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Re: Measuring exercise performance

Dear Editor

I very much enjoyed reading the Review article [1] by Professor Noakes and the letter [2] in the same edition of the BJSM July 2008.

As he rightly states measurement of VO₂max has several limitations in determining an athlete's potential. He also pointed out in the letter that research has shown that 'the rating of perceived exertion (RPE) rises as a linear function of the duration of exercise that remains', and extrapolation from this 'that humans have an exquisite capacity to predict accurately the duration of exercise they will be able to sustain at any exercise intensity'.

Would it therefore not be possible to determine an athlete's optimal running distance by getting them to run on a treadmill for 10 minutes and asking them to run as fast as possible for imagined distances of 5k, 10k, 40k, etc?

References

1. NOAKES TD. Testing for maximum oxygen consumption has produced a brainless model of human exercise performance. Br J Sports Med 2008; 42:551-555

2. NOAKES TD. Rating of perceived exertion as a predictor of the duration of exercise that remains until exhaustion. Br J Sports Med 2008; 42:623-624

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Re: The Hill model does exist

To the Editor: In my opinion the negative influence of Nobel Laureate AV Hill on subsequent generations of exercise physiologists is not about the plateau in VO2 or other physiological concepts criticized by Professor Tim Noakes in his article. Hill’s influence is much deeper than that. It is about the fundamental assumption over which the current physiological model of exercise tolerance has been built over the years: In well-motivated subjects used to physical exertion, exercise is terminated because the subject, due to muscle fatigue, is no longer able to produce the force/power required by the task.

Hill thought that muscle fatigue during intense whole-body exercise in athletic subjects was caused by “oxygen want and lactic acid in their muscles” (Gandevia, 2000). As correctly pointed out by Dr. Mark Burnley in his letters, since then many more central and peripheral mechanisms of muscle fatigue have been identified (McKenna and Hargreaves, 2008), and some of the conclusions reached by Hill in the early XX century have now been proven wrong. However, the main assumption of Hill’s model has remained unchallenged for many years, and the vast majority of exercise physiologists accept as true the proposition that athletic subjects stop exercise not because of motivational factors but because of muscle fatigue (Sejersted and Sjøgaard, 2000; Allen et al., 2008; Jones et al., 2008). The problem with this fundamental assumption is that it has never been proven valid. Furthermore, available scientific evidence suggests it is very likely to be invalid.

Indeed, in the literature there is plenty of evidence (Millet and Lepers, 2004) suggesting that after exhaustion, despite significant muscle fatigue, maximal voluntary force produced with the locomotor muscles is well above the force required by even maximal intensity aerobic exercise (less than 20% of resting MVC) (Löllgen et al., 1980). These findings do not provide conclusive evidence against Hill’s basic assumption because MVC tests are usually of isolated muscles in isometric conditions, and performed few minutes after exhaustive exercise. Therefore, these MVC tests are not specific to dynamic whole-body exercise, and some recovery of muscle fatigue may occur. However, scientists interested in muscle fatigue of isolated muscles have measured MVC in a specific manner immediately after terminating prolonged isometric contractions to exhaustion, and found very similar results: MVC at exhaustion (about 80% of resting MVC) is well above the force required by the submaximal task (5-30% of resting MVC). Therefore, these scientists have now concluded that the duration of sustained tasks is not necessarily limited by fatigue of the principal muscles (Enoka and Duchateau, 2008). The same may be true for even very high-intensity endurance exercise.

For how long can traditional exercise physiologists live with this elephant in their room? Given that their model of exercise tolerance is based on the assumption that central and/or peripheral muscle fatigue causes exhaustion, why nobody has checked, in more than 80 years, whether this assumption is true or not?

As Richard P. Feynman would certainly agree, the mere presence of muscle fatigue and/or its mechanisms (e.g. falling [PCr] and pH and rising [Pi] and [ADP]) does not prove that muscle fatigue directly limits time to exhaustion during incremental or constant-workload exercise tests.

Samuele M Marcora

REFERENCES

Allen DG, Lamb GD, Westerblad H. Skeletal muscle fatigue: cellular mechanisms. Physiol Rev. 2008; 88: 287-332

Enoka RM, Duchateau J. Muscle fatigue: what, why and how it influences muscle function. J Physiol. 2008; 586: 11-23.

Gandevia SC. Spinal and supraspinal factors in human muscle fatigue. Physiol Rev. 2001; 81: 1725-89.

Jones AM, Wilkerson DP, DiMenna F, Fulford J, Poole DC. Muscle metabolic responses to exercise above and below the "critical power" assessed using 31P-MRS. Am J Physiol Regul Integr Comp Physiol. 2008; 294:R585-93.

LĂśllgen H, Graham T, Sjogaard G. Muscle metabolites, force, and perceived exertion bicycling at varying pedal rates. Med Sci Sports Exerc. 1980; 12: 345-51.

