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Effects of jejunoileal autotransplantation on gastrointestinal regulatory peptides

  • Small Bowel Transplantation
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Abstract

Plasma gastrointestinal hormones were measured before and during feeding in eight dogs, more than one year after total autotransplant of the entire jejunoileum, and in controls. At sacrifice, tissues were taken from the transplanted segment and intact bowel for measurement of hormone and enteric neuropeptide content. Gastrin levels were reduced in autotransplanted dogs (fasting 63% of control, incremental response 67% of control, bothP<0.05), reflecting the loss of acid inhibitory reflexes. Secretin and cholecystokinin responses were identical between the two groups. Postprandial levels of gastric inhibitory peptide (incremental response 175% of control,P<0.005), insulin, and peptide YY (158% of control,P<0.05) were elevated following denervation, the former suggesting more rapid gastric emptying while the latter may reflect malabsorption. The neurotensin meal response was obtunded by denervation (incremental response 43% of control,P<0.05), providing evidence for a neural pathway for its release. Pancreatic polypeptide responses were identical between the groups, suggesting intact pancreatic innervation. Abnormal hormone secretion may contribute to the impaired fed motor responses seen following extrinsic denervation of the small bowel. In contrast, the neuropeptide content of the autotransplanted small intestine is normal, suggesting that extrinsic denervation has no long-term effects on peptide content of the enteric nervous system.

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References

  1. Treem WR: Short bowel syndrome.In Pediatric Gastrointestinal Disease. R Wyllie, JS Hyams (eds). Philadelphia, Saunders, 1993, pp 573–603

    Google Scholar 

  2. Goulet O, Revillon Y, Jan D, Brousse JN, De Potter S, Cera-Bensussan N, Rambaud C, Buisson C, Pellerin D, Mougenot JF: Small bowel transplantation in children. Transplant Proc 22:2499–2500, 1990

    Google Scholar 

  3. Grant D, Wall W, Zhong R, Mineault R, Sutherland F, Ghent C, Duff J: Experimental clinical intestinal transplantation: Initial experience of a Canadian center. Transplant Proc 22:2497–2498, 1990

    Google Scholar 

  4. Williams JW, Sankary HN, Foster PF: Splanchnic transplantation: An approach to the infant dependent on parenteral nutrition who develops irreversible liver disease. JAMA 261:1458–1462, 1989

    Google Scholar 

  5. Starzl TE, Rowe MI, Todo S: Transplantation of multiple abdominal viscera. JAMA 261:1449–1457, 1989

    Google Scholar 

  6. Cohen Z, Wassef R, Nordgren SR, Langer B: Experimental and clinical intestinal transplantation. Scand J Gastroenterol 20(suppl 117):63–67, 1985.

    Google Scholar 

  7. Sarr MG, Kelly KA: Myoelectric activity of the autotransplanted canine jejunoileum. Gastroenterology 81:303–310, 1981

    Google Scholar 

  8. Aeberhard PF, Magnenat LD, Zimmerman WA: Nervous control of myoelectric complex of the small bowel. Am J Physiol 238:G102-G108, 1980

    Google Scholar 

  9. Bueno L, Praddaude F, Ruckebusch Y: Propagation of electrical spike activity along the small intestine: Intrinsic versus extrinsic neural influences. J Physiol (London) 72:15–26, 1979

    Google Scholar 

  10. Heppel J, Kelly KA, Sarr MG: Neural control of canine small intestinal interdigestive myoelectric complexes. Am J Physiol 244:G95-G100, 1983

    Google Scholar 

  11. Sarr MG, Tanaka M, Duenes JA: Jejunoileal autotransplantation: Effects on small intestinal motility. Surg Forum 39:160–162, 1988

    Google Scholar 

  12. Niebel W, Beglinger C, Singer MV: Hormonal control of pancreatic secretion by intrajejunal HCl: Studies in dogs with an autotransplanted entire jejunoileum. Pancreas 6:341–349, 1991

    Google Scholar 

  13. Soper NJ, Sarr MG, DiMagno EP, Kelly KA, Go VLW: Influence ofin situ neural isolation of jejunoileum on post-prandial pancreaticobiliary secretion and gastric emptying. Dig Dis Sci 36:880–887, 1991

    Google Scholar 

  14. Malagelada J-R, Camilleri M, Stanghellini V: Manometric Diagnosis of Gastrointestinal Motility Disorders. New York, Thieme, 1986

    Google Scholar 

  15. Bass BL, Sayadi H, Harmon JW, Wall S, Korman LY: VIP receptors and content after bowel transplantation. J Surg Res 46:431–438, 1989

    Google Scholar 

  16. Evers BM, Townsend CM, Uchida T, Greeley GH, Allen E, Thompson JC: Effect of total jejunoileal denervation on fat-stimulated release of peptide YY and cholecystokinin. Surgery 108:248–253, 1990

    Google Scholar 

  17. Larosa CA, Blank MA, Kimura K, Jaffe BM: Effect of transplantation on tissue levels of substance P, vasoactive intestinal polypeptide, and serotonin in rat small intestine. Ann NY Acad Sci 594:336–346, 1990

