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Cerebral Vascular Control and Metabolism in Heat Stress

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ABSTRACT

This review provides an in‐depth update on the impact of heat stress on cerebrovascular functioning. The regulation of cerebral temperature, blood flow, and metabolism are discussed. We further provide an overview of vascular permeability, the neurocognitive changes, and the key clinical implications and pathologies known to confound cerebral functioning during hyperthermia. A reduction in cerebral blood flow (CBF), derived primarily from a respiratory‐induced alkalosis, underscores the cerebrovascular changes to hyperthermia. Arterial pressures may also become compromised because of reduced peripheral resistance secondary to skin vasodilatation. Therefore, when hyperthermia is combined with conditions that increase cardiovascular strain, for example, orthostasis or dehydration, the inability to preserve cerebral perfusion pressure further reduces CBF. A reduced cerebral perfusion pressure is in turn the primary mechanism for impaired tolerance to orthostatic challenges. Any reduction in CBF attenuates the brain's convective heat loss, while the hyperthermic‐induced increase in metabolic rate increases the cerebral heat gain. This paradoxical uncoupling of CBF to metabolism increases brain temperature, and potentiates a condition whereby cerebral oxygenation may be compromised. With levels of experimentally viable passive hyperthermia (up to 39.5‐40.0°C core temperature), the associated reduction in CBF (∼30%) and increase in cerebral metabolic demand (∼10%) is likely compensated by increases in cerebral oxygen extraction. However, severe increases in whole‐body and brain temperature may increase blood‐brain barrier permeability, potentially leading to cerebral vasogenic edema. The cerebrovascular challenges associated with hyperthermia are of paramount importance for populations with compromised thermoregulatory control—for example, spinal cord injury, elderly, and those with preexisting cardiovascular diseases. © 2015 American Physiological Society. Compr Physiol 5:1345‐1380, 2015.

