Human tissues in a dish: The research and ethical implications of organoid technology
Open accessAbstract
Ethics of organoid research: Growing functional human tissues and organs would provide much needed material for regeneration and repair. New technologies are taking us in that direction. In addition to their use in regenerative medicine, stem cells that grow and morph into organ-like structures known as organoids can be used in drug development and toxicology testing. The potential developments and possibilities are numerous and affect not only biomedicine but also areas of ongoing ethical debate, such as animal experimentation, research on human embryos and fetuses, ethics review, and patient consent. Bredenoord et al. review how organoids affect existing ethical debates and how they raise novel ethical dilemmas and professional responsibilities. Science , this issue p. 10.1126/science.aaf9414
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?
Reproducibility in multi-cellular and multi-tissue organoid systems decreases as it is challenging to coordinate proliferation and differentiation of multiple cell types.
“As recently discussed in another review focused on hepatic, biliary and pancreatic (HBP) organoids230, reproducibility in multi-cellular and multi-tissue organoid systems decreases as it is challenging to coordinate proliferation and differentiation of multiple cell types.”
From Organoids (2022) · cites this paper as [230]
Cites
<i>The Structure of Scientific Revolutions</i>
Kuhn, T. S., & Schlegel, R. (1963) · Physics Today · doi:10.1063/1.3050879 · Cited by 35,538 · see citing works
Modeling Development and Disease with Organoids
Clevers, H. (2016) · Cell · doi:10.1016/j.cell.2016.05.082 · Cited by 3,196 · see citing works
Self-citationOrganogenesis in a dish: Modeling development and disease using organoid technologies
Lancaster, M. A., & Knoblich, J. A. (2014) · Science · doi:10.1126/science.1247125 · Cited by 2,931 · see citing works
Self-citationProspective Derivation of a Living Organoid Biobank of Colorectal Cancer Patients
van de Wetering, M., Francies, H. E., Francis, J. M., Bounova, G., Iorio, F., Pronk, A., van Houdt, W., van Gorp, J., Taylor-Weiner, A., Kester, L., et al. (2015) · Cell · doi:10.1016/j.cell.2015.03.053 · Cited by 2,408 · see citing works
Self-citationOrganoid models of human and mouse ductal pancreatic cancer
Boj, S. F., Hwang, C.-I., Baker, L. A., Chio, I. I. C., Engle, D. D., Corbo, V., Jager, M., Ponz-Sarvise, M., Tiriac, H., Spector, M. S., et al. (2015) · Cell · doi:10.1016/j.cell.2014.12.021 · Cited by 2,150 · see citing works
Self-citationBrain-Region-Specific Organoids Using Mini-bioreactors for Modeling ZIKV Exposure
Qian, X., Nguyen, H. N., Song, M. M., Hadiono, C., Ogden, S. C., Hammack, C., Yao, B., Hamersky, G. R., Jacob, F., Zhong, C., et al. (2016) · Cell · doi:10.1016/j.cell.2016.04.032 · Cited by 2,127 · see citing works
The Meaning of Translational Research and Why It Matters
Woolf, S. H. (2008) · JAMA · doi:10.1001/jama.2007.26 · Cited by 1,910 · see citing works
Long-Term Culture of Genome-Stable Bipotent Stem Cells from Adult Human Liver
Huch, M., Gehart, H., van Boxtel, R., Hamer, K., Blokzijl, F., Verstegen, M. M. A., Ellis, E., van Wenum, M., Fuchs, S. A., de Ligt, J., et al. (2015) · Cell · doi:10.1016/j.cell.2014.11.050 · Cited by 1,619 · see citing works
Self-citationOrganoids as an in vitro model of human development and disease
Fatehullah, A., Tan, S. H., & Barker, N. (2016) · Nature Cell Biology · doi:10.1038/ncb3312 · Cited by 1,508 · see citing works
Schwank, G., Koo, B.-K., Sasselli, V., Dekkers, J. F., Heo, I., Demircan, T., Sasaki, N., Boymans, S., Cuppen, E., van der Ent, C. K., et al. (2013) · Cell Stem Cell · doi:10.1016/j.stem.2013.11.002 · Cited by 1,424 · see citing works
Self-citationNeurogenic radial glia in the outer subventricular zone of human neocortex
Hansen, D. V., Lui, J. H., Parker, P. R. L., & Kriegstein, A. R. (2010) · Nature · doi:10.1038/nature08845 · Cited by 1,388 · see citing works
The Brazilian Zika virus strain causes birth defects in experimental models
Cugola, F. R., Fernandes, I. R., Russo, F. B., Freitas, B. C., Dias, J. L. M., Guimarães, K. P., Benazzato, C., Almeida, N., Pignatari, G. C., Romero, S., et al. (2016) · Nature · doi:10.1038/nature18296 · Cited by 1,326 · see citing works
Acetate mediates a microbiome–brain–β-cell axis to promote metabolic syndrome
Perry, R. J., Peng, L., Barry, N. A., Cline, G. W., Zhang, D., Cardone, R. L., Petersen, K. F., Kibbey, R. G., Goodman, A. L., & Shulman, G. I. (2016) · Nature · doi:10.1038/nature18309 · Cited by 1,299 · see citing works
Zika Virus Infects Human Cortical Neural Progenitors and Attenuates Their Growth
Tang, H., Hammack, C., Ogden, S. C., Wen, Z., Qian, X., Li, Y., Yao, B., Shin, J., Zhang, F., Lee, E. M., et al. (2016) · Cell Stem Cell · doi:10.1016/j.stem.2016.02.016 · Cited by 1,292 · see citing works
A functional CFTR assay using primary cystic fibrosis intestinal organoids
Dekkers, J. F., Wiegerinck, C. L., de Jonge, H. R., Bronsveld, I., Janssens, H. M., de Winter-de Groot, K. M., Brandsma, A. M., de Jong, N. W. M., Bijvelds, M. J. C., Scholte, B. J., et al. (2013) · Nature Medicine · doi:10.1038/nm.3201 · Cited by 999 · see citing works
Self-citationFunctional engraftment of colon epithelium expanded in vitro from a single adult Lgr5+ stem cell
