AccScience Publishing / IJB / Volume 10 / Issue 1 / DOI: 10.36922/ijb.1214
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REVIEW

Droplet-based bioprinting for fabrication of tumor spheroids

Congying Liu1 Yuhe Chen1 Huawei Chen1 Pengfei Zhang1*
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1 School of Mechanical Engineering and Automation, Beihang University, Beijing, China
IJB 2024, 10(1), 1214 https://doi.org/10.36922/ijb.1214
Submitted: 30 June 2023 | Accepted: 14 August 2023 | Published: 2 January 2024
(This article belongs to the Special Issue Bioprinting process for tumor model development)
© 2024 by the Author(s). This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution 4.0 International License ( https://creativecommons.org/licenses/by/4.0/ )
Abstract

Cancer is now one of the leading causes of mortality worldwide, and the cancer treatment development is still slow due to the lack of efficient in vitro tumor models for studying tumorigenesis and facilitating drug development. Multicellular tumor spheroids can recapitulate the critical properties of tumors in vivo, including spatial organization, physiological responses, and metabolism, and are considered powerful platform for disease study and drug screening. Although several spheroid fabrication methods have been developed, most of them result in uncontrolled cell aggregations, yielding spheroids of variable size and function. Droplet-based bioprinting is capable of depositing cells in spatiotemporal manner so as to control the composition and distribution of printed biological constructs, thereby facilitating high-throughput fabrication of complicated and reproducible tumor spheroids. In this review, we introduce the progress of droplet-based bioprinting technology for the fabrication of tumor spheroids. First, different droplet-based bioprinting technologies are compared in terms of their strengths and shortcomings, which should be taken into account while fabricating tumor spheroids. Second, the latest advances in modeling distinct types of cancers and the enabled applications with tumor spheroids are summarized. Finally, we discuss the challenges and potentials revolving around the advances of bioprinting technology, improvement of spheroid quality, and integration of different technologies.

Keywords
Droplet-based bioprinting
Tumor spheroids
Tumor heterogeneity
Diagnosis
Anti-cancer drug screening
Funding
This work was supported by the National Natural Science Foundation of China (Grant Number 52205296) and National Science Fund for Excellent Young Scholars (Overseas).
References
  1. Xia C, Dong X, Li H, et al. Cancer statistics in China and United States, 2022: Profiles, trends, and determinants. Chin Med J (Engl). 2022;135(5):584-590. doi: 10.1097/CM9.0000000000002108
  2. Siegel RL, Miller KD, Fuchs HE, Jemal A. Cancer statistics, 2022. CA Cancer J Clin. 2022;72(1):7-33. doi: 10.3322/caac.21708
  3. Ferlay J, Colombet M, Soerjomataram I, et al. Cancer statistics for the year 2020: An overview. Int J Cancer. 2021; 149(4):778-789. doi: 10.1002/ijc.33588
  4. Zugazagoitia J, Guedes C, Ponce S, Ferrer I, Molina-Pinelo S, Paz-Ares L. Current challenges in cancer treatment. Clin Ther. 2016;38(7):1551-1566. doi: 10.1016/j.clinthera.2016.03.026
  5. Zhuang P, Chiang YH, Fernanda MS, He M. Using spheroids as building blocks towards 3D bioprinting of tumor microenvironment. Int J Bioprint. 2021;7(4):1-26. doi: 10.18063/ijb.v7i4.444
  6. Jo Y, Choi N, Kim K, Koo H-J, Choi J, Kim HN. Chemoresistance of cancer cells: Requirements of tumor microenvironment-mimicking in vitro models in anti-cancer drug development. Theranostics. 2018;8(19):5259- 5275. doi: 10.7150/thno.29098
  7. Chramiec A, 2022; A novel human multi-tissue system for preclinical drug evaluation and recapitulation of metastasis, thesis, ProQuest Dissertations & Theses Global, Columbia University, 28963406.
