The Laryngoscope C 2014 The American Laryngological, V

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Sleep Magnetic Resonance Imaging with Electroencephalogram in Obstructive Sleep Apnea Syndrome Pavel Kavcic, MD; Ales Koren, MD, PhD; Blaz Koritnik, MD, PhD; Igor Fajdiga, MD, PhD; Leja Dolenc Groselj, MD, PhD Objective: To evaluate the mechanism and level of upper airway obstruction in obstructive sleep apnea (OSA) patients during natural sleep, together with synchronous electroencephalogram and respiratory events registration at 3-Tesla magnetic resonance imaging (MRI) platform with high spatial and temporal resolution. Study Design: A prospective cohort study of 20 randomly selected OSA patients. Methods: Fifteen of 20 patients were able to complete spontaneous sleep during MRI. While asleep, dynamic MR images of pharynx were obtained in the midline sagittal view. During the scan, nasal and oral airflow, thoracoabdominal wall effort, and electroencephalogram were synchronously recorded. The physiologic data were retrospectively scored to identify periods of apneas and synchronized with dynamic MR images. Results: In all 15 patients, the site of complete airway obstruction occurred at the retropalatal space. We noticed different positions of the soft palate during apneic events. In seven of 15 patients (47%), the soft palate was attached to the tongue base and moved backward, compressing the airway. In five of 15 patients (33%), the soft palate was detached from the tongue base and solely moved backward, compressing the airway. In three patients (20%), we recorded both mechanisms of complete airway obstruction. In cases with attached soft palate to the tongue base, we noticed significant narrowing of the retrolingual space during apneic events. Conclusion: We describe a novel mechanism of obstruction dependent on the position of soft palate. This mechanism might play an important role in selecting candidates for surgery or treatment with hypoglossal nerve stimulation. Key Words: Magnetic resonance imaging, obstructive sleep apnea, soft palate, hypoglossal nerve stimulation. Level of Evidence: 2b. Laryngoscope, 00:000–000, 2014

INTRODUCTION Obstructive sleep apnea (OSA) represents the most common sleep-related breathing disorder, with a prevalence of 3% to 9% of women and 10% to 17% of men in the United States.1 The gold standard for diagnosis of OSA is overnight polysomnography (PSG), which is limited in that it does not provide any information regarding the site of upper airway obstruction during sleep. Continuous positive airway pressure (CPAP) is a highly effective first-line medical therapy; however, it is often poorly tolerated with low compliance rates.2 Treatment alternatives are surgical and other minimally invasive therapies. Surgery has relatively low success rates, with several adverse effects in the management of OSA patients.3 Recently, a new

From the Clinical Radiology Institute (P.K., A.K.); the Institute of Clinical Neurophysiology, Division of Neurology, University Medical Centre Ljubljana (B.K., L.D.G.); the Department of Neurology, Faculty of Medicine (B.K.); and the Clinic of Otorhinolaryngology and Cervicofacial Surgery (I.F.), University Medical Centre Ljubljana, Ljubljana, Slovenia. Editor’s Note: This Manuscript was accepted for publication November 13, 2014. The authors have no funding, financial relationships, or conflicts of interest to disclose. Send correspondence to Pavel Kavcic, MD, Clinical Radiology Institute, University Medical Centre, Ljubljana, Zaloska 7, 1000 Ljubljana, Slovenia. E-mail: [email protected] DOI: 10.1002/lary.25085

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promising treatment with stimulation of the hypoglossal nerve was reported to show significant reduction in the severity of OSA and self-reported sleepiness at year 1. Response rates were similar to CPAP treatment and higher compared to surgical outcomes.4 However, no effect of the hypoglossal nerve stimulation was reported in patients with palatal complete concentric collapse.5 The mechanism and level of upper airway obstruction plays an important role in selecting candidates for surgery and treatment with hypoglossal nerve stimulation.6 A better understanding of patterns of upper airway obstruction in OSA patients could help target treatment. Previous studies have shown that dynamic magnetic resonance imaging (MRI) can accurately assess the dynamic changes and site of upper airway obstruction in OSA patients.7–9 Sleep MRI as a new diagnostic tool was introduced, which simultaneously evaluates airway obstruction and respiratory events in real time during natural sleep.10,11 Thus far, only one study described a combined assessment of OSA patients with dynamic MRI and parallel electroencephalogram (EEG) registration during natural sleep.12 An important disadvantage of previous MRI studies was low spatial resolution, making image analysis difficult and imprecise. Recently, a new dedicated sleep MRI platform at 3 Tesla (T) was introduced, which allowed sleep maintenance despite the constant noise in the scanner.13 Kavcic et al.: Sleep MRI with EEG in OSAS

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In this study, we wanted to combine the advantages of previous dynamic MRI studies in OSA patients. The aim was to evaluate the mechanism and level of upper airway obstruction in real time during natural sleep, together with synchronous EEG and respiratory events registration at a 3T platform with high spatial and temporal resolution.

