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Cancer Epidemiology, Biomarkers & Prevention
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Review

Intake or Blood Levels of n-3 Polyunsaturated Fatty Acids and Risk of Colorectal Cancer: A Systematic Review and Meta-analysis of Prospective Studies

Youngyo Kim and Jeongseon Kim
Youngyo Kim
Department of Cancer Biomedical Science, Graduate School of Cancer Science and Policy, National Cancer Center, Goyang, South Korea.
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  • ORCID record for Youngyo Kim
Jeongseon Kim
Department of Cancer Biomedical Science, Graduate School of Cancer Science and Policy, National Cancer Center, Goyang, South Korea.
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DOI: 10.1158/1055-9965.EPI-19-0931 Published February 2020
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  • Figure 1.
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    Figure 1.

    Flow chart of study selection. The flow chart shows the process used to select prospective studies for the meta-analysis of the association between n-3 PUFAs and the risk of colorectal cancer.

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    Figure 2.

    A, Forest plot of prospective studies of colorectal cancer for the highest versus lowest category of n-3 PUFA intake, using a random-effects model. The sizes of the squares correspond to the inverse of the variance of the natural logarithm of the RR from each prospective study, and the diamond indicates the pooled RR. B, Pooled dose–response association between n-3 PUFA intake and colorectal cancer. Data were modeled with random-effects restricted cubic spline models with 3 knots. The vertical axis is on a log scale.

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    Figure 3.

    Pooled dose–response associations of EPA, DHA, DPA, and ALA intake with colorectal cancer. Data were modeled with random-effects restricted cubic spline models with 3 knots. The vertical axis is on a log scale.

  • Figure 4.
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    Figure 4.

    Forest plot of prospective studies of colorectal cancer for the highest versus lowest category of blood levels of n-3 PUFAs using a random-effects model. The sizes of the squares correspond to the inverse of the variance of the natural logarithm of the RR from each prospective study, and the diamond indicates the pooled RR.

Tables

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  • Table 1.

    Characteristics of prospective studies included in the meta-analysis of n-3 PUFAs and colorectal cancer.

