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1.  Metabolic Syndrome, Inflammation and Risk of Symptomatic Peripheral Artery Disease in Women: A Prospective Study 
Circulation  2009;120(12):1041-1047.
Metabolic syndrome (MetS) is associated with incident myocardial infarction and stroke and is linked with subclinical inflammation. However, prospective data pertaining to MetS and future peripheral artery disease (PAD) are sparse with few studies examining the role of inflammation. We therefore evaluated the relationship between MetS, inflammation, and incident PAD.
Methods and Results
We conducted a prospective cohort study among 27,111 women free of baseline cardiovascular disease participating in the Women’s Health Study. Subjects were followed for incident symptomatic PAD (n=114; median cohort follow-up=13.3 years). We used Cox proportional hazards models to compare PAD risk among women with and without MetS. We also evaluated relationships between MetS and subclinical inflammation as measured by high sensitivity C-reactive protein (hsCRP) and soluble intercellular adhesion molecule-1 (sICAM-1) and adjusted for these biomarkers in multivariable models. Women with MetS had a 62% increased risk of future PAD (HR 1.62; 95% CI 1.10–2.38). After multivariable adjustment, MetS remained significantly associated with PAD (adj HR 1.48; 95% CI 1.01–2.18) with a 21% risk increase per additional MetS-defining trait (adj HR 1.21; 95% CI 1.06–1.39). Median levels of hsCRP were 4.0 versus 1.5 mg/L (p<0.0001) and 374 versus 333 ng/mL for sICAM-1(p<0.0001) in women with and without MetS, respectively. When hsCRP and sICAM-1 were added to multivariable models, risk associated with the MetS was substantially attenuated and no longer significant (HR 1.14, 95% CI 0.75–1.73).
MetS is associated with an increased risk of future symptomatic PAD in women. This risk appears largely mediated by the effects of inflammation and endothelial activation.
PMCID: PMC2763563  PMID: 19738135
Peripheral artery disease; metabolic syndrome; inflammation; endothelial dysfunction; women
2.  Prediabetes Is Associated with an Increased Risk of Testosterone Deficiency, Independent of Obesity and Metabolic Syndrome 
PLoS ONE  2013;8(9):e74173.
The association between type 2 diabetes and low testosterone has been well recognized. However, testosterone levels in men with prediabetes have been rarely reported. We aimed to investigate whether prediabetes was associated with an increased risk of testosterone deficiency.
This study included 1,306 men whose sex hormones was measured during a medical examination. Serum total testosterone and sex hormone-binding globulin were measured; free and bioavailable testosterone concentrations were calculated by Vermeulen’s formula. Prediabetes was defined by impaired fasting glucose (IFG), impaired postprandial glucose (IPG), or glycated hemoglobin (HbA1c) 5.7%-6.4%. Logistic regression was performed to obtain the odds ratios (OR) for subnormal total testosterone (<300 ng/dL) or free testosterone (<6 ng/dL) in prediabetic and diabetic men compared with normoglycemic individuals, while adjusting for age, BMI, waist circumference, and metabolic syndrome (MetS).
Normoglycemia, prediabetes, and diabetes were diagnosed in 577 (44.2%), 543 (41.6%), and 186 (14.2%) men, respectively. Prediabetes was associated with an increased risk of subnormal total testosterone compared to normoglycemic individuals (age-adjusted OR=1.87; 95%CI=1.38-2.54). The risk remained significant in all multivariate analyses. After adjusting for MetS, the OR in prediabetic men equals that of diabetic patients (1.49 versus 1.50). IFG, IPG, and HbA1c 5.7%-6.4% were all associated with an increased risk of testosterone deficiency, with different levels of significance in multivariate analyses. However, neither prediabetes nor diabetes was associated with subnormal free testosterone in multivariate analyses.
Prediabetes is associated with an increased risk of testosterone deficiency, independent of obesity and MetS. After adjusting for MetS, the risk equals that of diabetes. Our data suggest that testosterone should be measured routinely in men with prediabetes.
PMCID: PMC3772062  PMID: 24069277
3.  Comprehensive analysis of circulating adipokines and hsCRP association with cardiovascular disease risk factors and metabolic syndrome in Arabs 
Cardiovascular diseases (CVD) are a leading cause of death worldwide including the Middle East. This is caused in part by the dysregulation of adipose tissue leading to increased production of pro-inflammatory adipokines and reduction in cardio-protective adipokines such as adiponectin. Ethnicity has been recognized as a major factor in the association between CVD risk factors and the different circulating adipokines. In this study, for the first time, the relationship between traditional cardiovascular risk factors, Metabolic Syndrome (MetS) and circulating level of adipokines in Arab ethnicity was investigated.
We conducted a population-based cross-sectional survey on 379 adult Arab participants living in Kuwait. Traditional cardiovascular risk factors such as blood pressure (BP), low density lipoprotein (LDL) and triglyceride (TG) were measured. Plasma levels of circulating Leptin, Plasminogen Activator Inhibitor (PAI-1) visfatin, adiponectin, resistin and adipsin were assessed using the multiplexing immunobead-based assay.
Circulating levels of High sensitivity C-Reactive Protein (hsCRP), Leptin, PAI-1 and adiponectin were significantly higher in Arab women than men (p < 0.0001). In multi-variate analysis, the homeostasis model assessment-insulin resistance (HOMA-IR) and body mass index (BMI) showed strong association with most of the biomarkers (p < 0.05). HsCRP showed significant association with all risk factors (p < 0.05). Leptin, PAI-1 and adipsin showed significant positive correlation with BMI, unlike adiponectin which showed inverse correlation (p < 0.05). Subjects in the highest tertile of leptin, PAI-1 and hsCRP had higher odds of having Metabolic Syndrome (MetS) (odd ratio [OR] = 3.02, 95% confidence interval [CI] = 1.47 – 6.19) and (OR = 2.52, 95% CI = 1.45 – 4.35), (OR = 4.26, 95% CI = 2.39 – 7.59) respectively. On the other hand subjects with highest tertile of adiponectin had lower odds of having MetS (OR = 0.22, 95% CI = 0.12 – 0.40). Leptin, PAI-1 and hsCRP showed significant positive association with increased MetS components (P-trend <0.05), while adiponectin was negatively associated with increased MetS components (P-trend <0.0001).