Yui, S., Nakamura, T., Sato, T., Nemoto, Y., Mizutani, T., Zheng, X., Ichinose, S., Nagaishi, T., Okamoto, R., Tsuchiya, K., et al. (2012) · Nature Medicine · doi:10.1038/nm.2695 · Cited by 805 · see citing works
Self-citationDang, J., Tiwari, S. K., Lichinchi, G., Qin, Y., Patil, V. S., Eroshkin, A. M., & Rana, T. M. (2016) · Cell Stem Cell · doi:10.1016/j.stem.2016.04.014 · Cited by 731 · see citing works
Self-organization of the human embryo in the absence of maternal tissues
Shahbazi, M. N., Jędrusik, A., Vuoristo, S., Recher, G., Hupalowska, A., Bolton, V. N., Fogarty, N. M. E., Campbell, A., Devito, L., Ilić, D., et al. (2016) · Nature Cell Biology · doi:10.1038/ncb3347 · Cited by 695 · see citing works
Self-organization of the in vitro attached human embryo
Deglincerti, A., Croft, G. F., Pietila, L., Zernicka‐Goetz, M., Siggia, E. D., & Brivanlou, A. H. (2016) · Nature · doi:10.1038/nature17948 · Cited by 682 · see citing works
Dekkers, J. F., Berkers, G., Kruisselbrink, E., Vonk, A., de Jonge, H. R., Janssens, H. M., Bronsveld, I., van de Graaf, E. A., Nieuwenhuis, E. E. S., Houwen, R. H. J., et al. (2016) · Science Translational Medicine · doi:10.1126/scitranslmed.aad8278 · Cited by 548 · see citing works
Self-citationExpression Analysis Highlights AXL as a Candidate Zika Virus Entry Receptor in Neural Stem Cells
Nowakowski, T. J., Pollen, A. A., Di Lullo, E., Sandoval-Espinosa, C., Bershteyn, M., & Kriegstein, A. R. (2016) · Cell Stem Cell · doi:10.1016/j.stem.2016.03.012 · Cited by 529 · see citing works
Swierstra, T., & Rip, A. (2007) · NanoEthics · doi:10.1007/s11569-007-0005-8 · Cited by 361 · see citing works
Festing, S., & Wilkinson, R. (2007) · EMBO Reports · doi:10.1038/sj.embor.7400993 · Cited by 316 · see citing works
The Singapore Statement on Research Integrity
Resnik, D. B., & Shamoo, A. E. (2011) · Accountability in Research · doi:10.1080/08989621.2011.557296 · Cited by 315 · see citing works
Scientific literacy and the myth of the scientific method
(1992) · Choice Reviews Online · doi:10.5860/choice.30-0877 · Cited by 277 · see citing works
Animal Experiments in Biomedical Research: A Historical Perspective
Franco, N. (2013) · Animals · doi:10.3390/ani3010238 · Cited by 265 · see citing works
Organoid Models of Human Gastrointestinal Development and Disease
Dedhia, P. H., Bertaux‐Skeirik, N., Zavros, Y. L., & Spence, J. R. (2016) · Gastroenterology · doi:10.1053/j.gastro.2015.12.042 · Cited by 246 · see citing works
Embryology policy: Revisit the 14-day rule
Hyun, I., Wilkerson, A., & Johnston, J. (2016) · Nature · doi:10.1038/533169a · Cited by 212 · see citing works
Drug discovery through stem cell-based organoid models
Ranga, A., Gjorevski, N., & Lutolf, M. P. (2014) · Advanced Drug Delivery Reviews · doi:10.1016/j.addr.2014.02.006 · Cited by 195 · see citing works
Astashkina, A. I., & Grainger, D. W. (2014) · Advanced Drug Delivery Reviews · doi:10.1016/j.addr.2014.02.008 · Cited by 194 · see citing works
Successful therapies for Alzheimer’s disease: why so many in animal models and none in humans?
Franco, R., & Cedazo-Minguez, A. (2014) · Frontiers in Pharmacology · doi:10.3389/fphar.2014.00146 · Cited by 183 · see citing works
A proposed definition of regenerative medicine
Daar, A. S., & Greenwood, H. (2007) · Journal of Tissue Engineering and Regenerative Medicine · doi:10.1002/term.20 · Cited by 167 · see citing works
From consent to institutions: Designing adaptive governance for genomic biobanks
O’Doherty, K. C., Burgess, M., Edwards, K., Gallagher, R. P., Hawkins, A. K., Kaye, J. S., McCaffrey, V., & Winickoff, D. E. (2011) · Social Science & Medicine · doi:10.1016/j.socscimed.2011.05.046 · Cited by 156 · see citing works
Mostert, M., Bredenoord, A. L., Biesaart, M. C. I. H., & van Delden, J. J. M. (2016) · European Journal of Human Genetics · doi:10.1038/ejhg.2015.239 · Cited by 143 · see citing works
Self-citationBioengineering approaches to guide stem cell-based organogenesis
Gjorevski, N., Ranga, A., & Lutolf, M. P. (2014) · Development · doi:10.1242/dev.101048 · Cited by 137 · see citing works
Caulfield, T., Sipp, D., Murry, C. E., Daley, G. Q., & Kimmelman, J. (2016) · Science · doi:10.1126/science.aaf4620 · Cited by 134 · see citing works
Organoid biobanking: identifying the ethics
Boers, S. N., van Delden, J. J. M., Clevers, H. C., & Bredenoord, A. L. (2016) · EMBO Reports · doi:10.15252/embr.201642613 · Cited by 106 · see citing works
Self-citationSteinbock, B. (2011) · Oxford University Press eBooks · doi:10.1093/acprof:oso/9780195341621.001.0001 · Cited by 97 · see citing works
Hild, M., & Jaffe, A. B. (2016) · Current Protocols in Stem Cell Biology · doi:10.1002/cpsc.1 · Cited by 95 · see citing works
Marx, V. (2015) · Nature · doi:10.1038/522373a · Cited by 93 · see citing works
Organoids as Models for Neoplastic Transformation
Neal, J. T., & Kuo, C. J. (2016) · Annual Review of Pathology Mechanisms of Disease · doi:10.1146/annurev-pathol-012615-044249 · Cited by 85 · see citing works
Kuijk, E., Rasmussen, S. A., Blokzijl, F., Huch, M., Gehart, H., Toonen, P. W., Begthel, H., Clevers, H. C., Geurts, A. M., & Cuppen, E. P. J. G. (2016) · Scientific Reports · doi:10.1038/srep22154 · Cited by 56 · see citing works
Self-citationBredenoord, A. L., Pennings, G., Smeets, H. J. M., & de Wert, G. M. W. R. (2007) · Human Reproduction Update · doi:10.1093/humupd/dmm037 · Cited by 55 · see citing works
Self-citationInclusion of Residual Tissue in Biobanks: Opt-In or Opt-Out?
