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American Journal of Epidemiology Advance Access originally published online on September 6, 2007
American Journal of Epidemiology 2007 166(10):1116-1125; doi:10.1093/aje/kwm197
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American Journal of Epidemiology © The Author 2007. Published by the Johns Hopkins Bloomberg School of Public Health. All rights reserved. For permissions, please e-mail: journals.permissions@oxfordjournals.org.

Fish Consumption, n-3 Fatty Acids, and Colorectal Cancer: A Meta-Analysis of Prospective Cohort Studies

Anouk Geelen1, Jannigje M. Schouten1, Claudia Kamphuis1, Bianca E. Stam1, Jan Burema1, Jacoba M. S. Renkema2, Evert-Jan Bakker3, Pieter van't Veer1 and Ellen Kampman1

1 Division of Human Nutrition, Wageningen University, Wageningen, The Netherlands
2 Wageningen UR Library, Wageningen University and Research Centre, Wageningen, The Netherlands
3 Mathematical and Statistical Methods Group, Wageningen University, Wageningen, The Netherlands

Correspondence to Dr. Anouk Geelen, Division of Human Nutrition, Wageningen University, P.O. Box 8129, 6700 EV Wageningen, the Netherlands (e-mail: anouk.geelen{at}wur.nl).

Received for publication January 30, 2007. Accepted for publication June 1, 2007.


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 
Animal studies show favorable effects of n-3 fatty acids on inflammation and cancer, but results from epidemiologic studies appear to be inconsistent. The authors conducted meta-analyses of prospective cohort studies that evaluated the association between fish consumption or n-3 fatty acids and colorectal cancer incidence or mortality. Random-effects models were used, and heterogeneity between study results was explored through stratified analyses. The pooled relative risks for the highest compared with the lowest fish consumption category were 0.88 (95% confidence interval: 0.78, 1.00) for colorectal cancer incidence (14 studies) and 1.02 (95% confidence interval: 0.90, 1.16) for colorectal cancer mortality (four studies). The pooled relative risks for colorectal cancer incidence were 0.96 (95% confidence interval: 0.92, 1.00) for each extra occurrence of fish consumption per week (seven studies) and 0.97 (95% confidence interval: 0.92, 1.03) for each extra 100 g of fish consumed per week (four studies). Stratified analysis showed that the pooled relative risk for colorectal cancer incidence was more pronounced for women and in studies with a large exposure contrast. In cohort studies, fish consumption was shown to slightly reduce colorectal cancer risk. Existing evidence that n-3 fatty acids inhibit colorectal carcinogenesis is in line with these results, but few data are available addressing this association.

cohort studies; colorectal neoplasms; fatty acids, omega-3; fishes; meta-analysis

Abbreviations: CI, confidence interval


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 
Colorectal cancer is the third most common cancer worldwide, with 945,000 new cases and 492,000 deaths yearly. This cancer is more common in developed than in developing countries (1). International variations in diet and colorectal cancer rates suggest that diet is an important preventable risk factor for colorectal cancer. The best established diet-related risk factors are overweight and processed and red meat, while dairy products and plant products may reduce risk (2).

Consumption of fish rich in n-3 fatty acids is suggested to reduce colorectal cancer risk through inhibition of the arachidonic acid cascade that plays a role in inflammation and has been linked to carcinogenesis (3). In 1997, the World Cancer Research Fund and the American Institute for Cancer Research published an extended review of observational studies on nutrition and cancer (4). They concluded that diets high in fish possibly have no association with the risk of colorectal cancer. This conclusion was based on the following 15 studies available until then. Three cohort studies (5–7) and eight case-control studies (8–15) did not find substantial associations between fish consumption and the risk of colon cancer. However, four case-control studies suggested that higher fish consumption might be associated with a reduced risk (16–19). Since 1997, several observational studies on fish consumption and colorectal cancer risk have been published. Prospective cohort studies are assumed to provide better evidence than case-control studies since they are not biased by recall of past dietary habits after cancer has been diagnosed. Furthermore, heterogeneity between study results may be assumed to be smaller, focusing on one study design.

