Abstract

Focused ultrasound (FUS) in combination with microbubbles temporally and locally increases the permeability of the blood-brain barrier (BBB) for facilitating drug delivery. However, the temporary effects of FUS on the brain microstructure and microcirculation need to be addressed. We used label-free optical coherence tomography (OCT) and OCT angiography (OCTA) to investigate the morphological and microcirculation changes in mouse brains due to FUS exposure at different power levels. Additionally, the recovery progress of the induced effects was studied. The results show that FUS exposure causes cerebral vessel dilation and can be identified and quantitatively analyzed via OCT/OCTA. Micro-hemorrhages can be detected when an excessive FUS exposure power is applied, causing the degradation of OCTA signal owing to strong scattering by leaked red blood cells (RBCs) and weaker backscattered intensity from RBCs in vessels. The vessel dilation effect due to FUS exposure was found to abate in several hours. This study demonstrates that the FUS-induced cerebral transiently dilated effects can be in-vivo differentiated and monitored with OCTA, and shows the feasibility of using OCT/OCTA as a novel tool for long-time monitoring of cerebral vascular dynamics during FUS-BBB opening process.

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

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References

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    [Crossref] [PubMed]

2017 (1)

2014 (6)

M. T. Tsai, F. Y. Chang, C. K. Lee, C. S. A. Gong, Y. X. Lin, J. D. Lee, C. H. Yang, and H. L. Liu, “Investigation of temporal vascular effects induced by focused ultrasound treatment with speckle-variance optical coherence tomography,” Biomed. Opt. Express 5(7), 2009–2022 (2014).
[Crossref] [PubMed]

H. L. Liu, C. H. Fan, C. Y. Ting, and C. K. Yeh, “Combining microbubbles and ultrasound for drug delivery to brain tumors: current progress and overview,” Theranostics 4(4), 432–444 (2014).
[Crossref] [PubMed]

E. Nance, K. Timbie, G. W. Miller, J. Song, C. Louttit, A. L. Klibanov, T. Y. Shih, G. Swaminathan, R. J. Tamargo, G. F. Woodworth, J. Hanes, and R. J. Price, “Non-invasive delivery of stealth, brain-penetrating nanoparticles across the blood-brain barrier using MRI-guided focused ultrasound,” J. Control. Release 189, 123–132 (2014).
[Crossref] [PubMed]

C. H. Fan, W. H. Lin, C. Y. Ting, W. Y. Chai, T. C. Yen, H. L. Liu, and C. K. Yeh, “Contrast-Enhanced Ultrasound Imaging for the Detection of Focused Ultrasound-Induced Blood-Brain Barrier Opening,” Theranostics 4(10), 1014–1025 (2014).
[Crossref] [PubMed]

A. Burgess, T. Nhan, C. Moffatt, A. L. Klibanov, and K. Hynynen, “Analysis of focused ultrasound-induced blood-brain barrier permeability in a mouse model of Alzheimer’s disease using two-photon microscopy,” J. Control. Release 192, 243–248 (2014).
[Crossref] [PubMed]

R. A. Leitgeb, R. M. Werkmeister, C. Blatter, and L. Schmetterer, “Doppler optical coherence tomography,” Prog. Retin. Eye Res. 41, 26–43 (2014).
[Crossref] [PubMed]

2013 (2)

T. Nhan, A. Burgess, E. E. Cho, B. Stefanovic, L. Lilge, and K. Hynynen, “Drug delivery to the brain by focused ultrasound induced blood-brain barrier disruption: Quantitative evaluation of enhanced permeability of cerebral vasculature using two-photon microscopy,” J. Control. Release 172(1), 274–280 (2013).
[Crossref] [PubMed]

M. T. Tsai, C. K. Lee, K. M. Lin, Y. X. Lin, T. H. Lin, T. C. Chang, J. D. Lee, and H. L. Liu, “Quantitative observation of focused-ultrasound-induced vascular leakage and deformation via fluorescein angiography and optical coherence tomography,” J. Biomed. Opt. 18(10), 101307 (2013).
[Crossref] [PubMed]

2012 (1)

C. H. Fan, H. L. Liu, C. Y. Huang, Y. J. Ma, T. C. Yen, and C. K. Yeh, “Detection of intracerebral hemorrhage and transient blood-supply shortage in focused-ultrasound-induced blood-brain barrier disruption by ultrasound imaging,” Ultrasound Med. Biol. 38(8), 1372–1382 (2012).
[Crossref] [PubMed]

2011 (2)

E. Jonathan, J. Enfield, and M. J. Leahy, “Correlation mapping method for generating microcirculation morphology from optical coherence tomography (OCT) intensity images,” J. Biophotonics 4(9), 583–587 (2011).
[PubMed]

J. Enfield, E. Jonathan, and M. Leahy, “In vivo imaging of the microcirculation of the volar forearm using correlation mapping optical coherence tomography (cmOCT),” Biomed. Opt. Express 2(5), 1184–1193 (2011).
[Crossref] [PubMed]

2010 (2)

N. McDannold, G. Clement, P. Black, F. Jolesz, and K. Hynynen, “Transcranial MRI-guided focused ultrasound surgery of brain tumors: Initial findings in three patients,” Neurosurgery 66(2), 323–332 (2010).
[Crossref] [PubMed]

A. Mariampillai, M. K. Leung, M. Jarvi, B. A. Standish, K. Lee, B. C. Wilson, A. Vitkin, and V. X. Yang, “Optimized speckle variance OCT imaging of microvasculature,” Opt. Lett. 35(8), 1257–1259 (2010).
[Crossref] [PubMed]

2009 (1)

2008 (3)

2007 (1)

A. M. Zysk, F. T. Nguyen, A. L. Oldenburg, D. L. Marks, and S. A. Boppart, “Optical coherence tomography: a review of clinical development from bench to bedside,” J. Biomed. Opt. 12(5), 051403 (2007).
[Crossref] [PubMed]

2005 (3)

W. M. Pardridge, “The blood-brain barrier: bottleneck in brain drug development,” NeuroRx 2(1), 3–14 (2005).
[Crossref] [PubMed]

K. Hynynen, N. McDannold, N. A. Sheikov, F. A. Jolesz, and N. Vykhodtseva, “Local and reversible blood-brain barrier disruption by noninvasive focused ultrasound at frequencies suitable for trans-skull sonications,” Neuroimage 24(1), 12–20 (2005).
[Crossref] [PubMed]

J. Zhang and Z. Chen, “In vivo blood flow imaging by a swept laser source based Fourier domain optical Doppler tomography,” Opt. Express 13(19), 7449–7457 (2005).
[Crossref] [PubMed]

2001 (1)

K. Hynynen, N. McDannold, N. Vykhodtseva, and F. A. Jolesz, “Noninvasive MR imaging-guided focal opening of the blood-brain barrier in rabbits,” Radiology 220(3), 640–646 (2001).
[Crossref] [PubMed]

An, L.

