A 3D bioprinting system to produce human-scale tissue constructs with structural integrity
Abstract
A challenge for tissue engineering is producing three-dimensional (3D), vascularized cellular constructs of clinically relevant size, shape and structural integrity. We present an integrated tissue-organ printer (ITOP) that can fabricate stable, human-scale tissue constructs of any shape. Mechanical stability is achieved by printing cell-laden hydrogels together with biodegradable polymers in integrated patterns and anchored on sacrificial hydrogels. The correct shape of the tissue construct is achieved by representing clinical imaging data as a computer model of the anatomical defect and translating the model into a program that controls the motions of the printer nozzles, which dispense cells to discrete locations. The incorporation of microchannels into the tissue constructs facilitates diffusion of nutrients to printed cells, thereby overcoming the diffusion limit of 100-200 μm for cell survival in engineered tissues. We demonstrate capabilities of the ITOP by fabricating mandible and calvarial bone, cartilage and skeletal muscle. Future development of the ITOP is being directed to the production of tissues for human applications and to the building of more complex tissues and solid organs.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Various biofunctional materials and cell types can be printed simultaneously onto a substrate of cell-compatible biomaterials to build 3D complex constructs with good spatial resolution and reproducibility.
“Various biofunctional materials and cell types can thus be printed simultaneously onto a substrate of cell-compatible biomaterials to build 3D complex constructs with good spatial resolution and reproducibility (Fig. 3a)130,148–151.”
From Tumor-on-a-chip: from bioinspired design to biomedical application (2021) · cites this paper as [150]
Cites
Calcium's Role in Mechanotransduction during Muscle Development
Damm, T. B., & Egli, M. (2014) · Cellular Physiology and Biochemistry · doi:10.1159/000356667 · Cited by 14,548 · see citing works
3D bioprinting of tissues and organs
Murphy, S. V., & Atala, A. (2014) · Nature Biotechnology · doi:10.1038/nbt.2958 · Cited by 7,034 · see citing works
Self-citationHydrogels for biomedical applications
Hoffman, A. S. (2002) · Advanced Drug Delivery Reviews · doi:10.1016/s0169-409x(01)00239-3 · Cited by 4,864 · see citing works
Bone Tissue Engineering: Recent Advances and Challenges
Amini, A. R., Laurencin, C. T., & Nukavarapu, S. P. (2012) · Critical Reviews in Biomedical Engineering · doi:10.1615/critrevbiomedeng.v40.i5.10 · Cited by 2,342 · see citing works
Isolation of amniotic stem cell lines with potential for therapy
Coppi, P. D., Bartsch, G. C., Siddiqui, M. M., et al. (2007) · Nature Biotechnology · doi:10.1038/nbt1274 · Cited by 1,877 · see citing works
Tissue-engineered autologous bladders for patients needing cystoplasty
Atala, A., Bauer, S. B., Söker, S., Yoo, J. J., & Retik, A. B. (2006) · The Lancet · doi:10.1016/s0140-6736(06)68438-9 · Cited by 1,835 · see citing works
Self-citationScaffold-free vascular tissue engineering using bioprinting
Norotte, C., Marga, F., Niklason, L. E., & Forgács, G. (2009) · Biomaterials · doi:10.1016/j.biomaterials.2009.06.034 · Cited by 1,342 · see citing works
Organ printing: computer-aided jet-based 3D tissue engineering
Mironov, V., Boland, T., Trusk, T. C., Forgács, G., & Markwald, R. R. (2003) · Trends in biotechnology · doi:10.1016/s0167-7799(03)00033-7 · Cited by 1,278 · see citing works
