Skip to main content
Top
Published in: European Journal of Pediatrics 8/2013

01-08-2013 | Original Article

Impaired endothelial function in female adolescents with type 1 diabetes measured by peripheral artery tonometry

Authors: Aagje Pareyn, Karel Allegaert, Willeke Asscherickx, Eva Peirsman, Peter Verhamme, Kristina Casteels

Published in: European Journal of Pediatrics | Issue 8/2013

Login to get access

Abstract

Background

The reactive hyperemia peripheral artery tonometry (RH-PAT) is a newly developed method for non-invasive endothelial function assessment.

Objective

The goal of this study is to determine whether a significant difference in RH-PAT score is present between adolescents with type 1 diabetes (T1D) in comparison with controls.

Subjects and methods

Thirty-four adolescents with T1D and 25 control subjects (age 12–20 years) underwent RH-PAT endothelial function testing after an overnight fast. Height, weight, body mass index (BMI), blood pressure (BP), fasting lipid profile, Tanner stage, and glucose level were determined in each child.

Results

Adolescents with T1D had significantly lower RH-PAT scores compared to healthy controls, and this difference remained significant when overweight cases were not considered (p < 0.05). This difference was also observed in the female subgroup (p = 0.005). The interindividual variability in RH-PAT observations in T1D cases was not explained by BMI standard deviation score (SDS), BP SDS, age, duration of T1D, hemoglobin A1c, triglycerides, and pubertal stage, respectively.

