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Print version ISSN 1517-8692
Rev Bras Med Esporte vol.12 no.4 Niterói July/Aug. 2006
Efectos de la sauna sobre las enfermedades cardiovasculares y las relacionadas al estilo de vida
B. TalebipourI; L.O.C. RodriguesII; M.C.V. MoreiraI
de Medicina da Universidade Federal de Minas Gerais
IILaboratório de Fisiologia do Exercício da Escola de Educação Física, Fisioterapia e Terapia Ocupacional
Sauna baths is popular practice among healthy young, adult and older people. The sports medicine physicians are frequently asked to evaluate the impact of sauna on diseases and on health in general. Sauna can be beneficial or dangerous depending on its use. In the past few years, sauna has been considered beneficial for patients with cardiovascular conditions, as well as for heart failure and lifestyle-related diseases, mainly by improving the peripheral endothelial function through the increase of the cardiac output and peripheral vasodilatation. The endothelial dysfunction is present in most of the cardiovascular diseases. The present article has the objective to review sauna effects on the cardiovascular system in healthy individuals and in some cardiovascular diseases.
Keywords: Sauna. Endothelial function. Heart failure. Systemic arterial hypertension. Thermoregulation.
Frecuentar la sauna es una práctica popular de jóvenes, adultos y ancianos saludables. Los médicos de deportes son, con frecuencia, solicitados a opinar sobre el impacto de la sauna en las enfermedades y en la salud de modo general. La sauna puede ser benéfica o maléfica dependiendo del uso que hacemos de ella. En los últimos años, la sauna viene siendo considerada como benéfica para los portadores de enfermedades cardiovasculares, tales como la insuficiencia cardiaca y enfermedades relacionadas con el estilo de vida, principalmente, por mejorar la función endotelial periférica, mediante la disminución de la falla cardiaca y la vaso dilatación periférica. La disfunción endotelial está presente en casi todas las enfermedades cardiovasculares. El presente artículo tiene la intención de hacer una revisión sobre los efectos de la sauna sobre el sistema cardiovascular en individuos saludables y en determinadas enfermedades cardiovasculares.
Palabras-clave: Sauna. Función endotelial. Insuficiencia cardiaca. Hipertensión arterial sistémica. Termorregulación.
Bathing in one form or other is the oldest custom people have practiced. It has been closely linked with the cultural movement, and has become an integral part of the history of civilization(1).
Sauna and Turkish bath are very popular in the Scandinavian and the Middle East countries respectively, and have been practiced with therapeutic purpose in many diseases for centuries.
The search for well-being and the fact that physical activities are increasingly being recommended to diminish sedentary life and incidence of diseases, bring as a consequence the proliferation of organizations and institutions related to sports practice and sauna, such as clubs and specialized clinics (spas). The target public consists of the young and the elderly, healthy or not.
With the increase of the incidence and prevalence of the cardiovascular diseases, obesity and sedentarism in the industrialized countries, including Brazil, we can observe the greater number of patients with cardiovascular diseases frequent these institutions and specifically sauna.
Sports medicine physicians are frequently asked about the possible effects of sauna on athletes' health, sedentary individuals and on the patients with different disease.
Physiological effects(2-4), benefits and risks(5), facts and fables(6) about the sauna were subject of extensive review. Recently, sauna was studied as a therapeutic option for cardiovascular diseases(7) and an improvement in clinical indicators with thermal therapy in lifestyles-related diseases was observed(8).
The main purpose of the present article is related to such therapeutic option, analyzing the thermoregulatory and cardiovascular variables involved with sauna exposure.
Sauna is characterized by its high temperature and dry air. The basic sauna consists of a wood-paneled room, an unpainted wooden platform and a heat source (electric, with a log source or gas). The size of the sauna should also be at least three m2 to allow proper heat balance, suitable humidity and adequate ventilation (3 to 8 times per hour). The suggested temperature is of 80º-100ºC at the face level and 30ºC at floor level(9). The relative humidity should be of 10% to 20% (40 to 70 g of water vapor/kg air)(9-10). The usual ritual consists of several short stays (5 to 20 min) in the sauna, alternated with cooling-off periods and followed by oral intake of fluids(6,11).
ACUTE SAUNA EFFECTS ON THERMOREGULATORY AND CARDIOVASCULAR VARIABLES
The sauna bath represents a heat load of 300-600 W/m2 of body surface area(10). The skin temperature rapidly increases to ± 40º-41ºC(2,9-10) and the thermoregulatory mechanisms are triggered.
Evaporative heat transfer by sweating is the only effective body heat loss channel in dry sauna(10).
