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Cardiovascular Responses to Immersion in a Hot Tub in Comparison With Exercise in Male Subjects With Coronary Artery Disease
Cardiovascular Responses to Immersion in a Hot Tub in Comparison With Exercise in Male Subjects With Coronary Artery Disease
THOMAS G. ALLISON, Ph.D., TODD D. MILLER, M.D., RAY W. SQUIRES, Ph.D., GERALD T. GAU, M.D., Division of Cardiovascular Diseases and Internal Medicine
In order to test the safety of hot tub use for persons with heart disease, 15 men with clinically stable coronary artery disease underwent 15 minutes of immersion in a hot tub at 40°C. On another day, they exercised on a cycle ergometer for 15 minutes; target heart rate was determined by standard methods. Tympanic temperature, skin temperature, electrocardiographic findings, blood pressure, plasma catecholamines, subjective comfort, and cardiovascular symptoms were monitored. The peak heart rate was significantly lower during the hot tub session versus the exercise session (85 ± 14 versus 112 ± 19 beats/min), as were the systolic (106 ± 15 versus 170 ± 21 mm Hg) and diastolic (61 ± 6 versus 83 ± 8 mm Hg) blood pressure measurements (P
Relaxing in a hot tub is a widely enjoyed type of recreation, as indicated by industry estimates of 1.9 million residential units in the United States as of Jan. 1, 1990; however, risks may be involved. A 1981 report ofthe US Consumer Product Safety Commission! examined 30 deaths associated with residential hot tubs. A maximal water temperature of 40°C was recommended because all the deaths studied occurred in temperatures that exceeded that level. The maximal duration of immersion was not specifically established, but the study stated that "20 to 30 minutes would be appropriate" for all adults except pregnant women. In practice, however, many public establishments advise patrons to limit use to 15 min-
utes. A sign is to be posted next to a hot tub with the following warning: "Persons suffering from heart disease, diabetes, or high or low blood pressure should not enter the tub without prior medical consultation and permission from their doctor." Data on the cardiovascular stress of hot tub use are limited, especially in subjects with coronary artery disease. Risk is possibly exaggerated in both the public and the professional mind. Relatively unscientific investigations contribute to the sensationalist view of hot tubs. In one such published study limited to observations of three subjects, the hot tub was referred to as "suicide soup" in the title of the article. 2 The safety of using a sauna has been extensively studied. Luurila' stated that 90 to 95% of Finnish patients with previous myocardial infarction resume regular sauna use within 1 year, and in statistical reviews, Rom045 concluded that no significant increase in heart attacks occurs in the sauna or soon afterward. Hullemann and Matthes" stated that the load
This study was supported in part by a grant from Mayo Foundation, and technical support was provided in part by Grant RR 00585 from the National Institutes of Health, Public Health Service. Address reprint requests to Dr. T. G. Allison, Division of Cardiovascular Diseases, Mayo Clinic, Rochester, MN 55905. Mayo Clin Proc 1993; 68:19-25
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© 1993 Mayo Foundationfor Medical Education and Research
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SAFETY OF HOT TUBS FOR MEN WITH HEART DISEASE
on the heart from a sauna (estimated at 60 W) can be compared with light physical work. Circulating catecholamines have been associated with cardiac arrhythmias? and myocardial ischemia" in patients with coronary artery disease and have also been shown to increase during heat stress? and moderately intense or prolonged exercise. 10,1I Catecholamines have been identified as precipitating factors of cardiac events after exercise.'? Any major increase in circulating catecholamines may indicate an additional risk for patients with heart disease who use a hot tub. The purpose of the current investigation was to assess the safety of hot tub use for men with stable coronary artery disease by (1) determining the changes in body temperature, cardiovascular stress, and circulating catecholamines during immersion in a hot tub for 15 minutes at 40°C and (2) comparing responses in the hot tub to those after 15 minutes of exercise on a cycle ergometer at an intensity determined by standard exercise prescription techniques for patients with heart disease. 12
MATERIAL AND METHODS Study Subjects.-The study group consisted of 15 men with angiographically confirmed coronary artery disease. They ranged in age from 45 to 65 years. Their general characteristics are listed in Table 1. A total of 12 subjects had a previous myocardial infarction; 8 had previously undergone coronary angioplasty, and 3 had previously undergone coronary artery bypass grafting. Infarct sites were the inferior wall (nine), anterior wall (five), and lateral wall (two). Eleven subjects had a history of multiple events: infarction and angioplasty (in six), infarction and bypass (in two), three infarctions (in one), two infarctions (in one), and two infarctions and percutaneous transluminal coronary angioplasty (in one). The mean left ventricular ejection fraction was 55 ± 11% (range, 31 to 71%). All subjects had undergone maximal treadmill testing not more than 1 month before the study; exercise electrocardiographic findings were positive for ischemia in three and borderline positive for ischemia in three. All subjects were free of congestive heart failure or uncontrolled hypertension; at least 3 months had elapsed since they had had a myocardial infarction or had undergone bypass grafting. All subjects except one were taking aspirin and cardiac medications: calcium channel blockers (N = 7), long-acting nitrates (N = 7), ~-adrenergic blockers (N = 6), and angiotensin converting enzyme inhibitor (N = 1). Subjects underwent testing for both trials while receiving their usual medications. Protocol»:-The study was approved by the Mayo Cardiovascular Research Committee and the Mayo Institutional Review Board. After informed consent was obtained, a
Table I.-Characteristics of the 15 Study Subjects With Coronary Artery Disease Variable
Mean±SD
Age (yr) Height (em) Weight (kg) Bodymassindex* Fat (%) Exercise capacity (mets)t
58.6 ± 6.3 178.5 ± 5.8 79.0 ± 8.8 26.2 ±2.5 25.7 ± 4.2 8.4 ± 2.3
*Weight (kg)/height (rrr'). tmets metabolic energy equivalents. =:J
