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© 2003 The American Society for Nutritional Sciences J. Nutr. 133:3310S-3318S, October 2003

Supplement: Proceedings of the Third International Scientific Symposium on Tea and Human Health

The Epidemiology of Tea Consumption and Colorectal Cancer Incidence1

Lenore Arab*,2 and Dora Il’yasova{dagger}

* Department of Epidemiology, University of North Carolina at Chapel Hill, Chapel Hill, NC; and {dagger} Department of Cancer Biology, Wake Forest University School of Medicine, Winston-Salem, NC

2To whom correspondence should be addressed. E-mail: Lenore{at}unc.edu.


   ABSTRACT
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 ABSTRACT
Literature search
 RESULTS
 DISCUSSION
 LITERATURE CITED
 
This manuscript provides a brief synopsis of 30 studies aimed at examining tea consumption as a factor in the incidence of colon and rectal cancers. The 30 papers examine populations in 12 countries and provide data on consumption of both black and green tea. These studies do not provide consistent evidence to support the theory from animal studies and basic research that tea is a potent chemopreventive agent. Details of the studies are presented, and the potential impact of measurement error, publication bias, the form of tea consumed, the appropriateness of the outcomes studied and the adjustment of confounders related to both tea consumption and risk of colorectal cancer or polyps in various countries are explored. In general, the data are not more consistent for green than for black tea. Particularly with green tea, the doses consumed do get into a perceived protective range in a significant subset of the population. A negative association is stronger in observational epidemiologic studies of rectal cancer than in colon cancer. There is no consistent adjustment for important potential confounders of any tea relationship, such as coffee and alcohol consumption and physical activity levels. Finally, the assessment of tea in most of these studies was based on a single question and therefore may have significant measurement error compared with more recent studies specifically aimed at assessing tea consumption.

KEY WORDS: • epidemiology • tea • colon • rectal • cancer

The first publication on tea and cancer registered by MEDLINE described carcinogenic activity of tea (1). The first report of epidemiologic results were unadjusted and showed no effect or a tendency towards increased risk at lower intake levels between tea drinking and colorectal cancer in Kansas, MO (2). This supports the concept of biased publication of findings that demonstrate and reinforce popular beliefs. The main hypothesis driving research at that time was that tea drinking had a harmful effect. All three caffeine-rich foods: tea, coffee and chocolate were considered carcinogenic in 1970s and 1980s (3–5). However, in the1990s the hypothesis was reversed and the anticarcinogenic potentials of tea were studied. This change of heart in the hypothesis originated from the experimental research started in mid-1980s (6) and continues until the present (7).

The basic scientific evidence of tea’s anticarcinogenic effect is building, and the resulting treatment recommendations, used alone or combined, should reduce cancer risk at a number of sites. This has not been supported by a powerful clinical trial, and therefore, the foundation for an effect in man rests on the observational epidemiologic research. However, the human epidemiologic studies do not at first glance provide consistent evidence supporting the realization of this potential. The thrust of this review is to examine the consistency of the effect of tea on colon cancer, rectal cancer or the formation of the premalignant lesion of colonic polyp formation in epidemiologic studies.


   Literature search
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 LITERATURE CITED
 
We conducted a literature search (MEDLINE, 1966–2002, October 31) using a combination of the following keywords: tea and colon, rectal, colorectal, large bowel, cecum or large intestine. We excluded the ecological studies (8–10) from the current review. Among the identified observational studies, four Italian case-control analyses were excluded (11–14), because they represented successive publications of an ongoing study and were later incorporated into a cumulative analysis (15). One study, conducted in Belgium (16), was also excluded from this review because the reported relative risk (RR) estimates were related to tea and coffee intake combined. The results from the publications are organized by outcome: colon cancer (Table 1), rectal cancer (Table 2); combined outcomes: colorectal cancer (Table 3), and polyps (Table 4). The majority of the publications presented more than one estimate of the RR associated with different outcomes and/or stratified by gender.


