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Nutrition and Cancer

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Foods and Food Groups Associated With the Incidence

of Colorectal Polyps: The Adventist Health Study
a a a a
Yessenia M. Tantamango , Synnove F. Knutsen , W. Lawrence Beeson , Gary Fraser &
b
Joan Sabate
a
Department of Epidemiology and Biostatistics , School of Public Health, Loma Linda
University , Loma Linda, California, USA
b
Department of Epidemiology and Biostatistics; and Department of Nutrition, School of
Public Health , Loma Linda University , Loma Linda, California, USA
Published online: 04 May 2011.

To cite this article: Yessenia M. Tantamango , Synnove F. Knutsen , W. Lawrence Beeson , Gary Fraser & Joan Sabate (2011)
Foods and Food Groups Associated With the Incidence of Colorectal Polyps: The Adventist Health Study, Nutrition and Cancer,
63:4, 565-572

To link to this article: http://dx.doi.org/10.1080/01635581.2011.551988

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 Nutrition and Cancer, 63(4), 565–572
Copyright
C 2011, Taylor & Francis Group, LLC

ISSN: 0163-5581 print / 1532-7914 online

DOI: 10.1080/01635581.2011.551988

Foods and Food Groups Associated With the Incidence

of Colorectal Polyps: The Adventist Health Study
Yessenia M. Tantamango, Synnove F. Knutsen, W. Lawrence Beeson,
and Gary Fraser
Department of Epidemiology and Biostatistics, School of Public Health, Loma Linda University,
Loma Linda, California, USA

Joan Sabate
Department of Epidemiology and Biostatistics; and Department of Nutrition, School of Public Health,
Loma Linda University, Loma Linda, California, USA
Downloaded by [University of Illinois Chicago] at 03:27 11 November 2014

past 2 decades. This decrease reflects an increase in screen-

Colorectal cancer (CRC) is a leading cause of cancer death in the ing that allows the detection and removal of colorectal polyps
United States. The majority of CRC arise in adenomatous polyps before they progress to cancer (2). Since colon polyps are
and 25–35% of colon adenoma risk could be avoidable by modify- found in populations with high incidence of CRC, it is be-
ing diet and lifestyle habits. We assessed the association between
lieved they share a common etiopathogenesis (3). Therefore, it
diet and the risk of self-reported physician-diagnosed colorectal
polyps among 2,818 subjects who had undergone colonoscopy. Sub- is important to focus our attention on the prevention of colon
jects participated in 2 cohort studies: the AHS-1 in 1976 and the adenomas.
AHS-2 from 2002–2005. Multivariate logistic regression analysis Results from international and correlational studies suggest
was used to estimate the period risk of incident cases of polyps; that environmental factors, especially dietary factors, play a vi-
441 cases of colorectal polyps were identified. Multivariate analy-
sis adjusted by age, sex, body mass index, and education showed
tal role in the risk of CRC (4–7). To what degree diet affects
a protective association with higher frequency of consumption of the risk of colon polyps and CRC remains unclear. Many case-
cooked green vegetables (OR 1 time/d vs. <5/wk = 0.76, 95% CI = control (8–12) and prospective studies (13–19) have found a sig-
0.59–0.97) and dried fruit (OR 3+ times/wk vs. <1 time/wk = 0.76, nificant protective association with intake of fruits, vegetables,
95%CI = 0.58–0.99). Consumption of legumes at least 3 times/wk and grains. Other studies (20), including intervention studies
reduced the risk by 33% after adjusting for meat intake. Con-
sumption of brown rice at least 1 time/wk reduced the risk by 40%.
(21,22), on the other hand, have yielded nonsignificant asso-
These associations showed a dose-response effect. High frequency ciations, although most have showed a marginally significant
of consumption of cooked green vegetables, dried fruit, legumes, protective effect.
and brown rice was associated with a decreased risk of colorectal The mechanism for how certain foods may reduce the risk of
polyps. CRC or colon polyps is still unclear. Bioactive components
in plant foods may induce antioxidative properties, thereby
reducing DNA damage, and may activate genes that detox-
INTRODUCTION ify carcinogenes (23), thereby inhibiting carcinogenesis (24).
Colorectal cancer (CRC) is the second leading cause of can- Some studies have concluded that plant foods provide the best
cer mortality in the United States and the third most common polypharmacy against the development of malignancy in tis-
cancer in both men and women; number 3 after prostate can- sues (25,26). However, it seems that there is not a single nu-
cer among males and number 3 after breast cancer among fe- trient that would be responsible for this protection but rather a
males (1). CRC incidence and mortality has decreased over the combination of nutrients. It is also possible that the biological
activity of one may depend on the presence or absence of other
substances.
Submitted 16 July 2010; accepted in final form 6 December 2010. In this study, we prospectively examined the effect of a num-
Address correspondence to Yessenia M. Tantamango, Department
of Epidemiology and Biostatistics, School of Public Health, Loma
ber of different foods and food groups, measured by frequency
Linda University, 24951 North Circle Drive, Nichol Hall, Loma Linda, of consumption, on risk of self-reported colon polyps among
CA 92350: Phone: 909-725-5162. E-mail: [email protected] subjects of the Adventist Health Study-1 cohort (27).

565
 566 Y. M. TANTAMANGO ET AL.

