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Abstract

Background: Early enteral nutrition is associated with a lower incidence of intraabdominal abscess in severely injured patients than parenteral nutrition (PN). We explored the underlying mechanisms by examining the influence of nutrition route on nuclear factor κB (NFκB) activation in peritoneal exudative cells (PECs) and peritoneal cytokine levels. Methods: Thirty male Institute Cancer Research mice were randomized to chow (n = 10), IV PN (n = 10), or intragastric (IG) PN (n = 10) and fed for 5 days. PECs were harvested at 2 or 4 hours after intraperitoneal injection of 2 mL of 1% glycogen. Intranuclear NFκB activity in PECs was examined by laser scanning cytometry. Cytokine (tumor necrosis factor-α [TNF-α], macrophage inflammatory protein-2 [MIP-2], interleukin-10 [IL-10]) levels in peritoneal lavaged fluid were determined by enzyme-linked immunosorbent assay. Results: Intranuclear NFκB at 2 hours was significantly higher in the chow and IG-PN groups than in the IV-PN group. TNF-α and IL-10 levels of the chow group were significantly higher than those of IV-PN mice at 2 hours, whereas those of IG-PN mice were midway between those of the chow and IV-PN groups. MIP-2 was significantly higher in the chow group than in the IG-PN and IV-PN mice at 2 hours. TNF-α levels correlated positively with intranuclear NFκB activity in PECs. Conclusions: Enteral nutrition may improve peritoneal defense by preserving early NFκB activation in PECs and cytokine responses.

We clarified an important mechanism for impaired peritoneal defense during lack of enteral nutrition. Parenterally fed mice showed delay of NFκB activation in peritoneal exudative cells and cytokine responses in glycogen-induced peritonitis, as compared with enterally fed animals.

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References

Fukatsu K, Zarzaur BL, Johnson CD, Lundberg AH, Wilcox HG, Kudsk KA. Enteral nutrition prevents remote organ injury and death after a gut ischemic insult. Ann Surg. 2001 ;233:660– 668.

Johnson CD, Kudsk KA, Fukatsu K, Renegar KB, Zarzaur BL. Route of nutrition influences generation of antibody-forming cells and initial defense to an active viral infection in the upper respiratory tract. Ann Surg. 2003;237:565– 573.

Kang W, Saito H, Fukatsu K, Ikeda S, Nagawa H. Brief refeeding rapidly reverses dietary restriction-induced nuclear factor kB downregulation in peritoneal resident cells. JPEN J Parenter Enteral Nutr. 2003 ;27:193– 197.

Kudsk KA. Effect of route and type of nutrition on intestinederived inflammatory responses. Am J Surg. 2003 ;185:16– 21.

Kusdk KA, Croce MA, Fabian TC. Enteral vs. parenteral feeding: effects on septic morbidity following blunt and penetrating abdominal trauma.Ann Surg. 1992;215:503– 513.

Moore FA, Felicano DV, Andrassy RJ. Early enteral feeding, compared with parenteral, reduces postoperative septic complications: the results of a meta-analysis. Ann Surg. 1992 ;216:172– 183.

Braga M, Gianotti L, Gentilini O, Paris V. Early postoperative enteral nutrition improves gut oxygenation and reduces costs compared with total parenteral nutrition. Crit Care Med. 2001 ;2:242– 248.

Kudsk KA, Li J, Renegar KB. Loss of upper respiratory tract immunity with parenteral feeding. Ann Surg. 1996 ;223:629– 638.

Dunn DL, Barke RA, Knight NB, Humphrey EW, Simmons RL. Role of resident macrophages, peripheral neutrophils, and translymphatic absorption in bacterial clearance from the peritoneal cavity. Infect Immunol. 1985 ;49:257– 264.

10.

Barnes PJ, Karlin M. NFkB: a pivotal transcription factor in chronic inflammatory diseases. N Engl J Med. 1997 ;336:1066– 1071.

11.

Ueno C, Fukatsu K, Kang W, et al. Route and type of nutrition influence NFkB activation in peritoneal resident cells. Shock. 2005 ;24:382– 387.

12.

Lin MT, Saito H, Fukushima R, et al. Route of nutritional supply influences local, systemic and remote organ responses to intraperitoneal bacterial challenge. Ann Surg. 1996 ;223:84– 93.

13.

Ikeda S, Saito H, Fukatsu K, et al. Dietary restriction impairs neutrophil exudation by reducing CD11b/CD18 expression and chemokine production. Arch Surg. 2001 ;136:297– 304.

14.

Maddaus MA, Ahrenholz D, Simmons RL. The biology of peritonitis and implications for treatment. Surg Clin North Am. 1988 ;68:431– 443.

15.

Carlos TM, Harlan JM. Leukocyte-endothelial adhesion molecule.Blood. 1994;84:2068– 2101.

16.

