Dietary red pepper ingestion increases carbohydrate... : Medicine & Science in Sports & Exercise (original) (raw)
Hot red pepper (Capsacum fruits), now one of the most widely consumed spices, has been used to flavor foods because of its pungency, color, and aroma (34). Also it has long been used as a preservative and medicine (33). Capsaicin is the major pungent principle in various Capsicum fruits(29). Kawada et al. reported that capsaicin enhances lipid metabolism (12) and energy metabolism(16)via catecholamine secretion from the adrenal medulla through sympathetic activation of the central nervous system(13,32,35). In humans Henry and Emery(10) reported that ingestion of chili and mustard sauces with meals results in a marked increase in diet-induced thermogenesis (DIT). It seems that hot red pepper ingestion increases energy expenditure (including DIT); however, it is unknown whether hot red pepper could change energy substrate utilization. Kawada et al. (16) have reported that intraperitoneal injection of capsaicin increased oxygen consumption and respiratory quotient (RQ). However, in another report they showed that capsaicin ingestion increased lipid metabolism in rats fed a high fat diet(12). Therefore, the effects of hot red pepper intake on energy substrate utilization are not clear.
Costill et al. (3,5,11) have suggested that research provides major support for a positive ergogenic effect of caffeine ingestion during endurance exercise. They proposed that the effect is achieved by an elevation in catecholamines, which enhance fat oxidation(either by increasing free fatty acid (FFA) levels or muscle triacyglycerol lipolysis) (8). Plasma FFA were elevated 1 h after caffeine ingestion in some studies(5,22,24,25,30) and unchanged in others (4,17,36). The failure to demonstrate consistently an increase in FFA may be a result of an increased uptake by the active muscle. However, many of these studies found no change in RQ (8).
Capsaicin (hot red pepper) is similar to caffeine in its physiological action, i.e., increasing plasma catecholamine levels. We have reported that capsaicin (6 mg·kg-1 body weight) has a liver glycogen sparing effect and stimulates lipolysis in adipose tissue during 2 h of treadmill exercise (20). However, the metabolic effects of hot red pepper are uncertain. The purpose of this study was to determine whether hot red pepper ingestion would elevate plasma catecholamine levels and alter energy substrate utilization at rest and during exercise in trained competitive runners.
METHODS
Subjects. Eight male middle and long distance runners (average training 100 km·wk-1) volunteered to participate in this investigation. The experimental procedures were explained and informed consent was obtained. The subjects were trained and had a maximal oxygen uptake(˙VO2max) of at least 53 ml·kg-1·min-1.˙VO2max was measured using standard indirect calorimetry techniques during an incremental exercise bout (9). Subject characteristics are shown in Table 1. The experiment was approved in accordance with the Helsinki Declaration of 1975.
Experimental design. Subjects reported to the laboratory on two occasions, separated in most cases by 1 wk. Each subject exercised for 1 h on two occasions after ingestion of a meal either with 10 g red pepper or without red pepper. The two trials were randomized. The subjects trained throughout the duration of the study; however, training was discontinued for 2 d before the experiment.
The day before the experiment the subjects were offered the same diet(about 3350 kJ) at 1900 h and then fasted until the next morning. For the test the subjects were awakened at 0530 h and arrived by car at the laboratory at 0630 h. After a 30-min rest, resting oxygen consumption was measured. After insertion of a 20-g cannula with a three-way valve into the forearm, the subjects were offered the experimental meal without or with 10 g of dried hot red pepper powder (Saemaul Kongjang l) as breakfast. The amount of hot red pepper powder used in this study was about 1.5 times the average daily consumption in Korean individuals (18). The composition of the dried hot red pepper powder is shown in Table 2. The subjects were allowed to ingest the experimental meals (with or without the dietary hot red pepper) with water (300 ml) over a 15-min period. The experimental meal composition was follows: 15% protein, 25% fat, and 60% carbohydrate as energy, respectively. The energy content of the meal was 2720 kJ.