Conclusions

The RH-PAT technique is used as a non-invasive test to assess for early vascular changes in high-risk patient groups. Endothelial dysfunction, measured by RH-PAT, was present in diabetic adolescent, especially in the female subgroup. Although additional longitudinal studies are required, early detection of this reversible process may have therapeutic and prognostic implications.
Literature
1.
go back to reference Bonetti PO, Pumper GM, Higano ST, Holmes DR Jr, Kuvin JT, Lerman A (2004) Noninvasive identification of patients with early coronary atherosclerosis by assessment of digital reactive hyperemia. J Am Coll Cardiol 44:2137–2141PubMedCrossRef Bonetti PO, Pumper GM, Higano ST, Holmes DR Jr, Kuvin JT, Lerman A (2004) Noninvasive identification of patients with early coronary atherosclerosis by assessment of digital reactive hyperemia. J Am Coll Cardiol 44:2137–2141PubMedCrossRef
2.
go back to reference Celermajer DS, Sorensen KE, Gooch VM et al (1992) Non-invasive detection of endothelial dysfunction in children and adults at risk of atherosclerosis. Lancet 340:1111–1115PubMedCrossRef Celermajer DS, Sorensen KE, Gooch VM et al (1992) Non-invasive detection of endothelial dysfunction in children and adults at risk of atherosclerosis. Lancet 340:1111–1115PubMedCrossRef
3.
go back to reference Chen Y, Osika W, Dangardt F, Gan LM, Strandvik B, Friberg P (2010) High levels of soluble intercellular adhesion molecule-1, insulin resistance and saturated fatty acids are associated with endothelial dysfunction in healthy adolescents. Atherosclerosis 211:638–642PubMedCrossRef Chen Y, Osika W, Dangardt F, Gan LM, Strandvik B, Friberg P (2010) High levels of soluble intercellular adhesion molecule-1, insulin resistance and saturated fatty acids are associated with endothelial dysfunction in healthy adolescents. Atherosclerosis 211:638–642PubMedCrossRef
4.
go back to reference Cole TJ, Bellizzi MC, Flegal KM, Dietz WH (2000) Establishing a standard definition for child overweight and obesity worldwide: international survey. BMJ 320:1240–1243PubMedCrossRef Cole TJ, Bellizzi MC, Flegal KM, Dietz WH (2000) Establishing a standard definition for child overweight and obesity worldwide: international survey. BMJ 320:1240–1243PubMedCrossRef
5.
go back to reference Corretti MC, Anderson TJ, Benjamin EJ et al (2002) Guidelines for the ultrasound assessment of endothelial-dependent flow-mediated vasodilation of the brachial artery: a report of the International Brachial Artery Reactivity Task Force. J Am Coll Cardiol 39:257–265PubMedCrossRef Corretti MC, Anderson TJ, Benjamin EJ et al (2002) Guidelines for the ultrasound assessment of endothelial-dependent flow-mediated vasodilation of the brachial artery: a report of the International Brachial Artery Reactivity Task Force. J Am Coll Cardiol 39:257–265PubMedCrossRef
6.
go back to reference De Angelis L, Millasseau SC, Smith A, Viberti G, Jones RH, Ritter JM, Chowienczyk PJ (2004) Sex differences in age-related stiffening of the aorta in subjects with type 2 diabetes. Hypertension 44:67–71PubMedCrossRef De Angelis L, Millasseau SC, Smith A, Viberti G, Jones RH, Ritter JM, Chowienczyk PJ (2004) Sex differences in age-related stiffening of the aorta in subjects with type 2 diabetes. Hypertension 44:67–71PubMedCrossRef
7.
go back to reference Dhindsa M, Sommerlad SM, DeVan AE, Barnes JN, Sugawara J, Ley O, Tanaka H (2008) Interrelationships among noninvasive measures of postischemic macro- and microvascular reactivity. J Appl Physiol 105:427–432PubMedCrossRef Dhindsa M, Sommerlad SM, DeVan AE, Barnes JN, Sugawara J, Ley O, Tanaka H (2008) Interrelationships among noninvasive measures of postischemic macro- and microvascular reactivity. J Appl Physiol 105:427–432PubMedCrossRef
8.
go back to reference Dziatkowiak H, Ciechanowska M, Wasikowa R et al (2002) Increase in the incidence of type 1 diabetes mellitus in children in three cities in Poland, 1987–1999. J Pediatr Endocrinol Metab 15:1153–1160PubMedCrossRef Dziatkowiak H, Ciechanowska M, Wasikowa R et al (2002) Increase in the incidence of type 1 diabetes mellitus in children in three cities in Poland, 1987–1999. J Pediatr Endocrinol Metab 15:1153–1160PubMedCrossRef
9.
go back to reference Fischer-Rasokat U, Spyridopoulos I, Walter J, Honold J, Zeiher AM, Fichtlscherer S (2012) Microvascular dysfunction and pulse wave reflection characterize different vascular pathologies in patients at cardiovascular risk. Vasa 41:192–199PubMedCrossRef Fischer-Rasokat U, Spyridopoulos I, Walter J, Honold J, Zeiher AM, Fichtlscherer S (2012) Microvascular dysfunction and pulse wave reflection characterize different vascular pathologies in patients at cardiovascular risk. Vasa 41:192–199PubMedCrossRef
10.
go back to reference Forte P, Kneale BJ, Milne E, Chowienczyk PJ, Johnston A, Benjamin N, Ritter JM (1998) Evidence for a difference in nitric oxide biosynthesis between healthy women and men. Hypertension 32:730–734PubMedCrossRef Forte P, Kneale BJ, Milne E, Chowienczyk PJ, Johnston A, Benjamin N, Ritter JM (1998) Evidence for a difference in nitric oxide biosynthesis between healthy women and men. Hypertension 32:730–734PubMedCrossRef
