Hostname: page-component-76fb5796d-5g6vh Total loading time: 0 Render date: 2024-04-27T17:58:53.378Z Has data issue: false hasContentIssue false
  • English
  • Français

Vascular function long term after Kawasaki disease: another piece of the puzzle?

Published online by Cambridge University Press:  05 July 2016

Fátima F. Pinto ,
Inês Gomes ,
Petra Loureiro ,
Sérgio Laranjo ,
Ana T. Timóteo  and
Miguel M. Carmo
Fátima F. Pinto*
Affiliation:
Pediatric Cardiology Department; Hospital Santa Marta, Centro Hospitalar de Lisboa Central (CHLC)Lisbon, Portugal
Inês Gomes
Affiliation:
Pediatric Cardiology Department; Hospital Santa Marta, Centro Hospitalar de Lisboa Central (CHLC)Lisbon, Portugal
Petra Loureiro
Affiliation:
Pediatric Cardiology Department; Hospital Santa Marta, Centro Hospitalar de Lisboa Central (CHLC)Lisbon, Portugal
Sérgio Laranjo
Affiliation:
Pediatric Cardiology Department; Hospital Santa Marta, Centro Hospitalar de Lisboa Central (CHLC)Lisbon, Portugal
Ana T. Timóteo
Affiliation:
Cardiology Department; Hospital de Santa Marta, (CHLC), Lisbon, Portugal
Miguel M. Carmo
Affiliation:
Cardiology Department; Hospital de Santa Marta, (CHLC), Lisbon, Portugal
*
Correspondence to: F. F. Pinto, MD, Pediatric Cardiology Department, Hospital de Santa Marta – CHLC, Rua de Santa Marta 50, 1169-024 Lisbon, Portugal. Tel:+35 121 359 4332; Fax:+35 121 359 4326; E-mail: Fatima.Pinto@hsmarta.min-saude.pt
Get access Rights & Permissions [Opens in a new window]

Abstract

Background

Kawasaki disease is an acute systemic vasculitis. Cardiac complications are frequent and include endothelial dysfunction in patients with coronary anomalies. Thus far, endothelial dysfunction in patients with no coronary lesions is poorly understood. Our aim was to access the vascular function in adolescents and young adults long term after Kawasaki disease, but without coronary aneurysms or any other cardiac risk factors.

Methods

We carried out a single-centre prospective study in a Portuguese population. We evaluated two groups of subjects: (1) Kawasaki disease patients over 11 years of age, diagnosed >5 years ago, 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 assessed. Endo-PAT and carotid intima-media thickness assessment were performed to determine vascular function.

Results

In total, 43 Kawasaki disease patients were assessed and compared with 43 controls. Kawasaki disease patients presented a decreased reactive hyperaemia index compared with controls (1.59±0.45 versus 1.98±0.41; p<0.001). Augmentation index was similar in both groups (−4.5±7 versus −5±9%; p 0.6). The mean carotid intima-media thickness was not significantly increased in the Kawasaki disease group. There were no statistically significant changes with regard to laboratory data.

Conclusions

Children with Kawasaki disease may have long-term sequelae, even when there is no discernible coronary artery involvement in the acute stage of the disease. Further research is needed to assess whether known strategies to improve endothelial function would bring potential benefits to Kawasaki disease patients.

Keywords

Kawasaki diseasevascular functionendothelium
Type
Original Articles
Information
Cardiology in the Young , Volume 27 , Issue 3 , March 2017 , pp. 488 - 497
Copyright
© Cambridge University Press 2016 

