- Email: [email protected]
The pattern of swallowing during sleep
Electroencephalography and Clinical Neurophysiology, 1975, 38:427-432 Elsevier Scientific Publishing Company, Amsterdam - Printed in The Netherlands
LABORATORY
427
NOTE
T H E P A T T E R N OF S W A L L O W I N G D U R I N G SLEEP | . LICHTER 1 AND R. C. MUIR
Department of Surgery, University of Ota9o Medical School, Dunedin (New Zealand) (Accepted for publication: November 13, 1974)
A study of the pattern of swallowing during sleep was prompted by an earlier investigation concerned with the measurement of nocturnal gastroesophageal reflux (Lichter 1974). In patients with reflux esophagitis, special problems arise in the clearance of reflux from the esophagus by swallowing. Booth et al. (1968) measured the number of swallows required to clear 15 ml of 0.1 HCI from the esophagus in 21 normal subjects and found that clearance was achieved in 10 swallows or less. In symptomatic patients with abnormal gastroesophageal reflux or esophagitis, acid clearing required many more swallows. This prolongation of clearance is associated with motor abnormalities found to occur in patients with esophagitis (Siegel and Hendrix 1963; Olsen and Schlegel 1965). The role of swallowing therefore assumes particular importance in the clearance of damaging gastroesophageal relux from the esophagus. The previous investigation (Lichter 1974) involved continuous measurement of intra-esophageal pH by means of a pH electrode, to which were taped fine polythene tubes for recording intra-esophageal pressures. It was noted that there were considerable periods during which no swallowing took place, and that during these periods refluxed material persisted within the esophagus. It was concluded that nocturnal reflux was particularly damaging because of the infrequency of swallowing during sleep. It was also observed that at periodic intervals, bursts of swallows occurred which cleared the acid reflux. The episodic occurrence of swallowing suggested that swallowing might be sleep-stage related. There are many examples of physiological variables that show fluctuations during sleep. A relationship of swallowing to REM sleep as part of the general physiological activation therefore seemed a reasonable hypothesis and the present study was designed to determine the pattern of swallowing and its relationship to the stages of sleep. METHOD Ten normal subjects (5 male and 5 female) ranging in age from 21 to 26 years were studied. The subjects had taken no hypnotics, sedatives or tranquillizers that might affect sleep, and enquiry confirmed that none had sleep disturbances or a history of psychiatric illness. The subjects were asked not i Supported by a Golden Kiwi Grant.
to undertake vigorous exercise after 8 p.m. and to avoid consumption of alcohol. They arrived at the laboratory at l0 p.m. after a normal day's work. Studies were carried out on 2 successive nights beginning at 11 p.m. and terminating at 7 a.m. the following morning. Swallow signals were recorded and the stages of sleep were defined by EEG, EOG, EMG and a body movement sensor, and recorded continuously overnight on an 8channel Grass Polygraph recorder. The terminology, criteria and techniques used for defining the stages of sleep, and of movement arousal, movement time and body movement, were those recommended in "A manual of standardized
terminology, techniques and scoring system for sleep stages of human subjects" (Rechtschaffen and Kales 1968). The Manual defines movement arousal as follows:
Movement arousal (MA): Any increase in EMG on any channel, which is accompanied by a change in pattern on any additional channel. For EMG channcls, the change in pattern may consist of either an increase in amplitude of the EMG signal or an amplifier blocking artifact. For EOG channels, the change of pattern may consist of either the occurrence of EMG activity, amplifier blocking artifacts or blink artifacts. For EEG channels, the change may consist of either a decrease in amplitude, an increase in alpha activity, a paroxysmal burst of high voltage activity, the presence of EMG activity, or amplifier blocking artifacts. Movement arousals are not used as epoch scores. The major purpose in defining movement arousal has been to aid in the scoring of stages by signalling the possibility that the continuity of the prevailing sleep stage has been disturbed in some way. Movement arousal need indicate only some increase in muscle activity and does not necessarily involve the substantial special displacement of the body which is implied by body movement. Movement arousal could r¢sult from an isolated small muscle contraction, a vigorous blink, or a facial grimace. To monitor the act of swallowing, a new instrument had to be devised, as previously described external devices for recording swallows (Kincaid 1951; Kydd and Neff 1964; Lear et al. 1965) were either too cumbersome or did not produce a signal that could readily be recorded alongside the parameters for sleep. An instrument using the Doppler principle (Sonicaid Fetal Heart Monitor) was adapted. The sensor was attached to the neck in the region of the larynx to
428
~. LICHTER AND R. C. MUIR
/% L~DM N
~m
,IW~-,IWF-'.'~I"
fin
--D'*. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
ll
.....................................................................................................
