Abstract
Objectives
This study aimed to examine the effects of green tea extract on working memory in healthy younger (21 - 29 y) and older (50 - 63 y) women.
Design
A single-blind, placebo-controlled, crossover design was used.
Setting
A university laboratory.
Participants
Twenty non-smoking Caucasian women were recruited in the younger (10) and older (10) age group.
Intervention
Subjects received 5.4 g green tea extract (at least 45% epigallocatechin-3-gallate) or placebo (cornstarch) within a 24-hour period.
Measurements
Working memory was measured by reading span and N-back task paradigm. Blood sample (20 mL) was collected and measured for plasma malondialdehyde (MDA) and total antioxidant capacity (TEAC) concentration. A 24-hour recall was conducted for each treatment period to ensure similar dietary patterns.
Results
Green tea extract significantly improved reading span performance in older women, indicated by higher absolute and partial scores of reading span. No significant changes were observed in the younger group. N-back latencies and accuracies were not significantly different after green tea treatment in either age group. Plasma concentration of MDA and TEAC were not different after green tea extract in either group.
Conclusion
Acute supplementation of decaffeinated green tea extract may enhance working memory capacity of women between 50 to 63 years of age. This study provides preliminary evidence that consumption of green tea extract may enhance the cognitive performance in older adults and thus provide potential chemopreventive benefits in this group. The mechanism should be explored in future research.
Key words: Green tea, working memory capacity, reading span, N-back task, oxidative stress
Introduction
Tea leaves, harvested from the plant Camellia sinensis, are used to produce green, black, and oolong tea (1). Black tea is more commonly consumed, representing 78% of tea production, while green tea constitutes 20% and is most frequently consumed in Japan and China (2). Green tea contains four major catechins, (-)-epigallocatechin-3-gallate (EGCG), (-)-epicatechin (EC), (-)-epicatechin-3-gallate (ECG), (-)-epigallocatechin (EGC), in addition to caffeine, tannin, and 300 other compounds (1). Epidemiological evidence suggests that green tea may provide chemopreventive benefits (3, 4, 5). A lower prevalence of cognitive impairment was associated with green tea consumption in adults over 55 years of age (6). Two cups of green tea per day was associated with 54% lower risk for cognitive impairment in adults over 70 years old, whereas effects were not evident for black/oolong tea or coffee (7). In subjects with mild cognitive impairment (MCI), consumption of 1.68 g green tea extract daily for four months significantly improved memory and attention (8).
Working memory is a central construct in psychology (9). It is defined as the structures and processes used for temporarily storing and manipulating information during ongoing interference (10). Although relevant for less than 10 seconds, working memory has a fundamental role in processing complex cognition, such as perception, attention control, problem-solving, logical reasoning, and language operations (11). Executive function is the attentional control system in the working memory model proposed by Baddeley and Hitch (11). Tea consumption has been associated with better cognitive function and lower risk of neurocognitive disorders in older adults (12, 13, 14). A single dose of green tea extract was found to significantly increase activation in the dorsolateral prefrontal cortex region of 21 – 28 year old men (15). This is a key region that engages executive function to allocate attentional resources during processing of working memory (16). Schmidt et al. suggested that increased activation may be a result of enhanced parieto-frontal connectivity induced by green tea consumption (17). However, increased activation observed using neuroimaging techniques did not produce better behavioral performance measured by N-back task (15, 17). The N-back task may not be sensitive enough to detect differences. Additional working memory measures should be included in the test battery. Furthermore, the activation may be confounded by caffeine in the green tea extract which is not present in the placebo. Studies are warranted to characterize the behavioral effects of green tea extract without caffeine on working memory. The objective of this study was to investigate the effects of decaffeinated green tea extract on working memory in women from younger and older age groups.
