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Appetite 56 (2011) 235–240 Contents lists available at ScienceDirect Appetite journal homepage: www.el

Contents lists available at ScienceDirect

Appetite

journal homepage: www.el sevier.com/locate/appet

Appetite journal homepage: www.el sevier.com/locate/appet Research report Black tea improves attention and

Research report

Black tea improves attention and self-reported alertness §

E.A. De Bruin a , * , M.J. Rowson b , L. Van Buren a , J.A. Rycroft b , G.N. Owen b , c

a Unilever R&D Vlaardingen, Olivier van Noortlaan 120, PB Box 114, NL-3130 AC Vlaardingen, The Netherlands b Unilever R&D Colworth, Colworth Science Park, Sharnbrook, Bedford MK44 1LQ, United Kingdom c National Hospital for Neurology & Neurosurgery, Institute of Neurology, Queen Square, London WC1N 3BG, United Kingdom

ARTICLE INFO

Article history:

Received 3 August 2010 Received in revised form 30 November 2010 Accepted 13 December 2010 Available online 21 December 2010

Keywords:

Attention

Alertness

Mood

Tea

Caffeine

Theanine

Plasma levels

ABSTRACT

Tea has previously been demonstrated to better help sustain alertness throughout the day in open-label studies. We investigated whether tea improves attention and self-reported alertness in two double- blind, randomised, placebo-controlled, crossover studies. Participants received black tea (made from commercially available tea bags) in one condition and placebo tea (hot water with food colours and flavours) similar in taste and appearance to real tea in the other condition. Attention was measured objectively with attention tests (the switch task and the intersensory-attention test) and subjectively with a self-report questionnaire (Bond–Lader visual analogue scales). In both studies, black tea significantly enhanced accuracy on the switch task (study 1 p < .002, study 2 p = .007) and self-reported alertness on the Bond–Lader questionnaire (study 1 p < .001, study 2 p = .021). The first study also demonstrated better auditory ( p < .001) and visual ( p = .030) intersensory attention after black tea compared to placebo. Simulation of theanine and caffeine plasma time–concentration curves indicated higher levels in the first study compared to the second, which supports the finding that tea effects on attention were strongest in the first study. Being the second most widely consumed beverage in the world after water, tea is a relevant contributor to our daily cognitive functioning. 2011 Elsevier Ltd. All rights reserved.

Introduction

Being able to concentrate and attend to the job at hand are important in our everyday life, whether at work, in your car driving home, or helping the kids with their homework in the evening. In this context, simple actions that could help sustain cognitive abilities throughout the day are welcome. Tea is the second most frequently consumed beverage in the world being only surpassed by water, and is often credited with cognitive benefits by consumers. A decade ago, scientists have started exploring the cognitive effects of tea. In these intial open-label studies, it was demonstrated that having a few cups of tea during the day increased subjective alertness and helped sustain arousal ( Hind- march, Quinlan, Moore, & Parkin, 1998; Hindmarch et al., 2000; Quinlan et al., 2000 ). Specifically, performance on the critical flicker fusion task was improved after tea as compared to water indicating higher levels of arousal ( Hindmarch et al., 1998, 2000 ). In addition, tea consumption was associated with faster choice

§ The authors would like to thank Nick Tyrrell, Mano Pillai, Suzanne Eino¨ ther, Vanessa Martens, Kay Budd-Fletcher, Daniel Rycroft, Nelly van der Meer, Selina Hira, Solene Naveos, and Timo Giesbrecht for their support. The studies were sponsored by Unilever. * Corresponding author. E-mail address: Eveline-de.Bruin@unilever.com (E.A. De Bruin).

0195-6663/$ – see front matter 2011 Elsevier Ltd. All rights reserved. doi: 10.1016/j.appet.2010.12.011

