Skip to main content
SpringerLink
Log in

Why Are High-Altitude Natives So Strong at Altitude? Maximal Oxygen Transport to the Muscle Cell in Altitude Natives

  • Chapter
  • First Online:
Hypoxia

Part of the book series: Advances in Experimental Medicine and Biology ((AEMB,volume 903))

Abstract

In hypoxia aerobic exercise performance of high-altitude natives is suggested to be superior to that of lowlanders; i.e., for a given altitude natives are reported to have higher maximal oxygen uptake (VO2max). The likely basis for this is a higher pulmonary diffusion capacity, which in turn ensures higher arterial O2 saturation (SaO2) and therefore also potentially a higher delivery of O2 to the exercising muscles. This review focuses on O2 transport in high-altitude Aymara. We have quantified femoral artery O2 delivery, arterial O2 extraction and calculated leg VO2 in Aymara, and compared their values with that of acclimatizing Danish lowlanders. All subjects were studied at 4100 m. At maximal exercise SaO2 dropped tremendously in the lowlanders, but did not change in the Aymara. Therefore arterial O2 content was also higher in the Aymara. At maximal exercise however, fractional O2 extraction was lower in the Aymara, and the a-vO2 difference was similar in both populations. The lower extraction levels in the Aymara were associated with lower muscle O2 conductance (a measure of muscle diffusion capacity). At any given submaximal exercise intensity, leg VO2 was always of similar magnitude in both groups, but at maximal exercise the lowlanders had higher leg blood flow, and hence also higher maximum leg VO2. With the induction of acute normoxia fractional arterial O2 extraction fell in the highlanders, but remained unchanged in the lowlanders. Hence high-altitude natives seem to be more diffusion limited at the muscle level as compared to lowlanders. In conclusion Aymara preserve very high SaO2 during hypoxic exercise (likely due to a higher lung diffusion capacity), but the effect on VO2max is reduced by a lower ability to extract O2 at the muscle level.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  1. Bastien GJ, Schepens B, Willems PA, Heglund NC. Energetics of load carrying in Nepalese porters. Science. 2005;308:1755.

    Article  CAS  PubMed  Google Scholar 

  2. Beall CM. Two routes to functional adaptation: Tibetan and Andean high-altitude natives. Proc Natl Acad Sci. 2007;104:8655–60.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Beall CM, Decker MJ, Brittenham GM, Kushner I, Gebremedhin A, Strohl KP. An Ethiopian pattern of human adaptation to high-altitude hypoxia. Proc Natl Acad Sci U S A. 2002;99:17215–8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Bellingham AJ, Detter JC, Lefant JC. Regulatory mechanisms of hemoglobin oxygen affinity in acidosis and alkalosis. J Clin Invest. 1971;50:700–6.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Bencowitz HZ, Wagner PD, West JB. Effect of change in P50 on exercise tolerance at high altitude: a theoretical study. J Appl Physiol. 1982;53:1487–95.

    CAS  PubMed  Google Scholar 

  6. Brody JS, Lahiri S, Simpser M, Motoyama EK, Velasquez T. Lung elasticity and airway dynamics in Peruvian natives to high altitude. J Appl Physiol. 1977;42:245–51.

    CAS  PubMed  Google Scholar 

  7. Brutsaert TD. Do high-altitude natives have enhanced exercise performance at altitude? Appl Physiol Nutr Metab. 2008;33:582–92.

    Article  CAS  PubMed  Google Scholar 

  8. Brutsaert TD, Haas JD, Spielvogel H. Absence of work efficiency differences during cycle ergometry exercise in Bolivian Aymara. High Alt Med Biol. 2004;5:41–59.

    Article  PubMed  Google Scholar 

  9. Brutsaert TD, Parra E, Shriver M, Gamboa A, Palaciso JA, Rivera M, Rodriguez I, Leon-Velarde F. Effects of birthplace and individual genetic admixture on lung volume and exercise phenotypes of Peruvian Quechua. Am J Phys Anthropol. 2004;123:390–8.

