Comparison of CIMT and FMD in the Brachial Artery Between Children With Acyanotic Congenital Heart Disease and Healthy Controls: A Case-Control Study
-
Alireza Ahmadi
,
Mehdi Ghaderian
,
Hajar Nourmohammadi
,
Mohammad Reza Sabri
,
Bahar Dehghan
,
Chehreh Mahdavi
Abstract
Background: Congenital heart disease (CHD), a developmental abnormality of the heart and vessels, is encountered in the pediatric age group frequently. Brachial artery flow-mediated dilation (FMD) and carotid intima-media thickness (CIMT) are indicators of subclinical cardiovascular disease and are used as surrogate measures of subclinical atherosclerosis. The present study aimed to compare CIMT and FMD between children with acyanotic congenital heart disease (ACHD) and healthy controls.
Methods: A case-control study on 50 children with ACHD and 43 healthy individuals was done in Isfahan, Iran, between 2021 and 2022. The case group was selected via non-random sampling, and healthy controls were recruited from the relatives of the patients. A checklist, including age, sex, body mass index, and blood pressure, was filled out for all the participants. Then, FMD and CIMT were measured with brachial and carotid artery ultrasonography.
Results: Fifty children with ACHD and 43 healthy individuals (controls) under 18 years old participated in this study. Of these, 44 (47.3%) were girls and 49 (52.7%) were boys. The mean FMD was significantly higher in the ACHD group than in the control group (0.084±0.027 vs 0.076±0.042; P=0.021; 95% CI, 007 to 0.122;). CIMT was significantly higher in the ACHD group than in the control group (0.39±0.12 vs 0.34±0.1; P=0.037; 95% CI, 0.009 to 0.102;). However, systolic and diastolic blood pressure did not show differences between the groups.
Conclusion: Based on our results, CIMT and FMD assessment may help detect early changes in peripheral vessels associated with atherosclerosis in the future in ACHD. Further studies are needed to confirm our findings.
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2. Candelino M, Tagi VM, Chiarelli F. Cardiovascular risk in children: a burden for future generations. Ital J Pediatr 2022;48:57.
3. Naqvi TZ, Lee MS. Carotid intima-media thickness and plaque in cardiovascular risk assessment. JACC Cardiovasc Imaging 2014;7:1025-1038.
4. Greenland P, LaBree L, Azen SP, Doherty TM, Detrano RC. Coronary artery calcium score combined with Framingham score for risk prediction in asymptomatic individuals. JAMA 2004;291:210-215.
5. Sabri MR, Tavana EN, Ahmadi A, Gheissari A. Effect of vitamin C on endothelial function of children with chronic renal failure: An experimental study. Adv Biomed Res 2015;4:260.
6. Dalla Pozza R, Ehringer-Schetitska D, Fritsch P, Jokinen E, Petropoulos A, Oberhoffer R; Association for European Paediatric Cardiology Working Group Cardiovascular Prevention. Intima media thickness measurement in children: A statement from the Association for European Paediatric Cardiology (AEPC) Working Group on Cardiovascular Prevention endorsed by the Association for European Paediatric Cardiology. Atherosclerosis 2015;238:380-387.
7. Rohit M, Shrivastava S. Acyanotic and Cyanotic Congenital Heart Diseases. Indian J Pediatr 2018;85:454-460.
8. Moller JH, Hoffman J IE, Benson DW, Van Hare GF, Wren C, eds. Pediatric Cardiovascular Medicine. 7th ed. Pondicherry: Wiley-Blackwell; 2012. p. 23–32.
9. Hoffman JI, Kaplan S. The incidence of congenital heart disease. J Am Coll Cardiol 2002;39:1890-900.
10. Ahmadi AR, Sabri MR, Navabi ZS, Ghaderian M, Dehghan B, Mahdavi C, Khodarahmi S. Early Results of the Persian Registry of Cardiovascular Disease/Congenital Heart Disease (PROVE/CHD) in Isfahan. J Tehran Heart Cent 2020;15:158-164.
