[Frontiers in Bioscience E4, 1975-1985, January 1, 2012]
The thermoneutral zone: implications for metabolic studies
Boris Kingma1, Arjan Frijns2, Wouter van Marken Lichtenbelt1
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TABLE OF CONTENTS
1. ABSTRACT
A thermoneutral environment is important for many human physiological studies. The thermoneutral zone (TNZ) is defined as the range of ambient temperatures without regulatory changes in metabolic heat production or evaporative heat loss. Many factors influence the thermoneutral zone, such as body composition, clothing, energy expenditure, age and gender. These factors have the potential to introduce bias in study results and therefore need to be taken into consideration in many metabolic studies or studies on obesity, medical conditions, thermal comfort or vigilance. Given new developments on the TNZ combined with historical views the aim of this review is to 1) provide insight in how the human TNZ is affected by internal and external factors, 2) indicate how skin blood flow characteristics could be used as an objective criterion for determining whether someone is in the thermoneutral zone, 3) explain implications of the TNZ on metabolic studies and 4) indicate future directions to enhance understanding of the TNZ, especially for the elderly and obese.
2. INTRODUCTION
2.1. Definition of thermoneutral zone
In 1902, Max Rubner was the first to put forward notion of a thermoneutral environment in mammals; he realized that his experiments on energy balance in nutrition could only be reproduced when the environmental conditions were equal (1). The concept was later adopted and applied to humans by Hardy and Dubois (1937) (2). They defined its lower limit as: "the maximum gradient (Tskin - Tair) over which the body can maintain its temperature without increase in heat production". In nude subjects they found a maximum gradient of 4.7�C at the lower limit of the neutral zone. This corresponded to an air temperature of 28.5�C. Below this limit heat loss regulation through vasoconstriction of the skin blood vessels was no longer sufficient to maintain body temperature (2, 3). Hardy and Dubois did not explicitly define an upper limit of the neutral zone, however their results indicated that evaporation was markedly increased at 32˚C (2). An explicit upper limit of the thermoneutral zone was later defined using heat stress (heart rate or increases in evaporative water loss as a criterion (4, 5).
Nowadays the definition of the thermoneutral zone is reformulated to: "the range of ambient temperature at which temperature regulation is achieved only by control of sensible (dry) heat loss, i.e. without regulatory changes in metabolic heat production or evaporative heat loss. The thermoneutral zone (TNZ) will therefore be different when insulation, posture or basal metabolism vary" (6). Here regulation of sensible heat loss refers to heat loss by conduction, convection or radiation (7). This means that thermoregulation in the thermoneutral zone only occurs through vasomotor control (8-10).
The concept of the thermoneutral zone is shown in Figure 1A. Below the lower critical temperature (LCT) of the TNZ heat balance can be achieved by up regulation of metabolic heat production (non-shivering thermogenesis and/or shivering). Above the upper critical temperature (UCT) heat balance can be achieved by increases in evaporation (sweating). In humans, the onset of sweating is accompanied with active vasodilation, which also contributes to the maintenance of heat balance by increasing heat transport from the body to the skin (11). Above the UCT heat production also increases due to increased blood circulation, activity of sweat glands and to increased body temperature (12).
For this review we only focus on the thermoneutral zone. Note that there is a clear distinction between the thermoneutral zone and the core interthreshold zone (CIZ). Both zones refer to a temperature range in which temperature regulation is achieved without increasing energy expenditure and without sweating. The difference between both zones is that the TNZ refers to the ambient temperature range, whereas the CIZ refers to the internal body temperature range (8).
2.2. Thermoneutral zone across studies
The TNZ has mainly been studied in animals (1, 13-17). However, some studies exist that focus on the human TNZ (2, 4, 5, 9, 18). Hardy and Dubois are the first to describe the TNZ in men and women (2, 18). Craig and Dvorak defined a TNZ in water (4). Hey and Katz studied the TNZ in newborns and Savage and Brengelmann studied skin blood flow in the TNZ (5, 9).
Research fields differ in defining the ambient temperature related to the TNZ. For instance, in the built environment operative temperature is used, which is a weighted combination of air temperature and radiative temperature (19-21). Others use air (dry bulb) temperature or control skin temperature directly by water immersion, or a water-perfused suit (22-34). Due to differences in thermal properties (mainly conduction) the thermoneutral zone in water is shifted upward compared to air (33˚C to 35.5˚C in water vs. 28.5˚C to 32˚C in air) (2, 4, 9, 10). In this review air temperature (i.e. dry bulb temperature) is used as the default TNZ medium.
2.3. Heat balance in the thermoneutral zone
In a steady state environment a subject can only be in the thermoneutral zone when heat production and heat loss are balanced. In classic textbooks on human thermoregulation heat balance is presented by the heat balance equation (35-37): S = (M - W) - (E + C + R +B), where heat storage (S) is defined as the difference between heat production (metabolism M corrected for work W) and heat loss (evaporation E, convection and conduction C, radiation R and respiration B).
Total heat production can be categorized into obligatory and facultative components (38). Obligatory components include: basal metabolic rate (BMR), the obligatory part of diet-induced thermogenesis (oDIT) and involuntary physical activity (e.g. feeding, posture). Facultative components include: the facultative part of diet induced thermogenesis (fDIT) and voluntary physical activity. Cold-induced thermogenesis is omitted here because it plays no role for subjects within the thermoneutral zone. BMR is the heat produced in an organism in a rested, awake, fasting and thermoneutral state and is needed to keep vital body processes functioning (6). In a resting sedentary male the energy expenditure is about 58Wm-2 (37). For comparison, typical values for energy expenditure in a reclining position or during sedentary activity are 46Wm-2 and 70Wm-2 respectively (21). Next, the obligatory part of DIT is necessary to process the food ingested. Note that DIT may also consist of a facultative part, i.e. burning excess calories and is the focus of many studies on obesity (39). DIT is typically 10% to 15% of total daily heat production (40). Physical activity thermogenesis (both voluntary and involuntary) occurs when muscles perform work; approximately 65% to 80% of energy associated with work is released as heat (41, 42).
Body heat is lost at the skin surface and by respiration. Heat produced within the body is transported to the skin by conduction through tissues and by blood perfusion (convection) (43, 44). At skin in distal areas (hands and feet) the primary heat influx comes from blood flow, whereas at more proximal sites (torso) heat is also delivered through conduction from underlying metabolically active tissues (liver, gut, etc) (45). In the thermoneutral zone the regulation of skin blood flow is crucial to maintain thermal balance.
Total skin blood flow can vary from close to 0 L min-1 in a cool environment to as high as 7.8 L min-1 in a hot environment (46, 47). In the thermoneutral zone, the amount of heat transported from core to skin by blood flow is estimated between 19Wm-2 (near the LCT) and 218Wm-2 (near the UCT) (9, 48).
