Microvascular imaging: techniques and opportunities for clinical physiological measurements

The microvasculature presents a particular challenge in physiological measurement because the vessel structure is spatially inhomogeneous and perfusion can exhibit high variability over time. This review describes, with a clinical focus, the wide variety of methods now available for imaging of the microvasculature and their key applications. Laser Doppler perfusion imaging and laser speckle contrast imaging are established, commercially-available techniques for determining microvascular perfusion, with proven clinical utility for applications such as burn-depth assessment. Nailfold capillaroscopy is also commercially available, with significant published literature that supports its use for detecting microangiopathy secondary to specific connective tissue diseases in patients with Raynaud's phenomenon. Infrared thermography measures skin temperature and not perfusion directly, and it has only gained acceptance for some surgical and peripheral microvascular applications. Other emerging technologies including imaging photoplethysmography, optical coherence tomography, photoacoustic tomography, hyperspectral imaging, and tissue viability imaging are also described to show their potential as techniques that could become established tools for clinical microvascular assessment. Growing interest in the microcirculation has helped drive the rapid development in perfusion imaging of the microvessels, bringing exciting opportunities in microvascular research.

[1]  Atam P Dhawan,et al.  Optical Imaging Modalities for Biomedical Applications , 2010, IEEE Reviews in Biomedical Engineering.

[2]  L. O. Svaasand,et al.  Remote plethysmographic imaging using ambient light. , 2008, Optics express.

[3]  Andrew K. Dunn,et al.  Introduction: feature issue on In Vivo Microcirculation Imaging , 2011, Biomedical optics express.

[4]  R. Busto,et al.  Neuroprotective effect of treatment with human albumin in permanent focal cerebral ischemia: histopathology and cortical perfusion studies. , 2001, European journal of pharmacology.

[5]  M. Klonizakis,et al.  Assessment of Lower Limb Microcirculation: Exploring the Reproducibility and Clinical Application of Laser Doppler Techniques , 2011, Skin Pharmacology and Physiology.

[6]  G. Spencer-Green Outcomes in primary Raynaud phenomenon: a meta-analysis of the frequency, rates, and predictors of transition to secondary diseases. , 1998, Archives of internal medicine.

[7]  I. Baumgartner,et al.  Call for a reference model of chronic hind limb ischemia to investigate therapeutic angiogenesis. , 2009, Vascular pharmacology.

[8]  Brett E. Bouma,et al.  Optical Coherence Tomography , 2013 .

[9]  C. Aalkjær,et al.  Vasomotion – what is currently thought? , 2011, Acta physiologica.

[10]  N. Harris,et al.  Use of infrared thermography as an endpoint in therapeutic trials of Raynaud's phenomenon and systemic sclerosis. , 2012, Clinical and experimental rheumatology.

[11]  P. Farr,et al.  The study of plaques of psoriasis using a scanning laser‐Doppler velocimeter , 1993, The British journal of dermatology.

[12]  K. A. Townsend,et al.  Validation of spectral domain optical coherence tomographic Doppler shifts using an in vitro flow model. , 2009, Investigative ophthalmology & visual science.

[13]  R. Nagai,et al.  Angiogenic Effects of Adrenomedullin in Ischemia and Tumor Growth , 2004, Circulation research.

[14]  T. Moore,et al.  An investigation into the blood‐flow characteristics of telangiectatic skin lesions in systemic sclerosis using dual‐wavelength laser Doppler imaging , 2009, Clinical and experimental dermatology.

[15]  N D Harris,et al.  Comparison of infrared thermography and laser speckle contrast imaging for the dynamic assessment of digital microvascular function. , 2012, Microvascular research.

[16]  F. M. van den Engh,et al.  Initial results of in vivo non-invasive cancer imaging in the human breast using near-infrared photoacoustics. , 2007, Optics express.

[17]  Tuan Vo-Dinh,et al.  Biomedical Photonics Handbook , 2003 .

[18]  F. Mastik,et al.  Contactless Multiple Wavelength Photoplethysmographic Imaging: A First Step Toward “SpO2 Camera” Technology , 2005, Annals of Biomedical Engineering.

[19]  Anthony J. Durkin,et al.  Noninvasive clinical assessment of port‐wine stain birthmarks using current and future optical imaging technology: a review , 2012, The British journal of dermatology.

[20]  J. Fujimoto,et al.  Optical coherence tomography: an emerging technology for biomedical imaging and optical biopsy. , 2000, Neoplasia.

[21]  R. Bray,et al.  Neural stimulation does not mediate attenuated vascular response in ACL‐deficient knees: Potential role of local inflammatory mediators , 2009, Journal of orthopaedic research : official publication of the Orthopaedic Research Society.

[22]  Sergio Calixto-Carrera,et al.  Novel approach to assess the emissivity of the human skin. , 2009, Journal of biomedical optics.

[23]  Mark A. Richardson,et al.  An introduction to hyperspectral imaging and its application for security, surveillance and target acquisition , 2010 .