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Figure 1. Figure 1. A schematic of the average thermal gradients of separate brain regions in 16 monkeys, adapted, with permission, from (). Values are expressed in °C as the difference between simultaneous measures of regional intracranial temperature and the temperature of aortic arterial blood. Anatomical placement is a frontal section (frontal 14.3) in accordance with the stereotaxic atlas of Olszewski (). Note the larger thermal gradients in the deeper regions of the brain, compared to the more superficial regions of the cortex.
Figure 2. Figure 2. Contemporary () static cerebral autoregulatory curve—that is, relationship between mean arterial pressure (MAP) with cerebral blood flow (CBF)—gray scale, and cerebral vascular resistance—red scale. Note the small plateau region (∼5 mmHg) where CBF remains constant, in contrast to the plateau region of 50 to 150 mmHg originally proposed by Lassen (). Further illustrated is the hysteresis of CA, whereby the cerebral vasculature is more effective at buffering increases than decreases in blood pressure. An analysis of 40 studies employing a within‐subject design indicate that the %ΔCBF/%ΔMAP slope is 0.82 ± 0.77 in the hypotensive range, and 0.21 ± 0.47 in the hypertensive range ().
Figure 3. Figure 3. Theoretical change in CMRO2 assuming a temperature coefficient (Q10) of 2—see Eq. 4. Although a simple exponential curve is presented, in vivo data indicate large variability, depending on the hyperthermic or hypothermic condition (e.g., background enzymatic milieu), and whether increasing or decreasing temperature. See text for detail.
Figure 4. Figure 4. Blood flow (Q) response to incremental changes in PaCO2 in the internal carotid artery (ICA) and vertebral artery (VA) as assessed by duplex ultrasound. Note the sigmoidal blood flow response in both the ICA and VA, with greater changes during hyper‐compared to hypocapnia. Figure adapted, with permission, from ().
Figure 5. Figure 5. Relationship between changes in middle cerebral artery velocity (MCAv) and core temperature (Tcore—left panel), partial pressure of end‐tidal CO2 (PETCO2—middle panel), and mean arterial pressure (MAP—right panel) from the 17 studies detailed in Table 1. All data derived during supine passive heat stress. Simple linear regressions exemplify the relationship between level of heat stress and reduction in MCAv (left panel) that is best explained by reductions in PETCO2 (middle panel). The lack of relationship between MCAv may reflect the variability in blood pressure measures while hyperthermic (), efficacious cerebral autoregulation (), and/or the blanketing influence of hypocapnia ().
Figure 6. Figure 6. Regional blood flow variation during mild passive heat stress (+1.0°C rectal temperature) assessed with pseudocontinuous arterial spin labeling magnetic resonance imaging. Hyperthermic = HT (blue bars); Normothermic = NC (green bars). Areas with red pointing arrows denote significant changes in blood flow. Reprinted from (), with permission.
Figure 7. Figure 7. Changes in MCAv and PCAv (left and right top panels, respectively) and blood flow in the ICA and VA (left and right bottom panels, respectively) to a 2.0°C increase in esophageal temperature during passive supine heating with and without end‐tidal CO2 corrected to baseline levels (PETCO2 clamped and PETCO2 unclamped, respectively). Dashed lines indicate mean data. Note that restoring PETCO2 to baseline levels abolishes the reduction in cerebral blood flow in most vessels measured. Although restoring PETCO2 was associated with a significant 4‐mmHg increase in MAP, these data clearly indicate a prominent role for arterial blood CO2 regulation of CBF during supine passive heat stress. Data adapted, with permission, from ().
Figure 8. Figure 8. Tolerance probability to graded lower body negative pressure (LBNP) up to 100 mmHg, while heat stressed (+1.5°C gastrointestinal temperature: dashed line; whole body heating day (WBH day)) and normothermic (solid line; NT day.). Note the significant reduction in tolerance to lower‐body negative pressure while heat stressed. This reduction is primarily attributed to inadequate preservation of MAP and, therefore, cerebral perfusion pressure (see text for discussion). Figure adapted, with permission, from ().
Figure 9. Figure 9. Blood flow (Q) response in the internal carotid artery (ICA), vertebral artery (VA), and external carotid artery (ECA) during progressive cycling to 80% of maximum. The reduction in ICA flow while VA flow continued to rise from 60% to 80% exercise intensity is potentially explained by the progressive increase in ECA flow. That is, because the ECA and ICA are both branches from the common carotid artery, an increase in ECA that is not compensated by proportional increases in common carotid flow, will inherently reduce ICA flow. See text for discussion. Figure adapted, with permission, from ().
Figure 10. Figure 10. Global cerebral blood flow (CBF; bottom panel), cerebral oxygen delivery (DO2; middle panel), and cerebral O2 extraction fraction (OEF top panel) before (pre‐Indo) and after (post‐Indo) administration of indomethacin (1.2 mg/kg). Indomethacin reduced CBF and in turn cerebral oxygen delivery by ∼30%, which was compensated by a ∼30% increase in oxygen extraction fraction. Middle solid line represents mean data from the four subject data points. Figure adapted, with permission, from ().
Figure 11. Figure 11. Illustration of the three functional barriers between the blood and brain. (A) The blood‐brain barrier (BBB) is found at the cerebral capillary endothelial cells. Tight junctions between endothelial cells limit paracellular passage of molecules larger than 400 to 500 Da. The BBB is the largest surface area for exchange in the brain, and is in closest contact to the parenchymal cells (no cell is further than ∼25 μm from a capillary). Heat stress opens the BBB by degradation of the tight‐junction proteins and increased vesicular/transport protein activity (see Fig. 13). (B) The blood‐CSF barrier is found at the choroid plexuses of the fourth, third, and lateral ventricles. Unlike the BBB, the endothelium of the capillaries in the choroid plexus is fenestrated. The blood‐CSF barrier is made up from tight junctions connecting the cuboidal choroid plexus cells. Tight junctions of the choroid plexus cells may also be compromised by heat stressed, evidenced by albumin staining of the ventricles following severe exposure to environmental heating in rats (). (C) The arachnoid barrier envelopes the entire brain located internal to the dura mater and consists of several layers of epithelial cells. Tight junctions, preventing paracellular passage, connect the innermost layer of epithelial cells. Although the arachnoid barrier is avascular, the arachnoid villi project into the sagittal sinus (not depicted), allowing CSF that is circulated in the subarachnoid space to drain out of the brain.
Figure 12. Figure 12. Percent change in cerebral water content in young rats from control throughout progressive heat stress via exposure to 38°C air temperature. Exposure for 4‐h generated rectal temperatures (Tre) of >+3.5°C (<42°C absolute), and significant increases in cerebral water content. Figure adapted, with permission, from ().
Figure 13. Figure 13. Putative schematic illustration of the blood‐brain barrier under heat stress. Breakdown of the tight‐junctions lead to increased passage of water‐soluble agents (including leukocytes and large proteins—e.g. albumin), while increased intracellular cationization from calcium influx increase vesicular transport. Increased protein transport activity may also directly result from increased tissue temperature. Candidate mediators include; (A) bradykinin via increasing intracellular leukocyte migration when acting on the astrocytes, or increasing intracellular calcium when acting on the B2 receptors of the endothelium, and (B) substance P, 5‐HT, and histamine via increasing prostaglandin release from the astrocytes, or by acting directly on the endothelial (via H2 receptors for histamine). Other potential mediators include increased free‐radical production/decreased removal, chiefly the interactions of nitric oxide and superoxide anon. See text for detail.
Figure 14. Figure 14. Integrative model of cerebrovascular changes to progressive passive heat stress. In the healthy human, Increases in core temperature of less than 1°C generally proffer little changes to the cerebrovascular. Thereafter, hyperventilation reduces the arterial partial pressure of CO2 (PaCO2), causing cerebral vasoconstriction and reductions in cerebral blood flow (CBF). Reductions in mean arterial pressure and potential increases in intracranial pressure with severe heat stress eventually yield reductions in cerebral perfusion pressure (CPP), causing further reductions in CBF. The cerebral metabolic rate of oxygen (CMRO2) progressively increases, attributed to the inherent biological response to temperature changes (Q10 effect). Although the attenuated CBF reduces cerebral oxygen delivery (DO2), the maintenance of CMRO2 is accomplished by proportional increases in oxygen extraction fraction (OEF) [up to a point; e.g., OEF will be at a maximum (∼70%) at ∼50 reduction in CBF].


