Red meat intake and risk of type 2 diabetes in a prospective cohort study of United States females and males

Abstract

Background: Studies with methodological advancements are warranted to confirm the relation of red meat consumption to the incidence of type 2 diabetes (T2D).

Objective: We aimed to assess the relationships of intakes of total, processed, and unprocessed red meat to risk of T2D and to estimate the effects of substituting different protein sources for red meats on T2D risk.

Methods: Our study included 216,695 participants (81% females) from the Nurses' Health Study (NHS), NHS II, and Health Professionals Follow-up Study (HPFS). Red meat intakes were assessed with semiquantitative food frequency questionnaires (FFQs) every 2 to 4 y since the study baselines. We used multivariable-adjusted proportional hazards models to estimate the associations between red meats and T2D.

Results: Over 5,483,981 person-years of follow-up, we documented 22,761 T2D cases. Intakes of total, processed, and unprocessed red meat were positively and approximately linearly associated with higher risks of T2D. Comparing the highest to the lowest quintiles, hazard ratios (HR) were 1.62 (95% confidence interval [CI]: 1.53, 1.71) for total red meat, 1.51 (95% CI: 1.44, 1.58) for processed red meat, and 1.40 (95% CI: 1.33, 1.47) for unprocessed red meat. The percentage lower risk of T2D associated with substituting 1 serving/d of nuts and legumes for total red meat was 30% (HR = 0.70, 95% CI: 0.66, 0.74), for processed red meat was 41% (HR = 0.59, 95% CI: 0.55, 0.64), and for unprocessed red meat was 29% (HR = 0.71, 95% CI: 0.67, 0.75); Substituting 1 serving/d of dairy for total, processed, or unprocessed red meat was also associated with significantly lower risk of T2D. The observed associations became stronger after we calibrated dietary intakes to intakes assessed by weighed diet records.

Conclusions: Our study supports current dietary recommendations for limiting consumption of red meat intake and emphasizes the importance of different alternative sources of protein for T2D prevention.

Keywords: calibration; processed red meat; red meat; sources of protein; substitution; type 2 diabetes; unprocessed red meat.

FIGURE 1

Associations between red meat intakes and risk of diabetes in the NHS, NHS II, and HPFS by categories. A, Hazard ratios of T2D comparing intakes of total red meat to the lowest intake category. B, Hazard ratios of T2D comparing intakes of processed red meat to the lowest intake category. C, Hazard ratios of T2D comparing intakes of unprocessed red meat to the lowest intake category. One serving of unprocessed red meat equals 85 g of pork, beef, or lamb; one serving of processed red meat equals 28 g of bacon or 45 g of hot dog, sausage, salami, bologna, or other processed red meats. The hazard ratios and 95% confidence intervals of T2D comparing each intake category with the reference category of <0.20 servings/d were estimated with Cox proportional hazards models stratified jointly by age in months and calendar time in 2-y groups and adjusted for race/ethnicity, smoking status, alcohol intake, physical activity (METs-hours/week), multivitamin use, menopausal status and hormone use (if in NHS or NHS II), family history of T2D, antihypertensive drug use, cholesterol-lowering drug use, baseline history of hypertension, glycemic index, poultry, fish, eggs, total dairy, nuts and legumes, fruits, vegetables, whole grain, and refined grain intakes, and socioeconomic status. Dietary intakes were cumulative averages from the baseline FFQ to the start of each 4-y follow-up interval. Abbreviations: NHS, Nurses’ Health Study; NHS II, Nurses’ Health Study II; HPFS, Health Professionals Follow-up Study