[24]  Alexei A. Kamshilin,et al.  Photoplethysmographic imaging of high spatial resolution , 2011, Biomedical optics express.

[25]  G. Nilsson,et al.  Laser Doppler perfusion imaging by dynamic light scattering , 1993, IEEE Transactions on Biomedical Engineering.

[26]  J A Crowe,et al.  64×64 pixel smart sensor array for laser Doppler blood flow imaging. , 2012, Optics letters.

[27]  D. Boas,et al.  Laser speckle contrast imaging in biomedical optics. , 2010, Journal of biomedical optics.

[28]  Jean-Philippe Sylvestre,et al.  A prototype hyperspectral system with a tunable laser source for retinal vessel imaging. , 2013, Investigative ophthalmology & visual science.

[29]  Janis Spigulis,et al.  Real-Time Photoplethysmography Imaging System , 2011 .

[30]  L. V. Doronina-Amitonova,et al.  Neurophotonics: optical methods to study and control the brain , 2015 .

[31]  Lihong V. Wang,et al.  Prospects of photoacoustic tomography. , 2008, Medical physics.

[32]  Conrad Kufta,et al.  Intraoperative infrared functional imaging of human brain , 2003, Annals of neurology.

[33]  P. Woo,et al.  Validation of a protocol for the assessment of skin temperature and blood flow in childhood localised scleroderma , 2009, Skin research and technology : official journal of International Society for Bioengineering and the Skin (ISBS) [and] International Society for Digital Imaging of Skin (ISDIS) [and] International Society for Skin Imaging.

[34]  T. King,et al.  Comparison of red and green laser doppler imaging of blood flow , 2004, Lasers in surgery and medicine.

[35]  J. Belch,et al.  Assessment of microvascular endothelial function in human skin. , 2001, Clinical science.

[36]  Anne Humeau-Heurtier,et al.  Blood Perfusion Values of Laser Speckle Contrast Imaging and Laser Doppler Flowmetry: Is a Direct Comparison Possible? , 2013, IEEE Transactions on Biomedical Engineering.

[37]  Lihong V. Wang,et al.  Neurovascular Photoacoustic Tomography , 2010, Front. Neuroenerg..

[38]  J G Flanagan,et al.  Regional variation in human retinal vessel oxygen saturation. , 2013, Experimental eye research.

[39]  P Dunnill,et al.  Doppler optical coherence tomography for measuring flow in engineered tissue. , 2004, Biosensors & bioelectronics.

[40]  C. O’Boyle,et al.  Man or Machine? The Clinimetric Properties of Laser Doppler Imaging in Burn Depth Assessment , 2011, Journal of burn care & research : official publication of the American Burn Association.

[41]  W. Ferrell,et al.  Novel use of laser Doppler imaging for investigating epicondylitis. , 2000, Rheumatology.

[42]  T. Moore,et al.  Pilot study of dual‐wavelength (532 and 633 nm) laser Doppler imaging and infrared thermography of morphoea , 2009, British Journal of Dermatology.

[43]  A C Shore,et al.  Capillaroscopy and the measurement of capillary pressure. , 2000, British journal of clinical pharmacology.

[44]  Huabei Jiang,et al.  4-D Photoacoustic Tomography , 2013, Scientific Reports.

[45]  C. Stehouwer,et al.  Microvascular dysfunction: An emerging pathway in the pathogenesis of obesity-related insulin resistance , 2013, Reviews in Endocrine and Metabolic Disorders.

[46]  E F Ring,et al.  Prostaglandin E1 infusions for vascular insufficiency in progressive systemic sclerosis. , 1981, Annals of the rheumatic diseases.

[47]  Anne Humeau-Heurtier,et al.  Assessment of Skin Microvascular Function and Dysfunction With Laser Speckle Contrast Imaging , 2012, Circulation. Cardiovascular imaging.

[48]  Nahum Gat,et al.  Imaging spectroscopy using tunable filters: a review , 2000, SPIE Defense + Commercial Sensing.

[49]  O. Airaksinen,et al.  Reproducibility of infrared thermography measurements in healthy individuals , 2008, Physiological measurement.

[50]  Panagiotis Artemiadis,et al.  A hybrid BMI-based exoskeleton for paresis: EMG control for assisting arm movements , 2017, Journal of neural engineering.

[51]  J. Belch,et al.  Enhanced sensitivity of the peripheral cholinergic vascular response in patients with chronic fatigue syndrome. , 2000, The American journal of medicine.

[52]  H. Svensson,et al.  Wound healing after total elbow replacement in rheumatoid arthritis. Wound complications in 50 cases and laser-Doppler imaging of skin microcirculation. , 1995, Acta orthopaedica Scandinavica.

[53]  John Allen Photoplethysmography and its application in clinical physiological measurement , 2007, Physiological measurement.

[54]  Alan Murray,et al.  Comparative reproducibility of dermal microvascular blood flow changes in response to acetylcholine iontophoresis, hyperthermia and reactive hyperaemia , 2010, Physiological measurement.