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. Kawasaki, T. Acute febrile mucocutaneous syndrome with lymphoid involvement with specific desquamation of the fingers and toes in children. Arerugi 1967; 16: 178–222.Google ScholarPubMed
2. Laranjo, S, Aidos, H, Lourenço, A, Rodrigues, V, Pinto, FF. Ten years of Kawasaki disease in Portugal: national database results. Rev Port Cardiol 2015; 34: 171.Google Scholar
3. Rowley, AH. The etiology of Kawasaki disease: superantigen or conventional antigen? Pediatr Infect Dis J 1999; 18: 69–70.CrossRefGoogle ScholarPubMed
4. Wang, CL, Wu, YT, Liu, CA, et al. Kawasaki disease: infection, immunity and genetics. Pediatr Infect Dis J 2005; 24: 998–1004.CrossRefGoogle ScholarPubMed
5. Duong, TT, Silverman, ED, Bissessar, MV, et al. Superantigenic activity is responsible for induction of coronary arteritis in mice: an animal model of Kawasaki disease. Int Immunol 2003; 15: 79–89.Google Scholar
6. Kato, H, Sugimura, T, Akagi, T, et al. Long-term consequences of Kawasaki disease. A 0-to 21-year follow-up study of 594 patients. Circulation 1996; 94: 1379–1385.Google Scholar
7. Gupta-Malhotra, M, Gruber, D, Abraham, SS, et al. Atherosclerosis in survivors of Kawasaki disease. J Pediatr 2009; 155: 572–577.Google Scholar
8. McCrindle, BW, McIntyre, S, Kim, C, et al. Are patients after Kawasaki disease at increased risk for accelerated atherosclerosis? J Pediatr 2007; 151: 244–248.Google Scholar
9. Newburger, JW, Burns, JC, Beiser, AS, et al. Altered lipid profile after Kawasaki syndrome. Circulation 1991; 84: 625–631.CrossRefGoogle ScholarPubMed
10. Mitani, Y, Sawada, H, Hayakawa, H, et al. Elevated levels of high-sensitivity C-reactive protein and serum amyloid-A late after Kawasaki disease: association between inflammation and late coronary sequelae in Kawasaki disease. Circulation 2005; 111: 38–43.Google Scholar
11. Dhillon, R, Clarkson, P, Donald, AE, et al. Endothelial dysfunction late after Kawasaki disease. Circulation 1996; 94: 2103–2106.CrossRefGoogle ScholarPubMed
12. Iemura, M, Ishii, M, Sugimura, T, et al. Long term consequences of regressed coronary aneurysms after Kawasaki disease: vascular wall morphology and function. Heart 2000; 83: 307–311.Google Scholar
13. Orenstein, JM, Shulman, ST, Fox, LM, et al. Three linked vasculopathic processes characterize Kawasaki disease: a light and transmission electron microscopic study. PLoS One 2012; 7: e38998.CrossRefGoogle ScholarPubMed
14. Burns, JC, Shike, H, Gordon, JB, et al. Sequelae of Kawasaki disease in adolescents and young adults. J Am Coll Cardiol 1996; 28: 253–257.Google Scholar
15. 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: 1074–1080.Google Scholar
16. Silva, AA, Maeno, Y, Hashmi, A, et al. Cardiovascular risk factors after Kawasaki disease: a case-control study. J Pediatr 2001; 138: 400–405.CrossRefGoogle ScholarPubMed
17. Furuyama, H, Odagawa, Y, Katoh, C, et al. Altered myocardial flow reserve and endothelial function late after Kawasaki disease. J Pediatr 2003; 142: 149–154.Google Scholar
18. Ikemoto, Y, Ogino, H, Terguchi, M, et al. Evaluation of preclinical atherosclerosis by flow-mediated dilation of the brachial artery and carotid artery analysis in patients with a history of Kawasaki disease. Pediatr Cardiol 2005; 26: 782–786.Google Scholar
19. 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: 1095–1099.CrossRefGoogle ScholarPubMed
20. Ross, R. Atherosclerosis an inflammatory disease. N Engl J Med 1999; 340: 115–126.CrossRefGoogle ScholarPubMed
21. Zeiher, AM, Drexler, H, Wollschlager, H, et al. Modulation of coronary vasomotor tone in humans. Progressive endothelial dysfunction with different early stages of coronary atherosclerosis. Circulation 1991; 83: 391–401.Google Scholar
22. Vita, JA, Keaney, JF Jr. Endothelial function: a barometer for cardiovascular risk. Circulation 2002; 106: 640–642.Google Scholar
23. Furchgott, RF, Zawadzki, JV. The obligatory role of endothelial cells in the relaxation of arterial smooth muscle by acetylcholine. Nature 1980; 288: 373–376.Google Scholar
24. Forstermann, U, Closs, EI, Pollock, JS, et al. Nitric oxide synthase isozymes. Characterization, purification, molecular cloning, and functions. Hypertension 1994; 23: 1121–1131.Google Scholar
25. Cooke, JP, Rossitch, E Jr, Andon, NA, et al. Flow activates an endothelial potassium channel to release an endogenous nitrovasodilator. J Clin Invest 1991; 88: 1663–1671.Google Scholar
26. Kadono, T, Sugiyama, H, Hoshiai, M, et al. Endothelial function evaluated by flow-mediated dilatation in pediatric vascular disease. Pediatr Cardiol 2005; 26: 385–390.Google Scholar
27. Deanfield, JE, Halcox, JP, Rabelink, TJ. Endothelial function and dysfunction: testing and clinical relevance. Circulation 2007; 115: 1285–1295.CrossRefGoogle ScholarPubMed
