Hierarchical poromechanical approach to investigate the impact of  mechanical loading on human skin micro-circulation

[en] Research on human skin anatomy reveals its complex multi-scale, multi-phase nature, with up to 70% of its composition being bounded and free water. Fluid movement plays a key role in the skin's mechanical and biological responses, influencing its time-dependent behavior and nutrient transport. Poroelastic modeling is a promising approach for studying skin dynamics across scales by integrating multi-physics processes. This paper introduces a hierarchical two-compartment model capturing fluid distribution in the interstitium and micro-circulation. A theoretical framework is developed with a biphasic interstitium -- distinguishing interstitial fluid and non-structural cells -- and analyzed through a one-dimensional consolidation test of a column. This biphasic approach allows separate modeling of cell and fluid motion, considering their differing characteristic times. An appendix discusses extending the model to include biological exchanges like oxygen transport. Preliminary results indicate that cell viscosity introduces a second characteristic time, and at high viscosity and short time scales, cells behave similarly to solids. A simplified model was used to replicate an experimental campaign on short time scales. Local pressure (up to 31 kPa) was applied to dorsal finger skin using a laser Doppler probe PF801 (Perimed Sweden), following a setup described in Fromy Brain Res (1998). The model qualitatively captured ischemia and post-occlusive reactive hyperemia, aligning with experimental data. All numerical simulations used the open-source software FEniCSx v0.9.0. To ensure transparency and reproducibility, anonymized experimental data and finite element codes are publicly available on GitHub.

Disciplines :

Engineering, computing & technology: Multidisciplinary, general & others

Author, co-author :

LAVIGNE, Thomas ; University of Luxembourg > Faculty of Science, Technology and Medicine (FSTM) > Department of Engineering (DoE)

URCUN, Stephane ; University of Luxembourg > Faculty of Science, Technology and Medicine > Department of Engineering > Team Stéphane BORDAS

Fromy, Bérengère

Josset-Lamaugarny, Audrey

Lagache, Alexandre

Suarez-Afanador, Camilo A.

Stéphane P. A. Bordas

Rohan, Pierre-Yves

Sciumè, Giuseppe

External co-authors :

yes

Language :

English

Title :

Hierarchical poromechanical approach to investigate the impact of mechanical loading on human skin micro-circulation

Publication date :

2025

Journal title :

International Journal for Numerical Methods in Biomedical Engineering

ISSN :

2040-7939

eISSN :

2040-7947

Publisher :

John Wiley & Sons, United Kingdom

Peer reviewed :

Peer Reviewed verified by ORBi

FnR Project :

FNR17013182 - CHAMP - Characterisation And Modelling Of Perfusion And Soft Tissue Damage In Pressure Ulcer Prevention, 2022 (01/09/2022-31/08/2025) - Thomas Jeffrey Hugo Marc Lavigne

Available on ORBilu :

since 29 June 2025

Statistics

Number of views

91 (0 by Unilu)

Number of downloads

26 (0 by Unilu)

