Hostname: page-component-8448b6f56d-m8qmq Total loading time: 0 Render date: 2024-04-20T04:07:35.527Z Has data issue: false hasContentIssue false

Mild Hypothermia Preserves Contractile Function and Inhibits Prostaglandin E2 Release from Metabolically Stressed Skeletal Muscle

Published online by Cambridge University Press:  18 September 2015

Valerie A. Cwik*
Affiliation:
Division of Neurology, the University of Alberta, Edmonton, Alberta
Ramanath Majumdar
Affiliation:
Division of Neurology, the University of Alberta, Edmonton, Alberta
Michael H. Brooke
Affiliation:
Division of Neurology, the University of Alberta, Edmonton, Alberta
*
Division of Neurology, 2E3.13 Walter MacKenzie Center, University of Alberta, 8440 - 112th Street, Edmonton, Alberta, Canada T6G 2B7
Rights & Permissions [Opens in a new window]

Abstract:

Core share and HTML view are not available for this content. However, as you have access to this content, a full PDF is available via the ‘Save PDF’ action button.

An in vitro model of muscle damage was used to investigate the protective effect of mild hypothermia in muscle injury. Rat epitrochlearis muscles were dissected in their entirety and suspended in Krebs-Ringer solution and DNP, a mitochondrial uncoupler, was added. PGE2, and lactate release and the contractile response to stimulation were measured and compared to untreated controls. Experiments were done at 37, 35, 33 and 27°C. At 37°C, DNP stimulated muscle releases large amounts of PGE2 and lactate and is unable to contract. As the temperature is reduced, there is progressive preservation of contractile force, although high lactate levels at the lowest temperatures indicate that the metabolic stress is still present. In contrast, DNP stimulated PGE2 release is completely inhibited at or below 35°C and may be related to a similar protective phenomenon seen in experimental ischemic neuronal death.

Résumé:

RÉSUMÉ:

Nous avons utilisé un modèle in vitro de lésion musculaire pour investiguer l'effet protecteur d'une légère hypothermie dans le traumatisme musculaire. Des muscles épitrochléens de rat ont été disséqués et suspendus dans une solution de Krebs-Ringer à laquelle du DNP, un découpleur mitochondrial, a été ajouté. La libération de PGE2 et de lactate ainsi que la réponse contractile à la stimulation ont été mesurées et comparées à celles de contrôles non traités. Les essais étaient faits à 37, 35, 33 et 27°C. A 37°C, le muscle stimulé par le DNP libère de grandes quantités de PGE2 et de lactate et il est incapable de se contracter. A mesure que la température est abaissée, on observe une préservation progressive de la force contractile, bien que de fortes concentrations de lactate aux températures les plus basses indiquent que le stress métabolique est encore présent. Par contre, la stimulation de la libération de PGE2 par le DNP est complètement inhibée à des températures de 35°C ou moins et peut être reliée à un phénomène protecteur semblable à celui observé dans la mort neuronale expérimentale par ischémie.

Type
Articles
Copyright
Copyright © Canadian Neurological Sciences Federation 1994

