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Review Article

Drug-eluting stents: a new treatment in the prevention of restenosis Part I: experimental studies

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Pages 51-61 | Received 16 May 2003, Accepted 03 Jul 2003, Published online: 23 May 2017

References

  • Serruys PW, de Jaegere P, Kiemeneij F, Macaya C, Rutsch W, Heyndrickx G, Emanuelsson H, Marco J, Legrand V, Materne P. Belardi J, Sigwart U, Colombo A, Goy JJ, van den Heuvel P. Delcan J, Morei M-A. A comparison of bal-loon-expandable-stent implantation with balloon angioplasty in patients with coronary artery disease. Benestent Study Group. N Engl J Med 1994; 331: 489–95.
  • Fischman DL, Leon MB, Bairn DS, Schatz RA, Savage MP, Penn I, Detre K, Veltri L, Ricci D, Nobuyoshi M, Cle-man M, Heuser R, Almond D, Teirstein PS, Fish RD, Colombo A, Brinker J, Moses J, Shaknovich A, Hirshfeld J, Bailey S, Ellis S, Rake R, Goldberg S. A randomized com-parison of coronary-stent placement and balloon angio-plasty in the treatment of coronary artery disease. Stent Restenosis Study Investigators. N Engl J Med 1994; 331: 496–501.
  • Mudra H, Di Mario C, de Jaegere P, Figulla HR, Macaya C, Zahn R, Wennerblom B, Rutsch W, Voudris V, Regar E, Henneke KH, Schachinger V, Zeiher A. Randomized com-parison of coronary stent implantation under ultrasound or angiographic guidance to reduce stent restenosis (OPTICUS Study). Circulation 2001; 104: 1343–9.
  • Virmani R, Farb A. Pathology of in-stent restenosis. Curr Opin Lipidol 1999; 10: 499–506.
  • Bult H. Restenosis: a challenge for pharmacology. Trends Pharmacol Sci 2000; 21: 274–9.
  • Meurice T, Bauters C, Hermant X, Codron V, VanBelle E, Mc Fadden EP, Lablanche J, Bertrand ME, Amouyel P. Effect of ACE inhibitors on angiographic restenosis after coronary stenting (PARIS): a randomised, double-blind, placebo-controlled trial. Lancet 2001; 357: 1321–4.
  • Serruys PW, Foley DP, Pieper M, Kleijne JA, de Feyter on behalf of the TRAPIST investigators PJ. The TRAPIST Study. A multicentre randomized placebo controlled clinical trial of trapidil for prevention of restenosis after coronary stenting, measured by 3-D intravascular ultrasound. Eur Heart J2001; 22: 1938–47.
  • Holmes DR, Jr., Savage M, Lablanche JM, Grip L, Serruys PW, Fitzgerald P, Fischman D, Goldberg S, Brinker JA, Zeiher AM, Shapiro LM, Willerson J, Davis BR, Fergu-son JJ, Popma J, King SB, III, Lincoff AM, Tcheng JE, Chan R, Granett JR, Poland M. Results of Prevention of REStenosis with Tranilast and its Outcomes (PRESTO) trial. Circulation 2002; 106: 1243–50.
  • Kastrati A, Schuhlen H, Hausleiter J, Walter H, Zitzmann-Roth E, Hadamitzky M, Elezi S, Ulm K, Dirschinger J, Neu-mann FJ, Schömig A. Restenosis after coronary stent place-ment and randomization to a 4-week combined antiplatelet or anticoagulant therapy: six-month angiographic follow-up of the Intracoronary Stenting and Antithrombotic Regimen (TSAR) Trial. Circulation 1997; 96: 462–7.
  • Acute platelet inhibition with abciximab does not reduce in-stent restenosis (ERASER study). The ERASER Inves-tigators. Circulation 1999; 100: 799–806.
  • Lee CW, Chae JK, Lim HY, Hong MK, Kim JJ, Park SW, Park SJ. Prospective randomized trial of corticosteroids for the prevention of restenosis after intracoronary stent implan-tation. Am Heart J 1999; 138: 60–3.
  • Eccleston DS, Horrigan MC, Ellis SG. Rationale for local drug delivery. Semin Interv Cardiol 1996; 1: 8–16.
