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Progress report Gastric emptying tests in man The present understanding of the normal control and regulation of gastric emptying has been established by investigations spanning more than 100 yearsl2. Alterations in the normal physiology have been implicated in the aetiology of gastroduodenal disease3'4 whilst a number of studies attribute some of the unpleasant sequelae following gastric surgery to changes in emptying5e6 7. Over this time a variety of methods have been developed to measure the rate of gastric emptying. These tests are reviewed, with particular emphasis on their clinical application and on the possible explanations for the conflicting results obtained before and after surgery for peptic ulceration. The mechanisms and regulation of gastric emptying have been the subject of previous extensive reviews2'8'9, and a brief outline is given below to provide a background to the subsequent discussion on gastric emptying tests. Mechanism of Gastric Emptying

Food, on entering the stomach, is initially accommodated in the fundus and body. Although peristaltic waves have not been demonstrated in the fundus pressure studies show regular slow contractions pushing the contents towards the antrum'0. Increased volumes of food do not result in a rapid rise in intragastric pressure due to the ability of the fundus to relax (receptive relaxation)". The response to food by the body and distal stomach is much more vigorous, the characteristic feature being the peristaltic wave which begins in the body and sweeps towards the pylorus to terminate in the distal antrum'123. The less vigorous waves fade out distally but the more active ones result in strong segmental contraction of the antrum which in turn is coordinated with duodenal muscular activity'14"5. This forceful contraction of the distal portion of the stomach has been called 'antral systole'16"17 but food does not always pass into the duodenum. Frequently the antral contents are retropulsed which further assists the mixing and emulsifying of the gastric contents'5. Gastric emptying is related to antral and duodenal activity and an open pylorus. The rate of emptying of liquids depends on the pressure gradient 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 of basic electrical rhythm coincidental with peristaltic waves. The electrical background is presumed to regulate contractions but its stimulation by food is probably multifactorial. In man the basic electrical rhythm can be conducted across the pylorus". Whether or not the electrical activity alone coordinates gastroduodenal function is speculative2l but the coordination of antral and duodenal contractions largely controls the rate of gastric emptying.

Regulation of Gastric Emptying Early reports described some food contents remaining in the stomach longer 235

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than others' 22 and fluids emptying differently from solids9 22'23. It is now known that the rate of emptying is influenced by the pH24'25'26 and osmolarity27'28'29 of the food eaten and that this regulation involves receptors in the 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. Of other hormones tested, both gastrin32'33,34'35 and secretin35'36 delay gastric emptying but have opposing effects on antral motor activity32'35'36. Gastric emptying is also dependent on neural factors both from the autonomic nervous 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. The use of solid foods has not been fully explored, apart from investigations using a food and barium mixture25'27. The emptying of solid foods may depend more on physical characteristics such as specific gravity and viscosity and less on the more established parameters of pH and osmolarity. It would also be attractive to have a common factor for each meal which determines the rate of gastric emptying. A step in this direction is the relating of the emptying rates of a balanced liquid diet (in monkeys) to the number of calories entering the duodenum39. Methods of Measurement GENERAL

In view of the above influences any attempt to quantitate the rate of gastric emptying must be strictly controlled. This has proved possible with liquid meals as shown by some excellent reproducibility figures40'41'42. Unfortunately conflicting results appear when solid meals are used43'44 which may be due to the lack of a standard 'solid' meal. Each group has its own concept of a solid meal varying from eggs, cornflakes, and milk45 to eggs, milk, bread and jam46 or to meat and potatoes47 whilst recently impregnated pieces of filter paper have been used.48. There is confusion about what constitutes 'solid' food, and the meals being used vary considerably in their physical characteristics such as osmolarity etc. Until there is a better standardization and definition of a 'solid' meal interpretation of results between groups is bound to be confusing. The possibility of the caloric value of the meal39 being the unifying factor influencing gastric emptying has now to be tested. HISTORICAL

