HEAT STROKE AND HYPERTHERMIA IN MARATHON RUNNERS C. H. Wyndham Chamber of Mines Research Laboratories Marshalltown, Transvaal South Africa University of the Witwatersrand Johannesburg, South Africa
Introduction Sir Adolphe Abrahams in his article on “Athletics” in the 1950 edition of the British Encyclopaedia of Medical Practice states: I am of the opinion that in healthy subjects the only serious potential risk to life from violent exercise is heat stroke-a danger well exhibited by examples I have seen of alarming collapse and, on one occasion, death. The correct precaution would be to prohibit the race in circumstances in which an occurrence might be expected-a moisture laden atmosphere, a following wind and the early afternoon of a day with a shade temperature of 85” F (29.Y C) or higher.
Sir Adolphe could not have expressed his warning about heat stroke in clearer terms, but, in spite of his warning, sports administrators still continue to arrange marathon running and cycling events in climatic conditions that are dangerous because of the risks of heat stroke. Prevention is better than cure, but for prevention to be effective there must be a good understanding of both the circumstances that lead to the condition and its pathophysiology.
Heat Exchange Studies in my laboratory l - 4 have demonstrated convincingly that Vo2 is highly correlated with gross body mass during both walking and running. In a study of six males varying in weight from 63 to 102 kg, correlation coefficients of between r = 0.85 and r = 0.99 were found for walking at 3.2, 4.8, and 8.0 km/hr, and running at 8.0, 9.7, 11.3, and 12.9 km/hr (FIGURES1 & 2). A similar, statistically significant correlation of r = 0.7 1 between Po* and body mass was found for six marathon runners when running at 18 km/hr, the speed needed to complete. a standard marathon in reasonable time. The physical 1 and characteristics and Vo, mnx values of these six runners are given in TABLE are compared with those of two sub-4-minute milers and 80 fit young Army trainees. All of these studies were carried out in Johannesburg, which is at an altitude 0.f 1,763 m above sea level. The V,),values of the six marathon runners when running at 18 km/ hr are 2, together with the percentages of mnx, the blood lactates, given in TABLE and the heart rates at rest and after 30 minutes of running. The pol varied from 2.6 I/min in the 50 kg to 3.5 Vmin in the 72-kg man. All of the percent-
voa
128
Wyndham: Heat Stroke and Hyperthermia
129
TABLE1 PHYSICAL AND PHYSIOLOGICAL CHARACTERISTICS OF ENDURANCE ATHLETES
Subjects
vo,m,x
Age (years)
Height (cm)
Weight (kg)
(literdmin)
(ml/min.kg)
22 21 18 20 20 34 22.5
175.6 182.2 164.9 176.5 183.5 177.8 176.7
61.05 63.65 51.05 68.90 71.55 65.45 63.61
3.87 3.67 3.42 4.28 4.40 4.09 3.95
63.39 57.66 66.99 62.15 6 1S O 62.49 62.36
19 24
174.4 183.4
62.00 65.35
4.32 4.13
69.68 63.19
17-19
174.4
66.30
3.15
47.21
Marathon runners
Mou. Mo. H. P.
Me. S.
Mean Sub-4-minute milers Z.
L. A rm y recruits
80 men
ages of V02mnxused while running a t 18 k m / h r were in excess of 7 5 % . One would expect, therefore, that some of these runners would be in anaerobic metabolism. Judged by the blood lactate levels after 30 minutes of running, this proved to be the case. Blood lactate levels in excess of 60 mg/100 ml were Their heart rates were also found in those runners using 85%-90% of in excess of 180 beats/ min.
v,,,
TABLE2 LACTATERESPONSEOF MARATHONRUNNERSAFTER 30 MINUTESAT 18 km/hr*
as % of maximum Vo,
Subjects Mou.
Speed (km/hr)
Lactate (mg/100 ml)
Rest
10.86 71.85 9.90 13.12 9.34 17.27 13.72 68.25 13.31 18.29 7.67 27.37
18
Mo.
Rest 18
H.
Rest 18
Rest
P.
18
Me.
Rest 18
S.
Rest 18
*
10 miles per hour.
PO,
(litedmin)
-
-
3.54
91.4
-
-
2.98 2.58
80.5 75.4
Heart Rate (beatdmin) 180 156
162
-
-
-
3.66
85.5
182
-
-
-
3.42 3.38
77.7
178
-
-
82.7
189
Annals New York Academy of Sciences
130
60
I
I
70
eo
I 90
I 100
B o d y m a s s (kg)
FIGURE1. Oxygen consumption in relation to body mass and walking or running speed for six males. The high levels of QO2 recorded in these men when running at 18 km/hr would be associated with high rates of heat production. These would cause their body temperatures to rise to heat stroke levels if the human body did not have a superbly efficient mechanism for ridding itself of waste heat-the evaporation of sweat. If we consider only the heat produced by aerobic metabolism, a 60-kg runner would produce 900 kcal (3,780 kJ) per hour, and if
Wyndham: Heat Stroke and Hyperthermia
131
he had no means of getting rid of waste heat his body temperature would rise to about 45" C after 30 minutes of running at 18 km/hr. All of the heat produced could, however, be dissipated by sweating 1,500 ml/hr of water and evaporating it. Do marathon runners sweat sufficiently for these high rates of evaporation from their body surfaces? Observations by my laboratory5 on 30 marathon runners in a 30-km race on a cool day (the dry bulb temperature rose from 9 ° C at 8 : O O AM to 17" C at noon and relative humidity fell from 90% to 30% ) showed that there is a significant correlation ( r = 0.90) between sweat rates and body masses, irrespective of the places in which the runners finished the race (FIGURE 3). From the regression line in FIGURE 3 one can estimate that a 60-kg runner would sweat at a rate of 1,250 ml/hr. Similar high rates of
4 I
2
I
3
I
6 I
4
1
8 I
m.p.h. I
kmlhr 10 I
6
1
12 I
7
1
8
Speed FIGURE2. Oxygen intake at different speeds of walking and running of men of different weights.