  • Brieger D, Topol E. Local drug delivery systems and pre-vention of restenosis. Cardiovasc Res 1997; 35: 405–13.
  • Heldman AW, Cheng L, Jenkins GM, Heller PF, Kim DW, Ware M, Jr., Nater C, Hruban RH, Rezai B, Abella BS, Bunge KE, Kinsella JL, Sollott SJ, Lakatta EG, Brinker JA, Hunter WL, Froehlich JP. Paclitaxel stent coating inhibits neointimal hyperplasia at 4 weeks in a porcine model of coronary restenosis. Circulation 2001; 103: 2289–95.
  • Palmaz JC. Review of polymeric graft materials for endovas-cular applications. J Vasc Interv Radiol 1998; 9: 7–13.
  • Whelan DM, van Beusekom HM, van der Giessen WJ. Mechanisms of drug loading and release kinetics. Semin Interv Cardiol 1998; 3: 127–31.
  • Alt E, Haehnel I, Beilharz C, Prietzel K, Preter D, Stem-berger A, Fliedner T, Erhardt W, Schömig A. Inhibition of neointima formation after experimental coronary artery stenting. A new biodegradable stent coating releasing hirudin and the prostacyclin analogue iloprost. Circulation 2000; 101: 1453–8.
  • De Scheerder IK, Wilczek KL, Verbeken EV, Vandorpe J, Lan PN, Schacht E, De Geest H, Piessens J. Biocompati-bility of polymer-coated oversized metallic stents implanted in normal porcine coronary arteries. Atherosclerosis 1995; 114: 105–14.
  • van der Giessen WJ, Lincoff AM, Schwartz RS, van Beusekom HM, Serruys PW, Holmes DR, Jr., Ellis SG, Topol EJ. Marked inflammatory sequelae to implantation of biodegradable and nonbiodegradable polymers in porcine coronary arteries. Circulation 1996; 94: 1690–7.
  • Cumberland DC, Gunn J, Malik N, Holt CM. Biomimicry 1: PC. Semi Interv Cardiol 1998; 3: 149–50.
  • Lewis AL, Tolhurst LA, Stratford PW. Analysis of a phos-phorylcholine-based polymer coating on a coronary stent pre- and post-implantation. Biomaterials 2002; 23: 1697–1706.
  • Aggarwal RK, Ireland DC, Azrin MA, Ezekowitz MD, de Bono DP, Gershlick AH. Antithrombotic potential of poly-mer-coated stents eluting platelet glycoprotein IIb/IIIa recep-tor antibody. Circulation 1996; 94: 3311–7.
  • Hwang CW, Wu D, Edelman ER. Physiological transport forces govern drug distribution for stent-based delivery. Cir-culation 2001; 104: 600–5.
  • Hwang CW, Edelman ER. Arterial ultrastructure influences transport of locally delivered drugs. Circ Res 2002; 90: 826–32.
  • Hardhammar PA, van Beusekom HM, Emanuelsson HU, Hofma SH, Albertsson PA, Verdouw PD, Boersma E, Ser-ruys PW, van der Giessen WJ. Reduction in thrombotic events with heparin-coated Palmaz-Schatz stents in normal porcine coronary arteries. Circulation 1996; 93: 423–30.
  • De Scheerder, I, Wang K, Wilczek K, Meuleman D, Van Amsterdam R, Vogel G, Piessens J, Van de Werf F. Experimental study of thrombogenicity and foreign body reaction induced by heparin-coated coronary stents. Circulation 1997; 95: 1549–53.
  • Ahn YK, Jeong MH, Kim JW, Kim SH, Cho JH, Cho JG, Park CS, Juhng SW, Park JC, Kang JC. Preventive effects of the heparin-coated stent on restenosis in the porcine model. Cathet Cardiovasc Intervent 1999; 48: 324–30.
  • Matsumoto Y, Shimokawa H, Morishige K, Eto Y, Takeshita A. Reduction in neointimal formation with a stent coated with multiple layers of releasable heparin in porcine coronary arteries. J Cardiovas Pharmacol 2002; 39: 513–22.
  • Gershlick AH. Local delivery of glycoprotein IIb/IIIa recep-tor inhibitors using drug eluting stents. Semin Interv Car-diol 1998; 3: 185–90.