Early comments on varying rates of gastric emptying in man were made by Beaumont' observing through a gastric fistula. The use of duodenal fistulae is unphysiological and is only applicable when the normal duodenum mechanisms are to be excluded.49 The first definitive studies into the emptying capacity of the stomach were carried out by Von Leube who did single gastric aspirations seven hours after the ingestion of a beef bouillon, potato puree, and bread meal50. Later repeated regular sampling of gastric contents was introduced51'52 and then popularized by Rehfuss53 and so was born the concept of the fractional test meal. Modifications to the method were made mainly by changes in the tube and altering the composition of the food. The history of the development of these procedures and of the test meal is excellently reviewed by Hollander and Penner54. Such tests are of historical

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

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

Because of the limitations of the fractional test meal the serial meal was devised23'41. A known volume of liquid containing a non-absorbable marker is given and the entire gastric contents are aspirated after a specific time interval. The test is repeated on several days with the meal being removed at different time intervals. By estimating the amount and concentration of marker 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 liquid meal. Its disadvantages are that it takes several days to complete and needs repeated 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 gastric emptying. In order to overcome the repeated intubations and the time disadvantage of the serial test meal, George" described a method using double sampling of the stomach contents. In this test, after giving the liquid meal, only small samples are withdrawn at regular intervals. Limited volumes of marker with known concentration are introduced into the stomach and the contents then mixed and resampled. By knowing the concentration and volumes of marker in the original meal and in the added samples it is possible to calculate the volume of meal left in the stomach. This technique, as well as the serial test meal, overcomes some of the errors due to dye dilutions which occurred with the earlier methods described65. Modifications to the test have been made by using a radioisotope as a marker because it offers information in simultaneously assessing small bowel transit7. It has an added advantage in being 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 Hunt emphasized that the double sampling method, as practised, does not indicate the contribution to volume by gastric secretion. He then indicated a way of measuring the Cl- and so estimate the volume added by gastric secretion56. The double sampling method has proved reliable and popular, particularly as it has clinical applications. The results40 closely confirm those of Hunt but the 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 is reached, a test meal with marker is put into the stomach. Duodenal aspirations are then analysed to calculate the rate at which the marker leaves the stomach. The results from this method42 are comparable to both the double sampling 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 tube in the antroduodenal area, and the necessity to recover all of the marker from the duodenum. It does not have the appeal of the simpler George method but its use nrfy be in those areas where associated studies on intestinal absorption 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 isotopic techniques. In this test a fluid meal is labelled with an isotope and the rate of gastric emptying determined by the rate at which activity decreases over the stomach area. A fixed scanner is used and, since this cannot separate out duodenal and small bowel activity, the isotope chosen was 1311-human serum albumin because it is broken down by the duodenum. Unfortunately the 1311 is absorbed and resecreted in the gastric juice. To calibrate for this an inert marker of 1251-polyvinylpyrrolidone is added to the meal and repeated aspirations are made from the stomach. The 1251 to ls'I ratio is then used to determine the volume of gastric secretion during the study"8. Whilst this method has an advantage over other isotopic techniques in that it indicates the contribution to volume by gastric secretion, it is relatively cumbersome when compared with the other non-invasive isotope methods discussed below. Efforts to use these established methods of emptying for solid meals were initially frustrated because of the size of the lumen of the tube. Recently a technique has been described59 in which a standard steak meal is given and the intragastric pH maintained at 5'5 by repeated sampling and titrating with NaH CO.. The amount of bicarbonate needed to raise the pH to 5'25 is an estimate of buffer content, and, by estimating this at varying time intervals, an indication of the rate of gastric emptying is obtained. Whilst there are inherent problems with the method in terms of adequate sampling and in providing an unphysiological environment by maintaining a constant intragastric pH, it does offer information about the rate and pattern of gastric secretion and emptying after a solid meal. Its use, as yet, has not been fully evaluated. RAD IOLOGICAL

