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Bioprinting of freestanding vascular grafts and the regulatory considerations for additively manufactured vascular prostheses

  • Author Footnotes
    1 Sara Abdollahi and Joseph Boktor contributed equally to this article and should be considered as co-first authors.
    Sara Abdollahi
    Footnotes
    1 Sara Abdollahi and Joseph Boktor contributed equally to this article and should be considered as co-first authors.
    Affiliations
    Division of Cardiac Surgery, Johns Hopkins Hospital, Baltimore, Maryland
    Search for articles by this author
  • Author Footnotes
    1 Sara Abdollahi and Joseph Boktor contributed equally to this article and should be considered as co-first authors.
    Joseph Boktor
    Footnotes
    1 Sara Abdollahi and Joseph Boktor contributed equally to this article and should be considered as co-first authors.
    Affiliations
    Division of Cardiac Surgery, Johns Hopkins Hospital, Baltimore, Maryland

    Department of Biology, Johns Hopkins University, Baltimore, Maryland
    Search for articles by this author
  • Narutoshi Hibino
    Correspondence
    Reprint requests: Narutoshi Hibino, Division of Cardiac Surgery, The Johns Hopkins Hospital, Zayed 7107, 1800 Orleans Street, Baltimore, MD 21287.
    Affiliations
    Division of Cardiac Surgery, Johns Hopkins Hospital, Baltimore, Maryland
    Search for articles by this author
  • Author Footnotes
    1 Sara Abdollahi and Joseph Boktor contributed equally to this article and should be considered as co-first authors.
      Vasculature is the network of blood vessels of an organ or body part that allow for the exchange of nutrients and waste to and from every cell, thus establishing a circulatory equilibrium. Vascular health is at risk from a variety of conditions that includes disease and trauma. In some cases, medical therapy can alleviate the impacts of the condition. Intervention is needed in other instances to restore the health of abnormal vasculature. The main approaches to treat vascular conditions are endovascular procedures and open vascular reconstruction that often requires a graft to accomplish. However, current vascular prostheses have limitations that include size mismatch with the native vessel, risk of immunogenicity from allografts and xenografts, and unavailability of autografts. In this review, we discuss efforts in bioprinting, an emerging method for vascular reconstruction. This includes an overview of 3D printing processes and materials, graft characterization strategies and the regulatory aspects to consider for the commercialization of 3D bioprinted vascular prostheses.

      Abbreviations:

      3D (three-dimensional), 3DP (3D printing), ASTM (American Society for Testing and Materials), bFGF (basic fibroblast growth factor), CAD (computer-aided design), EBM (electron beam melting), ePTFE (expanded polytetrafluoroethylene), FDM (fused deposition modeling), FDA (United States Food and Drug Administration), FD&C Act (Federal Food, Drug, and Cosmetic Act), GelMA (gelatin methacryloyl), LOM (laminated object manufacturing), MEMS (microelectromechanical systems), MRI (magnetic resonance imaging), NIST (National Institute of Standards and Technology), NO (nitric oxide), PDGF (platelet-derived growth factor), PDMS (polydimethyl siloxane), PET (polyethylene terephthalate), PGS (poly(glycerol sebacate)), PMA (Premarket Approval), PMN (Premarket Notification), PTFE (polytetrafluoroethylene), SLA or SL (stereolithography), SLS (selective laser sintering), VEGF (vascular endothelial growth factor)
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      References

      1. Vascular Trauma: Society for Vascular Surgery (SVS); 2018. Available from: vascular.org. Accessed November 11, 2018.

        • Lüscher TF
        • Creager MA
        • Beckman JA
        • Cosentino F
        Diabetes and vascular disease.
        Circulation. 2003; 108: 1655-1661
        • Hans SS
        • Weaver MR
        • Bove PG
        • Long GW
        Endovascular and open vascular reconstruction: a practical approach.
        CRC Press, Boca Raton2017
      2. Endovascular versus surgical treatment in patients with carotid stenosis in the Carotid and Vertebral Artery Transluminal Angioplasty Study (CAVATAS): a randomised trial.
        Lancet. 2001; 357: 1729-1737
        • Wiebers DO
        Unruptured intracranial aneurysms: natural history, clinical outcome, and risks of surgical and endovascular treatment.
        Lancet. 2003; 362: 103-110
        • Bianchi C
        • Ballard JL
        • Bergan JH
        • Killeen J
        Vascular reconstruction and major resection for malignancy.
        Arch Surg. 1999; 134: 851-855
        • Nishinari K
        • Krutman M
        • Aguiar Junior S
        • et al.
        Surgical outcomes of vascular reconstruction in soft tissue sarcomas of the lower extremities.
        J Vasc Surg. 2015; 62: 143-149
        • Sgroi MD
        • Narayan RR
        • Lane JS
        • et al.
        Vascular reconstruction plays an important role in the treatment of pancreatic adenocarcinoma.
        J Vasc Surg. 2015; 61: 475-480
      3. Contegra® Pulmonary Valved Conduit Medtronic; 2018. Available from: www.medtronic.com.

