CLINICAL RESEARCH: METABOLIC SYNDROME
Distributions of C-Reactive Protein and its Association With Metabolic Syndrome in Middle-Aged and Older Chinese People
Xingwang Ye, MSc*,
Zhijie Yu, MD, PhD*,
Huaixing Li, PhD*,
Oscar H. Franco, MD, DSc, PhD ,
Yong Liu, PhD* and
Xu Lin, MD, PhD*,*
* Institute for Nutritional Sciences, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences and Graduate School of the Chinese Academy of Sciences, Shanghai, China
Unilever Corporate Research, Colworth Park, Sharnbrook, Bedfordshire, United Kingdom.
Manuscript received September 25, 2006;
revised manuscript received January 5, 2007,
accepted January 15, 2007.
* Reprint requests and correspondence: Dr. Xu Lin, Institute for Nutritional Sciences, 294 Tai-Yuan Rd., Shanghai, 200031, China. (Email: xlin{at}sibs.ac.cn).
 |
Abstract
|
|---|
Objectives: We evaluated the distributions of C-reactive protein (CRP) and its association with metabolic syndrome (MetS) in middle-aged and older Chinese people.
Background: Several studies have suggested that CRP is a risk factor of MetS. However, it remains unclear how CRP levels are distributed and whether they are associated with MetS in Chinese people.
Methods: We conducted a population-based cross-sectional survey in 2005 in Beijing and Shanghai, with a total of 1,458 men and 1,831 women age 50 to 70 years. Metabolic syndrome was defined according to the updated National Cholesterol Education Program Adult Treatment Panel III criteria for Asian Americans.
Results: The median CRP level was 0.68 mg/l among the study population. The CRP levels were significantly higher among participants from Beijing or from urban areas than those in participants from Shanghai or from rural areas (p < 0.01). No gender difference in CRP levels was observed. The prevalence of MetS progressively increased with elevated CRP levels (p < 0.0001 for trend). In the highest quartile of CRP levels (>1.50 mg/l), the risk for MetS was substantially higher (odds ratio 5.97; 95% confidence interval 4.75 to 7.51) compared with that in the lowest quartile of CRP levels ( 0.33 mg/l) after adjustment for age, gender, geographic location, lifestyle factors, educational attainment, and family history of chronic diseases. This association was observed in both obese and nonobese participants.
Conclusions: The overall plasma level of CRP is low but highly associated with the MetS among the middle-aged and elderly Chinese population. Prospective studies are needed to investigate the role of CRP in the development of MetS and related chronic diseases among Chinese people.
|
Abbreviations and Acronyms
| | BMI = body mass index | | CI = confidence interval | | CRM = certified reference material | | CRP = C-reactive protein | | CVD = cardiovascular disease | | HDL = high-density lipoprotein | | LDL = low-density lipoprotein | | MetS = metabolic syndrome | | NCEP-ATPIII = National Cholesterol Education Program Adult Treatment Panel III | | OR = odds ratio |
|
Metabolic syndrome (MetS) is characterized as a concurrence of abnormalities including abdominal obesity, elevated blood pressure, dyslipidemia, and hyperglycemia. Owing to the global epidemic of obesity and sedentary lifestyle, MetS has become one of the most common health problems not only in the West but also in Asia (1). A recent study reported that, in 1992, the prevalence of MetS among Chinese men and women aged 35 to 64 years was 14.4% and 22.0%, respectively, according to the updated National Cholesterol Education Program-Adult Treatment Panel III (NCEP-ATPIII) definition for Asian Americans (2). Gu et al. (1) observed that the prevalence of MetS was higher among women, northern and urban residents compared with men, southern and rural individuals based upon the data from a national cross-sectional survey in China.
Increasing evidence suggests that chronic low-grade inflammation may be part of the "common soil" involving the pathogenesis of MetS, type 2 diabetes, and cardiovascular disease (CVD) (3). C-reactive protein (CRP), an acute-phase reactant, is the most extensively studied biomarker of low-grade inflammation. Compelling evidence has shown that mildly increased CRP is a predictor for CVD (4–6), type 2 diabetes (7,8), and MetS (9,10) in healthy people. However, CRP levels vary among different populations (11–14), and their relation with these diseases in non-Western populations remains unclear. In addition, CRP levels have also been reported to differ by gender (6,14–16) and other factors such as obesity, smoking, alcohol consumption, and physical activity (17). Existing evidence also suggests that CRP might be more strongly correlated with MetS in women than in men (6,9,18,19). Nevertheless, most studies have been conducted in Western populations, and little is known about the CRP distribution and its relation with MetS among Chinese people. In this study, we aimed to investigate the distributions of CRP and its association with MetS in a representative middle-aged and elderly Chinese population.
|
Methods
|
|---|
Study population.
