AJCN. First published ahead of print June 18, 2014 as doi: 10.3945/ajcn.114.084129.

Fried-food consumption and risk of type 2 diabetes and coronary artery disease: a prospective study in 2 cohorts of US women and men1–4 Leah E Cahill, An Pan, Stephanie E Chiuve, Qi Sun, Walter C Willett, Frank B Hu, and Eric B Rimm ABSTRACT Background: Through the processes of oxidation, polymerization, and hydrogenation, the cooking method of frying modifies both foods and their frying medium. However, it remains unknown whether the frequent consumption of fried foods is related to long-term cardiometabolic health. Objective: We examined fried-food consumption and risk of developing incident type 2 diabetes (T2D) or coronary artery disease (CAD). Design: Fried-food consumption was assessed by using a questionnaire in 70,842 women from the Nurses’ Health Study (1984–2010) and 40,789 men from the Health Professionals Follow-Up Study (1986–2010) who were free of diabetes, cardiovascular disease, and cancer at baseline. Time-dependent Cox proportional hazards models were used to estimate RRs and 95% CIs for T2D and CAD adjusted for demographic, diet, lifestyle, and other cardiometabolic risk factors. Results were pooled by using an inverse variance–weighted random-effects meta-analysis. Results: We documented 10,323 incident T2D cases and 5778 incident CAD cases. Multivariate-adjusted RRs (95% CIs) for individuals who consumed fried foods ,1, 1–3, 4–6, or $7 times/wk were 1.00 (reference), 1.15 (0.97, 1.35), 1.39 (1.30, 1.49), and 1.55 (1.32, 1.83), respectively, for T2D and 1.00 (reference), 1.06 (0.98, 1.15), 1.23 (1.14, 1.33), and 1.21 (1.06, 1.39), respectively, for CAD. Associations were largely attenuated when we further controlled for biennially updated hypertension, hypercholesterolemia, and body mass index. Conclusions: Frequent fried-food consumption was significantly associated with risk of incident T2D and moderately with incident CAD, and these associations were largely mediated by body weight and comorbid hypertension and hypercholesterolemia. Am J Clin Nutr doi: 10.3945/ajcn.114.084129.

INTRODUCTION

Frying is a common cooking method in Western countries, especially outside of the home where French fries and friedchicken products make up a substantial percentage of the items sold at fast-food restaurants. Through the processes of oxidation, polymerization, and hydrogenation, frying modifies both the composition of foods and their frying medium. With repeated use, oils deteriorate, which leads to a change in the fatty acid composition and absorption of other oil-degradation products into fried foods (1, 2). If proven to be detrimental to health, fried-food consumption could cause a substantial health burden because 25– 36% of North American adults patronize fast-food restaurants

daily (3, 4). However, if foods are fried with previously unused polyunsaturated and monounsaturated oils, recent evidence has suggested that there may be a benefit from the oils’ n26 and n23 fatty acids if they remain intact after frying (5). Therefore, making dietary recommendations for an appropriate frequency of fried-food consumption is currently complex. Despite substantial research into the relation between diet and major chronic diseases, the influence of fried-food consumption on long-term cardiometabolic health is unclear. In cross-sectional studies, fried-food consumption has been positively associated with several cardiometabolic risk factors including hypertension (6), low serum HDL cholesterol (7), and obesity (7, 8). In prospective studies, the Western-style dietary pattern includes fried foods as a major component and is generally positively associated with increased risk of type 2 diabetes (T2D)5 (9); however, to our knowledge, no prospective research has specifically quantified the association between fried-food consumption and T2D. One prospective cohort study and 2 case-control studies have reported inconsistent results of the association between fried-food consumption and risk of coronary artery disease (CAD) (10–12). Therefore, we aimed to examine prospectively whether the frequency of fried-food consumption (both at home and away from home) is associated with risk of incident T2D or CAD. 1 From the Departments of Nutrition (LEC, QS, WCW, FBH, and EBR) and Epidemiology (WCW, FBH, and EBR), Harvard School of Public Health, Boston, MA; the Channing Division of Network Medicine (QS, WCW, FBH, and EBR) and Division of Preventive Medicine (SEC), Department of Medicine, Brigham and Women’s Hospital and Harvard Medical School, Boston, MA; and the Saw Swee Hock School of Public Health (AP) and Yong Loo Lin School of Medicine (AP), National University of Singapore and National University Health System, Singapore. 2 LEC and AP contributed equally to the article. 3 Supported by the NIH (grants P01CA087969, UM1CA167552, RO1HL35464, RO1HL034594, U19CA055075, R01DK058845, P30DK046200, RO1HL60712, and U54CA155626) and a Canadian Institutes of Health Research Postdoctoral Fellowship (to LEC). 4 Address correspondence to LE Cahill, Department of Nutrition, Harvard School of Public Health, 655 Huntington Avenue, Boston, MA 02115. E-mail: [email protected]; or A Pan, Saw Swee Hock School of Public Health, National University of Singapore, 16 Medical Drive, Singapore 117597. E-mail: [email protected]. 5 Abbreviations used: AHEI, Alternative Healthy Eating Index; CAD, coronary artery disease; FFQ, food-frequency questionnaire; HPFS, Health Professionals Follow-Up Study; MI, myocardial infarction; NHS, Nurses’ Health Study; T2D, type 2 diabetes. Received January 17, 2014. Accepted for publication May 8, 2014. doi: 10.3945/ajcn.114.084129.

