fruit and vegetables in cancer prevention and vegetables in cancer...fruit and vegetables in cancer...

Fruit and Vegetables in Cancer Prevention

Harri Vainio and Elisabete Weiderpass

Abstract: Our aim was to review the epidemiological litera-

ture on possible cancer-preventive effects of the consumption

of fruits and vegetables in humans, to quantify the effect of

high versus low consumption of fruits and vegetables, and to

give an overall assessment of the existing evidence. We based

our work on an expert meeting conducted by the Interna-

tional Agency for Research on Cancer in 2003. A qualitative

reading and evaluation of relevant articles on the can-

cer-preventive effect of the consumption of fruits and vegeta-

bles was made followed by the calculation of the mean rela-

tive risk and range for cohort and case-control studies

separately. The possible population-preventable fraction for

modifying diet in relation to fruit and vegetable consumption

was calculated as well as an overall statement about the de-

gree of evidence for the cancer-preventive effect of fruit and

vegetable consumption for each cancer site. There is limited

evidence for a cancer-preventive effect of the consumption of

fruits and vegetables for cancer of the mouth and pharynx,

esophagus, stomach, colon-rectum, larynx, lung, ovary (veg-

etables only), bladder (fruit only), and kidney. There is inade-

quate evidence for a cancer-preventive effect of the consump-

tion of fruits and vegetables for all other sites. Applying this

range of risk difference to the range of prevalence of low in-

take, the preventable fraction for low fruit and vegetable in-

take would fall into the range of 5–12%. It is important to

recognize that this is only a crude range of estimates and that

the proportion of cancers that might be preventable by in-

creasing fruit and vegetable intake may vary beyond this

range for specific cancer sites and across different regions of

the world.

Introduction

In the early 1900s, the focus of diet research was on iden-

tifying and preventing nutrient-deficiency diseases. Later,

the focus changed to identifying nutrient requirements. More

recently, research has focused on the role of diet in maintain-

ing health and reducing the risk of noncommunicable dis-

eases such as cancer.

Potentially, all types of dietary components have potential

to affect health status, causing or preventing diseases. In the

past decades, abundant consumption of fruits and vegetables

has been associated with a lower risk of several chronic dis-

eases including cardiovascular diseases and overall mortality

(1). Consumption of fruits and vegetables is low, particularly

in developing nations. In 1998, only 6 of 14 World Health Or-

ganization regions had an availability of fruits and vegetables

to supply the recommended 400 g/day per inhabitant (1). In

1997, the World Cancer Research Fund and the American In-

stitute for Cancer Research produced an extensive report

stating that diets rich in fruits and vegetables “decrease the

risk of many cancers” (2). Their evaluation was based mainly

on the existing case-control studies, which have inherent

problems associated with measurement error. Since then,

more recent prospective cohort studies, where recall bias is

less of a problem, indicated that such diets may not be pre-

ventive against cancer. In 2003, the International Agency for

Research on Cancer (IARC) organized an expert meeting to

access the evidence based on published literature of the can-

cer-preventive effects of the consumption of fruits and vege-

tables (3). The purpose of this handbook was to provide an

up-to-date review of the knowledge about fruits and vegeta-

bles collectively. We summarize here the main results of this

meeting in what concerns cancer prevention in humans as

well as the most important articles published in the field

since then. A more complete and detailed description of the

results has been published elsewhere (3).

Methods

Definition of Fruits and Vegetables

Although culinary definitions are less precise than botani-

cal definitions, they are commonly used by researchers and

subjects in epidemiological surveys.

The culinary definition of fruits and vegetables refers to

edible parts of plant foods with the exclusion of cereal grains,

nuts, and seeds. The culinary term for fruit refers to the part

of a plant that contains the seeds and pulpy surrounding tis-

sue. Plant parts used as vegetables include stems and stalks,

roots, tubers, bulbs, leaves, flowers, some fruits, and pulses.

The definition and classification of fruits and vegetables are

NUTRITION AND CANCER, 54(1), 111–142

Copyright © 2006, Lawrence Erlbaum Associates, Inc.

H. Vainio is affiliated with the Finnish Institute of Occupational Health, Helsinki, Finland. E. Weiderpass is affiliated with The Cancer Registry of Norway,

N-0310, Oslo, Norway and the Karolinska Institutet, Department of Medical Epidemiology and Biostatistics, Stockholm, Sweden.

not precise and differ between dietary assessment instru-

ments depending on the purposes of the study and dietary

patterns of the population being evaluated.

