Peer Reviewed Studies That Resulted From the Bogalusa Heart Study

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Peer-reviewed

Research Article

Cigarette Smoking Exacerbates the Adverse Effects of Historic period and Metabolic Syndrome on Subclinical Atherosclerosis: The Bogalusa Eye Report

• Shengxu Li,
• Miaoying Yun,
• Camilo Fernandez,
• Jihua Xu,
• Sathanur R. Srinivasan,
• Wei Chen,
• Gerald Southward. Berenson

x

• Published: May 2, 2014
• https://doi.org/10.1371/journal.pone.0096368

Figures

Abstract

Historic period and metabolic syndrome are major risk factors for atherosclerosis. Nevertheless, express data is available regarding whether cigarette smoking, another major, modifiable risk factor, has synergistic effects with age and metabolic syndrome on subclinical atherosclerosis, particularly in young adults. This aspect was examined in 1,051 adults (747 whites and 304 blacks; aged 24–43 years) from the Bogalusa Heart Study. General linear models were used to examine the effects of cigarette smoking and its interactive furnishings with age and metabolic syndrome on carotid intima-media thickness (CIMT). After adjusting for age, race, and sex, current smokers had lower BMI (mean±SE: 27.4±0.4, 29.3±0.5, and 29.ix±0.3 kg/mⁱⁱ in electric current, onetime, and never smokers, respectively; p<0.0001) and lower levels of fasting glucose (82.viii±0.nine, 89.5±2.three, and 87.ane±ane.1 mg/dL, respectively; p = 0.001) and insulin (10.6±0.4, 14.two±i.0, 13.6±0. 6 µU/ml, respectively; p<0.0001). Despite being lean and having favorable levels of glucose and insulin, electric current smokers had greater CIMT (0.850±0.012, 0.808±0.011, and 0.801±0.006 mm, respectively; p = 0.0004). Importantly, cigarette smoking showed pregnant interactions with historic period and metabolic syndrome on CIMT: Age-related alter in CIMT in current smokers was significantly greater (0.013±0.002 mm/year) than in nonsmokers (former and never smokers combined) (0.008±0.001 mm/twelvemonth) (p for interaction = 0.005); the difference in CIMT between those with and without metabolic syndrome was significantly greater in current smokers (0.154±0.030 mm, p<0.0001) than in nonsmokers (0.031±0.014 mm, p = 0.03) (p for interaction<0.0001). In decision, cigarette smoking significantly exacerbates the agin furnishings of historic period and metabolic syndrome on subclinical atherosclerosis in young adults, which underscores the importance of prevention and cessation of cigarette smoking behavior in the young.

Citation: Li S, Yun M, Fernandez C, Xu J, Srinivasan SR, Chen W, et al. (2014) Cigarette Smoking Exacerbates the Adverse Furnishings of Age and Metabolic Syndrome on Subclinical Atherosclerosis: The Bogalusa Heart Study. PLoS One 9(v): e96368. https://doi.org/ten.1371/journal.pone.0096368

Editor: Yan Li, Shanghai Institute of Hypertension, China

Received: Jan 14, 2014; Accepted: April 5, 2014; Published: May 2, 2014

Copyright: © 2014 Li et al. This is an open-access article distributed under the terms of the Creative Eatables Attribution License, which permits unrestricted utilise, distribution, and reproduction in any medium, provided the original writer and source are credited.

Funding: The Bogalusa Heart Study is supported by grants 5R01ES021724 from National Institute of Environmental Wellness Scientific discipline and 2R01AG016592 from the National Institute on Crumbling. Shengxu Li is a scholar of the Building Interdisciplinary Enquiry in Women'south Health plan, supported past Honour Number K12HD043451 from the Eunice Kennedy Shriver National Institute of Child Wellness & Man Development. Shengxu Li is also partly supported by Grant 13SDG14650068 from American Heart Association. The funders had no function in report design, data collection and analysis, conclusion to publish, or grooming of the manuscript.

Competing interests: Shengxu Li is a member of the Editorial Board. This does non alter the authors' adherence to PLOS ONE Editorial policies and criteria.

