Normalization of atropine-induced postprandial dysrhythmias
with gastric pacing
Liwei
Qian,
Xuemei
Lin, and
J. D. Z.
Chen
Lynn Institute For Healthcare Research, Oklahoma City, Oklahoma
73112
 |
ABSTRACT |
Gastric pacing has received increasing attention
recently. However, few studies have systematically assessed the effect
of pacing on gastric dysrhythmias. The aims of this study were to investigate the effect of gastric pacing on gastric dysrhythmia and to
explore whether the effect of gastric pacing was mediated via
cholinergic nerves. Eight hound dogs implanted with three pairs of
serosal electrodes were studied. Three study sessions were performed on
each dog. The experiment was conducted sequentially as follows: a
30-min myoelectrical recording immediately after a meal, intravenous
injection of atropine or saline, and three sequential 20-min
myoelectrical recordings with or without gastric pacing during the
second 20-min recording. The percentage of regular slow waves
(3.5-7.0 cycles/min) was calculated using spectral analysis. The
percentage of the regular slow waves was progressively reduced from
96.7 ± 1.7% at baseline to 29.6 ± 9.0 (P < 0.001), 23.1 ± 7.1 (P < 0.001), and 27.3 ± 4.3% (P < 0.001),
respectively, during the first, second, and third 20 min after atropine
injection. Normalization of the gastric slow wave was achieved with
gastric pacing 2.3 ± 1.0 min after the initiation of pacing. The
percentage of regular slow waves was significantly increased both
during pacing (93.6 ± 2.4 vs. 23.1 ± 7.1%,
P < 0.002) and after pacing (70.9 ± 6.8 vs. 27.3 ± 4.3%,
P < 0.003) in comparison with the session without pacing. We conclude that
1) atropine induces gastric myoelectric dysrhythmia in the fed state,
2) gastric pacing is able to
normalize gastric postprandial dysrhythmia induced by atropine, and
3) the effect of gastric pacing is
not mediated by vagal cholinergic mechanism.
gastric myoelectric activity; gastric motility; electrogastrography; cholinergic mechanism; electrical
stimulation
 |
INTRODUCTION |
GASTRIC DYSRHYTHMIA has been found in a number of
clinical settings (6, 10), including unexplained nausea and vomiting (15), gastroparesis (1, 5), early pregnancy (29, 37), vagotomy (16,
36), and postsurgery (9). In these circumstances the frequency of the
gastric slow wave becomes either abnormally high (tachygastria),
abnormally low (bradygastria), or arrhythmic. Sometimes, an ectopic
pacemaker may exist in the antrum. Gastric dysrhythmias are associated
with gastric motor disorders and gastrointestinal symptoms.
Abnormalities in the frequency of the gastric slow wave may lead to
gastric hypomotility and/or uncoordinated or unpropagated antral contractions, yielding delayed emptying of the stomach. Therefore, it is conceivable that the normalization of gastric dysrhythmia may lead to an improvement in gastric motility, gastric emptying, and/or gastrointestinal symptoms.
Recently, gastric pacing has received increasing attention among
researchers and clinicians. A number of studies have been performed to
investigate the acute effect of gastric pacing on gastric motility,
gastric emptying, and gastrointestinal symptoms in both dogs (3, 11,
14, 18, 23, 26) and humans (13, 17, 21, 22, 24, 32, 34). Although some
of the results are still controversial, the majority of these studies
seem to indicate that gastric pacing is able to entrain gastric slow
waves, accelerate gastric emptying in patients with gastroparesis or the animal model of gastroparesis, and improve gastrointestinal symptoms. However, few studies have systematically assessed the effect
of gastric pacing on gastric dysrhythmias (21, 35). None has ever
investigated the mechanism of gastric pacing and whether the effect of
gastric pacing would last when pacing is terminated. The aims of this
study were to establish a postprandial model of gastric dysrhythmia in
dogs, to investigate the effect of gastric pacing on gastric
dysrhythmia, and to study whether the effect of gastric pacing is
mediated via the cholinergic mechanism.
 |
MATERIALS AND METHODS |
Subjects.
