Table 1.
Summary of Prospective Cohort Studies of Red Meat and Colorectal Cancer
| Author and Year | Cohort | Analytical Category (definition) | Number of Exposed Cases | Gender | Analytical Comparison | Relative Risk (95% CI) | Statistical Adjustment |
|---|---|---|---|---|---|---|---|
| Bostick et al. 1994 | Iowa Women's Health Study | Red meat | 37 | Women | Colon: > 11.0 vs < 4.0 servings/wk | 1.04 (0.62–1.76) | Age, total energy intake, alcohol, height, parity, total vitamin E intake, total vitamin E intake by age interaction term, and vitamin A supplement intake |
| Brink et al. 2005 | Netherlands Cohort Study | Quartiles of intake (4 vs 1) | Age, sex, quetelet index, smoking, energy intake, family hx of CRC | ||||
| Beef | 142 | Both | Colon | 1.28 (0.96–1.72) | |||
| 40 | Both | Rectum | 0.92 (0.57–1.49) | ||||
| Pork | 98 | Both | Colon | 0.77 (0.57–1.04) | |||
| 34 | Both | Rectum | 0.70 (0.43–1.13) | ||||
| Minced meat | 97 | Both | Colon | 0.93 (0.68–1.27) | |||
| 35 | Both | Rectum | 1.01 (0.62–1.67) | ||||
| Butler et al. 2008 | Singapore Chinese Health Study | Red meat | 74 | Both | Quartiles of intake (4 vs 1) | 1.01 (0.82–1.26) | Age, sex, dialect group, interview year, diabetes at baseline, smoking hx, BMI, alcohol intake, education, physical activity, family hx of CRC, total daily energy intake |
| Chan et al. 2005 [overlap with Wei 2004] | NHS (U.S.) | Beef, pork, or lamb as a main dish | 17 | Women | > 0.5 vs ≤ 0.5 servings/day | 1.21 (0.85–1.72) | Age, BMI, family hx of CRC, post-menopausal hormone use, previous endoscopy, current multi-vitamin use, regular aspirin use |
| Chao et al. 2005 | CPS II (U.S.) | Red meat (beef, pork, ham, liver, smoked meats, frankfurters, sausage, fried bacon, fried hamburger) | Quintiles of intake (5 vs 1) | Age, sex, total energy, education, BMI, smoking, recreational physical activity, multivitamin use, aspirin use, alcohol, hormone therapy, fruits, vegetables, high-grain foods | |||
| 210 | Both | Colon | 1.15 (0.90–1.46) | ||||
| 96 | Both | Rectal | 1.71 (1.15–2.52) | ||||
| 116 | Both | Proximal colon | 1.27 (0.91–1.76) | ||||
| 64 | Both | Distal colon | 0.71 (0.47–1.07) | ||||
| 124 | Men | Colon | 1.30 (0.93–1.81) | Age, total energy, education, BMI, smoking, recreational physical activity, multivitamin use, aspirin use, alcohol, hormone therapy, sex, fruits, vegetables, high-grain food | |||
| 86 | Women | Colon | 0.98 (0.68–1.40) | ||||
| Chen et al. 2003 | China | Pork | NR | Both | Colon: Pork eating, yes vs no | 1.48 (0.85–2.59) | Matched on age, gender, resident location |
| Chen et al. 1998 | Physicians Health Study (U.S.) | Red meat (beef, pork, lamb as a main dish, mixed dish, or sandwich; hot dogs) | 43 | Men | 1+ intake/day vs ≤ 0.5 | 1.17 (0.68–2.02) | BMI, physical activity, and alcohol |