Measuring Intake of Fruits and Vegetables

Questionnaire methods such as food-frequency question-

naires (FFQs) and diet history (DH) have been the most com-

monly used methods to assess individuals’ diets in case-con-

trol and cohort studies. These methods are designed to

estimate usual intake, allowing classification of subjects in

epidemiological studies. Twenty-four-hour recalls were

mostly used to validate FFQ and DH. Given the large

intra-individual variation in food intake, measurement errors

are an important source of potential misclassification and

bias. The estimation of fruit and vegetable intake using FFQ

and DH largely differs in epidemiological studies, depending

on the way the questionnaire is structured, the amount of spe-

cific questions, the method of assessing portion size, and the

types of fruits and vegetables assessed. In the following, we

present information from studies on fruit and vegetable in-

take as a group; no subgroup classification was used.

Integration of the Evidence:

Cancer-Preventive Effects of Fruit

and Vegetable Consumption in Humans

In reviewing the evidence, inclusion criteria were used.

Case reports were not considered, and ecological studies were

not used in the evaluation. Cohort and case-control studies

were always considered unless they were inadequate in con-

ception, design, conduct, or analysis. There have been several

instances of sequential or multiple publications of analyses of

the same or overlapping datasets. When the reports clearly re-

lated to the same or overlapping datasets, only data from the

largest or most recent publication were included.

The data considered are presented in detail elsewhere (3).

The data used in the evaluations also appear as plots (Figs.

1–36). Only those studies on total fruit or vegetable con-

sumption reporting confidence intervals and adjusted for the

main confounders for the relevant sites are included in the

plots. An estimate of the overall effect across all the evalu-

ated studies, calculated as explained subsequently, is pre-

sented, taking the size of the study (as reflected in the confi-

dence interval) into account when weighing the individual

study findings. The result of applying a test for heterogeneity

is given as a footnote to each plot. The reader is cautioned

that these summary estimates do not constitute the result of a

formal meta-analysis, and they should not be interpreted as

such.

The summary estimates in the plots were calculated as fol-

lows. Using the log of the relative risks for the highest versus

lowest exposure categories in the individual studies, desig-

nated as βi, the pooled estimate (summary value, βp) was ob-

tained, separately for cohort and case-control studies, as

βp = [Σi βi/var(βi)]/[Σi 1/var(βi)]

with estimated standard error

SE(βp) = [Σi 1/var(βi)]–1/2

The χ2 for heterogeneity was calculated as

χ2 = Σi (βi – βp)2/var(βi)

with (N – 1) degrees of freedom, where N is the total number

of studies.

Analyses and generation of the plots were performed us-

ing A Language and Environment for Statistical Computing

(R Foundation for Statistical Computing, Vienna, Austria)

(4). Individual studies are presented in the plot in chronologi-

cal order, with the “box size” proportional to the inverse of

their variance.

For some studies, results are reported for subcategories of

the population under study, for example, males and females,

pre- and postmenopausal women, and colon and rectal can-

cer. In the calculation of the overall effect and in the final

plot, the subgroups counted as individual studies; however,

when counting the number of evaluable studies for different

cancer sites, subgroups were considered as coming from a

single study.

Overall Evaluation of the Evidence

The group of experts who met at IARC made judgments

concerning the evidence that fruits and vegetables prevent

cancer in humans. In making the judgment, several criteria

are considered. Findings that are replicated in several studies

of the same design or using different approaches are more

likely to provide evidence of a true protective effect than iso-

lated observations from single studies. The results of studies

judged to be of high quality are given more weight. In sum-

marizing the data, evaluations of the strength of the evidence

for cancer-preventive activity and carcinogenic effects from

studies in humans are made, using standard terms, knowing

that the evaluations may change as new information becomes

available. The categories in which the potential cancer-pre-

ventive agent is classified are

• Sufficient evidence of cancer-preventive activity: A

causal relationship has been established between the agent or

intervention and the prevention of human cancer in studies in

which chance, bias, and confounding could be ruled out with

reasonable confidence.

• Limited evidence of cancer-preventive activity: The

data suggest a reduced risk for cancer with use of the agent or

intervention but are limited for making a definitive evalua-

tion either because chance, bias, or confounding could not be

ruled out with reasonable confidence or because the data are

restricted to intermediary biomarkers or uncertain validity in

the putative pathway to cancer.

• Inadequate evidence of cancer-preventive activity: The

available studies are of insufficient quality, consistency, or

statistical power to permit a conclusion regarding a can-

112 Nutrition and Cancer 2006

cer-preventive effect of the agent or intervention, or no data

on the prevention of cancer in humans are available.

• Evidence suggesting lack of cancer-preventive activity:

Several adequate studies of use or exposure to the agent or in-

tervention are mutually consistent in not showing a preven-

tive effect.

