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obesity reviews

doi: 10.1111/j.1467-789X.2010.00851.x

Etiology and Pathophysiology



Could increased time spent in a thermal comfort zone contribute to population increases in obesity?
F. Johnson1, A. Mavrogianni2, M. Ucci2, A. Vidal-Puig3 and J. Wardle1

Cancer Research UK Health Behaviour

Domestic winter indoor temperatures in the USA, UK and other developed countries appear to be following an upwards trend. This review examines evidence of a causal link between thermal exposures and increases in obesity prevalence, focusing on acute and longer-term biological effects of time spent in thermal comfort compared with mild cold. Reduced exposure to seasonal cold may have a dual effect on energy expenditure, both minimizing the need for physiological thermogenesis and reducing thermogenic capacity. Experimental studies show a graded association between acute mild cold and human energy expenditure over the range of temperatures relevant to indoor heating trends. Meanwhile, recent studies of the role of brown adipose tissue (BAT) in human thermogenesis suggest that increased time spent in conditions of thermal comfort can lead to a loss of BAT and reduced thermogenic capacity. Pathways linking cold exposure and adiposity have not been directly tested in humans. Research in naturalistic and experimental settings is needed to establish effects of changes in thermal exposures on weight, which may raise possibilities for novel public health strategies to address obesity. Keywords: Brown adipose tissue, indoor temperatures, obesity epidemiology, thermogenesis.
obesity reviews (2011) 12, 543551

Research Centre, Department of Epidemiology and Public Health, University College London, London, UK; 2The Bartlett School of Architechture, University College London, London, UK; 3Department of Clinical Biochemistry, University of Cambridge, Cambridge, UK

Received 24 October 2010; revised 22 November 2010; accepted 23 November 2010

Address for correspondence: Dr. Fiona Johnson, Cancer Research UK Health Behaviour Research Centre, Department of Epidemiology and Public Health, University College London, Gower Street, London WC1E 6BT, UK. E-mail:

Obesity is a growing global health problem, and although genetic factors play a substantial role in determining individual weight gain (1), they cannot explain the rapid upward trends in adiposity observed at a population level. Research into environmental drivers of these trends has focused primarily on either increased energy intake through uptake of Western diets, or decreased expenditure because of sedentary lifestyles. These are undoubtedly the major contributors to these temporal trends, but other environmental factors may also play a contributing role. More recently, it has been suggested that reduced exposure to ambient temperature variability in daily life could be another contributor (2). Increased time spent indoors,

widespread access to central heating and air conditioning, cheap fuel prices, improved energy efciency in buildings and increased expectations of thermal comfort all contribute to restricting the range of temperatures experienced in daily life, and reducing time spent under mild thermal stress. Prolonged exposure to temperatures below the human thermoneutral zone (TNZ: dened as the range of ambient temperatures at which metabolic rate is minimal) increases energy expenditure, and therefore has the potential to affect energy balance over time. There is also evidence that low ambient temperatures can affect the bodys ability to maintain energy balance by increasing the capacity for thermogenesis (3). This review summarizes evidence for increases in winter indoor temperatures in the UK and

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USA, and examines the biological plausibility of the hypothesis that exposure to seasonal cold could help to regulate energy balance and body weight on a population level. It documents evidence for metabolic responses to mild cold compared with a thermoneutral environment, and discusses the role of cold exposure in determining individual thermogenic capacity through brown adipose tissue (BAT) proliferation and activation.

Time trends in thermal comfort and indoor winter temperatures

There is evidence for a temporal trend for afuent populations to heat their domestic environments to temperatures closer to the lower limit of the TNZ (approximately 2527C for a naked adult human) (4). As part of the multidisciplinary study giving rise to this review, a parallel review of evidence for changes in the thermal environment (Mavrogianni et al., in preparation) brings together data on indoor winter temperatures from the USA, UK and other developed countries. Since the 1960s, a cultural shift in norms of thermal comfort (5) and expectations of thermal monotony (6) have been driven by the widespread uptake of central heating (79) and air conditioning (10,11). Data on winter indoor temperatures from different sources are difcult to compare directly because of variations in data collection methodologies and protocols, but a temporal trend is unmistakable (Fig. 1). UK surveys using spot measurements between 1978 and 1996 (12,13) suggest that mean living room temperatures have been increasing at a rate of 0.4C per decade, rising from 18.3C in 1978 to 19.1C in 1996. More recent data (2008) based on estimated thermostat settings (14) suggest an even steeper rise in living room temperatures (21.3C), although it should be noted that data from estimated thermostat settings (based on repeated measured temperature logs) (14) may not be directly comparable with spot measurements. Bedroom temperatures (not measured in the most recent study) increased by 1.8C per decade from 15.2C in 1978 to 18.5C in 1996. The most substantial longitudinal study from the USA covers the period from 1987 to 2005 and is based on self-reported thermostat settings (15). It shows fairly constant winter living room temperatures at times when the house is occupied (21.2C in 1987 and 21.4C in 2005), but a striking increase in night time bedroom temperatures which rose from 19.3C to 20.2C between 1987 and 2005, a mean increase of 0.5C per decade. These data are consistent with a convergence of temperatures in different rooms of the home, with bedrooms and hallways that were previously maintained at a cooler temperature than living rooms showing the steepest increases. Such a homogenous indoor thermal environment along with the trend for warmer bedrooms during the hours of sleep may substantially reduce cold exposure in the home.

