Gut, 1972, 13, 176-181

Gastric emptying of solid meals after truncalvagotomy and pyloroplasty in human subjects

D. J. COWLEY,' P. VERNON, T. JONES, H. I. GLASS, AND A. G. COX2

From the Departments ofSurgery, Medical Physics, and the MRC Cyclotron Unit, Royal Postgraduate MedicalSchool, Hammersmith Hospital, London

SUMMARY Gastric emptying of isotopically labelled solid meals was studied in normal humansubjects and in patients at different intervals after truncal vagotomy and Heineke-Mikulicz pyloro-plasty.One to four weeks after vagotomy and pyloroplasty gastric emptying was delayed grossly in some

patients regardless of the completeness of vagotomy. Patients with gross delay had symptoms ofgastric retention. Eight weeks later emptying had returned towards normal and one or more yearsafter vagotomy and pyloroplasty emptying was within the normal range.

A subthreshold dose of carbachol injected during the course of emptying of a meal in some ofthe postvagotomy patients had no detectable influence on the rate of emptying of the meal.

Symptoms of gastric retention are common inpatients who have recently had a truncal vagotomyand pyloroplasty (Williams and Barnes, 1969).Retention is a major Droblem after vagotomy alone(Dragstedt, Harper, Tovee, and Woodward, 1947)and even with the addition of a drainage procedurethe incidence may be as high as 17% (Barnes andWilliams, 1967). Dragstedt and his coworkersobserved that the symptoms improved with timeand attributed this to the return of tone to thevagally denervated stomach.

Recently, Tinker, Kocak, Jones, Glass, and Cox(1970) found that gastric emptying of solid mealswas delayed in patients tested less than a monthafter truncal vagotomy and pyloroplasty. When thesame patients were given a subthreshold dose ofcarbachol intravenously before they ate the mealgastric emptying was significantly accelerated. Theypostulated that the vagotomized stomach is super-sensitive to cholinergic stimuli and thus obeysCannon's law of denervation (Cannon, 1939). Theysuggested that if this applied only to patients whosevagotomy was complete it might provide the basis ofa test for completeness of vagotomy.We decided to study these phenomena further by

measuring gastric emptying of solid meals, labelledwith a radioisotope, in patients at different time'Present address: Department of Surgery University Hospital of SouthManchester, West Didsbury, Manchester.'Present address: Division of Surgery, Northwick Park Hospital andClinical Research Centre, Harrow, Middx.Received for publication 1 December 1971.

intervals after truncal vagotomy and pyloroplasty.We gave a subthreshold dose of carbachol to someof these patients midway through the recording ofthe emptying of the meal to determine whether ithad any effect on the emptying rate of the stomach.

Materials and Methods

Four groups of human subjects were studied(Table I). There was a control group of volunteers

Group No. in Each

Healthy volunteers 10{ 1-4 weeks' 14

After truncal vagotomy and pyloroplasty 1-4 months2 9> 12 months 7

Table I Patients studied'Mean 16 days'Mean 73 days

with no history of gastrointestinal disease. Threegroups of patients were tested at different timeintervals after truncal vagotomy and a Heineke-Mikulicz pyloroplasty for chronic duodenal ulcer:one to four weeks, one to four months, and morethan one year. Some of the patients tested at one tofour weeks were also studied at the later timeintervals, but no patient was tested more than twiceand the analysis of results was for unpaired groupsof subjects.

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Gastric emptying of solid meals after truncal vagotomy and pyloroplasty in human subjects

MEASUREMENT OF GASTRIC EMPTYINGThe method was similar to that described by Jones,Clark, Kocak, Cox, and Glass (1970) but modifiedto allow continuous recording of gastric radioactivityon magnetic tape. The patient, who had fasted for12 hours, ate a meal of two scrambled eggs, twoslices of buttered bread, a spoonful of jam, and300 ml of milk. One hundred microcuries of Caesium129, adsorbed on to zirconium phosphate, wasstirred into the milk. The radiation dose to the colon,the organ which received the highest dose, was 370millirads but the associated dose to the bone marrowwas only 4 millirads. This can be compared with aradiation dose of 1 062 millirads to the bonemarrow during a barium enema investigation(Report of Committee on Radiological Hazards toPatients, 1966). This radiation dose after Caesium129 is significantly lower than the dose associatedwith other, longer-lived isotopes.

