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Psychophysiology, 39 ~2002!, 826–834. Cambridge University Press. Printed in the USA. Copyright © 2002 Society for Psychophysiological Research DOI: 10.10170S0048577202011162

Stability of children’s and adolescents’ hemodynamic responses to psychological challenge: A three-year longitudinal study of a multiethnic cohort of boys and girls

KAREN A. MATTHEWS,a KRISTEN SALOMON,a KAREN KENYON,a and MICHAEL T. ALLEN b a b

Department of Psychiatry, University of Pittsburgh, Pittsburgh, Pennsylvania, USA Department of Education and Psychology, University of Southern Mississippi–Gulf Coast, Long Beach, Mississippi, USA

Abstract This report evaluated ~a! the temporal stability of hemodynamic responses to three tasks using impedance cardiography, and ~b! the influence of aging on stress responses in a multi-ethnic pediatric sample. One hundred children 8 to 10 years old and 49 adolescents 15 to 17 years old were tested at study entry and on average 3 years later. Results showed that the composite task-induced changes in stroke volume ~SV!, cardiac output ~CO!, total peripheral resistance ~TPR!, and pre-ejection period ~PEP! were moderately stable across 3 years ~rs 5 .36 to .51!, with children showing greater stability in task-induced CO change than did adolescents. However, the magnitude of the participant’s stress responses changed over time, varied by task, age group, and gender. These results suggest that hemodynamic responses to stress change with aging during childhood and adolescence and that they can be measured reliably. Descriptors: Impedance cardiography, Cardiovascular reactivity, Children, Adolescence, Stress, Aging

~SBP! and heart rate ~HR! responses is moderately stable across time, especially when responses to individual stressors are aggregated ~e.g., Kamarck, Jennings, & Manuck, 1993; Llabre et al., 1993; Swain & Suls, 1996!. Longer follow-up periods, for example, 4–7 years in several pediatric samples and 10 years in a young adult sample, reveal moderate stability of SBP and HR responses to stressors ~Matthews, Woodall, & Stoney, 1990; Murphy, Alpert, & Walker, 1991; Sherwood et al., 1997!. Hemodynamic patterns underlying blood pressure and HR responses to stress can be evaluated noninvasively by impedance cardiography that assesses stroke volume ~SV!, allowing the calculation of cardiac output ~CO! and total peripheral resistance ~TPR!. Given that African Americans and males tend to show large TPR responses to stress, whereas Whites and females tend to show large CO responses ~Allen, Stoney, Owens, & Matthews, 1993; Girdler, Turner, Sherwood, & Light, 1990; Light, Turner, Hinderliter, & Sherwood, 1993; Murphy, Stoney, Alpert, & Walker, 1995!, these patterns may be useful for interpreting group differences in blood pressure and HR. The reproducibility of impedance-derived measures of change during challenges has been studied, by and large, among adult men and across short time intervals. For example, moderate associations for SV and CO responses to behavioral challenges, such as mirror image tracing and reaction time, were obtained with repeated testing across a few weeks among men ~Fahrenberg, Schneider, & Safian, 1987; Kasprowicz, Manuck, Malkoff, & Krantz, 1990; Myrtek, 1985!. The cold pressor did not produce reliable changes ~Fahrenberg et al. 1987; Myrtek, 1985!.

Exaggerated cardiovascular responses to behavioral challenges may be a risk factor for the development of hypertension and atherosclerosis, diseases that develop over decades and begin in adolescence and young adulthood ~Krantz & Manuck, 1984; Rozanski, Blumenthal, & Kaplan, 1999!. Large blood pressure responses to physical and psychological challenge predict rises in resting blood pressure over time in adolescents ~Matthews, Woodall, & Allen, 1993; Murphy, Alpert, Walker, & Wiley, 1991!, including in those with a family history of hypertension ~Treiber, Turner, Davis, & Strong, 1997!, are elevated among those with central adiposity ~Barnes, Treiber, Davis, Kelley, & Strong, 1998!, and are related to left ventricular mass, although not consistently so ~Allen, Matthews, & Sherman, 1997; Papavassiliou, Treiber, Strong, Malpass, & Davis, 1996; Treiber et al., 1993!. The importance of stress-induced cardiovascular responses as a potential risk factor is heightened if those responses reflect a stable, individual difference variable across substantial portions of the life span when cardiovascular diseases are developing. By and large, published studies of the short-term reproducibility of stress responses show that the relative rank of systolic blood pressure

Research was supported by HL25767 and the Pittsburgh Mind–Body Center ~HL65111 and HL65112!. We thank Diana Buck and Jeanne Wess for their assistance in execution and planning the present protocol. Address requests for reprints to: Karen A. Matthews, Department of Psychiatry, University of Pittsburgh, 3811 O’Hara Street, Pittsburgh, PA 15213, USA. E-mail: [email protected].

