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Esophageal motility during food ingestion: A physiologic test of esophageal motor function
GASTROENTEROLOGY
1983;85:570-7
Esophageal Motility During Food Ingestion: A Physiologic Test of Esophageal Motor Function MARK
H. MELLOW
The Departments of Medicine at Georgetown University School of Medicine and the Veterans Administration Medical Center and the Division of Gastroenterology, Veterans Administration Medical Center, Washington, D.C.
It
is unknown whether esophageal motility, as assessed by standard motility testing, bears close relationship to motility occurring during food ingestion. Certainly, many patients, while reporting symptoms during food ingestion, are asymptomatic during standard motility testing; thus, a direct link between abnormal motility and symptomatology is often lacking. Twelve normal subjects and 5 patients with symptomatic esophageal motility disorders, therefore, underwent motility testing during upright ingestion of a meal which consisted of beef cubes and gravy. In normals, contraction parameters during food ingestion could not have been predicted by values obtained during standard testing (r = 0.2, p > 0.05). All 5 patients, although asymptomatic during standard testing, reported dysphagia during food ingestion. Evidence of abnormal motility could be observed simultaneously. Patterns of abnormality included nonperistaltic contractions (7.2 f 2.5 episodes per meal], instances of incomplete lower esophageal sphincter relaxation (2.8 -C 0.8 episodes per meal], and instances of lack of complete lower esophageal sphincter relaxation during ongoing esophageal contractions (4.6 + 1.0 episodes). These abnormalities were significantly more frequent in patients than in controls (p < O.OOl), and most had not been observed during standard testing in the patients. In addition, bethanechol significantly increased abnormal motility and increased dysphagia during food ingestion in the patients, but was without significant effect in controls. It was concluded, Received October 15, 1982. Accepted March 14, 1983. Address requests for reprints to Mark H. Mellow, M.D., Oklahoma City Clinic, Division of Gastroenterology, 701 N.E. 10th Street, Oklahoma City, Oklahoma 73104. The author thanks Cecilia Magnetti and the Dietetic Service for their support and Shirley A. Abernathy for her secretarial assistance. 0 1983 by the American Gastroenteroiogical Association 0016-5085/83/$3.00
therefore, that recording of esophageal motility during upright food ingestion appears to be of value in the diagnosis and characterization of motor abnormalities in patients with symptoms of esophageal motor
dysfunction.
In general, esophageal motility testing is performed with the patient in the supine position, as responses to small water boluses (5-10 cm3], ingested at set intervals (20-30 s), are recorded (1). These manometric techniques allow an accurate assessment of peristaltic activity and will offer an explanation of dysphagia or chest pain, or both, in many cases. The majority of patients, however, while reporting symptoms during food ingestion, will be asymptomatic during manometric evaluation (2). Thus, even after careful examination, the link between dysmotility and symptomatology is often lacking. In addition, it is not known whether esophageal motor function as assessed during “standard” esophageal motility testing (SEMT) bears any relationship to contractile activity during upright food ingestion. Recently, Kaye and Wexler (3) demonstrated that esophageal peristalsis is significantly altered by body position. Since the intraesophageal probe allows measurement of esophageal motility in the upright position, motility was evaluated during SEMT and food ingestion in the erect position in normal subjects and in patients with dysphagia. Materials The unteers with
study
population
no symptoms
primary
consisted
(6 men and 6 women),
gastrointestinal men),
and Methods
aged
or past history disorder,
30-67
esophageal
had the primary or endoscopic
yr
and [mean
motility
complaint evidence
of 12
aged 25-50 suggestive
5 patients 51
yr
yr),
disorders. of dysphagia,
of obstruction,
normal
(mean
of any upper
(3 women believed The
vol-
35 yr), and
to
5 patients
lacked and had
2
have all
radiologic no other
September
Table
MOTILITY DIJRIN(; FO01)
1983
1. Clinical
and Manometric
Patient. age (or). sex
INGESTION
571
Data M.W., 58. F
G.Z., 30. F
W.M.. 59, M
Y.J., 43, II’
WMc., 67. hl
S)TlptOIIlS
Dysphagid Chest pain Manometric data LESP (IIIJTIH~) (111 10-30) Incomplete LES relaxation? (nadir 2 5 mmHg) Esophageal contractions Amplitude (mmHg) (nl mean i 2 SD = 81 + 32) 5 cm 10 cm Duration (s) (nl mean 2 2 SD = 3.8 * 0.5) 5 cm 10 cm Nonperistaltic (%) LES = lower esophageal
sphincter.
84
158
72
197
231
51
83
71
187
305
6.7
6.2
5.0
8 .3
7.5
4.3
4.2
5.1
8.1
6.9
0
0
LESP = lower esophageal
sphincter
conditions known to produce esophageal motility disturbances (4-6) (Table 1). After fasting for at least 5 h, motility studies were performed, using intraesophageal pressure transducers (Model MP-3 probe, Honeywell, Inc., Denver, Col.) (7). Tracings were recorded on a multichannel direct-writing recorder (1508E Visicorder, Honeywell, Inc.) at a paper speed of 2.5 mm/s.
“Standard”
Esophageal
Motility
70
0
40
Testing
With the patients and subjects in the supine position. the probe was positioned so that all three transducers were in the stomach. The assembly was then withdrawn, at 0.5-cm intervals, through the area of the lower esophageal sphincter (LES). After this stepwise pull-through of the LES. the probe was positioned so as to record activity from 5 and 10 cm above the LES. Responses to 10 water swallows (s-cm” boluses), -30 s apart, were recorded. Subjects were then seated and the probe anchored so as to record from the LES and at 5 and 10 cm above the LES. Subjects were given a 180-g meal consisting of beef cubes and gravy, with water ad libitum. The meal was divided into two equal portions, the second portion (meal hTo. 2) being ingested 10 min after subcutaneous administration of bethanechol. 55 pg/kg. Subjects were instructed to press an event marker with every swallow (whether beef, water, or “dry”) and to ingest the meal at their normal pace. To determine whether an event marker to indicate swallows was, indeed, an accurate measure of swallowing, 4 subjects were tested with a recording catheter in the pharynx during food ingestion. To assess the temporal relationship between pharyngeal contractions and the event marking for each swallow, tracings were recorded at the increased paper speed of 5 mm/s. Swallows, as indicated by pharyngeal contractions, occurred 150 times. The subjects triggered the swallow-event marker on 145 of these actual swallows (97%); in 143, the pharyngeal con-
prrssurr:
traction and the event mark occurred within 0.5 s of each other. On only one occasion was the event marker triggered without an accompanying pharyngeal contraction. The following parameters were recorded: 1. During SEMT: mean and maximal amplitude; mean and maximal duration of contractions; number of nonperistaltic contractions; presence of spontaneous activity: presence of repetitive activity. Amplitude was measured, in millimeters of mercury, from the mean of esophageal baseline to the height of the contraction wave. Duration was measured, in seconds, from the onset of the major upstroke of the wave to the return of the wave to baseline. Maximal values refer to esophageal contractions having the greatest amplitude and duration. Spontaneous activity was defined as an esophageal contraction not preceded by swallow. Repetitive contractions were defined as three or more pressure peaks occurring in succession after a single swallow. Lower esophageal sphincter relaxation was evaluated during stepwise pull-through of the LES in the following manner: a “dry” swallow (no water bolus) was obtained at each station, and relaxation response was measured. If a dry swallow elicited an incomplete LES relaxation, a swallow was repeated in response to a 5-cm.’ water bolus, at the same station. Incomplete LES relaxation was defined as a fall in LES pressure to ~5 mmHg above midrespiratory gastric fundic pressure. [Using continuous sphincter pressure measurement, Dent (8) found a consistent swallow-associated drop in lower esophageal sphincter pressure (LESP) to 2.2 F 0.1 ntmHg in response to all swallows in normal subjects. Five millimeters of mercury represents an easily measurable value that is less susceptible to single-observer error. 1 2. During food ingestion: In addition to those parameters listed for SEMT, motility was analyzed with respect to number of swallows; number of contraction sequences [a contraction sequence was defined as an esophageal contraction occurring at both 5 cm and 10 cm above the LES in response to a swallow, whether peristaltic or nonperistaltic); number of “nontransmitted” swallows [number of
572
MELLOW
GASTROENTEROLOGY
swallows minus number of contraction sequences); number of nonperistaltic contraction sequences; evidence for absence of complete LES relaxation during esophageal contractions. Absence of complete LES relaxation was defined as the presence of a sustained pressure recording 25 mmHg above that of mean gastric fundic pressure. Absence of complete relaxation during esophageal contractions was noted as a result of (a) failure of the swallowinduced relaxation response, i.e., incomplete LES relaxation in association with a swallow-induced contraction, or (b) initial apparent complete LES relaxation but return to resting tone before conclusion of the contraction sequence (early LES “closure”). All persons studied were asked to relate any symptoms (e.g., dysphagia, chest pain) during SEMT and food ingestion. This study was approved by the Research and Development Committee and the Human Studies Committee, Veterans Administration Medical Center, April 1982.
