European Journal of Applied Physiology

, Volume 110, Issue 2, pp 367–377 | Cite as

Exercise with hypoventilation induces lower muscle oxygenation and higher blood lactate concentration: role of hypoxia and hypercapnia

  • Xavier Woorons
  • Nicolas Bourdillon
  • Henri Vandewalle
  • Christine Lamberto
  • Pascal Mollard
  • Jean-Paul Richalet
  • Aurélien Pichon
Original Article


Eight men performed three series of 5-min exercise on a cycle ergometer at 65% of normoxic maximal O2 consumption in four conditions: (1) voluntary hypoventilation (VH) in normoxia (VH0.21), (2) VH in hyperoxia (inducing hypercapnia) (inspired oxygen fraction [FIO2] = 0.29; VH0.29), (3) normal breathing (NB) in hypoxia (FIO2 = 0.157; NB0.157), (4) NB in normoxia (NB0.21). Using near-infrared spectroscopy, changes in concentration of oxy-(Δ[O2Hb]) and deoxyhemoglobin (Δ[HHb]) were measured in the vastus lateralis muscle. Δ[O2Hb − HHb] and Δ[O2Hb + HHb] were calculated and used as oxygenation index and change in regional blood volume, respectively. Earlobe blood samples were taken throughout the exercise. Both VH0.21 and NB0.157 induced a severe and similar hypoxemia (arterial oxygen saturation [SaO2] < 88%) whereas SaO2 remained above 94% and was not different between VH0.29 and NB0.21. Arterialized O2 and CO2 pressures as well as P50 were higher and pH lower in VH0.21 than in NB0.157, and in VH0.29 than in NB0.21. Δ[O2Hb] and Δ[O2Hb − HHb] were lower and Δ[HHb] higher at the end of each series in both VH0.21 and NB0.157 than in NB0.21 and VH0.29. There was no difference in Δ[O2Hb + HHb] between testing conditions. [La] in VH0.21 was greater than both in NB0.21 and VH0.29 but not different from NB0.157. This study demonstrated that exercise with VH induced a lower tissue oxygenation and a higher [La] than exercise with NB. This was caused by a severe arterial O2 desaturation induced by both hypoxic and hypercapnic effects.


Hypoventilation Hypoxemia Hypercapnia Breath holding NIRS Tissue oxygenation 



The authors thank all of the volunteers for time and dedication during this study and gratefully acknowledge the expert technical support provided by Didier Ramier.

Conflict of interest statement

The authors declare that they have no conflict of interest.