    Article  PubMed  Google Scholar 

  10. Brutsaert TD, Spielvogel H, Soria R, Caceres E, Buzenet G, Hass JD. Effect of developmental and ancestral high-altitude exposure on VO2peak of Andean and European/North American natives. Am J Phys Anthropol. 1999;110:435–55.

    Google Scholar 

  11. Brutsaert TD, Parra EJ, Shriver MD, Gamboa A, Palacios JA, Rivera M, Rodriguez I, Leon-Velarde F. Spanish genetic admixture is associated with larger VO2max decrement from sea level to 4,338 m in Peruvian Quechua. J Appl Physiol. 2003;95:519–28.

    Google Scholar 

  12. Calbet JAL, Boushel R, Radegran G, Sondergaard H, Wagner PD, Saltin B. Why is VO2max after altitude acclimatization still reduced despite normalization of arterial O2 content? Am J Physiol Regul Integr Comp Physiol. 2003;284:R304–16.

    Google Scholar 

  13. Calbet JAL, Robach P, Lundby C, Boushel R. Is pulmonary gas exchange during exercise in hypoxia impaired with the increase of cardiac output? Appl Physiol Nutr Metab. 2008;33:593–600.

    Article  CAS  PubMed  Google Scholar 

  14. Cerny FCDJA, Reddan WG. Pulmonary gas exchange in nonnative residents of high altitude. J Clin Invest. 1973;52:2993–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Chen QH, Ge RL, Wang XZ, Chen HX, Wu TY, Kobayashi T, Yoshimura K. Exercise performance of Tibetan and Han adolescents at altitudes of 3,417áand 4,300 m. J Appl Physiol. 1997;83:661–7.

    CAS  PubMed  Google Scholar 

  16. Claydon VE, Norcliffe LJ, Moore JP, Rivera-Ch M, Leon-Velarde F, Appenzeller O, Hainsworth R. Orthostatic tolerance and blood volumes in Andean high altitude dwellers. Exp Physiol. 2004;89:565–71.

    Article  CAS  PubMed  Google Scholar 

  17. DeGraff Jr AC, Grover RF, Johnson Jr RL, Hammond Jr JW, Miller JM. Diffusing capacity of the lung in Caucasians native to 3,100 m. J Appl Physiol. 1970;29:71–6.

    PubMed  Google Scholar 

  18. Dempsey JA, Reddan WG, Birnbaum ML, Forster HV, Thoden JS, Grover RF, Rankin J. Effects of acute through life-long hypoxic exposure on exercise pulmonary gas exchange. Respir Physiol. 1971;13:62–89.

    Article  CAS  PubMed  Google Scholar 

  19. Desplanches D, Hoppeler H, Tuscher L, Mayet MH, Spielvogel H, Ferretti G, Kayser B, Leuenberger M, Grunenfelder A, Favier R. Muscle tissue adaptations of high-altitude natives to training in chronic hypoxia or acute normoxia. J Appl Physiol. 1996;81:1946–51.

    CAS  PubMed  Google Scholar 

  20. Erzurum SC, Ghosh S, Janocha AJ, Xu W, Bauer S, Bryan NS, Tejero J, Hemann C, Hille R, Stuehr DJ, Feelisch M, Beall CM. Higher blood flow and circulating NO products offset high-altitude hypoxia among Tibetans. Proc Natl Acad Sci. 2007;104:17593–8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Favier R, Spielvogel H, Desplanches D, Ferretti G, Kayser B, Hoppeler H. Maximal exercise performance in chronic hypoxia and acute normoxia in high-altitude natives. J Appl Physiol. 1995;78:1868–74.

    CAS  PubMed  Google Scholar 

  22. Gamboa A, Gamboa JL, Holmes C, Sharabi Y, Leon-Velarde F, Fischman GJ, Appenzeller O, Goldstein DS. Plasma catecholamines and blood volume in native Andeans during hypoxia and normoxia. Clin Auton Res. 2006;16:40–5.