[55]  Ying Wang,et al.  Monitoring Microcirculation Changes in Port Wine Stains During Vascular Targeted Photodynamic Therapy by Laser Speckle Imaging , 2012, Photochemistry and photobiology.

[56]  V. Faria,et al.  SYSTEMATIC REVIEW OF LITERATURE , 2014 .

[57]  Lei Xi,et al.  Molecular photoacoustic tomography of breast cancer using receptor targeted magnetic iron oxide nanoparticles as contrast agents , 2014, Journal of biophotonics.

[58]  E. Ring,et al.  Quantitative Thermal Imaging to Assess Inositol Nicotinate Treatment for Raynaud's Syndrome , 1981, The Journal of international medical research.

[59]  H. Maricq,et al.  Patterns of finger capillary abnormalities in connective tissue disease by "wide-field" microscopy. , 1973, Arthritis and rheumatism.

[60]  A. Douplik,et al.  In vivo real time monitoring of vasoconstriction and vasodilation by a combined diffuse reflectance spectroscopy and Doppler optical coherence tomography approach , 2008, Lasers in surgery and medicine.

[61]  Phillip Blondeel,et al.  Assessment of burn depth and burn wound healing potential. , 2008, Burns : journal of the International Society for Burn Injuries.

[62]  A. Herrick,et al.  Quantifying digital vascular disease in patients with primary Raynaud’s phenomenon and systemic sclerosis , 1998, Annals of the rheumatic diseases.

[63]  N. Harris,et al.  Microvascular responses following digital thermal hyperaemia and iontophoresis measured by laser Doppler imaging in idiopathic inflammatory myopathy. , 2007, Rheumatology.

[64]  M. Sivak,et al.  Computer-aided diagnosis of dysplasia in Barrett's esophagus using endoscopic optical coherence tomography. , 2006 .

[65]  Geng Ku,et al.  Three-dimensional combined photoacoustic and optical coherence microscopy for in vivo microcirculation studies. , 2009, Optics express.

[66]  Pranab K. Dutta,et al.  Review of laser speckle-based analysis in medical imaging , 2012, Medical & Biological Engineering & Computing.

[67]  R. Freeman,et al.  Endothelial dysfunction and the expression of endothelial nitric oxide synthetase in diabetic neuropathy, vascular disease, and foot ulceration. , 1998, Diabetes.

[68]  Alexei A. Kamshilin,et al.  Variability of Microcirculation Detected by Blood Pulsation Imaging , 2013, PloS one.

[69]  Dynamic microvascular responses with a high speed TiVi imaging system , 2011, Journal of biophotonics.

[70]  A. Yodh,et al.  Diffuse Optical Tomography of Cerebral Blood Flow, Oxygenation, and Metabolism in Rat during Focal Ischemia , 2003, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[71]  H. Heidrich,et al.  Vital capillary microscopic findings in the nailfold of patients with diabetes mellitus. , 2000, VASA. Zeitschrift fur Gefasskrankheiten.

[72]  Vasilis Ntziachristos,et al.  Opto-acoustic imaging of drug discovery biomarkers. , 2012, Current pharmaceutical biotechnology.

[73]  M. Sivak,et al.  Image analysis for classification of dysplasia in Barrett’s esophagus using endoscopic optical coherence tomography , 2010, Biomedical optics express.

[74]  Jitendrakumar K Patel,et al.  Newer technologies/techniques and tools in the diagnosis of melanoma. , 2008, European journal of dermatology : EJD.

[75]  T. Moore,et al.  Dual wavelength (532 and 633 nm) laser Doppler imaging of plaque psoriasis , 2005, The British journal of dermatology.

[76]  Kevin Howell,et al.  Guidelines for specifying and testing a thermal camera for medical applications , 1919 .

[77]  L. Arendt-Nielsen,et al.  Tissue viability imaging for assessment of pharmacologically induced vasodilation and vasoconstriction in human skin. , 2010, Microvascular research.

[78]  Thilo Gambichler,et al.  Applications of optical coherence tomography in dermatology. , 2005, Journal of dermatological science.

[79]  Marie-Louise O'Connell,et al.  Tissue viability (TiVi) imaging: temporal effects of local occlusion studies in the volar forearm , 2009, Journal of biophotonics.

[80]  J. Jeng,et al.  Burn wound healing time assessed by laser Doppler imaging (LDI). Part 1: Derivation of a dedicated colour code for image interpretation. , 2012, Burns : journal of the International Society for Burn Injuries.

[81]  R. Gorodkin,et al.  Assessment of endothelial function in complex regional pain syndrome type I using iontophoresis and laser Doppler imaging. , 2004, Rheumatology.

[82]  Z. A. Awan,et al.  Human microvascular imaging: a review of skin and tongue videomicroscopy techniques and analysing variables , 2010, Clinical physiology and functional imaging.

[83]  Medical Imaging: Just What the Doctor (and the Researcher) Ordered: New Applications for Medical Imaging Technology , 2013, IEEE Pulse.

