DURING the growth and maturation associated

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1 Blood Pressure in Childhood The National Health Examination Survey WILLIAM R. HARLAN, M.D., JOAN CORNONI-HUNTLEY, PH.D., AND PAUL E. LEAVERTON, P H.D. SUMMARY Data were analyzed from the U.S. Health Examination Surrey (Cycle II) to determine relationships between blood pressure and other characteristics. This survey examined a national probability sample of children aged 6-11 years. Signifkant relationships were found for blood pressure and the following variables: chronological and skeletal age, skinfold thickness (adiposity) and other anthropometric measurements, pulse rate, and systolic murmurs. These relationships may be interpreted as indicating important relationships between blood pressure and growth, adiposity, and hemodynamic manifestations of cardiac output. Data from this representative population portray blood pressure relationships in childhood. (Hypertension 1: , 1979) KEY WORDS nationally representative population epidemiology blood pressure childhood body mass physiological maturation systolic murmurs DURING the growth and maturation associated with childhood and adolescence, blood pressure increases. Despite the generally held concept that primary hypertension may have its roots in these early years, it is not possible to define whether the blood pressure changes that occur with growth are entirely physiological or portend later development of high blood pressure. Identification of attributes that place a youth at increased risk of high blood pressure can have important implications for prevention, recognition, and early treatment of hypertension. Several studies 1 ' have explored the ranges of systolic and diastolic pressures in children and adolescents, and recommendations regarding "normal" and "high" levels of pressure have been proposed. 4 Additionally, investigators have examined characteristics with different levels of blood pressure and attempted to sort out the relative contributions of factors, genetic and environmental, that may produce blood pressure changes in the growing child that may be attributed to physiological maturation. However, these studies have been confined to limited and, in some instances, special population groups not neces- Presentcd in part at the Annual Meeting of the American Heart Association, Miami, Florida, November, Dr. Cornoni-Huntley's present address: National Center on Aging, Bethesda, Maryland 20pi4. Dr. Leaverton's present address: Director of Research, National Center for Health Statistics, Hyattsville, Maryland Address for reprints: William R. Harlan, M.D., G-1209 Towsley, Medical School, University of Michigan, Ann Arbor, Michigan sarily representative of the entire United States. The present study analyzes data from a representative population in which a broad range of relevant characteristics were measured. The United States Health Examination Surveys (HES) afford a unique source of data with which to explore the influences of demographic and physiological factors on blood pressure in growing children. These surveys carefully examined a large, nationally representative sample of children 6-17 years of age and measured a broad range of potentially relevant variables. Data from these examinations were analyzed to determine the relationships between blood pressure and pertinent demographic, social, developmental, and physiological characteristics. The findings from these surveys portray the behavior of blood pressure in youth and suggest physiological and pathologic mechanisms that may determine pressures during youth. This report examines blood pressure in children aged 6-11 years and a subsequent report deals with adolescents aged years. 6 Materials and Methods Surrey Population and Methods The Health Examination Survey, Cycle II, was based on a nationwide probability sample representing noninstitutionalized children, aged 6-11 years, of the United States but excluding Hawaii and Alaska. The sample is representative with respect to age, sex, race and geographic region. Of the 7417 children 559

