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American Journal of Epidemiology logoLink to American Journal of Epidemiology
. 2013 Jun 19;178(2):172–183. doi: 10.1093/aje/kwt099

Dietary Intakes of Red Meat, Poultry, and Fish During High School and Risk of Colorectal Adenomas in Women

Katharina Nimptsch *, Adam M Bernstein, Edward Giovannucci, Charles S Fuchs, Walter C Willett, Kana Wu
PMCID: PMC3712658  PMID: 23785116

Abstract

Adolescent diet may be etiologically relevant for colorectal carcinogenesis. We examined the association between meat and fish intakes during adolescence and the risk of colorectal adenomas later in life among 19,771 women participating in the Nurses' Health Study II. Subjects had completed a validated food frequency questionnaire in 1998 (when aged 34–51 years) about their diets during high school and subsequently underwent at least 1 lower-bowel endoscopy during the study period (1998–2007). During this period, 1,494 subjects were diagnosed with colorectal adenomas. Intake of red meat during adolescence was not associated with colorectal adenoma risk when comparing those in the highest versus lowest category of intake (odds ratio (OR) = 1.04, 95% confidence interval (CI): 0.81, 1.35). Similarly, intake of fish during adolescence was not associated with colorectal adenoma risk (OR = 0.96, 95% CI: 0.78, 1.17). Intake of poultry during adolescence was associated with a lower risk of total colorectal (OR = 0.80, 95% CI: 0.64, 0.99), distal (OR = 0.71, 95% CI: 0.51, 0.99), rectal (OR = 0.51, 95% CI: 0.29, 0.90), and advanced (OR = 0.60, 95% CI: 0.38, 0.93) adenomas. Replacement of 1 serving per day of red meat with 1 serving per day of poultry or fish was associated with 41% and 35% decreased risks for rectal adenomas and advanced adenomas, respectively. Our findings do not suggest an association between red meat intake during adolescence and colorectal adenomas later in life, but higher poultry intake during this time was associated with a lower risk of colorectal adenomas.

Keywords: adenomatous polyps, adolescent, fish, food intake, meat, poultry

Editor's note: An invited commentary on this article appears on page 184.

A report published in 2007 by the World Cancer Research Fund (London, United Kingdom) and the American Institute for Cancer Research (Washington, DC) concluded that there is “convincing” evidence that higher intakes of red and processed meats are causally associated with increased risk of colorectal cancers (1). In a recent meta-analysis that included 21 prospective studies, higher intakes of red and processed meats were significantly positively associated with the risk of colorectal cancer (2). Positive associations between red meat intake and the risk of colorectal adenomas, which are precursors of colorectal cancer (3), have been observed in some (4–7) but not all (8–10) studies. Possible mechanisms through which red and processed meats may be involved in carcinogenesis include heterocyclic amines and related compounds that are formed during the cooking process, as well as N-nitroso compounds that are formed endogenously from nitrate or nitrite, which are commonly added as preservatives to processed meats (11). Furthermore, it has been proposed that heme iron, which catalyzes the formation of N-nitroso compounds and oxidized lipids (12), may also play an important role in colorectal carcinogenesis (12–14). Limited evidence from several cohort studies suggests that fish intake is inversely associated with colorectal cancer risk (15–17), possibly through the effects of ω-3 polyunsaturated fatty acids, which are abundant in fatty fish (18). Poultry intake has been associated with decreased risk of colorectal cancer (16, 19, 20), but for colorectal adenomas, the evidence is less consistent (4–6, 10, 21, 22). The ratio of red meat to poultry and fish has been consistently positively associated with the risks of colorectal cancer (20, 23, 24) and adenomas (21).

All of these studies investigated diet during adulthood in relationship to colorectal cancer or adenomas; however, there is a lack of research focusing on dietary exposures earlier in life. We recently observed a positive association between body fatness in early life (5–10 years of age) and the risk of colorectal adenomas later in life independent of adult body fatness, suggesting that certain risk factors for colorectal cancer may act as early as childhood or adolescence (25). Colorectal carcinogenesis is a long process that can take several decades, and the initial steps of carcinogenesis may occur at young ages. Although few studies have investigated diet during adolescence in relationship to risk of colorectal cancer (26, 27), red meat intake during adolescence has been associated with the risk of breast cancer (28–30).

Our aim was to examine the association between intakes of unprocessed red meat, processed red meat, poultry, and fish during adolescence and the risk of colorectal adenomas later in life among participants of a large, prospective female cohort from the Nurses' Health Study II (NHS II).

MATERIALS AND METHODS

Study population

The NHS II is an ongoing prospective cohort study of 116,671 female registered nurses who were 25–42 years of age when they responded to a mailed questionnaire about their lifestyles and medical histories in 1989. Through biennial mailed questionnaires, study participants are followed to update risk factors for diseases and to ascertain newly diagnosed diseases. The study has maintained follow-up response rates of 90% or higher in each 2-year follow-up cycle (31). Dietary intakes during the previous year were assessed by self-administered food frequency questionnaires (FFQs) in 1991, 1995, 1999, and 2003. In 1997, participants were asked if they would be willing to fill out a supplemental high school food frequency questionnaire (HS-FFQ) about their diets during high school. Approximately 55% of the cohort indicated willingness to do so (n = 64,380), and 47,355 (83% of those who were sent the questionnaire) returned the HS-FFQ in 1998, at which time they were 34–51 years of age. Baseline diet and risk factors for colorectal cancer and adenomas did not differ substantially between women who indicated willingness to fill out the HS-FFQ and those who did not.

