1. Introduction
The various types of tea produced from a single plant species, Camellia sinensis, are distinguished by the processing technique: unoxidized tea as green tea, half-oxidized tea as oolong tea, and fully oxidized tea as black tea. In the course of oxidation catalyzed by endogenous enzymes, catechins are transformed to polymerized polyphenols, and caffeine is slightly decomposed [
1], alterations that might yield benefits and/or risks on diverse physiologic functions.
The effects of tea on energy metabolism have been assessed in parallel with the effects of caffeine. Many studies report that accumulated energy expenditure over 24 h is increased by caffeine ingestion [
2,
3,
4], although one study found no effect [
5]. The effect of caffeine ingestion on accumulated fat oxidation over 24 h, however, was not examined in any of these four studies [
2,
3,
4,
5]. Ingestion of green tea extract increases 24-h energy expenditure and decreases the 24-h respiratory quotient (RQ) [
5]. Another study found that 3 days of oolong tea ingestion increased the accumulated energy expenditure and fat oxidation over 24 h, whereas caffeine alone did not significantly increase 24-h fat oxidation [
4]. Thus, unidentified ingredient(s) of tea other than caffeine affects energy metabolism, particularly fat oxidation. Importantly, in these previous studies on energy metabolism, caffeine and/or tea were ingested for only 1 [
2,
3,
5] or 3 days [
4]. Known as caffeine tolerance, the acute effect of caffeine to increase blood pressure and heart rate diminishes over 1–4 days when caffeine ingestion is continued [
6]. Together, these findings warrant further investigation of the subacute and chronic effects of tea and caffeine consumption on energy metabolism.
Caffeine inhibits sleep by antagonizing adenosine receptors [
7,
8]. The link between sleep and energy homeostasis is suggested by recent epidemiologic studies, the results of which point to insufficient sleep as a risk factor for future weight gain [
9,
10,
11,
12,
13,
14]. Furthermore, sleep and energy metabolism are closely linked through “multi-tasking” molecules such as orexin, NPY, leptin, insulin, serotonin, and IL6 [
15,
16]. Since changes in energy metabolism was expected after caffeine/oolong tea consumption in the present study, the crosstalk between regulatory mechanisms of energy metabolism and sleep warrants our experimental design to assess energy metabolism and sleep at the same time.
The effects of caffeine and tea should therefore be evaluated from two perspectives: their effects on energy metabolism and their effects on sleep. The objective of the present study is to assess the effects of subacute ingestion of oolong tea and caffeine on energy metabolism and sleep. To evaluate the effects on the time course of energy metabolism over 24 h, we used whole room indirect calorimetry with an improved time resolution [
17]. Sleep was simultaneously monitored by polysomnography during the indirect calorimetry.
4. Discussion
Caffeine ingestion (>100 mg) has an acute effect to increase the energy expenditure [
2,
3,
5,
28,
29,
30,
31,
32,
33,
34]. One of the main findings of the present study is that subacute ingestion of caffeine (103.6 mg) did not increase the energy expenditure, suggesting that near complete tolerance to caffeine, in terms of stimulating energy expenditure, was acquired over 2 weeks of caffeine ingestion. Consistent with this notion was the lack of a stimulating effect of subacute ingestion of caffeine on the heart rate and sympathetic nervous system activity in the present study.
Caffeine attenuates the buildup of the homeostatic sleep propensity and delays sleep onset by blocking cerebral adenosine receptors [
8,
35]. Tolerance to the effects of caffeine on sleep latency, however, develop over 4 days of caffeine ingestion [
36]. In the present study, sleep onset latency was not prolonged by subacute ingestion of caffeine. Thus, the effects of tolerance to caffeine on energy expenditure, heart rate, and sleep latency developed over the 2 weeks of caffeine ingestion. On the other hand, subacute ingestion of caffeine alone increased fat oxidation compared to the placebo trial, which is in contrast with the acute effects of caffeine ingestion on 24-h energy metabolism—that is, an increase in energy expenditure without affecting RQ [
2,
3,
4] or no effect on energy expenditure and RQ [
5]. Thus, the effect of caffeine ingestion on energy expenditure and fat oxidation was dissociable, but the mechanisms underlying the distinct effect of caffeine on energy expenditure and fat oxidation remain to be clarified. Of note, mean daily caffeine intake of adult male Japanese is 268 ± 176 (mean ± SD) mg, 6% of which is consumed as oolong tea [
37]. Dose of caffeine in the present study, 103.6 mg, was within a range of daily caffeine intake.
