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Differential adrenergic response to extrinsic denervation in canine longitudinal jejunal and ileal smooth muscle

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Journal of Gastrointestinal Surgery

Abstract

Early postoperative complications after small bowel transplantation (SBT) are likely mediated, at least in part, by dysmotility caused by the obligate disruption of extrinsic and enteric nerves in the graft. Adrenergic hypersensitivity of gut smooth muscle has been observed in some (but not all) segments of intestine in various experimental models of SBT, highlighting regional and species variability in response to denervation. Little is known about changes in canine longitudinal muscle after extrinsic denervation. Six dogs each underwent either complete extrinsic denervation of the jejunoileum or a control operation (transection and reanastomosis of the proximal jejunum and distal ileum). In vitro contractile response of longitudinal muscle strips to norepinephrine was evaluated at the time of the operation, and 2 weeks and 8 weeks later. After extrinsic denervation, the jejunal response to norepinephrine was preserved at all time points; however, the ileum displayed a decreased sensitivity to norepinephrine, an effect unmasked after intramural neural blockade with tetrodotoxin. These data support a potential for neurally mediated dysmotility after SBT and reinforce the differences in responses to extrinsic denervation between species, as well as differences within different regions and between anatomic segments of small intestine in the same species.

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References

  1. Grant D. Intestinal transplantation: 1997 report of the international registry. Intestinal Transplant Registry. Transplantation 1999;67:1061–1064.

    Article  PubMed  CAS  Google Scholar 

  2. Abu-Elmagd K, Reyes J, Bond G, Mazariegos G, Wu T, Murase N, Sindhi R, Martin D, Coangelo J, ZakM, Janson D, Ezzelarab M, Dvorchik I, Parizhskaya M, Deutsch M, Demetris A, Fung J, Starzl TE. Clinical intestinal transplantation: A decade of a single center experience. Ann Surg 2001;234:404–416.

    Article  PubMed  CAS  Google Scholar 

  3. Sarr MG. A model of jejunoileal in vivo neural isolation of the entire jejunoileum: Transplantation and the effects on intestinal motility. J Surg Res 1989;47:266–272.

    Article  PubMed  CAS  Google Scholar 

  4. Johnson CP, Sarna SK, Cowles VE, Baytiyeh R, Zhu YR, Buchmann E, Bonham L, Roza AM, Adams MB. Effects of transection and reanastomosis on postprandial jejunal transit and contractile activity. Surgery 1995;117:531–537.

    Article  PubMed  CAS  Google Scholar 

  5. Mousa H, BuenoJ, Griffiths J, Kocoshis S, Todo S, Reyes J, DiLorenzo C. Intestinal motility after small bowel transplantation. Transplant Proc 1998;30:2535–2536.

    Article  PubMed  CAS  Google Scholar 

  6. Pernthaler H, Nehoda H, Riedmann B, Aichberger C, Mar-greiter R. Altered but preserved motility of a human small bowel allograft. Transplant Proc 1996;28:2794.

    PubMed  CAS  Google Scholar 

  7. Sugitani A, Bauer AJ, Reynolds JC, Halfter WM, Nomoto M, Starzl TE, Todo S. The effect of small bowel transplantation on the morphology and physiology of intestinal muscle. Transplantation 1997;63:186–194.

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  9. Nguyen BL, Thompson JS, Quigley EM. Regional variation in canine muscle mass and function. Dig Dis Sci 1995;401:491–1497.

    Google Scholar 

  10. Coupar IM, Liu L. A simple method for measuring the effects of drugs on intestinal longitudinal and circular muscle. J Pharmacol Toxicol Methods 1996;36:147–154.

    Article  PubMed  CAS  Google Scholar 

  11. Luckensmeyer GB, Keast JR. Activation of alpha- and beta-adrenoreceptors by sympathetic nerve stimulation in the large intestine of the rat. J Physiol 1998;510:549–561.

