Skip to main content

Metabolic Depletion and Failure: Muscle Cachexia During Injury and Sepsis

  • Chapter
Multiple Organ Failure

Abstract

Severe injury and sepsis are associated with metabolic changes in virtually all organs and tissues and include alterations in carbohydrate, lipid, and protein metabolism.1,2 One of the most prominent metabolic consequences of critical illness is the catabolic response in skeletal muscle. Metabolic depletion and failure in skeletal muscle result in muscle atrophy, weakness, and fatigue, preventing ambulation and delaying recovery in these patients. When respiratory muscles are involved in the catabolic response3, difficulties arise when weaning the patient from the ventilator. In addition, muscle weakness increases the risk for aspiration and pneumonia.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Hasselgren PO: Mediators, hormones, and control of metabolism: atregulation of protein, carbohydrate, and lipid metabolism in critical illness. In: Fischer JE (ed) Nutrition and Metabolism in the Surgical Patient, 2nd ed. Boston: little,Brown, 1996; 57–104.

    Google Scholar 

  2. Hill AG, Hill GL: Metabolic response to severe injury. Br J Surg 1998; 85: 884–890.

    Article  PubMed  CAS  Google Scholar 

  3. Reid WD, MacGowan NA: Respiratory muscle injury in animal models and humans. Mol Cell Biochem 1998; 179: 63–80.

    Article  PubMed  CAS  Google Scholar 

  4. Hasselgren PO, James JH, Benson DW, et al: Total and myofibrillar protein breakdown in different types of rat skeletal muscle: effects of sepsis and regulation by insulin. Metabolism 1989; 38: 634–640.

    Article  PubMed  CAS  Google Scholar 

  5. Long CL, Birkhahn RH, Geiger JW, et al: Urinary excretion of 3-methylhistidine: an assessment of muscle protein catabolism in adult normal subjects and during malnutrition, sepsis, and skeletal trauma. Metabolism 1981; 30: 765–776.

    Article  PubMed  CAS  Google Scholar 

  6. Vary TC, Kimball SR: Sepsis-induced changes in protein synthesis: differential effects on fast-and slow-twitch muscles. Am J Physiol 1992; 262: C1513–C1519.

    PubMed  CAS  Google Scholar 

  7. Chang HR, Bistrian B: The role of cytokines in the catabolic consequences of infection and injury. JPEN J Parenter Enteral Nutr 1998; 22: 156–166.

    Article  PubMed  CAS  Google Scholar 

  8. Zamir O, Hasselgren PO, Higashiguchi T, et al: Tumor necrosis factor and interleukin-1 induce muscle proteolysis through different mechanisms. Mediat Inflamm 1992; 1: 247–250.

    Article  CAS  Google Scholar 

  9. Zamir O, Hasselgren PO, Kunkel SL, et al: Evidence that tumor necrosis factor participates in the regulation of muscle proteolysis during sepsis. Arch Surg 1992; 127: 170–174.

    Article  PubMed  CAS  Google Scholar 

  10. Zamir O, O’Brien W, Thompson R, et al: Reduced muscle protein breakdown in septic rats following treatment with interleukin-1 receptor antagonist. Int J Biochem 1994; 26: 943–950.

    Article  PubMed  CAS  Google Scholar 

  11. Mealy K, van Lanschot JJB, Robinson BG, et al: Are the catabolic effects of tumor necrosis factor mediated by glucocorticoids? Arch Surg 1990; 125: 42–48.

    Article  PubMed  CAS  Google Scholar 

  12. Moldawer LL, Svaninger G, Gelin J, et al: Interleukin-1 and tumor necrosis factor do not regulate protein balance in skeletal muscle. Am J Physiol 1987; 253: C766–C773.

    PubMed  CAS  Google Scholar 

  13. Goldberg AL, Kettelhut IC, Furano K, et al: Activation of protein breakdown and prostaglandin E2 production in rat skeletal muscle in fever is signaled by a macrophage product distinct from interleukin-1 or other known monokines. J Clin Invest 1988; 81: 1378–1383.