---~,
E
..........................
Fig. I. A swallow associated with a movement arousal (MA) in Stage R E M . The EEG, E O G and E M G tracings show evidence of movement arousal. A body movement (BM) is recorded with the m o v e m e n t arousal. Abbreviations: SM, swallow movement tracing: SW, swallow. TABLE I The n u m b e r a n d the rate of m o v e m e n t arousals (MA) and o f swallows (SW) per epoch in each stage o f sleep for each of 10 subject nights. Stages of sleep 1
2
Patient 1 (Epochs) No. o f M A No. of SW No. of M A and SW Rate M A Rate SW
65 0 3 18 0.277 0.323
401 1 3 8 0.022 0.027
Patient 2 (Epochs) No. of M A No. of SW No. of M A and SW Rate M A Rate SW
43 6 2 1 0.163 0.070
361 1 1 8 0.025 0.025
Patient 3 (Epochs) No. of M A
72 13
338 11
3
4
REM
61 1 1 2 0.049 0.049
121 1 1 1
257 4 8 18 0.086 0.101
105 0 1 1 0.010 0.019
73 1 0 0
205 5 1 6 0.054 0.034
92 3
109 0
84 4
429
THE PATTERN OF SWALLOWING DURING SLEEP No. of SW No. of MA and SW Rate MA Rate SW
1 8 0.292 0.125
3 13 0.071 0.047
3 3 0.065 0.065
Patient 4 (Epochs) No. of MA No. of SW No. of MA and SW Rate MA Rate SW
65 2 1 2 0.062 0.046
306 15 1 15 0.098 0.052
132 4 2 6 0.075 0.061
129 2 0 1
149 4 1 11 0.101 0.081
Patient 5 (Epochs) No. of MA No. of SW No. of MA and SW Rate MA Rate SW
51 15 0 4 0.373 0.078
407 8 0 6 0.034 0.015
139 1 0 2 0.022 0.014
83 1 0 0
201 10 0 6 0.080 0.030
Patient 6 (Epochs) No. of MA No. of SW No. of MA and SW Rate MA Rate SW
62 5 0 9 0.226 0.145
409 8 4 22 0.073 0.064
71 1 1 3 0.056 0.056
90 0 0 0
248 9 4 20 0.117 0.097
Patient 7 (Epochs) No. of MA No. of SW No. of MA and SW Rate MA Rate SW
34 7 1 4 0.324 0.147
502 14 1 18 0.064 0.038
125 3 0 3 0.048 0.024
27 0 0 0
224 9 0 4 0.058 0.018
Patient 8 (Epochs) No. of MA No. of SW No. of MA and SW Rate MA Rate SW
29 5 0 4 0.310 0.138
314 14 0 12 0.083 0.038
153 5 0 5 0.065 0.033
88 5 1 2
249 5 0 12 0.068 0.048
Patient 9 (Epochs) No. of MA No. of SW No. of MA and SW Rate MA Rate SW
45 6 0 9 0.333 0.200
258 5 1 14 0.074 0.058
187 5 0 7 0.064 0.037
156 2 0 2
246 15 1 12 0.110 0.053
Patient 10 (Epochs) No. of MA No. of SW No. of MA and SW Rate MA Rate SW
63 17 1 28 0.714 0.460
426 28 0 20 0.112 0.047
67 4 1 1 0.075 0.030
106 1 1 1
222 55 1 14 0.311 0.068
4 4 0.095 0.095
430
~. LICHTER AND R. C. MUIR MOVEMENT AROUSALS M,Aa-MA with slioht movements F i MA. with m a j o r i:;~cly m o v e m e n t s I movement time
W
/
a,
LrLIj l
7
o
lit,Ill,
, ,
J
,
,= , I
, ,I I
II ,I t l.
,i
II,
,I, g,l.,
II
, II
II
li
.It
U .