Black, P.

N. McDannold, G. Clement, P. Black, F. Jolesz, and K. Hynynen, “Transcranial MRI-guided focused ultrasound surgery of brain tumors: Initial findings in three patients,” Neurosurgery 66(2), 323–332 (2010).
[Crossref] [PubMed]

Blatter, C.

R. A. Leitgeb, R. M. Werkmeister, C. Blatter, and L. Schmetterer, “Doppler optical coherence tomography,” Prog. Retin. Eye Res. 41, 26–43 (2014).
[Crossref] [PubMed]

Boppart, S. A.

A. M. Zysk, F. T. Nguyen, A. L. Oldenburg, D. L. Marks, and S. A. Boppart, “Optical coherence tomography: a review of clinical development from bench to bedside,” J. Biomed. Opt. 12(5), 051403 (2007).
[Crossref] [PubMed]

Burgess, A.

A. Burgess, T. Nhan, C. Moffatt, A. L. Klibanov, and K. Hynynen, “Analysis of focused ultrasound-induced blood-brain barrier permeability in a mouse model of Alzheimer’s disease using two-photon microscopy,” J. Control. Release 192, 243–248 (2014).
[Crossref] [PubMed]

T. Nhan, A. Burgess, E. E. Cho, B. Stefanovic, L. Lilge, and K. Hynynen, “Drug delivery to the brain by focused ultrasound induced blood-brain barrier disruption: Quantitative evaluation of enhanced permeability of cerebral vasculature using two-photon microscopy,” J. Control. Release 172(1), 274–280 (2013).
[Crossref] [PubMed]

Cable, A.

Chai, W. Y.

C. H. Fan, W. H. Lin, C. Y. Ting, W. Y. Chai, T. C. Yen, H. L. Liu, and C. K. Yeh, “Contrast-Enhanced Ultrasound Imaging for the Detection of Focused Ultrasound-Induced Blood-Brain Barrier Opening,” Theranostics 4(10), 1014–1025 (2014).
[Crossref] [PubMed]

Chang, F. Y.

Chang, T. C.

M. T. Tsai, C. K. Lee, K. M. Lin, Y. X. Lin, T. H. Lin, T. C. Chang, J. D. Lee, and H. L. Liu, “Quantitative observation of focused-ultrasound-induced vascular leakage and deformation via fluorescein angiography and optical coherence tomography,” J. Biomed. Opt. 18(10), 101307 (2013).
[Crossref] [PubMed]

Chen, J. C.

H. L. Liu, Y. Y. Wai, W. S. Chen, J. C. Chen, P. H. Hsu, X. Y. Wu, W. C. Huang, T. C. Yen, and J. J. Wang, “Hemorrhage detection during focused-ultrasound induced blood-brain-barrier opening by using susceptibility-weighted magnetic resonance imaging,” Ultrasound Med. Biol. 34(4), 598–606 (2008).
[Crossref] [PubMed]

Chen, W. S.

H. L. Liu, Y. Y. Wai, W. S. Chen, J. C. Chen, P. H. Hsu, X. Y. Wu, W. C. Huang, T. C. Yen, and J. J. Wang, “Hemorrhage detection during focused-ultrasound induced blood-brain-barrier opening by using susceptibility-weighted magnetic resonance imaging,” Ultrasound Med. Biol. 34(4), 598–606 (2008).
[Crossref] [PubMed]

Chen, Y.

Chen, Z.

Cho, E. E.

T. Nhan, A. Burgess, E. E. Cho, B. Stefanovic, L. Lilge, and K. Hynynen, “Drug delivery to the brain by focused ultrasound induced blood-brain barrier disruption: Quantitative evaluation of enhanced permeability of cerebral vasculature using two-photon microscopy,” J. Control. Release 172(1), 274–280 (2013).
[Crossref] [PubMed]

Clement, G.

N. McDannold, G. Clement, P. Black, F. Jolesz, and K. Hynynen, “Transcranial MRI-guided focused ultrasound surgery of brain tumors: Initial findings in three patients,” Neurosurgery 66(2), 323–332 (2010).
[Crossref] [PubMed]

Enfield, J.

E. Jonathan, J. Enfield, and M. J. Leahy, “Correlation mapping method for generating microcirculation morphology from optical coherence tomography (OCT) intensity images,” J. Biophotonics 4(9), 583–587 (2011).
[PubMed]

J. Enfield, E. Jonathan, and M. Leahy, “In vivo imaging of the microcirculation of the volar forearm using correlation mapping optical coherence tomography (cmOCT),” Biomed. Opt. Express 2(5), 1184–1193 (2011).
[Crossref] [PubMed]

Fan, C. H.

C. H. Fan, W. H. Lin, C. Y. Ting, W. Y. Chai, T. C. Yen, H. L. Liu, and C. K. Yeh, “Contrast-Enhanced Ultrasound Imaging for the Detection of Focused Ultrasound-Induced Blood-Brain Barrier Opening,” Theranostics 4(10), 1014–1025 (2014).
[Crossref] [PubMed]

H. L. Liu, C. H. Fan, C. Y. Ting, and C. K. Yeh, “Combining microbubbles and ultrasound for drug delivery to brain tumors: current progress and overview,” Theranostics 4(4), 432–444 (2014).
[Crossref] [PubMed]

C. H. Fan, H. L. Liu, C. Y. Huang, Y. J. Ma, T. C. Yen, and C. K. Yeh, “Detection of intracerebral hemorrhage and transient blood-supply shortage in focused-ultrasound-induced blood-brain barrier disruption by ultrasound imaging,” Ultrasound Med. Biol. 38(8), 1372–1382 (2012).
[Crossref] [PubMed]

Gong, C. S. A.

