The Journal of Pediatrics
Volume 150, Issue 3 , Pages 247-251, March 2007

Association between Brachial-Ankle Pulse Wave Velocity and Cardiovascular Risk Factors in Healthy Adolescents

Department of Laboratory Medicine, MizMedi Hospital, Gangseo-Gu, Seoul, Korea; and Department of Family Medicine, Yonsei University, College of Medicine, Yongdong Severance Hospital, Seoul, Korea.

Received 31 March 2006; received in revised form 16 September 2006; accepted 8 November 2006.

Article Outline

Objective

To investigate the associations between cardiovascular risk factors and arterial stiffness, measured as brachial-ankle pulse wave velocity (baPWV), in healthy adolescents.

Study design

In this cross-sectional study, 178 male and 84 female adolescents, aged 12 to 18 years, were recruited. Total homocysteine levels, serum lipid profiles, high-sensitivity C-reactive protein (hs-CRP) levels, fasting glucose levels, fasting insulin levels, and baPWV were measured.

Results

baPWV was significantly higher in male adolescents than in female adolescents. In both sex groups, baPWV was positively correlated with body mass index (BMI), waist circumference, waist-hip ratio, systolic and diastolic blood pressures, fasting insulin levels, homeostatic model assessment of insulin resistance, triglyceride levels, hs-CRP levels, and total homocysteine levels. In male adolescents, age, total cholesterol level, low-density lipoprotein cholesterol levels, and white blood cell counts were positively correlated with baPWV, and, in female adolescents, high-density lipoprotein cholesterol levels were negatively correlated with baPWV. In multivariate analysis, sex, mean blood pressure, BMI, and total homocysteine levels were found to be independent factors associated with baPWV.

Conclusion

Blood pressure, BMI, sex, and total homocysteine levels were independently associated with arterial stiffness, measured as baPWV, in healthy adolescents, suggesting that these risk factors may be associated with an increased risk of atherosclerosis in adolescents.

Abbreviations: baPWV, Brachial-ankle pulse wave velocity, BMI, Body mass index, CV, Cardiovascular, HDL-C, High-density lipoprotein cholesterol, HOMA-IR, Homeostatic model assessment of insulin resistance, hs-CRP, High-sensitivity C-reactive protein, IMT, Intima-media thickness, LDL-C, Low-density lipoprotein cholesterol, PWV, Pulse wave velocity, WHR, Waist-hip ratio

 

Although the clinical end-point of atherosclerosis mainly occurs in middle age or later in life, observations in pathology studies revealed that atherosclerotic lesions begin during childhood.1, 2 In addition, some of the traditional cardiovascular (CV) risk factors, which include hypercholesterolemia, hypertension, cigarette smoking, and obesity, may have an association with the development of atherosclerosis in adolescents or young adults.3, 4, 5 Recent studies have consistently shown that CV risk factors identified in childhood predict the carotid intima-media thickness (IMT) in adulthood.6, 7, 8 These observations suggest that early detection of modifiable CV risk factors in this population may have an impact on health in later life.

See editorial, p 219

Hyperhomocysteinemia may affect small vessels with time, beginning in childhood.9 Several studies have reported that the total homocysteine level has an association with atherosclerotic risk factors in groups of children with obesity,10 stroke,11 familial hypercholesterolemia,12 or arterial hypertension with type1 diabetes mellitus.13 However, it is unclear whether the total homocysteine level is associated with preclinical atherosclerosis in a healthy population.14, 15, 16

Increasing arterial stiffness is one of the pathological symptoms of vascular damage and is closely associated with atherosclerotic cardiovascular diseases.17 Pulse wave velocity (PWV) is known to be an indicator of arterial stiffness18 and a marker of vascular damage.19 The aim of this study was to determine the associations between arterial stiffness, measured as brachial-ankle pulse wave velocity (baPWV), and total homocysteine levels and other cardiovascular risk factors in apparently healthy adolescents.

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Methods 

All participants signed a consent form approved by the ethics committee of Yong-dong Severance Hospital (Seoul, Korea). Healthy volunteers were recruited from junior high schools or high schools via a public advertisement. A total of 178 male adolescents and 84 female adolescents, 12 to 18 years old, were surveyed for this study. Exclusion criteria included a medical history or evidence with physical examination of cardiovascular disease, diabetes mellitus, hypertension (resting blood pressure >140/90 mm Hg), a body weight fluctuation >5 kg in the previous 6 months, endocrine disorders, or medication that could affect cardiovascular function or metabolism. Participants completed a questionnaire to assess past and current medical illnesses and lifestyle choices such as alcohol ingestion and cigarette smoking. Alcohol ingestion was defined as the ingestion of alcohol >1 time per week. Smoking was defined as current cigarette smoking.