The first studies with x rays and the stomach were by Cannon60 and Kdstle6I but their interest was mainly in gastric motility rather than analysis of emptying times. Later McSwiney and Spurrell described their outline technique with radiopaque markers but its use is limited to experimental animals62. 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 suggested, including food intended to produce a physiological stimulus25'64'656". A criticism of all these is that barium may precipitate out and be irritant to the gastric mucosa". To overcome these difficulties Horton made use of enteric-coated barium sulphate granules added to the mealf67. Similarly Madsen and Ramussen have described a non-irritant physiological meal suitable for radiological studies". The disadvantage of all radiological methods is that they only measure the total emptying time, ie, time taken for all the food-barium mixture to leave the stomach, and cannot provide information 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 independent observers to estimate when the stomach was 75, 50, and 25% full. Such methods have considerable observer error and attempts to derive volumes from a two-dimensional film virtually excludes its usefulness. Meals labelled with barium are still used by some groups69 70,71 but it must be emphasized that the total emptying time is being measured, and, since the rate slows towards the end of the meal4l, the results are necessarily a crude estimate. ISOTOPE TESTS

The above tests, apart from that of Fordtran and Walsh59, are concerned entirely with liquid meals. Relatively little information is available about the emptying of solid food although it has been observed that it empties at a different rate" 22'23'72 and in a different manner9 to liquids. The opportunity to study gastric emptying of solid meals was provided by the unique approach of Griffiths et al using food labelled with a radioactive substance45. After the meal the rate of emptying is obtained by a scanning detector measuring the change in activity over the stomach area. The method requires some sophistication of equipment but the actual technique is simple and has the considerable advantage of being non-invasive. The results have been shown to fit an exponential pattern of emptying as described with liquid meals. Other isotope tests have developed but certain aspects in the technique warrant 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 studies in vitro have shown that in an acid medium the casein precipitates out taking some 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 salivary amylase? Is the gastric emptying rate being measured just the average between the liquid and solid components of the meal? In defence of solid meals it has been shown that liquids alone empty more rapidly than a solid meal alone72 so that whatever component is being measured solids influence the rate of emptying. Until further studies have been done looking into the intragastric effects of acid and enzymes on labelled meals it can only be assumed 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. Consideration has to be given to minimizing the radiation dose to the patient and the efficiency of the isotope in producing gamma rays (gamma rays being the main form of emission detectable outside the body). Other considerations are the availability of the compound and the expense in its preparation. A final problem with the choice of isotope is its affinity to be absorbed into the chosen meal. Heading et a176 compared emptying times in the same patient and with the same meal but with different isotopes. They found that the emptying time was much longer with 51Cr than with 113mIn. Studies in vitro showed that 51Cr was better absorbed onto the cornflakes and the suggestion was that measuring the rate of emptying of the "13mIn was measuring the liquid component of the meal. Whilst this interpretation is arguable the fact remains that careful assessment and studies in vitro are necessary before firm conclusions can be drawn, particularly when results between centres differ.