[84]  Akiko Maehara,et al.  Consensus standards for acquisition, measurement, and reporting of intravascular optical coherence tomography studies: a report from the International Working Group for Intravascular Optical Coherence Tomography Standardization and Validation. , 2012, Journal of the American College of Cardiology.

[85]  J. Isner,et al.  Transplantation of ex vivo expanded endothelial progenitor cells for therapeutic neovascularization. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[86]  K. Schomacker,et al.  Monitoring temporal development and healing of diabetic foot ulceration using hyperspectral imaging , 2011, Journal of biophotonics.

[87]  E. Van den kerckhove,et al.  A comparison between laser‐doppler imaging and colorimetry in the assessment of scarring: “a pilot study” , 2012, Skin research and technology : official journal of International Society for Bioengineering and the Skin (ISBS) [and] International Society for Digital Imaging of Skin (ISDIS) [and] International Society for Skin Imaging.

[88]  B. Wallin,et al.  Axon-reflex-mediated vasodilatation in the psoriatic plaque? , 1995, The Journal of investigative dermatology.

[89]  P. Dieppe,et al.  Treatment of Raynaud's phenomenon by intravenous infusion of prostacyclin (PGI2) , 1982, The British journal of dermatology.

[90]  Gangjun Liu,et al.  Advances in Doppler OCT. , 2013, Chinese optics letters : COL.

[91]  D. Coppola,et al.  Increased perfusion and angiogenesis in a hindlimb ischemia model with plasmid FGF-2 delivered by noninvasive electroporation , 2010, Gene Therapy.

[92]  H. Park,et al.  Nail bed hemorrhage: a clinical marker of optic disc hemorrhage in patients with glaucoma. , 2011, Archives of ophthalmology.

[93]  J. Mercer,et al.  Perfusion Dynamics of Free DIEP and SIEA Flaps During the First Postoperative Week Monitored With Dynamic Infrared Thermography , 2009, Annals of plastic surgery.

[94]  B. Hoogwerf,et al.  Evaluation of Diabetic Foot Ulcer Healing With Hyperspectral Imaging of Oxyhemoglobin and Deoxyhemoglobin , 2009, Diabetes Care.

[95]  E. Uhl,et al.  Hyperbaric oxygen improves wound healing in normal and ischemic skin tissue. , 1994, Plastic and reconstructive surgery.

[96]  Graham Dunn,et al.  Comparison of thermography and laser Doppler imaging in the assessment of Raynaud's phenomenon. , 2003, Microvascular research.

[97]  B. Hazleman,et al.  Prolonged effect of CGRP in Raynaud's patients: a double-blind randomised comparison with prostacyclin. , 1991, British journal of clinical pharmacology.

[98]  Maurizio Cutolo,et al.  The contribution of capillaroscopy to the differential diagnosis of connective autoimmune diseases. , 2007, Best practice & research. Clinical rheumatology.

[99]  Faisel Khan,et al.  Laser Doppler Imaging in the Investigation of Lower Limb Wounds , 2003, The international journal of lower extremity wounds.

[100]  L. Devgan,et al.  Modalities for the Assessment of Burn Wound Depth , 2006, Journal of burns and wounds.

[101]  A. Herrick Diagnosis and management of scleroderma peripheral vascular disease. , 2008, Rheumatic diseases clinics of North America.

[102]  Sven Weum,et al.  The Value of Dynamic Infrared Thermography (DIRT) in Perforator Selection and Planning of Free DIEP Flaps , 2009, Annals of plastic surgery.

[103]  Lihong V. Wang,et al.  Photoacoustic imaging and characterization of the microvasculature. , 2010, Journal of biomedical optics.

[104]  Q. Luo,et al.  Laser speckle imaging of blood flow in microcirculation. , 2004, Physics in medicine and biology.

[105]  N. Harris,et al.  Scanning laser Doppler imaging may predict disease progression of localized scleroderma in children and young adults , 2013, The British journal of dermatology.

[106]  C. Hutchinson,et al.  Vascular imaging. , 2004, Best practice & research. Clinical rheumatology.

[107]  A. Merla,et al.  Combined Thermal and Laser Doppler Imaging in the Assessment of Cutaneous Tissue Perfusion , 2007, 2007 29th Annual International Conference of the IEEE Engineering in Medicine and Biology Society.

[108]  T. Moore,et al.  Digital iontophoresis of vasoactive substances as measured by laser Doppler imaging--a non-invasive technique by which to measure microvascular dysfunction in Raynaud's phenomenon. , 2004, Rheumatology.

[109]  Niels-Henrik Holstein-Rathlou,et al.  Nephron blood flow dynamics measured by laser speckle contrast imaging. , 2011, American journal of physiology. Renal physiology.

[110]  Zijing Du,et al.  A study of blood flow dynamics in flap delay using the full-field laser perfusion imager. , 2011, Microvascular research.

[111]  S. Wilson,et al.  Hyperspectral image measurements of skin hemoglobin compared with transcutaneous PO2 measurements. , 2012, Annals of vascular surgery.

