Animal models of chemically induced intestinal inflammation: Predictivity and ethical issues

Pharmacology and Therapeutics

Volumn 139, Issue 1, 2013, Pages 71-86

  Dothel, Giovanni ^a   Vasina, Valentina ^a   Barbara, Giovanni ^a   De Ponti, Fabrizio ^a  

^a UNIVERSITY OF BOLOGNA   (Italy)

Author keywords

Biomarkers; Colitis; Drug development; Endpoints; Inflammatory bowel disease; Translational research

Indexed keywords

ALICAFORSEN; BALSALAZIDE; BETAMETHASONE; BL 7040; BORTEZOMIB; BUDESONIDE; CIPROFLOXACIN; GASTROINTESTINAL AGENT; GI 270384 X; GSK 1605786 A; HYDROCORTISONE; MESALAZINE; METHYLPREDNISOLONE; METRONIDAZOLE; MULTISTEM; NATALIZUMAB; NI 0401; OLSALAZINE; PREDNISONE; PROBIOTIC AGENT; QAX 576; REMESTEMCEL L; RIFAXIMIN; SALAZOSULFAPYRIDINE; TACROLIMUS; TOFACITINIB; UNCLASSIFIED DRUG; UNINDEXED DRUG; USTEKINUMAB; VEDOLIZUMAB; VIDOFLUDIMUS;

AGGRESSION; BEHAVIOR; CAENORHABDITIS ELEGANS; CALLITRICHINAE; CHRONIC DISEASE; CROHN DISEASE; DIARRHEA; DISEASE ACTIVITY; DISEASE MODEL; DNA POLYMORPHISM; DROSOPHILA MELANOGASTER; DRUG BIOAVAILABILITY; ENTERITIS; EXPERIMENTAL DOG; EXPERIMENTAL GUINEA PIG; EXPERIMENTAL MOUSE; EXPERIMENTAL PIG; EXPERIMENTAL RAT; FLUID INTAKE; FOOD INTAKE; GENETIC ENGINEERING; HUMAN; HYPERACTIVITY; IMMUNE SYSTEM; INNATE IMMUNITY; INTESTINE MUCOSA PERMEABILITY; KNOCKOUT GENE; LIPID PEROXIDATION; MEDICAL ETHICS; MICROBIOME; NEUTROPHIL CHEMOTAXIS; NONHUMAN; OCCULT BLOOD; OXIDATIVE STRESS; PATHOPHYSIOLOGY; PREDICTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; RANDOMIZATION; RECTUM HEMORRHAGE; REVIEW; SAMPLE SIZE; SHEEP; SPECIES; TH1 CELL; TH17 CELL; TISSUE INJURY; TRANSGENIC ANIMAL; ULCERATIVE COLITIS; WASTING SYNDROME; WEIGHT REDUCTION; ZEBRA FISH;

ANIMALS; BIOMEDICAL RESEARCH; DISEASE MODELS, ANIMAL; DRUG EVALUATION, PRECLINICAL; HUMANS; INFLAMMATORY BOWEL DISEASES; RESEARCH DESIGN;

EID: 84877922059     PISSN: 01637258     EISSN: 1879016X     Source Type: Journal    
DOI: 10.1016/j.pharmthera.2013.04.005     Document Type: Review

References (145)

1. Agenzia Italiana del Farmaco (AIFA) Guida all'uso dei farmaci 5 2008 Elsevier Masson, L.E.G.O. Lavis (TN), Italy
2. B.O. Ahn, K.H. Ko, T.Y. Oh, H. Cho, W.B. Kim, and K.J. Lee Efficacy of use of colonoscopy in dextran sulfate sodium induced ulcerative colitis in rats: the evaluation of the effects of antioxidant by colonoscopy Int J Colorectal Dis 16 2001 174 181
3. P. Alex, N.C. Zachos, T. Nguyen, L. Gonzales, T.E. Chen, and L.S. Conklin Distinct cytokine patterns identified from multiplex profiles of murine DSS and TNBS-induced colitis Inflamm Bowel Dis 15 2009 341 352
4. C.K. Ameho, A.A. Adjei, E.K. Harrison, K. Takeshita, T. Morioka, and Y. Arakaki Prophylactic effect of dietary glutamine supplementation on interleukin 8 and tumour necrosis factor alpha production in trinitrobenzene sulphonic acid induced colitis Gut 41 1997 487 493
5. G. An Small to large, lots to some, many to few: In silico navigation of the Translational Dilemma Crit Care Med 40 2012 1334 1335
6. C.A. Anderson, G. Boucher, C.W. Lees, A. Franke, M. D'Amato, and K.D. Taylor Meta-analysis identifies 29 additional ulcerative colitis risk loci, increasing the number of confirmed associations to 47 Nat Genet 43 2011 246 252
7. M. Balls The conflict over animal experimentation: Is the field of battle changing? Altern Lab Anim 40 2012 189 191
8. C. Bauer, P. Duewell, C. Mayer, H.A. Lehr, K.A. Fitzgerald, and M. Dauer Colitis induced in mice with dextran sulfate sodium (DSS) is mediated by the NLRP3 inflammasome Gut 59 2010 1192 1199