  • Baron JH, Gershlick AH, Hogrefe K, Armstrong J, Holt CM, Aggarwal RK, Azrin M, Ezekowitz M, de Bono DP. In vitro evaluation of c7E3-Fab (ReoProTm) eluting polymer-coated coronary stents. Cardiovasc Res 2000; 46: 585–94.
  • Fontaine AB, Borsa JJ, Dos PS, Hoffer EK, Bloch RD, Starr F, So C. Evaluation of local abciximab delivery from the surface of a polymer-coated covered stent: in vivo canine studies. J Vasc Interv Radiol 2001; 12: 487–92.
  • Alt E, Seliger C. Antithrombotic stent coatings: hirudin/iloprost combination. Semin Interv Cardiol 1998; 3: 177–83.
  • Muller DW, Golomb G, Gordon D, Levy RJ. Site-specific dexamethasone delivery for the prevention of neointimal thickening after vascular stent implantation. Coron Artery Dis 1994; 5: 435–42.
  • Lincoff AM, Furst JG, Ellis SG, Tuch RJ, Topol EJ. Sus-tained local delivery of dexamethasone by a novel intravas-cular eluting stent to prevent restenosis in the porcine coro-nary injury model. J Am Coll Cardiol 1997; 29: 808–16.
  • De Scheerder I, Wang K, Wilczek K, Van Dorpe J, Verbeken E, Desmet W, Schacht E, Piessens J. Local methylpred-nisolone inhibition of foreign body response to coated intra-coronary stents. Coron Artery Dis 1996; 7: 161–6.
  • Huang Y, Wang L, Verweire I, Qiang B, Liu X, Verbeken E, Schacht E, De Scheerder, I. Optimization of local methyl-prednisolone delivery to inhibit inflammatory reaction and neointimal hyperplasia of coated coronary stents. J Invasive Cardiol 2002; 14: 505–13.
  • Huang Y, Liu X, Wang L, Verbeken E, Li S, and De Scheerder. I. Local methylprednisolone delivery using a bio-divysio phosphorylcholine coated drug delivery stent reduces inflammation and neointimal hyperplasia in a porcine coro-nary stent model. Circulation 2002; 106 suppl. II: 11–357.
  • Gregory CR, Pratt RE, Huie P, Shorthouse R, Dzau VJ, Billingham ME, Morris RE. Effects of treatment with cyclosporine, FK 506, rapamycin, mycophenolic acid, or deoxyspergualin on vascular muscle proliferation in vitro and in vivo. Transplant Proc 1993; 25: 770–1.
  • Marx SO, Jayaraman T, Go LO, Marks AR. Rapamycin-FKBP inhibits cell cycle regulators of proliferation in vas-cular smooth muscle cells. CircRes 1995; 76: 412–7.
  • Mohacsi PJ, Tiiller D, Hulliger B, Wijngaard PL. Different inhibitory effects of immunosuppressive drugs on human and rat aortic smooth muscle and endothelial cell prolifer-ation stimulated by platelet-derived growth factor or endothelial cell growth factor. J Heart Lung Transplant 1997; 16: 484–92.
  • Gallo R, Padurean A, Jayaraman T, Marx S, Roque M, Adelman S, Chesebro J, Fallon J, Fuster V, Marks A, Badi-mon JJ. Inhibition of intimal thickening after balloon angioplasty in porcine coronary arteries by targeting regulators of the cell cycle. Circulation 1999; 99: 2164–70.
  • Poon M, Badimon JJ, Fuster V. Overcoming restenosis with sirolimus: from alphabet soup to clinical reality. Lancet 2002; 359: 619–22.
  • Poon M, Marx SO, Gallo R, Badimon JJ, Taubman MB, Marks AR. Rapamycin inhibits vascular smooth muscle cell migration. J Clin Invest 1996; 98: 2277–83.
  • Sun J, Marx SO, Chen HJ, Poon M, Marks AR, Rabbani LE. Role for p27”-’P1 in vascular smooth muscle cell migra-tion. Circulation 2001; 103: 2967–72.
  • Suzuki T, Kopia G, Hayashi S, Bailey LR, Llanos G, Wilensky R, Klugherz BD, Papandreou G, Narayan P, Leon MB, Yeung AC, Tio F, Tsao PS, Falotico R, Carter AJ. Stent-based delivery of sirolimus reduces neointimal for-mation in a porcine coronary model. Circulation 2001; 104: 1188–93.