venous access line was placed in the antecubital vein, and instrumentation was completed. Subjects then sat quietly for 6 minutes, after which baseline sitting and standing measurements were obtained. The subjects then immersed themselves in the hot tub for 15 minutes or pedaled for 15 minutes on a cycle ergometer. Tympanic temperature, skin temperature, electrocardiographic findings, blood pressure, comfort or perceived exertion ratings, and symptoms were monitored. After 15 minutes of immersion or exercise, measurements after standing and sitting were obtained. Monitoring continued while subjects sat for 9 minutes after immersion or exercise. Venous blood samples were obtained just before and at 3 and 15 minutes of immersion or exercise. The venous access line was used to avoid reflex changes in catecholamines from repeated venipunctures. (The first blood sample was obtained at least 20 minutes after insertion of the venous access line, a time frame that was thought to be adequate for eliminating any effects of the initial venipuncture.) Trials were conducted randomly on separate days within ±30 minutes of the same time of day. For the hot tub trial, subjects were immersed to the level of their nipple area in a semirecumbent posture in a residential model hot tub. Both arms and hands were kept underwater except during the blood pressure measurement, when the right arm was raised slightly out of the water and supported at shoulder level. The venipuncture site was protected with a waterproof plastic film (Tegaderm). The circulating water was maintained at approximately 40°C; a small, consistent decrease of 0.3°C occurred during the IS-minute immersion period. For the exercise trial, subjects pedaled a Schwinn BioDyne ergometer at 50 rpm for 15 minutes. For the first 3 minutes, the workload was set at 150 kpm/min. During the second 3 minutes, it was increased to 450 kpm/min. The workload was increased or decreased by 150 kpm/min every 3 minutes thereafter in accordance with a target heart rate of 60 to 70% of heart rate reserve'? and a rating of perceived exertion of 12 to 14 on the standard Borg scale. l2 ol 3 Most subjects maintained the target range at 450 kpm/min. The
Mayo Clin Proc, January 1993, Vol 68
mean final workload was 480 ± 32 kpmlmin (77 ± 5 W). The mean final rating of perceived exertion was 13 ± 1. Measurements.-Water, air, and skin temperatures were measured with a Yellow Springs model 44TA Tele-Thermometer, and tympanic temperature was measured with a Mon-a-therm model 6510. Both thermometers were batterypowered. For obtaining the tympanic temperature, a disposable, cotton-covered sensor was inserted into the subject's left ear as far as tolerated. In a previous study," both esophageal and rectal temperatures were measured during immersion in a hot tub. The rectal temperature responded too slowly to reflect accurately the rate of heating in the hot tub. The esophageal temperature responded more rapidly, but 50% of volunteers were unable to tolerate the esophageal probe. Although investigators have previously shown that tympanic temperature may be somewhat affected by ambient temperature and not solely dependent on the temperature of incoming arterial blood," tympanic temperature still seemed a reasonable compromise between rate of response and subject acceptance. Because cardiovascular responses were the primary focus of the current study, we believed that tympanic temperature would satisfactorily compare degree of hyperthermia and rate of heating between immersion and exercise. Skin temperatures were recorded with use of a #409B probe attached by an adhesive and insulating foam pad to the left shoulder above the waterline. Temperatures were recorded in a standard order at baseline sitting, each minute of immersion or exercise, and recovery. Water and air temperatures were monitored with #401 and #405 probes, respectively. The mean air temperature was 22.0°C during immersion trials and 21.8°C during exercise trials. Electrocardiographic findings were monitored continuously with a Marquette Electronics MAC-PC electrocardiograph. The unit contained an optical-electrical barrier and was operated by a 5-V battery for further prevention of electric shock. Disposable foam electrodes were covered by waterproof plastic film that permitted artifact-free tracings and stable baseline measurements in the hot tub. Blood pressure measurements were obtained by auscultation with use of a manually inflated cuff and a mercury sphygmomanometer. Blood pressure determinations and electrocardiographic findings were obtained at baseline sitting and standing, every 3 minutes during immersion or exercise, at immediate postimmersion and postexercise standing and sitting, and every 3 minutes during recovery. Baseline and 15minute electrocardiograms were 12-lead tracings; all others were V4 , V5 , and V6 • Electrocardiographic findings were otherwise monitored on V4 , V5, and V6leads continuously at 5 mmls throughout each trial to document all arrhythmias. Blood samples (20 ml) were withdrawn through the venous access line without use of a tourniquet while the subject was sitting immediately before immersion and at 3 and 15
SAFETY OF HOT TUBS FOR MEN WITH HEART DISEASE
21
minutes of immersion. (Because the collection procedure took 1 to llh minutes, collection began at llh and 131h minutes of immersion and exercise.) The samples were immediately iced and then centrifuged for 20 minutes at 3,000 rpm at 4°C within 45 minutes after collection. Separated plasma was added to 10 x 10--6 liters of 5% sodium metabisulfite and then frozen at -20°e. Samples were analyzed for free epinephrine and norepinephrine on the basis of a previously described method.P-'? During immersion and recovery, subjective comfort was assessed every 3 minutes with use of a nine-point scale that ranged from -4 to +4. The following verbal descriptors were used: "very uncomfortable" = -4; "neutral" = 0; and "very comfortable" = +4. This scale has been used previously. 14 During exercise, a rating of perceived exertion was assessed every 3 minutes with use of the standard Borg scale" of 6 to 20. Symptoms of shortness of breath, chest pain, nausea, light-headedness, drowsiness, and overheating were assessed after the comfort or perceived exertion rating by using a four-point scale-l = "just noticeable," 2 = "mild," 3 = "moderate," and 4 = "severe"; this scale has been used previously. 14 Statistical Analysis.-Changes in tympanic temperature, skin temperature, heart rate, and systolic and diastolic blood pressure from baseline to 15 minutes of immersion versus exercise were compared by using a one-factor analysis of variance with subjects as blocks. A confidence level of 0.05 was used.
