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An extract of black, green, and mulberry teas causes malabsorptionof carbohydrate but not of triacylglycerol in healthy volunteers1–3 Litao Zhong, Julie K Furne, and Michael D Levitt ABSTRACT
in green tea are dimerized to form a variety of theaflavins (1); Background: In vitro studies suggest that extracts of black, green,
thus, these teas may have different biological activities.
and mulberry teas could interfere with carbohydrate and triacylglyc- A putative beneficial effect of tea is its ability to induce weight erol absorption via their ability to inhibit ␣-amylase, ␣-glucosidase, loss. Support for this contention includes a controlled human trial sodium-glucose transporters, and pancreatic lipase.
that showed weight loss when tea was added to a dietary regimen Objective: We measured breath hydrogen and 13CO to investigate
(2) and a mouse study that showed that administration of a tea the ability of an extract of black, green, and mulberry tea leaves to extract with a high-fat diet eliminated the weight gain observed induce malabsorption of carbohydrate and triacylglycerol in healthy in the absence of tea (3). Several mechanisms have been postu- lated to account for this weight control. Modest increases in Design: In a crossover design, healthy adult volunteers randomly
energy expenditure have been reported with the ingestion of ingested test meals with a placebo beverage or a preparation con- oolong and green teas (4 – 6). In addition, tea could inhibit the taining an extract of black (0.1 g), green (0.1 g), and mulberry (1.0 absorption of carbohydrate or fat. In vitro experiments have g) teas. One test meal contained 50 g carbohydrate as white rice, 10 g shown that constituents of tea inhibit the activities of ␣-amylase butter, and 0.2 g [13C]triolein, and the beverages contained 10 g (7–10) and ␣-glucosidase (11–16) and of intestinal sodium- sucrose. The calorie content of the second test meal consisted en- dependent glucose transporters (17–21). The in vitro inhibition tirely of lipid (30 g olive oil and 0.2 g [13C]triolein). Breath- of pancreatic lipase (22–24) by tea extracts suggests that tea hydrogen and 13CO concentrations were assessed hourly for 8 h, might interfere with triacylglycerol absorption. However, no in and symptoms were rated on a linear scale.
vivo studies in humans or animals have shown that tea prepara- Results: With the carbohydrate-containing meal, the tea extract
tions cause malabsorption of carbohydrate or fat. In the present resulted in a highly significant increase in breath-hydrogen concen- report, we measured breath hydrogen and 13CO to investigate trations, which indicated appreciable carbohydrate malabsorption.
the ability of an extract of black, green, and mulberry tea leaves A comparison of hydrogen excretion after the carbohydrate- to induce malabsorption of carbohydrate and triacylglycerol in containing meal with that after the nonabsorbable disaccharide lac- tulose suggested that the tea extract induced malabsorption of 25%of the carbohydrate. The tea extract did not cause triacylglycerolmalabsorption or any significant increase in symptoms.
SUBJECTS AND METHODS
Conclusion: This study provides the basis for additional experi-
The study was approved by the Human Studies Subcommittee ments to determine whether the tea extract has clinical utility for the of the Minneapolis Veterans Affairs Medical Center, and in- formed consent was obtained from all subjects.
Study A: carbohydrate- and lipid-containing test meal
KEY WORDS
Malabsorption, carbohydrate, triacylglycerol, Twenty healthy volunteers (10 women and 10 men) aged tea extract, breath-hydrogen test, 13CO -breath test 23– 60 y fasted after their usual dinner until the following morn-ing (Ȃ0800), when the experiments were performed at the Min-neapolis Veterans Affairs Medical Center. After collection of INTRODUCTION
baseline breath samples for hydrogen and 13CO analysis, the It is widely believed that teas contain substances that are ben- subjects ingested a test meal consisting of white rice and butter.
