Download PDF
Int J Sports Med 2014; 35(12): 975-981
DOI: 10.1055/s-0034-1368724
Review
© Georg Thieme Verlag KG Stuttgart · New York

Does Heat Acclimation Improve Exercise Capacity at Altitude? A Cross-tolerance Model

A. C. White
1   Health, Exercise and Sports Sciences, University of New Mexico, Albuquerque, United States
,
R. M. Salgado
1   Health, Exercise and Sports Sciences, University of New Mexico, Albuquerque, United States
,
S. Schneider
1   Health, Exercise and Sports Sciences, University of New Mexico, Albuquerque, United States
,
J. A. Loeppky
1   Health, Exercise and Sports Sciences, University of New Mexico, Albuquerque, United States
,
T. A. Astorino
2   Kinesiology, CSU-San Marcos, San Marcos, United States
,
C. M. Mermier
1   Health, Exercise and Sports Sciences, University of New Mexico, Albuquerque, United States
› Author Affiliations
Further Information

Publication History



accepted after revision 10 January 2014

Publication Date:
09 May 2014 (online)

Also available at
    Permissions and Reprints

Abstract

New approaches to inducing altitude acclimation in a relatively short timeframe are needed, as it is not practical for many soldiers and athletes to gain access to specialized training facilities. Acclimation to one environmental stressor could enhance adaptation to various other stressors in animals and humans. This phenomenon has been described as cross-tolerance and involves the activation of common protective pathways. The purpose of this review is to discuss possible mechanisms involved in the cross-tolerance between heat and hypoxia. Future data could potentially support the use of a cross-tolerance model as a means for military personnel to prepare for deployment to high-altitude environments, as well as for athletes competing at high altitude.

