The pig as a preclinical model for intestinal ischemia-reperfusion and transplantation studies

Journal of Surgical Research

Volumn 178, Issue 2, 2012, Pages 807-819

  Yandza, Thierry ^a,b   Tauc, Michel ^c   Saint Paul, Marie Christine ^d   Ouaissi, Mehdi ^e   Gugenheim, Jean ^a   Hébuterne, Xavier ^a,c,d  

^a CENTRE HOSPITALIER UNIVERSITAIRE DE NICE   (France)

^b INSERM   (France)

^c UNIVERSITÉ CÔTE D'AZUR   (France)

^d UNIVERSITY HOSPITAL OF NICE   (France)

^e Service de Chirurgie Digestive   (France)

Author keywords

Ischemia reperfusion injury; Pig; Small bowel transplantation

Indexed keywords

ALLOTRANSPLANTATION; ANATOMICAL VARIATION; ANIMAL STRUCTURES; BLOOD SAMPLING; DIGESTIVE SYSTEM; EXPERIMENTAL MODEL; IMMUNE SYSTEM; INTESTINE TRANSPLANTATION; MALIGNANT HYPERTHERMIA; MEDICAL RESEARCH; NONHUMAN; PRESERVATION; PRIORITY JOURNAL; REPERFUSION INJURY; REVIEW; SMALL INTESTINE; SWINE;

ANIMALS; HEME OXYGENASE-1; IMMUNE SYSTEM; INTESTINES; MODELS, ANIMAL; NITRIC OXIDE; REPERFUSION INJURY; SWINE; TRANSPLANTATION, HOMOLOGOUS;

EID: 84869091243     PISSN: 00224804     EISSN: 10958673     Source Type: Journal    
DOI: 10.1016/j.jss.2012.07.025     Document Type: Review

References (100)

