Skip to main content

Advertisement

SpringerLink
Log in

Surface acoustic wave (SAW) techniques in tissue engineering

  • Review
  • Published:
Cell and Tissue Research Aims and scope Submit manuscript

Abstract

Recently, the introduction of surface acoustic wave (SAW) technique for microfluidics has drawn a lot of attention. The pattern and mutual communication in cell layers, tissues, and organs play a critical role in tissue homeostasis and regeneration and may contribute to disease occurrence and progression. Tissue engineering aims to repair and regenerate damaged organs, depending on biomimetic scaffolds and advanced fabrication technology. However, traditional bioengineering synthesis approaches are time-consuming, heterogeneous, and unmanageable. It is hard to pattern cells in scaffolds effectively with no impact on cell viability and function. Here, we summarize a biocompatible, easily available, label-free, and non-invasive tool, surface acoustic wave (SAW) technique, which is getting a lot of attention in tissue engineering. SAW technique can realize accurate sorting, manipulation, and cells’ pattern and rapid formation of spheroids. By integrating several SAW devices onto lab-on-a-chip platforms, tissue engineering lab-on-a-chip system was proposed. To the best of our knowledge, this is the first report to summarize the application of this novel technique in the field of tissue engineering.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Adams TNG, Jiang AYL, Mendoza NS, Ro CC, Lee DH, Lee AP, Flanagan LA (2020) Label-free enrichment of fate-biased human neural stem and progenitor cells. Biosens Bioelectron 152:111982

    Article  CAS  PubMed  Google Scholar 

  • Ai Y, Sanders CK, Marrone BL (2013) Separation of Escherichia coli bacteria from peripheral blood mononuclear cells using standing surface acoustic waves. Anal Chem 85:9126–9134

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Alajati A, Laib AM, Weber H, Boos AM, Bartol A, Ikenberg K, Korff T, Zentgraf H, Obodozie C, Graeser R et al (2008) Spheroid-based engineering of a human vasculature in mice. Nat Methods 5:439–445

    Article  CAS  PubMed  Google Scholar 

  • Alhasan L, Qi A, Al-Abboodi A, Rezk A, Chan PPY, Iliescu C, Yeo LY (2016) Rapid enhancement of cellular spheroid assembly by acoustically driven microcentrifugation. Acs Biomater Sci Eng 2:1013–1022

    Article  CAS  PubMed  Google Scholar 

  • Barnkob, R., Augustsson, P., Laurell, T., and Bruus, H. (2012). Acoustic radiation- and streaming-induced microparticle velocities determined by microparticle image velocimetry in an ultrasound symmetry plane. Physical review. E, Statistical, nonlinear, and soft matter physics 86, 056307.

  • Bouyer C, Chen P, Güven S, Demirtaş TT, Nieland TJ, Padilla F, Demirci U (2016) 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

    Article  CAS  PubMed  Google Scholar 

  • Chen B, Wu Y, Ao Z, Cai H, Nunez A, Liu Y, Foley J, Nephew K, Lu X, Guo F (2019) High-throughput acoustofluidic fabrication of tumor spheroids. Lab Chip 19:1755–1763

    Article  CAS  PubMed  Google Scholar 

  • Chen K, Wu M, Guo F, Li P, Chan CY, Mao Z, Li S, Ren L, Zhang R, Huang TJ (2016) Rapid formation of size-controllable multicellular spheroids via 3D acoustic tweezers. Lab Chip 16:2636–2643

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen P, Güven S, Usta OB, Yarmush ML, Demirci U (2015) Biotunable acoustic node assembly of organoids. Adv Healthc Mater 4:1937–1943

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen Y, Li S, Gu Y, Li P, Ding X, Wang L, McCoy JP, Levine SJ, Huang TJ (2014) Continuous enrichment of low-abundance cell samples using standing surface acoustic waves (SSAW). Lab Chip 14:924–930

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Choi C-H, Jung J-H, Rhee YW, Kim D-P, Shim S-E, Lee C-S (2007) Generation of monodisperse alginate microbeads and in situ encapsulation of cell in microfluidic device. Biomed Microdevice 9:855–862

    Article  CAS  Google Scholar 

  • Chung C, Mesa J, Miller GJ, Randolph MA, Gill TJ, Burdick JA (2006) Effects of auricular chondrocyte expansion on neocartilage formation in photocrosslinked hyaluronic acid networks. Tissue Eng 12:2665–2673

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Clark NM, Buckner E, Fisher AP, Nelson EC, Nguyen TT, Simmons AR, de Luis Balaguer MA, Butler-Smith T, Sheldon PJ, Bergmann DC et al (2019) Stem-cell-ubiquitous genes spatiotemporally coordinate division through regulation of stem-cell-specific gene networks. Nat Commun 10:5574

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Coller HA (2011) Cell biology The essence of quiescence. Science 334:1074–1075

