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DOI: 10.1055/s-0040-1710340
A Review of Design Considerations for Hemocompatibility within Microfluidic Systems
Publication History
Publication Date:
30 June 2020 (online)
Abstract
The manipulation of blood within in vitro environments presents a persistent challenge, due to the highly reactive nature of blood, and its multifaceted response to material contact, changes in environmental conditions, and stimulation during handling. Microfluidic Lab-on-Chip systems offer the promise of robust point-of-care diagnostic tools and sophisticated research platforms. The capacity for precise control of environmental and experimental conditions afforded by microfluidic technologies presents unique opportunities that are particularly relevant to research and clinical applications requiring the controlled manipulation of blood. A critical bottleneck impeding the translation of existing Lab-on-Chip technology from laboratory bench to the clinic is the ability to reliably handle relatively small blood samples without negatively impacting blood composition or function. This review explores design considerations critical to the development of microfluidic systems intended for use with whole blood from an engineering perspective. Material hemocompatibility is briefly explored, encompassing common microfluidic device materials, as well as surface modification strategies intended to improve hemocompatibility. Operational hemocompatibility, including shear-induced effects, temperature dependence, and gas interactions are explored, microfluidic sample preparation methodologies are introduced, as well as current techniques for on-chip manipulation of the whole blood. Finally, methods of assessing hemocompatibility are briefly introduced, with an emphasis on primary hemostasis and platelet function.
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References
- 1 Silberring J, Ciborowski P. Biomarker discovery and clinical proteomics. Trends Analyt Chem 2010; 29 (02) 128-128
- 2 Luppa PB, Müller C, Schlichtiger A, Schlebusch H. Point-of-care testing (POCT): current techniques and future perspectives. Trends Analyt Chem 2011; 30 (06) 887-898
- 3 Toner M, Irimia D. Blood-on-a-chip. Annu Rev Biomed Eng 2005; 7: 77-103
- 4 Boyd-Moss M, Baratchi S, Di Venere M, Khoshmanesh K. Self-contained microfluidic systems: a review. Lab Chip 2016; 16 (17) 3177-3192
- 5 Kim D, Finkenstaedt-Quinn S, Hurley KR, Buchman JT, Haynes CL. On-chip evaluation of platelet adhesion and aggregation upon exposure to mesoporous silica nanoparticles. Analyst (Lond) 2014; 139 (05) 906-913
- 6 Brazilek RJ, Tovar-Lopez FJ, Wong AKT. , et al. Application of a strain rate gradient microfluidic device to von Willebrand's disease screening. Lab Chip 2017; 17 (15) 2595-2608
- 7 Melin J, Quake SR. Microfluidic large-scale integration: the evolution of design rules for biological automation. Annu Rev Biophys Biomol Struct 2007; 36: 213-231
- 8 Wang YI, Oleaga C, Long CJ. , et al. Self-contained, low-cost Body-on-a-Chip systems for drug development. Exp Biol Med (Maywood) 2017; 242 (17) 1701-1713
- 9 Du G, Fang Q, den Toonder JM. Microfluidics for cell-based high throughput screening platforms—a review. Anal Chim Acta 2016; 903: 36-50
- 10 Jung W, Han J, Choi JW, Ahn CH. Point-of-care testing (POCT) diagnostic systems using microfluidic lab-on-a-chip technologies. Microelectron Eng 2015; 132: 46-57
- 11 Pandey CM, Augustine S, Kumar S. , et al. Microfluidics based point-of-care diagnostics. Biotechnol J 2018; 13 (01) 1700047
- 12 Weber M, Steinle H, Golombek S. , et al. Blood-contacting biomaterials: in vitro evaluation of the hemocompatibility. Front Bioeng Biotechnol 2018; 6: 99
- 13 Behbahani M, Behr M, Hormes M, Steinseifer U. A review of computational fluid dynamics analysis of blood pumps. Eur J Appl Math 2009; 20 (04) 363-397
- 14 Braune S, Grunze M, Straub A, Jung F. Are there sufficient standards for the in vitro hemocompatibility testing of biomaterials?. Biointerphases 2013; 8 (01) 33
- 15 Bélanger MC, Marois Y. Hemocompatibility, biocompatibility, inflammatory and in vivo studies of primary reference materials low-density polyethylene and polydimethylsiloxane: a review. J Biomed Mater Res 2001; 58 (05) 467-477
- 16 Weisenberg BA, Mooradian DL. Hemocompatibility of materials used in microelectromechanical systems: platelet adhesion and morphology in vitro. J Biomed Mater Res 2002; 60 (02) 283-291
- 17 Williams DF. On the mechanisms of biocompatibility. Biomaterials 2008; 29 (20) 2941-2953
- 18 Naahidi S, Jafari M, Edalat F, Raymond K, Khademhosseini A, Chen P. Biocompatibility of engineered nanoparticles for drug delivery. J Control Release 2013; 166 (02) 182-194
- 19 Lemm W. The Reference Materials of the European Communities: Results of Hemocompatibility Tests. Berlin, Germany: Springer Science & Business Media; 2013
- 20 Maitz MF, Martins MCL, Grabow N. , et al. The blood compatibility challenge. Part 4: surface modification for hemocompatible materials: passive and active approaches to guide blood-material interactions. Acta Biomater 2019; 94: 33-43
- 21 Sperling C, Fischer M, Maitz MF, Werner C. Blood coagulation on biomaterials requires the combination of distinct activation processes. Biomaterials 2009; 30 (27) 4447-4456
