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Carcinogenesis Advance Access originally published online on December 20, 2006
Carcinogenesis 2007 28(5):1074-1078; doi:10.1093/carcin/bgl252
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© The Author 2006. Published by Oxford University Press. All rights reserved. For Permissions, please email: journals.permissions@oxfordjournals.org

Green tea and the prevention of breast cancer: a case–control study in Southeast China

Min Zhang*, C. D'Arcy J. Holman, Jiang-ping Huang1 and Xing Xie1

The School of Population Health, The University of Western Australia, 35 Stirling Highway, Crawley, Perth, WA 6009, Australia
1 Women's Hospital, School of Medicine, Zhejiang University, Hangzhou, P. R. China

* To whom correspondence should be addressed. Tel: + 61 8 6488 8175; Fax: + 61 8 6488 1188; Email: min.zhang{at}uwa.edu.au


   Abstract
Top
 Abstract
Introduction
 Materials and methods
 Results
 Discussion
 References
 
Breast cancer is the most common malignancy in women worldwide. Tea has anticarcinogenic effects against breast cancer in experimental studies. However, epidemiologic evidence that tea protects against breast cancer has been inconsistent. A case–control study was conducted in Southeast China between 2004 and 2005. The incidence cases were 1009 female patients aged 20–87 years with histologically confirmed breast cancer. The 1009 age-matched controls were healthy women randomly recruited from breast disease clinics. Information on duration, frequency, quantity, preparation, type of tea consumption, diet and lifestyle were collected by face-to-face interview using a validated and reliable questionnaire. Conditional logistic regression analyses were used to estimate odds ratios (ORs) and associated 95% confidence intervals. Compared with non-tea drinkers, green tea drinkers tended to reside in urban, have better education and have higher consumption of coffee, alcohol, soy, vegetables and fruits. After adjusting established and potential confounders, green tea consumption was associated with a reduced risk of breast cancer. The ORs were 0.87 (0.73–1.04) in women consuming 1–249 g of dried green tea leaves per annum, 0.68 (0.54–0.86) for 250–499 g per annum, 0.59 (0.45–0.77) for 500–749 g per annum and 0.61 (0.48–0.78) for ≥750 g per annum, with a statistically significant test for trend (P < 0.001). Similar dose–response relationships were observed for duration of drinking green tea, number of cups consumed and new batches prepared per day. We conclude that regular consumption of green tea can protect against breast cancer. More research to closely examine the relationship between tea consumption and breast cancer risk is warranted.

Abbreviations: OR, odds ratio; weekly MET-hour, weekly metabolic equivalent task hour


   Introduction
Top
 Abstract
 Introduction
Materials and methods
 Results
 Discussion
 References
 
Breast cancer is the most common malignancy in women in the world and its rate is increasing in both developed and developing countries (1). There are profound geographic differences in the incidence rates of breast cancer. The rate in China is 18.7 per 100 000 women-years, which is 4- to 5-fold lower than rates typically found in developed countries (2). However, the rate of breast cancer increased by 50.5% from 1972 to 1994 in the now relatively affluent southeast of China (3).

Tea polyphenols, particularly green tea polyphenols, have been shown to possess anticarcinogenic effects against breast cancer in experimental models, both in vitro and in vivo (4–6). However, epidemiologic data, arising mainly from Western populations, are not supportive of a protective role of tea in the prevention of breast cancer (7–11). Most of the studies yielding null results were conducted in Western populations that consumed exclusively black tea (12). The results of human studies on the relationship between green tea and breast cancer risk have been inconsistent. Two case–control studies, conducted on Asian Americans and Chinese women in Singapore, found that green tea reduced the risk of breast cancer (13,14), whereas three cohort studies from Japan reported no association between green tea and breast cancer risk (15–17).