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Collins DJ, Khoo BL, Ma Z, Winkler A, Weser R, Schmidt H, Han J, Ai Y (2017) Selective particle and cell capture in a continuous flow using micro-vortex acoustic streaming. Lab Chip 17:1769–1777

    Article  CAS  PubMed  Google Scholar 

  • Collins DJ, Ma Z, Ai Y (2016) Highly localized acoustic streaming and size-selective submicrometer particle concentration using high frequency microscale focused acoustic fields. Anal Chem 88:5513–5522

    Article  CAS  PubMed  Google Scholar 

  • Darling EM, Topel M, Zauscher S, Vail TP, Guilak F (2008) Viscoelastic properties of human mesenchymally-derived stem cells and primary osteoblasts, chondrocytes, and adipocytes. J Biomech 41:454–464

    Article  PubMed  Google Scholar 

  • Davey HM, Kell DB (1996) Flow cytometry and cell sorting of heterogeneous microbial populations: the importance of single-cell analyses. Microbiol Rev 60:641–696

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Destgeer G, Ha B, Park J, Sung HJ (2016) Lamb wave-based acoustic radiation force-driven particle ring formation inside a sessile droplet. Anal Chem 88:3976–3981

    Article  CAS  PubMed  Google Scholar 

  • Ding X, Li P, Lin SC, Stratton ZS, Nama N, Guo F, Slotcavage D, Mao X, Shi J, Costanzo F et al (2013) Surface acoustic wave microfluidics. Lab Chip 13:3626–3649

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ding X, Lin SC, Kiraly B, Yue H, Li S, Chiang IK, Shi J, Benkovic SJ, Huang TJ (2012) On-chip manipulation of single microparticles, cells, and organisms using surface acoustic waves. Proc Natl Acad Sci USA 109:11105–11109

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ding X, Lin SC, Lapsley MI, Li S, Guo X, Chan CY, Chiang IK, Wang L, McCoy JP, Huang TJ (2012) Standing surface acoustic wave (SSAW) based multichannel cell sorting. Lab Chip 12:4228–4231

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ding X, Peng Z, Lin SC, Geri M, Li S, Li P, Chen Y, Dao M, Suresh S, Huang TJ (2014) Cell separation using tilted-angle standing surface acoustic waves. Proc Natl Acad Sci USA 111:12992–12997

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ding X, Shi J, Lin SC, Yazdi S, Kiraly B, Huang TJ (2012) Tunable patterning of microparticles and cells using standing surface acoustic waves. Lab Chip 12:2491–2497

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dissanayaka WL, Zhu L, Hargreaves KM, Jin L, Zhang C (2014) Scaffold-free prevascularized microtissue spheroids for pulp regeneration. J Dent Res 93:1296–1303

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dong J, Uemura T, Shirasaki Y, Tateishi T (2002) Promotion of bone formation using highly pure porous beta-TCP combined with bone marrow-derived osteoprogenitor cells. Biomaterials 23:4493–4502

    Article  CAS  PubMed  Google Scholar 

  • Drury JL, Mooney DJ (2003) Hydrogels for tissue engineering: scaffold design variables and applications. Biomaterials 24:4337–4351

    Article  CAS  PubMed  Google Scholar 

  • Dutta RC, Dutta AK (2009) Cell-interactive 3D-scaffold; advances and applications. Biotechnol Adv 27:334–339

    Article  CAS  PubMed  Google Scholar 

  • El-Ali J, Sorger PK, Jensen KF (2006) Cells on chips. Nature 442:403–411

    Article  CAS  PubMed  Google Scholar 

  • Evander M, Nilsson J (2012) Acoustofluidics 20: applications in acoustic trapping. Lab Chip 12:4667–4676

    Article  CAS  PubMed  Google Scholar 

  • Fallah MA, Myles VM, Krüger T, Sritharan K, Wixforth A, Varnik F, Schneider SW, Schneider MF (2010) Acoustic driven flow and lattice Boltzmann simulations to study cell adhesion in biofunctionalized mu-fluidic channels with complex geometry. Biomicrofluidics 4

  • Franke T, Abate AR, Weitz DA, Wixforth A (2009) Surface acoustic wave (SAW) directed droplet flow in microfluidics for PDMS devices. Lab Chip 9:2625–2627

    Article  CAS  PubMed  Google Scholar 

  • Freyman TM, Yannas IV, Gibson LJ (2001) Cellular materials as porous scaffolds for tissue engineering. Prog Mater Sci 46:273–282

    Article  CAS  Google Scholar 

  • Friedrich J, Seidel C, Ebner R, Kunz-Schughart LA (2009) Spheroid-based drug screen: considerations and practical approach. Nat Protoc 4:309–324

    Article  CAS  PubMed  Google Scholar 

  • Friend JR, Yeo LY, Arifin DR, Mechler A (2008) Evaporative self-assembly assisted synthesis of polymeric nanoparticles by surface acoustic wave atomization. Nanotechnology 19:145301