Cell Encapsulation in Biodegradable Hydrogels for Tissue Engineering Applications
Nicodemus, G. D., & Bryant, S. J. (2008) · Tissue Engineering Part B Reviews · doi:10.1089/ten.teb.2007.0332 · Cited by 1,242 · see citing works
Organ printing: Tissue spheroids as building blocks
Mironov, V., Visconti, R. P., Kasyanov, V., Forgacs, G., Drake, C. J., & Markwald, R. R. (2009) · Biomaterials · doi:10.1016/j.biomaterials.2008.12.084 · Cited by 1,238 · see citing works
Printing and Prototyping of Tissues and Scaffolds
Derby, B. (2012) · Science · doi:10.1126/science.1226340 · Cited by 1,108 · see citing works
3D Bioprinting of heterogeneous aortic valve conduits with alginate/gelatin hydrogels
Duan, B., Hockaday, L. A., Kang, K. H., & Butcher, J. T. (2012) · Journal of Biomedical Materials Research Part A · doi:10.1002/jbm.a.34420 · Cited by 1,005 · see citing works
The in vivo degradation, absorption and excretion of PCL-based implant
Sun, H., Mei, L., Song, C. X., Cui, X., & Wang, P. (2005) · Biomaterials · doi:10.1016/j.biomaterials.2005.09.019 · Cited by 977 · see citing works
Engineering vascularized tissue
Jain, R. K., Au, P., Tam, J., Duda, D. G., & Fukumura, D. (2005) · Nature Biotechnology · doi:10.1038/nbt0705-821 · Cited by 808 · see citing works
Application of inkjet printing to tissue engineering
Boland, T., Xu, T., Damon, B. J., & Cui, X. (2006) · Biotechnology Journal · doi:10.1002/biot.200600081 · Cited by 784 · see citing works
Human microvasculature fabrication using thermal inkjet printing technology
Cui, X., & Boland, T. (2009) · Biomaterials · doi:10.1016/j.biomaterials.2009.07.056 · Cited by 706 · see citing works
Direct Human Cartilage Repair Using Three-Dimensional Bioprinting Technology
Cui, X., Breitenkamp, K., Finn, M. G., Lotz, M., & DʼLima, D. D. (2012) · Tissue Engineering Part A · doi:10.1089/ten.tea.2011.0543 · Cited by 688 · see citing works
Xu, T., Binder, K. W., Albanna, M. Z., Dice, D. D., Zhao, W., Yoo, J. J., & Atala, A. (2012) · Biofabrication · doi:10.1088/1758-5082/5/1/015001 · Cited by 633 · see citing works
Self-citationLanders, R., Hübner, U., Schmelzeisen, R., & Mülhaupt, R. (2002) · Biomaterials · doi:10.1016/s0142-9612(02)00139-4 · Cited by 627 · see citing works
Choi, J. S., Lee, S. J., Christ, G. J., Atala, A., & Yoo, J. J. (2008) · Biomaterials · doi:10.1016/j.biomaterials.2008.03.031 · Cited by 611 · see citing works
Self-citationXu, T., Zhao, W., Zhu, J.-M., Albanna, M. Z., Yoo, J. J., & Atala, A. (2012) · Biomaterials · doi:10.1016/j.biomaterials.2012.09.035 · Cited by 609 · see citing works
Self-citationMikos, A. G., Herring, S. W., Ochareon, P., Elisseeff, J. H., Lu, H. H., Kandel, R. A., Schöen, F. J., Toner, M., Mooney, D. J., Atala, A., et al. (2006) · Tissue Engineering · doi:10.1089/ten.2006.12.3307 · Cited by 599 · see citing works
Self-citationHydrogels for Biomedical Applications
Hoffman, A. S. (2001) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2001.tb03823.x · Cited by 580 · see citing works
Lee, W., Debasitis, J., Lee, V. K., Lee, J.-H., Fischer, K., Edminster, K. R., Park, J., & Yoo, S.-S. (2009) · Biomaterials · doi:10.1016/j.biomaterials.2008.12.009 · Cited by 576 · see citing works
Atala, A., Kasper, F. K., & Mikos, A. G. (2012) · Science Translational Medicine · doi:10.1126/scitranslmed.3004890 · Cited by 545 · see citing works
Self-citationTissue-engineered autologous urethras for patients who need reconstruction: an observational study