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  		TABLE 1 Colon cancer

 

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  		TABLE 2 Rectal cancer

 

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  		TABLE 3 Colorectal cancer

 

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  		TABLE 4 Colorectal polyps

 

   RESULTS
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 LITERATURE CITED
 
The geography of epidemiologic studies of the association between tea and colorectal cancer includes Asia, Europe, and the Americas, with evidence from a total of 12 countries derived from 30 publications. The data in Table 1 on colon cancer present risk estimates from 19 studies, 7 of which are cohorts. Only two of the studies show a consistent dose-response negative relationship between tea consumption and colon cancer occurrence. They were the studies of Ji in China (21) and the British cohort results of Kinlen et al (41). Overall, no consistent effect was noted. The studies were controlled for age and gender in all cases. In addition, many controlled for physical activity, fiber and BMI. A number of studies examined other foods. Nine of the studies used daily consumption or consumption at all in comparison with nonconsumption for risk estimation. The range of effects is presented in Figure 1.



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  		FIGURE 1 Colon cancer. The studies are presented in the sequence as follows; units of contrast for the upper quanitle are presented. Kinlen 1998, 7–9 cups/d; Su 2002, <1.5 cups/d; Su 2002, >1.5 cups/d; Fredrikson 1995, >2 cups/d; Kata 1990, (green) daily; Inoue 1998, (green) occasional; Inoue 1998, (green) 1–3 cups/d; Ji 1997, (women) >200 g/mo; Kinlen 1998, >10 cups/d; Goldbohm 1996, (women) >5 cups/d; Cerhan 2001, <5.0 cups/d; Zheng 1996, >2 cups/d; Terry 2001, >2 cups/d; Goldbohm 1996, (women) 1 cup/d; Inoue 1998, (green) 4–6 cups/d; Inoue 1998, (green) >7 cups/d; Arts 2002, 1st quintile; Ji 1997, (men) >300 g/mo; Ji 1997, (women) 1–200 g/mo; Goldbohm 1996, (women) 4 cups/d; Kinlen 1998, 4–6 cups/d; Arts 2002, 2nd quintile; Goldbohm 1996, (men) 2 cups/d; Ji 1997, (men) 200–299 g/mo; Goldbohm 1996, (women) 3 cups/d; Arts 2002, 3rd quintile; Terry 2001, 1–6 cups/wk; Arts 2002, 4th quintile; Baron 1994, >1 cup/d; Tajima 1985, (green) >4 times/d; Slattery 1999, >1 cup/d; Nagano 2001, 2–4 times/d; Nagano 2001, 2->5 times/d; Kinlen 1998, 0–3 cups/d; Goldbohm 1996, (men) >5 cups/d; Goldbohm 1996, (women) 2 cups/d; Baron 1994, >10 cup/d; Goldbohm 1996, (men) 3 cups/d; Zheng 1996, weekly; Slattery 1999, <1 cup/d; Zheng 1996, 1 cup/d; Cerhan 2001, <3.1 cups/d; Terry 2001, 1 cup/d; Woolcott 2002, 3–4 cups/d; Woolcott 2002, >5 cups/d; Ji 1997, (men) 1–199 g/mo; Goldbohm 1996, (men) 3 cups/d; Woolcott 2002, 1–2 cups/d; Inoue 1998, (black) occasional; Tavani 1997, (yes); Cerhan 2001, 3.1–5.0 cups/d; Hartman 1998, <1 cup/d; Goldbohm 1996, (men) 1 cup/d; Inoue 1998, (black) daily; Tajima 1985, (black) yes; Hartman 1998, >1 cup/d; Yoshida 1992, (men) daily; Kata 1990, (black) daily; Yoshida 1992, (women) daily.

 
Rectal cancer results were more suggestive of potential prevention in some populations (Fig. 2). In six studies there seemed to be an indication of a reduction in risk with regular consumption. However, there were a number of studies that showed higher risk among tea consumers in case control as well as cohort designs, and among high consuming populations.