A positive effect of oolong tea consumption on energy expenditure was observed in two previous studies. One study reported that acute ingestion of oolong tea containing 77 mg caffeine, 81 mg epigallocatechin gallate, and 68 mg polymerized polyphenols increased energy expenditure following 2 h of tea consumption, but did not increase fat oxidation [
38]. Another study reported that oolong tea consumption (270 mg/day caffeine, 264 mg/day polymerized polyphenols) increased 24-h energy expenditure and fat oxidation on day 3 of consumption [
4]. In the present study, 2 weeks of oolong tea consumption increased fat oxidation, but did not increase the accumulated energy expenditure over 24 h, during sleep or during wake. Together, these findings indicate that over the 2 weeks of oolong tea consumption, the acute effects of oolong tea to increase energy expenditure were diminished but the stimulating effects on fat oxidation continued to be manifested. Experiments monitoring the adaptation process to chronic oolong tea consumption remain to be performed.
Considering half-life of caffeine ~5.7 h [
39], effects of oolong tea and caffeine consumption to decrease RQ and increase fat oxidation during sleep require cautious interpretation. The decrease in the RQ during the sleep by oolong tea consumption was significantly greater than that by caffeine ingestion. Visual inspection of the time course of the RQ suggested that the effect of oolong tea to decrease the RQ became clearer when the RQ in the placebo trial was lower; after overnight fasting before breakfast, in the late afternoon, and during sleep, but not immediately after oolong tea consumption at breakfast and lunch. These findings may reflect the slow pharmacokinetics of the substances responsible for the decreased RQ. Alternatively, the susceptibility of energy metabolism to the ingredients of the tea is enhanced during sleep, when fat oxidation is upregulated in a post-absorptive state. On the other hand, the effects of caffeine on the RQ did not correlate significantly with the inherent state of energy metabolism, i.e., the RQ in the placebo trial (
Figure 3). The findings of the present study suggest that the effects of unidentified ingredients in oolong tea to decrease the RQ were suppressed during wake. A plausible explanation for our findings is that the strong effects of a meal and subsequent insulin secretion masked the effect of oolong tea to decrease the RQ and stimulate fat oxidation.
The effects of oolong tea consumption to increase fat oxidation during sleep may have clinical relevance for controlling body weight and glucose metabolism. Several lines of evidence suggest that an individual’s capacity to oxidize dietary fat is a metabolic determinant of future weight gain [
40]. Mynatt et al. selected metabolically flexible and inflexible subjects based on the difference between 24-h and sleep RQ, and subsequent analysis of global skeletal muscle gene expression suggested a role of the RNA-binding protein HuR as a regulator of metabolic flexibilities in skeletal muscle metabolism [
41]. An elevated RQ during sleep may be a phenotype detected at the earliest stage in the pathogenesis of metabolic inflexibility and insulin resistance. The findings of the present study suggest that this phenotype may be corrected by interventions such as oolong tea consumption.
The effects of caffeine and oolong tea to increase the core body temperature were observed only during wake without any increase in energy expenditure, i.e., heat production. It is possible that an increase in the core body temperature by caffeine and oolong tea ingestion is due to reduced heat dissipation. The effects of caffeine and oolong tea on core body temperature are masked when peripheral heat dissipation is upregulated during sleep [
42]. The decreased heart rate and upregulated parasympathetic nervous activity by subacute caffeine consumption was not anticipated, and the mechanisms underlying these effects remain to be clarified.
This study has several limitations. First, abstinence from caffeine intake except the experimental beverage was imposed during the 14 days of intervention, but control for energy intake during the experimental 14 days was not perfect (
Figure 1). Second, the amount of caffeine consumed in the oolong tea and caffeine trials was matched in the present study to delineate the effective compound in the tea other than caffeine. This approach was used previously to assess the effect of green tea on the energy metabolism [
4,
5]. In the present protocol, however, the caffeine in the caffeinated water and the tea exerted strong effects on energy metabolism, and analysis of the small difference between the two experimental conditions is vulnerable to experimental error, i.e., the so-called ill-posed question. To further dissect the effective component in the oolong tea, experiments with decaffeinated oolong tea or tablets containing a specific catechin or polymerized polyphenol are warranted. The acute effects of epigallocatechin-3-gallate on energy expenditure and the RQ were assessed using a commercially available product, but no statistically significant effect on energy metabolism was detected [
43].
