Associations Between Adiposity Indicators and Elevated Blood Pressure Among Chinese Children and Adolescents

ORIGINAL ARTICLE Associations between adiposity indicators and elevated blood pressure among Chinese children and adolescents

B Dong1,2, Z Wang1,2, H-J Wang1 and J Ma1

Adiposity is closely related to elevated blood pressure (BP); however, which adiposity indicator is the best predictor of elevated BP among children and adolescents is unclear. To clarify this, 99 366 participants aged 7–17 years from the Chinese National Survey on Students’ Constitution and Health in 2010 were included in this study. The adiposity indicators, including weight, body mass index (BMI), waist circumference, waist-to-height ratio (WHtR), hip circumference, body adiposity index (BAI), waist-to-hip ratio (WHR) and skinfold thickness, were converted into z-scores before use. The associations between elevated BP and adiposity indicators z-scores were assessed by using logistic regression model and area under the receiver operating characteristic curve (AUC). In general, BAI, BMI and WHtR z-scores were superior for predicting elevated BP compared with weight, waist circumference, hip circumference, WHR and skinfold thickness z-scores. In both sexes, BMI z-score revealed slightly higher AUCs than other indicators. Our ﬁndings suggest that general adiposity indicators were equivalent, if not superior, to abdominal adiposity indicators to predict elevated BP. BMI could be a better predictor of elevated BP than other studied adiposity indicators in children.

Journal of Human Hypertension (2015) 29, 236–240; doi:10.1038/jhh.2014.95; published online 23 October 2014

INTRODUCTION the performance of this index for predicting elevated BP in Hypertension is the leading risk factor for cardiovascular disease children has not been assessed. mortality in populations and is responsible for 13% of deaths Using the data of Chinese National Survey on Students’ globally.1 Several studies supported the theory that the root cause Constitution and Health in 2010, one of the largest national of elevated blood pressure (BP) at adulthood may extend back to cross-sectional population-based studies among Chinese children childhood.2,3 Children and adolescents with elevated BP tend to and adolescents, we assessed and compared different adiposity fi have end-organ damage, including impaired vascular reactivity indicators and their associations with elevated BP, to nd the best and left ventricular hypertrophy.3 Therefore, elevated BP in predictor of elevated BP in children. children is an important public health issue. As bioactive mediators released by adiposity tissue can increase MATERIALS AND METHODS BP, obesity is one of the strongest predictors of childhood elevated BP.4,5 Body mass index (BMI) is the most frequently used Participants 6,7 The sampling procedures of 2010 Chinese National Survey on Students’ indicator for identifying obesity. Although some studies 21 8,9 Constitution and Health have been published previously in detail. In brief, suggested BMI as the strongest predictor of elevated BP, the fi fi this survey used a strati ed multistage sampling method to select Han ndings are still inconsistent about the best measurement for nationality students from primary and secondary schools. In the present predicting elevated BP in children. As studies in adults revealed study, 99 583 Han nationality children and adolescents aged 7–17 years that central obesity is more closely related to cardiovascular with the complete records were included. The participation rate of this disease risk,10,11 some researchers proposed that the indicators study was 99.72%. Two hundred and seventeen participants with extreme related to abdominal fat, such as waist circumference and waist- height, weight, BP, BMI, waist circumference, hip circumference or skinfold to-height ratio (WHtR), should be used for identifying elevated BP thickness (46 s.d.’s on either side of the mean) were excluded. As a result, a fi and other cardiovascular risk in children.12,13 Although some have total of 99 366 participants were included in the nal analysis of this study. This survey was conducted according to the guidelines laid down in the reported that WHtR and waist circumference are more strongly 14,15 Declaration of Helsinki and approved by the Ministry of Education, General associated with elevated BP than BMI, others have found Administration of Sport, Ministry of Health, State Ethnic Affairs Commission, 16 these measurements to have either a weaker or a similar Ministry of Science and Technology and the Ministry of Finance. Informed association.17,18 Therefore, it is unclear which adiposity indicators, consents were obtained verbally from both parents and students. The the general or the abdominal ones, would be the better indicator project of analysing the survey data was approved by the Medical Research for identifying children at risk of elevated BP. In addition, Bergman Ethics Committee of the University of Queensland (no. 2011001199). et al.19 recently developed an alternative parameter, body adiposity index (BAI), by using hip circumference and height to Measures reflect the percentage of body fat and found that it was a useful Anthropometric measurements were performed according to the same and easy measure for body fat percentage in adults.20 However, protocol at all survey sites.21 Students were asked to wear light clothes

