Exercise Physiology

The Science of Performance

How does a foundational myth become sacred scientific dogma?

The case of A.V. Hill and the anaerobiosis controversy

Part 3

 by Tim Noakes1

The A.V. Hill cardiovascular/anaerobic model of exercise physiology

The work of Nobel Laureates Frederick Grover Hopkins (Fletcher and Hopkins 1907) and Archibald Vivian Hill and their colleagues (Hill 1925, 1965; Hill and Lupton 1923; Hill et al. 1924a, 1924b) forms the basis for the popular conjecture that an oxygen limitation develops during maximal exercise causing skeletal muscle hypoxia/anaerobiosis to terminate exercise. This model enjoys an almost complete acceptance in virtually all modern textbooks of exercise physiology and has survived, essentially without serious intellectual challenge, already for almost 80 years (Bassett and Howley 1997, 2000; Bergh et al. 2000, Ekblom 2000; Wagner 2000; Bassett 2002).

This model holds that exercise performance is determined by the capacity of the athlete’s large heart to pump unusually large volumes of blood and oxygen to the muscles. This allows the muscles to achieve higher work rates before they outstrip the available oxygen supply, developing skeletal muscle anaerobiosis (Figure 4.1). This model remains the most popular for explaining why fatigue develops during exercise; how the body adapts to training; how these adaptations enhance performance and health and, as a consequence, how effective exercise training programmes should be structured.

This model further predicts that training increases ‘cardiovascular fitness’ especially by increasing the body’s maximum capacity to consume oxygen, measured as the maximum oxygen consumption (VO2 max). This effect results from an increased maximum capacity of the heart to pump blood (the cardiac output) and an enhanced capacity of the muscles to consume that oxygen, the latter by increasing the number of blood vessels (capillaries) in the skeletal muscles and the number and size of those subcellular structures, the mitochondriae, which produce the energy for the exercising muscles. It is argued that these adaptations delay the onset of skeletal muscle anaerobiosis during vigorous exercise, thereby reducing blood lactate concentrations in muscle and blood at all exercise intensities above the so-called ‘anaerobic threshold’ – the threshold which apparently indicates the onset of skeletal muscle anaerobiosis and the sudden onset of high rates of lactic acid (lactate) production by the increasingly anaerobic muscles. The delayed onset of this blood lactate accumulation after training then allows the exercising muscles to continue contracting for longer at higher intensities before the onset of fatigue. An important but unrecognized prediction of this model is that increases in (coronary) blood flow to the heart must be an essential adaptation to training (Noakes 2000). The higher coronary blood flow allows a greater pumping capacity of the heart, producing a greater cardiac output to perfuse the exercising muscles, which can then achieve a higher exercise capacity.

Figure 4.1

This model finds strong support from the confirmation that these changes do indeed result from training, as fully documented in the literature. The key question is whether these changes are causally linked; that is, do these changes cause the change in exercise performance or do they occur pari passu with one or more other adaptations that are the real cause of changes in exercise performance. For there are important deficiencies in this model which have been fully argued (Noakes 1988, 1991 1997, 1998; Noakes et al. 2001; Noakes 2000) and counter-argued (Bassett and Howley 1997, 2000; Bergh et al. 2000, Ekblom 2000; Wagner 2000) elsewhere and which do not need to be repeated here. But the fundamental contention of this model is the foundation belief that oxygen delivery determines the exercise performance; that is that oxygen delivery (A) causes the exercise performance (B) (Figure 4.2).

My special interest in this topic began when I read David Costill’s classic textbook A Scientific Approach to Distance Running in which he wrote: ‘Since the early work of Hill and Lupton (1923), exercise physiologists have associated the limits of human endurance with the ability to consume larger volumes of oxygen during exhaustive exercise’ (1979: 25–6).

This quote clearly identified what the recently retired Costill, representing as he does the link to the previous generation of influential exercise physiologists in the United States, considered to be the key foundation on which this universally accepted theory rests. It was when reading those studies that I detected a critical flaw and an unexpected hypothesis, both of which had been ignored (or perhaps dismissed) for more than 50 years.