Key words

hypoxia - plasma volume - performance
 

  • References

  • 1 Alexander JK, Grover RF. Mechanism of reduced cardiac stroke volume at high altitude. Clin Cardiol 1983; 6: 301-303
    CrossrefPubMedSearch in Google Scholar
  • 2 Aoyagi Y, McLellan TM, Shephard RJ. Effects of endurance training and heat acclimation on psychological strain in exercising men wearing protective clothing. Ergonomics 1998; 41: 328-357
    CrossrefPubMedSearch in Google Scholar
  • 3 Bass DE, Buskirk ER, Iampietro PF, Mager M. Comparison of blood volume during physical conditioning, heat acclimatization and sedentary living. J Appl Physiol 1958; 12: 186-188
    PubMedSearch in Google Scholar
  • 4 Bass DE, Henschel A. Responses of body fluid compartments to heat and cold. Physiol Rev 1956; 36: 128-144
    PubMedSearch in Google Scholar
  • 5 Beidleman BA, Muza SR, Fulco CS, Cymerman A, Ditzler DT, Stulz D, Staab JE, Robinson SR, Skrinar GS, Lewis SF, Sawka MN. Intermittent altitude exposures improve muscular performance at 4 300 m. J Appl Physiol 2003; 95: 1824-1832
    CrossrefPubMedSearch in Google Scholar
  • 6 Beidleman BA, Muza SR, Fulco CS, Cymerman A, Sawka MN, Lewis SF, Skrinar GS. Seven intermittent exposures to altitude improves exercise performance at 4 300 m. Med Sci Sports Exerc 2008; 40: 141-148
    CrossrefPubMedSearch in Google Scholar
  • 7 Berger NJ, Campbell IT, Wilkerson DP, Jones AM. Influence of acute plasma volume expansion on VO2 kinetics, VO2peak, and performance during high-intensity cycle exercise. J Appl Physiol 2006; 101: 707-714
    CrossrefPubMedSearch in Google Scholar
  • 8 Berglund B, Wide L. Erythropoietin concentrations and isoforms in urine of anonymous Olympic athletes during the Nagano Olympic Games. Scand J Med Sci Sports 2002; 12: 354-357
    CrossrefPubMedSearch in Google Scholar
  • 9 Buskirk ER, Kollias J, Akers RF, Prokop EK, Reategui EP. Maximal performance at altitude and on return from altitude in conditioned runners. J Appl Physiol 1967; 23: 259-266
    PubMedSearch in Google Scholar
  • 10 Calbet JA, Radegran G, Boushel R, Sondergaard H, Saltin B, Wagner PD. Plasma volume expansion does not increase maximal cardiac output or VO2max in lowlanders acclimatized to altitude. Am J Physiol 2004; 287: H1214-H1224
    PubMedSearch in Google Scholar
  • 11 Casas M, Casas H, Pages T, Rama R, Ricart A, Ventura JL, Ibanez J, Rodriguez FA, Viscor G. Intermittent hypobaric hypoxia induces altitude acclimation and improves the lactate threshold. Aviat Space Environ Med 2000; 71: 125-130
    PubMedSearch in Google Scholar
  • 12 Chapman RF, Stray-Gundersen J, Levine BD. Individual variation in response to altitude training. J Appl Physiol 1998; 85: 1448-1456
    PubMedSearch in Google Scholar
  • 13 Convertino VA. Blood volume: its adaptation to endurance training. Med Sci Sports Exerc 1991; 23: 1338-1348
    PubMedSearch in Google Scholar
  • 14 Coyle EF, Hopper MK, Coggan AR. Maximal oxygen uptake relative to plasma volume expansion. Int J Sports Med 1990; 11: 116-119
    Thieme ConnectPubMedSearch in Google Scholar
  • 15 Eckardt KU, Boutellier U, Kurtz A, Schopen M, Koller EA, Bauer C. Rate of erythropoietin formation in humans in response to acute hypobaric hypoxia. J Appl Physiol 1989; 66: 1785-1788
    PubMedSearch in Google Scholar
  • 16 Febbraio MA, Snow RJ, Hargreaves M, Stathis CG, Martin IK, Carey MF. Muscle metabolism during exercise and heat stress in trained men: effect of acclimation. J Appl Physiol 1994; 76: 589-597
    PubMedSearch in Google Scholar
  • 17 Feldser D, Agani F, Iyer NV, Pak B, Ferreira G, Semenza GL. Reciprocal positive regulation of hypoxia-inducible factor 1alpha and insulin-like growth factor 2. Cancer Res 1999; 59: 3915-3918