- 22 Bi H, Zhong W, Meng S, Kong J, Yang P, Liu B. Construction of a biomimetic surface on microfluidic chips for biofouling resistance. Anal Chem 2006; 78 (10) 3399-3405
- 23 Brash JL, Horbett TA, Latour RA, Tengvall P. The blood compatibility challenge. Part 2: protein adsorption phenomena governing blood reactivity. Acta Biomater 2019; 94: 11-24
- 24 Gokaltun A, Yarmush ML, Asatekin A, Usta OB. Recent advances in nonbiofouling PDMS surface modification strategies applicable to microfluidic technology. Technology (Singap World Sci) 2017; 5 (01) 1-12
- 25 Broos K, De Meyer SF, Feys HB, Vanhoorelbeke K, Deckmyn H. Blood platelet biochemistry. Thromb Res 2012; 129 (03) 245-249
- 26 Afshar-Kharghan V, Li CQ, Khoshnevis-Asl M, López JA. Kozak sequence polymorphism of the glycoprotein (GP) Ibalpha gene is a major determinant of the plasma membrane levels of the platelet GP Ib-IX-V complex. Blood 1999; 94 (01) 186-191
- 27 Toepke MW, Beebe DJ. PDMS absorption of small molecules and consequences in microfluidic applications. Lab Chip 2006; 6 (12) 1484-1486
- 28 Van Oeveren W. Obstacles in haemocompatibility testing. Scientifica 2013; 2013: 392584
- 29 Hildenbrand SL, Lehmann HD, Wodarz R, Ziemer G, Wendel HP. PVC-plasticizer DEHP in medical products: do thin coatings really reduce DEHP leaching into blood?. Perfusion 2005; 20 (06) 351-357
- 30 Haishima Y, Hayashi Y, Yagami T, Nakamura A. Elution of bisphenol-A from hemodialyzers consisting of polycarbonate and polysulfone resins. J Biomed Mater Res 2001; 58 (02) 209-215
- 31 Amoako K, Gbyli R. Improving the hemocompatibility of biomedical polymers. In: Siedlecki CA. , ed. Hemocompatibility of Biomaterials for Clinical Applications. Cambridge, United Kingdom: Elsevier; 2018: 223-252
- 32 Maitz MF. Applications of synthetic polymers in clinical medicine. Biosurf Biotribol 2015; 1 (03) 161-176
- 33 Mukhopadhyay R. When PDMS Isn't the Best. Anal Chem 2007; 79 (09) 3248-3253
- 34 Voskerician G, Shive MS, Shawgo RS. , et al. Biocompatibility and biofouling of MEMS drug delivery devices. Biomaterials 2003; 24 (11) 1959-1967
- 35 Berean K, Ou JZ, Nour M, Latham K. The effect of crosslinking temperature on the permeability of PDMS membranes: evidence of extraordinary CO2 and CH4 gas permeation. Separ Purif Tech 2014; 122: 96-104
- 36 Halldorsson S, Lucumi E, Gómez-Sjöberg R, Fleming RMT. Advantages and challenges of microfluidic cell culture in polydimethylsiloxane devices. Biosens Bioelectron 2015; 63: 218-231
- 37 Fan X, Jia C, Yang J. , et al. A microfluidic chip integrated with a high-density PDMS-based microfiltration membrane for rapid isolation and detection of circulating tumor cells. Biosens Bioelectron 2015; 71: 380-386
- 38 Xiong L, Chen P, Zhou Q. Adhesion promotion between PDMS and glass by oxygen plasma pre-treatment. J Adhes Sci Technol 2014; 28 (11) 1046-1054
- 39 Zang Y, Zang F, Di C-a, Zhu D. Advances of flexible pressure sensors toward artificial intelligence and health care applications. Mater Horiz 2015; 2 (02) 140-156
- 40 Nagahashi K, Teramura Y, Takai M. Stable surface coating of silicone elastomer with phosphorylcholine and organosilane copolymer with cross-linking for repelling proteins. Colloids Surf B Biointerfaces 2015; 134: 384-391
- 41 Agaoglu S, Diep P, Martini M, Kt S, Baday M, Araci IE. Ultra-sensitive microfluidic wearable strain sensor for intraocular pressure monitoring. Lab Chip 2018; 18 (22) 3471-3483
- 42 Berean KJ, Ou JZ, Daeneke T. , et al. 2D MoS2 PDMS nanocomposites for NO2 separation. Small 2015; 11 (38) 5035-5040
- 43 Bodas D, Khan-Malek C. Hydrophilization and hydrophobic recovery of PDMS by oxygen plasma and chemical treatment—an SEM investigation. Sens Actuators B Chem 2007; 123 (01) 368-373
- 44 Shirure VS, George SC. Design considerations to minimize the impact of drug absorption in polymer-based organ-on-a-chip platforms. Lab Chip 2017; 17 (04) 681-690
- 45 Grover WH, Skelley AM, Liu CN, Lagali ET. Monolithic membrane valves and diaphragm pumps for practical large-scale integration into glass microfluidic devices. Sens Actuators B Chem 2003; 89 (03) 315-323
- 46 Shokrieh MM, Mosalmani R, Omidi MJ. A strain-rate dependent micromechanical constitutive model for glass/epoxy composites. Compos Struct 2015; 121: 37-45
- 47 Curcio M, Bonis AD, Teghil R, Santagata A. Composite Thin Films of RKKP Glass With Improved Mechanical Properties and Surface Roughness For Bone-Related Implants. Colophon; 2016: 45
- 48 Lee C-Y, Wang W-T, Liu C-C, Fu L-M. Passive mixers in microfluidic systems: a review. Chem Eng J 2016; 288: 146-160
- 49 Grytsan A, Eriksson TSE, Watton PN, Gasser TC. Growth description for vessel wall adaptation: a thick-walled mixture model of abdominal aortic aneurysm evolution. Materials (Basel) 2017; 10 (09) 994
- 50 Nunes PS, Ohlsson P, Sala OO, Kutter JP. Cyclic olefin polymers: emerging materials for lab-on-a-chip applications. Microfluid Nanofluidics 2010; 9 (2-3): 145-161
- 51 Tsao C-W, DeVoe DL. Bonding of thermoplastic polymer microfluidics. Microfluid Nanofluidics 2009; 6 (01) 1-16
- 52 Becker H, Gärtner C. Polymer microfabrication technologies for microfluidic systems. Anal Bioanal Chem 2008; 390 (01) 89-111