Therefore, we decided to focus this meta-analysis on results from prospective cohort studies only to determine the pooled association between fish consumption or n-3 fatty acids and colorectal, colon, and rectal cancer incidence or mortality. Between-study heterogeneity could be expected to be present because the ranges of intake of fish are likely to differ between study populations. Moreover, population characteristics may be different as well. Stratified analyses might give some explanation for the observed heterogeneity and were conducted to investigate whether the association is more pronounced in certain subgroups.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 References
 
Search strategy
This meta-analysis of colorectal cancer was conducted within the framework of the second World Cancer Research Fund report, to be published in 2007. To ensure comprehensive retrieval of relevant papers, an information specialist conducted multidatabase searches of the following databases: Medline (via PubMed; National Library of Medicine, Bethesda, Maryland), Embase (Elsevier, Amsterdam, the Netherlands), ISI Web of science (Institute for Scientific Information, Philadelphia, Pennsylvania), Biological Abstracts (BIOSIS; Thomson Scientific, Stamford, Connecticut), Pascal (CNRS/INIST, Vandoeuvre-les-Nancy, France), National Research Register (NRR; Update Software Ltd., Oxford, United Kingdom), Latin American and Caribbean Center on Health Sciences Information (LILACS; Centro Latino-Americano e do Caribe de Informação em Ciências da Saúde, São Paulo, Brazil), Cochrane Library (Wiley, Chichester, United Kingdom), Current Contents (Institute for Scientific Information), and CAB Abstracts (CAB International, Wallingford, United Kingdom). We searched for all papers published until January 2006. The exposure search strategy was constructed to identify human observational and experimental studies reporting on the association between food, nutrition, and physical activity. The initial search was kept broad to capture all relevant publications. Details are available on request.

This search was combined with the search question for colorectal cancer, which was, for PubMed: (colorectal neoplasms[MeSH] OR intestinal polyps[MeSH] OR adenomatous polyps[MeSH]) OR ((benign*[tiab] OR malign*[tiab] OR neoplasm*[tiab] OR carcinoma*[tiab] OR cancer*[tiab] OR tumor*[tiab] OR tumour*[tiab] OR polyp*[tiab] OR adenom*[tiab]) AND (colon[tiab] OR colonic[tiab]) OR rectum[tiab] OR rectal[tiab] OR colorectum[tiab] OR colorectal[tiab] OR large bowel[tiab] OR large intestine*[tiab] OR gut[tiab]). ([tiab] searches the title and abstract fields only, [MeSH] searches the Medical Subject Headings field only, and the truncation symbol * searches all words with this combination of letters at the beginning.) The search strategy was adapted for other databases to fit database-specific features.

Selection of papers
Prospective cohort studies on colorectal cancer that included data on the exposures "fish" or "n-3 fatty acids" were considered eligible for meta-analysis. From all hits from the literature search, eligible papers were selected in a stepwise manner by a team of trained reviewers. The first selection step was based on title and keywords. If these items suggested that the reference concerned colorectal cancer or cancer in general and any food, nutrition, or physical-activity-related exposure, the reference was selected for the next step. In this second step, the decision to include or exclude this citation was based on the abstract. For the third selection step, the remaining full papers were read to determine whether they reported on human studies concerning colorectal cancer and food, nutrition, or physical activity. Abstracts for which the full article was not available were not included in the meta-analysis.

For this paper, the final selection step was carried out by one of the authors (A. G.) to select all prospective cohort studies (including nested case-control studies and case-cohort studies) that examined the association between fish consumption or n-3 fatty acid intake and colorectal cancer incidence and mortality. We made an explicit effort to include articles written in languages other than English. In addition, hand searches were undertaken to identify possible additional references not detected in the database searches.

Data extraction
Study characteristics and results of individual studies were extracted from included papers and were entered into a database. This database was developed within the framework of the systematic literature review in support of the upcoming revision of the World Cancer Research Fund International's report on diet, nutrition, physical activity, and cancer. Extracted data from a random 33 percent sample of included papers were checked by a second reviewer. Furthermore, a standardized data cleaning step preceded statistical analysis. This step consisted of a set of STATA commands (Stata Corporation, College Station, Texas) programmed by the review team as a tool to confirm correct data extraction. It was developed to systematically identify and correct the most frequently occurring extraction inaccuracies.

Selection of estimates for meta-analysis
If multiple publications on identical studies were found, only the main study or the most recent one with the longest follow-up was included. If one study presented estimates for different independent populations, for example, for men and women separately, data from both strata were included in the meta-analysis. When several estimates for the same exposure were presented, but they were different regarding their level of adjustment, the most adjusted estimate was chosen as the best one, unless the paper indicated that additional adjustment did not alter the results. In our analyses of colorectal cancer, we used estimates for the outcome colorectal cancer or, if these were not present, estimates on colon cancer. In our analyses of n-3 fatty acids, we used estimates for the exposure n-3 fish fatty acids or, if these were not present, estimates on (total) n-3 fatty acids or on docosahexaenoic acid.

