Thermoregulation in multiple sclerosis

Journal of Applied Physiology

Volumn 109, Issue 5, 2010, Pages 1531-1537

  Davis, Scott L ^a,b   Wilson, Thad E ^c,d   White, Andrea T ^e,f   Frohman, Elliot M ^b,g  

^a SOUTHERN METHODIST UNIVERSITY   (United States)

^b Departments of Neurology   (United States)

^c Biomedical Sciences   (United States)

^d OHIO UNIVERSITY   (United States)

^e Department of Exercise and Sport Science ^*  (United States)

^f UNIVERSITY OF UTAH   (United States)

^g Departments of Neurology and Ophthalmology   (United States)

Author keywords

Core temperature; Demyelination; Fatigue; Skin blood flow; Sweating

Indexed keywords

AUTONOMIC NERVOUS SYSTEM; BLOOD FLOW; CENTRAL NERVOUS SYSTEM; HEAT EXHAUSTION; HEMODYNAMICS; HUMAN; MULTIPLE SCLEROSIS; PATHOPHYSIOLOGY; REVIEW; SKIN; SWEATING; TEMPERATURE SENSE; THERMOREGULATION; VASCULARIZATION;

AUTONOMIC NERVOUS SYSTEM; BODY TEMPERATURE REGULATION; CENTRAL NERVOUS SYSTEM; HEAT EXHAUSTION; HEMODYNAMICS; HUMANS; MULTIPLE SCLEROSIS; REGIONAL BLOOD FLOW; SKIN; SWEATING; THERMOSENSING;

EID: 78149307923     PISSN: 87507587     EISSN: 15221601     Source Type: Journal    
DOI: 10.1152/japplphysiol.00460.2010     Document Type: Review

References (91)

