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• W2122664887 abstract "POINT-COUNTERPOINTPoint: Positive effects of intermittent hypoxia (live high:train low) on exercise performance are mediated primarily by augmented red cell volumeBenjamin D. Levine, and James Stray-GundersenBenjamin D. Levine, and James Stray-GundersenPublished Online:01 Nov 2005https://doi.org/10.1152/japplphysiol.00877.2005MoreSectionsPDF (73 KB)Download PDF ToolsExport citationAdd to favoritesGet permissionsTrack citations ShareShare onFacebookTwitterLinkedInEmailWeChat For nearly half a century, athletes have used “altitude training” to enhance sea level performance. Both altitude acclimatization and hypoxic exercise have been proposed as mediating this enhancement. However, hypoxic exercise impairs training quality (18, 19) and, in the absence of acclimatization, does not augment performance (30). The “living high-training low” model was therefore developed (19) and demonstrated to be effective for athletes of all abilities (4, 18, 26).So which of the myriad aspects of altitude acclimatization (16) might be responsible for improving performance of athletes at sea level? Rigorous use of accepted scientific principles must be applied to determine cause and effect. We would like to propose “Levine and Stray-Gundersen’s Postulates” (a modification of Nobel laureate Robert Koch “Koch’s Postulates”) to determine the etiology of performance enhancement with altitude exposure, as follows.First, the response (improvement in V̇o2 max and performance) must be present when the mechanism (increase in erythrocyte volume) is present. Corollary: when no increase in erythrocyte volume is present, there is no increase in V̇o2 max and no improvement in aerobic performance.Second, the mechanism must be isolatable and demonstrated to have an unequivocal relationship to altitude exposure and improved performance.Third, when the mechanism is manipulated independently (without altitude exposure), then the same improvement in physiological parameters and performance must occur. Corollary: in the presence of altitude exposure, when the specific mechanism is inhibited, then the outcome is prevented.In the original publication of the “live high-train low” model, we demonstrated clearly that exposure for >20 h/day to 2,500 m altitude for 4 wk led to an increase in erythrocyte volume, an increase in V̇o2 max, and improved performance in an event (5,000 m time trial) that is dependent on high rates of oxygen transport (18). In contrast, a control group exposed to identical training, but living at sea level, improved neither erythrocyte volume, V̇o2 max, nor performance. Although we have consistently emphasized that the “low-altitude training” component of the high-low model is essential to allow high rates of oxygen flux, which maintain the muscle structure and function required for success of an endurance athlete (27), we will focus exclusively on the “altitude acclimatization” component for the purposes of this debate.To further define the mechanisms underlying the improvement in performance with altitude training, all the altitude-living athletes from our previous studies (18, 28) were divided into two groups based on only one criterion: those who improved their race time by more than the group mean (“responders”) and those that got worse (“nonresponders”; Ref. 4). There were no differences between these groups with respect to numerous physiological variables that might influence acclimatization to altitude (4).Rather, the key distinguishing feature was that the responders had a greater increase in erythropoietin concentration with acute altitude exposure, which remained elevated for a more prolonged period of time. Indeed, the erythropoietin increase in the responders after 2 wk at altitude was equivalent to the peak response in the nonresponders, in whom erythropoietin had returned to baseline. This difference in erythropoietin response patterns was clearly physiologically significant and not a chance occurrence; the responders had an increase in erythrocyte volume and increased V̇o2 max, whereas the