- 53 Bernard M, Jubeli E, Bakar J, Tortolano L, Saunier J, Yagoubi N. Biocompatibility assessment of cyclic olefin copolymers: impact of two additives on cytotoxicity, oxidative stress, inflammatory reactions, and hemocompatibility. J Biomed Mater Res A 2017; 105 (12) 3333-3349
- 54 Roy S, Yue CY. Surface modification of COC microfluidic devices: a comparative study of nitrogen plasma treatment and its advantages over argon and oxygen plasma treatments. Plasma Process Polym 2011; 8 (05) 432-443
- 55 Feng Y, Zhao H, Behl M, Lendlein A, Guo J, Yang D. Grafting of poly(ethylene glycol) monoacrylates on polycarbonateurethane by UV initiated polymerization for improving hemocompatibility. J Mater Sci Mater Med 2013; 24 (01) 61-70
- 56 Ali U, Karim KJBA, Buang NA. A review of the properties and applications of poly (methyl methacrylate) (PMMA). Polym Rev 2015; 55 (04) 678-705
- 57 Genes LI, , V Tolan N, Hulvey MK, Martin RS, Spence DM. Addressing a vascular endothelium array with blood components using underlying microfluidic channels. Lab Chip 2007; 7 (10) 1256-1259
- 58 Neeves KB, Diamond SL. A membrane-based microfluidic device for controlling the flux of platelet agonists into flowing blood. Lab Chip 2008; 8 (05) 701-709
- 59 Alrifaiy A, Lindahl OA, Ramser K. Polymer-based microfluidic devices for pharmacy, biology and tissue engineering. Polymers (Basel) 2012; 4 (03) 1349-1398
- 60 Chianéa T, Cardot PJ, Assidjo E, Monteil J, Clarot I, Krausz P. Field- and flow-dependent trapping of red blood cells on polycarbonate accumulation wall in sedimentation field-flow fractionation. J Chromatogr B Biomed Sci Appl 1999; 734 (01) 91-99
- 61 Toh A, Wang Z, Wang Z. Ambient hot embossing of polycarbonate, poly-methyl methacrylate and cyclic olefin copolymer for microfluidic applications. Paper presented at: 2009 Symposium on Design, Test, Integration & Packaging of MEMS/MOEMS; 2009 IEEE; April 2009; Rome, Italy
- 62 Nge PN, Rogers CI, Woolley AT. Advances in microfluidic materials, functions, integration, and applications. Chem Rev 2013; 113 (04) 2550-2583
- 63 Sajiki J, Yonekubo J. Leaching of bisphenol A (BPA) to seawater from polycarbonate plastic and its degradation by reactive oxygen species. Chemosphere 2003; 51 (01) 55-62
- 64 Vandenberg LN, Hauser R, Marcus M, Olea N, Welshons WV. Human exposure to bisphenol A (BPA). Reprod Toxicol 2007; 24 (02) 139-177
- 65 Lu B, Xu T, Zheng S, Goldkom A, Tai Y-C. Parylene membrane slot filter for the capture, analysis and culture of viable circulating tumor cells. Paper presented at: 2010 IEEE 23rd International Conference on Micro Electro Mechanical Systems (MEMS 2010); January 2010; Wanchai, Hong Kong
- 66 Yu L, Kim BJ, Meng E. Chronically implanted pressure sensors: challenges and state of the field. Sensors (Basel) 2014; 14 (11) 20620-20644
- 67 Trantidou T, Prodromakis T, Toumazou C. Oxygen plasma induced hydrophilicity of Parylene-C thin films. Appl Surf Sci 2012; 261: 43-51
- 68 Chang TY, Yadav VG, De Leo S. , et al. Cell and protein compatibility of parylene-C surfaces. Langmuir 2007; 23 (23) 11718-11725
- 69 Friend J, Yeo L. Fabrication of microfluidic devices using polydimethylsiloxane. Biomicrofluidics 2010; 4 (02) 026502
- 70 Reynolds M, Elias A, Elliott DG, Backhouse C. Variation of thermal and mechanical properties of KMPR due to processing parameters. J Micromech Microeng 2012; 22 (12) 125023
- 71 Prokop C, Schoenhardt S, Mahmud T, Mitchell A. , et al. Bonding of SU-8 films onto KMPR structures for microfluidic, air-suspended photonic and optofluidic applications. J Micromech Microeng 2016; 26 (05) 055001
- 72 Convert L, Baril FG, Boisselle V. , et al. Blood compatible microfluidic system for pharmacokinetic studies in small animals. Lab Chip 2012; 12 (22) 4683-4692
- 73 Convert L, Chabot V, Zermatten PJ, Karnutsch C. Passivation of KMPR microfluidic channels with bovine serum albumin (BSA) for improved hemocompatibility characterized with metal-clad waveguides. Sens Actuators B Chem 2012; 173: 447-454
- 74 Werner C, Maitz MF, Sperling C. Current strategies towards hemocompatible coatings. J Mater Chem 2007; 17 (32) 3376-3384
- 75 Fischer M, Maitz MF, Werner C. Coatings for biomaterials to improve hemocompatibility. In: Siedlecki CA. , ed. Hemocompatibility of Biomaterials for Clinical Applications. Cambridge, United Kingdom: Elsevier; 2018: 163-190
- 76 Hasan A, Pandey LM. Polymers, surface-modified polymers, and self-assembled monolayers as surface-modifying agents for biomaterials. Polym Plast Technol Eng 2015; 54 (13) 1358-1378
- 77 Goodman SL, Cooper SL, Albrecht RM. The effects of substrate-adsorbed albumin on platelet spreading. J Biomater Sci Polym Ed 1991; 2 (02) 147-159
- 78 Pillai GJ, Greeshma MM, Menon D. Impact of poly(lactic-co-glycolic acid) nanoparticle surface charge on protein, cellular and haematological interactions. Colloids Surf B Biointerfaces 2015; 136: 1058-1066
- 79 Rabe M, Verdes D, Seeger S. Understanding protein adsorption phenomena at solid surfaces. Adv Colloid Interface Sci 2011; 162 (1-2): 87-106
- 80 Zarur AJ, Mehenti NZ, Heibel AT, Ying JY. Phase behavior, structure, and applications of reverse microemulsions stabilized by nonionic surfactants. Langmuir 2000; 16 (24) 9168-9176