Tea is a natural and historic beverage, consumed worldwide although at greatly varying levels (18). There are three types of tea with different types and concentration of polyphenols. Green tea is prepared in such a way as to preclude the oxidation of green leaf polyphenols. During black tea production, oxidation is promoted so that most of these substances are oxidized. Oolong tea is a partially oxidized product (19). In Western countries, the dominated type of tea consumed is black tea. Green tea, which is the main tea beverage in Japan and many parts of China, accounts for ~20% of worldwide tea production, whereas <2% of tea production is oolong tea, consumed mainly in southern China and Taiwan (20). Tea is now grown in ~30 countries, but geologic and botanic evidence suggest that the tea plant originated from China (18). As one of the most ancient and commonest beverages, tea has been consumed for thousand years in the orient and plays a central part in Chinese culture, with tea-drinking practices specific to different areas including the southeastern region of China.

In view of the variations in rates of breast cancer and tea-drinking practices, our case–control study was conducted in Southeast China to evaluate the association between breast cancer and tea consumption measured by type, duration, frequency and quantity of tea and the interactions between tea consumption and other lifestyle factors.


   Materials and methods
Top
 Abstract
 Introduction
 Materials and methods
Results
 Discussion
 References
 
A hospital-based case–control study of breast cancer risk was conducted in Hangzhou, the capital city of Zhejiang Province, during July 2004 and September 2005. All participants were Chinese women resident in Zhejiang Province and aged between 20 and 87 years. Cases were identified from medical records in four teaching hospitals of the School of Medicine, Zhejiang University. All the participating hospitals were public hospitals with 500–2000 beds and received patients from all over the province. A total of 1009 female patients, who newly diagnosed with invasive ductal carcinomas or in situ carcinoma of the breast, were recruited to the study. All diagnoses were histopathologically confirmed after surgery. The patients were excluded if breast cancer was neither the primary nor the final diagnosis. All relevant hospital and laboratory pathology reports were reviewed daily to ensure the completion of recruitment. The proportion of lost or non-responding patients among the cases was 1.2%. During the same period of data collection, 1009 healthy women were selected consecutively in the participating hospitals as controls to match each case's age within 5 year age group using a daily update of the list of cases. Each control was recruited as the first in the matched age group to attend the outpatient breast clinics and who consented to participate. The proportion of participation by selected controls was 98.7%. Potential control women were excluded if they had a previous diagnosis of either breast cancer or another malignant disease. The project received ethics clearance from both the Human Research Ethics Committee of The University of Western Australia and the Chinese hospital authorities.

Subjects were briefed regarding the general aims of the study to investigate lifestyle factors, confidentiality, and anonymity issues. An appointment for interview was made after obtaining their consent via an initial contact. A face-to-face interview was conducted in the hospital setting using a structured questionnaire and usually took 30–40 min. The cases were interviewed in breast surgery wards, most of them (91.6%) within 3 months after diagnosis, whereas the controls were interviewed in the outpatient clinic of the same hospital. A validated and reliable questionnaire was used to collect the information on (i) demographic and lifestyle characteristics, e.g. residential area, education and physical activity; (ii) tea consumption; (iii) food consumption assessed by a 100-item food frequency questionnaire and (iv) factors relevant to hormonal status, including menstrual history and menopausal status, reproductive and lactation history, oral contraceptive use, benign proliferation breast disease and family history of breast cancer. The cutoff date for dietary intake and physical activity was set as 1 year prior to diagnosis (cases) or interview (controls). If there was any change in their habits recently, only information on the habits before the change was used in data analysis. The reproducibility of the food frequency questionnaire has been assessed in a test–retest study, and intraclass correlation coefficients for the intake of total energy, alcohol, soybean, vegetables and fruits were 0.84, 0.88, 0.78, 0.75 and 0.88, respectively (21). The questionnaire was translated into Chinese and checked (back-translated) by professional Chinese translators. After interview, an anthropometric measurement was requested of all participants.