The majority of skin blood flow studies have been performed on the forearm. Extrapolation of blood flow data to whole body skin has to be performed with caution because of large regional differences (45, 49-51). For instance, skin of the head and hands only comprises 7% of the total skin surface, yet between 25% and 27% of total skin blood flow occurs in these areas (52). Blood flow changes to environmental temperature variations are also dependent on the skin region. For example total hand blood flow increased 29-fold during body heating of cooled subjects, whereas forearm blood flow increased 3-fold(50). With respect to reduction in heat loss through vasoconstriction, regional differences reported are about -17% at the head and trunk, -25% at the arms and legs and about -50% at the hands and feet (53). These regional differences in skin blood flow and heat transport are attributed to arterio venous anastomoses (AVAs). AVAs are only present in glabrous skin (palms, ventral region of fingers, soles, forehead and lips) (45, 48). When these AVAs are opened, they form a bypass for blood from arterioles to venules, whereas the blood otherwise would only flow through high resistance capillaries at the skin surface. Hence, opening of AVAs greatly increases heat transport to the skin (45, 54, 55). In a thermoneutral environment blood flow in AVA rich glabrous skin has a characteristic fluctuation with 2 to 3 vasoconstrictions per minute (56). This property, which is found in glabrous skin alone, can be used to measure whether a subject is within the TNZ (see practical considerations) (57).
Overall, the ability of skin to control heat loss is influenced by the vascular anatomy, flow rate, regulation of skin blood flow and the exposure to the environment. See for reviews on skin blood flow regulation Kellogg (2006) and Johnson and Kellogg (2010) (11, 58). Although the area of glabrous skin is small relative to the entire body surface, its importance for heat loss regulation is large. This is due to the above-mentioned AVA's and because glabrous skin areas are normally the skin areas that are actually exposed to the environment. Clothing covers most other parts of the skin. Therefore, in clothed humans, glabrous skin areas are considered as major contributors to heat regulation in the thermoneutral zone (59).
3. MODULATING FACTORS
The thermoneutral zone is influenced by several internal and external factors. Here we address the modulating effect of body composition, clothing, energy expenditure, age and gender on the TNZ. In Figure 1 the influences of these factors on the TNZ are shown. For comparisons the standard TNZ (LCT0 = 28.6˚C and UCT0 = 32.0˚C) was taken from a 28 years old nude male subject with standard basal metabolic rate (BMR0=58W/m2) and subcutaneous fat thickness (SFT0=7.5mm). The subscript "0" was used to denote the value of the standard, or reference subject. Where possible temperature data from literature was used, otherwise the theoretical influence was calculated as described in the corresponding sections.
Insulation of tissues can be viewed as a series of thermal resistances (inverse of conductivity) of muscle and subcutaneous fat (60). The thermal resistance of tissues is a function of both the conductivity and blood perfusion (see for an overview of heat conductivities of tissues refs. (61, 62)). In general fat mass is positively related to tissue insulation (63). For limb muscle the story is more complicated. In resting conditions, limb muscle tissue is a major factor of the insulative capacity of the body explaining up to 70% of the total insulation (28, 60, 64). However, the insulative effect of limb muscle is only present with reduction of blood flow. During exercise in cold conditions blood flow is maintained in limb muscle, which prevents insulation (60). Under resting conditions, subjects with higher limb muscle mass also have a higher volume of blood -and corresponding heat transport- flowing from the body to the limbs. Therefore, limb muscle mass is negatively associated with tissue insulation (63).
Tissue insulation is also influenced by the subcutaneous fat layer, which serves as an insulating layer between muscle and skin (25, 63-65). The thickness of the subcutaneous fat layer is by far the most important factor for the lower critical temperature when subjects are immersed in water (60). For reviews on the influence of tissue type on tissue insulation and temperature regulation see Rennie (1988) and Anderson (1999) (60, 64).
Rennie (1988) showed that the lower critical water temperature of the TNZ can be expressed as a function of the thickness of the subcutaneous fat + skin layer (SFT) (i.e. for subjects with equal heat production and muscle mass) (60). Here we use the same approach to show the influence of sub cutaneous fat thickness on the air TNZ (Figure 1B). It is assumed that all heat produced by the body is lost to the environment (windspeed≤0.05m/s), without the need for regulatory increases in evaporation. The LCT and UCT were calculated relative to the standard subject as follows: LCT = LCT0 + 0.92�BMR0�((SFT0-SFT)/kLCT) and UCT = UCT0 + 0.92�BMR0�((SFT0-SFT)/kUCT), where, k (Wm-1˚C) is the conductivity of the subcutaneous fat + skin layer. The factor 0.92 is used to correct for respiratory heat loss, i.e. 8% of total heat production (60). Near the LCT the thermal conductivity of subcutaneous fat and skin is lowest due to vasoconstriction (kLCT = 0.28 Wm-1˚C-1 from (28)). Near the UCT the thermal conductivity of subcutaneous fat and skin is higher due increased blood flow (kUCT = 0.73 Wm-1˚C-1 from (28)).
Although the calculation above does not account for regional differences in adiposity and other complexities, it does illustrate the impact of the subcutaneous fat layer on the thermoneutral zone. For instance, a subcutaneous fat thickness of 40mm (quite common in obesity (66)) results in a LCT of 22˚C. Note that LCT of 22˚C is for a nude subject. Inclusion of light clothing (0.5clo) lowers the LCT further to about 18˚C. With a lower LCT compared to lean subject, the obese may have a reduced need for cold-induced increases in energy expenditure, which in turn increases the likelihood of sustained overweight (67). Indeed, studies indicate that subjects with increased fat mass (both subcutaneous fat thickness and whole body fat percentage) are capable of enduring lower ambient temperatures without significantly increasing heat production (60, 68), or that the cold induced heat production is negatively related to the thickness of subcutaneous fat (25, 65, 69). In relation to the UCT, no study directly measured the UCT in obese subjects. Yet, it has been suggested that obese may have increased sweat gland activity at normal room temperature (Tair=20-22˚C) relative to lean subjects (70).
Body composition also influences the distribution of heat loss. Increased body fat is associated with decreased proximal temperatures (trunk) and increased distal skin temperatures (hands and feet) (71, 72), thereby decreasing heat loss from proximal sites and increasing heat loss from distal sites. This is of special relevance when thermoneutrality is obtained by means of local cooling (e.g. automotive industry). For instance, in obese more body heat can be extracted by hand cooling than in lean subjects.