References

REFERENCES

1. Choi, DW. Possible mechanisms limiting N-methyl-D-aspartate receptor overactivation and the therapeutic efficacy of N-methyl-D-aspartate antagonists. Stroke 1990; 21 (Suppl. 11): 11120–2.Google ScholarPubMed
2. Collins, RC, Dobkin, BH, Choi, DW. Selective vulnerability of the brain: new insights into the pathophysiology of stroke. Ann Intern Med 1989; 110: 9921000.CrossRefGoogle ScholarPubMed
3. Albers, GW, Goldberg, MP, Choi, DW. N-methyl-D-aspartate antagonists: ready for clinical trial in brain ischemia? Ann Neurol 1989; 25: 398403.CrossRefGoogle ScholarPubMed
4. Lipton, SA. Calcium channel antagonists in the prevention of neurotoxicity. Adv Pharmacol 1991; 22: 271297.CrossRefGoogle ScholarPubMed
5. Lieberman, A (ed.). Emerging perspectives in Parkinson’s disease. Neurology 1992; 42 (Suppl): 4148.Google ScholarPubMed
6. Oppenheim, RW. Motor neuron diseases: high hopes for a trophic factor. Nature 1992; 358: 451452.CrossRefGoogle ScholarPubMed
7. Sendtner, M, Schmalbruch, K, Stockli, KA, et al. Ciliary neurotrophic factor prevents degeneration of motor neurons in mouse mutant progressive motor neuronopathy. Nature 1992; 358: 502505.CrossRefGoogle ScholarPubMed
8. Jackson, MJ, Edwards, RH. Free radicals and trials of antioxidant therapy in muscle diseases. Adv Exp Med Biol 1990; 264: 485491.CrossRefGoogle ScholarPubMed
9. Sutherland, GR, Lesiuk, H, Hazendonk, P, et al. Magnetic resonance imaging and 3IP magnetic resonance spectroscopy study of the effect of temperature on ischemic brain injury. Can J Neurol Sci 1992; 19: 317325.CrossRefGoogle Scholar
10. Clifton, GL, Jiang, JY, Lyeth, BG, et al. Marked protection by moderate hypothermia after experimental traumatic brain injury. J Cereb Blood Flow Metab 1991; 11: 114121.CrossRefGoogle ScholarPubMed
11. Busto, R, Dietrich, WD, Globus, MY-T, et al. Small differences in intraischemic brain temperature critically determine the extent of ischemic neuronal injury. J Cereb Blood Flow Metab 1987; 7: 729738.CrossRefGoogle ScholarPubMed
12. Minamisawa, H, Smith, M-L, Siejso, BK. The effect of mild hyperthermia and hypothermia on brain damage following 5, 10, and 15 minutes of forebrain ischemia. Ann Neurol 1990; 28: 2633.CrossRefGoogle ScholarPubMed
13. Young, RSK, Olenginski, TP, Yagel, SK, Towfighi, J. The effect of graded hypothermia on hypoxic-ischemic brain damage: a neuropathological study in the neonatal rat. Stroke 1983; 14: 929934.CrossRefGoogle Scholar
14. Welsh, FA, Sims, RE, Harris, VA. Mild hypothermia prevents ischemic injury in gerbil hippocampus. J Cereb Blood Flow Metab 1990; 10: 557563.CrossRefGoogle ScholarPubMed
15. Connolly, JE, Boyd, RJ, Calvin, JW. The protective effect of hypothermia in cerebral ischemia: experimental and clinical application by selective brain cooling in the human. Surgery 1962; 52: 1524.Google ScholarPubMed
16. Uihlein, A, MacCarty, CS, Michenfelder, JD, Terry, HR, Daw, EF. Deep hypothermia and surgical treatment of intracranial aneurysms. JAMA 1966; 195: 127129.CrossRefGoogle ScholarPubMed
17. Siebke, H, Breivik, H, Rod, T, Lind, B. Survival after 40 minutes’ submersion without cerebral sequelae. Lancet 1975; 1: 12751277.CrossRefGoogle Scholar
18. Sekar, TS, MacDonnell, KF, Namsirikul, P, Herman, RS. Survival after prolonged submersion in cold water without neurologic sequelae. Arch Intern Med 1980; 140: 775779.CrossRefGoogle ScholarPubMed