The sweating begins rapidly and reaches its maximum level in ± 15 min. The total sweat secretion can go up to 0.5-1 kg/h and represents a heat loss of about 200 W/m2 of the body surface area(2,10).
The body cannot compensate for the heat load and causing elevation of internal temperature. The rectal temperature increase depends on the condition of the heat exposure and ranges from 0,4ºC(12) to 1ºC(13). The skin circulation increases substantially in order to prevent the body from heating. The skin blood flow, in the thermo-neutral condition (± 20ºC) and in rest corresponding to ± 5-10% of the cardiac output, can reach ± 50-70% of the cardiac output (7-8 L/min) in the sauna(14). The arterial blood pressure tends to decrease. However, such reduction is prevented by the elevation of the cardiac output by increased heart rate(3,14) and by the reduction of the blood flow to internal organs(14-15). The cardiac stroke volume does not change(3,14). The effect of sauna baths on the arterial blood pressure is variable (table 1). Repeated sauna baths improve the heat tolerance and reduce the magnitude of the changes of the variables mentioned above(12).
The thermoregulatory and cardiovascular effects of sauna exposure are resumed in table 1.
SKIN VASODILATION IN RESPONSE TO THERMAL STRESS IN HEALTHY INDIVIDUALS
Reflex control of blood flow to nonglabrous skin in humans is accomplished by two branches of the autonomous sympathetic nervous system: a noradrenergic active vasoconstrictor system(26) and an active vasodilator system acetylcholine-dependent(27) mediated by nitric oxide (NO)(28-30) and prostaglandins(30).
The nitric oxide is an important mediator of the homeostasis process and the defense mechanisms of the body. In vascular bed, the NO is produced by the endothelial cells through the endothelial nitric oxide synthase enzyme (eNOS), that is activated by mechanical stress (as shear stress, or tangential force done by the blood flow on the endothelial surface)(31-32) and stimulation by bradykinin and acetylcholine. The nitric oxide has many functions, but its action as endothelium derived relaxation factor is the most important in order to maintain the vascular homeostasis. It is widely accepted that nitric oxide produced by endothelial cells effects vasodilation in normal, healthy human vessels, including those found in the skin(28,33-37). The activation of the vasodilator system is responsible for 80% to 95% of the increase of the skin blood flow during the thermal stress(38-39). Considering that the total skin blood flow can reach 7-8 L/min in sauna(14), or 70% of the cardiac output during thermal stress, it is obvious the critical role of the active vasodilator system in the thermoregulation response and in the systemic hemodynamics variables.
SAUNA AND CONGESTIVE HEART FAILURE (CHF)
Endothelial function in CHF patients
In patients with CHF, the peripheral vascular resistance is increased via activation of the neurohormonal system, namely by autonomous sympathetic nervous system, rennin -angiotensin- aldosterone system (RAAS), and endothelin system(40-43).
The vascular endothelial function in patients with CHF, mainly represented by the endothelium-dependent vasodilation, is altered(44-50). Such alteration leads to the vascular tonus increase and remodeling of the blood vessels, which reduces the peripheral blood flow. Hence, the amount of oxygen for the skeletal muscles is compromised, with subsequent clinical symptoms and progressive exercise intolerance. The vascular endothelial dysfunction in the CHF is mainly due to the decrease of the nitric oxide production induced by the reduced gene expression of eNOS(51-53) and increased oxidative stress(54-55).
Thermal stress and endothelial function in CHF patients
The endothelium-dependent vasodilation alteration has been virtually reported in all cardiovascular diseases, including in atherosclerosis(56) and CHF. Using sauna bath as therapeutic option for CHF is not very recent, since in the 1950's decade the first studies with CHF patients were conducted(57-58) and the potential beneficial effect of sauna was suggested(58). However, some time later the studies emphasized especially its risks and recommended caution in its use for cardiac patients(20-21,59) .
It is widely known that the vasodilators, such as angiotensin converting enzyme inhibitors, improve the CHF and increase the peripheral perfusion(60). Since the endothelial function is altered in CHF, the endothelium is considered as a new therapeutic target in heart failure(61). Hence, the angiotensin converting enzyme inhibitors(62-63) and physical training(64-65) improve the endothelial function in CHF patients. One of the proposed mechanisms for the alteration of the endothelium-dependent vasodilation would be through the decrease of the NO production in the peripheral vessels in CHF patients(51-53). The decrease of peripheral perfusion would decrease the shear stress(66). The shear stress is an important stimulus for NO production(67) and eNOS expression(32,68-70). On the other hand, the heat increases the cardiac output and improves the peripheral perfusion in CHF patients(18). Consequently, with the cardiac output improvement in CHF patients, an increase of the shear stress, NO production and eNOS expression are expected. In other words, an improvement in the endothelial function in the peripheral vessels and consequently in the cardiac function is observed. Probably, the thermal stimulation directly increases the eNOS expression, since in a recent study, it was shown that heat increases the arterial eNOS expression(71).
