Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Pediatric Highlight
  • Published:

Gender differences in the relationships among obesity, adiponectin and brachial artery distensibility in adolescents and young adults

International Journal of Obesity volume 33, pages 1118–1125 (2009)Cite this article

Abstract

Background:

Obesity-related cardiovascular diseases (CVDs) are a major cause of cardiovascular (CV) mortality. Obesity-related reduction in vascular protective adipose-derived proteins, such as adiponectin (APN), has an important role.

Methods:

We compared brachial artery distensibility (BrachD) with APN, the level of adiposity and other CV risk factors (CVRFs) in 431 post-pubertal subjects (mean 17.9 years). Gender differences in average values were examined by t-tests. Correlations among BrachD, obesity and other CVRFs were examined. Regression analysis was performed to determine whether APN provided an independent contribution to BrachD, while controlling for obesity and other CVRFs.

Results:

Male subjects had lower BrachD (5.72±1.37 vs 6.45±1.60% change per mm Hg, P<0.0001) and lower APN (10.50±4.65 vs 13.20±6.53; all P<0.04) than female subjects. BrachD correlated with APN (r=0.25, P< 0.0001). Both BrachD and APN correlated with measures of body size, including height, weight and body mass index (BMI). Both correlated with higher systolic blood pressure, glucose, insulin and lower high-density lipoprotein cholesterol (all P<0.01). In multivariate analysis, APN, gender, APN*gender and BMI z-score predicted BrachD (r2=0.305). On the basis of gender difference, only BMI z-score was significant for male subjects (r2=0.080), whereas APN and BMI z-score contributed for female subjects (r2=0.242, all P<0.0001).

Conclusions:

BrachD is independently influenced by obesity in both male and female subjects. In female subjects, APN exerts an additional independent effect even after adjusting for blood pressure (BP), lipid levels and insulin. Differences in the effect of the APN–adiposity relationship on obesity-related vascular disease may be one reason for gender differences in the development and progression of atherosclerosis.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Figure 1

References

  1. Centers for Disease Control and Prevention. The burden of chronic diseases and their risk factors: national and state perspectives 2004. http://www.cdcgov/nccdphp/burdenbook2004.

  2. Faxon DP, Creager MA, Smith SC, Jr., Pasternak RC, Olin JW, Bettmann MA et al. Atherosclerotic vascular disease conference: executive summary: atherosclerotic vascular disease conference proceeding for healthcare professionals from a special writing group of the American Heart Association. Circulation 2004; 109: 2595–2604.

    Article  PubMed  Google Scholar 

  3. Urbina EM, Brinton TJ, Elkasabany A, Berenson GS . Brachial artery distensibility and relation to cardiovascular risk factors in healthy young adults (The Bogalusa Heart Study). Am J Cardiol 2002; 89: 946–951.

    Article  PubMed  Google Scholar 

  4. Brinton TJ, Cotter B, Kailasam MT, Brown DL, Chio S-S, O'Conor DT, et al., Development and validation of a noninvasive method to determine arterial pressure and vascular compliance. Am J Cardiol 1997; 80: 323–330.

    Article  CAS  PubMed  Google Scholar 

  5. Brinton TJ, Walls ED, Chio SS . Validation of pulse dynamic blood pressure measurement by auscultation. Blood Press Monit 1998; 3: 121–124.

    CAS  PubMed  Google Scholar 

  6. Nakamura M, Sugawara S, Arakawa N, Nagano M, Shizuka T, Shimoda Y et al. Reduced vascular compliance is associated with impaired endothelium-dependent dilatation in the brachial artery of patients with congestive heart failure. J Card Fail 2004; 10: 36–42.

    Article  CAS  PubMed  Google Scholar 

  7. Budoff MJ, Flores F, Tsai J, Frandsen T, Yamamoto H, Takasu J . Measures of brachial artery distensibility in relation to coronary calcification. Am J Hypertens 2003; 16: 350–355.

    Article  PubMed  Google Scholar 

  8. Urbina EM, Bean JA, D'Alessio D, Daniels SR, Dolan LM . Overweight and hyperinsulinemia provide individual contributions to compromises in brachial artery distensibility in healthy adolescents and young adults. 2007; 1: 200–207.

