Abstract
Three-dimensional (3D) bioprinting is an emerging biofabrication technology, driving many innovations and opening new avenues in regenerative therapeutics. The aim of 3D bioprinting is to fabricate grafts in vitro, which can then be implanted in vivo. However, the tissue culture ex vivo carries safety risks and thereby complicated manufacturing equipment and practice are required for tissues to be implanted in the humans. The implantation of printed tissues also adds complexities due to the difficulty in maintaining the structural integrity of fabricated constructs. To tackle this challenge, the concept of in situ 3D bioprinting has been suggested in which tissues are directly printed at the site of injury or defect. Such approach could be combined with cells freshly isolated from patients to produce custom-made grafts that resemble target tissue and fit precisely to target defects. Moreover, the natural cellular microenvironment in the body can be harnessed for tissue maturation resulting in the tissue regeneration and repair. Here, we discuss literature reports on in situ 3D printing and we describe future directions and challenges for in situ 3D bioprinting. We expect that this novel technology would find great attention in different biomedical fields in near future.
References
S. Ahadian, R.B. Sadeghian, S. Salehi, S. Ostrovidov, H. Bae, M. Ramalingam, A. Khademhosseini, Bioconjugated hydrogels for tissue engineering and regenerative medicine. Bioconjugate Chem. 26 1984–2001 (2015)
S. Ahadian, R. Civitarese, D. Bannerman, M.H. Mohammadi, R. Lu, E. Wang, L. Davenport-Huyer, B. Lai, B. Zhang, Y. Zhao, S. Mandla, A. Korolj, M. Radisic, Organ-on-a-chip platforms: a convergence of advanced materials, cells, and microscale technologies. Adv. Healthc. Mater. 7, 1700506 (2018)
M. Albanna, S. Murphy, W. Zhao, I. El-Amin, J. Tan, D. Dice, H.-W. Kang, J. Jackson, A. Atala, J. Yoo, In situ bioprinting of skin for reconstruction. J. Am. Coll. Surg. 187, e8 (2012)
E.D. Anderson, I. Sastalla, N.J. Earland, M. Mahnaz, I.N. Moore, F. Otaizo-Carrasquero, T.G. Myers, C.A. Myles, S.K. Datta, I.A. Myles, Prolonging culture of primary human keratinocytes isolated from suction blisters with the Rho kinase inhibitor Y-27632. Plos One 13, e0198862 (2018)
N. Ashammakhi, O. Kaarela, Three-dimensional bioprinting can help bone. J. Craniofac. Surg. 29, 9–11 (2018)
N. Ashammakhi, S. Ahadian, F. Zengjie, K. Suthiwanich, F. Lorestani, G. Orive, S. Ostrovidov, A. Khademhosseini, Advances and future perspectives in 4D bioprinting. Biotechnol. J. 13, 1800148 (2018)
N. Ashammakhi, S. Ahadian, M.A. Darabi, M. El Tahchi, J. Lee, K. Suthiwanich, A. Sheikhi, M.R. Dokmeci, R. Oklu, A. Khademhosseini, Minimally invasive and regenerative therapeutics. Adv. Mater. 31, 1804041 (2019)
K.W. Binder, W. Zhao, T. Aboushwareb, D. Dice, A. Atala, J. Yoo, In situ bioprinting of the skin for burns. J. Am. Coll. Surg. 211, S76 (2010)
D.L. Cohen, J.I. Lipton, L.J. Bonassar, H.J.B. Lipson, Additive manufacturing for in situ repair of osteochondral defects. Biofabrication 2, 035004 (2010)