It was recently reported that the thermal therapy in 60ºC produced systemic arterial, pulmonary arterial and venous vasodilation, reduced the preload and afterload and improved the cardiac output and the peripheral perfusion(18), clinical symptoms(72-73), life quality(73), and cardiac arrhythmias in CHF patients(74).
In infants with severe CHF secondary to ventricular septal defect, the sauna therapy decreased the systemic vascular resistance and increased the cardiac output(75). The sauna benefits in CHF patients are possibly caused by the improvement of the vascular endothelial function and normalization of the neurohormonal system(76).
Ikeda et al.(77) in an experimental study with hamsters, discovered that the observed improvements in the sauna therapy are due to the eNOS expression increase in the arterial endothelium. Later, in another study(78), they showed that the thermal therapy with sauna improves the survival of the TO-2 cardiomyopathic hamsters with CHF and, more recently, showed that the repetitive therapy with sauna increases the eNOS expression and the nitric oxide production in artery endothelium of TO-2 cardiomyopathic hamsters with CHF(79).
SAUNA AND SYSTEMIC ARTERIAL HYPERTENSION
Davies(22) evaluated the pressure response in three hypertensive individuals during sauna exposure (85ºC, 15 min) and immediate exposure to 24ºC e 4ºC (cold phase) and observed the reduction of the blood pressure in one patient (154/80 mm Hg for 110/60 mm Hg) in the sauna and increase of blood pressure in the cold phase of the experiment. The two other hypertensive patients showed an increase of the blood pressure during sauna (non-significant) and in the cold phase (up to 252/147 mm Hg). In the author's opinion, the blood pressure does not increase significantly in sauna; it even decreases. Caution should be taken in the exposure to 4ºC.
Sohar et al.(21) did not find reduction in the systolic (SBP) and diastolic blood pressure (DBP) in 6 hypertensive patients during sauna and in 2/6 patients the SBP and the DBP importantly increased. According to the authors, the hypertensive individuals should seriously consider the sauna risks. Luurila et al.(80) did not find change in the SBP during sauna, but a decrease of the DBP in 11 young patients with essential arterial hypertension after 4 weeks of treatment with placebo, and single exposure to sauna in the end of the experiment was observed (85ºC and 14-20 min).
The repetitive exposure to sauna (80ºC, 1 h, 2x/day, 7 days) in healthy individuals did not change the systolic blood pressure, however, a reduction of the diastolic blood pressure was observed(12).
Recently, the effect of repeated thermal therapy was evaluated(8,81) (60ºC, 15 min sauna, 30 min with blanket in the supine position post-sauna, 1x/day, 2 weeks) in 25 men with at least one coronary risk factor (8 with arterial hypertension, 3 with mellitus diabetes, 8 with hypercholesterolemia and 15 smokers). It has been observed that 2 weeks of sauna exposure significantly reduced the systolic and diastolic blood pressures. (SBP: 128 ± 18 mm Hg for 124 ± 17 mm Hg, p < 0,01; DBP: 77 ± 17 mm Hg for 72 ± 16 mm Hg, p <0,05). Winterfeld et al.(82-83) reported the beneficial effect of sauna, regularly practiced in hypertensive patients. In a study with 180 hypertensive patients and with other cardiovascular diseases, the mean blood pressure was lowered from 162/110 mm Hg to 139/92 mm Hg(82). In another study(83) with 47 hypertensive individuals (sauna 2x/week, during 3 months) the blood pressure decreases from 166/110 mm Hg to 143/92 mm Hg.
SAUNA AND CORONARY HEART DISEASE
The endothelial dysfunction is a systemic disorder involved in the etiopathogenic of atherosclerosis and its complications(46,84). The endothelial function is altered in patients with lifestyle-related diseases, such as hypercholesterolemia, systemic arterial hypertension, diabetes mellitus, smoking and obesity(85).
The endothelial cells secrete various vasoactive substances such as nitric oxide, prostacyclin, endothelium derived hyperpolarizating factors, endothelin, thromboxane, growth factor, cytokines among others, and the endothelial function is determined by the balance of these substances(86). It is believed that the NO decrease and the increase of the NO degradation induce atherosclerosis and probably cardiovascular diseases(56,85,87).
Many studies have shown that sauna exposure is well tolerated in patients with stable coronary arterial disease (CAD)(16-17,82,88).