    Google Scholar 

  9. Mahmud A, Feely J . Adiponectin and arterial stiffness. Am J Hypertens 2005; 18: 1543–1548.

    Article  CAS  PubMed  Google Scholar 

  10. Maahs DM, Ogden LG, Kinney GL, Wadwa P, Snell-Bergeon JK, Dabelea D et al. Low plasma adiponectin levels predict progression of coronary artery calcification. Circulation 2005; 111: 747–753.

    Article  CAS  PubMed  Google Scholar 

  11. Okamoto Y, Arita Y, Nishida M, Muraguchi M, Ouchi N, Takahashi M et al. An adipocyte-derived plasma protein, adiponectin, adheres to injured vascular walls. Horm Metab Res 2000; 32: 47–50.

    Article  CAS  PubMed  Google Scholar 

  12. Ouchi N, Kihara S, Arita Y, Maeda K, Kuriyama H, Okamoto Y et al. Novel modulator for endothelial adhesion molecules: adipocyte-derived plasma protein adiponectin. Circulation 1999; 100: 2473–2476.

    Article  CAS  PubMed  Google Scholar 

  13. Stefan N, Bunt JC, Salbe AD, Funahashi T, Matsuzawa Y, Tataranni PA . Plasma adiponectin concentrations in children: relationships with obesity and insulinemia. J Clin Endocrinol Metab 2002; 87: 4652–4656.

    Article  CAS  PubMed  Google Scholar 

  14. Shimabukuro M, Higa N, Asahi T, Oshiro Y, Takasu N, Tagawa T et al. Hypoadiponectinemia is closely linked to endothelial dysfunction in man. J Clin Endocrinol Metab 2003; 88: 3236–3240.

    Article  CAS  PubMed  Google Scholar 

  15. Matsuda M, Shimomura I, Sata M, Arita Y, Nishida M, Maeda N et al. Role of adiponectin in preventing vascular stenosis. The missing link of adipo-vascular axis. J Biol Chem 2002; 277: 37487–37491.

    Article  CAS  PubMed  Google Scholar 

  16. Goodman E, Adler NE, Daniels SR, Morrison JA, Slap GB, Dolan LM . Impact of objective and subjective social status on obesity in a biracial cohort of adolescents. Obes Res 2003; 11: 1018–1026.

    Article  PubMed  Google Scholar 

  17. Martin LJ, Woo JG, Daniels SR, Goodman E, Dolan LM . The relationships of adiponectin with insulin and lipids are strengthened with increasing adiposity. J Clin Endocrinol Metab 2005; 90: 4255–4259.

    Article  CAS  PubMed  Google Scholar 

  18. Andersen KK, Frystyk J, Wolthers OD, Heuck C, Flyvbjerg A . Gender differences of oligomers and total adiponectin during puberty: a cross-sectional study of 859 Danish school children. J Clin Endocrinol Metab 2007; 92: 1857–1862.

    Article  CAS  PubMed  Google Scholar 

  19. Dolan LM, Bean J, D'Alessio D, Cohen RM, Morrison JA, Goodman E et al. Frequency of abnormal carbohydrate metabolism and diabetes in a population-based screening of adolescents. J Pediatr 2005; 146: 751–758.

    Article  CAS  PubMed  Google Scholar 

  20. Centers for Disease Control and Prevention. http://www.cdc.gov/.

  21. Takahashi M, Arita Y, Yamagata K, Matsukawa Y, Okutomi K, Horie M et al. Genomic structure and mutations in adipose-specific gene, adiponectin. Int J Obes Relat Metab Disord 2000; 24: 861–868.

    Article  CAS  PubMed  Google Scholar 

  22. National High Blood Pressure Education Program Working Group on High Blood Pressure in Children and Adolescents. The fourth report on the diagnosis, evaluation, and treatment of high blood pressure in children and adolescents. Pediatrics 2004; 114: 555–576.

    Article  Google Scholar 

  23. SAS Institute. SAS OnlineDoc, Version 9.1. SAS Institute: Cary, NC, 2002.

  24. Tsou PL, Jiang YD, Chang CC, Wei JN, Sung FC, Lin CC et al. Sex-related differences between adiponectin and insulin resistance in schoolchildren. Diabetes Care 2004; 27: 308–313.

