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(Circulation. 1995;91:1101-1106.)
© 1995 American Heart Association, Inc.

Articles

Hyperdynamic Circulation and Cardiovascular Risk in Children and Adolescents

The Bogalusa Heart Study

Xiaozhang Jiang, MD, MPH; Sathanur R. Srinivasan, PhD; Elaine Urbina, MD; Gerald S. Berenson, MD

From the Tulane Center for Cardiovascular Health, School of Public Health & Tropical Medicine, Tulane University Medical Center, New Orleans, La.

	Abstract

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Background Hyperdynamic circulation has been reported to be associated with adverse levels of insulin, blood pressure, adiposity, and lipoproteins in the adult population. Whether this putatively insulin-mediated association also occurs in early life is not known. This aspect was examined in 2229 children and adolescents 8 to 17 years old living in Bogalusa, La.

Methods and Results Individuals were categorized as hyperdynamic (pulse pressure and heart rate in the upper quartile of the race-sex-age distribution), intermediate, and hypodynamic (pulse pressure and heart rate in the bottom quartile). Systolic blood pressure was significantly greater with a hyperdynamic circulation in both sexes (P<.0001), and several measures of obesity were greater with a hyperdynamic circulation. Hyperdynamic circulation was associated with statistically significant increases in triglyceride (P<.05) and fasting insulin (P<.01) in boys independently of age, race, and obesity. A decreasing trend with HDL cholesterol (P=.06) was also observed in boys. A significant association with total cholesterol (P<.05) was observed only in girls. In the analysis stratified by percent body fat, many of these features still occurred in obese individuals (top quartile) but not in lean individuals (bottom quartile). Further, when a subset of this cohort (n=1074) was followed over a 3-year period, the above trend persisted significantly in boys.

Conclusions The present study demonstrates that a hyperdynamic state as defined is associated with increased insulin levels and an adverse cardiovascular risk in early life.

Key Words: hemodynamics • insulin • risk factors • syndrome X

	Introduction

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Insulin resistance/hyperinsulinemia has been shown to be related to the risk of developing hypertension, obesity, and dyslipidemia, common cardiovascular risk factors in adults.^{1 2 3 4} Insulin resistance has been proposed to be a potential metabolic defect that underlies a constellation of these conditions known as syndrome X,⁵ deadly quartet,⁶ and insulin resistance syndrome.⁷ Recently, Stern and colleagues⁸ showed that a hyperdynamic circulation in the adult population is associated with increased levels of fasting and postglucose insulin, systolic blood pressure, triglycerides, and body fatness. Accordingly, these authors postulated that an insulin-induced hyperdynamic circulation is an early feature of an insulin resistance syndrome. Whether this association also occurs in early life is not known.

A number of studies have shown that insulin induces increases in cardiac output, cardiac contractility, and heart rate in experimental animals and humans.^{9 10 11 12} In addition, an independent relation between insulin and blood pressure has been demonstrated in children^{13 14} and adults.^{15 16} Thus, it has been theorized that an insulin-induced hyperdynamic circulation manifested by a widened pulse pressure and tachycardia might represent an early feature of the insulin resistance syndrome.⁸

In previous cross-sectional and prospective studies, we have observed the coexistence of cardiovascular risk factor variables related to syndrome X and their persistence in children and young adults.^{17 18 19} The present study examines the association between hemodynamic aspects of the circulation and cardiovascular risk related to the insulin resistance syndrome in children and adolescents from a biracial community.

	Methods

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Population Sample
The Bogalusa Heart Study is a biracial (two-thirds white and one-third black) community-based investigation of the early natural history of cardiovascular disease. The study population consists of all children and young adults living in Ward 4, with Bogalusa, La, as the main community (total population, 22 000). Since 1973, the population has been examined through repeated cross-sectional surveys with participation rates ranging between 80% and 93%. The design and methods of the Bogalusa Heart Study have been described in detail elsewhere.²⁰

During the 1984-1985 school year, a cross-sectional survey of 2559 children and adolescents 8 to 17 years old was conducted. Of these, 2231 participants had fasting insulin analysis. Three individuals who were pregnant were excluded from the analyses, resulting in a study population of 2229. Subsequently, during the year 1987-1988, the next cross-sectional survey of school children was conducted in Bogalusa. In all, 1074 individuals participated in both surveys, and their data were used for prospective analyses.

