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Plasma Alkylresorcinol Metabolite, a Biomarker of Whole-Grain Wheat

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Plasma Alkylresorcinol Metabolite, a Biomarker of Whole-Grain Wheat 440 Diabetes Care Volume 41, March 2018 Taoping Sun,1,2 Ying Rong,3 Xiaoli Hu,1,2 Plasma Alkylresorcinol Yalun Zhu,1,2 Hao Huang,1,2 Liangkai Chen,1,2 Peiyun Li,1,2 Metabolite, a Biomarker of Whole- Shuzhen Li,1,2 Wei Yang,1,2 Jinquan Cheng,4 Xuefeng Yang,1,2 Grain Wheat and Rye Intake, and Ping Yao,1,2 Frank B. Hu,5 and Risk of Type 2 Diabetes and Liegang Liu1,2 Impaired Glucose Regulation in aChinesePopulation Diabetes Care 2018;41:440–445 | https://doi.org/10.2337/dc17-1570 EPIDEMIOLOGY/HEALTH SERVICES RESEARCH OBJECTIVE To examine the association of plasma alkylresorcinol metabolite 3-(3,5-dihydroxyphenyl)- 1-propanoic acid (DHPPA), a biomarker of whole-grain wheat and rye intake, with type 2 diabetes (T2D) and impaired glucose regulation (IGR) in a Chinese pop- 1Department of Nutrition and Food Hygiene, ulation. Hubei Key Laboratory of Food Nutrition and Safety, School of Public Health, Tongji Medical College, RESEARCH DESIGN AND METHODS Huazhong University of Science and Technology, A total of 1,060 newly diagnosed T2D patients, 736 newly diagnosed IGR patients, Wuhan, China 2Ministry of Education Key Laboratory of Envi- and 1,443 control subjects with normal glucose tolerance were recruited in the case- ronment and Health, School of Public Health, control study. Plasma DHPPA concentrations were determined by high-performance Tongji Medical College, Huazhong University of liquid chromatography–tandem mass spectroscopy. Multivariate logistic regression Science and Technology, Wuhan, China 3 analysis was used to evaluate the independent association of plasma DHPPA con- Department of Nutrition, Shandong Provincial Hospital, Shandong University, Jinan, China centrations with the likelihood of T2D and IGR. 4Department of Microbiology, Shenzhen Center for Disease Control and Prevention, Shenzhen, RESULTS China After adjustment for age, sex, BMI, and family history of diabetes, the odds ratios 5Department of Nutrition, Harvard T.H. Chan (95% CI) of T2D and IGR were 0.57 (0.45, 0.73) and 0.66 (0.50, 0.85), respectively, School of Public Health, Boston, MA comparing the lowest with the highest quartile of plasma DHPPA concentrations. Corresponding authors: Liegang Liu, lgliu@ mails.tjmu.edu.cn, and Frank B. Hu, frank.hu@ Further adjustment for current smoking status, current alcohol consumption, phys- channing.harvard.edu. ical activity, history of hypertension, and educational level did not change the ob- Received 29 July 2017 and accepted 2 November served association materially. Similar results were also obtained in T2D and IGR 2017. groups combined. The inverse association of plasma DHPPA with T2D persisted This article contains Supplementary Data online in stratified analyses according to age, sex, BMI, current smoking status, current at http://care.diabetesjournals.org/lookup/ alcohol consumption, physical activity, family history of diabetes, and history of suppl/doi:10.2337/dc17-1570/-/DC1. hypertension. T.S. and Y.R. contributed equally to this work. © 2017 by the American Diabetes Association. CONCLUSIONS Readers may use this article as long as the work These findings suggested that higher plasma DHPPA concentrations were associated is properly cited, the use is educational and not for profit, and the work is not altered. More infor- with lower odds of T2D and IGR. Further studies are warranted to confirm these mation is available at http://www.diabetesjournals findings in prospective cohorts. .org/content/license. care.diabetesjournals.org Sun and Associates 441 The prevalence of type 2 diabetes (T2D) glucose regulation (IGR) in a case-control morning after an overnight fast and ve- has dramatically increased over the past study conducted among a Chinese Han nous blood samples drawn from the ante- few decades worldwide (1), leading to population. cubital vein were collected. This study considerable increases in related mortal- was approved by the ethics committee ity and economic cost. Although there are RESEARCH DESIGN AND METHODS of Tongji Medical College (Huazhong Uni- several modifiable risk factors for T2D, diet Study Population and Data Collection versity of Science and Technology, Wu- is clearly of paramount importance (2). This study population consisted of 3,239 han, China). All participants provided Recently, whole-grain intake has been participants: 1,060 newly diagnosed T2D writteninformedconsent. confirmed to have an inverse association patients, 736 newly diagnosed IGR pa- with the risk of developing T2D in several tients, and 1,443 control subjects with Laboratory Measurements The collected blood samples were sepa- prospective cohort studies (3–5). A meta- normal glucose tolerance (NGT). All cases rated for