Abstract

Laser speckle imaging (LSI) of mouse cerebral blood flow was compared through a transparent nanocrystalline yttria-stabilized zirconia (nc-YSZ) cranial implant over time (at days 0, 14, and 28, n = 3 mice), and vs. LSI through native skull (at day 60, n = 1 mouse). The average sharpness of imaged vessels was found to remain stable, with relative change in sharpness under 7.69% ± 1.2% over 28 days. Through-implant images of vessels at day 60 appeared sharper and smaller on average, with microvessels clearly visible, compared to through-skull images where vessels appeared blurred and distorted. These results suggest that long-term imaging through this implant is feasible.

© 2018 Optical Society of America under the terms of the OSA Open Access Publishing Agreement

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References

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2018 (1)

K. Kisler, D. Lazic, M. D. Sweeney, S. Plunkett, M. El Khatib, S. A. Vinogradov, D. A. Boas, S. Sakadži, and B. V. Zlokovic, “In vivo imaging and analysis of cerebrovascular hemodynamic responses and tissue oxygenation in the mouse brain,” Nat. Protoc. 13(6), 1377–1402 (2018).
[Crossref] [PubMed]

2017 (2)

S. C. Gnyawali, K. Blum, D. Pal, S. Ghatak, S. Khanna, S. Roy, and C. K. Sen, “Retooling laser speckle contrast analysis algorithm to enhance non-invasive high resolution laser speckle functional imaging of cutaneous microcirculation,” Sci. Rep. 7(1), 41048 (2017).
[Crossref] [PubMed]

M. I. Gutierrez, E. H. Penilla, L. Leija, A. Vera, J. E. Garay, and G. Aguilar, “Novel Cranial Implants of Yttria-Stabilized Zirconia as Acoustic Windows for Ultrasonic Brain Therapy,” Adv. Healthc. Mater. 6(21), 1700214 (2017).
[Crossref] [PubMed]

2016 (3)

C. Heo, H. Park, Y. T. Kim, E. Baeg, Y. H. Kim, S. G. Kim, and M. Suh, “A soft, transparent, freely accessible cranial window for chronic imaging and electrophysiology,” Sci. Rep. 6(1), 27818 (2016).
[Crossref] [PubMed]

Y. Damestani, D. E. Galan-Hoffman, D. Ortiz, P. Cabrales, and G. Aguilar, “Inflammatory response to implantation of transparent nanocrystalline yttria-stabilized zirconia using a dorsal window chamber model,” Nanomedicine (Lond.) 12(7), 1757–1763 (2016).
[Crossref] [PubMed]

W. Chen, K. Park, N. Volkow, Y. Pan, and C. Du, “cocaine-induced abnormal cerebral hemodynamic responses to forepaw stimulation assessed by integrated multi-wavelength spectroimaging and laser speckle contrast imaging,” IEEE J. Sel. Top Quantum Electron. 22, 6802608 (2016).

2015 (3)

V. Zuluaga-Ramirez, S. Rom, and Y. Persidsky, “Craniula: A cranial window technique for prolonged imaging of brain surface vasculature with simultaneous adjacent intracerebral injection,” Fluids Barriers CNS 12(1), 24 (2015).
[Crossref] [PubMed]

S. C. Gnyawali, K. G. Barki, S. S. Mathew-Steiner, S. Dixith, D. Vanzant, J. Kim, J. L. Dickerson, S. Datta, H. Powell, S. Roy, V. Bergdall, and C. K. Sen, “High-resolution harmonics ultrasound imaging for non-invasive characterization of wound healing in a pre-clinical swine model,” PLoS One 10(3), e0122327 (2015).
[Crossref] [PubMed]

I. Costantini, J. P. Ghobril, A. P. Di Giovanna, A. L. Allegra Mascaro, L. Silvestri, M. C. Müllenbroich, L. Onofri, V. Conti, F. Vanzi, L. Sacconi, R. Guerrini, H. Markram, G. Iannello, and F. S. Pavone, “A versatile clearing agent for multi-modal brain imaging,” Sci. Rep. 5(1), 9808 (2015).
[Crossref] [PubMed]

2014 (2)

S. Eriksson, J. Nilsson, and C. Sturesson, “Non-invasive imaging of microcirculation: a technology review,” Med. Devices (Auckl.) 7, 445–452 (2014).
[PubMed]

C. J. Roome and B. Kuhn, “Chronic cranial window with access port for repeated cellular manipulations, drug application, and electrophysiology,” Front. Cell. Neurosci. 8, 379 (2014).
[Crossref] [PubMed]

2013 (3)

M. Roustit and J. L. Cracowski, “Assessment of endothelial and neurovascular function in human skin microcirculation,” Trends Pharmacol. Sci. 34(7), 373–384 (2013).
[Crossref] [PubMed]

F. G. R. Fowkes, D. Rudan, I. Rudan, V. Aboyans, J. O. Denenberg, M. M. McDermott, P. E. Norman, U. K. A. Sampson, L. J. Williams, G. A. Mensah, and M. H. Criqui, “Comparison of global estimates of prevalence and risk factors for peripheral artery disease in 2000 and 2010: a systematic review and analysis,” Lancet 382(9901), 1329–1340 (2013).
[Crossref] [PubMed]