    Google Scholar 

  18. Nelson DK, Sarr MG, Go VLW:In vivo neural isolation of the canine jejunoileum: Temporal adaptation of enteric neuropeptides. Gut 32:1336–1341, 1991

    Google Scholar 

  19. Bloom SR, Long RG (eds): Radioimmunoassay of Gut Regulatory Peptides. Philadelphia, Saunders, 1982

    Google Scholar 

  20. Joekel CS, Herrington MK, Vanderhoof JA, Adrian TE: Postnatal development of circulating cholecystokinin and secretin, pancreatic growth, and exocrine function in guinea pigs. Int J Pancreatol 13:1–13, 1993

    Google Scholar 

  21. Lee YC, Allen JM, Uttenthal LO, Roberts PM, Gill SS, Bloom SR: Quantitation and characterization of human plasma neurotensin-like immunoreactivity in response to a meal. Dig Dis Sci 30:129–133, 1985

    Google Scholar 

  22. Adrian TE, Ferri G-L, Bacarese-Hamilton AJ, Fuessl HS, Polak JM, Bloom SR: Human distribution and release of a putative new gut hormone, peptide YY. Gastroenterol 89:1070–1077, 1985

    Google Scholar 

  23. Heding LG: Determination of total serum insulin (IRI) in insulin-treated diabetic patients. Diabetologia 8:260–266, 1972

    Google Scholar 

  24. Conlon JM: Regionally specific antisera to human β-preprotachykinin. Methods Neurosci 6:207–221, 1991

    Google Scholar 

  25. Yamashita Y, Kako N, Homma K, Hirai T, Toge T, Hinder RA, DeMeester TR, Adrian TE: Neuropeptide release from the isolated, perfused, lower esophageal sphincter region of the rabbit and the effect of vasoactive intestinal polypeptide on the sphincter. Surgery 112:227–234, 1992

    Google Scholar 

  26. Allen JM, Yeats JC, Adrian TE, Bloom SR: Radioimmunoassay of neuropeptide Y (NPY). Regul Pept 8:61–70, 1984

    Google Scholar 

  27. Adrian TE, Savage AP, Sagor GR, Allen JM, Bacarese-Hamilton AJ, Tatemoto K, Polak JM, Bloom SR: Effect of PYY on gastric pancreatic and biliary function in man. Gastroenterology 89:494–499, 1985

    Google Scholar 

  28. Savage AP, Adrian TE, Carolan G, Chatterjee VK, Bloom SR: Effects of peptide YY (PYY) on mouth to cecum intestinal transit time and on the rate of gastric emptying in healthy volunteers. Gut 70:166–170, 1987

    Google Scholar 

  29. Bilchik AJ, Adrian TE, Hines OJ, Ashley SW, Zinner MJ: Peptide YY is a physiological regulator of water and electrolyte absorption in the small bowel in vivo. Gastroenterology 105:1441–1448, 1993

    Google Scholar 

  30. Bilchik AJ, Hines OJ, Zinner MJ, Adrian TE, Berger JJ, McFadden DW, Ashley SW: Peptide YY augments postprandial small intestinal absorption in the conscious dog. Am J Surg 167:570–574, 1994

    Google Scholar 

  31. Adrian TE, Savage AP, Bacarese-Hamilton AJ, Wolfe K, Besterman HS, Bloom SR: Peptide YY abnormalities in gastrointestinal disease. Gastroenterology 90:379–384, 1986

    Google Scholar 

  32. Adrian TE, Savage AP, Fuessl HS, Wolfe K, Besterman HS, Bloom SR: Release of peptide YY (PYY) after resection of small bowel, colon or pancreas in man. Surgery 101:715–719, 1987

    Google Scholar 

  33. Bloom SR: An enteroglucagon tumor. Gut 17:520–523, 1972

    Google Scholar 

  34. Besterman HS, Bloom SR, Sarson DL, Blackburn AM, Johnstone DJ, Patel HR, Stewart JS, Modigliani R, Guerin S, Mallinson CN: Gut hormone profile in coeliac disease. Lancet 11:785–788, 1978

    Google Scholar 

  35. Besterman HS, Adrian TE, Mallinson CN, Christofides ND, Sarson DL, Pera A, Lombardo L, Modigliani R, Bloom SR: Gut hormone release after intestinal resection. Gut 23:854–861, 1982

    Google Scholar 

  36. Sarson DL, Scopinaro N, Bloom SR: Gut hormone changes after jejunoileal (JIB) or biliopancreatic (BPB) bypass surgery for morbid obesity. Int J Obes 5:471–480, 1981

    Google Scholar 

  37. Uttenthal LO, Batt RM, Carter MW, Bloom SR: Stimulation of DNA synthesis in cultured small intestine by partially purified enteroglucagon. Regul Pept 3:84–88, 1982

    Google Scholar 

  38. Lluis F, Gomez G, Masaki F, Greeley GH, Thompson JC: Peptide YY inhibits pancreatic secretion by inhibiting cholecystokinin release in the dog. Gastroenterology 94:137–144, 1988

