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      Early Remodeling of Saphenous Vein Grafts: Proliferation, Migration and Apoptosis of Adventitial and Medial Cells Occur Simultaneously with Changes in Graft Diameter and Blood Flow

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          Abstract

          Background: This study was designed to determine how migration and proliferation of adventitial and medial cells correlate temporally with hemodynamic characteristics including changes in diameter and blood flow in vein grafts. Methods: Male mongrel dogs underwent end-to-side reversed saphenous vein bypass grafting across a ligated femoral artery. Hemodynamic parameters were assessed by duplex ultrasound. Proliferating cells were labeled 24–48 h after grafting with 5-bromo-2′-deoxyuridine (BrdU). Grafts were removed on postoperative days 2, 5, 7 and 14. Immunohistochemistry was performed on graft sections with antibodies to nuclear antigen Ki-67 (MIB-1), BrdU and smooth muscle cell markers. Apoptosis was identified by modified TUNEL staining. Proliferating/apoptotic cells were quantified digitally. Results: Mean luminal cross-sectional area, blood flow and velocity increased from day 2 to 7. Cell proliferation was evident in adventitia and media on day 2, maximum on day 5 and decreased significantly by day 14. Apoptosis was maximum on day 5. Early proliferating cells (BrdU labeled) localized in the adventitia and media on day 2 were more prevalent in the neointima on days 5–14 suggesting inward migration. On day 2, proliferating cells stained positive only for vimentin. By days 5–14, proliferating cells stained for α-smooth-muscle actin, a phenotype characteristic of myofibroblasts. Conclusion: These results indicate that cell proliferation and apoptosis occur simultaneously within the adventitia and media of the vein during the first week following grafting, when changes in diameter and blood flow are greatest. In addition, proliferating adventitial cells subsequently migrate inwards to contribute to the formation of neointima.

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          Most cited references4

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          Vascular endothelial cell proliferation in culture and the influence of flow.

          The influence of laminar shear stress on cell proliferation was investigated for subconfluent bovine aortic endothelial cell monolayers seeded on either glass or Thermanox. The effect of both steady and pulsatile shear stress was studied. For bovine aortic endothelial cells on Thermanox exposed to steady flow, shear stress levels greater than 15 dyne/cm2 resulted in a dose-related reduction in the rate of cell proliferation. At 90 dyne/cm2, the rate of proliferation was virtually totally arrested for 48 h, but then resumed. Pulsatile shear stress produced an exaggeration of the effect observed in response to steady shear stress. Bovine aortic endothelial cells seeded on glass, exhibited a similar but more sensitive response, with a significant reduction in growth rate observed after 24 h at shear stress levels greater than 5 dyne/cm2 and a near cessation of proliferation at 13 dyne/cm2.
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            The characteristics and anatomic distribution of lesions that cause reversed vein graft failure: a five-year prospective study.

            The cause of vein graft failure in the intermediate postoperative period (3 to 18 months) has not been well defined. To delineate the incidence, characteristics, and anatomic distribution of lesions that cause graft failure in this critical interval, 227 consecutive infrainguinal reversed vein grafts (IRVGs) constructed at a single institution from July 1986 to December 1991 were prospectively entered into a duplex scan surveillance protocol. Duplex surveillance with arteriographic confirmation identified 29 patent, hemodynamically failing IRVGs during a mean follow-up of 22 months (range 1 to 64 months). An additional 18 grafts thrombosed before detection of any underlying abnormality; thrombolytic therapy and repeat operation uncovered the cause of occlusion in 12 of these grafts. The cause of graft failure (failing as well as failed) was therefore clear in 41 (87.2%) of 47 instances. The causes of failure were intrinsic graft stenosis (n = 28; 59.6%), inflow failure (n = 6; 12.8%), outflow failure (n = 4; 8.5%), muscle entrapment (n = 2; 4.3%), and hypercoagulable state (n = 2; 4.3%). The most common intrinsic graft lesion was focal intimal hyperplasia (18 lesions in 16 grafts) in the juxtaanastomotic position, occurring solely in the vein graft itself. It occurred with equal frequency immediately distal to the proximal anastomosis or proximal to the distal anastomosis. Only rarely (n = 5) did this involve the juxtaanastomotic artery. Focal midgraft valvular stenoses (n = 6) and diffuse myointimal hyperplasia (n = 4) were also detected. The peak incidence of graft failure was 4 to 12 months after operation (70% within 12 months, 80% within 18 months). We conclude that duplex surveillance of IRVGs is warranted by the 21% incidence of potentially remediable graft failure. A significant portion of these failures occur during the intermediate postoperative period (3 to 18 months), usually as a result of focal intrinsic vein graft lesions. With reversed vein conduits, these lesions arise predominantly in the vein graft itself, in the juxtaanastomotic position.
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              Blood flow and kinetics of smooth muscle cell proliferation in canine autogenous vein grafts: in vivo BrdU incorporation.

