Three-dimensional bioprinting of aneurysm-bearing tissue structure for endovascular deployment of embolization coils
Abstract
Various types of embolization devices have been developed for the treatment of cerebral aneurysms. However, it is challenging to properly evaluate device performance and train medical personnel for device deployment without the aid of functionally relevant models. Current in vitro aneurysm models suffer from a lack of key functional and morphological features of brain vasculature that limit their applicability for these purposes. These features include the physiologically relevant mechanical properties and the dynamic cellular environment of blood vessels subjected to constant fluid flow. Herein, we developed three-dimensionally (3D) printed aneurysm-bearing vascularized tissue structures using gelatin-fibrin hydrogel of which the inner vessel walls were seeded with human cerebral microvascular endothelial cells (hCMECs). The hCMECs readily exhibited cellular attachment, spreading, and confluency all around the vessel walls, including the aneurysm walls. Additionally, the in vitro platform was directly amenable to flow measurements via particle image velocimetry, enabling the direct assessment of the vascular flow dynamics for comparison to a 3D computational fluid dynamics model. Detachable coils were delivered into the printed aneurysm sac through the vessel using a microcatheter and static blood plasma clotting was monitored inside the aneurysm sac and around the coils. This biomimetic in vitro aneurysm model is amore »
- Publication Date:
- Research Org.:
- Lawrence Livermore National Laboratory (LLNL), Livermore, CA (United States)
- Sponsoring Org.:
- USDOE National Nuclear Security Administration (NNSA)
- OSTI Identifier:
- 1678777
- Alternate Identifier(s):
- OSTI ID: 1678780; OSTI ID: 1698292
- Report Number(s):
- LLNL-JRNL-807798
Journal ID: ISSN 1758-5090
- Grant/Contract Number:
- LDRD-20-ERD-013; AC52-07NA27344
- Resource Type:
- Published Article
- Journal Name:
- Biofabrication (Online)
- Additional Journal Information:
- Journal Name: Biofabrication (Online) Journal Volume: 13 Journal Issue: 1; Journal ID: ISSN 1758-5090
- Country of Publication:
- Country unknown/Code not available
- Language:
- English
- Subject:
- 42 ENGINEERING
Citation Formats
Jang, Lindy K., Alvarado, Javier A., Pepona, Marianna, Wasson, Elisa M., Nash, Landon D., Ortega, Jason M., Randles, Amanda, Maitland, Duncan J., Moya, Monica L., and Hynes, William F. Three-dimensional bioprinting of aneurysm-bearing tissue structure for endovascular deployment of embolization coils. Country unknown/Code not available: N. p., 2020.
Web. doi:10.1088/1758-5090/abbb9b.
Jang, Lindy K., Alvarado, Javier A., Pepona, Marianna, Wasson, Elisa M., Nash, Landon D., Ortega, Jason M., Randles, Amanda, Maitland, Duncan J., Moya, Monica L., & Hynes, William F. Three-dimensional bioprinting of aneurysm-bearing tissue structure for endovascular deployment of embolization coils. Country unknown/Code not available. https://doi.org/10.1088/1758-5090/abbb9b
Jang, Lindy K., Alvarado, Javier A., Pepona, Marianna, Wasson, Elisa M., Nash, Landon D., Ortega, Jason M., Randles, Amanda, Maitland, Duncan J., Moya, Monica L., and Hynes, William F. Tue .
"Three-dimensional bioprinting of aneurysm-bearing tissue structure for endovascular deployment of embolization coils". Country unknown/Code not available. https://doi.org/10.1088/1758-5090/abbb9b.