MATERIALS AND METHODS Subjects Twenty patients with a clinical and polysomnographic diagnosis of OSA were ascertained from the Sleep Centre of the Institute of Clinical Neurophysiology, University Medical Centre, Ljubljana, Slovenia. Inclusion criteria were moderate or severe OSA (AHI > 15) at diagnosis, with overnight PSG, age over 18 years, and no prior upper airway surgery or CPAP treatment. Exclusion criteria were a body mass index (BMI) greater than 40 kg/m2 and contraindications to MRI (including pacemaker, metallic implants, claustrophobia). Fifteen patients (13 men and 2 women) were able to complete spontaneous sleep during MRI and therefore were eligible for the study; the mean age of the cohort was 48.9 years (range, 21–65 years), the mean BMI was 34.6 kg/m2 (range, 26–40 kg/m2), and the mean apnea/ hypopnea index (AHI) was 60.5 (range, 15–97). Three patients in the cohort had moderate OSA (AHI 15–30), and 12 patients had severe OSA (AHI > 30). Four subjects were unable to complete spontaneous sleep due to the noise of MRI, and one subject developed claustrophobia. No patient received any treatment before MRI examination. All study subjects were refrained from sleep for 12 hours prior to imaging and were not allowed to ingest alcohol or sedatives on the day of the procedure. No pharmaceutical sedation was administered to facilitate sleep onset. Informed consent was obtained from all patients, and the study was approved by The National Medical Ethics Committee of the Republic of Slovenia.

Polysomnography All patients underwent a full, overnight, in-laboratory, technician-attended PSG assessment, which was recorded on a commercial PSG system (Nicolet One nEEG, Neurocare, Madison, WI) using standard PSG settings.14 The recording included EEG, electrooculography, chin surface electromyogram, electrocardiogram, nasal pressure (nasal pressure cannula), respiratory movements (chest and abdominal belts), oxyhemoglobin saturation (Nellcor Pulse Oximeter, OxismartXL, CovidienNellcor, Boulder, CO), and continuous video monitoring. On awakening the next morning, all subjects underwent arterial gas analysis (Gas Lyte sampler, Vital signs, Totowa, NJ). All recordings were visually analyzed, and the AHI was scored by a sleep expert, following the European Sleep Research Society guidelines and the American Association for Sleep Medicine guidelines.14,15

Magnetic Resonance Imaging Patients were scanned after 8 PM under continuous supervision by a radiologist. MRI was performed on a 3T MRI scanner (Magnetom Trio; Siemens, Erlangen, Germany) using a head and neck surface coil. Patients were allowed to sleep in a supine position with only their head in a neutral position; that is, the Frankfort plane perpendicular to horizontal. Head position was secured using a soft padding material between the head and coil. Acoustic scanner noise was attenuated with