The evaluations refer to fruits and vegetables as whole

classes, without consideration of separate subcategories.

Results

Oral Cavity and Pharynx

No cohort study on fruit consumption and risk of oral or

oropharyngeal cancer was identified. Most studies were hos-

pital-based case-control studies. For the 10 evaluated case-

control studies of fruit consumption (5–14) the mean relative

risk for high versus low consumption was 0.45 and the range

was 0.10–0.70 (Fig. 1).

In the large cohort study of Hirayama in Japan (15), the fre-

quency of intake of green-yellow vegetables was inversely as-

sociated with risk of oropharyngeal cancer nonsignificantly in

men and significantly in women. Seven case-control studies

were evaluated for vegetable intake (5–8,11–13), and the

mean relative risk for high versus low consumption was 0.49

and the range was 0.19–0.80 (Fig. 2). Concerns about residual

confounding by cigarette smoking, alcohol consumption, and

socioeconomic status as well as recall bias among cases and

selection bias among control subjects mayat least partiallyex-

plain these results. There are no consistent findings of an in-

verse association of salivary gland and nasopharynx cancer

with fruit and vegetable consumption.

Esophagus

An inverse association between fruit consumption and

mortality for esophagus cancer was found in one cohort

study (16). Among the 16 evaluated case-control studies

(7,9,17–30), the mean relative risk for high versus low fruit

consumption was 0.54 and the range was 0.14–1.50 (Fig. 3).

For vegetable consumption, no cohort studies were identi-

fied, and the results of 10 case-control studies that were eval-

uated (7,17–21,23,25,31,32) entailed a mean relative risk for

Vol. 54, No. 1 113

Figure 1. Case-control studies of oral and pharyngeal cancer and fruit consumption. (Reproduced with permission from the IARC Handbook of Cancer Preven-

tion, vol 8. Lyon, France: IARC Press, 2003.)

high versus low consumption of 0.64 and a range of

0.10–0.97 (Fig. 4). The studies evaluated did not indicate

gender-specific effects and were underpowered to detect ef-

fect modification by smoking and alcohol consumption. Se-

lection and recall bias or residual confounding cannot be

ruled out from the evaluated studies.

Stomach

For fruit consumption, 10 cohort (16,33–41) and 28

case-control studies (28,42–68) were evaluated. In the cohort

studies, the mean relative risk for high versus low consump-

tion was 0.85 and the range was 0.55–1.92 (Fig. 5). In the

case-control studies the mean was 0.63 and the range was

0.31–1.39 (Fig. 6).

For vegetable consumption 5 cohort studies

(33,35,39,41,69) and 20 case-control studies (31,42,43,

45,48,51,52,55–58,60,61,63,64,66,70–73) were evaluated.

For the cohort studies, the mean relative risk for high versus

low consumption was 0.94 and the range was 0.70–1.25 (Fig.

7); for the case-control studies, the mean relative risk for high

versus low consumption was 0.66 and the range was

0.30–1.70 (Fig. 8).

The reason that case-control studies tended to show in-

verse associations and cohorts did not is unclear. Recall bias

as well as changes in dietary patterns at early stages of dis-

ease may at least partially explain the discrepancy between

case-control and cohort studies mean results.

Colon and Rectum

For fruit consumption, 11 cohort studies (16,74–83) were

evaluated, and the mean relative risk for high versus low con-

sumption was 1.0 and the range was 0.50–1.60 (Fig. 9). For

the nine evaluated case-control studies (84–92), the mean rel-

ative risk for high versus low fruit consumption was 0.87 and

the range was 0.30–1.74 (Fig. 10).

For vegetable consumption, there were 10 evaluated co-

hort studies (74–83), and the mean relative risk for high ver-

sus low consumption was 0.94 and the range was 0.72–1.78

(Fig. 11). For the 13 evaluated case-control studies

(84–90,92–97), the mean relative risk for high versus low


Recall and selection bias in case-control studies and con-

founding in both case-control and cohort studies may have

affected the results.


Figure 2. Case-control studies of oral and pharyngeal cancer and vegetable consumption. (Reproduced with permission from the IARC Handbook of Cancer

Prevention, vol 8. Lyon, France: IARC Press, 2003.)

Liver

Only one cohort study (16) and three case-control studies

(98–101) were evaluated, and none found evidence of an as-

sociation between fruit consumption and liver cancer risk.

For vegetable consumption, the cohort study of Sauvaget

et al. (16) found a significant inverse association with

green-yellow vegetables, whereas Hirayama et al. (15) did

not. The cohort study by Yu et al. (102) reported a significant

reduced risk. For the case-control studies, La Vecchia et al.