One of the functions of clothing is to keep the microclimate around the body comfortable for a range of ambient temperatures. Factors that influence the insulation of clothing are: dry resistance, evaporative resistance, compression from wind and movements (37). Extensive databases on the thermal properties of clothing are available (73). The unit used to express the insulation value of clothing is the "Clo" (1 Clo = 0.155m2˚CW-1 = equivalent to a business suit). A simplified example of the impact of clothing on our thermal environment shows that in a steady state environment of a sedentary resting subject, clothing of 1 Clo lowers required ambient temperature by 9.7˚C (0.92x58Wm-2 x (0.155m2˚CW-1 +(7.5x10-3m / 0.28Wm-1˚C-1)) ≈ 9.7˚C; again the factor 0.92 is used to correct metabolic heat production for respiratory heat loss). Hence, relative to a nude subject, the ambient temperature of the thermoneutral zone is shifted downward by 9.7˚C, which results in a thermoneutral temperature of around 20.3˚C (30.0˚C - 9.7˚C = 20.3˚C). In summary, the ambient temperature of the TNZ is lowered according to the insulation provided by clothing (Figure 1C).
In resting conditions energy expenditure is influenced by factors such as diet, circadian rhythm, posture and acclimatization. These factors may cause a shift in the potential for temperature regulation by sensible heat loss, which may introduce a bias in studies on metabolism, skin blood flow, vigilance and thermal comfort.
Thermal balance can only be maintained when heat production is equal to heat loss. Therefore the TNZ is shifted to lower temperatures when energy expenditure increases (57, 74). Vice versa, the TNZ shifts to higher temperatures when energy expenditure decreases (see Figure 1D). The LCT and UCT were calculated relative to the standard subject as follows: LCT = LCT0 + 0.92�(BMR0-BMR)�(SFT0/kLCT) and UCT = UCT0 + 0.92�(BMR0-BMR)�(SFT0/kUCT).
Digestion of nutrients is associated with an increase in metabolic rate between +10% to +15% of total daily energy expenditure depending on the nutrients ingested (40, 75). However, the acute thermogenic effect of diet can be much higher (+25%) (76). To maintain thermal balance, heat loss should also increase with 25% and therefore the TNZ shifts to lower temperatures.
With respect to the influence of circadian rhythm on the TNZ: over the course of a day body temperature naturally follows both heat production and heat loss (77-80). Heat production is phase shifted approximately 1.2h ahead of heat loss, with a maximum at noon (+10% of mean 24h heat production) and a minimum at night (-6% of mean 24h heat production) (77, 78). On top of this circadian redistribution of skin blood flow (i.e. from trunk to the extremities) causes minimum internal heat conductance at day (-9% of mean 24h internal heat conduction) and maximum heat conductance at night (+5% of mean 24h internal heat conduction) (79). Therefore, the TNZ is lowest at noon and highest at night.
Posture affects both heat production and heat loss (81-83). In supine position heat production is decreased in muscles that are used during upright position (about -2% heat produced in thermoneutral conditions and about -19% heat produced in cool conditions) (82). As a consequence the TNZ in supine position is shifted upward relative to the TNZ in upright position. Furthermore, arterial baroreceptor reflexes that accompany a supine position cause vasodilatation both in muscle and skin tissue (+57% blood flow in femoral artery), which decreases insulation and contributes to the upward shift of the TNZ in supine vs. upright position (84).
Another factor that influences the TNZ is acclimatization. Relative to non-acclimatized people, those that are acclimatized to cold conditions maintain a significantly greater BMR (i.e. under thermoneutral conditions) (85). As a consequence, the TNZ is shifted downward in cold acclimatized vs. non-acclimatized subjects. The acclimatization can be induced by geography (e.g. tropic vs. arctic regions), altitude and by season (e.g. summer vs. winter in non-equatorial latitudes). With respect to seasonal acclimatization, increased BMR and increased sleeping metabolic rate have been measured in winter (+6% heat production for a 10˚C decrease in air temperature) (86, 87). Thus, depending on the season-induced acclimatization, the TNZ in winter is shifted to lower temperatures relative to the summer TNZ. However, in developed countries there is a continuing trend of increasing indoor temperatures, which reduces seasonal cold acclimatization and may have a causal relation to the increases in obesity prevalence (67). Moreover, obese subjects have a lower LCT due to increased insulation, which may further reduce the need for cold acclimatization and in turn may contribute to sustained overweight.
In neonates the thermoneutral zone depends greatly on the birth weight and ranges between 35.0˚C to 35.5˚C in 1kg babies and 33.8˚C to 34.5˚C in 2kg babies (5). Within about a month the TNZ ranges from 32.0˚C to 34.0˚C. Until adulthood the TNZ continues to decrease to the range from 28.6˚C to 32.0˚C. With further increasing age, changes occur in various factors that affect thermoregulation. With respect to body composition, lean mass is in general decreased in elderly, whereas fat mass is increased, and subcutaneous fat mass is decreased (88). Secondly, elderly show decreased temperature sensitivity (89, 90) and impaired neural control of vasoconstriction (10, 23, 25, 91-93). On top of that, results suggest that control of skin blood flow in elderly is not able to maintain thermal balance in the same skin temperature range as young adults (10). However, vasoconstriction might not be affected by age in all skin regions (31, 94, 95), and there are indications that the blunting effects of ageing on thermoregulation can partly be compensated for by physical fitness (31, 96, 97). Nevertheless, age is associated with impaired thermoregulation even during mild thermal challenges (23).
Although the majority of studies that describe age effects on thermoregulation relate to the internal temperature range for thermoregulation and not to the ambient temperature range, it does indicate that elderly have an impaired ability to maintain thermal balance in the cold and in the heat compared to young adults (23, 25, 98, 99). Elderly either fail to sense the thermal imbalance and/or they fail to respond appropriately (80). In conclusion, on average, elderly respond slower to slight disturbances in thermal balance and are not able to maintain thermal balance with vasomotor responses in the same temperature range as young adults. Consequently, the thermoneutral zone for elderly is narrower than for young adults, although the exact range has not yet been determined (Figure 1E).
Gender differences in thermoregulation are mainly explained by the differences in body characteristics and endocrinal physiology (26, 100). In general, yet with large individual differences, women have a larger surface to mass ratio, which implies that women are more prone to heat loss (100). On the other hand, women have a higher whole body and subcutaneous fat content than men, which in turn increases insulation (26, 64). Interestingly, in men, increased body fat is associated with lower proximal skin (torso and abdomen) temperatures and higher distal (hand and foot) temperatures (71, 72). Women are known to have colder skin at distal areas, despite the increased body fat content relative to men (101). Part of this effect can be attributed to reproductive hormones and the menstrual phase (102). Progesterone levels increase during the luteal phase, and cause an increased internal threshold temperature for vasodilation and sweating (102, 103). As a consequence, the extremities remain colder, more body heat is preserved and core body temperature rises. Vice versa, increased estrogen during the follicular phase decreases the threshold for vasodilatation, which causes increased distal temperature and lowers core temperature.
