Novel Optical Techniques for Imaging Microcirculation in the Diabetic Foot.

BACKGROUND The most severe diabetic foot ulcers are those related with critical ischemia, which is primarily diagnosed with non-invasive diagnostics. However, these diagnostics have several disadvantages. For example, they only provide global indications of the (macro)level of ischemia. A potential solution can be found in novel optical imaging techniques for local assessment of the microcirculation in diabetic foot ulcers. This review provides an overview of these imaging techniques (Laser Doppler Perfusion Imaging, Laser Speckle Contrast Imaging, Photoacoustic Imaging and Hyperspectral Imaging) and their applicability for the diagnostic assessment of microcirculation in diabetic foot ulcers. METHOD For each technique, the following parts are described: a) their technical background; b) general clinical applications; and, c) its application for microcirculation assessment in diabetic foot ulcers. Parts a-b are based on a narrative review of the literature, part c on a systematic review that was performed in the database Scopus, covering the period from January 1, 2000 to November 31, 2017. RESULTS Each of these techniques has specific advantages and disadvantages for imaging microcirculation. Potential clinical use depends on measurement aims, and clinical relevance. However, none of the techniques has a strongly established clinical relevance yet: we found a limited number of publications describing clinical outcomes. Future research is needed to determine which technique is the most clinically relevant for the assessment of microcirculation in diabetic foot ulcers. CONCLUSION Although promising, the currently available novel optical techniques need to be further improved technically and prospective trials are necessary to evaluate their clinical value.

[1]  Matthieu Roustit,et al.  Assessment of endothelial and neurovascular function in human skin microcirculation. , 2013, Trends in pharmacological sciences.

[2]  J. Mansfield,et al.  Hyperspectral imaging: a new approach to the diagnosis of hemorrhagic shock. , 2006, The Journal of trauma.

[3]  J. Reekers,et al.  IWGDF guidance on the diagnosis, prognosis and management of peripheral artery disease in patients with foot ulcers in diabetes , 2016, Diabetes/metabolism research and reviews.

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

[5]  M. Roustit,et al.  Cutaneous iontophoresis of treprostinil, a prostacyclin analog, increases microvascular blood flux in diabetic malleolus area. , 2015, European journal of pharmacology.

[6]  Ton van Leeuwen,et al.  Review of laser speckle contrast techniques for visualizing tissue perfusion , 2008, Lasers in Medical Science.

[7]  L. Uccioli,et al.  Prediction of outcome in individuals with diabetic foot ulcers: focus on the differences between individuals with and without peripheral arterial disease. The EURODIALE Study , 2008, Diabetologia.

[8]  F. M. van den Engh,et al.  Visualizing breast cancer using the Twente photoacoustic mammoscope: what do we learn from twelve new patient measurements? , 2012, Optics express.

[9]  R. Forsythe,et al.  Clinical implications of the angiosome model in peripheral vascular disease. , 2013, Journal of vascular surgery.

[10]  Diabetes Federation IDF Diabetes Atlas 9th Edition , 2019 .

[11]  H. Uetake,et al.  Novel assessment tool based on laser speckle contrast imaging to diagnose severe ischemia in the lower limb for patients with peripheral arterial disease , 2017, Lasers in surgery and medicine.

[12]  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.

[13]  A. Willfort,et al.  Laser Doppler imaging and capillary microscopy in ischemic ulcers. , 1999, Atherosclerosis.

[14]  L. Gould Technology: Noninvasive Assessment of Lower Extremity Healing Potential , 2008, Foot & ankle specialist.

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

[16]  P. Vajkoczy,et al.  Infarct prediction by intraoperative laser speckle imaging in patients with malignant hemispheric stroke , 2016, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[17]  Shiwu Zhang,et al.  Multi-scale hyperspectral imaging of cervical neoplasia , 2016, Archives of Gynecology and Obstetrics.

[18]  G Muyo,et al.  Spectral imaging of the retina , 2011, Eye.

[19]  Wen-Chuan Kuo,et al.  Review of near-infrared methods for wound assessment , 2016, Journal of biomedical optics.

[20]  A. Boulton,et al.  Venous oxygenation in the diabetic neuropathic foot: Evidence of arteriovenous shunting? , 2004, Diabetologia.

[21]  Kyung Soo Lee,et al.  Volume-Based Parameter of 18F-FDG PET/CT in Malignant Pleural Mesothelioma: Prediction of Therapeutic Response and Prognostic Implications , 2010, Annals of Surgical Oncology.

[22]  Chris Jun Hui Ho,et al.  Noninvasive real-time characterization of non-melanoma skin cancers with handheld optoacoustic probes , 2017, Photoacoustics.

[23]  H. Arksey,et al.  Scoping studies: towards a methodological framework , 2005 .

