Article Figures & Data
Tables
- Table 1.
Baseline characteristics of Sister Study participants by colorectal case status (N = 48,704).
Colorectal cancer (case) Non–colorectal cancer (noncase) Participant characteristics 216 100% 48,488 100% Age at baseline, years (mean, range) 216 59.9 (36.6–75.9) 48,488 55.7 (35.0–76.5) Follow-up time, years (mean, range) 216 5.0 (0.01–11.8) 48,488 8.7 (0.1–12.7) Diagnosis source Medical report or NDI 136 63.0 — — Self-report/next-of-kin 80 37.0 — — Missing 0 Race/ethnicity Non-Hispanic White 183 84.7 41,064 84.7 Non-Hispanic Black 18 8.3 3,901 8.1 Hispanic/other 15 6.9 3,513 7.3 Missing 0 10 Educational attainment High school or less 22 10.2 7,391 15.3 Some college 83 38.4 16,274 33.6 Bachelor's degree or above 111 51.4 24,815 51.2 Missing 0 8 Body mass index (kg/m2; mean, range) 216 28.9 (18.0–56.8) 48,476 27.7 (11.5–72.1) Smoking status Never 111 51.4 27,229 56.2 Former 85 39.4 17,351 35.8 Current 20 9.3 3,896 8.0 Missing 0 12 Alcohol status Nondrinker (never/former) 46 21.3 9,109 18.8 Light (≤3 drinks per week) 107 49.5 26,348 54.4 Moderate (>3–7 drinks per week) 36 16.7 7,568 15.6 Heavy (>7 drinks per week) 27 12.5 5,385 11.1 Missing 0 78 Menopausal status Premenopausal 34 15.7 16,650 34.4 Postmenopausal 182 84.3 31,808 65.6 Missing 0 30 Family history of colorectal cancer 27 12.7 4,627 9.7 Missing 3 560 Ever had colonoscopy 139 64.4 30,159 62.2 Missing 0 16 NSAID use in the past 12 months 33 15.3 9,179 18.3 Missing 0 0 Ever used HRT 109 50.7 21,980 45.5 Missing 1 151 Mean (range) Mean (range) Physical activity (total MET-hours per week) 213 46.0 (7.2–157.8) 48,078 50.8 (7.2–350.3) Total caloric intake (kcal/day) 216 1,654.6 (429.8–3,768.6) 48,488 1,616.9 (400.2–3,997) Unprocessed red meat intake (g/day) 216 31.2 (0–239.1) 48,488 28.4 (0–515.9) Processed meat intake (g/day) 216 16.7 (0.4–60.6) 48,488 14.9 (0–165.6) White meat intake (g/day) 216 44.5 (0–199.8) 48,488 42.6 (0–502.1) Fruit and vegetable intake (cup eq) 216 3.5 (0.5–11.7) 48,488 3.4 (0–21.0) Dairy intake (cup eq) 216 1.4 (0.1–5.5) 48,488 1.4 (0.02–9.4) Fiber intake (g/day) 216 16.8 (4.6–44.3) 48,488 17.0 (0–82.4) Fat intake (g/day) 216 69.8 (16.7–198.8) 48,488 67.8 (4.0–268.1) Dietary and supplementary folate (DFE) 216 927.6 (140.5–2,579.6) 48,488 939.6 (22.1–3,865.1) Dietary and supplementary calcium (mg/d) 216 1,261.4 (205.2–3,132.7) 48,488 1,292.2 (63.0–5,738.8) Abbreviations: DFE, dietary folate equivalents; HRT, hormone replacement therapy.
- Table 2.
Crude and adjusteda association between unprocessed red and processed meat consumption, meat subtypes, and specific meat products and risk of colorectal cancer.