MATERIAL AND METHODS Each of the food items were assessed individually. However,
responses for the various dairy products and meat questions
Study Population
were also summed to form a dairy and meat index. The meat
The study population was composed of the survivor cohort index was determined from responses to 6 questions on the
that responded to 2 lifestyle questionnaires, the Adventist Health current frequency of consumption of specific meat (beef–steak,
Study-1 (AHS-1) administered from 1976–1977, and the Ad- beef–hamburger, other–beef or veal, fish, poultry, and pork), and
ventist Health Study-2 (AHS-2) from 2002–2004. The AHS-1 one question on the current frequency of consumption of any
was designed to examine the risk of cancer, coronary heart dis- meat. This index has been used previously in this population for
ease, and all-cause mortality among non-Hispanic California assessment of associated colon cancer risk (18).
Seventh-Day Adventists (27). The purpose of the AHS-2 was to
provide more precise and comprehensive results investigating Case Ascertainment
the relationship between selected foods and the risk of can- Assessment of colorectal polyps was performed using the
cer (28). Details of how respondents to these 2 cohort studies baseline AHS-2 lifestyle questionnaire. This included questions
were identified and their information linked have been described on whether they had ever had a colonoscopy. They were also
elsewhere (29). Information obtained from these studies (AHS- asked about whether they had been told by a physician that
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1 and AHS-2) was considered protected health information and they had any of a number of specific conditions including “rec-
authorized by the Loma Linda University Institutional Review tal/colon polyps.” For each condition, they were also asked to
Board (IRB). specify the approximate time frame since first diagnosed with
Briefly, 5,095 subjects participated in these 2 cohort stud- the condition. The 5 time periods since first diagnosis were
ies. For the purpose of this study, we excluded (1) prevalent “less than 5 years ago,” “5 to 9 years ago,” “10 to 14 years
cases of colorectal polyps (82 cases), (2) history of CRC prior ago,” “15 to 19 years ago,” and “20+ years ago.” Those who
to the diagnosis of colon polyps (7 cases), and (3) history of had been diagnosed more than 20 yr ago were considered preva-
inflammatory intestinal conditions such as ulcerative colitis or lent cases in 1976 and were, therefore, excluded from our study
Crohn’s disease (9 cases) and diverticulitis (104 cases). To try population. To ensure higher validity of the self-reported out-
to minimize detection and selection bias, we excluded subjects come, only cases diagnosed after a colonoscopy were used in
who reported never having had a colonoscopy as well as those this study. A total of 590 new cases of rectal/colon polyps were
who reported having a colonoscopy later than the time of di- thus identified during the 26-yr follow-up since enrollment into
agnosis of polyps (n = 2,075). The total number of subjects the AHS-1. After exclusion criteria were applied to the cohort,
excluded was 2,277. Hence, the analytic population consists of 441 incident cases of rectal/colon polyps were included in the
2,818 subjects. analytic population of 2,818 subjects.

Dietary Assessment Statistical Methods

Dietary and lifestyle information was assessed with the use The statistical package SAS version 9.1 was used in all analy-
of a self-administered food-frequency questionnaire (FFQ) from ses. The characteristics of participants with and without incident
the AHS-1 in 1976. This questionnaire included questions on de- rectal/colon polyps were compared by independent t test for con-
mographics, past medical history, and psychosocial factors. The tinuous variables and chi-square test for categorical variables.
dietary section consisted of 55 nonquantitative food-frequency Frequency of intake of various foods was categorized into 3 or
questions in which participants were asked how often, on aver- more meaningful categories for this population and to assure
age, each food or beverage was consumed when following the adequate number of cases in each exposure category as well as
usual routine. Most dietary questions had 8 frequency categories be able to assess trends.
that ranged from “never or almost never” to “more than once Multivariable logistic regression analysis was used to assess
per day.” Variables such as dairy products (whole milk, lowfat the risk of rectal/colon polyps associated with the frequency of
milk, nonfat milk, buttermilk, and cheese), and sweets/desserts consumption of the different food variables. A basic model was
had 7 frequency categories that ranged from “never” to “over initially created for each of the candidate food variables [total
5 times per day.” There were questions about the type of bread meat, total white meat (poultry + fish), total red meat (beef +
consumed, with options being “white only,” “100% whole wheat pork), poultry, fish, pork, beef, salad, cooked green vegetables,
only,” “sprouted only,” “other only,” “combination of white and tomatoes, legumes, nuts, dried fruit, citrus fruit, winter fruit,
whole wheat or sprouted wheat bread,” “combination of white other seasonal fruit, brown rice, white rice, bread, total dairy
plus other only,” “combination of whole wheat plus sprouted products, cheese, whole milk, lowfat milk, nonfat milk, eggs,
wheat only,” “combination of whole wheat or sprouted wheat and sweets intake] controlling for age, gender, and body mass
plus other,” and “combination of white plus whole wheat or index (BMI). Only the food variables that showed a statistically
sprouted wheat plus other type of bread.” These bread cate- significant association with rectal/colon polyps were kept to be
gories were then collapsed into 3: “white,” “whole wheat,” and assessed, individually, in a multivariate model that adjusted for
“other.” possible confounders, which included family history of CRC
 FOOD GROUPS AND INCIDENCE OF COLORECTAL POLYPS 567