        • Carney JP
        • Zhang LM
        • Larson JJ
        • et al.
        The Hancock® Valved conduit for right ventricular outflow tract reconstruction in sheep for assessing new devices.
        J Heart Valve Dis. 2017; 4: 472-480
        • Zehr BP
        • Niblick CJ
        • Downey H
        • Ladowski JS
        Limb salvage with cryovein cadaver saphenous vein allografts used for peripheral arterial bypass: role of blood compatibility.
        Ann Vasc Surg. 2011; 25: 177-181
      4. Peripheral Vascular Surgery for Large Vessel Vasculitis. Inflammatory diseases of blood vessels.

        • Pashneh-Tala S
        • MacNeil S
        • Claeyssens F
        The tissue-engineered vascular graft-past, present, and future.
        Tissue Eng B Rev. 2015; 22: 68-100
        • Amaro E
        • Pophal S
        • Zoldos J
        Vascular reconstruction in a neonate after iatrogenic injury during cardiac catheterization.
        Plast Reconstr Surg – Global Open. 2017; 5: e1600
        • Min S-K
        • Cho S
        • Kim H-Y
        • Kim SJ
        Pediatric vascular surgery review with a 30-year-experience in a tertiary referral center.
        Vasc Spec Int. 2017; 33: 47-54
        • Kohler C
        • Attigah N
        • Demirel S
        • Zientara A
        • Weber M
        • Schwegler I
        A technique for a self-made bifurcated graft with bovine pericardial patch in infectious vascular reconstruction.
        J Vasc Surg Cases Innov Tech. 2016; 2: 158-160
        • Stather PW
        • Howard AQ.
        A novel technique for bifurcated bovine plus omniflow aortic graft reconstruction.
        Eur J Vasc Endovasc Surg. 2017; 53: 104
        • August K.
        The anatomy and physiology of capillaries.
        Yale University Press, New Haven1922
        • Dale HH.
        The oliver-sharpey lectures On the Activity of the Capillary Blood Vessels, and its Relation to Certain Forms of Toxaemia: delivered before the Royal College of Physicians of London.
        Br Med J. 1923; 1: 1006-1010
        • Thiriet M.
        Anatomy and physiology of the circulatory and ventilatory systems.
        Springer, New York2014
        • Clark JM
        • Glagov S.
        Transmural organization of the arterial media. The lamellar unit revisited.
        Arteriosclerosis. 1985; 5: 19-34
        • Mirea O
        • Donoiu I
        • Pleşea IE
        Arterial aging: a brief review.
        Rom J Morphol Embryol. 2012; 53: 473-477
        • Prince EA
        • Ahn SH.
        Basic vascular neuroanatomy of the brain and spine: what the general interventional radiologist needs to know.
        Semin Interv Radiol. 2013; 30: 234-239
        • Weinberg C
        • Bell E.
        A blood vessel model constructed from collagen and cultured vascular cells.
        Science. 1986; 231: 397-400
        • Konig G
        • McAllister TN
        • Dusserre N
        • et al.
        Mechanical properties of completely autologous human tissue engineered blood vessels compared to human saphenous vein and mammary artery.
        Biomaterials. 2009; 30: 1542-1550
        • Song HHG
        • Rumma RT
        • Ozaki CK
        • Edelman ER
        • Chen CS
        Vascular tissue engineering: progress, challenges, and clinical promise.
        Cell Stem Cell. 2018; 22: 340-354
        • Vyas C
        • Pereira R
        • Huang B
        • Liu F
        • Wang W
        • Bartolo P
        Engineering the vasculature with additive manufacturing.
        Curr Opin Biomed Eng. 2017; 2: 1-13
        • Syedain Z
        • Reimer J
        • Lahti M
        • Berry J
        • Johnson S
        • Tranquillo RT
        Tissue engineering of acellular vascular grafts capable of somatic growth in young lambs.
        Nat Commun. 2016; 7: 12951
        • Lin C-H
        • Hsia K
        • Ma H
        • Lee H
        • Lu J-H
        In vivo performance of decellularized vascular grafts: a review article.
        Int J Mol Sci. 2018; 19: 2101
        • Schneider KH
        • Enayati M
        • Grasl C
        • et al.
        Acellular vascular matrix grafts from human placenta chorion: impact of ECM preservation on graft characteristics, protein composition and in vivo performance.
        Biomaterials. 2018; 177: 14-26
        • Datta P
        • Ayan B
        • Ozbolat IT
        Bioprinting for vascular and vascularized tissue biofabrication.
        Acta Biomater. 2017; 51: 1-20
        • Norotte C
        • Marga FS
        • Niklason LE
        • Forgacs G
        Scaffold-free vascular tissue engineering using bioprinting.
        Biomaterials. 2009; 30: 5910-5917
        • Hoch E
        • Tovar GEM
        • Borchers K
        Bioprinting of artificial blood vessels: current approaches towards a demanding goal.
        Eur J Cardio-Thorac Surg. 2014; 46: 767-778
        • Skardal A
        • Zhang J
        • McCoard L
        • Oottamasathien S
        • Prestwich GD
        Dynamically crosslinked gold nanoparticle – hyaluronan hydrogels.
        Adv Mater. 2010; 22: 4736-4740
        • Skardal A
        • Zhang J
        • McCoard L
        • Xu X
        • Oottamasathien S
        • Prestwich GD
        Photocrosslinkable hyaluronan-gelatin hydrogels for two-step bioprinting.
        Tissue Eng A. 2010; 16: 2675-2685
        • Skardal A
        • Zhang J
        • Prestwich GD
        Bioprinting vessel-like constructs using hyaluronan hydrogels crosslinked with tetrahedral polyethylene glycol tetracrylates.
        Biomaterials. 2010; 31: 6173-6181
        • Wu PK
        • Ringeisen BR.
        Development of human umbilical vein endothelial cell (HUVEC) and human umbilical vein smooth muscle cell (HUVSMC) branch/stem structures on hydrogel layers via biological laser printing (BioLP).
        Biofabrication. 2010; 2014111
        • Chua CK
        • Wong CH
        • Yeong WY
        Chapter Five – Material characterization for additive manufacturing.
        in: Chua CK Wong CH Yeong WY Standards, quality control, and measurement sciences in 3D printing and additive manufacturing. Academic Press, 2017: 95-137
      5. International A. ASTM ISO/ASTM52900-15 standard terminology for additive manufacturing – general principles – terminology. West Conshohocken, PA;2015.

