Optical coherence tomography angiography as a novel approach to contactless evaluation of sublingual microcirculation: A proof of principle study.


Journal

Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288

Informations de publication

Date de publication:
25 03 2020
Historique:
received: 03 09 2019
accepted: 03 03 2020
entrez: 28 3 2020
pubmed: 28 3 2020
medline: 28 3 2020
Statut: epublish

Résumé

Microcirculatory disorders are crucial in pathophysiology of organ dysfunction in critical illness. Evaluation of sublingual microcirculation is not routinely conducted in daily practice due to time-consuming analysis and susceptibility to artifacts. We investigated the suitability of optical coherence tomography angiography (OCTA) for contactless evaluation of sublingual microcirculation. Sublingual microcirculation was imaged in 10 healthy volunteers, using an OCTA device and an incident dark field (IDF) illumination microscopy (current gold standard). OCTA images were analyzed with regard to flow density and perfused vessel density (PVD

Identifiants

pubmed: 32214141
doi: 10.1038/s41598-020-62128-2
pii: 10.1038/s41598-020-62128-2
pmc: PMC7096522
doi:

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

5408

Commentaires et corrections

Type : ErratumIn

Références

Erdem, Ö., Kuiper, J. W. & Tibboel, D. Hemodynamic coherence in critically ill pediatric patients. Best practice & research. Clinical anaesthesiology 30, 499–510, https://doi.org/10.1016/j.bpa.2016.10.002 (2016).
doi: 10.1016/j.bpa.2016.10.002
Massey, M. J. et al. Microcirculatory perfusion disturbances in septic shock: results from the ProCESS trial. Critical care (London, England) 22, 308, https://doi.org/10.1186/s13054-018-2240-5 (2018).
doi: 10.1186/s13054-018-2240-5
Scorcella, C. et al. MicroDAIMON study: Microcirculatory DAIly MONitoring in critically ill patients: a prospective observational study. Annals of intensive care 8, 64, https://doi.org/10.1186/s13613-018-0411-9 (2018).
doi: 10.1186/s13613-018-0411-9 pubmed: 29766322 pmcid: 5953911
Edul, V. S. K. et al. Quantitative assessment of the microcirculation in healthy volunteers and in patients with septic shock. Critical care medicine 40, 1443–1448, https://doi.org/10.1097/CCM.0b013e31823dae59 (2012).
doi: 10.1097/CCM.0b013e31823dae59 pubmed: 22430243
Top, A. P. C., Ince, C., Meij, N., de, van Dijk, M. & Tibboel, D. Persistent low microcirculatory vessel density in nonsurvivors of sepsis in pediatric intensive care. Critical care medicine 39, 8–13, https://doi.org/10.1097/CCM.0b013e3181fb7994 (2011).
doi: 10.1097/CCM.0b013e3181fb7994 pubmed: 21076287
den Uil, C. A. et al. The microcirculation in health and critical disease. Progress in cardiovascular diseases 51, 161–170, https://doi.org/10.1016/j.pcad.2008.07.002 (2008).
doi: 10.1016/j.pcad.2008.07.002
Ince, C. Hemodynamic coherence and the rationale for monitoring the microcirculation. Critical care (London, England) 19(Suppl 3), S8, https://doi.org/10.1186/cc14726 (2015).
doi: 10.1186/cc14726
Aykut, G., Veenstra, G., Scorcella, C., Ince, C. & Boerma, C. Cytocam-IDF (incident dark field illumination) imaging for bedside monitoring of the microcirculation. Intensive care medicine experimental 3, 40, https://doi.org/10.1186/s40635-015-0040-7 (2015).
doi: 10.1186/s40635-015-0040-7 pubmed: 26215807
Sherman, H., Klausner, S. & Cook, W. A. Incident dark-field illumination: a new method for microcirculatory study. Angiology 22, 295–303, https://doi.org/10.1177/000331977102200507 (1971).
doi: 10.1177/000331977102200507 pubmed: 5089888
Goedhart, P. T., Khalilzada, M., Bezemer, R., Merza, J. & Ince, C. Sidestream Dark Field (SDF) imaging: a novel stroboscopic LED ring-based imaging modality for clinical assessment of the microcirculation. Optics express 15, 15101–15114 (2007).
doi: 10.1364/OE.15.015101
Naumann, D. N. & Lima, A. Could resuscitation be based on microcirculation data? No. Intensive care medicine; https://doi.org/10.1007/s00134-018-5095-y (2018).