Figure 1 Mean winter indoor temperatures based on national household surveys in the US and UK. UK sources: 1978, national eld survey of house temperatures, spot measurements (12); 198696, the energy report of the English House Condition Survey, spot measurements (13); 2008, Carbon Reduction in Buildings project, estimated thermostat settings (14). US Source: Residential Energy Consumption Survey, self-reported thermostat settings (15).

Temperatures within private dwellings are only part of the story of reduced cold exposure. Workplace temperatures are also believed to be increasing (5,6) although there has been no systematic study of this. Other social trends likely to result in reduced seasonal cold exposure include reductions in walking and cycling in favour of temperature-controlled car transportation (16,17) and a decline in childrens outdoor play (18). Global environmental changes may also have had some effect, as cold temperatures and frosts have become less frequent (19), although how far climate changes have affected personal cold exposure is not known. These factors do not form part of this review, but they may be further contributors to the effects discussed here.

Human responses to cold

Two types of physiological responses to cold exposure can be distinguished in humans. Insulative responses entail a decrease in skin temperature through peripheral vasoconstriction, conserving heat and contributing to maintaining the temperature of internal organs. Adaptive thermogenic responses (heat generation for homeostatic purposes) lead to an increase in energy expenditure through shivering and non-shivering thermogenesis. Shivering is an acute response to cold exposure, generating heat through the involuntary

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contraction of skeletal muscle bres. During mild cold exposure shivering rapidly reduces through adaptation, although metabolic increases associated with cold exposure do not decrease, demonstrating that non-shivering thermogenic processes are present in humans (20,21). Nonshivering adaptive thermogenesis defends body temperature by the generation of heat in tissues, and is also initiated in response to eating (21). Diet-induced thermogenesis (DIT) consists of the obligatory energy cost of the digestion and absorption of the food consumed, and an additional facultative component which allows energy dissipation following food ingestion (i.e. adaptive thermogenesis). The effector mechanisms of cold-induced and DIT are believed to be closely related, and both are mediated by sympathetic activation (22,23). Blocking of sympathetic activity, both in animal experimental models and through therapeutic use of beta-adrenoceptor blocking agents, has been linked to reduced energy expenditure and weight gain (2427). Thermogenic responses to overfeeding and mild cold are highly correlated in humans, sharing 57% of their variance (28) suggesting the existence of a phenotype representing general thermogenic capacity. There is substantial indirect evidence that thermogenesis can play a signicant role in energy balance (2931). Both genetic mutations and ablative lesions that result in abnormal energy expenditure contribute to the development of obesity in laboratory animals (21), and defects of thermogenesis characterize several genetically obese strains (see Himms-Hagen for a review) (32). For example, leptin decient ob/ob mice not only display an obese phenotype and hyperphagia but also gain excess weight when pair-fed to lean peers (33) implicating a defect of energy expenditure that can not be fully accounted for by reduced physical activity (34).

remained equal (38). In practice, the extent to which compensatory behaviours counteract increases in expenditure is unclear. The majority of the studies in Table 1 used standardized clothing, a situation which is not directly comparable with a naturalistic setting, as clothing adjustment is a normal response to ambient temperature change. However, one study that allowed participants to adjust their clothing level for comfort (36) found that this did not fully mitigate the effects of cold on energy expenditure, although the expenditure gradient was less steep than where clothing was standardized (Fig. 2). Energy intake is also known to increase in response to increased expenditure (41) and the possible compensatory effects of this are discussed in more detail below.

The role of brown adipose tissue in cold-induced thermogenesis

Recent developments in the study of BAT have changed the way that adaptive thermogenesis in humans is understood and provided additional evidence for the signicance of thermogenic processes for energy balance. Unlike white adipose tissue which acts predominantly as an energy storage depot, BAT is a thermogenic organ, dissipating energy in the form of heat (42). BAT is rich in mitochondria which produce heat through the activation of the uncoupling protein (UCP)-1 mitochondrial UCP. BAT has long been known to be essential for thermogenesis in small mammals and human newborns, but brown fat stores diminish with age, and until recently the functional role of BAT in adult humans was believed to be negligible. However, recent research has demonstrated that BAT has a more signicant role in adult thermogenesis than was previously thought (43). The observation of BAT in adults has been largely a chance nding; like metastatic tumour tissue, brown adipocytes are able to incorporate high levels of glucose and are visible on radiological scans using uorodeoxyglucose (FDG) positron emission tomography (PET). The use of FDG PET scanning techniques for diagnostic purposes has led to the identication of BAT deposits in a varying proportion of adults (44). BAT is only discernable when activated, and cold ambient temperature at the time of imaging greatly increases the likelihood of observing BAT (44). A recent temperature-controlled study using PET imaging of healthy human subjects concluded that the presence of metabolically active BAT is normal among adult humans in conditions of mild cold (1719C) (73 [Correction added after online publication 7 February 2011: Reference 45 has been changed to 73]). Similarly, a recent study of lean and obese adults found evidence of BAT deposits in all but one of 24 subjects during cold (16C), but not during thermoneutral conditions (22C) (45) (Fig. 3), demonstrating that BAT is activated in conditions of mild cold. The authors calculate that the potential