For this analysis of colorectal adenomas, we included only women who returned the HS-FFQ and reported having had at least 1 lower-bowel endoscopy during the study period (i.e., between returning the HS-FFQ and December 2007). We excluded women with histories of cancer or colorectal polyps, as well as women who reported implausible daily caloric intakes on the 1991 baseline FFQ (<600 or ≥3,500 kcal/day) or the HS-FFQ (<500 or ≥5,000), leaving 19,771 women for the analysis. This study was approved by the institutional review boards of Brigham and Women's Hospital and the Harvard School of Public Health (both in Boston, Massachusetts).

Assessment of high school and adult dietary intakes

Dietary intakes during high school (grades 9–12, corresponding to ages 13–17 years) were assessed by using the 124-item HS-FFQ, which was specifically designed to include foods (e.g., milkshakes, peanut butter, French fries) that were commonly consumed during the time period when study participants attended high school (i.e., between 1960 and 1981). In the HS-FFQ, participants were asked to indicate how often, on average, they had consumed specific amounts of each food item when they were in high school. Possible responses ranged from “never or less than once per month” to “6 or more per day” (28). Reproducibility was investigated in 333 randomly selected NHS II participants who completed 2 HS-FFQs at a 4-year interval (32). Correlations were 0.65 (range, 0.50–0.77) for nutrient intake, 0.52 for red meat, 0.44 for chicken or turkey, and 0.59 for canned tuna. Validity was examined by comparing dietary intakes reported by mothers of 272 NHS II participants with intakes reported on the 1998 HS-FFQ (32); correlations of the nurses' own and their mothers’ reports were 0.40 (range, 0.13–0.59) for nutrient intake. In another validation study among 80 young adults (children of randomly selected NHS II participants) who had completed three 24-hour recalls and 2 youth/adolescent FFQs at ages 13–18 years and a HS-FFQ 10 years later, the mean correlations for nutrient intake between the HS-FFQ and the three 24-hour recalls and the youth/adolescent FFQ were 0.69 (range, 0.45–0.97) and 0.58 (range, 0.40–0.88), respectively (33). By using the First National Health and Nutrition Examination Survey (NHANES I) FFQ database, we calculated intakes of the main meat items investigated in this study in girls aged 13–18 years (34). NHANES I was conducted between 1971 and 1975, which represents approximately the median time period during which the NHS II participants attended high school (i.e., 1960–1981). Mean intakes in servings per day did not differ considerably when comparing intakes reported in the NHANES I with those in our study. In NHANES I, the mean reported intake of total meat (meat and poultry) was 1.36 (standard deviation (SD), 0.65) servings, and the mean intake of fish was 0.14 (SD, 0.14) servings; in NHS II, the mean intake of total meat was 1.96 (SD, 0.86) servings, and the mean intake of fish was 0.26 (SD, 0.24) servings.

Dietary intakes during adulthood were assessed in 1991, 1995, 1999, and 2003 by using semiquantitative FFQs (including approximately 131 food items), which ascertained habitual dietary intakes during the past 12 months (35).

Assessment of meat and fish intakes

The individual meat and fish items on the HS-FFQ were the same as those included in the adult FFQs. Unprocessed red meat was defined as “beef or lamb as a main dish,” “pork as a main dish,” or “beef, pork, or lamb as a sandwich or mixed dish.” Processed red meat was defined as “hot dog,” “bacon,” or “processed meats, e.g., salami, bologna, sausage, etc.” Poultry was defined as “chicken or turkey” or “chicken or turkey as a sandwich or mixed dish.” Fish was defined as “canned tuna,” “dark meat fish,” “breaded fish cakes, pieces, or fish sticks,” or “other fish.”

Ascertainment of cases

If a participant indicated a diagnosis of a colorectal polyp on 1 of the follow-up questionnaires, we asked her for permission to obtain her medical records. Study investigators verified the diagnosis of colorectal adenoma by review of the pathology reports and extracted information on anatomical locations, histological types, and sizes of the reported adenomas. Adenomas of the cecum, ascending colon, hepatic flexure, transverse colon, or splenic flexure were defined as proximal; those in the descending or sigmoid colon were defined as distal; and those in the rectosigmoid junction or rectum were defined as rectal adenomas. Large (≥1 cm) adenomas or adenomas with any mention of villous features or high-grade dysplasia were considered advanced adenomas, and small (<1 cm) or tubular adenomas were considered nonadvanced (early) adenomas.

Sigmoidoscopies versus colonoscopies

Before 2003, the NHS II follow-up questionnaires inquired only whether the participants had had a lower-bowel endoscopy (i.e., sigmoidoscopy or colonoscopy) during the past 2 years. Therefore, it is possible that some of the women who reported having a lower-bowel endoscopy before 2003 may have had sigmoidoscopies, which visualize only the rectum and distal colon, rather than colonoscopies, which also visualize the proximal colon. Starting with the 2003 follow-up questionnaire, subjects were asked separately about sigmoidoscopies and colonoscopies. In addition, on the 2005 questionnaire, participants were asked to provide information on when they had sigmoidoscopies versus colonoscopies in the past. The appropriateness of including proximal adenomas as an outcome in this setting has been described previously (25).