After finishing the meal the patient lay supineunder a gamma camera and was manoeuvred untilthe whole of the stomach, as depicted by the tracer,lay centrally in the field of view displayed on anoscilloscope. As soon as positioning was completedrecording of the radioactivity in the field viewed bythe gamma camera was begun and the informationstored continuously on magnetic tape. The meantime interval from the subject beginning to eat themeal to the start of the recording was 11.2 + 3.9 SDminutes. There were no significant differences be-tween the groups studied. The recording was carriedout for 90 minutes.The tape was later processed by a CDC 6600

computer, using a specially written programwhich gave a static output representing the field

Fig. 1 Static printout of the area scanned by thegamma camera in one normal subject. The stomachshows as an area of relatively high count rate. The gridreferences at margins are not shown.

viewed by the camera (Vernon and Glass, 1971a,1971b). Using the first two and half minutes ofrecorded data the stomach was shown as a welldefined area in the centre of the field and theboundaries of this area were delineated from a grid-reference system marked out on this printed sheet(Fig. 1). The figures delineating the area werepunched onto data cards and fed back into thecomputer with the tape. The computer, thus in-structed to view only the gastric area of the field,

Fig. 2 Dynamic printoutshowing emptying pattern ofstomach in Figure 1. Countrate per minute is usuallyshown at top of chart, timein seconds at bottom.

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D. J. Cowley, P. Vernon, T. Jones, H. L Glass, and A. G. Cox

printed out a dynamic picture showing the per-centage changes in total radioactivity of the areaeach minute for 90 minutes (Fig. 2). Each count wascorrected for background. It was found convenientfor statistical purposes to integrate the one-minutecounts for each five-minute period.

In some of the tests a subthreshold dose ofcarbachol (0-06 micrograms per kg body weight)was injected intravenously 40 minutes after therecording had been started.

Completeness of vagotomy was assessed by theinsulin test (Hollander, 1948).

Analysis of Results

The results were analysed in two different ways:1 The total radioactivity count in each five-minuteperiod was calculated as a percentage of the initialfive-minute count. Gastric emptying, expressed asthis percentage, was calculated at five minutes andthen at 10-minute intervals to 85 minutes after theinitial count. Mean percentage gastric emptying atthese time intervals was calculated for the differentgroups under study.2 In order to study and compare results in in-dividual patients, the half emptying time (TD was

% GASTRICEMPTYING

0

10

20

30

49

50

60

70

80

90

100

1 - 4 WEEKS AFTER TV+ P

CARBACHOL 0. 06, I kg 1. V.

-- CARBACHOL% (5)NOCARBACHOL

(9)

0 5 15 25 35 45 55 65 75 85

calculated. The regression equation for log10 ofcounts for five minutes (y) against time (x) wascalculated. The time in minutes for the stomach toempty by half (TO) was found from the regressionline. To determine whether emptying was mono-exponential during the 90-minute test period, the TIwas calculated for the 0-40- and 45-90-minute periodsseparately. Analysis by a paired t test revealed nosignificant differences between the mean TI 0-40 andTI 45-90 in any of the groups (see Table II). A mono-exponential emptying pattern was therefore assumedboth for normal subjects and for patients aftervagotomy. There were individual exceptions to thisrule but no trend could be discerned.

Results

EFFECT OF CARBACHOLSeven of the eight patients who received carbacholhad had a complete vagotomy. The patterns ofgastric emptying (Fig. 3) and TI values (Table If)were not changed by the administration of a sub-threshold dose of carbachol. Therefore, the resultsof all tests were used for analysis according to theclinical group of the patient and irrespective of theadministration or otherwise of carbachol.

1 - 4 MONTHS AFTER TV + P

CARBACHOL 0. 06pg I kg 1. V.

'-__ CARBACHOL(4)

xNOCARBACHOL

(4)

a . . . a a a a a

05 15 25 35 45 55 65 75 85

TIME IN MINUTESFig. 3 Lack of effect ofsubthreshold carbachol on the gastric emptying patterns ofpatients studied one to fourweeks and one to four months after truncal vagotomy andpyloroplasty. Comparison with patients not given carbachol.

a 1 E E *As

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Gastric emptying of solid meals after truncal vagotomy and pyloroplasty in human subjects

Group n TI (min) ± SEM Exactp

0-40 45-90

Volunteers 10 95 ± 12 119 ± 24 0251-4 weeks 121 552 + 284 368 i 107 0551-4 months 81 205 ± 74 114 i 8 0-26> 12 months 7 133 26 140 30 0-88All postvagotomy 16 157 ± 21 164 ± 25 0-82No carbacholAll with carbachol 11 272 i 74 252 ± 109 0.85

