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International Journal of Hyperthermia Volume 19, 2003 - Issue 3: Adverse temperature levels in the human-proceedings of the WHO conference
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Research Article

Hyperthermia induced pathophysiology of the central nervous system

H. S. Sharma Laboratory of Neuroanatomy, Department of Medical Cell Biology, Biomedical Centre, Uppsala University, SE-75123 Uppsala, Sweden
&
P. J. Hoopes Departments of Surgery and Radiation Oncology, Dartmouth Medical School and the Thayer School of Engineering, Dartmouth College Hanover, NH 03756, USA
Pages 325-354 | Published online: 09 Jul 2009

  • Gauss H, Meyer KA. Heat stroke: report of one hundred and fifty-eight cases from Cook County Hospital, Chicago. Am J Med Sci 1917; 154: 554-64.
  • Weisenburg TH. Nervous symptoms following sunstroke. JAMA 1912; 58: 2015-7.
  • Malamud N, Haymaker W, Custer RP. Heat stroke. A clinicopathological study of 125 fatal cases. Milit Surg 1964; 99: 397-449.
  • Sterner S. Summer heat illness. Postgrad Med 1990; 87: 67-73.
  • Hahn GM. Hyperthermia and Cancer, New York: Plenum Press, 1982.
  • Hoopes PJ. The effects of heat on the nervous system. In: Gutin PH, Leibel SA, Sheline GE, eds, Radiation Injury to the Nervous System, New York: Raven Press; 1991; 407-30.
  • Ryan TP, Trembly BS, Roberts DW, Strohbehn JW, Coughlin CT, Hoopes PJ. Brain hyperthermia I: interstitial microwave antenna array techniques, the Dartmouth experi- ence. Int J Radiat Oncol Biol Phys 1994; 29: 1065-78.
  • Hartman FW, Major RC. Pathological changes resulting from accurately controlled arti- ficial fever. Am J Clin Path 1935; 5: 392-410.
  • Alpers BJ. Hyperthermia due to lesions in the hypothalamus. Arch Neural & Psychiat 1936; 35: 30-42.
  • Siesjö BK. Brain Energy Metabolism, New York, Chichester: Wiley, 1978.
  • Sharma HS, Westman J. Brain functions in hot environment. Prog Brain Res 1998; 115:1527.
  • Sharma HS. Pathophysiology of blood-brain barrier, brain edema and cell injury following hyperthermia: new role of heat shock protein, nitric oxide and carbon monoxide. An experimental study in the rat using light and electron microscopy. Acta Universitatis Upsaliensis 1999; 830: 1-94.
  • Sharma HS, Westman J. Pathophysiology of hyperthermic brain injury. Current concepts, molecular mechanisms and pharmacological strategies. In: Oehnmichen, ed., Research in Legal Medicine Vol. 21 Hyperthermia, Burning and Carbon Monoxide, Lübeck Medical University Publications, Lübeck, Germany: Schmidt-Romhild Verlag, 2000; 79-120.
  • Bouchama A, Knochel JP. Heat stroke. N Engl J Med 2002; 25: 1978-88.
  • Knochel JP, Reed G. Disorders of heat regulation. In: Narins RG, ed., Maxwell & Kleeman's clinical disorders of fluid and electrolyte metabolism, 5th edn, New York: McGraw-Hill, 1994; 1549-90.
  • Milton AS. Physiology of Thermoregulation, Basel: Birkhauser, 1994.
  • Blatteis C. Thermoregulation: recent progress and New Frontiers. Ann. NY Acad Sci 1997; 813: 1-865.
  • Ellis FP. Mortality from heat illness and heat-aggravated illness in the United States. Environ Res 1972; 5: 1-58.
  • Austin MG, Berry JW. Observation on one hundred cases of heatstroke. JAMA 1956; 161: 1525-9.
  • Sharma HS, Westman J, Nyberg F. Pathophysiology of brain edema and cell changes following hyperthermic brain injury. Brain functions in hot environment. Prog Brain Res 1998; 115: 351-412.
  • Cervos-Navarro J, Ferszt R. Brain edema: pathology, diagnosis and therapy. Adv Neural, New York: Raven Press, 1980; 1-450.