11. Khasawneh W, Hakim F, Abu Ras O, Hejazi Y, Abu-Aqoulah A. Incidence and Patterns of Congenital Heart Disease Among Jordanian Infants, a Cohort Study From a University Tertiary Center. Front Pediatr 2020;8:219.
12. Wallooppillai NJ, Jayasinghe Mde S. Congenital heart disease in Ceylon. Br Heart J 1970;32:304-306.
13. van der Linde D, Konings EE, Slager MA, Witsenburg M, Helbing WA, Takkenberg JJ, Roos-Hesselink JW. Birth prevalence of congenital heart disease worldwide: a systematic review and meta-analysis. J Am Coll Cardiol 2011;58:2241-2247.
14. Ross R. Atherosclerosis--an inflammatory disease. N Engl J Med 1999;340:115-126.
15. Celermajer DS, Sorensen KE, Gooch VM, Spiegelhalter DJ, Miller OI, Sullivan ID, Lloyd JK, Deanfield JE. Non-invasive detection of endothelial dysfunction in children and adults at risk of atherosclerosis. Lancet 1992;340:1111-1115.
16. Sabri MR, Tavana EN, Ahmadi A, Hashemipour M. The effect of vitamin C on endothelial function of children with type 1 diabetes: an experimental study. Int J Prev Med 2014;5:999-1004.
17. Raitakari OT, Juonala M, Kähönen M, Taittonen L, Laitinen T, Mäki-Torkko N, Järvisalo MJ, Uhari M, Jokinen E, Rönnemaa T, Akerblom HK, Viikari JS. Cardiovascular risk factors in childhood and carotid artery intima-media thickness in adulthood: the Cardiovascular Risk in Young Finns Study. JAMA 2003;290:2277-2283.
18. Burke GL, Evans GW, Riley WA, Sharrett AR, Howard G, Barnes RW, Rosamond W, Crow RS, Rautaharju PM, Heiss G. Arterial wall thickness is associated with prevalent cardiovascular disease in middle-aged adults. The Atherosclerosis Risk in Communities (ARIC) Study. Stroke 1995;26:386-391.
19. Brunner H, Cockcroft JR, Deanfield J, Donald A, Ferrannini E, Halcox J, Kiowski W, Lüscher TF, Mancia G, Natali A, Oliver JJ, Pessina AC, Rizzoni D, Rossi GP, Salvetti A, Spieker LE, Taddei S, Webb DJ; Working Group on Endothelins and Endothelial Factors of the European Society of Hypertension. Endothelial function and dysfunction. Part II: Association with cardiovascular risk factors and diseases. A statement by the Working Group on Endothelins and Endothelial Factors of the European Society of Hypertension. J Hypertens 2005;23:233-246.
20. Sabri MR, Tavana EN, Ahmadi A, Mostafavy N. Does Vitamin C improve endothelial function in patients with Kawasaki disease? J Res Med Sci 2015;20:32-36.
21. Sorensen KE, Celermajer DS, Spiegelhalter DJ, Georgakopoulos D, Robinson J, Thomas O, Deanfield JE. Non-invasive measurement of human endothelium dependent arterial responses: accuracy and reproducibility. Br Heart J 1995;74:247-253.
22. Falk E. Pathogenesis of atherosclerosis. J Am Coll Cardiol 2006;47(8 Suppl):C7-12.
23. Bis JC, Kavousi M, Franceschini N, Isaacs A, Abecasis GR, Schminke U, et al. Meta-analysis of genome-wide association studies from the CHARGE consortium identifies common variants associated with carotid intima media thickness and plaque. Nat Genet 2011;43(10):940-947.
24. Lorenz MW, Markus HS, Bots ML, Rosvall M, Sitzer M. Prediction of clinical cardiovascular events with carotid intima-media thickness: a systematic review and meta-analysis. Circulation 2007;115:459-467.