[24]  M. Stern,et al.  In vivo evaluation of microcirculation by coherent light scattering , 1975, Nature.

[25]  J. Petrofsky,et al.  Effects of electrical stimulation on skin blood flow in controls and in and around stage III and IV wounds in hairy and non hairy skin. , 2005, Medical science monitor : international medical journal of experimental and clinical research.

[26]  W. Jeffcoate,et al.  Cost of diabetic foot disease to the National Health Service in England , 2014, Diabetic medicine : a journal of the British Diabetic Association.

[27]  A. Oraevsky,et al.  Laser optoacoustic imaging system for detection of breast cancer. , 2009, Journal of biomedical optics.

[28]  Hilla Peretz,et al.  Ju n 20 03 Schrödinger ’ s Cat : The rules of engagement , 2003 .

[29]  Nuno M Garcia,et al.  A review of thermal methods and technologies for diabetic foot assessment , 2015, Expert review of medical devices.

[30]  Chris Jun Hui Ho,et al.  Structural and functional 3D mapping of skin tumours with non‐invasive multispectral optoacoustic tomography , 2017, 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.

[31]  Zhongping Chen,et al.  Clinical testing of a photoacoustic probe for port wine stain depth determination , 2002, Lasers in surgery and medicine.

[32]  Stanislav Y. Emelianov,et al.  Biomedical Applications of Photoacoustic Imaging with Exogenous Contrast Agents , 2011, Annals of Biomedical Engineering.

[33]  R. Gillies,et al.  Systemic effects of shock and resuscitation monitored by visible hyperspectral imaging. , 2003, Diabetes technology & therapeutics.

[34]  K. Eriksson,et al.  Outcome of ischemic foot ulcer in diabetic patients who had no invasive vascular intervention. , 2013, European journal of vascular and endovascular surgery : the official journal of the European Society for Vascular Surgery.

[35]  Yuqi Zhang,et al.  Photoacoustic Drug Delivery , 2017, Sensors.

[36]  M. Huijberts,et al.  Resource utilisation and costs associated with the treatment of diabetic foot ulcers. Prospective data from the Eurodiale Study , 2008, Diabetologia.

[37]  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.

[38]  Y. Sakr Techniques to assess tissue oxygenation in the clinical setting. , 2010, Transfusion and apheresis science : official journal of the World Apheresis Association : official journal of the European Society for Haemapheresis.

[39]  R. Forsythe,et al.  Assessment of foot perfusion in patients with a diabetic foot ulcer , 2016, Diabetes/metabolism research and reviews.

[40]  K. Kusumoto,et al.  Comparison of neovascularization in dermal substitutes seeded with autologous fibroblasts or impregnated with bFGF applied to diabetic foot ulcers using laser Doppler imaging , 2014, Journal of Artificial Organs.

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

[42]  J. Reekers,et al.  Effectiveness of bedside investigations to diagnose peripheral artery disease among people with diabetes mellitus: a systematic review , 2016, Diabetes/metabolism research and reviews.

[43]  V. Tuchin Tissue Optics: Light Scattering Methods and Instruments for Medical Diagnosis , 2000 .

[44]  J. Reekers,et al.  Performance of prognostic markers in the prediction of wound healing or amputation among patients with foot ulcers in diabetes: a systematic review , 2016, Diabetes/metabolism research and reviews.

[45]  Martin J. Leahy,et al.  Biophotonic methods in microcirculation imaging , 2007 .

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

[47]  Vasilis Ntziachristos,et al.  Molecular imaging probes for multi-spectral optoacoustic tomography. , 2017, Chemical communications.

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

[49]  A. Murray,et al.  Reduced perfusion in systemic sclerosis digital ulcers (both fingertip and extensor) can be increased by topical application of glyceryl trinitrate☆ , 2017, Microvascular research.

[50]  W. Jeffcoate,et al.  Use of HSI to measure oxygen saturation in the lower limb and its correlation with healing of foot ulcers in diabetes , 2015, Diabetic medicine : a journal of the British Diabetic Association.

[51]  K. Alexiadou,et al.  Management of Diabetic Foot Ulcers , 2012, Diabetes Therapy.

[52]  Sicco A Bus,et al.  Diabetic Foot Ulcers and Their Recurrence. , 2017, The New England journal of medicine.

[53]  D. Faller,et al.  Medical hyperspectral imaging to facilitate residual tumor identification during surgery , 2007, Cancer biology & therapy.

[54]  D. Hernandez-Contreras,et al.  Narrative review: Diabetic foot and infrared thermography , 2016 .

[55]  Hidetoshi Takahashi,et al.  Optic Nerve Head Blood Flow, as Measured by Laser Speckle Flowgraphy, Is Significantly Reduced in Preperimetric Glaucoma , 2016, Current eye research.