Raya-Rivera, A. M., Esquiliano, D. R., Yoo, J. J., López‐Bayghen, E., Söker, S., & Atala, A. (2011) · The Lancet · doi:10.1016/s0140-6736(10)62354-9 · Cited by 475 · see citing works
Self-citationSkardal, A., Zhang, J., & Prestwich, G. D. (2010) · Biomaterials · doi:10.1016/j.biomaterials.2010.04.045 · Cited by 465 · see citing works
Direct‐write bioprinting three‐dimensional biohybrid systems for future regenerative therapies
Chang, C. C., Boland, E. D., Williams, S. K., & Hoying, J. B. (2011) · Journal of Biomedical Materials Research Part B Applied Biomaterials · doi:10.1002/jbm.b.31831 · Cited by 446 · see citing works
Cell patterning technologies for organotypic tissue fabrication
Guillotin, B., & Guillemot, F. (2011) · Trends in biotechnology · doi:10.1016/j.tibtech.2010.12.008 · Cited by 430 · see citing works
Ignatius, A. A., & Claes, L. (1996) · Biomaterials · doi:10.1016/0142-9612(96)81421-9 · Cited by 428 · see citing works
Fedorovich, N. E., de Wijn, J. R., Verbout, A. J., Alblas, J., & Dhert, W. J. A. (2008) · Tissue Engineering Part A · doi:10.1089/ten.a.2007.0158 · Cited by 415 · see citing works
Bioprinting of hybrid tissue constructs with tailorable mechanical properties
Schuurman, W., Khristov, V., Pot, M. W., van Weeren, P. R., Dhert, W. J. A., & Malda, J. (2011) · Biofabrication · doi:10.1088/1758-5082/3/2/021001 · Cited by 411 · see citing works
A cell-laden microfluidic hydrogel
Ling, Y., Rubin, J., Deng, Y., Huang, C., Demirci, U., Karp, J. M., & Khademhosseini, A. (2007) · Lab on a Chip · doi:10.1039/b615486g · Cited by 396 · see citing works
Engineering biological structures of prescribed shape using self-assembling multicellular systems
Jakab, K., Neagu, A., Mironov, V. A., Markwald, R. R., & Forgács, G. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0400164101 · Cited by 394 · see citing works
Bio-printing of collagen and VEGF-releasing fibrin gel scaffolds for neural stem cell culture
Lee, Y., Polio, S. R., Lee, W., Dai, G., Menon, L. G., Carroll, R. S., & Yoo, S. (2010) · Experimental Neurology · doi:10.1016/j.expneurol.2010.02.014 · Cited by 389 · see citing works
Shim, J., Lee, J., Kim, J. Y., & Cho, D. (2012) · Journal of Micromechanics and Microengineering · doi:10.1088/0960-1317/22/8/085014 · Cited by 382 · see citing works
Phillippi, J. A., Miller, E. D., Weiss, L. E., Huard, J., Waggoner, A. S., & Campbell, P. G. (2007) · Stem Cells · doi:10.1634/stemcells.2007-0520 · Cited by 361 · see citing works
Toward engineering functional organ modules by additive manufacturing
Marga, F. S., Jakab, K., Khatiwala, C. B., Shepherd, B. R., Dorfman, S., Hubbard, B. A., Colbert, S. H., & Forgács, G. (2012) · Biofabrication · doi:10.1088/1758-5082/4/2/022001 · Cited by 349 · see citing works
Bioprinting Endothelial Cells With Alginate for 3D Tissue Constructs
Khalil, S., & Sun, W. (2009) · Journal of Biomechanical Engineering · doi:10.1115/1.3128729 · Cited by 337 · see citing works
Wakelam, M. J. O. (1985) · Biochemical Journal · doi:10.1042/bj2280001 · Cited by 315 · see citing works
Skeletal muscle tissue engineering: methods to form skeletal myotubes and their applications
Ostrovidov, S., Hosseini, V., Ahadian, S., Fujie, T., Parthiban, S. P., Ramalingam, M., Bae, H., Kaji, H., & Khademhosseini, A. (2014) · Tissue Engineering Part B: Reviews · doi:10.1089/ten.teb.2013.0534 · Cited by 302 · see citing works
In vitro biocompatibility assessment of poly(ε-caprolactone) films using L929 mouse fibroblasts