Eight healthy female hound dogs (14.5-22.6 kg) were implanted with
pacing electrodes by laparotomy. Three pairs of 28-gauge cardiac pacing
wires (A&E Medical, Farmingdale, NJ) were implanted on the serosal
surface of the stomach along the greater curvature. The most distal
pair was 2 cm above the pylorus, and the distance between adjacent
pairs of electrodes was 4 cm. The electrodes in each pair were 1 cm
apart. The electrodes were affixed to the gastric serosa by
unabsorbable suture in the seromuscular layer of the stomach. The wires
were brought out through the anterior abdominal wall, channeled
subcutaneously along the right side of the trunk, and placed outside
the skin for the attachment of pacing or recording. The most proximal
pair of electrodes was used for forward pacing, whereas the remaining
two were used for recording gastric myoelectric activity.
The study was initiated about 10 days after the surgery. The protocol
was approved by the animal committee of the Veterans Affairs Hospital
(Oklahoma City, OK).
Study protocol.
Each dog was studied in three sessions on three different days in a
randomized order. In session 1 gastric
myoelectric activity was recorded for 90 min after a test meal (225 g
dry food, 838 kcal). Atropine (0.25 mg/kg; Elkin-Sinn, Cherry Hill, NJ)
was given intravenously at the 31st min. Session
2 was the same as session
1 except for the replacement of atropine with saline. Session 3 followed the same protocol
of session 1, except that forward
gastric pacing was applied during the 2nd 20 min after the injection of
atropine. The pacing signal was given at the most proximal pair of
electrodes (10 cm from the pylorus) and was composed of periodic
rectangular electrical pulses with a width of 550 ms, amplitude of 6 mA, and frequency of 6.67 cycles/min (cpm). These pacing parameters
were previously shown to be able to entrain gastric slow waves in dogs
(31).
Recording and analysis of gastric myoelectrical activity.
Gastric myoelectrical activity was recorded from the two distal pairs
of electrodes during the whole study using a multichannel recorder
(AcknowledgeIII; Biopac Systems, Santa Barbara, CA). All signals were
displayed on a computer monitor and saved on the hard disk by an
IBM-compatible 486 PC. The low and high cutoff frequencies of the
amplifier were 0.5 and 35 Hz, respectively. To lower the computational
load, the signals were low-pass filtered again by software with a
cutoff frequency of 10 Hz and sampled at 20 Hz. For the spectral
analysis of the gastric slow wave, the signal was further filtered and
sampled at 1 Hz. Adaptive spectral analysis was applied to compute the
running spectra of the recording on a minute-by-minute basis (7). The
percentage of regular gastric slow waves was used to assess the effects
of atropine and pacing. It was defined as the percentage of time during
which a dominant peak was observed in the range of 3.5-7.0 cpm in
the running spectra. The definition of regular slow waves as
3.5-7.0 cpm was based on the analysis of baseline data in all 8 dogs. The dominant peak in the range of 0.5-3.5 cpm was defined as
bradygastria. The dominant peak in the range of 7.0-12.0 cpm was
defined as tachygastria. The corresponding recording period was called
arrhythmia if there was no dominant peak in the range of 0.5-12.0
cpm (Fig. 1).

View larger version (55K):
[in this window]
[in a new window]
|
Fig. 1.
Running spectrum analysis was applied to compute regularity of gastric
slow waves. Percentage of regular slow waves was calculated as
percentage of time during which dominant peak was observed in range of
3.5-7.0 cycles/min (cpm). Spectrum with dominant peak in
0.5-3.5 cpm range was considered bradygastria. Spectrum with
dominant peak in range of 7.0-12.0 cpm was considered
tachygastria. If there was no obvious dominant peak in range of
0.5-12.0 cpm, spectrum was considered arrhythmia.
|
|
Statistical analysis.
To investigate the effects of atropine and pacing, the 60-min
postinjection data were divided into three 20-min periods. ANOVA was
applied to assess the difference among the data obtained during the
three 20-min periods after atropine or saline. To investigate the
effect of pacing on atropine-induced dysrhythmia, the data obtained in
session 1 (no pacing) and
session 3 (with pacing) were compared
using paired Student's t-test. All
values are expressed as means ± SE.
