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  • Review Article
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Ultrasound-assisted tissue engineering

Nature Reviews Bioengineering (2024)Cite this article

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Abstract

Combining cells, biomaterials and bioactive factors with biophysical cues to engineer cell and tissue constructs can address various applications, such as regenerative and personalized medicine, in addition to drug discovery and testing. However, challenges associated with the assembly of large, complex tissues integrating multiple cell types and functions require established technologies such as 3D printing to be combined with cell-assembly and cell-stimulation methods. Ultrasound is a potential tool for advancing tissue engineering, conferring the advantages of cytocompatibility and deep tissue penetration. In this Review, we discuss the application of ultrasound to the remote manipulation and assembly of biological building blocks, as well as the direct and indirect triggering of cellular processes, in combination with ultrasound-sensitive additives. Furthermore, we examine the role of ultrasound in tissue maturation, and in affecting the microenvironment and cell programming. Finally, we outline the challenges facing the technology and considerations for the widespread use of ultrasound in tissue engineering.

Key points

  • Ultrasound is a versatile and biocompatible method to remotely apply forces and transfer energy, with diverse potential applications in tissue engineering.

  • Parallel and rapid assembly of cells can be achieved by using ultrasound techniques in standalone setups or in combination with bioprinting to yield multilayer constructs with high local cell density.

  • Ultrasound can spatiotemporally alter the biochemical and biomechanical properties of scaffold materials to influence the fate of engineered cells and tissues.

  • Ultrasound can couple to cellular and molecular processes, manipulating cell behaviour and tissue morphogenesis.

  • Ultrasound methodologies will benefit from standardized protocols and instruments to allow widespread adoption in the tissue-engineering community.

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Fig. 1: Using sound waves within fabrication and maturation of biological tissues.
Fig. 2: Shaping of ultrasound fields and their use for directed assembly.
Fig. 3: Ultrasound for cell maturation and reprogramming.

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References

  1. Berthiaume, F., Maguire, T. J. & Yarmush, M. L. Tissue engineering and regenerative medicine: history, progress, and challenges. Annu. Rev. Chem. Biomol. Eng. 2, 403–430 (2011).

    Article  Google Scholar 

  2. Hoffman, T., Khademhosseini, A. & Langer, R. Chasing the paradigm: clinical translation of 25 years of tissue engineering. Tissue Eng. Part A 25, 679–687 (2019).

    Article  Google Scholar 

  3. Kim, Y. S., Smoak, M. M., Melchiorri, A. J. & Mikos, A. G. An overview of the tissue engineering market in the United States from 2011 to 2018. Tissue Eng. A 25, 1–8 (2019).

    Article  Google Scholar 

  4. Lancaster, M. A. & Knoblich, J. A. Organogenesis in a dish: modeling development and disease using organoid technologies. Science 345, 1247125 (2014).

    Article  Google Scholar 

  5. Loewa, A., Feng, J. J. & Hedtrich, S. Human disease models in drug development. Nat. Rev. Bioeng. https://doi.org/10.1038/s44222-023-00063-3 (2023).

  6. Langhans, S. A. Three-dimensional in vitro cell culture models in drug discovery and drug repositioning. Front. Pharmacol. 9, 6 (2018).

    Article  Google Scholar 

  7. Pampaloni, F. & Stelzer, E. H. Three-dimensional cell cultures in toxicology. Biotechnol. Genet. Eng. Rev. 26, 117–138 (2009).

    Article  Google Scholar 

  8. Nuwer, R. US agency seeks to phase out animal testing. Nature https://doi.org/10.1038/d41586-022-03569-9 (2022).

  9. Moysidou, C. M., Barberio, C. & Owens, R. M. Advances in engineering human tissue models. Front. Bioeng. Biotechnol. 8, 620962 (2020).

    Article  Google Scholar 

  10. Nichol, J. W. & Khademhosseini, A. Modular tissue engineering: engineering biological tissues from the bottom up. Soft Matter 5, 1312–1319 (2009).

    Article  Google Scholar 

  11. Blatchley, M. R. & Anseth, K. S. Middle-out methods for spatiotemporal tissue engineering of organoids. Nat. Rev. Bioeng. 1, 329–345 (2023).

    Article  Google Scholar 

  12. Cho, S., Discher, D. E., Leong, K. W., Vunjak-Novakovic, G. & Wu, J. C. Challenges and opportunities for the next generation of cardiovascular tissue engineering. Nat. Methods 19, 1064–1071 (2022).

    Article  Google Scholar 

  13. Agarwal, T., Subramanian, B. & Maiti, T. K. Liver tissue engineering: challenges and opportunities. ACS Biomater. Sci. Eng. 5, 4167–4182 (2019).

    Article  Google Scholar 

  14. Takebe, T. & Wells, J. M. Organoids by design. Science 364, 956–959 (2019).

    Article  Google Scholar 

  15. Matejčić, M. & Trepat, X. Mechanobiological approaches to synthetic morphogenesis: learning by building. Trends Cell Biol. 33, 95–111 (2023).

    Article  Google Scholar 

  16. Rademakers, T., Horvath, J. M., Blitterswijk, C. A. & LaPointe, V. L. S. Oxygen and nutrient delivery in tissue engineering: approaches to graft vascularization. J. Tissue Eng. Regen. Med. 13, 1815–1829 (2019).

    Article  Google Scholar 

  17. Auger, F. A., Gibot, L. & Lacroix, D. The pivotal role of vascularization in tissue engineering. Annu. Rev. Biomed. Eng. 15, 177–200 (2013).

    Article  Google Scholar 

  18. Armstrong, J. P. K. & Stevens, M. M. Using remote fields for complex tissue engineering. Trends Biotechnol. 38, 254–263 (2020).

    Article  Google Scholar 

  19. Dholakia, K., Drinkwater, B. W. & Ritsch-Marte, M. Comparing acoustic and optical forces for biomedical research. Nat. Rev. Phys. 2, 480–491 (2020).

    Article  Google Scholar 

  20. Primo, G. A. & Mata, A. 3D patterning within hydrogels for the recreation of functional biological environments. Adv. Funct. Mater. 31, 2009574 (2021).

    Article  Google Scholar 

  21. Ouyang, L. L., Armstrong, J. P. K., Salmeron-Sanchez, M. & Stevens, M. M. Assembling living building blocks to engineer complex tissues. Adv. Funct. Mater. 30, 1909009 (2020).