RESULTS
Temperatures.- Tympanic temperature began to increase after approximately 5 minutes of immersion (Fig. 1); it increased a mean of 0.6 ± 0.3°C to the end of the immersion period. The peak was 37.6 ± 0.5°C at 3 minutes of recovery; the overall increase was 1.0 ± OA°e. (This finding suggests a 3-minute lag between the blood temperature, which should have begun to decrease as the heat source was removed, and the tympanic temperature probe.) In contrast, tympanic temperature did not increase until at least 9 minutes of exercise; it then increased only 0.1 ± 0.1°C above the baseline at 15 minutes of exercise. As during immersion, the increase during recovery was slight; the peak was 37.0 ± OAoC, and the overall change was 0.3 ± 0.2°e. Changes in tympanic temperature differed significantly during immersion versus exercise (F = 25.63 and P<0.0002). Skin temperature began increasing slowly after 6 minutes of immersion (Fig. 2), presumably because of slightly warmer blood perfusing the skin at a constant rate. It then increased more rapidly during the final 4 minutes of immersion, presumably as blood temperature reached a critical value and triggered an increase in the blood flow in the skin. In contrast, skin temperature decreased progressively after
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SAFETY OF HOT TUBS FOR MEN WITH HEART DISEASE
34,--------------,-------,
37.• , - - - - - - - - - - - - - - , - - - - - - - ,
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Exercise/Immersion
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.6 33.5 ~ :J 'l;j
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32L-_-'-_-----'-_ _L-_--'-_-----'----'---'-L-_--'-_--'
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Time (Minutes)
Fig. 1. Tympanic temperature in 15 men with clinically stable coronary artery disease during exercise, immersion in a hottub,and recovery. Changes in tympanic temperature were significantly greater during immersion than during exercise (F = 25.63 and
Fig. 2. Skin temperature in 15 men with clinically stable.coronary artery disease during exercise, immersion in a hot tub, and recovery. Changes in skintemperature were significantly greaterduring immersion than duringexercise (F = 15.73 and P
about 6 minutes of exercise, even as tympanic temperature increased. The overall changes in skin temperature during immersion (+0.8 ± 1.2°C) and exercise (-D.2 ± 0.4°C) differed significantly (F = 15.73 and P<0.0014). Cardiovascular Responses.-Heart rate increased approximately 15 beats/min when the subjects stood to enter the hot tub, showed no further increase until 6 minutes of immersion, then increased linearly during the final 9 minutes in the hot tub to 85 ± 14 beats/min at 15 minutes (Fig. 3). In contrast, during exercise, heart rate increased to a peak of 112 ± 19 beats/min at 12 minutes. Changes in heart rate from baseline sitting to 15 minutes of immersion or exercise (+26 ± 9 versus +46 ± 17 beats/min) differed significantly (F = 22.36 and P<0.0003). During immersion, systolic pressure decreased gradually by a total of 16 ± 12 rom Hg, and diastolic pressure decreased by 11 ± 9 mm Hg (Fig. 4). During exercise, the blood pressure response differed considerably; systolic pressure increased 49 ± 19 mm Hg, and diastolic pressure increased 10 ± 10 mm Hg. The differences between immersion and exercise were highly significant (for systolic, F =118.44 and P
271 kprn/min (44 W) of exercise. For double product, however, hot tub immersion produced a myocardial oxygen demand expected at only 76 kprn/min (12.5 W) of exercise. As subjects stood to leave the hot tub, systolic pressure decreased an additional 11 ± 14 mm Hg, whereas heart rate increased by 17 ± 10 beats/min. Only three subjects reported light-headedness (a score of 1 on a four-point scale) at this time. The orthostatic systolic blood pressure change was not only greater than that observed from baseline sitting to baseline standing (-2 mm Hg with +16 beats/min heart rate change), but the absolute systolic pressures were significantly lower on standing after immersion than on standing before immersion (95 ± 15 versus 117 ± 21 mm Hg). None of the electrocardiographic findings obtained during immersion in the hot tub or during exercise was indicative of ischemia. Three of the exercise electrocardiograms, however, exhibited J-point depression and upsloping ST segments still depressed (0.05 to 0.10 mV) at 80 ms. In assessment of cardiac arrhythmias, 4 subjects had a total of 52 premature ventricular contractions while in the hot tub; 1 subject had 33. During exercise,S subjects had a total of 475 premature ventricular contractions; 1 subject had 356 ventricular ectopic beats, including a relatively long run of bigeminy. This person exhibited no arrhythmias during immersion. Another subject had 77 premature ventricular contractions during exercise, including several short runs of bigeminy and 10 pairs, but only 20 single ventricular ectopic beats during immersion. No ventricular tachycardia was detected; atrial ectopic activity was limited to a few single premature atrial contractions. Catecholamines.-Only norepinephrine levels were significantly affected by the experimental trials. During exer-
P
Mayo Clin Proc, January 1993, Vol 68
180 , - - - - - - - - - - - - - - - - - , - - - - - - - , Exercise ----&-
12() , - - - - - - - - - - - - - - - - - - , - - - - - - - ,
Exercise/Immersion
Recovery
110
(I)
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140
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120
til til
100
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23
SAFETY OF HOT TUBS FOR MEN WITH HEART DISEASE
Exercise Immersion
LSitLStand
--8------_8
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---B-----
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40 L...L_ _'--_-'-----_-'-_---'-_----'----'--'----'--_-'---_-'
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80
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Fig. 3. Heart rate in 15 men with clinically stable coronary artery disease during exercise, immersion in a hot tub, and recovery. Changes in heart rate were significantly greater during immersion than during exercise (F = 22.36 and P
cise, norepinephrine levels increased during the first 3 minutes and increased further to approximately 3 times the resting value at 15 minutes of exercise (Table 2). No significant change was noted during immersion. The change in norepinephrine during exercise was significantly greater than that during immersion (F = 26.78 and P
Fig. 4. Systolic (upper curve of the paired lines) and diastolic (lower curve ofthe paired lines) bloodpressuremeasurements in 15 men with clinically stable coronary artery disease during exercise, immersion in a hot tub, and recovery. Changes in systolic and diastolic blood pressure during immersion were significantly different from those during exercise (F = 118.44 and P
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SAFETY OF HOT TUBS FOR MEN WITH HEART DISEASE
Table2.-Free Norepinephrine and Epinephrine Levels Before and at 3 and 15 Minutes of Immersion in a Hot Tub or Exercise* Catecholamine Norepinephrine Immersion Exercise]
Epinephrine Immersion Exercise
Before
At3 minutes
At 15 minutes
0.30±0.06 0.26 ± 0.13
0.26±0.06 0.44 ±0.17
0.26± 0.12 0.78 ± 0.33
0.02±0.04 0.02±0.04
0.02±0.04 0.03± 0.05
0.02 ±0.05 0.04 ± 0.05
*AIl values are shown as ng/dl ± SD.