Statistical
Analysis
Values obtained during food ingestion and SEMT were compared using Student’s unpaired t-tests. Values obtained during food ingestion before bethanechol and after bethanechol were analyzed using Student’s paired ttests, with each person as his own control. Correlations between individual values obtained in each subject between food ingestion and SEMT were analyzed by calculating linear correlation coefficients.
Results Normal
Subjects
Standard esophageal motility testing. In normal subjects, the mean (2 SEM) amplitude and duration of esophageal contractions at 5 and 10 cm above the LES were 98 * 10 and 85 t 11 mmHg, 3.8 + 0.2 and 3.6 ? 0.2, respectively. All normal subjects exhibited apparent complete LES relaxation at each station during stepwise pull-through. In almost every instance, LES relaxation was noted in response to dry swallows. Food ingestion. Mean amplitude and duration of esophageal contractions at 5 and 10 cm above the LES during food ingestion were similar to values recorded during SEMT (88 ? 10 and 87 2 8 mmHg, p > 0.05 vs. SEMT, 3.8 t 0.3 and 3.3 + 0.2 s, p > 0.05 vs. SEMT). When mean amplitude during SEMT was plotted against that observed during food ingestion for each individual subject, however, there was poor concordance, i.e., one could not predict an individual’s mean amplitude of contractions in the distal esophagus during food ingestion from values obtained during SEMT (r = 0.2, p > 0.05). A summary of the data obtained from the 12 normal subjects during food ingestion follows. Subjects ate rather quickly, each portion being con-
Vol. 85, No. 3
sumed in -6 min. Swallowing frequency was high, a swallow occurring approximately every 12 s. Often a person would swallow rapidly in succession. Under these circumstances, swallows would not evoke a contraction sequence, but would be accompanied by apparent complete LES relaxation during the entire swallow sequence (Figure 1A). In addition, swallows would often appear to interrupt previously initiated contraction sequences [Figure 1B). Nearly half the swallows (45%) failed to elicit a contraction sequence. Nonperistaltic contractions were observed occasionally in many subjects but, as in standard motility testing, nonperistaltic events rarely exceeded 10% of all contractions in any one person. Absence of LES relaxation during an ongoing contraction was infrequent. It never occurred more than twice in any subject and was almost always seen in association with a low amplitude esophageal contraction. One subject noted a single episode of transient “sticking” accompanying a prolonged esophageal contraction. Food ingestion after bethanechol. The mean duration of esophageal contractions at 5 cm and at 10 cm above the LES were significantly increased in mealNo.2vs.mealNo. l(3.3 -C 0.2sto4.1 + 0.4sat 10 cm above the LES, p < 0.01; 3.8 ? 0.3 s to 4.6 + 0.4 s at 5 cm above the LES, p < 0.001). Otherwise, eating after bethanechol did not significantly alter any measured parameter. Most importantly, no increase in nonperistaltic esophageal contractions, instances of incomplete LES relaxation, or absence of complete LES relaxation during esophageal contractions were noted. (p > 0.1 vs. meal No. 1. See Figure 2.) In addition, no normal subject experienced dysphagia or chest pain during food ingestion after bethanechol. Patients Standard esophageal motility testing. Baseline manometric and clinical data for the 5 patients are shown in Table 1. Three patients (G.Z., Y.J., W.Mc.) fit clinical and manometric criteria for high amplitude peristaltic esophageal contractions with dysphagia (“nutcracker” esophagus) (9); the remaining 2 patients were considered to have severe nonspecific motor disorders. During stepwise pullthrough of the LES, complete relaxation was observed at each station in 3 patients (although occasionally a water swallow was required to demonstrate complete relaxation). In 1 patient, a single instance of incomplete LES relaxation (to 8 mmHg) was observed in response to water swallow. The remaining patient had several instances of incomplete LES relaxation. All patients were asymptomatic during SEMT.
September
Figure
MOTILITY
1983
DURING
FOOD
INGESTION
573
1. Subject M.M. during food ingestion, with recording catheters at lower esophageal sphincter (LES) and 5 cm and 10 cm above LES. S indicates swallows. Dotted fine (bottom, left) = mean gastric fundic pressure. This tracing demonstrates multiple rapid swallows without transmitted esophageal contractions, but accompanied by apparent complete LES relaxation (a). B. Subject M.M. during food ingestion. with recording catheters as in A. S indicates swallows (a). Swallows appear to interrupt ongoing contractions at 5 cm above the LES
The percent of “nontransmitted” swallows (swallows unassociated with contraction sequences) was greater in the normal subjects (44 2 4.4 vs. 28 ? 4.4 in meal No. 1, p = 0.06; 42 ? 4.1 vs. 21 + 2.3 in meal No. 2, p < 0.01). This might reflect slower food ingestion and, hence, the decreased swallow frequency in the patients. In addition. however, there was often a difference in the response to rapid swallowing. In normals, swallows appeared to interrupt ongoing contraction sequences (Figure 1B). In the patients, several instances in which rapid swallows failed to inhibit contraction sequences were noted (Figure 3C). Most strikingly, normals and patients differed
Food ingestion. Amplitudes and durations of distal esophageal contractions differed between normals and patients during food ingestion (Table 2). In addition, patients and normals differed in several other respects. Patients tended to ingest the meal at a slower pace than the normal subjects (360 -t 41 s vs. 510 t 56 s; 0.05 < p < 0.1). That this slower food ingestion was related to intrinsic difficulty with eating (i.e., dysphagia) is suggested by the observation that the difference between groups was greater during meal No. 2 (360 ? 43 s vs. 587 + 79 s in patients, p < 0.05) and that this increased food ingestion time in the patients was associated with a subjective increase in dysphagia.