  • Klugherz BD, Llanos G, Lieuallen W, Kopia GA, Papan-dreou G, Narayan P, Sasseen B, Adelman SJ, Falotico R, Wilensky RL. Twenty-eight-day efficacy and phamacoki-netics of the sirolimus-eluting stent. Coron Artery Dis 2002; 13: 183–8.
  • Kopia G A, Snead D, Falotico R, Lauer M, Fische11 T, Devries J, Carter A. J, Tio F, Hulsebos L, Turck P, Snodgrass J, and Dooley J. Pharmacokinetics and pharma-codynamics of sirolimus-eluting stents. Am J Cardiol 2002; 90 suppl. 6A: 115H.
  • Aggarwal M, Tsao PS., Kopia G, Yeung A, Tio F, Falotico R, Carter A J Stent based delivery of sirolimus is associated with increased levels of p271dP1 without long-term suppression of neointimal hyperplasia in the porcine model. Circulation 2002; 106 suppl. II: 11–357.
  • Guyon P, Teiger E, Chevalier B, Glatt B, and Royer T. Rapamycin-coated stent effectiveness in high arterial injury damage: a pig model experimentation. Am J Cardiol 2002; 90 suppl. 6A: 73H.
  • Schiff PB, Fant J, Horwitz SB. Promotion of microtubule assembly in vitro by taxol. Nature 1979; 277: 665–7.
  • Rowinsky EK, Donehower RC. Paclitaxel (taxol). N Engl J Med 1995; 332: 1004–14.
  • Axel DI, Kunert W, Goggelmann C, Oberhoff M, Herdeg C, Kuttner A, Wild DH, Brehm BR, Riessen R, Koveker G, Karsch KR. Paclitaxel inhibits arterial smooth muscle cell proliferation and migration in vitro and in vivo using local drug delivery. Circulation 1997; 96: 636–45.
  • Drachman DE, Edelman ER, Seifert P, Groothuis AR, Bornstein DA, Kamath KR, Palasis M, Yang D, Nott SH, Rogers C. Neointimal thickening after stent delivery of pacli-taxel: change in composition and arrest of growth over six months. J Am Coll Cardiol 2000; 36: 2325–32.
  • Farb A, Heller PF, Shroff S, Cheng L, Kolodgie FD, Carter AJ, Scott DS, Froehlich J, Virmani R. Pathological analysis of local delivery of paclitaxel via a polymer-coated stent. Circulation 2001; 104: 473–9.
  • Hong MK, Kornowski R, Bramwell 0, Ragheb AO, Leon MB. Paclitaxel-coated Gianturco-Roubin II (GR II) stents reduce neointimal hyperplasia in a porcine coronary in-stent restenosis model. Coron Artery Dis 2001; 12: 513–5.
  • McClean D, Finkelstein A, Kar S, Takizawa K, Honda T, Back N, Park K, Fishbein MC, Makkar R, Litvack F, Eigler N. Local drug delivery using a stent with programmable pharmacokinetics in vitro and in porcine coronary arteries. Circulation 2002; 106 suppl. II: 11–447.
  • Zohlnhöfer D, Klein CA, Richter T, Brandl R, Murr A, Niihrenberg T, Schömig A, Baeuerle PA, Neumann FJ. Gene expression profiling of human stent-induced neointima by cDNA array analysis of microscopic specimens retrieved by helix cutter atherectomy: Detection of FK506-binding pro-tein 12 upregulation. Circulation 2001; 103: 1396–402.
  • Matter C M, Kurz DJ, Wnendt S, Kozai T, Jaschko A, Joch H, Griinenfelder J, Ziind, G, Liischer T F. Tacrolimus (FK506), but not sirolimus (rapamycin) targets human vas-cular smooth muscle cells (VSMC), but spares endothelial cells (EC) - implications for drug-eluting stents. Circulation 2002; 106 suppl. II: 11–356.
  • Alt EU, Rihm M, Wolf T, Reimer C, Valina C, Pinkernell K. Implantation of tacrolimus coated stents in the pig coro-nary overstretch model at 1, 3 and 6 months. Circulation 2002; 106 suppl. II: 11–448.