    Article  PubMed  CAS  Google Scholar 

  • Frommelt T, Kostur M, Wenzel-Schäfer M, Talkner P, Hänggi P, Wixforth A (2008) Microfluidic mixing via acoustically driven chaotic advection. Phys Rev Lett 100:034502

    Article  PubMed  CAS  Google Scholar 

  • Girardo S, Cecchini M, Beltram F, Cingolani R, Pisignano D (2008) Polydimethylsiloxane-LiNbO3 surface acoustic wave micropump devices for fluid control into microchannels. Lab Chip 8:1557–1563

    Article  CAS  PubMed  Google Scholar 

  • Glass NR, Shilton RJ, Chan PP, Friend JR, Yeo LY (2012) Miniaturized Lab-on-a-Disc (miniLOAD). Small 8:1881–1888

    Article  CAS  PubMed  Google Scholar 

  • González-Cruz RD, Fonseca VC, Darling EM (2012) Cellular mechanical properties reflect the differentiation potential of adipose-derived mesenchymal stem cells. Proc Natl Acad Sci USA 109:E1523-1529

    Article  PubMed  PubMed Central  Google Scholar 

  • Gothard D, Tare RS, Mitchell PD, Dawson JI, Oreffo RO (2011) In search of the skeletal stem cell: isolation and separation strategies at the macro/micro scale for skeletal regeneration. Lab Chip 11:1206–1220

    Article  CAS  PubMed  Google Scholar 

  • Grogan SP, Pauli C, Chen P, Du J, Chung CB, Kong SD, Colwell CW Jr, Lotz MK, Jin S, D’Lima DD (2012) In situ tissue engineering using magnetically guided three-dimensional cell patterning. Tissue engineering Part C, Methods 18:496–506

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gronewold TM (2007) Surface acoustic wave sensors in the bioanalytical field: recent trends and challenges. Anal Chim Acta 603:119–128

    Article  CAS  PubMed  Google Scholar 

  • Guo F, Li P, French JB, Mao Z, Zhao H, Li S, Nama N, Fick JR, Benkovic SJ, Huang TJ (2015) Controlling cell-cell interactions using surface acoustic waves. Proc Natl Acad Sci USA 112:43–48

    Article  CAS  PubMed  Google Scholar 

  • Guttenberg Z, Muller H, Habermüller H, Geisbauer A, Pipper J, Felbel J, Kielpinski M, Scriba J, Wixforth A (2005) Planar chip device for PCR and hybridization with surface acoustic wave pump. Lab Chip 5:308–317

    Article  CAS  PubMed  Google Scholar 

  • Hagsäter SM, Jensen TG, Bruus H, Kutter JP (2007) Acoustic resonances in microfluidic chips: full-image micro-PIV experiments and numerical simulations. Lab Chip 7:1336–1344

    Article  PubMed  CAS  Google Scholar 

  • Hsiao AY, Torisawa YS, Tung YC, Sud S, Taichman RS, Pienta KJ, Takayama S (2009) Microfluidic system for formation of PC-3 prostate cancer co-culture spheroids. Biomaterials 30:3020–3027

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ingram M, Techy GB, Saroufeem R, Yazan O, Narayan KS, Goodwin TJ, Spaulding GF (1997) Three-dimensional growth patterns of various human tumor cell lines in simulated microgravity of a NASA bioreactor. In vitro cellular & developmental biology. Animal 33:459–466

    CAS  Google Scholar 

  • Jo MC, Guldiken R (2012) Active density-based separation using standing surface acoustic waves. Sens Actuators, A 187:22–28

    Article  CAS  Google Scholar 

  • Kang B, Shin J, Park HJ, Rhyou C, Kang D, Lee SJ, Yoon YS, Cho SW, Lee H (2018) High-resolution acoustophoretic 3D cell patterning to construct functional collateral cylindroids for ischemia therapy. Nat Commun 9:5402

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kasza KE, Rowat AC, Liu J, Angelini TE, Brangwynne CP, Koenderink GH, Weitz DA (2007) The cell as a material. Curr Opin Cell Biol 19:101–107

    Article  CAS  PubMed  Google Scholar 

  • Kievit FM, Florczyk SJ, Leung MC, Wang K, Wu JD, Silber JR, Ellenbogen RG, Lee JS, Zhang M (2014) Proliferation and enrichment of CD133(+) glioblastoma cancer stem cells on 3D chitosan-alginate scaffolds. Biomaterials 35:9137–9143

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim C, Chung S, Kim YE, Lee KS, Lee SH, Oh KW, Kang JY (2011) Generation of core-shell microcapsules with three-dimensional focusing device for efficient formation of cell spheroid. Lab Chip 11:246–252

    Article  CAS  PubMed  Google Scholar 

  • Kim C, Lee KS, Bang JH, Kim YE, Kim M-C, Oh KW, Lee SH, Kang JY (2011) 3-Dimensional cell culture for on-chip differentiation of stem cells in embryoid body. Lab Chip 11:874–882