1. Andersen EB, Nordenbo AM. Sympathetic vasoconstrictor responses in multiple sclerosis with thermo-regulatory dysfunction. Clin Auton Res 7: 13-16, 1997.
2. Avis SP, Pryse-Phillips WE. Sudden death in multiple sclerosis associated with sun exposure: a report of two cases. Can J Neurol Sci 22: 305-307, 1995.
3. Bassett SW, Lake BM. Use of cold applications in the management of spasticity: report of three cases. Phys Ther Rev 38: 333-334, 1958.
4. Beenakker EA, Oparina TI, Hartgring A, Teelken A, Arutjunyan AV, De Keyser J. Cooling garment treatment in MS: clinical improvement and decrease in leukocyte NO production. Neurology 57: 892-894, 2001.
5. Bigland-Ritchie B, Woods JJ. Changes in muscle contractile properties and neural control during human muscular fatigue. Muscle Nerve 7: 691-699, 1984.
6. Boulant JA. Hypothalamic neurons regulating body temperature. In: Handbook of Physiology. Environmental Physiology. Bethesda, MD: Am. Physiol Soc., sect. 4, vol. I, chapt. 6, 1996, p. 105-126.
7. Boynton BL, Garramone PM, Buca JT. Observations on the effects of cool baths for patients with multiple sclerosis. Phys Ther Rev 39: 297-299, 1959.
8. Cadarette BS, Cheuvront SN, Kolka MA, Stephenson LA, Montain SJ, Sawka MN. Intermittent microclimate cooling during exercise-heat stress in US army chemical protective clothing. Ergonomics 49: 209-219, 2006.
9. Capello E, Gardella M, Leandri M, Abbruzzese G, Minatel C, Tartaglione A, Battaglia M, Mancardi GL. Lowering body temperature with a cooling suit as symptomatic treatment for thermosensitive multiple sclerosis patients. Ital J Neurol Sci 16: 533-539, 1995.
10. Cartlidge NE. Autonomic function in multiple sclerosis. Brain 95: 661-664, 1972.
11. Confavreux C, Vukusic S. Natural history of multiple sclerosis: implications for counselling and therapy. Curr Opin Neurol 15: 257-266, 2002.
12. Crandall CG, Shibasaki M, Wilson TE, Cui J, Levine BD. Prolonged head-down tilt exposure reduces maximal cutaneous vasodilator and sweating capacity in humans. J Appl Physiol 94: 2330-2336, 2003.
13. Davis FA. Axonal conduction studies based on some considerations of temperature effects in multiple sclerosis. Electroencephalogr Clin Neurophysiol 28: 281-286, 1970.
14. Davis FA. Pathophysiology of multiple sclerosis and related clinical implications. Mod Treat 7: 890-902, 1970.
15. Davis SL, Frohman TC, Crandall CG, Brown MJ, Mills DA, Kramer PD, Stuve O, Frohman EM. Modeling Uhthoff's phenomenon in MS patients with internuclear ophthalmoparesis. Neurology 70: 1098-1106, 2008.
16. Davis SL, Korkmas MA, Crandall CG, Frohman EM. Impaired sweating in multiple sclerosis leads to increased reliance on skin blood flow for heat dissipation (Abstract). FASEB J 24: 991.925, 2010.
17. Davis SL, Wilson TE, Vener JM, Crandall CG, Petajan JH, White AT. Pilocarpine-induced sweat gland function in individuals with multiple sclerosis. J Appl Physiol 98: 1740-1744, 2005.
18. Edwards S, Lennox G, Robson K, Whiteley A. Hypothermia due to hypothalamic involvement in multiple sclerosis. J Neurol Neurosurg Psychiatry 61: 419-420, 1996.
19. Fealey RD, Sato K. Disorders of the eccrine sweat glands and sweating. In: Fitzpatrick's Dermatology in General Medicine, edited by Wolff K, Goldsmith LA, Katz SI, Gilchrest BA, Paller AS, Leffell DJ. Columbus, OH: McGraw-Hill, 2008, p. 215-243.
20. Flensner G, Lindencrona C. The cooling-suit: a study of ten multiple sclerosis patients' experiences in daily life. J Adv Nurs 29: 1444-1453, 1999.
21. Flouris AD, Cheung SS. Design and control optimization of microclimate liquid cooling systems underneath protective clothing. Ann Biomed Eng 34: 359-372, 2006.
22. Freal JE, Kraft GH, Coryell JK. Symptomatic fatigue in multiple sclerosis. Arch Phys Med Rehabil 65: 135-138, 1984.
