Hostname: page-component-76fb5796d-x4r87 Total loading time: 0 Render date: 2024-04-27T02:38:07.230Z Has data issue: false hasContentIssue false

Long-term evaluation of endothelial function in Kawasaki disease patients

Published online by Cambridge University Press:  08 October 2012

Fátima F. Pinto*
Affiliation:
Serviço de Cardiologia Pediátrica, Hospital de Santa Marta, Centro Hospitalar de Lisboa Central, EPE, Lisboa, Portugal
Sérgio Laranjo
Affiliation:
Serviço de Cardiologia Pediátrica, Hospital de Santa Marta, Centro Hospitalar de Lisboa Central, EPE, Lisboa, Portugal
Filipa Paramés
Affiliation:
Serviço de Cardiologia Pediátrica, Hospital de Santa Marta, Centro Hospitalar de Lisboa Central, EPE, Lisboa, Portugal
Isabel Freitas
Affiliation:
Serviço de Cardiologia Pediátrica, Hospital de Santa Marta, Centro Hospitalar de Lisboa Central, EPE, Lisboa, Portugal
Miguel Mota-Carmo
Affiliation:
Serviço de Cardiologia, Hospital de Santa Marta, Centro Hospitalar de Lisboa Central, EPE, Lisboa, Portugal
*
Correspondence to: Fátima F. Pinto, MD, Serviço de Cardiologia Pediátrica, Hospital de Santa Marta, Centro Hospitalar de Lisboa Central, EPE, Rua de Santa Marta, 1169-024 Lisboa, Portugal. Tel: +213594332; Fax: +213594034; E-mail: Fatima.Pinto@hsmarta.min-saude.pt

Abstract

Background

Kawasaki disease is an acute systemic vasculitis. Cardiac complications are frequent and include endothelial dysfunction in patients with coronary anomalies. So far, the presence of endothelial dysfunction in patients with no coronary lesions has not been demonstrated. Peripheral arterial tonometry (Endo-PAT) measures the microvascular function in response to local ischaemia and has been validated in adult population, but its use in children is scarce.

Aim

To evaluate endothelial dysfunction in children as a long-term complication after Kawasaki disease using Endo-PAT.

Methods

We evaluated two groups of subjects: (1) Kawasaki disease patients over 11 years of age, diagnosed for >5 years, with no coronary lesions, or any other risk factors for cardiovascular disease; (2) control group of individuals without cardiovascular risk factors. Patients and controls were clinically accessed. Endo-PAT was performed to determine reactive hyperaemia index and augmentation index.

Results

A total of 35 individuals (21 males, age 21 ± 6 years) were evaluated (group 1: 19; controls: 16). Kawasaki disease patients presented significant lower reactive hyperaemia index (1.68 ± 0.49 versus 2.31 ± 0.53; p = 0.001). Augmentation index was similar in both groups (−10 ± 7 versus −11 ± 5; p > 0.005). Most patients with Kawasaki disease disclosed endothelial dysfunction (68%) compared with only 12% in controls.

Conclusions

Endo-PAT is feasible and reproducible in the child population. Endothelial dysfunction is a frequent long-term complication in patients after Kawasaki disease with normal appearing coronary arteries. However, these results need validation in a larger population.

Type
Original Articles
Copyright
Copyright © Cambridge University Press 2012 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

