Focused Ultrasound-Induced Blood–Brain Barrier Opening to Enhance Temozolomide Delivery for Glioblastoma Treatment: A Preclinical Study

The purpose of this study is to assess the preclinical therapeutic efficacy of magnetic resonance imaging (MRI)-monitored focused ultrasound (FUS)-induced blood-brain barrier (BBB) disruption to enhance Temozolomide (TMZ) delivery for improving Glioblastoma Multiforme (GBM) treatment. MRI-monitored...

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Published inPloS one Vol. 8; no. 3; p. e58995
Main Authors Wei, Kuo-Chen, Chu, Po-Chun, Wang, Hay-Yan Jack, Huang, Chiung-Yin, Chen, Pin-Yuan, Tsai, Hong-Chieh, Lu, Yu-Jen, Lee, Pei-Yun, Tseng, I-Chou, Feng, Li-Ying, Hsu, Peng-Wei, Yen, Tzu-Chen, Liu, Hao-Li
Format Journal Article
LanguageEnglish
Published United States Public Library of Science 19.03.2013
Public Library of Science (PLoS)
Subjects
Animal tissues
Animals
Antineoplastic Agents, Alkylating - pharmacokinetics
Antineoplastic Agents, Alkylating - therapeutic use
Biology
Blood-brain barrier
Blood-Brain Barrier - metabolism
Blood-Brain Barrier - radiation effects
Brain
Brain - pathology
Brain cancer
Brain Neoplasms - diagnosis
Brain Neoplasms - drug therapy
Brain Neoplasms - mortality
Brain research
Brain tumors
Cancer therapies
Cell Line, Tumor
Cerebrospinal fluid
Chemotherapy
Clinical trials
Dacarbazine - analogs & derivatives
Dacarbazine - pharmacokinetics
Dacarbazine - therapeutic use
Development and progression
Disease Models, Animal
Drug Evaluation, Preclinical
Dyes
Electrical engineering
Engineering
Glioblastoma
Glioblastoma - diagnosis
Glioblastoma - drug therapy
Glioblastoma - mortality
Glioblastoma multiforme
Glioblastomas
Glioma cells
Health aspects
Histology
Magnetic resonance
Magnetic Resonance Imaging
Male
Medical imaging
Medicine
Molecular weight
Neuroimaging
Neurosurgery
NMR
Nuclear magnetic resonance
Parenchyma
Permeability
Rats
Sound
Spectrophotometry
Survival
Temozolomide
Tumors
Ultrasonic imaging
Ultrasound
United States > US
Taiwan
Online AccessGet full text

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Abstract The purpose of this study is to assess the preclinical therapeutic efficacy of magnetic resonance imaging (MRI)-monitored focused ultrasound (FUS)-induced blood-brain barrier (BBB) disruption to enhance Temozolomide (TMZ) delivery for improving Glioblastoma Multiforme (GBM) treatment. MRI-monitored FUS with microbubbles was used to transcranially disrupt the BBB in brains of Fisher rats implanted with 9L glioma cells. FUS-BBB opening was spectrophotometrically determined by leakage of dyes into the brain, and TMZ was quantitated in cerebrospinal fluid (CSF) and plasma by LC-MS\MS. The effects of treatment on tumor progression (by MRI), animal survival and brain tissue histology were investigated. Results demonstrated that FUS-BBB opening increased the local accumulation of dyes in brain parenchyma by 3.8-/2.1-fold in normal/tumor tissues. Compared to TMZ alone, combined FUS treatment increased the TMZ CSF/plasma ratio from 22.7% to 38.6%, reduced the 7-day tumor progression ratio from 24.03 to 5.06, and extended the median survival from 20 to 23 days. In conclusion, this study provided preclinical evidence that FUS BBB-opening increased the local concentration of TMZ to improve the control of tumor progression and animal survival, suggesting its clinical potential for improving current brain tumor treatment.
AbstractList The purpose of this study is to assess the preclinical therapeutic efficacy of magnetic resonance imaging (MRI)-monitored focused ultrasound (FUS)-induced blood-brain barrier (BBB) disruption to enhance Temozolomide (TMZ) delivery for improving Glioblastoma Multiforme (GBM) treatment. MRI-monitored FUS with microbubbles was used to transcranially disrupt the BBB in brains of Fisher rats implanted with 9L glioma cells. FUS-BBB opening was spectrophotometrically determined by leakage of dyes into the brain, and TMZ was quantitated in cerebrospinal fluid (CSF) and plasma by LC-MS\MS. The effects of treatment on tumor progression (by MRI), animal survival and brain tissue histology were investigated. Results demonstrated that FUS-BBB opening increased the local accumulation of dyes in brain parenchyma by 3.8-/2.1-fold in normal/tumor tissues. Compared to TMZ alone, combined FUS treatment increased the TMZ CSF/plasma ratio from 22.7% to 38.6%, reduced the 7-day tumor progression ratio from 24.03 to 5.06, and extended the median survival from 20 to 23 days. In conclusion, this study provided preclinical evidence that FUS BBB-opening increased the local concentration of TMZ to improve the control of tumor progression and animal survival, suggesting its clinical potential for improving current brain tumor treatment.