    Article  Google Scholar 

  22. Rufo, J., Cai, F., Friend, J., Wiklund, M. & Huang, T. J. Acoustofluidics for biomedical applications. Nat. Rev. Methods Primers 2, 30 (2022).

    Article  Google Scholar 

  23. Armstrong, J. P. K. et al. Engineering anisotropic muscle tissue using acoustic cell patterning. Adv. Mater. 30, 1802649 (2018).

    Article  Google Scholar 

  24. Deshmukh, D. V. et al. Continuous production of acoustically patterned cells within hydrogel fibers for musculoskeletal tissue engineering. Adv. Funct. Mater. 32, 2113038 (2022).

    Article  Google Scholar 

  25. Armstrong, J. P. K. et al. Tissue engineering cartilage with deep zone cytoarchitecture by high-resolution acoustic cell patterning. Adv. Healthc. Mater. 11, 2200481 (2022).

    Article  Google Scholar 

  26. Chen, P., Guven, S., Usta, O. B., Yarmush, M. L. & Demirci, U. Biotunable acoustic node assembly of organoids. Adv. Healthc. Mater. 4, 1937–1943 (2015).

    Article  Google Scholar 

  27. Cai, H. et al. Intelligent acoustofluidics enabled mini-bioreactors for human brain organoids. Lab Chip 21, 2194–2205 (2021).

    Article  Google Scholar 

  28. Gong, Z. et al. Acoustic droplet printing tumor organoids for modeling bladder tumor immune microenvironment within a week. Adv. Healthc. Mater. 10, 2101312 (2021).

    Article  Google Scholar 

  29. Friend, J. Acoustofluidics. Front. Acoust. 1, 1261027 (2023).

    Article  Google Scholar 

  30. Melde, K., Mark, A. G., Qiu, T. & Fischer, P. Holograms for acoustics. Nature 537, 518–522 (2016).

    Article  Google Scholar 

  31. Ma, Z. et al. Acoustic holographic cell patterning in a biocompatible hydrogel. Adv. Mater. 32, 1904181 (2020).

    Article  Google Scholar 

  32. Gu, Y. et al. Acoustofluidic holography for micro- to nanoscale particle manipulation. ACS Nano 14, 14635–14645 (2020).

    Article  Google Scholar 

  33. Jain, P., Kathuria, H. & Dubey, N. Advances in 3D bioprinting of tissues/organs for regenerative medicine and in-vitro models. Biomaterials 287, 121639 (2022).

    Article  Google Scholar 

  34. Tibbitt, M. W. & Anseth, K. S. Hydrogels as extracellular matrix mimics for 3D cell culture. Biotechnol. Bioeng. 103, 655–663 (2009).

    Article  Google Scholar 

  35. Brassard, J. A., Nikolaev, M., Hubscher, T., Hofer, M. & Lutolf, M. P. Recapitulating macro-scale tissue self-organization through organoid bioprinting. Nat. Mater. 20, 22–29 (2021).

    Article  Google Scholar 

  36. Gopinathan, J. & Noh, I. Recent trends in bioinks for 3D printing. Biomater. Res. 22, 11 (2018).

    Article  Google Scholar 

  37. Harley, W. S. et al. Advances in biofabrication techniques towards functional bioprinted heterogeneous engineered tissues: a comprehensive review. Bioprinting 23, 00147 (2021).

    Article  Google Scholar 

  38. Mohan, T. S., Datta, P., Nesaei, S., Ozbolat, V. & Ozbolat, I. T. 3D coaxial bioprinting: process mechanisms, bioinks and applications. Prog. Biomed. Eng. 4, 022003 (2022).

    Article  Google Scholar 

  39. Zhang, Y. S. et al. 3D extrusion bioprinting. Nat. Rev. Methods Primers 1, 75 (2021).

    Article  Google Scholar 

  40. Jentsch, S. et al. Multiscale 3D bioprinting by nozzle-free acoustic droplet ejection. Small Methods 5, e2000971 (2021).

    Article  Google Scholar 

  41. Fang, Y. et al. Rapid generation of multiplexed cell cocultures using acoustic droplet ejection followed by aqueous two-phase exclusion patterning. Tissue Eng. Part C 18, 647–657 (2012).

    Article  Google Scholar 

  42. Guillotin, B. & Guillemot, F. Cell patterning technologies for organotypic tissue fabrication. Trends Biotechnol. 29, 183–190 (2011).

    Article  Google Scholar 

  43. You, S. et al. High cell density and high-resolution 3D bioprinting for fabricating vascularized tissues. Sci. Adv. 9, eade7923 (2023).

    Article  Google Scholar 

  44. Bernal, P. N. et al. Volumetric bioprinting of complex living-tissue constructs within seconds. Adv. Mater. 31, 1904209 (2019).

    Article  Google Scholar 

  45. Ouyang, L. Pushing the rheological and mechanical boundaries of extrusion-based 3D bioprinting. Trends Biotechnol. 40, 891–902 (2022).

    Article  Google Scholar 

  46. Banerjee, D. et al. Strategies for 3D bioprinting of spheroids: a comprehensive review. Biomaterials 291, 121881 (2022).

    Article  Google Scholar 

  47. Xin, S. et al. Generalizing hydrogel microparticles into a new class of bioinks for extrusion bioprinting. Sci. Adv. 7, eabk3087 (2021).

    Article  Google Scholar 

  48. Ou, Y. et al. Bioprinting microporous functional living materials from protein-based core–shell microgels. Nat. Commun. 14, 322 (2023).

    Article  Google Scholar 

  49. Fennema, E., Rivron, N., Rouwkema, J., van Blitterswijk, C. & de Boer, J. Spheroid culture as a tool for creating 3D complex tissues. Trends Biotechnol. 31, 108–115 (2013).

    Article  Google Scholar 

  50. Safaee, S., Schock, M., Joyee, E. B., Pan, Y. & Chen, R. K. Field-assisted additive manufacturing of polymeric composites. Addit. Manuf. 51, 102642 (2022).

    Google Scholar 

  51. Chansoria, P. & Shirwaiker, R. 3D bioprinting of anisotropic engineered tissue constructs with ultrasonically induced cell patterning. Addit. Manuf. 32, 101042 (2020).