Our results show positive association between hsCRP, leptin, PAI-1 with increased MetS components and increase the odds of having MetS. Adiponectin on the other hand showed inverse correlation with MetS components and associated with reduction in MetS. Overall, our data highlights the significant clinical value these markers have in MetS especially hsCRP which can be used as good marker of low grade inflammation in Arabs.
PMCID: PMC3997236  PMID: 24716628
Adipokine; Arab; Metabolic syndrome; Cardiometabolic risk factors; Lipid profile; hsCRP; Leptin; Adiponectin; Visfatin; Resistin; Adipsin; Low grade inflammation
4.  Diagnosis of the Metabolic Syndrome Is Associated With Disproportionately High Levels of High-Sensitivity C-Reactive Protein in Non–Hispanic Black Adolescents 
Diabetes Care  2011;34(3):734-740.
Whereas it is known that the metabolic syndrome (MetS) has a paradoxically lower prevalence in non–Hispanic black adolescents than in non–Hispanic whites or Hispanics, the relative severity of MetS by race/ethnicity is unknown. Inflammation, indicated by high-sensitivity C-reactive protein (hsCRP), is a key factor linking MetS to cardiovascular disease and type 2 diabetes. Our goal was to determine whether elevations of hsCRP vary by race/ethnicity among adolescents with MetS.
We used the National Health and Nutrition Examination Survey (1999–2008) and evaluated adolescents (age 12–19 years) using a pediatric/adolescent adaptation of the ATP III definition of MetS. We used linear regression to evaluate the interaction between MetS status and ethnicity with respect to hsCRP concentration.
For male and female adolescents, MetS was associated with elevated hsCRP levels compared with adolescents without MetS. However, the elevation in hsCRP between adolescents with and without MetS was greater in non–Hispanic blacks compared with that in non–Hispanic whites (P = 0.04) but not that in Hispanics (P = 0.18). hsCRP concentrations correlated with individual MetS components similarly among all ethnicities. In an evaluation of adolescents diagnosed with MetS, non–Hispanic blacks had higher BMI and more hypertension than other ethnicities but there were no other racial/ethnic differences in the features of MetS.
Non–Hispanic black adolescents have a greater differential in hsCRP between those with and those without MetS than the differential in non–Hispanic whites but not that in Hispanics. Therefore, even though MetS has a low prevalence in non–Hispanic blacks, MetS is a particularly good indicator of inflammation in non–Hispanic black adolescents.
PMCID: PMC3041218  PMID: 21285387
5.  Do inflammation and procoagulation biomarkers contribute to the metabolic syndrome cluster? 
The metabolic syndrome (MetS), in addition to its lipid, metabolic, and anthropomorphic characteristics, is associated with a prothrombotic and the proinflammatory state. However, the relationship of inflammatory biomarkers to MetS is not clear.
To study the association between a group of thrombotic and inflammatory biomarkers and the MetS.
Ten conventional MetS risk variables and ten biomarkers were analyzed. Correlations, factor analysis, hexagonal binning, and regression of each biomarker with the National Cholesterol Education Program (NCEP) MetS categories were performed in the Family Heart Study (n = 2,762).
Subjects in the top 75% quartile for plasminogen activator inhibitor-1 (PAI1) had a 6.9 CI95 [4.2–11.2] greater odds (p < 0.0001) of being classified with the NCEP MetS. Significant associations of the corresponding top 75% quartile to MetS were identified for monocyte chemotactic protein 1 (MCP1, OR = 2.19), C-reactive protein (CRP, OR = 1.89), interleukin-6 (IL6, OR = 2.11), sICAM1 (OR = 1.61), and fibrinogen (OR = 1.86). PAI1 correlated significantly with all obesity and dyslipidemia variables. CRP had a high correlation with serum amyloid A (0.6) and IL6 (0.51), and a significant correlation with fibrinogen (0.46). Ten conventional quantitative risk factors were utilized to perform multivariate factor analysis. Individual inclusion, in this analysis of each biomarker, showed that, PAI1, CRP, IL6, and fibrinogen were the most important biomarkers that clustered with the MetS latent factors.
PAI1 is an important risk factor for MetS. It correlates significantly with most of the variables studied, clusters in two latent factors related to obesity and lipids, and demonstrates the greatest relative odds of the 10 biomarkers studied with respect to the MetS. Three other biomarkers, CRP, IL6, and fibrinogen associate also importantly with the MetS cluster. These 4 biomarkers can contribute in the MetS risk assessment.
PMCID: PMC2254623  PMID: 18154661
6.  Dysfunctional Adiposity and the Risk of Prediabetes and Type 2 Diabetes in Obese Adults 
The risk of type 2 diabetes mellitus is heterogeneous among obese individuals. Factors that discriminate prediabetes or diabetes risk within this population have not been well characterized. A dysfunctional adiposity phenotype, characterized by excess visceral fat and insulin resistance, may contribute to diabetes development in those with obesity.
To investigate associations between adiposity phenotypes and risk for incident prediabetes and diabetes in a multiethnic, population-based cohort of obese adults.
Design, Setting, and Participants
Among 732 obese participants (body mass index ≥30) aged 30 to 65 years without diabetes or cardiovascular disease enrolled between 2000 and 2002 in the Dallas Heart Study, we measured body composition by dual energy x-ray absorptiometry and magnetic resonance imaging (MRI); circulating adipokines and biomarkers of insulin resistance, dyslipidemia, and inflammation; and subclinical atherosclerosis and cardiac structure and function by computed tomography and MRI.
Main Outcome Measures
Incidence of diabetes through a median 7.0 years (interquartile range, 6.6–7.6) of follow-up. In a subgroup of 512 participants with normal fasting glucose values at baseline, incidence of the composite of prediabetes or diabetes was determined.
