Brown adipose tissue–associated postprandial thermogenesis in humans: Different effects of isocaloric meals rich in carbohydrate, fat, and protein

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Brown adipose tissue–associated postprandial thermogenesis in humans: Different effects of isocaloric meals rich in carbohydrate, fat, and protein

https://doi.org/10.21203/rs.3.rs-1762974/v1

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The increase of whole-body energy expenditure seen after a single meal ingestion, referred to as diet-induced thermogenesis (DIT), substantially varies depending on the meal’s macronutrient composition. Brown adipose tissue (BAT), a site of nonshivering thermogenesis, may be involved in DIT. To examine the effects of meal composition on BAT-associated DIT in humans, healthy male participants underwent [¹⁸F]fluorodeoxyglucose–positron emission tomography to assess BAT activity, and respiratory gas analysis for 2 hours after ingestion of a carbohydrate-, protein-, or fat-rich meal (C-meal, P-meal, and F-meal, respectively). The calculated DIT at 2 hours was 6.44 ± 2.01%, 3.49 ± 2.00%, and 2.32 ± 0.90% of the ingested energy after the P-meal, C-meal, and F-meal, respectively. The DIT after C-meal ingestion correlated positively with BAT activity (P = 0.011), and was approximately twice greater in the group with high-BAT activity than in the group with low-BAT activity (4.35 ± 1.74% vs. 2.12 ± 1.76%, P < 0.035). Conversely, the DIT after F-meal or P-meal ingestion did not correlate with BAT activity, with no difference between the two groups. Thus, BAT has a significant role in facultative DIT after ingestion of a carbohydrate-rich meal, but hardly after ingestion either protein- or fat-rich meal.

Brown adipose tissue (BAT) is the major site of nonshivering thermogenesis (NST) during cold exposure (cold-induced thermogenesis [CIT]) in small rodents [1]. Through [¹⁸F]fluorodeoxyglucose (FDG)–positron emission tomography (PET) and computed tomography (CT), metabolically active BAT was rediscovered in adult humans [2–5]. It is now confirmed that human BAT is activated by cold exposure and contributes to the regulation of whole-body energy expenditure (EE) and body fatness [6, 7]. NST seen after meal ingestion, referred to as the “specific dynamic action of food,” “thermic effects of food,” “postprandial thermogenesis”, or “diet-induced thermogenesis (DIT),” is also a significant component of the total EE in our daily life. Generally, DIT is divided into two components: obligatory and facultative thermogenesis. Obligatory thermogenesis refers to the obligatory response including digestion, absorption, and metabolism/storage of ingested nutrients. Facultative thermogenesis refers to additional responses, but its mechanisms remain poorly understood.

In 1980s, Glick et al. [8] suggested that BAT can be activated after a single meal because BAT’s respiration rate increased in 2 hours after food intake in rats. We [9] also found meal-induced metabolic activation of BAT in rats because 30 minutes after liquid meal ingestion, glucose utilization and fatty acid synthesis in sympathetically innervated BAT were increased. Through simultaneous 24-hour recording of food intake and oxygen consumption in mice deficient of uncoupling protein 1 (UCP1), which is a key molecule for BAT thermogenesis, the role of BAT in DIT was proven, owing to the lower whole-body oxygen consumption in UCP1-deficient mice than in wild-type mice, particularly during the eating period [10]. Consistent with these previous studies in small rodents, we [11, 12] demonstrated in healthy humans that DIT is approximately 50% higher in participants with metabolically active BAT than in those without it, suggesting BAT’s contribution to facultative DIT in humans [13]. Human BAT activation after meal intake is directly confirmed by PET/CT using [¹⁵O]O₂, [¹⁵O]H₂O, and [¹⁸F]fluoro-thiaheptadecanoic acid radiotracers [14].

DIT is roughly 10% of the energy content of ingested meals, but it varies depending on the macronutrient composition of meal, being approximately 3% for fat, 7–8% for carbohydrate, and 25–30% for protein [15, 16]. In rats, BAT is activated after ingestion of a high-carbohydrate meal, but to a lesser extent after ingestion of a high-protein or high-fat meal [17, 18]. There results collectively suggest that BAT-associated DIT is largely influenced by the macronutrient composition of meal. In this study, we aimed to measure DIT after the ingestion of a carbohydrate-, protein-, or fat-rich meal in healthy human volunteers and analyze its association with BAT activity.