1. T. Ueno, and M. Fukuzawa Current status of intestinal transplantation Surg Today 40 2010 1112
2. N.L. Tilney, and R.D. Guttmann Effects of initial ischemia/reperfusion injury on the transplanted kidney Transplantation 64 1997 945
3. P. Boros, and J.S. Bromberg New cellular and molecular immune pathway in ischemia/reperfusion injury Am J Transplant 6 2006 652
4. P. Salehi, J. Walker, and K.L. Madsen Relationship between endergic stress and pro-apoptotic/cytoprotective kinase mechanisms in intestinal preservation Surgery 141 2007 795
5. http://grants.nih.gov/grants/guide/noticefiles/not96-208.html
6. H.J. Rothkötter Anatomical particularities of the porcine immune system - A physician's view Dev Comp Immunol 33 2009 267
7. Z. Ibrahim, J. Busch, and M. Awwad Selected physiologic compatibilities and incompatibilities between human and porcine organ systems Xenotransplantation 13 2006 488
8. Allan D. Kirk Crossing the bridge: large animal models in translational transplantation research Immunol Rev 196 2003 176
9. S.P. Montgomery, S.R. Mog, and H. Xu Efficacy and toxicity of a protocol using sirolimus, tacrolimus, and daclizumab in a nonhuman primate renal allotransplant model Am J Transplant 2 2002 381
10. R.Y. Calne The initial study of the immunosuppressive effects of 6-mercaptopurine and azathioprine in organ transplantation and a few words on cyclosporin A World J Surg 6 1982 637
11. M.M. Swindle, and A.C. Smith Comparative anatomy and physiology of the pig Scand J Lab Anim Sci 25 1998 11
12. Y.I. Park, W.E. Rempel, W.J. Boylan, and T.P.E. Makhamberta Comparative growth curves of miniature and conventional pigs Genetics 83 1976 557
13. K. Gustafsson, S. Germana, and F. Hirsch Structure of miniature swine class II DRB genes: Conservation of hypervariable amino acid residues between distantly related mammalian species Proc Natl Acad Sci U S A 87 1990 9798
14. L.D. Schantz, K. Laber-Laird, S. Bingel, and M. Swindle Pigs: Applied anatomy of the gastrointestinal tract S.L. Jensen, H. Gregersen, Essentials of experimental surgery: Gastroenterology 1996 Harwood Academic New York 2611
15. J.E. Lindberg, and B. Ogle Digestive physiology of pigs. Proceedings of the 8th Symposium 2001 CABI Publishing New York
16. W.G. Pond, and H.J. Mersmann Biology of the domestic pig 2001 Comstock Publishing Associates Ithaca
17. F.A. Denz Age changes in lymph nodes J Pathol Bacteriol 59 1947 575
18. R.M. Binns, and R. Pabst Lymphoid tissue structure and lymphocyte trafficking in the pig Vet Immunol Immunopathol 43 1994 79
19. M.A. Bennell, and A.J. Husband Route of lymphocyte migration in pigs. I. Lymphocyte circulation in gut-associated lymphoid tissue Immunology 42 1981 469
20. R. Pabst, and H.J. Rothkötter Structure and function of the gut mucosal immune system R.S. Blumberg, M.F. Neurath, Immune mechanisms in inflammatory bowel disease 2006 Springer/Landes Bioscience New York 1
21. M. Bailey The mucosal immune system: recent developments and future directions in the pig Dev Comp Immunol 33 2009 375
22. T. Gramdin Animal handling Vet Clin North Am Food Anim Pract 3 1987 323
23. C.A. Smith, and M.D. Ficken Non-surgical cannulation of the vena cava for chronic blood collection in mature swine Lab Anim 41 1991 274
24. M.B. Bailie, S.K. Wixson, and M.S. Landi Vascular-access port implantation for serial blood sampling in conscious swine Lab Anim Sci 36 1986 413
25. G.M. Kaiser, M.M. Heuer, and N.R. Frühauf General handling and anesthesia for experimental surgery in pigs J Surg Res 130 2006 73
26. T. Yandza, M.F. Gerhardt, and M.C. Saint-Paul Significance of serum bile acids in small bowel allograft rejection in pigs Transplantation 87 2009 24
27. M.P. Pakarinen, P. Pirinen, and J. Lauronen Effects of transection and extrinsic denervation and a model of autotransplantation of the porcine jejunoileum on cholesterol biodynamics J Pediatr Surg 38 2003 1585
