Background
Methods
Search strategy
Study selection
Data exaction and quality assessment
Statistical analysis
Results
Characteristics of studies and data quality
Study, year | Country | Study design | Participants (cases) | Age (years) | Score quality | Protein type | Dietary assessment | Protein intake amounts (g) | RR (95% CI) | Adjustment for covariates |
---|---|---|---|---|---|---|---|---|---|---|
Ghadirian P, 1997 | Canada | Case-control | 1070 (402) | 35–79 | 6 | Total animal vegetable | Quantitative food frequency questionnaire | Colon Quartile 1 Quartile 2 Quartile 3 Quartile 4 | Colon 1 0.81(0.55–1.19) 0.91(0.62–1.32) 1.11(0.77–1.61) | Adjusted for gender, age, marital status, history of colon carcinoma in first-degree relatives, and total energy intake |
Goldbohm RA, 1994 | Netherlands | Cohort | 120,852 (215) | 55–69 | 8 | Animal | Semiquantitative food frequency questionnaire | Colon Quintile 1 Quintile 2 Quintile 3 Quintile 4 Quintile 5 | Colon 1 1.10(0.70–1.71) 1.05(0.67–1.65) 1.28(0.82–2.00) 0.90(0.57–1.42) | Adjusted for quintiles of energy and energy-adjusted nutrient intakes, sex, and dietary fiber intake |
Iscovich JM, 1992 | Argentina | Case-control | 330 (110) | NA | 7 | Total | Food-frequency questionnaire | Colon Quartile 1 Quartile 2 Quartile 3 Quartile 4 | Colon 1 0.94(0.46–1.90) 0.63(0.26–1.49) 1.03(0.33–3.21) | Adjusted for fiber at 19.02 g per day, other sources of energy intake |
Levi F, 2002 | Switzerland | Case-control | 836 (286) | ≤ 74 | 7 | Total | Food-frequency questionnaire | Colorectal Lowest Middle Highest | Colorectal 1 0.80(0.50–1.30) 1.10(0.70–1.70) | Adjusted for age, sex, education, physical activity, and residual energy |
Pietinen P, 1999 | Finland | Cohort | 27,111 (185) | 50–69 | 8 | Total Animal Vegetable | Food-frequency questionnaire | Colorectal 83.8 96.9 105.1 115.9 | Colorectal 1 1.20(0.80–1.70) 0.90(0.60–1.40) 0.90(0.50–1.50) | Adjusted for age, supplement group, smoking years, body mass index, alcohol, education, and physical activity at work, and calcium intake (except for milk protein and milk products) |
Prentice RL, 2009 | American | Cohort | 59,105 (280) | 50–89 | 8 | Total | Food-frequency questionnaire | Colon Quartile 1 Quartile 2 Quartile 3 Quartile 4 | Colon 1 0.97(0.70–1.34) 1.11(0.76–1.61) 0.96(0.64–1.44) | NA |
Prentice RL, 2009 | American | Cohort | 59,105 (280) | 50–89 | 8 | Total | Food-frequency questionnaire | Rectum Quartile 1 Quartile 2 Quartile 3 Quartile 4 | Rectum 1 1.22(0.56–2.65) 1.57(0.72–3.41) 1.08 (0.48–2.41) | NA |
Slattery ML, 1994 | American | Case-control | 623 (231) | 40–79 | 7 | Total | Food-frequency questionnaire | Colon ≤ 58.7 58.8–81.4 81.5–99.9 > 99.9 | Colon (men) 1 2.30(1.10–4.70) 2.40(1.00–5.70) 3.70(1.30–10.50) | Adjusted for age, religion, body mass index, crude fiber, and separate logistic models were used for each variable. Calcium as continuous variables in multiple logistic regression models. |
Slattery ML, 1994 | American | Case-control | 623 (231) | 40–79 | 7 | Total | Food-frequency questionnaire | Colon ≤ 49.7 49.8–63.5 63.6–79.1 > 79.1 | Colon (women) 1 0.90(0.40–1.90) 1.90(0.90–4.20) 2.70(0.90–7.70) | Adjusted for age, religion, body mass index, crude fiber, and separate logistic models were used for each variable. Calcium as continuous variables in multiple logistic regression models |