Of the 732 participants (mean age, 43 years; 65% women; 71% non-white), 84 (11.5%) developed diabetes. In multivariable analysis, higher baseline visceral fat mass (odds ratio [OR] per 1 SD [1.4 kg], 2.4; 95% CI, 1.6–3.7), fructosamine level (OR per 1 SD [1.1 μmol/L], 2.0; 95% CI, 1.4–2.7), fasting glucose level (OR per 1 SD [1.1 μmol/L], 1.9; 95% CI, 1.4–2.6), family history of diabetes (OR, 2.3; 95% CI, 1.3–4.3), systolic blood pressure (OR per 10 mm Hg, 1.3; 95% CI, 1.1–1.5), and weight gain over follow-up (OR per 1 kg, 1.06; 95% CI, 1.02–1.10) were independently associated with diabetes, with no associations observed for body mass index, total body fat, or abdominal subcutaneous fat. Among the 512 participants with normal baseline glucose values, the composite outcome of prediabetes or diabetes occurred in 39.1% and was independently associated with baseline measurements of visceral fat mass; levels of fasting glucose, insulin, and fructosamine; older age; non-white race; family history of diabetes; and weight gain over follow-up (P<.05 for each) but not with measurements of general adiposity.
Excess visceral fat and insulin resistance, but not general adiposity, were independently associated with incident prediabetes and type 2 diabetes mellitus in obese adults.
PMCID: PMC3556508  PMID: 22990274
7.  Higher serum soluble receptor for advanced glycation end product levels and lower prevalence of metabolic syndrome among Japanese adult men: a cross-sectional study 
Although several studies showed that decreased soluble receptor for advanced glycation end products (sRAGE) is associated with metabolic syndrome (MetS), inflammation level has not been considered, even though ligand–RAGE interaction induces inflammation. The objective of the study was to determine the association between sRAGE and MetS among Japanese adult in a cross-sectional survey, taking the level of low grade inflammation into consideration.
Serum soluble RAGE (sRAGE) were measured in 712 men and 176 women aged 30–83 years with serum C-reactive protein (hsCRP) concentration below 3 mg/L. MetS was defined using the criteria of the American Heart Association Scientific Statements of 2009.
After multivariable adjustment, among men, higher sRAGE levels were associated with lower odds of MetS as well as central obesity and elevated blood pressure. Comparing the extreme tertiles of sRAGE, odds ratios (95% confidence interval) were 0.58 (0.36–0.95; P for trend = 0.001) for MetS; 0.41 (0.25–0.52; P for trend < 0.001) for central obesity; and 0.45 (0.29–0.70; P for trend < 0.001) for elevated blood pressure. Moreover, participants were categorized according to their median hsCRP and sRAGE values. Men in the higher hsCRP/higher sRAGE category had a 40% lower odds ratio for MetS than those in the higher hsCRP/lower sRAGE category (P = 0.031). Among women, there was no association between sRAGE levels and the prevalence of MetS.
Higher circulating RAGE concentrations were associated with lower prevalence of MetS and its components among Japanese men.
PMCID: PMC4016590  PMID: 24602408
Endogenous secretory RAGE; Low grade inflammation; CRP
8.  Aldosterone, C-Reactive Protein, and Plasma B-Type Natriuretic Peptide Are Associated With the Development of Metabolic Syndrome and Longitudinal Changes in Metabolic Syndrome Components 
Diabetes Care  2013;36(10):3084-3092.
Several pathomechanisms are implicated in the pathogenesis of metabolic syndrome (MetS), most of which have not been investigated in African Americans (AAs). We examined the contribution of a selected panel of biomarkers to the development of MetS in Jackson Heart Study (JHS) participants in this investigation.
We evaluated 3,019 JHS participants (mean age, 54 years; 64% women) with measurements for seven biomarkers representing inflammation (high-sensitivity C-reactive protein [CRP]), adiposity (leptin), natriuretic pathway (B-natriuretic peptide [BNP]), adrenal pathway (cortisol and aldosterone), and endothelial function (endothelin and homocysteine). We related the biomarker panel to the development of MetS on follow-up and to longitudinal changes in MetS components.
There were 278 (22.9%) of 1,215 participants without MetS at baseline who had development of new-onset MetS at follow-up. The incidence of MetS was significantly associated with serum aldosterone (P = 0.004), CRP (P = 0.03), and BNP (P for trend = 0.005). The multivariable-adjusted odds ratios (95% CI) per SD increment of log biomarker were as follows: 1.25 (1.07–1.45) for aldosterone, 1.20 (1.02–1.43) for CRP, and 1.54 (1.07–2.23) and 1.91 (1.31–2.80) for low and high BNP quartiles, respectively. Aldosterone was positively associated with change in all MetS risk components, except low HDL cholesterol and waist circumference. CRP concentration was significantly and directly associated with change in systolic blood pressure (SBP) and waist circumference but inversely associated with HDL cholesterol. For BNP, we observed a U-shape relation with SBP and triglycerides.
Our analysis confirms that, in AAs, higher circulating aldosterone and CRP concentrations predict incident MetS. The nonlinear U-shape relation of BNP with MetS and its components has not been reported before and thus warrants replication.
PMCID: PMC3781556  PMID: 23757435
9.  Association of Endothelial and Oxidative Stress with Metabolic Syndrome and Subclinical Atherosclerosis: Multi-Ethnic Study of Atherosclerosis 
A cluster of metabolic abnormalities termed metabolic syndrome (MetS) is associated with vascular endothelial dysfunction and oxidative internal milieu. We examined whether the association of MetS with subclinical atherosclerosis is explained by biomarkers of endothelial damage and oxidative stress.
MESA is a population based study of 45-84 year old individuals of four US ethnicities without clinical cardiovascular disease. A random sample of 997 MESA participants had data on the following biomarkers: von Willebrand Factor, soluble intercellular adhesion molecule-1 (sICAM1), CD40 ligand, soluble thrombomodulin, E-selectin, and oxidized LDL (oxLDL). We examined whether the associations of MetS with B-mode ultrasound-defined common and internal carotid intimal medial thickness (IMT) and coronary artery calcium (CAC) measured using computerized tomography were explained by the biomarkers using multiple regression methods.
MetS was associated with higher levels of each of the biomarkers (p<0.001, CD40L suggestive association p=0.004), with greater IMT (p<0.001), and with greater extent of CAC in those in whom CAC was detectable (p=0.01). The association of MetS with measures of subclinical atherosclerosis remained unchanged after adjustment for the biomarkers. After adjusting for MetS, oxLDL was suggestively associated with greater prevalence of detectable CAC (p=0.005) and thicker internal carotid IMT (p=0.002), while sICAM-1was significantly associated with greater prevalence of detectable CAC (p=0.001).