Anthropometric measurements were taken with the participants in light clothing and without shoes. Height to the nearest 0.1 cm and weight to the nearest 0.1 kg were measured with an automatic height-weight scale. Body mass index (BMI) was calculated as the participants’ weight divided by their height squared. Waist circumference was measured at the midpoint between the lower border of the rib cage and the iliac crest. Hip circumference was measured at the widest part of the hip region, and thigh circumference was measured 10 cm proximal to the superior patella border. To reduce variation in measurements, 1 person measured all anthropometric parameters throughout the study.

baPWV was measured with a volume-plethysmographic apparatus (PWV/ABI, Colin Co., Komaki, Japan) as previously described.20, 21 This device simultaneously records the phonocardiogram, electrocardiogram, volume waveform, and arterial blood pressure at both the left and right brachia and ankles. Subjects were examined in the supine position. Electrodes were placed on both wrists to obtain an electrocardiogram. A microphone for a phonocardiogram was placed on the left margin of sternum to detect heart sounds. Occlusion cuffs, which were connected to a plethysmorgraphic sensor that determined the pulse volume waveform and an oscillometric pressure sensor that measured blood pressure on each extremity, were applied to both arms and ankles of subjects. The time interval between arm and ankle (ΔTa) was defined by the pulse transit time between the brachial and tibial arterial pressure waveforms. The distance between the right arm and ankle was estimated automatically on the basis of the subject’s height.22 The distance from suprasternal notch to elbow (ΔDa) and from suprasternal notch to ankle (ΔDb) were expressed with this equation:

and
The baPWV was calculated with this equation:
An earlier study reported that in healthy subjects, the coefficient of variation for interobserver reproducibility (n = 15) was 2.4%, and intraobserver reproducibility (n = 17) was 5.8%.21 Because there was a significant correlation between the right PWV and left PWV (r = 0.90, P < .001), the mean PWV value was used for analysis.23

After an 8-hour overnight fast, blood samples were obtained from each participant from an antecubital vein and placed into a plain and an EDTA tube. The total homocysteine level was measured with a competitive immunoassay using an Immulite 2000 (DPC, Pacific Concourse, LA), and the inter- and intra-assay variations were 6.8% ± 2.8% and 4.9% ± 1.7%, respectively. Levels of high sensitivity C-reactive protein (hs-CRP), fasting glucose, total cholesterol, triglycerides, and high-density lipoprotein cholesterol (HDL-C) were measured with an ADVIA 1650 Chemistry system (Bayer, Tarrytown, NY), and levels of low-density lipoprotein cholesterol (LDL-C) were calculated from the Friedewald equation.24 Fasting insulin levels were measured with an electrochemiluminescence immunoassay (Roche, Indianapolis, IN). Insulin resistance was estimated with the homeostatic model assessment of insulin resistance (HOMA-IR); the calculations were:

White blood cell (WBC) counts were assayed with an ADVIA 2120 Hematology System (Bayer, Tarrytown, NY). Data are expressed as means ± SD. Variables such as baPWV, hs-CRP levels, total homocysteine levels, triglyceride levels, fasting insulin levels, and HOMA-IR were logarithmically transformed before statistical analysis to improve normality. Clinical and metabolic characteristics between sexes of the study population were compared with the t test for continuous variables and the chi-square (χ2) test or Fisher exact test for categorical variables. Pearson (for continuous variables) or Spearman rank (for categorical variables) correlation analyses were used to assess the relationship of baPWV to clinical variables by sex. To determine independent association between arterial stiffness, measured as baPWV (dependent variables), and CV risk factors (explanatory variables) in this study, multivariate regression analysis was used. Data from 247 subjects (165 male adolescents and 82 female adolescents) who completed the questionnaire for lifestyle were used in multivariate analysis; 15 subjects (13 male adolescents and 2 female adolescents) did not respond to the questions about smoking habits or alcohol ingestion. Explanatory variables included in the multiple linear regression model were age, sex, mean blood pressure, fasting glucose level, total cholesterol level, HDL-C, triglyceride level, hs-CRP level, BMI, HOMA-IR, total homocysteine level, a current history of smoking (no = 0, yes = 1), and alcohol ingestion (no = 0, yes = 1). Significance was defined at the level of P = .05. All calculations were performed with SAS software version 8.01 (SAS Institute, Cary, NC).

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Results 

The clinical characteristics are shown in Table I. There was no significant difference in mean age, BMI, diastolic blood pressure, total cholesterol levels, triglyceride levels, HDL-C levels, LDL-C levels, and hs-CRP levels between sexes. In addition, there were no differences in health behaviors, such as smoking habits and alcohol ingestion, in the 2 groups. In contrast, waist circumference, waist-hip ratio (WHR), systolic blood pressure, baPWV, total homocysteine level (P < .001), fasting glucose level, fasting insulin level, and HOMA-IR (P < .05), were significantly lower in female subjects. The WBC count (P < .05) was significantly higher in female subjects compared with male subjects.