However, ventricular ectopic beats(16,18,20-21) and electrocardiographic alterations suggestive of ischemia were reported(16,20) and the recommendation about sauna use in patients with CAD is contradictory(20-21,23,89). Two Finnish studies(16,88) report that sauna was practiced after myocardial infarction or cardiac surgery. In a study with 117 patients after myocardial infarction, 87% practiced regular sauna bath immediately after hospital discharge(16). During 10 years follow-up, 82% of the patients continued to regularly practice sauna baths(88).
The angina pectoris incidence during daily physical activity was of 60%. Cardiac arrhythmias and electrocardiographic alterations suggestive of ischemia were significantly smaller during sauna comparing to an ergometric test(16).
Recently, Giannetti et al.(17) showed that sauna in patients with stable CAD is clinically well tolerated, although it is associated with reversible ischaemic alteration in the myocardial scintilography. Imamura et al.(81) reported that the repetitive treatment with sauna improved the endothelial function, altered in patients with coronary artery disease risk factors. Biro et al.(8) evaluated the effect of the repetitive treatment with sauna on lifestyle-related diseases and showed that the repeated thermal therapy improved the endothelial function and decreased body weight. As described above, the endothelial dysfunction presents the first step of the atherosclerosis and the authors suggest that the sauna treatment could prevent the atherosclerosis, especially if combined with diet and exercise.
RISK OF SAUNA IN HEART DISEASE PATIENTS
The clear contra-indication of sauna are: infections diseases, acute thoracic pain, unstable angina pectoris, recent myocardial infarction (4-6 week) descompensated heart failure, severe aortic stenosis, important cardiac arrhythmias, uncontrolled hypertension(16,88-89).
The effects of the use of b-blockers in sauna in healthy individuals(90-91) show that the blood pressure decreases significantly in the treated group, comparing to placebo, however, no important hypotension clinically was observed. Nevertheless, hypotensive reactions were reported in sauna with hypertensive patients treated with b -blocker(80).
In healthy individuals with transdermal nitroglycerin patches(92), an increased absorption of nitroglycerin in sauna and a significant decrease of the diastolic blood pressure were observed. The combination use of a short term nitroglycerin patch and sauna could importantly reduce the diastolic blood pressure and cause symptoms of cardiac ischemia. The stable CHF patients (ischemic and non-ischemic dilated cardiomyopathy) under maintenance treatment with the angiotensin converting enzyme inhibitors, diuretics, b-blockers and digital tolerate well sauna(16,18,72,76).
Hypertensive patients under treatment with calcium channel blockers(80), and non-hypertensive individuals treated with guanethidine(90) or captopril(91) tolerate well sauna. Sauna combined with alcohol intake increases the hypotension risk in healthy individuals(93), although it does not seem to cause cardiac arrhythmias.
ACCLIMATIZATION AND SAUNA
The studies about sauna originate mainly from countries with moderate and cold climate, and are conducted with individuals supposedly little adapted to heat. The sauna effect on acclimatized patients to tropical climate is questioned. The first step towards this answer was taken in our laboratory when the method of sauna thermal stimulus was standardized. Our results (submitted to publication) showed that the physiological responses of individuals living in tropical regions were similar to that ones found in the literature.
In resume, the systemic effects of sauna seem to occur via increase of the cardiac output and peripheral vasodilation, increase of the shear stress and improvement in the nitric oxide production via increase of eNOS expression. Such fact results in the improvement of the endothelial function, the common denominator found in virtually all cardiovascular diseases.
Sauna can be regarded as therapeutic option in patients with systemic arterial hypertension or cardiac failure and as prevention method against diseases related to endothelial dysfunction.