        • Mohamed OA
        • Masood SH
        • Bhowmik JL
        Optimization of fused deposition modeling process parameters: a review of current research and future prospects.
        Adv Manuf. 2015; 3: 42-53
        • Wang X
        • Jiang M
        • Zhou Z
        • Gou J
        • Hui D
        3D printing of polymer matrix composites: a review and prospective.
        Compos B: Eng. 2017; 110: 442-458
        • Yun JS
        • Park T-W
        • Jeong YH
        • Cho JH
        Development of ceramic-reinforced photopolymers for SLA 3D printing technology.
        Appl Phys A. 2016; 122: 629
        • Wittbrodt BT
        • Glover AG
        • Laureto J
        • et al.
        Life-cycle economic analysis of distributed manufacturing with open-source 3-D printers.
        Mechatronics. 2013; 23: 713-726
        • Hinton TJ
        • Jallerat Q
        • Palchesko RN
        • et al.
        Three-dimensional printing of complex biological structures by freeform reversible embedding of suspended hydrogels.
        Sci Adv. 2015; 1: 1-10
        • Ong CS
        • Fukunishi T
        • Zhang H
        • et al.
        Biomaterial-free three-dimensional bioprinting of cardiac tissue using human induced pluripotent stem cell derived cardiomyocytes.
        Sci Rep. 2017; 7: 4566
        • Wu W
        • DeConinck A
        • Lewis JA
        Omnidirectional printing of 3D microvascular networks.
        Adv Mater. 2011; 23: H178-HH83
        • Pati F
        • Jang J
        • Lee JW
        • Cho D-W
        Extrusion bioprinting. Essentials of 3D biofabrication and translation.
        Elsevier, 2015: 123-152
        • Tabriz AG
        • Hermida MA
        • Leslie NR
        • Shu W
        Three-dimensional bioprinting of complex cell laden alginate hydrogel structures.
        Biofabrication. 2015; 7045012
        • Bertassoni LE
        • Cardoso JC
        • Manoharan V
        • et al.
        Direct-write bioprinting of cell-laden methacrylated gelatin hydrogels.
        Biofabrication. 2014; 6024105
        • Jakab K
        • Norotte C
        • Damon B
        • et al.
        Tissue engineering by self-assembly of cells printed into topologically defined structures.
        Tissue Eng Part A. 2008; 14: 413-421
        • Yu Y
        • Moncal KK
        • Li JQ
        • et al.
        Three-dimensional bioprinting using self-assembling scalable scaffold-free “tissue strands” as a new bioink.
        Sci Rep. 2016; 6: 28714
        • Moldovan NI
        • Hibino N
        • Nakayama K
        Principles of the Kenzan method for robotic cell spheroid-based three-dimensional bioprinting.
        Tissue Eng B: Rev. 2017; 23: 237-244
        • Ong CS
        • Yesantharao P
        • Hibino N
        3D and 4D scaffold-free bioprinting.
        in: 3D and 4D printing in biomedical applications: process engineering and additive manufacturing. 2019: 317-342
        • Egaña JT
        • Fierro FA
        • Krüger S
        • et al.
        Use of human mesenchymal cells to improve vascularization in a mouse model for scaffold-based dermal regeneration.
        Tissue Eng Part A. 2009; 15: 1191-1200
        • Geiger F
        • Lorenz H
        • Xu W
        • et al.
        VEGF producing bone marrow stromal cells (BMSC) enhance vascularization and resorption of a natural coral bone substitute.
        Bone. 2007; 41: 516-522
        • L'heureux N
        • Pâquet S
        • Labbé R
        • Germain L
        • Auger FA
        A completely biological tissue-engineered human blood vessel.
        FASEB J. 1998; 12: 47-56
        • Yang J
        • Zhou W
        • Zheng W
        • et al.
        Effects of myocardial transplantation of marrow mesenchymal stem cells transfected with vascular endothelial growth factor for the improvement of heart function and angiogenesis after myocardial infarction.
        Cardiology. 2007; 107: 17-29
        • Elloumi-Hannachi I
        • Yamato M
        • Okano T
        Cell sheet engineering: a unique nanotechnology for scaffold-free tissue reconstruction with clinical applications in regenerative medicine.
        J Intern Med. 2010; 267: 54-70
        • Gibson I
        • Rosen D
        • Stucker B
        Material jetting. Additive manufacturing technologies: 3D printing, rapid prototyping, and direct digital manufacturing.
        Springer, New York, NY2015: 175-203
        • He Y
        • Wildman RD
        • Tuck CJ
        • Christie SDR
        • Edmondson S
        An investigation of the behavior of solvent based polycaprolactone ink for material jetting.
        Sci Rep. 2016; 6: 20852
        • Nakamura M
        • Kobayashi A
        • Takagi F
        • et al.
        Biocompatible inkjet printing technique for designed seeding of individual living cells.
        Tissue Eng. 2005; 11: 1658-1666
        • Nishiyama Y
        • Henmi C
        • Iwanaga S
        • et al.
        Ink jet three-dimensional digital fabrication for biological tissue manufacturing: analysis of alginate microgel beads produced by ink jet droplets for three dimensional tissue fabrication.
        J Imaging Sci Technol. 2008; 52 (60201-1–6)
        • Xu C
        • Christensen K
        • Zhang Z
        • Huang Y
        • Fu J
        • Markwald RR
        Predictive compensation-enabled horizontal inkjet printing of alginate tubular constructs.
        Manuf Lett. 2013; 1: 28-32
        • Christensen K
        • Xu C
        • Chai W
        • Zhang Z
        • Fu J
        • Huang Y
        Freeform inkjet printing of cellular structures with bifurcations.
        Biotechnol Bioeng. 2015; 112: 1047-1055
        • Guillotin B
        • Souquet A
        • Catros S
        • et al.
        Laser assisted bioprinting of engineered tissue with high cell density and microscale organization.
        Biomaterials. 2010; 31: 7250-7256
        • Yan J
        • Huang Y
        • Chrisey DB
        Laser-assisted printing of alginate long tubes and annular constructs.
        Biofabrication. 2013; 5015002
        • Calignano F
        • Manfredi D
        • Ambrosio EP
        • et al.
        Overview on additive manufacturing technologies.
        Proc IEEE. 2017; 105: 593-612
        • Gibson I
        • Rosen D
        • Stucker B
        Powder bed fusion processes. Additive manufacturing technologies: 3D printing, rapid prototyping, and direct digital manufacturing.
