- Email: [email protected]
Oolong Tea and Weight Loss
CHAPTER
42
Oolong Tea and Weight Loss Rong-Rong He1, Hiroshi Kurihara1, Victor R. Preedy2 1 Institute of Traditional Chinese Medicine and Natural Products, Jinan University, Guangzhou, China 2 Diabetes and Nutritional Sciences Division, School of Medicine, Kings College London, London, UK
Abbreviations EC epicatechin ECG epicatechin gallate EE energy expenditure EGC epigallocatechin EGCG epigallocatechin gallate EGF epidermal growth factor EI energy intake FAS fatty acid synthase HDL high-density lipoprotein HDL-C high-density lipoprotein cholesterol HSL hormone-sensitive lipase LDL low-density lipoprotein LDL-C low-density lipoprotein cholesterol OTPP oolong tea-polymerized polyphenols TC total cholesterol TF-1 theaflavin TF-2a theaflavin 3-gallate TF-2b theaflavin 3’-gallate TF-3 theaflavin 3,3’-digallate TG triglyceride
INTRODUCTION Historically, teas have been widely used to prevent obesity and improve lipid metabolism. However, the evidence-basis of such practices has hitherto been lacking. Oolong tea, green tea and black tea, which are non-, partially- and fully-fermented/oxidized teas, respectively, are the most commonly consumed teas, though there are others, such as white tea, which are less popular. Oolong tea is particularly consumed in Asia. In fact, oolong tea has an ancient history dating back over 400 years, originating from the Fujian province of China during the Ming dynasty. Presently, oolong tea from Fujian is exported to the whole world. Oolong tea is made from the tea plant Camellia sinensis through a unique process which includes withering under the strong sun and oxidation before curling and twisting. Oolong tea is semi-oxidized, and thus its chemical composition is reported to be more complex than other teas. Tea in Health and Disease Prevention. DOI: 10.1016/B978-0-12-384937-3.00042-2 Copyright Ó 2013 Elsevier Inc. All rights reserved.
509
SECTION 5 General Protective Aspects of Tea-Related Compounds
Oolong tea is not only renowned for its unique taste, but also its putative health benefits. One of these is its effects on weight loss. In China oolong tea is traditionally considered to have anti-obesity and hypolipidemic effects. Indeed this is supported by experimental studies in the early 1990s which confirmed that consumption of oolong tea reduced body weight. Since then, other studies have reported that the consumption of oolong tea blocked lipid absorption or promoted fat oxidation. In this chapter we describe in detail the putative mechanisms through which oolong tea impacts body weight and obesity.
ANTI-OBESITY EFFECTS OF OOLONG TEA IN HUMAN STUDIES Two decades ago Chen et al., (1992) first reported that oolong tea consumption effectively lowered blood pressure, plasma triglyceride and cholesterols in humans. Thereafter, they performed another study on 102 females and found that 67% of subjects had a reduced body weight after consumption of 8 g dry oolong tea leaves daily for six consecutive weeks (Chen et al, 1998). Although the dose of oolong tea in this clinical study was larger than normal daily intakes, the weight-reducing effects of oolong tea were shown by scientists for the first time. These two reports from China initiated further studies on weight loss and antiobesity effects of oolong tea.
510
In the beginning of the 21st century, the anti-obesity effects of oolong tea attracted Japanese researchers and tea developers. Suntory Ltd. (Osaka, Japan), a Japanese company famous for its drinks and beverages, had developed oolong tea as a commercial drink and carried out many scientific studies on its health benefits. They conducted a randomized crossover study to measure the influence of oolong tea consumption on 24 hour energy expenditure in 12 male volunteers. They provided full- or half-strength oolong tea, and caffeinated (containing caffeine equivalent to full strength oolong tea) or non-caffeinated water and measured energy expenditure by calorimetry. The results showed that consuming full strength oolong tea increased energy expenditure (that is burned more calories per day) than caffeinated water (Rumpler et al., 2001). The 24 hour resting energy expenditure increased from 7,032 kJ/d (water group) to 7,158, 7,320 and 7,227 kJ/day for the caffeinated water, half-strength and full-strength oolong tea groups, respectively. Suntory also conducted another study on females. This study involved 11 female participants consuming infusions of oolong tea (Komatsu et al., 2003). The results showed that oolong tea increased energy expenditure significantly, peaking at 90 minutes and the effect persisted for 120 minutes (Komatsu et al., 2003). Thus, the subject’s mean resting energy expenditure increased from approx 210 kJ/h to 240 kJ/h (Komatsu et al., 2003). Although this is a relatively moderate increase, consideration needs to be given to the implications of such increases over the long term or on a more frequent episodic basis. Additionally, Suntory researchers also conducted a double-blind placebo-controlled crossover experiment. Subjects were given a high-lipid diet containing 38 g/day of lipid, and a total of 750 ml of placebo or polyphenol-enriched oolong tea infusions, at three meals per day for a month. Feces were collected to measure the excretion of lipids. The study found that lipid excretion into feces was significantly higher in those consuming polyphenol-enriched oolong tea compared to those in the placebo group. Thus fecal lipid excretion increased from a mean of 9.4 (placebo group) to 19.3 g/3 day (polyphenol-enriched oolong tea group, P < 0.01; Hsu et al., 2006). In the same study, cholesterol excretion increased from 1.2 to 1.8 g/3 day (P ¼ 0.056) for the placebo and polyphenol-enriched oolong tea groups, respectively (Hsu et al., 2006). An epidemiological study of 1,103 Taiwanese adults found that habitual tea drinkers (defined as those who drank tea at least once per week for 6 months) who consumed tea for more than 10 years had a lower percentage of body fat (decrease by 19.6%) and waist to hip ratio (decrease by 2.1%) when compared to non-habitual consumers. This survey suggests
CHAPTER 42 Oolong Tea and Weight Loss
that consuming oolong tea may be beneficial in terms of anti-obesity therapies (Wu et al., 2003). Alternatively, there may be lifestyle factors that distinguish tea drinkers from non tea drinkers, and these factors themselves may contribute to the measured differences in body fat and waist to hip ratio. However, the latter supposition is not supported by the aforementioned studies by Chen et al., (1998), Rumpler et al., (2001), Komatsu et al., (2003) or Hsu et al., (2006) which clearly showed a direct beneficial effect of oolong tea on energy expenditure and lipid excretion. Other researchers also found that an intake of oolong tea significantly influenced, in a beneficial way, plasma adiponectin levels, low-density lipoprotein (LDL) particle size, total cholesterol (TC), high-density lipoprotein cholesterol (HDL-C), low-density lipoprotein cholesterol (LDL-C), serum triglyceride (TG) and plasma glucose levels in patients with coronary artery disease (Shimada et al., 2004). Stress-induced LDL oxidation was also prevented by the consumption of oolong tea in women (Kurihara et al., 2003). More recently, a large clinical trial was conducted to verify the anti-obesity effects of oolong tea. In a total of 102 obese subjects tested, 70% of severely obese subjects had lost more than 1 kg and 22% of them lost 3 kg or more of body weight after oolong tea consumption for 6 weeks. Similarly, 66% of overweight subjects lost more than 1 kg after oolong tea consumption. Subcutaneous fat content was decreased and waist circumference was reduced in 12% of the subjects. Moreover, it was observed that plasma TG levels of human with hypertriglyceridemia decreased by about 20%. The plasma TC levels in the subjects with hypercholesterodemia were also significantly decreased (He et al., 2009). All these research findings suggest that oolong tea is useful in treating obesity or hyperlipidemia in the clinical setting.
ANTI-OBESITY EFFECTS OF OOLONG TEA IN LABORATORY STUDIES The preceding sections clearly show that oolong tea has anti-obesity effects, from the evidence of a variety of clinical studies. Quite a number of pre-clinical studies have also been performed on the anti-obesity effects of oolong tea. For example, high-fat or high-sucrose diet-induced obesity models were used to evaluate the efficacy of oolong tea on the inhibition of fat accumulation in animals. Scientists in Ehime University (Ehime, Japan) found feeding a high-fat diet containing 40% beef tallow to mice for 10 weeks produced significant increases in body weight and parametrial (i.e. within the vicinity of the uterus) white adipose tissue weight compared to those fed laboratory chow. However, feeding high-fat diets containing 5% oolong tea powder reduced body weights by 10% and parametrical adipose tissue weight by 51% within 10 weeks (Han et al., 1999). Yang et al. (2001) also found that body weight gain was significantly reduced (by 35%) in rats fed with a high-sucrose diet and concomitantly provided with oolong tea extracts. In this study by Yang et al. (2001) the food efficiency (g body weight gain per Kcal) was reduced by 27%. Another study demonstrated that oolong tea lowered the fat/body ratio in rats fed with a high-energy diet (Mo et al., 2007). The studies above also showed that oolong tea effectively alleviated hyperlipidemia and hypertriglyceridemia. However, they were all based on models which used high-fat or highsucrose diets. In order to elaborate on the anti-obesity effects of oolong tea in animals fed normal diets, Kuo et al. (2005) evaluated the weight-suppressive effects of orally feeding oolong tea leaves to male Sprague-Dawley rats for 30 weeks. Compared with the control group, the relative weight ratios of liver to epididymal adipose tissue were decreased significantly by oolong tea consumption. Apart from observing the apparent effects on loss of body weight, measurement of relevant lipid metabolism indicators reveal that oolong tea has significant hypolipidemic effects.