Human energy expenditure in response to mild cold

A small number of studies have investigated the effects of mild cold on energy expenditure in humans using respiration chambers which allow the measurement of energy expenditure over periods of hours or days (28,3540). These studies (summarized in Table 1, with results illustrated in Fig. 2) demonstrate that energy expenditure in humans is negatively associated with thermal environment over a range of ambient temperatures from 15C to 28C, a range that encompasses normal indoor temperature exposures. Furthermore, the magnitude of the thermic response to changes in ambient temperatures is (theoretically) sufcient to affect energy balance. The authors of one of these studies suggest that the energy expenditure prompted by exposure to mild cold for 10% of the time over 10 years could be equivalent to an 8 kg difference in body weight, if other factors such as energy intake and external insulation

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Table 1 Human respiration chamber studies: measuring energy expenditure at varying ambient temperature
Design Temperature conditions 16C 22C 12.9 2.0 MJ day-1* 12.2 2.2 MJ day-1 Increase of 5.7% 2% at 16C compared with 22C 9.9 1.5 MJ day-1 8.9 1.3 MJ day-1 Decrease of 10 2% at 27C compared with 22C 8.3 1.9 MJ day-1 7.7 1.4 MJ day-1 Resting and fasting metabolic rate showed a decrease of 11 3.2% at 28C compared with 22C 9.2 MJ day-1 (SD = 0.7). 8.8 MJ day-1 (SD = 0.9) Increase of 5.0% at 20C compared with 28C 0.2C 0.2C 0.3C 80.3 78.3 81.0 5.8 W day-1 6.5 W day-1 6.8 W day-1 Participants used more clothing and bedcoverings at 20C but this did not fully compensate for the effects of lowered ambient temperature on energy expenditure Thermal comfort thresholds and range did not vary between the obese and lean participants Energy expenditure Other measurements



Westerterp-Plantenga et al. (2002) (37)

Male volunteers n=9 Age 24 5 years BMI 22.7 2.1 Participants stayed in a respiration chamber for 48 h on three occasions, once at 22C and twice at 27C Clothing and activity was standardized Fed in energy balance (ad libitum for the nal 24 h at 22C and once at 27C) Participants stayed in a whole-body calorimeter for 30 h on two occasions, once at 22C and once at 28C Clothing and activity was standardized Reported expenditure is the mean over rst 24 h Participants stayed in a respiration chamber twice for 24 h, once at 20C and once at 28C Choice of clothing and standardized activity and diet 20C 28C 22C 28C 22C 27C

Participants stayed for 60 h in a respiration chamber on three occasions: once at 22C and twice at 16C Clothing and activity was standardized Fed in energy balance (ad libitum for the nal 24 h at 22C and one of the 16C visits)

When participants were fed ad libitum, they overate by 32% at 22C and 34% at 16C (compared with intake needed for energy balance)

Indoor temperatures and obesity

Westerterp-Plantenga et al. (2002) (35)

Female volunteers n=8 Age 22 2 years BMI 22 3

When participants were fed ad libitum, they under-ate by 9.7% at 22C and 9.3% at 27C (compared with intake needed for energy balance)

F. Johnson et al.

Dauncey (1981) (38 [Correction added after online publication 7 February 2011: Reference 34 has been changed to Reference 38])

Female n=9 Age 32 4 years Weight = 57.1 2.2 kg

Warwick & Busby (1990) (36)

Female n = 6 Male n = 4 Age 23.1 years (SD = 5.2 years) BMI 27.6 (SD = 6.8) Participants stayed in the calorimeter for 24 h, once at their lower thermal comfort threshold, once at their higher threshold and once at the mid-point Thermal comfort zone was determined individually for each participant Mean heat loss calculated over a number of standardized food intake and exercise conditions 16C 22C 23.2 24.8 26.3

Blaza & Garrow (1983) (39)

Female Lean n = 5 Obese n = 5 Age 29.3 2.6 Weight 77.4 4.2 kg

Wijers et al. (2007) (28) 1.7 0.9

Male n = 13 Age 22.8 BMI 23.0 Participants stayed in a respiration chamber twice (summer and winter) at 22C for 1 h followed by 15C for 3 h Fasting for 10 h prior to and during the test

Participants stayed in a respiration chamber on three occasions: 36 h at 22C (fed in energy balance) 84 h at 16C (fed in energy balance ) 84 h at 22C (160% overfeeding not reported here)