More statistics

Scopus citations^®

Scopus citations^®
without self-citations

OpenCitations

OpenAlex citations

Bibliography

K. Vanderwee, M. Clark, C. Dealey, L. Gunningberg, and T. Defloor, “Pressure ulcer prevalence in europe: a pilot study,” Journal of Evaluation in Clinical Practice 13, no. 2 (2007): 227–235.
J. Kim, J. Lee, and E. Lee, “Risk Factors for Newly Acquired Pressure Ulcer and the Impact of Nurse Staffing on Pressure Ulcer Incidence,” Journal of Nursing Management 30, no. 5 (2020): O1–O9.
Z. Moore, P. Avsar, L. Conaty, D. H. Moore, D. Patton, and T. O'Connor, “The Prevalence of Pressure Ulcers in Europe, What Does the European Data Tell Us: A Systematic Review,” Journal of Wound Care 28, no. 11 (2019): 710–719.
D. Anthony, S. Parboteeah, M. Saleh, and P. Papanikolaou, “Norton, Waterlow and Braden Scores: A Review of the Literature and a Comparison Between the Scores and Clinical Judgement,” Journal of Clinical Nursing 17, no. 5 (2008): 646–653.
Y.-C. Hsu and E. Fuchs, “Building and Maintaining the Skin,” Cold Spring Harbor Perspectives in Biology 14, no. 7 (2021): a040840.
T. Burns, S. M. Breathnach, N. H. Cox, and C. Griffiths, Rook's Textbook of Dermatology, 8th ed. (Wiley-Blackwell, 2010).
R. Wong, S. Geyer, W. Weninger, J.-C. Guimberteau, and J. K. Wong, “The Dynamic Anatomy and Patterning of Skin,” Experimental Dermatology 25, no. 2 (2015): 92–98.
H. Joodaki and M. B. Panzer, “Skin Mechanical Properties and Modeling: A Review,” Proceedings of the Institution of Mechanical Engineers, Part H: Journal of Engineering in Medicine 232, no. 4 (2018): 323–343.
S. J. M. Yazdi and J. Baqersad, “Mechanical Modeling and Characterization of Human Skin: A Review,” Journal of Biomechanics 130 (2022): 110864.
J. M. Abdo, N. A. Sopko, and S. M. Milner, “The Applied Anatomy of Human Skin: A Model for Regeneration,” Wound Medicine 28 (2020): 100179.
K. K. Dwivedi, P. Lakhani, S. Kumar, and N. Kumar, “Effect of Collagen Fibre Orientation on the Poisson's Ratio and Stress Relaxation of Skin: An Ex Vivo and in Vivo Study,” Royal Society Open Science 9, no. 3 (2022): 211301.
F. Liao, S. Burns, and Y.-K. Jan, “Skin Blood Flow Dynamics and Its Role in Pressure Ulcers,” Journal of Tissue Viability 22, no. 2 (2013): 25–36.
I. M. Braverman, “Ultrastructure and Organization of the Cutaneous Microvasculature in Normal and Pathologic States,” Journal of Investigative Dermatology 93, no. 2 (1989): S2–S9.
B. Querleux, C. Cornillon, O. Jolivet, and J. Bittoun, “Anatomy and Physiology of Subcutaneous Adipose Tissue by in Vivo Magnetic Resonance Imaging and Spectroscopy: Relationships With Sex and Presence of Cellulite,” Skin Research and Technology 8, no. 2 (2002): 118–124.
K. Ceelen, A. Stekelenburg, S. Loerakker, et al., “Compression-Induced Damage and Internal Tissue Strains Are Related,” Journal of Biomechanics 41, no. 16 (2008): 3399–3404.
S. Loerakker, E. Manders, G. J. Strijkers, et al., “The Effects of Deformation, Ischemia, and Reperfusion on the Development of Muscle Damage During Prolonged Loading,” Journal of Applied Physiology 111, no. 4 (2011): 1168–1177.
S. Loerakker, A. Stekelenburg, G. J. Strijkers, et al., “Temporal Effects of Mechanical Loading on Deformation-Induced Damage in Skeletal Muscle Tissue,” Annals of Biomedical Engineering 38, no. 8 (2010): 2577–2587.
A. Stekelenburg, C. W. J. Oomens, G. J. Strijkers, K. Nicolay, and D. L. Bader, “Compression-Induced Deep Tissue Injury Examined With Magnetic Resonance Imaging and Histology,” Journal of Applied Physiology 100, no. 6 (2006): 1946–1954.
