Abstract

Photodynamic treatment (PDT) causes a significant increase in the permeability of the blood-brain barrier (BBB) in healthy mice. Using different doses of laser radiation (635 nm, 10-40 J/cm2) and photosensitizer (5-aminolevulinic acid – 5-ALA, 20 and 80 mg/kg, i.v.), we found that the optimal PDT for the reversible opening of the BBB is 15 J/cm2 and 5-ALA, 20 mg/kg, exhibiting brain tissues recovery 3 days after PDT. Further increases in the laser radiation or 5-ALA doses have no amplifying effect on the BBB permeability, but are associated with severe damage of brain tissues. These results can be an informative platform for further studies of new strategies in brain drug delivery and for better understanding of mechanisms underlying cerebrovascular effects of PDT-related fluorescence guided resection of brain tumor.

© 2017 Optical Society of America

Full Article  |  PDF Article
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References

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    [PubMed]
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2017 (4)

V. Kiviniemi, V. Korhonen, J. Kortelainen, S. Rytky, T. Keinänen, T. Tuovinen, M. Isokangas, E. Sonkajärvi, T. Siniluoto, J. Nikkinen, S. Alahuhta, O. Tervonen, T. Turpeenniemi-Hujanen, T. Myllylä, O. Kuittinen, and J. Voipio, “Real-time monitoring of human blood-brain barrier disruption,” PLoS One 12(3), e0174072 (2017).
[PubMed]

W. Stummer, H. Stepp, O. D. Wiestler, and U. Pichlmeier, “Randomized, Prospective Double-Blinded Study Comparing 3 Different Doses of 5-Aminolevulinic Acid for Fluorescence-Guided Resections of Malignant Gliomas,” Neurosurgery 81(2), 230–239 (2017).
[PubMed]

O. Semyachkina-Glushkovskaya, “Laser speckle imaging and wavelet analysis of cerebral blood flow associated with the opening of the blood–brain barrier by sound,” Chin. Opt. Lett. 15, 090002 (2017).

O. V. Semyachkina-Glushkovskaya, “Laser-induced generation of singlet oxygen and its role in the cerebrovascular physiology,” Prog. Quantum Electron. 55, 112–128 (2017).

2016 (1)

P. C. Chu, W. Y. Chai, C. H. Tsai, S. T. Kang, C. K. Yeh, and H. L. Liu, “Focused Ultrasound-Induced Blood-Brain Barrier Opening: Association with Mechanical Index and Cavitation Index Analyzed by Dynamic Contrast-Enhanced Magnetic-Resonance Imaging,” Sci. Rep. 6, 33264 (2016).
[PubMed]

2015 (2)

S. J. Madsen, C. Christie, S. J. Hong, A. Trinidad, Q. Peng, F. A. Uzal, and H. Hirschberg, “Nanoparticle-loaded macrophage-mediated photothermal therapy: potential for glioma treatment,” Lasers Med. Sci. 30(4), 1357–1365 (2015).
[PubMed]

P. K. Pandey, A. K. Sharma, and U. Gupta, “Blood brain barrier: An overview on strategies in drug delivery, realistic in vitro modeling and in vivo live tracking,” Tissue Barriers 4(1), e1129476 (2015).
[PubMed]

2014 (2)

H. L. Wang and T. W. Lai, “Optimization of Evans blue quantitation in limited rat tissue samples,” Sci. Rep. 4, 6588 (2014).
[PubMed]

T. Kuroiwa, “Photodynamic diagnosis and photodynamic therapy for the brain tumors,” Progress in Neuro-Oncology. 21, 14–21 (2014).

2013 (3)

S. Mitragotri, “Devices for overcoming biological barriers: The use of physical forces to disrupt the barriers,” Adv. Drug Deliv. Rev. 65(1), 100–103 (2013).
[PubMed]

S. Wu, K. Li, Y. Yan, B. Gran, Y. Han, F. Zhou, Y. T. Guan, A. Rostami, and G. X. Zhang, “Intranasal Delivery of Neural Stem Cells: A CNS-specific, Non-invasive Cell-based Therapy for Experimental Autoimmune Encephalomyelitis,” J. Clin. Cell. Immunol. 4(3), 24244890 (2013).
[PubMed]

S. J. Madsen, H. M. Gach, S. J. Hong, F. A. Uzal, Q. Peng, and H. Hirschberg, “Increased nanoparticle-loaded exogenous macrophage migration into the brain following PDT-induced blood-brain barrier disruption,” Lasers Surg. Med. 45(8), 524–532 (2013).
[PubMed]

2012 (2)

K. B. Chen, E. Y. Kuo, K. S. Poon, K. S. Cheng, C. S. Chang, Y. C. Liu, and T. W. Lai, “Increase in Evans blue dye extravasation into the brain in the late developmental stage,” Neuroreport 23(12), 699–701 (2012).
[PubMed]

M. J. Colditz and R. L. Jeffree, “Aminolevulinic acid (ALA)-protoporphyrin IX fluorescence guided tumour resection. Part 1: Clinical, radiological and pathological studies,” J. Clin. Neurosci. 19(11), 1471–1474 (2012).
[PubMed]

2011 (2)

A. Hoffmann, J. Bredno, M. Wendland, N. Derugin, P. Ohara, and M. Wintermark, “High and low molecular weight fluorescein isothiocyanate (FITC)-dextran to assess blood-brain barrier disruption: technical consideration,” Transl. Stroke Res. 2(1), 106–111 (2011).
[PubMed]

P. Agostinis, K. Berg, K. A. Cengel, T. H. Foster, A. W. Girotti, S. O. Gollnick, S. M. Hahn, M. R. Hamblin, A. Juzeniene, D. Kessel, M. Korbelik, J. Moan, P. Mroz, D. Nowis, J. Piette, B. C. Wilson, and J. Golab, “Photodynamic Therapy of Cancer: An Update,” CA Cancer J. Clin. 61(4), 250–281 (2011).
[PubMed]

2010 (1)

S. J. Madsen and H. Hirschberg, “Site-specific opening of the blood-brain barrier,” J. Biophotonics 3(5-6), 356–367 (2010).
[PubMed]

2008 (1)