511
SECTION 5 General Protective Aspects of Tea-Related Compounds
A correlation between obesity and hyperlipidemia has been previously confirmed in numerous studies. This is important to consider as excessive plasma TG and TC in obese subjects has the potential to cause cardiovascular diseases. Therefore, it is advisable to keep plasma TG and TC at normal levels to prevent diseases such as arteriosclerosis, cerebral apoplexy and myocardial infarction. In this regard, many studies have been conducted to clarify the effects of oolong tea on the reduction of circulating TG and TC levels in rats fed with high-fat or highsucrose diets. Thus, the levels of high density lipoproteins (HDL; known as ‘good lipoproteins’) are increased, and atherogenic indices reduced by oolong tea (Han et al., 1999; Yang et al., 2001). In addition, the HDL-C level are increased, and the LDL-C (known as ‘bad cholesterol’) level is decreased in rats treated with oolong tea (Han et al., 1999; Yang et al., 2001). Oolong tea also has protective effects in ameliorating metabolic abnormalities in plasma lipid profiles in mice subjected to restraint stress. When a lipid emulsion was injected intravenously into mice, restraint stress prolonged the half-life of TG elimination (Kurihara et al., 2002). Therefore, TG metabolism was disrupted by stress, and the use of TG as an energy source was decreased. The intake of oolong tea alleviated the stress-induced changes in lipid metabolism. This effect may have arisen from some non-specific stress-relieving property of oolong tea or acceleration of lipid metabolism by its bioactive components (Kurihara et al., 2002). Accordingly, one can surmise that oolong tea exerts its therapeutic potential by alleviating hyperlipidemia and hypertriglyceridemia.
ACTIVE COMPONENTS OF OOLONG TEA IN OBESITY REDUCTION
512
Polyphenols, alkaloids, saponins, polysaccharides and L-theanines are the main components that contribute to oolong tea’s putative medicinal properties (Jia et al., 2005; Khan and Mukhtar, 2007; Bukowski and Percival, 2008; Monobe et al., 2008). Caffeine and polyphenols are arguably the most important bioactive components in regards to the antiobesogenic properties of oolong tea. Caffeine, which is present at levels of up to 5e6% in tea, plays a key role because of its thermogenic and fat oxidizing properties. Several studies have shown that the polyphenols present in oolong tea reduce the risk of several diseases by virtue of their anti-fungal, anti-inflammation, anti-mutagenic, anti-oxidative effects. This is in addition to the ability of oolong tea to lower plasma TC and TG levels, and reduce blood pressure and platelet aggregation. Catechins, including epigallocatechin gallate (EGCG), epigallocatechin (EGC), epicatechin gallate (ECG) and epicatechin (EC), are the most biologically active group of polyphenols in oolong tea. EGCG accounts for 50e80% of the total catechins in oolong tea. Other polyphenols, such as flavan-3-ols, proanthocyanidins, theasinensins, and a few hydrolyzable tannins also inhibit pancreatic lipase activity. In addition, tea saponins were reported to inhibit pancreatic lipase activity in vitro (Han et al., 1999). However, this aforementioned observation needs to be interpreted with care because it did not consider the interference of tea catechins on pancreatic lipase (Han et al., 1999). Oolong tea polymerized polyphenols (OTPP) are derived from tea catechins by polyphenol oxidases and produced during the semi-fermentation and heating process of production. The fermentation of polyphenols in oolong tea ranges from 8% to 85%, depending on the variety and production style of the tea. Thearubigins and theaflavins are the representative and most abundant OTPPs in oolong tea (as shown in Figure 42.1). OTPPs are not found in green tea, and they are different from those in fully-fermented, black tea. OTPPs have inhibitory activities in vitro against some metabolic enzymes, such as glycosyltransferase and lipase. In animal studies, OTPP significantly suppresses both lymphatic and serum TG absorption when subjects are given high-fat diets (Nakai et al., 2005b). In human studies, OTPPs suppress postprandial serum TG and chylomicron in subjects fed with a high-lipid diet (Hara et al., 2004). Accordingly, these studies suggest that OTPPs are especially important components in oolong tea (Toyoda-Ono et al., 2007).
CHAPTER 42 Oolong Tea and Weight Loss
513 FIGURE 42.1 Structures of Catechins and Oolong Tea-Polymerized Polyphenols
ANTI-OBESITY MECHANISMS OF OOLONG TEA Excessive adiposity results from a disorder of energy homeostasis, which is the consequence of excessive energy intake that is not balanced by expenditure (Redinger, 2009). Either increasing energy expenditure (EE) or decreasing energy intake (EI) can achieve the goal of losing weight. So far, evidence suggests that the major mechanisms responsible for the anti-obesity effects of oolong tea include reducing energy intake, stimulating energy expenditure, suppressing lipogenesis and promoting lipolysis in adipose tissue. The preceding discussion raises the question of how oolong tea can assist in the prevention and/or the treatment of obesity. Firstly, oolong tea could decrease energy intake by inhibiting glucose or fat absorption. It was found that polyphenols, such as catechins, in oolong tea could inhibit the activities of some digestive enzymes like a-glucosidase and invertase to reduce absorption of glucose and sucrose (Matsumoto et al., 1993). Based on these findings, Liu and Huang (2010) found that oolong tea induced a reversible inhibition of a-amylase activity and blocked the degradation of carbohydrates, lowered blood glucose level and subsequently prevented the transformation of glucose into fats in adipose tissue. However, the decrease in energy intake by oolong tea is not uniquely dependent on the reduction of carbohydrate absorption. Other studies have shown that oolong tea suppresses the intestinal absorption of dietary fat by inhibiting pancreatic lipase (Han et al., 1999). The digestion of dietary fat is facilitated by pancreatic lipase, hence its inhibition could significantly decrease lipid absorption and increase lipid excretion into the feces. As shown in Table 42.1, the polyphenols
SECTION 5 General Protective Aspects of Tea-Related Compounds
TABLE 42.1 Inhibition of Pancreatic Lipase by Oolong Tea Extract and Catechins In vitro Polyphenols
IC50 (mM )
()-epigallocatechin 3,5-di-O-gallate Prodelphinidin B-2 3,3’-di-O-gallate Assamicain A Oolonghomobisflavan A Oolonghomobisflavan B Oolongtheanin 3’-O-gallate Theafavin Theafavin 3,3’-O-gallate
0.098 0.107 0.120 0.048 0.108 0.068 0.106 0.092
(Nakai et al, 2005a; Birari and Bhutani, 2007)
514
commonly found in oolong tea show potent inhibitory activities (IC50) on pancreatic lipase in vitro (Birari and Bhutani, 2007). Another piece of research also showed that oolong tea extract and catechins inhibit pancreatic lipase activity, and in this study ECG and EGCG were more potent than oolong tea extract (He et al., 2009). Other studies have shown lipid absorption was inhibited, since lipid excretion into the feces was significantly higher in humans consuming oolong tea. Cholesterol excretion also tended to increase when subjects were fed a high-lipid diet (Hsu et al., 2006). Based on the analysis of the structureeactivity relationship of these polyphenols, galloyl-ester moieties were found to be very important for inhibiting pancreatic lipase activities. This is supported by the observation that the inhibitory activity of these polyphenols is significantly decreased when the galloyl-ester moieties of the polyphenols are eliminated with tannin acyl hydrolase (Hsu et al., 2006). Furthermore, the inhibitory activity of OTPP on pancreatic lipase is stronger than that of total oolong tea extracts in vitro. These studies suggest that functional galloyl moieties and the polymerization of catechins are required for pancreatic lipase inhibition (Nakai et al., 2005a). Apart from inhibiting intestinal absorption, appetite suppression is another important way to limit energy intake. Many studies have confirmed the suppression of appetite by caffeine in rodents and humans. Kovacs et al. (2004) found lower leptin concentrations in habitual caffeine-beverage drinkers. Studies by Westerterp-Plantenga et al. (2005) also indicated that higher satiety was found in humans having habitual caffeine or tea consumption. The inhibitory effect of caffeine on appetite is related to a corticotropin-releasing factor and the sympathoadrenal system. Conceivably, the long-term consumption of oolong tea e which contains caffeine or other active compounds e may promote weight loss by suppressing appetite. In addition, theanines in oolong tea may also contribute to the regulation of appetite. It was reported that theanine could pass through the bloodebrain barrier and subsequently increase the release of dopamine or reduce serotonin concentrations in the brain. The importance of this relates to the fact that dopamine and serotonin are important neurotransmitters regulating appetite (Zheng et al., 2004). All the above indicate that appetite suppression by caffeine or theanines may be partly responsible for the anti-obesity effects of oolong tea. After controlling energy intake, it is also important to increase energy expenditure. Oolong tea is a semi-fermented tea containing more caffeine than green tea (Kao et al., 2006). It has been known for many years that caffeine can stimulate energy expenditure to varying degrees, and the use of caffeine alone or in combination with ephedrine has been proposed for the treatment of obesity (Dulloo et al., 1986, 1987; Astrup et al., 1991). Animal studies and prospective epidemiologic studies on weight loss suggest that long-term caffeine consumption decreases body weight (Cheung et al., 1988; Muroyama et al., 2003; Zheng et al., 2004; Lopez-Garcia et al., 2006; van Dam et al., 2006). These studies prove that caffeine increases energy expenditure both in animals and humans. The notion that caffeine is solely responsible for the increase in energy expenditure is controversial, however, since there are a number of complex constituents in
