pii: jc- 00172-16http://dx.doi.org/10.5664/jcsm.6290
CAS E R EPOR T S
Case Study: Imaging of Apnea Termination in a Patient with Obstructive Sleep Apnea during Natural Sleep Elizabeth Brown, PhD1,2; Lynne Bilston, PhD1 Neuroscience Research Australia (NeuRA) and University of New South Wales; 2Prince of Wales Hospital, NSW, Australia
1
A 55-year-old woman who presented to the sleep clinic with severe sleep apnea (OSA) (apnea-hypopnea index [AHI] 62) and excessive somnolence (Epworth Sleepiness Scale score 18/24), was imaged with MRI using the Spatial Modulation of Magnetization tagging sequence awake and asleep to visualize upper airway tissue movement. Awake quiet breathing resulted in minimal movement of upper airway tissues. Asleep sequences taken during airway opening post-apnea demonstrated neck extension, mandibular advancement, and widespread tongue deformation accompanying contraction of genioglossus. At the end of the asleep image sequence, the nasopharyngeal airway had a cross-sectional area larger than during quiet breathing awake and there was antero-lateral movement in the lateral walls. In conclusion, the airway responds to apnea by widespread contraction of the genioglossus, followed by mandibular advancement and neck extension. All these maneuvers stabilize and open the airway. Keywords: apnea, upper airway opening, MRI, genioglossus, mandibular advancement, extension Citation: Brown E, Bilston L. Case study: imaging of apnea termination in a patient with obstructive sleep apnea during natural sleep. J Clin Sleep Med 2016;12(11):1563–1564.
R E P O R T O F CAS E A 55-year-old woman presented to the sleep clinic with snoring, witnessed apneas, and excessive somnolence (Epworth Sleepiness Scale score 18/24). Standard polysomnogram demonstrated an apnea hypopnea index (AHI) of 62 and oxygen saturation below 90% for 1% of sleep time, consistent with severe obstructive sleep apnea (OSA). Informed consent and MRI safety clearance were obtained. The experimental aim was to capture upper airway muscle movements awake during inspiration and asleep during reopening post-apnea with the Spatial Modulation of Magnetization tagging technique, which has been published elsewhere.1 Briefly, it involves the laying down of a grid of saturated magnetization (see Figure 1) prior to ultra-fast imaging. The grid, which appears black, moves with the tissue, so that respiratory-related tissue movement can be visualized. The subject was chosen because of very excessive somnolence to increase the likelihood of sleep in the scanner and was allowed to fall asleep naturally in the scanner. The subject was assessed for sleep by the presence of irregular breathing, audible snoring, non-response to verbal communication, and self-report. We explored the possibility of EEG in the scanner, but EEG in the MRI is very difficult to analyze because the magnetic field gradients produce EEG artifacts due to induced currents in EEG wires. Cephalometric analysis of the mandible relative to the skull (cephalometric angle SN-B) pre and post apnea was measured (as described previously1 ). With the subject drowsy but awake, 3 sagittal sequences taken immediately prior to inspiration showed minimal dilatory genioglossus movement. This is in contrast to the image sequences taken asleep during airway opening post-apnea, where 2 sagittal image sequences which captured apnea termination showed 1563
neck extension, mandibular advancement, and widespread tongue deformation due to contraction of genioglossus (Figure 1 and Video 1 in the supplemental material). Nasopharyngeal genioglossus moved first then the mandible advanced and then the head extended. The posterior genioglossus moved infero-anteriorly, then superiorly. Post-apnea movement of the genioglossus was not only qualitatively different but also larger than airway dilation associated with awake inspiration (1.2 mm vs 0.04 mm). The mandible advanced on average 3.0 mm and the tip of the nose moved superiorly 1.9 mm. SN-B increased by 4 degrees post apnea, confirming the mandible moved independently of head extension. A third sequence timed to coincide with apnea termination showed a swallow