Data analysis
We performed meta-analyses of risk estimates comparing the highest category of exposure with the lowest category. The highest intake groups were defined as the top quantile or highest category (if categories were not of equal size) reported in the studies or the "yes" category from qualitative exposure data. We also conducted "per-unit" meta-analyses of risk estimates for a continuous increase in exposure. When possible, we calculated the relative risk per unit of one time a week or 100 g a week of fish intake (20, 21). The meta-analyses were performed by using random-effects models. This model takes into account both study sample size and between-study variation when weighing study effects and allows for different true effects between studies (22, 23). We quantified the extent of heterogeneity by using I2, the percentage of total variation across studies attributable to heterogeneity between studies rather than sampling variation within studies (24). If results from at least 10 studies were available, stratified analyses were carried out for the subgroups publication year (before or since 1997; the cutoff point was the publication year of the first World Cancer Research Fund report (4)), gender (men, women, both), geographic region (Europe, United States, or other), and difference between highest and lowest intake categories (consumption of fish <7 or ≥7 times/month). We created Begg's and Egger's funnel plots to detect small study bias. We carried out sensitivity analysis and reanalyzed the data by excluding one large study that tended to dominate the results. All statistical analyses were conducted by using the statistical software package Stata (SE version 8.0, Stata Corporation, College Station, Texas).


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 References
 
Fish consumption
In total, 22 publications reported results of 19 independent cohort studies on fish consumption and colorectal cancer incidence or mortality (5–7, 25–43). The publications by Goldbohm et al. (6) and Hirayama (29) were excluded from the meta-analysis because they reported on the same cohorts as the more recent publications by Lüchtenborg et al. (37) and Hirayama (30), respectively. The publication by Kearney et al. (33) was excluded because, although more recent, it reported on a less useful exposure (dark-meat fish) than the one studied by Giovannucci et al. (5), who reported on (total) fish consumption in the same cohort. The characteristics of the remaining 19 studies are summarized in table 1. Of these studies, 15 reported on colorectal cancer incidence and four on colorectal cancer mortality. The number of cases ranged from 29 in a study on colorectal cancer mortality (34) to 1,329 in the European Prospective Investigation into Cancer and Nutrition (39). Median follow-up duration was 10 years, with an interquartile range of 7–15 years. Food frequency questionnaires and interviews were used to assess exposure in all studies, except for one study that used 24-hour dietary recalls (28).


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  		TABLE 1. Papers included in the meta-analysis of fish consumption and colorectal cancer incidence or mortality or of n-3 fatty acids and colorectal cancer incidence

 
Colorectal cancer incidence
Meta-analysis of risk estimates of colorectal cancer incidence for the highest compared with the lowest fish consumption category could be performed on 16 estimates from 14 cohort studies (5, 7, 25–27, 32, 35–39, 41–43). The fish exposure definitions in this analysis included fish, fish and shellfish, and seafoods. Of the 16 estimates, the reported relative risks ranged from 0.46 (95 percent confidence interval (CI): 0.19, 1.11) (27) to 1.20 (95 percent CI: 0.60, 2.40) (43) (figure 1). The pooled relative risk for colorectal cancer was 0.88 (95 percent CI: 0.78, 1.00) for the highest compared with the lowest fish consumption category (figure 1, table 2). Of the total variation, 18.3 percent (p = 0.25) was attributable to variation across studies. Figure 2 shows no evidence that smaller studies with estimates inconsistent with the supposed association (close to 1.0 or even in the opposite direction) remained unpublished, which would have led to asymmetry in the funnel plot. In addition, Egger's test did not show convincing evidence of a possible publication bias (p = 0.66). When we excluded one of the most recent studies (39), also the study with the heaviest weight (15.1 percent of total), the pooled relative risk was 0.93 (95 percent CI: 0.83, 1.05). One study did not provide the data required for meta-analysis of a comparison of the highest and lowest fish consumption categories (28). In this study, no significant difference was observed regarding the mean combined fish and shellfish consumption of colon cancer cases, rectal cancer cases, and controls (67.6 g/day, 58.8 g/day, and 61.6 g/day, respectively).


Figure 1
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  		FIGURE 1. Forest plot of the relative risks of colorectal cancer incidence and fish consumption (highest compared with the lowest category), considering 16 independent estimates from 14 cohort studies. The arrow (<- used with Gaard, 1996, men) indicates that the lower limit of the 95% confidence interval (CI) is outside the area of the figure. The contribution of each estimate to the meta-analysis (its weight) is represented by the size of the black box.