    Article  PubMed  CAS  Google Scholar 

  14. Hasselgren PO, James JH, Benson DW, et al: Is there a circulating proteolysis-inducing factor during sepsis? Arch Surg 1990; 125: 510–514.

    Article  PubMed  CAS  Google Scholar 

  15. Damas P, Ledoux D, Nys M, et al: Cytokine serum level during severe sepsis in human: IL-6 as a marker of severity. Ann Surg 1992; 215: 356–362.

    Article  PubMed  CAS  Google Scholar 

  16. Tsujinaka T, Ebisui G, Fujita J, et al: Muscles undergo atrophy in association with increase of lysosomal cathepsin activity in interleukin-6 transgenic mouse. Biochem Biophys Res Commun 1995; 207: 168–174.

    Article  PubMed  CAS  Google Scholar 

  17. Strassman G, Fong M, Kenney JS, et al: Evidence for the involvement of interleukin-6 in experimental cancer cachexia. J Clin Invest 1992; 89: 1681–1684.

    Article  Google Scholar 

  18. Williams A, Wang JJ, Wang L, et al: Sepsis in mice stimulates muscle proteolysis in the absence of IL-6. Am J Physiol 1998; 275: R1983–R1991.

    PubMed  CAS  Google Scholar 

  19. Garzia-Martinez C, Lopez-Soriano FJ, Argiles JM: Interleukin-6 does not activate protein breakdown in rat skeletal muscle. Cancer Lett 1994; 76: 1–4.

    Article  Google Scholar 

  20. Espat NJ, Auffenberg T, Rosenberg JJ, et al: Ciliary neurotrophic factor is catabolic and shares with IL-6 the capacity to induce an acute phase response. Am J Physiol 1996; 271: R185–R190.

    PubMed  CAS  Google Scholar 

  21. Vaughan GM, Becker RA, Allen JP, et al: Cortisol and cortico trophin in burned patients. J Trauma 1982; 22: 263–273.

    Article  PubMed  CAS  Google Scholar 

  22. Darmann D, Matthews DE, Bier DM: Physiological hypercorti solemia increases proteolysis, glutamine and alanine production. Am J Physiol 1988; 255: E366–E373.

    Google Scholar 

  23. Kayali AG, Young VR, Goodman MM: Sensitivity of myofibrillar proteins to glucocorticoid-induced muscle proteolysis. Am J Physiol 1987; 252: E621–E626.

    PubMed  CAS  Google Scholar 

  24. Tiao G, Fagan J, Roegner V, et al: Energy-ubiquitin-dependent muscle proteolysis during sepsis in rats is regulated by glucocorticoids. J Clin Invest 1996; 97: 339–348.

    Article  PubMed  CAS  Google Scholar 

  25. Hall-Angeras M, Angeras U, Zamir O, et al: Effect of the glucocorticoid receptor antagonist RU38486 on muscle protein breakdown in sepsis. Surgery 1991; 109: 468–473.

    PubMed  CAS  Google Scholar 

  26. Fang CH, James JH, Ogle CK, et al: Influence of burn injury on protein metabolism in different types of skeletal muscle and the role of glucocorticoids. J Am Coll Surg 1995; 180: 33–42.

    PubMed  CAS  Google Scholar 

  27. Wing SS, Goldberg AL: Glucocorticoids activate the ATP-ubiquitin-dependent proteolytic system in skeletal muscle during fasting. Am J Physiol 1993; 264: E668–E676.

    PubMed  CAS  Google Scholar 

  28. Savary I, Debras E, Dardavet D, et al: Effect of glucocorticoid excess on skeletal muscle and heart protein synthesis in adult and old rats. Br J Nutr 1998; 79: 297–304.