General Examinations
Essentially, all cross-sectional surveys were conducted under the same protocols.²⁰ Informed consent was obtained before each screening. All participants were instructed to fast for 12 to 14 hours before venipuncture. The last food intake was assessed by interview on the morning of the examination. Anthropometric measurements included height, which was measured to ±0.1 cm, and weight, to ±0.1 kg. Subscapular and triceps skinfold thicknesses were measured to ±1 mm with Lange skinfold calipers. Since considerable age-related variations in the level of body fat at a given skinfold percentile are noted among children and adolescents, percent body fat was computed using the sum of subscapular and triceps skinfolds in an equation developed specifically for children.²¹ Rohrer index (RI) (weight divided by the cube of height) was also used as an index of overall adiposity.

Replicate blood pressure measurements were obtained on the right arm of subjects in a relaxed, sitting position. Arm measurements (length and circumference) were made according to protocols to ensure proper cuff size for blood pressure determination. Systolic and diastolic blood pressures were recorded as the first and fourth Korotkoff phases, respectively. The mean of six readings taken by two randomly assigned trained nurses was defined as the individual's blood pressure. Pulse pressure represents the difference between the first and fourth phases. Pulse rate was counted for 30 seconds by trained examiners. After a 10-second wait, pulse measurements were repeated for another 30-second period. The mean of two pulse readings was used as the individual's pulse rate. In the second survey, after 3 years, each participant's pulse rate was counted for 60 seconds by a Dinamap instrument (model 845XT, Critikon Inc), and the reading was obtained from the digital display.

Laboratory Analyses
Concentrations of serum total cholesterol and triglycerides were determined in a Technicon Auto-Analyzer II (Technicon Corp) according to the laboratory manual of the Lipid Research Clinics program.²² The laboratory has been standardized by the Centers for Disease Control in Atlanta, Ga, and is being monitored by a surveillance program. Serum VLDL cholesterol, LDL cholesterol, and HDL cholesterol were analyzed by a combination of heparin-calcium precipitation and agar-agarose gel electrophoresis procedures.²³

Plasma glucose was measured with a Beckman glucose analyzer by a glucose oxidase method. Plasma insulin determinations were performed by a radioimmunoassay procedure with the Phadebas Insulin Kit (Pharmacia Diagnostics AB).²⁴

Statistical Analysis
All analyses were performed with the SAS program.²⁵ Children were categorized into three groups on the basis of their pulse rate and pulse pressure as described by Stern et al⁸ : hyperdynamic, intermediate, and hypodynamic. All individuals were divided into quartiles according to their pulse rate and pulse pressure by age groups (2-year intervals), race, and sex. Hyperdynamic individuals were defined as individuals who had the uppermost 25% of both pulse rate and pulse pressure distributions. Hypodynamic individuals were defined as individuals who had the lowest 25% of both pulse rate and pulse pressure distribution. Intermediate individuals were defined as individuals whose pulse rate and pulse pressure were both within 25% to 75% of respective distributions. Individuals who did not fall into these three categories were excluded from the present analysis.

Since no significant interaction was observed between racial groups and hemodynamic status, both racial groups were pooled for analysis. Moreover, the racial distribution was nearly similar in the three hemodynamic categories. Mean levels of study variables were obtained on each category group. Due to their skewed distributions, fasting insulin and triglyceride values were logarithmically transformed in the analyses. Multiple linear regression analyses were performed to examine the trend of selected variables across three hemodynamic categories after adjustment for age, age squared, age cubed, and race or percent body fat. In the analysis, hemodynamic status was treated as an interval level variable: (1) was coded for hypodynamic, (2) for intermediate, and (3) for hyperdynamic. The effect of hemodynamic circulation was also examined after all subjects were categorized as lean (<25th percentile of percent body fat) or obese (>75th percentile of percent body fat) individuals according to age-specific (2-year interval), race-specific, and sex-specific percentiles of percent body fat. A ² test was used to determine whether the percentages of subjects in the fifth quintile for selected variables (the first quintile was used for HDL cholesterol) were significantly different from those expected by chance alone at each level of hemodynamic state.

Similar analyses were performed on a subset of the longitudinal cohort to determine whether or not those who remained hyperdynamic at baseline continue to show adverse cardiovascular risk at follow-up (3 years).