CHAPTER 42 Oolong Tea and Weight Loss
oolong tea. Some reports have claimed that oolong tea promotes the preferential use of fat as an energy source and achieves its anti-obesity effects through compounds other than caffeine (Rumpler et al., 2001). Subsequently, Komatsu’s studies (Kamatsu et al., 2003) confirmed that oolong tea increases energy expenditure not only via caffeine or EGCG but also by some types of polymerized polyphenol. Therefore, more research needs to be done to understand which components account for the increased energy expenditure in tea drinking. Inhibiting lipogenesis is another important factor in weight loss. Lipogenesis is the synthesis of esterified fatty acids, which produces TG from carbohydrates or other energy sources acquired in the diet. Fatty acid synthase (FAS) is an important enzyme involved in lipogenesis. It was reported that FAS might be a potential therapeutic target for the treatment of obesity (Loftus et al., 2000), and EGCG and ECG were found to be potent inhibitors of FAS. FAS expression was suppressed by EGCG, as studied in vitro, but not by catechin, EC or EGC. Furthermore, theaflavin (TF-1), theaflavin 3-gallate (TF-2a), theaflavin 3’-gallate (TF-2b) and theaflavin 3,3’-digallate (TF-3) also significantly suppressed FAS expression at both protein and mRNA levels (Loftus et al., 2000). These changes may lead to the inhibition of cell lipogenesis. Additional experimental results demonstrated that epidermal growth factor (EGF)-induced biosynthesis of lipids including TG, cholesterol and FA, and cell proliferation were significantly suppressed by EGCG and TF-3 (Yeh et al., 2003). These findings suggest that tea polyphenols suppressed FAS expression by down-regulating EGF receptor/PI3K/Akt/ Sp-1 signal transduction pathways (Lin and Lin-Shiau, 2006). Oolong tea could also exert anti-obesity effects by promoting lipolysis in adipocytes. Some evidence from high-fat-diet-treated mice indicated that caffeine isolated from oolong tea enhanced noradrenalin-induced lipolysis. As a non-specific antagonist of adenosine receptors, caffeine modifies energy metabolism through increasing intracellular free Ca2þ concentration and promoting catecholamine release from noradrenergic nerve terminals. Caffeine elevates metabolic rate and fatty acid availability by lipolysis. Meanwhile, caffeine also increases lipolysis by inhibiting the cyclic nucleotide phosphodiesterase, which is responsible for catalyzing the conversion of cyclic AMP to AMP. The resulting high tissue concentrations of cyclic AMP activate inactive hormone-sensitive lipase (HSL) to promote lipolysis. Finally, oolong tea could exert anti-obesity effects by modulating the proliferation and differentiation of adipocytes. Because adipocyte tissue growth can be due to both hyperplasia and hypertrophy, the screening of anti-obesity materials has focused on the processes of adipocyte proliferation and differentiation. Catechins and EGCG were proven to reduce the total TG accumulation in murine 3T3-L1 preadipocytes during their differentiation into adipocytes induced by dexamethasone, 1-methyl-3-isobutylxanthine and insulin (Hasegawa et al., 2003). EGCG and ECG inhibited acetyl-CoA carboxylase activity, a rate-limiting step in the fatty acid biosynthesis pathway, in 3T3-L1 cells. Therefore, the in vitro effect of EGCG on fat tissues may be mediated by the modulation of hormone-stimulated cell proliferation and differentiation or by the inhibition of lipogenesis or promotion of lipolysis (Hasegawa and Mori, 2000). To summarize, the above studies on the mechanisms of weight loss by oolong tea suggest that complex, multifaceted pathways are involved. However, the concomitant imposition of diet and other lifestyle factors on the cause, progression and regression of obesity and also genetic diversity all need to be considered in the development of obesity. For example, it has been proposed that the effects of catechins on energy expenditure may vary depending on genetic variability in COMT enzyme activity (Hursel et al., 2009).
COMPARISON OF THE ANTI-OBESITY EFFECTS OF OOLONG TEA AND GREEN TEA Oolong tea and green tea are produced from the same plant species (Camellia sinensis), but are distinguished by their processing techniques. For green tea production, the leaves are
515
SECTION 5 General Protective Aspects of Tea-Related Compounds
TABLE 42.2 Contents of Polyphenol and Caffeine in Oolong Tea and Green Tea Extracts Components Caffeine
Oolong Tea (mg/g)
Green Tea (mg/g)
64
53
30 6 10 2
43 25 5 8
14 16 3 7 114
29 19 6 5 e
Flavan-3-ols without galloyl moeity Gallocatechin Epigallocatechin Catechin Epicatechin Flavan-3-ols with galloyl moiety Epigallocatechin gallate Gallocatechin gallate Epigallocatechin gallate Catechin gallate Oolong tea polymerized polyphenols (OTPP) (Toyoda-Ono et al., 2007)
516
steamed soon after harvest to stop enzyme reactions. The leaves are then ground by hand to break the cells. For oolong tea production, the leaves are fermented under defined conditions to produce specific flavors by enzyme reactions. The leaves of oolong tea are not ground e the cells are kept intact. These processing differences mean that the components of oolong tea and green tea are quiet different (as shown in Table 42.2). The concentration of catechins in oolong tea is approximately half of that of green tea, while polymerized polyphenols seem to be absent in green tea but have significant concentrations in oolong tea. Although the polyphenol contents of oolong tea and green tea are markedly different, various studies have shown that green tea is also effective in weight loss, and the effects of the two have been compared in several studies. Ikeda et al. (1992) indicated that both tea catechins and heat-treated catechins suppress postprandial hypertriacylglycerolemia to almost the same extent in rats. They also showed that that such tea catechins inhibited the activity of pancreatic lipase in vitro in a dose-dependent manner (Ikeda et al., 1992). However, Yang reported that green tea exerted greater antihyperlipidemic effects than oolong tea (Yang et al., 2001). In contrast, Komatsu et al. (2003), from the Tokushima School of Medicine in Japan, claimed that oolong tea confers greater health benefits than green tea. For example, they found that the cumulative increases in energy expenditure after the consumption of oolong tea and green tea for 120 min were significantly increased by 10% and 4%, respectively (Komatsu et al., 2003). Studies also indicated that oolong tea shows a stronger ability to lower serum TG levels than non-fermented green tea. Oolong tea as well as non-fermented green tea, fully fermented pu-erh tea, and black tea all reduce serum level of total cholesterol, but partially fermented oolong tea leaves are strongest (Kuo et al., 2005). However, Wolfram (2007) reviewed the anti-obesity effects of green tea and suggested that the study of Komatsu may not be accurate because it lasted for only one session, and involved just 11 young females. Thus the results of the comparisons of anti-obesity effects of oolong tea with other types of tea are controversial and merit investigation.
CONCLUSION Tea has been used historically and currently as a popular beverage in both Oriental and Western countries. Evidence based on modern molecular and cellular studies support the
CHAPTER 42 Oolong Tea and Weight Loss
notion that consumption of green, oolong and black tea appears to modulate body weight and have a putative role in preventing obesity. Different animal and human experiments have attempted to elucidate the precise mechanisms through which this occurs. However, some results seem fragmentary and there is some inconsistency. Nevertheless, the weight-loss inducing properties of oolong tea can be categorized into several mechanisms. The active components of oolong tea which improve lipid metabolism appear to be caffeine and the polyphenols. Oolong tea appears to act as an anti-obesogenic agent and in weight control through its suppression of pancreatic lipase, thus impeding the absorption of lipids in the intestines. At the same time, oolong tea also increases energy expenditure by inducing thermogenesis and lipolysis. It also suppresses appetite. The present understanding of the anti-obesogenic effects of oolong tea might be superficial. However, these findings could lead to great discoveries in the future including the usage of oolong tea in treating diabetes. In summary, oolong tea is significantly hypolipidemic and anti-obesogenic.
SUMMARY POINTS l
l
l
l
In China, oolong tea has traditionally been considered to have anti-obesity and hypolipidemic effects. Since the early 1990s, many studies in both rodents and humans have verified the traditional notion that oolong tea is effective in obesity control and hyperlipidemia. The anti-obesity effects of oolong tea are due to the inhibition of energy intake and the promotion of energy utilization. These effects are due to its bioactive components, including caffeine, catechins and polymerized polyphenols.