  8. Dhiman HK, Ray AR,Panda AK. Three-dimensional chitosan scaffold-based MCF-7 cell culture for the determination of the cytotoxicity of tamoxifen. Biomaterials. 2005;26(9):979-986. doi: 10.1016/j.biomaterials.2004.04.012
  9. Imamura Y, Mukohara T, Shimono Y, et al. Comparison of 2D- and 3D-culture models as drug-testing platforms in breast cancer. Oncol Rep. 2015; 33(4):1837-1843. doi: 10.3892/or.2015.3767
  10. Hoarau-Vechot J, Rafii A, Touboul C, Pasquier J. Halfway between 2D and animal models: Are 3D cultures the ideal tool to study cancer-microenvironment interactions? Int J Mol Sci. 2018;19(1):181. doi: 10.3390/ijms19010181
  11. Kapalczynska M, Kolenda T, Przybyla W, et al. 2D and 3D cell cultures - a comparison of different types of cancer cell cultures. Arch Med Sci. 2018;14(4):910-919. doi: 10.5114/aoms.2016.63743
  12. Lin RZ, Chou LF, Chien CC, Chang H-Y. Dynamic analysis of hepatoma spheroid formation: Roles of E-cadherin and beta1-integrin. Cell Tissue Res. 2006;324(3):411-422. doi: 10.1007/s00441-005-0148-2
  13. Nath S, Devi GR. Three-dimensional culture systems in cancer research: Focus on tumor spheroid model. Pharmacol Ther. 2016;163: 94-108. doi: 10.1016/j.pharmthera.2016.03.013
  14. Xu T, Kincaid H, Atala A, Yoo J. High-throughput production of single-cell microparticles using an inkjet printing technology. J Manuf Sci E-T Asme. 2008;130(2):021017. doi: 10.1115/1.2903064
  15. Gao G, Yonezawa T, Hubbell K, Dai G, Cui X. Inkjet-bioprinted acrylated peptides and PEG hydrogel with human mesenchymal stem cells promote robust bone and cartilage formation with minimal printhead clogging. Biotechnol J. 2015;10(10):1568-1577. doi: 10.1002/biot.201400635
  16. Xu T, Gregory CA, Molnar P, et al. Viability and electrophysiology of neural cell structures generated by the inkjet printing method. Biomaterials. 2006;27(19):3580- 3588. doi: 10.1016/j.biomaterials.2006.01.048
  17. Campbell A, Philipovskiy A, Heydarian R, Varela-Ramirez A. 2D and 3D thermally bioprinted human MCF-7 breast cancer cells: A promising model for drug discovery. J Clin Oncol. 2019;37(15):2605. doi: 10.1200/JCO.2019.37.15_suppl.2605
  18. Xu T, Zhao W, Zhu JM, Albanna MZ, Yoo JJ, Atala A. Complex heterogeneous tissue constructs containing multiple cell types prepared by inkjet printing technology. Biomaterials. 2013;34(1):130-139. doi: 10.1016/j.biomaterials.2012.09.035
  19. Xu T, Jin J, Gregory C, J Hickman JJJ, Boland T. Inkjet printing of viable mammalian cells. Biomaterials. 2005;26(1):93-99. doi: 10.1016/j.biomaterials.2004.04.011
  20. Xu C, Chai W, Huang Y, Markwald RR. Scaffold-free inkjet printing of three-dimensional zigzag cellular tubes. Biotechnol Bioeng. 2012;109(12):3152-3160. doi: 10.1002/bit.24591
  21. Cheng E, Yu H, Ahmadi A, Cheung KC. Investigation of the hydrodynamic response of cells in drop on demand piezoelectric inkjet nozzles. Biofabrication. 2016;8(1): 015008. doi: 10.1088/1758-5090/8/1/015008
  22. Wijshoff H. The dynamics of the piezo inkjet printhead operation. Phys Rep. 2010;491(4-5):77-177. doi: 10.1016/j.physrep.2010.03.003
  23. Shi J, Wu B, Li S, Song J, Song Band Lu WF. Shear stress analysis and its effects on cell viability and cell proliferation in drop-on-demand bioprinting. Biomed Phys Eng Expr. 2018;4(4):045028. doi: 10.1088/2057-1976/aac946
  24. Kamisuki S, Hagata T, Tezuka C, Nose Y, Fujii M, Atobe M. A low power, small, electrostatically driven driven commercial inkjet head. Micro Electro Mechanical Systems - Ieee Eleventh Annual International Workshop Proceedings. 1998;1998;63-68.