The Nutrition and Health of Aging Population in China is a population-based study among non-institutionalized Chinese people age 50 to 70 years in Beijing and Shanghai, which was designed to investigate the effects of environmental and genetic factors and their interaction on the development of age-related chronic diseases. Beijing and Shanghai were selected as the 2 large cities representing the north and the south of China, respectively. A multistage sampling method was used to recruit the participants. The study was conducted simultaneously in both geographic locations from March to June 2005. In each city, 2 urban districts and 1 rural district were chosen to represent people with high to low socioeconomic status. In the sampling process, 400 participants from each urban district and 800 persons from each rural district were planned to be selected randomly from the eligible candidates listed in the residential registration record. The eligibility of the candidates was defined as those who were stable residents for at least 20 years in the areas and were free from the following conditions: 1) severe psychological disorders, physical disabilities, cancer, CVD, Alzheimer’s disease, or dementia, within 6 months; or 2) currently diagnosed with tuberculosis, AIDS, and other communicable diseases. One person from each household was allowed to participate, and it was required that at least 40% of the total participants were men in each district. All participants provided written informed consents. The protocol was approved by the Institutional Review Board of the Institute for Nutritional Sciences. A total of 3,289 eligible participants (1,458 men and 1,831 women) were recruited.
Data collection.
A home interview was conducted by trained physicians or public health workers from the local Centers for Disease Control and Prevention and community hospitals. Data of demographic variables, health status, health behavior, and physical activity (International Physical Activity Questionnaire, short last 7-day format) was collected using a standardized questionnaire. Smoking habit was defined as never, current (daily smoking, >6 months), and former (cessation of smoking, >6 months). Alcohol drinking was grouped into "yes" or "no." The physical activity level for each individual was classified as low, moderate, or high according to the questionnaire scoring protocol (20). Educational attainment of the participants was categorized into 3 groups according to the number of years of education (0 to 6, 7 to 9, and  10 years). Family history of chronic diseases was considered positive if the participants’ parents or siblings had a history of having 1 of the following diseases: coronary heart disease, stroke, type 2 diabetes, or hypertension.
All participants were invited to have a physical examination at the local health stations or the community clinics after the home interview. Participants were required to fast overnight. Anthropometric measurements were performed by trained medical professionals using a standardized protocol. Body weight and height were measured in light indoor clothing without shoes to the nearest 0.1 kg and 0.1 cm, respectively. Body mass index (BMI) was then calculated as weight (kg)/height (m)2. Participants were categorized as normal weight (<24.0 kg/m2), overweight (24.0 to 27.9 kg/m2), or obese (28.0 kg/m2) (21). Waist circumference was obtained at the mid-point between the lowest rib and the iliac crest to the nearest 0.1 cm, after inhalation and exhalation. Blood pressure was measured by using an electronic blood pressure monitor (Omron HEM-705CP, OMRON Healthcare Inc., Vernon Hills, Illinois) on the right arm of the participant in a comfortable sitting position after at least 5-min rest. Participants were asked to avoid vigorous exercise, eating, drinking, smoking, or long exposure to cold or hot temperatures for 1 h before the measurement. Three measurements were taken, and the mean of the last 2 measurements was used for analysis.
Laboratory methods.
Peripheral venous ethylenediaminetetraacetic acid blood samples were collected and centrifuged at 4°C, 3,000 rpm for 15 min. After being frozen, the samples were shipped in dry ice to the Institute for Nutritional Sciences and stored at –80°C until analysis. Total cholesterol, high-density lipoprotein (HDL) cholesterol, low-density lipoprotein (LDL) cholesterol, triglycerides, and glucose were measured enzymatically on an automatic analyzer (Hitachi 7080, Japan) with reagents purchased from Wako Pure Chemical Industries (Osaka, Japan). Plasma CRP was measured by a particle-enhanced immunoturbidimetric assay (Ultrasensitive CRP kit, Orion Diagnostica, Espoo, Finland) using microparticles coated with anti-human CRP antibodies. The CRP calibrator was standardized against the International Federation of Clinical Chemistry reference material (certified reference material [CRM] 470). The lower detection limit of the assay was 0.25 mg/l. The intra-assay coefficients of variation of the CRP levels were 6.6%, 0.3%, and 0.8% at 0.62, 3.34, and 8.71 mg/l, respectively, while the inter-assay coefficients of variation were 11.9%, 2.1%, and 3.4% at 0.59, 5.53, and 9.12 mg/l, respectively.