Introduction

Atherosclerotic diseases, similar coronary heart disease, are leading causes of deaths[1]. Many risk factors contribute to the acceleration of these conditions[2]. And amongst the take a chance factors, age is the most important[3], [4]. Metabolic syndrome, a common cluster of interrelated cardiometabolic factors including obesity, insulin resistance, dyslipidemia, and elevated claret pressure, is also predictive of atherosclerotic diseases and related bloodshed[5]–[8]. Additionally, cigarette smoking is a well-established, powerful hazard factor for morbidity and mortality associated atherosclerosis[nine]–[15]_ENREF_8_ENREF_8. These risk factors often exert a joint effect on the development of atherosclerosis. For example, Framingham Hazard Score, which combines multiple take chances factors, is used for assessment of cardiovascular risk[16]–[19].

Although the joint effect of multiple risk factors has been well established, express information is bachelor regarding whether cigarette smoking, a very common and modifiable risk factor[twenty], strengthens the agin effort of age and metabolic syndrome on atherosclerotic diseases. Such information is important in terms of early on prevention and identification of individuals with cardiovascular risk. Carotid intima-media thickness (CIMT) measured by ultrasound is widely used every bit a valid noninvasive measurement for subclinical atherosclerotic diseases, and is linked to the presence, extent, and development of atherosclerosis[21]–[24]_ENREF_18. Few studies have examined whether the association of age and metabolic syndrome with CIMT is modified by the condition of cigarette smoking[thirteen]. In the current study, we tested the hypothesis that cigarette smoking exacerbates the effects of age and metabolic syndrome on CIMT in a community-based sample of young adults from the Bogalusa Centre Study.

Methods

Ideals statement

Written informed consent was obtained from each participant of the study. The protocol was approved past the Institutional Review Board of the Tulane University Health Sciences Center.

Report sample

During 2000–2002, 1,203 young adults aged 24–43 years residing in a black-white community (65% white and 35% black) of Bogalusa, LA, were examined for cardiovascular risk factors[25]. Among these, 1,051individuals who had CIMT measurements were included in the current assay. The cardiovascular risk factor variables included body mass index (BMI), waist circumference, low-density lipoprotein (LDL) cholesterol, high-density lipoprotein (HDL) cholesterol, triglycerides, fasting glucose and insulin, systolic and diastolic blood pressure, and cigarette smoking status, along with demographic and lifestyle variables.

Examinations

The survey followed substantially the aforementioned protocol for risk gene measurements[26]. Participants were instructed to fast for 12 h earlier screening, with fourth dimension and compliance ascertained by interview on the morning of the examination. Height, weight, and waist circumference were measured twice and the mean values were used. Information on cigarette smoking condition, leisure fourth dimension physical activity, alcohol intake, and medications for blazon 2 diabetes, hypertension, and high cholesterol was obtained as part of a health addiction questionnaire[27]. For cigarette smoking condition, participants were grouped into 3 categories: current smokers, former smokers, and never smokers. Electric current smoking was defined by "I smoke at least one cigarette a week"; former smoking was defined past "I used to smoke at least one cigarette a calendar week"; and never smoking was defined every bit not existence a current or a old smoker. Alcohol drinking was divers by "drink alcohol during the past 12 months". Leisure time physical activity was categorized into iii groups, low, moderate, and vigorous physical activity, according to a class of i–5 for concrete activity outside of work, with 1 existence about inactive and 5 most agile (i = depression; 2–3 = moderate; 4–5 = vigorous). Replicate blood pressure measurements were obtained on the right arm of the participants in a relaxed, sitting position. Arm measurements, length and circumference, were made during the examination to ensure the use of a proper cuff size. Systolic and diastolic blood force per unit area levels were recorded as the beginning and fifth Korotkoff phases using mercury sphygmomanometers. These blood pressure readings were taken past each of two randomly assigned and trained observers and levels were reported as the hateful of six replicate readings.

Laboratory analyses

Serum full cholesterol and triglycerides levels were measured past enzymatic procedures on the Hitachi 902 Automated Analyzer (Roche Diagnostics, Indianapolis, IN). Serum lipoprotein cholesterols were analyzed using a combination of heparin–calcium precipitation and agar–agarose gel electrophoresis procedures[28]. The laboratory has been monitored for precision and accuracy of lipid measurements by the Lipid Standardization and Surveillance Plan of the Centers for Disease Control and Prevention, Atlanta, GA. A commercial radioimmunoassay kit was used for measuring plasma immunoreactive insulin levels (Pharmacia Diagnostics, Piscataway, NJ). Plasma glucose levels were measured as part of a multiple chemistry (SMA20) profile by a glucose oxidase method.

