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Published in: Pediatric Cardiology 7/2015

01-10-2015 | Original Article

Ascending Aorta Elastography After Kawasaki Disease Compared to Systemic Hypertension

Authors: Ian Nandlall, Roch L. Maurice, Anne Fournier, Aïcha Merouani, Nagib Dahdah

Published in: Pediatric Cardiology | Issue 7/2015

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Abstract

Kawasaki disease (KD) is a systemic vasculitis, classically affecting large- and medium-size arteries. The coronary arteries draw most of the clinical attention, whereas few studies have taken interest in the ascending aorta. Using a proprietary imaging-based mechanical biomarker (ImBioMark), we sought to determine aortic stiffness in KD compared to systemic hypertension (HTN) and healthy children. We evaluated parasternal long-axis views focused on the ascending aorta in 20 controls, 12 KD, and 8 HTN as a comparative clinical model of vascular stiffness. We calculated systolic and diastolic aortic wall strain with ImBioMark. Strain was tested for normality against height, systolic, and diastolic blood pressure in normal subjects. Strain from KD and HTN was normalized (Z score) accordingly. Z score comparisons were performed using nonparametric statistics. Age was similar between KD and HTN (9.1 ± 5.3 and 9.9 ± 5.3 years old; p = NS). Systolic and diastolic strain values were normally distributed against height, systolic blood pressure, and diastolic blood pressure in healthy subjects. HTN subjects had abnormal systolic and diastolic strain values (p < 0.0001). Whereas KD subjects had normal diastolic strain, systolic strain was significantly lower (p < 0.001), and systolic strain was intermediate between controls and HTN. There were no significant differences in aortic strain among KD, however, according to the presence of coronary artery aneurysms. Despite normal blood pressure, the ascending aorta in KD exhibits reduced strain during systole. This may reflect in situ rigidity of the aorta. The normal diastolic strain in KD may, in contrast, reflect normal peripheral vascular resistance.
Literature
1.
go back to reference Amano S, Hazama F, Kubagawa H, Tasaka K, Haebara H, Hamashima Y (1980) General pathology of Kawasaki disease: on the morphological alterations corresponding to the clinical manifestations. Acta Pathol Jpn 30:681–694PubMed Amano S, Hazama F, Kubagawa H, Tasaka K, Haebara H, Hamashima Y (1980) General pathology of Kawasaki disease: on the morphological alterations corresponding to the clinical manifestations. Acta Pathol Jpn 30:681–694PubMed
2.
go back to reference Ayer JG, Harmer JA, Marks GB, Avolio A, Celermajer DS (2010) Central arterial pulse wave augmentation is greater in girls than boys, independent of height. J Hypertens 28:306–313CrossRefPubMed Ayer JG, Harmer JA, Marks GB, Avolio A, Celermajer DS (2010) Central arterial pulse wave augmentation is greater in girls than boys, independent of height. J Hypertens 28:306–313CrossRefPubMed
3.
go back to reference Canter CE, Bower RJ, Strauss AW (1981) Atypical Kawasaki disease with aortic aneurysm. Pediatrics 68:885–888PubMed Canter CE, Bower RJ, Strauss AW (1981) Atypical Kawasaki disease with aortic aneurysm. Pediatrics 68:885–888PubMed
4.
go back to reference Cheung YF, Wong SJ, Ho MH (2007) Relationship between carotid intima-media thickness and arterial stiffness in children after Kawasaki disease. Arch Dis Child 92:43–47PubMedCentralCrossRefPubMed Cheung YF, Wong SJ, Ho MH (2007) Relationship between carotid intima-media thickness and arterial stiffness in children after Kawasaki disease. Arch Dis Child 92:43–47PubMedCentralCrossRefPubMed
5.
go back to reference Gaddum NR, Keehn L, Guilcher A, Gomez A, Brett S, Beerbaum P, Schaeffter T, Chowienczyk P (2015) Altered dependence of aortic pulse wave velocity on transmural pressure in hypertension revealing structural change in the aortic wall. Hypertension 65:362–369CrossRefPubMed Gaddum NR, Keehn L, Guilcher A, Gomez A, Brett S, Beerbaum P, Schaeffter T, Chowienczyk P (2015) Altered dependence of aortic pulse wave velocity on transmural pressure in hypertension revealing structural change in the aortic wall. Hypertension 65:362–369CrossRefPubMed
6.
go back to reference Horn BKP (1986) Robot vision. McGraw-Hill, New York, pp 278–298 Horn BKP (1986) Robot vision. McGraw-Hill, New York, pp 278–298
7.