References Astrup, A., Toubro, S., Cannon, S., et al., 1991. Thermogenic synergism between ephedrine and caffeine in healthy volunteers: a double-blind, placebo-controlled study. Metabolism 40, 323e329. Birari, R.B., Bhutani, K.K., 2007. Pancreatic lipase inhibitors from natural sources: unexplored potential. Drug Discov. Today 12, 879e889. Bukowski, J.F., Percival, S.S., 2008. L-theanine intervention enhances human gamma delta T lymphocyte function. Nutr. Rev. 66, 96e102. Chen, W., Yang, Z., Hosoda, K., et al., 1998. Clinical efficacy of oolong tea on anti-simple obesity. Nippon Rinsho Eiyo Gakkai Zasshi 20, 83e90. Chen, W.Y., Zheng, Q.Z., Ni, F., et al., 1992. Clinical observation of anti-hypertensive & hypolipidemic effects of fujian oolong tea. Journal of Fujian College of Traditional Chinese Medicine 2. Cheung, W.T., Lee, C.M., Ng, T.B., 1988. Potentiation of the anti-lipolytic effect of 2-chloroadenosine after chronic caffeine treatment. Pharmacology 36, 331e339. Dulloo, A.G., Miller, D.S., 1986. The thermogenic properties of ephedrine/methylxanthine mixtures: human studies. Int. J. Obes. 10, 467e481. Dulloo, A.G., Miller, D.S., 1987. Aspirin as a promoter of ephedrine-induced thermogenesis: potential use in the treatment of obesity. Am. J. Clin. Nutr. 45, 564e569. Flatt, J.P., 2007. Differences in basal energy expenditure and obesity. Obesity 15, 2546e2548. Han, L.K., Takaku, T., Li, J., et al., 1999. Anti-obesity action of oolong tea. Int. J. Obes. 23, 98e105. Hara, Y., Moriguchi, S., Kusumoto, A., et al., 2004. Suppressive effect of oolong tea polymerized polyphenolsenriched oolong tea on postprandial serum triglyceride elevation. Jpn. Pharmacol. Ther. 32, 335e342. Hasegawa, N., Mori, M., 2000. Effect of powdered green tea and its caffeine content on lipogenesis and lipolysis in 3T3-L1 cell. J. Health Sci. 46, 153e155. Hasegawa, N., Yamda, N., Mori, M., 2003. Powdered green tea has antilipogenic effect on zucker rats fed a high-fat diet. Phytother. Res. 17, 477e480. He, R.R., Chen, L., Lin, B.H., et al., 2009. Beneficial effects of oolong tea consumption on diet-induced overweight and obese subjects. Chin. J. Integr. Med. 15, 34e41. Hsu, T.F., Kusumoto, A., Abe, K., et al., 2006. Polyphenol-enriched oolong tea increases fecal lipid excretion. Eur. J. Clin. Nutr. 60, 1330e1336.
517
SECTION 5 General Protective Aspects of Tea-Related Compounds
Hursel, R., Viechtbauer, W., Westerterp-Plantenga, M.S., 2009. The effects of green tea on weight loss and weight maintenance: a meta-analysis. Int. J. Obes. 33, 956e961. Ikeda, I., Imasato, Y., Sasaki, E., et al., 1992. Tea catechins decrease micellar solubility and intestinal absorption of cholesterol in rats. Biochim. Biophys. Acta. 1127, 141e146. Jia, X.-D., Han, C., Chen, J.-S., 2005. Tea pigments induce cell-cycle arrest and apoptosis in HepG2 cells. World J. Gastroenterol. 11, 5273e5276. Kao, Y.H., Chang, H.H., Lee, M.J., Chen, C.L., 2006. Tea, obesity, and diabetes. Mol. Nutr. Food Res. 50, 188e210. Khan, N., Mukhtar, H., 2007. Tea polyphenols for health promotion. Life Sci. 81, 519e533. Komatsu, T., Nakamori, M., Komatsu, K., et al., 2003. Oolong tea increases energy metabolism in Japanese females. J. Med. Invest. 50, 170e175. Kovacs, E.M.R., Lejeune, M., Nijs, I., Westerterp-Plantenga, M.S., 2004. Effects of green tea on weight maintenance after body-weight loss. Br. J. Nutr. 91, 431e437. Kuo, K.L., Weng, M.S., Chiang, C.T., et al., 2005. Comparative studies on the hypolipidemic and growth suppressive effects of oolong, black, pu-erh, and green tea leaves in rats. J. Agric. Food Chem. 53, 480e489. Kurihara, H., Fukami, H., Koda, H., et al., 2002. Effects of oolong tea on metabolism of plasma fat in mice under restraint stress. Biosci. Biotechnol. Biochem. 66, 1955e1958. Kurihara, H., Fukami, H., Toyoda, Y., et al., 2003. Inhibitory effect of oolong tea on the oxidative state of low density lipoprotein (LDL). Biol. Pharm. Bull. 26, 739e742. Lin, J.K., Lin-Shiau, S.Y., 2006. Mechanisms of hypolipidemic and anti-obesity effects of tea and tea polyphenols. Mol. Nutr. Food Res. 50, 211e217. Liu, Y.-f., Huang, H.-h., 2010. Research on inhibition of extracts from oolong tea and puer tea on a-amylase from porcine pancreas. Food and Fermentation Industries 36. Loftus, T.M., Jaworsky, D.E., Frehywot, G.L., et al., 2000. Reduced food intake and body weight in mice treated with fatty acid synthase inhibitors. Science 288, 2379e2381. Lopez-Garcia, E., van Dam, R.M., Rajpathak, S., et al., 2006. Changes in caffeine intake and long-term weight change in men and women. Am. J. Clin. Nutr. 83, 674. Matsumoto, N., Ishigaki, F., Ishigaki, A., et al., 1993. Reduction of blood glucose levels by tea catechin. Biosci. Biotechnol. Biochem. 57 (4), 525e527.
518
Mo, B.-q., Li, Z., Zjao, Y., 2007. Weight-reducing effect of oolong tea extracts on rats. Modern Preventive Medicine 34. Monobe, M., Ema, K., Kato, F., Maeda-Yamamoto, M., 2008. Immunostimulating activity of a crude polysaccharide derived from green tea (Camellia sinensis) extract. J. Agric. Food Chem. 56, 1423e1427. Muroyama, K., Murosaki, S., Yamamoto, Y., et al., 2003. Anti-obesity effects of a mixture of thiamin, arginine, caffeine, and citric acid in non-insulin dependent diabetic KK mice. J. Nutr. Sci. Vitaminol. 49, 56e63. Nakai, M., Fukui, Y., Asami, S., et al., 2005a. Inhibitory effects of oolong tea polyphenols on pancreatic lipase in vitro. J. Agric. Food Chem. 53, 4593e4598. Nakai, M., Fukui, Y., Ono, Y., 2005b. Effect of oolong tea polypheerized polyphenols on mechanism of serum triglyceride elevation suppressive. J. Jpn. Soc. Study Obes. 11, 88e90. Redinger, R.N., 2009. Fat storage and the biology of energy expenditure. Transl. Res. 154, 52e60. Rumpler, W., Seale, J., Clevidence, B., et al., 2001. Oolong tea increases metabolic rate and fat oxidation in men. J. Nutr. 131, 2848e2852. Shimada, K., Kawarabayashi, T., Tanaka, A., et al., 2004. Oolong tea increases plasma adiponectin levels and lowdensity lipoprotein particle size in patients with coronary artery disease. Diabetes Res. Clin. Pract. 65, 227e234. Toyoda-Ono, Y., Yoshimura, M., Nakai, M., et al., 2007. Suppression of postprandial hypertriglyceridemia in rats and mice by oolong tea polymerized polyphenols. Biosci. Biotechnol. Biochem. 71, 971e976. van Dam, R.M., Willett, W.C., Manson, J.E., et al., 2006. Coffee, caffeine, and risk of type 2 diabetes e a prospective cohort study in younger and middle-aged US women. Diabetes Care 29, 398e403. Westerterp-Plantenga, M.S., Lejeune, M., Kovacs, E.M.R., 2005. Body weight loss and weight maintenance in relation to habitual caffeine intake and green tea supplementation. Obes. Res. 13, 1195e1204. Wolfram, S., 2007. Effects of green tea and EGCG on cardiovascular and metabolic health. J. Am. Coll. Nutr. 26, 373se388s. Wu, C.H., Lu, F.H., Chang, C.S., et al., 2003. Relationship among habitual tea consumption, percent body fat, and body fat distribution. Obes. Res. 11, 1088e1095. Yang, M.H., Wang, C.H., Chen, H.L., 2001. Green, oolong and black tea extracts modulate lipid metabolism in hyperlipidemia rats fed high-sucrose diet. J. Nutr. Biochem. 12, 14e20. Yeh, C.W., Chen, W.J., Chiang, C.T., et al., 2003. Suppression of fatty acid synthase in MCF-7 breast cancer cells by tea and tea polyphenols: a possible mechanism for their hypolipidemic effects. Pharmacogenomics J. 3, 267e276.
CHAPTER 42 Oolong Tea and Weight Loss
Zheng, G., Sayama, K., Okubo, T., et al., 2004. Anti-obesity effects of three major components of green tea, catechins, caffeine and theanine, in mice. In vivo 18, 55e62.
Further Reading Hirata, K., Dichek, H.L., Cioffi, J.A., et al., 1999. Cloning of a unique lipase from endothelial cells extends the lipase gene family. J. Biol. Chem. 274, 14170e14175. Kobayashi, M., Ichitani, M., Suzuki, Y., et al., 2009. Black-tea polyphenols suppress postprandial hypertriacylglycerolemia by suppressing lymphatic transport of dietary fat in rats. J. Agric. Food Chem. 57, 7131e7136. Mukhtar, H., Ahmad, N., 1999. Cancer chemoprevention: future holds in multiple agents. Toxicol. Appl. Pharmacol. 158, 207e210. Mukhtar, H., Ahmad, N., 2000. Tea polyphenols: prevention of cancer and optimizing health. Am. J. Clin. Nutr. 71, 1698Se1702S. Yang, C.S., Wang, Z.Y., 1993. Tea and cancer. J. Natl. Cancer Inst. 85, 1038e1049. Yang, T.T.C., Koo, M.W.L., 1997. Hypocholesterolemic effects of Chinese tea. Pharmacol. Res. 35, 505e512.
