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Method Article

Thrombus Profiling Assay: A Microfluidics-Based Platform for Comprehensively Characterizing Biomechanical Thrombogenesis

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DOI:

10.3791/69555

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January 9th, 2026

 ,  ,  , 
1Department of Biochemistry and Molecular Biology and Department of Pathology, University of Texas Medical Branch

* These authors contributed equally

In This Article

Summary

This work describes a microfluidic assay that uses shear stress to trigger thrombus formation in blood and characterizes the thrombus by multiple dimensions of readout. The assay can measure the prothrombotic tendency of blood samples, and is thus useful in disease diagnosis, drug discovery, as well as basic mechanistic studies related to thrombosis.

Abstract

Thrombosis is a pathological condition describing the abnormal accumulation of platelets and clotting factors in a blood vessel. While many works focused on platelet activation by soluble agonists as an underlying mechanism of thrombosis, it has often been overlooked that blood flow also facilitates thrombus formation. Especially, in the arteries, thrombosis is generally associated with arterial stenosis, which elevates the shear stress in the blood flow and facilitates the process of thrombogenesis, a phenomenon termed biomechanical thrombogenesis. For a long time, no bioassay was available to provide all-around and detailed insights into the process of biomechanical thrombogenesis. To address this, a thrombus profiling assay was developed by combining microfluidics with multi-color fluorescence imaging, which allows comprehensive characterization of biomechanical thrombogenesis with seven readouts covering the size and composition of the thrombus as well as platelet activation level. This thrombus profiling assay can be used to evaluate the prothrombotic tendency in humans and the efficacy of anti-thrombotic agents, and it is also useful for further understanding the mechanisms underlying arterial thrombosis.

Introduction

Thrombosis is a main cause of cardiovascular diseases, responsible for millions of deaths worldwide every year1. Currently, no bioassay is available in standard clinical settings for evaluating risks of thrombosis. Among the commercialized laboratory and point-of-care hematological function assays, conventional coagulation assays and aggregometry have been proven unreliable in predicting thrombosis or major adverse cardiovascular events2,3,4. Global thrombosis test5, PFA-100/2006, and global coagulation assays7,8,9,10,11 also have limited data supporting their performance.

Based on the current understanding, the process of thrombogenesis is mainly contributed to by three mechanisms. Besides the two conventionally acknowledged mechanisms, namely, biochemical platelet aggregation and coagulation, a third mechanism that is under-studied and often under-estimated is shear-driven platelet aggregation, which was also termed as "biomechanical platelet aggregation"12,13. In biomechanical platelet aggregation, high shear stress and shear gradient serve as the main drive for platelet crosslinking via GPIbα-von Willebrand factor (VWF), integrin αIIbβ3-VWF, and integrin αIIbβ3-fibrinogen interactions. In arterial thrombosis, biomechanical platelet aggregation likely serves as the most essential mechanism, considering that it is greatly reinforced by high shear flow caused by arterial stenosis. Therefore, thrombogenesis driven by biomechanical platelet aggregation was termed 'biomechanical thrombogenesis'12,14.

In previous works, a common method for experimentally observing biomechanical platelet aggregation is the microfluidic stenosis assay, wherein a site of severe stenosis is embedded into a straight channel. When blood is perfused over the channel under a physiological wall shear stress, pathologically high shear stress is generated around the stenotic site, which drives the accumulation of platelets to form a thrombus. However, previous works only utilized a single (for platelets, reflecting the thrombus size)15,16,17,18,19 or at most two (one for platelets and one for another biomarker) readout13,20, which are thus unable to achieve comprehensive characterization of the thrombus.

A thrombus profiling assay was recently developed, which incorporates multi-color fluorescence imaging in the microfluidic stenosis assay, achieving real-time tracking of 7 biomarkers (platelets, fibrinogen level, von Willebrand factor level, P-selectin expression level, phosphatidylserine exposure level, extended integrin αIIbβ3 expression level, fully active integrin αIIbβ3 expression level) in a thrombus, which sets the basis for comprehensively characterizing biomechanical thrombogenesis21. In this work, detailed protocols are provided on the preparation and performance of the thrombus profiling assay as well as the related data analysis. The hardware required for the assay includes an inverted multi-color fluorescence microscope and a microfluidic system. The assay uses a relatively small amount of human whole blood (less than 2 mL), has high cost-effectiveness (~$12 per sample), and derives results within 30 min. The assay can accurately detect the multi-dimensional prothrombotic abnormalities of individuals and evaluate the effects of anti-thrombotic agents in changing the size, composition, and platelet activation status of the thrombus, endorsing its wide application for both research and clinical purposes in the future21. It is noteworthy that the assay must use freshly collected heparinized blood. Storing the blood at 4 °C or for over 6 h or using anticoagulants other than heparin will either prevent thrombus from forming or render inaccurate results.