| Cross et al. 2007 | NIH-AARP Diet and Health Study (U.S.) | Red meat (beef, pork, and lamb; including bacon, beef, cold cuts, ham, hamburger, hot dogs, liver, pork, sausage, and steak; meats added to mixtures, such as pizza, chili, lasagna, and stew) | Quintiles of intake: 5 vs 1 62.7 g/1000 kcal vs 9.8 | Age, sex, education, marital status, family hx of cancer, race, BMI, smoking, frequency of vigorous physical activity, intake of: total energy, alcohol, fruits and vegetables | |||
| 1,190 | Both | Colorectal | 1.24 (1.12–1.36) | ||||
| Both | Colon | 1.17 (1.05–1.31) | |||||
| Both | Rectal | 1.45 (1.20–1.75) | |||||
| English et al. 2004 | Melbourne Collaborative Cohort Study (Australia) | Fresh red meat (veal or beef schnitzel, roast beef, veal, steak, meat balls, meatloaf, mixed dishes with beef, roast lamb/chops, pork/chops, rabbit, other game) | Quartiles (4 vs 1) | Sex, country of birth, energy intake, fat, cereal products | |||
| NR | Both | Colorectal | 1.4 (1.0–1.9) | ||||
| Both | Colon | 1.1 (0.7–1.6) | |||||
| Both | Rectal | 2.3 (1.2–4.2) | |||||
| Flood et al. 2003 | BCDDP (U.S.) | Red meat (bacon, beef, ham-burger, ham or other lunch meat, hot dogs, liver, pork, sausage; meat components of beef stew, chili, salad, spaghetti, vegetable soup) | NR | Women | Quintile 5 vs 1: 52.2+ g/1000 kcal vs ≤ 6.1 | 1.04 (0.77–1.41) | Energy, total meat [The following factors did not markedly affect the RR, thus, were not in the final model: smoking, education, BMI, alcohol, physical activity, dietary factors, micronutrients, anti-inflammatories] |
| Fraser 1999 [overlap with Singh and Fraser 1998] | 7th Day Adventists Health Study (California) | Red meat | NR | Both | Colon cancer among persons who consumed white meat < 1/wk: 1+ time/wk (red meat) vs never | 1.86 (1.15–3.02) | |
| Fung et al. 2010 [overlap with Wei et al. 2004] | NHS; HPFS (U.S.) | Red/processed meats | 87,312 | Women | Multivariate RR for each serving/d increase in DASH food component | 1.12 (0.99–1.26) | Age, BMI, alcohol intake, family hx of CRC, physical activity, aspirin use, colonoscopy, hx of polyps, multivitamin use, smoking, energy intake |
| 45,080 | Men | 1.08 (0.97–1.21) | |||||
| Gaard et al. 1996 | Norway | Colon | Age, attained age | ||||
| Meat balls | 15 | Men | 5+/month vs ≤ 1 | 0.61 (0.22–1.69) | |||
| Meat stews | 11 | Men | 5+/month vs ≤ 1 | 0.74 (0.21–2.64) | |||
| Meat balls | 13 | Women | 5+/month vs ≤ 1 | 1.08 (0.31–3.79) | |||
| Meat stews | 9 | Women | 5+/month vs ≤ 1 | 0.58 (0.16–2.13) | |||
| Giovannucci et al. 1994 [overlap with Wei et al. 2004] | HPFS (U.S.) | Red meat (beef, pork, or lamb as a main dish, sandwich or mixed dish; hamburger, hot dog, bacon, and preserved meats [e.g., sausage, salami, and bologna]) | 55 | Men | Colon: 129.5 g/day vs 18.5 | 1.71 (1.15–2.55) | Age, total energy intake |
| Beef, pork, or lamb as main dish | 16 | Men | Colon: ≥ 5 servings/wk vs 0 | 3.57 (1.58–8.06) | Age | ||
| Hsing et al. 1998 | Lutheran Brotherhood (U.S.) | Red meat (beef, bacon, fresh pork, smoked ham) | 60+ times/month vs < 15 | Age, smoking, alcohol, total calories | |||
| 14 | Men | Colorectal | 1.9 (0.9–4.3) | ||||
| 13 | Men | Colon | 1.8 (0.8–4.4) | ||||
