Critical core temperature: a hypothesis too simplistic to explain hyperthermia‐induced fatigue

It is striking that with manipulation of starting core temperature with acute water immersion (González-Alonso et al., 1999b) or chronic heat acclimatization (Nielsen et al., 1993), or when the rate of heat accumulation is altered by means of a water-perfused suit (González-Alonso et al., 1999b), trained cyclists exercising to exhaustion at a fixed submaximal work load in uncompensable hot environments terminate exercise at similar core temperatures, but with large differences in exercise duration (see Fig. 1). Furthermore, following 2 weeks of heat acclimatization, trained cyclists are capable of completing a prolonged time trial in the heat (outdoor settings: 36 °C dry air) faster and with markedly increased power output, but they achieve similar core temperatures at the end of the time trial (Racinais et al., 2015). Consistently across these observations, the average end-core temperature is reported to be ∼ 40 °C, and this has led to the suggestion of a ‘critical’ core temperature ultimately limiting exercise performance. Although several athletes surpass this core temperature level during real and simulated competitions in natural settings (Pugh et al., 2002; Racinais et al., 2015), some institutions have used 40 °C or even lower core temperature levels to set cut-off limits in scientific experiments, alluding to ethical reasons for safeguarding the health of the athlete. This has contributed to an almost dogmatic use of the critical core temperature hypothesis. (a) Esophageal temperature measured during cycling in 40°C environment after 30-min submersion to the neck in water at 17 °C (precooled), 36 °C (control) or 40 °C (preheated ). Data means ± standard error from seven subjects (modified from González-Alonso et al. (1999b) with permission). (b) Esophageal temperature (TC) response in a representative subject from acclimation study by Nielsen et al. (1993; modified from Nielsen et al. (1993) with permission) during 10 consecutive days of cycling in a 40 °C hot environment. The combined environmental and exercise-induced heat stress was uncompensable in both studies, largely because convective heat loss was markedly limited by the absence of fan cooling. However, the development of fatigue during exercise in the heat is not caused by one single factor, but the interaction of multiple interdependent physiologic processes and signals (Nybo et al., 2014). In this construct, it is an oversimplification to interpret the results as if the endpoint core/brain temperature is ‘critical’ and represents the ultimate safety break signal against catastrophic heat injury. In support, the end-temperature often differs when other factors of importance for fatigue are manipulated. For instance, concomitant development of dehydration, which aggravates physiologic strain, seems to lower the tolerable core temperature at the end of exhaustive exercise in the heat (González-Alonso et al., 1999a). On the other hand, manipulation of hyperthermia-induced central fatigue by enhancing the synaptic dopamine levels increases subjects exercise capacity in the heat and results in higher core temperatures at the end of exercise without reported side effects (Watson et al., 2005; Roelands et al., 2008). Also, during exercise in the heat or with passive heating, fatigue develops progressively as the subject becomes hyperthermic (Nybo & Nielsen, 2001; Morrison et al., 2004). This indicates that hyperthermia-induced fatigue is not an all-or-none phenomenon that occurs only when a certain ‘critical’ core temperature is surpassed. Moreover, untrained subjects seem to tolerate lower levels of hyperthermia and usually terminate exercise at core temperatures between 38 and 39 °C (Cheung & McLellan, 1998), while trained subjects on average may tolerate ∼ 40 °C, but with individual values of ∼ 41 °C reported in both laboratory experiments (González-Alonso et al., 1999b) and competitions (Pugh et al., 2002). Excessively high body temperatures can cause cell damage and mitochondrial dysfunction (White et al., 2007, 2012), but aside from pathophysiologic conditions leading to heat stroke (Sawka et al., 2011), it appears that human beings terminate volitional exercise well before such levels of harmful hyperthermia are reached. Taken together, these observations let us postulate that it is misleading to use the term critical core temperature in a reductionist way to characterize the influence of hyperthermia on the development of fatigue during prolonged exercise in the heat. In some conditions, the achievement of a high core temperature and inability to tolerate further heat storage may dominate, but one should not neglect the influence of the alterations in other physiologic processes occurring in parallel with hyperthermia. A dogmatic use of the ‘critical’ core temperature hypothesis will preclude major advances in our understanding and further identification of the hierarchy of physiologic factors underpinning fatigue in hot environments. Such advances in the fundamental knowledge and understanding in this area are of critical importance for providing physiologically based guidelines and developing novel strategies to delay or minimize the influence from heat stress in various exercise conditions and occupational settings.