Unfortunately these shifts in CIZ cannot be directly translated to shifts in the TNZ. A longitudinal study showed that in lightly dressed early pregnant women (i.e. prolonged high threshold for vasodilation) their TNZ was not statistically different from their post-partum follicular-phase (low threshold for vasodilation) TNZ (57). This suggests that there is no shift in the TNZ due to a change in sex hormones. However, during pregnancy, as the metabolic rate of the fetus and mother increased, there was a marked decrease in ambient temperature to reach TNZ (26.64˚C �0.64˚C at week 8 vs. 22.67˚C �0.58˚C at week 36).
Relative to men, thermoregulatory responses to cold and heat are shifted to higher body temperatures (104). Also women are reported to initiate sweating at higher heat loads than males (105, 106). Because of intrinsic gender related differences in body characteristics these internal temperature thresholds cannot be translated directly into changes within the TNZ. Nevertheless, semi-nude women are reported to increase metabolic heat production already when air temperature is decreased below 31˚C, whereas in men the LCT was 28.5˚C (18). Thus in general, relative to men, the thermoneutral zone of women is shifted upward. It is not yet known whether the width of the TNZ is affected.
4.
Due to the complex interactions of factors that influence the TNZ it is often difficult to make an a priori definition of the thermoneutral zone for any individual subject. When designing an experiment it would be much more practical to define an approximate thermoneutral environment based on the average subject characteristics (e.g. slightly warmer environment for women than for men), and actually measure during a test whether a subject is indeed within the thermoneutral zone. The environmental conditions can then be adjusted to the needs of the individual subject. This concept is used in some human studies (56, 57) and also in animal (rat) thermo-physiology (13, 17). For instance, the study of Hartgill et al. (2011) was conducted in a climatic chamber, which allowed for temperature adjustment to each subject. However, most metabolic studies do not use this concept, which might significantly affect the outcome of experiments. For instance, in nutrition it has been reported that resting metabolic rate (while in fasting condition) of clothed female subjects (wearing a thin cotton trouser suit) was higher at 22˚C than at 28˚C (4.329�0.152 kJ min-1 vs. 3.899�0.122 kJ min-1 respectively). However, after consumption of a meal no difference in resting metabolic rate was observed anymore (107). The author reasoned that before the meal, part of the capacity for diet-induced thermogenesis (DIT) was already used to maintain thermal balance at 22˚C (i.e. cold induced thermogenesis). Further, after the meal, the full capacity for facultative thermogenesis was reached both at 22˚C and 28˚C. Calculation of DIT is performed relative to the baseline resting energy expenditure. Hence, when only measurements at 22˚C would have been observed, there would have been a significant underestimation of the diet-induced thermogenesis. Since most metabolic studies do not incorporate the effects of TNZ-shifts, part of the high variability observed in diet-induced thermogenesis may be attributed to these temperature artifacts.
Relatively simple techniques exist to measure whether a subject is in its TNZ. The basic assumption is that in the TNZ the skin alternates between states of net vasodilation and net vasoconstriction, yet neither state dominates. In a thermoneutral environment blood flow in AVA rich glabrous skin has a characteristic fluctuation with 2 to 3 vasoconstrictions per minute (56). These fluctuations are directly observable by measuring skin blood flow (e.g. by Laser Doppler flowmetry, see Figure 2) or skin surface temperature (13). The major advantage of adopting these criteria for thermoneutrality in humans is that one has an objective criterion to determine whether an individual subject is in the TNZ.
In conclusion, to study temperature-induced responses in different groups (male vs. female; lean vs. obese), both groups should be relatively equidistant from their thermoneutral zone.
Further research is warranted to measure the effects of age, gender and obesity on the TNZ. The practical impact of these studies can be widespread from individual health to increased productivity and energy conservation in buildings. For instance, in elderly even a mild cold environment can contribute to health problems (108, 109). The same accounts for elderly in warm conditions (110). Precise knowledge of the TNZ is therefore especially important for those elderly that live in care houses.
Although there is some evidence that the lower critical temperature (LCT) of the TNZ is shifted upward in females vs. males, it is not known whether the UCT is also shifted upward. This is important to know, because TNZ differences between males and females could contribute to large variations observed in metabolic or nutritional studies (1, 107).
For obese subjects experimental results showed that the LCT is lowered with increased adiposity (60). Recently it has been suggested that effects of cold exposure on body weight could be studied in context of possible health strategies to tackle obesity (67). For such studies, precise knowledge of the TNZ is warranted. Moreover, since ambient temperature greatly influences the productivity of workers, with an optimum productivity in the TNZ (111), obese subjects might need cooler temperatures for optimal performance relative to their lean counterparts.
5.
For each individual the thermoneutral zone is influenced by factors such as body composition, clothing, energy expenditure, age and gender. Therefore, the thermoneutral zone varies between conditions and between individual subjects. Metabolic studies in which thermoregulatory responses affect the outcome should incorporate individual variations of the thermoneutral zone in study designs. Otherwise, biased study results may cause invalid conclusions. This implies that for sound comparison between subjects, the environmental conditions should be attuned to each individual. Characteristic fluctuations in glabrous skin blood flow can be further explored as an objective criterion to measure whether a subject is within the thermoneutral zone. Already slight deviations from the thermoneutral zone may affect health and productivity. Therefore further research on the thermoneutral zone is warranted, especially for the obese and elderly.
6. ACKNOWLEDGEMENTS
The authors would like to thank L. Schellen, G. Vijgen, M. Vosselman and A. v.d. Lans for their interesting contributions during discussions on the thermoneutral zone. This review was supported by AgentschapNL EOS-LT 03001 (W.D. van Marken Lichtenbelt).
