Blood clot behaves as a poro-visco-elastic material

Mechanical properties of blood clots play a crucial role in hemostasis and embolization. They are time-dependent and often described with viscoelastic models. But blood clots also exhibit some hallmark features of poroelasticity, as most biological tissues exhibit concurrent viscoelasticity and poroelasticity. In this study, we characterized the time-dependent behavior of blood clots, and developed an experimental-computational framework to decouple and model poroelastic and viscoelastic responses. Compression stress relaxation tests were conducted on bovine blood clots with different diameters to evaluate the influence of sample size on the relaxation time. In the compression tests, the mass of blood clots was measured to estimate fluid migration. To capture pure viscoelastic responses, rheological shear stress relaxation tests were carried out. A poroviscoelastic model was also proposed and calibrated to capture the complex multiaxial (compression and shear) relaxation behavior of blood clots. In unconfined compression tests, stresses relaxed markedly (average: 83%; range: 76-90%), and samples with larger diameters showed longer relaxation time. Blood clots lost about 24% of their initial masses, and the mass transport took place gradually in compression tests. Under shear deformation, blood clots relaxed in average 37% (range: 32-39%) which was much less than those under unconfined compression tests (in average 37% versus 83%). Unlike poroelastic and viscoelastic theories, the poroviscoelastic model accurately predicted multiaxial responses of blood clots under compression and shear; additionally, the estimated Darcy's coefficient (4.4×10-9 cm2) was found within the reported physiological range (0.1×10-9 to 36 × 10-9 cm2). The combination of size-dependent stress relaxation and mass loss under compression (due to poroelasticity) as well as substantial stress relaxation under shear deformation (due to viscoelasticity) demonstrate that blood clot behaves as a poroviscoelastic material; therefore, accurate interpretation of transient responses of blood clots requires a validated poroviscoelastic model. This work provides understanding and methodology on blood clot mechanics and will further motivate the development of clot-like biomaterials.