and was not analyzed. Axial images confirmed the subject had complete nasopharyngeal and oropharyngeal airway obstruction during apnea (Figure 1). At the end of airway opening, the average nasopharyngeal crosssectional area (CSA) of 2 sequences of apnea termination was larger than during awake quiet breathing (312 mm² vs 105 mm2 ). In the axial plane, the lateral airway walls moved laterally similar to previous imaging observations during passive mandibular advancement,2 with antero-lateral movement in the region of the pterygomandibular raphe. Other tissues in the nasopharyngeal plane moved anteriorly or antero-medially. D I SCUS S I O N Multiple airway dilator mechanisms are activated at apnea termination. Imaging of a sleeping severe OSA patient during airway reopening showed strong contraction of genioglossus, mandibular protrusion, and neck extension, with more widespread activation of the tongue muscles than during awake Journal of Clinical Sleep Medicine, Vol. 12, No. 11, 2016
E Brown and L Bilston. Imaging Apnea Termination
have not been seen in previous awake imaging. The rotational movement of genioglossus at apnea termination observed is in contrast to the predominantly anterior movement during wakeful quiet breathing in both normal subjects and OSA patients recorded previously.1 Very severe OSA subjects, including this subject, typically have minimal movement of genioglossus throughout the respiratory cycle during wakefulness, despite phasic activation of the genioglossus.1 However previous EMG studies have shown strong activation of genioglossus during apnea termination3 consistent with the motion observed here. Also post-apnea nasopharyngeal CSA increased around four times the initial awake CSA, consistent with previous data showing greater airflow at the end of apnea associated with cortical arousal.3 The large response may indicate that a high stimulus is required to initiate movement, but once opening begins the dilation is greater than needed to restore airflow. Mandibular advancement may stabilize the upper airway as it decreases the tissue pressure in both the anterior and lateral compartments of the airway4 and also increases the lateral dimensions of the airway.2,5 It is not surprising that neck extension was observed at the termination of apnea as neck extension increases oropharyngeal airway size and reduces airway wall compliance.6 These images show that in sleep postural mechanisms are used as part of opening the airway after an apnea. These maneuvers help to stabilize and open the airway.
Figure 1—The movement of upper airway opening at apnea termination as a sequence of 6 tagged images each 250 ms apart in 3 planes. Sagittal plane
* Nasopharnygeal plane
R E FE R E N CES 1. Brown EC, Cheng S, McKenzie DK, Butler JE, Gandevia SC, Bilston LE. Respiratory movement of upper airway tissue in obstructive sleep apnea. Sleep 2013;36:1069–76. 2. Brown EC, Cheng S, McKenzie DK, Butler JE, Gandevia SC, Bilston LE. Tongue and lateral upper airway movement with mandibular advancement. Sleep 2013;36:397–404. 3. Jordan A, Eckert DJ, Wellman A, Trinder JA, Malhotra A, White DP. Termination of respiratory events with and without cortical arousal in obstructive sleep apnea. Am J Respir Crit Care Med 2011;184:1183–119. 4. Kairaitis K, Stavrinou R, Parikh R, Wheatley J, Amis T. Mandibular advancement decreases pressures in the tissues surrounding the upper airway in rabbit. J Appl Physiol 2006;100:349–56. 5. Isono S, Tanaka A, Sho Y, Konno A, Nishino T. Advancement of the mandible improves velopharyngeal airway patency. J Appl Physiol 1995;79:2132–8. 6. Walsh JH, Maddison KJ, Platt PR, Hillman DR, Eastwood PR. Influence of head extension, flexion, and rotation on collapsibility of the passive upper airway. Sleep 2008;31:1440–7.
Oropharyngeal plane
The arrowheads indicate the position of the airway while collapsed. The arrow indicates approximately the original (dashed line) and final position (no dash) of the maxillary plane. The asterisk indicates the original position of the mandible in the sagittal plane. Video of the airway opening in the sagittal plane is available in supplemental material.
