Heat stroke: Role of the systemic inflammatory response

Journal of Applied Physiology

Volumn 109, Issue 6, 2010, Pages 1980-1988

  Leon, Lisa R ^a   Helwig, Bryan G ^a  

^a U S ARMY RESEARCH INSTITUTE OF ENVIRONMENTAL MEDICINE   (United States)

Author keywords

Cytokines; Exertional heat stroke; Heat stress; Hyperthermia; Systemic inflammatory response syndrome

Indexed keywords

AUTACOID;

AGE; AGING; ANIMAL; FITNESS; HEAT STROKE; HUMAN; IMMUNOLOGY; INCIDENCE; METABOLISM; MORTALITY; MULTIPLE ORGAN FAILURE; PATHOPHYSIOLOGY; REVIEW; SYSTEMIC INFLAMMATORY RESPONSE SYNDROME; THERMOREGULATION; TREATMENT OUTCOME;

AGE FACTORS; AGING; ANIMALS; BODY TEMPERATURE REGULATION; HEAT STROKE; HUMANS; INCIDENCE; INFLAMMATION MEDIATORS; MULTIPLE ORGAN FAILURE; PHYSICAL FITNESS; SYSTEMIC INFLAMMATORY RESPONSE SYNDROME; TREATMENT OUTCOME;

EID: 78149346372     PISSN: 87507587     EISSN: 15221601     Source Type: Journal    
DOI: 10.1152/japplphysiol.00301.2010     Document Type: Review

References (90)

