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Limitation of Heat Tolerance

J. R. S. Hales, R. W. Hubbard, S. L. Gaffin

10.1002/cphy.cp040115

Source: Supplement 14: Handbook of Physiology, Environmental Physiology

Originally published: 1996

Published online: January 2011

Full Article on Wiley Online Library



Abstract

The sections in this article are:

1 Occurrence and Diagnosis of Heatstroke
2 Principal Systemic Responses to or Effects of Severe Heat Stress
2.1 Observations on Heatstroke Patients
2.2 Experimental Observations
2.3 Hormones
3 Proposed Systemic Mechanisms Responsible for Heat Tolerance Limitation
3.1 Breakdown of Thermolytic Mechanisms
3.2 Critical Body Temperatures
3.3 Cardiopulmonary Malfunction
3.4 Conflicts with Cardiovascular Stability
4 Role of Endotoxins in Heatstroke
4.1 The Gastrointestinal Tract as a Source of Toxic Agents
4.2 Leakage of Intestinal Lipopolysaccharide
4.3 Hypothesis
4.4 Pathophysiology of Lipopolysaccharide
4.5 Heatstroke and Lipopolysaccharide
4.6 Lipopolysaccharide in Sports Medicine
4.7 Therapeutic Implications
5 Cellular and Molecular Perspectives of Heat Tolerance
5.1 Membrane Blebbing
5.2 Psychrophiles, Mesophiles, and Thermophiles
5.3 Cellular Heat Death and Membrane Fluidity
5.4 Local Anesthetics and Membrane Fluidity
5.5 Leaks, Pumps, and Energy Metabolism
5.6 Hyperthermia and Measurement of Intracellular Ions
5.7 Apophysis and Other Mechanisms of Cell Death
5.8 Temperature and Endocrine Effects
5.9 Hypokalemia and Heatstroke
5.10 Hyperthermia, Lactate, and Acid–Base Balance
5.11 Heat Shock and Protein Synthesis
6 Factors Modifying Heat Tolerance
6.1 Exercise
6.2 Fitness
6.3 Hypohydration
6.4 Heat Acclimation
6.5 Very Young Age and Old Age
6.6 Drugs Modifying Heat Tolerance
7 Critical Techniques
7.1 The Fundamental Experimental Approach
7.2 Temperature Interpretation
7.3 Choice of Animal Model
7.4 Elucidation of Reflexogenic Pathways
7.5 Measurement of Blood Flow
8 Conclusion
Figure 1. Figure 1.

Decreased skin capillary blood flow rate induced by severe hyperthermia in conscious baboons. At greater than 2°C rise, blood flow declined in all vascular beds compared to those at 1.5–2°C (Tso = Ttorso). From Hales 204, compiled from data of Hales et al. 215, with permission.
Figure 2. Figure 2.

Cardiovascular responses during exercise (between arrows) in humans approaching exhaustion. TPR = total peripheral resistance; RA‐MP = right atrial mean pressure; AoBP = aortic blood pressure; CBV = central blood volume; SV = stroke volume; s = skin; r = rectal; b = blood. From Rowell et al. 467, with permission.
Figure 3. Figure 3.

Cardoivascular response in humans at rest warmed with a water‐perfused suit. Ts = skin temperature; Tblood = blood temperature; FBF = forearm blood flow (representing skin). From Rowell 462, with permission.
Figure 4. Figure 4.

Redistribution of cardiac output in conscious sheep during exposure to an environment of 40°C dry‐bulb and 38°C wet‐bulb temperature. Normothermia: resting in thermoneutral environment with normal body temperatures (rectal temperature ≈ 39.5°C). Moderate hyperthermia: at the peak of rapid shallow panting with Δ rectal temperature ≈ 1°C. Severe hyperthermia: near maximal panting with Δ rectal temperature ≈ 2.5°C. Note that cardiac output, represented by circled area, did not change. From Hales 202, compiled from data of Hales 198,200, with permission.
Figure 5. Figure 5.

Changes in total, central, and systemic blood volume of anesthetized dogs during hyperthermia (mean ± SE). From Miki et al. 370, with permission.
Figure 6. Figure 6.