Serrano, M. C., Pagani, R., Vallet‐Regí, M., Peña, J., Rámila, A., Izquierdo, I., & Portolés, M. T. (2004) · Biomaterials · doi:10.1016/j.biomaterials.2004.01.037 · Cited by 273 · see citing works
Science in three dimensions: The print revolution
Jones, N. (2012) · Nature · doi:10.1038/487022a · Cited by 249 · see citing works
Inkjet printing of macromolecules on hydrogels to steer neural stem cell differentiation
Ilkhanizadeh, S., Teixeira, A. I., & Hermanson, O. (2007) · Biomaterials · doi:10.1016/j.biomaterials.2007.05.018 · Cited by 247 · see citing works
Cabodi, M., Choi, N., Gleghorn, J. P., Lee, C. S. D., Bonassar, L. J., & Stroock, A. D. (2005) · Journal of the American Chemical Society · doi:10.1021/ja054820t · Cited by 234 · see citing works
Biofabrication: an overview of the approaches used for printing of living cells
Ferris, C. J., Gilmore, K. G., Wallace, G. G., & Panhuis, M. I. H. (2013) · Applied Microbiology and Biotechnology · doi:10.1007/s00253-013-4853-6 · Cited by 227 · see citing works
Tissue-engineered autologous vaginal organs in patients: a pilot cohort study
Raya-Rivera, A. M., Esquiliano, D. R., Fierro-Pastrana, R., López‐Bayghen, E., Valencia, P., Ordorica-Flores, R. M., Söker, S., Yoo, J. J., & Atala, A. (2014) · The Lancet · doi:10.1016/s0140-6736(14)60542-0 · Cited by 225 · see citing works
Self-citationFabrication and characterization of bio-engineered cardiac pseudo tissues
Xu, T., Baicu, C. F., Aho, M., Zile, M. R., & Boland, T. (2009) · Biofabrication · doi:10.1088/1758-5082/1/3/035001 · Cited by 212 · see citing works
Ker, D. F. E., Nain, A. S., Weiss, L. E., Wang, J., Suhan, J. P., Amon, C. H., & Campbell, P. G. (2011) · Biomaterials · doi:10.1016/j.biomaterials.2011.07.025 · Cited by 206 · see citing works
Tool-path planning for direction-parallel area milling
Park, S. C., & Choi, B. K. (2000) · Computer-Aided Design · doi:10.1016/s0010-4485(99)00080-9 · Cited by 183 · see citing works
The Tissue-Engineered Auricle: Past, Present, and Future
Bichara, D. A., O'Sullivan, N.-A., Pomerantseva, I., Zhao, X., Sundback, C. A., Vacanti, J. P., & Randolph, M. A. (2011) · Tissue Engineering Part B Reviews · doi:10.1089/ten.teb.2011.0326 · Cited by 169 · see citing works
Costa, K. D., Lee, E. J., & Holmes, J. W. (2003) · Tissue Engineering · doi:10.1089/107632703768247278 · Cited by 158 · see citing works
Stachowiak, A. N., Bershteyn, A., Tzatzalos, E., & Irvine, D. J. (2004) · Advanced Materials · doi:10.1002/adma.200400507 · Cited by 150 · see citing works
Cooper, G. M., Miller, E. D., DeCesare, G. E., et al. (2009) · Tissue Engineering Part A · doi:10.1089/ten.tea.2009.0650 · Cited by 132 · see citing works
In situ bioprinting of the skin for burns
Binder, K. W., Zhao, W., Aboushwareb, T. A., Dice, D. D., Atala, A., & Yoo, J. J. (2010) · Journal of the American College of Surgeons · doi:10.1016/j.jamcollsurg.2010.06.198 · Cited by 124 · see citing works
Self-citationRecent Trends and Challenges in Complex Organ Manufacturing
Wang, X., Yan, Y., & Zhang, R. (2009) · Tissue Engineering Part B Reviews · doi:10.1089/ten.teb.2009.0576 · Cited by 112 · see citing works
Local Tissue Geometry Determines Contractile Force Generation of Engineered Muscle Networks
Bian, W., Juhas, M. E., Pfeiler, T. W., & Bursac, N. (2011) · Tissue Engineering Part A · doi:10.1089/ten.tea.2011.0313 · Cited by 87 · see citing works
Analysis of bending behavior of native and engineered auricular and costal cartilage
