Correlation between fat mass and blood pressure in healthy children

Transcription

1 Pediatr Nephrol (29) 24: DOI.7/s ORIGINAL ARTICLE Correlation between fat mass and blood pressure in healthy children Dorota Drozdz & Przemko Kwinta & Przemysław Korohoda & Jacek A. Pietrzyk & Maciej Drozdz & Krystyna Sancewicz-Pach Received: 9 December 28 /Revised: 2 April 29 /Accepted: 3 April 29 /Published online: 28 May 29 # IPNA 29 Abstract Obesity is a well-known risk factor for arterial hypertension. The aim of this study was to analyze which surrogate marker of adiposity, i.e., body mass index (BMI) or fat mass (FM), as measured by bioimpedance analysis (BIA), best correlated with blood pressure in healthy children. Body weight, height, and casual blood pressure (BP) were measured in 193 healthy children (3 boys), aged 8 16 years. Body composition was determined by BIA. The correlation between BMI and age was linear, whereas the correlation between percentage of FM and age was nonlinear and it was different in boys and girls. Blood D. Drozdz (*) : J. A. Pietrzyk Dialysis Unit, Polish-American Children s Hospital, Collegium Medicum of Jagiellonian University, 26 Wielicka Str, dadrozdz@cm-uj.krakow.pl P. Kwinta Department of Pediatrics, Polish-American Children s Hospital, Collegium Medicum of Jagiellonian University, P. Korohoda University of Science and Technology (AGH), M. Drozdz Department of Nephrology, Collegium Medicum of Jagiellonian University, K. Sancewicz-Pach Department of Pediatric Nephrology, Polish-American Children s Hospital, Collegium Medicum of Jagiellonian University, pressure standard deviation scores (SDS) correlated with FM SDS (BIA) over the entire normal range (systolic: r=.26, p=.2; diastolic: r=.33, p<.1). An evaluation of the children based on BP (three groups: BP < th, th < BP > 9th ; BP > 9th ) revealed that hypertensive children had a higher BMI (17.6 vs vs kg/m 2, respectively) and a greater FM (14. vs vs. 3.2%, respectively). In conclusion, the divergence in FM in healthy boys and girls can be determined by BIA but not by BMI. In healthy children, BP within the entire normal range correlated with FM, children with established hypertension presented with a significantly higher FM. The study points to FM as an important determinant of BP pressure in obese and nonobese children. Keywords Bioimpedance. BMI. Children. Fat mass. Hypertension Introduction A significant increase in obesity has been observed in children and adolescents in many parts of the world, as demonstrated by various comparisons of normative data published within the last 1 years [1 3]. Obesity may predispose to diabetes type II either in adulthood or as early as adolescence [4 6]. In addition, a positive association between body fat and hypertension has been reported in several studies [7 9]. Body mass index (BMI) has been used in many of such studies as the preferred index to assess body fat [ 13], but bioimpedance analysis (BIA) provides a good alternative method and is a simple and non-invasive approach to measure the fat mass more

2 1736 Pediatr Nephrol (29) 24: accurately [14]. Within the last few decades several investigations have preferred the application of BIA for estimating human body composition in healthy people and in patients suffering from different diseases [1 19]. However, there have been only a few studies in which the association between fat mass (FM), as assessed by BIA, and blood pressure (BP) has been investigated in children [2]. The aim of the study reported here was to compare the association between FM and BP measured either by BMI or BIA in obese and non-obese healthy children. Materials and methods Bioimpedance measurements were taken in a group of 193 children (9 girls and 3 boys), all of whom were pupils of two primary schools in Cracow. The study was approved by the Jagiellonian University Ethics Committee (ref. no. KE/98/6/B/176 of the 3rd July, 1998). All children, parents, and teachers were thoroughly informed about the purposes and contents of the study. Written informed consent was obtained from all