Table II Comparison of half-emptying times in firstand second halves of test'Other patients recorded for 75 minutes

PATTERNS OF GASTRIC EMPTYING AFTERVAGOTOMYIn Fig. 4, the mean percentage gastric emptyingpatterns of the three postvagotomy groups have beenplotted for comparison with the control group. Oneto four weeks after vagotomy gastric emptying wasconsistently and significantly slower than emptyingin the controls. One to four months after vagotomyemptying was still slower than in the controls butthe differences were much less and statisticallysignificant only at the end of the test. One to threeyears after vagotomy the difference between thepostoperative and control groups had disappeared.

HALF-EMPTYING TIMESThe TI of the individual patients is illustrated inFigure 5, which shows also the results in thosepatients who had tests at different stages aftervagotomy. Inspection of this illustration revealsthat the slower mean emptying time one to fourweeks after vagotomy was associated with a verywide scatter of results with gross delay in somepatients and results within the normal range inothers. Gross delay was not related to the complete-ness or otherwise of the vagotomy as judged by theinsulin test. One to four months after vagotomy sub-stantial recovery had occurred in patients whoexhibited gross delay one to four weeks aftervagotomy. One year or more after vagotomy, onlyone patient had a TI outside the normal range (allpatients in this group had a complete vagotomy).Symptoms of gastric retention in the 14 patients

tested one to four weeks after vagotomy correlatedwell with the results of the gastric emptying tests.Five patients had gross delay with a TI greater than400 minutes; all complained of troublesome fullnessafter meals, two had episodes of vomiting, and onehad frequent hiccups. One of three patients with aTI of 200 to 250 minutes had fullness after meals,and of six patients with a TI of 85 to 175 minutesonly one had slight fullness after meals.

1-4 weeks aftervagotomy (14)

1-4 months aftervagotomy (9)

uI0 5 25 45 65 85TIME IN MINUTES

1-3 years aftervagotomy (7)

L . I I

0 5 25 45 65 85

* CONTROLS (10)

MEAN ± S.E.M.O- O0 A/ILK VAMUIUMY 1 * K0. 01

Fig. 4 Comparisons ofgastric emptying pattern at different time intervals after vagotomy with normal gastricemptying pattern.

O r

c-1-

W 50

c^C-)

100 - A I I I A

0 5 25 45 65 85

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D. J. Cowley, P. Vernon, T. Jones, H. L Glass, and A. G. Cox

T i (MINUTES )

1600

1200

C - Complete VagetomyI - Incomplete Vagotmy

Fig. 5 Half-emptying time (T4) ofindividual subjects in the differentgroups. Six patients had a second testafter an interval of time.

0

0~

HEALTHY 1-4 1-4 > 12CONTROLS WEKS MONTHS MONTHS

a E

AFTER TV + P

Discussion

A subthreshold dose of carbachol injected half-waythrough the period of measurement had no detect-able influence on the rate of emptying of the meal inpatients after vagotomy. Therefore this method,based on the concept of supersensitivity, could notbe used to distinguish patients with complete andincomplete vagotomy. This finding does not neces-

sarily negate the suggestion of Tinker et al (1970)that this approach might provide an alternative tothe insulin test, because we studied the patients in adifferent way. Tinker and his colleagues did twoseparate tests, one with and the other withoutcarbachol, whereas we did a single test in the hopethat we could spare the patient a second visit to thehospital.An alternative explanation for the difference

between our findings and those of Tinker et al (1970)might be that their second test was sometimes doneafter an interval ofup to three weeks. We have foundthat spontaneous recovery in the rate of emptyingmay occur during this period.A temporary delay in the gastric emptying of solid

meals was observed in patients with duodenal ulcerafter truncal vagotomy and pyloroplasty. The delaywas followed by recovery to normal within threemonths. Tinker et al (1970) and Griffith, Owen, and