25. Melton PE, Carless MA, Curran JE, Dyer TD, Göring HH, Kent JW Jr, Drigalenko E, Johnson MP, Maccluer JW, Moses EK, Comuzzie AG, Mahaney MC, O'Leary DH, Blangero J, Almasy L. Genetic architecture of carotid artery intima-media thickness in Mexican Americans. Circ Cardiovasc Genet 2013;6:211-221.
26. Nambi V, Chambless L, Folsom AR, He M, Hu Y, Mosley T, Volcik K, Boerwinkle E, Ballantyne CM. Carotid intima-media thickness and presence or absence of plaque improves prediction of coronary heart disease risk: the ARIC (Atherosclerosis Risk In Communities) study. J Am Coll Cardiol 2010;55:1600-1607.
27. Meyer AA, Joharchi MS, Kundt G, Schuff-Werner P, Steinhoff G, Kienast W. Predicting the risk of early atherosclerotic disease development in children after repair of aortic coarctation. Eur Heart J 2005;26:617-622.
28. Ayer JG, Harmer JA, Nakhla S, Xuan W, Ng MK, Raitakari OT, Marks GB, Celermajer DS. HDL-cholesterol, blood pressure, and asymmetric dimethylarginine are significantly associated with arterial wall thickness in children. Arterioscler Thromb Vasc Biol 2009;29:943-949.
29. Reiner B, Oberhoffer R, Häcker AL, Ewert P, Müller J. Carotid Intima-Media Thickness in Children and Adolescents With Congenital Heart Disease. Can J Cardiol 2018;34:1618-1623.
30. El-Melegy NT, Mohamed NA. Angiogenic biomarkers in children with congenital heart disease: possible implications. Ital J Pediatr 2010;36:32.
31. Celletti FL, Waugh JM, Amabile PG, Brendolan A, Hilfiker PR, Dake MD. Vascular endothelial growth factor enhances atherosclerotic plaque progression. Nat Med 2001;7:425-429.
32. Yin HL, Luo CW, Dai ZK, Shaw KP, Chai CY, Wu CC. Hypoxia-inducible factor-1α, vascular endothelial growth factor, inducible nitric oxide synthase, and endothelin-1 expression correlates with angiogenesis in congenital heart disease. Kaohsiung J Med Sci 2016;32:348-55.
33. Nassef YE, Hamed MA, Aly HF. Inflammatory cytokines, apoptotic, tissue injury and remodeling biomarkers in children with congenital heart disease. Indian J Clin Biochem 2014;29:145-149.
34. Mayyas F, Niebauer M, Zurick A, Barnard J, Gillinov AM, Chung MK, Van Wagoner DR. Association of left atrial endothelin-1 with atrial rhythm, size, and fibrosis in patients with structural heart disease. Circ Arrhythm Electrophysiol 2010;3:369-379.
35. Tarp JB, Sørgaard MH, Christoffersen C, Jensen AS, Sillesen H, Celermajer D, Eriksson P, Estensen ME, Nagy E, Holstein-Rathlou NH, Engstrøm T, Søndergaard L. Subclinical atherosclerosis in patients with cyanotic congenital heart disease. Int J Cardiol 2019;277:97-103.
36. Joannides R, Haefeli WE, Linder L, Richard V, Bakkali EH, Thuillez C, Lüscher TF. Nitric oxide is responsible for flow-dependent dilatation of human peripheral conduit arteries in vivo. Circulation 1995;91:1314-1319.
37. Takase B, Uehata A, Akima T, Nagai T, Nishioka T, Hamabe A, Satomura K, Ohsuzu F, Kurita A. Endothelium-dependent flow-mediated vasodilation in coronary and brachial arteries in suspected coronary artery disease. Am J Cardiol 1998;82:1535-1539, A7-8.
38. Liao Y, Chen S, Liu X, Zhang Q, Ai Y, Wang Y, Jin H, Tang C, Du J. Flow-mediated vasodilation and endothelium function in children with postural orthostatic tachycardia syndrome. Am J Cardiol 2010;106:378-382.
39. Trojnarska O, Szczepaniak-Chicheł L, Gabriel M, Bartczak-Rutkowska A, Rupa-Matysek J, Tykarski A, Grajek S. Arterial stiffness and arterial function in adult cyanotic patients with congenital heart disease. J Cardiol 2017;70:62-67.
