Electroencephalography and Clinical Neurophysiology, 1978, 45:777--784
777
© Elsevier/North-Holland Scientific Publishers, Ltd.
EMG ACTIVITY OF CRICOTHYROID AND CHIN MUSCLES DURING WAKEFULNESS AND SLEEPING IN THE SLEEP APNEA SYNDROME D. KURTZ, J. KRIEGER and J. C1. STIERLE (D.K. and J.K.) Service d'Exploration Fonctionnelle du Systdme Nerveux, HSpital Civil, Strasbourg and (J.Cl.S.) Clinique ORL, HSpital Civil, Strasbourg (France)
(Accepted for publication: May 31, 1978)
The sleep apnea syndrome is characterized by transient respiratory arrests occurring as soon as the patient falls asleep or as soon as his sleep deepens. Three types of sleep apnea are usually distinguished: central apnea, characterized by absence of respiratory gas-flow and complete cessation of the activity of the respiratory muscles; obstructive apnea, i.e., absence of respiratory gas-flow despite the persistence of thoraco-abdominal respiratory movements; mixed apnea, which is a combination of central and obstructive apnea, the former always preceding the latter (Gastaut et al. 1965; Jung and Kuhlo 1965; Duron and Tassinari 1966;Lugaresi et al. 1967; Kurtz et al. 1972). Furthermore, several authors (Kurtz et al. 1971, 1976; Schwartz and Granelet-Eprinchard 1974) emphasize the importance of hypopnea, i.e., reduction to half-value of both the respiratory gas-flow and the amplitude of thoracic and abdominal respiratory movements. In the case of obstructive respiratory arrests, the major questions concern the site and mechanism of the upper airway obstruction. On the basis of personal observations (Krieger et al. 1976; Kurtz and Krieger (1978b), we hypothesized that the site of obstruction could be the larynx and that the obstruction could be produced by impaired respiratory activity of the laryngeal muscles. Therefore we studied the direct and integrated electromyographic (EMG) activity of the cricothyroid muscle during wakefulness and during sleep apneas. The results were
compared with those obtained in the same conditions for the chin muscles.
Patients and m e t h o d s The study was based on polygraphic recording of 7 adults with respiratory arrests during sleep. The EMG of the cricothyroid (CT) was recorded in the 7 subjects during wakefulness and in 2 of them during sleep and particularly during obstructive apneas. To record the EMG of the cricothyroid, bipolar electrodes made of 2 insulated steel wires bared for 0.5 mm at their tips and inserted into a hypodermic needle were employed (Basmajian and Stecko 1962). The needle was inserted percutaneously into the CT and then withdrawn leaving the wires within the muscle because of their barbed configuration. Continuous recording was sometimes difficult because of the mobility of the larynx during swallowing and postapneic hyperventilation; but the EMG electrodes never provoked any coughing reflex. Electrodes of the same type were used to record the EMG activity of the chin muscles; in this case each wire was inserted separately and the 2 wires were 5--10 mm apart. The muscles recorded were either m. mandibularis or m. mentalis. In both cases, the direct and the instantaneously integrated EMG activities were recorded on a Dynograph 54II (Beckman) and a Reega XVI Tr (Alvar).
778
D. KURTZ ET AL.
rate. The analysis of respiration was based on measurement of the respiratory gas-flow (V air), the inspiratory (V air insp.) and
Besides the EMG, the following variables were studied second by second: EEG, EOG, b o d y movements, ECG and instantaneous heart
"--= ~.
1500
t
t
t
t
v,i,, t Inlp. | ~ 0 0 "I
{'
f
mo~i. ..
t
+
•.
! 111c
20.4.77
! I
!
Thor.
i
!
! !
Plet.
t !
l
f
i !
t t
i
:t
!
I
J
Mvt
t t
EMG Cr.-Th.
~
~
i
t t
_
Fig. 1. Phasic inspiratory reinforcements of the erieothyroid muscle during wakefulness. Inspirations are marked by arrows; expirations by dotted lines. Vair: respiratory gas-flow; Vair Insp. : integrated inspiratory volume; Vair Exp.: integrated expiratory volume; C E e o 2 : percentage of CO2 in the expired air; Thor. Plet.: thoracic impedance ptethysmography; Abd. Mvt: abdominal movements measured by a strain gauge; EMG Cr.-Th.: integrated EMG of the erieothyroid muscle. Time scale: 1 see.
LARYNGEAL AND CHIN MUSCLE ACTIVITY IN SLEEP APNEA Results
e x p i r a t o r y (V air e x p . ) v o l u m e s a n d t h e perc e n t a g e o f CO: in t h e e x p i r e d air, a n d o n t h e study of the thoracic and abdominal movements by either impedance plethysmography or strain gauge ( f o r details see K u r t z a n d Krieger 1978a). rn h~
1 I
I
i
779
(1) EMG of the CT muscle During wakefulness a t o n i c a c t i v i t y w i t h phasic inspiratory reinforcements was r e c o r d e d . T h e phasic r e i n f o r c e m e n t s t a r t e d
~
'¸
:
•
.
.
.
.
.
.
~'-=1~lllIII" lai~
':
I
hp.
o~. ...... ...JAAAAA,~,AA~AAA~........,AIA~i~ ~IIlfllIIII fill:::::~
soo..~/i _ hw~
i.i
:
II00
1 .
