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Biophysical aspects of human thermoregulation during heat stress Matthew N. Cramer, Ollie Jay PII:DOI: S1566-0702(16)30030-3doi: 10.1016/j.autneu.2016.03. Reference: AUTNEU 1826 To appear in: Autonomic Neuroscience: Basic and Clinical Received date:Revised date: 1 October 20152 March 2016 Accepted date: 3 March 2016
Please cite this article as: Cramer, Matthew N., Jay, Ollie, Biophysical aspects of humanthermoregulation during heat stress, Autonomic Neuroscience: Basic and Clinical (2016), doi: 10.1016/j.autneu.2016.03.
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Biophysical aspects of human thermoregulation during heat stress
Matthew N. Cramer^1 and Ollie Jay1,2, (^1) School of Human Kinetics, Faculty of Health Sciences, University of Ottawa, ON, CANADA (^2) Thermal Ergonomics Laboratory, Faculty of Health Sciences, University of Sydney, NSW, AUSTRALIA (^3) Charles Perkins Centre, University of Sydney, NSW, AUSTRALIA
Conflicts of interest: none
Funding sources: M.N.C. was supported by an Excellence Scholarship from the University of Ottawa.
Keywords: heat exchange; heat balance; core temperature; sweating
Address for Correspondence: Dr. O. Jay Thermal Ergonomics Laboratory, Faculty of Health Sciences, University of Sydney, Lidcombe, NSW, 2141 AUSTRALIA Tel: +61 2 9351 9328 Fax: +61 2 9351 9204 E-mail: [email protected]
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Biophysics of human thermoregulation during heat stress
INTRODUCTION Heat stress causes a transient or persistent imbalance between heat gained and heat lost to the environment, resulting in body heat storage. Heat gain arises as a byproduct of cellular metabolism and/or exposure to external temperatures greater than the body surface. Heat loss occurs via conduction, convection, radiation and evaporation, the rates of which are governed by the physical properties of the skin (surface area, skin temperature and wettedness) and the environment (ambient and radiant temperatures, air movement, barometric pressure, ambient vapor pressure, clothing insulation) (Gagge and Nishi, 1977). The ability to restore or maintain heat balance through greater cutaneous vasodilation and eccrine sweating is often within the physical limits imposed by the environment. However, under the most thermally stressful conditions, heat balance may be impossible despite high levels of skin blood flow and rates of sweat production. For a given change in body heat storage, core temperature varies with the mass and composition of body tissues by altering the internal heat sink and average heat capacity of body tissues, respectively. This complex interaction between metabolic heat production, the physical properties of the skin and environment, and body size are the principal components determining core temperature responses (Figure 1), and ultimately determine whether heat balance is attainable or if core temperature will progressively rise to levels that are potentially harmful to health and performance. The purpose of this review is to present a current understanding of the biophysical factors that contribute to individual variability in the thermoregulatory responses to heat stress. The first section provides an overview of the physical properties affecting heat balance. The second section examines the independent and interactive effects of biophysical factors related to heat production and body morphology on the core temperature response to heat stress.
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BIOPHYSICS OF HUMAN HEAT BALANCE
A fundamental and useful reference point for any discussion of human energy exchange and core temperature regulation is the conceptual heat balance equation: S=M–Wk±K±R±C±Cres–Eres–Esk [W] (Eq. 1) In accordance with the law of energy conservation, the rate of body heat storage (S) is equal to the difference between rates of metabolic energy expenditure (or metabolic rate, M), external work (Wk), dry heat exchange from the skin by conduction (K), radiation (R), convection (C), convective heat exchange (Cres) and evaporative heat loss (Eres) from the respiratory tract, and evaporative heat loss from the skin (Esk). The SI unit for rates of energy conversion is watts (W); however, heat balance parameters are often expressed per square meter (W/m^2 ) of total body surface area (AD), which is conventionally estimated from body mass and standing height (DuBois and DuBois, 1916; Tikuisis et al., 2001). It may also be useful to express these values per kilogram of total body mass (W/kg) for certain applications discussed below. In some contexts, metabolic rate is expressed in kilojoules per minute (1 kJ/min≈17 W), kilocalories per minute (1 kcal/min≈70 W), or metabolic equivalents (1 MET=58.2 W/m^2 ). Metabolism always represents a source of heat gain; dry heat avenues can lead to heat gain or loss depending on the temperature gradient between the skin and environment (see below), but heat can only be lost by evaporation from the respiratory tract and skin. To maintain heat balance (S=0), the rate of total heat gain from metabolic and environmental heat sources must be equivalent to the rate of total heat loss. It follows that heat storage and internal temperature rise if the rate of total heat gain exceeds the rate of total heat loss (S>0); conversely, heat storage and internal temperature fall if the rate of total heat loss outweighs the rate of heat
