GASTRIC EMPTYING IN THE NORMAL DOG A Contrast Radiographic Technique TAKAYOSHI MIYABAYASHI, DVM, MS*, JOEP. MORGAN,DVM, VET MED DR?
A total of 22 radiographic studies was made to determine comparative gastric emptying times of two different solid test meals (intact kibble food and ground kibble food mixed with barium sulfate suspension) in four mature (15-26 months) normal Beagle dogs under controlled conditions. Complete gastric emptying times of the intact kibble and ground kibble meals of a given dose (8 g/kg of dog food plus 5-7 mlikg of the contrast agent) ranged from five to ten hours (7.6 f 1.98 hours with intact kibble meal and 7.0 & 1.86 hours with ground kibble meal). Feeding a halfdose of ground kibble meal (4 g/kg of dog food plus 3.5 mYkg of the contrast agent) resulted in complete gastric emptying times of four to six hours (4.7 f 0.67 hours). Individual dogs had repeatable gastric emptying times although the times varied among different dogs. Veterinary Radiology, Vol. 25, No. 4, 1984; p p 187-191.
Key words: dog, gastric emptying, UGI study.
I
the rate of gastric emptying is directly influenced by pressure differences and degree of resistance at the gastroduodenal junction.’ In terms of motility or contraction, the canine stomach has two distinct regions: proximal (the fundus and proximal body) and distal (the distal body and antrum). The former initiates slow, sustained contractions that are generalized, while the latter has rhythmic contraction waves (5.5 cycles/min).’ This difference in the pattern of contractions influences gastric emptying of liquids and solid foods. Liquids can be propelled into the duodenum by contractions of the proximal stomach alone. Solid foods, however, need to be reduced in size to pass through the pylorus. Reduction of food particle size results from: (1) mechanical grinding actions by the distal stomach, (2) some degree of digestion by enzymes, e.g., pepsin, and ( 3 ) infiltration of gastric juice and/or ingested fluids. Contraction waves of the distal stomach play a major role in this “churning” process.’ Some previously performed physiologic assessments of gastric emptying are not directly applicable to that seen in the clinical situation. Some used invaN DOGS,
sive methods as in electric activity transducer s t ~ d i e s ,and ~ , ~fistula formation ~ t u d i e s . ~ . ~ Others required specialized equipment, i.e., gamma cameras and radionuclides.lOvllDose of test meals used in some studies was not standardized. l 2 7 I 3 The purposes of this study were (1) to describe a technique for contrast radiographic assessment of gastric emptying of digestible solid food and (2) to define the complete gastric emptying time of healthy, young adult dogs. Materials and Methods Experimental Animals
Four male, mature Beagle dogs (18-26 months) were selected. All dogs were housed in a restricted area at the Laboratory for Energy-Related Health Research, University of California, Davis and had no contact with outside animals. They had routine vaccinations and normal physical examinations. All dogs had a normal liquid barium sulfate upper gastrointestinal (UGI) examination one week prior to this experiment. Test Meals
Supported in part by a grant from the United States Department of Energy. * This paper is part of a thesis written in partial fulfillment of the requirements for the Master of Science degree, University of California, Davis. t From the Department of Radiological Sciences, School of Veterinary Medicine, University of California, Davis, California 95616 and the Laboratory for Energy-Related Health Research (LEHR), University of California, Davis, California 95616. Dr. Miyabayashi was a graduate student, and Dr. Morgan is a professor in the Department of Radiological Sciences, Address reprint requests to Dr. Takayoshi Miyabayashi, Laboratory for Energy-Related Health Research, University of California, Davis, California 95616.
Test meals were composed of soiid food phase (dry kibble dog food)$ and liquid contrast medium phase (60% wt/vol barium sulfate suspension).II Kibble was used because of its homogeneous nutrient distribution and uniform caloric density as compared with canned $ Purina Field ’n Farm Dog Food, Ralston Purina Company, St. Louis, Missouri 63155. 11 Novapaque, 60% wt/vol barium sulfate suspension, Picker Corporation, Cleveland, Ohio 44101.
