Skip to main content
Log in

Nerve Terminals Containing Neuropeptides Decrease in Number After Massive Proximal Small Bowel Resection in the Piglet

  • Published:
Digestive Diseases and Sciences Aims and scope Submit manuscript

Abstract

The aim of this study was to evaluate possiblechanges in the neuropeptide innervation pattern of theremaining porcine ileum following 75% proximal resectionof the small intestine. Three-month-old piglets were operated on and two months postoperativelyfullthickness specimens of the proximal part of thedistal ileum wall were taken. Age-matched 3- and5-month-old unoperated piglets were used as controls. The number and intensity of VIP-, galanin-,enkephalin-, substance P-, and somatostatin-containingnerve fibers were estimated in sections processed forimmunofluorescence microscopy and subjected toquantitative scoring. The VIP-, galanin-, andenkephalin-immunoreactive fibers of the circular musclelayer and villi were also quantitated bycomputer-assisted morphometry. The number and intensityof VIP-immunoreactive fibers in the mucosa and circular muscle layermarkedly decreased after resection as compared to3-month-old and 5-month-old controls (P < 0.05). Thegalanin immunoreactivity index decreased significantly after resection in the circular muscle layer ascompared to both control groups (P < 0.05). Theincrease in the number of enkephalin-immunoreactivenerve fibers that normally occurred from 3 to 5 monthsof age was inhibited by the resection. We were notable to see any differences in somatostatin or substanceP immunoreactivity between the groups. The resultssuggest that massive resection induces significant changes in the neuropeptide-containinginnervation of the remaining small intestine. Thesefindings are compatible with altered motor activity andmucosa function in the remain intestine.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

REFERENCES

  1. Dowling R, Booth C: Structural and functional change s following small intestinal resection in the rat. Clin Sci 32:139 - 149, 1967

    Google Scholar 

  2. Hanson WR, Osborne JW, Sharp JG: Compensation by the residual intestine after intestinal rese ction in the rat. I. Influence of amount of tissue removed 72:692- 700, 1977

    Google Scholar 

  3. Hanson WR, Osborne JW, Sharp JG: Compensation by the residual intestine after intestinal resection in the rat. II. Inuence of postoperative time interval. Gastroenterology 72:701- 705, 1977

    Google Scholar 

  4. Schulzke JD, Fromm M, Bentzel CJ, Zeitz M, Menge H, Riecken EO: Ion transport in the experime ntal short bowel syndrome of the rat. Gastroenterology 102:497- 504, 1992

    Google Scholar 

  5. Pakarinen M, Miettinen TA, Lauronen J, Kuusanmäki P, Raivio P, Kivistö T, Halttunen J: Adaptation of cholesterol absorption after proximal resection of porcine small bowel. J Lipid Res 37:1766 - 1775, 1996

    Google Scholar 

  6. Whang EE, Dunn JC, Joffe H, Mahanty H, Zinner MJ, McFadden DW, Ashley SW: Enterocyte functional adaptation following intestinal resection. J Surg Res 60:370 - 374, 1996

    Google Scholar 

  7. Dowling RH: Small bowel adaptation and its regulation. Scand J Gastroenterol Suppl 74:53- 74, 1982

    Google Scholar 

  8. Lentze MJ: Intestinal adaptation in short-bowel syndrome. Eur J Pediatr 148:294 - 299, 1989

    Google Scholar 

  9. Miller ER, Ullrey DE: The pig as a model for human nutrition. Annu Rev Nutr 7:383- 406, 1987

    Google Scholar 

  10. McCance RA: Experimental rese ction of the intestine in newborn pigs. Br J Nutr 21:731- 740, 1967

    Google Scholar 

  11. Laplace JP: Compensatory hypertrophy of the residual small intestine afte r partial enterectomy. A neurohumoral feedback? Ann Rech Vet 11:165- 177, 1980

    Google Scholar 

  12. Margolis A, Ricour C, Harouchi A, Guyot M, Laouari D, Balsan S: Intestinal calcium-binding protein 3 months afte r massive small bowel re se ction in the piglet. Am J Clin Nutr 30:2041- 2046, 1977

    Google Scholar 

  13. Buie WD, Thursten OG, van Aerde JE, Thonson AB, Fedorak RN: Jejunum is preferable for construction of a Bianchi bowellengthening procedure in swine short bowel. J Pediatr Surg 28:102- 109, 1993

    Google Scholar 

  14. Costa M, Brookes SJ: The ente ric nervous system. Am J Gastroenterol 89:S129 - S137, 1994

    Google Scholar 

  15. Quigley E, Thompson JS: The motor re sponse to intestinal resection: Motor activity in the canine small intestine following distal resection. Gastroenterology 105:791- 798, 1993

