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Fruit, vegetables, and cancer prevention: A review of the epidemiological evidence a

b

Gladys Block , Blossom Patterson & Amy Subar

b

a

Public Health Nutrition Program, Dept. of Social and Administrative Health Sciences, School of Public Health, University of California, 419 Earl Warren Hall, Berkeley, CA, 94720 b

Division of Cancer Prevention and Control, National Cancer Institute, National Institutes of Health, Bethesda, MD, 20892 Published online: 04 Aug 2009.

To cite this article: Gladys Block , Blossom Patterson & Amy Subar (1992) Fruit, vegetables, and cancer prevention: A review of the epidemiological evidence, Nutrition and Cancer, 18:1, 1-29, DOI: 10.1080/01635589209514201 To link to this article: http://dx.doi.org/10.1080/01635589209514201

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Review

Fruit, Vegetables, and Cancer Prevention: A Review of the Epidemiological Evidence Downloaded by [Temple University Libraries] at 01:59 08 September 2013

Gladys Block, Blossom Patterson, and Amy Subar

Abstract Approximately 200 studies that examined the relationship between fruit and vegetable intake and cancers of the lung, colon, breast, cervix, esophagus, oral cavity, stomach, bladder, pancreas, and ovary are reviewed. A statistically significant protective effect of fruit and vegetable consumption was found in 128 of 156 dietary studies in which results were expressed in terms of relative risk. For most cancer sites, persons with low fruit and vegetable intake (at least the lower one-fourth of the population) experience about twice the risk of cancer compared with those with high intake, even after control for potentially confounding factors. For lung cancer, significant protection was found in 24 of 25 studies after control for smoking in most instances. Fruits, in particular, were significantly protective in cancers of the esophagus, oral cavity, and larynx, for which 28 of 29 studies were significant. Strong evidence of a protective effect of fruit and vegetable consumption was seen in cancers of the pancreas and stomach (26 of 30 studies), as well as in colorectal and bladder cancers (23 of 38 studies). For cancers of the cervix, ovary, and endometrium, a significant protective effect was shown in 11 of 13 studies, and for breast cancer a protective effect was found to be strong and consistent in a meta analysis. It would appear that major public health benefits could be achieved by substantially increasing consumption of these foods. (Nutr Cancer 18, 1-29, 1992)

Introduction Several authors have reviewed the epidemiological literature suggesting a protective role for /3-carotene (1,2) or vitamin C (3,4) in cancer incidence. In both cases, the weight of the evidence for a protective effect is impressive. All acknowledge, however, that it is impossible to be confident that a particular factor is the effective agent. Such investigations are conducted by asking respondents about their consumption of foods, particularly fruits and vegetables. With few exceptions, nature does not package a single nutrient in a particular food. Oranges and orange juice, for example, are important sources of vitamin C, folie acid, G. Block is affiliated with the School of Public Health, University of California, Berkeley, CA 94720. B. Patterson and A. Subar are affiliated with the Division of Cancer Prevention and Control, National Cancer Institute, National Institutes of Health, Bethesda, MD 20892.

Copyright © 1992, Lawrence Erlbaum Associates, Inc.