        Springer, New York, NY2015: 107-145
        • Shirazi SFS
        • Gharehkhani S
        • Mehrali M
        • et al.
        A review on powder-based additive manufacturing for tissue engineering: selective laser sintering and inkjet 3D printing.
        Sci Technol Adv Mater. 2015; 16033502
        • Wysocki B
        • Maj P
        • Sitek R
        • Buhagiar J
        • Kurzydłowski KJ
        • Święszkowski W
        Laser and electron beam additive manufacturing methods of fabricating titanium bone implants.
        Appl Sci. 2017; 7: 657
        • Mangano F
        • Chambrone L
        • van Noort R
        • Miller C
        • Hatton P
        • Mangano C
        Direct metal laser sintering titanium dental implants: a review of the current literature.
        Int J Biomater. 2014; 2014: 11
        • Krakhmalev P
        • Yadroitsev I
        • Yadroitsava I
        • De Smidt O
        Functionalization of biomedical Ti6Al4V via in situ alloying by Cu during laser powder bed fusion manufacturing.
        Materials. 2017; 10: 1154
        • Demir AG
        • Monguzzi L
        • Previtali B
        Selective laser melting of pure Zn with high density for biodegradable implant manufacturing.
        Addit Manuf. 2017; 15: 20-28
        • Gibson I
        • Rosen D
        • Stucker B
        Binder jetting. Additive manufacturing technologies: 3D printing, rapid prototyping, and direct digital manufacturing.
        Springer, New York, NY2015: 205-218
        • Hong D
        • Chou D-T
        • Velikokhatnyi OI
        • et al.
        Binder-jetting 3D printing and alloy development of new biodegradable Fe-Mn-Ca/Mg alloys.
        Acta Biomater. 2016; 45: 375-386
        • Khalyfa A
        • Vogt S
        • Weisser J
        • et al.
        Development of a new calcium phosphate powder-binder system for the 3D printing of patient specific implants.
        J Mater Sci: Mater Med. 2007; 18: 909-916
        • Suwanprateeb J
        • Chumnanklang R.
        Three-dimensional printing of porous polyethylene structure using water-based binders.
        J Biomed Mater Res B: Appl Biomater. 2006; 78B: 138-145
        • Mostafaei A
        • Stevens EL
        • Ference JJ
        • Schmidt DE
        • Chmielus M
        Binder jetting of a complex-shaped metal partial denture framework.
        Addit Manuf. 2018; 21: 63-68
        • Gibson I
        • Rosen D
        • Stucker B
        Directed energy deposition processes.
        Additive manufacturing technologies: 3D printing, rapid prototyping, and direct digital manufacturing. Springer, New York, NY2015: 245-268
        • Nakano T
        • Ishimoto T.
        Powder-based additive manufacturing for development of tailor-made implants for orthopedic applications.
        Kona Powder Part J. 2015; 32: 75-84
        • Carroll BE
        • Palmer TA
        • Beese AM
        Anisotropic tensile behavior of Ti–6Al–4V components fabricated with directed energy deposition additive manufacturing.
        Acta Mater. 2015; 87: 309-320
        • Bertol LS
        • Júnior WK
        • FPd Silva
        • Aumund-Kopp C
        Medical design: direct metal laser sintering of Ti–6Al–4V.
        Mater Des. 2010; 31: 3982-3988
        • Al-Imam H
        • Gram M
        • Benetti AR
        • Gotfredsen K
        Accuracy of stereolithography additive casts used in a digital workflow.
        J Prosthet Dent. 2018; 119: 580-585
        • Azari A
        • Nikzad S.
        The evolution of rapid prototyping in dentistry: a review.
        Rapid Prototyping J. 2009; 15: 216-225
        • Melchels FPW
        • Feijen J
        • Grijpma DW
        A review on stereolithography and its applications in biomedical engineering.
        Biomaterials. 2010; 31: 6121-6130
        • Sammartino G
        • Valle AD
        • Marenzi G
        • et al.
        Stereolithography in oral implantology a comparison of surgical guides.
        Implant Dent. 2004; 13: 133-139
        • Bhushan B
        • Caspers M.
        An overview of additive manufacturing (3D printing) for microfabrication.
        Microsyst Technol. 2017; 23: 1117-1124
        • Kim H-C
        • Lee S-H.
        Reduction of post-processing for stereolithography systems by fabrication-direction optimization.
        Comput-Aided Des. 2005; 37: 711-725
        • Meyer W
        • Engelhardt S
        • Novosel E
        • Elling B
        • Wegener M
        • Krüger H
        Soft polymers for building up small and smallest blood supplying systems by stereolithography.
        J Funct Biomater. 2012; 3: 257-268
        • Huber B
        • Engelhardt S
        • Meyer W
        • et al.
        Blood-vessel mimicking structures by stereolithographic fabrication of small porous tubes using cytocompatible polyacrylate elastomers, biofunctionalization and endothelialization.
        J Funct Biomater. 2016; 7: 11
        • Gibson I
        • Rosen D
        • Stucker B
        Sheet lamination processes. Additive manufacturing technologies: 3D printing, rapid prototyping, and direct digital manufacturing.
        Springer, New York, NY2015: 219-244
        • Chua CK
        • Wong CH
        • Yeong WY
        Chapter Two – Roadmap on Additive Manufacturing Standards.
        in: Chua CK Wong CH Yeong WY Standards, Quality Control, and Measurement Sciences in 3D Printing and Additive Manufacturing. Academic Press, 2017: 31-55
        • Kelly BE
        • Bhattacharya I
        • Heidari H
        • Shusteff M
        • Spadaccini CM
        • Taylor HK
        Volumetric additive manufacturing via tomographic reconstruction.
        Science. 2019; 363: 1075-1079
        • Kolesky DB
        • Truby RL
        • Gladman AS
        • Busbee TA
        • Homan KA
        • Lewis JA
        3D bioprinting of vascularized, heterogeneous cell-laden tissue constructs.
        Adv Mater. 2014; 26: 3124-3130
        • Kolesky DB
        • Homan KA
        • Skylar-Scott MA
        • Lewis JA
        Three-dimensional bioprinting of thick vascularized tissues.
        Proc Natl Acad Sci. 2016; 113: 3179-3184
        • Jafarkhani M
        • Salehi Z
        • Aidun A
        • Shokrgozar MA
        Bioprinting in vascularization strategies.
        Iran Biomed J. 2019; 23: 9-20
      6. Kambic HE, Kantrowitz A, Sung P, eds. Vascular graft update: safety and performance 1986; Philadelphia, Penn: ASTM.