FIGURE 2

Associations between total red meat (A) and unprocessed red meat (B) and risk of diabetes in the NHS, NHS II, and HPFS by categories of intake using different types of dietary assessments. One serving of unprocessed red meat equals 85 g of pork, beef, or lamb; one serving of processed red meat equals 28 g of bacon or 45 g of hot dog, sausage, salami, bologna, or other processed red meats. The hazard ratios and 95% confidence intervals of T2D comparing each intake category with the reference category of <0.20 servings/d were estimated with Cox proportional hazards models stratified jointly by age in months and calendar time in 2-y groups and adjusted for race/ethnicity, smoking status, alcohol intake, physical activity (METs-hours/week), multivitamin use, menopausal status and hormone use (if in NHS or NHS II), family history of T2D, antihypertensive drug use, cholesterol-lowering drug use, baseline history of hypertension, glycemic index, poultry, fish, eggs, total dairy, nuts and legumes, fruits, vegetables, whole grain, and refined grain intakes, and socioeconomic status. Red meat intakes were calculated as 1) intakes assessed only at baseline (Baseline); 2) cumulative averages of intakes assessed over the follow-up (Cumulative average); 3) cumulative averages of intakes assessed over the follow-up but excluding the most recent 3 assessments prior to T2D diagnosis (Cumulative no recent); 4) cumulative averages of the most recent 3 assessments prior to T2D diagnosis (Recent 3); and 5) simply updated intakes over the follow-up (Simple updated). Abbreviations: NHS, Nurses’ Health Study; NHS II, Nurses’ Health Study II; HPFS, Health Professionals Follow-up Study

FIGURE 3

Associations between substituting one serving of other protein sources for red meat intake and risk of T2D in the NHS, NHS II, and HPFS One serving of unprocessed red meat equals 85 g of pork, beef, or lamb; one serving of processed red meat equals 28 g of bacon or 45 g of hot dog, sausage, salami, bologna, or other processed red meats. The effect of substituting 1 serving/d of other protein sources for red meats was estimated by including both intakes as continuous variables in the same multivariable Cox model. The model was stratified jointly by age in months and calendar time in 2-y groups and adjusted for race/ethnicity, smoking status, alcohol intake, physical activity (METs-hours/week), multivitamin use, menopausal status and hormone use (if in NHS or NHS II), family history of T2D, antihypertensive drug use, cholesterol-lowering drug use, baseline history of hypertension, glycemic index, socioeconomic status, and dietary covariates intakes (including poultry, fish, eggs, total dairy, nuts and legumes, fruits, vegetables, whole grain, and refined grain) excluding the foods subject for substitutions. The HRs (and 95% confidence intervals [(CIs)]) were estimated using the difference in the estimated coefficients (and their pooled variances). Abbreviations: NHS, Nurses’ Health Study; NHS II, Nurses’ Health Study II; HPFS, Health Professionals Follow-up Study

FIGURE 4

Associations between every 1 serving/d increase in uncalibrated and calibrated red meat intakes and risk of diabetes in the NHS, NHS II, and HPFS One serving of unprocessed red meat equals 85 g pork, beef, or lamb; one serving of processed red meat equals 28 g bacon or 45 g hot dog, sausage, salami, bologna, or other processed red meats. We regressed red meats assessed by 7DDRs on intake assessed by FFQs using a two-part regression to account for intakes reported as zeros. The first part of the two-part regression employed logistic regression to handle zero and nonzero data, while the second part utilized linear regression to model nonzero intakes. For the dietary covariates, we fitted intakes measured with 7DDRs and FFQs with linear regressions. We calculated the cumulative averaged calibrated intakes and used Cox proportional hazards models to estimate their associations with T2D. The model was stratified jointly by age in months and calendar time in 2-y groups and adjusted for total energy intake, race/ethnicity (white adults, non-white adults), smoking status (never, past, current: 1-14 cigs/d, current: >15-24 cigs/d, current: >24 cigs/d), physical activity (<3, 3-9, 9-18, 18-27, ≥ 27 METs-h/week), multivitamin use, menopausal status and hormone use (if NHS or NHS II), family history of type 2 diabetes, antihypertensive drug use, cholesterol-lowering drug use, history of hypertension, AHEI-2010 excluding meat component, and socioeconomic status. Abbreviations: NHS, Nurses’ Health Study; NHS II, Nurses’ Health Study II; HPFS, Health Professionals Follow-up Study