.
.
.
•
.
;..
;.
.....
I~A,.-ii
: i..
i i i
,:
.:
"
1
SCH,..
o-{.i~i:..i ii 4
.....
'10~
iL,..J~ll
i i
.
.
.
.
.
.
'.. .
. i.. i.... ,
,:
.
.
.
.
.
.
27.7.77
Thor.
Plet.
Abd. Mvt
EMG
Cr.-Th.
Fig. 2. Variations in the tonic and phasic CT activities of the cricothyroid muscle during hypopneas. Abbreviations as in Fig. 1. Time scale: 10 sec.
780
D. KURTZ ET AL.
2 0 0 - - 3 0 0 msec b e f o r e the o n s e t o f inspiration and began to decrease 2 0 0 - - 3 0 0 msec b e f o r e t h e following e x p i r a t i o n (Fig. 1). During hypopneas in sleeping patients,
there was at first a gradual decrease in the tonic activity with persistence o f the phasic one. L a t e r the phasic activity also decreased or even disappeared c o m p l e t e l y until n o r m a l respiration r e s u m e d {Fig. 2).
01
.,,ooII Insp. Exp. 15(}01
5~ Vair
0
.
.
.
.
.
.
.
Insp.
SCH.. •
-:
CI~302 4
::-
"10N~:
27.7.77
Thor. Pier.
Abd. Mvt
EMG
/%
Fig. 3. EMG activity of the cricothyroid muscle during obstructive apnea. Notice complete disappearance of both tonic and phasic inspiratory activity during the apnea. Abbreviations and time scale as in Fig. 2.
L A R Y N G E A L AND CHIN MUSCLE ACTIVITY IN SLEEP APNEA
In the case o f o b s t r u c t i v e apnea both the tonic and phasic activities of the CT disappeared. Even during obstructive apnea with a valve phenomenon, i.e., low expiratory out-
a~
781
puts without any subsequent inspiration (see Kurtz and Krieger 1978a), no EMG activity was recorded in the CT. The resumption of respiration was marked by the reappearance
~04
:-: . . . . . '
HOE...
li!. b
$
o 10~
20.4.77
Thor. Plat.
Abd. M vt
EMG Chin
Fig. 4. Phasic inspiratory reinforcements of the EMG of the chin muscle which disappears during obstructive apneas. Time scale and abbreviations as in Fig. 3 but the sixth channel. EMG chin: integrated EMG of the chin muscles.
782 first of the phasic inspiratory activity (for 2--3 respiratory cycles) and secondly of the tonic activity (Fig. 3). Unfortunately we did not have the opportunity to record the EMG of the CT during central apneas. (2) EMG activity o f the chin muscles In some patients a phasic inspiratory activity, sometimes superimposed upon a tonic activity, was recorded in the chin muscles during wakefulness and sleep (Fig. 4). During hypopneas and obstructive or mixed apneas there was a close correlation between the activity of the chin muscles and that of the cricothyroid; the phasic activity disappeared at the onset of apnea and resumed as soon as respiration started again. However, in certain cases this phasic inspiratory activity of the chin muscles reappeared only after a prolonged period of wakefulness.
Discussion Under normal conditions the contraction of the CT results in lengthening of the vocal cords by putting them under tension and adds to the degree of adduction. Since it does not enter directly into the opening of the glottis, the choice of this muscle for the present study may be open to criticism. However, the posterior cricoarytenoid muscle producing abduction of the vocal cord can only be reached translaryngeally, which is inappropriate for prolonged recording. During wakefulness, according to the results of several authors (Andrew 1955; Buchthal and Faaborg-Andersen 1964; Burgat-Cadilhac et al. 1972), a phasic inspiratory activity is recorded in the CT. We could not demonstrate the occurrence of a phasic expiratory activity, which was recorded by Murtagh (1945), Fink et al. (1956), Nakamura et al. (1958) and R u d o m i n (1966). Haglund (1973) noted that in the CT some m o t o r units fire with a steady frequency, whereas in the others the discharge
D. KURTZ ET AL. frequency varies with Lhe respiratory phase, some showing an increase during inspiration, others during expiration. This disagreement could in part be explained by the recent results of Sherrey and Megirian {1977) who argued for functional plasticity of the laryngeal muscles. During obstructive sleep apnea both the tonic and the inspiratory phasic activities in the CT disappear. The loss of tone is probably related to falling asleep, whereas the inhibition of the phasic inspiratory activity of the CT, despite the persistence of thoracic or diaphragmatic respiratory movements, demonstrates an impairment of the respiratory function of the laryngeal muscles. The conjunction of inhibition of inspiratory activity of the laryngeal muscles with the subsequent closing of the glottis and inspiratory depressure could produce an obstruction; only low expiratory gas-flow could pass the glottic barrier (Kurtz and Krieger 1978a). This hypothesis is reinforced by direct fiber optic examination of the vocal cords, closing of the glottis being produced by progressive closing up of the vocal cords (Krieger et al. 1976). However, these findings are in disagreement with those published by several authors. According to