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performed at rest, all metabolic energy is ultimately converted to heat. During exercise, greater heat production arises from the increase in oxygen consumption (VO 2 ) required to meet the energetic demands of the active musculature. Some metabolic energy is converted to useful external work during activities such as cycling or rowing, but external work output is negligible during weight-bearing exercise such that the rates of metabolic energy expenditure and heat production are nearly equivalent (Snellen, 1960). Uphill walking and running lead to a net vertical displacement of body mass against gravity and thus result in a positive external work rate and a greater rate of heat production compared to level-grade walking/running at the same velocity (Bobbert, 1960). Although heat production rises with exercise intensity, the amount of heat produced at any absolute intensity will vary with mechanical efficiency or movement economy, that is, the ability to transform metabolic energy into useful work or movement. Gross efficiency refers to the percentage of whole-body metabolic energy expenditure that is converted to external work, and typically equals ≤25% during cycling or rowing (Fukunaga et al., 1986; Gaesser and Brooks, 1975; Moseley et al., 2004). During weight-bearing activities, movement economy is the mass- specific oxygen cost of moving 1 km (ml·kg−^1 ·km−^1 ) or relative VO 2 (ml·kg−^1 ·min−^1 ) at a specific velocity. Running economy usually ranges from 180-220 ml·kg−^1 ·km−^1 , depending on a variety of physiological and biomechanical factors (Barnes and Kilding, 2015; Daniels, 1985; Saunders et al., 2004). Extraordinary values in elite male and female runners of 150 ml·kg−^1 ·km−^1 (Lucia et al., 2008) and 165 ml·kg−^1 ·km−^1 (Jones, 2006), respectively, have also been reported.
Conduction
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Biophysics of human thermoregulation during heat stress Thermal conduction involves the diffusive transfer of heat between solid surfaces in direct contact with each other. According to Fourier’s Law, conduction is related to the temperature gradient between surfaces, the thermal conductivity of the material, and the thickness and area of contact between surfaces. Conduction with the external environment is generally considered negligible unless the skin is in contact with highly conductive surfaces for a prolonged duration, such as the post-operative use of warming blankets (Giuffre et al., 1991), treatment of fever with ice packs (Badjatia, 2009), or pre-competition cooling with ice vests or cold towels to enhance athletic performance (Ross et al., 2013).
Radiation Thermal radiation is the process of heat exchange between bodies of different surface temperatures in the form of electromagnetic waves. Within a radiant field, the rate of radiant heat exchange between the body and the environment will depend on the surface temperatures of all surrounding objects, body surface temperature and emissivity, clothing insulation, and the effective radiant surface area, which is influenced by a body’s orientation relative to other radiating objects. In an environment with multiple radiating bodies, it is useful to express radiant heat exchange in terms of the mean radiant temperature, defined as the uniform temperature of a hypothetical isothermal black enclosure within which a body would exchange the same amount of thermal radiation as in a real non-uniform environment, and measured using a standard black globe(ISO, 1998). Heat is gained via thermal radiation if mean radiant temperature exceeds skin temperature (e.g., heat wave), and lost if skin temperature exceeds mean radiant temperature (e.g., at room temperature). Of course, the most common source of radiant heat is the sun; other sources include radiant warming lamps used to prevent hypothermia in neonates (Molgat-Seon et
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Biophysics of human thermoregulation during heat stress Typical convective heat loss values during rest and exercise in air and water media are presented in Table 3. Due to a higher density (999.2 versus 1.225 kg/m^3 ), specific heat capacity (4.19 versus 1.01 kJ·kg−^1 ·K−^1 ), and thermal conductivity (578.8 versus 25.0 mW·m−^1 ·K−^1 ) (Lemmon and Harvey, 2015; Monteith and Unsworth, 2013), convection is much greater in water than air (Boutelier et al., 1977; Nadel et al., 1974; Nishi and Gagge, 1970). For this reason, water-perfusion suits have been widely employed to rapidly elevate core temperature in studies of reflex thermoregulatory and cardiovascular control during thermal stress (Crandall and Wilson, 2015; Johnson et al., 2014), while neck-deep cold-water immersion (<26°C) in a circulating bath is currently recommend for treatment of exertional heat stroke (Casa et al., 2015, 2007, 2005; Taylor et al., 2008). Nevertheless, electric fans are still useful to augment dry heat loss provided that skin temperature exceeds air temperature (Table 3 ). If air temperature is higher than skin temperature, fan-forced airflow over the skin will accelerate convective heat gain, and forced-air warming devices are frequently used to prevent peri- and post-operative hypothermia induced by anesthesia (Alderson et al., 2014; Warttig et al., 2014). Convection in air also facilitates sweat evaporation, leading to a higher rate of total heat loss that may be protective under severe heat stress despite a higher convective dry heat gain (Jay et al., 2015; Ravanelli et al., 2015b).
