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Critical Care

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Open Access 01-08-2007 | Research

Parenteral versus enteral nutrition: effect on serum cytokines and the hepatic expression of mRNA of suppressor of cytokine signaling proteins, insulin-like growth factor-1 and the growth hormone receptor in rodent sepsis

Authors: Michael J O'Leary, Aiqun Xue, Christopher J Scarlett, Andre Sevette, Anthony J Kee, Ross C Smith

Published in: Critical Care | Issue 4/2007

Abstract

Introduction

Early nutrition is recommended for patients with sepsis, but data are conflicting regarding the optimum route of delivery. Enteral nutrition (EN), compared with parenteral nutrition (PN), results in poorer achievement of nutritional goals but may be associated with fewer infections. Mechanisms underlying differential effects of the feeding route on patient outcomes are not understood, but probably involve the immune system and the anabolic response to nutrients. We studied the effect of nutrition and the route of delivery of nutrition on cytokine profiles, the growth hormone–insulin-like growth factor-1 (IGF-I) axis and a potential mechanism for immune and anabolic system interaction, the suppressors of cytokine signaling (SOCS), in rodents with and without sepsis.

Methods

Male Sprague–Dawley rats were randomized to laparotomy (Sham) or to cecal ligation and puncture (CLP), with postoperative saline infusion (Starve), with EN or with PN for 72 hours. Serum levels of IL-6 and IL-10 were measured by immunoassay, and hepatic expressions of cytokine-inducible SH2-containing protein, SOCS-2, SOCS-3, IGF-I and the growth hormone receptor (GHR) were measured by real-time quantitative PCR.

Results

IL-6 was detectable in all groups, but was only present in all animals receiving CLP-PN. IL-10 was detectable in all but one CLP-PN rat, one CLP-EN rat, approximately 50% of the CLP-Starve rats and no sham-operated rats. Cytokine-inducible SH2-containing protein mRNA was increased in the CLP-EN group compared with the Sham-EN group and the other CLP groups (P < 0.05). SOCS-2 mRNA was decreased in CLP-PN rats compared with Sham-PN rats (P = 0.07). SOCS-3 mRNA was increased with CLP compared with sham operation (P < 0.03). IGF-I mRNA (P < 0.05) and GHR mRNA (P < 0.03) were greater in the fed CLP animals and in the Sham-PN group compared with the starved rats.

Conclusion

In established sepsis, nutrition and the route of administration of nutrition influences the circulating cytokine patterns and expression of mRNA of SOCS proteins, GHR and IGF-I. The choice of the administration route of nutrition may influence cellular mechanisms that govern the response to hormones and mediators, which further influence the response to nutrients. These findings may be important in the design and analysis of clinical trials of nutritional interventions in sepsis in man.

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ASPEN Board of Directors and The Clinical Guidelines Task Force: Guidelines for the use of parenteral and enteral nutrition in adult and pediatric patients. J Parenter Enter Nutr 2002, 26: 33S-35S.

O'Leary-Kelley CM, Puntillo KA, Barr J, Stotts N, Douglas MK: Nutritional adequacy in patients receiving mechanical ventilation who are fed enterally. Am J Crit Care 2005, 14: 222-231.PubMed

Adam S, Batson S: A study of problems associated with the delivery of enteral feed in critically ill patients in five ICUs in the UK. Intensive Care Med 1997, 23: 261-266. 10.1007/s001340050326CrossRefPubMed

Gramlich L, Kichian K, Pinilla J, Rodych NJ, Dhaliwal R, Heyland DK: Does enteral nutrition compared to parenteral nutrition result in better outcomes in critically ill adult patients? A systematic review of the literature. Nutrition 2004, 20: 843-848. 10.1016/j.nut.2004.06.003CrossRefPubMed

Simpson F, Doig GS: Parenteral vs. enteral nutrition in the critically ill patient: a meta-analysis of trials using the intention to treat principle. Intensive Care Med 2005, 31: 12-23. 10.1007/s00134-004-2511-2CrossRefPubMed

Ross R, Meill J, Freeman E, Jones J, Matthews D, Preece M, Buchanan C: Critically ill patients have high basal growth hormone levels with attenuated oscillatory activity associated with low levels of insulin-like growth factor-I. Clin Endocrinol 1991, 35: 47-54.CrossRef

