Published online before print December 6, 2007, doi: 10.1161/ATVBAHA.107.151928
© 2008 American Heart Association, Inc.
Clinical and Population Studies |
Tea Consumption Is Inversely Associated With Carotid Plaques in Women
From Inserm, U744 (S.D., D.C., P.A., M.Z.), Lille; Department of Neurology (EA2691) (S.D.), University Hospital of Lille; Inserm, U700 (D.C., N.L., M.Z.), Paris; Inserm, U708 (C.T., A.A.), Paris; Inserm, U593 (J.F.D., P.B.G.), Bordeaux; Inserm, E0361 (K.R.), Montpellier; Inserm, U780 (P.D.), Paris; Centre de Médecine Préventive Cardiovasculaire (J.G.), Broussais Hospital, Paris, France.
Correspondence to Mahmoud Zureik, MD, PhD, Inserm, U700, Faculté de Médecine de Xavier Bichat, 16 Rue Henri Huchard, Paris, F-75018, France. E-mail zureik{at}bichat.inserm.fr
Abstract
Objective— The aim of this study was to assess the relationship of tea consumption with common carotid artery intima-media thickness (CCA-IMT) and carotid plaques.
Methods and Results— The study was performed on 6597 subjects aged 
65 years, recruited in the French population for the Three-City Study. Atherosclerotic plaques in the extracranial carotid arteries and CCA-IMT were measured using a standardized protocol. Results were tested for replication in another, younger, French population sample (EVA-Study, 1123 subjects). In the Three-City Study, increasing daily tea consumption was associated with a lower prevalence of carotid plaques in women: 44.0%, 42.5%, and 33.7% in women drinking no tea, 1 to 2 cups/d, and 3 cups/d (P=0.0001). This association was independent of age, center, major vascular risk factors, educational level, and dietary habits (adjOR=0.68[95%CI:0.54 to 0.86] for women drinking 3 cups/d compared with none). There was no association of tea consumption with carotid plaques in men, or CCA-IMT in both genders. In the EVA-Study, carotid plaque frequency was 18.8%, 18.5%, and 8.9% in women drinking no tea, 1 to 2 cups/d, and 3 cups/d (P=0.08).
Conclusion— In a large sample of elderly community subjects we showed for the first time that carotid plaques were less frequent with increasing tea consumption in women.
Our aim was to assess the relationship of tea consumption with common carotid artery intima-media thickness and carotid plaques in a large population-based sample of elderly subjects. Increasing daily tea consumption was associated with a lower prevalence of carotid plaques in women, independently of vascular risk factors and dietary habits.
Key Words: plaque • carotid arteries • atherosclerosis • intima-media thickness • tea
Tea is the second most widely used drink in the world.1 Because some of its constituents have antioxidant properties,2,3 there have been numerous studies on the relationship between tea consumption and several diseases, especially cancer4–7 and vascular disease.4,5,8–26 In particular, there is extensive literature on the association of tea consumption with coronary artery disease,8–13 myocardial infarction,14–18 stroke,19–22 and vascular death.4,5,9,14,15,18,23–26 Most studies found a negative association between these conditions and increasing tea consumption.4,5,10–13,16–18,20,21,24–26 Some however could not demonstrate any significant association8,9,14,19,22,23 and one study even demonstrated a positive association, suggesting a deleterious effect of tea consumption on coronary artery disease,15 although this relationship disappeared after multiple adjustment for other risk factors. A publication bias has been suggested, favoring results that show a protective effect of tea consumption.1 Furthermore, tea consumption being generally associated with a healthier lifestyle, it has been argued that the negative association that was observed in most studies may be attributable to selection bias. In addition, patients may have started drinking tea after a vascular event, because they thought it was healthier.
To our knowledge, until now no study has evaluated the relationship between tea consumption and carotid atherosclerosis. The latter can be assessed noninvasively, in asymptomatic subjects, therefore allowing population-based studies and avoiding the selection bias attributable to vascular events.