C. Colosi, S.R. Shin, V. Manoharan, S. Massa, M. Costantini, A. Barbetta, M.R. Dokmeci, M. Dentini, A. Khademhosseini, Microfluidic bioprinting of heterogeneous 3D tissue constructs using low-viscosity bioink. Adv. Mater. 28 677–684 (2016)
P. Datta, V. Ozbolat, B. Ayan, A. Dhawan, I.T. Ozbolat, Bone tissue bioprinting for craniofacial reconstruction. Biotechnol. Bioeng. 114, 2424–2431 (2017)
C. Di Bella, S. Duchi, C.D. O'Connell, R. Blanchard, C. Augustine, Z. Yue, F. Thompson, C. Richards, S. Beirne, C. Onofrillo, S.H. Bauquier, S.D. Ryan, P. Pivonka, G.G. Wallace, P.F. Choong, In situ handheld three-dimensional bioprinting for cartilage regeneration. J. Tissue. Eng. Regen. Med. 12, 611–621 (2018)
S. Duchi, C. Onofrillo, C. O’Connell, R. Blanchard, C. Augustine, A. Quigley, R. Kapsa, P. Pivonka, G. Wallace, C. Di Bella, Handheld co-axial bioprinting: Application to in situ surgical cartilage repair. Sci. Rep. 7, 5837 (2017)
N. Faramarzi, I.K. Yazdi, M. Nabavinia, A. Gemma, A. Fanelli, A. Caizzone, L.M. Ptaszek, I. Sinha, A. Khademhosseini, J.N. Ruskin, A. Tamayol, Patient-specific bioinks for 3D bioprinting of tissue engineering scaffolds. Adv. Healthc. Mater. 7, 1701347 (2018)
H. Gudapati, M. Hospodiuk, V. Ozbolat, D. Ravnic, I. Ozbolat, In-situ droplet-based bioprinting for functional skin regeneration. In: New Jersy Symposium on Biomaterials Science, (2017)
P.S. Gungor-Ozkerim, I. Inci, Y.S. Zhang, A. Khademhosseini, M.R. Dokmeci, Bioinks for 3D bioprinting: an overview. Biomater. Sci. 6, 915–946 (2018)
N. Hakimi, R. Cheng, L. Leng, M. Sotoudehfar, P.Q. Ba, N. Bakhtyar, S. Amini-Nik, M.G. Jeschke, A. Günther, Handheld skin printer: in situ formation of planar biomaterials and tissues. Lab. Chip. 18, 1440–1451 (2018)
V. Keriquel, F. Guillemot, I. Arnault, B. Guillotin, S. Miraux, J. Amédée, J.-C. Fricain, S.J.B. Catros, In vivo bioprinting for computer-and robotic-assisted medical intervention: preliminary study in mice. Biofabrication 2, 014101 (2010)
V. Keriquel, H. Oliveira, M. Rémy, S. Ziane, S. Delmond, B. Rousseau, S. Rey, S. Catros, J Amédée, F. Guillemot, J.C. Fricain, In situ printing of mesenchymal stromal cells, by laser-assisted bioprinting, for in vivo bone regeneration applications. Sci. Rep. 7, 1778 (2017)
A. Khademhosseini, R. Langer, A decade of progress in tissue engineering. Nat. Protoc. 11, 1775 (2016)
G.T. Kirby, A. Michelmore, L.E. Smith, J.D. Whittle, R.D. Short, Cell sheets in cell therapies. Cytotherapy 20, 169–180 (2018)
Y.-C. Li, Y.S. Zhang, A. Akpek, S.R. Shin, A. Khademhosseini, 4D bioprinting: the next-generation technology for biofabrication enabled by stimuli-responsive materials. Biofabrication 9, 012001 (2016)
Z. Li, C.C. Tasan, H. Springer, B. Gault, D. Raabe, Interstitial atoms enable joint twinning and transformation induced plasticity in strong and ductile high-entropy alloys. Sci. Rep. 7, 40704 (2017)
W. Liu, Y.S. Zhang, M.A. Heinrich, F.D. Ferrari, H.L. Jang, S.M. Bakht, M.M. Alvarez, J. Yang, Y.C. Li, G.T. Santiago, A.K. Miri, K. Zhu, P. Khoshakhlagh, G. Prakash, H. Cheng, X. Guan, Z. Zhong, J. Ju, G.H. Zhu, S.R. Shin, M.R. Dokmeci, A. Khademhosseini, Rapid continuous multimaterial extrusion bioprinting Adv. Mater. 29, 1604630 (2017)