Meat type Continuous Quartile 1 (Ref) Quartile 2 Quartile 3 Quartile 4 Ptrendb Aggregate meat variables Total meatc N cases (N adjusted) 216 (210) 50 (49) 52 (51) 50 (48) 64 (62) Median g/day 74.59 (1.0–651.0) 33.51 60.95 90.49 144.95 Crude, HR (95% CI) 1.13e (1.02–1.27) 1.0 1.07 (0.72–1.57) 1.06 (0.72–1.57) 1.40 (0.96–2.03) 0.09 Adjusted, HRadj (95% CI) 1.10e (0.95–1.27) 1.0 1.03 (0.69–1.54) 0.98 (0.65–1.50) 1.26 (0.80–1.98) 0.30 Unprocessed red meat N cases (N adjusted) 216 (210) 51 (51) 53 (52) 53 (50) 59 (57) Median g/day (range) 21.21 (0.0–515.9) 7.31 16.16 27.75 53.50 Crude, HR (95% CI) 1.23e (1.00–1.52) 1.0 1.07 (0.73–1.58) 1.10 (0.75–1.61) 1.24 (0.85–1.81) 0.24 Adjusted, HRadj (95% CI) 1.14e (0.88–1.48) 1.0 1.00 (0.68–1.49) 0.96 (0.64–1.44) 1.04 (0.68–1.60) 0.76 Processed meat N cases (N adjusted) 216 (210) 49 (49) 48 (47) 48 (47) 71 (67) Median g/day (range) 11.17 (0.0–165.6) 4.25 8.62 14.49 28.31 Crude, HR (95% CI) 1.40f (1.12–1.75) 1.0 1.03 (0.69–1.53) 1.09 (0.73–1.63) 1.70 (1.18–2.45) 0.002 Adjusted, HRadj (95% CI) 1.28f (0.98–1.67) 1.0 0.98 (0.66–1.48) 1.02 (0.68–1.55) 1.52 (1.01–2.30) 0.02 White meatd N cases (N adjusted) 216 (210) 50 (49) 58 (55) 47 (46) 61 (60) Median g/day 33.99 (0.0–502.1) 13.07 26.39 43.18 77.17 Crude, HR (95% CI) 1.11e (0.92–1.34) 1.0 1.20 (0.82–1.75) 0.97 (0.65–1.45) 1.30 (0.89–1.88) 0.36 Adjusted, HRadj (95% CI) 1.04e (0.84–1.30) 1.0 1.12 (0.77–1.79) 0.92 (0.60–1.39) 1.17 (0.77–1.79) 0.61 Meat subtypes Beef N cases (N adjusted) 216 (210) 66 (64) 33 (32) 63 (61) 54 (53) Median g/day 2.80 (0.0–249.3) 0.00 1.40 5.67 13.08 Crude, HR (95% CI) 1.08f (0.86–1.34) 1.0 1.35 (0.89–2.06) 1.34 (0.95–1.90) 1.18 (0.82–1.69) 0.40 Adjusted, HRadj (95% CI) 1.05f (0.83–1.32) 1.0 1.49 (0.97–2.29) 1.41 (0.99–2.01) 1.18 (0.81–1.70) 0.48 Pork N cases (N adjusted) 216 (210) 68 (66) 28 (28) 73 (72) 47 (44) Median g/day 1.45 (0.0–258.1) 0.00 1.45 3.39 13.54 Crude, HR (95% CI) 1.09f (0.80–1.50) 1.0 1.21 (0.78–1.89) 1.32 (0.95–1.84) 1.30 (0.90–1.89) 0.18 Adjusted, HRadj (95% CI) 1.00f (0.71–1.42) 1.0 1.34 (0.86–2.09) 1.42 (1.01–1.99) 1.25 (0.85–1.84) 0.35 Poultry N cases (N adjusted) 216 (210) 56 (55) 51 (49) 45 (43) 64 (63) Median g/day 19.48 (0.0–486.2) 6.15 14.20 25.60 50.97 Crude, HR (95% CI) 1.09f (0.96–1.24) 1.0 0.95 (0.65–1.39) 0.87 (0.59–1.30) 1.30 (0.90–1.86) 0.12 Adjusted, HRadj (95% CI) 1.05f (0.91–1.22) 1.0 0.90 (0.61–1.33) 0.80 (0.53–1.21) 1.18 (0.79–1.76) 0.27 Seafood N cases (N adjusted) 216 (210) 57 (55) 50 (49) 47 (46) 62 (60) Median g/day 11.23 (0.0–359.6) 3.32 8.25 15.08 31.84 Crude, HR (95% CI) 1.03f (0.86–1.24) 1.0 0.85 (0.58–1.24) 0.77 (0.52–1.13) 0.99 (0.69–1.42) 