Skip to main content
Log in

Long-term effects of jejunoileal autotransplantation on myoelectrical activity in canine small intestine

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

Abstract

We studied the longitudinal effects of autotransplantation on the motor function of the jejunoileum. By performing the autotransplantation procedure in a manner similar to that employed for allotransplantation, we sought to examine the long-term effects of both extrinsic denervation and the operative procedure itself on small intestinal motor function. Although initially disrupted, interdigestive myoelectrical activity demonstrated progressive organization: 88% of migrating myoelectrical complexes in animals studied between 12 and 20 months following autotransplantation demonstrated each phase of the complex in normal sequence. Longitudinal studies of several parameters of myoelectrical activity provided further evidence of progressive organization and entrainment of motor functions within the denervated intestine. Several abnormal myoelectrical patterns were observed within the autotransplanted segment, however, and coordination of either slow wave or phase III activity with the proximal innervated intestine did not recover with time. The major component of the myoelectrical response to feeding was permanently impaired with a delayed onset and shortened duration of the fed response. We conclude that the extrinsically denervated intestine recovers the ability to generate and organize all phases of the MMC but demonstrates permanent impairment of the major motor response to food. However, anoxic and cooling damage to enteric nerves and muscle, incurred during the autotransplantation procedure, may explain the persistence of abnormal motor patterns and impaired myoelectrical conduction and could play an important role, additional to that of extrinsic denervation, in the long-term motor function of the allotransplanted 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. Jaffe BM: Visceral interchange. Am J Surg 157:2–5, 1989

    PubMed  Google Scholar 

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

    Google Scholar 

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

    PubMed  Google Scholar 

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

    Google Scholar 

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

    PubMed  Google Scholar 

  6. Weisbrodt NW, Copeland EM, Thor PJ, Mukhopadhyay AK, Johnson LR: Nervous and humoral factors which govern the fasted and fed patterns of intestinal myoelectric activity.In G Vantrappen (ed). Proceedings of the Fifth International Symposium on Gastrointestinal Motility. Herentals, Typoff Press, 1974, pp 82–87

    Google Scholar 

  7. 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 

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

    PubMed  Google Scholar 

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

    Google Scholar 

  10. Code CF, Marlett JA: The interdigestive myoelectric complex of the stomach and small bowel of dogs. J Physiol (London) 296:289–309, 1975

    Google Scholar 

  11. Scheffe H: A method for judging all contrasts in the analysis of variance. Biometrika 40:87–104, 1953

    Google Scholar 

  12. Quigley EMM, Phillips SF, Dent J: Distinctive patterns of interdigestive motility at the canine ileocolonic junction. Gastroenterology 87:836–844, 1984

    PubMed  Google Scholar 

  13. Kruis W, Azpiroz F, Phillips SF: Contractile patterns and transit of fluid in canine terminal ileum. Am J Physiol 245:G264-G270, 1985

    Google Scholar 

  14. Siegle M-L, Ehrlein H-J: Interdigestive contractile patterns of the ileum in dogs. Am J Physiol 253:G452-G460, 1987

    PubMed  Google Scholar 

  15. Sarna SK: Giant migrating contractions and their myoelectric correlates in the small intestine. Am J Physiol 253:G697-G705, 1987

    PubMed  Google Scholar 

  16. Diamant NE, Bortoff A: Nature of the intestinal slow-wave frequency gradient. Am J Physiol 216:301–307, 1969

    PubMed  Google Scholar 

  17. Diamant NE, Bortoff A: Effects of transection on the intestinal slow-wave frequency gradient. Am J Physiol 216:734–743, 1969

    PubMed  Google Scholar 

  18. Grivel M-L, Ruckebusch Y: A study in the dog and cat of the electrical activity of the small intestine some months after transection and replantation of the gut. Life Sci 10:241–250, 1971

    Google Scholar 

  19. Sarna S, Condon RE, Cowles V: Enteric mechanisms of initiation of migrating myoelectric complexes in dogs. Gastroenterology 84:814–822, 1983

    PubMed  Google Scholar 

  20. Szurszewski J, Steggerda FR: The effect of hypoxia on the electrical slow wave of the canine small intestine. Am J Dig Dis 13:168–177, 1968

    PubMed  Google Scholar 

  21. Szurszewski J, Steggerda FR: The effect of hypoxia on the mechanical activity of the canine small intestine. Am J Dig Dis 13:178–185, 1968

    PubMed  Google Scholar 

  22. Cannon WB, Burket IR: The endurance of anemia by nerve cells in the myenteric plexus. Am J Physiol 32:347–357, 1913

    Google Scholar 

  23. Hukuhara RT, Sumi T, Kotani S: Role of the ganglion cells in the small intestine taken in the intestinal intrinsic reflexes. Jpn J Physiol 11:281–288, 1961

    PubMed  Google Scholar 

  24. Kyi KKJ, Daniel EE: The effects of ischemia on intestinal nerves and electrical slow waves. Am J Dig Dis 15:959–981, 1970

    PubMed  Google Scholar 

  25. Marik F, Code CF: Control of the interdigestive myoelectric activity in dogs by the vagus nerves and pentagastrin. Gastroenterology 69:387–395, 1975

    PubMed  Google Scholar 

  26. Weisbrodt NW, Copeland EM, Moore EP, Kearley RW, Johnson LR: Effect of vagotomy on electrical activity of the small intestine of the dog. Am J Physiol 228:650–654, 1975

    PubMed  Google Scholar 

  27. Marlett JA, Code CF: Effect of celiac and superior mesenteric ganglionectomy on interdigestive myoelectric complex in dogs. Am J Physiol 237:E432-E436, 1979