H. Hirschberg, F. A. Uzal, D. Chighvinadze, M. J. Zhang, Q. Peng, and S. J. Madsen, “Disruption of the Blood-Brain Barrier Following ALA-Mediated Photodynamic Therapy,” Lasers Surg. Med. 40(8), 535–542 (2008).
[PubMed]

2007 (2)

S. S. Hu, H. B. Cheng, Y. R. Zheng, R. Y. Zhang, W. Yue, and H. Zhang, “Effects of photodynamic therapy on the ultrastructure of glioma cells,” Biomed. Environ. Sci. 20(4), 269–273 (2007).
[PubMed]

W. M. Pardridge, “Blood-brain barrier delivery,” Drug Discov. Today 12(1-2), 54–61 (2007).
[PubMed]

2006 (2)

S. S. Stylli and A. H. Kaye, “Photodynamic therapy of cerebral glioma-A review Part I-A biological basis,” J. Clin. Neurosci. 13(6), 615–625 (2006).
[PubMed]

E. Angell-Petersen, S. Spetalen, S. J. Madsen, C. H. Sun, Q. Peng, S. W. Carper, M. Sioud, and H. Hirschberg, “Influence of light fluence rate on the effects of photodynamic therapy in an orthotopic rat glioma model,” J. Neurosurg. 104(1), 109–117 (2006).
[PubMed]

2003 (1)

S. Nag, “Blood-brain barrier permeability using tracers and immunohistochemistry,” Methods Mol. Med. 89, 133–144 (2003).
[PubMed]

2002 (1)

F. Yoshino, H. Shoji, and M. C. Lee, “Vascular effects of singlet oxygen (1O2) generated by photo-excitation on adrenergic neurotransmission in isolated rabbit mesenteric vein,” Redox Rep. 7(5), 266–270 (2002).
[PubMed]

2001 (1)

B. Krammer, “Vascular effects of photodynamic therapy,” Anticancer Res. 21(6B), 4271–4277 (2001).
[PubMed]

1999 (1)

A. K. Ghose, V. N. Viswanadhan, and J. J. Wendoloski, “A knowledge-based approach in designing combinatorial or medicinal chemistry libraries for drug discovery. 1. A qualitative and quantitative characterization of known drug databases,” J. Comb. Chem. 1(1), 55–68 (1999).
[PubMed]

1997 (1)

H. Mizukawa and E. Okabe, “Inhibition by singlet molecular oxygen of the vascular reactivity in rabbit mesenteric artery,” Br. J. Pharmacol. 121(1), 63–70 (1997).
[PubMed]

1996 (2)

W. I. Rosenblum and G. H. Nelson, “Singlet oxygen scavengers affect laser-dye impairment of endothelium-dependent responses of brain arterioles,” Am. J. Physiol. 270(4 Pt 2), H1258–H1263 (1996).
[PubMed]

V. H. Fingar, “Vascular effects of photodynamic therapy,” J. Clin. Laser Med. Surg. 14(5), 323–328 (1996).
[PubMed]

1992 (1)

L. A. Sporn and T. H. Foster, “Photofrin and light induces microtubule depolymerization in cultured human endothelial cells,” Cancer Res. 52(12), 3443–3448 (1992).
[PubMed]

1990 (1)

G. Vandeplassche, M. Bernier, F. Thoné, M. Borgers, Y. Kusama, and D. J. Hearse, “Singlet oxygen and myocardial injury: ultrastructural, cytochemical and electrocardiographic consequences of photoactivation of rose bengal,” J. Mol. Cell. Cardiol. 22(3), 287–301 (1990).
[PubMed]

1989 (1)

Y. Kusama, M. Bernier, and D. J. Hearse, “Singlet oxygen-induced arrhythmias. dose- and light-response studies for photoactivation of rose bengal in the rat heart,” Circulation 80(5), 1432–1448 (1989).
[PubMed]

1983 (1)

A. Saria and J. M. Lundberg, “Evans blue fluorescence: quantitative and morphological evaluation of vascular permeability in animal tissues,” J. Neurosci. Methods 8(1), 41–49 (1983).
[PubMed]

Agostinis, P.

P. Agostinis, K. Berg, K. A. Cengel, T. H. Foster, A. W. Girotti, S. O. Gollnick, S. M. Hahn, M. R. Hamblin, A. Juzeniene, D. Kessel, M. Korbelik, J. Moan, P. Mroz, D. Nowis, J. Piette, B. C. Wilson, and J. Golab, “Photodynamic Therapy of Cancer: An Update,” CA Cancer J. Clin. 61(4), 250–281 (2011).
[PubMed]

Alahuhta, S.

V. Kiviniemi, V. Korhonen, J. Kortelainen, S. Rytky, T. Keinänen, T. Tuovinen, M. Isokangas, E. Sonkajärvi, T. Siniluoto, J. Nikkinen, S. Alahuhta, O. Tervonen, T. Turpeenniemi-Hujanen, T. Myllylä, O. Kuittinen, and J. Voipio, “Real-time monitoring of human blood-brain barrier disruption,” PLoS One 12(3), e0174072 (2017).
[PubMed]

Angell-Petersen, E.

E. Angell-Petersen, S. Spetalen, S. J. Madsen, C. H. Sun, Q. Peng, S. W. Carper, M. Sioud, and H. Hirschberg, “Influence of light fluence rate on the effects of photodynamic therapy in an orthotopic rat glioma model,” J. Neurosurg. 104(1), 109–117 (2006).
[PubMed]

Berg, K.

P. Agostinis, K. Berg, K. A. Cengel, T. H. Foster, A. W. Girotti, S. O. Gollnick, S. M. Hahn, M. R. Hamblin, A. Juzeniene, D. Kessel, M. Korbelik, J. Moan, P. Mroz, D. Nowis, J. Piette, B. C. Wilson, and J. Golab, “Photodynamic Therapy of Cancer: An Update,” CA Cancer J. Clin. 61(4), 250–281 (2011).
[PubMed]

Bernier, M.

