Survey of the extracellular matrix architecture across the rat arterial tree

Objective: To understand arterial remodeling and the pathophysiology of arterial diseases, it is necessary to understand the baseline qualities and variations in arterial structure. Arteries could differ in wall thickness, laminar structure, and laminar fenestration depending on their position withi...

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Main Authors: Dylan D. McCreary, MS, Nolan F. Skirtich, BS, Elizabeth A. Andraska, MD, MS, Edith Tzeng, MD, Ryan M. McEnaney, MD
Format: Article
Language:English
Published: Elsevier 2022-01-01
Series:JVS - Vascular Science
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S2666350321000195
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author Dylan D. McCreary, MS
Nolan F. Skirtich, BS
Elizabeth A. Andraska, MD, MS
Edith Tzeng, MD
Ryan M. McEnaney, MD
author_facet Dylan D. McCreary, MS
Nolan F. Skirtich, BS
Elizabeth A. Andraska, MD, MS
Edith Tzeng, MD
Ryan M. McEnaney, MD
author_sort Dylan D. McCreary, MS
collection DOAJ
description Objective: To understand arterial remodeling and the pathophysiology of arterial diseases, it is necessary to understand the baseline qualities and variations in arterial structure. Arteries could differ in wall thickness, laminar structure, and laminar fenestration depending on their position within the arterial tree. We endeavored to evaluate and compare the extracellular matrix structure of different arteries throughout the arterial tree, from the aorta to the adductor muscle arteriole, with a particular focus on the internal elastic lamina (IEL). Methods: Arterial segments were harvested from male Sprague-Dawley rats and imaged using multiple modalities. En face scans by multiphoton microscopy were used to compare native-state adventitial collagen undulation and IEL fenestration. Results: Collagen undulation was similar across most examined arteries but straighter in the skeletal muscle arterioles (P < .05). The elastic lamellae showed several differences. The IEL fenestrae were similar in average size among abdominal aorta and celiac, renal, common iliac, and common femoral arteries (range, 14-24 μm2), with wide within-vessel variance (square of the standard deviation, 462-1904 μm4). However, they tended to be smaller (9.08 μm2) and less variable (square of the standard deviation, 88.3 μm4) in the popliteal artery. Fenestrae were greater in number in the superior mesenteric artery (SMA; 6686/mm2; P < .05) and profunda femoris artery (PFA; 11,042/mm2; P < .05) compared with the other examined vessels, which ranged in surface density from 3143/mm2 to 4362/mm2. The SMA and PFA also showed greater total fenestration as a proportion of the IEL surface area (SMA, 15.04%; P < .05; PFA, 24.11%; P < .001) than the other examined arteries (range of means, 4.7%-9.4%). The arteriolar IEL was structurally distinct, comparable to a low-density wireframe. Other structural differences were also noted, including differences in the number of medial lamellae along the arterial tree. Conclusions: We found that vessels at different locations along the arterial tree differ in structure. The SMA, PFA, and intramuscular arterioles have fundamental differences in the extracellular matrix structure compared with other arteries. Location-specific features such as the medial lamellae number and elastic laminar structure might have relevance to physiology and confer vulnerabilities to the development of pathology. : Clinical Relevance: Arterial pathologies affect and depend on elastic fibers and collagen. Medial arterial calcification involves mineral deposition onto elastic fibers and smooth muscle cell osteogenesis, which can be induced by elastin degradation. Degradation or remodeling of the extracellular matrix can be a critical component of atherosclerosis and hypertension. Pathologies can also be site-specific. Aneurysms are most common in the abdominal aorta (Ao), followed by the popliteal artery, which shows age-related changes to wall properties comparable to those in central elastic arteries. Visceral artery aneurysms, however, are rare. Location differences in arterial extracellular matrix structure could inform site-specific differences in arterial pathology.
