Summary
Sagittal abdominal diameter (SAD) was obtained in 65 adolescents referred for assessment of cardiometabolic risk. We found that SAD was associated with cardiometabolic risk factors independent of BMI in males, but that SAD was not superior to BMI or other measures of abdominal adiposity for the detection of metabolic syndrome.
Introduction
BMI is widely used to identify individuals with excess adiposity who may be at risk for cardiometabolic disease [1]. However, the use of BMI to screen for excess adiposity in children is limited by changes in body composition with growth and development [2]. Moreover, BMI does not provide information about abdominal fat. Abdominal obesity reflects excess subcutaneous and visceral adipose tissue (VAT). VAT is thought to be more metabolically active and predictive of cardiometabolic risk [3]. Measures of abdominal obesity including waist circumference (WC), sagittal abdominal diameter (SAD) and waist/hip ratio (WHR) have been shown to be strongly correlated with VAT [4, 5] and cardiometabolic risk factors [6]. In adults, SAD may be a more accurate measure of VAT [5] and better predictor of cardiometabolic disease [7, 8] than other anthropometric measures. The relationship between SAD and cardiometabolic risk in children remains unclear. Our objective was to evaluate the ability of SAD compared to WC, WHR, and BMI to identify the presence of cardiometabolic risk factors in a high-risk population of youth.
Methods
This study was approved by the IRB of The Children's Hospital of Philadelphia. 65 participants (26 male) aged 11-17 years referred to endocrinology for evaluation of cardiometabolic risk were recruited. Weight, height, SAD, WC, and WHR were obtained as previously described [5, 9]. BMI Z-scores were calculated [10] and categorized according to current recommendations [11] . Blood samples for cardiometabolic risk factors were obtained in the fasting state (Supplemental Methods). HOMA-IR was calculated as HOMA-IR = [fasting plasma insulin (μIU/mL) x fasting plasma glucose (mmol/L)] /22.5. Metabolic syndrome (MetSyn) was defined using the International Diabetes Federation Criteria [12].
Means/medians were compared by two-sample t-tests or Wilcoxon signed-rank tests; proportions by χ2 analysis. Outcomes were normalized by log transformations where indicated. Pearson and partial correlation coefficients were determined associations between measures of abdominal adiposity and cardiometabolic outcomes; tests of Hotelling's T and Steiger's Z statistics were used to compare strength of correlations. Receiver operator characteristic (ROC) curves were used to calculate the area under the curve (AUC) for anthropometric measures to identify MetSyn; χ2 tests were used to compare AUC values. Analyses were performed using Stata 12 (StataCorp, LP, College Station, TX).
Results
Participant characteristics are shown in Supplemental Table 1. Blacks comprised 68% of the sample. Mean BMI-Z was 2.2 ±0.3; 63/65 participants were obese, 2/65 were overweight. 14% of participants had MetSyn [12].
Significant correlations (p<0.05) were seen between all measures of abdominal adiposity and HOMA-IR, insulin, CPEP, and triglycerides in males, and hemoglobin A1C (HbA1c) in females (Table 1). Additionally, in females significant correlations were seen between WHR and CPEP and triglycerides and WC and HDL. In males, after adjusting for BMI-Z, significant correlations remained between SAD, WC, WHR and HOMA-IR, insulin, and CPEP. In females, after adjustment for BMI-Z, only the correlation between triglyceride level and WHR remained significant. The correlation between SAD and CPEP (0.775) in males was stronger than the correlation between BMI or BMI-Z and CPEP (0.612, 0.521).
Table 1.