    Google Scholar 

  52. Sriphutkiat, Y., Kasetsirikul, S., Ketpun, D. & Zhou, Y. Cell alignment and accumulation using acoustic nozzle for bioprinting. Sci. Rep. 9, 17774 (2019).

    Article  Google Scholar 

  53. Shao, M. H., Cui, B., Zheng, T. F. & Wang, C. H. Ultrasonic manipulation of cells for alleviating the clogging of extrusion-based bioprinting nozzles. J. Phys. Conf. Ser. 1798, 012009 (2021).

    Article  Google Scholar 

  54. Chansoria, P., Narayanan, L. K., Schuchard, K. & Shirwaiker, R. Ultrasound-assisted biofabrication and bioprinting of preferentially aligned three-dimensional cellular constructs. Biofabrication 11, 035015 (2019).

    Article  Google Scholar 

  55. Guex, A. G., Di Marzio, N., Eglin, D., Alini, M. & Serra, T. The waves that make the pattern: a review on acoustic manipulation in biomedical research. Mater. Today Bio 10, 100110 (2021).

    Article  Google Scholar 

  56. Wiklund, M. Acoustofluidics 12: biocompatibility and cell viability in microfluidic acoustic resonators. Lab Chip 12, 2018–2028 (2012).

    Article  Google Scholar 

  57. Ayan, B. et al. Aspiration-assisted freeform bioprinting of prefabricated tissue spheroids in a yield-stress gel. Commun. Phys. 3, 183 (2020).

    Article  Google Scholar 

  58. Olofsson, K., Hammarström, B. & Wiklund, M. Ultrasonic based tissue modelling and engineering. Micromachines 9, 594 (2018).

    Article  Google Scholar 

  59. Athanassiadis, A. G. et al. Ultrasound-responsive systems as components for smart materials. Chem. Rev. 122, 5165–5208 (2022).

    Article  Google Scholar 

  60. Hartono, D. et al. On-chip measurements of cell compressibility via acoustic radiation. Lab Chip 11, 4072–4080 (2011).

    Article  Google Scholar 

  61. Olofsson, K., Hammarström, B. & Wiklund, M. Acoustic separation of living and dead cells using high density medium. Lab Chip 20, 1981–1990 (2020).

    Article  Google Scholar 

  62. Jeger-Madiot, N. et al. Controlling the force and the position of acoustic traps with a tunable acoustofluidic chip: application to spheroid manipulations. J. Acoust. Soc. Am. 151, 4165–4179 (2022).

    Article  Google Scholar 

  63. Olofsson, K. et al. Acoustic formation of multicellular tumor spheroids enabling on-chip functional and structural imaging. Lab Chip 18, 2466–2476 (2018).

    Article  Google Scholar 

  64. Christakou, A. E., Ohlin, M., Onfelt, B. & Wiklund, M. Ultrasonic three-dimensional on-chip cell culture for dynamic studies of tumor immune surveillance by natural killer cells. Lab Chip 15, 3222–3231 (2015).

    Article  Google Scholar 

  65. Olofsson, K., Carannante, V., Takai, M., Onfelt, B. & Wiklund, M. Ultrasound-based scaffold-free core–shell multicellular tumor spheroid formation. Micromachines 12, 329 (2021).

    Article  Google Scholar 

  66. Bouyer, C. et al. A bio-acoustic levitational (BAL) assembly method for engineering of multilayered, 3D brain-like constructs, using human embryonic stem cell derived neuro-progenitors. Adv. Mater. 28, 161–167 (2016).

    Article  Google Scholar 

  67. Comeau, E. S., Hocking, D. C. & Dalecki, D. Ultrasound patterning technologies for studying vascular morphogenesis in 3D. J. Cell Sci. 130, 232–242 (2017).

    Google Scholar 

  68. Kang, B. et al. High-resolution acoustophoretic 3D cell patterning to construct functional collateral cylindroids for ischemia therapy. Nat. Commun. 9, 5402 (2018).

    Article  Google Scholar 

  69. Comeau, E. S. et al. In vivo acoustic patterning of endothelial cells for tissue vascularization. Sci. Rep. 13, 16082 (2023).

    Article  Google Scholar 

  70. Baudoin, M. & Thomas, J. L. Acoustic tweezers for particle and fluid micromanipulation. Annu. Rev. Fluid Mech. 52, 205–234 (2019).

    Article  MathSciNet  Google Scholar 

  71. Chen, K. et al. Rapid formation of size-controllable multicellular spheroids via 3D acoustic tweezers. Lab Chip 16, 2636–2643 (2016).

    Article  Google Scholar 

  72. Guo, F. et al. Three-dimensional manipulation of single cells using surface acoustic waves. Proc. Natl Acad. Sci. USA 113, 1522–1527 (2016).

    Article  Google Scholar 

  73. Cai, H. et al. Trapping cell spheroids and organoids using digital acoustofluidics. Biofabrication 12, 035025 (2020).

    Article  Google Scholar 

  74. Gao, Z. et al. A multifunctional acoustic tweezer for heterogenous assembloids patterning. Small Struct. 4, 2200288 (2023).

    Article  Google Scholar 

  75. Baudoin, M. et al. Spatially selective manipulation of cells with single-beam acoustical tweezers. Nat. Commun. 11, 4244 (2020).

    Article  Google Scholar 

  76. Cox, L., Croxford, A. & Drinkwater, B. W. Dynamic patterning of microparticles with acoustic impulse control. Sci. Rep. 12, 14549 (2022).

    Article  Google Scholar 

  77. Cox, L., Melde, K., Croxford, A., Fischer, P. & Drinkwater, B. W. Acoustic hologram enhanced phased arrays for ultrasonic particle manipulation. Phys. Rev. Appl. 12, 064055 (2019).

    Article  Google Scholar 

  78. Ma, Z. et al. Spatial ultrasound modulation by digitally controlling microbubble arrays. Nat. Commun. 11, 4537 (2020).

    Article  Google Scholar 

  79. Melde, K. et al. Compact holographic sound fields enable rapid one-step assembly of matter in 3D. Sci. Adv. 9, eadf6182 (2023).