G. Vandeplassche, M. Bernier, F. Thoné, M. Borgers, Y. Kusama, and D. J. Hearse, “Singlet oxygen and myocardial injury: ultrastructural, cytochemical and electrocardiographic consequences of photoactivation of rose bengal,” J. Mol. Cell. Cardiol. 22(3), 287–301 (1990).
[PubMed]

Y. Kusama, M. Bernier, and D. J. Hearse, “Singlet oxygen-induced arrhythmias. dose- and light-response studies for photoactivation of rose bengal in the rat heart,” Circulation 80(5), 1432–1448 (1989).
[PubMed]

Borgers, M.

G. Vandeplassche, M. Bernier, F. Thoné, M. Borgers, Y. Kusama, and D. J. Hearse, “Singlet oxygen and myocardial injury: ultrastructural, cytochemical and electrocardiographic consequences of photoactivation of rose bengal,” J. Mol. Cell. Cardiol. 22(3), 287–301 (1990).
[PubMed]

Bredno, J.

A. Hoffmann, J. Bredno, M. Wendland, N. Derugin, P. Ohara, and M. Wintermark, “High and low molecular weight fluorescein isothiocyanate (FITC)-dextran to assess blood-brain barrier disruption: technical consideration,” Transl. Stroke Res. 2(1), 106–111 (2011).
[PubMed]

Carper, S. W.

E. Angell-Petersen, S. Spetalen, S. J. Madsen, C. H. Sun, Q. Peng, S. W. Carper, M. Sioud, and H. Hirschberg, “Influence of light fluence rate on the effects of photodynamic therapy in an orthotopic rat glioma model,” J. Neurosurg. 104(1), 109–117 (2006).
[PubMed]

Cengel, K. A.

P. Agostinis, K. Berg, K. A. Cengel, T. H. Foster, A. W. Girotti, S. O. Gollnick, S. M. Hahn, M. R. Hamblin, A. Juzeniene, D. Kessel, M. Korbelik, J. Moan, P. Mroz, D. Nowis, J. Piette, B. C. Wilson, and J. Golab, “Photodynamic Therapy of Cancer: An Update,” CA Cancer J. Clin. 61(4), 250–281 (2011).
[PubMed]

Chai, W. Y.

P. C. Chu, W. Y. Chai, C. H. Tsai, S. T. Kang, C. K. Yeh, and H. L. Liu, “Focused Ultrasound-Induced Blood-Brain Barrier Opening: Association with Mechanical Index and Cavitation Index Analyzed by Dynamic Contrast-Enhanced Magnetic-Resonance Imaging,” Sci. Rep. 6, 33264 (2016).
[PubMed]

Chang, C. S.

K. B. Chen, E. Y. Kuo, K. S. Poon, K. S. Cheng, C. S. Chang, Y. C. Liu, and T. W. Lai, “Increase in Evans blue dye extravasation into the brain in the late developmental stage,” Neuroreport 23(12), 699–701 (2012).
[PubMed]

Chen, K. B.

K. B. Chen, E. Y. Kuo, K. S. Poon, K. S. Cheng, C. S. Chang, Y. C. Liu, and T. W. Lai, “Increase in Evans blue dye extravasation into the brain in the late developmental stage,” Neuroreport 23(12), 699–701 (2012).
[PubMed]

Cheng, H. B.

S. S. Hu, H. B. Cheng, Y. R. Zheng, R. Y. Zhang, W. Yue, and H. Zhang, “Effects of photodynamic therapy on the ultrastructure of glioma cells,” Biomed. Environ. Sci. 20(4), 269–273 (2007).
[PubMed]

Cheng, K. S.

K. B. Chen, E. Y. Kuo, K. S. Poon, K. S. Cheng, C. S. Chang, Y. C. Liu, and T. W. Lai, “Increase in Evans blue dye extravasation into the brain in the late developmental stage,” Neuroreport 23(12), 699–701 (2012).
[PubMed]

Chighvinadze, D.

H. Hirschberg, F. A. Uzal, D. Chighvinadze, M. J. Zhang, Q. Peng, and S. J. Madsen, “Disruption of the Blood-Brain Barrier Following ALA-Mediated Photodynamic Therapy,” Lasers Surg. Med. 40(8), 535–542 (2008).
[PubMed]

Christie, C.

S. J. Madsen, C. Christie, S. J. Hong, A. Trinidad, Q. Peng, F. A. Uzal, and H. Hirschberg, “Nanoparticle-loaded macrophage-mediated photothermal therapy: potential for glioma treatment,” Lasers Med. Sci. 30(4), 1357–1365 (2015).
[PubMed]

Chu, P. C.

P. C. Chu, W. Y. Chai, C. H. Tsai, S. T. Kang, C. K. Yeh, and H. L. Liu, “Focused Ultrasound-Induced Blood-Brain Barrier Opening: Association with Mechanical Index and Cavitation Index Analyzed by Dynamic Contrast-Enhanced Magnetic-Resonance Imaging,” Sci. Rep. 6, 33264 (2016).
[PubMed]

Colditz, M. J.

M. J. Colditz and R. L. Jeffree, “Aminolevulinic acid (ALA)-protoporphyrin IX fluorescence guided tumour resection. Part 1: Clinical, radiological and pathological studies,” J. Clin. Neurosci. 19(11), 1471–1474 (2012).
[PubMed]

Derugin, N.

A. Hoffmann, J. Bredno, M. Wendland, N. Derugin, P. Ohara, and M. Wintermark, “High and low molecular weight fluorescein isothiocyanate (FITC)-dextran to assess blood-brain barrier disruption: technical consideration,” Transl. Stroke Res. 2(1), 106–111 (2011).
[PubMed]

Fingar, V. H.

V. H. Fingar, “Vascular effects of photodynamic therapy,” J. Clin. Laser Med. Surg. 14(5), 323–328 (1996).
[PubMed]

Foster, T. H.

P. Agostinis, K. Berg, K. A. Cengel, T. H. Foster, A. W. Girotti, S. O. Gollnick, S. M. Hahn, M. R. Hamblin, A. Juzeniene, D. Kessel, M. Korbelik, J. Moan, P. Mroz, D. Nowis, J. Piette, B. C. Wilson, and J. Golab, “Photodynamic Therapy of Cancer: An Update,” CA Cancer J. Clin. 61(4), 250–281 (2011).
[PubMed]

L. A. Sporn and T. H. Foster, “Photofrin and light induces microtubule depolymerization in cultured human endothelial cells,” Cancer Res. 52(12), 3443–3448 (1992).
[PubMed]

Gach, H. M.