P < 0.05 was considered significant.
 |
RESULTS |
Effects of atropine.
Regular gastric slow waves of 3.5-7.0 cpm were observed in all
dogs in the fed state before the injection of atropine or saline (Fig.2A),
and the mean dominant frequency was 4.34 ± 0.16 cpm. Atropine
consistently induced gastric dysrhythmia (bradygastria or
tachygastria), which lasted at least 60 min (Fig. 2,
B and C). The percentage of 3.5-7.0
cpm slow waves was progressively reduced from 96.7 ± 1.7% before
atropine to 29.6 ± 9.0% (P < 0.001), 23.1 ± 7.1% (P < 0.001), and 27.3 ± 4.3% (P < 0.001) during the 1st, 2nd, and 3rd 20 min after atropine injection
(Fig. 3). Saline had no effects on the
gastric slow wave; the percentage of the 3.5-7.0 cpm slow wave was
94.0 ± 3.0, 99.4 ± 0.6, 95.6 ± 2.6, and 96.1 ± 2.3% during the corresponding recording periods (Fig. 3). Two
dogs showed dominant tachygastria with a frequency of 9.53 ± 0.35 cpm. The other six dogs presented bradygastria with a
frequency of 3.26 ± 0.08 cpm.

View larger version (25K):
[in this window]
[in a new window]
|
Fig. 2.
Recording of gastric myoelectrical activity in 3 different occasions.
A: typical normal gastric slow waves
in fed state before atropine. B:
typical recording obtained in 1 of 6 dogs with persistent bradygastria
after atropine. C: typical recording
measured in 1 of 2 dogs with dominant tachygastria after atropine.
|
|

View larger version (18K):
[in this window]
[in a new window]
|
Fig. 3.
Percentage of regular gastric slow waves (3.5-7.0 cpm) in fed
state before and after injection of atropine or saline. Percentage of
regular slow waves during 3 20-min periods after atropine was
significantly lower than before atropine (baseline) and corresponding
periods after saline.
|
|
Effects of pacing.
The normalization occurred a few minutes after gastric pacing was
initiated. The time required for normalization of the atropine-induced bradygastria in the six dogs was 1.12 ± 0.36 min and for
normalization of tachygastria in the two dogs, 5.97 ± 1.15 min. The average time for the normalization was 2.3 ± 1.0 min.
After this transient period the gastric slow wave was actually
completely entrained with the pacing stimulus.
Gastric pacing was found to be able to normalize atropine-induced
dysrhythmias, and the effect seemed to last at least for 20 min after
the termination of pacing. Both bradygastria and tachygastria were
entrained at the pacing frequency during pacing and remained at the
normal frequency range of 3.5-7.0 cpm after pacing (Figs.
4 and 5). The
percentage of 3.5-7.0 cpm slow waves was increased to 93.6 ± 2.4% during pacing (P < 0.02 in
comparison with that before pacing) and 70.9 ± 6.8% during the 20 min after pacing (P < 0.05 in
comparison with that before pacing; Fig.
6). It can also be seen from Fig. 6 that
the percentages of 3.5-7.0 cpm slow waves during and after pacing
were significantly higher than the corresponding periods in the session
of atropine without pacing (P < 0.003). All values presented were calculated from the recordings
obtained from the most distal pair of electrodes. However, these were
not different from the data obtained from the middle pair (Table
1).

View larger version (25K):
[in this window]
[in a new window]
|
Fig. 4.
Effects of gastric pacing on atropine-induced bradygastria in 1 of 6 dogs. A: bradygastria induced by
atropine before pacing. B: entrainment
of gastric slow wave with gastric pacing at a frequency of 6.67 cpm
during pacing. C: normalized gastric
slow waves with frequency of about 4.0 cpm after pacing.
|
|

View larger version (28K):
[in this window]
[in a new window]
|
Fig. 5.
Effect of gastric pacing on tachygastria in 1 of 2 dogs.
