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Analysis of the myoelectric characteristics of genioglossus in REM sleep and its improvement by CPAP treatment in OSA patients

Abstract

Objectives

To reveal the characteristics of genioglossus (GG) activation in moderate and severe obstructive sleep apnea (OSA) patients during rapid eye movement (REM) sleep compared with non-rapid eye movement (NREM) sleep and to determine whether continuous positive airway pressure (CPAP) could improve GG activation in OSA patients during sleep.

Methods

All subjects underwent polysomnography (PSG) with synchronous GG electromyography (GGEMG) recording with intra-oral surface electrodes at baseline on the first night. Only those subjects diagnosed with moderate and severe OSA were included and were manually titrated with CPAP to achieve a therapeutic pressure (Pt) with GGEMG recording on the second night.

Results

Nine OSA patients and six normal controls were analyzed in this study. The tonic GGEMG was higher in OSA patients during wakefulness (p = 0.003) and NREM sleep (p = 0.015), but it was not higher in REM sleep (p = 0.862). The average phasic activity of OSA patients was significantly higher in all stages, including wakefulness (p = 0.007), NREM sleep (p = 0.005), and REM sleep (p = 0.021). The peak phasic GGEMG was not different in wakefulness compared with normal controls (p = 0.240), but it was higher in OSA patients in NREM sleep (p = 0.001) and REM sleep (p = 0.021), and it was significantly reduced by using CPAP during sleep (NREM sleep: p = 0.027; REM sleep: p = 0.001).

Conclusions

Our results demonstrate that GG activation during NREM and REM sleep is associated with component differences. The tonic component of GGEMG exhibited less of a compensatory increase compared with the phasic component in REM sleep, suggesting that it may be one of the pathological mechanisms of UA collapsibility in REM sleep. In addition, treatment with CPAP can normalize GGEMG activity and mostly reduced the peak phasic GGEMG during sleep.

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Abbreviations

GG:

genioglossus

GGEMG:

genioglossus electromyography

REM:

rapid eye movement

NREM:

non-rapid eye movement

OSA:

obstructive sleep apnea

CPAP:

continuous positive airway pressure

Pt:

therapeutic pressure

PSG:

polysomnography

UA:

upper airway

AHI:

apnea-hypopnea index

BMI:

body mass index

EEG:

electroencephalogram

EOG:

electrooculogram

ECG:

electrocardiogram

AASM:

American Academy of Sleep Medicine

RMS:

root mean square

LSAT:

lowest oxygen saturation

MSAT:

mean oxygen saturation during sleep

OID3:

oxygen desaturation index of ≥ 3%

ARO:

arousal index

RERA:

respiratory effort–related arousals

References

  1. 1.

    Sutherland K, Cistulli PA (2015) Recent advances in obstructive sleep apnea pathophysiology and treatment. Sleep Biol Rhythms 13:26–40

  2. 2.

    Zinchuk AV, Gentry MJ, Concato J, Yaggi HK (2017) Phenotypes in obstructive sleep apnea: a definition, examples and evolution of approaches. Sleep Med Rev 35:113–123

  3. 3.

    Eckert DJ, White DP, Jordan AS, Malhotra A, Wellman A (2013) Defining phenotypic causes of obstructive sleep apnea. Identification of novel therapeutic targets. Am J Respir Crit Care Med 188:996–1004

  4. 4.

    Osman AM, Carter SG, Carberry JC, Eckert DJ (2018) Obstructive sleep apnea: current perspectives. Nat Sci Sleep 10:21–34

  5. 5.

    Cori JM, O’Donoghue FJ, Jordan AS (2018) Sleeping tongue: current perspectives of genioglossus control in healthy individuals and patients with obstructive sleep apnea. Nat Sci Sleep 10:169–179

  6. 6.