S. J. Madsen, H. M. Gach, S. J. Hong, F. A. Uzal, Q. Peng, and H. Hirschberg, “Increased nanoparticle-loaded exogenous macrophage migration into the brain following PDT-induced blood-brain barrier disruption,” Lasers Surg. Med. 45(8), 524–532 (2013).
[PubMed]

Ghose, A. K.

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P. Agostinis, K. Berg, K. A. Cengel, T. H. Foster, A. W. Girotti, S. O. Gollnick, S. M. Hahn, M. R. Hamblin, A. Juzeniene, D. Kessel, M. Korbelik, J. Moan, P. Mroz, D. Nowis, J. Piette, B. C. Wilson, and J. Golab, “Photodynamic Therapy of Cancer: An Update,” CA Cancer J. Clin. 61(4), 250–281 (2011).
[PubMed]

Golab, J.

P. Agostinis, K. Berg, K. A. Cengel, T. H. Foster, A. W. Girotti, S. O. Gollnick, S. M. Hahn, M. R. Hamblin, A. Juzeniene, D. Kessel, M. Korbelik, J. Moan, P. Mroz, D. Nowis, J. Piette, B. C. Wilson, and J. Golab, “Photodynamic Therapy of Cancer: An Update,” CA Cancer J. Clin. 61(4), 250–281 (2011).
[PubMed]

Gollnick, S. O.

P. Agostinis, K. Berg, K. A. Cengel, T. H. Foster, A. W. Girotti, S. O. Gollnick, S. M. Hahn, M. R. Hamblin, A. Juzeniene, D. Kessel, M. Korbelik, J. Moan, P. Mroz, D. Nowis, J. Piette, B. C. Wilson, and J. Golab, “Photodynamic Therapy of Cancer: An Update,” CA Cancer J. Clin. 61(4), 250–281 (2011).
[PubMed]

Gran, B.

S. Wu, K. Li, Y. Yan, B. Gran, Y. Han, F. Zhou, Y. T. Guan, A. Rostami, and G. X. Zhang, “Intranasal Delivery of Neural Stem Cells: A CNS-specific, Non-invasive Cell-based Therapy for Experimental Autoimmune Encephalomyelitis,” J. Clin. Cell. Immunol. 4(3), 24244890 (2013).
[PubMed]

Guan, Y. T.

S. Wu, K. Li, Y. Yan, B. Gran, Y. Han, F. Zhou, Y. T. Guan, A. Rostami, and G. X. Zhang, “Intranasal Delivery of Neural Stem Cells: A CNS-specific, Non-invasive Cell-based Therapy for Experimental Autoimmune Encephalomyelitis,” J. Clin. Cell. Immunol. 4(3), 24244890 (2013).
[PubMed]

Gupta, U.

P. K. Pandey, A. K. Sharma, and U. Gupta, “Blood brain barrier: An overview on strategies in drug delivery, realistic in vitro modeling and in vivo live tracking,” Tissue Barriers 4(1), e1129476 (2015).
[PubMed]

Hahn, S. M.

P. Agostinis, K. Berg, K. A. Cengel, T. H. Foster, A. W. Girotti, S. O. Gollnick, S. M. Hahn, M. R. Hamblin, A. Juzeniene, D. Kessel, M. Korbelik, J. Moan, P. Mroz, D. Nowis, J. Piette, B. C. Wilson, and J. Golab, “Photodynamic Therapy of Cancer: An Update,” CA Cancer J. Clin. 61(4), 250–281 (2011).
[PubMed]

Hamblin, M. R.

P. Agostinis, K. Berg, K. A. Cengel, T. H. Foster, A. W. Girotti, S. O. Gollnick, S. M. Hahn, M. R. Hamblin, A. Juzeniene, D. Kessel, M. Korbelik, J. Moan, P. Mroz, D. Nowis, J. Piette, B. C. Wilson, and J. Golab, “Photodynamic Therapy of Cancer: An Update,” CA Cancer J. Clin. 61(4), 250–281 (2011).
[PubMed]

Han, Y.

S. Wu, K. Li, Y. Yan, B. Gran, Y. Han, F. Zhou, Y. T. Guan, A. Rostami, and G. X. Zhang, “Intranasal Delivery of Neural Stem Cells: A CNS-specific, Non-invasive Cell-based Therapy for Experimental Autoimmune Encephalomyelitis,” J. Clin. Cell. Immunol. 4(3), 24244890 (2013).
[PubMed]

Hearse, D. J.

G. Vandeplassche, M. Bernier, F. Thoné, M. Borgers, Y. Kusama, and D. J. Hearse, “Singlet oxygen and myocardial injury: ultrastructural, cytochemical and electrocardiographic consequences of photoactivation of rose bengal,” J. Mol. Cell. Cardiol. 22(3), 287–301 (1990).
[PubMed]

Y. Kusama, M. Bernier, and D. J. Hearse, “Singlet oxygen-induced arrhythmias. dose- and light-response studies for photoactivation of rose bengal in the rat heart,” Circulation 80(5), 1432–1448 (1989).
[PubMed]

Hirschberg, H.

S. J. Madsen, C. Christie, S. J. Hong, A. Trinidad, Q. Peng, F. A. Uzal, and H. Hirschberg, “Nanoparticle-loaded macrophage-mediated photothermal therapy: potential for glioma treatment,” Lasers Med. Sci. 30(4), 1357–1365 (2015).
[PubMed]

S. J. Madsen, H. M. Gach, S. J. Hong, F. A. Uzal, Q. Peng, and H. Hirschberg, “Increased nanoparticle-loaded exogenous macrophage migration into the brain following PDT-induced blood-brain barrier disruption,” Lasers Surg. Med. 45(8), 524–532 (2013).
[PubMed]

S. J. Madsen and H. Hirschberg, “Site-specific opening of the blood-brain barrier,” J. Biophotonics 3(5-6), 356–367 (2010).
[PubMed]

H. Hirschberg, F. A. Uzal, D. Chighvinadze, M. J. Zhang, Q. Peng, and S. J. Madsen, “Disruption of the Blood-Brain Barrier Following ALA-Mediated Photodynamic Therapy,” Lasers Surg. Med. 40(8), 535–542 (2008).
[PubMed]

E. Angell-Petersen, S. Spetalen, S. J. Madsen, C. H. Sun, Q. Peng, S. W. Carper, M. Sioud, and H. Hirschberg, “Influence of light fluence rate on the effects of photodynamic therapy in an orthotopic rat glioma model,” J. Neurosurg. 104(1), 109–117 (2006).
[PubMed]

Hoffmann, A.