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dog food. Furthermore, the caloric density of many brands of dry kibble food is similar.I4 Three test meals were prepared: (1) intact kibble (1K)-8 g k g of intact kibble mixed manually with 5 mVkg of contrast medium, (2) ground kibble (GK)-8 g/kg of ground kibble prepared by grinding the same kibble in an electric blender to a particle size of less than 1 mm diameter and then manually mixing 7 ml/ kg of contrast medium, and (3) half-dose ground kibble (HGK)-4 g/kg of the ground kibble manually mixed with 3.5 ml/kg of contrast medium. The increased amount of contrast medium in GK was required to obtain maximum particle coating. Experimental Methods
All dogs were preconditioned by having one contrast radiographic study with IK and one with GK. Two IK and two GK studies were performed during the next three weeks. During this period, each dog had another upper gastrointestinal examination with 10 ml/ kg of liquid contrast medium to confirm the continued normal appearance of the gastrointestinal tract. During the fourth week, two radiographic studies with HGK were performed on three of the dogs. At least three days elapsed between successive radiographic examinations. The radiographic protocol for this experiment was as follows: Food was withheld 24 hours prior to the examination. Water intake was not restricted. A survey ventrodorsal abdominal radiograph was obtained. If the stomach was empty, the test meal was fed. Postprandial sequential ventrodorsal abdominal radiographs were obtained at 15 minutes and one, three, six, and nine hours. Additional hourly radiographs were made when gastric emptying was thought to be nearly complete. Complete gastric emptying time was defined as no test meal being visible within the stomach. Examinations were ended when complete gastric emptying was noted. Time of onset of gastric emptying of fluid and solid phases and time of complete gastric emptying were recorded. Radiographic patterns of test meals in the stomach were also evaluated.
1984 Results
The onset of the gastric emptying of IK, GK, and HGK is recorded (Table 1). With IK, a part of the contrast medium (liquid phase) entered the small intestine within 15 minutes postprandially in all dogs. The earliest passage of kibble from the stomach was noted within 15 minutes in 25% of the studies and within one hour in the remainder of the studies. With GK and HGK, no separation of contrast medium from the kibble was observed. The earliest passage of kibble and contrast medium from the stomach occurred within 15 minutes in 50% of GK studies and 33% of the HGK studies. Remainder of the studies showed the onset of the gastric emptying within one hour. The time of complete gastric emptying with IK, GK, and HGK was tabulated (Table 2). The mean and standard error (SE) of complete gastric emptying time were 7.6 k 1.98 hours with IK, 7.0 2 1.86 hours with GK, and 4.7 2 0.67 hours with HGK. Statistical analysis of the values of IK and GK studies did not show a significant difference (comparison of paired data by the t test). However, gastric emptying time for HGK studies was significantly longer than the calculated half value of gastric emptying time for GK in the same dog (P < 0.05), in which the mean and SE were 3.6 f 0.86 hours, respectively. The radiographic pattern of IK, GK, and HGK was different. With IK, a partial separation of the contrast medium surrounding kibble occurred, and this resulted in filling defect shadows and thus a mottled appearance (Fig. 1). However, no separation of the contrast medium from kibble particles was noted with GK and HGK. The radiographic pattern of GK and HGK in the stomach was more homogeneous than IK, although cluster formation was seen (Fig. 2). Discussion Some findings in current gastric physiology were reflected'in the results of this experiment, and they are probably applicable to clinical situations. First, times for complete gastric emptying of IK and GK were similar. Although times varied between dif-
TABLE1. The Onset of the Gastric Emptying of Three Digestible Kibble Test Meals Onset of Gastric Emptying Within 15 Minutes Test Meal Intact kibble Ground kibble Half ground kibble
Within 1 Hour
Separation of Liquid and Solid Phases
Liquid
Solid
Liquid
Solid
818
818
018
-
218 418 216
-
818 818 616
016
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TABLE2. Complete Gastric Emptying Times of Barium Sulfate Suspension and Dog Food Mixture Complete Gastric Emptying Times (hours) ~~
Body Weight Dog
(kg)
Age (mo)
1 2 3 4
12.4 13.1 11.3 8.5
26 21 20 1s
X* 2 SEt
lntact Kibble (IK) 6 10
8 7
6 9 8 7
7.6 2 1.98
Ground Kibble iGK) 6 9 7 6
7 9 7 5
7.0 2 1.86 (3.6 5 0.86)$
Half-dose Ground Kibble (HGK)
UGI Study (Liquid)
-
3 3 2 1
5 4 5
6 4 4
4.7 2 0.67
2.3
2
0.92
* t
= Mean. SE = Standard error. $ Calculated half-value of gastric emptying time of GK
ferent dogs, values were consistent in an individual dog for this experimental period. A day-to-day consistency in gastric emptying time within an individual has been r e p ~ r t e d . ~ . ' .Once '~ a normal value is achieved with this technique, it can be used for that dog as a control in evaluating future gastric emptying times in terms of altered gastric function.