Slattery ML, 1997 | American | Case-control | 2389 (1099) | 30–79 | 7 | Total | Food-frequency questionnaire | Colon (kcal) ≤ 263 264–331 332–407 408–512 > 512 | Colon (men) 1 1.25(0.95–1.65) 1.35(1.01–1.81) 1.33(0.95–1.84) 1.73(1.11–2.68) | Adjusted for age, body mass index, and family history of first-degree relative with colorectal cancer, use of aspirin and/or nonsteroidal anti-inflammatory drugs, physical activity, and dietary intake of fiber, cholesterol, and calcium |
Slattery ML, 1997 | American | Case-control | 2014 (894) | 30–79 | 7 | Total | Food-frequency questionnaire | Colon (kcal) ≤ 209 210–259 260–316 317–399 > 399 | Colon (women) 1 1.00(0.74–1.35) 1.02(0.74–1.40) 1.00(0.70–1.43) 0.91(0.56–1.48) | Adjusted for age, body mass index, and family history of first-degree relative with colorectal cancer, use of aspirin, and/or nonsteroidal anti-inflammatory drugs, physical activity, and dietary intake of fiber, cholesterol, and calcium |
Sun Z, 2012 | Canada | Case-control | 4241 (1760) | 20–74 | 7 | Total | Food-frequency questionnaire | Colorectal Quintile 1 Quintile 3 Quintile 5 | Colorectal 1 0.88(0.70–1.11) 0.85(0.69–1.00) | Adjusted for total energy intake. Other potential confounders included age, sex, BMI, physical activity, family history of CRC, polyps, diabetes, reported colon screening procedure, cigarette smoking, alcohol drinking, education attainment, household income, marital status, regular use of NSAID, regular use of multivitamin supplements, regular use of folate supplement, regular use of calcium supplement, reported HRT (females only), province of residence, and intakes of fruits, vegetables, and red meat. Variables were included in the final model based on a ≥ 10% alternation in the parameter coefficient of interest |
Tayyem RF, 2015 | Jordan | Case-control | 417 (169) | 53.8 ± 12.2 | 6 | Total | Quantitative food frequency questionnaire | Colorectal Quartile 1 Quartile 2 Quartile 3 Quartile 4 | Colorectal 1 1.66(0.74–3.69) 1.74(0.78–3.90) 3.62(1.63–8.04) | Adjusted for total energy intake normality of the distributions of dietary intake variables was assessed by the Shapiro-Wilk test. Non-normally distributed variables were log transformed. Other potential confounders included age, gender, BMI, physical activity (METs/week), family history (beyond the second degree) of CRC, education attainment, household income, marital status, and tobacco use |
Wakai K, 2006 | Japan | Case-control | 3042 (507) | 20–79 | 7 | Total | Food-frequency questionnaire | Colon Quartile 1 Quartile 2 Quartile 3 Quartile 4 | Colon 1 0.74(0.52–1.07) 0.65(0.45–0.95) 0.74(0.51–1.07) | Adjusted for age, sex, year of first visit, season of first visit to the hospital, reason for the visit, family history of colorectal cancer, body mass index, exercise, alcohol drinking, smoking, multivitamin use, and energy intake |
Wakai K, 2006 | Japan | Case-control | 3042 (507) | 20–79 | 7 | Total | Food-frequency questionnaire | Rectum Quartile 1 Quartile 2 Quartile 3 Quartile 4 | Rectum 1 0.83(0.57–1.22) 0.91(0.62–1.32) 0.71(0.47–1.06) | Adjusted for age, sex, year of first visit, season of first visit to the hospital, reason for the visit, family history of colorectal cancer, body mass index, exercise, alcohol drinking, smoking, multivitamin use, and energy intake |