Dubin, A., Henriquez, E. & Hernández, G. Monitoring peripheral perfusion and microcirculation. Current opinion in critical care 24, 173–180, https://doi.org/10.1097/MCC.0000000000000495 (2018).
doi: 10.1097/MCC.0000000000000495 pubmed: 29553951
Ince, C. Personalized physiological medicine. Critical care (London, England) 21, 308, https://doi.org/10.1186/s13054-017-1907-7 (2017).
doi: 10.1186/s13054-017-1907-7
Ince, C. The rationale for microcirculatory guided fluid therapy. Current opinion in critical care 20, 301–308, https://doi.org/10.1097/MCC.0000000000000091 (2014).
doi: 10.1097/MCC.0000000000000091 pubmed: 24758985
Lanzillo, R. et al. Optical coherence tomography angiography retinal vascular network assessment in multiple sclerosis. Multiple sclerosis (Houndmills, Basingstoke, England), 1352458517729463; https://doi.org/10.1177/1352458517729463 (2017).
Alnawaiseh, M., Schubert, F., Heiduschka, P. & Eter, N. Optical coherence tomography angiography in patients with retinitis pigmentosa. Retina (Philadelphia, Pa.), https://doi.org/10.1097/IAE.0000000000001904. (2017).
Alnawaiseh, M. et al. Quantitative analysis of retinal perfusion in mice using optical coherence tomography angiography. Experimental eye research 164, 151–156, https://doi.org/10.1016/j.exer.2017.09.003. (2017).
doi: 10.1016/j.exer.2017.09.003. pubmed: 28889963
Alnawaiseh, M. et al. OCT angiography in the mouse: A novel evaluation method for vascular pathologies of the mouse retina. Experimental eye research 145, 417–423, https://doi.org/10.1016/j.exer.2016.02.012 (2016).
doi: 10.1016/j.exer.2016.02.012 pubmed: 26946073
Jia, Y. et al. Optical coherence tomography angiography of optic disc perfusion in glaucoma. Ophthalmology 121, 1322–1332, https://doi.org/10.1016/j.ophtha.2014.01.021. (2014).
doi: 10.1016/j.ophtha.2014.01.021. pubmed: 24629312 pmcid: 4082728
Alnawaiseh, M., Brand, C., Lauermann, J. L. & Eter, N. Messung der Flussdichte mittels OCT-Angiographie. Einfluss von Alter und Geschlecht. Der Ophthalmologe: Zeitschrift der Deutschen Ophthalmologischen Gesellschaft; https://doi.org/10.1007/s00347-017-0539-2 (2017).
Alnawaiseh, M., Lahme, L., Treder, M., Rosentreter, A. & Eter, N. Short-term effects of exercise on optic nerve and macular perfusion measured by optical coherence tomography angiography. Retina (Philadelphia, Pa.) 37, 1642–1646, https://doi.org/10.1097/IAE.0000000000001419 (2017).
doi: 10.1097/IAE.0000000000001419
Lévêque, P.-M., Zéboulon, P., Brasnu, E., Baudouin, C. & Labbé, A. Optic Disc Vascularization in Glaucoma: Value of Spectral-Domain Optical Coherence Tomography Angiography. Journal of ophthalmology 2016, 6956717, https://doi.org/10.1155/2016/6956717 (2016).
doi: 10.1155/2016/6956717 pubmed: 26998352 pmcid: 4779818
Yarmohammadi, A. et al. Relationship between Optical Coherence Tomography Angiography Vessel Density and Severity of Visual Field Loss in Glaucoma. Ophthalmology 123, 2498–2508, https://doi.org/10.1016/j.ophtha.2016.08.041 (2016).
doi: 10.1016/j.ophtha.2016.08.041 pubmed: 27726964 pmcid: 5362128
Park, J. R. et al. 1423: Microcirculatory alterations in hemorrhagic shock and sepsis with optical coherence tomography. Critical care medicine 44, 431, https://doi.org/10.1097/01.ccm.0000510097.67054.8a (2016).
doi: 10.1097/01.ccm.0000510097.67054.8a
Alnawaiseh, M. et al. Feasibility of optical coherence tomography angiography to assess changes in retinal microcirculation in ovine haemorrhagic shock. Critical care (London, England) 22, 138, https://doi.org/10.1186/s13054-018-2056-3 (2018).
doi: 10.1186/s13054-018-2056-3
Ince, C. et al. Second consensus on the assessment of sublingual microcirculation in critically ill patients: results from a task force of the European Society of Intensive Care Medicine. Intensive care medicine; https://doi.org/10.1007/s00134-018-5070-7 (2018).
Bland, J. M. & Altman, D. G. Statistical methods for assessing agreement between two methods of clinical measurement. Lancet (London, England) 1, 307–310 (1986).
doi: 10.1016/S0140-6736(86)90837-8