Y. Damestani, C. L. Reynolds, J. Szu, M. S. Hsu, Y. Kodera, D. K. Binder, B. H. Park, J. E. Garay, M. P. Rao, and G. Aguilar, “Transparent nanocrystalline yttria-stabilized-zirconia calvarium prosthesis,” Nanomedicine (Lond.) 9(8), 1135–1138 (2013).
[Crossref] [PubMed]

2012 (2)

A. Y. Shih, C. Mateo, P. J. Drew, P. S. Tsai, and D. Kleinfeld, “A polished and reinforced thinned-skull window for long-term imaging of the mouse brain,” J. Vis. Exp. 61, 3742 (2012).
[Crossref] [PubMed]

J. Wang, Y. Zhang, T. H. Xu, Q. M. Luo, and D. Zhu, “An innovative transparent cranial window based on skull optical clearing,” Laser Phys. Lett. 9(6), 469–473 (2012).
[Crossref]

2011 (1)

D. Rizzoni, C. Aalkjaer, C. De Ciuceis, E. Porteri, C. Rossini, C. A. Rosei, A. Sarkar, and E. A. Rosei, “How to assess microvascular structure in humans,” High Blood Press. Cardiovasc. Prev. 18(4), 169–177 (2011).
[Crossref] [PubMed]

2010 (6)

J. E. Garay, “Current-Activated, Pressure-Assisted Densification of Materials,” Annu. Rev. Mater. Res. 40(1), 445–468 (2010).
[Crossref]

K. Nakamura, T. Kanno, P. Milleding, and U. Ortengren, “Zirconia as a dental implant abutment material: a systematic review,” Int. J. Prosthodont. 23(4), 299–309 (2010).
[PubMed]

D. A. Boas and A. K. Dunn, “Laser speckle contrast imaging in biomedical optics,” J. Biomed. Opt. 15(1), 011109 (2010).
[Crossref] [PubMed]

A. B. Parthasarathy, S. M. Kazmi, and A. K. Dunn, “Quantitative imaging of ischemic stroke through thinned skull in mice with Multi Exposure Speckle Imaging,” Biomed. Opt. Express 1(1), 246–259 (2010).
[Crossref] [PubMed]

D. Zhu, J. Wang, Z. Zhi, X. Wen, and Q. Luo, “Imaging dermal blood flow through the intact rat skin with an optical clearing method,” J. Biomed. Opt. 15(2), 026008 (2010).
[Crossref] [PubMed]

M. X. Tang, D. S. Elson, R. Li, C. Dunsby, and R. J. Eckersley, “Photoacoustics, thermoacoustics, and acousto-optics for biomedical imaging,” Proc. Inst. Mech. Eng. H 224(2), 291–306 (2010).
[Crossref] [PubMed]

2009 (3)

N. Li, X. Jia, K. Murari, R. Parlapalli, A. Rege, and N. V. Thakor, “High spatiotemporal resolution imaging of the neurovascular response to electrical stimulation of rat peripheral trigeminal nerve as revealed by in vivo temporal laser speckle contrast,” J. Neurosci. Methods 176(2), 230–236 (2009).
[Crossref] [PubMed]

J. E. Alaniz, F. G. Perez-Gutierrez, G. Aguilar, and J. E. Garay, “Optical properties of transparent nanocrystalline yttria stabilized zirconia,” Opt. Mater. 32(1), 62–68 (2009).
[Crossref]

A. Holtmaat, T. Bonhoeffer, D. K. Chow, J. Chuckowree, V. De Paola, S. B. Hofer, M. Hübener, T. Keck, G. Knott, W. C. Lee, R. Mostany, T. D. Mrsic-Flogel, E. Nedivi, C. Portera-Cailliau, K. Svoboda, J. T. Trachtenberg, and L. Wilbrecht, “Long-term, high-resolution imaging in the mouse neocortex through a chronic cranial window,” Nat. Protoc. 4(8), 1128–1144 (2009).
[Crossref] [PubMed]

2008 (1)

S. R. Casolco, J. Xu, and J. E. Garay, “Transparent/translucent polycrystalline nanostructured yttria stabilized zirconia with varying colors,” Scr. Mater. 58(6), 516–519 (2008).
[Crossref]

2007 (3)

J. D. Briers, “Laser speckle contrast imaging for measuring blood flow,” Opt. Appl. 37, 1 (2007).

L. A. Sokolnicki, S. K. Roberts, B. W. Wilkins, A. Basu, and N. Charkoudian, “Contribution of nitric oxide to cutaneous microvascular dilation in individuals with type 2 diabetes mellitus,” Am. J. Physiol. Endocrinol. Metab. 292(1), E314–E318 (2007).
[Crossref] [PubMed]

Z. Khalil, D. LoGiudice, B. Khodr, P. Maruff, and C. Masters, “Impaired peripheral endothelial microvascular responsiveness in Alzheimer’s disease,” J. Alzheimers Dis. 11(1), 25–32 (2007).
[Crossref] [PubMed]

2006 (2)

P. Li, S. Ni, L. Zhang, S. Zeng, and Q. Luo, “Imaging cerebral blood flow through the intact rat skull with temporal laser speckle imaging,” Opt. Lett. 31(12), 1824–1826 (2006).
[Crossref] [PubMed]