      7. FUSION Vascular Graft: MAQUET Holding B.V. & Co. KG; 2018. Available from: www.maquet.com. Accessed November 12, 2018.

      8. Uni-Graft® K DV: B. Braun Melsungen AG 2018, Available from:www.bbraun.com. Accessed November 12, 2018.

      9. GORE-TEX® Vascular Grafts: W. L. Gore & Associates; 2018, Available from: www.goremedical.com. Accessed November 12, 2018.

        • Jensen LP
        • Lepäntalo M
        • Fossdal JE
        • et al.
        Dacron or PTFE for above-knee femoropopliteal bypass. A multicenter randomised study.
        Eur J Vasc Endovasc Surg. 2007; 34: 44-49
      10. Artegraft® Collagen Vascular Graft Bovine Carotid Artery Graft (BCA): Artegraft, Inc; 2018. Available from:www.artegraft.com. Accessed November 13, 2018.

      11. AlboGraft® Polyester Vascular Graft: LeMaitre Vascular, Inc.; 2018. Available from: www.lemaitre.com. Accessed November 12, 2018.

        • Abdollahi S
        • Davis A
        • Miller JH
        • Feinberg AW
        Expert-guided optimization for 3D printing of soft and liquid materials.
        Plos One. 2018; 13
        • Hinton TJ
        • Hudson A
        • Pusch K
        • Lee A
        • Feinberg AW
        3D printing PDMS elastomer in a hydrophilic support bath via freeform reversible embedding.
        Acs Biomater Sci Eng. 2016; 2: 1781-1786
        • Kotz F
        • Arnold K
        • Bauer W
        • et al.
        Three-dimensional printing of transparent fused silica glass.
        Nature. 2017; 544: 337
        • Gantenbein S
        • Masania K
        • Woigk W
        • Sesseg JPW
        • Tervoort TA
        • Studart AR
        Three-dimensional printing of hierarchical liquid-crystal-polymer structures.
        Nature. 2018; 561: 226-230
        • Kim Y
        • Yuk H
        • Zhao R
        • Chester SA
        • Zhao X
        Printing ferromagnetic domains for untethered fast-transforming soft materials.
        Nature. 2018; 558: 274-279
      12. Conduits for Vascular Reconstruction in the Pediatric Patient WebMD LLC; 2017. Available from: emedicine.medscape.com/article/1018266-overview. Accessed November 14, 2018.

        • Ravi S
        • Chaikof EL.
        Biomaterials for vascular tissue engineering.
        Regener Med. 2010; 5: 107-120
        • Schmidt CE
        • Baier JM
        Acellular vascular tissues: natural biomaterials for tissue repair and tissue engineering.
        Biomaterials. 2000; 21: 2215-2231
        • Shojaee M
        • Bashur CA.
        Compositions including synthetic and natural blends for integration and structural integrity: engineered for different vascular graft applications.
        Adv Healthcare Mater. 2017; 61700001
        • Melchiorri AJ
        • Hibino N
        • Best CA
        • et al.
        3D-Printed Biodegradable Polymeric Vascular Grafts.
        Adv Healthcare Mater. 2016; 5: 319-325
        • Fukunishi T
        • Best CA
        • Sugiura T
        • et al.
        Preclinical study of patient-specific cell-free nanofiber tissue-engineered vascular grafts using 3-dimensional printing in a sheep model.
        J Thorac Cardiovasc Surg. 2017; 153: 924-932
        • Laura E
        • Peter YY.
        Additive manufacturing of vascular grafts and vascularized tissue constructs.
        Tissue Eng B: Rev. 2017; 23: 436-450
      13. Guidance document for vascular prostheses 510(k) submissions – guidance for industry and FDA staff: center for devices and radiological health (CDRH); 2000 [1/27/2019]. Available from: www.fda.gov/MedicalDevices/ucm073681.htm.