Brain stem evoked potentials in heatstroke patients. Upper: Component waves (No, Po, Na, Pa, Nb; I, III, V) of mid‐latency responses (MLRs) and brain stem auditory evoked responses (BAERs), recorded on admission of heatstroke patients and postcooling. Note: (1) flattening (F) of Pa wave of MLRs on admission, (2) reversibility of Pa wave postcooling (patient recovered), (3) normal BAERs on admission and postcooling. Lower: As above. Note: (1) Loss of MLRs on admission, not reversible postcooling, in a deeply comatose patient who died. (2) Normal BAERs. From Mustafa et al. 388, with permission.
Figure 7. Figure 7.

Sphering of erythrocytes, conspicuous in all collapsed runners (lower) and not detectable in healthy runners (upper). From Hales et al. 217, with permission.
Figure 8. Figure 8.

Decreases in work rate (M, metabolic heat production) and increases in fatigue (Traction) of an exercising goat each time hypothalamic temperature (THypo) oscillated toward 43°C with extracerebral core temperature (TPaor, paraaortic temperature) artificially controlled at 40°C. REHL = respiratory evaporative heat loss. From Caputa et al. 81, with permission.
Figure 9. Figure 9.

Work done (kg · m) vs. rate of heat storage (°C/min) for rats of different weights exercised to exhaustion at different temperatures and effects of several experimental manipulations on work heat storage relationship. Data compiled from Hubbard et al. 244,251, Durkot et al. 117 and Matthew et al. 365. Each experimental group of rats is connected to its control by a broken line. A. = atropine, D = diazepam, and PH = physostigmine administered prior to running 365 as was 2,4‐DNP (dinitrophenol; 146). Low K+ represents a group of rats made hypokalemic from a low K+ diet. From Hubbard et al. 247,254, with permission.
Figure 10. Figure 10.

Proposed scheme of the interacting sequence of events occurring from the beginning of exposure to a hot environment to death from heatstroke. Arrows indicate increased (↑) or decreased (↓) parameter, but note, for example, in the eighth line, ↑ ↑ SkBF & V shows that skin blood flow and volume are well above control levels but are reduced compared with ↑ ↑ ↑ in the fifth line. “Cellular” box includes, for example, 80%–90% protein inhibition, synthesis of HSPs, and increased (150%–200%) membrane ion flux rate. BF = blood flow; CO = cardiac output; CBV = central blood volume; CVP = central venous pressure; DIC = disseminated intravascular coagulation; el = electrolytes; Fl = fluids; kid = kidney; M = muscle; PBV = peripheral blood volume; Sk = skin; spl = splanchnic; TBV = total blood volume; Tc = core temperature; V = volume. Modified from Hales 207, with permission.
Figure 11. Figure 11.

Changes in nervous electrical activity evoked by heating body skin of anesthetized paralyzed rabbits. Cutaneous (Sympath. left ear) and visceral (N. splanchn.) sympathetic activity expressed as millimeter recorder deflection integrated over 30 s periods; temperature of skin (Tright ear), rectum (Tre), and plate on which the animal lay (Tplate), and mean arterial pressure (Pmar). From Riedel et al. 450, with permission.
Figure 12. Figure 12.

Relationship between greater splanchnic nerve activity (SNA) and core temperature recorded to nearest whole degree for anesthetized rats exposed to ambient temperature of 38°C. *Significantly different from 37°C. From Gisolfi et al. 170, with permission.
Figure 13. Figure 13.

Progressively rising forearm vascular conductance (FVC) due to body warming, can be partly reversed by lower‐body negative pressure (LBNP) in humans. HR = heart rate; TR = rectal temperature; Ts = skin temperature; MAP = mean arterial pressure. From Johnson et al. 267, with permission.
Figure 14. Figure 14.

Total extremity skin capillary (excluding arteriovenous anastomotic) blood flow of conscious sheep in a thermoneutral environment, then at two stages of severe heat stress during approximately 3 h ambient heating, namely, when CVP was minimal (core temperature ≈ 41°C) and just before termination of stress when core temperature ≈ 42°C. NORMAL = normal responses with no treatment besides heat. CONSTANT CVP = changes of CVP prevented by i.v. Macrodex. LOWERED CVP = measurements repeated with CVP artificially lowered for about 3 min using a pneumatic cuff on the inferior vena cava. Modified from Hales et al. 213, with permission.
Figure 15. Figure 15.