23. Frohman EM, Racke MK, Raine CS. Multiple sclerosis-the plaque and its pathogenesis. N Engl J Med 354: 942-955, 2006.
24. Gandevia SC, Allen GM, Butler JE, Taylor JL. Supraspinal factors in human muscle fatigue: evidence for suboptimal output from the motor cortex. J Physiol (Lond) 490: 529-536, 1996.
25. Goodman AD, Brown TR, Krupp LB, Schapiro RT, Schwid SR, Cohen R, Marinucci LN, Blight AR. Sustained-release oral fampridine in multiple sclerosis: a randomised, double-blind, controlled trial. Lancet 373: 732-738, 2009.
26. Grahn DA, Murray JV, Heller HC. Cooling via one hand improves physical performance in heat-sensitive individuals with multiple sclerosis: a preliminary study. BMC Neurology 8: 14, 2008.
27. Guthrie TC. Visual and motor changes in patients with multiple sclerosis; a result of induced changes in environmental temperature. AMA Arch Neurol Psychiatry 65: 437-451, 1951.
28. Guthrie TC, Nelson DA. Influence of temperature changes on multiple sclerosis: critical review of mechanisms and research potential. J Neurol Sci 129: 1-8, 1995.
29. Haensch CA, Jorg J. Autonomic dysfunction in multiple sclerosis. J Neurol 253, Suppl 1: I3-I9, 2006.
30. Huitinga I, De Groot CJ, Van der Valk P, Kamphorst W, Tilders FJ, waab DF. Hypothalamic lesions in multiple sclerosis. J Neuropathol Exp Neurol 60: 1208-1218, 2001.
31. Humm AM, Beer S, Kool J, Magistris MR, Kesselring J, Rosler KM. Quantification of Uhthoff's phenomenon in multiple sclerosis: a magnetic stimulation study. Clin Neurophysiol 115: 2493-2501, 2004.
32. Huxley AF. Ion movements during nerve activity. Ann NY Acad Sci 81: 221-246, 1959.
33. Ichinose TK, Inoue Y, Hirata M, Shamsuddin AK, Kondo N. Enhanced heat loss responses induced by short-term endurance training in exercising women. Exp Physiol 94: 90-102, 2009.
34. Judge SI, Bever CTJ. Potassium channel blockers in multiple sclerosis: neuronal Kv channels and effects of symptomatic treatment. Pharmacol Ther 111: 224-259, 2006.
35. Kay D, Marino FE, Cannon J, St. Clair Gibson A, Lambert MI, Noakes TD. Evidence for neuromuscular fatigue during high-intensity cycling in warm, humid conditions. Eur J Appl Physiol 84: 115-121, 2001.
36. Kenney WL, Johnson JM. Control of skin blood flow during exercise. Med Sci Sports Exerc 24: 303-312, 1992.
37. Kinnman J, Andersson T, Andersson G. Effect of cooling suit treatment in patients with multiple sclerosis evaluated by evoked potentials. Scand J Rehabil Med 32: 16-19, 2000.
38. Kinnman J, Andersson U, Wetterquist L, Kinnman Y, Andersson U. Cooling suit for multiple sclerosis: functional improvement in daily living? Scand J Rehabil Med 32: 20-24, 2000.
39. Krupp LB, Alvarez LA, LaRocca NG, Scheinberg LC. Fatigue in multiple sclerosis. Arch Neurol 45: 435-437, 1988.
40. Ku YT, Montgomery LD, Lee HC, Luna B, Webbon BW. Physiologic and functional responses of MS patients to body cooling. Am J Phys Med Rehabil 79: 427-434, 2000.
41. Kuno Y. Human Perspiration. Springfield, IL: Charles Thomas, 1956.
42. Lammens M, Lissoir F, Carton H. Hypothermia in three patients with multiple sclerosis. Clin Neurol Neurosurg 91: 117-121, 1989.
43. Latash M, Kalugina E, Nicholas J, Orpett C, Stefoski D, Davis F. Myogenic and central neurogenic factors in fatigue in multiple sclerosis. Mult Scler 1: 236-241, 1996.
44. Linker RA, Mohr A, Cepek L, Gold R, Prange H. Core hypothermia in multiple sclerosis: case report with magnetic resonance imaging localization of a thalamic lesion. Mult Scler 12: 112-115, 2006.
45. MacKenzie MA. Pathophysiology and clinical implications of human poikilothermia. Ann NY Acad Sci 813: 738-740, 1997.
46. Malhotra AS, Goren H. The hot bath test in the diagnosis of multiple sclerosis. JAMA 246: 1113-1114, 1981.
