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Published in: Respiratory Research 1/2017

Open Access 01-12-2017 | Letter to the Editor

Vascular function in asthmatic children and adolescents

Published in: Respiratory Research | Issue 1/2017

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Abstract

Background

Epidemiological studies have demonstrated an increased incidence of cardiovascular events in patients with bronchial asthma, but little is known about the relationship between asthma and vascular function. The purpose of this study was to evaluate endothelial function and arterial stiffness in children and adolescents with asthma.

Methods

A cross-sectional controlled study was designed. Measurements of endothelial function and arterial stiffness in asthmatic (13.6 ± 0.6 years) and control groups (14.9 ± 0.7 years) were taken by the non-invasive peripheral arterial tonometry (EndoPAT2000) determined by using the natural logarithm of the reactive hyperemia index (LnRHI) and the augmentation index (AIx@75%), respectively. Patients with asthma were also administered two questionnaires to evaluate asthma control and quality of life. Exercise functional capacity was evaluated using the Shuttle Walking Test (SWT). Only male participants were included in the present study.

Results

LnRHI and the walked distance during the SWT were similar between groups (p = 0.23 and p = 0.50, respectively). AIx@75% was significantly higher in the asthmatic group (-7.75 ± 1.7) compared to the control group (-15.25 ± 1.8), p < 0.04. In the control group, the LnRHI correlated positively with baseline systolic blood pressure (r = 0.53, p = 0.02) and mean arterial pressure (r = 0.50, p = 0.03), age (r = 0.61, p = 0.007), weight (r = 0.63, p = 0.004) and height (r = 0.56, p = 0.015). Besides that LnRHI correlated with FVC (r = 0.69, p = 0.002), FEV1, (r = 0.53, p = 0.03) and negatively with Tiffeneau index (FEV1/FVC%, r = −0.49 p = 0.04). The LnRHI of the asthmatic group did not correlate with the different variables evaluated.