Figure
Meal Non-Peristaltic Esophageal
Contractions
#2
Meal
#l
Meal
Incomplete LES Relaxation
#2
Meal Absence During
#l of Complete
Esophageal
LES Relaxation Contractions
2
Episodes of nonperistaltic COIItractions. incomplete lower esophageal sphincter (LES) relaxation. and absence of complete LES relaxation during ongoing esophageal contractions during food ingestion before [meal No. 1) ,md after bethanechol (meal No. 21 in normal subjects and patients (shaded bars). Mean f SEM are shown. *p ‘. 0.01 brtween normals and patients: **p i (I.001 between normals and patients.
MELLOW
574
Table
2.
GASTROENTEROLOGY
Esophageal
Contractions
(mm&)
5 cm
(n = 12) (n = 5)
Duration
Max”
Mean
Max
87 + 9 197 -c 52"
142 + 17 317 + 75"
87 2 8 149 f 39'
132 -t 10 294 2 56" amplitude
with respect to the number of episodes of nonperistaltic esophageal contractions, instances of incomplete LES relaxation, and instances of absence of complete LES relaxation during ongoing esophageal contractions (Figure 2). Figures 3-5 depict manometric events during food ingestion, focusing on these abnormalities. The responses during food ingestion of patient G.Z. are, perhaps, the most noteworthy (Figure 3). Standard motility testing demonstrated high amplitude peristaltic esophageal contractions (Figure 3A). In addition, normal LES relaxation was observed during stepwise LES pullthrough. During food ingestion, however, numerous nonperistaltic contractions were observed, along with several instances of incomplete or absent LES relaxation (Figures 3B and 3C). (This patient had undergone four previous SEMTs, all failing to show any of the abnormalities elicited during food ingestion.) While always remaining asymptomatic during SEMT, she complained of dysphagia during food ingestion, at a time of concurrent dysmotility (Figure 3B). The responses of patients Y.J. and W.Mc. during food ingestion are depicted in Figures 4 and 5. Like G.Z., the motility during food ingestion of patient Y.J. revealed a variety of types of dysmotility not noted during SEMT. In patient W.Mc., the major abnormality during food ingestion consisted of high amplitude, very prolonged esophageal contractions usually associated with apparent complete LES relaxation. Overall, 4 of the 5 patients reported dysphagia during ingestion of meal No. 1. As stated previously, none of the patients complained of dysphagia during SEMT. Effect of bethanechol on food ingestion. Mean amplitude of esophageal contractions was not significantly altered by bethanechol. There was a significant increase in maximal amplitude of contractions during meal No. 2 (317 ?I 65 mmHg to 359 as well as an increase in ‘-c 74 mmHg, p < 0.05), mean duration of contractions (7.0 + 0.9 s to 9.0 2 s, p <
3
0.05).
Unlike normal subjects, administration of bethanecho1 in the patients resulted in a significant increase in the number of episodes of nonperistaltic esophageal contractions (7.2 2 2.5 to 11.6 2 3.4
(s)
5 cm
10 cm
Mean
All values mean + SEM. I’Maximal = contraction with greatest < 0.02.( p < 0.01. d 0.05 < p < 0.1.p p < 0.001.
1.0
85, No.
During Food Ingestion Amplitude
Subjects Patients
Vol.
10 cm Max
Mean 3.7 + 0.4 7.0 r O.Y<'
or duration,
Figure
7.3 k 0.4 12.7 " 1.3"
or both, during
.
b
Mean
-
Max
3.2 t 0.2 6.4 k 0.9"
food ingestion
5.7 2 0.5 11.6 i- 1.3"
in each subject.
I1p
d
L
3. A. Patient G.Z. Representative responses during standard esophageal motility testing. Catheter positions 15, 10, and 5 cm above lower esophageal sphincter (LES). High amplitude peristaltic contractions are seen. B. Patient G.Z. during food ingestion, Recording catheters at LES [dotted lines) and 5 cm and 10 cm above LES. S indicates swallows. Dashed lines (bottom, left] = mean gastric fundic pressure. (a] No LES relaxation, in association with a nonperistaltic esophageal contraction. (b) Complete LES relaxation in association with a peristaltic contraction. (c) No LES relaxation in association with a peristaltic contraction. Dysphagia reported. C. Patient G.Z. during food ingestion. Catheter position as in B. S indicates swallows. Dotted lines = mean gastric fundic pressure. (a] Complete lower esophageal sphincter (LES) relaxation during peristaltic contraction. (b) During a preexisting contraction sequence, a swallow elicits a new contraction at 5 cm above the LES, in association with incomplete LES relaxation. This may represent an example of failure of neural inhibition. (c) Complete LES relaxation with a peristaltic contraction of markedly increased amplitude and duration. (d) Incomplete LES relaxation in association with nonperistaltic contraction.
September
Figure
MOTILITY
1983
4. Patient Y.J. during food ingestion. &cording catheters at lower esophageal sphincter (LES) (broken lines in B and C) and at 5 and 10 cm above LES. S indicates swallows. Dotted fine (bottom, left] = mean gastric fundic pressure. Note that scale differs between body of esophagus and LES. A. High amplitude peristaltic contractions with LES relaxation. No symptoms reported. 13. (a) indicates relaxation with high amplitude peristaltiL contraction. (b) indicates early LES “closure.” (c] indicates incomplete LES relaxation in response to swallow. Dysphagia reported. C. [a) indicates nonperistaltic repetitive contraction with complete LES relaxation. [b] indicates high amplitude. prolonged. nonperistaltic contraction. with LES relaxation. Dysphagia reported.
DURING
FOOD
INGESTION
575
amplitude and duration of contractions measured during standard manometry and those measured during food ingestion in normal subjects. Thus, one cannot predict motility during ingestion from that observed during routine manometric testing. The differences between contraction parameters during standard testing and food ingestion could have occurred as a result of several factors. Contractions in response to rapidly spaced swallows differ from those in response to swallows spaced at 20-30-s intervals (10). Also, bolus size and consistency may have affected contraction parameters since, in some subjects, amplitude and duration of contractions differed from those seen during standard testing even when swallows were spaced at intervals >20 s. Also, it has been shown that contractions in the upright position differ from those in the supine position (3). Whether a subject’s motility might differ as a result of type, temperature, or speed of food ingested, or some combination thereof, will require further study. Patients rarely complain of dysphagia during standard manometric testing, and none of the study patients, all with histories of dysphagia, experienced symptoms during standard testing. In contrast, dysphagia occurred during food ingestion in all 5 pa-
episodes per meal, p < 0.05) as well as instances of absence of complete LES relaxation during ongoing esophageal contractions (4.6 k 1.0 to 9.4 k 2.0 episodes per meal, p < 0.05; Figure 3). All 5 patients reported dysphagia during food ingestion after bethanechol that was, subjectively, greater than reported during meal No. 1.
Discussion
i.
‘,.
Although recent improvements in manometric technology have allowed more precise characterization of the peristaltic sequence, this study indicates that several parameters of esophageal contractions recorded during standard motility testing bear little relationship to those occurring during food ingestion. There was a poor correlation between
_.