@article{osti_1678777,
title = {Three-dimensional bioprinting of aneurysm-bearing tissue structure for endovascular deployment of embolization coils},
author = {Jang, Lindy K. and Alvarado, Javier A. and Pepona, Marianna and Wasson, Elisa M. and Nash, Landon D. and Ortega, Jason M. and Randles, Amanda and Maitland, Duncan J. and Moya, Monica L. and Hynes, William F.},
abstractNote = {Various types of embolization devices have been developed for the treatment of cerebral aneurysms. However, it is challenging to properly evaluate device performance and train medical personnel for device deployment without the aid of functionally relevant models. Current in vitro aneurysm models suffer from a lack of key functional and morphological features of brain vasculature that limit their applicability for these purposes. These features include the physiologically relevant mechanical properties and the dynamic cellular environment of blood vessels subjected to constant fluid flow. Herein, we developed three-dimensionally (3D) printed aneurysm-bearing vascularized tissue structures using gelatin-fibrin hydrogel of which the inner vessel walls were seeded with human cerebral microvascular endothelial cells (hCMECs). The hCMECs readily exhibited cellular attachment, spreading, and confluency all around the vessel walls, including the aneurysm walls. Additionally, the in vitro platform was directly amenable to flow measurements via particle image velocimetry, enabling the direct assessment of the vascular flow dynamics for comparison to a 3D computational fluid dynamics model. Detachable coils were delivered into the printed aneurysm sac through the vessel using a microcatheter and static blood plasma clotting was monitored inside the aneurysm sac and around the coils. This biomimetic in vitro aneurysm model is a promising method for examining the biocompatibility and hemostatic efficiency of embolization devices and for providing hemodynamic information which would aid in predicting aneurysm rupture or healing response after treatment.},
doi = {10.1088/1758-5090/abbb9b},
journal = {Biofabrication (Online)},
number = 1,
volume = 13,
place = {Country unknown/Code not available},
year = {Tue Oct 20 00:00:00 EDT 2020},
month = {Tue Oct 20 00:00:00 EDT 2020}
}
Free Publicly Available Full Text
Publisher's Version of Record
https://doi.org/10.1088/1758-5090/abbb9b
https://doi.org/10.1088/1758-5090/abbb9b
Other availability
Search WorldCat to find libraries that may hold this journal
Save to My Library
You must Sign In or Create an Account in order to save documents to your library.
Works referenced in this record:
In vivo comparison of shape memory polymer foam‐coated and bare metal coils for aneurysm occlusion in the rabbit elastase model
journal, February 2019
- Herting, Scott M.; Ding, Yonghong; Boyle, Anthony J.
- Journal of Biomedical Materials Research Part B: Applied Biomaterials, Vol. 107, Issue 8
In vitro and in vivo evaluation of a shape memory polymer foam-over-wire embolization device delivered in saccular aneurysm models: SHAPE MEMORY POLYMER FOAM-OVER-WIRE EMBOLIZATION DEVICE
journal, July 2015
- Boyle, Anthony J.; Landsman, Todd L.; Wierzbicki, Mark A.
- Journal of Biomedical Materials Research Part B: Applied Biomaterials, Vol. 104, Issue 7
PIV-Measured Versus CFD-Predicted Flow Dynamics in Anatomically Realistic Cerebral Aneurysm Models
journal, April 2008
- Ford, Matthew D.; Nikolov, Hristo N.; Milner, Jaques S.
- Journal of Biomechanical Engineering, Vol. 130, Issue 2
Bioactive versus Bare Platinum Coils in the Treatment of Intracranial Aneurysms: The MAPS (Matrix and Platinum Science) Trial
journal, January 2014
- McDougall, C. G.; Johnston, S. C.; Gholkar, A.
- American Journal of Neuroradiology, Vol. 35, Issue 5
Three-Dimensional Pulsatile Flow Simulation before and after Endovascular Coil Embolization of a Terminal Cerebral Aneurysm
journal, December 2001
- Groden, Christoph; Laudan, Jochen; Gatchell, Scott
- Journal of Cerebral Blood Flow & Metabolism, Vol. 21, Issue 12
A computational thrombus formation model: application to an idealized two-dimensional aneurysm treated with bare metal coils
journal, August 2018
- Horn, John D.; Maitland, Duncan J.; Hartman, Jonathan
- Biomechanics and Modeling in Mechanobiology, Vol. 17, Issue 6
Artificial Cerebral Aneurysm Model for Medical Testing, Training, and Research.
journal, January 2003
- Sugiu, Kenji; Martin, Jean-Baptiste; Jean, Beatrix
- Neurologia medico-chirurgica, Vol. 43, Issue 2
Treatment of Experimental Aneurysms Using Collagen-coated Microcoils Experimental Study: 133
journal, January 1995
- Dawson, Robert C.; Krisht, Ali F.; Barrow, Daniel L.
