Skip to main content
Top
Published in: Heart and Vessels 1/2013

01-01-2013 | Original Article

Assessment of vascular remodeling after the Fontan procedure using a novel very high resolution ultrasound method: arterial wall thinning and venous thickening in late follow-up

Authors: Taisto Sarkola, Edgar Jaeggi, Cameron Slorach, Wei Hui, Timothy Bradley, Andrew N. Redington

Published in: Heart and Vessels | Issue 1/2013

Login to get access

Abstract

The Fontan circulation is associated with an increased central venous pressure, decreased ventricular preload, and increased afterload. We postulated that these central hemodynamic abnormalities would have consequences for the structural and functional properties of the peripheral arteries and veins, and performed a cross-sectional study in a tertiary health-care setting. We prospectively examined venous and arterial wall morphology by very high resolution ultrasound (VHRU, 25–55 MHz), and function by conventional vascular ultrasound (flow-mediated dilatation, FMD) and applanation tonometry (pulse wave velocity, PWV) in 28 patients after the Fontan procedure (age 14.8 ± 1.3 years) and 54 age-matched controls. Pig venous samples were studied with VHRU and compared with histology for accuracy. The precision of the venous VHRU method was studied in healthy volunteers. The lumen dimension was reduced in Fontans compared with controls in the common carotid, brachial, radial, and femoral arteries (p < 0.05). The common carotid, brachial, radial, ulnar, femoral, and dorsal tibial artery intima-media thicknesses (IMTs) and the brachial, ulnar, and femoral artery adventitial thicknesses were decreased (p < 0.05 for all), while the cubital and dorsal tibial vein IMTs were increased in Fontans (p < 0.001). FMD, abdominal aortic stiffness, and carotid-femoral PWV were similar, while carotid-radial artery PWV was increased in Fontans (p < 0.01). Venous wall layer assessment with VHRU was accurate and precise. The Fontan circulation is associated with significant arterial and venous remodeling, presumably reflecting abnormalities of central hemodynamics. These novel data may be of clinical importance in the circulatory management as well as the understanding of the early pathogenesis of vasculopathy in patients after the Fontan procedure.
Appendix
Available only for authorised users
Literature
2.
go back to reference de Leval MR, Kilner P, Gewillig M, Bull C (1988) Total cavopulmonary connection: a logical alternative to atriopulmonary connection for complex Fontan operations. Experimental studies and early clinical experience. J Thorac Cardiovasc Surg 96:682–695PubMed de Leval MR, Kilner P, Gewillig M, Bull C (1988) Total cavopulmonary connection: a logical alternative to atriopulmonary connection for complex Fontan operations. Experimental studies and early clinical experience. J Thorac Cardiovasc Surg 96:682–695PubMed
3.
go back to reference Bridges ND, Lock JE, Castaneda AR (1990) Baffle fenestration with subsequent transcatheter closure. Modification of the Fontan operation for patients at increased risk. Circulation 82:1681–1689PubMedCrossRef Bridges ND, Lock JE, Castaneda AR (1990) Baffle fenestration with subsequent transcatheter closure. Modification of the Fontan operation for patients at increased risk. Circulation 82:1681–1689PubMedCrossRef
4.
go back to reference Black MD, van Son JA, Haas GS (1995) Extracardiac Fontan operation with adjustable communication. Ann Thorac Surg 60:716–718PubMedCrossRef Black MD, van Son JA, Haas GS (1995) Extracardiac Fontan operation with adjustable communication. Ann Thorac Surg 60:716–718PubMedCrossRef
5.
go back to reference Khairy P, Fernandes SM, Mayer JE Jr, Triedman JK, Walsh EP, Lock JE, Landzberg MJ (2008) Long-term survival, modes of death, and predictors of mortality in patients with Fontan surgery. Circulation 117:85–92PubMedCrossRef Khairy P, Fernandes SM, Mayer JE Jr, Triedman JK, Walsh EP, Lock JE, Landzberg MJ (2008) Long-term survival, modes of death, and predictors of mortality in patients with Fontan surgery. Circulation 117:85–92PubMedCrossRef