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._,I
.I’
:
_,
‘\- .-__..,,. z /c’7_ IO Ior.
Figure
5
Patient W.Mc. during food ingestion. Recording catheters at LES and at 5 and 10 cm above lower esophageal sphincter (LES). S indicates swallows. Dotted line (bottom, left) = mean gastric fundic pressure. Note high amplitude, prolonged esophageal contractions in association with apparent complete LES relaxation. Dysphagia reported.
576
MELLOW
tients. Moreover, evidence of dysmotility, presumably the cause of the dysphagia, could be observed simultaneously. Abnormal motility patterns, not seen during SEMT, were observed in the patients during food ingestion. Most commonly, this involved absence of complete LES relaxation during ongoing esophageal contractions, either as a result of failure of the swallow-induced relaxation response or, despite initial relaxation, reestablishment of resting LESP during an ongoing esophageal contraction. In 3 patients, nonperistaltic contractions were observed during food ingestion while “standard” motility testing exhibited only peristaltic contractions. Response to food ingestion in patient G.Z., diagnosed as having high amplitude peristaltic esophageal contractions (“nutcracker” esophagus), was especially noteworthy. Numerous instances of nonperistaltic esophageal contractions and of contractions occurring at times of incomplete LES relaxation were observed, neither of which had been apparent on several previous manometric studies. In previous studies, bethanechol was used in an attempt to elicit symptoms or esophageal motility abnormalities, or both (11). In the present investigation, a portion of the meal (meal No. 2) was ingested after bethanechol. Although 4 of the 5 patients were symptomatic during food ingestion alone, ingestion of food after bethanechol resulted in an increase in symptoms in these 4 and onset of dysphagia in the other patient, as well as more marked abnormalities in esophageal motility. At the dose employed, ingestion of food after bethanechol was not associated with abnormal motility patterns or symptoms in the controls. Thus, food ingestion after bethanechol may be a useful provocative test in patients who remain asymptomatic or whose motility is normal or near normal during food ingestion alone. shown that rapid Meyer et al. (10) have recently swallowing may affect peristalsis, both by initiating a refractory state of the esophageal smooth muscle and by direct inhibitory neuronal discharge. In their investigation, rapid ingestion of liquid boluses was examined during standard manometry. The findings in this study suggest that similar events occur during normal food ingestion (Figures 1A and lB), some rapid swallows interrupting an already initiated contraction sequence (presumably via neural inhibition], and other rapid swallows occurring without a resultant contraction sequence. In fact, a large percentage of time of food ingestion in normal subjects involved rapid swallowing with interrupted or noninitiated esophageal contractions, or with both, OCcurring in association with apparent complete LES relaxation, the esophagus presumably serving as a passive conduit. Before the onset of food ingestion, an effort was
GASTROENTEROLOGY
Vol. 85, No. 3
made to position the probe so as to record from at or near the maximal high pressure zone of the LES. Since some minor probe movement almost certainly occurred during the meal consumption, however, no attempt was made to quantify resting LESP during stages of the meal. Furthermore, due to longitudinal muscle contractions during peristalsis, the esophagus moves orad in relation to the rather fixed probe position. This orad movement may, on occasion, allow the probe to “drop” into the stomach, recording gastric fundic pressure rather than actual LES (12). Thus, some instances of LES “relaxrelaxation ation” during food ingestion may be more apparent than real. Continuous measurement of LESP by use of a “sleeve” device similar to that used by Dent (8) during perfusion manomentry should improve accuracy of observations regarding both LES relaxation and resting LESP. Probe movement artefact, however, could not explain the most important observation-that incomplete LES relaxation frequently occurred at times of ongoing esophageal contractions. In addition, these instances of incomplete LES relaxation during esophageal contractions were observed during patients’ complaints of dysphagia. Recent refinements in technique have allowed measurement of the transit of radionuclide bolus through the esophagus and, in certain patients, have revealed abnormalities when standard motility testing has been considered to be within normal limits (13). Thus, radionuclide transit studies appear to be useful screening tests for the presence of an esophageal motor disorder. The specific motor dysfunction responsible for delay in transit, however, is not defined in these studies, and instances of dysphagia or chest pain during transit studies have not been reported. Thus, manometry during upright food ingestion may be useful in pinpointing the exact type of abnormality in each patient and, perhaps, in enabling the physician to tailor treatment to the specific abnormality. For example, patients with evidence of predominant LES dysfunction during food ingestion might benefit from pneumatic dilation, whereas those patients with predominant abnormalities of esophageal dysmotility may benefit from pharmacologic agents that decrease amplitude or duration, or both, of contractions. In conclusion, this study demonstrates that esophageal motility during food ingestion differs from that occurring during standard manometry and that testing during food ingestion is more likely to allow observation of motor function while the patient is symptomatic. Since we eat and drink in an upright position, consume food at a variable pace, and swallow boluses of varying size and consistency, perhaps esophageal motility is better assessed under these conditions.
September
1983
MOTlLlTY
References 1. 2.
3. 4. 5.
6.
7.
Hollis JB. Caste11 DO. Effect of dry swallows and wet swalJ Appl lows of different volumes on esophageal peristalsis. Physiol 1975:33:1161-4. Brand DL, Martin D. Pope CE. Esophageal manometrics in patients with angina-like chest pain. Dig Dis Sci 1977; 22:300-4. Kaye MD, Wexler NM. Alteration of esophageal peristalsis by body position. Dig Dis Sci 1981;26:897-901. Bennett JR, Hendrix TR. Diffuse esophageal spasm, a disorder with more than one cause. Gastroenterology 1970;59:273-9. VanTrappen G, Janssens HO, Hellemans J, Coremans C. Achalasia. diffuse esophageal spasm, and related motility disorders. Gastroenterology 1979;76:450-7. Mellow MH. The effect of isosorbide and hydralazine in painful primary esophageal motility disorders. Gastroenterology 1982;83:364-70. Humphries TJ, Caste11 DO. Pressure profile of esophageal
8. 9.
10.
11.
12.
13.
DIJRINI;
FOOD
INGESTION
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peristalsis in normal humans as measured by direct intraesophageal transducers. Dig Dis Sci 1977:22:641-5. Dent J. A new technique for continuous sphincter pressure measurement. Gastroenterology 1976;71:263-7. Benjamin SB, Gerhardt DC, Caste11 DO. High amplitude. peristaltic esophageal contractions associated with chest pain and/or dysphagia. Gastroenterology 1979:77:478-83. Meyer GW, Gerhardt DC, Caste11 DO Human esophageal response to rapid swallowing: muscle refractor!, period or neural inhibition? Am J Physiol 1981;241:1;129-36. Mellow M. Symptomatic diffuse esophageal spasm; manometric follow-up and response to cholinergic stimulation and cholinesterase inhibition. Gastroenterology 1977:73:2:<7-40. Dodds WJ. Stewart ET, Hogan IVJ. Stef JJ. Arndorfer RC. Effe[.t of esophageal movement on intraluminal esophageal pressure recording. Gastroenterology 1974;67:592-6110. Russell COH, Hill LD, Holmes ER. Hull DA, Cannon R, Pope CE. Radionuclide transit: a sensitive screening test for esophageal dysfunction. Gastroenterology 1981:80:887-92.