(birth mother or birth father with CRC), education, physical TABLE 1

activity level, alcohol, smoking, constipation, intake of sweets, Baseline subject characteristics among subjects with (cases)
pain medication, multivitamins, and the different food variables. and without (noncases) rectal/colon polyps (The Adventist
All possible confounders, which also included food variables, Health Study, California, 1976–2002)
were introduced into these new models one at the time. Only
those variables that changed the main effect of the exposure Cases Noncases P
of interest 10% or more were included in the final model (30). Characteristic (n = 441) (n = 2,377) Value
None of the nonfood variables changed the main effect of the Age (mean ± SD) 73.4 ± 9.2 71.2 ± 9.7 <.01
exposure of interest, but among the food variables, only meat Body mass index (kg/m2)
intake met this criterion when assessing the effect of legume ≤23.2 39.8% 50.1% <.01
consumption. Likewise, salad intake changed the main effect 23.3–≤ 25.8 31.8% 26.3%
of brown rice. Therefore, these variables were included in the 25.9 + 28.4% 23.6%
final model. Education did not change the main effect of the Gender
food variables assessed, but it was included in the final model Female 52.2% 61.2% <.01
to adjust for socioeconomic status. Male 47.8% 38.8%
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To investigate a possible relationship between the different Family history (1st degree) of CRC
food variables and age, gender, or BMI, we also tested for a Yes 9.7% 5.0% <.01
multiplicative interaction using in the model the product term No 90.3% 95.0%
“food” × age, “food” × gender, and “food” × BMI. Education
≤High school 14.8% 15.8% .73
Some college 39.6% 40.6%
College graduate + 45.6% 43.6%
RESULTS Physical activity
During an average of 26 yr of follow-up, a total of 441 cases None 32.4% 26.9% .07
of rectal/colon polyps were identified in the analytic population Low 12.7% 15.9%
of 2,818 subjects. Moderate 18.1% 20.0%
Nondietary characteristics of the study population are pre- Vigorous 36.8% 37.2%
sented in Table 1. Rectal/colon polyp cases were older, had Alcohol
higher BMI, and tended to be more educated (college graduates Never 90.8% 93.5% .04
or more) than noncases. A higher proportion of cases reported Ever 9.2% 6.5%
positive family history of CRC among first-degree relatives, and Smoking
more men reported incident rectal/colon polyps than women. No Never 83.3% 85.5% .22
significant difference was found between cases and noncases for Ever 16.7% 14.5%
physical activity, constipation, use of pain medication, or use of Constipation
multivitamins. Never 8.8% 8.5% .79
Table 2 shows the association between food variables and Ever 91.2% 91.5%
rectal/colon polyps risk assessed in the basic model with ad- Pain medication
justment for age, gender, and BMI. In this population, where Never 96.3% 97.1% .38
more than 60% of the cases were vegetarians or nearly so (eat Ever 3.7% 2.9%
meat <1/wk) (Table 2), inverse associations were found for the Aspirin use
frequency of consumption of cooked green vegetables, legumes, Noncurrent 84.1% 82.1% .34
dried fruit, and brown rice. These associations were statistically 1+/wk 15.9% 17.9%
significant when comparing the highest vs. the lowest category Multivitamin
of intake. A dose-response effect (P trend < 0.05) was also Never 58.3% 59.7% .59
evident for these exposure factors. Ever 41.7% 40.3%
After controlling for the selected confounding factors and
education (Table 3), cooked green vegetables were associated
with a 24% reduction in the risk of rectal/colon polyps when
comparing intakes of 1 time/day or more with <5 times/wk (P
trend = .03). A dose-response effect (P trend = .02) was also least once a wk reduced the risk of rectal/colon polyps by about
evident for legume intake with a clear protective association. 40%. A dose-response effect was also evident.
When comparing dried fruit intake of 3 times/wk or more vs. When tested for a multiplicative interaction term between the
<1 time/wk, a 26% reduced risk of rectal/colon polyps was different food variables and age, gender, and BMI, no statistical
observed (P trend = .03). Finally, consumption of brown rice at significance was attained.
 568 Y. M. TANTAMANGO ET AL.

TABLE 2
Adjusted∗ odds ratio (OR) of rectal/colon polyps according to specific foods (The Adventist Health Study, California, 1976–2002)
Variable Cases OR 95% CI P Trend Variable Cases OR 95% CI P Trend
Total meat intake Winter fruit
Never 168 1.00 .76 <3/wk 105 1.00 .92
>0–<1/wk 111 1.06 0.80–1.41 3–6/wk 198 0.87 0.66–1.06
1+/wk 162 1.04 0.80–1.35 1+/day 138 0.99 0.74–1.35
Poultry Other fruit
Never 214 1.00 .56 <1/wk 100 1.00 .18
>0–<1/wk 187 1.03 0.82–1.30 1–2/wk 118 0.85 0.63–1.17
1+/wk 40 1.13 0.77–1.68 3+/wk 223 0.82 0.62–1.08
Beef Brown rice
Never 202 1.00 .62 Never 102 1.00 .02†
>0–<1/wk 112 0.89 0.68–1.16 <1/month 121 0.94 0.69–1.28
1+/wk 127 1.09 0.84–1.41 1–2/month 152 0.84 0.62–1.13
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Fish 1+/wk 66 0.67 0.47–0.95∗