FIG.1. Ventrodorsal abdominal radiograph of Dog 2 1 hour after ingestion of IK test meal. The contrast column in the small intestine appears uniformly radiopaque. This is due to the separation of the liquid phase of contrast material, while the kibble portion of the test meal is stored in the fundus and appears mottled (arrow).
Second, IK and GK (or HGK) had different gastric emptying patterns. The difference was due to the function of the proximal and distal stomach as previously described. It is known that a liquid is emptied from the stomach faster than a solid when a mixture of the
FIG. 2. Ventrodorsal abdominal radiograph of Dog 2 I hour after ingestion of GK test meal. The majority of the test meal is in the stomach and appears well mixed unlike Fig. 1. A small amount of the test meal has been evacuated from the stomach. The radiopaque coalesced test meal (arrow) can be seen in the antrum, surrounded by less radiopaque, fluid-like material, probably representing a mixture of contrast medium and gastric secretions.
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two is administered. Intact kibble had distinct liquid and solid phases, thus the liquid phase (contrast medium) was squeezed by the slow sustained contractions of the proximal stomach and emptied into the duodenum. The solid phase (kibble), however, was trapped at the pylorus to be reduced in size by the distal stomach. The GK and HGK studies added another important point in terms of onset of gastric emptying. Since GK had semisolid consistency, both liquid and solid phases were emptied from the stomach at the same time. It was easy to note the onset of gastric emptying; it was within one hour in all studies. It is known that if semisolid food is administered, contractile activities begin within 20 minutes and gradually increase in intensity,7,8,10,16 From these findings, the functional state of the proximal and distal stomach can be evaluated. With IK, it is possible to check the function of the proximal stomach. A nerve impairment would interrupt this function. In addition, with IK and preferably GK, the onset of gastric emptying can be evaluated. Absence of the solid phase in the small intestine on one-hour radiograph as well as abnormally long gastric emptying time would suggest a mechanical or functional impairment of the gastroduodenal junction or ahnormality in the distal stomach, e . g . , pyloric outlet obstruction, hypertrophic gastritis, l7 protruding neoplasia, or nerve dysfunction. Third, a rough estimate of gastric emptying rate was made using GK and HGK studies. It has been reported that digestible solid food is generally emptied from the stomach at a linear rate, while fluids are emptied exponentially.’ However, it was shown in one study that linear gastric emptying occurred only in the middle of the study, and near the end the rate showed an exponential pattern.* This finding was again demonstrated in six Beagle dogs where gastric emptying of the solid phase was a “monoexponential” function at least for the first 60 minutes. l 1 Although the present experiment did not measure rate, complete time for gastric emptying of HGK was statistically longer than the calculated half value for GK. This might be due to the linear-exponential pattern, since a small volume of ingesta is emptied with a slower rate than a large volume of ingesta. 15716
1984