1983;85:570-7
Esophageal Motility During Food Ingestion: A Physiologic Test of Esophageal Motor Function MARK
H. MELLOW
The Departments of Medicine at Georgetown University School of Medicine and the Veterans Administration Medical Center and the Division of Gastroenterology, Veterans Administration Medical Center, Washington, D.C.
It
is unknown whether esophageal motility, as assessed by standard motility testing, bears close relationship to motility occurring during food ingestion. Certainly, many patients, while reporting symptoms during food ingestion, are asymptomatic during standard motility testing; thus, a direct link between abnormal motility and symptomatology is often lacking. Twelve normal subjects and 5 patients with symptomatic esophageal motility disorders, therefore, underwent motility testing during upright ingestion of a meal which consisted of beef cubes and gravy. In normals, contraction parameters during food ingestion could not have been predicted by values obtained during standard testing (r = 0.2, p > 0.05). All 5 patients, although asymptomatic during standard testing, reported dysphagia during food ingestion. Evidence of abnormal motility could be observed simultaneously. Patterns of abnormality included nonperistaltic contractions (7.2 f 2.5 episodes per meal], instances of incomplete lower esophageal sphincter relaxation (2.8 -C 0.8 episodes per meal], and instances of lack of complete lower esophageal sphincter relaxation during ongoing esophageal contractions (4.6 + 1.0 episodes). These abnormalities were significantly more frequent in patients than in controls (p < O.OOl), and most had not been observed during standard testing in the patients. In addition, bethanechol significantly increased abnormal motility and increased dysphagia during food ingestion in the patients, but was without significant effect in controls. It was concluded, Received October 15, 1982. Accepted March 14, 1983. Address requests for reprints to Mark H. Mellow, M.D., Oklahoma City Clinic, Division of Gastroenterology, 701 N.E. 10th Street, Oklahoma City, Oklahoma 73104. The author thanks Cecilia Magnetti and the Dietetic Service for their support and Shirley A. Abernathy for her secretarial assistance. 0 1983 by the American Gastroenteroiogical Association 0016-5085/83/$3.00
therefore, that recording of esophageal motility during upright food ingestion appears to be of value in the diagnosis and characterization of motor abnormalities in patients with symptoms of esophageal motor
dysfunction.
In general, esophageal motility testing is performed with the patient in the supine position, as responses to small water boluses (5-10 cm3], ingested at set intervals (20-30 s), are recorded (1). These manometric techniques allow an accurate assessment of peristaltic activity and will offer an explanation of dysphagia or chest pain, or both, in many cases. The majority of patients, however, while reporting symptoms during food ingestion, will be asymptomatic during manometric evaluation (2). Thus, even after careful examination, the link between dysmotility and symptomatology is often lacking. In addition, it is not known whether esophageal motor function as assessed during “standard” esophageal motility testing (SEMT) bears any relationship to contractile activity during upright food ingestion. Recently, Kaye and Wexler (3) demonstrated that esophageal peristalsis is significantly altered by body position. Since the intraesophageal probe allows measurement of esophageal motility in the upright position, motility was evaluated during SEMT and food ingestion in the erect position in normal subjects and in patients with dysphagia. Materials The unteers with
study
population
no symptoms
primary
consisted
(6 men and 6 women),
gastrointestinal men),
and Methods
aged
or past history disorder,
30-67
esophageal
had the primary or endoscopic
yr
and [mean
motility
complaint evidence
of 12
aged 25-50 suggestive
5 patients 51
yr
yr),
disorders. of dysphagia,
of obstruction,
normal
(mean
of any upper
(3 women believed The
vol-
35 yr), and
to
5 patients
lacked and had
2
have all
radiologic no other
September
Table
MOTILITY DIJRIN(; FO01)
1983
1. Clinical
and Manometric
Patient. age (or). sex
INGESTION
571
Data M.W., 58. F
G.Z., 30. F
W.M.. 59, M
Y.J., 43, II’
WMc., 67. hl
S)TlptOIIlS
Dysphagid Chest pain Manometric data LESP (IIIJTIH~) (111 10-30) Incomplete LES relaxation? (nadir 2 5 mmHg) Esophageal contractions Amplitude (mmHg) (nl mean i 2 SD = 81 + 32) 5 cm 10 cm Duration (s) (nl mean 2 2 SD = 3.8 * 0.5) 5 cm 10 cm Nonperistaltic (%) LES = lower esophageal
sphincter.
84
158
72
197
231
51
83
71
187
305
6.7
6.2
5.0
8 .3
7.5
4.3
4.2
5.1
8.1
6.9
0
0
LESP = lower esophageal
sphincter
conditions known to produce esophageal motility disturbances (4-6) (Table 1). After fasting for at least 5 h, motility studies were performed, using intraesophageal pressure transducers (Model MP-3 probe, Honeywell, Inc., Denver, Col.) (7). Tracings were recorded on a multichannel direct-writing recorder (1508E Visicorder, Honeywell, Inc.) at a paper speed of 2.5 mm/s.
“Standard”
Esophageal
Motility
70
0
40
Testing
With the patients and subjects in the supine position. the probe was positioned so that all three transducers were in the stomach. The assembly was then withdrawn, at 0.5-cm intervals, through the area of the lower esophageal sphincter (LES). After this stepwise pull-through of the LES. the probe was positioned so as to record activity from 5 and 10 cm above the LES. Responses to 10 water swallows (s-cm” boluses), -30 s apart, were recorded. Subjects were then seated and the probe anchored so as to record from the LES and at 5 and 10 cm above the LES. Subjects were given a 180-g meal consisting of beef cubes and gravy, with water ad libitum. The meal was divided into two equal portions, the second portion (meal hTo. 2) being ingested 10 min after subcutaneous administration of bethanechol. 55 pg/kg. Subjects were instructed to press an event marker with every swallow (whether beef, water, or “dry”) and to ingest the meal at their normal pace. To determine whether an event marker to indicate swallows was, indeed, an accurate measure of swallowing, 4 subjects were tested with a recording catheter in the pharynx during food ingestion. To assess the temporal relationship between pharyngeal contractions and the event marking for each swallow, tracings were recorded at the increased paper speed of 5 mm/s. Swallows, as indicated by pharyngeal contractions, occurred 150 times. The subjects triggered the swallow-event marker on 145 of these actual swallows (97%); in 143, the pharyngeal con-
prrssurr:
traction and the event mark occurred within 0.5 s of each other. On only one occasion was the event marker triggered without an accompanying pharyngeal contraction. The following parameters were recorded: 1. During SEMT: mean and maximal amplitude; mean and maximal duration of contractions; number of nonperistaltic contractions; presence of spontaneous activity: presence of repetitive activity. Amplitude was measured, in millimeters of mercury, from the mean of esophageal baseline to the height of the contraction wave. Duration was measured, in seconds, from the onset of the major upstroke of the wave to the return of the wave to baseline. Maximal values refer to esophageal contractions having the greatest amplitude and duration. Spontaneous activity was defined as an esophageal contraction not preceded by swallow. Repetitive contractions were defined as three or more pressure peaks occurring in succession after a single swallow. Lower esophageal sphincter relaxation was evaluated during stepwise pull-through of the LES in the following manner: a “dry” swallow (no water bolus) was obtained at each station, and relaxation response was measured. If a dry swallow elicited an incomplete LES relaxation, a swallow was repeated in response to a 5-cm.’ water bolus, at the same station. Incomplete LES relaxation was defined as a fall in LES pressure to ~5 mmHg above midrespiratory gastric fundic pressure. [Using continuous sphincter pressure measurement, Dent (8) found a consistent swallow-associated drop in lower esophageal sphincter pressure (LESP) to 2.2 F 0.1 ntmHg in response to all swallows in normal subjects. Five millimeters of mercury represents an easily measurable value that is less susceptible to single-observer error. 1 2. During food ingestion: In addition to those parameters listed for SEMT, motility was analyzed with respect to number of swallows; number of contraction sequences [a contraction sequence was defined as an esophageal contraction occurring at both 5 cm and 10 cm above the LES in response to a swallow, whether peristaltic or nonperistaltic); number of “nontransmitted” swallows [number of
572
MELLOW
GASTROENTEROLOGY
swallows minus number of contraction sequences); number of nonperistaltic contraction sequences; evidence for absence of complete LES relaxation during esophageal contractions. Absence of complete LES relaxation was defined as the presence of a sustained pressure recording 25 mmHg above that of mean gastric fundic pressure. Absence of complete relaxation during esophageal contractions was noted as a result of (a) failure of the swallowinduced relaxation response, i.e., incomplete LES relaxation in association with a swallow-induced contraction, or (b) initial apparent complete LES relaxation but return to resting tone before conclusion of the contraction sequence (early LES “closure”). All persons studied were asked to relate any symptoms (e.g., dysphagia, chest pain) during SEMT and food ingestion. This study was approved by the Research and Development Committee and the Human Studies Committee, Veterans Administration Medical Center, April 1982.