parents. The mean age (± standard deviation, SD) of the study cohort was 11.8± 2.2 years, the mean body mass was 42.6±12.8 kg, and the mean height was 11.1±13. cm. Body mass and height measurements were obtained using medical scales between 8 hours and 12 hours (noon), and arterial BP and bioimpedance were measured immediately thereafter. The limb bioimpedance was measured by a multifrequency BIA 2 M analyzer (at frequencies of 1,,, and khz) using Bianostic electrodes (Data Input, Darmstadt, Germany). During the BIA examination the children were in the supine position, with their limbs apart at an angle of approximately 4 C. The electrodes were placed on the left side of the body. The proximal electrodes were fastened to the back surface of the upper limb, directly above the wrist joint gap, and on the lower limb, just above the tarsal joint; the distal ones were attached 3 cm below. Nutri 4 software was used to analyze fat tissue content (FM), and the data obtained were used to prepare charts of fat mass content and BMI for the 193 children in the study according to gender and age in healthy children. Weight and height were expressed as standard deviation scores (SDS) based on Polish national data [21]. Blood pressure was measured in the sitting position using a mercury sphygmomanometer, and fifth phase diastolic BP was used to characterize diastolic pressure. Due to differences in BP due to height and gender, the results were coded. The children were placed into three groups according to the BP measurements: group 1, BP < th ; group 2, th < BP < 9th ; group 3, BP > 9th. Qualitative values were compared by the direct Fisher test, and the distribution of quantitative values was checked for normality. The groups were compared by variance analysis. Statistica for Windows ver. 6.PL (StatSoft, Tulsa, OK, 21) software was employed for the analysis, and p<. was considered to be statistically significant. The least mean squares (LMS) values were calculated, and charts were drawn using the LMS system (Institute of Child Health [22]). Results In our study cohort of healthy children, we observed a gradual increase of BMI between ages 8 and 16 years: in girls and in boys (Fig. 1b, d). In the girls of our study cohort, the gradual increase in FM correlated with age ( % of body mass), whereas in boys, the changes in FM followed a different pattern: there was an increase in FM until with maximal values were reached at 11 years of age and then a progressive decrease in FM thereafter, i.e. during puberty (9.7 vs. 13 vs. 9.9) (Fig. 1a, c). The increase in BMI in boys was linear and did not correlate with changes in FM content. The age and height of children within the different BP groups [BP < th (group 1); th < BP < 9th (group 2); BP > 9th (arterial hypertension; group 3)] did not differ; however, statistically significant differences were found between the BP groups for systolic BP and weight (4.6 vs vs kg, respectively; p<.1), the percentage of FM (14. vs vs. 3.2%, respectively; p<.1), and BMI (17.6 vs vs kg/m 2, respectively; p<.1). Significant differences between group 1 or 2 and group 3 were also observed for data expressed as SDS: for systolic BP and weight (.12 vs..43 vs. 2.12, respectively; p<.1), the percentage of FM (.11 vs..23 vs. 1.9, respectively; p<.1), and BMI (.17 vs..31 vs. 1.89, respectively; p<.1) (Fig. 2). The children with diastolic BP > 9th (group 3) were significantly heavier (body mass in group 1 vs. group 2 vs. group 3: 41.2 vs vs. 2.8 kg, respectively; p=.6, respectively), had a greater amount of fat mass (.8 vs. 6.9 vs kg, respectively), and had a greater percentage of FM (13. vs. 1.3 vs. 23.2%, respectively; p<.1) as well greater BMI (17.6 vs vs. 22., respectively; p<.1). A significant difference between all study groups was observed for diastolic BP and FM expressed as SDS (.3 vs..1 vs.97, respectively; p<.1) (Fig. 3). Significant differences between group 1 or 2 and group 3 were noted for the SDS data for diastolic BP and weight (. vs..24 vs. 1.27, respectively; p<.1), and BMI (.18 vs..1 vs. 1.3, respectively; p<.1).