Conclusion

The increased AIx@75% without changes in LnRHI in asthmatic patients could mean that an early detection of vascular impairment may precede endothelial dysfunction, and that different mechanisms may contribute to the pathogenesis and progression of cardiovascular events in this population. A large prospective and randomized controlled study should be done to evaluate the physiopathological mechanisms underlying the association between arterial stiffness and asthma.
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Literature
1.
go back to reference FitzGerald JM, Bateman ED, Boulet LF, Cruz AA, Haahtela T, Levy ML, O’Byrne P, Paggiaro P, Pedersen SE, Soto-Quiroz M, et al. Global strategy for asthma management and prevention. 2015. FitzGerald JM, Bateman ED, Boulet LF, Cruz AA, Haahtela T, Levy ML, O’Byrne P, Paggiaro P, Pedersen SE, Soto-Quiroz M, et al. Global strategy for asthma management and prevention. 2015.
2.
go back to reference Wood LG, Baines KJ, Fu JJ, Scott HA, Gibson PG. The neutrophilic inflammatory phenotype is associated with systemic inflammation in asthma. Chest. 2012;142(1):86–93.CrossRefPubMed Wood LG, Baines KJ, Fu JJ, Scott HA, Gibson PG. The neutrophilic inflammatory phenotype is associated with systemic inflammation in asthma. Chest. 2012;142(1):86–93.CrossRefPubMed
3.
go back to reference Girdhar A, Kumar V, Singh A, Menon B, Vijayan VK. Systemic inflammation and its response to treatment in patients with asthma. Respir Care. 2011;56(6):800–5.CrossRefPubMed Girdhar A, Kumar V, Singh A, Menon B, Vijayan VK. Systemic inflammation and its response to treatment in patients with asthma. Respir Care. 2011;56(6):800–5.CrossRefPubMed
4.
go back to reference Iribarren C, Tolstykh IV, Miller MK, Sobel E, Eisner MD. Adult asthma and risk of coronary heart disease, cerebrovascular disease, and heart failure: a prospective study of 2 matched cohorts. Am J Epidemiol. 2012;176(11):1014–24.CrossRefPubMed Iribarren C, Tolstykh IV, Miller MK, Sobel E, Eisner MD. Adult asthma and risk of coronary heart disease, cerebrovascular disease, and heart failure: a prospective study of 2 matched cohorts. Am J Epidemiol. 2012;176(11):1014–24.CrossRefPubMed
5.
go back to reference Schroeder EB, Welch VL, Couper D, Nieto FJ, Liao DP, Rosamond WD, Heiss G. Lung function and incident coronary heart disease - The atherosclerosis risk in communities study. Am J Epidemiol. 2003;158(12):1171–81.CrossRefPubMed Schroeder EB, Welch VL, Couper D, Nieto FJ, Liao DP, Rosamond WD, Heiss G. Lung function and incident coronary heart disease - The atherosclerosis risk in communities study. Am J Epidemiol. 2003;158(12):1171–81.CrossRefPubMed
6.
go back to reference Schanen JG, Iribarren C, Shahar E, Punjabi NM, Rich SS, Sorlie PD, Folsom AR. Asthma and incident cardiovascular disease: the atherosclerosis risk in communities study. Thorax. 2005;60(8):633–8.CrossRefPubMedPubMedCentral Schanen JG, Iribarren C, Shahar E, Punjabi NM, Rich SS, Sorlie PD, Folsom AR. Asthma and incident cardiovascular disease: the atherosclerosis risk in communities study. Thorax. 2005;60(8):633–8.CrossRefPubMedPubMedCentral
7.
go back to reference Onufrak S, Abramson J, Vaccarino V. Adult-onset asthma is associated with increased carotid atherosclerosis among women in the atherosclerosis risk in communities (ARIC) study. Atherosclerosis. 2007;195(1):129–37.CrossRefPubMed Onufrak S, Abramson J, Vaccarino V. Adult-onset asthma is associated with increased carotid atherosclerosis among women in the atherosclerosis risk in communities (ARIC) study. Atherosclerosis. 2007;195(1):129–37.CrossRefPubMed
8.