9. C. Becker, M.C. Fantini, and M.F. Neurath High resolution colonoscopy in live mice Nat Protoc 1 2006 2900 2904
10. Biomarkers Definitions Working Group Biomarkers and surrogate endpoints: preferred definitions and conceptual framework Clin Pharmacol Ther 69 2001 89 95
11. G. Bouma, and W. Strober The immunological and genetic basis of inflammatory bowel disease Nat Rev Immunol 3 2003 521 533
12. D.M. Bouvier, S. Bremer, S. Casati, M. Ceridono, S. Coecke, and R. Corvi ECVAM and new technologies for toxicity testing Adv Exp Med Biol 745 2012 154 180
13. M.J. Brown, and K.A. Murray Phenotyping of genetically engineered mice: Humane, ethical, environmental, and husbandry issues ILAR J 47 2006 118 123
14. J.P. Burke, J.J. Mulsow, C. O'Keane, N.G. Docherty, R.W. Watson, and P.R. O'Connell Fibrogenesis in Crohn's disease Am J Gastroenterol 102 2007 439 448
15. Canadian Council on Animal Care Three Rs: Promoting Awareness, Knowledge and Sensitivity to the Ethics of Animal use http://www.ccac.ca/Documents/ Publications/Resource/Vol-32.pdf 2010 (Accessed on 12/2/2013)
16. Canadian Council on Animal Care Back to Basics: Focusing on the Three Rs and Animal Welfare http://www.ccac.ca/Documents/Publications/Resource/Vol-33.pdf 2011 (Accessed on 12/2/2013)
17. G.G. Cancado, J.A. Fiuza, N.C. de Paiva, L.C. Lemos, N.D. Ricci, and P.H. Gazzinelli-Guimaraes Hookworm products ameliorate dextran sodium sulfate-induced colitis in BALB/c mice Inflamm Bowel Dis 17 2011 2275 2286
18. G.Y. Chen, and G. Nunez Inflammasomes in intestinal inflammation and cancer Gastroenterology 141 2011 1986 1999
19. I.J. Claes, S.C. De Keersmaecker, J. Vanderleyden, and S. Lebeer Lessons from probiotic-host interaction studies in murine models of experimental colitis Mol Nutr Food Res 55 2011 1441 1453
20. I.J. Claes, S. Lebeer, C. Shen, T.L. Verhoeven, E. Dilissen, and H.G. De Impact of lipoteichoic acid modification on the performance of the probiotic Lactobacillus rhamnosus GG in experimental colitis Clin Exp Immunol 162 2010 306 314
21. N. Cook, D.I. Jodrell, and D.A. Tuveson Predictive in vivo animal models and translation to clinical trials Drug Discov Today 17 2012 253 260
22. J. Cooke, H. Zhang, L. Greger, A.L. Silva, D. Massey, and C. Dawson Mucosal genome-wide methylation changes in inflammatory bowel disease Inflamm Bowel Dis 18 2012 2128 2137
23. L.A. Dieleman, B.U. Ridwan, G.S. Tennyson, K.W. Beagley, R.P. Bucy, and C.O. Elson Dextran sulfate sodium-induced colitis occurs in severe combined immunodeficient mice Gastroenterology 107 1994 1643 1652
24. A. Dignass, A.G. Van, J.O. Lindsay, M. Lemann, J. Soderholm, and J.F. Colombel The second European evidence-based Consensus on the diagnosis and management of Crohn's disease: Current management J Crohns Colitis 4 2010 28 62
25. S. Ding, K.L. Walton, R.E. Blue, K. Macnaughton, S.T. Magness, and P.K. Lund Mucosal healing and fibrosis after acute or chronic inflammation in wild type FVB-N mice and C57BL6 procollagen alpha1(I)-promoter-GFP reporter mice PLoS One 7 2012 e42568
26. M.R. Ehrenstein, and C. Mauri If the treatment works, do we need to know why?: The promise of immunotherapy for experimental medicine J Exp Med 204 2007 2249 2252
27. D.E. Elliott, J. Li, A. Blum, A. Metwali, K. Qadir, and J.F. Urban Jr. Exposure to schistosome eggs protects mice from TNBS-induced colitis Am J Physiol Gastrointest Liver Physiol 284 2003 G385 G391
28. C.O. Elson, Y. Cong, S. Brandwein, C.T. Weaver, R.P. Mccabe, and M. Mahler Experimental models to study molecular mechanisms underlying intestinal inflammation Ann N Y Acad Sci 859 1998 85 95