Definition of MetS.
The MetS was defined based upon the updated NCEP-ATPIII for Asian Americans (22) as presenting 3 or more of the following components: 1) waist circumference 90 cm for men or 80 cm for women; 2) triglycerides 1.7 mmol/l; 3) HDL cholesterol <1.03 mmol/l for men or <1.30 mmol/l for women; 4) blood pressure 130/85 mm Hg or current use of anti-hypertensive medications; and 5) fasting glucose 5.6 mmol/l or previously diagnosed type 2 diabetes or on oral antidiabetic agents or insulin.
Statistical analyses.
All undetectable CRP values (<0.25 mg/l) were replaced with 0.12 mg/l, and natural log transformations were performed to approximate normality. General linear model for continuous variables and Cochran-Mantel-Haenszel statistics for categorical variables were applied for the comparison between men and women after adjustment for region (Beijing/Shanghai) and residence (urban/rural). The median level of CRP was tested with Wilcoxon rank sum test when comparing between strata (men and women, Beijng and Shanghai, urban and rural). Spearman partial correlation coefficients of CRP, BMI, and elements of MetS were calculated after adjusting for age, gender, and residence. The Kruskal-Wallis test was used to evaluate the association of median CRP levels across numbers of MetS components. The prevalence of MetS was calculated after stratification by gender, region, and residence, respectively. Multivariate logistic regression models were used to estimate the odds ratios (ORs) for the components of MetS or MetS itself. Potential confounding variables associated with CRP and the MetS as suggested by previous publications were controlled in the regression models. The variables were age (continuous), smoking, alcohol drinking, physical activity, education, and family history of chronic diseases, along with gender, region, and residence. In addition, BMI was considered an intermediate factor in the regression model to be adjusted further. Analyses were also repeated in the subgroups of gender, region, and residence, respectively. To calculate the ORs for MetS according to the quartile of CRP levels and obesity status, considering the high correlation of BMI with waist circumference, we used a modified definition of MetS (composed as having 2 or more MetS components without central obesity). Data management and statistical analyses were performed with the SAS statistical package version 9.1 (SAS Institute, Cary, North Carolina). Statistical tests were 2-sided, and a p value <0.05 was considered statistically significant.
|
Results
|
|---|
Characteristics of the participants.
Compared with men, women had higher BMI, total cholesterol, LDL cholesterol, and HDL cholesterol (all p < 0.0001) and lower fasting glucose (p = 0.0005), while men had higher diastolic blood pressure and waist circumference than women (p < 0.0001) (Table 1). A larger proportion of men than women were current smokers (56.1% vs. 5.5%), alcohol drinkers (52.1% vs. 9.9%), and had higher levels of education and physical activity (p < 0.0001).
Distribution of CRP levels.
The median of CRP was 0.68 mg/l in the total population. No significant difference in the CRP concentrations was observed between men and women (Table 2). Beijing participants had a higher CRP level than their Shanghai counterparts (geometric mean 0.84 vs. 0.60 mg/l, p < 0.0001). The difference remained significant after further adjustment for age, BMI, smoking, alcohol drinking, physical activity, family history of chronic diseases, and 4 MetS components (except central obesity) (p < 0.0001). Urban participants had a significantly higher CRP level compared with their rural counterparts (p < 0.01), and the difference disappeared when age and BMI were adjusted.
Association between CRP and MetS.
C-reactive protein was significantly associated with BMI and waist circumference (Table 3). The correlation coefficients between CRP and other components of MetS were slightly lower. As expected, CRP levels increased gradually with increasing numbers of MetS components (Fig. 1). The CRP median for those with 0, 1, 2, 3, 4, and 5 features of MetS were 0.38, 0.44, 0.58, 0.93, 1.10, and 1.72 mg/l, respectively (p < 0.0001 for trend).
View larger version (16K):
[in this window]
[in a new window]
[Download PPT slide]
|
Figure 1 Distribution of CRP Levels According to the Numbers of Components of the Metabolic Syndrome
Data are shown as medians (25th and 75th percentiles); p < 0.0001 for trend. CRP = C-reactive protein.
|
|
The prevalence of MetS progressively increased from 20.2% to 62.4% across CRP quartiles (Table 4). A similar trend was observed in each subgroup: male and female, Beijing and Shanghai, and urban and rural residents (all p < 0.0001 for trend). In each CRP quartile, the prevalence of the MetS was higher among women, Beijing or urban residents compared with their corresponding counterparts. In addition, the prevalence of each MetS feature (i.e., central obesity, elevated blood pressure, hypertriglyceridemia, low HDL cholesterol, and hyperglycemia) increased progressively with elevated CRP levels regardless of gender, region, or residence (all p < 0.0001 for trend).