Gastaut et al. (1965), it is the prolapse of the tongue that produces the obstruction. Gastaut's hypothesis is supported by the results of Remmers et al. (1976) and Harper and Sauerland (1978): in the genio-glossal muscles the high voltage continuous background activity, together with transient bursts of discharges during inspirations, disappears during obstructive apneas. Furthermore the results of Schwartz and Escande {1967) and Smirne and Comi (1975) favor an obstruction of the upper airway at the pharyngeal level. Their findings are in agreement with the fiber optic observations of Weitzman et al. (1978) and Hill et al. (1978). A phasic respiratory activity was also recorded by Hill et al. (1978) in the pharyngeal muscles, and obstructive apneas were always accompanied by disappearance of that phasic activity. In addition, we demon-
LARYNGEAL AND CHIN MUSCLE ACTIVITY IN SLEEP APNEA strated a phasic inspiratory activity of the chin muscles during wakefulness and sleep and its inhibition during obstructive apneas. These results constitute some evidence of a phasic inspiratory muscle activity at the glossal, pharyngeal, laryngeal and sometimes facial levels. The role of this phasic activity is to keep the upper airway open during inspiration; its impairment at different levels may produce an obstruction at either the pharyngeal or the laryngeal level. Perhaps certain anatomical abnormalities (micrognathia, hypertrophic tonsils, narrowed upper airway) may cause variation in the site of the obstruction of the upper airways. Thus central and obstructive apneas could be considered as two different types of dissociation of muscular respiratory activity. In the central respiratory arrests the inhibition is mainly confined to a thoracic and diaphragmatic level: despite our failure to record the EMG activity of the laryngeal muscles during central apneas, it seems probable that in that case the activity of the laryngeal muscles is not sustained, because during all the central apneas we observed, the glottis remained open (Kurtz and Krieger 1978a, b). On the other hand, during obstructive apneas, as previously shown, only the phasic respiratory activity of the laryngeal or pharyngeal muscles, or both, is inhibited. This hypothesis is supported by the experimental studies undertaken by Orem et al. (1974) showing that respiratory neurons, probably related to the accessory respiratory muscles of the upper airway, completely or intermittently lose their respiratory activity during sleep. Summary The authors studied the direct and integrated EMG activities of the cricothyroid (CT) and chin muscles in 7 patients with the sleep apnea syndrome. They noted: (1) A tonic activity with phasic inspiratory reinforcements in the CT during wakefulness. (2) A decrease in the tonic activity w i t h o u t
783
any modification of the phasic inspiratory reinforcement during sleep. (3) A decrease or even disappearance of the phasic activity during sleep-induced hypopneas. (4) A complete cessation of both the tonic and the phasic activities of the CT during obstructive apneas: resumption of respiration is marked b y the reappearance first of the phasic inspiratory activity and secondly of the tonic one. (5) In some patients similar activities are recorded in the chin muscles during wakefulness, sleep and sleep apnea. These results favor possible obstruction of the upper airway at the laryngeal level: the conjunction of inhibition of the inspiratory activity of the laryngeal muscles with the subsequent closing of the glottis and inspiratory depressure could produce an obstruction.
Rdsum6 Activitd EMG des muscles crico-thyro'fdiens et de la houppe du m e n t o n au cours d'apndes induites par le sommeil
Les auteurs ~tudiant l'activit~ EMG directe et intdgrde des muscles crico-thyro~diens (CT) et de la houppe du menton chez 7 sujets pr~sentant des apn~es au cours du s o m m e i l , notent que: (1) A l'dtat de veille une activit~ tonique renforcement phasique inspiratoire est recueillie dans le CT. (2) Le sommeil entraine une diminution de l'activit~ tonique mais ne modifie pas l'activitd phasique inspiratoire. (3) Au cours d'hypopndes, l'activit~ phasique inspiratoire diminue ou dispara~t compl~tement. (4) En cas d'apndes obstructives, aucune activit~ EMG, tonique ou phasique n'est recueillie dans le CT. (5) Une ~volution similaire de l'activit~ EMG est relev~e dans les muscles de la houppe du menton chez certains sujets. Ces r~sultats sont en faveur d'une possible
784 o b s t r u c t i o n d es v o l e s a 6 r i e n n e s s u p 6 r i e u r e s au n i v e a u d u l a r y n x ; la c o n j o n c t i o n d e l ' i n h i b i tion de l'activit6 E M G des muscles laryng6s e t d e la d 6 p r e s s i o n i n s p i r a t o i r e p e u t e n t r a ~ n e r une o b s t r u c t i o n g l o t t i q u e par a d o s s e m e n t des cordes vocales.
