Display options
Share it on

Front Oncol. 2020 Jun 05;10:739. doi: 10.3389/fonc.2020.00739. eCollection 2020.

Blood-Brain Barrier, Blood-Brain Tumor Barrier, and Fluorescence-Guided Neurosurgical Oncology: Delivering Optical Labels to Brain Tumors.

Frontiers in oncology

Evgenii Belykh, Kurt V Shaffer, Chaoqun Lin, Vadim A Byvaltsev, Mark C Preul, Lukui Chen

Affiliations

  1. Department of Neurosurgery, Barrow Neurological Institute, St. Joseph's Hospital and Medical Center, Phoenix, AZ, United States.
  2. Department of Neurosurgery, School of Medicine, Southeast University, Nanjing, China.
  3. Department of Neurosurgery, Irkutsk State Medical University, Irkutsk, Russia.
  4. Department of Neurosurgery, Neuroscience Center, Cancer Center, Integrated Hospital of Traditional Chinese Medicine, Southern Medical University, Guangzhou, China.

PMID: 32582530 PMCID: PMC7290051 DOI: 10.3389/fonc.2020.00739

Abstract

Recent advances in maximum safe glioma resection have included the introduction of a host of visualization techniques to complement intraoperative white-light imaging of tumors. However, barriers to the effective use of these techniques within the central nervous system remain. In the healthy brain, the blood-brain barrier ensures the stability of the sensitive internal environment of the brain by protecting the active functions of the central nervous system and preventing the invasion of microorganisms and toxins. Brain tumors, however, often cause degradation and dysfunction of this barrier, resulting in a heterogeneous increase in vascular permeability throughout the tumor mass and outside it. Thus, the characteristics of both the blood-brain and blood-brain tumor barriers hinder the vascular delivery of a variety of therapeutic substances to brain tumors. Recent developments in fluorescent visualization of brain tumors offer improvements in the extent of maximal safe resection, but many of these fluorescent agents must reach the tumor via the vasculature. As a result, these fluorescence-guided resection techniques are often limited by the extent of vascular permeability in tumor regions and by the failure to stain the full volume of tumor tissue. In this review, we describe the structure and function of both the blood-brain and blood-brain tumor barriers in the context of the current state of fluorescence-guided imaging of brain tumors. We discuss features of currently used techniques for fluorescence-guided brain tumor resection, with an emphasis on their interactions with the blood-brain and blood-tumor barriers. Finally, we discuss a selection of novel preclinical techniques that have the potential to enhance the delivery of therapeutics to brain tumors in spite of the barrier properties of the brain.

Copyright © 2020 Belykh, Shaffer, Lin, Byvaltsev, Preul and Chen.

Keywords: 5-aminolevulinic acid; blood-brain barrier; blood-tumor barrier; drug delivery; enhanced permeability and retention; fluorescein sodium; fluorescence-guided surgery; indocyanine green

