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When is VO2max not max?

December 30th, 2011

Last spring, I had the opportunity to visit the sports science research group at the University of Cape Town. While I was there, I heard about some very surprising new research raising questions about the definition of VO2max. Since the research hadn’t yet been published, I agreed not to write about it; that paper has now been published in the January issue of the British Journal of Sports Medicine, so here goes.

A little background to start. The concept of VO2max — the absolute limit on how much oxygen you can deliver to your exercising muscles — is controversial these days, because it implies a physical limit on endurance performance. That idea, entrenched for the last century, has been challenged recently by researchers led by Cape Town’s Tim Noakes, whose “Central Governor Theory” argues that we never actually reach our ultimate physical limits — instead, our brains hold us back to protect us.

The new issue of BJSM actually contains eight different papers that could be interpreted as supporting Noakes’s basic thesis. And Noakes himself has an introductory article that offers a good overview of the debate and why it matters, for those who aren’t familiar with it. The full text of that intro is freely available here. Here’s Noakes’s somewhat oversimplified summary of the current status quo thinking:

In 1923, Nobel Laureate Archibald V Hill developed the currently popular model of exercise fatigue. According to his understanding, fatigue develops in the exercising skeletal muscles when the heart is no longer able to produce a cardiac output which is sufficient to cover the exercising muscles’ increased demands for oxygen. This causes skeletal muscle anaerobiosis (lack of oxygen) leading to lactic acidosis. The lactic acid so produced then ‘poisons’ the muscles, impairing their function and causing all the symptoms we recognise as ‘fatigue’.

We already know for sure that lactic acid doesn’t “poison” the muscles. But what about the idea of VO2max?

According to Hill, during the period between progressive exercise and exhaustion, whole body oxygen consumption reached a maximum value – the maximum oxygen consumption (VO2max) – ‘beyond which no effort can drive it’.

Two studies in the new issue of BJSM appear to show that VO2max isn’t actually “maximal” — you can get a higher value. As Noakes argues:

Had Hill shown this in 1923, he could not have concluded that maximal exercise performance is controlled by a limiting cardiac output. Instead a more complex explanation is required to explain why athletes always terminate exercise before they reach an ultimate oxygen limitation.

Okay, so much for intro. The study, by Fernando Beltrami and his colleagues in Cape Town, introduces a new VO2max protocol. VO2max is usually tested with an incremental design: you get on a treadmill (or an exercise bike), and the speed/workload gets higher/harder every minute or so until you reach failure. At some point before you reach failure, the amount of oxygen you’re using will have reached a plateau. Beltrami’s test is a decremental protocol. You start at a speed/workload slightly higher than what you were able to reach in a conventional incremental test, and then the speed is progressively reduced.

The subjects in the study all did a series of tests, as shown below. The key test was on visit number 4, when the experimental group did their decremental test:

Now, why would you expect a different result from a decremental test instead of an incremental test?

We reasoned that if subjects knew beforehand that the test would become progressively easier the longer it continued, the possibility was that any biological controls directing the termination of exercise might be relaxed, thus allowing the achievement of a VO2max higher than that achieved with conventional INC.

In other words, if the plateau observed in conventional VO2max tests is mediated by the brain in some way, rather than being purely physical, then it might be possible to change the plateau. And here are the VO2max produced in those multiple tests by the two groups:

Sure enough, the VO2 produced in the decremental test is higher by 4.4% (with p=0.004) than in the incremental test. Strangely, it stays at this new higher value in the subsequent incremental test — even though there were no related physiological changes. Heart rate, breathing rate, and ventilation at VO2max were the same in the different protocols. So what’s going on?

Emotional stress can affect blood flow during exercise and stimulation of sympathetic cholinergic fibres are thought to promote arteriolar vasodilatation and to induce changes in metabolism, producing a switch from aerobic metabolism to increased oxygen-independent glycolytic pathways… We propose the interesting possibility that an anticipatory difference in perception of the future workload might impact the sympathetic or parasympathetic drives and lead to differences in the metabolic response during exercise.

That’s just speculation. But what’s not speculation is that the subjects in this study did conventional VO2max tests and produced reproducible plateaus; then they did another test that just involved changing the order of the speed, and produced higher Vo2max values. Whatever is happening here, it’s not tenable to argue that the VO2max values measured in conventional incremental tests represent some absolute physical limit on the body’s ability to deliver oxygen to working muscles.

  1. December 30th, 2011 at 18:02 | #1

    Interesting study! Would like to see the RER and HR data. But, achievement of VO2max during sub-maximal protocols is well established (Karlsson 1967). I am wondering if RPE was measured, and how they eliminated any bias related to performing an incremental versus decremental test.

