Photoacoustic imaging of lamina cribrosa microcapillaries in porcine eyes.

Due to the embedded nature of the lamina cribrosa (LC) microcapillary network, conventional imaging techniques have failed to obtain the high-resolution images needed to assess the perfusion state of the LC. In this study, both optical resolution (OR) and acoustic resolution (AR) photoacoustic microscopy (PAM) techniques were used to obtain static and dynamic information about LC perfusion in ex vivo porcine eyes. The OR-PAM system could resolve a perfused LC microcapillary network with a lateral resolution of 4.2 μm and also provided good depth information (33 μm axial resolution) to visualize through-thickness vascular variations. The AR-PAM system was capable of detecting time-dependent perfusion variations. This study represents the first step towards using an emerging imaging modality (PAM) to study the LC's perfusion, which could be a basis for further investigation of the hemodynamic aspects of glaucomatous optic neuropathy.

[1]  Chulhong Kim,et al.  Acoustic resolution photoacoustic microscopy , 2014, Biomedical Engineering Letters.

[2]  James V Jester,et al.  Application of second harmonic imaging microscopy to assess structural changes in optic nerve head structure ex vivo. , 2007, Journal of biomedical optics.

[3]  R. T. Hart,et al.  The optic nerve head as a biomechanical structure: a new paradigm for understanding the role of IOP-related stress and strain in the pathophysiology of glaucomatous optic nerve head damage , 2005, Progress in Retinal and Eye Research.

[4]  Shuliang Jiao,et al.  Integrating photoacoustic ophthalmoscopy with scanning laser ophthalmoscopy, optical coherence tomography, and fluorescein angiography for a multimodal retinal imaging platform. , 2012, Journal of biomedical optics.

[5]  Junjie Yao,et al.  Multi-scale photoacoustic tomography using reversibly switchable bacterial phytochrome as a near-infrared photochromic probe , 2015, Nature Methods.

[6]  Junjie Yao,et al.  Near-infrared optical-resolution photoacoustic microscopy. , 2014, Optics letters.

[7]  F. Medeiros,et al.  The pathophysiology and treatment of glaucoma: a review. , 2014, JAMA.

[8]  Qifa Zhou,et al.  Ultrasound-aided Multi-parametric Photoacoustic Microscopy of the Mouse Brain , 2015, Scientific Reports.

[9]  Yong Zhou,et al.  Tutorial on photoacoustic tomography , 2016, Journal of biomedical optics.

[10]  P. Causin,et al.  A poroelastic model for the perfusion of the lamina cribrosa in the optic nerve head. , 2014, Mathematical biosciences.

[11]  V. Ntziachristos.  Going deeper than microscopy: the optical imaging frontier in biology , 2010, Nature Methods.

[12]  Leopold Schmetterer,et al.  Doppler Optical Coherence Tomography , 2014, Progress in Retinal and Eye Research.

[13]  Martial Geiser,et al.  Ocular blood flow assessment using continuous laser Doppler flowmetry , 2010, Acta ophthalmologica.

[14]  Manojit Pramanik,et al.  Molecular photoacoustic imaging of angiogenesis with integrin‐targeted gold nanobeacons , 2011, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[15]  Lihong V. Wang,et al.  A practical guide to photoacoustic tomography in the life sciences , 2016, Nature Methods.

[16]  Sri Gowtham Thakku,et al.  Factors Influencing Lamina Cribrosa Microcapillary Hemodynamics and Oxygen Concentrations. , 2016, Investigative ophthalmology & visual science.

[17]  Vasilis Ntziachristos,et al.  Advances in real-time multispectral optoacoustic imaging and its applications , 2015, Nature Photonics.

[18]  H. Grossniklaus,et al.  Morphometric analysis of the choroid, Bruch's membrane, and retinal pigment epithelium in eyes with age-related macular degeneration. , 1996, Investigative ophthalmology & visual science.

[19]  Manojit Pramanik,et al.  Switchable Acoustic and Optical Resolution Photoacoustic Microscopy for In Vivo Small-animal Blood Vasculature Imaging. , 2017, Journal of visualized experiments : JoVE.

