Skip to main content
SpringerLink
Log in

Limiting factors to oxygen transport on Mount Everest 30 years after: a critique of Paolo Cerretelli’s contribution to the study of altitude physiology

  • Review Article
  • Published:
European Journal of Applied Physiology Aims and scope Submit manuscript

Abstract

In 1976, Paolo Cerretelli published an article entitled “Limiting factors to oxygen transport on Mount Everest” in the Journal of Applied Physiology . The paper demonstrated the role of cardiovascular oxygen transport in limiting maximal oxygen consumption (V̇O2max). In agreement with the predominant view of V̇O2max limitation at that time, however, its results were taken to mean that cardiovascular oxygen transport does not limit V̇O2max at altitude. So it was argued that the limiting factor could be in the periphery, and muscle blood flow was proposed as a possible candidate. Despite this suggestion, the conclusion generated a series of papers on muscle structural characteristics. These experiments demonstrated a loss of muscle oxidative capacity in chronic hypoxia, and thus provided an unambiguous refutation of the then widespread hypothesis that an increased muscle oxidative capacity is needed at altitude to compensate for the lack of oxygen. This analysis is followed by a short account of Cerretelli’s more recent work, with a special attention to the subject of the so-called “lactate paradox”.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Åstrand PO (1952) Experimental studies of physical working capacity in relation to sex and age. Munksgaard, Copenhagen

  • Åstrand PO, Cuddy TE, Saltin B, Stenberg J (1964) Cardiac output during submaximal and maximal work. J Appl Physiol 19:268–274

    CAS  Google Scholar 

  • Bannister RG, Cunningham DJC (1954) The effects on respiration and performance during exercise of adding oxygen to the inspired air. J Physiol (Lond) 125:118–137

    Google Scholar 

  • Bender PR, Groves BM, McCullough RE, McCullough RG, Trad L, Young AJ, Cymerman A, Reeves JT (1989) Decreased exercise muscle lactate release after high altitude acclimatization. J Appl Physiol 67:1456–1462

    Google Scholar 

  • Brooks GA, Wolfel EE, Groves BM, Bender PR, Butterfield GE, Cymerman A, Mazzeo R, Sutton JR (1992) Muscle accounts for glucose disposal but not blood lactate appearance during exercise after acclimatization to 4,300 m. J Appl Physiol 72:2435–2445

    CAS  PubMed  Google Scholar 

  • Brooks GA, Wolfel EE, Butterfield GE, Cymerman A, Roberts AC, Mazzeo R, Reeves JT (1998) Poor relation between arterial [lactate] and leg net release during exercise at 4,300 m altitude. Am J Physiol 275:R1192–R1201

    CAS  PubMed  Google Scholar 

  • Cerretelli P (1959) Esistenza di una permanente stimolazione ipossica del centro respiratorio in individui acclimatati a quote di 5000–7500 m. s.l.m. (Himalaya). Atti Congresso Internazionale di Medicina Aeronautica e Spaziale, Rome, pp 1–8

  • Cerretelli P (1961) Some aspects of the respiratory function in man acclimatized to high altitude (the Himalayas). Int Z Angew Physiol 18:386–392

    CAS  Google Scholar 

  • Cerretelli P (1967) Lactacid O2 debt in chronic and acute hypoxia. In: Margaria R (ed) Exercise at altitude. Excerpta Medica, Amsterdam, pp 58–64

  • Cerretelli P (1976) Limiting factors to oxygen transport on Mount Everest. J Appl Physiol 40:658–667

    Google Scholar 

  • Cerretelli P (1982) O2 breathing at altitude: effects on maximal performance. In: Brendel W, Zinc RA (eds) High altitude physiology and medicine. Springer, Berlin Heidelberg New York pp 9–15

  • Cerretelli P, Margaria R (1961) Maximum oxygen consumption at altitude. Int Z Angew Physiol 18:460–464

    CAS  Google Scholar 

  • Cerretelli P, Bordoni U, Debijadji R, Saracino F (1967) Respiratory and circulatory factors affecting the maximal aerobic power in hypoxia. Arch Fisiol 65:344–357