I
i~
II
II
I
movement arousals
,I I,I, IlL I 2
I 0
IJ,I 60
l 120
I
U
180 time in
240
Jill 300
It 360
tl
ID,
no
of swallows
420
minutes
Fig. 2. The relationship of swallows to movement ~.rousals and the stages of sleep is shown in one of the subjects studied. record signals produced by laryngeal movements and the sounds produced by swallowing. Its reliability was checked against intraluminal esophageal pressure recordings and these showed that a reproducible distinctive signal pattern was obtained. To check the validity of the recordings, subjects were observed throughout the night to relate the events observed (body movements, wakefulness or sleep, swallows) with the recordings made. The Doppler system for recording swallows was monitored through headphones, when a characteristic sound was produced which was related to a distinct recorded pattern on the chart. This could readily be differentiated from deflectionscaused by movements and sounds other than those produced by swallowing.
paniment of movement arousals associated with swallows. Movement arousals occurred not only between, but during sleep stages; they were not evenly distributed througout the stages of sleep~most occurring in Stages REM, 1 and 2 (Fig. 2). Of the swallows during a night's sleep 33.3 ~ occurred in Stage REM, 20.2~o in Stage 1, and 31.70 in Stage 2. The number and the rate of movement arousals and of swallows per epoch in each stage of sleep for each of 10 subject nights is shown in Table I. There is an association between movement arousals and swallows in sleep Stages 1, 2, 3 and REM. Stage 4 has been excluded from the statistical analysis because of the small number of swallows recorded (See Table II).
RESULTS
DISCUSSION
The average number of swallows per hour in the subjects studied, on each of 2 consecutive nights, ranged between 2.1 and 9.1 swallows per hour (average 5.8). For each individual the number of swallows varied little on the 2 nights. To avoid any "first-night effect" (Agnew et al. 1966) only the results of second night studies were further considered. The overnight studies showed that swallowing was associated with movement arousals (Fig. 1). The polygraphic records showed a delay between the onset of movement arousal and the act of swallowing. Movement arousals occurred in only a small proportion of the total number of epochs (8.2 ~), but swallows occurred during a significant proportion of movement arousals (range 41.7-87.3 ~ ; average 60.7~). Body movements were not a necessary accom-
The number of swallows per hour recorded in our study is similar to that reported in an investigation conducted in 1965 by Lear et al. They reported that during sleep there were always intervals when swallowing was absent for long periods (mean duration 30.3 min), the average number of such periods being seven per night. No previous study has related the pattern of swallowing to the stages of sleep or to a specific event during sleep. Our investigation demonstrated that swallowing during sleep was associated with movement arousal. A possible explanation of this association may be that stimuli that give rise to the swallowing reflex may themselves affect and modulate the nightly progression of sleep stages. Swallows might then be related to sleep stages, and the first indication of a swallow
431
THE PATTERN OF SWALLOWING DURING SLEEP TABLE II
Comparison of the observed association between movement arousals (MA) and swallows (SW) and the expected association between M A and SW as derived from a Poisson distribution. Patients
Types of sleep 1
1 2 3 4 5 6 7 8 9 10
2
3
REM
Obs.
Exp.
P*
Obs.
Exp.
P*
Obs.
Exp.
P*
Obs.
Exp.