go back to reference Ikeda K, Ihara K, Yamaguchi K, Muneuchi J, Ohno T, Mizuno Y, Hara T (2008) Genetic analysis of MMP gene polymorphisms in patients with Kawasaki disease. Pediatr Res 63:182–185CrossRefPubMed Ikeda K, Ihara K, Yamaguchi K, Muneuchi J, Ohno T, Mizuno Y, Hara T (2008) Genetic analysis of MMP gene polymorphisms in patients with Kawasaki disease. Pediatr Res 63:182–185CrossRefPubMed
8.
go back to reference Lapierre C, Bitsch A, Guérin R, Garel L, Miró J, Dahdah N (2010) Follow-up chest X-Ray in patients with Kawasaki disease: the significance and clinical application of coronary artery macro-calcification. Pediatr Cardiol 31:56–61CrossRefPubMed Lapierre C, Bitsch A, Guérin R, Garel L, Miró J, Dahdah N (2010) Follow-up chest X-Ray in patients with Kawasaki disease: the significance and clinical application of coronary artery macro-calcification. Pediatr Cardiol 31:56–61CrossRefPubMed
9.
go back to reference Lau AC, Duong TT, Ito S, Yeung RS (2008) Matrix metalloproteinase 9 activity leads to elastin breakdown in an animal model of Kawasaki disease. Arthritis Rheum 58:854–863CrossRefPubMed Lau AC, Duong TT, Ito S, Yeung RS (2008) Matrix metalloproteinase 9 activity leads to elastin breakdown in an animal model of Kawasaki disease. Arthritis Rheum 58:854–863CrossRefPubMed
10.
go back to reference Laurent S, Boutouyrie P, Asmar R, Gautier I, Laloux B, Guize L, Ducimetiere P, Benetos A (2001) Aortic stiffness is an independent predictor of all-cause and cardiovascular mortality in hypertensive patients. Hypertension 37:1236–1241CrossRefPubMed Laurent S, Boutouyrie P, Asmar R, Gautier I, Laloux B, Guize L, Ducimetiere P, Benetos A (2001) Aortic stiffness is an independent predictor of all-cause and cardiovascular mortality in hypertensive patients. Hypertension 37:1236–1241CrossRefPubMed
11.
go back to reference Lee SJ, Ahn HM, You JH, Hong YM (2009) Carotid intima-media thickness and pulse wave velocity after recovery from Kawasaki disease. Korean Circ J 39:264–269PubMedCentralCrossRefPubMed Lee SJ, Ahn HM, You JH, Hong YM (2009) Carotid intima-media thickness and pulse wave velocity after recovery from Kawasaki disease. Korean Circ J 39:264–269PubMedCentralCrossRefPubMed
12.
go back to reference Lin YT, Manlhiot C, Ching JC, Han RK, Nield LE, Dillenburg R, Pepelassis D, Lai LS, Smythe JF, Chahal N, Yeung RS, McCrindle BW (2010) Repeated systematic surveillance of Kawasaki disease in Ontario from 1995 to 2006. Pediatr Int 52:699–706CrossRefPubMed Lin YT, Manlhiot C, Ching JC, Han RK, Nield LE, Dillenburg R, Pepelassis D, Lai LS, Smythe JF, Chahal N, Yeung RS, McCrindle BW (2010) Repeated systematic surveillance of Kawasaki disease in Ontario from 1995 to 2006. Pediatr Int 52:699–706CrossRefPubMed
13.
go back to reference Margossian R, Lu M, Minich LL, Bradley TJ, Cohen MS, Li JS, Printz BF, Shirali GS, Sleeper LA, Newburger JW, Colan SD (2011) Pediatric Heart Network Investigators. Predictors of coronary artery visualization in Kawasaki disease. J Am Soc Echocardiogr 24:53–59PubMedCentralCrossRefPubMed Margossian R, Lu M, Minich LL, Bradley TJ, Cohen MS, Li JS, Printz BF, Shirali GS, Sleeper LA, Newburger JW, Colan SD (2011) Pediatric Heart Network Investigators. Predictors of coronary artery visualization in Kawasaki disease. J Am Soc Echocardiogr 24:53–59PubMedCentralCrossRefPubMed
14.
go back to reference Maurice RL, Dahdah N (2012) Characterization of aortic remodeling following Kawasaki disease: toward a fully-developed automatic bi-parametric model. Med Phys 30:6104–6110CrossRef Maurice RL, Dahdah N (2012) Characterization of aortic remodeling following Kawasaki disease: toward a fully-developed automatic bi-parametric model. Med Phys 30:6104–6110CrossRef
15.