After the meal subjects were allowed to sit in comfortable chairs. Blood samples from the cannula and expired gas samples were collected for 2.5 h at rest. After resting for 2.5 h, the subjects exercised using a bicycle ergometer (Monark, Varberg, Sweden) at a pedaling frequency of 50 rpm and an intensity of 150 W (approximate 60% of ˙VO2max) for 1 h. Blood and expired gas samples were collected every 30 min during rest and every 10 min during exercise. Blood samples during exercise were taken while the subjects were still exercising. The results of the experiment were not disclosed to the subjects or the investigators until completion of the entire study. The procedures of the experiment were performed in a laboratory chamber with a room temperature of 20°C and 50% humidity. The experimental procedures are shown in Figure 1.
Gas-exchange measurement. Expired gas samples were collected in a Douglas bag at 5-min intervals during rest and at 1-min intervals during exercise and directed to a CR-50 respirometer (Fukuoka Co., Ltd., Fukuoka, Japan) to measure ventilation. The mixed expired gas samples were simultaneously analyzed on a Beckman OM-11 and LB-2 (Beckman Instruments, Palo Alto, CA) gas analyzer previously calibrated for O2 and CO2(9).
Analysis of blood. Blood samples obtained from an earlobe were used to determined lactate levels. Blood lactate concentrations were measured on a Roche 640 lactate analyzer (Roche Bio-Electronics, Basel, Switzerland)(26). Blood samples obtained via the cannula were centrifuged at 4°C immediately after drawing and plasma was stored at-80°C. Plasma glucose (1), triacylglycerol, and free fatty acid (23) were measured as previously described. Plasma glycerol levels were determined by enzymatically using a kit(Boehringer Mannheim-Yamanouchi, Inc., Tokyo, Japan). Plasma epinephrine and norepinephrine levels were assayed by high-performance liquid chromatography(HPLC, Model LC-6A, Shimazu, Tokyo, Japan; pre-column, Prepac Set, Eicom, Kyoto, Japan; main column, CA-50DS, 150 × 4.6 mm, Eicom, Kyoto, Japan) as previously described (19).
Statistical analysis. The results are expressed as mean ± SEM. The data were analyzed using a two-way ANOVA (28). Time after meal (12 time points) and meal type (control and hot red pepper) were the independent variables. Significant differences between means were determined using Newman Kuels post-hoc test. The level of significance was set at P < 0.05.
RESULTS
Oxygen consumption. The ingestion of the meal with 10 g hot red pepper produced a slight increase in O2 consumption at 30 min after the meal, but it was not significant (P = 0.56). The O2 consumption after 30 min throughout the exercise was not different between the control group and those who ate the red pepper meal (Fig. 2A). Energy expenditure calculated from O2 consumption and respiratory quotient (RQ) showed the same trend of O2 consumption(Fig. 2B).
Respiratory quotient. The respiratory quotient increased slightly in both trials following the meal (Fig. 3). This initial rise was significantly higher in those who had the hot red pepper meal than the control group during the resting phase. The higher RQ in the hot red pepper group was maintained during 60 min of bicycle ergometer exercise.
Blood measurements. Plasma glucose concentrations were slightly(but not significantly) lower after 120 min for the hot red pepper group compared with those of the control group at the same time point(Fig. 4A). The concentration during exercise was not different between the two groups.
Blood lactate concentrations were significantly elevated at 60 and 150 min after the hot red pepper meal compared with the control meal during 150 min of rest (Fig. 4B). In addition, blood lactate levels were higher in the hot red pepper group compared with the control group during exercise.
Plasma triacylglycerol (TG) concentrations were higher at 60 and 150 min after the hot red pepper meal as compared with the control meal during exercise (Fig. 5A).
Plasma FFA levels were lower at 30 (P = 0.54), 40 (P = 0.51) and 50 min (P = 0.52) of the exercise and plasma glycerol concentrations were slightly decreased at 40 (P = 0.51), 50(P = 0.55), and 60 min (P = 0.52) of the exercise phase after the hot red pepper meal, but these differences were not significant(Figs. 5B, C).
Plasma catecholamines. Plasma epinephrine concentration was significantly elevated after 30 min for the hot red pepper group compared with the control group; however, there were no differences between the groups at 60 min and 150 min in the rest period (Fig. 6A). Plasma epinephrine concentrations were significantly higher during exercise at 60 min in the hot red pepper group compared with the control group
Plasma norepinephrine concentrations were also significantly increased at 30 min after the hot red pepper meal; however, the levels were not different after 60 and 150 min of rest or during exercise (Fig. 6B).