References

  1. J Control Release. 2013 Nov 28;172(1):12-21 - PubMed
  2. World Neurosurg. 2014 Dec;82(6):1171-86 - PubMed
  3. Photodiagnosis Photodyn Ther. 2019 Sep;27:327-335 - PubMed
  4. Am J Pathol. 2004 Aug;165(2):601-8 - PubMed
  5. Expert Rev Neurother. 2015 May;15(5):477-91 - PubMed
  6. J Neurooncol. 2019 Feb;141(3):595-607 - PubMed
  7. Invest Ophthalmol Vis Sci. 1986 Jul;27(7):1107-14 - PubMed
  8. Cancer Res. 1997 Jul 1;57(13):2799-805 - PubMed
  9. Br J Neurosurg. 2018 Apr;32(2):141-148 - PubMed
  10. Expert Rev Anticancer Ther. 2016;16(1):71-81 - PubMed
  11. J Clin Neurosci. 2012 Dec;19(12):1611-6 - PubMed
  12. Genes Dev. 2003 Mar 1;17(5):545-80 - PubMed
  13. J Neurosurg. 2014 Jan;120(1):291 - PubMed
  14. Curr Pharm Biotechnol. 2011 Apr;12(4):647-55 - PubMed
  15. World Neurosurg. 2014 Jul-Aug;82(1-2):175-85 - PubMed
  16. Adv Exp Med Biol. 1993;331:273-84 - PubMed
  17. Acta Neuropathol. 2012 Dec;124(6):763-75 - PubMed
  18. J Neurosurg. 2013 Aug;119(2):427-33 - PubMed
  19. Front Surg. 2019 Aug 13;6:49 - PubMed
  20. Surg Neurol Int. 2016 Dec 12;7(Suppl 40):S995-S1003 - PubMed
  21. J Control Release. 2010 Mar 19;142(3):296-8 - PubMed
  22. J Pharmacol Exp Ther. 2002 May;301(2):507-12 - PubMed
  23. Neurosurg Clin N Am. 2019 Jan;30(1):85-93 - PubMed
  24. Pflugers Arch. 2017 Jan;469(1):123-134 - PubMed
  25. Neurosurg Focus. 2015 Mar;38(3):E10 - PubMed
  26. J Neurosurg. 2018 Apr 1;:1-10 - PubMed
  27. Biomed Opt Express. 2017 Oct 17;8(11):5040-5048 - PubMed
  28. Neurosurg Clin N Am. 2019 Jan;30(1):95-101 - PubMed
  29. Pflugers Arch. 2007 Jun;454(3):345-59 - PubMed
  30. Am J Physiol. 1970 Jul;219(1):270-4 - PubMed
  31. World J Surg Oncol. 2016 Aug 24;14(1):225 - PubMed
  32. Adv Drug Deliv Rev. 2011 Mar 18;63(3):136-51 - PubMed
  33. Neurosurgery. 1996 Feb;38(2):308-17 - PubMed
  34. Cancer Res. 1994 Sep 1;54(17):4564-8 - PubMed
  35. Eur Radiol. 2019 Apr;29(4):1893-1902 - PubMed
  36. Neurosurg Clin N Am. 2012 Jul;23(3):371-7 - PubMed
  37. Circ Res. 2007 Feb 2;100(2):158-73 - PubMed
  38. J Transl Med. 2008 Dec 18;6:80 - PubMed
  39. Pharm Res. 2013 Oct;30(10):2523-37 - PubMed
  40. J Pharmacol Exp Ther. 2016 Feb;356(2):267-75 - PubMed
  41. Front Neurosci. 2017 Feb 23;11:86 - PubMed
  42. Sci Rep. 2015 Jan 22;5:7958 - PubMed
  43. Theranostics. 2019 Feb 28;9(6):1752-1763 - PubMed
  44. Neurosurgery. 2015 Nov;77(5):663-73 - PubMed
  45. J Control Release. 2011 Dec 20;156(3):381-9 - PubMed
  46. Acta Oncol. 2014 Mar;53(3):405-13 - PubMed
  47. J Photochem Photobiol B. 1997 Jan;37(1-2):151-3 - PubMed
  48. Am J Physiol. 1985 May;248(5 Pt 2):H712-8 - PubMed
  49. Acta Neurochir (Wien). 2017 Feb;159(2):363-367 - PubMed
  50. Acta Neuropathol. 1983;59(1):1-10 - PubMed
  51. Surg Neurol. 1993 Dec;40(6):451-6 - PubMed
  52. J Neurosurg. 2015 Jun;122(6):1360-9 - PubMed
  53. Annu Rev Neurosci. 2007;30:235-58 - PubMed
  54. J Cell Biol. 2015 May 25;209(4):493-506 - PubMed
  55. Oncology (Williston Park). 2016 Nov 15;30(11):963, 966-7 - PubMed