1. Argaud L, Ferry T, Le QH, Marfisi A, Ciorba D, Achache P, Ducluzeau R, Robert D. Short-and long-term outcomes of heatstroke following the 2003 heat wave in Lyon, France. Arch Intern Med 167:2177-2183, 2007.
2. Asakura H, Suga Y, Yoshida T, Ontachi Y, Mizutani T, Kato M, Ito T, Morishita E, Yamazaki M, Miyamoto K, Nakao S. Pathophysiology of disseminated intravascular coagulation (DIC) progresses at a different rate in tissue factor-induced and lipopolysaccharide-induced DIC models in rats. Blood Coagul Fibrinolysis 14:221-228, 2003.
3. Bagley WH, Yang H, Shah KH. Rhabdomyolysis. Intern Emerg Med 2:210-218, 2007.
4. Barbui T, Falanga A. Disseminated intravascular coagulation in acute leukemia. Semin Thromb Hemost 27:593-604, 2001.
5. Bernard GR, Vincent JL, Laterre PF, LaRosa SP, Dhainaut JF, Lopez-Rodriguez A, Steingrub JS, Garber GE, Helterbrand JD, Ely EW, Fisher CJ Jr. Efficacy and safety of recombinant human activated protein C for severe sepsis. N Engl J Med 344:699-709, 2001.
6. Borden KA, Cutter SL. Spatial patterns of natural hazards mortality in the United States. Int J Health Geogr 7:64-76, 2008.
7. Bouchama A, Al-Sedairy S, Siddiqui S, Shail E, Rezeig M. Elevated pyrogenic cytokines in heatstroke. Chest 104:1498-1502, 1993.
8. Bouchama A, Hammami MM, Haq A, Jackson J, Al-Sedairy S. Evidence for endothelial cell activation/injury in heatstroke. Crit Care Med 24:1173-1178, 1996.
9. Bouchama A, Knochel JP. Heat stroke. N Engl J Med 346:1978-1988, 2002.
10. Bouchama A, Kunzelmann C, Dehbi M, Kwaasi A, Eldali A, Zobairi F, Freyssinet JM, de Prost D. Recombinant activated protein C attenuates endothelial injury and inhibits procoagulant microparticles release in baboon heatstroke. Arterioscler Thromb Vasc Biol 28:1318-1325, 2008.
11. Bouchama A, Ollivier V, Roberts G, Al MF, de Prost D, Eldali A, Saussereau E, El-Sayed R, Chollet-Martin S. Experimental heatstroke in baboon: analysis of the systemic inflammatory response. Shock 24:332-335, 2005.
12. Bouchama A, Parhar RS, el-Yazigi A, Sheth K, Al-Sedairy S. Endotoxemia and release of tumor necrosis factor and interleukin 1 alpha in acute heatstroke. J Appl Physiol 70:2640-2644, 1991.
13. Bouchama A, Roberts G, Al MF, El-Sayed R, Lach B, Chollet-Martin S, Ollivier V, Al BR, Loualich A, Nakeeb S, Eldali A, de Prost D. Inflammatory, hemostatic, and clinical changes in a baboon experimental model for heatstroke. J Appl Physiol 98:697-705, 2005.
14. Boulant JA. Hypothalamic neurons regulating body temperature. In: Handbook of Physiology, Section 4: Environmental Physiology. Bethesda, MD: Am Physiol Soc, 1996, p. 105-125.
15. Bradfield JW. Control of spillover. The importance of Kupffer-cell function in clinical medicine. Lancet 2:883-886, 1974.
16. Broessner G, Beer R, Franz G, Lackner P, Engelhardt K, Brenneis C, Pfausler B, Schmutzhard E. Case report: severe heat stroke with multiple organ dysfunction-a novel intravascular treatment approach. Crit Care 9: R498-R501, 2005.
17. Bynum G, Brown J, Dubose D, Marsili M, Leav I, Pistole TG, Hamlet M, LeMaire M, Caleb B. Increased survival in experimental dog heatstroke after reduction of gut flora. Aviat Space Environ Med 50:816-819, 1979.
18. Carter R, III, Cheuvront SN, Williams JO, Kolka MA, Stephenson LA, Sawka MN, Amoroso PJ. Epidemiology of hospitalizations and deaths from heat illness in soldiers. Med Sci Sports Exerc 37:1338-1344, 2005.
19. CDC. Heat-Related Mortality-Arizona, 1993-2002, and United States, 1979-2002. Morbid Mortal Weekly 54:628-630, 2005.
20. CDC. Heat-Related Deaths-United States, 1999-2003. Morbid Mortal Weekly 55:796-798, 2006.
21. Chang DM. The role of cytokines in heat stroke. Immunol Invest 22:553-561, 1993.
22. Chao TC, Sinniah R, Pakiam JE. Acute heat stroke deaths. Pathology 13:145-156, 1981.
