Surgical removal of the pregastric pouch does not affect voluntary ethanol consumption in golden hamsters

Surgical removal of the pregastric pouch does not affect voluntary ethanol consumption in golden hamsters

Physiology & Behavior,Vol. 57, No. 6, pp. 1127-1129, 1995 Copyright © 1995 ElsevierScienceLtd Printed in the USA. All rights reserved 0031-9384/95 $9...

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Physiology & Behavior,Vol. 57, No. 6, pp. 1127-1129, 1995 Copyright © 1995 ElsevierScienceLtd Printed in the USA. All rights reserved 0031-9384/95 $9.50 + .00

Pergamon 0031-9384(95)00020-8

Surgical Removal of the Pregastric Pouch Does Not Affect Voluntary Ethanol Consumption in Golden Hamsters DAVID

DIBATTISTA

Psychology Department, Brock University, St. Catharines, Ontario CANADA L2S 3A1, E-mail: ddibatti @ spartan.ac.brocku.ca DtBATI'ISTA, D. Surgical removal of the pregastric pouch does not affect voluntary ethanol consumption in golden hamsters. PHYSIOL BEHAV 57(6) 1127 - ! 129, 1995.--Golden hamsters underwent either surgical removal of the pregastric pouch (PGX) or sham surgery. Following recovery from surgery, hamsters were given free access to 15% (v/v) ethanol solution for 40 days, and then to 30% ethanol solution for a further 32 days. PGX and sham-operated hamsters ingested similar amounts of absolute ethanol throughout the study, with intake exceeding 15 g/kg/day when 30% ethanol solution was available. The failure to find a significant effect of surgical treatment on ethanol intake was not attributable to a lack of statistical power, but rather suggests that other factors, such as the hamster's high levels of hepatic alcohol dehydrogenase, are responsible for the hamster's unusual tolerance for ethanol. Golden hamster

Pregastric pouch

Ethanol

Alcohol

G O L D E N hamsters readily ingest certain substances that other rodents consume only in moderate amounts. One such substance is the disaccharide sugar lactose, the carbohydrate found in milk. Most adult mammals are ,deficient in the intestinal enzyme lactase (17,27), which splits lactose into the absorbable monosaccharides glucose and galactose, and lactose ingestion may produce negative consequences that lead to the development of conditioned taste avoidance (7,24). Adult hamsters resemble other mammals in being deficient in intestinal lactase (1,2), but in contrast to other rodents that have been studied, hamsters prefer lactose solutions to water across a wide range of concentrations, and voluntarily consume lactose in substantial quantities (9,10). The hamster's unusual tolerance for lactose has recently been shown to depend on its possession of a pregastric pouch that is similar in both structure .and function to the rumen of herbivores (11). In hamsters, ingested food first enters the pregastric pouch, where it remains for up I:o an hour or more (5,13), with volatile fatty acids being produced and absorbed into the bloodstream (16). Food then passes into the gastric pouch, which is similar to the glandular stomach of monogastric mammals (16), and thence into the small intestine, lit has been found that surgical removal of the pregastric pouch causes hamsters to reduce voluntary lactose consumption by 40% (11). It appears that microorganisms residing in the pregastric pouch act upon ingested lactose and break it down into its constituent monosaccharides before it enters the small intestine. Thus, the breakdown of lactose within the pregastric pouch seems to prevent hamsters from suffering the negative consequences of lactose ingestion that may be experienced by monogastric animals (7,24). Ethanol is another substance that golden hamsters consume more avidly than do other rodents. Whereas most rodents prefer water to ethanol solutions at ethanol concentrations higher than