  • Go KG, Baethmann A. Recent Progress in the Study and Therapy of Brain Edema, New York: Plennum Press, 1984.
  • Wahl M, Unterberg A, Baethmann A, Schilling L. Mediators of blood-brain barrier dysfunction and formation of vasogenic brain edema. J Cereb Blood Flow Metab, 1988; 8: 621-34.
  • Sharabi Y, Danon YL, Berkenstadt H, Almog S, Mimouni-Bloch A, Zisman A, Dani S, Atsmon J. Survey of symptoms following intake of pyridostigmine during Persian Gulf War. Isr J Med Sci 1991; 27: 656-8.
  • Hanin I. The Gulf War, stress and a leaky blood-brain barrier (News & Views). Nature Med 1996; 2: 1307-8.
  • Friedman A, Kaufer D, Shemer J, Hendler I, Soreq H, Tur-Kapsa I. Pyridostigmine brain penetration under stress enhances neuronal excitability and induces early immediate transcriptional response. Nature Med 1996, 2; 1382-5.
  • Sharma HS, Dey PK. Impairment of blood-brain barrier by immobilization stress: role of serotonin. Indian J Physiol Pharmacol 1981; 25: 111-22.
  • Sharma H S. Blood-brain barrier in stress. PhD Thesis, Varanasi (India): Banaras Hindu University, 1982.
  • Sharma HS, Dey PK. Role of 5-HT on increased permeability of blood-brain barrier under heat stress. Indian J Physiol Pharmacol 1984; 28: 259-67.
  • Sharma HS, Dey PK. Probable involvement of 5-hydroxytryptamine in increased permeability of blood-brain barrier under heat stress. Neuropharmacology 1986; 25: 161-7.
  • Sharma HS, Dey PK. Influence of long-term immobilization stress on regional bloodbrain barrier permeability, cerebral blood flow and 5-HT level in conscious normotensive young rats. J Neurolog Sci 1986; 72: 61-76.
  • Sharma HS, Dey PK. Influence of long-term acute heat exposure on regional blood-brain barrier permeability, cerebral blood flow and 5-HT level in conscious normotensive young rats. Brain Res 1987; 424: 153-62.
  • Sharma HS, Cervos-Navarro J. Brain oedema and cellular changes induced by acute heat stress in young rats. Acta Neurochir (Wien) 1990; Suppl. 51: 383-6.
  • Sharma HS, Cervós-Navarro J, Dey PK. Increased blood-brain barrier permeability following acute short-term forced-swimming exercise in conscious normotensive young rats. Neurosci Res 1991; 10: 211-21.
  • Hart GR, Anderson RJ, Crumpler CP, Shulkin A, Reed G, Knochel JP. Epidemic classical heat stroke: clinical characteristics and course of 28 patients. Medicine 1982; 61: 189-97.
  • Knochel JP. Environmental heat illness. An eclectic review. Arch Intern Med 1974; 133: 841-64.
  • Zimmerman HM. Temperature disturbances and the hypothalamus. A Research. Nerv Ment Dis Proc 1940; 20: 824-40.
  • Kapp DS and Lord PF. Thermal tolerance to whole body hyperthermia. Int J Radiat Oncol Biol Phys 1983; 9: 917-21.
  • Bull JMC. An update on the anticancer effects of a combination of chemotherapy and hyperthermia. Cancer Res 1984; 44: 4853-4875.
  • Ryan TP, Hoopes PJ, Taylor JH, Strohbehn JW, Roberts DW, Double EB, Coughlin CT. Experimental brain hyperthermia: techniques for heat delivery and thermometry. Int J Radiat Oncol Biol Phys 1991; 20: 739-50.
  • Ryan TP, Wykoff R, Hoopes PJ. An automated temperature mapping system for use in ultrasound or microwave hyperthermia. J Biomed Eng 1991; 13: 348-54.
  • Sminia P, van der Zee J, Wondergem J, Haveman J. Effect of hyperthermia on the central nervous system: a review. Int J Hyperthermia 1994; 10: 1-30.
  • van der Zee J. Whole body hyperthermia. The development of and experience with a clinical method. Dissertation, Rotterdam (Netherlands): Erasmus University, 1987.