Deptala A, Bedner E, Gorczyca W, Darzynkiewicz Z. Activation of nuclear kappa B (NFkB) assayed by laser scanning cytometry.Cytometry. 1998;33:376– 382.

17.

Kang W, Saito H, Fukatsu K, et al. Effects of tyrosine kinase signaling inhibition on survival after cecal ligation and puncture in diet restricted mice. JPEN J Parenter Enteral Nutr. 2001 ;25:291– 298.

18.

Yuksel M, Okajima K, Uchiba M, Okabe H. Gabexate mesilate, a synthetic protease inhibitor, inhibits lipopolysaccharide-induced tumor necrosis factor: a production by inhibiting activation of both nuclear factor-kB and activator protein-1 in human monocytes. J Pharmacol Exp Ther. 2002;305:298– 305.

19.

Guizani-Tabbane L, Ben-Aissa K, Belghith M, Sassi A, Dellagi K. Leishmania major amastigotes induce p50/c-Rel NF-kappa B transcription factor in human macrophages: involvement in cytokine synthesis. Infect Immunol. 2004;72:2582– 2589.

20.

Walley KR, Lukacs NW, Standiford TJ, Strieter RM, Kunkel SL. Elevated levels of macrophage inflammatory protein-2 in severe murine peritonitis increase neutrophil recruitment and mortality. Infect Immunol. 1997;65:3847– 3851.

21.

Sakai S, Hiroshi O, Nakajima K, Terasawa K. Inhibitory effect of ferulic acid on macrophage inflammatory protein-2 production in a murine macrophage cell line. Cytokine. 1996 ;9:242– 248.

22.

Moon SK, Cha BY, Kim CH. ERK1/2 mediates TNF-alpha-induced matrix metalloproteinase-9 expression in human vascular smooth muscle cells via the regulation of NF-kappaB and AP-1: involvement of the ras dependent pathway.J Cell Physiol. 2004;198:417– 427.

23.

Celdran A, Inarrea P, Fernandez J, Larrocha C, Madero R. Neutrophil dynamics in abdominal cavity of peritonitic rats treated with antiseptics.Int Surg. 1993;78:354– 356.

24.

Foulds S, Galustian C, Mansfield AO, Schachter M. Transcription factor NFkB expression and postsurgical organ dysfunction. Ann Surg. 2001;233:70– 78.

25.

Moore EE, Moore FA, Franciose RJ, Kim FJ, Biffi WL, Banerjee A. The postischemic gut serves as a priming bed for circulating neutrophils that provoke multiple organ failure. J Trauma. 1994 ;37:881– 887.

26.

Shou J, Redmond HP, Leon P, Hofmann KP, Daly JM. Elemental diet alters macrophage function in mice. J Surg Res. 1990 ;51:192– 196.

27.

Wu Y, Kudsk KA, DeWitt C, Tolley EA, Li J. Route and type of nutrition influence IgA-mediating intestinal cytokines. Ann Surg. 1999;229:662– 668.

28.

De Souza CT, Araujo EP, Bordin S, et al. Consumption of a fat-rich diet activates a pro-inflammatory response and induces insulin resistance in the hypothalamus. Endocrinology. 2005 ;146:4192– 4199.

29.

Blanco-Colio LM, Valderrama M, Alvarez-Sala LA, et al. Red wine intake prevents nuclear factor-kappaB activation in peripheral blood mononuclear cells of healthy volunteers during postprandial lipemia.Circulation. 2000;102:1020– 1026.

30.

Bellido C, Lopez-Miranda J, Blanco-Colio LM, et al. Butter and walnuts, but not olive oil, elicit postprandial activation of nuclear transcription factor kappaB in peripheral blood mononuclear cells from healthy men. Am J Clin Nutr. 2004 ;80:1487– 1491.

31.

Rusyn I, Bradham CA, Cohn L, et al. Corn oil rapidly activates nuclear factor-kappa B in hepatic Kupffer cells by oxidant-dependent mechanisms. Carcinogenesis. 1999 ;20:2095– 2100.

32.

Mahaffey SM, Copeland EM 3rd, Talbert JL, Baumgartner TG, Sitren HS. Further studies of a technique for total parenteral nutrition in the mouse. Nutr Res. 1985;5:1121– 1130.

33.

Kang W, Saito H, Fukatsu K, Hidemura A, Matsuda T. Diet restriction impairs extracellular signal-regulated kinase activation of peritoneal exudative cells after N-formyl-methionylleucyl-phenylalanine stimulation in a murine peritonitis model. JPEN J Parenter Enteral Nutr. 2002 ;26:259– 264.

34.

Kudsk KA, Minard G, Croce MA, et al. A randomized trial of isonitrogenous enteral diets after severe trauma: an immuneenhancing diet reduces septic complications. Ann Surg. 1996 ;224:531– 543.

Lack of Enteral Nutrition Delays Nuclear Factor Kappa B Activation in Peritoneal Exudative Cells in a Murine Glycogen-Induced Peritonitis Model

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