    CAS  PubMed  Google Scholar 

  • Cerretelli P, Veicsteinas A, Marconi C (1982) Anaerobic metabolism at high altitude: the lactacid mechanism. In: Brendel W, Zinc RA (eds) High altitude physiology and medicine. Springer, Berlin Heidelberg New York, pp 94–102

  • Cerretelli P, Marconi C, Dériaz O, Giezendanner D (1984) After effects of chronic hypoxia on cardiac output and muscle blood flow at rest and exercise. Eur J Appl Physiol 53:92–96

    Google Scholar 

  • Dejours P, Girard F, Labrousse Y, Teillac A (1959) Etude de la régulation de la ventilation de repos chez l’homme en haute altitude. Rev Fr Etud Clin Biol 4:115–127

    CAS  Google Scholar 

  • Dempsey JA, Hanson PG, Henderson KS (1984) Exercise-induced arterial hypoxaemia in healthy human subjects at sea level. J Physiol (Lond) 355:161–175

    Google Scholar 

  • Desplanches D, Hoppeler H, Linossier MT, Denis C, Claassen H, Dormois D, Lacour JR, Geyssant A (1993) Effects of training in normoxia and normobaric hypoxia on human muscle ultrastructure. Pflugers Arch 425:263–267

    CAS  PubMed  Google Scholar 

  • Desplanches D, Hoppeler H, Tüscher L, Mayet MH, Spielvogel H, Ferretti G, Kayser B, Leuenberger M, Grünefelder A, Favier R (1996) Muscle tissue adaptations of high altitude natives to training in chronic hypoxia or acute normoxia. J Appl Physiol 81:1946–1951

    Google Scholar 

  • Dill DB, Edwards HT, Folling A, Oberg SA, Pappenheimer AM, Talbot JH (1931). Adaptations of the organism to changes in oxygen pressure. J Physiol (Lond) 71:47–63

    Google Scholar 

  • Di Prampero PE (1985) Metabolic and circulatory limitations to V̇O2max at the whole animal level. J Exp Biol 115:319–331

    PubMed  Google Scholar 

  • Di Prampero PE, Ferretti G (1990) Factors limiting maximal oxygen consumption in humans. Respir Physiol 80:113–128

    PubMed  Google Scholar 

  • Edwards HT (1936) Lactic acid in rest and work at high altitude. Am J Physiol 116:367–375

    CAS  Google Scholar 

  • Ekblom B (1969) The effect of physical training on oxygen transport system in man. Acta Physiol Scand Suppl 328:1-45

    Google Scholar 

  • Ekblom B, Hermansen L (1968) Cardiac output in athletes. J Appl Physiol 25:619–625

    CAS  PubMed  Google Scholar 

  • Ekblom B, Åstrand PO, Saltin B, Stenberg J, Wallström B (1968) Effect of training on circulatory response to exercise. J Appl Physiol 24:518–528

    CAS  PubMed  Google Scholar 

  • Ekblom B, Goldbarg AN, Gullbring B (1972) Response to exercise after blood loss and reinfusion. J Appl Physiol 33:175–180

    CAS  PubMed  Google Scholar 

  • Ekblom B, Wilson G, Åstrand PO (1976) Central circulation during exercise after venesection and reinfusion of red blood cells. J Appl Physiol 40:379–383

    CAS  PubMed  Google Scholar 

  • Fagraeus L, Karlsson J, Linnarsson D, Saltin B (1973) Oxygen uptake during maximal work at lowered and raised ambient air pressures. Acta Physiol Scand 87:411–421

    CAS  PubMed  Google Scholar 

  • Ferretti G, di Prampero PE (1995) Factors limiting maximal O2 consumption: effects of acute changes in ventilation. Respir Physiol 99:259–271

    Article  CAS  PubMed  Google Scholar 

  • Ferretti G, Moia C, Thomet JM, Kayser B (1997) The decrease of maximal oxygen consumption during hypoxia in man: a mirror image of the oxygen equilibrium curve. J Physiol (Lond) 498:231–237