P*
18 1 8 2 4 9 4 4 9 28
5.8 0.5 2.6 0.2 1.5 2.0 1.6 1.2 3.0 20.7
0.0001 0.4*** 0.01 0.02 0.06*** 0.001 0.1"** 0.04 0.01 0.03
8 8 13 15 6 22 18 12 14 20
0.2 0.2 1.1 1.6 0.2 1.9 1.2 1.0 1.1 2.2
0.000001 0.000001 0.000001 0.000001 0.000001 0.000001 0.000001 0.000001 0.000001 0.000001
2 1 3 6 2 3 3 5 7 1
0.1 0.0 0.4 0.6 0.0 0.2 0.1 0.3 0.4 0.1
0.01 ? 0.01 0.00001 0.01"* 0.01 0.001 0.001 0.000001 0.1"**
18 6 4 11 6 20 4 12 12 14
2.2 0.4 0.8 1.2 0.5 2.8 0.2 0.8 1.4 4.7
0.000001 0.00001 0.01 0.000001 0.0001 0.00001 0.0001 0.000001 0.000001 0.001
* P < Probability that the number in the "observed" column (Obs.) or a larger number could be obtained from a Poisson distribution with a mean as given in the "expected" column (Exp.). ** The expected value has been corrected to 1 decimal place and it is still possible in this case togive an upper limit to P. *** These results are not significant at the 5 % (P< 0.05) level. t The expected value is too small for a reliable estimat~ of the upper limit of P to be obtained except that P < 0.1. response may be a movement arousal. On the other hand there may be a direct relationship between sleep stages and movement arousals, with swallows associated with movement arousals ; the relationship between swallows and sleep stages would then qe indirect. Movement arousals occurred largely during sleep stages, being most frequent on Stages REM, 1 and 2. Such a direct relationship would suggest that there may be more significance to movement arousal than the mere signalling of a change o f sleep stage. The frequency o f swallowing, and in particular the long periods when no swallowing takes place, directly bears on the problem o f the degree o f damage caused to the esophagus by gastroesophageal reflux. Reflux persists in the esophagus until cleared by swallowing, and the major damage occurring in this condition probably takes place in sleep during the "no-swallow" periods. Factors which enhance delta sleep, such as sleep deprivation would tend to prolong the intervals between swallows; drugs that affect the depth of sleep may have a similar effect. It can also be postulated that hypnotics and other drugs that reduce the RE M component of sleep may significantly reduce the number of movement arousals (frequent in Stage REM) and the number of swallows during sleep. There is, however. no information in the literature on the direct effect o f drugs on movement arousal. This situation probably arises from the fact that movement arousals have not heretofore been associated with any physiological events.
by means of EEG, EOG and EMG, and swallowing was monitored by means o f an external sensing device attached to the neck. It was found that during sleep, swallowing is episodic, with long swallow-free periods. Swallows occur almost exclusively in association with movement arousals which are most frequent during Stages REM, 1 and 2 of sleep. RESUME LE CYCLE D ' A V A L E M E N T P E N D A N T LE S O M M E I L La structure d'avalement dans le sommeil a 6t6 recherch6 par une 6tude de 10 sujets normaux. Le cycle du sommeil fut classifi6 par moyen de I'EEG, I'EOG et I'EMG, et l'avalement rut contr616 par moyen d'un appareil sensim~tre attach6 au COU.
On a trouv6 que dans le sommeil, l'avalement est episodique avec des longues periodes sans avalement. Les avalements se produisent presque exclusivement avec des mouvements de r6veil, lesquels sont plus fr6quents pendant les phases REM, 1 et 2 du sommeil. We wish to acknowledge the help and advice of Dr. David Marks of the Department of Psychology, University of Otago, and the technical assistance of Mr. Leslie Wong of the Otago Hospital Board. We are grateful to Dr. D. C. E. Manley of the Department of Preventive and Social Medicine for the statistical analysis.
SUMMARY REFERENCES The pattern of swallowing during sleep was investigated by means of a study in 10 normal subjects. Sleep was staged
AGNEW,H. W., WEBB, W. B. and WILLIAMS, R. L. The first
432 night effect: an EEG study of sleep. Psychophysiology, 1966, 2: 263-266. BOOTH, D. J., KEMMERER, W. T. and SKINNER, D. B. Acid clearing from the distal esophagus. Arch. Sur9., 1968, 96 : 731-734. KINCAID, R. N. Frequency of deglutition in man: its relation to overbite. Angle Orthodont., 1951, 21: 34-43. KYDD, W. L. and NE~, C. W. Frequency of deglutition of tongue thrusters compared to a sample population of normal swallowers. J. dent. Res., 1964, 43: 363-369. LEAR, C. S. C., FLANAGAt~,J. B. J. and MOORREZS,C. F. A. The frequency of deglutition in man. Arch. oral Biol., 1965, 10: 83-100.
i. LICHTER AND R. C. MUIR LICHTER, I. Measurement of gastro-oesophageal acid reflux : significance in hiatus hernia. Brit. J. Surg., 1974, 61: 253-258. OLSEN, A. M. and SCHLEGEL, J. F. Motility disturbances caused by oesophagitis. J. thorac, cardiovasc. Surg., 1965, 50: 607-712. RECHTSCHAFFEN, A. and KALES, A. A manual of standardiz, ed terminology, techniques and scoring system Jor sleep stages of human subjects. U.S. Department of Health, Education and Welfare, Publication No. 204, Bethesda, Md., 1968. SIEGEL, C. I. and HENDRIX, T. R. Esophageal motor abnormalities induced by acid perfusion in patients with heartburn, J. clin. Invest., 1963, 42: 686-695.