A: tachygastria induced by atropine
before pacing. B: entrained gastric
slow waves with gastric pacing at a frequency of 6.67 cpm during
pacing. C: normalized gastric slow
waves with a frequency of about 5 cpm after pacing.
|
|

View larger version (20K):
[in this window]
[in a new window]
|
Fig. 6.
Percentage of regular gastric slow waves (3.5-7.0 cpm) in 2 sessions with atropine and with or without gastric pacing during 2nd 20 min after atropine. Percentage of regular slow waves during and after
pacing was significantly higher than that before pacing and that of
corresponding periods in session with atropine and without gastric
pacing.
|
|
 |
DISCUSSION |
This study demonstrated that atropine was able to induce gastric
dysrhythmia and gastric pacing was capable of normalizing atropine-induced dysrhythmia. There was a transient time of a few
minutes before normalization took place when pacing was initiated. The
effect of pacing lasted for at least 20 min more when pacing was
terminated. The normalization in the six dogs with dominant bradygastria occurred earlier than that in the two dogs with dominant tachygastria.
Gastric dysrhythmia is defined as abnormal myoelectrical rhythm of the
stomach. It is further classified as tachygastria, bradygastria, and
arrhythmia (6). It is not only found in a number of clinical
circumstances but is also induced by chemical agents such as
epinephrine (27), glucagon (2), metenkephalin, or
PGE2 (28, 30), atropine, morphine,
and large doses of histamine (38), insulin, secretion,
CCK-pancreozymin, and pentagastrin (8). It is also known that
chemically dissimilar drugs can cause similar myoelectrical
disturbances and that spontaneous and drug-induced dysrhythmias exhibit
the same origin and propagational characteristic (27). Daniel (8)
reported that the appearance of antral dysrhythmia corresponded with
the dominance of sympathetic over parasympathetic activity. Stoddard et
al. (38) observed arrhythmia after insulin and glucagon and also
attributed this to a relative increase of sympathetic over
parasympathetic activity. In this study we assessed the effects of
atropine quantitatively using the advanced spectral analysis method and
found persistent tachygastria in 25% and bradygastria in 75% of the
dogs after atropine. However, it is unknown why the same dosage led to
two different effects. We hypothesize that the normal pacemaker of the
stomach is controlled by vagal cholinergic activity and that once the
control is blocked by atropine an ectopic pacemaker that is either
bradygastria or tachygastria would develop.
Atropine, a competitive antagonist of ACh and other muscarinic
agonists, can effectively inhibit the effects of vagal impulses, thus
decrease gastric tone and motility. A higher dose was used in this
study because the aim of the experiment was to induce as much
dysrhythmia as possible to assess the effect of gastric pacing in
normalization of dysrhythmia. It is known that full therapeutic doses
(0.5-1.0 mg) of atropine produce definite and prolonged inhibitory
effects on the motor activity of the stomach. These inhibitory effects
are incomplete and do not block responses to gastrointestinal hormone
or to noncholinergic neurohumoral transmitters (4). However, a high
dose of atropine can almost completely inhibit the parasympathetic
control of the gastrointestinal tract and cause a higher-degree
blockade of muscarinic cholinergic receptors (4). Gustavsson
and Lindberg (20) found that the frequency of gastric myoelectric
activity in the fed state was decreased dose-dependently by bolus
injection of atropine in humans. Regulatory effects of the vagus have
previously been reported. Gastric dysrhythmia has frequently been
observed in patients after vagotomy (16, 25). The atropine-induced
dysrhythmias observed in the current study might be attributed to the
inhibition of the vagal activity by atropine.
Efficacy of gastric pacing is largely dependent on pacing parameters
(32). The parameters that are most effective in entraining gastric slow
waves are considered as the optimal parameters. Frequency, amplitude,
and width of the pacing stimulus are the three important parameters
that contribute to the success or failure of entrainment. It has been
reported that the complete entrainment of gastric slow waves was
possible only when the pacing frequency was slightly higher than the
intrinsic gastric frequency (32, 34). One of the early studies,
however, reported the entrainment of gastric slow waves with a
frequency lower than the intrinsic gastric frequency (26).