    Google Scholar 

  16. Quigley E, Thompson J, Adrian T: Motor adaptation following extensive rese ction of the small intestine. Gastroenterology 108:A673, 1995

    Google Scholar 

  17. Wittmann T, Crenner F, Koenig M, Grenier JF: Adaptive changes in postprandial motility after intestinal re section and bypass. Electromyographic study in rats. Dig Dis Sci 33:1370 - 1376, 1988

    Google Scholar 

  18. Johnson CP, Sarna SK, Zhu YR, Buchmann E, Bonham L, Telford GL, Roza AM, Adams MB: Delayed gastroduodenal emptying is an important mechanism for control of intestinal transit in short-gut syndrome. Am J Surg 171:90 - 95, 1996

    Google Scholar 

  19. Buchan AM, Curtis SB, Lund PK, Pederson RA: Effect of massive small bowel resection on components of the peptidergic innervation of the rat small intestine. Digestion 2:134 - 141, 1990

    Google Scholar 

  20. Adrian TE, Thompson JS, Quigley EMM: Enteric neuropeptide abnormalities following small bowel rese ction and the effect of a tape ring and lengthening procedure. Trans Proc 28:2552- 2553, 1996

    Google Scholar 

  21. Buts JP, De Keyser N, Dive C: Cellular adaptation of the rat small intestine after proximal enterectomy: Changes in microvillous enzyme s and in the se cretory component of immunoglobulins. Pediatr Res 22:29 - 33, 1987

    Google Scholar 

  22. Postuma R, Moroz S, Friesen F: Extreme short-bowel syndrome in an infant. J Pediatr Surg 18:264 - 268, 1983

    Google Scholar 

  23. Sigalet DL, Lees GM, Aherne F, van Aerde JE, Fedorak RN, Keelan M, Thomson AB: The physiology of adaptation to small bowel resection in the pig: An integrated study of morphological and functional changes. J Pediatr Surg 25:650 - 657, 1990

    Google Scholar 

  24. Ekblad E, Winther C, Ekman R, Hakanson R, Sundler F: Projections of peptide-containing neurons in rat small intestine. Neuroscience 20:169 - 188, 1987

    Google Scholar 

  25. Daniel EE, Furness JB, Costa M, Belbeck L: The projections of chemically identified nerve fibres in canine ileum. Cell Tissue Res 247:377- 384, 1987

    Google Scholar 

  26. Shen Z, Klover Stahl B, Larsson LT, Malmfors G, Ekblad E, Sundler F: Peptide-containing neurons remain unaffected after intestinal autotransplantation: An expe rimental study in the piglet. Eur J Pediatr Surg 3:271- 277, 1993

    Google Scholar 

  27. McConalogue K, Furness JB: Gastrointestinal neurotransmitters. Baillieres Clin Endocrinol Metab 8:51- 76, 1994

    Google Scholar 

  28. Diaz Juarez JL, Bodega G, Arilla E, Prieto JC: Interaction of vasoactive intestinal peptide with rat small intestinal epithelial ce lls after intestinal resection. Biosci Rep 5:559 - 566, 1985

    Google Scholar 

  29. Lezoche E, Carlei F, Vagni V, Mora GV, Speranza V: Elevated plasma leve ls of vasoactive intestinal polypeptide in short bowel syndrome. Am J Surg 145:369 - 370, 1983

    Google Scholar 

  30. Adrian TE, Thompson JS, Quigley EMM, Staab P: The release of the enteric neuropeptides following small bowel resection, with and without bypass of the ileocecal junction. Gastroenterology 108:A268, 1995

    Google Scholar 

  31. Bauer FE: Galanin: A new biologically active gastrointestinal neuropeptide. Z Gastroenterol 28:160 - 169, 1990 (in German)

    Google Scholar 

  32. Bilchik AJ, Hines OJ, Adrian TE, Skotzko MJ, McFadden DW, Zinner MJ, Ashley SW: Early regional expression and se cre tion of peptide YY and enteroglucagon after massive resection of small bowel. J Am Coll Surg 180:417- 426, 1995

    Google Scholar 

  33. Brown DR, Hildebrand KR, Parsons AM, Soldani G: Effects of galanin on smooth muscle and mucosa of porcine jejunum. Peptides 11:497- 500, 1990

    Google Scholar 

  34. Dockray G: Physiology of enteric neuropeptides. InPhysiology of the Gastrointestinal Tract. LR Johnson (eds). New York, Raven Press, 1994, pp 611- 641

    Google Scholar 

Download references

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Vento, P., Kiviluoto, T., Pakarinen, M. et al. Nerve Terminals Containing Neuropeptides Decrease in Number After Massive Proximal Small Bowel Resection in the Piglet. Dig Dis Sci 43, 1102–1110 (1998). https://doi.org/10.1023/A:1018803423167

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1018803423167

Navigation