    Oliven R, Cohen G, Dotan Y, Somri M, Schwartz AR, Oliven A (2018) Alteration in upper airway dilator muscle coactivation during sleep: comparison of patients with obstructive sleep apnea and healthy subjects. J Appl Physiol 124:421–429

  7. 7.

    Wijesuriya NS, Gainche L, Jordan AS, Berlowitz DJ, LeGuen M, Rochford PD, O’Donoghue FJ, Ruehland WR, Carberry JC, Butler JE, Eckert DJ (2018) Genioglossus reflex responses to negative upper airway pressure are altered in people with tetraplegia and obstructive sleep apnoea. J Physiol 596:2853–2864

  8. 8.

    Zhao D, Li Y, Xian J, Qu Y, Zhang J, Cao X, Ye J (2016) Relationship of genioglossus muscle activation and severity of obstructive sleep apnea and hypopnea syndrome among Chinese patients. Acta Otolaryngol 136:819–825

  9. 9.

    Malhotra A, Pillar G, Fogel RB, Beauregard J, Edwards JK, Slamowitz DI, Shea SA, White DP (2000) Genioglossal but not palatal muscle activity relates closely to pharyngeal pressure. Am J Respir Crit Care Med 162:1058–1062

  10. 10.

    Edwards BA, White DP (2011) Control of the pharyngeal musculature during wakefulness and sleep: implications in normal controls and sleep apnea. Head Neck 33(Suppl 1):37–45

  11. 11.

    Dotan Y, Pillar G, Tov N, Oliven R, Steinfeld U, Gaitini L, Odeh M, Schwartz AR, Oliven A (2013) Dissociation of electromyogram and mechanical response in sleep apnoea during propofol anaesthesia. Eur Respir J 41:74–84

  12. 12.

    Zhang H, Ye JY, Hua L, Chen ZH, Ling L, Zhu Q, Wang LM, Zheng L, Zhang YH (2015) Inhomogeneous neuromuscular injury of the genioglossus muscle in subjects with obstructive sleep apnea. Sleep Breath 19:539–545

  13. 13.

    Lo YL, Jordan AS, Malhotra A, Wellman A, Heinzer RC, Schory K, Dover L, Fogel RB, White DP (2006) Genioglossal muscle response to CO2 stimulation during NREM sleep. Sleep 29:470–477

  14. 14.

    O’Connor CM, Lowery MM, Doherty LS, McHugh M, O’Muircheartaigh C, Cullen J, Nolan P, McNicholas WT, O’Malley MJ (2007) Improved surface EMG electrode for measuring genioglossus muscle activity. Respir Physiol Neurobiol 159:55–67

  15. 15.

    Zhao D, Li Y, Xian J, Qu Y, Cao X, Ye J (2017) The combination of anatomy and genioglossus activity in predicting the outcomes of velopharyngeal surgery. Otolaryngol Head Neck Surg 156:567–574

  16. 16.

    Horner RL, Hughes SW, Malhotra A (2013) State-dependent and reflex drives to the upper airway: basic physiology with clinical implications. J Appl Physiol 116:325–336

  17. 17.

    McSharry DG, Saboisky JP, Deyoung P, Jordan AS, Trinder J, Smales E, Hess L, Chamberlin NL, Malhotra A (2014) Physiological mechanisms of upper airway hypotonia during REM sleep. Sleep 37:561–569

  18. 18.

    Carberry JC, Jordan AS, White DP, Wellman A, Eckert DJ (2015) Upper airway collapsibility (Pcrit) and pharyngeal dilator muscle activity are sleep-stage dependent. Sleep 39:511–521

  19. 19.

    McGinley BM, Schwartz AR, Schneider H, Kirkness JP, Smith PL, Patil SP (2008) Upper airway neuromuscular compensation during sleep is defective in obstructive sleep apnea. J Appl Physiol 105:197–205

  20. 20.

    Sowho M, Amatoury J, Kirkness JP, Patil SP (2014) Sleep and respiratory physiology in adults. Clin Chest Med 35:469–481

  21. 21.