eficial to health. (A search of the key words “tea health benefits”brings up Œ5 million entries on Google.) Although most of the 1 From NatureGen Inc, San Diego, CA (LZ), and VAMC (Research Ser- alleged benefits of tea are not supported by solid scientific evi- vice/151), Minneapolis, MN (JKF and MDL).
dence, teas contain a variety of biologically active compounds Supported by NatureGen, Inc, San Diego, CA, and VAMC (Research that might influence metabolic reactions. Most of the commonly 3 Reprints not available. Address correspondence to MD Levitt, VAMC ingested teas are derived from the leaf of the Camellia sinensis (Research Service/151), 1 Veterans Drive, Minneapolis, MN 55417. E-mail: plant, and various types of tea are created via manipulations (eg, drying, fermentation) of this leaf. As green tea is fermented to oolong and then to black tea, polyphenol compounds (catechins) Accepted for publication April 29, 2006.
Am J Clin Nutr 2006;84:551–5. Printed in USA. 2006 American Society for Nutrition The rice was boiled for 20 min, and then individual portions (176g containing 50 g carbohydrate) were frozen with 10 g butter.
Immediately before being ingested, the meals were warmed in amicrowave oven, and 0.2 g [13C]triolein (Cambridge IsotopeLaboratories, Andover, MA) was thoroughly mixed into themeal. Five hundred milliliters warm water and 10 g sucrose wereadded to the tea extract beverage or placebo preparation, whichwere well stirred. The subjects were randomly assigned to drinkeither the tea extract or the placebo beverage concurrently withthe meal. Breath samples were then collected at hourly intervalsfor 8 h. At the end of each test period, the subjects were asked torate a variety of symptoms—including nausea, bloating, abdom-inal discomfort, rectal gas, and obfuscating symptoms— on apreviously described linear scale that ranged from 0 (none) to 4(severe) (25). In addition, loose bowel movements were noted.
FIGURE 1. Mean (ȀSEM) breath-hydrogen concentrations in 20 sub-
One week later the test was repeated after the subjects ingested jects who ingested a meal consisting of 50 g rice (carbohydrate), 10 g butter,and 0.2 g [13C]triolein with a tea extract beverage (ᮀ) or a placebo beverage the opposite preparation from that ingested in the initial study.
(F), both of which contained 10 g sucrose. The significance of the differenceswas determined with a 2-tailed paired t test. Values obtained with the 2 Study B: lipid-containing, carbohydrate-free test meal
treatments were not significantly different between the 0- and 1-h measure-ments. Each hourly measurement from 2 to 8 h, however, was significantly Ten of the subjects took part in a second study that followed the greater when the tea extract was ingested (P ҃ 0.026 at 2 h, P ҃ 0.013 at 3 h, same format as study A; however, the caloric content of the meal and P  0.003 from 4 to 8 h).
consisted entirely of lipid (30 g olive oil plus 0.2 g [13C]triolein).
The tea leaf extract or placebo was similar to that described in theprevious study; however, sucrose was replaced with 1 g of the each breath sample relative to that of the baseline sample was noncaloric sweetener sucralose (Splenda McNeil Nutritionals, determined by mass spectroscopy, which was performed by a Fort Washington, PA). Breath samples were obtained for 13CO commercial laboratory (Metabolic Solutions Inc, Nashua, NH).
measurements as described in study A.