LABORATORY
427
NOTE
T H E P A T T E R N OF S W A L L O W I N G D U R I N G SLEEP | . LICHTER 1 AND R. C. MUIR
Department of Surgery, University of Ota9o Medical School, Dunedin (New Zealand) (Accepted for publication: November 13, 1974)
A study of the pattern of swallowing during sleep was prompted by an earlier investigation concerned with the measurement of nocturnal gastroesophageal reflux (Lichter 1974). In patients with reflux esophagitis, special problems arise in the clearance of reflux from the esophagus by swallowing. Booth et al. (1968) measured the number of swallows required to clear 15 ml of 0.1 HCI from the esophagus in 21 normal subjects and found that clearance was achieved in 10 swallows or less. In symptomatic patients with abnormal gastroesophageal reflux or esophagitis, acid clearing required many more swallows. This prolongation of clearance is associated with motor abnormalities found to occur in patients with esophagitis (Siegel and Hendrix 1963; Olsen and Schlegel 1965). The role of swallowing therefore assumes particular importance in the clearance of damaging gastroesophageal relux from the esophagus. The previous investigation (Lichter 1974) involved continuous measurement of intra-esophageal pH by means of a pH electrode, to which were taped fine polythene tubes for recording intra-esophageal pressures. It was noted that there were considerable periods during which no swallowing took place, and that during these periods refluxed material persisted within the esophagus. It was concluded that nocturnal reflux was particularly damaging because of the infrequency of swallowing during sleep. It was also observed that at periodic intervals, bursts of swallows occurred which cleared the acid reflux. The episodic occurrence of swallowing suggested that swallowing might be sleep-stage related. There are many examples of physiological variables that show fluctuations during sleep. A relationship of swallowing to REM sleep as part of the general physiological activation therefore seemed a reasonable hypothesis and the present study was designed to determine the pattern of swallowing and its relationship to the stages of sleep. METHOD Ten normal subjects (5 male and 5 female) ranging in age from 21 to 26 years were studied. The subjects had taken no hypnotics, sedatives or tranquillizers that might affect sleep, and enquiry confirmed that none had sleep disturbances or a history of psychiatric illness. The subjects were asked not i Supported by a Golden Kiwi Grant.
to undertake vigorous exercise after 8 p.m. and to avoid consumption of alcohol. They arrived at the laboratory at l0 p.m. after a normal day's work. Studies were carried out on 2 successive nights beginning at 11 p.m. and terminating at 7 a.m. the following morning. Swallow signals were recorded and the stages of sleep were defined by EEG, EOG, EMG and a body movement sensor, and recorded continuously overnight on an 8channel Grass Polygraph recorder. The terminology, criteria and techniques used for defining the stages of sleep, and of movement arousal, movement time and body movement, were those recommended in "A manual of standardized
terminology, techniques and scoring system for sleep stages of human subjects" (Rechtschaffen and Kales 1968). The Manual defines movement arousal as follows:
Movement arousal (MA): Any increase in EMG on any channel, which is accompanied by a change in pattern on any additional channel. For EMG channcls, the change in pattern may consist of either an increase in amplitude of the EMG signal or an amplifier blocking artifact. For EOG channels, the change of pattern may consist of either the occurrence of EMG activity, amplifier blocking artifacts or blink artifacts. For EEG channels, the change may consist of either a decrease in amplitude, an increase in alpha activity, a paroxysmal burst of high voltage activity, the presence of EMG activity, or amplifier blocking artifacts. Movement arousals are not used as epoch scores. The major purpose in defining movement arousal has been to aid in the scoring of stages by signalling the possibility that the continuity of the prevailing sleep stage has been disturbed in some way. Movement arousal need indicate only some increase in muscle activity and does not necessarily involve the substantial special displacement of the body which is implied by body movement. Movement arousal could r¢sult from an isolated small muscle contraction, a vigorous blink, or a facial grimace. To monitor the act of swallowing, a new instrument had to be devised, as previously described external devices for recording swallows (Kincaid 1951; Kydd and Neff 1964; Lear et al. 1965) were either too cumbersome or did not produce a signal that could readily be recorded alongside the parameters for sleep. An instrument using the Doppler principle (Sonicaid Fetal Heart Monitor) was adapted. The sensor was attached to the neck in the region of the larynx to
428
~. LICHTER AND R. C. MUIR
/% L~DM N
~m
,IW~-,IWF-'.'~I"
fin
--D'*. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
ll
.....................................................................................................