Methods
Subjects were recruited into the 18 – 30 y or 50 – 70 y age group with the following inclusion criteria: Caucasian, apparently healthy, non-smoking, BMI 18.6 - 27 kg/m2, and waist circumference < 35 inches. Exclusion criteria included being pregnant or lactating, reporting use of green tea products, psychotropic substances, anti-inflammatory drugs, a history of surgically-induced menopause, brain injury, depression, Attention Deficit Hyperactivity Disorder, schizophrenia, cancer, diabetes, stroke, myocardial infarction, thrombosis, blood clotting disorder, liver or kidney diseases, gastrointestinal problems, HIV positive or AIDS, estrogen or progesterone replacement therapy. Fasting blood samples were collected by auto-lancets and analyzed (CardioChek® PA, Polymer Technology Systems, Indianapolis, IN) to exclude those with high fasting glucose (> 125 mg/dL), total cholesterol (≥ 240 mg/dL), calculated LDL (≥ 160 mg/dL), or triglyceride (≥ 200 mg/dL). A written informed consent was signed by subjects; the Indiana University institutional review board approved the study (#1406408282). Subjects completed the mini-mental state examination (MMSE) as a measurement of global cognitive function (7, 18), and reported education level, handedness, and alcohol consumption.
Subjects were randomly assigned to receive decaffeinated green tea extract (Sunphenon® 90D capsules, at least 45% EGCG, Taiyo International, Minneapolis, MN) and placebo treatments, each separated by a one-week washout period. Capsules provided 5.4 g green tea extract (900 mg x 6 doses) or cornstarch over 24 hours (Figure 1). Subjects were directed to refrain from caffeine, supplements, alcohol, psychoactive drugs, prescription and over-the-counter medications for 24 hours, and fast overnight prior to testing. Barrier or hormonal contraceptives were required by all premenopausal women. Fasting was confirmed by blood tests for glucose and triglycerides (Figure 1). A 24-hour dietary recall was collected using a multiple-pass method (Nutrition Data System for Research, 2014 University of Minnesota, Minneapolis, MN). Subjects completed assessments of working memory using Inquisit 4.0.4 (Millisecond Software, Seattle, WA), including reading span [19, 20] and N-back tasks (21). Intravenous blood (20 mL) was drawn and plasma was analyzed for malondialdehyde (MDA) concentration (22), and total antioxidant capacity (23).
Figure 1.
Study design
Data were analyzed using SAS 9.3 (SAS Institute, Cary, NC). Demographic variables were analyzed using independent t-tests or chi-squared test. Dietary intake, reading span, and oxidative biomarkers were analyzed using mixed models. Contrasts were assigned to examine partial interactions. Data for N-back tests were analyzed using Wilcoxon Signed Rank test and adjusted for multiple comparisons (False Discovery Rate). Significance was reported when P < 0.05.
Results
Demographic characteristics of participants are presented in Table 1. Subjects were white, right-handed, had predominantly college or higher education (80%), and all were without severe cognitive impairment (MMSE score < 24). Average blood glucose, triglyceride, and total cholesterol were within normal ranges (60 - 100 mg/dL, < 150 mg/dL, < 200 mg/dL, respectively). Dietary patterns were similar between treatment periods (Table 1).
Table 1.