519
42
Oolong Tea and Weight Loss Rong-Rong He1, Hiroshi Kurihara1, Victor R. Preedy2 1 Institute of Traditional Chinese Medicine and Natural Products, Jinan University, Guangzhou, China 2 Diabetes and Nutritional Sciences Division, School of Medicine, Kings College London, London, UK
Abbreviations EC epicatechin ECG epicatechin gallate EE energy expenditure EGC epigallocatechin EGCG epigallocatechin gallate EGF epidermal growth factor EI energy intake FAS fatty acid synthase HDL high-density lipoprotein HDL-C high-density lipoprotein cholesterol HSL hormone-sensitive lipase LDL low-density lipoprotein LDL-C low-density lipoprotein cholesterol OTPP oolong tea-polymerized polyphenols TC total cholesterol TF-1 theaflavin TF-2a theaflavin 3-gallate TF-2b theaflavin 3’-gallate TF-3 theaflavin 3,3’-digallate TG triglyceride
INTRODUCTION Historically, teas have been widely used to prevent obesity and improve lipid metabolism. However, the evidence-basis of such practices has hitherto been lacking. Oolong tea, green tea and black tea, which are non-, partially- and fully-fermented/oxidized teas, respectively, are the most commonly consumed teas, though there are others, such as white tea, which are less popular. Oolong tea is particularly consumed in Asia. In fact, oolong tea has an ancient history dating back over 400 years, originating from the Fujian province of China during the Ming dynasty. Presently, oolong tea from Fujian is exported to the whole world. Oolong tea is made from the tea plant Camellia sinensis through a unique process which includes withering under the strong sun and oxidation before curling and twisting. Oolong tea is semi-oxidized, and thus its chemical composition is reported to be more complex than other teas. Tea in Health and Disease Prevention. DOI: 10.1016/B978-0-12-384937-3.00042-2 Copyright Ó 2013 Elsevier Inc. All rights reserved.
509
SECTION 5 General Protective Aspects of Tea-Related Compounds
Oolong tea is not only renowned for its unique taste, but also its putative health benefits. One of these is its effects on weight loss. In China oolong tea is traditionally considered to have anti-obesity and hypolipidemic effects. Indeed this is supported by experimental studies in the early 1990s which confirmed that consumption of oolong tea reduced body weight. Since then, other studies have reported that the consumption of oolong tea blocked lipid absorption or promoted fat oxidation. In this chapter we describe in detail the putative mechanisms through which oolong tea impacts body weight and obesity.
ANTI-OBESITY EFFECTS OF OOLONG TEA IN HUMAN STUDIES Two decades ago Chen et al., (1992) first reported that oolong tea consumption effectively lowered blood pressure, plasma triglyceride and cholesterols in humans. Thereafter, they performed another study on 102 females and found that 67% of subjects had a reduced body weight after consumption of 8 g dry oolong tea leaves daily for six consecutive weeks (Chen et al, 1998). Although the dose of oolong tea in this clinical study was larger than normal daily intakes, the weight-reducing effects of oolong tea were shown by scientists for the first time. These two reports from China initiated further studies on weight loss and antiobesity effects of oolong tea.
510
In the beginning of the 21st century, the anti-obesity effects of oolong tea attracted Japanese researchers and tea developers. Suntory Ltd. (Osaka, Japan), a Japanese company famous for its drinks and beverages, had developed oolong tea as a commercial drink and carried out many scientific studies on its health benefits. They conducted a randomized crossover study to measure the influence of oolong tea consumption on 24 hour energy expenditure in 12 male volunteers. They provided full- or half-strength oolong tea, and caffeinated (containing caffeine equivalent to full strength oolong tea) or non-caffeinated water and measured energy expenditure by calorimetry. The results showed that consuming full strength oolong tea increased energy expenditure (that is burned more calories per day) than caffeinated water (Rumpler et al., 2001). The 24 hour resting energy expenditure increased from 7,032 kJ/d (water group) to 7,158, 7,320 and 7,227 kJ/day for the caffeinated water, half-strength and full-strength oolong tea groups, respectively. Suntory also conducted another study on females. This study involved 11 female participants consuming infusions of oolong tea (Komatsu et al., 2003). The results showed that oolong tea increased energy expenditure significantly, peaking at 90 minutes and the effect persisted for 120 minutes (Komatsu et al., 2003). Thus, the subject’s mean resting energy expenditure increased from approx 210 kJ/h to 240 kJ/h (Komatsu et al., 2003). Although this is a relatively moderate increase, consideration needs to be given to the implications of such increases over the long term or on a more frequent episodic basis. Additionally, Suntory researchers also conducted a double-blind placebo-controlled crossover experiment. Subjects were given a high-lipid diet containing 38 g/day of lipid, and a total of 750 ml of placebo or polyphenol-enriched oolong tea infusions, at three meals per day for a month. Feces were collected to measure the excretion of lipids. The study found that lipid excretion into feces was significantly higher in those consuming polyphenol-enriched oolong tea compared to those in the placebo group. Thus fecal lipid excretion increased from a mean of 9.4 (placebo group) to 19.3 g/3 day (polyphenol-enriched oolong tea group, P < 0.01; Hsu et al., 2006). In the same study, cholesterol excretion increased from 1.2 to 1.8 g/3 day (P ¼ 0.056) for the placebo and polyphenol-enriched oolong tea groups, respectively (Hsu et al., 2006). An epidemiological study of 1,103 Taiwanese adults found that habitual tea drinkers (defined as those who drank tea at least once per week for 6 months) who consumed tea for more than 10 years had a lower percentage of body fat (decrease by 19.6%) and waist to hip ratio (decrease by 2.1%) when compared to non-habitual consumers. This survey suggests
CHAPTER 42 Oolong Tea and Weight Loss
that consuming oolong tea may be beneficial in terms of anti-obesity therapies (Wu et al., 2003). Alternatively, there may be lifestyle factors that distinguish tea drinkers from non tea drinkers, and these factors themselves may contribute to the measured differences in body fat and waist to hip ratio. However, the latter supposition is not supported by the aforementioned studies by Chen et al., (1998), Rumpler et al., (2001), Komatsu et al., (2003) or Hsu et al., (2006) which clearly showed a direct beneficial effect of oolong tea on energy expenditure and lipid excretion. Other researchers also found that an intake of oolong tea significantly influenced, in a beneficial way, plasma adiponectin levels, low-density lipoprotein (LDL) particle size, total cholesterol (TC), high-density lipoprotein cholesterol (HDL-C), low-density lipoprotein cholesterol (LDL-C), serum triglyceride (TG) and plasma glucose levels in patients with coronary artery disease (Shimada et al., 2004). Stress-induced LDL oxidation was also prevented by the consumption of oolong tea in women (Kurihara et al., 2003). More recently, a large clinical trial was conducted to verify the anti-obesity effects of oolong tea. In a total of 102 obese subjects tested, 70% of severely obese subjects had lost more than 1 kg and 22% of them lost 3 kg or more of body weight after oolong tea consumption for 6 weeks. Similarly, 66% of overweight subjects lost more than 1 kg after oolong tea consumption. Subcutaneous fat content was decreased and waist circumference was reduced in 12% of the subjects. Moreover, it was observed that plasma TG levels of human with hypertriglyceridemia decreased by about 20%. The plasma TC levels in the subjects with hypercholesterodemia were also significantly decreased (He et al., 2009). All these research findings suggest that oolong tea is useful in treating obesity or hyperlipidemia in the clinical setting.
ANTI-OBESITY EFFECTS OF OOLONG TEA IN LABORATORY STUDIES The preceding sections clearly show that oolong tea has anti-obesity effects, from the evidence of a variety of clinical studies. Quite a number of pre-clinical studies have also been performed on the anti-obesity effects of oolong tea. For example, high-fat or high-sucrose diet-induced obesity models were used to evaluate the efficacy of oolong tea on the inhibition of fat accumulation in animals. Scientists in Ehime University (Ehime, Japan) found feeding a high-fat diet containing 40% beef tallow to mice for 10 weeks produced significant increases in body weight and parametrial (i.e. within the vicinity of the uterus) white adipose tissue weight compared to those fed laboratory chow. However, feeding high-fat diets containing 5% oolong tea powder reduced body weights by 10% and parametrical adipose tissue weight by 51% within 10 weeks (Han et al., 1999). Yang et al. (2001) also found that body weight gain was significantly reduced (by 35%) in rats fed with a high-sucrose diet and concomitantly provided with oolong tea extracts. In this study by Yang et al. (2001) the food efficiency (g body weight gain per Kcal) was reduced by 27%. Another study demonstrated that oolong tea lowered the fat/body ratio in rats fed with a high-energy diet (Mo et al., 2007). The studies above also showed that oolong tea effectively alleviated hyperlipidemia and hypertriglyceridemia. However, they were all based on models which used high-fat or highsucrose diets. In order to elaborate on the anti-obesity effects of oolong tea in animals fed normal diets, Kuo et al. (2005) evaluated the weight-suppressive effects of orally feeding oolong tea leaves to male Sprague-Dawley rats for 30 weeks. Compared with the control group, the relative weight ratios of liver to epididymal adipose tissue were decreased significantly by oolong tea consumption. Apart from observing the apparent effects on loss of body weight, measurement of relevant lipid metabolism indicators reveal that oolong tea has significant hypolipidemic effects.
