|Year : 2020 | Volume
| Issue : 2 | Page : 75-81
Motor unit potential analysis of the palatal muscles in obstructive sleep apnea syndrome
Feray Karaali-Savrun1, Nurten Uzun Adatepe1, Gülçin Benbir Şenel1, Rahsan Inan1, Hakan Kaynak1, Asim Kaytaz2, Derya Karadeniz1
1 Department of Neurology, Cerrahpasa School of Medicine, Istanbul University, Istanbul, Turkey
2 Department of Ear, Nose and Throat, Cerrahpasa School of Medicine, Istanbul University, Istanbul, Turkey
|Date of Submission||22-Feb-2019|
|Date of Decision||29-Oct-2019|
|Date of Acceptance||08-Nov-2019|
|Date of Web Publication||29-Jun-2020|
Gülçin Benbir Şenel
Department of Neurology, Cerrahpasa School of Medicine, Istanbul University, Istanbul 34098
Source of Support: None, Conflict of Interest: None
Objectives: Among different theories about pathogenesis of obstructive sleep apnea syndrome (OSAS), dysfunction of upper airway muscles still awaits to be delineated. The aim of this study is to examine differences in motor unit potential (MUP) parameters of upper airway muscles between OSAS patients and healthy controls. Methods: Ten male patients diagnosed as OSAS by whole-night polysomnography were analyzed for MUP parameters of genioglossus (GG) muscle, palatoglossus muscle (PG), palatopharyngeus muscle, and uvular (U) muscle. Eight healthy volunteer men matched by age were enrolled as a control group. Results: In PG muscle parameters, the mean MUP area was significantly smaller (P = 0.040) in OSAS patients than those in controls. On the other hand, U muscle parameters showed a significantly larger mean MUP area (P = 0.022) in OUAS patients compared to those in the control group. In OSAS patients, the percentages of polyphasic MUPs of GG and PG muscles were significantly high (P < 0.001 and P = 0.05, respectively). Body mass index was positively correlated with number of phases of GG muscle (rs = 0.63, P < 0.05) and duration of U muscle (rs = 0.71, P < 0.05) in OSAS patients. Other MUP parameters of palatal muscles were similar between the two groups. Conclusion: Our results showed that, although mild in severity, structural neurogenic and myogenic changes characterized as mild and nonuniform MUP changes may co-exist in OSAS patients. These changes in palatal muscles may be attributed to compensatory adaptation of muscle fibers to other precipitating factors in OSAS.
Keywords: Motor unit potentials, obstructive sleep apnea syndrome, pathogenesis, upper airway muscles
|How to cite this article:|
Karaali-Savrun F, Adatepe NU, Şenel GB, Inan R, Kaynak H, Kaytaz A, Karadeniz D. Motor unit potential analysis of the palatal muscles in obstructive sleep apnea syndrome. Neurol Sci Neurophysiol 2020;37:75-81
|How to cite this URL:|
Karaali-Savrun F, Adatepe NU, Şenel GB, Inan R, Kaynak H, Kaytaz A, Karadeniz D. Motor unit potential analysis of the palatal muscles in obstructive sleep apnea syndrome. Neurol Sci Neurophysiol [serial online] 2020 [cited 2021 Sep 22];37:75-81. Available from: http://www.nsnjournal.org/text.asp?2020/37/2/75/288415
| Introduction|| |
Obstructive sleep apnea syndrome (OSAS) is characterized by episodic occurrence of hypopneas and/or apneas during sleep secondary to repeated episodes of partial and/or complete obstruction of the upper airway in the oropharyngeal region, possibly precipitated by sleep-related atonia in upper airway muscles.,, The retropalatal airway, which is the area behind the soft palate and base of the tongue, is the major site of narrowing in OSAS. The retropalatal airway is controlled by soft palate muscle activity and constitutes the most vulnerable part of the upper airway, as it lacks substantial bony or rigid support. Reduced palatal muscle activity during sleep and negative pressure within the upper airway lumen will result in increased resistance in the retropalatal airway, which is a common site of occlusion in OSAS. Upper airway muscles known to be responsive to negative pressure within the upper airway lumen are genioglossus (GG),, palatoglossus (PG), and palatopharyngeus (PP) muscles.