References Andrew, B.L. The resl)iratory displacement of the larynx: a study of the innnervation of accessory respiratory muscles. J. Physiol. (Lond.), 1955, 130: 474--487. Basmajian, J.V. and Stecko, G. A new bipolar electrode for electromyography. J. appl. Physiol., 1962, 17: 849. Buchthal, F. and Faaborg-Andersen, K. Electromyography of laryngeal and respiratory muscles. Ann. Otol. (St. Louis), 1964, 73: 118--123. Burgat-Cadilhac, CI., Dapres, G., Botella, J.P. et Cadilhae, J. Les fonetions des muscles pr61aryng6s. Etude 61ectromyographique. Rev. EEG Neurophysiol., 1972, 2: 344--351. Duron, B. et Tassinari, A. Syndrome de Pickwick et syndrome cardiorespiratoire de l'ob6sit6. A p r o p o s d'une observation. J. franq. M6d. Chir. thor., 1966, 20: 207--222. Fink, B.R., Basek, M. and Epanchin, U. The mechanism of opening of the human larynx. Laryngoscope (St. Louis), 1956, 66: 410--425. Gastaut, It., Tassinari, C.A. et Duron, B. Etude polygraphique des manifestations 6pisodiques (hypniques et respiratoires) du syndrome de Pickwick. Rev. neurol., 1965, 112: 568--579. tiaglund, S. The normal electromyogram in human ericothyroid muscle. Aeta oto-laryng. (Stoekh.), 1973, 75: 448--453. Itarper, R.M. and Sauerland, E.K. The role of the tongue in sleep apnea. In: Ch. Guilleminault and W.C. Dement (Eds.), Sleep Apnea Syndromes. Kroc Foundation Series, Vol. 11. Allan R. Liss, New York, 1978: 219--234. tlill, M.W., (3uilleminault, C. and Simmons, F.B. Fiber optic and EMG studies in hypersomnia-sleep apnea syndrome. In: Ch. Guilleminault and W.C. Dement (Eds.), Sleep Apnea Syndromes. Kroc Foundation Series, Vol. 11. Allan R. Liss, New York, 1978: 249--258. ,lung, R. and Kuhlo, W. Neurophysiological studies of abnormal night sleep and the pickwickian syndrome. In: K. Akert, C. Bally and J.P. Schad6 (Eds.), Sleep Mechanisms. Progress in Brain Research, Vo]. 18. Elsevier, Amsterdam, 1965: 140- 159. Krieger, J., Kuriz, D. et Roeslin, N. Observation fibroscopique direete au cours des apn6es hypniques chez un sujet piekwickien. Nouv. Presse m6d., 1976, 5: 2890. Kurtz, l). and Krieger, J. Analysis of apnea in sleep
D. KURTZ ET AL. apnea In: Ch. Guilleminault and W.C. Demenl (Eds.), Sleep Apnea Syndromes. Kroe Foundation Series, Vol. 11. Allan R. Liss, New York, 1978: 145--159. Kurtz, D. et Krieger, J. Les arr6ts respiratoires au eours du sommeil. Rev. neurol., 1978b, 134: i 1 22. Kurtz, D., Meunier-Carus, J., Bapst-Reiter, J., Lonsdoffer, J., Michetetti, G., Benignus, E. et Rohmer, F~ Probl0mes nosologiques pos6s par certaines formes d'hypersomnie. Rev. EEG Neurophysio!., 1971, 1 : 227--230. Kurtz, D., Lonsdorfer; J., Meunier-Carus, J., Micheletti, G. et Lampert-Benignus, E. Contribution l'6tude du type et de la r6partition des apn6es au tours du syndrome de Pickwick. Rev. EEG Neurophysiol., 1972, 2: 367--378. Kurtz, D., Krieger, J. et Lonsdorfer, J. S6quences hypno-apn6"fques chez les sujets pickwickiens. Groupements apn4"fques et trains d'apn6es. Rev. EEG Neurophysiol., 1976, 6 : 6 2 - - 6 9 . Lugaresi, E., Coccagna, G. et Berti Ceroni, G. Syndrome de Pickwick et syndrome d'hypoventilation alv6olaire primaire. Rex,. neurol., 1967, 116: 678-679. Murtagh, J.A. The respiratory function of the larynx. Ann. Otol. (St. Louis), 1945, 54: 307--321. Nakamura, I., Uyeda, Y. and Sonoda, Y. Electromyographic study on respiratory movements of the intrinsic laryngeal muscles. Laryngoscope (St. Louis), 1958, 6 8 : 1 0 9 - - 1 1 9 . Orem, J., Montplaisir, ,L and Dement, W. Changes in the activity of respiratory neurons during sleep. Brain Res., 1974, 82: 309--315. Returners, J.P., De Groot, W.J. and Sauerland, E.K. Upper airway obstruction during sleep; role of the genioglossus. Clin. Res., 1976, 24: 33. Rudomin, P. The electrical activity of the ericothyroid muscles of the cat. Arch. int. Physiol. Biochim., 1966, 74: 135- 153. Schwartz, B.A. et Escande, J.P. Etude cin4radiographique de la respiration hypnique pickwickienne. Rev. neurol., 1967, 116: 677--678. Schwartz, B.A. et Granelet-Eprinchard, M.F. Traitement et surveillance des pickwiekiens: trois modes 6volutifs typiques. Rev, EEG Neurophysiol., 1974, t : '79---88. Sherrvy, J.tl. and Megirian, D. State dependence of upper airway respiratory motoneurones: functions of the cricothyroid and nasolabial muscles of the unanesthesized rat. Electroenceph. clin. Neurophysiol., 1977, 43: 218--228. Smirne, S. et Coral, G. Etude s6rigraphique des apn6es obstructives des pickwickiens. Rev. EEG Neurophysiol., 1975, 6 : 1 2 6 . Weitzman, E.D., Pollak, C.P., Borowiecki, B., Burack, B., Shprintzen, R. and Rakoff, S. The hypersomnia sleep apnea syndrome: site and mechanism of upper airway obstruction. In: Ch. GuilIeminault and W.C. Demenl (Eds.), Sleep Apnea Syndromes. Kroc Foundation Series, Vol. 11. Allan R. Liss, New York, 1978: 235--248_
777
© Elsevier/North-Holland Scientific Publishers, Ltd.