| Iso and Kubota 2007 [overlap with Kojima et al. 2004] | Japan Collaborative Cohort Study | Beef | 15 | Men | Colon | 1.30 (0.74–2.29) | Age, area of study |
| 10 | Men | Rectal | 1.11 (0.55–2.20) | ||||
| 12 | Women | Colon | 0.80 (0.43–1.50) | ||||
| 3 | Women | Rectal | 0.78 (0.23–2.63) | ||||
| Pork | 23 | Men | Colon | 0.81 (0.48–1.36) | |||
| 29 | Men | Rectal | 1.44 (0.85–2.44) | ||||
| 31 | Women | Colon | 0.95 (0.61–1.49) | ||||
| 11 | Women | Rectal | 0.77 (0.35–1.65) | ||||
| Ham and sausages | 38 | Men | Colon | 1.41 (0.95–2.08) | |||
| 21 | Men | Rectal | 0.89 (0.55–1.46) | ||||
| 22 | Women | Colon | 0.90 (0.56–1.44) | ||||
| 14 | Women | Rectal | 1.30 (0.69–2.46) | ||||
| Liver | 6 | Men | Colon | 0.82 (0.36–1.88) | |||
| 6 | Men | Rectal | 1.03 (0.44–2.38) | ||||
| 5 | Women | Colon | 0.71 (0.29–1.75) | ||||
| 5 | Women | Rectal | 1.57 (0.61–4.03) | ||||
| Jarvinen et al. 2001 | Mobile Clinic Health Examination Survey (Finland) | Red meat | Quartiles of daily intake (4 vs 1) | Age, sex, BMI, occupation, smoking, geography, energy intake, vegetable and fruit consumption, cereal intake | |||
| NR | Both | Colorectal | 1.50 (0.77–2.94) | ||||
| Both | Colon | 1.34 (0.57–3.15) | |||||
| Both | Rectal | 1.82 (0.60–5.52) | |||||
| Kabat et al. 2007 | NBSS (Canada) | Red meat (ascertained from 22 meat items including beef, pork, ham, bacon, pork-based lunch meats, veal) | 40.3 g/day vs < 14.25 | Age, BMI, menopausal status, oral contraception, hormone replacement use, diet (fat, fiber, folic acid, total calories), smoking, alcohol, education, physical activity | |||
| NR | Women | Colorectal | 1.12 (0.86–1.46) | ||||
| Women | Colon | 0.88 (0.64–1.21) | |||||
| Women | Rectal | 1.95 (1.21–3.16) | |||||
| Kato et al. 1997 | New York, Florida | Red meat | NR | Women | Quartiles of intake (4 vs 1) | 1.23 (0.68–2.22) | Age, total calorie intake, education, enrollment place |
| Khan et al. 2004 | Japan | Meat, except chicken (pork, beef, mutton, liver, ham, sausages) | NR | Men | Several times/wk; everyday vs never; several times/yr; several times/month | 2.0 (0.6–6.3) | Age, smoking |
| NR | Women | Several times/wk; everyday vs never; several times/yr; several times/month | 1.0 (0.3–3.0) | Age, health status, health education, health screening and smoking | |||
| Kojima et al. 2004 | Japan Collaborative Cohort Study | 3–7/wk vs 0–2/month | Age, family hx of CRC, BMI, alcohol, smoking, walking per day, education, regions of enrollment | ||||
| Beef | 11 | Men | Colon | 1.46 (0.74–2.86) | |||
| 10 | Men | Rectal | 1.38 (0.68–2.78) | ||||
| Pork | 17 | Men | Colon | 1.14 (0.61–2.14) | |||
| 20 | Men | Rectal | 1.11 (0.61–2.03) | ||||
| Beef | 11 | Women | Colon | 1.11 (0.57–2.14) | |||
| 1 | Women | Rectal | 0.37 (0.05–2.84) | ||||
| Pork | 20 | Women | Colon | 0.93 (0.54–1.60) | |||
| 3 | Women | Rectal | 0.32 (0.09–1.15) | ||||
| Larsson et al. 2005 | Swedish Mammo-graphy Cohort | Red meat (whole beef, chopped meat, minced meat, bacon, hot dogs, ham or other lunch meat, blood pudding, kidney or liver, liver pate) | Women | 94+ g/day vs < 50 | Age, BMI, education, energy intake, alcohol, saturated fat, calcium, folate, fruits, vegetables, whole grain foods | ||
