Each type of perivascular system is characterized by a different set of advantages and disadvantages.
Table 4 presents a comparative view of the perivascular system properties discussed in this review.
Gel formulations present strong disadvantages in terms of localization, mechanical support and sustaining drug release. However, the insufficient sustained release can be outweighed by drug-loaded particle addition to the gels. Meshes and sheaths are the most challenging to be placed since the system has to be applied like a sock around the vein and then sutured in place. Meshes mechanical support compared to sheaths can nevertheless be more efficient as their macroporosity allows for the elastic deformation of the tube. Sheaths, on the other hand, allow for sustained release, while examples of meshes sustaining the release are not encountered in the literature. Cuffs and wraps present the advantage of having moderated scores in all properties, although their solid nature precludes repeated administration.
Table 4.: Comparative view of the perivascular system type and their properties evaluation.
+ Extremely unlikely, ++ Unlikely, +++ Neutral, ++++ Likely, +++++ Extremely likely
Conclusion
Perivascular administration is the most promising approach to prevent focal vascular pathologies occurring after vascular surgery, such as bypasses or arteriovenous fistulas placements. A wide range of perivascular MDs and DDSs have been reported in the literature over the last 25 years. This is not reflected in the clinical routine, as the success of clinical trials is moderate. This is due to the high degree of complexity of these systems. Each element of the system should be carefully selected in order to correlate with the vascular pathophysiology and the peculiarities of the application site. Ease of application, conformable covering of the graft and retention on site are prerequisites for perivascular systems. Gel formulations have been designed to meet these needs, but they lack the
Gel Gel + particles Mesh Sheath Cuff Wrap
Ease of administration +++++ +++++ + + +++ ++++
Repeated administration ++++ ++++ + + + +
Localization ++ ++ +++++ +++++ ++++ +++
Mechanical support + + +++++ ++++ +++ ++
Sustaining drug release + +++++ + +++ +++ +++
CHAPTER I - Perivascular medical devices and drug eluting systems: Making the right choices
33 mechanical properties to constrict the vessel. Constriction provided by non-degradable knitted nitinol meshes was shown to be important but failed to improve vessel patency in clinical trials.
Bioresorbable systems are preferred in surgery, but more evidences are needed to conclude on the optimal duration of the sytem. Innovation from endovascular approaches, such as biodegradable magnesium alloys stents, might benefit to novel perivascular systems. It now becomes clear that mechanical support is not sufficient for successful perivascular approaches, and a carefully selected drug is undoubtedly needed to reinforce the effect. Nevertheless, the drug needs to be delivered in the appropriate time course, matching the development of the pathology; for this, PLGA is optimal.
Clinical trials on perivascular DDSs are ongoing. A system combining all the above-mentioned features has not yet been developed.
References
[1] F.W. Mohr, M.-C. Morice, A.P. Kappetein, T.E. Feldman, E. Ståhle, A. Colombo, M.J. Mack, D.R. Holmes Jr, M.-A. Morel, N.V. Dyck, V.M. Houle, K.D. Dawkins, P.W. Serruys, Coronary artery bypass graft surgery versus percutaneous coronary intervention in patients with three-vessel disease and left main coronary disease:
5-year follow-up of the randomised, clinical SYNTAX trial, The Lancet 381(9867) (2013) 629-638.
[2] S. Deb, H.C. Wijeysundera, D.T. Ko, H. Tsubota, S. Hill, S.E. Fremes, Coronary artery bypass graft surgery vs percutaneous interventions in coronary revascularization: A systematic review, JAMA 310(19) (2013) 2086-2095.
[3] M.D. Gerhard-Herman, H.L. Gornik, C. Barrett, N.R. Barshes, M.A. Corriere, D.E. Drachman, L.A.
Fleisher, F.G.R. Fowkes, N.M. Hamburg, S. Kinlay, R. Lookstein, S. Misra, L. Mureebe, J.W. Olin, R.A.G.
Patel, J.G. Regensteiner, A. Schanzer, M.H. Shishehbor, K.J. Stewart, D. Treat-Jacobson, M.E. Walsh, 2016 AHA/ACC Guideline on the Management of Patients With Lower Extremity Peripheral Artery Disease:
Executive Summary, A Report of the American College of Cardiology/American Heart Association Task Force on Clinical Practice Guidelines (2016).
[4] A.B. Bernstein, E. Hing, A. Moss, K. Allen, A. Siller, R. Tiggle, Health care in America: Trends in utilization., Hyattsville, Maryland: National Center for Health Statistics, 2003.
[5] Eurostat, Cardiovascular diseases statistics, European Comission, 2016.
[6] P.P. Goodney, A.W. Beck, J. Nagle, H.G. Welch, R.M. Zwolak, National trends in lower extremity bypass surgery, endovascular interventions, and major amputations, J. Vasc. Surg. 50(1) (2009) 54-60.
