Artigos

INTRODUCTION
High Blood Pressure (HBP) is a major public health problem in the domain of non-communicable chronic diseases, including among younger populations. It has been found that children and adolescents with blood pressure above 120/80 mmHg or 90th percentile for age and sex are at heightened risk of developing hypertension in adulthood, particularly if elevated blood pressure coincides with overweight or obesity.1-3 HBP in this age group has often been overlooked and inadequately managed.4 In 2008, the Brazilian Ministry of Health launched the Study of Cardiovascular Risks in Adolescents (SCRA), with the primary aim of assessing cardiovascular risk factors and estimating the fraction of HBP attributable to obesity among Brazilian adolescents aged 12 to 17 years. The study seeks to inform policy initiatives aimed at mitigating obesity in Brazil.5
Some studies suggest that anthropometric parameters such as body mass index (BMI), waist circumference (WC) and height-to-waist ratio (HWR) may be used to define general and central obesity. Furthermore, research suggests that children and adolescents with a low BMI but with a WC exceeding half their height may also face an increased risk of HBP, indicating that relying solely on BMI measurement may underestimate the risk of high blood pressure. 6-8
The identification and treatment of adolescents with elevated blood pressure (EBP) or HBP, especially when asymptomatic, is challenging. The impact of HBP on cardiovascular health, both in childhood and in early adulthood, can be mitigated by early diagnosis and subsequent lifestyle intervention.4-5,9 The identification of technically simple, accessible, and inexpensive measures that signal an increased risk for HBP, thereby allowing frequent surveillance, can be a useful strategy in public health policies. The present study intends to compare the performance of different anthropometric parameters in the prediction of altered blood pressure in a Brazilian sample of adolescents aged between 13 and 18 years.

METHODS
A cross-sectional study that included adolescents aged 13 to 18 years old attending a high school in Southern Brazil. The project was approved by the Research Ethics Committee of the Federal University of Rio Grande and authorized by the Federal Institute of Education, Science and Technology of Rio Grande do Sul Campus Rio Grande (IFRS - Campus Rio Grande).
The minimum sample size was estimated at 211 participants, plus an addition of 20% (n=42) for dropouts, with a result of a minimum of 253 students. The sample size calculation was based on an expected prevalence of 30% for BP above 120/80 mmHg or 90% percentile, as found by the SCRA5, with a confidence level of 95% and a maximum alpha error of five percentage points.
The project was widely publicized at school and students were invited to participate after brief explanations in the classrooms, with the consent of the teachers. The signing of the Informed Consent Form by the student and his/her responsible was a condition to participate in the research. Those who chose not to participate in the research were considered as refusals and those who were not found after two or three attempts to contact them as losses.
Blood pressure percentile by sex, age and height was the independent variable and the dependent variables included weight, BMI, WC and WCR. The measurements were performed at the school, in an appropriate environment, following standardized procedures according to instructions by the manufacturers of the employed devices. The personnel who collected data were selected among components of the institution's health team and students of the technical course in nursing, before being properly trained by the researchers.
In the first evaluation, a standard questionnaire developed for the Health at School Project and that includes full name, registration number, date of birth and sex was applied. BP was measured twice, about 15 minutes apart, and the average of the two measurements was recorded. Participant’s height, weight and WC were also measured. The BMI calculation was performed by the ratio of weight measurement (in kilograms) to height (in meters) squared. The value obtained was categorized by the Z score, considering age, sex and BMI, according to WHO criteria. To calculate the WHR, the ratio of waist circumference to height (both in centimeters) was used, the result of which varies from zero to one, ideally less than 0.5.
If the BP was above 120/80 mmHg or 90% percentile for sex, age and height, a second BP measurement was performed within 15 days. If the BP measured in the second visit was again above 120/80 mmHg or 90% percentile for sex, age and height, the student was referred, within 15 days, to the institution's outpatient clinic for a new BP evaluation to confirm EBP or HBP, according to the BP classification criteria recommended by the last American Guideline. As this guideline recommends that, for research situations, the diagnosis of EBP and HBP remain being based on blood pressure percentiles until the age of 18 years, these criteria was used for the entire sample evaluated (including those over 13 years of age). Systolic and diastolic BP < 90th percentile was considered as normal, BP ? 90th percentile and < 95th percentile was considered EBP, and BP ? 95th percentile for age, sex and height were considered as HBP. All participants received a report with individual physical data and guidance, including referral for additional investigation and treatment, according to the results of the evaluations.
The percentage of students who participated in the research was evaluated by comparing the total number of enrollments with the total number of registrations in the research (participants and refusals).