Statistical
Analysis
Values obtained during food ingestion and SEMT were compared using Student’s unpaired t-tests. Values obtained during food ingestion before bethanechol and after bethanechol were analyzed using Student’s paired ttests, with each person as his own control. Correlations between individual values obtained in each subject between food ingestion and SEMT were analyzed by calculating linear correlation coefficients.
Results Normal
Subjects
Standard esophageal motility testing. In normal subjects, the mean (2 SEM) amplitude and duration of esophageal contractions at 5 and 10 cm above the LES were 98 * 10 and 85 t 11 mmHg, 3.8 + 0.2 and 3.6 ? 0.2, respectively. All normal subjects exhibited apparent complete LES relaxation at each station during stepwise pull-through. In almost every instance, LES relaxation was noted in response to dry swallows. Food ingestion. Mean amplitude and duration of esophageal contractions at 5 and 10 cm above the LES during food ingestion were similar to values recorded during SEMT (88 ? 10 and 87 2 8 mmHg, p > 0.05 vs. SEMT, 3.8 t 0.3 and 3.3 + 0.2 s, p > 0.05 vs. SEMT). When mean amplitude during SEMT was plotted against that observed during food ingestion for each individual subject, however, there was poor concordance, i.e., one could not predict an individual’s mean amplitude of contractions in the distal esophagus during food ingestion from values obtained during SEMT (r = 0.2, p > 0.05). A summary of the data obtained from the 12 normal subjects during food ingestion follows. Subjects ate rather quickly, each portion being con-
Vol. 85, No. 3
sumed in -6 min. Swallowing frequency was high, a swallow occurring approximately every 12 s. Often a person would swallow rapidly in succession. Under these circumstances, swallows would not evoke a contraction sequence, but would be accompanied by apparent complete LES relaxation during the entire swallow sequence (Figure 1A). In addition, swallows would often appear to interrupt previously initiated contraction sequences [Figure 1B). Nearly half the swallows (45%) failed to elicit a contraction sequence. Nonperistaltic contractions were observed occasionally in many subjects but, as in standard motility testing, nonperistaltic events rarely exceeded 10% of all contractions in any one person. Absence of LES relaxation during an ongoing contraction was infrequent. It never occurred more than twice in any subject and was almost always seen in association with a low amplitude esophageal contraction. One subject noted a single episode of transient “sticking” accompanying a prolonged esophageal contraction. Food ingestion after bethanechol. The mean duration of esophageal contractions at 5 cm and at 10 cm above the LES were significantly increased in mealNo.2vs.mealNo. l(3.3 -C 0.2sto4.1 + 0.4sat 10 cm above the LES, p < 0.01; 3.8 ? 0.3 s to 4.6 + 0.4 s at 5 cm above the LES, p < 0.001). Otherwise, eating after bethanechol did not significantly alter any measured parameter. Most importantly, no increase in nonperistaltic esophageal contractions, instances of incomplete LES relaxation, or absence of complete LES relaxation during esophageal contractions were noted. (p > 0.1 vs. meal No. 1. See Figure 2.) In addition, no normal subject experienced dysphagia or chest pain during food ingestion after bethanechol. Patients Standard esophageal motility testing. Baseline manometric and clinical data for the 5 patients are shown in Table 1. Three patients (G.Z., Y.J., W.Mc.) fit clinical and manometric criteria for high amplitude peristaltic esophageal contractions with dysphagia (“nutcracker” esophagus) (9); the remaining 2 patients were considered to have severe nonspecific motor disorders. During stepwise pullthrough of the LES, complete relaxation was observed at each station in 3 patients (although occasionally a water swallow was required to demonstrate complete relaxation). In 1 patient, a single instance of incomplete LES relaxation (to 8 mmHg) was observed in response to water swallow. The remaining patient had several instances of incomplete LES relaxation. All patients were asymptomatic during SEMT.
September
Figure
MOTILITY
1983
DURING
FOOD
INGESTION
573
1. Subject M.M. during food ingestion, with recording catheters at lower esophageal sphincter (LES) and 5 cm and 10 cm above LES. S indicates swallows. Dotted fine (bottom, left) = mean gastric fundic pressure. This tracing demonstrates multiple rapid swallows without transmitted esophageal contractions, but accompanied by apparent complete LES relaxation (a). B. Subject M.M. during food ingestion. with recording catheters as in A. S indicates swallows (a). Swallows appear to interrupt ongoing contractions at 5 cm above the LES
The percent of “nontransmitted” swallows (swallows unassociated with contraction sequences) was greater in the normal subjects (44 2 4.4 vs. 28 ? 4.4 in meal No. 1, p = 0.06; 42 ? 4.1 vs. 21 + 2.3 in meal No. 2, p < 0.01). This might reflect slower food ingestion and, hence, the decreased swallow frequency in the patients. In addition. however, there was often a difference in the response to rapid swallowing. In normals, swallows appeared to interrupt ongoing contraction sequences (Figure 1B). In the patients, several instances in which rapid swallows failed to inhibit contraction sequences were noted (Figure 3C). Most strikingly, normals and patients differed
Food ingestion. Amplitudes and durations of distal esophageal contractions differed between normals and patients during food ingestion (Table 2). In addition, patients and normals differed in several other respects. Patients tended to ingest the meal at a slower pace than the normal subjects (360 -t 41 s vs. 510 t 56 s; 0.05 < p < 0.1). That this slower food ingestion was related to intrinsic difficulty with eating (i.e., dysphagia) is suggested by the observation that the difference between groups was greater during meal No. 2 (360 ? 43 s vs. 587 + 79 s in patients, p < 0.05) and that this increased food ingestion time in the patients was associated with a subjective increase in dysphagia.