---~,
E
..........................
Fig. I. A swallow associated with a movement arousal (MA) in Stage R E M . The EEG, E O G and E M G tracings show evidence of movement arousal. A body movement (BM) is recorded with the m o v e m e n t arousal. Abbreviations: SM, swallow movement tracing: SW, swallow. TABLE I The n u m b e r a n d the rate of m o v e m e n t arousals (MA) and o f swallows (SW) per epoch in each stage o f sleep for each of 10 subject nights. Stages of sleep 1
2
Patient 1 (Epochs) No. o f M A No. of SW No. of M A and SW Rate M A Rate SW
65 0 3 18 0.277 0.323
401 1 3 8 0.022 0.027
Patient 2 (Epochs) No. of M A No. of SW No. of M A and SW Rate M A Rate SW
43 6 2 1 0.163 0.070
361 1 1 8 0.025 0.025
Patient 3 (Epochs) No. of M A
72 13
338 11
3
4
REM
61 1 1 2 0.049 0.049
121 1 1 1
257 4 8 18 0.086 0.101
105 0 1 1 0.010 0.019
73 1 0 0
205 5 1 6 0.054 0.034
92 3
109 0
84 4
429
THE PATTERN OF SWALLOWING DURING SLEEP No. of SW No. of MA and SW Rate MA Rate SW
1 8 0.292 0.125
3 13 0.071 0.047
3 3 0.065 0.065
Patient 4 (Epochs) No. of MA No. of SW No. of MA and SW Rate MA Rate SW
65 2 1 2 0.062 0.046
306 15 1 15 0.098 0.052
132 4 2 6 0.075 0.061
129 2 0 1
149 4 1 11 0.101 0.081
Patient 5 (Epochs) No. of MA No. of SW No. of MA and SW Rate MA Rate SW
51 15 0 4 0.373 0.078
407 8 0 6 0.034 0.015
139 1 0 2 0.022 0.014
83 1 0 0
201 10 0 6 0.080 0.030
Patient 6 (Epochs) No. of MA No. of SW No. of MA and SW Rate MA Rate SW
62 5 0 9 0.226 0.145
409 8 4 22 0.073 0.064
71 1 1 3 0.056 0.056
90 0 0 0
248 9 4 20 0.117 0.097
Patient 7 (Epochs) No. of MA No. of SW No. of MA and SW Rate MA Rate SW
34 7 1 4 0.324 0.147
502 14 1 18 0.064 0.038
125 3 0 3 0.048 0.024
27 0 0 0
224 9 0 4 0.058 0.018
Patient 8 (Epochs) No. of MA No. of SW No. of MA and SW Rate MA Rate SW
29 5 0 4 0.310 0.138
314 14 0 12 0.083 0.038
153 5 0 5 0.065 0.033
88 5 1 2
249 5 0 12 0.068 0.048
Patient 9 (Epochs) No. of MA No. of SW No. of MA and SW Rate MA Rate SW
45 6 0 9 0.333 0.200
258 5 1 14 0.074 0.058
187 5 0 7 0.064 0.037
156 2 0 2
246 15 1 12 0.110 0.053
Patient 10 (Epochs) No. of MA No. of SW No. of MA and SW Rate MA Rate SW
63 17 1 28 0.714 0.460
426 28 0 20 0.112 0.047
67 4 1 1 0.075 0.030
106 1 1 1
222 55 1 14 0.311 0.068
4 4 0.095 0.095
430
~. LICHTER AND R. C. MUIR MOVEMENT AROUSALS M,Aa-MA with slioht movements F i MA. with m a j o r i:;~cly m o v e m e n t s I movement time
W
/
a,
LrLIj l
7
o
lit,Ill,
, ,
J
,
,= , I
, ,I I
II ,I t l.
,i
II,
,I, g,l.,
II
, II
II
li
.It
U .
