PEDIATRICS Vol. 121 No. 1 January 2008, pp. 115-122 (doi:10.1542/peds.2006-3720)
ARTICLE |
Relationships of Cardiovascular Phenotypes With Healthy Weight, at Risk of Overweight, and Overweight in US Youths
Georgia Prevention Institute, Department of Pediatrics, Medical College of Georgia, Augusta, Georgia
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ABSTRACT |
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OBJECTIVE. This study aimed to evaluate comprehensively the cardiovascular phenotypes of cardiovascular disease-free youths at risk of overweight, in comparison with healthy weight and overweight.
METHODS. Casual and ambulatory blood pressure measurements, noninvasive hemodynamic profiles, pulse wave velocity, left ventricular structure and function, and overnight sodium excretion were examined in a cohort of US black and white youths (n = 972; mean age: 17.6 ± 3.3 years).
RESULTS. The occurrence of at risk of overweight was 
17% in either black youths or white youths. In white youths, there was a 2-mmHg increase in casual systolic blood pressure for each increasing step in the 3 BMI categories (healthy weight, 109.5 ± 0.5 mmHg; at risk of overweight, 111.5 ± 0.6 mmHg; overweight, 113.5 ± 1.1 mmHg). Ambulatory systolic blood pressure showed a similar increase with the increase in BMI. A blunted nocturnal decline in ambulatory diastolic blood pressure with the categorical BMI increase was observed in black youths. In both racial groups, cardiac output and stroke volume were significantly enhanced sequentially from healthy weight to at risk of overweight to overweight. In black youths, both casual and ambulatory heart rate increased significantly with the increase in BMI. Moreover, there was a linear increase of left ventricular mass index from the healthy-weight group to the at risk of overweight group, with the overweight group having the highest value. In white youths, carotid-dorsalis pedis pulse wave velocity increased significantly as the BMI increased. Regardless of race, overnight sodium excretion showed a significant increase from healthy-weight subjects to overweight subjects, with at risk of overweight subjects having intermediate values.
CONCLUSIONS. Youths at risk of overweight, compared with healthy-weight youths, seem to have increased cardiovascular risks. Our data suggest that the status of at risk of overweight already has clinical implications in youths.
Key Words: at risk of overweight • youths • blood pressure • arterial stiffness • hemodynamics • left ventricular structure and function
Abbreviations: CDC—Centers for Disease Control and Prevention • BP—blood pressure • PWV—pulse wave velocity • SV—stroke volume • HR—heart rate • SBP—systolic blood pressure • DBP—diastolic blood pressure • LVM—left ventricular mass
Body fatness in adults is associated with a clustering of cardiovascular risk factors, including increased vascular tone, arterial stiffening, blood pressure (BP) elevation, and atherogenic vascular phenotypes.1–3 The significant increase in the prevalence of overweight youths in the past decades has been well recognized.4 BMI, irrespective of its limitations, is considered to provide a reliable indicator of body fatness.3 On the basis of the distribution approach, the US Centers for Disease Control and Prevention (CDC) recently designated a new term for BMI, namely, at risk of overweight. The BMI for individuals at risk of overweight falls between healthy weight and overweight, which includes >16% of the pediatric population 2 to 19 years of age.4
It is, however, still debatable whether this at risk of overweight category should be regarded as an arbitrary cutoff point or a precursor for cardiovascular consequences. Simply, is there a "dose-response" relationship in cardiovascular risks for the 3 BMI categories (healthy weight, at risk of overweight, and overweight)? It is well known that overweight in adults is associated with cardiovascular disease, hypertension, and type 2 diabetes mellitus.3 Similarly, data are required to show whether at risk of overweight status might predict elevated cardiovascular risk in cardiovascular disease-free young individuals. We think that a closer look at the antecedents of cardiovascular disease in youths with regard to such an important BMI category is warranted.