Evaporation Heat loss through sweat evaporation is the principal avenue of heat loss during exercise in most environments, and the only means by which humans can dissipate heat from the skin if environmental temperatures exceed skin temperature—conditions that would otherwise lead to dry heat gain. Evaporation is a two-step process involving the phase transition of sweat on the
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skin surface from liquid to vapor at a constant temperature (latent heat transfer), followed by the diffusion of vapor across the boundary layer and into the surrounding air. The driving force for evaporation is the vapor pressure gradient between the saturated skin surface and the ambient air, but evaporation is also influenced by air velocity, skin wettedness, and AD. Due to the relationship between convective heat and mass (vapor) transfer (Kerslake, 1972), higher air velocities lead to simultaneous elevations in convection and evaporation (Adams et al., 1992; Clifford et al., 1959). Skin wettedness is a non-dimensional term representing the theoretical fraction of surface area that if fully covered in sweat, would result in a given rate of evaporation from the skin (Gagge, 1937), and expressed as the ratio between the rate of evaporation from the skin (Esk) and the maximum capacity for evaporation (Emax), which reflects the limit to evaporative heat loss imposed by the environment from a fully wet skin surface. The absolute value of Emax is a function of the maximum skin wettedness, the skin-air vapor pressure gradient (itself dependent on skin and air temperatures and ambient humidity), air velocity and density, the evaporative resistance of clothing, and AD (Figure 2). Maximum skin wettedness depends on heat acclimation state, with values ~0.85 and 1.00 for non-heat-acclimated and heat-acclimated individuals, respectively (Candas et al., 1979a, 1979b). An influence of high aerobic fitness on maximum skin wettedness to heat-acclimated levels has been assumed (Mora-Rodriguez et al., 2010); however, this possibility has not been empirically demonstrated. It is often useful to express evaporation and skin wettedness in terms of heat balance requirements. The rate of evaporation required for heat balance (Ereq) is the rate of evaporative heat loss needed to balance metabolic and environmental sources of heat gain: Ereq=M–Wk±K±R±C±Cres–Eres [W] (Eq. 2)
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threshold, as the observed sweat rate exceeds the sweat rate needed for Ereq. This threshold ωreq is estimated to be between 0.20 and 0.74, and will depend on clothing, air velocity, and body posture (Alber-Wallerstrom and Holmer, 1985; Candas et al., 1979a, 1979b; Givoni, 1963; Kerslake, 1963). The non-evaporated fraction of secreted sweat ends up trapped in clothing or drips off the body, contributing nothing to whole-body heat loss. In practice, evaporative heat loss is commonly estimated using partitional calorimetry (Gagge, 1996; Kenny and Jay, 2013) based on the latent heat of vaporization of sweat of 2426 J/g (Wenger, 1972) and changes in body mass corrected for rates of fluid ingestion/excretion, metabolic and respiratory mass losses arising from CO 2 /O 2 exchange and respiratory evaporation (Mitchell et al., 1972), and any non-evaporated sweat. The amount of sweat trapped in clothing may be measured by weighing clothing before and after exposure, while non-evaporated sweat that has dripped off the skin may be captured, and subsequently weighed, using oil-filled collection pans placed beneath the individual (Adams et al., 1992; Alber-Wallerstrom and Holmer, 1985; Candas et al., 1979a, 1979b).