    Finally, does the central governor theory apply to sub-maximal efforts when V02max is achieved?

  2. Marc
    December 31st, 2011 at 20:06 | #2

    Right, well, to say VO2max is not max doesn’t follow from what I understand about this research, but maybe saying ‘the way you’ve been testing hasn’t given you your actual max, it’s probably about 4.5% higher’ is about right. It sounds to me as though Noakes has merely changed the method of measurement to one where we can better measure VO2max, but has the definition of VO2max been changed? Our methods of hitting the ceiling have merely been corrected, but it’s not as though there is no ceiling. Maybe that wasn’t the point of the study though…

  3. alex
    December 31st, 2011 at 21:05 | #3

    @Kieran: Not sure I entirely understand the question. What bias? VO2max has been defined in a certain way since the 1920s, and very rigorously defined since the 1960s. This new test achieves a higher value than that standard test, so that standard test can’t be the “max.”

    @Marc: Let me clarify the statement: VO2max as it has been defined for the last 90 years is not max. And it’s not as simple as saying “Oh, the max is 4.5% higher than we thought.” How do we know that new value is a “max”? The whole argument that what we observe in incremental tests is a fundamental physical limit of the human body was based on the fact that the measurement appears to plateau. But now we know there are ways of eliciting VO2max measurements above that plateau. That doesn’t mean the plateau was mismeasured — it means that plateau doesn’t correspond to any particular physical limit.

    Now, that doesn’t mean that the human body has NO physical limit on oxygen uptake. Obviously you’re never going to get any human up to five trillion ml/min/kg. The question is: do humans ever reach a consistent, reproducible limit dictated by physical limitations (i.e. a bottleneck in oxygen delivery somewhere between the point where it enters your mouth and it’s used in your muscles)? Or do the apparent maxima we observe (like the plateau in the incremental test) correspond to some other regulatory process, like Noakes’s central governor?

  4. Jordan
    December 31st, 2011 at 22:31 | #4

    I would be interested to see the individual subject data, and the Lab’s TEM for running these tests, this mean data as is often presented may be misrepresenting the truth. It is possible that the effect isn’t really seen in each of the decremental group subjects, maybe one strong outlier is pulling up the mean, it also interesting the final incremental shows essentially the same result as the decrimental. If Noake’s Central governor theory holds true and explains why a traditional test would produce a lower value, why does it not limit this final incremental? I shall have to read the actual paper at some point, but from having discussed a lot of Noake’s work over the past year and a half with some very smart people, there are usually alot of flaws and twisting of facts in his arguements. I respect that he questions traditionally held views, but he has never provided any real credible evidence for his theory that I have seen, until now perhaps?

  5. alex
    December 31st, 2011 at 22:48 | #5

    @Jordan: Lots of people don’t like Noakes, so it might have been better if I hadn’t mentioned his name. So forget Noakes, and forget the Central Governor theory (which wasn’t mentioned in the paper). You suggest that the data may be misrepresenting the truth. If you really think that’s the case, you should request the original data from the study authors, as scientific misconduct is a serious offence.

    But if we accept that the data presented in the paper hasn’t been fabricated or manipulated (as I do), then the important question is: how can these results be explained within the conventional theory of VO2max? To answer that question, we don’t need to pay attention to any of Noakes’s theories, whatever “twisting of facts” he engages in. This isn’t theory; it’s an experimental observation. How does the current theory account for this observation?

  6. January 2nd, 2012 at 20:51 | #6

    The bias was introduced to the reverse group by stating to them that ” …if the subjects knew beforehand that the would become progressively easier …” that they would emotionally relax and as a result perform better. The reverse group could quite easily have under-performed on their incremental test. Unfortunately, the abstract doesn’t provide any descriptives of the subjects so we can’t really see how well matched the groups were, nor does it break down the methodology whereby I would hope that the achievement of VO2max was verified with RER, HR and BLa measurements.

    I tend to believe that a finite VO2max can be achieved, there is very good data from Taylor (1955) and recently Hawkins (2007) supporting the concept.

  7. alex
    January 2nd, 2012 at 21:24 | #7

    @Kieran: It sounds to me like you’re agreeing with the authors here. According to the conventional understanding of VO2max, how could they have “underperformed” in the incremental test? It’s (theoretically, at least) a measurement of a physical trait (like height or blood volume), not a performance measurement. They achieved a plateau, and that plateau was confirmed via a subsequent supramaximal verification stage. That’s the definition of how to measure VO2max, as per Hawkins (2007)!