40. Cordina RL, Nakhla S, O'Meagher S, Leaney J, Graham S, Celermajer DS. Widespread endotheliopathy in adults with cyanotic congenital heart disease. Cardiol Young 2015;25:511-519.
41. Ciftel M, Simşek A, Turan O, Kardelen F, Akçurin G, Ertuğ H. Endothelial dysfunction and atherosclerosis in children with irreversible pulmonary hypertension due to congenital heart disease. Ann Pediatr Cardiol 2012;5:160-164.
2. Candelino M, Tagi VM, Chiarelli F. Cardiovascular risk in children: a burden for future generations. Ital J Pediatr 2022;48:57.
3. Naqvi TZ, Lee MS. Carotid intima-media thickness and plaque in cardiovascular risk assessment. JACC Cardiovasc Imaging 2014;7:1025-1038.
4. Greenland P, LaBree L, Azen SP, Doherty TM, Detrano RC. Coronary artery calcium score combined with Framingham score for risk prediction in asymptomatic individuals. JAMA 2004;291:210-215.
5. Sabri MR, Tavana EN, Ahmadi A, Gheissari A. Effect of vitamin C on endothelial function of children with chronic renal failure: An experimental study. Adv Biomed Res 2015;4:260.
6. Dalla Pozza R, Ehringer-Schetitska D, Fritsch P, Jokinen E, Petropoulos A, Oberhoffer R; Association for European Paediatric Cardiology Working Group Cardiovascular Prevention. Intima media thickness measurement in children: A statement from the Association for European Paediatric Cardiology (AEPC) Working Group on Cardiovascular Prevention endorsed by the Association for European Paediatric Cardiology. Atherosclerosis 2015;238:380-387.
7. Rohit M, Shrivastava S. Acyanotic and Cyanotic Congenital Heart Diseases. Indian J Pediatr 2018;85:454-460.
8. Moller JH, Hoffman J IE, Benson DW, Van Hare GF, Wren C, eds. Pediatric Cardiovascular Medicine. 7th ed. Pondicherry: Wiley-Blackwell; 2012. p. 23–32.
9. Hoffman JI, Kaplan S. The incidence of congenital heart disease. J Am Coll Cardiol 2002;39:1890-900.
10. Ahmadi AR, Sabri MR, Navabi ZS, Ghaderian M, Dehghan B, Mahdavi C, Khodarahmi S. Early Results of the Persian Registry of Cardiovascular Disease/Congenital Heart Disease (PROVE/CHD) in Isfahan. J Tehran Heart Cent 2020;15:158-164.
11. Khasawneh W, Hakim F, Abu Ras O, Hejazi Y, Abu-Aqoulah A. Incidence and Patterns of Congenital Heart Disease Among Jordanian Infants, a Cohort Study From a University Tertiary Center. Front Pediatr 2020;8:219.
12. Wallooppillai NJ, Jayasinghe Mde S. Congenital heart disease in Ceylon. Br Heart J 1970;32:304-306.
13. van der Linde D, Konings EE, Slager MA, Witsenburg M, Helbing WA, Takkenberg JJ, Roos-Hesselink JW. Birth prevalence of congenital heart disease worldwide: a systematic review and meta-analysis. J Am Coll Cardiol 2011;58:2241-2247.
14. Ross R. Atherosclerosis--an inflammatory disease. N Engl J Med 1999;340:115-126.
15. Celermajer DS, Sorensen KE, Gooch VM, Spiegelhalter DJ, Miller OI, Sullivan ID, Lloyd JK, Deanfield JE. Non-invasive detection of endothelial dysfunction in children and adults at risk of atherosclerosis. Lancet 1992;340:1111-1115.
16. Sabri MR, Tavana EN, Ahmadi A, Hashemipour M. The effect of vitamin C on endothelial function of children with type 1 diabetes: an experimental study. Int J Prev Med 2014;5:999-1004.