Correlations and partial correlations between anthropometric measures of adiposity and cardiometabolic outcomes
| Males | |||||||||||
|---|---|---|---|---|---|---|---|---|---|---|---|
| Pearson Correlation Coefficients | Partial Correlation Coefficients (adjusted for BMI) | Partial Correlation Coefficients (adjusted for BMI-Z) | |||||||||
| BMI | BMI-Z | SAD | WC | WHR | SAD | WC | WHR | SAD | WC | WHR | |
| Homa IR1 | 0.4522 | 0.356 | 0.5593 | 0.5304 | 0.5303 | 0.330 | 0.316 | 0.353 | 0.4832 | 0.4582 | 0.4252 |
| Insulin1 | 0.6694 | 0.6103 | 0.7624 | 0.7614 | 0.6303 | 0.4842 | 0.4912 | 0.360 | 0.5783 | 0.5763 | 0.3962 |
| Glucose | -0.308 | -0.373 | -0.294 | -0.207 | -0.081 | ||||||
| CPEP | 0.6122 | 0.5212 | 0.7753,5 | 0.7073 | 0.6983 | 0.6043 | 0.4532 | 0.5002 | 0.7103 | 0.5763 | 0.5513 |
| A1c | 0.141 | 0.193 | 0.053 | 0.065 | 0.207 | ||||||
| TRI1 | 0.6023 | 0.5323 | 0.6133 | 0.5943 | 0.5793 | 0.271 | 0.150 | 0.321 | 0.385 | 0.321 | 0.368 |
| LDL | -0.174 | -0.195 | -0.115 | -0.204 | -0.308 | ||||||
| HDL1 | -0.208 | -0.251 | -0.119 | -0.050 | -0.048 | ||||||
| Females | |||||||||||
|---|---|---|---|---|---|---|---|---|---|---|---|
| Pearson Correlation Coefficients | Partial Correlation Coefficients (adjusted for BMI) | Partial Correlation Coefficients (adjusted for BMI-Z) | |||||||||
| BMI | BMI-Z | SAD | WC | WHR | SAD | WC | WHR | SAD | WC | WHR | |
| Homa IR1 | 0.024 | 0.142 | 0.059 | 0.152 | 0.245 | ||||||
| Insulin1 | 0.102 | 0.216 | 0.101 | 0.205 | 0.250 | ||||||
| Glucose | -0.026 | 0.120 | 0.005 | 0.046 | 0.172 | ||||||
| CPEP | 0.203 | 0.281 | 0.270 | 0.280 | 0.3342 | 0.204 | 0.212 | 0.276 | 0.066 | 0.100 | 0.233 |
| A1c | 0.3272 | 0.3652 | 0.4133 | 0.3502 | 0.3342 | 0.297 | 0.141 | 0.221 | 0.213 | 0.110 | 0.190 |
| TRI1 | 0.095 | 0.208 | 0.177 | 0.307 | 0.4192 | 0.225 | 0.4483 | 0.4233 | 0.013 | 0.237 | 0.3732 |
| LDL | 0.150 | 0.191 | 0.130 | 0.191 | 0.171 | ||||||
| HDL1 | -0.3902 | -0.4082 | -0.238 | -0.4042 | -0.253 | 0.201 | -0.145 | -0.100 | 0.093 | -0.148 | -0.067 |
HOMA-IR, insulin, triglycerides, and HDL were normalized using logarithmictransformation. Spearman correlation coefficients were also performed on non-transformed variables and they did not differ substantially from values reported above.
Statistically significant correlation, p<0.05
Statistically significant correlation, p<0.01
Statistically significant correlation, p<0.0001
Statistically stronger correlation compared to BMI and BMI-Z, assessed by Hotelling's T and Steiger's Z, p<0.05
The ability of SAD to identify MetSyn using AUC values (Table 2) in males (0.605) and females (0.648) did not differ from other measures of abdominal adiposity or BMI. The addition of SAD to BMI or BMI-Z did not result in a greater AUC compared to BMI or BMI-Z alone. In females, the AUC for WC (0.778) and BMI-Z with WC (0.833) was greater than the AUC for BMI-Z alone (0.657).
Table 2.
AUC for measures of abdominal adiposity and BMI to identify metabolic syndrome in males and females
| AUC |
AUC |
||||
|---|---|---|---|---|---|
| Males | Females | Males | Females | ||
| BMI-Z | 0.456 | 0.657 | BMI | 0.590 | 0.593 |
| SAD | 0.605 | 0.648 | SAD | 0.605 | 0.648 |
| WC | 0.561 | 0.7781 | WC | 0.561 | 0.778 |
| WHR | 0.614 | 0.833 | WHR | 0.614 | 0.833 |
| BMI-Z+SAD | 0.728 | 0.639 | BMI+SAD | 0.772 | 0.639 |
| BMI-Z+WC | 0.623 | 0.8332 | BMI+WC | 0.614 | 0.889 |
| BMI-Z+WHR | 0.597 | 0.852 | BMI+WHR | 0.614 | 0.843 |
Statistically significant difference from BMI-Z, p=0.03
Stasticially significant difference from BMI-Z, p=0.02
Conclusions
SAD in males was significantly correlated with several cardiometabolic risk factors independent of BMI, but the strength of those correlations did not differ from other measures of abdominal adiposity. Notably, CPEP had a stronger correlation with SAD compared to BMI in males. CPEP may be an early marker of impaired glucose metabolism in obese adolescents [13] raising the possibility that SAD could improve upon BMI for the early detection of diabetes risk. After adjustment for BMI, SAD was not significantly correlated with any cardiometabolic risk factors in females.