28. M. Oishi, T. Yagi, and T. Matsuno Changes in plasma endotoxin levels after small bowel auto/allo-transplantation in pigs Transplant Proc 30 1998 2616
29. J. Calleja-Kempin, J. Vasquez-Estevez, and J. Martin-Cavanna Vascular thrombosis in small bowel transplantation: a comparative study in the pig Transplant Proc 30 1998 2646
30. T.L. Fu, W.T. Zhang, and Q.P. Chen Effects of L-arginine on serum nitric oxide, nitric oxide synthase and mucosal Na+-K+-ATPase and nitric oxide synthase activity in segmental small bowel autotransplantation model World J Gastroenterol 11 2005 3605
31. H. Mousa, J. Bueno, and J. Griffiths Intestinal motility after small bowel transplantation Transplant Proc 30 1988 2535
32. J. Lauronen, M.P. Pakarinen, and P. Pirinen Effects of extrinsic denervation with or without ischemia-reperfusion injury on constitutional mucosal characteristics in porcine jejunoileum Dig Dis Sci 46 2001 476
33. R.C. Lillehei, B. Goott, and F.A. Miller The physiologic response of the small bowel of the dog to ischemia including prolonged in vitro preservation of the bowel with successful replacement and survival Ann Surg 150 1959 543
34. M.G. Sarr, J.A. Duenes, and M. Tanaka A model of jejunoileal in vivo neural isolation of the entire jejunoileum: transplantation and the effects on intestinal motility J Surg Res 47 1989 266
35. T. Yandza, M. Mekaouche, and J. Breaud In situ intestinal ischemia-reperfusion injury in the pig: a model using the first jejunal artery for flushing World J Surg 31 2007 1863
36. J.C. Llanos, A.B. Neto, and M.M. Lerco Induction of short gut syndrome and transplantation in a porcine model Transplant Proc 38 2006 1855
37. K.L. Chan, K.W. Chan, and P.K.H. Tam Segmental small bowel allograft-ischemic injury and regeneration J Pediatr Surg 33 1988 1703
38. C.J. Chiu, A.H. McArdle, and R. Brown Intestinal mucosal lesion in low-flow states Arch Surg 101 1970 478
39. J. Pirenne, E. Benedetti, and S. Moon Porcine model of combined small and large bowel transplantation: surgical aspects Transplant Proc 28 1996 2726
40. S. Weith, M. Kessler, and H. Fonouni Review of various technique of small bowel transplantation in pigs J Surg Res 171 2011 709
41. H. Kaneko, M.A. Fischman, and T.M. Buckley A comparison of portal versus systemic venous drainage in the pig small-bowel allograft recipient Surgery 109 1991 663
42. M. Fraczek, P. Hevelke, and M. Kotulski Small bowel transplantation, harvesting technique and graft preparation in pigs Ann Transplant 12 2007 19
43. R.W.G. Gruessner Large animal models in intestinal transplantation Transplant Proc 30 1998 2629
44. P. Ruiz, A. Bagni, and R. Brown Histological criteria for the identification of acute cellular rejection in human small bowel allografts: results of the Pathology Workshop at the VIII International Small Bowel Transplant Symposium Transplant Proc 36 2004 335
45. R.E. Nakhleh, A.C. Gruessner, and J. Pirenne Rejection of the colon versus ileum in a pig model of total bowel transplantation Transplant Proc 28 1996 2445
46. S. Sarnacki, Y. Révillon, and N. Cerf-Bensussan Long-term small-bowel survival induced by a spontaneously tolerated liver allograft in inbred rat strains Transplantation 54 1992 383
47. G. Malmfors, R. Hakanson, and L. Okmian Peptidergic nerves persist after jejunal autotransplantation: an experimental study in the piglet J Ped Surg 15 1980 53
48. D.K. Nelson, M.G. Sarr, and V.L. Go In vivo neural isolation of the canine jejunoileum: temporal adaptation of enteric neuropeptides Gut 32 1991 1336
49. A. Sugitani, J.C. Reynolds, M. Tsuboi, and S. Todo Extrinsic intestinal reinnervation after canine small bowel autotransplantation Surgery 123 1998 25
50. G. Privitera, R. Biffi, and G. Rossi Influence of different protocols of antibiotic prophylaxis on endoluminal bacterial overgrowth and translocation following small-bowel or combined liver-small-bowel transplantation in large-animal model Transplant Proc 29 1997 1826