Relation of forearm venous volume (at 30 cm H2O venous pressure) to LBNP at 37°, 28°, and 18°C (mean ± SE). From Tripathi et al. 562, with permission.
Figure 16. Figure 16.

Changes in forearm venous volume and compliance (FVC) (mean ± SE) with CVP (mean ± SE) at 28° and 37°C. *Significantly different from control (P < 0.01). From Tripathi et al. 559, with permission.
Figure 17. Figure 17.

Responses (mean ± SE) to environmental heating at 46°C in unanesthetized rats. Exposure time is represented as percentage of total time (% time) to account for differences in duration of individual experiments. Mean arterial pressure (MAP) and heart rate (HR) represent changes from control levels. Resistance levels are indicated by percent (%) changes from control levels; Tc = core temperature; SMA = superior mesenteric artery; LIA = left iliac artery; ECA = external caudal artery. From Kregel et al. 313, with permission.
Figure 18. Figure 18.

Demonstration of improved heat tolerance due to endotoxin tolerance in rats. Thermal area = temperature x time. From DuBose et al. 113, with permission.
Figure 19. Figure 19.

Cardiovascular parameters and LPS concentrations in portal and systemic circulations of anesthetized monkeys during heat stress. The rise in plasma LPS appeared first in the portal vein but not in the systemic circulation until 10–15 min later. However, the drop in natural anti‐LPS IgG occurred at about 39°–40°C. Since the drop can best be explained by consumption of specific antibodies by LPS, this suggests that LPS leaks out slowly from the intestines at temperatures as low as 39°–40°C. From Gathiram et al. 160, with permission.
Figure 20. Figure 20.

% mortality and % severe blebbing of G1 cells heated at 45.5°C. Solid circles represent % mortality, open squares represent % of cells with diameter of largest bleb to diameter of cell body ratio ≥ 0.45. Redrawn from Borelli et al. 49, with permission.
Figure 21. Figure 21.

Representative data for surviving fraction of linolenic (L) and oleic (O) acid substituted E. coli K1060 grown at 25°, 37°, or 41°C and heated at 47°C for times up to 4 h. At each temperature a greater proportion of cells enriched in membrane‐hardening saturated fatty acid (oleic) survived. From Yatvin 607, with permission.
Figure 22. Figure 22.

Representative data showing surviving fraction of E coli K1060 cells grown at 37°C in presence of oleic acid and either heated only or heated in presence of 10 mM procaine–HCl for up to 5 h at 47°C. Similar results were obtained when cells were held at either 46° or 48°C. The membrane‐fluidizing agent Procaine reduced survival. From Yatvin 607, with permission.
Figure 23. Figure 23.

A scheme representing membrane organization of GAPD and PGK in association with the Na+‐K+ pump in human red blood cells. Addition of substrates in this figure (PGA = phosphoglycerate; GAPG = glyceraldehyde‐3‐phosphate dehydrogenase; PGK = phosphoglycerate kinase) generates ATP within the membrane pool that is preferentially utilized by the Na+‐K+ ATPase. Redrawn from Gick et al. 167 and Proverbio et al. 441. From Hubbard 241, with permission.
Figure 24. Figure 24.

Heat resistance of skeletal muscle of white rat. Abscissa; temperature of heating; ordinate; retention time of electric excitability in minutes, logarithmic scale. Note the more rapid decline in excitability above 41°C. From Alexandrov 5, taken from Skholl 526, with permission.
Figure 25. Figure 25.

Effect of hyperthermia (42°C,•) compared with control cells (37°C,○) on 42K uptake by exponentially growing CHO cells. Since net flux at 15 min was zero, the observed elevation in 42K+ uptake must have been balanced by an equal K+ efflux through other pathway(s). From Stevenson et al. 534, with permission.
Figure 26. Figure 26.