Demographic characteristics and dietary intake of subjects
| Younger group | Older group | P | |||
|---|---|---|---|---|---|
| Demographic characteristics | |||||
| Age (y) | 23.3 ± 2.4 | 57.0 ± 4.7 | < 0.01 | ||
| BMI (kg/m2) | 21.7 ± 1.8 | 23.0 ± 2.7 | 0.21 | ||
| Highest education | 0.67 | ||||
| High school | 3 | 1 | |||
| College | 6 | 7 | |||
| Graduate school | 1 | 2 | |||
| Handedness | n/a | ||||
| Right | 10 | 10 | |||
| Left | 0 | 0 | |||
| Global cognitive function | 28.7 ± 1.3 | 28.6 ± 1.1 | 0.85 | ||
| Glucose (mg/dL) | 68.9 ± 7.1 | 75.0 ± 6.8 | 0.07 | ||
| Triglyceride (mg/dL) | 76.7 ± 32.0 | 77.2 ± 36.9 | 0.97 | ||
| Total cholesterol (mg/dL) | 147.6 ± 26.8 | 155.8 ± 33.2 | 0.55 | ||
| Dietary intake during treatment | P | P | |||
| Calories (kJ) | Placebo | 6744.9 ± 846.8 | 0.26 | 7369.0 ± 1602.4 | 0.37 |
| Green tea | 7222.9 ± 1354.2 | 6994.8 ± 1739.7 | |||
| Fat (g) | Placebo | 68.7 ± 22.0 | 0.64 | 72.7 ± 19.9 | 0.93 |
| Green tea | 72.3 ± 17.4 | 72.0 ± 37.1 | |||
| Saturated fat (g) | Placebo | 22.2 ± 7.3 | 1.00 | 22.9 ± 6.6 | 0.74 |
| Green tea | 22.2 ± 6.0 | 24.0 ± 13.4 | |||
| Carbohydrate (g) | Placebo | 187.8 ± 66.9 | 0.52 | 215.2 ± 69.7 | 0.50 |
| Green tea | 203.7 ± 70.0 | 198.3 ± 56.6 | |||
| Protein (g) | Placebo | 70.2 ± 18.0 | 0.47 | 74.2 ± 26.6 | 0.49 |
| Green tea | 75.9 ± 24.6 | 68.8 ± 26.7 | |||
| Vitamin C (mg) | Placebo | 121.2 ± 103.8 | 0.84 | 82.2 ± 54.1 | 0.55 |
| Green tea | 110.6 ± 105.5 | 113.3 ± 88.3 | |||
| Vitamin E (mg) | Placebo | 9.6 ± 3.5 | 0.07 | 9.1 ± 4.6 | 0.61 |
| Green tea | 11.8 ± 6.0 | 10.3 ± 7.5 | |||
| Vitamin A (µg) | Placebo | 912.7 ± 678.0 | 0.19 | 866.5 ± 782.2 | 0.97 |
| Green tea | 1356.6 ± 1050.5 | 747.6 ± 613.2 | |||
| Carotenoids (µg) | Placebo | 13437.4 ± 12924.9 | 0.11 | 8364.9 ± 6096.1 | 0.25 |
| Green tea | 17891.3 ± 13655.0 | 6515.1 ± 6764.2 |
Values are mean ± SD, n = 20. Independent t-tests or chi-square test was used to compare the demographic variables between age groups. A mixed model, with age as the between-subject factor and treatment as the within-subject factor, was used to compare the dietary intake between treatments within each group.
The absolute score and partial score for reading span in the older group were improved by 23% and 9.7%, respectively, after green tea extract (P = 0.04, P = 0.047, Table 2). Total errors were 35% lower in older group after green tea extract, though the result became nonsignificant after adjusting for multiple comparisons (P = 0.09). In the younger group, green tea extract did not affect the absolute score (P = 0.17), partial score (P = 0.37), or total errors (P = 0.79). p ]The mean 1-back latency in the older group was lower after green tea extract and this change was marginally significant (P = 0.055), but no significant change was observed in the younger group (P = 0.77). Green tea extract did not affect the latency of 0-back, 2-back, and 3-back in the older group (P = 0.32, P = 0.46, P = 0.56) or the younger group (P = 0.32, P = 0.85, P = 0.56). No significant changes were observed in the accuracy of 0-, 1-, 2-, or 3-back tests after green tea extract in either age group (Table 2). Plasma MDA concentration and total antioxidant capacity did not change after green tea extract in either age group (Table 2).
Table 2.