1Institute of Child and Adolescent Health, School of Public Health, Peking University Health Science Center, Beijing, People’s Republic of China and 2Centre for Chronic Disease, School of Medicine, University of Queensland, Herston, Queensland, Australia. Correspondence: Dr Z Wang, School of Medicine, University of Queensland, 817 Health Sciences Building, Royal Brisbane and Women's Hospital, Herston, QLD 4029, Australia or Professor J Ma, Institute of Child and Adolescent Health, School of Public Health, Peking University Health Science Center, 38 Xueyuan Road, Haidian District, Beijing 100191, People’s Republic of China. E-mail: [email protected] or [email protected] Received 14 March 2014; revised 18 June 2014; accepted 18 July 2014; published online 23 October 2014 Adiposity indicators and childhood blood pressure B Dong et al 237 only and to stand straight without shoes. Height was measured using a RESULTS wall-mounted stadiometer to the nearest 0.1 cm, and weight was There were 49 514 boys and 49 852 girls included in this study. measured with a scale to the nearest 0.1 kg. Waist circumference was Their descriptive characteristics are showed in Table 1. For boys measured horizontally 1 cm above the navel at the end of normal expiration and hip circumference was measured at maximal protrusion of and girls, 7.4% and 6.4%, respectively, demonstrated an elevated the buttocks, by a nonelastic flexible tape to the nearest 0.1 cm. Height, BP. As shown in Table 2, most indicators were highly or weight, waist and hip circumference were measured twice, and the mean moderately correlated with each other, with the Pearson value was recorded. Skinfold thickness was measured using skinfold correlation coefficients ranging from 0.13 to 0.92. calipers to the nearest 0.5 mm at three sites on the right side of the body: Figure 1 displays the ORs and 95% CI of elevated BP for 1 unit (1) triceps, between the tip of the olecranon process of the ulna and the (s.d.) increase in adiposity indicators. It is obvious that every acromion process of the scapula; (2) subscapular, 1.0 cm below the tip of the scapula; and (3) abdominal, intersection of umbilical horizontal line adiposity indicator positively associated with elevated BP, with the and right midclavicular line. In each participant, three measurements were ORs ranging from 1.36 (95% CI: 1.31, 1.40) to 1.77 (95% CI: 1.71, taken and the mean value was recorded for one skinfold site. 1.83; all P-values o0.001). Among all the adiposity indicators, BP was measured according to the recommendation of the National BAI z-scores revealed the highest risk of elevated BP in boys High Blood Pressure Education Program (NHBPEP) Working Group in Children and Adolescents,2 using an auscultation mercury sphygmomanometer with an appropriate cuff size for children. BP measurements were taken 5 min after resting. Systolic blood pressure was defined as the onset Table 1. Characteristics of children and adolescents aged 7–17 years of ‘tapping’ Korotkoff sounds, and diastolic blood pressure was defined as the fifth Korotkoff sounds. An average of three BP measurements at a Measurement Boys (n = 49 514) Girls (n = 49 852) single visit was calculated for each child. In addition, all measurement instruments, including stadiometer, scale, Age, year 12.0 (3.2) 12.0 (3.2) tape, skinfold calipers and sphygmomanometer, were calibrated before Height, cm 152.9 (17.4) 148.3 (13.6) Weight, kg 45.8 (16.2) 41.3 (12.5) use. All technicians were required to pass a standard training course for − 2 measurements, and all measurements were conducted by the same team BMI, kg m 18.9 (3.6) 18.3 (3.2) of field technicians in each administrative region. BMI group, % Overweight 13.8 8.5 Definitions of adiposity indicators and elevated BP Obesity 8.8 4.6 BMI was calculated as weight (kg)/height2 (m2) and categorized as normal SBP, mm Hg 106.6 (13.0) 102.8 (11.6) weight, overweight and obese according to the references for Chinese DBP, mm Hg 65.5 (10.1) 64.4 (9.4) children and adolescents.22 BAI was calculated according to the formula EBP, % 7.4 6.4 proposed by Bergman et al.19 BAI = hip circumference (cm)/height WC, cm 66.3 (10.6) 63.0 (8.8) (m)1.5 − 18. WHtR was computed as waist circumference (cm)/height WHtR 0.43 (0.05) 0.42 (0.04) (cm), and waist-to-hip ratio (WHR) as waist circumference (cm)/hip HC, cm 79.4 (11.5) 79.0 (11.0) circumference (cm). The sum of triceps, subscapular and abdominal BAI 24.1 (3.9) 25.7 (3.2) skinfolds was used as skinfold thickness. In addition, elevated BP was WHR 0.84 (0.06) 0.80 (0.06) defined as systolic blood pressure or diastolic blood pressure at least 95th SFT, mm 36.6 (22.4) 44.0 (20.8) age-, sex- and height-specific percentile according to the reference of 2 Abbreviations: BAI, body adiposity index; BMI, body mass index; DBP, NHBPEP working group. diastolic blood pressure; EBP, elevated blood pressure; HC, hip circumfer- As the units vary among different adiposity indicators, the indicators ence; SBP, systolic blood pressure; SFT, skinfold thickness; WC, waist including weight, BMI, waist circumference, WHtR, hip circumference, BAI, circumference; WHR, waist-to-hip ratio; WHtR, waist-to-height ratio. Note: fi WHR and skinfold thickness were converted into age- and sex-speci c s.d. Data were shown as the mean (s.d.) or percentage. scores (z-scores), to make the effect estimates for different adiposity indicators comparable.