Arrhenius plot of active K+ influx and Na+ influx in Reuber H35 hepatoma cells. Active K+ influx (o) and Na+ influx (•) were measured using 86Rb+ and 22Na+, respectively, as radioactive tracers. Cells were incubated at the appropriate temperature for 15 min before flux measurements were started. Note stability and constant stoichiometry of Na+‐K+ pump up to 43°C. Points, mean values of nine measurements from three different experiments. From Boonstra et al. 47, with permission.
Figure 27. Figure 27.

Effect of heat shock on active K+ influx and K+ efflux in Reuber H35 hepatoma cells. Top, active K+ influx or Na+‐K+ pump‐mediated K+ influx was measured using 86Rb+ as radioactive tracer. Ouabain was used at a final concentration of 5 mM and added 1 min prior to addition of tracer. Points, means; bars, SE (n = 3). Bottom, K+ efflux measured using 42K+ as radioactive tracer. Note rapidity of rises and falls of K+ influx and efflux with heating and cooling. Efflux rate constant was calculated using equations from a one‐compartment system; K+ influx and efflux measured at 37°C or at 42°C as indicated. Points, means; bars, SE (n = 3). From Boonstra et al. 47, with permission.
Figure 28. Figure 28.

Loss of Na+‐K+ ATPase activity in HeLa cells treated at 45°C. Monolayer cultures in 80 oz bottles were treated at 45°C for various time periods by immersion in a water bath. Cells were then washed, collected, and assayed for ATPase (bars = SD). Note 50% loss of activity in approx. 4–5 min at 45°C. From Burdon and Cutmore 70, with permission.
Figure 29. Figure 29.

Recovery of Na+‐K+ ATPase activity at 37°C after heat treatment of HeLa cells at 45°C. Monolayer cultures were subjected to heat treatment at 45°C for 10 min. They were returned to normal growth temperature of 37°C and cultures were removed, washed, and assayed for ATPase at various times. Resulting activities (•) expressed as % of Na+ −K+ ATPase activity in untreated control cells grown at 37°C; relative enzyme activity in cells treated at 45°C for 10 min but then incubated for 2 h at 37°C in presence of cycloheximide (25 μg/ml) (□) or actinomycin D (2 μ/ml) (○) (bars = SD). From Burdon and Cutmore 70, with permission.
Figure 30. Figure 30.

Ouabain‐sensitive ATP‐hydrolysing activity of crude membrane preparations isolated from mouse fibroblast LM cells at different temperatures; data points are mean values of four experiments. These isolated membrane‐bound Na+‐K+ ATPase pumps were stable up to 46°C. Compare with Fig. 28. From Ruifrok et al. 471, with permission.
Figure 31. Figure 31.

Ouabain‐sensitive K+ influx, measured with 86Rb+ as tracer during incubation at 37°C and 44°C. Kinetic measurements made at 37°C in nonheated cells and at 44°C after various hyperthermic treatments at 44°C. Data points are mean ± SEM of three separate experiments. Values corrected for loss by cell lysis. From Ruifrok et al. 472, with permission.
Figure 32. Figure 32.

Rectal temperature (n = 4), mean venous lactate concentrations, and minute ventilatory volumes (n = 6) of six subjects during prolonged exhaustive treadmill running under three thermal conditions: normal, hyperthermal, and hypothermal. Treadmill speed was identical under each condition, set at approximately 70% of each subject's maximum aerobic power. From MacDougall et al. 349, with permission.
Figure 33. Figure 33.

Effect of heat shock on protein synthesis in Reuber H35 hepatoma cells, measured using [3H] leucine. Rate of incorporation calculated from a 30 min period. Data expressed as percentage of control values (mean ± SE, n = 3). From Boonstra et al. 47, with permission.
Figure 34. Figure 34.

Solute leakage in 10 ml of water at 45°C with or without 2 h preincubation of seedlings at 40°C. At indicated times, amounts of amino acids and soluble sugars in medium were estimated and conductivity measured. Open symbols with and filled symbols without preincubation. Heat pretreatment reduced the amount of cell damage, resulting in reduced losses of sugars, amino acids, and ions. From Lin et al. 333, with permission.
Figure 35. Figure 35.

Mean hemolymph Na+ (—) or K+ (—) of ten 10°C and ten 25°C acclimated crayfish as a function of time of exposure at 32°C. (Vertical bars = ± SEM). From Bowler 52, with permission.
Figure 36. Figure 36.

