Imaging and modeling of acute pressure-induced changes of collagen and elastin microarchitectures in pig and human resistance arteries

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Resumé

The impact of disease related changes in the extracellular matrix (ECM) on the mechanical properties of human resistance arteries largely remains to be established. Resistance arteries from both pig and human parietal pericardium (PRA) display a different ECM microarchitecture compared to frequently used rodent mesenteric arteries. We hypothesized that the biaxial mechanics of PRA mirror pressure induced changes in the ECM microarchitecture. This was tested using isolated pig PRA as model system, integrating vital imaging, pressure myography and mathematical modeling. Collagenase and elastase digestions were applied to evaluate the loadbearing roles of collagen and elastin, respectively. The incremental elastic modulus linearly related to the straightness of adventitial collagen fibers circumferentially and longitudinally (both R(2)≥0.99), while there was a nonlinear relationship to the internal elastic lamina elastin fiber branching angles. Mathematical modeling suggested a collagen recruitment strain (mean±SEM) of 1.1±0.2 circumferentially and 0.20±0.01 longitudinally, corresponding to a pressure of ~40mmHg, a finding supported by the vital imaging. The integrated method was tested on human PRA to confirm its validity. These showed limited circumferential distensibility and elongation and a collagen recruitment strain of 0.8±0.1 circumferentially and 0.06±0.02 longitudinally, reached at a distending pressure below 20mmHg. This was confirmed by vital imaging showing negligible microarchitectural changes of elastin and collagen upon pressurization. In conclusion, we show for the first time in resistance arteries a quantitative relationship between pressure-induced changes in the extracellular matrix and the arterial wall mechanics. The strength of the integrated methods invites for future detailed studies of microvascular pathologies.

OriginalsprogEngelsk
TidsskriftAmerican Journal of Physiology: Heart and Circulatory Physiology
Vol/bind313
Udgave nummer1
Sider (fra-til)H164–H178
ISSN0363-6135
DOI
StatusUdgivet - 2017

Fingeraftryk

Pericardium
Mechanics
Myography
Adventitia
Elastic Modulus
Weight-Bearing
Collagenases
Rodentia
Pathology

Citer dette

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title = "Imaging and modeling of acute pressure-induced changes of collagen and elastin microarchitectures in pig and human resistance arteries",
abstract = "The impact of disease related changes in the extracellular matrix (ECM) on the mechanical properties of human resistance arteries largely remains to be established. Resistance arteries from both pig and human parietal pericardium (PRA) display a different ECM microarchitecture compared to frequently used rodent mesenteric arteries. We hypothesized that the biaxial mechanics of PRA mirror pressure induced changes in the ECM microarchitecture. This was tested using isolated pig PRA as model system, integrating vital imaging, pressure myography and mathematical modeling. Collagenase and elastase digestions were applied to evaluate the loadbearing roles of collagen and elastin, respectively. The incremental elastic modulus linearly related to the straightness of adventitial collagen fibers circumferentially and longitudinally (both R(2)≥0.99), while there was a nonlinear relationship to the internal elastic lamina elastin fiber branching angles. Mathematical modeling suggested a collagen recruitment strain (mean±SEM) of 1.1±0.2 circumferentially and 0.20±0.01 longitudinally, corresponding to a pressure of ~40mmHg, a finding supported by the vital imaging. The integrated method was tested on human PRA to confirm its validity. These showed limited circumferential distensibility and elongation and a collagen recruitment strain of 0.8±0.1 circumferentially and 0.06±0.02 longitudinally, reached at a distending pressure below 20mmHg. This was confirmed by vital imaging showing negligible microarchitectural changes of elastin and collagen upon pressurization. In conclusion, we show for the first time in resistance arteries a quantitative relationship between pressure-induced changes in the extracellular matrix and the arterial wall mechanics. The strength of the integrated methods invites for future detailed studies of microvascular pathologies.",
keywords = "Journal Article",
author = "Maria Bloksgaard and Leurgans, {Thomas M} and Bart Spronck and Heusinkveld, {Maarten Hg} and Bjarne Thorsted and Kristoffer Rosenstand and Inger Nissen and Hansen, {Ulla Melchior} and Brewer, {Jonathan R} and Bagatolli, {Luis A} and Rasmussen, {Lars M} and Akhmadjon Irmukhamedov and Reesink, {Koen D} and {De Mey}, {Jo G R}",
note = "Copyright {\circledC} 2017, American Journal of Physiology-Heart and Circulatory Physiology.",
year = "2017",
doi = "10.1152/ajpheart.00110.2017",
language = "English",
volume = "313",
pages = "H164–H178",
journal = "American Journal of Physiology: Heart and Circulatory Physiology",
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TY - JOUR