  • Rihm M, Steimer W, Wolf T, Reimers C, and Alt E. Absence of systemic, but high local vessel wall concentrations following implantation of lipophilic immunosuppressant tacrolimus coated stents. Circulation 2002; 106 suppl. II: 11–355.
  • Wieneke H, Dirsch O, Sawitowski T, Wnendt S, Brauer H, Gu JL, Dahmen U, Erbel R. Synergistic effects of a novel nanoporous stent coating and tacrolimus on intima prolif-eration in rabbits. Eur Heart J 2002; 23 suppl.: 692.
  • Schuurman HJ, Cottens S, Fuchs S, Joergensen J, Meerloo T, Sedrani R, Tanner M, Zenke G, Schuler W SDZ RAD, a new rapamycin derivative: synergism with cyclosporine. Transplantation 1997; 64: 32–5.
  • Schuler W, Sedrani R, Cottens S, Haberlin B, Schulz M, Schuurman HJ, Zenke G, Zerwes HG, Schreier MH. SDZ RAD, a new rapamycin derivative: pharmacological prop-erties in vitro and in vivo. Transplantation 1997; 64: 36–42.
  • Honda H, Kar S, Honda T, Takizawa K, Meguro T, Fishbein MC, Makkar R, Eigler N, Litvack F. Everolimus-eluting stents significantly inhibit neointimal hyperplasia in an experimental pig coronary model. Am J Cardiol 2002; 90 suppl. 6A: 73H.
  • Honda T, Kar S, Honda H, Takizawa K, McClean D, Fishbein MC, Eigler N, Litvack F. Stent-based delivery of everolimus leads to complete vessel wall healing without tox-icity in a 90-day porcine model. Am J Cardiol 2002; 90 suppl. 6A: 80H.
  • Schwartz RS, Burke SE, Cromack K, Tarcha P, Chen S, Robinson KA. Marked neointimal inhibition from a drug eluting stent: effects of local ABT-578 in the porcine coro-nary model. Circulation 2002; 106 suppl. II: 11–448.
  • New G, Moses JW, Roubin GS, Leon MB, Colombo A, Iyer SS, Tio FO, Mehran R, Kipshidze N. Estrogen-eluting, phosphorylcholine-coated stent implantation is associated with reduced neointimal formation but no delay in vascular repair in a porcine coronary model. Catheter Cardiovasc Interv 2002; 57: 266–71.
  • Santoian ED, Schneider JE, Gravanis MB, Foegh M, Tarazona N, Cipolla GD, King SB, III. Angiopeptin inhibits intimal hyperplasia after angioplasty in porcine coronary arteries. Circulation 1993; 88: 11–4.
  • Foegh ML, Asotra S, Conte JV, Howell M, Kagan E, Verma K, Ramwell PW. Early inhibition of myointimal pro-liferation by angiopeptin after balloon catheter injury in the rabbit. J Vasc Surg 1994; 19: 1084–91.
  • De Scheerder I, Wilczek K, Van Dorpe J, Verbeken E, Cathapermal S, Wang K, Desmet W, Schacht E, Foegh M, De Geest H, Piessens J. Local angiopeptin delivery usingcoated stents reduces neointimal proliferation in over-stretched porcine coronary arteries. J Invasive Cardiol 1996; 8: 215–22.
  • Armstrong J, Gunn J, Arnold N, Malik N, Chan KH, Vick T, Stratford P, Cumberland DC, Holt CM. Angiopeptin-eluting stents: observations in human vessels and pig coronary arteries. J Invasive Cardiol 2002; 14: 230–38.
  • Gobeil F, Laflamme M, Bouchard M, Campbell E, Wood M, St-Jacques P, Vincent J, Leclerc G. Biodivysio stent coated with metalloproteinase inhibitor reduces neointimal hyperplasia in a porcine coronary artery restenosis model. Circulation 2001; 104 suppl. II: 11–388.
  • Robinson KA, Chronos NAF, Royal G, Suh L, Cipolla GD, Virmani R, Stack R S. Actinomycin-D drug-eluting stents preserve lumen size and inhibit fibrocellular neointima in pig coronary arteries. Circulation 2001; 104 suppl. II: 11–506.