Williams CD, 2010 | American | Case-control | 1520 (720) | 59.6 ± 10.3 | 8 | Total | Food-frequency questionnaire | Colorectal Quartile 1 Quartile 2 Quartile 3 Quartile 4 | Colorectal (whites) 1 0.90(0.64–1.27) 0.86(0.57–1.30) 0.57(0.32–1.01) | Adjusted for age, sex, education, body mass index, family history, nonsteroidal anti-inflammatory drug use, physical activity, calcium, fiber, and total energy |
Williams CD, 2010 | American | Case-control | 384 (225) | 58.0 ± 10.0 | 8 | Total | Food-frequency questionnaire | Colorectal Quartile 1 Quartile 2 Quartile 3 Quartile 4 | Colorectal (African Americans) 1 1.05(0.51–2.16) 0.81(0.32–2.05) 0.58(0.16–2.10) | Adjusted for age, sex, education, body mass index, family history, nonsteroidal anti-inflammatory drug use, physical activity, calcium, fiber, and total energy |
Yang SY, 2016 | Korea | Case-control | 1056 (406) | 30–70 | 8 | Animal | Food-frequency questionnaire | Colorectal Tertile 1 Tertile 2 Tertile 3 | Colorectal (men) 1 0.71(0.47–1.07) 1.25(0.88–1.78) | Adjusted for total energy intake, waist circumference, BMI, HDL cholesterol, fasting glucose, alcohol intake, smoking status, and family history of colorectal adenoma |
Yang SY, 2016 | Korea | Case-control | 658 (151) | 30–70 | 8 | Animal | Food-frequency questionnaire | Colorectal Tertile 1 Tertile 2 Tertile 3 | Colorectal (women) 1 0.71(0.30–1.68) 0.87(0.52–1.46) | Adjusted for total energy intake, waist circumference, BMI, HDL cholesterol, fasting glucose, alcohol intake, smoking status, and family history of colorectal adenoma |
Yang SY, 2016 | Korea | Case-control | 1056 (406) | 30–70 | 8 | Vegetable | Food-frequency questionnaire | Colorectal Tertile 1 Tertile 2 Tertile 3 | Colorectal (men) 1 0.93(0.63–1.37) 0.96(0.60–1.53) | Adjusted for total energy intake, waist circumference, BMI, HDL cholesterol, fasting glucose, alcohol intake, smoking status, and family history of colorectal adenoma |
Yang SY, 2016 | Korea | Case-control | 658 (151) | 30–70 | 8 | Vegetable | Food-frequency questionnaire | Colorectal Tertile 1 Tertile 2 Tertile 3 | Colorectal (women) 1 0.78(0.39–1.56) 0.54(0.27–1.11) | Adjusted for total energy intake, waist circumference, BMI, HDL cholesterol, fasting glucose, alcohol intake, smoking status, and family history of colorectal adenoma |
Dietary protein intake and risk of colorectal cancer
Sources of heterogeneity and subgroup analysis
Subgroups | No. cases | No. studies | RR (95% CI) |
I
2 (%) |
P
heterogeneity
|
---|---|---|---|---|---|
All studies | 8187 | 21 | 1.006(0.857–1.179) | 53.4 | 0.002 |
Disease type | |||||
Colon | 3446 | 9 | 1.135(0.871–1.480) | 55.4 | 0.022 |
Rectum | 282 | 2 | 0.773(0.538–1.111) | 0.0 | 0.363 |
Study design | |||||
Cohort | 680 | 4 | 0.939(0.730–1.209) | 0.0 | 0.980 |
Case-control | 7507 | 17 | 1.030(0.846–1.254) | 62.6 | 0.000 |
Sex | |||||
Both | 4394 | 10 | 0.913(0.737–1.132) | 53.3 | 0.023 |
Men | 2204 | 5 | 1.306(0.932–1.829) | 54.6 | 0.066 |
Women | 1589 | 6 | 0.931(0.710–1.220) | 20.5 | 0.279 |
Protein | |||||
Total | 6858 | 16 | 1.049(0.856–1.285) | 60.6 | 0.001 |
Animal | 1359 | 5 | 1.041(0.866–1.252) | 0.0 | 0.624 |
Vegetable | 1144 | 4 | 0.851(0.602–1.203) | 49.9 | 0.112 |
Geographic locations | |||||
America | 5711 | 11 | 1.072(0.838–1.372) | 56.4 | 0.011 |
Asia | 1790 | 7 | 0.962(0.694–1.333) | 69.0 | 0.004 |
Europe | 686 | 3 | 0.972(0.738–1.280) | 0.0 | 0.785 |