Blood pressure regulation III: What happens when one system must serve two masters: Temperature and pressure regulation?

European Journal of Applied Physiology

Volumn 114, Issue 3, 2014, Pages 467-479

  Kenney, W Larry ^a   Stanhewicz, Anna E ^a   Bruning, Rebecca S ^a   Alexander, Lacy M ^a  

^a PENNSYLVANIA STATE UNIVERSITY   (United States)

Author keywords

Blood pressure; Cardiac output; Exercise; Heat stress; Skin blood flow

Indexed keywords

ANIMAL; BLOOD FLOW; BLOOD PRESSURE; BODY TEMPERATURE; EXERCISE; HUMAN; PHYSIOLOGY; REVIEW; TEMPERATURE;

ANIMALS; BLOOD PRESSURE; BODY TEMPERATURE; EXERCISE; HUMANS; REGIONAL BLOOD FLOW; TEMPERATURE;

EID: 84894646798     PISSN: 14396319     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00421-013-2652-5     Document Type: Review

References (87)

1. Andersen P, Saltin B (1985) Maximal perfusion of skeletal muscle in man. J Physiol 366:233-249
2. Basu R, Samet JM (2002) Relation between elevated ambient temperature and mortality: a review of the epidemiologic evidence. Epidemiol Rev 24(2):190-202
3. Bevegard BS, Shepherd JT (1966) Reaction in man of resistance and capacity vessels in forearm and hand to leg exercise. J Appl Physiol 21(1):123-132
4. Brengelmann GL, Johnson JM, Hermansen L, Rowell LB (1977) Altered control of skin blood flow during exercise at high internal temperatures. J Appl Physiol 43(5):790-794
5. Brothers RM, Bhella PS, Shibata S, Wingo JE, Levine BD, Crandall CG (2009) Cardiac systolic and diastolic function during whole body heat stress. Am J Physiol Heart Circ Physiol 296(4):H1150-H1156. doi: 10.1152/ajpheart.01069. 2008
6. Bruning RS, Dahmus JD, Kenney WL, Alexander LM (2013) Aspirin and Clopidogrel Alter Core Temperature and Skin Blood Flow during Heat Stress. Med Sci Sports Exerc 45(4):674-682
7. Crandall CG (2000) Carotid baroreflex responsiveness in heat-stressed humans. Am J Physiol Heart Circ Physiol 279(4):H1955-H1962
8. Crandall CG (2008) Heat stress and baroreflex regulation of blood pressure. Med Sci Sports Exerc 40(12):2063-2070. doi: 10.1249/MSS. 0b013e318180bc98
9. Crandall CG, Gonzalez-Alonso J (2010) Cardiovascular function in the heat-stressed human. Acta Physiol (Oxf) 199(4):407-423. doi: 10.1111/j.1748-1716.2010.02119.xAPS2119
10. Crandall CG, Johnson JM, Kosiba WA, Kellogg DL Jr (1996) Baroreceptor control of the cutaneous active vasodilator system. J Appl Physiol 81(5):2192-2198
11. Crandall CG, Wilson TE, Marving J, Vogelsang TW, Kjaer A, Hesse B, Secher NH (2008) Effects of passive heating on central blood volume and ventricular dimensions in humans. J Physiol 586(1):293-301. doi: 10.1113/jphysiol.2007. 143057
12. Cui J, Wilson TE, Crandall CG (2002) Baroreflex modulation of sympathetic nerve activity to muscle in heat-stressed humans. Am J Physiol Regul Integr Comp Physiol 282(1):R252-R258. doi: 10.1152/ajpregu.00337.2001
13. Dastre A, Morat JP (1884) Influence du sang asphyxique sur l'appareil nerveux de la circulation. American Heart Journal 76:769-774
14. Durand S, Davis SL, Cui J, Crandall CG (2005) Exogenous nitric oxide inhibits sympathetically mediated vasoconstriction in human skin. J Physiol 562(Pt 2):629-634. doi: 10.1113/jphysiol.2004.075747
15. Gagge AP, Gonzalez RR (2010) Mechanisms of heat exchange: biophysics and physiology. In: Comprehensive physiology, Wiley, Inc., USA. doi: 10.1002/cphy.cp040104