1. M. Rubner: The laws of energy conservation in nutrition. Academic Press, INC. (London) LTD., London (1982)
2. J. D. Hardy and E. F. Dubois: Basal metabolism, radiation, convection and vaporization at temperatures of 22 to 35C. The Journal of Nutrition, 15(5), 477-497 (1937)
3. J. D. Hardy and E. F. Dubois: Regulation of Heat Loss from the Human Body. Proc Natl Acad Sci U S A, 23(12), 624-31 (1937)
doi:10.1073/pnas.23.12.624
doi:10.1073/pnas.23.12.631
4. A. B. Craig, Jr. and M. Dvorak: Thermal regulation during water immersion. J Appl Physiol, 21(5), 1577-85 (1966)
PMid:5923229
5. E. N. Hey and G. Katz: The optimum thermal environment for naked babies. Arch Dis Child, 45(241), 328-34 (1970)
doi:10.1136/adc.45.241.328
PMid:5427846 PMCid:1647588
6. T. C. IUPS: Glossary of terms for thermal physiology. Third edition. Revised by The Commission for Thermal Physiology of the International Union of Physiological Sciences (IUPS Thermal Commission). The Japanese Journal of Physiology, 51(2), 245-80 (2001)
7. F. P. Incropera, D. P. DeWitt, T. L. Bergman and S. A. Lavine: Introduction to Heat Transfer. John Wiley & Sons, Inc., (2007)
8. I. B. Mekjavic and O. Eiken: Contribution of thermal and nonthermal factors to the regulation of body temperature in humans. J Appl Physiol, 100(6), 2065-72 (2006)
doi:10.1152/japplphysiol.01118.2005
PMid:16410380
9. M. V. Savage and G. L. Brengelmann: Control of skin blood flow in the neutral zone of human body temperature regulation. J Appl Physiol, 80(4), 1249-57 (1996)
PMid:8926253
10. G. L. Brengelmann and M. V. Savage: Temperature regulation in the neutral zone. Ann N Y Acad Sci, 813, 39-50 (1997)
doi:10.1111/j.1749-6632.1997.tb51670.x
PMid:9100860
11. D. L. Kellogg, Jr.: In vivo mechanisms of cutaneous vasodilation and vasoconstriction in humans during thermoregulatory challenges. J Appl Physiol, 100(5), 1709-18 (2006)
doi:10.1152/japplphysiol.01071.2005
PMid:16614368
12. C. F. Consolazio, L. R. Matoush, R. A. Nelson, J. B. Torres and G. J. Isaac: Environmental temperature and energy expenditures. Journal of Applied Physiology, 18, 65-8 (1963)
PMid:14022656
13. A. A. Romanovsky, A. I. Ivanov and Y. P. Shimansky: Selected contribution: ambient temperature for experiments in rats: a new method for determining the zone of thermal neutrality. J Appl Physiol, 92(6), 2667-79 (2002)
PMid:12015388
14. D. P. Clarkson, C. L. Schatte and J. P. Jordan: Thermal neutral temperature of rats in helium-oxygen, argon-oxygen, and air. Am J Physiol, 222(6), 1494-8 (1972)
PMid:5030207
15. K. Morgan: Thermoneutral zone and critical temperatures of horses. Journal of Thermal Biology, 23(1), 59-61 (1998)
doi:10.1016/S0306-4565(97)00047-8
16. Y. Smith and O. B. Kok: A Suggested Thermoneutral Zone for African Lions (Panthera leio Linnaeus, 1758) in the Southwestern Kalahari, Namibia. Pakistan Journal of Biological Sciences, 9(13), 2535-2537 (2006)
doi:10.3923/pjbs.2006.2535.2537
17. M. C. Almeida, A. A. Steiner, N. C. Coimbra and L. G. Branco: Thermoeffector neuronal pathways in fever: a study in rats showing a new role of the locus coeruleus. J Physiol, 558(Pt 1), 283-94 (2004)
doi:10.1113/jphysiol.2004.066654
PMid:15146040 PMCid:1664907
18. J. D. Hardy and E. F. Du Bois: Differences between Men and Women in Their Response to Heat and Cold. Proc Natl Acad Sci U S A, 26(6), 389-98 (1940)
doi:10.1073/pnas.26.6.389
19. P. O. Fanger: Assessment of man's thermal comfort in practice. Br J Ind Med, 30(4), 313-24 (1973)
PMid:4584998 PMCid:1069471
20. L. Schellen, W. D. van Marken Lichtenbelt, M. G. Loomans, J. Toftum and M. H. de Wit: Differences between young adults and elderly in thermal comfort, productivity, and thermal physiology in response to a moderate temperature drift and a steady-state condition. Indoor Air, 20(4), 273-83 (2010)
doi:10.1111/j.1600-0668.2010.00657.x
PMid:20557374
21. ISOTC159: Ergonomics of the thermal environmet - Analytical determination and interpretation of thermal comfort using calculation of the PMV and PPD indices and local thermal comfort criteria (ISO 7730:2005,IDT). ISO copyright office, Geneva (2005)
22. H. A. Daanen, E. van de Vliert and X. Huang: Driving performance in cold, warm, and thermoneutral environments. Appl Ergon, 34(6), 597-602 (2003
doi:10.1016/S0003-6870(03)00055-3
23. D. W. deGroot and W. L. Kenney: Impaired defense of core temperature in aged humans during mild cold stress. Am J Physiol Regul Integr Comp Physiol, 292(1), R103-8 (2007)
doi:10.1152/ajpregu.00074.2006
PMid:17197640
24. W. D. van Marken Lichtenbelt, J. W. Vanhommerig, N. M. Smulders, J. M. Drossaerts, G. J. Kemerink, N. D. Bouvy, P. Schrauwen and G. J. Teule: Cold-activated brown adipose tissue in healthy men. N Engl J Med, 360(15), 1500-8 (2009)
doi:10.1056/NEJMoa0808718
PMid:19357405
25. G. M. Budd, J. R. Brotherhood, A. L. Hendrie and S. E. Jeffery: Effects of fitness, fatness, and age on men's responses to whole body cooling in air. J Appl Physiol, 71(6), 2387-93 (1991)
PMid:1778937
26. P. Tikuisis, I. Jacobs, D. Moroz, A. L. Vallerand and L. Martineau: Comparison of thermoregulatory responses between men and women immersed in cold water. J Appl Physiol, 89(4), 1403-11 (2000)
PMid:11007575
27. A. Veicsteinas, G. Ferretti and D. W. Rennie: Superficial shell insulation in resting and exercising men in cold water. J Appl Physiol, 52(6), 1557-64 (1982)
PMid:7107465
28. M. B. Ducharme and P. Tikuisis: In vivo thermal conductivity of the human forearm tissues. J Appl Physiol, 70(6), 2682-90 (1991)
PMid:1885465
