Label-free microfluidic enrichment of ring-stage Plasmodium falciparum-infected red blood cells using non-inertial hydrodynamic lift

Malaria Journal

Volumn 13, Issue 1, 2014, Pages

  Geislinger, Thomas M ^a,b,c   Chan, Sherwin ^b   Moll, Kirsten ^b   Wixforth, Achim ^a,c   Wahlgren, Mats ^b   Franke, Thomas ^a,c,d  

^a UNIVERSITY OF AUGSBURG   (Germany)

^b KAROLINSKA INSTITUTE   (Sweden)

^c NANOSYSTEMS INITIATIVE MUNICH NIM   (Germany)

^d UNIVERSITY OF GLASGOW   (United Kingdom)

Author keywords

Enrichment; Erythrocytes; Lab on a chip; Malaria; Microfluidic; Non inertial lift; Plasmodium falciparum; Red blood cells; Ring stage

Indexed keywords

DIMETICONE;

ANIMAL CELL; ARTICLE; CELL SELECTION; CELL WALL; ERYTHROCYTE; HYDRODYNAMICS; INJECTION; LAB ON A CHIP; MICROFLUIDICS; NONHUMAN; PARASITE; PLASMODIUM FALCIPARUM; RESERVOIR; SEPARATION TECHNIQUE; SYRINGE; BLOOD; DEVICES; FLOW CYTOMETRY; HUMAN; ISOLATION AND PURIFICATION; MALARIA FALCIPARUM; MICROFLUIDIC ANALYSIS; PARASITEMIA; PARASITOLOGY; PROCEDURES;

ERYTHROCYTES; FLOW CYTOMETRY; HUMANS; MALARIA, FALCIPARUM; MICROFLUIDIC ANALYTICAL TECHNIQUES; PARASITEMIA; PLASMODIUM FALCIPARUM;

EID: 84907915509     PISSN: None     EISSN: 14752875     Source Type: Journal    
DOI: 10.1186/1475-2875-13-375     Document Type: Article

References (46)