0.88 Adjusted, HRadj (95% CI) 0.98f (0.80–1.20) 1.0 0.83 (0.56–1.22) 0.74 (0.49–1.10) 0.90 (0.61–1.34) 0.84 Specific unprocessed red and processed meat products Hamburgers, cheeseburgers N cases (N adjusted) 216 (210) 49 (48) 55 (54) 79 (76) 33 (32) Median g/day 4.87 (0.0–219.0) 0.61 2.43 5.62 20.86 Crude, HR (95% CI) 1.28f (0.95–1.73) 1.0 1.13 (0.77–1.66) 1.27 (0.89–1.81) 1.46 (0.94–2.27) 0.09 Adjusted, HRadj (95% CI) 1.17f (0.84–1.62) 1.0 1.11 (0.75–1.65) 1.18 (0.81–1.71) 1.29 (0.80–2.07) 0.28 Ham, baloney, lunch meat N cases (N adjusted) 216 (210) 61 (61) 41 (40) 68 (66) 46 (43) Median g/day 1.87 (0.0–112.0) 0.46 1.39 4.31 24.26 Crude, HR (95% CI) 1.28f (0.95–1.73) 1.0 0.91 (0.61–1.36) 1.14 (0.80–1.61) 1.42 (0.97–2.09) 0.04 Adjusted, HRadj (95% CI) 1.18f (0.85–1.64) 1.0 0.87 (0.58–1.30) 1.07 (0.75–1.52) 1.25 (0.83–1.88) 0.15 Bacon N cases (N adjusted) 216 (210) 64 (62) 31 (31) 58 (57) 63 (60) Median g/day 0.43 (0.0–25.6) 0.11 0.31 0.63 1.97 Crude, HR (95% CI) 2.29g (1.27–4.13) 1.0 1.02 (0.67–1.57) 1.44 (1.01–2.06) 1.58 (1.11–2.24) 0.01 Adjusted, HRadj (95% CI) 2.07g (1.10–3.94) 1.0 1.02 (0.66–1.58) 1.41 (0.98–2.02) 1.46 (1.01–2.11) 0.03 Hot dogs, dinner sausages N cases (N adjusted) 216 (210) 90 (87) 32 (32) 46 (45) 48 (46) Median g/day 1.48 (0.0–180.0) 0.74 1.48 1.50 6.92 Crude, HR (95% CI) 1.07g (0.77–1.49) 1.0 1.11 (0.74–1.67) 1.03 (0.72–1.47) 1.36 (0.95–1.93) 0.09 Adjusted, HRadj (95% CI) 0.93g (0.62–1.40) 1.0 1.08 (0.72–1.63) 0.99 (0.69–1.42) 1.23 (0.84–1.79) 0.21 Breakfast sausages N cases (N adjusted) 216 (210) 60 (59) 52 (52) 24 (22) 80 (77) Median g/day 0.89 (0.0–81.0) 0.00 0.45 0.90 3.86 Crude, HR (95% CI) 1.57g (1.26–1.97) 1.0 0.98 (0.68–1.42) 0.91 (0.57–1.47) 1.98 (1.42–2.78) <0.001 Adjusted, HRadj (95% CI) 1.47g (1.14–1.90) 1.0 0.97 (0.67–1.41) 0.83 (0.51–1.35) 1.85 (1.30–2.64) <0.001 Note: Significant (P < 0.05) values are bolded.
↵aModel adjusted for total calories (kcal/day, continuous), BMI (kg/m2, continuous), highest educational attainment (high school or less, some college, Bachelor's degree, and above), physical activity (MET-h/wk), race/ethnicity (non-Hispanic White, non-Hispanic Black, Hispanic/other), and family history of colorectal cancer (yes/no).
↵bPtrend calculated using assigning the median value of each quartile.
↵cTotal meat is a sum variable of red meat (including organ meat), processed meat, and white meat.
↵dWhite meat includes seafood and poultry.
↵ePer 50 grams/day.
↵fPer 25 grams/day.
↵gPer 10 grams/day.
- Table 3.
Multivariable HRadja for the association between red meat intake by cooking practice and/or doneness level and risk of colorectal cancer.