  25. Nishiyama Y, Nakamura M, Henmi C, et al. Development of a three-dimensional bioprinter: construction of cell supporting structures using hydrogel and State-Of-The-Art inkjet technology. J Biomech Eng. 2009;131(3):035001. doi: 10.1115/1.3002759
  26. Gao D, Yao D, Leist SK, Fei Y, Zhou J. Mechanisms and modeling of electrohydrodynamic phenomena. Int J Bioprint. 2019;5(1):166. doi: 10.18063/ijb.v5i1.166
  1. Eagles PA, Qureshi AN, Jayasinghe SN. Electrohydrodynamic jetting of mouse neuronal cells. Biochem J. 2006;394(2): 375-378. doi: 10.1042/BJ20051838
  2. Workman VL, Tezera LB, Elkington PT, Jayasinghe SN. Controlled generation of microspheres incorporating extracellular matrix fibrils for three-dimensional cell culture. Adv Funct Mater. 2014;24(18):2648-2657. doi: 10.1002/adfm.201303891
  3. Gasperini L, Maniglio D, Motta A, Migliaresi C. An electrohydrodynamic bioprinter for alginate hydrogels containing living cells. Tissue Eng Part C Methods. 2015;21(2):123-132. doi: 10.1089/ten.TEC.2014.0149
  4. Chen CH, Saville DA, Aksay IA. Electrohydrodynamic “drop-and-place” particle deployment. Appl Phys Lett. 2006;88(15):154104. doi: 10.1063/1.2191733
  5. Poellmann MJ, Barton KL, Mishra S, Johnson AJW. Patterned hydrogel substrates for cell culture with electrohydrodynamic jet printing. Macromol Biosci. 2011;11(9):1164-1168. doi: 10.1002/mabi.201100004
  6. Gudapati H, Dey M, Ozbolat I. A comprehensive review on droplet-based bioprinting: Past, present and future. Biomaterials. 2016;102: 20-42. doi: 10.1016/j.biomaterials.2016.06.012
  7. Onses MS, Sutanto E, Ferreira PM, Alleyne AG, Rogers JA. Mechanisms, capabilities, and applications of high-resolution electrohydrodynamic jet printing. Small. 2015;11(34):4237-4266. doi: 10.1002/smll.201500593
  8. Kim HS, Lee DY, Park JH, Hwang JH, Jung HI. Optimization of electrohydrodynamic writing technique to print collagen. Exp Tech. 2007;31(4):15-19. doi: 10.1111/j.1747-1567.2007.00154.x
  9. Chen X, O’Mahony AP,Barber T. The assessment of average cell number inside in-flight 3D printed droplets in microvalve-based bioprinting. J Appl Phys. 2022;131(22):224701. doi: 10.1063/5.0096468
  10. Ng WL, Lee JM, Yeong WY, Naing MW. Microvalve-based bioprinting process, bioinks and applications. Biomater Sci. 2017;5(4):632-647. doi: 10.1039/c6bm00861e
  11. Faulkner-Jones A, Fyfe C, Cornelissen DJ, et al. Bioprinting of human pluripotent stem cells and their directed differentiation into hepatocyte-like cells for the generation of mini-livers in 3D. Biofabrication. 2015;7(4):044102. doi: 10.1088/1758-5090/7/4/044102
  12. Chen X, O’Mahony AP, Barber T. Experimental study of the stable droplet formation process during micro-valve-based three-dimensional bioprinting. Phys Fluids. 2023;35(1):011903. doi: 10.1063/5.0129985
  13. Xu F, Moon SJ, Emre AE, et al. A droplet-based building block approach for bladder smooth muscle cell (SMC) proliferation. Biofabrication. 2010;2(1):014105. doi: 10.1088/1758-5082/2/1/014105
  14. Xu F, Celli J, Rizvi I, Moon Sangjun, Hasan T, Demirci U. A three-dimensional in vitro ovarian cancer coculture model using a high-throughput cell patterning platform. Biotechnol J. 2011;6(2):204-212. doi: 10.1002/biot.201000340
  15. Demirci U, Montesano G. Cell encapsulating droplet vitrification. Lab Chip. 2007;7(11):1428-1433. doi: 10.1039/b705809h
  16. Faulkner-Jones A, Greenhough S, King JA, Gardner J, Courtney A, Shu W. Development of a valve-based cell printer for the formation of human embryonic stem cell spheroid aggregates. Biofabrication. 2013;5(1):015013. doi: 10.1088/1758-5082/5/1/015013