29. C.O. Elson, R.B. Sartor, G.S. Tennyson, and R.H. Riddell Experimental models of inflammatory bowel disease Gastroenterology 109 1995 1344 1367
30. European Council Council Directive of 24 November 1986 on the approximation of laws, regulations and administrative provisions of the Member States regarding the protections of animals used for experimental and other scientific purposes 1986 (Accessed on 11/2/2013)
31. European Medicines Agency European Medicines Agency http://www.ema. europa.eu/ema/index.jsp?curl=pages/medicines/landing/epar-search.jsp&mid= WC0b01ac058001d124 2012 (Accessed on 15/10/2012)
32. European Parliament and Council Directive 2010/63/EU of the European Parliament and of the Council on the protection of animals used for scientific purposes 2010 (Accessed on 11/2/2013)
33. S. Fichtner-Feigl, C.A. Young, A. Kitani, E.K. Geissler, H.J. Schlitt, and W. Strober IL-13 signaling via IL-13R alpha2 induces major downstream fibrogenic factors mediating fibrosis in chronic TNBS colitis Gastroenterology 135 2003-13 2008 2013
34. G.A. Fitzgerald Opinion: anticipating change in drug development: The emerging era of translational medicine and therapeutics Nat Rev Drug Discov 4 2005 815 818
35. L.R. Fitzpatrick, L. Deml, C. Hofmann, J.S. Small, M. Groeppel, and S. Hamm 4SC-101, a novel immunosuppressive drug, inhibits IL-17 and attenuates colitis in two murine models of inflammatory bowel disease Inflamm Bowel Dis 16 2010 1763 1777
36. L.R. Fitzpatrick, K. Meirelles, J.S. Small, F.J. Puleo, W.A. Koltun, and R.N. Cooney A new model of chronic hapten-induced colitis in young rats J Pediatr Gastroenterol Nutr 50 2010 240 250
37. I.J. Fuss, F. Heller, M. Boirivant, F. Leon, M. Yoshida, and S. Fichtner-Feigl Nonclassical CD1d-restricted NK T cells that produce IL-13 characterize an atypical Th2 response in ulcerative colitis J Clin Invest 113 2004 1490 1497
38. I.J. Fuss, M. Neurath, M. Boirivant, J.S. Klein, M.C. de la, and S.A. Strong Disparate CD4+ lamina propria (LP) lymphokine secretion profiles in inflammatory bowel disease. Crohn's disease LP cells manifest increased secretion of IFN-gamma, whereas ulcerative colitis LP cells manifest increased secretion of IL-5 J Immunol 157 1996 1261 1270
39. M.S. Geier, R.N. Butler, P.M. Giffard, and G.S. Howarth Lactobacillus fermentum BR11, a potential new probiotic, alleviates symptoms of colitis induced by dextran sulfate sodium (DSS) in rats Int J Food Microbiol 114 2007 267 274
40. S.F. Ghasemi-Niri, A.H. Abdolghaffari, S. Fallah-Benakohal, M. Hosseinpour-Feizi, P. Mahdaviani, and H. Jamalifar On the benefit of whey-cultured Lactobacillus casei in murine colitis J Physiol Pharmacol 62 2011 341 346
41. Y. Gong, J.K. Barbay, A.B. Dyatkin, T.A. Miskowski, E.S. Kimball, and S.M. Prouty Synthesis and biological evaluation of novel pyridazinone-based alpha4 integrin receptor antagonists J Med Chem 49 2006 3402 3411
42. A. Goto, Y. Arimura, Y. Shinomura, K. Imai, and Y. Hinoda Antisense therapy of MAdCAM-1 for trinitrobenzenesulfonic acid-induced murine colitis Inflamm Bowel Dis 12 2006 758 765
43. J. Gottfries, S. Melgar, and E. Michaelsson Modelling of mouse experimental colitis by global property screens: A holistic approach to assess drug effects in inflammatory bowel disease PLoS One 7 2012 e30005
44. L.J. Hall, E. Faivre, A. Quinlan, F. Shanahan, K. Nally, and S. Melgar Induction and activation of adaptive immune populations during acute and chronic phases of a murine model of experimental colitis Dig Dis Sci 56 2011 79 89