Some technical problems should be discussed in terms of application of this technique to clinical cases. First, at the end of each examination, overlying contrast-medium-laden feces obscured the stomach. In this instance, lateral views can be substituted to detect the presence of test meal in the stomach. Second, palatability of the test meal can create problems. It is possible to place food normally fed on the test meal to increase the patient’s appetite. However, the amount should be minimal so that it does not alter gastric emptying time. Force-feeding is an alternative method. Third, the animal’s cooperation is necessary when making the radiographs. Extreme excitement alters the time of gastric emptying. The use of chemical restraint should be avoided because most tranquilizers hasten or delay gastric emptying.’* It is an advantage that positioning is not critical in performance of this technique. Conclusion
The contrast radiographic technique described previously resulted in a qualitative evaluation of function of proximal and distal parts of the stomach. Considering current gastric physiology, the digestible solid food contrast examination can be applied: (I) to examine pyloric obstruction and functional impairment of the proximal and distal stomach and (2) to serve as a presurgical or predrug therapy data base in terms of gastric emptying time. Technical problems may result from: (1) palatability of the test meal, (2) excitement of the animal, and (3) superimposition of the contrast-medium-laden feces over the stomach. Although more normal studies are required, the normal gastric emptying time in dogs with the full dose meal using this technique is five to ten hours. Onset of gastric emptying of the solid phase should occur within one hour postprandially. A linear-exponential pattern is a normal finding in gastric emptying of digestible solid food. A small-dose meal, as used in the HGK studies, may not initiate the normal emptying rhythm. Thus examination of gastric emptying should utilize the full dose meal (8 g/kg of solid food and 57 mVkg of contrast medium).
REFEREI\ICES 1 . Kelly KA. Motility of the stomach and gastroduodenal junction. In: Johnson LR, ed. Physiology of the gastrointestinal tract. New York: Raven Press, 1981:393-410. 2. Kelly KA, Code CF, Elveback LR. Patterns of canine gastric electrical activity. Am J Physiol 1969;217:46I-70. 3. Sarna SK, Daniel EE, Kingma YJ. Simulation of the electriccontrol activity of the stomach by an array of relaxation oscillators. Am J Dig Dis 1972;17:299-310. 4. Smout AJPM, Van der Schee EJ, Grashuis JL. Postprandial and interdigestive gastric electrical activity in the dog rccorded by means of cutaneous electrodes. In: Christensen J , ed. Gastrointestinal motility. New York: Raven Press, 1980: 187-94. 5. Mroz CT, Kelly KA. The Role of the extrinsic antral nerves
in the regulation of gastric emptying. Surg Gynecol Obstet 1977 ;145:369-77. 6. Wilbur BG, Kelly KA. Effect of proximal gastric, complete gastric, and truncal vagotomy on canine gastric electric activity, motility, and emptying. Ann Surg 1973;178:295-303. 7. Itoh Z, Aizawa I, Thkeuchi S, Takayanagi R. Diurnal changes in gastric motor activity in conscious dogs. Am J Dig Dis 1977;22:117-24. 8. Hinder RA, Kelly KA. Canine gastric emptying of solids and liquids. Am J Physiol 1977;233:E335-E340. 9. Meyer JH, Mandiola S, Shadchehr A, Cohen M. Dispersion of solid food by the canine stomach. Gastroenterology 1977;72:1102. 10. Akkermans LMA, Jacobs F, Hong-Yoe 0, Roelofs JMM,
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Wittebol P. A noninvasive method to quantify antral contractile activity in man and dog (A preliminary report). In: Christensen J, ed. Gastrointestinal Motility. New York: Raven Press, 1980:195-202. 1 1 . Theodorakis MC. External scintigraphy in measuring rate of gastric emptying in Beagles. Am J Physiol 1980;239:G39-G43.