    Article  PubMed  CAS  Google Scholar 

  29. Odedra BR, Bates PC, Millward DJ: Time course of the effect of catabolic doses of corticosterone on protein turnover in rat skeletal muscle and liver. Biochem J 1983; 214: 617–627.

    PubMed  CAS  Google Scholar 

  30. Hong DH, Forsberg NE: Effects of dexamethasone on protein degradation and protease gene expression in rat L8 myotube cultures. Mol Cell Endocrinol 1995; 108: 199–209.

    Article  PubMed  CAS  Google Scholar 

  31. Wang L, Luo GJ, Wang JJ, et al: Dexamethasone stimulates proteasome-and calcium-dependent proteolysis in cultured L6 myotubes. Shock 1998; 10: 298–306.

    Article  PubMed  CAS  Google Scholar 

  32. Del Ray A, Besedovsky HO: Metabolic and neuroendocrine effects of pro-inflammatory cytokines. Eur J Clin Invest 1992; 22: 10–15.

    Google Scholar 

  33. Kern JA, Lamb RJ, Reed JC, et al: Dexamethasone inhibition of interleukin-1 beta production by human monocytes. J Clin Invest 1988; 81: 237–244.

    Article  PubMed  CAS  Google Scholar 

  34. Hall-Angeras M, Angeras U, Zamir O, et al: Interaction between corticosterone and tumor necrosis factor stimulated protein breakdown in rat skeletal muscle, similar to sepsis. Surgery 1990; 108: 460–466.

    PubMed  CAS  Google Scholar 

  35. Tisdale MJ: New cachexic factors. Curr Opin Clin Nutr Metab Care 1998; 1: 253–256.

    Article  PubMed  CAS  Google Scholar 

  36. Todorov PT, Deacon M, Tisdale MJ: Structural analysis of a tumor-produced sulfated glycoprotein capable of initiating muscle protein degradation. J Biol Chem 1997; 272: 12279–12288.

    Article  PubMed  CAS  Google Scholar 

  37. Clowes GHA, George BC, Villee CA, et al: Muscle proteolysis induced by a circulating peptide in patients with trauma and sepsis. N Engl J Med 1983; 308: 545–552.

    Article  PubMed  Google Scholar 

  38. Thompson MG, Palmer RM: Signaling pathways regulating protein turnover in skeletal muscle. Cell Signal 1998; 10: 1–11.

    Article  PubMed  CAS  Google Scholar 

  39. Tiao G, Fagan JM, Samuels N, et al: Sepsis stimulates non lysosomal energy-dependent proteolysis and increases ubiquitin mRNA levels in rat skeletal muscle. J Clin Invest 1994; 94: 2255–2264.

    Article  PubMed  CAS  Google Scholar 

  40. Tiao G, Hobler SC, Wang JJ, et al: Sepsis is associatedwith increased mRNAs of the ubiquitin-proteasome proteolytic pathway in human skeletal muscle. J Clin Invest 1997; 99: 163–168.

    Article  PubMed  CAS  Google Scholar 

  41. Hobler SC, Tiao G, Fischer JE, et al: The sepsis-induced increasein muscle proteolysis is blocked by specific proteasome inhibitors. Am J Physiol 1998; 274: R30–R37.

    PubMed  CAS  Google Scholar 

  42. Attaix D, Taillandier D: The critical role of the ubiquitin proteasome pathway in muscle wasting in comparison to lysosomal and calcium-dependent systems. Adv Mol Cell Biol 1998; 27: 235–266.

    Article  CAS  Google Scholar 

  43. Voisin L, Breuille O, Combaret L, et al: Muscle wasting in a ratmodel of long lasting sepsis results from the activation oflysosomal, calcium-activated, and ubiquitin-proteasome proteolytic pathways. J Clin Invest 1996; 97: 1610–1617.