45. N. Hamamoto, K. Maemura, I. Hirata, M. Murano, S. Sasaki, and K. Katsu Inhibition of dextran sulphate sodium (DSS)-induced colitis in mice by intracolonically administered antibodies against adhesion molecules (endothelial leucocyte adhesion molecule-1 (ELAM-1) or intercellular adhesion molecule-1 (ICAM-1)) Clin Exp Immunol 117 1999 462 468
46. J. Hampe, A. Franke, P. Rosenstiel, A. Till, M. Teuber, and K. Huse A genome-wide association scan of nonsynonymous SNPs identifies a susceptibility variant for Crohn disease in ATG16L1 Nat Genet 39 2007 207 211
47. R. Hansen, J.M. Thomson, E.M. El-Omar, and G.L. Hold The role of infection in the aetiology of inflammatory bowel disease J Gastroenterol 45 2010 266 276
48. L.E. Harrington, P.R. Mangan, and C.T. Weaver Expanding the effector CD4 T-cell repertoire: The Th17 lineage Curr Opin Immunol 18 2006 349 356
49. M. Heath Training and competency of laboratory animal science staff in keeping with the 2010/63/EU Directive Lab Anim Europe 12 2012
50. T. Hisamatsu, T. Kanai, Y. Mikami, K. Yoneno, K. Matsuoka, and T. Hibi Immune aspects of the pathogenesis of inflammatory bowel disease Pharmacol Ther 137 2013 283 297
51. J.C. Hoffmann, N.N. Pawlowski, A.A. Kuhl, W. Hohne, and M. Zeitz Animal models of inflammatory bowel disease: An overview Pathobiology 70 2002 121 130
52. E.H. Huang, J.J. Carter, R.L. Whelan, Y.H. Liu, J.O. Rosenberg, and H. Rotterdam Colonoscopy in mice Surg Endosc 16 2002 22 24
53. S. Inoue, H. Nakase, M. Matsuura, S. Mikami, S. Ueno, and N. Uza The effect of proteasome inhibitor MG132 on experimental inflammatory bowel disease Clin Exp Immunol 156 2009 172 182
54. S. Ishihara, M.M. Aziz, T. Yuki, H. Kazumori, and Y. Kinoshita Inflammatory bowel disease: Review from the aspect of genetics J Gastroenterol 44 2009 1097 1108
55. A.R. Jurjus, N.N. Khoury, and J.M. Reimund Animal models of inflammatory bowel disease J Pharmacol Toxicol Methods 50 2004 81 92
56. T.V. Kalima, H. Saloniemi, and T. Rahko Experimental regional enteritis in pigs Scand J Gastroenterol 11 1976 353 362
57. N.C. Keramaris, N.K. Kanakaris, C. Tzioupis, G. Kontakis, and P.V. Giannoudis Translational research: From benchside to bedside Injury 39 2008 643 650
58. C. Kilkenny, W.J. Browne, I.C. Cuthill, M. Emerson, and D.G. Altman Improving bioscience research reporting: The ARRIVE guidelines for reporting animal research PLoS Biol 8 2010 e1000412
59. C.J. Kim, J.A. Kovacs-Nolan, C. Yang, T. Archbold, M.Z. Fan, and Y. Mine l-Tryptophan exhibits therapeutic function in a porcine model of dextran sodium sulfate (DSS)-induced colitis J Nutr Biochem 21 2010 468 475
60. Y.S. Kim, M.H. Lee, A.S. Ju, and K.J. Rhee Th17 responses are not induced in dextran sodium sulfate model of acute colitis Immune Netw 11 2011 416 419
61. I. Koboziev, F. Karlsson, S. Zhang, and M.B. Grisham Pharmacological intervention studies using mouse models of the inflammatory bowel diseases: Translating preclinical data into new drug therapies Inflamm Bowel Dis 17 2011 1229 1245
62. H. Laroui, S.A. Ingersoll, H.C. Liu, M.T. Baker, S. Ayyadurai, and M.A. Charania Dextran sodium sulfate (DSS) induces colitis in mice by forming nano-lipocomplexes with medium-chain-length fatty acids in the colon PLoS One 7 2012 e32084
63. G. Latella, A. Vetuschi, R. Sferra, G. Zanninelli, A. D'Angelo, and V. Catitti Smad3 loss confers resistance to the development of trinitrobenzene sulfonic acid-induced colorectal fibrosis Eur J Clin Invest 39 2009 145 156