reaction time performance ( Hindmarch et al., 2000 ) and higher levels of self-reported alertness ( Quinlan et al., 2000 ). The effects of tea on arousal and alertness may be due to its natural ingredients such as caffeine. Many studies have reported that caffeine improves performance on attention tests (e.g., Brice & Smith, 2002; Horne & Reyner, 1996; Lieberman, Tharion, Shukitt- Hale, Speckman, & Tulley, 2002; Rogers et al., 2005 ), even at levels comparable to those in a cup of tea (35–60 mg; Durlach, 1998; Lieberman, Wurtman, Emde, Roberts, & Coviella, 1987; Smit & Rogers, 2000; Smith, 2009; Smith, Sturgess, & Gallagher, 1999 ). As tea is one of the main dietary sources of caffeine globally, it may thus significantly contribute to improved cognitive function in many people ( Bryan, 2008; Ruxton, 2008 ). In addition to caffeine, a cup of tea naturally contains 5–23 mg theanine ( g -N-ethylglutamine), an amino acid virtually exclusive to tea. Theanine when ingested on its own increases calmness and relaxation (e.g., Abdou et al., 2006; Lu et al., 2004; Nobre, Rao, & Owen, 2008 ). In vitro work suggests that theanine interacts with the effects of caffeine ( Kimura & Murata, 1986 ), which is supported by EEG studies showing that theanine alone significantly synchronises brain activity related to attentional processing ( Gomez-Ramirez et al., 2007; Gomez-Ramirez, Kelly, Montesi, & Foxe, 2009 ), but in combination with caffeine induces even greater synchronisation ( Kelly, Gomez-Ramirez, Montesi, & Foxe, 2008 ). Behavioural studies confirmed the positive effects of theanine and caffeine on attention ( Einother, Martens, Rycroft, & de Bruin, 2010;

]

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I G 236 E.A. De Bruin et al. / Appetite 56 (2011) 235–240 Fig. 1. Plasma

Fig. 1. Plasma time–concentration profiles of caffeine (a) and theanine (b) based on the dosing regime in study 1 (boxes) and 2 (circles).

Giesbrecht, Rycroft, Rowson, & de Bruin, 2010; Owen, Parnell, de Bruin, & Rycroft, 2008 ). Moreover, tea is associated with more consistent levels of alertness throughout the day than coffee, even when matched for caffeine content ( Hindmarch et al., 1998 ), suggesting that tea ingredients such as theanine may modify the alerting effect of caffeine. Besides caffeine and theanine, prelimi- nary evidence indicates that flavonoids may also improve cognitive performance ( Macready et al., 2009 ), and there may be other tea ingredients with a positive impact on attention yet to be discovered. Thus, tea may be a likely candidate for improving attention in everyday life. In the two systematic studies described in the present paper we investigated the effects of two commercially available black tea blends on attention and self-reported alertness using a double-blind, randomised placebo-controlled, cross-over design. In the first study, a relatively strong tea blend containing 2.6 g/L tea solids (PG Tips tea) was used as this was the first randomised and placebo-controlled study on tea and attention. As the results were positive, the study was repeated with a slightly less strong tea (Lipton Yellow Label tea; 1.9 g/L tea solids) to find out whether the effects were dose-dependent. Plasma curves were simulated based on the dosing regime and population character- istics of the two current studies and pharmacokinetic data on caffeine and theanine from previous studies (see Van der Pijl, Chen, & Mulder, 2010 for theanine; caffeine data unpublished) in a

physiologically based pharmacokinetic model (GastroPlus; Parrot and Lave´ , 2008 ). These simulations indicated that the caffeine and theanine peak plasma levels in the second study were very likely to be slightly lower than those in the first study (see Fig. 1 a for caffeine and b for theanine) thus allowing for first indications of dose dependency.

Methods

Twenty-six volunteers (20 females) aged on average 30.7 years ( SD = 11.2) took part in study 1, and 32 volunteers (15 females) aged on average 30.3 years ( SD = 10.1) participated in study 2. The sample size of study 1 was loosely based on the observational tea studies by Hindmarch et al. (1998, 2000) and Quinlan et al. (2000). The sample size required for study 2 was calculated to be 36 based on the first study, taking a smaller effect size and an anticipated drop-out rate of 20% into account. Participants were regular caffeine consumers (average caffeine intake 306.4 mg/day ( SD = 148.6) in study 1 mg/ day and 280.1 mg/day ( SD = 142.2) in study 2), and had a body mass index (BMI) between 18 and 32. Exclusion criteria were allergies to caffeine or herbal supplements, colour blindness, dyslexia, preg- nancy, breastfeeding, and use of recreational drugs and medication with the exception of the contraceptive pill. The studies were approved by the Unilever Colworth Research Ethics Committee and were carried out in accordance with the ethical standards laid down in the 1964 Declaration of Helsinki. Participants provided written informed consent prior to inclusion in the study and were paid for their participation. A crossover, double-blind, randomised, placebo-controlled design was used in both studies. In study 1, participants received two servings of placebo tea in one condition and two servings of black tea in the other condition over the course of 60 min. In study 2, participants received three servings of placebo tea in one condition and three servings of black tea in the other condition over the course of 90 min. Treatments were allocated using a Latin square design such that the order of treatments was counter- balanced across participants. Visits were separated by at least 6 days and at most 14 days. For study 1, the tea was prepared by pouring 235 ml of boiled, de-ionised water onto a PG Tips tea bag. The tea was passively infused for 60 s after which the tea bag was removed and allowed to drip over the cup for 3 s. 200 ml of the infusion was then poured and served in a fresh cup. The placebo was prepared by adding 10 mg caramel colour 602, 10 m l red food colour, 7 mg tea flavour 502840, 150 mg oak tannin, and 150 mg grape seed tannin powders to 200 ml boiled, de-ionized water. For study 2, the tea was prepared by pouring 190 ml of boiled, de-ionised water onto a Lipton Yellow Label tea bag. The tea was passively infused for 90 s, after which the tea bag was removed and allowed to drip over the cup for 3 s. Ten milliliter water at room temperature was added. The placebo was prepared by adding 190 ml boiled, de-ionized water to a 10-ml aliquot at room temperature containing 20 mg caramel colour 602, 4 m l red food colour, 3 mg tea flavour 502840, and 120 mg oak tannin. See Table 1 for the amount of tea solids, caffeine, and theanine in each study. The tea flavours and colours used have no known