Respiratory Heat Losses In addition to the skin, heat is also exchanged between the respiratory tract and the external environment during pulmonary ventilation. As inspired air travels down the airway, it is heated to the body’s internal temperature and fully saturated with moisture drawn from the airway surface. Upon expiration, heat transferred to the inspired air via convection and evaporation is lost to the surrounding environment. Based on the principles of convective and evaporative heat loss, the rate of respiratory heat exchange will depend on the temperature gradient between the inspired air and body core, ambient humidity, and ventilation rate.
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Although respiratory heat loss is highest in cold/dry conditions, it nonetheless contributes marginally to total whole-body heat loss due to the relatively poor thermal conductivity of air. For example, during exercise at a moderate work rate eliciting 500 W of metabolic heat at the same low vapor pressure (0.1 kPa: 5% RH at 20°C, 80% RH at −20°C), total respiratory heat loss is higher in – 20°C (88 W) compared to +20°C (60 W) due entirely to the greater respiratory convection at – 20°C. Further, 500 W of heat production at an ambient temperature of 20°C results in only a slightly higher total heat loss at 10% relative humidity (RH; 0.23 kPa) of 59 W compared to 90% RH (2.10 kPa) of 42 W, resulting from a higher Eres of 49 W at 10% RH versus 33 W at 90% RH. In each example, more than 400 W of additional skin surface heat loss would still be required to stabilize core temperature, demonstrating the relatively minor contribution of respiratory heat losses to whole-body heat balance.
BIOPHYSICAL FACTORS AND THERMOREGULATORY RESPONSES TO HEAT STRESS It is well recognized that the core temperature and thermoregulatory sweating responses to heat stress demonstrate a high degree of individual variability that may be explained by a variety of physiological and biophysical factors (Anderson, 1999; Kenney, 1985; Kenny and Jay, 2013). Recent evidence suggests that among individuals matched for physiological traits (e.g., age, sex, and health status), biophysical factors related to heat production and body morphology predominately determine the core temperature and sweating responses to exercise. The following section will provide a summary of these findings with an emphasis on exercise heat stress, although the same physical principles governing heat exchange and storage (as outlined above) may also be applied to passive environmental heat stress.
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rate of heat production and thus change in core temperature between these runners. Additionally, since Ereq is primarily determined by the rate of heat production and the main predictor of whole- body sweat rate (Cramer and Jay, 2015; Gagnon et al., 2013), and skin temperature varies largely with ambient temperature, similar rates of total heat loss should also be observed between these runners. However, at 50% of VO2max, the absolute VO 2 (L/min) of the high-VO2max runner is higher, leading to greater heat production and Ereq compared to the low-VO2max runner, such that greater changes core temperature and higher sweat rates would be expected in the high-VO2max runner unless a high VO2max itself causes a more rapid onset and sensitivity of sweating (Nadel et al., 1974; Roberts et al., 1977). In accordance with this model, Jay et al. (2011) assessed changes in core temperature following exercise at a fixed %VO2max and at a fixed absolute rate of heat production and Ereq between groups of high (~60 ml·kg–^1 ·min–^1 ) or low (~40 ml·kg–^1 ·min–^1 ) VO2max, but matched for age, sex, and body size. Exercise at 60% of VO2max in both groups led to a much greater rate of heat production in the high- (834 W) vs. low-VO2max (600 W) group, and consequently, the change in core temperature, whole-body sweat rate, and local sweat rate were greater in the high- VO2max group. In contrast, changes in core temperature and sweating rates were not different between high- and low-VO2max groups during exercise at the same absolute rate of heat production (~540 W) despite large differences in %VO2max (40% versus 58%). Importantly, no differences in sweating onset or sweat sensitivity were observed in each trial, indicating no independent effect of VO2max on thermoeffector control. Similar findings were reported by Stapleton et al. (2010) pre- vs. post-8 weeks of aerobic training that improved VO2max by 10% from ~49 to ~54 ml·kg–^1 ·min–^1 , and by Smoljanić et al. (2014) between mass-matched groups of high- and low-VO2max during treadmill running. Collectively, these studies support the classic
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findings of Nielsen (1938), and suggest that core temperature and sweating responses to exercise among individuals matched for body size should be compared using fixed absolute heat production, irrespective of %VO2max and exercise modality.