The association of MetS with subclinical atherosclerosis was independent of its association with biomarkers of endothelial damage and oxidative stress, suggesting that metabolic abnormalities and oxidative endothelial damage may lead to atherosclerotic disease through distinct mechanisms.
PMCID: PMC3130805  PMID: 21505504
Metabolic syndrome; biomarkers; coronary artery atherosclerosis; carotid arteries
10.  Relationship of Weekly Activity Minutes to Metabolic Syndrome in Prediabetes: The Healthy Living Partnerships to Prevent Diabetes 
Physical inactivity contributes to metabolic syndrome (MetS) in overweight/obesity. However, little is known about this relationship in prediabetes.
The study purpose is to examine relationships between physical activity (PA) and MetS in prediabetes. The Healthy Living Partnerships to Prevent Diabetes tested a community translation of the Diabetes Prevention Program (DPP). Three hundred one overweight/obese prediabetics provided walking minutes/week (WM) and total activity minutes/week (AM) via the International Physical Activity Questionnaire. MetS was at least 3 of waist (men ≥ 102 cm, women ≥ 88 cm), triglycerides (≥150 mg·dl), blood pressure (≥130·85 mm Hg), glucose (≥100mg·dl), and HDL (men < 40mg·dl, women < 50mg·dl).
The sample was 57.5% female, 26.7% nonwhite/Hispanic, 57.9 ± 9.5 years and had a body mass index (BMI) 32.7 ± 4 kg·m2. Sixty percent had MetS. Eighteen percent with MetS reported at least 150 AM compared with 29.8% of those without MetS. The odds of MetS was lower with greater AM (Ptrend = .041) and WM (Ptrend = .024). Odds of MetS with 0 WM were 2.08 (P = .046) and with no AM were 2.78 (P = .009) times those meeting goal. One hour additional WM led to 15 times lower MetS odds.
Meeting PA goals reduced MetS odds in this sample, which supported PA for prediabetes to prevent MetS.
PMCID: PMC3765007  PMID: 23036940
obesity; walking; physical activity
11.  Metabolic syndrome, C-reactive protein and microalbuminuria in a rural Chinese population: a cross-sectional study 
BMC Nephrology  2013;14:118.
Microalbuminuria is an early marker of chronic kidney disease (CKD). Previous studies have shown that either metabolic syndrome (MetS) or chronic inflammation is related to renal impairment. The aim of this study was to investigate the association between MetS, C-reactive protein (CRP) and microalbuminuria in a rural Chinese population.
This was a cross-sectional study using data from the Handan Eye Study. MetS was defined according to the Chinese Diabetes Society (CDS) criteria. CRP levels ≥ 3 mg/L were classified as high CRP. Microalbuminuria was defined as a urinary albumin/creatinine ratio (ACR) of 30–300 mg/g.
We included 4191 subjects aged ≥ 30 years in this analysis. The prevalence of MetS and microalbuminuria in the group was 25.7% and 15.6%, respectively. The odds ratio (OR) of microalbuminuria in subjects with MetS was 1.25 (95% confidence interval (CI): 1.03 − 1.51) compared with those without microalbuminuria. In multivariate logistic regression analysis, high blood pressure (OR 1.36, 95% CI: 1.10 − 1.67) and high fasting blood glucose (OR 1.44, 95% CI: 1.17 − 1.76) were independently associated with microalbuminuria. Subjects with high CRP and MetS had a 1.46-fold greater risk of having microalbuminuria compared with those with low CRP without MetS (95% CI: 1.06 − 2.01).
In this rural Chinese population aged ≥30 years, MetS and microalbuminuria were independently related and the combination of high CRP and MetS was associated with an increased risk of microalbuminuria.
PMCID: PMC3674949  PMID: 23725496
Microalbuminuria; Metabolic syndrome; Inflammation; Epidemiology
12.  Association of Biomarkers of Inflammation with Dyslipidemia and Its Components among Mongolians in China 
PLoS ONE  2014;9(2):e89023.
This study aims to examine the association between inflammatory biomarkers and dyslipidemia and its components among Mongolians in China.
Data were obtained from 2544 Mongolians via standard questionnaires and blood samples in Inner Mongolia, China. High sensitivity C-reactive protein (hsCRP), soluble intercellular adhesion molecule-1 (sICAM-1) and soluble E-selectin (sE-selectin) as well as blood lipids were examined.
Individuals with dyslipidemia had higher levels of hsCRP, sICAM-1 and sE-selectin than those without dyslipidemia (all P values<0.001). Compared to the lowest quartile of inflammatory biomarkers, individuals with the highest quartile were more likely to have dyslipidemia (odds ratio, 95% confidence interval: 3.215, 2.551–4.116 for hsCRP; 1.575, 1.253–1.980 for sICAM-1; 1.495, 1.193–1.873 for sE-selectin). Moreover, hsCRP was associated with all the components of dyslipidemia, whereas, sICAM-1 was not related to high density lipoprotein cholesterol (HDL-c) or triglycerides (TAG). Additionally, sE-selectin was just associated with TAG.
Our study indicated that elevated plasma levels of hsCRP, sICAM-1 and sE-selectin were positively and significantly associated with increased risk of dyslipidemia among Mongolians. However, the associations were not identical for different inflammatory biomarkers with the components of dyslipidemia.
PMCID: PMC3928392  PMID: 24558466
13.  Trend analysis of diabetic prevalence and incidence in a rural area of South Korea between 2003–2008 
Aims/Introduction:  This study determined the change in prevalence of diabetes and prediabetes over a period of 5 years in South Korea. The incidence of diabetes and prediabetes and risk factors associated with the development of diabetes were also investigated.
Materials and Methods:  The Dalseong population‐based cohort survey recruited 1806 subjects who were over 20‐years‐old in 2003. Five years later, 1287 of the original subjects were re‐evaluated and 187 new subjects were added to the study. All participants completed a questionnaire, were given a physical examination, and provided blood samples for analysis including 2 h oral glucose tolerances.
