Int J Biometeorol (2011) 55:229–234 DOI 10.1007/s00484-010-0328-y
ORIGINAL PAPER
Effects of aging on thermoregulatory responses and hormonal changes in humans during the four seasons in Japan Maki Sato & Dominika Kanikowska & Junichi Sugenoya & Yoko Inukai & Yuuki Shimizu & Naoki Nishimura & Satoshi Iwase
Received: 15 December 2009 / Revised: 14 April 2010 / Accepted: 27 April 2010 / Published online: 30 May 2010 # ISB 2010
Abstract Physiological functions are impaired in various organs in aged people, as manifest by, e.g., renal and cardiac dysfunction and muscle atrophy. The elderly are also at increased risk of both hypothermia and hyperthermia in extreme temperatures. The majority of those over 65 years old have elevated serum osmolality. Our hypothesis is that the elderly have suppressed osmolality control in different seasons compared to the young. Eight healthy young men and six healthy older men participated in this study. The experiments were performed during spring, summer, autumn and winter in Japan, with average atmospheric temperatures of 15–20°C in spring, 25–30°C in summer, 15–23°C in autumn and 5–10°C in winter. Each subject immersed his lower legs in warm water at 40°C for 30 min. Core (tympanic) temperature and sweat rate at chest were recorded continuously. Blood was taken pre-immersion to measure the concentrations of antidiuretic hormone, serum osmolality, plasma renin activity, angiotensin II, aldosterone, leptin, thyroid stimulating hormone, fT3 and fT4. The results suggested that the elderly have suppressed osmolality control compared to the young; osmolality was especially elevated in winter compared to the summer in elderly subjects. Therefore, particularly in the elderly, balancing fluid by drinking water should be encouraged to maintain euhydration status in winter. M. Sato (*) : D. Kanikowska : J. Sugenoya : Y. Inukai : Y. Shimizu : N. Nishimura : S. Iwase Department of Physiology, Aichi Medical University, Nagakute, Aichi 480-1195, Japan e-mail:
[email protected] D. Kanikowska Department of Biology and Environmental Studies, University of Medical Science, Poznan, Poland
Keywords Elderly . Seasonality . Osmolality . Antidiuretic hormone
Introduction The physiological functions of various organs are impaired in aged people, leading to, e.g., muscle atrophy and renal and cardiac dysfunction. The majority of those over 65 years old have elevated serum osmolality (O’Neill and Mclean 1992), as well as changes in the concentration of serum thyroid hormones, which are known to regulate the metabolic thermostat by changing the basal metabolic rate in aging (van den Beld et al. 2005). Higher osmolality induces blood viscosity and various diseases (Intaglietta 2009). Bhalla et al. (2000) demonstrated that high plasma osmolality in the acute phase of stroke is associated with an excessive mortality rate. The elderly are at increased risk of both hypothermia and hyperthermia in extreme temperatures (Van Someren 2007). The incidence of cardiovascular-related mortality increases in winter (Bhaskaran et al. 2009), particularly in the elderly (Collins 1986). Elderly subjects have lower metabolic heat production and an attenuated vasoconstrictor response to cold exposure, and fail to maintain their core temperature (DeGroot and Kenney 2007). Dehydration is also a frequent etiology associated with morbidity and mortality in elderly people, who have less sensation of thirst than the young (Remington and Hultman 2007). Reduced thirst and water intake have been observed in healthy elderly people during water deprivation, thermal dehydration and infusion of hypertonicity (McAloon Dyke et al. 1997). Reduced water consumption can affect the risk of urinary stone disease as well as overall health in the elderly (Kleiner 1999).
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Secretion of antidiuretic hormone (ADH) is stimulated mainly by a reduction in blood volume and increased plasma osmolality. ADH secretion is effected by changes in osmolality rather than similar changes in blood volume. Because ADH is correlated strongly with plasma osmolality, when osmolality increases, secretion of ADH is elevated. Aldosterone also contributes to water retention in the body by activating the secretion of plasma renin activity and angiotensin II. Leptin, a hormone present in adipose tissue, correlates with body fat in humans and other species (Maffei et al. 1995; Halaas et al. 1995). Serum leptin levels are higher in the elderly than in the young (Van Den Saffele et al. 1999). No study to date has focused on the seasonal differences in thermoregulatory and hormonal changes in aged people. Our hypothesis is that the elderly have suppressed osmolality control compared to the young, and that the level of suppression varies in different seasons.