- Neurosurgery, Vol. 36, Issue 1
Second-Generation Hydrogel Coils for the Endovascular Treatment of Intracranial Aneurysms: A Randomized Controlled Trial
journal, March 2018
- Taschner, Christian A.; Chapot, René; Costalat, Vincent
- Stroke, Vol. 49, Issue 3
Examining metastatic behavior within 3D bioprinted vasculature for the validation of a 3D computational flow model
journal, August 2020
- Hynes, W. F.; Pepona, M.; Robertson, C.
- Science Advances, Vol. 6, Issue 35
Activation of Rac1 by shear stress in endothelial cells mediates both cytoskeletal reorganization and effects on gene expression
journal, December 2002
- Tzima, E.
- The EMBO Journal, Vol. 21, Issue 24
Endovascular Creation of an in Vivo Bifurcation Aneurysm Model in Rabbits
journal, October 1999
- Cloft, Harry J.; Altes, Talisa A.; Marx, William F.
- Radiology, Vol. 213, Issue 1
Assessment of Normal Flow Velocity in Basal Cerebral Veins: A Transcranial Doppler Ultrasound Study
journal, July 1996
- Valdueza, José Manuel; Schmierer, Klaus; Mehraein, Susan
- Stroke, Vol. 27, Issue 7
Subarachnoid haemorrhage
journal, January 2007
- van Gijn, Jan; Kerr, Richard S.; Rinkel, Gabriel JE
- The Lancet, Vol. 369, Issue 9558
Experimental and numerical study of the effect of pulsatile flow on wall displacement oscillation in a flexible lateral aneurysm model
journal, September 2019
- Mu, L. Z.; Li, X. Y.; Chi, Q. Z.
- Acta Mechanica Sinica, Vol. 35, Issue 5
A comparison of the elasticity of live, dead, and fixed brain tissue
journal, July 1970
- Metz, Howard; McElhaney, James; Ommaya, Ayub K.
- Journal of Biomechanics, Vol. 3, Issue 4
Suitability of lattice Boltzmann inlet and outlet boundary conditions for simulating flow in image‐derived vasculature
journal, April 2019
- Feiger, Bradley; Vardhan, Madhurima; Gounley, John
- International Journal for Numerical Methods in Biomedical Engineering
Topic review: surface modifications enhancing biological activity of guglielmi detachable coils in treating intracranial aneurysms
journal, July 2000
- Abrahams, John M.; Diamond, Scott L.; Hurst, Robert W.
- Surgical Neurology, Vol. 54, Issue 1
Impact of aneurysmal geometry on intraaneurysmal flow: a computerized flow simulation study
journal, January 2008
- Szikora, Istvan; Paal, Gyorgy; Ugron, Adam
- Neuroradiology, Vol. 50, Issue 5
Endovascular coiling versus neurosurgical clipping for patients with aneurysmal subarachnoid haemorrhage
journal, October 2005
- van der Schaaf, Irene; Algra, Ale; Wermer, Marieke
- Cochrane Database of Systematic Reviews
A Model for Collision Processes in Gases. I. Small Amplitude Processes in Charged and Neutral One-Component Systems
journal, May 1954
- Bhatnagar, P. L.; Gross, E. P.; Krook, M.
- Physical Review, Vol. 94, Issue 3
Expression and transcriptional regulation of ABC transporters and cytochromes P450 in hCMEC/D3 human cerebral microvascular endothelial cells
journal, March 2009
- Dauchy, Sandrine; Miller, Florence; Couraud, Pierre-Olivier
- Biochemical Pharmacology, Vol. 77, Issue 5
Anin vitro anatomic model of the human cerebral arteries with saccular arterial aneurysms
journal, March 1997
- Gailloud, P.; Pray, J. R.; Muster, M.
- Surgical and Radiologic Anatomy, Vol. 19, Issue 2
Significance of Volume Embolization Ratio as a Predictor of Recanalization on Endovascular Treatment of Cerebral Aneurysms with Guglielmi Detachable Coils
journal, November 2000
- Uchiyama, N.; Kida, S.; Nomura, M.
- Interventional Neuroradiology, Vol. 6, Issue 1_suppl
Tissue-engineered aneurysm models for in vitro assessment of neurovascular devices
journal, March 2019
- Shen, Tiffany W.; Puccini, Brandon; Temnyk, Kristen
- Neuroradiology, Vol. 61, Issue 6
Influence of Hemodynamic Factors on Rupture of Intracranial Aneurysms: Patient-Specific 3D Mirror Aneurysms Model Computational Fluid Dynamics Simulation
journal, July 2011
- Lu, G.; Huang, L.; Zhang, X. L.