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Protocol

This protocol follows the guidelines of and has been approved by the Human Research Ethics Committee of The University of Texas Medical Branch. The experimental hardware setup consists of a microfluidic device, perfusion components (connectors, tubing, syringe, and syringe pump), and an inverted microscope with optical components enabling bright-field and multi-color fluorescence imaging. A multi-LED light house and a multi-pass filter cube are used in the microscope to split 4 fluorescent channels with minimal mutual bleed-through: excitation: 391/32, 479/33, 554/24, 638/31, and emission: 435/30, 519/25, 594/32, 695/58. Wear personal protective equipment, including gloves, eye protection, and a lab jacket, for all experimental procedures. The reagents and the equipment used are listed in the Table of Materials.

1. Microfluidic device preparation

  1. Design a master mold to contain rectangular channels (200 µm wide × 50 µm high) that incorporate a site of 80% luminal narrowing. Each channel has dedicated inlets and outlets for tubing connections (Figure 1; see Supplementary File 1 for the original design file).
  2. Based on the design, use a silicon wafer to fabricate an SU-8 photoresist master mold via standard photolithography. Tape the mold at the bottom of a 15-cm Petri dish (Figure 2A).
  3. Prepare PDMS mixture by mixing the prepolymer base and curing agent in the silicone elastomer kit at a 10:1 weight ratio. Pour the mixture onto the master mold (Figure 2B).
  4. Place the plate containing the PDMS mixture in a vacuum desiccator to degas and eliminate entrapped air bubbles.
    NOTE: Maintain the plate under vacuum for a minimum of 2 h until bubbles are completely removed.
  5. Thermally cure the PDMS mixture by incubating it at 75 °C for 2 h.
  6. Carefully cut out the cured PDMS from the master mold (Figure 2C,D) and section it into individual chip units.
  7. Create the inlet and outlet by punching holes at the designated locations using a probe needle (Figure 2E).
    NOTE: Use a compressed air duster to remove any residual debris from the punched holes. To minimize surface contamination, clean the PDMS devices using adhesive sealing tape prior to bonding.
  8. In a chemical hood, spray 75% ethanol on a task wipe, and use the wetted task wipe to wipe and clean glass slides. Leave the glass slides to dry.
  9. In a chemical hood, treat the glass slides and PDMS chips with a high-frequency generator for 30 s and 20 s, respectively, and then align each chip with a glass slide. Gently press the chip onto the glass slide surface so that it can be bound.
    NOTE: This step needs to be done in a chemical hood because the high-frequency generator produces ozone during usage, which is harmful to health.
  10. Thermally bond the devices by incubating them at 150 °C for 15 min. After cooling down, the devices will be ready to use (Figure 2F).
  11. Store the devices at room temperature under dust-free conditions.
  12. Use a pincer to remove the plastic part of the probe needles, and bend the metal tubes to 90°. These bent tubes will be used as connectors for the microfluidic devices.

2. Fluorescent sensor preparation

NOTE: The experiment uses a total of 7 fluorescent sensors: SZ22-FITC, fibrinogen-Alexa Fluor 405, 2.2.9-Alexa Fluor 555, AK4-Alexa Fluor 647, Annexin V-Pacific Blue, MBC 370.2-Alexa Fluor 555, PAC-1-Alexa Fluor 647. Among them, fibrinogen, 2.2.9, and MBC 370.2 are only commercially available in the unconjugated form and need to be fluorescently conjugated in the lab.