Participant characteristics

A total of 41 young male participants underwent FDG-PET/CT, anthropometrics, and body composition analysis and then participated in indirect calorimetry before and after test meal ingestion (Table 1). Eleven out of those who consumed the C-meal also participated in the calorimetry for the P-meal. The participants were divided into two groups according to the BAT activity: BAT-negative and BAT-positive using the cut-off value of SUV_max=1.5 as recommended by Chen et al. [19]. However, the number of the BAT-negative group was 4–5 out of 15–19 participants, and was too small to compare statistically with the BAT-positive group. Accordingly, the participants were divided into two groups: those with lower (Low-BAT group) and higher (High-BAT group) than the median value of SUV_max. The mean SUV_max in the High-BAT group was 5.8–10 times higher than that in the Low-BAT group (Table 1). Age, anthropometric parameters, and resting EE before meal ingestion were not significantly different between the two groups.

DIT based on the test meals

Figure 1 shows whole-body EE before and after meal ingestion in all participants regardless of having low- and high-BAT activities. After meal ingestion, EE increased rapidly at 30 minutes and thereafter (Fig. 1a). Given that the absolute values of basal EE and postprandial increase (calculated as the difference from the basal EE) vary depending on the body size and ingested amount of energy, the ingested meal amount was adjusted to 7.9 kcal/kg body weight in the present study. Thus, the postprandial increase calculated in relation to body weight was higher after the P-meal than after the C-meal and F-meal (Fig. 1b), and ANOVA revealed highly significant effects of time, meal, and time × meal interaction (P < 0.001). This result was also confirmed when postprandial increase was integrated as the area under the curve and expressed as % of ingested energy. DIT thus calculated at 0–60 and 60–120 minutes was highest after the P-meal and lowest after the F-meal, and that at 0–120 minutes was 6.44 ± 2.01%, 3.49 ± 2.00%, and 2.32 ± 0.90% after the P-, C-, and F-meals, respectively (Fig. 1c).

Effects of BAT activity on DIT

After C-meal ingestion, EE seemed to increase with time more in the High-BAT group than in the Low-BAT group (Fig. 2a), and ANOVA revealed a significant time × BAT interaction in postprandial EE increase (P = 0.038, Fig. 2b). The integrated DIT at 0-120 minutes was significantly greater in the High-BAT group than in the Low-BAT group (4.35 ± 1.74% vs. 2.12 ± 1.76%, P < 0.05) (Fig. 2c). Moreover, DIT showed a significant positive correlation with BAT activity expressed as Log SUVmax (P = 0.011, Fig. 3a). A significant positive correlation was also found between BAT activity and DIT at 0–60 minutes (P = 0.013) and 60–120 minutes (P = 0.010).

After P-meal ingestion, EE, postprandial increase in EE, and DIT were almost comparable between the two groups (Fig. 2d, 2e, 2f), and DIT did not significantly correlate with BAT activity (P = 0.194, Figs. 3b). After F-meal ingestion, EE seemed to increase with time similarly in the two groups (Fig. 2g), but ANOVA revealed a significant time × BAT interaction (P = 0.036) in postprandial increase (Fig. 2h). DIT at 0–60 minutes was significantly higher (P < 0.05) in the High-BAT group than in the Low-BAT group (Fig. 2i). However, DIT at 60–120 and 0–120 minutes showed no significant difference between such groups (Fig. 2i). In addition, DIT showed no significant correlation with BAT activity (P = 0.189, Fig. 3c), although DIT at 0–60 minutes tended to correlate positively with BAT activity (P = 0.064).

Postprandial response of blood parameters

Blood glucose increased rapidly and remarkably after C-meal ingestion (Fig. 4a) but only slightly after P- and F-meal ingestion (Figs. 4d, 4g). The postprandial response of blood glucose was not significantly different between the two groups. Similarly, the postprandial responses of blood FFA (Figs. 4b, 4e, 4h) and insulin (Figs. 4c, 4f, 4i) showed no significant differences between such groups.