Giesbertz, N. A. A., Bredenoord, A. L., & van Delden, J. J. M. (2012) · PLoS Biology · doi:10.1371/journal.pbio.1001373 · Cited by 48 · see citing works
Self-citationBroad Consent Is Consent for Governance
Boers, S. N., van Delden, J. J. M., & Bredenoord, A. L. (2015) · The American Journal of Bioethics · doi:10.1080/15265161.2015.1062165 · Cited by 43 · see citing works
Self-citationEthics of mitochondrial gene replacement: from bench to bedside
Bredenoord, A. L., & Braude, P. (2010) · BMJ · doi:10.1136/bmj.c6021 · Cited by 42 · see citing works
Self-citationTaking the “Soft Impacts” of Technology into Account: Broadening the Discourse in Research Practice
van der Burg, S. (2009) · Social Epistemology · doi:10.1080/02691720903364191 · Cited by 38 · see citing works
Human stem cell-based disease modeling: prospects and challenges
Johnson, J. Z., & Hockemeyer, D. F. (2015) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2015.10.007 · Cited by 32 · see citing works
Stem Cell Trials for Cardiovascular Medicine: Ethical Rationale
Niemansburg, S. L., Teraa, M., Hesam, H., van Delden, J. J. M., Verhaar, M. C., & Bredenoord, A. L. (2013) · Tissue Engineering Part A · doi:10.1089/ten.tea.2013.0332 · Cited by 22 · see citing works
Self-citationEthics and Refinement in Animal Research
Olsson, I. A. S., Hansen, A. K., & Sandøe, P. (2007) · Science · doi:10.1126/science.317.5845.1680 · Cited by 21 · see citing works
The end of animal life: a start for ethical debate
Stassen, E. N., & Meijboom, F. L. B. (2015) · Wageningen Academic Publishers eBooks · doi:10.3920/978-90-8686-808-7 · Cited by 19 · see citing works
ETHICS, AMBIGUITY AVERSION, AND THE REVIEW OF COMPLEX TRANSLATIONAL CLINICAL TRIALS
Kimmelman, J. (2011) · Bioethics · doi:10.1111/j.1467-8519.2010.01856.x · Cited by 18 · see citing works
Societal Impacts of Regenerative Medicine: Reflections on The Views of Orthopedic Professionals
Niemansburg, S. L., Tempels, T., Dhert, W. J. A., van Delden, J. J. M., & Bredenoord, A. L. (2015) · Regenerative Medicine · doi:10.2217/rme.14.69 · Cited by 13 · see citing works
Self-citationNew company aims to broaden researchers' access to organoids
Chakradhar, S. (2016) · Nature Medicine · doi:10.1038/nm0416-338 · Cited by 11 · see citing works
Harms to animals - can we agree on how best to limit them?