[7] I. Fishbein, M. Chorny, G. Golomb, Treatment of restenosis by controlled-release delivery systems of tyrphostins, Drug Dev. Res. 50(3-4) (2000) 487-496.
[8] C.D. Owens, W.J. Gasper, A.S. Rahman, M.S. Conte, Vein graft failure, J. Vasc. Surg. 61(1) (2015) 203-216.
[9] T. Okada, D.H. Bark, M.R. Mayberg, Localized release of perivascular heparin inhibits intimal proliferation after endothelial injury without systemic anticoagulation, Neurosurgery 25(6) (1989) 892-8.
[10] J.A. Barra, A. Volant, J.P. Leroy, J. Braesco, J. Airiau, J. Boschat, J.J. Blanc, P. Penther, Constrictive perivenous mesh prosthesis for preservation of vein integrity. Experimental results and application for coronary bypass grafting, J. Thorac. Cardiovasc. Surg. 92(3 Pt 1) (1986) 330-6.
[11] I. Fishbein, R. Brauner, M. Chorny, J. Gao, X. Chen, H. Laks, G. Golomb, Local delivery of mithramycin restores vascular reactivity and inhibits neointimal formation in injured arteries and vascular grafts, J. Control.
Release 77(3) (2001) 167-181.
[12] S.M. Seedial, S. Ghosh, R.S. Saunders, P.A. Suwanabol, X. Shi, B. Liu, K.C. Kent, Local drug delivery to prevent restenosis, J. Vasc. Surg. 57(5) (2013) 1403-1414.
CHAPTER I - Perivascular medical devices and drug eluting systems: Making the right choices
34 [13] T. Schachner, G. Laufer, J. Bonatti, In vivo (animal) models of vein graft disease, Eur. J. Cardiothorac.
Surg. 30(3) (2006) 451-63.
[14] J. Schoettler, J. Jussli-Melchers, C. Grothusen, L. Stracke, F. Schoeneich, S. Stohn, G. Hoffmann, J.
Cremer, Highly flexible nitinol mesh to encase aortocoronary saphenous vein grafts: first clinical experiences and angiographic results nine months postoperatively, Interact. Cardiovasc. Thorac. Surg. 13(4) (2011) 396-400.
[15] T. Schachner, Pharmacologic inhibition of vein graft neointimal hyperplasia, J. Thorac. Cardiovasc. Surg.
131(5) (2006) 1065-1072.
[16] H. Bult, Restenosis: a challenge for pharmacology, Trends Pharmacol. Sci. 21(7) (2000) 274-279.
[17] D. Wiedemann, A. Kocher, N. Bonaros, S. Semsroth, G. Laufer, M. Grimm, T. Schachner, Perivascular administration of drugs and genes as a means of reducing vein graft failure, Curr. Opin. Pharmacol. 12(2) (2012) 203-216.
[18] M.S. Lemson, J.H.M. Tordoir, M.J.A.P. Daemen, P.J.E.H.M. Kitslaar, Intimal Hyperplasia in Vascular Grafts, Eur. J. Vasc. Endovasc. Surg. 19(4) (2000) 336-350.
[19] L.A. Orloff, A.J. Domb, D. Teomim, I. Fishbein, G. Golomb, Biodegradable implant strategies for inhibition of restenosis, Adv. Drug Deliv. Rev. 24(1) (1997) 3-9.
[20] E.R. Edelman, Perivascular delivery of heparin regulates myointimal hyperplasia, Reactive Polymers 25(2-3) (1995) 149-156.
[21] G. Golomb, M. Mayberg, A.J. Domb, Polymeric perivascular delivery systems, in: A.J. Domb (Ed.), Polymeric site- specific Pharmacotherapy, John Wiley & Sons Ltd.1994, pp. 205-19.
[22] V. Vijayan, F.C.T. Smith, G.D. Angelini, R.A. Bulbulia, J.Y. Jeremy, External Supports and the Prevention of Neointima Formation in Vein Grafts, Eur. J. Vasc. Endovasc. Surg. 24(1) (2002) 13-22.
[23] M. Desai, J. Mirzay-Razzaz, D.D. von, S. Sarkar, G. Hamilton, A.M. Seifalian, Inhibition of neointimal formation and hyperplasia in vein grafts by external stent/sheath, Vasc. Med. 15(4) (2010) 287-97.
[24] J. Hu, S. Wan, External support in preventing vein graft failure, Asian Cardiovasc. Thorac. Ann. 20(5) (2012) 615-622.
[25] M.A. Chaudhary, L.-W. Guo, X. Shi, G. Chen, S. Gong, B. Liu, K.C. Kent, Periadventitial drug delivery for the prevention of intimal hyperplasia following open surgery, J. Control. Release 233 (2016) 174-180.