E. B. Hutchinson, B. Stefanovic, A. P. Koretsky, and A. C. Silva, “Spatial flow-volume dissociation of the cerebral microcirculatory response to mild hypercapnia,” Neuroimage 32(2), 520–530 (2006).
[Crossref] [PubMed]

2005 (3)

2003 (1)

H. Cheng, Q. Luo, S. Zeng, S. Chen, J. Cen, and H. Gong, “Modified laser speckle imaging method with improved spatial resolution,” J. Biomed. Opt. 8(3), 559–564 (2003).
[Crossref] [PubMed]

2002 (1)

2001 (1)

A. K. Dunn, H. Bolay, M. A. Moskowitz, and D. A. Boas, “Dynamic imaging of cerebral blood flow using laser speckle,” J. Cereb. Blood Flow Metab. 21(3), 195–201 (2001).
[Crossref] [PubMed]

1996 (1)

J. D. Briers and S. Webster, “Laser speckle contrast analysis (LASCA): a nonscanning, full-field technique for monitoring capillary blood flow,” J. Biomed. Opt. 1(2), 174–179 (1996).
[Crossref] [PubMed]

1993 (1)

S. F. Hulbert, “The use of alumina and zirconia in surgical implants,” An Introduction to Bioceramics 1, 25–40 (1993).
[Crossref]

1989 (2)

P. Christel, A. Meunier, M. Heller, J. P. Torre, and C. N. Peille, “Mechanical properties and short-term in-vivo evaluation of yttrium-oxide-partially-stabilized zirconia,” J. Biomed. Mater. Res. 23(1), 45–61 (1989).
[Crossref] [PubMed]

Y. Aizu, H. Ambar, T. Yamamoto, and T. Asakura, “Measurements of flow velocity in a microscopic region using dynamic laser speckles based on the photon correlation,” Opt. Commun. 72(5), 269–273 (1989).
[Crossref]

1988 (1)

P. Christel, A. Meunier, J. M. Dorlot, J. M. Crolet, J. Witvoet, L. Sedel, and P. Boutin, “Biomechanical compatibility and design of ceramic implants for orthopedic surgery,” Ann. N. Y. Acad. Sci. 523(1 Bioceramics), 234–256 (1988).
[Crossref] [PubMed]

1987 (1)

1984 (1)

J. K. Gourley and D. D. Heistad, “Characteristics of reactive hyperemia in the cerebral circulation,” Am. J. Physiol. 246(1), H52–H58 (1984).
[PubMed]

1981 (1)

T. Asakura and N. Takai, “Dynamic laser speckles and their application to velocity measurements of the diffuse object,” Appl. Phys. (Berl.) 25(3), 179–194 (1981).
[Crossref]

1976 (1)

Aalkjaer, C.

D. Rizzoni, C. Aalkjaer, C. De Ciuceis, E. Porteri, C. Rossini, C. A. Rosei, A. Sarkar, and E. A. Rosei, “How to assess microvascular structure in humans,” High Blood Press. Cardiovasc. Prev. 18(4), 169–177 (2011).
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Aboyans, V.

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M. I. Gutierrez, E. H. Penilla, L. Leija, A. Vera, J. E. Garay, and G. Aguilar, “Novel Cranial Implants of Yttria-Stabilized Zirconia as Acoustic Windows for Ultrasonic Brain Therapy,” Adv. Healthc. Mater. 6(21), 1700214 (2017).
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S. C. Gnyawali, K. Blum, D. Pal, S. Ghatak, S. Khanna, S. Roy, and C. K. Sen, “Retooling laser speckle contrast analysis algorithm to enhance non-invasive high resolution laser speckle functional imaging of cutaneous microcirculation,” Sci. Rep. 7(1), 41048 (2017).
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S. R. Casolco, J. Xu, and J. E. Garay, “Transparent/translucent polycrystalline nanostructured yttria stabilized zirconia with varying colors,” Scr. Mater. 58(6), 516–519 (2008).
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H. Cheng, Q. Luo, S. Zeng, S. Chen, J. Cen, and H. Gong, “Modified laser speckle imaging method with improved spatial resolution,” J. Biomed. Opt. 8(3), 559–564 (2003).
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L. A. Sokolnicki, S. K. Roberts, B. W. Wilkins, A. Basu, and N. Charkoudian, “Contribution of nitric oxide to cutaneous microvascular dilation in individuals with type 2 diabetes mellitus,” Am. J. Physiol. Endocrinol. Metab. 292(1), E314–E318 (2007).
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Chen, S.

H. Cheng, Q. Luo, S. Zeng, S. Chen, J. Cen, and H. Gong, “Modified laser speckle imaging method with improved spatial resolution,” J. Biomed. Opt. 8(3), 559–564 (2003).
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W. Chen, K. Park, N. Volkow, Y. Pan, and C. Du, “cocaine-induced abnormal cerebral hemodynamic responses to forepaw stimulation assessed by integrated multi-wavelength spectroimaging and laser speckle contrast imaging,” IEEE J. Sel. Top Quantum Electron. 22, 6802608 (2016).

Cheng, H.