12.1 11.5

0.2 MJ day-1 0.1 MJ day-1

Van Ooijen et al. (2004) (40)

Male n = 10 Female n = 10 Age = 26 5 BMI = 1732

15C (summer) 15 C (winter) 22 C

5.1 KJ m-1 (7.3 MJ day-1) 5.3 KJ m-1 (7.6 MJ day-1) 4.7 KJ m-1 (6.8 MJ day-1)

Reduced metabolic response to cold in summer compared with winter (metabolic increase at 15C: winter 11.5%, summer 7.0%) Relative contribution of metabolic and core temperature change was subject-specic and consistent over summer and winter tests

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*Measured during energy balance feeding period. Mean temperature over 10 participants. Adjusted for fat-free mass.

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14 13 12 11 10

24h EE (MJ day-1)

9 8 7 6 5 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30

Ambient temperature (C) Westerterp-Plantenga et al., 2002 (37) Warwick & Busby, 1990 (36) Westerterp-Plantenga et al., 2002 (35) Wijers et al., 2007 (28) Dauncey, 1981 (38) van Ooijen et al., 2004 (40)

Figure 2 Changes in energy expenditure in response to ambient temperature, human respiration chamber studies. EE, energy expenditure. (Correction added after online publication 7 February 2011: Reference 34 has been changed to Reference 38).

energy expenditure of the BAT seen in this study could, if fully activated, contribute substantially to energy balance, expending energy equivalent to 4 kg of adipose tissue over the course of a year (73) [Correction added after online publication 7 February 2011: (73) was added to the end of the sentence as it had previously been missed out.].

The role of adaptation in BAT response to cold exposure

Studies of cold adaptation show that infrequent exposure to cold (such as may be inferred from the increased time spent in comfortable indoor temperatures) will result in reduced thermogenic potential and lower capacity for energy expenditure in response to acute cold exposure. Sympathetic activation in response to cold triggers adaptive recruitment of BAT through proliferation and differentiation of precursor cells and hypertrophy of existing brown adipocytes (3). Cold adaptation in laboratory animals results in both a general darkening of the adipose tissue, indicating an increase in the proportion of brown adipocytes (46), and increased size of BAT depots (47,48). A similar association between chronic cold exposure and BAT has been observed in humans: with larger BAT deposits and greater aerobic energy metabolism in the adipose tissue of Finnish outdoor workers compared with indoor workers (49).

Figure 3 Comparative PET-CT scans reveal the patterns of 18F-FDG uptake in the same subject after exposure to cold (16C) and under thermoneutral conditions. From van Marken Lichtenbelt et al. (45). Reproduced with permission. CT, computed tomography; FDG, uorodeoxyglucose; PET, positron emission tomography.

Seasonal differences in the prevalence of active BAT in humans have also been observed, suggesting that BAT development is induced by the increased exposure to cold that is associated with seasonal temperature changes. A retrospective analysis of a series of 3614 PET/computed tomography diagnostic scans (50) demonstrated that BAT activity was associated with both lower average monthly temperature (r2 = 0.70) and seasonal shortening of hours of daylight

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(a) Average maximum monthly outdoor temperature (C) 35 30 25 20 15 10 5 0 0 (c) Average maximum monthly outdoor temperature (C) 35 30 25 20 15 10 5 0 0 5 10 15 USA-fat monthly incidence (%) 20 r = 0.62 5 10 15 USA-fat monthly incidence (%) 20 r = 0.55

(b) Average maximum monthly outdoor temperature (C) 35 30 25 20 15 10 5 0 0 (d) Average maximum monthly outdoor temperature (C) 35 30 25 20 15 10 5 0 0 5 10 15 USA-fat monthly incidence (%) 20 r = 0.34 5 10 15 USA-fat monthly incidence (%) 20 r = 0.61

Figure 4 Correlation between incidence of uptake in supraclavicular area fat (BAT) and average monthly outdoor maximum temperature. Incidence is compared with temperature of same month (a) and temperature of 1 month (b), 2 months (c) and 3 months (d) before. From Cohade et al. (51). Reproduced with permission. BAT, brown adipose tissue.

(r2 = 0.88). A similar study (51) found that the incidence of BAT observed in a series of 1017 clinical FDG-PET scans was signicantly related to season, being highest during the coldest months of the year. These studies did not control for the ambient indoor temperature at the time of the scan, but there are two reasons to suppose that this may reect seasonal development of BAT rather than simply the acute effects of temperature at the time of scanning. First, both studies found that the BAT prevalence distribution lagged slightly behind the external temperature distribution which may indicate a latency period for the development of BAT in response to seasonal temperature changes (Fig. 4). Second, a further study which examined energy expenditure in response to a standardized temperature in summer and winter (15C) found greater energy expenditure in response to this temperature in winter than in summer (40) (Table 1). These studies suggest that even in a temperate climate, seasonal cold adaptation occurs in humans, and that this is likely to be at least partially explained by proliferation of BAT during the winter months.

laboratory animals, the thermic response to food is greater in animals that have undergone cold adaptation (52,53) and inhibited in animals kept at thermoneutrality (54), implicating BAT in the process of DIT (21). Substantial inter-individual variation in weight gain response to overfeeding is observed in humans (5557) and this has been attributed in part to individual differences in DIT (58). Studies of a single nucleotide polymorphism associated with level of UCP-1 gene expression (and hence capacity for BAT activation) have shown that children with the low UCP-1 expression variants had lower thermogenic responses to a high-fat meal (59) and the same variants were associated with higher body mass index in a Czech population study (60).