64. I.C. Lawrance, F. Wu, A.Z. Leite, J. Willis, G.A. West, and C. Fiocchi A murine model of chronic inflammation-induced intestinal fibrosis down-regulated by antisense NF-kappa B Gastroenterology 125 2003 1750 1761
65. E.G. Lee, D.L. Boone, S. Chai, S.L. Libby, M. Chien, and J.P. Lodolce Failure to regulate TNF-induced NF-kappaB and cell death responses in A20-deficient mice Science 289 2000 2350 2354
66. M. Leenaars, C.R. Hooijmans, N. van V., G. ter R., M. Leeflang, and L. Hooft A step-by-step guide to systematically identify all relevant animal studies Lab Anim 46 2012 24 31
67. R.E. Ley, P.J. Turnbaugh, S. Klein, and J.I. Gordon Microbial ecology: Human gut microbes associated with obesity Nature 444 2006 1022 1023
68. V.S. Li, and H. Clevers In vitro expansion and transplantation of intestinal crypt stem cells Gastroenterology 143 2012 30 34
69. J. Lin, and D.J. Hackam Worms, flies and four-legged friends: The applicability of biological models to the understanding of intestinal inflammatory diseases Dis Model Mech 4 2011 447 456
70. Holm T. Lindebo, S.S. Poulsen, H. Markholst, and S. Reedtz-Runge Pharmacological evaluation of the SCID T cell transfer model of colitis: As a model of Crohn's disease Int J Inflamm 2012 2012 1 11
71. M.D. Lindner Clinical attrition due to biased preclinical assessments of potential efficacy Pharmacol Ther 115 2007 148 175
72. E.V. Loftus Jr. Clinical epidemiology of inflammatory bowel disease: Incidence, prevalence, and environmental influences Gastroenterology 126 2004 1504 1517
73. P.K. Lund, and C.C. Zuniga Intestinal fibrosis in human and experimental inflammatory bowel disease Curr Opin Gastroenterol 17 2001 318 323
74. M. Mahler, I.J. Bristol, E.H. Leiter, A.E. Workman, E.H. Birkenmeier, and C.O. Elson Differential susceptibility of inbred mouse strains to dextran sulfate sodium-induced colitis Am J Physiol 274 1998 G544 G551
75. E.A. Mayer, and S.M. Collins Evolving pathophysiologic models of functional gastrointestinal disorders Gastroenterology 122 2002 2032 2048
76. S. Melgar, A. Karlsson, and E. Michaelsson Acute colitis induced by dextran sulfate sodium progresses to chronicity in C57BL/6 but not in BALB/c mice: Correlation between symptoms and inflammation Am J Physiol Gastrointest Liver Physiol 288 2005 G1328 G1338
77. S. Melgar, L. Karlsson, E. Rehnstrom, A. Karlsson, H. Utkovic, and L. Jansson Validation of murine dextran sulfate sodium-induced colitis using four therapeutic agents for human inflammatory bowel disease Int Immunopharmacol 8 2008 836 844
78. J. Mestas, and C.C. Hughes Of mice and not men: Differences between mouse and human immunology J Immunol 172 2004 2731 2738
79. Q. Mi, N.Y. Li, C. Ziraldo, A. Ghuma, M. Mikheev, and R. Squires Translational systems biology of inflammation: Potential applications to personalized medicine Per Med 7 2010 549 559
80. S.C. Ming, and H. Goldman Ulcerative colitis and Crohn's disease S.C. Ming, H. Goldman, Pathology of the gastrointestinal tract 1998 Lippincott Williams & Wilkins Philadelphia, PA 1020
81. A. Mizoguchi Animal models of inflammatory bowel disease Prog Mol Biol Transl Sci 105 2012 263 320
82. A. Mizoguchi, and E. Mizoguchi Animal models of IBD: Linkage to human disease Curr Opin Pharmacol 10 2010 578 587
83. A. Mizoguchi, E. Mizoguchi, and A.K. Bhan Immune networks in animal models of inflammatory bowel disease Inflamm Bowel Dis 9 2003 246 259
84. G.P. Morris, P.L. Beck, M.S. Herridge, W.T. Depew, M.R. Szewczuk, and J.L. Wallace Hapten-induced model of chronic inflammation and ulceration in the rat colon Gastroenterology 96 1989 795 803