1. Taubert, KA, Rowley, AH, Shulman, ST. Nationwide survey of Kawasaki disease and acute reactive hyperaemia rheumatic fever. J Pediatr 1991; 119: 279282.CrossRefGoogle Scholar
2. Newburger, JW, Takahashi, M, Gerber, MA, et al. Diagnosis, treatment, and long-term management of Kawasaki disease: 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. Circulation 2004; 110: 27472771.CrossRefGoogle Scholar
3. Kawasaki, T, Kosaki, F, Okawa, S, Shigematsu, I, Yanagawa, H. A new infantile acute febrile mucocutaneous lymph node syndrome (MLNS) prevailing in Japan. Pediatrics 1974; 54: 271276.CrossRefGoogle ScholarPubMed
4. Iemura, M, Ishii, M, Sugimura, T, Akagi, T, Kato, H. Long term consequences of regressed coronary aneurysms after Kawasaki disease: vascular wall morphology and function. Heart 2000; 83: 307311.CrossRefGoogle ScholarPubMed
5. Noto, N, Okada, T, Yamasuge, M, et al. Noninvasive assessment of the early progression of atherosclerosis in adolescents with Kawasaki disease and coronary artery lesions. Pediatrics 2001; 107: 10951099.CrossRefGoogle ScholarPubMed
6. Cheung, YF, Wong, SJ, Ho, MH. Relationship between carotid intima-media thickness and arterial stiffness in children after Kawasaki disease. Arch Dis Child 2007; 92: 4347.CrossRefGoogle ScholarPubMed
7. Cheung, YF, Yung, TC, Tam, SC, Ho, MH, Chau, AK. Novel and traditional cardiovascular risk factors in children after Kawasaki disease: implications for premature atherosclerosis. J Am Coll Cardiol 2004; 43: 120124.CrossRefGoogle ScholarPubMed
8. Amano, S, Hazama, F, Hamashima, Y. Pathology of Kawasaki disease: II. Distribution and incidence of the vascular lesions. Jpn Circ J 1979; 43: 741748.CrossRefGoogle ScholarPubMed
9. Singh, S, Bansal, A, Gupta, A, Kumar, RM, Mittal, BR. Kawasaki disease: a decade of experience from North India. Int Heart J 2005; 46: 679689.CrossRefGoogle ScholarPubMed
10. Suzuki, A, Yamagishi, M, Kimura, K, et al. Functional behaviour and morphology of the coronary artery wall in patients with Kawasaki disease assessed by intravascular ultrasound. J Am Coll Cardiol 1996; 27: 291296.CrossRefGoogle ScholarPubMed
11. Sugimura, T, Kato, H, Inoue, O, Takagi, J, Fukuda, T, Sato, N. Vasodilatory response of the coronary arteries after Kawasaki disease: evaluation by intracoronary injection of isosorbide dinitrate. J Pediatr 1992; 121: 684688.CrossRefGoogle ScholarPubMed
12. Yamakawa, R, Ishii, M, Sugimura, T, et al. Coronary endothelial dysfunction after Kawasaki disease: evaluation by intracoronary injection of acetylcholine. J Am Coll Cardiol 1998; 31: 10741080.CrossRefGoogle ScholarPubMed
13. Hamaoka, K, Onouchi, Z, Ohmochi, Y. Coronary flow reserve in children with Kawasaki disease without angiographic evidence of coronary stenosis. Am J Cardiol 1992; 69: 691692.CrossRefGoogle ScholarPubMed
14. Hamaoka, K, Onouchi, Z, Kamiya, Y, Sakata, K. Evaluation of coronary flow velocity dynamics and flow reserve in patients with Kawasaki disease by means of a Doppler guide wire. J Am Coll Cardiol 1998; 31: 833840.CrossRefGoogle ScholarPubMed
15. Mitani, Y, Okuda, Y, Shimpo, H, et al. Impaired endothelial function in epicardial coronary arteries after Kawasaki disease. Circulation 1997; 96: 454461.Google ScholarPubMed
16. Hauser, M, Bengel, F, Kuehn, A, et al. Myocardial blood flow and coronary flow reserve in children with “normal” epicardial coronary arteries after the onset of Kawasaki disease assessed by positron emission tomography. Pediatr Cardiol 2004; 25: 108112.Google ScholarPubMed
17. Muzik, O, Paridon, SM, Singh, TP, Morrow, WR, Dayanikli, F, Di Carli, MF. Quantification of myocardial blood flow and flow reserve in children with a history of Kawasaki disease and normal coronary arteries using positron emission tomography. J Am Coll Cardiol 1996; 28: 757762.CrossRefGoogle ScholarPubMed
18. Cicala, S, Galderisi, M, Grieco, M, et al. Transthoracic echo-Doppler assessment of coronary microvascular function late after Kawasaki disease. Pediatr Cardiol 2008; 29: 321327.CrossRefGoogle ScholarPubMed
19. Ghelani, SJ, Singh, S, Manojkumar, R. Endothelial dysfunction in a cohort of North Indian children with Kawasaki disease without overt coronary artery involvement. J Cardiol 2009; 53: 226231.CrossRefGoogle Scholar
