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Cardiovascular risk in nonobese hypertensive adolescents: a study based on plasma biomarkers and ultrasonographic assessment of early atherosclerosis

Journal of Human Hypertension volume 27, pages 191–196 (2013)Cite this article

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Abstract

The objective of this study was to investigate the vascular status, left-ventricular mass and biomarkers of endothelial activation in hypertensive (HT) adolescents, with particular attention to comparing nonobese with obese patients. Seventy-nine newly diagnosed HT adolescents aged 15.1±2.1 years (divided into 34 nonobese and 45 obese) were compared with 35 healthy volunteers. Intima–media thickness (IMT), flow-mediated dilation (FMD) and left-ventricular mass index (LVMi) were determined using ultrasound. Adhesion molecules and inflammatory interleukins (ILs), together with lipids and insulin resistance (HOMA), were also studied. HT obese adolescents had higher triglycerides, HOMA, and elevated levels of interleukin-6, tumor necrosis factor-α, soluble intercellular adhesion molecule-1 and soluble E-selectin compared with controls and nonobese HT patients. FMD was lower in HT groups (8.5±4.5% in nonobese, P=0.004; 8.1±4.9%, P=0.01 in obese vs 12.5±4.9%; in control), and IMT was higher (0.52±0.06 mm, P<0.001 in nonobese; 0.54±0.05 mm, P<0.001 in obese vs 0.42±0.05 mm in control). Higher LVMi was found in both HT groups, with the highest value in the nonobese group being 37.8±5.3 g m−2.7 vs 28.4±5.3 g m−2.7 in controls (P=0.003). In conclusion, nonobese HT adolescents had the same early cardiovascular deteriorations assessed ultrasonographically as their obese HT peers, although metabolic alterations and endothelial activation measured as plasma biomarkers were more pronounced in obese individuals. The potential mechanisms of early atherosclerosis in nonobese HT adolescents need further evaluation in prospective studies because these factors may differ considerably from those found in young obese individuals with HT.

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References

  1. Urbina EM, Williams RV, Alpert BS, Collins RT, Daniels SR, Hayman L et al. Noninvasive assessment of subclinical atherosclerosis in children and adolescents: recommendations for standard assessment for clinical research: a scientific statement from the American Heart Association. Hypertension 2009; 54: 919–950.

    Article  CAS  Google Scholar 

  2. Rosamond W, Flegal K, Furie K, Go A, Greenlund K, Haase N et al. Heart disease and stroke statistics--2008 update: a report from the American Heart Association Statistics Committee and Stroke Statistics Subcommittee. Circulation 2008; 17: e25–146.

    Google Scholar 

  3. Bao W, Srinivasan SR, Wattigney WA, Berenson GS . Persistence of multiple cardiovascular risk clustering related to syndrome X from childhood to young adulthood. The Bogalusa Heart Study. Arch Intern Med 1994; 154: 1842–1847.

    Article  CAS  Google Scholar 

  4. Bao W, Threefoot SA, Srinivasan SR, Berenson GS . Essential hypertension predicted by tracking of elevated blood pressure from childhood to adulthood: the Bogalusa Heart Study. Am J Hypertens 1995; 8: 657–665.

    Article  CAS  Google Scholar 

  5. Aggoun Y, Farpour-Lambert NJ, Marchand LM, Golay E, Maggio AB, Beghetti M . Impaired endothelial and smooth muscle functions and arterial stiffness appear before puberty in obese children and are associated with elevated ambulatory blood pressure. Eur Heart J 2008; 29: 792–799.

    Article  Google Scholar 

  6. Brady TM, Fivush B, Flynn JT, Parekh R . Ability of blood pressure to predict left ventricular hypertrophy in children with primary hypertension. J Pediatr 2008; 152: 73–78, e1.

    Article  Google Scholar 

  7. Li S, Chen W, Srinivasan SR, Berenson GS . Childhood blood pressure as a predictor of arterial stiffness in young adults: The Bogalusa Heart Study. Hypertension 2004; 43: 541–546.

    Article  Google Scholar 

  8. Hansen ML, Gunn PW, Kaelber DC . Underdiagnosis of hypertension in children and adolescents. JAMA 2007; 298: 874–879.

    Article  CAS  Google Scholar 

  9. Balagopal PB, de Ferranti SD, Cook S, Daniels SR, Gidding SS, Hayman LL et al. Nontraditional risk factors and biomarkers for cardiovascular disease: mechanistic, research and clinical considerations for youth: a scientific statement from the American Heart Association. Circulation 2011; 123: 2749–2769.