- 81 Wong I, Ho C-M. Surface molecular property modifications for poly(dimethylsiloxane) (PDMS) based microfluidic devices. Microfluid Nanofluidics 2009; 7 (03) 291-306
- 82 Abdallah B, Ros A. Surface coatings for microfluidic-based biomedical devices. In: Li XJ, Zhou Y. , eds. Microfluidic Devices for Biomedical Applications. Elsevier; 2013: 63-99
- 83 Jenkins CS, Packham MA, Kinlough-Rathbone RL, Mustard JF. Interactions of polylysine with platelets. Blood 1971; 37 (04) 395-412
- 84 Zhong D, Jiao Y, Zhang Y. , et al. Effects of the gene carrier polyethyleneimines on structure and function of blood components. Biomaterials 2013; 34 (01) 294-305
- 85 Chou T-C, Fu E, Wu CJ, Yeh JH. Chitosan enhances platelet adhesion and aggregation. Biochem Biophys Res Commun 2003; 302 (03) 480-483
- 86 Tosatti S, De Paul SM, Askendal A. , et al. Peptide functionalized poly(L-lysine)-g-poly(ethylene glycol) on titanium: resistance to protein adsorption in full heparinized human blood plasma. Biomaterials 2003; 24 (27) 4949-4958
- 87 Dong P, Hao W, Wang Z, Wang T. Fabrication and biocompatibility of polyethyleneimine/heparin self-assembly coating on NiTi alloy. Thin Solid Films 2008; 516 (16) 5168-5171
- 88 Balan V, Verestiuc L. Strategies to improve chitosan hemocompatibility: a review. Eur Polym J 2014; 53: 171-188
- 89 Blaszykowski C, Sheikh S, Thompson M. Surface chemistry to minimize fouling from blood-based fluids. Chem Soc Rev 2012; 41 (17) 5599-5612
- 90 Yu ZTF, Joseph JG, Liu SX. , et al. Centrifugal microfluidics for sorting immune cells from whole blood. Sens Actuators B Chem 2017; 245: 1050-1061
- 91 Ulman A. Formation and structure of self-assembled monolayers. Chem Rev 1996; 96 (04) 1533-1554
- 92 Love JC, Estroff LA, Kriebel JK, Nuzzo RG, Whitesides GM. Self-assembled monolayers of thiolates on metals as a form of nanotechnology. Chem Rev 2005; 105 (04) 1103-1169
- 93 Sperling C, Schweiss RB, Streller U, Werner C. In vitro hemocompatibility of self-assembled monolayers displaying various functional groups. Biomaterials 2005; 26 (33) 6547-6557
- 94 de los Santos Pereira A, Sheikh S, Blaszykowski C. , et al. Antifouling polymer brushes displaying antithrombogenic surface properties. Biomacromolecules 2016; 17 (03) 1179-1185
- 95 Hasan A, Pandey L. Self-assembled monolayers in biomaterials. In: Narayan R. , ed. Nanobiomaterials. Cambridge, United Kingdom: Elsevier; 2018: 137-178
- 96 Kidambi S, Chan C, Lee I. Selective depositions on polyelectrolyte multilayers: self-assembled monolayers of m-dPEG acid as molecular template. J Am Chem Soc 2004; 126 (14) 4697-4703
- 97 Zhang S. Biological and Biomedical Coatings Handbook: Applications. Boca Raton, FL: CRC Press; 2016
- 98 Leung JM, Berry LR, Atkinson HM. , et al. Surface modification of poly (dimethylsiloxane) with a covalent antithrombin–heparin complex for the prevention of thrombosis: use of polydopamine as bonding agent. J Mater Chem B Mater Biol Med 2015; 3 (29) 6032-6036
- 99 Thorslund S, Sanchez J, Larsson R, Nikolajeff F, Bergquist J. Bioactive heparin immobilized onto microfluidic channels in poly(dimethylsiloxane) results in hydrophilic surface properties. Colloids Surf B Biointerfaces 2005; 46 (04) 240-247
- 100 Jackson SP. The growing complexity of platelet aggregation. Blood 2007; 109 (12) 5087-5095
- 101 Casa LDC, Deaton DH, Ku DN. Role of high shear rate in thrombosis. J Vasc Surg 2015; 61 (04) 1068-1080
- 102 Jafarnejad M, Cromer WE, Kaunas RR, Zhang SL, Zawieja DC, Moore Jr JE. Measurement of shear stress-mediated intracellular calcium dynamics in human dermal lymphatic endothelial cells. Am J Physiol Heart Circ Physiol 2015; 308 (07) H697-H706
- 103 Philo JS, Arakawa T. Mechanisms of protein aggregation. Curr Pharm Biotechnol 2009; 10 (04) 348-351
- 104 Maa YF, Hsu CC. Protein denaturation by combined effect of shear and air-liquid interface. Biotechnol Bioeng 1997; 54 (06) 503-512
- 105 Tsai H-M, Sussman II, Nagel RL. Shear stress enhances the proteolysis of von Willebrand factor in normal plasma. Blood 1994; 83 (08) 2171-2179
- 106 Schneider SW, Nuschele S, Wixforth A. , et al. Shear-induced unfolding triggers adhesion of von Willebrand factor fibers. Proc Natl Acad Sci U S A 2007; 104 (19) 7899-7903
- 107 Ruggeri ZM. Platelet adhesion under flow. Microcirculation 2009; 16 (01) 58-83
- 108 Nesbitt WS, Westein E, Tovar-Lopez FJ. , et al. A shear gradient-dependent platelet aggregation mechanism drives thrombus formation. Nat Med 2009; 15 (06) 665-673
- 109 Lanotte L, Mauer J, Mendez S. , et al. Red cells' dynamic morphologies govern blood shear thinning under microcirculatory flow conditions. Proc Natl Acad Sci U S A 2016; 113 (47) 13289-13294
- 110 Yilmaz F, Gundogdu MY. A critical review on blood flow in large arteries; relevance to blood rheology, viscosity models, and physiologic conditions. Korea-Australia Rheol J 2008; 20 (04) 197-211
- 111 Arwatz G, Smits AJ. A viscoelastic model of shear-induced hemolysis in laminar flow. Biorheology 2013; 50 (1-2): 45-55
- 112 Leverett LB, Hellums JD, Alfrey CP, Lynch EC. Red blood cell damage by shear stress. Biophys J 1972; 12 (03) 257-273
- 113 Horobin JT, Sabapathy S, Simmonds MJ. Repetitive supra-physiological shear stress impairs red blood cell deformability and induces hemolysis. Artif Organs 2017; 41 (11) 1017-1025