6.
go back to reference Shachar GB, Fuhrman BP, Wang Y, Lucas RV Jr, Lock JE (1982) Rest and exercise hemodynamics after the Fontan procedure. Circulation 65:1043–1048PubMedCrossRef Shachar GB, Fuhrman BP, Wang Y, Lucas RV Jr, Lock JE (1982) Rest and exercise hemodynamics after the Fontan procedure. Circulation 65:1043–1048PubMedCrossRef
7.
go back to reference Olivier M, O’Leary PW, Pankratz VS, Lohse CM, Walsh BE, Tajik AJ, Seward JB (2003) Serial Doppler assessment of diastolic function before and after the Fontan operation. J Am Soc Echocardiogr 16:1136–1143 Olivier M, O’Leary PW, Pankratz VS, Lohse CM, Walsh BE, Tajik AJ, Seward JB (2003) Serial Doppler assessment of diastolic function before and after the Fontan operation. J Am Soc Echocardiogr 16:1136–1143
8.
go back to reference Krishnan US, Taneja I, Gewitz M, Young R, Stewart J (2009) Peripheral vascular adaptation and orthostatic tolerance in Fontan physiology. Circulation 120:1775–1783PubMedCrossRef Krishnan US, Taneja I, Gewitz M, Young R, Stewart J (2009) Peripheral vascular adaptation and orthostatic tolerance in Fontan physiology. Circulation 120:1775–1783PubMedCrossRef
9.
go back to reference Senzaki H, Masutani S, Ishido H, Taketazu M, Kobayashi T, Sasaki N, Asano H, Katogi T, Kyo S, Yokote Y (2006) Cardiac rest and reserve function in patients with Fontan circulation. J Am Coll Cardiol 47:2528–2535PubMedCrossRef Senzaki H, Masutani S, Ishido H, Taketazu M, Kobayashi T, Sasaki N, Asano H, Katogi T, Kyo S, Yokote Y (2006) Cardiac rest and reserve function in patients with Fontan circulation. J Am Coll Cardiol 47:2528–2535PubMedCrossRef
10.
go back to reference Valente AM, Bhatt AB, Cook S, Earing MG, Gersony DR, Aboulhosn J, Opotowsky AR, Lui G, Gurvitz M, Graham D, Fernandes SM, Khairy P, Webb G, Gerhard-Herman M, Landzberg MJ, AARCC (Alliance for Adult Research in Congenital Cardiology) Investigators (2010) The CALF (Congenital Heart Disease in Adults Lower Extremity Systemic Venous Health in Fontan Patients) study. J Am Coll Cardiol 56:144–150 Valente AM, Bhatt AB, Cook S, Earing MG, Gersony DR, Aboulhosn J, Opotowsky AR, Lui G, Gurvitz M, Graham D, Fernandes SM, Khairy P, Webb G, Gerhard-Herman M, Landzberg MJ, AARCC (Alliance for Adult Research in Congenital Cardiology) Investigators (2010) The CALF (Congenital Heart Disease in Adults Lower Extremity Systemic Venous Health in Fontan Patients) study. J Am Coll Cardiol 56:144–150
11.
go back to reference Kiesewetter CH, Sheron N, Vettukattill JJ, Hacking N, Stedman B, Millward-Sadler H, Haw M, Cope R, Salmon AP, Sivaprakasam MC, Kendall T, Keeton BR, Iredale JP, Veldtman GR (2007) Hepatic changes in the failing Fontan circulation. Heart 93:579–584PubMedCrossRef Kiesewetter CH, Sheron N, Vettukattill JJ, Hacking N, Stedman B, Millward-Sadler H, Haw M, Cope R, Salmon AP, Sivaprakasam MC, Kendall T, Keeton BR, Iredale JP, Veldtman GR (2007) Hepatic changes in the failing Fontan circulation. Heart 93:579–584PubMedCrossRef
12.
go back to reference Mertens L, Hagler DJ, Sauer U, Somerville J, Gewillig M (1998) Protein-losing enteropathy after the Fontan operation: an international multicenter study. PLE study group. J Thorac Cardiovasc Surg 115:1063–1073PubMedCrossRef Mertens L, Hagler DJ, Sauer U, Somerville J, Gewillig M (1998) Protein-losing enteropathy after the Fontan operation: an international multicenter study. PLE study group. J Thorac Cardiovasc Surg 115:1063–1073PubMedCrossRef
13.