  56. Neurosurg Focus. 2016 Mar;40(3):E11 - PubMed
  57. J Control Release. 2013 Nov 28;172(1):391 - PubMed
  58. Nature. 2010 Nov 25;468(7323):557-61 - PubMed
  59. J Neurooncol. 1994;20(2):121-39 - PubMed
  60. Br J Pharmacol. 2010 Mar;159(6):1339-53 - PubMed
  61. Biomaterials. 2017 May;126:31-38 - PubMed
  62. J Neurosurg. 2018 Dec 14;131(6):1974-1984 - PubMed
  63. Front Oncol. 2019 May 22;9:423 - PubMed
  64. Glia. 2013 Dec;61(12):1939-58 - PubMed
  65. Neuroimage. 2019 Feb 15;187:32-55 - PubMed
  66. Neurosurgery. 2019 Oct 1;85(4):E739-E746 - PubMed
  67. Int J Nanomedicine. 2017 Jul 28;12:5421-5431 - PubMed
  68. Drug Metab Dispos. 2008 Jul;36(7):1385-405 - PubMed
  69. Brain Res. 2019 Sep 1;1718:231-241 - PubMed
  70. Cell. 2015 Nov 19;163(5):1064-1078 - PubMed
  71. Clin Neurosurg. 2012;59:107-13 - PubMed
  72. Front Oncol. 2019 Jul 03;9:554 - PubMed
  73. Lancet Neurol. 2010 Sep;9(9):906-20 - PubMed
  74. Expert Opin Drug Deliv. 2016 Jul;13(7):963-75 - PubMed
  75. J Pharm Pharmacol. 2019 Sep;71(9):1370-1383 - PubMed
  76. Microvasc Res. 2009 Mar;77(2):166-73 - PubMed
  77. Mol Cancer Ther. 2013 Aug;12(8):1638-50 - PubMed
  78. Jpn J Cancer Res. 1998 Mar;89(3):307-14 - PubMed
  79. JAMA Otolaryngol Head Neck Surg. 2016 Apr;142(4):330-8 - PubMed
  80. J Neurosurg. 2018 May 1;:1-10 - PubMed
  81. Cancer Lett. 2016 Jan 1;370(1):153-64 - PubMed
  82. Methods Mol Biol. 2010;624:25-37 - PubMed
  83. Sci Rep. 2015 Aug 18;5:13298 - PubMed
  84. Proc Natl Acad Sci U S A. 1998 Apr 14;95(8):4607-12 - PubMed
  85. J Control Release. 2011 Jun 30;152(3):402-10 - PubMed
  86. Trends Cancer. 2015 Dec;1(4):252-265 - PubMed
  87. Neurosurgery. 1989 Oct;25(4):523-31; discussion 531-2 - PubMed
  88. J Neurosurg. 2018 Feb;128(2):380-390 - PubMed
  89. Sci Rep. 2018 Nov 30;8(1):17523 - PubMed
  90. Proc Soc Exp Biol Med. 1966 Aug-Sep;122(4):957-63 - PubMed
  91. Contemp Oncol (Pozn). 2018 Mar;22(1A):23-32 - PubMed
  92. J Cereb Blood Flow Metab. 2012 Nov;32(11):1959-72 - PubMed
  93. Theranostics. 2018 Mar 8;8(8):2134-2146 - PubMed
  94. Front Oncol. 2019 Sep 24;9:925 - PubMed
  95. Nat Rev Neurol. 2018 Mar;14(3):133-150 - PubMed
  96. Drug Deliv. 2016 Sep;23(7):2327-2337 - PubMed
  97. Ann Med Health Sci Res. 2012 Jul;2(2):191-8 - PubMed
  98. J Control Release. 2001 Jul 6;74(1-3):295-302 - PubMed
  99. Photochem Photobiol. 2010 Sep-Oct;86(5):1154-60 - PubMed
  100. Oper Neurosurg (Hagerstown). 2019 Jul 1;17(1):32-42 - PubMed
  101. Front Oncol. 2019 Oct 02;9:966 - PubMed
  102. J Neurooncol. 2019 Feb;141(3):479-486 - PubMed
  103. Arch Ophthalmol. 1993 Sep;111(9):1165-6 - PubMed
  104. Int J Mol Sci. 2015 Oct 28;16(10):25865-80 - PubMed
  105. J Neuropathol Exp Neurol. 2012 Sep;71(9):806-13 - PubMed
  106. J Neuroimmunol. 2001 Mar 1;114(1-2):168-72 - PubMed
  107. Front Oncol. 2019 Jul 17;9:620 - PubMed
  108. Theranostics. 2018 Feb 5;8(6):1481-1493 - PubMed
  109. Biochim Biophys Acta. 2006 Jul;1763(7):723-36 - PubMed