- 114 Zhao H, Shaqfeh ES. Shear-induced platelet margination in a microchannel. Phys Rev E Stat Nonlin Soft Matter Phys 2011; 83 (6 Pt 1): 061924
- 115 Barshtein G, Wajnblum D, Yedgar S. Kinetics of linear rouleaux formation studied by visual monitoring of red cell dynamic organization. Biophys J 2000; 78 (05) 2470-2474
- 116 Moazzam F, DeLano FA, Zweifach BW, Schmid-Schönbein GW. The leukocyte response to fluid stress. Proc Natl Acad Sci U S A 1997; 94 (10) 5338-5343
- 117 Coughlin MF, Schmid-Schönbein GW. Pseudopod projection and cell spreading of passive leukocytes in response to fluid shear stress. Biophys J 2004; 87 (03) 2035-2042
- 118 Lawrence MB, Kansas GS, Kunkel EJ, Ley K. Threshold levels of fluid shear promote leukocyte adhesion through selectins (CD62L,P,E). J Cell Biol 1997; 136 (03) 717-727
- 119 Sperandio M, Pickard J, Unnikrishnan S, Acton ST, Ley K. Analysis of leukocyte rolling in vivo and in vitro. Methods Enzymol 2006; 416: 346-371
- 120 Lu H, Soria C, Cramer EM. , et al. Temperature dependence of plasmin-induced activation or inhibition of human platelets. Blood 1991; 77 (05) 996-1005
- 121 Blok SLJ, Engels GE, van Oeveren W. In vitro hemocompatibility testing: the importance of fresh blood. Biointerphases 2016; 11 (02) 029802
- 122 Wolberg AS, Meng ZH, Monroe III DM, Hoffman M. A systematic evaluation of the effect of temperature on coagulation enzyme activity and platelet function. J Trauma 2004; 56 (06) 1221-1228
- 123 Kermode JC, Zheng Q, Milner EP. Marked temperature dependence of the platelet calcium signal induced by human von Willebrand factor. Blood 1999; 94 (01) 199-207
- 124 Waugh R, Evans EA. Thermoelasticity of red blood cell membrane. Biophys J 1979; 26 (01) 115-131
- 125 Kim J, Lee H, Shin S. Advances in the measurement of red blood cell deformability: a brief review. J Cell Biotechnol 2015; 1 (01) 63-79
- 126 Neumann F-J, Schmid-Schönbein H, Ohlenbusch H. Temperature-dependence of red cell aggregation. Pflugers Arch 1987; 408 (05) 524-530
- 127 Lim HJ, Lee YJ, Nam JH, Chung S, Shin S. Temperature-dependent threshold shear stress of red blood cell aggregation. J Biomech 2010; 43 (03) 546-550
- 128 Rosina J, Kvasnák E, Suta D, Kolárová H, Málek J, Krajci L. Temperature dependence of blood surface tension. Physiol Res 2007; 56 (01) (Suppl. 01) S93-S98
- 129 Jaspard F, Nadi M. Dielectric properties of blood: an investigation of temperature dependence. Physiol Meas 2002; 23 (03) 547-554
- 130 Bradley AF, Severinghaus JW, Stupfel M. Effect of temperature on PCO2 and PO2 of blood in vitro. J Appl Physiol 1956; 9 (02) 201-204
- 131 Eckmann DM, Bowers S, Stecker M, Cheung AT. Hematocrit, volume expander, temperature, and shear rate effects on blood viscosity. Anesth Analg 2000; 91 (03) 539-545
- 132 Pinho D, Rodrigues RO, Faustino V, Yaginuma T, Exposto J, Lima R. Red blood cells radial dispersion in blood flowing through microchannels: the role of temperature. J Biomech 2016; 49 (11) 2293-2298
- 133 Biswas CK, Ramos JM, Agroyannis B, Kerr DN. Blood gas analysis: effect of air bubbles in syringe and delay in estimation. Br Med J (Clin Res Ed) 1982; 284 (6320): 923-927
- 134 Haycox CL, Ratner BD. In vitro platelet interactions in whole human blood exposed to biomaterial surfaces: insights on blood compatibility. J Biomed Mater Res 1993; 27 (09) 1181-1193
- 135 Kalman PG, McCullough DA, Ward CA. Evacuation of microscopic air bubbles from Dacron reduces complement activation and platelet aggregation. J Vasc Surg 1990; 11 (04) 591-598
- 136 Gong J, Larsson R, Ekdahl KN, Mollnes TE, Nilsson U, Nilsson B. Tubing loops as a model for cardiopulmonary bypass circuits: both the biomaterial and the blood-gas phase interfaces induce complement activation in an in vitro model. J Clin Immunol 1996; 16 (04) 222-229
- 137 Elam J-H, Nygren H. Adsorption of coagulation proteins from whole blood on to polymer materials: relation to platelet activation. Biomaterials 1992; 13 (01) 3-8
- 138 Mu X, Zheng W, Sun J, Zhang W, Jiang X. Microfluidics for manipulating cells. Small 2013; 9 (01) 9-21
- 139 Kim L, Toh YC, Voldman J, Yu H. A practical guide to microfluidic perfusion culture of adherent mammalian cells. Lab Chip 2007; 7 (06) 681-694
- 140 Karlsson JM, Gazin M, Laakso S. , et al. Active liquid degassing in microfluidic systems. Lab Chip 2013; 13 (22) 4366-4373
- 141 Monahan J, Gewirth AA, Nuzzo RG. A method for filling complex polymeric microfluidic devices and arrays. Anal Chem 2001; 73 (13) 3193-3197
- 142 Lochovsky C, Yasotharan S, Günther A. Bubbles no more: in-plane trapping and removal of bubbles in microfluidic devices. Lab Chip 2012; 12 (03) 595-601
- 143 Forget AL, Dombrowski CC, Amitani I, Kowalczykowski SC. Exploring protein-DNA interactions in 3D using in situ construction, manipulation and visualization of individual DNA dumbbells with optical traps, microfluidics and fluorescence microscopy. Nat Protoc 2013; 8 (03) 525-538
- 144 Mason TJ, Mason TJ. Sonochemistry. Vol. 2. New York, NY: Oxford University Press; 1999
- 145 Shatalov V, Noga I, Zinchenko A. Degassing of bioliquids in low electromagnetic fields. Elec J Biol 2010;6(03):67–72