1. WHO, World Malaria Report 2013 Geneva: World Health Organization 2013 284
2. Human malaria parasites in continuous culture. Trager W, Jensen JB, Science 1976 193 673 675 10.1126/science.781840 781840
3. History of the discovery of the malaria parasites and their vectors. Cox FE, Parasit Vectors 2010 3 5 10.1186/1756-3305-3-5 20205846
4. Analysis of the Plasmodium falciparum proteome by high-accuracy mass spectrometry. Lasonder E, Ishihama Y, Andersen JS, Vermunt AMW, Pain A, Sauerwein RW, Eling WMC, Hall N, Waters AP, Stunnenberg HG, Mann M, Nature 2002 419 537 542 10.1038/nature01111 12368870
5. Evolution of adverse changes in stored RBCs. Bennett-Guerrero E, Veldman TH, Doctor A, Telen MJ, Ortel TL, Reid TS, Mulherin MA, Zhu H, Buck RD, Califf RM, McMahon TJ, Proc Natl Acad Sci U S A 2007 104 17063 17068 10.1073/pnas.0708160104 17940021
6. Quantitative imaging of human red blood cells infected with Plasmodium falciparum. Esposito A, Choimet J-B, Skepper JN, Mauritz JMA, Lew VL, Kaminski CF, Tiffert T, Biophys J 2010 99 953 960 10.1016/j.bpj.2010.04.065 20682274
7. Concentration and separation of erythrocytes infected with Plasmodium falciparum by gradient centrifugation. Mrema JE, Campbell GH, Miranda R, Jaramillo AL, Rieckmann KH, Bull World Health Organ 1979 57 133 138 371850
8. Separation and concentration of schizonts of Plasmodium falciparum by Percoll gradients. Rivadeneira EM, Wasserman M, Espinal CT, J Protozool 1983 30 367 370 10.1111/j.1550-7408.1983.tb02932.x 6313915
9. Characterization of permeation pathways appearing in the host membrane of Plasmodium falciparum infected red blood cells. Ginsburg H, Kutner S, Krugliak M, Cabantchik ZI, Mol Biochem Parasitol 1985 14 313 322 10.1016/0166-6851(85)90059-3 3887158
10. Plasmodium falciparum maturation abolishes physiologic red cell deformability. Cranston H, Boylan C, Carroll G, Science 1984 223 400 403 10.1126/science.6362007 6362007
11. Membrane transport in the malaria-infected erythrocyte. Kirk K, Physiol Rev 2001 81 495 537 11274338
12. Purification of mature-stage Plasmodium falciparum by gelatine flotation. Goodyer ID, Johnson J, Eisenthal R, Hayes DJ, Ann Trop Med Parasitol 1994 88 209 211 8067816
13. Concentration and purification by magnetic separation of the erythrocytic stages of all human Plasmodium species. Ribaut C, Berry A, Chevalley S, Reybier K, Morlais I, Parzy D, Nepveu F, Benoit-Vical F, Valentin A, Malar J 2008 7 45 10.1186/1475-2875-7-45 18321384
14. Sorting of circulating tumor cells (MV3-melanoma) and red blood cells using non-inertial lift. Geislinger TM, Franke T, Biomicrofluidics 2013 7 44120 10.1063/1.4818907 24404053
15. Methods in Malaria Research UK and USA: Glasgow and Manassas, Moll K, Kaneko A, Scherf A, Wahlgren M, 6 2013
16. Soft Lithography. Xia Y, Whitesides GM, Annu Rev Mater Sci 1998 28 153 184 10.1146/annurev.matsci.28.1.153
17. Microfluidics: Fluid physics at the nanoliter scale. Squires T, Quake S, Rev Mod Phys 2005 77 977 1026 10.1103/RevModPhys.77.977
18. Role of erythrocyte deformability during capillary wetting. Zhou R, Gordon J, Palmer AF, Chang H-C, Biotechnol Bioeng 2006 93 201 211 10.1002/bit.20672 16302256
19. The lift on a tank-treading ellipsoidal cell in a shear flow. Olla P, J Phys II 1997 7 1533 1540
20. Vesicles and red blood cells in flow: From individual dynamics to rheology. Vlahovska PM, Podgorski T, Misbah C, Comptes Rendus Phys 2009 10 775 789 10.1016/j.crhy.2009.10.001
21. The viscosity of the blood in narrow capillary tubes. Fahraeus R, Lindqvist T, Am J Physiol 1931 96 562 568
22. Hydrodynamic lift of vesicles and red blood cells in flow-from Fåhræus & Lindqvist to microfluidic cell sorting. Geislinger TM, Franke T, Adv Colloid Interface Sci 2014 208C 161 176
23. Tank treading and unbinding of deformable vesicles in shear flow: determination of the lift force. Abkarian M, Lartigue C, Viallat A, Phys Rev Lett 2002 88 068103 11863856
24. Symmetry breaking and cross-streamline migration of three-dimensional vesicles in an axial Poiseuille flow. Farutin A, Misbah C, Phys Rev E 2014 89 042709
25. Fluid vesicles with viscous membranes in shear flow. Noguchi H, Gompper G, Phys Rev Lett 2004 93 258102 15697949