51. M. Spada, M. Alessiani, and M. Fabbi Bacterial translocation is enhanced in pig intestinal transplantation when the colon is included in the graft Transplant Proc 28 1996 2658
52. O. Goulet, V. Colomb-Jung, and F. Joly Role of the colon in short bowel syndrome and intestinal transplantation J Pediatr Gastroenterol Nutr 48 Suppl 2 2009 S66
53. L. Cobianchi, S. Zonta, and J. Vigano Experimental small bowel transplantation from non-heart-beating donors: a large-animal study Transplant Proc 41 2009 55
54. D.N. Granger, M.E. Hollwarth, and D.A. Parks Ischemia-reperfusion injury: role of oxygen-derived free radicals Acta Physiol Scand 548 1986 47
55. S.E. Kong, L.R. Blennerhassett, and K.A. Heel Ischaemia-reperfusion injury to the intestine Aust NZ J Surg 68 1998 554
56. E.P. Molmenti, T. Ziambaras, and D.H. Perlmutter Evidence for an acute phase response in human intestinal epithelial cells J Biol Chem 268 1993 14116
57. O. Zamir, P.O. Hasselgren, and T. Higashiguchi Effect of sepsis or cytokine administration on release of gut peptides Am J Surg 163 1992 181
58. I.H. Mallick, W. Yang, M.C. Winslet, and A.M. Seifalian Ischemia-reperfusion injury of the intestine and protective strategies against injury Digest Dis Sci 49 2004 1359
59. W. Jassem, S.V. Fuggle, and M. Rela The role of mitochondria in ischemia/reperfusion injury Transplantation 73 2002 493
60. D.L. Carden, and D.N. Granger Pathophysiology of ischaemia reperfusion injury J Pathol 190 2000 255
61. K.A. Kuenzler, P.Y. Pearson, and M.Z. Schwartz Interleukin-11 enhances intestinal absorptive function after ischemia-reperfusion injury J Pediatr Surg 37 2002 457
62. S. Aksoyek, I. Cinel, and D. Avlan Intestinal ischemic preconditioning protects the intestine and reduces bacterial translocation Shock 18 2002 476
63. R.D. Berg Bacterial translocation from the gastrointestinal tract Adv Exp Med Biol 473 1999 11
64. L. Cicalese, P. Sileri, and M. Green Bacterial translocation in clinical intestinal transplantation Transplantation 71 2001 1414
65. D.A. Parks, T.K. Williams, and J.S. Beckman Conversion of xanthine dehydrogenase to oxidase in ischemic rat intestine: a reevaluation Am J Physiol 254 1988 G768
66. D.N. Granger, G. Rutili, and J.M. McCord Role of superoxide radicals in intestinal ischemia Gastroenterology 81 1981 22
67. R. Harrison Structure and function of xanthine oxidoreductase: where are we now? Free Radic Biol Med 33 2002 774
68. D. Cooper, J. Russell, and K.D. Chitman Leukocyte dependence of platelet adhesion in postcapillary venules Am J Physiol Heart Circ Physiol 286 2004 H1895
69. E.M. Mbachu, L.V. Klein, B.B. Rubin, and T.F. Lindsay A monoclonal antibody against cytokine-induced neutrophil chemoattractant attenuates injury in the small intestine in a model of ruptured abdominal aortic aneurysm J Vasc Surg 39 2004 1104
70. S. Nalini, M.M. Mathan, and K.A. Balasubramanian Oxygen free radical induced damage during intestinal ischemia/reperfusion in normal and xanthine oxidase deficient rats Mol Cell Biochem 124 1993 59
71. S. Massberg, A.P. Gonzalez, and R. Leiderer In vivo assessment of the influence of cold preservation time on microvascular reperfusion injury after experimental small bowel transplantation Br J Surg 85 1998 127
72. S.K. Ozel, M. Yuksel, and G. Haklar Nitric oxide and endothelin relationship in intestinal ischemia/reperfusion injury (II) Prostaglandins Leukot Essent Fatty Acids 64 2001 253
73. T. Tsuruma, A. Yagihashi, and T. Matsuno The heat-shock protein 70 family reduces ischemia/reperfusion injury in small intestine Transplant Proc 28 1996 2629
74. S.D. Fleming, B.W. Starnes, and J.G. Kiang Heat stress protection against mesenteric I/R induced alterations in intestinal mucosa in rats J Appl Physiol 92 2002 2600
75. E.W. Albrecht, C.A. Stegeman, and P. Heeringa Protective role of endothelial nitric oxide synthase J Pathol 199 2003 8