Figure 1. A schematic of the average thermal gradients of separate brain regions in 16 monkeys, adapted, with permission, from (). Values are expressed in °C as the difference between simultaneous measures of regional intracranial temperature and the temperature of aortic arterial blood. Anatomical placement is a frontal section (frontal 14.3) in accordance with the stereotaxic atlas of Olszewski (). Note the larger thermal gradients in the deeper regions of the brain, compared to the more superficial regions of the cortex.


Figure 2. Contemporary () static cerebral autoregulatory curve—that is, relationship between mean arterial pressure (MAP) with cerebral blood flow (CBF)—gray scale, and cerebral vascular resistance—red scale. Note the small plateau region (∼5 mmHg) where CBF remains constant, in contrast to the plateau region of 50 to 150 mmHg originally proposed by Lassen (). Further illustrated is the hysteresis of CA, whereby the cerebral vasculature is more effective at buffering increases than decreases in blood pressure. An analysis of 40 studies employing a within‐subject design indicate that the %ΔCBF/%ΔMAP slope is 0.82 ± 0.77 in the hypotensive range, and 0.21 ± 0.47 in the hypertensive range ().


Figure 3. Theoretical change in CMRO2 assuming a temperature coefficient (Q10) of 2—see Eq. 4. Although a simple exponential curve is presented, in vivo data indicate large variability, depending on the hyperthermic or hypothermic condition (e.g., background enzymatic milieu), and whether increasing or decreasing temperature. See text for detail.


Figure 4. Blood flow (Q) response to incremental changes in PaCO2 in the internal carotid artery (ICA) and vertebral artery (VA) as assessed by duplex ultrasound. Note the sigmoidal blood flow response in both the ICA and VA, with greater changes during hyper‐compared to hypocapnia. Figure adapted, with permission, from ().


Figure 5. Relationship between changes in middle cerebral artery velocity (MCAv) and core temperature (Tcore—left panel), partial pressure of end‐tidal CO2 (PETCO2—middle panel), and mean arterial pressure (MAP—right panel) from the 17 studies detailed in Table 1. All data derived during supine passive heat stress. Simple linear regressions exemplify the relationship between level of heat stress and reduction in MCAv (left panel) that is best explained by reductions in PETCO2 (middle panel). The lack of relationship between MCAv may reflect the variability in blood pressure measures while hyperthermic (), efficacious cerebral autoregulation (), and/or the blanketing influence of hypocapnia ().


Figure 6. Regional blood flow variation during mild passive heat stress (+1.0°C rectal temperature) assessed with pseudocontinuous arterial spin labeling magnetic resonance imaging. Hyperthermic = HT (blue bars); Normothermic = NC (green bars). Areas with red pointing arrows denote significant changes in blood flow. Reprinted from (), with permission.


Figure 7. Changes in MCAv and PCAv (left and right top panels, respectively) and blood flow in the ICA and VA (left and right bottom panels, respectively) to a 2.0°C increase in esophageal temperature during passive supine heating with and without end‐tidal CO2 corrected to baseline levels (PETCO2 clamped and PETCO2 unclamped, respectively). Dashed lines indicate mean data. Note that restoring PETCO2 to baseline levels abolishes the reduction in cerebral blood flow in most vessels measured. Although restoring PETCO2 was associated with a significant 4‐mmHg increase in MAP, these data clearly indicate a prominent role for arterial blood CO2 regulation of CBF during supine passive heat stress. Data adapted, with permission, from ().


Figure 8. Tolerance probability to graded lower body negative pressure (LBNP) up to 100 mmHg, while heat stressed (+1.5°C gastrointestinal temperature: dashed line; whole body heating day (WBH day)) and normothermic (solid line; NT day.). Note the significant reduction in tolerance to lower‐body negative pressure while heat stressed. This reduction is primarily attributed to inadequate preservation of MAP and, therefore, cerebral perfusion pressure (see text for discussion). Figure adapted, with permission, from ().