Statistical analysis

The association between meat and fish intakes during high school (as categorical variables) and the risk of colorectal adenomas later in life was analyzed by using multivariable logistic regression to calculate odds ratios approximating relative risks. Tests for trends across categories were performed by modeling the median values of each intake category as continuous variables and deriving the P value for trend by using Wald's test. Categories were defined by taking into consideration portion sizes derived from the 1994–1996 Continuing Survey of Food Intakes by Individuals (36). In addition, associations were examined by modeling meat and fish intakes as continuous variables (in g/day).

Multivariable models were adjusted for known and suspected risk factors for colorectal cancer and adenomas, including age at return of the HS-FFQ, family history of colorectal cancer, time period of endoscopy, number of reported endoscopies during the study period (1 endoscopy vs. ≥2 endoscopies), endoscopy prior to the study period (i.e., endoscopy prior to the return of the HS-FFQ, yes/no), reason for the last endoscopy (screening vs. symptoms), height, body mass index (weight (kg)/height (m)2) at age 18 years, pack-years of smoking, adolescent and current physical activity levels, aspirin use, and current cumulative average alcohol intake. Covariates that were assessed repeatedly in follow-up questionnaires (smoking, physical activity, and aspirin use) were updated to best represent the exposure in the 2-year interval before the most recent endoscopy. To best represent long-term adult dietary intakes, we calculated cumulative updated intakes by averaging intakes from all available FFQs up to the start of the 2-year interval prior to the most recent endoscopy. Additional adjustments for age at menarche, oral contraceptive use, menopausal status/postmenopausal hormone use, pack-years of smoking before age 20 or 30 years, body shape during adolescence (instead of body mass index at age 18 years, estimated by 9-level pictograms) (32), current body mass index, current dietary intakes (energy, fat, fiber, folate, calcium, and vitamin D) or dietary intakes during high school (fat, protein, fiber, calcium, folate, and vitamin D) did not change risk estimates substantially and were not included in the final models.

We also estimated the risk of adenomas associated with substitution of 1 food item for another (e.g., poultry for total red meat). For this analysis, both items were included in the multivariable model as continuous variables, and the odds ratios and 95% confidence intervals were calculated from the difference in their coefficients and their covariance (37, 38).

We investigated the associations between meat and fish intakes during adolescence and colorectal adenoma by location (proximal, distal, or rectal) and stage (nonadvanced or advanced). By using polytomous logistic regression, we performed paired comparisons of the association between diet during high school and the occurrence of adenoma subtypes (39).

All reported P values are 2-sided, and a P < 0.05 was considered statistically significant.

RESULTS

Among 19,771 women who underwent at least 1 lower-bowel endoscopy between 1998 and December 2007, 1,494 women were diagnosed with at least 1 colorectal adenoma. These consisted of 714 proximal, 675 distal, and 249 rectal adenomas. By stage, 1,113 cases were classified as nonadvanced and 305 as advanced adenomas.

Intakes of meat and fish during high school correlated moderately with adult intakes (cumulative updated average). Spearman correlation coefficients for intakes in high school and adulthood were 0.34 for total red meat, 0.33 for unprocessed red meat, 0.27 for processed red meat, 0.29 for poultry, and 0.38 for fish (all P's < 0.0001). The median reported intake of total red meat during high school was 124.4 g/day (interquartile range (IQR), 91–164 g/day), which was twice that during adulthood (median, 57 g/day; IQR, 37–78 g/day). Intake of poultry was slightly lower during high school (median, 32 g/day; IQR, 26–66 g/day) than during adulthood (median, 51 g/day; IQR, 35–68 g/day), and dietary intake of fish was similar during high school (median, 22 g/day; IQR, 14–36 g/day) and adulthood (median, 18 g/day; IQR, 11–28 g/day).

Table 1 shows the characteristics of study participants by the lowest and highest categories of total red meat, poultry, and fish intakes during high school.

Table 1.

Characteristics by the Lowest and Highest Categories of Red Meat, Poultry, and Fish Intakes During High School, Nurses' Health Study II, United States, 1998–2007a