    Article  PubMed  Google Scholar 

  23. Garrido E, Rodas G, Javierre C, Segura R, Estruch VVRL. Cardiorespiratory response to exercise in elite Sherpa climbers transferred to sea level. Med Sci Sports Exerc. 1997;29:937–42.

    Article  CAS  PubMed  Google Scholar 

  24. Haseler LJ, Hogan MC, Richardson RS. Skeletal muscle phosphocreatine recovery in exercise-trained humans is dependent on O2 availability. J Appl Physiol. 1999;86:2013–8.

    CAS  PubMed  Google Scholar 

  25. Haseler LJ, Lin A, Hoff J, Richardson RS. Oxygen availability and PCr recovery rate in untrained human calf muscle: evidence of metabolic limitation in normoxia. Am J Physiol Regul Integr Comp Physiol. 2007;293:R2046–51.

    Article  CAS  PubMed  Google Scholar 

  26. Haseler LJ, Lin AP, Richardson RS. Skeletal muscle oxidative metabolism in sedentary humans: 31P-MRS assessment of O2 supply and demand limitations. J Appl Physiol. 2004;97:1077–81.

    Article  PubMed  Google Scholar 

  27. Hochachka PW. The lactate paradox: analysis of underlying mechanisms. Ann Sports Med. 1989;4:184–8.

    Google Scholar 

  28. Hochachka PW, Stanley C, Matheson GO, McKenzie DC, Allen PS, Parkhouse WS. Metabolic and work efficiencies during exercise in Andean natives. J Appl Physiol. 1991;70:1720–30.

    CAS  PubMed  Google Scholar 

  29. Hochachka PW, Stanley C, McKenzie DC, Villena A, Monge C. Enzyme mechanisms for pyruvate-to-lactate flux attenuation: a study of Sherpas, Quechuas, and hummingbirds. Int J Sports Med. 1992;13:S119–22.

    Article  CAS  PubMed  Google Scholar 

  30. Hsia CCW, Carbayo JJ, Yan X, Bellotto DJ. Enhanced alveolar growth and remodeling in Guinea pigs raised at high altitude. Respir Physiol Neurobiol. 2005;147:105–15.

    Article  PubMed  Google Scholar 

  31. Hurtado A. In: Dill DB, Adolph EE, Wiber CG, editors. Handbook of physiology. Washington DC: American Physiological Society; 1964. p. 843–60.

    Google Scholar 

  32. Johnson Jr RL, Cassidy SS, Grover RF, Schutte JE, Epstein RH. Functional capacities of lungs and thorax in beagles after prolonged residence at 3,100 m. J Appl Physiol. 1985;59:1773–82.

    PubMed  Google Scholar 

  33. Juel C, Lundby C, Sander M, Calbet JAL, van Hall G. Human skeletal muscle and erythrocyte proteins involved in acid-base homeostasis: adaptations to chronic hypoxia. J Physiol. 2003;548:639–48.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Kayser B, Hoppeler H, Claassen H, Cerretelli P. Muscle structure and performance capacity of Himalayan Sherpas. J Appl Physiol. 1991;70:1938–42.

    Article  CAS  PubMed  Google Scholar 

  35. Lundby C, Calbet JAL, Sander M, van Hall G, Mazzeo RS, Stray-Gundersen J, Stager JM, Chapman RF, Saltin B, Levine BD. Exercise economy does not change after acclimatization to moderate to very high altitude. Scand J Med Sci Sports. 2007;17:281–91.

    CAS  PubMed  Google Scholar 

  36. Lundby C, Calbet JAL, van Hall G, Saltin B, Sander M. Pulmonary gas exchange at maximal exercise in Danish lowlanders during 8 wk of acclimatization to 4,100 m and in high-altitude Aymara natives. Am J Physiol Regul Integr Comp Physiol. 2004;287:R1202–8.

    Article  CAS  PubMed  Google Scholar 

  37. Lundby C, Pilegaard H, Andersen JL, van Hall G, Sander M, Calbet JAL. Acclimatization to 4100 m does not change capillary density or mRNA expression of potential angiogenesis regulatory factors in human skeletal muscle. J Exp Biol. 2004;207:3865–71.