Therefore, this cross-sectional study aimed at comprehensively examining cardiovascular structure and function of the at risk of overweight status in a large cohort of black and white US youths living in the same environment and drawn from the Georgia Cardiovascular Twin Study. Twin studies provide an efficient research design for the study of genetic and environmental influences underlying complex traits. Many studies have shown that both quantitative and disease phenotypes for twins are similar to those of age-matched subjects from the general population.5,6 Therefore, twins are representative of singleton populations. In particular, research on twins has proved to be a valid epidemiologic tool for studying cardiovascular disease.5,6
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METHODS |
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Study Population
Subject recruitment was described previously.7,8 In brief, the twin pairs were recruited through announcements in local media and flyers distributed to public middle and high schools within 120 miles of the study location (Augusta, GA). Zygosity of all same-gender pairs was determined by DNA fingerprinting. Subjects were classified as black if (1) both parents reported being of African heritage or (2) parents considered themselves and their child to be black. Subjects were classified as white if (1) both parents reported being of European ancestry or (2) they considered themselves and their child to be white and not of Hispanic, Native American, or Asian descent. All subjects were apparently healthy, on the basis of parental reports of the child's medical history. Informed consent was provided by all subjects or their parents (if the subjects were <18 years of age). The institutional review board of the Medical College of Georgia approved the study.
Body weight, height, and waist circumference were evaluated by using established protocols.9 Triceps, subscapular, and suprailiac skinfold thicknesses were measured with a Lange skinfold caliper (Cambridge Scientific Products, Cambridge, MA), and the sum of the 3 skinfold measurements was computed.
Casual BP and Hemodynamic Measurements
The testing procedure was described previously.10 Hemodynamics and heart rate (HR) were measured by using a Dinamap 1846 SX monitor (Criticon, Tampa, FL). Measurements were taken at 11, 13, and 15 minutes during a 15-minute relaxation period in which subjects were instructed to relax as completely as possible while laying supine on a hospital bed, with their heads resting on a pillow. The averages of the 3 measurements were used to represent resting hemodynamic data. Stroke volume (SV), cardiac output, and total peripheral resistance were measured through bioimpedance cardiography (NCCOM-3; BoMeD Medical Manufacturing, Irvine, CA).
Ambulatory BP Measurements
The procedures for ambulatory BP recordings were described in detail previously.11 An ambulatory BP monitor (model 90207; SpaceLabs, Redmond, WA) was fitted to the nondominant arm. Measures were obtained every 20 minutes during the day (8 AM to 10 PM) and every 30 minutes during the night (midnight to 6 AM). Transitional periods from 6 AM to 8 AM and from 10 PM to midnight were not included in the analyses. Adequacy of recordings was based on acceptable readings, using previously established criteria,4 for 
14 readings over the 14 hours designated as daytime and 6 readings over the 6 hours designated as nighttime, as suggested by the European Society of Hypertension Working Group on Blood Pressure Monitoring.12
Pulse Wave Velocity Measurements
Carotid-radial (radial) pulse wave velocity (PWV) and carotid-dorsalis pedis (foot) PWV were measured noninvasively with applanation tonometry (Millar Instruments, Houston, TX)13 and commercially available acquisition and analysis software (SphygmoCor; AtCor Medical, Sydney, Australia). Pressure waves were recorded at the common carotid and radial arteries for the radial PWV and at the common carotid and dorsalis pedis arteries for the foot PWV. PWV was then calculated automatically from measurements of pulse transit time and the distance traveled by the pulse between the 2 recording sites (PWV = distance [in meters]/transit time [in seconds]).13
Echocardiographic Measurements
Two D-directed, M-mode echocardiograms were performed by using a Hewlett-Packard Sonos 1500 echocardiograph (Hewlett-Packard, Andover, MA). Left ventricular posterior wall thickness in diastole, interventricular septal thickness in diastole, and left ventricular internal dimension in diastole were measured according to the American Society of Echocardiography conventions.14 Left ventricular mass (LVM) was derived by using the formula described by Devereux et al,15 which has been validated for use in individuals with normal cardiac function. On the basis of the recommendation of de Simone et al,16 LVM was divided by height2.7 to adjust for normal growth (LVM index). Relative wall thickness = (left ventricular posterior wall thickness in diastole + interventricular septal thickness in diastole)/left ventricular internal dimension in diastole. Midwall fractional shortening and midwall fractional shortening ratio were calculated by using established formulas.9
Overnight Urinary Sodium Collection
Urine samples were collected from bedtime to time of awakening the next morning, for the measurement of overnight sodium excretion. Sodium concentrations were measured, in equivalents per milliliter, with the ion-selective electrode method by using a Nova 16 system (Nova Biomedical, Boston, MA). The overnight urinary sodium excretion rate was calculated as follows: urinary sodium excretion rate (in milliequivalents per hour) = sodium concentration x urine volume/1000 per hour.
