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“This oxygen uptake value doesn’t look right”: on interpreting exercise tests in athletes

December 15, 2015

This post is inspired by a discussion between Antoine Vayer, Jeroen Swart and myself a few days ago on Twitter.  Vayer is a former coach of the Festina cycling team, and a strong advocate of interpreting power output data in the context of doping.  Swart is an exercise physiologist and sports physician who has been involved in the testing of Chris Froome at GSK (or embroiled in the testing, depending on how you look at it – the social media reaction has been quite something.  I can’t put my finger on quite what kind of something it’s been, but it’s something nonetheless).  I noticed that Vayer had put up some data from an incremental cycling test, with the following challenge to “experts”:  “Game 1/10 for experts from Lisbeth ! Who got this VO2 [oxygen uptake] >91 ml/mn/kg ? Is he a cheater or not ? Is it possible ?”.  Now, I consider myself something of an expert here.  In fact, I’d say that the number of people in the world who understand the VO2 response to exercise better than me could comfortably fit in a double-decker bus, and some of them are dead.  So I had a quick look at the data.

The maximal oxygen uptake (VO2max) value was recorded during an incremental test in which it appears that the athlete exercised for about 4 minutes each stage and rested between stages, with gas exchange data recorded every 30 seconds.  The 91 mL/kg/min VO2max was recorded towards the end of the penultimate stage displayed in Vayer’s tweet.  But there was something odd about it. The VO2, in absolute terms was 6.29 L/min, but this value was achieved at a power output of 425 W.  Any exercise physiologist faced with a high VO2 will naturally enquire about the power at which it was achieved, or if faced with a high power output, will enquire about the VO2 achieved.  The first thing you learn (or should learn) when analysing test data like this is to ask the question “does it look right?”.  If the data deviate wildly from what is considered normal, it’s probably wrong for some reason.  This works for athletic data as well as any other because there are robust relationships between VO2 and power output.  Vayer’s data make no physiological sense.

The VO2-power output relationship follows this rule-of-thumb: for every watt of power produced, you consume about 10 mL of oxygen in the steady state (give or take 1 mL/min/W).  This makes for a very handy error detector in the lab.  This works by taking any absolute VO2 value (in this case 6.29 L/min), subtracting ~0.80-1.00 L/min to account for the O2 cost of pedalling, and dividing the answer by power output.  In this case, 6290-1000 = 5290/425 = 12.4 mL/min/W (this figure is known as the “gain” for VO2).  In other words, there appears to be a very large error in VO2 of about 1.0 L/min.  The actual VO2 that should be associated with a power output of 425 W is ~5.25 L/min (assuming a baseline pedalling VO2 of 1.0 L/min, which at a cadence of 92 rpm seems reasonable).  It may even be lower than that in an efficient athlete. Jeroen Swart estimated 4.95 ± 0.15 L/min VO2 for the same power.

By way of contrast, Chris Froome’s recent data produces a gain of ~9.4 mL/min/W (5.91 L/min, less 1 L/min, so 4910/525 = 9.4).  This is a normal VO2 gain, and may even be an underestimate given that this was measured during a ramp test, in contrast to the 4 minute stages used by Vayer (quite correctly if steady state VO2 was an important variable to measure).  In Froome’s case, the 30 W/min ramp is non-steady state and VO2 will lag power output.  Additionally, if Froome had a plateau in VO2 (or was approaching one), this would have reduced the gain still further.  Thus, it is reasonable to suppose that his steady-state VO2 gain would be higher than 9.4 mL/min/W. In all likelihood, it would be very close to 10 mL/min/W.  Why, then, is the VO2 recorded in the test in question so high?  There are four possibilities: 1) an extravagant metabolic response by the cyclist; 2) an error in standardisation of ambient conditions; 3) an ergometer calibration error, or 4) an error in the flow or oxygen sensor and/or calibration.

