The development of animal models for the study of necrotizing enterocolitis

DMM Disease Models and Mechanisms

Volumn 1, Issue 2-3, 2008, Pages 94-98

  Sodhi, Chhinder ^a,b   Richardson, Ward ^a,b   Gribar, Steven ^a,b   Hackam, David J ^a,b  

^a CHILDREN S HOSPITAL OF PITTSBURGH   (United States)

^b UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA TOCOPHEROL; ARGININE; CAPTOPRIL; GRANULOCYTE COLONY STIMULATING FACTOR; HYDROCORTISONE; INTESTINAL TREFOIL FACTOR; PENTOXIFYLLINE; POLYUNSATURATED FATTY ACID;

CAUSE OF DEATH; DISABILITY; HISTOPATHOLOGY; MULTIPLE ORGAN FAILURE; NECROTIZING ENTEROCOLITIS; NONHUMAN; PATHOGENESIS; PIGLET; PREMATURITY; PRIORITY JOURNAL; REVIEW; SEPSIS; TUBE FEEDING; ANIMAL; DISEASE MODEL; HUMAN; NEWBORN; NEWBORN DISEASE; PATHOPHYSIOLOGY;

ANIMALIA;

ANIMALS; DISEASE MODELS, ANIMAL; ENTEROCOLITIS, NECROTIZING; HUMANS; INFANT, NEWBORN; INFANT, NEWBORN, DISEASES; INFANT, PREMATURE;

EID: 64249145652     PISSN: 17548403     EISSN: 17548411     Source Type: Journal    
DOI: 10.1242/dmm.000315     Document Type: Review

References (56)