Effects of 1-week green tea consumption on performance of working memory and oxidative stress biomarkers1
| Measurements | Placebo | Younger group Green tea | P | Placebo | Older group Green tea | P | |
|---|---|---|---|---|---|---|---|
| Reading span2 | |||||||
| Absolute score | 51.5 ± 4.9 | 56.6 ± 4.4 | 0.17 | 39.5 ± 6.2 | 48.6 ± 5.2 | 0.04 * | |
| Partial score | 65.6 ± 2.4 | 67.7 ± 2.3 | 0.37 | 58.5 ± 3.7 | 64.2 ± 2.8 | 0.047 * | |
| Errors | 3.0 ± 0.5 | 2.7 ± 1.0 | 0.79 | 3.1 ± 0.8 | 2.0 ± 0.6 | 0.09 | |
| N-back latency3 | |||||||
| 0-back, ms | 480.6 ± 21.3 | 507.6 ± 31.9 | 0.32 | 525.8 ± 17.7 | 550.9 ± 28.9 | 0.32 | |
| 1-back, ms | 555.6 ± 27.7 | 544.1 ± 37.9 | 0.77 | 614.1 ± 29.8 | 575.4 ± 26.3 | 0.055 | |
| 2-back, ms | 629.0 ± 47.2 | 628.9 ± 49.6 | 0.85 | 673.0 ± 69.7 | 722.1 ± 66.4 | 0.46 | |
| 3-back, ms | 741.4 ± 70.9 | 808.4 ± 77.4 | 0.56 | 808.5 ± 64.9 | 852.4 ± 90.3 | 0.56 | |
| N-back accuracy3 | |||||||
| 0-back, % | 98.7 ± 0.9 | 98.7 ± 0.9 | 0.99 | 98.7 ± 0.9 | 98.7 ± 0.9 | 0.99 | |
| 1-back, % | 96.0 ± 1.5 | 96.0 ± 1.8 | 0.99 | 97.3 ± 1.5 | 98.0 ± 1.0 | 0.99 | |
| 2-back, % | 92.0 ± 3.3 | 92.0 ± 2.4 | 0.87 | 84.0 ± 5.3 | 89.3 ± 2.8 | 0.87 | |
| 3-back, % | 71.3 ± 7.6 | 63.3 ± 7.0 | 0.67 | 63.7 ± 4.1 | 58.7 ± 5.0 | 0.67 | |
| Oxidative stress biomarkers | |||||||
| Plasma MDA, μM | 3.8 ± 0.4 | 3.3 ± 0.4 | 0.36 | 4.3 ± 0.6 | 4.6 ± 0.4 | 0.36 | |
| Plasma TEAC, μM | 5.5 ± 0.3 | 5.5 ± 0.3 | 0.42 | 5.2 ± 0.2 | 5.1 ± 0.2 | 0.42 |
Values are mean ± SEM, n = 20. Data for reading span and oxidative stress biomarkers were log transformed and analyzed by mixed model, with age as the between-subject factor and treatment as the within-subject factor. Data for N-back was analyzed by Wilcoxon Signed Rank nonparametric test.
P<0.05, compared to placebo; ** P<0.01, compared to placebo. MDA, malondialdehyde. TEAC, total antioxidant capacity;
Subjects read aloud at their own pace sentences presented on the screen, while remembering a letter that was presented after each sentence for later recall. Subjects were required to indicate the veracity of each sentence by responding true or false within 1.5 s. After a series of sentences, the subject recalled letters in the sequence presented. A total of 15 sets, 3 each consisting of 3, 4, 5, 6, 7 sentences that were 13-16 words in length, were presented in a random order. The test was terminated when the subject failed to recall all three items of a given set. Absolute score is the sum of letters where all items in a set were recalled in the correct order. Partial score is the sum of letters recalled in the correct serial position, regardless of whether the entire set was recalled correctly. Errors are the total number of errors made on the processing component of the task.
Subjects were presented with a stream of letters, and the task was to decide for each letter whether it matched the one presented N items before. A total of 12 blocks were presented in a pseudo-random order, including 3 blocks for each level of N-back (n = 0, 1, 2, 3). Each block contained 15 letters using 20 different consonants. Each letter was presented for 500 ms and paused for 2000 ms. Of the 15 letters, 5 were targets and 10 were non-targets. The computer selected letters and randomly assigned them as targets or non-targets. For each N-back level, the correct response was recorded as total hits minus false alarms. Accuracy (%) was calculated as (total hits - false alarms)/5. Latency was recorded as the reaction time for the correct response to target letters. To reduce the learning effect, subjects practiced three blocks for each N-back level before proceeding to the actual test.