B. J. van Nierop, A. Stekelenburg, S. Loerakker, et al., “Diffusion of Water in Skeletal Muscle Tissue Is Not Influenced by Compression in a Rat Model of Deep Tissue Injury,” Journal of Biomechanics 43, no. 3 (2010): 570–575.
W. A. Traa, M. C. van Turnhout, J. L. Nelissen, G. J. Strijkers, D. L. Bader, and C. W. Oomens, “There Is an Individual Tolerance to Mechanical Loading in Compression Induced Deep Tissue Injury,” Clinical biomechanics 63 (2019): 153–160.
S. Tsuji, S. Ichioka, N. Sekiya, and T. Nakatsuka, “Analysis of Ischemia-Reperfusion Injury in a Microcirculatory Model of Pressure Ulcers,” Wound Repair and Regeneration 13, no. 2 (2005): 209–215.
S. Coleman, C. Gorecki, E. A. Nelson, et al., “Patient Risk Factors for Pressure Ulcer Development: Systematic Review,” International Journal of Nursing Studies 50, no. 7 (2013): 974–1003.
V. D. Sree, M. K. Rausch, and A. B. Tepole, “Linking Microvascular Collapse to Tissue Hypoxia in a Multiscale Model of Pressure Ulcer Initiation,” Biomechanics and Modeling in Mechanobiology 18, no. 6 (2019): 1947–1964.
M.-S. Nguyen-Tu, A.-L. Begey, J. Decorps, et al., “Skin Microvascular Response to Pressure Load in Obese Mice,” Microvascular Research 90 (2013): 138–143.
D. Fukumura and R. K. Jain, “Tumor Microvasculature and Microenvironment: Targets for Anti-Angiogenesis and Normalization,” Microvascular Research 74, no. 2 (2007): 72–84.
N. S. Russell, B. Floot, E. van Werkhoven, et al., “Blood and Lymphatic Microvessel Damage in Irradiated Human Skin: The Role of Tgf−β$$ \mathrm{Tgf}-\beta $$, Endoglin and Macrophages,” Radiotherapy and Oncology 116, no. 3 (2015): 455–461.
E. Tesselaar, A. M. Flejmer, S. Farnebo, and A. Dasu, “Changes in Skin Microcirculation During Radiation Therapy for Breast Cancer,” Acta Oncologica 56, no. 8 (2017): 1072–1080.
R. I. Kelly, R. Pearse, R. H. Bull, J.-L. Leveque, J. de Rigal, and P. S. Mortimer, “The Effects of Aging on the Cutaneous Microvasculature,” Journal of the American Academy of Dermatology 33, no. 5 (1995): 749–756.
U. Baran, W. J. Choi, and R. K. Wang, “Potential Use of Oct−Based Microangiography in Clinical Dermatology,” Skin Research and Technology 22, no. 2 (2015): 238–246.
K. Farkas, E. Kolossváry, Z. Járai, J. Nemcsik, and C. Farsang, “Non-Invasive Assessment of Microvascular Endothelial Function by Laser Doppler Flowmetry in Patients With Essential Hypertension,” Atherosclerosis 173, no. 1 (2004): 97–102.
M. Rossi, A. Carpi, C. Di Maria, F. Galetta, and G. Santoro, “Spectral Analysis of Laser Doppler Skin Blood Flow Oscillations in Human Essential Arterial Hypertension,” Microvascular Research 72, no. 1–2 (2006): 34–41.
C. Svedman, G. W. Cherry, E. Strigini, and T. J. Ryan, “Laser Doppler Imaging of Skin Microcirculation,” Acta Dermato-Venereologica 78, no. 2 (1998): 114–118.
S. Kubli, B. Waeber, A. Dalle-Ave, and F. Feihl, “Reproducibility of Laser Doppler Imaging of Skin Blood Flow as a Tool to Assess Endothelial Function,” Journal of Cardiovascular Pharmacology 36, no. 5 (2000): 640–648.
C. Millet, M. Roustit, S. Blaise, and J. Cracowski, “Comparison Between Laser Speckle Contrast Imaging and Laser Doppler Imaging to Assess Skin Blood Flow in Humans,” Microvascular Research 82, no. 2 (2011): 147–151.
L. An, J. Qin, and R. K. Wang, “Ultrahigh Sensitive Optical Microangiography for in Vivo Imaging of Microcirculations Within Human Skin Tissue Beds,” Optics Express 18, no. 8 (2010): 8220–8228.
L. Poffo, J.-M. Goujon, R. Le Page, et al., “Laser double doppler flowmeter,” in Biophotonics: Photonic Solutions for Better Health Care IV, vol. 9129, ed. J. Popp, V. V. Tuchin, D. L. Matthews, F. S. Pavone, and P. Garside (SPIE, 2014), 91290X.