  17. Lee W, Debasitis JC, Lee VK, et al. Multi-layered culture of human skin fibroblasts and keratinocytes through three-dimensional freeform fabrication. Biomaterials. 2009;30(8):1587-1595. doi: 10.1016/j.biomaterials.2008.12.009
  18. Moon S, Hasan SK, Song YS, et al. Layer by layer three-dimensional tissue epitaxy by cell-laden hydrogel droplets. Tissue Eng Part C-Me. 2010;16(1):157-166. doi: 10.1089/ten.tec.2009.0179
  19. Jentsch S, Nasehi R, Kuckelkorn C, Gundert B, Aveic S, Fischer H. Multiscale 3D bioprinting by nozzle-free acoustic droplet ejection. Small Methods. 2021;5(6):2000971. doi: 10.1002/smtd.202000971
  20. Chen K, Jiang E, Wei X, et al. The acoustic droplet printing of functional tumor microenvironments. Lab Chip. 2021;21(8):1604-1612. doi: 10.1039/d1lc00003a
  21. Hadimioglu B, Stearns R, Ellson R. Moving liquids with sound: The physics of acoustic droplet ejection for robust laboratory automation in life sciences. J Lab Autom. 2016;21(1):4-18. doi: 10.1177/2211068215615096
  22. Elrod SA, Hadimioglu B, Khuri-Yakub BT, et al. Nozzleless droplet formation with focused acoustic beams. J Appl Phys. 1989;65(9):3441-3447. doi: 10.1063/1.342663
  23. Demirci U, Montesano G. Single cell epitaxy by acoustic picolitre droplets. Lab Chip. 2007;7(9):1139-1145. doi: 10.1039/b704965j
  24. Sriphutkiat Y, Kasetsirikul S, Ketpun D, Zhou Y. Cell alignment and accumulation using acoustic nozzle for bioprinting. Sci Rep. 2019;9(1):17774. doi: 10.1038/s41598-019-54330-8
  25. Chen Y, Liu X, Zhang C, Zhao Y. Enhancing and suppressing effects of an inner droplet on deformation of a double emulsion droplet under shear. Lab Chip. 2015;15(5):1255-1261. doi: 10.1039/c4lc01231c
  26. Zhang S, Li G, Man J, et al. Fabrication of microspheres from high-viscosity bioink using a novel microfluidic-based 3D bioprinting nozzle. Micromachine Basel. 2020; 11(7):681. doi: 10.3390/mi11070681
  27. Mesquita CRS, Charelli LE, Baptista LS, Naveira-Cotta CP, Balbino TA. 2021;Continuous-mode encapsulation of human stem cell spheroids using droplet-based glass-capillary microfluidic device for 3D bioprinting technology. Biochem Eng J. 174: 8. doi: 10.1016/j.bej.2021.108122
  28. Zhang P, Abate AR. High-definition single-cell printing: cell-by-cell fabrication of biological structures. Adv Mater. 2020;32(52):2005346. doi: 10.1002/adma.202005346
  29. Gunti S, Hoke ATK, Vu KP, London NR. Organoid and spheroid tumor models: Techniques and applications. Cancers. 2021;13(4):874. doi: 10.3390/cancers13040874
  30. Fennema E, Rivron N, Rouwkema J, van Blitterswijk C, de Boer J. Spheroid culture as a tool for creating 3D complex tissues. Trends Biotechnol. 2013;31(2):108-115. doi: 10.1016/j.tibtech.2012.12.003
  31. Baghban R, Roshangar L, Jahanban-Esfahlan R, et al. Tumor microenvironment complexity and therapeutic implications at a glance. Cell Commun Signal. 2020;18(1):59. doi: 10.1186/s12964-020-0530-4
  32. Vinci M, Gowan S, Boxall F, et al. Advances in establishment and analysis of three-dimensional tumor spheroid-based functional assays for target validation and drug evaluation. Bmc Biology. 2012;10: 29. doi: 10.1186/1741-7007-10-29
  33. Qi X, Prokhorova AV, Mezentsev AV, et al. Comparison of EMT-related and multi-drug resistant gene expression, extracellular matrix production, and drug sensitivity in NSCLC spheroids generated by scaffold-free and scaffold-based methods. Int J Mol Sci. 2022;23(21):13306. doi: 10.3390/ijms232113306
  34. Ho WJ, Pham EA, Kim JW, et al. Incorporation of multicellular spheroids into 3-D polymeric scaffolds provides an improved tumor model for screening anticancer drugs. Cancer Sci. 2010;101(12):2637-2643. doi: 10.1111/j.1349-7006.2010.01723.x