Figure
Meal Non-Peristaltic Esophageal
Contractions
#2
Meal
#l
Meal
Incomplete LES Relaxation
#2
Meal Absence During
#l of Complete
Esophageal
LES Relaxation Contractions
2
Episodes of nonperistaltic COIItractions. incomplete lower esophageal sphincter (LES) relaxation. and absence of complete LES relaxation during ongoing esophageal contractions during food ingestion before [meal No. 1) ,md after bethanechol (meal No. 21 in normal subjects and patients (shaded bars). Mean f SEM are shown. *p ‘. 0.01 brtween normals and patients: **p i (I.001 between normals and patients.
MELLOW
574
Table
2.
GASTROENTEROLOGY
Esophageal
Contractions
(mm&)
5 cm
(n = 12) (n = 5)
Duration
Max”
Mean
Max
87 + 9 197 -c 52"
142 + 17 317 + 75"
87 2 8 149 f 39'
132 -t 10 294 2 56" amplitude
with respect to the number of episodes of nonperistaltic esophageal contractions, instances of incomplete LES relaxation, and instances of absence of complete LES relaxation during ongoing esophageal contractions (Figure 2). Figures 3-5 depict manometric events during food ingestion, focusing on these abnormalities. The responses during food ingestion of patient G.Z. are, perhaps, the most noteworthy (Figure 3). Standard motility testing demonstrated high amplitude peristaltic esophageal contractions (Figure 3A). In addition, normal LES relaxation was observed during stepwise LES pullthrough. During food ingestion, however, numerous nonperistaltic contractions were observed, along with several instances of incomplete or absent LES relaxation (Figures 3B and 3C). (This patient had undergone four previous SEMTs, all failing to show any of the abnormalities elicited during food ingestion.) While always remaining asymptomatic during SEMT, she complained of dysphagia during food ingestion, at a time of concurrent dysmotility (Figure 3B). The responses of patients Y.J. and W.Mc. during food ingestion are depicted in Figures 4 and 5. Like G.Z., the motility during food ingestion of patient Y.J. revealed a variety of types of dysmotility not noted during SEMT. In patient W.Mc., the major abnormality during food ingestion consisted of high amplitude, very prolonged esophageal contractions usually associated with apparent complete LES relaxation. Overall, 4 of the 5 patients reported dysphagia during ingestion of meal No. 1. As stated previously, none of the patients complained of dysphagia during SEMT. Effect of bethanechol on food ingestion. Mean amplitude of esophageal contractions was not significantly altered by bethanechol. There was a significant increase in maximal amplitude of contractions during meal No. 2 (317 ?I 65 mmHg to 359 as well as an increase in ‘-c 74 mmHg, p < 0.05), mean duration of contractions (7.0 + 0.9 s to 9.0 2 s, p <
3
0.05).
Unlike normal subjects, administration of bethanecho1 in the patients resulted in a significant increase in the number of episodes of nonperistaltic esophageal contractions (7.2 2 2.5 to 11.6 2 3.4
(s)
5 cm
10 cm
Mean
All values mean + SEM. I’Maximal = contraction with greatest < 0.02.( p < 0.01. d 0.05 < p < 0.1.p p < 0.001.
1.0
85, No.
During Food Ingestion Amplitude
Subjects Patients
Vol.
10 cm Max
Mean 3.7 + 0.4 7.0 r O.Y<'
or duration,
Figure
7.3 k 0.4 12.7 " 1.3"
or both, during
.
b
Mean
-
Max
3.2 t 0.2 6.4 k 0.9"
food ingestion
5.7 2 0.5 11.6 i- 1.3"
in each subject.
I1p
d
L
3. A. Patient G.Z. Representative responses during standard esophageal motility testing. Catheter positions 15, 10, and 5 cm above lower esophageal sphincter (LES). High amplitude peristaltic contractions are seen. B. Patient G.Z. during food ingestion, Recording catheters at LES [dotted lines) and 5 cm and 10 cm above LES. S indicates swallows. Dashed lines (bottom, left] = mean gastric fundic pressure. (a] No LES relaxation, in association with a nonperistaltic esophageal contraction. (b) Complete LES relaxation in association with a peristaltic contraction. (c) No LES relaxation in association with a peristaltic contraction. Dysphagia reported. C. Patient G.Z. during food ingestion. Catheter position as in B. S indicates swallows. Dotted lines = mean gastric fundic pressure. (a] Complete lower esophageal sphincter (LES) relaxation during peristaltic contraction. (b) During a preexisting contraction sequence, a swallow elicits a new contraction at 5 cm above the LES, in association with incomplete LES relaxation. This may represent an example of failure of neural inhibition. (c) Complete LES relaxation with a peristaltic contraction of markedly increased amplitude and duration. (d) Incomplete LES relaxation in association with nonperistaltic contraction.
September
Figure
MOTILITY
1983
4. Patient Y.J. during food ingestion. &cording catheters at lower esophageal sphincter (LES) (broken lines in B and C) and at 5 and 10 cm above LES. S indicates swallows. Dotted fine (bottom, left] = mean gastric fundic pressure. Note that scale differs between body of esophagus and LES. A. High amplitude peristaltic contractions with LES relaxation. No symptoms reported. 13. (a) indicates relaxation with high amplitude peristaltiL contraction. (b) indicates early LES “closure.” (c] indicates incomplete LES relaxation in response to swallow. Dysphagia reported. C. [a) indicates nonperistaltic repetitive contraction with complete LES relaxation. [b] indicates high amplitude. prolonged. nonperistaltic contraction. with LES relaxation. Dysphagia reported.
DURING
FOOD
INGESTION
575
amplitude and duration of contractions measured during standard manometry and those measured during food ingestion in normal subjects. Thus, one cannot predict motility during ingestion from that observed during routine manometric testing. The differences between contraction parameters during standard testing and food ingestion could have occurred as a result of several factors. Contractions in response to rapidly spaced swallows differ from those in response to swallows spaced at 20-30-s intervals (10). Also, bolus size and consistency may have affected contraction parameters since, in some subjects, amplitude and duration of contractions differed from those seen during standard testing even when swallows were spaced at intervals >20 s. Also, it has been shown that contractions in the upright position differ from those in the supine position (3). Whether a subject’s motility might differ as a result of type, temperature, or speed of food ingested, or some combination thereof, will require further study. Patients rarely complain of dysphagia during standard manometric testing, and none of the study patients, all with histories of dysphagia, experienced symptoms during standard testing. In contrast, dysphagia occurred during food ingestion in all 5 pa-
episodes per meal, p < 0.05) as well as instances of absence of complete LES relaxation during ongoing esophageal contractions (4.6 k 1.0 to 9.4 k 2.0 episodes per meal, p < 0.05; Figure 3). All 5 patients reported dysphagia during food ingestion after bethanechol that was, subjectively, greater than reported during meal No. 1.
Discussion
i.
‘,.
Although recent improvements in manometric technology have allowed more precise characterization of the peristaltic sequence, this study indicates that several parameters of esophageal contractions recorded during standard motility testing bear little relationship to those occurring during food ingestion. There was a poor correlation between
_.