Carotid ultrasonography

Trained sonographers performed ultrasound examinations with a Toshiba Sonolayer SSH160A, a seven.5 MHz linear array transducer on subjects in the supine position with the head slightly extended and turned to the opposite management of the carotid artery beingness studied. Images were recorded at the mutual carotid, carotid seedling (bifurcation), and internal carotid arteries bilaterally co-ordinate to previously developed protocols for the Atherosclerosis Risk In Communities Study[29]. Images were recorded on S-VHS tapes and read by certified readers from the Division of Vascular Ultrasound Inquiry using a semiautomatic ultrasound image processing plan developed by the California Found of Technology Jet Propulsion Laboratory (Pasadena, California) according to strict protocols[29], [thirty]. The hateful of the maximum carotid IMT readings of three right and three left far walls for common, seedling and internal segments was used. Subjects who had missing values on both sides of whatsoever of the three sites were excluded from the electric current study.

Statistical methods

Information analyses were performed using SAS nine.3. CIMT was used as the outcome variable. Diagnostic criteria for components of metabolic syndrome from the updated NCEP ATP 3 guidelines[31] included: (i) intestinal obesity (waist circumference ≥102 cm for men and ≥88 cm for women), (ii) hypertriglyceridemia (fasting triglycerides≥150 mg/dl), (3) low HDL cholesterol (<40 mg/dl for men and <50 mg/dl for women, or taking cholesterol lowing mediction), (4) loftier blood pressure level (≥130/≥85 mmHg or taking antihypertensive medication), and (5) high fasting glucose (≥100 mg/dl or taking antidiabetic medication). CIMT, waist circumference, triglycerides, and insulin were log-transformed to improved normality before belittling comparisons. Chi-foursquare test was used to examine differences in proportions of dichotomous variables in different study groups. Full general linear models were used to examine the associations between risk factor variables and CIMT. To examine the interaction effects of cigarette smoking with age and metabolic syndrome, interaction terms between these variables were included in the model with the main terms included equally well in a single model. Later on significant interactions between historic period and smoking and between metabolic syndrome had been identified, nosotros performed stratified analyses by cigarette smoking status while adjusted for race, sex, leisure time concrete activeness, alcohol intake, LDL cholesterol, insulin, medications for blazon ii diabetes, hypertension, and high cholesterol, and metabolic syndrome or age, when appropriate. We also performed sensitivity analyses stratified by race and sex.

Results

Overall, 30.seven% (323/1051) of the participants were electric current smokers, and 20.7% (220/1051) had metabolic syndrome. Blacks vs. whites and females vs. males had favorable lipids levels; blacks vs. whites and males vs. females had higher claret pressure and fasting glucose levels and greater CIMT (Table 1).

Current smokers had lower BMI, smaller waist circumference and lower levels of fasting glucose and insulin than nonsmokers (Table 2). Despite being leaner and having improved insulin resistance, current smokers had greater CIMT than nonsmokers (least square hateful±SE: 0.853±0.009, 0.796±0.013 and 0.801±0.006 mm in electric current, former, and never smokers, respectively; p<0.0001, adapted for race, sex, leisure fourth dimension physical activity, alcohol intake, LDL cholesterol, insulin, medications for type 2 diabetes, hypertension, and high cholesterol, LDL cholesterol, insulin, and metabolic syndrome); however, there was no significant deviation in CIMT betwixt old and never smokers (p = 0.72). After like adjustment, historic period was significantly associated with CIMT, with an increase of 0.010±0.001 mm (β±SE) in CIMT each year (p<0.0001); metabolic syndrome remained significantly associated CIMT, with an increment of 0.062±0.014 mm in CIMT (p<0.001) for those with metabolic syndrome compared to those without.

Smoking significantly modified the associations between age and CIMT (p for interaction  =  0.03) and between metabolic syndrome and CIMT (p for interaction  =  0.001). Because there was no deviation in this modifying upshot between never smokers and former smokers (p for interaction with age  =  0.57 and p for interaction with metabolic syndrome  =  0.thirteen) and there was no significant divergence in CIMT betwixt never smokers and sometime smokers, nosotros combined former smokers and never smokers equally nonsmokers. As shown in Figure ane, age-related alter in CIMT was 0.008±0.001 mm/year in nonsmokers (p<0.0001) and 0.013±0.002 mm/year in current smokers (p<0.0001) (p for interaction = 0.005). In Figure two, the divergence in CIMT between those with metabolic syndrome and those without was significantly greater in smokers (0.973±0.026 vs. 0.818±0.012 mm; difference 0.154±0.030 mm, p<0.0001) than in nonsmokers (0.826±0.012 mm vs. 0.795±0.006 mm; difference 0.031±0.014 mm, p = 0.03) (p for interaction<0.0001). The observed interactions remained significant when we further adapted for internal diameter at diastole (p = 0.04 for interaction with age and p = 0.0002 for interaction with metabolic syndrome).

