Skip to main content

Advertisement

Log in

Microvascular Endothelial Function Assessed Using Peripheral Arterial Tonometry in Adolescents with Repaired Congenital Heart Disease

  • Research
  • Published:
Pediatric Cardiology Aims and scope Submit manuscript

Abstract

Atherosclerosis can develop in adult patients with congenital heart disease (CHD) and should be given attention. Endothelial function is well known as a predictor of the development of atherosclerosis but has not been well investigated in patients with repaired CHD. This study aimed to clarify the endothelial function and its relationship with clinical backgrounds and parameters in adolescents with various types of repaired CHDs. Endothelial function was evaluated using peripheral arterial tonometry (PAT). The reactive hyperemia index (RHI) was evaluated and compared between adolescents with repaired CHD and those in the control group. The relationship between the clinical background and parameters was also investigated in patients with repaired CHD. Forty-eight patients with repaired CHD (age 14.0 ± 3.3 years) and 114 healthy volunteers were included in this study. Patients with repaired CHD comprised 16 with repaired non-cyanotic CHD, 14 with repaired tetralogy of Fallot, and 18 who underwent the Fontan procedure. RHI in the repaired CHD group was significantly lower than in the control group. There was no significant correlation between the RHI and blood biochemical markers, such as uric acid, creatine, and brain natriuretic peptide levels. The RHI was significantly higher in patients taking angiotensin-converting enzyme (ACE) inhibitors and angiotensin receptor blockers (ARBs) than in those not taking them. Endothelial function was impaired in adolescents with repaired CHD compared to that in the control group. Microvascular endothelial dysfunction developed even in adolescents with simple non-cyanotic CHD.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  1. McGill HC, McMahan CA, Zieske AW, Sloop GD, Walcott JV, Troxclair DA, Malcom GT, Tracy RE, Oalmann MC, Strong JP (2000) Associations of coronary heart disease risk factors with the intermediate lesion of atherosclerosis in youth. The Pathobiological Determinants of Atherosclerosis in Youth (PDAY) Research Group. Arterioscler Thromb Vasc Biol 20:1998–2004. https://doi.org/10.1161/01.atv.20.8.1998

    Article  PubMed  Google Scholar 

  2. Otani N, Toyoda S, Sakuma M, Hayashi K, Ouchi M, Fujita T, Anzai N, Tanaka A, Node K, Uemura N, Inoue T (2018) Effects of uric acid on vascular endothelial function from bedside to bench. Hypertens Res 41:923–931. https://doi.org/10.1038/s41440-018-0095-4

    Article  PubMed  Google Scholar 

  3. Sesti G, Mannino GC, De Lorenzo C, Greco A, Sciacqua A, Marini MA, Andreozzi F, Perticone F (2013) A functional variant of the dimethylarginine dimethylaminohydrolase-2 gene is associated with chronic kidney disease. Atherosclerosis 231:141–144. https://doi.org/10.1016/j.atherosclerosis.2013.08.041

    Article  CAS  PubMed  Google Scholar 

  4. Hornig B, Maier V, Drexler H (1996) Physical training improves endothelial function in patients with chronic heart failure. Circulation 93:210–214. https://doi.org/10.1161/01.cir.93.2.210

    Article  CAS  PubMed  Google Scholar 

  5. Jacob M, Saller T, Chappell D, Rehm M, Welsch U, Becker BF (2013) Physiological levels of A-, B- and C-type natriuretic peptide shed the endothelial glycocalyx and enhance vascular permeability. Basic Res Cardiol 108:347. https://doi.org/10.1007/s00395-013-0347-z

    Article  CAS  PubMed  Google Scholar 

  6. Shiina Y, Toyoda T, Kawasoe Y, Tateno S, Shirai T, Wakisaka Y, Matsuo K, Mizuno Y, Terai M, Hamada H, Niwa K (2011) Prevalence of adult patients with congenital heart disease in Japan. Int J Cardiol 146:13–16. https://doi.org/10.1016/j.ijcard.2009.05.032