Sandøe, P., Franco, N. H., Lund, T. B., Weary, D. M., & Olsson, I. A. S. (2015) · Research at the University of Copenhagen (University of Copenhagen) · Cited by 9 · see citing works
Mostert, M., Bredenoord, A. L., Biesaart, M. C. I. H., & van Delden, J. J. M. (2016) · European Journal of Human Genetics · doi:10.1038/ejhg.2016.71 · Cited by 8 · see citing works
Self-citationHabets, M. G. J. L., van Delden, J. J. M., Niemansburg, S. L., Atkins, H. L., & Bredenoord, A. L. (2016) · Molecular Therapy · doi:10.1038/mt.2016.202 · Cited by 6 · see citing works
Self-citationFDA should stand firm on stem-cell treatments
(2016) · Nature · doi:10.1038/535007b · Cited by 6 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Patient-derived organoids model treatment response of metastatic gastrointestinal cancers
Vlachogiannis, G., Hedayat, S., Vatsiou, A., Jamin, Y., Fernández-Mateos, J., Khan, K., Lampis, A., Eason, K., Huntingford, I., Burke, R., et al. (2018) · Science · doi:10.1126/science.aao2774 · Cited by 2,096 · see citing works
Zhao, Z., Chen, X., Dowbaj, A. M., Sljukic, A., Bratlie, K., Lin, L., Fong, E. L. S., Balachander, G. M., Chen, Z., Soragni, A., et al. (2022) · Nature Reviews Methods Primers · doi:10.1038/s43586-022-00174-y · Cited by 1,001 · see citing works
Cancer modeling meets human organoid technology
Tuveson, D., & Clevers, H. (2019) · Science · doi:10.1126/science.aaw6985 · Cited by 935 · see citing works
Self-citationThe role of adult hippocampal neurogenesis in brain health and disease
Toda, T., Parylak, S. L., Linker, S. B., & Gage, F. H. (2019) · Molecular Psychiatry · doi:10.1038/s41380-018-0036-2 · Cited by 719 · see citing works
Human Organoids: Tools for Understanding Biology and Treating Diseases
Schutgens, F., & Clevers, H. C. (2019) · Annual Review of Pathology Mechanisms of Disease · doi:10.1146/annurev-pathmechdis-012419-032611 · Cited by 506 · see citing works
Self-citationBiological responses to physicochemical properties of biomaterial surface
Rahmati, M., Silva, E. A., Reseland, J. E., Heyward, C. A., & Haugen, H. J. (2020) · Chemical Society Reviews · doi:10.1039/d0cs00103a · Cited by 403 · see citing works
Materials design by synthetic biology
Tang, T., An, B., Huang, Y., Vasikaran, S., Wang, Y., Jiang, X., Lu, T. K., & Zhong, C. (2020) · Nature Reviews Materials · doi:10.1038/s41578-020-00265-w · Cited by 403 · see citing works
Rethinking organoid technology through bioengineering
Garreta, E., Kamm, R. D., Lopes, S. M. C. D. S., Lancaster, M. A., Weiss, R., Trepat, X., Hyun, I., & Montserrat, N. (2020) · Nature Materials · doi:10.1038/s41563-020-00804-4 · Cited by 326 · see citing works
Building Models of Brain Disorders with Three-Dimensional Organoids
Amin, N. D., & Paşca, S. P. (2018) · Neuron · doi:10.1016/j.neuron.2018.10.007 · Cited by 312 · see citing works
Review: adult neurogenesis contributes to hippocampal plasticity
Toda, T., & Gage, F. H. (2017) · Cell and Tissue Research · doi:10.1007/s00441-017-2735-4 · Cited by 262 · see citing works
3D Spatiotemporal Mechanical Microenvironment: A Hydrogel‐Based Platform for Guiding Stem Cell Fate
Ma, Y., Lin, M., Huang, G., Li, Y., Wang, S., Bai, G., Lu, T. J., & Xu, F. (2018) · Advanced Materials · doi:10.1002/adma.201705911 · Cited by 230 · see citing works
Cerebral organoids: ethical issues and consciousness assessment
Lavazza, A., & Massimini, M. (2018) · Journal of Medical Ethics · doi:10.1136/medethics-2017-104555 · Cited by 217 · see citing works
Organ-on-a-Chip for Cancer and Immune Organs Modeling
Sun, W., Luo, Z., Lee, J., Kim, H., Lee, K., Tebon, P., Feng, Y., Dokmeci, M. R., Sengupta, S., & Khademhosseini, A. (2019) · Advanced Healthcare Materials · doi:10.1002/adhm.201801363 · Cited by 221 · see citing works
Clinical applications of human organoids
Verstegen, M. M. A., Coppes, R. P., Béghin, A., Coppi, P. D., Gerli, M., de Graeff, N., Pan, Q., Saito, Y., Shi, S., ZADPOOR, A. A., et al. (2025) · Nature Medicine · doi:10.1038/s41591-024-03489-3 · Cited by 228 · see citing works
Organoids: a systematic review of ethical issues
de Jongh, D., Massey, E. K., Berishvili, E., Fonseca, L. M., Lebreton, F., Bellofatto, K., Bignard, J., Seißler, J., Buerck, L. W.-V., Honarpisheh, M. M., et al. (2022) · Stem Cell Research & Therapy · doi:10.1186/s13287-022-02950-9 · Cited by 208 · see citing works
Reshaping the Tumor Stroma for Treatment of Pancreatic Cancer
Vennin, C., Murphy, K. J., Morton, J. P., Cox, T. R., Pajic, M., & Timpson, P. (2017) · Gastroenterology · doi:10.1053/j.gastro.2017.11.280 · Cited by 203 · see citing works
Engineering human islet organoids from iPSCs using an organ-on-chip platform
Tao, T., Wang, Y., Chen, W., Li, Z., Su, W., Guo, Y., Deng, P., & Qin, J. (2019) · Lab on a Chip · doi:10.1039/c8lc01298a · Cited by 198 · see citing works
High-Content Monitoring of Drug Effects in a 3D Spheroid Model
Mittler, F., Obeïd, P., Rulina, A. V., Haguet, V., Gidrol, X., & Balakirev, M. Y. (2017) · Frontiers in Oncology · doi:10.3389/fonc.2017.00293 · Cited by 197 · see citing works