Figure 1. Scatter plot between age and carotid intima-media thickness (CIMT) in cigarette smokers and nonsmokers.

P value was adjusted for race, sex activity, leisure time physical action, alcohol intake, LDL cholesterol, insulin, medications for type 2 diabetes, hypertension, and high cholesterol, LDL cholesterol, insulin, and metabolic syndrome components.

https://doi.org/10.1371/periodical.pone.0096368.g001

Effigy 2. Carotid intima-media thickness (CIMT) past cigarette smoking status and metabolic syndrome.

Metabolic syndrome was defined according to the updated NCEP ATP Three guidelines[31]. P value was adjusted for race, sex, leisure fourth dimension concrete action, booze intake, LDL cholesterol, insulin, medications for type two diabetes, hypertension, and high cholesterol, LDL cholesterol, insulin, and metabolic syndrome components.

https://doi.org/10.1371/periodical.pone.0096368.g002

For race and sex stratified analyses, overall similar trends for interactions between age and cigarette smoking and between metabolic syndrome and cigarette smoking were observed as in the full sample, though the degree of significance of the interaction terms varied (p = 0.09 and p = 0.04 in white males; p = 0.94 and p = 0.007 in white females; p = 0.06 and p = 0.15 in black males; and p = 0.eighteen and p = 0.006 in black females, for interaction with age and for interaction with metabolic syndrome, respectively).

Give-and-take

In the current study, cigarette smokers had significantly higher CIMT than nonsmokers despite having lower BMI and waist circumference and improved insulin resistance. If CIMT represents vascular age for an individual, current smokers were about 6–seven years older than nonsmokers in terms of their respective vascular ages (0.052–0.057 mm departure in CIMT between current smokers and nonsmokers divided by age-related change 0.008 mm/year in nonsmokers). Further, cigarette smoking exacerbated the adverse effects of age and metabolic syndrome on CIMT and then that the influence of age and metabolic syndrome on CIMT was much stronger in electric current smokers than in nonsmokers. These findings from a customs-based sample emphasize the importance of prevention and cessation of cigarette smoking behavior in the young.

Current smokers have a smaller overall body size reflected in lower BMI and smaller waist circumference than nonsmokers. This is consistent with previous reports[32], [33]. Farther, smokers had lower levels of insulin and glucose than nonsmokers, independent of obesity measures such every bit BMI or waist circumference. The relationship between cigarette smoking and insulin resistance has not been consistent across studies. Henkin et al. did not find whatsoever association between active smoking and insulin sensitivity in the Insulin Resistance Atherosclerosis Study[34]. Similar findings were reported past Hughes et al.[35]. However, in a large prospective report, Cho et al. reported that smoking was an contained risk factor for type 2 diabetes, peculiarly among those with low insulin secretion and loftier insulin resistance at baseline[36]. Onat et al. found in a longitudinal study that smoking in males led to reduced insulin sensitivity and in females to increased insulin sensitivity[37]. The reasons for such disagreement amongst studies are not clear. Influences of a combination of some unaccounted for socioeconomic and/or lifestyle factors and potential biases may contribute to such discrepancies.

Despite being leaner and having improved insulin resistance, cigarette smokers had greater CIMT than nonsmokers, indicating that these cigarette smokers had increased atherosclerosis. Patently, the agin effects of cigarette smoking overtook the potential benefits, if whatever, of decreased obesity and low insulin resistance due to cigarette smoking. We have previously shown cigarette smokers accept lower small-scale avenue compliance and higher systemic vascular resistance than nonsmokers[38]. Our study is besides consequent with the findings from the Cardiovascular Risk in the Immature Finns study[39], [40] and from a Chinese study[ix]. In addition to its direct upshot on CIMT, cigarette smoking also strengthened the adverse effects of historic period and metabolic syndrome, 2 major determinants of atherosclerosis, on the vasculature. Historic period-related modify in CIMT in nonsmokers was only 0.008 mm, which increased to 0.013 mm in current smokers. Every bit a result, it can exist hands inferred that cigarette smokers not just have increased CIMT, merely also have accelerated vascular aging procedure, which at least partially explains why cigarette smokers have increased gamble for cardiovascular events. Further, the agin effect of metabolic syndrome on CIMT was vastly increased from 0.031 mm in nonsmokers to 0.154 mm in current smokers. Such departure emphasizes the synergistic effects betwixt cigarette smoking and metabolic syndrome and between cigarette smoking and age on the vasculature of the young.

