Influence of the mode of heating on cerebral blood flow, non‐invasive intracranial pressure and thermal tolerance in humans

Abstract

Key points The human brain is particularly vulnerable to heat stress; this manifests as impaired cognition, orthostatic tolerance, work capacity and eventually, brain death. The brain's limitation in the heat is often ascribed to inadequate cerebral blood flow (CBF), but elevated intracranial pressure is commonly observed in mammalian models of heat stroke and can on its own cause functional impairment. The CBF response to incremental heat strain was dependent on the mode of heating, decreasing by 30% when exposed passively to hot, humid air (sauna), while remaining unchanged or increasing with passive hot‐water immersion (spa) and exercising in a hot environment. Non‐invasive intracranial pressure estimates (nICP) were increased universally by 18% at volitional thermal tolerance across all modes of heat stress, and therefore may play a contributing role in eliciting thermal tolerance. The sauna, more so than the spa or exercise, poses a greater challenge to the brain under mild to severe heating due to lower blood flow but similarly increased nICP. Abstract The human brain is particularly vulnerable to heat stress; this manifests as impaired cognitive function, orthostatic tolerance, work capacity, and eventually, brain death. This vulnerability is often ascribed to inadequate cerebral blood flow (CBF); however, elevated intracranial pressure (ICP) is also observed in mammalian models of heat stroke. We investigated the changes in CBF with incremental heat strain under three fundamentally different modes of heating, and assessed whether heating per se increased ICP. Fourteen fit participants (seven female) were heated to thermal tolerance or 40°C core temperature (Tc; oesophageal) via passive hot‐water immersion (spa), passive hot, humid air exposure (sauna), cycling exercise, and cycling exercise with CO2 inhalation to prevent heat‐induced hypocapnia. CBF was measured with duplex ultrasound at each 0.5°C increment in Tc and ICP was estimated non‐invasively (nICP) from optic nerve sheath diameter at thermal tolerance. At thermal tolerance, CBF was decreased by 30% in the sauna (P < 0.001), but was unchanged in the spa or with exercise (P ≥ 0.140). CBF increased by 17% when end‐tidal PnormalCO2 was clamped at eupnoeic pressure (P < 0.001). On the contrary, nICP increased universally by 18% with all modes of heating (P < 0.001). The maximum Tc was achieved with passive heating, and preventing hypocapnia during exercise did not improve exercise or thermal tolerance (P ≥ 0.146). Therefore, the regulation of CBF is dramatically different depending on the mode and dose of heating, whereas nICP responses are not. The sauna, more so than the spa or exercise, poses a greater challenge to the brain under equivalent heat strain.

Blunted cerebrovascular CO2 reactivity to satisfy the hungry heat stressed brain

“…These results by Gibbons and colleagues (2021) provide novel evidence that reductions in cerebrovascular CO 2 reactivity per se likely contribute favourably to CBF regulation during severe heat stress. Additionally, as reductions in CBF during severe heat strain did not dictate thermal tolerance or affect exercise performance, these results may indicate an increased possibility of cerebral oxidative/pro‐inflammatory stress (via reduced convective heat loss) with prolonged sauna/spa heat therapy and hyperthermic exercise prior to achieving subjective tolerance.…”

“…5 C of Gibbons et al . 2021). These data are supported by classic work by Harper and Glass (1965) who showed that substantial hypotension effectively overrules the vasoconstrictive ability of the cerebrovasculature to respond to reductions in (Harper & Glass, 1965).…”

From pigeon holes to descending spirals: a paradigm of physiology, cognitive performance and behaviour in extreme environments

“…It is well established that the brain, in particular the centres responsible for cardiorespiratory control, responds rapidly to homeostatic perturbations such as hypoxia (Bailey et al, 2009;Gibbons et al, 2020) and increases or decreases in temperature (Caldwell et al, 2020;Gibbons et al, 2020Gibbons et al, , 2021. In turn, the subsequent detrimental effects of hypoxia on cognitive performance have also been well-studied (see McMorris et al, 2017 andAndo et al, 2020 for a review).…”

Sodium bicarbonate ingestion mitigates the heat-induced hyperventilation and reduction in cerebral blood velocity during exercise in the heat

“…This hyperventilation results in excessive elimination of CO 2 from the body, which leads to reductions in arterial CO 2 pressure (Pa CO 2 ) (hypocapnia) (5,(12)(13)(14)(15). Because Pa CO 2 is a key determinant of cerebral circulation (16)(17)(18)(19)(20), the hypocapnia likely contributes to the cerebral hypoperfusion, as indicated by a reduction in middle cerebral artery mean blood velocity (MCAV) during hyperthermia (5,6,(21)(22)(23)(24). This cerebral hypoperfusion may limit heat exchange within the brain (25,26) as well as the fuel supply for the brain's increasing metabolism during hyperthermia (13,27).…”

“…It seems plausible, therefore, that sodium bicarbonate ingestion could attenuate heat-induced hyperventilation during exercise in the heat and, in turn, the hypocapnia. If so, the reduction in hypocapnia associated with sodium bicarbonate ingestion may increase cerebral blood flow, as hypocapnia is the primary factor causing cerebral vasoconstriction during prolonged exercise in the heat (6,23). Up to now, however, these possibilities have not been directly tested.…”