28. Hamburg, NM, Palmisano, J, Larson, MG, et al. Relation of brachial and digital measures of vascular function in the community: the Framingham Heart Study. Hypertension 2011; 57: 390–396.Google Scholar
29. 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: 168–174.Google Scholar
30. Laurent, S, Cockcroft, J, Van Bortel, L, et al. Expert consensus document on arterial stiffness: methodological issues and clinical applications. Eur Heart J 2006; 27: 2588–2605.Google Scholar
31. Newburger, J, Keflioglu-Scheiber, A, Opazo Saez, AM, et al. Augmentation index is associated with cardiovascular risk. J Hypertens 2002; 20: 2407–2414.Google Scholar
32. Urbina, EM, Williams, RV, Alpert, BS, et al. Noninvasive assessment of subclinical atherosclerosis in children and adolescents: recommendations for standard assessment for clinical research: a scientific statement from the American Heart Association. Hypertension 2009; 54: 919–950.Google Scholar
33. Meena, RS, Rohit, M, Gupta, A, et al. Carotid intima-media thickness in children with Kawasaki disease. Rheumatol Int 2014; 34: 1117–1121.Google Scholar
34. Lee, SJ, Ahn, HM, You, JH, et al. Carotid intima media thickness and pulse wave velocity after recovery from Kawasaki disease. Korean Circ J 2009; 39: 264–269.CrossRefGoogle ScholarPubMed
35. Cole, TJ, Bellizi, MC, Flegal, KM, et al. Establishing a standard definition for child overweight and obesity worldwide: international survey. BMJ 2000; 320: 1240–1243.Google Scholar
36. Ayusawa, M, Sonobe, T, Uemura, S, et al. Revision of diagnostic guidelines for Kawasaki disease (the 5th revised edition). Pediatr Int 2005; 47: 232–234.Google Scholar
37. Kuvin, JT, Karas, RH. Clinical utility of endothelial function testing: ready for prime time? Circulation 2003; 107: 3243–3247.CrossRefGoogle ScholarPubMed
38. 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: 168–174.CrossRefGoogle ScholarPubMed
39. Selamet Tierney, ES, Newburger, JW, Gauvreau, K, et al. Endothelial pulse amplitude testing: feasibility and reproducibility in adolescents. J Pediatr 2009; 154: 901–905.Google Scholar
40. Pinto, FF, Laranjo, S, Paramés, F, et al. Long-term evaluation of endothelial function in Kawasaki disease patients. Cardiol Young 2013; 23: 517–522.Google Scholar
41. Roman, MJ, Naqvi, TZ, Gardin, JM, et al. Clinical application of non-invasive vascular ultrasound in cardiovascular risk stratification: a report from the American Society of Echocardiography and the Society for Vascular Medicine and Biology. J Am Soc Echocardiogr 2006; 11: 201–211.Google Scholar
42. Touboul, PJ, Hennerici, MG, Meairs, S, et al. Mannheim carotid intima-media thickness and plaque consensus (2004-2006-2011). An update on behalf of the advisory board of the 3rd, 4th and 5th watching the risk symposia, at the 13th, 15th and 20th European Stroke Conferences, Mannheim, Germany, 2004, Brussels, Belgium, 2006, and Hamburg, Germany, 2011. Cerebrovasc Dis 2012; 34: 290–296.Google Scholar
43. 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: 691–692.CrossRefGoogle ScholarPubMed
44. 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: 108–112.Google ScholarPubMed
45. Cheung, YF, Wong, SJ, Ho, MHK. Relationship between carotid intima-media thickness and arterial stiffness in children after Kawasaki disease. Arch Dis Child. 2007; 92: 43–47.CrossRefGoogle ScholarPubMed
46. Ooyanagi, R, Fuse, S, Tomita, H, et al. Pulse wave velocity and ankle brachial index in patients with Kawasaki disease. Pediatr Int 2004; 46: 398–402.Google Scholar
47. Mitani, Y, Okuda, Y, Shimpo, H, et al. Impaired endothelial function in epicardial coronary arteries after Kawasaki disease. Circulation 1997; 96: 454–461.Google Scholar
48. Dalla Pozza, R, Bechtold, S, Urschel, S, et al. Subclinical atherosclerosis, but normal autonomic function after Kawasaki syndrome. J Pediatr 2007; 151: 239–243.CrossRefGoogle Scholar
49. Tierney, ESS, Gal, D, Gauvreau, K, et al. Vascular health in Kawasaki Disease. J Am Coll Cardiol 2013; 62: 1114–1121.CrossRefGoogle Scholar
50. 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. Pediatrics 2004; 114: 1708–1733.Google Scholar
51. Newburger, JW, Takahashi, M, Gerber, MA, et al. Guidelines for diagnosis and management of cardiovascular sequelae in Kawasaki disease (JCS 2008) – digest version. Circ J 2010; 74: 1989–2020.Google Scholar
52. Gersony, WM. The adult after Kawasaki disease the risks for late coronary events. J Am Coll Cardiol 2009; 54: 1921–1923.Google Scholar
53. Gordon, JB, Kahn, AM, Burns, JC. When children with Kawasaki disease grow up; myocardial and vascular complications in adulthood. J Am Coll Cardiol 2009; 54: 1911–1912.CrossRefGoogle ScholarPubMed
54. Libby, P, Ridker, PM, Maseri, A. Inflammation and atherosclerosis. Circulation 2002; 105: 1135–1143.CrossRefGoogle ScholarPubMed