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Aortic Aneurysms in a Rat Model: In Vivo MR Imaging of Endovascular Cell Therapy¹

¹ From INSERM U 698, Bioengineering Department, University Paris 7-University Paris 13, X. Bichat Hospital, Paris, France (J.F.D., D.L.); Radiology Department (J.F.D.) and Centre National de la Recherche Scientifique, Unité Nixte de Recherche 7054 (J.D., E.A.), Assistance Publique-Hôpitaux de Paris, IFR de Médecine, University Paris 12, H. Mondor Hospital, Créteil, France; Laboratoire Matière et Systèmes Complexes, Paris, France (C.R., F.G.); Laboratoire de Resonance Magnetique Nucleaire Biologique-Institut de Chimie des Substances Naturelles, Gif sur Yvette, France (P.M., B.G.); Laboratoire des Liquides Ioniques et Interfaces Chargées, Paris, France (C.R., J.R., J.N.P.); and Radiology Department, Tenon Hospital, Assistance Publique-Hôpitaux de Paris, Paris, France (F.P.B.). Received January 7, 2007; revision requested March 2; revision received April 16; accepted May 7; final version accepted June 18. Supported by the Centre National de la Recherche Scientifique (CNRS), the French Institut National de la Santé et de la Recherche Médicale (INSERM), the Ministère de l'Education Nationale de l'Enseignement Supérieur et de la Recherche (Action Concertée Incitative technologies pour la santé), Université Paris 13 (Bonus qualité recherche and Institut Federal de Recherche Paris-Nord Plaine de France), University Paris 12 Val de Marne, the Fondation Bettencourt-Schueller (Prix Coup d'Elan), and the Fondation de la Recherche Médicale. C.R. supported by the French Direction Générale de l'Armement (DGA doctorat fellowship). Address correspondence to J.F.D. (e-mail: jean-francois.deux{at}hmn.aphp.fr).

View larger version (6K): [in this window] [in a new window] [Download PPT slide]   Figure 1: Experimental in vivo MR imaging scheme.

View larger version (60K): [in this window] [in a new window] [Download PPT slide]   Figure 2: Transverse in vivo 1.5-T T2*-weighted gradient-echo MR images (16/2.8, 30° flip angle) of AAAs before (A1–A4) and after delivery of IONP VSMCs (B1), fluorescence- and iron-labeled VSMCs (B2), fluorescence-labeled VSMCs (B3), and free iron particles (B4). Note intermediate signal intensity of aneurysm wall before VSMC injection (A1–A4). Vessel lumen appears as bright area (). B1 shows areas of hypointense signal (black arrows) next to aneurysm wall after delivery of IONP VSMCs. Signal intensity of aortic lumen appears darker probably because of susceptibility artifacts induced by seeded magnetically labeled cells. Low-signal-intensity areas (white arrow) were depicted above aortic wall in three rats, suggesting leaks around aorta during cell delivery. B2, Area of hypointense signal (arrow) was detected in only half the aortic wall when rat was not rotated during cell seeding. No signal intensity change was detected after delivery of non–iron-labeled VSMCs (B3) and free iron nanoparticles (B4). Fluorescence labeling revealed fluorescent cells next to aortic wall after delivery of VSMCs labeled with both iron and red fluorescent dye (B2 inset) or red fluorescent dye only (non–iron labeled, B3 inset). Scale bar = 1 mm.

View larger version (57K): [in this window] [in a new window] [Download PPT slide]   Figure 3: Transverse in vivo 1.5-T T2*-weighted gradient-echo MR images (16/2.8, 30° flip angle) of AAAs (in different animals) 7 (left), 14 (middle), and 28 (right) days after delivery of IONP VSMCs show areas of hypointense signal (arrows) around aortic wall. Vessel lumen appears as bright area (). Scale bar = 1 mm.

View larger version (47K): [in this window] [in a new window] [Download PPT slide]   Figure 4: Transverse T2*-weighted gradient-echo MR images (16/2.8, 30° flip angle) of AAAs immediately before (far left image) and days 0 (second image from left), 21 (third image from left), and 28 (far right image) after delivery of IONP VSMCs (in same animal) show areas of hypointense signal (arrows) in the aortic wall. Low-signal-intensity area is circular on day 0 and more focal (next to posterior part of aortic wall) on days 21 and 28. Vessel lumen appears as bright area (). Scale bar = 1 mm.

View larger version (150K): [in this window] [in a new window] [Download PPT slide]   Figure 5a: (a) Transverse high-field-strength ex vivo 9.4-T T2*-weighted gradient-echo MR image (100/3, 25° flip angle) of aorta 28 days after delivery of IONP VSMCs shows crescent-shaped low-signal-intensity area (arrow) in deep portion of aortic wall, adjacent to a more focal low-signal-intensity area (black arrowhead). Focal nodular low-signal-intensity areas (white arrowhead) are also seen in external part of aortic wall. (b) Perls Prussian blue–stained histologic section (5 µm) of same area (original magnification, x40) shows iron-loaded cells in deep part of neointima (arrow and black arrowhead) and in adventitia (white arrowhead). Localization of iron-loaded cells is similar to that of low-signal-intensity areas in a. Scale bar = 0.5 mm.

View larger version (138K): [in this window] [in a new window] [Download PPT slide]   Figure 5b: (a) Transverse high-field-strength ex vivo 9.4-T T2*-weighted gradient-echo MR image (100/3, 25° flip angle) of aorta 28 days after delivery of IONP VSMCs shows crescent-shaped low-signal-intensity area (arrow) in deep portion of aortic wall, adjacent to a more focal low-signal-intensity area (black arrowhead). Focal nodular low-signal-intensity areas (white arrowhead) are also seen in external part of aortic wall. (b) Perls Prussian blue–stained histologic section (5 µm) of same area (original magnification, x40) shows iron-loaded cells in deep part of neointima (arrow and black arrowhead) and in adventitia (white arrowhead). Localization of iron-loaded cells is similar to that of low-signal-intensity areas in a. Scale bar = 0.5 mm.

View larger version (111K): [in this window] [in a new window] [Download PPT slide]   Figure 6: Histologic cross sections of AAAs on days 0–28 after VSMC delivery. A1–A4, Perls Prussian blue staining revealed iron-loaded cells (arrows) next to aortic wall on day 0 and in neointima on days 7, 14, and 28. C1–C4, Some Perls Prussian blue–negative macrophages (arrowheads) were detected on days 0, 7, 14, and 28. B1–B4, Colabeling for -actin and Perls Prussian blue staining in the media revealed iron-containing cells positive for -actin (arrows) on days 0, 7, 14, and 28. Some Perls Prussian blue–positive cells in the neointima and adventitia were negative at both macrophage staining (data not shown) and -actin staining on days 14 and 28. Arrowheads in B3 and B4 indicate Perls Prussian blue–positive cells negative at -actin staining in the neointima on days 14 and 28, respectively. Twin arrows in C3 indicate a Perls Prussian blue–positive cell in the adventitia on day 14. Some Perls Prussian blue–positive macrophages (arrow in C4) were also identified in the adventitia on day 28.