511
SECTION 5 General Protective Aspects of Tea-Related Compounds
A correlation between obesity and hyperlipidemia has been previously confirmed in numerous studies. This is important to consider as excessive plasma TG and TC in obese subjects has the potential to cause cardiovascular diseases. Therefore, it is advisable to keep plasma TG and TC at normal levels to prevent diseases such as arteriosclerosis, cerebral apoplexy and myocardial infarction. In this regard, many studies have been conducted to clarify the effects of oolong tea on the reduction of circulating TG and TC levels in rats fed with high-fat or highsucrose diets. Thus, the levels of high density lipoproteins (HDL; known as ‘good lipoproteins’) are increased, and atherogenic indices reduced by oolong tea (Han et al., 1999; Yang et al., 2001). In addition, the HDL-C level are increased, and the LDL-C (known as ‘bad cholesterol’) level is decreased in rats treated with oolong tea (Han et al., 1999; Yang et al., 2001). Oolong tea also has protective effects in ameliorating metabolic abnormalities in plasma lipid profiles in mice subjected to restraint stress. When a lipid emulsion was injected intravenously into mice, restraint stress prolonged the half-life of TG elimination (Kurihara et al., 2002). Therefore, TG metabolism was disrupted by stress, and the use of TG as an energy source was decreased. The intake of oolong tea alleviated the stress-induced changes in lipid metabolism. This effect may have arisen from some non-specific stress-relieving property of oolong tea or acceleration of lipid metabolism by its bioactive components (Kurihara et al., 2002). Accordingly, one can surmise that oolong tea exerts its therapeutic potential by alleviating hyperlipidemia and hypertriglyceridemia.
ACTIVE COMPONENTS OF OOLONG TEA IN OBESITY REDUCTION
512
Polyphenols, alkaloids, saponins, polysaccharides and L-theanines are the main components that contribute to oolong tea’s putative medicinal properties (Jia et al., 2005; Khan and Mukhtar, 2007; Bukowski and Percival, 2008; Monobe et al., 2008). Caffeine and polyphenols are arguably the most important bioactive components in regards to the antiobesogenic properties of oolong tea. Caffeine, which is present at levels of up to 5e6% in tea, plays a key role because of its thermogenic and fat oxidizing properties. Several studies have shown that the polyphenols present in oolong tea reduce the risk of several diseases by virtue of their anti-fungal, anti-inflammation, anti-mutagenic, anti-oxidative effects. This is in addition to the ability of oolong tea to lower plasma TC and TG levels, and reduce blood pressure and platelet aggregation. Catechins, including epigallocatechin gallate (EGCG), epigallocatechin (EGC), epicatechin gallate (ECG) and epicatechin (EC), are the most biologically active group of polyphenols in oolong tea. EGCG accounts for 50e80% of the total catechins in oolong tea. Other polyphenols, such as flavan-3-ols, proanthocyanidins, theasinensins, and a few hydrolyzable tannins also inhibit pancreatic lipase activity. In addition, tea saponins were reported to inhibit pancreatic lipase activity in vitro (Han et al., 1999). However, this aforementioned observation needs to be interpreted with care because it did not consider the interference of tea catechins on pancreatic lipase (Han et al., 1999). Oolong tea polymerized polyphenols (OTPP) are derived from tea catechins by polyphenol oxidases and produced during the semi-fermentation and heating process of production. The fermentation of polyphenols in oolong tea ranges from 8% to 85%, depending on the variety and production style of the tea. Thearubigins and theaflavins are the representative and most abundant OTPPs in oolong tea (as shown in Figure 42.1). OTPPs are not found in green tea, and they are different from those in fully-fermented, black tea. OTPPs have inhibitory activities in vitro against some metabolic enzymes, such as glycosyltransferase and lipase. In animal studies, OTPP significantly suppresses both lymphatic and serum TG absorption when subjects are given high-fat diets (Nakai et al., 2005b). In human studies, OTPPs suppress postprandial serum TG and chylomicron in subjects fed with a high-lipid diet (Hara et al., 2004). Accordingly, these studies suggest that OTPPs are especially important components in oolong tea (Toyoda-Ono et al., 2007).
CHAPTER 42 Oolong Tea and Weight Loss
513 FIGURE 42.1 Structures of Catechins and Oolong Tea-Polymerized Polyphenols
ANTI-OBESITY MECHANISMS OF OOLONG TEA Excessive adiposity results from a disorder of energy homeostasis, which is the consequence of excessive energy intake that is not balanced by expenditure (Redinger, 2009). Either increasing energy expenditure (EE) or decreasing energy intake (EI) can achieve the goal of losing weight. So far, evidence suggests that the major mechanisms responsible for the anti-obesity effects of oolong tea include reducing energy intake, stimulating energy expenditure, suppressing lipogenesis and promoting lipolysis in adipose tissue. The preceding discussion raises the question of how oolong tea can assist in the prevention and/or the treatment of obesity. Firstly, oolong tea could decrease energy intake by inhibiting glucose or fat absorption. It was found that polyphenols, such as catechins, in oolong tea could inhibit the activities of some digestive enzymes like a-glucosidase and invertase to reduce absorption of glucose and sucrose (Matsumoto et al., 1993). Based on these findings, Liu and Huang (2010) found that oolong tea induced a reversible inhibition of a-amylase activity and blocked the degradation of carbohydrates, lowered blood glucose level and subsequently prevented the transformation of glucose into fats in adipose tissue. However, the decrease in energy intake by oolong tea is not uniquely dependent on the reduction of carbohydrate absorption. Other studies have shown that oolong tea suppresses the intestinal absorption of dietary fat by inhibiting pancreatic lipase (Han et al., 1999). The digestion of dietary fat is facilitated by pancreatic lipase, hence its inhibition could significantly decrease lipid absorption and increase lipid excretion into the feces. As shown in Table 42.1, the polyphenols
SECTION 5 General Protective Aspects of Tea-Related Compounds
TABLE 42.1 Inhibition of Pancreatic Lipase by Oolong Tea Extract and Catechins In vitro Polyphenols
IC50 (mM )
()-epigallocatechin 3,5-di-O-gallate Prodelphinidin B-2 3,3’-di-O-gallate Assamicain A Oolonghomobisflavan A Oolonghomobisflavan B Oolongtheanin 3’-O-gallate Theafavin Theafavin 3,3’-O-gallate
0.098 0.107 0.120 0.048 0.108 0.068 0.106 0.092
(Nakai et al, 2005a; Birari and Bhutani, 2007)
514
commonly found in oolong tea show potent inhibitory activities (IC50) on pancreatic lipase in vitro (Birari and Bhutani, 2007). Another piece of research also showed that oolong tea extract and catechins inhibit pancreatic lipase activity, and in this study ECG and EGCG were more potent than oolong tea extract (He et al., 2009). Other studies have shown lipid absorption was inhibited, since lipid excretion into the feces was significantly higher in humans consuming oolong tea. Cholesterol excretion also tended to increase when subjects were fed a high-lipid diet (Hsu et al., 2006). Based on the analysis of the structureeactivity relationship of these polyphenols, galloyl-ester moieties were found to be very important for inhibiting pancreatic lipase activities. This is supported by the observation that the inhibitory activity of these polyphenols is significantly decreased when the galloyl-ester moieties of the polyphenols are eliminated with tannin acyl hydrolase (Hsu et al., 2006). Furthermore, the inhibitory activity of OTPP on pancreatic lipase is stronger than that of total oolong tea extracts in vitro. These studies suggest that functional galloyl moieties and the polymerization of catechins are required for pancreatic lipase inhibition (Nakai et al., 2005a). Apart from inhibiting intestinal absorption, appetite suppression is another important way to limit energy intake. Many studies have confirmed the suppression of appetite by caffeine in rodents and humans. Kovacs et al. (2004) found lower leptin concentrations in habitual caffeine-beverage drinkers. Studies by Westerterp-Plantenga et al. (2005) also indicated that higher satiety was found in humans having habitual caffeine or tea consumption. The inhibitory effect of caffeine on appetite is related to a corticotropin-releasing factor and the sympathoadrenal system. Conceivably, the long-term consumption of oolong tea e which contains caffeine or other active compounds e may promote weight loss by suppressing appetite. In addition, theanines in oolong tea may also contribute to the regulation of appetite. It was reported that theanine could pass through the bloodebrain barrier and subsequently increase the release of dopamine or reduce serotonin concentrations in the brain. The importance of this relates to the fact that dopamine and serotonin are important neurotransmitters regulating appetite (Zheng et al., 2004). All the above indicate that appetite suppression by caffeine or theanines may be partly responsible for the anti-obesity effects of oolong tea. After controlling energy intake, it is also important to increase energy expenditure. Oolong tea is a semi-fermented tea containing more caffeine than green tea (Kao et al., 2006). It has been known for many years that caffeine can stimulate energy expenditure to varying degrees, and the use of caffeine alone or in combination with ephedrine has been proposed for the treatment of obesity (Dulloo et al., 1986, 1987; Astrup et al., 1991). Animal studies and prospective epidemiologic studies on weight loss suggest that long-term caffeine consumption decreases body weight (Cheung et al., 1988; Muroyama et al., 2003; Zheng et al., 2004; Lopez-Garcia et al., 2006; van Dam et al., 2006). These studies prove that caffeine increases energy expenditure both in animals and humans. The notion that caffeine is solely responsible for the increase in energy expenditure is controversial, however, since there are a number of complex constituents in