Am J Clin Nutr doi: 10.3945/ajcn.114.084129. Printed in USA. Ó 2014 American Society for Nutrition

Copyright (C) 2014 by the American Society for Nutrition

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SUBJECTS AND METHODS

Study populations The Nurses’ Health Study (NHS) is a prospective cohort of 121,700 female registered nurses aged 30–55 y at baseline in 1976. The Health Professionals Follow-Up Study (HPFS) is a prospective study of 51,529 male health professionals aged 40– 75 y at enrollment in 1986. Participants in both studies have been followed through mailed biennial questionnaires that ascertained medical histories, lifestyles, and health-related behaviors as previously described (13). More than 95% of participants were of white European descent. Study protocols were approved by the institutional review boards of the Brigham and Women’s Hospital and the Harvard School of Public Health. In the current analysis, we used the years when fried-food consumption was first assessed in the cohorts as the baseline (1984 for NHS: n = 97,476; 1986 for HPFS n = 51,529). Participants were excluded from the current analysis at baseline if they had self-reported cancer (except nonmelanoma skin cancer), diabetes, cardiovascular disease (angina, stroke, CAD, or coronary artery bypass graft surgery) (n = 9890 women and 6554 men), reported unusual energy intakes (,800 or .4200 kcal/d for men and ,500 or .3500 kcal/d for women) or did not answer the food-frequency questionnaire (FFQ) or questions of fried-food consumption (n = 16,026 women, and 1948 men) and subjects who only replied to the baseline questionnaire or had an unknown mortality or disease status during follow-up (n = 718 women and 2238 men). After exclusions, data from 70,842 women and 40,789 men were available for the analysis. The retention percentage of the 2 cohorts is .90% of potential person-times. Fried-food consumption and other dietary assessment On the FFQ, participants were asked “how often do you eat fried food away from home (e.g. French fries, fried chicken, fried fish)?” and “how often do you eat food that is fried at home (Exclude the use of “Pam”-type spray)?” Both questions had 4 possible responses as follows: ,1, 1–3, 4–6 or $7 times/wk. Questions were assessed in the NHS in 1984, 1986, and every 4 y thereafter and every 4 y starting from 1986 in the HPFS. Fried-food consumption at home and fried-food consumption away from home were analyzed separately and also added together to examine total fried-food consumption. To assess the overall diet quality, a diet score for each participant was calculated on the basis of the previously described 2010 Alternative Healthy Eating Index (AHEI) (14), which was designed to target food choices that have been associated with reduced chronic disease risk. Outcome assessment Outcomes for the current analysis were incident T2D and CAD [defined as nonfatal myocardial infarction (MI) or fatal CAD]. On each biennial questionnaire, participants were asked to indicate whether they had physician-diagnosed T2D or MI in the previous 2 y. For newly diagnosed T2D, we sent out a supplementary questionnaire to collect information regarding symptoms, diagnostic tests, and hypoglycemic therapy. T2D was confirmed on the basis of National Diabetes Data Group diagnostic criteria (15) before 1997 and American Diabetes Association criteria (16) after 1997

by using information from the supplementary questionnaire. Only confirmed cases were included in the analysis. The validity of the supplementary questionnaire for diabetes diagnosis has been documented previously in both the HPFS (17) and NHS (18). For newly reported MI, medical records and autopsy reports were examined for confirmation by study physicians blinded to the participant’s exposure status. Nonfatal MI was defined by WHO criteria, which require clinical symptoms and either diagnostic changes on electrocardiogram or elevated cardiac enzymes (19). Deaths were identified from state vital records and the National Death Index or reported by the participant’s next of kin or the postal system. Fatal CAD was confirmed by hospital records or autopsy. Statistical analysis We calculated each individual’s person-years from the date of return of the baseline questionnaire to the date of diagnosis of T2D or CAD, last returned questionnaire, death, or the end of follow-up (30 June 2010 for the NHS and 31 January 2010 for the HPFS), whichever came first. To examine associations between fried-food consumption and cardiometabolic diseases, we used time-dependent Cox proportional hazards models conditioned on age and follow-up cycle to estimate RRs and 95% CIs for both cohorts individually and then pooled together with the use of an inverse-variance–weighted meta-analysis by a randomeffects model, which allowed for between-study heterogeneity (20). In multivariate models, we adjusted for the following potential risk factors of cardiometabolic diseases: age (continuous), white (yes or no), family history of diabetes (yes or no), smoking status [never, past, or current (1–14, 15–24, or $25 cigarettes/d)], alcohol intake (0, 0.1–4.9, 5.0–14.9, or $15.0 g/d in women; 0, 0.1–4.9, 5.0–29.9, or $30.0 g/d in men), physical activity (,3.0, 3.0–8.9, 9.0–17.9, 18.0–26.9, or $27.0 metabolic equivalent task hours per week (21, 22), total energy intake (quintiles), and diet quality as represented by the AHEI (quintiles). Both total polyunsaturated fats and trans fats were components of the AHEI-2010. In sensitivity analyses, we further adjusted for specific types of fat such as trans fat and polyunsaturated fat as well as versions of the AHEI that were derived without trans and polyunsaturated fats. In women, we also adjusted for postmenopausal status and menopausal hormone use [premenopausal or postmenopausal (never, past, or current hormone use)]. We further adjusted for biennially updated hypertension, hypercholesterolemia, and BMI (in kg/m2) ,23.0, 23.0–24.9, 25.0–29.9, 30.0–34.9, or $35.0) to assess whether risks for T2D or CAD could be mediated by these comorbidities. Most nondietary variables were updated every 2 y in the analysis, and dietary variables were updated every 4 y. We stopped updating dietary variables, including fried-food consumption, when a participant reported a diagnosis of hypertension, hypercholesterolemia, or cancer (and also diabetes for the CAD analysis) because these conditions might lead to changes in diet (23). We also conducted a sensitivity analysis of continuing to update dietary variables after the diagnosis of these comorbidities alongside adjustment for the comorbidity. We conducted analyses stratified by cardiometabolic risk factors including BMI, AHEI, hypertension, hypercholesterolemia, and dietary factors (including red meat, fish, chicken, and