2 560 HYPERTENSION VOL 1, No 6, NOVEMBER-DECEMBER 1979 selected for the sample, 7119 (96%) were examined. Primary sampling units were either a single county or a group of contiguous counties. Secondary sampling units were household clusters. Finally, households within clusters were selected, and children within the 6-11 age range were interviewed and examined. Fiftyone percent of the children were male. There were 6100 whites and 987 blacks; 32 children of other ethnic backgrounds were excluded from our analyses because of the small number.'' 7 Examinations were performed from 1963 to Each child was given a standardized examination providing information on health and behavior characteristics. The examination included a physical examination given by a pediatrician assisted by a nurse, a dental examination given by a dentist, behavior tests administered by a psychologist, and other tests and measurements performed by laboratory and x-ray technicians. Anthropometric measurements, vision, and hearing tests were included. Prior to the examination, socioeconomic and demographic data were gathered from the parents or an adult living in the household. A medical history and information on behavior characteristics were also obtained at this time. A standard manual of operations was developed to cover all aspects of the examination. 7 The details regarding measurement and the distribution of these variables are described in several publications,"* 10 and only those measurements germane to the present report are described in detail. Two blood pressure measurements were made, the first at the beginning of the examination and the second near the conclusion, just after obtaining a resting electrocardiogram. The pressures were recorded in the supine position by nurses using a mercury sphygmomanometer and either a 9.5-cm pediatric cuff or a 13-cm adult cuff. The cuff size was selected to be at least 20% wider than the arm diameter or cover approximately two-thirds of the arm. Readings were made to the nearest 2 mm Hg and cessation of sound (fifth Korotkoff phase) was taken as diastolic pressure. In the usual instance when there was no loss of sound, the point of muffling (fourth Korotkoff phase) was used. The two blood pressures were averaged for subsequent analysis. The first measured blood pressure was higher than the second by 3.6/1.7 mm Hg (medians). Detailed aspects of blood pressure methodology and observed agreement are described elsewhere and can be summarized as indicating that there was good agreement among the four nurses. 8 Analysis of data from the individual nurses indicated that their recording differences, although small, did not bias the results of the study with respect to race, sex, or body stature and digit preference was not important. 8 was obtained by a nurse at the conclusion of the cardiovascular examination. During the examination, the pediatrician recorded all murmurs. Based on the murmur characteristics (intensity, character, duration, and timing) and the location and associated findings (thrills, abnormal heart sounds) and electrocardiograms and chest radiographs, the pediatrician made an assessment of the murmur. The murmurs were classified as "significant," "possibly significant," or "innocent." These designations of murmurs were made by the examining pediatrician and reflect his/her assessment of the likelihood that the murmur was associated with cardiovascular disease. The "significant" murmurs were louder and thought to be associated with underlying disease; the "innocent" murmurs were soft and felt to be benign; and those "possibly significant" represent murmurs that could not be placed in either category. s were detected in 27% of the children and diastolic murmurs in less than 1%. In the children, 3.5% of the murmurs were classified as "significant" or "possibly significant" and the remainder as "innocent." There were no significant differences in the prevalence of murmurs in the two races (26.7% for white children and 26.0% for black children). 9 For this analysis, the "significant" and "possibly significant" categories were grouped together into a single category, "possibly significant" because no follow-up data were available to confirm the importance of the findings. Height was measured in stocking feet with back and heels against an upright height scale. of the partially clothed subject was measured on a Toledo self-balancing scale that mechanically printed the weight to a tenth of a pound directly on the permanent record. Anthropometric measurements and skinfold thickness were obtained using conventional methodology. Measurements of skinfolds were taken at triceps, subscapular, and maxillary ("lateral chest wall") areas using Lange skinfold calipers and recorded to the nearest millimeter. Two measurements were made to the nearest half-millimeter, and if discrepencies occurred, a third measurement was made. 10 was determined from a radiograph of the right wrist and hand by comparing the film with selected standards from the Gruelich and Pyle atlas. 11 Data Analysis Two strategies were used in analyzing the data. First a series of hypotheses were specified a priori from other studies in children and adults. Relationships between systolic and diastolic blood pressures and the following variables were examined: age, sex, race, height, weight, skinfolds, skeletal age, anthropometric measurements, geographic region, urban/rural residence and socioeconomic status. Relationships were tested using Student's t tests, chisquare tests and F tests where appropriate. The interaction of variables was examined by controlling for one variable while examining the other variables under study. All variables found to have a significant relationship with blood pressure were entered into a multiple stepwise regression analysis to predict the dependent variables, systolic or diastolic blood pressure. The distribution of all continuous variables was examined and, where necessary, a logarithmic transformation was made to achieve a normal distribution.

3 BLOOD PRESSURE IN CHILDHOOD/ffaWa/i et al. 561 Results Mean systolic and diastolic blood pressures were found to increase with age for each sex-race group (fig. 1). In contrast to the findings in a similar survey of adults, 12 the mean systolic pressures in black children tended to be lower than for white children. However, the diastolic pressures were higher in black children, notably in black boys. The differences in diastolic pressures are statistically significant and consistent throughout the age range. Further analysis of blood pressure distributions by age, race and sex are available. 8 Systolic and diastolic pressures correlated significantly with many anthropometric measurements, skeletal age and several hemodynamic assessments. These relationships were consistent within each age-sex-race group, although the strength of the relationships varied, generally being least for black males. Because of the multiple intercorrelations of these variables, simple correlations are not presented. Multiple stepwise regressions of these variables on systolic pressure afford a more efficient means of establishing which variables make a unique contribution to explanation of variance in blood pressure. The multiple regressions for each race-sex group are presented in tables 1-4. Several regressions were computed for each group by deleting or substituting independent variables that were closely interrelated. was consistently the first variable selected and accounted for the major amount of explained variance in blood pressure (tables 1 and 2) when all variables were included. However, in growing children weight reflects a number of separate changes including growth, adiposity and physiologic maturation. Therefore, we substituted measures of these individual features but did not include weight in the regressions calculated in tables 3 and 4., skinfold thickness, pulse rate and systolic murmurs were selected in multiple regressions when weight was not included as an independent variable. Only variables contributing 1% or more to explanation of variance are listed. The results from both analyses are similar for all race-sex groups. In similar computations, weight/height 2 (Quetelet's Index) was found to substitute for skinfold thickness without loss of prediction. (or weight/height 2 ) and pulse rate were the variables that consistently predicted diastolic pressure. A greater amount of variance (r*) could be explained for systolic pressure as compared to diastolic, partially because the variance of systolic pressure is greater. Separate analyses were performed for important categorical variables. s related to WHITE BLACK SYSTOLIC DIASTOLIC 6 7 i II 6 AGE IN YEARS 8 10 II o o FEMALES ' MALES FIGURE 1. Mean systolic and diastolic blood pressures for children in Cycle II of the National Health Examination Survey. Dotted lines = females, solid lines = males.

