Low Carbohydrate–Diet Scores and Long-Term Risk of Type 2 Diabetes
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Diabetes Care Volume 39, January 2016 43 – Wei Bao,1,2 Shanshan Li,1 Low Carbohydrate Diet Scores and Jorge E. Chavarro,3,4,5 Deirdre K. Tobias,3,6 Yeyi Zhu,1 Frank B. Hu,3,4,5 and Long-term Risk of Type 2 Diabetes Cuilin Zhang1 Among Women With a History of Gestational Diabetes Mellitus: A Prospective Cohort Study Diabetes Care 2016;39:43–49 | DOI: 10.2337/dc15-1642 OBJECTIVE Low-carbohydrate diets (LCDs) may improve short-term glycemic control in pa- MANAGEMENT OF GESTATIONAL DIABETES MELLITUS tients with gestational diabetes mellitus (GDM), but the long-term effect on pro- gression from GDM to type 2 diabetes mellitus (T2DM) is unknown. We aimed to examine the long-term risk of T2DM in association with a low-carbohydrate di- etary pattern among women with a history of GDM. RESEARCH DESIGN AND METHODS ’ Overall, 4,502 women with a history of GDM from the Nurses Health Study II 1 ’ Epidemiology Branch, Division of Intramural (NHSII) cohort, as part of the Diabetes & Women s Health (DWH) study, were Population Health Research, Eunice Kennedy followed up from 1991 to 2011. Overall, animal, or vegetable LCD scores, which Shriver National Institute of Child Health and represent adherence to different low-carbohydrate dietary patterns, were calcu- Human Development, National Institutes of lated using diet intake information assessed every 4 years since 1991 by validated Health, Rockville, MD 2Department of Epidemiology, College of Public food-frequency questionnaires. We used Cox proportional hazards models to Health, University of Iowa, Iowa City, IA estimate hazard ratios (HRs) and 95% CIs. 3Department of Nutrition, Harvard T.H. Chan School of Public Health, Boston, MA RESULTS 4Department of Epidemiology, Harvard T.H. We documented 722 incident cases of T2DM during 68,897 person-years of ob- Chan School of Public Health, Boston, MA 5Channing Division of Network Medicine, De- servation. The multivariable-adjusted HRs (95% CIs) of T2DM, comparing the high- partment of Medicine, Brigham and Women’s est with lowest quintiles, were 1.36 (1.04–1.78) for overall LCD score (P = 0.003 for Hospital and Harvard Medical School, Boston, trend), 1.40 (1.06–1.84) for animal LCD score (P = 0.004 for trend), and 1.19 (0.91– MA 6 1.55) for vegetable LCD score (P = 0.50 for trend). Division of Preventive Medicine, Brigham and Women’s Hospital and Harvard Medical School, Boston, MA CONCLUSIONS Corresponding author: Cuilin Zhang, zhangcu@ Among women with a history of GDM, a low-carbohydrate dietary pattern, par- mail.nih.gov. ticularly with high protein and fat intake mainly from animal-source foods, is Received 27 July 2015 and accepted 9 October associated with higher T2DM risk, whereas a low-carbohydrate dietary pattern 2015. with high protein and fat intake from plant-source foods is not significantly asso- This article contains Supplementary Data online ciated with risk of T2DM. at http://care.diabetesjournals.org/lookup/ suppl/doi:10.2337/dc15-1642/-/DC1. © 2016 by the American Diabetes Association. Type 2 diabetes mellitus (T2DM) has become a worldwide epidemic, underscoring Readers may use this article as long as the work is the importance of preventing T2DM as a public health priority (1). Women with a properly cited, the use is educational and not for history of gestational diabetes mellitus (GDM), a common pregnancy complication, profit, and the work is not altered. represent a group at high risk of T2DM (2). Specifically, women with GDM have See accompanying articles, pp. 13, 16, sevenfold increased risk of developing T2DM compared with those with a 24, 31, 39, 50, 53, 55, 61, and 65. 44 LCD Score and T2DM Risk After GDM Diabetes Care Volume 39, January 2016 normoglycemic pregnancy (3). Although RESEARCH DESIGN AND METHODS food by the nutrient content of the GDM is detected during pregnancy, Study Population specified portion based on food compo- most women with GDM probably The study population is composed of sition data from U.S. Department of Ag- have reduced insulin secretion and/or women with a history of GDM in the riculture and data from manufacturers. chronic insulin resistance before preg- Nurses’ Health Study II (NHSII), as part Intakes of carbohydrate, fat, and pro- nancy, and the glucose intolerance of the ongoing Diabetes & Women’s tein were expressed as nutrient densi- may deteriorate through their life span Health (DWH) study (13), which aims to ties (i.e., percent of energy), and intakes (2). The roles of dietary and lifestyle fac- identify determinants of the progression of other nutrients were energy adjusted tors in modifying the natural course of from GDM to T2DM. The NHSII, estab- using the residual method (18). A previ- the progression from GDM to overt lished in 1989, is an ongoing prospective ous validation study comparing energy- T2DM remain to be elucidated