SUBM I SSI O N & CO R R ESPO NDENCE I NFO R M ATI O N
quiet breathing. At apnea termination, there was a coordinated airway opening response involving genioglossus, mandibular advancement (possibly via activation of superficial fibers of masseter and pterygoid muscles), and neck extensors. This is reminiscent of the “triple airway maneuver” (neck extension, mandibular protrusion, and mouth opening) used to stabilize the airway during anesthesia. These images show that airway reopening involves more than airway dilators. Head movement and mandibular advancement Journal of Clinical Sleep Medicine, Vol. 12, No. 11, 2016
1564
Submitted for publication April, 2016 Submitted in final revised form June, 2016 Accepted for publication July, 2016 Address correspondence to: Professor Lynne Bilston, Neuroscience Research Australia, Barker St, Randwick, NSW 2031 Australia; Tel: +61-2-9399-1673; Fax: +61-2-9399-1027; Email: [email protected]
D I SCLO S U R E S TAT E M E N T This was not an industry supported study. This research was supported by an NHMRC project Grant 455228. Dr. Bilston is supported by an NHMRC fellowship. Dr. Bilston has received consulting income from Linguaflex LLC not related to this study. Dr. Brown has indicated no financial conflicts of interest. All research was conducted at Neuroscience Research Australia
CAS E R EPOR T S
Case Study: Imaging of Apnea Termination in a Patient with Obstructive Sleep Apnea during Natural Sleep Elizabeth Brown, PhD1,2; Lynne Bilston, PhD1 Neuroscience Research Australia (NeuRA) and University of New South Wales; 2Prince of Wales Hospital, NSW, Australia
1
A 55-year-old woman who presented to the sleep clinic with severe sleep apnea (OSA) (apnea-hypopnea index [AHI] 62) and excessive somnolence (Epworth Sleepiness Scale score 18/24), was imaged with MRI using the Spatial Modulation of Magnetization tagging sequence awake and asleep to visualize upper airway tissue movement. Awake quiet breathing resulted in minimal movement of upper airway tissues. Asleep sequences taken during airway opening post-apnea demonstrated neck extension, mandibular advancement, and widespread tongue deformation accompanying contraction of genioglossus. At the end of the asleep image sequence, the nasopharyngeal airway had a cross-sectional area larger than during quiet breathing awake and there was antero-lateral movement in the lateral walls. In conclusion, the airway responds to apnea by widespread contraction of the genioglossus, followed by mandibular advancement and neck extension. All these maneuvers stabilize and open the airway. Keywords: apnea, upper airway opening, MRI, genioglossus, mandibular advancement, extension Citation: Brown E, Bilston L. Case study: imaging of apnea termination in a patient with obstructive sleep apnea during natural sleep. J Clin Sleep Med 2016;12(11):1563–1564.
R E P O R T O F CAS E A 55-year-old woman presented to the sleep clinic with snoring, witnessed apneas, and excessive somnolence (Epworth Sleepiness Scale score 18/24). Standard polysomnogram demonstrated an apnea hypopnea index (AHI) of 62 and oxygen saturation below 90% for 1% of sleep time, consistent with severe obstructive sleep apnea (OSA). Informed consent and MRI safety clearance were obtained. The experimental aim was to capture upper airway muscle movements awake during inspiration and asleep during reopening post-apnea with the Spatial Modulation of Magnetization tagging technique, which has been published elsewhere.1 Briefly, it involves the laying down of a grid of saturated magnetization (see Figure 1) prior to ultra-fast imaging. The grid, which appears black, moves with the tissue, so that respiratory-related tissue movement can be visualized. The subject was chosen because of very excessive somnolence to increase the likelihood of sleep in the scanner and was allowed to fall asleep naturally in the scanner. The subject was assessed for sleep by the presence of irregular breathing, audible snoring, non-response to verbal communication, and self-report. We explored the possibility of EEG in the scanner, but EEG in the MRI is very difficult to analyze because the magnetic field gradients produce EEG artifacts due to induced currents in EEG wires. Cephalometric analysis of the mandible relative to the skull (cephalometric angle SN-B) pre and post apnea was measured (as described previously1 ). With the subject drowsy but awake, 3 sagittal sequences taken immediately prior to inspiration showed minimal dilatory genioglossus movement. This is in contrast to the image sequences taken asleep during airway opening post-apnea, where 2 sagittal image sequences which captured apnea termination showed 1563
neck extension, mandibular advancement, and widespread tongue deformation due to contraction of genioglossus (Figure 1 and Video 1 in the supplemental material). Nasopharyngeal genioglossus moved first then the mandible advanced and then the head extended. The posterior genioglossus moved infero-anteriorly, then superiorly. Post-apnea movement of the genioglossus was not only qualitatively different but also larger than airway dilation associated with awake inspiration (1.2 mm vs 0.04 mm). The mandible advanced on average 3.0 mm and the tip of the nose moved superiorly 1.9 mm. SN-B increased by 4 degrees post apnea, confirming the mandible moved independently of head extension. A third sequence timed to coincide with apnea termination showed a swallow and was not analyzed. Axial images confirmed the subject had complete nasopharyngeal and oropharyngeal airway obstruction during apnea (Figure 1). At the end of airway opening, the average nasopharyngeal crosssectional area (CSA) of 2 sequences of apnea termination was larger than during awake quiet breathing (312 mm² vs 105 mm2 ). In the axial plane, the lateral airway walls moved laterally similar to previous imaging observations during passive mandibular advancement,2 with antero-lateral movement in the region of the pterygomandibular raphe. Other tissues in the nasopharyngeal plane moved anteriorly or antero-medially. D I SCUS S I O N Multiple airway dilator mechanisms are activated at apnea termination. Imaging of a sleeping severe OSA patient during airway reopening showed strong contraction of genioglossus, mandibular protrusion, and neck extension, with more widespread activation of the tongue muscles than during awake Journal of Clinical Sleep Medicine, Vol. 12, No. 11, 2016
E Brown and L Bilston. Imaging Apnea Termination
have not been seen in previous awake imaging. The rotational movement of genioglossus at apnea termination observed is in contrast to the predominantly anterior movement during wakeful quiet breathing in both normal subjects and OSA patients recorded previously.1 Very severe OSA subjects, including this subject, typically have minimal movement of genioglossus throughout the respiratory cycle during wakefulness, despite phasic activation of the genioglossus.1 However previous EMG studies have shown strong activation of genioglossus during apnea termination3 consistent with the motion observed here. Also post-apnea nasopharyngeal CSA increased around four times the initial awake CSA, consistent with previous data showing greater airflow at the end of apnea associated with cortical arousal.3 The large response may indicate that a high stimulus is required to initiate movement, but once opening begins the dilation is greater than needed to restore airflow. Mandibular advancement may stabilize the upper airway as it decreases the tissue pressure in both the anterior and lateral compartments of the airway4 and also increases the lateral dimensions of the airway.2,5 It is not surprising that neck extension was observed at the termination of apnea as neck extension increases oropharyngeal airway size and reduces airway wall compliance.6 These images show that in sleep postural mechanisms are used as part of opening the airway after an apnea. These maneuvers help to stabilize and open the airway.
Figure 1—The movement of upper airway opening at apnea termination as a sequence of 6 tagged images each 250 ms apart in 3 planes. Sagittal plane
* Nasopharnygeal plane
R E FE R E N CES 1. Brown EC, Cheng S, McKenzie DK, Butler JE, Gandevia SC, Bilston LE. Respiratory movement of upper airway tissue in obstructive sleep apnea. Sleep 2013;36:1069–76. 2. Brown EC, Cheng S, McKenzie DK, Butler JE, Gandevia SC, Bilston LE. Tongue and lateral upper airway movement with mandibular advancement. Sleep 2013;36:397–404. 3. Jordan A, Eckert DJ, Wellman A, Trinder JA, Malhotra A, White DP. Termination of respiratory events with and without cortical arousal in obstructive sleep apnea. Am J Respir Crit Care Med 2011;184:1183–119. 4. Kairaitis K, Stavrinou R, Parikh R, Wheatley J, Amis T. Mandibular advancement decreases pressures in the tissues surrounding the upper airway in rabbit. J Appl Physiol 2006;100:349–56. 5. Isono S, Tanaka A, Sho Y, Konno A, Nishino T. Advancement of the mandible improves velopharyngeal airway patency. J Appl Physiol 1995;79:2132–8. 6. Walsh JH, Maddison KJ, Platt PR, Hillman DR, Eastwood PR. Influence of head extension, flexion, and rotation on collapsibility of the passive upper airway. Sleep 2008;31:1440–7.
Oropharyngeal plane
The arrowheads indicate the position of the airway while collapsed. The arrow indicates approximately the original (dashed line) and final position (no dash) of the maxillary plane. The asterisk indicates the original position of the mandible in the sagittal plane. Video of the airway opening in the sagittal plane is available in supplemental material.
SUBM I SSI O N & CO R R ESPO NDENCE I NFO R M ATI O N
quiet breathing. At apnea termination, there was a coordinated airway opening response involving genioglossus, mandibular advancement (possibly via activation of superficial fibers of masseter and pterygoid muscles), and neck extensors. This is reminiscent of the “triple airway maneuver” (neck extension, mandibular protrusion, and mouth opening) used to stabilize the airway during anesthesia. These images show that airway reopening involves more than airway dilators. Head movement and mandibular advancement Journal of Clinical Sleep Medicine, Vol. 12, No. 11, 2016
1564
Submitted for publication April, 2016 Submitted in final revised form June, 2016 Accepted for publication July, 2016 Address correspondence to: Professor Lynne Bilston, Neuroscience Research Australia, Barker St, Randwick, NSW 2031 Australia; Tel: +61-2-9399-1673; Fax: +61-2-9399-1027; Email: [email protected]
D I SCLO S U R E S TAT E M E N T This was not an industry supported study. This research was supported by an NHMRC project Grant 455228. Dr. Bilston is supported by an NHMRC fellowship. Dr. Bilston has received consulting income from Linguaflex LLC not related to this study. Dr. Brown has indicated no financial conflicts of interest. All research was conducted at Neuroscience Research Australia