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white noise headphones and earplugs. The lights in the room were turned off to facilitate sleep. While awake, patients were scanned using a T1 turbo spin-echo (TSE) sequence (time to repetition/time to echo [TR/ TE] 400/12) in transversal plane spanning from the roof of the nasal cavity to the trachea. Technical parameters were: field of view (FOV) of 20 3 20 cm; 512 3 512 matrix with a pixel resolution of 0.86 mm 3 0.86 mm; slice thickness of 2 mm and zero spacing between the slices. Each subject was allowed to fall and remain asleep for up to 2 hours while continuous real-time dynamic imaging was performed. During sleep, single-slice images were obtained in the midline sagittal view from the forebrain to the upper-third of the trachea using a T1 TSE sequence (TR/TE 200/26); FOV of 20 3 22 cm; matrix 232 3 256; slice thickness 10 mm. The imaging time for each image was 5 seconds. In five patients, we additionally performed fast gradientecho cine sequence (TR/TE 45.3/2.7); FOV of 20 3 22 cm; matrix 170 3 208; slice thickness 6 mm with the imaging time 1 fps. EEG was recorded continuously during MRI scanning using a Brain Vision system with a 64-channel MR compatible electrode cap BrainCap MR and BrainAmp MR amplifiers (Brain Products, Munich, Germany). The EEG data were sampled at 5 kHz with 0.016 to 250 Hz filters, synchronized with a 10-MHz MRI scanner clock using the SyncBox (Brain Products). Impedance at all electrodes was kept below 20 kX. MRI gradient and cardioballistic artifacts were removed offline using the Brain Vision Analyzer 2 software (Brain Products). During the scan, other physiological parameters were also synchronously recorded: nasal and oral airflow, thoracoabdominal wall effort (Nicolet One nEEG, Neurocare, Madison, WI) and pulse rate with oxygen saturation (Nellcor Pulse Oximeter; OxismartXL, Covidien-Nellcor, Boulder, CO). The physiologic data were retrospectively scored to identify periods of apneas and synchronized with dynamic MRI. The onset of sleep was recognized by detection of stage 1 or 2 nonrapid eye movement sleep EEG findings.14 Periods of apnea lasting longer than 10 seconds in the airstream monitor were used as a criterion for apnea. Anatomically, we divided oropharynx to the retropalatal space, which extends from the hard palate to the inferior border of the uvula, and the retrolingual space, which extends from the inferior border of the uvula to the superior border of the epiglottis. An airway obstruction was defined as a complete occlusion of upper airway for at least 10 seconds. While sleeping, we measured the minimum retrolingual diameter in an anteroposterior direction during breathing and during apnea. Measurements during apnea were done at the same level as during breathing. The images were reviewed by two radiologists, and conclusions were reached by consensus.

Statistical Analysis Neck circumference, BMI, AHI, and retrolingual diameter results are expressed as mean 6 standard deviation. Neck circumference, BMI, and AHI data were compared between two groups with different patterns of upper airway obstruction by a two-tailed t test. Retrolingual diameter data were compared by a two-tailed paired t test. A P value < 0.05 was recognized as statistically significant.

RESULTS In all 20 patients, on-line EEG registration was feasible in the magnetic field. MRI was performed in 19 patients, excluding the one with newly found Kavcic et al.: Sleep MRI with EEG in OSAS

Fig. 1. Midline sagittal magnetic resonance images of open (A) and complete upper airway obstruction at the retropalatal level (B). Soft palate is attached to the tongue base and together with it moves backward, compressing the airway. Note the significant narrowing of the retrolingual space (white line).

claustrophobia. Typical EEG findings for sleep periods were present in 15 of 19 patients during MR imaging. Average sleeping time was 27 minutes, 33 seconds, per patient (range, 10 minutes 25 seconds–35 minutes 1 second). All 15 patients showed light sleep stages (1 or 2), no patient showed deep sleep stages (3 or 4) or REM sleep. In all 15 patients who were able to complete spontaneous sleep, the nasal and oral airflow detector showed multiple apneic events. During apneic events, paradoxical breathing was registered by a thoracoabdominal strain gauge,

which is characteristic for OSA. In the remaining four patients who did not manage to fall asleep in the scanner, the nasal and oral airflow detector showed no apneic events. While awake, none of the patients showed signs of upper airway obstruction on MR images. Notably, in all 15 patients with polysomnographically-detected sleep and apneic events, MRI successfully showed the site of complete airway obstruction. Average MRI recording time was 10 minutes, 13 seconds, per patient (range,

Fig. 2. Midline sagittal magnetic resonance images of open (A) and complete upper airway obstruction at the retropalatal level (B). Soft palate is detached to the tongue base and solely moves backward, compressing the airway. There is no narrowing of the retrolingual space (white line).

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Fig. 3. Midline sagittal magnetic resonance images showing two types of complete airway obstruction: open airway (A), obstruction with soft palate attached (B) or detached (C) to the tongue base. Note the significant narrowing of the retrolingual space in the first type and no narrowing in the second type of obstruction (white line).

