Epidemiology/Health Services/Psychosocial Research ORIGINAL ARTICLE A Prospective Study of Red Meat Consumption and Type 2 Diabetes in Middle-Aged and Elderly Women The Women’s Health Study 1,2 1,2,4 YIQING SONG, MD JULIE E. BURING, SCD suspected as an important and indepen- 1,2,3 1,2 JOANN E. MANSON, MD, DRPH SIMIN LIU, MD, SCD dent contributor to risk of type 2 diabetes. This hypothesis was first generated based on the evidence from ecologic and mi- grant studies (2,3) and subsequently sup- OBJECTIVE — The aim of this study was to prospectively assess the relation between red ported by several cross-sectional and meat intake and incidence of type 2 diabetes. prospective studies of dietary patterns and diabetes (4–6). RESEARCH DESIGN AND METHODS — Over an average of 8.8 years, we evaluated Since the Seventh Day Adventists 37,309 participants in the Women’s Health Study aged Ն45 years who were free of cardiovas- Study first reported a positive association cular disease, cancer, and type 2 diabetes and completed validated semiquantitative food fre- between total meat intake and risk of type quency questionnaires in 1993. 2 diabetes in a population with a large proportion of vegetarians (7), few studies RESULTS — During 326,876 person-years of follow-up, we documented 1,558 incident have specifically assessed this relation be- cases of type 2 diabetes. After adjusting for age, BMI, total energy intake, exercise, alcohol intake, cigarette smoking, and family history of diabetes, we found positive associations between intakes tween meat consumption and incidence of red meat and processed meat and risk of type 2 diabetes. Comparing women in the highest of diabetes. Of note, two recent cohort quintile with those in the lowest quintile, the multivariate-adjusted relative risks (RRs) of type 2 studies in U.S. men and women observed diabetes were 1.28 for red meat (95% CI 1.07–1.53, P Ͻ 0.001 for trend) and 1.23 for processed a significant association between frequent meat intake (1.05–1.45, P ϭ 0.001 for trend). Furthermore, the significantly increased diabetes consumption of processed meat and an risk appeared to be most pronounced for frequent consumption of total processed meat (RR increased risk of type 2 diabetes (8,9). 1.43, 95% CI 1.17–1.75 for Ն5/week vs. Ͻ1/month, P Ͻ 0.001 for trend) and two major However, because of scarce data, it is un- subtypes, which were bacon (1.21, 1.06–1.39 for Ն2/week vs. Ͻ1/week, P ϭ 0.004 for trend) Ն Ͻ ϭ clear whether these observed positive as- and hot dogs (1.28, 1.09–1.50 for 2/week vs. 1/week, P 0.003 for trend). These results sociations are consistent in other cohorts. remained significant after further adjustment for intakes of dietary fiber, magnesium, glycemic Furthermore, it remains uncertain load, and total fat. Intakes of total cholesterol, animal protein, and heme iron were also signifi- cantly associated with a higher risk of type 2 diabetes. whether the adverse association of red meat or processed meat consumption CONCLUSIONS — Our data indicate that higher consumption of total red meat, especially with diabetes risk is mediated through its various processed meats, may increase risk of developing type 2 diabetes in women. high fat content, protein, or some other specific components produced from cer- Diabetes Care 27:2108–2115, 2004 tain cooking or processing practices such as nitrates and nitrites. Therefore, we prospectively investi- he adoption of a “western diet” char- products, snacks, sweets, French fries, gated the associations of red and pro- acterized by high intakes of red and and pizza, is believed to contribute to the cessed meat and various subtypes of each, T processed meat as well as other epidemic of type 2 diabetes in the world and type of major nutrients, with the in- components, including refined grain (1). A diet high in red meat has long been cidence of type 2 diabetes in the Women’s ●●●●●●●●●●●●●●●●●●●●●●●●●●●●●●●●●●●●●●●●●●●●●●●●● Health Study (WHS), comprised of a large cohort of U.S. women. From the 1Division of Preventive Medicine, Department of Medicine, Brigham and Women’s Hospital and Harvard Medical School, Boston, Massachusetts; the 2Department of Epidemiology, Harvard School of Public Health, Boston, Massachusetts; the 3Channing Laboratory, Department of Medicine, Brigham and RESEARCH DESIGN AND Women’s Hospital and Harvard Medical School, Boston, Massachusetts; and the 4Department of Ambulatory METHODS — The WHS is a random- Care and Prevention, Harvard Medical School, Boston, Massachusetts. ized, double-blind, placebo-controlled Address correspondence and reprint requests to Simin Liu, MD, ScD, Division of Preventive Medicine, Brigham and Women’s Hospital, 900 Commonwealth Ave. East, Boston, MA 02215. E-mail: trial designed to evaluate the balance of [email protected]. benefits and risks of low-dose aspirin and Received for publication 4 May 2004 and accepted in revised form 