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Obesity and season as determinants of high blood pressure in a school-based screening study

Abstract

This school-based screening study assessed the prevalence of high blood pressure (BP) levels according to the European Society of Hypertension (ESH) 2016 guidelines. Moreover, risk factors for BP elevation, and the effect of geographic and seasonal factors on BP screening were investigated. BP and anthropometric measurements were obtained from 2832 children and adolescents, aged 6–18 years, during the period 2013–2016. Three BP measurements were performed using a mercury sphygmomanometer, and the mean of the last two was used for the analysis. Obesity was defined according to the International Obesity Task Force (IOTF) criteria. The prevalence of high–normal BP/hypertension and overweight/obesity was 3.7%/0.9%, and 22.9%/8.5%, respectively. The majority of the participants presenting high BP (≥90th percentile) were overweight or obese. Increased prevalence of high BP was observed during spring (5.5%) and winter (5%) compared with 2.5% in autumn (P<0.05). SBP z scores were higher in males, during spring and summer, and in urban areas. In conclusion, a low rate of high–normal and hypertensive BP levels was found despite the high prevalence of overweight and obesity. Overweight and obesity were associated with higher BP levels, but there was also a seasonal difference in the prevalence of high BP levels.

Introduction

Hypertension (HTN) in children is a condition with increasing interest due to its escalating prevalence and its potential adverse consequences [1], such as target organ damage already occurring during childhood [2], and the appearance of cardiovascular disease in adulthood [3]. Overweight and obesity are significant risk factors for cardiovascular morbidity and mortality. In several countries, the rise in childhood obesity causes concerns for future life expectancy [4].

Τhe increasing trends in blood pressure (BP) values are significantly, but not exclusively, attributable to the constant increase of childhood obesity. Other factors, such as environmental, socio-economical, seasonal, and geographical can affect BP values and the prevalence of HTN [5]. There is a plethora of epidemiological studies assessing the prevalence of HTN and investigating the effect of possible risk factors in BP values. The comparison of their conclusions is difficult, because the studied populations, regarding age, lifestyle, ethnicity [6, 7], and the methods for BP measurement (i.e., auscultatory or oscillometric, the number of BP readings used) [8] vary a lot across the studies. Moreover, the lack of unified BP references for determining elevated BP does not permit international comparisons of elevated BP in children and adolescents.

The current school-based study aimed to assess the prevalence of high BP levels according to the European Society of Hypertension (ESH) 2016 guidelines [9], and to investigate risk factors for BP elevation in childhood and adolescence. Moreover, geographical and seasonal risk factors were investigated for their effect on BP population screening.

Subjects and methods

Design and population

A cross-sectional, school-based population BP screening study was performed in the county of Kastoria; a region of Northern Greece with ~50,322 inhabitants, 46 primary and high schools currently operating, and 4924 registered students, aged 6–18 years old. The Greek Ministry of National Education, the National Educational Institute, and the Ethics Committee of the Aristotle University of Thessaloniki approved the study protocol.

All schools in the county were included in the study. Approval from the school directors was obtained. A detailed letter explaining the aims of the study and a consent form for participating in the study were sent to all parents or guardians. The population sample included children and adolescents, whose parents/guardians gave their informed consent to participate in the study. In case of adolescents, an informed consent from the adolescents themselves was also obtained. The participation rate was 57.5%. There were no specific exclusion criteria apart from refusal to participate in the study.

A trained, experienced pediatrician, and a trained researcher, both members of the research team, visited all 46 schools during the period September 2013–June 2016. At the screening visit, the pediatrician explained to the students the purpose of the study and the following procedure. Their examination was performed in a quiet, tempered room. Two students were entering the room and resting in a seated position for 5 min. Personal history, birth weight (BW), and gestational age (GA) were obtained of a subset of the population from the children’s birth certificates and medical records that the parents were instructed to bring during the scheduled school visits.

BP measurement

A mercury sphygmomanometer (Riester diplomat-presameter CE 0124, Rudolf Riester GmbH, Jungingen, Germany) was used for the BP measurement. Different cuff sizes were available. Specifically, the mid-arm circumference was assessed and the correct cuff size was used, so that the bladder length was 80–100% of the circumference of the arm, and the width was at least 40%. BP was measured on the right arm to the nearest 1 mmHg with the student quiet, seated with the back supported, and feet uncrossed on the floor after a 5-min rest. The trained pediatrician measured BP thrice with a 2-min interval, and the last two BPs of this single occasion were averaged for the analysis.