    Article  Google Scholar 

  80. Athanassiadis, A. G. et al. Multiplane diffractive acoustic networks. IEEE Trans. Ultrason. Ferroelect. Freq. Contr. 70, 441–448 (2023).

    Article  Google Scholar 

  81. Chen, P. et al. Microscale assembly directed by liquid-based template. Adv. Mater. 26, 5936–5941 (2014).

    Article  Google Scholar 

  82. Ren, T., Chen, P., Gu, L., Ogut, M. G. & Demirci, U. Soft ring-shaped cellu-robots with simultaneous locomotion in batches. Adv. Mater. 32, 1905713 (2020).

    Article  Google Scholar 

  83. Wang, J. et al. Acoustic fabrication of living cardiomyocyte-based hybrid biorobots. ACS Nano 16, 10219–10230 (2022).

    Article  Google Scholar 

  84. Serpooshan, V. et al. Bioacoustic-enabled patterning of human iPSC-derived cardiomyocytes into 3D cardiac tissue. Biomaterials 131, 47–57 (2017).

    Article  Google Scholar 

  85. Petta, D. et al. Sound-induced morphogenesis of multicellular systems for rapid orchestration of vascular networks. Biofabrication 13, 015004 (2020).

    Article  Google Scholar 

  86. Di Marzio, N. et al. Sound-based assembly of a microcapillary network in a Saturn-like tumor model for drug testing. Mater. Today Bio 16, 100357 (2022).

    Article  Google Scholar 

  87. Tognato, R. et al. Sound-based assembly of three-dimensional cellularized and acellularized constructs. Mater. Today Bio 22, 100775 (2023).

    Article  Google Scholar 

  88. Gu, L. et al. Size- and density-dependent acoustic differential bioassembly of spatially defined heterocellular architecture. Biofabrication 15, 015019 (2023).

    Article  Google Scholar 

  89. Wu, D. et al. Biomolecular actuators for genetically selective acoustic manipulation of cells. Sci. Adv. 9, eadd9186 (2023).

    Article  Google Scholar 

  90. Bach, J. S. & Bruus, H. Suppression of acoustic streaming in shape-optimized channels. Phys. Rev. Lett. 124, 214501 (2020).

    Article  Google Scholar 

  91. Karlsen, J. T., Qiu, W., Augustsson, P. & Bruus, H. Acoustic streaming and its suppression in inhomogeneous fluids. Phys. Rev. Lett. 120, 054501 (2018).

    Article  Google Scholar 

  92. Qiu, W., Karlsen, J. T., Bruus, H. & Augustsson, P. Experimental characterization of acoustic streaming in gradients of density and compressibility. Phys. Rev. Appl. 11, 024018 (2019).

    Article  Google Scholar 

  93. Hammarström, B., Laurell, T. & Nilsson, J. Seed particle-enabled acoustic trapping of bacteria and nanoparticles in continuous flow systems. Lab Chip 12, 4296–4304 (2012).

    Article  Google Scholar 

  94. Bazou, D., Castro, A. & Hoyos, M. Controlled cell aggregation in a pulsed acoustic field. Ultrasonics 52, 842–850 (2012).

    Article  Google Scholar 

  95. Hoyos, M. & Castro, A. Controlling the acoustic streaming by pulsed ultrasounds. Ultrasonics 53, 70–76 (2013).

    Article  Google Scholar 

  96. Wolfenson, H., Yang, B. & Sheetz, M. P. Steps in mechanotransduction pathways that control cell morphology. Annu. Rev. Physiol. 81, 585–605 (2019).

    Article  Google Scholar 

  97. Hofer, M. & Lutolf, M. P. Engineering organoids. Nat. Rev. Mater. 6, 402–420 (2021).

    Article  Google Scholar 

  98. Saraswathibhatla, A., Indana, D. & Chaudhuri, O. Cell–extracellular matrix mechanotransduction in 3D. Nat. Rev. Mol. Cell Biol. 24, 495–516 (2023).

    Article  Google Scholar 

  99. Chaudhuri, O., Cooper-White, J., Janmey, P. A., Mooney, D. J. & Shenoy, V. B. Effects of extracellular matrix viscoelasticity on cellular behaviour. Nature 584, 535–546 (2020).

    Article  Google Scholar 

  100. Elosegui-Artola, A. et al. Matrix viscoelasticity controls spatiotemporal tissue organization. Nat. Mater. 22, 117–127 (2023).

    Article  Google Scholar 

  101. Kim, T. et al. Deep brain stimulation by blood–brain-barrier-crossing piezoelectric nanoparticles generating current and nitric oxide under focused ultrasound. Nat. Biomed. Eng. 7, 149–163 (2023).

    Article  Google Scholar 

  102. Carley, E., King, M. C. & Guo, S. Integrating mechanical signals into cellular identity. Trends Cell Biol. 32, 669–680 (2022).

    Article  Google Scholar 

  103. Maresca, D. et al. Biomolecular ultrasound and sonogenetics. Annu. Rev. Chem. Biomol. Eng. 9, 229–252 (2018).

    Article  Google Scholar 

  104. Norris, E. G., Dalecki, D. & Hocking, D. C. Using acoustic fields to fabricate ECM-based biomaterials for regenerative medicine applications. Recent Prog. Mater. 2, 1–24 (2020).

    Article  Google Scholar 

  105. Blinc, A., Francis, C., Trudnowski, J. & Carstensen, E. Characterization of ultrasound-potentiated fibrinolysis in vitro. Blood 81, 2636–2643 (1993).

    Article  Google Scholar 

  106. Garvin, K. A., VanderBurgh, J., Hocking, D. C. & Dalecki, D. Controlling collagen fiber microstructure in three-dimensional hydrogels using ultrasound. J. Acoust. Soc. Am. 134, 1491–1502 (2013).

    Article  Google Scholar 

  107. Ray, A. & Provenzano, P. P. Aligned forces: origins and mechanisms of cancer dissemination guided by extracellular matrix architecture. Curr. Opin. Cell Biol. 72, 63–71 (2021).

    Article  Google Scholar 

  108. Huebsch, N. et al. Ultrasound-triggered disruption and self-healing of reversibly cross-linked hydrogels for drug delivery and enhanced chemotherapy. Proc. Natl Acad. Sci. USA 111, 9762–9767 (2014).