Ethical issues related to brain organoid research
Hyun, I., Scharf-Deering, J. C., & Lunshof, J. E. (2020) · Brain Research · doi:10.1016/j.brainres.2020.146653 · Cited by 186 · see citing works
Modeling Neurological Diseases With Human Brain Organoids
Wang, H. (2018) · Frontiers in Synaptic Neuroscience · doi:10.3389/fnsyn.2018.00015 · Cited by 172 · see citing works
Moral Limits of Brain Organoid Research
Koplin, J. J., & Savulescu, J. (2019) · The Journal of Law Medicine & Ethics · doi:10.1177/1073110519897789 · Cited by 156 · see citing works
Ethical Considerations in Animal Research: The Principle of 3R’s
Dı́az, L., Zambrano, E., Flores, M. E., Contreras, M., Crispín, J. C., Alemán, G., Bravo, C., Armenta-Espinosa, A., Valdés, V. J., Tovar, A. R., et al. (2020) · Revista de investigaci�n Cl�nica · doi:10.24875/ric.20000380 · Cited by 150 · see citing works
Articular cartilage repair biomaterials: strategies and applications
Wang, M., Wu, Y., Li, G., Lin, Q., Zhang, W., Liu, H., & Su, J. (2024) · Materials Today Bio · doi:10.1016/j.mtbio.2024.100948 · Cited by 145 · see citing works
Kassis, T., Hernandez‐Gordillo, V., Langer, R., & Griffith, L. G. (2019) · Scientific Reports · doi:10.1038/s41598-019-48874-y · Cited by 141 · see citing works
Organoid based personalized medicine: from bench to bedside
Li, Y., Tang, P., Cai, S., Peng, J., & Hua, G. (2020) · Cell Regeneration · doi:10.1186/s13619-020-00059-z · Cited by 138 · see citing works
A framework for the investigation of rare genetic disorders in neuropsychiatry
Sanders, S., Şahin, M., Hostyk, J. A., Thurm, A. E., Jacquemont, S., Avillach, P., Douard, E. A., Martin, C. L., Modi, M. E., Moreno-De-Luca, A., et al. (2019) · Nature Medicine · doi:10.1038/s41591-019-0581-5 · Cited by 119 · see citing works
Organoid systems to study the human female reproductive tract and pregnancy
Alzamil, L., Νικολακοπούλου, Κ., & Turco, M. Y. (2020) · Cell Death and Differentiation · doi:10.1038/s41418-020-0565-5 · Cited by 121 · see citing works
Cancer research using organoid technology
Kretzschmar, K. (2021) · Journal of Molecular Medicine · doi:10.1007/s00109-020-01990-z · Cited by 120 · see citing works
Optic neuropathies: the tip of the neurodegeneration iceberg
Carelli, V., Morgia, C. L., Ross‐Cisneros, F. N., & Sadun, A. A. (2017) · Human Molecular Genetics · doi:10.1093/hmg/ddx273 · Cited by 114 · see citing works
Should the 14‐day rule for embryo research become the 28‐day rule?
Appleby, J., & Bredenoord, A. L. (2018) · EMBO Molecular Medicine · doi:10.15252/emmm.201809437 · Cited by 111 · see citing works
Self-citationThree‐Dimensional Models of the Human Brain Development and Diseases
Jorfi, M., D’Avanzo, C., Kim, D. Y., & Irimia, D. (2017) · Advanced Healthcare Materials · doi:10.1002/adhm.201700723 · Cited by 102 · see citing works
Guidance document on Good cell and tissue culture practice 2.0 (GCCP 2.0)
Pamies, D. (2021) · ALTEX · doi:10.14573/altex.2111011 · Cited by 100 · see citing works
Organoids as hybrids: ethical implications for the exchange of human tissues
Boers, S. N., van Delden, J. J. M., & Bredenoord, A. L. (2018) · Journal of Medical Ethics · doi:10.1136/medethics-2018-104846 · Cited by 99 · see citing works
Self-citationOrganoids of the female reproductive tract
Chumduri, C., & Turco, M. Y. (2021) · Journal of Molecular Medicine · doi:10.1007/s00109-020-02028-0 · Cited by 99 · see citing works
Modelling metabolic diseases and drug response using stem cells and organoids
Hu, W., & Lazar, M. A. (2022) · Nature Reviews Endocrinology · doi:10.1038/s41574-022-00733-z · Cited by 98 · see citing works
Foglietta, F., Canaparo, R., Muccioli, G., Terreno, E., & Serpe, L. (2020) · Life Sciences · doi:10.1016/j.lfs.2020.117784 · Cited by 95 · see citing works
Human cerebral organoids and consciousness: a double-edged sword
Lavazza, A. (2020) · Bioethics News · doi:10.1007/s40592-020-00116-y · Cited by 93 · see citing works
Clinical translation of patient-derived tumour organoids- bottlenecks and strategies
Foo, M. A., You, M., Chan, S. L., Sethi, G., Bonney, G. K., Yong, W. P., Chow, E. K., Fong, E. L. S., Wang, L., & Goh, B.-C. (2022) · Biomarker Research · doi:10.1186/s40364-022-00356-6 · Cited by 94 · see citing works
Topraggaleh, T. R., Valojerdi, M. R., Montazeri, L., & Baharvand, H. (2019) · Biomaterials Science · doi:10.1039/c8bm01001c · Cited by 91 · see citing works
Regeneration of pulpo-dentinal–like complex by a group of unique multipotent CD24a + stem cells
Chen, H., Fu, H., Wu, X. S., Duan, Y., Zhang, S., Hu, H., Liao, Y., Wang, T., Yang, Y., Chen, G., et al. (2020) · Science Advances · doi:10.1126/sciadv.aay1514 · Cited by 91 · see citing works
Zheng, F., Xiao, Y., Liu, H., Fan, Y., & Dao, M. (2021) · Advanced Biology · doi:10.1002/adbi.202000024 · Cited by 92 · see citing works
A deep learning model for detection and tracking in high-throughput images of organoid
