MR-guided focused ultrasound liquid biopsy enriches circulating biomarkers in patients with brain tumors.


Journal

Neuro-oncology
ISSN: 1523-5866
Titre abrégé: Neuro Oncol
Pays: England
ID NLM: 100887420

Informations de publication

Date de publication:
01 10 2021
Historique:
pubmed: 12 3 2021
medline: 6 10 2021
entrez: 11 3 2021
Statut: ppublish

Résumé

Liquid biopsy is promising for early detection, monitoring of response, and recurrence of cancer. The blood-brain barrier (BBB) limits the shedding of biomarker, such as cell-free DNA (cfDNA), into the blood from brain tumors, and their detection by conventional assays. Transcranial MR-guided focused ultrasound (MRgFUS) can safely and transiently open the BBB, providing an opportunity for less-invasive access to brain pathology. We hypothesized that MRgFUS can enrich the signal of circulating brain-derived biomarkers to aid in liquid biopsy. Nine patients were treated in a prospective single-arm, open-label trial to investigate serial MRgFUS and adjuvant temozolomide combination in patients with glioblastoma (NCT03616860). Blood samples were collected as an exploratory measure within the hours before and after sonication, with control samples from non-brain tumor patients undergoing BBB opening (BBBO) alone (NCT03739905). Brain regions averaging 7.8 ± 6.0 cm3 (range 0.8-23.1 cm3) were successfully treated within 111 ± 39 minutes without any serious adverse events. We found MRgFUS acutely enhanced plasma cfDNA (2.6 ± 1.2-fold, P < .01, Wilcoxon signed-rank test), neuron-derived extracellular vesicles (3.2 ± 1.9-fold, P < .01), and brain-specific protein S100b (1.4 ± 0.2-fold, P < .01). Further comparison of the cfDNA methylation profiles suggests a signature that is disease- and post-BBBO-specific, in keeping with our hypothesis. We also found cfDNA-mutant copies of isocitrate dehydrogenase 1 (IDH1) increased, although this was in only one patient known to harbor the tumor mutation. This first-in-human proof-of-concept study shows MRgFUS enriches the signal of circulating brain-derived biomarkers, demonstrating the potential of the technology to support liquid biopsy for the brain.

Sections du résumé

BACKGROUND
Liquid biopsy is promising for early detection, monitoring of response, and recurrence of cancer. The blood-brain barrier (BBB) limits the shedding of biomarker, such as cell-free DNA (cfDNA), into the blood from brain tumors, and their detection by conventional assays. Transcranial MR-guided focused ultrasound (MRgFUS) can safely and transiently open the BBB, providing an opportunity for less-invasive access to brain pathology. We hypothesized that MRgFUS can enrich the signal of circulating brain-derived biomarkers to aid in liquid biopsy.
METHODS
Nine patients were treated in a prospective single-arm, open-label trial to investigate serial MRgFUS and adjuvant temozolomide combination in patients with glioblastoma (NCT03616860). Blood samples were collected as an exploratory measure within the hours before and after sonication, with control samples from non-brain tumor patients undergoing BBB opening (BBBO) alone (NCT03739905).
RESULTS
Brain regions averaging 7.8 ± 6.0 cm3 (range 0.8-23.1 cm3) were successfully treated within 111 ± 39 minutes without any serious adverse events. We found MRgFUS acutely enhanced plasma cfDNA (2.6 ± 1.2-fold, P < .01, Wilcoxon signed-rank test), neuron-derived extracellular vesicles (3.2 ± 1.9-fold, P < .01), and brain-specific protein S100b (1.4 ± 0.2-fold, P < .01). Further comparison of the cfDNA methylation profiles suggests a signature that is disease- and post-BBBO-specific, in keeping with our hypothesis. We also found cfDNA-mutant copies of isocitrate dehydrogenase 1 (IDH1) increased, although this was in only one patient known to harbor the tumor mutation.
CONCLUSIONS
This first-in-human proof-of-concept study shows MRgFUS enriches the signal of circulating brain-derived biomarkers, demonstrating the potential of the technology to support liquid biopsy for the brain.