3 Pediatr Nephrol (29) 24: Fig. 1 a Fat mass (FM) (%) in healthy girls according to age. b Body mass index (BMI) in healthy girls according to age. c FM (%) in healthy boys according to age. d BMI in healthy boys according to age FM (%) FM (%) a c BMI BMI b d Fat tissue content (as body mass percentage) was significantly correlated with systolic (r=.26, p=.2) and diastolic (r=.33, p<.1) BP (Fig. 4a, b). (SDS) Group 1 Group 2 Group 3 weight height FM BMI Data are presented as mean + SD Fig. 2 Comparison of weight, height {standard deviation score (SDS) based on Polish national data [21]}, FM, and BMI (SDS based on collected data) between the three groups of children classified according to systolic blood pressure (BP). Green circle BP < th, yellow square th < BP < 9th, red diamond BP > 9th Discussion This is the first published study to demonstrate that BP is correlated with FM not only in obese children but within the entire normal range for FM (Fig. 4). Our results lead to the conclusion that FM is an important determinant of BP in obese and non-obese healthy children. In adults, BMI is used as a surrogate marker for overweight and obesity. Adults with moderate obesity (BMI 32. kg/m 2 ) have been proven to run a double risk of developing arterial hypertension compared to individuals with normal body mass [6]. Among middle-aged women, BMI is the dominant predictor of risk for diabetes mellitus [4]. In children, due to the changes in BM composition related to growing and puberty, BMI should be assessed on the basis of diagrams or BMI SDS. Kelishadi et al. reported a significant correlation between mean parental BMI and hypertension in children []. The application of an electrical BIA analysis enables body content assessment together with the evaluation of the amount of FM [14]. Exact measurements of FM can be obtained using this simple

4 1738 Pediatr Nephrol (29) 24: (SDS) weight height FM BMI Data are presented as mean +/- SD Group 1 Group 2 Group 3 Fig. 3 Comparison of weight, height (SDS based on Polish national data [21]), FM, and BMI (SDS based on collected data) between the groups selected according to diastolic BP. Green circle BP < th, yellow square th < BP < 9th, red diamond BP > 9th method if the analysis is performed under uniform conditions and in healthy children with a uniform hydration state. In the study reported here, we compared the increase in BMI to the increase in body FM with increasing age. Whereas there is a linear relationship between BMI and age, this is not true for the correlation between FM and age. First, the increase of FM in terms of percentage is steeper up to the age of 11 years than thereafter and, secondly, there is a distinct gender dimorphism. We found that the percentage FM in the boys of our study cohort decreased in late puberty whereas this was not the case in the girls (Fig. 1a, c). Similar results were observed in a German study using anthropometric measurements (fat fold thickness) for estimating FM. In the study published by Schaefer et al., BMI predicted FM (estimated by anthropometric measurements) in girls (r=.84) and in obese boys (r=.8) but not in the non-obese two thirds of the male population [23]. Obviously, this difference between boys and girls can only be identified when the fat percentage is measured directly by BIA or estimated from fat fold thickness. In contrast, the BMI is calculated using the equation of body mass expressed in kilograms of body weight divided by height expressed in square meters. As such, a change in body composition, such as a decrease of FM and increase of muscle mass, is missed. Consequently, there is a linear increase in the BMI with increasing age in both females and males. Therefore, the BMI should be considered to be of limited usefulness for predicting FM mass in individual children, especially in boys during puberty. A meta-analysis of eight large epidemiological studies conducted in the USA showed that the odds ratio of elevated BP was significantly higher in patients that fall within the range of the upper normal of the BMI than in those that are found in the range of the lower s; this was true for both genders and in all ethnic and age groups [12]. Systolic BP was significantly more influenced by BMI for Caucasians than for Afro-American adolescent males. These phenomena can be explained by race differences in terms of body composition, so that the fat and muscle contents cannot be described using BMI. Data collected in the NHANES III study revealed significant race differences for mean percentage of FM in boys aged years: from 18.4% for non-hispanic Whites to 22.% for Mexican-Americans. Similar results were observed in the group of girls in the same age ranges (24.8 vs. 28.6%, respectively) [1]. In this large study of 1,912 children, BIA was used to evaluate body composition. In Systolic BP (SDS) Diastolic BP (SDS) a r=.2622; p< Fat mass (SDS) b r=.33; p< Fat mass (SDS) Fig. 4 a Correlation between fat mass determined by bioimpedance (BIA; presented as SDS) and systolic BP. b. Correlation between FM determined by BIA (presented as SDS) and diastolic BP