  1. Belardinelli R, Barstow TJ, Porszasz J, Wasserman K (1995a) Changes in skeletal muscle oxygenation during incremental exercise measured with near infrared spectroscopy. Eur J Appl Physiol Occup Physiol 70:487–492CrossRefPubMedGoogle Scholar
  2. Belardinelli R, Barstow TJ, Porszasz J, Wasserman K (1995b) Skeletal muscle oxygenation during constant work rate exercise. Med Sci Sports Exerc 27:512–519PubMedGoogle Scholar
  3. Boone J, Koppo K, Barstow TJ, Bouckaert J (2009) Pattern of deoxy[Hb + Mb] during ramp cycle exercise: influence of aerobic fitness status. Eur J Appl Physiol 105:851–859CrossRefPubMedGoogle Scholar
  4. Bourdillon N, Mollard P, Letournel M, Beaudry M, Richalet JP (2009a) Non-invasive evaluation of the capillary recruitment in the human muscle during exercise in hypoxia. Respir Physiol Neurobiol 165:237–244CrossRefPubMedGoogle Scholar
  5. Bourdillon N, Mollard P, Letournel M, Beaudry M, Richalet JP (2009b) Interaction between hypoxia and training on NIRS signal during exercise: contribution of a mathematical model. Respir Physiol Neurobiol 169:50–61CrossRefPubMedGoogle Scholar
  6. Brooks GA (1991) Current concepts in lactate exchange. Med Sci Sports Exerc 23:895–906PubMedGoogle Scholar
  7. Costes F, Barthelemy JC, Feasson L, Busso T, Geyssant A, Denis C (1996) Comparison of muscle near-infrared spectroscopy and femoral blood gases during steady-state exercise in humans. J Appl Physiol 80:1345–1350CrossRefPubMedGoogle Scholar
  8. De Blasi RA, Cope M, Elwell C, Safoue F, Ferrari M (1993) Noninvasive measurement of human forearm oxygen consumption by near infrared spectroscopy. Eur J Appl Physiol Occup Physiol 67:20–25CrossRefPubMedGoogle Scholar
  9. De Blasi RA, Ferrari M, Natali A, Conti G, Mega A, Gasparetto A (1994) Noninvasive measurement of forearm blood flow and oxygen consumption by near-infrared spectroscopy. J Appl Physiol 76:1388–1393PubMedGoogle Scholar
  10. DeLorey DS, Shaw CN, Shoemaker JK, Kowalchuk JM, Paterson DH (2004) The effect of hypoxia on pulmonary O2 uptake, leg blood flow and muscle deoxygenation during single-leg knee-extension exercise. Exp Physiol 89:293–302CrossRefPubMedGoogle Scholar
  11. Dicker SG, Lofthus GK, Thornton NW, Brooks GA (1980) Respiratory and heart rate responses to tethered controlled frequency breathing swimming. Med Sci Sports Exerc 12:20–23PubMedGoogle Scholar
  12. Dufour SP, Ponsot E, Zoll J, Doutreleau S, Lonsdorfer-Wolf E, Geny B, Lampert E, Fluck M, Hoppeler H, Billat V, Mettauer B, Richard R, Lonsdorfer J (2006) Exercise training in normobaric hypoxia in endurance runners. I. Improvement in aerobic performance capacity. J Appl Physiol 100:1238–1248CrossRefPubMedGoogle Scholar
  13. Ehrsam RE, Heigenhauser GJ, Jones NL (1982) Effect of respiratory acidosis on metabolism in exercise. J Appl Physiol 53:63–69PubMedGoogle Scholar
  14. Esaki K, Hamaoka T, Radegran G, Boushel R, Hansen J, Katsumura T, Haga S, Mizuno M (2005) Association between regional quadriceps oxygenation and blood oxygen saturation during normoxic one-legged dynamic knee extension. Eur J Appl Physiol 95:361–370CrossRefPubMedGoogle Scholar
  15. Geiser J, Vogt M, Billeter R, Zuleger C, Belforti F, Hoppeler H (2001) Training high-living low: changes of aerobic performance and muscle structure with training at simulated altitude. Int J Sports Med 22:579–585CrossRefPubMedGoogle Scholar
  16. Graham T, Wilson BA, Sample M, Van Dijk J, Bonen A (1980) The effects of hypercapnia on metabolic responses to progressive exhaustive work. Med Sci Sports Exerc 12:278–284PubMedGoogle Scholar