FRIED FOOD, DIABETES, AND CORONARY HEART DISEASE

potato consumption) to determine whether any interactions existed between risk factors and fried-food consumption on risk of T2D or CAD. The likelihood ratio test was used to test for interactions of cross-product terms. We tested for proportional hazards assumptions and examined differences over time by dividing the study into 2 time periods to incorporate knowledge development regarding trans fats (23). Analyses stratified by the type of fat used for frying at home were also conducted. Data were analyzed with SAS software (version 9.2; SAS Institute). We considered 2-tailed P values #0.05 to be statistically significant. RESULTS

In the NHS, 14.0% and 3.5% of women reported fried-food consumption 4–6 and $7 times/wk, respectively (Table 1). Corresponding proportions in men were 22.6% and 7.4%. In both cohorts, frequent fried-food consumption was related to younger age, lower physical activity, higher BMI, and a higher prevalence of smoking. Participants with a higher frequency of fried-food consumption also had a lower diet quality as measured by the AHEI. Specific to food items, participants with a higher frequency of fried-food consumption consumed more red meat, potatoes, and sugar-sweetened beverages and less fruit, vegetables, whole grains, fish, and alcohol. The total energy from trans fat was higher with the greater frequency of friedfood consumption. We showed that participants who frequently ate fried food at home were also more likely to consume fried food away from home. However, people who frequently ate fried food away from home ($4 times/wk) were younger, less likely to be married, and drank more sugar-sweetened beverages than did subjects who frequently ate fried food at home ($4 times/wk) (see Supplemental Table 1 under “Supplemental data” in the online issue). During follow-up, we documented 10,323 incident T2D cases (6974 women and 3349 men). In the multivariate-adjusted model, compared with participants who consumed fried foods ,1 time/wk, individuals who consumed fried foods 1–3, 4–6, or $7 times/wk had significantly higher risk of T2D; pooled RRs (95% CIs) were 1.15 (0.97, 1.35), 1.39 (1.30, 1.49), and 1.55 (1.32, 1.83), respectively (Table 2). The association was largely attenuated but remained significant after additional adjustment for biennially updated hypertension, hypercholesterolemia, and BMI with pooled RRs (95% CIs) of 1.06 (0.97, 1.16), 1.13 (1.07, 1.20), and 1.19 (1.00, 1.40), respectively. During follow-up, we documented 5778 incident CAD cases (2687 women and 3091 men). In comparison with participants who consumed fried foods ,1 time/wk, pooled multivariateadjusted RRs (95% CIs) for risk of CAD were 1.06 (0.98, 1.15), 1.23 (1.14, 1.33), and 1.21 (1.06, 1.39), for individuals who consumed fried foods 1–3, 4–6, and $7 times/wk, respectively (Table 3). The association was mostly attenuated with pooled RRs (95% CIs) of 1.03 (0.97, 1.09), 1.13 (1.04, 1.22), and 1.08 (0.95, 1.24), respectively, after further adjustment for biennially updated hypertension, hypercholesterolemia, and BMI. When CAD analyses were conducted for fatal and nonfatal CAD separately from each other (data not shown), results were similar to what we reported for total CAD. The association with T2D was generally stronger for eating fried food away from home [RR: 1.81 (95% CI: 1.58, 2.08) for comparison of $4 times/ wk with ,1 time/wk] than eating fried

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food at home (corresponding RR: 1.26; 95% CI: 1.09, 1.47) in the multivariate model without hypertension, hypercholesterolemia, and BMI (Table 2). We also showed that eating fried food away from home was more related to CAD than eating fried food at home in women (Table 3) but not men. Results for both T2D and CAD were essentially unchanged when we adjusted for specific types of fat such as trans fat and polyunsaturated fat or for other AHEI variables derived differently in regards to these specific types of fat (data not shown). Results remained unchanged in the sensitivity analysis of continuing to update dietary variables after the diagnosis of a potential intermediate health condition (data not shown). For both T2D and CAD, we generally did not find significant interactions between fried-food consumption and BMI, hypertension, hypercholesterolemia, dietary quality, or specific food items (red meat, fish, chicken, or potato), or whether cases occurred before or after 1998 (see Supplementary Tables 2 and 3 under “Supplemental data” in the online issue). Neither stratified analyses by these factors or by type of frying oil provided additional information on associations between fried-food consumption and cardiometabolic diseases (data not shown). DISCUSSION

In 2 large, prospective cohorts, we observed that frequent fried-food consumption was significantly associated with risk of incident T2D and CAD. These associations remained significant after extensive adjustment for demographic, diet, and lifestyle factors. To the best of our knowledge, this is the first prospective study to examine the relation between the frequency of fried-food consumption and risk of T2D. Previous studies have reported that some of the major food items commonly used for frying, such as potatoes and red meat, are positively associated with increased risk of T2D (24–29). However, our results were not substantially altered with adjustment for the overall diet quality and specific food items, which suggested that the association was independent of food items used for frying. The positive association between fried-food consumption and T2D has been supported by findings from other longitudinal studies that investigated the association between fast- or restaurant-food consumption and T2D risk, including the Black Women’s Health Study (30), the Singapore Chinese Health Study (31), and the Coronary Artery Risk Development in Young Adults study (32). We showed a stronger association with risk of T2D when eating fried food away from home than eating at home, which may have several explanations. First, oils deteriorate during frying, especially when the oils are reused, which is a practice that may be more common away from home than at home. Second, portion sizes are often larger (33) and sodium contents higher (34) in restaurant meals than in meals eaten at home. Furthermore, specific food choices might differ at home compared with in a restaurant; eg, our participants who frequently ate fried foods away from home had higher sugar-sweetened–beverage consumption than did those who did not (data not shown). However, the associations remained after adjustment for diet quality, which included caloric intake, sodium intake, and sugar-sweetened–beverage consumption. In the current analysis, fried-food consumption was moderately associated with incident CAD. Recently, the Spanish cohort of the European Prospective Investigation into Cancer and Nutrition