Jia, Y. et al. Quantitative optical coherence tomography angiography of vascular abnormalities in the living human eye. Proceedings of the National Academy of Sciences of the United States of America 112, E2395–402, https://doi.org/10.1073/pnas.1500185112 (2015).
doi: 10.1073/pnas.1500185112 pubmed: 25897021 pmcid: 4426471
Carnevali, A. et al. Optical Coherence Tomography Angiography: A Useful Tool for Diagnosis of Treatment-Naïve Quiescent Choroidal Neovascularization. American journal of ophthalmology 169, 189–198, https://doi.org/10.1016/j.ajo.2016.06.042 (2016).
doi: 10.1016/j.ajo.2016.06.042 pubmed: 27394033
Stanzel, T. P. et al. Comparison of Optical Coherence Tomography Angiography to Indocyanine Green Angiography and Slit Lamp Photography for Corneal Vascularization in an Animal Model. Scientific reports 8, 11493, https://doi.org/10.1038/s41598-018-29752-5 (2018).
doi: 10.1038/s41598-018-29752-5 pubmed: 30065317 pmcid: 6068177
Cennamo, G., Romano, M. R., Nicoletti, G., Velotti, N. & Crecchio, Gde Optical coherence tomography angiography versus fluorescein angiography in the diagnosis of ischaemic diabetic maculopathy. Acta ophthalmologica 95, e36–e42, https://doi.org/10.1111/aos.13159 (2017).
doi: 10.1111/aos.13159 pubmed: 27417658
Kraan, H. et al. Buccal and sublingual vaccine delivery. Journal of controlled release: official journal of the Controlled Release Society 190, 580–592, https://doi.org/10.1016/j.jconrel.2014.05.060 (2014).
doi: 10.1016/j.jconrel.2014.05.060
Winning, T. A. & Townsend, G. C. Oral mucosal embryology and histology. Clinics in Dermatology 18, 499–511, https://doi.org/10.1016/S0738-081X(00)00140-1 (2000).
doi: 10.1016/S0738-081X(00)00140-1 pubmed: 11134845
Lauermann, J. L., Eter, N. & Alten, F. Optical Coherence Tomography Angiography Offers New Insights into Choriocapillaris Perfusion. Ophthalmologica. Journal international d’ophtalmologie. International journal of ophthalmology. Zeitschrift fur Augenheilkunde 239, 74–84, https://doi.org/10.1159/000485261 (2018).
doi: 10.1159/000485261 pubmed: 29353272
Kurokawa, K., Liu, Z. & Miller, D. T. Adaptive optics optical coherence tomography angiography for morphometric analysis of choriocapillaris Invited. Biomedical optics express 8, 1803–1822, https://doi.org/10.1364/BOE.8.001803 (2017).
doi: 10.1364/BOE.8.001803 pubmed: 28663867 pmcid: 5480582
Acheampong, A. & Vincent, J.-L. A positive fluid balance is an independent prognostic factor in patients with sepsis. Critical care (London, England) 19, 251, https://doi.org/10.1186/s13054-015-0970-1 (2015).
doi: 10.1186/s13054-015-0970-1
Bennett, V. A., Vidouris, A. & Cecconi, M. Effects of Fluids on the Macro- and Microcirculations. Critical care (London, England) 22, 74, https://doi.org/10.1186/s13054-018-1993-1 (2018).
doi: 10.1186/s13054-018-1993-1
Neyra, J. A. et al. Cumulative Fluid Balance and Mortality in Septic Patients With or Without Acute Kidney Injury and Chronic Kidney Disease. Critical care medicine 44, 1891–1900, https://doi.org/10.1097/CCM.0000000000001835 (2016).
doi: 10.1097/CCM.0000000000001835 pubmed: 27352125 pmcid: 5505731
Wang, N., Jiang, L., Zhu, B., Wen, Y. & Xi, X.-M. Fluid balance and mortality in critically ill patients with acute kidney injury: a multicenter prospective epidemiological study. Critical care (London, England) 19, 371, https://doi.org/10.1186/s13054-015-1085-4 (2015).
doi: 10.1186/s13054-015-1085-4
Yang, J., Liu, L., Campbell, J. P., Huang, D. & Liu, G. Handheld optical coherence tomography angiography. Biomedical optics express 8, 2287–2300, https://doi.org/10.1364/BOE.8.002287 (2017).
doi: 10.1364/BOE.8.002287 pubmed: 28736672 pmcid: 5516829
Campbell, J. P. et al. Handheld Optical Coherence Tomography Angiography and Ultra-Wide-Field Optical Coherence Tomography in Retinopathy of Prematurity. JAMA ophthalmology 135, 977–981, https://doi.org/10.1001/jamaophthalmol.2017.2481 (2017).
doi: 10.1001/jamaophthalmol.2017.2481 pubmed: 28750113 pmcid: 6583755