The aim of the present study was to assess the relationship between tea consumption and both common carotid artery intima-media thickness (CCA-IMT) and carotid plaques in a large French population-based study, the Three-City (3C) Study.27 We subsequently tested whether the results found in the 3C Study could be replicated in an independent and younger French population sample (EVA Study28).
Methods
The 3C Study is a 3-center prospective cohort study, whose design has been described in detail elsewhere.27 Briefly 9693 noninstitutionalized persons aged 65 years and over were recruited from the electoral rolls of three French cities (Bordeaux, Dijon, and Montpellier) between March 1999 and March 2001. Three-hundred ninety-nine persons were subsequently excluded, 7 because they were aged less than 65 years and 392 because they refused to participate in the interview. A baseline ultrasound examination of the carotid arteries was proposed to participants under the age of 85 who were able to come to the examination centers. Because of logistic concerns, the ultrasound examination was not offered to persons included during the last 4 months of subject recruitment. A baseline ultrasound examination of the carotid arteries was thus performed in 6635 subjects. After exclusion of subjects with missing data on tea consumption and carotid plaque characteristics the present study was performed on 6597 individuals. For technical reasons 168 subjects could not have CCA-IMT measures.
For the ultrasound examination, the B-mode system (Ultramark 9 High Definition Imaging) with a 5- to 10-MHz sounding was used at each of the 3 centers, and a centralized reading was performed according to a standardized protocol. The procedure has been described in detail elsewhere.29 The presence of plaques was defined as localized echo structures encroaching into the vessel lumen for which the distance between the media-adventitia interface and the internal side of the lesion was 1 mm, on the common carotid arteries, the carotid bifurcations and the internal carotid arteries. The IMT was measured at a site free of any discrete plaques along a 10-mm-long segment of the far wall of the common carotid artery (CCA) as the distance between the lumen-intima interface and the media-adventitia interface. On average, 75 measurements were automatically performed on each image and on each side, and a mean CCA-IMT value was computed for each side.30 The CCA-IMT value used in the analyses was a mean of right and left mean values.
Information about demographic background, medical history, and personal habits was collected during a face-to-face interview using a standardized questionnaire administered by trained nurses. Participants were asked to estimate their tea and coffee consumption in cups per day and their consumption of fish, meat, raw vegetables, baked fruit, or vegetables in meals per week. A general description of the dietary patterns of the sample has been published elsewhere.31 Educational level was separated into primary or short technical, secondary or long technical, and university level. History of vascular disease was defined as a history of hospitalization for stroke, myocardial infarction, coronary surgery or angioplasty, or surgery for peripheral artery disease, and women were asked in detail about previous or current hormone replacement therapy (HRT). Baseline blood pressure was measured twice in a sitting position using a digital tensiometer (OMRON M4). Centralized measurements of biological parameters were performed. Diabetes mellitus was defined as a fasting glucose level 7.0 mmol/L and/or an antidiabetic therapy. Hypertension was defined as a systolic blood pressure 160 mm Hg or a diastolic blood pressure 95 mm Hg or a blood pressure lowering therapy, hypercholesterolemia as a total cholesterol 7.25 mmol/L or a cholesterol lowering therapy. Body-mass index (BMI) was calculated as the ratio of weight (kg) to the square of height (m2).
The EVA study is another French prospective cohort study, whose design has been described in detail elsewhere.28 Briefly 1389 persons aged 59 to 71 years were recruited in the general population between June 1991 and July 1993. A baseline ultrasound examination of the carotid arteries was performed in 1384 subjects. After exclusion of subjects with missing data on tea consumption and carotid plaques characteristics, the present analysis was performed on 1123 subjects (661 women and 462 men). Carotid parameters and vascular risk factors were defined as previously published.28 There was no information on meat, fish, vegetable, and fruit consumption.