Annals New York Academy of Sciences
132
f. X
X
I 1 SO
I
1
60
I
I
I
B o d y weight
I
1
80
70
(kg)
FIGURE3. Sweat loss in terms of body weight for marathon runners. sweating were shown by Costill et aL6 Therefore, provided thc humidity of the air is sufficiently low to allow all of the sweat to evaporate, marathon runners probably are able to sweat fast enough to remain in thermal balance with the high rates of aerobic heat production. The runners who might get into difficulty in this regard are those who develop a high level of anaerobic metabolism. A few examples of such runners were shown in TABLE 2. Anaerobic metabolism adds materially to the production of waste heat, and runners in anaerobic metabolism might not be able to sweat at sufficiently high rates to maintain thermal balance. There are problems associated with the high rates of sweating needed to maintain thermal balance in marathon running. If the runners do not drink at a sufficient rate to replace the water losses from sweating, they may develop severe dehydration. Dehydration materially affects the ability of the human body to regulate body temperature. This is well shown in studies from my lab~ratory.~Those runners who drank sufficient water to keep their level of dehydration below 3% of body mass had rectal temperatures of around 38.5" C at the end of the 30-km race, which is normal (FIGURE 4). However, in those men who did not drink sufficient water to keep below this safe level of dehydration, there was a significant positive correlation between the rectal temperature and the extent of dehydration. From the regression line fitted to these data one
Wyndham: Heat Stroke and Hyperthermia
133
can predict that runners who develop more than 5 % dehydration would be likely to finish the race with rectal temperatures around 41" C. Interestingly enough, this prediction agrees well with Pugh's observation: on a marathon runner: On a warm day in the United Kingdom he sweated at a rate of 1,800 ml/hr and developed a rectal temperature of 41.1" C in association with 6.7% dehydration. H y perthermia
Body temperature is invariably raised above 38" C during a marathon run,5* and, if the runner is dehydrated, the rectal temperature may rise above 40" C. This poses the problem of whether body temperatures raised to such levels for prolonged periods of at least 2 hours in a standard marathon can cause damage to cells in vital organs. Evidence of damage to vital organs is revealed either in elevated serum enzyme levels or .in deranged function of an organ. McKechnie et al.s made a detailed study of ECG changes, serum enzymes, and blood potassium in 20 marathon runners immediately after a race and, in some, a fortnight later. They did not find any evidence of myocardial damage in the ECG. The mean values of the serum enzymes GOT, GPT, and LDH were all elevated above normal (TABLE 3 ) . Abnormal values were found in 8, 13, and 8 of the 20 riinners for GOT, GPT, and LDH, respectively. In two runners GOT was above 100 units, in one of the two GPT was above 100 units, and in both LDH was above 700 units. Serum aldolase was raised above
X
X
e
.
x
X
+.
2
3
4
5
P e r c e n t a g e water deficit
FIGURE 4. Rectal temperature in relation to percentage water deficit for marathon
runners.
134
Annals New York Academy of Sciences
normal in all 20 runners and was still above normal in four of the six runners who returned for further study two weeks later. Serum potassium levels were raised in all 20 runners. Rose et uLV measured total LDH, total CPK, and LDH isoenzymes in six men after a standard marathon. Significant increases were found in total LDH and total CPK and in the LDH isoenzymes -3, -4, and -5 but not in the isoenzymes -1 and -2, the fractions found in cardiac muscle and the kidney. No measurements were made of rectal temperature or of blood lactate and pH by McKechnie et al. or Rose et al. Hence we have no evidence of whether hyperthermia or metabolic acidosis played any part in the cell damage that was revealed by the raised serum enzyme levels. In an attempt to determine whether prolonged hyperthermia, without metabolic acidosis, causes cell damage,. my laboratory lo exercised I5 physically conditioned and heat-acclimatized men for 4 hours at a Vo, of 1.32 Vmin in hot and humid conditions. This heat stress and exercise condition caused their rectal temperatures to rise to 3 9 ' 4 0 " C for most of the period of the experiment. The rate of exercise was chosen to give a v0,of well below 50% of the men's VOlmorvalues in order to ensure that they would not be in anaerobic metabolism and develop metabolic acidosis. TABLE3
SERUM ENZYMES IN HEATSTROKE VICTIMS, MARATHON RUNNERS, AND
GOT GPT
LDH
44
20
Normal Men
Marathon Runners
36 24 308
60 50 436
NORMALS
40 Heat Stroke Victims
Time after Heat Stroke 0 hr 48 hr 96 hr 518 112 2058
1007 843 3283
210 349 656
Control studies were made at the same work rate and for the same period in cool conditions and resulted in rectal temperature rising to a mean of 37.5" C. The serum enzymes GOT, GPT, LDH, and CPK, were significantly higher when the men's rectal temperatures were raised to 39O-40" C than at 37.5" C. The increase in serum enzyme levels in the men with hyperthermia of this order were, however, neither as consistent nor as high as those reported by Kew et al." in heat stroke cases (TABLE 3), nor did the increase persist after the exercise ceased. It seems reasonable to conclude on the available evidence that "physiological" levels of hyperthermia, i.e., rectal temperatures of below 41' C result in only mild and transient damage to cells in the human body. However, as shown ip the earlier section, marathon runners commonly run at above 75% of Yo,mar and some develop marked metabolic acidosis as indicated by elevated blood lactate values. The combination of mild hyperthermia and metabolic acidosis would be expected to result in more severe cell damage than hyperthermia alone, and it is probably this combination of insults to the cell that caused such high serum enzyme values in two of the runners studied by McKechnie et al. These were the two men with GOT and G P T values of
Wyndham: Heat Stroke and Hyperthermia
135
over 100 units and LDH values of over 700 units. None of these runners apparently had any signs and symptoms of damage to vital organs but, in my view, it is merely a greater degree and extent of damage to vital organs that leads to the syndrome of nephropathy described by Dancaster et al. (1969) in two runners in a Comrades Marathon, an 80-km race between Durban and Pietermaritzburg in Natal, South Africa. Both of these cases had severe, transient renal damage and will be described in detail in the section on heat strokc. The question may well be asked what criteria should be used to distinguish the case with hyperthermia and evidence of cell damage, as shown by elevated serum enzymes and/or deranged function of a vital organ, from a case of genuine heat stroke. Two criteria are useful in this regard. One is that there should be definite evidence of cerebral involvement for the diagnosis of heat stroke to be made. This may, on the one hand, be cerebral depression with collapse into unconsciousness with stupor or coma or cerebral stimulation with great irritability, attacks on helpers, and, finally, convulsions or fits. The other criterion is that the serum enzyme levels should be markedly elevated above normal and should continue to rise for the first 48 hours after the collapse. Difficulties arise when the collapse into unconsciousness is of short duration or the evidence of cerebral stimulation is relatively mild, such as mere irritability of the subject. It is in these cases that serial measurements of serum enzymes are of great help in arriving at a correct diagnosis. Heat Stroke A number of heat stroke cases have been reported as a result of prolonged, intense physical exercise in warm and hot humid weather. There was the case of the British marathon runner at the Empire Games in Canada in 1955. A fatal case of heat stroke occurred during the Tour de France in 195912 in a cyclist who had drugged himself with amphetamines. There were three nonfatal cases