Characteristic Total Red Meat Intake During High School, g/day
 Poultry Intake During High School, g/day
 Fish Intake During High School, g/day
<75 (n = 2,869)
 ≥200 (n = 2,295)
 <20 (n = 3,998)
 ≥80 (n = 2,372)
 <10 (n = 3,641)
 ≥40 (n = 3,457)
Mean (SD) % Mean (SD) % Mean (SD) % Mean (SD) % Mean (SD) % Mean (SD) %
Age at 1997 questionnaire returnb, years 43.7 (4.2) 44.3 (3.8) 44.5 (3.9) 43.6 (4.1) 43.7 (4.2) 44.2 (3.9)
Age at most recent endoscopyb, years 51.1 (4.5) 51.7 (4.1) 51.8 (4.1) 51.0 (4.4) 51.1 (4.5) 51.5 (4.2)
BMIc (baseline) 24.8 (5.0) 27.1 (6.0) 25.7 (5.4) 26.0 (5.6) 25.7 (5.6) 26.2 (5.8)
BMIc at age 18 years 20.7 (2.9) 21.7 (3.5) 20.9 (3.1) 21.4 (3.4) 21.0 (3.1) 21.4 (3.4)
Height, cm 164.6 (6.6) 165.1 (6.6) 164.6 (6.9) 164.8 (6.6) 164.6 (6.6) 164.8 (6.6)
Current smokers (baseline) 9 11 11 8 10 9
Physical activity during 9th–12th grades, MET hours/week 48.0 (35.1) 52.6 (37.7) 47.8 (35.6) 54.2 (37.5) 48.5 (35.8) 54.2 (37.5)
Premenopausal status (baseline) 96 94 95 95 95 95
Family history of colorectal cancer (baseline) 19 20 21 20 21 20
Reason for most recent endoscopy was screening 70 66 66 68 67 67
Aspirin use (baseline) 2 or more times/ week 10 13 12 11 12 11
Dietary intakes during high school
 Animal fat, g/dayd 69.8 (17.2) 94.4 (14.8) 81.6 (19.5) 81.9 (15.3) 84.4 (19.0) 78.5 (15.7)
 Animal protein, g/dayd 70.4 (18.2) 91.4 (14.1) 72.8 (17.1) 92.9 (15.5) 76.1 (17.7) 86.8 (15.9)
 Calcium, mg/dayd 1,181 (403) 930 (274) 1,119 (390) 1,010 (301) 1,092 (382) 1,050 (312)
 Total folate, μg/dayd 350 (112) 285 (69) 307 (99) 329 (92) 302 (96) 334 (88)
 Heme iron, mg/dayd 1.2 (0.5) 2.4 (0.6) 1.6 (0.7) 2.1 (0.6) 1.7 (0.7) 1.9 (0.6)
 Total red meat, g/day 54.9 (17.7) 241 (45) 121 (62) 141 (59) 125 (60) 136 (60)
 Processed meat, g/day 9.4 (7.7) 40.7 (29.2) 21.9 (19.7) 23.1 (17.3) 20.6 (18.9) 24.6 (18.9)
 Poultry, g/day 40.4 (31.4) 51.8 (31.8) 15.3 (5.7) 105 (31) 39.8 (28.8) 57.3 (35.0)
 Fish, g/day 24.6 (28.2) 28.6 (25.8) 20.6 (23.1) 34.2 (27.6) 4.7 (3.2) 60.7 (27.7)
Adult dietary intakese
 Alcohol, g/day 3.2 (5.7) 3.4 (6.2) 2.9 (5.6) 3.7 (5.9) 3.0 (5.8) 3.8 (6.1)
 Animal fat, g/dayd 30.9 (9.6) 36.1 (9.1) 34.0 (9.6) 32.6 (8.7) 34.9 (9.4) 32.2 (9.1)
 Animal protein, g/dayd 58.9 (16.2) 65.4 (14.2) 60.5 (15.3) 64.4 (15.1) 61.8 (14.9) 63.5 (15.3)
 Calcium, mg/dayd 1,107 (445) 1,025 (400) 1,061 (431) 1,064 (394) 1,048 (423) 1,066 (410)
 Total folate, μg/dayd 508 (248) 451 (207) 462 (230) 497 (229) 459 (228) 493 (226)
 Heme iron, mg/dayd 1.0 (0.4) 1.3 (0.4) 1.1 (0.4) 1.2 (0.4) 1.1 (0.4) 1.1 (0.4)
 Total red meat, g/day 43.1 (31.2) 84.2 (48.4) 62.1 (41.6) 61.8 (41.4) 65.3 (40.0) 59.1 (40.6)
 Processed meat, g/day 4.4 (5.5) 8.0 (9.0) 6.1 (7.2) 5.8 (6.6) 6.0 (6.8) 5.6 (6.3)
 Poultry, g/day 55.7 (36.5) 69.7 (42.4) 52.5 (38.6) 78.5 (41.2) 58.4 (37.5) 70.2 (40.2)
 Fish, g/day 22.4 (19.7) 23.9 (21.9) 19.1 (17.0) 27.9 (21.7) 14.8 (14.6) 33.4 (25.4)
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Abbreviations: BMI, body mass index; MET, metabolic equivalent of task; SD, standard deviation.

a Values are standardized to the age distribution of the study population.

b Values are not age adjusted.

c Body mass index is weight (kg)/height (m)2.

d Energy adjusted by residual method.

e Cumulative updated average of 1991 and 1995 food frequency questionnaires.

In multivariable adjusted models, intakes during high school of total red meat, unprocessed red meat, processed red meat, and fish were not associated with risk of colorectal adenomas (Table 2). Associations were similar after additional adjustments for adult energy intake and total red meat, unprocessed red meat, processed red meat, and fish intakes, respectively (Table 2). When we examined fish intake by type of fish, neither breaded fish, canned tuna, dark meat fish, nor other fish was associated with risk of colorectal adenomas (data not shown). Greater intake of poultry during high school was associated with a lower risk of colorectal adenoma, and associations became statistically significant after adjustment for adult energy and poultry intakes (OR of the highest vs. lowest category = 0.80, 95% CI: 0.64, 0.99). Risk estimates from age-adjusted models were similar to those from multivariable-adjusted models (data not shown). When we mutually adjusted for intakes during high school of unprocessed red meat, processed red meat, poultry, and fish in multivariable models, the associations shown in Table 2 did not change considerably (data not shown). A high ratio of total red meat to poultry intake during high school was associated with increased risk of colorectal adenoma.

Table 2.