    Google Scholar 

  • Feyerabend P (1975) Against method. Verso, London

  • Gold AJ, Johnson TF, Costello LC (1973) Effects of altitude stress on mitochondrial function. Am J Physiol 224:946–949

    CAS  PubMed  Google Scholar 

  • Grassi B, Ferretti G, Kayser B, Marzorati M, Colombini A, Marconi C, Cerretelli P (1995) Maximal rate of blood lactate accumulation during exercise at high altitude in humans. J Appl Physiol 79:331–339

    Google Scholar 

  • Grassi B, Marzorati M, Kayser B, Bordini M, Colombini A, Conti M, Marconi C, Cerretelli P (1996) Peak blood lactate and blood lactate vs. workload during acclimatization to 5050 m and in the deacclimatization. J Appl Physiol 80:685–692

    Google Scholar 

  • Grassi B, Mognoni P, Marzorati M, Mattiotti S, Marconi C, Cerretelli P (2001) Power and peak blood lactate at 5050 m with 10 and 30 s “all out” cycling. Acta Physiol Scand 172:189–194

    Article  CAS  PubMed  Google Scholar 

  • Green HJ, Sutton JR, Cymerman A, Young PM, Houston CS (1989) Operation Everest II: Adaptations in human skeletal muscle. J Appl Physiol 66:2454–2461

    Google Scholar 

  • Hochachka PW (1989) The lactate paradox: analysis of the underlying mechanisms. Ann Sports Med 4:184–188

    Google Scholar 

  • Hochachka PW, Stanley C, Merkt J, Sumar-Kalinowski J (1983) Metabolic meaning of elevated levels of oxidative enzymes in high altitude adapted animals: an interpretive hypothesis. Respir Physiol 52:303–313

    Article  CAS  PubMed  Google Scholar 

  • Holmgren A, Åstrand PO (1966) DL and the dimensions and functional capacities of the O2 transport system in humans. J Appl Physiol 21:1463–1470

    CAS  PubMed  Google Scholar 

  • Hoppeler H, Luethi P, Claassen E, Weibel ER, Howald H (1973) The ultrastructure of the normal human skeletal muscle. A morphometric analysis of untrained men, women, and well-trained orienteers. Pflugers Arch 334:217–232

    Google Scholar 

  • Hoppeler H, Howald H, Conley K, Lindstedt SL, Claassen H, Vock P, Weibel ER (1985) Endurance training in humans: aerobic capacity and structure of skeletal muscle. J Appl Physiol 59:320–327

    Google Scholar 

  • Hoppeler H, Kleinert E, Schlegel C, Claassen H, Howald H, Cerretelli P (1990) Muscular exercise at high altitude. II. Morphological adaptation of skeletal muscle to chronic hypoxia. Int J Sports Med 11 [Suppl 1]: S3–S9

    Google Scholar 

  • Howald H, Pette D, Simoneau JA, Uber A, Hoppeler H, Cerretelli P (1990) Muscular exercise at high altitude. III. Effects of chronic hypoxia on muscle enzyme activity. Int J Sports Med 11 [Suppl 1]: S10–S14

    Google Scholar 

  • Kayser B, Hoppeler H, Claassen H, Cerretelli P (1991) Muscle structure and performance capacity of Himalayan Sherpas. J Appl Physiol 70:1938–1942

    Google Scholar 

  • Kayser B, Ferretti G, Grassi B, Binzoni T, Cerretelli P (1993) Maximal lactic capacity at high altitude. Effect of bicarbonate loading. J Appl Physiol 75:1070–1074

    Google Scholar 

  • Kayser B, Hoppeler H, Desplanches D, Broers B, Marconi C, Cerretelli P (1996) Muscle ultrastructure and biochemistry of lowland Tibetans. J Appl Physiol 81:419–425

    CAS  PubMed  Google Scholar 

  • Lundby C, Saltin B, van Hall G (2000) The “lactate paradox”, evidence for a transient change in the course of acclimatization to severe hypoxia in lowlanders. Acta Physiol Scand 170:265–269

    Article  CAS  PubMed  Google Scholar 

  • Margaria R, Cerretelli P, Marchi S, Rossi L (1961) Maximum exercise in oxygen. Int Z Angew Physiol 18:465–467