    Article  CAS  PubMed  Google Scholar 

  • Kirkham GR, Britchford E, Upton T, Ware J, Gibson GM, Devaud Y, Ehrbar M, Padgett M, Allen S, Buttery LD et al (2015) Precision assembly of complex cellular microenvironments using holographic optical tweezers. Sci Rep 5:8577

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kloss D, Fischer M, Rothermel A, Simon JC, Robitzki AA (2008) Drug testing on 3D in vitro tissues trapped on a microcavity chip. Lab Chip 8:879–884

    Article  CAS  PubMed  Google Scholar 

  • Kumar G, Tison CK, Chatterjee K, Pine PS, McDaniel JH, Salit ML, Young MF, Simon CG Jr (2011) The determination of stem cell fate by 3D scaffold structures through the control of cell shape. Biomaterials 32:9188–9196

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Länge K, Blaess G, Voigt A, Götzen R, Rapp M (2006) Integration of a surface acoustic wave biosensor in a microfluidic polymer chip. Biosens Bioelectron 22:227–232

    Article  PubMed  CAS  Google Scholar 

  • Langer R, Vacanti JP (1993) Tissue engineering. Science 260:920–926

    Article  CAS  PubMed  Google Scholar 

  • Lata JP, Guo F, Guo J, Huang PH, Yang J, Huang TJ (2016) Surface acoustic waves grant superior spatial control of cells embedded in hydrogel fibers. Adv Mater 28:8632–8638

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lee J, Choi YS, Lee Y, Lee HJ, Lee JN, Kim SK, Han KY, Cho EC, Park JC, Lee SS (2011) Sensitive and simultaneous detection of cardiac markers in human serum using surface acoustic wave immunosensor. Anal Chem 83:8629–8635

    Article  CAS  PubMed  Google Scholar 

  • Lee JS, Jin Y, Park H-J, Yang K, Lee MS, Yang HS, Cho S-W (2017) In situ bone tissue engineering with an endogenous stem cell mobilizer and osteoinductive nanofibrous polymeric scaffolds. Biotechnol J 12:1700062

    Article  CAS  Google Scholar 

  • Li H, Chang J (2004) Fabrication and characterization of bioactive wollastonite/PHBV composite scaffolds. Biomaterials 25:5473–5480

    Article  CAS  PubMed  Google Scholar 

  • Li H, Friend JR, Yeo LY (2007a) A scaffold cell seeding method driven by surface acoustic waves. Biomaterials 28:4098–4104

    Article  CAS  PubMed  Google Scholar 

  • Li H, Friend JR, Yeo LY (2007b) Surface acoustic wave concentration of particle and bioparticle suspensions. Biomed Microdevices 9:647–656

    Article  CAS  PubMed  Google Scholar 

  • Li P, Mao Z, Peng Z, Zhou L, Chen Y, Huang P-H, Truica CI, Drabick JJ, El-Deiry WS, Dao M (2015) Acoustic separation of circulating tumor cells. Proc Natl Acad Sci 112:4970–4975

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lin H, Zhang D, Alexander PG, Yang G, Tan J, Cheng AW, Tuan RS (2013) Application of visible light-based projection stereolithography for live cell-scaffold fabrication with designed architecture. Biomaterials 34:331–339

    Article  CAS  PubMed  Google Scholar 

  • Lin SC, Mao X, Huang TJ (2012) Surface acoustic wave (SAW) acoustophoresis: now and beyond. Lab Chip 12:2766–2770

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lindvall O, Kokaia Z (2006) Stem cells for the treatment of neurological disorders. Nature 441:1094–1096

    Article  CAS  PubMed  Google Scholar 

  • Liu CY, Matsusaki M, Akashi M (2016) Control of vascular network location in millimeter-sized 3D-tissues by micrometer-sized collagen coated cells. Biochem Biophys Res Commun 472:131–136

    Article  CAS  PubMed  Google Scholar 

  • Machado HL, Kittrell FS, Edwards D, White AN, Atkinson RL, Rosen JM, Medina D, Lewis MT (2013) Separation by cell size enriches for mammary stem cell repopulation activity. Stem Cells Transl Med 2:199–203

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Marimuthu M, Rousset N, St-Georges-Robillard A, Lateef MA, Ferland M, Mes-Masson AM, Gervais T (2018) Multi-size spheroid formation using microfluidic funnels. Lab Chip 18:304–314

    Article  CAS  PubMed  Google Scholar 

  • Martin I, Wendt D, Heberer M (2004) The role of bioreactors in tissue engineering. Trends Biotechnol 22:80–86

    Article  CAS  PubMed  Google Scholar 

  • Meng L, Cai F, Zhang Z, Niu L, Jin Q, Yan F, Wu J, Wang Z, Zheng H (2011) Transportation of single cell and microbubbles by phase-shift introduced to standing leaky surface acoustic waves. Biomicrofluidics 5:44104–4410410