- 146 Xu L, Lee H, Jetta D, Oh KW. Vacuum-driven power-free microfluidics utilizing the gas solubility or permeability of polydimethylsiloxane (PDMS). Lab Chip 2015; 15 (20) 3962-3979
- 147 Lee C-J, Hsu Y-H. Vacuum pouch microfluidic system and its application for thin-film micromixers. Lab Chip 2019; 19 (17) 2834-2843
- 148 Song Q, Sun J, Mu Y, Xu Y. A new method for polydimethylsiloxane (PDMS) microfluidic chips to maintain vacuum-driven power using Parylene C. Sens Actuators B Chem 2018; 256: 1122-1130
- 149 Dimov IK, Basabe-Desmonts L, Garcia-Cordero JL. , et al. Stand-alone self-powered integrated microfluidic blood analysis system (SIMBAS). Lab Chip 2011; 11 (05) 845-850
- 150 Sung JH, Shuler ML. Prevention of air bubble formation in a microfluidic perfusion cell culture system using a microscale bubble trap. Biomed Microdevices 2009; 11 (04) 731-738
- 151 Zheng W, Wang Z, Zhang W, Jiang X. A simple PDMS-based microfluidic channel design that removes bubbles for long-term on-chip culture of mammalian cells. Lab Chip 2010; 10 (21) 2906-2910
- 152 Wang Y, Lee D, Zhang L. , et al. Systematic prevention of bubble formation and accumulation for long-term culture of pancreatic islet cells in microfluidic device. Biomed Microdevices 2012; 14 (02) 419-426
- 153 Xu J, Vaillant R, Attinger D. Use of a porous membrane for gas bubble removal in microfluidic channels: physical mechanisms and design criteria. Microfluid Nanofluidics 2010; 9 (4-5): 765-772
- 154 Skelley AM, Voldman J. An active bubble trap and debubbler for microfluidic systems. Lab Chip 2008; 8 (10) 1733-1737
- 155 Kang JH, Kim YC, Park J-K. Analysis of pressure-driven air bubble elimination in a microfluidic device. Lab Chip 2008; 8 (01) 176-178
- 156 Liu C, Thompson JA, Bau HH. A membrane-based, high-efficiency, microfluidic debubbler. Lab Chip 2011; 11 (09) 1688-1693
- 157 Braune S, Walter M, Schulze F, Lendlein A, Jung F. Changes in platelet morphology and function during 24 hours of storage. Clin Hemorheol Microcirc 2014; 58 (01) 159-170
- 158 Seyfert U, Jung F. Criteria and principles of in vitro hemocompatibility testing according to the ISO 10993 (4). Transfus Med Hemother 2000; 27 (06) 317-322
- 159 Tripathi S, Kumar YVBV, Prabhakar A, Joshi SS, Agarwal A. Passive blood plasma separation at the microscale: a review of design principles and microdevices. J Micromech Microeng 2015; 25 (08) 083001
- 160 Fernández Gavela A, Grajales García D, Ramirez JC, Lechuga LM. Last advances in silicon-based optical biosensors. Sensors (Basel) 2016; 16 (03) 285
- 161 Rackus DG, Shamsi MH, Wheeler AR. Electrochemistry, biosensors and microfluidics: a convergence of fields. Chem Soc Rev 2015; 44 (15) 5320-5340
- 162 Sonker M, Sahore V, Woolley AT. Recent advances in microfluidic sample preparation and separation techniques for molecular biomarker analysis: a critical review. Anal Chim Acta 2017; 986: 1-11
- 163 Femia EA, Scavone M, Lecchi A, Cattaneo M. Effect of platelet count on platelet aggregation measured with impedance aggregometry (Multiplate™ analyzer) and with light transmission aggregometry. J Thromb Haemost 2013; 11 (12) 2193-2196
- 164 Paniccia R, Priora R, Liotta AA, Abbate R. Platelet function tests: a comparative review. Vasc Health Risk Manag 2015; 11: 133-148
- 165 van Werkum JW, van der Stelt CA, Seesing TH, Hackeng CM, ten Berg JM. A head-to-head comparison between the VerifyNow P2Y12 assay and light transmittance aggregometry for monitoring the individual platelet response to clopidogrel in patients undergoing elective percutaneous coronary intervention. J Thromb Haemost 2006; 4 (11) 2516-2518
- 166 Seah YFS, Hu H, Merten CA. Microfluidic single-cell technology in immunology and antibody screening. Mol Aspects Med 2018; 59: 47-61
- 167 Shields IV CW, Reyes CD, López GP. Microfluidic cell sorting: a review of the advances in the separation of cells from debulking to rare cell isolation. Lab Chip 2015; 15 (05) 1230-1249
- 168 Kersaudy-Kerhoas M, Sollier E. Micro-scale blood plasma separation: from acoustophoresis to egg-beaters. Lab Chip 2013; 13 (17) 3323-3346
- 169 Mielczarek WS, Obaje EA, Bachmann TT, Kersaudy-Kerhoas M. Microfluidic blood plasma separation for medical diagnostics: is it worth it?. Lab Chip 2016; 16 (18) 3441-3448
- 170 Yu ZTF, Aw Yong KM, Fu J. Microfluidic blood cell sorting: now and beyond. Small 2014; 10 (09) 1687-1703
- 171 Maria MS, Chandra T, Sen A. Capillary flow-driven blood plasma separation and on-chip analyte detection in microfluidic devices. Microfluid Nanofluidics 2017; 21 (04) 72
- 172 VanDelinder V, Groisman A. Separation of plasma from whole human blood in a continuous cross-flow in a molded microfluidic device. Anal Chem 2006; 78 (11) 3765-3771
- 173 Mach AJ, Di Carlo D. Continuous scalable blood filtration device using inertial microfluidics. Biotechnol Bioeng 2010; 107 (02) 302-311
- 174 Lenshof A, Ahmad-Tajudin A, Järås K. , et al. Acoustic whole blood plasmapheresis chip for prostate specific antigen microarray diagnostics. Anal Chem 2009; 81 (15) 6030-6037
- 175 Szydzik C, Khoshmanesh K, Mitchell A, Karnutsch C. Microfluidic platform for separation and extraction of plasma from whole blood using dielectrophoresis. Biomicrofluidics 2015; 9 (06) 064120
