Transition from parenteral to enteral nutrition induces immediate diet-dependent gut histological and immunological responses in preterm neonates

American Journal of Physiology - Gastrointestinal and Liver Physiology

Volumn 301, Issue 3, 2011, Pages

  Siggers, Jayda ^a,d   Sangild, Per T ^a   Jensen, Tim K ^b   Siggers, Richard H ^a   Skovgaard, Kerstin ^b   Støy, Ann Cathrine F ^a   Jensen, Bent B ^c   Thymann, Thomas ^a   Bering, Stine B ^a   Boye, Mette ^b  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

^b TECHNICAL UNIVERSITY OF DENMARK   (Denmark)

^c AARHUS UNIVERSITY   (Denmark)

^d Dept of Human Nutrition ^*  (Denmark)

Author keywords

Birth; Enteral feeding; Histopathology; Intestine; Pig

Indexed keywords

CLAUDIN; INTERLEUKIN 18; INTERLEUKIN 1ALPHA; INTERLEUKIN 6; NITRIC OXIDE SYNTHASE; TOLL LIKE RECEPTOR 4; TUMOR NECROSIS FACTOR ALPHA;

ARTICLE; CELL DEGENERATION; CLOSTRIDIUM; COLOSTRUM; DIET; EDEMA; ENTERIC FEEDING; ENTEROCOCCUS; ENZYME ACTIVITY; GENE EXPRESSION; HISTOLOGY; IMMUNE RESPONSE; INTESTINE FUNCTION; MUCOSAL BLEEDING; NECROSIS; NEWBORN; NONHUMAN; PARENTERAL NUTRITION; PHASE TRANSITION; PREMATURITY; PRIORITY JOURNAL; STREPTOCOCCUS; SWINE;

ANIMALS; COLOSTRUM; ENTERAL NUTRITION; ENTEROCOLITIS, NECROTIZING; HUMANS; INFANT FORMULA; INFANT, NEWBORN; INFANT, PREMATURE; PARENTERAL NUTRITION, TOTAL; SWINE;

EID: 80052275991     PISSN: 01931857     EISSN: 15221547     Source Type: Journal    
DOI: 10.1152/ajpgi.00400.2010     Document Type: Article

References (37)