Never 215 1.00 .64 White rice
>0–<1/wk 187 0.94 0.75–1.18 Never 128 1.00 .67
1+/wk 39 1.25 0.85–1.85 <1/month 113 1.14 0.85–1.53
White meat 1–2/m 154 1.22 0.93–1.61
Never 191 1.00 .40 1+/wk 46 0.93 0.63–1.36
>0–<1/wk 187 0.92 0.73–1.16 Bread
1+/wk 63 1.27 0.92–1.77 White 28 1.00 .69
Red meat Wheat 269 0.88 0.56–1.39
Never 202 1.00 .64 Other 141 0.97 0.60–1.56
>0–<1/wk 112 0.89 0.68–1.16 Cheese
1+/wk 127 1.08 0.84–1.41 <1/wk 118 1.00 .74
Salad 1–2/wk 163 0.85 0.65–1.12
<5/wk 168 1.00 .94 >2/wk 160 0.94 0.71–1.24
5–6/wk 108 0.95 0.72–1.26 Whole milk
1+/day 165 1.01 0.79–1.30 Never 169 1.00 .26
Cooked green vegetables <1/wk–<1/day 162 0.97 0.76–1.24
<5/wk 193 1.00 .03† 1+/day 110 1.20 0.91–1.58
5–6/wk 102 0.78 0.59–1.04 Lowfat milk
1+/day 146 0.76 0.60–0.98 Never 187 1.00 .23
Tomatoes <1/wk–<1/day 114 0.95 0.72–1.24
<3/wk 144 1.00 .93 1+/day 140 0.86 0.67–1.10
3–4/wk 147 0.89 0.68–1.16 Nonfat milk
5+/wk 150 1.01 0.78–1.32 Never 270 1.00 .26
Legumes <1/wk–<1/day 86 0.87 0.66–1.16
<1/month 48 1.00 1+/day 85 0.87 0.67–1.15
1/mo–3/wk 294 0.96 0.68–1.35 .05 Eggs
3+/wk 99 0.73 0.49–1.08 <1/wk 174 1.00 .32
Nuts 1–2/wk 185 0.88 0.69–1.11
<1/wk 147 1.00 2+/wk 82 0.88 0.65–1.19
1–4/wk 195 0.78 0.62–1.02 .19 Dairy
5+/wk 99 0.84 0.62–1.13 <1/day 57 1.00 .55
Dried fruit 1/day–<2/day 152 1.04 0.73–1.48
<1/wk 189 1.00 .03† 2+/day 232 0.95 0.68–1.32
1–2 /wk 119 0.77 0.59–1.006 Sweets
3+/wk 133 0.76 0.58–0.98 <1/wk 66 1.00 .10
Citrus fruit 1–2/wk 141 1.08 0.77–1.51
<1/wk 156 1.00 .58 3–6/wk 148 1.18 0.84–1.66
1–2/wk 137 1.001 0.77–1.31 1+/day 86 1.32 0.91–1.92
3+/wk 148 0.93 0.71–1.21
∗
Adjusted by age, gender, and body mass index.
†
P value < 0.05.
 FOOD GROUPS AND INCIDENCE OF COLORECTAL POLYPS 569