1. Lehtmets ML. The sauna bath. Am J Phys Med 1957;36:21-64. [ Links ]
2. Hasan J, Karvonen MJ, Piironen P. Special review. Part I. Physiological effects of extreme heat as studied in the Finnish "sauna" bath. Am J Phys Med 1966;45: 296-314. [ Links ]
3. Hasan J, Karvonen MJ, Piironen P. Special review. Part II. Physiological effects of extreme heat as studied in the Finnish "sauna" bath. Am J Phys Med 1967;46: 1226-46. [ Links ]
4. Kauppinen K, Vuori I. Man in the sauna. Ann Clin Res 1986;18:173-85. [ Links ]
5. Hannuksela M, Ellahham S. Benefits and risks of sauna bathing. Am J Med 2001; 110:118-26. [ Links ]
6. Kauppinen K. Facts and fables about the sauna. Ann N Y Acad Sci 1997;813:654-62. [ Links ]
7. Nguyen Y, Naseer N, Frishman WH. Sauna as a therapeutic option for cardiovascular disease. Cardiol Rev 2004;12:321-4. [ Links ]
8. Biro S, Masuda A, Kihara T, Tei C. Clinical implications of thermal therapy in lifestyle-related diseases. Exp Biol Med 2003;228:1245-9. [ Links ]
9. Helamaa E, Äikäs E. The secret of good "löyly". Ann Clin Res 1988;20:224-9. [ Links ]
10. Leppäluoto J. Human thermoregulation in sauna. Ann Clin Res 1988;20:240-3. [ Links ]
11. Ahonen E, Nousiainen U. The sauna and body fluid balance. Ann Clin Res 1988; 20:257-61. [ Links ]
12. Leppäluoto J, Tuominen M, Väänänen A, Karpakka, Vuori J. Some cardiovascular and metabolic effects of repeated sauna bathing. Acta Physiol Scand 1986;128: 77-81. [ Links ]
13. Leppäluoto J, Arjamaa O, Vuolteenaho O, Ruskoaho H. Passive heat exposure leads to delayed increase in plasma levels of atrial natriuretic peptide in humans J Appl Physiol 1991;71(2):716-20. [ Links ]
14. Vuori I. Sauna bather's circulation. Ann Clin Res 1988;20:249-56. [ Links ]
15. Rowell LB, Brengelmann GL, Blackmon JR, Murray JA. Redistribution of blood flow during sustained high skin temperature in resting man. J Appl Physiol 1970; 28:415-20. [ Links ]
16. Luurila OJ. Arrhythmias and other cardiovascular responses during Finnish sauna and exercise testing in healthy men and postmyocardial infarction patients. Acta Med Scand 1980;641(Suppl):1-60. [ Links ]
17. Giannetti N, Juneau M, Arsenault A, Behr MA, Grégoire J, Tessier M, et al. Sauna-induced myocardial ischemia in patients with coronary artery disease. Am J Med 1999;107:228-33. [ Links ]
18. Tei C, Horikiri Y, Park JC, Jeong JW, Chang KS, Toyama Y, et al. Acute hemodynamic improvement by thermal vasodilation in congestive heart failure. Circulation 1995;91:2582-90. [ Links ]
19. Kukkonen-Harjula K, Oja P, Laustiola K, Vuori I, Jolkkonen J, Siitonen S, et al. Haemodynamic and hormonal responses to heat exposure in a Finnish sauna bath. Eur J Appl Physiol 1989;58:543-50. [ Links ]
20. Taggart P, Parkinson P, Carruthers M. Cardiac responses to thermal, physical, and emotional stress. BMJ 1972;3:71-6. [ Links ]
21. Sohar E, Shoenfeld Y, Shapiro Y, Ohry A, Cabili S, et al. Effects of exposure to Finnish sauna. Israel J Med Sci 1976;12:1275-82. [ Links ]
22. Davies H. Cardiovascular effects of the sauna. Am J Phys Med 1975;54:178-85. [ Links ]
23. Shoenfeld Y, Sohar E, Ohry A, Shapiro Y. Heat stress: comparison of short exposure to severe dry and wet heat in saunas. Arch Phys Med Rehabil 1976;57:126-9. [ Links ]
24. Lammintausta R, Syvälahti E, Pekkarinen. Change in hormones reflecting sympathetic activity in the Finnish sauna. Ann Clin Res 1976;8:266-71. [ Links ]
25. Kosunen KJ, Pakarinen AJ, Kuoppasalmi K, Adlercreutz H. Plasma renin activity, angiotensin II, and aldosterone during intense heat stress. J Appl Physiol 1976; 41(3):323-7. [ Links ]
26. Pérgola, PE, Kellogg DL, Johanson JM, Kosiba WA, Solomon DE. Role of sympathetic nerves in the vascular effects of local temperature in human forearm skin. Am J Physiol 1993;265(3 Pt 2):H785-92. [ Links ]
27. Kellogg DL, Pérgola PE, Piest KL, Kosiba WA, Crandall CG, Grossmann M, et al. Cutaneous active vasodilation in humans is mediated by cholinergic nerve co-transmission. Circ Res 1995;77:1222-8. [ Links ]
28. Dietz NM, Rivera JM, Warner DO, Joyner MJ. Is nitric oxide involved in cutaneous vasodilation during body heating in humans? J Appl Physiol 1994;76:2047-53. [ Links ]