    Article  Google Scholar 

  109. Sun, Y., Chen, L.-G., Fan, X.-M. & Pang, J.-L. Ultrasound responsive smart implantable hydrogels for targeted delivery of drugs: reviewing current practices. Int. J. Nanomed. 17, 5001–5026 (2022).

    Article  Google Scholar 

  110. Lutolf, M. P. et al. Synthetic matrix metalloproteinase-sensitive hydrogels for the conduction of tissue regeneration: engineering cell-invasion characteristics. Proc. Natl Acad. Sci. USA 100, 5413–5418 (2003).

    Article  Google Scholar 

  111. Kloxin, A. M., Kasko, A. M., Salinas, C. N. & Anseth, K. S. Photodegradable hydrogels for dynamic tuning of physical and chemical properties. Science 324, 59–63 (2009).

    Article  Google Scholar 

  112. Huo, S. et al. Mechanochemical bond scission for the activation of drugs. Nat. Chem. 13, 131–139 (2021).

    Article  Google Scholar 

  113. Chandan, R., Mehta, S. & Banerjee, R. Ultrasound-responsive carriers for therapeutic applications. ACS Biomater. Sci. Eng. 6, 4731–4747 (2020).

    Article  Google Scholar 

  114. Moreno‐Gomez, N., Athanassiadis, A. G., Poortinga, A. T. & Fischer, P. Antibubbles enable tunable payload release with low‐intensity ultrasound. Adv. Mater. 35, 2305296 (2023).

    Article  Google Scholar 

  115. Kim, G. et al. High-intensity focused ultrasound-induced mechanochemical transduction in synthetic elastomers. Proc. Natl Acad. Sci. USA 116, 10214–10222 (2019).

    Article  Google Scholar 

  116. Lampi, M. C. & Reinhart-King, C. A. Targeting extracellular matrix stiffness to attenuate disease: from molecular mechanisms to clinical trials. Sci. Transl. Med. 10, eaao0475 (2018).

    Article  Google Scholar 

  117. Barriga, E. H., Franze, K., Charras, G. & Mayor, R. Tissue stiffening coordinates morphogenesis by triggering collective cell migration in vivo. Nature 554, 523–527 (2018).

    Article  Google Scholar 

  118. Nele, V. et al. Ultrasound-triggered enzymatic gelation. Adv. Mater. 32, 1905914 (2020).

    Article  Google Scholar 

  119. Sheeran, P. S., Luois, S. H., Mullin, L. B., Matsunaga, T. O. & Dayton, P. A. Design of ultrasonically-activatable nanoparticles using low boiling point perfluorocarbons. Biomaterials 33, 3262–3269 (2012).

    Article  Google Scholar 

  120. Farrell, E. et al. Spatiotemporal control of myofibroblast activation in acoustically-responsive scaffolds via ultrasound-induced matrix stiffening. Acta Biomater. 138, 133–143 (2022).

    Article  Google Scholar 

  121. McBeath, R., Pirone, D. M., Nelson, C. M., Bhadriraju, K. & Chen, C. S. Cell shape, cytoskeletal tension, and rhoa regulate stem cell lineage commitment. Dev. Cell 6, 483–495 (2004).

    Article  Google Scholar 

  122. Connelly, J. T. et al. Actin and serum response factor transduce physical cues from the microenvironment to regulate epidermal stem cell fate decisions. Nat. Cell Biol. 12, 711–718 (2010).

    Article  Google Scholar 

  123. Gjorevski, N. et al. Tissue geometry drives deterministic organoid patterning. Science 375, eaaw9021 (2022).

    Article  Google Scholar 

  124. Paun, I. A. et al. Osteogenic cells differentiation on topological surfaces under ultrasound stimulation. J. Mater. Sci. 54, 11213–11230 (2019).

    Article  Google Scholar 

  125. Higgins, S. G. et al. High‐aspect‐ratio nanostructured surfaces as biological metamaterials. Adv. Mater. 32, 1903862 (2020).

    Article  Google Scholar 

  126. Lim, W. A. The emerging era of cell engineering: harnessing the modularity of cells to program complex biological function. Science 378, 848–852 (2022).

    Article  Google Scholar 

  127. Iacoponi, F. et al. Optimal low-intensity pulsed ultrasound stimulation for promoting anti-inflammatory effects in macrophages. APL Bioeng. 7, 016114 (2023).

    Article  Google Scholar 

  128. Fechheimer, M. et al. Transfection of mammalian cells with plasmid DNA by scrape loading and sonication loading. Proc. Natl Acad. Sci. USA 84, 8463–8467 (1987).

    Article  Google Scholar 

  129. Bao, S., Thrall, B. D. & Miller, D. L. Transfection of a reporter plasmid into cultured cells by sonoporation in vitro. Ultrasound Med. Biol. 23, 953–959 (1997).

    Article  Google Scholar 

  130. Qiu, Y. et al. The correlation between acoustic cavitation and sonoporation involved in ultrasound-mediated DNA transfection with polyethylenimine (PEI) in vitro. J. Control. Rel. 145, 40–48 (2010).

    Article  Google Scholar 

  131. Stewart, M. P., Langer, R. & Jensen, K. F. Intracellular delivery by membrane disruption: mechanisms, strategies, and concepts. Chem. Rev. 118, 7409–7531 (2018).

    Article  Google Scholar 

  132. Mizrahi, N. et al. Low intensity ultrasound perturbs cytoskeleton dynamics. Soft Matter 8, 2438–2443 (2012).

    Article  Google Scholar 

  133. Blackmore, J., Shrivastava, S., Sallet, J., Butler, C. R. & Cleveland, R. O. Ultrasound neuromodulation: a review of results, mechanisms and safety. Ultrasound Med. Biol. 45, 1509–1536 (2019).

    Article  Google Scholar 

  134. Jerusalem, A. et al. Electrophysiological–mechanical coupling in the neuronal membrane and its role in ultrasound neuromodulation and general anaesthesia. Acta Biomater. 97, 116–140 (2019).

    Article  Google Scholar 

  135. Kamimura, H. A. S., Conti, A., Toschi, N. & Konofagou, E. E. Ultrasound neuromodulation: mechanisms and the potential of multimodal stimulation for neuronal function assessment. Front. Phys. 8, 150 (2020).