A. Hoffmann, J. Bredno, M. Wendland, N. Derugin, P. Ohara, and M. Wintermark, “High and low molecular weight fluorescein isothiocyanate (FITC)-dextran to assess blood-brain barrier disruption: technical consideration,” Transl. Stroke Res. 2(1), 106–111 (2011).
[PubMed]

Hong, S. J.

S. J. Madsen, C. Christie, S. J. Hong, A. Trinidad, Q. Peng, F. A. Uzal, and H. Hirschberg, “Nanoparticle-loaded macrophage-mediated photothermal therapy: potential for glioma treatment,” Lasers Med. Sci. 30(4), 1357–1365 (2015).
[PubMed]

S. J. Madsen, H. M. Gach, S. J. Hong, F. A. Uzal, Q. Peng, and H. Hirschberg, “Increased nanoparticle-loaded exogenous macrophage migration into the brain following PDT-induced blood-brain barrier disruption,” Lasers Surg. Med. 45(8), 524–532 (2013).
[PubMed]

Hu, S. S.

S. S. Hu, H. B. Cheng, Y. R. Zheng, R. Y. Zhang, W. Yue, and H. Zhang, “Effects of photodynamic therapy on the ultrastructure of glioma cells,” Biomed. Environ. Sci. 20(4), 269–273 (2007).
[PubMed]

Isokangas, M.

V. Kiviniemi, V. Korhonen, J. Kortelainen, S. Rytky, T. Keinänen, T. Tuovinen, M. Isokangas, E. Sonkajärvi, T. Siniluoto, J. Nikkinen, S. Alahuhta, O. Tervonen, T. Turpeenniemi-Hujanen, T. Myllylä, O. Kuittinen, and J. Voipio, “Real-time monitoring of human blood-brain barrier disruption,” PLoS One 12(3), e0174072 (2017).
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Jeffree, R. L.

M. J. Colditz and R. L. Jeffree, “Aminolevulinic acid (ALA)-protoporphyrin IX fluorescence guided tumour resection. Part 1: Clinical, radiological and pathological studies,” J. Clin. Neurosci. 19(11), 1471–1474 (2012).
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Juzeniene, A.

P. Agostinis, K. Berg, K. A. Cengel, T. H. Foster, A. W. Girotti, S. O. Gollnick, S. M. Hahn, M. R. Hamblin, A. Juzeniene, D. Kessel, M. Korbelik, J. Moan, P. Mroz, D. Nowis, J. Piette, B. C. Wilson, and J. Golab, “Photodynamic Therapy of Cancer: An Update,” CA Cancer J. Clin. 61(4), 250–281 (2011).
[PubMed]

Kang, S. T.

P. C. Chu, W. Y. Chai, C. H. Tsai, S. T. Kang, C. K. Yeh, and H. L. Liu, “Focused Ultrasound-Induced Blood-Brain Barrier Opening: Association with Mechanical Index and Cavitation Index Analyzed by Dynamic Contrast-Enhanced Magnetic-Resonance Imaging,” Sci. Rep. 6, 33264 (2016).
[PubMed]

Kaye, A. H.

S. S. Stylli and A. H. Kaye, “Photodynamic therapy of cerebral glioma-A review Part I-A biological basis,” J. Clin. Neurosci. 13(6), 615–625 (2006).
[PubMed]

Keinänen, T.

V. Kiviniemi, V. Korhonen, J. Kortelainen, S. Rytky, T. Keinänen, T. Tuovinen, M. Isokangas, E. Sonkajärvi, T. Siniluoto, J. Nikkinen, S. Alahuhta, O. Tervonen, T. Turpeenniemi-Hujanen, T. Myllylä, O. Kuittinen, and J. Voipio, “Real-time monitoring of human blood-brain barrier disruption,” PLoS One 12(3), e0174072 (2017).
[PubMed]

Kessel, D.

P. Agostinis, K. Berg, K. A. Cengel, T. H. Foster, A. W. Girotti, S. O. Gollnick, S. M. Hahn, M. R. Hamblin, A. Juzeniene, D. Kessel, M. Korbelik, J. Moan, P. Mroz, D. Nowis, J. Piette, B. C. Wilson, and J. Golab, “Photodynamic Therapy of Cancer: An Update,” CA Cancer J. Clin. 61(4), 250–281 (2011).
[PubMed]

Kiviniemi, V.

V. Kiviniemi, V. Korhonen, J. Kortelainen, S. Rytky, T. Keinänen, T. Tuovinen, M. Isokangas, E. Sonkajärvi, T. Siniluoto, J. Nikkinen, S. Alahuhta, O. Tervonen, T. Turpeenniemi-Hujanen, T. Myllylä, O. Kuittinen, and J. Voipio, “Real-time monitoring of human blood-brain barrier disruption,” PLoS One 12(3), e0174072 (2017).
[PubMed]

Korbelik, M.

P. Agostinis, K. Berg, K. A. Cengel, T. H. Foster, A. W. Girotti, S. O. Gollnick, S. M. Hahn, M. R. Hamblin, A. Juzeniene, D. Kessel, M. Korbelik, J. Moan, P. Mroz, D. Nowis, J. Piette, B. C. Wilson, and J. Golab, “Photodynamic Therapy of Cancer: An Update,” CA Cancer J. Clin. 61(4), 250–281 (2011).
[PubMed]

Korhonen, V.

V. Kiviniemi, V. Korhonen, J. Kortelainen, S. Rytky, T. Keinänen, T. Tuovinen, M. Isokangas, E. Sonkajärvi, T. Siniluoto, J. Nikkinen, S. Alahuhta, O. Tervonen, T. Turpeenniemi-Hujanen, T. Myllylä, O. Kuittinen, and J. Voipio, “Real-time monitoring of human blood-brain barrier disruption,” PLoS One 12(3), e0174072 (2017).
[PubMed]

Kortelainen, J.