29. Kellogg DL, Zhao JL, Friel C, Roman LJ. Nitric oxide concentration increases in the cutaneous interstitial space during heat stress in humans. J Appl Physiol 2003; 94:1971-7. [ Links ]
30. Kellogg DL, Zhao JL, Coey U, Green JV. Acetylcholine-induced vasodilation is mediated by nitric oxide and prostaglandins in human skin. J Appl Physiol 2005; 98:629-32. [ Links ]
31. Moncada S, Higgs A. The L-arginine-nitric oxide pathway. N Engl J Med 1993; 329:2002-12. [ Links ]
32. Davis ME, Cai H, Drummond GR, Harrison DG. Shear stress regulates endothelial nitric oxide synthase expression through c-Src by divergent signaling pathways. Circ Res 2001;89:1073-80. [ Links ]
33. Kellogg DL, Crandall CG, Liu Y, Charkoudian N, Johnson M. Nitric oxide and cutaneous active vasodilation during heat stress in humans. J Appl Physiol 1998;85: 824-9. [ Links ]
34. Kellogg DL, Liu Y, Kosiba IF, O'Donnell D. Role of nitric oxide in the vascular effects of local warming of the skin in humans. J Appl Physiol 1999;86:1185-90. [ Links ]
35. Shastry S, Reed AS, Halliwill JR, Reed AS, Joyner J. Effects of nitric oxide synthase inhibition on cutaneous vasodilation during body heating in humans. J Appl Physiol 1998;85:830-4. [ Links ]
36. Shastry S, Minson CT, Wilson SA, Dietz NM, Joyner MJ. Effects of atropine and L-NAME on cutaneous blood flow during body heating in humans. J Appl Physiol 2000;88:467-72. [ Links ]
37. Clough GF. Role of nitric oxide in the regulation of microvascular perfusion in human skin in vivo. J Physiol 1999;516:549-57. [ Links ]
38. Fox RH, Edholm OG. Nervous control of the cutaneous circulation. Br Med Bull 1963;19:110-4. [ Links ]
39. Rowell LB. Reflex control of the cutaneous vasculature. J Invest Dermatol 1977; 69:154-66. [ Links ]
40. Cohn J. Abnormalities of peripheral sympathetic nervous system control in congestive heart failure. Circulation 1990;82:I59-I67. [ Links ]
41. Floras JS. Clinical aspects of sympathetic activation and parasympathetic withdrawal in heart failure. J Am Coll Cardiol 1993;22:72A-84A. [ Links ]
42. Benedict CR, Johnstone DE, Weiner DH, Bourassa MG, Bittner V, Kay R, et al. Relation of neurohumoral activation to clinical variables and degree of ventricular dysfunction: a report from the registry of studies on left ventricular dysfunction. J Am Coll Cardiol 1994;23:1410-20. [ Links ]
44. Kubo SH, Rector TS, Bank AJ, Williams RE, Heifetz SM. Endothelium-dependent vasodilation is attenuated in patients with heart failure. Circulation 1991; 84:1589-96. [ Links ]
45. Katz SD, Biasucci L, Sabba C, Strom JA, Jondeau G, Galvo M, et al. Impaired-endothelium-mediated vasodilation in the peripheral vasculature of patients with congestive heart failure. J Am Coll Cardiol 1992;19:918-25. [ Links ]
46. Drexler H, Hornig B. Endothelial dysfunction in human disease. J Mol Cell Cardiol 1999;31:51-60. [ Links ]
47. Mombouli JV, Vanhoutte PM. Endothelial dysfunction: from physiology to therapy. J Mol Cell Cardiol 1999;31:61-74. [ Links ]
48. Colombo PC, Banchs JE, Celaj S, Talreja A, Lachmann J, Malla S, et al. Endothelial cell activation in patients with decompensated heart failure. Circulation 2005; 111(1):58-62. [ Links ]
49. Morgan DR, Dixon LJ, Hanratty CG, Hughes SM, Leahey WJ, Rooney KP, et al. Impaired endothelium-dependent and -independent vasodilation in elderly patients with chronic heart failure. Eur J Heart Fail 2004;6(7):901-8. [ Links ]
50. Chong AY, Blann AD, Patel J, Freestone B, Hughes E, Lip GY. Endothelial dysfunction and damage in congestive heart failure: relation of flow-mediated dilation to circulating endothelial cells, plasma indexes of endothelial damage, and brain natriuretic peptide. Circulation 2004;110(13):1794-8. [ Links ]
51. Smith CJ, Sun D, Hoegler C, Roth BS, Zhang X, Zhao G, et al. Reduced gene expression of vascular endothelial NO synthase and cyclooxygenase-1 in heart failure. Circ Res 1996;78:58-64. [ Links ]