H. Cheng, Q. Luo, S. Zeng, S. Chen, J. Cen, and H. Gong, “Modified laser speckle imaging method with improved spatial resolution,” J. Biomed. Opt. 8(3), 559–564 (2003).
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P. Christel, A. Meunier, J. M. Dorlot, J. M. Crolet, J. Witvoet, L. Sedel, and P. Boutin, “Biomechanical compatibility and design of ceramic implants for orthopedic surgery,” Ann. N. Y. Acad. Sci. 523(1 Bioceramics), 234–256 (1988).
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Y. Damestani, D. E. Galan-Hoffman, D. Ortiz, P. Cabrales, and G. Aguilar, “Inflammatory response to implantation of transparent nanocrystalline yttria-stabilized zirconia using a dorsal window chamber model,” Nanomedicine (Lond.) 12(7), 1757–1763 (2016).
[Crossref] [PubMed]

Y. Damestani, C. L. Reynolds, J. Szu, M. S. Hsu, Y. Kodera, D. K. Binder, B. H. Park, J. E. Garay, M. P. Rao, and G. Aguilar, “Transparent nanocrystalline yttria-stabilized-zirconia calvarium prosthesis,” Nanomedicine (Lond.) 9(8), 1135–1138 (2013).
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S. C. Gnyawali, K. G. Barki, S. S. Mathew-Steiner, S. Dixith, D. Vanzant, J. Kim, J. L. Dickerson, S. Datta, H. Powell, S. Roy, V. Bergdall, and C. K. Sen, “High-resolution harmonics ultrasound imaging for non-invasive characterization of wound healing in a pre-clinical swine model,” PLoS One 10(3), e0122327 (2015).
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Di Giovanna, A. P.

I. Costantini, J. P. Ghobril, A. P. Di Giovanna, A. L. Allegra Mascaro, L. Silvestri, M. C. Müllenbroich, L. Onofri, V. Conti, F. Vanzi, L. Sacconi, R. Guerrini, H. Markram, G. Iannello, and F. S. Pavone, “A versatile clearing agent for multi-modal brain imaging,” Sci. Rep. 5(1), 9808 (2015).
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S. C. Gnyawali, K. G. Barki, S. S. Mathew-Steiner, S. Dixith, D. Vanzant, J. Kim, J. L. Dickerson, S. Datta, H. Powell, S. Roy, V. Bergdall, and C. K. Sen, “High-resolution harmonics ultrasound imaging for non-invasive characterization of wound healing in a pre-clinical swine model,” PLoS One 10(3), e0122327 (2015).
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P. Christel, A. Meunier, J. M. Dorlot, J. M. Crolet, J. Witvoet, L. Sedel, and P. Boutin, “Biomechanical compatibility and design of ceramic implants for orthopedic surgery,” Ann. N. Y. Acad. Sci. 523(1 Bioceramics), 234–256 (1988).
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W. Chen, K. Park, N. Volkow, Y. Pan, and C. Du, “cocaine-induced abnormal cerebral hemodynamic responses to forepaw stimulation assessed by integrated multi-wavelength spectroimaging and laser speckle contrast imaging,” IEEE J. Sel. Top Quantum Electron. 22, 6802608 (2016).

Dunn, A. K.

Dunsby, C.

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Fujii, H.

Galan-Hoffman, D. E.

Y. Damestani, D. E. Galan-Hoffman, D. Ortiz, P. Cabrales, and G. Aguilar, “Inflammatory response to implantation of transparent nanocrystalline yttria-stabilized zirconia using a dorsal window chamber model,” Nanomedicine (Lond.) 12(7), 1757–1763 (2016).
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M. I. Gutierrez, E. H. Penilla, L. Leija, A. Vera, J. E. Garay, and G. Aguilar, “Novel Cranial Implants of Yttria-Stabilized Zirconia as Acoustic Windows for Ultrasonic Brain Therapy,” Adv. Healthc. Mater. 6(21), 1700214 (2017).
[Crossref] [PubMed]

Y. Damestani, C. L. Reynolds, J. Szu, M. S. Hsu, Y. Kodera, D. K. Binder, B. H. Park, J. E. Garay, M. P. Rao, and G. Aguilar, “Transparent nanocrystalline yttria-stabilized-zirconia calvarium prosthesis,” Nanomedicine (Lond.) 9(8), 1135–1138 (2013).
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[Crossref]

S. R. Casolco, J. Xu, and J. E. Garay, “Transparent/translucent polycrystalline nanostructured yttria stabilized zirconia with varying colors,” Scr. Mater. 58(6), 516–519 (2008).
[Crossref]

Ghatak, S.

S. C. Gnyawali, K. Blum, D. Pal, S. Ghatak, S. Khanna, S. Roy, and C. K. Sen, “Retooling laser speckle contrast analysis algorithm to enhance non-invasive high resolution laser speckle functional imaging of cutaneous microcirculation,” Sci. Rep. 7(1), 41048 (2017).
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I. Costantini, J. P. Ghobril, A. P. Di Giovanna, A. L. Allegra Mascaro, L. Silvestri, M. C. Müllenbroich, L. Onofri, V. Conti, F. Vanzi, L. Sacconi, R. Guerrini, H. Markram, G. Iannello, and F. S. Pavone, “A versatile clearing agent for multi-modal brain imaging,” Sci. Rep. 5(1), 9808 (2015).
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S. C. Gnyawali, K. Blum, D. Pal, S. Ghatak, S. Khanna, S. Roy, and C. K. Sen, “Retooling laser speckle contrast analysis algorithm to enhance non-invasive high resolution laser speckle functional imaging of cutaneous microcirculation,” Sci. Rep. 7(1), 41048 (2017).
[Crossref] [PubMed]

S. C. Gnyawali, K. G. Barki, S. S. Mathew-Steiner, S. Dixith, D. Vanzant, J. Kim, J. L. Dickerson, S. Datta, H. Powell, S. Roy, V. Bergdall, and C. K. Sen, “High-resolution harmonics ultrasound imaging for non-invasive characterization of wound healing in a pre-clinical swine model,” PLoS One 10(3), e0122327 (2015).
[Crossref] [PubMed]

Gong, H.