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Stability of hemodynamic responses However, quite high correlations for SV, CO, and TPR to aggregated task measures were obtained across several weeks in several samples of men ~Kamarck et al., 1992!. A recent study of 33 Caucasian children also found moderately high stability of SV, CO, and TPR changes during serial subtraction, handgrip, and mirror image tracing across one week ~McGrath & O’Brien, 2001!. The objective of the present study was to evaluate the temporal stability of SV, CO, and TPR reactivity to challenges in a multiethnic sample of boys and girls. At study entry, children who were 8–10 years old and prepubertal, and adolescents who were 15–17 years old and postpubertal were evaluated in a standard laboratory protocol. Approximately 3 years later, the protocol was repeated and included a reaction time task, a mirror image tracing task, and a cold forehead challenge selected because they elicit different autonomic patterns of responding. A secondary objective was to evaluate the influence of aging on the magnitude of stress responses across a 3-year period among children and adolescents. We had previously reported that adolescents in our initial evaluation exhibited greater increases in SV and CO and greater decreases in pre-ejection period ~PEP! during the reaction time task than did children, suggesting a stronger betaadrenergic response among adolescents ~Allen & Matthews, 1997!. There was little evidence for age group differences in alphaadrenergic and parasympathetic activation. We examined CO, SV, and PEP reactivity during the reaction task in particular to see if children’s responses resembled adolescents’ responses more closely at the follow-up session. Our previous analysis also found that female adolescents exhibited a greater increase in CO and SV across all tasks, whereas male adolescents had a larger TPR response ~Allen & Matthews, 1997!. Female children also exhibited a greater CO response to tasks than did male children. Race did not predict TPR responses in our sample, although Whites showed greater HR variability increases than did Blacks ~Salomon, Matthews, & Allen, 2000!. We hypothesized that upon retesting 3 years later, the female children would resemble the female adolescents, that is, both female age groups would show greater CO and SV responses to tasks than males, whereas both male age groups would show greater TPR responses to tasks than females. Method Participants Our sample was composed of 24 Black and 25 White girls and 22 Black and 29 White boys all initially aged 8 to 10 years old at study entry; and 9 Black and 15 White girls and 10 Black and 15 White boys, all initially aged 15 to 17 years old at study entry who participated in the follow-up examination on average 3.1 years later ~SD 5 0.82, range 1.4– 6.2 years!. Of those eligible to participate at the follow-up session, 15 could not be located, 13 declined follow-up participation, and 1 was deceased. Participants were recruited from school districts in the metropolitan Pittsburgh area. Eligibility requirements at study entry were no history of cardiovascular disease or any condition that would require medication that might affect the cardiovascular system ~e.g., high blood pressure, asthma, oral contraception, etc.!; no drug or alcohol abuse or history of mental illness or any professional psychiatric counseling within the past year; less than 80% above their ideal weight according to metropolitan height and weights tables; and no smoking within 12 hr prior to the session. The weight criterion was imposed due to concerns about obtaining impedance cardiography signals of adequate fi-

827 delity with heavier children; less than 2% of potential participants were excluded during initial screening because of weight. Black and White participants were matched for years of parental education ~M years 5 13.0 years for mother and 13.4 years for father! and no parent had a professional degree. At follow-up, having an elective echocardiogram at the initial evaluation was added as an eligibility criterion for the adolescents. In the first phase of the project, approximately equal numbers of 8- to 10-year-olds and 15- to 17-year-olds were recruited because the primary objective was to describe cardiovascular responses to stress according to current pubertal status or age. In the second phase, additional children 8 to 10 years old were recruited and all eligible participants were reassessed, with the primary objective to describe how movement through the pubertal transition affects stress responses. To reach this objective, we did not need to test all the adolescents, and the adolescents without the elective echocardiogram were not recontacted. Physiological Recording Apparatus Impedance cardiography and the electrocardiogram ~ECG! were used for the measurement of SV, PEP, and HR. A Minnesota Impedance Cardiograph Model 304B obtained basal transthoracic impedance waveforms ~Z0! and the first derivative of pulsatile impedance ~dZ0dt! waveforms using a tetrapolar lead configuration ~Kubicek, Patterson, & Witsoe, 1970!. Disposable aluminum0Mylar band electrodes were applied to the neck and chest following published guidelines ~Sherwood et al., 1990! with the voltage electrodes placed around the base of the neck and around the thorax at the level of the xiphisternal junction. Current electrodes were placed at least 3 cm distal to each voltage electrode and supplied a 4-mA, 100-kHz signal to the thoracic region. The ECG signal was transduced using two active Cleartrace LT disposable Ag0AgCl electrodes ~Conmed Andover Medical, Haverhill, MA! placed on each side of the abdomen below the impedance electrode bands, and a ground electrode beside the navel. The ECG signal was filtered and amplified by a Coulbourn S75-11 amplifier0coupler. Processing of the impedance signals and ECG was accomplished using the Cardiac Output Program ~COP!, an on-line computerized video graphics system for impedance cardiography analysis ~Microtronics Corp., Chapel Hill, NC!. Basal impedance, the first derivative of the pulsatile impedance signal ~dZ0dt!, and the ECG were sampled at 500 Hz per channel by a Gateway 80386-based microcomputer hosting a Computer Boards CIO-AD08 analog-todigital converter board. The output of the COP program included SV, HR, CO, calculated as the product of mean SV and HR for a given period, and PEP. The COP program calculates SV using the Kubicek equation ~Kubicek, Karnegis, Patterson, Witsoe, & Mattson, 1966! and ensemble-averaged waveforms over the designated time periods. Details of the calculations of the various physiological measures from impedance cardiography can be found in Sherwood et al. ~1990!. Systolic ~SBP! and diastolic ~DBP! blood pressures were monitored using an IBS Model SD-700A automated blood pressure monitor ~IBS Corp., Waltham, MA! with a standard occluding cuff placed on the participant’s nondominant arm. The monitor uses a low-frequency sensor mounted on the cuff to detect arterial wall motion and Korotkoff vibrations. It has an automatic inflation and deflation, which can be preset for any rate ranging from 1 to 6 mmHg, and indicates invalid readings due to movement, artifacts, noise, and so forth. Pediatric, adult, and obese cuffs were used according to the arm size of the participant. The pressure

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K.A. Matthews et al.

readings were entered into the COP program after the experimental session was over, and the program automatically computed TPR using the formula TPR 5@~~~SBP 2 DBP!03! 1 DBP!0CO# * 80, where TPR is in units of dyne-s0cm 5 , CO is in liters0minute, and SBP and DBP are in millimeters of mercury. Customized software allowed us to extract continuous interbeat interval ~IBI! data from files created by the COP program. These IBI files were screened and edited for artifactual values. Experimental Tasks The following three tasks were administered at both Time 1 and Time 2; a fourth task was not readministered. All tasks were presented while the participant sat upright in a comfortable lounge chair that had a detachable desk surface. Reaction time. A computerized choice reaction time task required the participant to respond as quickly as possible to a 1000 Hz tone presented via headphones by pressing a joystick button, but to refrain from responding to a 2000 Hz tone. Tones were presented at irregular intervals by an AT&T 6300 microcomputer during the 3-min task. The task was programmed so that participants earned 75 points for each time they beat the average reaction time of previous trials, and 20 points for correctly withholding a response to the incorrect tone. Thirty points were subtracted for responding to the incorrect tone. Two cents were given to the participant for each point that he or she earned. Task performance was measured in terms of points earned and average reaction time. This task was chosen on the basis of past studies indicating that the task elicits increases in myocardial reactivity due to an increase in beta-adrenergic activity ~e.g., Allen, Boquet, & Shelley, 1991!. Mirror tracing. Participants were required to trace around a copper star with a metal stylus while only being allowed to see the mirror image of the star. The tracing apparatus ~Stoelting Co., Chicago, IL! was interfaced to an AT&T 6300 microcomputer, and customized software kept track of the task time and whether the stylus was on the star. Going off the star produced a loud beep through the headphones. Task performance was measured in star segments traced, as well as the percentage of the total time that the participant was off the star. Task time was 3 min. This task has been previously described as producing increases in vascular resistance due to increased alpha-adrenergic activation ~e.g., Kasprowicz et al., 1990!. Cold forehead. A two-quart bag of two parts crushed ice and one part water was placed on the participant’s head for 1 min. The participants were informed of the time remaining during the minute in order to encourage completion of the minute, although the instructions for the task clearly indicated that the ice bag would be removed if the pain became too intense. Only 1 participant was unable to complete the entire minute. At the end of the task, participants were asked to rate their perception of both cold and pain during the task on a 7-point Likert scale, with 1 being no pain or cold and 7 being extreme pain or extremely cold. This task evokes a strong alpha-adrenergic activation in many participants and the cold on the face also produces a vagal bradycardia in some, presumably due to a rudimentary “dive reflex.”