Red meat cooking method and/or doneness Continuous (50 g/day) Quartile 1 (Ref) Quartile 2 Quartile 3 Quartile 4 Ptrendb Grilled red meat N cases 210 60 46 62 42 Median g/day 2.43 0.0 1.20 5.62 20.86 HRadj (95% CI) 1.20 (0.83–1.73) 1.0 1.23 (0.84–1.82) 1.31 (0.91–1.88) 1.20 (0.80–1.80) 0.62 Grilled red meat (excl. pork) N cases 203 56 46 61 40 Median g/day 2.43 0.0 1.23 5.62 20.86 HRadj (95% CI) 1.35 (0.90–2.01) 1.0 1.29 (0.87–1.92) 1.32 (0.91–1.91) 1.28 (0.84–1.94) 0.49 Pan-fried red meatc N cases 210 155 — — 55 Median g/day 0.0 0.0 — — 5.62 HRadj (95% CI) 0.99 (0.47–2.06) 1.0 — — 1.01 (0.74–1.38) 0.90 Medium-well to charred red meat N cases 208 62 39 57 50 Median g/day 2.43 0.0 1.23 5.62 10.43 HRadj (95% CI) 0.99 (0.61–1.61) 1.0 0.99 (0.66–1.48) 1.14 (0.79–1.64) 1.03 (0.70–1.51) 0.73 Grilled and medium-well to charred red meatc N cases 210 117 — 42 51 Median g/day 0.0 0.0 — 2.43 10.43 HRadj (95% CI) 0.72 (0.33–1.60) 1.0 — 0.89 (0.62–1.26) 1.01 (0.72–1.41) 0.90 Note: Significant (P < 0.05) values are bolded.
↵aModel adjusted for total calories (kcal/day, continuous), BMI (kg/m2, continuous), highest educational attainment (high school or less, some college, Bachelor's degree and above), physical activity (MET-h/wk, continuous), race/ethnicity (non-Hispanic White, non-Hispanic Black, Hispanic/other), and family history of colorectal cancer (yes/no).
↵bPtrend calculated using assigning the median value of each quartile.
↵cFor pan-fried meat, quartiles 1–3 are combined. For grilled and medium-well to charred red meat, quartiles 1–2 are combined.
- Table 4.
Multivariable HRadj for the association between meat cooking practices, doneness, and risk of colorectal cancer for specific red meat productsa.
Cases HRadjb (95% CI) Preferred meat cooking method by meat product Steak Don't eat steak 11 1.0 Pan-fried 16 2.09 (0.96–4.53) Oven broiled 29 1.69 (0.84–3.40) Grilled or barbequed 151 2.23 (1.20–4.14) Hamburger Don't eat hamburgers or cheeseburgers 9 1.0 Pan-fried 39 1.63 (0.79–3.40) Oven broiled 11 1.55 (0.64–3.75) Grilled or barbequed 144 1.98 (1.00–3.91) Pork chops Don't eat pork chops 30 1.0 Pan-fried 58 1.19 (0.76–1.86) Baked 59 1.17 (0.74–1.80) Oven broiled 17 1.11 (0.61–2.03) Grilled or barbequed 44 1.13 (0.70–1.80) Preferred meat doneness by meat product Steak Don't eat steak 12 1.0 Rare or medium rare 85 2.34 (1.27–4.32) Medium or medium-well 86 1.52 (0.83–2.79) Well done, very well done, or charred 25 1.55 (0.77–3.11) Hamburger Don't eat hamburgers or cheeseburgers 9 1.0 Rare or medium rare 22 2.27 (1.04–4.95) Medium or medium-well 89 1.77 (0.88–3.52) Well done, very well done, or charred 88 1.84 (0.92–3.68) Pork chops Don't eat pork chops 28 1.0 Just until done 47 1.31 (0.82–2.10) Well done 97 1.06 (0.69–1.62) Very well done or charred 35 1.50 (0.91–2.49) Bacon or sausage Don't eat bacon or sausages 17 1.0 Just until done 23 1.67 (0.89–3.14) Well done, crisp, or charred 168 1.32 (0.80–2.18) Grilled and doneness preferences combined, by meat product Steak: doneness and grilled combined Don't eat steak 12 1.0 Rare or medium rare 62 2.58 (1.37–4.86) Medium or medium-well 73 1.93 (1.04–3.60) Well done, very well done, or charred 16 1.75 (0.82–3.74) Hamburgers: doneness and grilled combined Don't eat hamburgers or cheeseburgers 9 1.0 Rare or medium rare 17 2.62 (1.16–5.93) Medium or medium-well 71 2.01 (0.99–4.06) Well done, very well done, or charred 59 1.97 (0.97–4.00) Note: Significant (P < 0.05) values are bolded.