(100) found no effect of all vegetables but an effect for fruit

and vegetables combined (103). Hadziyannis et al. (98),

Fukuda et al. (104), and Kuper et al. (101) found no associa-

tion for vegetable consumption and risk of liver cancer.

Biliary Tract

One cohort study (16) found no association between fruit

consumption and risk of gallbladder cancer. One case-con-

trol study (105) showed a significant protective effect of con-

sumption of fruit and vegetables combined, whereas two

other case-control studies on green-yellow vegetables

(15,16) found no association.

Pancreas

In the four evaluated cohort studies that also considered

smoking as a confounding factor in the analysis

(16,106–108), all found inverse, nonsignificant associations

for pancreas cancer with increased fruit consumption. In six

case-control studies (109–114) the mean relative risk for

high versus low consumption was 0.72, and the range was

0.07–0.92 (Fig. 13).

Nonsignificant inverse associations were found in the two

evaluated cohort studies of vegetable consumption

(106,108). For the five evaluated case-control studies

(109,111–114), the mean relative risk for high versus low

consumption of vegetables was 0.80 and the range was

0.32–1.03 (Fig. 14).

Vol. 54, No. 1 115

Figure 3. Case-control studies of esophageal cancer and fruit consumption. S, squamous cell carcinoma; A, adenocarcinoma. (Reproduced with permission

from the IARC Handbook of Cancer Prevention, vol 8. Lyon, France: IARC Press, 2003.)

In studies where the proxies of patients were interviewed,

as well as those studies that excluded deceased cases, report-

ing bias is a serious concern. Many of the inverse associa-

tions were found in studies where the response rates among

controls were low.

Larynx

Four case-control studies (7,115–117) were evaluated for

fruit consumption, and the mean relative risk for high versus

low consumption was 0.63 and the range was 0.38–0.80 (Fig.

15).

For vegetable consumption, the four evaluated case-con-

trol studies (7,115–117) had a mean relative risk of 0.49 and a

range of 0.17–1.1 (Fig. 16).

The majority of the studies were hospital based, with the

exception of one large population-based study. Control for

smoking was rather crude in earlier studies. One study pre-

sented results for fruit and vegetable consumption according

to smoking and alcohol consumption history, and the effect

of fruit and vegetable consumption among smokers and

among drinkers was weaker than among nonsmokers and

among nondrinkers. This indicates that the possibility of re-

call and selection bias in earlier studies cannot be ruled out.

Lung

For the 13 evaluated cohort studies of fruit consumption

(16,74,118–128), the mean relative risk for high versus low


For the 21 evaluated case-control studies (57,129–148),

the mean relative risk for high versus low consumption of

fruit was 0.70 and the range was 0.33–2.04 (Fig. 18).

For 11 cohort studies on vegetable consumption

(74,119–128), the mean relative risk was 0.80 and the range

was 0.47–1.37 (Fig. 19).


Figure 4. Case-control studies of esophageal cancer and vegetable consumption. S, squamous cell carcinoma; A, adenocarcinoma. (Reproduced with permis-

sion from the IARC Handbook of Cancer Prevention, vol 8. Lyon, France: IARC Press, 2003.)

For 18 evaluated case-control studies on vegetable con-

sumption, (129–133,135,137,139,140,143,145,147,149–154)

the mean relative risk was 0.69 and the range was 0.30–1.49

(Fig. 20). There were no clear differences in the results for

men and women, hospital- and population-based studies, nor

between morphological categories on lung cancer. The

strength of the inverse association was smaller in cohort than

in case-control studies, leaving the possibility of recall and

selection bias in the case-control studies.

Although the newer cohort studies have attempted to care-

fully control for confounding by smoking, residual con-

founding cannot be excluded, and cohort studies usually fail

to capture changes in smoking and diet after cohort enroll-

ment. Studies that did subanalysis among nonsmokers usu-

ally found a weaker effect, although the results are not en-

tirely consistent.

Breast

For fruit consumption, there were six evaluated cohort

studies (16,74,155–158), and the mean relative risk for high

versus low consumption was 0.94 and the range was

0.64–1.43 (Fig. 21). For the 12 evaluated case-control studies

(9,159–169), the mean relative risk for high versus low fruit


For five evaluated cohort studies of vegetable consump-

tion (74,155–158), the mean relative risk for high versus low


For 12 evaluated case-control studies (159–161,

163–167,170–173), the mean relative risk for high versus

low vegetable consumption was 0.66 and the range was

0.09–1.40 (Fig. 24).