[26] K.R. Stenmark, M.E. Yeager, K.C. El Kasmi, E. Nozik-Grayck, E.V. Gerasimovskaya, M. Li, S.R. Riddle, M.G. Frid, The adventitia: essential regulator of vascular wall structure and function, Annu. Rev. Physiol. 75 (2013) 23-47.
[27] K. Maiellaro, W.R. Taylor, The role of the adventitia in vascular inflammation, Cardiovasc. Res. 75(4) (2007) 640-648.
[28] M.A. Lovich, E.R. Edelman, Mechanisms of transmural heparin transport in the rat abdominal aorta after local vascular delivery, Circ. Res. 77(6) (1995) 1143-50.
[29] E.R. Edelman, M.A. Nugent, M.J. Karnovsky, Perivascular and intravenous administration of basic fibroblast growth factor: vascular and solid organ deposition, Proc. Nat. Acad. Sci. U.S.A. 90(4) (1993) 1513-1517.
[30] K. Yahagi, F.D. Kolodgie, F. Otsuka, A.V. Finn, H.R. Davis, M. Joner, R. Virmani, Pathophysiology of native coronary, vein graft, and in-stent atherosclerosis, Nat Rev Cardiol 13(2) (2016) 79-98.
[31] M.G. Davies, P.O. Hagen, Pathophysiology of vein graft failure: a review, Eur. J. Vasc. Endovasc. Surg.
9(1) (1995) 7-18.
[32] A.C. Newby, A.B. Zaltsman, Molecular mechanisms in intimal hyperplasia, J. Pathol. 190(3) (2000) 300-9.
[33] M.A. Reidy, Regulation of Arterial Smooth Muscle Growth, in: S.M.M. Schwartz, Robert P. (Ed.), The Vascular Smooth Muscle Cell, Academic Press, San Diego, 1995, pp. 271-295.
CHAPTER I - Perivascular medical devices and drug eluting systems: Making the right choices
35 [34] S.M. Schwartz, E.R. O'Brien, D. DeBlois, C.M. Giachelli, Relevance of Smooth Muscle Replication and Development to Vascular Disease, in: S.M.M. Schwartz, Robert P. (Ed.), The Vascular Smooth Muscle Cell, Academic Press, San Diego, 1995, pp. 81-139.
[35] Y. Shi, J.E. O'Brien, A. Fard, J.D. Mannion, D. Wang, A. Zalewski, Adventitial Myofibroblasts Contribute to Neointimal Formation in Injured Porcine Coronary Arteries, Circulation 94(7) (1996) 1655-1664.
[36] N.A. Scott, G.D. Cipolla, C.E. Ross, B. Dunn, F.H. Martin, L. Simonet, J.N. Wilcox, Identification of a Potential Role for the Adventitia in Vascular Lesion Formation After Balloon Overstretch Injury of Porcine Coronary Arteries, Circulation 93(12) (1996) 2178-2187.
[37] J.N. Wilcox, R. Waksman, S.B. King, N.A. Scott, The role of the adventitia in the arterial response to angioplasty: The effect of intravascular radiation, Int. J. Radiat. Oncol. Biol. Phys. 36(4) (1996) 789-796.
[38] S. Sartore, A. Chiavegato, E. Faggin, R. Franch, M. Puato, S. Ausoni, P. Pauletto, Contribution of Adventitial Fibroblasts to Neointima Formation and Vascular Remodeling: From Innocent Bystander to Active Participant, Circ. Res. 89(12) (2001) 1111-1121.
[39] M.W. Majesky, Adventitia and Perivascular Cells, Arterioscler. Thromb. Vasc. Biol. 35(8) (2015) 31-35.
[40] M. Schillinger, E. Minar, Restenosis after percutaneous angioplasty: the role of vascular inflammation, Vascular health and risk management 1(1) (2005) 73-8.
[41] P.J. Shah, I. Gordon, J. Fuller, S. Seevanayagam, A. Rosalion, J. Tatoulis, J.S. Raman, B.F. Buxton, Factors affecting saphenous vein graft patency: clinical and angiographic study in 1402 symptomatic patients operated on between 1977 and 1999, J. Thorac. Cardiovasc. Surg. 126(6) (2003) 1972-1977.
[42] P. Klinkert, P.N. Post, P.J. Breslau, B.J.H. van, Saphenous vein versus PTFE for above-knee femoropopliteal bypass. A review of the literature, Eur. J. Vasc. Endovasc. Surg. 27(4) (2004) 357-62.
[43] H.R. Zurbrügg, F. Knollmann, M. Musci, M. Wied, M. Bauer, T. Chavez, A. Krukenberg, R. Hetzer, The biocompound method in coronary artery bypass operations: surgical technique and 3-year patency, Ann.
Thorac. Surg. 70(5) (2000) 1536-1540.