19. Nesher, R, Karl, IE, Kaiser, KE, Kipnis, DM. Epitrochlearis muscle. I. Mechanical performance, energetics, and fiber composition. Am J Physiol 1980; 239: E454-E460.Google ScholarPubMed
20. Brooke, MH, Choski, R, Kaiser, KK. Inosine monophosphate production is proportional to muscle force in vitro. Neurology 1986; 36: 288291.CrossRefGoogle ScholarPubMed
21. Lowry, OH, Passonneau, JV. A flexible system of enzymatic analysis. Orlando, FL: Academic Press, 1972.Google Scholar
22. Allen, FM. Surgical considerations of temperature in ligated limbs. Am J Surg 1939; 45: 459464.CrossRefGoogle Scholar
23. Ikemoto, Y, Kobayashi, H, Usui, M, Ishii, S. Changes in serum myoglobin levels caused by tourniquet ischemia under normothermic and hypothermic conditions. Clin Orthop 1988; 234: 296302.CrossRefGoogle Scholar
24. Swanson, AB, Livengood, LC, Sattel, AB. Local hypothermia to prolong safe tourniquet time. Clin Orthop 1991; 264: 200208.CrossRefGoogle Scholar
25. Tamai, S. Digit replantation: analysis of 163 replantations in an 11 year period. Clin Plast Surg 1978; 5: 195209.CrossRefGoogle Scholar
26. Sapega, AA, Heppenstall, RB, Sokolow, DP, et al. The bioenergetics of preservation of limbs before replantation. J Bone Joint Surg 1988; 70-A: 15001513.CrossRefGoogle ScholarPubMed
27. McMaster, WC, Liddle, S. Cryotherapy influence on posttraumatic limb edema. Clin Orthop 1980; 150: 283287.CrossRefGoogle Scholar
28. Wright, JG, Kerr, JC, Valeri, CR, Hobson, RW. Regional hypothermia protects against ischemia-reperfusion injury in isolated canine gracilis muscle. J Trauma 1988; 28: 10261031.CrossRefGoogle ScholarPubMed
29. Presta, M, Ragnotti, G. Quantification of damage to striated muscle after normothermic or hypothermic ischemia. Clin Chem 1981; 27: 297302.CrossRefGoogle ScholarPubMed
30. Wright, JG, Araki, CT, Belkin, M, Hobson, RW. Postischemic hypothermia diminishes skeletal muscle reperfusion edema. J Surg Res 1989; 47: 389396.CrossRefGoogle ScholarPubMed
31. Norwood, WI, Norwood, CR. Influence of hypothermia on intracellular pH during anoxia. Am J Physiol 1982; 243: C62-C65.CrossRefGoogle ScholarPubMed
32. Berntman, L, Welsh, FA, Harp, JR. Cerebral protective effect of lowgrade hypothermia. Anesthesiology 1981; 55: 495498.CrossRefGoogle Scholar
33. Harris, K, Walker, PM, Mickle, DAG, et al. Metabolic response of skeletal muscle to ischemia. Am J Physiol 1986; 250: H213-H220.Google ScholarPubMed
34. Edgar, AD, Strosznajder, J, Horrocks, LA. Activation of ethanolamine phospholipase A2 in brain during ischemia. J Neurochem 1982; 39: 11111116.CrossRefGoogle ScholarPubMed
35. Dempsey, RJ, Roy, MW, Meyer, K, Cowen, DE, Tai, H-H. Development of cyclooxygenase and lipoxygenase metabolites of arachidonic acid after transient cerebral ischemia. J Neurosurg 1986; 64: 118124.CrossRefGoogle ScholarPubMed
36. Moskowitz, MA, Kiwak, KJ, Hekimian, K, Levine, L. Synthesis of compounds with properties of leukotrienes C4 and D4 in gerbil brains after ischemia and reperfusion. Science 1984; 224: 886889.CrossRefGoogle ScholarPubMed
37. Yoshida, S, Inoh, S, Asano, T, et al. Effect of transient ischemia on free fatty acids and phospholipids in the gerbil brain. J Neurosurg 1980; 53: 323331.CrossRefGoogle ScholarPubMed
