Aortic valve-mediated wall shear stress is heterogeneous and predicts regional aortic elastic fiber thinning in bicuspid aortic valve-associated aortopathy

Emilie Bollache, David G. Guzzardi, Samaneh Sattari, Katherine E. Olsen, Elena S. Di Martino, S Chris Malaisrie, Pim van Ooij, Jeremy D Collins, James Carr, Patrick M McCarthy, Michael Markl, Alex J. Barker, Paul W.M. Fedak*

*Corresponding author for this work

Research output: Contribution to journalArticle

14 Citations (Scopus)

Abstract

Objectives: The objectives of this study were to investigate an association between the magnitude of flow-mediated aortic wall shear stress (WSS) and medial wall histopathology in patients with bicuspid aortic valve (BAV) with aortopathy. Methods: Patients with BAV (n = 27; 52 ± 15 years; 3 women; proximal thoracic aorta diameter = 4.4 ± 0.7 and 4.6 ± 0.5 cm) who underwent prophylactic aortic resection received preoperative 3-dimensional time-resolved phase-contrast magnetic resonance imaging with 3-dimensional velocity encoding to quantify WSS relative to a population of healthy age- and sex-matched tricuspid aortic valve control participants (n = 20). Quantitative histopathology was conducted on BAV aorta tissue samples resected at surgery (n = 93), and correlation was performed between elastic fiber thickness and in vivo aortic WSS as continuous variables. Validation of elastic fiber thickness was achieved by correlation relative to tissue stiffness determined using biaxial biomechanical testing (n = 22 samples). Results: Elastic fibers were thinner and WSS was higher along the greater curvature compared with other circumferential regions (vs anterior wall: P =.003 and P =.0001, respectively; lesser curvature: both P =.001). Increased regional WSS was associated with decreased elastic fiber thickness (r = −0.25; P =.02). Patient stratification with subanalysis showed an increase in the correlation between WSS and histopathology with aortic valve stenosis (r = −0.36; P =.002) and smaller aortic diameters (<4.5 cm: r = −0.39; P =.03). Elastic fiber thinning was associated with circumferential stiffness (r = −0.41; P =.06). Conclusions: For patients with BAV, increased aortic valve-mediated WSS is significantly associated with elastic fiber thinning, particularly with aortic valve stenosis and in earlier stages of aortopathy. Elastic fiber thinning correlates with impaired tissue biomechanics. These novel findings further implicate valve-mediated hemodynamics in the progression of BAV aortopathy.

Original languageEnglish (US)
Pages (from-to)2112-2120.e2
JournalJournal of Thoracic and Cardiovascular Surgery
Volume156
Issue number6
DOIs
StatePublished - Dec 1 2018

Fingerprint

Elastic Tissue
Aortic Valve
Aortic Valve Stenosis
Tricuspid Valve
Bicuspid Aortic Valve
Thoracic Aorta
Biomechanical Phenomena
Aorta
Hemodynamics
Magnetic Resonance Imaging
Population

Keywords

  • 4D flow MRI
  • aortopathy
  • bicuspid aortic valve
  • wall shear stress

ASJC Scopus subject areas

  • Surgery
  • Pulmonary and Respiratory Medicine
  • Cardiology and Cardiovascular Medicine