1. Amann RI, Binder BJ, Olson RJ, Chisholm SW, Devereux R, Stahl DA. Combination of 16S ribosomal-RNA-targeted oligonucleotide probes with flow-cytometry for analyzing mixed microbial-populations. Appl Environ Microbiol 56: 1919-1925, 1990.
2. Bjornvad CR, Schmidt M, Petersen YM, Jensen SK, Offenberg H, Elnif J, Sangild PT. Preterm birth makes the immature intestine sensitive to feeding-induced intestinal atrophy. Am J Physiol Regul Integr Comp Physiol 289: R1212-R1222, 2005.
3. Bjornvad CR, Thymann T, Deutz NE, Burrin DG, Jensen SK, Jensen BB, Molbak L, Boye M, Larsson LI, Schmidt M, Michaelsen KF, Sangild PT. Enteral feeding induces diet-dependent mucosal dysfunction, bacterial proliferation, and necrotizing enterocolitis in preterm pigs on parenteral nutrition. Am J Physiol Gastrointest Liver Physiol 295: G1092-G1103, 2008.
4. Caplan MS, Pathophysiology and prevention of neonatal necrotizing enterocolitis. In: Fetal and Neonatal Physiology (3rd ed.), edited by Polin RA, Fox WW, Abman SH. St. Louis: Saunders, 2004, vol. 2, p. 1169-1172.
5. Cilieborg MS, Boye M, Thymann T, Jensen BB, Sangild PT. Dietdependent effects of minimal enteral nutrition on intestinal function and necrotizing enterocolitis in preterm pigs. JPEN J Parenter Enteral Nutr 35: 32-42, 2011.
6. Claud EC, Walker WA. Hypothesis: inappropriate colonization of the premature intestine can cause neonatal necrotizing enterocolitis. FASEB J 15: 1398-1403, 2001.
7. Cole JR, Chai B, Farris RJ, Wang Q, Kulam-Syed-Mohideen AS, McGarrel DM, Bandela AM, Cardenas E, Garrity GM, Tiedje JM. The ribosomal database project (RDP-II): introducing myRDP space and quality controlled public data. Nucleic Acids Res 35: D169-D172, 2007.
8. Goldman AS. Modulation of the gastrointestinal tract of infants by human milk. Interfaces and interactions. An evolutionary perspective. J Nutr 130, 25 Suppl: 426S-431S, 2000.
9. Hack CJ. Integrated transcriptome and proteome data: the challenges ahead. Brief Funct Genomic Proteomic 3: 212-219, 2004.
10. Halpern MD, Clark JA, Saunders TA, Doelle SM, Hosseini DM, Stagner AM, Dvorak B. Reduction of experimental necrotizing enterocolitis with anti-TNF-α. Am J Physiol Gastrointest Liver Physiol 290: G757-G764, 2006.
11. Halpern MD, Holubec H, Dominguez JA, Meza YG, Williams CS, Ruth MC, McCuskey RS, Dvorak B. Hepatic inflammatory mediators contribute to intestinal damage in necrotizing enterocolitis. Am J Physiol Gastrointest Liver Physiol 284: G695-G702, 2003.
12. Halpern MD, Holubec H, Meza YG, Williams CS, Doelle S, Margelofsky TA, Dvorak B. Inhibition of hepatic TNF alpha decreases the severity of experimental necrotizing enterocolitis (Abstract). Pediatr Res 53: 393A, 2003.
13. Halpern MD, Khailova L, Molla-Hosseini D, Arganbright K, Reynolds C, Yajima M, Hoshiba J, Dvorak B. Decreased development of necrotizing enterocolitis in IL-18-deficient mice. Am J Physiol Gastrointest Liver Physiol 294: G20-G26, 2008.
14. Hunter CJ, Upperman JS, Ford HR, Camerini V. Understanding the susceptibility of the premature infant to necrotizing enterocolitis (NEC). Pediatr Res 63: 1-3, 2008.
15. Jesse N, Neu J. Necrotizing enterocolitis: relationship to innate immunity, clinical features, and strategies for prevention. NeoReviews 7: e143-e150, 2006.
16. Kim YM, Talanian RV, Li J, Billiar TR. Nitric oxide prevents IL-1beta and IFN-gamma-inducing factor (IL-18) release from macrophages by inhibiting caspase-1 (IL-1beta-converting enzyme). J Immunol 161: 4122-4128, 1998.
17. Lefer AM, Lefer DJ 2nd. Nitric oxide protects in intestinal inflammation. Am J Physiol Gastrointest Liver Physiol 276: G572-G575, 1999.
18. Lin PW, Stoll BJ. Necrotising enterocolitis. Lancet 368: 1271-1283, 2006.
19. Lucas A, Cole TJ. Breast-milk and neonatal necrotizing enterocolitis. Lancet 336: 1519-1523, 1990.
20. Monteleone G, Trapasso F, Parrello T, Biancone L, Stella A, Iuliano R, Luzza F, Fusco A, Pallone F. Bioactive IL-18 expression is upregulated in Crohn's disease. J Immunol 163: 143-147, 1999.