| NR | Women | Colorectal | 1.32 (1.03–1.68) | ||||
| Women | Rectal | 1.28 (0.83–1.98) | |||||
| Women | Proximal colon | 1.03 (0.67–1.60) | |||||
| Women | Distal colon | 2.22 (1.34–3.68) | |||||
| Beef and pork (whole beef, minced meat, chopped beef) | Women | 4+ servings/wk vs < 2 | |||||
| NR | Women | Colorectal | 1.22 (0.98–1.53) | ||||
| Women | Rectal | 1.08 (0.72–1.62) | |||||
| Women | Proximal colon | 1.10 (0.74–1.64) | |||||
| Women | Distal colon | 1.99 (1.26–3.14) | |||||
| Lee et al. 2009 | Shanghai Women's Health Study (China) | Red meat | 67+ g/day vs < 24 | Age, education, income, survey season, tea consumption, NSAID use, energy intake, and fiber intake | |||
| 62 | Women | Colorectal | 0.8 (0.6–1.1) | ||||
| 41 | Women | Colon | 0.9 (0.6–1.5) | ||||
| 21 | Women | Rectal | 0.6 (0.3–1.1) | ||||
| Lin et al. 2004 | Women's Health Study (U.S.) | Red meat (beef or lamb as main dish, beef, pork, or lamb in a sandwich, hot dogs, bacon, processed meats, hamburgers) | 30 | Women | 1.42+ servings/day vs ≤ 0.13 | 0.66 (0.40–1.09) | Age, random treatment assignment, BMI, family hx of CRC, hx of polyps, physical activity, smoking, alcohol, postmenopausal hormone therapy, total energy |
| Luchtenborg et al. 2005 [same popu-lation as Brink et al. 2005] | NLCS (Netherlands) | Quartiles of intake (4 vs 1) | Age, sex, family hx of CRC, smoking, BMI, energy intake | ||||
| Beef | 134 | Both | Colon | 1.29 (0.96–1.73) | |||
| 38 | Both | Rectal | 0.95 (0.59–1.54) | ||||
| Pork | 92 | Both | Colon | 0.77 (0.57–1.04) | |||
| 31 | Both | Rectal | 0.70 (0.44–1.13) | ||||
| Minced meat | 93 | Both | Colon | 0.93 (0.68–1.27) | |||
| 33 | Both | Rectal | 1.01 (0.61–1.66) | ||||
| Norat et al. 2005 | EPIC (Europe) | Red meat (fresh, minced, and frozen beef, veal, pork, lamb) | ≥ 80 g/day vs < 10 | Age, sex, energy, height, weight, occupational physical activity, smoking, alcohol intake, dietary fiber, center | |||
| 250 | Both | Colorectal | 1.17 (0.92–1.49) | ||||
| NR | Both | Colon | 1.20 (0.88–1.61) | ||||
| Both | Rectal | 1.13 (0.74–1.71) | |||||
| Both | Proximal (right) colon | 1.18 (0.73–1.91) | |||||
| Both | Distal (left) colon | 1.24 (0.80–1.94) | |||||
| Nöthlings et al. 2009 | Multiethnic Cohort Study (Hawaii, Los Angeles County) | Red meat | 240 | Both | 26.0+ g/1,000 kcal/day vs 0 to < 10.4 | 0.96 (0.74–1.23) | Age at blood draw, sex, ethnicity, family hx of CRC, BMI, physical activity, smoking, intake of dietary fiber, calcium, vitamin D, folic acid, and ethanol |
| Oba et al. 2006 | Japan | Red meat (beef, pork) | 32 | Men | Colon: 56.6+ g vs ≤ 18.7 | 1.03 (0.64–1.66) | Age, height, BMI, smoking, alcohol, physical activity |
| 27 | Women | Colon: 42.3+ g vs ≤ 10.7 | 0.79 (0.49–1.28) | ||||