nonresponders did not. Furthermore, the increase in V̇o2 max was exactly what would be predicted from change in blood volume and hemoglobin concentration (31): predicted increase 248 ml/min − actual increase 245 ml/min(4). This derivation model was confirmed prospectively in another population (4, 26).Although our results have led us to focus on the erythropoietic pathway, this was not an exclusive hypothesis at the beginning of our experiments. For example, in large numbers of runners (n > 100), running economy never changed (18, 19); anaerobic capacity never changed (16, 18, 19); muscle biopsies did not increase in buffer capacity or oxidative enzymes (27). Thus the weight of evidence has led us inexorably toward the primary effect of altitude acclimatization, given an adequate exposure, on sea level performance in competitive athletes being on the erythropoietic pathways.But is there other evidence that altitude exposure is erythropoietic? Indeed, this evidence is extensive and quite compelling, particularly when the exposure is high enough and sustained for a long enough period of time. For example, cross-sectional studies in North (33) and South America (12, 20, 23) have demonstrated that there is an elevated red cell mass in natives of high altitude that is proportional to the altitude of residence and oxyhemoglobin saturation (12, 33). When sea level natives ascend acutely to altitude, there is a large increase in iron turnover that begins immediately on exposure (6, 11, 20). Most convincingly, direct examination of the bone marrow during acute high-altitude exposure has documented a dramatic increase in erythroid cell lines, from 20.0% at sea level to 40.5% after 1 mo at 4,300 m (11, 20). Accelerated erythropoiesis has also been confirmed in elite athletes at more moderate altitudes (7, 10, 24, 32). Thus despite rare exceptions (8), the evidence from multiple research groups has confirmed that moderate altitude exposure for nearly 24 h/day increases the red cell mass even in elite athletes.But do lesser durations of exposure also increase the red cell mass? Clearly very short duration exposures of even extreme altitude are not sufficient to accomplish this goal (14). However, 12-16 h/day of normobaric hypoxia for 3 (3) or 4 wk (15, 21, 22) closely replicates the results observed in the field studies with an increase in both hemoglobin mass and V̇o2 max. In contrast, our opponents, using only 8–10 h/day of normobaric hypoxia (2,500–3,000 m) for 10–21 days failed to demonstrate an increase in hemoblobin mass or V̇o2 max (1). We would submit that this exposure is insufficient to stimulate a sustained accelerated erythropoiesis—the “dose” of altitude is simply too low (17).Recent advances in the basic science of hypoxia response pathways may explain this apparent “threshold” phenomenon (25). For example, the principal transcriptional activator of gene expression in hypoxic cells is hypoxia-inducible factor-1α (HIF-1α). Under well-oxygenated conditions, HIF-1α is hydroxylated and binds to the Von Hipple-Lindau factor, which targets the entire complex for ubiquitin degradation. This process is so rapid, that in the presence of oxygen, HIF-1α has one of the shortest half-lives of any known protein (13). Moreover, when altitude natives or sojourners return to sea level, there is a suppression of erythropoietin (4, 6, 18, 20), a reduction in iron turnover and erythroid cell lines (11, 20), and a marked decrease in red cell survival time (20), termed “neocytolysis.” Both the rapid destruction of HIF-1α and neocytolysis may compromise the ability of short duration (<12–16 h/day) hypoxia to increase the red cell mass.So what about the last of “Koch’s postulates”? Can the red cell mass be manipulated independently from altitude exposure and obtain the same effect? Clearly this is so. For example, increasing the red cell mass directly by blood doping or indirectly by injecting erythropoietin improves V̇o2 max, laboratory-based performance (2, 5), and success in international competition (29). Furthermore, low-dose erythropoietin injection increases the erythrocyte