B. Varghese, T. G. van Leeuwen, and W. Steenbergen, “Coherence Domain Path Length Resolved Approaches in Optical Doppler Flowmetry,” in Handbook of Interferometers: Research, Technology and Applications (Nova Science Publishers, Inc, 2009), 317–344.
M. S. Folgosi-Correa and G. E. C. Nogueira, “Time of Correlation of Low-Frequency Fluctuations in the Regional Laser Doppler Flow Signal From Human Skin,” in Biophotonics: Photonic Solutions for Better Health Care III, vol. 8427, ed. J. Popp, W. Drexler, V. V. Tuchin, and D. L. Matthews (SPIE, 2012), 84272D.
D. Bauer, R. Grebe, and A. Ehrlacher, “First Phase Microcirculatory Reaction to Mechanical Skin Irritation: A Three Layer Model of a Compliant Vascular Tree,” Journal of Theoretical Biology 232, no. 2 (2005): 249–260.
K. Mithraratne, H. Ho, P. Hunter, and J. Fernandez, “Mechanics of the Foot Part 2: A Coupled Solid-Fluid Model to Investigate Blood Transport in the Pathologic Foot,” International Journal for Numerical Methods in Biomedical Engineering 28, no. 10 (2012): 1071–1081.
R. G. M. Breuls, C. V. C. Bouten, C. W. J. Oomens, D. L. Bader, and F. P. T. Baaijens, “A Theoretical Analysis of Damage Evolution in Skeletal Muscle Tissue With Reference to Pressure Ulcer Development,” Journal of Biomechanical Engineering 125, no. 6 (2003): 902–909.
R. G. M. Breuls, B. G. Sengers, C. W. J. Oomens, C. V. C. Bouten, and F. P. T. Baaijens, “Predicting Local Cell Deformations in Engineered Tissue Constructs: A Multilevel Finite Element Approach,” Journal of Biomechanical Engineering 124, no. 2 (2002): 198–207.
A. Lustig, R. Margi, A. Orlov, D. Orlova, L. Azaria, and A. Gefen, “The Mechanobiology Theory of the Development of Medical Device-Related Pressure Ulcers Revealed Through a Cell-Scale Computational Modeling Framework,” Biomechanics and Modeling in Mechanobiology 20, no. 3 (2021): 851–860.
K. Terzaghi, “Theoretical Soil Mechanics.” 1943.
S. Budday, T. C. Ovaert, G. A. Holzapfel, P. Steinmann, and E. Kuhl, “Fifty Shades of Brain: A Review on the Mechanical Testing and Modeling of Brain Tissue,” Archives of Computational Methods in Engineering 27, no. 4 (2019): 1187–1230.
M. Hosseini-Farid, M. Ramzanpour, J. McLean, M. Ziejewski, and G. Karami, “A Poro-Hyper-Viscoelastic Rate-Dependent Constitutive Modeling for the Analysis of Brain Tissues,” Journal of the Mechanical Behavior of Biomedical Materials 102 (2020): 103475.
A. Greiner, N. Reiter, F. Paulsen, et al., “Poro-Viscoelastic Effects During Biomechanical Testing of Human Brain Tissue,” Frontiers in Mechanical Engineering 7 (2021): 708350.
S. Urcun, D. Baroli, P.-Y. Rohan, et al., “Non-Operable Glioblastoma: Proposition of Patient-Specific Forecasting by Image-Informed Poromechanical Model,” Brain Multiphysics 4 (2023): 100067.
S. Urcun, P.-Y. Rohan, G. Sciumè, and S. P. Bordas, “Cortex Tissue Relaxation and Slow to Medium Load Rates Dependency Can Be Captured by a Two-Phase Flow Poroelastic Model,” Journal of the Mechanical Behavior of Biomedical Materials 126 (2022): 104952.
S. Hervas-Raluy, B. Wirthl, P. E. Guerrero, et al., “Tumour Growth: An Approach to Calibrate Parameters of a Multiphase Porous Media Model Based on in Vitro Observations of Neuroblastoma Spheroid Growth in a Hydrogel Microenvironment,” Computers in Biology and Medicine 159 (2023): 106895.
A. Carrasco-Mantis, T. Randelovic, H. Castro-Abril, I. Ochoa, M. Doblaré, and J. A. Sanz-Herrera, “A Mechanobiological Model for Tumor Spheroid Evolution With Application to Glioblastoma: A Continuum Multiphysics Approach,” Computers in Biology and Medicine 159 (2023): 106897.