Extravagant metabolism

It is possible that the relationship between VO2 and power output can be altered by exercising at high intensities for prolonged periods.  This increases the VO2 gain, and values >12 mL/min/W have been observed in the literature.  So the “slow component of oxygen uptake” could drive the VO2 above the predicted steady state value and increase the gain.  I have done a bit of work on the slow component, and I think it may be a factor in this test.  It is, however, unlikely to explain the VO2 being 1.0 L/min above expected.  This is because, as its name suggests, the slow component takes time to express itself.  It takes 90-120 to emerge from the “normal” or “fast component” of the response, and if you fit a curve to it, it has a time constant of at least 200 seconds.  It therefore takes many minutes to develop, and in this test many minutes we do not have (nor does the VO2 does seem to be systematically rising in the 425 W stage).  It is also unlikely that previous test stages generated much slow component behaviour.  This is again partly due to their length, and partly due to the modest blood lactate concentrations measured (2.1 mM at 375 W).  The slow component only develops above the lactate threshold, and in the 375 W stage the cyclist is only just above it.  Any slow component would be small even if the 375 W stage was continued for 6-8 minutes.  Finally, the denominator of the VO2 gain equation is against us: the largest slow components recorded in the literature are for exhaustive exercise bouts lasting 10-15 minutes, and they can exceed 1 L/min.  To achieve this in the time required in this stage would need VO2 to rise at an unbelievably swift rate, and we just don’t see this happening.  So, whilst the slow component of VO2 is real and significant, it does not appear to be an explanation for the high VO2 values reported.

Ambient conditions and gas exchange calculations

Pulmonary gas exchange variables must be corrected from ambient temperatures and pressures to standardised temperatures before interpretation.  These days using automated systems these calculations are done automatically, but sometimes input is needed as part of routine calibration.  For ventilation, values are expressed BTPS – Body Temperature and Pressure, Saturated – because the true volume exhaled at the time matters.  For VO2 (and VCO2), the correction provides Standard Temperature and Pressure for Dry gas (STPD).  The only way to introduce error here is to fail to change the ambient temperature settings prior to analysis.  However, a 10°C error in temperature (unheard of in a well-ventilated or an air-conditioned laboratory) would change VO2 by no more than ~0.3 L/min.  A similar error would occur if you got barometric pressure wrong by 30 mmHg.  Thus, it is unlikely that a 1.0 L/min error would be introduced here.

Ergometer calibration

A cycle ergometer that is not calibrated can produce very strange VO2 responses.  I vividly remember taking delivery of an ergometer that had not been stored correctly and its flywheel was off by a few millimetres.  Being electrically-braked, a few millimetres is huge, and I was exhausted at a power output 150 W lower than normal with an (apparently) enormous VO2 gain.  But my VO2max was in the normal range, so it didn’t seem to be the gas analyser, and it just felt wrong.  In the case in hand, it is the VO2 that seems too high, not the power.  And an elite cyclist would also very quickly realise if the ergometer was out. As an example, I once started a treadmill test on an athlete who got quite animated about how hard the 10 km/h warm-up felt.  It turned out that somebody had changed the settings to miles per hour!  The ergometer is not likely to be the problem in this case.

The gas analyser

The origin of the error can be limited to the gas analysis system.  I am not sure whether the Oxycon system being used in this test (as Vayer told me it was) was being used in a mixing chamber mode or breath-by-breath, but it seems that the ventilatory variables look normal: minute ventilation is not astoundingly high for an athlete producing 90 mL/kg/min (if anything it is too low).  Indeed, the VE/VO2 ratio at maximal exercise is usually >35 in my experience.  Here it is ~32.  Not that low, but low all the same.  In short, the flow sensor or ventilatory volume measurement is not a strong contender for the extra litre/min of VO2.

This leaves us with the O2 sensor itself.  The origin of the error is impossible to pin-down without knowing the precise specifications of the analyser (there are a number of Oxycon models, some which use fuel cell type analysers, others paramagnetic sensors), but it is possible that an electrochemical fuel cell analyser had reached the end of its life at the time of the test and started reading high. Alternatively, a calibration error resulting in incorrect zero and/or span calibration could have caused a systematic error in VO2.  It is important to state that this error is not peculiar to the 425 W stage: the 375 W stage preceding it produces gain values of around 12 mL/min/W , so this error is evident throughout the test [in a previous edit, I said 14.5 mL/min/W – I’d forgotten to subtract baseline VO2 in the calculation.  Mistakes are easy to make with gas exchange data!].  A calibration error on one of the calibration points would amplify the erroneous gain at lower power outputs, wherein the expired O2 fraction (FEO2) would be lower than during maximal exercise (that is, the error will get larger or smaller as FEO2 falls away from 20.95%).  That we are not seeing this means that the whole calibration curve is systematically in error.  The cause of this (analyser ‘drift’ or fuel cell end-of-life performance) is impossible to call without data from the calibration procedure itself.