23. Chen CM, Hou CC, Cheng KC, Tian RL, Chang CP, Lin MT. Activated protein C therapy in a rat heat stroke model. Crit Care Med 34:1960-1966, 2006.
24. Deitch EA. Animal models of sepsis and shock: a review and lessons learned. Shock 9:1-11, 1998.
25. Dematte JE, O'Mara K, Buescher J, Whitney CG, Forsythe S, McNamee T, Adiga RB, Ndukwu IM. Near-fatal heat stroke during the 1995 heat wave in Chicago. Ann Intern Med 129:173-181, 1998.
26. Dokladny K, Moseley PL, Ma TY. Physiologically relevant increase in temperature causes an increase in intestinal epithelial tight junction permeability. Am J Physiol Gastrointest Liver Physiol 290: G204-G212, 2006.
27. Donoghue ER, Graham MA, Jentzen JM, Lifschultz BD, Luke JL, Mirchandani HG. Criteria for the diagnosis of heat-related deaths: National Association of Medical Examiners. Position paper. National Association of Medical Examiners Ad Hoc Committee on the Definition of Heat-Related Fatalities. Am J Forensic Med Pathol 18:11-14, 1997.
28. Dorozynski A. Chirac announces investigation into heat wave's death toll. BMJ 327:465, 2003.
29. Drobatz KJ, Macintire DK. Heat-induced illness in dogs: 42 cases (1976-1993). J Am Vet Med Assoc 209:1894-1899, 1996.
30. DuBose DA, Basamania K, Maglione L, Rowlands J. Role of bacterial endotoxins of intestinal origin in rat heat stress mortality. J Appl Physiol 54:31-36, 1983.
31. Gader AM, al-Mashhadani SA, al-Harthy SS. Direct activation of platelets by heat is the possible trigger of the coagulopathy of heat stroke. Br J Haematol 74:86-92, 1990.
32. Gathiram P, Wells MT, Brock-Utne JG, Gaffin SL. Antilipopolysaccharide improves survival in primates subjected to heat stroke. Circ Shock 23:157-164, 1987.
33. Giercksky T, Boberg KM, Farstad IN, Halvorsen S, Schrumpf E. Severe liver failure in exertional heat stroke. Scand J Gastroenterol 34:824-827, 1999.
34. Goddard CJ, Warnes TW. Raised liver enzymes in asymptomatic patients: investigation and outcome. Dig Dis 10:218-226, 1992.
35. Graber CD, Reinhold RB, Breman JG, Harley RA, Hennigar GR. Fatal heat stroke. Circulating endotoxin and gram-negative sepsis as complications. JAMA 216:1195-1196, 1971.
36. Hall DM, Buettner GR, Oberley LW, Xu L, Matthes RD, Gisolfi CV. Mechanisms of circulatory and intestinal barrier dysfunction during whole body hyperthermia. Am J Physiol Heart Circ Physiol 280: H509-H521, 2001.
37. Hammami MM, Bouchama A, Al-Sedairy S, Shail E, AlOhaly Y, Mohamed GE. Concentrations of soluble tumor necrosis factor and interleukin-6 receptors in heatstroke and heatstress. Crit Care Med 25:1314-1319, 1997.
38. Hashim IA, Al-Zeer A, Al-Shohaib S, Al-Ahwal M, Shenkin A. Cytokine changes in patients with heatstroke during pilgrimage to Makkah. Mediators Inflamm 6:135-139, 1997.
39. Hassanein T, Perper JA, Tepperman L, Starzl TE, Van Thiel DH. Liver failure occurring as a component of exertional heatstroke. Gastroenterology 100:1442-1447, 1991.
40. Hassanein T, Razack A, Gavaler JS, Van Thiel DH. Heatstroke: its clinical and pathological presentation, with particular attention to the liver. Am J Gastroenterol 87:1382-1389, 1992.
41. Huisse MG, Pease S, Hurtado-Nedelec M, Arnaud B, Malaquin C, Wolff M, Gougerot-Pocidalo MA, Kermarrec N, Bezeaud A, Guillin MC, Paoletti X, Chollet-Martin S. Leukocyte activation: the link between inflammation and coagulation during heatstroke. A study of patients during the 2003 heat wave in Paris. Crit Care Med 36:2288-2295, 2008.
42. Hutchison VH. Critical thermal maxima in salamanders. Physiol Zool 34:92-125, 1961.
43. Inoue Y, Shibasaki M, Ueda H, Ishizashi H. Mechanisms underlying the age-related decrement in the human sweating response. Eur J Appl Physiol Occup Physiol 79:121-126, 1999.