4 562 HYPERTENSION VOL 1, No 6, NOVEMBER-DECEMBER 1979 TABLE 1. Multiple Stepwise Regression of Selected Variables on Systolic and Diastolic Blood Pressure in Males 6-11 Years of Age Variable r 1 White males Diaetolic BP /height 1 Black males systolic blood pressure in each sex-race group in the age ranges 6 to 8 years and 9 to 11 years (fig. 2). There was no relationship between systolic murmurs and diastolic pressure. When the groups were divided according to the presence and intensity of murmurs ("no murmur," "innocent murmur" and "possibly significant murmur"), there were statistically significant trends in systolic pressure. Significant relationships persisted when pulse rate and chest wall thickness (chest skinfolds) were controlled. Differential and TABLE 3. Alternate Regression Model in Males 6-11 Years of Age Deleting? Variable r* White males Black males Diaatolic BP * deleted as an independent variable. / height 1 was equivalent to skinfold thickness in each prediction. TABLE 2. Multiple Stepwise Regression of Selected Variables on Systolic and Diastolic Blood Pressure in Females 6-11 Years of Age Variable r* White females Diaetolic BP Black females Height Height potentially biased recording of murmurs and blood pressures by the various physician/nurse examiner teams was explored as a possible explanation for this finding. Data from each of the 37 examiner teams were analyzed separately. The overall relationship between murmurs and systolic pressure was not refuted by individual examiner data. Analysis of other examination variables and demographic characteristics revealed only one significant relationship with blood pressure. Systolic blood TABLE 4. Alternate Regression Model in Females 6-11 Years of Age Deleting? Variable r* White females Height Black females Height * deleted as an independent variable. / height 1 was equivalent to skinfold thickness in each prediction.

5 BLOOD PRESSURE IN CHILDHOOD/#ar/an et al. 563,20 WHITE FEMALES WHITE MALES BLACK FEMALES I BLACK MALES 115 E MO CO CO 105 o 2! AGE IN YEARS MURMUR ft"innocent" MURMUR >"POSSIBLY SIGNIFICANT" MURMUR FIGURE 2. Relationship between systolic blood pressure and the presence and intensity of systolic murmurs. The standard error of mean is indicated by the brackets at the top of each bar. pressure was slightly (approximately 1 mg Hg) higher in the southern region and diastolic pressure slightly higher in the middle-western region (p < 0.01) for each sex-race group. Although specifically sought, no relationship was found for systolic or diastolic blood pressure and the following: Population density (urban/rural or population of residence) Family income level Educational attainment of parents Intelligence quotient of subject Reported history of renal disease Hearing levels by audiometry. Discussion Data from this survey, which is based on a national sample of children, afford interesting comparisons with adult studies and provide insights into the determinants of blood pressure in growing children. Blood pressure increases with age, and systolic pressure tends to be higher in white males and females than in black children of the same age. Similar blood pressures and age trends have been reported in children of the same age range. 1 ' 1 " u Even in primitive societies, a rise in blood pressure occurs during childhood, but blood pressure rarely increases after adolescence in these societies, and high blood pressure is unusual. 16 ' 16 Therefore, in seeking adult precursors of hypertension, it is necessary to discriminate between factors related to maturational rises in blood pressure (physiological factors) and potentially pathological factors responsible for blood pressure increases. These latter factors might be the precursors of hypertension. The variables related to blood pressure in children may be grouped into three, not mutually exclusive, categories: growth, body composition and hemodyrtamic variables. Childhood growth reflects both an increase in body size and physiological maturation. Data from this survey and that of adolescents indicate that physiological maturation is more closely related to blood pressure than chronological age. There are both direct and indirect measurements of maturation on which to base this statement. is a direct measure of physiological maturation and more accurately describes the progression toward adult development than chronological age. 17 is more consistently related to blood pressure than chronological age. The data of Voors et al. a '" also infer a relationship between physiological age and blood pressure, although the measurement is less direct. They found height to be a more important correlate of blood pressure in growing children than age. Because height is also a measure of progression toward attainment of adult size, one would expect this relationship