  • Kerner T, Deja M, Ahlers O, Hildebrandt B, Dicing A, Riess H, Wust P, Gerlach H. Acta Anaesthesiol Scand 2002; 46: 561-6.
  • Tanaka R, Kim CH, Yamada N, Saito Y. Radiofrequency hyperthermia for malignant brain tumours: preliminary results of clinical trials. Neurosurgery 1987; 21: 478-83.
  • Petrovich Z, Langholz B, Gibbs FA, Sapozink MD, Krapp DS, Stewart RJ, Emami B, Oleson J, Senzer N, Slater J, Astrahan M. Int J Radiat Oncol (Biol Phys) 1989 Mar; 16 (3): 601-7.
  • Salzman SK. Neural Monitoring. The Prevention of Intraoperative Injury, New Jersey: Humanna Press, 1990.
  • Mellergard P, Nordström CH. Epidural temperature and possible intracerebral temperature gradients in man. Br J Neurosurg 1990; 4: 31-8.
  • Cabanac M. Selective brain cooling and thermoregulatory set-point. J Basic Clin Physiol Pharmacol 1998; 9: 3-13.
  • Gabay C, Kushner I. Acute phase proteins and other systemic response to inflammation. NEnglJMed 1999; 340: 448-54 [Erratum, 340: 1376].
  • Chang DM. The role of cytokines in heatstroke. Immunol Invest 1993; 22: 553-61.
  • Katschinski DM, Wiedemann GJ, Longo W, d'Oleire FR, Spriggs D, Robbins HI. Whole body hyperthermia cytokine induction: a review, and unifying hypothesis for myeloprotection in the setting of cytotoxic therapy. Cytokine Growth Factor Rev 1999; 10: 93-97.
  • Pedersen BK, Hoffman-Goetz L. Exercise and the immune system: regulation, integration, and adaptation. Physiol Rev 2000; 80: 1055-81.
  • Kraybill WG, Olenki T, Evans SS, Ostberg JR, O'Leary KA, Gibbs JF, Repasky EA. A phase I study of fever-range whole body hyperthermia (FR-WBH) in patients with advances solid tumours:correlation with mouse models. Int J Hyperthermia 2002; 18: 253-66.
  • Gottschalk PG, Thomas JE. Heat stroke. Mayo Clin Proc 1966; 41: 470-82.
  • Frankel HM, Ellis JP Jr, Cain SM. Development of tissue hypoxia during progressive hyperthermia in dogs. Am J Physiol 1963; 205: 733-7.
  • Shibolet S, Coll R, Gilat T, Sohar E. Heatstroke: its clinical picture and mechanisms in 36 cases. Quart J Med 1967; 36: 525-48.
  • Shapiro Y, Rosenthal T, Sohar E. Experimental heatstroke. A model in dogs. Arch Int Med 1973; 131:688-92.
  • Chapot G, Muller M, Barrault N, Dargnat N, Languillat J-M. A correlation between PaCO2 and body temperature in febrile patients. Thorax 1974; 29: 104-5.
  • Nemoto EM, Frankel HM. Cerebral oxygenation and metabolism during progressive hyperthermia. Am J Physiol 1970; 1219: 1784-8.
  • Field J (II), Fuhrman FA, Martin AW. Effect of temperature on the oxygen consumption of brain tissue. J Neurophysiol 1944; 7: 117-26.
  • Burger FJ, Fuhrman FA. Evidence of injury by heat in mammalian tissues. Am J Physiol 1964; 206: 1057-61.
  • Heyman A, Patterson JL Jr, Nichols FT Jr. The effects of induced fever on cerebral functions in neurosyphlis. J Clin Invest 1950; 29: 1335-41.
  • Demers HG, Spaich P, Usinger W. Der Hirnkreislauf bei erhöhter Körper-temperature. Verh Dtsch ges Kreislaufforschg 1969; 35: 131-40.
  • Reinmuth OM, Scheinberg P, Bourne B. Total cerebral blood flow and metabolism. Arch Neural (Chic) 1965; 12: 49-66.
  • Hales JRS, Findlay JD, Mabon RM. Tissue hypoxia in oxen exposed to severe heat. Respir Physiol 1967; 3: 43-6.