EMG ACTIVITY OF CRICOTHYROID AND CHIN MUSCLES DURING WAKEFULNESS AND SLEEPING IN THE SLEEP APNEA SYNDROME D. KURTZ, J. KRIEGER and J. C1. STIERLE (D.K. and J.K.) Service d'Exploration Fonctionnelle du Systdme Nerveux, HSpital Civil, Strasbourg and (J.Cl.S.) Clinique ORL, HSpital Civil, Strasbourg (France)
(Accepted for publication: May 31, 1978)
The sleep apnea syndrome is characterized by transient respiratory arrests occurring as soon as the patient falls asleep or as soon as his sleep deepens. Three types of sleep apnea are usually distinguished: central apnea, characterized by absence of respiratory gas-flow and complete cessation of the activity of the respiratory muscles; obstructive apnea, i.e., absence of respiratory gas-flow despite the persistence of thoraco-abdominal respiratory movements; mixed apnea, which is a combination of central and obstructive apnea, the former always preceding the latter (Gastaut et al. 1965; Jung and Kuhlo 1965; Duron and Tassinari 1966;Lugaresi et al. 1967; Kurtz et al. 1972). Furthermore, several authors (Kurtz et al. 1971, 1976; Schwartz and Granelet-Eprinchard 1974) emphasize the importance of hypopnea, i.e., reduction to half-value of both the respiratory gas-flow and the amplitude of thoracic and abdominal respiratory movements. In the case of obstructive respiratory arrests, the major questions concern the site and mechanism of the upper airway obstruction. On the basis of personal observations (Krieger et al. 1976; Kurtz and Krieger (1978b), we hypothesized that the site of obstruction could be the larynx and that the obstruction could be produced by impaired respiratory activity of the laryngeal muscles. Therefore we studied the direct and integrated electromyographic (EMG) activity of the cricothyroid muscle during wakefulness and during sleep apneas. The results were
compared with those obtained in the same conditions for the chin muscles.
Patients and m e t h o d s The study was based on polygraphic recording of 7 adults with respiratory arrests during sleep. The EMG of the cricothyroid (CT) was recorded in the 7 subjects during wakefulness and in 2 of them during sleep and particularly during obstructive apneas. To record the EMG of the cricothyroid, bipolar electrodes made of 2 insulated steel wires bared for 0.5 mm at their tips and inserted into a hypodermic needle were employed (Basmajian and Stecko 1962). The needle was inserted percutaneously into the CT and then withdrawn leaving the wires within the muscle because of their barbed configuration. Continuous recording was sometimes difficult because of the mobility of the larynx during swallowing and postapneic hyperventilation; but the EMG electrodes never provoked any coughing reflex. Electrodes of the same type were used to record the EMG activity of the chin muscles; in this case each wire was inserted separately and the 2 wires were 5--10 mm apart. The muscles recorded were either m. mandibularis or m. mentalis. In both cases, the direct and the instantaneously integrated EMG activities were recorded on a Dynograph 54II (Beckman) and a Reega XVI Tr (Alvar).
778
D. KURTZ ET AL.
rate. The analysis of respiration was based on measurement of the respiratory gas-flow (V air), the inspiratory (V air insp.) and
Besides the EMG, the following variables were studied second by second: EEG, EOG, b o d y movements, ECG and instantaneous heart
"--= ~.
1500
t
t
t
t
v,i,, t Inlp. | ~ 0 0 "I
{'
f
mo~i. ..
t
+
•.
! 111c
20.4.77
! I
!
Thor.
i
!
! !
Plet.
t !
l
f
i !
t t
i
:t
!
I
J
Mvt
t t
EMG Cr.-Th.
~
~
i
t t
_
Fig. 1. Phasic inspiratory reinforcements of the erieothyroid muscle during wakefulness. Inspirations are marked by arrows; expirations by dotted lines. Vair: respiratory gas-flow; Vair Insp. : integrated inspiratory volume; Vair Exp.: integrated expiratory volume; C E e o 2 : percentage of CO2 in the expired air; Thor. Plet.: thoracic impedance ptethysmography; Abd. Mvt: abdominal movements measured by a strain gauge; EMG Cr.-Th.: integrated EMG of the erieothyroid muscle. Time scale: 1 see.
LARYNGEAL AND CHIN MUSCLE ACTIVITY IN SLEEP APNEA Results
e x p i r a t o r y (V air e x p . ) v o l u m e s a n d t h e perc e n t a g e o f CO: in t h e e x p i r e d air, a n d o n t h e study of the thoracic and abdominal movements by either impedance plethysmography or strain gauge ( f o r details see K u r t z a n d Krieger 1978a). rn h~
1 I
I
i
779
(1) EMG of the CT muscle During wakefulness a t o n i c a c t i v i t y w i t h phasic inspiratory reinforcements was r e c o r d e d . T h e phasic r e i n f o r c e m e n t s t a r t e d
~
'¸
:
•
.
.
.
.
.
.
~'-=1~lllIII" lai~
':
I
hp.
o~. ...... ...JAAAAA,~,AA~AAA~........,AIA~i~ ~IIlfllIIII fill:::::~
soo..~/i _ hw~
i.i
:
II00
1 .