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and glutathione and moderately good sources of carotenoids. Thus, in most cases, the nutrient that is reported or reviewed reflects the interest of the investigator or reviewer, and we cannot be certain that it is, in fact, the actual protective factor. In addition, it is not clear that it is one nutrient instead of another. Indeed, it is clear that nutrients act together, with optimal levels of several being required for optimal protection (5-7). The search for a single protective agent, a "magic bullet" nutrient, however, has led to an insufficient appreciation of the strength and consistency of the evidence that fruits and vegetables themselves have an important protective effect against a very wide range of human cancers. An appreciation of this relationship could have an important impact on the nature of public health education and policy. The purpose of this paper is to review the epidemiological studies that have examined the relationship between fruit and vegetable intake and cancer incidence or mortality. Although the focus of this review is not on nutrients, in many cases the investigators reported their results in terms of nutrients, usually /3-carotene or vitamin C. Such studies provide direct evidence of the role of fruit and vegetable intake (the primary sources of those nutrients) and are reviewed here with that emphasis. Associations with retinol are omitted for the following reasons: retinol is obtained exclusively from animal sources; retinol levels in the body are homeostatically controlled and are uninfluenced by provitamin A intake, except in severely malnourished persons; and finally, carotenoid activity is thought to result from its antioxidant and free radical scavenging activity rather than through conversion to retinol, and retinol is a much poorer radical scavenger than ^-carotene. The observation in many studies of different effects of retinol and carotenoids is consistent with these observations. No international or regional correlation studies are included, because it is difficult to rule out indirect or spurious associations (8). This review is limited to case-control and prospective epidemiological studies in humans—studies in which both dietary intake (or blood nutrient levels) and cancer status are identified in the same individuals. In most studies, information about diet before disease is obtained by means of a questionnaire on frequency of consumption of various foods. Respondents are then grouped into those with low, moderate, or high intake of individual foods, groups of foods, or nutrients calculated from them. Risk is usually expressed as relative risk (RR): the risk of cancer in the group exposed to a risk factor (such as low fruit/vegetable intake) is expressed as a ratio of the risk in the group not exposed (here, those with high intake). For this review, all risks have been expressed in this direction, so that an RR > 1.0 indicates an increased risk of cancer among those with low intake. For example, an RR of 2.0 indicates that those with infrequent consumption of fruits and vegetables are estimated to have twice the risk of that cancer compared with those with frequent consumption. Studies are grouped below by cancer site. Table 1 summarizes those studies of invasive cancer in which results are expressed in terms of RR or odds ratio (OR) and in which statistical significance was given. Table 1 omits studies of precancerous conditions and of serum rather than diet and, in a few cases, very small studies. For these reasons, the values in Table 1 may differ from summaries in the text. We have attempted to be comprehensive and have reviewed every study we could identify through 1991 in which the role of fruits and vegetables in cancer incidence was assessed. In some studies, results were reported separately for 20 or more foods. In such instances, we focused on foods widely accepted as potentially important, such as leafy green vegetables, carrots, and citrus fruits. In other studies, only a nutrient index (carotenoids or vitamin C) was reported; in these cases, the direction and significance of that nutrient constituted the criterion for an effect of vegetables or fruit. Significance was based on tests reported by the investigators: p < 0.05 or more extreme, the lower level (LL) of the 95% confidence interval (CI) at an RR > 1.0, or a significant trend test.

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Table 1. Summary of Epidemiological Studies of Fruit and Vegetable Intake and Cancer Prevention" References

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All sites except prostate All sites Lung* Larynx

(9,12,14-19 29,31-37, 39-46,48) (49-52)

Oral Cavity, Pharynx'

(51,55-62)

Esophagus*

Bladder'

(51,64-70, 72-79) (14,82,84-86, 89,90,92-98, 100-102,104-107) (86, 110-116,119, 120A.121-133, 135,136,138, 141) (9,150-153)

Pancreas

(156-167)

Cervix*

(169-174, 176,180) (182,184, 185,247) (190,202-206)

Stomach* Colorectal'

Ovary Breast' Prostate"1 Miscellaneous"

(9,14,210,211, 213,216,217, 219,221-226) (183,232-236, 237)

No. of Studies

Protective* (p < 0.05)

Harmful" (p < 0.05)

156 170 25

128 132 24

4 6 0

4

4

0

9

9

0

16

15

0

19

17

1

27

20

3'

1.9 (0.3-3.3)

5

3

0

11

9

0

8

7

0

4

3

0

14

8"

0

14

4

2

2.1 (1.6-2.1) 2.8 (1.4-6.4) 2.0 (1.2-4.7) 1.8 (1.1-2.3) 1.3 (1.1-2.8) 1.3 (0.6-3.5)

8

6

0

Relative Risk*

2.2 (1.2-7.0) 2.3 (2.1-2.8) 2.0 (1.7-2.5) 2.0 (0.7-4.8) 2.5 (0.5-5.8)

a: These studies of invasive cancers reported on diet rather than serum, expressed the effect in terms of relative risk (RR) or odds ratio, and stated statistical significance. Multiple reports on the same dataset are omitted, as are studies with 70 years of age. Similarly, in a study in Hawaii (30,211,212), among men >70 years old, risk increased with increasing intake of all nutrients reported, including total carotenes (RR = 1.6, trend p = 0.08). A reanalysis, however, revealed that the entire association was with papaya and was significant only for ethnic Japanese and that ß-carotene was not associated with prostate cancer (213). Neither these nor the Buffalo results were adjusted for energy or fat intake. Investigators in Washington, D C , reported two methodologically similar case-control studies of black men (214,215). Total vitamin A from animal and vegetable sources was assessed and respondents were asked to report, retrospectively, their dietary intake when at 30-49 and >50 years of age. A significant positive association was seen at the younger but not at the older age, in contrast to the Buffalo and Hawaii studies. In the second study, no association was found for energy-adjusted nutrient intake in either age period (215). Several other case-control studies, however, showed significant protective effects of either fruits/vegetables or carotenoid indexes. Schuman and co-workers (216) found a significant negative association with carrot intake. Similarly, Ross and colleagues (217,218) showed a protective effect for carrots among Whites but not Blacks and a protective effect of spinach/greens among Blacks but not Whites; both effects were statistically significant. Low intake of /3-carotene was a risk factor only among those with a low-fat diet, whereas no effect of /3-carotene was observed among those with high fat intake. In addition, in two recent Japanese reports using identical subjects (219,220), a protective effect of jS-carotene, but not retinol, was found. The risk associated with low intake ranged from 2.1 to 2.8 for absolute intake and from 2.9 to 3.5 for intake per kilocalorie, which was highly significant for trend. A stronger protective effect was seen among men > 70 years of age, although the results for younger men still suggested a protective effect for /3-carotene. In a large study in the United States (221), significant two- to threefold reductions in risk were found with higher /3-carotene intake, but only among men 74 years of age (14). In a case-control study of Japanese men, Mishina and others (225) also observed that green and yellow vegetable consumption was associated with decreased prostate cancer risk, but the association (based on 30 discordant pairs) was not significant. In Italy (226), individuals were asked about a single vegetable item, "green vegetables"; infrequent consumption (defined as < 5 times/wk) was found to be unrelated to risk when adjusted for meat and dairy intake and other variables.

