{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,1]],"date-time":"2026-10-01T05:53:02Z","timestamp":1790833982259,"version":"4.1.0"},"reference-count":34,"publisher":"AIP Publishing","issue":"2","funder":[{"name":"Ecole Doctorale E.E.A.","award":["PhD Felloship"],"award-info":[{"award-number":["PhD Felloship"]}]},{"name":"i-MUST"},{"DOI":"10.13039\/501100004794","name":"Centre National de la Recherche Scientifique","doi-asserted-by":"publisher","award":["PEPS MITI"],"award-info":[{"award-number":["PEPS MITI"]}],"id":[{"id":"10.13039\/501100004794","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100006687","name":"Universit\u00e9 Claude Bernard Lyon 1","doi-asserted-by":"publisher","award":["Postdoc Felloship"],"award-info":[{"award-number":["Postdoc Felloship"]}],"id":[{"id":"10.13039\/501100006687","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100009081","name":"Institut National des Sciences Appliqu\u00e9es de Lyon","doi-asserted-by":"publisher","award":["Postdoc Felloship"],"award-info":[{"award-number":["Postdoc Felloship"]}],"id":[{"id":"10.13039\/501100009081","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["pubs.aip.org"],"crossmark-restriction":true},"short-container-title":[],"published-print":{"date-parts":[[2020,3,1]]},"abstract":"<jats:p>Micropipette aspiration, optical tweezers, rheometry, or ecktacytometry have been used to study the shape recovery of healthy human Red Blood Cells (RBCs) and measure associated relaxation times of the order of 100\u2013300\u2009ms. These measurements are in good agreement with the Kelvin\u2013Voigt model, which describes the cell as a visco-elastic material, predicting that its relaxation time only depends on cell intrinsic properties. However, such mechanical solicitation techniques are far from being relevant regarding RBC solicitation in vivo. In this paper, we report for the first time the existence of two different behaviors of the RBC shape recovery while flowing out of a microfluidic constricted channel. The calculation of the viscous stress corresponding to the frontier between the two recovery modes confirms that the RBC resistance to shear \u03bc is the elastic property dominating the transition between the two recovery behaviors. We also quantified associated recovery times \u03c4r and report values as low as 4\u2009ms\u2014which is almost two decades smaller than the typical RBC relaxation time\u2014at high viscosity and flow velocity of the carrier fluid. Although we cannot talk about relaxation time because the cell is never at rest, we believe that the measured shape recovery time arises from the coupling of the cell intrinsic deformability and the hydrodynamic stress. Depending on the flow conditions, the cell mechanics becomes dominant and drives the shape recovery process, allowing the measurement of recovery times of the same order of magnitude than relaxation times previously published. Finally, we demonstrated that the measurement of the shape recovery time can be used to distinguish Plasmodium falciparum (causing malaria) infected RBCs from healthy RBCs.<\/jats:p>","DOI":"10.1063\/5.0005198","type":"journal-article","created":{"date-parts":[[2020,4,28]],"date-time":"2020-04-28T10:45:38Z","timestamp":1588070738000},"update-policy":"https:\/\/doi.org\/10.1063\/aip-crossmark-policy-page","source":"Crossref","is-referenced-by-count":17,"title":["Dual shape recovery of red blood cells flowing out of a microfluidic constriction"],"prefix":"10.1063","volume":"14","author":[{"given":"A.","family":"Amirouche","sequence":"first","affiliation":[{"name":"Universit\u00e9 de Lyon, Institut des Nanotechnologies de Lyon INL-UMR5270 CNRS 1 , Universit\u00e9 Lyon 1, Villeurbanne F-69622,","place":["France"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"J.","family":"Esteves","sequence":"additional","affiliation":[{"name":"Universit\u00e9 de Lyon, Institut des Nanotechnologies de Lyon INL-UMR5270 CNRS 1 , Universit\u00e9 Lyon 1, Villeurbanne