- 176 Heath JR, Ribas A, Mischel PS. Single-cell analysis tools for drug discovery and development. Nat Rev Drug Discov 2016; 15 (03) 204-216
- 177 Wu J, Lin J-M. Microfluidic technology for single-cell capture and isolation. In: Microfluidics for Single-Cell Analysis. Singapore: Springer; 2019: 27-51
- 178 Mazutis L, Gilbert J, Ung WL, Weitz DA, Griffiths AD, Heyman JA. Single-cell analysis and sorting using droplet-based microfluidics. Nat Protoc 2013; 8 (05) 870-891
- 179 Prakadan SM, Shalek AK, Weitz DA. Scaling by shrinking: empowering single-cell 'omics' with microfluidic devices. Nat Rev Genet 2017; 18 (06) 345-361
- 180 Song Y, Tian T, Shi Y. , et al. Enrichment and single-cell analysis of circulating tumor cells. Chem Sci (Camb) 2017; 8 (03) 1736-1751
- 181 Gossett DR, Weaver WM, Mach AJ. , et al. Label-free cell separation and sorting in microfluidic systems. Anal Bioanal Chem 2010; 397 (08) 3249-3267
- 182 Kuntaegowdanahalli SS, Bhagat AA, Kumar G, Papautsky I. Inertial microfluidics for continuous particle separation in spiral microchannels. Lab Chip 2009; 9 (20) 2973-2980
- 183 Yan S, Zhang J, Yuan D, Li W. Hybrid microfluidics combined with active and passive approaches for continuous cell separation. Electrophoresis 2017; 38 (02) 238-249
- 184 Li X, Soler M, Szydzik C. , et al. Label-free optofluidic nanobiosensor enables real-time analysis of single-cell cytokine secretion. Small 2018; 14 (26) e1800698
- 185 Joensson HN, Samuels ML, Brouzes ER. , et al. Detection and analysis of low-abundance cell-surface biomarkers using enzymatic amplification in microfluidic droplets. Angew Chem Int Ed Engl 2009; 48 (14) 2518-2521
- 186 Sinkala E, Sollier-Christen E, Renier C. , et al. Profiling protein expression in circulating tumour cells using microfluidic western blotting. Nat Commun 2017; 8: 14622
- 187 Kaiser M, Jug F, Julou T. , et al. Monitoring single-cell gene regulation under dynamically controllable conditions with integrated microfluidics and software. Nat Commun 2018; 9 (01) 212
- 188 Kimmerling RJ, Lee Szeto G, Li JW. , et al. A microfluidic platform enabling single-cell RNA-seq of multigenerational lineages. Nat Commun 2016; 7: 10220
- 189 Huang L, Bian S, Cheng Y. , et al. Microfluidics cell sample preparation for analysis: advances in efficient cell enrichment and precise single cell capture. Biomicrofluidics 2017; 11 (01) 011501
- 190 Antfolk M, Laurell T. Continuous flow microfluidic separation and processing of rare cells and bioparticles found in blood—a review. Anal Chim Acta 2017; 965: 9-35
- 191 Shen Y, Yalikun Y, Tanaka Y. Recent advances in microfluidic cell sorting systems. Sens Actuators B Chem 2018; 282: 268-281
- 192 Magnusson C, Augustsson P, Lenshof A, Ceder Y, Laurell T, Lilja H. Clinical-scale cell-surface-marker independent acoustic microfluidic enrichment of tumor cells from blood. Anal Chem 2017; 89 (22) 11954-11961
- 193 Quang LD, Thuy HTT, Tung BT. , et al. Dielectrophoresis microfluidic enrichment platform with built-in capacitive sensor for rare tumor cell detection. Biochip J 2018; 12 (02) 114-122
- 194 Lin S, Zhi X, Chen D. , et al. A flyover style microfluidic chip for highly purified magnetic cell separation. Biosens Bioelectron 2019; 129: 175-181
- 195 Keloth A, Anderson O, Risbridger D, Paterson L. Single cell isolation using optical tweezers. Micromachines (Basel) 2018; 9 (09) 434
- 196 Kim G-Y, Han J-I, Park J-K. Inertial microfluidics-based cell sorting. Biochip J 2018; 12 (04) 257-267
- 197 Khetani S, Mohammadi M, Nezhad AS. Filter-based isolation, enrichment, and characterization of circulating tumor cells. Biotechnol Bioeng 2018; 115 (10) 2504-2529
- 198 Zinggeler M, Brandstetter T, Rühe J. Biophysical insights on the enrichment of cancer cells from whole blood by (affinity) filtration. Sci Rep 2019; 9 (01) 1246
- 199 Yamada H, Yoshida Y, Terada N, Hagihara S, Komatsu T, Terasawa A. Fabrication of gravity-driven microfluidic device. Rev Sci Instrum 2008; 79 (12) 124301
- 200 Cheng Y, Ye X, Ma Z, Xie S, Wang W. High-throughput and clogging-free microfluidic filtration platform for on-chip cell separation from undiluted whole blood. Biomicrofluidics 2016; 10 (01) 014118
- 201 Brassard D, Geissler M, Descarreaux M. , et al. Extraction of nucleic acids from blood: unveiling the potential of active pneumatic pumping in centrifugal microfluidics for integration and automation of sample preparation processes. Lab Chip 2019; 19 (11) 1941-1952
- 202 Travagliati M, Shilton RJ, Pagliazzi M, Tonazzini I, Beltram F, Cecchini M. Acoustofluidics and whole-blood manipulation in surface acoustic wave counterflow devices. Anal Chem 2014; 86 (21) 10633-10638
- 203 Park J, Park J-K. Finger-actuated microfluidic device for the blood cross-matching test. Lab Chip 2018; 18 (08) 1215-1222
- 204 Cai H, Stott MA, Ozcelik D, Parks JW, Hawkins AR, Schmidt H. On-chip wavelength multiplexed detection of cancer DNA biomarkers in blood. Biomicrofluidics 2016; 10 (06) 064116
- 205 Li J, Chang KW, Wang CH, Yang CH, Shiesh SC, Lee GB. On-chip, aptamer-based sandwich assay for detection of glycated hemoglobins via magnetic beads. Biosens Bioelectron 2016; 79: 887-893
- 206 Szydzik C, Brazilek RJ, Khoshmanesh K. , et al. Elastomeric microvalve geometry affects haemocompatibility. Lab Chip 2018; 18 (12) 1778-1792