20. Patvardhan, EA, Heffernan, KS, Ruan, JM, Soffler, MI, Karas, RHI, Kuvin, JT. Assessment of vascular endothelial function with peripheral arterial tonometry: information at your fingertips? Cardiol Rev 2010; 18: 2028.CrossRefGoogle ScholarPubMed
21. 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 2006; 101: 545548.CrossRefGoogle ScholarPubMed
22. Kuvin, JT, Karas, RH. Clinical utility of endothelial function testing: ready for prime time? Circulation 2003; 107: 32433247.CrossRefGoogle ScholarPubMed
23. Kuvin, JT, Patel, AR, Sliney, KA, et al. Assessment of peripheral vascular endothelial function with finger arterial pulse wave amplitude. Am Heart J 2003; 146: 168174.CrossRefGoogle ScholarPubMed
24. Selamet Tierney, ES, Newburger, JW, Gauvreau, K, et al. Endothelial pulse amplitude testing: feasibility and reproducibility in adolescents. J Pediatr 2009; 154: 901905.CrossRefGoogle ScholarPubMed
25. Haller, MJ, Stein, J, Shuster, J, et al. Peripheral artery tonometry demonstrates altered endothelial function in children with type 1 diabetes. Pediatr Diabetes 2007; 8: 193198.CrossRefGoogle ScholarPubMed
26. Ayusawa, M, Sonobe, T, Uemura, S, et al. Revision of diagnostic guidelines for Kawasaki disease (the 5th revised edition). Pediatr Int 2005; 47: 232234.CrossRefGoogle ScholarPubMed
27. Bonetti, PO, Pumper, GM, Higano, ST, et al. Noninvasive identification of patients with early coronary atherosclerosis by assessment of digital reactive hyperemia. JACC 2004; 44: 21372141.CrossRefGoogle ScholarPubMed
28. Duong, TT, Silverman, ED, Bissessar, MV, Yeung, RS. Superantigenic activity is responsible for induction of coronary arteritis in mice: an animal model of Kawasaki disease. Int Immunol 2003; 15: 7989.CrossRefGoogle ScholarPubMed
29. Rowley, AH. The etiology of Kawasaki disease: superantigen or conventional antigen? Pediatr Infect Dis J 1999; 18: 6970.CrossRefGoogle ScholarPubMed
30. Wang, CL, Wu, YT, Liu, CA, Kuo, HC, Yang, KD. Kawasaki disease: infection, immunity and genetics. Pediatr Infect Dis J 2005; 24: 9981004.CrossRefGoogle ScholarPubMed
31. Leung, DY. Immunologic aspects of Kawasaki syndrome. J Rheumatol Suppl 1990; 24: 1518.Google ScholarPubMed
32. Burns, JC, Shike, H, Gordon, JB, Malhotra, A, Schoenwetter, M, Kawasaki, T. Sequelae of Kawasaki disease in adolescents and young adults. J Am Coll Cardiol 1996; 28: 253257.CrossRefGoogle ScholarPubMed
33. Kato, H, Sugimura, T, Akagi, T, et al. Long-term consequences of Kawasaki disease. A 10- to 21-year follow-up study of 594 patients. Circulation 1996; 94: 13791385.CrossRefGoogle ScholarPubMed
34. Furuyama, H, Odagawa, Y, Katoh, C, et al. Altered myocardial flow reserve and endothelial function late after Kawasaki disease. J Pediatr 2003; 142: 149154.CrossRefGoogle ScholarPubMed
35. Dhillon, R, Clarkson, P, Donald, AE, et al. Endothelial dysfunction late after Kawasaki disease. Circulation 1996; 94: 21032106.CrossRefGoogle ScholarPubMed
36. Deng, YB, Xiang, HJ, Chang, Q, Li, CL. Evaluation by high-resolution ultrasonography of endothelial function in brachial artery after Kawasaki disease and the effects of intravenous administration of vitamin C. Circ J 2002; 66: 908912.CrossRefGoogle ScholarPubMed
37. Dalla Pozza, R, Bechtold, S, Urschel, S, Kozlik-Feldmann, R, Netz, H. Subclinical atherosclerosis, but normal autonomic function after Kawasaki disease. J Pediatr 2007; 151: 239243.CrossRefGoogle ScholarPubMed
38. Kadono, T, Sugiyama, H, Hoshiai, M, et al. Endothelial function evaluated by flow-mediated dilatation in pediatric vascular disease. Pediatr Cardiol 2005; 26: 385390.CrossRefGoogle ScholarPubMed
39. Ikemoto, Y, Ogino, H, Teraguchi, M, Kobayashi, Y. Evaluation of preclinical atherosclerosis by flow-mediated dilatation of the brachial artery and carotid artery analysis in patients with a history of Kawasaki disease. Pediatr Cardiol 2005; 26: 782786.CrossRefGoogle ScholarPubMed
40. McCrindle, BW, McIntyre, S, Kim, C, Lin, T, Adeli, K. Are patients after Kawasaki disease at increased risk for accelerated atherosclerosis? J Pediatr 2007; 151: 244248.CrossRefGoogle ScholarPubMed
41. Noto, N, Okada, T, Karasawa, K, et al. Age-related acceleration of endothelial dysfunction and subclinical atherosclerosis in subjects with coronary artery lesions after Kawasaki disease. Pediatr Cardiol 2006; 30: 262268.CrossRefGoogle Scholar