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TABLE 1 Baseline characteristics of participants according to the frequency of fried-food consumption in the NHS and the HPFS1 Frequency of fried-food consumption Characteristic NHS (1984) n Age (y) BMI (kg/m2) Physical activity (MET-h/wk) Race (white) (%) Marital status (married) (%) Current smoker (%) Hypertension (%) High cholesterol (%) Family history of diabetes (%) Parental MI before age 60 y (%) Premenopausal (%) Dietary intake Total energy (kcal/d) Alcohol (g/d) AHEI score Fruit (serving/d) Vegetables (serving/d) Whole grain (g/d) Nuts (serving/d) Potato (servings/d) Dairy products (servings/d) SSB (serving/d) Coffee (cups/d) Red meat (servings/d) Fish (servings/d) Poultry (servings/d) PS ratio trans Fat (% of energy) HPFS (1986) n Age (y) BMI (kg/m2) Physical activity (MET-h/wk) Race (white) Marital status (married) Current smoker Hypertension High cholesterol Family history of diabetes Parental MI before age 60 y Dietary intake Total energy (kcal/d) Alcohol (g/d) AHEI score Fruit (servings/d) Vegetables (servings/d) Whole grain (g/d) Nuts (servings/d) Potato (servings/d) Dairy products (servings/d) SSB (servings/d) Coffee (cups/d) Red meat (servings/d) Fish (servings/d) Poultry (servings/d) PS ratio trans Fat (% of energy)

,1 time/wk

1–3 times/wk

4–6 times/wk

$7 times/wk

35,594 50.8 6 7.12 24.6 6 4.4 16.0 6 23.0 98.2 87.7 23.0 20.3 8.2 27.6 19.2 48.9

22,857 49.9 6 7.1 24.9 6 4.6 12.8 6 19.1 97.6 88.5 25.1 19.7 7.0 29.1 19.1 53.5

9910 48.4 6 7.0 25.5 6 5.1 11.5 6 15.8 97.4 87.3 25.5 19.0 6.3 28.9 18.8 61.2

2481 48.5 6 6.8 26.1 6 5.6 10.2 6 18.3 96.3 85.6 25.9 21.3 7.1 30.9 19.7 60.7

1618 7.2 50.8 2.3 3.2 16.1 0.1 0.4 2.0 0.7 2.4 0.9 0.3 0.3 0.5 1.7

6 6 6 6 6 6 6 6 6 6 6 6 6 6 6 6

494 11.2 10.8 1.4 1.7 14.5 0.2 0.3 1.3 1.0 1.8 0.6 0.3 0.2 0.2 0.6

15,232 54.3 6 9.5 25.2 6 3.1 24.3 6 32.4 95.3 91.2 7.8 20.0 11.4 18.8 12.2 1839 11.1 56.8 2.7 3.3 26.5 0.2 0.4 1.8 0.6 1.8 0.8 0.4 0.4 0.6 1.1

6 6 6 6 6 6 6 6 6 6 6 6 6 6 6 6

564 14.8 11.3 1.7 1.8 22.7 0.4 0.3 1.3 1.0 1.7 0.7 0.3 0.3 0.2 0.5

1809 7.0 45.5 2.0 2.9 12.5 0.1 0.6 2.0 0.8 2.5 1.2 0.2 0.3 0.6 2.1

6 6 6 6 6 6 6 6 6 6 6 6 6 6 6 6

513 11.5 9.8 1.3 1.5 11.4 0.2 0.4 1.3 1.1 1.9 0.7 0.2 0.2 0.2 0.6

13,317 52.8 6 9.4 25.5 6 3.3 20.5 6 27.8 95.2 90.7 9.8 19.0 10.0 18.4 11.8 1980 11.7 51.7 2.3 3.0 20.6 0.2 0.6 2.0 0.8 1.9 1.2 0.3 0.3 0.6 1.3

6 6 6 6 6 6 6 6 6 6 6 6 6 6 6 6

591 15.6 10.8 1.5 1.6 17.8 0.4 0.4 1.4 1.0 1.8 0.7 0.3 0.2 0.2 0.5

1961 6.5 42.9 1.9 2.8 10.6 0.1 0.7 2.0 1.0 2.5 1.5 0.2 0.3 0.6 2.2

6 6 6 6 6 6 6 6 6 6 6 6 6 6 6 6

540 11.1 9.2 1.2 1.5 9.4 0.2 0.4 1.3 1.1 2.0 0.7 0.2 0.2 0.2 0.6

9218 51.4 6 9.2 25.8 6 3.4 19.6 6 28.7 94.9 91.4 10.5 18.4 9.3 19.4 11.8 2126 11.4 48.8 2.1 2.8 17.3 0.3 0.7 2.0 0.9 2.0 1.4 0.3 0.3 0.5 1.4