Figure 9. Blood flow (Q) response in the internal carotid artery (ICA), vertebral artery (VA), and external carotid artery (ECA) during progressive cycling to 80% of maximum. The reduction in ICA flow while VA flow continued to rise from 60% to 80% exercise intensity is potentially explained by the progressive increase in ECA flow. That is, because the ECA and ICA are both branches from the common carotid artery, an increase in ECA that is not compensated by proportional increases in common carotid flow, will inherently reduce ICA flow. See text for discussion. Figure adapted, with permission, from ().


Figure 10. Global cerebral blood flow (CBF; bottom panel), cerebral oxygen delivery (DO2; middle panel), and cerebral O2 extraction fraction (OEF top panel) before (pre‐Indo) and after (post‐Indo) administration of indomethacin (1.2 mg/kg). Indomethacin reduced CBF and in turn cerebral oxygen delivery by ∼30%, which was compensated by a ∼30% increase in oxygen extraction fraction. Middle solid line represents mean data from the four subject data points. Figure adapted, with permission, from ().


Figure 11. Illustration of the three functional barriers between the blood and brain. (A) The blood‐brain barrier (BBB) is found at the cerebral capillary endothelial cells. Tight junctions between endothelial cells limit paracellular passage of molecules larger than 400 to 500 Da. The BBB is the largest surface area for exchange in the brain, and is in closest contact to the parenchymal cells (no cell is further than ∼25 μm from a capillary). Heat stress opens the BBB by degradation of the tight‐junction proteins and increased vesicular/transport protein activity (see Fig. 13). (B) The blood‐CSF barrier is found at the choroid plexuses of the fourth, third, and lateral ventricles. Unlike the BBB, the endothelium of the capillaries in the choroid plexus is fenestrated. The blood‐CSF barrier is made up from tight junctions connecting the cuboidal choroid plexus cells. Tight junctions of the choroid plexus cells may also be compromised by heat stressed, evidenced by albumin staining of the ventricles following severe exposure to environmental heating in rats (). (C) The arachnoid barrier envelopes the entire brain located internal to the dura mater and consists of several layers of epithelial cells. Tight junctions, preventing paracellular passage, connect the innermost layer of epithelial cells. Although the arachnoid barrier is avascular, the arachnoid villi project into the sagittal sinus (not depicted), allowing CSF that is circulated in the subarachnoid space to drain out of the brain.


Figure 12. Percent change in cerebral water content in young rats from control throughout progressive heat stress via exposure to 38°C air temperature. Exposure for 4‐h generated rectal temperatures (Tre) of >+3.5°C (<42°C absolute), and significant increases in cerebral water content. Figure adapted, with permission, from ().


Figure 13. Putative schematic illustration of the blood‐brain barrier under heat stress. Breakdown of the tight‐junctions lead to increased passage of water‐soluble agents (including leukocytes and large proteins—e.g. albumin), while increased intracellular cationization from calcium influx increase vesicular transport. Increased protein transport activity may also directly result from increased tissue temperature. Candidate mediators include; (A) bradykinin via increasing intracellular leukocyte migration when acting on the astrocytes, or increasing intracellular calcium when acting on the B2 receptors of the endothelium, and (B) substance P, 5‐HT, and histamine via increasing prostaglandin release from the astrocytes, or by acting directly on the endothelial (via H2 receptors for histamine). Other potential mediators include increased free‐radical production/decreased removal, chiefly the interactions of nitric oxide and superoxide anon. See text for detail.


Figure 14. Integrative model of cerebrovascular changes to progressive passive heat stress. In the healthy human, Increases in core temperature of less than 1°C generally proffer little changes to the cerebrovascular. Thereafter, hyperventilation reduces the arterial partial pressure of CO2 (PaCO2), causing cerebral vasoconstriction and reductions in cerebral blood flow (CBF). Reductions in mean arterial pressure and potential increases in intracranial pressure with severe heat stress eventually yield reductions in cerebral perfusion pressure (CPP), causing further reductions in CBF. The cerebral metabolic rate of oxygen (CMRO2) progressively increases, attributed to the inherent biological response to temperature changes (Q10 effect). Although the attenuated CBF reduces cerebral oxygen delivery (DO2), the maintenance of CMRO2 is accomplished by proportional increases in oxygen extraction fraction (OEF) [up to a point; e.g., OEF will be at a maximum (∼70%) at ∼50 reduction in CBF].
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Anthony R. Bain, Lars Nybo, Philip N. Ainslie. Cerebral Vascular Control and Metabolism in Heat Stress. Compr Physiol 2015, 5: 1345-1380. doi: 10.1002/cphy.c140066