go back to reference Costello JM, Steinhorn D, McColley S, Gerber ME, Kumar SP (2002) Treatment of plastic bronchitis in a Fontan patient with tissue plasminogen activator: a case report and review of the literature. Pediatrics 109:e67PubMedCrossRef Costello JM, Steinhorn D, McColley S, Gerber ME, Kumar SP (2002) Treatment of plastic bronchitis in a Fontan patient with tissue plasminogen activator: a case report and review of the literature. Pediatrics 109:e67PubMedCrossRef
14.
go back to reference Jin SM, Noh CI, Bae EJ, Choi JY, Yun YS (2007) Impaired vascular function in patients with Fontan circulation. Int J Cardiol 120:221–226PubMedCrossRef Jin SM, Noh CI, Bae EJ, Choi JY, Yun YS (2007) Impaired vascular function in patients with Fontan circulation. Int J Cardiol 120:221–226PubMedCrossRef
15.
go back to reference Mahle WT, Todd K, Fyfe DA (2003) Endothelial function following the Fontan operation. Am J Cardiol 91:1286–1288PubMedCrossRef Mahle WT, Todd K, Fyfe DA (2003) Endothelial function following the Fontan operation. Am J Cardiol 91:1286–1288PubMedCrossRef
16.
go back to reference Inai K, Saita Y, Takeda S, Nakazawa M, Kimura H (2004) Skeletal muscle hemodynamics and endothelial function in patients after Fontan operation. Am J Cardiol 93:792–797PubMedCrossRef Inai K, Saita Y, Takeda S, Nakazawa M, Kimura H (2004) Skeletal muscle hemodynamics and endothelial function in patients after Fontan operation. Am J Cardiol 93:792–797PubMedCrossRef
17.
go back to reference Sarkola T, Redington AN, Keeley F, Bradley T, Jaeggi E (2010) Transcutaneous very high resolution ultrasound to quantify arterial wall layers of muscular and elastic arteries: validation of a method. Atherosclerosis 212:516–523PubMedCrossRef Sarkola T, Redington AN, Keeley F, Bradley T, Jaeggi E (2010) Transcutaneous very high resolution ultrasound to quantify arterial wall layers of muscular and elastic arteries: validation of a method. Atherosclerosis 212:516–523PubMedCrossRef
18.
go back to reference Sarkola T, Redington AN, Slorach C, Hui W, Bradley T, Jaeggi E (2011) Assessment of vascular phenotype using a novel very-high resolution ultrasound technique in adolescents after aortic coarctation repair and/or stent implantation: relationship to central hemodynamics and left ventricular mass. Heart 97:1788–1793PubMedCrossRef Sarkola T, Redington AN, Slorach C, Hui W, Bradley T, Jaeggi E (2011) Assessment of vascular phenotype using a novel very-high resolution ultrasound technique in adolescents after aortic coarctation repair and/or stent implantation: relationship to central hemodynamics and left ventricular mass. Heart 97:1788–1793PubMedCrossRef
19.
go back to reference Sarkola T, Abadilla AA, Chahal N, Jaeggi E, McCrindle BW (2011) Feasibility of very-high resolution ultrasound to assess elastic and muscular arterial wall morphology in adolescents attending an outpatient clinic for obesity and lipid abnormalities. Atherosclerosis 219(2):610–615PubMedCrossRef Sarkola T, Abadilla AA, Chahal N, Jaeggi E, McCrindle BW (2011) Feasibility of very-high resolution ultrasound to assess elastic and muscular arterial wall morphology in adolescents attending an outpatient clinic for obesity and lipid abnormalities. Atherosclerosis 219(2):610–615PubMedCrossRef
20.
go back to reference Pickering TG, Hall JE, Appel LJ, Falkner BE, Graves J, Hill MN, Jones DW, Kurtz T, Sheps SG, Roccella EJ, Subcommittee of Professional, Public Education of the American Heart Association Council on High Blood Pressure Research (2005) Recommendations for blood pressure measurement in humans and experimental animals: part 1: blood pressure measurement in humans: a statement for professionals from the Subcommittee of Professional and Public Education of the American Heart Association Council on High Blood Pressure Research. Hypertension 45:142–161PubMed Pickering TG, Hall JE, Appel LJ, Falkner BE, Graves J, Hill MN, Jones DW, Kurtz T, Sheps SG, Roccella EJ, Subcommittee of Professional, Public Education of the American Heart Association Council on High Blood Pressure Research (2005) Recommendations for blood pressure measurement in humans and experimental animals: part 1: blood pressure measurement in humans: a statement for professionals from the Subcommittee of Professional and Public Education of the American Heart Association Council on High Blood Pressure Research. Hypertension 45:142–161PubMed