  • Carlsson C, Hägerdal M, Siesjö BK. The effect of hyperthermia upon oxygen consump- tion and blood flow in the cerebral cortex of the rat. Acta Anaesth Scand 1976; 26: 1001-6.
  • Thrall DE, Prescott DM, Samulski TV, Dewhirst MW, Cline JM, Lee J, Page RL, Oleson JR. Serious toxidty associated with annular microwave array induction of whole-body hyperthermia in normal dogs. Int J Hyperthermia 1992; 8: 23-32.
  • Britt RH, Lyons BE, Ryan T, Saxer E, Obana W, Rossi G. Effect of whole body hyperthermia on auditory brainstem and somatosensory and visualevoked potentials. In: Hales RRS, ed., Thermal Physiology, New York: Raven Press, 1984; 519-23.
  • Marsh RR, Yamane H, Potsic WP. Auditory brain-stem response and temperature. Relationship in the guinea pig. Electroencephalog Clin Neurophysiol 1984; 57: 289-93.
  • Sharma HS, Dey PK, Kumar A. Role of circulating 5-HT and lung MAO activity in physiological processes of heat adaptation in conscious young rats. Biomedicine 1986; 6: 31-40.
  • Sharma HS, Cervós-Navarro J. Nimodipine improves cerebral blood flow and reduces brain edema, cellular damage and blood-brain barrier permeability following heat stress in young rats. In: Krieglstein J, Oberpichler H, eds, Pharmacology of Cerebral Ischemia, Boca Raton, FL: CRC Press), 1990; 303-10.
  • Sharma HS, Cervós-Navarro J, Dey PK. Acute heat exposure causes cellular alteration in cerebral cortex of young rats. NeuroReport 1991; 2: 155-8.
  • Sharma HS, Cervós-Navarro J, Dey PK. Rearing at high ambient temperature during later phase of the brain development enhances functional plasticity of the CNS and induces tolerance to heat stress. An experimental study in the conscious normotensive young rats. Brain Dysfunction 1991; 4: 104-24.
  • Sharma HS, Zimmer C, Westman J, Cervós-Navarro J. Acute systemic heat stress increases glial fibrillary acidic protein immunoreactivity in brain. An experimental study in the conscious normotensive young rats. Neuroscience 1992; 48: 889-901.
  • Sharma HS, Kretzschmar R, Cervos-Navarro J, Ermisch A, Ruble H-J, Dey PK. Age- related pathophysiology of the blood-brain barrier in heat stress. Prog Brain Res 1992; 91 : 189-96.
  • Sharma HS, Westman J, Nyberg F, Cervós-Navarro J, Dey PK. Role of serotonin in heat adaptation: an experimental study in the conscious young rat. Endocrine Reg 1992; 26: 133-42.
  • Sharma HS, Nyberg F, Cervós-Navarro J, Dey PK. Role of catecholamines in the patho- physiology of heat stress. Proc 7th Int Catecholamine Symp, 22-26 June; Amsterdam, Netherlands, 1992; 287.
  • Sharma HS, Westman J, Nyberg F, Cervós-Navarro J, Dey PK. Role of serotonin and prostaglandins in brain edema induced by heat stress. An experimental study in the rat. Acta Neurochirurgica (Suppl) 1994; 60: 65-70.
  • Sharma HS, Westman J, Nyberg F, Zimmer C, Cervós-Navarro J, Dey PK. Selective vulnerability of rat hippocampus in heat stress. In: Milton AS, ed., Temperature Regulation. Advances in Pharmacological Science, Basel: Birkhauser, 1994; 267-72.
  • Sharma HS, Westman J, Cervós-Navarro J, Dey PK, Nyberg F. Probable involvement of serotonin in the increased permeability of the blood-brain barrier by forced swimming. An experimental study using Evans blue and 131I-sodium tracers in the rat. Behav Brain Res 1995; 72: 189-96.
  • Sharma HS, Westman J, Cervós-Navarro J, Nyberg F. Role of neurochemicals in brain edema and cell changes following hyperthermic brain injury in the rat. Acta Neurochir 1997; (Suppl. 70): 269-74.