H. Cheng, Q. Luo, S. Zeng, S. Chen, J. Cen, and H. Gong, “Modified laser speckle imaging method with improved spatial resolution,” J. Biomed. Opt. 8(3), 559–564 (2003).
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Gutierrez, M. I.

M. I. Gutierrez, E. H. Penilla, L. Leija, A. Vera, J. E. Garay, and G. Aguilar, “Novel Cranial Implants of Yttria-Stabilized Zirconia as Acoustic Windows for Ultrasonic Brain Therapy,” Adv. Healthc. Mater. 6(21), 1700214 (2017).
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Heo, C.

C. Heo, H. Park, Y. T. Kim, E. Baeg, Y. H. Kim, S. G. Kim, and M. Suh, “A soft, transparent, freely accessible cranial window for chronic imaging and electrophysiology,” Sci. Rep. 6(1), 27818 (2016).
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N. Li, X. Jia, K. Murari, R. Parlapalli, A. Rege, and N. V. Thakor, “High spatiotemporal resolution imaging of the neurovascular response to electrical stimulation of rat peripheral trigeminal nerve as revealed by in vivo temporal laser speckle contrast,” J. Neurosci. Methods 176(2), 230–236 (2009).
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Y. Damestani, C. L. Reynolds, J. Szu, M. S. Hsu, Y. Kodera, D. K. Binder, B. H. Park, J. E. Garay, M. P. Rao, and G. Aguilar, “Transparent nanocrystalline yttria-stabilized-zirconia calvarium prosthesis,” Nanomedicine (Lond.) 9(8), 1135–1138 (2013).
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D. Rizzoni, C. Aalkjaer, C. De Ciuceis, E. Porteri, C. Rossini, C. A. Rosei, A. Sarkar, and E. A. Rosei, “How to assess microvascular structure in humans,” High Blood Press. Cardiovasc. Prev. 18(4), 169–177 (2011).
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Roberts, S. K.

L. A. Sokolnicki, S. K. Roberts, B. W. Wilkins, A. Basu, and N. Charkoudian, “Contribution of nitric oxide to cutaneous microvascular dilation in individuals with type 2 diabetes mellitus,” Am. J. Physiol. Endocrinol. Metab. 292(1), E314–E318 (2007).
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Rom, S.

V. Zuluaga-Ramirez, S. Rom, and Y. Persidsky, “Craniula: A cranial window technique for prolonged imaging of brain surface vasculature with simultaneous adjacent intracerebral injection,” Fluids Barriers CNS 12(1), 24 (2015).
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Roome, C. J.

C. J. Roome and B. Kuhn, “Chronic cranial window with access port for repeated cellular manipulations, drug application, and electrophysiology,” Front. Cell. Neurosci. 8, 379 (2014).
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Rosei, C. A.

D. Rizzoni, C. Aalkjaer, C. De Ciuceis, E. Porteri, C. Rossini, C. A. Rosei, A. Sarkar, and E. A. Rosei, “How to assess microvascular structure in humans,” High Blood Press. Cardiovasc. Prev. 18(4), 169–177 (2011).
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Rosei, E. A.

D. Rizzoni, C. Aalkjaer, C. De Ciuceis, E. Porteri, C. Rossini, C. A. Rosei, A. Sarkar, and E. A. Rosei, “How to assess microvascular structure in humans,” High Blood Press. Cardiovasc. Prev. 18(4), 169–177 (2011).
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D. Rizzoni, C. Aalkjaer, C. De Ciuceis, E. Porteri, C. Rossini, C. A. Rosei, A. Sarkar, and E. A. Rosei, “How to assess microvascular structure in humans,” High Blood Press. Cardiovasc. Prev. 18(4), 169–177 (2011).
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S. J. Rothberg and B. J. Halkon, “Laser vibrometry meets laser speckle,” in Sixth International Conference on Vibration Measurements by Laser Techniques: Advances and Applications, (SPIE, 2004), 12.