    Article  PubMed  CAS  Google Scholar 

  • Mirabella T, MacArthur JW, Cheng D, Ozaki CK, Woo YJ, Yang M, Chen CS (2017) 3D-printed vascular networks direct therapeutic angiogenesis in ischaemia. Nat Biomed Eng 1

  • Morrison SJ, Kimble J (2006) Asymmetric and symmetric stem-cell divisions in development and cancer. Nature 441:1068–1074

    Article  CAS  PubMed  Google Scholar 

  • Müller P, Gaebel R, Lemcke H, Wiekhorst F, Hausburg F, Lang C, Zarniko N, Westphal B, Steinhoff G, David R (2017) Intramyocardial fate and effect of iron nanoparticles co-injected with MACS(®) purified stem cell products. Biomaterials 135:74–84

    Article  PubMed  CAS  Google Scholar 

  • Muller PB, Barnkob R, Jensen MJ, Bruus H (2012) A numerical study of microparticle acoustophoresis driven by acoustic radiation forces and streaming-induced drag forces. Lab Chip 12:4617–4627

    Article  CAS  PubMed  Google Scholar 

  • Murphy CM, Matsiko A, Haugh MG, Gleeson JP, O’Brien FJ (2012) Mesenchymal stem cell fate is regulated by the composition and mechanical properties of collagen-glycosaminoglycan scaffolds. J Mech Behav Biomed Mater 11:53–62

    Article  CAS  PubMed  Google Scholar 

  • Murua A, Portero A, Orive G, Hernández RM, de Castro M, Pedraz JL (2008) Cell microencapsulation technology: towards clinical application. J Control Release 132:76–83

    Article  CAS  PubMed  Google Scholar 

  • Nahmias Y, Schwartz RE, Verfaillie CM, Odde DJ (2005) Laser-guided direct writing for three-dimensional tissue engineering. Biotechnol Bioeng 92:129–136

    Article  CAS  PubMed  Google Scholar 

  • Nam J, Lim H, Kim C, Yoon Kang J, Shin S (2012) Density-dependent separation of encapsulated cells in a microfluidic channel by using a standing surface acoustic wave. Biomicrofluidics 6:24120–2412010

    Article  PubMed  CAS  Google Scholar 

  • Nam J, Lim H, Kim D, Shin S (2011) Separation of platelets from whole blood using standing surface acoustic waves in a microchannel. Lab Chip 11:3361–3364

    Article  CAS  PubMed  Google Scholar 

  • Napolitano AP, Chai P, Dean DM, Morgan JR (2007) Dynamics of the self-assembly of complex cellular aggregates on micromolded nonadhesive hydrogels. Tissue Eng 13:2087–2094

    Article  CAS  PubMed  Google Scholar 

  • Naseer SM, Manbachi A, Samandari M, Walch P, Gao Y, Zhang YS, Davoudi F, Wang W, Abrinia K, Cooper JM et al (2017) Surface acoustic waves induced micropatterning of cells in gelatin methacryloyl (GelMA) hydrogels. Biofabrication 9:015020

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Nichol JW, Koshy ST, Bae H, Hwang CM, Yamanlar S, Khademhosseini A (2010) Cell-laden microengineered gelatin methacrylate hydrogels. Biomaterials 31:5536–5544

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Norotte C, Marga FS, Niklason LE, Forgacs G (2009) Scaffold-free vascular tissue engineering using bioprinting. Biomaterials 30:5910–5917

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • O’Brien FJ (2011) Biomaterials & scaffolds for tissue engineering. Mater Today 14:88–95

    Article  CAS  Google Scholar 

  • Ofek G, Willard VP, Koay EJ, Hu JC, Lin P, Athanasiou KA (2009) Mechanical characterization of differentiated human embryonic stem cells. J Biomech Eng 131:061011

    Article  PubMed  Google Scholar 

  • Orloff ND, Dennis JR, Cecchini M, Schonbrun E, Rocas E, Wang Y, Novotny D, Simmonds RW, Moreland J, Takeuchi I et al (2011) Manipulating particle trajectories with phase-control in surface acoustic wave microfluidics. Biomicrofluidics 5:44107–441079

    Article  PubMed  Google Scholar 

  • Pawell RS, Inglis DW, Barber TJ, Taylor RA (2013) Manufacturing and wetting low-cost microfluidic cell separation devices. Biomicrofluidics 7:56501

    Article  PubMed  Google Scholar 

  • Pethig R (2010) Review article-dielectrophoresis: status of the theory, technology, and applications. Biomicrofluidics 4

  • Pfeiffer MJ, Schalken JA (2010) Stem cell characteristics in prostate cancer cell lines. Eur Urol 57:246–254

    Article  CAS  PubMed  Google Scholar 

  • Piyasena ME, Graves SW (2014) The intersection of flow cytometry with microfluidics and microfabrication. Lab Chip 14:1044–1059