Heat load from passive heating compared with heat plus exercise necessary to cause death in rats. Note increased mortality of exercised rats at equivalent heat loads. From Hubbard et al. 245, with permission.
Figure 37. Figure 37.

(A) Dose–response curves of percentage of surviving rats with serum AST (formerly SGOT) levels in excess of 1,000 IU/liter vs. maximum core temperatures of run‐exhausted or restrained‐heated rats. Values in insert represent mean ± SE of core temperature at indicated percentages. CT50 for run rats was significantly different from CT50 for heated rats (P < 0.025). Redrawn from Hubbard et al. 244, with permission. (B) Dose–response curves of percent mortality vs. temperature on admission in human heatstroke patients. In A, note increased morbidity (enzyme release) in exercising at equivalent Tc's. In B, note the similarity to motality data in exertional vs. classical heatstroke in humans. Data recalculated by method of Reed and Muench from sources indicated in insert. Redrawn from Hubbard et al. 248, with permission.
Figure 38. Figure 38.

Percent mortality 24 h after work‐heat tolerance test in sedentary and trained rats exhausted at indicated range of colonic temperatures (Tc). Above each point is the number of rats represented. Exercise training improved tolerance to lethal hyperthermia. From Fruth and Gisolfi 150, with permission.


Figure 1.

Decreased skin capillary blood flow rate induced by severe hyperthermia in conscious baboons. At greater than 2°C rise, blood flow declined in all vascular beds compared to those at 1.5–2°C (Tso = Ttorso). From Hales 204, compiled from data of Hales et al. 215, with permission.



Figure 2.

Cardiovascular responses during exercise (between arrows) in humans approaching exhaustion. TPR = total peripheral resistance; RA‐MP = right atrial mean pressure; AoBP = aortic blood pressure; CBV = central blood volume; SV = stroke volume; s = skin; r = rectal; b = blood. From Rowell et al. 467, with permission.



Figure 3.

Cardoivascular response in humans at rest warmed with a water‐perfused suit. Ts = skin temperature; Tblood = blood temperature; FBF = forearm blood flow (representing skin). From Rowell 462, with permission.



Figure 4.

Redistribution of cardiac output in conscious sheep during exposure to an environment of 40°C dry‐bulb and 38°C wet‐bulb temperature. Normothermia: resting in thermoneutral environment with normal body temperatures (rectal temperature ≈ 39.5°C). Moderate hyperthermia: at the peak of rapid shallow panting with Δ rectal temperature ≈ 1°C. Severe hyperthermia: near maximal panting with Δ rectal temperature ≈ 2.5°C. Note that cardiac output, represented by circled area, did not change. From Hales 202, compiled from data of Hales 198,200, with permission.



Figure 5.

Changes in total, central, and systemic blood volume of anesthetized dogs during hyperthermia (mean ± SE). From Miki et al. 370, with permission.



Figure 6.

Brain stem evoked potentials in heatstroke patients. Upper: Component waves (No, Po, Na, Pa, Nb; I, III, V) of mid‐latency responses (MLRs) and brain stem auditory evoked responses (BAERs), recorded on admission of heatstroke patients and postcooling. Note: (1) flattening (F) of Pa wave of MLRs on admission, (2) reversibility of Pa wave postcooling (patient recovered), (3) normal BAERs on admission and postcooling. Lower: As above. Note: (1) Loss of MLRs on admission, not reversible postcooling, in a deeply comatose patient who died. (2) Normal BAERs. From Mustafa et al. 388, with permission.



Figure 7.

Sphering of erythrocytes, conspicuous in all collapsed runners (lower) and not detectable in healthy runners (upper). From Hales et al. 217, with permission.



Figure 8.

Decreases in work rate (M, metabolic heat production) and increases in fatigue (Traction) of an exercising goat each time hypothalamic temperature (THypo) oscillated toward 43°C with extracerebral core temperature (TPaor, paraaortic temperature) artificially controlled at 40°C. REHL = respiratory evaporative heat loss. From Caputa et al. 81, with permission.



Figure 9.