Shields (1966a) also found this delay in gastricemptying shortly after truncal vagotomy andpyloroplasty but they did not investigate the pos-sibility that recovery takes place. In the presentstudy, the group studied one to four weeks aftervagotomy showed a statistically significant delay inemptying compared with the healthy controls, butthere were great differences between individuals inthe group. Some exhibited gross delay in emptyingwhile the emptying times of others were within thenormal range. Gross delay was associated with thesymptoms of gastric retention. Delay occurredregardless of whether the vagotomy was completeor incomplete; some patients with incompletelyvagotomized stomachs emptied very slowly andothers with a complete vagotomy emptied rapidly.Thus, in order to explain this phenomenon of a tem-porary delay of emptying in certain patients a factorother than vagal denervation of the stomach mustbe postulated. This factor might be a paradoxicalnarrowing at the pyloroplasty. All of the presentgroup had a Heineke-Mikulicz pyloroplasty. Thiswas closed with two layers of sutures in 10 patientsand with one layer in four patients. The length ofthe pyloroplasty incision was not often measured atoperation and it is therefore impossible to determineretrospectively the reason for a temporary post-operative narrowing. Griffith, Owen, Kirkman, and

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Gastric emptying of solid meals after truncal vagotomy and pyloroplasty in human subjects 181

Shields (1966b) showed some evidence that emptyingis more rapid after a vagotomy and Finney pyloro-plasty than after a vagotomy and Heineke-Mikuliczpyloroplasty. A prospective controlled trial of thetwo types of pyloroplasty could resolve this point.

Buckler (1967) studied the emptying of semi-solidmeals in patients who had undergone various typesof gastric surgery. He found that a simple pyloro-plasty produced a delay in emptying compared withcontrols. When it was combined with truncal vago-tomy still greater delay ensued. McKelvey, Connell,and Kennedy (1970) studied the emptying of liquidmeals after vagotomy and pyloroplasty and foundthat emptying varied according to the posture of thepatient; lying on the left side was associated withvery slow emptying, lying on the right side with veryrapid emptying. They concluded that the vagoto-mized stomach behaves as an 'incontinent organ'.

In the present study we have attempted to keepall the factors involved in measuring gastric empty-ing constant for every patient, thus posture is un-likely to account for differences between the groups.We have used a solid meal and whilst it is possiblethat this empties differently from liquids we havenotattemptedto study the effect of different postures.

The authors wish to thank Miss Diane Whait, MrsPenny Shilling, and Miss Anne Morash for technicalassistance and Miss Stephanie Nichols for secretarialhelp.

References

Barnes, A. D., and Williams, J. A. (1967). Stomach drainage aftervagotomy and pyloroplasty. Amer. J. Surg., 113, 494-497.

Buckler, K. G. (1967). Effects ofgastric surgery upon gastric emptyingin cases of peptic ulceration. Gut, 8, 137-147.

Cannon, W. B. (1939). A law of denervation. Amer. J. med. Sci., 198,737-750.

Dragstedt, L. R., Harper, P. V., Jr., Tovee, E. B., and Woodward, E.R. (1947). Section of the vagus nerves to the stomach in thetreatment of peptic ulcer: complications and end results afterfour years. Ann. Surg., 126, 687-699.

Griffith, G. H., Owen, G. M., and Shields, R. (1966a). The rate ofgastric emptying in gastroduodenal disease. (Abstr.) Brit. J.Surg., 53, 995.

Griffith, G. H., Owen, G. M., Kirkman, S., and Shields, R. (1966b).Measurements of rate of gastric emptying using chromium 51.Lancet, 1, 1244 1245.

Hollander, F. (1948). Laboratory procedures in the study ofvagotomy(with particular reference to the insulin test). Gastroenterology,11, 419-425.

Jones, T., Clark, J. C., Kocak, N., Cox, A. G., and Glass, H. I.(1970). Measurement of gastric emptying using the scintillationcamera and 12Ca. Brit. J. Radiol., 43, 537-541.

McKelvey, S. T. D., Connell, A. M., and Kennedy, T. L. (1969). Gastricemptying and transit time as factors in postvagotomy diarrhoea.Gut, 10, 1047.

Ministry of Health and Scottish Home and Health Department(1966). (Final Report of Committee) Radiological Hazards toPatients. H.M.S.O., London.

Tinker, J., Kocak, N., Jones, T., Glass, H. I., and Cox, A. G. (1970).Supersensitivity and gastric emptying after vagotomy. Gut, 11,502-505.

Vernon, P., and Glass, H. I. (1971a). An off-line digital system for usewith a gamma camera. Phys. med. Biol., 16, 405-415.

Vernon, P., and Glass, H. I. (1971b). Processing gamma camera dataobtained from an off-line system. In Dynamic Studies withRadioisotopes in Medicine, pp. 133-143. International AtomicEnergy Agency, Vienna.

Williams, J. A., and Barnes, A. D. (1969). Post-operative gastricretention. In After Vagotomy, edited by J. A. Williams andA. G. Cox, ch. 14. Butterworths, London.

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