Definitions of Healthy Weight, At Risk of Overweight, and Overweight
Anthropometric data were measured with standard methods and a Healthometer scale (Continental Scale, Chicago, IL), by trained observers. Height was measured with the subject standing without shoes and anything that might interfere with direct horizontal contact with the top of the head, and weight was measured with only light clothing. BMI was calculated as weight (in kilograms)/(height [in meters])2. For subjects <18 years of age, the exact BMI percentile was computed. According to the CDC growth charts (www.cdc.gov/nchs/about/major/nhanes/growthcharts/datafiles.htm), BMI of 5th percentile and <85th percentile was defined as healthy weight, BMI of 85th percentile and <95th percentile was defined as at risk of overweight, and BMI of 95th percentile was defined as overweight.17 For subjects 18 years of age, BMI of 18.5 kg/m2 and <25 kg/m2 was defined as healthy weight, BMI of 25 kg/m2 and <30 kg/m2 was defined as at risk of overweight, and BMI of 30 kg/m2 was defined as overweight.
Definitions of Prehypertension and Hypertension
For individuals <18 years of age, prehypertension was defined as an average BP of 90th percentile and systolic BP (SBP) or diastolic BP (DBP) of <95th percentile, according to age, gender, and height, or SBP was 120 mmHg and DBP was 80 mmHg; then hypertension was defined as an average BP of 95th percentile for SBP or DBP18 The height percentiles were determined from the standard height charts derived from the 2000 CDC growth charts.19 For individuals 18 years of age, according to the Seventh Report of the Joint National Committee on Prevention, Detection, Evaluation, and Treatment of High Blood Pressure, those with SBP of 120 to 139 mmHg and DBP of 80 to 89 mmHg were considered prehypertensive and those with SBP of 140 mmHg and DBP of 90 mmHg were considered hypertensive.20
Statistical Analyses
The statistical analyses were performed with Stata 8.0 software (Stata, College Station, TX). The gender ratios among healthy weight, at risk of overweight, and overweight were compared with a 
2 test for black youths and white youths separately. Values are presented as adjusted mean ± SE. Logarithmic transformation was performed to obtain an approximation of normal distribution when necessary. Ages among healthy weight, at risk of overweight, and overweight were compared with one-way analysis of variance. Differences in continuous variables among healthy weight, at risk of overweight, and overweight were compared with generalized estimating equations, a regression technique that allows for the relatedness within twins and yields unbiased SEs and P values.21 When the overall comparisons of phenotypes among the 3 BMI categories showed a significant difference, generalized estimating equation analysis was performed again, with the at risk of overweight group as the reference group. All analyses were adjusted for possible confounders, including age and gender. The differences among healthy weight, at risk of overweight, and overweight were compared for black youths and white youths separately. P < .05 was deemed statistically significant.