[44] E. Arvela, P. Kauhanen, A. Albäck, M. Lepäntalo, A. Neufang, F. Adili, T. Schmitz-Rixen, Initial Experience with a New Method of External Polyester Scaffolding for Infrainguinal Vein Grafts, Eur. J.
Cardiothorac. Surg. 38(4) (2009) 456-462.
[45] G.J. Murphy, A.C. Newby, J.Y. Jeremy, A. Baumbach, G.D. Angelini, A randomized trial of an external Dacron sheath for the prevention of vein graft disease: The Extent study, J. Thorac. Cardiovasc. Surg. 134(2) (2007) 504-505.
[46] R.W. Emery, E. Solien, U. Klima, Clinical evaluation of the eSVS Mesh: First-in-Man trial outcomes, ASAIO J. 61(2) (2015) 178-83.
[47] M. Genoni, D. Odavic, H. Loblein, O. Dzemali, Use of the eSVS Mesh: external vein support does not negatively impact early graft patency, Innovations (Phila) 8(3) (2013) 211-4.
[48] U. Klima, A.A. Elsebay, M.R. Gantri, J. Bangardt, G. Miller, R.W. Emery, Computerized tomographic angiography in patients having eSVS Mesh(R) supported coronary saphenous vein grafts: intermediate term results, J. Cardiothorac. Surg. 9 (2014).
[49] G. Rescigno, A. Angelini, A. D'Alfonso, L. Torracca, Coronary graft use of a new external mesh support, Interact. Cardiovasc. Thorac. Surg. 10(4) (2010) 645-647.
[50] R.W. Emery, E. Solien, J.D. Puskas, Implantation of the eSVS Mesh: Modification of Recommended Technique, Innovations (Phila) 10(2) (2015) 146-149.
[51] H.M. Nugent, A. Groothuis, P. Seifert, J.L. Guerraro, M. Nedelman, T. Mohanakumar, E.R. Edelman, Perivascular Endothelial Implants Inhibit Intimal Hyperplasia in a Model of Arteriovenous Fistulae: A Safety and Efficacy Study in the Pig, J.Vasc. Res. 39(6) (2002) 524-533.
[52] M.S. Conte, H.M. Nugent, P. Gaccione, I. Guleria, P. Roy-Chaudhury, J.H. Lawson, Multicenter phase I/II trial of the safety of allogeneic endothelial cell implants after the creation of arteriovenous access for hemodialysis use: The V-HEALTH study, J. Vasc. Surg. 50(6) (2009) 1359-1368.
[53] L. Mátyás, M. Berry, G. Menyhei, L. Tamás, G. Acsády, P. Cuypers, F. Halmos, A.C. de Vries, V.
Forgacs, G. Ingenito, R. Avelar, The Safety and Efficacy of a Paclitaxel-delivery Wrap for Preventing
CHAPTER I - Perivascular medical devices and drug eluting systems: Making the right choices
36 Peripheral Bypass Graft Stenosis: A 2-Year Controlled Randomized Prospective Clinical Study, Eur. J. Vasc.
Endovasc. Surg. 35(6) (2008) 715-722.
[54] Angiotech Pharmaceuticals, Safety Study of the Vascular Wrap Paclitaxel-Delivery Mesh for Hemodialysis Vascular Access. <https://clinicaltrials.gov/ct2/show/NCT01033357>, 2009-2013).
[55] Angiotech Pharmaceuticals, Safety and Efficacy of Angiotech Vascular Wrap Paclitaxel-Delivery Mesh for Hemodialysis Vascular Access. <https://clinicaltrials.gov/ct2/show/NCT00448708>, 2007-2011 (accessed 10.10.2016.).
[56] W.D. Paulson, N. Kipshidze, K. Kipiani, N. Beridze, M.V. DeVita, S. Shenoy, S.S. Iyer, Safety and efficacy of local periadventitial delivery of sirolimus for improving hemodialysis graft patency: first human experience with a sirolimus-delivery collagen membrane (Coll-R), Nephrol. Dial. Transplant. 27(3) (2012) 1219-24.
[57] C. Basile, K. Konner, C. Lomonte, The haemodialysis arteriovenous graft: is a new era coming?, Nephrol.
Dial. Transplant. 27(3) (2012) 876-878.
[58] Johann Wolfgang Goethe University Hospitals, Pilot Study to Asses the Function and Patency of Polyester-Coated Composite Bypasses From Autologous Varicose Veins.
<https://ClinicalTrials.gov/show/NCT00460291>, 2007).
[59] National University Hospital of Singapore, The eSVS Mesh External Saphenous Vein Support Trial (eSVS). <https://clinicaltrials.gov/ct2/show/NCT00777777>, 2008).
[60] Kips Bay Medical Inc, The eMESH 1 Feasibility Study (eMESH 1).
<https://clinicaltrials.gov/ct2/show/NCT01676376>, 2012-2015).