Observed value À age- and sex- specific mean z À score ¼ Age- and sex- specific s:d: Table 2. Correlation coefﬁcients between the adiposity indicator z- scores in boys and girls aged 7–17 years

Indicator BMI-z Weight-z WHtR-z WC-z BAI-z HC-z SFT-z Statistical analysis The correlations between adiposity indicator z-scores were examined by Boys using Pearson correlation. The odds ratios (ORs) and 95% conﬁdence Weight-z 0.92 intervals (CIs) between elevated BP and adiposity indicator z-scores were WHtR-z 0.89 0.76 estimated using logistic regression models. To compare the coefﬁcients of WC-z 0.91 0.90 0.94 two adiposity indicators, seemingly unrelated estimation was used, as BAI-z 0.79 0.57 0.84 0.71 described by Weesie.23 The area under the receiver operating characteristic HC-z 0.87 0.93 0.78 0.89 0.72 curve (AUC) represents the probability of correctly classifying children with SFT-z 0.83 0.79 0.81 0.84 0.68 0.78 and without elevated BP, ranging from 0.5 (no discrimination) to 1 (perfect WHR-z 0.56 0.47 0.78 0.72 0.37 0.34 0.55 discrimination).24 We calculated the AUCs to evaluate the performances of different indicator z-scores and compared the AUCs of two adiposity Girls variables by using χ2 test. We also performed the above analyses Weight-z 0.90 separately for different age groups. As the results were similar for different WHtR-z 0.83 0.67 age groups, we presented the results from the most parsimonious models WC-z 0.85 0.85 0.93 based on the largest sample size. Physical activity was considered as a BAI-z 0.76 0.50 0.77 0.61 potential confounding factor; however, the results were markedly similar HC-z 0.82 0.90 0.67 0.82 0.67 SFT-z 0.76 0.73 0.67 0.72 0.55 0.68 with those before physical activity was adjusted for (data not shown). WHR-z 0.41 0.31 0.74 0.67 0.20 0.13 0.37 Analyses were also conducted in models with interaction terms for sex and each adiposity indicator, which showed that there were interaction effects Abbreviations: BAI, body adiposity index; BMI, body mass index; HC, hip between several adiposity indicators and elevated BP. Therefore, results circumference; SFT, skinfold thickness; WC, waist circumference; WHR, were displayed by sex. Analyses were performed with the Stata 13 waist-to-hip ratio; WHtR, waist-to-height ratio. software (College Station, TX, USA).