    Article  PubMed  Google Scholar 

  7. Tarp JB, Clausen P, Celermajer D, Christoffersen C, Jensen AS, Sørensen K, Sillesen H, Estensen ME, Nagy E, Holstein-Rathlou NH, Engstrøm T, Feldt-Rasmussen B, Søndergaard L (2020) Vascular function in adults with cyanotic congenital heart disease. Int J Cardiol Heart Vasc 30:100632. https://doi.org/10.1016/j.ijcha.2020.100632

    Article  PubMed  PubMed Central  Google Scholar 

  8. Niwa K, Perloff JK, Bhuta SM, Laks H, Drinkwater DC, Child JS, Miner PD (2001) Structural abnormalities of great arterial walls in congenital heart disease: light and electron microscopic analyses. Circulation 103:393–400. https://doi.org/10.1161/01.cir.103.3.393

    Article  CAS  PubMed  Google Scholar 

  9. Goldstein BH, Golbus JR, Sandelin AM, Warnke N, Gooding L, King KK, Donohue JE, Gurney JG, Goldberg CS, Rocchini AP, Charpie JR (2011) Usefulness of peripheral vascular function to predict functional health status in patients with Fontan circulation. Am J Cardiol 108:428–434. https://doi.org/10.1016/j.amjcard.2011.03.064

    Article  PubMed  Google Scholar 

  10. Lambert E, d’Udekem Y, Cheung M, Sari CI, Inman J, Ahimastos A, Eikelis N, Pathak A, King I, Grigg L, Schlaich M, Lambert G (2013) Sympathetic and vascular dysfunction in adult patients with Fontan circulation. Int J Cardiol 167:1333–1338. https://doi.org/10.1016/j.ijcard.2012.04.015

    Article  PubMed  Google Scholar 

  11. Lin ZB, Ci HB, Li Y, Cheng TP, Liu DH, Wang YS, Xu J, Yuan HX, Li HM, Chen J, Zhou L, Wang ZP, Zhang X, Ou ZJ, Ou JS (2017) Endothelial microparticles are increased in congenital heart diseases and contribute to endothelial dysfunction. J Transl Med 15:4. https://doi.org/10.1186/s12967-016-1087-2

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Kuvin JT, Patel AR, Sliney KA, Pandian NG, Sheffy J, Schnall RP, Karas RH, Udelson JE (2003) Assessment of peripheral vascular endothelial function with finger arterial pulse wave amplitude. Am Heart J 146:168–174. https://doi.org/10.1016/S0002-8703(03)00094-2

    Article  PubMed  Google Scholar 

  13. Odanaka Y, Takitani K, Katayama H, Fujiwara H, Kishi K, Ozaki N, Ashida A, Takaya R, Tamai H (2017) Microvascular endothelial function in Japanese early adolescents. J Clin Biochem Nutr 61:228–232. https://doi.org/10.3164/jcbn.17-58

    Article  PubMed  PubMed Central  Google Scholar 

  14. 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 154:901–905. https://doi.org/10.1016/j.jpeds.2008.12.028

    Article  PubMed  Google Scholar 

  15. de Groot PC, Thijssen D, Binkhorst M, Green DJ, Schokking M, Hopman MT (2010) Vascular function in children with repaired tetralogy of Fallot. Am J Cardiol 106:851–855. https://doi.org/10.1016/j.amjcard.2010.05.009

    Article  PubMed  Google Scholar 

  16. Tomiyama H, Higashi Y, Takase B, Node K, Sata M, Inoue T, Ishibashi Y, Ueda S, Shimada K, Yamashina A (2011) Relationships among hyperuricemia, metabolic syndrome, and endothelial function. Am J Hypertens 24:770–774. https://doi.org/10.1038/ajh.2011.55