TABLE 3 with high vs. low intake of green vegetables. A case-control

Final multivariate adjusted model with odds ratio for study performed on southern Californians also found that fre-
rectal/colon polyps according to selected dietary factors (The quent consumption of green vegetables, fruits (including raisins
Adventist Health Study, California, 1976–2002) and prunes), and grains (including brown rice) was associated
with a decrease in polyp prevalence (9).
Variable OR 95% CI P (Trend) Many hypotheses have been developed to explain the rela-
Cooked green vegetablesa tionship between diet and the risk of CRC (44–46). For the most
<5/wk 1.00 Reference .03† part, dietary factors that correlate with a predisposition to colon
5–6/wk 0.78 0.59–1.04 cancer are also associated with a risk of colon adenoma (47).
1+/day 0.76 0.59–0.97 Thus, it is possible that the same hypotheses that relate diet to
Legumesb CRC may also explain its relationship with colon adenomas.
<1/mo 1.00 Reference .02† These hypotheses tend to be based on the concept of high-risk
1/mo–3/wk 0.90 0.62–1.30 diets, which may either contain high levels of carcinogens or
3+/wk 0.67 0.44–1.01 lack one or more anticarcinogenic protective factors. It is also
Dried fruitc well known that diets with a high intake of fruits and vegetables
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<1/wk 1.00 Reference .03† contain dietary fiber and phytochemicals that may inhibit colon
1–2/wk 0.77 0.59–1.01 carcinogenesis (48,49).
3+/wk 0.76 0.58–0.99 Diets high in meat intake have been shown in different studies
Brown riced to increase the risk of CRC (18,50–54) and incident (12,55–58)
Never 1.00 Reference .007† and recurrent colon polyps (59). In fact, AHS-1 found that meat
<1/mo 0.94 0.69–1.29 consumption predicted risk of CRC (18). Several mechanisms
1–2/m 0.84 0.63–1.14 have been postulated to explain this (45,48,57–60). However, in
1+/wk 0.60 0.42–0.87 our study we did not find associations between meat intake and
incident polyps, although the confidence intervals still admit
a
Multivariate model adjusted by age, gender, body mass index the possibility of modest effects that we did not detect. It is also
(BMI), and education. possible that meat intake has more of an effect on the progression
b
Multivariate model adjusted by age, gender, BMI, education, and
from polyps to carcinoma, instead of the transition from normal
meat intake.
c to neoplastic mucosa.
Multivariate model adjusted by age, gender, BMI, and education.
d
Multivariate model adjusted by age, gender, BMI, education, and Cruciferous vegetables such as broccoli contain sul-
salad. foraphane, which detoxifies carcinogenic compounds. Also, all
†
P value < 0.05. green plant parts contain chlorophyll, which modifies genotoxic
effects of known toxins (61). Among the most studied bioactive
DISCUSSION compounds of these vegetables associated with cancer protec-
In this 26-yr follow-up study, a higher frequency of con- tion are glucosinolates and isothiocyanates, which induce phase
sumption of cooked green vegetables, legumes, dried fruit, and 2 detoxication enzymes and boost antioxidant status (23,62).
brown rice was associated with a decreased risk of rectal/colon Finally, it has also been reported that some nutrients found in
polyps. these food variables are highly bioavailable after being cooked,
Although many epidemiological studies (9,12,25,31–35) which would improve their protective function (48).
have shown the protective effect of fruits, vegetables, and grains Legumes are a source of fermentable dietary fiber, which is a
on rectal/colon adenoma risk, others have not (20,35,36), or were precursor of luminal butyrate, a compound with antiinflamma-
limited to specific circumstances. In some studies, the protec- tory and antineoplastic properties (63,64). The high fiber content
tive association was limited only to vegetables (11,37,38), fruits would also dilute potential carcinogens by decreasing the over-
(33,39), or grains (40). Finally, others have demonstrated an in- all transit time of the fecal bulk, by binding bile acids (65) or by
verse relationship limited to size (40), number of adenoma (37), a volatile fatty-acid-mediated lowering of the colonic pH that
colon but not rectum (41) or specific colon subsites (37). Ran- could slow conversion of primary to secondary bile acids (66).
domized clinical trials assessing colon polyp recurrence have Other bioactive constituents of legumes that have anticarcino-
not detected an association with these food sources (35,42,43). genic properties and could potentially account for a protective
The differences in findings may be due to specific limitations of effect include saponins, protease inhibitors, inositol hexaphos-
these studies, such as, in the case of experimental studies, the phate, gamma-tocopherol, and phytosterols (67). In addition,
intervention period having been too short to have an effect on legumes have a low glycemic index (GI), which is associated
tumor development. with a reduced risk of CRC (48). It is also possible that there
Similar to our findings, a study conducted by Millen et al. (41) is a specific factor in legumes that modifies one or more of the
as part of the Prostate, Lung, Colorectal, Ovarian (PLCO) Can- hypothesized carcinogenic mechanisms that occur in the colon
cer Screening Program observed a decreased risk of adenoma because of a higher red meat intake, as suggested by the study
 570 Y. M. TANTAMANGO ET AL.

of Singh and Fraser (18). Other studies support our findings nutrients with anticarcinogenic properties will be able to better
of legumes as a protective factor against incidence (14,37) and explain the observed findings.
recurrence (21) of colon polyps.
Dried fruits may be protective mostly due to their high fiber ACKNOWLEDGMENTS
content, which slows glucose absorption and thus promotes bet- The study was supported in part by NIH Grants 2RO1-CA
ter glucose control. The fiber also reduces hyperinsulinemia and 14703-15 and 5RO1 CA 094594.
produces short-chain fatty acids that have been shown to reduce
cancer cell growth in vitro (68).
The protective effect of brown rice may also be explained REFERENCES
due to its high content of fiber. Additionally, its content of 1. American Cancer Society: Cancer Facts and Figures 2010. American Can-
cer Society: Atlanta, GA, 2010.
phytates and protease inhibitors may play an important role in 2. Edwards BK, Ward E, Kohler BA, Eheman C, Zauber AG, et al.: Annual
its protection (48). report to the nation on the status of cancer, 1975–2006, featuring colorec-
The major strength of our study is its prospective de- tal cancer trends and impact of interventions (risk factors, screening, and
sign with 26 yr of follow-up. This eliminates the possibil- treatment) to reduce future rates. Cancer 116, 544–573, 2010.
ity of recall bias when assessing food intake. About 80% of 3. Enders G and El-Deiry WS: Colon polyps. Available at
Downloaded by [University of Illinois Chicago] at 03:27 11 November 2014