Table I. Clinical and metabolic characteristics of study participants
CharacteristicsMale (n = 178)Female (n = 84)P value
Age (years)14.5±1.214.8±1.5.09
Adiposity index
BMI (kg/m2)25.1±5.025.0±4.6.88
Waist (cm)82.5±14.077.9±10.8<.001
WHR0.83±0.070.8±0.06<.001
Blood pressure (mm Hg)
Systolic121.0±9.8114.4±10.5<.001
Diastolic61.8±7.060.9±7.3.37
Glucose tolerance index
Fasting glucose (mg/dL)83.9±8.981.3±8.5<.05
Fasting insulin (μIU/mL)14.1±10.711.7±7.1<.05
HOMA-IR3.0±2.62.4±1.5<.05
Lipid profile
Total cholesterol (mg/dL)166.0±31.9170.5±32.1.28
Triglyceride (mg/dL)96.1±53.598.4±51.0.53
HDL-C (mg/dL)45.4±8.647.7±8.8.05
LDL-C (mg/dL)101.2±26.0103.2±30.2.61
Inflammatory index
hs-CRP (mg/mL)0.11±0.20.11±0.3.43
WBC (103/μL)6.87±1.67.36±1.6<.05
baPWV (cm/sec)1034.8±97.4960.8±106.5<.001
Homocysteine (μmol/L)9.9±3.07.4±2.6<.001
Lifestyle
Smoking⁎ (n)10(170)5(82).99
Alcohol† (n)8(165)3(83).76‡

Data are shown as mean ± SD. P values were calculated with t test or χ2-test.

⁎Number of adolescents reporting active smoking at present. (A total of 170 male and 82 female adolescents completed the questionnaire for smoking habit.)

†Number of adolescents reporting alcohol ingestion ≥1 time a week. (A total of 165 male and 83 female adolescents completed to the questionnaire for the habit of alcohol ingestion.)

‡Cells have expected counts <5; P value is calculated with the Fisher exact test.

In both sex groups, baPWV was positively correlated with BMI, waist circumference, WHR, systolic blood pressure, diastolic blood pressure, fasting insulin level, HOMA-IR, triglyceride level, hs-CRP level, and total homocysteine level. In male subjects, age, total cholesterol level, LDL-C level, and WBC were positively correlated with baPWV, and in female subjects, HDL-C level was negatively correlated with baPWV, as shown in Table II.

Table II. Correlations between brachial-ankle pulse wave velocity and various parameters
baPWV
MaleFemale
rP valuerP value
Age (years)0.30<.0010.11.33
Adiposity index
BMI (kg/m2)0.49<.0010.67<.001
Waist (cm)0.51<.0010.52<.001
WHR0.38<.0010.30<.01
Blood pressure (mm Hg)
Systolic0.50<.0010.63<.001
Diastolic0.43<.0010.53<.001
Glucose tolerance index
Fasting glucose (mg/dL)–0.03.720.06.60
Fasting insulin (μIU/mL)0.23<.010.43<.001
HOMA-IR0.20<.010.42<.001
Lipid profile
Total cholesterol (mg/dL)0.20<.010.18.10
Triglyceride (mg/dL)0.35<.0010.33<.001
HDL-C (mg/dL)–0.12.11–0.23<.05
LDL-C (mg/dL)0.18<.050.16.14
Inflammatory index
hs-CRP (mg/mL)0.23<.010.27<.05
WBC (103/μL)0.20<.010.04.70
Homocysteine (μmol/L)0.24<.010.22<.05
Life style
Smoking⁎0.07.330.19.09
Alcohol†0.19<.050.06.56

Coefficients (r) and P values were calculated with the Pearson correlation analysis for continuous variables (male subjects = 178, female subjects = 84) and the Spearman rank correlation analysis for smoking (male subjects = 170, female subjects = 82) and alcohol (male subjects = 165, female subjects = 83).

⁎Active smoking at present.

†Alcohol ingestion ≥1 time a week.

Sex, mean blood pressure, BMI, and total homocysteine level were found to be independent factors significantly associated with arterial stiffness in the multivariate analysis, as shown in Table III. Other clinical variables, such as age, fasting glucose level, total cholesterol level, HDL-C level, triglyceride level, hs-CRP level, HOMA-IR, a current history of smoking, and alcohol ingestion, which were included in a multiple regression model, were not significantly associated with baPWV.

Table III. Multiple regression⁎ analysis to assess independent relationships between baPWV and clinical variables (N = 247)
VariablesParameter estimateSEP value
Gender†0.0510.012< .001
MBP0.0040.001< .001
BMI0.0060.002< .001
Homocysteine0.0420.018< .05

Variables significantly associated with for baPWV (P < 0.05) are shown in the table.