volume to a degree that is virtually identical to that acquired by 4 wk of altitude exposure to 2,500 m, data that have been obtained in collaboration with our opponents (17). Finally, when the increase in erythrocyte volume at altitude is inhibited in athletes by iron deficiency (9, 19) or infection (27), V̇o2 max does not increase and performance is not augmented.In summary, the evidence demonstrates that given adequate exposure (living high enough, long enough, for enough hours per day), altitude is clearly erythropoietic even in elite athletes and leads to an increase in erythrocyte volume/red cell mass, V̇o2 max, and performance in endurance sport. To our knowledge, there are no other effects of altitude acclimatization (including all the alternatives proposed by our opponents) that can be manipulated independently and demonstrated to improve athletic performance over a sustained period of time. The magnitude of the response at altitude is qualitatively and quantitatively similar to that induced by isolated manipulation of the red cell mass (low-dose Epo injection), and the outcome is prevented if the erythropoietic process is impaired by iron deficiency or infection. Thus we would contend that all of Koch’s Postulates have been fulfilled for determining a cause-and-effect relationship between erythropoiesis and success of altitude training.REFERENCES1 Ashenden MJ, Gore CJ, Dobson GP, and Hahn AG. “Live high, train low” does not change the total haemoglobin mass of male endurance athletes sleeping at a simulated altitude of 3000 m for 23 nights. 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J Clin Invest 47: 1627–1639, 1968.Crossref | ISI | Google Scholar Download PDF Previous Back to Top Next FiguresReferencesRelatedInformationCited ByCross-adaptation between heat and hypoxia: mechanistic insights into aerobic exercise performanceAlexandros Sotiridis, Tadej Debevec, Nickos Geladas, and Igor B. Mekjavic19 October 2022 | American Journal of Physiology-Regulatory, Integrative and Comparative Physiology, Vol. 323, No. 5Training at moderate altitude improves submaximal but not maximal performance-related parameters in elite rowers14 October 2022 | Frontiers in Physiology, Vol. 13Single Leg Cycling Offsets Reduced Muscle Oxygenation in Hypoxic Environments26 July 2022 | International Journal of Environmental Research and Public Health, Vol. 19, No. 15Practical Application of Altitude/Hypoxic Training for Olympic Medal Performance: The Team USA Experience14 June 2022 | Journal of Science in Sport and Exercise, Vol. 98High Intraindividual Variability in the Response of Serum Erythropoietin to Multiple Simulated Altitude ExposuresHigh Altitude Medicine & Biology, Vol. 23, No. 1A Comparative Study of Hematological Parameters of Endurance Runners at Guna Athletics Sport Club (3100 Meters above Sea Level) and Ethiopian Youth Sport Academy (2400 Meters above Sea Level), EthiopiaJournal of Sports Medicine, Vol. 2021ResponseExercise and Sport Sciences Reviews, Vol. 49, No. 3Heat Versus Altitude Training for Endurance Performance at Sea Level12 October 2020 | Exercise and Sport Sciences Reviews, Vol. 49, No. 1Intermittent hypoxia modulates redox homeostasis, lipid metabolism associated inflammatory processes and redox post-translational modifications: Benefits at high altitude13 May 2020 | Scientific Reports, Vol. 10, No. 1Blood Volumes Following Preseason Heat Versus Altitude: A Case Study of Australian FootballersInternational Journal of Sports Physiology and Performance, Vol. 15, No. 4Hypoxic Training Is Beneficial in Elite AthletesMedicine & Science in Sports & Exercise, Vol. 52, No. 2Intensified Training Supersedes the Impact of Heat and/or Altitude for Increasing Performance in Elite Rugby Union PlayersInternational Journal of Sports Physiology and PerformanceNo ergogenic effects of a 10-day combined heat and hypoxic acclimation on aerobic performance in normoxic thermoneutral or hot conditions25 September 2019 | European Journal of Applied Physiology, Vol. 119, No. 11-12Effect of a 16-Day Altitude Training Camp on 3,000-m Steeplechase Running