Data were analyzed with the SAS 8.02 software package (SAS Institute Inc). The main dependent variables, carotid plaques and CCA-IMT, were studied as a qualitative and a quantitative variable, respectively. For the statistical analyses tea consumption was divided into 3 groups: 3 cups per day, 1 to 2 cups per day, and none. The univariate and multivariable relationships of CCA-IMT and tea consumption categories were tested by analysis of variance and analysis of covariance. The univariate and multivariable relationships of carotid plaques and tea consumption categories were tested by chi-square test and logistic regression. Multivariable analyses were adjusted for center, age, BMI, smoking habits, hypertension, hypercholesterolemia, diabetes, history of vascular disease, alcohol consumption, educational level, coffee, meat, fish, raw fruit, raw vegetables, baked fruit, and vegetables consumption in the Three-City study. Alcohol and coffee consumption were studied as quantitative variables (in grams and cups per day, respectively); fish, meat, raw fruit, raw vegetables and baked fruit or vegetables consumption were studied as qualitative variables ( versus <2 times per week for fish consumption and versus <4 times per week for meat, fruit, and vegetable consumption). In the EVA study, multivariable analyses were adjusted for age, BMI, smoking habits, hypertension, hypercholesterolemia, diabetes, history of vascular disease, alcohol consumption, educational level, and coffee consumption. All the analyses were performed in men and women separately.
Results
The main characteristics of the Three-City Study population per gender and per category of tea consumption are presented in Tables 1 and 2
. Tea consumption was inversely associated with age, BMI, hypertension, diabetes, and smoking in women, with alcohol consumption in men, and with meat and coffee consumption in both genders (Table 1 and 2). Conversely, there was a positive association of tea consumption with a high educational level and with consumption of fish and baked fruit or vegetables in both genders and with hormone replacement therapy in women (Tables 1 and 2).
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Increasing daily tea consumption was associated with a lower prevalence of carotid plaques in women only in a univariate and multivariable model, but not with CCA-IMT (Table 3). The multivariable OR for carotid plaques in women drinking 3 cups of tea per day, compared with women drinking none, was similar when the variable hypertension was replaced by the systolic blood pressure value and the use of antihypertensive drugs (OR=0.68 [95%CI: 0.54 to 0.86]), when the variable hypercholesterolemia was replaced by LDL-cholesterol level, HDL-cholesterol level, and the use of cholesterol-lowering drugs (OR=0.69 [95%CI: 0.55 to 0.88]), when the variable diabetes was replaced by fasting glucose level (OR=0.68 [95%CI: 0.54 to 0.86]), and when all 3 variables were replaced at the same time (OR=0.69 [95%CI: 0.55 to 0.88]). After exclusion of subjects with a history of vascular disease the results were unchanged as well: multivariable OR=0.70 (95%CI: 0.56 to 0.89) for carotid plaques in women drinking 3 cups of tea per day compared with none. In women, the association of carotid plaques with tea consumption 3 cups per day was similar among current or former smokers (multivariable OR=0.47 [95%CI: 0.28 to 0.79]) and never smokers (multivariable OR=0.72 [95%CI: 0.55 to 0.94]). It was similar as well in women who had been taking a hormone replacement therapy (multivariable OR=0.77 [95%CI: 0.52 to 1.15]) and those who hadn’t (multivariable OR=0.63 [95%CI: 0.47 to 0.84]). The same inverse association of tea consumption with carotid plaques was found in other selected patient subgroups, such as women aged 
or >75 years, with a BMI or >27, with or without hypertension, with a primary or short technical versus secondary or university education, and with a raw fruit, raw vegetable and baked fruit, or vegetables consumption or <4/week, respectively. No significant interaction was noted (data not shown).
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The frequency of women consuming 3 cups of tea per day was 14.7%, 10.9%, and 9.7% among women with no plaque, 1 site with plaques, and 2 or more sites with plaques, whereas the frequency of women consuming no tea was 59.6%, 62.1%, and 65.4% among women with no plaque, 1 site with plaques, and 2 or more sites with plaques (P=0.0005).
There was no association of tea consumption with carotid plaques in men or with CCA-IMT in both genders (Table 3).