11.
12.
go back to reference Haller MJ, Stein J, Shuster J et al (2007) Peripheral artery tonometry demonstrates altered endothelial function in children with type 1 diabetes. Pediatr Diabetes 8:193–198PubMedCrossRef Haller MJ, Stein J, Shuster J et al (2007) Peripheral artery tonometry demonstrates altered endothelial function in children with type 1 diabetes. Pediatr Diabetes 8:193–198PubMedCrossRef
13.
go back to reference Hamburg NM, Keyes MJ, Larson MG et al (2008) Cross-sectional relations of digital vascular function to cardiovascular risk factors in the Framingham Heart Study. Circulation 117:2467–2474PubMedCrossRef Hamburg NM, Keyes MJ, Larson MG et al (2008) Cross-sectional relations of digital vascular function to cardiovascular risk factors in the Framingham Heart Study. Circulation 117:2467–2474PubMedCrossRef
14.
go back to reference Harrington J, Peña AS, Gent R, Hirte C, Couper J (2010) Aortic intima media thickness is an early marker of atherosclerosis in children with type 1 diabetes mellitus. J Pediatr 156:237–241PubMedCrossRef Harrington J, Peña AS, Gent R, Hirte C, Couper J (2010) Aortic intima media thickness is an early marker of atherosclerosis in children with type 1 diabetes mellitus. J Pediatr 156:237–241PubMedCrossRef
15.
go back to reference Järvisalo MJ, Raitakari M, Toikka JO et al (2004) Endothelial dysfunction and increased arterial intima-media thickness in children with type 1 diabetes. Circulation 109:1750–1755PubMedCrossRef Järvisalo MJ, Raitakari M, Toikka JO et al (2004) Endothelial dysfunction and increased arterial intima-media thickness in children with type 1 diabetes. Circulation 109:1750–1755PubMedCrossRef
16.
go back to reference Kannel WB, McGee DL (1979) Diabetes and cardiovascular disease. The Framingham study. JAMA 241:2035–2038PubMedCrossRef Kannel WB, McGee DL (1979) Diabetes and cardiovascular disease. The Framingham study. JAMA 241:2035–2038PubMedCrossRef
17.
go back to reference Kavey RE, Allada V, Daniels SR et al (2006) Cardiovascular risk reduction in high-risk pediatric patients: a scientific statement from the American Heart Association Expert Panel on Population and Prevention Science; the Councils on Cardiovascular Disease in the Young, Epidemiology and Prevention, Nutrition, Physical Activity and Metabolism, High Blood Pressure Research, Cardiovascular Nursing, and the Kidney in Heart Disease; and the Interdisciplinary Working Group on Quality of Care and Outcomes Research: endorsed by the American Academy of Pediatrics. Circulation 114:2710–2738PubMedCrossRef Kavey RE, Allada V, Daniels SR et al (2006) Cardiovascular risk reduction in high-risk pediatric patients: a scientific statement from the American Heart Association Expert Panel on Population and Prevention Science; the Councils on Cardiovascular Disease in the Young, Epidemiology and Prevention, Nutrition, Physical Activity and Metabolism, High Blood Pressure Research, Cardiovascular Nursing, and the Kidney in Heart Disease; and the Interdisciplinary Working Group on Quality of Care and Outcomes Research: endorsed by the American Academy of Pediatrics. Circulation 114:2710–2738PubMedCrossRef
18.
go back to reference Kim JA, Montagnani M, Koh KK, Quon MJ (2006) Reciprocal relationships between insulin resistance and endothelial dysfunction: molecular and pathophysiological mechanisms. Circulation 113:1888–1904PubMedCrossRef Kim JA, Montagnani M, Koh KK, Quon MJ (2006) Reciprocal relationships between insulin resistance and endothelial dysfunction: molecular and pathophysiological mechanisms. Circulation 113:1888–1904PubMedCrossRef
19.
go back to reference Kuvin JT, Patel AR, Sliney KA et al (2003) Assessment of peripheral vascular endothelial function with finger arterial pulse wave amplitude. Am Heart J 146:168–174PubMedCrossRef Kuvin JT, Patel AR, Sliney KA et al (2003) Assessment of peripheral vascular endothelial function with finger arterial pulse wave amplitude. Am Heart J 146:168–174PubMedCrossRef
20.
go back to reference Lantin-Hermoso RL, Rosenfeld CR, Yuhanna IS, German Z, Chen Z, Shaul PW (1997) Estrogen acutely stimulates nitric oxide synthase activity in fetal pulmonary artery endothelium. Am J Physiol 273:119–126 Lantin-Hermoso RL, Rosenfeld CR, Yuhanna IS, German Z, Chen Z, Shaul PW (1997) Estrogen acutely stimulates nitric oxide synthase activity in fetal pulmonary artery endothelium. Am J Physiol 273:119–126
22.
go back to reference Mahmud FH, Earing MG, Lee RA, Lteif AN, Driscoll DJ, Lerman A (2006) Altered endothelial function in asymptomatic male adolescents with type 1 diabetes. Congenit Heart Dis 1:98–103PubMedCrossRef Mahmud FH, Earing MG, Lee RA, Lteif AN, Driscoll DJ, Lerman A (2006) Altered endothelial function in asymptomatic male adolescents with type 1 diabetes. Congenit Heart Dis 1:98–103PubMedCrossRef
23.