in such a cohort study of 116,430 female nurses adjusted macronutrient intake assessed high-risk population. In previous studies, aged 24–44 years at study initiation by the FFQ with four 1-week diet records we found that higher diet quality and a (14). The participants receive a biennial found the Pearson correlation coeffi- physically active lifestyle are associated questionnaire to update information on cients were 0.61 for total carbohydrates, with lower risk of T2DM among women health-related behaviors and disease 0.52 for total protein, and 0.54 for total with prior GDM (4,5). outcomes. Follow-up for each question- fat (16). Low-carbohydrate diets (LCDs) are naire cycle is greater than 90%. This study To represent adherence to various among the most popular diets that are was approved by the Partners Human Re- low-carbohydrate dietary patterns, we claimedtopromoteweightloss(6). search Committee (Boston, MA), with calculated three LCD scores (i.e., overall These diets are appealing because of participants’ consent implied by the re- LCD score, animal LCD score, and vege- not having to count calories or compro- turn of the questionnaires. table LCD score) for each participant, as mise the consumption of many palat- In this cohort, dietary information previously described (19,20). Briefly, we able foods. However, LCDs are at risk was collected first in 1991 and every divided study participants into 11 strata for being nutritionally inadequate or 4 years thereafter using a semiquantita- accordingtoeachoffat,protein,and imbalanced because they enforce re- tive food-frequency questionnaire carbohydrate intake, expressed as per- striction of food choices (7). These diets (FFQ). Participants were eligible for in- centages of energy. We assigned them limit consumption of some healthful clusion in this analysis if they reported 0–10 points for increasing intake of total dietary components, such as whole GDM before 1991 or incident GDM fat, 0–10 points for increasing intake of grains, dietary fiber, fruit, and vegeta- through the 2001 questionnaire. GDM total protein, and inversely, 10–0 points bles, and they can be high in animal fat was last captured on the 2001 question- for increasing intake of carbohydrates. and red meat, which have been associ- naire because most of the NHSII partic- Then we summed points for the three ated with an increased risk of T2DM (8). ipants passed reproductive age. In a macronutrients to create an overall LCD Therefore, long-term adherence to prior validation study among a subgroup score, which ranged from 0 to 30. Simi- LCDs, particularly those mainly based of this cohort, 94% of GDM self-reports larly, we also created an animal LCD on animal-source foods, may have un- were confirmed by medical records (14). score to represent preferential substitu- favorable effects on glucose homeosta- In a random sample of parous women tion of carbohydrates with fat and sis and increase the risk of T2DM. A without GDM, 83% reported a glucose protein from animal sources and a previous study found a dietary pattern screening test during pregnancy, and vegetable LCD score to represent pref- score representing moderately low car- 100% reported frequent prenatal urine erential substitution of carbohydrates bohydrate, high animal protein, and screenings, indicating a high level of with fat and protein from vegetable high animal fat intakes was positively GDM surveillance in this cohort (14). sources. The animal LCD score was associated with T2DM risk (9). Participants were excluded from this based on intakes of carbohydrate, ani- Women with GDM are advised to analysis if they reported chronic disease mal protein, and animal fat, and the limit carbohydrate intake during and (T2DM, cardiovascular disease, cancer) vegetable LCD score was based on in- after pregnancy as a key component before their GDM pregnancy or before takes of carbohydrate, vegetable protein, of medical nutrition therapy. For in- the return of their first post-GDM FFQ, and vegetable fat. A higher score reflects a stance, the Endocrine Society Clinical had a multiple-birth pregnancy, or did higher intake of fat and protein and a Practice Guideline suggests that women not return any post-GDM FFQ. lower intake of carbohydrate, indicating with GDM should limit carbohydrate closer adherence to a low-carbohydrate intake to 35–45% of total calories Exposure Assessment dietary pattern. (10). LCDs may improve short-term gly- Every 4 years since 1991, the partici- cemic control in patients with GDM pants reported their usual intake (fre- Covariate Assessment (11,12), but the long-term effect on quency ranging from never to .6 Information on age, weight, race/ the progression from GDM to T2DM is times/day) during the past year of a ethnicity, family history of diabetes, smok- unknown. In this study, we examined standard portion of each item in the ing status, age at first birth, use of oral the long-term risk of T2DM in asso- FFQ.