[112]  Evelyn Regar,et al.  Optical coherence tomography for evaluation of coronary stents in vivo , 2013, Expert review of cardiovascular therapy.

[113]  H. Svensson,et al.  Sympathetic and parasympathetic neuropathy are frequent in both type 1 and type 2 diabetic patients. , 2004, Diabetes care.

[114]  W. Nyka,et al.  Decreased Reactivity of Skin Microcirculation in Response to l-Arginine in Later-Onset Type 1 Diabetes , 2013, Diabetes Care.

[115]  Comparison of tissue viability imaging and colorimetry: skin blanching , 2009, Skin research and technology : official journal of International Society for Bioengineering and the Skin (ISBS) [and] International Society for Digital Imaging of Skin (ISDIS) [and] International Society for Skin Imaging.

[116]  Shigeki Nakauchi,et al.  Detection and visualization of intracutaneous allergic type‐specific elements using long‐wavelength near‐infrared hyperspectral imaging , 2013, Skin research and technology : official journal of International Society for Bioengineering and the Skin (ISBS) [and] International Society for Digital Imaging of Skin (ISDIS) [and] International Society for Skin Imaging.

[117]  J. Briers,et al.  Laser Doppler, speckle and related techniques for blood perfusion mapping and imaging. , 2001, Physiological measurement.

[118]  Liron Pantanowitz,et al.  Review of advanced imaging techniques , 2012, Journal of pathology informatics.

[119]  Andrew K. Dunn,et al.  Laser Speckle Contrast Imaging of Cerebral Blood Flow , 2011, Annals of Biomedical Engineering.

[120]  F. Trautinger,et al.  Capillaroscopy of toes , 2013, Journal der Deutschen Dermatologischen Gesellschaft = Journal of the German Society of Dermatology : JDDG.

[121]  M. Leahy,et al.  Sub‐epidermal imaging using polarized light spectroscopy for assessment of skin microcirculation , 2007, Skin research and technology : official journal of International Society for Bioengineering and the Skin (ISBS) [and] International Society for Digital Imaging of Skin (ISDIS) [and] International Society for Skin Imaging.

[122]  Claes L. Asker,et al.  Microvascular arteriovenous shunting is a probable pathogenetic mechanism in erythromelalgia. , 2000, The Journal of investigative dermatology.

[123]  Joakim Henricson,et al.  Hyperaemic changes in forearm skin perfusion and RBC concentration after increasing occlusion times. , 2010, Microvascular research.

[124]  D. Sainsbury Critical evaluation of the clinimetrics of laser Doppler imaging in burn assessment. , 2008, Journal of wound care.

[125]  Leslie Mertz,et al.  Technology Comes to the Playing Field: New World of Sports Promises Fewer Injuries, Better Performance , 2013, IEEE Pulse.

[126]  Patricia A. Broderick,et al.  Biosensors for Brain Trauma and Dual Laser Doppler Flowmetry: Enoxaparin Simultaneously Reduces Stroke-Induced Dopamine and Blood Flow while Enhancing Serotonin and Blood Flow in Motor Neurons of Brain, In Vivo , 2010, Sensors.

[127]  M Roustit,et al.  Excellent reproducibility of laser speckle contrast imaging to assess skin microvascular reactivity. , 2010, Microvascular research.

[128]  Stephen A. Boppart,et al.  Optical coherence tomography for rapid tissue screening and directed histological sectioning. , 2013, Studies in health technology and informatics.

[129]  Thomas M van Gulik,et al.  Real-time assessment of renal cortical microvascular perfusion heterogeneities using near-infrared laser speckle imaging. , 2010, Optics express.

[130]  C. Millet,et al.  Aging is associated with a diminished axon reflex response to local heating on the gaiter skin area. , 2012, Microvascular research.

[131]  L. Fabricio,et al.  Periungual capillaroscopy in psoriasis. , 2012, Anais brasileiros de dermatologia.

[132]  Zhongping Chen,et al.  Visualization and measurement of capillary-driven blood flow using spectral domain optical coherence tomography , 2012, Microfluidics and nanofluidics.

[133]  Yu Sun,et al.  Use of ambient light in remote photoplethysmographic systems: comparison between a high-performance camera and a low-cost webcam. , 2012, Journal of biomedical optics.

[134]  J S Beck,et al.  A preliminary assessment of laser Doppler perfusion imaging in human skin using the tuberculin reaction as a model. , 1993, Physiological measurement.

[135]  Theo Lasser,et al.  Real-time full field laser Doppler imaging , 2011, Biomedical optics express.

[136]  Nitish V Thakor,et al.  Longitudinal in vivo monitoring of rodent glioma models through thinned skull using laser speckle contrast imaging , 2012, Journal of biomedical optics.

[137]  Ofer Levi,et al.  Rapid monitoring of cerebral ischemia dynamics using laser-based optical imaging of blood oxygenation and flow , 2012, Biomedical optics express.

