Impairment of maximal aerobic power with moderate hypoxia in endurance athletes: Do skeletal muscle mitochondria play a role?

American Journal of Physiology - Regulatory Integrative and Comparative Physiology

Volumn 298, Issue 3, 2010, Pages

  Ponsot, Elodie ^a,b   Dufour, Stéphane P ^a,c   Doutreleau, Stéphane ^a   Lonsdorfer Wolf, Evelyne ^a   Lampert, Eliane ^a   Piquard, François ^a   Geny, Bernard ^a   Mettauer, Bertrand ^d   Ventura Clapier, Renée ^e   Richard, Ruddy ^a  

^a HÔPITAL CIVIL   (France)

^b ÖREBRO UNIVERSITY   (Sweden)

^c UNIVERSITÉ DE STRASBOURG   (France)

^d Association pour le Depistage du Cancer Colorectal en Alsace   (France)

^e UNIVERSITÉ PARIS SACLAY   (France)

Author keywords

Cardiac output; Exercise

Indexed keywords

ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATE; CREATINE; MITOCHONDRIAL CREATINE KINASE;

ADULT; AEROBIC CAPACITY; ANTHROPOMETRY; ARTERIAL OXYGEN TENSION; ARTICLE; ATHLETE; CARDIOVASCULAR RESPONSE; CONTROLLED STUDY; ENDURANCE SPORT; EXERCISE TEST; HEART OUTPUT MEASUREMENT; HUMAN; HUMAN EXPERIMENT; HUMAN TISSUE; HYPOXIA; INSPIRATORY CAPACITY; MALE; MEMBRANE PERMEABILITY; METABOLISM; MITOCHONDRIAL RESPIRATION; MUSCLE BIOPSY; MUSCLE CELL; NORMAL HUMAN; OXYGEN CONSUMPTION; PERFORMANCE MEASUREMENT SYSTEM; PRIORITY JOURNAL; QUALITATIVE ANALYSIS; QUANTITATIVE ANALYSIS; SENSITIVITY ANALYSIS; SKELETAL MUSCLE; TASK PERFORMANCE; TURNOVER TIME; VASTUS LATERALIS MUSCLE; VENOUS OXYGEN TENSION;

EID: 77749308391     PISSN: 03636119     EISSN: 15221490     Source Type: Journal    
DOI: 10.1152/ajpregu.00216.2009     Document Type: Article

References (51)