        • Refson JS
        • Schachter M
        • Patel MK
        • et al.
        Vein graft stenosis and the heparin responsiveness of human vascular smooth muscle cells.
        Circulation. 1998; 97: 2506-2510
        • Sindermann JR
        • March KL.
        Heparin responsiveness in vitro as a prognostic tool for vascular graft stenosis.
        Circulation. 1998; 97: 2486-2490
        • Gilotti AC
        • Nimlamool W
        • Pugh R
        • et al.
        Heparin responses in vascular smooth muscle cells involve cGMP-dependent protein kinase (PKG).
        J Cell Physiol. 2014; 229: 2142-2152
        • Allaire E
        • Mandet C
        • Bruneval P
        • Bensenane S
        • Becquemin JP
        • Michel JB
        Cell and extracellular matrix rejection in arterial concordant and discordant xenografts in the rat.
        Transplantation. 1996; 62: 794-803
        • Hoopes CW
        • Platt JF.
        Molecular strategies for clinical xenotransplantation in cardiothoracic surgery.
        Semin Thorac Cardiovasc Surg. 1996; 8: 156-174
        • Chlupác J
        • Filová E
        • Bacáková L
        Blood vessel replacement: 50 years of development and tissue engineering paradigms in vascular surgery.
        Physiol Res. 2009; 58: S119-S139
        • Sekine H
        • Shimizu T
        • Yang J
        • Kobayashi E
        • Okano T
        Pulsatile myocardial tubes fabricated with cell sheet engineering.
        Circulation. 2006; 114: I87-I93
        • van Duinen V
        • van den Heuvel A
        • Trietsch SJ
        • et al.
        96 perfusable blood vessels to study vascular permeability in vitro.
        Sci Rep. 2017; 7: 18071
        • Radu M
        • Chernoff J.
        An in vivo assay to test blood vessel permeability.
        J Vis Exp: JoVE. 2013; (e50062-e)
        • Chakfe N
        • Riepe G
        • Dieval F
        • et al.
        Longitudinal ruptures of polyester knitted vascular prostheses.
        J Vasc Surg. 2001; 33: 1015-1021
        • Tanaka H
        • Okada K
        • Yamashita T
        • Kawanishi Y
        • Matsumori M
        • Okita Y
        Disruption of the vascular prosthesis caused by aortic calcification after replacement of the thoracoabdominal aortic aneurysm.
        Ann Thorac Surg. 2006; 82: 1097-1099
        • Quiñones-Baldrich WJ
        • Moore WS
        • Ziomek S
        • Chvapil M
        Development of a “leak-proof,” knitted Dacron vascular prosthesis.
        J Vasc Surg. 1986; 3: 895-903
        • Drury JK
        • Ashton TR
        • Cunningham JD
        • Maini R
        • Pollock JG
        Experimental and clinical experience with a gelatin impregnated dacron prosthesis.
        Ann Vasc Surg. 1987; 1: 542-547
        • Prager M
        • Polterauer P
        • Böhmig H-J
        • et al.
        Collagen versus gelatin-coated Dacron versus stretch polytetrafluoroethylene in abdominal aortic bifurcation graft surgery: results of a seven-year prospective, randomized multicenter trial.
        Surgery. 2001; 130: 408-414
        • Vohra R
        • Drury JK
        • Shapiro D
        • Shenkin A
        • Pollock JG
        Sealed versus unsealed knitted dacron prostheses: a comparison of the acute phase protein response.
        Ann Vasc Surg. 1987; 1: 548-551
        • Singh C
        • Wong CS
        • Wang X
        Medical textiles as vascular implants and their success to mimic natural arteries.
        J Funct Biomater. 2015; 6: 500-525
        • Kidane AG
        • Burriesci G
        • Edirisinghe M
        • Ghanbari H
        • Bonhoeffer P
        • Seifalian AM
        A novel nanocomposite polymer for development of synthetic heart valve leaflets.
        Acta Biomater. 2009; 5: 2409-2417
        • Kim B-S
        • Mooney DJ.
        Development of biocompatible synthetic extracellular matrices for tissue engineering.
        Trends Biotechnol. 1998; 16: 224-230
        • Lee SJ
        • Yoo JJ
        • Lim GJ
        • Atala A
        • Stitzel J
        In vitro evaluation of electrospun nanofiber scaffolds for vascular graft application.
        J Biomed Mater Res A. 2007; 83A: 999-1008
        • Shum-Tim D
        • Stock U
        • Hrkach J
        • et al.
        Tissue engineering of autologous aorta using a new biodegradable polymer.
        Ann Thorac Surg. 1999; 68: 2298-2304
        • Hernandez-Richter T
        • Schardey HM
        • Löhlein F
        • et al.