5 minutes 10 seconds–20 minutes 52 seconds). We recorded 3.3 apneas per patient (range, 1–8). In all patients, the site of complete obstruction occurred in the retropalatal space; no patient had an obstruction at the retrolingual space or a multiple level obstruction. Furthermore, we analyzed the position of soft palate during apneic events. In seven of 15 patients (47%), the soft palate was attached to the tongue base and together with it moved backward, compressing the airway (Figs. 1A and 1B). In five of 15 patients (33%), the soft palate was detached to the tongue base and solely moved backward, compressing the airway (Figs. 2A and 2B). In three patients (20%), we recorded both mechanisms of complete airway obstruction; the soft palate was either attached or detached to the tongue base during apneic events (Figs. 3A, 3B, and 3C).16 In cases with an attached soft palate to the tongue base (n 5 7 1 3), we noticed a significant narrowing of the retrolingual space in an anteroposterior direction. During apneic events, the retrolingual space narrowed from 12.4 6 2.8 mm to 9.3 6 3.2 mm (P 5 0.002). In cases with detached soft palate to the tongue base during apneic events (n 5 5 1 3), the retrolingual space narrowed from 12.3 6 3.7 mm to 11.1 6 4.6 mm, no significant difference (P 5 0.21). Data for each subject are shown in Table I. We found no statistically significant differences in neck circumference, BMI, and AHI between the group with an attached soft palate and the group with a detached soft palate to the tongue base during apneic events. Neck circumference was 46.0 6 3.4 cm in the first group and 47.2 6 2.2 cm in the second group (P 5 0.62). BMI was 33.3 6 4.0 kg/m2 in the first group and 37.2 6 2.2 kg/m2 in the second group (P 5 0.08). AHI was 49.6 6 29.7 in the first group and 74.8 6 7.7 in the second group (P 5 0.10).

DISCUSSION This MRI study demonstrated the precise site of upper airway obstruction, together with synchronous Laryngoscope 00: Month 2014

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EEG and respiratory events registration, during natural sleep in OSA patients. All patients who were able to complete spontaneous sleep were found to be in light sleep (stage 1 and 2) during imaging. Nasal and oral airflow reductions were coincident with the airway obstructions seen on the MRI. The MRI showed persistent isolated obstruction at the retropalatal level in all 15 cases. Findings confirm previous observations that retropalatal space is the most common site of upper airway obstruction in OSA patients.8,11,17,18 We did not find any complete obstruction at the retrolingual level, as described in previous imaging studies.17–20 Close inspection of our patients revealed that the base of the tongue was not in contact with the retropharyngeal wall during apneic events. We did not perform axial images during sleep and may have missed some retrolingual stenosis due to the lateral wall collapse. Notably, it was previously shown that lateral wall collapse can have an important role in the pathogenesis of OSA.13,20 In our study, we have used only medial sagittal images for which both the retropalatal and retrolingual space can be easily visualized together. Also, we may have not detected retrolingual obstructions because none of our patients achieved deep sleep (stage 3 or 4) during imaging. Ultralow-field MRI study of OSA patients showed that the obstruction site varies in different sleep stages. The airway obstruction extended from palatopharynx at sleep onset to glossopharynx during REM sleep.21 The majority of sleep MRI studies were done on patients undergoing drug-induced sleep.17,18,20,22–24 Medications for inducing sleep can have variable inhibitory effects on ventilatory drive and airway muscle tone, thereby potentially producing false positive obstructions and overestimation of obstruction sites. According to the current literature, snoring and airway obstruction can be observed and induced in 79% to 95% of all manually sedated patients.25 In the few MRI studies of OSA patients in spontaneous sleep, the retropalatal space was found to be by far the most frequent level of Kavcic et al.: Sleep MRI with EEG in OSAS

TABLE I. Demographic Data, Type of Obstruction, and Retrolingual Space Diameter for Each Subject. Retrolingual Space Diameter in Anteroposterior Direction (mm) Neck Circumference (cm)

BMI

AHI

Type of Retropalatal Obstruction

1

49

39

70

2 3

50 49

37 40

61 64

4

44

40

5 6

43 48

7 8 9

Subject

Sleep/Open Airway

Apnea

D

17.5

12.2

A D

16 9.6

16 8.9

75

A1D

15.3

7.8*/16.7†

32 36

32 78

A D

9.4 16.7

5 17.5

49

34

97

A

13.2

11

48 47

31 37

69 55

A A

11.5 16.4

10.4 12

10

44

36

15

A

8.6

8.2

11 12

46 41

36 28

83 28

D A1D

10 10

6 6.6*/11.1†

13

42

31

83

A1D

11.8

6.5*/11.9†

14 15

41 44

26 35

18 79

A D

11.9 7.7

9.6 4.2

*Retrolingual space diameter with soft palate attached to the tongue base. † Retrolingual space diameter with soft palate detached to the tongue base. A 5 soft palate attached to the tongue base; AHI 5 apnea-hypopnea index; BMI 5 body mass index; D 5 soft palate detached to the tongue base.

