Skip to main content
Top
Published in: European Journal of Applied Physiology 12/2013

01-12-2013 | Original Article

Adolescent blood pressure hyperreactors have a higher reactive hyperemic index at the fingertip

Authors: Thomas Radtke, Prisca Eser, Susi Kriemler, Hugo Saner, Matthias Wilhelm

Published in: European Journal of Applied Physiology | Issue 12/2013

Login to get access

Abstract

Purpose

The use of peripheral arterial tonometry (PAT) to assess microvascular endothelial function is getting increasingly popular in the pediatric population. The aim of the present study was to examine the impact of blood pressure (BP) hyperreactivity on microvascular hyperemic reaction in healthy, normotensive adolescents.

Methods

Fifty-two adolescents with a mean age of 14.5 ± 0.7 years were investigated. Microvascular endothelial function was assessed at rest and after exhaustive cycling exercise using PAT to determine the reactive hyperemic index (RHI, primary endpoint). Hyperreactors were identified according to their cardiovascular response to a cold pressor test. Indices of autonomic tone were assessed with an ambulatory electrocardiograph and cardiopulmonary exercise testing was performed on a cycle ergometer. Physical activity was measured using accelerometry. ANOVA with repeated measures and Tukey HSD post hoc tests were applied to determine differences between BP hyperreactors and controls (normal reactors).

Results

Sixteen adolescents were identified as hyperreactors and matched with regard to age, sex, pubertal status, and height with 16 normal reactors. At rest, hyperreactors had a significantly higher RHI than normal reactors (2.1 ± 0.4 vs. 1.6 ± 0.4, P = 0.003). After exhaustive cycling exercise, the differences in RHI were abolished. No differences between these two groups existed in physical activity levels, exercise capacity and indices of autonomic tone.