17. Raitakari OT, Juonala M, Kähönen M, Taittonen L, Laitinen T, Mäki-Torkko N, Järvisalo MJ, Uhari M, Jokinen E, Rönnemaa T, Akerblom HK, Viikari JS. Cardiovascular risk factors in childhood and carotid artery intima-media thickness in adulthood: the Cardiovascular Risk in Young Finns Study. JAMA 2003;290:2277-2283.
18. Burke GL, Evans GW, Riley WA, Sharrett AR, Howard G, Barnes RW, Rosamond W, Crow RS, Rautaharju PM, Heiss G. Arterial wall thickness is associated with prevalent cardiovascular disease in middle-aged adults. The Atherosclerosis Risk in Communities (ARIC) Study. Stroke 1995;26:386-391.
19. Brunner H, Cockcroft JR, Deanfield J, Donald A, Ferrannini E, Halcox J, Kiowski W, Lüscher TF, Mancia G, Natali A, Oliver JJ, Pessina AC, Rizzoni D, Rossi GP, Salvetti A, Spieker LE, Taddei S, Webb DJ; Working Group on Endothelins and Endothelial Factors of the European Society of Hypertension. Endothelial function and dysfunction. Part II: Association with cardiovascular risk factors and diseases. A statement by the Working Group on Endothelins and Endothelial Factors of the European Society of Hypertension. J Hypertens 2005;23:233-246.
20. Sabri MR, Tavana EN, Ahmadi A, Mostafavy N. Does Vitamin C improve endothelial function in patients with Kawasaki disease? J Res Med Sci 2015;20:32-36.
21. Sorensen KE, Celermajer DS, Spiegelhalter DJ, Georgakopoulos D, Robinson J, Thomas O, Deanfield JE. Non-invasive measurement of human endothelium dependent arterial responses: accuracy and reproducibility. Br Heart J 1995;74:247-253.
22. Falk E. Pathogenesis of atherosclerosis. J Am Coll Cardiol 2006;47(8 Suppl):C7-12.
23. Bis JC, Kavousi M, Franceschini N, Isaacs A, Abecasis GR, Schminke U, et al. Meta-analysis of genome-wide association studies from the CHARGE consortium identifies common variants associated with carotid intima media thickness and plaque. Nat Genet 2011;43(10):940-947.
24. Lorenz MW, Markus HS, Bots ML, Rosvall M, Sitzer M. Prediction of clinical cardiovascular events with carotid intima-media thickness: a systematic review and meta-analysis. Circulation 2007;115:459-467.
25. Melton PE, Carless MA, Curran JE, Dyer TD, Göring HH, Kent JW Jr, Drigalenko E, Johnson MP, Maccluer JW, Moses EK, Comuzzie AG, Mahaney MC, O'Leary DH, Blangero J, Almasy L. Genetic architecture of carotid artery intima-media thickness in Mexican Americans. Circ Cardiovasc Genet 2013;6:211-221.
26. Nambi V, Chambless L, Folsom AR, He M, Hu Y, Mosley T, Volcik K, Boerwinkle E, Ballantyne CM. Carotid intima-media thickness and presence or absence of plaque improves prediction of coronary heart disease risk: the ARIC (Atherosclerosis Risk In Communities) study. J Am Coll Cardiol 2010;55:1600-1607.
27. Meyer AA, Joharchi MS, Kundt G, Schuff-Werner P, Steinhoff G, Kienast W. Predicting the risk of early atherosclerotic disease development in children after repair of aortic coarctation. Eur Heart J 2005;26:617-622.
28. Ayer JG, Harmer JA, Nakhla S, Xuan W, Ng MK, Raitakari OT, Marks GB, Celermajer DS. HDL-cholesterol, blood pressure, and asymmetric dimethylarginine are significantly associated with arterial wall thickness in children. Arterioscler Thromb Vasc Biol 2009;29:943-949.
29. Reiner B, Oberhoffer R, Häcker AL, Ewert P, Müller J. Carotid Intima-Media Thickness in Children and Adolescents With Congenital Heart Disease. Can J Cardiol 2018;34:1618-1623.