  110. Chem Soc Rev. 2019 Jun 4;48(11):2967-3014 - PubMed
  111. Cancer Res. 1986 Dec;46(12 Pt 1):6387-92 - PubMed
  112. World J Gastroenterol. 2015 Aug 7;21(29):8769-75 - PubMed
  113. Sci Rep. 2017 Feb 07;7:42070 - PubMed
  114. J Clin Pharmacol. 2011 May;51(5):672-8 - PubMed
  115. World Neurosurg. 2019 Jul;127:31-37 - PubMed
  116. J Photochem Photobiol B. 2004 Mar 19;74(1):29-38 - PubMed
  117. Nat Rev Neurosci. 2006 Jan;7(1):41-53 - PubMed
  118. NeuroRx. 2005 Jan;2(1):86-98 - PubMed
  119. Proc Natl Acad Sci U S A. 2018 Oct 2;115(40):E9429-E9438 - PubMed
  120. Microvasc Res. 1999 Nov;58(3):312-28 - PubMed
  121. Neurosurg Focus. 2014 Feb;36(2):E1 - PubMed
  122. Br J Neurosurg. 2015;29(6):850-8 - PubMed
  123. J Med Chem. 2006 Dec 28;49(26):7559-83 - PubMed
  124. Neuropharmacology. 2017 Jul 1;120:4-7 - PubMed
  125. Cold Spring Harb Perspect Biol. 2015 Jan 05;7(1):a020412 - PubMed
  126. J Neurosurg Pediatr. 2011 May;7(5):522-6 - PubMed
  127. Clin Neurol Neurosurg. 2018 Dec;175:57-60 - PubMed
  128. ACS Nano. 2019 Jan 22;13(1):386-398 - PubMed
  129. Biochem Biophys Res Commun. 2014 Jun 20;449(1):44-8 - PubMed
  130. J Neurosurg. 2011 Dec;115(6):1131-8 - PubMed
  131. Neuro Oncol. 2003 Apr;5(2):79-88 - PubMed
  132. Neurosurg Clin N Am. 2012 Jul;23(3):439-49 - PubMed
  133. J Surg Res. 2015 Feb;193(2):567-76 - PubMed
  134. J Biol Chem. 2003 Feb 7;278(6):4135-44 - PubMed
  135. J Pharmacol Exp Ther. 2008 Mar;324(3):1064-72 - PubMed
  136. Neurosurg Focus. 2014 Feb;36(2):E16 - PubMed
  137. Am J Physiol. 1999 Aug;277(2):C330-42 - PubMed
  138. Sci Rep. 2019 Jun 17;9(1):8666 - PubMed
  139. Pharm Res. 2003 Apr;20(4):537-44 - PubMed
  140. Front Neurosci. 2019 Jan 11;12:1019 - PubMed
  141. J Pharm Sci. 2014 Oct;103(10):3235-43 - PubMed
  142. Transl Stroke Res. 2011 Mar;2(1):106-11 - PubMed
  143. PLoS One. 2017 Jan 19;12(1):e0169292 - PubMed
  144. Drug Deliv. 2018 Nov;25(1):364-375 - PubMed
  145. Prog Exp Tumor Res. 1984;27:132-53 - PubMed
  146. Nat Rev Cancer. 2020 Jan;20(1):26-41 - PubMed
  147. Front Oncol. 2019 Sep 26;9:963 - PubMed
  148. Neurosurgery. 2019 Oct 1;85(4):E641-E649 - PubMed
  149. Int J Mol Sci. 2015 Oct 28;16(10):25912-33 - PubMed
  150. Cancer Manag Res. 2018 Oct 12;10:4325-4331 - PubMed
  151. J Neurosurg. 2018 Dec 21;131(6):1819-1828 - PubMed
  152. Glia. 2010 Jul;58(9):1094-103 - PubMed
  153. Photodiagnosis Photodyn Ther. 2013 Feb;10(1):42-50 - PubMed
  154. Clin Neurol Neurosurg. 2018 Sep;172:177-182 - PubMed
  155. Drug Resist Updat. 2015 Mar;19:1-12 - PubMed
  156. J Neurosurg. 1994 Dec;81(6):902-9 - PubMed
  157. Curr Protoc Neurosci. 2017 Apr 10;79:9.58.1-9.58.15 - PubMed
  158. Expert Opin Ther Targets. 2015;19(8):1059-72 - PubMed
  159. PLoS One. 2012;7(3):e33060 - PubMed
  160. Endothelium. 2008 Sep-Oct;15(5-6):254-64 - PubMed
  161. Photochem Photobiol. 2014 Sep-Oct;90(5):1136-43 - PubMed
  162. Clin Cancer Res. 2018 Jan 1;24(1):52-61 - PubMed
  163. NeuroRx. 2005 Jan;2(1):3-14 - PubMed
  164. Radiology. 2001 May;219(2):316-33 - PubMed