Bian, X., Li, G., Wang, C., Liu, W., Lin, X., Chen, Z., Cheung, M., & Luo, X. (2021) · Computers in Biology and Medicine · doi:10.1016/j.compbiomed.2021.104490 · Cited by 92 · see citing works
Organoids: An intermediate modeling platform in precision oncology
Jin, M., Han, R.-R., Qiu, G., Ju, X.-C., Lou, G., & Jin, W. (2017) · Cancer Letters · doi:10.1016/j.canlet.2017.11.021 · Cited by 88 · see citing works
Sun, G., Li, Z., Wang, W., Chen, Z., Zhang, L., Li, Q., Wei, S., Li, B., Xu, J., Chen, L., et al. (2017) · Journal of Gastroenterology · doi:10.1007/s00535-017-1408-0 · Cited by 85 · see citing works
Cardiac organoid — a promising perspective of preclinical model
Zhao, D., Lei, W., & Hu, S. (2021) · Stem Cell Research & Therapy · doi:10.1186/s13287-021-02340-7 · Cited by 82 · see citing works
Development of Collagen-Based 3D Matrix for Gastrointestinal Tract-Derived Organoid Culture
Jee, J. H., Lee, D. H., Ko, J., Hahn, S., Jeong, S. Y., Kim, H. K., Park, E., Choi, S. Y., Jeong, S., Lee, J. W., et al. (2019) · Stem Cells International · doi:10.1155/2019/8472712 · Cited by 80 · see citing works
A Method for Cryogenic Preservation of Human Biopsy Specimens and Subsequent Organoid Culture
Tsai, Y.-H., Czerwinski, M. J., Wu, A., Dame, M. K., Attili, D., Hill, E. M., Colacino, J. A., Nowacki, L. M., Shroyer, N. F., Higgins, P., et al. (2018) · Cellular and Molecular Gastroenterology and Hepatology · doi:10.1016/j.jcmgh.2018.04.008 · Cited by 80 · see citing works
Multimodal Single-Cell Analysis Reveals Physiological Maturation in the Developing Human Neocortex
Mayer, S., Chen, J., Velmeshev, D., Mayer, A., Eze, U. C., Bhaduri, A., da Cunha, C. E., Jung, D., Arjun, A., Li, E., et al. (2019) · Neuron · doi:10.1016/j.neuron.2019.01.027 · Cited by 81 · see citing works
One-step synthesis of composite hydrogel capsules to support liver organoid generation from hiPSCs
Wang, Y., Liu, H., Zhang, M., Wang, H., Chen, W., & Qin, J. (2020) · Biomaterials Science · doi:10.1039/d0bm01085e · Cited by 78 · see citing works
Reyes-Furrer, A. A., Andrade, S. D., Bachmann, D., Jeker, H., Steinmann, M., Accart, N., Dunbar, A., Rausch, M., Bono, E., Rimann, M., et al. (2021) · Communications Biology · doi:10.1038/s42003-021-02691-0 · Cited by 80 · see citing works
Limitations of human brain organoids to study neurodegenerative diseases: a manual to survive
Urrestizala-Arenaza, N., Cerchio, S., Cavaliere, F., & Magliaro, C. (2024) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2024.1419526 · Cited by 80 · see citing works
Organoid technology for tissue engineering
He, J., Zhang, X., Xia, X., Han, M., Li, F., Li, C., Li, Y., & Gao, D. (2020) · Journal of Molecular Cell Biology · doi:10.1093/jmcb/mjaa012 · Cited by 77 · see citing works
Zhang, J., Griesbach, J. K., Ganeyev, M., Zehnder, A., Zeng, P., Schädli, G. N., de Leeuw, A. M., Lai, Y., Rubert, M., & Müller, R. (2022) · Biofabrication · doi:10.1088/1758-5090/ac73b9 · Cited by 77 · see citing works
Consent for governance in the ethical use of organoids
Boers, S. N., & Bredenoord, A. L. (2018) · Nature Cell Biology · doi:10.1038/s41556-018-0112-5 · Cited by 77 · see citing works
Self-citationBiomimicry, Biofabrication, and Biohybrid Systems: The Emergence and Evolution of Biological Design
Raman, R., & Bashir, R. (2017) · Advanced Healthcare Materials · doi:10.1002/adhm.201700496 · Cited by 74 · see citing works
Strategies for genetic manipulation of adult stem cell-derived organoids
Menche, C., & Farin, H. F. (2021) · Experimental & Molecular Medicine · doi:10.1038/s12276-021-00609-8 · Cited by 70 · see citing works
Organoid Technology: Current Standing and Future Perspectives
Shariati, L., Esmaeili, Y., Javanmard, S. H., Bidram, E., & Amini, A. (2021) · Stem Cells · doi:10.1002/stem.3379 · Cited by 69 · see citing works
Ethics parallel research: an approach for (early) ethical guidance of biomedical innovation
Jongsma, K. R., & Bredenoord, A. L. (2020) · BMC Medical Ethics · doi:10.1186/s12910-020-00524-z · Cited by 68 · see citing works
Self-citationHuman Organoids for the Study of Retinal Development and Disease
Bell, C. M., Zack, D. J., & Berlinicke, C. A. (2020) · Annual Review of Vision Science · doi:10.1146/annurev-vision-121219-081855 · Cited by 63 · see citing works
Lavazza, A. (2020) · Brain Research · doi:10.1016/j.brainres.2020.147146 · Cited by 62 · see citing works
Breeding Brains? Patients’ and Laymen’s Perspectives on Cerebral Organoids
Haselager, D. R., Boers, S. N., Jongsma, K. R., Vinkers, C. H., Broekman, M. L. D., & Bredenoord, A. L. (2020) · Regenerative Medicine · doi:10.2217/rme-2020-0108 · Cited by 61 · see citing works
Self-citationTumor organoids: From inception to future in cancer research
Yang, L., Yang, S., Li, X., Li, B., Li, Y., Zhang, X., Ma, Y., Peng, X., Jin, H., Fan, Q., et al. (2019) · Cancer Letters · doi:10.1016/j.canlet.2019.04.005 · Cited by 60 · see citing works