CHAPTER 42 Oolong Tea and Weight Loss
oolong tea. Some reports have claimed that oolong tea promotes the preferential use of fat as an energy source and achieves its anti-obesity effects through compounds other than caffeine (Rumpler et al., 2001). Subsequently, Komatsu’s studies (Kamatsu et al., 2003) confirmed that oolong tea increases energy expenditure not only via caffeine or EGCG but also by some types of polymerized polyphenol. Therefore, more research needs to be done to understand which components account for the increased energy expenditure in tea drinking. Inhibiting lipogenesis is another important factor in weight loss. Lipogenesis is the synthesis of esterified fatty acids, which produces TG from carbohydrates or other energy sources acquired in the diet. Fatty acid synthase (FAS) is an important enzyme involved in lipogenesis. It was reported that FAS might be a potential therapeutic target for the treatment of obesity (Loftus et al., 2000), and EGCG and ECG were found to be potent inhibitors of FAS. FAS expression was suppressed by EGCG, as studied in vitro, but not by catechin, EC or EGC. Furthermore, theaflavin (TF-1), theaflavin 3-gallate (TF-2a), theaflavin 3’-gallate (TF-2b) and theaflavin 3,3’-digallate (TF-3) also significantly suppressed FAS expression at both protein and mRNA levels (Loftus et al., 2000). These changes may lead to the inhibition of cell lipogenesis. Additional experimental results demonstrated that epidermal growth factor (EGF)-induced biosynthesis of lipids including TG, cholesterol and FA, and cell proliferation were significantly suppressed by EGCG and TF-3 (Yeh et al., 2003). These findings suggest that tea polyphenols suppressed FAS expression by down-regulating EGF receptor/PI3K/Akt/ Sp-1 signal transduction pathways (Lin and Lin-Shiau, 2006). Oolong tea could also exert anti-obesity effects by promoting lipolysis in adipocytes. Some evidence from high-fat-diet-treated mice indicated that caffeine isolated from oolong tea enhanced noradrenalin-induced lipolysis. As a non-specific antagonist of adenosine receptors, caffeine modifies energy metabolism through increasing intracellular free Ca2þ concentration and promoting catecholamine release from noradrenergic nerve terminals. Caffeine elevates metabolic rate and fatty acid availability by lipolysis. Meanwhile, caffeine also increases lipolysis by inhibiting the cyclic nucleotide phosphodiesterase, which is responsible for catalyzing the conversion of cyclic AMP to AMP. The resulting high tissue concentrations of cyclic AMP activate inactive hormone-sensitive lipase (HSL) to promote lipolysis. Finally, oolong tea could exert anti-obesity effects by modulating the proliferation and differentiation of adipocytes. Because adipocyte tissue growth can be due to both hyperplasia and hypertrophy, the screening of anti-obesity materials has focused on the processes of adipocyte proliferation and differentiation. Catechins and EGCG were proven to reduce the total TG accumulation in murine 3T3-L1 preadipocytes during their differentiation into adipocytes induced by dexamethasone, 1-methyl-3-isobutylxanthine and insulin (Hasegawa et al., 2003). EGCG and ECG inhibited acetyl-CoA carboxylase activity, a rate-limiting step in the fatty acid biosynthesis pathway, in 3T3-L1 cells. Therefore, the in vitro effect of EGCG on fat tissues may be mediated by the modulation of hormone-stimulated cell proliferation and differentiation or by the inhibition of lipogenesis or promotion of lipolysis (Hasegawa and Mori, 2000). To summarize, the above studies on the mechanisms of weight loss by oolong tea suggest that complex, multifaceted pathways are involved. However, the concomitant imposition of diet and other lifestyle factors on the cause, progression and regression of obesity and also genetic diversity all need to be considered in the development of obesity. For example, it has been proposed that the effects of catechins on energy expenditure may vary depending on genetic variability in COMT enzyme activity (Hursel et al., 2009).
COMPARISON OF THE ANTI-OBESITY EFFECTS OF OOLONG TEA AND GREEN TEA Oolong tea and green tea are produced from the same plant species (Camellia sinensis), but are distinguished by their processing techniques. For green tea production, the leaves are
515
SECTION 5 General Protective Aspects of Tea-Related Compounds
TABLE 42.2 Contents of Polyphenol and Caffeine in Oolong Tea and Green Tea Extracts Components Caffeine
Oolong Tea (mg/g)
Green Tea (mg/g)
64
53
30 6 10 2
43 25 5 8
14 16 3 7 114
29 19 6 5 e
Flavan-3-ols without galloyl moeity Gallocatechin Epigallocatechin Catechin Epicatechin Flavan-3-ols with galloyl moiety Epigallocatechin gallate Gallocatechin gallate Epigallocatechin gallate Catechin gallate Oolong tea polymerized polyphenols (OTPP) (Toyoda-Ono et al., 2007)
516
steamed soon after harvest to stop enzyme reactions. The leaves are then ground by hand to break the cells. For oolong tea production, the leaves are fermented under defined conditions to produce specific flavors by enzyme reactions. The leaves of oolong tea are not ground e the cells are kept intact. These processing differences mean that the components of oolong tea and green tea are quiet different (as shown in Table 42.2). The concentration of catechins in oolong tea is approximately half of that of green tea, while polymerized polyphenols seem to be absent in green tea but have significant concentrations in oolong tea. Although the polyphenol contents of oolong tea and green tea are markedly different, various studies have shown that green tea is also effective in weight loss, and the effects of the two have been compared in several studies. Ikeda et al. (1992) indicated that both tea catechins and heat-treated catechins suppress postprandial hypertriacylglycerolemia to almost the same extent in rats. They also showed that that such tea catechins inhibited the activity of pancreatic lipase in vitro in a dose-dependent manner (Ikeda et al., 1992). However, Yang reported that green tea exerted greater antihyperlipidemic effects than oolong tea (Yang et al., 2001). In contrast, Komatsu et al. (2003), from the Tokushima School of Medicine in Japan, claimed that oolong tea confers greater health benefits than green tea. For example, they found that the cumulative increases in energy expenditure after the consumption of oolong tea and green tea for 120 min were significantly increased by 10% and 4%, respectively (Komatsu et al., 2003). Studies also indicated that oolong tea shows a stronger ability to lower serum TG levels than non-fermented green tea. Oolong tea as well as non-fermented green tea, fully fermented pu-erh tea, and black tea all reduce serum level of total cholesterol, but partially fermented oolong tea leaves are strongest (Kuo et al., 2005). However, Wolfram (2007) reviewed the anti-obesity effects of green tea and suggested that the study of Komatsu may not be accurate because it lasted for only one session, and involved just 11 young females. Thus the results of the comparisons of anti-obesity effects of oolong tea with other types of tea are controversial and merit investigation.
CONCLUSION Tea has been used historically and currently as a popular beverage in both Oriental and Western countries. Evidence based on modern molecular and cellular studies support the
CHAPTER 42 Oolong Tea and Weight Loss
notion that consumption of green, oolong and black tea appears to modulate body weight and have a putative role in preventing obesity. Different animal and human experiments have attempted to elucidate the precise mechanisms through which this occurs. However, some results seem fragmentary and there is some inconsistency. Nevertheless, the weight-loss inducing properties of oolong tea can be categorized into several mechanisms. The active components of oolong tea which improve lipid metabolism appear to be caffeine and the polyphenols. Oolong tea appears to act as an anti-obesogenic agent and in weight control through its suppression of pancreatic lipase, thus impeding the absorption of lipids in the intestines. At the same time, oolong tea also increases energy expenditure by inducing thermogenesis and lipolysis. It also suppresses appetite. The present understanding of the anti-obesogenic effects of oolong tea might be superficial. However, these findings could lead to great discoveries in the future including the usage of oolong tea in treating diabetes. In summary, oolong tea is significantly hypolipidemic and anti-obesogenic.
SUMMARY POINTS l
l
l
l
In China, oolong tea has traditionally been considered to have anti-obesity and hypolipidemic effects. Since the early 1990s, many studies in both rodents and humans have verified the traditional notion that oolong tea is effective in obesity control and hyperlipidemia. The anti-obesity effects of oolong tea are due to the inhibition of energy intake and the promotion of energy utilization. These effects are due to its bioactive components, including caffeine, catechins and polymerized polyphenols.