  • Sharma HS, Westman J, Alm P, Sjöquist P-Ö, Cervós-Navarro J, Nyberg F. Involvement of nitric oxide in the pathophysiology of acute heat stress in the rat influence of a new antioxidant compoundh 290/51. Ann NY AcadSci 1997b; 813: 581-90.
  • Sharma HS, Westman J, Cervós-Navarro J, Dey PK, Nyberg F. Opioid receptor antago- nists attenuate heat stress induced reduction in cerebral blood flow, increased blood-brain barrier permeability, vasogenic edema and cell changes in the rat. Ann NY Acad Sci 1997; 813: 559-71.
  • Dey S, Dey PK, Sharma HS. Regional metabolism of 5-hydroxytryptamine in brain under acute and chronic heat stress. Indian J Physiol Pharmacol 1993; 37: 8-12.
  • Hall WW, Wakefield FG. A study of experimental heatstroke. JAMA 1927; 89: 17782.
  • Morgan LO. Cell changes in some of the hypothalamic nuclei in experimental fever. J Neurophysiol 1938; 1: 281-5.
  • Weiner JC. Experimental study of heat collapse. J Ind Hyg Toxicol 1938; 20: 389-400.
  • Wilson SJ, Doan CA. The pathogenesis of hemorrhage in artificially induced fever. Ann Int Med 1939; 13: 1214-29.
  • Adolph EF. Tolerance to heat and dehydration in several species of mammals. Am J Physiol 1947; 151: 564-75.
  • Haubbard RW, Bowers WD, Mather WT, Curtis FC, Criss REL, Sheldon GM, Ratteree JWJ. Rat model of acute heat stroke mortality. J Appl Physiol 1977; 42: 807-16.
  • Buolochnik ED, Zyablov MP. Effect of hyperthermia induced by a high ambient tem- perature on the direct cortical response. Byulleten 'Eksperimental'noi Biologii i Meditsiny 1978; 84: 657-60.
  • Lee DHK. Terrestrial animals in dry heat. In: Dill DB, Adolph EF, Wilber CG, eds, Handbook Physiol, Section IV, Adaptation to the Environment, Washington: American Physiological Society, 1964; 55-72.
  • Rapoport SI. Blood-Brain Barrier in Physiology and Medicine, New York: Raven Press, 1976.
  • Sharma HS, Aim P, Westman J. Nitric oxide and carbon monoxide in the pathophysiol- ogy of brain functions in heat stress. Prog Brain Res 1998; 115: 297-333.
  • Sharma HS. Bradykinin2 receptor antagonist HOE-140 attenuates blood-spinal cord barrier permeability following trauma to the rat spinal cord. Acta Neurochir (Wien) 2000; Suppl. 76: 159-63.
  • Elliott KAC, Jasper H. Measurement of experimentally induced brain swelling and shrinkage. Am J Physiol 1949; 157: 122-8.
  • Olesen SP. An electrophysiological study of microvascular permeability and its modulation by chemical mediators. Acta Physiol Scand 1989; 136 (Suppl. 579): 1-28.
  • Bradbury MWB. The Concept of a Blood-Brain Barrier, London: Chicester, 1979.
  • Black KL. Biochemical opening of the blood-brain barrier. Adv Drug Del Rev 1995; 15: 37-52.
  • Toh CC. Effect of temperature on the 5-hydroxytryptamine content of tissues. J Physiol (Land) 1960; 151: 410-5.
  • Sharma HS, Olsson Y, Dey PK. Changes in blood-brain barrier and cerebral blood flow following elevation of circulating serotonin level in anaesthetized rats. Brain Res 1990; 517: 215-23.
  • Sharma HS, Nyberg F, Gordh T, Aim P, Westman J. Neurotrophic factors attenuate neuronal nitric oxide synthase upregulation, microvascular permeability disturbances, edema formation and cell injury in the spinal cord following trauma. In: Stalberg E, Sharma HS, Olsson Y, eds, Spinal Cord Monitoring, Wien, New York: Springer-Verlag, 1998; 118-48.
  • Westman J, Sharma HS. Heat shock protein response in the CNS following heat stress. Prog Brain Res 1998; 115: 207-39.