- American Journal of Neuroradiology, Vol. 32, Issue 7
Ruptured Cerebral Aneurysms
journal, January 2005
- Ellegala, Dilantha B.; Day, Arthur L.
- New England Journal of Medicine, Vol. 352, Issue 2
The effects of stenting and endothelial denudation on aneurysm and branch occlusion in experimental aneurysm models
journal, June 2007
- Darsaut, Tim; Bouzeghrane, Fatiha; Salazkin, Igor
- Journal of Vascular Surgery, Vol. 45, Issue 6
Transforming Growth Factor β-coated Platinum Coils for Endovascular Treatment of Aneurysms: An Animal Study
journal, September 2001
- de Gast, Anjob N.; Altes, Tally A.; Marx, William F.
- Neurosurgery, Vol. 49, Issue 3
Computational study of clot formation in aneurysms treated with shape memory polymer foam
journal, January 2020
- Horn, John D.; Maitland, Duncan J.; Hartman, Jonathan
- Medical Engineering & Physics, Vol. 75
Role of the Endothelial Lining in Persistence of Residual Lesions and Growth of Recurrences After Endovascular Treatment of Experimental Aneurysms
journal, March 2002
- Raymond, Jean; Sauvageau, Eric; Salazkin, Igor
- Stroke, Vol. 33, Issue 3
Surgical management of unruptured intracranial aneurysms
journal, March 1994
- Solomon, Robert A.; Fink, Matthew E.; Pile-Spellman, John
- Journal of Neurosurgery, Vol. 80, Issue 3
In Vivo Experimental Intracranial Aneurysm Models: A Systematic Review
journal, October 2009
- Bouzeghrane, F.; Naggara, O.; Kallmes, D. F.
- American Journal of Neuroradiology, Vol. 31, Issue 3
In Vitro Assessment of Flow Variability in an Intracranial Aneurysm Model Using 4D Flow MRI and Tomographic PIV
journal, June 2020
- Medero, Rafael; Ruedinger, Katrina; Rutkowski, David
- Annals of Biomedical Engineering, Vol. 48, Issue 10
Autologous adipose-derived mesenchymal stem cells improve healing of coiled experimental saccular aneurysms: an angiographic and histopathological study
journal, January 2017
- Rouchaud, Aymeric; Brinjikji, Waleed; Dai, Daying
- Journal of NeuroInterventional Surgery, Vol. 10, Issue 1
Mechanical Heterogeneity of the Rat Hippocampus Measured by Atomic Force Microscope Indentation
journal, May 2007
- Elkin, Benjamin S.; Azeloglu, Evren U.; Costa, Kevin D.
- Journal of Neurotrauma, Vol. 24, Issue 5
Analytic solutions of simple flows and analysis of nonslip boundary conditions for the lattice Boltzmann BGK model
journal, April 1997
- He, Xiaoyi; Zou, Qisu; Luo, Li-Shi
- Journal of Statistical Physics, Vol. 87, Issue 1-2
Evaluation of the Basilar Artery Flow Velocity by Transcranial Doppler Ultrasonography
journal, January 1992
- Cantu, Carlos; Yasaka, Masahiro; Tsuchiya, Takashi
- Cerebrovascular Diseases, Vol. 2, Issue 6
Quantitative Characterization of the Hemodynamic Environment in Ruptured and Unruptured Brain Aneurysms
journal, December 2010
- Cebral, J. R.; Mut, F.; Weir, J.
- American Journal of Neuroradiology, Vol. 32, Issue 1
A 3D neurovascular microfluidic model consisting of neurons, astrocytes and cerebral endothelial cells as a blood–brain barrier
journal, January 2017
- Adriani, Giulia; Ma, Dongliang; Pavesi, Andrea
- Lab on a Chip, Vol. 17, Issue 3
Association between hemodynamic conditions and occlusion times after flow diversion in cerebral aneurysms
journal, April 2014
- Mut, Fernando; Raschi, Marcelo; Scrivano, Esteban
- Journal of NeuroInterventional Surgery, Vol. 7, Issue 4
Numerical blood flow analysis: Arterial bifurcation with a saccular aneurysm
journal, January 1988
- Perktold, K.; Kenner, T.; Hilbert, D.