M. de Lucio, Y. Leng, H. Wang, P. P. Vlachos, and H. Gomez, “Modeling Drug Transport and Absorption in Subcutaneous Injection of Monoclonal Antibodies: Impact of Tissue Deformation, Devices, and Physiology,” International Journal of Pharmaceutics 661 (2024): 124446.
T. Ricken and L. Lambers, “On Computational Approaches of Liver Lobule Function and Perfusion Simulation,” GAMM-Mitteilungen 42, no. 4 (2019): e201900016.
M. Kazemi, Y. Dabiri, and L. P. Li, “Recent Advances in Computational Mechanics of the Human Knee Joint,” Computational and Mathematical Methods in Medicine 2013 (2013): 1–27.
S. Uzuner, L. Li, S. Kucuk, and K. Memisoglu, “Changes in Knee Joint Mechanics After Medial Meniscectomy Determined With a Poromechanical Model,” Journal of Biomechanical Engineering 142, no. 10 (2020): 101006.
R. Bulle, “A posteriori error estimation for finite element approximations of fractional Laplacian problems and applications to poro-elasticity. Theses, Université Bourgogne Franche-Comté; Université du Luxembourg.” 2022.
R. Bulle, G. Alotta, G. Marchiori, et al., “The Human Meniscus Behaves as a Functionally Graded Fractional Porous Medium Under Confined Compression Conditions,” Applied Sciences 11, no. 20 (2021): 9405.
S. Uzuner, G. Kuntze, L. Li, J. Ronsky, and S. Kucuk, “Creep Behavior of Human Knee Joint Determined With High-Speed Biplanar Video-Radiography and Finite Element Simulation,” Journal of the Mechanical Behavior of Biomedical Materials 125 (2022): 104905.
T. Lavigne, G. Sciumè, S. Laporte, et al., “Société de biomécanique Young Investigator Award 2021: Numerical Investigation of the Time-Dependent Stress–Strain Mechanical Behaviour of Skeletal Muscle Tissue in the Context of Pressure Ulcer Prevention,” Clinical Biomechanics 93 (2022): 105592.
G. Sciumè, “Mechanistic Modeling of Vascular Tumor Growth: An Extension of Biot's Theory to Hierarchical Bi-Compartment Porous Medium Systems,” Acta Mechanica 232, no. 4 (2021): 1445–1478.
S. Urcun, P.-Y. Rohan, W. Skalli, P. Nassoy, S. P. A. Bordas, and G. Sciumè, “Digital Twinning of Cellular Capsule Technology: Emerging Outcomes From the Perspective of Porous Media Mechanics,” PLoS One 16, no. 7 (2021): e0254512.
M. de Lucio, Y. Leng, A. Hans, et al., “Modeling Large-Volume Subcutaneous Injection of Monoclonal Antibodies With Anisotropic Porohyperelastic Models and Data-Driven Tissue Layer Geometries,” Journal of the Mechanical Behavior of Biomedical Materials 138 (2023): 105602.
Y. Fang, J. Cui, J. Xu, J. Ma, Z. Liu, and H. Zhang, “Research Progress and Clinical Application of Laser Doppler Blood Flow Measurement Technology,” Proceedings of SPIE-The International Society for Optical Engineering 13182 (2024): 131822B.
T. Pedanekar, R. Kedare, and A. Sengupta, “Monitoring Tumor Progression by Mapping Skin Microcirculation With Laser Doppler Flowmetry,” Lasers in Medical Science 34, no. 1 (2018): 61–77.
B. Fromy, P. Abraham, and J.-L. Saumet, “Non-Nociceptive Capsaicin-Sensitive Nerve Terminal Stimulation Allows for an Original Vasodilatory Reflex in the Human Skin,” Brain Research 811, no. 1–2 (1998): 166–168.
B. Fromy, P. Abraham, and J.-L. Saumet, “Progressive Calibrated Pressure Device to Measure Cutaneous Blood Flow Changes to External Pressure Strain,” Brain Research Protocols 5, no. 2 (2000): 198–203.
T. Lavigne, S. Urcun, P.-Y. Rohan, G. Sciumè, D. Baroli, and S. P. Bordas, “Single and Bi-Compartment Poro-Elastic Model of Perfused Biological Soft Tissues: FEniCSx Implementation and Tutorial,” Journal of the Mechanical Behavior of Biomedical Materials 143 (2023): 105902.