Furthermore, recent reports showed that pacing at frequencies much
higher than the intrinsic slow-wave frequency (20-1,200
cycles/min) induced antral contractions (13, 14, 19). In a recent study it was found that energy of pacing stimuli, which was determined by the
pulse width and the pulse amplitude, was equally important in achieving
complete entrainment in patients with gastroparesis (33). The
parameters used in this study were found to be the most effective for
the entrainment of gastric slow waves in the canine model (31). Using
these parameters, complete entrainment was achieved after a transient
period of a few minutes both in the dogs with dominant bradygastria and
in the dogs with dominant tachygastria. It seemed easier (or faster) to
normalize bradygastria (bring the frequency up by pacing) than to
normalize tachygastria (bring the frequency down).
Recently, a number of studies have indicated that gastric pacing with
appropriate parameters is able to entrain gastric slow waves and
improve gastric motility and emptying both in dogs and in humans.
Bellahsene et al. (3) demonstrated that gastric pacing could accelerate
gastric emptying in the canine model of gastroparesis. McCallum et al.
(33) reported an improvement of gastric emptying and symptoms in
patients with gastroparesis. Using high-frequency stimulation, Familoni
et al. (13) observed an increase in gastric motility in dog. However,
few studies have systematically investigated the effect of gastric
pacing on gastric dysrhythmias (21, 35), and none has studied this
effect quantitatively. In this study we quantitatively investigated the
effect of gastric pacing on the canine model of atropine-induced
postprandial gastric dysrhythmias and found that gastric pacing could
markedly normalize the abnormality of gastric myoelectric activity. In
addition, we noted that the effect could last at least 20 min after
pacing was terminated.
Although gastric pacing could abolish abnormal gastric electrical
rhythms and restore a healthy pattern of slow waves, its mechanism is
still unclear. Although atropine was used to block the vagal activity
in this study, pacing could still entrain and normalize the irregular
rhythm of the gastric slow wave. This suggests that the mechanism of
gastric pacing is not via the cholinergic nerves and may be via some
other neurohumoral pathways.
 |
ACKNOWLEDGEMENTS |
We thank Loretta Dunnaway for assistance in the preparation of the manuscript.
 |
FOOTNOTES |
This study was supported by a biomedical research grant from the
Whitaker Foundation.
The costs of publication of this
article were defrayed in part by the
payment of page charges. The article
must therefore be hereby marked
"advertisement"
in accordance with 18 U.S.C. §1734 solely to indicate this fact.
Address for reprint requests: J. D. Z. Chen, Lynn Institute for
Healthcare Research, 5300 N. Independence Ave., Suite 130, Oklahoma
City, OK 73112.
Received 11 March 1998; accepted in final form 23 October 1998.
 |
REFERENCES |
1.
Abell, T. L.,
M. Camiller,
V. S. Hench,
and
J. R. Malagelada.
Gastric electromechanical function and gastric emptying in diabetic gastroparesis.
Eur. J. Gastroenterol. Hepatol.
3:
163-167,
1991.
2.
Abell, T. L.,
and
J.-R. Malagelada.
Glucagon evoked gastric dysrhythmia in human shown by an improved electrogastrographic technique.
Gastroenterology
88:
1932-1940,
1985[Medline].
3.
Bellahsene, B. E.,
C. D. Lind,
B. D. Schirmer,
O. L. Updike,
and
R. W. McCallum.
Acceleration of gastric emptying with electrical stimulation in a canine model of gastroparesis.
Am. J. Physiol.
262 (Gastrointest. Liver Physiol. 25):
G826-G834,
1992[Abstract/Free Full Text].
4.
Brown, J. H.,
and
P. Taylor.
Muscarinic receptor agonist and antagonists.
In: The Pharmacological Basis of Therapeutics (9th Ed.), edited by J. G. Hardman,
and L. E. Limbird. New York: McGraw-Hill, 1996, p. 148-153.
5.
Chen, J. D. Z.,
and
R. W. McCallum.
Gastric slow wave abnormality in gastroparesis patients.