[Change from before to 15 minutes is significantly greater for exercise than for immersion (F = 26.78 and P
Previous studies have established that skin exposed to local heating undergoes pronounced vasodilatation.e" Rapidly increasing skin temperature during the final minutes of immersion suggests that vasodilatation also occurs in nonimmersed skin. This vasodilatory response was not noted during the 15 minutes of exercise performed in the current study, presumably because core temperature failed to increase substantially. The minimal decrease in skin temperature during exercise was interpreted as being due to vasoconstriction and related to the increase in plasma norepinephrine. The considerable difference in blood pressure response between exercise and immersion was likely due in part to vasodilatation of cutaneous tissue during immersion. During the exercise trial, the increase in norepinephrine with no increase in epinephrine is interpreted as an increase in sympathetic neural activity without an adrenal medullary response I 1,26 and is consistent with the relatively low intensity of the work performed. Similarly, Ratge and colleagues" found a threshold of 100 W for an increase in epinephrine during exercise, whereas norepinephrine levels were increased at 50 W; a higher threshold for epinephrine versus norepinephrine increase had been previously observed.v-? The absence of any significant change in circulating catecholamines during immersion implies that the degree of heat stress during 15 minutes of immersion at 40°C was insufficient to elicit either a sympathetic neural or an adrenal medullary response. Rowell and coworkers ' ! also found no additive effect of mild heat stress (38°C waterperfused suit) on either epinephrine or norepinephrine levels in young men during either resting or exercising at 50 W. In contrast, Ratge and associates" observed significant increases in both free norepinephrine and free epinephrine levels in subjects after 20 minutes in a steam bath with an air temperature of 50°C. Those subjects, however, had a mean heart rate of 131 beats/min in comparison with 85 beats/min in the subjects in the current study (maximum, 115 beats/min in any subject).
Mayo Clin Proc, January 1993, Vol 68
Immediate blood pressure changes on standing after immersion are a result of simultaneous shifts in blood to the periphery as water pressure is relieved and to the lower extremities as the gravitational gradient is increased. Hypotension after sauna bathing has also been reported.P" Although none of the subjects in the current study experienced more than a rating of 1 for light-headedness, even in the presence of blood pressure-lowering medication in 14 of 15 subjects, some potential risk for syncope may exist in patients with initially low blood pressure measurements before immersion. CONCLUSION The data from the current study support the following conclusions: (1) No adverse responses were observed during the hot tub trials in the current group of subjects. (2) The physiologic responses to immersion in a hot tub and exercise differed.. (3) Cardiovascular stress during immersion is significantly less severe than during cycle ergometry at a standard target heart rate. (4) Men with stable coronary artery disease who exercise without experiencing difficulty are unlikely to experience problems while immersed in a hot tub for 15 minutes or less at 40°C. (5) Users of hot tubs should be aware of possible hypotension as they stand to exit from the tub, and persons with low blood pressure measurements at rest 01' symptoms of orthostatic hypotension (or both) should probably not use hot tubs. Of importance, the current study did not address safety of hot tub use after ingestion of alcohol, in patients with severe coronary disease or other heart disease who are advised not to exercise in an unsupervised environment, if the water temperature exceeds 40°C or the duration of exposure exceeds 15 minutes (or both), in patients who have been exercising before immersion, or for women with cardiovascular disease. ACKNOWLEDGMENT The authors acknowledge the assistance of Gertrude M. Tyee, Ph.D., Department of Physiology and Biophysics, and her laboratory staff in the analysis of the plasma catecholamines, and we thank Laurie L. Mather for assistance with the preparation of the illustrations for this article. Thatcher Pools & Spas, Inc., of Rochester, Minnesota, loaned a Hot Springs Spa to us for the duration of the current study. REFERENCES 1. Brown V. Spa associated hazards: an updateand summary. Washington (DC): US Consumer Product Safety Commission, 1981 2. TurnerB, Pennefather J, Edmonds C. Cardiovascular effects of hot water immersion (suicide soup). Med J Aust 1980; 2:39
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3. 4. 5. 6.
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Luurila OJ. Cardiac arrhythmias, sudden death and the Finnish sauna bath. Adv Cardio11978; 25:73-81 Romo M. Factors related to sudden death in acute ischaemic heart disease: a community study in Helsinki. Acta Med Scand [Suppl] 1972; 547:1-92 Romo M. Heart-attacks and the sauna [letter]. Lancet 1976; 2:809 Htilleman K-D, Matthes D. Comparative telemetric measurements on heart attack patients and normal persons in the sauna, taking an ergometer test, at sports and at an interview. In: Teir H, Collan Y, Valtakari P, editors. Sauna Studies. Helsinki: The Finnish Sauna Society, 1976: 181-189 McCance AJ, Forfar JC. Myocardial ischaemia and ventricular arrhythmias precipitated by physiological concentrations of adrenaline in patients with coronary heart disease. Br HeartJ 1991; 66:316-319 Rocco MB, Barry J, Campbell S, Nabel E, Cook EF, Goldman L, et al. Circadian variation of transient myocardial ischemia in patients with coronary artery disease. Circulation 1987; 75:395-400 Mpller N, Beckwith R, Butler PC, Christensen NJ, 0rskov H, Alberti KGMM. Metabolic and hormonal responses to exogenous hyperthermia in man. Clin Endocrinol (Oxf) 1989; 30:651-660 Dimsdale JE, Hartley LH, Guiney T, Ruskin IN, Greenblatt D. Postexercise peril: plasma catecholamines and exercise. JAMA 1984; 251:630-632 Rowell LB, Brengelmann GL, Freund PRo Unaltered norepinephrine-heart rate relationship in exercise with exogenous heat. J Appl Physiol1987; 62:646-650 American College of Sports Medicine. Guidelines for Exercise Testing and Prescription. 4th ed. Philadelphia: Lea & Febiger, 1991: 93-159 Borg GAV. Perceived exertion: a note on "history" and methods. Med Sci Sports 1973; 5:90-93 Allison TG, Reger WE. Thermoregulatory, cardiovascular, and psychophysical response to alcohol in men in 40°C water. J Appl Physiol1992; 72:2099-2107 Nadel ER, Horvath SM. Comparison of tympanic membrane and deep body temperatures in man. Life Sci 1970; 9:869875 Bove AA, DeweyJD, Tyee GM. Increased conjugated dopamine in plasma after exercise training. J Lab Clin Med 1984; 104:77-85 Devalon ML, Miller TD, Squires RW, Rogers PJ, Bove AA, Tyee GM. Dopa in plasma increases during acute exercise
SAFETY OF HOT TUBS FOR MEN WITH HEART DISEASE