  17. Graham TE, Barclay JK, Wilson BA (1986) Skeletal muscle lactate release and glycolytic intermediates during hypercapnia. J Appl Physiol 60:568–575PubMedGoogle Scholar
  18. Grassi B, Quaresima V, Marconi C, Ferrari M, Cerretelli P (1999) Blood lactate accumulation and muscle deoxygenation during incremental exercise. J Appl Physiol 87:348–355PubMedGoogle Scholar
  19. Grassi B, Pogliaghi S, Rampichini S, Quaresima V, Ferrari M, Marconi C, Cerretelli P (2003) Muscle oxygenation and pulmonary gas exchange kinetics during cycling exercise on-transitions in humans. J Appl Physiol 95:149–158PubMedGoogle Scholar
  20. Holmer I, Gullstrand L (1980) Physiological responses to swimming with controlled frequency of breathing. Scand J Sports Sci 2:1–6Google Scholar
  21. Hsieh SS, Hermiston RT (1983) The acute effects of controlled breathing swimming on glycolytic parameters. Can J Appl Sport Sci 8:149–154PubMedGoogle Scholar
  22. Im J, Nioka S, Chance B, Rundell KW (2001) Muscle oxygen desaturation is related to whole body \( \dot{V}{\text{O2}} \) during cross-country ski skating. Int J Sports Med 22:356–360Google Scholar
  23. Katz A, Sahlin K (1988) Regulation of lactic acid production during exercise. J Appl Physiol 65:509–518PubMedGoogle Scholar
  24. Legrand R, Ahmaidi S, Moalla W, Chocquet D, Marles A, Prieur F, Mucci P (2005) O2 arterial desaturation in endurance athletes increases muscle deoxygenation. Med Sci Sports Exerc 37:782–788CrossRefPubMedGoogle Scholar
  25. MacDonald MJ, Tarnopolsky MA, Green HE, Hughson RL (1999) Comparison of femoral blood gases and muscle near-infrared spectroscopy at exercise onset in humans. J Appl Physiol 86:687–693PubMedGoogle Scholar
  26. Maehara K, Riley M, Galassetti P, Barstow TJ, Wasserman K (1997) Effect of hypoxia and carbon monoxide on muscle oxygenation during exercise. Am J Respir Crit Care Med 155:229–235PubMedGoogle Scholar
  27. Mancini DM, Bolinger L, Li H, Kendrick K, Chance B, Wilson JR (1994) Validation of near-infrared spectroscopy in humans. J Appl Physiol 77:2740–2747PubMedGoogle Scholar
  28. Meeuwsen T, Hendriksen IJ, Holewijn M (2001) Training-induced increases in sea-level performance are enhanced by acute intermittent hypobaric hypoxia. Eur J Appl Physiol 84:283–290CrossRefPubMedGoogle Scholar
  29. Melissa L, MacDougall JD, Tarnopolsky MA, Cipriano N, Green HJ (1997) Skeletal muscle adaptations to training under normobaric hypoxic versus normoxic conditions. Med Sci Sports Exerc 29:238–243PubMedGoogle Scholar
  30. Millet GP, Roels B, Schmitt L, Woorons X, Richalet JP (2010) Combining hypoxic methods for peak performance. Sports Med 40:1–25CrossRefPubMedGoogle Scholar
  31. Mollard P, Woorons X, Letournel M, Cornolo J, Lamberto C, Beaudry M, Richalet JP (2007) Role of maximal heart rate and arterial O2 saturation on the decrement of \( \dot{V}_{{{\text{O}}_{ 2} { \max }}} \) in moderate acute hypoxia in trained and untrained men. Int J Sports Med 28:186–192Google Scholar
  32. Peltonen JE, Paterson DH, Shoemaker JK, Delorey DS, Dumanoir GR, Petrella RJ, Kowalchuk JM (2009) Cerebral and muscle deoxygenation, hypoxic ventilatory chemosensitivity and cerebrovascular responsiveness during incremental exercise. Respir Physiol Neurobiol 169:24–35CrossRefPubMedGoogle Scholar
  33. Rupp T, Perrey S (2009) Effect of severe hypoxia on prefrontal cortex and muscle oxygenation responses at rest and during exhaustive exercise. Adv Exp Med Biol 645:329–334CrossRefPubMedGoogle Scholar
  34. Sharp RL, Williams DJ, Bevan L (1991) Effects of controlled frequency breathing during exercise on blood gases and acid-base balance. Int J Sports Med 12:62–65CrossRefPubMedGoogle Scholar