47. Marino FE. Heat reactions in multiple sclerosis: an overlooked paradigm in the study of comparative fatigue. Int J Hyperthermia 25: 34-40, 2009.
48. Martin PG, Marino FE, Rattey J, Kay D, Cannon J. Reduced voluntary activation of human skeletal muscle during shortening and lengthening contractions in whole body hyperthermia. Exp Physiol 90: 225-236, 2005.
49. Meyer-Heim A, Rothmaier M, Weder M, Kool J, Schenk P, Kesselring J. Advanced lightweight cooling-garment technology: functional improvements in thermosensitive patients with multiple sclerosis. Mult Scler 13: 232-237, 2007.
50. Nelson DA, Jeffreys WH, McDowell DF. Effects of induced hyperthermia on some neurological diseases. AMA Arch Neurol Psychiatry 79: 31-39, 1958.
51. Nelson DA, McDowell DF. The effects of induced hyperthermia on patients with multiple sclerosis. J Neurol Neurosurg Psychiatry 22: 113-116, 1959.
52. Ng AV, Miller RG, Gelinas D, Kent-Braun JA. Functional relationships of central and peripheral muscle alterations in multiple sclerosis. Muscle Nerve 29: 843-852, 2004.
53. Noronha MJ, Vas CJ, Aziz H. Autonomic dysfunction (sweating responses) in multiple sclerosis. J Neurol Neurosurg Psychiatry 31: 19-22, 1968.
54. Nunneley SA, Maldonado RJ. Head and/or torso cooling during simulated cockpit heat stress. Aviat Space Environ Med 54: 496-499, 1983.
55. Nybo L, Nielsen B. Hyperthermia and central fatigue during prolonged exercise in humans. J Appl Physiol 91: 1055-1060, 2001. (Pubitemid 32803896)
56. Ollivier CP. De la moelle epiniere et de ses maladies. Paris: Crevot, 1824.
57. Petajan JH, Gappmaier E, White AT, Spencer MK, Mino L, Hicks RW. Impact of aerobic training on fitness and quality of life in multiple sclerosis. Ann Neurol 39: 432-441, 1996.
58. Petajan JH, White AT. Motor-evoked potentials in response to fatiguing grip exercise in multiple sclerosis patients. Clin Neurophysiol 111: 2188-2195, 2000.
59. Petajan JH, White AT. Recommendations for physical activity in patients with multiple sclerosis. Sports Med 27: 179-191, 1999.
60. Rasminsky M. The effects of temperature on conduction in demyelinated single nerve fibers. Arch Neurol 28: 287-292, 1973.
61. Rice CL, Vollmer TL, Bigland-Ritchie B. Neuromuscular responses of patients with multiple sclerosis. Muscle Nerve 15: 1123-1132, 1992.
62. Romani A, Bergamaschi R, Versino M, Zilioli A, Callieco R, Cosi V. Circadian and hypothermia-induced effects on visual and auditory evoked potentials in multiple sclerosis. Clin Neurophysiol 111: 1602-1606, 2000.
63. Romanovsky AA. Thermoregulation: some concepts have changed. Functional architecture of the thermoregulatory system. Am J Physiol Regul Integr Comp Physiol 292: R37-R46, 2007.
64. Saari A, Tolonen U, Paakko E, Suominen K, Jauhiainen J, Sotaniemi KA, Myllyla VV. Sudomotor dysfunction in patients with optic neuritis. Clin Auton Res 20:199-204, 2010.
65. Saari A, Tolonen U, Paakko E, Suominen K, Jauhiainen J, Sotaniemi KA, Myllyla VV. Sweating impairment in patients with multiple sclerosis. Acta Neurol Scand 120: 358-363, 2009.
66. Schauf CL, Davis FA. Impulse conduction in multiple sclerosis: a theoretical basis for modification by temperature and pharmacological agents. J Neurol Neurosurg Psychiatry 37: 152-161, 1974.
67. Scherokman BJ, Selhorst JB, Waybright EA, Jabbari B, Bryan GE, Maitland CG. Improved optic nerve conduction with ingestion of ice water. Ann Neurol 17: 418-419, 1985.
68. Schwid SR, Petrie MD, Murray R, Leitch J, Bowen J, Alquist A, Pelligrino R, Roberts A, Harper-Bennie J, Milan MD, Guisado R, Luna B, Montgomery L, Lamparter R, Ku YT, Lee H, Goldwater D, Cutter G, Webbon B. A randomized controlled study of the acute and chronic effects of cooling therapy for MS. Neurology 60: 1955-1960, 2003.
