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      Collagen Biomechanics in Cerebral Arteries and Bifurcations Assessed by Polarizing Microscopy

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          Collagen is the main matrix protein of the artery wall. We have used the known correlation between collagen birefringence and its mechanical properties to assess the wall structural integrity in brain arteries and their bifurcation regions, which are the sites of formation of saccular aneurysms. Segments of 28 brain arteries, including bifurcations, were pressure fixed and sectioned in one of three orthogonal planes. Measurements were taken by polarizing microscopy of the birefringence of collagen fibers at the apex of bifurcations and in the main layers of the artery wall – adventitia, media and intima. Dimensional data were obtained of the layers in order to estimate wall properties. Along the apex of the flow divider we measured a narrow band of collagen (birefringence 30% higher than the adjacent adventitia) providing strength and stiffness in that region. There is a thin cell-free outer layer of the tunica media (mean thickness 11 µm) comprised of densely packed coaligned collagen with high birefringence. From the fiber birefringence and directional alignment of the individual layers we calculated that the adventitia contributes about one third of circumferential and almost all of longitudinal strength of intracranial arteries.

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          Directional wall strength in saccular brain aneurysms from polarized light microscopy.

          The aneurysm wall, which must withstand arterial blood pressure, is composed of layered collagen. Wall strength is related to both collagen fiber strength and orientation. When the aneurysm enlarges, the amount and organization of the collagen fibers change, potentially increasing the risk of rupture. We studied the directional organization and molecular strength of the collagen fibers layer by layer across the walls of four aneurysms in order to measure their mechanical integrity. The technique incorporates the birefringent properties of collagen, enabling us to use linearly polarized light for measuring the orientation of the fibers, and the Sénarmont compensator to measure the birefringence and thus mechanical strength. Intact aneurysms were obtained at autopsy, fixed at physiological pressure, sectioned at 4 microm, and stained with 0.05% picrosirius red. By combining birefringence and orientation data we estimated tensile strength as a function of direction on the aneurysmal wall. The average breaking strength of the wall ranged from 0.73 to 1.9 MPa. Comparing the weakest to the strongest direction, the breaking strength varied by a factor of up to 2X, implying a significant degree of mechanical anisotropy.
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            Differential distribution and expressions of collagens in the cerebral aneurysmal wall.

            To investigate the role of collagens in the formation and rupture of cerebral aneurysms, we examined the distribution and synthesis of vascular collagens in the wall of normal human cerebral main trunks and of cerebral aneurysms using immunohistochemistry and in situ hybridization techniques. Fifteen cerebral aneurysmal walls were resected at operation; control cerebral main trunks were obtained from seven autopsy cases. Semiserial sections from the specimens were subjected to immunofluorescence and immunohistochemical staining with antibodies to collagen types I, III, IV, V, VI, desmin and alpha-smooth muscle actin. In addition, type III collagen mRNA was examined by in situ hybridization. Immunohistochemical study showed that all collagen types were grossly preserved in the aneurysmal wall, although the distribution patterns were different for each collagen. The distribution of major fibrillar collagen types I and III was more diffuse and homogeneous in the luminal layer of the aneurysmal wall than the media of the control artery, although the intensity of immunohistochemical staining was weaker in the abluminal layer of the aneurysmal wall than the adventitia of the control artery. Collagen types IV and V were distributed more sparsely in the luminal layer of the aneurysmal wall than the media of the control artery. Collagen type VI was noted in the luminal as well as the abluminal layer of the aneurysmal wall, whereas it was located exclusively in the adventitia of the control artery. In situ hybridization showed that the signal for collagen type III mRNA on fibroblastic and smooth muscle cells was higher in the aneurysmal walls than the control arteries, suggesting up-regulation of type III collagen transcription in the cerebral aneurysmal wall. The study of the distribution and synthetic regulation of various types of collagen in the aneurysmal wall may be essential for understanding the formation of the aneurysmal wall and its protection against enlargement or rupture.
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              Stereological analysis of the layered collagen of human intracranial aneurysms


                Author and article information

                J Vasc Res
                Journal of Vascular Research
                S. Karger AG
                August 2003
                26 September 2003
                : 40
                : 4
                : 406-415
                Department of Medical Biophysics, University of Western Ontario, London, Ont., Canada
                72831 J Vasc Res 2003;40:406–415
                © 2003 S. Karger AG, Basel

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                Page count
                Figures: 3, Tables: 4, References: 31, Pages: 10
                Research Paper


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