http://emedicine.medscape.com/article/172674-overview, 2008.
this population (unpublished information) did not make ma- 4. Armstrong B and Doll R: Environmental factors and cancer incidence and
jor changes in their dietary habits during these years of fol- mortality in different countries, with special reference to dietary practices.
lowup, which also reduces the risk of measurement error in the Int J Cancer 15, 617–631, 1975.
exposure status. The unique lifestyle of the Adventist popula- 5. Honda T, Kai I, and Ohi G: Fat and dietary fiber intake and colon cancer
tion, with a very low percentage of alcohol or smoking habits, mortality: a chronological comparison between Japan and the United States.
Nutr Cancer 33, 95–99, 1999.
reduces the possibility of confounding by these nondietary 6. Locke FB and King H: Cancer mortality risk among Japanese in the United
factors. States. J Natl Cancer Inst 65, 1149–1156, 1980.
Limitations of this study include the possibility that partici- 7. Kono S and Ahn Y: Vegetables, cereals and colon cancer mortality: long-
pants may have overestimated some of their food consumption term trend in Japan. Eur J Cancer Prev 9, 363–365, 2000.
as a result of increased awareness of the potentially beneficial 8. Neugut AI, Garbowski G, Lee WC, Murray T, Nieves JW, et al.: Dietary
risk factors for the incidence and recurrence and recurrence of colorectal
effects on cancer, or due to social desirability. However, this adenomatous polyps. Ann Internal Med 118, 91–95, 1993.
type of misclassification should be nondifferential, biasing the 9. Witte JS, Longnecker M., Bird CL, Lee ER, Frankl HD, et al.: Relation of
results toward the null. Due to the lack of hospital records of vegetable, fruit and grain consumption to colorectal adenomatous polyps.
colonoscopy, there is also the possibility of measurement error Am J Epidemiol 144, 1015–1025, 1996.
in the outcome assessment. But again, this misclassification is 10. Levi F, Pasche C, Lucchini F, and La Vecchia C: Dietary fiber and the risk
of colorectal cancer. Eur J Cancer 37, 2091–2096, 2001.
most likely to be nondifferential, biasing the result toward the 11. Benito E, Cabeza E, Moreno B, Obrador A, and Bosch FX: Diet and
null. Survivors from the baseline AHS-1 study who also en- colorectal adenomas: a case-control study in Majorca. Int J Cancer 55,
rolled in the AHS-2 may have been healthier than the original 213–219, 1993.
cohort, which could bias the estimates of colon polyps risk in 12. Austin GL, Adair LS, Galanko JA, Martin CF, Satia JA, et al.: A diet high
the target population. The AHS-1 FFQ was limited in the total in fruits and low in meats reduces the risk of colorectal adenomas. J Nutr
137, 999–1004, 2007.
number of foods. Moreover, we could not adequately adjust for 13. Mai V, Flood A, Peters U, Lacey J, Schairer C, et al.: Dietary fibre
energy intake, an important known risk factor for colon polyps, and risk of colorectal cancer in the Breast Cancer Detection Demostra-
although we did adjust for BMI. Thus, in order to reach a better tion Project (BCDDP) follow-up cohort. Int J Epidemiol 32, 234–239,
understanding of the roles of individual food groups and nu- 2003.
trients, the use of an improved dietary instrument is required. 14. Michels KB, Giovannucci E, Chan AT, Singhania R, Fuchs CS, et al.: Fruit
and vegetable consumption and colorectal adenomas in the Nurses’ Health
Finally, different physiological mechanisms occur during food Study. Cancer Res 66, 3942–3953, 2006.
transit through the large intestine that may increase exposure to 15. Terry P, Giovannucci E, Michels KB, Bergkvist L, Hansen H, et al.: Fruit,
carcinogens that contribute to cancer risk. We only asked about vegetables, dietary fiber, and risk of colorectal cancer. J Natl Cancer Inst
rectal/colon polyps without asking about the specific site. Thus, 93, 525–533, 2001.
this lack of information on the specific site of the polyps, as well 16. Bingham SA, Day NE, Luben R, Ferrari P, Slimani N, et al.: Dietary fibre in
food and protection against colorectal cancer in the European Prospective
as the lack of histological classification, constitutes another lim- Investigation into Cancer and Nutrition (EPIC): an observational study.
itation of our study. Lancet 361, 1496–1501, 2003.
In conclusion, our findings identify some foods—cooked 17. Hsing AW, McLaughlin JK, Chow W-H, Schuman LM, Co Chien HT,
green vegetables, legumes, dried fruit, and brown rice—as et al.: Risk factors for colorectal cancer in a prospective study among U.S.
significantly inversely associated with the risk of rectal/colon white men. Int J Cancer 77, 549–553, 1998.
18. Singh P and Fraser G: Dietary risk factors for colon cancer in a low-risk
polyps. However, we are aware of the difficulty assessing nu- population. Amer J Epidemiol 148, 761–774, 1998.
tritional factors and the need for additional and better-designed 19. Wakai K, Date C, Fukui M, Tamakoshi K, Watanabe Y, et al.: Dietary fiber
studies. The anticarcinogenic properties of foods are still being and risk of colorectal cancer in the Japan collaborative cohort study. Cancer
explored, and it is possible that interactions between various Epidemiol Biomarkers Prev 16, 668–675, 2007.
 FOOD GROUPS AND INCIDENCE OF COLORECTAL POLYPS 571