DIT is roughly 10% of the energy content of ingested meal, and it varies depending on meal composition, being 3% for fat, 7–8% for carbohydrate, and 25–30% for protein [15, 16]. Similarly, our results demonstrated that DIT was highest after the P-meal (6.4%) and lowest after the F-meal (2.3%), and approximately 3.5% after the C-meal. Our DIT values are lower than the reported values because of the duration of the measurement. The above-mentioned DIT was obtained for 6–10 hours after meal ingestion, whereas the DIT in our study was measured for 2 hours after meal ingestion. We [11, 12] previously reported that DIT with a mixed meal containing 60% carbohydrate was approximately 8.6% when measured for 5 hours using a whole-room human calorimeter. In the present study, EE was measured for 2 hours using a respiratory gas analyzer connected to a ventilated food; thus, collecting a stable value for a longer time period was difficult, probably because of the increasing stress of repeated immobilization for the measurement.

The present study also demonstrated that DIT after the C-meal was almost twice higher in the High-BAT group than in the Low-BAT group. Moreover, DIT showed a highly significant correlation with BAT activity. These results are consistent with our previous report that DIT with a mixed meal containing 60% carbohydrate was approximately 1.5 times higher in participants with active BAT than in those without it [11, 12], suggesting that a substantial component of DIT after a C-meal is attributable to BAT activation. Vosselman et al. [20] measured BAT activity using FDG-PET/CT in healthy volunteers 120 minutes after intake of a carbohydrate-rich meal (CPF energy ratio of 78:12:10), and found that postprandial FDG uptake into BAT was much lower than cold-induced uptake, whereas whole-body EE was comparable. Vrieze et al. [21] also reported an unexpected reduction in FDG uptake into BAT compared with that after overnight fasting. Although these results seem to be in conflict with the idea of postprandial activation of BAT thermogenesis, they can be explained by increased insulin-stimulated FDG uptake into skeletal muscle, which reduces FDG bioavailability for BAT, which in turn leads to underestimation of BAT activity. Actually, using ¹⁵O[O_2, H₂O]-PET instead of FDG-PET, Din et al. [14] demonstrated the activation of BAT thermogenesis 15 minutes after ingestion of a meal containing 58% carbohydrate.

In our study, the postprandial responses of blood glucose, FFA, and insulin were similar in the Low- and High-BAT groups; hence, the difference in DIT between the two groups may not be attributable to the difference in digestion and absorption of the ingested nutrients. Recently, Loeliger et al. [22] reported that human BAT activity assessed by FDG-PET/MRI was associated with EE increase after mild cold exposure, but not with that after an oral glucose load; thus, they argued that DIT is independent from BAT activation. Such apparent discrepancy still cannot be explained clearly, but it may have resulted from the difference in the loaded substances and their energy content. We gave a nutritionally balanced food with a CPF energy ratio of 51:11:38 at a dose of 7.9 kcal/kg body weight (total energy of 430–580 kcal), whereas they gave 75 g (300 kcal) of glucose dissolved in tap water solution. They also did not show the participants’ body weight; thus, the energy dose could not be calculated. Another possible reason is that the rate for the digestion and absorption of our C-meal is different from that of their glucose solution, thereby affecting the results. In fact, postprandial EE increased for at least 2 hours in our study, whereas that in their study increased for only 1 hour.

Contrary to C-meal ingestion, P-meal or F-meal ingestion showed that DIT was not significantly different between the Low- and High-BAT groups. Consistently, the DIT in P-meal or F-meal showed no correlation with BAT activity. The DIT 1 hour after the F-meal was slightly but significantly higher in the High-BAT group than in the Low-BAT group, suggesting that BAT may contribute to fat-induced DIT only during the initial phase. These results seem compatible with those reported in rats in which the in vitro respiration rate of BAT was lower after P- or F-meals than after C-meals [17, 18]. Thus, facultative thermogenesis by BAT after protein or fat ingestion is considerably less, or negligible, compared with that after carbohydrate ingestion.