 

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  		TABLE 2. Results of meta-analyses of studies on fish consumption, n-3 fatty acid intake, and colorectal, colon, and rectal cancer incidence and colorectal cancer mortality

 

Figure 2
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  		FIGURE 2. Begg's funnel plot (16 estimates from 14 cohort studies) with pseudo–95% confidence limits for the relative risks (RRs) of colorectal cancer incidence and fish consumption category (highest compared with the lowest category).

 
Results of stratified analyses are shown in table 3. The pooled relative risks were 0.78 (95 percent CI: 0.58, 1.06) for women and 0.94 (95 percent CI: 0.75, 1.18) for men. In studies in which the difference in fish consumption between the highest and lowest intake categories was seven or more times per month, the pooled relative risk was 0.78 (95 percent CI: 0.66, 0.92); in studies in which this contrast was less, the relative risk was 0.95 (95 percent CI: 0.81, 1.11). Stratification by year of publication (before or after 1997) and region (Europe, United States, or Australia) did not markedly influence the observed associations.


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  		TABLE 3. Stratified pooled relative risks and 95% confidence intervals for the highest (compared with the lowest) fish consumption and colorectal cancer incidence

 
Nine estimates from seven studies could be used in the meta-analysis per unit of one time per week of fish consumption and risk of colorectal cancer incidence (7, 25–27, 36, 38, 43). The pooled relative risk was 0.96 (95 percent CI: 0.92, 1.00) for each extra time per week that fish was consumed (table 2). Four estimates from four studies could be used in the meta-analysis expressing risk of colorectal cancer incidence per 100 g of fish consumption per week (5, 28, 39, 41). The pooled relative risk was 0.97 (95 percent CI: 0.92, 1.03; table 2).

Colon and rectal cancer incidence
Nine estimates from eight studies could be used in the meta-analysis of fish consumption and colon cancer incidence (5, 7, 25–27, 37, 39, 43). The pooled relative risk was 0.87 (95 percent CI: 0.74, 1.02) for the highest compared with the lowest fish consumption category (table 2). The association between fish consumption and rectal cancer incidence was reported in four studies (26, 37, 39, 43). The pooled relative risk was 0.84 (95 percent CI: 0.55, 1.29) for the highest compared with the lowest fish consumption category (table 2).

Colorectal cancer mortality
For fish consumption and colorectal cancer mortality, six estimates from four studies were available (30, 31, 34, 44). The pooled relative risk for the highest compared with the lowest fish consumption category was 1.02 (95 percent CI: 0.90, 1.16; table 2).

n-3 fatty acids
In total, four independent publications reported on n-3 fatty acid intake calculated from dietary questionnaires and colorectal cancer incidence (25, 41, 45, 46). Of these studies, two reported on (total) n-3 fatty acids (25, 46), one on n-3 fish fatty acids (41), and one on docosahexaenoic acid (45). The characteristics of these studies are summarized in table 1. Meta-analysis of risk estimates for colorectal cancer incidence for the highest compared with the lowest n-3 fatty acid intake could be performed on three estimates from three cohort studies (25, 41, 45). The pooled relative risk was 0.91 (95 percent CI: 0.70, 1.19) for the highest compared with the lowest n-3 fatty acid intake category (table 2). One study did not provide the data required for meta-analysis of comparison of the highest and lowest n-3 fatty acid intake categories (46). In this study, no statistically significant difference (p = 0.94) was found between the median n-3 fatty acids intakes of colorectal cancer cases and controls (for both, 0.8 g/day).


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
References
 
In this meta-analysis, we found a borderline significant 12 percent lower risk of colorectal cancer for those in the highest fish consumption category compared with those in the lowest consumption category. The association was more pronounced (a 22 percent lower risk) in the studies in which the difference between the highest and lowest categories of fish consumption was at least seven times per month. In the "per-unit" analyses, we found a lower risk of colorectal cancer for each extra time that fish was consumed per week and for each extra 100 g of fish intake per week (4 percent and 3 percent, respectively). The pooled relative risk for fish consumption and colon cancer and also for rectal cancer was comparable with the pooled relative risk for colorectal cancer incidence. Regarding colorectal cancer mortality, no evidence of an association with fish consumption was found. A nonsignificant inverse association was found for n-3 fatty acid intake and colorectal cancer incidence from the results of only a few studies.