Procedures:
Blood pressure measurement: The participants were instructed to avoid the use of stimulant foods and drinks at least 30 minutes before blood pressure measurement, which was performed after five minutes seating with the back supported and the feet on the floor. The measurement was performed on the right arm, due to the possibility of coarctation of the aorta, with the device aligned at the level of the heart according to the manufacturer's instructions. The first and second evaluations used an automatic wrist blood pressure monitor, Omron® (Kyoto, Japan), model HEM 6221, with a position sensor on the device that improves measurement accuracy and validated in 2014.10-11 The third BP evaluation employed standard auscultatory method, using a sphygmomanometer (Tycos, Welch Allyn, USA) and stethoscope (Littmann, 3M, USA).
Measurement of Anthropometric Variables: Height and body weight (with light clothes) were measured using an electronic scale (accuracy of 0.1 kilograms), with a stadiometer attached (accuracy of 0.1 centimeters) model LD 1050 (Leader, São Paulo Brazil). WC was measured using a tape measure model T872 (Wiso, China), with a resolution in millimeters and a length of 1.5 meters. All equipment has certification and validation by the National Institute of Metrology, Quality and Technology.
Statistical Analysis
The variables central tendency and dispersion were described as median and interquartile range (IQR) for nonparametric data, mean and standard deviation for parametric data, and absolute and relative frequencies for categorical data. The comparison of anthropometric variables between normotensive, altered blood pressure and HBP individuals was performed using ANOVA or Kruskal-Wallis. The association between anthropometric parameters and blood pressure was evaluated by the Spearman correlation test. The comparison between the predictive performance of anthropometric variables for EBP and HBP employed the area under the curve in the ROC analysis. An alpha error of less than 5% was considered significant. Statistical analysis was performed using the Stata 15.1 statistical package (StataCorp LP, Texas).

RESULTS
Data were collected from 328 students, 51% female, with a median age of 16 (IQR 16-17) years, 77% within the age range of 16 to 17 years, 22% aged 15 years and 1 % aged 14 years. The median height was 1.65 (IQR 1.60-1.72) m, 1.60 (IQR 1.57-1.65) m in female and 1.72 (IQR 1.66-1.76)) m in male participants. The median BMI was 22.5 (IQR 20.5-25.1) kg/m², with 66% of students within the appropriate weight (35% females and 31% males). Overweight was found in 24% of students, 11.9% of which were female. Obesity was present in 10% of the sample (6% in males). One male student (0.3%), 16 years old, was underweight. The median WC was 77 (IQR 77.3-84.3) cm. WC varied according to biological sex, greater in males, ranging from 59.3 cm to 126.5 cm. The median of WHR was 0.46 (IQR 0.51-0.44), being higher in males. There were 9 (2.4%) losses in the second visits, and 34 (10.4%) losses in the third visit. (Figure 1)
Blood pressure in the first evaluation: The sum of the prevalence of EBP and HBP was greater than 50% if the average of the two BP measurements from the first day was used alone and classified according to the American Guideline percentile table (2017). On this occasion, 39.6% of the sample had normal BP, 22.6% presented EBP and 37.8% had HBP. EBP and HBP were more frequent in males and females, respectively (Table 1). Despite a significant correlation between BP measured on a single day and BP measured on three different occasions (p<0.001), the measurements on a single day correctly classified normotensives in only 45.4% of the sample (18% of students classified as EBP and 23.6% of students classified as HBP on the first day, when evaluated on two other occasions, were classified as normotensive). The correlation coefficient between the mean systolic BP in this first measurement and the anthropometric parameters WC, WHR and BMI were 0.30 (p<0.001), 0.21 (p<0.001) and 0.22 (p<0.001), respectively. The correlation coefficients between mean diastolic BP and WC, WHR and BMI were 0.20 (p<0.001), 0.17 (p=0.004) and 0.14 (p=0.02), respectively.
Blood pressure measured on three occasions: In the classification based on BP measurements on three different occasions, which meets the requirement of the American Guideline (2017), 87% of the adolescents were normotensive and 13% had altered blood pressure, 6% with EBP and 7% HBP. Altered BP was most frequent in male adolescents (p=0.01) (Table 2).
BMI was significantly different between normotensive and altered blood pressure participants, being higher (22.4 [IQR 21.1-26.1]) kg/m² in individuals with EBP or HBP (23.7 [IQR 21.9-28.1]) kg/m², than normotensive participants (22.1 [IQR 20.2-24.6]) kg/m² (p=0.02) (Table 3). The median BMI was even higher (24.6 [IQR 21.2-27.9]) kg/m² among the 44 students who did not attend for subsequent BP measurements (losses). BMI dichotomized into obese or non-obese participants was also significantly different according to BP classification groups (p=0.03) (Table 3). The correlation coefficient between systolic BP in the second and third measurements with BMI was 0.19 (p<0.001) and 0.32 (p<0.001), respectively.