	Results

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The distributions of individuals falling into a hemodynamic status by race and sex are presented in Table 1. The racial distributions of hyperdynamic individuals were nearly similar. The relation between body fat and hyperdynamic circulation is presented in Table 2. Several measures of obesity were all significantly greater with hyperdynamic circulation in boys. Moreover, hyperdynamic children had greater central obesity.

View this table: [in this window] [in a new window]   Table 1. Distribution of Hemodynamic Status in Children and Adolescents, by Race and Sex

View this table: [in this window] [in a new window]   Table 2. Mean Levels of Anthropometric, Pulse Rate, and Pulse Pressure Variables According to Hemodynamic Status and Sex of Children and Adolescents 8 to 17 Years Old

Table 3 compares mean levels of study variables by hemodynamic status in boys and girls. In general, most of the study variables showed a trend toward higher values, except diastolic blood pressure and HDL cholesterol (in boys), which showed an opposite trend across the three categories. After adjustment for age, race, and percent body fat, systolic blood pressure rose significantly in both sexes with a hyperdynamic circulation. A significant sex difference was observed in relation to lipoprotein variables and insulin. Fasting insulin and triglycerides were all increased significantly with a hyperdynamic circulation in boys. A decreasing trend with HDL cholesterol (P=.06) was also observed only in boys. However, no significant trend was observed in girls, with the exception of a positive trend for total cholesterol. Fasting glucose levels showed no trend with hemodynamic status.

View this table: [in this window] [in a new window]   Table 3. Mean Levels of Study Variables According to Hemodynamic Status and Sex of Children and Adolescents 8 to 17 Years Old

Table 4 shows trends with hemodynamic status in lean boys (<25th percentiles of body fat) versus obese boys (>75th percentiles of body fat). Although the significant trends with blood pressure were still present in both lean and obese groups, the association of hyperdynamic circulation with lipoprotein variables and insulin was not statistically significant in the lean group. In contrast, a significant trend with hyperdynamic circulation persisted in the obese group. The corresponding analyses for girls are presented in Table 5. Pulse rate, pulse pressure, and blood pressure showed significant trends with hemodynamic status in both groups. Total cholesterol levels tend to increase with a more hyperdynamic circulation in the obese group. A similar observation was found when this analysis was repeated with the Rohrer index (data not shown).

View this table: [in this window] [in a new window]   Table 4. Mean Levels of Study Variables According to Low or High Percentage of Body Fat and Hemodynamic Status in Boys 8 to 17 Years Old

View this table: [in this window] [in a new window]   Table 5. Mean Levels of Study Variables According to Low or High Percentage of Body Fat and Hemodynamic Status in Girls

In studies of the bivariate relations between hemodynamic status and selected cardiovascular risk factor variables, the percentage of hyperdynamic subjects in the uppermost quintile for triglycerides, insulin, and percent body fat was significantly greater than that expected by chance alone (20%) in boys and for LDL cholesterol and percent body fat in girls (data not shown).

The effect of baseline hemodynamic status on cardiovascular risk factor variables followed over a 3-year period in a subset is presented in Table 6. Follow-up levels of percent body fat, Rohrer index, HDL cholesterol, triglycerides, and insulin continued to show significant trends with baseline hemodynamic status in boys. In girls, these trends, although in the expected directions, did not reach significance, except for triglycerides.

View this table: [in this window] [in a new window]   Table 6. Effect of Baseline Hemodynamic Status on Study Variables After 3-Year Follow-Up

	Discussion

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The present community-based study made on free-living, presumably healthy, children and adolescents shows that individuals with a hyperdynamic circulation tend to display increasing levels of body fatness, insulin, systolic blood pressure, and triglycerides and decreasing HDL cholesterol. Longitudinal analyses on a subset showed persistence of these trends over a 3-year period. These observations confirm previous studies made in adults⁸ but extend the observations to childhood and adolescence.