A.K. Miri, D. Nieto, L. Iglesias, H. Goodarzi Hosseinabadi, S. Maharjan, G.U. Ruiz-Esparza, P. Khoshakhlagh, A. Manbachi, M.R. Dokmeci, S. Chen, S.R. Shin, Y.S. Zhang, A. Khademhosseini, Microfluidics-enabled multimaterial maskless stereolithographic bioprinting. Adv. Mater. 30, 1800242 (2018)
A. Skardal, D. Mack, E. Kapetanovic, A. Atala, J.D. Jackson, J. Yoo, S. Soker, Bioprinted amniotic fluid-derived stem cells accelerate healing of large skin wounds. Stem. Cells Transl. Med. 1, 792–802 (2012)
A. Skardal, S.V. Murphy, K. Crowell, D. Mack, A. Atala, S. Soker, A tunable hydrogel system for long-term release of cell-secreted cytokines and bioprinted in situ wound cell delivery. J. Biomed. Mater. Res. B Appl. Biomater. 105, 1986–2000 (2017)
P. Sofokleous, E. Stride, W. Bonfield, M.J.M.S. Edirisinghe, Design, construction and performance of a portable handheld electrohydrodynamic multi-needle spray gun for biomedical applications. Mater. Sci. Eng. C Mater. Biol. Appl. 33, 213–223 (2013)
R. Sood, D.E. Roggy, M.J. Zieger, M. Nazim, B.C. Hartman, J.T. Gibbs A comparative study of spray keratinocytes and autologous meshed split-thickness skin graft in the treatment of acute burn injuries, Wounds 27 31–40 (2015)
N. Taira, K. Ino, J. Robert, H. Shiku, Electrochemical printing of calcium alginate/gelatin hydrogel. Electrochem. Acta 281, 429–436 (2018)
N. Tellisi, N.A. Ashammakhi, F. Billi, O. Kaarela, Three dimensional printed bone implants in the clinic. J. Craniofac. Surg. 29, 2363–2367 (2018)
M. Wang, J. He, Y. Liu, M. Li, D. Li, Z. Jin, The trend towards in vivo bioprinting. Int. J. Bioprinting 1, 15–26 (2015a)
S. Wang, J.M. Lee, W.Y. Yeong, Smart hydrogels for 3D bioprinting. Int. J. Bioprinting 1, 3–14 (2015b)
Y.S. Zhang, A. Arneri, S. Bersini, S.-R. Shin, K. Zhu, Z. Goli-Malekabadi, J. Aleman, C. Colosi, F. Busignani, V. Dell'Erba, C. Bishop, T. Shupe, D. Demarchi, M. Moretti, M. Rasponi, M.R. Dokmeci, A. Atala, A. Khademhosseini, Bioprinting 3D microfibrous scaffolds for engineering endothelialized myocardium and heart-on-a-chip. Biomaterials 110, 45–59 (2016)
Y.S. Zhang, K. Yue, J. Aleman, K. Mollazadeh-Moghaddam, S.M. Bakht, J. Yang, W. Jia, V. Dell’Erba, P. Assawes, S.R. Shin, M.R. Dokmeci, R. Oklu, A. Khademhosseini, 3D bioprinting for tissue and organ fabrication. Ann. Biomed. Eng. 45, 148–163 (2017)
Acknowledgements
The authors acknowledge funding from the National Institutes of Health (EB021857, AR066193, AR057837, CA214411, HL137193, EB024403, EB023052, EB022403, and EB021857), and Air Force Office of Sponsored Research under award #FA9550-15-1-0273.
Author information
Authors and Affiliations
Corresponding authors
Ethics declarations
Conflict of interest
The authors have no competing interests.
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Ashammakhi, N., Ahadian, S., Pountos, I. et al. In situ three-dimensional printing for reparative and regenerative therapy. Biomed Microdevices 21, 42 (2019). https://doi.org/10.1007/s10544-019-0372-2
Published:
DOI: https://doi.org/10.1007/s10544-019-0372-2