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and after exercise training. J Lab Clin Med 1989; 114:321327 Faithfull NS, Reinhold HS, van den Berg AP, van Rhoon GC, van der Zee J, Wike-Hooley JL. Cardiovascular changes during whole body hyperthermia treatment of advanced malignancy. Eur J Appl Physiol1984; 53:274-281 Versteegh PMR, van den Hoogen RHWM, Zwaveling A. Systemic hyperthermia by the immersion bath method. Neth J Surg 1981; 33:195-199 Kirsch KA, Rocker L, von Ameln H, Hrynyschyn K. The cardiac filling pressure following exercise and thermal stress. Yale J BioI Med 1986; 59:257-265 Arborelius M Jr, Balldin UI, Lilja B, Lundgren CEG. Hemodynamic changes in man during immersion with the head above water. Aerospace Med 1972; 43:592-598 Begin R, Epstein M, Sackner MA, Levinson R, Dougherty R, Duncan D. Effects of water immersion to the neck on pulmonary circulation and tissue volume in man. J Appl Physiol 1976; 40:293-299 Echt M, Lange L, Gauer OH. Changes of peripheral venous tone and central transmural venous pressure during immersion in a thermo-neutral bath. Pflugers Arch 1974; 352:211217 Rowell LB, Brengelmann GL, Blackmon JR, Murray JA. Redistribution of blood flow during sustained high skin temperature in resting man. J Appl Physiol1970; 28:415-420 Rowell LB, Brengelmann GL, Detry J-MR, Wyss C. Venomotor responses to rapid changes in skin temperature in exercising man. J Appl Physiol1971; 30:64-71 Shah SD, Tse TF, Clutter WE, Cryer PE. The human sympathochromaffin system. Am J Physiol 1984; 247 :E380E384 Ratge D, Gehrke A, Melzner I, Wisser H. Free and conjugated catecholamines in human plasma during physical exercise. Clin Exp Pharmacol Physiol1986; 13:543-553 Hartley LH, Mason JW, Hogan RP, Jones LG, Kotchen TA, Mougey EH, et al. Multiple hormonal responses to graded exercise in relation to physical training. J Appl PhysioI1972; 33:602-606 Bloom SR, Johnson RH, Park DM, Rennie MJ, Sulaiman WR. Differences in the metabolic and hormonal response to exercise between racing cyclists and untrained individuals. J Physiol (Lond) 1976; 258:1-18 Taggart P, Parkinson P, Carruthers M. Cardiac responses to thermal, physical, and emotional stress. BMJ 1972; 3:71-76
THOMAS G. ALLISON, Ph.D., TODD D. MILLER, M.D., RAY W. SQUIRES, Ph.D., GERALD T. GAU, M.D., Division of Cardiovascular Diseases and Internal Medicine
In order to test the safety of hot tub use for persons with heart disease, 15 men with clinically stable coronary artery disease underwent 15 minutes of immersion in a hot tub at 40°C. On another day, they exercised on a cycle ergometer for 15 minutes; target heart rate was determined by standard methods. Tympanic temperature, skin temperature, electrocardiographic findings, blood pressure, plasma catecholamines, subjective comfort, and cardiovascular symptoms were monitored. The peak heart rate was significantly lower during the hot tub session versus the exercise session (85 ± 14 versus 112 ± 19 beats/min), as were the systolic (106 ± 15 versus 170 ± 21 mm Hg) and diastolic (61 ± 6 versus 83 ± 8 mm Hg) blood pressure measurements (P
Relaxing in a hot tub is a widely enjoyed type of recreation, as indicated by industry estimates of 1.9 million residential units in the United States as of Jan. 1, 1990; however, risks may be involved. A 1981 report ofthe US Consumer Product Safety Commission! examined 30 deaths associated with residential hot tubs. A maximal water temperature of 40°C was recommended because all the deaths studied occurred in temperatures that exceeded that level. The maximal duration of immersion was not specifically established, but the study stated that "20 to 30 minutes would be appropriate" for all adults except pregnant women. In practice, however, many public establishments advise patrons to limit use to 15 min-
utes. A sign is to be posted next to a hot tub with the following warning: "Persons suffering from heart disease, diabetes, or high or low blood pressure should not enter the tub without prior medical consultation and permission from their doctor." Data on the cardiovascular stress of hot tub use are limited, especially in subjects with coronary artery disease. Risk is possibly exaggerated in both the public and the professional mind. Relatively unscientific investigations contribute to the sensationalist view of hot tubs. In one such published study limited to observations of three subjects, the hot tub was referred to as "suicide soup" in the title of the article. 2 The safety of using a sauna has been extensively studied. Luurila' stated that 90 to 95% of Finnish patients with previous myocardial infarction resume regular sauna use within 1 year, and in statistical reviews, Rom045 concluded that no significant increase in heart attacks occurs in the sauna or soon afterward. Hullemann and Matthes" stated that the load
This study was supported in part by a grant from Mayo Foundation, and technical support was provided in part by Grant RR 00585 from the National Institutes of Health, Public Health Service. Address reprint requests to Dr. T. G. Allison, Division of Cardiovascular Diseases, Mayo Clinic, Rochester, MN 55905. Mayo Clin Proc 1993; 68:19-25
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© 1993 Mayo Foundationfor Medical Education and Research
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Mayo Clin Proc, January 1993, Vol 68
SAFETY OF HOT TUBS FOR MEN WITH HEART DISEASE
on the heart from a sauna (estimated at 60 W) can be compared with light physical work. Circulating catecholamines have been associated with cardiac arrhythmias? and myocardial ischemia" in patients with coronary artery disease and have also been shown to increase during heat stress? and moderately intense or prolonged exercise. 10,1I Catecholamines have been identified as precipitating factors of cardiac events after exercise.'? Any major increase in circulating catecholamines may indicate an additional risk for patients with heart disease who use a hot tub. The purpose of the current investigation was to assess the safety of hot tub use for men with stable coronary artery disease by (1) determining the changes in body temperature, cardiovascular stress, and circulating catecholamines during immersion in a hot tub for 15 minutes at 40°C and (2) comparing responses in the hot tub to those after 15 minutes of exercise on a cycle ergometer at an intensity determined by standard exercise prescription techniques for patients with heart disease. 12
MATERIAL AND METHODS Study Subjects.-The study group consisted of 15 men with angiographically confirmed coronary artery disease. They ranged in age from 45 to 65 years. Their general characteristics are listed in Table 1. A total of 12 subjects had a previous myocardial infarction; 8 had previously undergone coronary angioplasty, and 3 had previously undergone coronary artery bypass grafting. Infarct sites were the inferior wall (nine), anterior wall (five), and lateral wall (two). Eleven subjects had a history of multiple events: infarction and angioplasty (in six), infarction and bypass (in two), three infarctions (in one), two infarctions (in one), and two infarctions and percutaneous transluminal coronary angioplasty (in one). The mean left ventricular ejection fraction was 55 ± 11% (range, 31 to 71%). All subjects had undergone maximal treadmill testing not more than 1 month before the study; exercise electrocardiographic findings were positive for ischemia in three and borderline positive for ischemia in three. All subjects were free of congestive heart failure or uncontrolled hypertension; at least 3 months had elapsed since they had had a myocardial infarction or had undergone bypass grafting. All subjects except one were taking aspirin and cardiac medications: calcium channel blockers (N = 7), long-acting nitrates (N = 7), ~-adrenergic blockers (N = 6), and angiotensin converting enzyme inhibitor (N = 1). Subjects underwent testing for both trials while receiving their usual medications. Protocol»:-The study was approved by the Mayo Cardiovascular Research Committee and the Mayo Institutional Review Board. After informed consent was obtained, a