Roy, R., Kohles, S. S., Zaporojan, V. V., et al. (2004) · Journal of Biomedical Materials Research Part A · doi:10.1002/jbm.a.10068 · Cited by 74 · see citing works
Durmus, N. G., Taşoğlu, S., & Demirci, U. (2013) · Nature Materials · doi:10.1038/nmat3665 · Cited by 66 · see citing works
Engineered Cartilage Covered Ear Implants for Auricular Cartilage Reconstruction
Lee, S. J., Broda, C., Atala, A., & Yoo, J. J. (2010) · Biomacromolecules · doi:10.1021/bm100856g · Cited by 62 · see citing works
Self-citationKo, I. K., Lee, B., Lee, S. J., Andersson, K., Atala, A., & Yoo, J. J. (2013) · Biomaterials · doi:10.1016/j.biomaterials.2013.01.029 · Cited by 53 · see citing works
Self-citationCell survival and proliferation after encapsulation in a chemically modified Pluronic® F127 hydrogel
Lippens, E., Swennen, I., Gironès, J., et al. (2011) · Journal of Biomaterials Applications · doi:10.1177/0885328211427774 · Cited by 45 · see citing works
A New Slicing Procedure for Rapid Prototyping Systems
Liao, Y., & Chiu, Y. Y. (2001) · The International Journal of Advanced Manufacturing Technology · doi:10.1007/s001700170034 · Cited by 42 · see citing works
Kim, J., Jeong, S. Y., Ju, Y. M., Yoo, J. J., Smith, T. L., Khang, G., Lee, S. J., & Atala, A. (2013) · Biomedical Materials · doi:10.1088/1748-6041/8/1/014107 · Cited by 33 · see citing works
Self-citationZignani, M. (2000) · Biomaterials · doi:10.1016/s0142-9612(00)00065-x · Cited by 27 · see citing works
da Graca, B., & Filardo, G. (2010) · The American Journal of Cardiology · doi:10.1016/j.amjcard.2010.08.056 · Cited by 6 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Additive manufacturing (3D printing): A review of materials, methods, applications and challenges
Ngo, T. D., Kashani, A., Imbalzano, G., Nguyen, K. T. Q., & Hui, D. (2018) · Composites Part B: Engineering · doi:10.1016/j.compositesb.2018.02.012 · Cited by 8,431 · see citing works
3D bioprinting of collagen to rebuild components of the human heart
Lee, A., Hudson, A. R., Shiwarski, D. J., Tashman, J. W., Hinton, T. J., Yerneni, S., Bliley, J. M., Campbell, P. G., & Feinberg, A. W. (2019) · Science · doi:10.1126/science.aav9051 · Cited by 1,782 · see citing works
A guide to the organ-on-a-chip
Leung, C. M., de Haan, P., Ronaldson-Bouchard, K., Kim, G.-A., Ko, J., Rho, H. S., Chen, Z., Habibovic, P., Jeon, N. L., Takayama, S., et al. (2022) · Nature Reviews Methods Primers · doi:10.1038/s43586-022-00118-6 · Cited by 1,116 · see citing works
Advances in 4D Printing: Materials and Applications
Kuang, X., Roach, D. J., Wu, J., Hamel, C. M., Ding, Z., Wang, T., Dunn, M. L., & Qi, H. J. (2019) · Advanced Functional Materials · doi:10.1002/adfm.201805290 · Cited by 1,095 · see citing works
Advances in organ-on-a-chip engineering
Zhang, B., Korolj, A., Lai, B. F. L., & Radisic, M. (2018) · Nature Reviews Materials · doi:10.1038/s41578-018-0034-7 · Cited by 1,017 · see citing works
Direct 3D bioprinting of perfusable vascular constructs using a blend bioink
Jia, W., Gungor-Ozkerim, P. S., Zhang, Y. S., Yue, K., Zhu, K., Liu, W., Pi, Q., Byambaa, B., Dokmeci, M. R., Shin, S. R., et al. (2016) · Biomaterials · doi:10.1016/j.biomaterials.2016.07.038 · Cited by 922 · see citing works
Soft and elastic hydrogel-based microelectronics for localized low-voltage neuromodulation
Liu, Y., Liu, J., Chen, S., Lei, T., Kim, Y., Niu, S., Wang, H., Wang, X., Foudeh, A. M., Tok, J. B.-H., et al. (2019) · Nature Biomedical Engineering · doi:10.1038/s41551-018-0335-6 · Cited by 811 · see citing works