↵aFor each model, the reference category includes participants who reported eating red meat but not the specific meat product or using the specific cooking method under evaluation.
↵bModel adjusted for total calories (kcal/day, continuous), BMI (kg/m2, continuous), highest educational attainment (high school or less, some college, Bachelor's degree and above), physical activity (MET-h/wk, continuous), race/ethnicity (non-Hispanic White, non-Hispanic Black, Hispanic/other), and family history of colorectal cancer (yes/no).
- Table 5.
Multivariable HRadja for the association between processed meat consumption and risk of colorectal cancer by age and BMI status at baseline.
Age at baselinec BMI statusd,e < 55 years old (N = 22,950) 55+ years old (N = 25,756) Normal (N = 18,312) Overweight (N = 15,493) Obese (N = 14,346) N HRadj (95% CI) N HRadj (95% CI) N HRadj (95% CI) N HRadj (95% CI) N HRadj (95% CI) Processed meat Continuous (per 25 g/day) 62 1.07 (0.67–1.72) 148 1.40 (1.02–1.94) 62 1.03 (0.56–1.88) 76 1.35 (0.87–2.10) 70 1.35 (0.89–2.04) Tertile 1 (4.96 g/day) 15 1.0 52 1.0 22 1.0 28 1.0 16 1.0 Tertile 2 (11.20 g/day) 20 1.05 (0.53–2.07) 42 0.94 (0.62–1.42) 28 1.77 (1.00–3.14) 20 0.72 (0.40–1.30) 14 0.70 (0.32–1.38) Tertile 3 (24.58 g/day) 27 1.12 (0.56–2.25) 54 1.41 (0.92–2.17) 12 0.99 (0.47–2.11) 28 1.15 (0.64–2.07) 40 1.58 (0.83–3.01) Ptrendb 0.81 0.07 0.92 0.46 0.03 Ham, baloney, lunch meat Continuous (per 25 g/day) 62 0.97 (0.54–1.75) 148 1.30 (0.88–1.93) 62 0.98 (0.48–2.00) 76 1.28 (0.75–2.16) 70 1.26 (0.75–2.10) Tertile 1 (0.46 g/day) 10 1.0 63 1.0 27 1.0 24 1.0 21 1.0 Tertile 2 (2.15 g/day) 26 1.76 (0.85–3.67) 43 0.76 (0.51–1.12) 14 0.61 (0.32–1.17) 31 1.26 (0.73–2.15) 24 0.89 (0.49–1.60) Tertile 3 (16.00 g/day) 26 2.00 (0.94–4.25) 42 1.11 (0.74–1.67) 21 1.35 (0.75–2.45) 21 1.22 (0.66–2.24) 25 1.16 (0.63–2.15) Ptrendb 0.22 0.32 0.10 0.82 0.40 Hot dogs, dinner sausages Continuous (per 10 g/day) 62 0.85 (0.43–1.72) 148 0.97 (0.60–1.58) 62 0.82 (0.27–2.47) 76 0.85 (0.38–1.90) 70 0.96 (0.57–1.63) Tertile 1 (0.74 g/day) 25 1.0 62 1.0 27 1.0 31 1.0 28 1.0 Tertile 2 (1.48 g/day) 12 0.73 (0.37–1.47) 35 1.02 (0.68–1.55) 20 1.59 (0.89–2.85) 21 1.18 (0.68–2.06) 7 0.31 (0.14–0.71) Tertile 3 (3.46 g/day) 25 1.06 (0.59–1.90) 50 1.34 (0.91–1.98) 15 1.42 (0.75–2.72) 24 1.21 (0.70–2.10) 35 1.02 (0.61–1.71) Ptrendb 0.71 0.11 0.20 0.59 0.38 Bacon Continuous (per 10 g/day) 62 3.72 (1.79–7.76) 148 1.10 (0.40–3.06) 62 0.94 (0.13–6.74) 76 1.94 (0.61–6.17) 70 2.67 (1.16–6.15) Tertile 1 (0.11 g/day) 12 1.0 50 1.0 23 1.0 26 1.0 12 1.0 Tertile 2 (0.43 g/day) 14 1.06 (0.49–2.30) 52 1.28 (0.86–1.89) 20 1.23 (0.67–2.25) 26 1.13 (0.65–1.95) 20 1.41 (0.69–2.91) Tertile 3 (1.83 g/day) 36 2.63 (1.34–5.14) 46 1.10 (0.73–1.66) 19 1.49 (0.80–2.76) 24 0.99 (0.56–1.74) 38 2.17 (1.12–4.19) Ptrendb <0.001 0.84 0.15 0.80 0.01 Breakfast sausages Continuous (per 10 g/day) 62 1.31 (0.82–2.11) 148 1.54 (1.15–2.06) 62 1.51 (0.71–3.20) 76 1.31 (0.78–2.20) 70 1.46 (1.04–2.05) Tertile 1 (0.00 g/day) 18 1.0 49 1.0 29 1.0 23 1.0 15 1.0 Tertile 2 (0.89 g/day) 10 0.51 (0.23–1.11) 46 1.07 (0.72–1.61) 20 0.88 (0.50–1.56) 23 1.06 (0.59–1.89) 12 0.71 (0.33–1.52) Tertile 3 (2.08 g/day) 34 1.57 (0.87–2.83) 53 1.48 (0.99–2.21) 13 0.89 (0.46–1.73) 30 1.59 (0.91–2.77) 43 2.03 (1.11–3.70) Ptrendb 0.05 0.05 0.65 0.07 0.003 Note: Significant (P < 0.05) values are bolded.