Results:  Age‐adjusted prevalence of diabetes rose from 6.7% in 2003 to 9.1% in 2008. The prevalence of prediabetes also increased from 18.5% in 2003 to 28.4% in 2008. The incidence rates of diabetes and prediabetes were 18.3 per 1000 person‐years and 55.4 per 1000 person‐years, respectively. The development of diabetes was associated with impaired fasting glucose (IFG) (odds ratio [OR] 5.661), impaired glucose tolerance (IGT) (OR: 6.013), age (OR 1.013), and waist‐to‐hip ratio (OR 1.513). After excluding the IFG and IGT, systolic blood pressure (OR 1.023), high‐sensitivity C‐reactive protein (hsCRP; OR 1.097), triglyceride (OR 1.002) and waist‐to‐hip ratio (OR 1.696) were statistically significant risk factors in a multivariate logistic regression analysis.
Conclusions:  A significant rise in the prevalence of diabetes and prediabetes was observed between 2003 and 2008. In addition, this study newly demonstrated that waist‐to‐hip ratio and hsCRP were associated with the development of diabetes after adjusting for several confounding factors. (J Diabetes Invest, doi: 10.1111/j.2040‐1124.2010.00045.x, 2010)
PMCID: PMC4020719  PMID: 24843430
Diabetes mellitus; Prevalence; South Korea
14.  Association of C-Reactive Protein With Reduced Forced Vital Capacity in a Nonsmoking U.S. Population With Metabolic Syndrome and Diabetes  
Diabetes Care  2008;31(10):2000-2002.
OBJECTIVE—A relationship between inflammation, measured by C-reactive protein (CRP), and forced vital capacity (FVC) in diabetes or metabolic syndrome (MetS) has not been established. We investigated whether high CRP is related to reduced FVC in MetS and diabetes.
RESEARCH DESIGN AND METHODS—We examined the association of MetS/diabetes and CRP (normal ≤3 mg/l, high >3 mg/l) with predicted FVC in 4,272 nonsmoking U.S. adults aged 18–79 years without lung disease in the Third National Health and Nutrition Examination Survey. Logistic regression examined odds of FVC <80% by CRP and MetS/diabetes.
RESULTS—Mean FVC in individuals with MetS and high CRP (95.7%) and those with diabetes and high CRP (93.7%) was lower than in those with no MetS/diabetes and normal CRP (101.7%) (P < 0.01) and was lower in those with MetS and high CRP (95.7%) than in those with MetS and normal CRP (98.5%) (P < 0.01). The odds ratio (95% CI) of FVC <80% was highest in individuals with MetS and high CRP (odds ratio 4.26 [95% CI 2.08–8.73], P < 0.01) compared with those with no MetS/diabetes and normal CRP.
CONCLUSIONS—Elevated CRP is associated with lower FVC in people with MetS.
PMCID: PMC2551643  PMID: 18591402
15.  Metabolic Syndrome, Inflammation, and the Incident Heart Failure in the Elderly: the Cardiovascular Health Study 
Circulation. Heart failure  2008;1(4):242-248.
Inflammation markers and MetS are associated with risk of CHF. We evaluated whether combining inflammation markers and metabolic syndrome (MetS) provided additive information for incident congestive heart failure (CHF), and if incorporating inflammation markers to the MetS definition added prognostic information.
Methods and Results
We studied 4017 men and women ≥ 65 years old, without baseline CHF or diabetes, participating in the Cardiovascular Health Study, an observational study with 12.2 years follow-up and 966 cases of incident CHF. Baseline “C-reactive protein (CRP)-MetS” or “interleukin-6 (IL-6)-MetS” were defined as presence of 3 out of 6 components, with elevated CRP (≥3 mg/L) or IL-6 (≥2.21 pg/mL) as a 6th component added to ATPIII criteria. Cox models adjusted for CHF risk factors and incident coronary disease, were used to calculate HRs for CHF. MetS and elevated inflammation markers were independently associated with CHF risk (HRs, 95 % CI: 1.32, 1.16–1.51 for MetS; 1.53, 1.34–1.75 for CRP; 1.37, 1.19–1.55 for IL-6). There was a 20% relative excess risk attributed to the combination of MetS and CRP (95% CI −44% to 88%). CRP-MetS and IL-6-MetS definitions reclassified 18% and 13%, respectively of participants as MetS. Both CRP-MetS and IL-6-MetS increased risk of CHF by 60% compared to those without MetS.
MetS and inflammation markers provided additive information on CHF risk in this elderly cohort. Inflammation-incorporated MetS definitions identified more participants with the same risk level as ATPIII MetS. Considering inflammation markers and MetS together may be useful in clinical and research settings.
PMCID: PMC2762642  PMID: 19808298
heart failure; metabolism; inflammation
16.  Differential association between metabolic syndrome and coronary artery disease evaluated with cardiac computed tomography according to the presence of diabetes in a symptomatic Korean population 
Metabolic syndrome (MetS) is associated with increased risks of diabetes and coronary artery disease (CAD). Despite the controversial inclusion of established diabetes in MetS, the association between MetS and CAD according to diabetes status has not been elucidated in the Asian population.
We evaluated the association between MetS and CAD using the parameters including any plaque, obstructive plaque, and coronary artery calcium score (CACS) >100 according to diabetes status in 2,869 symptomatic Korean subjects who underwent cardiac computed tomographic angiography.
The prevalence of MetS was significantly higher in the diabetic subjects than in the non-diabetic subjects (69% vs. 34%, P <0.001). The incidence of any plaque (64% vs. 43%, P <0.001), obstructive plaque (26% vs. 13%, P = 0.006), and CACS >100 (23% vs. 12%, P = 0.012) was significantly higher in diabetic subjects than in non-diabetic subjects. Among the MetS components, decreased high-density lipoprotein level was significantly associated with any plaque (odds ratio [OR] 1.35), obstructive plaque (OR 1.55), and CACS >100 (OR 1.57) in the non-diabetic subjects (P <0.01, respectively). However, none of the MetS components were associated with all the parameters in the diabetic subjects. Multivariate regression analysis revealed that MetS and the number of MetS components (MetSN) were independently associated with any plaque (MetS: OR 1.55, P <0.001; MetSN: OR 1.22, P <0.001), obstructive plaque (MetS: OR 1.52, P = 0.003; MetSN: OR 1.25, P <0.001), and CACS >100 (MetS: OR 1.46, P = 0.015; MetSN: OR 1.21, P = 0.004) only in the non-diabetic subjects, respectively.