References Astrup, A., Toubro, S., Cannon, S., et al., 1991. Thermogenic synergism between ephedrine and caffeine in healthy volunteers: a double-blind, placebo-controlled study. Metabolism 40, 323e329. Birari, R.B., Bhutani, K.K., 2007. Pancreatic lipase inhibitors from natural sources: unexplored potential. Drug Discov. Today 12, 879e889. Bukowski, J.F., Percival, S.S., 2008. L-theanine intervention enhances human gamma delta T lymphocyte function. Nutr. Rev. 66, 96e102. Chen, W., Yang, Z., Hosoda, K., et al., 1998. Clinical efficacy of oolong tea on anti-simple obesity. Nippon Rinsho Eiyo Gakkai Zasshi 20, 83e90. Chen, W.Y., Zheng, Q.Z., Ni, F., et al., 1992. Clinical observation of anti-hypertensive & hypolipidemic effects of fujian oolong tea. Journal of Fujian College of Traditional Chinese Medicine 2. Cheung, W.T., Lee, C.M., Ng, T.B., 1988. Potentiation of the anti-lipolytic effect of 2-chloroadenosine after chronic caffeine treatment. Pharmacology 36, 331e339. Dulloo, A.G., Miller, D.S., 1986. The thermogenic properties of ephedrine/methylxanthine mixtures: human studies. Int. J. Obes. 10, 467e481. Dulloo, A.G., Miller, D.S., 1987. Aspirin as a promoter of ephedrine-induced thermogenesis: potential use in the treatment of obesity. Am. J. Clin. Nutr. 45, 564e569. Flatt, J.P., 2007. Differences in basal energy expenditure and obesity. Obesity 15, 2546e2548. Han, L.K., Takaku, T., Li, J., et al., 1999. Anti-obesity action of oolong tea. Int. J. Obes. 23, 98e105. Hara, Y., Moriguchi, S., Kusumoto, A., et al., 2004. Suppressive effect of oolong tea polymerized polyphenolsenriched oolong tea on postprandial serum triglyceride elevation. Jpn. Pharmacol. Ther. 32, 335e342. Hasegawa, N., Mori, M., 2000. Effect of powdered green tea and its caffeine content on lipogenesis and lipolysis in 3T3-L1 cell. J. Health Sci. 46, 153e155. Hasegawa, N., Yamda, N., Mori, M., 2003. Powdered green tea has antilipogenic effect on zucker rats fed a high-fat diet. Phytother. Res. 17, 477e480. He, R.R., Chen, L., Lin, B.H., et al., 2009. Beneficial effects of oolong tea consumption on diet-induced overweight and obese subjects. Chin. J. Integr. Med. 15, 34e41. Hsu, T.F., Kusumoto, A., Abe, K., et al., 2006. Polyphenol-enriched oolong tea increases fecal lipid excretion. Eur. J. Clin. Nutr. 60, 1330e1336.
517
SECTION 5 General Protective Aspects of Tea-Related Compounds
Hursel, R., Viechtbauer, W., Westerterp-Plantenga, M.S., 2009. The effects of green tea on weight loss and weight maintenance: a meta-analysis. Int. J. Obes. 33, 956e961. Ikeda, I., Imasato, Y., Sasaki, E., et al., 1992. Tea catechins decrease micellar solubility and intestinal absorption of cholesterol in rats. Biochim. Biophys. Acta. 1127, 141e146. Jia, X.-D., Han, C., Chen, J.-S., 2005. Tea pigments induce cell-cycle arrest and apoptosis in HepG2 cells. World J. Gastroenterol. 11, 5273e5276. Kao, Y.H., Chang, H.H., Lee, M.J., Chen, C.L., 2006. Tea, obesity, and diabetes. Mol. Nutr. Food Res. 50, 188e210. Khan, N., Mukhtar, H., 2007. Tea polyphenols for health promotion. Life Sci. 81, 519e533. Komatsu, T., Nakamori, M., Komatsu, K., et al., 2003. Oolong tea increases energy metabolism in Japanese females. J. Med. Invest. 50, 170e175. Kovacs, E.M.R., Lejeune, M., Nijs, I., Westerterp-Plantenga, M.S., 2004. Effects of green tea on weight maintenance after body-weight loss. Br. J. Nutr. 91, 431e437. Kuo, K.L., Weng, M.S., Chiang, C.T., et al., 2005. Comparative studies on the hypolipidemic and growth suppressive effects of oolong, black, pu-erh, and green tea leaves in rats. J. Agric. Food Chem. 53, 480e489. Kurihara, H., Fukami, H., Koda, H., et al., 2002. Effects of oolong tea on metabolism of plasma fat in mice under restraint stress. Biosci. Biotechnol. Biochem. 66, 1955e1958. Kurihara, H., Fukami, H., Toyoda, Y., et al., 2003. Inhibitory effect of oolong tea on the oxidative state of low density lipoprotein (LDL). Biol. Pharm. Bull. 26, 739e742. Lin, J.K., Lin-Shiau, S.Y., 2006. Mechanisms of hypolipidemic and anti-obesity effects of tea and tea polyphenols. Mol. Nutr. Food Res. 50, 211e217. Liu, Y.-f., Huang, H.-h., 2010. Research on inhibition of extracts from oolong tea and puer tea on a-amylase from porcine pancreas. Food and Fermentation Industries 36. Loftus, T.M., Jaworsky, D.E., Frehywot, G.L., et al., 2000. Reduced food intake and body weight in mice treated with fatty acid synthase inhibitors. Science 288, 2379e2381. Lopez-Garcia, E., van Dam, R.M., Rajpathak, S., et al., 2006. Changes in caffeine intake and long-term weight change in men and women. Am. J. Clin. Nutr. 83, 674. Matsumoto, N., Ishigaki, F., Ishigaki, A., et al., 1993. Reduction of blood glucose levels by tea catechin. Biosci. Biotechnol. Biochem. 57 (4), 525e527.
518
Mo, B.-q., Li, Z., Zjao, Y., 2007. Weight-reducing effect of oolong tea extracts on rats. Modern Preventive Medicine 34. Monobe, M., Ema, K., Kato, F., Maeda-Yamamoto, M., 2008. Immunostimulating activity of a crude polysaccharide derived from green tea (Camellia sinensis) extract. J. Agric. Food Chem. 56, 1423e1427. Muroyama, K., Murosaki, S., Yamamoto, Y., et al., 2003. Anti-obesity effects of a mixture of thiamin, arginine, caffeine, and citric acid in non-insulin dependent diabetic KK mice. J. Nutr. Sci. Vitaminol. 49, 56e63. Nakai, M., Fukui, Y., Asami, S., et al., 2005a. Inhibitory effects of oolong tea polyphenols on pancreatic lipase in vitro. J. Agric. Food Chem. 53, 4593e4598. Nakai, M., Fukui, Y., Ono, Y., 2005b. Effect of oolong tea polypheerized polyphenols on mechanism of serum triglyceride elevation suppressive. J. Jpn. Soc. Study Obes. 11, 88e90. Redinger, R.N., 2009. Fat storage and the biology of energy expenditure. Transl. Res. 154, 52e60. Rumpler, W., Seale, J., Clevidence, B., et al., 2001. Oolong tea increases metabolic rate and fat oxidation in men. J. Nutr. 131, 2848e2852. Shimada, K., Kawarabayashi, T., Tanaka, A., et al., 2004. Oolong tea increases plasma adiponectin levels and lowdensity lipoprotein particle size in patients with coronary artery disease. Diabetes Res. Clin. Pract. 65, 227e234. Toyoda-Ono, Y., Yoshimura, M., Nakai, M., et al., 2007. Suppression of postprandial hypertriglyceridemia in rats and mice by oolong tea polymerized polyphenols. Biosci. Biotechnol. Biochem. 71, 971e976. van Dam, R.M., Willett, W.C., Manson, J.E., et al., 2006. Coffee, caffeine, and risk of type 2 diabetes e a prospective cohort study in younger and middle-aged US women. Diabetes Care 29, 398e403. Westerterp-Plantenga, M.S., Lejeune, M., Kovacs, E.M.R., 2005. Body weight loss and weight maintenance in relation to habitual caffeine intake and green tea supplementation. Obes. Res. 13, 1195e1204. Wolfram, S., 2007. Effects of green tea and EGCG on cardiovascular and metabolic health. J. Am. Coll. Nutr. 26, 373se388s. Wu, C.H., Lu, F.H., Chang, C.S., et al., 2003. Relationship among habitual tea consumption, percent body fat, and body fat distribution. Obes. Res. 11, 1088e1095. Yang, M.H., Wang, C.H., Chen, H.L., 2001. Green, oolong and black tea extracts modulate lipid metabolism in hyperlipidemia rats fed high-sucrose diet. J. Nutr. Biochem. 12, 14e20. Yeh, C.W., Chen, W.J., Chiang, C.T., et al., 2003. Suppression of fatty acid synthase in MCF-7 breast cancer cells by tea and tea polyphenols: a possible mechanism for their hypolipidemic effects. Pharmacogenomics J. 3, 267e276.
CHAPTER 42 Oolong Tea and Weight Loss
Zheng, G., Sayama, K., Okubo, T., et al., 2004. Anti-obesity effects of three major components of green tea, catechins, caffeine and theanine, in mice. In vivo 18, 55e62.
Further Reading Hirata, K., Dichek, H.L., Cioffi, J.A., et al., 1999. Cloning of a unique lipase from endothelial cells extends the lipase gene family. J. Biol. Chem. 274, 14170e14175. Kobayashi, M., Ichitani, M., Suzuki, Y., et al., 2009. Black-tea polyphenols suppress postprandial hypertriacylglycerolemia by suppressing lymphatic transport of dietary fat in rats. J. Agric. Food Chem. 57, 7131e7136. Mukhtar, H., Ahmad, N., 1999. Cancer chemoprevention: future holds in multiple agents. Toxicol. Appl. Pharmacol. 158, 207e210. Mukhtar, H., Ahmad, N., 2000. Tea polyphenols: prevention of cancer and optimizing health. Am. J. Clin. Nutr. 71, 1698Se1702S. Yang, C.S., Wang, Z.Y., 1993. Tea and cancer. J. Natl. Cancer Inst. 85, 1038e1049. Yang, T.T.C., Koo, M.W.L., 1997. Hypocholesterolemic effects of Chinese tea. Pharmacol. Res. 35, 505e512.
519