| Ollberding et al. 2012 [overlap with Nöthlings et al. 2009] | Multiethnic Cohort Study (Hawaii, Los Angeles County) | Total red meat | 697 | Both | 47.99 g/1,000 kcal/day vs 7.41 | 1.02 (0.91–1.16) | Age, ethnicity, sex, family hx of CRC, hx of colorectal polyp, BMI, smoking, NSAID use, alcohol consumption, vigorous physical activity, hx of diabetes, hormone replacement therapy use (females only), total calories, dietary fiber, calcium, folate, and vitamin D |
| Red meat excluding processed red meat | 659 | Both | 34.86 g/1,000 kcal/day vs 4.59 | 0.98 (0.87–1.10) | |||
| Pietinen et al. 1999 | ATBC Study (Finland) | Beef, pork, lamb | 45 | Men | 99+ g vs < 36 | 0.8 (0.5–1.2) | Age, supplement group, smoking, BMI, alcohol, education, physical activity at work, calcium intake |
| Total red meat | 45 | Men | 203 g vs < 80 | 1.1 (0.7–1.7) | |||
| Sato et al. 2006 | Miyagi Cohort Study (Japan) | Beef | 1–2/wk vs almost never | Age, sex, smoking, alcohol, BMI, education, family hx of cancer, walking, consumption of fat, calcium, fiber | |||
| 46 | Both | Colorectal | 0.93 (0.67–1.30) | ||||
| 25 | Both | Colon | 0.84 (0.54–1.32) | ||||
| 21 | Both | Rectal | 1.01 (0.62–1.67) | ||||
| 16 | Both | Proximal colon | 0.97 (0.55–1.70) | ||||
| 8 | Both | Distal colon | 1.06 (0.46–2.43) | ||||
| Pork (excluding ham or sausage) | 3–4/wk vs almost never | ||||||
| 73 | Both | Colorectal | 1.13 (0.79–1.74) | ||||
| 48 | Both | Colon | 1.46 (0.81–2.62) | ||||
| 26 | Both | Rectal | 0.74 (0.39–1.42) | ||||
| 24 | Both | Proximal colon | 1.05 (0.50–2.22) | ||||
| 16 | Both | Distal colon | 1.90 (0.63–5.74) | ||||
| Sellers et al. 1998 [overlap with Bostick et al. 1994] | Iowa Women's Health Study | Red meat (beef, beef stew, hamburger, liver, venison) | Colon > 7 servings/wk vs < 3.5 | Age, energy intake, hx of polyps | |||
| 16 | Women | Family hx of colon cancer | 1.0 (0.5–2.1) | ||||
| 53 | Women | No family hx of colon cancer | 1.3 (0.8–2.0) | ||||
| Singh and Fraser 1998 | Adventist Health Study (California) | Red meat (current intake of beef or pork) | 45 | Both | Colon: 1+/wk vs never | 1.41 (0.90–2.21) | Age, sex, BMI, physical activity, smoking, alcohol, aspirin use, parental hx of colon cancer |
| Takachi et al. 2011 | JPHC (Japan) | Red meat (3 beef dishes – steak, grilled beef, and stewed beef; and 6 pork dishes – stir-fried pork, deep-fried pork, stewed pork in Western style, stewed pork in Japanese style, pork in soup, and pork liver) | 102 g/d vs 15 g/d | Age, Public Health Center area, BMI, smoking status, alcohol consumption, physical activity, medication use for diabetes, hx of diabetes, screening examinations, energy intake, calcium, vitamin D, folate, dietary fiber, and dried and salted fish | |||
| 91 | Men | Colon | 1.27 (0.93–1.74) | ||||
| 36 | Men | Rectal | 0.93 (0.58–1.49) | ||||
| 34 | Men | Proximal colon | 1.07 (0.66–1.75) | ||||
| 51 | Men | Distal colon | 1.42 (0.92–2.19) | ||||
| 93 g/d vs 14 g/day | |||||||
| 70 | Women | Colon | 1.48 (1.01–2.17) | ||||
| 22 | Women | Rectal | 0.81 (0.43–1.52) | ||||
| 42 | Women | Proximal colon | 1.57 (0.95–2.58) | ||||
| 23 | Women | Distal colon | 1.21 (0.63–2.32) | ||||