in the Danish cyclists in the hot humid weather during the Olympic Games in Rome in 1960.':' Heat stroke should be suspected if a marathon is run on a warm day and a runner develops some of the following premonitory symptoms and signs. He may become irritable and aggressive and may even assault anyone who tries to remonstrate with him or help him; or he may display emotional instability with hysterical weeping; or he may be apathetic and fail to respond to questioning. In this phase the subject may be disorientated in time and space. He may run the wrong way around the track and be unaware of the time of the day. He may develop an unsteady gait and a glassy stare. Finally he may collapse and become unconscious or he may have a convulsive seizure. His skin may be hot and dry or he may sweat profusely. His pulse may be rapid and feeble or it may be full and bounding. If a marathon runner has any of these premonitory symptoms and signs and collapses, heat stroke should be suspected and an immediate rectal temperature measurement should be made. If the temperature is over 41" C, and especially if above 45" C, heat stroke should be diagnosed and emergency treatment started. The first priority is to cool the man until the rectal temperature falls to 38°C. If there is a delay in the diagnosis and the man arrives in hospital after 2 or more hours without being cooled with a rectal temperature of, say, 45" C the chances of a fatal outcome are about 7:10.'" The best way of
136
Annals New
York Academy of Sciences
cooling the man is to spray water over his body and blow air over it with a strong fan.15 Generally these resources are not available and in that case water should be thrown over the man's body and the body kept wet. Spectators should be asked to fan the man with a large piece of cardboard. The man should not be piaced in a bath of ice-water as advocated by some heat physiologists. This method of treating heat stroke is dangerous because it is very difficult to control the extent of fall in rectal temperature and circulatory shock may occur, with fatal results, during the rewarming phase. Prompt cooling of suspected heat stroke cases is the most effective way of preventing damage to vital organs. It is important to take a sample of blood from such cases as soon as possible and again at 48 and 96 hours after the collapse for the measurement of certain serum enzymes such as GOT, GPT, LDH, and CPK. TABLE 3 contains levels of these serum enzymes in samples of men at rest, after marathon running, and with heat stroke. The heat stroke values are at the time of admission to hospital and at 48 and 96 hours after admission. In definite cases of heat stroke all of these serum enzymes are markedly elevated on admission to hospital, continue to rise for the first 48 hours, and then fall but still remain above normal limits after 96 hours according to Kew et The extent of elevation of serum enzyme levels and the length of time they are elevated are useful indicators of the amount of damage to vital organs, such as the kidney, and also are an aid to prognosis.ll The first priority in the treatment of a suspected case of heat stroke is cooling the patient until the rectal temperature reaches 38" C. However, this may take an hour or more and during this period it is important to take steps to prevent damage to vital organs by two of the common complications of heat stroke: These are circulatory collapse and metabolic acidosis. When these complications occur the cell is subject to three simultaneous insults. They are cell anoxia due to poor local circulation, a low pH, and hyperthermia, which increases cell metabolism. Circulatory shock is best treated by intravenous fluids, which must be given sufficiently rapidly to restore the blood pressure as soon as possibly to avoid the renal vascular shut-down that accompanies circulatory shock. Severe metabolic acidosis occurs in some cases of heat stroke. Wyndham et al.l.l reported a case with a pH of 7.280, a P ~ . of~ ,18 mmHg, a base excess of -14.5 mEq/l and standard bicarbonate of 14.4 mEq/l. Cases with severe metabolic acidosis improve dramatically when treated with intravenous bicarbonate solutions. Up to 30 g of bicarbonate is sometimes required to restore acid/ base balance. Where prompt cooling of a suspected case of heat stroke is not carried out damage may occur to certain target organs. These are the kidney,l6 the heart,Ir the liver,'" and the brain." Kidney damage with acute renal failure is a common complication of heat stroke in circumstances where men exercise vigorously in warm or hot conditions such as army recruits undergoing hard physical exercise in warm weather or miners working physically in hot and humid mines.lG*19* *" Scheir et coined the apt phrase of "nephropathy associated with heat stress and exercise" for this syndrome. Most of the patients with this condition who survive the acute stage make a complete recovery, but Kew et ~ 1 found . ~ that ~ four of their forty cases of heat stroke developed chronic interstitial nephritis. Relatively few cases of this syndrome have been reported in marathon runners. A notable exception is the occurrence of two cases during a Comrades Marathon (80 km) reported by Dancaster et al.23 One case was a runner of
Wyndham: Heat Stroke and Hyperthermia
137
38 years of age who suffered a severe collapse during the race. He was in a stupor for some while after the collapse and passed loose stools and vomited during this phase. He passed no urine for 48 hours after the collapse and he had a blood pressure of 200/ 130 and a BUN of 186 mg/ 100 mi? He gradually improved on intravenous therapy and conservative treatment over the next 2 weeks, and his blood pressure, BUN, and renal function returned to normal. The other case felt very ill and was dizzy after the race. He also had an episode of diarrhea. He passed only 400 ml of urine in the next four days and during this period his blood pressure rose to 160/90 and his BUN to 176 mg/100 ml. His serum GOT was 135 units; GPT, 180 units; and LDH, 1,500 units. On intravenous therapy he developed a massive diuresis of 4,000 ml on the fifth day and went on to recover completely. It is comforting to know that if heat stroke is suspected, if the diagnosis is made sufficiently early, and if proper treatment is instituted (particularly immediate body cooling), then the chances of a fatal outcome are very low. The key issue is that the sports medical officer and track officials should be on the lookout for the occurrence of heat stroke if a marathon is run on a warm and humid day. The sports medical officer should be armed with a rectal thermometer and should not hesitate to make a rectal temperature measurement if a runner behaves abnormally and particularly if he collapses. Recommendations
24
(1 ) Running and cycling marathons should not be run in warm and humid weather. If the climatic condition over the period in which the race would be run exceeds 25" C wet bulb - globe temperature in the week prior to the race the runners are at risk from heat stroke and officials should be warned to look out for abnormal behavior on the part of the runners. If wet bulb - globe temperature exceeds 28' C the race should be called off. (2) Adequate amounts of water should be available at least at 20-minute intervals and competitors should be warned of the dangers of dehydration and be encouraged to drink at least a cupful of water (300 ml) at*:se intervals. ( 3 ) In the event of a runner behaving abnormally and collapsing, a rectal temperature measurement should be made, and if it is above 41" C, the runner should be treated for heat stroke. He should be cooled immediately, and if there are clinical signs and symptoms of stock and/or metabolic acidosis, appropriate treatment should be started &iring the period of cooling. (4) A sample of blood should be taken as soon as possible and sent to a clinical pathology laboratory for estimation of the serum enzymes GOT, GPT, LDH, and CPK. ( 5 ) If the diagnosis of heat stroke is confirmed by the serum enzyme measurements, then the runner should be admitted to hospital and a careful watch kept on renal function.