After the meeting, a large cohort study on the association

between fruits and vegetables and breast cancer risk has been

published with null results (174).

Cervix

No cohort studies on fruit and vegetable consumption and

cervix cancer risk were identified. For the case-control stud-

ies, there was no consistent effect and very little evidence of

an effect of either fruit or vegetable consumption (175–180).

Given the very strong effect of human papillomavirus (HPV)

with the disease, there is concern about the appropriate con-

Vol. 54, No. 1 117

Figure 5. Cohort studies of stomach cancer and fruit consumption. (Reproduced with permission from the IARC Handbook of Cancer Prevention, vol 8. Lyon,

France: IARC Press, 2003.)

trol for possible confounding or modifying effect by the in-

fection. One study examined the risk restricted to HPV-posi-

tive women, and the results were similar when both

HPV-positive and -negative controls were included or when

controls were limited to women with HPV infection.

Endometrium

The association between fruit and vegetable consumption

has been studied only in case-control studies. For seven eval-

uated case-control studies (180–186), the mean relative risk

for high versus low fruit consumption was 1.03 and the range

was 0.67–1.97 (Fig. 25). For five evaluated case-control stud-

ies on vegetable consumption (181–185), the relative risk for

high versus low consumption was 0.75 and the range was

0.65–1.00 (Fig. 26). The combined effect of fruit and vegeta-

ble consumption was inversely associated with endometrial

cancer risk in one cohort and three case-control studies. Body

mass index, as a proxy of obesity, an established risk factor

for endometrial cancer, has been adjusted in several but not

all of the previous studies.

Ovary

For fruit consumption, the number of studies available

was limited: two cohort (187,188) and four case-control


Figure 6. Case-control studies of stomach cancer and fruit consumption. B, blacks; W, whites; H, hospital controls; P, population controls; M, males; F, females;

I, intestinal type; D, diffuse type; C, cardia; N, noncardia; FH+, gastric cancer family history positive; F–, gastric cancer family history negative; *, not applica-

ble. (Reproduced with permission from the IARC Handbook of Cancer Prevention, vol 8. Lyon, France: IARC Press, 2003.)

Vol. 54, No. 1 119

Figure 7. Cohort studies of stomach cancer and vegetable consumption. M, males; F, females. (Reproduced with permission from the IARC Handbook of Can-

cer Prevention, vol 8. Lyon, France: IARC Press, 2003.)

Figure 8. Case-control studies of stomach cancer and vegetable consumption. I, intestinal type; D, diffuse type; M, males; F, females; C, cardia; N, noncardia; *,

not applicable. (Reproduced with permission from the IARC Handbook of Cancer Prevention, vol 8. Lyon, France: IARC Press, 2003.)

studies (189–192), and the results were inconsistent but in

general indicating no association. For vegetable consump-

tion, an inverse association was found in two cohort (nonsig-

nificant results) (187,188) and five (189,190,192–194) of six

case-control (191) studies. In one case-control study there

was an inverse association for the combined consumption of

fruits and vegetables (190).

Prostate

For eight evaluated cohort studies of fruit consumption

(74,195–201), the mean relative risk for high versus low con-

sumption was 1.11 and the range was 0.84–1.57 (Fig. 27). For

nineevaluatedcase-control studies (9,202–209), themeanrel-

ative risk was 1.08 and the range was 0.40–1.70 (Fig. 28).

The results for fruit are consistent and suggest that high

fruit consumption does not reduce prostate cancer risk. The

increased risk found in some studies may be due to bias asso-

ciated with prostate cancer screening and detection in

health-conscious men.

For vegetable consumption, the mean relative risk for high

versus low consumption in six evaluated cohort studies

(74,197–201) was 0.95 and the range was 0.7–1.04 (Fig. 29).

For nine evaluated case-control studies (202–204,206–211),

the mean relative risk for high versus low consumption was

0.90 and the range was 0.6–1.39 (Fig. 30).

Thus, for vegetables, the majority of studies have reported

a slight, nonsignificant lower risk for higher consumption.

Testis

There were no cohort studies on testis cancer, and two

case-control studies are available (212,213).

Bladder

There were five cohort studies evaluated (214–218), and

the mean relative risk for high versus low consumption of

fruit was 0.87 and the range was 0.63–1.12 (Fig. 31).


Figure 9. Cohort studies of colorectal cancer and fruit consumption. M, males; F, females; CR, colorectal; C, colon; R, rectum. (Reproduced with permission


For the four available case-control studies (219–222), the

mean relative risk for high versus low intake was 0.74 and the

range was 0.53–0.95 (Fig. 32).

