progress report gastric emptying tests in man

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Progress reportGastric emptying tests in manThe present understanding of the normal control and regulation of gastricemptying has been established by investigations spanning more than 100yearsl2. Alterations in the normal physiology have been implicated in theaetiology of gastroduodenal disease3'4 whilst a number of studies attributesome of the unpleasant sequelae following gastric surgery to changes inemptying5e6 7. Over this time a variety of methods have been developed tomeasure the rate of gastric emptying. These tests are reviewed, with particularemphasis on their clinical application and on the possible explanations for theconflicting results obtained before and after surgery for peptic ulceration. Themechanisms and regulation of gastric emptying have been the subject ofprevious extensive reviews2'8'9, and a brief outline is given below to provide abackground to the subsequent discussion on gastric emptying tests.

Mechanism of Gastric Emptying

Food, on entering the stomach, is initially accommodated in the fundus andbody. Although peristaltic waves have not been demonstrated in the funduspressure studies show regular slow contractions pushing the contents towardsthe antrum'0. Increased volumes of food do not result in a rapid rise inintragastric pressure due to the ability of the fundus to relax (receptiverelaxation)". The response to food by the body and distal stomach is muchmore vigorous, the characteristic feature being the peristaltic wave whichbegins in the body and sweeps towards the pylorus to terminate in the distalantrum'123. The less vigorous waves fade out distally but the more activeones result in strong segmental contraction of the antrum which in turn iscoordinated with duodenal muscular activity'14"5. This forceful contractionof the distal portion of the stomach has been called 'antral systole'16"17 butfood does not always pass into the duodenum. Frequently the antral contentsare retropulsed which further assists the mixing and emulsifying of the gastriccontents'5. Gastric emptying is related to antral and duodenal activity and anopen pylorus. The rate of emptying of liquids depends on the pressuregradient between the stomach and duodenum'8.Another index of the motor activity of the stomach is the electrical activity

of the stmooth muscle'9. Bursts of action potentials appear on the cycles ofbasic electrical rhythm coincidental with peristaltic waves. The electricalbackground is presumed to regulate contractions but its stimulation by foodis probably multifactorial. In man the basic electrical rhythm can be conduc-ted across the pylorus". Whether or not the electrical activity alone coordin-ates gastroduodenal function is speculative2l but the coordination of antraland duodenal contractions largely controls the rate of gastric emptying.

Regulation of Gastric Emptying

Early reports described some food contents remaining in the stomach longer235

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than others' 22 and fluids emptying differently from solids9 22'23. It is nowknown that the rate of emptying is influenced by the pH24'25'26 and osmo-larity27'28'29 of the food eaten and that this regulation involves receptors inthe duodenum28. Further, the volume of food modifies the rate of emptying30.Hormones also affect gastric emptying. One example is the effect of fatty

acids on the duodenum which may be mediated by 'enterogastrone'8'31. Ofother hormones tested, both gastrin32'33,34'35 and secretin35'36 delay gastricemptying but have opposing effects on antral motor activity32'35'36. Gastricemptying is also dependent on neural factors both from the autonomicnervous system37 and higher centres38.Most studies investigating the control of gastric emptying have utilized

fluid meals because of the ease of control of the physiological stimuli. Theuse of solid foods has not been fully explored, apart from investigationsusing a food and barium mixture25'27. The emptying of solid foods maydepend more on physical characteristics such as specific gravity and viscosityand less on the more established parameters of pH and osmolarity. It wouldalso be attractive to have a common factor for each meal which determinesthe rate of gastric emptying. A step in this direction is the relating of theemptying rates of a balanced liquid diet (in monkeys) to the number ofcalories entering the duodenum39.

Methods of Measurement

GENERALIn view of the above influences any attempt to quantitate the rate of gastricemptying must be strictly controlled. This has proved possible with liquidmeals as shown by some excellent reproducibility figures40'41'42. Unfortunate-ly conflicting results appear when solid meals are used43'44 which may bedue to the lack of a standard 'solid' meal. Each group has its own concept ofa solid meal varying from eggs, cornflakes, and milk45 to eggs, milk, breadand jam46 or to meat and potatoes47 whilst recently impregnated pieces offilter paper have been used.48. There is confusion about what constitutes'solid' food, and the meals being used vary considerably in their physicalcharacteristics such as osmolarity etc. Until there is a better standardizationand definition of a 'solid' meal interpretation of results between groups isbound to be confusing. The possibility of the caloric value of the meal39being the unifying factor influencing gastric emptying has now to be tested.