    PubMedSearch in Google Scholar
  • 18 Fortney SM, Wenger CB, Bove JR, Nadel ER. Effect of blood volume on forearm venous and cardiac stroke volume during exercise. J Appl Physiol 1983; 55: 884-890
    PubMedSearch in Google Scholar
  • 19 Fregly MJ. Cross-acclimatization between cold and altitude in rats. Am J Physiol 1954; 176: 267-274
    PubMedSearch in Google Scholar
  • 20 Fulco CS, Rock PB, Cymerman A. Maximal and submaximal exercise performance at altitude. Aviat Space Environ Med 1998; 69: 793-801
    PubMedSearch in Google Scholar
  • 21 Gagge AP, Nishi Y. Heat exchange between human skin surface and thermal environment. Compr Physiol 2011; 69-92
    PubMedSearch in Google Scholar
  • 22 Gallagher SA, Hackett PH. High-altitude illness. Emerg Med Clin North Am 2004; 22: 329-355
    CrossrefPubMedSearch in Google Scholar
  • 23 Ge RL, Witkowski S, Zhang Y, Alfrey C, Sivieri M, Karlsen T, Resaland GK, Harber M, Stray-Gundersen J, Levine BD. Determinants of erythropoietin release in response to short-term hypobaric hypoxia. J Appl Physiol 2002; 92: 2361-2367
    CrossrefPubMedSearch in Google Scholar
  • 24 Gore CJ, Little SC, Hahn AG, Scroop GC, Norton KI, Bourdo PC, Woolford SM, Buckley JD, Stanef T, Campbell DP, Watson DB, Emonson DL. Reduced performance of male and female athletes at 580 m altitude. Eur J Appl Physiol 1997; 75: 136-143
    CrossrefPubMedSearch in Google Scholar
  • 25 Grant SM, Green HJ, Phillips SM, Enns DL, Sutton JR. Fluid and electrolyte hormonal responses to exercise and acute plasma volume expansion. J Appl Physiol 1996; 81: 2386-2392
    PubMedSearch in Google Scholar
  • 26 Green HJ, Roy B, Grant S, Hughson R, Burnett M, Otto C, Pipe A, McKenzie D, Johnson M. Increases in submaximal cycling efficiency mediated by altitude acclimatization. J Appl Physiol 2000; 89: 1189-1197
    PubMedSearch in Google Scholar
  • 27 Greenleaf JE, Brock PJ. Na+ and Ca2+ ingestion: plasma volume-electrolyte distribution at rest and exercise. J Appl Physiol 1980; 48: 838-847
    PubMedSearch in Google Scholar
  • 28 Greenleaf JE, Greenleaf J, Card DH, Saltin B. Exercise-temperature regulation in man during acute exposure to simulated altitude. J Appl Physiol 1969; 26: 290-296
    PubMedSearch in Google Scholar
  • 29 Hackett PH, Roach RC. High-altitude illness. N Engl J Med 2001; 345: 107-114
    CrossrefPubMedSearch in Google Scholar
  • 30 Harrison MH. Effects on thermal stress and exercise on blood volume in humans. Physiol Rev 1985; 65: 149-209
    CrossrefPubMedSearch in Google Scholar
  • 31 Heinicke K, Heinicke I, Schmidt W, Wolfarth B. A three-week traditional altitude training increases hemoglobin mass and red cell volume in elite biathlon athletes. Int J Sports Med 2005; 26: 350-355
    Thieme ConnectPubMedSearch in Google Scholar
  • 32 Heled Y, Peled A, Yanovich R, Shargal E, Pilz-Burstein R, Epstein Y, Moran DS. Heat acclimation and performance in hypoxic conditions. Aviat Space Environ Med 2012; 83: 649-653
    CrossrefPubMedSearch in Google Scholar
  • 33 Hiestand WA, Stemler FW, Jasper RL. Increased anoxic resistance resulting from short period heat adaptation. Proc Soc Exp Biol Med 1955; 88: 94-95
    CrossrefPubMedSearch in Google Scholar
  • 34 Hopper MK, Coggan AR, Coyle EF. Exercise stroke volume relative to plasma-volume expansion. J Appl Physiol 1988; 64: 404-408
    PubMedSearch in Google Scholar
  • 35 Horowitz M. Matching the heart to heat-induced circulatory load: heat-acclimatory responses. News Physiol Sci 2003; 18: 215-221
    PubMedSearch in Google Scholar
  • 36 Horowitz M, Eli-Berchoer L, Wapinski I, Friedman N, Kodesh E. Stress-related genomic responses during the course of heat acclimation and its association with ischemic-reperfusion cross-tolerance. J Appl Physiol 2004; 97: 1496-1507