↵aFor age, model adjusted for total calories (kcal/day, continuous), BMI (kg/m2, continuous), highest educational attainment (high school or less, some college, Bachelor's degree and above), physical activity (MET-h/wk, continuous), race/ethnicity (non-Hispanic White, non-Hispanic Black, Hispanic/other), and family history of colorectal cancer (yes/no); for BMI, model adjusted for total calories (kcal/day, continuous), highest educational attainment (high school or less, some college, Bachelor's degree and above), physical activity (MET-h/wk, continuous), race/ethnicity (non-Hispanic White, Non-Hispanic Black, Hispanic/other), and family history of colorectal cancer (yes/no).
↵bPtrend calculated using assigning the median value of each tertile.
↵cTest for interaction: age and red meat (P = 0.30); age and processed meat (P = 0.31); age and hot dogs/dinner sausages (P = 0.36); age and ham/baloney/lunch meat (P = 0.72); age and bacon (P = 0.05); age and breakfast sausage (P = 0.24).
↵dTest for interaction: BMI and red meat (P = 0.71); BMI and processed meat (P = 0.68); BMI and hot dogs/dinner sausages (P = 0.97); BMI and ham/baloney/lunch meat (P = 0.29); BMI and bacon (P = 0.10); BMI and breakfast sausage (P = 0.24).
↵eNormal BMI: 18.5–24.9; overweight BMI: 25.0–29.9; obese BMI: ≥ 30.0 [underweight (BMI < 18.5, N = 541 noncases, 2 cases) excluded].
Additional Files
Supplementary Data
- Supplementary Tables 1-5 (NO COLOR) - Supplemental Table 1. Multivariable-adjusted hazard ratios (HRadj) for the association between meat consumption and risk of colon or rectal cancer Supplemental Table 2. Multivariable-adjusted hazard ratios (HRadj) for the association between meat consumption and risk of colorectal cancer (CRC) by diagnosis source Supplemental Table 3. Adjusted categorical models of unprocessed red meat, processed meat, white meat, and specific meat products and risk of colorectal cancer, mutually-adjusting for other meat consumption variables Supplemental Table 4. Continuous and categorical final models of aggregate meat and specific meat products and risk of colorectal cancer, excluding women with (1) a previous cancer diagnosis, (2) a family history of CRC, (3) a CRC diagnosis made within 1 year of baseline, and (4) a CRC diagnosis made within 1 year of baseline Supplemental Table 5. Adjusted association between unprocessed red meat, processed meat, meat subtypes, and specific meat products and risk of colorectal cancer, using energy-adjusted meat intake.
Volume 29, Issue 1