about 8% or so, hamsters prefer ethanol solutions to water across a wide range of concentrations (14,20). Thus, under free-choice conditions, hamsters derive the majority of their dally water ration from ethanol solution at concentrations up to 15% and drink substantial amounts of ethanol solutions even at concentrations up to 45% (6,20). In addition, depending on the concentration of ethanol solution offered, hamsters may consume more than 15 g/ kg/day of absolute ethanol and derive more than one-third of their total caloric intake from ethanol (6); in contrast, nonselectively bred strains of rat typically ingest only 2 - 3 g/kg/day. Although hamsters tend to consume much more ethanol than do other rodents, there is a growing body of evidence that hamsters and rats respond similarly to various manipulations that affect ethanol consumption. Thus, like rats, hamsters increase their ethanol intake when salt is added to the diet (12) and decrease it when a serotonin uptake inhibitor is administered (19). Despite their prodigious voluntary intake of ethanol, hamsters do not demonstrate either withdrawal symptoms or serious organ disorder following prolonged ethanol consumption, apparently because ethanol metabolism is rapid and efficient (4,15,20,22). One factor that may contribute to the hamster's tolerance for ethanol is the presence of high levels of hepatic alcohol dehydrogenase, the enzyme that metabolizes ethanol to acetaldehyde (20). It has also been suggested (11,23) that the hamster's tolerance for ethanol may be related to its possession of a pregastric pouch. Thus, microorganisms in the pregastric pouch may act to metabolize, at least to some degree, orally ingested ethanol before it is absorbed into the bloodstream and thereby contribute to the hamster's unusual tolerance for ingested ethanol. Although there is no direct evidence to support this hypothesis, it is well established that microorganisms capable of metabolizing ethanol to acetic acid do exist (e.g., Acetobacter and Gluconobacter spp.; 1127

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FIG. 1. Mean intake of absolute ethanol (g/kg/day) by hamsters during 8-day blocks. SEMs ranged from 0.40 to 0.80 for 15% ethanol, and from 0.33 to 1.02 for 30% ethanol. see refs. 3,26) and that these microorganisms could flourish in the environment provided by the pregastric pouch (16,21). If microorganisms residing in the pregastric pouch do indeed play an important role in permitting hamsters to consume large quantities of ethanol, then removal of the pregastric pouch should inhibit ethanol intake. The following experiment was therefore carried out to determine whether surgical removal of the pregastric pouch influences voluntary ethanol consumption in golden hamsters.

METHOD Subjects Sixteen adult male golden hamsters (Mesocricetus auratus), bred in the colony at Brock University, were housed individually in hanging wire cages (25 × 18 x 15 cm). Hamsters had continuous access to tap water and powdered Purina Rodent Chow (No. 5001) throughout the experiment. The housing room was kept at 21-23 ° Celsius and illuminated on a 14:10 light-dark cycle (lights on at 0800 h).

Surgery Because the surgical procedure has been described in detail elsewhere (11), only a brief description will be provided here. After being deprived of food and water for 3 - 5 h to insure that the pregastric pouch would be empty, hamsters were anesthetized with halothane and a midline incision was made in the abdomen. The pregastric pouch was carefully isolated and excised, the gastric pouch was returned to its original location, and the incision was closed. Sham-operated hamsters were treated in a similar fashion, with the pregastfic pouch being isolated from surrounding structures, but not ligated and removed.

Procedure Hamsters were randomly assigned to two groups (n = 8/ group) to undergo either pregastric pouch removal (PGX) or sham surgery, as described above. Beginning 20-24 days after surgery, all hamsters were given continuous free access to 15% ethanol (v/v) for 40 days, and then to 30% ethanol for a further

32 days. Ethanol solutions were presented in containers designed to reduce spillage and evaporation (see ref. 9 for details). Ethanol intake was recorded at two-day intervals. Purina chow and water were always freely available.

RESULTS Ethanol consumption data (g/kg/day) were analyzed using a two-way ANOVA with one between-subjects variable (surgical treatment) and one within-subjects variable (8-day blocks); corrections for degrees of freedom for the within-subjects variable were carried out following the recommendations of Keppel (18). The data are summarized in Fig. 1. Neither the main effect of treatment, F(1, 14) = 0.72, nor the treatment × blocks interaction, F(6, 83) = 0.81, proved significant. Even during the first two days of exposure to ethanol, intakes of the two treatment groups differed only slightly (PGX: Mean +_ SEM = 8.5 _ 0.8 g/kg/day; Sham: 9.4 +_ 1.5), and they remained similar throughout the experiment. Thus, removal of the pregastric pouch did not significantly affect ethanol consumption. However, the main effect of blocks was significant, F(6, 83) = 53.7, p < .001. In keeping with previous findings (e.g., 8), ethanol intake was greater during 30% ethanol presentation than during the last three 8-day blocks of 15% ethanol presentation (mean ___ SE = 15.5 ___0.31 vs. 12.2 ___0.40 g/kg/day, respectively). All animals were active and apparently healthy from the time of surgery until the termination of the study. A 2 X 2 ANOVA (surgical treatment x time) was carried out on the initial and the final body weights. A significant main effect of time, F(1, 14) = 200.4, p < 0.001, indicated that during the 72-day period of ethanol availability, body weights increased significantly (PGX: start = 118.5 ___3.6 g, finish = 154.8 ___4.1; Sham: start = 119.4 ___2.6, finish = 148.6 _+ 5.4). Other effects were not significant (surgical treatment: F(1, 14) = 0.26; surgical treatment x time: F(1, 14) = 2.36). Necropsy of PGX hamsters revealed that removal of the pregastric pouch had been successful in all cases and that there had been no regrowth of the pouch. All surgical wounds were found to have healed cleanly, with no signs of infection.