    CrossrefPubMedSearch in Google Scholar
  • 37 Horowitz M, Parnes S, Hasin Y. Mechanical and metabolic performance of the rat heart: effects of combined stress of heat acclimation and swimming training. J Basic Clin Physiol Pharmacol 1993; 4: 139-156
    PubMedSearch in Google Scholar
  • 38 Horowitz M, Peyser YM, Muhlrad A. Alterations in cardiac myosin isoenzymes distribution as an adaptation to chronic environmental heat stress in the rat. J Mol Cell Cardiol 1986; 18: 511-515
    CrossrefPubMedSearch in Google Scholar
  • 39 Horowitz M, Shimoni Y, Parnes S, Gotsman MS, Hasin Y. Heat acclimation: cardiac performance of isolated rat heart. J Appl Physiol 1986; 60: 9-13
    PubMedSearch in Google Scholar
  • 40 Kanstrup IL, Ekblom B. Acute hypervolemia, cardiac performance, and aerobic power during exercise. J Appl Physiol 1982; 52: 1186-1191
    PubMedSearch in Google Scholar
  • 41 Leblanc J. Stress and interstress adaptation. Fed Proc 1969; 28: 996-1000
    PubMedSearch in Google Scholar
  • 42 Levi E, Vivi A, Hasin Y, Tassini M, Navon G, Horowitz M. Heat acclimation improves cardiac mechanics and metabolic performance during ischemia and reperfusion. J Appl Physiol 1993; 75: 833-839
    PubMedSearch in Google Scholar
  • 43 Levine BD, Stray-Gundersen J. “Living high-training low”: effect of moderate-altitude acclimatization with low-altitude training on performance. J Appl Physiol 1997; 83: 102-112
    PubMedSearch in Google Scholar
  • 44 Levy E, Hasin Y, Navon G, Horowitz M. Chronic heat improves mechanical and metabolic response of trained rat heart on ischemia and reperfusion. Am J Physiol 1997; 272: H2085-H2094
    PubMedSearch in Google Scholar
  • 45 Lorenzo S, Halliwill JR, Sawka MN, Minson CT. Heat acclimation improves exercise performance. J Appl Physiol 2010; 109: 1140-1147
    CrossrefPubMedSearch in Google Scholar
  • 46 Lundby C, Millet GP, Calbet JA, Bartsch P, Subudhi AW. Does ‘altitude training’ increase exercise performance in elite athletes?. Br J Sports Med 2012; 46: 792-795
    CrossrefPubMedSearch in Google Scholar
  • 47 Lunt HC, Barwood MJ, Corbett J, Tipton MJ. ‘Cross-adaptation’: habituation to short repeated cold-water immersions affects the response to acute hypoxia in humans. J Physiol 2010; 588: 3605-3613
    CrossrefPubMedSearch in Google Scholar
  • 48 Maher JT, Jones LG, Hartley LH. Effects of high-altitude exposure on submaximal endurance capacity of men. J Appl Physiol 1974; 37: 895-898
    PubMedSearch in Google Scholar
  • 49 Mairbaurl H, Schobersberger W, Humpeler E, Hasibeder W, Fischer W, Raas E. Beneficial effects of exercising at moderate altitude on red cell oxygen transport and on exercise performance. Pflugers Arch 1986; 406: 594-599
    CrossrefPubMedSearch in Google Scholar
  • 50 Maloyan A, Eli-Berchoer L, Semenza GL, Gerstenblith G, Stern MD, Horowitz M. HIF-1alpha-targeted pathways are activated by heat acclimation and contribute to acclimation-ischemic cross-tolerance in the heart. Physiol Genomics 2005; 23: 79-88
    CrossrefPubMedSearch in Google Scholar
  • 51 Mazzeo RS, Bender PR, Brooks GA, Butterfield GE, Groves BM, Sutton JR, Wolfel EE, Reeves JT. Arterial catecholamine responses during exercise with acute and chronic high-altitude exposure. Am J Physiol 1991; 261: E419-E424
    PubMedSearch in Google Scholar
  • 52 Mazzeo RS, Wolfel EE, Butterfield GE, Reeves JT. Sympathetic response during 21 days at high altitude (4 300 m) as determined by urinary and arterial catecholamines. Metabolism 1994; 43: 1226-1232
    CrossrefPubMedSearch in Google Scholar