McKenna MJ, Hargreaves M. Resolving fatigue mechanisms determining exercise performance: integrative physiology at its finest! J Appl Physiol. 2008; 104: 286-7.

Millet GY, Lepers R. Alterations of neuromuscular function after prolonged running, cycling and skiing exercises. Sports Med. 2004; 34: 105-16.

Sejersted OM, Sj�gaard G. Dynamics and consequences of potassium shifts in skeletal muscle and heart during exercise. Physiol Rev. 2000; 80: 1411-81.

Send letter to journal:
Re: On "misleading interpretations": the "Hill model" does not exist

Dear Editor:

I now better appreciate Prof. Noakes' reasons for using the words he used following his response to my eletter posted on the BJSM Blog, and consider the issue of "data exclusion" settled. However, I would like to make the following points to clarify my position and respond to Noakes' interpretation of the physiology:

1. I do not consider myself "wedded to the Hill model" because the "Hill model" as presented by Noakes bears no relationship to my understanding of the physiological response to exercise. It is my contention that the "Hill model" is an erroneous caricature of the physiology of exercise that Noakes uses as a straw man in contrast to his central governor model. Few scientists are likely to defend the view that cardiac output and VO₂ must always be identical at exhaustion, for the evidence against this proposition is overwhelming! In short, the “Hill model” is not a contemporary model of exercise physiology, it is a vehicle invented by Noakes.

2. “Oxygen consumption" or, more correctly, pulmonary oxygen uptake, is not a "surrogate measure of cardiac output and the state of muscle oxygenation". To claim this indicates a misunderstanding or misrepresentation of basic physiological measurements. Pulmonary VO₂ is useful because in both the non-steady state and the steady state it closely reflects muscle VO₂, which itself reflects energetic events occurring in the cell. If one accepts that the rate of energy transfer is an important consideration during exercise, then measuring the most quantitatively significant energy transfer process is worthwhile. Furthermore, the phrase “state of muscle oxygenation” is hopelessly vague. Does Noakes mean “muscle O₂ extraction”, “arterio-venous oxygen difference” or “intracellular [or mitochondrial] PO₂”? The first two measures are difficult to make, whilst the latter is currently impossible to make during whole-body exercise.

3. I do not “believe” that exhaustion occurs before VO₂max is attained during "extreme" exercise, it is an experimental fact: exercise is terminated whilst VO₂ is still rising in a futile attempt to meet the energetic demand.[1] Exercise under these conditions is terminated because the subject is no longer able to sustain the power requirements of the task (in my experience not because the subject is unwilling), but this says little of the mechanism. Classic works on the aetiology of muscle fatigue acknowledge that fatigue processes occur at a number of sites within the neuromuscular system,[2,3] and I certainly embrace this. Exhaustion at these “extreme” work rates is attended by falling [PCr] and pH and rising [Pi] and [ADP], amongst other derangements known to cause a fall in tension produced by the myocyte.[4] However, measurements of these processes in whole-body exercise are presently too spatially or temporally crude to be definitive – but that is certainly not a reason to reject the periphery as a plausible or even pivotal contributor to task failure (exhaustion). Note also that the identification of metabolites involved in substrate-level phosphorylation does not imply that the conditions within the cell are “anaerobic”: the concentrations of these metabolites will change progressively during exercise above the so-called “critical power”[5] irrespective of cellular PO₂.[6]

4. Noakes argues that the “simulaneous [sic] measurement of muscle activation” is required to test the alternate (central governor) theory “that maximal exercise always terminates before there is 100% activation of all the available motor units in the exercising limbs”. However, this is impossible to verify with current technology. Even if electromyographic recordings are taken from the surface of a large number of muscles and normalised to some measure of maximal voluntary muscle function (such as an MVC), this will not provide an estimate of the fractional number of motor units that are active. The EMG signal is determined, in part, by the number of active muscle fibres in the region of interrogation, their firing frequency, and the conductivity of the tissues between the fibres and the electrodes, not simply by the number of active motor units. A method of determining the total number of active motor units during whole-body exercise would be very useful but does not currently exist.

The processes leading to additional motor unit recruitment during rhythmic whole-body exercise are far from understood. However, it is logical that in conditions where the rate of O₂ delivery is maximal (i.e., when cardiac output is maximal) the recruitment of additional motor units will lead to worsening metabolic conditions within the exercising muscles, as those newly recruited fibres will also extract O₂ from the microvasculature. The consequent fall in microvascular PO₂ will make the appropriate matching of O₂ demand and supply (essential for the continuance of exercise) increasingly difficult. Additional motor unit recruitment is thus likely to yield diminishing returns in terms of sustaining the required power output. In this scenario, task failure will occur before all motor units are activated even in the absence of a “governor”.