ETHANOL INGESTION

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DISCUSSION Although surgical removal of the pregastric pouch of golden hamsters has no remarkable effects on either total food intake (25) or growth (13), it has been shown to dramatically decrease lactose consumption (11). The results of the present study indicate that pouch removal does not have any substantial effect on hamsters' prodigious consumption of ethanol. W h e n drinking 30% ethanol solution, both sham-operated hamsters and P G X hamsters ingested about 15 g/kg/day of absolute ethanol, an amount which is similar to the very high intakes observed in previous research (4,6). Thus, hamsters consume substantial amounts of ethanol even when the pregastric pouch has been surgically removed prior to the initial exposure to ethanol. The failure to find a sitgnificant effect of surgical treatment on ethanol intake in this study cannot simply be attributed to a lack of statistical power. Under the conditions of this study, the power

of the statistical test to detect even a relatively modest 20% decrease in ethanol intake resulting from removal of the pregastric pouch was approximately 0.97. Thus, it is reasonable to conclude that under the conditions of this study surgical removal of the pregastric pouch has no substantial effect on ethanol consumption in golden hamsters. This finding indicates that other factors, such as the hamster's high levels of hepatic alcohol dehydrogenase (20), may be responsible for the hamster's unusual tolerance for ethanol. ACKNOWLEDGEMENTS This research was supported by an operating grant from the Natural Sciences and Engineering Research Council of Canada. Thanks to Dayle Belme, Margaret Grimwood, and Michele Robillard for their assistance in the laboratory.

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15. Harris, R. A.; Krause, W.; Goh, E.; Case, J. Behavioral and biochemical effects of chronic consumption of ethanol by hamsters. Pharmacol. Biocbem. Behav. 10:343-347; 1979. 16. Hoover, W. H.; Mannings, C. L.; Sheerin, H. E. Observations on digestion in the golden hamster. J. Anim. Sci. 28:349-352; 1969. 17. Johnson, J. D.; Kretchmer, N.; Simoons, F. J. Lactose malabsorption:Its biology and history. Advances Pediatrics 21:197-237; 1974. 18. Keppel, G. Design and analysis:A researcher's handbook. Englewood Cliffs, New Jersey: Prentice Hall; 1991. 19. Keung- W. M.; Vallee, B. L. Daidzin and daidzein suppress freechoice ethanol intake in Syrian Golden hamsters. Proceedings of the National Academy of Sciences USA. 90:10008-10012; 1993. 20. Kulkosky, P. J.; Cornell, N. W. Free-choice ethanol intake and ethanol metabolism in the hamster and rat. Pharmacol. Biochem. Behav. 11:439-444; 1979. 21. Kunstyr, I. Some quantitative and qualitative aspects of the stomach microflora of the conventional rat and hamster. Zentralblatt fur Veterinarmedizin A. 21:553-561 ; 1974. 22. McMillan, D. E.; Ellis, F. W.; Frye, G. D.; Pick, J. R. Failure of signs of physical dependence to develop in hamsters after prolonged consumption of large doses of ethanol. Pharmacol. Biochem. Behav. 7:55-57; 1977. 23. National Research Council. Nutrient requirements of laboratory animals. 3rd ed. Washington, D.C.: National Academy of Sciences; 1978. 24. Pelchat, M. L.; Grill, H. J.; Rozin, P.; Jacobs, J. Quality of acquired response to tastes by Rattus norvegicus depends on type of associated discomfort. J. Comp. Psychol. 97:140-153; 1983. 25. Rowland, N. E. Ingestive behaviour of Syrian hamsters: Advantages of the comparative approach. Brain Res. Bull. 15:417-423; 1985. 26. Salle, A. J. Fundamentals principles of bacteriology. 7th ed. New York: McGraw-Hill; 1973. 27. Scrimshaw, N. S.; Murray, E. B. The acceptability of milk and milk products in populations with a prevalence of lactose intolerance. Am. J. Clin. Nutrition 48:1083-1159; 1988.