Hanes, J.

E. Nance, K. Timbie, G. W. Miller, J. Song, C. Louttit, A. L. Klibanov, T. Y. Shih, G. Swaminathan, R. J. Tamargo, G. F. Woodworth, J. Hanes, and R. J. Price, “Non-invasive delivery of stealth, brain-penetrating nanoparticles across the blood-brain barrier using MRI-guided focused ultrasound,” J. Control. Release 189, 123–132 (2014).
[Crossref] [PubMed]

Hsu, P. H.

H. L. Liu, Y. Y. Wai, W. S. Chen, J. C. Chen, P. H. Hsu, X. Y. Wu, W. C. Huang, T. C. Yen, and J. J. Wang, “Hemorrhage detection during focused-ultrasound induced blood-brain-barrier opening by using susceptibility-weighted magnetic resonance imaging,” Ultrasound Med. Biol. 34(4), 598–606 (2008).
[Crossref] [PubMed]

Huang, B. H.

Huang, C. Y.

C. H. Fan, H. L. Liu, C. Y. Huang, Y. J. Ma, T. C. Yen, and C. K. Yeh, “Detection of intracerebral hemorrhage and transient blood-supply shortage in focused-ultrasound-induced blood-brain barrier disruption by ultrasound imaging,” Ultrasound Med. Biol. 38(8), 1372–1382 (2012).
[Crossref] [PubMed]

Huang, W. C.

H. L. Liu, Y. Y. Wai, W. S. Chen, J. C. Chen, P. H. Hsu, X. Y. Wu, W. C. Huang, T. C. Yen, and J. J. Wang, “Hemorrhage detection during focused-ultrasound induced blood-brain-barrier opening by using susceptibility-weighted magnetic resonance imaging,” Ultrasound Med. Biol. 34(4), 598–606 (2008).
[Crossref] [PubMed]

Hynynen, K.

A. Burgess, T. Nhan, C. Moffatt, A. L. Klibanov, and K. Hynynen, “Analysis of focused ultrasound-induced blood-brain barrier permeability in a mouse model of Alzheimer’s disease using two-photon microscopy,” J. Control. Release 192, 243–248 (2014).
[Crossref] [PubMed]

T. Nhan, A. Burgess, E. E. Cho, B. Stefanovic, L. Lilge, and K. Hynynen, “Drug delivery to the brain by focused ultrasound induced blood-brain barrier disruption: Quantitative evaluation of enhanced permeability of cerebral vasculature using two-photon microscopy,” J. Control. Release 172(1), 274–280 (2013).
[Crossref] [PubMed]

N. McDannold, G. Clement, P. Black, F. Jolesz, and K. Hynynen, “Transcranial MRI-guided focused ultrasound surgery of brain tumors: Initial findings in three patients,” Neurosurgery 66(2), 323–332 (2010).
[Crossref] [PubMed]

K. Hynynen, N. McDannold, N. A. Sheikov, F. A. Jolesz, and N. Vykhodtseva, “Local and reversible blood-brain barrier disruption by noninvasive focused ultrasound at frequencies suitable for trans-skull sonications,” Neuroimage 24(1), 12–20 (2005).
[Crossref] [PubMed]

K. Hynynen, N. McDannold, N. Vykhodtseva, and F. A. Jolesz, “Noninvasive MR imaging-guided focal opening of the blood-brain barrier in rabbits,” Radiology 220(3), 640–646 (2001).
[Crossref] [PubMed]

Jarvi, M.

Jiang, J.

Jolesz, F.

N. McDannold, G. Clement, P. Black, F. Jolesz, and K. Hynynen, “Transcranial MRI-guided focused ultrasound surgery of brain tumors: Initial findings in three patients,” Neurosurgery 66(2), 323–332 (2010).
[Crossref] [PubMed]

Jolesz, F. A.

K. Hynynen, N. McDannold, N. A. Sheikov, F. A. Jolesz, and N. Vykhodtseva, “Local and reversible blood-brain barrier disruption by noninvasive focused ultrasound at frequencies suitable for trans-skull sonications,” Neuroimage 24(1), 12–20 (2005).
[Crossref] [PubMed]

K. Hynynen, N. McDannold, N. Vykhodtseva, and F. A. Jolesz, “Noninvasive MR imaging-guided focal opening of the blood-brain barrier in rabbits,” Radiology 220(3), 640–646 (2001).
[Crossref] [PubMed]

Jonathan, E.

E. Jonathan, J. Enfield, and M. J. Leahy, “Correlation mapping method for generating microcirculation morphology from optical coherence tomography (OCT) intensity images,” J. Biophotonics 4(9), 583–587 (2011).
[PubMed]

J. Enfield, E. Jonathan, and M. Leahy, “In vivo imaging of the microcirculation of the volar forearm using correlation mapping optical coherence tomography (cmOCT),” Biomed. Opt. Express 2(5), 1184–1193 (2011).
[Crossref] [PubMed]

Khurana, M.

Klibanov, A. L.

E. Nance, K. Timbie, G. W. Miller, J. Song, C. Louttit, A. L. Klibanov, T. Y. Shih, G. Swaminathan, R. J. Tamargo, G. F. Woodworth, J. Hanes, and R. J. Price, “Non-invasive delivery of stealth, brain-penetrating nanoparticles across the blood-brain barrier using MRI-guided focused ultrasound,” J. Control. Release 189, 123–132 (2014).
[Crossref] [PubMed]

A. Burgess, T. Nhan, C. Moffatt, A. L. Klibanov, and K. Hynynen, “Analysis of focused ultrasound-induced blood-brain barrier permeability in a mouse model of Alzheimer’s disease using two-photon microscopy,” J. Control. Release 192, 243–248 (2014).
[Crossref] [PubMed]

Leahy, M.