    Article  CAS  PubMed  Google Scholar 

  25. Sabin MA, Holly JMP, Shield JPH, Turner SJ, Grohmann MJ, Stewart CEH et al. Mature subcutaneous and visceral adipocyte concentrations of adiponectin are highly correlated in prepubertal children and inversely related to body mass index standard deviation score. J Clin Endocrinol Metab 2006; 91: 332–335.

    Article  CAS  PubMed  Google Scholar 

  26. Urbina EM, Kieltkya L, Tsai J, Srinivasan SR, Berenson GS . Impact of multiple cardiovascular risk factors on brachial artery distensibility in young adults: the Bogalusa Heart Study. Am J Hypertens 2005; 18: 767–771.

    Article  PubMed  Google Scholar 

  27. Sinha R, Fisch G, Teague B, Tamborlane WV, Banyas B, Allen K et al. Prevalence of impaired glucose tolerance among children and adolescents with marked obesity. N Engl J Med 2002; 346: 802–810.

    Article  CAS  PubMed  Google Scholar 

  28. Zebekakis PE, Nawrot T, Thijs L, Balkestein EJ, van der Heijden-Spek J, Van Bortel LM et al. Obesity is associated with increased arterial stiffness from adolescence until old age. J Hypertens 2005; 23: 1839–1846.

    Article  CAS  PubMed  Google Scholar 

  29. Whincup PH, Gilg JA, Donald AE, Katterhorn M, Oliver C, Cook DG et al. Arterial distensibility in adolescents: the influence of adiposity, the metabolic syndrome, and classic risk factors. Circulation 2005; 112: 1789–1797.

    Article  CAS  PubMed  Google Scholar 

  30. Tounian P, Aggoun Y, Dubern B, Varille V, Guy-Grand B, Sidi D et al. Presence of increased stiffness of the common carotid artery and endothelial dysfunction in severely obese children: a prospective study. Lancet 2001; 358: 1400–1404.

    Article  CAS  PubMed  Google Scholar 

  31. Oren A, Vos LE, Bos WJ, Safar ME, Uiterwaal CS, Gorissen WH et al. Gestational age and birth weight in relation to aortic stiffness in healthy young adults: two separate mechanisms? Am J Hypertens 2003; 16: 79.

    Article  PubMed  Google Scholar 

  32. Urbina EM, Srinivasan SR, Kieltyka RL, Tang R, Bond MG, Chen W et al. Correlates of carotid artery stiffness in young adults: The Bogalusa Heart Study. Atherosclerosis 2004; 176: 157–164.

    Article  CAS  PubMed  Google Scholar 

  33. van der Heijden-Spek JJ, Staessen JA, Fagard RH, Hoeks AP, Boudier HA, van Bortel LM . Effect of age on brachial artery wall properties differs from the aorta and is gender dependent: a population study. Hypertension 2000; 35: 637–642.

    Article  CAS  PubMed  Google Scholar 

  34. Kawecka-Jaszcz K, Czarnecka D, Olszanecka A, Rajzer M, Jankowski P . The effect of hormone replacement therapy on arterial blood pressure and vascular compliance in postmenopausal women with arterial hypertension. J Hum Hypertens 2002; 16: 509–516.

    Article  CAS  PubMed  Google Scholar 

  35. Karim R, Hodis HN, Stanczyk FZ, Lobo RA, Mack WJ . Relationship between serum levels of sex hormones and progression of subclinical atherosclerosis in postmenopausal women. J Clin Endocrinol Metab 2008; 93: 131–138.

    Article  CAS  PubMed  Google Scholar 

  36. Kallikazaros I, Tsioufis C, Zambaras P, Stefanadis C, Toutouzas P . Conjugated estrogen administration improves common carotid artery elastic properties in normotensive postmenopausal women. Clin Cardiol 2002; 25: 167–172.

    Article  PubMed  Google Scholar 

  37. Ahimastos AA, Formosa M, Dart AM, Kingwell BA . Gender differences in large artery stiffness pre- and post puberty. J Clin Endocrinol Metab 2003; 88: 5375–5380.

    Article  CAS  PubMed  Google Scholar 

  38. Ouchi N, Kihara S, Arita Y, Nishida M, Matsuyama A, Okamoto Y et al. Adipocyte-derived plasma protein, adiponectin, suppresses lipid accumulation and class A scavenger receptor expression in human monocyte-derived macrophages. Circulation 2001; 103: 1057–1063.