G. Sciumè, D. P. Boso, W. G. Gray, C. Cobelli, and B. A. Schrefler, “A Two-Phase Model of Plantar Tissue: A Step Toward Prediction of Diabetic Foot Ulceration,” International Journal for Numerical Methods in Biomedical Engineering 30, no. 11 (2014): 1153–1169.
A. Wahlsten, M. Pensalfini, A. Stracuzzi, G. Restivo, R. Hopf, and E. Mazza, “On the Compressibility and Poroelasticity of Human and Murine Skin,” Biomechanics and Modeling in Mechanobiology 18, no. 4 (2019): 1079–1093.
G. Sciumè, M. Ferrari, and B. A. Schrefler, “Saturation–Pressure Relationships for Two- and Three-Phase Flow Analogies for Soft Matter,” Mechanics Research Communications 62 (2014): 132–137.
G. Sciumè, R. Santagiuliana, M. Ferrari, P. Decuzzi, and B. Schrefler, “A Tumor Growth Model With Deformable Ecm,” Physical Biology 11, no. 6 (2014): 065004.
W. G. Gray and C. T. Miller, Introduction to the Thermodynamically Constrained Averaging Theory for Porous Medium Systems (Springer, 2014).
I. A. Baratta, J. P. Dean, J. S. Dokken, et al., “Dolfinx: The next generation fenics problem solving environment.” 2023.
M. Alnæs, J. Blechta, J. Hake, et al., “The Fenics Project Version 1.5,” Archive of Numerical Software 3 (2015) Starting Point and Frequency: Year: 2013.
C. Geuzaine and J. Remacle, “Gmsh: A 3-d Finite Element Mesh Generator With Built-In Pre- and Post-Processing Facilities,” International Journal for Numerical Methods in Engineering 79, no. 11 (2009): 1309–1331.
A. Kallepalli, J. Halls, D. B. James, and M. A. Richardson, “An Ultrasonography-Based Approach for Tissue Modelling to Inform Photo-Therapy Treatment Strategies,” Journal of Biophotonics 15, no. 4 (2022): e202100275.
A. Humeau-Heurtier, E. Guerreschi, P. Abraham, and G. Mahé, “Relevance of Laser Doppler and Laser Speckle Techniques for Assessing Vascular Function: State of the Art and Future Trends,” IEEE Transactions on Biomedical Engineering 60, no. 3 (2013): 659–666.
I. Fredriksson, M. Larsson, and T. Strömberg, “Measurement Depth and Volume in Laser Doppler Flowmetry,” Microvascular Research 78, no. 1 (2009): 4–13.
A. Fedorovich, O. Drapkina, K. Pronko, V. Sinopalnikov, and V. Zemskov, Telemonitoring of Capillary Blood Flow in the Human Skin: New Opportunities and Prospects (Clinical Practice, 2018).
M. Rossi, A. Carpi, F. Galetta, F. Franzoni, and G. Santoro, “The Investigation of Skin Blood Flowmotion: A New Approach to Study the Microcirculatory Impairment in Vascular Diseases?,” Biomedicine & Pharmacotherapy 60, no. 8 (2006): 437–442.
B. Fagrell, A. Fronek, and M. Intaglietta, “A Microscope-Television System for Studying Flow Velocity in Human Skin Capillaries,” American Journal of Physiology. Heart and Circulatory Physiology 233, no. 2 (1977): H318–H321.
E. Mukhina, P.-Y. Rohan, N. Connesson, and Y. Payan, “Calibration of the Fat and Muscle Hyperelastic Material Parameters for the Assessment of the Internal Tissue Deformation in Relation to Pressure Ulcer Prevention,” Computer Methods in Biomechanics and Biomedical Engineering 23, no. sup1 (2020): S197–S199.
A. Kalra and A. Lowe, “Mechanical Behaviour of Skin: A Review,” Journal of Materials Science and Engineering 5, no. 4 (2016).
C. Pailler-Mattei, S. Bec, and H. Zahouani, “In Vivo Measurements of the Elastic Mechanical Properties of Human Skin by Indentation Tests,” Medical Engineering & Physics 30, no. 5 (2008): 599–606.
T. Raveh Tilleman, M. Tilleman, and H. Neumann, “The Elastic Properties of Cancerous Skin: Poisson's Ratio and Young's Modulus,” Optimization of Incisions in Cutaneous Surgery Including Mohs' Micrographic Surgery 105, no. 2 (2004): 753–755.