    Article  Google Scholar 

  136. Rabut, C. et al. Ultrasound technologies for imaging and modulating neural activity. Neuron 108, 93–110 (2020).

    Article  Google Scholar 

  137. Imashiro, C. et al. Travelling ultrasound promotes vasculogenesis of three‐dimensional‐monocultured human umbilical vein endothelial cells. Biotechnol. Bioeng. 118, 3760–3769 (2021).

    Article  Google Scholar 

  138. Bashardoust Tajali, S., Houghton, P., MacDermid, J. C. & Grewal, R. Effects of low-intensity pulsed ultrasound therapy on fracture healing: a systematic review and meta-analysis. Am. J. Phys. Med. Rehabil. 91, 349–367 (2012).

    Article  Google Scholar 

  139. Zhou, X. et al. Improved human bone marrow mesenchymal stem cell osteogenesis in 3D bioprinted tissue scaffolds with low intensity pulsed ultrasound stimulation. Sci. Rep. 6, 32876 (2016).

    Article  Google Scholar 

  140. Palanisamy, P., Alam, M., Li, S., Chow, S. K. H. & Zheng, Y. Low‐intensity pulsed ultrasound stimulation for bone fractures healing: a review. J. Ultrasound Med. 41, 547–563 (2022).

    Article  Google Scholar 

  141. Ikeda, K. et al. Effects of low-intensity pulsed ultrasound on the differentiation of C2C12 cells. Life Sci. 79, 1936–1943 (2006).

    Article  Google Scholar 

  142. Lai, C.-H. et al. Effects of low-intensity pulsed ultrasound, dexamethasone/TGF-β1 and/or BMP-2 on the transcriptional expression of genes in human mesenchymal stem cells: chondrogenic vs. osteogenic differentiation. Ultrasound Med. Biol. 36, 1022–1033 (2010).

    Article  Google Scholar 

  143. Ambattu, L. A., Gelmi, A. & Yeo, L. Y. Short‐duration high frequency megahertz‐order nanomechanostimulation drives early and persistent osteogenic differentiation in mesenchymal stem cells. Small 18, 2106823 (2022).

    Article  Google Scholar 

  144. Duque, M. et al. Sonogenetic control of mammalian cells using exogenous transient receptor potential A1 channels. Nat. Commun. 13, 600 (2022).

    Article  Google Scholar 

  145. Yoo, S., Mittelstein, D. R., Hurt, R. C., Lacroix, J. & Shapiro, M. G. Focused ultrasound excites cortical neurons via mechanosensitive calcium accumulation and ion channel amplification. Nat. Commun. 13, 493 (2022).

    Article  Google Scholar 

  146. Collins, M. N. & Mesce, K. A. A review of the bioeffects of low-intensity focused ultrasound and the benefits of a cellular approach. Front. Physiol. 13, 1047324 (2022).

    Article  Google Scholar 

  147. Zhang, M. et al. Cell mechanical responses to subcellular perturbations generated by ultrasound and targeted microbubbles. Acta Biomater. 155, 471–481 (2023).

    Article  Google Scholar 

  148. Riehl, B. D., Park, J.-H., Kwon, I. K. & Lim, J. Y. Mechanical stretching for tissue engineering: two-dimensional and three-dimensional constructs. Tissue Eng. Part B 18, 288–300 (2012).

    Article  Google Scholar 

  149. Brown, T. D. Techniques for mechanical stimulation of cells in vitro: a review. J. Biomech. 33, 3–14 (2000).

    Article  Google Scholar 

  150. Terraciano, V. et al. Differential response of adult and embryonic mesenchymal progenitor cells to mechanical compression in hydrogels. Stem Cell 25, 2730–2738 (2007).

    Article  Google Scholar 

  151. Datta, N. et al. In vitro generated extracellular matrix and fluid shear stress synergistically enhance 3D osteoblastic differentiation. Proc. Natl Acad. Sci. USA 103, 2488–2493 (2006).

    Article  Google Scholar 

  152. Kapur, S., Baylink, D. J. & William Lau, K.-H. Fluid flow shear stress stimulates human osteoblast proliferation and differentiation through multiple interacting and competing signal transduction pathways. Bone 32, 241–251 (2003).

    Article  Google Scholar 

  153. Ozcelik, A. et al. Acoustofluidic rotational manipulation of cells and organisms using oscillating solid structures. Small 12, 5120–5125 (2016).

    Article  Google Scholar 

  154. Ahmed, D. et al. Rotational manipulation of single cells and organisms using acoustic waves. Nat. Commun. 7, 11085 (2016).

    Article  Google Scholar 

  155. Coussios, C. C. & Roy, R. A. Applications of acoustics and cavitation to noninvasive therapy and drug delivery. Annu. Rev. Fluid Mech. 40, 395–420 (2008).

    Article  MathSciNet  Google Scholar 

  156. Shiraishi, K. et al. Biophysical forces mediated by respiration maintain lung alveolar epithelial cell fate. Cell 186, 1478–1492.e15 (2023).

    Article  Google Scholar 

  157. Nitsan, I., Drori, S., Lewis, Y. E., Cohen, S. & Tzlil, S. Mechanical communication in cardiac cell synchronized beating. Nat. Phys. 12, 472–477 (2016).

    Article  Google Scholar 

  158. Mishra, P., Hill, M. & Glynne-Jones, P. Deformation of red blood cells using acoustic radiation forces. Biomicrofluidics 8, 034109 (2014).

    Article  Google Scholar 

  159. Bezer, J. H., Koruk, H., Rowlands, C. J. & Choi, J. J. Elastic deformation of soft tissue-mimicking materials using a single microbubble and acoustic radiation force. Ultrasound Med. Biol. 46, 3327–3338 (2020).

    Article  Google Scholar 

  160. Zhang, Y. & Habibovic, P. Delivering mechanical stimulation to cells: state of the art in materials and devices design. Adv. Mater. 34, 2110267 (2022).

    Article  Google Scholar 

  161. Cafarelli, A. et al. Piezoelectric nanomaterials activated by ultrasound: the pathway from discovery to future clinical adoption. ACS Nano 15, 11066–11086 (2021).

    Article  Google Scholar 

  162. Yildiz, D., Göstl, R. & Herrmann, A. Sonopharmacology: controlling pharmacotherapy and diagnosis by ultrasound-induced polymer mechanochemistry. Chem. Sci. 13, 13708–13719 (2022).

