Skip to main content
PMC home page
Annals of Surgery logoLink to Annals of Surgery
. 1990 May;211(5):630–638.

Differential effects of gut hormones on pancreatic and intestinal growth during administration of an elemental diet.

B M Evers 1, M Izukura 1, C M Townsend Jr 1, T Uchida 1, J C Thompson 1
PMCID: PMC1358240  PMID: 2339923

Abstract

Liquid elemental diets (ED) will, in time, cause atrophy of the gut. Pentagastrin (PG), neurotensin (NT), and bombesin (BBS) are peptides that have trophic effects on the gut of normal rats. This study examined the effect of these three agents on gut atrophy produced by ED. Four groups of rats were given an ED and injected with either saline (control), PG (250 micrograms/kg), NT (300 micrograms/kg), or BBS (10 micrograms/kg) subcutaneously every 8 hours for 5 or 10 days. A fifth group was fed rat chow ad libidum. The rats were killed on day 6 or 11; the pancreas and segments of small intestine were removed. Atrophy of ileal mucosa was apparent on days 6 and 11, and atrophy of jejunal mucosa was manifest by day 11. Bombesin prevented jejunal mucosal atrophy and significantly increased ileal mucosal growth (compared with control). Neurotensin prevented the jejunal, but not the ileal, mucosal atrophy produced by ED. Pentagastrin had no effect on gut mucosa. Bombesin and PG, but not NT, stimulated pancreatic growth. Neurotensin stimulates pancreaticobiliary secretions (PBS), which are known to stimulate gut growth. Jejunoileal bypass was performed to determine whether trophic effects of NT on gut mucosa were mediated through stimulation of PBS. After 1 week treatment, animals were killed and segments of intestine removed. As expected NT was trophic for gut mucosa in continuity with the luminal stream; furthermore NT produced significant stimulation of growth of gut mucosa in the bypassed segment. We conclude that both BBS and NT are trophic for intestinal mucosa of rats given ED; both agents have a more pronounced effect on jejunum. The trophic effect of NT is mediated, in part, by a mechanism unrelated to stimulation of PBS. Bombesin and NT may have important regulatory functions in the adaptive growth of small bowel mucosa and in the maintenance of gut mucosal integrity.