38. Gaudet, RJ, Alam, I, Levine, L. Accumulation of cyclooxygenase products of arachidonic acid metabolism in gerbil brain during reperfusion after bilateral common carotid artery occlusion. J Neurochem 1980; 35: 653658.CrossRefGoogle ScholarPubMed
39. Dempsey, RJ, Combs, DJ, Maley, ME, et al. Moderate hypothermia reduces postischemic edema development and leukotriene production. Neurosurgery 1987; 21: 177181.CrossRefGoogle ScholarPubMed
40. Miller, LP, Hsu, C. Therapeutic potential for adenosine receptor activation in ischemic brain injury. J Neurotrauma 1992; 9 (Suppl 2): S563-S577.Google ScholarPubMed
41. Park, CK, Nehls, DG, Graham, DI, Teasdale, GM, McCulloch, J. The glutamate antagonist MK-801 reduces focal ischemic brain damage in the rat. Ann Neurol 1988; 24: 543551.CrossRefGoogle ScholarPubMed
42. Simon, R, Shiraishi, K. N-methyl-D-aspartate antagonist reduces stroke size and regional glucose metabolism. Ann Neurol 1990; 27: 606611.CrossRefGoogle ScholarPubMed
43. Buchan, A, Pulsinelli, WA. Hypothermia but not the N-methyl-D-aspartate antagonist, MK-801, attenuates neuronal damage in gerbils subjected to transient global ischemia. J Neuroscience 1990; 10: 311316.CrossRefGoogle Scholar
44. Duncan, CJ, Jackson, MJ. Different mechanisms mediate structural changes and intracellular enzyme efflux following damage to skeletal muscle. J Cell Sci 1987; 87: 183188.CrossRefGoogle ScholarPubMed
45. Jackson, MJ, Wagenmakers, AJM, Edwards, RHT. Effect of inhibitors of arachidonic acid metabolism on efflux of intracellular enzymes from skeletal muscle following experimental damage. Biochem J 1987; 241: 403407.CrossRefGoogle ScholarPubMed
46. Phoenix, J, Edwards, RHT, Jackson, MJ. Inhibition of Ca2+ -induced cytosolic enzyme efflux from skeletal muscle by vitamin E and related compounds. Biochem J 1989; 257: 207213.CrossRefGoogle ScholarPubMed
47. Jones, DA, Jackson, MJ, McPhail, G, Edwards, RHT. Experimental mouse muscle damage: the importance of external calcium. Clin Sci 1984; 66: 317322.CrossRefGoogle ScholarPubMed
48. Vandenburgh, HH, Hatfaludy, S, Sohar, I, Shansky, J. Stretch-induced prostaglandins and protein turnover in cultured skeletal muscle. Am J Physiol 1990; 259: C232-C240.CrossRefGoogle ScholarPubMed
49. Baracos, V, Rodemann, HP, Dinarello, CA, Goldberg, AL. Stimulation of muscle protein degradation and prostaglandin E, release by leukocytic pyrogen (interleukin-1). ? Engl J Med 1983; 308: 553558.CrossRefGoogle Scholar
50. Rodemann, HP, Goldberg, AL. Arachidonic acid, prostaglandin E2 and F2a influence rates of protein turnover in skeletal and cardiac muscle. J Biol Chem 1982; 257: 16321638.CrossRefGoogle Scholar
51. Jackson, MJ, Brooke, MH, Kaiser, K, Edwards, RHT. Creatine kinase release and prostaglandin E2 release from isolated Duchenne muscle. Neurology 1991; 41: 101104.CrossRefGoogle ScholarPubMed
52. Kariman, K, Chance, B, Burkhart, DS, Bolinger, LA. Uncoupling effects of 2,4-dinitrophenol on electron transfer reactions and cell bioenergetics in rat brain in situ. Brain Res 1986; 366: 300306.CrossRefGoogle ScholarPubMed
53. Heller, SL, Brooke, MH, Kaiser, KK, Choski, R. 2,4-Dinitrophenol, muscle biopsy, and McArdle’s disease. Neurology 1988; 38: 1519.CrossRefGoogle ScholarPubMed
54. Melemd, C, Karpati, G, Carpenter, S. Experimental mitochondrial myopathy produced by in vivo uncoupling of oxidative phosphorylation. J Neurol Sci 1975; 26: 305318.CrossRefGoogle Scholar