As expected, increased ORs for the MetS or its components were observed from the 1st to the 4th CRP quartiles (p < 0.0001 for trend) (Table 5). Compared with the people in the lowest CRP quartile, those in the highest quartile had an OR of 5.97 (95% confidence interval [CI] 4.75 to 7.51) for the MetS, 5.82 (95% CI 4.64 to 7.30) for central obesity, 2.32 (95% CI 1.84 to 2.92) for elevated blood pressure, 4.39 (95% CI 3.36 to 5.73) for hypertriglyceridemia, 2.81 (95% CI 2.27 to 3.49) for low HDL cholesterol, and 1.86 (95% CI 1.50 to 2.29) for hyperglycemia, respectively, after adjustment for smoking, alcohol drinking, physical activity, education, and family history of chronic diseases along with age, gender, region, and residence (model 2). The ORs decreased substantially, but were still significant, after further adjustment for BMI (model 3). The increased risks for the MetS corresponding to increased CRP levels were consistent among all the subgroups. Marginally higher ORs for women were observed (p for interaction on gender and CRP quartiles = 0.0405) (model 2). However, the interaction between gender and quartiles of CRP became non-significant after further adjustment for BMI.
View this table:
[in this window]
[in a new window]
|
Table 5 Odds Ratios and 95% Confidence Interval for MetS and its Individual Components According to Quartile of CRP
|
|
The risk of MetS was more pronounced among participants with increased CRP levels and/or BMI (Fig. 2). A significant interaction between CRP and BMI on the risk for MetS was observed (p = 0.0052). In the normal weight group, participants with the highest CRP level had 67% higher risk for MetS than those in the lowest CRP quartile (OR = 1.67 [95% CI 1.22 to 2.28] for Q4 vs. OR = 1.00 for Q1 [reference group]). Among the obese participants, those in the 4th CRP quartile had a 4.6-fold OR for MetS compared with those in the 1st CRP quartile (OR = 15.65 [95% CI 9.66 to 25.34] for Q4 vs. OR = 3.40 [95% CI 1.73 to 6.67] for Q1).
View larger version (30K):
[in this window]
[in a new window]
[Download PPT slide]
|
Figure 2 Adjusted Odds Ratios for Modified Metabolic Syndrome According to the Quartile of CRP and Obesity Status
Adjusted for age, gender, region, residence, smoking, drinking, physical activity, education, and family history of coronary heart disease, stroke, diabetes, and hypertension (p = 0.0052 for interaction of C-reactive protein [CRP] and obesity status). Modified metabolic syndrome was defined as having 2 or more components of metabolic syndrome without central obesity.
|
|
|
Discussion
|
|---|
In general, we found that the distribution of CRP levels in the middle-aged and elderly population in China substantially differed by geographic location. Furthermore, higher CRP levels were associated with an increased risk of MetS, and this association was independent of lifestyle factors, education level, family history of chronic diseases, and BMI.
Previous studies have suggested that CRP levels may be lower in Chinese compared with Caucasian populations. Anand et al. (12) reported that Chinese living in Canada had the lowest CRP level (median 0.69 mg/l) whereas South Asian and ‘native Canadians’ had higher levels compared with Caucasians (median 1.24 mg/l). Similar results were observed in the Study of Women’s Health Across the Nation (13): CRP levels in Japanese (median 0.5 mg/l) and Chinese (median 0.7 mg/l) were lower while higher levels were observed in Hispanic and African-American compared with Caucasian women (median 1.4 mg/l). Interestingly, the CRP level in our study population was similar to the levels found in Chinese in these 2 studies (12,13). In contrast, Yen et al. (23) reported that the CRP level (median 1.5 mg/l) among healthy Chinese men in Taiwan was close to the level found in Western studies. However, 37% of the subjects had CRP levels below the lowest detectable limit (1.0 mg/l) in their study, and 2,046 of 8,374 were excluded for the CRP analysis. Shiesh et al. (24) found that the median CRP among healthy individuals age 45 to 81 years in Taiwan was 0.62 mg/l when using a much more sensitive assay, which was similar to the result in the present study. The reason why Chinese and most East Asians have significantly lower CRP levels than Western populations is unclear. Genetic diversity was reported to influence the baseline level of CRP (25). Relatively low BMI and environmental factors such as diet and lifestyle were also suggested to modulate the CRP concentration (17).