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RESULTS |
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Clinical Characteristics
Data for this study were available for 972 twins (44.6% black youths) from the Georgia Cardiovascular Twin Study, including 232 monozygotic and 254 dizygotic pairs of same-gender or opposite-gender twins (mean age: 17.6 ± 3.3 years). In total, 539 white (269 male and 270 female) and 433 black (193 male and 240 female), monozygotic or dizygotic twins were enrolled in the study. As shown in Table 1, the occurrence of at risk of overweight was consistent between black youths and white youths (17.1% vs 16.9%), but overweight was much more common in black youths than in white youths (22.6% vs 12.1%; P < .001). Of interest, among the subjects <18 years of age, there were more overweight black youths than overweight white youths (24.2% vs 9.2%), although the proportions at risk of overweight were similar between white youths and black youths (13.7% vs 13.4%). For both black youths and white youths, skinfold thicknesses of the 3 regions (triceps, subscapular, and suprailiac), the sum of the 3 skinfold measurements, and waist circumference increased significantly in parallel with the weight categories.
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Casual BP and Hemodynamic Profile
Table 2 shows that the presence of prehypertension and hypertension combined was more common among the at risk of overweight subjects than the healthy-weight subjects, among both black youths and white youths. In particular, in white youths, the rate of prehypertension showed a gradient increase with weight gain. In white youths, each increasing step in BMI category showed a
2-mmHg increase in casual SBP. In black youths only, DBP declined slightly with increasing BMI category. In either black youths or white youths, among the 3 BMI categories, SV and cardiac output increased with BMI gain, whereas total peripheral resistance decreased. In black youths, HR increased significantly with BMI increases. Gender was found to be a significant codeterminant for most of the hemodynamic phenotypes stratified according to the BMI categories.
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Ambulatory BP and HR
As shown in Table 3, in either white youths or black youths, 24-hour ambulatory SBP, ambulatory daytime SBP, and ambulatory nighttime SBP increased in the sequence of healthy weight to at risk of overweight to overweight, but results reached statistical significance only for white youths. In black youths, the 24-hour ambulatory DBP decreased significantly with increasing BMI category. The blunted decline of ambulatory DBP from daytime to nighttime ("dipping") with the increase in BMI was statistically significant for black youths. In both black youths and white youths, 24-hour ambulatory HR, daytime ambulatory HR, and nighttime ambulatory HR increased with the increase in BMI, although these trends reached statistical significance only for black youths. The gender effects are shown in Table 3.
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Overnight Urinary Sodium Excretion
As shown in Table 1, for both black youths and white youths, there was a linear increase in the overnight urinary sodium excretion with increasing BMI category.
Cardiovascular Structure and Function
In white youths, foot PWV increased significantly from healthy weight to overweight, with at risk of overweight showing an intermediate value as described in Table 4. In black youths, however, radial PWV decreased with BMI increases across the 3 BMI categories. In both black youths and white youths, interventricular septal thickness in diastole, left ventricular internal dimension in diastole, and left ventricular posterior wall thickness in diastole increased significantly with increases in BMI. The increase in relative wall thickness reached significance (P < .001) only for black youths. Regardless of race, the overweight group had the greatest value for LVM index, the healthy-weight group had the lowest value, and the at risk of overweight group had an intermediate value. In black youths, the midwall fractional shortening ratio decreased with BMI increases. The gender effects are included in Table 4.