  1. To conjugate fibrinogen with Alexa Fluor 405:
    1. Make a fresh 0.1 M sodium bicarbonate buffer, pH 8.5.
    2. Dilute fibrinogen stock to 1 mg/mL in phosphate-buffered saline (PBS; 137 mM NaCl, 2.7 mM KCl, 10 mM Na2HPO4, 1.8 mM KH2PO4, pH 7.4).
    3. Add 1/10 volume of sodium bicarbonate buffer to the fibrinogen solution.
    4. Mix 1 mL fibrinogen with 1 mg Alexa Fluor 405 NHS-ester and incubate for 1 h at room temperature on a rotator. Protect from light.
    5. Remove the storage buffer from a purification column by centrifuging the column at 1,100 × g for 2 min, and discard the flow-through. Load the reaction solution onto the column, mount the column onto a compatible collection vial, and centrifuge at 1,100 × g for 5 min to harvest the fibrinogen-Alexa Fluor 405.
    6. Use a spectrophotometer to measure the absorbance at 280 nm (A280; protein signal) and 405 nm (A405; dye signal) wavelength. Calculate protein concentration and F/P ratio (fluorescence: protein molar ratio).
      NOTE: The F/P ratio should be in the range of 8-10.
    7. Store fibrinogen-Alexa Fluor 405 at 4 °C in the dark.
  2. To conjugate 2.2.9 and MBC 370.2 antibodies with Alexa Fluor 555:
    1. Make a fresh 0.1 M sodium bicarbonate buffer, pH 8.5.
    2. Dilute antibody stock to 1 mg/mL in amine-free buffer.
    3. Add 1/10 volume of sodium bicarbonate buffer to the antibody solution.
    4. Mix 100 µL antibody with 1 vial (100 µg) of Alexa Fluor 555 NHS-ester and incubate for 1 h at room temperature on a rotator. Protect from light.
    5. Remove the storage buffer from a purification column by centrifuging the column at 1,100 × g for 2 min, and discard the flow-through. Load the reaction solution onto the column, mount the column onto a compatible collection vial, and centrifuge at 1,100 × g for 5 min to harvest the 2.2.9- or MBC 370.2-Alexa Fluor 555.
    6. Use a spectrophotometer to measure the absorbance at 280 nm (A280; protein signal) and 555 nm (A555; dye signal) wavelength. Calculate antibody concentration and F/P ratio (fluorescence: antibody molar ratio).
      NOTE: The F/P ratio should be in the range of 1-1.5.
    7. Store 2.2.9- and MBC 370.2-Alexa Fluor 555 in 4 °C in the dark.
      NOTE: Avoid over-labeling - high F/P ratio may impair biological function.

3. Blood collection from human subjects

NOTE: This procedure must be conducted by qualified medical personnel (e.g., licensed nurses, certified phlebotomists). Also, obtain written informed consent from the individuals participating in the study.

  1. Prepare the syringe by aspirating 500 µL of Tyrode buffer (12 mM NaHCO3, 10 mM Hepes, 137 mM NaCl, 2.7 mM KCl, 5.5 mM D-Glucose, 0.5% bovine serum albumin, pH 7.4) containing 0.32 U/mL heparin per 10 mL of blood to be collected.
  2. Collect blood via venipuncture. Use an empty syringe to collect the first 2 mL of blood to discard. Then, change to the heparin-containing syringe to collect the blood sample. Pull the syringe slowly to minimize platelet activation.
  3. Transfer the collected blood into a 15-mL centrifuge tube and keep it under 37 °C.
    NOTE: Blood samples should be used for experiments within 6 h of collection.

4. Thrombus profiling assay

NOTE: It is recommended to perform all procedures involving blood handling in a biosafety cabinet whenever possible to avoid blood spills on the experimentalist. If this is not possible, then use a benchtop splash shield.