Work done (kg · m) vs. rate of heat storage (°C/min) for rats of different weights exercised to exhaustion at different temperatures and effects of several experimental manipulations on work heat storage relationship. Data compiled from Hubbard et al. 244,251, Durkot et al. 117 and Matthew et al. 365. Each experimental group of rats is connected to its control by a broken line. A. = atropine, D = diazepam, and PH = physostigmine administered prior to running 365 as was 2,4‐DNP (dinitrophenol; 146). Low K+ represents a group of rats made hypokalemic from a low K+ diet. From Hubbard et al. 247,254, with permission.



Figure 10.

Proposed scheme of the interacting sequence of events occurring from the beginning of exposure to a hot environment to death from heatstroke. Arrows indicate increased (↑) or decreased (↓) parameter, but note, for example, in the eighth line, ↑ ↑ SkBF & V shows that skin blood flow and volume are well above control levels but are reduced compared with ↑ ↑ ↑ in the fifth line. “Cellular” box includes, for example, 80%–90% protein inhibition, synthesis of HSPs, and increased (150%–200%) membrane ion flux rate. BF = blood flow; CO = cardiac output; CBV = central blood volume; CVP = central venous pressure; DIC = disseminated intravascular coagulation; el = electrolytes; Fl = fluids; kid = kidney; M = muscle; PBV = peripheral blood volume; Sk = skin; spl = splanchnic; TBV = total blood volume; Tc = core temperature; V = volume. Modified from Hales 207, with permission.



Figure 11.

Changes in nervous electrical activity evoked by heating body skin of anesthetized paralyzed rabbits. Cutaneous (Sympath. left ear) and visceral (N. splanchn.) sympathetic activity expressed as millimeter recorder deflection integrated over 30 s periods; temperature of skin (Tright ear), rectum (Tre), and plate on which the animal lay (Tplate), and mean arterial pressure (Pmar). From Riedel et al. 450, with permission.



Figure 12.

Relationship between greater splanchnic nerve activity (SNA) and core temperature recorded to nearest whole degree for anesthetized rats exposed to ambient temperature of 38°C. *Significantly different from 37°C. From Gisolfi et al. 170, with permission.



Figure 13.

Progressively rising forearm vascular conductance (FVC) due to body warming, can be partly reversed by lower‐body negative pressure (LBNP) in humans. HR = heart rate; TR = rectal temperature; Ts = skin temperature; MAP = mean arterial pressure. From Johnson et al. 267, with permission.



Figure 14.

Total extremity skin capillary (excluding arteriovenous anastomotic) blood flow of conscious sheep in a thermoneutral environment, then at two stages of severe heat stress during approximately 3 h ambient heating, namely, when CVP was minimal (core temperature ≈ 41°C) and just before termination of stress when core temperature ≈ 42°C. NORMAL = normal responses with no treatment besides heat. CONSTANT CVP = changes of CVP prevented by i.v. Macrodex. LOWERED CVP = measurements repeated with CVP artificially lowered for about 3 min using a pneumatic cuff on the inferior vena cava. Modified from Hales et al. 213, with permission.



Figure 15.

Relation of forearm venous volume (at 30 cm H2O venous pressure) to LBNP at 37°, 28°, and 18°C (mean ± SE). From Tripathi et al. 562, with permission.



Figure 16.

Changes in forearm venous volume and compliance (FVC) (mean ± SE) with CVP (mean ± SE) at 28° and 37°C. *Significantly different from control (P < 0.01). From Tripathi et al. 559, with permission.



Figure 17.

Responses (mean ± SE) to environmental heating at 46°C in unanesthetized rats. Exposure time is represented as percentage of total time (% time) to account for differences in duration of individual experiments. Mean arterial pressure (MAP) and heart rate (HR) represent changes from control levels. Resistance levels are indicated by percent (%) changes from control levels; Tc = core temperature; SMA = superior mesenteric artery; LIA = left iliac artery; ECA = external caudal artery. From Kregel et al. 313, with permission.



Figure 18.

Demonstration of improved heat tolerance due to endotoxin tolerance in rats. Thermal area = temperature x time. From DuBose et al. 113, with permission.



Figure 19.