    PubMed  Google Scholar 

  28. Itoh Z, Aizawa I, Takeuchi S: Neural regulation of interdigestive motor activity in canine jejunum. Am J Physiol 240:G324-G330, 1981

    PubMed  Google Scholar 

  29. Sarna S, Stoddard C, Belbeck L, McWade D: Intrinsic nervous control of migrating myoelectric complexes. Am J Physiol 241:G16-G23, 1981

    PubMed  Google Scholar 

  30. Hall KE, El-Sharkawy TY, Diamant NE: Vagal control of migrating motor complex in the dog. Am J Physiol 243:G276-G284, 1982

    PubMed  Google Scholar 

  31. Chung SA, Diamant NE: Small intestinal motility in fasted and post-prandial states: Effect of transient vagosympathetic blockade. Am J Physiol 252:G301-G308, 1987

    PubMed  Google Scholar 

  32. Fox DA, Bass P: Selective myenteric neuronal denervation of the rat jejunum. Gastroenterology 87:572–577, 1984

    PubMed  Google Scholar 

  33. Pearce AN, Wingate DL: Myoelectric and absorptive activity in the transected canine small bowel. J Physiol (London) 302:11–12P, 1980

    Google Scholar 

  34. Pinnington J, Wingate DL: The effects of motilin on periodic myoelectric spike activity in intact and transected canine small intestine. J Physiol (London) 337:471–478, 1983

    Google Scholar 

  35. Quigley EMM, Thompson JS, Lof J: Disruption of canine jejunal interdigestive myoelectrical activity by artificial ileocolonic sphincter. Dig Dis Sci 34:1434–1442, 1989

    PubMed  Google Scholar 

  36. Matsumoto T, Sarna SK, Condon RE, Cowles VE, Frantzides C: Differential sensitivities of morphine and motilin to initiate migrating motor complex in isolated intestinal segments. Regeneration of intrinsic nerves. Gastroenterology 90:61–67, 1986

    PubMed  Google Scholar 

  37. Sarna SK: Cyclic motor activity; migrating motor complex: 1985. Gastroenterology 89:894–913, 1985

    PubMed  Google Scholar 

  38. Tanaka M, Sarr MG: Total duodenectomy: Effect on canine gastrointestinal motility. J Surg Res 42:483–493, 1987

    PubMed  Google Scholar 

  39. Lang IM, Sarna SK, Condon RE: The generation of phases I and II of the migrating myoelectric complex in the dog. Am J Physiol 251(Gastrointest Liver Physiol 14):G201-G207, 1986

    PubMed  Google Scholar 

  40. Kumar D, Wingate D, Ruckebusch Y: Circadian variation in the propagation velocity of the migrating motor complex. Gastroenterology 91:926–930, 1986

    PubMed  Google Scholar 

  41. Sarna S, Condon RE, Cowles V: Morphine versus motilin in the initiation of migrating myoelectric complexes. Am J Physiol 245:G217-G220, 1983

    PubMed  Google Scholar 

  42. Sarr MG, Duenes JA: Site of action of morphine sulfate and motilin in the induction of “premature” phase III-like activity in the canine gastrointestinal tract. Surgery 103:653–661, 1988

    PubMed  Google Scholar 

  43. Borody TJ, Quigley EMM, Phillips SF, Wienbeck M, Tucker RL, Haddad A, Zinsmeister AR: Effects of morphine and atropine on motility and transit in the human ileum. Gastroenterology 89:562–570, 1985

    PubMed  Google Scholar 

  44. Telford GL, Hashmonai M, Moses AJ, Szurszewski JH: Morphine initiates migrating myoelectrical complexes by acting on peripheral opioid receptors. Am J Physiol 249:G557-G562, 1985

    PubMed  Google Scholar 

  45. Jian R, Janssens J, Vantrappen G, Ceccatelli P: Influence of metenkephalin analogue on motor activity of the gastrointestinal tract. Gastroenterology 93:114–120, 1987

    PubMed  Google Scholar 

  46. Yanda R, Summers RW: Activity fronts in fed dogs: Effect of β-adrenergic agonist. Am J Physiol 245:G647-G650, 1983

    PubMed  Google Scholar 

  47. Malmfors G, Hakanson R, Okmaian L, Sundler F: Peptidergic nerves persist after jejunal autotransplantation: An experimental study in the piglet. J Pediatr Surg 15:53–55, 1980

    PubMed  Google Scholar 

  48. Kewenter J: The vagal control of jejunal and ileal motility and blood flow. Acta Physiol Scand 65(suppl 251): 1–68, 1965

    Google Scholar 

  49. Phillips SF, Quigley EMM, Kumar D, Kamath PS: Motility of the ileocolonic junction. Gut 29:390–406, 1988

    PubMed  Google Scholar 

  50. Quigley EMM, Borody TJ, Phillips SF, Wienbeck M, Tucker RL, Haddad A: Motility of the terminal ileum and ileocecal sphincter in healthy man. Gastroenterology 87:857–866, 1984

    PubMed  Google Scholar 

  51. Sarr MG, Duenes JA: Intestinal transplantation: Early and late effects on intestinal motility. Gastroenterology 94:A399, 1988 (abstract)

    Google Scholar 

  52. Hall KE, El-Sharkawy TY, Diamant NE: Vagal control of canine postprandial upper gastrointestinal motility. Am J Physiol 250:G501-G510, 1986

    PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Quigley, E.M.M., Spanta, A.D., Rose, S.G. et al. Long-term effects of jejunoileal autotransplantation on myoelectrical activity in canine small intestine. Digest Dis Sci 35, 1505–1517 (1990). https://doi.org/10.1007/BF01540569

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF01540569

Key words

Navigation