| Thun et al. 1992 | CPS II (U.S.) | Red meat | NR | Men | Colon | No association (data NR) | Matched on age, race, and sex. Adjusted for total fat, exercise, BMI, family hx of colon cancer, aspirin use, intake of vegetables, fruits, and grains |
| Beef | Men | Inverse association (data NR) | Matched on age, race, and sex | ||||
| Pork | Men | Positive association (data NR) | |||||
| Red meat | NR | Women | Colon | No association (data NR) | |||
| Beef | Women | Inverse association (data NR) | |||||
| Pork | Women | Positive association (data NR) | |||||
| Tiemersma et al. 2002 | Netherlands | Fresh red meat (beef, pork) | 45 | Both | 5+/wk vs 0–3/wk | 1.6 (0.9–2.9) | Age, sex, center, total energy intake, alcohol, body height |
| 30 | Men | 5+/wk vs 0–3/wk | 2.7 (1.1–6.7) | ||||
| 15 | Women | 5+/wk vs 0–3/wk | 1.2 (0.5–2.8) | ||||
| Wei et al. 2004 | NHS; HPFS (U.S.) | Beef, pork, lamb as a main dish | 5+/wk vs 0 | Age, family hx, BMI, physical activity, processed meat, alcohol, calcium, folate, height, smoking before age 30, hx of endoscopy, and gender | |||
| 155 | Both | Colon | 1.43 (1.00–2.05) | ||||
| 31 | Both | Rectum | 0.90 (0.47–1.75) | ||||
| HPFS | 32 | Men | Colon | 1.35 (0.80–2.27) | Age, family hx, BMI, physical activity, alcohol, calcium, folate, height, smoking before age 30, hx of endoscopy | ||
| 7 | Men | Rectum | 0.90 (0.34–2.45) | ||||
| NHS | 123 | Women | Colon | 1.31 (0.73–2.36) | |||
| 24 | Women | Rectum | 0.92 (0.31–2.71) | ||||
| Willett et al. 1990 [overlap with Wei et al. 2004] | NHS (U.S.) | Red meat (beef, pork or lamb as a main dish sandwich or mixed dish, hamburger, hotdogs, preserved meats, and bacon) | 134+ g/day vs < 59 | ||||
| 44 | Women | Colon | 1.77 (1.09–2.88) | Age and total energy intake | |||
| 44 | Women | Colon | 1.61 (1.03–2.53) | Age, total energy intake, and chicken and fish consumption | |||
| Wu et al. 2004 [overlap with Wei et al. 2004] | HPFS (U.S.) | Red meat | NR | Men | Colon: High vs low | 1.40 (0.92–2.13) | Multivariate (not explicitly stated for this analysis) |
| Red meat dish (beef, pork, lamb as main dish) | Men | Colon: High vs low | 1.68 (1.21–2.33) |
Notes: Outcome is colorectal cancer (CRC), unless otherwise noted.
a
Case-cohort study.
b
Nested case-control.
c
Study not included in meta-analysis because red meat item not explicitly defined.
ATBC = Alpha-Tocopherol, Beta-Carotene Cancer Prevention; BCDDP = Breast Cancer Detection Demonstration Project; BMI = body mass index; CRC = colorectal cancer; CPS II = Cancer Prevention Study II; EPIC = European Prospective Investigation into Cancer and Nutrition; DASH = Dietary Approaches to Stop Hypertension; JPHC= Japan Public Health Center-based Prospective Study; HPFS=– Health Professionals Follow Up Study; hx = history; NBSS=– National Breast Screening Study; NIH-AARP = National Institutes of Health-AARP (formerly the American Association for Retired Persons); NHS=– Nurses' Health Study; NLCS=– Netherlands Cohort Study; NR = not reported; NSAID = nonsteroidal anti-inflammatory