6 6 6 6 6 6 6 6 6 6 6 6 6 6 6 6

609 15.3 10.3 1.4 1.5 14.7 0.4 0.4 1.4 1.0 1.9 0.8 0.2 0.3 0.2 0.5

2122 5.9 40.9 1.8 2.8 9.3 0.1 0.8 2.0 1.1 2.7 1.7 0.2 0.3 0.5 2.3

6 6 6 6 6 6 6 6 6 6 6 6 6 6 6 6

581 11.0 9.1 1.3 1.5 8.6 0.2 0.5 1.4 1.3 2.1 0.8 0.2 0.3 0.2 0.6

3022 50.9 6 9.0 25.8 6 3.3 16.9 6 27.2 94.3 90.4 14.1 16.7 8.0 18.9 11.9 2356 11.5 45.1 1.8 2.8 14.0 0.3 0.9 2.1 1.0 2.2 1.9 0.3 0.3 0.51 1.6

6 6 6 6 6 6 6 6 6 6 6 6 6 6 6 6

643 16.4 9.9 1.3 1.6 11.9 0.4 0.5 1.5 1.1 1.9 0.9 0.2 0.3 0.2 0.5

1 AHEI, Alternative Healthy Eating Index; HPFS, Health Professionals Follow-Up Study; MET-h, metabolic equivalent task hours; MI, myocardial infarction; NHS, Nurses’ Health Study; PS, polyunsaturated fat:saturated fat; SSB, sugar-sweetened beverage. 2 Mean 6 SD (all such values).

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FRIED FOOD, DIABETES, AND CORONARY HEART DISEASE TABLE 2 RRs (95% CIs) for type 2 diabetes in the NHS and the HPFS according to the frequency of fried-food consumption1 Frequency of fried-food consumption

NHS (1984–2010) Total fried food Cases/person-years Age-adjusted model Model 1 Model 2 Model 3 Model 4 Fried food at home Cases/person-years Age-adjusted model Model 1 Model 2 Model 3 Model 4 Fried food away from home Cases/person-years Age-adjusted model Model 1 Model 2 Model 3 Model 4 HPFS (1986–2010) Total fried food Cases/person-years Age-adjusted model Model 1 Model 2 Model 3 Model 4 Fried food at home Cases/person-years Age-adjusted model Model 1 Model 2 Model 3 Model 4 Fried food away from home Cases/person-years Age-adjusted model Model 1 Model 2 Model 3 Model 4 Pooled results Total fried food Age-adjusted model Model 1 Model 2 Model 3 Model 4 Fried food at home Age-adjusted model Model 1 Model 2 Model 3 Model 4 Fried food away from home Age-adjusted model

,1 time/wk

1–3 times/wk

4–6 times/wk

$7 times/wk

P-trend

3364/910,839 1.00 1.00 1.00 1.00 1.00

2336/522,931 1.21 (1.15, 1.27) 1.14 (1.08, 1.20) 1.06 (1.00, 1.12) 1.05 (1.00, 1.11) 1.02 (0.96, 1.08)

1027/169,336 1.76 (1.64, 1.89) 1.55 (1.44, 1.66) 1.35 (1.26, 1.45) 1.22 (1.14, 1.32) 1.11 (1.04, 1.20)

247/34,199 2.12 (1.87, 2.42) 1.70 (1.50, 1.94) 1.43 (1.25, 1.64) 1.23 (1.08, 1.41) 1.09 (0.96, 1.25)

— ,0.001 ,0.001 ,0.001 ,0.001 0.004

4033/1,021,194 1.00 1.00 1.00 1.00 1.00

2531/549,827 1.16 (1.10, 1.22) 1.10 (1.05, 1.16) 1.01 (0.96, 1.06) 1.00 (0.95, 1.05) 0.99 (0.94, 1.04)

410/66,283 1.66 (1.49, 1.83) 1.40 (1.26, 1.55) 1.18 (1.06, 1.31) 1.06 (0.95, 1.17) 1.01 (0.91, 1.12)

— ,0.001 ,0.001 0.009 0.36 0.98

5313/1,371,685 1.00 1.00 1.00 1.00 1.00

1563/25,4850 1.72 (1.62, 1.82) 1.54 (1.45, 1.63) 1.41 (1.33, 1.49) 1.28 (1.21, 1.36) 1.15 (1.08, 1.22)

98/10,769 2.64 (2.16, 3.23) 2.22 (1.82, 2.71) 1.98 (1.62, 2.42) 1.69 (1.38, 2.07) 1.45 (1.19, 1.78)

— ,0.001 ,0.001 ,0.001 ,0.001 ,0.001

1253/372,858 1.00 1.00 1.00 1.00 1.00

1092/261,460 1.30 (1.20, 1.41) 1.28 (1.18, 1.38) 1.25 (1.15, 1.36) 1.17 (1.08, 1.28) 1.12 (1.03, 1.21)

1830/501,598 1.00 1.00 1.00 1.00 1.00

1289/291,410 1.25 (1.16, 1.34) 1.22 (1.14, 1.31) 1.18 (1.10, 1.27) 1.12 (1.04, 1.20) 1.07 (0.99, 1.15)

230/42,682 1.54 (1.34, 1.77) 1.46 (1.27, 1.67) 1.38 (1.19, 1.59) 1.29 (1.12, 1.48) 1.17 (1.02, 1.35)

— ,0.001 ,0.001 ,0.001 ,0.001 0.02

1932/536,520 1.00 1.00 1.00 1.00 1.00

1207/263,463 1.39 (1.30, 1.50) 1.35 (1.26, 1.45) 1.32 (1.22, 1.42) 1.19 (1.10, 1.28) 1.11 (1.03, 1.20)

210/35,707 1.93 (1.67, 2.23) 1.78 (1.54, 2.06) 1.71 (1.48, 1.98) 1.47 (1.27, 1.70) 1.33 (1.15, 1.54)

— ,0.001 ,0.001 ,0.001 ,0.001 ,0.001

1.00 1.00 1.00 1.00 1.00

1.25 1.20 1.15 1.11 1.06

(1.16, (1.08, (0.97, (0.99, (0.97,

1.34) 1.34) 1.35) 1.23) 1.16)