1. Anand, R. J., Leaphart, C. L., Mollen, K. P. and Hackam, D. J. (2007). The role of the intestinal barrier in the pathogenesis of necrotizing enterocolitis. Shock 27, 124-133. (Pubitemid 46105827)
2. Anttila, A., Kauppinen, H., Koivusalo, A., Heikkila, P., Savilahti, E. and Rintala, R. (2003). T-cell-mediated mucosal immunity is attenuated in experimental necrotizing enterocolitis. Pediatr. Surg. Int. 19, 326-330. (Pubitemid 37046191)
3. Baregamian, N., Rychahou, P., Hawkins, H. K., Evers, B. M. and Chung, D. H. (2007). Phosphatidylinositol 3-kinase pathway regulates hypoxia-inducible factor-1 to protect from intestinal injury during necrotizing enterocolitis. Surgery 142, 295-302. (Pubitemid 47198681)
4. Barlow, B. and Santulli, T. V. (1975). Importance of multiple episodes of hypoxia or cold stress on the development of enterocolitis in an animal model. Surgery 77, 687-690.
5. Blakely, M. L., Lally, K. P., McDonald, S., Brown, R. L., Barnhart, D. C., Ricketts, R. R., Thompson, W. R., Scherer, L. R., Klein, M. D., Letton, R. W. et al. (2005). Postoperative outcomes of extremely low birth-weight infants with necrotizing enterocolitis or isolated intestinal perforation: a prospective cohort study by the NICHD Neonatal Research Network. Ann. Surg. 241, 984-989; discussion 989-994. (Pubitemid 40733974)
6. Cadir, F. O., Bicakci, U., Tander, B., Kilicoglu-Aydin, B., Rizalar, R., Ariturk, E., Aydin, O. and Bernay, F. (2008). Protective effects of vitamin E and omeprazole on the hypoxia/reoxygenation induced intestinal injury in newborn rats. Pediatr. Surg. Int. 24, 809-813.
7. Canpolat, F. E., Yurdakök, M., Ozsoy, S., Haziroglu, R. and Korkmaz, A. (2006). Protective effects of recombinant human granulocyte colony stimulating factor in a rat model of necrotizing enterocolitis. Pediatr. Surg. Int. 22, 719-723. (Pubitemid 44341721)
8. Caplan, M., Miller-Catchpole, R., Kaup, S., Russell, T., Lickerman, M., Amer, M., Xiao, Y. and Thomson, R., Jr (1999). Bifidobacterial supplementation reduces the incidence of necrotizing enterocolitis in a neonatal rat model. Gastroenterology 117, 577-583.
9. Caplan, M. S., Hedlund, E., Adler, L. and Hsueh, W. (1994). Role of asphyxia and feeding in a neonatal rat model of necrotizing enterocolitis. Pediatr. Pathol. 14, 1017-1028. (Pubitemid 24357149)
10. Caplan, M. S., Lickerman, M., Adler, L., Dietsch, G. N. and Yu, A. (1997). The role of recombinant platelet-activating factor acetylhydrolase in a neonatal rat model of necrotizing enterocolitis. Pediatr. Res. 42, 779-783. (Pubitemid 27509535)
11. Carrasco, R., Pera, M., May, F. E., Westley, B. R., Martinez, A. and Morales, L. (2004). Trefoil factor family peptide 3 prevents the development and promotes healing of ischemia-reperfusion injury in weanling rats. J. Pediatr. Surg. 39, 1693-1700. (Pubitemid 39488001)
12. Cetin, S., Ford, H. R., Sysko, L. R., Agarwal, C., Wang, J., Neal, M. D., Baty, C., Apodaca, G. and Hackam, D. J. (2004). Endotoxin inhibits intestinal epithelial restitution through activation of Rho-GTPase and increased focal adhesions. J. Biol. Chem. 279, 24592-24600. (Pubitemid 38725326)
13. Cetin, S., Leaphart, C. L., Li, J., Ischenko, I., Hayman, M., Upperman, J., Zamora, R., Watkins, S., Ford, H. R., Wang, J. et al. (2007). Nitric oxide inhibits enterocyte migration through activation of RhoA-GTPase in a SHP-2-dependent manner. Am. J. Physiol. Gastrointest. Liver Physiol. 292, G1347-G1358. (Pubitemid 47084651)
14. Ceylan, H., Yüncü, M., Gürel, A., Armutçu, F., Gergerlioglu, H. S., Bagci, C. and Demiryürek, A. T. (2005). Effects of whole-body hypoxic preconditioning on hypoxia/reoxygenation-induced intestinal injury in newborn rats. Eur. J. Pediatr. Surg. 15, 325-332.
15. Cintra, A. E., Martins, J., Patrício, F. R., Higa, E. M. and Montero, E. F. (2008). Nitric oxide levels in the intestines of mice submitted to ischemia and reperfusion: L-arginine effects. Transplant. Proc. 40, 830-835. (Pubitemid 351608648)
16. Cohen, I. T., Nelson, S., Moxley, R. A., Hirsh, M. P., Counihan, T. C. and Martin, R. F. (1991). Necrotizing enterocolitis in a neonatal piglet model. J. Pediatr. Surg. 26, 598-601.
17. Crissinger, K. D., Burney, D., Velasquez, O. R. and Gonzalez, E. (1994). An animal model of necrotizing enterocolitis induced by infant formula and ischemia in developing piglets. Gastroenterology 106, 1215-1222. (Pubitemid 24129237)