    Article  CAS  PubMed  Google Scholar 

  38. Lundby C, Sander M, van Hall G, Saltin B, Calbet JAL. Maximal exercise and muscle oxygen extraction in acclimatizing lowlanders and high altitude natives. J Physiol. 2006;573:535–47.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Mairbaurl H, Oelz O, Bartsch P. Interactions between Hb, Mg, DPG, ATP, and Cl determine the change in Hb-O2 affinity at high altitude. J Appl Physiol. 1993;74:40–8.

    Article  CAS  PubMed  Google Scholar 

  40. Malville NJ, Byrnes WC, Lim HA, Basnyat R. Commercial porters of eastern Nepal: health status, physical work capacity, and energy expenditure. Am J Hum Biol. 2001;13:44–56.

    Article  CAS  PubMed  Google Scholar 

  41. Marconi C, Marzorati M, Grassi B, Basnyat B, Colombini A, Kayser B, Cerretelli P. Second generation Tibetan lowlanders acclimatize to high altitude more quickly than Caucasians. J Physiol. 2004;556:661–71.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Marconi C, Marzorati M, Sciuto D, Ferri A, Cerretelli P. Economy of locomotion in high-altitude Tibetan migrants exposed to normoxia. J Physiol. 2005;569:667–75.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. McDonough P, Dane DM, Hsia CCW, Yilmaz C, Johnson Jr RL. Long-term enhancement of pulmonary gas exchange after high-altitude residence during maturation. J Appl Physiol. 2006;100:474–81.

    Article  PubMed  Google Scholar 

  44. Niu W, Wu Y, Li B, Chen N, Song S. Effects of long-term acclimatization in lowlanders migrating to high altitude: comparison with high altitude residents. Eur J Appl Physiol Occup Physiol. 1995;71:543–8.

    Article  CAS  PubMed  Google Scholar 

  45. Oelz O, Howald H, Di Prampero PE, Hoppeler H, Claassen H, Jenni R, Buhlmann A, Ferretti G, Bruckner JC, Veicsteinas A, et al. Physiological profile of world-class high-altitude climbers. J Appl Physiol. 1986;60:1734–42.

    CAS  PubMed  Google Scholar 

  46. Rådegran G. Exercise limb blood flow response to acute and chronic hypoxia in Danish lowlanders and Aymara natives. Acta Physiol. 2008;192:531–9.

    Article  Google Scholar 

  47. Reynafarje C, Lozano R, Valdivieso J. The polycythemia of high altitudes: iron metabolism and related aspects. Blood. 1959;14:433–55.

    CAS  PubMed  Google Scholar 

  48. Roach RC, Koskolou MD, Calbet JA, Saltin B. Arterial O2 content and tension in regulation of cardiac output and leg blood flow during exercise in humans. Am J Physiol Heart Circ Physiol. 1999;276:H438–45.

    CAS  Google Scholar 

  49. Saltin B, Grover RF, Blomqvist G, Hartley LH, Johnson Jr RL. Maximal oxygen uptake and cardiac output after 2 weeks at 4,350 m. J Appl Physiol. 1968;25:400–9.

    Google Scholar 

  50. Samaja M, Crespi T, Guazzi M, Vandegriff KF. Oxygen transport in blood at high altitude: role of the hemoglobin-oxygen affinity and impact of the phenomena related to hemoglobin allosterism and red cell function. Eur J Appl Physiol. 2003;90:351–9.

    Article  CAS  PubMed  Google Scholar 

  51. Sanchez C, Merino C, Figallo M. Simultaneous measurement of plasma volume and cell mass in polycythemia of high altitude. J Appl Physiol. 1970;28:775–8.