We subsequently tested whether similar results could be replicated in the EVA study.28 Briefly, 462 men (of whom 68 drank 1 to 2 and 11 drank 3 cups of tea per day) and 661 women (of whom 173 drank 1 to 2 and 79 drank 3 cups of tea per day) were studied. There was no association between tea consumption and carotid plaques or CCA-IMT in men and no association between tea consumption and CCA-IMT in women, but a trend toward a lower frequency of carotid plaques with increasing tea consumption was found in women (Table 4).
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Discussion
In a large sample of French elderly community subjects we found that carotid plaques were significantly less frequent with increasing tea consumption in women, in particular for a consumption of 3 cups per day. There was no association of tea consumption with carotid plaques in men and with CCA-IMT in both genders.
This is, to our knowledge, the first study on the association of tea consumption with carotid atherosclerosis. Its strengths are: (1) the large size of the sample, (2) the population-based setting, (3) the fact that the results remained unchanged after adjustment for several potential confounders in relation with lifestyle (such as smoking habits, coffee consumption, dietary habits, educational level) and after stratifying into different subpopulations. Furthermore, we were able to replicate a similar trend in the EVA study,28 a smaller, independent and younger, population sample.
The main limitation is that, even though we adjusted for a large number of lifestyle parameters, there may be some degree of residual confounding by socioeconomic status and nutritional habits. Indeed, tea consumption may also be an overall indicator of a general "healthy" dietary pattern and lifestyle as suggested by its association with a more favorable cardiovascular profile, which may not be fully taken into account by adjustment on the available covariates. Few people drank large amounts of tea (3 cups/day), compared with other countries,5 but this is mainly expected to reduce the power of the study. Similarly, we had no information on the duration of tea consumption, and the type of tea, but again, this measurement imprecision is also mostly expected to reduce statistical power. Another limitation is the cross-sectional design of the study, which makes the time-dependent relationship between high tea consumption and low frequency of carotid plaques uncertain. However, tea consumption modification as a consequence of the presence of carotid atherosclerosis is hardly plausible.
The fact that the inverse association between tea consumption and carotid plaques in women was unchanged after adjustment and stratification, and that we found a similar trend in another independent population, makes it quite unlikely that the association is only attributable to chance. Even though we cannot exclude some degree of residual confounding by lifestyle factors, our results suggest a protective effect of tea consumption on carotid plaque formation. This in line with experimental data, demonstrating that green tea ingestion reduces atherosclerotic plaque formation in cholesterol-fed rabbits.32 There are several hypotheses concerning the mechanisms underlying this potential protective effect. Some tea constituents, especially polyphenolic flavonoids, have antioxidant properties2,3 and were shown to inhibit LDL oxidation, a key event in early atherogenesis.33 Tea also has antithrombotic properties via inhibition of platelet agregation34,35 and was shown to improve endothelial function.36 More recently, antiinflammatory effects of tea were demonstrated, which may also contribute to a protective effect on atherosclerosis, the latter being now recognized as largely mediated by inflammation.37 Finally, tea consumption may have a favorable effect on vascular risk factors, such as antihyperlipidemic properties.38 In the present study, the results were unchanged after adjusting for and stratifying on hypercholesterolemia and diabetes, suggesting that this indirect mechanism played only a minor role in our populations.