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Plouffe BD, Mahalanabis M, Lewis LH, Klapperich CM, Murthy SK (2012) Clinically relevant microfluidic magnetophoretic isolation of rare-cell populations for diagnostic and therapeutic monitoring applications. Anal Chem 84:1336–1344

    Article  CAS  PubMed  Google Scholar 

  • Poon Z, Lee WC, Guan G, Nyan LM, Lim CT, Han J, Van Vliet KJ (2015) Bone marrow regeneration promoted by biophysically sorted osteoprogenitors from mesenchymal stromal cells. Stem Cells Transl Med 4:56–65

    Article  CAS  PubMed  Google Scholar 

  • Qi A, Friend JR, Yeo LY, Morton DA, McIntosh MP, Spiccia L (2009) Miniature inhalation therapy platform using surface acoustic wave microfluidic atomization. Lab Chip 9:2184–2193

    Article  CAS  PubMed  Google Scholar 

  • Qi A, Yeo L, Friend J, Ho J (2010) The extraction of liquid, protein molecules and yeast cells from paper through surface acoustic wave atomization. Lab Chip 10:470–476

    Article  CAS  PubMed  Google Scholar 

  • Ramón-Azcón J, Ahadian S, Obregón R, Camci-Unal G, Ostrovidov S, Hosseini V, Kaji H, Ino K, Shiku H, Khademhosseini A et al (2012) Gelatin methacrylate as a promising hydrogel for 3D microscale organization and proliferation of dielectrophoretically patterned cells. Lab Chip 12:2959–2969

    Article  PubMed  CAS  Google Scholar 

  • Renaudin A, Chabot V, Grondin E, Aimez V, Charette PG (2010) Integrated active mixing and biosensing using surface acoustic waves (SAW) and surface plasmon resonance (SPR) on a common substrate. Lab Chip 10:111–115

    Article  CAS  PubMed  Google Scholar 

  • Rezk AR, Qi A, Friend JR, Li WH, Yeo LY (2012) Uniform mixing in paper-based microfluidic systems using surface acoustic waves. Lab Chip 12:773–779

    Article  CAS  PubMed  Google Scholar 

  • Richard C, Fakhfouri A, Colditz M, Striggow F, Kronstein-Wiedemann R, Tonn T, Medina-Sánchez M, Schmidt OG, Gemming T, Winkler A (2019) Blood platelet enrichment in mass-producible surface acoustic wave (SAW) driven microfluidic chips. Lab Chip 19:4043–4051

    Article  CAS  PubMed  Google Scholar 

  • Rogers PR, Friend JR, Yeo LY (2010) Exploitation of surface acoustic waves to drive size-dependent microparticle concentration within a droplet. Lab Chip 10:2979–2985

    Article  CAS  PubMed  Google Scholar 

  • Romero D (2016) Breast cancer: CTC heterogeneity is dynamic. Nature reviews Clinical oncology 13:654–654

    Article  CAS  PubMed  Google Scholar 

  • Schirhagl R, Fuereder I, Hall EW, Medeiros BC, Zare RN (2011) Microfluidic purification and analysis of hematopoietic stem cells from bone marrow. Lab Chip 11:3130–3135

    Article  CAS  PubMed  Google Scholar 

  • Schriebl K, Lim S, Choo A, Tscheliessnig A, Jungbauer A (2010) Stem cell separation: a bottleneck in stem cell therapy. Biotechnol J 5:50–61

    Article  CAS  PubMed  Google Scholar 

  • Shao J, Zhang W, Yang T (2015) Using mesenchymal stem cells as a therapy for bone regeneration and repairing. Biol Res 48:62

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Shao S, Gao Y, Xie B, Xie F, Lim SK, Li G (2011) Correction of hyperglycemia in type 1 diabetic models by transplantation of encapsulated insulin-producing cells derived from mouse embryo progenitor. J Endocrinol 208:245–255

    CAS  PubMed  Google Scholar 

  • Shi J, Ahmed D, Mao X, Lin SC, Lawit A, Huang TJ (2009) Acoustic tweezers: patterning cells and microparticles using standing surface acoustic waves (SSAW). Lab Chip 9:2890–2895

    Article  CAS  PubMed  Google Scholar 

  • Shi J, Huang H, Stratton Z, Huang Y, Huang TJ (2009) Continuous particle separation in a microfluidic channel via standing surface acoustic waves (SSAW). Lab Chip 9:3354–3359

    Article  CAS  PubMed  Google Scholar 

  • Shi J, Mao X, Ahmed D, Colletti A, Huang TJ (2008) Focusing microparticles in a microfluidic channel with standing surface acoustic waves (SSAW). Lab Chip 8:221–223

    Article  CAS  PubMed  Google Scholar 

  • Shi J, Yazdi S, Lin SC, Ding X, Chiang IK, Sharp K, Huang TJ (2011) Three-dimensional continuous particle focusing in a microfluidic channel via standing surface acoustic waves (SSAW). Lab Chip 11:2319–2324