Biofabrication strategies for 3D in vitro models and regenerative medicine
Moroni, L., Burdick, J. A., Highley, C., Lee, S. J., Morimoto, Y., Takeuchi, S., & Yoo, J. J. (2018) · Nature Reviews Materials · doi:10.1038/s41578-018-0006-y · Cited by 753 · see citing works
Self-citationMulti-tissue interactions in an integrated three-tissue organ-on-a-chip platform
Skardal, A., Murphy, S. V., Devarasetty, M., Mead, I., Kang, H.-W., Seol, Y.-J., Shrike Zhang, Y., Shin, S.-R., Zhao, L., Aleman, J., et al. (2017) · Scientific Reports · doi:10.1038/s41598-017-08879-x · Cited by 623 · see citing works
Self-citationHydrogel Bioink Reinforcement for Additive Manufacturing: A Focused Review of Emerging Strategies
Chimene, D., Kaunas, R., & Gaharwar, A. K. (2020) · Advanced Materials · doi:10.1002/adma.201902026 · Cited by 600 · see citing works
González-Henríquez, C. M., Sarabia-Vallejos, M. A., & Rodriguez-Hernandez, J. (2019) · Progress in Polymer Science · doi:10.1016/j.progpolymsci.2019.03.001 · Cited by 562 · see citing works
Bioinks and bioprinting technologies to make heterogeneous and biomimetic tissue constructs
Ashammakhi, N., Ahadian, S., Xu, C., Montazerian, H., Ko, H., Nasiri, R., Barros, N., & Khademhosseini, A. (2019) · Materials Today Bio · doi:10.1016/j.mtbio.2019.100008 · Cited by 549 · see citing works
Organoid-on-a-chip and body-on-a-chip systems for drug screening and disease modeling
Skardal, A., Shupe, T., & Atala, A. (2016) · Drug Discovery Today · doi:10.1016/j.drudis.2016.07.003 · Cited by 512 · see citing works
Self-citationBioprinting for vascular and vascularized tissue biofabrication
Datta, P., Ayan, B., & Ozbolat, I. T. (2017) · Acta Biomaterialia · doi:10.1016/j.actbio.2017.01.035 · Cited by 431 · see citing works
Assessment methodologies for extrusion-based bioink printability
Gillispie, G., Prim, P., Copus, J., Fisher, J., Mikos, A. G., Yoo, J. J., Atala, A., & Lee, S. J. (2020) · Biofabrication · doi:10.1088/1758-5090/ab6f0d · Cited by 426 · see citing works
Self-citationAskari, M., Afzali Naniz, M., Kouhi, M., Saberi, A., Zolfagharian, A., & Bodaghi, M. (2021) · Biomaterials Science · doi:10.1039/d0bm00973c · Cited by 369 · see citing works
Kupfer, M. E., Lin, W.-H., Ravikumar, V., Qiu, K., Wang, L., Gao, L., Bhuiyan, D. B., Lenz, M., Ai, J., Mahutga, R. R., et al. (2020) · Circulation Research · doi:10.1161/circresaha.119.316155 · Cited by 329 · see citing works
The Synergy of Scaffold-Based and Scaffold-Free Tissue Engineering Strategies
Ovsianikov, A., Khademhosseini, A., & Mironov, V. (2018) · Trends in Biotechnology · doi:10.1016/j.tibtech.2018.01.005 · Cited by 314 · see citing works
Cellular and Molecular Probing of Intact Human Organs
Zhao, S., Todorov, M. I., Cai, R., -Maskari, R. A., Steinke, H., Kemter, E., Mai, H., Rong, Z., Warmer, M., Stanic, K., et al. (2020) · Cell · doi:10.1016/j.cell.2020.01.030 · Cited by 292 · see citing works
Printed aerogels: chemistry, processing, and applications
Feng, J., Su, B.-L., Xia, H., Zhao, S., Gao, C., Wang, L., Ogbeide, O., Feng, J., & Hasan, T. (2021) · Chemical Society Reviews · doi:10.1039/c9cs00757a · Cited by 313 · see citing works
<i>In situ</i>handheld three‐dimensional bioprinting for cartilage regeneration
Di Bella, C., Duchi, S., O'Connell, C. D., Blanchard, R., Augustine, C., Yue, Z., Thompson, F., Richards, C., Beirne, S., Onofrillo, C., et al. (2018) · Journal of Tissue Engineering and Regenerative Medicine · doi:10.1002/term.2476 · Cited by 313 · see citing works