HISTORICALEarly comments on varying rates of gastric emptying in man were made byBeaumont' observing through a gastric fistula. The use of duodenal fistulae isunphysiological and is only applicable when the normal duodenum mechan-isms are to be excluded.49 The first definitive studies into the emptying capa-city of the stomach were carried out by Von Leube who did single gastricaspirations seven hours after the ingestion of a beef bouillon, potato puree,and bread meal50. Later repeated regular sampling of gastric contents wasintroduced51'52 and then popularized by Rehfuss53 and so was born theconcept of the fractional test meal. Modifications to the method were mademainly by changes in the tube and altering the composition of the food. Thehistory of the development of these procedures and of the test meal isexcellently reviewed by Hollander and Penner54. Such tests are of historical

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Gastric emptying tests in man

interest since they only measure the total emptying time of a component ofthe meal and offer little information about the pattern of emptying.

Modern Methods

The evolution and usefulness of subsequent methods for investigating therate of gastric emptying will be discussed under the following headings:(1) intubation tests, (2) radiological tests, and (3) isotope tests.

INTUBATION TESTSBecause of the limitations of the fractional test meal the serial meal wasdevised23'41. A known volume of liquid containing a non-absorbable markeris given and the entire gastric contents are aspirated after a specific timeinterval. The test is repeated on several days with the meal being removedat different time intervals. By estimating the amount and concentration ofmarker in each sample it is possible to determine the rate of gastric emptying.This method allows for the contribution to volume by gastric secretions.Data points are obtained which outline the pattern of emptying of the liquidmeal. Its disadvantages are that it takes several days to complete and needsrepeated nasogastric intubation so that its clinical application is limited.However, it is a reliable and reproducible test4l and its use (in volunteers)has resulted in considerable information about the regulation of gastricemptying.

In order to overcome the repeated intubations and the time disadvantageof the serial test meal, George" described a method using double samplingof the stomach contents. In this test, after giving the liquid meal, only smallsamples are withdrawn at regular intervals. Limited volumes of marker withknown concentration are introduced into the stomach and the contents thenmixed and resampled. By knowing the concentration and volumes of markerin the original meal and in the added samples it is possible to calculate thevolume of meal left in the stomach. This technique, as well as the serialtest meal, overcomes some of the errors due to dye dilutions which occurredwith the earlier methods described65. Modifications to the test have beenmade by using a radioisotope as a marker because it offers information insimultaneously assessing small bowel transit7. It has an added advantage inbeing easier to estimate than phenol red which was the original marker used.As briefly mentioned by George, additional information can be obtained

by measuring the Cl- and H+ concentration in the samples. Recently Huntemphasized that the double sampling method, as practised, does not indicatethe contribution to volume by gastric secretion. He then indicated a way ofmeasuring the Cl- and so estimate the volume added by gastric secretion56.The double sampling method has proved reliable and popular, particularlyas it has clinical applications. The results40 closely confirm those of Hunt butthe main disadvantage is that it is suitable for liquid meals only.More recently a test has been described which allows for the simultaneous

studies of gastric emptying together with intestinal absorption and digestion42.It involves duodenal intubation and perfusion and, once a steady state isreached, a test meal with marker is put into the stomach. Duodenal aspira-tions are then analysed to calculate the rate at which the marker leaves thestomach. The results from this method42 are comparable to both the doublesampling technique and the serial test meal. However the disadvantages are

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the difficulty in intubating the duodenum, the possible influences of a tubein the antroduodenal area, and the necessity to recover all of the marker fromthe duodenum. It does not have the appeal of the simpler George methodbut its use nrfy be in those areas where associated studies on intestinalabsorption are being carried out.The method described by Bromster et a157 is discussed under this section

since it involves nasogastric intubation, although it also incorporates isotopictechniques. In this test a fluid meal is labelled with an isotope and the rate ofgastric emptying determined by the rate at which activity decreases over thestomach area. A fixed scanner is used and, since this cannot separate outduodenal and small bowel activity, the isotope chosen was 1311-human serumalbumin because it is broken down by the duodenum. Unfortunately the1311 is absorbed and resecreted in the gastric juice. To calibrate for this aninert marker of 1251-polyvinylpyrrolidone is added to the meal and repeatedaspirations are made from the stomach. The 1251 to ls'I ratio is then used todetermine the volume of gastric secretion during the study"8. Whilst thismethod has an advantage over other isotopic techniques in that it indicatesthe contribution to volume by gastric secretion, it is relatively cumbersomewhen compared with the other non-invasive isotope methods discussedbelow.