go back to reference Nurnberger J, Keflioglu-Scheiber A, Saez AMO, Wenzel RR, Philipp T, Schafers RF. Augmentation index is associated with cardiovascular risk. J Hypertens. 2002;20(12):2407–14.CrossRefPubMed Nurnberger J, Keflioglu-Scheiber A, Saez AMO, Wenzel RR, Philipp T, Schafers RF. Augmentation index is associated with cardiovascular risk. J Hypertens. 2002;20(12):2407–14.CrossRefPubMed
9.
go back to reference Sun WX, Jin D, Li Y, Wang RT. Increased arterial stiffness in stable and severe asthma. Respir Med. 2014;108(1):57–62.CrossRefPubMed Sun WX, Jin D, Li Y, Wang RT. Increased arterial stiffness in stable and severe asthma. Respir Med. 2014;108(1):57–62.CrossRefPubMed
10.
go back to reference Weiler Z, Zeldin Y, Magen E, Zamir D, Kidon MI. Pulmonary function correlates with arterial stiffness in asthmatic patients. Respir Med. 2010;104(2):197–203.CrossRefPubMed Weiler Z, Zeldin Y, Magen E, Zamir D, Kidon MI. Pulmonary function correlates with arterial stiffness in asthmatic patients. Respir Med. 2010;104(2):197–203.CrossRefPubMed
11.
go back to reference Ayer JG, Belousova EG, Harmer JA, Toelle B, Celermajer DS, Marks GB. Lung function is associated with arterial stiffness in children. Plos One. 2011;6(10):e26303.CrossRefPubMedPubMedCentral Ayer JG, Belousova EG, Harmer JA, Toelle B, Celermajer DS, Marks GB. Lung function is associated with arterial stiffness in children. Plos One. 2011;6(10):e26303.CrossRefPubMedPubMedCentral
12.
go back to reference Libby P, Okamoto Y, Rocha VZ, Folco E. Inflammation in atherosclerosis: transition from theory to practice. Circ J. 2010;74(2):213–20.CrossRefPubMed Libby P, Okamoto Y, Rocha VZ, Folco E. Inflammation in atherosclerosis: transition from theory to practice. Circ J. 2010;74(2):213–20.CrossRefPubMed
13.
go back to reference Koska J, Schwartz EA, Mullin MP, Schwenke DC, Reaven PD. Improvement of postprandial endothelial function after a single dose of Exenatide in individuals with impaired glucose tolerance and recent-onset type 2 diabetes. Diabetes Care. 2010;33(5):1028–30.CrossRefPubMedPubMedCentral Koska J, Schwartz EA, Mullin MP, Schwenke DC, Reaven PD. Improvement of postprandial endothelial function after a single dose of Exenatide in individuals with impaired glucose tolerance and recent-onset type 2 diabetes. Diabetes Care. 2010;33(5):1028–30.CrossRefPubMedPubMedCentral
14.
go back to reference Kelly AS, Metzig AM, Steinberger J, Braunlin EA. Endothelial function in children and adolescents with mucopolysaccharidosis. J Inherit Metab Dis. 2013;36(2):221–5.CrossRefPubMed Kelly AS, Metzig AM, Steinberger J, Braunlin EA. Endothelial function in children and adolescents with mucopolysaccharidosis. J Inherit Metab Dis. 2013;36(2):221–5.CrossRefPubMed
15.
go back to reference Kuvin JT, Patel AR, Sliney KA, Pandian NG, Sheffy J, Schnall RP, Karas RH, Udelson JE. Assessment of peripheral vascular endothelial function with finger arterial pulse wave amplitude. Am Heart J. 2003;146(1):168–74.CrossRefPubMed Kuvin JT, Patel AR, Sliney KA, Pandian NG, Sheffy J, Schnall RP, Karas RH, Udelson JE. Assessment of peripheral vascular endothelial function with finger arterial pulse wave amplitude. Am Heart J. 2003;146(1):168–74.CrossRefPubMed
16.
go back to reference Ruan Y, Wei W, Yan J, Sun L, Lian H, Zhao X, Liang R, Xiaole L, Fan Z. Time rate of blood pressure variation is associated with endothelial function in patients with metabolic syndrome. Int Heart J. 2016;57(2):226–33.CrossRefPubMed Ruan Y, Wei W, Yan J, Sun L, Lian H, Zhao X, Liang R, Xiaole L, Fan Z. Time rate of blood pressure variation is associated with endothelial function in patients with metabolic syndrome. Int Heart J. 2016;57(2):226–33.CrossRefPubMed
17.
