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Song et al. Lipids in Health and Disease (2016) 15:70 DOI 10.1186/s12944-016-0239-y

RESEARCH

Open Access

Associations between non-traditional lipid measures and risk for type 2 diabetes mellitus in a Chinese community population: a cross-sectional study Qiaofeng Song1†, Xiaoxue Liu1†, Anxin Wang2,3, Youxin Wang4, Yong Zhou3, Wenhua Zhou1 and Xizhu Wang1*

Abstract Background: This study investigated associations between type 2 diabetes mellitus and non-traditional lipid measures (total cholesterol (TC)/high-density lipoprotein cholesterol (HDL-C), triglycerides (TG)/HDL-C, and non-HDL-C). Methods: We conducted a community-based, cross-sectional study of 9 078 participants aged 18 years or older (4 768 men and 4 310 women) who lived in the Jidong community, Tangshan, China. The adjusted odds ratios for type 2 diabetes were calculated for every standard deviation change in TC, log-transformed TG, HDL-C, LDL-C, non-HDL-C, TC/HDL-C, and log-transformed TG/HDL-C using multivariate logistic regression analysis. Receiver operating characteristic (ROC) curve analysis was used to define the points of maximum sum of sensitivity and specificity for each lipid measure as a predictor for type 2 diabetes. Results: Prevalence of type 2 diabetes was 6.29 %. Higher TC, TG, LDL-C, non-HDL-C, TC/HDL-C, and TG/HDL-C, and lower HDL-C levels were individually associated with type 2 diabetes in multivariate analyses (all P < 0.05). TC/HDL-C was superior at discriminating between participants with and without type 2 diabetes compared with LDL-C (comparing ROC: P < 0.001), HDL-C (P < 0.001), TG (P = 0.012), TC (P < 0.001), non-HDL-C (P = 0.001), and TG/HDL-C (P = 0.03). The cutoff point for TC/HDL-C was 1.30 mmol/L in this population from the Jidong community. Sensitivity and specificity values for TC/HDL-C were 0.77 and 0.53, respectively. Conclusions: TC/HDL-C is associated with type 2 diabetes and is superior to LDL-C and HDL-C as a risk marker in this population. Keywords: Lipids, Non-HDL cholesterol, type 2 diabetes

Background The prevalence of type 2 diabetes mellitus is increasing globally. In the United States, approximately 18.8 million people were diagnosed with diabetes mellitus in 2010 [1]. The China National Diabetes and Metabolic Disorders Study reported that there were 92.4 million adults with diabetes from June 2007 to May 2008 in China [2]. However, there was also about 148.2 million adults with * Correspondence: [email protected] Qiaofeng Song and Xiaoxue Liu share the first authorship. † Equal contributors 1 Department of Cardiology, Tangshan People’s Hospital, North China University of Science and Technology, No.65 Shengli Road, Lunan District, Tangshan 063000, China Full list of author information is available at the end of the article

prediabetes, defined as impaired fasting glucose and/or impaired glucose tolerance. Identification of risk factors for the development of type 2 diabetes is urgently needed to better understand and prevent this public health epidemic in China. Previous studies have confirmed that type 2 diabetes can be prevented by identifying and intervening in the development of risk factors [3–5]. Studies have shown that dyslipidemia is one of the known risk factors for type 2 diabetes [6, 7]. Traditional lipid measures, including total cholesterol (TC), low-density lipoprotein cholesterol (LDL-C), and triglycerides (TG), are well documented in their association with the incidence of type 2 diabetes [6, 8]. Additionally, evidence indicates that non-high-

© 2016 Song et al. Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

Song et al. Lipids in Health and Disease (2016) 15:70

density lipoprotein cholesterol (non-HDL-C) is a superior marker for the development of vascular disease compared with LDL-C, the traditional lipid measure [9–12]. Other studies have reported that lipid ratios, such as TC/HDL-C, have shown a predictive value for cardiovascular disease [13, 14]. Ley et al. reported that non-HDL-C was associated with the incidence of type 2 diabetes and was superior to LDL-C as a risk predictor in 606 diabetes-free participants [15]. Another prospective study reported that lipid ratios (TG/HDL-C and TC/HDL-C) were associated with the incidence of type 2 diabetes among Iranians [16]. There is a lack of data on associations between nontraditional lipid measures (TC/HDL-C, TG/HDL-C, and non-HDL-C) and type 2 diabetes in China. The current study investigated the association between non-traditional lipid measures with type 2 diabetes and compared their predictive significance to those of traditional lipid variables, including TC, LDL-C, and TG, in a population from the Jidong community, China. We hypothesized that nontraditional lipid measures (TC/HDL-C, TG/HDL-C, and non-HDL-C) are associated with type 2 diabetes and are superior to LDL-C and HDL-C as risk markers in this population.

Methods Study design and population

From July 2013 to August 2014, 9 078 residents of the Jidong community aged 18 years and older were invited to participate in the study. The community is geographically located in Tangshan, which is a modern industrial city located in the central section of the circulating Bohai Sea Gulf region of China and mainly comprises employees of Jidong Oilfield Inc. After excluding participants with incomplete information on type 2 diabetes and lipid measurement data, 8 829 participants were included in the study. At baseline, physical examinations and surveys were conducted by trained medical professionals from medical centers of Jidong Oil Field Inc. The study was approved by the Ethics Committee of Jidong Oilfield Inc. Medical Centers, and signed informed consent was obtained from all participants. Assessment of potential covariates

A questionnaire was used to obtain data on age, sex, marital status, personal monthly income, smoking, drinking, physical activity, education level, and history of diseases (hypertension, type 2 diabetes, stroke, cancer, myocardial infarction). Questionnaires were administered in person by research doctors. Anthropometric measurements, including height, weight, body mass index (BMI), and blood pressure, were measured by three trained doctors and nurses. Height was measured to the nearest 0.1 cm using a tape measure.

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Weight was measured to the nearest 0.1 kg using calibrated platform scales. BMI was calculated as body weight (kg) divided by the square of height (m2). Blood pressure was measured using a mercury sphygmomanometer. Two readings for systolic blood pressure and diastolic blood pressure were taken at 5-min intervals with participants resting in a chair during between measurements. The average of the two readings was used for analyses. If the two measurements differed by more than 5 mmHg, an additional reading was taken, and the average of the three readings was used [17]. Hypertension was defined based on a personal history of hypertension, systolic blood pressure ≥140 mmHg, diastolic blood pressure ≥90 mmHg, or currently taking antihypertensive medication prescribed by a physician [18]. Biochemical index

Blood samples were drawn by trained phlebotomists from participants after an overnight fast for 8–12 h. Venous blood samples in tubes containing ethylenediaminetetraacetic acid trisodium salt hydrate were immediately placed on ice after antecubital venipuncture. Fasting blood glucose (FBG) was measured using the hexokinase/ glucose-6-phosphate dehydrogenase method [19]. TC was measured using the endpoint test method [20]. HDL-C and LDL-C levels were measured using the direct test method [21], and TG was measured using the GPO method [22] (inter-assay coefficient of variation: