Hostname: page-component-586b7cd67f-gb8f7 Total loading time: 0 Render date: 2024-11-23T15:41:33.036Z Has data issue: false hasContentIssue false
  • English
  • Français

Optimization of Vascular Casting for Three-Dimensional Fluorescence Cryo-Imaging of Collateral Vessels in the Ischemic Rat Hindlimb

Published online by Cambridge University Press:  23 February 2017

Janina C.V. Schwarz ,
Monique G.J.T.B. van Lier ,
Erik N.T.P. Bakker ,
Judith de Vos ,
Jos A.E. Spaan ,
Ed VanBavel  and
Maria Siebes
Janina C.V. Schwarz
Affiliation:
Department of Biomedical Engineering and Physics, Academic Medical Center, University of Amsterdam, Meibergdreef 9, 1105 AZ Amsterdam, The Netherlands
Monique G.J.T.B. van Lier
Affiliation:
Department of Biomedical Engineering and Physics, Academic Medical Center, University of Amsterdam, Meibergdreef 9, 1105 AZ Amsterdam, The Netherlands
Erik N.T.P. Bakker
Affiliation:
Department of Biomedical Engineering and Physics, Academic Medical Center, University of Amsterdam, Meibergdreef 9, 1105 AZ Amsterdam, The Netherlands
Judith de Vos
Affiliation:
Department of Biomedical Engineering and Physics, Academic Medical Center, University of Amsterdam, Meibergdreef 9, 1105 AZ Amsterdam, The Netherlands
Jos A.E. Spaan
Affiliation:
Department of Biomedical Engineering and Physics, Academic Medical Center, University of Amsterdam, Meibergdreef 9, 1105 AZ Amsterdam, The Netherlands
Ed VanBavel
Affiliation:
Department of Biomedical Engineering and Physics, Academic Medical Center, University of Amsterdam, Meibergdreef 9, 1105 AZ Amsterdam, The Netherlands
Maria Siebes*
Affiliation:
Department of Biomedical Engineering and Physics, Academic Medical Center, University of Amsterdam, Meibergdreef 9, 1105 AZ Amsterdam, The Netherlands
*
*Corresponding author.[email protected]
Get access

Abstract

Development of collateral vessels, arteriogenesis, may protect against tissue ischemia, however, quantitative data on this process remain scarce. We have developed a technique for replicating the entire arterial network of ischemic rat hindlimbs in three dimensions (3D) based on vascular casting and automated sequential cryo-imaging. Various dilutions of Batson’s No. 17 with methyl methacrylate were evaluated in healthy rats, with further protocol optimization in ischemic rats. Penetration of the resin into the vascular network greatly depended on dilution; the total length of casted vessels below 75 µm was 13-fold higher at 50% dilution compared with the 10% dilution. Dilutions of 25–30%, with transient clamping of the healthy iliac artery, were optimal for imaging the arterial network in unilateral ischemia. This protocol completely filled the lumina of small arterioles and collateral vessels. These appeared as thin anastomoses in healthy legs and increasingly larger vessels during ligation (median diameter 1 week: 63 µm, 4 weeks: 127 µm). The presented combination of quality casts with high-resolution cryo-imaging enables automated, detailed 3D analysis of collateral adaptation, which furthermore can be combined with co-registered 3D distributions of fluorescent molecular imaging markers reflecting biological activity or perfusion.

Keywords

3D imagingvascular imagingvascular castinghindlimb ischemiacollateral vessels
Type
Biological Applications
Information
Microscopy and Microanalysis , Volume 23 , Issue 1 , February 2017 , pp. 77 - 87
Copyright
© Microscopy Society of America 2017 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Bassingthwaighte, J.B., Yipintsoi, T. & Harvey, R.B. (1974). Microvasculature of the dog left ventricular myocardium. Microvasc Res 7(2), 229–249.Google Scholar
Biggs, D.S. & Andrews, M. (1997). Acceleration of iterative image restoration algorithms. Appl Opt 36(8), 1766–1775.Google Scholar
Distasi, M.R., Case, J., Ziegler, M.A., Dinauer, M.C., Yoder, M.C., Haneline, L.S., Dalsing, M.C., Miller, S.J., Labarrere, C.A., Murphy, M.P., Ingram, D.A. & Unthank, J.L. (2009). Suppressed hindlimb perfusion in Rac2-/- and Nox2-/- mice does not result from impaired collateral growth. Am J Physiol Heart Circ Physiol 296(3), H877–H886.Google Scholar
Faber, J.E., Chilian, W.M., Deindl, E., van Royen, N. & Simons, M. (2014). A brief etymology of the collateral circulation. Arterioscler Thromb Vasc Biol 34(9), 1854–1859.CrossRefGoogle ScholarPubMed
Grabherr, S., Djonov, V., Yen, K., Thali, M. & Dirnhofer, R. (2007). Postmortem angiography: Review of former and current methods. Am J Roentgenol 188(3), 832–838.Google Scholar
Haenssgen, K., Makanya, A.N. & Djonov, V. (2014). Casting materials and their application in research and teaching. Microsc Microanal 20(2), 493–513.Google Scholar
Hakimzadeh, N., van Horssen, P., van Lier, M.G., van den Wijngaard, J.P., Belterman, C., Coronel, R., Piek, J.J., Verberne, H.J., Spaan, J.A. & Siebes, M. (2014). Detection and quantification methods of monocyte homing in coronary vasculature with an imaging cryomicrotome. J Mol Cell Cardiol 76, 196–204.Google Scholar
Heuslein, J.L., Meisner, J.K., Li, X., Song, J., Vincentelli, H., Leiphart, R.J., Ames, E.G., Blackman, B.R. & Price, R.J. (2015). Mechanisms of amplified arteriogenesis in collateral artery segments exposed to reversed flow direction. Arterioscler Thromb Vasc Biol 35(11), 2354–2365.Google Scholar
Hodde, K.C. & Nowell, J.A. (1980). SEM of micro-corrosion casts. Scan Electron Microsc 2, 89–106.Google Scholar
Hossler, F.E. & Douglas, J.E. (2001). Vascular corrosion casting: Review of advantages and limitations in the application of some simple quantitative methods. Microsc Microanal 7(3), 253–264.Google Scholar
Jacoby, C., Böring, Y., Beck, A., Zernecke, A., Aurich, V., Weber, C., Schrader, J. & Flögel, U. (2008). Dynamic changes in murine vessel geometry assessed by high-resolution magnetic resonance angiography: A 9.4T study. J Magn Reson Imaging 28(3), 637–645.CrossRefGoogle ScholarPubMed
Kratky, R.G., Lo, D.K. & Roach, M.R. (1991). Quantitative measurement of fixation rate and dimension changes in the aldehyde/pressure-fixed canine carotid artery. Blood Vessels 28(5), 386–395.Google Scholar
Krucker, T., Lang, A. & Meyer, E. (2006). New polyurethane-based material for vascular corrosion casting with improved physical and imaging characteristics. Microsc Res Tech 69(2), 138–147.Google Scholar
Lagerveld, B.W., van Horssen, P., Laguna, M.P., van den Wijngaard, J.P., Siebes, M., Wijkstra, H., de la Rosette, J.J. & Spaan, J.A. (2011). Gradient changes in porcine renal arterial vascular anatomy and blood flow after cryoablation. J Urol 186(2), 681–686.Google Scholar
Lametschwandtner, A., Lametschwandtner, U. & Weiger, T. (1984). Scanning electron microscopy of vascular corrosion casts—technique and applications. Scan Electron Microsc 2, 663–695.Google Scholar
Levesque, M.J., Cornhill, J.F. & Nerem, R.M. (1979). Vascular casting. A new method for the study of the arterial endothelium. Atherosclerosis 34(4), 457–467.Google Scholar
Limbourg, A., Korff, T., Napp, L., Schaper, W., Drexler, H. & Limbourg, F. (2009). Evaluation of postnatal arteriogenesis and angiogenesis in a mouse model of hind-limb ischemia. Nat Protoc 4(12), 1737–1746.CrossRefGoogle Scholar
Lotfi, S., Patel, A.S., Mattock, K., Egginton, S., Smith, A. & Modarai, B. (2013). Towards a more relevant hind limb model of muscle ischaemia. Atherosclerosis 227(1), 1–8.Google Scholar
Madeddu, P., Emanueli, C., Spillmann, F., Meloni, M., Bouby, N., Richer, C., Alhenc-Gelas, F., Van Weel, V., Eefting, D., Quax, P., Hu, Y., Xu, Q., Hemdahl, A., van Golde, J., Huijberts, M., de Lussanet, Q., Struijker Boudier, H., Couffinhal, T., Duplaa, C., Chimenti, S., Staszewsky, L., Latini, R., Baumans, V. & Levy, B. (2006). Murine models of myocardial and limb ischemia: Diagnostic end-points and relevance to clinical problems. Vascul Pharmacol 45(5), 281–301.Google Scholar