go back to reference Nohria A, Gerhard-Herman M, Creager MA, Hurley S, Mitra D, Ganz P. Role of nitric oxide in the regulation of digital pulse volume amplitude in humans. J Appl Physiol (1985). 2006;101(2):545–8.CrossRef Nohria A, Gerhard-Herman M, Creager MA, Hurley S, Mitra D, Ganz P. Role of nitric oxide in the regulation of digital pulse volume amplitude in humans. J Appl Physiol (1985). 2006;101(2):545–8.CrossRef
18.
go back to reference Hedetoft M, Olsen NV. Evaluation of endothelial function by peripheral arterial tonometry and relation with the nitric oxide pathway. Nitric Oxide. 2014;42:1–8.CrossRefPubMed Hedetoft M, Olsen NV. Evaluation of endothelial function by peripheral arterial tonometry and relation with the nitric oxide pathway. Nitric Oxide. 2014;42:1–8.CrossRefPubMed
19.
go back to reference Higashi Y. Assessment of endothelial function. History, methodological aspects, and clinical perspectives. Int Heart J. 2015;56(2):125–34.CrossRefPubMed Higashi Y. Assessment of endothelial function. History, methodological aspects, and clinical perspectives. Int Heart J. 2015;56(2):125–34.CrossRefPubMed
20.
go back to reference Jeroncic A, Gunjaca G, Mrsic DB, Mudnic I, Brizic I, Polasek O, Boban M. Normative equations for central augmentation index: assessment of inter-population applicability and how it could be improved. Sci Rep. 2016;6:27016.CrossRefPubMedPubMedCentral Jeroncic A, Gunjaca G, Mrsic DB, Mudnic I, Brizic I, Polasek O, Boban M. Normative equations for central augmentation index: assessment of inter-population applicability and how it could be improved. Sci Rep. 2016;6:27016.CrossRefPubMedPubMedCentral
21.
go back to reference Nelson MR, Stepanek J, Cevette M, Covalciuc M, Hurst RT, Tajik AJ. Noninvasive measurement of central vascular pressures with arterial tonometry: clinical revival of the pulse pressure waveform? Mayo Clin Proc. 2010;85(5):460–72.CrossRefPubMedPubMedCentral Nelson MR, Stepanek J, Cevette M, Covalciuc M, Hurst RT, Tajik AJ. Noninvasive measurement of central vascular pressures with arterial tonometry: clinical revival of the pulse pressure waveform? Mayo Clin Proc. 2010;85(5):460–72.CrossRefPubMedPubMedCentral
22.
go back to reference Selamet Tierney ES, Newburger JW, Gauvreau K, Geva J, Coogan E, Colan SD, de Ferranti SD. Endothelial pulse amplitude testing: feasibility and reproducibility in adolescents. J Pediatr. 2009;154(6):901–5.CrossRefPubMed Selamet Tierney ES, Newburger JW, Gauvreau K, Geva J, Coogan E, Colan SD, de Ferranti SD. Endothelial pulse amplitude testing: feasibility and reproducibility in adolescents. J Pediatr. 2009;154(6):901–5.CrossRefPubMed
23.
go back to reference Bruno RM, Gori T, Ghiadoni L. Endothelial function testing and cardiovascular disease: focus on peripheral arterial tonometry. Vasc Health Risk Manag. 2014;10:577–84.PubMedPubMedCentral Bruno RM, Gori T, Ghiadoni L. Endothelial function testing and cardiovascular disease: focus on peripheral arterial tonometry. Vasc Health Risk Manag. 2014;10:577–84.PubMedPubMedCentral
24.
go back to reference Juniper EF, O’Byrne PM, Guyatt GH, Ferrie PJ, King DR. Development and validation of a questionnaire to measure asthma control. Eur Respir J. 1999;14(4):902–7.CrossRefPubMed Juniper EF, O’Byrne PM, Guyatt GH, Ferrie PJ, King DR. Development and validation of a questionnaire to measure asthma control. Eur Respir J. 1999;14(4):902–7.CrossRefPubMed
25.
go back to reference Juniper EF. How important is quality of life in pediatric asthma? Pediatr Pulmonol Suppl. 1997;15:17–21.CrossRefPubMed Juniper EF. How important is quality of life in pediatric asthma? Pediatr Pulmonol Suppl. 1997;15:17–21.CrossRefPubMed
26.
go back to reference Roxo JPF, Ponte EV, Ramos DCB, Pimentel L, D’Oliveira Júnior A, Cruz AA. Portuguese-language version of the Asthma Control Test: validation for use in Brazil. J Bras Pneumol. 2010;36:159–66.CrossRefPubMed Roxo JPF, Ponte EV, Ramos DCB, Pimentel L, D’Oliveira Júnior A, Cruz AA. Portuguese-language version of the Asthma Control Test: validation for use in Brazil. J Bras Pneumol. 2010;36:159–66.CrossRefPubMed