Tea consumption was measured using a tea questionnaire adapted from our previous studies (22,23). The reproducibility of the tea questionnaire has been evaluated and the intraclass correlation coefficient was 0.83 for tea consumption (21). This high coefficient for test–retest reliability suggested that the questionnaire may be relied upon in assessing tea consumption. This self-reported instrument was used to assess tea consumption by several methods. The participants were first classified as either ‘never’ or ‘ever’ tea drinkers in their lives. Information was then sought from all ‘ever’ drinkers on their consumption patterns, namely, preparation method, type of tea drank, duration of each type of tea drinking, usual frequency of cups consumed (counting the number of 350–400 ml cups, the typical teacup used by Zhejiang residents), frequency of new batches of tea brewed, quantity of dried tea-leaf consumed per year and date that tea drinking ceased. The frequency of cups and number of new batch of tea consumed were categorized as never or seldom, once a month, 2–3 times a month, once a week, 2–3 times a week, 4–6 times a week, once a day, 2–3 times a day and ≥4 times a day. For infrequent tea drinkers and those drinking less than one cup at a time, the actual tea consumption was recorded. The quantity of dried tea leaves consumed per year was also requested in terms of a standard Chinese measure, the liang (equivalent to 50 g).

All data were checked for completeness at the end of each interview. The data were coded and analyzed using the SPSS version 11.0. Data collected by different interviewers were compared and confirmed no consistent difference in recording of key variables such as tea consumption within cases or controls. The tea consumption variables were grouped into three or four categories to facilitate analysis with non-tea drinkers as reference group. Physical activity was expressed in terms of weekly metabolic equivalent task hour (weekly MET-hour) following previous studies (24). MET scores 6, 4.5 and 2.5 were assigned, respectively, for vigorous, moderate and walking activity based on a compendium of physical activities (25). Total energy intake was estimated using Chinese Food Composition Tables (26). Soy intake was expressed in terms of total isoflavone intake (mg isoflavones/1000 kcal). Intake of isoflavones was calculated from soy food items using a USDA nutrient database, which had been developed specifically for Chinese immigrants in America (27).

Demographic characteristics and potential risk factors between cases and controls, and selected characteristics in tea drinkers and non-drinkers were compared using a t-test for continuous variables and chi-square test for categorical variables. We analyzed the data using both conditional logistic regression on available matched pairs and unconditional logistic regression with the ‘formal’ matching factor of 5 year age group as a stratifying variable. There was no practical difference in the results, but as there was also a degree of ‘operational’ matching on other factors, we believe that the conditional analysis results to be the one best justified by the circumstances of our study. Odds ratios (ORs), 95% confidence intervals and P values for potential risk factors were estimated to take account of the matching arrangement within 5 year age intervals. Univariate analysis was undertaken to screen potential explanatory variables for subsequent multivariate analysis. We firstly evaluated the association between tea consumption and breast cancer risk, adjusting for residential area, education, body mass index (calculated as the current weight in kilograms divided by square of height in meters), age at menarche, number of children breastfed, menopausal status, oral contraceptive use, hormone replacement therapy, biopsy-confirmed benign breast diseases, family history of breast cancer and total energy intake. We further assessed the effect of tea on breast cancer risk by including additional terms for passive smoking, alcohol and coffee consumption, physical activity, and intake of soy, vegetables, and fruits. These variables were included in the models because they emerged either as significant risk factors for breast cancer in previous studies (13,14,28) or as potential confounders associated to green tea drinking based on comparison test or the univariate analysis. Each quantitative or ordinal measure of tea consumption was subjected to a linear trend test. The proportion of in situ carcinoma was only 3% of all breast cancer patients in the study, which may reflect the fact that early detection programs such as mammographic screening were not prevalent in China during the study period. Such a small number of in situ carcinoma patients made it impracticable to study them separately. The study only focuses on green tea due to few tea drinkers drank black or oolong tea.


   Results
Top
 Abstract
 Introduction
 Materials and methods
 Results
Discussion
 References
 
Selected characteristics of subjects with and without breast cancer are shown in Table I. There was no difference between cases and controls in residential area, education, menopausal status, number of delivery of full-term pregnancy, number of children breastfed, tobacco smoking, alcohol and coffee consumption, physical activity in terms of weekly MET-hour and body mass index. Compared with controls, the breast cancer cases tended to have less oral contraceptive use and hormone replacement therapy, lower consumption of soy, vegetables and fruits, but more of them were exposed to passive smoking, menarche age before 13 years, biopsy-confirmed benign breast diseases, breast cancer in the first-degree relatives and higher energy intake. In particular, only 44.7% of the cases were classified as tea drinkers compared with 65.5% of the controls. Among all the tea drinkers, 89% drank green tea only, 4.9% black tea only, 0.3% oolong tea only and 5.8% both green and black tea.