44. Kenney MJ, Fels RJ. Sympathetic nerve regulation to heating is altered in senescent rats. Am J Physiol Regul Integr Comp Physiol 283: R513-R520, 2002.
45. Kew M, Bersohn I, Seftel H, Kent G. Liver damage in heatstroke. Am J Med 49:192-202, 1970.
46. Khogali M. Epidemiology of heat illnesses during the Makkah Pilgrimages in Saudi Arabia. Int J Epidemiol 12:267-273, 1983.
47. Kilbourne EM, Choi K, Jones TS, Thacker SB. Risk factors for heatstroke. A case-control study. JAMA 247:3332-3336, 1982.
48. Knupfer H, Preiss R. sIL-6R: more than an agonist? Immunol Cell Biol 86:87-91, 2008.
49. Lambert GP, Gisolfi CV, Berg DJ, Moseley PL, Oberley LW, Kregel KC. Selected contribution: Hyperthermia-induced intestinal permeability and the role of oxidative and nitrosative stress. J Appl Physiol 92:1750-1761, 2002.
50. Leon LR. Heat stroke and cytokines. Prog Brain Res 162:481-524, 2007.
51. Leon LR, Blaha MD, DuBose DA. Time course of cytokine, corticosterone, and tissue injury responses in mice during heat strain recovery. J Appl Physiol 100:1400-1409, 2006.
52. Leon LR, DuBose DA, Mason CW. Heat stress induces a biphasic thermoregulatory response in mice. Am J Physiol Regul Integr Comp Physiol 288: R197-R204, 2005.
53. Leon LR, Gordon CJ, Helwig BG, Rufolo DM, Blaha MD. Thermoregulatory, behavioral, and metabolic responses to heat stroke in a conscious mouse model. Am J Physiol Regul Integr Comp Physiol 299: R241-R248, 2010.
54. Leon LR, White AA, Kluger MJ. Role of IL-6 and TNF in thermoregulation and survival during sepsis in mice. Am J Physiol Regul Integr Comp Physiol 275: R269-R277, 1998.
55. Line RL, Rust GS. Acute exertional rhabdomyolysis. Am Fam Physician 52:502-506, 1995.
56. Lu KC, Wang JY, Lin SH, Chu P, Lin YF. Role of circulating cytokines and chemokines in exertional heatstroke. Crit Care Med 32:399-403, 2004.
57. Luterbacher J, Dietrich D, Xoplaki E, Grosjean M, Wanner H. European seasonal and annual temperature variability, trends, and extremes since 1500. Science 303:1499-1503, 2004.
58. Malamud N, Haymaker W, Custer RP. Heat Stroke: clinico-pathologic study of 125 fatal cases. Mil Surg 99:397-449, 1946.
59. Maron MB, Wagner JA, Horvath SM. Thermoregulatory responses during competitive marathon running. J Appl Physiol 42:909-914, 1977.
60. McClung JP, Hasday JD, He JR, Montain SJ, Cheuvront SN, Sawka MN, Singh IS. Exercise-heat acclimation in humans alters baseline levels and ex vivo heat inducibility of HSP72 and HSP90 in peripheral blood mononuclear cells. Am J Physiol Regul Integr Comp Physiol 294: R185-R191, 2008.
61. Mendeloff AI, Smith DE. Extreme physical effort in summer heat followed by collapse, stupor, purpura, jaundice and azotemia. Am J Med 18:659-670, 1955.
62. Minson CT, Wladkowski SL, Cardell AF, Pawelczyk JA, Kenney WL. Age alters the cardiovascular response to direct passive heating. J Appl Physiol 84:1323-1332, 1998.
63. Misset B, De JB, Bastuji-Garin S, Gattolliat O, Boughrara E, Annane D, Hausfater P, Garrouste-Org, Carlet J. Mortality of patients with heatstroke admitted to intensive care units during the 2003 heat wave in France: a national multiple-center risk-factor study. Crit Care Med 34:1087-1092, 2006.
64. Mustafa KY, Omer O, Khogali M, Jamjoom A, Gumaa KA, Abu el-Nasr N, Gader MA. Blood coagulation and fibrinolysis in heat stroke. Br J Haematol 61:517-523, 1985.
65. Naughton MP, Henderson A, Mirabelli MC, Kaiser R, Wilhelm JL, Kieszak SM, Rubin CH, McGeehin MA. Heat-related mortality during a 1999 heat wave in Chicago. Am J Prev Med 22:221-227, 2002.
66. Newcomb D, Bolgos G, Green L, Remick DG. Antibiotic treatment influences outcome in murine sepsis: mediators of increased morbidity. Shock 10:110-117, 1998.
67. Nolan JP. Endotoxin, reticuloendothelial function, and liver injury. Hepatology 1:458-465, 1981.