.
.
.
•
.
;..
;.
.....
I~A,.-ii
: i..
i i i
,:
.:
"
1
SCH,..
o-{.i~i:..i ii 4
.....
'10~
iL,..J~ll
i i
.
.
.
.
.
.
'.. .
. i.. i.... ,
,:
.
.
.
.
.
.
27.7.77
Thor.
Plet.
Abd. Mvt
EMG
Cr.-Th.
Fig. 2. Variations in the tonic and phasic CT activities of the cricothyroid muscle during hypopneas. Abbreviations as in Fig. 1. Time scale: 10 sec.
780
D. KURTZ ET AL.
2 0 0 - - 3 0 0 msec b e f o r e the o n s e t o f inspiration and began to decrease 2 0 0 - - 3 0 0 msec b e f o r e t h e following e x p i r a t i o n (Fig. 1). During hypopneas in sleeping patients,
there was at first a gradual decrease in the tonic activity with persistence o f the phasic one. L a t e r the phasic activity also decreased or even disappeared c o m p l e t e l y until n o r m a l respiration r e s u m e d {Fig. 2).
01
.,,ooII Insp. Exp. 15(}01
5~ Vair
0
.
.
.
.
.
.
.
Insp.
SCH.. •
-:
CI~302 4
::-
"10N~:
27.7.77
Thor. Pier.
Abd. Mvt
EMG
/%
Fig. 3. EMG activity of the cricothyroid muscle during obstructive apnea. Notice complete disappearance of both tonic and phasic inspiratory activity during the apnea. Abbreviations and time scale as in Fig. 2.
L A R Y N G E A L AND CHIN MUSCLE ACTIVITY IN SLEEP APNEA
In the case o f o b s t r u c t i v e apnea both the tonic and phasic activities of the CT disappeared. Even during obstructive apnea with a valve phenomenon, i.e., low expiratory out-
a~
781
puts without any subsequent inspiration (see Kurtz and Krieger 1978a), no EMG activity was recorded in the CT. The resumption of respiration was marked by the reappearance
~04
:-: . . . . . '
HOE...
li!. b
$
o 10~
20.4.77
Thor. Plat.
Abd. M vt
EMG Chin
Fig. 4. Phasic inspiratory reinforcements of the EMG of the chin muscle which disappears during obstructive apneas. Time scale and abbreviations as in Fig. 3 but the sixth channel. EMG chin: integrated EMG of the chin muscles.
782 first of the phasic inspiratory activity (for 2--3 respiratory cycles) and secondly of the tonic activity (Fig. 3). Unfortunately we did not have the opportunity to record the EMG of the CT during central apneas. (2) EMG activity o f the chin muscles In some patients a phasic inspiratory activity, sometimes superimposed upon a tonic activity, was recorded in the chin muscles during wakefulness and sleep (Fig. 4). During hypopneas and obstructive or mixed apneas there was a close correlation between the activity of the chin muscles and that of the cricothyroid; the phasic activity disappeared at the onset of apnea and resumed as soon as respiration started again. However, in certain cases this phasic inspiratory activity of the chin muscles reappeared only after a prolonged period of wakefulness.
Discussion Under normal conditions the contraction of the CT results in lengthening of the vocal cords by putting them under tension and adds to the degree of adduction. Since it does not enter directly into the opening of the glottis, the choice of this muscle for the present study may be open to criticism. However, the posterior cricoarytenoid muscle producing abduction of the vocal cord can only be reached translaryngeally, which is inappropriate for prolonged recording. During wakefulness, according to the results of several authors (Andrew 1955; Buchthal and Faaborg-Andersen 1964; Burgat-Cadilhac et al. 1972), a phasic inspiratory activity is recorded in the CT. We could not demonstrate the occurrence of a phasic expiratory activity, which was recorded by Murtagh (1945), Fink et al. (1956), Nakamura et al. (1958) and R u d o m i n (1966). Haglund (1973) noted that in the CT some m o t o r units fire with a steady frequency, whereas in the others the discharge
D. KURTZ ET AL. frequency varies with Lhe respiratory phase, some showing an increase during inspiration, others during expiration. This disagreement could in part be explained by the recent results of Sherrey and Megirian {1977) who argued for functional plasticity of the laryngeal muscles. During obstructive sleep apnea both the tonic and the inspiratory phasic activities in the CT disappear. The loss of tone is probably related to falling asleep, whereas the inhibition of the phasic inspiratory activity of the CT, despite the persistence of thoracic or diaphragmatic respiratory movements, demonstrates an impairment of the respiratory function of the laryngeal muscles. The conjunction of inhibition of inspiratory activity of the laryngeal muscles with the subsequent closing of the glottis and inspiratory depressure could produce an obstruction; only low expiratory gas-flow could pass the glottic barrier (Kurtz and Krieger 1978a). This hypothesis is reinforced by direct fiber optic examination of the vocal cords, closing of the glottis being produced by progressive closing up of the vocal cords (Krieger et al. 1976). However, these findings are in disagreement with those published by several authors. According to