Colonic Motor Activity in Women During Sleep

Colonic Motor Activity in Women During Sleep
Timothy P. Roarty,1 Paul M. Suratt,2 Peter Hellmann,3 and R.W. McCallum3
(1) Division of Gastroenterology and Hepatology, Department of Medicine, (2) Division of Pulmonary Critical
Care Medicine and the Sleep Disorders Center, Department of Medicine (3) General Clinical Research Center,
University of Virginia Health Sciences Center, Charlottesville, Virginia
Summary: The relationship between colonic motility, sleep, and arousals from sleep has never been studied in women
and only once in men. The purpose of this study was to determine how sleep and arousals from sleep affected colonic
motility in women during the follicular phase of their menstrual cycle. We monitored sleep and segmental colonic motility in six healthy women during the follicular phase of the menstrual cycle. We observed no colonic motility during sleep;
during awake periods or during arousals, we observed isolated low-amplitude bursts of colonic motility. This colonic motility occurred during 25% of the arousal and awakening time. In contrast, morning awakening was associated with highamplitude independent and related colonic motility in all colonic segments. We conclude that in women in the follicular
phase of their menstrual cycle, colonic motility is inhibited during sleep; colonic motility at night only occurs during arousals
or awakenings from sleep
Key words: Sleep; colon; women
ments per day and ò3 bowel movements per week. None
were taking medications, and all denied recent or habitual
use of laxatives. Written informed consent was obtained
and the protocol was approved by the Human
Investigations Committee at the University of Virginia
Health Sciences Center.
THE COLON IS REPORTED TO BE QUIESCENT at
night in adult males.1-5 Only one study, however, monitored sleep and colonic motility simultaneously.6 Colonic
motility has not been studied in women during sleep, even
though women dominate the irritable bowel syndrome and
idiopathic constipation populations. The purpose of our
study was to determine the association between colonic
motor activity and sleep in women.
Experimental Protocol
Subjects were admitted to the clinical research center at
the University of Virginia. On day 1, serum B-HCG was
obtained and subjects ingested four liters of an electrolyte
polyethylene glycol solution (Colyte). On the first night,
electrodes were placed on subjects’ heads to simulate a
sleep study but no recording were made.
Measurement of colonic motility.—On the morning
of day 2, colonoscopy was performed under midazolam
sedation and an 8 French solid-state colonic motility
catheter (Millar Instruments Model #SSD-471) with five
pressure transducers distributed over 105 cm was placed in
the colon. Placement of the distal end of the motility
catheter at the mid-transverse colon or beyond was confirmed with a flatplate KUB radiograph. Pressures could
MATERIALS AND METHODS
Subjects
We studied six healthy female volunteers (mean age
32, range 20-44) in the follicular phase of their menstrual
cycle who had no history of sleep disorder, gastrointestinal
complaints, or abdominal surgery, and who described a
“normal” bowel movement pattern of ó2 bowel moveAccepted for publication January, 1998
Address correspondence and requests for reprints to Paul M. Suratt, MD,
Sleep Disorders Center, Box #546, University of Virginia Health Sciences
Center, Charlottesville, VA 22908.
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Colonic motility during sleep—Roarty et al
Table 1.—Sleep architecture in individual subjects
Total sleep
Percent of total sleep time in each sleep stage
SUBJECT
NO.
Sleep
period,
min
Sleep
time,
min
Sleep
efficiency,
%
1
2
3
4
REM
1+2
3+4
A
400
370
90
8.2
52.1
16.1
9.9
13.8
60.3
25.9
B
458
368
77
10.9
63.5
12.5
10.2
2.9
74.4
22.7
C
380
335
69
4.8
73.1
11.9
7.5
2.7
77.9
19.4
D
467
380
80
4.6
88.2
1.4
0.4
5.4
92.8
1.8
E
469
299
59
2.0
69.7
22.4
3.8
2.0
71.7
26.3
F
440
411
86
9.5
51.1
8.1
28.3
3.0
60.6
36.4
mean
435
361
77
7
66
12
10
5
73
22
Table 2.—Episodes of colonic activity during epochs scored as awake, NREM and REM
AWAKE
NREM
REM
NREM+REM
Subject no
total
no/hr
total
no/hr
total
no/hr
total
no/hr
A
20
41
0
0
0
0
0
0
B
32
22
38
6.4
1
5.7
39
6.4
C
11
5
3
0.6
1
6.7
4
0.7
D
38
25
13
2.2
0
0
13
2
E
16
4.7
0
0
0
0
0
0
F
12
13
1
0.2
0
0
1
0.1
mean
22
18
9.2
1.6
0.3
2.1
9.5
1.5
be measured in the sigmoid, descending, transverse, and in
most cases the right colon.
Subjects ate 2000 kcal/day divided in three equicaloric
portions consisting of 50% carbohydrate, 30% fat, 20%
protein, and 15 grams of fiber, and consumed within a 30minute time period. Subjects remained in bed during the
protocol and colonic motility was recorded throughout the
night. Prior to removal of the catheter, a KUB flatplate was
taken to confirm that it had not migrated.
Colon pressures were recorded on paper, on 1/8" magnetic tape, and on a Nicolet UltraSom computer (Nicolet
Biomedical Inc., Madison, Wis). Events greater than 5 mm
Hg of deflection in one or in two or more successive leads
during sleep not associated with movement were counted
as single colonic motility events. The paper record was
SLEEP, Vol. 21, No. 3, 1998
visually reviewed to eliminate movement and other artifacts.