    Article  PubMed  CAS  Google Scholar 

  44. Hasselgren PO, Fischer JE: The ubiquitin-proteasome pathway: review of a novel intracellular mechanism of muscle protein breakdown during sepsis and other catabolic conditions. Ann Surg 1997; 225: 307–316.

    Article  PubMed  CAS  Google Scholar 

  45. Hershko A, Ciechanover A: The ubiquitin system for protein degradation. Annu Rev Biochem 1992; 61: 761–807.

    Article  PubMed  CAS  Google Scholar 

  46. Wing SS, Banville D: 14-kDa ubiquitin-conjugating enzyme: structure of the rat gene and regulation upon fasting and by insulin. Am J Physiol 1994; 267: E39–E48.

    PubMed  CAS  Google Scholar 

  47. Weissman JS, Sigler PB, Horwich AL: From the cradle to the grave: ring complexes in the life of a protein. Science 1995; 268: 523–524.

    Article  PubMed  CAS  Google Scholar 

  48. Fang CH, Tiao G, James JH, et al: Burn injury stimulates multiple proteolytic pathways in skeletal muscle, including the ubiquitin-energy-dependent pathway. J Am Coll Surg 1995; 180: 161–170.

    PubMed  CAS  Google Scholar 

  49. Hobler SC, Williams AB, Fischer D, et al: The activity and expression of the 20S proteasome are increased in skeletal muscle during sepsis. Am J Physiol 1999; 277: R434–R440.

    PubMed  CAS  Google Scholar 

  50. Wing SS, Bedard N: Insulin-like growth factor I stimulates degradation of an mRNA transcript encoding the 14 kDa ubiquitin conjugating enzyme. Biochem J 1996; 319: 455–461.

    PubMed  CAS  Google Scholar 

  51. Hobler SC, Wang JJ, Williams AB, et al: Sepsis is associated with increased ubiquitin conjugating enzyme E2-14kDa mRNA in skeletal muscle. Am J Physiol 1999; 276: R468–R473.

    PubMed  CAS  Google Scholar 

  52. Tiao G, Lieberman MA, Fischer JE, et al: Intracellular regulation of protein degradation during sepsis is different in fast-and slow twitch muscle. Am J Physiol 1997; 272: 849–R856.

    Google Scholar 

  53. Fang CH, Li BG, Tiao G, et al: The molecular regulation of protein breakdown following burn injury is different in fast-and slow-twitch skeletal muscle. Int J Mol Med 1998; 1: 163–169.

    PubMed  CAS  Google Scholar 

  54. Lee DH, Goldberg AL: Proteasome inhibitors: valuable new tools for cell biologists. Trends Cell Biol 1998; 8: 397–403.

    Article  PubMed  CAS  Google Scholar 

  55. Fenteany G, Standaert RF, Lane WS, et al: Inhibition of proteasome activities and subunit-specific amino-terminal threonine modification by lactacystin. Science 1995; 268: 726–731.

    Article  PubMed  CAS  Google Scholar 

  56. Tawa NE, Odessey R, Goldberg AL: Inhibitors of the proteasome reduce the accelerated proteolysis in atrophying rat skeletal muscles. J Clin Invest 1997; 100: 197–203.

    Article  PubMed  CAS  Google Scholar 

  57. Fang CH, Wang JJ, Hobler S, et al: Proteasome blockers inhibit protein breakdown in skeletal muscle after burn injury in rats. Clin Sci 1998; 95: 225–233.

    Article  PubMed  CAS  Google Scholar 

  58. Dick LR, Cruikshank AA, Grenier L, et al: Mechanistic studies on the inactivation of the proteasome by lactacystin: a central role for clasto-lactacystin beta-lactone. J Biol Chem 1996; 271: 7273–7276.

    Article  PubMed  CAS  Google Scholar 

  59. Mansoor O, Beaufrere B, Boirie Y, et al: Increased mRNA levels for components of the lysosomal, calcium-activated, and ATP-ubiquitin-dependent proteolytic pathways in skeletal muscle from head trauma patients. Proc Natl Acad Sci USA 1996; 93: 2714–2718.