Three cohort studies evaluated vegetable consumption

(215,217,218), and the mean relative risk for high versus

low consumption was 0.94 and the range was 0.72–1.16

(Fig. 33).

For the three case-control studies evaluated (219,220,

222), the mean relative risk for low vegetable consumption

was 0.89 and the range was 0.66–1.14 (Fig. 34).

Kidney

Two cohort studies were evaluated: one did not show an

association with total fruit consumption (223) and the other

one had too few cases to be informative (224). Seven

case-control studies were evaluated (9,225–230), and the

mean relative risk for high versus low fruit consumption was

0.76 and the range was 0.20–1.20 (Fig. 35).

Four case-control studies (and no cohort studies) were

evaluated for vegetable consumption (226,227,229,230).

The mean relative risk for high versus low intake was 0.86

and the range was 0.30–1.60 (Fig. 36).

All evaluated case-control studies presented results

adjusted for body mass index and smoking, and most stud-

ies used population-based controls. However, recall bias

cannot be completely excluded as an explanation for the

results.

Brain

Three case-control studies of adult (231–233) and five for

childhood brain cancers (234–238) considered fruit and veg-

etable consumption usually as one among many study hy-

potheses. All adult studies and three childhood studies

showed inverse associations with fruit and/or vegetable con-

sumption. Only one of the three childhood studies showed a

statistically significant inverse association (234); in the other

two the associations were nonsignificant (235,237).

Vol. 54, No. 1 121

Figure 10. Case-control studies of colorectal cancer and fruit consumption. M, males; F, females; CR, colorectal; C, colon; R, rectum. (Reproduced with per-

mission from the IARC Handbook of Cancer Prevention, vol 8. Lyon, France: IARC Press, 2003.)

Thyroid

No cohort studies were available, and none of the three

case-control studies evaluated found a significant association

with total fruit or vegetable consumption (239–241).

Non-Hodgkin Lymphoma

A nonsignificant inverse association was found in both of

the two cohort studies of fruit consumption (242,243). The

only case-control study evaluated showed no evidence of as-

sociation with fruit consumption (244).

For vegetable consumption, one (243) of three cohort

studies evaluated (15,242,243) showed an inverse associa-

tion. The only case-control study evaluated for vegetable

consumption showed no association (245).

Leukemia

The only cohort study available evaluated green-yellow

vegetables only (and no fruit) and found no association (15).

Overall Evaluation

After the evaluating the evidence presented previously, it

has been concluded that there is limited evidence for a can-

cer-preventive effect of the consumption of fruits and vegeta-

bles for cancer of the mouth and pharynx, esophagus, stom-

ach, colon-rectum, larynx, lung, ovary (vegetables only),

bladder (fruit only), and kidney in humans.

There is inadequate evidence for a cancer-preventive ef-

fect of the consumption of fruits and vegetables for all other

sites.


Figure 11. Cohort studies of colorectal cancer and vegetable consumption. M, males; F, females; CR, colorectal; C, colon; R, rectum. (Reproduced with permis-


Preventable Fraction

The proportion of any disease potentially preventable by

modification of a risk factor in a population is determined by

both the strength of the risk factor, as represented by the rela-

tive risk, and the prevalence of the risk factor. This proportion

is commonly known as the “preventable fraction” (also

sometimes called the “population attributable risk”) (246).

The certainty in any estimate of preventable fraction, includ-

ing that for the fraction of cancers that is due to low intake of

fruits and vegetables, is dependent on the precision of both

the relative risk associated with low intake and the proportion

of the population consuming low levels. It is clear that many

of the relative risk estimates are uncertain and that the preva-

lence of exposure to low intake varies widely across studies

and cancer sites. Therefore, confidence in an estimate of any

particular cancer’s preventable fraction for low fruit and veg-

etable intake must be low.

Nevertheless, we calculated the preventable fractions for

cancer sites for which there was at least limited support for a

causal association to estimate the approximate extent of the

potential prevention that could be linked to increasing fruit

and vegetable intake. Although the relative risks and

prevalences of low intake vary widely between studies, in

many of the studies reviewed, the levels of fruit and vegetable

intake being compared were the highest versus lowest

quartiles or tertiles (that is, range of prevalence of low intake

of 25–33%), and the relative risk estimates were generally in

the range of 20–30% lower risk for subjects in the highest

category of intake. Applying this range of risk difference to

Vol. 54, No. 1 123

Figure 12. Case-control studies of colorectal cancer and vegetable consumption. M, males; F, females; CR, colorectal; C, colon; R, rectum. (Reproduced with

permission from the IARC Handbook of Cancer Prevention, vol 8. Lyon, France: IARC Press, 2003.)