Leahy, M. J.

E. Jonathan, J. Enfield, and M. J. Leahy, “Correlation mapping method for generating microcirculation morphology from optical coherence tomography (OCT) intensity images,” J. Biophotonics 4(9), 583–587 (2011).
[PubMed]

Lee, C. K.

M. T. Tsai, F. Y. Chang, C. K. Lee, C. S. A. Gong, Y. X. Lin, J. D. Lee, C. H. Yang, and H. L. Liu, “Investigation of temporal vascular effects induced by focused ultrasound treatment with speckle-variance optical coherence tomography,” Biomed. Opt. Express 5(7), 2009–2022 (2014).
[Crossref] [PubMed]

M. T. Tsai, C. K. Lee, K. M. Lin, Y. X. Lin, T. H. Lin, T. C. Chang, J. D. Lee, and H. L. Liu, “Quantitative observation of focused-ultrasound-induced vascular leakage and deformation via fluorescein angiography and optical coherence tomography,” J. Biomed. Opt. 18(10), 101307 (2013).
[Crossref] [PubMed]

Lee, C. Y.

Lee, J. D.

M. T. Tsai, F. Y. Chang, C. K. Lee, C. S. A. Gong, Y. X. Lin, J. D. Lee, C. H. Yang, and H. L. Liu, “Investigation of temporal vascular effects induced by focused ultrasound treatment with speckle-variance optical coherence tomography,” Biomed. Opt. Express 5(7), 2009–2022 (2014).
[Crossref] [PubMed]

M. T. Tsai, C. K. Lee, K. M. Lin, Y. X. Lin, T. H. Lin, T. C. Chang, J. D. Lee, and H. L. Liu, “Quantitative observation of focused-ultrasound-induced vascular leakage and deformation via fluorescein angiography and optical coherence tomography,” J. Biomed. Opt. 18(10), 101307 (2013).
[Crossref] [PubMed]

Lee, K.

Lee, Y. J.

Leitgeb, R. A.

R. A. Leitgeb, R. M. Werkmeister, C. Blatter, and L. Schmetterer, “Doppler optical coherence tomography,” Prog. Retin. Eye Res. 41, 26–43 (2014).
[Crossref] [PubMed]

Leung, M. K.

Lilge, L.

T. Nhan, A. Burgess, E. E. Cho, B. Stefanovic, L. Lilge, and K. Hynynen, “Drug delivery to the brain by focused ultrasound induced blood-brain barrier disruption: Quantitative evaluation of enhanced permeability of cerebral vasculature using two-photon microscopy,” J. Control. Release 172(1), 274–280 (2013).
[Crossref] [PubMed]

Lin, K. M.

M. T. Tsai, C. K. Lee, K. M. Lin, Y. X. Lin, T. H. Lin, T. C. Chang, J. D. Lee, and H. L. Liu, “Quantitative observation of focused-ultrasound-induced vascular leakage and deformation via fluorescein angiography and optical coherence tomography,” J. Biomed. Opt. 18(10), 101307 (2013).
[Crossref] [PubMed]

Lin, T. H.

M. T. Tsai, C. K. Lee, K. M. Lin, Y. X. Lin, T. H. Lin, T. C. Chang, J. D. Lee, and H. L. Liu, “Quantitative observation of focused-ultrasound-induced vascular leakage and deformation via fluorescein angiography and optical coherence tomography,” J. Biomed. Opt. 18(10), 101307 (2013).
[Crossref] [PubMed]

Lin, W. H.

C. H. Fan, W. H. Lin, C. Y. Ting, W. Y. Chai, T. C. Yen, H. L. Liu, and C. K. Yeh, “Contrast-Enhanced Ultrasound Imaging for the Detection of Focused Ultrasound-Induced Blood-Brain Barrier Opening,” Theranostics 4(10), 1014–1025 (2014).
[Crossref] [PubMed]

Lin, Y. X.

M. T. Tsai, F. Y. Chang, C. K. Lee, C. S. A. Gong, Y. X. Lin, J. D. Lee, C. H. Yang, and H. L. Liu, “Investigation of temporal vascular effects induced by focused ultrasound treatment with speckle-variance optical coherence tomography,” Biomed. Opt. Express 5(7), 2009–2022 (2014).
[Crossref] [PubMed]

M. T. Tsai, C. K. Lee, K. M. Lin, Y. X. Lin, T. H. Lin, T. C. Chang, J. D. Lee, and H. L. Liu, “Quantitative observation of focused-ultrasound-induced vascular leakage and deformation via fluorescein angiography and optical coherence tomography,” J. Biomed. Opt. 18(10), 101307 (2013).
[Crossref] [PubMed]

Liu, H. L.

C. H. Fan, W. H. Lin, C. Y. Ting, W. Y. Chai, T. C. Yen, H. L. Liu, and C. K. Yeh, “Contrast-Enhanced Ultrasound Imaging for the Detection of Focused Ultrasound-Induced Blood-Brain Barrier Opening,” Theranostics 4(10), 1014–1025 (2014).
[Crossref] [PubMed]

H. L. Liu, C. H. Fan, C. Y. Ting, and C. K. Yeh, “Combining microbubbles and ultrasound for drug delivery to brain tumors: current progress and overview,” Theranostics 4(4), 432–444 (2014).
[Crossref] [PubMed]

M. T. Tsai, F. Y. Chang, C. K. Lee, C. S. A. Gong, Y. X. Lin, J. D. Lee, C. H. Yang, and H. L. Liu, “Investigation of temporal vascular effects induced by focused ultrasound treatment with speckle-variance optical coherence tomography,” Biomed. Opt. Express 5(7), 2009–2022 (2014).
[Crossref] [PubMed]

M. T. Tsai, C. K. Lee, K. M. Lin, Y. X. Lin, T. H. Lin, T. C. Chang, J. D. Lee, and H. L. Liu, “Quantitative observation of focused-ultrasound-induced vascular leakage and deformation via fluorescein angiography and optical coherence tomography,” J. Biomed. Opt. 18(10), 101307 (2013).
[Crossref] [PubMed]