[138]  I. Winship,et al.  Laser Speckle Contrast Imaging of Collateral Blood Flow during Acute Ischemic Stroke , 2010, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[139]  Maurizio Cutolo,et al.  Assessing microvascular changes in systemic sclerosis diagnosis and management , 2010, Nature Reviews Rheumatology.

[140]  Maurizio Cutolo,et al.  How to perform and interpret capillaroscopy. , 2013, Best practice & research. Clinical rheumatology.

[141]  Örjan Smedby,et al.  Real-time intraoperative visualization of myocardial circulation using augmented reality temperature display , 2013, The International Journal of Cardiovascular Imaging.

[142]  P. Messina,et al.  Microcirculation in the healing of surgical wounds in the oral cavity. , 2013, International journal of oral and maxillofacial surgery.

[143]  P. Emery,et al.  Virtual skin biopsy by optical coherence tomography: the first quantitative imaging biomarker for scleroderma , 2013, Annals of the rheumatic diseases.

[144]  T. Pullar,et al.  Investigation of cutaneous microvascular activity and flare response in patients with fibromyalgia syndrome. , 2001, Rheumatology.

[145]  C. Taylor,et al.  Noninvasive imaging techniques in the assessment of scleroderma spectrum disorders. , 2009, Arthritis and rheumatism.

[146]  Xueding Wang,et al.  Photoacoustic tomography to identify inflammatory arthritis , 2012, Journal of biomedical optics.

[147]  A. Seifalian,et al.  Comparison of laser Doppler perfusion imaging, laser Doppler flowmetry, and thermographic imaging for assessment of blood flow in human skin. , 1994, European journal of vascular surgery.

[148]  D. Pollock,et al.  Acute effects of periarterial sympathectomy on the cutaneous microcirculation , 1997, Journal of orthopaedic research : official publication of the Orthopaedic Research Society.

[149]  G. Clough,et al.  Comparison of the effects of levocetirizine and loratadine on histamine‐induced wheal, flare, and itch in human skin , 2001, Allergy.

[150]  Heidrich,et al.  Vitalkapillarmikroskopische Befunde am Nagelfalz bei Diabetes mellitus , 2013 .

[151]  Iveta Waczulíková,et al.  Healing process of venous ulcers: the role of microcirculation , 2013, International wound journal.

[152]  Stephen A. Boppart,et al.  Imaging developing neural morphology using optical coherence tomography , 1996, Journal of Neuroscience Methods.

[153]  Moustapha Hamdi,et al.  Accuracy of early burn depth assessment by laser Doppler imaging on different days post burn. , 2009, Burns : journal of the International Society for Burn Injuries.

[154]  Bernard Choi,et al.  Blood flow dynamics after laser therapy of port wine stain birthmarks , 2009, BiOS.

[155]  M. Roustit,et al.  Skin microvascular endothelial function as a biomarker in cardiovascular diseases? , 2015, Pharmacological reports : PR.

[156]  Roy Kalawsky,et al.  Noncontact imaging photoplethysmography to effectively access pulse rate variability , 2012, Journal of biomedical optics.

[157]  Can Ince,et al.  Validation of near-infrared laser speckle imaging for assessing microvascular (re)perfusion. , 2010, Microvascular research.

[158]  W Feng,et al.  Influence of overlying tissue and probe geometry on the sensitivity of a near-infrared tissue oximeter. , 2001, Physiological measurement.

[159]  B. Hazleman,et al.  Placebo controlled study showing therapeutic benefit of iloprost in the treatment of Raynaud's phenomenon. , 1992, The Journal of rheumatology.

[160]  C H Chang,et al.  Use of dynamic capillaroscopy for studying cutaneous microcirculation in patients with diabetes mellitus. , 1997, Microvascular research.

[161]  Junjie Yao,et al.  Photoacoustic tomography: fundamentals, advances and prospects. , 2011, Contrast media & molecular imaging.

[162]  Sijung Hu,et al.  Development of effective photoplethysmographic measurement techniques: From contact to non-contact and from point to imaging , 2009, 2009 Annual International Conference of the IEEE Engineering in Medicine and Biology Society.

[163]  M. Gomes,et al.  Antihypertensive Treatment Improves Microvascular Rarefaction and Reactivity in Low‐Risk Hypertensive Individuals , 2013, Microcirculation.

[164]  Folke Sjöberg,et al.  Assessing paediatric scald injuries using Laser Speckle Contrast Imaging. , 2013, Burns : journal of the International Society for Burn Injuries.

[165]  John A. Detre,et al.  Laser Doppler Imaging of Activation-Flow Coupling in the Rat Somatosensory Cortex , 1999, NeuroImage.

[166]  Mohammad Sultan Mahmud,et al.  Review of speckle and phase variance optical coherence tomography to visualize microvascular networks , 2013, Journal of biomedical optics.

[167]  T. King,et al.  Laser doppler imaging--a new technique for quantifying microcirculatory flow in patients with primary Raynaud's phenomenon and systemic sclerosis. , 1999, Microvascular research.