    Article  Google Scholar 

  163. Mitragotri, S. Healing sound: the use of ultrasound in drug delivery and other therapeutic applications. Nat. Rev. Drug Discov. 4, 255–260 (2005).

    Article  Google Scholar 

  164. Rich, J., Tian, Z. & Huang, T. J. Sonoporation: past, present, and future. Adv. Mater. Technol. 7, 2100885 (2022).

    Article  Google Scholar 

  165. Yu, H. & Xu, L. Cell experimental studies on sonoporation: state of the art and remaining problems. J. Control. Rel. 174, 151–160 (2014).

    Article  Google Scholar 

  166. Aryal, M., Arvanitis, C. D., Alexander, P. M. & McDannold, N. Ultrasound-mediated blood–brain barrier disruption for targeted drug delivery in the central nervous system. Adv. Drug Deliv. Rev. 72, 94–109 (2014).

    Article  Google Scholar 

  167. Fletcher, S.-M. P., Choi, M., Ogrodnik, N. & O’Reilly, M. A. A porcine model of transvertebral ultrasound and microbubble-mediated blood-spinal cord barrier opening. Theranostics 10, 7758–7774 (2020).

    Article  Google Scholar 

  168. Bleker, S. et al. Modulation of the blood–retina-barrier permeability by focused ultrasound: computational and experimental approaches. J. Acoust. Soc. Am. 153, A68 (2023).

    Article  Google Scholar 

  169. Oberli, M. A., Schoellhammer, C. M., Langer, R. & Blankschtein, D. Ultrasound-enhanced transdermal delivery: recent advances and future challenges. Ther. Deliv. 5, 843–857 (2014).

    Article  Google Scholar 

  170. Lentacker, I., De Cock, I., Deckers, R., De Smedt, S. C. & Moonen, C. T. W. Understanding ultrasound induced sonoporation: definitions and underlying mechanisms. Adv. Drug Deliv. Rev. 72, 49–64 (2014).

    Article  Google Scholar 

  171. Son, S. et al. Multifunctional sonosensitizers in sonodynamic cancer therapy. Chem. Soc. Rev. 49, 3244–3261 (2020).

    Article  Google Scholar 

  172. Crum, L., Bailey, M., Hwang, J. H., Khokhlova, V. & Sapozhnikov, O. Therapeutic ultrasound: recent trends and future perspectives. Phys. Procedia 3, 25–34 (2010).

    Article  Google Scholar 

  173. Yang, Y. et al. Sonothermogenetics for noninvasive and cell-type specific deep brain neuromodulation. Brain Stimul. 14, 790–800 (2021).

    Article  Google Scholar 

  174. Shapiro, M. G. et al. Biogenic gas nanostructures as ultrasonic molecular reporters. Nat. Nanotechnol. 9, 311–316 (2014).

    Article  Google Scholar 

  175. Lakshmanan, A. et al. Acoustic biosensors for ultrasound imaging of enzyme activity. Nat. Chem. Biol. 16, 988–996 (2020).

    Article  Google Scholar 

  176. Ibsen, S., Tong, A., Schutt, C., Esener, S. & Chalasani, S. H. Sonogenetics is a non-invasive approach to activating neurons in Caenorhabditis elegans. Nat. Commun. 6, 8264 (2015).

    Article  Google Scholar 

  177. Leskinen, J. J. & Hynynen, K. Study of factors affecting the magnitude and nature of ultrasound exposure with in vitro set-ups. Ultrasound Med. Biol. 38, 777–794 (2012).

    Article  Google Scholar 

  178. Snehota, M., Vachutka, J., Ter Haar, G., Dolezal, L. & Kolarova, H. Therapeutic ultrasound experiments in vitro: review of factors influencing outcomes and reproducibility. Ultrasonics 107, 106167 (2020).

    Article  Google Scholar 

  179. Izadifar, Z., Izadifar, Z., Chapman, D. & Babyn, P. An introduction to high intensity focused ultrasound: systematic review on principles, devices, and clinical applications. J. Clin. Med. 9, 460 (2020).

    Article  Google Scholar 

  180. Miller, D. L. et al. Overview of therapeutic ultrasound applications and safety considerations. J. Ultrasound Med. 31, 623–634 (2012).

    Article  Google Scholar 

  181. Qiu, Y. et al. Acoustic devices for particle and cell manipulation and sensing. Sensors 14, 14806–14838 (2014).

    Article  Google Scholar 

  182. Jin, Y. et al. Magnetic control of axon navigation in reprogrammed neurons. Nano Lett. 19, 6517–6523 (2019).

    Article  Google Scholar 

  183. Yun, S. et al. Design of magnetically labeled cells (mag-cells) for in vivo control of stem cell migration and differentiation. Nano Lett. 18, 838–845 (2018).

    Article  Google Scholar 

  184. Kappes, M. et al. Superparamagnetic iron oxide nanoparticles for targeted cell seeding: magnetic patterning and magnetic 3D cell culture. Adv. Funct. Mater. 32, 2203672 (2022).

    Article  Google Scholar 

  185. Bratt-Leal, A. M., Kepple, K. L., Carpenedo, R. L., Cooke, M. T. & McDevitt, T. C. Magnetic manipulation and spatial patterning of multi-cellular stem cell aggregates. Integr. Biol. 3, 1224–1232 (2011).

    Article  Google Scholar 

  186. Rangarajan, S., Madden, L. & Bursac, N. Use of flow, electrical, and mechanical stimulation to promote engineering of striated muscles. Ann. Biomed. Eng. 42, 1391–1405 (2014).

    Article  Google Scholar 

  187. Borchers, S., Himmelbach, M., Logothetis, N. & Karnath, H.-O. Direct electrical stimulation of human cortex — the gold standard for mapping brain functions? Nat. Rev. Neurosci. 13, 63–70 (2012).

    Article  Google Scholar 

  188. Jimenez-Gambin, S., Jimenez, N., Benlloch, J. M. & Camarena, F. Holograms to focus arbitrary ultrasonic fields through the skull. Phys. Rev. Appl. 12, 014106 (2019).

    Article  Google Scholar 

  189. Karatum, O., Han, M., Erdogan, E. T., Karamursel, S. & Nizamoglu, S. Physical mechanisms of emerging neuromodulation modalities. J. Neural Eng. 20, 031001 (2023).