[56]  Luma V. Halig,et al.  Hyperspectral imaging and quantitative analysis for prostate cancer detection. , 2012, Journal of biomedical optics.

[57]  L. Khaodhiar,et al.  Topical methyl nicotinate-induced skin vasodilation in diabetic neuropathy. , 2003, Journal of diabetes and its complications.

[58]  G. Leese,et al.  Blood flow changes in diabetic foot ulcers treated with dermal replacement therapy. , 2002, The Journal of foot and ankle surgery : official publication of the American College of Foot and Ankle Surgeons.

[59]  C. Wittens,et al.  Prediction of venous wound healing with laser speckle imaging , 2017, Phlebology.

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

[61]  Wiendelt Steenbergen,et al.  Feasibility of photoacoustic/ultrasound imaging of synovitis in finger joints using a point-of-care system , 2017, Photoacoustics.

[62]  Folke Sjöberg,et al.  Microvascular blood flow in scalds in children and its relation to duration of wound healing: A study using laser speckle contrast imaging. , 2016, Burns : journal of the International Society for Burn Injuries.

[63]  Shiwu Zhang,et al.  Multimodal imaging of cutaneous wound tissue , 2015, Journal of biomedical optics.

[64]  K. Hoffmann,et al.  Laser Doppler imaging of axial and random pattern flaps in the maxillo-facial area. A preliminary report. , 1994, Journal of cranio-maxillo-facial surgery : official publication of the European Association for Cranio-Maxillo-Facial Surgery.

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

[66]  John Allen,et al.  Microvascular imaging: techniques and opportunities for clinical physiological measurements , 2014, Physiological measurement.

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

[68]  Lihong V. Wang,et al.  In vivo functional photoacoustic microscopy of cutaneous microvasculature in human skin. , 2011, Journal of biomedical optics.

[69]  Benjamin A Lipsky,et al.  The 2015 IWGDF guidance documents on prevention and management of foot problems in diabetes: development of an evidence‐based global consensus , 2016, Diabetes/metabolism research and reviews.

[70]  Chulhong Kim,et al.  Programmable Real-time Clinical Photoacoustic and Ultrasound Imaging System , 2016, Scientific Reports.

[71]  Seong G. Kong,et al.  Hyperspectral Fluorescence Imaging for Mouse Skin Tumor Detection , 2006 .

[72]  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.

[73]  J. Briers,et al.  Laser speckle contrast imaging for measuring blood flow , 2007 .

[74]  Konstantin I Maslov,et al.  Handheld photoacoustic microscopy to detect melanoma depth in vivo. , 2014, Optics letters.

[75]  Thomas E. Lyons,et al.  Early changes in the skin microcirculation and muscle metabolism of the diabetic foot , 2005, The Lancet.

[76]  D. Ferris,et al.  Multimodal Hyperspectral Imaging for the Noninvasive Diagnosis of Cervical Neoplasia , 2001, Journal of lower genital tract disease.

[77]  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.

[78]  J. Chin,et al.  Evaluation of hyperspectral technology for assessing the presence and severity of peripheral artery disease. , 2011, Journal of vascular surgery.

[79]  David G Armstrong,et al.  Health Care Service and Outcomes Among an Estimated 6.7 Million Ambulatory Care Diabetic Foot Cases in the U.S. , 2017, Diabetes Care.

[80]  Vasilis Ntziachristos,et al.  Optoacoustic Imaging of Human Vasculature: Feasibility by Using a Handheld Probe. , 2016, Radiology.

[81]  A. Icks,et al.  Incidence of lower extremity amputations in the diabetic compared with the non-diabetic population: A systematic review , 2017, PloS one.

[82]  Xinmai Yang,et al.  Nanoparticles for photoacoustic imaging. , 2009, Wiley interdisciplinary reviews. Nanomedicine and nanobiotechnology.

[83]  T. Ledin,et al.  Impaired microvascular function related to poor metabolic control in young patients with diabetes , 2005, Clinical physiology and functional imaging.

[84]  Anne Humeau-Heurtier,et al.  Relevance of Laser Doppler and Laser Speckle Techniques for Assessing Vascular Function: State of the Art and Future Trends , 2013, IEEE Transactions on Biomedical Engineering.

[85]  Aksone Nouvong,et al.  Hyperspectral Imaging in Diabetic Foot Wound Care , 2010, Journal of diabetes science and technology.

[86]  Gert E. Nilsson,et al.  Evaluation of a Laser Doppler Flowmeter for Measurement of Tissue Blood Flow , 1980, IEEE Transactions on Biomedical Engineering.

[87]  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.

[88]  Alexander A. Oraevsky,et al.  Optoacoustic imaging of blood for visualization and diagnostics of breast cancer , 2002, SPIE BiOS.