MetS was independently associated with the presence and severity of CAD only in the non-diabetic subjects among the symptomatic Korean population.
PMCID: PMC4236521  PMID: 25138993
Metabolic syndrome; Diabetes; Coronary artery disease; Coronary computed tomographic angiography
17.  Association of High Sensitivity C-Reactive Protein with the Components of Metabolic Syndrome in Diabetic and Non-Diabetic Individuals 
Background and Objectives: High sensitivity C-reactive protein (hsCRP) has been associated with metabolic syndrome (MetS) and its components. Several studies have suggested hsCRP to be used as a marker for the primary prevention of cardiovascular diseases. So, we aimed to evaluate the association between hsCRP levels and the components of MetS in diabetic and non-diabetic population.
Materials and Methods: Type II diabetic patients (T2DM) (n= 121) and healthy controls (n= 121) were enrolled for the study. Anthropometric measurements were taken along with blood pressure from the arm. Ten ml of blood was collected after overnight fasting for the measurement of lipid profile, hsCRP, C-peptide and glucose levels. Insulin resistance (HOMA2-IR) was estimated by HOMA2 calculator utilizing glucose and C-peptide values. All participants were classified into two groups on the basis of the presence or absence of MetS. Data were analysed through SPSS 14 software.
Results: hsCRP, C-peptide and HOMA2-IR were significantly higher in T2DM subjects when compared with controls. As the number of the components of MetS increased, there was a linear increase in hsCRP levels in whole study population (p trend <.001), diabetic subjects (p trend <.001), as well as in controls (p trend <.001). HOMA2-IR and hsCRP levels were found to be better than LDL cholesterol and waist circumference for predicting the presence of MetS.
Conclusion: hsCRP was found to be better than LDL cholesterol and waist circumference for the prediction of MetS. Hence, hsCRP could be used as a defining marker of MetS in the near future.
PMCID: PMC4129304  PMID: 25120975
C-peptide; HOMA2 calculator; Insulin resistance
18.  The value of Apolipoprotein B/Apolipoprotein A1 ratio for metabolic syndrome diagnosis in a Chinese population: a cross-sectional study 
The apoB/apoA1 ratio has been reported to be associated with the metabolic syndrome (MetS), and it may be a more convenient biomarker in MetS predicting. However, whether apoB/apoA1 ratio is a better indicator of metabolic syndrome than other biomarkers and what is the optimal cut-off value of apoB/apoA1 ratio as an indicator of metabolic syndrome in Chinese population remain unknown. Thus, we carried out the current study to assess the predictive value of apoB/apoA1 ratio and determine the optimal cut-off value of apoB/apoA1 ratio for diagnosing MetS in a Chinese population.
We selected 1,855 subjects with MetS and 6,265 individuals without MetS based on the inclusion and exclusion criteria from the China Health Nutrition Survey (CHNS) in 2009. MetS was identified based on the diagnostic criteria of International Diabetes Federation (2005). Logistic regression was used to estimate the association between the apoB/apoA1 ratio and risk of MetS, and receiver operating characteristics (ROC) curve analysis was performed to test the predictive value of apoB/apoA1 ratio and calculate the appropriate cut-off value.
Compared with the lowest quartile of apoB/apoA1 ratio, subjects in the fourth quartile had a higher risk of MetS in both men [odds ratio (OR) = 2.64, 95% confidence interval (CI) =1.82-3.83] and women (OR = 5.18, 95% CI = 3.87-6.92) after adjustment for potential confounders. The optimal cut-off value of apoB/apoA1 ratio for MetS detection was 0.85 in men and 0.80 in women. Comparisons of ROC curves indicated that apoB/apoA1 ratio was better than traditional biomarkers in predicting MetS.
Our results suggest that, apoB/apoA1 ratio has a promising predictive effectiveness in detection of MetS. An apoB/apoA1 ratio higher than 0.85 in men and 0.80 in women may be a promising and convenient marker of MetS.
PMCID: PMC4041140  PMID: 24886173
Metabolic syndrome; Apolipoprotein ratio; ROC curve
19.  Low-Grade Albuminuria Is Associated with Metabolic Syndrome and Its Components in Middle-Aged and Elderly Chinese Population 
PLoS ONE  2013;8(6):e65597.
Micro-albuminuria has been well established as one of the risk factors of metabolic syndrome (MetS). However, the association of MetS and its components with low-grade albuminuria among those with normal urinary albumin excretion has not been clearly elucidated in Chinese population.
Methodology and Findings
A cross-sectional study was conducted among 9,579 participants with normal urinary albumin excretion, who were recruited from Jia Ding District, Shanghai, China. The single-void first morning urine sample was collected for urinary albumin and creatinine measurements, and urinary albumin-to-creatinine ratio (UACR) was calculated as urinary albumin divided by creatinine. Low-grade albuminuria was classified as sex-specific upper UACR quartile in this population. MetS was defined according to the National Cholesterol Education Program Adult Treatment Panel III criteria. The prevalence of MetS and its components increased across the UACR quartiles (all P trend <0.01). A multivariable adjusted logistic regression analysis revealed that the prevalence of MetS was gradually elevated according to the UACR quartiles (adjusted odds ratios [ORs] were 1.14, 1.24 and 1.59 for UACR quartiles 2, 3 and 4, compared with the lowest quartile; P trend<0.0001). In the further stratified logistic regression analyses, the associations between low-grade albuminuria and MetS were significant in both sex strata (male and female), both age strata (<60 and ≥60 years), both body mass index strata (<24 and ≥24 kg/m2), and both diabetes strata (yes and no). Compared to the lowest UACR quartile, the participants in the highest quartile of UACR had the highest prevalence of central obesity (OR = 1.43; 95%CI = 1.25–1.63), high blood pressure (OR = 1.64; 95%CI = 1.43–1.87), hyperglycemia (OR = 1.52; 95%CI = 1.30–1.78) and high triglycerides (OR = 1.19; 95%CI = 1.04–1.37).
Conclusions and Significance
Low-grade albuminuria was significantly associated with the increasing prevalence of MetS and its components in the middle-aged and elderly Chinese population with normal urinary albumin excretion.
PMCID: PMC3689760  PMID: 23805186
20.  Impact of HbA1c criterion on the definition of glycemic component of the metabolic syndrome: the China health and nutrition survey 2009 
BMC Public Health  2013;13:1045.