Reflex activation of upper airway muscles by upper airway negative pressure , and changes in the activity of palatal muscles with route of respiration  showed that upper airway muscles are important modulators in the maintenance of upper airway patency. Laryngeal adductor activity was also shown to be prominent accompanying increased upper airway pressure during hypopnea. Multiunit electromyography (EMG) activity of GG muscle, which is the primary protrudor of the tongue, was found to be greater in OSAS patients. Some other structural abnormalities, changes in neural drive, and/or disturbed properties of the endurance of upper airway muscles have been shown in patients with OSAS. Needle EMG studies have previously demonstrated partial denervation in oropharyngeal muscles in OSAS.
On this basis, studies in this area have long focused on upper airway muscles relevant to the pathogenesis of OSAS, investigating motor unit potentials (MUPs) of these muscles. However, there is still an ongoing debate whether and to what extent neuromuscular alterations contribute to upper airway occlusion. In this study, we aimed to analyze MUP parameters of GG, PG, PP, and uvular (U) muscles in patients with OSAS and to compare our results with those obtained in the healthy control group.
| Methods|| |
Ten male patients with OSAS and age-matched eight healthy volunteer men as a control group  were prospectively enrolled. All participants underwent a thorough medical evaluation to exclude neurological disorders, or other disorders affecting the upper airway, or sleep disorders other than sleep apnea. None of the participants was on any medication known to affect muscle activity, such as antidepressants or benzodiazepines. Demographic data were recorded including age, gender, body mass index (BMI), neck circumference, and disease duration of OSAS. Our study was approved by a local ethical committee (with a number of 17/09/2003-22161), and a written informed consent form was obtained from all participants.
All patients with OSAS had a whole-night polysomnography (PSG), which was applied with central, frontal, and occipital electroencephalography placed on the scalp according to international 10–20 system, right and left electrooculography, surface EMG on the chin and bilateral legs, electrocardiography, oronasal thermistor, nasal airflow, thoracal and abdominal respiratory efforts, oxygen saturation, and body position. Synchronized video recording was done all through the night. Evaluations of PSG were done according to the American Academy of Sleep Medicine Manual for the scoring of sleep and associated events. The diagnosis of OSAS was established as 15 or more abnormal respiratory events per 1 h of sleep. All participants in the control group were evaluated clinically in detail, and OSAS was excluded using the Berlin questionnaire.
EMG investigations of untreated OSAS patients and controls were obtained 2 h after awakening in the morning. Throughout the procedure, participants were told to lay down comfortably, relax in supine position, breathe quietly, and remain awake. The skin temperature was maintained at 32°C. Filter settings were arranged as 10 kHz for high cut and 5 Hz for low cut. Sweep speed was 5 ms/div, and gain was 100 μV/division.
For MUP analysis, a 4-channel EMG device (Keypoint Natus, USA) was used in the electrophysiology laboratory. Instruments were calibrated before the collection of data. MUP analysis was made with a computer-supported analyzing method of the same device. Two types of concentric needle electrodes (26 G, 37 mm, recording area of 0.07 mm 2 and 23 G, 75 mm, recording area of 0.67 mm 2, Alpine Biomed) were used. A ground electrode was placed over the right clavicle during EMG procedures.
GG, PG, PP, and U muscles were investigated using multi-MUP analysis. All procedures were explained to participants before testing. Needle insertion was performed percutaneously for GG and through an intraoral approach for the other muscles. Lidocaine spray (40 mg, Xylocaine, AstraZeneca) was topically applied to oropharynx structures through an intraoral approach, and an anesthetic cream (Emla, AstraZeneca) was topically applied on the skin under the chin at least 30 min before EMG recordings through a percutaneous approach. For GG recordings, concentric needle electrode was inserted 3 mm lateral to the frenulum bilaterally and into 15–20 mm deep into the body of GG muscle. For recordings from PG muscle, electrodes were inserted 5 mm deep into the anterior arch of the pharyngeal fauces. Needle insertion areas were the posterior arch of the pharyngeal fauces for PP muscle and uvula for U muscle.
Confirmation of examined muscles under investigation was made by the use of muscle-specific maneuvers and by observation of MUPs on screen associated with appropriate sounds through loudspeaker simultaneously. At first, spontaneous activity was tested in resting muscles. Then, MUPs were studied in muscles at slight voluntary effort. MUPs were collected, and 25 MUPs with good quality were selected for each muscle for the final analysis. Among MUP parameters, amplitude, duration, area, rise time, thickness (area divided by amplitude), and number of phases and/or turns were calculated. MUP amplitudes were calculated from peak to peak amplitude (in μV), duration was measured from onset of the first to offset of the last deviation from baseline (in ms), area was calculated as the sum of MUP values (in mV ms) multiplied by sampling interval, rise time was the time between initial positive peak and subsequent negative peak (in μs), the number of MUP phases was counted as baseline crossings − 1, and a turn was the change in the direction of MUP amplitude for at least 25 mV.,, All MUP parameters were done and interpreted by one investigator using the above-mentioned methods.
SPSS (Statistical Package for the Social Sciences, Chicago, IL, USA) 16. 0 for Windows package program was used for statistical analysis. Numerical variables were given as mean ± standard deviation, and categorical variables were expressed as numbers and/or percentages. EMG variables between patients with OSAS and healthy volunteers were compared using Mann–Whitney U-test. Spearman's correlation was used to detect the presence of any correlation between EMG parameters and clinical data. The threshold level was established to <0.05 for statistical significance.
| Results|| |
The mean age of patients with OSAS was 43.5 ± 10.7 years (between 26 and 58 years), and the mean age of controls was 40.2 ± 9.1 years (between 27 and 50 years, P = 0.592). The mean disease duration was 9.2 ± 6.2 years (ranging between 3 and 20 years), and the mean respiratory disturbance index was 41.2 ± 11.5/h (between 15 and 85/h) in OSAS patients. The mean BMI was higher in OSAS patients compared to those in healthy controls (33.29 ± 4.05 vs. 23.64 ± 2.51 kg/m 2, respectively, P = 0.0004). The mean neck circumference was significantly higher in the patient group (45.00 ± 3.71 vs. 36.75 ± 2.49 cm, respectively; P = 0.0004). The demographic data of patients and controls are given in [Table 1].
In EMG analysis, insertional activity was normal in all muscles analyzed, and no spontaneous activity was observed. The MUP analysis data of four muscles are given in [Table 2], [Table 3], [Table 4], [Table 5]. The mean MUP area of PG muscle was smaller in OSAS patients (198.6 ± 135.3 μV ms) compared to those in controls (399.0 ± 236.8 μV ms), which was statistically significant (P = 0.040). The MUP area of U muscle was also significantly larger in patients with OSAS than those in the control group (322.2 ± 262.2 μV ms versus 131.5 ± 57.3 μV ms correspondingly, P = 0.022). The polyphasic MUP ratio was significantly increased in GG muscle (P < 0.001) and in PG muscle (P = 0.05) in OSAS patients compared to those in healthy controls. Other MUP parameters were found similar between the two groups [Table 2], [Table 3], [Table 4], [Table 5].
|Table 2: The comparison of electromyographic characteristics of genioglossus muscle between patients with obstructive sleep apnea syndrome and healthy controls|
Click here to view
|Table 3: The comparison of electromyographic characteristics of palatoglossus muscle between patients with obstructive sleep apnea syndrome and healthy controls|
Click here to view
|Table 4: The comparison of electromyographic characteristics of palatopharyngeus muscle between patients with obstructive sleep apnea syndrome and healthy controls|
Click here to view
|Table 5: The comparison of electromyographic characteristics of uvular muscle between patients with obstructive sleep apnea syndrome and healthy controls|
Click here to view
In correlation analysis, mean age, mean neck circumference, disease duration, and respiratory disturbance index were found not to be significantly correlated with EMG data in the OSAS group. The sentence was revised by fragmenting into two as follows: In the control group, there was a positive correlation between neck circumference and mean number of MUP phases (rs= 0.76, P < 0.05), MUP duration (rs= −0.72, P < 0.05) and MUP thickness (rs= −0.71, P < 0.05) of PP muscle. There was also a positive correlation between neck circumference and mean number of MUP phases of U muscle (rs= 0.76, P < 0.05). In the patients with OSAS, there was a positive correlation between BMI and mean MUP rise time of GG muscle (rs= 0.69, P < 0.05), mean number of MUP phases of GG muscle (rs= 0.63, P < 0.05), and mean MUP duration of U muscle (rs= 0.71, P < 0.05). In healthy controls, there was also a positive correlation between BMI and mean number of MUP phases of PP muscle (rs= 0.75, P < 0.05) and mean number of MUP phases of U muscle (rs= 0.77, P < 0.05). Other variables failed to show any correlation with anthropological measures Other variables failed to show any correlation with anthropological measures [Table 2], [Table 3], [Table 4], [Table 5].