5 Pediatr Nephrol (29) 24: native American children aged 8 11 years, the mean fat content reached 38.4% of the body mass [16]. Due to a physiological increase of arterial BP during childhood, it is impossible to directly compare absolute values of arterial BP between the groups. Therefore, we assessed each reading against diagrams for age and height [24]. In healthy children, the increase in systolic and diastolic BP correlated with the amount of FM. Interestingly, a statistically significant difference existed in the amount of FM within the normal values of diastolic BP between the group of children with diastolic BP < th and the group of children with a BP between the th and 9th. No statistically significant difference was observed between the groups 1 and 2 for the systolic BP, but the children with systolic hypertension had a significantly greater amount of FM. The results from our study seem to prove an association between obesity and the development of arterial hypertension in children. Siervogel et al. observed a similar correlation between systolic arterial BP and the amount of FM in healthy male adults []. Because of a rapid increase in the number of children suffering from obesity, a growing number of pediatric patients may require complex diagnosis of arterial hypertension and its proper management. Such an evaluation should include BIA measurements as a rule. To answer the question whether a weight gain or fat gain is the stronger predictor of an increase in BP at any given age or with increasing age, the use of BIA seems to be preferable to the BMI index for fat measurements. Indeed, testing for correlations between BP and body weight SDS or BMI SDS or FM SDS showed the strongest correlation for FM SDS versus diastolic BP SDS. On the other hand, none of the correlations differed greatly (Figs. 2, 3). The reduction of body mass results in reduced hypertension, and this approach is one of the basic nonpharmacological management methods of arterial hypertension [26]. The data from two prospective population-based cohort studies (the Tecumseh Community Health Study and the Framingham Heart Study) showed an association between fat loss and decreased mortality rate. In contrast, weight loss was associated with increased mortality rate [27]. These results confirm the importance of using methods (such as BIA) that enable FM gain and muscle mass gain to be distinguished. One limitation of our study was the use of casual BP measurements. Ambulatory 24-h BP measurements would probably have given more reliable BP values that would have enabled the exclusion of white coat and masked hypertension cases. However, casual BP measurements were performed by the same observer at the schools of the probands, i.e. in an environment well-known to the children. In such a setting, similarly to home BP measurements [28], white coat hypertension is not as frequently expected as during office measurements. Furthermore, even if white coat hypertension cannot be completely ruled out, this is equally true for both obese and non-obese children. Consequently, the main finding of our investigation, i.e. BP and hypertension correlates with FM, seems to be valid. Another limitation of our investigation is the missing gold standard method, such as dual energy X-ray absorptiometry [29] for FM evaluation when comparing BIA values versus BMI values. However, we have shown that BIA is able to demonstrate the acknowledged divergence of FM during puberty in healthy boys and girls, whereas this was not possible with BMI. This is a strong argument to support the claim that the BIA method for FM evaluation is superior to the use of BMI. In conclusion, the divergence in FM in healthy boys and girls can be determined by BIA but not by BMI. In healthy children, BP within the normal range correlates with FM, while children with hypertension were found to have a significantly higher FM. These results demonstrate that FM may be one regulator of BP even in non-obese children. Acknowledgements The study was supported by unrestricted grant of Polish Ministry of Science (no 4 PE 13 14) and 3T11E1326. References 1. Angelopoulos PD, Milionis HJ, Moschonis G, Manios Y (26) Relations between obesity and hypertension: preliminary data from a cross-sectional study in primary schoolchildren: The children study. Eur J Clin Nutr 6: Ogden CL, Flegal KM, Carroll MD, Johnson CL (22) Prevalence and trends in overweight among US children and adolescents, JAMA 288: Troiano RP, Flegal KM, Kuczmarski RJ, Campbell SM, Johnson CL (199) Overweight prevalence and trends for children and adolescents. 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