Scanningless and continuous 3D bioprinting of human tissues with decellularized extracellular matrix
Yu, C., Ma, X., Zhu, W., Wang, P., Miller, K. L., Stupin, J., Koroleva-Maharajh, A., Hairabedian, A., & Chen, S. (2019) · Biomaterials · doi:10.1016/j.biomaterials.2018.12.009 · Cited by 272 · see citing works
Engineering the multiscale complexity of vascular networks
O’Connor, C., Brady, E., Zheng, Y., Moore, E., & Stevens, K. R. (2022) · Nature Reviews Materials · doi:10.1038/s41578-022-00447-8 · Cited by 271 · see citing works
Zhang, K., Fu, Q., Yoo, J., Chen, X., Chandra, P., Mo, X., Song, L., Atala, A., & Zhao, W. (2017) · Acta Biomaterialia · doi:10.1016/j.actbio.2016.12.008 · Cited by 268 · see citing works
Self-citation3D Bioprinted in vitro metastatic models via reconstruction of tumor microenvironments
Meng, F., Meyer, C. M., Joung, D., Vallera, D. A., McAlpine, M. C., & Panoskaltsis‐Mortari, A. (2019) · Advanced Materials · doi:10.1002/adma.201806899 · Cited by 262 · see citing works
Tumor-on-a-chip: from bioinspired design to biomedical application
Liu, X., Fang, J., Huang, S., Wu, X., Xie, X., Wang, J., Liu, F., Zhang, M., Peng, Z., & Hu, N. (2021) · Microsystems & Nanoengineering · doi:10.1038/s41378-021-00277-8 · Cited by 246 · see citing works
The arrival of commercial bioprinters – Towards 3D bioprinting revolution!
Choudhury, D., Anand, S., & Naing, M. W. (2024) · International Journal of Bioprinting · doi:10.18063/ijb.v4i2.139 · Cited by 189 · see citing works
Efficient myotube formation in 3D bioprinted tissue construct by biochemical and topographical cues
Kim, W., Lee, H., Lee, J., Atala, A., Yoo, J. J., Lee, S. J., & Kim, G. H. (2020) · Biomaterials · doi:10.1016/j.biomaterials.2019.119632 · Cited by 185 · see citing works
Self-citationDesign, printing, and engineering of regenerative biomaterials for personalized bone healthcare
Jia, Z., Xu, X., Zhu, D., & Zheng, Y. (2023) · Progress in Materials Science · doi:10.1016/j.pmatsci.2023.101072 · Cited by 176 · see citing works
3D Bioprinting of Breast Cancer Models for Drug Resistance Study
Wang, Y., Shi, W., Kuss, M., Mirza, S., Qi, D., Krasnoslobodtsev, A., Zeng, J., Band, H., Band, V., & Duan, B. (2018) · ACS Biomaterials Science & Engineering · doi:10.1021/acsbiomaterials.8b01277 · Cited by 157 · see citing works
Fang, Y., Guo, Y., Wu, B., Liu, Z., Ye, M., Xu, Y., Ji, M., Chen, L., Lu, B., Nie, K., et al. (2023) · Advanced Materials · doi:10.1002/adma.202205082 · Cited by 155 · see citing works
Skylar-Scott, M. A., Huang, J. Y., Lu, A., Ng, A. H. M., Duenki, T., Liu, S., Nam, L. L., Damaraju, S., Church, G. M., & Lewis, J. A. (2022) · Nature Biomedical Engineering · doi:10.1038/s41551-022-00856-8 · Cited by 160 · see citing works
Albritton, J. L., & Miller, J. S. (2017) · Disease Models & Mechanisms · doi:10.1242/dmm.025049 · Cited by 154 · see citing works
Nakayama, K. H., Quarta, M., Paine, P., Alcazar, C., Karakikes, I., Garcia, V., Abilez, O. J., Calvo, N. S., Simmons, C. S., Rando, T. A., et al. (2019) · Communications Biology · doi:10.1038/s42003-019-0416-4 · Cited by 113 · see citing works
Bioprinting technologies for disease modeling
Memic, A., Navaei, A., Mirani, B., Cordova, J. A. V., Aldhahri, M., Dolatshahi-Pirouz, A., Akbari, M., & Nikkhah, M. (2017) · Biotechnology Letters · doi:10.1007/s10529-017-2360-z · Cited by 73 · see citing works
3D bioprinting of cell-laden constructs for regenerative medicine