[61] G. Rescigno, C. Aratari, S.M. Matteucci, G. Gironi, A. D'Alfonso, L. Torracca, R. Parisi, N. Schicchi, V.
Cola, Saphenous Vein Graft Wrapping by Nitinol Mesh: A Word of Caution, Thorac. Cardiovasc. Surg.
[64] R.J. Laham, F.W. Sellke, E.R. Edelman, J.D. Pearlman, J.A. Ware, D.L. Brown, J.P. Gold, M. Simons, Local Perivascular Delivery of Basic Fibroblast Growth Factor in Patients Undergoing Coronary Bypass Surgery, Circulation 100(18) (1999) 1865-1871.
[65] Vascular Therapies Inc, Safety and Efficacy of the Sirolimus-Delivery Collagen Implant to Assess AV
Fistula Outcomes in Patients on Hemodialysis (ACCESS).
<https://clinicaltrials.gov/ct2/show/NCT02513303>, 2015).
[66] I. Mylonaki, F. Strano, S. Deglise, E. Allémann, F. Alonso, J.-M. Corpataux, C. Dubuis, J.-A. Haefliger, O. Jordan, F. Saucy, F. Delie, Perivascular sustained release of atorvastatin from a hydrogel-microparticle delivery system decreases intimal hyperplasia, J. Control. Release 232 (2016) 93-102.
[67] S.C. Owen, H. Li, W.G. Sanders, A.K. Cheung, C.M. Terry, Correlation of tissue drug concentrations with in vivo magnetic resonance images of polymer drug depot around arteriovenous graft, J. Control. Release 146(1) (2010) 23-30.
[68] C.D. Owens, W.J. Gasper, J. Walker, H. Alley, M.S. Conte, S.M. Grenon, Safety and Feasibility of Adjunctive Dexamethasone Infusion into the Adventitia of the Femoro-popliteal Artery Following Endovascular Revascularization, J. Vasc. Surg. 59(4) (2014) 1016-1024.
[69] C.M. Terry, L. Li, H. Li, I. Zhuplatov, D.K. Blumenthal, S.E. Kim, S.C. Owen, E.G. Kholmovski, K.D.
Fowers, R. Rathi, A.K. Cheung, In vivo evaluation of the delivery and efficacy of a sirolimus-laden polymer gel for inhibition of hyperplasia in a porcine model of arteriovenous hemodialysis graft stenosis, J. Control.
Release 160 (2012) 459-467.
[70] N.S. Jones, M.G. Glenn, L.A. Orloff, M.R. Mayberg, Prevention of microvascular thrombosis with controlled-release transmural heparin, Arch. Otolaryngol. Head Neck Surg. 116(7) (1990) 779-785.
CHAPTER I - Perivascular medical devices and drug eluting systems: Making the right choices
37 [71] P. Zilla, M. Wolf, N. Rafiee, L. Moodley, D. Bezuidenhout, M. Black, P. Human, T. Franz, Utilization of shape memory in external vein-graft meshes allows extreme diameter constriction for suppressing intimal hyperplasia: A non-human primate study, J. Vasc. Surg. 49(6) (2009) 1532-1542.
[72] P. Zilla, L. Moodley, M.F. Wolf, D. Bezuidenhout, M.S. Sirry, N. Rafiee, W. Lichtenberg, M. Black, T.
Franz, Knitted nitinol represents a new generation of constrictive external vein graft meshes, J. Vasc. Surg.
54(5) (2011) 1439-1450.
[73] T. Kuji, T. Masaki, K. Goteti, L. Li, S. Zhuplatov, C.M. Terry, W. Zhu, J.K. Leypoldt, R. Rathi, D.K.
Blumenthal, S.E. Kern, A.K. Cheung, Efficacy of local dipyridamole therapy in a porcine model of arteriovenous graft stenosis, Kidney Int. 69(12) 2179-2185.
[74] I. Skalský, O. Szárszoi, E. Filová, M. Pařízek, A. Lytvynets, J. Malušková, A. Lodererová, E. Brynda, V.
Lisá, Z. Burdíková, M. Čapek, J. Pirk, L. Bačáková, A perivascular system releasing sirolimus prevented intimal hyperplasia in a rabbit model in a medium-term study, Int. J. Pharm. 427(2) (2012) 311-319.
[75] X. Yu, T. Takayama, S.A. Goel, X. Shi, Y. Zhou, K.C. Kent, W.L. Murphy, L.-W. Guo, A rapamycin-releasing perivascular polymeric sheath produces highly effective inhibition of intimal hyperplasia, J. Control.
Release 191 (2014) 47-53.
[76] B. Kelly, M. Melhem, J. Zhang, G. Kasting, J. Li, M. Krishnamoorthy, S. Heffelfinger, S. Rudich, P.