DISCUSSION
This study provides new information about the physiological effects of hot red pepper on energy metabolism at rest and during exercise. We show in this study that ingesting a meal with 10 g of hot red pepper powder increases respiratory quotient. Energy expenditure was slightly but nonsignificantly increased by the hot red pepper at 30 min after the meal. These results suggest that hot red pepper ingestion promotes carbohydrate oxidation by enhancing plasma epinephrine concentration without increasing energy expenditure. It is thought that the effects of the hot red pepper powder on energy metabolism may be caused by the capsaicin in the hot red pepper because the energy content in the meal with the hot red pepper powder was only 4% higher than the energy content of the control meal (2820 kJ vs 2720 kJ for the hot red pepper meal and control meal, respectively).
Effects of hot red pepper ingestion at rest. The ingestion of the meal with hot red pepper increased oxygen consumption by 13% (4.60 ± 0.33 vs 5.21 ± 0.14 ml·min-1·kg-1 for the control meal and hot red pepper meal, respectively) and energy expenditure by 10% (5.48 ± 0.50 vs 6.02 ± 0.29 kJ·min-1) compared with the control meal at 30 min after the meal, but not significantly(Fig. 2). Kawada et al. (16) reported that intraperitoneal injection of capsaicin (3 mg or 6 mg·kg-1) increased oxygen consumption in rats(16). Henry and Emery (10) examined the effect of spiced (3 g of chili sauce + 3 g of mustard sauce) food on resting metabolic rate in humans. They found that its ingestion resulted in a 25% increase in energy expenditure. Our data for oxygen consumption and energy expenditure in this study were consistent with their data.
Capsaicin ingested as a food component is readily absorbed through the gastrointestinal tract into the portal blood with serum albumin and is then transported to the whole body (15). It stimulates the visceral afferent sensory neurons (21). This stimulation is transmitted to the spinal neuron; then the adrenal sympathetic efferent nerve is activated, and enhanced adrenal catecholamines secretion occurs(34). Catecholamines that are secreted into the blood react with β-adrenergic receptors in liver and adipocytes, enhancing glycogenolysis and lipolysis and resulting in formation of energy-producing substrates (34). These mobilized energy substrates are circulated throughout the body and used in peripheral tissues such as muscles, which then increase body heat production. Yoshida et al.(37) found that intramuscular injection of capsaicin enhanced the interscapular brown adipose tissue (IBAT) function, i.e., increasing temperature, GDP-binding, and oxygen consumption. Kawada et al.(14) reported that intake of capsaicin slightly increased the thermogenin content in IBAT. These results show that capsaicin can increase IBAT thermogenesis. Therefore, we conclude that energy metabolism enhancement of IBAT partially contributes to the thermogenesis action of capsaicin in rats. In fact, ingestion of the hot red pepper meal in this study significantly increased the plasma concentration of epinephrine (81%) and norepinephrine (76%) at 30 min after the experimental meal compared with the control meal. However, we conclude that the increase of plasma catecholamines levels in this study did not affect thermogenesis in BAT because it is thought that thermogenesis action of BAT in humans is minimal(6).
Kawada et al. (16) reported intraperitoneal injection of capsaicin increased RQ and serum glucose and rapidly decreased liver glycogen content. They also found that treatment with propranolol (aβ-blocker) could protect against elevation of oxygen consumption and RQ. They concluded that the thermogenic action of capsaicin is exerted through direct or indirect adrenergic effects. However, they also reported(12) that capsaicin intake (0.014% of diet) for 10 d decreased abdominal adipose tissue weight by increasing lipolytic activity in rats fed a high fat diet (60% as fat). However, in the present study RQ and blood lactate levels were elevated following ingestion of a meal containing of 10 g hot red pepper. This result suggests that hot red pepper ingestion would enhance carbohydrate oxidation more than fat oxidation. We have also reported that a meal with hot red pepper ingestion significantly increases resting carbohydrate oxidation in men (38). The reasons for increased carbohydrate oxidation after a hot red pepper meal in the present study, in contrast with previous results, are that 1) hot red pepper was used, not capsaicin, 2) the study was designed to examine the acute effects of hot red pepper, 3) human subjects were used (others used rats), and 4) the experimental meal had low/medium fat content (high fat diets were used in other experiments).