T1 - Imaging and modeling of acute pressure-induced changes of collagen and elastin microarchitectures in pig and human resistance arteries

AU - Bloksgaard, Maria

AU - Leurgans, Thomas M

AU - Spronck, Bart

AU - Heusinkveld, Maarten Hg

AU - Thorsted, Bjarne

AU - Rosenstand, Kristoffer

AU - Nissen, Inger

AU - Hansen, Ulla Melchior

AU - Brewer, Jonathan R

AU - Bagatolli, Luis A

AU - Rasmussen, Lars M

AU - Irmukhamedov, Akhmadjon

AU - Reesink, Koen D

AU - De Mey, Jo G R

N1 - Copyright © 2017, American Journal of Physiology-Heart and Circulatory Physiology.

PY - 2017

Y1 - 2017

N2 - The impact of disease related changes in the extracellular matrix (ECM) on the mechanical properties of human resistance arteries largely remains to be established. Resistance arteries from both pig and human parietal pericardium (PRA) display a different ECM microarchitecture compared to frequently used rodent mesenteric arteries. We hypothesized that the biaxial mechanics of PRA mirror pressure induced changes in the ECM microarchitecture. This was tested using isolated pig PRA as model system, integrating vital imaging, pressure myography and mathematical modeling. Collagenase and elastase digestions were applied to evaluate the loadbearing roles of collagen and elastin, respectively. The incremental elastic modulus linearly related to the straightness of adventitial collagen fibers circumferentially and longitudinally (both R(2)≥0.99), while there was a nonlinear relationship to the internal elastic lamina elastin fiber branching angles. Mathematical modeling suggested a collagen recruitment strain (mean±SEM) of 1.1±0.2 circumferentially and 0.20±0.01 longitudinally, corresponding to a pressure of ~40mmHg, a finding supported by the vital imaging. The integrated method was tested on human PRA to confirm its validity. These showed limited circumferential distensibility and elongation and a collagen recruitment strain of 0.8±0.1 circumferentially and 0.06±0.02 longitudinally, reached at a distending pressure below 20mmHg. This was confirmed by vital imaging showing negligible microarchitectural changes of elastin and collagen upon pressurization. In conclusion, we show for the first time in resistance arteries a quantitative relationship between pressure-induced changes in the extracellular matrix and the arterial wall mechanics. The strength of the integrated methods invites for future detailed studies of microvascular pathologies.

AB - The impact of disease related changes in the extracellular matrix (ECM) on the mechanical properties of human resistance arteries largely remains to be established. Resistance arteries from both pig and human parietal pericardium (PRA) display a different ECM microarchitecture compared to frequently used rodent mesenteric arteries. We hypothesized that the biaxial mechanics of PRA mirror pressure induced changes in the ECM microarchitecture. This was tested using isolated pig PRA as model system, integrating vital imaging, pressure myography and mathematical modeling. Collagenase and elastase digestions were applied to evaluate the loadbearing roles of collagen and elastin, respectively. The incremental elastic modulus linearly related to the straightness of adventitial collagen fibers circumferentially and longitudinally (both R(2)≥0.99), while there was a nonlinear relationship to the internal elastic lamina elastin fiber branching angles. Mathematical modeling suggested a collagen recruitment strain (mean±SEM) of 1.1±0.2 circumferentially and 0.20±0.01 longitudinally, corresponding to a pressure of ~40mmHg, a finding supported by the vital imaging. The integrated method was tested on human PRA to confirm its validity. These showed limited circumferential distensibility and elongation and a collagen recruitment strain of 0.8±0.1 circumferentially and 0.06±0.02 longitudinally, reached at a distending pressure below 20mmHg. This was confirmed by vital imaging showing negligible microarchitectural changes of elastin and collagen upon pressurization. In conclusion, we show for the first time in resistance arteries a quantitative relationship between pressure-induced changes in the extracellular matrix and the arterial wall mechanics. The strength of the integrated methods invites for future detailed studies of microvascular pathologies.

KW - Journal Article

U2 - 10.1152/ajpheart.00110.2017

DO - 10.1152/ajpheart.00110.2017

M3 - Journal article

C2 - 28432057

VL - 313

SP - H164–H178

JO - American Journal of Physiology: Heart and Circulatory Physiology

JF - American Journal of Physiology: Heart and Circulatory Physiology

SN - 0363-6135

IS - 1

ER -