References 1. WYNDHAM, C. H. & A. J. A.
HEYNS. 1969. Determinants of oxygen consumption and maximum oxygen intake of Bantu and Causasian males. Intern Z. Angew Physiol. 2'1: 51-75.
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Annals New York Academy of Sciences
2. WYNDHAM, C. H., N. B. STRYDOM, C. H. VAN GRAAN, A. J. VAN RENSBURG, C. G. ROGERS, J. S. GRAYSON & W. H. VAN DER WALT.1971. Walk or jog for health. 1. The energy c6sts of walking and running at different speeds. S. Afr. Med. J. 45: 50-53. 3. WYNDHAM, c. H., W. H. VAN DER WALT,A. J. VAN RENSBURG & c. G. ROGERS. 1971. The influence of body weight on energy expenditure during walking on a road and a treadmill. Intern. Z. Angew Physiol. 29: 285-292. 4. VAN DER WALT, W. H. & C. H. WYNDHAM.1973. An equation for the prediction of the energy expenditure of walking and running. J. Appl. Physiol. 34(3): 559-563. 5. WYNDHAM, C. H. & N. B. STRYDOM.1969. The danger of an inadequate water intake during marathon running. S. Afr. Med. J. 43: 893-896. 6. COSTILL,D .L., W. F. KAMMER & A. FISHER.1970. Fluid ingestion during distance running. Arch. Environ. Health 21: 520-525. 7. PUGH,L. G. C. E. 1967. Rectal temperatures, weight losses and sweat rates in marathon running. J. Appl. Physiol. 23(3): 347-352. 8. MCKECHNIE,J. K., W. P. LEARY,0. M. JOUBERT.1967. Some electrocardiographic and biochemical changes in marathon runners. S. Afr. Med. J. 41: 722-725. 9. ROSE, L. I., J. E. BROUSSER & K. H. COOPER.1970. Serum enzymes after marathon running. J. Appl. Physiol. 29(3): 355-357. C. H., M. C. KEW, R. KOK, I. BERSOHN& N. B. STRYDOM.1974. 10. WYNDHAM, 11. 12. 13. 14.
Serum enzyme changes in unacclimatised and acclimatised men under severe heat stress. J. Apl. Physiol. 37(5): 695-698. KEw, M. C., I. BERSOHN & H. C. SEFTEL. 1971. The diagnostic and prognostic significance of serum enzyme changes in heat stroke. Trans. R. Soc. Trop. Med. Hyg. 65: 325-330. BERNHEIM, I. T. & J. N. Cox. 1960. Coup de chaleur et intoxication amphetamine chez un sportiff. Schweiz Med. Wochenscher. 9 0 322-331. SHIBOLET, S., M. C. LANCESTER & Y. DANOU.1976. Heat stroke: A review. Aviat. Space Environ. Med. 47(3): 280-301. WYNDHAM, C. H. 1966. A survey of research initiated by the Chamber of Mines into the clinical aspects of heat stroke. Proc. Mine Med. Officers Assoc.
4 6 68-80. 15. WYNDHAM, C. H., N. B. STRYDOM,M. H. COOKE,J. F. MORRISON, J. S. MATITZ, P. W. FLEMING & J. S. WARD. 1959. Methods of cooling subjects with hyperpyrexia. J. Appl. Physiol. 14: 771-776. & N. W. LEVIN. 1967. The effects of heat stroke on 16. KEW, M. C., C. ABRAHAMS the function and structure of the kidney. Quart. J. Med. 36: 277-300. & I. BERSOHN.1969. The heart in heat stroke. 17. KEW, M. C., R. B. K. TUCKER Amer. Heart J. 77: 324-335. 18. KEW, M. C., I. BERSOHN & H. C. SEFTEL. 1970. Liver damage in heat stroke. Amer. J. Med. 49: 192-202. S.. R. COLL& T. GILAT. 1967. Heat stroke: Its clinical picture and 19. SHIBOLET, mechanisms in thirty-six cases. Quart. J. Med. 3 6 524-548. 20. VERTEL,R. M. & T. P. KNOCHEL.1967. Acute renal failure due to heat injury. Amer. J. Med. 43: 435-451. 21. SCHIER, R. W., J. HONO& H. I. KELLER. 1967. Nephropathy associated with heat stress and exercise. Ann. Intern. Med. 67: 350-376. & H. C. SEFTEL. 1970. Chronic interstitial nephritis 22. KEW, M. C., C. ABRAHAMS as a consequence of heat stroke. Quart. J. Med. 39: 189-199. C. P., W. C. DUCKWORTH & C. J. ROPER. 1969. Nepropathy in 23. DANCASTER, marathon runners. S. Afr. Med. J. 43: 758-760. 24. WYNDHAM, C. H. & N. B. STRYDOM.1972. Physical exercise in high temperature. I n Sportmedizen. W. Hollman, Ed. : 131-150. Springer-Verlag. Berlin.