27.
go back to reference La Scala CSK, Naspitz CK, Solé D. Adaptation and validation of the Pediatric Asthma Quality of Life Questionnaire (PAQLQ) in Brazilian asthmatic children and adolescents. J Pediatr. 2005;81:54–60.CrossRef La Scala CSK, Naspitz CK, Solé D. Adaptation and validation of the Pediatric Asthma Quality of Life Questionnaire (PAQLQ) in Brazilian asthmatic children and adolescents. J Pediatr. 2005;81:54–60.CrossRef
28.
go back to reference Singh SJ, Morgan MDL, Scott S, Walters D, Hardman AE. Development of a shuttle walking test of disability in patients with chronic airways obstruction. Thorax. 1992;47(12):1019–24.CrossRefPubMedPubMedCentral Singh SJ, Morgan MDL, Scott S, Walters D, Hardman AE. Development of a shuttle walking test of disability in patients with chronic airways obstruction. Thorax. 1992;47(12):1019–24.CrossRefPubMedPubMedCentral
29.
go back to reference GINA. Global strategy for asthma management and prevention. 2015. GINA. Global strategy for asthma management and prevention. 2015.
30.
go back to reference Hadi HA, Carr CS, Al Suwaidi J. Endothelial dysfunction: cardiovascular risk factors, therapy, and outcome. Vasc Health Risk Manag. 2005;1(3):183–98.PubMedPubMedCentral Hadi HA, Carr CS, Al Suwaidi J. Endothelial dysfunction: cardiovascular risk factors, therapy, and outcome. Vasc Health Risk Manag. 2005;1(3):183–98.PubMedPubMedCentral
31.
go back to reference Tousoulis D, Charakida M, Stefanadis C. Endothelial function and inflammation in coronary artery disease. Heart. 2006;92(4):441–4.PubMed Tousoulis D, Charakida M, Stefanadis C. Endothelial function and inflammation in coronary artery disease. Heart. 2006;92(4):441–4.PubMed
32.
go back to reference Tattersall MC, Guo M, Korcarz CE, Gepner AD, Kaufman JD, Liu KJ, Barr RG, Donohue KM, McClelland RL, Delaney JA, et al. Asthma predicts cardiovascular disease events: the multi-ethnic study of atherosclerosis. Arterioscler Thromb Vasc Biol. 2015;35(6):1520–5.CrossRefPubMedPubMedCentral Tattersall MC, Guo M, Korcarz CE, Gepner AD, Kaufman JD, Liu KJ, Barr RG, Donohue KM, McClelland RL, Delaney JA, et al. Asthma predicts cardiovascular disease events: the multi-ethnic study of atherosclerosis. Arterioscler Thromb Vasc Biol. 2015;35(6):1520–5.CrossRefPubMedPubMedCentral
33.
go back to reference Chen Y, Dangardt F, Osika W, Berggren K, Gronowitz E, Friberg P. 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. 2012;220(1):269–74.CrossRefPubMed Chen Y, Dangardt F, Osika W, Berggren K, Gronowitz E, Friberg P. 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. 2012;220(1):269–74.CrossRefPubMed
34.
go back to reference Pareyn A, Allegaert K, Verhamme P, Vinckx J, Casteels K. Impaired endothelial function in adolescents with overweight or obesity measured by peripheral artery tonometry. Pediatr Diabetes. 2015;16(2):98–103.CrossRefPubMed Pareyn A, Allegaert K, Verhamme P, Vinckx J, Casteels K. Impaired endothelial function in adolescents with overweight or obesity measured by peripheral artery tonometry. Pediatr Diabetes. 2015;16(2):98–103.CrossRefPubMed
35.
go back to reference Moore LE, Bhutani M, Petersen SR, McMurtry MS, Byers BW, Tedjasaputra V, Stickland MK. Physical activity, fitness, and vascular health in patients with asthma. J Allergy Clin Immunol. 2015;136(3):809–11.CrossRefPubMed Moore LE, Bhutani M, Petersen SR, McMurtry MS, Byers BW, Tedjasaputra V, Stickland MK. Physical activity, fitness, and vascular health in patients with asthma. J Allergy Clin Immunol. 2015;136(3):809–11.CrossRefPubMed
36.