68. Nybo L. Exercise and heat stress: cerebral challenges and consequences. Prog Brain Res 162:29-43, 2007.
69. Opal SM, Fisher CJ Jr, Dhainaut JF, Vincent JL, Brase R, Lowry SF, Sadoff JC, Slotman GJ, Levy H, Balk RA, Shelly MP, Pribble JP, LaBrecque JF, Lookabaugh J, Donovan H, Dubin H, Baughman R, Norman J, DeMaria E, Matzel K, Abraham E, Seneff M. Confirmatory interleukin-1 receptor antagonist trial in severe sepsis: a phase III, randomized, double-blind, placebo-controlled, multicenter trial. The Interleukin-1 Receptor Antagonist Sepsis Investigator Group. Crit Care Med 25:1115-1124, 1997.
70. Paidas CN, Mooney ML, Theodorakis NG, De Maio A. Accelerated recovery after endotoxic challenge in heat shock-pretreated mice. Am J Physiol Regul Integr Comp Physiol 282: R1374-R1381, 2002.
71. Patel DR, Gyamfi R, Torres A. Exertional rhabdomyolysis and acute kidney injury. Phys Sportsmed 37:71-79, 2009.
72. Pease S, Bouadma L, Kermarrec N, Schortgen F, Regnier B, Wolff M. Early organ dysfunction course, cooling time and outcome in classic heatstroke. Intensive Care Med 35:1454-1458, 2009.
73. Remick DG. Cytokine therapeutics for the treatment of sepsis: why has nothing worked? Curr Pharm des 9:75-82, 2003.
74. Roberts WO. Death in the heat: can football heat stroke be prevented? Curr Sports Med Rep 3:1-3, 2004.
75. Saissy JM. Liver transplantation in a case of fulminant liver failure after exertion. Intensive Care Med 22:831, 1996.
76. Schar C, Jendritzky G. Climate change: hot news from summer 2003. Nature 432:559-560, 2004.
77. Schobitz B, Pezeshki G, Pohl T, Hemmann U, Heinrich PC, Holsboer F, Reul JM. Soluble interleukin-6 (IL-6) receptor augments central effects of IL-6 in vivo. FASEB J 9:659-664, 1995.
78. Smalley B, Janke RM, Cole D. Exertional heat illness in Air Force basic military trainees. Mil Med 168:298-303, 2003.
79. Sonna LA, Wenger CB, Flinn S, Sheldon HK, Sawka MN, Lilly CM. Exertional heat injury and gene expression changes: a DNA microarray analysis study. J Appl Physiol 96:1943-1953, 2004.
80. Stauss HM, Morgan DA, Anderson KE, Massett MP, Kregel KC. Modulation of baroreflex sensitivity and spectral power of blood pressure by heat stress and aging. Am J Physiol Heart Circ Physiol 272: H776-H784, 1997.
81. Szold O, Reider-Groswasser II, Abraham RB, Aviram G, Segev Y, Biderman P, Sorkine P. Gray-white matter discrimination-a possible marker for brain damage in heat stroke? Eur J Radiol 43:1-5, 2002.
82. Varghese GM, John G, Thomas K, Abraham OC, Mathai D. Predictors of multi-organ dysfunction in heatstroke. Emerg Med J 22:185-187, 2005.
83. Wagner M, Kaufmann P, Fickert P, Trauner M, Lackner C, Stauber RE. Successful conservative management of acute hepatic failure following exertional heatstroke. Eur J Gastroenterol Hepatol 15:1135-1139, 2003.
84. Wallace RF, Kriebel D, Punnett L, Wegman DH, Amoroso PJ. Prior heat illness hospitalization and risk of early death. Environ Res 104:290-295, 2007.
85. Wallimann T, Hemmer W. Creatine kinase in non-muscle tissues and cells. Mol Cell Biochem 133-134:193-220, 1994.
86. Wang AY, Li PK, Lui SF, Lai KN. Renal failure and heatstroke. Ren Fail 17:171-179, 1995.
87. Warren HS, Suffredini AF, Eichacker PQ, Munford RS. Risks and benefits of activated protein C treatment for severe sepsis. N Engl J Med 347:1027-1030, 2002.
88. White JG. Effects of heat on platelet structure and function. Blood 32:324-335, 1968.
89. Wilkinson DA, Burholt DR, Shrivastava PN. Hypothermia following whole-body heating of mice: effect of heating time and temperature. Int J Hyperthermia 4:171-182, 1988.
90. Winkenwerder M, Sawka MN. Disorders due to heat and cold. In: Cecil Medicine, edited by Goldman L and Ausiello D. Philadelphia: Elsevier Science, 2007, p. 763-767.