    Article  CAS  PubMed  Google Scholar 

  39. DzieliAska Z, Januszewicz A, Wiecek A, Demkow M, Makowiecka-CieAla M, Prejbisz A et al. Decreased plasma concentration of a novel anti-inflammatory protein--adiponectin--in hypertensive men with coronary artery disease. Thromb Res 2003; 110: 365–369.

    Article  Google Scholar 

  40. Otsuka F, Sugiyama S, Kojima S, Maruyoshi H, Funahashi T, Matsui K et al. Plasma adiponectin levels are associated with coronary lesion complexity in men with coronary artery disease. J Am Coll Cardiol 2006; 48: 1155–1162.

    Article  CAS  PubMed  Google Scholar 

  41. Civitarese AE, Jenkinson CP, Richardson D, Bajaj M, Cusi K, Kashyap S et al. Adiponectin receptors gene expression and insulin sensitivity in non-diabetic Mexican Americans with or without a family history of Type 2 diabetes. Diabetologia 2004; 47: 816–820.

    Article  CAS  PubMed  Google Scholar 

  42. Della Mea P, Lupia M, Bandolin V, Guzzon S, Sonino N, Vettor R et al. Adiponectin, insulin resistance, and left ventricular structure in dipper and nondipper essential hypertensive patients. Am J Hypertens 2005; 18: 30–35.

    Article  PubMed  Google Scholar 

  43. Wang ZV, Scherer PE . Adiponectin, cardiovascular function, and hypertension. Hypertension 2008; 51: 8–14.

    Article  CAS  PubMed  Google Scholar 

  44. Fernandez-Real JM, Castro A, Vazquez G, Casamitjana R, Lopez-Bermejo A, Penarroja G et al. Adiponectin is associated with vascular function independent of insulin sensitivity. Diabetes Care 2004; 27: 739–745.

    Article  CAS  PubMed  Google Scholar 

  45. Tan KC, Xu A, Chow WS, Lam MC, Ai VH, Tam SC et al. Hypoadiponectinemia is associated with impaired endothelium-dependent vasodilation. J Clin Endocrinol Metab 2004; 89: 765–769.

    Article  CAS  PubMed  Google Scholar 

  46. Bakkaloglu SA, Buyan N, Funahashi T, Pasaoglu H, Elhan AH, Hasanoglu E et al. Adiponectin levels and atherosclerotic risk factors in pediatric chronic peritoneal dialysis patients. Perit Dial Int 2005; 25: 357–361.

    CAS  PubMed  Google Scholar 

  47. Agewall S . Is impaired flow-mediated dilatation of the brachial artery a cardiovascular risk factor? Curr Vasc Pharmacol 2003; 1: 107–109.

    Article  CAS  PubMed  Google Scholar 

  48. Araki T, Emoto M, Yokoyama H, Maeno T, Hatsuda S, Mori K et al. The association of plasma adiponectin level with carotid arterial stiffness. Metabolism 2006; 55: 587–592.

    Article  CAS  PubMed  Google Scholar 

  49. Pilz S, Horejsi R, Moller R, Almer G, Scharnagl H, Stojakovic T et al. Early atherosclerosis in obese juveniles is associated with low serum levels of adiponectin. J Clin Endocrinol Metab 2005; 90: 4792–4796.

    Article  CAS  PubMed  Google Scholar 

  50. Gullu H, Erdogan D, Caliskan M, Tok D, Yildirim E, Ulus T et al. Interrelationship between noninvasive predictors of atherosclerosis: transthoracic coronary flow reserve, flow-mediated dilation, carotid intima-media thickness, aortic stiffness, aortic distensibility, elastic modulus, and brachial artery diameter. Echocardiography 2006; 23: 835–842.

    Article  PubMed  Google Scholar 

  51. Singhal A, Jamieson N, Fewtrell M, Deanfield J, Lucas A, Sattar N . Adiponectin predicts insulin resistance but not endothelial function in young healthy adolescents. J Clin Endocrinol Metab 2005; 90: 4615–4621.

    Article  CAS  PubMed  Google Scholar 

  52. Butte NF, Comuzzie AG, Cai G, Cole SA, Mehta NR, Bacino CA . Genetic and environmental factors influencing fasting serum adiponectin in Hispanic children. J Clin Endocrinol Metab 2005; 90: 4170–4176.