The purpose of this study is to assess the preclinical therapeutic efficacy of magnetic resonance imaging (MRI)-monitored focused ultrasound (FUS)-induced blood-brain barrier (BBB) disruption to enhance Temozolomide (TMZ) delivery for improving Glioblastoma Multiforme (GBM) treatment. MRI-monitored FUS with microbubbles was used to transcranially disrupt the BBB in brains of Fisher rats implanted with 9L glioma cells. FUS-BBB opening was spectrophotometrically determined by leakage of dyes into the brain, and TMZ was quantitated in cerebrospinal fluid (CSF) and plasma by LC-MS\MS. The effects of treatment on tumor progression (by MRI), animal survival and brain tissue histology were investigated. Results demonstrated that FUS-BBB opening increased the local accumulation of dyes in brain parenchyma by 3.8-/2.1-fold in normal/tumor tissues. Compared to TMZ alone, combined FUS treatment increased the TMZ CSF/plasma ratio from 22.7% to 38.6%, reduced the 7-day tumor progression ratio from 24.03 to 5.06, and extended the median survival from 20 to 23 days. In conclusion, this study provided preclinical evidence that FUS BBB-opening increased the local concentration of TMZ to improve the control of tumor progression and animal survival, suggesting its clinical potential for improving current brain tumor treatment.The purpose of this study is to assess the preclinical therapeutic efficacy of magnetic resonance imaging (MRI)-monitored focused ultrasound (FUS)-induced blood-brain barrier (BBB) disruption to enhance Temozolomide (TMZ) delivery for improving Glioblastoma Multiforme (GBM) treatment. MRI-monitored FUS with microbubbles was used to transcranially disrupt the BBB in brains of Fisher rats implanted with 9L glioma cells. FUS-BBB opening was spectrophotometrically determined by leakage of dyes into the brain, and TMZ was quantitated in cerebrospinal fluid (CSF) and plasma by LC-MS\MS. The effects of treatment on tumor progression (by MRI), animal survival and brain tissue histology were investigated. Results demonstrated that FUS-BBB opening increased the local accumulation of dyes in brain parenchyma by 3.8-/2.1-fold in normal/tumor tissues. Compared to TMZ alone, combined FUS treatment increased the TMZ CSF/plasma ratio from 22.7% to 38.6%, reduced the 7-day tumor progression ratio from 24.03 to 5.06, and extended the median survival from 20 to 23 days. In conclusion, this study provided preclinical evidence that FUS BBB-opening increased the local concentration of TMZ to improve the control of tumor progression and animal survival, suggesting its clinical potential for improving current brain tumor treatment.
Audience Academic
Author Tsai, Hong-Chieh
Feng, Li-Ying
Tseng, I-Chou
Wei, Kuo-Chen
Lu, Yu-Jen
Liu, Hao-Li
Yen, Tzu-Chen
Chen, Pin-Yuan
Hsu, Peng-Wei
Lee, Pei-Yun
Huang, Chiung-Yin
Wang, Hay-Yan Jack
Chu, Po-Chun
AuthorAffiliation 3 Department of Biological Sciences, National Sun Yat-sen University, Kaohsiung, Taiwan
1 Department of Neurosurgery, Chang-Gung University and Memorial Hospital, Taoyuan, Taiwan
2 Department of Electrical Engineering, Chang-Gung University, Taoyuan, Taiwan
4 Department of Nuclear Medicine and Molecular Imaging Center, Chang-Gung University and Memorial Hospital, Taoyuan, Taiwan
The Ohio State University, United States of America
5 Healthy Aging Research Center, Chang-Gung University, Taoyuan, Taiwan
AuthorAffiliation_xml – name: The Ohio State University, United States of America
– name: 3 Department of Biological Sciences, National Sun Yat-sen University, Kaohsiung, Taiwan
– name: 1 Department of Neurosurgery, Chang-Gung University and Memorial Hospital, Taoyuan, Taiwan
– name: 4 Department of Nuclear Medicine and Molecular Imaging Center, Chang-Gung University and Memorial Hospital, Taoyuan, Taiwan
– name: 5 Healthy Aging Research Center, Chang-Gung University, Taoyuan, Taiwan
– name: 2 Department of Electrical Engineering, Chang-Gung University, Taoyuan, Taiwan
Author_xml – sequence: 1
  givenname: Kuo-Chen