Cardiovascular parameters and LPS concentrations in portal and systemic circulations of anesthetized monkeys during heat stress. The rise in plasma LPS appeared first in the portal vein but not in the systemic circulation until 10–15 min later. However, the drop in natural anti‐LPS IgG occurred at about 39°–40°C. Since the drop can best be explained by consumption of specific antibodies by LPS, this suggests that LPS leaks out slowly from the intestines at temperatures as low as 39°–40°C. From Gathiram et al. 160, with permission.



Figure 20.

% mortality and % severe blebbing of G1 cells heated at 45.5°C. Solid circles represent % mortality, open squares represent % of cells with diameter of largest bleb to diameter of cell body ratio ≥ 0.45. Redrawn from Borelli et al. 49, with permission.



Figure 21.

Representative data for surviving fraction of linolenic (L) and oleic (O) acid substituted E. coli K1060 grown at 25°, 37°, or 41°C and heated at 47°C for times up to 4 h. At each temperature a greater proportion of cells enriched in membrane‐hardening saturated fatty acid (oleic) survived. From Yatvin 607, with permission.



Figure 22.

Representative data showing surviving fraction of E coli K1060 cells grown at 37°C in presence of oleic acid and either heated only or heated in presence of 10 mM procaine–HCl for up to 5 h at 47°C. Similar results were obtained when cells were held at either 46° or 48°C. The membrane‐fluidizing agent Procaine reduced survival. From Yatvin 607, with permission.



Figure 23.

A scheme representing membrane organization of GAPD and PGK in association with the Na+‐K+ pump in human red blood cells. Addition of substrates in this figure (PGA = phosphoglycerate; GAPG = glyceraldehyde‐3‐phosphate dehydrogenase; PGK = phosphoglycerate kinase) generates ATP within the membrane pool that is preferentially utilized by the Na+‐K+ ATPase. Redrawn from Gick et al. 167 and Proverbio et al. 441. From Hubbard 241, with permission.



Figure 24.

Heat resistance of skeletal muscle of white rat. Abscissa; temperature of heating; ordinate; retention time of electric excitability in minutes, logarithmic scale. Note the more rapid decline in excitability above 41°C. From Alexandrov 5, taken from Skholl 526, with permission.



Figure 25.

Effect of hyperthermia (42°C,•) compared with control cells (37°C,○) on 42K uptake by exponentially growing CHO cells. Since net flux at 15 min was zero, the observed elevation in 42K+ uptake must have been balanced by an equal K+ efflux through other pathway(s). From Stevenson et al. 534, with permission.



Figure 26.

Arrhenius plot of active K+ influx and Na+ influx in Reuber H35 hepatoma cells. Active K+ influx (o) and Na+ influx (•) were measured using 86Rb+ and 22Na+, respectively, as radioactive tracers. Cells were incubated at the appropriate temperature for 15 min before flux measurements were started. Note stability and constant stoichiometry of Na+‐K+ pump up to 43°C. Points, mean values of nine measurements from three different experiments. From Boonstra et al. 47, with permission.



Figure 27.

Effect of heat shock on active K+ influx and K+ efflux in Reuber H35 hepatoma cells. Top, active K+ influx or Na+‐K+ pump‐mediated K+ influx was measured using 86Rb+ as radioactive tracer. Ouabain was used at a final concentration of 5 mM and added 1 min prior to addition of tracer. Points, means; bars, SE (n = 3). Bottom, K+ efflux measured using 42K+ as radioactive tracer. Note rapidity of rises and falls of K+ influx and efflux with heating and cooling. Efflux rate constant was calculated using equations from a one‐compartment system; K+ influx and efflux measured at 37°C or at 42°C as indicated. Points, means; bars, SE (n = 3). From Boonstra et al. 47, with permission.



Figure 28.

Loss of Na+‐K+ ATPase activity in HeLa cells treated at 45°C. Monolayer cultures in 80 oz bottles were treated at 45°C for various time periods by immersion in a water bath. Cells were then washed, collected, and assayed for ATPase (bars = SD). Note 50% loss of activity in approx. 4–5 min at 45°C. From Burdon and Cutmore 70, with permission.



Figure 29.