12. Van Liere EJ, Crisler G. Normal emptying time of the stomach of the dog. Proc SOCExp Biol and Med 1937;31:85-7. 13. Interone CV, Del Finado JE, Miller B, Bombeck T, Nyhus LM. Parietal cell vagotomy: studies of gastric emptying and observations of protection from histamine-induced ulcer. Arch Surg 1971 ;102:43-4.
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14. Kronfeld DS. Nature and use of commercial dog foods. J Am Vet Med Assoc 1975;166:487-93. 15. Kelly KA. Gastric emptying of liquids and solids: roles of proximal and distal stomach. Am J Physiol 1980;239:G7l-G79. 16. Malagelada JR. Quantification of gastric solid-liquid discrimination during digestion of ordinary meals. Gastroenterology 1977;72:1264-7. 17. Happe RP, van den Brom WE, van der Gaag I. Duodenogastric reflux in the dog, a clinicopathological study. Res Vet Sci 1982;33:280-6. 18. Zontine WJ. Effect of chemical restraint drugs on the passage of barium sulfate through the stomach and duodenum of dogs. J Am Vet Med Assoc 1973;162:878-84.
RADIOGRAPHIC DIAGNOSIS Signalment
Eight-year-old, male, Airedale Terrier. History
(1) Weight loss and intermittent nasal discharge of several months duration. (2) Acute loss of vision on the day of presentation. Physical Examination
(1) Small amount of dried mucoid discharge present over the external nares. (2) No detectable vision with total absence of the menace as well as both direct and consensual pupillary reflexes. Radiography
(1) Under general anesthesia survey radiographs of the skull were obtained. A contrast study was then performed to evaluate more thoroughly the areas surrounding the optic nerves and chiasm. (2) The angularis oculi veins were surgically exposed and catheterized. (3) A cavernous sinus venogram was obtained by repeating skull radiographs at the end of rapid, simultaneously delivered injections of 10 ml of meglumine and sodium diatrizoate* into each angularis oculi vein. (4) See Figures 1 and 2. Radiographic Findings
(1) Survey radiographs of the skull were normal (not shown). (2) A cavernous sinus venogram from a normal dog is provided for comparison (Fig. 1). In the dorsoventral abnormal venogram (Fig. 2A), contrast medium is seen approaching the cavernous venous sinus rostrally in the ophthalmic vein, centrally in the retroglenoid vein, and caudally in the condyloid vein. However, no
* Renovist,
Squibb, Princeton, New Jersey 08540.
contrast medium fills either the orbital plexus or cavernous venous sinus. A similar lack of filling is seen in the lateral venogram (Fig. 2B). (3) A cerebral arteriogram was normal (not shown). Radiographic Diagnosis
Mass or brain swelling in the cranial half of the ventral cranial vault. Discussion
Cavernous sinus venography was used to identify an abnormal soft-tissue mass in the ventral cranial vault. Prior to radiographic evaluation a thorough ophthalmoscopic examination and an electroretinogram were performed; no abnormalities were found. Failure to elicit a visual-evoked response suggested a conduction disturbance between the orbital optic nerves and occipital cortex. The radiographic findings, therefore, confirmed the clinical and electrodiagnostic assessment of a lesion in the visual pathway in the region of the optic chiasm. Cavernous sinus venography and cerebral anteriography have been used to evaluate and localize spaceoccupying lesions in the cranial vault. In at least one report,' however, cavernous sinus venography was found to be more sensitive in revealing abnormalities, particularly those involving the floor of the cranial cavity. The owner was given a grave prognosis, and the animal was euthanized. At necropsy, the brain and floor of the cranial vault appeared grossly normal. On further dissection, however, an abnormal soft-tissue mass that invaded the cavernous sinus and bones at the base of the cranium was discovered. The histopathologic diagnosis of the mass was adenocarcinoma, probably of olfactory origin. Extensive degeneration was seen in both the intracranial optic nerves and optic chiasm. Blindness resulted from compression of the optic nerves by the growing tumor. Antegrade wallerian degeneration had progressed to the level of the optic chiasm.