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DISCUSSION |
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TOPABSTRACTMETHODSRESULTSDISCUSSIONREFERENCES |
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The present study provides additional evidence that young individuals at risk of overweight whose BMI is not within the optimal range but does not exceed the overweight threshold may posses elevated cardiovascular risks. In this twin cohort, the occurrence of at risk of overweight was
17% in either black youths or white youths, which is similar to the rate for Spanish schoolchildren (16%)22 but less than the rate for American Indian adolescents (25%).23 Furthermore, overweight was twice as common in black youths as in white youths. From healthy weight to at risk of overweight to overweight, there was an obvious gradient growth in waist circumference and triceps, subscapular, and suprailiac skinfold thicknesses, indicating that young individuals at risk of overweight have greater than optimal fatness and adipose tissue accumulation. In particular, waist circumference has been advocated as an indicator of abdominal fat content. Increased waist circumference, in combination with or independent of BMI, may predict cardiovascular risk factors among youths at risk of overweight.24,25 In either black youths or white youths, the occurrence of prehypertension and hypertension combined increased with the increase in BMI category. In white youths, the rate of prehypertension alone was significantly higher for the at risk of overweight group than the healthy-weight group, demonstrating that higher than optimal weight is associated with higher than optimal BP. A 2-mmHg BP increase may not be of clinical significance at the individual level, but it has a significant impact on a population level, especially in the pediatric population. BP elevation tracks from late childhood into adulthood and follows a relatively consistent progression. BP elevation early in life places a cumulative burden on the cardiovascular system.26,27 Ambulatory BP measurements offer advantages over casual BP readings, such as tracking of circadian BP patterns.12 More specifically, only a few studies have addressed the impact of weight gain on ambulatory BP levels in youths.28 Our data for youths showed that ambulatory daytime SBP and nighttime SBP increased in step with the weight categories. These findings support the concept that the risk for essential hypertension can be attributed directly to excess weight in older adults.29 In particular, in white youths, both ambulatory daytime SBP and nighttime SBP were significantly greater in the at risk of overweight subjects than in the healthy-weight subjects, indicating that early weight gain contributes to BP elevation.
Alexander et al30 characterized overweight as a state in which elevated blood volume, enlarged vascular tree, and increased cardiac output were all thought necessary to sustain the demands of an expanded adipose tissue mass. In the present study, SV and cardiac output were increased in the at risk of overweight youths, especially black youths, which suggests that the high-output state may already be present in the early stage of weight gain. Excess adipose tissue generates an increase in oxygen consumption and subsequently requires an increase in cardiac output.3 Total peripheral resistance was, however, decreased with BMI increases according to the categories. This finding was in accordance with previous reports in overweight hypertensive adults31 and might be a result of compensatory widening of the vascular tree. The absolute lowering of systemic resistance could be inadequate in the presence of increased demands for circulating volume. The elevation of cardiac output was previously considered to be related primarily to increases in SV rather than HR.32 In this study, casual HR and 24-hour HR (including daytime and nighttime) also increased with the categorical weight increase, although the increases were statistically significant only for black youths. The acceleration of HR together with the elevation of SV contributes to the increase in cardiac output. One explanation for the HR increase is that the demands of excess adipose tissue might have exceeded the compensatory capacity of SV alone. HR acceleration can also be a sign of sympathetic hyperactivity, which is the common feature of overweight in humans and in animal models.33 Furthermore, increased HR variability was found previously in overweight adolescents, which suggests an altered balance between sympathetic and parasympathetic activity in relation to excess weight gain.34
Among both black youths and white youths, subjects at risk of overweight showed increased LVM, lower left ventricular contractility, and lower vascular compliance, compared with healthy-weight individuals. This observation is in accordance with findings from the Strong Heart Study, in which unfavorable alterations in cardiac geometric features and function were shown for 460 American Indian adolescents.23 In white youths, we observed a "staircase" increase of foot PWV across the 3 BMI categories, which suggests increased stiffness of the arterial wall with increases in weight status.