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shilton RJ, Travagliati M, Beltram F, Cecchini M (2014) Nanoliter-droplet acoustic streaming via ultra high frequency surface acoustic waves. Adv Mater 26:4941–4946

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Song H, Rosano JM, Wang Y, Garson CJ, Prabhakarpandian B, Pant K, Klarmann GJ, Perantoni A, Alvarez LM, Lai E (2015) Continuous-flow sorting of stem cells and differentiation products based on dielectrophoresis. Lab Chip 15:1320–1328

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Suzuki M, Yasukawa T, Shiku H, Matsue T (2008) Negative dielectrophoretic patterning with different cell types. Biosens Bioelectron 24:1049–1053

    Article  CAS  PubMed  Google Scholar 

  • Tan MK, Friend JR, Yeo LY (2007) Microparticle collection and concentration via a miniature surface acoustic wave device. Lab Chip 7:618–625

    Article  CAS  PubMed  Google Scholar 

  • Tan MK, Friend JR, Yeo LY (2009) Interfacial jetting phenomena induced by focused surface vibrations. Phys Rev Lett 103:024501

    Article  PubMed  CAS  Google Scholar 

  • Tan WH, Takeuchi S (2007) Monodisperse alginate hydrogel microbeads for cell encapsulation. Adv Mater 19:2696–2701

    Article  CAS  Google Scholar 

  • Tasoglu S, Yu CH, Gungordu HI, Guven S, Vural T, Demirci U (2014) Guided and magnetic self-assembly of tunable magnetoceptive gels. Nature communications 5:4702

    Article  CAS  PubMed  Google Scholar 

  • Timmins NE, Dietmair S, Nielsen LK (2004) Hanging-drop multicellular spheroids as a model of tumour angiogenesis. Angiogenesis 7:97–103

    Article  PubMed  Google Scholar 

  • Tomlinson MJ, Tomlinson S, Yang XB, Kirkham J (2013) Cell separation: terminology and practical considerations. J Tissue Eng 4:2041731412472690

    Article  PubMed  Google Scholar 

  • Travagliati M, Shilton RJ, Pagliazzi M, Tonazzini I, Beltram F, Cecchini M (2014) Acoustofluidics and whole-blood manipulation in surface acoustic wave counterflow devices. Anal Chem 86:10633–10638

    Article  CAS  PubMed  Google Scholar 

  • Tsang WP, Shu Y, Kwok PL, Zhang F, Lee KK, Tang MK, Li G, Chan KM, Chan WY, Wan C (2013) CD146+ human umbilical cord perivascular cells maintain stemness under hypoxia and as a cell source for skeletal regeneration. PLoS ONE 8:e76153

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tumbleston JR, Shirvanyants D, Ermoshkin N, Janusziewicz R, Johnson AR, Kelly D, Chen K, Pinschmidt R, Rolland JP, Ermoshkin A et al (2015) Additive manufacturing. Continuous liquid interface production of 3D objects. Science 347:1349–1352

    Article  CAS  PubMed  Google Scholar 

  • Vander Griend DJ, Karthaus WL, Dalrymple S, Meeker A, DeMarzo AM, Isaacs JT (2008) The role of CD133 in normal human prostate stem cells and malignant cancer-initiating cells. Can Res 68:9703–9711

    Article  CAS  Google Scholar 

  • Volpatti LR, Yetisen AK (2014) Commercialization of microfluidic devices. Trends Biotechnol 32:347–350

    Article  CAS  PubMed  Google Scholar 

  • Vykoukal J, Vykoukal DM, Freyberg S, Alt EU, Gascoyne PR (2008) Enrichment of putative stem cells from adipose tissue using dielectrophoretic field-flow fractionation. Lab Chip 8:1386–1393

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang K, Zhou W, Lin Z, Cai F, Li F, Wu J, Meng L, Niu L, Zheng H (2018) Sorting of tumour cells in a microfluidic device by multi-stage surface acoustic waves. Sens Actuators B Chem 258:1174–1183

    Article  CAS  Google Scholar 

  • Wang T, Green R, Nair RR, Howell M, Mohapatra S, Guldiken R, Mohapatra SS (2015) Surface acoustic waves (SAW)-based biosensing for quantification of cell growth in 2D and 3D cultures. Sensors (Basel, Switzerland) 15:32045–32055

    Article  CAS  Google Scholar 

  • Wang X, Wenk E, Zhang X, Meinel L, Vunjak-Novakovic G, Kaplan DL (2009) Growth factor gradients via microsphere delivery in biopolymer scaffolds for osteochondral tissue engineering. Journal of controlled release : official journal of the Controlled Release Society 134:81–90

    Article  CAS  Google Scholar 

  • Wendt D, Riboldi SA, Cioffi M, Martin I (2009) Potential and bottlenecks of bioreactors in 3D cell culture and tissue manufacturing. Adv Mater 21:3352–3367