        The prevention and treatment of vascular graft infection with a triclosan (Irgasan)-bonded Dacron graft: an experimental study in the pig.
        EurJ Vasc Endovasc Surg. 2000; 20: 413-418
        • Enayati M
        • Eilenberg M
        • Grasl C
        • et al.
        Biocompatibility assessment of a new biodegradable vascular graft via in vitro co-culture approaches and in vivo model.
        Ann Biomed Eng. 2016; 44: 3319-3334
        • Halloran PF.
        Immunosuppressive drugs for kidney transplantation.
        N Engl J Med. 2004; 351: 2715-2729
        • Epperson DE
        • Pober JS.
        Antigen-presenting function of human endothelial cells. Direct activation of resting CD8 T cells.
        J Immunol. 1994; 153: 5402-5412
        • Wagner E
        • Roy R
        • Marois Y
        • Douville Y
        • Guidoin R
        Fresh venous allografts in peripheral arterial reconstruction in dogs. Effects of histocompatibility and of short-term immunosuppression with cyclosporine A and mycophenolate mofetil.
        J Thorac Cardiovasc Surg. 1995; 110: 1732-1744
        • Nowicki KW
        • Hosaka K
        • He Y
        • McFetridge PS
        • Scott EW
        • Hoh BL
        Novel high-throughput in vitro model for identifying hemodynamic-induced inflammatory mediators of cerebral aneurysm formation.
        Hypertension. 2014; 64: 1306-1313
        • Kaneko N
        • Mashiko T
        • Namba K
        • Tateshima S
        • Watanabe E
        • Kawai K
        A patient-specific intracranial aneurysm model with endothelial lining: a novel in vitro approach to bridge the gap between biology and flow dynamics.
        J Neurointerv Surg. 2018; 10: 306
        • Klink A
        • Heynens J
        • Herranz B
        In vivo characterization of a new abdominal aortic aneurysm mouse model with conventional and molecular magnetic resonance imaging.
        J Am Coll Cardiol. 2011; 58: 2522-2530
        • Tsui JC.
        Experimental models of abdominal aortic aneurysms.
        Open Cardiovasc Med J. 2010; 4: 221-230
        • May J
        • Stephen M.
        Multiple aneurysms in Dacron velour graft.
        Arch Surg. 1978; 113: 320-321
        • Hallin RW.
        Complications with the mandril-grown (Sparks) Dacron arterial graft.
        Am Surg. 1975; 41: 550-554
        • Carrabba M
        • Madeddu P.
        Current strategies for the manufacture of small size tissue engineering vascular grafts.
        Front Bioeng Biotechnol. 2018; 6: 41
        • Kumar VA
        • Caves JM
        • Haller CA
        • et al.
        Acellular vascular grafts generated from collagen and elastin analogs.
        Acta Biomater. 2013; 9: 8067-8074
        • Li X
        • Xu J
        • Nicolescu CT
        • Marinelli JT
        • Tien J
        Generation, endothelialization, and microsurgical suture anastomosis of strong 1-mm-diameter collagen tubes.
        Tissue Eng A. 2017; 23: 335-344
        • Bouzeghrane F
        • Naggara O
        • Kallmes DF
        • Berenstein A
        • Raymond J
        In vivo experimental intracranial aneurysm models: a systematic review.
        Am J Neuroradiol. 2010; 31: 418-423
        • Suntornnond R
        • Tan EYS
        • An J
        • Chua CK
        A highly printable and biocompatible hydrogel composite for direct printing of soft and perfusable vasculature-like structures.
        Sci Rep. 2017; 7: 16902
        • Jia W
        • Gungor-Ozkerim PS
        • Zhang YS
        • et al.
        Direct 3D bioprinting of perfusable vascular constructs using a blend bioink.
        Biomaterials. 2016; 106: 58-68
        • Cui H
        • Nowicki M
        • Fisher JP
        • Zhang LG
        3D Bioprinting for organ regeneration.
        Adv Healthcare Mater. 2017; 6https://doi.org/10.1002/adhm.201601118
        • Kabirian F
        • Ditkowski B
        • Zamanian A
        • Hoylaerts MF
        • Mozafari M
        • Heying R
        Controlled NO-release from 3D-printed small-diameter vascular grafts prevents platelet activation and bacterial infectivity.
        ACS Biomater Sci Eng. 2019; 5: 2284-2296
        • Chen T.
        In situ detection of mycoplasma contamination in cell cultures by fluorescent Hoechst 33258 stain.
        Exp Cell Res. 1977; 104: 255-262
      14. U.S. Food and Drug Administration Silver Spring: U.S. Department of Health and Human Services; 2019. Available from: www.fda.gov. Accessed January 14, 2019.