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Studies of serum retinol (227,228) or serum /3-carotene obtained after cancer diagnosis (229) are not discussed here. However, Willett and colleagues (10) examined serum carotenoids in persons who were free of cancer at the time the blood was drawn. No differences were found between those who developed prostate cancer within the next five years (« = 11) and controls. In contrast, Knekt and associates (26) found a three- to fivefold reduction in risk of subsequent prostate cancer among men who were in the highest quintile of serum /3-carotene at baseline, adjusted for smoking and after exclusion of the first two years of follow-up. Others have found significant inverse associations with retinol (230,231); in one of these studies (230), no association was found with serum /S-carotene, although there was a suggestion of a relationship with another carotenoid, lycopene. In summary, the three studies showing a significant increased risk with increased intake all were based on vitamin A or carotene indexes, and none was adjusted for fat intake. The four studies showing a significant protective effect with increased intake either reported only on foods or, if nutrient scores were reported, on nutrients adjusted for fat or calories. In one study (217) the risk of vegetables or carotenoids was examined by strata of fat intake, and low intake was associated with increased risk only in those with low fat intake. Of the studies with equivocal results, several were small, did not examine energy-adjusted values, or asked about only a single food item. Thus, the data for prostate cancer are inconclusive, but future work should focus on frequency of intake of foods, retinol and carotenoids separately, energy-adjusted nutrient scores, and risks within strata of fat or meat intake. Miscellaneous Sites For malignant melanoma, weak inverse trends have been observed with plasma /3-carotene (232) or carotene-rich foods (232; CDJ Holman, unpublished data). In studies of thyroid cancer (233,234), significant reductions in risk have been associated with green vegetables and fresh fruit. In a Japanese study of biliary tract cancer (235), daily consumption of vegetables and fruits was associated with significant two- to threefold reductions in risk. In a single study on mesothelioma, Schiffman and co-workers (236) found a protective effect of frequent consumption of vegetables, highly significant for home-grown produce and cruciferous vegetables, even after adjustment for exposure to asbestos. La Vecchia and others (183) found infrequent consumption of green vegetables and fresh fruit to be highly significant risk factors for endometrial cancer, conferring RRs of 2-4 after multivariate adjustment for potentially confounding factors. Discussion For sites other than the prostate, in 128 of 156 studies of dietary intake that calculated a RR, a statistically significant protective effect of fruits and vegetables or the nutrients derived from them was found; dietary intake was significantly positively associated in only 4 studies, about what would be expected by chance. Thus, overall the evidence of an association between fruit and vegetable consumption and cancer prevention is exceptionally strong and consistent. The vast majority of these studies have been published in peer-reviewed journals and have included appropriate control for possible confounding factors. If chance alone were operating, 4 of the 156 studies would be expected to be statistically significantly protective, on the basis of a two-tailed test at a 0.05 significance level. Factors other than chance, however, might have produced these results. Publication bias probably exists but could not account for the overwhelming weight of the evidence. Even if 150 negative studies had been suppressed, the resulting almost 50% significance rate would be remarkable. In addition, one would not expect suppression of studies that found significantly harmful results; yet in only 6 of 170 were such results found, about what would