The foundation of the classical Hill cardiovascular/anaerobic model (Noakes 2000) can be traced to the pivotal influence that the original study of Fletcher and Hopkins (1907) at Cambridge University exerted on the thinking of Hill and his colleagues in Manchester. Fletcher and Hopkins wished to establish whether or not ‘within a muscle itself, means exist for an oxidative control of its own acid formation, or for the alteration or destruction of acid which has been formed, either there or by muscular activity elsewhere in the body’ (1907: 16).  They were perplexed by the consistent finding at that time, that lactic acid (lactate) concentrations in excised skeletal muscle preparations were always high, regardless of the experimental conditions, for example whether the excised muscle came from rested, exercised, fresh or preserved tissue. They wondered whether this unexpected finding resulted not from ‘the technical difficulties of lactic acid estimation, but that it is due to the difficulties inherent in the extractive treatment of an irritable muscle’ (Needham and Baldwin 1949: 59).

By rapidly immersing the excised muscle in ice-cold alcohol, they were able to show that the freshly excised hind limb muscles of frogs had low initial lactic acid concentrations and released little lactic acid during the first 24 hours when incubated in air at room temperature. Even less lactate was produced when the muscles were stored in oxygen-enriched air also at room temperature. Lactic acid production was substantially increased when the muscles were stored in hydrogen; this effect was increased at higher temperatures. Next, they electrically stimulated the muscles in the excised hind limbs to contract until they no longer responded to stimulation. After prolonged stimulation, muscle lactic acid concentrations were elevated but were only about one-half the concentrations measured in muscles exposed acutely to chemical- or heat induced damage. Finally, previously stimulated muscles were left to recover for 18 or more hours either in room air, or in nitrogen or oxygen at different temperatures. In all cases, lactic acid concentrations were lowest in muscles exposed to oxygen at any temperature. Accordingly Fletcher and Hopkins (1907) concluded that:

The lactic acid content of muscle is profoundly affected by the nature of the treatment received before or during the extraction. ... The increase of acid is most rapid under anaerobic conditions, is slower in air, and it is not to be observed in an atmosphere of pure oxygen (297–8).

Thus

the excised but undamaged muscle when exposed to a sufficient tension of oxygen has in itself the power of dealing in some way with the lactic acid which has accumulated during fatigue and regaining irritability in an atmosphere of pure oxygen, their content of lactic acid is greatly reduced (ibid: 297).

They concluded that ‘Lactic acid is spontaneously developed, under anaerobic conditions in excised muscle’ and that ‘fatigue due to contractions is accompanied by an increase of lactic acid’ (ibid: 301).

Fletcher and Hopkins (1907) did not conclude either that anaerobiosis was the sole reason for increased lactic acid production by amphibian muscle or that the ‘increase of lactic acid’ caused fatigue. They merely described these separate phenomena whilst developing a novel technique (immediate immersion in ice cold alcohol), accurately to measure muscle lactic acid concentrations.  Historically, however, these studies have been interpreted somewhat differently.  They have been seen to establish the classical interpretation that lactic acid production by skeletal muscle during exercise requires the absence of skeletal muscle aerobiosis (hence anaerobiosis) and that the increased production of lactic acid causes a peripherally located skeletal muscle fatigue, according to the mechanism shown in Figure 4.1.

As a result, when Hill and his colleagues measured increased blood lactate concentrations during exercise in humans (Hill et al. 1924b), they were bound to conclude that the muscles were contracting anaerobically since: ‘Lactic acid does not accumulate so long as the oxygen supply remains adequate’ (Hill et al. 1924a: 136). Thus arose the first pillar of the concept that oxygen deficiency limits maximum exercise performance (Noakes 1988, 1991, 1997, 1998, 2000; Noakes et al. 2001) specifically as a result of skeletal muscle anaerobiosis and a resulting lactic acidosis.