Although the present study further indicated a low overall CRP level in Chinese people, when region or residence was considered, Beijing and urban participants showed significantly higher CRP levels than their Shanghai and rural counterparts. One plausible explanation for increased CRP level may be the higher prevalence of obesity in Beijing and among urban residents (1). Previous studies have showed that higher BMI and waist circumference are related to elevated CRP levels (26). In fact, in this study, after adjusting for BMI, the differences in the CRP level between the regions attenuated remarkably, and the differences between the residences disappeared. However, the differences between the regions could not be fully explained by age, BMI, lifestyle factors, family history of chronic diseases, and MetS components (without central obesity). Other potential factors such as diet and anti-inflammatory drugs may also contribute to the differences in CRP levels (17). Consistent with the results from Chinese living in Canada (12) and Taiwan (24), no gender differences were observed for CRP levels in our study.
In line with the results in other population studies (6,9,18,19,27–31), the CRP was highly associated with individual MetS features and MetS itself in our study population. A similar association was found between men and women in our study after controlling for most confounding factors (including BMI) although a slightly stronger association in women than in men was indicated in other populations even further adjusted for BMI (9,19). The discrepancy between our study and others may be due to the differences in age, BMI, and hormonal profiles (6,9,18,19). More studies are needed to explore whether gender-specific associations between CRP and MetS exist in Chinese people.
Consistent with the studies in other populations (9,10,19), BMI is a pivotal mediator for the association between CRP and the MetS in this Chinese population regardless of gender, region, and residence. However, even though BMI has a predominant influence on the CRP profile and the overall risk of MetS, data from the current study showed that the increased CRP levels per se were highly associated with the individual features of MetS and MetS itself.
Metabolic syndrome is a well-established risk factor for CVD (4–6). Though we did not investigate the relation between MetS and CVD, supporting evidence from a recent study showed a 1.7-fold increased risk of CVD among elderly Chinese people with MetS (32). Based on the high correlation observed in our study between CRP and MetS, it is reasonable to assume that an elevated CRP level might be associated with a higher risk of CVD in Chinese people. However, the CRP levels in our population were low, and approximately 50% of our participants with MetS had CRP levels below 1 mg/l (median for participants with MetS: 1.04 mg/l), which is considered "low risk" for subsequent CVD according to the criteria proposed by Centers for Disease Control and Prevention and the American Heart Association (33). The criteria were mainly generated from studies performed in Caucasian populations. Hence, prospective studies are warranted to investigate CRP, MetS, and other risk factors related to CVD to verify whether the suggested cutoff points are valid in the Chinese population.
To our knowledge, this is the first large-scale, population-based study to investigate CRP distribution and its relation with updated NCEP-ATPIII MetS among both genders in China. One of the advantages of this study was that participants had been recruited from the north (Beijing) and the south (Shanghai) and urban and rural areas, representing a relatively wide range of middle-aged and older Chinese people. In addition, most confounding factors for the risk of MetS in this study were carefully taken into consideration in the regression analyses. Furthermore, the field study was done within a relatively short period of time; thus the seasonal influence on the biomarkers and other lifestyle factors was minimized.
Admittedly, with the cross-sectional nature, it is not possible to establish a cause-effect relationship between CRP levels and MetS. In addition, a relatively large proportion (16.5%) of our study population had a CRP level below the detectable limit due to the overall low CRP level in the Chinese population. Nonetheless, the assay was standardized to the reference material 470, and the CRP levels in our study were consistent with those reported in the literature in which CRP kits were also standardized to CRM 470 (12,13,24). Finally, only 1 fasting blood sample was collected, and the magnitude of the intra-individual variation on the CRP concentration, lipids, and glucose could not be determined.
|
Conclusions
|
|---|
Our study indicates that the overall CRP level in both genders is low and varies with regions and residences among the middle-aged and older Chinese population. There is a strong association between the CRP level and the MetS. Considering the high prevalence of the MetS accompanied with low CRP level in the Chinese population, prospective studies with solid end points of diabetes and CVD are needed to establish biologically relevant CRP cutoff points for future risk assessment and disease prevention.
|
Acknowledgments
|
|---|
The authors thank Drs. Xinghuo Pang, Zhen Zhang, Shufang Jiao, Hong Liu, Shulong Zou, and all other physicians and staff participating in the field work of this study. Thanks are also due to Sharon Catt for her valuable comments during the preparation of the manuscript.
|
Footnotes
|
|---|
This study was funded by research grants from the National Natural Science Foundation of China (30371209), the Innovation Direction Projects of the Chinese Academy of Sciences (KSCX2-2-25), the Science and Technology Commission of Shanghai Municipality (04DZ14007), and the Shanghai-Unilever Research Development Fund (200306).