21.
go back to reference Willard JE, Netto D, Demian SE, Haagen DR, Brickner ME, Eichhorn EJ, Grayburn PA (1992) Intravascular ultrasound imaging of saphenous vein grafts in vitro: comparison with histologic and quantitative angiographic findings. J Am Coll Cardiol 19:759–764PubMedCrossRef Willard JE, Netto D, Demian SE, Haagen DR, Brickner ME, Eichhorn EJ, Grayburn PA (1992) Intravascular ultrasound imaging of saphenous vein grafts in vitro: comparison with histologic and quantitative angiographic findings. J Am Coll Cardiol 19:759–764PubMedCrossRef
22.
go back to reference Hong MK, Mintz GS, Hong MK, Abizaid AS, Pichard AD, Satler LF, Kent KM, Leon MB (1999) Intravascular ultrasound assessment of the presence of vascular remodeling in diseased human saphenous vein bypass grafts. Am J Cardiol 84:992–998PubMedCrossRef Hong MK, Mintz GS, Hong MK, Abizaid AS, Pichard AD, Satler LF, Kent KM, Leon MB (1999) Intravascular ultrasound assessment of the presence of vascular remodeling in diseased human saphenous vein bypass grafts. Am J Cardiol 84:992–998PubMedCrossRef
23.
go back to reference Hirai T, Sasayama S, Kawasaki T, Yagi S (1989) Stiffness of systemic arteries in patients with myocardial infarction. A noninvasive method to predict severity of coronary atherosclerosis. Circulation 80:78–86PubMedCrossRef Hirai T, Sasayama S, Kawasaki T, Yagi S (1989) Stiffness of systemic arteries in patients with myocardial infarction. A noninvasive method to predict severity of coronary atherosclerosis. Circulation 80:78–86PubMedCrossRef
24.
go back to reference Vogt M, Kühn A, Baumgartner D, Baumgartner C, Busch R, Kostolny M, Hess J (2005) Impaired elastic properties of the ascending aorta in newborns before and early after successful coarctation repair: proof of a systemic vascular disease of the prestenotic arteries? Circulation 111:3269–3273PubMedCrossRef Vogt M, Kühn A, Baumgartner D, Baumgartner C, Busch R, Kostolny M, Hess J (2005) Impaired elastic properties of the ascending aorta in newborns before and early after successful coarctation repair: proof of a systemic vascular disease of the prestenotic arteries? Circulation 111:3269–3273PubMedCrossRef
25.
go back to reference Bramwell JC, Hill AV (1922) Velocity of transmission of the pulse wave and elasticity of the arteries. Lancet 1:891–892CrossRef Bramwell JC, Hill AV (1922) Velocity of transmission of the pulse wave and elasticity of the arteries. Lancet 1:891–892CrossRef
26.
go back to reference Rajzer MW, Wojciechowska W, Klocek M, Palka I, Brzozowska-Kiszka M, Kawecka-Jaszcz K (2008) Comparison of aortic pulse wave velocity measured by three techniques: Complior, SphygmoCor and Arteriograph. J Hypertens 26:2001–2007PubMedCrossRef Rajzer MW, Wojciechowska W, Klocek M, Palka I, Brzozowska-Kiszka M, Kawecka-Jaszcz K (2008) Comparison of aortic pulse wave velocity measured by three techniques: Complior, SphygmoCor and Arteriograph. J Hypertens 26:2001–2007PubMedCrossRef
27.
go back to reference Wilkinson IB, Fuchs SA, Jansen IM, Spratt JC, Murray GD, Cockcroft JR, Webb DJ (1998) Reproducibility of pulse wave velocity and augmentation index measured by pulse wave analysis. J Hypertens 16:2079–2084PubMedCrossRef Wilkinson IB, Fuchs SA, Jansen IM, Spratt JC, Murray GD, Cockcroft JR, Webb DJ (1998) Reproducibility of pulse wave velocity and augmentation index measured by pulse wave analysis. J Hypertens 16:2079–2084PubMedCrossRef
28.