© 2015 Macmillan Publishers Limited Journal of Human Hypertension (2015) 236 – 240 Adiposity indicators and childhood blood pressure B Dong et al 238 (OR = 1.77, 95% CI: 1.71, 1.83), followed by BMI z-score (OR = 1.72, to identify children and adolescents with elevated BP, with the 95% CI: 1.67, 1.76) and WHtR z-score (OR = 1.70, 95% CI: 1.65, 1.75). AUCs ranging from 0.584 to 0.658 (all P-values o0.001). Among Meanwhile, BAI, BMI and WHtR z-score associated with the similar all adiposity indicators, BMI, BAI and WHtR z-score displayed a risk of elevated BP in girls, with the ORs ranging from 1.63 (95% CI: similar ability to identify elevated BP in boys, with the AUCs 1.57, 1.68) to 1.66 (95% CI: 1.61, 1.71). OR estimates were markedly ranging from 0.655 to 0.658. Meanwhile, BMI z-score revealed a similar after adjusting for physical activity. significantly better ability than all of the other indicators to Figure 2 shows the AUCs of different adiposity indicators for identify elevated BP in girls (AUC = 0.644). elevated BP by sex. All adiposity indicators have a modest ability DISCUSSION In the present study, all adiposity indicators revealed a similar association with the risk of elevated BP, as well as the ability to identify children and adolescents with elevated BP. However, we found that BMI, BAI and WHtR z-scores were superior for predicting elevated BP compared with weight, waist circumference, hip circumference, WHR and skinfold thickness z-scores. Meanwhile, BMI, in general, performed best as the predictor of elevated BP among the studied adiposity indicators, with AUCs ranging from 0.644 to 0.656. In adults, abdominal adiposity indicators (such as waist circumference and WHtR) are superior to other adiposity indicators in discriminating elevated BP and other cardiovascular risks.11 The plausible explanation for this relates to the higher metabolic and inflammatory activity of visceral fat deposits within the abdominal cavity.5 However, in a cohort study, the abdominal adiposity indicator was inferior to BMI for assessing the risk of elevated BP in childhood.25 In our previous study, we reported that waist circumference and skinfold thickness had similar associations with the BP level when weight and height were controlled for.26 Consistent with these findings, this study revealed that general adiposity indicators (such as BMI and BAI) highly Figure 1. The ORs and 95% CIs of elevated blood pressure for correlated with abdominal adiposity indicators (such as WHtR). In adiposity indicator z-scores among Chinese children and adoles- – addition, general (such as BMI and BAI) and abdominal (such as cents aged 7 17 years. (P-values for the difference of ORs between WHtR) adiposity indicators have a similar ability to assess the risk adiposity indicators and BMI. BAI, body adiposity index; BMI, body mass index; CI, confidence interval; HC, hip circumference; OR, odds of elevated BP. A cohort study in children revealed that almost ratio; SFT, skinfold thickness; WC, waist circumference; WHR, waist- 90% of abdominal adiposity was subcutaneous, which indicated to-hip ratio; WHtR, waist-to-height ratio). that the amount of visceral adiposity was relatively small in children.27 Thus, we suggest that fat distribution may have relatively less impact on elevated BP in childhood than a general adiposity indicator. Our findings revealed that BMI demonstrated the best performance of identifying children with elevated BP among all studied indicators. However, consistent with the Bogalusa Heart Study and other surveys,16,17,28 we observed that the differences of identifying elevated BP among various indicators were small, and all adiposity indicators had a moderate ability to discriminate children with or without elevated BP. Chiolero et al.29 compared the ability of BMI and WHtR alone and in combination to predict elevated BP and found that combining two measurements did not confer additional discrimination power to BMI or WHtR alone. Therefore, we think adiposity indicators alone cannot sufficiently predict elevated BP, and other factors of potential importance, such as insulin resistance and increased sympathetic nervous system activity, should be considered when investigating the mechanism of childhood elevated BP.3,30 Recent evidence suggested that the location of waist circumference measurement affected the association between waist circumference and cardiovascular risk.31 However, the location of waist circumference measurement is different between the recommendations of the Anthropometric Standardization Refer- Figure 2. The AUCs and s.e.’s of different adiposity indicators’ z- ence Manual, the World Health Organization and the National scores for elevated blood pressure among Chinese children and 32 fl – Institutes of Health. These differences might in uence the adolescents aged 7 17 years. (P-values for the difference of AUCs comparability of the results of different studies. According to our between adiposity indicators and BMI. AUC, area under receiver operating characteristic curve; BAI, body adiposity index; study, abdominal adiposity indicators were not better than BMI, body mass index; HC, hip circumference; SFT, skinfold general adiposity indicators, such as BMI, to assess the risk of thickness; WC, waist circumference; WHR, waist-to-hip ratio; WHtR, elevated BP or to discriminate children with elevated BP. waist-to-height ratio). Therefore, we suggested that a general adiposity indicator, such

Journal of Human Hypertension (2015) 236 – 240 © 2015 Macmillan Publishers Limited Adiposity indicators and childhood blood pressure B Dong et al 239 as BMI, could be a better variable to predict elevated BP in their cooperation. This work is supported by the grant from the National Health and childhood than other studied adiposity indicators. Medical Research Council of Australia (APP1045000) to ZW; Specialized Research Our findings implicated that the fat distribution may have less Fund for the Doctoral Program of Higher Education of China (20120001110016) and impact on elevated BP, and general indicators, such as BMI, could National Natural Science Foundation of China (81172683) and Research Special Fund be a good indicator for predicting elevated BP among children for Public Welfare Industry of Health of China (201202010) to JM. and adolescents. In further research, especially the large epidemiological surveys where the addition of more sophisticated AUTHOR CONTRIBUTIONS measurements might raise the cost markedly, abdominal adiposity indicators, such as WHtR, are unnecessarily employed. In addition, Study concept and design: BD, JM and ZW. Acquisition of data: JM. Analysis and BAI could be a useful variable to predict cardiovascular health interpretation of data: BD, ZW, JM and H-JW. Draft of the manuscript: BD. Critical outcome among children and adolescents, if it would reveal a revision of the manuscript for important intellectual content: ZW, JM and H-JW. close association with other risk factors of cardiovascular disease Administrative, technical and material support: ZW, JM and H-JW. in further studies. This study has several strengths. Data were derived from a REFERENCES national survey with a large sample size (n = 99 366) and various anthropometry measurements, which allowed us to quantify and 1 WHO. 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