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spelling doaj.art-3e6141a9a9784e759d1d4eb050208ab72023-01-05T06:47:43ZengElsevierJVS - Vascular Science2666-35032022-01-013114Survey of the extracellular matrix architecture across the rat arterial treeDylan D. McCreary, MS0Nolan F. Skirtich, BS1Elizabeth A. Andraska, MD, MS2Edith Tzeng, MD3Ryan M. McEnaney, MD4Department of Surgery, University of Pittsburgh School of Medicine, Pittsburgh, Pa; Department of Surgical Service, Veterans Affairs Pittsburgh Healthcare System, Pittsburgh, PaDepartment of Surgery, University of Pittsburgh School of Medicine, Pittsburgh, Pa; Department of Surgical Service, Veterans Affairs Pittsburgh Healthcare System, Pittsburgh, PaDepartment of Surgery, University of Pittsburgh School of Medicine, Pittsburgh, PaDepartment of Surgery, University of Pittsburgh School of Medicine, Pittsburgh, Pa; Department of Surgical Service, Veterans Affairs Pittsburgh Healthcare System, Pittsburgh, PaDepartment of Surgery, University of Pittsburgh School of Medicine, Pittsburgh, Pa; Department of Surgical Service, Veterans Affairs Pittsburgh Healthcare System, Pittsburgh, Pa; Correspondence: Ryan M. McEnaney, MD, Department of Surgery, University of Pittsburgh Medical Center, UPMC Presbyterian South Tower, 3rd Floor, Rm E351.5, 200 Lothrop St, Pittsburgh, PA 15213Objective: To understand arterial remodeling and the pathophysiology of arterial diseases, it is necessary to understand the baseline qualities and variations in arterial structure. Arteries could differ in wall thickness, laminar structure, and laminar fenestration depending on their position within the arterial tree. We endeavored to evaluate and compare the extracellular matrix structure of different arteries throughout the arterial tree, from the aorta to the adductor muscle arteriole, with a particular focus on the internal elastic lamina (IEL). Methods: Arterial segments were harvested from male Sprague-Dawley rats and imaged using multiple modalities. En face scans by multiphoton microscopy were used to compare native-state adventitial collagen undulation and IEL fenestration. Results: Collagen undulation was similar across most examined arteries but straighter in the skeletal muscle arterioles (P < .05). The elastic lamellae showed several differences. The IEL fenestrae were similar in average size among abdominal aorta and celiac, renal, common iliac, and common femoral arteries (range, 14-24 μm2), with wide within-vessel variance (square of the standard deviation, 462-1904 μm4). However, they tended to be smaller (9.08 μm2) and less variable (square of the standard deviation, 88.3 μm4) in the popliteal artery. Fenestrae were greater in number in the superior mesenteric artery (SMA; 6686/mm2; P < .05) and profunda femoris artery (PFA; 11,042/mm2; P < .05) compared with the other examined vessels, which ranged in surface density from 3143/mm2 to 4362/mm2. The SMA and PFA also showed greater total fenestration as a proportion of the IEL surface area (SMA, 15.04%; P < .05; PFA, 24.11%; P < .001) than the other examined arteries (range of means, 4.7%-9.4%). The arteriolar IEL was structurally distinct, comparable to a low-density wireframe. Other structural differences were also noted, including differences in the number of medial lamellae along the arterial tree. Conclusions: We found that vessels at different locations along the arterial tree differ in structure. The SMA, PFA, and intramuscular arterioles have fundamental differences in the extracellular matrix structure compared with other arteries. Location-specific features such as the medial lamellae number and elastic laminar structure might have relevance to physiology and confer vulnerabilities to the development of pathology. : Clinical Relevance: Arterial pathologies affect and depend on elastic fibers and collagen. Medial arterial calcification involves mineral deposition onto elastic fibers and smooth muscle cell osteogenesis, which can be induced by elastin degradation. Degradation or remodeling of the extracellular matrix can be a critical component of atherosclerosis and hypertension. Pathologies can also be site-specific. Aneurysms are most common in the abdominal aorta (Ao), followed by the popliteal artery, which shows age-related changes to wall properties comparable to those in central elastic arteries. Visceral artery aneurysms, however, are rare. Location differences in arterial extracellular matrix structure could inform site-specific differences in arterial pathology.http://www.sciencedirect.com/science/article/pii/S2666350321000195ArteriesArteriolesElastic tissueExtracellular matrixFibrillar collagens
spellingShingle Dylan D. McCreary, MS
Nolan F. Skirtich, BS
Elizabeth A. Andraska, MD, MS
Edith Tzeng, MD
Ryan M. McEnaney, MD
Survey of the extracellular matrix architecture across the rat arterial tree
JVS - Vascular Science
Arteries
Arterioles
Elastic tissue
Extracellular matrix
Fibrillar collagens
title Survey of the extracellular matrix architecture across the rat arterial tree
title_full Survey of the extracellular matrix architecture across the rat arterial tree
title_fullStr Survey of the extracellular matrix architecture across the rat arterial tree
title_full_unstemmed Survey of the extracellular matrix architecture across the rat arterial tree
title_short Survey of the extracellular matrix architecture across the rat arterial tree
title_sort survey of the extracellular matrix architecture across the rat arterial tree
topic Arteries
Arterioles
Elastic tissue
Extracellular matrix
Fibrillar collagens
url http://www.sciencedirect.com/science/article/pii/S2666350321000195
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