Statistics and calculations
Test products
The significance of differences between means observed with the 2 treatments was determined by 2-tailed paired t test. The The active preparation, a proprietary product, consisted of a quantity of carbohydrate malabsorption induced by the tea ex- mixture of extracts of green (0.1 g), black (0.1 g), and mulberry tract preparation was estimated by first determining the differ- (1.0 g) tea leaves. The approximate quantities of the potential ence between the sum of breath-hydrogen concentrations ob- antiabsorptive components per dose of our tea extract beverage served over hours 1– 8 when subjects ingested tea extract or (measured by HPLC) were as follows: 5 mg deoxynojirimycin- placebo. The grams of carbohydrate represented by this differ- type compounds, 100 mg epicatechin gallate, 300 mg epigallo- ence in hydrogen were estimated by comparison with the previ- catechin gallate, and 100 mg theaflavin. The control beverage ously observed difference in the sum of hydrogen concentrations contained trace quantities of red dye no. 40 and caramel to pro- over hours 1– 8 when 55 healthy subjects ingested 10 g lactulose vide a brown color similar to that of the tea extract. (Both prod- or a noncaloric beverage (27). The excess sum of breath- ucts were supplied by NatureGen Inc, San Diego, CA.) The taste hydrogen concentrations observed with 10 g lactulose averaged of the 2 test materials differed, and subjects were aware of the 6.2 ␮mol/L; thus, carbohydrate malabsorption induced by tea extract in the present study was estimated from the formula Breath collections
Expired air was sampled for hydrogen concentration as de- scribed previously (26). Breath samples for 13CO analysis were collected by having the subject expire through a straw into a glass tube (Labco Exetainer; Labco International Inc, Houston, TX),which was sealed immediately after withdrawal of the straw.
Analyses
Each breath collection for hydrogen measurement was ana- Breath-hydrogen concentration
lyzed for carbon dioxide (Capstar 100; CWE Inc, Ardmore, PA) The mean (ȀSEM) hourly breath-hydrogen concentrations to ensure that an adequate alveolar sample had been collected.
observed after ingestion of the rice and butter meal with each of The hydrogen concentration of the rare sample that contained the 2 treatments are shown in Figure 1. The hydrogen concen-
4.5% CO (5 of 360 samples) was normalized to 5% CO tration at baseline was not significantly different from that at 1 h.
(observed hydrogen concentration ҂ 5%/observed carbon diox- However, the curves significantly diverged by 2 h, with the ide concentration). The hydrogen concentration was measured breath-hydrogen concentration being significantly greater in the by gas chromatography with a molecular sieve column, nitrogen group receiving the tea extract beverage at each hourly time point as the carrier gas, and a reduction detector (Trace Analytic, from 2 to 8 h. The sum of the breath-hydrogen concentrations for Menlo Park, CA). The atom percent (atom%) excess of 13CO in hours 1– 8 (a value that closely approximated the area under the TEA EXTRACT INDUCES MALABSORPTION OF CARBOHDYRATE TABLE 1
Comparison of symptoms reported by healthy subjects in the 8-h period
after ingestion of a standard carbohydrate- and lipid-containing meal plus
a tea extract or placebo
1 Symptoms were rated on a linear scale of 0 (none) to 4 (severe).
2 Calculated with a 2-tailed paired t tests, not corrected for multiple 3 x៮ Ȁ SEM (all such values).
Symptoms
The severity of symptoms reported by the subject for the 8 h of study A are shown in Table 1. No significant differences (P 
FIGURE 2. Mean (ȀSEM) atom% excess of 13C in expired air after
0.05) in symptoms were observed for any symptom between the ingestion of 2 different test meals: a tea extract (ᮀ) or a placebo (F). The 2 treatment groups. Similarly, no significant differences in symp- significance of the differences was determined with a 2-tailed paired t test.
toms were observed between the 2 treatment groups in study B Study A: results for 20 healthy subjects who ingested a meal consisting of 50 g carbohydrate as rice, 10 g butter, and 0.2 g [13C]triolein with the tea extractor placebo solution, both of which contained 10 g sucrose. Values at 0 – 4 hwere not significantly different between the 2 treatment groups. The valueswere significantly greater in the tea extract group than in the placebo group DISCUSSION
at 5– 8 h (P ҃ 0.014 at 5 h and P  0.001 at 6 – 8 h). Study B: results for 10 We used measurements of breath-hydrogen and of breath- subjects who ingested a carbohydrate-free meal consisting of 30 g olive oil and 0.2 g [13C]triolein with the tea extract or placebo solution, both of which CO to determine whether ingestion of a tea extract preparation contained 1 g sucralose (noncaloric sweetener). No significant differences induced malabsorption of carbohydrate or fat. Carbohydrate were observed at any time point (P Œ 0.2).