    CAS  PubMed  Google Scholar 

  52. Schoene RB. Limits of human lung function at high altitude. J Exp Biol. 2001;204:3121–7.

    CAS  PubMed  Google Scholar 

  53. Stringer W, Wasserman K, Casaburi R, Porszasz J, Maehara K, French W. Lactic acidosis as a facilitator of oxyhemoglobin dissociation during exercise. J Appl Physiol. 1994;76:1462–7.

    Article  CAS  PubMed  Google Scholar 

  54. van Hall G, Jensen-Urstad M, Rosdahl H, Holmberg HC, Saltin B, Calbet JAL. Leg and arm lactate and substrate kinetics during exercise. Am J Physiol Endocrinol Metab. 2003;284:E193–205.

    Article  PubMed  Google Scholar 

  55. van Hall G, Lundby C, Araoz M, Calbet JAL, Sander M, Saltin B. The lactate paradox revisited in lowlanders during acclimatization to 4100m and in high altitude natives. J Physiol. 2009;587(Pt 5):1117–29.

    Article  PubMed  PubMed Central  Google Scholar 

  56. Vogel JA, Hartley LH, Cruz JC. Cardiac output during exercise in altitude natives at sea level and high altitude. J Appl Physiol. 1974;36:173–6.

    CAS  PubMed  Google Scholar 

  57. Wagner PD, Sutton JR, Reeves JT, Cymerman A, Groves BM, Malconian MK. Operation Everest II: pulmonary gas exchange during a simulated ascent of Mt. Everest J Appl Physiol. 1987;63:2348–59.

    CAS  PubMed  Google Scholar 

  58. Wagner PD, Araoz M, Boushel R, Calbet JAL, Jessen B, Radegran G, Spielvogel H, Sondegaard H, Wagner H, Saltin B. Pulmonary gas exchange and acid-base state at 5,260 m in high-altitude Bolivians and acclimatized lowlanders. J Appl Physiol. 2002;92:1393–400.

    Article  PubMed  Google Scholar 

  59. West JB, Wagner PD. Predicted gas exchange on the summit of Mt. Everest Respir Physiol. 1980;42:1–16.

    Article  CAS  PubMed  Google Scholar 

  60. Winslow RM. Red cell properties and optimal oxygen transport. Adv Exp Med Biol. 1988;227:117–36.

    Article  CAS  PubMed  Google Scholar 

  61. Zhuang J, Droma T, Sutton JR, Groves BM, McCullough RE, McCullough RG, Sun S, Moore LG. Smaller alveolar-arterial O2 gradients in Tibetan than Han residents of Lhasa (3658 m). Respir Physiol. 1996;103:75–82.

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Zurich Center for Integrative Human Physiology, University of Zurich, Zürich, Switzerland

    Carsten Lundby

  2. Department of Physical Education, University of Las Palmas de Gran Canaria, Las Palmas, Spain

    Jose A. L. Calbet

  3. Research Institute of Biomedical and Health Sciences (IUIBS), Las Palmas de Gran Canaria, Canary Islands, Spain

    Jose A. L. Calbet

Authors
  1. Carsten Lundby
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jose A. L. Calbet
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Carsten Lundby or Jose A. L. Calbet .

Editor information

Editors and Affiliations

  1. Altitude Research Center, University of Colorado Anschutz Medical, AURORA, Colorado, USA

    Robert C. Roach

  2. Institute for Altitude Medicine, Telluride, Colorado, USA

    Peter H. Hackett

  3. Division of Physiology 0623A, University of California - San Diego, La Jolla, California, USA

    Peter D. Wagner

Rights and permissions

Reprints and permissions

Copyright information

© 2016 Springer Science+Business Media New York

About this chapter

Cite this chapter

Lundby, C., Calbet, J.A.L. (2016). Why Are High-Altitude Natives So Strong at Altitude? Maximal Oxygen Transport to the Muscle Cell in Altitude Natives. In: Roach, R., Hackett, P., Wagner, P. (eds) Hypoxia. Advances in Experimental Medicine and Biology, vol 903. Springer, Boston, MA. https://doi.org/10.1007/978-1-4899-7678-9_5

Download citation

Publish with us

Policies and ethics

Search

Navigation