Body Surface Area As the interface with the external environment, the dimensions of the body surface have an important effect on whole-body heat exchange. As discussed above, the absolute rates of convection, radiation, and evaporation will be greatest in individuals with the largest AD for a given set of skin (temperature, wettedness) and environmental (temperature, air velocity and density) properties. Similarly, whole-body absolute heat loss potential (e.g., Emax) is greater among larger individuals with higher AD. Since the attainment of heat balance depends on matching the rate of heat production with an equivalent rate of heat loss, large individuals with high AD will be able to sustain a higher absolute rate of heat production while still remaining in heat balance due to greater heat loss potential (Figure 4). However, even with a large AD, individuals with diseases of or injuries to the skin can result in a loss of effective AD (the area of the skin that can participate in heat dissipation), resulting in lower absolute rates of heat loss and therefore limits on how much heat can be generated while remaining in heat balance (Figure 4). For a given thermal load (combination of metabolic and environmental heat gain), smaller individuals or individuals with a lower effective AD will have a relatively limited ability to dissipate heat and therefore an impaired ability to safely regulate core temperature at high ambient temperatures and/or during exercise. This is perhaps best demonstrated among burn survivors with injured and grafted skin (Ganio et al., 2015), following sympathectomy (Cramer and Jay, 2012; Shih and Lin, 1979), and individuals with spinal cord lesions (Sawka et al., 1989).
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its thermal inertia. Secondly, the energy cost of weight-bearing exercise varies with body mass, such that the absolute energy cost of movement is greater in heavier individuals (Passmore and Durnin, 1955). For a given change in body heat content and tissue composition, the change in core temperature should be inversely related to the body mass such that smaller individuals experience a greater change in core temperature during exercise at a fixed absolute rate of heat production (Havenith, 2001; Havenith et al., 1998, 1995), and likely contributed to the wide variation in core temperature responses during fixed-speed treadmill walking within the ‘prescriptive zone’ (Lind, 1970). Recently, Cramer and Jay (2014) investigated the independent effect of body mass in determining the core temperature response to exercise (Figure 5). Among individuals matched for age, sex, and heat acclimation status, exercise eliciting 500 and 600 W of heat production resulted in greater changes in rectal temperature in lighter ( 67 .6 kg) compared to heavier (91. kg) individuals. Given the independent influences of both heat production and body mass, core temperature responses were further compared between the same groups at two levels of heat production per kilogram of total body mass (6.5 and 9.0 W/kg). Despite large differences in body mass and the absolute rate of heat production, core temperature changes at both 6.5 W/kg (~0.80°C) and 9.0 W/kg (~1.05°C) were similar between groups. These observations confirm the independent effect of body mass on core temperature, and provide a novel approach to identify potential impairments in core temperature regulation as a function of factors such as disease, injury etc., between independent groups of dissimilar body mass. During uncompensable heat stress, a high body mass should also influence the rate of rise in core temperature due to a lower AD-to-mass ratio that accompanies a larger body size. This arises from the relatively smaller increase in AD for a given increase in body mass. Although a
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number of studies have investigated the relationship between core temperature and AD-to-mass ratio during heat stress, the findings appear equivocal (Haymes et al., 1974; Marino et al., 2000; Shvartz et al., 1973). Theoretically, at high ambient temperature, rates of heat exchange relative to AD are similar regardless of body size; however, the corresponding rates of heat exchange per unit of mass are higher in lighter-weight individuals (Table 4). As a result, the rate of heat storage should be greater for an equivalent metabolic heat load, and should result in greater core temperature changes among individuals with a lower AD-to-mass ratio (Marino et al., 2000; Ravanelli et al., 2015a).
Body Composition Variation in the relative contribution of lean tissue, fat, and bone to total body mass determines the average heat capacity of the body based on thermal properties of individual tissue types. Adipose tissue has a lower heat capacity (2.51 J·g−^1 ·°C−^1 ) compared to ‘lean’ tissues (3. J·g−^1 °C−^1 ) (Stolwijk, 1971). Consequently, individuals of higher adiposity would be expected to have greater changes in core temperature for a given change in body heat content and mass. During heat exposure, higher levels of adiposity should result in either a greater change in core temperature if heat loss is unaffected or a similar core temperature response if heat loss (e.g. sweat evaporation) is augmented. Unfortunately, evidence supporting these possibilities is equivocal. The lack of consensus at least partly reflects the fact that few studies have properly controlled exercise intensity for both heat production and body mass (Adams et al., 2015; Dougherty et al., 2009; Leites et al., 2013; Sehl et al., 2012). Modest differences in body fat percentage of ~10% does not influence core temperature responses during exercise at a fixed heat production in W/kg (Cramer et al., 2012; Cramer and Jay, 2014; Jay et al., 2011), while