Experimental Protocol Recruitment of participants was accomplished with the assistance of a number of school districts in the suburban Pittsburgh area. Letters describing the study were delivered to the administrative offices of the school districts, where address labels for parents of age-eligible children and adolescents were affixed by school personnel and the letters subsequently mailed. Parents who were interested in finding out additional information were given phone numbers to call for an initial screening interview. The protocol was explained to the parents in detail during the initial recruitment contact. Adolescents and their parents were required to sign a consent form prior to participation in the protocol; children younger than 18 signed an assent form and their parents signed a separate consent form prior to their participation. All consent and assent forms were approved by the Psychosocial Institutional Review Board of the University of Pittsburgh Medical Center. Participants arrived at the laboratory at about 8:30 a.m. after an overnight fast and fluid restriction. Height, weight, and skin folds were measured after the participant changed into a hospital gown. A venous blood draw was then performed for a variety of biochemical assays. After the blood draw, the participants were fed a light breakfast, followed by the application of electrodes for impedance cardiography and the ECG. The blood pressure cuff was placed on the upper aspect of the nondominant arm with the microphone placed above an area where the brachial artery could be palpated. The children were then given instructions for an initial 10-min rest period. The reaction time, mirror tracing, and cold forehead tasks were given in a counterbalanced order with 8-min intertask rest periods after each task, with the cold forehead having an additional 2 min following the removal of the ice bag. Longer intertask rest periods were not feasible because of restlessness of young participants. With the time needed to explain the next task and for the experimenter to enter and leave the room, the time between tasks was 10 to 15 min. A final 10-min rest period followed the last task. Sensors were removed following the last rest period, and participants were then given a number of psychosocial questionnaires, the results of which are not reported here. Participants were paid $75 for completing the protocol, along with money earned on the reaction time task. Appointments for resting echocardiographic examinations of participants at a local hospital were generally scheduled at the close of the laboratory protocol. These examinations usually occurred within a few weeks of the reactivity session. Data Reduction Data for HR and impedance-derived variables were collected on a minute-by-minute basis during the last 3 min of the initial and final rest periods, during the last minute of the intertask rest periods, and during all 3 min of reaction time and mirror tracing. For impedance cardiography calculations, 55 s of each minute were used for ensemble averaging. These minute-by-minute values were averaged to form means for each period. Data were collected in 10-s blocks during the minute of cold forehead ~7 s of each 10-s block were ensemble averaged! and averaged. Blood pressures were taken at the 5-, 7-, and 9-min mark of the initial and final rest periods, and the last two readings were averaged to form SBP and DBP means for those periods, coinciding with impedance cardiography sampling. One blood pressure reading was taken at the 7-min mark of each of the three intertask rest periods. Three readings were taken during the reaction time and mirror tracing tasks, and these readings were averaged to form task means. Finally, one blood pressure reading was taken during the

Stability of hemodynamic responses

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cold forehead task, the reading being initiated 15 s into the ice bag application, and one reading was taken 2 min after the ice bag was removed ~not part of the intertask interval!. Data Analyses The initial rest period was selected as the baseline period because the majority of cardiovascular measures were lowest during this period. Reactivity scores were computed by subtracting baseline mean level of a variable from each task mean. Data were reviewed initially for implausible values, for example, pulse pressure less than 15 mmHg, heart rates less than 40 bpm, and then formal tests of skewness and kurtosis were conducted on baseline levels and change scores. There were several outliers for change in TPR and SV. Those analyses were conducted with and without the outliers. In only one case did the results change, and that case is noted below. To evaluate changes across time on the cardiovascular measures, we conducted 2 3 2 3 2 3 2 repeated measures ANOVAs, with Age Group, Gender, and Race as the between-subjects factors, and Time ~Time 1 vs. Time 2! as the repeated measures factor. Task with three levels was an additional within factor for the analyses of reactivity. We used SPSS GLM, followed by tests for simple effects for evaluating interactions terms, and reported sphericity tests for effects involving Task, and h 2 for effect size. We reported here the unique effects pursuant to the main focus of the paper, the within effects involving Time, either as a main effect or in interaction with other blocking factors, at p , .05, and all other effects at p , .01. We did this because the focus of this paper is on changes and stability over time, and we already have reported age, gender, and race group effects based on Time 1 data ~Allen & Matthews, 1997; Salomon et al. 2000!. Highest order interaction terms were interpreted unless they accounted for a small portion of

the variance, relative to the variance accounted for by lower order interactions and main effects. Effect sizes were reported for the evaluation of interaction terms. To evaluate the stability of the cardiovascular measures across time, baseline and task-induced change scores were correlated between Time 1 and Time 2, adjusting for the duration between examinations. As recommended by Kamarck et al. ~1993!, we developed a task composite score by standardizing the change scores within task and age group and summing. In this way, each task contributed equally to the total reactivity score. Then these composite scores were also correlated across sessions. Differences in correlation coefficients by age group, gender, and race were accomplished by converting the correlations to Fisher’s z and dividing by the standard error of the difference of the z coefficients.