29. Y. S. Park, D. W. Rennie, I. S. Lee, Y. D. Park, K. S. Paik, D. H. Kang, D. J. Suh, S. H. Lee, S. Y. Hong and S. K. Hong: Time course of deacclimatization to cold water immersion in Korean women divers. J Appl Physiol, 54(6), 1708-16 (1983)
PMid:6874495
30. A. C. Burton and H. C. Bazett: A study of the average temperature of the tissues, of the exchanges of heat and vasomotor responses in man by means of a bath calorimeter. Am. J. Physiol, 117, 36-54 (1936)
31. B. R. Kingma, A. J. Frijns, W. H. Saris, A. A. van Steenhoven and W. D. van Marken Lichtenbelt: Cold-induced vasoconstriction at forearm and hand skin sites: the effect of age. Eur J Appl Physiol, 109(5), 915-21 (2010)
doi:10.1007/s00421-010-1414-x
PMid:20300768 PMCid:2892071
32. P. E. Pergola, D. L. Kellogg, Jr., J. M. Johnson and W. A. Kosiba: Reflex control of active cutaneous vasodilation by skin temperature in humans. Am J Physiol, 266(5 Pt 2), H1979-84 (1994)
PMid:8203597
33. J. M. Johnson, P. E. Pergola, F. K. Liao, D. L. Kellogg, Jr. and C. G. Crandall: Skin of the dorsal aspect of human hands and fingers possesses an active vasodilator system. J Appl Physiol, 78(3), 948-54 (1995)
PMid:7775340
34. C. S. Thompson and W. L. Kenney: Altered neurotransmitter control of reflex vasoconstriction in aged human skin. J Physiol, 558(Pt 2), 697-704 (2004
doi:10.1113/jphysiol.2004.065714
PMid:15181162 PMCid:1664979
35. A. C. Burton and O. G. Edholm: Man in a cold environment, . Edward Arnold (Publishers) LTD., London (1955)
36. C. Gisolfi and F. Mora: The Hot Brain: Survival, Temperature and the Human Body. Cambridge, MIT Press, (2000)
37. K. Parsons: Human Thermal Environments. Taylor & Francis, (2003)
38. W. D. van Marken Lichtenbelt and P. Schrauwen: Implications of Non-shivering Thermogenesis for Energy Balance Regulation in Humans (2011)
39. S. L. Wijers, W. H. Saris and W. D. van Marken Lichtenbelt: Individual thermogenic responses to mild cold and overfeeding are closely related. J Clin Endocrinol Metab, 92(11), 4299-305 (2007)
doi:10.1210/jc.2007-1065
40. N. R. Stob, C. Bell, M. A. van Baak and D. R. Seals: Thermic effect of food and beta-adrenergic thermogenic responsiveness in habitually exercising and sedentary healthy adult humans. J Appl Physiol, 103(2), 616-22 (2007)
doi:10.1152/japplphysiol.01434.2006
PMid:17463294
41. G. A. Gaesser and G. A. Brooks: Muscular efficiency during steady-rate exercise: effects of speed and work rate. J Appl Physiol, 38(6), 1132-9 (1975)
PMid:1141128
42. D. C. Poole, G. A. Gaesser, M. C. Hogan, D. R. Knight and P. D. Wagner: Pulmonary and leg VO2 during submaximal exercise: implications for muscular efficiency. J Appl Physiol, 72(2), 805-10 (1992)
PMid:1559962
43. H. H. Pennes: Analysis of tissue and arterial blood temperatures in the resting human forearm. J Appl Physiol, 1(2), 93-122 (1948)
PMid:18887578
44. E. H. Wissler: Pennes' 1948 paper revisited. J Appl Physiol, 85(1), 35-41 (1998)
PMid:9655751
45. I. Roddie: Circulation to skin and adipose Tissue. In: Handbook of Physiology, A critical, comprehensive presentation of physiological knowledge and concepts. Ed J. T. Shepherd, F. M. Abboud&S. R. Geiger. American Physiological Society, Bethesda, Maryland (1983)
46. J. D. Hardy and G. F. Soderstrom: Heat loss from the nude body and peripheral blood flow at temperatures of 22C to 35C. Journal of Nutrition, 16(5), 494-510 (1938)
47. L. B. Rowell: Human cardiovascular adjustments to exercise and thermal stress. Physiol Rev, 54(1), 75-159 (1974)
PMid:4587247
48. J. M. Johnson, G. L. Brengelmann, J. R. Hales, P. M. Vanhoutte and C. B. Wenger: Regulation of the cutaneous circulation. Fed Proc, 45(13), 2841-50 (1986)
PMid:3780992
49. R. Thauer: Circulatory adjustments to climatic requirements. In: Handbook of Physiology. Ed W. F. Hamilton&P. Dow. American Phsyiological Society, Washington DC (1965)
50. I. C. Roddie, J. T. Shepherd and R. F. Whelan: The contribution of constrictor and dilator nerves to the skin vasodilatation during body heating. J Physiol, 136(3), 489-97 (1957)
PMid:13429515 PMCid:1358869
51. E. Tur, M. Tur, H. I. Maibach and R. H. Guy: Basal perfusion of the cutaneous microcirculation: measurements as a function of anatomic position. J Invest Dermatol, 81(5), 442-6 (1983)
doi:10.1111/1523-1747.ep12522619
PMid:6631055
52. A. B. Hertzman and W. C. Randall: Regional differences in the basal and maximal rates of blood flow in the skin. J Appl Physiol, 1(3), 234-41 (1948)
PMid:18885668
53. D. I. Sessler, A. Moayeri, R. Stoen, B. Glosten, J. Hynson and J. McGuire: Thermoregulatory vasoconstriction decreases cutaneous heat loss. Anesthesiology, 73(4), 656-60 (1990)
doi:10.1097/00000542-199010000-00011
PMid:2221434
54. H. V. Sparks: Skin and Muscle. In: Peripheral Circulation. Ed C. P. Johnson. John Wiley & Sons, Inc., New York (1978)
55. D. Grahn and H. Craig Heller: Heat Transfer in Humans: Lessons from Large Hibernators. In: Life in the Cold: Evolution, Mechanisms, Adaptation, and Application. Ed B. M. Barnes&H. V. Carey. Biological papers of the University of Alaska, (2004)
56. T. K. Bergersen: A search for arteriovenous anastomoses in human skin using ultrasound Doppler. Acta Physiol Scand, 147(2), 195-201 (1993)
doi:10.1111/j.1748-1716.1993.tb09489.x
PMid:8475746
57. T. W. Hartgill, T. K. Bergersen and J. Pirhonen: Core body temperature and the thermoneutral zone: a longitudinal study of normal human pregnancy. Acta Physiol (Oxf) (2011)
58. Thermoregulatory and thermal control in the human cutaneous circulation. Front Biosci (Schol Ed). 1(2), 825-53 (2010)