  165. Cancer Manag Res. 2012;4:325-34 - PubMed
  166. Nat Commun. 2018 Jul 25;9(1):2336 - PubMed
  167. Neuro Oncol. 2019 Nov 1;21(Suppl 5):v1-v100 - PubMed
  168. Neurosurgery. 1994 Nov;35(5):930-40; discussion 940-1 - PubMed
  169. Macromol Biosci. 2015 Nov;15(11):1571-85 - PubMed
  170. Nanomedicine (Lond). 2013 Dec;8(12):1913-25 - PubMed
  171. Biochem Biophys Res Commun. 2001 Jun 22;284(4):863-9 - PubMed
  172. Acta Neurochir (Wien). 2015 Dec;157(12):2199-200 - PubMed
  173. Clin Neurosurg. 2008;55:20-6 - PubMed
  174. World Neurosurg. 2017 Oct;106:120-130 - PubMed
  175. Acta Pharm Sin B. 2016 Jul;6(4):287-96 - PubMed
  176. Clin Cancer Res. 2012 Oct 15;18(20):5731-40 - PubMed
  177. Mol Aspects Med. 2013 Apr-Jun;34(2-3):95-107 - PubMed
  178. World Neurosurg. 2018 May;113:e51-e69 - PubMed
  179. J Surg Oncol. 2018 Aug;118(2):356-361 - PubMed
  180. J Neurosurg. 2009 Mar;110(3):583-8 - PubMed
  181. J Pharmacol Exp Ther. 2002 Jun;301(3):838-51 - PubMed
  182. J Clin Invest. 1960 Apr;39:592-600 - PubMed
  183. J Neurooncol. 2019 Feb;141(3):495-505 - PubMed
  184. PLoS One. 2019 May 13;14(5):e0216503 - PubMed
  185. Neuro Oncol. 2016 Jan;18(1):27-36 - PubMed
  186. Mol Cancer Ther. 2017 Dec;16(12):2902-2912 - PubMed
  187. Clin Chem. 1987 Jun;33(6):765-8 - PubMed
  188. Int J Nanomedicine. 2017 May 22;12:3899-3911 - PubMed
  189. Mol Pharm. 2018 Mar 5;15(3):911-922 - PubMed
  190. Nat Commun. 2014 Jun 19;5:4196 - PubMed
  191. Neurosurgery. 2011 Sep;69(3):668-76 - PubMed
  192. Photodiagnosis Photodyn Ther. 2012 Sep;9(3):204-14 - PubMed
  193. Neuron Glia Biol. 2006 Feb;2(1):39-49 - PubMed
  194. Photochem Photobiol. 2011 Nov-Dec;87(6):1419-26 - PubMed
  195. Am J Physiol. 1993 Sep;265(3 Pt 1):G445-52 - PubMed
  196. PLoS One. 2013 Apr 24;8(4):e61694 - PubMed
  197. ISRN Biochem. 2013 May 21;2013:238428 - PubMed
  198. Clin Pharmacol Ther. 2013 Dec;94(6):636-9 - PubMed
  199. J Neurochem. 2001 Mar;76(5):1597-600 - PubMed
  200. Nanomedicine. 2012 Feb;8(2):147-66 - PubMed
  201. Jpn J Clin Oncol. 2009 Nov;39(11):756-66 - PubMed
  202. Cancer. 1999 Oct 1;86(7):1347-53 - PubMed
  203. J Drug Target. 2003 Jan;11(1):45-52 - PubMed
  204. Expert Opin Drug Metab Toxicol. 2016 May;12(5):499-508 - PubMed
  205. ACS Nano. 2014 Feb 25;8(2):1231-42 - PubMed
  206. J Pharm Sci. 2003 Oct;92(10):2090-7 - PubMed
  207. Br J Neurosurg. 2018 Oct;32(5):528-535 - PubMed
  208. Curr Neurovasc Res. 2016;13(3):249-60 - PubMed
  209. Int J Nanomedicine. 2016 Oct 18;11:5381-5414 - PubMed
  210. Front Oncol. 2019 Aug 06;9:727 - PubMed
  211. J Neurochem. 2008 Aug;106(4):1534-44 - PubMed
  212. J Anat. 2002 Jun;200(6):541-8 - PubMed
  213. Nat Commun. 2018 May 18;9(1):1991 - PubMed
  214. Am J Physiol. 1994 Jun;266(6 Pt 1):G1108-22 - PubMed
  215. World J Otorhinolaryngol Head Neck Surg. 2015 Oct 23;1(1):11-16 - PubMed
  216. Exp Neurol. 1983 Feb;79(2):564-8 - PubMed
  217. Circ Res. 2017 Jan 6;120(1):179-206 - PubMed