Table 1 Amount of tea solids and caffeine and theanine content per serving and in total per visit for each study.

 

Tea solids

Caffeine

Theanine

Servings

Tea solids

Caffeine

Theanine

Per 200-ml serving (mg)

Per visit (ml)

In total per visit (mg)

Study

1

520

50

23

2 200 3 200

1040

100

46

Study

2

380

30

12

1140

90

36

E.A. De Bruin et al. / Appetite 56 (2011) 235–240

237

effects on cognition. Experienced tea tasters rated the taste and appearance of the placebo teas in both studies as very similar to the respective real teas.

clear-headed, co-ordinated, energetic, quick-witted, attentive, proficient, interested), Contentedness (contented, happy, amica- ble, gregarious, tranquil), and Calmness (calm, relaxed). The Bond–

Analysis

Procedure

Lader mood rating scales are frequently used in studies of pharmacological drugs and previously demonstrated increased

Participants arrived at the laboratory at 12:00 midday having consumed only their normal breakfast and water, and having abstained from alcoholic beverages and caffeinated foods and medications from 9 pm the previous day. Participants were provided with a standardized lunch, and were required to consume an identical meal on each visit. Following lunch, participants completed a set of attention tests.

Test battery

self-reported alertness following caffeine with or without theanine (e.g., Giesbrecht et al., 2010; Haskell, Kennedy, Milne, Wesnes, & Scholey, 2008; Owen et al., 2008 ). The order in which the tests were administered was fixed in each session in both studies in the following order: intersensory- attention task, switch task, Bond–Lader mood rating scales.

After this first set of tests (baseline), they consumed the first drink during a 10-min break. They then completed the second set of tests (session 1), after which they consumed another drink during the second 10-min break. After that, another set of tests (session 2) followed. In study 1, the participants received two drinks and completed three test sessions per condition in total. In study 2, the participants received three drinks and completed four test sessions per condition in total (see Table 2 ).

Proportion correct responses and reaction times on the attention tests, and subjective factor scores were analysed using a 2 2 mixed model ANOVA with a repeated-measures covariance structure. Subjects were modelled as a random effect, and treatment (black tea or placebo tea) and session (2 sessions after the drinks in study 1; and 3 sessions after the drinks in study 2) were used as within-subject factors. Baseline scores and treatment order were employed as covariates. For the switch task, trial type (1st, 2nd, and 3rd trial after switching to another rule within the

Results

The switch task measured the ability to shift attention between different task sets ( Monsell, 2003 ). During each trial, one letter and one number were displayed on the screen simultaneously for 1 s. The letters were randomly drawn from a set of four vowels (A, E, I, or U) and four consonants (G, K, M, or R) and the numbers from a set of four even (2, 4, 6, or 8) and four odd numbers (3, 5, 7, or 9).

test) and response type (correct hit, correct withhold) were used as additional within-subject factors. Alpha was set at 5% (two-sided). Only significant main effects and interactions involving tea are reported here. Figures depict means and standard errors corrected for baseline.

