Skip to main content

Characterization of the alteration of nutritional state in brain injury induced by fluid percussion in rats

Intensive Care Medicine volume 31, pages 281–288 (2005)Cite this article

Abstract

Objective

Patients suffering from traumatic brain injury (TBI) undergo rapid weight loss with negative nitrogen balance and enhanced whole-body protein breakdown, with protein wasting causing morbidity and increased mortality. Many experimental models of TBI have been used to evaluate strategies to improve the outcome of these patients, but nutritional status has not been considered in experiments published to date, although this may have great importance and influence the results obtained with TBI models. This study characterized the hypercatabolism level and nutritional status of TBI rats.

Design

Twenty-four male Wistar rats were randomized into three groups. Rats from the TBI group were anesthetized and fluid percussion was applied. The pair-fed (PF) group was healthy but was pair-fed to the TBI group. The ad libitum (AL) group was healthy and fed ad libitum. The study was performed over 10 days post-TBI.

Measurements and results

TBI in rats was characterized by remarkable long-lasting anorexia, renal failure (creatinine clearance: AL 1.8±0.2 and PF 1.5±0.1 vs. TBI 0.9±0.1 l/24 hour), anorexia (appetite depressed throughout the study), increased myofibrillar proteolysis (3-methylhistidine/creatinine ratio (day 2: AL 36±1 and PF 38±2 vs. TBI 54±5 µmol/mmol), and intestinal atrophy (ileum: AL 29.3±2.5 and PF 28.7±1.1 vs. TBI 22.5±1.4 mg/cm). In addition, anorexia led to muscular atrophy and decreased nitrogen balance. The metabolic alterations described above can increase morbidity and mortality.

Conclusions

TBI by fluid percussion in rats is a model reproducing the metabolic and nutritional alterations observed in clinical practice and is suitable for further studies exploring the efficacy of optimized nutritional support.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

43,34 €

Price includes VAT (Finland)
Tax calculation will be finalised during checkout.

Fig. 1
Fig. 2
Fig. 3

Reference

  1. Mansoor O, Beaufrere B, Boirie Y, Ralliere C, Taillandier D, Aurousseau E, Schoeffler P, Arnal M, Attaix D (1996) Increased mRNA levels for components of the lysosomal, Ca2+-activated, and ATP-ubiquitin-dependent proteolytic pathways in skeletal muscle from head trauma patients. Proc Natl Acad Sci U S A 93:2714–2718

    Article  CAS  PubMed  Google Scholar 

  2. Herndon DN, Hart DW, Wolf SE, Chinkes DL, Wolfe RR (2001) Reversal of catabolism by beta-blockade after severe burns. N Engl J Med 345:1223–1229

    Article  CAS  PubMed  Google Scholar 

  3. Vary TC, Kimball SR (1992) Regulation of hepatic protein synthesis in chronic inflammation and sepsis. Am J Physiol 262:C445–C452

    CAS  PubMed  Google Scholar 

  4. Alexander JW (1995) Specific nutrients and the immune response. Nutrition 11:229–232

    CAS  PubMed  Google Scholar 

  5. Jeevanandam M (1995) Trauma and sepsis. In: Cynober L (ed). Amino acid metabolism and therapy in health and nutritional disease. CRC Press, pp 245–255

  6. Piot-Grosjean O, Wahl F, Gobbo O, Stutzmann JM (2001) Assessment of sensorimotor and cognitive deficits induced by a moderate traumatic injury in the right parietal cortex of the rat. Neurobiol Dis 8:1082–1093

    Article  CAS  PubMed  Google Scholar 

  7. Bareyre F, Wahl F, McIntosh TK, Stutzmann JM (1997) Time course of cerebral edema after traumatic brain injury in rats: effects of riluzole and mannitol. J Neurotrauma 14:839–849

    CAS  PubMed  Google Scholar 

  8. Mendez C, Jurkovich GJ, Wener MH, Garcia I, Mays M, Maier RV (1996) Effects of supplemental dietary arginine, canola oil, and trace elements on cellular immune function in critically injured patients. Shock 6:7–12

    CAS  PubMed  Google Scholar 

  9. Wischmeyer PE, Kahana M, Wolfson R, Ren H, Musch MM, Chang EB (2001) Glutamine reduces cytokine release, organ damage, and mortality in a rat model of endotoxemia. Shock 16:398–402