[168]  P. Bacon,et al.  Nailfold capillary microscopy in healthy children and in childhood rheumatic diseases: a prospective single blind observational study , 2003, Annals of the rheumatic diseases.

[169]  B. Falkner,et al.  Non-invasive assessment of microvascular and endothelial function. , 2013, Journal of visualized experiments : JoVE.

[170]  Douglas J. Fox,et al.  Laser speckle contrast imaging of cerebral blood flow in humans during neurosurgery: a pilot clinical study. , 2010, Journal of biomedical optics.

[171]  Paul McNamara,et al.  Comparison of instruments for investigation of microcirculatory blood flow and red blood cell concentration. , 2009, Journal of biomedical optics.

[172]  C A Hajivassiliou,et al.  Non‐invasive measurement of colonic blood flow distribution using laser Doppler imaging , 1998, The British journal of surgery.

[173]  Laser Doppler assessment of dermal circulatory changes in people with coronary artery disease. , 2012, Microvascular research.

[174]  A. Shore,et al.  The effect of acetylcholine on finger capillary pressure and capillary flow in healthy volunteers. , 1996, The Journal of physiology.

[175]  J. Jeng,et al.  Burn wound healing time assessed by laser Doppler imaging. Part 2: validation of a dedicated colour code for image interpretation. , 2011, Burns : journal of the International Society for Burn Injuries.

[176]  C. Millet,et al.  Comparison between laser speckle contrast imaging and laser Doppler imaging to assess skin blood flow in humans. , 2011, Microvascular research.

[177]  J. Belch,et al.  Differences in Endothelial Function and Vascular Reactivity between Scottish and Arabic Populations , 2003, Scottish medical journal.

[178]  G. Clough Role of nitric oxide in the regulation of microvascular perfusion in human skin in vivo , 1999, The Journal of physiology.

[179]  R. Trapp,et al.  Nailfold capillaroscopy in type I diabetics with vasculopathy and limited joint mobility. , 1986, The Journal of rheumatology.

[180]  Bahar Davoudi,et al.  Noninvasive in vivo structural and vascular imaging of human oral tissues with spectral domain optical coherence tomography , 2012, Biomedical optics express.

[181]  A. Shore,et al.  Responses of the skin microcirculation to acetylcholine and sodium nitroprusside in patients with NIDDM , 1995, Diabetologia.

[182]  G. Kennedy,et al.  Low-grade inflammation and arterial wave reflection in patients with chronic fatigue syndrome. , 2008, Clinical science.

[183]  J. Briers,et al.  Comparison of laser speckle contrast imaging with laser Doppler for assessing microvascular function. , 2011, Microvascular research.

[184]  Fabian Kiessling,et al.  Non-invasive imaging for studying anti-angiogenic therapy effects , 2013, Thrombosis and Haemostasis.

[185]  Wiendelt Steenbergen,et al.  The Twente Photoacoustic Mammoscope: system overview and performance , 2005, Physics in medicine and biology.

[186]  Guolan Lu,et al.  Medical hyperspectral imaging: a review , 2014, Journal of biomedical optics.

[187]  Ulrich Dirnagl,et al.  Functional imaging with Laser Speckle Contrast Analysis: Vascular compartment analysis and correlation with Laser Doppler Flowmetry and somatosensory evoked potentials , 2006, Brain Research.

[188]  N. Verdonschot,et al.  Micromechanics of postmortem‐retrieved cement–bone interfaces , 2010, Journal of orthopaedic research : official publication of the Orthopaedic Research Society.

[189]  Jürgen Lademann,et al.  Evaluation of optical coherence tomography as a non‐invasive diagnostic tool in cutaneous wound healing , 2014, Skin research and technology : official journal of International Society for Bioengineering and the Skin (ISBS) [and] International Society for Digital Imaging of Skin (ISDIS) [and] International Society for Skin Imaging.

[190]  Kan-Zhi Liu,et al.  Assessment of Skin Flaps Using Optically Based Methods for Measuring Blood Flow and Oxygenation , 2005, Plastic and reconstructive surgery.

[191]  You-Gang Yang,et al.  Reconstruction of thermographic signals to map perforator vessels in humans , 2012, Quantitative infrared thermography journal.

[192]  Yiqun Zhu,et al.  Low resource processing algorithms for laser Doppler blood flow imaging. , 2011, Medical engineering & physics.

[193]  E. Ring,et al.  Infrared thermal imaging in medicine , 2012, Physiological measurement.

[194]  L. Liaudet,et al.  Comparison of skin microvascular reactivity with hemostatic markers of endothelial dysfunction and damage in type 2 diabetes , 2008, Vascular health and risk management.

[195]  S. Jacques Optical properties of biological tissues: a review , 2013, Physics in medicine and biology.

[196]  J. Belch,et al.  Current concepts in assessment of microvascular endothelial function using laser Doppler imaging and iontophoresis. , 2008, Trends in cardiovascular medicine.