go back to reference Maurice RL, Ohayon J, Frétigny Y, Bertrand M, Soulez G, Cloutier G (2004) Non-invasive vascular elastography: theoretical Framework. IEEE Trans Med Imaging 23:164–180CrossRefPubMed Maurice RL, Ohayon J, Frétigny Y, Bertrand M, Soulez G, Cloutier G (2004) Non-invasive vascular elastography: theoretical Framework. IEEE Trans Med Imaging 23:164–180CrossRefPubMed
16.
go back to reference Maurice RL, Soulez G, Giroux M-F, Cloutier G (2008) Non-invasive vascular elastography for carotid artery characterization on subjects without previous history of atherosclerosis. Med Phys 35:3436–3443CrossRefPubMed Maurice RL, Soulez G, Giroux M-F, Cloutier G (2008) Non-invasive vascular elastography for carotid artery characterization on subjects without previous history of atherosclerosis. Med Phys 35:3436–3443CrossRefPubMed
17.
go back to reference Maurice RL, Dahdah N, Tremblay J (2012) Imaging-based biomarkers: characterization of post-Kawasaki vasculitis in infants and hypertension phenotype in rat model. Int J Vasc Med 2012:364145PubMedCentralPubMed Maurice RL, Dahdah N, Tremblay J (2012) Imaging-based biomarkers: characterization of post-Kawasaki vasculitis in infants and hypertension phenotype in rat model. Int J Vasc Med 2012:364145PubMedCentralPubMed
18.
go back to reference McCrindle BW, McIntyre S, Kim C, Lin T, Adeli K (2007) Are patients after Kawasaki disease at increased risk for accelerated atherosclerosis? J Pediatr 151:244–248CrossRefPubMed McCrindle BW, McIntyre S, Kim C, Lin T, Adeli K (2007) Are patients after Kawasaki disease at increased risk for accelerated atherosclerosis? J Pediatr 151:244–248CrossRefPubMed
19.
go back to reference McEniery CM, Yasmin B, Hall IR, Qasem A, Wilkinson IB, Cockcroft JR, ACCT Investigators (2005) Normal vascular aging: differential effects on wave reflection and aortic pulse wave velocity: the Anglo-Cardiff Collaborative Trial (ACCT). J Am Coll Cardiol 46:1753–1760CrossRefPubMed McEniery CM, Yasmin B, Hall IR, Qasem A, Wilkinson IB, Cockcroft JR, ACCT Investigators (2005) Normal vascular aging: differential effects on wave reflection and aortic pulse wave velocity: the Anglo-Cardiff Collaborative Trial (ACCT). J Am Coll Cardiol 46:1753–1760CrossRefPubMed
20.
go back to reference Nakagawa R, Kuwata S, Kurishima C, Saiki H, Iwamoto Y, Sugimoto M, Ishido H, Masutani S, Senzaki H (2014) Arterial stiffness in patients after Kawasaki disease without coronary artery involvement Assessment by performing brachial ankle pulse wave velocity and cardio-ankle vascular index. J Cardiol. doi:10.1016/j.jjcc.2014.10.003 Nakagawa R, Kuwata S, Kurishima C, Saiki H, Iwamoto Y, Sugimoto M, Ishido H, Masutani S, Senzaki H (2014) Arterial stiffness in patients after Kawasaki disease without coronary artery involvement Assessment by performing brachial ankle pulse wave velocity and cardio-ankle vascular index. J Cardiol. doi:10.​1016/​j.​jjcc.​2014.​10.​003
21.
go back to reference Nakamura Y, Yashiro M, Uehara R, Sadakane A, Tsuboi S, Aoyama Y, Kotani K, Tsogzolbaatar EO, Yanagawa H (2012) Epidemiologic features of Kawasaki disease in Japan: results of the 2009–2010 nationwide survey. J Epidemiol 22:216–221PubMedCentralCrossRefPubMed Nakamura Y, Yashiro M, Uehara R, Sadakane A, Tsuboi S, Aoyama Y, Kotani K, Tsogzolbaatar EO, Yanagawa H (2012) Epidemiologic features of Kawasaki disease in Japan: results of the 2009–2010 nationwide survey. J Epidemiol 22:216–221PubMedCentralCrossRefPubMed
22.
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
23.
go back to reference Newburger JW, Takahashi M, Gerber MA, Gewitz MH, Tani LY, Burns JC, Shulman ST, Bolger AF, Ferrieri P, Baltimore RS, Wilson WR, Baddour LM, Levison ME, Pallasch TJ, Falace DA, Taubert KA (2004) Committee on Rheumatic Fever, Endocarditis and Kawasaki Disease; Council on Cardiovascular Disease in the Young; American Heart Association; American Academy of Pediatrics : a statement for health professionals from the Committee on Rheumatic Fever, Endocarditis and Kawasaki Disease, Council on Cardiovascular Disease in the Young, American Heart Association. Diagnosis, treatment, and long-term management of Kawasaki disease. Circulation 110:2747–2771CrossRefPubMed Newburger JW, Takahashi M, Gerber MA, Gewitz MH, Tani LY, Burns JC, Shulman ST, Bolger AF, Ferrieri P, Baltimore RS, Wilson WR, Baddour LM, Levison ME, Pallasch TJ, Falace DA, Taubert KA (2004) Committee on Rheumatic Fever, Endocarditis and Kawasaki Disease; Council on Cardiovascular Disease in the Young; American Heart Association; American Academy of Pediatrics : a statement for health professionals from the Committee on Rheumatic Fever, Endocarditis and Kawasaki Disease, Council on Cardiovascular Disease in the Young, American Heart Association. Diagnosis, treatment, and long-term management of Kawasaki disease. Circulation 110:2747–2771CrossRefPubMed
24.
go back to reference Okubo M, Ino T, Takahashi K, Kishiro M, Akimoto K, Yamashiro Y (2001) Age dependency of stiffness of the abdominal aorta and the mechanical properties of the aorta in Kawasaki disease in children. Pediatr Cardiol 22:198–203CrossRefPubMed Okubo M, Ino T, Takahashi K, Kishiro M, Akimoto K, Yamashiro Y (2001) Age dependency of stiffness of the abdominal aorta and the mechanical properties of the aorta in Kawasaki disease in children. Pediatr Cardiol 22:198–203CrossRefPubMed
25.
go back to reference Orenstein JM, Shulman ST, Fox LM, Baker SC, Takahashi M, Bhatti TR, Russo PA, Mierau GW, de Chadarévian JP, Perlman EJ, Trevenen C, Rotta AT, Kalelkar MB, Rowley AH (2012) Three linked vasculopathic processes characterize Kawasaki disease: a light and transmission electron microscopic study. PLoS ONE 7:e38998PubMedCentralCrossRefPubMed Orenstein JM, Shulman ST, Fox LM, Baker SC, Takahashi M, Bhatti TR, Russo PA, Mierau GW, de Chadarévian JP, Perlman EJ, Trevenen C, Rotta AT, Kalelkar MB, Rowley AH (2012) Three linked vasculopathic processes characterize Kawasaki disease: a light and transmission electron microscopic study. PLoS ONE 7:e38998PubMedCentralCrossRefPubMed
26.
go back to reference Ravekes WJ, Colan SD, Gauvreau K, Baker AL, Sundel RP, van der Velde ME, Fulton DR, Newburger JW (2001) Aortic root dilation in Kawasaki disease. Am J Cardiol 87:919–922CrossRefPubMed Ravekes WJ, Colan SD, Gauvreau K, Baker AL, Sundel RP, van der Velde ME, Fulton DR, Newburger JW (2001) Aortic root dilation in Kawasaki disease. Am J Cardiol 87:919–922CrossRefPubMed
27.
go back to reference Satou GM, Giamelli J, Gewitz MH (2007) Kawasaki disease: diagnosis, management, and long-term implications. Cardiol Rev 15:163–169CrossRefPubMed Satou GM, Giamelli J, Gewitz MH (2007) Kawasaki disease: diagnosis, management, and long-term implications. Cardiol Rev 15:163–169CrossRefPubMed
28.
go back to reference Schimizu C, Jain S, Davila S, Hibberd ML, Lin KO, Molkara D, Frazer JR, Sun S, Baker AL, Newburger JW, Rowley AH, Shulman ST, Burgner D, Breunis WB, Kuijpers TW, Wright VJ, Levin M, Eleftherohorinou H, Coin L, Popper SJ, Relman DA, Fury W, Lin C, Mellis S, Tremoulet AH, Burns JC (2011) Transforming growth factor-beta signaling pathway in patients with Kawasaki disease. Circ Cardiovasc Genet 4:16–25CrossRef Schimizu C, Jain S, Davila S, Hibberd ML, Lin KO, Molkara D, Frazer JR, Sun S, Baker AL, Newburger JW, Rowley AH, Shulman ST, Burgner D, Breunis WB, Kuijpers TW, Wright VJ, Levin M, Eleftherohorinou H, Coin L, Popper SJ, Relman DA, Fury W, Lin C, Mellis S, Tremoulet AH, Burns JC (2011) Transforming growth factor-beta signaling pathway in patients with Kawasaki disease. Circ Cardiovasc Genet 4:16–25CrossRef
29.