Participants were required to respond to even numbers, but only when the font colour was purple, or to vowels, but only when the

Study 1

font colour was red (instruction counterbalanced between sessions). The font colour and therefore the task ‘switched’ every three trials in a predictable manner. Participants completed four 2.5-min blocks of 144 stimulus pairs during each session in both

Intersensory attention Participants made more correct responses on the intersensory subtasks (auditory: F 1,79.7 = 14.2, p < 0.001; see Fig. 2 ; visual:

studies. This test has repeatedly been shown to be sensitive to the

F 1,63.7 = 5.2, p < 0.030; see Fig. 3 ), and responded faster (visual:

effect of caffeine and theanine on attention ( Einother et al., 2010; Giesbrecht et al., 2010; Owen et al., 2008 ). The intersensory attention task measured the ability to

F 1,18.6 = 4.7 p = 0.043) after tea compared to after placebo. There were no main effects of tea or tea-by-session interactions for correct responses or reaction times on the unisensory subtasks.

selectively deploy attention to stimuli presented in the visual and auditory modalities ( Foxe, Simpson, & Ahlfors, 1998 ). Each trial consisted of an auditory cue instructing participants to attend to either the auditory or visual modality followed by auditory stimuli or visual stimuli (unisensory), or both auditory and visual stimuli (intersensory) after 1200 ms. Participants were required to

Task switching Participants made more correct responses after black tea than after placebo tea ( F 1,22.4 = 12.0, p = 0.002; see Fig. 4 ). There was no main effect of tea on reaction times. Switch costs were present as expected but not influenced by tea.

perform a discrimination task (same or different) in the cued modality. Participants completed six (study 1) or four (study 2) blocks of trials during each session, each containing a total of 100 cue–stimuli pairs and lasting approximately 5 min. This test has previously been shown to be sensitive to the effect of theanine on attention ( Gomez-Ramirez et al., 2007 ; trend for the effect of caffeine and theanine in Einother et al., 2010 ).

Mental state Participants felt significantly more alert and less calm after tea than after placebo (Composite Alertness F 1,22.9 = 23.83, p < 0.001, see Fig. 5 ; Composite Calmness F 1,25 = 8.20, p = 0.008; due to a decrease on the item ‘relaxed’). There was no difference in Contentedness between the conditions ( F 1,25 = 0.63, p = 0.44).

Self-reported mental state was measured using the Bond–Lader visual analogue mood rating scales ( Bond & Lader, 1974 ).

Study 2

Participants were asked to indicate how they felt at that moment on sixteen 100-mm visual analogue scales anchored at either end by an adjective pair (e.g., Tense/Relaxed). The individual scores were combined to form three factors: Alertness (alert, strong,

Intersensory attention There were no significant differences in the number of correct responses or reaction times between the tea and placebo

Table 2 Timing of test sessions in minutes relative to the first drink in each study.

 

Baseline

Drink

Session 1

Drink

Session 2

Drink

Session 3

End

Study 1

40

0

10

50

60

100

Study 2

30

0

10

40

50

80

90

120

]

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]

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et al. / Appetite 56 (2011) 235–240 ] [ ( ) T D $ F I

Fig. 2. Percentage correct responses on the auditory intersensory attention subtask (study 1). Main effect of tea ( p = .001).

[ ( ) T D $ F I G ]

1). Main effect of tea ( p = .001). [ ( ) T D $ F

Fig. 3. Percentage correct responses on the visual intersensory attention subtask (study 1). Main effect of tea ( p = 0.030).

[ ( ) T D $ F I G ]

1). Main effect of tea ( p = 0.030). [ ( ) T D $ F

Fig. 4. Percentage correct responses on the attention switching task (study 1). Main effect of tea ( p < .002).

conditions, but there was a trend for more correct responses in the visual unisensory subtask after tea ( F 1,31.4 = 3.1, p = .09).

after tea ( F 1 , 3 1 . 4 = 3.1, p = .09). Fig.

Fig. 5. Change from baseline in self reported alertness (study 1). Main effect of tea

( p < .001).

[ ( ) T D $ F I G ]

Main effect of tea ( p < .001). [ ( ) T D $ F I

Fig. 6. Percentage correct responses on the attention switching task (study 2). Main effect of tea ( p = 0.007).

[ ( ) T D $ F I G ]

2). Main effect of tea ( p = 0.007). [ ( ) T D $ F

Fig. 7. Change from baseline in self reported alertness (study 2). Main effect of tea ( p = 0.021).

F 1,28.6 = 3.2, p = 0.085) after tea than after placebo. There was no difference in feelings of calmness between the conditions (Composite Calmness F 1,30.2 = 0.03, p = 0.86).

Discussion

Task switching Participants made more correct responses after tea than after placebo ( F 1,28.9 = 8.53, p = 0.007; see Fig. 6 ). There was no difference in reaction times between the conditions. Switch costs were present as expected but not influenced by tea.

Mental state Participants felt significantly more alert (Composite Alertness F 1,34.2 = 5.9, p = 0.021, Fig. 7 ) and there was a tendency towards greater feelings of contentedness (Composite Contentedness

The aim of the current studies was to find out whether black tea influences attention. Following previous open-label studies indicating positive effects ( Hindmarch et al., 1998, 2000; Quinlan et al., 2000 ), in the current studies two commercially available tea blends without modified levels of caffeine or theanine (or any other ingredient) were tested using a double-blind, randomised, placebo-controlled, cross-over design. Both studies indicated that tea improved attention as demonstrated with improved perfor- mance on objective attention tests and as self-reported on a mental-state scale.