P. Lakhani, K. K. Dwivedi, A. Parashar, and N. Kumar, “Non-Invasive in Vivo Quantification of Directional Dependent Variation in Mechanical Properties for Human Skin,” Frontiers in Bioengineering and Biotechnology 9 (2021): 749492.
R. Sanders, “Torsional Elasticity of Human Skin in Vivo,” Pfl Gers Archiv European Journal of Physiology 342, no. 3 (1973): 255–260.
C. W. Oomens, M. van Vijven, and G. W. Peters, “Chapter 16–Skin Mechanics,” in Biomechanics of Living Organs, volume 1 of Translational Epigenetics, ed. Y. Payan and J. Ohayon (Academic Press, 2017), 347–357.
N. Nakagawa, M. Matsumoto, and S. Sakai, “In Vivo Measurement of the Water Content in the Dermis by Confocal Raman Spectroscopy,” Skin Research and Technology 16, no. 2 (2010): 137–141.
R. Oftadeh, B. K. Connizzo, H. T. Nia, C. Ortiz, and A. J. Grodzinsky, “Biological Connective Tissues Exhibit Viscoelastic and Poroelastic Behavior at Different Frequency Regimes: Application to Tendon and Skin Biophysics,” Acta Biomaterialia 70 (2018): 249–259.
R. Oftadeh, M. Azadi, M. Donovan, et al., “Poroelastic Behavior and Water Permeability of Human Skin at the Nanoscale,” PNAS Nexus 2, no. 8 (2023): pgad240.
Y. Leng, M. de Lucio, and H. Gomez, “Using Poro-Elasticity to Model the Large Deformation of Tissue During Subcutaneous Injection,” Computer Methods in Applied Mechanics and Engineering 384 (2021): 113919.
D. Han, Z. Huang, E. Rahimi, and A. M. Ardekani, “Solute Transport Across the Lymphatic Vasculature in a Soft Skin Tissue,” Biology 12, no. 7 (2023): 942.
H. Nogami, K. Komatsutani, T. Hirata, and R. Sawada, “Integrated Laser Doppler Blood Flowing Combining Optical Contact Force,” in 2019 International Conference on Electronics Packaging, ICEP 2019 (IEEE, 2019), 287–290.
A. Ajan, K. Roberg, I. Fredriksson, and J. Abtahi, “Reproducibility of Laser Doppler Flowmetry in Gingival Microcirculation. A Study on Six Different Protocols,” Microvascular Research 153 (2024): 104666.
A. A. Kouadio, F. Jordana, N. J. Koffi, P. Le Bars, and A. Soueidan, “The Use of Laser Doppler Flowmetry to Evaluate Oral Soft Tissue Blood Flow in Humans: A Review,” Archives of Oral Biology 86 (2018): 58–71.
J. S. Petrofsky and L. Berk, Skin Moisture and Heat Transfer (Springer Berlin Heidelberg, 2012), 561–580.
C. Mrowietz, R. Franke, G. Pindur, U. Wolf, and F. Jung, “Reference Range and Variability of Laser-Doppler-Fluxmetry,” Clinical Hemorheology and Microcirculation 67, no. 3–4 (2017): 347–353.
T. Borchardt, J. Ernst, A. Helmke, et al., “Effect of Direct Cold Atmospheric Plasma (di) on Microcirculation of Intact Skin in a Controlled Mechanical Environment,” Microcirculation 24, no. 8 (2017): e12399.
W. Fei, S. Xu, J. Ma, et al., “Fundamental Supply of Skin Blood Flow in the Chinese Han Population: Measurements by a Full-Field Laser Perfusion Imager,” Skin Research and Technology 24, no. 4 (2018): 656–662.
M. Saha, V. Dremin, I. Rafailov, A. Dunaev, S. Sokolovski, and E. Rafailov, “Wearable Laser Doppler Flowmetry Sensor: A Feasibility Study With Smoker and Non-Smoker Volunteers,” Biosensors 10, no. 12 (2020): 201.
M. V. Volkov, D. A. Kostrova, N. B. Margaryants, et al., “Evaluation of Blood Microcirculation Parameters by Combined Use of Laser Doppler Flowmetry and Videocapillaroscopy Methods,” in Saratov Fall Meeting 2016: Optical Technologies in Biophysics and Medicine XVIII, ed. V. V. Tuchin, E. A. Genina, D. E. Postnov, and V. L. Derbov (SPIE, 2017), 1033607.