Li, C., & Cui, W. (2021) · Engineered Regeneration · doi:10.1016/j.engreg.2021.11.005 · Cited by 70 · see citing works
Bioprinting and organ-on-chip applications towards personalized medicine for bone diseases
Arrigoni, C., Gilardi, M., Bersini, S., Candrian, C., & Moretti, M. (2017) · Stem Cell Reviews and Reports · doi:10.1007/s12015-017-9741-5 · Cited by 68 · see citing works
Fang, Y., Sun, W., Zhang, T., & Xiong, Z. (2022) · Biomaterials · doi:10.1016/j.biomaterials.2021.121298 · Cited by 40 · see citing works
Advancements in Soft-Tissue Prosthetics Part A: The Art of Imitating Life
Cruz, R. L. J., Ross, M. T., Powell, S. K., & Woodruff, M. A. (2020) · Frontiers in Bioengineering and Biotechnology · doi:10.3389/fbioe.2020.00121 · Cited by 39 · see citing works
Injectable Therapeutic Organoids Using Sacrificial Hydrogels
Rossen, N. S., Anandakumaran, P. N., zur Nieden, R., Lo, K., Luo, W., Park, C., Huyan, C., Fu, Q., Song, Z., Singh-Moon, R. P., et al. (2020) · iScience · doi:10.1016/j.isci.2020.101052 · Cited by 36 · see citing works
Lekkala, V. K. R., Kang, S.-Y., Liu, J., Shrestha, S., Acharya, P., Joshi, P., Zolfaghar, M., Lee, M., Vanga, M. G., Jamdagneya, P., et al. (2024) · ACS Biomaterials Science & Engineering · doi:10.1021/acsbiomaterials.4c00179 · Cited by 25 · see citing works
3D printing a biocompatible elastomer for modeling muscle regeneration after volumetric muscle loss
Kiratitanaporn, W., Berry, D. B., Mudla, A., Fried, T., Lao, A., Yu, C., Hao, N., Ward, S. R., & Chen, S. (2022) · Biomaterials Advances · doi:10.1016/j.bioadv.2022.213171 · Cited by 20 · see citing works
Advanced Bioresin Formulation for 3D-Printed Bone Scaffolds: PCLDMA and p-PLA Integration
Sakarya, D., Zorlu, T., Yücel, S., Sahin, Y. M., & Özarslan, A. C. (2024) · Polymers · doi:10.3390/polym16040534 · Cited by 10 · see citing works
Gao, Q., Yu, K., Chen, F., Lu, L., & Zhang, P. (2022) · Pharmaceutics · doi:10.3390/pharmaceutics14102108 · Cited by 8 · see citing works
- Authors
- Kang, H.-W., Lee, S. J., Ko, I. K., Kengla, C., Yoo, J. J., & Atala, A.
- Affiliations
- Wake Forest University Health Sciences (US)
- Corresponding author
- Atala, Anthony
- Venue
- Nature Biotechnology
- Published
- 2016-02-15
- Volume
- 34
- Issue
- 3
- Pages
- 312-319
- ISSN
- 0733-222X (ISSN-L)
- 1087-0156
- 1546-1696
- OpenAlex
- W2286771936
- Cited by
- 2,622
- References
- 66
- Citations by year
- 2026: 98 · 2025: 199 · 2024: 211 · 2023: 225 · 2022: 296 · 2021: 313 · 2020: 351 · 2019: 298 · 2018: 280 · 2017: 233 · 2016: 113 · 2012: 1
- FWCI
- 148.25
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature Biotechnology (publishedVersion)
- PubMed (publishedVersion)
- Scholarworks@UNIST (Ulsan National Institute of Science and Technology) (submittedVersion)
- Topics
- Physical Sciences › Engineering › Biomedical Engineering › 3D Printing in Biomedical Research
- Health Sciences › Medicine › Surgery › Tissue Engineering and Regenerative Medicine
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Medicine › Hydrogels: synthesis, properties, applications
- Keywords
- 3D bioprinting, vascularized tissue constructs, cell-laden hydrogels, biodegradable polymers, mechanical stability, computer-aided design, microchannels, nutrient diffusion, mandible, calvarial bone, cartilage, skeletal muscle, tissue engineering
- MeSH terms
- Biocompatible Materials, Humans, Mandible, Polymers, Hydrogels, Tissue Engineering, Tissue Scaffolds, Bioprinting, Printing, Three-Dimensional
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review