I
i~
II
II
I
movement arousals
,I I,I, IlL I 2
I 0
IJ,I 60
l 120
I
U
180 time in
240
Jill 300
It 360
tl
ID,
no
of swallows
420
minutes
Fig. 2. The relationship of swallows to movement ~.rousals and the stages of sleep is shown in one of the subjects studied. record signals produced by laryngeal movements and the sounds produced by swallowing. Its reliability was checked against intraluminal esophageal pressure recordings and these showed that a reproducible distinctive signal pattern was obtained. To check the validity of the recordings, subjects were observed throughout the night to relate the events observed (body movements, wakefulness or sleep, swallows) with the recordings made. The Doppler system for recording swallows was monitored through headphones, when a characteristic sound was produced which was related to a distinct recorded pattern on the chart. This could readily be differentiated from deflectionscaused by movements and sounds other than those produced by swallowing.
paniment of movement arousals associated with swallows. Movement arousals occurred not only between, but during sleep stages; they were not evenly distributed througout the stages of sleep~most occurring in Stages REM, 1 and 2 (Fig. 2). Of the swallows during a night's sleep 33.3 ~ occurred in Stage REM, 20.2~o in Stage 1, and 31.70 in Stage 2. The number and the rate of movement arousals and of swallows per epoch in each stage of sleep for each of 10 subject nights is shown in Table I. There is an association between movement arousals and swallows in sleep Stages 1, 2, 3 and REM. Stage 4 has been excluded from the statistical analysis because of the small number of swallows recorded (See Table II).
RESULTS
DISCUSSION
The average number of swallows per hour in the subjects studied, on each of 2 consecutive nights, ranged between 2.1 and 9.1 swallows per hour (average 5.8). For each individual the number of swallows varied little on the 2 nights. To avoid any "first-night effect" (Agnew et al. 1966) only the results of second night studies were further considered. The overnight studies showed that swallowing was associated with movement arousals (Fig. 1). The polygraphic records showed a delay between the onset of movement arousal and the act of swallowing. Movement arousals occurred in only a small proportion of the total number of epochs (8.2 ~), but swallows occurred during a significant proportion of movement arousals (range 41.7-87.3 ~ ; average 60.7~). Body movements were not a necessary accom-
The number of swallows per hour recorded in our study is similar to that reported in an investigation conducted in 1965 by Lear et al. They reported that during sleep there were always intervals when swallowing was absent for long periods (mean duration 30.3 min), the average number of such periods being seven per night. No previous study has related the pattern of swallowing to the stages of sleep or to a specific event during sleep. Our investigation demonstrated that swallowing during sleep was associated with movement arousal. A possible explanation of this association may be that stimuli that give rise to the swallowing reflex may themselves affect and modulate the nightly progression of sleep stages. Swallows might then be related to sleep stages, and the first indication of a swallow
431
THE PATTERN OF SWALLOWING DURING SLEEP TABLE II
Comparison of the observed association between movement arousals (MA) and swallows (SW) and the expected association between M A and SW as derived from a Poisson distribution. Patients
Types of sleep 1
1 2 3 4 5 6 7 8 9 10
2
3
REM
Obs.
Exp.
P*
Obs.
Exp.
P*
Obs.
Exp.
P*
Obs.
Exp.
P*
18 1 8 2 4 9 4 4 9 28
5.8 0.5 2.6 0.2 1.5 2.0 1.6 1.2 3.0 20.7
0.0001 0.4*** 0.01 0.02 0.06*** 0.001 0.1"** 0.04 0.01 0.03
8 8 13 15 6 22 18 12 14 20
0.2 0.2 1.1 1.6 0.2 1.9 1.2 1.0 1.1 2.2
0.000001 0.000001 0.000001 0.000001 0.000001 0.000001 0.000001 0.000001 0.000001 0.000001
2 1 3 6 2 3 3 5 7 1
0.1 0.0 0.4 0.6 0.0 0.2 0.1 0.3 0.4 0.1
0.01 ? 0.01 0.00001 0.01"* 0.01 0.001 0.001 0.000001 0.1"**
18 6 4 11 6 20 4 12 12 14
2.2 0.4 0.8 1.2 0.5 2.8 0.2 0.8 1.4 4.7
0.000001 0.00001 0.01 0.000001 0.0001 0.00001 0.0001 0.000001 0.000001 0.001