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Williamson SC, Mitter R, Hepburn AC, Wilson L, Mantilla A, Leung HY, Robson CN, Heer R (2013) Characterisations of human prostate stem cells reveal deficiency in class I UGT enzymes as a novel mechanism for castration-resistant prostate cancer. Br J Cancer 109:950–956

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wixforth A, Strobl C, Gauer C, Toegl A, Scriba J, v Guttenberg, Z. (2004) Acoustic manipulation of small droplets. Anal Bioanal Chem 379:982–991

    Article  CAS  PubMed  Google Scholar 

  • Wu Y, Ao Z, Bin C, Muhsen M, Bondesson M, Lu X, Guo F (2018) Acoustic assembly of cell spheroids in disposable capillaries. Nanotechnology 29:504006

    Article  PubMed  CAS  Google Scholar 

  • Xavier M, Holm SH, Beech JP, Spencer D, Tegenfeldt JO, Oreffo ROC, Morgan H (2019) Label-free enrichment of primary human skeletal progenitor cells using deterministic lateral displacement. Lab Chip 19:513–523

    Article  CAS  PubMed  Google Scholar 

  • Xu T, Jin J, Gregory C, Hickman JJ, Boland T (2005) Inkjet printing of viable mammalian cells. Biomaterials 26:93–99

    Article  PubMed  CAS  Google Scholar 

  • Yager P, Edwards T, Fu E, Helton K, Nelson K, Tam MR, Weigl BH (2006) Microfluidic diagnostic technologies for global public health. Nature 442:412–418

    Article  CAS  PubMed  Google Scholar 

  • Yetisen AK, Akram MS, Lowe CR (2013) Paper-based microfluidic point-of-care diagnostic devices. Lab Chip 13:2210–2251

    Article  CAS  PubMed  Google Scholar 

  • Yin L, Wu Y, Yang Z, Tee CA, Denslin V, Lai Z, Lim CT, Lee EH, Han J (2018) Microfluidic label-free selection of mesenchymal stem cell subpopulation during culture expansion extends the chondrogenic potential in vitro. Lab Chip 18:878–889

    Article  CAS  PubMed  Google Scholar 

  • Yourek, G., Hussain, M.A., and Mao, J.J. (2007). Cytoskeletal changes of mesenchymal stem cells during differentiation. ASAIO journal (American Society for Artificial Internal Organs : 1992) 53, 219–228.

  • Yu VWC, Yusuf RZ, Oki T, Wu J, Saez B, Wang X, Cook C, Baryawno N, Ziller MJ, Lee E et al (2016) Epigenetic memory underlies cell-autonomous heterogeneous behavior of hematopoietic stem cells. Cell 167:1310-1322.e1317

    Article  CAS  PubMed  Google Scholar 

  • Zhang AP, Qu X, Soman P, Hribar KC, Lee JW, Chen S, He S (2012) Rapid fabrication of complex 3D extracellular microenvironments by dynamic optical projection stereolithography. Adv Mater 24:4266–4270

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhao S, Wehner R, Bornhäuser M, Wassmuth R, Bachmann M, Schmitz M (2010) Immunomodulatory properties of mesenchymal stromal cells and their therapeutic consequences for immune-mediated disorders. Stem cells and development 19:607–614

    Article  CAS  PubMed  Google Scholar 

  • Zhu W, Qu X, Zhu J, Ma X, Patel S, Liu J, Wang P, Lai CS, Gou M, Xu Y et al (2017) Direct 3D bioprinting of prevascularized tissue constructs with complex microarchitecture. Biomaterials 124:106–115

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Funding

This work was supported by National Natural Science Foundation of China (No. 31627801), National Natural Science Foundation of China (No. 31800826), and China Postdoctoral Science Foundation Funded Project (No. 2020M671728).

Author information

Author notes

  1. Deming Jiang and Jingwen Liu contributed equally to this work.

Authors and Affiliations

  1. Biosensor National Special Laboratory, Key Laboratory for Biomedical Engineering of Education Ministry, Department of Biomedical Engineering, Zhejiang University, Hangzhou, 310027, China

    Deming Jiang, Yuxiang Pan, Liujing Zhuang & Ping Wang

  2. Department of Gastroenterology, Second Affiliated Hospital, Zhejiang University School of Medicine, Hangzhou, 310009, China

    Jingwen Liu

  3. State Key Laboratory for Sensor Technology, Chinese Academy of Sciences, Shanghai, 200050, China

    Ping Wang

Authors
  1. Deming Jiang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jingwen Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yuxiang Pan
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Liujing Zhuang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Ping Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Ping Wang.

Ethics declarations

Ethical approval

This article does not contain any studies with human participants performed by any of the authors.

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Jiang, D., Liu, J., Pan, Y. et al. Surface acoustic wave (SAW) techniques in tissue engineering. Cell Tissue Res 386, 215–226 (2021). https://doi.org/10.1007/s00441-020-03397-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00441-020-03397-1

Keywords

Search

Navigation