Table I.-Characteristics of the 15 Study Subjects With Coronary Artery Disease Variable
Mean±SD
Age (yr) Height (em) Weight (kg) Bodymassindex* Fat (%) Exercise capacity (mets)t
58.6 ± 6.3 178.5 ± 5.8 79.0 ± 8.8 26.2 ±2.5 25.7 ± 4.2 8.4 ± 2.3
*Weight (kg)/height (rrr'). tmets metabolic energy equivalents. =:J
venous access line was placed in the antecubital vein, and instrumentation was completed. Subjects then sat quietly for 6 minutes, after which baseline sitting and standing measurements were obtained. The subjects then immersed themselves in the hot tub for 15 minutes or pedaled for 15 minutes on a cycle ergometer. Tympanic temperature, skin temperature, electrocardiographic findings, blood pressure, comfort or perceived exertion ratings, and symptoms were monitored. After 15 minutes of immersion or exercise, measurements after standing and sitting were obtained. Monitoring continued while subjects sat for 9 minutes after immersion or exercise. Venous blood samples were obtained just before and at 3 and 15 minutes of immersion or exercise. The venous access line was used to avoid reflex changes in catecholamines from repeated venipunctures. (The first blood sample was obtained at least 20 minutes after insertion of the venous access line, a time frame that was thought to be adequate for eliminating any effects of the initial venipuncture.) Trials were conducted randomly on separate days within ±30 minutes of the same time of day. For the hot tub trial, subjects were immersed to the level of their nipple area in a semirecumbent posture in a residential model hot tub. Both arms and hands were kept underwater except during the blood pressure measurement, when the right arm was raised slightly out of the water and supported at shoulder level. The venipuncture site was protected with a waterproof plastic film (Tegaderm). The circulating water was maintained at approximately 40°C; a small, consistent decrease of 0.3°C occurred during the IS-minute immersion period. For the exercise trial, subjects pedaled a Schwinn BioDyne ergometer at 50 rpm for 15 minutes. For the first 3 minutes, the workload was set at 150 kpm/min. During the second 3 minutes, it was increased to 450 kpm/min. The workload was increased or decreased by 150 kpm/min every 3 minutes thereafter in accordance with a target heart rate of 60 to 70% of heart rate reserve'? and a rating of perceived exertion of 12 to 14 on the standard Borg scale. l2 ol 3 Most subjects maintained the target range at 450 kpm/min. The
Mayo Clin Proc, January 1993, Vol 68
mean final workload was 480 ± 32 kpmlmin (77 ± 5 W). The mean final rating of perceived exertion was 13 ± 1. Measurements.-Water, air, and skin temperatures were measured with a Yellow Springs model 44TA Tele-Thermometer, and tympanic temperature was measured with a Mon-a-therm model 6510. Both thermometers were batterypowered. For obtaining the tympanic temperature, a disposable, cotton-covered sensor was inserted into the subject's left ear as far as tolerated. In a previous study," both esophageal and rectal temperatures were measured during immersion in a hot tub. The rectal temperature responded too slowly to reflect accurately the rate of heating in the hot tub. The esophageal temperature responded more rapidly, but 50% of volunteers were unable to tolerate the esophageal probe. Although investigators have previously shown that tympanic temperature may be somewhat affected by ambient temperature and not solely dependent on the temperature of incoming arterial blood," tympanic temperature still seemed a reasonable compromise between rate of response and subject acceptance. Because cardiovascular responses were the primary focus of the current study, we believed that tympanic temperature would satisfactorily compare degree of hyperthermia and rate of heating between immersion and exercise. Skin temperatures were recorded with use of a #409B probe attached by an adhesive and insulating foam pad to the left shoulder above the waterline. Temperatures were recorded in a standard order at baseline sitting, each minute of immersion or exercise, and recovery. Water and air temperatures were monitored with #401 and #405 probes, respectively. The mean air temperature was 22.0°C during immersion trials and 21.8°C during exercise trials. Electrocardiographic findings were monitored continuously with a Marquette Electronics MAC-PC electrocardiograph. The unit contained an optical-electrical barrier and was operated by a 5-V battery for further prevention of electric shock. Disposable foam electrodes were covered by waterproof plastic film that permitted artifact-free tracings and stable baseline measurements in the hot tub. Blood pressure measurements were obtained by auscultation with use of a manually inflated cuff and a mercury sphygmomanometer. Blood pressure determinations and electrocardiographic findings were obtained at baseline sitting and standing, every 3 minutes during immersion or exercise, at immediate postimmersion and postexercise standing and sitting, and every 3 minutes during recovery. Baseline and 15minute electrocardiograms were 12-lead tracings; all others were V4 , V5 , and V6 • Electrocardiographic findings were otherwise monitored on V4 , V5, and V6leads continuously at 5 mmls throughout each trial to document all arrhythmias. Blood samples (20 ml) were withdrawn through the venous access line without use of a tourniquet while the subject was sitting immediately before immersion and at 3 and 15
SAFETY OF HOT TUBS FOR MEN WITH HEART DISEASE
21
minutes of immersion. (Because the collection procedure took 1 to llh minutes, collection began at llh and 131h minutes of immersion and exercise.) The samples were immediately iced and then centrifuged for 20 minutes at 3,000 rpm at 4°C within 45 minutes after collection. Separated plasma was added to 10 x 10--6 liters of 5% sodium metabisulfite and then frozen at -20°e. Samples were analyzed for free epinephrine and norepinephrine on the basis of a previously described method.P-'? During immersion and recovery, subjective comfort was assessed every 3 minutes with use of a nine-point scale that ranged from -4 to +4. The following verbal descriptors were used: "very uncomfortable" = -4; "neutral" = 0; and "very comfortable" = +4. This scale has been used previously. 14 During exercise, a rating of perceived exertion was assessed every 3 minutes with use of the standard Borg scale" of 6 to 20. Symptoms of shortness of breath, chest pain, nausea, light-headedness, drowsiness, and overheating were assessed after the comfort or perceived exertion rating by using a four-point scale-l = "just noticeable," 2 = "mild," 3 = "moderate," and 4 = "severe"; this scale has been used previously. 14 Statistical Analysis.-Changes in tympanic temperature, skin temperature, heart rate, and systolic and diastolic blood pressure from baseline to 15 minutes of immersion versus exercise were compared by using a one-factor analysis of variance with subjects as blocks. A confidence level of 0.05 was used.