52. Agnoletti L, Curello S, Bachetti T, Malacarne F, Gaia G, Comini L, et al. Serum from patients with severe heart failure downregulates eNOS and is proapoptotic: role of tumor necrosis factor-alpha. Circulation 1999;100(19):1983-91. [ Links ]
53. Katz SD, Khan T, Zeballos GA, Mathew L, Potharlanka P, Knecht M, et al. Decreased activity of the L-arginine-nitric oxide metabolic pathway in patients with congestive heart failure. Circulation 1999;99:2113-7. [ Links ]
54. Kojda G, Harrison D. Interactions between NO and reactive oxygen species: pathophysiological importance in atherosclerosis, hypertension, diabetes and heart failure. Cardiovasc Res 1999;43:562-71. [ Links ]
55. Guzik TJ, West NE, Black E, McDonald D, Ratnatunga C, Pillai R, et al. Vascular superoxide production by NAD(P)H oxidase: association with endothelial dysfunction and clinical risk factors. Circ Res 2000;86:e85-e90. [ Links ]
56. Kawashima S, Yokoyama M. Dysfunction of endothelial nitric oxide synthase and atherosclerosis. Arterioscler Thromb Vasc Biol 2004;24:998-1005. [ Links ]
57. Berenson GS, Burch GE. The response of patients with congestive heart failure to a rapid elevation in atmospheric temperature and humidity. Am J Med Sci 1952;223:45-53. [ Links ]
58. Burch GE, Hyman A. Influence of a hot and a humid environment upon cardiac output and work in normal man and in patients with chronic congestive heart failure at rest. Am Heart J 1957;53:665-79. [ Links ]
59. El Sherif N, Shahwan L, Sorour AH. The effect of acute thermal stress on general and pulmonary hemodynamics in the cardiac patient. Am Heart J 1970;79:305-17. [ Links ]
60. The SOLVD Investigators: Effect of enalapril on survival in patients with reduced left ventricular ejection fractions and congestive heart failure. N Engl J Med 1991; 325(5):293-302. [ Links ]
61. Drexler H. Endothelium as a therapeutic target in heart failure. Circulation 1998; 98:2652-5. [ Links ]
62. Jeserich M, Pape L, Just H, Hornig B, Kupfer M, Münzel T, et al. Effect of long-term angiotensin converting enzyme inhibition on vascular function in patients with chronic congestive heart failure. Am J Cardiol 1995;76:1079-82. [ Links ]
63. Nakamura M, Funakoshi T, Arakawa N, Yoshida H, Makita S, Hiramori K. Effect of angiotensin-converting enzyme inhibitors on endothelium-dependent peripheral vasodilation in patients with chronic heart failure. J Am Coll Cardiol 1994;24:1321-7. [ Links ]
64. Hornig B, Maier V, Drexler H. Physical training improves endothelial function in patients with chronic heart failure. Circulation 1996;93:210-4. [ Links ]
65. Moyna NM, Thompson PD. The effect of physical activity on endothelial function in man. Acta Physiol Scand 2004;180(2):113-23. [ Links ]
66. Drexler H. Hypertension, heart failure, and endothelial function. Am J Cardiol 1998;82:20S-22S. [ Links ]
67. Rubanyi GM, Romero JC, Vanhoutte PM. Flow-induced release of endothelium-derived relaxing factor. Am J Physiol 1986;250:H1145-H1149. [ Links ]
68. Noris M, Morigi M, Donadelli R, Aiello S, Foppolo M, Todeschini M, et al. Nitric oxide synthesis by cultured endothelial cells is modulated by flow conditions. Circ Res 1995;76:536-43. [ Links ]
69. Nadaud S, Philippe M, Arnal JF, Michel JB, Soubrier F. Sustained increase in aortic endothelial nitric oxide synthase expression in vivo in a model of chronic high blood flow. Circ Res 1996;79:857-63. [ Links ]
70. Ballermann BJ, Dardik A, Eng E, Liu A. Shear stress and the endothelium. Kidney Int 1998;54(67):S100-S108. [ Links ]
71. Harris MB, Blackstone MA, Ju H, Virginia J, Venema VJ, Venema RC. Heat-induced increases in endothelial NO synthase expression and activity and endothelial NO release. Am J Physiol Heart Circ Physiol 2003;285:H333-H340. [ Links ]
72. Tei C, Tanaka N. Thermal vasodilation as a treatment of congestive heart failure: a novel approach. J Cardiol 1996;27:29-30. [ Links ]
73. Michalsen A, Lüdtke R, Bühring M, Spahn G, Langhorst J, Dobos G. Thermal hydrotherapy improves quality of life and hemodynamic function in patients with chronic heart failure. Am Heart J 2003;146(4):728-33. [ Links ]
74. Kihara T, Biro S, Ikeda Y, Fukudome T, Shinsato T, Masuda A, et al. Effects of repeated sauna treatment on ventricular arrythmias in patients with chronic heart failure. Circ J 2004;68:1146-51. [ Links ]