Methods
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Measurements Body temperature Tympanic temperature was measured with a thermistor (Sensor Technica, Aichi, Japan) attached to the tympanic membrane. The ear pinna was filled with cotton to insulate the transfer of heat and moisture. Measurements of local sweat The sweat rate was measured at the chest using a capacitance hygrometer (HMI-14; Vaisala, Finland). A capsule covering a skin area of 8 cm2 was placed on the chest area and ventilated with dry nitrogen at a rate of 1.5lmin−1. Thermal sensation Subjective thermal sensation was queried every 5–10 min, both pre-immersion and during immersion, using the following scale: (1) cold, (2) cool, (3) slightly cool, (4) neutral, (5) slightly warm, (6) warm, (7) hot.
Subjects Sample collection and laboratory analyses Eight healthy young men [23±1.1 (mean ± SE) years, height: 172±1.4 cm, weight: 66.0±1.6 kg, body mass index (BMI): 22.2±0.6) and six healthy elder men (70±2.0 years, height: 162±2.3 cm, weight: 58.8±2.6 kg, BMI: 22.4±0.6) participated in this study. All subjects gave written informed consent before the experiment, which was approved by the Ethics Committee, Aichi Medical University. None of the subjects had either cardiovascular abnormalities or skin lesions. Protocol The experiments were performed during spring, summer, autumn and winter in Japan, 2007–2008, Aichi prefecture (latitude 35°10′ longitude 136°57.9′). The average atmospheric temperature is 15–20°C in spring, 25–30°C in summer, 15–23°C in autumn and 5–10°C in winter. The experiment was performed at the same time of day to avoid circadian influences. Each subject, wearing a Tshirt and shorts, immersed his lower legs in warm water at 40°C for 30 min in a sitting position in a climatic chamber set at 26°C and 50% relative humidity. Immersion of the legs in hot water has been established as a standard method to enhance sweating and body temperature (Kanikowska et al. 2010). Core (tympanic) temperature and sweat rate at chest were recorded continuously. Blood was taken pre-immersion after staying in a climatic chamber for 30 min.
Blood samples were taken pre-immersion to measure plasma ADH (Mitsubishi Kagaku Latron, Tokyo, Japan), plasma renin activity (PRA: SRL, Tokyo, Japan), angiotensin II (ANGII: PerkinElmer, Boston, MA; SRL) and aldosterone (ALD: SRL) by radio immunoassay (RIA) methods using commercial kits; serum thyroid stimulating hormone (TSH), serum free triiodothyronine (fT3) and free thyroxine (fT4) were measured using a commercially available electrochemiluminescence immunoassay according to the manufacturer’s instructions (ECLIA: Hitachi, Tokyo, Japan), and serum leptin (leptin: LINCO Research, St. Charles, MO) by RIA methods using commercial kits. Osmolality was measured by the freezing point method using serum (Arkray, Kyoto, Japan ). Data analysis Data are expressed as mean ± SE. The linear relationship between tympanic (core) temperature and sweat rate was compared with ANCOVA and Bonferroni’s post-hoc test (see Fig. 1). Sweat rates reflect sudomotor nerve activity derived from the central thermoregulatory mechanism, and sweat rate increases linearly with a rise in body temperature (Sugenoya et al. 1990). The linear relationship between osmolality and ADH was compared with ANCOVA and Bonferroni’s post-hoc test (see Fig. 2). Comparisons between the young and elderly during the four seasons
Int J Biometeorol (2011) 55:229–234
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eld
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0.2
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Tympanic temperature(°C) Fig. 1 Regression line relating sweat rate at chest to a given tympanic temperature during leg water immersion in young (A) and elderly (B) subjects in spring (■), summer (▲), autumn (□) and winter ( )
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were analyzed using two-way ANOVA (see Figs. 3, 4 and 5). Comparisons among seasons were analyzed using one-way ANOVA and Tukey’s post-hoc test. Comparisons among seasons during immersion were analyzed using two-way
ALD (pg/ml)
Sweat rate (mg/cm2/min)
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25
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Fig. 3 Concentration of plasma renin activity (PRA; top panel), angiotensin II (ANGII; middle panel) and aldosterone (ALD; bottom panel) in different seasons in young (■) and elderly (▲) subjects
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Fig. 2 Regression line relating antidiuretic hormone (ADH) to a given osmolality in summer and winter in young and elderly subjects. Young summer (■), young winter (□), elderly summer (▲) and elderly winter ( )
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summer autumn season
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Fig. 4 Leptin concentration in different seasons in young (■) and elderly (▲) subjects
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Int J Biometeorol (2011) 55:229–234 young 4
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TSH ( µ IU/ml)
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Fig. 6 Thermal sensation during water immersion in young (A) and elderly (B) during spring (■), summer (▲), autumn (□) and winter ( )
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fT4 (ng/dl)
hot
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Sweat rate 0.5
0 spring
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Fig. 5 Serum thyroid stimulating hormone (TSH) and serum free T3 and free T4 concentrations in different seasons in young (■) and elderly (▲) subjects
ANOVA (see Fig. 6). A P value of