Introduction Sir Adolphe Abrahams in his article on “Athletics” in the 1950 edition of the British Encyclopaedia of Medical Practice states: I am of the opinion that in healthy subjects the only serious potential risk to life from violent exercise is heat stroke-a danger well exhibited by examples I have seen of alarming collapse and, on one occasion, death. The correct precaution would be to prohibit the race in circumstances in which an occurrence might be expected-a moisture laden atmosphere, a following wind and the early afternoon of a day with a shade temperature of 85” F (29.Y C) or higher.
Sir Adolphe could not have expressed his warning about heat stroke in clearer terms, but, in spite of his warning, sports administrators still continue to arrange marathon running and cycling events in climatic conditions that are dangerous because of the risks of heat stroke. Prevention is better than cure, but for prevention to be effective there must be a good understanding of both the circumstances that lead to the condition and its pathophysiology.
Heat Exchange Studies in my laboratory l - 4 have demonstrated convincingly that Vo2 is highly correlated with gross body mass during both walking and running. In a study of six males varying in weight from 63 to 102 kg, correlation coefficients of between r = 0.85 and r = 0.99 were found for walking at 3.2, 4.8, and 8.0 km/hr, and running at 8.0, 9.7, 11.3, and 12.9 km/hr (FIGURES1 & 2). A similar, statistically significant correlation of r = 0.7 1 between Po* and body mass was found for six marathon runners when running at 18 km/hr, the speed needed to complete. a standard marathon in reasonable time. The physical 1 and characteristics and Vo, mnx values of these six runners are given in TABLE are compared with those of two sub-4-minute milers and 80 fit young Army trainees. All of these studies were carried out in Johannesburg, which is at an altitude 0.f 1,763 m above sea level. The V,),values of the six marathon runners when running at 18 km/ hr are 2, together with the percentages of mnx, the blood lactates, given in TABLE and the heart rates at rest and after 30 minutes of running. The pol varied from 2.6 I/min in the 50 kg to 3.5 Vmin in the 72-kg man. All of the percent-
voa
128
Wyndham: Heat Stroke and Hyperthermia
129
TABLE1 PHYSICAL AND PHYSIOLOGICAL CHARACTERISTICS OF ENDURANCE ATHLETES
Subjects
vo,m,x
Age (years)
Height (cm)
Weight (kg)
(literdmin)
(ml/min.kg)
22 21 18 20 20 34 22.5
175.6 182.2 164.9 176.5 183.5 177.8 176.7
61.05 63.65 51.05 68.90 71.55 65.45 63.61
3.87 3.67 3.42 4.28 4.40 4.09 3.95
63.39 57.66 66.99 62.15 6 1S O 62.49 62.36
19 24
174.4 183.4
62.00 65.35
4.32 4.13
69.68 63.19
17-19
174.4
66.30
3.15
47.21
Marathon runners
Mou. Mo. H. P.
Me. S.
Mean Sub-4-minute milers Z.
L. A rm y recruits
80 men
ages of V02mnxused while running a t 18 k m / h r were in excess of 7 5 % . One would expect, therefore, that some of these runners would be in anaerobic metabolism. Judged by the blood lactate levels after 30 minutes of running, this proved to be the case. Blood lactate levels in excess of 60 mg/100 ml were Their heart rates were also found in those runners using 85%-90% of in excess of 180 beats/ min.
v,,,
TABLE2 LACTATERESPONSEOF MARATHONRUNNERSAFTER 30 MINUTESAT 18 km/hr*
as % of maximum Vo,
Subjects Mou.
Speed (km/hr)
Lactate (mg/100 ml)
Rest
10.86 71.85 9.90 13.12 9.34 17.27 13.72 68.25 13.31 18.29 7.67 27.37
18
Mo.
Rest 18
H.
Rest 18
Rest
P.
18
Me.
Rest 18
S.
Rest 18
*
10 miles per hour.
PO,
(litedmin)
-
-
3.54
91.4
-
-
2.98 2.58
80.5 75.4
Heart Rate (beatdmin) 180 156
162
-
-
-
3.66
85.5
182
-
-
-
3.42 3.38
77.7
178
-
-
82.7
189
Annals New York Academy of Sciences
130
60
I
I
70
eo
I 90
I 100
B o d y m a s s (kg)
FIGURE1. Oxygen consumption in relation to body mass and walking or running speed for six males. The high levels of QO2 recorded in these men when running at 18 km/hr would be associated with high rates of heat production. These would cause their body temperatures to rise to heat stroke levels if the human body did not have a superbly efficient mechanism for ridding itself of waste heat-the evaporation of sweat. If we consider only the heat produced by aerobic metabolism, a 60-kg runner would produce 900 kcal (3,780 kJ) per hour, and if
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he had no means of getting rid of waste heat his body temperature would rise to about 45" C after 30 minutes of running at 18 km/hr. All of the heat produced could, however, be dissipated by sweating 1,500 ml/hr of water and evaporating it. Do marathon runners sweat sufficiently for these high rates of evaporation from their body surfaces? Observations by my laboratory5 on 30 marathon runners in a 30-km race on a cool day (the dry bulb temperature rose from 9 ° C at 8 : O O AM to 17" C at noon and relative humidity fell from 90% to 30% ) showed that there is a significant correlation ( r = 0.90) between sweat rates and body masses, irrespective of the places in which the runners finished the race (FIGURE 3). From the regression line in FIGURE 3 one can estimate that a 60-kg runner would sweat at a rate of 1,250 ml/hr. Similar high rates of
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Speed FIGURE2. Oxygen intake at different speeds of walking and running of men of different weights.