Full text

PDF
630

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Altmann G. G. Influence of bile and pancreatic secretions on the size of the intestinal villi in the rat. Am J Anat. 1971 Oct;132(2):167–177. doi: 10.1002/aja.1001320204. [DOI] [PubMed] [Google Scholar]
  2. Alverdy J. C., Aoys E., Moss G. S. Total parenteral nutrition promotes bacterial translocation from the gut. Surgery. 1988 Aug;104(2):185–190. [PubMed] [Google Scholar]
  3. Anastasi A., Erspamer V., Bucci M. Isolation and structure of bombesin and alytesin, 2 analogous active peptides from the skin of the European amphibians Bombina and Alytes. Experientia. 1971 Feb 15;27(2):166–167. doi: 10.1007/BF02145873. [DOI] [PubMed] [Google Scholar]
  4. Baker J. W., Deitch E. A., Li M., Berg R. D., Specian R. D. Hemorrhagic shock induces bacterial translocation from the gut. J Trauma. 1988 Jul;28(7):896–906. doi: 10.1097/00005373-198807000-00002. [DOI] [PubMed] [Google Scholar]
  5. Bury K. D., Stephens R. V., Cha C. J., Randall H. T. Chemically defined diets. Can J Surg. 1974 May;17(3):124–134. [PubMed] [Google Scholar]
  6. Deitch E. A., Winterton J., Berg R. Thermal injury promotes bacterial translocation from the gastrointestinal tract in mice with impaired T-cell-mediated immunity. Arch Surg. 1986 Jan;121(1):97–101. doi: 10.1001/archsurg.1986.01400010111015. [DOI] [PubMed] [Google Scholar]
  7. Doyle H., Greeley G. H., Jr, Mate L., Sakamoto T., Townsend C. M., Jr, Thompson J. C. Distribution of neurotensin in the canine gastrointestinal tract. Surgery. 1985 Mar;97(3):337–341. [PubMed] [Google Scholar]
  8. Ekman R., Ivarsson S., Jansson L. Bombesin, neurotensin and pro-gamma-melanotropin immunoreactants in human milk. Regul Pept. 1985 Mar;10(2-3):99–105. doi: 10.1016/0167-0115(85)90004-7. [DOI] [PubMed] [Google Scholar]
  9. Evers B. M., Gomez G., Townsend C. M., Jr, Rajaraman S., Thompson J. C. Endogenous cholecystokinin regulates growth of human cholangiocarcinoma. Ann Surg. 1989 Sep;210(3):317–323. doi: 10.1097/00000658-198909000-00007. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Fatemi S. H., Cullan G. E., Sharp J. G. Evaluation of the effects of pentagastrin, gastrin and pancreatic glucagon on cell proliferation in the rat gastrointestinal tract. Cell Tissue Kinet. 1984 Mar;17(2):119–133. doi: 10.1111/j.1365-2184.1984.tb00574.x. [DOI] [PubMed] [Google Scholar]
  11. Feurle G. E., Müller B., Rix E. Neurotensin induces hyperplasia of the pancreas and growth of the gastric antrum in rats. Gut. 1987;28 (Suppl):19–23. doi: 10.1136/gut.28.suppl.19. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Fine H., Levine G. M., Shiau Y. F. Effects of cholecystokinin and secretin on intestinal structure and function. Am J Physiol. 1983 Sep;245(3):G358–G363. doi: 10.1152/ajpgi.1983.245.3.G358. [DOI] [PubMed] [Google Scholar]
  13. Fox A. D., Kripke S. A., De Paula J., Berman J. M., Settle R. G., Rombeau J. L. Effect of a glutamine-supplemented enteral diet on methotrexate-induced enterocolitis. JPEN J Parenter Enteral Nutr. 1988 Jul-Aug;12(4):325–331. doi: 10.1177/0148607188012004325. [DOI] [PubMed] [Google Scholar]
  14. Freeman J. B., Egan M. C., Millis B. J. The elemental diet. Surg Gynecol Obstet. 1976 Jun;142(6):925–932. [PubMed] [Google Scholar]
  15. Gleeson M. H., Bloom S. R., Polak J. M., Henry K., Dowling R. H. Endocrine tumour in kidney affecting small bowel structure, motility, and absorptive function. Gut. 1971 Oct;12(10):773–782. doi: 10.1136/gut.12.10.773. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Gregor M., Menge H., Stössel R., Riecken E. O. Effect of monoclonal antibodies to enteroglucagon on ileal adaptation after proximal small bowel resection. Gut. 1987;28 (Suppl):9–14. doi: 10.1136/gut.28.suppl.9. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Gélinas M. D., Morin C. L. Effects of bile and pancreatic secretions on intestinal mucosa after proximal small bowel resection in rats. Can J Physiol Pharmacol. 1980 Sep;58(9):1117–1123. doi: 10.1139/y80-167. [DOI] [PubMed] [Google Scholar]
  18. Johnson L. R., Copeland E. M., Dudrick S. J., Lichtenberger L. M., Castro G. A. Structural and hormonal alterations in the gastrointestinal tract of parenterally fed rats. Gastroenterology. 1975 May;68(5 Pt 1):1177–1183. [PubMed] [Google Scholar]
  19. Johnson L. R., Lichtenberger L. M., Copeland E. M., Dudrick S. J., Castro G. A. Action of gastrin on gastrointestinal structure and function. Gastroenterology. 1975 May;68(5 Pt 1):1184–1192. [PubMed] [Google Scholar]
  20. Johnson L. R. The trophic action of gastrointestinal hormones. Gastroenterology. 1976 Feb;70(2):278–288. [PubMed] [Google Scholar]
  21. Lehy T., Puccio F., Chariot J., Labeille D. Stimulating effect of bombesin on the growth of gastrointestinal tract and pancreas in suckling rats. Gastroenterology. 1986 Jun;90(6):1942–1949. doi: 10.1016/0016-5085(86)90265-9. [DOI] [PubMed] [Google Scholar]