Recovery of Na+‐K+ ATPase activity at 37°C after heat treatment of HeLa cells at 45°C. Monolayer cultures were subjected to heat treatment at 45°C for 10 min. They were returned to normal growth temperature of 37°C and cultures were removed, washed, and assayed for ATPase at various times. Resulting activities (•) expressed as % of Na+ −K+ ATPase activity in untreated control cells grown at 37°C; relative enzyme activity in cells treated at 45°C for 10 min but then incubated for 2 h at 37°C in presence of cycloheximide (25 μg/ml) (□) or actinomycin D (2 μ/ml) (○) (bars = SD). From Burdon and Cutmore 70, with permission.



Figure 30.

Ouabain‐sensitive ATP‐hydrolysing activity of crude membrane preparations isolated from mouse fibroblast LM cells at different temperatures; data points are mean values of four experiments. These isolated membrane‐bound Na+‐K+ ATPase pumps were stable up to 46°C. Compare with Fig. 28. From Ruifrok et al. 471, with permission.



Figure 31.

Ouabain‐sensitive K+ influx, measured with 86Rb+ as tracer during incubation at 37°C and 44°C. Kinetic measurements made at 37°C in nonheated cells and at 44°C after various hyperthermic treatments at 44°C. Data points are mean ± SEM of three separate experiments. Values corrected for loss by cell lysis. From Ruifrok et al. 472, with permission.



Figure 32.

Rectal temperature (n = 4), mean venous lactate concentrations, and minute ventilatory volumes (n = 6) of six subjects during prolonged exhaustive treadmill running under three thermal conditions: normal, hyperthermal, and hypothermal. Treadmill speed was identical under each condition, set at approximately 70% of each subject's maximum aerobic power. From MacDougall et al. 349, with permission.



Figure 33.

Effect of heat shock on protein synthesis in Reuber H35 hepatoma cells, measured using [3H] leucine. Rate of incorporation calculated from a 30 min period. Data expressed as percentage of control values (mean ± SE, n = 3). From Boonstra et al. 47, with permission.



Figure 34.

Solute leakage in 10 ml of water at 45°C with or without 2 h preincubation of seedlings at 40°C. At indicated times, amounts of amino acids and soluble sugars in medium were estimated and conductivity measured. Open symbols with and filled symbols without preincubation. Heat pretreatment reduced the amount of cell damage, resulting in reduced losses of sugars, amino acids, and ions. From Lin et al. 333, with permission.



Figure 35.

Mean hemolymph Na+ (—) or K+ (—) of ten 10°C and ten 25°C acclimated crayfish as a function of time of exposure at 32°C. (Vertical bars = ± SEM). From Bowler 52, with permission.



Figure 36.

Heat load from passive heating compared with heat plus exercise necessary to cause death in rats. Note increased mortality of exercised rats at equivalent heat loads. From Hubbard et al. 245, with permission.



Figure 37.

(A) Dose–response curves of percentage of surviving rats with serum AST (formerly SGOT) levels in excess of 1,000 IU/liter vs. maximum core temperatures of run‐exhausted or restrained‐heated rats. Values in insert represent mean ± SE of core temperature at indicated percentages. CT50 for run rats was significantly different from CT50 for heated rats (P < 0.025). Redrawn from Hubbard et al. 244, with permission. (B) Dose–response curves of percent mortality vs. temperature on admission in human heatstroke patients. In A, note increased morbidity (enzyme release) in exercising at equivalent Tc's. In B, note the similarity to motality data in exertional vs. classical heatstroke in humans. Data recalculated by method of Reed and Muench from sources indicated in insert. Redrawn from Hubbard et al. 248, with permission.



Figure 38.

Percent mortality 24 h after work‐heat tolerance test in sedentary and trained rats exhausted at indicated range of colonic temperatures (Tc). Above each point is the number of rats represented. Exercise training improved tolerance to lethal hyperthermia. From Fruth and Gisolfi 150, with permission.

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Article Title: Limitation of Heat Tolerance
 

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J. R. S. Hales, R. W. Hubbard, S. L. Gaffin. Limitation of Heat Tolerance. Compr Physiol 2011, Supplement 14: Handbook of Physiology, Environmental Physiology: 285-355. First published in print 1996. doi: 10.1002/cphy.cp040115