In 2009, a unified definition of metabolic syndrome (MetS) was proposed, of which, the glycemic component is defined on the basis of fasting plasma glucose (FPG) level. Recently, the American Diabetes Association (ADA) recommended the use of glycated hemoglobin (HbA1c) as an alternative to FPG to define prediabetes. Hence, we aim to compare the performance of HbA1c and FPG in the definition of glycemic component of the MetS among Chinese adults.
We conducted a cross-sectional analysis of 7641 Chinese participants aged ≥18 years using data from the China Health and Nutrition Survey 2009. MetS was defined according to the consensus criteria in 2009. We compared the use of HbA1c versus FPG in the definition of the glycemic component of MetS. Increased HbA1c value was defined following the criterion of HbA1c cut-off point of ≥5.7% recommended by the ADA.
Overall, 1136 (14.9%) had MetS according to FPG ≥ 5.6 mmol/l, and 1640 (21.5%) had MetS according to HbA1c ≥ 5.7%. Compared with individuals with FPG-based diagnosis of MetS, individuals with HbA1c-based diagnosis of MetS were older, had higher levels of LDL-C, magnesium, and transferrin, and lower levels of uric acid. Of those found to have MetS according to either FPG or HbA1c (n = 2008), overlap between HbA1c- and FPG-based diagnosis of MetS was limited (n = 768, 38.2%). The overlap index regarding MetS diagnosed by FPG or HbA1c persisted low in each evaluated subgroup (≤ 50.0%).
We note limited overlap and poor agreement between FPG- and HbA1c-based diagnosis of MetS. Screening MetS through introduction of HbA1c in addition to FPG could contribute to identification of more people with MetS.
PMCID: PMC3924337  PMID: 24188743
Fasting plasma glucose; HbA1c; Metabolic syndrome; CVD risk factors
21.  Impaired Retinal Vasodilator Responses in Prediabetes and Type 2 Diabetes 
Acta ophthalmologica  2013;91(6):e462-e469.
In diabetes, endothelial dysfunction and subsequent structural damage to blood vessels can lead to heart attacks, retinopathy and strokes. However, it is unclear whether prediabetic subjects exhibit microvascular dysfunction indicating early stages of arteriosclerosis and vascular risk. The purpose of this study was to examine whether retinal reactivity may be impaired early in the hyperglycemic continuum and may be associated with markers of inflammation.
Individuals with prediabetes (n = 22), type 2 diabetes (n = 25) and healthy age and body composition matched controls (n = 19) were studied. We used the Dynamic Vessel Analyzer to assess retinal vasoreactivity (percent change in vessel diameter) during a flickering light stimulation. Fasting highly sensitive c-reactive protein (hs-CRP), a marker of inflammation, was measured in blood plasma.
Prediabetic and diabetic individuals had attenuated peak vasodilator and relative amplitude changes in retinal vein diameters to the flickering light stimulus compared to healthy controls (peak dilation: prediabetic subjects 3.3 ± 1.8 %, diabetic subjects 3.3 ± 2.1% controls 5.6 ± 2.6%, p = .001; relative amplitude: prediabetic subjects 4.3 ± 2.2%, diabetic subjects 5.0 ± 2.6% and control subjects 7.2 ± 3.2%, p = .003). Similar findings were observed in retinal arteries. Levels of hs-CRP were not associated with either retinal vessel response parameters.
Retinal reactivity was impaired in prediabetic and type 2 diabetic individuals in parallel with reduced insulin sensitivity but not associated with levels of hs-CRP. Retinal vasoreactivity measurements may be a sensitive tool to assess early vascular risk.
PMCID: PMC3749269  PMID: 23742315
prediabetes; type 2 diabetes; retinal reactivity; vasodilation; flickering light stimulation
22.  Microvascular dysfunction in the course of metabolic syndrome induced by high-fat diet 
Metabolic syndrome (MetS) is associated with increased risk of cardiovascular disease (CVD). One important feature underlying the pathophysiology of many types of CVD is microvascular dysfunction. Although components of MetS are themselves CVD risk factors, the risk is increased when the syndrome is considered as one entity. We aimed to characterize microvascular function and some of its influencing factors in the course of MetS development.
Development of MetS in C57BL/6 mice on a high-fat diet (HFD, 51% of energy from fat) was studied. The initial phase of MetS (I-MetS) was defined as the first 2 weeks of HFD feeding, with the fully developed phase occurring after 8 weeks of HFD. We characterized these phases by assessing changes in adiposity, blood pressure, and microvascular function. All data are presented as mean ± standard error (SEM). Differences between cumulative dose–response curves of myograph experiments were calculated using non-linear regression analysis. In other experiments, comparisons between two groups were made with Student’s t-test. Comparisons between more than two groups were made using one-way ANOVA with Tukey post-hoc test. A probability value <0.05 was considered statistically significant.
I-MetS mice presented with weight gain, blood pressure elevation, and microvascular dysfunction characterized by augmented vasoconstriction. This finding, contrary to those in mice with fully developed MetS, was not associated with endothelial dysfunction, insulin resistance, or systemic inflammation. In the initial phase, perivascular adipose tissue showed no sign of inflammation and had no influence on the pattern of vasoconstriction. These findings suggest that the onset of hypertension in MetS is strongly influenced by vascular smooth muscle cell dysfunction and independent of important factors known to influence microvascular function and consequently blood pressure levels.
We identified in I-MetS the occurrence of isolated augmented vasoconstriction along with blood pressure elevation, but not the presence of classical MetS components known to influence microvascular function. These findings increase our understanding of the pathophysiology of CVD risk associated with MetS.
PMCID: PMC3916304  PMID: 24490784
High-fat diet; Metabolic syndrome; Hypertension; Microvascular dysfunction; Vasoconstriction
23.  Prevalence of chronic kidney disease across levels of glycemia among adults in Pudong New Area, Shanghai, China 
BMC Nephrology  2013;14:253.
Few population-based studies have examined the relationship between glycemic status and chronic kidney disease (CKD) in China. We examined the prevalence of CKD across categories of glycemia [diagnosed diabetes, undiagnosed diabetes (fasting plasma glucose [FPG] ≥ 126 mg/dL), prediabetes (FPG 100–126 mg/dL) and normal glycemia (FPG <100 mg/dL)] among Chinese adults and assessed the relative contribution of dysglycemia (prediabetes and/or diabetes) to the burden of CKD.