Results T tests compared the study entry baseline and reactivity scores of participants and eligible nonparticipants. The only difference was that nonparticipants had smaller PEP decreases during the mirror image tracing task, p , .05. Baseline Levels across Time Table 1 presents the means for children and adolescents for resting levels for each cardiovascular variable and body mass index ~BMI! for each session for boys and girls, children and adolescents. Significant race effects were few and, for simplicity, the tabled data are not partitioned by race. Blood pressure. Baseline SBP varied by Gender, F~1,136! 5 29.6, p , .001, h 2 5 .179; by Age Group, F~1,136! 5 38.6,

Table 1. Mean (SD) Baseline Measures at Time 1 and Time 2 for Children and Adolescents Females Variable Systolic BP ~mmHg! Children Adolescents Diastolic BP ~mmHg! Children Adolescents Heart rate ~bpm! Children Adolescents PEP ~ms! Children Adolescents Stroke volume ~ml! Children Adolescents Cardiac output ~l0min! Children Adolescents TPR ~dyne-s0cm 5 ! Children Adolescents BMI ~kg0m 2 ! Children Adolescents

Males

Time 1 ~SD!

Time 2 ~SD!

Time 1 ~SD!

Time 2 ~SD!

105.0 ~7.5! 109.5 ~7.8!

104.4 ~9.0! 109.3 ~9.0!

109.5 ~7.5! 118.5 ~7.5!

108.4 ~9.4! 120.9 ~9.1!

61.8 ~8.4! 63.3 ~7.6!

61.6 ~8.4! 68.7 ~11.0!

62.9 ~9.4! 60.3 ~9.1!

61.7 ~8.7! 66.0 ~7.9!

85.7 ~9.4! 73.4 ~10.5!

83.9 ~8.9! 73.9 ~9.4!

82.1 ~11.5! 61.2 ~9.2!

74.8 ~9.1! 63.1 ~7.7!

92.9 ~7.3! 104.6 ~7.0!

99.2 ~11.2! 105.8 ~13.4!

95.9 ~7.2! 111.3 ~9.2!

105.1 ~10.3! 111.6 ~11.1!

49.5 ~9.4! 96.5 ~25.0!

67.0 ~17.0! 93.6 ~19.5!

52.2 ~13.9! 107.8 ~26.3!

71.0 ~16.5! 98.4 ~20.7!

4.2 ~0.7! 7.0 ~1.7!

5.5 ~1.2! 6.9 ~1.4!

4.2 ~1.0! 6.4 ~1.2!

5.2 ~1.0! 6.1 ~1.0!

1,491 ~286! 954 ~242!

1,139 ~240! 999 ~239!

1,585 ~447! 1,023 ~242!

1,247 ~398! 1,141 ~269!

17.5 ~2.1! 21.9 ~3.1!

20.2 ~3.4! 23.3 ~3.6!

17.8 ~2.6! 23.9 ~4.1!

20.2 ~3.4! 26.3 ~3.6!

830 p , .001, h 2 5 .221; and by Time 3 Age Group 3 Race 3 Gender, F~1,136! 5 4.3, p 5 .04, h 2 5 .031. Males and adolescents had higher SBP than did females and children. Among males, Black adolescents and children had similar SBP at the two examinations, whereas White children declined in SBP ~Ms 5 110 to 107 mmHg! and White adolescents increased from the initial to follow-up examination ~Ms 5 117 to 121 mmHg!, h 2 5 .088 for Time 3 Age Group 3 Race among males. Among females, there were no significant interaction effects. Baseline DBP varied by Time, F~1,136! 5 6.1, p 5 .02, h 2 5 .043; and Time 3 Age Group, F~1,136! 5 9.7, p 5 .002, h 2 5 .067. DBP increased over time among adolescents, h 2 5 .212 for Time effect, but not among children. Heart rate and PEP. Baseline heart rate varied by Time, F~1,136! 5 4.2, p 5 .04, h 2 5 .030; Gender ~1,136! 5 32.5, p , .001, h 2 5 .193; Age Group, F~1,136! 5 75.5, p , .001, h 2 5 .357; Time 3 Age Group, F~1,136! 5 12.4, p 5 .001, h 2 5 .084; and Time 3 Age Group 3 Gender ~1,136! 5 4.1, p , .05, h 2 5 .029. Heart rate was higher among females than males and among children than adolescents at both sessions. Heart rate decreased across sessions among the male children, but not among male adolescents, h 2 5 .199, for Time 3 Age among males; there were no effects among females. Baseline PEP varied by Time, F~1,135! 5 24.7, p , .001, h 2 5 .154; Age Group, F~1,135! 5 41.4, p , .001, h 2 5 .235; Gender ~1,135! 5 16.7, p , .001, h 2 5 .110; Time 3Age Group, F~1,135! 5 17.3, p , .001, h 2 5 .114; and Race 3 Gender, F~1,135! 5 7.2, p 5 .008, h 2 5 .051. PEP levels increased across time among children, h 2 5 .483 for Time effect among children, but not among adolescents. PEP was longer among males than females and among adolescents than children at both sessions. Stroke volume and cardiac output. Baseline SV varied by Time, F~1,135! 5 18.8, h 2 5 .122; Age Group, F~1,135! 5 189.5, p , 001, h 2 5 .584; Time 3 Race, F~1,135! 5 8.8, p 5 .004, h 2 5 .061; and Time 3 Age Group, F~1,135! 5 52.2, p , .001, h 2 5 .279. SV increased across sessions, but only among children, h 2 5 .595 for Time effect and not among adolescents. Blacks increased more in SV ~Ms 5 71.0 to 82.6 ml!, h 2 5 .361 for Time effect among Blacks, whereas Whites changed very little. Adolescents had higher SV levels than did children. Baseline CO varied by Time, F~1,135! 5 30.3, p , .001, h 2 5 .183; Age Group, F~1,135! 5 101.3, p , .001, h 2 5 .429; Time 3 Race ~1,135! 5 10.8, p , .001, h 2 5 .074; and Time 3 Age group ~1,135! 5 46.5, p , .001, h 2 5 .256. CO increased from the initial to follow-up examination among the children only, h 2 5 .586 for Time effect among children. CO increased from initial to follow-up examination among Blacks only ~Ms 5 5.1 to 6.0 l0min!, h 2 5 .390 for Time effect among Blacks. Total peripheral resistance. Baseline TPR varied by Time, F~1,135! 5 22.4, p , .001, h 2 5 .142; by Age Group, F~1,135! 5 43.4, p , .001, h 2 5 .243; by Time 3 Race ~1,135! 5 4.0, p , .05, h 2 5 .028, and Time 3 Age Group, F~1,135! 5 51.1, p , .001, h 2 5 .275. Adolescents increased in TPR levels, h 2 5 .057 for Time effect, whereas children decreased over time, h 2 5 .490 for Time effect. Blacks decreased in TPR levels across sessions ~Ms 5 1348 to 1152 dyne-s0cm 5 !, h 2 5 .245 for Time effect, to a greater extent than did Whites ~Ms 5 1202 to 1122 dyne-s0cm 5 !, h 2 5 .097 for Time effect. Overall, children had higher levels of TPR than did adolescents.