Discussion
To our knowledge, this is the first study investigating acute effects of decaffeinated green tea extract on working memory in younger and older groups of healthy women with no obvious signs of mental impairment. Reading span has been proven to be a reliable and valid measure of working memory (19). The absolute and partial scores measured in this study were comparable with previous studies (24). The mean absolute score of the older group improved by 23% after green tea; similarly, the mean partial score was also 9.7% higher. These minor but statistically significant improvement suggest that acute intake of green tea extract may enhance working memory function. These effects were not observed in the younger group. A possible explanation is that the older group might have experienced subtle cognitive impairment due to the aging process (25), that was responsive to the green tea extract, whereas the younger women had no decline, and thus nothing could be improved by the extract. Park et al. reported similar results in adults (40 – 75 y) with MCI (MMSE score 21 – 23); they found that four months of green tea extract consumption (1.68 g/day) improved memory, selective attention, and alertness by significantly increasing memory quotient, word reading, and brain theta waves in the temporal, frontal, parietal, and occipital areas in the eye-open and reading states (8). Ide et al. found that green tea powder (2 g/day, for three months) significantly increased the MMSE score in older adults over 65 years of age (26). Interestingly, N-back performance did not change in either age group. This may seem in conflict with the reading span results. However, these two measures were only weakly correlated (r = 0.10 - 0.24), suggesting that each measure might independently explain part of the variance in working memory (27). Research has suggested that reading span is an index of working memory capacity, whereas N-back task may reflect more of working memory processing (28). Therefore, green tea extract might have a greater impact on the capacity rather than the processing of working memory.
Only 1-back latency of the older group showed marginally significant reduction after green tea, while other latencies remained unchanged. This may be explained by the higher reliability of 1-back latency (r = 0.94), compared with 2- and 3-back latencies, as described in prior research (27). Our findings are similar to other studies that examined effects of green tea extract on N-back performance. Borgwardt et al. showed that a single dose of green tea extract (13.75 g or 27.5 g) administered to 12 adult men (21 – 28 y) led to no changes in the latency and total errors in 0-, 1-, and 2-back tests (15). N-back accuracies did not change after green tea in the present study. Schmidt et al. also reported that N-back accuracy (calculated as the z score of total hits minus the z score of false alarms) did not change after green tea extract (17). They suggested that green tea extract might enhance working memory processing by increasing brain activation in the dorsal lateral prefrontal cortex and the parieto-frontal connectivity (15, 17). However, increased activation did not result in any behavioral changes. Furthermore, the two studies (15, 17) may be confounded by caffeine that was in the green tea extract but not in placebo. The present study reduced confounding by using decaffeinated green tea extract that contained 8.37 mg caffeine per 900 mg extract (0.93% caffeine).
The present study has several limitations. First, the extract was given over a short duration, which may explain the lack of changes in plasma oxidative biomarkers. Future studies may extend the treatment period to better characterize the effect. Secondly, plasma catechin concentrations were not measured; however, compliance was assured as doses were delivered to subjects and consumption was monitored in person. Previous studies have already characterized the pharmacokinetics of plasma EGCG following a similar dose of decaffeinated green tea extract (29, 30). Furthermore, our study sample size is low, especially for N-back measurements. Oxidative DNA damage (8-hydroxy-2' -deoxyguanosine and comet assay) may be measured in future studies to provide other markers for oxidative stress.
This study provides preliminary evidence that acute supplementation of decaffeinated green tea extract may enhance working memory capacity of women between 50 to 63 years of age. The mechanism behind this phenomenon should be explored in future studies.
Conflicts of Interest
The authors have nothing to disclose.
Ethical Standard
This research was approved by the Institutional Review Board of the Indiana University.
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