1.00 1.00 1.00 1.00 1.00

1.20 1.16 1.09 1.05 1.02

(1.11, (1.05, (0.93, (0.95, (0.94,

1.29) 1.28) 1.27) 1.17) 1.10)

1.00

1.55 (1.26, 1.90)

751/155,888 1.57 (1.43, 1.72) 1.49 (1.36, 1.64) 1.45 (1.32, 1.59) 1.28 (1.16, 1.41) 1.16 (1.06, 1.28)

1.67 1.53 1.39 1.24 1.13

(1.49, (1.44, (1.30, (1.17, (1.07,

253/45,484 1.88 (1.64, 2.15) 1.76 (1.53, 2.02) 1.69 (1.47, 1.95) 1.46 (1.27, 1.69) 1.29 (1.12, 1.49)

1.87) 1.62) 1.49) 1.32) 1.20)

2.00 1.73 1.55 1.34 1.19

(1.77, (1.57, (1.32, (1.13, (1.00,

2.26) 1.90) 1.83) 1.59) 1.40)

— ,0.001 ,0.001 ,0.001 ,0.001 ,0.001

,0.001 ,0.001 ,0.001 ,0.001 ,0.001

1.75) 1.54) 1.47) 1.40) 1.25)

,0.001 ,0.001 0.03 0.17 0.37

2.24 (1.65, 3.04)

,0.001

1.61 1.42 1.26 1.16 1.08

(1.49, (1.31, (1.09, (0.96, (0.93,

(Continued)

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CAHILL ET AL

TABLE 2 (Continued ) Frequency of fried-food consumption ,1 time/wk Model Model Model Model

1 2 3 4

1.00 1.00 1.00 1.00

1–3 times/wk 1.44 1.37 1.24 1.13

(1.27, (1.28, (1.15, (1.08,

1.64) 1.46) 1.33) 1.19)

$7 times/wk

4–6 times/wk 1.97 1.81 1.55 1.37

(1.59, (1.58, (1.36, (1.22,

2.44) 2.08) 1.76) 1.54)

P-trend ,0.001 ,0.001 ,0.001 ,0.001

1 Time-dependent Cox proportional hazards models conditioned on age and follow-up cycle were used for both cohorts individually and then pooled together in an inverse-variance–weighted meta-analysis by using a random-effects model. Model 1 was adjusted for age (y), race (white or nonwhite), family history of diabetes (yes or no), smoking status [never, past, current [1–14, 15–24, or $25 cigarettes/d)], alcohol intake (0, 0.1–4.9, 5.0–14.9, or $15.0 g/d in women; 0, 0.1–4.9, 5.0–29.9, or $30.0 g/d in men), physical activity (,3.0, 3.0–8.9, 9.0–17.9, 18.0–26.9, $27.0 metabolic equivalent task hours per week), postmenopausal status, and menopausal hormone use [premenopausal or postmenopausal (never, past, or current hormone use); in women only]. Model 2 was adjusted as for model 1 and for total energy intake and the Alternative Healthy Eating Index (quintiles). Model 3 was adjusted as for model 2 and for hypertension and hypercholesterolemia. Model 4 was adjusted as for model 3 and for BMI (in kg/m2; ,23.0, 23.0–24.9, 25.0–29.9, 30.0–34.9, and $35.0). HPFS, Health Professionals Follow-Up Study; NHS, Nurses’ Health Study.

reported that fried-food consumption was not associated with CAD in 40,757 adults during 8–12 y follow-up; the authors suggested that this was because oils used for frying in Spain are mainly olive oil and sunflower oil (11). In a case-control study from Costa Rica, where frying food is a daily practice, Kabagambe et al (10) reported no association between the consumption of fried foods and risk of nonfatal acute MI, which was potentially attributable to the absence of a large reference group of individuals who did not fry their foods regularly. The results of the current analysis are consistent with the INTERHEART study (5761 nonfatal MI cases and 10,646 controls from 52 countries), which observed an OR of 1.13 (95% CI: 1.02, 1.25) for highest compared with lowest quartiles of fried-food intake after multivariate adjustment (12). In our analyses, relations of fried-food consumption with risks of T2D and CAD were substantially attenuated with adjustment for BMI, hypertension, and hypercholesterolemia. Several studies have reported that fried-food consumption is associated with weight gain, including a combined study of the NHS and HPFS (35). Multiple cross-sectional studies have also linked the consumption of fried foods to an increased likelihood of cardiometabolic risk factors such as body weight and obesity (8), hypertension (6), and low serum HDL cholesterol (7). Although the process of frying food is complex and not well understood, frying is known to alter the quality and energy density of food (2) while also often improving the palatability of food through changes to texture and color (such as making the food crunchy, crisp, and golden brown). Through polymerization, oxidation, and hydrogenation, frying modifies both foods and frying mediums, which leads to an increase in the absorption of oil-degradation products by foods being fried and also a loss of unsaturated fatty acids such as linoleic and linolenic acids and an increase in corresponding trans fatty acids (36). It has been well documented that small changes in the proportion of essential fatty acids in the diet can have important health impacts (37). The amount that frying adulterates fats depends on the frying technique (deep or pan frying), extent of oil degradation, type and composition of the food (38), and type of oil used (39). For example, olive oil is less prone to oxidation than other oils are (39), and has been reported to impart cardiometabolic health benefits when used for frying (5). However, in general, frying increases amounts of cholesterol oxidation products (40) and