Energy intake: adaptive responses to changes in ambient temperature

Lower energy expenditure occurring at temperatures approaching thermoneutrality may be partly counterbalanced by a reduced food intake. Research in livestock and laboratory animals shows that intake is substantially reduced at higher temperatures (6163). In humans, too, ambient temperature is known to affect appetite, intake and food choice (6467). Two short-term respiration chamber studies in which participants were fed ad

The role of cold exposure in diet-induced thermogenesis

Reduced cold exposure may also have an impact on individuals capacity to expend excess ingested energy (52). In

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libitum (35,37) found that intake adjustment compensated accurately for temperature-induced changes in expenditure. It has been suggested, however, that long-term regulation of food intake to maintain energy balance is not tightly coupled to energy expenditure in humans, being strongly inuenced by factors such as the social and eating environment, and the composition, energy density, variety and palatability of foods (68). A recent review (69) concluded that modifying thermogenesis in animals and humans through articial manipulation of UCP-1 uncoupling or cold exposure leads to changes in energy balance and body weight, with changes in intake not fully compensating for changes in expenditure. There is also evidence from animal studies that availability of highly palatable food may override temperaturerelated compensatory adjustments in intake. This has important implications for intake in the Western obesogenic environment where food is easily available and highly palatable. Laboratory animals fed a high-fat diet do not suppress their food intake at thermoneutral temperatures, and gain weight. In contrast, mice on a low-fat diet reduce food intake at thermoneutrality and do not gain additional weight (70). Similarly, energy intake in rats increases in response to a modest reduction in ambient temperature, but for those eating a low-fat (chow) diet this is insufcient to adequately compensate for increased metabolic output, resulting in a reduced growth rate and body weight (71). These human and animal experimental models suggest that while intake is somewhat suppressed at higher temperatures, this is unlikely to fully compensate for the reduced energy expenditure of a warm environment, particularly where highly palatable foods are available.

This review examined whether increased duration of exposure to temperatures approaching thermoneutrality and decreases in exposure to mild seasonal cold might be factors contributing to population rises in obesity (2). There is evidence from the UK and USA for an increase and homogenization of temperatures in domestic settings, a trend that is likely to have been fuelled by increasing expectations of thermal comfort in wealthy Western countries. However, studies of ambient temperatures in specic locations cannot capture a detailed picture of the frequency and duration of thermal exposures in the course of an individuals daily activities, and there is a need to document personal and socially patterned trends in cold exposure. Nonetheless, trends in domestic winter indoor temperatures strongly suggest that seasonal cold exposure is decreasing among populations of afuent countries. Knowledge of the mechanisms of human responses to cold exposure has taken great strides in recent years with a

renewed interest in the role of BAT in human thermogenesis. Recent research suggests that reduced exposure to cold can be expected to have a dual impact on the ability to control body weight. First, more time spent in the thermal comfort zone reduces the frequency or duration of occasions on which cold-induced energy expenditure is initiated. Experimental studies of human energy expenditure in response to cold in a controlled environment show that energy expenditure in humans increases in response to acute cold exposure (28,3540,72), and that energy expenditure shows a graded association with acute cold exposure over a range of temperatures relevant to trends in indoor heating (Fig. 2). Studies of changes in food intake, which have the potential to compensate for reduced energy expenditure at temperatures of thermal comfort, suggest that while some intake adjustment to restore energy balance takes place, this is unlikely to compensate fully for reduced expenditure (69). There is also evidence from animal models that with a highly palatable and energy-dense food supply the expected decreases in intake in response to reduced energy expenditure are attenuated (70,71). If this effect is also seen in humans, it is of particular signicance given that an obesogenic food environment goes along with the thermal comfort of Western lifestyles, and this may override a natural propensity to reduce food intake in warmer conditions. Second, as thermogenic capacity (and notably development and retention of BAT) is stimulated by cold exposure (3), an increase in time spent in conditions of thermal comfort will inevitably lead to a reduced thermogenic capacity and loss of BAT. Individuals with low levels of BAT are at a disadvantage in terms of their ability to regulate their energy expenditure. Studies of seasonal variation in BAT activation and energy expenditure in response to acute cold suggest that thermogenic capacity is responsive to moderate changes in exposure to cold (such as those experienced seasonally by residents of Western temperate climates) (40,50,51). Homogenization of the indoor thermal environment almost certainly reduces exposure to seasonal cold. In laboratory animals, reductions in BAT affect not only the ability to generate heat to defend body temperature, but also the efciency of DIT (31). However, the signicance of this putative pathway from thermal comfort to excess adiposity in humans is not yet established. The research discussed here supports the biological plausibility of a causal link between increased time spent in thermal comfort and increased adiposity in the population, while also highlighting signicant gaps in understanding of the pathways involved. There have been no direct studies of the effects of variation in long-term thermal environment on energy balance or body weight in humans, and the design of such a study presents considerable methodological challenges. It is also unclear how far behavioural adaptations such as clothing adjustments reduce the effects of