    Article  Google Scholar 

  190. Parfenov, V. A. et al. Biofabrication of a functional tubular construct from tissue spheroids using magnetoacoustic levitational directed assembly. Adv. Healthc. Mater. 9, 2000721 (2020).

    Article  Google Scholar 

  191. Leighton, T. G. What is ultrasound? Prog. Biophys. Mol. Biol. 93, 3–83 (2007).

    Article  Google Scholar 

  192. Bertin, N. et al. Bubble-based acoustic micropropulsors: active surfaces and mixers. Lab Chip 17, 1515–1528 (2017).

    Article  Google Scholar 

  193. Wiklund, M., Green, R. & Ohlin, M. Acoustofluidics 14: applications of acoustic streaming in microfluidic devices. Lab Chip 12, 2438 (2012).

    Article  Google Scholar 

  194. Salari, A. et al. Dancing with the cells: acoustic microflows generated by oscillating cells. Small 16, 1903788 (2020).

    Article  Google Scholar 

  195. Rasouli, R., Villegas, K. M. & Tabrizian, M. Acoustofluidics — changing paradigm in tissue engineering, therapeutics development, and biosensing. Lab Chip 23, 1300–1338 (2023).

    Article  Google Scholar 

  196. Friend, J. & Yeo, L. Y. Microscale acoustofluidics: microfluidics driven via acoustics and ultrasonics. Rev. Mod. Phys. 83, 647–704 (2011).

    Article  Google Scholar 

  197. Drinkwater, B. W. Dynamic-field devices for the ultrasonic manipulation of microparticles. Lab Chip 16, 2360–2375 (2016).

    Article  Google Scholar 

  198. Kinsler, L. E. et al. (eds) Fundamentals of Acoustics 149–170 (Wiley, 2000).

  199. Kinsler, L. E. et al. (eds) Fundamentals of Acoustics 210–245 (Wiley, 2000).

  200. Blaeser, A. et al. Controlling shear stress in 3D bioprinting is a key factor to balance printing resolution and stem cell integrity. Adv. Healthc. Mater. 5, 326–333 (2016).

    Article  Google Scholar 

  201. Miri, A. K. et al. Effective bioprinting resolution in tissue model fabrication. Lab Chip 19, 2019–2037 (2019).

    Article  Google Scholar 

  202. Adhikari, J. et al. Effects of processing parameters of 3D bioprinting on the cellular activity of bioinks. Macromol. Biosci. 21, 2000179 (2021).

    Article  Google Scholar 

  203. Madrid-Wolff, J., Boniface, A., Loterie, D., Delrot, P. & Moser, C. Controlling light in scattering materials for volumetric additive manufacturing. Adv. Sci. 9, 2105144 (2022).

    Article  Google Scholar 

  204. Gudapati, H., Dey, M. & Ozbolat, I. A comprehensive review on droplet-based bioprinting: past, present and future. Biomaterials 102, 20–42 (2016).

    Article  Google Scholar 

  205. Li, X. et al. Inkjet bioprinting of biomaterials. Chem. Rev. 120, 10793–10833 (2020).

    Article  Google Scholar 

  206. Duck, F. A. Medical and non-medical protection standards for ultrasound and infrasound. Prog. Biophys. Mol. Biol. 93, 176–191 (2007).

    Article  Google Scholar 

  207. Baker, K. G., Robertson, V. J. & Duck, F. A. A review of therapeutic ultrasound: biophysical effects. Phys. Ther. 81, 1351–1358 (2001).

    Article  Google Scholar 

  208. FDA. Marketing clearance of diagnostic ultrasound systems and transducers. U.S. Food and Drug Administration https://www.fda.gov/media/71100/download (2019).

  209. Apfel, R. E. & Holland, C. K. Gauging the likelihood of cavitation from short-pulse, low-duty cycle diagnostic ultrasound. Ultrasound Med. Biol. 17, 179–185 (1991).

    Article  Google Scholar 

  210. Hariharan, P., Myers, M. R. & Banerjee, R. K. HIFU procedures at moderate intensities — effect of large blood vessels. Phys. Med. Biol. 52, 3493–3513 (2007).

    Article  Google Scholar 

  211. Ter Haar, G. et al. Guidance on reporting ultrasound exposure conditions for bio-effects studies. Ultrasound Med. Biol. 37, 177–183 (2011).

    Article  Google Scholar 

  212. Preston, R. C. & Shaw, A. Recommended Ultrasound Field Safety Classification for Medical Diagnostic Devices. Measurement Good Practice Guide, 50. National Physical Laboratory https://eprintspublications.npl.co.uk/2113/ (2001).

  213. Fontana, F. et al. Development and validation of low-intensity pulsed ultrasound systems for highly controlled in vitro cell stimulation. Ultrasonics 116, 106495 (2021).

    Article  Google Scholar 

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Acknowledgements

The research was in part supported by the European Research Council under the ERC Advanced Grant Agreement HOLOMAN (no. 788296); and the German Research Foundation (Deutsche Forschungsgemeinschaft, DFG) under Germany’s Excellence Strategy through the Excellence Cluster 3D Matter Made to Order (EXC-2082/1-390761711) and the Carl-Zeiss-Stiftung (P2022-04-073).

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  1. These authors contributed equally: Kai Melde, Athanasios G. Athanassiadis, Dimitris Missirlis.

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  1. Max Planck Institute for Medical Research, Heidelberg, Germany

    Kai Melde, Athanasios G. Athanassiadis, Dimitris Missirlis, Minghui Shi, Senne Seneca & Peer Fischer

  2. Institute for Molecular Systems Engineering and Advanced Materials, Heidelberg University, Heidelberg, Germany

    Kai Melde, Athanasios G. Athanassiadis, Dimitris Missirlis, Minghui Shi, Senne Seneca & Peer Fischer

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K.M. and P.F. are inventors on a patent related to this work granted by the European Patent Office (EP3034281 B1). K.M. and P.F. declare no other competing interests. The remaining authors declare no competing interests.

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Melde, K., Athanassiadis, A.G., Missirlis, D. et al. Ultrasound-assisted tissue engineering. Nat Rev Bioeng (2024). https://doi.org/10.1038/s44222-024-00166-5

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