go back to reference Selamet Tierney ES, Gal D, Gauvreau K, Baker AL, Trevey S, O’Neill SR, Jaff MR, de Ferranti S, Fulton DR, Colan SD, Newburger JW (2013) Vascular health in Kawasaki disease. J Am Coll Cardiol 62:1114–1121CrossRefPubMed Selamet Tierney ES, Gal D, Gauvreau K, Baker AL, Trevey S, O’Neill SR, Jaff MR, de Ferranti S, Fulton DR, Colan SD, Newburger JW (2013) Vascular health in Kawasaki disease. J Am Coll Cardiol 62:1114–1121CrossRefPubMed
30.
go back to reference Sengupta D, Kahn AM, Burns JC, Sankaran S, Shadden SC, Marsden AL (2012) Image-based modeling of hemodynamics in coronary artery aneurysms caused by Kawasaki disease. Biomech Model Mechanobiol 11:915–932CrossRefPubMed Sengupta D, Kahn AM, Burns JC, Sankaran S, Shadden SC, Marsden AL (2012) Image-based modeling of hemodynamics in coronary artery aneurysms caused by Kawasaki disease. Biomech Model Mechanobiol 11:915–932CrossRefPubMed
31.
go back to reference Tobayama H, Takahashi K, Fukunaga H, Matsui K, Tanaka N, Harada M, Furukawa T, Oda H, Akimoto K, Kishiro M, Shimizu T (2013) Analysis of arterial function in adults with a history of Kawasaki disease. J Cardiol 61:330–335CrossRefPubMed Tobayama H, Takahashi K, Fukunaga H, Matsui K, Tanaka N, Harada M, Furukawa T, Oda H, Akimoto K, Kishiro M, Shimizu T (2013) Analysis of arterial function in adults with a history of Kawasaki disease. J Cardiol 61:330–335CrossRefPubMed
32.
go back to reference Vaujois L, Dallaire F, Maurice RL, Fournier A, Houde C, Thérien J, Cartwright D, Dahdah N (2013) The biophysical properties of the aorta are altered following Kawasaki disease with severe coronary artery lesions. J Am Soc Echocardiogr 26:1388–1396CrossRefPubMed Vaujois L, Dallaire F, Maurice RL, Fournier A, Houde C, Thérien J, Cartwright D, Dahdah N (2013) The biophysical properties of the aorta are altered following Kawasaki disease with severe coronary artery lesions. J Am Soc Echocardiogr 26:1388–1396CrossRefPubMed
34.
go back to reference Wang M, Zhang J, Telljohann R, Jiang L, Wu J, Monticone RE, Kapoor K, Talan M, Lakatta EG (2012) Chronic matrix metalloproteinase inhibition retards age-associated arterial proinflammation and increase in blood pressure. Hypertension 60:459–466PubMedCentralCrossRefPubMed Wang M, Zhang J, Telljohann R, Jiang L, Wu J, Monticone RE, Kapoor K, Talan M, Lakatta EG (2012) Chronic matrix metalloproteinase inhibition retards age-associated arterial proinflammation and increase in blood pressure. Hypertension 60:459–466PubMedCentralCrossRefPubMed
35.
go back to reference Zakaria T, Qin Z, Maurice RL (2010) Optical-flow-based B-Mode elastography: application in the hypertensive rat carotid. IEEE Trans Med Imaging 29:570–577CrossRefPubMed Zakaria T, Qin Z, Maurice RL (2010) Optical-flow-based B-Mode elastography: application in the hypertensive rat carotid. IEEE Trans Med Imaging 29:570–577CrossRefPubMed
Metadata
Title
Ascending Aorta Elastography After Kawasaki Disease Compared to Systemic Hypertension
Authors
Ian Nandlall
Roch L. Maurice
Anne Fournier
Aïcha Merouani
Nagib Dahdah
Publication date
01-10-2015
Publisher
Springer US
Published in
Pediatric Cardiology / Issue 7/2015
Print ISSN: 0172-0643
Electronic ISSN: 1432-1971
DOI
https://doi.org/10.1007/s00246-015-1175-8

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