18. De Plaen, I. G., Liu, S., Tian, R., Neequaye, I., May, M. J., Han, X. B., Hsueh, W., Jilling, T., Lu, J. and Caplan, M. S. (2007). Inhibition of nuclear factor-kappaB ameliorates bowel injury and prolongs survival in a neonatal rat model of necrotizing enterocolitis. Pediatr. Res. 61, 716-721. (Pubitemid 46800282)
19. Di Lorenzo, M., Bass, J. and Krantis, A. (1995a). An intraluminal model of necrotizing enterocolitis in the developing neonatal piglet. J. Pediatr. Surg. 30, 1138-1142.
20. Di Lorenzo, M., Bass, J. and Krantis, A. (1995b). Use of L-arginine in the treatment of experimental necrotizing enterocolitis. J. Pediatr. Surg. 30, 235-240.
21. Dimmitt, R. A., Glew, R., Colby, C., Brindle, M., Skarsgard, E. and Moss, R. L. (2003). Serum cytosolic beta-glucosidase activity in a rat model of necrotizing enterocolitis. Pediatr. Res. 54, 462-465. (Pubitemid 37159113)
22. Dvorak, B., Halpern, M., Holubec, H., Williams, C. S., McWilliam, D. L., Dominguez, J. A., Stepankova, R., Payne, C. M. and McCuskey, R. S. (2002). Epidermal growth factor reduces the development of necrotizing enterocolitis in a neonatal rat model. Am. J. Physiol. Gastrointest. Liver Physiol. 282, G156-G164. (Pubitemid 34650110)
23. Dvorak, B., Halpern, M., Holubec, H., Dvorakova, K., Dominguez, J. A., Williams, C. S., Meza, Y. G., Kozakova, H. and McCuskey, R. S. (2003). Maternal milk reduces severity of necrotizing enterocolitis and increases intestinal IL-10 in a neonatal rat model. Pediatr. Res. 53, 426-433. (Pubitemid 36237397)
24. Ewer, A. K., Al-Salti, W., Coney, A. M., Marshall, J. M., Ramani, P. and Booth, I. W. (2004). The role of platelet activating factor in a neonatal piglet model of necrotising enterocolitis. Gut 53, 207-213. (Pubitemid 38125507)
25. Feng, J., El-Assal, O. N. and Besner, G. E. (2005). Heparin-binding EGF-like growth factor (HB-EGF) and necrotizing enterocolitis. Semin. Pediatr. Surg. 14, 167-174. (Pubitemid 41111603)
26. Feng, J., El-Assal, O. N. and Besner, G. E. (2006). Heparin-binding epidermal growth factor-like growth factor decreases the incidence of necrotizing enterocolitis in neonatal rats. J. Pediatr. Surg. 41, 144-149. (Pubitemid 43067508)
27. Frost, B. L., Jilling, T. and Caplan, M. S. (2008). The importance of pro-inflammatory signaling in neonatal necrotizing enterocolitis. Semin. Perinatol. 32, 100-106.
28. Grave, G. D., Nelson, S., Walker, W. A., Moss, R. L., Dvorak, B., Hamilton, F. A., Higgins, R. and Raju, T. N. (2007). New therapies and preventive approaches for necrotizing enterocolitis: report of a research planning workshop. Pediatr. Res. 62, 510-514. (Pubitemid 47476215)
29. Gribar, S. C., Anand, R., Sodhi, C. P. and Hackam, D. J. (2008). The role of epithelial Toll-like receptor signaling in the pathogenesis of intestinal inflammation. J. Leukoc. Biol. 83, 493-498. (Pubitemid 351966856)
30. Guthmann, F. and Kluthe, C. (2007). Intestinal trefoil factor in treatment of neonatal necrotizing enterocolitis in the rat model. J. Perinat. Med. 35, 556. (Pubitemid 350219130)
31. Halpern, M. D., Clark, J., Saunders, T. A., Doelle, S. M., Hosseini, D. M., Stagner, A. M. and Dvorak, B. (2006). Reduction of experimental necrotizing enterocolitis with anti-TNF-alpha. Am. J. Physiol. Gastrointest. Liver Physiol. 290, G757-G764.
32. Halpern, M. D., Khailova, L., Molla-Hosseini, D., Arganbright, K., Reynolds, C., Yajima, M., Hoshiba, J. and Dvorak, B. (2008). Decreased development of necrotizing enterocolitis in IL-18-deficient mice. Am. J. Physiol. Gastrointest. Liver Physiol. 294, G20-G26.
33. Henry, M. C. and Moss, R. L. (2005). Surgical therapy for necrotizing enterocolitis: bringing evidence to the bedside. Semin. Pediatr. Surg. 14, 181-190.
34. Henry, M. C. and Moss, R. L. (2008). Neonatal necrotizing enterocolitis. Semin. Pediatr. Surg. 17, 98-109.
35. Hsueh, W., Caplan, M. S., Qu, X. W., Tan, X. D., De Plaen, I. G. and Gonzalez-Crussi, F. (2003). Neonatal necrotizing enterocolitis: clinical considerations and pathogenetic concepts. Pediatr. Dev. Pathol. 6, 6-23. (Pubitemid 36323623)
36. Israel, E. J., Shiffrin, E., Carter, E. A., Freiberg, E. and Walker, W. A. (1990). Prevention of necrotizing enterocolitis in the rat with prenatal cortisone. Gastroenterology 99, 1333-1338. (Pubitemid 20381867)
37. Jilling, T., Simon, D., Lu, J., Meng, F. J., Li, D., Schy, R., Thomson, R. B., Soliman, A., Arditi, M. and Caplan, M. S. (2006). The roles of bacteria and TLR4 in rat and murine models of necrotizing enterocolitis. J. Immunol. 177, 3273-3282. (Pubitemid 44277847)