Conclusions

Our data suggest that normotensive hyperreactors have a markedly higher RHI compared to normal reactors. Future studies using PAT to assess microvascular endothelial function should bare in mind the large effect of vascular hyperreactivity.
Literature
go back to reference Abboud FM, Harwani SC, Chapleau MW (2012) Autonomic neural regulation of the immune system: implications for hypertension and cardiovascular disease. Hypertension 59:755–762PubMedCrossRef Abboud FM, Harwani SC, Chapleau MW (2012) Autonomic neural regulation of the immune system: implications for hypertension and cardiovascular disease. Hypertension 59:755–762PubMedCrossRef
go back to reference Armstrong N, Williams J, Balding J, Gentle P, Kirby B (1991) The peak oxygen uptake of British children with reference to age, sex and sexual maturity. Eur J Appl Physiol Occup Physiol 62:369–375PubMedCrossRef Armstrong N, Williams J, Balding J, Gentle P, Kirby B (1991) The peak oxygen uptake of British children with reference to age, sex and sexual maturity. Eur J Appl Physiol Occup Physiol 62:369–375PubMedCrossRef
go back to reference Barnett PH, Hines EA Jr, Schirger A, Gage RP (1963) Blood pressure and vascular reactivity to the cold pressor test. Restudy of 207 subjects 27 years later. JAMA 183:845–848PubMedCrossRef Barnett PH, Hines EA Jr, Schirger A, Gage RP (1963) Blood pressure and vascular reactivity to the cold pressor test. Restudy of 207 subjects 27 years later. JAMA 183:845–848PubMedCrossRef
go back to reference Berntson GG, Bigger JT Jr, Eckberg DL, Grossman P, Kaufmann PG, Malik M, Nagaraja HN, Porges SW, Saul JP, Stone PH, Van der Molen MW (1997) Heart rate variability: origins, methods, and interpretive caveats. Psychophysiology 34:623–648PubMedCrossRef Berntson GG, Bigger JT Jr, Eckberg DL, Grossman P, Kaufmann PG, Malik M, Nagaraja HN, Porges SW, Saul JP, Stone PH, Van der Molen MW (1997) Heart rate variability: origins, methods, and interpretive caveats. Psychophysiology 34:623–648PubMedCrossRef
go back to reference Chen Y, Dangardt F, Osika W, Berggren K, Gronowitz E, Friberg P (2012) Age- and sex-related differences in vascular function and vascular response to mental stress longitudinal and cross-sectional studies in a cohort of healthy children and adolescents. Atherosclerosis 220:269–274PubMedCrossRef Chen Y, Dangardt F, Osika W, Berggren K, Gronowitz E, Friberg P (2012) Age- and sex-related differences in vascular function and vascular response to mental stress longitudinal and cross-sectional studies in a cohort of healthy children and adolescents. Atherosclerosis 220:269–274PubMedCrossRef
go back to reference Coffman JD (1994) Effects of endothelium-derived nitric oxide on skin and digital blood flow in humans. Am J Physiol Heart Circ Physiol 267:H2087–H2090 Coffman JD (1994) Effects of endothelium-derived nitric oxide on skin and digital blood flow in humans. Am J Physiol Heart Circ Physiol 267:H2087–H2090
go back to reference Fernandez JR, Redden DT, Pietrobelli A, Allison DB (2004) Waist circumference percentiles in nationally representative samples of African-American, European-American, and Mexican-American children and adolescents. J Pediatr 145:439–444PubMedCrossRef Fernandez JR, Redden DT, Pietrobelli A, Allison DB (2004) Waist circumference percentiles in nationally representative samples of African-American, European-American, and Mexican-American children and adolescents. J Pediatr 145:439–444PubMedCrossRef
go back to reference Flaa A, Eide IK, Kjeldsen SE, Rostrup M (2008) Sympathoadrenal stress reactivity is a predictor of future blood pressure: an 18-year follow-up study. Hypertension 52:336–341PubMedCrossRef Flaa A, Eide IK, Kjeldsen SE, Rostrup M (2008) Sympathoadrenal stress reactivity is a predictor of future blood pressure: an 18-year follow-up study. Hypertension 52:336–341PubMedCrossRef