F-69622,","place":["France"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"A.","family":"Lavoignat","sequence":"additional","affiliation":[{"name":"Malaria Research Unit, SMITh, Institut de Chimie et de Biochimie Mol\u00e9culaires et Supramol\u00e9culaires ICBMS-UMR5246 CNRS 2 , Universit\u00e9 Lyon 1, Villeurbanne F-69622,","place":["France"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-5735-6759","authenticated-orcid":false,"given":"S.","family":"Picot","sequence":"additional","affiliation":[{"name":"Malaria Research Unit, SMITh, Institut de Chimie et de Biochimie Mol\u00e9culaires et Supramol\u00e9culaires ICBMS-UMR5246 CNRS 2 , Universit\u00e9 Lyon 1, Villeurbanne F-69622,","place":["France"]},{"name":"Institute of Parasitology and Medical Mycology, Croix-Rousse Hospital 3 , Hospices Civils de Lyon, 69004 Lyon,","place":["France"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-7005-5574","authenticated-orcid":false,"given":"R.","family":"Ferrigno","sequence":"additional","affiliation":[{"name":"Universit\u00e9 de Lyon, Institut des Nanotechnologies de Lyon INL-UMR5270 CNRS 1 , Universit\u00e9 Lyon 1, Villeurbanne F-69622,","place":["France"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-3787-1825","authenticated-orcid":false,"given":"M.","family":"Faivre","sequence":"additional","affiliation":[{"name":"Universit\u00e9 de Lyon, Institut des Nanotechnologies de Lyon INL-UMR5270 CNRS 1 , Universit\u00e9 Lyon 1, Villeurbanne F-69622,","place":["France"]}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"317","published-online":{"date-parts":[[2020,4,28]]},"reference":[{"key":"2025100217065287500_c1","doi-asserted-by":"publisher","first-page":"787","DOI":"10.1146\/annurev.bb.23.060194.004035","article-title":"Mechanical properties of the red cell membrane in relation to molecular structure and genetic defects","volume":"23","year":"1994","journal-title":"Annu. Rev. Biophys. Biomol. Struct."},{"key":"2025100217065287500_c2","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1016\/S0006-3495(76)85658-5","article-title":"Membrane viscoelasticity","volume":"16","year":"1976","journal-title":"Biophys. J."},{"key":"2025100217065287500_c3","doi-asserted-by":"publisher","first-page":"101","DOI":"10.1016\/S0006-3495(79)85238-8","article-title":"Red cell extensional recovery and the determination of membrane viscosity","volume":"26","year":"1979","journal-title":"Biophys. J."},{"key":"2025100217065287500_c4","doi-asserted-by":"publisher","first-page":"495","DOI":"10.1016\/S0006-3495(88)82982-5","article-title":"On the measurement of shear elastic moduli and viscosities of erythrocyte plasma membranes by transient deformation in high frequency electric fields","volume":"54","year":"1988","journal-title":"Biophys. J."},{"key":"2025100217065287500_c5","doi-asserted-by":"publisher","first-page":"209","DOI":"10.1146\/annurev.ph.49.030187.001233","article-title":"Erythrocyte membrane elasticity and viscosity","volume":"49","year":"1987","journal-title":"Annu. Rev. Physiol."},{"key":"2025100217065287500_c6","doi-asserted-by":"publisher","first-page":"463","DOI":"10.1016\/S0006-3495(78)85395-8","article-title":"Theoretical and experimental studies on viscoelastic properties of erythrocyte membrane","volume":"24","year":"1978","journal-title":"Biophys. J."},{"key":"2025100217065287500_c7","doi-asserted-by":"publisher","first-page":"115","DOI":"10.1016\/S0006-3495(79)85239-X","article-title":"Thermoelasticity of red blood cell membrane","volume":"26","year":"1979","journal-title":"Biophys. J."},{"key":"2025100217065287500_c8","doi-asserted-by":"publisher","first-page":"63","DOI":"10.1016\/S0006-3495(83)84324-0","article-title":"Red cell and ghost viscoelasticity. effects of haemoglobin concentration and in vivo aging","volume":"43","year":"1983","journal-title":"Biophys. J."},{"key":"2025100217065287500_c9","doi-asserted-by":"publisher","first-page":"35","DOI":"10.1016\/j.mvr.2011.03.004","article-title":"Start-up shape dynamics of red blood cells in microcapillary flow","volume":"82","year":"2011","journal-title":"Microvasc. Res."