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In the selection of instruments to detect the gamma emission there is yet again 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 bowel activity necessitating the use of 1251-PVP as discussed above. Scintiscanning75,76877, whether by a single or double-headed device, is able to separate out extragastric activity satisfactorily. Its main disadvantage is the time 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 have rapid gastric emptying. Because of this time factor only limited numbers of data points are available in any one study which is a considerable handicap when 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 been used by other groupS43,78 79. It has the distinct advantage of being able to record counts as frequently as one minute or less and so offer considerable information throughout the entire period of study. The accuracy of the method depends on localizing the area of interest over the stomach, a problem which relates to any scanning technique. Another disadvantage of the gamma camera is that no correction is made for changes in depth of the isotope (and hence absorption) with the size of the patient. As a result of phantom studies, Harvey et al suggest this may not be a significantly large error72. The Gamma camera gives more information than other techniques and full use can only be made of the data if computer facilities are available. Although the possibilities with the use of such complex equipment are exciting the intricacy and expense must limit its use. Summary of Available Tests A wide range of tests is available to measure gastric emptying and the selection of just one of these may seem confusing. However, the choice can be narrowed depending on the cooperation of the patient, the reason for the investigation, and the type of meal chosen. Routine testing of patients should be as comfortable as possible and for this reason the double sampling method (for liquids) or an isotope technique (for solids) would be acceptable. The use of a meal with enteric-coated barium granules may be substituted if facilities for radioactive substances are not available but these can only measure the total emptying time which is of restricted interest. Should the studies be carried out on volunteers prepared to have repeated nasogastric intubation then the serial test meal has value. Here again, however, most workers would prefer the quicker George method and, if necessary calculate the 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 estimating the total emptying time. Other groups have expressed the results as a percentage of the amount emptied from the stomach at varying time intervals after eating80. The results of the serial test meal are approximated to an exponential and by plotting the log of the volume of meal against time a linear 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 for the volume of meal remaining in the stomach to diminish by half (Tj)41. As a result of these studies most other workers have expressed their findings in terms of T' whether the data fitted on an exponential or a linear relationship40,42'45,72 The use of the half emptying time is convenient and an easily understood parameter particularly when comparing gastric emptying between different groups of patients. However, the whole of the emptying curve is not adequately described by a single exponential because of difference at the beginning and end of the meaP30. To overcome dissatisfaction with the single exponential the square root of the volume of the meal remaining in the stomach has been suggested as an alternative81. In order to test the accuracy of an exponential or linear fit to describe the data as well as that of the square root of the volume remaining a study was carried out on information collected from 29 gastric emptying studies. After applying strict statistical criteria (such as the mean square error) an acceptable fit was obtained in only seven out of the 29 curves82. This inadequacy is confirmed in a recent report47 which also showed that by applying an exponential to the multiple data points obtained with the Gamma camera considerable information about the pattern of emptying is being discarded. These authors have suggested a different approach to express the results of gastric emptying curves utilizing the principal component method of analysis. This involves examining a whole set of records to obtain components common to all the gastric emptying curves. The proportion to which each component is present in an individual record is called the coefficient which can then be used to characterize that record. A high degree of accuracy with this method can be shown by the ability of the coefficients to reconstruct patient curves. Results with this method are still preliminary and the possible use of these components has to be defined. They will need to be much more useful than the Ti before such an attractive, though inaccurate, method will be abandoned.

Peptic Ulceration and Gastric Emptying At the present time tests for measuring gastric emptying have little application in the diagnosis and prognosis of gastrointestinal disease. Their use is essentially experimental in the understanding of physiological and clinical problems. One such problem is the effect of peptic ulceration and the various types of vagotomy on the rate and pattern of gastric emptying. Evidence is conflicting and highlights some of the difficulties in interpretation of results between centres as well as exposing deficiencies in the understanding of the pathophysiology of these conditions. Patients with duodenal ulceration have shown an increase in the overall rate of gastric emptying59,75'83 but others find no change40'84'85. The most striking difference between these conflicting reports is in methodology. An increased rate of emptying is demonstrated in studies using some type of solid meal whereas no change was seen when a liquid meal was used. In one exception to this47 the use of a radioactive labelled solid meal failed to demonstrate a difference between duodenal ulcer patients and controls when measuring the half emptying time. However, significant differences were found in the patterns of emptying as estimated by the principal component method 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 solid foods but not of liquids. It is difficult to explain an increase in the rate of gastric emptying since duodenal ulcer patients have a tendency to produce excess acid which, theoretically, should slow emptying26. Perhaps the reverse is true and increased rates of gastric emptying produce hyperacidity28. An alternative explanation is that the presence of a duodenal ulcer affects osmo- and pH receptors in such a way as to interfere with the duodenal inhibition of gastric emptying. However, there is good evidence to refute this suggestion85. This would not explain the difference between the rates of emptying of solids and liquids. There is, presumably, an important stimulus associated with the emptying of solid meals which is affected by the presence of a duodenal ulcer. Possibly the ulcer impairs the control of antro-duodenal contractions thereby reducing the resistance to outflow from the stomach and so increase the rate of emptying. Liquids, on the other hand, may require less of a pressure gradient before emptying86 and so would be unaffected unless the duodenal pathology was gross. The above speculations emphasize the importance of understanding the normal physiology in the emptying of solid food before changes in this pattern due to gastroduodenal disease can be

explained. In patients with gastric ulceration the changes in gastric emptying also seem to depend on the type of meal chosen. The picture is further complicated by the position of the gastric ulcer and the possible presence of associated duodenal ulceration. Using liquid meals a delay in gastric emptying was found57'87 lending support to the theory of gastric stasis producing gastric ulceration8. Even after excluding those patients with pyloro-duodenal pathology, George showed delayed gastric emptying in the presence of a simple lesser curve ulcer. With solid food and a scanning technique no change was found in the rate of gastric emptying in patients with uncomplicated lesser curve ulcers but considerable variation appeared in results when the ulcer lay in the antral region75. Considerably more information is needed before any conclusion can be reached on changes in gastric emptying in subjects with gastric ulceration. Gastric Emptying after Truncal Vagotomy and Pyloroplasty