C. H. Fan, H. L. Liu, C. Y. Huang, Y. J. Ma, T. C. Yen, and C. K. Yeh, “Detection of intracerebral hemorrhage and transient blood-supply shortage in focused-ultrasound-induced blood-brain barrier disruption by ultrasound imaging,” Ultrasound Med. Biol. 38(8), 1372–1382 (2012).
[Crossref] [PubMed]

H. L. Liu, Y. Y. Wai, W. S. Chen, J. C. Chen, P. H. Hsu, X. Y. Wu, W. C. Huang, T. C. Yen, and J. J. Wang, “Hemorrhage detection during focused-ultrasound induced blood-brain-barrier opening by using susceptibility-weighted magnetic resonance imaging,” Ultrasound Med. Biol. 34(4), 598–606 (2008).
[Crossref] [PubMed]

Louttit, C.

E. Nance, K. Timbie, G. W. Miller, J. Song, C. Louttit, A. L. Klibanov, T. Y. Shih, G. Swaminathan, R. J. Tamargo, G. F. Woodworth, J. Hanes, and R. J. Price, “Non-invasive delivery of stealth, brain-penetrating nanoparticles across the blood-brain barrier using MRI-guided focused ultrasound,” J. Control. Release 189, 123–132 (2014).
[Crossref] [PubMed]

Ma, Y. J.

C. H. Fan, H. L. Liu, C. Y. Huang, Y. J. Ma, T. C. Yen, and C. K. Yeh, “Detection of intracerebral hemorrhage and transient blood-supply shortage in focused-ultrasound-induced blood-brain barrier disruption by ultrasound imaging,” Ultrasound Med. Biol. 38(8), 1372–1382 (2012).
[Crossref] [PubMed]

Mariampillai, A.

Marks, D. L.

A. M. Zysk, F. T. Nguyen, A. L. Oldenburg, D. L. Marks, and S. A. Boppart, “Optical coherence tomography: a review of clinical development from bench to bedside,” J. Biomed. Opt. 12(5), 051403 (2007).
[Crossref] [PubMed]

McDannold, N.

N. McDannold, G. Clement, P. Black, F. Jolesz, and K. Hynynen, “Transcranial MRI-guided focused ultrasound surgery of brain tumors: Initial findings in three patients,” Neurosurgery 66(2), 323–332 (2010).
[Crossref] [PubMed]

K. Hynynen, N. McDannold, N. A. Sheikov, F. A. Jolesz, and N. Vykhodtseva, “Local and reversible blood-brain barrier disruption by noninvasive focused ultrasound at frequencies suitable for trans-skull sonications,” Neuroimage 24(1), 12–20 (2005).
[Crossref] [PubMed]

K. Hynynen, N. McDannold, N. Vykhodtseva, and F. A. Jolesz, “Noninvasive MR imaging-guided focal opening of the blood-brain barrier in rabbits,” Radiology 220(3), 640–646 (2001).
[Crossref] [PubMed]

Miller, G. W.

E. Nance, K. Timbie, G. W. Miller, J. Song, C. Louttit, A. L. Klibanov, T. Y. Shih, G. Swaminathan, R. J. Tamargo, G. F. Woodworth, J. Hanes, and R. J. Price, “Non-invasive delivery of stealth, brain-penetrating nanoparticles across the blood-brain barrier using MRI-guided focused ultrasound,” J. Control. Release 189, 123–132 (2014).
[Crossref] [PubMed]

Moffatt, C.

A. Burgess, T. Nhan, C. Moffatt, A. L. Klibanov, and K. Hynynen, “Analysis of focused ultrasound-induced blood-brain barrier permeability in a mouse model of Alzheimer’s disease using two-photon microscopy,” J. Control. Release 192, 243–248 (2014).
[Crossref] [PubMed]

Moriyama, E. H.

Munce, N. R.

Nance, E.

E. Nance, K. Timbie, G. W. Miller, J. Song, C. Louttit, A. L. Klibanov, T. Y. Shih, G. Swaminathan, R. J. Tamargo, G. F. Woodworth, J. Hanes, and R. J. Price, “Non-invasive delivery of stealth, brain-penetrating nanoparticles across the blood-brain barrier using MRI-guided focused ultrasound,” J. Control. Release 189, 123–132 (2014).
[Crossref] [PubMed]

Nguyen, F. T.

A. M. Zysk, F. T. Nguyen, A. L. Oldenburg, D. L. Marks, and S. A. Boppart, “Optical coherence tomography: a review of clinical development from bench to bedside,” J. Biomed. Opt. 12(5), 051403 (2007).
[Crossref] [PubMed]

Nhan, T.

A. Burgess, T. Nhan, C. Moffatt, A. L. Klibanov, and K. Hynynen, “Analysis of focused ultrasound-induced blood-brain barrier permeability in a mouse model of Alzheimer’s disease using two-photon microscopy,” J. Control. Release 192, 243–248 (2014).
[Crossref] [PubMed]

T. Nhan, A. Burgess, E. E. Cho, B. Stefanovic, L. Lilge, and K. Hynynen, “Drug delivery to the brain by focused ultrasound induced blood-brain barrier disruption: Quantitative evaluation of enhanced permeability of cerebral vasculature using two-photon microscopy,” J. Control. Release 172(1), 274–280 (2013).
[Crossref] [PubMed]

Oldenburg, A. L.

A. M. Zysk, F. T. Nguyen, A. L. Oldenburg, D. L. Marks, and S. A. Boppart, “Optical coherence tomography: a review of clinical development from bench to bedside,” J. Biomed. Opt. 12(5), 051403 (2007).
[Crossref] [PubMed]

Pardridge, W. M.

W. M. Pardridge, “The blood-brain barrier: bottleneck in brain drug development,” NeuroRx 2(1), 3–14 (2005).
[Crossref] [PubMed]

Price, R. J.