go back to reference Forte P, Copland M, Smith LM, Milne E, Sutherland J, Benjamin N (1997) Basal nitric oxide synthesis in essential hypertension. Lancet 349:837–842PubMedCrossRef Forte P, Copland M, Smith LM, Milne E, Sutherland J, Benjamin N (1997) Basal nitric oxide synthesis in essential hypertension. Lancet 349:837–842PubMedCrossRef
go back to reference Haller MJ, Stein J, Shuster J, Theriaque D, Silverstein J, Schatz DA, Earing MG, Lerman A, Mahmud FH (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, Theriaque D, Silverstein J, Schatz DA, Earing MG, Lerman A, Mahmud FH (2007) Peripheral artery tonometry demonstrates altered endothelial function in children with type 1 diabetes. Pediatr Diabetes 8:193–198PubMedCrossRef
go back to reference Hamburg NM, Palmisano J, Larson MG, Sullivan LM, Lehman BT, Vasan RS, Levy D, Mitchell GF, Vita JA, Benjamin EJ (2011) Relation of brachial and digital measures of vascular function in the community: the Framingham heart study. Hypertension 57:390–396PubMedCrossRef Hamburg NM, Palmisano J, Larson MG, Sullivan LM, Lehman BT, Vasan RS, Levy D, Mitchell GF, Vita JA, Benjamin EJ (2011) Relation of brachial and digital measures of vascular function in the community: the Framingham heart study. Hypertension 57:390–396PubMedCrossRef
go back to reference Hautala AJ, Makikallio TH, Seppanen T, Huikuri HV, Tulppo MP (2003) Short-term correlation properties of R–R interval dynamics at different exercise intensity levels. Clin Physiol Funct Imaging 23:215–223PubMedCrossRef Hautala AJ, Makikallio TH, Seppanen T, Huikuri HV, Tulppo MP (2003) Short-term correlation properties of RR interval dynamics at different exercise intensity levels. Clin Physiol Funct Imaging 23:215–223PubMedCrossRef
go back to reference Hayashi K, Miyachi M, Seno N, Takahashi K, Yamazaki K, Sugawara J, Yokoi T, Onodera S, Mesaki N (2006) Variations in carotid arterial compliance during the menstrual cycle in young women. Exp Physiol 91:465–472PubMedCrossRef Hayashi K, Miyachi M, Seno N, Takahashi K, Yamazaki K, Sugawara J, Yokoi T, Onodera S, Mesaki N (2006) Variations in carotid arterial compliance during the menstrual cycle in young women. Exp Physiol 91:465–472PubMedCrossRef
go back to reference Hines EA (1937) Reaction of the blood pressure of 400 school children to a standard stimulus. JAMA 108:1249–1250CrossRef Hines EA (1937) Reaction of the blood pressure of 400 school children to a standard stimulus. JAMA 108:1249–1250CrossRef
go back to reference Hines EA, Brown GE (1936) The cold pressor test for measuring the reactivity of the blood pressure: data concerning 571 normal and hypertensive subjects. Am Heart J 11:1–9CrossRef Hines EA, Brown GE (1936) The cold pressor test for measuring the reactivity of the blood pressure: data concerning 571 normal and hypertensive subjects. Am Heart J 11:1–9CrossRef
go back to reference Kasagi F, Akahoshi M, Shimaoka K (1995) Relation between cold pressor test and development of hypertension based on 28-year follow-up. Hypertension 25:71–76PubMedCrossRef Kasagi F, Akahoshi M, Shimaoka K (1995) Relation between cold pressor test and development of hypertension based on 28-year follow-up. Hypertension 25:71–76PubMedCrossRef
go back to reference Lee CR, Bass A, Ellis K, Tran B, Steele S, Caughey M, Stouffer GA, Hinderliter AL (2012) Relation between digital peripheral arterial tonometry and brachial artery ultrasound measures of vascular function in patients with coronary artery disease and in healthy volunteers. Am J Cardiol 109:651–657PubMedCrossRef Lee CR, Bass A, Ellis K, Tran B, Steele S, Caughey M, Stouffer GA, Hinderliter AL (2012) Relation between digital peripheral arterial tonometry and brachial artery ultrasound measures of vascular function in patients with coronary artery disease and in healthy volunteers. Am J Cardiol 109:651–657PubMedCrossRef
go back to reference Mahmud FH, Hill DJ, Cuerden MS, Clarson CL (2009) Impaired vascular function in obese adolescents with insulin resistance. J Pediatr 155:678–682PubMedCrossRef Mahmud FH, Hill DJ, Cuerden MS, Clarson CL (2009) Impaired vascular function in obese adolescents with insulin resistance. J Pediatr 155:678–682PubMedCrossRef