75. Sugahara Y, Ishii M, Muta H, Egami K, Akagi T, Matsuishi T. Efficacy and safety of thermal vasodilation therapy by sauna in infants with severe congestive heart failure secondary to ventricular septal defect. Am J Cardiol 2003;92:109-13. [ Links ]
76. Kihara T, Biro S, Imamura M, Yoshifuku S, Takasaki K, Ikeda Y, et al. Repeated sauna treatment improves vascular endothelial and cardiac function in patients with chronic heart failure. J Am Coll Cardiol 2002;39:754-9. [ Links ]
77. Ikeda Y, Biro S, Kamogawa Y, Yoshifuku S, Eto H, Orihara K, et al. Repeated thermal therapy upregulates arterial endothelial nitric oxide synthase expression in Syrian golden hamsters. Jpn Circ J 2001;65:434-8. [ Links ]
78. Ikeda Y, Biro S, Kamogawa Y, Yoshifuku S, Kihara T, Minagoe S, et al. Effect of repeated sauna therapy on survival in TO-2 cardiomyopathic hamsters with heart failure. Am J Cardiol 2002;90:343-5. [ Links ]
79. Ikeda Y, Biro S, Kamogawa Y, Yoshifuku S, Eto H, Orihara K, et al. Repeated sauna therapy increases arterial endothelial nitric oxide synthase expression and nitric oxide production in cardiomyopathic hamsters. Circ J 2005;69(6):722-9. [ Links ]
80. Luurila OJ, Kohvakka A, Sundberg S. Comparison of blood pressure response to heat stress in sauna in young hypertensive patients treated with atenolol and diltiazem. Am J Cardiol 1989;64:97-9. [ Links ]
81. Imamura M, Biro S, Kihara T, Yoshifuku S, Takasaki K, Otsuji Y, et al. Repeated thermal therapy improves impaired vascular endothelial function in patients with coronary risk factors. J Am Coll Cardiol 2001;38:1083-8. [ Links ]
82. Winterfeld HJ, Siewert J, Strangfeld D, Bohm D, Aurisch R, Engelmann U, et al. Effects of sauna therapy on patients with coronary heart disease with hypertension after bypass operation, after heart aneurysm operation and essential hypertension. Z Gesamte Inn Med 1993;48:247-50. [ Links ]
83. Siewert C, Siewert H, Winterfeld HJ, Strangfeld D. Changes of central and peripheral hemodynamics during isometric and dynamic exercise in hypertensive patients before and after regular sauna therapy. Z Kardiol 1994;83:652-7. [ Links ]
84. Ross R. Atherosclerosis: an inflammatory disease. N Engl J Med 1999;340:115-26. [ Links ]
85. Bonetti PO, Lerman LO, Lerman A. Endothelial dysfunction: a marker of atherosclerotic risk. Arterioscler Thromb Vasc Biol 2003;23:168-75. [ Links ]
86. Behrendt D, Ganz P. Endothelial function: from vascular biology to clinical applications. Am J Cardiol 2002;90(10C):40L-48L. [ Links ]
87. Paniagua OA, Bryant MB, Panza JA. Role of endothelial nitric oxide in shear stress-induced vasodilation of human microvasculature: diminished activity in hypertensive and hypercholesterolemic patients. Circulation 2001;103:1752-8. [ Links ]
88. Eisalo A, Luurila OJ. The Finnish sauna bath and cardiovascular diseases. Ann Clin Res 1988;20:267-70. [ Links ]
89. Luurila OJ. The sauna and the heart. J Intern Med 1992;231:319-20. [ Links ]
90. Iisalo E, Kanto J, Pihlajamaki K. Effects of propranolol and guanethidine on circulatory adaptation in the Finnish sauna. Ann Clin Res 1969;1:251-5. [ Links ]
91. Vanakoski J, Seppala T. Effects of a Finnish sauna on the pharmacokinetics and hemodynamic actions of propranolol and captopril in healthy volunteers. Eur J Clin Pharmacol 1995;48:133-7. [ Links ]
92. Barkve TF, Langseth-Manrique K, Bredensen J, Gjesdal K. Increased uptake of transdermal glyceryl trinitrate during physical exercise and during high ambient temperature. Am Heart J 1986;112:537-41. [ Links ]
93. Roine R, Luurila OJ, Suokas A, Heikkonen E, Koskinen P, Ylikahri R, et al. Alcohol and sauna bathing: effects on cardiac rhythm, blood pressure, serum electrolyte and cortisol concentrations. J Intern Med 1992;231:333-8. [ Links ]
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Received in 19/7/05. Final version received in 7/10/05. Approved in 25/1/06.
All the authors declared there is not any potential conflict of interests regarding this article.