go back to reference Arrebola-Moreno AL, Laclaustra M, Kaski JC. Noninvasive assessment of endothelial function in clinical practice. Rev Esp Cardiol (Engl Ed). 2012;65(1):80–90.CrossRef Arrebola-Moreno AL, Laclaustra M, Kaski JC. Noninvasive assessment of endothelial function in clinical practice. Rev Esp Cardiol (Engl Ed). 2012;65(1):80–90.CrossRef
37.
go back to reference Harkness LM, Ashton AW, Burgess JK. Asthma is not only an airway disease, but also a vascular disease. Pharmacol Ther. 2015;148:17–33.CrossRefPubMed Harkness LM, Ashton AW, Burgess JK. Asthma is not only an airway disease, but also a vascular disease. Pharmacol Ther. 2015;148:17–33.CrossRefPubMed
38.
go back to reference Rodrigues-Machado MG, Magalhaes GS, Cardoso JA, Kangussu LM, Murari A, Caliari MV, Oliveira ML, Cara DC, Noviello ML, Marques FD, et al. AVE 0991, a non-peptide mimic of angiotensin-(1-7) effects, attenuates pulmonary remodelling in a model of chronic asthma. Br J Pharmacol. 2013;170(4):835–46.CrossRefPubMedPubMedCentral Rodrigues-Machado MG, Magalhaes GS, Cardoso JA, Kangussu LM, Murari A, Caliari MV, Oliveira ML, Cara DC, Noviello ML, Marques FD, et al. AVE 0991, a non-peptide mimic of angiotensin-(1-7) effects, attenuates pulmonary remodelling in a model of chronic asthma. Br J Pharmacol. 2013;170(4):835–46.CrossRefPubMedPubMedCentral
39.
go back to reference Magalhaes GS, Rodrigues-Machado MG, Motta-Santos D, Silva AR, Caliari MV, Prata LO, Abreu SC, Rocco PR, Barcelos LS, Santos RA, et al. Angiotensin-(1-7) attenuates airway remodelling and hyperresponsiveness in a model of chronic allergic lung inflammation. Br J Pharmacol. 2015;172(9):2330–42.CrossRefPubMedPubMedCentral Magalhaes GS, Rodrigues-Machado MG, Motta-Santos D, Silva AR, Caliari MV, Prata LO, Abreu SC, Rocco PR, Barcelos LS, Santos RA, et al. Angiotensin-(1-7) attenuates airway remodelling and hyperresponsiveness in a model of chronic allergic lung inflammation. Br J Pharmacol. 2015;172(9):2330–42.CrossRefPubMedPubMedCentral
40.
go back to reference Charakida M, Masi S, Loukogeorgakis SP, Deanfield JE. The role of flow-mediated dilatation in the evaluation and development of antiatherosclerotic drugs. Curr Opin Lipidol. 2009;20(6):460–6.CrossRefPubMed Charakida M, Masi S, Loukogeorgakis SP, Deanfield JE. The role of flow-mediated dilatation in the evaluation and development of antiatherosclerotic drugs. Curr Opin Lipidol. 2009;20(6):460–6.CrossRefPubMed
41.
go back to reference Bhangoo A, Sinha S, Rosenbaum M, Shelov S, Ten S. Endothelial function as measured by peripheral arterial tonometry increases during pubertal advancement. Hormone Res Paediatrics. 2011;76(4):226–33.CrossRef Bhangoo A, Sinha S, Rosenbaum M, Shelov S, Ten S. Endothelial function as measured by peripheral arterial tonometry increases during pubertal advancement. Hormone Res Paediatrics. 2011;76(4):226–33.CrossRef
42.
go back to reference Morris AA, Patel RS, Binongo JNG, Poole J, al Mheid I, Ahmed Y, Stoyanova N, Vaccarino V, Din-Dzietham R, Gibbons GH, et al. Racial differences in arterial stiffness and microcirculatory function between black and white Americans. J Am Heart Assoc. 2013;2(2):e002154.CrossRefPubMedPubMedCentral Morris AA, Patel RS, Binongo JNG, Poole J, al Mheid I, Ahmed Y, Stoyanova N, Vaccarino V, Din-Dzietham R, Gibbons GH, et al. Racial differences in arterial stiffness and microcirculatory function between black and white Americans. J Am Heart Assoc. 2013;2(2):e002154.CrossRefPubMedPubMedCentral
Metadata
Title
Vascular function in asthmatic children and adolescents
Publication date
01-12-2017
Published in
Respiratory Research / Issue 1/2017
Electronic ISSN: 1465-993X
DOI
https://doi.org/10.1186/s12931-016-0488-3

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