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be expected by chance. Furthermore, all dietary epidemiology studies are major undertakings that tend to be published somewhere, regardless of the results, and almost always report on a wide variety of dietary and nondietary factors. It is unlikely that the absence of significance of one food group would result in a publication bias. The issue of multiple comparisons is a more serious problem but, again, cannot account for the preponderance of the evidence, and many of the results reported here were significant at the p < 0.01 or 0.001 level. It is also appropriate to ask whether, if one searched for effects of other groups of foods (such as grain products or legumes), a similar proportion might be found to be significantly associated with the disease. This appears not to be the case. Among the case-control or prospective colorectal cancer studies in which the role of individual breads, grain products, or fiber from grains was reported, significant protection associated with these foods was found in only 2 of 12 studies; in 8 of these studies, significant associations were found for fruits or vegetables or their fibers (88, 113, 115, 117, 119, 123, 126, 129-131, 138, 141). Another legitimate objection might be raised: that these studies have shown association but not causality. In particular, one might suspect that some associated demographic or behavioral factor is the true causative agent, such as higher education and socioeconomic status, better medical care, or avoidance of smoking or fatty foods. Although this cannot be ruled out, it should be noted that many of the studies reviewed here have controlled for smoking and in some cases for socioeconomic status and fat or energy intake. In a number of studies, significant effects have been found even within strata of smokers or nonsmokers, so the observation that smokers eat fewer fruits and vegetables is not explanatory. In addition, the 170 studies in Table 1 were conducted in 17 different nations and include populations as different as the Netherlands, China, India, Turkey, upstate New York, and rural Blacks in Louisiana. It is hard to imagine a correlate of fruit and vegetable consumption that could explain identical conclusions in such disparate groups. Many of the populations in which protective effects have been observed do not have the same cluster of correlated behaviors found in the United States. For example, in many developing countries, the alternative to a high-fruit/vegetable diet is not a diet high in fat or meat but one high in a starchy staple such as rice. It is likely that the overall quality of the diet is important, but no other food groups (e.g., meats, dairy) are consistently found to be protective in these studies. If one concedes that a disproportionate number of studies has shown statistically significant protection, one might ask whether the results are clinically significant. It would appear that they are. In the vast majority of studies, a dose-response relationship ("more is better") has been found in which those in the lower end of the distribution experience a cancer risk generally at least twice as high as those in the upper end. Because imperfect dietary assessment methods generally result in an underestimate of the actual risk (190), it is very likely that the cancer risks are greater than twofold. These at-risk groups are not tiny fractions of the population, but represent the lower one-fifth to lower one-third of the population or even more in populations or subgroups with a low overall fruit/vegetable intake. Bjelke (110) even suggests that, for colorectal cancer, the majority of the population may be at substantial increased risk compared with a small minority whose fruit/vegetable consumption is high. Few if any risk factors besides smoking (and alcohol for the oral/esophageal cancers) confer risks of this magnitude. The biochemical and biological rationale for an effect of these foods is extremely strong. Fruits and vegetables are the principal, and in many societies the only, sources of the antioxidant nutrients vitamin C and carotenoids. In addition, in the United States they are also the main source of vitamin E (237). The central role of oxidative events and free radical damage in cancer causation is well established, as is the fact that antioxidants can block or repair such damage (5,238,239). Other mechanisms, involving folate and fiber, may also be

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important for some cancers. Carotenoids, vitamin C, folate, fiber, and other constituents may all be factors, probably acting jointly rather than singly. Ascorbic acid is an important reducing agent and free radical scavenger (240) and also prevents or reduces the formation of carcinogens such as nitrosamines (241,242). Carotenoids are also free radical scavengers, and some may also influence cell differentiation through conversion to retinol (243). Certainly, more research is needed to elucidate mechanisms of action of all these constituents, particularly their joint actions and their impact on the risks associated with factors such as smoking and fat intake. From a public health perspective, however, it is not necessary to understand the biochemistry, an understanding that will occur slowly and will not be complete in the foreseeable future. The results presented above suggest that substantial public health and clinical benefits could be achieved simply by increasing the public's consumption of fruits and vegetables. The National Research Council has recommended consumption of five servings of fruits and vegetables daily (244), a level that was strongly protective in most of the studies reported above. In contrast, in the NHANES II survey, only 10% of the US population consumed that number (245). Dietary recommendations and campaigns emphasizing fruits and vegetables rather than nutrients have several advantages. First, there is little need for educational efforts, because people already know what fruits and vegetables are. Second, people can easily monitor whether they have reached a goal that is expressed in terms of servings of fruit and vegetables. Such self-monitoring is very important for continued compliance and is much more difficult to accomplish when the recommendation is in terms of grams. Finally, it is a positive message—not something they have to give up but something they can eat more of, and virtually everyone enjoys some fruits and some vegetables. In 1854, John Snow stopped a cholera epidemic simply by taking the handle off the pump. The research presented above suggests that consumption of fruits and vegetables may be a handle that, if manipulated by public policy, clinical advice, and public education, could have a substantial impact on a wide range of cancers. Acknowledgments and Notes Address reprint requests to Dr. G. Block, Public Health Nutrition Program, Dept. of Social and Administrative Health Sciences, School of Public Health, 419 Earl Warren Hall, University of California, Berkeley, CA 94720. Submitted 19 February 1991; accepted in final form 27 March 1992.

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