5,584 Chinese adults aged 20–79 years were selected from the Pudong New Area of Shanghai through a multistage random sampling. Demographic and lifestyle characteristics, anthropometry and blood pressure were measured. Biochemical assays included FPG, serum creatinine and lipids, urinary creatinine and albumin. Prevalence of albuminuria [urine albumin-to-creatinine ratio (ACR) ≥ 30 mg/g], decreased kidney function and CKD (either decreased kidney function or albuminuria) across levels of glycemia were estimated.
The prevalence of albuminuria, decreased kidney function and CKD each increased with higher glycemic levels (P < 0.001). Based on the MDRD Study equation, the unadjusted CKD prevalence was 30.9%, 28.5%, 14.1% and 9.2% in those with diagnosed diabetes, undiagnosed diabetes, prediabetes and normoglycemia, respectively. The corresponding age-, gender- and hypertension-adjusted CKD prevalence were 25.8%, 25.0%, 12.3% and 9.1%, respectively. In a multivariable analysis, the factors associated with CKD were hypertension (Odds ratio [OR] 1.70, 95% confidence interval [CI]: 1.42-2.03), dysglycemia (OR 1.65, 95% CI: 1.39-1.95), female gender (OR 1.48, 95% CI: 1.25-1.75), higher triglycerides (OR 1.14, 95% CI: 1.08-1.20 per mmol/L), higher body mass index (OR 1.08, 95% CI: 1.05-1.10 per kg/m2), and older age (OR 1.02, 95% CI: 1.01 -1.03 per year). The population attributable risks (PARs) associated with diabetes, prediabetes, dysglycemia (diabetes and prediabetes) and hypertension were 18.4%, 19.7%, 30.3% and 44.5% for CKD as defined by the MDRD study equation, and 15.8%, 24.4%, 29.2% and 10.0% with the CKD-EPI equation. Estimates of prevalence and ORs of the relative contribution of various risk factors to CKD obtained with the CKD-EPI equation were similar.
As much as 30% of the CKD burden may be associated with dysglycemia among Chinese adults, independent of age, gender and hypertension status. Prevention and control of diabetes and prediabetes should be a high priority in reducing the CKD burden in China.
PMCID: PMC4225706  PMID: 24238578
Chronic kidney disease; Glycemia; Epidemiology
24.  An evaluation of the metabolic syndrome in a large multi-ethnic study: the Family Blood Pressure Program 
The Family Blood Pressure Program is an ongoing, NHLBI-sponsored, multi-center program to study the genetic determinants of high blood pressure. The goal of this particular study was to study patterns of metabolic syndrome (MetS) in four ethnic groups: African Americans, Caucasians, Hispanics, and Asians.
A major part of participants in three networks GENOA, HyperGEN and SAPPHIRe were recruited mainly through hypertensive probands. MetS was defined as a categorical trait following the National Cholesterol Education Program definition (c-MetS). MetS was also characterized quantitatively through multivariate factor analyses (FA) of 10 risk variables (q-MetS). Logistic regression and frequency tables were used for studying associations among traits.
Using the NCEP definition, the Hispanic sample, which by design was enriched for type 2 diabetes (T2D), had a very high prevalence of MetS (73%). In contrast, its prevalence in Chinese was the lowest (17%). In African Americans and Hispanics, c-MetS was more prevalent in women than in men. Association of c-MetS with type 2 diabetes (T2D) was prominent in the Hispanics and African Americans, less pronounced in the Whites and Japanese, (although still significant), and weakest in the Chinese sample.
Using FA without rotation, we found that the main factor loaded obesity (OBS) and blood pressure (BP) in African Americans; OBS and insulin (INS) in Hispanics, in Japanese, and in Whites; and OBS alone in Chinese. In Hispanics, Whites, and Japanese, BP loaded as a separate factor. Lipids in combination with INS also loaded in a separate factor. Using FA with Varimax rotation, 4 independent factors were identified: "Obesity-INS," "Blood pressure," "Lipids-INS," and "Central obesity." They explained about 60% of the variance present in the original risk variables.
MetS ethnic differences were identified. Ascertaining for hypertension or T2D increased the MetS prevalence in networks compared with the one in the US general population. Obesity was the most prominent risk factor contributing to both c-MetS and q-MetS. INS contributed in two important factors (obesity and lipids). The information imbedded into c-MetS trait /q-MetS factors scores can contribute in future research of the MetS, especially its utilization in the genetic analysis.
PMCID: PMC1201342  PMID: 16076393
25.  Metabolic syndrome among a middle-aged population in the Red River Delta region of Vietnam 
Metabolic syndrome (MetS) is a clustering of metabolic risk factors for cardiovascular diseases and type 2 diabetes. The study aimed to estimate the prevalence of MetS, its components, and their associations among rural middle-aged population in Vietnam.
A cross-sectional study with a representative sample (n = 2443) was conducted to collect data on demographic, socioeconomic, anthropometric, lifestyles, plasma glucose, and lipid profile. The age- and sex-adjusted prevalences of MetS and its components were calculated using the direct standardization. Associations of risk factors with MetS were evaluated using logistic regression, taken into account the confounding factors.
The total age- and sex-adjusted prevalence (95% CI) of MetS was 16.3% (14.0 - 18.6). The most frequent component of MetS was high triglycerides (43.2%), followed by low HDL-C (42.0%), elevated blood pressure (29.2%), high plasma glucose (14.3%), and central obesity (12.3%). Of the total population, only 17.6% did not have any component of MetS and more than 40% had at least two MetS components. The association of MetS with residence, age, body mass index, marital status, and siesta time per day was statistically significant in univariate analysis and replicated in multivariate analysis.
The MetS prevalence and its components are common and major public health burden in the middle-aged adults in Vietnam. Habitants living in urban, being never-married, having an increase in age, BMI, and siesta time per day are significantly associated with MetS, and they should be paid much more attention for screening and implementing preventive activities.
PMCID: PMC4179436  PMID: 25261978
Metabolic syndrome; Population–based study; Prevalence; Associated factors; Vietnamese

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