go back to reference Celermajer DS, Sorensen KE, Gooch VM, Spiegelhalter DJ, Miller OI, Sullivan ID, Lloyd JK, Deanfield JE (1992) Non-invasive detection of endothelial dysfunction in children and adults at risk of atherosclerosis. Lancet 340:1111–1115PubMedCrossRef Celermajer DS, Sorensen KE, Gooch VM, Spiegelhalter DJ, Miller OI, Sullivan ID, Lloyd JK, Deanfield JE (1992) Non-invasive detection of endothelial dysfunction in children and adults at risk of atherosclerosis. Lancet 340:1111–1115PubMedCrossRef
29.
go back to reference Kuczmarski RJ, Ogden CL, Guo SS, Grummer-Strawn LM, Flegal KM, Mei Z, Wei R, Curtin LR, Roche AF, Johnson CL (2002) 2000 CDC Growth Charts for the United States: methods and development. National Center for Health Statistics. Vital Health Stat 11(246). http://www.cdc.gov/growthcharts/. Accessed 1 Sept 2010 Kuczmarski RJ, Ogden CL, Guo SS, Grummer-Strawn LM, Flegal KM, Mei Z, Wei R, Curtin LR, Roche AF, Johnson CL (2002) 2000 CDC Growth Charts for the United States: methods and development. National Center for Health Statistics. Vital Health Stat 11(246). http://​www.​cdc.​gov/​growthcharts/​. Accessed 1 Sept 2010
30.
go back to reference Bland JM, Altman DG (1986) Statistical methods for assessing agreement between two methods of clinical measurement. Lancet 1:307–310PubMedCrossRef Bland JM, Altman DG (1986) Statistical methods for assessing agreement between two methods of clinical measurement. Lancet 1:307–310PubMedCrossRef
31.
go back to reference McCrindle BW, Williams RV, Mitchell PD, Hsu DT, Paridon SM, Atz AM, Li JS, Newburger JW, Pediatric Heart Network Investigators (2006) Relationship of patient and medical characteristics to health status in children and adolescents after the Fontan procedure. Circulation 113:1123–1129PubMedCrossRef McCrindle BW, Williams RV, Mitchell PD, Hsu DT, Paridon SM, Atz AM, Li JS, Newburger JW, Pediatric Heart Network Investigators (2006) Relationship of patient and medical characteristics to health status in children and adolescents after the Fontan procedure. Circulation 113:1123–1129PubMedCrossRef
32.
go back to reference László A, Pintér A, Horváth T, Kádár K, Temesvári A, Kollai M, Studinger P (2011) Impaired carotid artery elastic function in patients with tetralogy of Fallot. Heart Vessels 26:542–548PubMedCrossRef László A, Pintér A, Horváth T, Kádár K, Temesvári A, Kollai M, Studinger P (2011) Impaired carotid artery elastic function in patients with tetralogy of Fallot. Heart Vessels 26:542–548PubMedCrossRef
33.
go back to reference Järvisalo MJ, Rönnemaa T, Volanen I, Kaitosaari T, Kallio K, Hartiala JJ, Irjala K, Viikari JS, Simell O, Raitakari OT (2002) Brachial artery dilatation responses in healthy children and adolescents. Am J Physiol Heart Circ Physiol 282:H87–H92PubMed Järvisalo MJ, Rönnemaa T, Volanen I, Kaitosaari T, Kallio K, Hartiala JJ, Irjala K, Viikari JS, Simell O, Raitakari OT (2002) Brachial artery dilatation responses in healthy children and adolescents. Am J Physiol Heart Circ Physiol 282:H87–H92PubMed
34.
go back to reference Nerla R, Di Monaco A, Sestito A, Lamendola P, Di Stasio E, Romitelli F, Lanza GA, Crea F (2011) Transient endothelial dysfunction following flow-mediated dilation assessment. Heart Vessels 26:524–529PubMedCrossRef Nerla R, Di Monaco A, Sestito A, Lamendola P, Di Stasio E, Romitelli F, Lanza GA, Crea F (2011) Transient endothelial dysfunction following flow-mediated dilation assessment. Heart Vessels 26:524–529PubMedCrossRef
Metadata
Title
Assessment of vascular remodeling after the Fontan procedure using a novel very high resolution ultrasound method: arterial wall thinning and venous thickening in late follow-up
Authors
Taisto Sarkola
Edgar Jaeggi
Cameron Slorach
Wei Hui
Timothy Bradley
Andrew N. Redington
Publication date
01-01-2013
Publisher
Springer Japan
Published in
Heart and Vessels / Issue 1/2013
Print ISSN: 0910-8327
Electronic ISSN: 1615-2573
DOI
https://doi.org/10.1007/s00380-011-0217-2

Other articles of this Issue 1/2013

Heart and Vessels 1/2013 Go to the issue