Gastaut et al. (1965), it is the prolapse of the tongue that produces the obstruction. Gastaut's hypothesis is supported by the results of Remmers et al. (1976) and Harper and Sauerland (1978): in the genio-glossal muscles the high voltage continuous background activity, together with transient bursts of discharges during inspirations, disappears during obstructive apneas. Furthermore the results of Schwartz and Escande {1967) and Smirne and Comi (1975) favor an obstruction of the upper airway at the pharyngeal level. Their findings are in agreement with the fiber optic observations of Weitzman et al. (1978) and Hill et al. (1978). A phasic respiratory activity was also recorded by Hill et al. (1978) in the pharyngeal muscles, and obstructive apneas were always accompanied by disappearance of that phasic activity. In addition, we demon-
LARYNGEAL AND CHIN MUSCLE ACTIVITY IN SLEEP APNEA strated a phasic inspiratory activity of the chin muscles during wakefulness and sleep and its inhibition during obstructive apneas. These results constitute some evidence of a phasic inspiratory muscle activity at the glossal, pharyngeal, laryngeal and sometimes facial levels. The role of this phasic activity is to keep the upper airway open during inspiration; its impairment at different levels may produce an obstruction at either the pharyngeal or the laryngeal level. Perhaps certain anatomical abnormalities (micrognathia, hypertrophic tonsils, narrowed upper airway) may cause variation in the site of the obstruction of the upper airways. Thus central and obstructive apneas could be considered as two different types of dissociation of muscular respiratory activity. In the central respiratory arrests the inhibition is mainly confined to a thoracic and diaphragmatic level: despite our failure to record the EMG activity of the laryngeal muscles during central apneas, it seems probable that in that case the activity of the laryngeal muscles is not sustained, because during all the central apneas we observed, the glottis remained open (Kurtz and Krieger 1978a, b). On the other hand, during obstructive apneas, as previously shown, only the phasic respiratory activity of the laryngeal or pharyngeal muscles, or both, is inhibited. This hypothesis is supported by the experimental studies undertaken by Orem et al. (1974) showing that respiratory neurons, probably related to the accessory respiratory muscles of the upper airway, completely or intermittently lose their respiratory activity during sleep. Summary The authors studied the direct and integrated EMG activities of the cricothyroid (CT) and chin muscles in 7 patients with the sleep apnea syndrome. They noted: (1) A tonic activity with phasic inspiratory reinforcements in the CT during wakefulness. (2) A decrease in the tonic activity w i t h o u t
783
any modification of the phasic inspiratory reinforcement during sleep. (3) A decrease or even disappearance of the phasic activity during sleep-induced hypopneas. (4) A complete cessation of both the tonic and the phasic activities of the CT during obstructive apneas: resumption of respiration is marked b y the reappearance first of the phasic inspiratory activity and secondly of the tonic one. (5) In some patients similar activities are recorded in the chin muscles during wakefulness, sleep and sleep apnea. These results favor possible obstruction of the upper airway at the laryngeal level: the conjunction of inhibition of the inspiratory activity of the laryngeal muscles with the subsequent closing of the glottis and inspiratory depressure could produce an obstruction.
Rdsum6 Activitd EMG des muscles crico-thyro'fdiens et de la houppe du m e n t o n au cours d'apndes induites par le sommeil
Les auteurs ~tudiant l'activit~ EMG directe et intdgrde des muscles crico-thyro~diens (CT) et de la houppe du menton chez 7 sujets pr~sentant des apn~es au cours du s o m m e i l , notent que: (1) A l'dtat de veille une activit~ tonique renforcement phasique inspiratoire est recueillie dans le CT. (2) Le sommeil entraine une diminution de l'activit~ tonique mais ne modifie pas l'activitd phasique inspiratoire. (3) Au cours d'hypopndes, l'activit~ phasique inspiratoire diminue ou dispara~t compl~tement. (4) En cas d'apndes obstructives, aucune activit~ EMG, tonique ou phasique n'est recueillie dans le CT. (5) Une ~volution similaire de l'activit~ EMG est relev~e dans les muscles de la houppe du menton chez certains sujets. Ces r~sultats sont en faveur d'une possible
784 o b s t r u c t i o n d es v o l e s a 6 r i e n n e s s u p 6 r i e u r e s au n i v e a u d u l a r y n x ; la c o n j o n c t i o n d e l ' i n h i b i tion de l'activit6 E M G des muscles laryng6s e t d e la d 6 p r e s s i o n i n s p i r a t o i r e p e u t e n t r a ~ n e r une o b s t r u c t i o n g l o t t i q u e par a d o s s e m e n t des cordes vocales.