K.A. Matthews et al. BMI. BMI varied by Time, F~1,141! 5 136.5, p , .001, h 2 5 .492; Gender, F~1,141! 5 7.5, p 5 .007, h 2 5 .050; Age Group, F~1,141! 5 86.5, p , .001, h 2 5 .380; and Age 3 Gender, F~1,141! 5 6.2, p 5 .014, h 2 5 .04. BMI increased from the initial to follow-up session, and adolescents males had the largest BMI. Cardiovascular Reactivity across Time Table 2 shows the changes in blood pressure, HR, SV, CO, and TPR from baseline to each task for each group collapsed across race. Blood pressure. SBP reactivity varied by Task, F~2,250! 5 15.00, p , .001, E 5 .75, h 2 5 .107; Task 3 Time, F~2,250! 5 36.66, p , .001, E 5 .89, h 2 5 .227; and by Task 3 Time 3 Age Group, F~2,250! 5 8.03, p , .001, h 2 5 .060. SBP reactivity was greater during the cold forehead task than the other two tasks. SBP reactivity declined over time during the mirror image tracing task, h 2 5 .056 for Time effect, increased over time during the cold forehead task, h 2 5 .183 for Time effect, whereas during reaction time task, children showed no change in reactivity over time and adolescents declined, h 2 5 .030 for Time 3 Age Group interaction. DBP reactivity varied by Task, F~2,252! 5 102.53, p , .001, E 5 .80, h 2 5 .449; Time 3 Task, F~2,252! 5 7.52, p , .01, E 5 .94, h 2 5 .056; Time 3 Age Group 3 Gender, F~1,126! 5 6.81, p 5 .01, h 2 5 .051; Time 3 Race, F~1,126! 5 4.23, p 5 .04, h 2 5 .032, and Time 3 Task 3 Age Group 3 Race, F~2,252! 5 3.51, p 5 .03, h 2 5 .027. DBP reactivity was greatest during the cold forehead task, followed by reactivity during the mirror image tracing task, followed by reactivity during the reaction time task. Among adolescents, males exhibited greater DBP reactivity than did females, h 2 5 .186 for Gender, and increased from the first to second session, whereas females declined, h 2 5 .109 for Time 3 Gender. Among children, there were no Gender and Time 3 Gender effects. The four-way interaction was not interpretable. Heart rate and PEP. HR reactivity varied by Age Group, F~1,133! 5 6.81, p , .01, h 2 5 .049; Time, F~1,133! 5 37.49, p , .001, h 2 5 .220; and Task, F~2,266! 5 73.87, p , .001, E 5 .86, h 2 5 .357. HR reactivity was larger during the reaction time and mirror image tracing tasks, relative to the cold forehead task. HR reactivity declined with retesting and was greater in the adolescents than in the children. PEP reactivity, defined as greater declines from baseline, varied by Task, F~2,264! 5 241.1, p , .001, E 5 .72, h 2 5 .646; Time, F~1,132! 5 26.5, p , .001, h 2 5 .167; Time 3 Age Group, F~1,132! 5 12.2, p , .001, h 2 5 .085; Time 3 Age Group 3 Task, F~2,264! 5 9.2, p , .001, h 2 5 .065, Time 3 Gender, F~1, 132! 5 9.0, p , .001, h 2 5 .064; Time 3 Gender 3 Task, F~2,264! 5 3.8, p 5 .02, h 2 5 .028, and Time 3 Race 3 Gender, F~1,132! 5 4.3, p 5 .04, h 2 5 .032. Greater PEP reactivity was apparent during the reaction time task, followed by the mirror image tracing task, with a decrease in reactivity occurring during the cold forehead task. PEP reactivity declined across sessions among the adolescents during the reaction time and cold forehead tasks, whereas it increased for children during the reaction time task, h 2 5 .137 and .038 for the Time 3 Age Group interactions for the two tasks, respectively. ~Note there was no significant interaction of Time 3 Age Group 3 Gender 3 Task.! During the reaction time and mirror image tracing tasks, PEP reactivity declined to a greater extent across sessions among males than among females, h 2 5 .063 and .053, for Time 3 Gender for the two tasks, respectively. The decline in PEP reactivity across tasks was par-

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Table 2. Mean (SD) Change Scores Measures at Time 1 and Time 2 for Children and Adolescents Females Variable Systolic BP ~mmHg!

Diastolic BP ~mmHg!

Heart rate ~bpm!

PEP ~ms!

Stroke volume ~ml!

Cardiac output ~l0min!

TPR ~dyne-s0cm5 !

Task Reaction time Children Adolescents Mirror tracing Children Adolescents Cold forehead Children Adolescents Reaction time Children Adolescents Mirror tracing Children Adolescents Cold forehead Children Adolescents Reaction time Children Adolescents Mirror tracing Children Adolescents Cold forehead Children Adolescents Reaction time Children Adolescents Mirror tracing Children Adolescents Cold Forehead Children Adolescents Reaction time Children Adolescents Mirror tracing Children Adolescents Cold forehead Children Adolescents Reaction time Children Adolescents Mirror tracing Children Adolescents Cold forehead Children Adolescents Reaction time Children Adolescents Mirror tracing Children Adolescents Cold forehead Children Adolescents

Time 1 ~SD!