BP groups were stratified according to the ESH 2016 staging scheme for children and adolescents. Children aged 6–15 years old with systolic BP (SBP) and/or diastolic BP (DBP) ≥ 95th percentile for sex, age, and height were classified in the hypertension group. If the SBP and/or DBP was ≥ 90th percentile but < 95th percentile, the children were defined as having high–normal BP. For adolescent boys and girls older than 15 years old, the cutoffs for high–normal BP and hypertension were 130–139/85–89 mmHg and ≥140/90 mmHg, respectively. Isolated systolic hypertension (ISH) in children was defined if SBP≥95th percentile and DBP<90th percentile, while in adolescents older than 15 years old was defined if SBP≥140 mmHg and DBP<90 mmHg [9].

Anthropometry

Body weight was measured to the nearest 0.1 kg with students in light clothes without shoes using an electronic weighing scale (Seca 877, Hamburg, Germany), and height was measured to the nearest 0.1 cm using a portable fixed stadiometer (Seca 213, Hamburg, Germany) with students standing without shoes, their shoulders in a relaxed position, their arms hanging freely, and their head aligned in Frankfurt Horizontal plane.

Waist and hip circumference were measured with a non-elastic measuring-tape to the nearest 0.1 cm. Waist circumference was measured on the navel level at minimal respiration. Hip circumference was measured at the widest point, above major trochanters of the femur.

Body mass index (BMI) was calculated by dividing weight (kg) by height squared (m2).

Overweight and obesity were defined according to the International Obesity Task Force (IOTF) criteria [10]. The international cutoffs for overweight and obesity are based on the country—averaged centiles corresponding to BMI 25 and 30 at 18 years of age, respectively.

Children with recorded BW and GA were classified as small for gestational age (SGA)-preterm, appropriate for gestational age (AGA)-preterm, SGA-term or AGA-term, according to the United States-based BW for GA ref. [11].

Statistical analysis

The IBM SPSS 24.0 (SPSS Inc, Chicago, IL, USA) statistical package was used to analyze the data. Standard descriptive statistics, t test or non-parametric methods were used as appropriate for the comparison between the groups. Linear regression analysis was performed to determine the risk of high BP by covariates. Univariate general linear models were used to examine the effect of sex, obesity, season of screening, and school area (city/rural) on BP levels. Estimated marginal means after adjustment for multiple comparisons by Bonferroni were used to assess for differences on BP levels between sexes, weight groups, season, and school area of BP screening. A P-value <0.05 was considered statistically significant.

Results

The study population included 2832 children and adolescents aged 6–18 years old. Anthropometric and BP data are described in Table 1. The prevalence of high–normal BP and HTN in the population was 3.7% and 0.9%, respectively, according to the ESH 2016 BP classification.

Table 1 Demographic and clinical data of the population

Thirty-one percent of the population were overweight (22.9%) or obese (8.5%). The majority of the participants with high BP (≥90th percentile) had excess body weight. Particularly, 56.1% of the participants that presented high–normal BP, 55.5% of the participants with hypertensive BP levels, and 66.7% of the participants with isolated systolic hypertensive BP levels were overweight or obese (Fig. 1). Both the highest prevalence of overweight–obesity and high BP levels were found in 6–12 years old group children (62% vs. 38%, P<0.001 for overweight–obesity, and 72.9% vs. 27.1% P = 0.05 for BP levels ≥90th percentile for age, sex, and height) (data not shown). The highest prevalence of high–normal (12.5%) and hypertensive BP levels (2%) was observed at 6th grade children (Fig. 2). There was a linear increase of SBP z score with increasing BMI z score (P = 0.000, R2 = 0.051), but not for DBP z score (Fig. 3). Obese and overweight children presented a 3.15 times increased likelihood to have high–normal BP or HTN (95% CI 2.21–4.49, P<0.001).

Fig. 1
figure1

Prevalence of high BP classification by BMI groups

Fig. 2
figure2

Prevalence of high–normal BP and hypertension, overweight (OW), and obesity by grade

Fig. 3
figure3

Linear association between BMI z score and BP z scores

High BP levels prevalence did not differ by sex, BW, or gestation week. Prevalence rates for high BP were similar in urban and in the surrounding rural schools (5.2% vs. 4%). Increased prevalence of high–normal or hypertensive BP levels was observed during spring (5.5%) and winter (5%) period, compared with 2.5% in autumn (P<0.05) and 4% in summer. There was no difference in the prevalence of overweight and obesity between urban and rural areas, or among seasons of screening.