    Article  PubMed  CAS  Google Scholar 

  12. Siegle ML, Buhner S, Schemann M, Schmid HR, Ehrlein HJ. Propagation velocities and frequencies of contractions along canine small intestine. Am J Physiol 1990;258:738–744.

    Google Scholar 

  13. Rahman MS, Taguchi T, Nakao M, Yamada T, Suita S. Long-term results of short segmental syngeneic small intestinal transplantation: Comparison of jejunal and ileal grafts. J Pediatr Surg 1996;31:908–911.

    Article  PubMed  CAS  Google Scholar 

  14. Balsiger BM, Duenes JA, Ohtani N, Sarr MG. Extrinsic denervation of canine jejunum causes neuronal adrenergic and muscular cholinergic hypersensitivity. Gastroenterology 1999;116:A1075.

    Google Scholar 

  15. Belloli C, Re G, Arioli F, Badino P, Carcano R, Odore R, Girardi C, Beretta C. Differences between longitudinal and circular smooth muscle in β-adrenergic control of motility of isolated equine ileum. Am J Vet Res 1997;58:1422–1426.

    PubMed  CAS  Google Scholar 

  16. Balsiger BM, Duenes JA, Ohtani N, Sarr MG. Adrenergic and cholinergic contractile mechanisms adapt after chronic extrinsic denervation of the small bowel. Gastroenterology 2000;118:A2088.

    Google Scholar 

  17. Shibata C, Balsiger BM, Anding WJ, Sarr MG. Adrenergic denervation hypersensitivity in ileal circular smooth muscle after small bowel transplantation in rats. Dig Dis Sci 1997; 42:2213–2221.

    Article  PubMed  CAS  Google Scholar 

  18. Shibata C, Murr MM, Balsiger BM, Anding WJ, Sarr MG. Contractile activity of circular smooth muscle in rats one year after small bowel transplantation: Differing adaptive response of the jejunum and ileum to denervation. J Gastrointest Surg 1998;2:463–472.

    Article  PubMed  CAS  Google Scholar 

  19. Ohtani N, Balsiger BM, Anding WJ, Duenes JA, Sarr MG. Small bowel transplantation induces adrenergic hypersensitivity in ileal longitudinal smooth muscle in rats. J Gastrointest Surg 2000;4:77–85.

    Article  PubMed  CAS  Google Scholar 

  20. Murr MM, Miller VM, Sarr MG. Contractile properties of enteric smooth msucle after small bowel transplantation in rats. Am J Surg 1996;171:212–218.

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  22. Yunker AM, Galligan JJ. Extrinsic denervation increases NADPH diaphorase staining in myenteric nerves of guinea pig ileum. Neurosci Lett 1994;167:51–54.

    Article  PubMed  CAS  Google Scholar 

  23. Stadelmann AM, Fink JG, Telford GL, Walgenbach-Tel-ford S, Koch TR. Nitric oxide synthase is increased following small intestinal transplantation in the rat. Neurosci Lett 1999;266:97–100.

    Article  PubMed  CAS  Google Scholar 

  24. Taguchi T, Guo R, Masumoto K, Nada O, Nakao M, Yanai K, Suita S. Chronological change of distribution in nitric oxide and peptidergic neurons after rat small intestinal transplantation. J Pediatr Surg 1999;34:341–345.

    Article  PubMed  CAS  Google Scholar 

  25. Ishii H, Kusunoki M, Yamamura T, Utsonomiya J. Effects of neuropeptides on smooth muscle contraction after small bowel transplantation. Eur Surg Res 1997;29:362–367.

    PubMed  CAS  Google Scholar 

  26. Osinski MA, Bass P. Chronic denervation of rat jejunum results in cholinergic supersensitivity due to reduction of cholinesterase activity. J Pharmacol Exp Ther 1993;226:1684–1690.