20. Smith-Warner SA, Elmer P, Fosdick L, Randall B, Bostick R, et al.: Fruits, 41. Millen AE, Subar AF, Graubard BI, Peters U, Hayes RB, et al.: Fruit and
vegetables, and adenomatous polyps: the Minnesota Cancer Prevention Unit vegetable intake and prevalence of colorectal adenoma in a cancer screening
Case-Control Study. Amer J Epidemiol 155, 1104–1113, 2002. trial. Am J Clin Nutr 86, 1754–1764, 2007.
21. Lanza E, Hartman T, Albert P, Shield R, Slattery M, et al.: High dry 42. Azano T and Mcleod RS: Dietary fiber for the prevention of colorectal ade-
bean intake and reduced risk of advanced colorectal adenoma recurrence nomas and carcinomas. Cochrane Database Syst Rev. 2002; 4: CD003430.
among participants in the polyp prevention trial. J Nutr 136, 1896–1903, 43. Lanza E, BinbingY, Murphy G, Albert PS, Caan B, et al.: The Polyp
2006. Prevention Trial-Continued Follow-up Study: no effect of a lowfat, high-
22. Schatzkin A, Lanza E, Corle D, Lance MP, Iber F, et al.: Lack of effect of a fiber, high-fruit, and -vegetable diet on adenoma recurrence eight years
low-fat, high fiber diet on the recurrence of colorectal adenomas. New Eng after randomization. Cancer Epidemiol Biomarkers Prev 19, 1745–1752,
J Med 342, 1149–1155, 2000. 2007.
23. Finley JW: Proposed criteria for assessing the efficacy of cancer reduction 44. Bruce WR, Giacca A, and Medline A: Possible mechanisms relating diet
by plant foods enriched in carotenoids, glucosinolates, polyphenols and and risk of colon cancer. Cancer Epidemiol Biomarkers Prev 9, 1271–1279,
selenocompounds. Ann Botany 95, 1075–1096, 2005. 2000.
24. Valko M, Rhodes CJ, Moncol J, Izakovic M, and Mazur M: Free radi- 45. Johnson IT and Lund EK: Nutrition, obesity and colorectal cancer. Aliment
cals, metals and antioxidants in oxidative stress-induced cancer. Chem Biol Pharmacol Ther 26, 161–181, 2007.
Interact 160, 1–40, 2006. 46. Potter JD: Colorectal cancer: molecules and populations. J Natl Cancer
25. Millen AE, Subar AF, Graubard BI, Peters U, Hayes RB, et al.: Fruit and Inst, 91, 916–932, 1999.
vegetable intake and prevalence of colorectal adenoma in a cancer screening 47. Itzkowitz S and Rochester J: Colonic polyps and polyposis syndromes. In:
Downloaded by [University of Illinois Chicago] at 03:27 11 November 2014