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  		Table I. Selected characteristics of subjects with and without breast cancer

 
Selected characteristics between green tea drinkers and non-tea drinkers are presented in Table II. Compared with non-tea drinkers, green tea drinkers tended to reside in urban, have better education and have higher consumption of coffee, alcohol, soy, vegetables and fruits. There is no significant difference between green tea drinkers and non-tea drinkers with respect to menarche age before 13 years, menopausal status, tobacco smoking, passive smoking, physical activity (weekly MET-hour), body mass index and energy intake.


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  		Table II. Selected characteristics between green tea drinkers and non-tea drinkers

 
Table III reports the adjusted ORs and associated 95% confidence intervals for green tea consumption measures. The risk of breast cancer declined with increasing quantity, duration and frequency of green tea consumed. In the final models, compared with non-tea drinkers, the adjusted ORs were 0.87 (0.73–1.04) in women consuming 1–249 g of dried green tea leaves per annum, 0.68 (0.54–0.86) for 250–499 g per annum, 0.59 (0.45–0.77) for 500–749 g per annum and 0.61 (0.48–0.78) for ≥750 g per annum, with a statistically significant test for trend (P < 0.001). The adjusted ORs were 0.66 (0.56–0.78), 0.57 (0.47–0.69) and 0.59 (0.41–0.84) in those who consumed green tea ≥20 years, ≥2 cups a day, and ≥2 new batches a day, respectively. A significant inverse dose–response relationship between green tea consumption and breast cancer risk was observed across all the measurements.


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  		Table III. Associations between green tea consumption and breast cancer risk in Chinese women

 

   Discussion
Top
 Abstract
 Introduction
 Materials and methods
 Results
 Discussion
References
 
This case–control study conducted in Southeast China was specifically designed to evaluate the hypothesis that green tea consumption affects breast cancer risk and to assess potential confounders of green tea consumption. Although a number of studies have investigated the effect of green tea on risk of breast cancer, few have examined green tea exposure base on a comprehensive set of measures of duration, frequency, preparation and weight of tea consumed. Our results in Chinese women suggest that increasing duration, frequency and quantity of green tea consumed was inversely associated with breast cancer risk in a significant dose–response relationship.

This study provided evidence that green tea consumption is associated with a reduced risk of breast cancer. Many studies have documented that the incidence rate of breast cancer has been increasing over the past three decades in most countries including China (1–3). Compared with an earlier sample of women drawn from the same area of Southeast China in 1999–2000 (22), the prevalence of tea consumption in controls in the present study had decreased by ~10%. This correlated with an increased incidence rate of breast cancer in the same population (3). It seems probably that changes in lifestyle, including a trend away from the tradition of drinking green tea, are playing a role in the movement of breast cancer rates in China toward those of Western countries.

Our findings are consistent with the evidence from experimental studies. Tea, one of the most frequently consumed beverages worldwide, and other possible cancer-preventive agents have been the object of substantial interest over the last three decades. Laboratory studies based on in vitro and in vivo models have consistently demonstrated anticarcinogenic effects of tea polyphenols against breast cancer (4–6). In contrast, the previous epidemiologic evidence has been inconclusive (7–11,13–17). The study found that green tea protects against breast cancer. Our finding may elaborate on the inconclusive evidence on tea and breast cancer in previous studies, since most of the studies yielding null results were conducted in Western populations that consumed exclusively black tea (12). The inconsistent outcomes from epidemiological studies may be explained in part by variations in exposure levels to tea and other risk factors for breast cancer across study populations (10). Lack of detailed information on tea exposure or lack of control of potential confounding factors may also limit the conclusions drawn from previous observational studies. It is important to identify the potential confounders of green tea consumption in the study population. Our study found that green tea drinkers were more probably than non-tea drinkers to reside in urban, have better education and have higher consumption of coffee, alcohol, soy, vegetables and fruits. Thus, any residual confounding from these lifestyle factors would have affected the apparent protective effect of green tea.