1. Amann M. Viewpoint: Fatigue mechanisms determining exercise performance: integrative physiology is systems physiology. J Appl Physiol 104: 1543, 2008.
2. Amann M, Proctor LT, Sebranek JJ, Eldridge MW, Pegelow DF, Dempsey JA. Somatosensory feedback from the limbs exerts inhibitory influences on central neural drive during whole body endurance exercise. J Appl Physiol 105: 1714-1724, 2008.
3. Amann M, Proctor LT, Sebranek JJ, Pegelow DF, Dempsey JA. Opioid-mediated muscle afferents inhibit central motor drive and limit peripheral muscle fatigue development in humans. J Physiol 587: 271-283, 2009.
4. Amann M, Romer LM, Pegelow DF, Jacques AJ, Hess CJ, Dempsey JA. Effects of arterial oxygen content on peripheral locomotor muscle fatigue. J Appl Physiol 101: 119-127, 2006.
5. Amann M, Romer LM, Subudhi AW, Pegelow DF, Dempsey JA. Severity of arterial hypoxaemia affects the relative contributions of peripheral muscle fatigue to exercise performance in healthy humans. J Physiol 581: 389-403, 2007.
6. Angermann M, Hoppeler H, Wittwer M, Dapp C, Howald H, Vogt M. Effect of acute hypoxia on maximal oxygen uptake and maximal performance during leg and upper-body exercise in Nordic combined skiers. Int J Sports Med 27: 301-306, 2006.
7. Beaver WL, Wasserman K, Whipp BJ. A new method for detecting anaerobic threshold by gas exchange. J Appl Physiol 60: 2020-2027, 1986.
8. 2max in unacclimatized runners. Int J Sports Med 24: 9-14, 2003.
9. Bourdillon N, Mollard P, Letournel M, Beaudry M, Richalet JP. Non-invasive evaluation of the capillary recruitment in the human muscle during exercise in hypoxia. Respir Physiol Neurobiol 165: 237-244, 2009.
10. Charloux A, Lonsdorfer-Wolf E, Richard R, Lampert E, Oswald-Mammosser M, Mettauer B, Geny B, Lonsdorfer J. A new impedance cardiograph device for the non-invasive evaluation of cardiac output at rest and during exercise: comparison with the "direct" Fick method. Eur J Appl Physiol 82: 313-320, 2000.
11. 2. J Appl Physiol 68: 833-842, 1990.
12. Daussin FN, Zoll J, Ponsot E, Dufour SP, Doutreleau S, Lonsdorfer E, Ventura-Clapier R, Mettauer B, Piquard F, Geny B, Richard R. Training at high exercise intensity promotes qualitative adaptations of mitochondrial function in human skeletal muscle. J Appl Physiol 104: 1436-1441, 2008.
13. di Prampero PE. Factors limiting maximal performance in humans. Eur J Appl Physiol 90: 420-429, 2003.
14. Friedmann B, Frese F, Menold E, Bartsch P. Individual variation in the reduction of heart rate and performance at lactate thresholds in acute normobaric hypoxia. Int J Sports Med 26: 531-536, 2005.
15. Fulco CS, Rock PB, Cymerman A. Maximal and submaximal exercise performance at altitude. Aviat Space Environ Med 69: 793-801, 1998.
16. Gore CJ, Little SC, Hahn AG, Scroop GC, Norton KI, Bourdon 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 Occup Physiol 75: 136-143, 1997.
17. Hanada A, Sander M, González-Alonso J. Human skeletal muscle sympathetic nerve activity, heart rate and limb haemodynamics with reduced blood oxygenation and exercise. J Physiol 551: 635-647, 2003.
18. Hansen J, Sander M, Hald CF, Victor RG, Thomas GD. Metabolic modulation of sympathetic vasoconstriction in human skeletal muscle: role of tissue hypoxia. J Physiol 527: 387-396, 2000.
19. 2 availability. J Appl Physiol 86: 2013-2018, 1999.
20. 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 293: R2046-R2051, 2007.
21. 2 supply and demand limitations. J Appl Physiol 97: 1077-1081, 2004.
22. O2. J Appl Physiol 85: 1457-1463, 1998.
23. 2 uptake in rat skeletal muscles in situ. J Physiol 541: 1003-1012, 2002.
24. Hogan MC, Richardson RS, Haseler LJ. Human muscle performance and PCr hydrolysis with varied inspired oxygen fractions: a 31P-MRS study. J Appl Physiol 86: 1367-1373, 1999.
25. Hoppeler H, Weibel ER. Structural and functional limits for oxygen supply to muscle. Acta Physiol Scand 168: 445-456, 2000.
26. Koistinen P, Takala T, Martikkala V, Leppaluoto J. Aerobic fitness influences the response of maximal oxygen uptake and lactate threshold in acute hypobaric hypoxia. Int J Sports Med 16: 78-81, 1995.
27. Kuznetsov AV, Tiivel T, Sikk P, Kaambre T, Kay L, Daneshrad Z, Rossi A, Kadaja L, Peet N, Seppet E, Saks VA. Striking differences between the kinetics of regulation of respiration by ADP in slow-twitch and fast-twitch muscles in vivo. Eur J Biochem 241: 909-915, 1996.