Males Time 2 ~SD!

Time 1 ~SD!

Time 2 ~SD!

6.3 ~8.7! 8.2 ~7.9!

7.9 ~8.8! 4.9 ~5.8!

8.8 ~6.5! 12.4 ~7.1!

7.3 ~7.2! 8.8 ~8.4!

7.5 ~7.3! 8.0 ~6.5!

6.6 ~8.1! 4.2 ~5.5!

7.1 ~7.6! 12.7 ~7.8!

7.1 ~8.2! 8.6 ~7.3!

10.0 ~10.0! 6.7 ~5.9!

13.3 ~8.8! 15.9 ~10.8!

8.8 ~10.3! 8.5 ~6.3!

12.5 ~10.2! 14.0 ~10.0!

5.7 ~9.3! 5.5 ~8.7!

6.7 ~8.4! 1.6 ~6.8!

6.8 ~9.8! 5.6 ~6.9!

3.4 ~8.7! 6.7 ~6.3!

7.8 ~9.7! 9.3 ~7.0!

9.8 ~8.1! 4.2 ~6.3!

8.9 ~9.0! 14.0 ~7.8!

6.2 ~8.5! 11.5 ~9.1!

13.9 ~12.6! 15.2 ~7.7!

17.3 ~12.3! 16.3 ~10.3!

14.8 ~14.1! 15.8 ~11.6!

14.4 ~12.5! 24.0 ~12.8!

6.7 ~6.4! 9.7 ~6.2!

5.0 ~8.1! 5.4 ~5.8!

8.2 ~9.0! 11.7 ~8.0!

4.3 ~6.6! 5.8 ~6.7!

8.4 ~6.7! 9.8 ~5.3!

4.3 ~6.1! 5.1 ~5.2!

7.6 ~7.5! 8.4 ~4.9!

4.0 ~4.6! 5.4 ~4.9!

0.5 ~7.2! 3.0 ~5.9!

21.7 ~8.1! 0.6 ~7.8!

0.6 ~8.2! 3.2 ~5.1!

22.7 ~8.0! 20.4 ~4.4!

24.9 ~4.7! 29.9 ~6.8!

28.0 ~8.5! 27.2 ~5.8!

26.4 ~6.6! 212.8 ~8.1!

25.4 ~7.9! 24.9 ~10.2!

23.9 ~3.8! 24.4 ~4.7!

24.2 ~4.6! 22.6 ~4.7!

22.7 ~4.6! 23.3 ~3.8!

0.4 ~4.6! 20.7 ~7.2!

0.6 ~3.9! 20.1 ~4.6!

1.8 ~4.8! 3.7 ~4.5!

1.8 ~4.1! 1.7 ~3.6!

3.7 ~4.9! 5.2 ~5.8!

21.0 ~3.9! 4.1 ~9.3!

2.3 ~6.1! 1.4 ~7.8!

22.2 ~6.2! 20.7 ~11.4!

21.8 ~8.1! 23.9 ~11.9!

21.3 ~5.0! 22.8 ~9.2!

21.9 ~5.5! 21.3 ~8.2!

24.4 ~5.6! 28.5 ~10.8!

27.1 ~5.6! 25.7 ~6.8!

20.4 ~5.5! 24.6 ~9.1!

23.2 ~7.9! 27.0 ~8.2!

22.4 ~7.2! 25.8 ~12.3!

25.2 ~9.6! 26.2 ~7.4!

0.2 ~.4! 1.4 ~1.1!

0.5 ~.7! 0.7 ~.7!

0.3 ~.7! 1.2 ~1.1!

0.3 ~.4! 0.8 ~.6!

0.1 ~.6! 0.4 ~.6!

0.0 ~.6! 0.3 ~.6!

20.3 ~.4! 0.0 ~.5!

0.0 ~.4! 0.0 ~.7!

20.4 ~.6! 20.4 ~.7!

20.2 ~.5! 0.0 ~.4!

20.6 ~.5! 20.5 ~.4!

31.1 ~188! 279.7 ~156!

0.8 ~147! 239.6 ~80!

116.3 ~297! 259.3 ~140!

42.7 ~191! 87.3 ~190!

56.6 ~198! 9.0 ~112!

124.2 ~148! 21.8 ~91!

205.7 ~283! 122.4 ~155!

175.1 ~155! 157.0 ~171!

281.6 ~314! 151.5 ~140!

389.2 ~309! 274.6 ~205!

402.8 ~499! 181.7 ~164!

424.3 ~314! 412.7 ~248!

0.2 ~.7! 0.3 ~1.0!

832 ticularly due to Black males, Ms 5 22.6 and 1.7, h 2 5 .149 for Time 3 Gender interaction among Black males, with no significant effect involving Time among Black females, Ms 5 22.7 and 22.9. The Time 3 Gender interaction for Whites was nonsignificant. Stroke volume and cardiac output. SV reactivity varied by Task, F~2,264! 5 36.3, p , .001, E 5 .94, h 2 5 .216; Gender, F~1,132! 5 12.4, p , .001, h 2 5 .086; Task 3 Gender, F~2,264! 5 5.6, p , .001, h 2 5 .041; Task 3 Age Group, F~2,264! 5 6.7, p , .001, h 2 5 .048; Time 3 Task, F~2,264! 5 3.4, p 5 .04, E 5 .97, h 2 5 .025; Time 3 Task 3 Age Group, F~2,264! 5 11.7, p , .001, h 2 5 .082; and Time 3 Task 3 Race, F~2,264! 5 4.3, p 5 .02, h 2 5 .031. None of the tasks elicited overall increases in SV, with the cold forehead and mirror image tracing tasks eliciting the largest declines from baseline. Relative to males, females exhibited greater SV reactivity ~or smaller declines! during the reaction time task at both sessions, h 2 5 .082 for Gender effect, and during the mirror image tracing at both sessions, h 2 5 .132 for Gender effect. During the reaction time task, children increased in SV reactivity upon retesting to a greater extent than did the adolescents, h 2 5 .054 for Time 3 Age Group interaction, with SV reactivity declining upon retesting during the cold forehead task in both age groups combined, h 2 5 .046 for Time effect. During the reaction time task, Blacks’ SV reactivity decreased from the initial to follow-up evaluation ~Ms 5 20.04 to 22.7 ml! more than did Whites ~Ms 5 0.2 to 1.7 ml!, h 2 5 .042 for Time 3 Race interaction, with no other effects obtained during the remaining tasks. CO reactivity varied by Task, F~2,264! 5 138.8, p , .001, E 5 .94, h 2 5 .513; Age Group, F~1,132! 5 23.7, p , .001, h 2 5 .152; Task 3 Age Group, F~2,264! 5 12.9, p , .001, h 2 5 .089; Gender, F~1,132! 5 11.8, p , .001, h 2 5 .082; Time, F~1,132! 5 45.6, p , .001, h 2 5 .257, Time 3 Age Group, F~1,132! 5 12.4, p , .001, h 2 5 .086, Time 3 Task 3 Age Group, F~2,264! 5 18.2, p , .001, h 2 5 .121. CO reactivity was modest in size, but greatest during the reaction time task and least during the cold forehead task, and greater in females than in males. During the reaction time task, adolescents decreased in CO reactivity across sessions, whereas the children were similar across sessions, h 2 5 .192 for Time 3 Age Group interaction; during mirror image tracing, adolescents had greater CO reactivity than did children at both sessions, h 2 5 .140 for Time effect; and during the cold forehead task there were no effects with Time or Age Group.