    Article  CAS  PubMed  Google Scholar 

  17. Taher R, Sara JD, Prasad M, Kolluri N, Toya T, Lerman LO, Lerman A (2019) Elevated serum uric acid is associated with peripheral endothelial dysfunction in women. Atherosclerosis 290:37–43. https://doi.org/10.1016/j.atherosclerosis.2019.07.013

    Article  CAS  PubMed  Google Scholar 

  18. Hirata Y, Sugiyama S, Yamamoto E, Matsuzawa Y, Akiyama E, Kusaka H, Fujisue K, Kurokawa H, Matsubara J, Sugamura K, Maeda H, Iwashita S, Jinnouchi H, Matsui K, Ogawa H (2014) Endothelial function and cardiovascular events in chronic kidney disease. Int J Cardiol 173:481–486. https://doi.org/10.1016/j.ijcard.2014.03.085

    Article  PubMed  Google Scholar 

  19. Enomoto K, Yamabe H, Toyama K, Matsuzawa Y, Yamamuro M, Uemura T, Morihisa K, Iwashita S, Kaikita K, Sugiyama S, Ogawa H (2011) Improvement effect on endothelial function in patients with congestive heart failure treated with cardiac resynchronization therapy. J Cardiol 58:69–73. https://doi.org/10.1016/j.jjcc.2011.01.010

    Article  PubMed  Google Scholar 

  20. Ki YJ, Seo JB, Kim HL, Lim WH, Seo HY, Lee JY, Chung WY (2017) Comparison of endothelial function improvement estimated with reactive hyperemia index between ramipril and telmisartan in hypertensive patients. Clin Hypertens 23:4. https://doi.org/10.1186/s40885-016-0060-y

    Article  PubMed  PubMed Central  Google Scholar 

  21. Watanabe T, Barker TA, Berk BC (2005) Angiotensin II and the endothelium: diverse signals and effects. Hypertension 45:163–169. https://doi.org/10.1161/01.HYP.0000153321.13792.b9

    Article  CAS  PubMed  Google Scholar 

  22. Caprio M, Newfell BG, la Sala A, Baur W, Fabbri A, Rosano G, Mendelsohn ME, Jaffe IZ (2008) Functional mineralocorticoid receptors in human vascular endothelial cells regulate intercellular adhesion molecule-1 expression and promote leukocyte adhesion. Circ Res 102:1359–1367. https://doi.org/10.1161/CIRCRESAHA.108.174235

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Suwaidi JA, Hamasaki S, Higano ST, Nishimura RA, Holmes DR, Lerman A (2000) Long-term follow-up of patients with mild coronary artery disease and endothelial dysfunction. Circulation 101:948–954. https://doi.org/10.1161/01.cir.101.9.948

    Article  CAS  PubMed  Google Scholar 

Download references

Funding

No funding was received to assist with the preparation of this manuscript.

Author information

Authors and Affiliations

Authors

Contributions

All authors contributed to the study’s conception and design. Material preparation, data collection, and analysis were performed by YO, KK, AA, and KT. The first draft of the manuscript was written by YO and all authors commented on the previous versions of the manuscript. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Yutaka Odanaka.

Ethics declarations

Competing Interests

There are no potential competing interests to disclose.

Ethical Approval

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki Declaration and its later amendments or comparable ethical standards. The study protocol was approved by the ethics committee of the Osaka Medical and Pharmaceutical University (Code No. 134).

Consent to Participate

Informed consent was obtained from all participants and their parents.

Consent to Publish

The participants consented to the submission of the paper to the journal.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Odanaka, Y., Kishi, K., Takigiku, K. et al. Microvascular Endothelial Function Assessed Using Peripheral Arterial Tonometry in Adolescents with Repaired Congenital Heart Disease. Pediatr Cardiol (2023). https://doi.org/10.1007/s00246-023-03283-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00246-023-03283-x

Keywords

Navigation