| Discussion|| |
Our study showed that the mean MUP area of U muscle was significantly larger in OSAS patients, but the MUP area of PG muscle was smaller, contrary to what is expected. The polyphasic MUP ratio was significantly high in GG and PG muscles in OSAS patients. We also found that there was a positive correlation in OSAS patients between BMI and number of phases of GG muscle and mean duration of U muscle. In controls, a positive correlation was present between BMI and mean number of MUP phases of PP and U muscles. Furthermore, in controls, neck circumference showed a positive correlation with the mean number of MUP phases, duration and thickness of PP muscle, and mean number of MUP phases of U muscle.
MUPs represent the sum of synchronously firing activity of a muscle or some fibers of a motor unit. This constitutes a basic structure of a motor unit with well-known parameters as diameter, distribution, or number of muscle fibers. For this reason, any structural abnormality in a motor unit will result in alterations in MUP parameters. Quantitation of MUP parameters is, therefore, being used to define neuromuscular disorders since EMG was first introduced.
In myopathic conditions, duration and amplitude of MUPs decrease, whereas larger duration and higher amplitude than normal potentials appear in neuropathic conditions. Similarly, area measurements may also help to differentiate neuropathy from myopathy. Duration is the reflection of number and diameter of fibers, which contributes to form MUP activity. Duration is increased when there is an increase in number of fibers, especially of those with large diameter. This shows the presence of denervation in skeletal muscles with collateral sprouting and reinnervation.,,,
The maximum temporal dispersion of MUP is defined by increased number of phases and duration. In patients with neuropathy and myopathy, there is an increased incidence of polyphasic MUPs, and this abnormal parameter is thus nonspecific. Differentiation between myopathy and neuropathy is done by a combination with other parameters.,
In the literature, there are many studies investigating the EMG characteristics of GG, PG, and PP muscles.,,, In a recent study, MUP parameters of tongue protrudor muscles were reported to be significantly larger in OSAS patients compared to controls, independent of patient characteristics, severity of sleep breathing disorder, or its duration. The authors emphasized the role of denervation injury, which occurred secondary to vibrations in upper airways, but they also mentioned the need for further well-designed studies. Studies on neuromuscular function of the soft palate and uvula muscle showed the presence of neuropathy characterized by diffuse inflammation and aberrant neural structures. It was also demonstrated that more severe snoring and/or sleep apnea had a correlation with worse dysfunction in sensory nerves together with atrophy in both nerves and muscle fibers of soft palate and uvula. On this basis, it was concluded upon recent evidences that neurogenic pathology may explain the loss of muscular tone in the soft palate and/or uvula in parallel with evolving obstructive sleep apnea from snoring.
Upper airway patency mainly relies on the dilating and stabilizing forces generated by the sustained muscle activity in the upper airway, particularly the GG muscle., It is widely accepted that the GG muscle has significantly increased resting activity in both inspiration and expiration in OSAS compared to controls.,, It was demonstrated that MUPs obtained from GG muscle are of longer duration in patients with OSAS, suggesting neurogenic changes secondary to neural injury associated with obstructive sleep apnea.