  35. Qiu P, Qu X, Brackett DJ, Lerner MR, Li D, Mao C. Silica-based branched hollow microfibers as a biomimetic extracellular matrix for promoting tumor cell growth in vitro and in vivo. Adv Mater. 2013;25(17):2492-2496. doi: 10.1002/adma.201204472
  36. Ong SM, Zhao Z, Arooz T, et al. Engineering a scaffold-free 3D tumor model for in vitro drug penetration studies. Biomaterials. 2010;31(6):1180-1190. doi: 10.1016/j.biomaterials.2009.10.049
  37. Oliveira MB, Neto AI, Correia CR, Rial-Hermida MI, Alvarez-Lorenzo C, Mano JF. Superhydrophobic chips for cell spheroids high-throughput generation and drug screening. ACS Appl Mater Interfaces. 2014;6(12):9488-9495. doi: 10.1021/am5018607
  38. Franchi-Mendes T, Lopes N, Brito C. Heterotypic tumor spheroids in agitation-based cultures: A scaffold-free cell model that sustains long-term survival of endothelial cells. Front Bioeng Biotechnol. 2021;9: 649949. doi: 10.3389/fbioe.2021.649949
  39. Tu TY, Wang Z, Bai J, et al. Rapid prototyping of concave microwells for the formation of 3D multicellular cancer aggregates for drug screening. Adv Healthc Mater. 2014;3(4):609-616. doi: 10.1002/adhm.201300151
  40. Kim JA, Choi JH, Kim M, et al. High-throughput generation of spheroids using magnetic nanoparticles for three-dimensional cell culture. Biomaterials. 2013;34(34):8555-8563. doi: 10.1016/j.biomaterials.2013.07.056
  41. Bowser DA, Moore MJ. 2019;Biofabrication of neural microphysiological systems using magnetic spheroid bioprinting. Biofabrication. 12(1):015002. doi: 10.1088/1758-5090/ab41b4
  42. Chen K, Wu M, Guo F, et al. Rapid formation of size-controllable multicellular spheroids via 3D acoustic tweezers. Lab Chip. 2016;16(14):2636-2643. doi: 10.1039/c6lc00444j
  43. Rasouli R, Tabrizian M. Rapid formation of multicellular spheroids in boundary-driven acoustic microstreams. Small. 2021;17(39):2101931. doi: 10.1002/smll.202101931
  44. Sebastian A, Buckle AM, Markx GH. Tissue engineering with electric fields: Immobilization of mammalian cells in multilayer aggregates using dielectrophoresis. Biotechnol Bioeng. 2007;98(3):694-700. doi: 10.1002/bit.21416
  45. Maris JM, Matthay KK. Molecular biology of neuroblastoma. J Clin Oncol. 1999;17(7):2264. doi: 10.1200/jco.1999.17.7.2264
  46. Bhoopathi P, Pradhan AK, Bacolod MD, et al. Regulation of neuroblastoma migration, invasion, and in vivo metastasis by genetic and pharmacological manipulation of MDA-9/ Syntenin. Oncogene. 2019;38(41):6781-6793. doi: 10.1038/s41388-019-0920-5
  47. Ducker M, Millar V, Ebner D, Szele FG. A semi-automated and scalable 3D spheroid assay to study neuroblast migration. Stem Cell Rep. 2020;15(3):789-802. doi: 10.1016/j.stemcr.2020.07.012
  48. Utama RH, Atapattu L, O’Mahony AP, et al. A 3D bioprinter specifically designed for the high-throughput production of matrix-embedded multicellular spheroids. iScience. 2020;23(10):101621. doi: 10.1016/j.isci.2020.101621
  49. Martin-Belmonte F, Perez-Moreno M. Epithelial cell polarity, stem cells and cancer. Nat Rev Cancer. 2011;12(1):23-38. doi: 10.1038/nrc3169
  50. Trondle K, Rizzo L, Pichler R, et al. Scalable fabrication of renal spheroids and nephron-like tubules by bioprinting and controlled self-assembly of epithelial cells. Biofabrication. 2021;13(3):035019. doi: 10.1088/1758-5090/abe185
  51. Caruso S, Calatayud AL, Pilet J, et al. Analysis of liver cancer cell lines identifies agents with likely efficacy against hepatocellular carcinoma and markers of response. Gastroenterology. 2019;157(3):760-776. doi: 10.1053/j.gastro.2019.05.001