    If this measurement was affected by the fact that the subjects could “emotionally relax and as a result perform better,” then that proves exactly what the authors of the study are saying: that the plateau in VO2max tests doesn’t correspond to a straightforward physical limitation (e.g. that the heart can’t pump oxygen any faster, or whatever theory you subscribe to), but instead can be affected by mental state.

    Incidentally, you mention the Hawkins 2007 paper. What this paper showed is that they were able to (a) obtain a plateau in their subjects using an incremental test, and (b) perform a subsequent supramaximal stage that produced the same VO2max value. The new paper (which I’m happy to e-mail you if you’re interested) used exactly the same protocol to obtain their initial VO2max values. Then they used the decremental protocol to obtain a higher value. So how can the value measured by the Hawkins protocol be considered “maximal”?

  8. January 2nd, 2012 at 22:39 | #8

    I would be interested in reading the paper and looking at the data, thanks in advance!

    VO2max performance may well be influenced by mental state, and that’s my point. If the athletes believed that their decremental test would be easier (as the authors stated to them prior to testing), the inverse may also have been communicated to them.

    Whether or not the “mental state” has a physiological or psychological is a different matter and I am not sure that they’ve answered it here. Once again, the relevant RER, HR and BLa data for all tests would help.

  9. alex
    January 2nd, 2012 at 22:46 | #9

    @Kieran: So… you agree with the authors of the study?

    Here’s the traditional definition of VO2max:

    “According to Hill, during the period between progressive exercise and exhaustion, whole body oxygen consumption reached a maximum value – the maximum oxygen consumption (VO2max) – ‘beyond which no effort can drive it’.”

    If you’re saying that VO2max can be influenced by mental state, then what you’re saying is that the traditional definition of VO2max, as currently taught to exercise physiologists around the world, is wrong. And that’s what the authors of this paper are saying too.

  10. Fernando Beltrami
    January 5th, 2012 at 04:51 | #10

    First of all, hello Alex! I came to your blog through a friend that saw it and called my attention. It’s a pity we didn’t meet when you were visiting in Cape Town. I must say you defending the work better then I would, so thanks!

    @Kieran: HR data is the same for both groups, even individually. RER is definitely coming down during decremental runs, and it is going up (as you’d expect) during the incrementals. We couldn’t reach statistical significance though, but there is a change in pattern. Lactate does not work… values are simply high for both trials.

    @Marc: as Alex said, the point is that yes, we found a new max. But for the last 90 years, “max” was a function of having a plateau. The study showed that a plateau is no longer evidence for a physical limitation. Therefore we just have another “max” until a new protocol comes up, different from the absolute max we had so far.

    @Jordan: individual data ranged from 0 to 12% change. Data we did not use showed that if we get the chance to improve the decremental test we get higher values. Since the test is decremental, if it starts too high or goes down too quickly you loose it. As for twisting and flaws, please be careful on your words. We have to assume that our peers are serious people doing serious work, and this is the take we have on every single paper we read. As for agreeing with someone else’s logic and reasoning, you have all the rights not to. We are looking for answers for the same questions.

    @Kieran: the study used the best sets of criteria available out there. Running uphill was the exercise mode because it is known to produce the higher values on subjects. Fit people were investigated (we have a similar set of data with elite 28-30min 10k runners), data came from three different labs, supramaximal test were used (as per hawkins yoou quoted), familiarization sessions were performed and randomization of subjects into the groups was done only on day 3, after the baseline tests.

    As for the psychological component: the hypothesis of difference response from the “getting easier” perspective was put forward before the study was performed, as it should. In simple terms, there are tons of papers showing that running harder does not show a higehr VO2max. So there was only one other option, running slower, toward more aerobic speeds. The decremental test shows itself harder than an incremental one, by the way. However, when a stage changes, the immediate feeling is better during DEC than during INC.

    We do not, however, have a decent explanation (yet) as to what then limits VO2 during the incremental or to why it remains higher on the last test. This study was created to test the hypothesis that a plateau in VO2 during INC was a physical limitation in our capacity to use oxygen, which for the past 90 years was thought to be the case, and was always a strong argument against the central governor.

    Alex, thanks once again for commenting our work!

  11. January 8th, 2012 at 18:37 | #11

    @Alex: my point about mental state was that “VO2max performance” can be affected by it, meaning that a VO2max test result can be dependent on factors such as motivation prior to the test. I am not saying that the primary determinant of physiological VO2max is the brain; it isn’t. The limit lies with the heart and lungs.

    We know that a plateau is not always observable following VO2max tests and this finding has been repeated numerously. That’s why strict secondary criteria are used to determine whether or not VO2max has been achieved which help complete the picture, these are: RER of 1.15, HR of >90%MHR, and a BLa of 8-9mm, none of which were achieved for any group in this study.