go back to reference Masse LC, Fuemmeler BF, Anderson CB, Matthews CE, Trost SG, Catellier DJ, Treuth M (2005) Accelerometer data reduction: a comparison of four reduction algorithms on select outcome variables. Med Sci Sports Exerc 37:S544–S554PubMedCrossRef Masse LC, Fuemmeler BF, Anderson CB, Matthews CE, Trost SG, Catellier DJ, Treuth M (2005) Accelerometer data reduction: a comparison of four reduction algorithms on select outcome variables. Med Sci Sports Exerc 37:S544–S554PubMedCrossRef
go back to reference Menkes MS, Matthews KA, Krantz DS, Lundberg U, Mead LA, Qaqish B, Liang KY, Thomas CB, Pearson TA (1989) Cardiovascular reactivity to the cold pressor test as a predictor of hypertension. Hypertension 14:524–530PubMedCrossRef Menkes MS, Matthews KA, Krantz DS, Lundberg U, Mead LA, Qaqish B, Liang KY, Thomas CB, Pearson TA (1989) Cardiovascular reactivity to the cold pressor test as a predictor of hypertension. Hypertension 14:524–530PubMedCrossRef
go back to reference Morris NM, Udry JR (1980) Validation of a self-administered instrument to assess stage of adolescent development. J Youth Adolesc 9:271–280CrossRef Morris NM, Udry JR (1980) Validation of a self-administered instrument to assess stage of adolescent development. J Youth Adolesc 9:271–280CrossRef
go back to reference National High Blood Pressure Education Program Working Group on High Blood Pressure in Children and Adolescents (2004) The fourth report on the diagnosis, evaluation, and treatment of high blood pressure in children and adolescents. Pediatrics 114:555–576CrossRef National High Blood Pressure Education Program Working Group on High Blood Pressure in Children and Adolescents (2004) The fourth report on the diagnosis, evaluation, and treatment of high blood pressure in children and adolescents. Pediatrics 114:555–576CrossRef
go back to reference Niskanen JP, Tarvainen MP, Ranta-Aho PO, Karjalainen PA (2004) Software for advanced HRV analysis. Comput Methods Programs Biomed 76:73–81PubMedCrossRef Niskanen JP, Tarvainen MP, Ranta-Aho PO, Karjalainen PA (2004) Software for advanced HRV analysis. Comput Methods Programs Biomed 76:73–81PubMedCrossRef
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
go back to reference Paridon SM, Alpert BS, Boas SR, Cabrera ME, Caldarera LL, Daniels SR, Kimball TR, Knilans TK, Nixon PA, Rhodes J, Yetman AT (2006) Clinical stress testing in the pediatric age group: a statement from the American Heart Association Council on Cardiovascular Disease in the Young, Committee on Atherosclerosis, Hypertension, and Obesity in Youth. Circulation 113:1905–1920PubMedCrossRef Paridon SM, Alpert BS, Boas SR, Cabrera ME, Caldarera LL, Daniels SR, Kimball TR, Knilans TK, Nixon PA, Rhodes J, Yetman AT (2006) Clinical stress testing in the pediatric age group: a statement from the American Heart Association Council on Cardiovascular Disease in the Young, Committee on Atherosclerosis, Hypertension, and Obesity in Youth. Circulation 113:1905–1920PubMedCrossRef
go back to reference Peng CK, Havlin S, Stanley HE, Goldberger AL (1995) Quantification of scaling exponents and crossover phenomena in nonstationary heartbeat time series. Chaos 5:82–87PubMedCrossRef Peng CK, Havlin S, Stanley HE, Goldberger AL (1995) Quantification of scaling exponents and crossover phenomena in nonstationary heartbeat time series. Chaos 5:82–87PubMedCrossRef
go back to reference Radtke T, Khattab K, Eser P, Kriemler S, Saner H, Wilhelm M (2012) Puberty and microvascular function in healthy children and adolescents. J Pediatr 161:887–891PubMedCrossRef Radtke T, Khattab K, Eser P, Kriemler S, Saner H, Wilhelm M (2012) Puberty and microvascular function in healthy children and adolescents. J Pediatr 161:887–891PubMedCrossRef