Waters MJ, Shang CA, Behncken SN, Tam SP, Li H, Shen B, Lobie PE: Growth hormone as a cytokine. Clin Exp Pharmacol Physiol 1999, 26: 760-764. 10.1046/j.1440-1681.1999.03129.xCrossRefPubMed

Gibson FA, Hinds CJ: Growth hormone and insulin-like growth factors in critical illness. Intensive Care Med 1997, 23: 369-378. 10.1007/s001340050343CrossRefPubMed

Hawker FH, Stewart PM, Baxter RC, Borkmann M, Tan K, Caterson ID, McWilliam DB: Relationship of somatomedin C/insulin-like growth factor I levels to conventional nutritional indices in critically ill patients. Crit Care Med 1987, 15: 732-736. 10.1097/00003246-198708000-00004CrossRefPubMed

10.

Baxter RC: Changes in the IGF–IGFBP axis in critical illness. Best Pract Res Clin Endocrinol Metab 2001, 15: 421-434. 10.1053/beem.2001.0161CrossRefPubMed

11.

Baxter RC, Hawker FH, To C, Stewart PM, Holman SR: Thirty day monitoring of insulin-like growth factors and their binding proteins in intensive care unit patients. Growth Hormone IGF Res 1998, 8: 455-463. 10.1016/S1096-6374(98)80298-0CrossRef

12.

Nicholson SE, Hilton DJ: The SOCS proteins: a new family of negative regulators of signal transduction. J Leukoc Biol 1998, 63: 665-668.PubMed

13.

Yumet G, Shumate ML, Bryant P, Lang CH, Cooney RN: Hepatic growth hormone resistance during sepsis is associated with increased suppressors of cytokine signaling expression and impaired growth hormone signaling. Crit Care Med 2006, 34: 1420-1427. 10.1097/01.CCM.0000215113.66070.E0CrossRefPubMed

14.

Johnson TS, O'Leary M, Justice SK, Maamra M, Zarkesh-Esfahani SH, Furlanetto R, Preedy VR, Hinds CJ, El Nahas AM: Differential expression of suppressors of cytokine signalling genes in response to nutrition and growth hormone in the septic rat. J Endocrinol 2001, 169: 409-415. 10.1677/joe.0.1690409CrossRefPubMed

15.

Scarlett CJ, O'Leary MJ, Kee AJ, Nielsen A, Sevette A, Baxter RC, Smith RC: Survival and protein turnover in severe abdominal sepsis: parenteral versus enteral nutrition. Clin Nutr 2004, 23: 1135-1145. 10.1016/j.clnu.2004.02.008CrossRefPubMed

16.

Kee AJ, Smith RC: The effect of the rate and route of nutrient delivery on total body organ composition in rats. Nutrition 1996, 12: 180-188. 10.1016/S0899-9007(96)91123-5CrossRefPubMed

17.

Rozen S, Skaletsky H: Primer3 on the WWW for general users and for biologist programmers. Methods Mol Biol 2000, 132: 365-386.PubMed

18.

Baker MK, Mikhitarian K, Osta W, Callahan K, Hoda R, Brescia F, Kneuper-Hall R, Mitas M, Cole DJ, Gillanders WE: Molecular detection of breast cancer cells in the peripheral blood of advanced-stage breast cancer patients using multimarker real-time reverse transcription-polymerase chain reaction and a novel porous barrier density gradient centrifugation technology. Clin Cancer Res 2003, 9: 4865-4871.PubMed

19.

Kudsk KA: Effect of route and type of nutrition on intestine-derived inflammatory response. Am J Surg 2003, 185: 16-21. 10.1016/S0002-9610(02)01146-7CrossRefPubMed

20.

Ueno C, Fukatsu K, Kang W, Maeshima Y, Moriya T, Hara E, Nagayoshi H, Omata J, Saito H, Hiraide H, Mochizuki H: Route and type of nutrition influence nuclear factor κB activation in peritoneal resident cells. Shock 2005, 24: 382-387. 10.1097/01.shk.0000180623.29188.3bCrossRefPubMed

21.

Cui X-L, Iwasa M, Kuge H, Sasaguri S, Ogoshi S: Route of feeding influences the production and expression of tumor necrosis factor α in burned rats. Surg Today 2001, 31: 615-625. 10.1007/s005950170096CrossRefPubMed

22.