ROC curve analysis revealed that SAD alone or in conjunction with BMI did not improve identification of MetSyn compared to BMI or other measures of abdominal adiposity. The use of WC (either alone or with BMI) was superior to BMI for the detection of MetSyn in females, suggesting a role for the assessment of abdominal adiposity in this population. Findings of previous studies comparing the ability of BMI and measures of abdominal adiposity to identify cardiometabolic risk factors are conflicting. WC has been found to be associated with cardiometabolic risk factors independent of BMI in some studies [14, 15] while others have found that measures of abdominal adiposity are not better than BMI for the identification of cardiometabolic risk [16, 17]. A recent study reported measures of abdominal adiposity were not better predictors of VAT than BMI in children [18], which may explain these negative findings.
The results of our study may be limited by the high prevalence of obesity in our population (mean BMI-Z of 2.2). It is possible that measures of abdominal adiposity may be more useful predictors of cardiometabolic risk in non-obese individuals where excess abdominal adiposity could be missed if using a whole body measure such as BMI [19]. Future studies of children with a range of BMI are needed to identify the populations in which measurements of abdominal adiposity including SAD will improve cardiometabolic risk assessment. SAD has been added to the National Health and Nutrition Examination Survey procedures [20] which will provide opportunities for such studies. In summary, our results suggest that in an obese pediatric population, SAD is correlated with a number of cardiometabolic risk factors, but it does not improve upon BMI, WC, or WHR for the identification of MetSyn.
Supplementary Material
Acknowledgments
Grants:
This research was funded as a pilot study of NIH-NINR P30-NR-005043 from the Center for Health Outcomes, University of Pennsylvania, School of Nursing. The Clinical and Translational Research Center is supported by UL1TR000003
Footnotes
Publisher's Disclaimer: This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final citable form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
Meetings: Preliminary data was presented at the 2011 American Diabetes Association National Meeting, San Diego, CA, USA
REFERENCES
- 1.Standards of medical care in diabetes--2013. Diabetes Care. 2013;36(Suppl 1):S11–66. doi: 10.2337/dc13-S011. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 2.Demerath EW, Schubert CM, Maynard LM, Sun SS, Chumlea WC, Pickoff A, Czerwinski SA, Towne B, Siervogel RM. Do changes in body mass index percentile reflect changes in body composition in children? Data from the Fels Longitudinal Study. Pediatrics. 2006;117:e487–495. doi: 10.1542/peds.2005-0572. [DOI] [PubMed] [Google Scholar]
- 3.Goran MI, Gower BA. Relation between visceral fat and disease risk in children and adolescents. Am J Clin Nutr. 1999;70:149S–156S. doi: 10.1093/ajcn/70.1.149s. [DOI] [PubMed] [Google Scholar]
- 4.Brambilla P, Bedogni G, Moreno LA, Goran MI, Gutin B, Fox KR, Peters DM, Barbeau P, De Simone M, Pietrobelli A. Crossvalidation of anthropometry against magnetic resonance imaging for the assessment of visceral and subcutaneous adipose tissue in children. Int J Obes (Lond) 2006;30:23–30. doi: 10.1038/sj.ijo.0803163. [DOI] [PubMed] [Google Scholar]
- 5.Zamboni M, Turcato E, Armellini F, Kahn HS, Zivelonghi A, Santana H, Bergamo-Andreis IA, Bosello O. Sagittal abdominal diameter as a practical predictor of visceral fat. Int J Obes Relat Metab Disord. 1998;22:655–660. doi: 10.1038/sj.ijo.0800643. [DOI] [PubMed] [Google Scholar]
- 6.Schwandt P, Bertsch T, Haas GM. Anthropometric screening for silent cardiovascular risk factors in adolescents: The PEP Family Heart Study. Atherosclerosis. 2010;211:667–671. doi: 10.1016/j.atherosclerosis.2010.03.032. [DOI] [PubMed] [Google Scholar]