26. Vacillating breathing and tumbling of vesicles under shear flow. Misbah C, Phys Rev Lett 2006 96 028104 16486649
27. Swinging and tumbling of elastic capsules in shear flow. Kessler S, Finken R, Seifert U, J Fluid Mech 2008 605 20
28. Orientation and dynamics of a vesicle in tank-treading motion in shear flow. Kantsler V, Steinberg V, Phys Rev Lett 2005 95 258101 16384512
29. Vesicles and red blood cells in shear flow. Abkarian M, Viallat A, Soft Matter 2008 4 653 10.1039/b716612e
30. Vesicles in Poiseuille flow. Danker G, Vlahovska P, Misbah C, Phys Rev Lett 2009 102 148102 19392488
31. Full dynamics of a red blood cell in shear flow. Dupire J, Socol M, Viallat A, Proc Natl Acad Sci U S A 2012 109 20808 20813 10.1073/pnas.1210236109 23213229
32. The red cell as a fluid droplet: tank tread-like motion of the human erythrocyte membrane in shear flow. Fischer TM, Stöhr-Lissen M, Schmid-Schönbein H, Science 1978 202 894 896 10.1126/science.715448 715448
33. On the energy dissipation in a tank-treading human red blood cell. Fischer TM, Biophys J 1980 32 863 868 10.1016/S0006-3495(80)85022-3 7260306
34. Swinging of red blood cells under shear flow. Abkarian M, Faivre M, Viallat A, Phys Rev Lett 2007 98 188302 17501614
35. Multiscale approach to link red blood cell dynamics, shear viscosity, and ATP release. Forsyth AM, Wan J, Owrutsky PD, Abkarian M, Stone HA, Proc Natl Acad Sci U S A 2011 108 10986 10991 10.1073/pnas.1101315108 21690355
36. Hydrodynamic lift of vesicles under shear flow in microgravity. Callens N, Minetti C, Coupier G, Mader MA, Dubois F, Misbah C, Podgorski T, Europhys Lett 2008 83 24002 10.1209/0295-5075/83/24002
37. Separation of blood cells using hydrodynamic lift. Geislinger TM, Eggart B, Braunmüller S, Schmid L, Franke T, Appl Phys Lett 2012 100 183701 10.1063/1.4709614
38. The malaria-infected red blood cell: structural and functional changes. Cooke BM, Mohandas N, Coppel RL, Adv Parasitol 2001 50 1 86 11757330
39. Antibodies in malarial sera to parasite antigens in the membrane of erythrocytes infected with early asexual stages of Plasmodium falciparum. Perlmann H, Berzins K, Wahlgren M, Carlsson J, Björkman A, Patarroyo ME, Perlmann P, J Exp Med 1984 159 1686 1704 10.1084/jem.159.6.1686 6374012
40. The ring-infected erythrocyte surface antigen (RESA) of Plasmodium falciparum stabilizes spectrin tetramers and suppresses further invasion. Pei X, Guo X, Coppel R, Bhattacharjee S, Haldar K, Gratzer W, Mohandas N, An X, Blood J 2007 110 1036 1042 10.1182/blood-2007-02-076919
41. Effect of plasmodial RESA protein on deformability of human red blood cells harboring Plasmodium falciparum. Mills JP, Diez-Silva M, Quinn DJ, Dao M, Lang MJ, Tan KSW, Lim CT, Milon G, David PH, Mercereau-Puijalon O, Bonnefoy S, Suresh S, Proc Natl Acad Sci U S A 2007 104 9213 9217 10.1073/pnas.0703433104 17517609
42. Microfluidic biomechanical assay for red blood cells parasitized by Plasmodium falciparum. Guo Q, Reiling SJ, Rohrbach P, Ma H, Lab Chip 2012 12 1143 1150 10.1039/c2lc20857a 22318405
43. Refractive index maps and membrane dynamics of human red blood cells parasitized by Plasmodium falciparum. Park Y, Diez-Silva M, Popescu G, Lykotrafitis G, Choi W, Feld MS, Suresh S, Proc Natl Acad Sci U S A 2008 105 13730 13735 10.1073/pnas.0806100105 18772382
44. Deformability based cell margination-A simple microfluidic design for malaria-infected erythrocyte separation. Hou HW, Bhagat AAS, Lin Chong AG, Mao P, Wei Tan KS, Han J, Lim CT, Lab Chip 2010 10 2605 2613 10.1039/c003873c 20689864
45. Retention of Plasmodium falciparum ring-infected erythrocytes in the slow, open microcirculation of the human spleen. Safeukui I, Correas J-M, Brousse V, Hirt D, Deplaine G, Mulé S, Lesurtel M, Goasguen N, Sauvanet A, Couvelard A, Kerneis S, Khun H, Vigan-Womas I, Ottone C, Molina TJ, Tréluyer J-M, Mercereau-Puijalon O, Milon G, David PH, Buffet PA, Blood 2008 112 2520 2528 10.1182/blood-2008-03-146779 18579796
46. Lab-on-a-chip: microfluidics in drug discovery. Dittrich PS, Manz A, Nat Rev Drug Discov 2006 5 210 218 10.1038/nrd1985 16518374