    Google Scholar 

  39. Hosotani R, Inoue K, Kogire M, Tatemoto K, Mutt V, Suzuki T, Rayford PL, Tobe T: Effect of natural peptide YY on pancreatic secretion and cholecystokinin release in conscious dogs. Dig Dis Sci 34:468–473, 1989

    Google Scholar 

  40. Nelson DK, Furlow BL, Go VL, Sarr MG: Enteroendocrine peptides in a canine model of orthotopic jejunoileal autotransplantation. Regul Pept 45:421–434, 1993

    Google Scholar 

  41. Blackburn AM, Fletcher DR, Bloom SR, Christofides ND, Long RG, Fitzpatrick ML: Effect of neurotensin on gastric function in man. Lancet 11:987–989, 1980

    Google Scholar 

  42. Blackburn AM, Christofides ND, Ghatei MA, Sarson DL, Ebeid FH, Ralphs DNL, Bloom SR: Elevation of plasma neurotesin in the dumping syndrome. Clin Sci 59:237–243, 1980

    Google Scholar 

  43. Al-Saffar A, Theodorsson-Norheim E, Rosell S: Nervous control of the release of neurotensin-like immunoreactivity from the small intestine of the rat. Acta Physiol Scand 122:1–6, 1984

    Google Scholar 

  44. Soffer EE, Adrian TE: The effect of meal composition and sham feeding on duodenojejunal motility in humans. Dig Dis Sci 37:1009–1014, 1992

    Google Scholar 

  45. Jian R, Besterman HS, Sarson DL, Rymes C, Hostein J, Bloom SR, Rambaud JC: Colonic inhibition of gastric secretion in man. Dig Dis Sci 26:195–201, 1981

    Google Scholar 

  46. Preston DM, Adrian TE, Christofides ND, Lennard-Jones JE, Bloom SR: Positive correlation between symptoms and circulating motilin, pancreatic polypeptide and gastrin levels in functional bowel disease. Gut 26:1059–1064, 1985

    Google Scholar 

  47. Thompson J, Rose SS, Spanta AD, Quigley EMM: The long term effects of jejunoileal autotransplantation on intestinal function. Surgery 111:62–68, 1992

    Google Scholar 

  48. Brown JC, Dryburgh JR: A gastric inhibitory polypeptide: The complete amino acid sequence. Canad J Biochem 49:867–872, 1971

    Google Scholar 

  49. Dupré J, Ross SA, Watson D, Brown JC: Stimulation of insulin secretion by gastric inhibitory peptide in man. J Clin Endocrinol 37:826–827, 1973

    Google Scholar 

  50. Christifides ND, Long RG, Fitzpatrick ML, McGregor GP, Bloom SR: Effect of motilin on the gastric emptying of glucose and fat in humans. Gastroenterology 80:456–460, 1981

    Google Scholar 

  51. Quigley EMM, Spanta AD, Rose SG, Lof J, Thompson J: Long-term effects of jejunoileal autotransplantation on myoelectrical activity in canine small intestine. Dig Dis Sci 35:1505–1517, 1990

    Google Scholar 

  52. Manolas KJ, Adrian TE, Farmer HM, Bacarese-Hamilton AJ, Bloom SR, Welbourn RB: Effect of food on porcine gut regulatory peptides in portal venous blood. Horm Res 22:284–290, 1985

    Google Scholar 

  53. Schwartz TW, Holst JJ, Fahrenkrug J, Lindkaer Jensen S, Nielsen DV, Rehfeld JF, Schaffalitzky de Muckadell OB, Stadil F: Vagal, cholinergic regulation of pancreatic polypeptide secretion. J Clin Invest 61:781–789, 1978

    Google Scholar 

  54. Adrian TE, Bloom SR, Besterman HS, Barnes AJ, Cooke TJC, Russell RCG, Faber RG: Mechanism of pancreatic polypeptide release in man. Lancet 11:161–163, 1976

    Google Scholar 

  55. Sarr MG, Dunes JM, Tanaka M: A model of in vivo neural isolation of the entire jejunoileum: transplantation and the effects on intestinal motility. J Surg Res 47:266–272, 1989

    Google Scholar 

  56. Thor K, Rosell S, Rokaeus A, Kager L: Gln4-neurotensin changes the motility pattern of the duodenum and proximal jejunum from a fasting-type to a fed-type. Gastroenterology 83:569–574, 1982

    Google Scholar 

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Presented in part at the Sixth Biennial Symposium of the American Motility Society, Newport, Rhode Island, October 15, 1990; and has appeared in part in abstract form: Gastroenterology 96:1228, 1990, and Gastroenterology 100:A413, 1991.

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Adrian, T.E., Quigley, E.M.M., Rose, S.G. et al. Effects of jejunoileal autotransplantation on gastrointestinal regulatory peptides. Digest Dis Sci 39, 2457–2466 (1994). https://doi.org/10.1007/BF02087667

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  • DOI: https://doi.org/10.1007/BF02087667

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