6 564 HYPERTENSION VOL 1, No 6, NOVEMBER-DECEMBER 1979 to hold. It would, however, be a less precise measure of physiological maturation because final height will vary individually. In comparative analysis using the HES data, height was predictive only when skeletal age was deleted from analysis. was consistently correlated with blood pressure in these analyses (tables 1 and 2), but in growing children this factor reflects growth and adiposity. Therefore, in our analyses, we sought to sort out the influences of each component and found an effect of both physiological maturation and adiposity. These observations are compatible with the biological inference that growth and increasing body size are associated with cardiovascular adaptation that includes increasing blood pressure. In adults, there is no association between blood pressure and skeletal size or lean body mass; this suggests that this change is a physiological response to growth and maturation and probably does not forecast a risk for adolescent or adult hypertension. The relationship of blood pressure to body mass is complex. Body mass index (weight/height 2 or other indices) is an indirect assessment of several body components (adipose, muscle and skeletal tissue). The inclusion of height provides some correction for size and growth. Sorting out the independent contributions of these components is facilitated in the HES data because skinfold thickness, an estimate of subcutaneous fat, was measured. is related to blood pressure in children, and this relationship persists after controlling for age (skeletal or chronological) and for height. In these analyses, skinfold thickness was highly correlated with weight/height 2 (Quetelet's Index) and the two variables were interchangeable in their ability to predict blood pressure. A similar relationship between adiposity and blood pressure is present for adolescents and adults.' 11B Therefore, this relationship during childhood may have important prognostic significance, particularly since relative body fatness persists as children progress through adolescence. 20 ' 21 For example, in these studies rank-order correlations range from 0.69 to 0.75 for skinfolds and from 0.80 to 0.86 for height, which is generally accepted as a persistent rank-order characteristic for growing children. Two hemodynamic characteristics, pulse rate and systolic murmurs, were found to be related to blood pressure levels. These relationships are independent of other factors, such as body size, and are found in each age-sex-race group. Other studies of children and young adults have demonstrated a consistent, direct relationship between pulse rate and systolic pressure. 22 ' M The relationship of pulse rate to diastolic pressure is generally not as strong, although it was a significant predictor in the present studies. These observations and physiological studies of patients with "early" or "labile" high blood pressure have suggested that increased cardiac output is an important hemodynamic alteration in early hypertension." The increased cardiac output has been attributed to increased pulse rate, as well as increased stroke volume. Both these physiological observations and the epidemiological studies reassert the importance of the heart in blood pressure regulation. The association between systolic murmurs and systolic pressure was unexpected but consistent in children and youths.' Potentially confounding factors that might explain the relationship were examined, but pulse rate, body size, chest wall thickness, and observer bias were not responsible. Cross-sectional studies in adults also reveal a relationship between systolic murmurs and blood pressure (personal communication with J. Cornoni-Huntley on data from the U.S. Health Examination Survey I on adults). Despite the difficulty in standardizing physician assessment of murmurs and changing presence and intensity of murmurs, the relationship in cross-sectional examinations seems consistently present. However, the murmurs may be transient and the relationship evanescent, with no prognostic significance. A follow-up review of these children in Cycle III of the Health Examination Survey indicates that this is probably the situation. 6 One of the unique attributes of these surveys is the nationally representative nature which permits exploration of a broad range of potentially important demographic variables with little likelihood that biased selection will prejudice the findings. Relationships between blood pressure and socioeconomic status, educational attainment of parents, intelligence of subject, and population density (urban/rural) were sought but not found. Geographical region was associated with minor, but statistically significant, blood pressure differences, but these differences were not present in the subsequent survey (HES III), suggesting that they do not indicate important or consistent biological trends. 18 Physiological variables appear to be more important than demographic factors. Despite an exhaustive analysis of an extensive range of variables, less than half of the blood pressure variance could be explained, and this has been true for other studies in children. 1 ' 18 The remaining unexplained variance probably includes genetic factors, neurogenic variability during examination, and other unknown factors. Nevertheless, this survey and the other studies agree on factors that may have predictive value for subsequent blood pressure. These studies, because of their cross-sectional nature, do not indicate which relationships between blood pressure and other characteristics are "physiologic" and which have prognostic importance for subsequent high blood pressure. From childhood through late adulthood, adiposity and pulse rate are consistently found to be related to blood pressure. Longitudinal observations will be required to determine whether this has predictive value for subsequent blood pressure. Long-term studies 19 ' M support this thesis for young adults, but longitudinal observations in children are necessary to determine whether these characteristics are also predictive during childhood. On the other hand, skeletal size is not related to blood pressure in adults, and other studies are consistent with the thesis that blood pressure differences associated with childhood growth and lean body mass have no long-term implications for blood pressure.

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