malabsorption provides substrate for most of the hydrogen pro-duced in humans, which can be assessed by measuring breath- curve for 1– 8 h) averaged 12.2 Ȁ 2.0 and 2.7 Ȁ 0.6 ␮mol/L in the hydrogen concentrations (28, 29). In contrast, fat is not fer- groups receiving tea extract and placebo, respectively (P  mented to carbon dioxide by the colonic bacteria, and carbon 0.001). Using Equation 1, this difference in hydrogen (9.5 dioxide production from lipid reflects the host’s metabolism of ␮mol/L) indicated that the tea extract induced malabsorption of absorbed lipid. Studies using triolein labeled with 13C (30, 31) or Ȃ15 g of the 60 g of carbohydrate in the meal over the 8-h test 14C (32, 33) showed that fat malabsorption documented by fecal fat measurements was associated with a reduction in labeledcarbon dioxide excretion.
Breath-13CO measurements
In the present study, the subjects ingested standard meals with The mean (ȀSEM) hourly 13C atom% excesses (hourly values a beverage containing tea extract or placebo. The initial test meal minus baseline value) for the 2 treatments when subjects ingested contained 60 g carbohydrate (50 g starch as white rice and 10 g the rice and butter meal (study A) are shown in Figure 2. Al-
sucrose in the tea extract or the placebo) and 10.2 g fat. White rice though the measurements at hours 1– 4 were not significantly was used as the complex carbohydrate because, in contrast with different between the 2 treatments, the values were significantly most complex carbohydrates, rice starch is nearly completely higher for tea extract than for placebo at hours 5– 8. The sum absorbed by healthy subjects (34). Thus, a rice meal allows of the values for hours 1– 8 averaged 0.0256 Ȁ 0.0017 and breath testing to more sensitively determine whether a manipu- 0.0213 Ȁ 0.0019 atom% excess for the tea extract and the lation significantly increases hydrogen excretion, ie, causes placebo, respectively (P ҃ 0.014). The 13C atom% excess starch malabsorption. As shown in Figure 1, the breath-hydrogen values after ingestion of the lipid-containing (30 g olive oil plus concentration declined with the placebo, which indicated that [13C]triolein), carbohydrate-free meal (study B) are shown in residual fermentable colonic substrate was not replenished via Figure 2. In contrast with the results in study A, the sum of the malabsorption of carbohydrate in the test meal. In contrast, the values for hours 1– 8 for the tea extract (0.012 Ȁ 0.0025 atom% ingestion of tea extract resulted in increased breath-hydrogen excess) was virtually identical to that with the placebo (0.012 Ȁ concentrations, which were significantly greater than the values 0.0023 atom% excess) (P ҃ 0.95), and none of the hourly mea- observed with placebo for each hourly measurement between 2 surements showed significant differences (P Œ 0.2) between the and 8 h. Thus, the tea extract clearly induced malabsorption of the The carbohydrate malabsorption induced by the tea extract indicates that carbohydrate malabsorption induced by tea ex- was estimated by comparing the difference in breath-hydrogen tracts also could influence blood glucose concentrations. A sim- concentrations between the tea extract and placebo groups with ilar observation has been reported with an extract of the root of those observed previously (27) in healthy volunteers who in- Salacia oblonga (44, 45). This extract reduces glucose absorp- gested 10 g lactulose (see Equation 1). This calculation suggested tion via inhibition of intestinal ␣-glucosidase by 2 compounds, that Ȃ15 g of the 60 g of carbohydrate in the test meal was not salcinol and kotanol, that differ in structure from the absorbed. This may be a low estimate because nonabsorbed ma- ␣-glucosidase inhibitors in the tea preparation. It also should be terial in the test meal could have been fermented less rapidly than noted that 2 ␣-glucosidase–inhibiting drugs of bacterial origin (acarbose and miglitol) are available for the treatment of diabe- Elucidation of the mechanisms and specific tea extracts re- tes. However, the use of these drugs in the United States has been sponsible for the carbohydrate malabsorption will require addi- limited