[20]  Wei Shi,et al.  Non-interferometric photoacoustic remote sensing microscopy , 2017, Light: Science & Applications.

[21]  Lihong V. Wang,et al.  Label-free photoacoustic ophthalmic angiography. , 2010, Optics letters.

[22]  Gadi Wollstein,et al.  Imaging of the Lamina Cribrosa in Glaucoma: Perspectives of Pathogenesis and Clinical Applications , 2013, Current eye research.

[23]  Manojit Pramanik,et al.  In vivo studies of transdermal nanoparticle delivery with microneedles using photoacoustic microscopy. , 2017, Biomedical optics express.

[24]  Nicholas G Strouthidis,et al.  Altering the way the optic nerve head responds to intraocular pressure-a potential approach to glaucoma therapy. , 2013, Current opinion in pharmacology.

[25]  Qifa Zhou,et al.  Reflection-mode submicron-resolution in vivo photoacoustic microscopy. , 2012, Journal of biomedical optics.

[26]  Chulhong Kim,et al.  In Vivo Photoacoustic Imaging of Anterior Ocular Vasculature: A Random Sample Consensus Approach , 2017, Scientific Reports.

[27]  J. Seylaz,et al.  Long-Term in Vivo Investigation of Mouse Cerebral Microcirculation by Fluorescence Confocal Microscopy in the Area of Focal Ischemia , 2005, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[28]  C. Ross Ethier,et al.  Phase-Contrast Micro-Computed Tomography Measurements of the Intraocular Pressure-Induced Deformation of the Porcine Lamina Cribrosa , 2016, IEEE Transactions on Medical Imaging.

[29]  Lihong V. Wang,et al.  Functional photoacoustic microscopy for high-resolution and noninvasive in vivo imaging , 2006, Nature Biotechnology.

[30]  Hao F. Zhang,et al.  Photoacoustic imaging of the eye: A mini review , 2016, Photoacoustics.

[31]  Jin Young Kim,et al.  Fast optical-resolution photoacoustic microscopy using a 2-axis water-proofing MEMS scanner , 2015, Scientific Reports.

[32]  T. Nakazawa.  Ocular Blood Flow and Influencing Factors for Glaucoma , 2016, Asia-Pacific journal of ophthalmology.

[33]  Douglas R. Anderson,et al.  Ocular perfusion pressure in glaucoma , 2014, Acta ophthalmologica.

[34]  Leopold Schmetterer,et al.  Use of laser speckle flowgraphy in ocular blood flow research , 2010, Acta ophthalmologica.

[35]  Ji Yi,et al.  A combined method to quantify the retinal metabolic rate of oxygen using photoacoustic ophthalmoscopy and optical coherence tomography , 2014, Scientific Reports.

[36]  L. Schmetterer,et al.  Ocular perfusion pressure and ocular blood flow in glaucoma , 2013, Current opinion in pharmacology.

[37]  Yannis M Paulus,et al.  Photoacoustic ocular imaging. , 2010, Optics letters.

[38]  C. R. Ethier,et al.  Deformation of the Lamina Cribrosa and Optic Nerve Due to Changes in Cerebrospinal Fluid Pressure , 2017, Investigative ophthalmology & visual science.

[39]  Manojit Pramanik,et al.  Performance Characterization of a Switchable Acoustic Resolution and Optical Resolution Photoacoustic Microscopy System , 2017, Sensors.

[40]  C. Burgoyne.  A biomechanical paradigm for axonal insult within the optic nerve head in aging and glaucoma. , 2011, Experimental eye research.

[41]  J. Jonas,et al.  Predictions of Optic Nerve Traction Forces and Peripapillary Tissue Stresses Following Horizontal Eye Movements. , 2017, Investigative ophthalmology & visual science.

[42]  Dao-Yi Yu,et al.  Correlating morphometric parameters of the porcine optic nerve head in spectral domain optical coherence tomography with histological sections , 2010, British Journal of Ophthalmology.

[43]  Walter J. Riker.  A Review of J , 2010 .

[44]  Paul Kumar Upputuri,et al.  Dynamic in vivo imaging of small animal brain using pulsed laser diode-based photoacoustic tomography system. , 2017, Journal of biomedical optics.