69. Sharma KR, Kent-Braun JA, Mynhier MA, Weiner MW, Miller RG. Evidence of an abnormal intramuscular component of fatigue in multiple sclerosis. Muscle Nerve 18: 1403-1411, 1995.
70. Sheean GL, Murray NM, Rothwell JC, Miller DH, Thompson AJ. An electrophysiological study of the mechanism of fatigue in multiple sclerosis. Brain 120: 299-315, 1997.
71. Shibasaki M, Wilson TE, Cui J, Levine BD, Crandall CG. Exercise throughout 6 degrees head-down tilt bed rest preserves thermoregulatory responses. J Appl Physiol 95: 1817-1823, 2003.
72. Smith KJ, McDonald WI. The pathophysiology of multiple sclerosis: the mechanisms underlying the production of symptoms and the natural history of the disease. Philos Trans R Soc Lond B Biol Sci 354: 1649-1673, 1999.
73. National Multiple Sclerosis Society. Symptoms of MS. http://www. nationalmssociety.org/about-multiple-sclerosis/what-we-know-about-ms/ symptoms/indexaspx. [3 June, 2010].
74. Sullivan F, Hutchinson M, Bahandeka S, Moore RE. Chronic hypothermia in multiple sclerosis. J Neurol Neurosurg Psychiatry 50: 813-815, 1987.
75. Syndulko K, Jafari M, Woldanski A, Baumhefner RW, Tourtellotte WW. Effects of temperature in multiple sclerosis: a review of literature. J Neurol Rehabil 10: 23-34, 1996.
76. Tasaki I. Properties of myelinated fibres in frog sciatic nerve and in spinal cord as examined by microelectrodes. Jpn J Physiol 3: 73, 1953.
77. Uhthoff W. Untersuchungen uber die bei der multiplen Herdsklerose vorkommenden Augenstorungen. Arch Psychiatr Nervenkr 20: 55, 1889.
78. van Diemen HA, van Dongen MM, Dammers JW, Polman CH. Increased visual impairment after exercise (Uhthoff's phenomenon) in multiple sclerosis: therapeutic possibilities. Eur Neurol 32: 231-234, 1992.
79. Vas CJ. Sexual impotence and some autonomic disturbances in men with multiple sclerosis. Acta Neurol Scand 45: 166-182, 1969.
80. Watson CW. Effect of lowering of body temperature on the symptoms and signs of multiple sclerosis. N Engl J Med 261: 1253-1259, 1959.
81. Waxman SG, Geschwind N. Major morbidity related to hyperthermia in multiple sclerosis. Ann Neurol 13: 348, 1983.
82. Webb P, Troutman SJ Jr, Annis JF. Automatic cooling in water cooled space suits. Aerospace Med 41: 269-277, 1970.
83. Weiss N, Hasboun D, Demeret S, Fontaine B, Bolgert F, Lyon-Caen O, Chabas D. Paroxysmal hypothermia as a clinical feature of multiple sclerosis. Neurology 72: 193-195, 2009.
84. White AT, Davis SL, Vener JM, Wendt L. Effect of increased core temperature on cortical excitability and fatigue in multiple sclerosis patients (Abstract). Med Sci Sports Exerc 40: S300, 2008.
85. White AT, Davis SL, Wilson TE. Metabolic, thermoregulatory, and perceptual responses during exercise after lower vs. whole body precooling. J Appl Physiol 94: 1039-1044, 2003.
86. White AT, Wilson TE, Davis SL, Petajan JH. Effect of precooling on physical performance in multiple sclerosis. Mult Scler 6: 176-180, 2000.
87. White KD, Scoones DJ, Newman PK. Hypothermia in multiple sclerosis. J Neurol Neurosurg Psychiatry 61: 369-375, 1996.
88. White LJ, Dressendorfer RH. Exercise and multiple sclerosis. Sports Med 34: 1077-1100, 2004.
89. Wilson TE, Johnson SC, Petajan JH, Davis SL, Gappmaier E, Luetkemeier MJ, White AT. Thermal regulatory responses to submaximal cycling following lower-body cooling in humans. Eur J Appl Physiol 88: 67-75, 2002.
90. Wilson TE, Monahan KD, Fogelman A, Kearney ML, Sauder CL, Ray CA. Aerobic training improves in vivo cholinergic responsiveness but not sensitivity of eccrine sweat glands. J Invest Dermatol 130: 2328-2330, 2010.
91. Young AJ, Sawka MN, Epstein Y, Decristofano B, Pandolf KB. Cooling different body surfaces during upper and lower body exercise. J Appl Physiol 63: 1218-1223, 1987.