Am. J. Gastroenterol.
87:
477-482,
1992[Medline].
6.
Chen, J. D. Z.,
J. Pan,
and
R. W. McCallum.
Clinical significance of gastric myoelectric dysrhythmias.
Dig. Dis. Sci.
13:
275-290,
1995.
7.
Chen, J. D. Z.,
W. R. Stewart,
and
R. W. McCallum.
Adaptive spectral analysis of episodic rhythmic variation in the cutaneous electrogastrogram.
IEEE Trans. Biomed. Eng.
40:
128-135,
1993[Medline].
8.
Daniel, E. E.
The electrical and contractile activity of the pylorus region in dogs and the effects of drugs.
Gastroenterology
37:
268-281,
1965.
9.
Dauchel, J. J.,
C. Schang,
J. Kachelhoffer,
R. R. Eloy,
and
J. F. Grenrer.
Gastrointestinal myoelectrical activity during the postoperative period in man.
Digestion
14:
294-303,
1976.
10.
Dubois, A.
Gastric dysrhythmias: pathophysiological and etiologic factors.
Mayo Clin. Proc.
64:
246-250,
1989[Medline].
11.
Eagon, J. C.,
and
K. A. Kelly.
Effects of gastric pacing on canine gastric motility and emptying.
Am. J. Physiol.
265 (Gastrointest. Liver Physiol. 28):
G767-G774,
1993[Abstract/Free Full Text].
12.
Eagon, J. C.,
and
N. J. Soper.
Gastrointestinal pacing.
Surg. Clin. North Am.
73:
1161-1172,
1993[Medline].
13.
Familoni, B. O.,
T. L. Abell,
G. Voeller,
A. Salem,
and
O. Gaber.
Electrical stimulation at a frequency higher than basal rate in human stomach.
Dig. Dis. Sci.
42:
885-891,
1997[Medline].
14.
Familoni, B. O.,
T. L. Abell,
G. Voeller,
A. Salem,
and
B. Johnson.
Efficacy of electrical stimulation at frequencies higher than basal rate in canine stomach.
Dig. Dis. Sci.
42:
892-897,
1997[Medline].
15.
Geldof, H.,
E. J. van der Schee,
M. van Blankenstein,
and
J. L. Grahuis.
Electrogastrographic study of gastric myoelectrical activity in patients with unexplained nausea and vomiting.
Gut
26:
799-808,
1986[Abstract].
16.
Geldof, H.,
E. J. van der Schee,
M. van Blankenstein,
A. J. P. M. Smout,
and
L. M. A. Akkermans.
Effects of highly selective vagotomy on gastric myoelectrical activity.
Dig. Dis. Sci.
35:
960-975,
1990.
17.
GEMS Study Group.
Electrical stimulation for the treatment of gastroparesis: preliminary report of a multicenter international trial (Abstract).
Gastroenterology
110:
A668,
1996.
18.
Grundfest-Broniatowski, S.,
C. R. Davies,
E. Olsen,
G. Jacobs,
J. Kasick,
S. M. Chou,
Y. Nose,
and
R. E. Herman.
Electrical control of gastric emptying in denervated and reinnervated canine stomach: a pilot study.
Artif. Organs
14:
254-259,
1990[Medline].
19.
Grundfest-Broniatowski, S.,
A. Morritz,
L. Ilyes,
G. Jacobs,
J. Kasick,
E. Olsen,
and
Y. Nose.
Voluntary control of an ileal pouch by coordinated electrical stimulation: a pilot study in dog.
Dis. Colon Rectum
31:
261-267,
1988[Medline].
20.
Gustavsson, J., and G. Lindberg. Atropine reduces
dose-dependently the frequency of gastric electric activity in the fed
state (Abstract). In: Proc. of Fifth International
Workshop on Electrogastrography, Washington, DC, 1997, p. 25.
21.
Hocking, M. P.
Postoperative gastroparesis and tachygastria-response to electrical stimulation and erythromycin.
Surgery
114:
538-542,
1993[Medline].
22.