  surname: Wei
  fullname: Wei, Kuo-Chen
– sequence: 2
  givenname: Po-Chun
  surname: Chu
  fullname: Chu, Po-Chun
– sequence: 3
  givenname: Hay-Yan Jack
  surname: Wang
  fullname: Wang, Hay-Yan Jack
– sequence: 4
  givenname: Chiung-Yin
  surname: Huang
  fullname: Huang, Chiung-Yin
– sequence: 5
  givenname: Pin-Yuan
  surname: Chen
  fullname: Chen, Pin-Yuan
– sequence: 6
  givenname: Hong-Chieh
  surname: Tsai
  fullname: Tsai, Hong-Chieh
– sequence: 7
  givenname: Yu-Jen
  surname: Lu
  fullname: Lu, Yu-Jen
– sequence: 8
  givenname: Pei-Yun
  surname: Lee
  fullname: Lee, Pei-Yun
– sequence: 9
  givenname: I-Chou
  surname: Tseng
  fullname: Tseng, I-Chou
– sequence: 10
  givenname: Li-Ying
  surname: Feng
  fullname: Feng, Li-Ying
– sequence: 11
  givenname: Peng-Wei
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  fullname: Hsu, Peng-Wei
– sequence: 12
  givenname: Tzu-Chen
  surname: Yen
  fullname: Yen, Tzu-Chen
– sequence: 13
  givenname: Hao-Li
  surname: Liu
  fullname: Liu, Hao-Li
BackLink https://www.ncbi.nlm.nih.gov/pubmed/23527068$$D View this record in MEDLINE/PubMed
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Copyright COPYRIGHT 2013 Public Library of Science
2013 Wei et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License: https://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.
2013 Wei et al 2013 Wei et al
Copyright_xml – notice: COPYRIGHT 2013 Public Library of Science
– notice: 2013 Wei et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License: https://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.
– notice: 2013 Wei et al 2013 Wei et al
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Conceived and designed the experiments: KCW PCC HYJW CYH PYC HCT YJL ICT PYL TCY HLL; Performed the experiments: PCC HYJW CYH PYC HCT YJL ICT PYL TCY. Analyzed the data: HYJW CYH YJL ICT PYL TCY. Contributed reagents/materials/analysis tools: PCC HYJW CYH PYC HCT YJL ICT PYL. Wrote the paper: KCW PCC HYJW CYH HLL.
Competing Interests: The authors have declared that no competing interests exist.
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Snippet The purpose of this study is to assess the preclinical therapeutic efficacy of magnetic resonance imaging (MRI)-monitored focused ultrasound (FUS)-induced...
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SubjectTerms Animal tissues
Animals
Antineoplastic Agents, Alkylating - pharmacokinetics
Antineoplastic Agents, Alkylating - therapeutic use
Biology
Blood-brain barrier
Blood-Brain Barrier - metabolism
Blood-Brain Barrier - radiation effects
Brain
Brain - pathology
Brain cancer
Brain Neoplasms - diagnosis
Brain Neoplasms - drug therapy
Brain Neoplasms - mortality
Brain research
Brain tumors
Cancer therapies
Cell Line, Tumor
Cerebrospinal fluid
Chemotherapy
Clinical trials
Dacarbazine - analogs & derivatives
Dacarbazine - pharmacokinetics
Dacarbazine - therapeutic use
Development and progression
Disease Models, Animal
Drug Evaluation, Preclinical
Dyes
Electrical engineering
Engineering
Glioblastoma
Glioblastoma - diagnosis
Glioblastoma - drug therapy
Glioblastoma - mortality
Glioblastoma multiforme
Glioblastomas
Glioma cells
Health aspects
Histology
Magnetic resonance
Magnetic Resonance Imaging
Male
Medical imaging
Medicine
Molecular weight
Neuroimaging
Neurosurgery
NMR
Nuclear magnetic resonance
Parenchyma
Permeability
Rats
Sound
Spectrophotometry
Survival
Temozolomide
Tumors
Ultrasonic imaging
Ultrasound
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Title Focused Ultrasound-Induced Blood–Brain Barrier Opening to Enhance Temozolomide Delivery for Glioblastoma Treatment: A Preclinical Study
URI https://www.ncbi.nlm.nih.gov/pubmed/23527068
https://www.proquest.com/docview/1330889305
https://www.proquest.com/docview/1319615610
https://pubmed.ncbi.nlm.nih.gov/PMC3602591
https://doaj.org/article/2251bf4aef264ebfbba1da2637ad6b04
http://dx.doi.org/10.1371/journal.pone.0058995
Volume 8
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