    CAS  PubMed  Google Scholar 

  10. Toulmond S, Duval D, Serrano A, Scatton B, Benavides J (1993) Biochemical and histological alterations induced by fluid percussion brain injury in the rat. Brain Res 620:24–31

    Article  CAS  PubMed  Google Scholar 

  11. Wahl F, Renou E, Mary V, Stutzmann JM (1997) Riluzole reduces brain lesions and improves neurological function in rats after a traumatic brain injury. Brain Res 756:247–255

    Article  CAS  PubMed  Google Scholar 

  12. Maltin CA, Delday MI, Baillie AGS, Grubb DA, Garlick PJ (1989) Fiber-type composition of nine rat muscles I. Changes during the first year of life. Am J Physiol 257:E823–E827

    CAS  PubMed  Google Scholar 

  13. Hasselgren PO, Hall-Angeras M, Angeras U, Benson D, James JH, Fischer JE (1990) Regulation of total and myofibrillar protein breakdown in rat extensor digitorum longus and soleus muscle incubated flaccid or at resting length. Biochem J 267:37–44

    CAS  PubMed  Google Scholar 

  14. Fleury P, Aberham R (1951) Recherche sur le dosage des protéines par la méthode photométrique du Biuret selon la technique de Gornall. Ann Biol Clin (Paris) 9:453–466

    Google Scholar 

  15. Sjölin J, Stjernström H, Henneberg S, Andersson E, Martensson J, Friman G, Larsson J (1989) Splanchnic and peripheral release of 3-methylhistidine in relation to its urinary excretion in human infection. Metabolism 38:23–29

    Article  PubMed  Google Scholar 

  16. Long CL, Birkhahn RH, Geiger JW, Betts JE, Schiller WR, Blakemore WS (1981) Urinary excretion of 3-methylhistidine: an assessment of muscle protein catabolism in adult normal subjects and during malnutrition, sepsis, and skeletal trauma. Metabolism 30:765–776

    Article  CAS  PubMed  Google Scholar 

  17. Le Boucher J, Charret C, Coudray-Lucas C, Giboudeau J, Cynober L (1997) Amino acid determination in biological fluids by automated ion-exchange chromatography: performance of Hitachi L-8500A. Clin Chem 43:1421–1428

    PubMed  Google Scholar 

  18. Young VR, Munro HN (1978) N-Methylhistidine (3-methylhistidine) and muscle protein turnover: an overview. Fed Proc 37:2291–2300

    CAS  PubMed  Google Scholar 

  19. Blanc MC, Neveux N, Laromiguiere M, Berard MP, Cynober L (2000) Evaluation of a newly available biochemical analyzer: the Olympus AU 600. Clin Chem Lab Med 38:465–475

    Article  CAS  PubMed  Google Scholar 

  20. Martindale RG, Cresci GA (2001) The use of immune enhancing diet in head injury. JPEN J Parenter Enteral Nutr 25:S27–S28

    CAS  PubMed  Google Scholar 

  21. Schlegel L, Coudray-Lucas C, Barbut F, Le Boucher J, Pernet P, Cynober L (1999) Bacterial dissemination, rather than translocation, mediates hypermetabolic response in endotoxemic rats. Crit Care Med 27:1511–1516

    Article  CAS  PubMed  Google Scholar 

  22. Breuille D, Voisin L, Contrepois M, Arnal M, Rose F, Obled C (1999) A sustained rat model for studying the long-lasting catabolic state of sepsis. Infect Immun 67:1079–1085

    CAS  PubMed  Google Scholar 

  23. Kaiyala KJ, Woods SC, Schwartz MW (1995) New model for the regulation of energy balance and adiposity by the central nervous system. Am J Clin Nutr 62:1123S-1134S

    CAS  PubMed  Google Scholar 

  24. Le Boucher J, Obled C, Farges MC, Cynober L (1997) Ornithine alpha-ketoglutarate modulates tissue protein metabolism in burn-injured rats. Am J Physiol 273:557–E563

    Google Scholar 

  25. Cooney RN, Kimball SR, Vary TC (1997) Regulation of skeletal muscle protein turnover during sepsis: mechanisms and mediators. Shock 7:1–16

    PubMed  Google Scholar 

  26. Minet-Quinard R, Moinard C, Walrand S, Villie F, Vasson MP, Davot P, Chopineau J, Cynober L (2000) Induction of a catabolic state in rats by dexamethasone: dose or time dependancy? JPEN J Parenter Enteral Nutr 24:30–36