    Article  Google Scholar 

  10. Sorof J, Daniels S . Obesity hypertension in children: a problem of epidemic proportions. Hypertension 2002; 40: 441–447.

    Article  CAS  Google Scholar 

  11. Raj M, Sundaram KR, Paul M, Sudhakar A, Kumar RK . Body mass index trend and its association with blood pressure distribution in children. J Hum Hypertens 2010; 24: 652–658.

    Article  CAS  Google Scholar 

  12. Rahmouni K, Correia ML, Haynes WG, Mark AL . Obesity-associated hypertension: new insights into mechanisms. Hypertension 2005; 45: 9–14.

    Article  CAS  Google Scholar 

  13. Glowinska-Olszewska B, Tolwinska J, Urban M . Relationship between endothelial dysfunction, carotid artery intima media thickness and circulating markers of vascular inflammation in obese hypertensive children and adolescents. J Pediatr Endocrinol Metab 2007; 20: 1125–1136.

    Article  CAS  Google Scholar 

  14. Lande MB, Carson NL, Roy J, Meagher CC . Effects of childhood primary hypertension on carotid intima media thickness: a matched controlled study. Hypertension 2006; 48: 40–44.

    Article  CAS  Google Scholar 

  15. Litwin M, Trelewicz J, Wawer Z, Antoniewicz J, Wierzbicka A, Rajszys P et al. Intima-media thickness and arterial elasticity in hypertensive children: controlled study. Pediatr Nephrol 2004; 19: 767–774.

    Article  Google Scholar 

  16. 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 

  17. Urbina EM, Alpert B, Flynn J, Hayman L, Harshfield GA, Jacobson M et al. Ambulatory Blood Pressure Monitoring in Children and Adolescents: Recommendations for Standard Assessment. A Scientific Statement From the American Heart Association Atherosclerosis, Hypertension, and Obesity in Youth Committee of the Council on Cardiovascular Disease in the Young and the Council for High Blood Pressure Research. Hypertension 2008; 52: 433–451.

    Article  CAS  Google Scholar 

  18. Nawarycz T, Ostrowska-Nawarycz L . Body mass index in the school age children and youth from the city of Lodz. Pol Merkur Lekarski 2007; 23: 264–270.

    PubMed  Google Scholar 

  19. Coretti MC, Anderson TJ, Benjamin EJ, Celermajer D, Charbonneau F, Creager MA et al. Guidelines for the ultrasound assessment of endothelial-dependent flow-mediated vasodilation of the brachial artery. J Am Coll Cardiol 2002; 39: 257–265.

    Article  Google Scholar 

  20. Jourdan C, Wuhl E, Litwin M, Fahr K, Trelewicz J, Jobs K et al. Normative values for intima-media thickness and distensibility of large arteries in healthy adolescents. J Hypertens 2005; 23: 1707–1715.

    Article  CAS  Google Scholar 

  21. Daniels SR, Kimball TR, Morrison JA, Khoury P, Meyer RA . Indexing left ventricular mass to account for differences in body size in children and adolescents without cardiovascular disease. Am J Cardiol 1995; 76: 699–701.

    Article  CAS  Google Scholar 

  22. de Simone G, Devereux RB, Daniels SR, Koren MJ, Meyer RA, Laragh JH . Effect of growth on variability of left ventricular mass: assessment of allometric signals in adults and children and their capacity to predict cardiovascular risk. J Am Coll Cardiol 1995; 25: 1056–1062.

    Article  CAS  Google Scholar 

  23. Burke GL, Evans GW, Riley WA, Sharrett AR, Howard G, Barnes RW et al. Arterial wall thickness is associated with prevalent cardiovascular disease in middle-aged adults. The Atherosclerosis Risk in Communities (ARIC) Study. Stroke 1995; 26: 386–391.

    Article  CAS  Google Scholar 

  24. Krantz JS, Mack WJ, Hodis HN, Liu CR, Liu CH, Kaufman FR . Early onset of subclinical atherosclerosis in young persons with type 1 diabetes. J Pediatr 2004; 145: 452–457.

    Article  Google Scholar 

  25. Lavrencic A, Kosmina B, Keber I, Videcnik V, Keber D . Carotid intima-media thickness in young patients with familial hypercholesterolaemia. Heart 1996; 76: 321–325.

    Article  CAS  Google Scholar 

  26. Ayer JG, Harmer JA, Nakhla S, Xuan W, Ng MK, Raitakari OT et al. HDL-cholesterol, blood pressure, and asymmetric dimethylarginine are significantly associated with arterial wall thickness in children. Arterioscler Thromb Vasc Biol 2009; 29: 943–949.