go back to reference Mahmud FH, Van Uum S, Kanji N, Thiessen-Philbrook H, Clarson CL (2008) Impaired endothelial function in adolescents with type 1 diabetes mellitus. J Pediatr 152:557–562PubMedCrossRef Mahmud FH, Van Uum S, Kanji N, Thiessen-Philbrook H, Clarson CL (2008) Impaired endothelial function in adolescents with type 1 diabetes mellitus. J Pediatr 152:557–562PubMedCrossRef
24.
go back to reference Nadeau KJ, Regensteiner JG, Bauer TA et al (2010) Insulin resistance in adolescents with type 1 diabetes and its relationship to cardiovascular function. J Clin Endocrinol Metab 95:513–521PubMedCrossRef Nadeau KJ, Regensteiner JG, Bauer TA et al (2010) Insulin resistance in adolescents with type 1 diabetes and its relationship to cardiovascular function. J Clin Endocrinol Metab 95:513–521PubMedCrossRef
25.
go back to reference Nathan DM, Cleary PA, Backlund JY et al (2005) Intensive diabetes treatment and cardiovascular disease in patients with type 1 diabetes. N Engl J Med 353:2643–2653PubMedCrossRef Nathan DM, Cleary PA, Backlund JY et al (2005) Intensive diabetes treatment and cardiovascular disease in patients with type 1 diabetes. N Engl J Med 353:2643–2653PubMedCrossRef
26.
go back to reference Newkumet KM, Goble MM, Young RB, Kaplowitz PB, Schieken RM (1994) Altered blood pressure reactivity in adolescent diabetes. Pediatrics 93:616–621PubMed Newkumet KM, Goble MM, Young RB, Kaplowitz PB, Schieken RM (1994) Altered blood pressure reactivity in adolescent diabetes. Pediatrics 93:616–621PubMed
27.
go back to reference Nohria A, Gerhard-Herman M, Creager MA, Hurley S, Mitra D, Ganz P (2006) Role of nitric oxide in the regulation of digital pulse volume amplitude in humans. J Appl Physiol 101:545–548PubMedCrossRef Nohria A, Gerhard-Herman M, Creager MA, Hurley S, Mitra D, Ganz P (2006) Role of nitric oxide in the regulation of digital pulse volume amplitude in humans. J Appl Physiol 101:545–548PubMedCrossRef
28.
go back to reference Selamet Tierney ES, Newburger JW, Gauvreau K, Geva J, Coogan E, Colan SD, de Ferranti SD (2009) Endothelial pulse amplitude testing: feasibility and reproducibility in adolescents. J Pediatr 154:901–905PubMedCrossRef Selamet Tierney ES, Newburger JW, Gauvreau K, Geva J, Coogan E, Colan SD, de Ferranti SD (2009) Endothelial pulse amplitude testing: feasibility and reproducibility in adolescents. J Pediatr 154:901–905PubMedCrossRef
29.
go back to reference Toumba M, Savva SC, Bacopoulou I, Apsiotou T, Georgiou T, Stavrou S, Skordis N (2007) Rising incidence of type 1 diabetes mellitus in children and adolescents in Cyprus in 2000–2004. Pediatr Diabetes 8:374–376PubMedCrossRef Toumba M, Savva SC, Bacopoulou I, Apsiotou T, Georgiou T, Stavrou S, Skordis N (2007) Rising incidence of type 1 diabetes mellitus in children and adolescents in Cyprus in 2000–2004. Pediatr Diabetes 8:374–376PubMedCrossRef
30.
go back to reference Wexler DJ, Grant RW, Meigs JB, Nathan DM, Cagliero E (2005) Sex disparities in treatment of cardiac risk factors in patients with type 2 diabetes. Diabetes Care 28:514–520PubMedCrossRef Wexler DJ, Grant RW, Meigs JB, Nathan DM, Cagliero E (2005) Sex disparities in treatment of cardiac risk factors in patients with type 2 diabetes. Diabetes Care 28:514–520PubMedCrossRef
31.
go back to reference Widlansky ME, Gokce N, Keaney JF Jr, Vita JA (2003) The clinical implications of endothelial dysfunction. J Am Coll Cardiol 42:1149–1160PubMedCrossRef Widlansky ME, Gokce N, Keaney JF Jr, Vita JA (2003) The clinical implications of endothelial dysfunction. J Am Coll Cardiol 42:1149–1160PubMedCrossRef
32.
go back to reference Wilkinson IB, Webb DJ (2001) Venous occlusion plethysmography in cardiovascular research: methodology and clinical applications. J Clin Pharmacol 52:631–646 Wilkinson IB, Webb DJ (2001) Venous occlusion plethysmography in cardiovascular research: methodology and clinical applications. J Clin Pharmacol 52:631–646
33.
go back to reference Writing Team for the Diabetes Control and Complications Trail/Epidemiology of Diabetes Interventions and Complications Research Group (2002) Effect of intensive therapy on the microvascular complications of type 1 diabetes mellitus. JAMA 287:2563–2569CrossRef Writing Team for the Diabetes Control and Complications Trail/Epidemiology of Diabetes Interventions and Complications Research Group (2002) Effect of intensive therapy on the microvascular complications of type 1 diabetes mellitus. JAMA 287:2563–2569CrossRef
Metadata
Title
Impaired endothelial function in female adolescents with type 1 diabetes measured by peripheral artery tonometry
Authors
Aagje Pareyn
Karel Allegaert
Willeke Asscherickx
Eva Peirsman
Peter Verhamme
Kristina Casteels
Publication date
01-08-2013
Publisher
Springer Berlin Heidelberg
Published in
European Journal of Pediatrics / Issue 8/2013
Print ISSN: 0340-6199
Electronic ISSN: 1432-1076
DOI
https://doi.org/10.1007/s00431-013-1988-5

Other articles of this Issue 8/2013

European Journal of Pediatrics 8/2013 Go to the issue