  218. Curr Pharm Biotechnol. 2012 Sep;13(12):2380-7 - PubMed
  219. Fluids Barriers CNS. 2012 Nov 09;9(1):23 - PubMed
  220. Front Neurosci. 2014 Dec 03;8:392 - PubMed
  221. Front Surg. 2019 Jul 16;6:41 - PubMed
  222. J Pharm Sci. 2015 Sep;104(9):3092-100 - PubMed
  223. J Neurosurg. 2018 Sep 7;131(3):724-734 - PubMed
  224. Curr Pharm Des. 2008;14(16):1581-93 - PubMed
  225. Drug Discov Today. 2008 Dec;13(23-24):1099-106 - PubMed
  226. Cancer Res. 2015 Oct 15;75(20):4283-91 - PubMed
  227. Acta Neuropathol. 2007 Nov;114(5):443-58 - PubMed
  228. Cancer Res. 1987 Aug 15;47(16):4432-43 - PubMed
  229. Neurosurgery. 1999 Apr;44(4):732-40; discussion 740-1 - PubMed
  230. Acta Pharm Sin B. 2016 Jul;6(4):268-86 - PubMed
  231. Clin Cancer Res. 2007 Apr 15;13(8):2463-70 - PubMed
  232. Nat Rev Drug Discov. 2016 Apr;15(4):275-92 - PubMed
  233. Proc Natl Acad Sci U S A. 2002 Oct 1;99(20):12617-21 - PubMed
  234. Front Surg. 2019 Oct 01;6:56 - PubMed
  235. JAMA Neurol. 2018 Feb 1;75(2):246-254 - PubMed
  236. Nat Med. 2013 Dec;19(12):1584-96 - PubMed
  237. Int J Oncol. 2004 Jul;25(1):37-45 - PubMed
  238. Bioimpacts. 2016;6(4):225-248 - PubMed
  239. Invest Ophthalmol Vis Sci. 1998 Jun;39(7):1286-90 - PubMed
  240. J Neurooncol. 2019 Feb;141(3):477-478 - PubMed
  241. Cancer Cell. 2016 Apr 11;29(4):508-522 - PubMed
  242. Cancer Manag Res. 2012;4:309-23 - PubMed
  243. Neuro Oncol. 2000 Jan;2(1):45-59 - PubMed
  244. Nature. 2010 Nov 25;468(7323):562-6 - PubMed
  245. Adv Drug Deliv Rev. 2013 Jan;65(1):71-9 - PubMed
  246. Neuro Oncol. 2011 Aug;13(8):806-19 - PubMed
  247. Neurosurgery. 1980 Jul;7(1):44-52 - PubMed
  248. Front Neurol. 2019 Jun 11;10:549 - PubMed
  249. J Surg Oncol. 2011 Sep 1;104(3):323-32 - PubMed
  250. Surv Ophthalmol. 2000 Jul-Aug;45(1):15-27 - PubMed
  251. Int J Oncol. 2007 Dec;31(6):1539-45 - PubMed
  252. Am J Physiol. 1972 Aug;223(2):323-31 - PubMed
  253. J Control Release. 2016 Aug 10;235:34-47 - PubMed
  254. Adv Drug Deliv Rev. 2007 Jul 10;59(6):454-77 - PubMed
  255. Neurosurgery. 2016 Dec;79(6):856-871 - PubMed
  256. J Clin Invest. 1998 Jun 15;101(12):2761-7 - PubMed
  257. Neurosurg Focus. 2016 Mar;40(3):E8 - PubMed
  258. Front Oncol. 2019 Jul 18;9:583 - PubMed
  259. Microcirculation. 2016 Apr;23(3):173-82 - PubMed
  260. J Photochem Photobiol B. 1997 Oct;40(3):313-9 - PubMed
  261. Chem Sci. 2017 Aug 1;8(8):5371-5384 - PubMed
  262. Clin Cancer Res. 2017 May 1;23(9):2203-2212 - PubMed
  263. J Neurooncol. 2019 Oct;145(1):75-83 - PubMed
  264. J Oncol. 2019 Jul 22;2019:9342796 - PubMed
  265. Toxicol Sci. 2013 Dec;136(2):328-43 - PubMed
  266. PLoS One. 2017 Jan 3;12(1):e0166061 - PubMed
  267. J Neurochem. 2002 Apr;81(1):203-6 - PubMed
  268. Neurophotonics. 2017 Jan;4(1):011010 - PubMed
  269. Clin Transl Med. 2018 Mar 1;7(1):11 - PubMed
  270. Neurosurgery. 2009 Mar;64(3 Suppl):ons53-60; discussion ons60-1 - PubMed
  271. Am J Pathol. 2012 Oct;181(4):1126-41 - PubMed
  272. J Neurosurg. 2019 May 10;:1-10 - PubMed

Publication Types