency surgery, MR imaging visualizes immediate postoperative effects on the soft tissue of the soft palate and the tongue base.29,30
ADVANTAGE AND LIMITATIONS Magnetic resonance imaging provides an image with excellent contrast of the soft tissue structures in patients with OSAS. A fast MR imaging is able to show the anatomical obstruction dynamically during apnea. Magnetic resonance imaging does not expose patients to ionizing radiation, and it allows imaging in multiple planes. The major limitations of MR imaging are as
FIGURE 10. Obstructive sleep apnea syndrome pretreatment and posttreatment. A, Sagittal T2-weighted image before treatment shows an enlarged and elongated soft palate that narrows the velopharynx (arrow). B, Sagittal T2-weighted image after oral appliance shows a widened velopharynx (arrow).
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follows: long examination time, noisy scanning, claustrophobic effects experienced by many people while in the gantry tube, and high cost. The lack of a comfortable sleep environment also limits the ability to use MR imaging during sleep.4–8
SUMMARY AND CONCLUSION Magnetic resonance imaging is essential for diagnosis and treatment planning of OSAS because it can detect the level, degree, and causes of the upper airway obstruction. It has a role in prediction treatment response and monitoring of patients with OSAS after therapy. REFERENCES 1. Kendzerska T, Mollayeva T, Gershon AS, et al. Untreated obstructive sleep apnea and the risk for serious long-term adverse outcomes: a systematic review. Sleep Med Rev. 2014;18:49–59. 2. Mannarino M, Di Filippo F, Pirro M. Obstructive sleep apnea syndrome. Eur J Intern Med. 2012;23:586–593. 3. Simon S, Collop N. Latest advances in sleep medicine: obstructive sleep apnea. Chest. 2012;142:1645–1651. 4. Strauss R, Burgoyne C. Diagnostic imaging and sleep medicine. Dent Clin North Am. 2008;52:891–915. 5. Junior C, Filho H, Gomes C, et al. Radiological findings in patients with obstructive sleep apnea. J Bras Pneumol. 2013;39:98–101.
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27. Freedman N. Treatment of obstructive sleep apnea syndrome. Clin Chest Med. 2010;31:187–201. 28. Fleck RJ, Mahmoud M, McConnell K, et al. An adverse effect of positive airway pressure on the upper airway documented with magnetic resonance imaging. JAMA Otolaryngol Head Neck Surg. 2013;139: 636–638. 29. Choudhury M, Padmanabhan TV. A preliminary report on the effect of a mandibular advancement device on obstructive sleep apnea using magnetic resonance imaging and polysomnography. Int J Prosthodont. 2012;25: 613–618. 30. Schaaf W, Wootten C, Donnelly L, et al. Findings on MR sleep studies as biomarkers to predict outcome of genioglossus advancement in the treatment of obstructive sleep apnea in children and young adults. AJR Am J Roentgenol. 2010;194:1204–1209.
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