Association Between Meat and Fish Intakes During High School and Colorectal Adenomas, Nurses' Health Study II, United States, 1998–2007

No. of Cases No. of Controls Adjusted ORa 95% CI Adjusted ORb 95% CI
Total red meat intake, g/dayc
 <75 191 2,678 1.00 Referent 1.00 Referent
 75 to <100 273 3,136 1.17 0.95, 1.44 1.17 0.95, 1.43
 100 to <125 282 3,410 1.08 0.88, 1.33 1.08 0.87, 1.32
 125 to <150 246 3,046 1.02 0.82, 1.27 1.01 0.81, 1.26
 150 to <200 323 3,885 1.08 0.87, 1.33 1.06 0.85, 1.31
 ≥200 179 2,116 1.08 0.84, 1.39 1.04 0.81, 1.35
  P for trend 0.98 0.79
 Per 100 g 0.97 0.87, 1.09 0.95 0.85, 1.07
Unprocessed red meat intake, g/day
 <50 129 1,593 1.00 Referent 1.00 Referent
 50 to <75 278 3,431 0.92 0.73, 1.16 0.93 0.74, 1.18
 75 to <100 320 3,837 0.92 0.73, 1.16 0.93 0.74, 1.18
 100 to <150 473 6,102 0.84 0.67, 1.05 0.85 0.67, 1.07
 ≥150 294 3,307 0.96 0.75, 1.23 0.96 0.74, 1.23
  P for trend 0.85 0.76
 Per 50 g 0.99 0.93, 1.05 0.98 0.92, 1.05
Processed red meat intake, g/day
 <10 365 4,538 1.00 Referent 1.00 Referent
 10 to <20 375 4,704 0.98 0.83, 1.15 0.97 0.83, 1.14
 20 to <40 497 5,810 1.03 0.88, 1.20 1.02 0.88, 1.19
 ≥40 257 3,216 0.93 0.77, 1.12 0.92 0.76, 1.11
  P for trend 0.65 0.59
 Per 25 g 0.98 0.90, 1.06 0.98 0.90, 1.06
Poultry intake, g/dayd
 <20 321 3,677 1.00 Referent 1.00 Referent
 20 to <40 533 6,379 0.97 0.83, 1.13 0.96 0.82, 1.12
 40 to <80 480 5,955 0.93 0.79, 1.09 0.92 0.78, 1.08
 ≥80 158 2,214 0.82 0.66, 1.02 0.80 0.64, 0.99
  P for trend 0.07 0.05
 Per 50 g 0.95 0.86, 1.05 0.94 0.85, 1.04
Fish intake, g/daye
 <10 279 3,362 1.00 Referent 1.00 Referent
 10 to <20 419 5,133 0.99 0.83, 1.17 0.99 0.84, 1.17
 20 to <30 369 4,427 1.01 0.85, 1.20 1.02 0.85, 1.22
 30 to <40 170 2,144 0.94 0.76, 1.16 0.95 0.76, 1.18
 ≥40 257 3,200 0.95 0.79, 1.16 0.96 0.78, 1.17
  P for trend 0.55 0.59
 Per 25 g 1.00 0.93, 1.06 1.00 0.93, 1.07
Ratio of total red meat to poultry
 Quintile 1 265 3,616 1.00 Referent 1.00 Referent
 Quintile 2 292 3,668 1.06 0.89, 1.28 1.05 0.87, 1.26
 Quintile 3 297 3,521 1.12 0.93, 1.34 1.10 0.92, 1.33
 Quintile 4 291 3,647 1.05 0.87, 1.26 1.03 0.85, 1.24
 Quintile 5 326 3,507 1.20 1.00, 1.44 1.20 0.99, 1.44
  P for trend 0.09 0.12
Ratio of total red meat to poultry and fish
 Quintile 1 282 3,649 1.00 Referent 1.00 Referent
 Quintile 2 295 3,608 0.99 0.83, 1.19 1.00 0.83, 1.20
 Quintile 3 258 3,696 0.84 0.70, 1.02 0.83 0.69, 1.01
 Quintile 4 320 3,617 1.10 0.92, 1.32 1.08 0.90, 1.30
 Quintile 5 328 3,584 1.12 0.93, 1.33 1.11 0.92, 1.33
  P for trend 0.09 0.13
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Abbreviations: CI, confidence interval; OR, odds ratio.

a Model 1 is adjusted for age (in years), family history of colorectal cancer (first-degree relative, yes/no), time period of endoscopy (2-year study period interval), number of reported endoscopies during the study period (1 endoscopy vs. ≥2 endoscopies), endoscopy prior to study period (yes/no), reason for most recent endoscopy (screening vs. symptoms), height, body mass index (weight (kg)/height (m)2) at age 18 years (<18.5, 18.5 to <23, 23 to <25, or ≥25), pack-years of smoking (0, >0 to 10, >10 to 20, >20 to 40, or >40), current physical activity (quintiles), physical activity during 9th–12th grades (quintiles), aspirin use (never, past, or current 1 day/week, 2–3 days/week, 4–5 days/week, or ≥6 days/week), high school energy intake (quintiles), and current cumulative average alcohol intake (quintiles).

b Model 2 is additionally adjusted for adult energy intake and respective exposure variable (e.g., models for total red meat intake during high school were adjusted for cumulative updated average total red meat intake during adulthood).

c Unprocessed red meat was defined as “beef or lamb as a main dish,” “pork as a main dish,” “beef, pork, or lamb as a sandwich or mixed dish,” “hamburger,” or “meatloaf” and processed red meat was defined as “hot dog,” “bacon,” or “processed meats, e.g., salami, bologna, sausage, etc.” on the high school food frequency questionnaire.

d Poultry was defined as “chicken or turkey” or “chicken or turkey as a sandwich or mixed dish” on the high school food frequency questionnaire.

e Fish was defined as “canned tuna,” “dark meat fish,” “breaded fish cakes, pieces, or fish sticks,” or “other fish” on the high school food frequency questionnaire.