28. 2max decrement during exposure to acute hypoxia. J Appl Physiol 64: 1486-1492, 1988.
29. 2max: what do we know, and what do we still need to know? J Physiol 586: 25-34, 2008.
30. 2 demand at the microcirculatory level. J Physiol 586: 123-130, 2008.
31. Mollard P, Woorons X, Letournel M, Lamberto C, Favret F, Pichon A, Beaudry M, Richalet JP. Determinants of maximal oxygen uptake in moderate acute hypoxia in endurance athletes. Eur J Appl Physiol 100: 663-673, 2007.
32. Mortensen SP, Dawson EA, Yoshiga CC, Dalsgaard MK, Damsgaard R, Secher NH, González-Alonso J. Limitations to systemic and locomotor limb muscle oxygen delivery and uptake during maximal exercise in humans. J Physiol 566: 273-285, 2005.
33. N'Guessan B, Zoll J, Ribera F, Ponsot E, Lampert E, Ventura-Clapier R, Veksler V, Mettauer B. Evaluation of quantitative and qualitative aspects of mitochondrial function in human skeletal and cardiac muscles. Mol Cell Biochem 256-257: 267-280: 2004.
34. Ponsot E, Dufour SP, Zoll J, Doutrelau S, N'Guessan B, Geny B, Hoppeler H, Lampert E, Mettauer B, Ventura-Clapier R, Richard R. Exercise training in normobaric hypoxia in endurance runners. II. Improvement of mitochondrial properties in skeletal muscle. J Appl Physiol 100: 1249-1257, 2006.
35. Poole DC, Brown MD, Hudlicka, O. Counterpoint: There is not capillary recruitment in active skeletal muscle during exercise. J Appl Physiol 104: 891-893; discussion 893-894, 2008.
36. Richard R, Lonsdorfer-Wolf E, Charloux A, Doutreleau S, Buchheit M, Oswald-Mammosser M, Lampert E, Mettauer B, Geny B, Lonsdorfer J. Non-invasive cardiac output evaluation during a maximal progressive exercise test, using a new impedance cardiograph device. Eur J Appl Physiol 85: 202-207, 2001.
37. 2max during acute hypobaric hypoxia. Med Sci Sports Exerc 30: 869-879, 1998.
38. Romer LM, Haverkamp HC, Amann M, Lovering AT, Pegelow DF, Dempsey JA. Effect of acute severe hypoxia on peripheral fatigue and endurance capacity in healthy humans. Am J Physiol Regul Integr Comp Physiol 292: R598-R606, 2007.
39. Saks VA, Veksler VI, Kuznetsov AV, Kay L, Sikk P, Tiivel T, Tranqui L, Olivares J, Winkler K, Wiedemann F, Kunz WS. Permeabilized cell and skinned fiber techniques in studies of mitochondrial function in vivo. Mol Cell Biochem 184: 81-100, 1998.
40. 2max is limited primarily by cardiac output and locomotor muscle blood flow. J Appl Physiol 100: 744-745, 2006.
41. Stenberg J, Ekblom B, Messin R. Hemodynamic response to work at simulated altitude, 4,000 m. J Appl Physiol 21: 1589-1594, 1966.
42. O2. Am J Physiol Heart Circ Physiol 283: H871-H878, 2002.
43. Veksler VI, Kuznetsov AV, Anflous K, Mateo P, van Deursen J, Wieringa B, Ventura-Clapier R. Muscle creatine kinase-deficient mice. II. Cardiac and skeletal muscles exhibit tissue-specific adaptation of the mitochondrial function. J Biol Chem 270: 19921-19929, 1995.
44. Veksler VI, Kuznetsov AV, Sharov VG, Kapelko VI, Saks VA. Mitochondrial respiratory parameters in cardiac tissue: a novel method of assessment by using saponin-skinned fibers. Biochim Biophys Acta 892: 191-196, 1987.
45. Ventura-Clapier R, Kuznetsov A, Veksler V, Boehm E, Anflous K. Functional coupling of creatine kinases in muscles: species and tissue specificity. Mol Cell Biochem 184: 231-247, 1998.
46. Wagner PD, Gale GE, Moon RE, Torre-Bueno JR, Stolp BW, Saltzman HA. Pulmonary gas exchange in humans exercising at sea level and simulated altitude. J Appl Physiol 61: 260-270, 1986.
47. Walsh B, Tonkonogi M, Sahlin K. Effect of endurance training on oxidative and antioxidative function in human permeabilized muscle fibres. Pflügers Arch 442: 420-425, 2001.
48. Wasserman K, Hansen JE, Sue DY, Whipp BJ, Casaburi R. Principles of Exercise Testing and Interpretation. Baltimore, MD: Williams & Wilkins, 1994.
49. Wilson DF, Erecinska M, Drown C, Silver IA. The oxygen dependence of cellular energy metabolism. Arch Biochem Biophys 195: 485-493, 1979.
50. 2 uptake during submaximal exercise with β-adrenergic blockade at 4,300 m. J Appl Physiol 85: 1092-1102, 1998.
51. Zoll J, Sanchez H, N'Guessan B, Ribera F, Lampert E, Bigard X, Serrurier B, Fortin D, Geny B, Veksler V, Ventura-Clapier R, Mettauer B. Physical activity changes the regulation of mitochondrial respiration in human skeletal muscle. J Physiol 543: 191-200, 2002.