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  		FIGURE 2 Rectal cancer. The studies are presented in the sequence as follows; units of contrast for the upper quanitle are presented. Kato 1990, (black) daily; Arts 2002, 4th quintile; Ill’yasova (in press), (women) >160 g/mo; Kinlen 1998, 0–3 cups/d; Ill’yasova (in press), (women) 80–160 g/mo; Ji 1997, (women) 1–200 g/mo; Arts 2002, 2nd quintile; Baron 1994, >1 cup/d; Ji 1997, (women) >200 g/mo; Ill’yasova (in press), (men) 80–160 g/mo; Goldbohm 1996, (women) 2 cups/d; Goldbohm 1996, (women) 1 cup/d; Arts 2002, 3rd quintile; Ji 1997, (men) 200–299 g/mo; Zheng 1996, >2 cups/d; Goldbohm 1996, (women) >5 cups/d; Ji 1997, (men) >300 g/mo; Goldbohm 1996, (women) 3 cups/d; Goldbohm 1996, (men) 2 cups/d; Kinlen 1998, 7–9 cups/d; Ill’yasova (in press), (men) >160 g/mo; Goldbohm 1996, (men) 3 cups/d; Zheng 1996, 1 cup/d; Goldbohm 1996, (women) 4 cups/d; Hartman 1998, >1 cup/d; Zheng 1996, weekly; Cerhan 2001, <3.1cups/d; Kinlen 1998, 4–6 cups/d; Kinlen 1998, >10 cups/d; Tajima 1985, (green) >4 times/d; Tajima 1985, (black) yes; Ji 1997, (men) 1–199 g/mo; Cerhan 2001, <5.0 cups/d; Heilbrun 1986, almost never; Hartman 1998, <1 cup/d; Inoue 1998, (green) 1–3 cups/d; Goldbohm 1996, (men) 4 cups/d; Goldbohm 1996, (men) 1 cup/d; Baron 1994, >10 cup/d; Woolcott 2002, 1–2 cups/d; Woolcott 2002, >5 cups/d; Tavani 1997, (yes); Inoue 1998, (black) daily; Woolcott 2002, 3–4 cups/d; Inoue 1998, (green) >7 cups/d; Inoue 1998, (black) occasional; Nagano 2001, 2–4 times/d; Nagano 2001, 2->5 times/d; Heilbrun 1986, <twice/wk; Kato 1990, (green) daily; Terry 2001, 1–6 cups/wk; Cerhan 2001, 3.1–5.0 cups/d; Inoue 1998, (green) occasional; Inoue 1998, (green) 4–6 cups/d; Goldbohm 1996, (men) >5 cups/d; Terry 2001, >2 cups/d; Yoshida 1992, (men) daily; Heilbrun 1986, 2–4 times/wk; Heilbrun 1986, daily; Heilbrun 1986, >once/d; Yoshida 1992, (women) daily.

 
Eleven studies combined colon and rectal cancer cases and reported a single risk estimate across both. These tended to be studies with weaker designs and less control for potential confounders in their analyses.

Four studies, including one cohort and three population-based case control studies, published risk ratios for recurrence or prevalence of colonic polyps as a function of tea consumption. Two of these were in Japanese populations, one Danish and one American. Both of the Japanese studies suggested protective associations, neither of the other two did. Both of the Japanese studies were prevalence based however, which might lead to biased findings.


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Camelia sinensis is the plant whose leaves are used to brew tea. There are many types of tea, and they differ in their ingredient profile. Aside from cultivar differences, the differences are largely due to the extent to which enzymatic processes are halted within the tea leaf, resulting in green tea, or left to proceed to form oolong and black teas. The primary antioxidant potential of tea is attributed to its catechins, chief among them, epigallocatechin gallate, which is richest in green tea. Although both green and black tea were studied in the epidemiologic studies, there were geographic biases with most of the studies on green tea conducted in China and Japan (17–23). The relationship between black tea and colorectal cancer was examined in European countries (Denmark, Finland, Italy, the Netherlands, Russia, Sweden, the UK), in Americas (Argentina, Canada, US), and in Japan (Tables 1, 2, 3, 4). Black tea is the major hot beverage in the UK and Russia, and green tea in Japan and China. The studies’ findings did not, however, coalesce around the type of tea, as many protective studies were conducted on black tea consuming populations as on green tea consumers. Iced black tea is in many parts of the US the most frequently consumed form of tea. This is especially true of the South. There is evidence that the preventive agents in tea may precipitate out in the cold form of the beverage. They are reduced or lost in decaffeinated products, which is less of a problem because its use is less frequent. This phenomenon would however result in an overestimation of exposure.