[197]  Simon Wessely,et al.  Chronic Fatigue Syndrome , 1996, BMJ : British Medical Journal.

[198]  P. Gasser,et al.  Nailfold Videomicroscopy and Local Cold Test in Type I Diabetics , 1992, Angiology.

[199]  M. Dewhirst,et al.  Hyperspectral imaging of hemoglobin saturation in tumor microvasculature and tumor hypoxia development. , 2005, Journal of biomedical optics.

[200]  J Serup,et al.  Guidelines for visualization of cutaneous blood flow by laser Doppler perfusion imaging , 2002, Contact dermatitis.

[201]  R. Kruger,et al.  Photoacoustic ultrasound (PAUS)--reconstruction tomography. , 1995, Medical physics.

[202]  Sijung Hu,et al.  A study of opto-physiological modeling to quantify tissue absorbance in imaging photoplethysmography , 2010, 2010 Annual International Conference of the IEEE Engineering in Medicine and Biology.

[203]  Yu Sun,et al.  Motion-compensated noncontact imaging photoplethysmography to monitor cardiorespiratory status during exercise. , 2011, Journal of biomedical optics.

[204]  E. Rosato,et al.  Digital ischemic necrosis in a patient with systemic sclerosis: the role of laser Doppler perfusion imaging. , 2009, VASA. Zeitschrift fur Gefasskrankheiten.

[205]  Ivan Cordovil,et al.  Evaluation of systemic microvascular endothelial function using laser speckle contrast imaging. , 2012, Microvascular research.

[206]  T. Hotokebuchi,et al.  Evaluation of blood flow within the subchondral bone of the femoral head: Use of the laser speckle method at surgery for osteonecrosis , 1999, Journal of orthopaedic research : official publication of the Orthopaedic Research Society.

[207]  A. Murray,et al.  Chronic fatigue syndrome and impaired peripheral pulse characteristics on orthostasis–a new potential diagnostic biomarker , 2012, Physiological measurement.

[208]  Cutaneous bioengineering instrumentation standardization: the Tissue Viability Imager , 2009, Skin research and technology : official journal of International Society for Bioengineering and the Skin (ISBS) [and] International Society for Digital Imaging of Skin (ISDIS) [and] International Society for Skin Imaging.

[209]  Lei Xi,et al.  Miniature probe combining optical-resolution photoacoustic microscopy and optical coherence tomography for in vivo microcirculation study. , 2013, Applied optics.

[210]  Theo Lasser,et al.  High-speed laser Doppler perfusion imaging using an integrating CMOS image sensor. , 2005, Optics express.

[211]  I. C. Munch,et al.  Flow patterns on spectral‐domain optical coherence tomography reveal flow directions at retinal vessel bifurcations , 2014, Acta ophthalmologica.

[212]  A. Carlizza,et al.  Spinal Cord Stimulation: Predictive Parameters of Outcome in Patients Suffering From Critical Lower Limb Ischemia. A Preliminary Study , 2011, Neuromodulation : journal of the International Neuromodulation Society.

[213]  Christopher P. Denton,et al.  A comparison of infrared thermography (IRT) and full-field laser perfusion imaging (FLPI) for assessment of hand cold challenge and dermal inflammation , 2022 .

[214]  Jiann-Der Lee,et al.  Quantitative observation of focused-ultrasound-induced vascular leakage and deformation via fluorescein angiography and optical coherence tomography , 2013, Journal of biomedical optics.

[215]  P. Oberg,et al.  Use of a new laser Doppler flowmeter for measurement of capillary blood flow in skeletal muscle after bullet wounding. , 1979, Acta chirurgica Scandinavica. Supplementum.

[216]  P O Byrne,et al.  A laser Doppler scanner for imaging blood flow in skin. , 1991, Journal of biomedical engineering.

[217]  B Waeber,et al.  Reproducibility of laser Doppler imaging of skin blood flow as a tool to assess endothelial function. , 2000, Journal of cardiovascular pharmacology.

[218]  Yoshihiko Hamamoto,et al.  New method for detection of gastric cancer by hyperspectral imaging: a pilot study , 2013, Journal of biomedical optics.

[219]  M. Gladwin,et al.  Imaging hemoglobin oxygen saturation in sickle cell disease patients using noninvasive visible reflectance hyperspectral techniques: effects of nitric oxide. , 2003, American journal of physiology. Heart and circulatory physiology.

[220]  Ramiro S. Maldonado,et al.  The use of optical coherence tomography in intraoperative ophthalmic imaging. , 2011, Ophthalmic surgery, lasers & imaging : the official journal of the International Society for Imaging in the Eye.

[221]  S. Marshall,et al.  Treatment of Raynaud's phenomenon with the selective serotonin reuptake inhibitor fluoxetine. , 2001, Rheumatology.

[222]  Alejandro F Frangi,et al.  Vascular Imaging , 2005, IEEE Trans. Medical Imaging.

[223]  P. Beard Biomedical photoacoustic imaging , 2011, Interface Focus.