by side effects (eg, gas and diarrhea) and by a relatively tional studies. Mulberry leaf contains alkaloids of the minor effect on blood glucose concentrations. The structure of 1-deoxynojirimycin type that inhibit intestinal ␣-glucosidase ␣-glucosidase inhibitors in mulberry tea differs from that of (14). Green tea supplies epicatechin gallate and epigallocatechin acarbose, but is similar to that of miglitol. It remains to be de- gallate, compounds that inhibit mucosal sodium-glucose trans- termined whether carbohydrate malabsorption induced by our porters (17, 18). Black tea, via its theaflavin content, is an inhib- tea extract offers any benefits over those obtained with acarbose itor of ␣-amylase (8). The quantities of these compounds in one or miglitol. Although a significant increase in gaseous symptoms dose of our tea extract preparation are equivalent (depending on was not reported after ingestion of either the tea extract or the the compound) to that which would be contained in 5–20 cups placebo (Table 1), studies in which tea extract is administered (1.2– 4.8 L) of conventional tea. The extraction process reduced with each meal should be performed before it can be claimed that the caffeine of the tea extract to 50% of that of 1 cup (0.24 L) of tea extract–induced carbohydrate malabsorption is associated with fewer symptoms than has been observed with ␣-glucosi- dase–inhibiting drugs. Indeed, it would be surprising if the de- CO measurements did not support the concept that gree of malabsorption observed with the tea extract (25% of total the tea extract inhibited triacylglycerol absorption. Rather, the13 ingested carbohydrate) were not associated with some degree of CO concentration was significantly greater when tea extract accompanied the standard meal (Figure 2), a finding that cannot Extracts of black, green, and mulberry teas have been con- be explained by tea extract enhancing the absorption of lipid sumed for many years by enormous numbers of Asians, and because [13C]triolein absorption should approach 100% with the these products are considered safe. Green and black tea ex- placebo. One possible explanation is that the extract-induced tracts also are widely used in the Western world. Although tea carbohydrate malabsorption resulted in more rapid oxidization extracts have been shown to interact with the metabolism of of newly absorbed, labeled lipid because of the lesser availability other drugs (46, 47), serious complications possibly attribut- of glucose for energy utilization. It is also possible that the tea able to ingestion of these extracts are rare (48). Thus, although extract caused more rapid oxidation of absorbed [13C]oleic acid, the potential for unintended serious side effects is seemingly independent of differences in carbohydrate absorption (4). To low, rare unexpected side effects of the extract can be confi- differentiate between these 2 possibilities, 10 subjects ingested a dently excluded only after the product has been consumed in lipid-containing (30 g olive oil containing [13C]triolein), an environment where medical surveillance is adequate to carbohydrate-free meal plus the tea extract or placebo. No sig- nificant differences in 13CO excretion were observed, which suggested that the higher 13CO noted with the carbohydrate- JKF helped design the protocol, recruited the subjects, and analyzed the containing meal reflected the influence of the extract-induced data. MDL contributed to the design of the protocol, analyzed the data, and carbohydrate malabsorption on lipid metabolism.
wrote the manuscript. LZ was involved in the design of the protocol but hadno involvement in the collection or analysis of the data. LZ is president of The ability of a tea extract to inhibit carbohydrate absorption NatureGen, the company that provided the tea extract and placebo used in this has potential clinical utility for weight control and the treatment study. JKF and MDL had no financial interest in NatureGen or any other type of diabetes. Assuming that the tea extract causes malabsorption of conflict of interest with the material presented in this article.
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