Hu, X., Xia, Z., & Cai, K. (2022) · Journal of Materials Chemistry B · doi:10.1039/d1tb02537f · Cited by 57 · see citing works
Biohybrid robotics: From the nanoscale to the macroscale
Mestre, R., Patiño, T., & Sánchez, S. (2021) · Wiley Interdisciplinary Reviews Nanomedicine and Nanobiotechnology · doi:10.1002/wnan.1703 · Cited by 56 · see citing works
Ommen, D. D. Z.-V., de Poel, E., Kruisselbrink, E., Oppelaar, H., Vonk, A. M., Janssens, H. M., van der Ent, C. K., Hagemeijer, M. C., & Beekman, J. M. (2018) · Journal of Cystic Fibrosis · doi:10.1016/j.jcf.2018.02.007 · Cited by 55 · see citing works
Automated Design of Pluripotent Stem Cell Self-Organization
Libby, A. R. G., Briers, D., Haghighi, I., Joy, D. A., Conklin, B. R., Belta, C. A., & McDevitt, T. C. (2019) · Cell Systems · doi:10.1016/j.cels.2019.10.008 · Cited by 59 · see citing works
Robust detection of undifferentiated iPSC among differentiated cells
Sekine, K., Tsuzuki, S., Yasui, R., Kobayashi, T., Ikeda, K., Hamada, Y., Kanai, E., Camp, J. G., Treutlein, B., Ueno, Y., et al. (2020) · Scientific Reports · doi:10.1038/s41598-020-66845-6 · Cited by 53 · see citing works
Granat, L. M., Kambhampati, O., Klosek, S., Niedzwecki, B., Parsa, K., & Zhang, D. (2019) · Animal Models and Experimental Medicine · doi:10.1002/ame2.12077 · Cited by 56 · see citing works
Modeling of Hypoxic Brain Injury through 3D Human Neural Organoids
Kim, M. S., Kim, D., Kang, H. K., Kook, M. G., Choi, S. W., & Kang, K. (2021) · Cells · doi:10.3390/cells10020234 · Cited by 55 · see citing works
The moral status of cerebral organoids
Hostiuc, S., Rusu, M. C., Negoi, I., Perlea, P., Dorobanţu, B., & Drima, E. P. (2019) · Regenerative Therapy · doi:10.1016/j.reth.2019.02.003 · Cited by 54 · see citing works
Engineering human hepato-biliary-pancreatic organoids from pluripotent stem cells
Koike, H., Iwasawa, K., Ouchi, R., Maezawa, M., Kimura, M., Kodaka, A., Nishii, S., Thompson, W. L., & Takebe, T. (2021) · Nature Protocols · doi:10.1038/s41596-020-00441-w · Cited by 55 · see citing works
Al‐Lamki, R. S., Bradley, J. R., & Pober, J. S. (2017) · Frontiers in Medicine · doi:10.3389/fmed.2017.00148 · Cited by 53 · see citing works
Cao, W., Liu, J., Wang, L., Li, M., Verstegen, M. M. A., Yin, Y., Ma, B., Chen, K., Bolkestein, M., Sprengers, D., et al. (2018) · Carcinogenesis · doi:10.1093/carcin/bgy129 · Cited by 50 · see citing works
Nguyen, R., Bae, S. D. W., Qiao, L., & George, J. (2021) · Cancer Letters · doi:10.1016/j.canlet.2021.03.017 · Cited by 50 · see citing works
Feng, J., Lu, H. J., Ma, W., Tian, W., Lu, Z., Yang, H., Cai, Y., Cai, P., Sun, Y., Zhou, Z., et al. (2022) · Protein & Cell · doi:10.1007/s13238-022-00906-6 · Cited by 49 · see citing works
Hu, Y., Zhu, T., Cui, H., & Cui, H. (2024) · Advanced Healthcare Materials · doi:10.1002/adhm.202403762 · Cited by 49 · see citing works
Kim, E. M., Lee, Y. B., Kim, S., Park, J., Lee, J., Kim, S. W., Park, H., & Shin, H. (2019) · Acta Biomaterialia · doi:10.1016/j.actbio.2019.09.028 · Cited by 49 · see citing works
Gołąbek-Grenda, A., & Olejnik, A. M. (2022) · Cellular Signalling · doi:10.1016/j.cellsig.2022.110375 · Cited by 48 · see citing works
Pichl, A., Ranisch, R., ALTINOK, O. A., Antonakaki, M., Barnhart, A. J., Bassil, K. C., Boyd, J. L., Chinaia, A. A., Diner, S., Gaillard, M., et al. (2023) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2023.1194706 · Cited by 48 · see citing works
Commercialization of Organoids
Choudhury, D., Ashok, A., & Naing, M. W. (2020) · Trends in Molecular Medicine · doi:10.1016/j.molmed.2019.12.002 · Cited by 48 · see citing works
Biobanking of human gut organoids for translational research
Perrone, F. M., & Zilbauer, M. (2021) · Experimental & Molecular Medicine · doi:10.1038/s12276-021-00606-x · Cited by 50 · see citing works
The technology, opportunities, and challenges of Synthetic Biological Intelligence
Kagan, B. J., Gyngell, C., Lysaght, T., Cole, V. M., Sawai, T., & Savulescu, J. (2023) · Biotechnology Advances · doi:10.1016/j.biotechadv.2023.108233 · Cited by 48 · see citing works
Immune Curbing of Cancer Stem Cells by CTLs Directed to NANOG
Wefers, C., Schreibelt, G., Massuger, L. F. A. G., de Vries, I. J. M., & Torensma, R. (2018) · Frontiers in Immunology · doi:10.3389/fimmu.2018.01412 · Cited by 46 · see citing works
Organoids as Innovative Models for Bone and Joint Diseases
Huang, J., Zhang, L., Lü, A., & Liang, C. (2023) · Cells · doi:10.3390/cells12121590 · Cited by 47 · see citing works
Boers, S. N., Groot, K. M. D. W., Noordhoek, J. J., Gulmans, V. A. M., van der Ent, C. K., van Delden, J. J. M., & Bredenoord, A. L. (2018) · Journal of Cystic Fibrosis · doi:10.1016/j.jcf.2018.02.004 · Cited by 45 · see citing works
Self-citationLensink, M. A., Boers, S. N., Jongsma, K. R., Carter, S. E., van der Ent, C. K., & Bredenoord, A. L. (2020) · Journal of Cystic Fibrosis · doi:10.1016/j.jcf.2020.11.015 · Cited by 46 · see citing works