85. P.J. Morrissey, K. Charrier, S. Braddy, D. Liggitt, and J.D. Watson CD4+ T cells that express high levels of CD45RB induce wasting disease when transferred into congenic severe combined immunodeficient mice. Disease development is prevented by cotransfer of purified CD4+ T cells J Exp Med 178 1993 237 244
86. C. Mowat, A. Cole, A. Windsor, T. Ahmad, I. Arnott, and R. Driscoll Guidelines for the management of inflammatory bowel disease in adults Gut 60 2011 571 607
87. N.A. Nagalingam, J.Y. Kao, and V.B. Young Microbial ecology of the murine gut associated with the development of dextran sodium sulfate-induced colitis Inflamm Bowel Dis 17 2011 917 926
88. NC3Rs Systematic reviews of animal research 2012 (Accessed on 18/12/2012)
89. A. Negaard, E.M. Loberg, P.A. Naess, M. Eriksen, and N.E. Klow Feasibility of MRI in experimentally induced inflammatory small bowel disease: A pilot study in a porcine model Dig Dis Sci 55 2010 14 20
90. Nuffield Council on Bioethics The ethics of research involving animals 2005 Nuffield Council on Bioethics London (http://www.nuffieldbioethics.org/ animal-research. Accessed on 18-12-2012)
91. W.T. O'Connor, A. Smyth, and M.D. Gilchrist Animal models of traumatic brain injury: A critical evaluation Pharmacol Ther 130 2011 106 113
92. Y. Okada, N. Maeda, S. Takakura, K. Miyata, and M. Koshiba Tacrolimus ameliorates dextran sulfate sodium-induced colitis in mice: Implication of interferon-gamma and interleukin-1beta suppression Biol Pharm Bull 34 2011 1823 1827
93. S. Onoue, N. Igarashi, S. Yamada, and Y. Tsuda High-throughput reactive oxygen species (ROS) assay: An enabling technology for screening the phototoxic potential of pharmaceutical substances J Pharm Biomed Anal 46 2008 187 193
94. J.J. O'Shea, and W.E. Paul Mechanisms underlying lineage commitment and plasticity of helper CD4+ T cells Science 327 2010 1098 1102
95. J. Panes, M. Aceituno, F. Gil, R. Miquel, J.M. Pique, and A. Salas Efficacy of an inhibitor of adhesion molecule expression (GI270384X) in the treatment of experimental colitis Am J Physiol Gastrointest Liver Physiol 293 2007 G739 G748
96. M. Perse, and A. Cerar Dextran sodium sulphate colitis mouse model: Traps and tricks J Biomed Biotechnol 2012 2012 718617
97. S.E. Plevy, and S.R. Targan Future therapeutic approaches for inflammatory bowel diseases Gastroenterology 140 2011 1838 1846
98. D.K. Podolsky The current future understanding of inflammatory bowel disease Best Pract Res Clin Gastroenterol 16 2002 933 943
99. P.R. Pouillart, F. Depeint, A. Abdelnour, L. Deremaux, O. Vincent, and J.C. Maziere Nutriose, a prebiotic low-digestible carbohydrate, stimulates gut mucosal immunity and prevents TNBS-induced colitis in piglets Inflamm Bowel Dis 16 2010 783 794
100. P. Pound, S. Ebrahim, P. Sandercock, M.B. Bracken, and I. Roberts Where is the evidence that animal research benefits humans? BMJ 328 2004 514 517
101. F. Powrie, M.W. Leach, S. Mauze, S. Menon, L.B. Caddle, and R.L. Coffman Inhibition of Th1 responses prevents inflammatory bowel disease in scid mice reconstituted with CD45RBhi CD4+ T cells Immunity 1 1994 553 562
102. F. Rieder, S. Kessler, M. Sans, and C. Fiocchi Animal models of intestinal fibrosis: New tools for the understanding of pathogenesis and therapy of human disease Am J Physiol Gastrointest Liver Physiol 303 2012 G786 G801
103. W.M.S. Russell, and R.L. Burch The principles of humane experimental technique 1959 Methuen & Co. Ltd. London
104. F. Sams-Dodd Strategies to optimize the validity of disease models in the drug discovery process Drug Discov Today 11 2006 355 363