  1. Dilute VWF monomer to 2 µg/mL in PBS. Pre-coat the microfluidic devices with VWF monomer and incubate for 1 h at room temperature.
  2. Incubate the blood sample with fluorescent sensor Set 1 or 2 for 10 min at room temperature:
    1. Set 1: SZ22-FITC (0.5 µg/mL), fibrinogen-Alexa Fluor 405 (60 µg/mL), 2.2.9-Alexa Fluor 555 (1 µg/mL), AK4-Alexa Fluor 647 (1 µg/mL).
    2. Set 2: SZ22-FITC (0.5 µg/mL), Annexin V-Pacific Blue (1 µg/mL), MBC 370.2-Alexa Fluor 555 (1 µg/mL), PAC-1-Alexa Fluor 647 (1 µg/mL).
      NOTE: Because two sensor sets need to be used separately, each blood sample needs to be tested at least twice (once with sensor Set 1 and once with sensor Set 2) to acquire a complete data set.
  3. Connect a microfluidic device with inlet and outlet connectors and tubing. Connect the other end of the inlet connector with a tube containing PBS, and the other end of the outlet connector with a syringe. Mount the syringe onto a syringe pump. Mount the microfluidic device onto an inverted microscope, and manually maneuver the stage to find the site of stenosis under the microscope (Figure 3A).
  4. Fill the microfluidic channel and tubing with PBS using the syringe pump at a flow rate of 0.5 mL/min. Ensure that no air bubbles are present around the site of stenosis.
  5. Connect the inlet tubing with the blood sample, and perfuse the blood sample through the microfluidic channel using the syringe pump at a flow rate of 0.018 mL/min (Figure 3A).
  6. Set the exposure time and gain of each fluorescence channel. Perform real-time multi-color fluorescence imaging by alternating among the 4 channels, exciting one kind of fluorophore at a time. Meanwhile, find the focus plane of the thrombus, and record signals at the site of stenosis, typically spanning 15-30 min (Figure 4).
    NOTE: The exposure time of each channel needs to be adjusted so that the fluorescent signal is easily distinguishable while avoiding saturation (Figure 4). In the present system, healthy subjects' blood samples typically render the following signal intensity range within the formed thrombus: SZ22-FITC, 70-110; fibrinogen-Alexa Fluor 405, 60-100; 2.2.9-Alexa Fluor 555, 70-110; AK4-Alexa Fluor 647, 45-75; Annexin V-Pacific Blue, 35-65; MBC 370.2-Alexa Fluor 555, 45-85; PAC-1-Alexa Fluor 647, 10-30. Notably, however, a small proportion of healthy subjects would render a non-typical readout. Therefore, it is recommended to test at least 5 healthy subject's blood samples to make sure that the exposure time for each channel is selected properly.

5. Data analysis

  1. Open the data file using ImageJ 1.53 (Fiji, National Institutes of Health).
    NOTE: Each file should contain a total of 4 videos from 4 different channels. The following procedure is generally applicable to any time point that the user is interested in analyzing.
  2. Use the SZ22-FITC channel to identify the contour of the thrombus, and use 'Polygon selections' to roughly select the area of the thrombus (Figure 5A,B).
  3. For each channel, use Image -> Adjust -> Threshold to eliminate the background (Figure 5C), and then use Analyze -> Measure to measure the area and average intensity of the signal within the thrombus.
    NOTE: SZ22-FITC stains platelets and thus reflects thrombus size. In Set 1, fibrinogen-Alexa Fluor 405 reflects fibrinogen enrichment level, 2.2.9-Alexa Fluor 555 reflects von Willebrand factor (VWF) enrichment level, and AK4-Alexa Fluor 647 reflects P-selection expression. In Set 2, Annexin V-Pacific Blue reflects phosphatidylserine (PS) exposure, MBC 370.2-Alexa Fluor 555 reflects integrin αIIbβ3 activation to the extended conformation (E+ αIIbβ3), and PAC-1-Alexa Fluor 647 reflects integrin αIIbβ3 full activation (Act. αIIbβ3)21.

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Results

The thrombus profiling assay perfuses blood through a stenotic channel to allow shear-driven thrombus formation, and performs real-time multi-color fluorescence imaging to collect multi-dimensional information on the formed thrombus. By completing experiments using both Set 1 and Set 2 sensors, one should be able to characterize the thrombus in aspects including size, enrichment of crosslinking proteins (von Willebrand factor, fibrinogen), as well as platelet activation level (reflected by P-selection expression, PS expo...

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Discussion

By combining the microfluidic stenosis assay with multi-color fluorescence imaging, the thrombus profiling assay provides a convenient and powerful approach to study biomechanical thrombogenesis and platelet mechanobiology. Meanwhile, the assay is useful in a wide range of applications. For instance, it can be used to screen anti-thrombotic agents that specifically inhibit biomechanical platelet aggregation, where the molecular target and mechanism of action can be deduced from the effect barcode21

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Disclosures

The authors have no conflicts of interest to disclose.

