In vivo optical imaging of the viable epidermis around the nailfold capillaries for the assessment of heart failure severity in humans

Heart failure (HF) is among the socially significant diseases, involving over 2% of the adult population in the developed countries. Diagnostics of the HF severity remains complicated due to the absence of specific symptoms and objective criteria. Here, we present an indicator of the HF severity based on the imaging of tissue parameters around the nailfold capillaries. High resolution nailfold video capillaroscopy was performed to determine the perivascular zone (PZ) size around nailfold capillaries, and 2‐photon tomography with fluorescence lifetime imaging was used to investigate PZ composition. We found that the size of PZ around the nailfold capillaries strongly correlates with HF severity. Further investigations using 2‐photon tomography demonstrated that PZ corresponds to the border of viable epidermis and it was suggested that the PZ size variations were due to the different amounts of interstitial fluid that potentially further translates in clinically significant oedema. The obtained results allow for the development of a quantitative indicator of oedematous syndrome, which can be used in various applications to monitor the dynamics of interstitial fluid retention. We therefore suggest PZ size measured with nailfold video capillaroscopy as a novel quantitative sensitive non‐invasive marker of HF severity.

[1]  P. Mortimer,et al.  Skin microvascular architecture and perfusion studied in human postmastectomy oedema by intravital video-capillaroscopy. , 1994, International journal of microcirculation, clinical and experimental.

[2]  A. Bollinger,et al.  Microvascular Changes in Chronic Venous Insufficiency—A Review , 1995, Cardiovascular surgery.

[3]  G. Schmid-Schönbein,et al.  Transvascular and Interstitial Migration of Neutrophils in Rat Mesentery , 1996, Microcirculation.

[4]  C. Baerwald,et al.  Electron microscopy and capillaroscopically guided nailfold biopsy in connective tissue diseases: detection of ultrastructural changes of the microcirculatory vessels. , 1998, British journal of rheumatology.

[5]  C. Fonseca,et al.  Prevalence of chronic heart failure in Southwestern Europe: the EPICA study , 2002, European journal of heart failure.

[6]  A. Kroon,et al.  Microvascular Abnormalities in Chronic Heart Failure: A Cross‐Sectional Analysis , 2003, Microcirculation.

[7]  V. L. C. Halfoun,et al.  Videocapillaroscopy and Diabetes mellitus: area of transverse segment in nailfold capillar loops reflects vascular reactivity. , 2003, Diabetes research and clinical practice.

[8]  J. Vincent,et al.  Microvascular alterations in patients with acute severe heart failure and cardiogenic shock. , 2004, American heart journal.

[9]  R. Scrivo,et al.  Nailfold capillaroscopy changes in systemic lupus erythematosus: correlations with disease activity and autoantibody profile , 2005, Lupus.

[10]  Yukio Yamada,et al.  Depth profile of diffuse reflectance near‐infrared spectroscopy for measurement of water content in skin , 2005, 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.

[11]  A. Pena,et al.  Spectroscopic analysis of keratin endogenous signal for skin multiphoton microscopy. , 2005, Optics express.

[12]  George Hripcsak,et al.  Technical Brief: Agreement, the F-Measure, and Reliability in Information Retrieval , 2005, J. Am. Medical Informatics Assoc..

[13]  Georgios N Stamatas,et al.  In vivo monitoring of cutaneous edema using spectral imaging in the visible and near infrared. , 2006, The Journal of investigative dermatology.

[14]  A. Hoes,et al.  Clinical epidemiology of heart failure , 2007, Heart.

[15]  Stefan Kray,et al.  Simultaneous dual-band ultra-high resolution optical coherence tomography. , 2007, Optics express.

[16]  Daniel Henrion,et al.  Evaluation of the microcirculation in hypertension and cardiovascular disease. , 2007, European heart journal.

[17]  M. Cutolo,et al.  Scoring the nailfold microvascular changes during the capillaroscopic analysis in systemic sclerosis patients , 2007, Annals of the rheumatic diseases.

[18]  A. Pries,et al.  A review of methods for assessment of coronary microvascular disease in both clinical and experimental settings. , 2008, Cardiovascular research.

[19]  The specificity of capillaroscopic pattern in connective autoimmune diseases. A comparison with microvascular changes in diseases of social importance: arterial hypertension and diabetes mellitus , 2009 .

[20]  M. Anastasiou-Nana,et al.  Physical Exercise Improves the Peripheral Microcirculation of Patients With Chronic Heart Failure , 2009, Journal of cardiopulmonary rehabilitation and prevention.