E. Nance, K. Timbie, G. W. Miller, J. Song, C. Louttit, A. L. Klibanov, T. Y. Shih, G. Swaminathan, R. J. Tamargo, G. F. Woodworth, J. Hanes, and R. J. Price, “Non-invasive delivery of stealth, brain-penetrating nanoparticles across the blood-brain barrier using MRI-guided focused ultrasound,” J. Control. Release 189, 123–132 (2014).
[Crossref] [PubMed]

Schmetterer, L.

R. A. Leitgeb, R. M. Werkmeister, C. Blatter, and L. Schmetterer, “Doppler optical coherence tomography,” Prog. Retin. Eye Res. 41, 26–43 (2014).
[Crossref] [PubMed]

Sheikov, N. A.

K. Hynynen, N. McDannold, N. A. Sheikov, F. A. Jolesz, and N. Vykhodtseva, “Local and reversible blood-brain barrier disruption by noninvasive focused ultrasound at frequencies suitable for trans-skull sonications,” Neuroimage 24(1), 12–20 (2005).
[Crossref] [PubMed]

Shih, T. Y.

E. Nance, K. Timbie, G. W. Miller, J. Song, C. Louttit, A. L. Klibanov, T. Y. Shih, G. Swaminathan, R. J. Tamargo, G. F. Woodworth, J. Hanes, and R. J. Price, “Non-invasive delivery of stealth, brain-penetrating nanoparticles across the blood-brain barrier using MRI-guided focused ultrasound,” J. Control. Release 189, 123–132 (2014).
[Crossref] [PubMed]

Song, J.

E. Nance, K. Timbie, G. W. Miller, J. Song, C. Louttit, A. L. Klibanov, T. Y. Shih, G. Swaminathan, R. J. Tamargo, G. F. Woodworth, J. Hanes, and R. J. Price, “Non-invasive delivery of stealth, brain-penetrating nanoparticles across the blood-brain barrier using MRI-guided focused ultrasound,” J. Control. Release 189, 123–132 (2014).
[Crossref] [PubMed]

Standish, B. A.

Stefanovic, B.

T. Nhan, A. Burgess, E. E. Cho, B. Stefanovic, L. Lilge, and K. Hynynen, “Drug delivery to the brain by focused ultrasound induced blood-brain barrier disruption: Quantitative evaluation of enhanced permeability of cerebral vasculature using two-photon microscopy,” J. Control. Release 172(1), 274–280 (2013).
[Crossref] [PubMed]

Swaminathan, G.

E. Nance, K. Timbie, G. W. Miller, J. Song, C. Louttit, A. L. Klibanov, T. Y. Shih, G. Swaminathan, R. J. Tamargo, G. F. Woodworth, J. Hanes, and R. J. Price, “Non-invasive delivery of stealth, brain-penetrating nanoparticles across the blood-brain barrier using MRI-guided focused ultrasound,” J. Control. Release 189, 123–132 (2014).
[Crossref] [PubMed]

Tamargo, R. J.

E. Nance, K. Timbie, G. W. Miller, J. Song, C. Louttit, A. L. Klibanov, T. Y. Shih, G. Swaminathan, R. J. Tamargo, G. F. Woodworth, J. Hanes, and R. J. Price, “Non-invasive delivery of stealth, brain-penetrating nanoparticles across the blood-brain barrier using MRI-guided focused ultrasound,” J. Control. Release 189, 123–132 (2014).
[Crossref] [PubMed]

Timbie, K.

E. Nance, K. Timbie, G. W. Miller, J. Song, C. Louttit, A. L. Klibanov, T. Y. Shih, G. Swaminathan, R. J. Tamargo, G. F. Woodworth, J. Hanes, and R. J. Price, “Non-invasive delivery of stealth, brain-penetrating nanoparticles across the blood-brain barrier using MRI-guided focused ultrasound,” J. Control. Release 189, 123–132 (2014).
[Crossref] [PubMed]

Ting, C. Y.

H. L. Liu, C. H. Fan, C. Y. Ting, and C. K. Yeh, “Combining microbubbles and ultrasound for drug delivery to brain tumors: current progress and overview,” Theranostics 4(4), 432–444 (2014).
[Crossref] [PubMed]

C. H. Fan, W. H. Lin, C. Y. Ting, W. Y. Chai, T. C. Yen, H. L. Liu, and C. K. Yeh, “Contrast-Enhanced Ultrasound Imaging for the Detection of Focused Ultrasound-Induced Blood-Brain Barrier Opening,” Theranostics 4(10), 1014–1025 (2014).
[Crossref] [PubMed]

Trung, N. H.

Tsai, M. T.

Vitkin, A.

Vitkin, I. A.

Vykhodtseva, N.

K. Hynynen, N. McDannold, N. A. Sheikov, F. A. Jolesz, and N. Vykhodtseva, “Local and reversible blood-brain barrier disruption by noninvasive focused ultrasound at frequencies suitable for trans-skull sonications,” Neuroimage 24(1), 12–20 (2005).
[Crossref] [PubMed]

K. Hynynen, N. McDannold, N. Vykhodtseva, and F. A. Jolesz, “Noninvasive MR imaging-guided focal opening of the blood-brain barrier in rabbits,” Radiology 220(3), 640–646 (2001).
[Crossref] [PubMed]

Wai, Y. Y.

H. L. Liu, Y. Y. Wai, W. S. Chen, J. C. Chen, P. H. Hsu, X. Y. Wu, W. C. Huang, T. C. Yen, and J. J. Wang, “Hemorrhage detection during focused-ultrasound induced blood-brain-barrier opening by using susceptibility-weighted magnetic resonance imaging,” Ultrasound Med. Biol. 34(4), 598–606 (2008).
[Crossref] [PubMed]

Wang, J. J.

H. L. Liu, Y. Y. Wai, W. S. Chen, J. C. Chen, P. H. Hsu, X. Y. Wu, W. C. Huang, T. C. Yen, and J. J. Wang, “Hemorrhage detection during focused-ultrasound induced blood-brain-barrier opening by using susceptibility-weighted magnetic resonance imaging,” Ultrasound Med. Biol. 34(4), 598–606 (2008).
[Crossref] [PubMed]

Wang, R. K.