    Article  CAS  PubMed  Google Scholar 

  53. Mattern HM, Lloyd PG, Sturek M, Hardin CD, Mattern HM, Lloyd PG et al. Gender and genetic differences in bladder smooth muscle PPAR mRNA in a porcine model of the metabolic syndrome. Mol Cell Biochem 2007; 302: 43–49.

    Article  CAS  PubMed  Google Scholar 

  54. Ciana P, Biserni A, Tatangelo L, Tiveron C, Sciarroni AF, Ottobrini L et al. A novel peroxisome proliferator-activated receptor responsive element-luciferase reporter mouse reveals gender specificity of peroxisome proliferator-activated receptor activity in liver. Mol Endocrinol 2007; 21: 388–400.

    Article  CAS  PubMed  Google Scholar 

  55. Ibabe A, Bilbao E, Cajaraville MP, Ibabe A, Bilbao E, Cajaraville MP . Expression of peroxisome proliferator-activated receptors in zebrafish (Danio rerio) depending on gender and developmental stage. Histochem Cell Biol 2005; 123: 75–87.

    Article  CAS  PubMed  Google Scholar 

  56. Djouadi F, Weinheimer CJ, Saffitz JE, Pitchford C, Bastin J, Gonzalez FJ et al. A gender-related defect in lipid metabolism and glucose homeostasis in peroxisome proliferator- activated receptor alpha- deficient mice. J Clin Invest 1998; 102: 1083–1091.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Verma S, Szmitko PE, Verma S, Szmitko PE . The vascular biology of peroxisome proliferator-activated receptors: modulation of atherosclerosis. Can J Cardiol 2006; 22 (Suppl B): 12B–17B.

    Article  PubMed  PubMed Central  Google Scholar 

  58. Yu JG, Javorschi S, Hevener AL, Kruszynska YT, Norman RA, Sinha M et al. The effect of thiazolidinediones on plasma adiponectin levels in normal, obese, and type 2 diabetic subjects. Diabetes 2002; 51: 2968–2974.

    Article  CAS  PubMed  Google Scholar 

  59. Ryan AS, Berman DM, Nicklas BJ, Sinha M, Gingerich RL, Meneilly GS et al. Plasma adiponectin and leptin levels, body composition, and glucose utilization in adult women with wide ranges of age and obesity. Diabetes Care 2003; 26: 2383–2388.

    Article  CAS  PubMed  Google Scholar 

  60. Comuzzie AG, Funahashi T, Sonnenberg G, Martin LJ, Jacob HJ, Black AE et al. The genetic basis of plasma variation in adiponectin, a global endophenotype for obesity and the metabolic syndrome. J Clin Endocrinol Metab 2001; 86: 4321–4325.

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We gratefully acknowledge the work of the PSD research team and the administration, staff, teachers, students and parents of the Princeton School District. The authors had full access to the data and take responsibility for its integrity. We have read and have agreed to the paper as written. This work was supported by NIH grants DK59183, 0M01 RR 08084, NHLBI (5K23HL80447) and a Trustee Grant from Cincinnati Children's Hospital.

Author information

Authors and Affiliations

  1. Division of Preventive Cardiology, Cincinnati Children's Hospital Medical Center, Cincinnati, OH, USA

    E M Urbina & P Khoury

  2. Division of Biostatistics and Epidemiology, Cincinnati Children's Hospital Medical Center, Cincinnati, OH, USA

    L J Martin

  3. Division of Endocrinology, Department of Internal Medicine, University of Cincinnati College of Medicine, Cincinnati, OH, USA

    D D'Alessio

  4. Department of Pediatrics, University of Cincinnati College of Medicine, Cincinnati, OH, USA

    E M Urbina, P Khoury, L J Martin & L M Dolan

  5. Division of Endocrinology, Cincinnati Children's Hospital Medical Center, Cincinnati, OH, USA

    L M Dolan

Authors
  1. E M Urbina
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. P Khoury
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. L J Martin
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. D D'Alessio
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. L M Dolan
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to E M Urbina.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Urbina, E., Khoury, P., Martin, L. et al. Gender differences in the relationships among obesity, adiponectin and brachial artery distensibility in adolescents and young adults. Int J Obes 33, 1118–1125 (2009). https://doi.org/10.1038/ijo.2009.164

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/ijo.2009.164

Keywords

This article is cited by

Search

Advanced search

Quick links