  52. Chen Y, Sun W, Kang L, et al. Microfluidic co-culture of liver tumor spheroids with stellate cells for the investigation of drug resistance and intercellular interactions. Analyst. 2019;144(14):4233-4240. doi: 10.1039/c9an00612e
  53. Khomich O, Ivanov AV, Bartosch B. Metabolic hallmarks of hepatic stellate cells in liver fibrosis. Cells. 2020;9(1):24. doi: 10.3390/cells9010024
  54. Hong G, Kim J, Oh H, et al. Production of multiple cell-laden microtissue spheroids with a biomimetic hepatic-lobule-like structure. Adv Mater. 2021;33(36):2102624. doi: 10.1002/adma.202102624
  55. Zhang P, Li X, Chen JY, Abate AR. Controlled fabrication of functional liver spheroids with microfluidic flow cytometric printing. Biofabrication. 2022;14(4):045011. doi: 10.1088/1758-5090/ac8622
  56. Trounson A. The production and directed differentiation of human embryonic stem cells. Endocr Rev. 2006;27(2):208-219. doi: 10.1210/er.2005-0016
  57. Sun YS, Zhao Z, Yang ZN, et al. Risk factors and preventions of breast cancer. Int J Biol Sci. 2017;13(11):1387-1397. doi: 10.7150/ijbs.21635
  58. Polyak K. Breast cancer: origins and evolution. J Clin Invest. 2007;117(11):3155-3163. doi: 10.1172/JCI33295
  59. Markovitz-Bishitz Y, Tauber Y, Afrimzon E, et al. A polymer microstructure array for the formation, culturing, and high throughput drug screening of breast cancer spheroids. Biomaterials. 2010;31(32):8436-8444. doi: 10.1016/j.biomaterials.2010.07.050
  60. Ling K, Huang G, Liu J, et al. Bioprinting-based high-throughput fabrication of three-dimensional MCF-7 human breast cancer cellular spheroids. Engineering. 2015;1(2):269- 274. doi: 10.15302/j-eng-2015062
  61. Johnson PA, Menegatti S, Chambers AC, et al. A rapid high throughput bioprinted colorectal cancer spheroid platform for in vitro drug- and radiation-response. Biofabrication. 2022;15(1):014103. doi: 10.1088/1758-5090/ac999f
  62. Wang H, Tian T, Zhang J. Tumor-associated macrophages (TAMs) in colorectal cancer (CRC):From mechanism to therapy and prognosis. Int J Mol Sci. 2021;22(16):8470. doi: 10.3390/ijms22168470
  63. Jiang L, Ji N, Zhou Y, et al. CAL 27 is an oral adenosquamous carcinoma cell line. Oral Oncol. 2009;45(11):204-207. doi: 10.1016/j.oraloncology.2009.06.001
  64. Tanaka T, Ishigamori R. Understanding carcinogenesis for fighting oral cancer. J Oncol. 2011;2011: 603740. doi: 10.1155/2011/603740
  65. Kronemberger GS, Miranda G, Tavares RSN, Montenegro B. Recapitulating tumorigenesis in vitro: opportunities and challenges of 3D bioprinting. Front Bioeng Biotechnol. 2021;9: 682498. doi: 10.3389/fbioe.2021.682498
  66. Ota H, Miki N. Microfluidic experimental platform for producing size-controlled three-dimensional spheroids. Sens Actuators, A. 2011;169(2):266-273. doi: 10.1016/j.sna.2011.03.051
  67. Dornhof J, Zieger V, Kieninger J, et al. Bioprinting-based automated deposition of single cancer cell spheroids into oxygen sensor microelectrode wells. Lab Chip. 2022;22(22):4369-4381. doi: 10.1039/d2lc00705c
  68. Chang HN, Moo-Young M. Estimation of oxygen penetration depth in immobilized cells. Appl Microbiol Biotechnol. 1988;29(2):107-112. doi: 10.1007/BF00939293
  69. Rouwkema J, Rivron NC,van Blitterswijk CA. Vascularization in tissue engineering. Trends Biotechnol. 2008;26(8): 434-441. doi: 10.1016/j.tibtech.2008.04.009
  70. Lee VK, Guohao D, Hongyan Z, Yoo S. Generation of 3-D glioblastoma-vascular niche using 3-D bioprinting. Proceedings of the 41st Annual Northeast Biomedical Engineering Conference (NEBEC). 2015;1-2.