    Article  CAS  Google Scholar 

  27. Hanevold C, Waller J, Daniels S, Portman R, Sorof J . The effects of obesity, gender, and ethnic group on left ventricular hypertrophy and geometry in hypertensive children: a collaborative study of the International Pediatric Hypertension Association. Pediatrics 2004; 113: 328–333.

    Article  Google Scholar 

  28. Litwin M, Niemirska A, Sladowska J, Antoniewicz J, Daszkowska J, Wierzbicka A et al. Left ventricular hypertrophy and arterial wall thickening in children with essential hypertension. Pediatr Nephrol 2006; 21: 811–819.

    Article  Google Scholar 

  29. Meyer AA, Kundt G, Steiner M, Schuff-Werner P, Kienast W . Impaired flow-mediated vasodilation, carotid artery intima-media thickening, and elevated endothelial plasma markers in obese children: the impact of cardiovascular risk factors. Pediatrics 2006; 117: 1560–1567.

    Article  Google Scholar 

  30. Kapiotis S, Holzer G, Schaller G, Haumer M, Widhalm H, Weghuber D et al. A proinflammatory state is detectable in obese children and is accompanied by functional and morphological vascular changes. Arterioscler Thromb Vasc Biol 2006; 26: 2541–2546.

    Article  CAS  Google Scholar 

  31. Kampoli AM, Tousoulis D, Antoniades C, Siasos G, Stefanadis C . Biomarkers of premature atherosclerosis. Trends Mol Med 2009; 15: 323–332.

    Article  CAS  Google Scholar 

  32. Ridker PM . High sensitivity C-reactive protein, inflammation and cardiovascular risk: from concept to clinical practice to clinical benefit. Am Heart J 2004; 148: S19–S26.

    Article  CAS  Google Scholar 

  33. Reinehr T, Kiess W, de Sousa G, Stoffel-Wagner B, Wunsch R . Intima media thickness in childhood obesity: relations to inflammatory marker, glucose metabolism, and blood pressure. Metabolism 2006; 55: 113–118.

    Article  CAS  Google Scholar 

  34. Akinci G, Akinci B, Coskun S, Bayindir P, Hekimsoy Z, Ozmen B . Evaluation of markers of inflammation, insulin resistance and endothelial dysfunction in children at risk for overweight. Hormones (Athens) 2008; 7: 156–162.

    Article  Google Scholar 

  35. Glowinska B, Urban M, Koput A . Cardiovascular risk factors in children with obesity, hypertension and diabetes: lipoprotein (a) levels and body mass index correlate with family history of cardiovascular disease. Eur J Pediatr 2002; 161: 511–518.

    Article  CAS  Google Scholar 

  36. Solini A, Santini E, Passaro A, Madec S, Ferrannini E . Family history of hypertension, anthropometric parameters and markers of early atherosclerosis in young healthy individuals. J Hum Hypertens 2009; 23: 801–807.

    Article  CAS  Google Scholar 

  37. Falkner B, Lurbe E, Schaefer F . High blood pressure in children: clinical and health policy implications. J Clin Hypertens (Greenwich) 2010; 12: 261–276.

    Article  Google Scholar 

  38. Gopinath B, Baur LA, Hardy LL, Kifley A, Rose KA, Wong TY et al. Relationship between a range of sedentary behaviours and blood pressure during early adolescence. J Hum Hypertens (e-pub ahead of print 26 May 2011; doi:10.1038/jhh.2011.40).

  39. Assadi F . Effect of microalbuminuria lowering on regression of left ventricular hypertrophy in children and adolescents with essential hypertension. Pediatr Cardiol 2007; 28: 27–33.

    Article  Google Scholar 

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Acknowledgements

This study was supported by the Polish State Committee for Scientific Research (grant number NN407144639).

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Authors and Affiliations

  1. Department of Paediatrics, Diabetology with Cardiology Division, Endocrinology, Medical University of Białystok, Białystok University Children's Hospital, Białystok, Poland

    B Głowińska-Olszewska, J Tołwińska, W Łuczyński & A Bossowski

  2. Department of Paediatrics and Developmental Disorders, Medical University of Białystok, Białystok, Poland

    J Konstantynowicz

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  1. B Głowińska-Olszewska
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Correspondence to B Głowińska-Olszewska.

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Głowińska-Olszewska, B., Tołwińska, J., Łuczyński, W. et al. Cardiovascular risk in nonobese hypertensive adolescents: a study based on plasma biomarkers and ultrasonographic assessment of early atherosclerosis. J Hum Hypertens 27, 191–196 (2013). https://doi.org/10.1038/jhh.2012.11

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