Waist circumference was also greater (80 [IQR 74.2-93.0]) cm in individuals with EBP or HPT (81.9 [IQR 78.5-94.9]) cm when compared with normotensive participants (76.0 [IQR 70.5-82.5]) cm (p<0.001). (Table 3) In the group classified as losses, an even greater WC was observed (84.4 [IQR 72.6-92.5] cm). The correlation coefficient between systolic BP in the second and third measurements and WC was 0.27 (p<0.001) and 0.38 (p<0.001), respectively.
The waist height ratio was 0.46 (IQR 0.43-0.50) in normotensive individuals, 0.49 (IQR 0.45-0.57) in adolescents with EBP and 0.49 (IQR 0.45-0.56) in HBP patients (p=0.006) (Table 3). The correlation coefficient between systolic BP in the second and third measurements with WHR was 0.20 (p<0.001) and 0.31 (p<0.001), respectively.
In the ROC analysis, the area under the curve in the prediction of HBP was 0.71 (95%CI 0.60-0.82) for WC and 0.64 (95%CI 0.51-0.77) for WHR (p=0.02) and 0.65 (95%CI 0.54-0.77) for BMI. There was no significant difference between BMI and WC (p=0.15) or WHR (p=0.72) in the prediction of HBP (Figure 2). In the EBP prediction, the area under the curve for WC was 0.63 (95%CI 0.48-0.78), for WHR was 0.65 (95%CI 0.49-0.80) and for BMI was 0.59 (95%CI 0.45-0.73), with no significant differences between anthropometric parameters.

DISCUSSION
The present analysis found that simply measuring the waist circumference may be as informative as weighing and measuring to calculate the BMI or measuring the stature to calculate the height-to-waist ratio, in terms of assessing the risk for altered blood pressure among Brazilian adolescents.
Costa et al. published a cross-sectional study of Brazilian adolescents, 66% of them women, mean age of 16.8 years and found that WC and male sex are strong indicators of cardiovascular risk. 3 Bozza et al. also found a positive association between WC and high blood pressure in their study of young people from Curitiba, Brazil, 15 the same finding by Quadros et al.14 Therefore, both confirm the findings described here regarding the association between WC, male sex and obesity with EBP or HBP. In the sample studied by Bozza, et al.15 the association between BP and BMI was not evaluated. Beck et al., however, found, in a southern Brazilian city, higher BP values in males and individuals with higher BMI, with BP evaluated in up to three measurements on different days. 23 In a study by Zhang, Zhao and Chu, the authors found a higher prevalence of HBP in a group of Chinese children and adolescents with low BMI and high WC. 6 Aguilar-Morales et al. found a better predictive ability of REC for dyslipidemia among Mexican children.7 A systematic review also suggests that WC, WCR and BMI are useful in the early identification of individuals at higher risk of developing EBP and HBP. 8
In the ROC analysis of the present sample, WC presented a discretely greater AUC than WCR and BMI, attaining statistical significance only against WCR. The greater association of WC with HBP may mean that visceral fat, better evaluated by this measure, may have a greater impact on blood pressure, or that BMI, as it does not differ between lean and fat mass, may not be a so good marker for obesity. It is interesting to note that the WCR, adjusting WC for height, did not show superior performance to WC alone in predicting altered blood pressure, perhaps due to the sample being almost all the same age.
Another interesting finding from this study, despite not being our primary outcome, was the prevalence of elevated BP and high blood pressure was greater than 50% if the average of the two BP measurements from the first day was used alone and classified according to the American Guideline percentile table (2017). On this occasion, only 39.6% of the sample had normal BP, 22.6% presented EBP and 37.8% had HBP. EBP and HBP were more frequent in males and females, respectively (Table 1). Despite a significant correlation between BP measured on a single day and BP measured on three different occasions (p<0.001), the prevalence of altered BP was above 50% when the diagnosis was based on BP measurements on a single day, and this figure was reduced to values around 10% when the diagnosis was based on BP measurements on three different occasions. Therefore, as expected, the single-day measurement overestimated the prevalence of EBP and HBP. There was no significant difference between anthropometric parameters in their performance as predictors of altered blood pressure, although waist circumference performed slightly better in terms of areas under the curve and correlation coefficients.
According to the 7th Brazilian Guideline 13, the prevalence of hypertension among children and adolescents has doubled in the last 20 years, and varies from 3% to 5%, while the prevalence of prehypertension (now elevated BP) is between 10% and 15% (according to criteria of the 2004 American Guideline and BP measurements on three occasions). In the analysis of the present study, using the American Guideline 201712 as a reference, the prevalence was 7% and 6% for hypertension and elevated blood pressure, respectively.