  • Johansson BB, Owman Ch, Widner H. Pathophysiology of the blood-brain barrier. Fernström Foundation Series 14, Amsterdam: Elsevier, 1990: 1-340.
  • Lum H, Malik AB. Regulation of vascular endothelial barrier function. Am J Physiol 1944; 267: 223-9.
  • Davson H. Physiology of the Cerebrospinal Fluid, London: Churchill, 1967.
  • Brightman MW, Reese TS. Junctions between intimately apposed cell membranes in the vertebrate brain. J Cell Biol 1969; 40: 648-77.
  • Driscoll BF, Kramer AJ, Kies MW. Myelin basic protein:Location of multiple indepen- dent antigenic regions. Science 1974; 184: 73-5.
  • Cervos-Navarro J, Sharma HS, Westman J, Bongcam-Rudloff E. Glial reactions in the central nervous system following heat stress. Prog Brain Res 1998; 115: 241-74.
  • Bredt DS, Snyder SH. Nitric oxide, a novel neuronal messenger. Neuron 1992; 8: 3-11.
  • Chiueh CC, Gilbert DL, Colton CA. The neurobiology of NO" and OH. Ann NY Acad Sei 1994; 738: 1-471.
  • Sharma HS, Drieu K, Alm P, Westman J. Upregulation of neuronal nitric oxide synthase, edema and cell injury following heat stress are reduced by pretreatment with EGB-761 in the rat. / Therm Biol 1999; 24: 439-6.
  • Sharma HS, Drieu K, Alm P, Westman J. Role of nitric oxide in blood-brain barrier permeability, brain edema and cell damage following hyperthermic brain injury, an experimental study using EGB-761 and Gingkolide B pretreatment in the rat. Acta Neurochir (Wien) 2000; Suppl. 76: 81-6.
  • Alm P, Sharma HS, Hedlund S, Sjöquist P-O, Westman J. Nitric oxide in the patho- physiology of hyperthermic brain injury. Influence of a new anti-oxidant compound H290/51. Amino Acids 1998; 14: 95-104.
  • Lindquist S. The heat-shock response. Ann Rev Biochem 1986; 55: 1151-91.
  • Welch WJ. Mammalian stress response: cell physiology, structure/function of stress proteins, and implications for medicine and diseases. Physiol Rev 1992; 72: 1063-81.
  • Westman J, Drieu K, Sharma HS. Antioxidant compounds EGB-761 and BN-520 21 attenuate heat shock protein (HSP 72 kD) response, edema and eel] changes following hyperthermic brain injury. An experimental study using immunohistochemistry in the rat. Amino Acids 2000; 19: 339-50.
  • Hedlund S, Sharma HS, Sjöquist P-O, Westman J. A new antioxidant compound h-290/ 51 attenuates heat shock protein (HSP 72 kD) response, breakdown of the blood-brain barrier permeability, edema and cell injury following acute heat exposure. An experimental study using light and electron microscopy in the rat. J Therm Biol 1999; 24: 40914.
  • Walters TJ, Ryan KL, Mason PA. Regional distribution of Hsp 70 in the CNS of young and old food-restricted rats following hyperthermia. Brain Res Bull 2001; 55: 367-74.
  • Oglesbee MJ, Alldinger S, Vasconcelos D, Diehl KA, Shinko PD, Baumgärtner W, Tallman R, Podell M. Intrinsic thermal resistance of the canine brain. Neuroscience 2002; 113:55-64.
  • King YT, Lin CS, Lin JH, Lee WC. Whole body hyperthermia induced thermotolerance is associated with the induction of heat shock protein 70 in mice. J Exp Biol 2002; 205: 273-8.
  • Hughes P, Dragunow M. Induction of immediate-early genes and the control of neuro- transmitter-regulated gene expression within the nervous system. Pharmacol Rev 1995; 47: 133-78.
  • Le Grevés P, Sharma HS, Westman J, Aim P, Nyberg F. Acute heat stress induced edema and nitric oxide synthase Upregulation and downregulates mRNA levels of the NMDARl, MNDAR2 and NMDAR2B subunits in the rat hippocampus. Acta Neurochir 1997; Suppl. 70: 275-8.
  • Selye H. Stress in Health and Disease, London: Butterworths, 1976.

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