  71. Trondle K, Koch F, Finkenzeller G, et al. Bioprinting of high cell-density constructs leads to controlled lumen formation with self-assembly of endothelial cells. J Tissue Eng Regen Med. 2019;13(10):1883-1895. doi: 10.1002/term.2939
  72. Chambers AF, Groom AC, MacDonald IC. Dissemination and growth of cancer cells in metastatic sites. Nat Rev Cancer. 2002;2(8):563-572. doi: 10.1038/nrc865
  73. Yilmaz M, Christofori G, Lehembre F. Distinct mechanisms of tumor invasion and metastasis. Trends Mol Med. 2007;13(12):535-541. doi: 10.1016/j.molmed.2007.10.004
  74. Pennacchietti S, Michieli P, Galluzzo M, Mazzone M, Giordano S, Comoglio PM. Hypoxia promotes invasive growth by transcriptional activation of the met protooncogene. Cancer Cell. 2003;3(4):347-361. doi: 10.1016/S1535-6108(03)00085-0
  75. Chen H, Du L, Li J, et al. Modeling cancer metastasis using acoustically bio-printed patient-derived 3D tumor microtissues. J Mater Chem B. 2022;10(11): 1843-1852. doi: 10.1039/d1tb02789a
  76. Seftor RE, Hess AR, Seftor EA, et al. Tumor cell vasculogenic mimicry: From controversy to therapeutic promise. Am J Pathol. 2012;181(4):1115-1125. doi: 10.1016/j.ajpath.2012.07.013
  77. Lee JM, Choi JW, Ahrberg CD, et al. Generation of tumor spheroids using a droplet-based microfluidic device for photothermal therapy. Microsyst Nanoeng. 2020;6(1):52. doi: 10.1038/s41378-020-0167-x
  78. Yu L, Chen MC, Cheung KC. Droplet-based microfluidic system for multicellular tumor spheroid formation and anticancer drug testing. Lab Chip. 2010;10(18):2424-2432. doi: 10.1039/c004590j
  79. Shi J, Song J, Song B, Lu WF. Multi-objective optimization design through machine learning for Drop-on-Demand bioprinting. Engineering. 2019;5(3):586-593. doi: 10.1016/j.eng.2018.12.009
  80. Ota S, Horisaki R, Kawamura Y, et al. Ghost cytometry. Science. 2018;360(6394):1246-1251. doi: 10.1126/science.aan0096
  81. De Moor L, Merovci I, Baetens S, et al. High-throughput fabrication of vascularized spheroids for bioprinting. Biofabrication. 2018;10(3):035009. doi: 10.1088/1758-5090/aac7e6
  82. Souza TKF, Nucci MP, Mamani JB, et al. Image and motor behavior for monitoring tumor growth in C6 glioma model. PLoS ONE. 2018;13(7):e0201453. doi: 10.1371/journal.pone.0201453
  83. 109. Liu J, Li K, Liu B. Far-red/near-infrared conjugated polymer nanoparticles for long-term in situ monitoring of liver tumor growth. Adv Sci. 2015;2(5):1500008. doi: 10.1002/advs.201500008
Conflict of interest
The authors declare no conflicts of interest.
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International Journal of Bioprinting, Electronic ISSN: 2424-8002 Print ISSN: 2424-7723, Published by AccScience Publishing