Self-citationRecognizing the ethical implications of stem cell research: A call for broadening the scope
Assen, L., Jongsma, K. R., Isasi, R. M., Tryfonidou, M. A., & Bredenoord, A. L. (2021) · Stem Cell Reports · doi:10.1016/j.stemcr.2021.05.021 · Cited by 44 · see citing works
Self-citationModeling rare diseases with induced pluripotent stem cell technology
Anderson, R. H., & Francis, K. R. (2018) · Molecular and Cellular Probes · doi:10.1016/j.mcp.2018.01.001 · Cited by 43 · see citing works
Mandl, M., Viertler, H. P., Hatzmann, F. M., Brucker, C., Großmann, S., Waldegger, P., Rauchenwald, T., Mattesich, M., Zwierzina, M., Pierer, G., et al. (2022) · Adipocyte · doi:10.1080/21623945.2022.2044601 · Cited by 42 · see citing works
A new era of stem cell and developmental biology: from blastoids to synthetic embryos and beyond
Kim, Y., Kim, I. S., & Shin, K. (2023) · Experimental & Molecular Medicine · doi:10.1038/s12276-023-01097-8 · Cited by 44 · see citing works
Media portrayal of ethical and social issues in brain organoid research
Presley, A., Samsa, L. A., & Dubljević, V. (2022) · Philosophy Ethics and Humanities in Medicine · doi:10.1186/s13010-022-00119-z · Cited by 41 · see citing works
Castilla‐Casadiego, D. A., Reyes-Ramos, A. M., Domenech, M., & Almodóvar, J. (2019) · Annals of Biomedical Engineering · doi:10.1007/s10439-019-02400-3 · Cited by 41 · see citing works
Ren, W., Wang, L., Zhang, X., Feng, X., Zhuang, L., Jiang, N., Xu, R. C., Li, X., Wang, P., Sun, X., et al. (2020) · Theranostics · doi:10.7150/thno.46750 · Cited by 39 · see citing works
Bassil, K. C., & Horstkötter, D. (2023) · Cambridge Quarterly of Healthcare Ethics · doi:10.1017/s0963180123000038 · Cited by 37 · see citing works
Rallabandi, H. R., Yang, H., Oh, K. B., Lee, H.-C., Byun, S. J., & Lee, B. R. (2020) · Tissue Engineering and Regenerative Medicine · doi:10.1007/s13770-020-00278-0 · Cited by 38 · see citing works
Wang, G., Wen, B., Ren, X., Li, E., Zhang, Y., Guo, M., Xu, Y. J., Whitsett, J. A., Kalin, T. V., & Kalinichenko, V. V. (2021) · American Journal of Respiratory and Critical Care Medicine · doi:10.1164/rccm.202003-0758oc · Cited by 38 · see citing works
Engineering Ethics and Self-Organizing Models of Human Development: Opportunities and Challenges
Hyun, I. (2017) · Cell stem cell · doi:10.1016/j.stem.2017.09.002 · Cited by 38 · see citing works
Organ Transplantation in Iran; Current State and Challenges with a View on Ethical Consideration
Kiani, M., Abbasi, M., Ahmadi, M., & Salehi, B. (2018) · Journal of Clinical Medicine · doi:10.3390/jcm7030045 · Cited by 35 · see citing works
If Human Brain Organoids Are the Answer to Understanding Dementia, What Are the Questions?
Ooi, L., Dottori, M., Cook, A. L., Engel, M., Gautam, V., Grubman, A., Hernández, D., King, A. E., Maksour, S., Anastacio, H. T. D., et al. (2020) · The Neuroscientist · doi:10.1177/1073858420912404 · Cited by 34 · see citing works
Hypes and Hopes of Stem Cell Therapies in Dentistry: a Review
y Baena, A. R., Casasco, A., & Monti, M. (2022) · Stem Cell Reviews and Reports · doi:10.1007/s12015-021-10326-4 · Cited by 36 · see citing works
- Authors
- Bredenoord, A. L., Clevers, H., & Knoblich, J. A.
- Affiliations
- University Medical Center Utrecht (NL)
- Royal Netherlands Academy of Arts and Sciences (NL)
- Institute of Molecular Biotechnology (AT)
- Corresponding author
- Knoblich, Juergen A.
- Venue
- Science
- Published
- 2017-01-20
- Volume
- 355
- Issue
- 6322
- ISSN
- 0036-8075 (ISSN-L)
- 1095-9203
- OpenAlex
- W2576832945
- Cited by
- 334
- References
- 58
- Citations by year
- 2026: 25 · 2025: 39 · 2024: 40 · 2023: 32 · 2022: 38 · 2021: 37 · 2020: 44 · 2019: 31 · 2018: 30 · 2017: 18
- FWCI
- 4.13
- Type
- journal article
- Language
- en
- Open access
- green
- dspace.library.uu.nl
- Locations
- Science (publishedVersion)
- PubMed (publishedVersion)
- Data Archiving and Networked Services (DANS) (submittedVersion)
- Utrecht University Repository (Utrecht University) (submittedVersion, other-oa)
- KNAW research portal (Royal Academy of Art and Sciences (KNAW)) (submittedVersion)
- Utrecht University Repository (Utrecht University) (submittedVersion)
- Funders
- The Netherlands Organization for Health Research and Development (731010020)
- Austrian Academy of Sciences
- Austrian Science Fund (I_1281-B19, Z_153_B09)
- European Research Council
- Topics
- Health Sciences › Medicine › Physiology › Biomedical Ethics and Regulation
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Pluripotent Stem Cells Research
- Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Ethics and bioethics in healthcare
- Keywords
- organoids, stem cells, research ethics, alternatives to animal testing, precision medicine, organoid transplantation, gene therapy
- MeSH terms
- Gene Editing, Animals, Humans, Organoids, Animal Experimentation, Embryo Research, Fetal Research, Tissue Culture Techniques, Precision Medicine, Stem Cell Research
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