    Google Scholar 

  27. Hirose R, Taguchi T, Hirata Y, Yamada T, Nada O, Suita S. Immunohistochemical demonstration of enteric nervous distribution after syngeneic small bowel transplantation in rats. Surgery 1995;117:560–569.

    Article  PubMed  CAS  Google Scholar 

  28. Taguchi T, Zorchta E, Sonnino RE, Guttman FM. Small intestinal transplantation in the rat: Effect on physiological properties of smooth muscle and nerves. J Pediatr Surg 1989;24:1258–1263.

    Article  PubMed  CAS  Google Scholar 

  29. Malmfors G, Hakanson R, Okmian L, Sundler F. Peptidergic nerves persist after jejunal autotransplantation: An experimental study in the piglet. J Pediatr Surg 1980;15:53–56.

    Article  PubMed  CAS  Google Scholar 

  30. Nakahata N, Nakanishi H, Suzuki T. Prejunctional inhibition mediated via alpha 2-adrenoceptors in excitatory transmission of canine small intestine. J Pharm Pharmacol 1982;34:510–513.

    PubMed  CAS  Google Scholar 

  31. De Ponti F, Giaroni C, Cosentino M, Lecchini S, Frigo G. Adrenergic mechanisms in the control of gastrointestinal motility: From basic science to clinical applications. Pharmacol Ther 1996;69:59–78.

    Article  PubMed  Google Scholar 

  32. Kostka P, Sipos SN, Kwan CY, Niles LP, Daniel EE. Identification and characterization of presynaptic and postsynaptic beta adrenoreceptors in the longitudinal smooth muscle/myenteric plexus of dog ileum. J Pharmacol Exp Ther 1989;251:305–310.

    PubMed  CAS  Google Scholar 

  33. Lu G, Sarr MG, Szurszewski JH. Effect of extrinsic denervation in a canine model of jejunoileal autotransplantation on mechanical and electrical activity of jejunal circular smooth muscle. Dig Dis Sci 1997;42:40–46.

    Article  PubMed  CAS  Google Scholar 

  34. Sarna SK. Gastrointestinal longitudinal muscle contractions. Am J Physiol 1993;265:156–164.

    Google Scholar 

  35. Tonini M, Lecchini S, Frigo G, Crema A. Action of tetrodotoxin on spontaneous electrical activity of some smooth muscle preparations. Eur J Pharmacol 1974;29:236–240.

    Article  PubMed  CAS  Google Scholar 

  36. McIntyre AS, Thompson DG, Day S, Burnham WR, Walker ER. Modulation of human upper intestinal nutrient transit by a beta adrenoreceptor mediated pathway. Gut 1992;33:1062–1070.

    Article  PubMed  CAS  Google Scholar 

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Authors and Affiliations

  1. Gastroenterology Research Unit and Department of Surgery, Mayo Clinic, Rochester, Minnesota

    Nicholas J. Zyromski M.D., Judy A. Duenes B.S., Michael L. Kendrick M.D., Karen D. Libsch M.D., Roland Seiler B.S., Toshiyuki Tanaka M.D. & Michael G. Sarr M.D. (Professor of Surgery, Chair)

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  1. Nicholas J. Zyromski M.D.
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  2. Judy A. Duenes B.S.
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  3. Michael L. Kendrick M.D.
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  4. Karen D. Libsch M.D.
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  5. Roland Seiler B.S.
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  6. Toshiyuki Tanaka M.D.
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  7. Michael G. Sarr M.D.
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Supported by grants from the National Institutes of Health (NIH DK39337 and NIH DK07198) and the Mayo Foundation.

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Zyromski, N.J., Duenes, J.A., Kendrick, M.L. et al. Differential adrenergic response to extrinsic denervation in canine longitudinal jejunal and ileal smooth muscle. J Gastrointest Surg 6, 418–425 (2002). https://doi.org/10.1016/S1091-255X(02)00006-9

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  • DOI: https://doi.org/10.1016/S1091-255X(02)00006-9

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