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temperature on energy expenditure, or whether decreased energy expenditure in thermal comfort is matched by decreased energy intake, in a food environment in which energy-dense and highly palatable food is widely available. Establishing the signicance and magnitude of the effects of both short-term and long-term thermal exposures on body weight could lead to the development of novel therapies to address obesity on an individual and a population level.

Conicts of Interest Statement


The Heating and Obesity Trends research project is funded by he UCL Crucible Centre. The Crucible Centre is part of the cross-council Lifelong Health and Wellbeing Initiative. Funding from the BBSRC, EPSRC, ESRC and MRC is gratefully acknowledged.

1. Maes HH, Neale MC, Eaves LJ. Genetic and environmental factors in relative body weight and human adiposity. Behav Genet 1997; 27: 325351. 2. Keith SW, Redden DT, Katzmarzyk PT, Boggiano MM, Hanlon EC, Benca RM, Ruden D, Pietrobelli A, Barger JL, Fontaine KR, Wang C, Aronne LJ, Wright SM, Baskin M, Dhurandhar NV, Lijoi MC, Grilo CM, DeLuca M, Westfall AO, Allison DB. Putative contributors to the secular increase in obesity: exploring the roads less travelled 2. Int J Obes (Lond) 2006; 30: 15851594. 3. Klingenspor M. Cold-induced recruitment of brown adipose tissue thermogenesis. Exp Physiol 2003; 88: 141148. 4. Erikson H, Krog J, Andersen KL, Scholander PF. The critical temperature in naked man. Acta Physiol Scand 1956; 37: 3539. 5. Chappells H, Shove E. Debating the future of comfort: environmental sustainability, energy consumption and the indoor environment. Build Res Inf 2005; 33: 3240. 6. Healy S. Air-conditioning and the homogenization of people and built environments. Build Res Inf 2008; 36: 3241. 7. Schipper L, Johnson F, Howarth R, Andersson B, Price L. Energy Use in Sweden: An International Perspective. Lawrence Berkeley Laboratory: Berkely, CA, 1993. 8. Meyer W. Why indoor climates change: a case study. Clim Change 2002; 55: 395407. 9. Utley J, Shorrock L. Domestic energy fact le 2008. Building Research Establishment 2010 May 29; [WWW document]. URL Accessed 10th October 2010. 10. Arsenault R. The end of the long hot summer the airconditioner and southern culture. Journal South Hist 1984; 50: 597628. 11. Biddle J. Explaining the spread of residential air conditioning, 1955-198030. Explor Econ Hist 2008; 45: 402423. 12. Hunt DRG, Gidman MI. A national eld survey of house temperatures. Build Environ 1982; 17: 107124. 13. Department for the Environment Transport and the Regions (DETR). English House Condition Survey 1996. UK, 1996.