V. Kiviniemi, V. Korhonen, J. Kortelainen, S. Rytky, T. Keinänen, T. Tuovinen, M. Isokangas, E. Sonkajärvi, T. Siniluoto, J. Nikkinen, S. Alahuhta, O. Tervonen, T. Turpeenniemi-Hujanen, T. Myllylä, O. Kuittinen, and J. Voipio, “Real-time monitoring of human blood-brain barrier disruption,” PLoS One 12(3), e0174072 (2017).
[PubMed]

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B. Krammer, “Vascular effects of photodynamic therapy,” Anticancer Res. 21(6B), 4271–4277 (2001).
[PubMed]

Kuittinen, O.

V. Kiviniemi, V. Korhonen, J. Kortelainen, S. Rytky, T. Keinänen, T. Tuovinen, M. Isokangas, E. Sonkajärvi, T. Siniluoto, J. Nikkinen, S. Alahuhta, O. Tervonen, T. Turpeenniemi-Hujanen, T. Myllylä, O. Kuittinen, and J. Voipio, “Real-time monitoring of human blood-brain barrier disruption,” PLoS One 12(3), e0174072 (2017).
[PubMed]

Kuo, E. Y.

K. B. Chen, E. Y. Kuo, K. S. Poon, K. S. Cheng, C. S. Chang, Y. C. Liu, and T. W. Lai, “Increase in Evans blue dye extravasation into the brain in the late developmental stage,” Neuroreport 23(12), 699–701 (2012).
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T. Kuroiwa, “Photodynamic diagnosis and photodynamic therapy for the brain tumors,” Progress in Neuro-Oncology. 21, 14–21 (2014).

Kusama, Y.

G. Vandeplassche, M. Bernier, F. Thoné, M. Borgers, Y. Kusama, and D. J. Hearse, “Singlet oxygen and myocardial injury: ultrastructural, cytochemical and electrocardiographic consequences of photoactivation of rose bengal,” J. Mol. Cell. Cardiol. 22(3), 287–301 (1990).
[PubMed]

Y. Kusama, M. Bernier, and D. J. Hearse, “Singlet oxygen-induced arrhythmias. dose- and light-response studies for photoactivation of rose bengal in the rat heart,” Circulation 80(5), 1432–1448 (1989).
[PubMed]

Lai, T. W.

H. L. Wang and T. W. Lai, “Optimization of Evans blue quantitation in limited rat tissue samples,” Sci. Rep. 4, 6588 (2014).
[PubMed]

K. B. Chen, E. Y. Kuo, K. S. Poon, K. S. Cheng, C. S. Chang, Y. C. Liu, and T. W. Lai, “Increase in Evans blue dye extravasation into the brain in the late developmental stage,” Neuroreport 23(12), 699–701 (2012).
[PubMed]

Lee, M. C.

F. Yoshino, H. Shoji, and M. C. Lee, “Vascular effects of singlet oxygen (1O2) generated by photo-excitation on adrenergic neurotransmission in isolated rabbit mesenteric vein,” Redox Rep. 7(5), 266–270 (2002).
[PubMed]

Li, K.

S. Wu, K. Li, Y. Yan, B. Gran, Y. Han, F. Zhou, Y. T. Guan, A. Rostami, and G. X. Zhang, “Intranasal Delivery of Neural Stem Cells: A CNS-specific, Non-invasive Cell-based Therapy for Experimental Autoimmune Encephalomyelitis,” J. Clin. Cell. Immunol. 4(3), 24244890 (2013).
[PubMed]

Liu, H. L.

P. C. Chu, W. Y. Chai, C. H. Tsai, S. T. Kang, C. K. Yeh, and H. L. Liu, “Focused Ultrasound-Induced Blood-Brain Barrier Opening: Association with Mechanical Index and Cavitation Index Analyzed by Dynamic Contrast-Enhanced Magnetic-Resonance Imaging,” Sci. Rep. 6, 33264 (2016).
[PubMed]

Liu, Y. C.

K. B. Chen, E. Y. Kuo, K. S. Poon, K. S. Cheng, C. S. Chang, Y. C. Liu, and T. W. Lai, “Increase in Evans blue dye extravasation into the brain in the late developmental stage,” Neuroreport 23(12), 699–701 (2012).
[PubMed]

Lundberg, J. M.

A. Saria and J. M. Lundberg, “Evans blue fluorescence: quantitative and morphological evaluation of vascular permeability in animal tissues,” J. Neurosci. Methods 8(1), 41–49 (1983).
[PubMed]

Madsen, S. J.

S. J. Madsen, C. Christie, S. J. Hong, A. Trinidad, Q. Peng, F. A. Uzal, and H. Hirschberg, “Nanoparticle-loaded macrophage-mediated photothermal therapy: potential for glioma treatment,” Lasers Med. Sci. 30(4), 1357–1365 (2015).
[PubMed]

S. J. Madsen, H. M. Gach, S. J. Hong, F. A. Uzal, Q. Peng, and H. Hirschberg, “Increased nanoparticle-loaded exogenous macrophage migration into the brain following PDT-induced blood-brain barrier disruption,” Lasers Surg. Med. 45(8), 524–532 (2013).
[PubMed]

S. J. Madsen and H. Hirschberg, “Site-specific opening of the blood-brain barrier,” J. Biophotonics 3(5-6), 356–367 (2010).
[PubMed]

H. Hirschberg, F. A. Uzal, D. Chighvinadze, M. J. Zhang, Q. Peng, and S. J. Madsen, “Disruption of the Blood-Brain Barrier Following ALA-Mediated Photodynamic Therapy,” Lasers Surg. Med. 40(8), 535–542 (2008).
[PubMed]

E. Angell-Petersen, S. Spetalen, S. J. Madsen, C. H. Sun, Q. Peng, S. W. Carper, M. Sioud, and H. Hirschberg, “Influence of light fluence rate on the effects of photodynamic therapy in an orthotopic rat glioma model,” J. Neurosurg. 104(1), 109–117 (2006).
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S. Mitragotri, “Devices for overcoming biological barriers: The use of physical forces to disrupt the barriers,” Adv. Drug Deliv. Rev. 65(1), 100–103 (2013).
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H. Mizukawa and E. Okabe, “Inhibition by singlet molecular oxygen of the vascular reactivity in rabbit mesenteric artery,” Br. J. Pharmacol. 121(1), 63–70 (1997).
[PubMed]

Moan, J.