Figure 13. Case-control studies of pancreas cancer and fruit consumption. M, males; F, females. (Reproduced with permission from the IARC Handbook of

Cancer Prevention, vol 8. Lyon, France: IARC Press, 2003.)

Figure 14. Case-control studies of pancreas cancer and vegetable consumption. M, males; F, females. (Reproduced with permission from the IARC Handbook

of Cancer Prevention, vol 8. Lyon, France: IARC Press, 2003.)

Vol. 54, No. 1 125

Figure 15. Case-control studies of larynx cancer and fruit consumption. (Reproduced with permission from the IARC Handbook of Cancer Prevention, vol 8.

Lyon, France: IARC Press, 2003.)

Figure 16. Case-control studies of larynx cancer and vegetable consumption. (Reproduced with permission from the IARC Handbook of Cancer Prevention, vol

8. Lyon, France: IARC Press, 2003.)

the range of prevalence of low intake, the preventable frac-

tion for low fruit and vegetable intake would fall into the

range of 5–12%. It is important to recognize that this is only a

crude range of estimates and that the proportion of cancers

that might be preventable by increasing fruit and vegetable

intake may vary beyond this range for specific cancer sites

and across different regions of the world.

There have been many estimates of the fraction of can-

cer preventable by increasing fruit and vegetable intake

based on individual case-control studies but only two based

on meta-analyses. van’t Veer et al. (247) reviewed pub-

lished studies and estimated the population attributable

risks for all cancer sites due to consumption of 250 g of

fruits and vegetables per day compared with the recom-

mended 400 g/day. They made three estimates based on dif-

ferent assumptions of the size of the relative risks: a “best

guess” estimate (19%), an “optimistic” estimate (28%), and

a “conservative” estimate (6%). Riboli and Norat (248) es-

timated the preventable fractions for esophageal, stomach,

and colorectal cancers in various populations around the

world using relative risks derived from a meta-analysis of

published studies (largely from developed countries) cou-

pled with regional prevalence estimates derived from

sources including FAO data. This approach led to estimates

of the proportion of cancers preventable by increasing fruit

and vegetable intake from current levels to 350 g/day in the

range of 8–16% for colorectal cancer and 20–30% for

esophageal and gastric cancers; these estimates varied sub-

stantially in different regions of the world.

The preventable fraction estimates of 5–12% for the

groups of cancers evaluated here as having limited evidence

for an inverse association with fruit and vegetable consump-

tion are similar to the estimates for all cancer sites made by

van’t Veer et al. (247) and to the estimates for colorectal can-

cer by Riboli and Norat (248), but they are lower than the

Riboli and Norat (248) estimates for esophageal and stomach

cancers. The range of estimates of the fraction of selected

cancers preventable by increasing intake of fruits and vegeta-

bles is only an approximation. The true relative risk for low

intake is quite uncertain given limitations in dietary assess-

ment and in study designs. In addition, the mix of various

cancers as well as the prevalence of low intake can vary sub-

stantially across different populations.

The present estimates for the fraction of selected cancers

preventable by increasing fruit and vegetable intake could

be either high or low. They would be too high if the relative


Figure 17. Cohort studies of lung cancer and fruit consumption. M, males; F, females; I, intervention arm; P, placebo arm. (Reproduced with permission from

the IARC Handbook of Cancer Prevention, vol 8. Lyon, France: IARC Press, 2003.)

risk estimates on which the measure is based are inflated by

biases in study design and/or uncontrolled confounding by

other factors. On the other hand, they would be too low if

the relative risks were underestimated because of

misclassification arising from random errors in estimating

dietary intake. In addition, benefits of increasing fruit and

vegetable intake may well extend beyond those at the low-

est levels of intake. Shifting the diets of entire populations

over long periods to lower levels of risk can have a greater

impact on population health than reducing risk only for a

subgroup at highest risk (249). Increasing fruit and vegeta-

ble intake in populations is likely also to be accompanied

by other beneficial changes in diet composition and in other

chronic diseases.

Acknowledgments and Notes

We thank the participants in the meeting in Lyon in 2003: G. Link, H.

Boeng, T. Byers, L.O. Dragsted, P.J. Elmer, A. Ferro-Luzzi, J.L.

Freudenheim, T. Key, J.W. Lampe, F. Levi, J. Little, A.J. Michael, A.B.

Miller, J. Pennington, B.S. Reddy, R. Saracci, A. Schatzkin, S.

Smith-Warner, G. Stoner, S. Tsugane, P.A. van den Brandt, P. Vineis, and A.