In summary, Prof. Noakes’ representation of the physiology of exercise could be charitably described as inaccurate. The “Hill model” is not one that any physiologist is “wedded” to because it does not exist. Therein lay the “misleading interpretations” to which I referred in my first letter. One final point needs to be made:

If the “absence of any such catastrophe [myocardial ischaemia or rigor during exercise] suggests the presence of an anticipatory, complex, regulatory control system”[7], then surely the presence of myocardial ischaemia during exercise[8] suggests the absence of an anticipatory, complex regulatory control system? How long can the central governor theory survive with this elephant in the room?

“It does not make any difference how beautiful your guess is. It does not make any difference how smart you are, who made the guess, or what his name is - if it disagrees with experiment it’s wrong. That’s all there is to it.” Richard P. Feynman.

References

1. Hill DW, Poole DC, Stevens JC. The relationship between power and the time to achieve VO₂max. Med Sci Sports Exerc. 2002;34:709-714

2. Bigland-Ritchie B, Woods JJ. Changes in muscle contractile properties and neural control during human muscular fatigue. Muscle Nerve. 1984;7:691-699.

3. Gandevia SC. Spinal and supraspinal factors in human muscle fatigue. Physiol Rev. 2001;81:1725-1789.

4. Fitts RH. The cross-bridge cycle and skeletal muscle fatigue. J Appl Physiol. 2008;104:551-558.

5. Jones AM, Wilkerson DP, DiMenna F, Fulford J, Poole DC. Muscle metabolic responses to exercise above and below the “critical power” assessed using 31-PMRS. Am J Physiol Regul Integr Comp Physiol. 2008;294:R585-R593.

6. Richardson RS, Newcomer SC, Noyszewski EA. Skeletal muscle intracellular PO₂ assessed by myoglobin desaturation: response to graded exercise. J Appl Physiol. 2001;91:2679-2685.

7. Noakes TD. Peer review/fair review: How did A.V. Hill understand the VO₂max and the “plateau phenomenon”? Still no clarity? Brit J Sports Med, in press. DOI: 10.1136/bjsm.2008.046771.

8. Bogaty P, Poirier P, Boyer L, Jobin J, Dagenais GR. What induces the warm-up ischemia/angina phenomenon: exercise or myocardial ischemia? Circulation. 2003;107:1858-1863.

Send letter to journal:
Re: There is a “biologically plausible explanation” for lower supramaximal oxygen uptake

Dear Editor

I read with concern the recent review of Noakes[1] accepted for publication in the journal. Noakes suggests that there is no “biologically plausible explanation” for the observation of lower oxygen uptake (VO₂) values in supramaximal exercise compared to incremental exercise.[2] Noakes further argues that those supramaximal data are therefore questionable and should be excluded, thus resulting in the conclusions of the original authors being disproved. Noakes’ first assertion (biological implausibility) is incorrect. His second assertion is at best biased, and at worst could be viewed as endorsing unethical practices.

The observation of lower VO₂ values at exhaustion during supramaximal exercise could be attributed to normal biological variation (random error). However, the kinetics of VO₂ dictates the rate at which VO₂ rises to meet the energetic demand. In situations where exhaustion occurs before the kinetics drive VO₂ to the maximum (so-called “extreme intensity exercise”[3]), VO₂ will be lower than that measured in an incremental test performed to exhaustion. The boundary between “severe intensity exercise” (wherein VO₂ reaches VO₂max before exercise termination) and “extreme exercise” has been estimated to be ~110-135% VO₂max,[3,4] providing the “biologically plausible explanation” Noakes wishes to deny.

To argue exclusion of the supramaximal data is ethically troubling. Such exclusion, in this case solely for the purpose of interpretation, results in grossly biased conclusions. For any scientist, particularly one as influential as Noakes, to adopt such an approach does a disservice to students of exercise science. It would be tragic indeed if these impressionable proto-scientists use Noakes’ precedence to endorse unethical data manipulation techniques to promote their own subjective opinions. Accordingly, I call upon Noakes to retract these statements to prevent further misleading interpretations from entering the literature.

References

1. Noakes TD. Peer review/fair review: How did A.V. Hill understand the VO2max and the “plateau phenomenon”? Still no clarity? Brit J Sports Med, in press. DOI: 10.1136/bjsm.2008.046771.

2. Hawkins MN, Raven PD, Snell PG, Stray-Gundersen J, Levine BD. Maximal oxygen uptake as a parametric parameter of cardiorespiratory capacity. Med Sci Sports Exerc. 2007;39:103-107.

3. Hill DW, Poole DC, Stevens JC. The relationship between power and the time to achieve VO2max. Med Sci Sports Exerc. 2002;34:709-714.

4. Wilkerson DP, Koppo K, Barstow TJ, Jones AM. Effect of work rate on the functional ‘gain’ of Phase II pulmonary O2 uptake response to exercise. Respir Physiol Neurobiol. 2004;142: 211-223.