In conclusion, I’m overthinking this.

Or, to put it another way, the issues above illustrate why physiological testing is unlikely to ever be a major pillar of anti-doping efforts: there are too many sources of error, as well as too much variation in testing protocols, the equipment and ergometers used between labs.  Anybody who has attended a conference on sports physiology will appreciate that there are almost as many measures of “threshold” as there are people working in the field.  Getting scientists and practitioners to agree measurement standards seems a very long way off.  Even if such standards could be agreed, there are no clear physiological “red lines” above which doping can be inferred.  This is because athletes, like all humans, occupy a normal distribution of physiological function.  More correctly, the parameters of endurance performance (be they physiological, biomechanical, psychological) are all normally distributed, and the sum of these distributions makes the athlete who they are.  Doping can and does shift some of those curves, but from where to where? For specific individuals we simply don’t know most of the time, and until we are sure a change in physiological test results are not due to errors we inadvertently introduce, we never will know.

 

So with that, Merry Christmas…

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8 Comments leave one →
  1. December 16, 2015 6:05 am

    Great article Mark, thanks – helped clarify some of the issues for the ‘non-experts’ in this field! (-:

  2. Sinjin permalink
    December 17, 2015 12:10 am

    I think you’ve hit the nail on the head, VO2max is a redundant test and physiological parameter! Reads like you’ve just ‘proved’ that ; ). I think you came close with an extravagant metabolism, Froome could easily have had a very efficient cardio-respiratory delivery and mitochondrial density but may just not be able to convert through poor muscle ATP kinetics/ contraction. Surely a higher VO2 would suggest better consumption through respiratory shunt, capilliarisation and diffusion, usually brought about by haemoglobin/ myoglobin saturation which EPO serves to increase? His VO2peak value increased but his wVO2 dropped slightly over 8 years?? Q. How can an indirect measure, so convoluted and erroneous as VO2max (changed to VO2peak because the plateau principle has never been established, as only an apparent maximum is measured) be regarded as a worthwhile measure of performance subject to so many variables have any integrity as a robust parameter?……….. A. Purely because of historical reasons and ‘sport science’ lack of ability to embrace new concepts and approaches. Plus obvious commercial reasons. http://www.sportsci.org/2011/ss.pdf

  3. Wally Bixby permalink
    December 17, 2015 12:56 am

    Great article. Thanks for the sanity in the sea of madness!

  4. kiloo permalink
    December 17, 2015 10:30 am

    So for doping matter, better to rely on volumes of PED trafficking and police inquiring to believe that sport at top level it’s more likeky they are doped.

  5. Les permalink
    December 18, 2015 3:53 pm

    Another informed and interesting blog post Mark.

  6. Sinjin permalink
    January 13, 2016 7:07 pm

    Mark, any thoughts? Or that bus is leaving without you!! ; )

    • January 13, 2016 10:14 pm

      Yes: my view is that VO2max is far from redundant. I’m not sure I follow your “respiratory shunt” or “poor muscle ATP kinetics” points, but in this case the higher VO2 measured in the test is caused by technical error, not physiological adaptation. The locus of control for submaximal VO2 is in the muscle so far as we can tell. When VO2max is attained, this is usually a sign that an element or elements of the O2 conductance pathway from mouth to mitochondrion has reached a functional limit.

      There have been a number of studies that have refuted the role of a central governor in determining VO2max: simply stated, there is no evidence that VO2 is limited by a regulatory mechanism, since you can increase external power (and cardiac work) at VO2max, but VO2 does not go up. Peter Wagner’s work on the limitations to VO2max is the best available in my opinion. http://www.ncbi.nlm.nih.gov/pubmed/20483502

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