P. Agostinis, K. Berg, K. A. Cengel, T. H. Foster, A. W. Girotti, S. O. Gollnick, S. M. Hahn, M. R. Hamblin, A. Juzeniene, D. Kessel, M. Korbelik, J. Moan, P. Mroz, D. Nowis, J. Piette, B. C. Wilson, and J. Golab, “Photodynamic Therapy of Cancer: An Update,” CA Cancer J. Clin. 61(4), 250–281 (2011).
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Mroz, P.

P. Agostinis, K. Berg, K. A. Cengel, T. H. Foster, A. W. Girotti, S. O. Gollnick, S. M. Hahn, M. R. Hamblin, A. Juzeniene, D. Kessel, M. Korbelik, J. Moan, P. Mroz, D. Nowis, J. Piette, B. C. Wilson, and J. Golab, “Photodynamic Therapy of Cancer: An Update,” CA Cancer J. Clin. 61(4), 250–281 (2011).
[PubMed]

Myllylä, T.

V. Kiviniemi, V. Korhonen, J. Kortelainen, S. Rytky, T. Keinänen, T. Tuovinen, M. Isokangas, E. Sonkajärvi, T. Siniluoto, J. Nikkinen, S. Alahuhta, O. Tervonen, T. Turpeenniemi-Hujanen, T. Myllylä, O. Kuittinen, and J. Voipio, “Real-time monitoring of human blood-brain barrier disruption,” PLoS One 12(3), e0174072 (2017).
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S. Nag, “Blood-brain barrier permeability using tracers and immunohistochemistry,” Methods Mol. Med. 89, 133–144 (2003).
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Nelson, G. H.

W. I. Rosenblum and G. H. Nelson, “Singlet oxygen scavengers affect laser-dye impairment of endothelium-dependent responses of brain arterioles,” Am. J. Physiol. 270(4 Pt 2), H1258–H1263 (1996).
[PubMed]

Nikkinen, J.

V. Kiviniemi, V. Korhonen, J. Kortelainen, S. Rytky, T. Keinänen, T. Tuovinen, M. Isokangas, E. Sonkajärvi, T. Siniluoto, J. Nikkinen, S. Alahuhta, O. Tervonen, T. Turpeenniemi-Hujanen, T. Myllylä, O. Kuittinen, and J. Voipio, “Real-time monitoring of human blood-brain barrier disruption,” PLoS One 12(3), e0174072 (2017).
[PubMed]

Nowis, D.

P. Agostinis, K. Berg, K. A. Cengel, T. H. Foster, A. W. Girotti, S. O. Gollnick, S. M. Hahn, M. R. Hamblin, A. Juzeniene, D. Kessel, M. Korbelik, J. Moan, P. Mroz, D. Nowis, J. Piette, B. C. Wilson, and J. Golab, “Photodynamic Therapy of Cancer: An Update,” CA Cancer J. Clin. 61(4), 250–281 (2011).
[PubMed]

Ohara, P.

A. Hoffmann, J. Bredno, M. Wendland, N. Derugin, P. Ohara, and M. Wintermark, “High and low molecular weight fluorescein isothiocyanate (FITC)-dextran to assess blood-brain barrier disruption: technical consideration,” Transl. Stroke Res. 2(1), 106–111 (2011).
[PubMed]

Okabe, E.

H. Mizukawa and E. Okabe, “Inhibition by singlet molecular oxygen of the vascular reactivity in rabbit mesenteric artery,” Br. J. Pharmacol. 121(1), 63–70 (1997).
[PubMed]

Pandey, P. K.

P. K. Pandey, A. K. Sharma, and U. Gupta, “Blood brain barrier: An overview on strategies in drug delivery, realistic in vitro modeling and in vivo live tracking,” Tissue Barriers 4(1), e1129476 (2015).
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W. M. Pardridge, “Blood-brain barrier delivery,” Drug Discov. Today 12(1-2), 54–61 (2007).
[PubMed]

Peng, Q.

S. J. Madsen, C. Christie, S. J. Hong, A. Trinidad, Q. Peng, F. A. Uzal, and H. Hirschberg, “Nanoparticle-loaded macrophage-mediated photothermal therapy: potential for glioma treatment,” Lasers Med. Sci. 30(4), 1357–1365 (2015).
[PubMed]

S. J. Madsen, H. M. Gach, S. J. Hong, F. A. Uzal, Q. Peng, and H. Hirschberg, “Increased nanoparticle-loaded exogenous macrophage migration into the brain following PDT-induced blood-brain barrier disruption,” Lasers Surg. Med. 45(8), 524–532 (2013).
[PubMed]

H. Hirschberg, F. A. Uzal, D. Chighvinadze, M. J. Zhang, Q. Peng, and S. J. Madsen, “Disruption of the Blood-Brain Barrier Following ALA-Mediated Photodynamic Therapy,” Lasers Surg. Med. 40(8), 535–542 (2008).
[PubMed]

E. Angell-Petersen, S. Spetalen, S. J. Madsen, C. H. Sun, Q. Peng, S. W. Carper, M. Sioud, and H. Hirschberg, “Influence of light fluence rate on the effects of photodynamic therapy in an orthotopic rat glioma model,” J. Neurosurg. 104(1), 109–117 (2006).
[PubMed]

Pichlmeier, U.

W. Stummer, H. Stepp, O. D. Wiestler, and U. Pichlmeier, “Randomized, Prospective Double-Blinded Study Comparing 3 Different Doses of 5-Aminolevulinic Acid for Fluorescence-Guided Resections of Malignant Gliomas,” Neurosurgery 81(2), 230–239 (2017).
[PubMed]

Piette, J.