Efforts to use these established methods of emptying for solid meals wereinitially frustrated because of the size of the lumen of the tube. Recently atechnique has been described59 in which a standard steak meal is given and theintragastric pH maintained at 5'5 by repeated sampling and titrating withNaH CO.. The amount of bicarbonate needed to raise the pH to 5'25 is anestimate of buffer content, and, by estimating this at varying time intervals,an indication of the rate of gastric emptying is obtained. Whilst there areinherent problems with the method in terms of adequate sampling and inproviding an unphysiological environment by maintaining a constant intra-gastric pH, it does offer information about the rate and pattern of gastricsecretion and emptying after a solid meal. Its use, as yet, has not been fullyevaluated.

RAD IOLOGICALThe first studies with x rays and the stomach were by Cannon60 and Kdstle6Ibut their interest was mainly in gastric motility rather than analysis ofemptying times. Later McSwiney and Spurrell described their outlinetechnique with radiopaque markers but its use is limited to experimentalanimals62.The use of fluid barium to measure emptying times has been abandoned

since it is unphysiological and fails to reproduce the effects of solid foods3.Following this a variety of meals incorporating barium sulphate were sug-gested, including food intended to produce a physiological stimulus25'64'656".A criticism of all these is that barium may precipitate out and be irritant tothe gastric mucosa". To overcome these difficulties Horton made use ofenteric-coated barium sulphate granules added to the mealf67. SimilarlyMadsen and Ramussen have described a non-irritant physiological mealsuitable for radiological studies". The disadvantage of all radiologicalmethods is that they only measure the total emptying time, ie, time taken forall the food-barium mixture to leave the stomach, and cannot provideinformation during the two to six hours it may take for the stomach to

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empty. A quantitative attempt was made by Sun"6 by getting independentobservers to estimate when the stomach was 75, 50, and 25% full. Suchmethods have considerable observer error and attempts to derive volumesfrom a two-dimensional film virtually excludes its usefulness.

Meals labelled with barium are still used by some groups69 70,71 but itmust be emphasized that the total emptying time is being measured, and,since the rate slows towards the end of the meal4l, the results are necessarilya crude estimate.

ISOTOPE TESTSThe above tests, apart from that of Fordtran and Walsh59, are concernedentirely with liquid meals. Relatively little information is available aboutthe emptying of solid food although it has been observed that it emptiesat a different rate" 22'23'72 and in a different manner9 to liquids. The oppor-tunity to study gastric emptying of solid meals was provided by the uniqueapproach of Griffiths et al using food labelled with a radioactive substance45.After the meal the rate of emptying is obtained by a scanning detectormeasuring the change in activity over the stomach area. The method requiressome sophistication of equipment but the actual technique is simple and hasthe considerable advantage of being non-invasive. The results have beenshown to fit an exponential pattern of emptying as described with liquidmeals. Other isotope tests have developed but certain aspects in the techniquewarrant discussion.The first is the confusion in the choice of meal which has been emphasized

earlier. Another problem with the food is its fate in vivo. With milk studiesin vitro have shown that in an acid medium the casein precipitates out takingsome of the isotope and leaving the remainder in the supernatant73. Similarly,if potato is used what is the fate of the isotope after the action of salivaryamylase? Is the gastric emptying rate being measured just the averagebetween the liquid and solid components of the meal? In defence of solidmeals it has been shown that liquids alone empty more rapidly than a solidmeal alone72 so that whatever component is being measured solids influencethe rate of emptying. Until further studies have been done looking into theintragastric effects of acid and enzymes on labelled meals it can only beassumed with caution that the rate of emptying of the food and of the marker(isotope) are identical.The choice of isotope varies widely between workers45'46'47'74'75'76. Con-

sideration has to be given to minimizing the radiation dose to the patientand the efficiency of the isotope in producing gamma rays (gamma raysbeing the main form of emission detectable outside the body). Other con-siderations are the availability of the compound and the expense in itspreparation. A final problem with the choice of isotope is its affinity to beabsorbed into the chosen meal. Heading et a176 compared emptying times inthe same patient and with the same meal but with different isotopes. Theyfound that the emptying time was much longer with 51Cr than with 113mIn.Studies in vitro showed that 51Cr was better absorbed onto the cornflakesand the suggestion was that measuring the rate of emptying of the "13mInwas measuring the liquid component of the meal. Whilst this interpretationis arguable the fact remains that careful assessment and studies in vitro arenecessary before firm conclusions can be drawn, particularly when resultsbetween centres differ.