The associations shown in Table 2 were also not substantially changed after additional adjustment for intakes during high school of total fat, animal fat, cholesterol, polyunsatured fatty acids (fish intake models only), total protein, or heme iron (by adding each nutrient separately into the multivariable model; data not shown). The inverse association between poultry intake during high school and the risk of colorectal adenoma persisted after adjustment for fruit and vegetable intakes during high school and glycemic index/load. By using factor analysis as described elsewhere (40) and dietary information from the HS-FFQ, we derived a score for a “Western” dietary pattern, which is characterized by high intakes of desserts, snacks, red and processed meats, and refined grains, as well as a score for a “prudent” dietary pattern, which is characterized by high intakes of healthy foods such as vegetables, fruit, and better quality grains. Inclusion of a Western or a prudent dietary pattern score (separately) in the multivariable models did not alter the observed inverse association between poultry intake during high school and colorectal adenomas.

Associations were not substantially changed when analysis was restricted to cases diagnosed at the first endoscopy (OR for total adenoma in the highest vs. lowest category of poultry intake = 0.83, 95% CI: 0.66, 1.04; P for trend = 0.07). Results were also similar when we examined associations of adenomas with quintiles of meat and fish intakes during adolescence (data not shown).

When associations were examined by adenoma subsite, results were similar to those observed for total colorectal adenomas, except that significant inverse associations between poultry intakes were observed only for distal and rectal adenomas (Table 3). Intake of poultry during high school was significantly inversely associated with advanced adenomas but not with nonadvanced adenomas. A high ratio of total red meat to poultry was significantly positively associated with rectal and advanced adenomas. No significant differences in the associations between meat and fish intakes and colorectal adenomas by anatomical location or histological stage were observed, with the exception of poultry intake and proximal versus distal adenomas (P for difference = 0.04).

Table 3.

Association Between Meat and Fish Intakes During High School and Colorectal Adenomas by Location and Stage, Nurses' Health Study II, United States, 1998–2007

Dietary Intakes Proximal Adenomas (n = 714)
 Distal Adenomas (n = 675)
 Rectal Adenomas (n = 249)
 Nonadvanced Adenomas (n = 1,113)
 Advanced Adenomas (n = 305)
Adjusteda OR 95% CI Adjusteda OR 95% CI Adjusteda OR 95% CI Adjusteda OR 95% CI Adjusteda OR 95% CI
Total red meat intake, g/day
 <75 1.00 Referent 1.00 Referent 1.00 Referent 1.00 Referent 1.00 Referent
 75 to <100 1.12 0.84, 1.51 1.21 0.91, 1.62 1.22 0.74, 1.99 1.09 0.83, 1.44 1.39 0.93, 2.07
 100 to <125 1.31 0.98, 1.75 0.97 0.72, 1.31 1.05 0.63, 1.74 1.1 0.84, 1.45 1.24 0.83, 1.87
 125 to <150 1.13 0.83, 1.54 0.98 0.72, 1.34 1.05 0.62, 1.79 0.96 0.72, 1.29 1.1 0.71, 1.69
 150 to <200 1.11 0.82, 1.50 1.00 0.73, 1.36 1.32 0.80, 2.20 1.06 0.80, 1.41 1.04 0.68, 1.61
 ≥200 1.07 0.74, 1.55 0.97 0.67, 1.40 1.19 0.66, 2.17 0.99 0.71, 1.40 1.31 0.81, 2.14
  P for trend 0.94 0.49 0.50 0.77 0.91
 Per 100 g 0.93 0.79, 1.10 0.91 0.77, 1.08 1.03 0.79, 1.34 0.94 0.81, 1.10 0.99 0.79, 1.24
Poultry intake, g/day
 <20 1.00 Referent 1.00 Referent 1.00 Referent 1.00 Referent 1.00 Referent
 20 to <40 0.87 0.69, 1.08 1.06 0.85, 1.32 0.97 0.68, 1.38 0.79 0.65, 0.98 0.94 0.70, 1.26
 40 to <80 0.94 0.75, 1.18 0.88 0.69, 1.12 0.79 0.54, 1.17 0.84 0.68, 1.05 0.77 0.56, 1.06
 ≥80 0.87 0.65, 1.18 0.71 0.51, 0.99 0.51 0.29, 0.90 0.80 0.60, 1.06 0.60 0.38, 0.93
  P for trend 0.80 0.01 0.01 0.37 0.01
 Per 50 g 1.01 0.88, 1.16 0.86 0.74, 0.99 0.77 0.60, 0.99 0.99 0.87, 1.13 0.77 0.63, 0.95
Fish intake, g/day
 <10 1.00 Referent 1.00 Referent 1.00 Referent 1.00 Referent 1.00 Referent
 10 to <20 1.03 0.81, 1.32 0.84 0.66, 1.07 1.17 0.79, 1.73 0.98 0.78, 1.23 1.15 0.83, 1.60
 20 to <30 1.15 0.90, 1.48 0.85 0.66, 1.09 0.96 0.63, 1.48 1.02 0.81, 1.30 1.07 0.76, 1.52
 30 to <40 1.06 0.78, 1.44 0.80 0.58, 1.09 1.12 0.68, 1.84 1.02 0.76, 1.36 1.03 0.67, 1.56
 ≥40 1.05 0.79, 1.40 0.89 0.67, 1.19 0.76 0.46, 1.24 1.08 0.83, 1.41 0.88 0.59, 1.32
  P for trend 0.75 0.62 0.15 0.46 0.30
 Per 25 g 1.00 0.91, 1.11 1.04 0.95, 1.13 0.87 0.72, 1.05 1.06 0.98, 1.15 0.90 0.77, 1.05
Ratio of total red meat to poultry
 Quintile 1 1.00 Referent 1.00 Referent 1.00 Referent 1.00 Referent 1.00 Referent
 Quintile 2 1.18 0.92, 1.53 0.97 0.74, 1.27 1.10 0.69, 1.74 1.02 0.80, 1.29 1.08 0.75, 1.56
 Quintile 3 1.18 0.91, 1.53 1.11 0.85, 1.45 1.47 0.94, 2.28 1.02 0.80, 1.31 1.13 0.78, 1.63
 Quintile 4 1.01 0.78, 1.32 1.02 0.78, 1.34 1.10 0.69, 1.75 0.93 0.72, 1.19 1.10 0.76, 1.58
 Quintile 5 1.17 0.90, 1.53 1.21 0.93, 1.58 1.64 1.05, 2.54 1.19 0.94, 1.52 1.44 1.01, 2.06
  P for trend 0.67 0.14 0.05 0.30 0.07
Ratio of total red meat to poultry and fish
 Quintile 1 1.00 Referent 1.00 Referent 1.00 Referent 1.00 Referent 1.00 Referent
 Quintile 2 0.99 0.77, 1.27 1.03 0.79, 1.34 0.99 0.63, 1.56 0.90 0.71, 1.14 1.23 0.85, 1.79
 Quintile 3 0.70 0.53, 0.91 0.94 0.72, 1.23 0.91 0.57, 1.44 0.68 0.53, 0.88 1.10 0.76, 1.60
 Quintile 4 1.09 0.85, 1.39 0.94 0.72, 1.23 1.49 0.97, 2.27 0.99 0.78, 1.25 1.22 0.84, 1.77
 Quintile 5 0.98 0.75, 1.27 1.22 0.94, 1.59 1.40 0.90, 2.17 0.96 0.75, 1.22 1.60 1.11, 2.31
  P for trend 0.73 0.11 0.07 0.33 0.07
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Abbreviations: CI, confidence interval; OR, odds ratio.