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f. X
X
I 1 SO
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60
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B o d y weight
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FIGURE3. Sweat loss in terms of body weight for marathon runners. sweating were shown by Costill et aL6 Therefore, provided thc humidity of the air is sufficiently low to allow all of the sweat to evaporate, marathon runners probably are able to sweat fast enough to remain in thermal balance with the high rates of aerobic heat production. The runners who might get into difficulty in this regard are those who develop a high level of anaerobic metabolism. A few examples of such runners were shown in TABLE 2. Anaerobic metabolism adds materially to the production of waste heat, and runners in anaerobic metabolism might not be able to sweat at sufficiently high rates to maintain thermal balance. There are problems associated with the high rates of sweating needed to maintain thermal balance in marathon running. If the runners do not drink at a sufficient rate to replace the water losses from sweating, they may develop severe dehydration. Dehydration materially affects the ability of the human body to regulate body temperature. This is well shown in studies from my lab~ratory.~Those runners who drank sufficient water to keep their level of dehydration below 3% of body mass had rectal temperatures of around 38.5" C at the end of the 30-km race, which is normal (FIGURE 4). However, in those men who did not drink sufficient water to keep below this safe level of dehydration, there was a significant positive correlation between the rectal temperature and the extent of dehydration. From the regression line fitted to these data one
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can predict that runners who develop more than 5 % dehydration would be likely to finish the race with rectal temperatures around 41" C. Interestingly enough, this prediction agrees well with Pugh's observation: on a marathon runner: On a warm day in the United Kingdom he sweated at a rate of 1,800 ml/hr and developed a rectal temperature of 41.1" C in association with 6.7% dehydration. H y perthermia
Body temperature is invariably raised above 38" C during a marathon run,5* and, if the runner is dehydrated, the rectal temperature may rise above 40" C. This poses the problem of whether body temperatures raised to such levels for prolonged periods of at least 2 hours in a standard marathon can cause damage to cells in vital organs. Evidence of damage to vital organs is revealed either in elevated serum enzyme levels or .in deranged function of an organ. McKechnie et al.s made a detailed study of ECG changes, serum enzymes, and blood potassium in 20 marathon runners immediately after a race and, in some, a fortnight later. They did not find any evidence of myocardial damage in the ECG. The mean values of the serum enzymes GOT, GPT, and LDH were all elevated above normal (TABLE 3 ) . Abnormal values were found in 8, 13, and 8 of the 20 riinners for GOT, GPT, and LDH, respectively. In two runners GOT was above 100 units, in one of the two GPT was above 100 units, and in both LDH was above 700 units. Serum aldolase was raised above
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P e r c e n t a g e water deficit
FIGURE 4. Rectal temperature in relation to percentage water deficit for marathon
runners.
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normal in all 20 runners and was still above normal in four of the six runners who returned for further study two weeks later. Serum potassium levels were raised in all 20 runners. Rose et uLV measured total LDH, total CPK, and LDH isoenzymes in six men after a standard marathon. Significant increases were found in total LDH and total CPK and in the LDH isoenzymes -3, -4, and -5 but not in the isoenzymes -1 and -2, the fractions found in cardiac muscle and the kidney. No measurements were made of rectal temperature or of blood lactate and pH by McKechnie et al. or Rose et al. Hence we have no evidence of whether hyperthermia or metabolic acidosis played any part in the cell damage that was revealed by the raised serum enzyme levels. In an attempt to determine whether prolonged hyperthermia, without metabolic acidosis, causes cell damage,. my laboratory lo exercised I5 physically conditioned and heat-acclimatized men for 4 hours at a Vo, of 1.32 Vmin in hot and humid conditions. This heat stress and exercise condition caused their rectal temperatures to rise to 3 9 ' 4 0 " C for most of the period of the experiment. The rate of exercise was chosen to give a v0,of well below 50% of the men's VOlmorvalues in order to ensure that they would not be in anaerobic metabolism and develop metabolic acidosis. TABLE3
SERUM ENZYMES IN HEATSTROKE VICTIMS, MARATHON RUNNERS, AND
GOT GPT
LDH
44
20
Normal Men
Marathon Runners
36 24 308
60 50 436
NORMALS
40 Heat Stroke Victims
Time after Heat Stroke 0 hr 48 hr 96 hr 518 112 2058
1007 843 3283
210 349 656
Control studies were made at the same work rate and for the same period in cool conditions and resulted in rectal temperature rising to a mean of 37.5" C. The serum enzymes GOT, GPT, LDH, and CPK, were significantly higher when the men's rectal temperatures were raised to 39O-40" C than at 37.5" C. The increase in serum enzyme levels in the men with hyperthermia of this order were, however, neither as consistent nor as high as those reported by Kew et al." in heat stroke cases (TABLE 3), nor did the increase persist after the exercise ceased. It seems reasonable to conclude on the available evidence that "physiological" levels of hyperthermia, i.e., rectal temperatures of below 41' C result in only mild and transient damage to cells in the human body. However, as shown ip the earlier section, marathon runners commonly run at above 75% of Yo,mar and some develop marked metabolic acidosis as indicated by elevated blood lactate values. The combination of mild hyperthermia and metabolic acidosis would be expected to result in more severe cell damage than hyperthermia alone, and it is probably this combination of insults to the cell that caused such high serum enzyme values in two of the runners studied by McKechnie et al. These were the two men with GOT and G P T values of
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over 100 units and LDH values of over 700 units. None of these runners apparently had any signs and symptoms of damage to vital organs but, in my view, it is merely a greater degree and extent of damage to vital organs that leads to the syndrome of nephropathy described by Dancaster et al. (1969) in two runners in a Comrades Marathon, an 80-km race between Durban and Pietermaritzburg in Natal, South Africa. Both of these cases had severe, transient renal damage and will be described in detail in the section on heat strokc. The question may well be asked what criteria should be used to distinguish the case with hyperthermia and evidence of cell damage, as shown by elevated serum enzymes and/or deranged function of a vital organ, from a case of genuine heat stroke. Two criteria are useful in this regard. One is that there should be definite evidence of cerebral involvement for the diagnosis of heat stroke to be made. This may, on the one hand, be cerebral depression with collapse into unconsciousness with stupor or coma or cerebral stimulation with great irritability, attacks on helpers, and, finally, convulsions or fits. The other criterion is that the serum enzyme levels should be markedly elevated above normal and should continue to rise for the first 48 hours after the collapse. Difficulties arise when the collapse into unconsciousness is of short duration or the evidence of cerebral stimulation is relatively mild, such as mere irritability of the subject. It is in these cases that serial measurements of serum enzymes are of great help in arriving at a correct diagnosis. Heat Stroke A number of heat stroke cases have been reported as a result of prolonged, intense physical exercise in warm and hot humid weather. There was the case of the British marathon runner at the Empire Games in Canada in 1955. A fatal case of heat stroke occurred during the Tour de France in 