reduces the activity of paraoxonase (41), which is an enzyme that inhibits the oxidation of LDL cholesterol. The consumption of foods fried with reused oils has been associated with a higher prevalence of arterial hypertension (6) and impaired arterial endothelial function (42) compared with when the same oil was previously unused. There were several limitations in our analysis. First, we do not know what specific fried foods our participants ate. We were also limited in knowing the duration, temperature, and method (deep or pan) used for frying and how often oils had been reused. Certain less obviously fried foods, such as doughnuts, may not have been considered fried foods by some participants. Furthermore, it is possible that persons with hypertension, high cholesterol, or obesity may have been less likely to consume or report the consumption of fried foods. Similarly, energy intakes reported by the FFQ may have been underestimated (43), which would have affected the adjustment for energy in our analysis. Our study had several strengths, including a large sample size and the repeated comprehensive assessment of many lifestyle characteristics that were gathered prospectively with a long duration of follow-up. As such, we were able to assess the confounding effects and modification of the association for fried-food consumption by other dietary components or lifestyle factors. Nevertheless, it was still possible that we were unable to account for all unhealthy lifestyle characteristics associated with greater fried-food consumption. The time period of our study (1984–2010) fit well with changes to policy and subsequent practice regarding trans fats in restaurants. The fast-food industry switched from beef tallow to trans-fat rich vegetable oils for deep-fat frying after public demand in 1985, and it was not until 2008 that many American restaurants stopped the use of trans fats. Even though fried-food questions were asked repeatedly and consistently every 4 y, we could not exclude the possibility of unmeasured confounding. However, the relatively homogenous study population could have reduced residual confounding because of the unmeasured socioeconomic variability. Because our participants were predominantly non-Hispanic white health professionals, the generalizability of observed associations may be limited to populations of similar characteristics. Future studies with detailed information on amounts and portion sizes of fried foods as well as types of oils used, times and temperatures used for frying, types of frying (deep fried compared with pan fried), and the degree to which

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FRIED FOOD, DIABETES, AND CORONARY HEART DISEASE TABLE 3 RRs (95% CIs) for coronary heart disease in the NHS and the HPFS according to the frequency of fried-food consumption1 Frequency of fried-food consumption

NHS (1984–2010) Total fried food Cases/person-years Age-adjusted model Model 1 Model 2 Model 3 Model 4 Fried food at home Cases/person-years Age-adjusted model Model 1 Model 2 Model 3 Model 4 Fried food away from home Cases/person-years Age-adjusted model Model 1 Model 2 Model 3 Model 4 HPFS (1986-2010) Total fried food Cases/person-years Age-adjusted model Model 1 Model 2 Model 3 Model 4 Fried food at home Cases/person-years Age-adjusted model Model 1 Model 2 Model 3 Model 4 Fried food away from home Cases/person-years Age-adjusted model Model 1 Model 2 Model 3 Model 4 Pooled results Total fried food Age-adjusted model Model 1 Model 2 Model 3 Model 4 Fried food at home Age-adjusted model Model 1 Model 2 Model 3 Model 4 Fried food away from home Age-adjusted model

,1 time/wk

1–3 times/wk

4–6 times/wk

$7 times/wk

P-trend

1430/942,425 1.00 1.00 1.00 1.00 1.00

861/545,997 1.11 (1.02, 1.21) 1.07 (0.98, 1.16) 1.02 (0.93, 1.11) 1.01 (0.93, 1.10) 1.01 (0.92, 1.10)

316/180,120 1.40 (1.24, 1.58) 1.28 (1.13, 1.45) 1.17 (1.03, 1.33) 1.10 (0.97, 1.25) 1.09 (0.96, 1.24)

80/37,259 1.69 (1.35, 2.12) 1.48 (1.18, 1.86) 1.33 (1.06, 1.68) 1.20 (0.95, 1.51) 1.18 (0.93, 1.48)

— ,0.001 ,0.001 0.02 0.05 0.08

1621/1,059,906 1.00 1.00 1.00 1.00 1.00

918/575,006 1.10 (1.02, 1.20) 1.07 (0.98, 1.16) 1.01 (0.93, 1.10) 1.00 (0.92, 1.09) 1.00 (0.92, 1.09)

148/70,889 1.44 (1.21, 1.70) 1.30 (1.10, 1.54) 1.17 (0.98, 1.39) 1.08 (0.91, 1.29) 1.07 (0.90, 1.28)

— ,0.001 0.002 0.14 0.45 0.52

2210/1,422,207 1.00 1.00 1.00 1.00 1.00

452/271,536 1.35 (1.22, 1.49) 1.25 (1.13, 1.38) 1.19 (1.07, 1.32) 1.12 (1.01, 1.24) 1.11 (1.00, 1.23)

25/12,058 1.71 (1.15, 2.54) 1.44 (0.97, 2.14) 1.34 (0.90, 1.99) 1.19 (0.80, 1.76) 1.16 (0.78, 1.72)

— ,0.001 ,0.001 0.001 0.04 0.08

1287/380,284 1.00 1.00 1.00 1.00 1.00

988/268,648 1.17 (1.08, 1.28) 1.14 (1.05, 1.24) 1.11 (1.02, 1.20) 1.06 (0.97, 1.16) 1.05 (0.97, 1.15)

1709/513,408 1.00 1.00 1.00 1.00 1.00

1180/299,716 1.24 (1.15, 1.34) 1.21 (1.12, 1.30) 1.16 (1.08, 1.25) 1.12 (1.04, 1.21) 1.11 (1.03, 1.20)

202/44,327 1.38 (1.19, 1.60) 1.30 (1.12, 1.51) 1.21 (1.04, 1.41) 1.15 (1.00, 1.35) 1.14 (0.98, 1.33)