105. G.J. Sanger, J.D. Holbrook, and P.L. Andrews The translational value of rodent gastrointestinal functions: A cautionary tale Trends Pharmacol Sci 32 2011 402 409
106. A. Santana, C. Medina, M.C. Paz-Cabrera, F. Diaz-Gonzalez, E. Farre, and A. Salas Attenuation of dextran sodium sulphate induced colitis in matrix metalloproteinase-9 deficient mice World J Gastroenterol 12 2006 6464 6472
107. F. Scheiffele, and I.J. Fuss Induction of TNBS colitis in mice Curr Protoc Immunol Chapter 15 2002 (Unit)
108. A. Schirbel, and C. Fiocchi Inflammatory bowel disease: Established and evolving considerations on its etiopathogenesis and therapy J Dig Dis 11 2010 266 276
109. N. Schmidt, E. Gonzalez, A. Visekruna, A.A. Kuhl, C. Loddenkemper, and H. Mollenkopf Targeting the proteasome: partial inhibition of the proteasome by bortezomib or deletion of the immunosubunit LMP7 attenuates experimental colitis Gut 59 2010 896 906
110. S.Z. Sheikh, and S.E. Plevy The role of the macrophage in sentinel responses in intestinal immunity Curr Opin Gastroenterol 26 2010 578 582
111. W. Shen, and S.K. Durum Synergy of IL-23 and Th17 cytokines: New light on inflammatory bowel disease Neurochem Res 35 2010 940 946
112. X.Z. Shi, J.H. Winston, and S.K. Sarna Differential immune and genetic responses in rat models of Crohn's colitis and ulcerative colitis Am J Physiol Gastrointest Liver Physiol 300 2011 G41 G51
113. B. Siegmund, and M. Zeitz Innate and adaptive immunity in inflammatory bowel disease World J Gastroenterol 17 2011 3178 3183
114. E.F. Stange, S.P. Travis, S. Vermeire, W. Reinisch, K. Geboes, and A. Barakauskiene European evidence-based Consensus on the diagnosis and management of ulcerative colitis: Definitions and diagnosis J Crohns Colitis 2 2008 1 23
115. C.S. Stevenson, and M.A. Birrell Moving towards a new generation of animal models for asthma and COPD with improved clinical relevance Pharmacol Ther 130 2011 93 105
116. W. Strober, and I.J. Fuss Proinflammatory cytokines in the pathogenesis of inflammatory bowel diseases Gastroenterology 140 2011 1756 1767
117. W. Strober, I. Fuss, and P. Mannon The fundamental basis of inflammatory bowel disease J Clin Invest 117 2007 514 521
118. K. Suzuki, X. Sun, M. Nagata, T. Kawase, H. Yamaguchi, and V. Sukumaran Analysis of intestinal fibrosis in chronic colitis in mice induced by dextran sulfate sodium Pathol Int 61 2011 228 238
119. A. Swidsinski, V. Loening-Baucke, M. Vaneechoutte, and Y. Doerffel Active Crohn's disease and ulcerative colitis can be specifically diagnosed and monitored based on the biostructure of the fecal flora Inflamm Bowel Dis 14 2008 147 161
120. H. Szabo, G. Fiorino, A. Spinelli, S. Rovida, A. Repici, and A.C. Malesci Review article: anti-fibrotic agents for the treatment of Crohn's disease - Lessons learnt from other diseases Aliment Pharmacol Ther 31 2010 189 201
121. A.A. te Velde, M.I. Verstege, and D.W. Hommes Critical appraisal of the current practice in murine TNBS-induced colitis Inflamm Bowel Dis 12 2006 995 999
122. S.P. Travis, E.F. Stange, M. Lemann, T. Oresland, W.A. Bemelman, and Y. Chowers European evidence-based consensus on the management of ulcerative colitis: Current management J Crohns Colitis 2 2008 24 62
123. F.M. Uckun, H. Tibbles, Z. Ozer, S. Qazi, and A. Vassilev Anti-inflammatory activity profile of JANEX-1 in preclinical animal models Bioorg Med Chem 16 2008 1287 1298