Evaluation of heterogeneity is a crucial part of any meta-analysis. In the meta-analysis of the highest compared with the lowest category of fish consumption and colorectal cancer incidence, about 18.3 percent of the total variation was attributable to variation across studies (p = 0.25). We accounted for this heterogeneity by using a random-effects model. In addition, sources of heterogeneity were investigated and identified. Stratified analyses showed a stronger inverse association among women compared with men, although neither association reached statistical significance. In two studies, the association was assessed for both men and women; in one of these, the association was weaker for women than for men. Therefore, there does not appear to be a consistent sex-specific association. The association was slightly more pronounced in studies from the United States than in those from Europe. A significant pooled association was found among the studies with a large difference between the highest and lowest categories of intake and not in studies with a smaller exposure contrast. Results of the "per-unit" meta-analysis of risk estimates for a continuous increase in fish consumption account for this exposure contrast. A 4 percent (95 percent CI: 0 percent, 8 percent) decrease in risk was found per extra time per week of fish consumption. If we assume a dose-response relation, this is approximately equal to a relative risk of 0.962 = 0.92 for two extra times per week of fish consumption, which is the average difference between the highest and lowest intake categories.

The European Prospective Investigation into Cancer and Nutrition study (39) was the largest study included in our meta-analysis. The pooled relative risk became weaker if we excluded the results of this study from the meta-analysis of fish and colorectal cancer incidence (sensitivity analysis). One of the largest ranges of fish intake was found in the European Prospective Investigation into Cancer and Nutrition study. The difference between fish consumption in the highest and lowest intake categories was 70 g/day, whereas the difference was not larger than 10–25 g/day in half of the other studies. The results from this large study provide strong evidence for a protective effect from fish consumption. Unpublished results from the Physicians' Health Study show that men who ate fish five or more times a week had a 40 percent lower risk of developing colorectal cancer compared with men who ate fish less than once a week. If published, this study would replace the less pronounced results from a nested case-control study within the same cohort, but after shorter follow-up, currently included in our meta-analyses (38). The unpublished results provide additional evidence for a beneficial effect of fish on colorectal cancer incidence.

Another important issue is exposure assessment. Food frequency questionnaires and interviews were the exposure assessment tools used in all studies but one (28). It is plausible that bias might still be present. The validity of the questionnaires, especially concerning fish consumption, may be low.

Another limitation of meta-analyses of this sort is heterogeneity of the food item, the range of intakes, preparation methods, and related dietary patterns. Because of a deficit in information on correlated dietary factors provided in the papers, it was, for example, not possible to study a potential confounding or modifying effect of meat consumption or alpha-linolenic acid intake. Therefore, the results should be interpreted cautiously. With these modest associations, it is possible that residual confounding could explain the association and that, if the principal causal component of fish was isolated, the true association could be much stronger.

Serum level of n-3 fatty acids could be used as a marker of fish consumption. n-3 fatty acids are hypothesized to be one of the main beneficial components of fish, besides vitamin D and selenium. Higher levels of vitamin D may decrease risk of colorectal cancer, but intakes higher than customary are required if exposure to sunshine is low (47, 48). Anticancer effects of selenium have been demonstrated by studies in cells and animals and by some human observational studies (49, 50). n-3 fatty acids are important components of cell membranes, appear to have antiinflammatory effects, and inhibit the growth of many different types of tumor cells (3, 51, 52). The meta-analysis on n-3 fatty acids and colorectal cancer incidence included three studies that reported n-3 fatty acid intake calculated from fish consumption, and no statistically significant effect was found. We found two nested case-control studies that reported on the relation between blood levels of n-3 fatty acids and risk of colorectal cancer. In the study from Japan, a significantly decreased risk was found for the highest versus the lowest quartile of n-3 fatty acid levels and colorectal cancer for men, but not for women (53). In the Physicians' Health Study, blood levels of long-chain n-3 fatty acids were associated with decreased risk of colorectal cancer among men not using aspirin (54).

In conclusion, our results indicate that fish consumption, and possibly n-3 fatty acid intake, inhibits colorectal carcinogenesis. In prospective cohort studies, fish consumption reduces colorectal cancer risk, particularly if the intake is relatively large. Extra consumption of fish once per week corresponds to a 4 percent lower risk of colorectal cancer.


   ACKNOWLEDGMENTS
 
This work was funded by WCRF International. It is part of the World Cancer Research Fund International project preparing the report, "Food, Nutrition, Physical Activity and the Prevention of Cancer: a Global Perspective." It does not necessarily represent the views of WCRF International; an independent panel will assess all of the information from a series of systematic reviews of all cancer sites, and it will draw conclusions and make recommendations based on these reviews and on other relevant evidence.

The authors thank all members of the Dutch systematic literature review team for their help in conducting this study: Marian Bos, Akke Botma, Simone Croezen, Maureen van den Donk, Khahn Le, Henk van Kranen, Mirjam Meltzer, Janneke Ploemacher, Salome Scholtens, Fleur Schouten, and Evelien Smit.

Conflict of interest: none declared.


   References
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 

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