},{"key":"2025100217065287500_c10","doi-asserted-by":"publisher","first-page":"747","DOI":"10.1016\/S0006-3495(73)86021-7","article-title":"Measurement of the elastic modulus for red cell membrane using a fluid mechanical technique","volume":"13","year":"1973","journal-title":"Biophys. J."},{"key":"2025100217065287500_c11","doi-asserted-by":"publisher","first-page":"3","DOI":"10.1016\/S0076-6879(89)73003-2","article-title":"Structure and deformation properties of red blood cells: Concepts and quantitative methods","volume":"173","year":"1989","journal-title":"Meth. Enzymol."},{"key":"2025100217065287500_c12","doi-asserted-by":"publisher","first-page":"1121","DOI":"10.1182\/blood.V59.6.1121.1121","article-title":"Geometric, osmotic, and membrane mechanical properties of density-separated human red cells","volume":"59","year":"1982","journal-title":"Blood"},{"key":"2025100217065287500_c13","doi-asserted-by":"publisher","first-page":"784","DOI":"10.1016\/S0006-3495(92)81644-2","article-title":"Conformation and elasticity of the isolated red blood cell membrane skeleton","volume":"63","year":"1992","journal-title":"Biophys. J."},{"key":"2025100217065287500_c14","doi-asserted-by":"publisher","first-page":"378","DOI":"10.1038\/307378a0","article-title":"Viscoelastic properties of erythrocyte membranes in high-frequency electric fields","volume":"307","year":"1984","journal-title":"Nature"},{"key":"2025100217065287500_c15","doi-asserted-by":"publisher","first-page":"275","DOI":"10.1182\/blood.V65.2.275.275","article-title":"Age related changes in deformability of human erythrocytes","volume":"65","year":"1985","journal-title":"Blood"},{"key":"2025100217065287500_c16","doi-asserted-by":"publisher","first-page":"283","DOI":"10.1182\/blood.V65.2.283.283","article-title":"Microrheologic investigation of erythrocyte deformability in diabetes mellitus","volume":"65","year":"1985","journal-title":"Blood"},{"key":"2025100217065287500_c17","doi-asserted-by":"publisher","first-page":"563","DOI":"10.1172\/JCI109888","article-title":"Analysis of factors regulating erythrocyte deformability","volume":"66","year":"1980","journal-title":"J. Clin. Invest."},{"key":"2025100217065287500_c18","doi-asserted-by":"publisher","first-page":"11240","DOI":"10.1039\/c2sm26513c","article-title":"Hydrodynamic deformation reveals two coupled modes\/times scales of red blood cell relaxation","volume":"8","year":"2012","journal-title":"Soft Matter"},{"key":"2025100217065287500_c19","doi-asserted-by":"publisher","first-page":"4974","DOI":"10.1021\/ac980656z","article-title":"Rapid prototyping of microfluidic systems in poly(dimethylsiloxane)","volume":"70","year":"2004","journal-title":"Anal. Chem."},{"key":"2025100217065287500_c20","doi-asserted-by":"publisher","first-page":"673","DOI":"10.1126\/science.781840","article-title":"Human malaria parasites in continuous culture","volume":"193","year":"1976","journal-title":"Science"},{"key":"2025100217065287500_c21","doi-asserted-by":"publisher","first-page":"521","DOI":"10.1002\/jcp.1041250323","article-title":"Characterization of permeation pathways in the plasma membrane of human erythrocytes infected with early stages of plasmodium falciparum: Association with parasite development","volume":"125","year":"1985","journal-title":"J. Cell. Physiol."},{"key":"2025100217065287500_c22","doi-asserted-by":"publisher","first-page":"427","DOI":"10.1016\/S0956-5663(97)00109-7","article-title":"Modular concept of a laboratory on a chip for chemical and biochemical analysis","volume":"13","year":"1998","journal-title":"Biosens. Bioelectron."},{"key":"2025100217065287500_c23","doi-asserted-by":"publisher","first-page":"15705","DOI":"10.1038\/s41598-018-33411-0","article-title":"Acoustophoretic orientation of red blood cells for diagnosis of red cell health and pathology","volume":"8","year":"2018","journal-title":"Sci. Rep."