The fact that we found an association of tea consumption with carotid plaques and not with CCA-IMT may reflect that carotid plaques represent a more advanced stage of atherosclerosis than elevated CCA-IMT. Interestingly, tea consumption was also found to be associated with a risk reduction for severe but not moderate or mild aortic atherosclerosis.39 Moreover, although it was shown to be an independent predictor of carotid plaque occurrence,28,40 elevated CCA-IMT may in some instances reflect nonatherosclerotic thickening, such as an adaptive response to altered shear stress on the arterial wall.41
Why tea consumption was associated with carotid plaques in women only is unclear. Although increasing tea consumption was significantly associated with a more favorable vascular risk profile in women than in men (Tables 1 and 2
), we believe this is unlikely to account entirely for the association of carotid plaques with tea consumption observed in women but not in men. Indeed, the results were unchanged after stratifying on or adjusting for several vascular risk factors. Noteworthy, results were still unchanged when systolic blood pressure, use of antihypertensive drugs, LDL-cholesterol level, HDL-cholesterol level, use of lipid-lowering drugs, and glucose level were used in the multivariable model instead of hypertension, hypercholesterolemia, and diabetes as defined in the methods section. Interestingly, 2 other studies also found an inverse association of tea consumption with severe aortic atherosclerosis in women only39 and a more prominent inverse association of cardiovascular and all-cause mortality with tea consumption in women compared with men.5 Besides, 3 studies9,14,22 that did not find any association of tea consumption with atherosclerosis were performed in men only. To explain this discrepancy between men and women, an estrogen-like activity of tea constituents has been suggested and a positive correlation of tea intake with serum prolactin concentration, considered as a bioassay for estrogenic activity, was demonstrated.42 Although we did not measure estrogen activity, our results were unchanged after adjustment for or stratification on HRT. Other authors have suggested a better bioavailability of quercetin (a tea flavonol with antioxidative properties) in women, especially in those using oral contraceptives.43 Alternatively, a confounding effect of smoking was suggested in the Ohsaki Study,5 based on the observation that men were more likely to smoke and that the inverse association of green tea consumption with cardiovascular mortality was more pronounced in subjects who had never smoked, even though there was no significant interaction. We did not observe such a difference between smokers and nonsmokers in the present study. Finally, because men drank less tea than women, we cannot exclude that an association of tea consumption with carotid plaques in men was missed because of insufficient statistical power. If such an association does exist, however, our results suggest that it is weak.
Our results are consistent with most studies that have assessed the relationship between tea consumption and either vascular events4,5,16–18,21,24–26 or aortic and coronary atherosclerosis,10–13,39 suggesting a protective effect of tea consumption. The only study that found a significant positive association between tea consumption and coronary morbidity and mortality, suggesting a deleterious effect of tea, was performed in the United Kingdom (UK),15 where tea drinking is associated with a lower social status and less healthy habits,1 as opposed to most other Western countries where tea consumption is related to a healthier lifestyle. The large size of our population, the robustness to adjustment for several potential confounders, including educational level and nutritional habits, and the fact that we replicated the same trend in an independent cohort, all suggest a true inverse association between tea consumption and carotid plaques in elderly French women. This lends support to previous results showing an inverse association between tea consumption and atherosclerosis or vascular event. Ideally, the causal relationship between tea consumption and reduced atherosclerosis ought to be confirmed in a randomized trial, but this poses a number of methodological challenges, such as the quantity and duration of tea consumption needed in the treatment arm. Besides, the feasibility and acceptability of such a trial is questionable.
In conclusion, we described for the first time an inverse association between carotid plaques and tea consumption in elderly women from the French general population. This may suggest a protective effect of tea consumption on carotid atherosclerosis in elderly women, but further studies are warranted to confirm this and improve our understanding of the underlying mechanisms.
Acknowledgments
Sources of Funding
The 3C Study has been conducted under a partnership agreement between the Institut National de la Santé et de la Recherche Médicale (INSERM), the Victor Segalen – Bordeaux II University, and Sanofi-Aventis. The Fondation pour la Recherche Médicale funded the preparation and initiation of the study. The 3C-Study is also supported by the Caisse Nationale Maladie des Travailleurs Salariés, Direction Générale de la Santé, MGEN, Institut de la Longévité, Conseils Régionaux of Aquitaine and Bourgogne, Fondation de France, the Institut de Santé Publique, d’Épidémiologie et de Développement (ISPED, Bordeaux), Ministry of Research - INSERM Programme "Cohortes et collections de données biologiques". Mahmoud Zureik was a recipient of a "Contrat d’Interface" grant from INSERM - Centre Hospitalier Universitaire de Lille.
Disclosures
None.
Footnotes
Original received July 17, 2007; final version accepted November 16, 2007.
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