Moore FA, Feliciano DV, Andrassy RJ, McArdle AH, Booth FV, Morgenstein-Wagner TB, Kellum JM Jr, Welling RE, Moore EE: Early enteral feeding, compared with parenteral, reduces postoperative septic complications. The results of a meta-analysis. Ann Surg 1992, 216: 172-183. 10.1097/00000658-199208000-00008PubMedCentralCrossRefPubMed

23.

Wu Y, Kudsk KA, DeWitt RC, Tolley EA, Li J: Route and type of nutrition influence IgA-mediated intestinal cytokines. Ann Surg 1999, 229: 662-668. 10.1097/00000658-199905000-00008PubMedCentralCrossRefPubMed

24.

Gonnella PA, Helton WS, Robinson M, Wilmore D: O-side chain of Escherichia coli endotoxin 0111:B4 is transported across the intestinal epithelium in the rat: evidence for increased transport during total parenteral nutrition. Eur J Cell Biol 1992, 59: 224-227.PubMed

25.

Alverdy JC, Aoys E, Moss GS: Total parenteral nutrition promotes bacterial translocation from the gut. Surgery 1988, 104: 185-190.PubMed

26.

Fong Y, Marano MA, Barber A, He W, Moldawer LL, Bushman ED, Coyle SM, Shires GT, Lowry SF: Total parenteral nutrition and bowel rest modify the metabolic response to endotoxin in humans. Ann Surg 1989, 210: 449-457. 10.1097/00000658-198910000-00005PubMedCentralCrossRefPubMed

27.

Santos AA, Rodrick ML, Jacobs DO, Dinarello CA, Wolff SM, Mannick JA, Wilmore DW: Does the route of feeding modify the inflammatory response? Ann Surg 1994, 220: 155-163. 10.1097/00000658-199408000-00006PubMedCentralCrossRefPubMed

28.

Wojnar MM, Fan J, Li YH, Lang CH: Endotoxin-induced changes in IGF-I differ in rats provided enteral vs parenteral nutrition. Am J Physiol 1999, 276: E455-E464.PubMed

29.

O'Leary MJ, Quinton N, Ferguson CN, Preedy VR, Ross RJ, Hinds CJ: In rats with sepsis, the acute fall in IGF-I is associated with an increase in circulating growth hormone-binding protein levels. Intensive Care Med 2000, 26: 1547-1552. 10.1007/s001340000656CrossRefPubMed

30.

Defalque D, Brandt N, Ketelsegers JM, Thissen JP: GH insensitivity induced by endotoxin injection is associated with decreased liver GH receptors. Am J Physiol 1999, 276: E565-E572.PubMed

31.

Mao Y, Ling PR, Fitzgibbons TP, McCowen KC, Frick GP, Bistrian BR, Smith RJ: Endotoxin-induced inhibition of growth hormone receptor signaling in rat liver in vivo. Endocrinology 1999, 140: 5505-5515. 10.1210/en.140.12.5505PubMed

32.

Meier R, Beglinger C, Layer P, Gullo L, Keim V, Laugier R, Friess H, Schweitzer M, Macfie J, the ESPEN Consensus Group: ESPEN guidelines on nutrition in acute pancreatitis: European Society of Parenteral and Enteral Nutrition. Clin Nutr 2002, 21: 173-183. 10.1054/clnu.2002.0543CrossRefPubMed

Title: Parenteral versus enteral nutrition: effect on serum cytokines and the hepatic expression of mRNA of suppressor of cytokine signaling proteins, insulin-like growth factor-1 and the growth hormone receptor in rodent sepsis
Authors: Michael J O'Leary
Aiqun Xue
Christopher J Scarlett
Andre Sevette
Anthony J Kee
Ross C Smith
Publication date: 01-08-2007
Publisher: BioMed Central
Published in: Critical Care / Issue 4/2007
Electronic ISSN: 1364-8535
DOI: https://doi.org/10.1186/cc5972

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Parenteral versus enteral nutrition: effect on serum cytokines and the hepatic expression of mRNA of suppressor of cytokine signaling proteins, insulin-like growth factor-1 and the growth hormone receptor in rodent sepsis

Abstract

Introduction

Methods

Results

Conclusion

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Abstract

Introduction

Methods

Results

Conclusion

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