go back to reference Radtke T, Khattab K, Brugger N, Eser P, Saner H, Wilhelm M (2013a) High-volume sports club participation and autonomic nervous system activity in children. Eur J Clin Invest. doi:10.1111/eci.12112 PubMed Radtke T, Khattab K, Brugger N, Eser P, Saner H, Wilhelm M (2013a) High-volume sports club participation and autonomic nervous system activity in children. Eur J Clin Invest. doi:10.​1111/​eci.​12112 PubMed
go back to reference Radtke T, Kriemler S, Eser P, Saner H, Wilhelm M (2013b) Physical activity intensity and surrogate markers for cardiovascular health in adolescents. Eur J Appl Physiol 113:1213–1222PubMedCrossRef Radtke T, Kriemler S, Eser P, Saner H, Wilhelm M (2013b) Physical activity intensity and surrogate markers for cardiovascular health in adolescents. Eur J Appl Physiol 113:1213–1222PubMedCrossRef
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
go back to reference Tarvainen MP, Ranta-Aho PO, Karjalainen PA (2002) An advanced detrending method with application to HRV analysis. IEEE Trans Biomed Eng 49:172–175PubMedCrossRef Tarvainen MP, Ranta-Aho PO, Karjalainen PA (2002) An advanced detrending method with application to HRV analysis. IEEE Trans Biomed Eng 49:172–175PubMedCrossRef
go back to reference Task Force of the European Society of Cardiology and the North American Society of Pacing and Electrophysiology (1996) Heart rate variability: standards of measurement, physiological interpretation and clinical use. Circulation 93:1043–1065CrossRef Task Force of the European Society of Cardiology and the North American Society of Pacing and Electrophysiology (1996) Heart rate variability: standards of measurement, physiological interpretation and clinical use. Circulation 93:1043–1065CrossRef
go back to reference Treuth MS, Schmitz K, Catellier DJ, McMurray RG, Murray DM, Almeida MJ, Going S, Norman JE, Pate R (2004) Defining accelerometer thresholds for activity intensities in adolescent girls. Med Sci Sports Exerc 36:1259–1266PubMedCrossRef Treuth MS, Schmitz K, Catellier DJ, McMurray RG, Murray DM, Almeida MJ, Going S, Norman JE, Pate R (2004) Defining accelerometer thresholds for activity intensities in adolescent girls. Med Sci Sports Exerc 36:1259–1266PubMedCrossRef
go back to reference Tulppo MP, Kiviniemi AM, Hautala AJ, Kallio M, Seppanen T, Makikallio TH, Huikuri Heikki V (2005) Physiological background of the loss of fractal heart rate dynamics. Circulation 112:314–319PubMedCrossRef Tulppo MP, Kiviniemi AM, Hautala AJ, Kallio M, Seppanen T, Makikallio TH, Huikuri Heikki V (2005) Physiological background of the loss of fractal heart rate dynamics. Circulation 112:314–319PubMedCrossRef
go back to reference Van Zwieten PA, Timmermans PB, Brummelen P (1984) Role of alpha adrenoreceptors in hypertension and in antihypertensive drug treatment. Am J Med 77:17–25PubMed Van Zwieten PA, Timmermans PB, Brummelen P (1984) Role of alpha adrenoreceptors in hypertension and in antihypertensive drug treatment. Am J Med 77:17–25PubMed
go back to reference Victor RG, Leimbach WN Jr, Seals DR, Wallin BG, Mark AL (1987) Effects of the cold pressor test on muscle sympathetic nerve activity in humans. Hypertension 9:429–436PubMedCrossRef Victor RG, Leimbach WN Jr, Seals DR, Wallin BG, Mark AL (1987) Effects of the cold pressor test on muscle sympathetic nerve activity in humans. Hypertension 9:429–436PubMedCrossRef
go back to reference Wood DL, Sheps SG, Elveback LR, Schirger A (1984) Cold pressor test as a predictor of hypertension. Hypertension 6:301–306PubMedCrossRef Wood DL, Sheps SG, Elveback LR, Schirger A (1984) Cold pressor test as a predictor of hypertension. Hypertension 6:301–306PubMedCrossRef
Metadata
Title
Adolescent blood pressure hyperreactors have a higher reactive hyperemic index at the fingertip
Authors
Thomas Radtke
Prisca Eser
Susi Kriemler
Hugo Saner
Matthias Wilhelm
Publication date
01-12-2013
Publisher
Springer Berlin Heidelberg
Published in
European Journal of Applied Physiology / Issue 12/2013
Print ISSN: 1439-6319
Electronic ISSN: 1439-6327
DOI
https://doi.org/10.1007/s00421-013-2735-3

Other articles of this Issue 12/2013

European Journal of Applied Physiology 12/2013 Go to the issue