BAT thermogenesis is activated through the sympathetic nerve (SN) and β-adrenoceptor (βAR) axis. Based on this well-accepted view, this axis may also play a key role in DIT. In both experimental animals and humans, the SN activity assessed from the plasma levels of noradrenaline (NA) and tissue NA turnover decreases during fasting but increases immediately after food intake [23–26]. More notably, postprandial SN activation is higher after carbohydrate ingestion than after protein or fat ingestion [26–29]. These results are quite consistent with our present results and support the idea that the SN–βAR–BAT axis is activated after C-meal ingestion but only slightly after P- or F-meal ingestion, thereby contributing substantially to facultative DIT. However, reports on the effect of βAR blockers on DIT in humans are conflicting; some demonstrated decreased DIT, while others showed no effects [30–32]. Such discrepancy still could not be explained clearly, but it may be related to individual differences in BAT activity, that is, blockade of βAR suppresses DIT only in participants with high-BAT activity. All previous studies did not take the participants’ BAT activity into consideration and showed the combined data of all participants.

In addition, some mechanisms different from and/or in combination with the SN–βAR axis are likely involved in human DIT. One of the possible factors is secretin. Li et al. [33] found that the secretin receptor in murine brown adipocytes was highly expressed and that secretin activated BAT thermogenesis in vitro and in vivo. They also confirmed that the increment of plasma secretin levels induced by a single meal positively correlated with oxygen consumption and fatty acid uptake rates in human BAT. Therefore, meal-associated increase in circulating secretin activates BAT thermogenesis by binding to the receptor in brown adipocytes. Direct evidence for the thermogenic action of secretin on human BAT was obtained using FDG-PET/CT after secretin infusion, which significantly increased FDG uptake in supraclavicular BAT. However, to our knowledge, the insight into whether or not secretin action blockade suppresses DIT in humans remains unreported. Physiologically, acids in the duodenal luminal chime stimulate secretin secretion, but the mechanism on how the macronutrient composition of ingested meal affects the duodenal acidity and/or plasma secretin levels is still undetermined. Further human studies are needed to clarify the mechanisms of BAT-associated DIT, with references to the roles of secretin, other gastrointestinal factors, and the SN–βAR axis.

There are some limitations to our study. First, the study was to use a parallel design, not a crossover design which would be better to compare the effect of different meals. In fact, 11 out of 19 participants who consumed the C-meal also participated in the calorimetry for the P-meal, but none of them could participate in that for the F-meal, mainly because of different study years. However, this would not be critical in our study, the main objective of which was to examine the effect of BAT on DIT after individual meals. Another limitation to the present study is that DIT was assessed from the EE measurement only for 2 hours after meal ingestion. As DIT is known to persist for 5 hours or more, we may have missed any differences that occur at the later phase.

In conclusion, DIT after a single C-meal in healthy human participants was higher in those with higher BAT activity than in those with lower BAT activity. The DIT after a P-meal and a F-meal was higher and lower, respectively, than that after a C-meal; however, it had no correlation with BAT activity. These results suggest that BAT has a significant role in facultative DIT after carbohydrate ingestion but hardly after protein or fat ingestion. Thus, dietary carbohydrate may be the most effective macronutrient for postprandial activation of BAT. To obtain further evidence for this, direct measurement of EE by BAT itself is needed, for example, by using ¹⁵O[O_2, H₂O]-PET.

Participants

Through poster advertisements and oral communication, 41 healthy males aged 20–29 years were recruited. Before the study began, all participants provided written informed consent. They underwent FDG-PET/CT after acute cold exposure to assess BAT activity and indirect calorimetry in winter (December to March). The study protocol was approved by the institutional review board of Tenshi College. All experiments were performed in accordance with the tenets of the Declaration of Helsinki.

Test meals

The composition and energy content of the test meals were as follows. A carbohydrate-rich meal (C-meal) was prepared using commercially available nutritionally balanced foods (Calorie Mate Block, Calorie Mate Liquid, Otsuka Pharmaceutical Co., Tokyo, Japan). A protein-rich meal (P-meal) was prepared by combining nutritionally balanced foods and a liquid containing whey protein powder (DNS Inc. Tokyo, Japan). A fat-rich meal (F-meal) was prepared by combining nutritionally balanced foods, pork meat sausage, and a liquid containing rapeseed oil, skim milk, and soybean lecithin. These three meals yielded a carbohydrate/protein/fat (CPF) energy ratio of 51:11:38, 23:62:15, and 22:11:67, respectively. The participants consumed one of the test meals at a total energy of 430–580 kcal (7.9 kcal/kg body weight), with 100–200 mL of water as needed in 10 minutes.