Mondy, W., Casteleyn, C., Loo, D., Raja, M., Singleton, C. & Jacot, J. (2013). Osmium tetroxide labeling of (poly)methyl methacrylate corrosion casts for enhancement of micro-CT microvascular imaging. Microsc Microanal 19(6), 1416–1427.Google Scholar
Oses, P., Renault, M.A., Chauvel, R., Leroux, L., Allières, C., Séguy, B., Lamazière, J.M., Dufourcq, P., Couffinhal, T. & Duplàa, C. (2009). Mapping 3-dimensional neovessel organization steps using micro-computed tomography in a murine model of hindlimb ischemia-brief report. Arterioscler Thromb Vasc Biol 29(12), 2090–2092.Google Scholar
Poole, K.M., Tucker-Schwartz, J.M., Sit, W.W., Walsh, A.J., Duvall, C.L. & Skala, M.C. (2013). Quantitative optical imaging of vascular response in vivo in a model of peripheral arterial disease. Am J Physiol Heart Circ Physiol 305(8), H1168–H1180.Google Scholar
Potter, R.F. & Groom, A.C. (1983). Capillary diameter and geometry in cardiac and skeletal muscle studied by means of corrosion casts. Microvasc Res 25(1), 68–84.Google Scholar
Reddy, P.A., Douglas, J.E., Schulte, M. & Hossler, F.E. (1995). The effect of prefixation on the quality of vascular corrosion casts of rat heart. Cardiovasc Pathol 4(2), 133–140.Google Scholar
Schaper, W. (2009). Collateral circulation: Past and present. Basic Res Cardiol 104(1), 5–21.CrossRefGoogle ScholarPubMed
Schirmer, S., van Nooijen, F., Piek, J. & van Royen, N. (2009). Stimulation of collateral artery growth: Travelling further down the road to clinical application. Heart 95(3), 191–197.Google Scholar
Shireman, P.K. & Quinones, M.P. (2005). Differential necrosis despite similar perfusion in mouse strains after ischemia. J Surg Res 129(2), 242–250.CrossRefGoogle ScholarPubMed
Spaan, J.A.E., ter Wee, R., van Teeffelen, J.W.G.E., Streekstra, G., Siebes, M., Kolyva, C., Vink, H., Fokkema, D.S. & VanBavel, E. (2005). Visualisation of intramural coronary vasculature by an imaging cryomicrotome suggests compartmentalisation of myocardial perfusion areas. Med Biol Eng Comput 43(4), 431–435.CrossRefGoogle ScholarPubMed
Stacy, M.R., Paeng, J.C. & Sinusas, A.J. (2015). The role of molecular imaging in the evaluation of myocardial and peripheral angiogenesis. Ann Nucl Med 29(3), 217–223.CrossRefGoogle ScholarPubMed
van den Wijngaard, J.P., Schulten, H., van Horssen, P., Ter Wee, R.D., Siebes, M., Post, M.J. & Spaan, J.A. (2011). Porcine coronary collateral formation in the absence of a pressure gradient remote of the ischemic border zone. Am J Physiol Heart Circ Physiol 300(5), H1930–H1937.Google Scholar
van den Wijngaard, J.P.H.M., Schwarz, J.C.V., van Horssen, P., van Lier, M.G.J.T.B., Dobbe, J.G.G., Spaan, J.A.E. & Siebes, M. (2013). 3D Imaging of vascular networks for biophysical modeling of perfusion distribution within the heart. J Biomech 46(2), 229–239.Google Scholar
van Horssen, P., Siebes, M., Hoefer, I., Spaan, J.A.E. & van den Wijngaard, J.P.H.M. (2010). Improved detection of fluorescently labeled microspheres and vessel architecture with an imaging cryomicrotome. Med Biol Eng Comput 48(8), 735–744.Google Scholar
Weiger, T., Lametschwandtner, A. & Stockmayer, P. (1986). Technical parameters of plastics (Mercox CL-2B and various methylmethacrylates) used in scanning electron microscopy of vascular corrosion casts. Scan Electron Microsc 1, 243–252.Google Scholar
Welten, S.M., Bastiaansen, A.J., de Jong, R., de Vries, M.R., Peters, E.H., Boonstra, M., Sheikh, S.P., La Monica, N., Kandimalla, E.R., Quax, P.H. & Nossent, A.Y. (2014). Inhibition of 14q32 MicroRNAs miR-329, miR-487b, miR-494 and miR-495 increases neovascularization and blood flow recovery after ischemia. Circ Res 115(8), 696–708.Google Scholar
Westerweel, P.E., Rookmaaker, M.B., van Zonneveld, A.J., Bleys, R.L.A.W., Rabelink, T.J. & Verhaar, M.C. (2005). A study of neovascularization in the rat ischemic hindlimb using Araldite casting and Spalteholtz tissue clearing. Cardiovasc Pathol 14(6), 294–297.Google Scholar
Zhang, Z., Slobodianski, A., Ito, W.D., Arnold, A., Nehlsen, J., Weng, S., Lund, N., Liu, J., Egaña, J.T., Lohmeyer, J.A., Müller, D.F. & Machens, H.G. (2011). Enhanced collateral growth by double transplantation of gene-nucleofected fibroblasts in ischemic hindlimb of rats. PLoS One 6(4), e19192.CrossRefGoogle ScholarPubMed
Ziegler, M.A., Distasi, M.R., Bills, R.G., Miller, S.J., Alloosh, M., Murphy, M.P., Akingba, A.G., Sturek, M., Dalsing, M.C. & Unthank, J.L. (2010). Marvels, mysteries, and misconceptions of vascular compensation to peripheral artery occlusion. Microcirculation 17(1), 3–20.Google Scholar

Schwarz supplementary material

Schwarz supplementary material 1

Download Schwarz supplementary material(Video)
Video 41 MB