Wang, Y. L.

Werkmeister, R. M.

R. A. Leitgeb, R. M. Werkmeister, C. Blatter, and L. Schmetterer, “Doppler optical coherence tomography,” Prog. Retin. Eye Res. 41, 26–43 (2014).
[Crossref] [PubMed]

Wilson, B. C.

Woodworth, G. F.

E. Nance, K. Timbie, G. W. Miller, J. Song, C. Louttit, A. L. Klibanov, T. Y. Shih, G. Swaminathan, R. J. Tamargo, G. F. Woodworth, J. Hanes, and R. J. Price, “Non-invasive delivery of stealth, brain-penetrating nanoparticles across the blood-brain barrier using MRI-guided focused ultrasound,” J. Control. Release 189, 123–132 (2014).
[Crossref] [PubMed]

Wu, X. Y.

H. L. Liu, Y. Y. Wai, W. S. Chen, J. C. Chen, P. H. Hsu, X. Y. Wu, W. C. Huang, T. C. Yen, and J. J. Wang, “Hemorrhage detection during focused-ultrasound induced blood-brain-barrier opening by using susceptibility-weighted magnetic resonance imaging,” Ultrasound Med. Biol. 34(4), 598–606 (2008).
[Crossref] [PubMed]

Yang, C. H.

Yang, V. X.

Yeh, C. K.

C. H. Fan, W. H. Lin, C. Y. Ting, W. Y. Chai, T. C. Yen, H. L. Liu, and C. K. Yeh, “Contrast-Enhanced Ultrasound Imaging for the Detection of Focused Ultrasound-Induced Blood-Brain Barrier Opening,” Theranostics 4(10), 1014–1025 (2014).
[Crossref] [PubMed]

H. L. Liu, C. H. Fan, C. Y. Ting, and C. K. Yeh, “Combining microbubbles and ultrasound for drug delivery to brain tumors: current progress and overview,” Theranostics 4(4), 432–444 (2014).
[Crossref] [PubMed]

C. H. Fan, H. L. Liu, C. Y. Huang, Y. J. Ma, T. C. Yen, and C. K. Yeh, “Detection of intracerebral hemorrhage and transient blood-supply shortage in focused-ultrasound-induced blood-brain barrier disruption by ultrasound imaging,” Ultrasound Med. Biol. 38(8), 1372–1382 (2012).
[Crossref] [PubMed]

Yen, T. C.

C. H. Fan, W. H. Lin, C. Y. Ting, W. Y. Chai, T. C. Yen, H. L. Liu, and C. K. Yeh, “Contrast-Enhanced Ultrasound Imaging for the Detection of Focused Ultrasound-Induced Blood-Brain Barrier Opening,” Theranostics 4(10), 1014–1025 (2014).
[Crossref] [PubMed]

C. H. Fan, H. L. Liu, C. Y. Huang, Y. J. Ma, T. C. Yen, and C. K. Yeh, “Detection of intracerebral hemorrhage and transient blood-supply shortage in focused-ultrasound-induced blood-brain barrier disruption by ultrasound imaging,” Ultrasound Med. Biol. 38(8), 1372–1382 (2012).
[Crossref] [PubMed]

H. L. Liu, Y. Y. Wai, W. S. Chen, J. C. Chen, P. H. Hsu, X. Y. Wu, W. C. Huang, T. C. Yen, and J. J. Wang, “Hemorrhage detection during focused-ultrasound induced blood-brain-barrier opening by using susceptibility-weighted magnetic resonance imaging,” Ultrasound Med. Biol. 34(4), 598–606 (2008).
[Crossref] [PubMed]

Zhang, J.

Zysk, A. M.

A. M. Zysk, F. T. Nguyen, A. L. Oldenburg, D. L. Marks, and S. A. Boppart, “Optical coherence tomography: a review of clinical development from bench to bedside,” J. Biomed. Opt. 12(5), 051403 (2007).
[Crossref] [PubMed]

Biomed. Opt. Express (3)

J. Biomed. Opt. (2)

M. T. Tsai, C. K. Lee, K. M. Lin, Y. X. Lin, T. H. Lin, T. C. Chang, J. D. Lee, and H. L. Liu, “Quantitative observation of focused-ultrasound-induced vascular leakage and deformation via fluorescein angiography and optical coherence tomography,” J. Biomed. Opt. 18(10), 101307 (2013).
[Crossref] [PubMed]

A. M. Zysk, F. T. Nguyen, A. L. Oldenburg, D. L. Marks, and S. A. Boppart, “Optical coherence tomography: a review of clinical development from bench to bedside,” J. Biomed. Opt. 12(5), 051403 (2007).
[Crossref] [PubMed]

J. Biophotonics (1)

E. Jonathan, J. Enfield, and M. J. Leahy, “Correlation mapping method for generating microcirculation morphology from optical coherence tomography (OCT) intensity images,” J. Biophotonics 4(9), 583–587 (2011).
[PubMed]

J. Control. Release (3)

E. Nance, K. Timbie, G. W. Miller, J. Song, C. Louttit, A. L. Klibanov, T. Y. Shih, G. Swaminathan, R. J. Tamargo, G. F. Woodworth, J. Hanes, and R. J. Price, “Non-invasive delivery of stealth, brain-penetrating nanoparticles across the blood-brain barrier using MRI-guided focused ultrasound,” J. Control. Release 189, 123–132 (2014).
[Crossref] [PubMed]

T. Nhan, A. Burgess, E. E. Cho, B. Stefanovic, L. Lilge, and K. Hynynen, “Drug delivery to the brain by focused ultrasound induced blood-brain barrier disruption: Quantitative evaluation of enhanced permeability of cerebral vasculature using two-photon microscopy,” J. Control. Release 172(1), 274–280 (2013).
[Crossref] [PubMed]

A. Burgess, T. Nhan, C. Moffatt, A. L. Klibanov, and K. Hynynen, “Analysis of focused ultrasound-induced blood-brain barrier permeability in a mouse model of Alzheimer’s disease using two-photon microscopy,” J. Control. Release 192, 243–248 (2014).
[Crossref] [PubMed]