Several mechanisms may explicate the increased burden of atherosclerosis in current cigarette smokers. Cigarette smoking is known to take a deleterious effect on endothelial cells and thus increased invasion of lipids particles and monocytes[15]. Secondly, cigarette smoking also increases inflammation, which is an important initiator and correspondent to atherosclerosis[xv]. Several inflammation markers, like C-reactive protein, interleukin-half-dozen, and tumor necrosis factor alpha, along with adhesion molecules may exist involved[15]. In addition, there are more than 4,000 known chemicals in cigarette smoke, many of which may have potential damaging effects on the vasculature[15]. Finally, age and metabolic syndrome are also linked to endothelial dysfunction, inflammation, and oxidative stress[41]. Deleterious effects by aging and metabolic syndrome may outset and maintain a vicious wheel that significantly accelerates atherosclerosis[41], [42]_ENREF_41, as seen in our study from a sample of relatively young adults. Our study suggests that this barbarous bike is strengthened by the adverse effects of cigarette smoking.

Results of our study strongly back up prevention of cigarette smoking behavior in young adults. As indicated past the greater CIMT among electric current smokers, cigarette smokers at an average age of 36.iv years already had increased atherosclerosis, which may be very hard to opposite. In addition, the agin effect of metabolic syndrome was less significant in nonsmokers. All these results contend for effective health educational activity programs to prevent cigarette smoking at a immature historic period. Moreover, results from our study as well emphasize the importance of smoking cessation on vascular health because cigarette smoking significantly accelerated the age-related change in CIMT. It is as well of import to target cigarette smokers with metabolic syndrome.

The current report has important strengths. Our study was community-based, which makes our results more generalizable to a larger population with a similar demographic limerick. In addition, data collection process followed a strict protocol with effective quality assurance/control measures. Finally, instruments to measure cigarette smoking and CIMT have been previously validated. On the other hand, our study was cross-sectional in nature. Potential confounding and selection bias might be nowadays. Nonetheless, since participants were not aware of their CIMT measurements, the observed associations were less likely to be distorted every bit a outcome of changed behavior or opposite causation. Notwithstanding, longitudinal studies are needed to further confirm the results in the current report. We too recognize that the usefulness and definition of metabolic syndrome remains controversial[43], [44]. The interaction betwixt cigarette smoking and metabolic syndrome may accept reflected interactions betwixt cigarette smoking and individual components of metabolic syndrome. Future studies should examine whether the interaction between cigarette smoking and metabolic syndrome is driven by interactions with certain private components of metabolic syndrome. Finally, information technology should be noted that nosotros used a composite value derived from measurements in different carotid sites. Due to unlike hemodynamic and anatomic properties in these sites, interactions observed in the current study may vary according to site, which warrants site-specific analysis in hereafter studies.

In decision, the current study demonstrates that cigarette smoking is associated with increased atherosclerosis as indicated by CIMT. Farther, cigarette smoking exacerbates the adverse effects of historic period and metabolic syndrome on the vasculature. Our results emphasize the importance of prevention and cessation of cigarette smoking behavior in the young. Futurity longitudinal studies are needed to confirm the current findings and to evaluate the effects of abeyance of cigarette smoking beliefs.

Acknowledgments

The Bogalusa Heart Study is a joint effort of many investigators and staff members whose contribution is gratefully best-selling. We particularly thank the participants, without whom the current written report would not have been possible.

Author Contributions

Conceived and designed the experiments: SL MY WC GSB. Performed the experiments: SL CF JX SRS WC GSB. Analyzed the data: SL WC CF MY. Wrote the paper: SL MY WC GSB.

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Source: https://journals.plos.org/plosone/article?id=10.1371/journal.pone.0096368

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