195912 in a cyclist who had drugged himself with amphetamines. There were three nonfatal cases in the Danish cyclists in the hot humid weather during the Olympic Games in Rome in 1960.':' Heat stroke should be suspected if a marathon is run on a warm day and a runner develops some of the following premonitory symptoms and signs. He may become irritable and aggressive and may even assault anyone who tries to remonstrate with him or help him; or he may display emotional instability with hysterical weeping; or he may be apathetic and fail to respond to questioning. In this phase the subject may be disorientated in time and space. He may run the wrong way around the track and be unaware of the time of the day. He may develop an unsteady gait and a glassy stare. Finally he may collapse and become unconscious or he may have a convulsive seizure. His skin may be hot and dry or he may sweat profusely. His pulse may be rapid and feeble or it may be full and bounding. If a marathon runner has any of these premonitory symptoms and signs and collapses, heat stroke should be suspected and an immediate rectal temperature measurement should be made. If the temperature is over 41" C, and especially if above 45" C, heat stroke should be diagnosed and emergency treatment started. The first priority is to cool the man until the rectal temperature falls to 38°C. If there is a delay in the diagnosis and the man arrives in hospital after 2 or more hours without being cooled with a rectal temperature of, say, 45" C the chances of a fatal outcome are about 7:10.'" The best way of
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cooling the man is to spray water over his body and blow air over it with a strong fan.15 Generally these resources are not available and in that case water should be thrown over the man's body and the body kept wet. Spectators should be asked to fan the man with a large piece of cardboard. The man should not be piaced in a bath of ice-water as advocated by some heat physiologists. This method of treating heat stroke is dangerous because it is very difficult to control the extent of fall in rectal temperature and circulatory shock may occur, with fatal results, during the rewarming phase. Prompt cooling of suspected heat stroke cases is the most effective way of preventing damage to vital organs. It is important to take a sample of blood from such cases as soon as possible and again at 48 and 96 hours after the collapse for the measurement of certain serum enzymes such as GOT, GPT, LDH, and CPK. TABLE 3 contains levels of these serum enzymes in samples of men at rest, after marathon running, and with heat stroke. The heat stroke values are at the time of admission to hospital and at 48 and 96 hours after admission. In definite cases of heat stroke all of these serum enzymes are markedly elevated on admission to hospital, continue to rise for the first 48 hours, and then fall but still remain above normal limits after 96 hours according to Kew et The extent of elevation of serum enzyme levels and the length of time they are elevated are useful indicators of the amount of damage to vital organs, such as the kidney, and also are an aid to prognosis.ll The first priority in the treatment of a suspected case of heat stroke is cooling the patient until the rectal temperature reaches 38" C. However, this may take an hour or more and during this period it is important to take steps to prevent damage to vital organs by two of the common complications of heat stroke: These are circulatory collapse and metabolic acidosis. When these complications occur the cell is subject to three simultaneous insults. They are cell anoxia due to poor local circulation, a low pH, and hyperthermia, which increases cell metabolism. Circulatory shock is best treated by intravenous fluids, which must be given sufficiently rapidly to restore the blood pressure as soon as possibly to avoid the renal vascular shut-down that accompanies circulatory shock. Severe metabolic acidosis occurs in some cases of heat stroke. Wyndham et al.l.l reported a case with a pH of 7.280, a P ~ . of~ ,18 mmHg, a base excess of -14.5 mEq/l and standard bicarbonate of 14.4 mEq/l. Cases with severe metabolic acidosis improve dramatically when treated with intravenous bicarbonate solutions. Up to 30 g of bicarbonate is sometimes required to restore acid/ base balance. Where prompt cooling of a suspected case of heat stroke is not carried out damage may occur to certain target organs. These are the kidney,l6 the heart,Ir the liver,'" and the brain." Kidney damage with acute renal failure is a common complication of heat stroke in circumstances where men exercise vigorously in warm or hot conditions such as army recruits undergoing hard physical exercise in warm weather or miners working physically in hot and humid mines.lG*19* *" Scheir et coined the apt phrase of "nephropathy associated with heat stress and exercise" for this syndrome. Most of the patients with this condition who survive the acute stage make a complete recovery, but Kew et ~ 1 found . ~ that ~ four of their forty cases of heat stroke developed chronic interstitial nephritis. Relatively few cases of this syndrome have been reported in marathon runners. A notable exception is the occurrence of two cases during a Comrades Marathon (80 km) reported by Dancaster et al.23 One case was a runner of
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38 years of age who suffered a severe collapse during the race. He was in a stupor for some while after the collapse and passed loose stools and vomited during this phase. He passed no urine for 48 hours after the collapse and he had a blood pressure of 200/ 130 and a BUN of 186 mg/ 100 mi? He gradually improved on intravenous therapy and conservative treatment over the next 2 weeks, and his blood pressure, BUN, and renal function returned to normal. The other case felt very ill and was dizzy after the race. He also had an episode of diarrhea. He passed only 400 ml of urine in the next four days and during this period his blood pressure rose to 160/90 and his BUN to 176 mg/100 ml. His serum GOT was 135 units; GPT, 180 units; and LDH, 1,500 units. On intravenous therapy he developed a massive diuresis of 4,000 ml on the fifth day and went on to recover completely. It is comforting to know that if heat stroke is suspected, if the diagnosis is made sufficiently early, and if proper treatment is instituted (particularly immediate body cooling), then the chances of a fatal outcome are very low. The key issue is that the sports medical officer and track officials should be on the lookout for the occurrence of heat stroke if a marathon is run on a warm and humid day. The sports medical officer should be armed with a rectal thermometer and should not hesitate to make a rectal temperature measurement if a runner behaves abnormally and particularly if he collapses. Recommendations
24
(1 ) Running and cycling marathons should not be run in warm and humid weather. If the climatic condition over the period in which the race would be run exceeds 25" C wet bulb - globe temperature in the week prior to the race the runners are at risk from heat stroke and officials should be warned to look out for abnormal behavior on the part of the runners. If wet bulb - globe temperature exceeds 28' C the race should be called off. (2) Adequate amounts of water should be available at least at 20-minute intervals and competitors should be warned of the dangers of dehydration and be encouraged to drink at least a cupful of water (300 ml) at*:se intervals. ( 3 ) In the event of a runner behaving abnormally and collapsing, a rectal temperature measurement should be made, and if it is above 41" C, the runner should be treated for heat stroke. He should be cooled immediately, and if there are clinical signs and symptoms of stock and/or metabolic acidosis, appropriate treatment should be started &iring the period of cooling. (4) A sample of blood should be taken as soon as possible and sent to a clinical pathology laboratory for estimation of the serum enzymes GOT, GPT, LDH, and CPK. ( 5 ) If the diagnosis of heat stroke is confirmed by the serum enzyme measurements, then the runner should be admitted to hospital and a careful watch kept on renal function.