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In the selection of instruments to detect the gamma emission there is yetagain a choice to be made. Fixed detectors, as used by Bromster et al57'6,suffer from not being able to separate out the duodenal and small bowelactivity necessitating the use of 1251-PVP as discussed above. Scinti-scanning75,76877, whether by a single or double-headed device, is able toseparate out extragastric activity satisfactorily. Its main disadvantage is thetime taken to record a single observation (from six to 10 minutes or longer)which is likely to result in inaccuracies, particularly in patients who may haverapid gastric emptying. Because of this time factor only limited numbers ofdata points are available in any one study which is a considerable handicapwhen compared with more suitable detectors.As a result of these deficiencies with scintiscanning Harvey et al (1970)

advocated the use of the Gamma camera72 and this device has since beenused by other groupS43,78 79. It has the distinct advantage of being able torecord counts as frequently as one minute or less and so offer considerableinformation throughout the entire period of study. The accuracy of themethod depends on localizing the area of interest over the stomach, a prob-lem which relates to any scanning technique. Another disadvantage of thegamma camera is that no correction is made for changes in depth of theisotope (and hence absorption) with the size of the patient. As a result ofphantom studies, Harvey et al suggest this may not be a significantly largeerror72. The Gamma camera gives more information than other techniquesand full use can only be made of the data if computer facilities are available.Although the possibilities with the use of such complex equipment areexciting the intricacy and expense must limit its use.

Summary of Available Tests

A wide range of tests is available to measure gastric emptying and theselection of just one of these may seem confusing. However, the choice canbe narrowed depending on the cooperation of the patient, the reason for theinvestigation, and the type of meal chosen. Routine testing of patients shouldbe as comfortable as possible and for this reason the double sampling method(for liquids) or an isotope technique (for solids) would be acceptable. Theuse of a meal with enteric-coated barium granules may be substituted iffacilities for radioactive substances are not available but these can onlymeasure the total emptying time which is of restricted interest. Should thestudies be carried out on volunteers prepared to have repeated nasogastricintubation then the serial test meal has value. Here again, however, mostworkers would prefer the quicker George method and, if necessary calculatethe contribution to volume by gastric secretion as previously discussed.

Expression of Results

The results of gastric emptying studies have been expressed in divers ways.Some methods of measurement, eg, radiological, are only capable of estimat-ing the total emptying time. Other groups have expressed the results as apercentage of the amount emptied from the stomach at varying time intervalsafter eating80. The results of the serial test meal are approximated to anexponential and by plotting the log of the volume of meal against time alinear relationship could be established. The regression equation was then

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calculated and from it the half emptying time obtained, ie, the time taken forthe volume of meal remaining in the stomach to diminish by half (Tj)41. Asa result of these studies most other workers have expressed their findings interms of T' whether the data fitted on an exponential or a linear relation-ship40,42'45,72The use of the half emptying time is convenient and an easily understood

parameter particularly when comparing gastric emptying between differentgroups of patients. However, the whole of the emptying curve is not ade-quately described by a single exponential because of difference at the begin-ning and end of the meaP30. To overcome dissatisfaction with the singleexponential the square root ofthe volume of the meal remaining in the stomachhas been suggested as an alternative81. In order to test the accuracy of anexponential or linear fit to describe the data as well as that of the square rootof the volume remaining a study was carried out on information collectedfrom 29 gastric emptying studies. After applying strict statistical criteria(such as the mean square error) an acceptable fit was obtained in only sevenout of the 29 curves82. This inadequacy is confirmed in a recent report47 whichalso showed that by applying an exponential to the multiple data pointsobtained with theGamma camera considerable information about the patternof emptying is being discarded. These authors have suggested a differentapproach to express the results of gastric emptying curves utilizing theprincipal component method of analysis. This involves examining a wholeset of records to obtain components common to all the gastric emptyingcurves. The proportion to which each component is present in an individualrecord is called the coefficient which can then be used to characterize thatrecord. A high degree of accuracy with this method can be shown by theability of the coefficients to reconstruct patient curves. Results with thismethod are still preliminary and the possible use of these components has tobe defined. They will need to be much more useful than the Ti before suchan attractive, though inaccurate, method will be abandoned.