  35. Subudhi AW, Dimmen AC, Roach RC (2007) Effects of acute hypoxia on cerebral and muscle oxygenation during incremental exercise. J Appl Physiol 103:177–183CrossRefPubMedGoogle Scholar
  36. Subudhi AW, Lorenz MC, Fulco CS, Roach RC (2008) Cerebrovascular responses to incremental exercise during hypobaric hypoxia: effect of oxygenation on maximal performance. Am J Physiol Heart Circ Physiol 294:H164–H171CrossRefPubMedGoogle Scholar
  37. Terrados N, Melichna J, Sylvén C, Jansson E, Kaijser L (1988) Effects of training at simulated altitude on performance and muscle metabolic capacity in competitive road cyclists. Eur J Appl Physiol Occup Physiol 57:203–209CrossRefPubMedGoogle Scholar
  38. Terrados N, Jansson E, Sylven C, Kaijser L (1990) Is hypoxia a stimulus for synthesis of oxidative enzymes and myoglobin? J Appl Physiol 68:2369–2372PubMedGoogle Scholar
  39. Town GP, Vanness JM (1990) Metabolic responses to controlled frequency breathing in competitive swimmers. Med Sci Sports Exerc 22:112–116PubMedGoogle Scholar
  40. Vogt M, Puntschart A, Geiser J, Zuleger C, Billeter R, Hoppeler H (2001) Molecular adaptations in human skeletal muscle to endurance training under simulated hypoxic conditions. J Appl Physiol 91:173–182PubMedGoogle Scholar
  41. Westerblad H, Allen DG, Lännergren J (2002) Muscle fatigue: lactic acid or inorganic phosphate the major cause? News Physiol Sci 17:17–21PubMedGoogle Scholar
  42. Wilson JR, Mancini DM, McCully K, Ferraro N, Lanoce V, Chance B (1989) Noninvasive detection of skeletal muscle underperfusion with near-infrared spectroscopy in patients with heart failure. Circulation 80:1668–1674PubMedGoogle Scholar
  43. Woorons X, Mollard P, Lamberto C, Letournel M, Richalet JP (2005) Effect of acute hypoxia on maximal exercise in trained and sedentary women. Med Sci Sports Exerc 37:147–154CrossRefPubMedGoogle Scholar
  44. Woorons X, Mollard P, Pichon A, Duvallet A, Richalet JP, Lamberto C (2007) Prolonged expiration down to residual volume leads to severe arterial hypoxemia in athletes during submaximal exercise. Respir Physiol Neurobiol 158:75–82CrossRefPubMedGoogle Scholar
  45. Woorons X, Mollard P, Pichon A, Duvallet A, Richalet J-P, Lamberto C (2008) Effects of a 4-week training with voluntary hypoventilation carried out at low pulmonary volumes. Respir Physiol Neurobiol 160:123–130PubMedGoogle Scholar
  46. Yamamoto Y, Mutoh Y, Kobayashi H, Miyashita M (1987) Effects of reduced frequency breathing on arterial hypoxemia during exercise. Eur J Appl Physiol 56:522–527CrossRefGoogle Scholar
  47. Yamamoto Y, Takei Y, Mutoh Y, Miyashita M (1988) Delayed appearance of blood lactate with reduced frequency breathing during exercise. Eur J Appl Physiol Occup Physiol 57:462–466CrossRefPubMedGoogle Scholar
  48. Zoll J, Ponsot E, Dufour S, Doutreleau S, Ventura-Clapier R, Vogt M, Hoppeler H, Richard R, Fluck M (2006) Exercise training in normobaric hypoxia in endurance runners. III. Muscular adjustments of selected gene transcripts. J Appl Physiol 100:1258–1266CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag 2010

Authors and Affiliations

  • Xavier Woorons
    • 1
    • 3
  • Nicolas Bourdillon
    • 1
  • Henri Vandewalle
    • 2
  • Christine Lamberto
    • 1
    • 2
  • Pascal Mollard
    • 1
  • Jean-Paul Richalet
    • 1
    • 2
  • Aurélien Pichon
    • 1
  1. 1.Université Paris 13Laboratoire “Réponses cellulaires et fonctionnelles à l’hypoxie”, EA 2363 UFR-SMBHBobigny CedexFrance
  2. 2.Hôpital AvicenneBobignyFrance
  3. 3.Association pour la Recherche et la Promotion de l’Entraînement en Hypoventilation (ARPEH)LilleFrance

Personalised recommendations