    Article  PubMed  CAS  Google Scholar 

  60. Williams AB, Sun X, Fischer JE, et al: The expression of genes in the ubiquitin-proteasome proteolytic pathway is increased in skeletal muscle from patients with cancer. Surgery (in press)

    Google Scholar 

  61. Tiao G, Fagan J, Roegner V, et al: Energy-ubiquitin-dependent muscle proteolysis during sepsis in rats is regulated by glucocorticoids. J Clin Invest 1996; 97: 339–348.

    Article  PubMed  CAS  Google Scholar 

  62. Auclair D, Garrel DR, Zerouala AC, et al: Activation of the ubiquitin pathway in rat skeletal muscle by catabolic doses of glucocorticoids. Am J Physiol 1997; 272: C1007–C1016.

    PubMed  CAS  Google Scholar 

  63. Ralliere C, Tauveron I, Taillandier D, et al: Glucocorticoids do not regulate the expression of proteolytic genes in skeletal muscle from Cushing’s syndrome patients. J Clin Endocrinol Metab 1997; 82: 3161–3164.

    Article  PubMed  CAS  Google Scholar 

  64. Roberts RG, Redfern CPF, Goodship THJ: Changes in the expression of proteolytic enzymes following correction of acidosis in humans with renal failure [abstract 1]. Presented at the Fourth International Symposium on Amino Acid/Protein Metabolism in Health and Disease, Padova, Italy, April 1996

    Google Scholar 

  65. Price SR, England K, Bailey JK, et al: Acidosis and glucocorticoids concomitantly increase ubiquitin and proteasome subunit mRNAs in rat muscle. Am J Physiol 1994; 267: C955–C960.

    PubMed  CAS  Google Scholar 

  66. Madura K, Dohmen RJ, Varshavsky A: N-recognin/Ubc2 interactions in the N-end rule pathway. J Biol Chem 1993; 268: 12046–12054.

    PubMed  CAS  Google Scholar 

  67. Varshavsky A: The N-end rule pathway of protein degradation. Genes Cells 1997; 2: 13–28.

    Article  PubMed  CAS  Google Scholar 

  68. Kwon YT, Reiss Y, Fried VA, et al: The mouse and human genes encoding the recognition component of the N-end rule pathway. Proc Natl Acad Sci USA 1998; 95: 7898–7903.

    Article  PubMed  CAS  Google Scholar 

  69. Solomon V, Lecker SH, Goldberg AL: The N-end rule pathway catalyzes a major fraction of the protein degradation in skeletal muscle. J Biol Chem 1998; 273: 25216–25222.

    Article  PubMed  CAS  Google Scholar 

  70. Solomon V, Barracos V, Sarraf P, et al: Rates of ubiquitin conjugation increase when muscles atrophy, largely through activation of the N-end rule pathway. Proc Natl Acad Sci USA 1998; 95: 12602–12607.

    Article  PubMed  CAS  Google Scholar 

  71. Williams A, deCourten-Myers GM, Fischer JE, et al: Sepsis stimulates release of myofilaments in skeletal muscle by a calcium-dependent mechanism. FASEB J 1999; 13: 1435–1443.

    PubMed  CAS  Google Scholar 

  72. Kimball SR, Vary TC, Jefferson LS: Regulation of protein synthesis by insulin. Annu Rev Physiol 1994; 56: 321–348.

    Article  PubMed  CAS  Google Scholar 

  73. Hasselgren PO, Fischer JE: Regulation by insulin of muscle protein metabolism during sepsis and other catabolic conditions. Nutrition 1992; 8: 434–439.

    PubMed  CAS  Google Scholar 

  74. Thorell A, Nygren J, Hirschman MF, et al: Surgery-induced insulin resistance in human patients: relation to glucose transport and utilization. Am J Physiol 1999; 276: E754–E761.