  • Fukumoto Y, Shimokawa H, Kozai T, Kadokami T, Kuwata K, Owada MK, Shiraishi T, Kuga T, Egashira K, Takeshita A. Tyrosine kinase inhibitor suppresses the (re) stenotic changes of the coronary artery after balloon injury in pigs. Cardiovasc Res 1996; 32: 1131–40.
  • Yamawaki T, Shimokawa H, Kozai T, Miyata K, Higo T, Tanaka E, Egashira K, Shiraishi T, Tamai H, Igaki K, Takeshita A. Intramural delivery of a specific tyrosine kinase inhibitor with biodegradable stent suppresses the restenotic changes of the coronary artery in pigs in vivo. J Am Coll Cardiol 1998; 32: 780–6.
  • Cooper JA. Effects of cytochalasin and phalloidin on actin. J Cell Biol 1987; 105: 1473–8.
  • Numaguchi K, Eguchi S, Yamakawa T, Motley ED, Inagami T. Mechanotransduction of rat aortic vascular smooth muscle cells requires RhoA and intact actin fila-ments. Circ Res 1999; 85: 5–11.
  • Bruijns RH, Bult H. Effects of local cytochalasin D deliv-ery on smooth muscle cell migration and on collar-induced intimal hyperplasia in the rabbit carotid artery. Br J Phar-macol 2001; 134: 473–83.
  • Olorundare OE, Simmons SR, Albrecht RM. CytochalasinD and E. effects on fibrinogen receptor movement and cytoskeletal reorganization in fully spread, surface-activated platelets: a correlative light and electron microscopic inves-tigation. Blood 1992; 79: 99–109.
  • Anderson SI, Hotchin NA, Nash GB. Role of the cytoskele-ton in rapid activation of CD1 lb/CD18 function and its subsequent downregulation in neutrophils. J Cell Sci 2000; 113: 2737–45.
  • Salu KJ, Yanming H, Bosmans JM, Bult H, Xiaoshun L, De Scheerder IK, Vrints CJ. Direct cytochalasin D stent coating inhibits neointimal formation in a porcine coronary model. Circulation 2001; 104 suppl. II: 11–506.
  • Salu KJ, Bosmans JM, Huang Y, Liu X, Li S, Wang L, Ver-beken E, Bult H, Vrints CJ, De Scheerder IK. Cytochalasin D-coated coronary stents inhibit neointimal formation in a porcine coronary model. Am J Cardiol 2002; 90 suppl. 6A: 71H.
  • Salu KJ, Bosmans JM, Bult H, Huang Y, Liu X, De Scheerder IK, Vrints CJ. Latrunculin A inhibits smooth muscle cell proliferation and neointimal formation in a porcine coronary stent model. Eur Heart J 2002; 23 suppl.: 143.
  • Salu KJ, Bosmans JM, Huang Y, Liu X, Li S, Wang L, Verbeken E, Bult H, Vrints CJ, De Scheerder IK. Latrunculin A coated coronary stents inhibit neointimal hyperplasia in a porcine coronary model. Circulation 2002; 106 suppl. II: 11–520.
  • van Beusekom HMM, Ferrero V, Harteveld MS, Punt MG, Rodjan S, van Dullemen, M, van der Giessen WJ. Quinapri-lat coated PC stents do not attenuate intimal thickening in a porcine coronary model. Eur Heart J2002; 23 suppl.: 691.
  • van Beusekom HMM, Regar E, Visser-van der Veer S, van Dullemen M, Rodjan S, Punt MG., Harteveld M, and van der Giessen WJ. Simvastatin coated PC stents do not attenuate intimal thickening in a porcine coronary model. Eur Heart J 2002; 23 suppl.: 691.
  • Stefanadis C, Tsiamis E, Vaina S, Stefanadi E, Tsekoura D, Toutouzas K, Poulis D, Toutouzas P. Stent-based delivery of combined chemotherapy with cis-platinum and mitoxan-drone in a porcine coronary model to prevent restenosis. Eur Heart J 2002; 23 suppl.: 143.
  • Swanson N, Hogrefe K, Javed Q, Malik N, Gershlick AH, VEGF-eluting stents reduce stent thrombosis, but not restenosis, in vivo. Eur Heart J 2002; 23 suppl.: 143.

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