Polysomnography.—Monitoring was performed
using conventional techniques7 with electroencephalograms (C3/A2 and O2/A1), bilateral electooculograms,
submental electromyograms, and an electrocardiogram,
and recorded on the Nicolet UltraSom computer. Sleep was
staged manually in 30-second epochs using standard criteria.7 Arousals were defined as an abrupt shift in EEG frequency lasting 3 or more seconds.8
RESULTS
Sleep architecture for each subject is displayed in
Table 1. Subjects had an average of 6.55 ±SD 3.81 arousals
286
Colonic motility during sleep—Roarty et al
per hour of sleep and 3.04 ±0.98 awakenings per hour of
sleep.
Colonic activity during the sleep study was essentially
quiet in contrast to that during the daytime (Figs. 1 and 2).
All colonic activity during the study occurred when subjects were awake or during an arousal (Table 2). Some
episodes occurred during epochs scored as sleep, but these
activity episodes occurred after or during an arousal.
Conversely, only 16% ±21.5 SD of arousals were associated with colonic motility. The majority of colonic activity
events occurred during epochs scored as awake (mean =
18/hr ± 13.9), and very few occurred during epochs scored
as sleep (mean = 1.5/hr ± 2.5), p<0.01). Only two episodes
of colonic activity occurred during epochs scored as REM,
although subjects spent only 5% ±4.48 SD of their total
sleep time in REM. The majority of the colonic motility
episodes occurring during epochs scored as sleep occurred
during NREM sleep.
We observed only low-amplitude contractions (less
than 40 mm Hg), which usually occurred in isolated or two
adjacent pressure sensors (Figure 1). No high-amplitude
contractions (100-200 mm Hg) occurred when the subject
was asleep or awake. With morning awakening, while subjects were in bed with minimal movement, high-amplitude
independent and related colonic motility occurred in all
colonic segments. This activity was further augmented with
the consumption of breakfast, and persisted for an hour or
more postprandially.
Figure 1a
DISCUSSION
Figure 1b
This study has shown that women during the follicular
phase of their menses have no colonic motility during nocturnal sleep. Isolated burst of colonic motility occurred
only during arousals or awakening from sleep. Colonic
motility occurred in only 16% of arousals.
Furukawa and colleagues reported that in healthy
young males, sleep had a profound inhibitory effect on
propagating and nonpropagating colonic activity.6 During
stage 1 sleep, they found 2.4 propagating contractions/
hour; during stage 2, 1.2/hour; during stages 3 and 4,
0/hour; and during REM, 1.4/hour. While 54% of these
propagating contractions occurred during arousals or awakenings, 46% of them occurred spontaneously during stable
sleep.
Our study, in contrast, found that colonic activity
occurred only during epochs of wakefulness or during
arousals, and that no colonic activity occurred during sleep.
Furakawa’s study may not have detected all arousals
because they used only one central EEG lead to monitor
sleep, C3/A2. Arousals are frequently only observed in
EEG leads placed over the occipital region. They also used
a fluid-filled catheter which continuously infused water
into the colon and may have altered colonic activity. On
Figure 1c
Figure 1.—Typical colonic motility patterns observed during the sleep study. a.
low amplitude contractions occurring with arousal at night. This activity occurs
in an apparent temporal fashion from left to right colon. b. low amplitude contractions with arousal occurring mainly in the proximal colon with evidence that
some but not all are propagated. c. Tracing typical of predominant nighttime quiescence associated with NREM sleep.
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287
Colonic motility during sleep—Roarty et al
Figure 2a
Figure 3.—Sustained sigmoidal activity seen in sleep study in subject
C during awake state.
ACKNOWLEDGMENTS
The authors would like to thank the nurses and staff of
the Endoscopy Unit, the Sleep Disorders Center, and the
General Clinical Research Center at the University of
Virginia Health Sciences Center for their assistance. Data
management and analysis made possible in part by the use
of CLINFO hardware and software and the assistance of
David Boyd, UVA GCRC NIH Grant M01RR00847.
Figure 2b
Figure 2—Daytime colonic motility tracings in same subjects who participated in the sleep study. a. postprandial stimulated colonic activity, b.
high amplitude propagating contractions observed postprandially in subject the evening of the sleep study.
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the other hand, their use of a water-filled catheter permitted
them a greater number of sampling positions.
Our study was performed in women during the follicular phase of their menstrual cycle, since their sleep may differ depending on the stage of their cycle.9 Women were
chosen because they tend to dominate the irritable bowel
syndrome and idiopathic constipation populations, of
which we plan to pursue studies in the future. Results from
this study suggest that subjects with frequent arousals and
awakenings from sleep may have more frequent episodes
of colonic activity. This may have implications for nocturnal continence in patients with irritable bowel syndrome.
Our data may be skewed by the relatively small amount
of time spent in REM sleep. Our subjects spent an average
of only 5% of sleep in REM, and only two episodes of
colonic motility were seen during this time. Based on the
limited amount of data we obtained for REM sleep, we hesitate to draw any strong conclusions concerning colonic
motility and REM.
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Colonic motility during sleep—Roarty et al