14. Shipworth M, Firth S, Gentry M, Wright A, Shipworth D, Lomas K. Central heating thermostat settings and timing:building demographics. Build Res Inf 2010; 38: 50. 15. US Energy Information Administration. Residential Energy Consumption Survey. EIA 2010; [WWW document]. URL http:// Accessed 21st September 2010. 16. US Department of Transportation. National Household Travel Survey 2001. 2001. 17. Ofce for National Statistics. Transport Trends 2009. The Stationery Ofce: London, 2010. 18. Johnson KA, Klaas SJ. The changing nature of play: implications for pediatric spinal cord injury32. J Spinal Cord Med 2007; 30: S71S75. 19. Intergovernmental Panel on Climate Change. Climate change 2007. Synthesis report. Intergovernmental Panel on Climate Change 2007; [WWW document]. URL publications_and_data/ar4/syr/en/contents.html. Accessed 21st September 2010. 20. DAVIS TR. Chamber cold acclimatization in man. J Appl Physiol 1961; 16: 9491146. 21. Lowell BB, Spiegelman BM. Towards a molecular understanding of adaptive thermogenesis. Nature 2000; 404: 652660. 22. Danforth EJ, Burger A. The role of thyroid hormones in the control of energy expenditure. Clin Endocrinol Metab 1984; 13: 581595. 23. Young JB, Saville E, Rothwell NJ, Stock MJ, Landsberg L. Effect of diet and cold exposure on norepinephrine turnover in brown adipose tissue of the rat. J Clin Invest 1982; 69: 10611071. 24. Astrup A, Simonsen L, Christensen NJ. Effects of betaadrenergic blockade on meal-induced thermogenesis4. Clin Physiol 1990; 10: 305307. 25. ODea K, Esler M, Leonard P, Stockigt JR, Nestel P. Noradrenaline turnover during under- and over-eating in normal weight subjects. Metabolism 1982; 31: 896899. 26. Landsberg L, Saville ME, Young JB. Sympathoadrenal system and regulation of thermogenesis. Am J Physiol 1984; 247 (2 Pt 1): E181E189. 27. Acheson K, Jequier E, Wahren J. Inuence of beta-adrenergic blockade on glucose-induced thermogenesis in man1. J Clin Invest 1983; 72: 981986. 28. Wijers SL, Saris WH, van Marken Lichtenbelt WD. Individual thermogenic responses to mild cold and overfeeding are closely related. J Clin Endocrinol Metab 2007; 92: 42994305. 29. Richard D. Energy expenditure: a critical determinant of energy balance with key hypothalamic controls. Minerva Endocrinol 2007; 32: 173183. 30. Himms-Hagen J. Defective brown adipose tissue thermogenesis in obese mice. Int J Obes 1985; 9(Suppl. 2): 1724. 31. Jequier E. Thermogenic responses induced by nutrients in man: their importance in energy balance regulation. Experientia Suppl 1983; 44: 2644. 32. Himms-Hagen J. Brown adipose tissue thermogenesis, energy balance, and obesity. Can J Biochem Cell Biol 1984; 62: 610617. 33. Trayhurn P. The development of obesity in animals: the role of genetic susceptibility. Clin Endocrinol Metab 1984; 13: 451 474. 34. Dauncey MJ, Brown D. Role of activity-induced thermogenesis in twenty-four hour energy expenditure of lean and genetically obese (ob/ob) mice. Q J Exp Physiol 1987; 72: 549559. 35. Westerterp-Plantenga MS, van Marken Lichtenbelt WD, Cilissen C, Top S. Energy metabolism in women during short exposure to the thermoneutral zone. Physiol Behav 2002; 75: 227235.

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Indoor temperatures and obesity

F. Johnson et al.


36. Warwick PM, Busby R. Inuence of mild cold on 24 h energy expenditure in normally clothed adults. Br J Nutr 1990; 63: 481488. 37. Westerterp-Plantenga MS, van Marken Lichtenbelt WD, Strobbe H, Schrauwen P. Energy metabolism in humans at a lowered ambient temperature. Eur J Clin Nutr 2002; 56: 288296. 38. Dauncey MJ. Inuence of mild cold on 24 h energy expenditure, resting metabolism and diet-induced thermogenesis. Br J Nutr 1981; 45: 257267. 39. Blaza S, Garrow JS. Thermogenic response to temperature, exercise and food stimuli in lean and obese women, studied by 24 h direct calorimetry. Br J Nutr 1983; 49: 171180. 40. van Ooijen AM, van Marken Lichtenbelt WD, van Steenhoven AA, Westerterp KR. Seasonal changes in metabolic and temperature responses to cold air in humans. Physiol Behav 2004; 82: 545553. 41. King NA, Caudwell P, Hopkins M, Byrne NM, Colley R, Hills AP, Stubbs JR, Blundell JE. Metabolic and behavioral compensatory responses to exercise interventions: barriers to weight loss. Obesity (Silver Spring) 2007; 15: 13731383. 42. Cannon B, Nedergaard J. Developmental biology: neither fat nor esh13. Nature 2008; 454: 947948. 43. Farmer SR. Obesity: be cool, lose weight. Nature 2009; 458: 839840. 44. Nedergaard J, Bengtsson T, Cannon B. Unexpected evidence for active brown adipose tissue in adult humans. Am J Physiol Endocrinol Metab 2007; 293: E444E452. 45. van Marken Lichtenbelt WD, Vanhommerig JW, Smulders NM, Drossaerts JM, Kemerink GJ, Bouvy ND, Schrauwen P, Teule GJ. Cold-activated brown adipose tissue in healthy men. N Engl J Med 2009; 360: 15001508. 46. Cinti S. The role of brown adipose tissue in human obesity. Nutr Metab Cardiovasc Dis 2006; 16: 569574. 47. Bukowiecki L, Collet AJ, Follea N, Guay G, Jahjah L. Brown adipose tissue hyperplasia: a fundamental mechanism of adaptation to cold and hyperphagia. Am J Physiol 1982; 242: E353E359. 48. Geloen A, Collet AJ, Bukowiecki LJ. Role of sympathetic innervation in brown adipocyte proliferation. Am J Physiol 1992; 263 (6 Pt 2): R1176R1181. 49. Huttunen P, Hirvonen J, Kinnula V. The occurrence of brown adipose tissue in outdoor workers. Eur J Appl Physiol Occup Physiol 1981; 46: 339345. 50. Au-Yong IT, Thorn N, Ganatra R, Perkins AC, Symonds ME. Brown adipose tissue and seasonal variation in humans. Diabetes 2009; 58: 25832587. 51. Cohade C, Mourtzikos KA, Wahl RL. USA-Fat: prevalence is related to ambient outdoor temperature-evaluation with 18F-FDG PET/CT. J Nucl Med 2003; 44: 12671270. 52. Allard M, Leblanc J. Effects of cold acclimation, cold exposure, and palatability on postprandial thermogenesis in rats. Int J Obes 1988; 12: 169178. 53. Rothwell NJ, Saville ME, Stock MJ. Factors inuencing the acute effect of food on oxygen consumption in the rat. Int J Obes 1982; 6: 5359. 54. Rothwell NJ, Stock MJ. Inuence of environmental temperature on energy balance, diet-induced thermogenesis and brown fat activity in cafeteria-fed rats. Br J Nutr 1986; 56: 123129. 55. Bouchard C, Tremblay A, Despres JP, Nadeau A, Lupien PJ, Theriault G, Dussault J, Moorjani S, Pinault S, Fournier G. The response to long-term overfeeding in identical twins. N Engl J Med 1990; 322: 14771482. 56. Joosen AM, Bakker AH, Westerterp KR. Metabolic efciency and energy expenditure during short-term overfeeding. Physiol Behav 2005; 85: 593597.