124. B.A. Vallance, M.I. Gunawan, B. Hewlett, P. Bercik, K.C. Van, and F. Galeazzi TGF-beta1 gene transfer to the mouse colon leads to intestinal fibrosis Am J Physiol Gastrointest Liver Physiol 289 2005 G116 G128
125. A.G. Van, A. Dignass, J. Panes, L. Beaugerie, J. Karagiannis, and M. Allez The second European evidence-based Consensus on the diagnosis and management of Crohn's disease: Definitions and diagnosis J Crohns Colitis 4 2010 7 27
126. Various authors Biomarkers and Surrogate Endpoints: Clinical Research and Applications 2000 Elsevier Amsterdam
127. Various authors DRUGDEX® System http://www.thomsonhc.com/home/ dispatch 2012 Accessed on 15/10/2012a
128. Various authors Farmadati http://www.farmadati.it/ 2012 (Accessed on 15/10/2012b)
129. V. Vasina, E. Abu-Gharbieh, G. Barbara, R. De Giorgio, R. Colucci, and C. Blandizzi The beta3-adrenoceptor agonist SR58611A ameliorates experimental colitis in rats Neurogastroenterol Motil 20 2008 1030 1041
130. W. Vermeulen, J.G. De Man, S. Nullens, P.A. Pelckmans, B.Y. De Winter, and T.G. Moreels The use of colonoscopy to follow the inflammatory time course of TNBS colitis in rats Acta Gastroenterol Belg 74 2011 304 311
131. A.C. Villani, M. Lemire, E. Louis, M.S. Silverberg, C. Collette, and G. Fortin Genetic variation in the familial Mediterranean fever gene (MEFV) and risk for Crohn's disease and ulcerative colitis PLoS One 4 2009 e7154
132. J.L. Wallace, and C.M. Keenan An orally active inhibitor of leukotriene synthesis accelerates healing in a rat model of colitis Am J Physiol 258 1990 G527 G534
133. J.L. Wallace, T. Le, L. Carter, C.B. Appleyard, and P.L. Beck Hapten-induced chronic colitis in the rat: Alternatives to trinitrobenzene sulfonic acid J Pharmacol Toxicol Methods 33 1995 237 239
134. M. Wehling Assessing the translatability of drug projects: What needs to be scored to predict success? Nat Rev Drug Discov 8 2009 541 546
135. D.J. Wells Animal welfare and the 3Rs in European biomedical research Ann N Y Acad Sci 1245 2011 14 16
136. A. Wendler, and M. Wehling The translatability of animal models for clinical development: Biomarkers and disease models Curr Opin Pharmacol 10 2010 601 606
137. A. Wendler, and M. Wehling Translatability scoring in drug development: Eight case studies J Transl Med 10 2012 1 11
138. S. Wirtz, C. Neufert, B. Weigmann, and M.F. Neurath Chemically induced mouse models of intestinal inflammation Nat Protoc 2 2007 541 546
139. P.A. Wood Phenotype assessment: Are you missing something? Comp Med 50 2000 12 15
140. F. Wu, and S. Chakravarti Differential expression of inflammatory and fibrogenic genes and their regulation by NF-kappaB inhibition in a mouse model of chronic colitis J Immunol 179 2007 6988 7000
141. M.A. Wurbel, M.G. McIntire, P. Dwyer, and E. Fiebiger CCL25/CCR9 interactions regulate large intestinal inflammation in a murine model of acute colitis PLoS One 6 2011 e16442
142. R.J. Xavier, and D.K. Podolsky Unravelling the pathogenesis of inflammatory bowel disease Nature 448 2007 427 434
143. T. Yabana, Y. Arimura, H. Tanaka, A. Goto, M. Hosokawa, and K. Nagaishi Enhancing epithelial engraftment of rat mesenchymal stem cells restores epithelial barrier integrity J Pathol 218 2009 350 359
144. Y. Yan, V. Kolachala, G. Dalmasso, H. Nguyen, H. Laroui, and S.V. Sitaraman Temporal and spatial analysis of clinical and molecular parameters in dextran sodium sulfate induced colitis PLoS One 4 2009 e6073
145. M.Y. Zhu, Y.M. Lu, Y.X. Ou, H.Z. Zhang, and W.X. Chen Dynamic progress of 2,4,6-trinitrobenzene sulfonic acid induced chronic colitis and fibrosis in rat model J Dig Dis 13 2012 421 429