K.A. Matthews et al. Associations of Cardiovascular Measures Over Time Table 3 reports the partial correlation coefficients for the baseline measures and composite reactivity scores, adjusted for duration, for the entire sample and adolescents and children, taken separately. The baseline measures of SBP, HR, PEP, SV, CO, and TPR were all reliable across time and the magnitude of the associations was substantial. Baseline DBP levels were associated across time among adolescents only. A comparison of the magnitude of associations between children and adolescents showed that adolescents’ baseline HR was more stable than children’s, p 5 .04. With the exception of DBP, the composite reactivity scores were reliable across time in the full sample, with the impedance measures showing correlations as large as SBP and HR associations. Comparisons of the magnitude of the associations between children and adolescents showed that children’s composite CO reactivity scores were more stable than those of adolescents, p 5 .008. The remainder of the composite scores did not differ between adolescents and children, but TPR composite reactivity scores were greater among males than females, rs 5 .59 and .28, respectively, p 5 .03. Blacks and Whites did not differ in the magnitude of the associations. Partial correlations, adjusted for duration between examinations, between individual task reactivity scores at the two sessions are presented in Table 4 for the full sample and the two age groups separately. In the full sample, the associations were moderate in size and statistically significant, except for DBP reactivity scores. Among adolescents, the associations were apparent for HR reactivity during all tasks, SBP and TPR reactivity during two tasks, and DBP and PEP reactivity during one task. Among children, the associations were apparent for all tasks for PEP, HR, CO, TPR, and SV reactivity; and for two of the three tasks for SBP reactivity.

Table 3. Partial Correlation Coefficients for Baseline and Composite Task Change Scores between Examinations, Adjusted for Duration Children Variable

Total peripheral resistance. TPR reactivity varied by Task, F~2,248! 5 113.0, p , .001, E 5 .94, h 2 5 .477; Age Group, F~1,124!5 7.8, p , .01, h 2 5 .059; by Gender, F~1,124! 5 8.3, p , .01, h 2 5 .063; Time 3 Age Group, F~1,124! 5 5.2, p , .02, h 2 5 .040; Time 3 Age Group 3 Gender, F~1,124! 5 4.9, p 5 .03, h 2 5 .038; Time 3 Task, F~2,248! 5 8.1, p , .001, E 5 .97, h 2 5 .062; and Time 3 Task 3 Age Group, F~2,248! 5 3.7, p , .03, h 2 5 .029. Cold forehead task elicited greater TPR reactivity than did mirror image tracing task, which elicited greater TPR reactivity than did the reaction time task. Children and males elicited greater reactivity than did their counterparts. Among the adolescents, males increased in TPR reactivity from the initial to follow-up session more than did females, h 2 5 .093 for Time 3 Gender among the adolescent age group with no effects among the child age group. During the reaction time task, adolescents increased in TPR reactivity from the initial to follow-up session, whereas the children declined, h 2 5 .089 for the Time 3 Age Group interaction; TPR reactivity increased over sessions during the cold forehead task, regardless of age group, h 2 5 .107 for Time.

Systolic BP ~mmHg! Baseline Composite task change Diastolic BP ~mmHg! Baseline Composite task change Heart rate ~bpm! Baseline Composite task change PEP ~ms! Baseline Composite task change Stroke volume ~ml! Baseline Composite task change Cardiac output ~l0min! Baseline Composite task change TPR ~dyne-s0cm 5 ! Baseline Composite task change

Adolescents

All

r

p value

r

p value

r

p value

.61 .36

,.001 .001

.74 .50

,.001 .001

.65 .41

,.001 ,.001

.18 .03

.07 .80

.33 .08

.026 .61

.24 .04

.004 .62

.57 .28

,.001 .006

.77 .29

,.001 .05

.63 .29

,.001 .001

.66 .49

,.001 ,.001

.53 .36

,.001 .015

.63 .42

,.001 ,.001

.52 .41

,.001 ,.001

.58 .21

,.001 .17

.53 .36

,.001 ,.001

.48 .52

,.001 ,.001

.63 .08

,.001 .57

.52 .40

,.001 ,.001

.51 .58

,.001 ,.001

.61 .33

,.001 .032

.54 .51

,.001 ,.001

Note: Degrees of freedom varied from 86 to 93 for children, 41 to 45 for adolescents, and 131 to 141 for entire sample.

Stability of hemodynamic responses

833

Table 4. Partial Correlation Coefficients for Each Task Change Score between Examinations, Adjusted for Duration Children Variable Systolic BP ~mmHg! Diastolic BP ~mmHg! Heart rate ~bpm! PEP ~ms! Stroke volume ~ml! Cardiac output ~l0min! TPR ~dyne-s0cm 5 !