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M. Roustit and J. L. Cracowski, “Assessment of endothelial and neurovascular function in human skin microcirculation,” Trends Pharmacol. Sci. 34(7), 373–384 (2013).
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S. C. Gnyawali, K. Blum, D. Pal, S. Ghatak, S. Khanna, S. Roy, and C. K. Sen, “Retooling laser speckle contrast analysis algorithm to enhance non-invasive high resolution laser speckle functional imaging of cutaneous microcirculation,” Sci. Rep. 7(1), 41048 (2017).
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F. G. R. Fowkes, D. Rudan, I. Rudan, V. Aboyans, J. O. Denenberg, M. M. McDermott, P. E. Norman, U. K. A. Sampson, L. J. Williams, G. A. Mensah, and M. H. Criqui, “Comparison of global estimates of prevalence and risk factors for peripheral artery disease in 2000 and 2010: a systematic review and analysis,” Lancet 382(9901), 1329–1340 (2013).
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I. Costantini, J. P. Ghobril, A. P. Di Giovanna, A. L. Allegra Mascaro, L. Silvestri, M. C. Müllenbroich, L. Onofri, V. Conti, F. Vanzi, L. Sacconi, R. Guerrini, H. Markram, G. Iannello, and F. S. Pavone, “A versatile clearing agent for multi-modal brain imaging,” Sci. Rep. 5(1), 9808 (2015).
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K. Kisler, D. Lazic, M. D. Sweeney, S. Plunkett, M. El Khatib, S. A. Vinogradov, D. A. Boas, S. Sakadži, and B. V. Zlokovic, “In vivo imaging and analysis of cerebrovascular hemodynamic responses and tissue oxygenation in the mouse brain,” Nat. Protoc. 13(6), 1377–1402 (2018).
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F. G. R. Fowkes, D. Rudan, I. Rudan, V. Aboyans, J. O. Denenberg, M. M. McDermott, P. E. Norman, U. K. A. Sampson, L. J. Williams, G. A. Mensah, and M. H. Criqui, “Comparison of global estimates of prevalence and risk factors for peripheral artery disease in 2000 and 2010: a systematic review and analysis,” Lancet 382(9901), 1329–1340 (2013).
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D. Rizzoni, C. Aalkjaer, C. De Ciuceis, E. Porteri, C. Rossini, C. A. Rosei, A. Sarkar, and E. A. Rosei, “How to assess microvascular structure in humans,” High Blood Press. Cardiovasc. Prev. 18(4), 169–177 (2011).
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P. Christel, A. Meunier, J. M. Dorlot, J. M. Crolet, J. Witvoet, L. Sedel, and P. Boutin, “Biomechanical compatibility and design of ceramic implants for orthopedic surgery,” Ann. N. Y. Acad. Sci. 523(1 Bioceramics), 234–256 (1988).
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S. C. Gnyawali, K. Blum, D. Pal, S. Ghatak, S. Khanna, S. Roy, and C. K. Sen, “Retooling laser speckle contrast analysis algorithm to enhance non-invasive high resolution laser speckle functional imaging of cutaneous microcirculation,” Sci. Rep. 7(1), 41048 (2017).
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L. A. Sokolnicki, S. K. Roberts, B. W. Wilkins, A. Basu, and N. Charkoudian, “Contribution of nitric oxide to cutaneous microvascular dilation in individuals with type 2 diabetes mellitus,” Am. J. Physiol. Endocrinol. Metab. 292(1), E314–E318 (2007).
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K. Kisler, D. Lazic, M. D. Sweeney, S. Plunkett, M. El Khatib, S. A. Vinogradov, D. A. Boas, S. Sakadži, and B. V. Zlokovic, “In vivo imaging and analysis of cerebrovascular hemodynamic responses and tissue oxygenation in the mouse brain,” Nat. Protoc. 13(6), 1377–1402 (2018).
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Y. Damestani, C. L. Reynolds, J. Szu, M. S. Hsu, Y. Kodera, D. K. Binder, B. H. Park, J. E. Garay, M. P. Rao, and G. Aguilar, “Transparent nanocrystalline yttria-stabilized-zirconia calvarium prosthesis,” Nanomedicine (Lond.) 9(8), 1135–1138 (2013).
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T. Asakura and N. Takai, “Dynamic laser speckles and their application to velocity measurements of the diffuse object,” Appl. Phys. (Berl.) 25(3), 179–194 (1981).
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N. Li, X. Jia, K. Murari, R. Parlapalli, A. Rege, and N. V. Thakor, “High spatiotemporal resolution imaging of the neurovascular response to electrical stimulation of rat peripheral trigeminal nerve as revealed by in vivo temporal laser speckle contrast,” J. Neurosci. Methods 176(2), 230–236 (2009).
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A. Y. Shih, C. Mateo, P. J. Drew, P. S. Tsai, and D. Kleinfeld, “A polished and reinforced thinned-skull window for long-term imaging of the mouse brain,” J. Vis. Exp. 61, 3742 (2012).
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S. C. Gnyawali, K. G. Barki, S. S. Mathew-Steiner, S. Dixith, D. Vanzant, J. Kim, J. L. Dickerson, S. Datta, H. Powell, S. Roy, V. Bergdall, and C. K. Sen, “High-resolution harmonics ultrasound imaging for non-invasive characterization of wound healing in a pre-clinical swine model,” PLoS One 10(3), e0122327 (2015).
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I. Costantini, J. P. Ghobril, A. P. Di Giovanna, A. L. Allegra Mascaro, L. Silvestri, M. C. Müllenbroich, L. Onofri, V. Conti, F. Vanzi, L. Sacconi, R. Guerrini, H. Markram, G. Iannello, and F. S. Pavone, “A versatile clearing agent for multi-modal brain imaging,” Sci. Rep. 5(1), 9808 (2015).
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M. I. Gutierrez, E. H. Penilla, L. Leija, A. Vera, J. E. Garay, and G. Aguilar, “Novel Cranial Implants of Yttria-Stabilized Zirconia as Acoustic Windows for Ultrasonic Brain Therapy,” Adv. Healthc. Mater. 6(21), 1700214 (2017).
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K. Kisler, D. Lazic, M. D. Sweeney, S. Plunkett, M. El Khatib, S. A. Vinogradov, D. A. Boas, S. Sakadži, and B. V. Zlokovic, “In vivo imaging and analysis of cerebrovascular hemodynamic responses and tissue oxygenation in the mouse brain,” Nat. Protoc. 13(6), 1377–1402 (2018).
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W. Chen, K. Park, N. Volkow, Y. Pan, and C. Du, “cocaine-induced abnormal cerebral hemodynamic responses to forepaw stimulation assessed by integrated multi-wavelength spectroimaging and laser speckle contrast imaging,” IEEE J. Sel. Top Quantum Electron. 22, 6802608 (2016).