Following vagotomy and pyloroplasty liquid test meals empty faster than before operation5'7'77'i84'88. This could be explained by the pyloroplasty alone. The rate of emptying of liquids is dependent on the pressure gradient between the stomach and duodenum2'9 providing that the resistance at the pylorus is contant'8. Since a pyloroplasty reduces the resistance at the pylorus it favours an increase in the rate of gastric emptying. The division of antral muscles when making a pyloroplasty may diminish the force of antral contractions89 and hence reduce gastric pressure. However, this is a lesser effect than the reduction of the resistance at the pylorus. Support for the concept that pyloroplasty accelerates gastric emptying comes from the demonstration that adding a pyloroplasty to highly selective vagotomy produces a faster emptying rate than if this type of vagotomy is done without a 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. This power of accomnmodation is lost following vagotomy, resulting in increased intragastric pressure9O,91 92 which can contribute to the rapid emptying of liquids 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 and pyloroplasty80'93. Further work showed that the delay occurred in the early postoperative phase43 with a return to preoperative levels some months later43'94. A persistent change at this later time was an initial rapid phase of emptying94 despite the overall rate being normal. The delay in gastric emptying lasts for at least several weeks and warrants a drainage procedure with the vagotomy95'96. The impaired emptying is unlikely to be due to interference with local reflexes coordinating antral distension and contraction to duodenal relaxation since this mechanism is unaffected by vagotomy97,98. The cause is almost certainly due to the effect of the vagotomy since it has been shown that vagotomy impairs antral motility92 99. The suggestion that the antrum is concerned primarily with the emptying of solid food'O° emphasizes the problems associated with denervating that part of the stomach. Why the loss of receptive relaxation and reduced pyloric resistance enhances emptying of liquids and not of solids is not clear. The delayed gastric emptying after surgery becomes confusing when other factors such as gravity7'79 and the type of pyloroplasty44 are considered.

Gastric Emptying after Highly Selective Vagotomy In order to avoid many of the motility disturbances seen with truncal vagotomy and drainage the operation of highly selective vagotomy (proximal gastric vagotomy) has gained considerable support. This procedure preserves the vagal innervation to the antrum whilst denervating the body and fundus. Experimental evidence suggests that control over emptying is better after highly selective vagotomy92"101"102 and early clinical results are encouraging'03" 04. Gastric emptying after highly selective vagotomy is still under assessment. The rate of emptying of fluid meals was still faster postoperatively than preoperatively36'79. This finding could again be explained by the loss of receptive relaxation by the fundus following denervation92. Other workers using radiopaque meals have shown little disturbance in the total emptying time following highly selective vagotomy7l" 05. Radioactive-labelled solid food has been used in two subsequent reports. In one the gastric emptying rate was increased following highly selective vagotomy when the patient was standing but not in the supine position79. In the other report gastric emptying was slowed soon after surgery but then returned to normal'06. This improvement with time was also noted in half the patients who underwent truncal vagotomy and pyloroplasty. Undoubtedly further investigations are needed before the theoretical advantages of highly selective vagotomy can be established.

Conclusions

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

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solid and liquid meals. Increased or decreased rates of emptying after varying types of vagotomy and their relationship to symptoms still remains an open question. The influence of gastrointestinal hormones and of various drugs on gastric motility also require acceptable tests of gastric emptying. Indeed, there is an obvious need for reproducible techniques. At present the two methods which seem suitable for clinical use are the double sampling technique using liquid meals and an isotope method for solid food. What is also 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 Royal Infirmary) for providing the original stimulus to write this paper and for their subsequent help in its preparation. H. J. SHEINER

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Gastric emptying tests in man.

Gut, 1975, 16, 235-247 Progress report Gastric emptying tests in man The present understanding of the normal control and regulation of gastric emptyi...
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