plasma within 1 h and then analysis on nutritional studies (6) also were consecutively recruited from indi- stored at 280°C until analysis. Plasma found beneficial effects of whole grains viduals who, for the first time, received a levels of biochemical parameters, includ- on several cardiometabolic risk factors diagnosis of T2D in the Department of En- ing fasting plasma glucose, 2-h postglu- such as fasting glucose, blood insulin, and docrinology, Tongji Hospital, Tongji Medical cose load, total cholesterol, triglyceride, blood lipids. The abundance of dietary College, Wuhan, China, from February HDL cholesterol, and LDL cholesterol, fiber, minerals, vitamins, and phytochemi- 2012 to December 2015. Concomitantly, were measured as previously described cals may contribute to the protective we recruited control subjects from the (23). effects (7,8). general population undergoing a routine Plasma DHPPA was analyzed by high- Available prospective studies on the health checkup in the same hospital. All performance liquid chromatography– association between whole grains and cases were frequency matched with tandem mass spectroscopy (LC-MS/MS) risk of T2D have generally assessed whole- control subjects based on sex and age (AB Sciex QTRAP 4500; Applied Biosys- grain intake through self-administered (65 years). The inclusion criteria were tems, Foster City, CA). Briefly, 50 mLof food frequency questionnaires. However, age $30 years, BMI ,40 kg/m2,andno plasma sample was spiked with the inter- it is always challenging in free-living pop- history of a diagnosis of diabetes or re- nal standard (1 ng of syringic acid). The ulations to accurately measure food and ceiving pharmacological treatment for hy- sample was hydrolyzed overnight at 37°C nutrient intakes, especially for whole-grain perlipidemia and hypertension. Subjects with b-glucuronidase/sulfatase (16) and intake because of the limitations of with clinically significant neurological, en- then extracted with acetonitrile. After whole-grain food composition data docrinological, or other systemic dis- centrifuge, the supernatant was collected, (9,10). Inaccurate identification of differ- eases, as well as those with acute illness and the procedure was repeated once. ent whole-grain constituents as well as and chronic inflammatory or infective dis- The combined supernatants were evapo- incorrect estimation of whole-grain foods eases, were excluded from the study. All rated to dryness under vacuum at 35°C. canleadtomeasurementerrorsand the participants enrolled were of Chinese The residue was then reconstituted in underestimates of health benefits of Han ethnicity. 50 mL of solvent (acetonitrile/water, 1:1, whole grains (11). These together make The diagnostic criteria for IGR and T2D v/v) for LC-MS/MS analysis. Four replicate dietary biomarkers significant as addi- were recommended by the World Health quality control samples were analyzed tional estimates of dietary intake. Organization in 1999, incorporating both in each batch (n = 48). The within- and Alkylresorcinols are phenolic lipids fasting plasma glucose and a 2-h oral glu- between-batch coefficients of variation abundant in the outer layers of rye and cose tolerance test (75 g of glucose) (22). were both ,10%. Validation of this method wheat grain, but absent in highly refined IGR was defined as impaired fasting glu- isdescribedintheSupplementaryData. white flour and most other cereal prod- cose (fasting plasma glucose $6.1 mmol/L ucts (12,13). In human subjects, intact and ,7.0 mmol/L, and 2-h postglucose Statistical Analysis alkylresorcinols and their main metabo- load ,7.8 mmol/L) and/or impaired The differences in plasma DHPPA and lites (3,5-dihydroxybenozoic acid, glucose tolerance (fasting plasma glu- basic characteristics between case and DHBA; 3-(3,5-dihydroxyphenyl)-1-propa- cose ,7.0 mmol/L, and 2-h postglucose control subjects were assessed using noic acid, DHPPA) are measurable in load $7.8 mmol/L and ,11.1 mmol/L). Mann-Whitney U test (continuous varia- plasma (14–16). Recently, they have T2D was confirmed when fasting plasma bles, skewed distribution), Student t test been suggested as biomarkers of whole- glucose was $7.0 mmol/L and/or 2-h (continuous variables, normal distribu- grain wheat and rye intake in epidemio- postglucose load was $11.1 mmol/L. tion), and x2 test (categorical variables). logical studies (17–19). Considering that Basic characteristics, including age, Multiple logistic regression analysis was the estimated half-life is significantly sex, smoking status, alcohol consumption, used to estimate the association be- longer for DHPPA (16.3 h) than DHBA physical activity, history of hypertension, tween plasma DHPPA concentration and (10.1 h) and alkylresorcinols (5 h) (20), family history of diabetes, and educational risk of T2D and IGR. To calculate the odds plasma DHPPA appears to
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