      15. ANSI/AAMI/ ISO 25539-1: 2003/(R)2014 Cardiovascular implants — Endovascular devices — Part 1: Endovascular prostheses Arlington, VA: Association for the Advancement of Medical Instrumentation (AAMI); 2003. Available from:my.aami.org/aamiresources/previewfiles/2553901_1404_preview.pdf. Accessed January 14, 2019.

      16. Technical Considerations for Additive Manufactured Medical Devices: Guidance for industry and food and drug administration staff Center for Devices and Radiological Health (CDRH); 2017. Available from: www.fda.gov/downloads/MedicalDevices/DeviceRegulationandGuidance/GuidanceDocuments/UCM499809.pdf.

      17. Di Prima M CJ, Anderson J, Kiarashi N. FDA Webinar- Technical Considerations for Additive Manufactured Medical Devices 2018. Available from: www.fda.gov/downloads/Training/CDRHLearn/UCM592927.pdf. Accessed January 14, 2019.

        • Di Prima M
        • Coburn J
        • Hwang D
        • Kelly J
        • Khairuzzaman A
        • Ricles L
        Additively manufactured medical products – the FDA perspective.
        3D Print Med. 2016; 2: 1
      18. National Institute of Standards and Technology (NIST), Gaithersburg, Maryland2016 (Available from: Accessed January 14, 2019)
        • Christensen A
        • Rybicki FJ.
        Maintaining safety and efficacy for 3D printing in medicine.
        3D Print Med. 2017; 3: 1
      19. OpenStax. Anatomy & Physiology: OpenStax CNX; Available from:http://cnx.org/contents/[email protected]. Accessed February 26, 2016.

      20. Overview over 3D printing technologies Zürich, Switzerland 2018. Available from: www.additively.com. Accessed April 9, 2019.

      21. Sciaky Inc., IL2019 (Available from: Accessed April 9, 2019)
      22. Laminated object manufacturing, LOM Stockholm, Sweden: Manufacturing Guide Sweden AB; Available from: www.manufacturingguide.com/en/laminated-object-manufacturing-lom. Accessed April 9, 2019.