- 207 Szydzik C, Brazilek RJ, Akbaridoust F. , et al. active micropump-mixer for rapid antiplatelet drug screening in whole blood. Anal Chem 2019; 91 (16) 10830-10839
- 208 Zhong JF, Chen Y, Marcus JS. , et al. A microfluidic processor for gene expression profiling of single human embryonic stem cells. Lab Chip 2008; 8 (01) 68-74
- 209 King KR, Wang S, Irimia D, Jayaraman A, Toner M, Yarmush ML. A high-throughput microfluidic real-time gene expression living cell array. Lab Chip 2007; 7 (01) 77-85
- 210 Zhang C, Xing D, Li Y. Micropumps, microvalves, and micromixers within PCR microfluidic chips: advances and trends. Biotechnol Adv 2007; 25 (05) 483-514
- 211 Lee J, Estlack Z, Somaweera H, Wang X, Lacerda CMR, Kim J. A microfluidic cardiac flow profile generator for studying the effect of shear stress on valvular endothelial cells. Lab Chip 2018; 18 (19) 2946-2954
- 212 Chen Y, Chan HN, Michael SA. , et al. A microfluidic circulatory system integrated with capillary-assisted pressure sensors. Lab Chip 2017; 17 (04) 653-662
- 213 Leung K, Zahn H, Leaver T. , et al. A programmable droplet-based microfluidic device applied to multiparameter analysis of single microbes and microbial communities. Proc Natl Acad Sci U S A 2012; 109 (20) 7665-7670
- 214 Szydzik C, Gavela AF, Herranz S. , et al. An automated optofluidic biosensor platform combining interferometric sensors and injection moulded microfluidics. Lab Chip 2017; 17 (16) 2793-2804
- 215 Kim J, Stockton AM, Jensen EC, Mathies RA. Pneumatically actuated microvalve circuits for programmable automation of chemical and biochemical analysis. Lab Chip 2016; 16 (05) 812-819
- 216 Szydzik C, Niego B, Dalzell G, Knoerzer M. Fabrication of complex PDMS microfluidic structures and embedded functional substrates by one-step injection moulding. RSC Adv 2016; 6 (91) 87988-87994
- 217 Harris LF, Killard AJ. Microfluidics in coagulation monitoring devices: a mini review. Anal Methods 2018; 10 (30) 3714-3719
- 218 Kumar V, Packirisamy G, Lakshmanan VK, Pandiyaraj KN. Surface analysis technique for assessing hemocompatibility of biomaterials. In: Siedlecki C. , ed. Hemocompatibility of Biomaterials for Clinical Applications. Cambridge, United Kingdom: Elsevier; 2018: 119-161
- 219 Sanak M, Jakieła B, Węgrzyn W. Assessment of hemocompatibility of materials with arterial blood flow by platelet functional tests. Bull Pol Acad Sci Tech Sci 2010; 58 (02) 317-322
- 220 Streller U, Sperling C, Hübner J, Hanke R, Werner C. Design and evaluation of novel blood incubation systems for in vitro hemocompatibility assessment of planar solid surfaces. J Biomed Mater Res B Appl Biomater 2003; 66 (01) 379-390
- 221 Inglis DW, Morton KJ, Davis JA. , et al. Microfluidic device for label-free measurement of platelet activation. Lab Chip 2008; 8 (06) 925-931
- 222 Evander M, Ricco AJ, Morser J, Kovacs GT, Leung LL, Giovangrandi L. Microfluidic impedance cytometer for platelet analysis. Lab Chip 2013; 13 (04) 722-729
- 223 Li Z, Delaney MK, O'Brien KA, Du X. Signaling during platelet adhesion and activation. Arterioscler Thromb Vasc Biol 2010; 30 (12) 2341-2349
- 224 Varga-Szabo D, Braun A, Nieswandt B. Calcium signaling in platelets. J Thromb Haemost 2009; 7 (07) 1057-1066
- 225 Gutierrez E, Petrich BG, Shattil SJ, Ginsberg MH, Groisman A, Kasirer-Friede A. Microfluidic devices for studies of shear-dependent platelet adhesion. Lab Chip 2008; 8 (09) 1486-1495
- 226 Banerjee D, Mazumder S, Kumar Sinha A. Involvement of nitric oxide on calcium mobilization and arachidonic acid pathway activation during platelet aggregation with different aggregating agonists. Int J Biomed Sci 2016; 12 (01) 25-35
- 227 Westein E, de Witt S, Lamers M, Cosemans JM, Heemskerk JW. Monitoring in vitro thrombus formation with novel microfluidic devices. Platelets 2012; 23 (07) 501-509
- 228 Branchford BR, Ng CJ, Neeves KB, Di Paola J. Microfluidic technology as an emerging clinical tool to evaluate thrombosis and hemostasis. Thromb Res 2015; 136 (01) 13-19
- 229 Jain A, Graveline A, Waterhouse A, Vernet A, Flaumenhaft R, Ingber DE. A shear gradient-activated microfluidic device for automated monitoring of whole blood haemostasis and platelet function. Nat Commun 2016; 7: 10176
- 230 Schoeman RM, Lehmann M, Neeves KB. Flow chamber and microfluidic approaches for measuring thrombus formation in genetic bleeding disorders. Platelets 2017; 28 (05) 463-471
- 231 Herbig BA, Yu X, Diamond SL. Using microfluidic devices to study thrombosis in pathological blood flows. Biomicrofluidics 2018; 12 (04) 042201
- 232 Ting LH, Feghhi S, Taparia N. , et al. Contractile forces in platelet aggregates under microfluidic shear gradients reflect platelet inhibition and bleeding risk. Nat Commun 2019; 10 (01) 1204
- 233 Kamath S, Blann AD, Lip GY. Platelet activation: assessment and quantification. Eur Heart J 2001; 22 (17) 1561-1571
- 234 Lu Q, Malinauskas RA. Comparison of two platelet activation markers using flow cytometry after in vitro shear stress exposure of whole human blood. Artif Organs 2011; 35 (02) 137-144
- 235 Lee KK, Ahn CH. A new on-chip whole blood/plasma separator driven by asymmetric capillary forces. Lab Chip 2013; 13 (16) 3261-3267