On the other hand, different results have been reported in the literature on GG endurance times, recovery times, or basal tonic activity., These authors observed no difference in baseline (tonic) palatal muscle EMG activity between OSAS patients and normal controls, but they reported that PG muscle had decreased EMG reflex responses to negative pressure in the upper airway in OSAS patients compared to those in healthy controls. They have concluded that there may be an altered upper airway neuromuscular function and impairment of EMG reflex responses in OSAS, which may have a significant role in the development of upper airway narrowing and obstruction during sleep.
Motor neuron pathologies such as spontaneous activity, polyphasic potentials of increased duration, or reduced interference pattern were also reported in patients with OSAS., In our study, the mean MUP area or amplitude of GG muscle was similar between OSAS patients and controls; however, the polyphasic MUP ratio was significantly high in GG and PG muscles. The mean MUP area of U muscle was also significantly larger in patients with OSAS. Large mean MUP areas in U muscle and small mean MUP areas in PG muscle together with increased polyphasic potentials in GG and PG muscles were interpreted as mild and nonspecific neurogenic and/or myogenic MUP changes in our study because there was no any other associated MUP changes. However, although mild and nonspecific, these changes may be accepted as accompanying or worsening factors in addition to other precipitating conditions of OSAS.
Because all OSAS patients were overweight or obese (with a mean BMI of 33.2 kg/m 2), different risk factors and mechanisms are likely to be present in obese and nonobese OSAS patients versus those with craniofacial abnormalities. Dilator muscle activation was shown to correlate less well with BMI, but anatomical factors in craniofacial structures were reported to be important in defining upper airway anatomy independent of body weight. Activation in upper airway muscles was strongly related to the collapsibility of the upper airway, more than to BMI, which shows that obesity is not the main factor in the pathogenesis of OSAS, but several other factors may determine OSAS. In addition, BMI was associated only with small reductions in neurophysiological EMG parameters such as amplitude or velocity of sensory and/or mixed nerves, and a consistent association between BMI and amplitudes or latencies of MUP parameters has not been proven yet. Anatomically fat pads in the parapharyngeal area were shown to increase together with increasing age, which was documented to be independent of overall body fat ratio or neck circumference.
Among the limitations of our study, we could not perform MUP analysis during sleep because of the lack of implantable EMG electrodes. GG muscle activity was demonstrated to reduce sleep onset following the alpha-theta transition both in healthy individuals and OSAS patients., Second, only male patients were evaluated here, and the number of participants was small. We could not perform electrophysiological and histopathological correlation due to the lack of biopsy specimens. In the literature, inconclusive results have been reported on oropharyngeal muscle histopathology; some were ascribed to myopathy, postulated to result from activity-induced injury, interpreted to be of unclear in etiology, or attributed to mixed etiology composed of neurogenic and myopathic causes., Biopsy studies from GG muscle showed an increase in type II muscle fibers in patients with OSAS compared to healthy controls, while other findings showed evidence for partial denervation in motor nerves., Finally, we did not repeat our evaluations after the effective treatment of OSAS. In the literature, a small number of studies have investigated whether these changes in the upper airway muscle in OSAS are reversible upon efficient treatment of OSAS with positive airway pressure therapy, but those histopathological changes were not present in patients with treated OSAS., Prospective, placebo-controlled, randomized studies with large number of participants are still needed to demonstrate changes in the upper airway muscle in the pathophysiology of OSAS, and the effect of OSAS treatment should be analyzed.
Financial support and sponsorship
Conflicts of interest
There are no conflicts of interest.
| References|| |
Zhao M, Barber T, Cistulli PA, Sutherland K, Rosengarten G. Simulation of upper airway occlusion without and with mandibular advancement in obstructive sleep apnea using fluid-structure interaction. J Biomech 2013;46:2586-92.
Wilkinson V, Malhotra A, Nicholas CL, Worsnop C, Jordan AS, Butler JE, et al
. Discharge patterns of human genioglossus motor units during arousal from sleep. Sleep 2010;33:379-87.
Mu L, Sobotka S, Chen J, Su H, Sanders I, Adler CH, et al
. Arizona Parkinson's disease consortium. Altered pharyngeal muscles in Parkinson disease. J Neuropathol Exp Neurol 2012;71:520-30.