    White DP (2005) Pathogenesis of obstructive and central sleep apnea. Am J Respir Crit Care Med 172:1363–1370

  22. 22.

    Saboisky JP, Butler JE, Fogel RB, Taylor JL, Trinder JA, White DP, Gandevia SC (2006) Tonic and phasic respiratory drives to human genioglossus motoneurons during breathing. J Neurophysiol 95:2213–2221

  23. 23.

    Cao MT, Sternbach JM, Guilleminault C (2017) Continuous positive airway pressure therapy in obstuctive sleep apnea: benefits and alternatives. Expert Rev Respir Med 11:259–272

  24. 24.

    Kushida CA, Chediak A, Berry RB, Brown LK, Gozal D, Iber C, Parthasarathy S, Quan SF, Rowley JA, Positive Airway Pressure Titration Task F et al (2008) Clinical guidelines for the manual titration of positive airway pressure in patients with obstructive sleep apnea. J Clin Sleep Med 4:157–171

  25. 25.

    Iber C, Ancoli-Israel S, Chesson AL, Quan SF (2007) The AASM manual for the scoring of sleep and associated events: rules, terminology and technical specifications

  26. 26.

    McSharry D, O’Connor C, McNicholas T, Langran S, O’Sullivan M, Lowery M, McNicholas WT (2012) Genioglossus fatigue in obstructive sleep apnea. Respir Physiol Neurobiol 183:59–66

  27. 27.

    Lo YL, Jordan AS, Malhotra A, Wellman A, Heinzer RA, Eikermann M, Schory K, Dover L, White DP (2007) Influence of wakefulness on pharyngeal airway muscle activity. Thorax 62:799–805

  28. 28.

    Taranto-Montemurro L, Sands SA, Grace KP, Azarbarzin A, Messineo L, Salant R, White DP, Wellman DA (2018) Neural memory of the genioglossus muscle during sleep is stage-dependent in healthy subjects and obstructive sleep apnea patients. J Physiol 596:5163–5173

  29. 29.

    RB F, A M GP, JK E, J B SAS, DP W (2001) Genioglossal activation in patients with obstructive sleep apnea versus control subjects. Mechanisms of muscle control. Am J Respir Crit Care Med 164:2025–2030

  30. 30.

    Fogel RB, Trinder J, White DP, Malhotra A, Raneri J, Schory K, Kleverlaan D, Pierce RJ (2005) The effect of sleep onset on upper airway muscle activity in patients with sleep apnoea versus controls. J Physiol 564:549–562

  31. 31.

    Sankari A, Pranathiageswaran S, Maresh S, Hosni AM, Badr MS (2017) Characteristics and consequences of non-apneic respiratory events during sleep. Sleep 40(1):1–8

  32. 32.

    Dotan Y, Pillar G, Schwartz AR, Oliven A (2015) Asynchrony of lingual muscle recruitment during sleep in obstructive sleep apnea. J Appl Physiol 118:1516–1524

  33. 33.

    Jordan AS, Wellman A, Heinzer RC, Lo YL, Schory K, Dover L, Gautam S, Malhotra A, White DP (2007) Mechanisms used to restore ventilation after partial upper airway collapse during sleep in humans. Thorax 62:861–867

  34. 34.

    Svanborg E (2005) Impact of obstructive apnea syndrome on upper airway respiratory muscles. Respir Physiol Neurobiol 147:263–272

  35. 35.

    Fenik VB, Davies RO, Kubin L (2005) REM sleep-like atonia of hypoglossal (XII) motoneurons is caused by loss of noradrenergic and serotonergic inputs. Am J Respir Crit Care Med 172:1322–1330

  36. 36.

    Morrison JL, Sood S, Liu H, Park E, Nolan P, Horner RL (2003) GABAA receptor antagonism at the hypoglossal motor nucleus increases genioglossus muscle activity in NREM but not REM sleep. J Physiol 548:569–583

  37. 37.