57. Diaz EO, Prentice AM, Goldberg GR, Murgatroyd PR, Coward WA. Metabolic response to experimental overfeeding in lean and overweight healthy volunteers. Am J Clin Nutr 1992; 56: 641655. 58. Wijers SL, Saris WH, van Marken Lichtenbelt WD. Recent advances in adaptive thermogenesis: potential implications for the treatment of obesity. Obes Rev 2009; 10: 218226. 59. Nagai N, Sakane N, Ueno LM, Hamada T, Moritani T. The -3826 A>G variant of the uncoupling protein-1 gene diminishes postprandial thermogenesis after a high fat meal in healthy boys. J Clin Endocrinol Metab 2003; 88: 56615667. 60. Sramkova D, Krejbichova S, Vcelak J, Vankova M, Samalikova P, Hill M, Kvasnickova H, Dvorakova K, Vondra K, Hainer V, Bendlova B. The UCP1 gene polymorphism A-3826G in relation to DM2 and body composition in Czech population. Exp Clin Endocrinol Diabetes 2007; 115: 303307. 61. Marsden A, Morris TR. Quantitative review of the effects of environmental temperature on food intake, egg output and energy balance in laying pullets. Br Poult Sci 1987; 28: 693 704. 62. Macari M, Dauncey MJ, Ingram DL. Changes in food intake in response to alterations in the ambient temperature: modications by previous thermal and nutritional experience. Pugers Arch 1983; 396: 231237. 63. Stanier MW. Effect of environmental temperature and food intake on the distribution of fat in growing hairless mice. Br J Nutr 1977; 37: 279284. 64. Stroebele N, De Castro JM. Effect of ambience on food intake and food choice. Nutrition 2004; 20: 821838. 65. Johnson RE, Kark RM. Environment and food intake in man. Science 1947; 105: 378379. 66. Tharion WJ, Lieberman HR, Montain SJ, Young AJ, BakerFulco CJ, Delany JP, Hoyt RW. Energy requirements of military personnel. Appetite 2005; 44: 4765. 67. Herman C. Effects of Heat on Appetite. In: Marriott BM (ed.). Nutritional Needs in Hot Environments: Applications for Military Personnel in Field Operations. National Academy Press: Washington, DC, 1993, pp. 187214. 68. Levitsky DA. The non-regulation of food intake in humans: hope for reversing the epidemic of obesity. Physiol Behav 2005; 86: 623632. 69. Cannon B, Nedergaard J. Thermogenesis challenges the adipostat hypothesis for body-weight control. Proc Nutr Soc 2009; 68: 401407. 70. Rippe C, Berger K, Boiers C, Ricquier D, Erlanson-Albertsson C. Effect of high-fat diet, surrounding temperature, and enterostatin on uncoupling protein gene expression3. Am J Physiol Endocrinol Metab 2000; 279: E293E300. 71. Rowe EA, Rolls BJ. Effects of environmental temperature on dietary obesity and growth in rats. Physiol Behav 1982; 28: 219 226. 72. van Marken Lichtenbelt WD, Schrauwen P, van De KS, Westerterp-Plantenga MS. Individual variation in body temperature and energy expenditure in response to mild cold. Am J Physiol Endocrinol Metab 2002; 282: E1077E1083. 73. Virtanen KA, Lidell ME, Orava J, Heglind M, Westergren R, Niemi T, Taittonen M, Laine J, Savisto NJ, Enerbck S, Nuutila P. Functional brown adipose tissue in healthy adults. N Engl J Med 2009; 360: 15181525. [Correction added after online publication 7 February 2011: Reference 73 has been added as it had previously been missed out]

2011 The Authors obesity reviews 2011 International Association for the Study of Obesity 12, 543551