    PubMed  CAS  Google Scholar 

  75. Hasselgren PO, Warner BW, James JH, et al: Effect of insulin on amino acid uptake and protein turnover in skeletal muscle from septic rats: evidence for insulin resistance of protein breakdown. Arch Surg 1987; 122: 228–233.

    Article  PubMed  CAS  Google Scholar 

  76. Hinton PS, Littlejohn SP, Allison FP, et al: Insulin and glucose to reduce the catabolic response to injury in burned patients. Lancet 1971; 17: 767–769.

    Article  Google Scholar 

  77. Wilmore DW, Moylan JA, Briston B, et al: Anabolic effects of human growth hormone and high caloric feedings following thermal injury. Surg Gynecol Obstet 1974; 138: 855–884.

    Google Scholar 

  78. Jiang SM, He GZ, Zhang SY, et al: Low-dose growth hormone and hypocaloric nutrition attenuate the protein-catabolic response after major operation. Ann Surg 1989; 210: 513–524.

    Article  PubMed  CAS  Google Scholar 

  79. Public communication from Pharmacia & Upjohn Pharmaceuticals and Rolf Gunnarsson, M.D., to all industry and medical community involved with the use or potential use of recombinant human growth hormone, October 1997

    Google Scholar 

  80. Ramirez RJ, Wolf SE, Barro AE, et al: Growth hormone treatment in pediatric burns: a safe therapeutic approach. Ann Surg 1998; 228: 439–448.

    Article  PubMed  CAS  Google Scholar 

  81. Fang CH, Li BG, Wang JJ, et al: Insulin-like growth factor I (IGF-I) stimulates protein synthesis and inhibits protein breakdown in muscle from burned rats. JPENJ Parenter Enteral Nutr 1997; 21: 245–251.

    Article  CAS  Google Scholar 

  82. Fang CH, Li BG, Wang JJ, et al: Treatment of rats with insulin-like growth factor I inhibit the catabolic response in skeletal muscle Mowing burn injury. Am J Physiol 1998; 275: R1091–R1098.

    PubMed  CAS  Google Scholar 

  83. Fang CH, Li BG, James JH, et al: The anabolic effects of IGF-I in skeletal muscle are not caused by increased cell volume. JPENJ Parenter Enteral Nutr 1998; 22: 115–119.

    Article  CAS  Google Scholar 

  84. Hobler SC, Williams A, Fischer JE, et al: Insulin-like growth factor I (IGF-I) stimulates protein synthesis but does not inhibit protein breakdown in muscle from septic rats. Am J Physiol 1998; 274: R571–R576.

    PubMed  CAS  Google Scholar 

  85. Fang CH, James JH, Ogle C, et al: Influence of burn injury on protein metabolism in different types of skeletal muscle and the role of glucocorticoids. J Am Coll Surg 1995; 180: 33–42.

    PubMed  CAS  Google Scholar 

  86. Fisher CJ, Dhainhaut JFA, Opal SM, et al: Recombinant human interleukin-1 receptor antagonist in the treatment of patients with sepsis syndrome: results from a randomized, double-blind, placebo-controlled trial. JAMA 1994; 271: 1836–1843.

    Article  PubMed  Google Scholar 

  87. Zeni F, Freeman B, Natanson C: Anti-inflammatory therapies to treat sepsis and septic shock: a reassessment. Crit Care Med 1997; 25: 1095–1100.

    Article  PubMed  CAS  Google Scholar 

  88. Breuille D, Farge MC, Rose R, et al: Pentoxifylline decreases the body weight loss and muscle protein wasting during chronic sepsis. Am J Physiol 1994; 268: E636–E641.

    Google Scholar 

  89. Sax HC, Talamini MA, Fischer JE: Clinical use of branched-chain amino acids in liver disease, sepsis, trauma, and burns. Arch Surg 1986; 121: 358–366.