References Andrew, B.L. The resl)iratory displacement of the larynx: a study of the innnervation of accessory respiratory muscles. J. Physiol. (Lond.), 1955, 130: 474--487. Basmajian, J.V. and Stecko, G. A new bipolar electrode for electromyography. J. appl. Physiol., 1962, 17: 849. Buchthal, F. and Faaborg-Andersen, K. Electromyography of laryngeal and respiratory muscles. Ann. Otol. (St. Louis), 1964, 73: 118--123. Burgat-Cadilhac, CI., Dapres, G., Botella, J.P. et Cadilhae, J. Les fonetions des muscles pr61aryng6s. Etude 61ectromyographique. Rev. EEG Neurophysiol., 1972, 2: 344--351. Duron, B. et Tassinari, A. Syndrome de Pickwick et syndrome cardiorespiratoire de l'ob6sit6. A p r o p o s d'une observation. J. franq. M6d. Chir. thor., 1966, 20: 207--222. Fink, B.R., Basek, M. and Epanchin, U. The mechanism of opening of the human larynx. Laryngoscope (St. Louis), 1956, 66: 410--425. Gastaut, It., Tassinari, C.A. et Duron, B. Etude polygraphique des manifestations 6pisodiques (hypniques et respiratoires) du syndrome de Pickwick. Rev. neurol., 1965, 112: 568--579. tiaglund, S. The normal electromyogram in human ericothyroid muscle. Aeta oto-laryng. (Stoekh.), 1973, 75: 448--453. Itarper, R.M. and Sauerland, E.K. The role of the tongue in sleep apnea. In: Ch. Guilleminault and W.C. Dement (Eds.), Sleep Apnea Syndromes. Kroc Foundation Series, Vol. 11. Allan R. Liss, New York, 1978: 219--234. tlill, M.W., (3uilleminault, C. and Simmons, F.B. Fiber optic and EMG studies in hypersomnia-sleep apnea syndrome. In: Ch. Guilleminault and W.C. Dement (Eds.), Sleep Apnea Syndromes. Kroc Foundation Series, Vol. 11. Allan R. Liss, New York, 1978: 249--258. ,lung, R. and Kuhlo, W. Neurophysiological studies of abnormal night sleep and the pickwickian syndrome. In: K. Akert, C. Bally and J.P. Schad6 (Eds.), Sleep Mechanisms. Progress in Brain Research, Vo]. 18. Elsevier, Amsterdam, 1965: 140- 159. Krieger, J., Kuriz, D. et Roeslin, N. Observation fibroscopique direete au cours des apn6es hypniques chez un sujet piekwickien. Nouv. Presse m6d., 1976, 5: 2890. Kurtz, l). and Krieger, J. Analysis of apnea in sleep
D. KURTZ ET AL. apnea In: Ch. Guilleminault and W.C. Demenl (Eds.), Sleep Apnea Syndromes. Kroe Foundation Series, Vol. 11. Allan R. Liss, New York, 1978: 145--159. Kurtz, D. et Krieger, J. Les arr6ts respiratoires au eours du sommeil. Rev. neurol., 1978b, 134: i 1 22. Kurtz, D., Meunier-Carus, J., Bapst-Reiter, J., Lonsdoffer, J., Michetetti, G., Benignus, E. et Rohmer, F~ Probl0mes nosologiques pos6s par certaines formes d'hypersomnie. Rev. EEG Neurophysio!., 1971, 1 : 227--230. Kurtz, D., Lonsdorfer; J., Meunier-Carus, J., Micheletti, G. et Lampert-Benignus, E. Contribution l'6tude du type et de la r6partition des apn6es au tours du syndrome de Pickwick. Rev. EEG Neurophysiol., 1972, 2: 367--378. Kurtz, D., Krieger, J. et Lonsdorfer, J. S6quences hypno-apn6"fques chez les sujets pickwickiens. Groupements apn4"fques et trains d'apn6es. Rev. EEG Neurophysiol., 1976, 6 : 6 2 - - 6 9 . Lugaresi, E., Coccagna, G. et Berti Ceroni, G. Syndrome de Pickwick et syndrome d'hypoventilation alv6olaire primaire. Rex,. neurol., 1967, 116: 678-679. Murtagh, J.A. The respiratory function of the larynx. Ann. Otol. (St. Louis), 1945, 54: 307--321. Nakamura, I., Uyeda, Y. and Sonoda, Y. Electromyographic study on respiratory movements of the intrinsic laryngeal muscles. Laryngoscope (St. Louis), 1958, 6 8 : 1 0 9 - - 1 1 9 . Orem, J., Montplaisir, ,L and Dement, W. Changes in the activity of respiratory neurons during sleep. Brain Res., 1974, 82: 309--315. Returners, J.P., De Groot, W.J. and Sauerland, E.K. Upper airway obstruction during sleep; role of the genioglossus. Clin. Res., 1976, 24: 33. Rudomin, P. The electrical activity of the ericothyroid muscles of the cat. Arch. int. Physiol. Biochim., 1966, 74: 135- 153. Schwartz, B.A. et Escande, J.P. Etude cin4radiographique de la respiration hypnique pickwickienne. Rev. neurol., 1967, 116: 677--678. Schwartz, B.A. et Granelet-Eprinchard, M.F. Traitement et surveillance des pickwiekiens: trois modes 6volutifs typiques. Rev, EEG Neurophysiol., 1974, t : '79---88. Sherrvy, J.tl. and Megirian, D. State dependence of upper airway respiratory motoneurones: functions of the cricothyroid and nasolabial muscles of the unanesthesized rat. Electroenceph. clin. Neurophysiol., 1977, 43: 218--228. Smirne, S. et Coral, G. Etude s6rigraphique des apn6es obstructives des pickwickiens. Rev. EEG Neurophysiol., 1975, 6 : 1 2 6 . Weitzman, E.D., Pollak, C.P., Borowiecki, B., Burack, B., Shprintzen, R. and Rakoff, S. The hypersomnia sleep apnea syndrome: site and mechanism of upper airway obstruction. In: Ch. GuilIeminault and W.C. Demenl (Eds.), Sleep Apnea Syndromes. Kroc Foundation Series, Vol. 11. Allan R. Liss, New York, 1978: 235--248_