59. E. J. Van Someren: Thermoregulation and aging. Am J Physiol Regul Integr Comp Physiol, 292(1), R99-102 (2007)
doi:10.1152/ajpregu.00557.2006
PMid:16902181
60. D. W. Rennie: Tissue heat transfer in water: lessons from the Korean divers. Med Sci Sports Exerc, 20(5 Suppl), S177-84 (1988)
doi:10.1249/00005768-198810001-00016
61. H. F. Bowman, E. G. Cravalho and M. Woods: Theory, measurement, and application of thermal properties of biomaterials. Annu Rev Biophys Bioeng, 4(00), 43-80 (1975)
doi:10.1146/annurev.bb.04.060175.000355
PMid:1098563
62. A. Shitzer: Heat transfer in medicine and biology: analysis and applications. Plenum Press, London (1985)
63. D. W. deGroot, G. Havenith and W. L. Kenney: Responses to mild cold stress are predicted by different individual characteristics in young and older subjects. J Appl Physiol, 101(6), 1607-15 (2006)
doi:10.1152/japplphysiol.00717.2006
PMid:16888045
64. G. S. Anderson: Human morphology and temperature regulation. Int J Biometeorol, 43(3), 99-109 (1999)
doi:10.1007/s004840050123
PMid:10639901
65. M. G. Hayward and W. R. Keatinge: Roles of subcutaneous fat and thermoregulatory reflexes in determining ability to stabilize body temperature in water. J Physiol, 320, 229-51 (1981)
PMid:7320937 PMCid:1244044
66. J. Wang, B. Laferrere, J. C. Thornton, R. N. Pierson, Jr. and F. X. Pi-Sunyer: Regional subcutaneous-fat loss induced by caloric restriction in obese women. Obesity research, 10(9), 885-90 (2002)
doi:10.1038/oby.2002.121
PMid:12226136
67. F. Johnson, A. Mavroggiani, M. Ucci, A. Vidal-Puig and J. Wardle: Could increased time spent in a thermal comfort zone contribute to population increases in obesity? Obes Rev (2011)
68. S. L. Wijers, W. H. Saris and W. D. van Marken Lichtenbelt: Cold-Induced Adaptive Thermogenesis in Lean and Obese. Obesity (Silver Spring) (2010)
69. P. Tikuisis, D. G. Bell and I. Jacobs: Shivering onset, metabolic response, and convective heat transfer during cold air exposure. J Appl Physiol, 70(5), 1996-2002 (1991)
PMid:1864780
70. H. Loffler, J. U. Aramaki and I. Effendy: The influence of body mass index on skin susceptibility to sodium lauryl sulphate. Skin Res Technol, 8(1), 19-22 (2002)
doi:10.1046/j.0909-752x
71. D. M. Savastano, A. M. Gorbach, H. S. Eden, S. M. Brady, J. C. Reynolds and J. A. Yanovski: Adiposity and human regional body temperature. Am J Clin Nutr, 90(5), 1124-31 (2009)
doi:10.3945/ajcn.2009.27567
PMid:19740972 PMCid:2762153
72. A. M. Claessens-van Ooijen, K. R. Westerterp, L. Wouters, P. F. Schoffelen, A. A. van Steenhoven and W. D. van Marken Lichtenbelt: Heat production and body temperature during cooling and rewarming in overweight and lean men. Obesity (Silver Spring), 14(11), 1914-20 (2006)
doi:10.1038/oby.2006.223
PMid:17135606
73. ASHRAE: ASHRAE handbook, fundamentals. Atlanta (2005)
74. A. Meltzer: Thermoneutral zone and resting metabolic rate of broilers. Br Poult Sci, 24(4), 471-6 (1983)
doi:10.1080/00071668308416763
PMid:6667388
75. I. Macdonald: Differences in dietary-induced thermogenesis following the ingestion of various carbohydrates. Ann Nutr Metab, 28(4), 226-30 (1984)
doi:10.1159/000176808
PMid:6476787
76. R. Swaminathan, R. F. King, J. Holmfield, R. A. Siwek, M. Baker and J. K. Wales: Thermic effect of feeding carbohydrate, fat, protein and mixed meal in lean and obese subjects. Am J Clin Nutr, 42(2), 177-81 (1985)
PMid:4025189
77. K. Krauchi and A. Wirz-Justice: Circadian rhythm of heat production, heart rate, and skin and core temperature under unmasking conditions in men. Am J Physiol, 267(3 Pt 2), R819-29 (1994)
PMid:8092328
78. K. Krauchi: How is the circadian rhythm of core body temperature regulated? Clin Auton Res, 12(3), 147-9 (2002)
doi:10.1007/s10286-002-0043-9
79. J. Aschoff: Circadian control of body temperature. J. therm. Biol, 8, 143 to 147 (1983)
80. E. J. Van Someren, R. J. Raymann, E. J. Scherder, H. A. Daanen and D. F. Swaab: Circadian and age-related modulation of thermoreception and temperature regulation: mechanisms and functional implications. Ageing Res Rev, 1(4), 721-78 (2002)
doi:10.1016/S1568-1637(02)00030-2
81. P. Tikuisis and M. B. Ducharme: The effect of postural changes on body temperatures and heat balance. Eur J Appl Physiol Occup Physiol, 72(5-6), 451-9 (1996)
doi:10.1007/BF00242275
PMid:8925816
82. G. C. Donaldson, M. Scarborough, K. Mridha, L. Whelan, M. Caunce and W. R. Keatinge: Effect of posture on body temperature of young men in cold air. Eur J Appl Physiol Occup Physiol, 73(3-4), 326-31 (1996)
doi:10.1007/BF02425494
PMid:8781864
83. S. Aizawa and M. Cabanac: The influence of temporary semi-supine and supine postures on temperature regulation in humans. Journal of Thermal Biology, 27, 109-114 (2002)
doi:10.1016/S0306-4565(01)00023-7
84. H. Edfeldt and J. Lundvall: Sympathetic baroreflex control of vascular resistance in comfortably warm man. Analyses of neurogenic constrictor responses in the resting forearm and in its separate skeletal muscle and skin tissue compartments. Acta Physiol Scand, 147(4), 437-47 (1993)
doi:10.1111/j.1748-1716.1993.tb09519.x
PMid:8493877
85. W. R. Leonard, M. V. Sorensen, V. A. Galloway, G. J. Spencer, M. J. Mosher, L. Osipova and V. A. Spitsyn: Climatic influences on basal metabolic rates among circumpolar populations. Am J Hum Biol, 14(5), 609-20 (2002)
doi:10.1002/ajhb.10072
PMid:12203815
86. S. Osiba: The seasonal variation of basal metabolism and activity of thyroid gland in man. Jpn J Physiol, 7(4), 355-65 (1957)