- 7.de Souza NC, de Oliveira EP. Sagittal abdominal diameter shows better correlation with cardiovascular risk factors than waist circumference and BMI. Journal of diabetes and metabolic disorders. 2013;12:41. doi: 10.1186/2251-6581-12-41. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 8.Pajunen P, Rissanen H, Laaksonen MA, Heliovaara M, Reunanen A, Knekt P. Sagittal abdominal diameter as a new predictor for incident diabetes. Diabetes Care. 2013;36:283–288. doi: 10.2337/dc11-2451. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 9.Lipman TH, Hench KD, Benyi T, Delaune J, Gilluly KA, Johnson L, Johnson MG, McKnight-Menci H, Shorkey D, Shults J, Waite FL, Weber C. A multicentre randomised controlled trial of an intervention to improve the accuracy of linear growth measurement. Arch Dis Child. 2004;89:342–346. doi: 10.1136/adc.2003.030072. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 10.Kuczmarski RJ, Ogden CL, Grummer-Strawn LM, Flegal KM, Guo SS, Wei R, Mei Z, Curtin LR, Roche AF, Johnson CL. CDC growth charts: United States. Adv Data. 2000:1–27. [PubMed] [Google Scholar]
- 11.Krebs NF, Himes JH, Jacobson D, Nicklas TA, Guilday P, Styne D. Assessment of child and adolescent overweight and obesity. Pediatrics. 2007;120(Suppl 4):S193–228. doi: 10.1542/peds.2007-2329D. [DOI] [PubMed] [Google Scholar]
- 12.Zimmet P, Alberti G, Kaufman F, Tajima N, Silink M, Arslanian S, Wong G, Bennett P, Shaw J, Caprio S. The metabolic syndrome in children and adolescents. Lancet. 2007;369:2059–2061. doi: 10.1016/S0140-6736(07)60958-1. [DOI] [PubMed] [Google Scholar]
- 13.Weiss R, D'Adamo E, Santoro N, Hershkop K, Caprio S. Basal alpha-cell up-regulation in obese insulin-resistant adolescents. J Clin Endocrinol Metab. 2011;96:91–97. doi: 10.1210/jc.2010-1275. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 14.Freedman DS, Serdula MK, Srinivasan SR, Berenson GS. Relation of circumferences and skinfold thicknesses to lipid and insulin concentrations in children and adolescents: the Bogalusa Heart Study. Am J Clin Nutr. 1999;69:308–317. doi: 10.1093/ajcn/69.2.308. [DOI] [PubMed] [Google Scholar]
- 15.Lee S, Bacha F, Gungor N, Arslanian SA. Waist circumference is an independent predictor of insulin resistance in black and white youths. J Pediatr. 2006;148:188–194. doi: 10.1016/j.jpeds.2005.10.001. [DOI] [PubMed] [Google Scholar]
- 16.Lawlor DA, Benfield L, Logue J, Tilling K, Howe LD, Fraser A, Cherry L, Watt P, Ness AR, Davey Smith G, Sattar N. Association between general and central adiposity in childhood, and change in these, with cardiovascular risk factors in adolescence: prospective cohort study. BMJ. 2010;341:c6224. doi: 10.1136/bmj.c6224. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 17.Al-Attas OS, Al-Daghri NM, Alokail MS, Alkharfy KM, Draz H, Yakout S, Sabico S, Chrousos G. Association of body mass index, sagittal abdominal diameter and waist-hip ratio with cardiometabolic risk factors and adipocytokines in Arab children and adolescents. BMC Pediatr. 2012;12:119. doi: 10.1186/1471-2431-12-119. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 18.Koren D, Marcus CL, Kim C, Gallagher PR, Schwab R, Bradford RM, Zemel BS. Anthropometric predictors of visceral adiposity in normal-weight and obese adolescents. Pediatr Diabetes. 2013 doi: 10.1111/pedi.12042. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 19.Taylor SA, Hergenroeder AC. Waist circumference predicts increased cardiometabolic risk in normal weight adolescent males. Int J Pediatr Obes. 2011;6:e307–311. doi: 10.3109/17477166.2011.575149. [DOI] [PubMed] [Google Scholar]
- 20.National Center for Health Statistics [August 3 2013];National Health and Nutrition Examination Survey: Anthropometry Procedures Manual. 2011 Internet: http://www.cdc.gov/nchs/data/nhanes/nhanes_11_12/Anthropometry_Procedures_Man ual.pdf.
Associated Data
This section collects any data citations, data availability statements, or supplementary materials included in this article.