    What exercise physiologists are being taught is that the limits to VO2max lie with the inability of the cardio-respiratory to respond to muscular demands during maximal exercise. This paper offers no counter-argument, and this paper doesn’t shift the paradigm in any other direction.

    @Fernando: it would have been interesting if you had have published the individual descriptives and the composition of each group per subject. It would also help if you had a more uniform group of subjects (from 17-47 years in your study, mean age 29 years) that were all runners or cross-country skiers but not a mixture.

    I am interested in your comment “The decremental test shows itself harder than an incremental one, by the way”. In what respect?

  12. alex
    January 8th, 2012 at 20:02 | #12

    @Kieran: So, to cut through the jargon, your explanation for this result is that the subjects failed to reach VO2max in their incremental tests, even though they achieved plateaus which were subsequently verified by a supramaximal test as suggested by Hawkins (the reference that you yourself suggested in an earlier comment)?

    Let me ask you a purely hypothetical question. If the initial incremental tests were performed to your satisfaction (i.e. you did them yourself), and then a subsequent decremental test produced a higher result, would that change your view of the nature and significance of VO2max?

  13. RH
    January 10th, 2012 at 22:09 | #13

    I am a complete layman on this subject, but when a scientific measure is called BLa, I feel confident enough to chime in. :)

    @Kieran
    “the limits to VO2max lie with the inability of the cardio-respiratory to respond to muscular demands during maximal exercise”.

    This paradigm depends on the ability of exercising muscles to signal their exact demands to the cardiorespiratory system and the cardiorespiratoty system do deliver the exact amount in the right place.

    The problem seems to me, that in most sports, only a particular group of muscles is using large quantities of oxygen, but the delivery system delivers via the whole circulatory system, so demand is local while delivery is wholesale.

    Is there an exact known pathway through which the oxygen demand of the nmuscles are mediated to the cardiorespiratory system? If not, the paradigm is merely hypothetical. If so, is this signalling pathway allways signalling the exact oxigen demand? If so, is the delivery system always delivering the exact ammount on the right place, not mediated by other demands, such as, say, temperature regulation, CO2 regulation, blood pressure regulation, or psychological states like panic or anticipation?

    If one of the answers is no, should the paradigm not be something like “the limits to VO2max lie in the ability of active muscles to signal their demands exactly and the cardio-repiratory system to match the signaled demand”?

    It doesn’t take too much for an interacting system to be dependent previous states, so you don’t have to be comitted to a central governor to allow for different VO2 max in different circumstances. Several captains on one ship is enough.

  14. Fernando
    January 13th, 2012 at 00:49 | #14

    @Kieran: yes, performance is influenced by mental status. However, is someone reaches a plateau and latter run at higher intensities with no further increases in VO2 you have to believe they have reached their maximum.

    Second, how can you say no secondary criteria was reached: first of all, the primary criteria was reached (the plateau). Second, most subjects did indeed reach the secondary criteria you mention (HR and RER).

    This paper shows that the human body, as it is during a plateau (what you called inability to respond to muscular demands), is able to consume ~4,5% more oxygen… so I ask you, why does it fail during the plateau if it can, as we showed, use more oxygen?

    I don’t see what influence a more uniform group would have here… if anything by using a less equal group we played against our odds to find real differences. As I mentioned before, the study was repeated on elite runners with the same results.

    On the being a harder test issue, try it for yourself (I’m serious, please don’t take it as an offense). Running a decremental exercise test set to exhaust you in ~6min feels much than an incremental test, which only have some 2-3 min of really hard running at the end.

  15. February 6th, 2012 at 04:51 | #15

    @all, sorry for delayed response.

    @RH As of yet, there hasn’t been a single well defined metabolic signal in the muscle that the cardio-respiratory system is responding to, that’s OK. What we know in ex. physiology is that VO2max is a product of processes of both convection & diffusion, and to read that this is “wrong” when the evidence is very strong with very precise mechanisms having been well identified is very premature. As for cardio-respiratory system responding to muscle signals, cardiac output matches VO2 very precisely.

    @Alex: on the hypothetical question, I think that it would be interesting to conduct this experiment on a homogenous group of athletes all involved in the same sport (running, cycling).

    @Fernando: for your secondary criteria, the individual descriptive data isn’t published so we don’t know. No offense taken for the “try it for yourself” comment, but it’s not for me to determine whether it’s harder or not. Did you take RPE during the test?

    And of course, mental state affects performance. However if there’s a physiological mechanism behind it is unanswered.

  1. January 2nd, 2012 at 18:43 | #1
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