P. Agostinis, K. Berg, K. A. Cengel, T. H. Foster, A. W. Girotti, S. O. Gollnick, S. M. Hahn, M. R. Hamblin, A. Juzeniene, D. Kessel, M. Korbelik, J. Moan, P. Mroz, D. Nowis, J. Piette, B. C. Wilson, and J. Golab, “Photodynamic Therapy of Cancer: An Update,” CA Cancer J. Clin. 61(4), 250–281 (2011).
[PubMed]

Poon, K. S.

K. B. Chen, E. Y. Kuo, K. S. Poon, K. S. Cheng, C. S. Chang, Y. C. Liu, and T. W. Lai, “Increase in Evans blue dye extravasation into the brain in the late developmental stage,” Neuroreport 23(12), 699–701 (2012).
[PubMed]

Rosenblum, W. I.

W. I. Rosenblum and G. H. Nelson, “Singlet oxygen scavengers affect laser-dye impairment of endothelium-dependent responses of brain arterioles,” Am. J. Physiol. 270(4 Pt 2), H1258–H1263 (1996).
[PubMed]

Rostami, A.

S. Wu, K. Li, Y. Yan, B. Gran, Y. Han, F. Zhou, Y. T. Guan, A. Rostami, and G. X. Zhang, “Intranasal Delivery of Neural Stem Cells: A CNS-specific, Non-invasive Cell-based Therapy for Experimental Autoimmune Encephalomyelitis,” J. Clin. Cell. Immunol. 4(3), 24244890 (2013).
[PubMed]

Rytky, S.

V. Kiviniemi, V. Korhonen, J. Kortelainen, S. Rytky, T. Keinänen, T. Tuovinen, M. Isokangas, E. Sonkajärvi, T. Siniluoto, J. Nikkinen, S. Alahuhta, O. Tervonen, T. Turpeenniemi-Hujanen, T. Myllylä, O. Kuittinen, and J. Voipio, “Real-time monitoring of human blood-brain barrier disruption,” PLoS One 12(3), e0174072 (2017).
[PubMed]

Saria, A.

A. Saria and J. M. Lundberg, “Evans blue fluorescence: quantitative and morphological evaluation of vascular permeability in animal tissues,” J. Neurosci. Methods 8(1), 41–49 (1983).
[PubMed]

Semyachkina-Glushkovskaya, O.

Semyachkina-Glushkovskaya, O. V.

O. V. Semyachkina-Glushkovskaya, “Laser-induced generation of singlet oxygen and its role in the cerebrovascular physiology,” Prog. Quantum Electron. 55, 112–128 (2017).

Sharma, A. K.

P. K. Pandey, A. K. Sharma, and U. Gupta, “Blood brain barrier: An overview on strategies in drug delivery, realistic in vitro modeling and in vivo live tracking,” Tissue Barriers 4(1), e1129476 (2015).
[PubMed]

Shoji, H.

F. Yoshino, H. Shoji, and M. C. Lee, “Vascular effects of singlet oxygen (1O2) generated by photo-excitation on adrenergic neurotransmission in isolated rabbit mesenteric vein,” Redox Rep. 7(5), 266–270 (2002).
[PubMed]

Siniluoto, T.

V. Kiviniemi, V. Korhonen, J. Kortelainen, S. Rytky, T. Keinänen, T. Tuovinen, M. Isokangas, E. Sonkajärvi, T. Siniluoto, J. Nikkinen, S. Alahuhta, O. Tervonen, T. Turpeenniemi-Hujanen, T. Myllylä, O. Kuittinen, and J. Voipio, “Real-time monitoring of human blood-brain barrier disruption,” PLoS One 12(3), e0174072 (2017).
[PubMed]

Sioud, M.

E. Angell-Petersen, S. Spetalen, S. J. Madsen, C. H. Sun, Q. Peng, S. W. Carper, M. Sioud, and H. Hirschberg, “Influence of light fluence rate on the effects of photodynamic therapy in an orthotopic rat glioma model,” J. Neurosurg. 104(1), 109–117 (2006).
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Sonkajärvi, E.

V. Kiviniemi, V. Korhonen, J. Kortelainen, S. Rytky, T. Keinänen, T. Tuovinen, M. Isokangas, E. Sonkajärvi, T. Siniluoto, J. Nikkinen, S. Alahuhta, O. Tervonen, T. Turpeenniemi-Hujanen, T. Myllylä, O. Kuittinen, and J. Voipio, “Real-time monitoring of human blood-brain barrier disruption,” PLoS One 12(3), e0174072 (2017).
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W. Stummer, H. Stepp, O. D. Wiestler, and U. Pichlmeier, “Randomized, Prospective Double-Blinded Study Comparing 3 Different Doses of 5-Aminolevulinic Acid for Fluorescence-Guided Resections of Malignant Gliomas,” Neurosurgery 81(2), 230–239 (2017).
[PubMed]

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W. Stummer, H. Stepp, O. D. Wiestler, and U. Pichlmeier, “Randomized, Prospective Double-Blinded Study Comparing 3 Different Doses of 5-Aminolevulinic Acid for Fluorescence-Guided Resections of Malignant Gliomas,” Neurosurgery 81(2), 230–239 (2017).
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Figures (3)

Fig. 1
Fig. 1 Fluorescent intensity at 635 nm associated with 5-ALA signal before light irradiation and 90 min after light irradiation of mouse brain.
Fig. 2
Fig. 2 Fluorescence spectra of brain tissues with different 5-ALA dose applied – autofluorescence and exogenous fluorophore emission are observed.
Fig. 3
Fig. 3 The PDT-induced BBB disruption evaluated by confocal imaging of FITC-dextran (70 kD) extravasation from cerebral microvessels into the brain parenchyma and histological analysis of solutes leakage. A – confocal imaging: left – no extravasation of FITC-dextran in control group without laser application; middle- strong extravasation of FITC-dextran defined as a bright cloud (circled) clearly associated with group of vessels [19]; right - diffuse extravasation of FITC-dextran (circled) defined as extensive leakage of the tracer including several groups of cerebral microvessels. B – histological results: left – no solutes leakage in normal brain tissues; middle – moderate perivascular edema suggesting solute leakage from cerebral microvessels and accumulation of solutes in perivascular space; right – severe perivascular edema reflecting the stronger BBB disruption for solute leakage.

Tables (1)

Tables Icon

Table 1 The 5-ALA-PDT-related changes in the BBB permeability to Evans Blue

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