  • 53 Miyagawa K, Kamijo Y, Ikegawa S, Goto M, Nose H. Reduced hyperthermia-induced cutaneous vasodilation and enhanced exercise-induced plasma water loss at simulated high altitude (3 200 m) in humans. J Appl Physiol 2011; 110: 157-165
    CrossrefPubMedSearch in Google Scholar
  • 54 Muza SR, Beidleman BA, Fulco CS. Altitude preexposure recommendations for inducing acclimatization. High Alt Med Biol 2010; 11: 87-92
    CrossrefPubMedSearch in Google Scholar
  • 55 Nadel ER, Fortney SM, Wenger CB. Effect of hydration state of circulatory and thermal regulations. J Appl Physiol 1980; 49: 715-721
    CrossrefPubMedSearch in Google Scholar
  • 56 Nielsen B, Hales JR, Strange S, Christensen NJ, Warberg J, Saltin B. Human circulatory and thermoregulatory adaptations with heat acclimation and exercise in a hot, dry environment. J Physiol 1993; 460: 467-485
    CrossrefPubMedSearch in Google Scholar
  • 57 Pandolf KB. Time course of heat acclimation and its decay. Int J Sports Med 1998; 19 (Suppl. 02) S157-S160
    Thieme ConnectPubMedSearch in Google Scholar
  • 58 Patterson MJ, Stocks JM, Taylor NA. Sustained and generalized extracellular fluid expansion following heat acclimation. J Physiol 2004; 559: 327-334
    CrossrefPubMedSearch in Google Scholar
  • 59 Pugh LG. Blood volume and haemoglobin concentration at altitudes above 18 000 ft. (5 500 M). J Physiol 1964; 170: 344-354
    CrossrefPubMedSearch in Google Scholar
  • 60 Rasmussen P, Siebenmann C, Diaz V, Lundby C. Red cell volume expansion at altitude: a meta-analysis and Monte Carlo simulation. Med Sci Sports Exerc 2013; 45: 1767-1772
    CrossrefPubMedSearch in Google Scholar
  • 61 Roach RC, Maes D, Sandoval D, Robergs RA, Icenogle M, Hinghofer-Szalkay H, Lium D, Loeppky JA. Exercise exacerbates acute mountain sickness at simulated high altitude. J Appl Physiol 2000; 88: 581-585
    PubMedSearch in Google Scholar
  • 62 Robach P, Cairo G, Gelfi C, Bernuzzi F, Pilegaard H, Vigano A, Santambrogio P, Cerretelli P, Calbet JA, Moutereau S, Lundby C. Strong iron demand during hypoxia-induced erythropoiesis is associated with down-regulation of iron-related proteins and myoglobin in human skeletal muscle. Blood 2007; 109: 4724-4731
    CrossrefPubMedSearch in Google Scholar
  • 63 Robach P, Dechaux M, Jarrot S, Vaysse J, Schneider JC, Mason NP, Herry JP, Gardette B, Richalet JP. Operation Everest III: role of plasma volume expansion on VO2max during prolonged high-altitude exposure. J Appl Physiol 2000; 89: 29-37
    PubMedSearch in Google Scholar
  • 64 Roy BD, Green HJ, Grant SM, Tarnopolsky MA. Acute plasma volume expansion alters cardiovascular but not thermal function during moderate intensity prolonged exercise. Can J Physiol Pharmacol 2000; 78: 244-250
    CrossrefPubMedSearch in Google Scholar
  • 65 Saunders PU, Telford RD, Pyne DB, Cunningham RB, Gore CJ, Hahn AG, Hawley JA. Improved running economy in elite runners after 20 days of simulated moderate-altitude exposure. J Appl Physiol 2004; 96: 931-937
    CrossrefPubMedSearch in Google Scholar
  • 66 Savourey G, Garcia N, Besnard Y, Hanniquet AM, Fine MO, Bittel J. Physiological changes induced by pre-adaptation to high altitude. Eur J Appl Physiol 1994; 69: 221-227
    CrossrefPubMedSearch in Google Scholar
  • 67 Sawka MN, Convertino VA, Eichner ER, Schnieder SM, Young AJ. Blood volume: importance and adaptations to exercise training, environmental stresses, and trauma/sickness. Med Sci Sports Exerc 2000; 32: 332-348
    CrossrefPubMedSearch in Google Scholar
  • 68 Sawka MN, Coyle EF. Influence of body water and blood volume on thermoregulation and exercise performance in the heat. Exerc Sport Sci Rev 1999; 27: 167-218
    PubMedSearch in Google Scholar