Univariate analysis with dependent variables SBP and DBP z scores showed that season of BP screening had a positive significant effect on SBP and DBP z scores after adjustment for grade. Male sex, overweight, and obese groups presented also significant positive associations with SBP and DBP z scores, while living in the city area was associated only with higher SBP, but not with DBP z scores. BW groups did not show any associations with BP z scores (Table 2). Based on estimated marginal means after adjustment for grade and BMI z score, SBP z scores were higher in males compared with females, during spring and summer compared with winter and autumn, and in the city compared with rural areas (Table 3 and Fig. 4).

Table 2 Univariate analysis for the association between BP z scores and sex, BMI groups, birth weight groups, season of BP screening, and school area
Table 3 Mean difference in SBP and DBP z scores based on estimated marginal means after adjustment for multiple comparisons by Bonferroni
Fig. 4
figure4

Mean SBP and DBP z scores based on estimated marginal means by (a) school area adjusted by grade and BMI z score, (b) season of BP screening adjusted by grade and BMI z score, (c) sex adjusted by grade and BMI z score, and (d) BMI group adjusted by grade

Discussion

This study estimated the prevalence of high–normal BP and HTN in Northern Greece at 3.7% and 0.9%, respectively, based on the ESH 2016 guidelines for the management of high BP in children and adolescents staging scheme. The reported prevalence of high–normal BP and HTN in screening studies from Europe and North America varies from 3.1% to 36.8% and from 1.6% to 7.9%, respectively [12,13,14]. Particularly, the prevalence of elevated BP in studies from Greece varies between 5.2 and 40% [15, 16]. In our study, the highest prevalence of high BP levels was observed at 6th grade children, aged 12 years old. Similarly, in a previous study, which reported a high prevalence of high BP levels in Greek students, the study population was 9–13 years old [16]. These findings imply that the prevalence of high BP levels is higher in younger age groups than in adolescence in Greece, and may be attributed to the higher prevalence of overweight and obesity in the younger age group.

The prevalence of overweight and obesity was found 31% in the study population. Other Greek studies demonstrated a similar prevalence of overweight/obesity ranging from 30 to 40% [15, 16], which is among the highest in the developed countries [4]. Childhood overweight and obesity are considered an epidemic problem during the last decades [4], although a recent pooled analysis of 2416 population-based studies showed that the escalating trends in children’s and adolescents’ BMI have reached a plateau in many developed countries [17]. Μany studies have documented an association between BP and BMI in children and adolescents and have indicated that BP levels in children have increased in parallel with the increasing prevalence of obesity [6, 14, 18, 19]. In line with these studies, the current study showed that BP is associated with BMI independently of sex, age, and height. The majority of participants with high BP (≥90th percentile) were overweight or obese. Obese and overweight children had increased likelihood to have high–normal BP or HTN. Further analysis showed that there was a linear increase of SBP z score with increasing BMI z score, but not for DBP z score. However, there are data that BP has decreased over time despite the increasing obesity trends [20]. Moreover, in the current study, 66.7% of the participants presenting ISH were overweight or obese. ISH has been recognized as the most common type of HTN in childhood [6], the most prevalent phenotype in overweight/obese children [16, 21] and is associated with elevated left ventricular mass, a significant risk factor for cardiovascular morbidity and mortality [22].

In the current study, the rates of high BP levels did not differ by sex, but SBP and DBP z scores were higher in males compared with females. In some previous studies, the prevalence of high BP levels differs by sex [12], while in others there is no such difference [23]. Although sex has been associated with different HTN rates in adults, this has not consistently been the case in pediatric populations [24].

Several studies have also shown that low BW is associated with elevated BP later in adulthood [25]. Studies evaluating the association between BW and BP in children and adolescents have controversial results. Some of them have shown an inverse association between BW and BP [26], while others have reported positive association [27] or no association between BW and BP [28]. Lule et al., in a recent systematic review [29], concluded that the relationship between BW and later BP among African children and adolescents varied according to the participants’ age. In the current study, no association was found between BW or GA and the rates of high BP. Given these findings, the causality of this association has to be examined by longitudinal studies.

The present study found no differences between urban and rural areas regarding the prevalence of overweight and obesity and the prevalence of high BP levels. However, living in an urban area was found to have a significant positive effect on SBP z score, but not on DBP z score. That effect remained after adjustment for grade and BMI z score. Previous studies have assessed the urban–rural discrepancy in BP in children and their results are varying [30]. In the county of Kastoria, there is not a great difference between rural and urban areas regarding lifestyle, educational and socio-economical status, and other factors affecting the prevalence of high BP levels.