Acknowledgements

Research related to this paper and the development of the thrombus profiling assay in the Chen lab were supported by National Heart, Lung, and Blood Institute grant R00HL153678 (Y.C.), National Institute on Aging, the Claude D. Pepper Older Americans Independence Center Award #P30-AG024832 (Y.C.), UTMB Team Science Pilot Research Award (Y.C.), American Heart Association Postdoctoral Fellowship 20POST35080023 (Y.C.), and American Heart Association Transformational Project Award 25TPA1471420 (Y.C.). This work was performed in part at the San Diego Nanotechnology Infrastructure (SDNI) of UCSD, a member of the National Nanotechnology Coordinated Infrastructure, which is supported by the National Science Foundation (Grant ECCS-2025752).

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Materials

List of materials used in this article
NameCompanyCatalog NumberComments
10-mL SyringesHenke Sass Wolf5100-X00V0Blood sample collection
15-mL falcon tubesGenesee Scientific28-101Blood sample storage
1-mL gastight glass syringeHamilton81331Hardware assembly
2.2.9MERU VasImmuneThrombus staining
20 X1/2 Probe NeedlesMcMaster-CarrM919Making PDMS devices
20-mL SyringesHenke Sass Wolf5200-X00V0Blood sample collection
70% ethanolSigma-AldrichEX0281-1Disinfection of gastight syringes and cleaning of glass slides
AK4-Alexa Fluor 647BioLegend304918Thrombus staining
Alexa Fluor 405 NHS EsterInvitrogenA30000Fibrinogen labeling
Alexa fluor 555 antibody labeling kitInvitrogenA88065MBC 370.2 and 2.2.9 labeling
Annexin V-Pacific BlueInvitrogen501121505Thrombus staining
Cleaning DusterOffice Depot911245Making PDMS devices
Craft Hobby Knife Set with Wooden BoxExcel Blades44282Making PDMS devices
Deionized water ThermoFisher Scientific 751-628Washing of gastight syringes
DesiccatorBel ArtF420270000Degasing PDMS
Disposable Multipurpose Laboratory SpatulaLevGo17211Mixing the silicone elastomer base and curing agent 
Dye and Biotin Removal Spin ColumnZebaA44296SFibrinogen labeling
FibrinogenInnovative ResearchIHUFBG25MGThrombus staining
Fusion 200-X syringe pumpChemyx Inc.0720XHardware assembly
Heparin Sigma-AldrichH3149Blood sample anticoagulation
High Frequency GeneratorElectro-technic product Inc.BD-20Making PDMS devices
Human VWF monomerSino Biological Inc.10973-H08CMicrofuidic device coating
Image J v1.53 softwareFiji, National Institute of HealthData analysis
Inverted microscopeLeicaDM IL LED; filter cube: Leica DFT51010; lighthouse: LED5Hardware assembly
KimwipesKimberly- Clark Professional34120Cleaning of glass slides
Luer lock capsInternational Medical Industries, Inc.57100BBlood sample collection
MBC 370.2KerafastEBW104Thrombus staining
Microscope cover glassesPaul Marienfeld GmbH & Co. KGES0107222Making PDMS devices
Mini-Razor Blade ScraperStanley28-100Making PDMS devices
NanoDrop 2000 UV-Vis SpectrophotometerThermo ScientificND-2000Protein concentration and F/P ratio measurement
OvenLab-Line Instruments3512Making PDMS devices
PAC-1-Alexa Fluor 647BioLegend362806Thrombus staining
Plastic cupThermoFisher Scientific S04589Mixing the silicone elastomer base and curing agent 
SU-8 photoresist master  moldUC San Diego Nano3 Nanofabrication Cleanroom FacilityMaking PDMS devices
Sylgard 184 Silicone Elastomer KitKrayden DowDC4019862PDMS
SZ22-FITC Beckman CoulterIM 1756UThrombus staining
TubingCole -Palmer Instrument Co.06422-01Hardware assembly

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Microfluidic DevicesPlatelet ActivationFluorescence ImagingArterial ThrombosisVon Willebrand FactorProthrombotic TendencySyringe PumpImageJ Analysis
Thrombus Profiling Assay: A Microfluidics-Based Platform for Comprehensively Characterizing Biomechanical Thrombogenesis
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