    CAS  Google Scholar 

  • Margaria R, Cerretelli P, Mangili F (1964) Balance and kinetics of anaerobic energy release durino strenuous exercise in man. J Appl Physiol 19:623–628

    Google Scholar 

  • Margaria R, Mangili F, Cuttica F, Cerretelli P (1965) The kinetics of the oxygen consumption at the onset of muscular exercise in man. Ergonomics 8:49–54

    Google Scholar 

  • Margaria R, Camporesi E, Aghemo P, Sassi G (1972) The effect of O2 breathing on maximal aerobic power. Pflugers Arch 336:225–235

    CAS  PubMed  Google Scholar 

  • McDougall JD, Green HJ, Sutton JR, Coates G, Cymerman A, Young P, Houston CS (1991) Operation Everest II. Structural adaptations in skeletal muscle in response to extreme simulated altitude. Acta Physiol Scand 142:421–427

    CAS  PubMed  Google Scholar 

  • Oelz O, Howald H, di Prampero PE, Hoppeler H, Claassen H, Jenni R, Bühlmann A, Ferretti G, Brückner JC, Veicsteinas A, Gussoni M, Cerretelli P (1986) Physiological profile of world class high altitude climbers. J Appl Physiol 60:1734–1742

    Google Scholar 

  • Poole DC, Mathieu-Costello O (1989) Skeletal muscle capillary geometry: adaptation to chronic hypoxia. Respir Physiol 77:21–30

    Article  CAS  PubMed  Google Scholar 

  • Pugh LGCE, Gill MB, Lahiri S, Milledge JS, Ward MP, West JB (1964) Muscular exercise at great altitudes. J Appl Physiol 19:431–440

    CAS  Google Scholar 

  • Reynafarjee (1962) Myoglobin content and enzymatic activity of muscle and altitude adaptation. J Appl Physiol 17:301–305

    Google Scholar 

  • Rowell LB (1974) Human cardiovascular adjustments to exercise and thermal stress. Physiol Rev 54:75–159

    CAS  PubMed  Google Scholar 

  • Saltin B (1973) Oxygen transport by the circulatory system during exercise in man. In: Keul J (ed) Limiting factors of physical performance. Thieme, Stuttgart, pp 235–252

  • Saltin B, Åstrand PO (1967) Maximal oxygen consumption in athletes. J Appl Physiol 23: 353–358

    CAS  PubMed  Google Scholar 

  • Taylor CR, Weibel ER (eds) (1981) Design of the mammalian respiratory system. Respir Physiol 44:1-164

    CAS  Google Scholar 

  • Van Hall G, Calbet JAL, Sondergaard H, Saltin B (2001) The re-establishment of the normal blood lactate response to exercise in humans after prolonged acclimatization to altitude. J Physiol (Lond) 536:963–975

    Google Scholar 

  • Wagner PD (1993) Algebraic analysis of the determinants of V̇O2max. Respir Physiol 93:221–237

    Article  CAS  PubMed  Google Scholar 

  • West JB (1983) Climbing Mount Everest without oxygen: an analysis of maximal exercise during extreme hypoxia. Respir Physiol 52:265–279

    Article  CAS  PubMed  Google Scholar 

  • West JB (1986) Lactate during exercise at extreme altitude. Fed Proc 45:2953–2957

    CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Laboratorio di Fisiologia Umana, Dipartimento di Scienze Biomediche e Biotecnologie, Università di Brescia, Viale Europa 11, 25100 , Brescia, Italy

    Guido Ferretti

  2. Département de Physiologie, Centre Médical Universitaire, Geneva, Switzerland

    Guido Ferretti

Authors
  1. Guido Ferretti
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Guido Ferretti.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Ferretti, G. Limiting factors to oxygen transport on Mount Everest 30 years after: a critique of Paolo Cerretelli’s contribution to the study of altitude physiology. Eur J Appl Physiol 90, 344–350 (2003). https://doi.org/10.1007/s00421-003-0923-2

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00421-003-0923-2

Keywords

Search

Navigation