|
References
|
|---|
1. Gu D, Reynolds K, Wu X, et al. Prevalence of the metabolic syndrome and overweight among adults in China Lancet 2005;365:1398-1405.[CrossRef][Web of Science][Medline]2. Liu J, Grundy SM, Wang W, et al. Ethnic-specific criteria for the metabolic syndrome: evidence from China Diabetes Care 2006;29:1414-1416.[Free Full Text] 3. Tataranni PA, Ortega E. A burning question: does an adipokine-induced activation of the immune system mediate the effect of overnutrition on type 2 diabetes? Diabetes 2005;54:917-927.[Abstract/Free Full Text] 4. Ridker PM, Buring JE, Cook NR, Rifai N. C-reactive protein, the metabolic syndrome, and risk of incident cardiovascular events: an 8-year follow-up of 14 719 initially healthy American women Circulation 2003;107:391-397.[Abstract/Free Full Text] 5. Danesh J, Wheeler JG, Hirschfield GM, et al. C-reactive protein and other circulating markers of inflammation in the prediction of coronary heart disease N Engl J Med 2004;350:1387-1397.[Abstract/Free Full Text] 6. Rutter MK, Meigs JB, Sullivan LM, D’Agostino Sr. RB, Wilson PWF. C-reactive protein, the metabolic syndrome, and prediction of cardiovascular events in the Framingham Offspring Study Circulation 2004;110:380-385.[Abstract/Free Full Text] 7. Nakanishi S, Yamane K, Kamei N, Okubo M, Kohno N. Elevated C-reactive protein is a risk factor for the development of type 2 diabetes in Japanese Americans Diabetes Care 2003;26:2754-2757.[Abstract/Free Full Text] 8. Hu FB, Meigs JB, Li TY, Rifai N, Manson JE. Inflammatory markers and risk of developing type 2 diabetes in women Diabetes 2004;53:693-700.[Abstract/Free Full Text] 9. Han TS, Sattar N, Williams K, Gonzalez-Villalpando C, Lean ME, Haffner SM. Prospective study of C-reactive protein in relation to the development of diabetes and metabolic syndrome in the Mexico City Diabetes Study Diabetes Care 2002;25:2016-2021.[Abstract/Free Full Text] 10. Laaksonen DE, Niskanen L, Nyyssonen K, et al. C-reactive protein and the development of the metabolic syndrome and diabetes in middle-aged men Diabetologia 2004;47:1403-1410.[Web of Science][Medline] 11. Albert MA, Glynn RJ, Buring J, Ridker PM. C-reactive protein levels among women of various ethnic groups living in the United States (from the Women’s Health Study) Am J Cardiol 2004;93:1238-1242.[CrossRef][Web of Science][Medline] 12. Anand SS, Razak F, Yi Q, et al. C-reactive protein as a screening test for cardiovascular risk in a multiethnic population Arterioscler Thromb Vasc Biol 2004;24:1509-1515.[Abstract/Free Full Text] 13. Matthews KA, Sowers MF, Derby CA, et al. Ethnic differences in cardiovascular risk factor burden among middle-aged women: Study of Women’s Health Across the Nation (SWAN) Am Heart J 2005;149:1066-1073.[CrossRef][Web of Science][Medline] 14. Khera A, McGuire DK, Murphy SA, et al. Race and gender differences in C-reactive protein levels J Am Coll Cardiol 2005;46:464-469.[Abstract/Free Full Text] 15. Yamada S, Gotoh T, Nakashima Y, et al. Distribution of serum C-reactive protein and its association with atherosclerotic risk factors in a Japanese population: Jichi Medical School Cohort Study Am J Epidemiol 2001;153:1183-1190.[Abstract/Free Full Text] 16. Ford ES, Giles WH, Mokdad AH, Myers GL. Distribution and correlates of C-reactive protein concentrations among adult US women Clin Chem 2004;50:574-581.[Abstract/Free Full Text] 17. Ledue TB, Rifai N. Preanalytic and analytic sources of variations in C-reactive protein measurement: implications for cardiovascular disease risk assessment Clin Chem 2003;49:1258-1271.[Abstract/Free Full Text] 18. Nakanishi N, Shiraishi T, Wada M. C-reactive protein concentration is more strongly related to metabolic syndrome in women than in men: the Minoh Study Circ J 2005;69:386-391.[CrossRef][Web of Science][Medline] 19. Bo S, Gentile L, Ciccone G, et al. The metabolic syndrome and high C-reactive protein: prevalence and differences by sex in a southern-European population-based cohort Diabetes Metab Res Rev 2005;21:515-524.[CrossRef][Web of Science][Medline] 20. Guidelines for data processing and analysis of the International Physical Activity Questionnaire (IPAQ). Available at: http://www.ipaq.ki.se/dloads/IPAQ%20LS%20Scoring%20Protocols_Nov05.pdf. Accessed July 01, 2006. 