RESULTS
Temperatures.- Tympanic temperature began to increase after approximately 5 minutes of immersion (Fig. 1); it increased a mean of 0.6 ± 0.3°C to the end of the immersion period. The peak was 37.6 ± 0.5°C at 3 minutes of recovery; the overall increase was 1.0 ± OA°e. (This finding suggests a 3-minute lag between the blood temperature, which should have begun to decrease as the heat source was removed, and the tympanic temperature probe.) In contrast, tympanic temperature did not increase until at least 9 minutes of exercise; it then increased only 0.1 ± 0.1°C above the baseline at 15 minutes of exercise. As during immersion, the increase during recovery was slight; the peak was 37.0 ± OAoC, and the overall change was 0.3 ± 0.2°e. Changes in tympanic temperature differed significantly during immersion versus exercise (F = 25.63 and P<0.0002). Skin temperature began increasing slowly after 6 minutes of immersion (Fig. 2), presumably because of slightly warmer blood perfusing the skin at a constant rate. It then increased more rapidly during the final 4 minutes of immersion, presumably as blood temperature reached a critical value and triggered an increase in the blood flow in the skin. In contrast, skin temperature decreased progressively after
22
Mayo Clin Proc, January 1993, Vol 68
SAFETY OF HOT TUBS FOR MEN WITH HEART DISEASE
34,--------------,-------,
37.• , - - - - - - - - - - - - - - , - - - - - - - ,
Exercise --s-Immersion ----A-
Recovery
Exercise/Immersion
Exercise --s-Immersion ----A-
.6 33.5 ~ :J 'l;j
lii
a. E ~
33
:i:
32.5
c::
(/)
Exercise/Immersion
Recovery
38.4 '--_---'-_-..L_ _'--_--'-_---'--'-.l-J_ _- - ' - _ - ' o 9 12 15 16 17 l' 21 24
Time (Minutes)
32L-_-'-_-----'-_ _L-_--'-_-----'----'---'-L-_--'-_--'
o
9
12
15 16 17 18
21
24
Time (Minutes)
Fig. 1. Tympanic temperature in 15 men with clinically stable coronary artery disease during exercise, immersion in a hottub,and recovery. Changes in tympanic temperature were significantly greater during immersion than during exercise (F = 25.63 and
Fig. 2. Skin temperature in 15 men with clinically stable.coronary artery disease during exercise, immersion in a hot tub, and recovery. Changes in skintemperature were significantly greaterduring immersion than duringexercise (F = 15.73 and P
about 6 minutes of exercise, even as tympanic temperature increased. The overall changes in skin temperature during immersion (+0.8 ± 1.2°C) and exercise (-D.2 ± 0.4°C) differed significantly (F = 15.73 and P<0.0014). Cardiovascular Responses.-Heart rate increased approximately 15 beats/min when the subjects stood to enter the hot tub, showed no further increase until 6 minutes of immersion, then increased linearly during the final 9 minutes in the hot tub to 85 ± 14 beats/min at 15 minutes (Fig. 3). In contrast, during exercise, heart rate increased to a peak of 112 ± 19 beats/min at 12 minutes. Changes in heart rate from baseline sitting to 15 minutes of immersion or exercise (+26 ± 9 versus +46 ± 17 beats/min) differed significantly (F = 22.36 and P<0.0003). During immersion, systolic pressure decreased gradually by a total of 16 ± 12 rom Hg, and diastolic pressure decreased by 11 ± 9 mm Hg (Fig. 4). During exercise, the blood pressure response differed considerably; systolic pressure increased 49 ± 19 mm Hg, and diastolic pressure increased 10 ± 10 mm Hg. The differences between immersion and exercise were highly significant (for systolic, F =118.44 and P
271 kprn/min (44 W) of exercise. For double product, however, hot tub immersion produced a myocardial oxygen demand expected at only 76 kprn/min (12.5 W) of exercise. As subjects stood to leave the hot tub, systolic pressure decreased an additional 11 ± 14 mm Hg, whereas heart rate increased by 17 ± 10 beats/min. Only three subjects reported light-headedness (a score of 1 on a four-point scale) at this time. The orthostatic systolic blood pressure change was not only greater than that observed from baseline sitting to baseline standing (-2 mm Hg with +16 beats/min heart rate change), but the absolute systolic pressures were significantly lower on standing after immersion than on standing before immersion (95 ± 15 versus 117 ± 21 mm Hg). None of the electrocardiographic findings obtained during immersion in the hot tub or during exercise was indicative of ischemia. Three of the exercise electrocardiograms, however, exhibited J-point depression and upsloping ST segments still depressed (0.05 to 0.10 mV) at 80 ms. In assessment of cardiac arrhythmias, 4 subjects had a total of 52 premature ventricular contractions while in the hot tub; 1 subject had 33. During exercise,S subjects had a total of 475 premature ventricular contractions; 1 subject had 356 ventricular ectopic beats, including a relatively long run of bigeminy. This person exhibited no arrhythmias during immersion. Another subject had 77 premature ventricular contractions during exercise, including several short runs of bigeminy and 10 pairs, but only 20 single ventricular ectopic beats during immersion. No ventricular tachycardia was detected; atrial ectopic activity was limited to a few single premature atrial contractions. Catecholamines.-Only norepinephrine levels were significantly affected by the experimental trials. During exer-
P
Mayo Clin Proc, January 1993, Vol 68
180 , - - - - - - - - - - - - - - - - - , - - - - - - - , Exercise ----&-
12() , - - - - - - - - - - - - - - - - - - , - - - - - - - ,
Exercise/Immersion
Recovery
110
(I)
(;j II: t:
90
E
140
~
120
til til
100
~
80
---b--
- -8 -- -- -- -8 -- -- __-b
_
Q.