Environmental factors may affect BP level [31]. The influence of seasonal variation on BP has been documented in adults [31], but scarcely studied in children [32]. Specifically, BP levels seem to be higher during winter compared with summer. This phenomenon is partially attributed to outside temperature and other climate factors [32]. Furthermore, milder sleep problems when the weather is very hot [33] and less physical activity during winter [34] can influence the BP values. The May month measurement cross-sectional multinational survey [35] demonstrated a variation in SBP by day, with the highest SBP recorded on Saturday and lowest BP on Tuesday. This finding may be attributed to several environmental factors, including a major role of alcohol consumption, influencing BP values. We observed a higher prevalence of high–normal or hypertensive BP levels during spring and winter compared with autumn and summer, which is in line with the literature. Although we did not measure and record the ambient temperature, in Kastoria–North of Greece the climate is cold with spring temperatures being lower than autumn ones [36], possibly explaining the higher BP levels in spring. Moreover, the higher prevalence of high BP values during winter and spring can be attributed to the increasing workload during the academic year and the increasing stress for the forthcoming exams at the end of spring and early summer. The effect of stressors on BP levels in children and young adults has been investigated in previous studies showing associations with cardiovascular reactivity, but still more research is needed to elucidate this association [37,38,39].

The results of the present study should be interpreted considering its strengths and limitations. The main limitation of the current study is that BP measurements were taken in a single visit, while the diagnosis of HTN requires elevated BP values on at least three separate occasions [14]. BP measurement in one visit overestimates the BP level and therefore, the prevalence of HTN [14]. Nevertheless, the prevalence of high–normal and hypertensive BP levels was rather low in our study. We assumed that the estimated prevalence of high BP was partly affected by the use of the mercury sphygmomanometer, on one hand, and the aforementioned design of the study, which may have limited the white-coat effect, on the other hand. Another limitation of the study is its epidemiological design that does not permit a causal relationship between the studied parameters to be found. Finally, participation rate in the study was moderate and could be considered as limitation of the study introducing bias for the high BP levels prevalence in the study population. On the other hand, this is the first study in Greece conducted in a county of Greek province and included representative samples from all schools in the municipality. Moreover, the use of a mercury sphygmomanometer for the BP measurements could be considered as strength of the study, as the normative data and the cutoff points for the diagnosis of HTN emanated from the auscultatory method.

In conclusion, in this Greek population, a low rate of high–normal and hypertensive BP levels was found in a single visit following the ESH 2016 guidelines protocol for BP measurement, despite the high prevalence of overweight/obesity. Overweight and obesity were associated with higher BP levels, but there was also a seasonal difference in the prevalence of high BP levels. When assessing the prevalence of high BP in children and adolescents and the factors affecting BP levels, researchers should take into account not only the different guidelines used for BP measurement and diagnosis of high BP and the different characteristics of the studied population, but also the geographic area and the season of screening. Future collaborative multinational studies using unified methodology are needed for the estimation of the prevalence of hypertension in the general pediatric population.

Summary

What is known about topic

  • Excess body weight is associated with high BP levels.

  • BP levels in childhood have decreased over time in European and American studies, despite the increasing obesity trends, suggesting that other BP determinants need to be investigated.

What this study adds

  • There is a discordance between obesity prevalence and hypertension rate in children and adolescents.

  • In addition to excess body weight, which could only in part explain the high BP levels, geographical and seasonal factors may affect BP levels and the estimated prevalence of hypertension in epidemiological studies.

Data availability

The datasets generated and analyzed during the current study are available from the corresponding author on reasonable request.

Additional information

Publisher’s note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

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Authors’ contributions

TN: performed data collection, drafted the initial paper, revised and approved the final version; SS: analyzed the data, edited, revised, and approved the final version; KP and NP: edited, revised, and approved the final version; CA: analyzed the data; KK and FP: supervised the study, revised, and approved the final draft; VK: designed the study, edited, revised, and approved the final version.

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Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All procedures in the study werein accordance with the ethical standards of the Greek Ministry of National Education, the National Educational Institute and the Ethics Committee of Aristotle University of Thessaloniki, which approved the study protocol (65104/Γ7/15–05–2013).

Informed consent

Informed consent was obtained from all individual participants included in the study and their parents or legal guardians.

Correspondence to Thomaitsa Nika.

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