Peptic Ulceration and Gastric Emptying

At the present time tests for measuring gastric emptying have little applicationin the diagnosis and prognosis of gastrointestinal disease. Their use is essen-tially experimental in the understanding of physiological and clinical problems.One such problem is the effect of peptic ulceration and the various types ofvagotomy on the rate and pattern of gastric emptying. Evidence is conflictingand highlights some of the difficulties in interpretation of results betweencentres as well as exposing deficiencies in the understanding of the patho-physiology of these conditions.

Patients with duodenal ulceration have shown an increase in the overallrate of gastric emptying59,75'83 but others find no change40'84'85. The moststriking difference between these conflicting reports is in methodology. Anincreased rate of emptying is demonstrated in studies using some type of solidmeal whereas no change was seen when a liquid meal was used. In oneexception to this47 the use of a radioactive labelled solid meal failed todemonstrate a difference between duodenal ulcer patients and controls whenmeasuring the half emptying time. However, significant differences werefound in the patterns of emptying as estimated by the principal componentmethod of analysis. Thus it would seem that patients with duodenal ulcera-

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tion have a change in the rate and/or pattern of gastric emptying of solidfoods but not of liquids.

It is difficult to explain an increase in the rate of gastric emptying sinceduodenal ulcer patients have a tendency to produce excess acid which,theoretically, should slow emptying26. Perhaps the reverse is true and in-creased rates of gastric emptying produce hyperacidity28. An alternativeexplanation is that the presence of a duodenal ulcer affects osmo- and pHreceptors in such a way as to interfere with the duodenal inhibition of gastricemptying. However, there is good evidence to refute this suggestion85. Thiswould not explain the difference between the rates of emptying of solids andliquids. There is, presumably, an important stimulus associated with theemptying of solid meals which is affected by the presence of a duodenal ulcer.Possibly the ulcer impairs the control of antro-duodenal contractionsthereby reducing the resistance to outflow from the stomach and so increasethe rate of emptying. Liquids, on the other hand, may require less of apressure gradient before emptying86 and so would be unaffected unless theduodenal pathology was gross. The above speculations emphasize theimportance of understanding the normal physiology in the emptying of solidfood before changes in this pattern due to gastroduodenal disease can beexplained.

In patients with gastric ulceration the changes in gastric emptying alsoseem to depend on the type of meal chosen. The picture is further complicatedby the position of the gastric ulcer and the possible presence of associatedduodenal ulceration. Using liquid meals a delay in gastric emptying wasfound57'87 lending support to the theory of gastric stasis producing gastriculceration8. Even after excluding those patients with pyloro-duodenalpathology, George showed delayed gastric emptying in the presence of asimple lesser curve ulcer. With solid food and a scanning technique nochange was found in the rate of gastric emptying in patients with uncompli-cated lesser curve ulcers but considerable variation appeared in resultswhen the ulcer lay in the antral region75. Considerably more information isneeded before any conclusion can be reached on changes in gastric emptyingin subjects with gastric ulceration.

Gastric Emptying after Truncal Vagotomy and Pyloroplasty

Following vagotomy and pyloroplasty liquid test meals empty faster thanbefore operation5'7'77'i84'88. This could be explained by the pyloroplastyalone. The rate of emptying of liquids is dependent on the pressure gradientbetween the stomach and duodenum2'9 providing that the resistance at thepylorus is contant'8. Since a pyloroplasty reduces the resistance at thepylorus it favours an increase in the rate of gastric emptying. The divisionof antral muscles when making a pyloroplasty may diminish the force ofantral contractions89 and hence reduce gastric pressure. However, this is alesser effect than the reduction of the resistance at the pylorus. Support forthe concept that pyloroplasty accelerates gastric emptying comes from thedemonstration that adding a pyloroplasty to highly selective vagotomyproduces a faster emptying rate than if this type of vagotomy is done withouta drainage procedure5.Vagotomy cannot be excluded as a contributing factor towards rapid

gastric emptying of fluids. Receptive relaxation of the fundus of the stomach

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on ingestion of food" maintains a fairly constant intragastric pressure. Thispower of accomnmodation is lost following vagotomy, resulting in increasedintragastric pressure9O,91 92 which can contribute to the rapid emptying ofliquids after vagotomy and pyloroplasty.With tests using solid foods the results are quite different from the above.