38. Koivusalo, A., Kauppinen, H., Anttila, A., Heikkilä, P., Rintala, R. and Lindahl, H. (2000). Rectosigmoid pHi monitoring during experimental necrotizing enterocolitis. J. Pediatr. Surg. 35, 1462-1467. (Pubitemid 30769589)
39. Koivusalo, A., Kauppinen, H., Anttila, A., Rautelin, H., Jusufovic, J., Lindahl, H. and Rintala, R. (2002). Intraluminal casein model of necrotizing enterocolitis for assessment of mucosal destruction, bacterial translocation, and the effects of allopurinol and Nacetylcysteine. Pediatr. Surg. Int. 18, 712-717. (Pubitemid 36285675)
40. Langer, J. C., Sohal, S. and Blennerhassett, P. (1995). Mucosal permeability after subclinical intestinal ischemia-reperfusion injury: an exploration of possible mechanisms. J. Pediatr. Surg. 30, 568-572.
41. Leaphart, C. L., Cavallo, J., Gribar, S. C., Cetin, S., Li, J., Branca, M. F., Dubowski, T. D., Sodhi, C. P. and Hackam, D. J. (2007a). A critical Role for TLR4 in the pathogenesis of necrotizing enterocolitis by modulating intestinal injury and repair. J. Immunology 179, 4808-4820.
42. Leaphart, C. L., Qureshi, F., Cetin, S., Li, J., Dubowski, T., Batey, C., Beer-Stolz, D., Guo, F., Murray, S. A. and Hackam, D. J. (2007b). Interferon-[gamma] inhibits intestinal restitution by preventing gap junction communication between enterocytes. Gastroenterology 132, 2395-2411. (Pubitemid 46890858)
43. Lin, P. W. and Stoll, B. J. (2006). Necrotising enterocolitis. Lancet 368, 1271-1283.
44. Lin, P. W., Nasr, T. and Stoll, B. J. (2008). Necrotizing enterocolitis: recent scientific advances in pathophysiology and prevention. Semin. Perinatol. 32, 70-82.
45. Lu, J., Jilling, T., Li, D. and Caplan, M. S. (2007). Polyunsaturated fatty acid supplementation alters proinflammatory gene expression and reduces the incidence of necrotizing enterocolitis in a neonatal rat model. Pediatr. Res. 61, 427-432. (Pubitemid 46569295)
46. Nadler, E. P., Dickinson, E., Knisely, A., Zhang, X. R., Boyle, P., Beer-Stolz, D., Watkins, S. C. and Ford, H. R. (2000). Expression of inducible nitric oxide synthase and interleukin-12 in experimental necrotizing enterocolitis. J. Surg. Res. 92, 71-77. (Pubitemid 30437462)
47. Sangild, P. (2006). Gut responses to enteral nutrition in preterm infants and animals. Exp. Biol. Med. 231, 1695-1711.
48. Sangild, P. T., Siggers, R. H., Schmidt, M., Elnif, J., Bjornvad, C. R., Thymann, T., Grondahl, M. L., Hansen, A. K., Jensen, S. K., Boye, M. et al. (2006). Diet- and colonization-dependent intestinal dysfunction predisposes to necrotizing enterocolitis in preterm pigs. Gastroenterology 130, 1776-1792. (Pubitemid 43668865)
49. Seitz, G., Warmann, S., Guglielmetti, A., Heitmann, H., Ruck, P., Kreis, M. E. and Fuchs, J. (2005). Protective effect of tumor necrosis factor alpha antibody on experimental necrotizing enterocolitis in the rat. J. Pediatr. Surg. 40, 1440-1445. (Pubitemid 41248008)
50. Shah, P. and Shah, V. (2007). Arginine supplementation for prevention of necrotising enterocolitis in preterm infants. Cochrane Database Syst. Rev. 3, CD004339. (Pubitemid 351805441)
51. Shi, L., Zhang, B., Yu, H. G., Yu, J. P. and Xi, J. L. (2007). Intestinal trefoil factor in treatment of neonatal necrotizing enterocolitis in the rat model. J. Perinat. Med. 35, 443-446. (Pubitemid 47237591)
52. Siggers, R. H., Thymann, T., Jensen, B. B., Mølbak, L., Heegaard, P. M., Schmidt, M., Buddington, R. K. and Sangild, P. T. (2008). Elective cesarean delivery affects gut maturation and delays microbial colonization but does not increase necrotizing enterocolitis in preterm pigs. Am. J. Physiol. Regul. Integr. Comp. Physiol. 294, R929-R938. (Pubitemid 351346972)
53. Stoll, B. (1994). Epidemiology of necrotizing enterocolitis. Clin. Perinatol. 21, 205-218.
54. Travadi, J., Patole, S., Charles, A., Dvorak, B., Doherty, D. and Simmer, K. (2006). Pentoxifylline reduces the incidence and severity of necrotizing enterocolitis in a neonatal rat model. Pediatr. Res. 60, 185-189. (Pubitemid 44297590)
55. Warner, B. W. and Warner, B. B. (2005). Role of epidermal growth factor in the pathogenesis of neonatal necrotizing enterocolitis. Semin. Pediatr. Surg. 14, 175-180. (Pubitemid 41111604)
56. Zani, A., Eaton, S., Leon, F. F., Malerba, A., Hall, N. J., De Coppi, P., Smith, V. V. and Pierro, A. (2008). Captopril reduces the severity of bowel damage in a neonatal rat model of necrotizing enterocolitis. J. Pediatr. Surg. 43, 308-314. (Pubitemid 351226219)