Ploner, S. B. et al. Toward quantitative optical coherence tomography angiography: Visualizing Blood Flow Speeds in Ocular Pathology Using Variable Interscan Time Analysis. Retina (Philadelphia, Pa.) 36(Suppl 1), S118–S126, https://doi.org/10.1097/IAE.0000000000001328 (2016).
doi: 10.1097/IAE.0000000000001328
Wang, R. K., Zhang, Q., Li, Y. & Song, S. Optical coherence tomography angiography-based capillary velocimetry. Journal of biomedical optics 22, 66008, https://doi.org/10.1117/1.JBO.22.6.066008 (2017).
doi: 10.1117/1.JBO.22.6.066008 pubmed: 28617921
Li, Y., Wei, W. & Wang, R. K. Capillary flow homogenization during functional activation revealed by optical coherence tomography angiography based capillary velocimetry. Scientific reports 8, 4107, https://doi.org/10.1038/s41598-018-22513-4 (2018).
doi: 10.1038/s41598-018-22513-4 pubmed: 29515156 pmcid: 5841298
Kashani, A. H. et al. Optical coherence tomography angiography: A comprehensive review of current methods and clinical applications. Progress in retinal and eye research 60, 66–100, https://doi.org/10.1016/j.preteyeres.2017.07.002 (2017).
doi: 10.1016/j.preteyeres.2017.07.002 pubmed: 28760677 pmcid: 5600872
Chu, Z. et al. Quantitative assessment of the retinal microvasculature using optical coherence tomography angiography. Journal of biomedical optics 21, 66008, https://doi.org/10.1117/1.JBO.21.6.066008 (2016).
doi: 10.1117/1.JBO.21.6.066008 pubmed: 27286188
Jia, Y. et al. Quantitative optical coherence tomography angiography of choroidal neovascularization in age-related macular degeneration. Ophthalmology 121, 1435–1444, https://doi.org/10.1016/j.ophtha.2014.01.034 (2014).
doi: 10.1016/j.ophtha.2014.01.034 pubmed: 24679442 pmcid: 4082740
Coscas, F. et al. Normative Data for Vascular Density in Superficial and Deep Capillary Plexuses of Healthy Adults Assessed by Optical Coherence Tomography Angiography. Investigative ophthalmology & visual science 57, OCT211–23, https://doi.org/10.1167/iovs.15-18793 (2016).
doi: 10.1167/iovs.15-18793
Spaide, R. F., Fujimoto, J. G. & Waheed, N. K. Image artifacts in optical coherence tomography angiography. Retina (Philadelphia, Pa.) 35, 2163–2180, https://doi.org/10.1097/IAE.0000000000000765 (2015).
doi: 10.1097/IAE.0000000000000765
Jia, Y. et al. Split-spectrum amplitude-decorrelation angiography with optical coherence tomography. Optics express 20, 4710–4725, https://doi.org/10.1364/OE.20.004710 (2012).
doi: 10.1364/OE.20.004710 pubmed: 22418228 pmcid: 3381646
Kraus, M. F. et al. Motion correction in optical coherence tomography volumes on a per A-scan basis using orthogonal scan patterns. Biomedical optics express 3, 1182–1199, https://doi.org/10.1364/BOE.3.001182 (2012).
doi: 10.1364/BOE.3.001182 pubmed: 22741067 pmcid: 3370961
Kraus, M. F. et al. Quantitative 3D-OCT motion correction with tilt and illumination correction, robust similarity measure and regularization. Biomedical optics express 5, 2591–2613, https://doi.org/10.1364/BOE.5.002591 (2014).
doi: 10.1364/BOE.5.002591 pubmed: 25136488 pmcid: 4132991
Massey, M. J. et al. The microcirculation image quality score: development and preliminary evaluation of a proposed approach to grading quality of image acquisition for bedside videomicroscopy. Journal of critical care 28, 913–917, https://doi.org/10.1016/j.jcrc.2013.06.015 (2013).
doi: 10.1016/j.jcrc.2013.06.015 pubmed: 23972316
Hessler, M. et al. A new complimentary web-based tool for manual analysis of microcirculation videos: Validation of the Capillary Mapper against the current gold standard AVA 3.2. Microcirculation (New York, N.Y.: 1994) 25, e12505, https://doi.org/10.1111/micc.12505 (2018).
doi: 10.1111/micc.12505
Backer, Dde et al. How to evaluate the microcirculation: report of a round table conference. Critical care (London, England) 11, R101, https://doi.org/10.1186/cc6118 (2007).
doi: 10.1186/cc6118
Massey, M. J. & Shapiro, N. I. A guide to human in vivo microcirculatory flow image analysis. Critical care (London, England) 20, 35, https://doi.org/10.1186/s13054-016-1213-9 (2016).
doi: 10.1186/s13054-016-1213-9