76. B. Wu, R. Iwakiri, and S. Tsunada iNOS enhances rat intestinal apoptosis after ischemia-reperfusion Free Radic Biol Med 33 2002 649
77. P. Kubes, and D.M. McCafferty Nitric oxide and intestinal inflammation Am J Med 109 2000 150
78. X.W. Qu, H. Wang, and I.G. De Plaen Neuronal nitric oxide synthase (NOS) regulates the expression of inducible NOS in rat small intestine via modulation of nuclear factor kappa B FASEB J 15 2001 439
79. D.A. Wink, I. Hanbauer, and M.C. Krishna Nitric oxide protects against cellular damage and cytotoxicity from reactive oxygen species Proc Natl Acad Sci U S A 90 1993 9813
80. U. Siebenlist, G. Franzoso, and K. Brown Structure, regulation and function of NF-kappa B Annu Rev Cell Biol 10 1994 405
81. T. Collins, M.A. Read, and A.S. Neish Transcriptional regulation of endothelial cell adhesion molecules: NF-kappa B and cytokine-inducible enhancers FASEB J 9 1995 899
82. P.J. Barnes Nuclear factor-kappa B Int J Biochem Cell Biol 29 1997 867
83. T.S. Blackwell, and J.W. Christman The role of nuclear factor-kappa B in cytokine gene regulation Am J Respir Cell Mol Biol 17 1997 3
84. M. Spiecker, H. Darius, and K. Kaboth Differential regulation of endothelial cell adhesion molecule expression by nitric oxide donors and antioxidants J Leukoc Biol 63 1998 732
85. H.B. Peng, P. Libby, and J.K. Liao Induction and stabilization of I kappa B alpha by nitric oxide mediates inhibition of NF-kappa B J Biol Chem 270 1995 14214
86. B.O. Attuwaybi, R.A. Kozar, and S.D. Moore-Olufemi Heme oxygenase-1 induction by hemin protects against gut ischemia/reperfusion injury J Surg Res 118 2004 53
87. M. Katori, R.W. Busuttil, and J.W. Kupiec-Weglinski Heme oxygenase-1 system in organ transplantation Transplantation 74 2002 905
88. T.J. Vachharajani, J. Work, A.C. Issekutz, and D.N. Granger Heme oxygenase modulates selectin expression in different regional vascular beds Am J Physiol Heart Circ Physiol 278 2000 H1613
89. W.G. Austen Jr., L. Kobzik, and M.C. Carroll The role of complement and natural antibody in intestinal ischemia reperfusion injury Int J Immunopathol Pharmacol 16 2003 1
90. S.A. Gibbs, M.R. Weiser, and L. Kobzik P-selectin mediates intestinal ischemic injury by enhancing complement deposition Surgery 119 1996 652
91. M.C. Montalto, M.L. Hart, and J.E. Jordan Role for complement in mediating intestinal nitric-oxide synthase-2 and superoxide dismutase expression Am J Physiol Gastrointest Liver Physiol 285 2003 G197
92. L.A. Hernandez, M.B. Grisham, and D.N. Granger A role for iron in oxidant-mediated ischemic injury to intestinal microvasculature Am J Physiol 253 1987 G49
93. M.F. Tsan, and B. Gao Endogenous ligands of Toll-like receptors J Leukoc Biol 76 2004 514
94. D.N. Cook, D.S. Pisetsky, and D.A. Schwartz Toll-like receptors in the pathogenesis of human disease Nat Immunol 5 2004 975
95. S.M. Krams, M. Wang, and R.O. Castillo Toll-like receptor 4 contributes to small intestine allograft rejection Transplantation 90 2010 1272
96. A. Hutchings, J. Wu, and C. Asiedu The immune decision toward allograft tolerance in non-human primates requires early inhibition of innate immunity and induction of immune regulation Transpl Immunol 11 2003 335
97. H. He, J.R. Stone, and D.L. Perkins Analysis of differential immune responses induced by innate and adaptive immunity following transplantation Immunology 109 2003 185
98. D. Linfert, T. Chowdhry, and H. Rabb Lymphocytes and ischemia-reperfusion injury Transplant Rev (Orlando) 23 2009 1
99. T. El-Sawy, M. Miura, and R. Fairchild Early T cell response to allografts occurring prior to alloantigen priming up-regulates innate mediated inflammation and graft necrosis Am J Pathol 165 2004 147
100. A.B. Adams, M.A. Williams, and T.R. Jones Heterologous immunity provides a potent barrier to transplantation tolerance J Clin Invest 111 2003 1887