Desai, P. Roy-Chaudhury, Perivascular paclitaxel wraps block arteriovenous graft stenosis in a pig model, Nephrol. Dial. Transplant. 21(9) (2006) 2425-2431.
[77] K.J. Lee, S.H. Park, J.Y. Lee, H.C. Joo, E.H. Jang, Y.-N. Youn, W. Ryu, Perivascular biodegradable microneedle cuff for reduction of neointima formation after vascular injury, J. Control. Release 192(0) (2014) 174-181.
[78] W.G. Sanders, P.C. Hogrebe, D.W. Grainger, A.K. Cheung, C.M. Terry, A biodegradable perivascular wrap for controlled, local and directed drug delivery, J. Control. Release 161(1) (2012) 81-89.
[79] X. Shi, G. Chen, L.-W. Guo, Y. Si, M. Zhu, S. Pilla, B. Liu, S. Gong, K.C. Kent, Periadventitial application of rapamycin-loaded nanoparticles produces sustained inhibition of vascular restenosis, PLoS One 9(2) (2014) e89227/1-e89227/12, 12 pp.
[80] A. Forte, M. Grossi, K.M. Turczynska, K. Svedberg, B. Rinaldi, M. Donniacuo, A. Holm, B. Baldetorp, M. Vicchio, M. De Feo, P. Santè, U. Galderisi, L. Berrino, F. Rossi, P. Hellstrand, B.-O. Nilsson, M. Cipollaro, Local inhibition of ornithine decarboxylase reduces vascular stenosis in a murine model of carotid injury, Int.
J. Cardiol. 168(4) (2013) 3370-3380.
[81] M.-J. Jung, J.-S. Kwon, N.-K. Park, Y.-K. Kim, T.J. Shim, I.H. Jeong, J.-W. Bae, K.-K. Hwang, D.-W.
Kim, M.-C. Cho, Perivascular delivery of rapamycin in pluronic gel inhibits neointimal hyperplasia in a rat carotid artery injury model, and the complementary role of carotid arteriography, Korean Circ. J. 38(2) (2008) 80-86.
[82] T. Schachner, Y. Zou, A. Oberhuber, A. Tzankov, T. Mairinger, G. Laufer, J.O. Bonatti, Local application of rapamycin inhibits neointimal hyperplasia in experimental vein grafts, Ann. Thorac. Surg. 77(5) (2004) 1580-1585.
[83] Y. Hu, Y. Zou, H. Dietrich, G. Wick, Q. Xu, Inhibition of Neointima Hyperplasia of Mouse Vein Grafts by Locally Applied Suramin, Circulation 100(8) (1999) 861-868.
[84] N. Ishizaka, J. Taguchi, Y. Kimura, Y. Ikari, T. Aizawa, M. Togo, K. Miki, K. Kurokawa, M. Ohno, Effects of a single local administration of cilostazol on neointimal formation in balloon-injured rat carotid artery, Atherosclerosis 142(1) (1999) 41-46.
[85] G.J. Fulton, M.G. Davies, L. Barber, E. Svendsen, P.-O. Hagen, Locally Applied Antisense Oligonucleotide to Proliferating Cell Nuclear Antigen Inhibits Intimal Thickening in Experimental Vein Grafts, Ann Vasc Surg 12(5) (1998) 412-417.
[86] J. Taguchi, J. Abe, H. Okazaki, M. Ochiai, M. Ohno, Y. Takuwa, K. Kurokawa, Angiotensin converting enzyme inhibitors or DuP753 prevent neointimal formation following balloon injury with single topical or multiple systemic application, Biochem. Biophys. Res. Commun. 196(2) (1993) 969-74.
[87] J. Li, B. Wang, Y. Wang, Thermo-sensitive polymers for controlled-release drug delivery systems, Int. J.
Pharmacol. 2(5) (2006) 513-519.
CHAPTER I - Perivascular medical devices and drug eluting systems: Making the right choices
38 [88] M. Simons, E.R. Edelman, J.-L. DeKeyser, R. Langer, R.D. Rosenberg, Antisense c-myb oligonucleotides inhibit intimal arterial smooth muscle cell accumulation in vivo, Nature 359(6390) (1992) 67-70.
[89] B. Madhu, I. Elmroth, A. Lundgren, B. Abrahamsson, B. Soussi, A novel evaluation of subcutaneous formulations by in vivo magnetic resonance imaging (MRI), Pharmac. Res. 45(3) (2002) 207-212.
[90] B. Jeong, Y.H. Bae, D.S. Lee, S.W. Kim, Biodegradable block copolymers as injectable drug-delivery systems, Nature 388(6645) (1997) 860-862.
[91] T. Masaki, R. Rathi, G. Zentner, J.K. Leypoldt, S.F. Mohammad, G.L. Burns, L. Li, S. Zhuplatov, T.