[¹⁸F]FDG-PET/CT

BAT activity was measured using [¹⁸F]FDG-PET/CT, as previously reported [2]. Briefly, after fasting for 10−12 hours, participants wore light clothes (T-shirt and shorts) and remained in a room at 19 °C for 2 hours. Intermittently, a towel-wrapped ice block was placed against the soles of their feet. After 1 hour, the participants received [¹⁸F]FDG (1.66–5.18 MBq/kg body weight) intravenously and remained in the same cold conditions for another hour. One hour after FDG administration, PET/CT was performed at 24 °C room temperature using a dedicated PET/CT system (Aquiduo [Toshiba Medical Systems, Otawara, Japan], Biograph 16 [Siemens Medical Solutions, Knoxville, TN, USA], or Discovery PET/CT 600 [GE Healthcare, Waukesha, WI, USA]). Detectable FDG uptake into the supraclavicular BAT was assessed by visual judgment. In parallel, the FDG uptake was quantified as the maximal standardized uptake value (SUV_max).

Indirect calorimetry

Postprandial thermogenesis was estimated by measuring whole-body EE before and after meal ingestion with the use of a respiratory gas analyzer connected to a ventilated hood (AR-1, Arco System, Kashiwa, Chiba, Japan). Briefly, after fasting for 10–14 hours, the participants relaxed on a bed while wearing light clothing in a room at 27 °C, and oxygen consumption and carbon dioxide production were continuously recorded for 30 min. In the last 10-minute period, the stable value was used to calculate the basal EE. Then, the participants had one of the test meals (C-meal, P-meal, or F-meal) with a total energy of 7.9 kcal/kg body weight in 10 minutes. After 15, 45, 75, and 105 minutes, the respiratory gas parameters were recorded for 20 minutes, and the EE during the last 10 minutes was calculated. After the calorimetry, blood samples were collected from the median cubital vein.

Analysis of body composition and blood parameters

Body composition was measured by the multifrequency bioelectric impedance method (HBF-361, Omron Healthcare, Kyoto, Japan). Blood glucose, free fatty acids (FFA), and insulin were analyzed by Glucose C-test (Wako, Tokyo), NEFA C-test (Wako), and insulin ELISA (Mercodia AB, Sweden), respectively.

Statistical analysis

Values are presented as the mean ± standard deviation. All statistical data were analyzed using SPSS (version 26, IBM Japan, Tokyo, Japan). The EE values were examined using two-way analysis of variance (ANOVA) for repeated measures based on a within-participant factor (time) and a between-participant factor (BAT). The differences in DIT after the C-, P- and F-meals were compared by ANOVA followed by Tukey’s post hoc test. The differences between the High- and Low-BAT groups were compared by Student's t-test. P values of less than 0.05 were considered significant.

DATA AVILABILITY

The data that support the findings of this study are available from the corresponding author upon reasonable request.

ACKNOWLEDGMENTS

We thank Dr. Yuko Okamatsu-Ogura, Faculty of Veterinary Medicine, Hokkaido University and Dr. Hitoshi Wakabayashi, Laboratory of Environmental Ergonomics, Faculty of Engineering, Hokkaido University, for their help for recruiting participants.

AUTHOR CONTRIBUTIONS

SA, MM, and MS conceived and designed the study. SA, MM, TY, TH, TK, IO performed the experiments. SA, MM, TY, and MS performed data analysis and interpretation. MS wrote the paper, and all authors read and approved the paper.

CONFLICT OF INTEREST: The authors declare that no conflict of interest exists.

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Table 1 is available in the Supplementary Files section

No competing interests reported.

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Brown adipose tissue–associated postprandial thermogenesis in humans: Different effects of isocaloric meals rich in carbohydrate, fat, and protein

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Abstract

Figures

Introduction

Results

Participant characteristics

DIT based on the test meals

Effects of BAT activity on DIT

Postprandial response of blood parameters

Discussion

Methods

Declarations

References

Table

Additional Declarations

Supplementary Files

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