PMid:13501954
87. G. Plasqui, A. D. Kester and K. R. Westerterp: Seasonal variation in sleeping metabolic rate, thyroid activity, and leptin. Am J Physiol Endocrinol Metab, 285(2), E338-43 (2003)
PMid:12857676
88. G. A. Borkan, D. E. Hults, S. G. Gerzof, A. H. Robbins and C. K. Silbert: Age changes in body composition revealed by computed tomography. J Gerontol, 38(6), 673-7 (1983)
PMid:6630900
89. H. W. Huang, W. C. Wang and C. C. Lin: Influence of age on thermal thresholds, thermal pain thresholds, and reaction time. J Clin Neurosci, 17(6), 722-6
doi:10.1016/j.jocn.2009.10.003
PMid:20356747
90. J. Smolander: Effect of cold exposure on older humans. Int J Sports Med, 23(2), 86-92 (2002)
doi:10.1055/s-2002-20137
PMid:11842354
91. C. S. Thompson-Torgerson, L. A. Holowatz, N. A. Flavahan and W. L. Kenney: Rho kinase-mediated local cold-induced cutaneous vasoconstriction is augmented in aged human skin. Am J Physiol Heart Circ Physiol, 293(1), H30-6 (2007)
doi:10.1152/ajpheart.00152.2007
PMid:17416609
92. C. S. Thompson-Torgerson, L. A. Holowatz and W. L. Kenney: Altered mechanisms of thermoregulatory vasoconstriction in aged human skin. Exerc Sport Sci Rev, 36(3), 122-7 (2008)
doi:10.1097/JES.0b013e31817bfd47
PMid:18580292
93. F. Khan, V. A. Spence and J. J. Belch: Cutaneous vascular responses and thermoregulation in relation to age. Clin Sci (Lond), 82(5), 521-8 (1992)
94. J. A. Wagner and S. M. Horvath: Influences of age and gender on human thermoregulatory responses to cold exposures. J Appl Physiol, 58(1), 180-6 (1985)
PMid:3968009
95. T. E. Wilson, K. D. Monahan, D. S. Short and C. A. Ray: Effect of age on cutaneous vasoconstrictor responses to norepinephrine in humans. Am J Physiol Regul Integr Comp Physiol, 287(5), R1230-4 (2004)
doi:10.1152/ajpregu.00467.2004
PMid:15475505
96. W. L. Kenney and C. G. Armstrong: Reflex peripheral vasoconstriction is diminished in older men. J Appl Physiol, 80(2), 512-5 (1996)
PMid:8929592
97. R. J. Petrella, D. A. Cunningham, P. M. Nichol and R. Thayer: Cardiovascular responses to facial cooling are age and fitness dependent. Med Sci Sports Exerc, 31(8), 1163-8 (1999)
doi:10.1097/00005768-199908000-00013
98. C. G. Armstrong and W. L. Kenney: Effects of age and acclimation on responses to passive heat exposure. J Appl Physiol, 75(5), 2162-7 (1993)
PMid:8307874
99. A. Dufour and V. Candas: Ageing and thermal responses during passive heat exposure: sweating and sensory aspects. Eur J Appl Physiol, 100(1), 19-26 (2007) doi:10.1007/s00421-007-0396-9
doi:10.1007/s00421-007-0396-9
PMid:17242944
100. H. Kaciuba-Uscilko and R. Grucza: Gender differences in thermoregulation. Curr Opin Clin Nutr Metab Care, 4(6), 533-6 (2001)
doi:10.1097/00075197-200111000-00012
PMid:11706289
101. J. M. Stocks, N. A. Taylor, M. J. Tipton and J. E. Greenleaf: Human physiological responses to cold exposure. Aviat Space Environ Med, 75(5), 444-57 (2004)
PMid:15152898
102. N. Charkoudian: Influences of female reproductive hormones on sympathetic control of the circulation in humans. Clin Auton Res, 11(5), 295-301 (2001)
doi:10.1007/BF02332974
PMid:11758795
103. M. A. Kolka and L. A. Stephenson: Control of sweating during the human menstrual cycle. Eur J Appl Physiol Occup Physiol, 58(8), 890-5 (1989)
doi:10.1007/BF02332224
PMid:2767071
104. D. J. Cunningham, J. A. Stolwijk and C. B. Wenger: Comparative thermoregulatory responses of resting men and women. J Appl Physiol, 45(6), 908-15 (1978)
PMid:730596
105. G. P. Kenny and O. Jay: Evidence of a greater onset threshold for sweating in females following intense exercise. Eur J Appl Physiol, 101(4), 487-93 (2007)
doi:10.1007/s00421-007-0525-5
PMid:17671791
106. T. Ichinose-Kuwahara, Y. Inoue, Y. Iseki, S. Hara, Y. Ogura and N. Kondo: Sex differences in the effects of physical training on sweat gland responses during a graded exercise. Exp Physiol, 95(10), 1026-32
doi:10.1113/expphysiol.2010.053710
PMid:20696786
107. M. J. Dauncey: Influence of mild cold on 24 h energy expenditure, resting metabolism and diet-induced thermogenesis. Br J Nutr, 45(2), 257-67 (1981)
doi:10.1079/BJN19810102
108. K. L. Hess, T. E. Wilson, C. L. Sauder, Z. Gao, C. A. Ray and K. D. Monahan: Aging affects the cardiovascular responses to cold stress in humans. J Appl Physiol, 107(4), 1076-82 (2009)
doi:10.1152/japplphysiol.00605.2009
PMid:19679742 PMCid:2763834
109. P. Wilkinson, S. Pattenden, B. Armstrong, A. Fletcher, R. S. Kovats, P. Mangtani and A. J. McMichael: Vulnerability to winter mortality in elderly people in Britain: population based study. BMJ, 329(7467), 647 (2004)
doi:10.1136/bmj.38167.589907.55
PMid:15315961
110. R. Basu: High ambient temperature and mortality: a review of epidemiologic studies from 2001 to 2008. Environ Health, 8, 40 (2009)
doi:10.1186/1476-069X-8-40
PMid:19758453 PMCid:2759912
111. O. Seppanen, W. J. Fisk and . Indoor climate and productivity. Rehva J, 3, 8-11 (2005)
Abbreviations: AVA: Arterio venous anastomose, BMR: Basal metabolic rate, CIZ: Core interthreshold zone, DIT: Diet induced thermogenesis, LCT: Lower critical temperature, SFT: Subcutaneous fat thickness, TNZ: Thermoneutral zone, UCT: Upper critical temperature
Key Words: Thermoregulation, Metabolism, Skin blood flow, Body composition, Thermoneutrality, Review
Send correspondence to: Boris Kingma, Maastricht University, Department of Human Biology, Universiteitssingel 50, P.O. Box 616, NL-6200 MD Maastricht, Tel: 31 043 388 42 60, Fax: 31043 367 09 76, E-mail:B.Kingma@maastrichtuniversity.nl