},{"key":"2025100217065287500_c24","doi-asserted-by":"publisher","first-page":"4173","DOI":"10.1021\/ac990372u","article-title":"Microchip flow cytometry using electrokinetic focusing","volume":"71","year":"1999","journal-title":"Anal. Chem."},{"key":"2025100217065287500_c25","doi-asserted-by":"publisher","first-page":"3677","DOI":"10.1016\/j.bios.2009.05.037","article-title":"Three-dimensional focusing of red blood cells in microchannel flows for bio-sensing applications","volume":"24","year":"2009","journal-title":"Biosens. Bioelectron."},{"key":"2025100217065287500_c26","first-page":"147","article-title":"Geometrical focusing of cells in a microfluidic device: An approach to separate blood plasma","volume":"43","year":"2006","journal-title":"Biorheology"},{"key":"2025100217065287500_c27","doi-asserted-by":"publisher","first-page":"534","DOI":"10.1039\/C9SM01740B","article-title":"Cross-sectional focusing of red blood cells in a constricted microfluidic channel","volume":"16","year":"2020","journal-title":"Soft Matter"},{"key":"2025100217065287500_c28","doi-asserted-by":"publisher","first-page":"45050","DOI":"10.1039\/C4RA08276A","article-title":"Geometrical alignment for improving cell evaluation in a microchannel with application on multiple myeloma red blood cells","volume":"4","year":"2014","journal-title":"RSC Adv."},{"key":"2025100217065287500_c29","doi-asserted-by":"publisher","first-page":"449","DOI":"10.1039\/C0LC00348D","article-title":"Microfluidics analysis of red blood cell membrane viscosity","volume":"11","year":"2011","journal-title":"Lab Chip"},{"key":"2025100217065287500_c30","doi-asserted-by":"publisher","first-page":"27","DOI":"10.1016\/S0006-3495(83)84319-7","article-title":"Bending elastic modulus of red blood cell membrane derived from buckling instability in micropipette aspiration tests","volume":"43","year":"1983","journal-title":"Biophys. J."},{"issue":"9","key":"2025100217065287500_c31","doi-asserted-by":"publisher","first-page":"941","DOI":"10.1016\/S0006-3495(73)86036-9","article-title":"New membrane concept applied to the analysis of fluid shear- and micropipette-deformed red blood cells","volume":"13","year":"1973","journal-title":"Biophys. J."},{"key":"2025100217065287500_c32","doi-asserted-by":"publisher","first-page":"1145","DOI":"10.1016\/S0006-3495(99)77279-6","article-title":"A new determination of the shear modulus of the human erythrocyte membrane using optical tweezers","volume":"76","year":"1999","journal-title":"Biophys. J."},{"key":"2025100217065287500_c33","doi-asserted-by":"publisher","first-page":"2126","DOI":"10.1016\/j.bpj.2015.03.046","article-title":"Viscoelastic transient of confined red blood cells","volume":"108","year":"2015","journal-title":"Biophys. J."},{"key":"2025100217065287500_c34","doi-asserted-by":"publisher","first-page":"489","DOI":"10.3233\/BIR-1996-33607","article-title":"Determination of red blood cell shape recovery time constant in a couette system by the analysis of light reflectance and ektacytometry","volume":"33","year":"1996","journal-title":"Biorheology"}],"container-title":["Biomicrofluidics"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/pubs.aip.org\/aip\/bmf\/article-pdf\/doi\/10.1063\/5.0005198\/20726796\/024116_1_5.0005198.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"https:\/\/pubs.aip.org\/aip\/bmf\/article-pdf\/doi\/10.1063\/5.0005198\/20726796\/024116_1_5.0005198.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,2]],"date-time":"2025-10-02T21:07:01Z","timestamp":1759439221000},"score":1,"resource":{"primary":{"URL":"https:\/\/pubs.aip.org\/bmf\/article\/14\/2\/024116\/134172\/Dual-shape-recovery-of-red-blood-cells-flowing-out"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2020,3,1]]},"references-count":34,"journal-issue":{"issue":"2","published-print":{"date-parts":[[2020,3,1]]}},"URL":"https:\/\/doi.org\/10.1063\/5.0005198","relation":{},"ISSN":["1932-1058"],"issn-type":[{"value":"1932-1058","type":"electronic"}],"subject":[],"published-other":{"date-parts":[[2020,3]]},"published":{"date-parts":[[2020,3,1]]},"article-number":"024116"}}