trial. Am J Clin Nutr 86, 1754–1764, 2007. Felman: Sleisenger & Fordtran’s Gastrointestinal and Liver Disease, 8th
26. Potter JD: Cancer prevention: Epidemiology and experiment. Cancer Lett ed., WB Saunders, Philadelphia, 2006, pp. 2713–2757.
114, 7–9, 1997. 48. World Cancer Research Fund /American Institute for Cancer Research:
27. Beeson WL, Mills PK, Phillips RL, Andrews M, and Fraser GE: Chronic Food, nutrition, physical activity and the prevention of cancer: a global
disease among Seventh-Day Adventists, a low risk group. Rationale, perspective. In: Vegetables, Fruits, Pulses (Legumes), Nuts, Seeds, Herbs,
methodology, and description of the population. Cancer (Phila) 64, Spices. American Institute for Cancer Research: Washington, DC, pp.
570–581, 1989. 66–116, 2007.
28. Butler TL, Fraser G, Beeson WL, Knutsen SF, Herring RP, et al.: Cohort 49. Steinmetz KA and Potter JD: Vegetables, fruit and cancer. II. Mechanisms.
profile: the Adventist Health Study-2 (AHS-2). Int J Epidemiol 37, 260–265, Cancer Causes Control 2, 427–442, 1991.
2008. 50. Hsing AW, McLaughlin JK, Chow W-H, Schuman LM, Co Chien HT et al.:
29. Thorpe DL, Knutsen S, Beeson WL, and Fraser GE: The effect of vigorous Risk factors for colorectal cancer in a prospective study aming U.S. white
physical activity and the wrist fracture over 25 years in a low-risk survivor men. Int J Cancer 77, 549–553, 1998.
cohort. J Bone Miner Metab 24, 476–483, 2006. 51. Singh P and Fraser G: Dietary risk factors for colon cancer in a low-risk
30. Rothman KJ: Using regression models in epidemiologic analysis. In: Epi- population. Amer J Epidemiol 148, 761–774, 1998.
demiology: An Introduction. New York: Oxford University Press 2002, pp. 52. Bidoli E, Franceschi S, Talamini R, Barra S, and La Vecchia C: Food
193–197. consumption and cancer of the colon and rectum in northeastern Italy. Int
31. Park Y, Subar AF, Kipnis V, et al.: Fruit and vegetable intakes and risk of J Cancer 50, 223–229, 1992.
colorectal cancer in the NIH–AARP Diet and Health Study. Am J Epidemiol 53. Butler LM, Sinha R, Millikan RC, Martin CF, Newman B, et al.: Het-
166, 170–180, 2007. erocyclic amines, meat intake, and association with colon cancer in a
32. Jacobs E, Lanza E, Alberts DS, Chiu-Hsieh H, Jiang R, et al.: Fiber, sex, population-based study. Am J Epidemiol 157, 434–445, 2003.
and colorectal adenoma: results of a pooled analysis. Am J Clin Nutr 83, 54. Norat T, Binghan S, Ferrari P, Slimani N, Jenab M, et al.: Meat, fish, and
343–349, 2006. colorectal cancer risk: the European Prospective Investigation into Cancer
33. Platz EA, Giovannucci E, Rimm EB, Rockett HR, Stampfer MJ, et al.: and Nutrition. J Nat Cancer Inst 97, 906–915, 2005.
Dietary fiber and distal colorectal adenoma in men. Cancer Epidemiol 55. Yoon H, Benamouzig R, Little J, Francois-Collange M, and Tome D: Sys-
Biomarkers Prev 6, p. 661–670, 1997. tematic review of epidemiological studies on meat, dairy products, and egg
34. Michels KB, Giovannucci E, Chan AT, Singhania R, Fuchs CS, et al.: Fruit consumption and risk of colorectal denomas. Eur J Cancer Prev 9, 151–164,
and vegetable consumption and colorectal adenomas in the Nurses’ Health 2000.
Study. Cancer Res 66, 3942–3953, 2006. 56. Giovannucci E, Stampfer M, Colditz G, Rimm EB, and Willett WC: Rela-
35. Schatzkin A, Lanza E, Corle D, Lance MP, Iber F, et al.: Lack of effect of a tionship of diet to risk of colorectal adenoma in men. J Natl Cancer Inst
low-fat, high fiber diet on the recurrence of colorectal adenomas. New Eng 84, 91–98, 1992.
J Med 342, 1149–1155, 2000. 57. Probst-Hensch N, Sinha R, Longnecker MP, Witte JS, Ingles SA, et al.:
36. Michels KB, Giovannucci E, Joshipura KJ, Rosner BA, Stampfer MJ, et al.: Meat preparation and colorectal adenomas in a large sigmoidoscopy-based
Prospective study of fruit and vegetable consumption and incidence of colon case-control study in California (United States). Cancer Causes Control
and rectal cancers. J Natl Cancer Inst 92, 1740–1752, 2000. 8,175–183, 1997.
37. Kato I, Tominaga S, Akira M, Yoshii Y, Shirai M, et al.: A comparative 58. Wu K, Giovannucci E, Byrne C, Platz EA, Fuchs C, et al.: Meat mutagens
case-control study of colorectal cancer and adenoma. Jpn J Cancer Res 81, and risk of distal colon adenoma in a cohort of U.S. men. Cancer Epidemiol
1101–1108, 1990. Biomarkers Prev 15, 1120–1125, 2006.
38. Kune G, Kune S, Read AE, MacGowan K, Penfold C, et al.: Colorectal 59. Martinez ME, Jacobs E, Ashbeck EL, Sinha R, Lance P, et al.: Meat in-
polyps, diet, alcohol, and family history of colorectal cancer: a case-control take, preparation methods, mutagens and colorectal adenoma recurrence.
study. Nutr Cancer 16, 25–30, 1991. Carcinogenesis 28, 2019–2027, 2007.
39. Macquart-Moulin G, Riboli E, Cornee J, Kaaks R, and Berthezene P: Col- 60. Giovannucci E and Goldin E: The role of fat, fatty acids, and total en-
orectal polyps and diet: a case-control study in Marseilles. Int J Cancer 40, ergy intake in the etiology of human colon cancer. Amer J Clin Nutr 66,
179–188, 1987. 1564S–1571S, 1997.
40. Kono S, Imanishi K, Shinchi K, and Yanai F: Relationship of diet to small 61. Sarkar D, Sharma A, and Talukder G: Chlorophyll and cholo-
and large adenomas of the sigmoid colon. Jpn J Cancer Res 84, 13–19, phyllin as modifiers or genotoxic effects. Mut Res 318, 239–247,
1993. 1994.
 572 Y. M. TANTAMANGO ET AL.

62. Shapiro TA, Fahey J, Wade CW, Stephenson KK, and Talalay P: Chemopro- 65. Potter JD: Nutrition and colorectal cancer. Cancer Causes Control 7,
tective glucosinolates and isothiocyanates of broccoli sprouts: metabolism 127–146, 1996.
and excretion in humans. Cancer Epidemiol Biomarkers Prev 10, 501–508, 66. Topping DL and Clifton PM: Short-chain fatty acids and human colonic
2001. function: roles of resistant starch and nonstarch polysaccharides. Physiol
63. Tong X, Yin L, and Giardina C: Butyrate suppresses Cox-2 activation in Rev 81, 1031–1064, 2001.
colon cancer cells through HDAC inhibition. Biochem Biophys Res Com- 67. Peipins LA and Sandler RS: Epidemiology of colorectal adenomas. Epi-
mun 317, 463–471, 2004. demiol Rev 16, 273–297, 1994.
64. Videla S, Villaseca J, Antolin M, Garcia-Lafuente A, Guarner F, et al.: 68. Gamet L, Daviaud D, Denis-Pouxviel C, Remesy C, and Murat JC: Effects
Dietary insulin improves distal colitis induced by dextran sodium sulfate in of short-chain fatty acids on growth and differentiation of the human colon
the rat. Am J Gastroenterol 96, 1486–1493, 2001. cancer cell line HT29. Int J Cancer 52, 286–289, 1992.
Downloaded by [University of Illinois Chicago] at 03:27 11 November 2014