16. Gonzalez-Alonso J (1998) Separate and combined influences of dehydration and hyperthermia on cardiovascular responses to exercise. Int J Sports Med 19(Suppl 2):S111-S114
17. Gonzalez-Alonso J, Calbet JA, Nielsen B (1998) Muscle blood flow is reduced with dehydration during prolonged exercise in humans. J Physiol 513(Pt 3):895-905
18. Gonzalez-Alonso J, Mora-Rodriguez R, Coyle EF (1999a) Supine exercise restores arterial blood pressure and skin blood flow despite dehydration and hyperthermia. Am J Physiol 277(2 Pt 2):H576-H583
19. Gonzalez-Alonso J, Teller C, Andersen SL, Jensen FB, Hyldig T, Nielsen B (1999b) Influence of body temperature on the development of fatigue during prolonged exercise in the heat. J Appl Physiol 86(3):1032-1039
20. Hagbarth KE, Hallin RG, Hongell A, Torebjork HE, Wallin BG (1972) General characteristics of sympathetic activity in human skin nerves. Acta Physiol Scand 84(2):164-176
21. Havenith G, Inoue Y, Luttikholt V, Kenney WL (1995) Age predicts cardiovascular, but not thermoregulatory, responses to humid heat stress. Eur J Appl Physiol 70(1):88-96
22. Hodges GJ, Kosiba WA, Zhao K, Alvarez GE, Johnson JM (2007) The role of baseline in the cutaneous vasoconstrictor responses during combined local and whole body cooling in humans. Am J Physiol Heart Circ Physiol 293(5):H3187-H3192. doi: 10.1152/ajpheart.00815.2007
23. Holowatz LA, Kenney WL (2010) Peripheral mechanisms of thermoregulatory control of skin blood flow in aged humans. J Appl Physiol 109(5):1538-1544. doi: 10.1152/japplphysiol.00338.2010
24. Holowatz LA, Thompson-Torgerson CS, Kenney WL (2007) Altered mechanisms of vasodilation in aged human skin. Exerc Sport Sci Rev 35(3):119-125. doi: 10.1097/jes.0b013e3180a02f85
25. Holowatz LA, Thompson-Torgerson C, Kenney WL (2010) Aging and the control of human skin blood flow. Front Biosci: J Virtual Libr 15:718-739. doi: 3642
26. Johnson JM (2010) Exercise in a hot environment: the skin circulation. Scand J Med Sci Sports 20(Suppl 3):29-39. doi: 10.1111/j.1600-0838.2010.01206.x
27. Johnson JM, Park MK (1982) Effect of heat stress on cutaneous vascular responses to the initiation of exercise. J Appl Physiol 53(3):744-749
28. Johnson JM, Niederberger M, Rowell LB, Eisman MM, Brengelmann GL (1973) Competition between cutaneous vasodilator and vasoconstrictor reflexes in man. J Appl Physiol 35(6):798-803
29. Johnson JM, Rowell LB, Brengelmann GL (1974) Modification of the skin blood flow-body temperature relationship by upright exercise. J Appl Physiol 37(6):880-886
30. Johnson JM, Brengelmann GL, Hales JR, Vanhoutte PM, Wenger CB (1986) Regulation of the cutaneous circulation. Fed Proc 45(13):2841-2850
31. Keller DM, Cui J, Davis SL, Low DA, Crandall CG (2006) Heat stress enhances arterial baroreflex control of muscle sympathetic nerve activity via increased sensitivity of burst gating, not burst area, in humans. J Physiol 573(Pt 2):445-451. doi: jphysiol.2006.10866210.1113/jphysiol.2006.108662
32. Keller DM, Low DA, Wingo JE, Brothers RM, Hastings J, Davis SL, Crandall CG (2009) Acute volume expansion preserves orthostatic tolerance during whole-body heat stress in humans. J Physiol 587(Pt 5):1131-1139. doi: 10.1113/jphysiol.2008.165118
33. Keller DM, Sander M, Stallknecht B, Crandall CG (2010) alpha-Adrenergic vasoconstrictor responsiveness is preserved in the heated human leg. J Physiol 588(Pt 19):3799-3808. doi: 10.1113/jphysiol.2010.194506