  • 69 Sawka MN, Pandolf KB, Avellini BA, Shapiro Y. Does heat acclimation lower the rate of metabolism elicited by muscular exercise?. Aviat Space Environ Med 1983; 54: 27-31
    PubMedSearch in Google Scholar
  • 70 Semenza GL. Hypoxia-inducible factor 1: master regulator of O2 homeostasis. Curr Opin Genet Dev 1998; 8: 588-594
    CrossrefPubMedSearch in Google Scholar
  • 71 Semenza GL. Hydroxylation of HIF-1: oxygen sensing at the molecular level. Physiology 2004; 19: 176-182
    CrossrefPubMedSearch in Google Scholar
  • 72 Senay Jr LC, Pivarnik JM. Fluid shifts during exercise. Exerc Sport Sci Rev 1985; 13: 335-387
    PubMedSearch in Google Scholar
  • 73 Senay LC, Mitchell D, Wyndham CH. Acclimatization in a hot, humid environment: body fluid adjustments. J Appl Physiol 1976; 40: 786-796
    PubMedSearch in Google Scholar
  • 74 Shepherd J, Vanhoutte PM. Integrated responses of the cardiovascular system to stress. In: Shepherd J, Vanhoutte PM. 3rd ed. The Human Cardiovascular System. New York: Raven; 1980: 156-179
    Search in Google Scholar
  • 75 Sjogaard G, Adams RP, Saltin B. Water and ion shifts in skeletal muscle of humans with intense dynamic knee extension. Am J Physiol 1985; 248: R190-R196
    PubMedSearch in Google Scholar
  • 76 Stenberg J, Ekblom B, Messin R. Hemodynamic response to work at simulated altitude, 4 000 m. J Appl Physiol 1966; 21: 1589-1594
    PubMedSearch in Google Scholar
  • 77 Takamata A, Nose H, Kinoshita T, Hirose M, Itoh T, Morimoto T. Effect of acute hypoxia on vasopressin release and intravascular fluid during dynamic exercise in humans. Am J Physiol 2000; 279: R161-R168
    PubMedSearch in Google Scholar
  • 78 Terrados N, Jansson E, Sylven C, Kaijser L. Is hypoxia a stimulus for synthesis of oxidative enzymes and myoglobin?. J Appl Physiol 1990; 68: 2369-2372
    PubMedSearch in Google Scholar
  • 79 Tipton M. A case for combined environmental stressor studies. Extrem Physiol Med 2012; 1: 7
    CrossrefPubMedSearch in Google Scholar
  • 80 Warburton DE, Gledhill N, Jamnik VK, Krip B, Card N. Induced hypervolemia, cardiac function, VO2max, and performance of elite cyclists. Med Sci Sports Exerc 1999; 31: 800-808
    CrossrefPubMedSearch in Google Scholar
  • 81 Watt MJ, Garnham AP, Febbraio MA, Hargreaves M. Effect of acute plasma volume expansion on thermoregulation and exercise performance in the heat. Med Sci Sports Exerc 2000; 32: 958-962
    PubMedSearch in Google Scholar
  • 82 Wegner B. Human heat acclimation. In: Pandolf K, Sawka MN, Gonzalez RR. Human Performance Physiology and Environmental Medicine at Terrestrial Extremes. Indianapolis: Benchmark Press, Inc; 1988: 153-197
    Search in Google Scholar
  • 83 West JB, Boyer SJ, Graber DJ, Hackett PH, Maret KH, Milledge JS, Peters Jr RM, Pizzo CJ, Samaja M, Sarnquist FH, Schoene RB, Winslow RM. Maximal exercise at extreme altitudes on Mount Everest. J Appl Physiol 1983; 55: 688-698
    PubMedSearch in Google Scholar
  • 84 Wolfel EE, Groves BM, Brooks GA, Butterfield GE, Mazzeo RS, Moore LG, Sutton JR, Bender PR, Dahms TE, McCullough RE, McCullough RG, Huang S, Sun S, Grover RF, Hultgren HN, Reeves JT. Oxygen transport during steady-state submaximal exercise in chronic hypoxia. J Appl Physiol 1991; 70: 1129-1136
    PubMedSearch in Google Scholar
  • 85 Young AJ, Sawka MN, Levine L, Cadarette BS, Pandolf KB. Skeletal muscle metabolism during exercise is influenced by heat acclimation. J Appl Physiol 1985; 59: 1929-1935
    PubMedSearch in Google Scholar
  • 86 Zappe DH, Tankersley CG, Meister TG, Kenney WL. Fluid restriction prior to cycle exercise: effects on plasma volume and plasma proteins. Med Sci Sports Exerc 1993; 25: 1225-1230
    PubMedSearch in Google Scholar