obstruction,11 indicating that drug-induced sleep might produce false positive obstructions at the retrolingual level. Also, combined obstructions were found to be a much more frequent finding in drug-induced sleep endoscopy than endoscopy during natural sleep.25 In cases for which soft palate was attached to the tongue base during apneic events, we noticed a significant narrowing of the retrolingual space. However, there was no narrowing of the retrolingual space in cases with detached soft palate to the tongue base. Close examination of three patients with both mechanisms of complete airway obstruction revealed that all three had significant narrowing of the retrolingual space while soft palate was attached to the tongue base and no narrowing while soft palate was detached to the tongue base. Therefore, it can be speculated that narrowing is a consequence of the soft palate pulling the tongue backward due to a surface tension mechanism. The narrowing of the retrolingual space might also be misinterpreted as a retrolingual obstruction if the spatial resolution is low or when a narrowing greater than 50% is defined as obstruction.11 Interestingly, in previous imaging studies retrolingual obstruction was always combined with the retropalatal obstruction; no subject showed isolated retrolingual obstruction.11,17,20,22 We describe a type of airway obstruction for which the soft palate detaches from the base of the tongue and solely moves backward to the posterior pharyngeal wall, compressing the airway. This type of obstruction was previously reported.26 The mechanism is challenging to explain because we would expect soft palate to detach from the posterior pharyngeal wall when the patient tries to inhale. We believe that an increased surface Laryngoscope 00: Month 2014

tension mechanism may have a role in the strong attachment of the soft palate to the posterior pharyngeal wall. The soft palate and the pharyngeal mucosa normally have a low surface tension due to saliva production by their own accessory glands. Interestingly, OSA patients often experience dry mouth upon awakening due to a lack of saliva.27 This dry mouth might be explained by mouth breathing or by reduction in saliva production. OSA patients were shown to have increased levels of sympathetic nervous system activity28 and reduced vagal tone,29 which may reduce saliva production and increase surface tension of the upper airway liquids that contribute to the upper airway obstruction.30 There is a distinct group of patients who do not respond to hypoglossal nerve stimulation.4,5 Hypoglossal nerve stimulation produces anterior displacement of the tongue, thus enlarging retrolingual space. We assume that this type of treatment might not be beneficial in patients with isolated retropalatal obstruction for which soft palate is detached from the base of the tongue, as we describe here. In a study by Strollo et al., druginduced sleep endoscopy was performed in three patients with a large increase of AHI after stimulation; it showed closed retropalatal airway despite the elimination of tongue base collapse.4 In a study by Vanderveken et al., hypoglossal nerve stimulation was not effective in patients with palatal complete concentric collapse, whereas it was effective in patients with both anteroposterior palatal and tongue base collapse.5 A possible explanation might be that when soft palate is attached to the tongue base, the hypoglossal nerve stimulation is effective by keeping the tongue base together with the attached soft palate in an anterior position. Kavcic et al.: Sleep MRI with EEG in OSAS

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The limitations to our study are the relatively small sample size and the fact that none of our patients achieved deep sleep in the scanner. Noisy and claustrophobic environment of sleep MRI is probably the reason why none of the patients achieved spontaneous deep sleep. Another disadvantage of sleep MRI is the fact that the patient is limited to the supine position only. Despite initial head positioning in neutral position, we noticed slight neck extension in few patients during sleep, which might also affect upper airway collapsibility. Sleep MRI is not an alternative to PSG, but an additional test that provides important information about dynamic characteristics of upper airway obstruction.

CONCLUSION This dynamic MRI study, with synchronous EEG and respiratory events registration during natural sleep in OSA patients, showed that complete airway obstructions were isolated to the retropalatal level. We described a novel mechanism of obstruction that is dependent on the position of the soft palate. This mechanism might play an important role in selecting candidates for surgery or treatment with hypoglossal nerve stimulation.

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Kavcic et al.: Sleep MRI with EEG in OSAS

Sleep magnetic resonance imaging with electroencephalogram in obstructive sleep apnea syndrome.

To evaluate the mechanism and level of upper airway obstruction in obstructive sleep apnea (OSA) patients during natural sleep, together with synchron...
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