30. El-Melegy NT, Mohamed NA. Angiogenic biomarkers in children with congenital heart disease: possible implications. Ital J Pediatr 2010;36:32.
31. Celletti FL, Waugh JM, Amabile PG, Brendolan A, Hilfiker PR, Dake MD. Vascular endothelial growth factor enhances atherosclerotic plaque progression. Nat Med 2001;7:425-429.
32. Yin HL, Luo CW, Dai ZK, Shaw KP, Chai CY, Wu CC. Hypoxia-inducible factor-1α, vascular endothelial growth factor, inducible nitric oxide synthase, and endothelin-1 expression correlates with angiogenesis in congenital heart disease. Kaohsiung J Med Sci 2016;32:348-55.
33. Nassef YE, Hamed MA, Aly HF. Inflammatory cytokines, apoptotic, tissue injury and remodeling biomarkers in children with congenital heart disease. Indian J Clin Biochem 2014;29:145-149.
34. Mayyas F, Niebauer M, Zurick A, Barnard J, Gillinov AM, Chung MK, Van Wagoner DR. Association of left atrial endothelin-1 with atrial rhythm, size, and fibrosis in patients with structural heart disease. Circ Arrhythm Electrophysiol 2010;3:369-379.
35. Tarp JB, Sørgaard MH, Christoffersen C, Jensen AS, Sillesen H, Celermajer D, Eriksson P, Estensen ME, Nagy E, Holstein-Rathlou NH, Engstrøm T, Søndergaard L. Subclinical atherosclerosis in patients with cyanotic congenital heart disease. Int J Cardiol 2019;277:97-103.
36. Joannides R, Haefeli WE, Linder L, Richard V, Bakkali EH, Thuillez C, Lüscher TF. Nitric oxide is responsible for flow-dependent dilatation of human peripheral conduit arteries in vivo. Circulation 1995;91:1314-1319.
37. Takase B, Uehata A, Akima T, Nagai T, Nishioka T, Hamabe A, Satomura K, Ohsuzu F, Kurita A. Endothelium-dependent flow-mediated vasodilation in coronary and brachial arteries in suspected coronary artery disease. Am J Cardiol 1998;82:1535-1539, A7-8.
38. Liao Y, Chen S, Liu X, Zhang Q, Ai Y, Wang Y, Jin H, Tang C, Du J. Flow-mediated vasodilation and endothelium function in children with postural orthostatic tachycardia syndrome. Am J Cardiol 2010;106:378-382.
39. Trojnarska O, Szczepaniak-Chicheł L, Gabriel M, Bartczak-Rutkowska A, Rupa-Matysek J, Tykarski A, Grajek S. Arterial stiffness and arterial function in adult cyanotic patients with congenital heart disease. J Cardiol 2017;70:62-67.
40. Cordina RL, Nakhla S, O'Meagher S, Leaney J, Graham S, Celermajer DS. Widespread endotheliopathy in adults with cyanotic congenital heart disease. Cardiol Young 2015;25:511-519.
41. Ciftel M, Simşek A, Turan O, Kardelen F, Akçurin G, Ertuğ H. Endothelial dysfunction and atherosclerosis in children with irreversible pulmonary hypertension due to congenital heart disease. Ann Pediatr Cardiol 2012;5:160-164.
| Files | ||
| Issue | Vol 18 No 4 (2023): J Teh Univ Heart Ctr | |
| Section | Original Article(s) | |
| DOI | https://doi.org/10.18502/jthc.v18i4.14824 | |
| Keywords | ||
| Heart defects Congenital Vasodilatation Carotid intima-media thickness Atherosclerosis | ||
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How to Cite
1.
Ahmadi A, Ghaderian M, Nourmohammadi H, Sabri MR, Dehghan B, Mahdavi C. Comparison of CIMT and FMD in the Brachial Artery Between Children With Acyanotic Congenital Heart Disease and Healthy Controls: A Case-Control Study. J Tehran Heart Cent. 2023;18(4):256-260.