Chirananthavat, S.-J. Kim, S. Kern, J. Holman, S.W. Kim, A.K. Cheung, Inhibition of neointimal hyperplasia in vascular grafts by sustained perivascular delivery of paclitaxel, Kidney Int. 66(5) (2004) 2061-2069.
[92] G.M. Zentner, R. Rathi, C. Shih, J.C. McRea, M.-H. Seo, H. Oh, B.G. Rhee, J. Mestecky, Z. Moldoveanu, M. Morgan, S. Weitman, Biodegradable block copolymers for delivery of proteins and water-insoluble drugs, J. Control. Release 72(1–3) (2001) 203-215.
[93] W. Zhu, T. Masaki, Y.H. Bae, R. Rathi, A.K. Cheung, S.E. Kern, Development of a sustained-release system for perivascular delivery of dipyridamole, J. Biomed. Mater. Res. B 77B(1) (2006) 135-143.
[94] B. Jeong, Y.H. Bae, S.W. Kim, In situ gelation of PEG-PLGA-PEG triblock copolymer aqueous solutions and degradation thereof, J. Biomed. Mater. Res. 50(2) (2000) 171-177.
[95] R.L. Dunn, The Atrigel drug delivery system, Drugs Pharm. Sci. 126(Modified-Release Drug Delivery Technology) (2003) 647-655.
[96] A. Chaux, X.M. Ruan, M.C. Fishbein, Y. Ouyang, S. Kaul, J.A. Pass, J.M. Matloff, Perivascular delivery of a nitric oxide donor inhibits neointimal hyperplasia in vein grafts implanted in the arterial circulation, J.
Thorac. Cardiovasc. Surg. 115(3) (1998) 604-14.
[97] B. Flick, C.E. Talsness, R. Jäckh, R. Buesen, S. Klug, Embryotoxic potential of N-methyl-pyrrolidone (NMP) and three of its metabolites using the rat whole embryo culture system, Toxicol. Appl. Pharm. J. 237(2) (2009) 154-167.
[98] A.M. Saillenfait, F. Gallissot, I. Langonné, J.P. Sabaté, Developmental toxicity of N-methyl-2-pyrrolidone administered orally to rats, Food Chem. Toxicol. 40(11) (2002) 1705-1712.
[99] A. Hatefi, B. Amsden, Biodegradable injectable in situ forming drug delivery systems, J. Control. Release 80(1–3) (2002) 9-28.
[100] A. Chajara, M. Raoudi, B. Delpech, H. Levesque, Inhibition of arterial cells proliferation in vivo in injured arteries by hyaluronan fragments, Atherosclerosis 171(1) (2003) 15-9.
[101] G.A. Ferns, M. Konneh, C. Rutherford, E. Woolaghan, E.E. Anggard, Hyaluronan (HYAL-BV 5200) inhibits neo-intimal macrophage influx after balloon-catheter induced injury in the cholesterol-fed rabbit, Atherosclerosis 114(2) (1995) 157-64.
[102] S.P. Evanko, J.C. Angello, T.N. Wight, Formation of hyaluronan- and versican-rich pericellular matrix is required for proliferation and migration of vascular smooth muscle cells, Arterioscler. Thromb. Vasc. Biol.
19(4) (1999) 1004-13.
[103] N. Nagy, T. Freudenberger, A. Melchior-Becker, K. Rock, M. Ter Braak, H. Jastrow, M. Kinzig, S.
Lucke, T. Suvorava, G. Kojda, A.A. Weber, F. Sorgel, B. Levkau, S. Ergun, J.W. Fischer, Inhibition of hyaluronan synthesis accelerates murine atherosclerosis: novel insights into the role of hyaluronan synthesis, Circulation 122(22) (2010) 2313-22.
[104] F.E. Lennon, P.A. Singleton, Hyaluronan regulation of vascular integrity, Am. J. Cardiovasc. Dis. 1(3) (2011) 200-13.
[105] B. Sadowitz, K. Seymour, V. Gahtan, K.G. Maier, The role of hyaluronic acid in atherosclerosis and intimal hyperplasia, J Surg Res 173(2) (2012) e63-72.
[106] D. Mishaly, I. Fishbein, D. Moscovitz, G. Golomb, Site-specific delivery of colchicine in rat carotid artery model of restenosis, J. Control. Release 45(1) (1997) 65-73.
[107] T.R. Kohler, P.M. Toleikis, D.M. Gravett, R.L. Avelar, Inhibition of neointimal hyperplasia in a sheep model of dialysis access failure with the bioabsorbable vascular wrap paclitaxel-delivery mesh, J. Vasc. Surg.
45(5) (2007) 1029-1038.
CHAPTER I - Perivascular medical devices and drug eluting systems: Making the right choices
39 [108] N.M.M. Pires, B.L. van der Hoeven, M.R. de Vries, L.M. Havekes, B.J. van Vlijmen, W.E. Hennink, P.H.A. Quax, J.W. Jukema, Local perivascular delivery of anti-restenotic agents from a drug-delivery poly(-caprolactone) stent cuff, Biomaterials 26(26) (2005) 5386-5394.