Wang, J.

J. Wang, Y. Zhang, T. H. Xu, Q. M. Luo, and D. Zhu, “An innovative transparent cranial window based on skull optical clearing,” Laser Phys. Lett. 9(6), 469–473 (2012).
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D. Zhu, J. Wang, Z. Zhi, X. Wen, and Q. Luo, “Imaging dermal blood flow through the intact rat skin with an optical clearing method,” J. Biomed. Opt. 15(2), 026008 (2010).
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Wang, Z.

Q. Liu, Z. Wang, and Q. Luo, “Temporal clustering analysis of cerebral blood flow activation maps measured by laser speckle contrast imaging,” J. Biomed. Opt. 10(2), 024019 (2005).
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J. D. Briers and S. Webster, “Laser speckle contrast analysis (LASCA): a nonscanning, full-field technique for monitoring capillary blood flow,” J. Biomed. Opt. 1(2), 174–179 (1996).
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D. Zhu, J. Wang, Z. Zhi, X. Wen, and Q. Luo, “Imaging dermal blood flow through the intact rat skin with an optical clearing method,” J. Biomed. Opt. 15(2), 026008 (2010).
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L. A. Sokolnicki, S. K. Roberts, B. W. Wilkins, A. Basu, and N. Charkoudian, “Contribution of nitric oxide to cutaneous microvascular dilation in individuals with type 2 diabetes mellitus,” Am. J. Physiol. Endocrinol. Metab. 292(1), E314–E318 (2007).
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F. G. R. Fowkes, D. Rudan, I. Rudan, V. Aboyans, J. O. Denenberg, M. M. McDermott, P. E. Norman, U. K. A. Sampson, L. J. Williams, G. A. Mensah, and M. H. Criqui, “Comparison of global estimates of prevalence and risk factors for peripheral artery disease in 2000 and 2010: a systematic review and analysis,” Lancet 382(9901), 1329–1340 (2013).
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P. Christel, A. Meunier, J. M. Dorlot, J. M. Crolet, J. Witvoet, L. Sedel, and P. Boutin, “Biomechanical compatibility and design of ceramic implants for orthopedic surgery,” Ann. N. Y. Acad. Sci. 523(1 Bioceramics), 234–256 (1988).
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J. Wang, Y. Zhang, T. H. Xu, Q. M. Luo, and D. Zhu, “An innovative transparent cranial window based on skull optical clearing,” Laser Phys. Lett. 9(6), 469–473 (2012).
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Zhang, L.

Zhang, Y.

J. Wang, Y. Zhang, T. H. Xu, Q. M. Luo, and D. Zhu, “An innovative transparent cranial window based on skull optical clearing,” Laser Phys. Lett. 9(6), 469–473 (2012).
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Zhi, Z.

D. Zhu, J. Wang, Z. Zhi, X. Wen, and Q. Luo, “Imaging dermal blood flow through the intact rat skin with an optical clearing method,” J. Biomed. Opt. 15(2), 026008 (2010).
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J. Wang, Y. Zhang, T. H. Xu, Q. M. Luo, and D. Zhu, “An innovative transparent cranial window based on skull optical clearing,” Laser Phys. Lett. 9(6), 469–473 (2012).
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K. Kisler, D. Lazic, M. D. Sweeney, S. Plunkett, M. El Khatib, S. A. Vinogradov, D. A. Boas, S. Sakadži, and B. V. Zlokovic, “In vivo imaging and analysis of cerebrovascular hemodynamic responses and tissue oxygenation in the mouse brain,” Nat. Protoc. 13(6), 1377–1402 (2018).
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Zuluaga-Ramirez, V.