Cite this

Bollache, Emilie ; Guzzardi, David G. ; Sattari, Samaneh ; Olsen, Katherine E. ; Di Martino, Elena S. ; Malaisrie, S Chris ; van Ooij, Pim ; Collins, Jeremy D ; Carr, James ; McCarthy, Patrick M ; Markl, Michael ; Barker, Alex J. ; Fedak, Paul W.M. / Aortic valve-mediated wall shear stress is heterogeneous and predicts regional aortic elastic fiber thinning in bicuspid aortic valve-associated aortopathy. In: Journal of Thoracic and Cardiovascular Surgery. 2018 ; Vol. 156, No. 6. pp. 2112-2120.e2.
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title = "Aortic valve-mediated wall shear stress is heterogeneous and predicts regional aortic elastic fiber thinning in bicuspid aortic valve-associated aortopathy",
abstract = "Objectives: The objectives of this study were to investigate an association between the magnitude of flow-mediated aortic wall shear stress (WSS) and medial wall histopathology in patients with bicuspid aortic valve (BAV) with aortopathy. Methods: Patients with BAV (n = 27; 52 ± 15 years; 3 women; proximal thoracic aorta diameter = 4.4 ± 0.7 and 4.6 ± 0.5 cm) who underwent prophylactic aortic resection received preoperative 3-dimensional time-resolved phase-contrast magnetic resonance imaging with 3-dimensional velocity encoding to quantify WSS relative to a population of healthy age- and sex-matched tricuspid aortic valve control participants (n = 20). Quantitative histopathology was conducted on BAV aorta tissue samples resected at surgery (n = 93), and correlation was performed between elastic fiber thickness and in vivo aortic WSS as continuous variables. Validation of elastic fiber thickness was achieved by correlation relative to tissue stiffness determined using biaxial biomechanical testing (n = 22 samples). Results: Elastic fibers were thinner and WSS was higher along the greater curvature compared with other circumferential regions (vs anterior wall: P =.003 and P =.0001, respectively; lesser curvature: both P =.001). Increased regional WSS was associated with decreased elastic fiber thickness (r = −0.25; P =.02). Patient stratification with subanalysis showed an increase in the correlation between WSS and histopathology with aortic valve stenosis (r = −0.36; P =.002) and smaller aortic diameters (<4.5 cm: r = −0.39; P =.03). Elastic fiber thinning was associated with circumferential stiffness (r = −0.41; P =.06). Conclusions: For patients with BAV, increased aortic valve-mediated WSS is significantly associated with elastic fiber thinning, particularly with aortic valve stenosis and in earlier stages of aortopathy. Elastic fiber thinning correlates with impaired tissue biomechanics. These novel findings further implicate valve-mediated hemodynamics in the progression of BAV aortopathy.",
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author = "Emilie Bollache and Guzzardi, {David G.} and Samaneh Sattari and Olsen, {Katherine E.} and {Di Martino}, {Elena S.} and Malaisrie, {S Chris} and {van Ooij}, Pim and Collins, {Jeremy D} and James Carr and McCarthy, {Patrick M} and Michael Markl and Barker, {Alex J.} and Fedak, {Paul W.M.}",
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Aortic valve-mediated wall shear stress is heterogeneous and predicts regional aortic elastic fiber thinning in bicuspid aortic valve-associated aortopathy. / Bollache, Emilie; Guzzardi, David G.; Sattari, Samaneh; Olsen, Katherine E.; Di Martino, Elena S.; Malaisrie, S Chris; van Ooij, Pim; Collins, Jeremy D; Carr, James; McCarthy, Patrick M; Markl, Michael; Barker, Alex J.; Fedak, Paul W.M.

In: Journal of Thoracic and Cardiovascular Surgery, Vol. 156, No. 6, 01.12.2018, p. 2112-2120.e2.

Research output: Contribution to journalArticle

TY - JOUR

T1 - Aortic valve-mediated wall shear stress is heterogeneous and predicts regional aortic elastic fiber thinning in bicuspid aortic valve-associated aortopathy

AU - Bollache, Emilie

AU - Guzzardi, David G.

AU - Sattari, Samaneh

AU - Olsen, Katherine E.

AU - Di Martino, Elena S.

AU - Malaisrie, S Chris

AU - van Ooij, Pim

AU - Collins, Jeremy D

AU - Carr, James

AU - McCarthy, Patrick M

AU - Markl, Michael

AU - Barker, Alex J.

AU - Fedak, Paul W.M.

