Brown Adipose Tissue Is Linked to a Distinct Thermoregulatory Response to Mild Cold in People

Abstract

Brown adipose tissue (BAT) plays an important role in thermoregulation in rodents. Its role in temperature homeostasis in people is less studied. To this end, we recruited 18 men [8 subjects with no/minimal BAT activity (BAT-) and 10 with pronounced BAT activity (BAT+)]. Each volunteer participated in a 6 h, individualized, non-shivering cold exposure protocol. BAT was quantified using positron emission tomography/computed tomography. Body core and skin temperatures were measured using a telemetric pill and wireless thermistors, respectively. Core body temperature decreased during cold exposure in the BAT- group only (-0.34°C, 95% CI: -0.6 to -0.1, p = 0.03), while the cold-induced change in core temperature was significantly different between BAT+ and BAT- subjects (BAT+ vs. BAT-, 0.43°C, 95% CI: 0.20-0.65, p = 0.0014). BAT volume was associated with the cold-induced change in core temperature (p = 0.01) even after adjustment for age and adiposity. Compared to the BAT- group, BAT+ subjects tolerated a lower ambient temperature (BAT-: 20.6 ± 0.3°C vs. BAT+: 19.8 ± 0.3°C, p = 0.035) without shivering. The cold-induced change in core temperature (r = 0.79, p = 0.001) and supraclavicular temperature (r = 0.58, p = 0.014) correlated with BAT volume, suggesting that these non-invasive measures can be potentially used as surrogate markers of BAT when other methods to detect BAT are not available or their use is not warranted. These results demonstrate a physiologically significant role for BAT in thermoregulation in people. This trial has been registered with Clinaltrials.gov: NCT01791114 (https://clinicaltrials.gov/ct2/show/NCT01791114).

Keywords: body core temperature; brown adipose tissue; cold exposure; supraclavicular skin temperature; thermoregulation.

Figure 1

CONSORT diagram of the study.

Figure 2

Brown adipose tissue (BAT), cold exposure (CE) tolerance, and thermal sensation. (A) Mean standardized uptake value (SUV) for glucose in various tissues at 6 h of CE. SQAT, subcutaneous adipose tissue; VAT, visceral adipose tissue. (B) Thermal sensation in subjects with detectable BAT (BAT+) and without detectable BAT (BAT−) at 5 h of CE. (C) Cooling garments temperature in BAT+ and BAT− subjects at 5 h of CE. (D) Ambient room temperature in BAT+ and BAT− subjects at 5 h of CE. The data are means and standard deviations. ^*p = 0.035 using Mann–Whitney test and ^***p = 0.001 using paired t-test.

Figure 3

Brown adipose tissue (BAT) and body temperature. (A) Cold-induced change in core temperature in subjects with detectable BAT (BAT+) and without detectable BAT (BAT−). **p = 0.0014 using Student's t-test, ^*p = 0.03 using one sample t-test. (B) Correlation of BAT volume with the change in body core temperature using Pearson's r. (C) Cold-induced change in supraclavicular skin temperature in BAT+ and BAT− subjects. ^**p = 0.007 using by one sample t-test, ^*p = 0.03 using Student's t-test. (D) Correlation of BAT volume with the change in supraclavicular skin body temperature using Pearson's r. The data are means and standard deviations. The dashed lines represent 95% confidence intervals.

Figure 4

Brown adipose tissue (BAT) activation, skin perfusion, and cardiovascular response to cold exposure (CE). (A) Average skin temperature in subjects with detectable BAT (BAT+) and without detectable BAT (BAT−) in thermoneutral (TN) conditions and at 5 h of CE. (B) Distal (hand, foot) skin temperature in BAT+ and BAT− subjects in TN conditions and after 5 h of CE. (C) Vasoconstriction/skin perfusion in BAT+ and BAT− subjects in TN conditions and at 5 h of CE. (D) Heart rate in BAT+ and BAT− subjects in TN conditions and at 5 h of CE. (E,F) Systolic (E) and diastolic (F) blood pressure in BAT+ and BAT− subjects in TN conditions and at 5 h of CE. Data are means and standard deviations. The data are means and SD. ^*p < 0.05, ^***p = 0.001, ^****p < 0.001 using paired t-test.