Energetics and Biomechanics: A Case Study22 November 2019 | Frontiers in Sports and Active Living, Vol. 1Contemporary Periodization of Altitude Training for Elite Endurance Athletes: A Narrative Review26 August 2019 | Sports Medicine, Vol. 49, No. 11Special Environments: Altitude and HeatInternational Journal of Sport Nutrition and Exercise Metabolism, Vol. 29, No. 2Relationship between total hemoglobin mass and competitive performance in endurance athletesThe Journal of Sports Medicine and Physical Fitness, Vol. 59, No. 3Comprehensive overview of hemoglobin mass and blood volume in elite athletes across a wide range of different sporting disciplinesThe Journal of Sports Medicine and Physical Fitness, Vol. 59, No. 2Altitude training in endurance running: perceptions of elite athletes and support staff22 June 2018 | Journal of Sports Sciences, Vol. 37, No. 2Adaptations in muscle oxidative capacity, fiber size, and oxygen supply capacity after repeated-sprint training in hypoxia combined with chronic hypoxic exposureS. van der Zwaard, F. 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Chapman, Abigail S. Laymon Stickford, Carsten Lundby, and Benjamin D. Levine1 April 2014 | Journal of Applied Physiology, Vol. 116, No. 7Pro: Live High+Train Low Does Improve Sea Level Performance Beyond that Achieved with the Equivalent Living and Training at Sea LevelHigh Altitude Medicine & Biology, Vol. 14, No. 4Rebuttal to the Con StatementHigh Altitude Medicine & Biology, Vol. 14, No. 4Ten days of simulated live high:train low altitude training increases Hbmass in elite water polo players26 November 2013 | British Journal of Sports Medicine, Vol. 47, No. Suppl 1Relationship between changes in haemoglobin mass and maximal oxygen uptake after hypoxic exposure26 November 2013 | British Journal of Sports Medicine, Vol. 47, No. Suppl 1Prevailing evidence contradicts the notion of a “normobaric oxygen paradox”31 March 2012 | European Journal of Applied Physiology, Vol. 112, No. 12Vitamin C Supplementation Does not Improve Hypoxia-Induced ErythropoiesisHigh Altitude Medicine & Biology, Vol. 13, No. 4Genetic and Environmental Influences on Gas Exchange1 October 2012Influence of altitude training modality on performance and total haemoglobin mass in elite swimmers11 January 2012 | European Journal of Applied Physiology, Vol. 112, No. 9Four weeks of normobaric “live high-train low” do not alter muscular or systemic capacity for maintaining pH and K+ homeostasis during intense exerciseN. B. Nordsborg, C. Siebenmann, R. A. Jacobs, P. Rasmussen, V. Diaz, P. Robach, and C. Lundby15 June 2012 | Journal of Applied Physiology, Vol. 112, No. 12Is live high-train low altitude training relevant for elite athletes with already high total hemoglobin mass?22 May 2012 | Scandinavian Journal of Medicine & Science in Sports, Vol. 22, No. 3Short intermittent hypoxic exposures augment ventilation but do not alter regional cerebral and muscle oxygenation during hypoxic exerciseRespiratory Physiology & Neurobiology, Vol. 181, No. 2Effects of high altitude training on exercise capacity: fact or myth26 November 2010 | Sleep and Breathing, Vol. 16, No. 1The Effect of a Sleep High–Train Low Regimen on the Finger Cold-Induced Vasodilation ResponseHigh Altitude Medicine & Biology, Vol. 13, No. 1“Live high–train low” using normobaric hypoxia: a double-blinded, placebo-controlled studyChristoph Siebenmann, Paul Robach, Robert A. 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Truijens, Ferran A. Rodríguez, Nathan E. Townsend, James Stray-Gundersen, Christopher J. Gore, and Benjamin D. Levine1 February 2008 | Journal of Applied Physiology, Vol. 104, No. 2The biochemistry of drugs and doping methods used to enhance aerobic sport performance1 February 2008 | Essays in Biochemistry, Vol. 44Pre-acclimation to exercise in normobaric hypoxiaEuropean Journal of Sport Science, Vol. 8, No. 1Physiological Responses to Exercise at AltitudeSports Medicine, Vol. 38, No. 1Performance of runners and swimmers after four weeks of intermittent hypobaric hypoxic exposure plus sea level trainingFerran A. Rodríguez, Martin