34. Kellogg DL Jr, Johnson JM, Kosiba WA (1991a) Competition between cutaneous active vasoconstriction and active vasodilation during exercise in humans. Am J Physiol 261(4 Pt 2):H1184-H1189
35. Kellogg DL Jr, Johnson JM, Kosiba WA (1991b) Control of internal temperature threshold for active cutaneous vasodilation by dynamic exercise. J Appl Physiol 71(6):2476-2482
36. Kellogg DL Jr, Crandall CG, Liu Y, Charkoudian N, Johnson JM (1998) Nitric oxide and cutaneous active vasodilation during heat stress in humans. J Appl Physiol: Respir, Environ Exerc Physiol 85(3):824-829
37. Kenney WL, Tankersley CG, Newswanger DL, Hyde DE, Puhl SM, Turner NL (1990) Age and hypohydration independently influence the peripheral vascular response to heat stress. J Appl Physiol 68(5):1902-1908
38. Kenney WL, Tankersley CG, Newswanger DL, Puhl SM (1991) Alpha 1-adrenergic blockade does not alter control of skin blood flow during exercise. Am J Physiol Heart Circ Physiol 260(3 Pt 2):H855-H861
39. Kenny GP, Gagnon D, Dorman LE, Hardcastle SG, Jay O (2010) Heat balance and cumulative heat storage during exercise performed in the heat in physically active younger and middle-aged men. Eur J Appl Physiol 109(1):81-92. doi: 10.1007/s00421-009-1266-4
40. Lee JF, Harrison ML, Brown SR, Brothers RM (2012) The magnitude of heat-stress induced reductions in cerebral perfusion does not predict heat-stress induced reductions in tolerance to a simulated hemorrhage. J Appl Physiol. doi: 10.1152/japplphysiol.00878.2012
41. Lind AR (1963) A physiological criterion for setting thermal environmental limits for everyday work. J Appl Physiol 18:51-56
42. Low DA, Wingo JE, Keller DM, Davis SL, Zhang R, Crandall CG (2008) Cerebrovascular responsiveness to steady-state changes in end-tidal CO2 during passive heat stress. J Appl Physiol 104(4):976-981. doi: 10.1152/japplphysiol. 01040.2007
43. Low DA, Keller DM, Wingo JE, Brothers RM, Crandall CG (2011) Sympathetic nerve activity and whole body heat stress in humans. J Appl Physiol 111(5):1329-1334. doi: 10.1152/japplphysiol.00498.2011
44. Lucas RA, Ganio MS, Pearson J, Crandall CG (2012) Sweat loss during heat stress contributes to subsequent reductions in lower-body negative pressure tolerance. Exp Physiol. doi: 10.1113/expphysiol.2012.068171
45. Mack G, Nose H, Nadel ER (1988) Role of cardiopulmonary baroreflexes during dynamic exercise. J Appl Physiol 65(4):1827-1832
46. Mack GW, Nose H, Takamata A, Okuno T, Morimoto T (1994) Influence of exercise intensity and plasma volume on active cutaneous vasodilation in humans. Med Sci Sports Exerc 26(2):209-216
47. Minson CT, Wladkowski SL, Cardell AF, Pawelczyk JA, Kenney WL (1998) Age alters the cardiovascular response to direct passive heating. J Appl Physiol 84(4):1323-1332
48. Minson CT, Wladkowski SL, Pawelczyk JA, Kenney WL (1999) Age, splanchnic vasoconstriction, and heat stress during tilting. Am J Physiol 276(1 Pt 2):R203-R212
49. Minson CT, Berry LT, Joyner MJ (2001) Nitric oxide and neurally mediated regulation of skin blood flow during local heating. J Appl Physiol 91(4):1619-1626
50. Mortensen SP, Dawson EA, Yoshiga CC, Dalsgaard MK, Damsgaard R, Secher NH, Gonzalez-Alonso J (2005) Limitations to systemic and locomotor limb muscle oxygen delivery and uptake during maximal exercise in humans. J Physiol 566(Pt 1):273-285. doi: 10.1113/jphysiol.2005.086025