[21]  Gaël Varoquaux,et al.  Scikit-learn: Machine Learning in Python , 2011, J. Mach. Learn. Res..

[22]  Lihong V. Wang,et al.  In vivo photoacoustic microscopy of human cutaneous microvasculature and a nevus. , 2011, Journal of biomedical optics.

[23]  Harlan M Krumholz,et al.  National and regional trends in heart failure hospitalization and mortality rates for Medicare beneficiaries, 1998-2008. , 2011, JAMA.

[24]  Christopher G. Rylander,et al.  Effect of Localized Mechanical Indentation on Skin Water Content Evaluated Using OCT , 2011, Int. J. Biomed. Imaging.

[25]  Martin Leahy,et al.  In vivo imaging of the microcirculation of the volar forearm using correlation mapping optical coherence tomography (cmOCT) , 2011, Biomedical optics express.

[26]  A. Fedorovich Non-invasive evaluation of vasomotor and metabolic functions of microvascular endothelium in human skin. , 2012, Microvascular research.

[27]  N. Wiernsperger,et al.  Microvascular diseases: is a new era coming? , 2012, Cardiovascular & hematological agents in medicinal chemistry.

[28]  Harald Sattmann,et al.  High-speed polarization sensitive optical coherence tomography scan engine based on Fourier domain mode locked laser , 2012, Biomedical optics express.

[29]  Lihong V. Wang,et al.  Photoacoustic Tomography: In Vivo Imaging from Organelles to Organs , 2012, Science.

[30]  Jürgen Popp,et al.  From molecular structure to tissue architecture: collagen organization probed by SHG microscopy , 2013, Journal of biophotonics.

[31]  Huanyu Cheng,et al.  Epidermal Impedance Sensing Sheets for Precision Hydration Assessment and Spatial Mapping , 2013, IEEE Transactions on Biomedical Engineering.

[32]  Susan M Daly,et al.  ‘Go with the flow ’: A review of methods and advancements in blood flow imaging , 2013, Journal of biophotonics.

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

[34]  C. Salvarani,et al.  Nailfold capillaroscopic changes in dermatomyositis and polymyositis , 2015, Clinical Rheumatology.

[35]  Yongjian Zhu,et al.  Penetration of silver nanoparticles into porcine skin ex vivo using fluorescence lifetime imaging microscopy, Raman microscopy, and surface-enhanced Raman scattering microscopy , 2014, Journal of biomedical optics.

[36]  Björn-Erik Erlandsson,et al.  Nailfold Capillaroscopy in Rheumatic Diseases: Which Parameters Should Be Evaluated? , 2015, BioMed research international.

[37]  A. Triantafyllou,et al.  Capillary Rarefaction as an Index for the Microvascular Assessment of Hypertensive Patients , 2015, Current Hypertension Reports.

[38]  The pixelation of mass spectrometry , 2015 .

[39]  C. Grana,et al.  Dynamic Optical Coherence Tomography in Dermatology , 2016, Dermatology.

[40]  Oliver Distler,et al.  An EULAR study group pilot study on reliability of simple capillaroscopic definitions to describe capillary morphology in rheumatic diseases. , 2016, Rheumatology.

[41]  Volkmar Falk,et al.  2016 ESC Guidelines for the diagnosis and treatment of acute and chronic heart failure , 2016, Revista espanola de cardiologia.

[42]  J. Lademann,et al.  Fluorescence detection of protein content in house dust: the possible role of keratin , 2017, Indoor air.

[43]  M. Biase,et al.  Nailfold capillaroscopic changes in patients with idiopathic pulmonary arterial hypertension and systemic sclerosis-related pulmonary arterial hypertension. , 2017, Microvascular research.

[44]  V. Tuchin,et al.  A comparative study of ex vivo skin optical clearing using two‐photon microscopy , 2017, Journal of biophotonics.

[45]  Maxim E. Darvin,et al.  Two-photon autofluorescence lifetime imaging of human skin papillary dermis in vivo: assessment of blood capillaries and structural proteins localization , 2017, Scientific Reports.

[46]  G. Maldonado,et al.  Nailfold capillaroscopy in diabetes mellitus. , 2017, Microvascular research.

[47]  Potentialities of Digital Capillaroscopy in the Diagnostics of Oedema Syndrome , 2017 .

[48]  S. A. Rodionov,et al.  Formation of hemoglobin photoproduct is responsible for two-photon and single photon-excited fluorescence of red blood cells , 2018, Laser Physics Letters.