Hocking, M. P.,
S. B. Voel,
and
C. A. Sninsky.
Human gastric myoelectrical activity and gastric emptying following gastric surgery and with pacing.
Gastroenterology
103:
1811-1816,
1992[Medline].
23.
Johnson, B.,
B. Familoni,
T. L. Abell,
R. Werkman,
and
G. Wood.
Development of a canine model for gastric pacing (Abstract).
Gastroenterology
98:
A362,
1990.
24.
Kelly, K. A.
Pacing the gut.
Gastroenterology
103:
1967-1969,
1992[Medline].
25.
Kelly, K. A.,
and
C. F. Code.
Effect of transthoracic vagotomy on canine gastric activity.
Gastroenterology
57:
51-59,
1969[Medline].
26.
Kelly, K. A.,
and
R. C. LaForce.
Pacing the canine stomach with electric stimulation.
Am. J. Physiol.
222:
588-594,
1972[Medline].
27.
Kim, C. H.,
F. Azpiroz,
and
J. R. Malagelada.
Characteristic of spontaneous and drug-induced gastric dysrhythmias in chronic canine model.
Gastroenterology
90:
421-427,
1986[Medline].
28.
Kim, C. H.,
R. B. Hanson,
T. L. Abell,
M. Camilleri,
and
J. R. Malagelada.
Effects of inhibition of prostaglandin synthesis on epinephrine induced gastroduodenal electromechanical changes in humans.
Mayo Clin. Proc.
64:
149-157,
1989[Medline].
29.
Koch, K. L.,
R. M. Stern,
and
M. W. Vasey.
Gastric dysrhythmias and nausea of pregnancy.
Dig. Dis. Sci.
35:
961-968,
1990[Medline].
30.
Lee, K. Y.,
W. Y. Chey,
and
D. Coy.
Experimental production of tachyarrhythmia in canine antrum (Abstract).
Gastroenterology
76:
1182,
1979.
31.
Lin, X. M.,
M. Zhang,
and
J. D. Z. Chen.
Effective pacing parameters for the entrainment of gastrointestinal slow waves in dogs (Abstract).
Gastroenterology
114:
G3257,
1998.
32.
Lin, Z. Y.,
R. W. McCallum,
B. D. Schirmar,
and
J. D. Z. Chen.
Effects of pacing parameters on entrainment of gastric slow waves in patients with gastroparesis.
Am. J. Physiol.
274 (Gastrointest. Liver Physiol. 37):
G186-G191,
1998[Abstract/Free Full Text].
33.
McCallum, R. W.,
J. D. Z. Chen,
Z. Y. Lin,
B. D. Schirmer,
R. D. William,
and
R. A. Ross.
Gastric pacing improves emptying and symptoms in patients with gastroparesis.
Gastroenterology
114:
456-461,
1998[Medline].
34.
Miedema, B. W.,
M. G. Sarr,
and
K. A. Kelly.
Pacing the human stomach.
Surgery
111:
143-150,
1992[Medline].
35.
Morrison, P.,
B. M. Meidema,
L. Kohler,
and
K. A. Kelly.
Electrical dysrhythmias in the roux jejunal limb: cause and treatment.
Am. J. Surg.
160:
252-256,
1990[Medline].
36.
Nelsen, T. S.,
E. R. L. Eigenbrodt,
L. A. Keoshian,
C. Bunker,
and
L. Johnson.
Alterations in muscular and electrical activity of stomach following vagotomy.
Arch. Surg.
94:
821-835,
1967[Medline].
37.
Riezzo, G.,
F. Pezzolla,
G. Darconza,
and
I. Giorgio.
Gastric myoelectrical activity in the first trimester of pregnancy: a cutaneous electrogastrographic study.
Am. J. Gastroenterol.
87:
702-707,
1992[Medline].
38.
Stoddard, C. J.,
R. H. Smallwood,
and
H. L. Duthie.
Electrical arrhythmia's in the human stomach.
Gut
22:
705-712,
1981[Abstract].
Am J Physiol Gastroint Liver Physiol 276(2):G387-G392
0002-9513/99 $5.00
Copyright © 1999 the American Physiological Society