51. Nadel ER (1980) Circulatory and thermal regulations during exercise. Fed Proc 39(5):1491-1497
52. Nadel ER (1986) Non-thermal influences on the control of skin blood flow have minimal effects on heat transfer during exercise. Yale J Biol Med 59(3):321-327
53. Nadel ER, Cafarelli E, Roberts MF, Wenger CB (1979) Circulatory regulation during exercise in different ambient temperatures. J Appl Physiol 46(3):430-437
54. Nagashima K, Nose H, Takamata A, Morimoto T (1998) Effect of continuous negative-pressure breathing on skin blood flow during exercise in a hot environment. J Appl Physiol 84(6):1845-1851
55. Nelson MD, Haykowsky MJ, Stickland MK, Altamirano-Diaz LA, Willie CK, Smith KJ, Petersen SR, Ainslie PN (2011) Reductions in cerebral blood flow during passive heat stress in humans: partitioning the mechanisms. J Physiol 589(Pt 16):4053-4064. doi: 10.1113/jphysiol.2011.212118
56. Nielsen B (1996) Olympics in Atlanta: a fight against physics. Med Sci Sports Exerc 28(6):665-668
57. Nielsen B, Rowell LB, Bonde-Petersen F (1984) Cardiovascular responses to heat stress and blood volume displacements during exercise in man. Eur J Appl Physiol 52(4):370-374
58. Nielsen B, Savard G, Richter EA, Hargreaves M, Saltin B (1990) Muscle blood flow and muscle metabolism during exercise and heat stress. J Appl Physiol 69(3):1040-1046
59. Nishiyasu T, Shi X, Mack GW, Nadel ER (1993) Forearm vascular responses to baroreceptor unloading at the onset of dynamic exercise. J Appl Physiol 75(2):979-985
60. Normell LA, Wallin BG (1974) Sympathetic skin nerve activity and skin temperature changes in man. Acta Physiol Scand 91(3):417-426
61. Nose H, Mack GW, Shi XR, Morimoto K, Nadel ER (1990) Effect of saline infusion during exercise on thermal and circulatory regulations. J Appl Physiol 69(2):609-616
62. Pearson J (2011) Hemodynamic responses to heat stress in the resting and exercising human leg: insight into the effect of temperature on skeletal muscle blood flow. Am J Physiol Regul Integr Comp Physiol 300(3):R663-R673. doi: 10.1152/ajpregu.00662.2010
63. Pearson J, Lucas RA, Crandall CG (2012) Elevated local skin temperature impairs cutaneous vasoconstrictor responses to a simulated hemorrhagic challenge while heat stressed. Exp Physiol. doi: 10.1113/expphysiol.2012.068353
64. Pearson J, Lucas RA, Crandall CG (2013) Elevated local skin temperature impairs cutaneous vasoconstrictor responses to a simulated haemorrhagic challenge while heat stressed. Exp Physiol 98(2):444-450. doi: 10.1113/expphysiol.2012.068353
65. Roberts MF, Wenger CB (1980) Control of skin blood flow during exercise by thermal reflexes and baroreflexes. J Appl Physiol 48(4):717-723
66. Rowell LB (1974) Human cardiovascular adjustments to exercise and thermal stress. Physiol Rev 54(1):75-159
67. Rowell LB (1984) Reflex control of regional circulations in humans. J Auton Nerv Syst 11(2):101-114
68. Rowell LB (1986) Human circulation: regulation during physical stress. Oxford University Press, New York
69. Rowell LB (1993) Human cardiovascular control. Oxford University Press, New York
70. Rowell LB, Blackmon JR, Martin RH, Mazzarella JA, Bruce RA (1965) Hepatic clearance of indocyanine green in man under thermal and exercise stresses. J Appl Physiol 20(3):384-394