Auteurs

Michael Hessler (M)

Department of Anesthesiology, Intensive Care, and Pain Therapy, University Hospital Muenster, Albert-Schweitzer-Campus 1, Building A1, Muenster, Germany.

Pieter Nelis (P)

Department of Ophthalmology, University Hospital Muenster, Domagkstraße 15, Muenster, Germany.
Department of Ophthalmology, University of Brussels (VUB), Laarbeeklaan 101, Jette, Belgium.

Christian Ertmer (C)

Department of Anesthesiology, Intensive Care, and Pain Therapy, University Hospital Muenster, Albert-Schweitzer-Campus 1, Building A1, Muenster, Germany. ertmer@anit.uni-muenster.de.

Maged Alnawaiseh (M)

Department of Ophthalmology, University Hospital Muenster, Domagkstraße 15, Muenster, Germany.

Florian Lehmann (F)

Department of Anesthesiology, Intensive Care, and Pain Therapy, University Hospital Muenster, Albert-Schweitzer-Campus 1, Building A1, Muenster, Germany.

Christina Schmidt (C)

Department of Anesthesiology, Intensive Care, and Pain Therapy, University Hospital Muenster, Albert-Schweitzer-Campus 1, Building A1, Muenster, Germany.

Tim-Gerald Kampmeier (TG)

Department of Anesthesiology, Intensive Care, and Pain Therapy, University Hospital Muenster, Albert-Schweitzer-Campus 1, Building A1, Muenster, Germany.

Sebastian Willy Rehberg (SW)

Department of Anesthesiology, Intensive Care, Emergency Medicine, Transfusion Medicine and Pain Therapy, Protestant Hospital of the Bethel Foundation, Burgsteig, Bielefeld, Germany.

Philip-Helge Arnemann (PH)

Department of Anesthesiology, Intensive Care, and Pain Therapy, University Hospital Muenster, Albert-Schweitzer-Campus 1, Building A1, Muenster, Germany.

Alexandros Rovas (A)

Department of Medicine D, Division of General Internal Medicine, Nephrology, and Rheumatology, University Hospital Muenster, Albert-Schweitzer-Campus 1, Muenster, Germany.

Classifications MeSH