V. Zuluaga-Ramirez, S. Rom, and Y. Persidsky, “Craniula: A cranial window technique for prolonged imaging of brain surface vasculature with simultaneous adjacent intracerebral injection,” Fluids Barriers CNS 12(1), 24 (2015).
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Adv. Healthc. Mater. (1)

M. I. Gutierrez, E. H. Penilla, L. Leija, A. Vera, J. E. Garay, and G. Aguilar, “Novel Cranial Implants of Yttria-Stabilized Zirconia as Acoustic Windows for Ultrasonic Brain Therapy,” Adv. Healthc. Mater. 6(21), 1700214 (2017).
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T. Asakura and N. Takai, “Dynamic laser speckles and their application to velocity measurements of the diffuse object,” Appl. Phys. (Berl.) 25(3), 179–194 (1981).
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Biomed. Opt. Express (1)

Fluids Barriers CNS (1)

V. Zuluaga-Ramirez, S. Rom, and Y. Persidsky, “Craniula: A cranial window technique for prolonged imaging of brain surface vasculature with simultaneous adjacent intracerebral injection,” Fluids Barriers CNS 12(1), 24 (2015).
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C. J. Roome and B. Kuhn, “Chronic cranial window with access port for repeated cellular manipulations, drug application, and electrophysiology,” Front. Cell. Neurosci. 8, 379 (2014).
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D. Rizzoni, C. Aalkjaer, C. De Ciuceis, E. Porteri, C. Rossini, C. A. Rosei, A. Sarkar, and E. A. Rosei, “How to assess microvascular structure in humans,” High Blood Press. Cardiovasc. Prev. 18(4), 169–177 (2011).
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IEEE J. Sel. Top Quantum Electron. (1)

W. Chen, K. Park, N. Volkow, Y. Pan, and C. Du, “cocaine-induced abnormal cerebral hemodynamic responses to forepaw stimulation assessed by integrated multi-wavelength spectroimaging and laser speckle contrast imaging,” IEEE J. Sel. Top Quantum Electron. 22, 6802608 (2016).

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P. Christel, A. Meunier, M. Heller, J. P. Torre, and C. N. Peille, “Mechanical properties and short-term in-vivo evaluation of yttrium-oxide-partially-stabilized zirconia,” J. Biomed. Mater. Res. 23(1), 45–61 (1989).
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J. Biomed. Opt. (5)

D. Zhu, J. Wang, Z. Zhi, X. Wen, and Q. Luo, “Imaging dermal blood flow through the intact rat skin with an optical clearing method,” J. Biomed. Opt. 15(2), 026008 (2010).
[Crossref] [PubMed]

J. D. Briers and S. Webster, “Laser speckle contrast analysis (LASCA): a nonscanning, full-field technique for monitoring capillary blood flow,” J. Biomed. Opt. 1(2), 174–179 (1996).
[Crossref] [PubMed]

H. Cheng, Q. Luo, S. Zeng, S. Chen, J. Cen, and H. Gong, “Modified laser speckle imaging method with improved spatial resolution,” J. Biomed. Opt. 8(3), 559–564 (2003).
[Crossref] [PubMed]

Q. Liu, Z. Wang, and Q. Luo, “Temporal clustering analysis of cerebral blood flow activation maps measured by laser speckle contrast imaging,” J. Biomed. Opt. 10(2), 024019 (2005).
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Figures (7)

Fig. 1
Fig. 1 Reflectance and transmittance spectra of Window to the Brain implant.
Fig. 2
Fig. 2 a) Illustration of the Window to the Brain concept in human and mouse skulls, b) Schematic of the experimental imaging setup, c) Schematic of the craniotomy location on murine cranium and regions of interest: ROI 1, the nc-YSZ implant and ROI 2, the left parietal bone, d) Timeline for imaging procedures.
Fig. 3
Fig. 3 a) Regular images and LSI images for exposure times of 1, 2, 6, and 10 ms, at 0, 14 and 28 days post-surgery from Mouse 3 (scale bars = 1 mm). b) Contrast intensity profiles of lines across the images (shown as a dashed line in panel a) at 0, 14 and 28 days post-surgery from Mouse 3. The arrows in a) show the vessels that are intersected by the profile lines shown in b), labeled as V1 through V4 in day 0 image and profile (V4 arrow was not shown in day 14 and day 28 since the microvessel is not visible). The inset in b) shows how noise parameters, |ΔK|, FWHM and fall distance are determined from the line profiles.
Fig. 4
Fig. 4 a) SNR for different exposure times and imaging time points (mean and standard error) and b) Relative change in fall distance between days 14 and 28 vs day 0 for 3 vessels each of Mice 1-3 (dashed lines represent mean change i5n fall distance for all 9 vessels).
Fig. 5
Fig. 5 a) LSI temporal contrast images for 4 exposure times in Mouse 4. The left side of each image is the WttB implant (ROI 1), and ROI 2 is the corresponding region of skull on the right side of each image. b) Regular image of implant, showing the arbitrary locations where line profiles were taken. c) Example contrast intensity profiles along the midline of ROI 1 and 2 for exposure time 6 ms. The arrows in a) and c) show the vessels that are intersected by the midline intensity profiles. Scale bars = 1 mm.
Fig. 6
Fig. 6 a) Mean SNR of contrast intensity along arbitrary line profiles on the implant and skull for 4 separate exposure times (error bars represent standard error), b) and c) SNR and sharpness (respectively) vs FWHM for all vessels intersected by arbitrary line profiles on the implant and skull for the LSI temporal contrast image acquired with 6 ms exposure time.
Fig. 7
Fig. 7 Relative blood flow velocity in the 6 ms exposure time LSI temporal contrast image from Mouse 4. Scale bar = 1 mm.

Equations (3)

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K t (x,y)= σ (x,y) I (x,y) = 1 (N1) { n=1 N [ I (x,y) (n) I (x,y) ] 2 ) } I (x,y)
SNR= ΔK σ K n
Relative fall distance= Fall distance-Fall distanc e Day0 Fall distanc e Day0

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