- Basic Research in Cardiology, Vol. 83, Issue 1
Poly-vinyl alcohol hydrogel vascular models for in vitro aneurysm simulations: the key to low friction surfaces
journal, August 2004
- Ohta, Makoto; Handa, Akira; Iwata, Hiroo
- Technology and Health Care, Vol. 12, Issue 3
A comparison of the measured and predicted flowfield in a patient-specific model of an abdominal aortic aneurysm
journal, May 2008
- O'Rourke, M. J.; McCullough, J. P.
- Proceedings of the Institution of Mechanical Engineers, Part H: Journal of Engineering in Medicine, Vol. 222, Issue 5
A DSA-Based Method Using Contrast-Motion Estimation for the Assessment of the Intra-Aneurysmal Flow Changes Induced by Flow-Diverter Stents
journal, November 2012
- Pereira, V. M.; Bonnefous, O.; Ouared, R.
- American Journal of Neuroradiology, Vol. 34, Issue 4
In vitro study of haemodynamics in a giant saccular aneurysm model: influence of flow dynamics in the parent vessel and effects of coil embolisation
journal, October 1994
- Gobin, Y. P.; Counord, J. L.; Flaud, P.
- Neuroradiology, Vol. 36, Issue 7
Lattice BGK Models for Navier-Stokes Equation
journal, February 1992
- Qian, Y. H.; D'Humières, D.; Lallemand, P.
- Europhysics Letters (EPL), Vol. 17, Issue 6
Arterial Wall Shear Stress: Observations from the Bench to the Bedside
journal, January 2003
- Paszkowiak, Jacek J.; Dardik, Alan
- Vascular and Endovascular Surgery, Vol. 37, Issue 1
Multi-time-lag PIV analysis of steady and pulsatile flows in a sidewall aneurysm
journal, May 2014
- Bouillot, P.; Brina, O.; Ouared, R.
- Experiments in Fluids, Vol. 55, Issue 6
In vivo cerebral aneurysm models
journal, July 2019
- Thompson, John W.; Elwardany, Omar; McCarthy, David J.
- Neurosurgical Focus, Vol. 47, Issue 1
Flexible tubular replicas of abdominal aortic aneurysms
journal, March 2002
- Berry, E.; Marsden, A.; Dalgarno, K. W.
- Proceedings of the Institution of Mechanical Engineers, Part H: Journal of Engineering in Medicine, Vol. 216, Issue 3
Physiological remodeling of bifurcation aneurysms: preclinical results of the eCLIPs device
journal, February 2018
- Marotta, Thomas R.; Riina, Howard A.; McDougall, Ian
- Journal of Neurosurgery, Vol. 128, Issue 2
Three-dimensional bioprinting of thick vascularized tissues
journal, March 2016
- Kolesky, David B.; Homan, Kimberly A.; Skylar-Scott, Mark A.
- Proceedings of the National Academy of Sciences, Vol. 113, Issue 12
Relation between Aneurysm Volume, Packing, and Compaction in 145 Cerebral Aneurysms Treated with Coils
journal, June 2004
- Sluzewski, Menno; van Rooij, Willem Jan; Slob, Marian J.
- Radiology, Vol. 231, Issue 3
Subarachnoid haemorrhage: diagnosis, causes and management
journal, February 2001
- van Gijn, J.; Rinkel, G. J. E.
- Brain, Vol. 124, Issue 2
Pulsatile non-Newtonian blood flow simulation through a bifurcation with an aneurysm
journal, December 1989
- Perktold, K.; Peter, R.; Resch, M.
- Biorheology, Vol. 26, Issue 6
Performance Analysis of the Lattice Boltzmann Model Beyond Navier-Stokes
conference, May 2013
- Randles, Amanda Peters; Kale, Vivek; Hammond, Jeff
- 2013 IEEE International Symposium on Parallel & Distributed Processing (IPDPS), 2013 IEEE 27th International Symposium on Parallel and Distributed Processing
Human Blood-Brain Barrier Disruption by Retroviral-Infected Lymphocytes: Role of Myosin Light Chain Kinase in Endothelial Tight-Junction Disorganization
journal, August 2007
- Afonso, Philippe Vicente; Ozden, Simona; Prevost, Marie-Christine
- The Journal of Immunology, Vol. 179, Issue 4