Since the finding that green tea has a protective effect on breast cancer has important implications, it is necessary to emphasis our study's limitations and strengths. A feature of the study was that extensive information was obtained on tea consumption as well as diet, lifestyle and factors relevant to hormonal status. A validated and reliable instrument specifically for Chinese women was used to collect this information. Nevertheless, the case–control design may have introduced certain sources of bias. The breast canner cases were identified from medical records and interviewed in breast surgery wards, while the controls were randomly selected from outpatient clinics in the same hospitals by matching on the age of cases. The majority of patients are self-referred in China. Under the recruitment procedure, the cases and controls arose from the same populations of women using the hospitals and, thus, if a control was later to develop breast cancer it was highly probably that she would have been treated in the same hospital. Selection bias was also minimized by a selection for controls that was unrelated to convenience or clinician contact. Our research interest in any type of tea consumption (not specifically green tea) and breast cancer was revealed at the time of the interview to explain why the questions on tea were so detailed. However, in assessing the likelihood of any information bias, which we consider to have been low, it was relevant that no mention occurred in popular media of any association between tea consumption and breast cancer prior to and at the time of the research. Although tea consumption, like other personal habits, can be reported by the subjects with reasonable accuracy, misclassification of exposure may still exist. However, such random errors are probably to bias results toward the null and could not account for the strongly inverse associations reported here. Exposure of cases to risk factors may change due to disease status. However, >90% cases were newly diagnosed and interviewed within 3 months. It appears unlikely that disease status materially affected the interview responses and the notion that cases would have either recalled more tea drinking or dramatically increased their tea drinking is implausible.

The bioavailability of tea polyphenols from the method of preparation in Southeast China has been documented in the literature (29,30). The first two cups brewed from each new batch contain almost equal amounts of epigallocatechin gallate (the main active constituent of tea polyphenols), but its level can be substantially decreased in the third cup. It has been reported that 69–85% of the total antioxidant in tea leave enter liquid tea within 5 min of brewing. Additional antioxidants become soluble with a second brewing for an additional 5 min (18). Drinking tea slowly has been suggested as an effective way of delivering tea catechin (31). Although tea polyphenols can be distributed from the digestive tract to various organs, including the mammary gland tissue in animal experiments (32), only hot but not iced black tea consumption was associated with a significantly lower risk of skin cancer (33), suggesting that the protective effects of tea can be influenced by the method of preparation.

Our result is consistent with two case–control studies in Asian Americans and Chinese women in Singapore (13,14), but three cohort studies from Japan, where green tea drinking is ubiquitous, have reported that green tea was not associated to breast cancer risk (15–17). However, another cohort study in a Japanese population found green tea consumption was associated with a reduction in general cancer mortality and a later onset of cancer at all sites (34). Although green tea is the main type of tea consumed in both Japan and Southeast China, there are some important differences in the prevalence and levels of its exposure. In our study, level of tea exposure varied greatly in the study population. Because of this we were able to designate non-tea drinkers as the reference group, which included 55.3% of cases and 35.5% of controls. The Japanese studies suffered from a lack of unexposed subjects such that only 2% of the subjects were non-drinkers of green tea. Therefore, the effect on risk of breast cancer was estimated using daily consumption of <1 cup as a reference group. This may have reduced the extent of exposure contrast and the capacity of the Japanese studies to detect any sizeable effect.

In conclusion, the study suggests that increasing duration, frequency and quantity of green tea consumption reduce the risk of breast cancer in Chinese women. It follows that increased consumption of green tea in women with little or no consumption could protect against breast cancer development. This finding has biological plausibility, being supported by strong evidence of tumor-inhibitory effects of green tea in animal studies and other in vitro and in vivo experiments. It also provides an explanation of one of the factors that may account for the low but increasing incidence rate of breast cancer in China. More research to closely examine the relationship between tea consumption and breast cancer risk is warranted.


   Acknowledgments
 
The authors acknowledge with gratitude the participation of the Chinese women as subjects. We are grateful for the collaboration received from the participating hospitals and their staff. The first author is supported through a postdoctoral fellowship from the National Health and Medical Research Council (Australia, ID 303292).


   References
Top
 Abstract
 Introduction
 Materials and methods
 Results
 Discussion
 References
 

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Received July 7, 2006; revised October 9, 2006; accepted December 15, 2006.


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