  22. Lhoste E., Aprahamian M., Pousse A., Hoeltzel A., Stock-Damge C. Trophic effect of bombesin on the rat pancreas: is it mediated by the release of gastrin or cholecystokinin? Peptides. 1985;6 (Suppl 3):89–97. doi: 10.1016/0196-9781(85)90356-0. [DOI] [PubMed] [Google Scholar]
  23. Mainz D. L., Black O., Webster P. D. Hormonal control of pancreatic growth. J Clin Invest. 1973 Sep;52(9):2300–2304. doi: 10.1172/JCI107418. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Mayston P. D., Barrowman J. A. The influence of chronic administration of pentagastrin on the rat pancreas. Q J Exp Physiol Cogn Med Sci. 1971 Apr;56(2):113–122. doi: 10.1113/expphysiol.1971.sp002105. [DOI] [PubMed] [Google Scholar]
  25. Miyata M., Rayford P. L., Thompson J. C. Hormonal (gastrin, secretin, cholecystokinin) and secretory effects of bombesin and duodenal acidification in dogs. Surgery. 1980 Feb;87(2):209–215. [PubMed] [Google Scholar]
  26. Morin C. L., Ling V., Bourassa D. Small intestinal and colonic changes induced by a chemically defined diet. Dig Dis Sci. 1980 Feb;25(2):123–128. doi: 10.1007/BF01308310. [DOI] [PubMed] [Google Scholar]
  27. Morin C. L., Ling V. Effect of pentagastrin on the rat small intestine after resection. Gastroenterology. 1978 Aug;75(2):224–229. [PubMed] [Google Scholar]
  28. Oscarson J. E., Veen H. F., Williamson R. C., Ross J. S., Malt R. A. Compensatory postresectional hyperplasia and starvation atrophy in small bowel: dissociation from endogenous gastrin levels. Gastroenterology. 1977 May;72(5 Pt 1):890–895. [PubMed] [Google Scholar]
  29. Roy C. C., Laurendeau G., Doyon G., Chartrand L., Rivest M. R. The effect of bile and of sodium taurocholate on the epithelial cell dynamics of the rat small intestine. Proc Soc Exp Biol Med. 1975 Sep;149(4):1000–1004. doi: 10.3181/00379727-149-38943. [DOI] [PubMed] [Google Scholar]
  30. Sagor G. R., Ghatei M. A., O'Shaughnessy D. J., Al-Mukhtar M. Y., Wright N. A., Bloom S. R. Influence of somatostatin and bombesin on plasma enteroglucagon and cell proliferation after intestinal resection in the rat. Gut. 1985 Jan;26(1):89–94. doi: 10.1136/gut.26.1.89. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Sakamoto T., Newman J., Fujimura M., Greeley G. H., Jr, Townsend C. M., Jr, Thompson J. C. Role of neurotensin in pancreatic secretion. Surgery. 1984 Aug;96(2):146–153. [PubMed] [Google Scholar]
  32. Solomon T. E., Morisset J., Wood J. G., Bussjaeger L. J. Additive interaction of pentagastrin and secretin on pancreatic growth in rats. Gastroenterology. 1987 Feb;92(2):429–435. doi: 10.1016/0016-5085(87)90138-7. [DOI] [PubMed] [Google Scholar]
  33. Spector M. H., Traylor J., Young E. A., Weser E. Stimulation of mucosal growth by gastric and ileal infusion of single amino acids in parenterally nourished rats. Digestion. 1981;21(1):33–40. doi: 10.1159/000198517. [DOI] [PubMed] [Google Scholar]
  34. Steiner M., Bourges H. R., Freedman L. S., Gray S. J. Effect of starvation on the tissue composition of the small intestine in the rat. Am J Physiol. 1968 Jul;215(1):75–77. doi: 10.1152/ajplegacy.1968.215.1.75. [DOI] [PubMed] [Google Scholar]
  35. Upp J. R., Jr, Poston G. J., MacLellan D. G., Townsend C. M., Jr, Barranco S. C., Thompson J. C. Mechanisms of the trophic actions of bombesin on the pancreas. Pancreas. 1988;3(2):193–198. doi: 10.1097/00006676-198804000-00014. [DOI] [PubMed] [Google Scholar]
  36. Weser E., Bell D., Tawil T. Effects of octapeptide-cholecystokinin, secretin, and glucagon on intestinal mucosal growth in parenterally nourished rats. Dig Dis Sci. 1981 May;26(5):409–416. doi: 10.1007/BF01313582. [DOI] [PubMed] [Google Scholar]
  37. Weser E., Vandeventer A., Tawil T. Stimulation of small bowel mucosal growth by midgut infusion of different sugars in rats maintained by total parenteral nutrition. J Pediatr Gastroenterol Nutr. 1982;1(3):411–416. doi: 10.1097/00005176-198201030-00023. [DOI] [PubMed] [Google Scholar]
  38. Williamson R. C., Bauer F. L., Ross J. S., Malt R. A. Contributions of bile and pancreatic juice to cell proliferation in ileal mucosa. Surgery. 1978 May;83(5):570–576. [PubMed] [Google Scholar]
  39. Wilmore D. W., Smith R. J., O'Dwyer S. T., Jacobs D. O., Ziegler T. R., Wang X. D. The gut: a central organ after surgical stress. Surgery. 1988 Nov;104(5):917–923. [PubMed] [Google Scholar]
  40. Wood J. G., Hoang H. D., Bussjaeger L. J., Solomon T. E. Effect of neurotensin on pancreatic and gastric secretion and growth in rats. Pancreas. 1988;3(3):332–339. doi: 10.1097/00006676-198805000-00015. [DOI] [PubMed] [Google Scholar]
  41. Wood J. G., Hoang H. D., Bussjaeger L. J., Solomon T. E. Neurotensin stimulates growth of small intestine in rats. Am J Physiol. 1988 Dec;255(6 Pt 1):G813–G817. doi: 10.1152/ajpgi.1988.255.6.G813. [DOI] [PubMed] [Google Scholar]
  42. Young E. A., Cioletti L. A., Winborn W. B., Traylor J. B., Weser E. Comparative study of nutritional adaptation to defined formula diets in rats. Am J Clin Nutr. 1980 Oct;33(10):2106–2118. doi: 10.1093/ajcn/33.10.2106. [DOI] [PubMed] [Google Scholar]

Articles from Annals of Surgery are provided here courtesy of Lippincott, Williams, and Wilkins

RESOURCES