— ,0.001 ,0.001 ,0.001 0.01 0.02

2006/548,049 1.00 1.00 1.00 1.00 1.00

963/271,895 1.16 (1.07, 1.25) 1.12 (1.04, 1.21) 1.08 (1.00, 1.17) 1.02 (0.94, 1.10) 1.01 (0.93, 1.09)

122/37,507 1.32 (1.10, 1.58) 1.21 (1.01, 1.46) 1.15 (0.95, 1.38) 1.05 (0.87, 1.26) 1.03 (0.85, 1.24)

— ,0.001 0.002 0.04 0.60 0.83

1.00 1.00 1.00 1.00 1.00

1.14 1.11 1.06 1.04 1.03

(1.08, (1.03, (0.98, (0.97, (0.97,

1.21) 1.18) 1.15) 1.10) 1.09)

1.00 1.00 1.00 1.00 1.00

1.17 1.14 1.08 1.06 1.06

(1.04, (1.00, (0.94, (0.95, (0.95,

1.32) 1.29) 1.24) 1.18) 1.17)

1.00

1.25 (1.08, 1.44)

643/161,080 1.40 (1.27, 1.54) 1.34 (1.21, 1.47) 1.27 (1.15, 1.40) 1.18 (1.06, 1.30) 1.16 (1.05, 1.28)

1.40 1.31 1.23 1.15 1.13

(1.30, (1.22, (1.14, (1.06, (1.04,

173/47,439 1.35 (1.15, 1.58) 1.25 (1.06, 1.46) 1.16 (0.98, 1.36) 1.06 (0.90, 1.25) 1.04 (0.88, 1.22)

1.51) 1.42) 1.33) 1.24) 1.22) 1.41 1.26 1.19 1.13 1.11

1.49 1.33 1.21 1.11 1.08 (1.26, (1.13, (1.07, (1.00, (0.99,

1.57) 1.41) 1.34) 1.26) 1.24)

1.41 (1.12, 1.78)

(1.20, (1.13, (1.06, (0.97, (0.95,

1.85) 1.58) 1.39) 1.26) 1.24)

— ,0.001 ,0.001 ,0.001 0.01 0.03

,0.001 ,0.001 ,0.001 0.001 0.006 ,0.001 ,0.001 0.002 0.04 0.04 0.005 (Continued)

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CAHILL ET AL

TABLE 3 (Continued ) Frequency of fried-food consumption ,1 time/wk Model Model Model Model

1 2 3 4

1.00 1.00 1.00 1.00

1–3 times/wk 1.18 1.13 1.06 1.05

(1.06, (1.03, (0.97, (0.95,

$7 times/wk

4–6 times/wk

1.31) 1.23) 1.17) 1.15)

1.25 1.18 1.07 1.05

(1.06, (0.99, (0.91, (0.89,

1.48) 1.39) 1.27) 1.25)

P-trend 0.01 0.03 0.22 0.33

1 Time-dependent Cox proportional hazards models conditioned on age and follow-up cycle were used for both cohorts individually and then pooled together in an inverse-variance–weighted meta-analysis by using a random-effects model. Model 1 was adjusted for age (y), race (white or nonwhite), parental myocardial infarction before the age of 60 y (yes or no), smoking status [never, past, or current (1–14, 15–24, or $25 cigarettes/d)], alcohol intake (0, 0.1–4.9, 5.0–14.9, or $15.0 g/d in women; 0, 0.1–4.9, 5.0–29.9, or $30.0 g/d in men), physical activity (,3, 3.0–8.9, 9.0–17.9, 18.0–26.9, or $27.0 metabolic equivalent task hours per week), postmenopausal status, and menopausal hormone use [premenopausal or postmenopausal (never, past, or current hormone use); in women only]. Model 2 was adjusted as for model 1 and for total energy intake and the Alternative Healthy Eating Index (quintiles). Model 3 was adjusted as for model 2 and for hypertension and hypercholesterolemia. Model 4 was adjusted as for model 3 and for BMI (in kg/m2; ,23.0, 23.0–24.9, 25.0– 29.9, 30.0–34.9, and $35.0). HPFS, Health Professionals Follow-Up Study; NHS, Nurses’ Health Study.

oils are reused are warranted to confirm our findings in other populations. In conclusion, in 2 large, prospective cohorts, we observed that frequent fried-food consumption was significantly associated with risk of incident T2D and CAD. These associations were mediated in part by BMI, hypertension, and hypercholesterolemia. The findings lend support to the large body of evidence connecting the ubiquity of Western-style fast-food intake to the global T2D and CAD epidemic. Additional studies are required to confirm our findings and elucidate whether the strong associations we observed between fried-food consumption and risk of T2D and CAD are attributable to habitual fried-food consumption having a causal role in the development of T2D and CAD or rather being a marker of an unhealthy lifestyle. Regardless, from a clinical and public health perspective, we have identified a risk factor for T2D and CAD that may be readily modifiable by lifestyle or cooking choices that lead to the consumption of less fried foods, especially those foods consumed away from home. We are indebted to participants in the NHS and HPFS for their continuing outstanding support and the staff working in these studies for their valuable help. The authors’ responsibilities were as follows— LEC and AP: analyzed data, wrote the manuscript, and had primary responsibility for the final content of the manuscript; and all authors: provided critical revisions to the manuscript for important intellectual content, satisfied the authorship criteria of the International Committee of Medical Journal Editors, designed and conducted the research, and read and approved the final manuscript. None of the authors reported any conflicts of interest.

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Fried-food consumption and risk of type 2 diabetes and coronary artery disease: a prospective study in 2 cohorts of US women and men.

Through the processes of oxidation, polymerization, and hydrogenation, the cooking method of frying modifies both foods and their frying medium. Howev...
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