References 1. WYNDHAM, C. H. & A. J. A.
HEYNS. 1969. Determinants of oxygen consumption and maximum oxygen intake of Bantu and Causasian males. Intern Z. Angew Physiol. 2'1: 51-75.
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2. WYNDHAM, C. H., N. B. STRYDOM, C. H. VAN GRAAN, A. J. VAN RENSBURG, C. G. ROGERS, J. S. GRAYSON & W. H. VAN DER WALT.1971. Walk or jog for health. 1. The energy c6sts of walking and running at different speeds. S. Afr. Med. J. 45: 50-53. 3. WYNDHAM, c. H., W. H. VAN DER WALT,A. J. VAN RENSBURG & c. G. ROGERS. 1971. The influence of body weight on energy expenditure during walking on a road and a treadmill. Intern. Z. Angew Physiol. 29: 285-292. 4. VAN DER WALT, W. H. & C. H. WYNDHAM.1973. An equation for the prediction of the energy expenditure of walking and running. J. Appl. Physiol. 34(3): 559-563. 5. WYNDHAM, C. H. & N. B. STRYDOM.1969. The danger of an inadequate water intake during marathon running. S. Afr. Med. J. 43: 893-896. 6. COSTILL,D .L., W. F. KAMMER & A. FISHER.1970. Fluid ingestion during distance running. Arch. Environ. Health 21: 520-525. 7. PUGH,L. G. C. E. 1967. Rectal temperatures, weight losses and sweat rates in marathon running. J. Appl. Physiol. 23(3): 347-352. 8. MCKECHNIE,J. K., W. P. LEARY,0. M. JOUBERT.1967. Some electrocardiographic and biochemical changes in marathon runners. S. Afr. Med. J. 41: 722-725. 9. ROSE, L. I., J. E. BROUSSER & K. H. COOPER.1970. Serum enzymes after marathon running. J. Appl. Physiol. 29(3): 355-357. C. H., M. C. KEW, R. KOK, I. BERSOHN& N. B. STRYDOM.1974. 10. WYNDHAM, 11. 12. 13. 14.
Serum enzyme changes in unacclimatised and acclimatised men under severe heat stress. J. Apl. Physiol. 37(5): 695-698. KEw, M. C., I. BERSOHN & H. C. SEFTEL. 1971. The diagnostic and prognostic significance of serum enzyme changes in heat stroke. Trans. R. Soc. Trop. Med. Hyg. 65: 325-330. BERNHEIM, I. T. & J. N. Cox. 1960. Coup de chaleur et intoxication amphetamine chez un sportiff. Schweiz Med. Wochenscher. 9 0 322-331. SHIBOLET, S., M. C. LANCESTER & Y. DANOU.1976. Heat stroke: A review. Aviat. Space Environ. Med. 47(3): 280-301. WYNDHAM, C. H. 1966. A survey of research initiated by the Chamber of Mines into the clinical aspects of heat stroke. Proc. Mine Med. Officers Assoc.
4 6 68-80. 15. WYNDHAM, C. H., N. B. STRYDOM,M. H. COOKE,J. F. MORRISON, J. S. MATITZ, P. W. FLEMING & J. S. WARD. 1959. Methods of cooling subjects with hyperpyrexia. J. Appl. Physiol. 14: 771-776. & N. W. LEVIN. 1967. The effects of heat stroke on 16. KEW, M. C., C. ABRAHAMS the function and structure of the kidney. Quart. J. Med. 36: 277-300. & I. BERSOHN.1969. The heart in heat stroke. 17. KEW, M. C., R. B. K. TUCKER Amer. Heart J. 77: 324-335. 18. KEW, M. C., I. BERSOHN & H. C. SEFTEL. 1970. Liver damage in heat stroke. Amer. J. Med. 49: 192-202. S.. R. COLL& T. GILAT. 1967. Heat stroke: Its clinical picture and 19. SHIBOLET, mechanisms in thirty-six cases. Quart. J. Med. 3 6 524-548. 20. VERTEL,R. M. & T. P. KNOCHEL.1967. Acute renal failure due to heat injury. Amer. J. Med. 43: 435-451. 21. SCHIER, R. W., J. HONO& H. I. KELLER. 1967. Nephropathy associated with heat stress and exercise. Ann. Intern. Med. 67: 350-376. & H. C. SEFTEL. 1970. Chronic interstitial nephritis 22. KEW, M. C., C. ABRAHAMS as a consequence of heat stroke. Quart. J. Med. 39: 189-199. C. P., W. C. DUCKWORTH & C. J. ROPER. 1969. Nepropathy in 23. DANCASTER, marathon runners. S. Afr. Med. J. 43: 758-760. 24. WYNDHAM, C. H. & N. B. STRYDOM.1972. Physical exercise in high temperature. I n Sportmedizen. W. Hollman, Ed. : 131-150. Springer-Verlag. Berlin.