21. Bei-Fan Z, Cooperative Meta-Analysis Group of Working Group on Obesity in China Predictive values of body mass index and waist circumference for risk factors of certain related diseases in Chinese adults: study on optimal cut-off points of body mass index and waist circumference in Chinese adults Asia Pac J Clin Nutr 2002;11:S685-S693.[CrossRef][Medline] 22. Grundy SM, Cleeman JI, Daniels SR, et al. Diagnosis and management of the metabolic syndrome: an American Heart Association/National Heart, Lung, and Blood Institute scientific statement Circulation 2005;112:e285-e290.[Free Full Text] 23. Yen ML, Yang CY, Yen BL, Ho YL, Cheng WC, Bai CH. Increased high sensitivity C-reactive protein and neutrophil count are related to increased standard cardiovascular risk factors in healthy Chinese men Int J Cardiol 2006;110:191-198.[CrossRef][Medline] 24. Shiesh SC, Chou TC, Lin XZ, Kao PC. Determination of C-reactive protein with an ultra-sensitivity immunochemiluminometric assay J Immunol Methods 2006;311:87-95.[CrossRef][Web of Science][Medline] 25. MacGregor AJ, Gallimore JR, Spector TD, Pepys MB. Genetic effects on baseline values of C-reactive protein and serum amyloid A protein: a comparison of monozygotic and dizygotic twins Clin Chem 2004;50:130-134.[Abstract/Free Full Text] 26. Visser M, Bouter LM, McQuillan GM, Wener MH, Harris TB. Elevated C-reactive protein levels in overweight and obese adults JAMA 1999;282:2131-2135.[Abstract/Free Full Text] 27. Festa A, D’Agostino Jr. R, Howard G, Mykkanen L, Tracy RP, Haffner SM. Chronic subclinical inflammation as part of the insulin resistance syndrome: the Insulin Resistance Atherosclerosis Study (IRAS) Circulation 2000;102:42-47.[Abstract/Free Full Text] 28. Frohlich M, Imhof A, Berg G, et al. Association between C-reactive protein and features of the metabolic syndrome: a population-based study Diabetes Care 2000;23:1835-1839.[Abstract/Free Full Text] 29. Ford ES. The metabolic syndrome and C-reactive protein, fibrinogen, and leukocyte count: findings from the Third National Health and Nutrition Examination Survey Atherosclerosis 2003;168:351-358.[CrossRef][Web of Science][Medline] 30. Lee WY, Park JS, Noh SY, et al. C-reactive protein concentrations are related to insulin resistance and metabolic syndrome as defined by the ATP III report Int J Cardiol 2004;97:101-106.[CrossRef][Web of Science][Medline] 31. Wannamethee SG, Lowe GD, Shaper AG, Rumley A, Lennon L, Whincup PH. The metabolic syndrome and insulin resistance: relationship to haemostatic and inflammatory markers in older non-diabetic men Atherosclerosis 2005;181:101-108.[CrossRef][Web of Science][Medline] 32. He Y, Jiang B, Wang J, et al. Prevalence of the metabolic syndrome and its relation to cardiovascular disease in an elderly Chinese population J Am Coll Cardiol 2006;47:1588-1594.[Abstract/Free Full Text] 33. Pearson TA, Mensah GA, Alexander RW, et al. Markers of inflammation and cardiovascular disease: application to clinical and public health practice: a statement for healthcare professionals from the Centers for Disease Control and Prevention and the American Heart Association Circulation 2003;107:499-511.[Free Full Text]
This article has been cited by other articles:
|
|
|
|
 
Q. Qi, H. Li, R. J.F. Loos, C. Liu, Y. Wu, F. B. Hu, H. Wu, L. Lu, Z. Yu, and X. Lin
Common variants in KCNQ1 are associated with type 2 diabetes and impaired fasting glucose in a Chinese Han population
Hum. Mol. Genet.,
September 15, 2009;
18(18):
3508 - 3515.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
A. Khera, G. L. Vega, S. R. Das, C. Ayers, D. K. McGuire, S. M. Grundy, and J. A. de Lemos
Sex Differences in the Relationship between C-Reactive Protein and Body Fat
J. Clin. Endocrinol. Metab.,
September 1, 2009;
94(9):
3251 - 3258.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
Y. Wu, H. Li, R. J. F. Loos, Q. Qi, F. B. Hu, Y. Liu, and X. Lin
RBP4 variants are significantly associated with plasma RBP4 levels and hypertriglyceridemia risk in Chinese Hans
J. Lipid Res.,
July 1, 2009;
50(7):
1479 - 1486.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
L. Lu, Z. Yu, A. Pan, F. B. Hu, O. H. Franco, H. Li, X. Li, X. Yang, Y. Chen, and X. Lin
Plasma 25-Hydroxyvitamin D Concentration and Metabolic Syndrome Among Middle-Aged and Elderly Chinese Individuals
Diabetes Care,
July 1, 2009;
32(7):