C. Mrowietz, R. Franke, G. Pindur, R. Sternitzky, F. Jung, and U. Wolf, “Evaluation of Laser-Doppler-Fluxmetry for the Diagnosis of Microcirculatory Disorders,” Clinical Hemorheology and Microcirculation 71, no. 2 (2019): 129–135.
D. Fuchs, P. P. Dupon, L. A. Schaap, and R. Draijer, “The Association Between Diabetes and Dermal Microvascular Dysfunction Non-Invasively Assessed by Laser Doppler With Local Thermal Hyperemia: A Systematic Review With Meta-Analysis,” Cardiovascular Diabetology 16, no. 1 (2017): 11.
G. V. Balasubramanian, N. Chockalingam, and R. Naemi, “The Role of Cutaneous Microcirculatory Responses in Tissue Injury, Inflammation and Repair at the Foot in Diabetes,” Frontiers in Bioengineering and Biotechnology 9 (2021): 732753.
J. Ostergren and B. Fagrell, “Skin Capillary Blood Cell Velocity in Man. Characteristics and Reproducibility of the Reactive Hyperemia Response,” International Journal of Microcirculation, Clinical and Experimental 5, no. 1 (1986): 37–51.
R. Argarini, K. J. Smith, H. H. Carter, L. H. Naylor, R. A. McLaughlin, and D. J. Green, “Visualizing and Quantifying the Impact of Reactive Hyperemia on Cutaneous Microvessels in Humans,” Journal of Applied Physiology 128, no. 1 (2020): 17–24.
M. Wang-Evers, M. J. Casper, J. Glahn, et al., “Assessing the Impact of Aging and Blood Pressure on Dermal Microvasculature by Reactive Hyperemia Optical Coherence Tomography Angiography,” Scientific Reports 11, no. 1 (2021): 13411.
J.-L. Cracowski, C. T. Minson, M. Salvat-Melis, and J. R. Halliwill, “Methodological Issues in the Assessment of Skin Microvascular Endothelial Function in Humans,” Trends in Pharmacological Sciences 27, no. 9 (2006): 503–508.
S. Golay, C. Haeberli, A. Delachaux, et al., “Local Heating of Human Skin Causes Hyperemia Without Mediation by Muscarinic Cholinergic Receptors or Prostanoids,” Journal of Applied Physiology 97, no. 5 (2004): 1781–1786.
P. J. Choi, V. E. Brunt, N. Fujii, and C. T. Minson, “New Approach to Measure Cutaneous Microvascular Function: An Improved Test of No-Mediated Vasodilation by Thermal Hyperemia,” Journal of Applied Physiology 117, no. 3 (2014): 277–283.
B. J. Wong, S. J. Williams, and C. T. Minson, “Minimal Role for h1and h2histamine Receptors in Cutaneous Thermal Hyperemia to Local Heating in Humans,” Journal of Applied Physiology 100, no. 2 (2006): 535–540.
R. Rosenberry and M. D. Nelson, “Reactive Hyperemia: A Review of Methods, Mechanisms, and Considerations,” American Journal of Physiology. Regulatory, Integrative and Comparative Physiology 318, no. 3 (2020): R605–R618.
T. Basiladze, G. Bekaia, N. Gongadze, and N. Mitagvaria, “Possible Mechanism of Hyperemia in the Skin Caused by Non-Painful Mechanical Pressure,” Georgian Medical News 238 (2015): 83–88.
F. Leo, T. Krenz, G. Wolff, et al., “Assessment of Tissue Perfusion and Vascular Function in Mice by Scanning Laser Doppler Perfusion Imaging,” Biochemical Pharmacology 176 (2020): 113893.
A. G. Horn, K. M. Schulze, R. E. Weber, et al., “Post-Occlusive Reactive Hyperemia and Skeletal Muscle Capillary Hemodynamics,” Microvascular Research 140 (2022): 104283.
E. Javadi, M. J. Armstrong, and S. Jamali, “A Fully Physiologically-Informed Time- and Rate-Dependent Hemorheological Constitutive Model,” Journal of Rheology 67, no. 3 (2023): 775–788.
J. Zhang, “Effect of Suspending Viscosity on Red Blood Cell Dynamics and Blood Flows in Microvessels,” Microcirculation 18, no. 7 (2011): 562–573.
O. Yalcin, D. Ortiz, A. T. Williams, P. C. Johnson, and P. Cabrales, “Perfusion Pressure and Blood Flow Determine Microvascular Apparent Viscosity,” Experimental Physiology 100, no. 8 (2015): 977–987.