'0
o o iii
(I)
70
60
Immersion
:l
III
I
160
.s
a.
~
C» I
E"oo .0
23
SAFETY OF HOT TUBS FOR MEN WITH HEART DISEASE
Exercise Immersion
LSitLStand
--8------_8
60
b
b
_ ----
Exercise/Immersion
---B-----
Recovery
40 L...L_ _'--_-'-----_-'-_---'-_----'----'--'----'--_-'---_-'
-----A-
'--_--'-_-'-_--'-_-----JL-l...-'--'----_-'-_---'
5OL...L_ _ 0 3
80
12
21
24
0
L
L
S~
Stand
3
12
21
24
Time (Minutes)
Time (Minutes)
Fig. 3. Heart rate in 15 men with clinically stable coronary artery disease during exercise, immersion in a hot tub, and recovery. Changes in heart rate were significantly greater during immersion than during exercise (F = 22.36 and P
cise, norepinephrine levels increased during the first 3 minutes and increased further to approximately 3 times the resting value at 15 minutes of exercise (Table 2). No significant change was noted during immersion. The change in norepinephrine during exercise was significantly greater than that during immersion (F = 26.78 and P
Fig. 4. Systolic (upper curve of the paired lines) and diastolic (lower curve ofthe paired lines) bloodpressuremeasurements in 15 men with clinically stable coronary artery disease during exercise, immersion in a hot tub, and recovery. Changes in systolic and diastolic blood pressure during immersion were significantly different from those during exercise (F = 118.44 and P
24
SAFETY OF HOT TUBS FOR MEN WITH HEART DISEASE
Table2.-Free Norepinephrine and Epinephrine Levels Before and at 3 and 15 Minutes of Immersion in a Hot Tub or Exercise* Catecholamine Norepinephrine Immersion Exercise]
Epinephrine Immersion Exercise
Before
At3 minutes
At 15 minutes
0.30±0.06 0.26 ± 0.13
0.26±0.06 0.44 ±0.17
0.26± 0.12 0.78 ± 0.33
0.02±0.04 0.02±0.04
0.02±0.04 0.03± 0.05
0.02 ±0.05 0.04 ± 0.05
*AIl values are shown as ng/dl ± SD.
[Change from before to 15 minutes is significantly greater for exercise than for immersion (F = 26.78 and P
Previous studies have established that skin exposed to local heating undergoes pronounced vasodilatation.e" Rapidly increasing skin temperature during the final minutes of immersion suggests that vasodilatation also occurs in nonimmersed skin. This vasodilatory response was not noted during the 15 minutes of exercise performed in the current study, presumably because core temperature failed to increase substantially. The minimal decrease in skin temperature during exercise was interpreted as being due to vasoconstriction and related to the increase in plasma norepinephrine. The considerable difference in blood pressure response between exercise and immersion was likely due in part to vasodilatation of cutaneous tissue during immersion. During the exercise trial, the increase in norepinephrine with no increase in epinephrine is interpreted as an increase in sympathetic neural activity without an adrenal medullary response I 1,26 and is consistent with the relatively low intensity of the work performed. Similarly, Ratge and colleagues" found a threshold of 100 W for an increase in epinephrine during exercise, whereas norepinephrine levels were increased at 50 W; a higher threshold for epinephrine versus norepinephrine increase had been previously observed.v-? The absence of any significant change in circulating catecholamines during immersion implies that the degree of heat stress during 15 minutes of immersion at 40°C was insufficient to elicit either a sympathetic neural or an adrenal medullary response. Rowell and coworkers ' ! also found no additive effect of mild heat stress (38°C waterperfused suit) on either epinephrine or norepinephrine levels in young men during either resting or exercising at 50 W. In contrast, Ratge and associates" observed significant increases in both free norepinephrine and free epinephrine levels in subjects after 20 minutes in a steam bath with an air temperature of 50°C. Those subjects, however, had a mean heart rate of 131 beats/min in comparison with 85 beats/min in the subjects in the current study (maximum, 115 beats/min in any subject).
Mayo Clin Proc, January 1993, Vol 68
Immediate blood pressure changes on standing after immersion are a result of simultaneous shifts in blood to the periphery as water pressure is relieved and to the lower extremities as the gravitational gradient is increased. Hypotension after sauna bathing has also been reported.P" Although none of the subjects in the current study experienced more than a rating of 1 for light-headedness, even in the presence of blood pressure-lowering medication in 14 of 15 subjects, some potential risk for syncope may exist in patients with initially low blood pressure measurements before immersion. CONCLUSION The data from the current study support the following conclusions: (1) No adverse responses were observed during the hot tub trials in the current group of subjects. (2) The physiologic responses to immersion in a hot tub and exercise differed.. (3) Cardiovascular stress during immersion is significantly less severe than during cycle ergometry at a standard target heart rate. (4) Men with stable coronary artery disease who exercise without experiencing difficulty are unlikely to experience problems while immersed in a hot tub for 15 minutes or less at 40°C. (5) Users of hot tubs should be aware of possible hypotension as they stand to exit from the tub, and persons with low blood pressure measurements at rest 01' symptoms of orthostatic hypotension (or both) should probably not use hot tubs. Of importance, the current study did not address safety of hot tub use after ingestion of alcohol, in patients with severe coronary disease or other heart disease who are advised not to exercise in an unsupervised environment, if the water temperature exceeds 40°C or the duration of exposure exceeds 15 minutes (or both), in patients who have been exercising before immersion, or for women with cardiovascular disease. ACKNOWLEDGMENT The authors acknowledge the assistance of Gertrude M. Tyee, Ph.D., Department of Physiology and Biophysics, and her laboratory staff in the analysis of the plasma catecholamines, and we thank Laurie L. Mather for assistance with the preparation of the illustrations for this article. Thatcher Pools & Spas, Inc., of Rochester, Minnesota, loaned a Hot Springs Spa to us for the duration of the current study. REFERENCES 1. Brown V. Spa associated hazards: an updateand summary. Washington (DC): US Consumer Product Safety Commission, 1981 2. TurnerB, Pennefather J, Edmonds C. Cardiovascular effects of hot water immersion (suicide soup). Med J Aust 1980; 2:39
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