    Poothrikovil RP, Al Abri MA (2012) Snoring-induced nerve lesions in the upper airway. Sultan Qaboos Univ Med J 12:161–168

  38. 38.

    Woods MJ, Nicholas CL, Semmler JG, Chan JK, Jordan AS, Trinder J (2015) Common drive to the upper airway muscle genioglossus during inspiratory loading. J Neurophysiol 114:2883–2892

  39. 39.

    Svanborg E (2001) Upper airway nerve lesions in obstructive sleep apnea. Am J Respir Crit Care Med 164:187–189

  40. 40.

    Fry AC (2004) The role of resistance exercise intensity on muscle fibre adaptations. Sports Med 34:663–679

  41. 41.

    Eckert DJ, Lo YL, Saboisky JP, Jordan AS, White DP, Malhotra A (2011) Sensorimotor function of the upper-airway muscles and respiratory sensory processing in untreated obstructive sleep apnea. J Appl Physiol 111:1644–1653

  42. 42.

    Eckert DJ, Younes MK (2014) Arousal from sleep: implications for obstructive sleep apnea pathogenesis and treatment. J Appl Physiol 116:302–313

  43. 43.

    Cori JM, Thornton T, O’Donoghue FJ, Rochford PD, White DP, Trinder J, Jordan AS (2017) Arousal-induced hypocapnia does not reduce genioglossus activity in obstructive sleep apnea. Sleep 40(6):1–11

  44. 44.

    Jordan AS, O’Donoghue FJ, Cori JM, Trinder J (2017) Physiology of arousal in obstructive sleep apnea and potential impacts for sedative treatment. Am J Respir Crit Care Med 196:814–821

  45. 45.

    Haba-Rubio J, Sforza E, Weiss T, Schröder C, Krieger J (2005) Effect of CPAP treatment on inspiratory arousal threshold during NREM sleep in OSAS. Sleep Breath 9:12–19

  46. 46.

    Carrera M, Barbe F, Sauleda J, Tomas M, Gomez C, Agusti AG (1999) Patients with obstructive sleep apnea exhibit genioglossus dysfunction that is normalized after treatment with continuous positive airway pressure. Am J Respir Crit Care Med 159:1960–1966

  47. 47.

    White DP, Lombard RM, Cadieux RJ, Zwillich CW (1985) Pharyngeal resistance in normal humans: influence of gender, age, and obesity. J Appl Physiol 58:365–371

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Acknowledgments

The authors are grateful for the technical support provided by staff in the Department of Otolaryngology, Beijing Tsinghua Chang Gung Hospital, and to Prof. Hong Xu for fruitful discussions.

Funding

This work was supported by the National Natural Science Foundation of China [grant number 81670918, 81873696] and Beijing Municipal Administration of Hospitals Clinical Medicine Development of Special Funding Support (XMLX201703).

Author information

Prof. Jingying Ye, Di Zhao, Guoping Yin and Yuhuan Zhang contributed to the experimental design and interpretation of the results. Jingjing Li and Xin Cao collected and analyzed the data. Yingqian Zhou contributed to data analysis and interpretation and wrote the manuscript. All authors contributed to the final version.

Correspondence to Jingying Ye.

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Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.

This study was approved by the Beijing Tsinghua Chang Gung Hospital Institutional Review Board.

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Informed consent was obtained from all individual participants included in the study.

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Zhou, Y., Zhao, D., Yin, G. et al. Analysis of the myoelectric characteristics of genioglossus in REM sleep and its improvement by CPAP treatment in OSA patients. Sleep Breath (2019). https://doi.org/10.1007/s11325-019-01875-7

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Keywords

  • Obstructive sleep apnea
  • Genioglossus
  • Intra-oral surface electrode
  • Neuromuscular lesions
  • Continuous positive airway pressure