[109] S.G.E. Barker, L.C. Tilling, G.C. Miller, J.E. Beesley, G. Fleetwood, G.T. Stavri, P.A. Baskerville, J.F.
Martin, The adventitia and atherogenesis: removal initiates intimal proliferation in the rabbit which regresses on generation of a ‘neoadventitia’, Atherosclerosis 105(2) (1994) 131-144.
[110] J.K. Jackson, J. Smith, K. Letchford, K.A. Babiuk, L. Machan, P. Signore, W.L. Hunter, K. Wang, H.M.
Burt, Characterization of perivascular poly(lactic-co-glycolic acid) films containing paclitaxel, Int. J. Pharm.
283(1–2) (2004) 97-109.
[111] J. Huang, J. Zhang, A. Pathak, J. Li, G.A. Stouffer, Perivascular Delivery of Blebbistatin Reduces Neointimal Hyperplasia after Carotid Injury in the Mouse, J. Pharmacol. Exp. Ther. 336(1) (2011) 116-126.
[112] G. Golomb, I. Fishbein, S. Banai, D. Mishaly, D. Moscovitz, S.D. Gertz, A. Gazit, E. Poradosu, A.
Levitzki, Controlled delivery of a tyrphostin inhibits intimal hyperplasia in a rat carotid artery injury model, Atherosclerosis 125(2) (1996) 171-182.
[113] R. Brauner, H. Laks, D.C. Drinkwater, Jr., G. Chaudhuri, O. Shvarts, T. Drake, S. Bhuta, D. Mishaly, I.
Fishbein, G. Golomb, Controlled periadventitial administration of verapamil inhibits neointimal smooth muscle cell proliferation and ameliorates vasomotor abnormalities in experimental vein bypass grafts, J.
Thorac. Cardiovasc. Surg. 114(1) (1997) 53-63.
[114] Q.-A. Thai, E.M. Oshiro, R.J. Tamargo, Inhibition of experimental vasospasm in rats with the periadventitial administration of ibuprofen using controlled-release polymers, Stroke 30(1) (1999) 140-147.
[115] P.E. Signore, L.S. Machan, J.K. Jackson, H. Burt, P. Bromley, J.E. Wilson, B.M. McManus, Complete inhibition of intimal hyperplasia by perivascular delivery of paclitaxel in balloon-injured rat carotid arteries, J. Vasc. Interv. Radiol. 12 (2001) 79-88.
[116] S. Kawatsu, K. Oda, Y. Saiki, Y. Tabata, K. Tabayashi, External Application of Rapamycin-Delivery Film at Anastomotic Sites Inhibits Neointimal Hyperplasia in a Canine Model, Ann. Thorac. Surg. 84(2) (2007) 560-567.
[117] E. Filova, M. Parizek, J. Olsovska, Z. Kamenik, E. Brynda, T. Riedel, M. Vandrovcova, V. Lisa, L.
Machova, I. Skalsky, O. Szarszoi, T. Suchy, L. Bacakova, Perivascular sirolimus-delivery system, Int. J.
Pharm. 404(1–2) (2011) 94-101.
[118] R. Roeder, J. Wolfe, N. Lianakis, T. Hinson, L.A. Geddes, J. Obermiller, Compliance, elastic modulus, and burst pressure of small-intestine submucosa (SIS), small-diameter vascular grafts, J. Biomed. Mater. Res.
47(1) (1999) 65-70.
[119] A. Longchamp, F. Alonso, C. Dubuis, F. Allagnat, X. Berard, P. Meda, F. Saucy, J.-M. Corpataux, D.
Sébastien, J.-A. Haefliger, The use of external mesh reinforcement to reduce intimal hyperplasia and preserve the structure of human saphenous veins, Biomaterials 35(9) (2014) 2588-2599.
[120] J.Y. Jeremy, P. Gadsdon, N. Shukla, V. Vijayan, M. Wyatt, A.C. Newby, G.D. Angelini, On the biology of saphenous vein grafts fitted with external synthetic sheaths and stents, Biomaterials 28(6) (2007) 895-908.
[121] J.Y. Jeremy, R. Bulbulia, J.L. Johnson, P. Gadsdon, V. Vijayan, N. Shukla, F.C.T. Smith, G.D. Angelini, A bioabsorbable (polyglactin), nonrestrictive, external sheath inhibits porcine saphenous vein graft thickening,
[121] J.Y. Jeremy, R. Bulbulia, J.L. Johnson, P. Gadsdon, V. Vijayan, N. Shukla, F.C.T. Smith, G.D. Angelini, A bioabsorbable (polyglactin), nonrestrictive, external sheath inhibits porcine saphenous vein graft thickening,