    FirstAge atStudy size
    author, yearCountryCohort nameFollow-up periodbaseline, yearsSubjectsNo. of casesSex of subjectsExposureAdjustment for covariates
    Bostick, 1994United StatesThe Iowa Women's Health Study5 years55–6935,215212Femalen-3 PUFA intakeAge, total energy intake, height, parity, total vitamin E intake, a total vitamin E by age interaction term, and vitamin A supplement intake
    Pietinen, 1999FinlandThe Alpha-Tocopherol, Beta-Carotene Cancer Prevention Study8 years50–6927,111185Malen-3 PUFA intakeAge, supplement group, smoking years, BMI, alcohol, education, physical activity at work, and calcium intake
    Terry, 2001SwedenThe Swedish Mammography Screening Cohort9.6 years40–7461,463460Femalen-3 PUFA intakeAge, BMI, education level, energy intake, intakes of red meat and alcohol, energy, dietary fiber, calcium, vitamin C, folic acid, and vitamin D. Saturated fat, monounsaturated fat, polyunsaturated fat.
    Kojima, 2005JapanJapan Collaborative Cohort Study7.1 years40–79650169Male and femaleBlood levels of n-3 PUFAsFamily history of colorectal cancer in first-degree relatives, BMI, education, smoking and alcohol drinking history, green leafy vegetable intake, and physical exercise. Cases and controls were matched on age and participating institution.
    Oba, 2006JapanA community-based cohort in Japan7 years≥3530,221203Male and femalen-3 PUFA intakeAge, height, BMI, total pack-years of cigarette smoking, alcohol intake, and physical activity
    Hall, 2007United StatesPhysicians' Health Study1982–199540–84460178MaleBlood levels of n-3 PUFAsBMI, multivitamin use, history of diabetes, random assignment to aspirin or placebo, vigorous exercise, alcohol intake, and quartile of red meat intake. Controls were matched on age and smoking status.
    Hall, 2008United StatesPhysicians' Health Study17.6 years53.6, mean21,406500Malen-3 PUFA intakeAge, smoking, BMI, multivitamin use, history of diabetes, random assignment to aspirin or placebo, vigorous exercise, alcohol intake, and quartile of red meat intake
    Butler, 2009SingaporeSingapore Chinese Health Study9.8 years45–7461,321961Male and femalen-3 PUFA intakeAge at interview, sex, dialect group (Cantonese, Hokkien), interview year, diabetes at baseline, smoking history, BMI, alcohol intake, education, any weekly physical activity, first-degree relative diagnosed with colorectal cancer, and total daily energy intake
    Murff, 2009ChinaShanghai Women's Health Study1996–200740–7073,242396Femalen-3 PUFA intakeAge, energy intake, total energy-adjusted n-6 PUFA intake, energy-adjusted ratio of total n-6 PUFA to n-3 PUFA intake, BMI, current smoker, alcohol use, regular physical activity in past 5 y, total energy-adjusted red meat intake, menopausal status, hormone replacement therapy use, multivitamin use, and aspirin use
    Daniel, 2009United StatesCancer Prevention Study-II Nutrition Cohort6 years70 male 68 female, mean99,080869Male and femalen-3 PUFA intakeAge, energy, recreational physical activity, NSAID use, colorectal screening, BMI, and red and processed meat, low-fat dairy, fruit, and vegetable intake
    Sasazuki, 2011JapanThe Japan Public Health Center9.3 years40–6998,4661,268Male and femalen-3 PUFA intakeAge, area, BMI, smoking status, alcohol drinking, past history of or medication use for diabetes mellitus, METs, screening for colorectal cancer, total calorie, intake of calcium, vitamin D, fiber, and red meat
    Key, 2012United KingdomUK Dietary Cohort Consortium1985–200661.7, mean2,415547Male and femalen-3 PUFA intakeAge, date of diary, sex, height, weight, energy intake, alcohol intake, fiber intake, smoking, education, social class, physical activity
    Kantor, 2014United StatesVITamins And Lifestyle Study6.7 years50–7668,109488Male and femalen-3 PUFA intakeAge, sex, race/ethnicity, education, BMI, energy intake, MET-hr per wk of moderate/vigorous activity, alcohol intake, smoking history, multivitamin use, calcium intake, dietary fiber intake, fruit and vegetable intake, red/processed meat intake, aspirin use, nonaspirin NSAID drug use, family history of colorectal cancer, history of sigmoidoscopy/colonoscopy, history of polyps, hormone replacement therapy, cardiovascular disease, memory loss, use of cholesterol-lowering drugs, and omega-6 (linoleic +arachidonic) intake
    Song, 2014United StatesNurses' Health Study24 years30–5576,3861,469Femalen-3 PUFA intakeAge, calendar year, family history of colorectal cancer, prior lower gastrointestinal endoscopy, pack-years of smoking before age 30, BMI, physical activity, current multivitamin use, postmenopausal status and hormone use, regular aspirin or NSAID use, total caloric intake, red meat, processed meat, alcohol consumption, energy-adjusted intake of folate, calcium, vitamin D, and total fiber
    Song, 2014United StatesHealth Professionals Follow-up Study26 years40–7547,143987Malen-3 PUFA intakeAge, calendar year, family history of colorectal cancer, prior lower gastrointestinal endoscopy, pack-years of smoking before age 30, BMI, physical activity, current multivitamin use, regular aspirin or NSAID use, total caloric intake, red meat, process meat, alcohol consumption and energy-adjusted intake of folate, calcium, vitamin D, and total fiber
    Hodge, 2015AustraliaMelbourne Collaborative Cohort Study9 years40–6941,514395Male and femalen-3 PUFA intake; blood levels of n-3 PUFAsAge, education, alcohol intake, smoking status, physical activity, total energy intake and stratified by: sex, ethnicity (Southern-European migrant vs. not), and family history of cancer
    Kraja, 2015NetherlandsRotterdam Study14.6 years≥554,967222Male and femalen-3 PUFA intakeAge, sex, energy-adjusted dietary fiber intake, intake of vegetable, trans fat, fruit, alcohol, and sodium
    Navarro, 2016United StatesWomen's Health Initiative prospective cohort11.7 years50–79134,0171,952Femalen-3 PUFA intakeAge, total energy intake, BMI, education, family history of colorectal cancer, history of colonoscopy, current NSAID use, alcohol intake, smoking history, physical activity, ever use of hormone therapy, folate, calcium, and red meat intake, study component, randomization assignment and treatment arm
    Butler, 2017SingaporeSingapore Chinese Health Study3.3 years45–74700350Male and femaleBlood levels of n-3 PUFAsBMI, smoking, education level, alcohol use, weekly physical activity, history of diabetes, and use of NSAIDs. The control was matched to an index case by sex, dialect group, age, date of baseline interview, and date of biospecimen collection.
    Aglago, 2019EuropeEuropean Prospective Investigation into Cancer and Nutrition14.9 years51.3, mean476,1606,291Male and femalen-3 PUFA intake; blood levels of n-3 PUFAsAge, sex, center, BMI, height, physical activity, smoking, education, and intakes of energy, alcohol, red and processed meat, fiber, dairy products
    • Abbreviations: MET, metabolic equivalent; No., number.