Mu L, Chen J, Li J, Arnold M, Sobotka S, Nyirenda T, et al
. Sensory ınnervation of the human soft palate. Anat Rec (Hoboken) 2018;301:1861-70.
Fraigne JJ, Orem JM. Phasic motor activity of respiratory and non-respiratory muscles in REM sleep. Sleep 2011;34:425-34.
Huang J, Pinto SJ, Yuan H, Katz ES, Karamessinis LR, Bradford RM, et al
. Upper airway collapsibility and genioglossus activity in adolescents during sleep. Sleep 2012;35:1345-52.
Zhou YQ, Ye JY. Neuromuscular properties of genioglossus activity in healthy adults and obstructive sleep apnea patients. Zhonghua Er Bi Yan Hou Tou Jing Wai Ke Za Zhi 2018;53:70-2.
Oliven R, Cohen G, Somri M, Schwartz AR, Oliven A. Peri-pharyngeal muscle response to inspiratory loading: Comparison of patients with OSA and healthy subjects. J Sleep Res 2018;30:e12756.
Mortimore IL, Mathur R, Douglas NJ. Effect of posture, route of respiration, and negative pressure on palatal muscle activity in humans. J Appl Physiol 1995;79:448-54.
Genta PR, Owens RL, Edwards BA, Sands SA, Eckert DJ, Butler JP, et al
. Influence of pharyngeal muscle activity on inspiratory negative effort dependence in the human upper airway. Respir Physiol Neurobiol 2014;201:55-9.
Oliven R, Cohen G, Dotan Y, Somri M, Schwartz AR, Oliven A. Alteration in upper airway dilator muscle coactivation during sleep: Comparison of patients with obstructive sleep apnea and healthy subjects. J Appl Physiol (1985) 2018;124:421-9.
Gupta A, Kumar R, Bhattacharya D, Thukral BB, Suri JC. Craniofacial and upper airway profile assessment in North Indian patients with obstructive sleep apnea. Lung India 2019;36:94-101.
] [Full text]
Svanborg E. Impact of obstructive apnea syndrome on upper airway respiratory muscles. Respir Physiol Neurobiol 2005;147:263-72.
Kim JH, Guilleminault C. The nasomaxillary complex, the mandible, and sleep-disordered breathing. Sleep Breath 2011;15:185-93.
Savrun FK, Benbir B, Inan R, Kaytaz A, Kaynak H. Multi-MUP analysis of palatal muscles in healthy men. J Turk Sleep Med JTSM 2014;1:43-5.
Iber C, Ancoli-Israel S, Chesson AL, Quan SF; For the American Academy of Sleep Medicine. The AASM Manual for the Scoring of Sleep and Associated Events – Rules, Terminology and Technical Specifications. Westchester, IL: AASM; 2007.
American Academy of Sleep Medicine. International Classification of Sleep Disorders. 3rd
ed. Darien, IL: American Academy of Sleep Medicine; 2014.
Ng SS, Tam W, Chan TO, To KW, Ngai J, Chan KK, et al
. Use of Berlin questionnaire in comparison to polysomnography and ome sleep study in patients with obstructive sleep apnea. Respir Res 2019;20:40.
Kimura J. Electromyography. Eletrodiagnosis in Diseases of Nerve and Muscle Principles and Practice. Part IV. 4th
ed. Oxford: Oxford University Press; 2013. p. 339-42.
Adatepe T, Ertaş M, Adatepe NU. Pratik EMG - Kaslar, Sinirler ve Protokoller. SEP Medikal Yayınları: İstanbul; 2017.
Boe SG, Dalton BH, Harwood B, Doherty TJ, Rice CL. Inter-rater reliability of motor unit number estimates and quantitative motor unit analysis in the tibialis anterior muscle. Clin Neurophysiol 2009;120:947-52.
Podnar S. Predictive values of motor unit potential analysis in limb muscles. Clin Neurophysiol 2009;120:937-40.
Stalberg E. Methods for the quantification of conventional needle EMG. In: Stålberg E, editor. Clinical Neurophysiology of Disorders of Muscle and Neuromuscular Junction, Including Fatigue. Amsterdam: Elsevier Science; 2003. p. 213-44.