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In both studies, tea improved overall accuracy on the switch task indicating that both teas enhanced the ability to attend and respond to stimuli according to the rule cued by the colour of the stimuli. Subjects responded more slowly after switching from one rule to another within the test as expected; these ‘switch costs’ ( Monsell, 2003 ) were not differentially influenced by tea. In addition, tea also improved accuracy and reaction times on the intersensory-attention test in the first study study indicating that the slightly stronger tea enabled the participants to respond more correctly and faster to stimuli in the task-relevant modality while ignoring stimuli simultaneously presented in the irrelevant modality. This simultaneous increase in accuracy and reduction in reaction time after tea is in line with findings from previous studies on theanine and caffeine and enhanced attentional processing ( Gomez-Ramirez et al., 2007; Kelly et al., 2008 ). Together, the findings on the switch task and intersensory- attention task suggest that tea improves the ability to focus attention on the task at hand but does not influence switching between task rules. Alternatively, the finding that the effects of tea were strongest on the task performed towards the end of the test session could also indicate that tea may counteract effects of fatigue. Caffeine is known to reduce fatigue in low-arousal situations such as working at night and driving (e.g., Brice & Smith, 2001; Lieberman et al., 2002; Smith, Sutherland, & Christopher, 2005 ). It would be interesting to examine the effects of caffeine in combination with theanine on these real-life activities. Possibly, tea can help sustain attention in everyday life by reducing momentary lapses of attention in fatiguing situations. The improvements in attention after tea that were measured with objective tests of accuracy and response speed were associated with increased self-reported alertness in both studies. This indicates that the improvements in attention after tea measured objectively with standardised cognitive tests were noticeable to the participants and are thus relevant to tea consumers. In addition, in the first study, self-reported calmness decreased after tea. More detailed exploratory analyses revealed that this was due to a decrease on one item measuring relaxation, which is consistent with increased subjective alertness after tea. This lends support to the idea that theanine, while increasing calmness and relaxation in isolation, modulates attentional processing when combined with caffeine. Although both studies indicated that black tea improves attention, the effects were stronger in the first than in the second study. This could be due to differences in caffeine and theanine plasma levels resulting from differences between studies in tea blends and timing of consumption of the drinks. Moreover, the fact that the intersensory attention test, which was always adminis- tered first after any drink, only four blocks were completed in study 2 versus six blocks in study 1 may have allowed for a lower build- up of plasma levels of active ingredients during this test in the second study as compared to the first. Thus, the present findings provide tentative evidence that the attention effects of tea behave in a dose-dependent manner. Yet, a more thorough study with a dose–response design using different levels of tea strength, and consequently of caffeine and theanine, is needed to further support this assertion. As the participants in the current studies were habitual caffeine consumers abstaining from caffeine the night before each visit, it may be argued that the positive effect of tea on attention reflects reversal of caffeine withdrawal rather than a net effect (cf. the caffeine studies of James & Rogers, 2005; Keane & James, 2008; Rogers et al., 2005; Yeomans, Ripley, Davies, Rusted, & Rogers, 2002 ). However, caffeine has been demonstrated to improve performance in non-withdrawn as well as withdrawn participants ( Smith, 2002; Smith et al., 2005 ), in withdrawn participants after very short abstinence periods (1 h; Warburton, 1995 ), and also in

light, non-dependent caffeine users ( Childs & de Wit, 2006; Hewlett & Smith, 2006 ) and in non-users ( Smith, Christopher, & Sutherland, 2006 ), suggesting a net effect of caffeine on attention. Moreover, adding the amount of caffeine habitually consumed as a covariate to the analyses of the current studies did not change the results. Thus, relief from caffeine withdrawal seems unlikely to account for the currently reported effect of tea on attention. To our knowledge, this paper reports the first two studies on the effects of tea on attention using a double-blind, randomised, placebo-controlled design. Both studies indicated that black tea improves attention. To conclusively determine whether differ- ences in tea strength and dosing regime can explain the subtle differences in results between the studies, a dose–response study on tea and attention should be carried out. A study with a full factorial design contrasting tea with and without theanine and/or caffeine could shed more light on the relative contribution of theanine and caffeine to the effect of tea on attention. Being the second most widely consumed beverage in the world after water, tea is a relevant contributor to our daily cognitive functioning.

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