21. Nadler EP, Stanford A, Zhang XR, Schall LC, Alber SM, Watkins SC, Ford HR. Intestinal cytokine gene expression in infants with acute necrotizing enterocolitis: interleukin-11 mRNA expression inversely correlates with extent of disease. J Pediatr Surg 36: 1122-1129, 2001.
22. Pizarro TT, Michie MH, Bentz M, Woraratanadharm J, Smith MF Jr, Foley E, Moskaluk CA, Bickston SJ, Cominelli F. IL-18, a novel immunoregulatory cytokine, is up-regulated in Crohn's disease: expression and localization in intestinal mucosal cells. J Immunol 162: 6829-6835, 1999.
23. Sangild PT, Siggers RH, Schmidt M, Elnif J, Bjornvad CR, Thymann T, Grondahl ML, Hansen AK, Jensen SK, Boye M, Moelbak L, Buddington RK, Westrom BR, Holst JJ, Burrin DG. Diet-and colonization-dependent intestinal dysfunction predisposes to necrotizing enterocolitis in preterm pigs. Gastroenterology 130: 1776-1792, 2006.
24. Sangild PT, Sjostrom H, Noren O, Fowden AL, Silver M. The prenatal development and glucocorticoid control of brush-border hydrolases in the pig small-intestine. Pediatr Res 37: 207-212, 1995.
25. Schnabl KL, Van Aerde JE, Thomson ABR, Clandinin MT. Necrotizing enterocolitis: a multifactorial disease with no cure. World J Gastroenterol 14: 2142-2161, 2008.
26. Siggers RH, Thymann T, Jensen BB, Molbak L, Heegaard PMH, Schmidt M, Buddington RK, Sangild PT. 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, 2008.
27. Siggers RH, Thymann T, Siggers JL, Schmidt M, Hansen AK, Sangild PT. Bacterial colonization affects early organ and gastrointestinal growth in the neonate. Livest Sci 109: 14-18, 2007.
28. Siggers RH, Siggers J, Boye M, Thymann T, Molbak L, Leser T, Jensen BB, Sangild PT. Early administration of probiotics alters bacterial colonization and limits diet-induced gut dysfunction and severity of necrotizing enterocolitis in preterm pigs. J Nutr 138: 1437-1444, 2008.
29. Skovgaard K, Mortensen S, Boye M, Hedegaard J, Heegaard PM. Hepatic gene expression changes in pigs experimentally infected with the lung pathogen Actinobacillus pleuropneumoniae as analysed with an innate immunity focused microarray. Innate Immun 16: 343-353, 2010.
30. Ten Hove T, Corbaz A, Amitai H, Aloni S, Belzer I, Graber P, Drillenburg P, Van Deventer SJH, Chvatchko Y, Te Velde AA. Blockade of endogenous IL-18 ameliorates TNBS-induced colitis by decreasing local TNF-α production in mice. Gastroenterology 121: 1372-1379, 2001.
31. Thymann T, Møller HK, Stoll B, Støy AC, Buddington RK, Bering SB, Jensen BB, Olutoye OO, Siggers RH, Mølbak L, Sangils PT, Brurrin DG. Carbohydrate maldigestion induces necrotizing enterocolitis in preterm pigs. Am J Physiol Gastrointest Liver Physiol 297: G1115-G1125, 2009.
32. Van Haver ER, Oste M, Thymann T, Sys SU, Lamers WH, Weyns ALM, Sangild PT, Van Ginneken CJ. Enteral feeding reduces endothelial nitric oxide synthase in the caudal intestinal microvasculature of preterm piglets. Pediatr Res 63: 137-142, 2008.
33. Van Haver ER, Sangild PT, Oste M, Siggers JL, Weyns AL, Van Ginneken CJ. Diet-dependent mucosal colonization and interleukin-1beta responses in preterm pigs susceptible to necrotizing enterocolitis. J Pediatr Gastroenterol Nutr 49: 90-98, 2009.
34. Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, De Paepe A, Speleman F. Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 3: 1-12, 2002.
35. Waligora-Dupriet AJ, Dugay A, Auzeil N, Huerre M, Butel MJ. Evidence for clostridial implication in necrotizing enterocolitis through bacterial fermentation in a gnotobiotic quail model. Pediatr Res 58: 629-635, 2005.
36. Washburn MP, Koller A, Oshiro G, Ulaszek RR, Plouffe D, Deciu C, Winzeler E, Yates JR. Protein pathway and complex clustering of correlated mRNA and protein expression analyses in Saccharomyces cerevisiae. Proc Natl Acad Sci USA 100: 3107-3112, 2003.
37. Yang YH, Dudoit S, Luu P, Lin DM, Peng V, Ngai J, Speed TP. Normalization for cDNA microarray data: a robust composite method addressing single and multiple slide systematic variation. Nucleic Acids Res 30: e15, 2002.