71. Rowell LB, Brengelmann GL, Blackmon JR, Twiss RD, Kusumi F (1968) Splanchnic blood flow and metabolism in heat-stressed man. J Appl Physiol 24(4):475-484
72. Savard GK, Nielsen B, Laszczynska J, Larsen BE, Saltin B (1988) Muscle blood flow is not reduced in humans during moderate exercise and heat stress. J Appl Physiol 64(2):649-657
73. Shastry S, Dietz NM, Halliwill JR, Reed AS, Joyner MJ (1998) Effects of nitric oxide synthase inhibition on cutaneous vasodilation during body heating in humans. J Appl Physiol: Respir, Environ Exerc Physiol 85(3):830-834
74. Shibasaki M, Durand S, Davis SL, Cui J, Low DA, Keller DM, Crandall CG (2007) Endogenous nitric oxide attenuates neutrally mediated cutaneous vasoconstriction. J Physiol 585(Pt 2):627-634. doi: 10.1113/jphysiol.2007.144030
75. Shibasaki M, Low DA, Davis SL, Crandall CG (2008) Nitric oxide inhibits cutaneous vasoconstriction to exogenous norepinephrine. J Appl Physiol 105(5):1504-1508. doi: 10.1152/japplphysiol.91017.2008
76. Smolander J, Holmer I (1991) Individual response to physical work in the heat in relation to sweating and skin blood flow. Int Arch Occup Environ Health 63(3):225-226
77. Taylor WF, Johnson JM, O'Leary DS, Park MK (1984) Modification of the cutaneous vascular response to exercise by local skin temperature. J Appl Physiol 57(6):1878-1884
78. Taylor WF, Johnson JM, Kosiba WA, Kwan CM (1988) Graded cutaneous vascular responses to dynamic leg exercise. J Appl Physiol 64(5):1803-1809
79. Taylor WF, Johnson JM, Kosiba WA (1990) Roles of absolute and relative load in skin vasoconstrictor responses to exercise. J Appl Physiol 69(3):1131-1136
80. Wilson TE, Crandall CG (2011) Effect of thermal stress on cardiac function. Exerc Sport Sci Rev 39(1):12-17. doi: 10.1097/JES.0b013e318201eed6
81. Wilson TE, Cui J, Crandall CG (2001) Absence of arterial baroreflex modulation of skin sympathetic activity and sweat rate during whole-body heating in humans. J Physiol 536(Pt 2):615-623 (pii: PHY-12483)
82. Wilson TE, Cui J, Zhang R, Witkowski S, Crandall CG (2002) Skin cooling maintains cerebral blood flow velocity and orthostatic tolerance during tilting in heated humans. J Appl Physiol 93(1):85-91. doi: 10.1152/japplphysiol.01043. 2001
83. Wilson TE, Tollund C, Yoshiga CC, Dawson EA, Nissen P, Secher NH, Crandall CG (2007) Effects of heat and cold stress on central vascular pressure relationships during orthostasis in humans. J Physiol 585(Pt 1):279-285. doi: 10.1113/jphysiol.2007.137901
84. Wilson TE, Brothers RM, Tollund C, Dawson EA, Nissen P, Yoshiga CC, Jons C, Secher NH, Crandall CG (2009) Effect of thermal stress on Frank-Starling relations in humans. J Physiol 587(Pt 13):3383-3392. doi: 10.1113/jphysiol.2009. 170381
85. Wingo JE, Low DA, Keller DM, Brothers RM, Shibasaki M, Crandall CG (2009) Effect of elevated local temperature on cutaneous vasoconstrictor responsiveness in humans. J Appl Physiol 106(2):571-575. doi: 10.1152/japplphysiol.91249.2008
86. Wyss CR, Brengelmann GL, Johnson JM, Rowell LB, Niederberger M (1974) Control of skin blood flow, sweating, and heart rate: role of skin vs. core temperature. J Appl Physiol 36(6):726-733
87. Yamazaki F, Sone R (2000) Modulation of arterial baroreflex control of heart rate by skin cooling and heating in humans. J Appl Physiol 88(2):393-400