Waist circumference was also a significant correlates of baPWV when entered into the model instead of BMI.

⁎Data from a total of 247 subjects who completed the questionnaire for the life style were used in multivariate analysis, including age, gender, mean blood pressure, homocysteine, BMI, fasting glucose, total cholesterol, HDL cholesterol, Triglyceride, hs-CRP, HOMA-IR, and current history of smoking and alcohol ingestion as independent variables. (R2; 0.46, F-value; 18.09, P < .001).

†Male:1 Female:0.

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Discussion 

This study shows that baPWV in healthy adolescents has a significant association with a number of CV risk factors, including systolic and diastolic blood pressure, adiposity, insulin resistance, lipid profiles, and total homocysteine levels. This suggests that arterial stiffness can be affected by CV risk factors as early as the second decade of life. Furthermore, vascular changes in this population may not be confined to high-risk groups. These findings are consistent with earlier, community-based reports, showing inverse associations between arterial distensibility measured with a non-invasive ultrasound scanning technique and CV risk factors, such as cholesterol levels3 and adiposity with its associated metabolic disturbances,25 in children and adolescents. Because arterial stiffness is a marker of future CV risk and mortality in adults and the elderly,26, 27, 28 therapeutic modification of CV risk factors in adolescents may help to prevent atherosclerosis and CV disease in adults.

We found that the total homocysteine level has an independent association with arterial stiffness in adolescents. Although it is well-established that hyperhomocysteinemia is an independent predictor for CV disease in the adult population,29 there have been only a few studies to clarify this association in children or young adults. Zhu et al10 reported that homocysteine levels in obese female children were significantly correlated with carotid intima thickness and flow-mediated dilatation. Martos et al30 reported that increased homocysteine levels may be involved in the pathogenesis of atherosclerosis. However, other observational studies in healthy young Northern Irish adults,15 obese non-atherosclerotic patients,31 and middle-aged volunteers16 did not find any association between total homocysteine levels and PWV.

The association between baPWV and blood pressure in this study is in concordance with earlier studies showing an inverse association between arterial distensibility and blood pressure in adolescents25 and healthy young adults.32 In addition, Li et al reported that childhood blood pressure predicts arterial stiffness measured as baPWV in young adults.33 They found that 1 single measurement of systolic blood pressure in childhood, regardless of its variation, was associated with baPWV in young adults.33 Mean IMT was higher in men than in women. Men also demonstrated a higher mean PWV and prevalence of plaque.16

In this study, the baPWV of adolescents was significantly related to BMI, WHR, and hs-CRP level, suggesting a link between obesity and inflammation and atherogenic changes. Obese children showed a significantly increased IMT, compared with a normal-weight control group,8, 34 and the common carotid artery stiffness of obese children is associated with obesity and insulin resistance.35 hs-CRP level was positively correlated with baPWV in our study, in accordance with other studies.36, 37 CRP induces complement activation, enhances infiltrations of monocytes, and stimulates monocytes to produce tissue factor, a potent stimulus for thrombosis, thus enhancing the risk of thrombosis and the generation of atherosclerosis lesions.38, 39

Carotid IMT,40 flow-mediated dilatation,41 and PWV18, 19 have all been shown to reflect early atherosclerosis or future risk of CV disease. Among these surrogate markers, measurement of baPWV may have an advantage in its use in the primary care setting or large population studies because this simple method does not require specialized skills and is easy, time saving, and relatively free from operator bias compared with other assessments.21, 42, 43 Although the value of carotid IMT for CV risk prediction has been studied most extensively and supported by a large number of clinical trials,44 this technique must be performed by trained personnel and may have substantial variation in reproducibility because of differences in technical protocols.44 Further, flow-mediated dilatation is of limited of use because of large inter-individual variation.44, 45

To our knowledge, there are few studies of baPWV in healthy children. Niboshi et al46 reported in a study with a large sample size of Japanese children that baPWV in children is largely influenced by age and sex. Collins et al47 measured baPWV of African-American and Caucasian children in a pilot study with a small sample size and suggested racial differences of baPWV compared with the measurements in age-matched Chinese children.48 Further studies are needed to clarify this issue.

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PII: S0022-3476(06)01109-7

doi:10.1016/j.jpeds.2006.11.038

Refers to article:

  • Assessment of Vascular Function: Pulse Wave Velocity

    Bruce S. Alpert, R. Thomas Collins
    The Journal of Pediatrics March 2007 (Vol. 150, Issue 3, Pages 219-220)

The Journal of Pediatrics
Volume 150, Issue 3 , Pages 247-251, March 2007

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