  • Table 2.

    Summary of pooled RRs of colorectal cancer risk for n-3 PUFAs.

    VariableNo. of studiesRR95% CIP for difference
    n-3 PUFA intake
    High versus low n-3 fatty acid intake
    All studies170.970.90–1.04
    Sex
     Male80.950.84–1.060.59
     Female100.990.89–1.09
    Geographic region
     United States70.950.84–1.07
     Europe50.980.83–1.150.83a
     Asia41.010.88–1.160.59a
     Oceania11.070.76–1.500.59a
    Cancer sites
     Colon90.940.83–1.060.49b
      Proximal40.840.72–1.000.11c
      Distal41.120.84–1.48
     Rectal70.980.87–1.11
    Duration of follow-up
     <Median90.980.86–1.110.89
     ≥Median80.960.88–1.05
    Type of fatty acids
     ALA71.010.92–1.12
     EPA50.890.80–0.990.04d
     DHA50.880.81–0.960.05d
     DPA30.870.74–1.030.01d
    Quality score
     <1020.920.54–1.560.79
     ≥10150.970.90–1.04
    Adjustment for age, BMI, smoking, alcohol, and physical activity
     Yes110.950.88–1.010.79
     No60.990.82–1.19
    Increase of g/day in n-3 PUFA intake
     n-3 PUFA, 0.5 g/day131.000.97–1.03
     ALA, 0.1 g/day51.000.996–1.01
     EPA, 0.1 g/day30.950.92–0.98
     DHA, 0.1 g/day30.970.95–0.99
     DPA, 0.1 g/day20.870.73–1.03
    Blood levels of n-3 PUFAs
    High versus low blood levels of n-3 fatty acids
    All studies50.790.64–0.98
    Sex
     Male20.410.18–0.940.49
     Female10.850.38–1.91
    Geographic region
     Asia20.760.50–1.150.98
     Non-Asia30.800.62–1.02
    Cancer sites
     Colon20.810.62–1.060.47
     Rectal11.080.69–1.67
    Duration of follow-up
     <Median30.730.51–1.050.75
     ≥Median20.830.64–1.08
    Type of fatty acids
     ALA30.880.49–1.58
     EPA50.820.67–1.000.75e
     DHA50.800.61–1.060.77e
     DPA30.720.46–1.120.60e
    Quality score
     <1020.810.59–1.110.87
     ≥1030.750.53–1.08
    Adjustment for age, BMI, smoking, alcohol, and physical activity
     Yes30.670.41–1.100.70
     No20.820.66–1.01
    Increase of 1% in blood levels of n-3 PUFAs
     All studies30.960.92–1.00
    • Abbreviation: No., number.

    • ↵aP value difference in RRs of n-3 PUFA intake for Europe versus United States (P = 0.83), Asia versus United States (P = 0.59), and Oceania versus United States (P = 0.59).

    • ↵bP value difference in RRs of n-3 PUFA intake for rectal cancer versus colon cancer.

    • ↵cP value difference in RRs of n-3 PUFA intake for distal colon cancer versus proximal colon cancer.

    • ↵dP value difference in RRs of n-3 PUFA intake for EPA versus ALA (P = 0.04), DHA versus ALA (P = 0.05), and DPA versus ALA (P = 0.01).

    • ↵eP value difference in RRs of blood levels of n-3 PUFAs for EPA versus ALA (P = 0.75), DHA versus ALA (P = 0.77), and DPA versus ALA (P = 0.60).

Additional Files

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    • Supplementary Tables 1-2 and Figure 1. - Supplementary Table 1. Search terms for literature search. Supplementary Table 2. Summary of pooled relative risks (RR) of colorectal cancer risk for marine n-3 PUFAs.Supplementary Figure 1. Pooled dose-response association between marine n-3 PUFA intake and colorectal cancer.
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Cancer Epidemiology Biomarkers & Prevention: 29 (2)
February 2020
Volume 29, Issue 2
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Intake or Blood Levels of n-3 Polyunsaturated Fatty Acids and Risk of Colorectal Cancer: A Systematic Review and Meta-analysis of Prospective Studies
Youngyo Kim and Jeongseon Kim
Cancer Epidemiol Biomarkers Prev February 1 2020 (29) (2) 288-299; DOI: 10.1158/1055-9965.EPI-19-0931

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Intake or Blood Levels of n-3 Polyunsaturated Fatty Acids and Risk of Colorectal Cancer: A Systematic Review and Meta-analysis of Prospective Studies
Youngyo Kim and Jeongseon Kim
Cancer Epidemiol Biomarkers Prev February 1 2020 (29) (2) 288-299; DOI: 10.1158/1055-9965.EPI-19-0931
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