Neuroimage (1)

K. Hynynen, N. McDannold, N. A. Sheikov, F. A. Jolesz, and N. Vykhodtseva, “Local and reversible blood-brain barrier disruption by noninvasive focused ultrasound at frequencies suitable for trans-skull sonications,” Neuroimage 24(1), 12–20 (2005).
[Crossref] [PubMed]

NeuroRx (1)

W. M. Pardridge, “The blood-brain barrier: bottleneck in brain drug development,” NeuroRx 2(1), 3–14 (2005).
[Crossref] [PubMed]

Neurosurgery (1)

N. McDannold, G. Clement, P. Black, F. Jolesz, and K. Hynynen, “Transcranial MRI-guided focused ultrasound surgery of brain tumors: Initial findings in three patients,” Neurosurgery 66(2), 323–332 (2010).
[Crossref] [PubMed]

Opt. Express (2)

Opt. Lett. (3)

Prog. Retin. Eye Res. (1)

R. A. Leitgeb, R. M. Werkmeister, C. Blatter, and L. Schmetterer, “Doppler optical coherence tomography,” Prog. Retin. Eye Res. 41, 26–43 (2014).
[Crossref] [PubMed]

Radiology (1)

K. Hynynen, N. McDannold, N. Vykhodtseva, and F. A. Jolesz, “Noninvasive MR imaging-guided focal opening of the blood-brain barrier in rabbits,” Radiology 220(3), 640–646 (2001).
[Crossref] [PubMed]

Theranostics (2)

H. L. Liu, C. H. Fan, C. Y. Ting, and C. K. Yeh, “Combining microbubbles and ultrasound for drug delivery to brain tumors: current progress and overview,” Theranostics 4(4), 432–444 (2014).
[Crossref] [PubMed]

C. H. Fan, W. H. Lin, C. Y. Ting, W. Y. Chai, T. C. Yen, H. L. Liu, and C. K. Yeh, “Contrast-Enhanced Ultrasound Imaging for the Detection of Focused Ultrasound-Induced Blood-Brain Barrier Opening,” Theranostics 4(10), 1014–1025 (2014).
[Crossref] [PubMed]

Ultrasound Med. Biol. (2)

H. L. Liu, Y. Y. Wai, W. S. Chen, J. C. Chen, P. H. Hsu, X. Y. Wu, W. C. Huang, T. C. Yen, and J. J. Wang, “Hemorrhage detection during focused-ultrasound induced blood-brain-barrier opening by using susceptibility-weighted magnetic resonance imaging,” Ultrasound Med. Biol. 34(4), 598–606 (2008).
[Crossref] [PubMed]

C. H. Fan, H. L. Liu, C. Y. Huang, Y. J. Ma, T. C. Yen, and C. K. Yeh, “Detection of intracerebral hemorrhage and transient blood-supply shortage in focused-ultrasound-induced blood-brain barrier disruption by ultrasound imaging,” Ultrasound Med. Biol. 38(8), 1372–1382 (2012).
[Crossref] [PubMed]

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Figures (7)

Fig. 1
Fig. 1 Schematic diagrams of (a) the FUS system and (b) the SS-OCT setup. FC: fiber coupler; DC: dispersion compensator; M: mirror; GV: two-axis galvanometer; SL: scanning lens; BD: balanced detector.
Fig. 2
Fig. 2 2D OCT images of mouse brains obtained before (a)-(d) and at 30 minutes after the exposure to different FUS power levels of (e) 1 W, (f) 2 W (g) 2.5 W, and (h) 5 W, respectively. DM: dura mater, AM: arachnoid mater, SDS: subdural space, SAS: subarachnoid space, PM: pia mater, BV: blood vessel, and C: cortex. Yellow arrows represent the AM location before the exposure; red arrows represent the AM location after the exposure. The scalar bar in (h) represents 1 mm.
Fig. 3
Fig. 3 (a)-(d) 2D OCT images of the same brain region as in Fig. 2(d) obtained at 60, 90, 120, and 150 minutes after FUS exposure. (e) The scattering intensity profiles along the transverse direction at the locations indicated by the yellow-dash lines in Figs. 2(d), 2(h), and 3(a)-3(d). BV: blood vessel. The scalar bar represents 1 mm.
Fig. 4
Fig. 4 Corresponding MIP OCT angiographies of Fig. 2. (a)-(d) OCT angiographies obtained before FUS exposure. (e)-(h) OCT angiographies obtained at 30 minutes after FUS exposure at different power levels of 1, 2, 2.5, and 5 W, respectively. (i), (k) Photos of the entire brain of (g) and (h) by using Evans blue as the contrast agent (power is 2.5 W and 5W, respectively). (j), (l) Stained brain slices (power is 2.5W and 5W, respectively). White line in (i) and (k) indicate the corresponding locations of (j) and (l). The scalar bar in (h) represents 500 μm.
Fig. 5
Fig. 5 Time series of (a) R and (b) RVD values obtained without FUS exposure (0-W case) and after FUS exposure with different FUS power of 1, 2, and 2.5 W. The regions for the RVD estimation for each power level are marked by the white lines in Figs. 4(a)-4(c).
Fig. 6
Fig. 6 (a)-(g) MIP angiographies of the mouse brain (the same brain measured in Fig. 4(a)) obtained at 210, 240, 270, 300, 330, 360, and 390 minutes after 1-W FUS exposure. (h)-(n) MIP angiographies of the mouse brain (the same brain measured in Fig. 4(b)) obtained at 210, 240, 270, 300, 330, 360, and 390 minutes after 2-W FUS exposure.
Fig. 7
Fig. 7 Time series of (a) R and (b) RVD values measured after FUS exposure with different FUS power of 1 and 2 W. The regions for the RVD estimation were marked by the dash lines in Figs. 6(a) and 6(h).

Equations (3)

Equations on this page are rendered with MathJax. Learn more.

S V i j k = 1 N k = 1 N ( I i j k 1 N k = 1 N I i j k ) 2
R = D FUS D i
R V D = A FUS A i

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