Wolk. We acknowledge the invaluable contribution of the IARC secretariat,

in particular: F. Bianchini, J. Cheney, S. Franceschi, R. Kaaks, T. Norat, E.

Riboli, and N. Slimani. Both authors worked previously at the International

Agency for Research on Cancer (Lyon, France) and participated in the ex-

pert meeting in which the body of this document was written. Harri Vainio

was the chief of the Unit of Cancer Chemoprevention and the main editor of

the IARC Handbooks of Cancer Prevention. Address correspondence to Dr.

E. Weiderpass, The Cancer Registry of Norway, Montebello, N-0310, Oslo,

Norway. Phone: + 358 40 845 3406. FAX: + 47 22 45 13 70. E-mail: ewv@

kreftregisteret.no.

Vol. 54, No. 1 127

Figure 18. Case-control studies of lung cancer and fruit consumption. B, blacks; W, whites; M, males; F, females; A, adenocarcinoma; S, squamous and small

cell carcinoma; Sm, smokers; NonSm, nonsmokers; *, not applicable. (Reproduced with permission from the IARC Handbook of Cancer Prevention, vol 8.



Figure 19. Cohort studies of lung cancer and vegetable consumption. M, males; F, females; I, intervention arm; P, placebo arm. (Reproduced with permission


Figure 20. Case-control studies of lung cancer and vegetable consumption. B, blacks; W, whites; M, males; F, females; Sm, smokers; NonSm, nonsmokers; *,

not applicable. (Reproduced with permission from the IARC Handbook of Cancer Prevention, vol 8. Lyon, France: IARC Press, 2003.)

Vol. 54, No. 1 129

Figure 21. Cohort studies of breast cancer and fruit consumption. pre, premenopausal; post, postmenopausal; I, incidence. (Reproduced with permission from


Figure 22. Case-control studies of breast cancer and fruit consumption. pre, premenopausal; post, postmenopausal; *, not applicable. (Reproduced with permis-



Figure 23. Cohort studies of breast cancer and vegetable consumption. pre, premenopausal; post, postmenopausal; I, incidence. (Reproduced with permission


Figure 24. Case-control studies of breast cancer and vegetable consumption. pre, premenopausal; post, postmenopausal; *, not applicable. (Reproduced with

permission from the IARC Handbook of Cancer Prevention, vol 8. Lyon, France: IARC Press, 2003.)

Vol. 54, No. 1 131

Figure 25. Case-control studies of endometrial cancer and fruit consumption. (Reproduced with permission from the IARC Handbook of Cancer Prevention,

vol 8. Lyon, France: IARC Press, 2003.)

Figure 26. Case-control studies of endometrial cancer and vegetable consumption. (Reproduced with permission from the IARC Handbook of Cancer Preven-

tion, vol 8. Lyon, France: IARC Press, 2003.)


Figure 27. Cohort studies of prostate cancer and fruit consumption. *, not applicable. (Reproduced with permission from the IARC Handbook of Cancer Pre-

vention, vol 8. Lyon, France: IARC Press, 2003.)

Figure 28. Case-control studies of prostate cancer and fruit consumption. (Reproduced with permission from the IARC Handbook of Cancer Prevention, vol 8.


Vol. 54, No. 1 133

Figure 29. Cohort studies of prostate cancer and vegetable consumption. *, not applicable. (Reproduced with permission from the IARC Handbook of Cancer

Prevention, vol 8. Lyon, France: IARC Press, 2003.)

Figure 30. Case-control studies of prostate cancer and vegetable consumption. (Reproduced with permission from the IARC Handbook of Cancer Prevention,



Figure 31. Cohort studies of bladder cancer and fruit consumption. (Reproduced with permission from the IARC Handbook of Cancer Prevention, vol 8. Lyon,

France: IARC Press, 2003.)

Figure 32. Case-control studies of bladder cancer and fruit consumption. (Reproduced with permission from the IARC Handbook of Cancer Prevention, vol 8.


Vol. 54, No. 1 135

Figure 33. Cohort studies of bladder cancer and vegetable consumption. (Reproduced with permission from the IARC Handbook of Cancer Prevention, vol 8.


Figure 34. Case-control studies of bladder cancer and vegetable consumption. (Reproduced with permission from the IARC Handbook of Cancer Prevention,



Figure 35. Case-control studies of renal cell cancer and fruit consumption. M, males; F, females. (Reproduced with permission from the IARC Handbook of

Cancer Prevention, vol 8. Lyon, France: IARC Press, 2003.)

Figure 36. Case-control studies of renal cell cancer and vegetable consumption. M, males; F, females; NonSm, nonsmokers. (Reproduced with permission from


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