Adolescents

All

Task

r

p value

r

p value

r

p value

Reaction time Mirror tracing Cold forehead Reaction time Mirror tracing Cold forehead Reaction time Mirror tracing Cold forehead Reaction time Mirror tracing Cold forehead Reaction time Mirror tracing Cold forehead Reaction time Mirror tracing Cold forehead Reaction time Mirror tracing Cold forehead

.22 .13 .46 .02 2.01 .15 .38 .28 .42 .45 .33 .34 .34 .44 .34 .48 .54 .28 .37 .45 .48

.035 .22 ,.001 .83 .94 .14 ,.001 .007 ,.001 ,.001 .001 .001 .001 ,.001 .001 ,.001 ,.001 .005 ,.001 ,.001 ,.001

.50 .64 .28 2.16 .39 .05 .43 .32 .44 .31 .29 .11 2.09 .25 .29 .04 .08 .18 .09 .40* .32

,.001 ,.001 .06 .30 .008 .77 .003 .033 .002 .037 .06 .45 .54 .10 .06 .79 .62 .22 .57 .006 .035

.31 .30 .40 2.04 .12 .12 .40 .29 .42 .40 .29 .26 .20 .39 .32 .35 .39 .23 .28 .44 .43

,.001 ,.001 ,.001 .65 .16 .16 ,.001 ,.001 ,.001 ,.001 ,.001 .002 .017 ,.001 ,.001 ,.001 ,.001 .007 .001 ,.001 ,.001

Note: Degrees of freedom varied from 89 to 92 for children, 43 to 45 for adolescents, and 135 to 141 for entire sample. *p , .10 in analysis removing two outliers.

Discussion The primary objective of the present article was to determine the stability over 3 years in impedance-derived hemodynamic responses to behavioral challenges in a multiethnic group of children and adolescents. Our results showed that the baseline measures of CO, TPR, SV, PEP, HR, and blood pressure were reliable over time with the associations ranging from .50 to .74, excluding DBP. The breakdown by age group showed that the baseline measures were equally stable in both age groups, except for greater HR stability among adolescents. The lower reliability for DBP is probably due to greater measurement error ~the difficulty in assessing DBP in children by Korotkoff sounds, with some children having very low DBP; Berenson, 1980!. With regard to the composite measures of reactivity, all measures show reasonable stability over the 3-year period in the full sample, with the magnitude of associations being as high for PEP, CO, SV, and TPR as for SBP and HR. The associations are smaller for reactivity measures than for baseline measures ~except for TPR!, but that is not surprising given that the reactivity measures include error variance from both the task and baseline measures. Furthermore, even though the tasks were the same and were presented in the same counterbalanced order, such factors as the experimenter, time of the year, and motivation to perform the tasks may have changed over time, which would impact stress responses to a greater extent than baseline responses. Statistical comparisons of size of associations for children and adolescents reveal that children were more similar in their CO reactivity scores across the 3 years than were adolescents. In fact, adolescents did not exhibit a significant association over time in CO reactivity, partly because SV reactivity across time was not significant. The analyses of stability across individual tasks show similar patterns for the full sample and for the children. However, among

the adolescents, fewer individual task reactivity scores were reliable across time, and of the impedance-derived measures, TPR reactivity exhibited stability to two of the three tasks. Why did this pattern occur? Sample size was smaller for the adolescents ~49 vs. 100 children!, resulting in wide confidence intervals for adolescents’ estimates. Another factor is related to our secondary objective: to describe effects of aging or retesting on changes in cardiovascular function during behavioral challenges. We had expected that children would increase in their CO, SV, and PEP reactivity response to the reaction time task, that is, become more similar to the adolescents. There was modest support for these hypotheses, as SV and PEP reactivity during the reaction time task did increase for children upon retesting. However, children’s CO reactivity responses stayed the same, whereas the adolescents’ declined. Even though testing occurred almost 3 years apart, it was possible that stress responses habituated somewhat, so that the proposed effects of aging increasing children’s reactivity responses were masked. The previously observed gender differences in CO, PEP, and TPR responses to stress in adulthood and in adolescents at the initial evaluation were maintained upon retesting. These findings suggest that early in the life course, males are more likely to be vasoconstrictors, whereas females are more likely to be myocardial reactors. The precise cardiovascular risk associated with these patterns has yet to be determined. How do our findings compare with previous stability estimates of impedance measures? For mirror image tracing, Kasprowicz et al. ~1990! reported correlations ranging from .31 to .73 for cardiac index, PEP, HR, SBP, and DBP among 39 young men across 4 weeks. For an aversive reaction time task, Sherwood et al. ~1997! reported correlations of .20 to .46 for PEP, HR, SBP, and DBP among 55 predominantly White men across 10 years. For cold pressor, Fahrenberg et al. ~1987! reported no association of

834

K.A. Matthews et al.

CO across 3 weeks. Kamarck et al. ~1992! found correlations of .70–.78 for PEP, SV, and TPR responses to a tracking task similar to mirror image tracing among White men across several weeks. Finally, in the study most similar to our own, McGrath and O’Brien ~2001! found associations that were fairly high across 1 week ~rs 5 .35 to .72!, except for DBP, which was low ~rs 5 .10 to .23!, and resembled those obtained among the children in our sample across 3 years. Limitations of our study include a relatively short intertask period ~10 to 15 min! dictated by the difficulties of children remaining still throughout a long testing period and the possibility that the cold forehead task reactivity affected reactivity to later tasks. These effects, therefore, would have contributed to increasing the error variance, given the study design of counterbalanced tasks. The number of adolescents in the protocol was small be-

cause of additional eligibility criterion imposed after their initial recruitment and evaluation and because the primary objective of the follow-up evaluation required recruiting additional children ages 8 to 10 years old. Strengths include the multi-ethnic nature of the sample, lengthy follow-up period, and excellent retention rate. In summary, we have found that impedance-derived measures of TPR, CO, and SV and measures of PEP are moderately stable in children and adolescents across a long period of time. The weaker associations for adolescents may be due to sample size. The gender differences in CO and TPR responses to stress are apparent in childhood and males were more stable in TPR reactivity than females. Our laboratory is evaluating the effect of the pubertal transition on impedance-derived responses to stress in order to understand the effects of hormonal regulation on beta-, alpha-, and mixed-adrenergic responses to behavioral challenges.

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