a Multivariable model adjusted for age (in years), family history of colorectal cancer (first-degree relative, yes/no), time period of endoscopy (2-year study period interval), number of reported endoscopies during the study period (1 endoscopy vs. ≥2 endoscopies), endoscopy prior to study period (yes/no), reason for most recent endoscopy (screening vs. symptoms), height, body mass index (weight (kg)/height (m)2) at age 18 years (<18.5, 18.5 to <23, 23 to <25, or ≥25), pack-years of smoking (0, >0 to 10, >10 to 20, >20 to 40, or >40), current physical activity (quintiles), physical activity during 9th–12th grades (quintiles), aspirin use (never, past, or current 1 day/week, 2–3 days/week, 4–5 days/week, or ≥6 days/week), high school energy intake (quintiles), current cumulative average alcohol intake (quintiles), and current total red meat, poultry, and fish intakes.

Substitution of 1 serving per day of major protein sources with 1 serving of total red meat during high school was not significantly associated with risk of total, proximal, or distal adenomas (Figure 1, proximal data not shown). However, substitution of 1 serving per day of poultry or fish for 1 serving per day of total red meat was associated with a 41% lower risk of rectal adenomas (OR = 0.59, 95% CI: 0.37, 0.94) and a 35% lower risk of advanced adenomas (OR = 0.65, 95% CI: 0.45, 0.95), whereas substitution of other protein sources for total red meat was not significantly associated with risk of rectal or advanced adenomas.

Figure 1.

Figure 1.

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Odds ratios (ORs) and 95% confidence intervals (CIs) for risk of adenoma and subtypes of adenoma associated with replacement of 1 serving per day of various protein sources for 1 serving of total red meat during high school in the Nurses' Health Study II, United States, 1998–2007. Multivariable model adjusted for age (in years), family history of colorectal cancer (first-degree relative, yes/no), time period of endoscopy (2-year study period interval), number of reported endoscopies during the study period (1 endoscopy vs. ≥2 endoscopies), reason for most recent endoscopy (screening vs. symptoms), height, body mass index (weight (kg)/height (m)2) at age 18 years (<18.5, 18.5 to <23, 23 to <25, or ≥25), pack-years of smoking (0, 0 to 10, >10 to 20, >20 to 40, or >40), current physical activity (quintiles), physical activity during 9th–12th grades (quintiles), aspirin use (never, past, or current 1 day/week, 2–3 days/week, 4–5 days/week, or ≥6 days/week), high school energy intake (quintiles), and current cumulative average alcohol intake (quintiles).

Among women who answered the HS-FFQ and who had a lower-bowel endoscopy during the study period, higher total red meat intake in adulthood was significantly positively associated with risk of distal and nonadvanced adenomas. Intakes of poultry and fish during adulthood were not significantly associated with the risk of colorectal adenomas (data not shown).

When comparing women with high intakes of total red meat (≥125 g/day), poultry (≥40 g/day), or fish (≥30 g/day) during adolescence and adulthood with women with low intakes (total red meat <125 g/day, poultry <40 g/day, or fish <30 g/day) during adolescence and adulthood, we observed no significant associations with colorectal adenomas. Similarly, no significant interactions were observed with regard to the risk of colorectal adenomas after cross-classifying tertiles of high school and adult meat and fish intakes (data not shown).