Plasma insulin has been demonstrated to play multiple and important roles in the cardiovascular system. Insulin infusions have been shown to increase cardiac output, cardiac contractility, and heart rate in experimental animals and humans.^{9 10 11 12} Possible physiological mechanisms include stimulation of the sympathetic nervous system, resulting in increases in norepinephrine release²⁶ and enhanced renal tubular sodium reabsorption,²⁷ followed by an increase in extracellular volume and cardiac output²⁸ and induction of vascular smooth-muscle cell hypertrophy.²⁹

Insulin resistance has been suggested to be the underlying factor linking compensatory hyperinsulinemia, glucose intolerance, dyslipidemia, and hypertension.⁵ The present observations suggest that a hyperdynamic state reflects early manifestations of the insulin resistance syndrome, or syndrome X. Since obesity is an important component of this syndrome, further analyses were performed to note the association between percent body fat and a hyperdynamic circulation. As might be expected, cardiovascular risk factor variables related to insulin resistance significantly in the obese group but not in the lean group. Since clustering of obesity, hypertension, dyslipidemia, and disturbances in carbohydrate metabolism are often found in the same individual, insulin resistance or hyperinsulinemia may enhance these associations. Voors et al³⁰ observed in Bogalusa children that various measures of obesity were also highly related to an insulin response after a glucose load. Moreover, the strong relation of central fat to insulin response was noted in Bogalusa children.³¹ Smoak et al¹⁷ examined the relation of obesity, especially subscapular skinfolds in contrast to triceps (peripheral) skinfolds, to clustering of systolic blood pressure, fasting insulin, and lipoprotein changes in children, indicating that centrally obese subjects had greater clustering than expected compared with lean subjects. The present study also found a strong association between a hyperdynamic circulation and central obesity. Insulin sensitivity shows a strongly inverse correlation with the degree of obesity; also, decreased insulin sensitivity occurs in obese, hypertensive individuals.³² These observations suggest that a decreased insulin sensitivity, even in asymptomatic obese individuals, may underlie the clustering. Obesity generated from various causes probably underlies this clustering as well.

Although the association between hyperdynamic circulation and many features of insulin resistance syndrome was in the expected direction in both boys and girls, the relation was significant only among boys. The difference may reflect physiological and hormonal interactions occurring within the two sex groups during pubertal development. Previous studies in adults have shown significant relations in both men and women.⁸

Some prospective population studies have found that a rapid heart rate is a risk factor for future hypertension. Hypertensive individuals with a hyperdynamic status often display high cardiac output, low peripheral resistance, and rapid heart rate.^{33 34} Lund-Johansen³⁴ described a transition from high cardiac output to elevated vascular resistance in early borderline hypertensive patients with hyperdynamic circulation. Young et al³⁵ showed catecholamine excretion related to body size and obesity, implicating diet and insulin secretion as affecting cardiovascular dynamics. Also, Stern et al⁸ found that hyperdynamic circulation was a strong predictor of type II diabetes in an 8-year follow-up study. Our longitudinal analyses of hyperdynamic individuals showed a tendency to have higher levels of systolic blood pressure, triglyceride, VLDL cholesterol, insulin, increasing percent body fat, and decreased HDL cholesterol levels over a 3-year period. These observations indicate that hyperdynamic children not only display an early form of insulin resistance but also tend to continually maintain many features of the insulin resistance syndrome. Continuation of such clustering with persistence of hemodynamic features could be a marker for high cardiovascular risk and premature cardiovascular events.

These observations reinforce the concept that hyperdynamic circulation is an early feature of insulin resistance syndrome. It is of interest that high systolic blood pressure carried a high cardiovascular risk in the Framingham Study. In the present study of children and adolescents, if a wide pulse pressure was selected, high systolic pressure coupled with low diastolic pressure ensued. It is likely that this trend persists into adulthood, when an increased vascular rigidity develops with aging and accounts for systolic hypertension. The observed association between a hyperdynamic status and other cardiovascular risk factors in childhood and adolescence has implications for prevention, particularly for instituting measures such as weight control, exercise, and a prudent diet.

	Acknowledgments

 
This continuing research is supported by funds from the National Heart, Lung, and Blood Institute of the US Public Health Service, grant HL-38844.

	Footnotes

 
Reprint requests to Gerald S. Berenson, MD, Tulane Center for Cardiovascular Health, Tulane University School of Public Health & Tropical Medicine, 1501 Canal St, 14th Floor, New Orleans, LA 70112-2824.

Received June 14, 1994; accepted October 5, 1994.

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This Article Abstract Alert me when this article is cited Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Request Permissions Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Jiang, X. Articles by Berenson, G. S. Search for Related Content PubMed PubMed Citation Articles by Jiang, X. Articles by Berenson, G. S. Pubmed/NCBI databases Compound via MeSH Substance via MeSH