9 June 2004. vitamin E in the primary prevention of Abbreviations: ADA, American Diabetes Association; SFFQ, semiquantitative food frequency question- cardiovascular disease and cancer (10). naire; WHS, Women’s Health Study. We randomized a total of 39,876 female A table elsewhere in this issue shows conventional and Syste`me International (SI) units and conversion Ն factors for many substances. health professionals aged 45 years who © 2004 by the American Diabetes Association. were free of coronary heart disease, 2108 DIABETES CARE, VOLUME 27, NUMBER 9, SEPTEMBER 2004 Song and Associates stroke, and cancer (other than nonmela- Thereafter, all of the participants were ergy intake. In multivariate models, we noma skin cancer). Of them, 98% pro- asked annually whether and when they adjusted for age (continuous), BMI (con- vided detailed information about their had been diagnosed with diabetes since tinuous), total energy intake (quintiles), diet, completing a 131-item semiquanti- completing the previous questionnaire. smoking status (current, past, and never), tative food frequency questionnaire Two complementary approaches have exercise (rarely/never, Ͻ1/week, 1–3/ (SFFQ) in 1993 (10). We excluded indi- been used to confirm self-reported type 2 week, and Ն4/week), alcohol intake viduals with Ͼ70 items left blank in their diabetes in the WHS. First, we attempted (rarely/never, 1–3 drinks/month, 1– 6 SFFQ and with energy intake outside the to contact 473 women with self-reported drinks/week, Ն1 drink/day), and family range of 2,514 kJ (600 kcal) and 14,665 diabetes who provided a blood sample as history of diabetes (yes/no) and then fur- kJ (3,500 kcal), with reported diabetes at part of a nested case-control study of dia- ther adjusted for dietary factors, includ- baseline, and with completed data on betes, to verify the self-reported diagnosis ing intakes of dietary fiber (quintiles), meat consumption, which left 37,309 (15). Using the American Diabetes Asso- glycemic load (quintiles), total fat (quin- women for the analysis. This study has ciation (ADA) diagnostic criteria (16), the tiles), and magnesium (quintiles). Tests of been conducted according to the ethical self-reported diagnosis of diabetes was linear trend across increasing categories guidelines of Brigham and Women’s Hos- confirmed in 406 (91%) of 446 women of intake were conducted by assigning the pital. Written informed consent was ob- who responded via telephone interview medians of intakes in quintiles treated as a tained from all participants. (15). Second, a random sample of 147 continuous variable. A likelihood ratio women with self-reported diabetes was test was used to assess the significance of Assessment of meat intake mailed a supplemental diabetes question- interaction terms. We also did separate For each food, a commonly used unit or naire, also using the ADA criteria to par- analyses for intakes of type of fat, protein, portion size was specified, and each par- allel the telephone interview. Among 136 dietary heme iron, and total iron. All sta- ticipant was asked how often she had con- respondents, 124 (91%) women were tistical analyses were conducted using sumed that amount, on average, over the classified as having type 2 diabetes by the SAS (version 8.0; SAS Institute, Cary, previous year. Nine possible responses supplemental questionnaire. In addition, NC). ranging from “never” to “six or more times 113 of the 124 women gave permission to per day” were recorded. Intake of each contact their primary care physician. RESULTS — At baseline in 1993, the meat item was calculated by multiplying Ninety-seven of the 113 physicians re- differences comparing the highest intake the intake frequency of individual items sponded, of whom 90 provided adequate to the lowest intake among 37,309 in those food categories by their weights, information to apply the ADA criteria. For women were ϳ10-fold in total red meat estimated from the specified portion size. these 90 women, 89 (99%) were con- intake (Table 1). High consumers of red Nutrient intakes were computed by mul- firmed to have type 2 diabetes on the basis meat tended to be current smokers and tiplying the frequency of consumption of of the combined information from the less likely to exercise, use postmeno- each unit of food from the SFFQ by the supplemental questionnaire and physi- pausal hormones, or use supplements of nutrient content of the specified portion cian information. Thus, we believe that multivitamins than those who rarely con- size according to food composition tables self-reported type 2 diabetes is valid in the sumed red meat. Women with higher in- from the Harvard Food Composition Da- WHS. take of red meat also had a higher BMI and tabase (11). Each nutrient was adjusted were more likely to have a history of hy- for total energy using the residual method Data analysis pertension and a family history of diabe- (12).