J. Truijens, Nathan E. Townsend, James Stray-Gundersen, Christopher J. Gore, and Benjamin D. Levine1 November 2007 | Journal of Applied Physiology, Vol. 103, No. 5GXT Responses in Altitude-Acclimatized Cyclists during Sea-Level SimulationMedicine & Science in Sports & Exercise, Vol. 39, No. 10The effects of nightly normobaric hypoxia and high intensity training under intermittent normobaric hypoxia on running economy and hemoglobin massMituso Neya, Taisuke Enoki, Yasuko Kumai, Takayuki Sugoh, and Takashi Kawahara1 September 2007 | Journal of Applied Physiology, Vol. 103, No. 3Live High + Train Low: Thinking in Terms of an Optimal Hypoxic DoseInternational Journal of Sports Physiology and Performance, Vol. 2, No. 3Variability of Erythropoietin Response to Sleeping at Simulated Altitude: A Cycling Case StudyInternational Journal of Sports Physiology and Performance, Vol. 2, No. 3Introduction to Altitude/Hypoxic Training SymposiumMedicine & Science in Sports & Exercise, Vol. 39, No. 9Nonhematological Mechanisms of Improved Sea-Level Performance after Hypoxic ExposureMedicine & Science in Sports & Exercise, Vol. 39, No. 9Physical Fitness and Hematological Changes During Acclimatization to Moderate Altitude: A Retrospective StudyHigh Altitude Medicine & Biology, Vol. 8, No. 3Unchanged Anaerobic and Aerobic Performance after Short-Term Intermittent HypoxiaMedicine & Science in Sports & Exercise, Vol. 39, No. 5References3 January 2013Determining an erythropoietin threshold is not sufficient for accelerating erythrocyte production13 December 2006 | European Journal of Applied Physiology, Vol. 99, No. 3Determining an erythropoietin threshold is not sufficient for accelerating erythrocyte production by Julien V. Brugniaux and Aurélien Pichon13 December 2006 | European Journal of Applied Physiology, Vol. 99, No. 3Increased serum erythropoietin but not red cell production after 4 wk of intermittent hypobaric hypoxia (4,000–5,500 m)Christopher J. Gore, Ferran A. Rodríguez, Martin J. Truijens, Nathan E. Townsend, James Stray-Gundersen, and Benjamin D. Levine1 November 2006 | Journal of Applied Physiology, Vol. 101, No. 5Should artificial high altitude environments be considered doping?Scandinavian Journal of Medicine and Science in Sports, Vol. 16, No. 5Physiological characteristics of the best Eritrean runners—exceptional running economyApplied Physiology, Nutrition, and Metabolism, Vol. 31, No. 5Running performance after adaptation to acutely intermittent hypoxiaEuropean Journal of Sport Science, Vol. 6, No. 3Living high–training low: effect on erythropoiesis and maximal aerobic performance in elite Nordic skiers20 June 2006 | European Journal of Applied Physiology, Vol. 97, No. 6Influence of “living high–training low” on aerobic performance and economy of work in elite athletes13 June 2006 | European Journal of Applied Physiology, Vol. 97, No. 5Live high-train low for 24 days increases hemoglobin mass and red cell volume in elite endurance athletesJon Peter Wehrlin, Peter Zuest, Jostein Hallén, and Bernard Marti1 June 2006 | Journal of Applied Physiology, Vol. 100, No. 6Comment on Point:Counterpoint “Positive effects of intermittent hypoxia (live high:train low) on exercise performance are/are not mediated primarily by augmented red cell volume”José A L Calbet, Robert Boushel, and Carsten Lundby1 February 2006 | Journal of Applied Physiology, Vol. 100, No. 2Commentary on Point-CounterpointStefan Keslacy1 January 2006 | Journal of Applied Physiology, Vol. 100, No. 1Comments on Point:Counterpoint “Positive effects of intermittent hypoxia (live high:train low) on exercise performance are/are not mediated primarily by augmented red cell volume”Timothy David Noakes1 December 2005 | Journal of Applied Physiology, Vol. 99, No. 6 More from this issue > Volume 99Issue 5November 2005Pages 2053-2055 Copyright & PermissionsCopyright © 2005 the American Physiological Societyhttps://doi.org/10.1152/japplphysiol.00877.2005PubMed16227463History Published online 1 November 2005 Published in print 1 November 2005 Metrics" @default.
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