* P < Probability that the number in the "observed" column (Obs.) or a larger number could be obtained from a Poisson distribution with a mean as given in the "expected" column (Exp.). ** The expected value has been corrected to 1 decimal place and it is still possible in this case togive an upper limit to P. *** These results are not significant at the 5 % (P< 0.05) level. t The expected value is too small for a reliable estimat~ of the upper limit of P to be obtained except that P < 0.1. response may be a movement arousal. On the other hand there may be a direct relationship between sleep stages and movement arousals, with swallows associated with movement arousals ; the relationship between swallows and sleep stages would then qe indirect. Movement arousals occurred largely during sleep stages, being most frequent on Stages REM, 1 and 2. Such a direct relationship would suggest that there may be more significance to movement arousal than the mere signalling of a change o f sleep stage. The frequency o f swallowing, and in particular the long periods when no swallowing takes place, directly bears on the problem o f the degree o f damage caused to the esophagus by gastroesophageal reflux. Reflux persists in the esophagus until cleared by swallowing, and the major damage occurring in this condition probably takes place in sleep during the "no-swallow" periods. Factors which enhance delta sleep, such as sleep deprivation would tend to prolong the intervals between swallows; drugs that affect the depth of sleep may have a similar effect. It can also be postulated that hypnotics and other drugs that reduce the RE M component of sleep may significantly reduce the number of movement arousals (frequent in Stage REM) and the number of swallows during sleep. There is, however. no information in the literature on the direct effect o f drugs on movement arousal. This situation probably arises from the fact that movement arousals have not heretofore been associated with any physiological events.
by means of EEG, EOG and EMG, and swallowing was monitored by means o f an external sensing device attached to the neck. It was found that during sleep, swallowing is episodic, with long swallow-free periods. Swallows occur almost exclusively in association with movement arousals which are most frequent during Stages REM, 1 and 2 of sleep. RESUME LE CYCLE D ' A V A L E M E N T P E N D A N T LE S O M M E I L La structure d'avalement dans le sommeil a 6t6 recherch6 par une 6tude de 10 sujets normaux. Le cycle du sommeil fut classifi6 par moyen de I'EEG, I'EOG et I'EMG, et l'avalement rut contr616 par moyen d'un appareil sensim~tre attach6 au COU.
On a trouv6 que dans le sommeil, l'avalement est episodique avec des longues periodes sans avalement. Les avalements se produisent presque exclusivement avec des mouvements de r6veil, lesquels sont plus fr6quents pendant les phases REM, 1 et 2 du sommeil. We wish to acknowledge the help and advice of Dr. David Marks of the Department of Psychology, University of Otago, and the technical assistance of Mr. Leslie Wong of the Otago Hospital Board. We are grateful to Dr. D. C. E. Manley of the Department of Preventive and Social Medicine for the statistical analysis.
SUMMARY REFERENCES The pattern of swallowing during sleep was investigated by means of a study in 10 normal subjects. Sleep was staged
AGNEW,H. W., WEBB, W. B. and WILLIAMS, R. L. The first
432 night effect: an EEG study of sleep. Psychophysiology, 1966, 2: 263-266. BOOTH, D. J., KEMMERER, W. T. and SKINNER, D. B. Acid clearing from the distal esophagus. Arch. Sur9., 1968, 96 : 731-734. KINCAID, R. N. Frequency of deglutition in man: its relation to overbite. Angle Orthodont., 1951, 21: 34-43. KYDD, W. L. and NE~, C. W. Frequency of deglutition of tongue thrusters compared to a sample population of normal swallowers. J. dent. Res., 1964, 43: 363-369. LEAR, C. S. C., FLANAGAt~,J. B. J. and MOORREZS,C. F. A. The frequency of deglutition in man. Arch. oral Biol., 1965, 10: 83-100.
i. LICHTER AND R. C. MUIR LICHTER, I. Measurement of gastro-oesophageal acid reflux : significance in hiatus hernia. Brit. J. Surg., 1974, 61: 253-258. OLSEN, A. M. and SCHLEGEL, J. F. Motility disturbances caused by oesophagitis. J. thorac, cardiovasc. Surg., 1965, 50: 607-712. RECHTSCHAFFEN, A. and KALES, A. A manual of standardiz, ed terminology, techniques and scoring system Jor sleep stages of human subjects. U.S. Department of Health, Education and Welfare, Publication No. 204, Bethesda, Md., 1968. SIEGEL, C. I. and HENDRIX, T. R. Esophageal motor abnormalities induced by acid perfusion in patients with heartburn, J. clin. Invest., 1963, 42: 686-695.