A study conducted between 1999 and 2012, using data from the National Health and Nutrition Examination Survey (NHANES) and a single BP measurement, found a higher prevalence of above-normal BP among boys (15% to 19%) than in girls ( 7% to 12%), difference attributed to height variation, with higher values among adolescents.12 The same author describes a real prevalence of HBP of around 3.5% and EBP of 2.2% to 3.5% in children and adolescents when measurements are repeated in a clinical setting, with higher rates in overweight participants. The difference between the rates of altered blood pressure found according to the number of measurements at different times has been attributed to the inherent variability of BP or to the accommodation effect (adaptation to the experience of measuring BP).12
For every five children evaluated by NHANES, one would have an indication to be re-evaluated on two more occasions on different days to confirm the diagnosis. The results of the present study, with BP measurements on up to three different days, showed a clear reduction in the prevalence of altered pressure throughout the reassessments. The difference in BP between the sexes was also evident in the analyses, as well as the association of altered blood pressure with obesity. Another study among adolescents aged 10 to 17 years found a prevalence of 35.2% (95% CI 31.9-38.6) for BP above the 95th percentile using only one measure, figures almost as high as those in the present study.14 Another one found an altered BP prevalence of 18.2% (95% CI 15.2-21.6) among Brazilian adolescents, with BP measured on two consecutive days.15
In April 2019, the Guidance Manual of the Scientific Department of Nephrology of the Brazilian Society of Pediatrics began to recommend the use of the American Guideline percentile tables (2017) in the assessment of blood pressure in children and adolescents.16 This guideline presents new percentile tables for individuals aged 1 to 17 years, based on data from the same population and using the same methods used by the Fourth Report (2004)17, but excluding overweight or obese children and adolescents, due to the influence of excess weight in the occurrence of EBP and HPT. In addition, it recommends that, in clinical practice, cutoff points for adults should be adopted from 13 years of age onwards, to align pediatric guidelines with those of adults and facilitate conduct in the transition from adolescence to adulthood.12 Also, the change of the term prehypertension to EBP in the American Guideline (2017) also aims to align with the guidelines for adults. However, in research situations, the Guideline recommends that the percentile classification should continue to be used until the age of 18, for precision in the BP classification. The BP reclassification studies according to the changes incorporated with the American Guideline (2017) confirmed the trend of increasing prevalence of HBP among male adolescents.18,19 The comparison of BP classification with the American guidelines (2004 and 2017), found a small proportion of children reclassified to EBP or HPT.20 Several recent studies confirm that the use of the American Guideline (2017) results in an overall increase in the prevalence of hypertension, particularly in obese young people, as the guideline better classifies those overweight or obese, corroborating the finding of the present study.
The present study has some limitations, such as the loss of 13% of participants who had their BP measured on the first day and did not return for subsequent measurements. It was observed that individuals classified as losses had greater WC, and that their inclusion would potentially increase the real prevalence of ABP. Another limitation was the measurement of anthropometric parameters and BP assessment on the same day as the questionnaire, which may have caused some discomfort in the students due to psychosocial questions, determining higher blood pressure levels, which may have reduced in the subsequent measures. Finally, it is noteworthy that the use of a wrist oscillometric device is not the method recommended by guidelines to measuring BP, despite this technique speeds up screening by people trained outside the health area. However, cases of altered BP were checked with an aneroid or arm oscillometer device in the third BP evaluation, as established by the guideline.
As a strong point of the study, the measurement of blood pressure in three different visits, with standardized time intervals, which minimizes the possible effects of white coat hypertension, the effect of accommodation and natural anxiety in adolescents. In addition, the use of the 2017 American Guideline as a reference for BP percentiles tends to increase the accuracy in detecting the weight effects on blood pressure.
As other national surveys have shown, 3,14-15,24 the SCRA results also point to important regional contrasts, probably because they present different designs in terms of data collection. However, everyone agrees that excess weight, measured by BMI or WC, is associated with altered blood pressure. Obesity therefore represents an important modifiable cardiovascular risk factor, and preventive measures aimed at lifestyle should be implemented. In addition, single-day BP measurement cannot be used for the clinical diagnosis of ABP. The single measure has unquestionable value in large population surveys, such as the North American NHANES and SCRA in Brazil, focused on assessing regional contrasts and/or temporal trends, but it should never be used in the clinical diagnosis of the individual patient or to motivate therapeutic approaches.

CONCLUSIONS
The measurement of waist circumference, a simple and low-cost procedure, depending on a simple measuring tape, presented a performance similar or possibly superior to other more complex parameters in the prediction of risk for altered BP. Blood pressure measurement on a single occasion is not adequate for blood pressure classification in clinical practice. Although the three visits are recommended by all guidelines, there are still many clinical publications based on blood pressure measured once. The present findings therefore suggest that the measurement of BP and anthropometric parameters should be included in the clinical routine of pediatricians.

REFERENCES
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