PY - 2018/12/1

Y1 - 2018/12/1

N2 - Objectives: The objectives of this study were to investigate an association between the magnitude of flow-mediated aortic wall shear stress (WSS) and medial wall histopathology in patients with bicuspid aortic valve (BAV) with aortopathy. Methods: Patients with BAV (n = 27; 52 ± 15 years; 3 women; proximal thoracic aorta diameter = 4.4 ± 0.7 and 4.6 ± 0.5 cm) who underwent prophylactic aortic resection received preoperative 3-dimensional time-resolved phase-contrast magnetic resonance imaging with 3-dimensional velocity encoding to quantify WSS relative to a population of healthy age- and sex-matched tricuspid aortic valve control participants (n = 20). Quantitative histopathology was conducted on BAV aorta tissue samples resected at surgery (n = 93), and correlation was performed between elastic fiber thickness and in vivo aortic WSS as continuous variables. Validation of elastic fiber thickness was achieved by correlation relative to tissue stiffness determined using biaxial biomechanical testing (n = 22 samples). Results: Elastic fibers were thinner and WSS was higher along the greater curvature compared with other circumferential regions (vs anterior wall: P =.003 and P =.0001, respectively; lesser curvature: both P =.001). Increased regional WSS was associated with decreased elastic fiber thickness (r = −0.25; P =.02). Patient stratification with subanalysis showed an increase in the correlation between WSS and histopathology with aortic valve stenosis (r = −0.36; P =.002) and smaller aortic diameters (<4.5 cm: r = −0.39; P =.03). Elastic fiber thinning was associated with circumferential stiffness (r = −0.41; P =.06). Conclusions: For patients with BAV, increased aortic valve-mediated WSS is significantly associated with elastic fiber thinning, particularly with aortic valve stenosis and in earlier stages of aortopathy. Elastic fiber thinning correlates with impaired tissue biomechanics. These novel findings further implicate valve-mediated hemodynamics in the progression of BAV aortopathy.

AB - Objectives: The objectives of this study were to investigate an association between the magnitude of flow-mediated aortic wall shear stress (WSS) and medial wall histopathology in patients with bicuspid aortic valve (BAV) with aortopathy. Methods: Patients with BAV (n = 27; 52 ± 15 years; 3 women; proximal thoracic aorta diameter = 4.4 ± 0.7 and 4.6 ± 0.5 cm) who underwent prophylactic aortic resection received preoperative 3-dimensional time-resolved phase-contrast magnetic resonance imaging with 3-dimensional velocity encoding to quantify WSS relative to a population of healthy age- and sex-matched tricuspid aortic valve control participants (n = 20). Quantitative histopathology was conducted on BAV aorta tissue samples resected at surgery (n = 93), and correlation was performed between elastic fiber thickness and in vivo aortic WSS as continuous variables. Validation of elastic fiber thickness was achieved by correlation relative to tissue stiffness determined using biaxial biomechanical testing (n = 22 samples). Results: Elastic fibers were thinner and WSS was higher along the greater curvature compared with other circumferential regions (vs anterior wall: P =.003 and P =.0001, respectively; lesser curvature: both P =.001). Increased regional WSS was associated with decreased elastic fiber thickness (r = −0.25; P =.02). Patient stratification with subanalysis showed an increase in the correlation between WSS and histopathology with aortic valve stenosis (r = −0.36; P =.002) and smaller aortic diameters (<4.5 cm: r = −0.39; P =.03). Elastic fiber thinning was associated with circumferential stiffness (r = −0.41; P =.06). Conclusions: For patients with BAV, increased aortic valve-mediated WSS is significantly associated with elastic fiber thinning, particularly with aortic valve stenosis and in earlier stages of aortopathy. Elastic fiber thinning correlates with impaired tissue biomechanics. These novel findings further implicate valve-mediated hemodynamics in the progression of BAV aortopathy.

KW - 4D flow MRI

KW - aortopathy

KW - bicuspid aortic valve

KW - wall shear stress

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JO - Journal of Thoracic and Cardiovascular Surgery

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