    Article  PubMed  CAS  Google Scholar 

  90. Buse MG, Reid SS: Leucine: a possible regulator of protein turnover in muscle. J Clin Invest 1975; 56: 1250–1261.

    Article  PubMed  CAS  Google Scholar 

  91. Hasselgren PO, James JH, Warner BW, et al: Protein synthesis and degradation in skeletal muscle from septic rats: response to leucine and alpha-ketoisocaproic acid. Arch Surg 1988; 123: 640–644.

    Article  PubMed  CAS  Google Scholar 

  92. MacLennan PA, Brown RA, Rennie MJ: A positive relationship between protein synthetic rate and intracellular glutamine concentration in perfused rat skeletal muscle. FEBS Lett 1987; 215: 187–191.

    Article  PubMed  CAS  Google Scholar 

  93. MacLennan PA, Smith K, Weryk B, et al: Inhibition of protein breakdown by glutamine in perfused rat skeletal muscle, FEBS Lett 1988; 237: 133–136.

    Article  PubMed  CAS  Google Scholar 

  94. Roth E, Funovics J, Muhlbacher F, et al: Metabolic disorders in severe abdominal sepsis: glutamine deficiency in skeletal muscle. Clin Nutr 1982; 1: 25–41.

    Article  PubMed  CAS  Google Scholar 

  95. Hammarqvist F, Wernerman J, Ali R, et al: Addition of glutamine to total parenteral nutrition after elective abdominal surgery spares free glutamine in muscle, counteracts the fall in muscle protein synthesis, and improves nitrogen balance. Ann Surg 1989; 209: 455–461.

    Article  PubMed  CAS  Google Scholar 

  96. Karner J, Roth E, Ollenschlager G, et al: Glutamine-containing dipeptides as infusion substrates in the septic state. Surgery 1989; 106: 893–900.

    PubMed  CAS  Google Scholar 

  97. Fang CH, James JH, Fischer JE, et al: Is muscle protein turnover regulated by intracellular glutamine during sepsis? JPEN J Parenter Enteral Nutr 1995; 19: 279–285.

    Article  PubMed  CAS  Google Scholar 

  98. Kiyama T, Witte MB, Thornton FJ, et al: The route of nutrition support affects the early phase of wound healing. JPENJ Parenter Enteral Nutr 1998; 22: 276–279.

    Article  CAS  Google Scholar 

  99. Evoy D, Lieberman MD, Fahey TJ, et al: Immunonutrition: the role of arginine. Nutrition 1998; 14: 611–617.

    Article  PubMed  CAS  Google Scholar 

  100. Wilmore DW, Shabert JK: Role of glutamine in immunologic responses. Nutrition 1998; 14: 618–626.

    Article  PubMed  CAS  Google Scholar 

  101. Alexander JW: Immunonutrition: the role of omega-3 fatty acids. Nutrition 1998; 14: 627–633.

    Article  PubMed  CAS  Google Scholar 

  102. Lipman TO: Grains or veins: is enteral nutrition really better than parenteral nutrition? A look at the evidence. JPEN J Parenter Enteral Nutr 1998; 22: 167–182.

    Article  PubMed  CAS  Google Scholar 

Download references

Authors

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2000 Springer Science+Business Media New York

About this chapter

Cite this chapter

Pritts, T.A., Fischer, D.R., Hasselgren, PO. (2000). Metabolic Depletion and Failure: Muscle Cachexia During Injury and Sepsis. In: Baue, A.E., Faist, E., Fry, D.E. (eds) Multiple Organ Failure. Springer, New York, NY. https://doi.org/10.1007/978-1-4612-1222-5_38

Download citation

  • DOI: https://doi.org/10.1007/978-1-4612-1222-5_38

  • Publisher Name: Springer, New York, NY

  • Print ISBN: 978-1-4612-7049-2

  • Online ISBN: 978-1-4612-1222-5

  • eBook Packages: Springer Book Archive

Publish with us

Policies and ethics