              The effects of blood flow on the kinetics of smooth muscle cell (SMC) proliferation were examined in canine autogenous vein grafts with a distal poor run-off model. The in vivo bromodeoxyuridine (BrdU, a thymidine analogue) incorporation method was used to label proliferating SMCs in each layer of the vein graft. The BrdU labeling index (LI) was defined as a percentage of labeled cells compared to the total number of SMCs, and BrdU LIs were measured in the media and the intima of the graft. The development of intimal thickening of grafts was accelerated at 2 to 4 weeks after implantation. In poor run-off limbs with an abnormal blood flow condition, as characterized by a low flow and a low shear stress variation, the intima of the graft thickened more progressively than that in control limbs with a normal blood flow. In both groups, the medial BrdU LIs reached a maximum 3 to 5 days after implantation and decreased thereafter. The peak of the intimal BrdU LIs occurred at 1 week in both groups. The intimal LIs of the grafts in poor run-off limbs (6.34% at 1 week and 2.97% at 2 weeks) were significantly higher than those in control limbs (5.34 and 1.98%) for 2 weeks after implantation (P < 0.05). The medial SMC proliferation and the following intimal SMC proliferation of vein grafts were accelerated prior to development of the intimal thickening. SMC proliferation in the intima was prominent in a poor run-off limb with a low flow and a low shear stress variation.
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                Author and article information

                Journal
                JVR
                J Vasc Res
                10.1159/issn.1018-1172
                Journal of Vascular Research
                S. Karger AG
                1018-1172
                1423-0135
                2000
                December 2000
                10 January 2001
                : 37
                : 6
                : 576-584
                Affiliations
                Departments of aSurgery and bPhysiology and Biophysics, Mayo Clinic and Foundation, Rochester, Minn., USA
                Article
                54091 J Vasc Res 2000;37:576–584
                10.1159/000054091
                11146412
                63335775-c24f-4678-8012-a021e85834b0
                © 2000 S. Karger AG, Basel

                Copyright: All rights reserved. No part of this publication may be translated into other languages, reproduced or utilized in any form or by any means, electronic or mechanical, including photocopying, recording, microcopying, or by any information storage and retrieval system, without permission in writing from the publisher. Drug Dosage: The authors and the publisher have exerted every effort to ensure that drug selection and dosage set forth in this text are in accord with current recommendations and practice at the time of publication. However, in view of ongoing research, changes in government regulations, and the constant flow of information relating to drug therapy and drug reactions, the reader is urged to check the package insert for each drug for any changes in indications and dosage and for added warnings and precautions. This is particularly important when the recommended agent is a new and/or infrequently employed drug. Disclaimer: The statements, opinions and data contained in this publication are solely those of the individual authors and contributors and not of the publishers and the editor(s). The appearance of advertisements or/and product references in the publication is not a warranty, endorsement, or approval of the products or services advertised or of their effectiveness, quality or safety. The publisher and the editor(s) disclaim responsibility for any injury to persons or property resulting from any ideas, methods, instructions or products referred to in the content or advertisements.

                History
                Page count
                Figures: 6, References: 28, Pages: 9
                Categories
                Research Paper

                General medicine,Neurology,Cardiovascular Medicine,Internal medicine,Nephrology
                Intimal hyperplasia,Smooth muscle differentiation,Neointima,Fibroblasts,Myofibroblasts

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