Initial studies demonstrated delayed gastric emptying following vagotomy andpyloroplasty80'93. Further work showed that the delay occurred in the earlypostoperative phase43 with a return to preoperative levels some monthslater43'94. A persistent change at this later time was an initial rapid phase ofemptying94 despite the overall rate being normal. The delay in gastricemptying lasts for at least several weeks and warrants a drainage procedurewith the vagotomy95'96. The impaired emptying is unlikely to be due tointerference with local reflexes coordinating antral distension and contractionto duodenal relaxation since this mechanism is unaffected by vagotomy97,98.The cause is almost certainly due to the effect of the vagotomy since it hasbeen shown that vagotomy impairs antral motility92 99. The suggestion thatthe antrum is concerned primarily with the emptying of solid food'O° empha-sizes the problems associated with denervating that part of the stomach.Why the loss of receptive relaxation and reduced pyloric resistance enhancesemptying of liquids and not of solids is not clear. The delayed gastric empty-ing after surgery becomes confusing when other factors such as gravity7'79and the type of pyloroplasty44 are considered.

Gastric Emptying after Highly Selective Vagotomy

In order to avoid many of the motility disturbances seen with truncal vago-tomy and drainage the operation of highly selective vagotomy (proximalgastric vagotomy) has gained considerable support. This procedure preservesthe vagal innervation to the antrum whilst denervating the body and fundus.Experimental evidence suggests that control over emptying is better afterhighly selective vagotomy92"101"102 and early clinical results are encourag-ing'03" 04. Gastric emptying after highly selective vagotomy is still underassessment. The rate of emptying of fluid meals was still faster postoperativelythan preoperatively36'79. This finding could again be explained by the lossof receptive relaxation by the fundus following denervation92. Other workersusing radiopaque meals have shown little disturbance in the total emptyingtime following highly selective vagotomy7l" 05. Radioactive-labelled solidfood has been used in two subsequent reports. In one the gastric emptyingrate was increased following highly selective vagotomy when the patient wasstanding but not in the supine position79. In the other report gastric emptyingwas slowed soon after surgery but then returned to normal'06. This improve-ment with time was also noted in half the patients who underwent truncalvagotomy and pyloroplasty. Undoubtedly further investigations are neededbefore the theoretical advantages of highly selective vagotomy can beestablished.

Conclusions

Gastric emptying tests in man can be applied to a number of clinical andphysiological problems. Further understanding is needed on the effects ofpeptic ulceration particularly to explain the differences in emptying between

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244 H. J. Sheiner

solid and liquid meals. Increased or decreased rates of emptying after varyingtypes of vagotomy and their relationship to symptoms still remains an openquestion. The influence of gastrointestinal hormones and of various drugson gastric motility also require acceptable tests of gastric emptying. Indeed,there is an obvious need for reproducible techniques. At present the twomethods which seem suitable for clinical use are the double sampling tech-nique using liquid meals and an isotope method for solid food. What isalso needed are methods to standardize the meal, particularly with solids,and an agreed expression of results.

I would like to thank Professor H. L. Duthie, Dr D. C. Barber, and Dr P. J.Howlett (Departments of Surgery and Medical Physics, Sheffield RoyalInfirmary) for providing the original stimulus to write this paper and fortheir subsequent help in its preparation.

H. J. SHEINER

Department of Surgery,Perth Medical Centre,

Shenton Park,Western Australia

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Gastric emptying tests in man 247

1"Pedersen, G., and Amdrup, E. (1970). The gastroointestinal passage of a physiological contrast medium induodenal ulcer patients before and after vagotomy of the parietal cell mass with preserved antral innerva-tion or a selective gastric vagotomy with a Finney pyloroplasty. (Abstr.) In Advance Abstracts 4thWorld Congress of Gastroenterology, edited by P. Riis, P. Anthonisen, and H. Baden, p. 443. DanishGastroenterological Association, Copenhagen.

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