Stalberg E, Daube JR. Electromyographic methods. In: Stålberg E, editor. Clinical Neurophysiology of Disorders of Muscle and Neuromuscular Junction, Including Fatigue. Amsterdam: Elsevier Science; 2003. p. 147-85.
Bilston LE, Gandevia SC. Biomechanical properties of the human upper airway and their effect on its behavior during breathing and in obstructive sleep apnea. J Appl Physiol (1985) 2014;116:314-24.
Podnar S, Dolenc-Grosel JL. Neuropathic changes in the tongue protrude muscles in patients with snoring or obstructive sleep apnea. Neurophysiol Clin 2018;48:269-75.
Patel JA, Ray BJ, Salvador FC, Gouveia C, Zaghi S, Camacho M. Neuromuscular function of the soft palate and uvula in snoring and obstructive sleep apnea: A systematic review. Am J Otolaryngol 2018;39:327-37.
Oliven R, Cohen G, Somri M, Schwartz AR, Oliven A. Spectral analysis of peri-pharyngeal muscles' EMG in patients with OSA and healthy subjects. Respir Physiol Neurobiol 2019;260:53-7.
Dotan Y, Golibroda T, Oliven R, Netzer A, Gaitini L, Toubi A, et al
. Parameters affecting pharyngeal response to genioglossus stimulation in sleep apnoea. Eur Respir J 2011;38:338-47.
Douglas NJ, Jan MA, Yildirim N, Warren PM, Drummond PG. The effect of posture and breathing route on genioglossal electromyogram activity in normal subjects and in patients with the sleep apnea/hypopnea syndrome. Am Rev Respir Dis 1993;148:1341-5.
Cao Y, McGuire M, Liu C, Malhotra A, Ling L. Phasic respiratory modulation of pharyngeal collapsibility via neuromuscular mechanisms in rats. J Appl Physiol (1985) 2012;112:695-703.
Pawar SM, Taksande AB, Singh R. Effect of body mass index on parameters of nerve conduction study in Indian population. Indian J Physiol Pharmacol 2012;56:88-93.
Carlisle T, Carthy ER, Glasser M, Drivas P, McMillan A, Cowie MR, et al
. Upper airway factors that protect against obstructive sleep apnoea in healthy older males. Eur Respir J 2014;44:685-93.
Jadcherla SR, Hogan WJ, Shaker R. Physiology and pathophysiology of glottic reflexes and pulmonary aspiration: From neonates to adults. Semin Respir Crit Care Med 2010;31:554-60.
Trinder J, Jordan AS, Nicholas CL. Discharge properties of upper airway motor units during wakefulness and sleep. Prog Brain Res 2014;212:59-75.
Ramchandren S, Gruis KL, Chervin RD, Lisabeth L, Concannon M, Wolfe J, et al
. Hypoglossal nerve conduction findings in obstructive sleep apnea. Muscle Nerve 2010;42:257-61.
Stål PS, Johansson B. Abnormal mitochondria organization and oxidative activity in the palate muscles of long-term snorers with obstructive sleep apnea. Respiration 2012;83:407-17.
De Bellis M, Pagni F, Ronchi S, Limonta G, Gorla S, Nicoletti G, et al
. Immunohistochemical and histomorphometric study of human uvula innervation: A comparative analysis of non-snorers versus apneic snorers. Sleep Breath 2012;16:1033-40.
Bisogni V, Pengo MF, De Vito A, Maiolino G, Rossi GP, Moxham J, et al
. Electrical stimulation for the treatment of obstructive sleep apnoea: A review of the evidence. Expert Rev Respir Med 2017;11:711-20.
Chwieśko-Minarowska S, Minarowski Ł, Szewczak WA, Chyczewska E, Kuryliszyn-Moskal A. Efficacy of daytime transcutaneous electrical stimulation of the genioglossus muscle in patients with obstructive sleep apnea syndrome: Short report. Eur Arch Otorhinolaryngol 2016;273:3891-5.
[Table 1], [Table 2], [Table 3], [Table 4], [Table 5]