1278 - 1283.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
Z. Yu, X. Ye, J. Wang, Q. Qi, O. H. Franco, K. L. Rennie, A. Pan, H. Li, Y. Liu, F. B. Hu, et al.
Associations of Physical Activity With Inflammatory Factors, Adipocytokines, and Metabolic Syndrome in Middle-Aged and Older Chinese People
Circulation,
June 16, 2009;
119(23):
2969 - 2977.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
A. Cartier, M. Cote, I. Lemieux, L. Perusse, A. Tremblay, C. Bouchard, and J.-P. Despres
Sex differences in inflammatory markers: what is the contribution of visceral adiposity?
Am. J. Clinical Nutrition,
May 1, 2009;
89(5):
1307 - 1314.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
L. Sun, O. H. Franco, F. B. Hu, L. Cai, Z. Yu, H. Li, X. Ye, Q. Qi, J. Wang, A. Pan, et al.
Ferritin Concentrations, Metabolic Syndrome, and Type 2 Diabetes in Middle-Aged and Elderly Chinese
J. Clin. Endocrinol. Metab.,
December 1, 2008;
93(12):
4690 - 4696.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
A. Pan, O. H. Franco, J. Ye, W. Demark-Wahnefried, X. Ye, Z. Yu, H. Li, and X. Lin
Soy Protein Intake Has Sex-Specific Effects on the Risk of Metabolic Syndrome in Middle-Aged and Elderly Chinese
J. Nutr.,
December 1, 2008;
138(12):
2413 - 2421.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
Q. Qi, J. Wang, H. Li, Z. Yu, X. Ye, F. B Hu, O. H Franco, A. Pan, Y. Liu, and X. Lin
Associations of resistin with inflammatory and fibrinolytic markers, insulin resistance, and metabolic syndrome in middle-aged and older Chinese
Eur. J. Endocrinol.,
November 1, 2008;
159(5):
585 - 593.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
Y. Wu, H. Li, R. J.F. Loos, Z. Yu, X. Ye, L. Chen, A. Pan, F. B. Hu, and X. Lin
Common Variants in CDKAL1, CDKN2A/B, IGF2BP2, SLC30A8, and HHEX/IDE Genes Are Associated With Type 2 Diabetes and Impaired Fasting Glucose in a Chinese Han Population
Diabetes,
October 1, 2008;
57(10):
2834 - 2842.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
A. Kelley-Hedgepeth, D. M. Lloyd-Jones, A. Colvin, K. A. Matthews, J. Johnston, M. R. Sowers, B. Sternfeld, R. C. Pasternak, C. U. Chae, and for the SWAN Investigators
Ethnic Differences in C-Reactive Protein Concentrations
Clin. Chem.,
June 1, 2008;
54(6):
1027 - 1037.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
A. N. DeMaria, J. J. Bax, O. Ben-Yehuda, P. Clopton, G. K. Feld, G. S. Ginsburg, B. H. Greenberg, J. D. Knoke, W. Y.W. Lew, J. A.C. Lima, et al.
Highlights of the year in JACC 2007.
J. Am. Coll. Cardiol.,
January 29, 2008;
51(4):
490 - 512.
[Full Text]
[PDF]
|
|
|
|
|
|
|
H. Li, Y. Wu, R. J.F. Loos, F. B. Hu, Y. Liu, J. Wang, Z. Yu, and X. Lin
Variants in the Fat Mass and Obesity-Associated (FTO) Gene Are Not Associated With Obesity in a Chinese Han Population
Diabetes,
January 1, 2008;
57(1):
264 - 268.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
Q. Qi, Z. Yu, X. Ye, F. Zhao, P. Huang, F. B. Hu, O. H. Franco, J. Wang, H. Li, Y. Liu, et al.
Elevated Retinol-Binding Protein 4 Levels Are Associated with Metabolic Syndrome in Chinese People
J. Clin. Endocrinol. Metab.,
December 1, 2007;
92(12):
4827 - 4834.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
Top
Abstract
Methods