,.. ,~
,.’ ., ;...:,;,_...
._,I
.I’
:
_,
‘\- .-__..,,. z /c’7_ IO Ior.
Figure
5
Patient W.Mc. during food ingestion. Recording catheters at LES and at 5 and 10 cm above lower esophageal sphincter (LES). S indicates swallows. Dotted line (bottom, left) = mean gastric fundic pressure. Note high amplitude, prolonged esophageal contractions in association with apparent complete LES relaxation. Dysphagia reported.
576
MELLOW
tients. Moreover, evidence of dysmotility, presumably the cause of the dysphagia, could be observed simultaneously. Abnormal motility patterns, not seen during SEMT, were observed in the patients during food ingestion. Most commonly, this involved absence of complete LES relaxation during ongoing esophageal contractions, either as a result of failure of the swallow-induced relaxation response or, despite initial relaxation, reestablishment of resting LESP during an ongoing esophageal contraction. In 3 patients, nonperistaltic contractions were observed during food ingestion while “standard” motility testing exhibited only peristaltic contractions. Response to food ingestion in patient G.Z., diagnosed as having high amplitude peristaltic esophageal contractions (“nutcracker” esophagus), was especially noteworthy. Numerous instances of nonperistaltic esophageal contractions and of contractions occurring at times of incomplete LES relaxation were observed, neither of which had been apparent on several previous manometric studies. In previous studies, bethanechol was used in an attempt to elicit symptoms or esophageal motility abnormalities, or both (11). In the present investigation, a portion of the meal (meal No. 2) was ingested after bethanechol. Although 4 of the 5 patients were symptomatic during food ingestion alone, ingestion of food after bethanechol resulted in an increase in symptoms in these 4 and onset of dysphagia in the other patient, as well as more marked abnormalities in esophageal motility. At the dose employed, ingestion of food after bethanechol was not associated with abnormal motility patterns or symptoms in the controls. Thus, food ingestion after bethanechol may be a useful provocative test in patients who remain asymptomatic or whose motility is normal or near normal during food ingestion alone. shown that rapid Meyer et al. (10) have recently swallowing may affect peristalsis, both by initiating a refractory state of the esophageal smooth muscle and by direct inhibitory neuronal discharge. In their investigation, rapid ingestion of liquid boluses was examined during standard manometry. The findings in this study suggest that similar events occur during normal food ingestion (Figures 1A and lB), some rapid swallows interrupting an already initiated contraction sequence (presumably via neural inhibition], and other rapid swallows occurring without a resultant contraction sequence. In fact, a large percentage of time of food ingestion in normal subjects involved rapid swallowing with interrupted or noninitiated esophageal contractions, or with both, OCcurring in association with apparent complete LES relaxation, the esophagus presumably serving as a passive conduit. Before the onset of food ingestion, an effort was
GASTROENTEROLOGY
Vol. 85, No. 3
made to position the probe so as to record from at or near the maximal high pressure zone of the LES. Since some minor probe movement almost certainly occurred during the meal consumption, however, no attempt was made to quantify resting LESP during stages of the meal. Furthermore, due to longitudinal muscle contractions during peristalsis, the esophagus moves orad in relation to the rather fixed probe position. This orad movement may, on occasion, allow the probe to “drop” into the stomach, recording gastric fundic pressure rather than actual LES (12). Thus, some instances of LES “relaxrelaxation ation” during food ingestion may be more apparent than real. Continuous measurement of LESP by use of a “sleeve” device similar to that used by Dent (8) during perfusion manomentry should improve accuracy of observations regarding both LES relaxation and resting LESP. Probe movement artefact, however, could not explain the most important observation-that incomplete LES relaxation frequently occurred at times of ongoing esophageal contractions. In addition, these instances of incomplete LES relaxation during esophageal contractions were observed during patients’ complaints of dysphagia. Recent refinements in technique have allowed measurement of the transit of radionuclide bolus through the esophagus and, in certain patients, have revealed abnormalities when standard motility testing has been considered to be within normal limits (13). Thus, radionuclide transit studies appear to be useful screening tests for the presence of an esophageal motor disorder. The specific motor dysfunction responsible for delay in transit, however, is not defined in these studies, and instances of dysphagia or chest pain during transit studies have not been reported. Thus, manometry during upright food ingestion may be useful in pinpointing the exact type of abnormality in each patient and, perhaps, in enabling the physician to tailor treatment to the specific abnormality. For example, patients with evidence of predominant LES dysfunction during food ingestion might benefit from pneumatic dilation, whereas those patients with predominant abnormalities of esophageal dysmotility may benefit from pharmacologic agents that decrease amplitude or duration, or both, of contractions. In conclusion, this study demonstrates that esophageal motility during food ingestion differs from that occurring during standard manometry and that testing during food ingestion is more likely to allow observation of motor function while the patient is symptomatic. Since we eat and drink in an upright position, consume food at a variable pace, and swallow boluses of varying size and consistency, perhaps esophageal motility is better assessed under these conditions.
September
1983
MOTlLlTY
References 1. 2.
3. 4. 5.
6.
7.
Hollis JB. Caste11 DO. Effect of dry swallows and wet swalJ Appl lows of different volumes on esophageal peristalsis. Physiol 1975:33:1161-4. Brand DL, Martin D. Pope CE. Esophageal manometrics in patients with angina-like chest pain. Dig Dis Sci 1977; 22:300-4. Kaye MD, Wexler NM. Alteration of esophageal peristalsis by body position. Dig Dis Sci 1981;26:897-901. Bennett JR, Hendrix TR. Diffuse esophageal spasm, a disorder with more than one cause. Gastroenterology 1970;59:273-9. VanTrappen G, Janssens HO, Hellemans J, Coremans C. Achalasia. diffuse esophageal spasm, and related motility disorders. Gastroenterology 1979;76:450-7. Mellow MH. The effect of isosorbide and hydralazine in painful primary esophageal motility disorders. Gastroenterology 1982;83:364-70. Humphries TJ, Caste11 DO. Pressure profile of esophageal
8. 9.
10.
11.
12.
13.
DIJRINI;
FOOD
INGESTION
577
peristalsis in normal humans as measured by direct intraesophageal transducers. Dig Dis Sci 1977:22:641-5. Dent J. A new technique for continuous sphincter pressure measurement. Gastroenterology 1976;71:263-7. Benjamin SB, Gerhardt DC, Caste11 DO. High amplitude. peristaltic esophageal contractions associated with chest pain and/or dysphagia. Gastroenterology 1979:77:478-83. Meyer GW, Gerhardt DC, Caste11 DO Human esophageal response to rapid swallowing: muscle refractor!, period or neural inhibition? Am J Physiol 1981;241:1;129-36. Mellow M. Symptomatic diffuse esophageal spasm; manometric follow-up and response to cholinergic stimulation and cholinesterase inhibition. Gastroenterology 1977:73:2:<7-40. Dodds WJ. Stewart ET, Hogan IVJ. Stef JJ. Arndorfer RC. Effe[.t of esophageal movement on intraluminal esophageal pressure recording. Gastroenterology 1974;67:592-6110. Russell COH, Hill LD, Holmes ER. Hull DA, Cannon R, Pope CE. Radionuclide transit: a sensitive screening test for esophageal dysfunction. Gastroenterology 1981:80:887-92.