Plasma TG levels in the present study were significantly increased at 120 min after the meal with hot red pepper (Fig. 5A). This result means that hot red pepper ingestion may promote TG secretion from the liver by increasing plasma catecholamine levels and/or inhibit TG utilization as an energy substrate. It appears more likely that the inhibition of TG utilization for energy substrate is the case in this study because RQ and blood lactate concentrations were higher in the hot red pepper trial than in the control trial at the same time point.
In contrast, Watanabe et al. have suggested that neonatal(31) and adult (34) capsaicin pretreatment inhibited capsaicin-induced adrenal catecholamine secretion in anesthetized rats. We conclude that our subjects did not have a long-term dietary history of hot red pepper use as they reported a weakness for spicy foods, including hot red pepper, prior to participation. Therefore, we did not need to address the effects of dietary history of hot red pepper on catecholamine secretion.
Effects of hot red pepper ingestion during exercise. The oxygen consumption and energy expenditure during 1 h of ergometry exercise were not different between the hot red pepper and control trials. However, RQ during exercise and at rest was significantly higher in the hot red pepper trial than in the control trial. Moreover, blood lactate levels were significantly higher at 40 and 60 min in the hot red pepper trial. These results suggest that hot red pepper ingestion before exercise mainly increases carbohydrate oxidation for exercise energy fuel. In addition, plasma catecholamine levels were increased by the hot red pepper meal ingestion before exercise, notwithstanding the exercise-induced increase in the plasma catecholamines levels.
Costill et al. (3,11), Ivy et al.(11), and Graham et al. (27) have reported that caffeine ingestion produced an ergogenic effect during prolonged endurance exercise. They proposed that caffeine elevated plasma catecholamine concentrations stimulate fat metabolism, either by increasing adipose tissue and/or muscle triacylglycerol lipolysis, and consequently FFA oxidation. In this regard, we expected that the effect of dietary hot red pepper ingestion would be similar to that of the caffeine. However, this was not the case. One explanation for the increased carbohydrate oxidation following hot red pepper ingestion is that a low fat diet (with hot red pepper) was given to the subjects. Therefore, it is thought that exogenous carbohydrate was oxidized for energy substrate rather than fat. It is well established that increased fat oxidation for energy substrate utilization enhances prolong exercise performance in athletes (2,7). According to these reports, hot red pepper ingestion before exercise could decrease endurance performance in athletes because hot red pepper can promote glycogen depletion in muscle and/or liver.
In summary, the meal with hot red pepper increased carbohydrate oxidation for energy substrate more than the meal without hot red pepper at rest. The increase of carbohydrate oxidation with the hot red pepper meal may be explained in part by the increased plasma catecholamine levels. This phenomenon was investigated during 1 h submaximal exercise.
Figure 1-Experimental protocol.
Figure 2-Oxygen consumption (:
A ) and energy expenditure ( B ) during the rest and exercise after the control (○) or hot red pepper meal (•) ingestion. Values are means± SEM.
P < 0.05).
Figure 4-The changes in plasma glucose (:
A ) and blood lactate ( B ) after ingestion of the control (○) or hot red pepper (•) meal during the rest and exercise. Values are means± SEM. *Statistically significant difference from the values of the control meal ( P < 0.05).
Figure 5-The changes of plasma triacylglycerol(:
A ), free fatty acid ( B ), and glycerol ( C ) after ingestion of the control (○) or hot red pepper (•) meal during rest and exercise. Values are means± SEM. *Statistically significant difference from the values of the control meal ( P < 0.05).
Figure 6-Concentrations of plasma epinephrine(:
A ) and norepinephrine ( B ) after ingestion of the control (○) or hot red pepper (•) meal during the rest and exercise. Values are means ± SEM. *Statistically significant difference from the values of the control meal( P < 0.05).
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Keywords:
RESPIRATORY QUOTIENT; FAT OXIDATION; CARBOHYDRATE OXIDATION; CATECHOLAMINES; EXERCISE
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