Animal experiments suggest that the effective chemopreventive dose exceeds four cups per day. In the epidemiologic literature, Japanese studies often showed the power to study this dose with most studies showing three or four different categories ranging to five or more cups per day. Although black tea is also studied in a number of the Japanese publications, the unit of measure is generally consumption, yes or no, with the highest consumption category being "daily" or "consumers" (Tables 1, 2, 3, 4). This is much less frequent than the extreme used for green tea comparisons. The Scandinavian countries generally compared drinking one or more cups per day with none or less than one. Italy and Argentina also showed the highest levels of black tea consumption being limited to one cup per day at most (15,25). Italians and Scandinavians traditionally drink coffee and in Argentina, "mate" (Ilex Paraguariensis or Ilex Paraguensis), a form of tea made from South American evergreen or holly plants, is a traditional beverage. The dose of tea should have been adequate to see an effect in the larger studies in many of the populations. The general lack of effect, if not due to an inadequate dose, could be related to measurement error or lack of appropriate control for confounding factors.

Another concern is that tea consumption in countries that traditionally consume coffee may reflect noncoffee consumption, and the effect attributed to tea may be in fact due to the absence of coffee or reasons dictating that choice. Although there is no need to adjust for this in the Asian studies, few of the US or European studies, where coffee consumption predominates, did adjust for coffee consumption.

A few other potential confounding factors should be carefully examined in studies of tea and colon or rectal cancer. The most significant factors that might reasonably confound a tea association with colon or rectal cancer are socioeconomic status, BMI and the dietary profile aside from tea usage and alcohol consumption. Most studies did control for BMI, age and gender. Few of them addressed economic status, and those few used education as a surrogate for socioeconomic status. Other foods, which may be associated with both tea usage and colorectal cancer risk, also should be considered confounders, depending upon the population. These have not been consistently considered, but across the studies in individual cases, fruit and vegetable intake, fiber intake from all sources or from fruit, vegetables and cereal separately considered, calcium, vitamin C, vitamin D and folic acid as well as total caloric intakes were included in the adjustments. This makes cross comparisons of studies difficult because different subsets were used.

Genetic polymorphisms may also impact findings in as much as they affect the metabolism of active ingredients in tea. Nonstratification of such subsets may mask a strong effect in a subset of the population.

Until the mid-1990s, epidemiologic research passively accumulated the estimates of association between tea consumption and colorectal cancer. The majority of studies were not specifically designed to investigate this association; they were often conducted to study other dietary effects on colorectal cancer, particularly fiber, and used a single question to assess tea consumption. This lies in stark contrast to the level of detail in more recent tea assessment tools (27,29) and may explain imprecise risk estimates.

Finally, the validity of the assessment and unbiased capture of incident disease states is an important consideration. Hospital based case-control studies of these conditions are vulnerable to bias, as are the studies of polyps that are based upon prevalence estimates.


   FOOTNOTES
 
1 Presented as part of "The Third International Scientific Symposium on Tea and Human Health: Role of Flavonoids in the Diet," given at the United States Department of Agriculture, September 23, 2002. This conference was sponsored by the American Cancer Society, American College of Nutrition, American Health Foundation, American Society for Nutritional Sciences, Food and Agriculture Organization, and the Linus Pauling Institute at Oregon State University and was supported by a grant from the Tea Council of the U.S.A. Guest editor for this symposium was Jeffrey Blumberg, PhD, Jean Mayer USDA Human Nutrition Research Center on Aging, Tufts University, Boston, MA 02111. Back


   LITERATURE CITED
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 LITERATURE CITED
 

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