DISCUSSION

In this study, total red meat or fish intake during high school was not associated with risk of colorectal adenomas later in life. Intake of poultry during high school was inversely associated with the risk of distal, rectal, and advanced adenomas.

Very few studies have investigated the association between childhood or adolescent diet and the risk of colorectal cancer later in life. In some northern European countries, extreme energy restriction in children and adolescents during World War II was associated with lower colorectal cancer risk in later life (41, 42). It has also been suggested that adolescence may be a time of susceptibility to epigenetic modulations (e.g., as a result of dietary exposures) that may affect colorectal cancer risk later in life (43). In the National Institutes of Health (NIH)–AARP Diet and Health Study (27), a large prospective cohort that used a 37-item FFQ to ascertain dietary intakes at ages 12–13 years, no significant associations between dietary intake of red or processed meat during adolescence and the risk of colon or rectal cancer were observed. However, significantly increased risks of colon and rectal cancers were observed when comparing participants in the highest tertile of red or processed meat intake during adolescence, adulthood, or both with participants in the lowest tertile during both adolescence and adulthood; we could not confirm this finding in an equivalent analysis of colorectal adenoma.

We observed significant inverse associations between higher intake of poultry during high school and the risk of colorectal adenomas later in life, independent of unprocessed and processed red meat intakes and fish intake. There is no well-established plausible biological mechanism to explain this association. It is possible that poultry intake during adolescence is simply a marker of a healthy diet or lifestyle that may track through the course of life. However, after adjustment for a prudent dietary pattern or lifestyle factors such as physical activity, body mass index, or smoking, the significant inverse association between poultry intake during high school and the risk of adenoma persisted. Nevertheless, residual confounding by healthy lifestyle cannot be excluded. We are not aware of any study relating poultry intake during adolescence to the risk of adenoma in later life. Significant inverse associations between poultry intake during adulthood and the risk of colorectal cancer have been observed in several studies (16, 19, 20), although most studies have reported nonsignificant inverse associations (17, 23, 44–46). We observed only slightly decreased odds ratios for distal and rectal adenomas associated with higher fish intake during high school, but intake ranges were low, and dark meat fish (a good source of ω-3 fatty acids), which may inhibit colorectal carcinogenesis (18), was rarely consumed during high school.

We observed no association between total red meat intake during high school and the risk of colorectal adenomas. Because the average total red meat intake during high school was substantially higher than during adulthood in our study, it is possible that we did not observe a positive association because there were few women with very low or no total red meat intake during high school (10th percentile of total red meat intake during high school was 67 g/day).

In our study, dietary intake during adolescence was assessed retrospectively by using the HS-FFQ when study participants were 34–53 years of age. Thus, we had to rely on participants' memories and abilities to correctly estimate their dietary intakes when they attended high school; therefore, potential misclassification is a limitation of our study (47). However, cases diagnosed before they completed the HS-FFQ were excluded, thereby reducing the possibility of recall bias. Furthermore, any misclassification of exposure should be nondifferential, thus biasing the risk estimates toward the null association (47). In the absence of assessments of diet actually made during adolescence, the HS-FFQ is a dietary instrument with reasonable reproducibility and validity (32, 33) for use in prospective studies with long follow-up periods.

Major strengths of this study include the large sample size and the ability to examine subtypes of colorectal adenoma. The detailed and repeated assessment of diet and lifestyle factors allowed for comprehensive adjustment of many potentially confounding factors, including confounding by adult dietary intake.

In conclusion, our findings do not suggest that intake of red meat during adolescence is associated with the risk of colorectal adenoma later in life, but adolescent poultry intake was associated with a lower risk of distal, rectal, and advanced adenomas. Substitution of fish or poultry for red meat during high school may reduce the risk of rectal and advanced adenomas.

ACKNOWLEDGMENTS

Author affiliations: Department of Nutrition, Harvard School of Public Health, Boston, Massachusetts (Katharina Nimptsch, Adam M. Bernstein, Edward Giovannucci, Walter C. Willett, Kana Wu); Molecular Epidemiology Research Group, Max Delbrück Center for Molecular Medicine, Berlin, Germany (Katharina Nimptsch); Department of Epidemiology, Harvard School of Public Health, Boston, Massachusetts (Edward Giovannucci, Walter C. Willett); Channing Division of Network Medicine, Department of Medicine, Brigham and Women's Hospital and Harvard Medical School, Boston, Massachusetts (Edward Giovannucci, Charles S. Fuchs, Walter C. Willett); Department of Medical Oncology, Dana-Farber Cancer Institute, Boston, Massachusetts (Charles S. Fuchs); and the Wellness Institute, Cleveland Clinic, Lyndhurst, Ohio (Adam Bernstein).

The authors acknowledge funding from the American Institute for Cancer Research (investigator-initiated grant to K. W.), the National Cancer Institute (grant R01 CA50385 to W. C. W.), and the Entertainment Industry Foundation's National Colorectal Cancer Research Alliance.

We thank the staff of the Nurses’ Health Study II for their valuable contributions, as well as the cancer registries of the following states for their help: Alabama, Arizona, Arkansas, California, Colorado, Connecticut, Delaware, Florida, Georgia, Idaho, Illinois, Indiana, Iowa, Kentucky, Louisiana, Maine, Maryland, Massachusetts, Michigan, Nebraska, New Hampshire, New Jersey, New York, North Carolina, North Dakota, Ohio, Oklahoma, Oregon, Pennsylvania, Rhode Island, South Carolina, Tennessee, Texas, Virginia, Washington, and Wyoming.

Conflict of interest: none declared.

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