Of interest, overnight urinary sodium excretion, which might reflect dietary salt intake, exhibited a significant "dose-response" increase in association with the categorical BMI increase in both race groups. The Intersalt Study demonstrated that overweight adult individuals usually ate more food than healthy-weight adults; along with greater food intake, they also ingested more sodium.35 Salt loading leads to extracellular volume expansion, high cardiac output, and BP elevation and contributes to cardiac hypertrophy. In addition, weight gain is associated with salt sensitivity, contributing to the hyperdynamic circulation and cardiac load through the renin-angiotensin-aldosterone system, sympathetic nervous system, and intrarenal physical forces.29,34,36 Ideally, the results need to be confirmed in an independent cohort with 24-hour urinary sodium excretion measurements, which are more-accurate measures of dietary salt intake. The effects of at risk of overweight on the relationship between nocturnal sodium excretion and BP deserves further investigation.37
There were 2 observations contrary to our hypotheses. First, casual DBP and 24-hour ambulatory DBP were decreased with the categorical BMI increase, especially in black youths. However, this is in line with a few previous findings in the literature. For instance, the 1999 to 2002 National Health and Nutrition Examination Survey demonstrated that lower DBP was associated with higher BMI in 4508 adolescents 12 to 19 years of age.38 In the present study, a blunted nocturnal decline in ambulatory DBP with the categorical BMI increase was observed, especially in black youths. It is known that individuals with a blunted nocturnal decline in BP, referred to as "nondippers," display the highest cardiovascular risk, because such individuals are exposed to a greater cardiovascular load each day.39 Second, radial PWV was unchanged with the BMI increase in white youths and decreased significantly with the BMI increase in black youths. We found previously that DBP was the most important hemodynamic predictor for PWV; the variance explained by the DBP model alone approached that for the full model for PWV.40 Because DBP was correlated negatively with the BMI categories, the inverse correlation between radial PWV and the BMI categories should not be unexpected.
There were limitations of the present study. First, the use of the dorsalis pedis as an alternative to the femoral measurement site was considered less sensitive, although more readily accepted by youths. Foot PWV represents a mixture of both proximal elastic arteries and distal muscular arteries. Some differences with other reports, which typically measured carotid-femoral PWV, are thus expected. However, the previous findings revealed that foot PWV, as a combination of central and peripheral measures, was correlated more strongly with age than was radial PWV.40 This is quite comparable to the characteristic of carotid-femoral PWV. In addition, the genetic influences on foot PWV and radial PWV differed significantly.40 Second, there is concern about the accuracy of hemodynamic assessments, such as cardiac output measurements, with impedance cardiography. Nevertheless, this technique is noninvasive and feasible for large population studies. Third, there may be concerns regarding whether results from twin studies can be generalized to the general population. We and others demonstrated previously that twins are representative of singleton populations, and studies of twins are valid epidemiologic tools for common diseases such as hypertension.5,6 Fourth, this study is limited by the cross-sectional design. Longitudinal follow-up monitoring would indicate the dynamic changes in cardiovascular structure and function caused by at risk of overweight status. Lastly, there are limitations in the CDC definitions of BMI and BP cutoff values. For example, ethnic/racial differences in the development of body size and height in adolescents were not included. Therefore, caution should be used in generalizing our results with US youths to other adolescent populations.
Although there is a continuum of cardiovascular risk across levels of BMI, our data suggest that a simple BMI threshold, that is, at risk of overweight, already has clinical implications in youths. This study suggests strongly that a variety of adaptations and alterations in cardiovascular structure and function are associated with this higher than optimal weight status. Furthermore, the likelihood of clustering of cardiovascular risk factors is enhanced in cardiovascular disease-free young individuals at risk of overweight. Optimal approaches to effective preventive strategies in youths should include early recognition, dietary intervention, stress reduction, prevention of weight gain, weight loss, and physical activity.
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ACKNOWLEDGMENTS |
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This study was supported by grants from the National Heart, Lung, and Blood Institute (HL56622, HL76723, HL77230, HL85817 and HL69999) and the American Heart Association (0430078N and 0435146N).
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FOOTNOTES |
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Accepted Jun 26, 2007.
Address correspondence to Yanbin Dong, MD, PhD, Georgia Prevention Institute, Department of Pediatrics, Medical College of Georgia, Building HS-1640, Augusta, GA 30912-3715. E-mail: ydong{at}mcg.edu
The authors have indicated they have no financial relationships relevant to this article to disclose.
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  E. Velkoska, T. J. Cole, R. G. Dean, L. M. Burrell, and M. J. Morris Early Undernutrition Leads to Long-Lasting Reductions in Body Weight and Adiposity Whereas Increased Intake Increases Cardiac Fibrosis in Male Rats J. Nutr., September 1, 2008; 138(9): 1622 - 1627. [Abstract] [Full Text] [PDF]
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