    CAS  PubMed  Google Scholar 

  27. Druml W, Fischer M, Liebisch B, Lenz K, Roth E (1994) Elimination of amino acids in renal failure. Am J Clin Nutr 60:418–423

    CAS  PubMed  Google Scholar 

  28. Souba WW, Austgen TR (1990) Interorgan glutamine flow following surgery and infection. JPEN J Parenter Enteral Nutr 14 [Suppl]:90S–93S

    Google Scholar 

  29. Austgen TR, Chakrabarti R, Chen MK, Souba WW (1992) Adaptive regulation in skeletal muscle glutamine metabolism in endotoxin-treated rats. J Trauma 32:600–607

    CAS  PubMed  Google Scholar 

  30. Parry-Billings M, Leighton B, Dimitriadis GD, De Vasconcelos PRL, Newsholme EA (1989) Skeletal muscle glutamine metabolism during sepsis in the rat. Int J Biochem 21:419–423

    Article  CAS  PubMed  Google Scholar 

  31. Parry-Billings P, Evans J, Calder PC, Newsholme EA (1990) Does glutamine contribute to immunosuppression after major burns? Lancet 336:523–525

    Article  CAS  PubMed  Google Scholar 

  32. Fischer CP, Bode BP, Abcouver SF, Lukaszewicz GC, Souba WW (1995) Hepatic uptake of glutamine and other amino acids during infection and inflammation. Shock 3:315–322

    CAS  PubMed  Google Scholar 

  33. Levillain O, Parvy P, Hassler C (1997) Amino acid handling in uremic rats: citrulline, a reliable marker of renal insufficiency and proximal tubular dysfunction. Metabolism 46:611–618

    Article  CAS  PubMed  Google Scholar 

  34. Cano N (1990) Métabolisme des acides aminés au cours de l’insuffisance rénale chronique. Nutr Clin Métabol 4:151–162

    Google Scholar 

  35. Chambon-Savanovitch C, Felgines C, Farges MC, Pernet P, Cezard J, Raul F, Cynober L, Vasson MP (1999) Severe dietary restriction initiated in aged rats: evidence for poor adaptation in terms of protein metabolism and intestinal functions. Eur J Clin Invest 29:504–511

    Article  CAS  PubMed  Google Scholar 

  36. Felgines C, Savanovitch C, Farges MC, Cynober L, Vasson MP (1999) Protein metabolism in rats during long-term dietary restriction: influence of aging. JPEN J Parenter Enteral Nutr 23:32–37

    CAS  PubMed  Google Scholar 

  37. Holt PR, Wu S, Yeh KY (1986) Ileal hyperplastic response to starvation in the rat. Am J Physiol 251:124–G131

    Google Scholar 

  38. Cynober L (1989) Amino acid metabolism in thermal burns. JPEN J Parenter Enteral Nutr 13:196–205

    CAS  PubMed  Google Scholar 

Download references

Author information

Affiliations

  1. Laboratoire de Biologie de la Nutrition EA 2498, Faculté de Pharmacie, 4 avenue de l’Observatoire, 75270, Paris Cedex 06, France

    Christophe Moinard, Nathalie Neveux, Carine Genthon & Luc Cynober

  2. Laboratoire de Biochimie A, Hotel Dieu, Assistance Publique Hôpitaux de Paris, Paris, France

    Nathalie Neveux

  3. Laboratoire de pharmacologie de la circulation cérébrale EA 2510, Faculté de Pharmacie, Paris 5, Paris, France

    Nicolas Royo, Catherine Marchand-Verrecchia & Michel Plotkine

Authors
  1. Christophe Moinard
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Nathalie Neveux
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Nicolas Royo
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Carine Genthon
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Catherine Marchand-Verrecchia
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Michel Plotkine
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Luc Cynober
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Christophe Moinard.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Moinard, C., Neveux, N., Royo, N. et al. Characterization of the alteration of nutritional state in brain injury induced by fluid percussion in rats. Intensive Care Med 31, 281–288 (2005). https://doi.org/10.1007/s00134-004-2489-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00134-004-2489-9

Keywords

  • Trauma
  • Hypercatabolism
  • Amino acids
  • Muscles
  • Intestine and renal failure