Identifiants

pubmed: 33693781
pii: 6167330
doi: 10.1093/neuonc/noab057
pmc: PMC8485448
doi:

Substances chimiques

Biomarkers 0

Banques de données

ClinicalTrials.gov
['NCT03739905', 'NCT03616860']

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

1789-1797

Commentaires et corrections

Type : CommentIn

Informations de copyright

© The Author(s) 2021. Published by Oxford University Press on behalf of the Society for Neuro-Oncology.

Références

Sci Transl Med. 2016 Jun 15;8(343):343re2
pubmed: 27306666
N Engl J Med. 2013 Mar 28;368(13):1199-209
pubmed: 23484797
Proc Natl Acad Sci U S A. 2006 Aug 1;103(31):11719-23
pubmed: 16868082
Neuroimage. 2005 Jan 1;24(1):12-20
pubmed: 15588592
NPJ Genom Med. 2018 Nov 23;3:31
pubmed: 30479833
Nature. 2018 Mar 22;555(7697):469-474
pubmed: 29539639
Neuro Oncol. 2016 Jul;18(7):974-81
pubmed: 26819443
Cancer Med. 2017 Oct;6(10):2194-2202
pubmed: 28834325
Nat Rev Neurol. 2021 Jan;17(1):7-22
pubmed: 33106619
Sci Rep. 2018 Apr 26;8(1):6553
pubmed: 29700310
N Engl J Med. 2008 Jul 24;359(4):366-77
pubmed: 18596266
Ultrasound Med Biol. 2007 Apr;33(4):584-90
pubmed: 17337109
Nature. 2018 Nov;563(7732):579-583
pubmed: 30429608
Neurosurgery. 2017 Sep 1;64(CN_suppl_1):134-138
pubmed: 28899049
Nat Commun. 2019 Sep 26;10(1):4373
pubmed: 31558719
Nat Rev Cancer. 2020 Jan;20(1):26-41
pubmed: 31601988
Front Neurosci. 2017 May 22;11:278
pubmed: 28588440
Clin Cancer Res. 2019 Jul 1;25(13):3793-3801
pubmed: 30890548
Nat Commun. 2018 Jul 25;9(1):2336
pubmed: 30046032
Sci Rep. 2019 Jan 23;9(1):321
pubmed: 30674905
Sci Rep. 2020 May 4;10(1):7449
pubmed: 32366915

Auteurs

Ying Meng (Y)

Sunnybrook Research Institute, Toronto, Ontario, Canada.
Division of Neurosurgery, Department of Surgery, University of Toronto, Toronto, Ontario, Canada.

Christopher B Pople (CB)

Sunnybrook Research Institute, Toronto, Ontario, Canada.

Suganth Suppiah (S)

Division of Neurosurgery, Department of Surgery, University of Toronto, Toronto, Ontario, Canada.

Maheleth Llinas (M)

Sunnybrook Research Institute, Toronto, Ontario, Canada.

Yuexi Huang (Y)

Sunnybrook Research Institute, Toronto, Ontario, Canada.

Arjun Sahgal (A)

Sunnybrook Research Institute, Toronto, Ontario, Canada.
Odette Cancer Centre, Sunnybrook Health Sciences Centre, Toronto, Ontario, Canada.
Department of Radiation Oncology, Faculty of Medicine, University of Toronto, Toronto, Ontario, Canada.

James Perry (J)

Sunnybrook Research Institute, Toronto, Ontario, Canada.
Odette Cancer Centre, Sunnybrook Health Sciences Centre, Toronto, Ontario, Canada.
Division of Neurology, Department of Medicine, University of Toronto, Toronto, Ontario, Canada.

Julia Keith (J)

Sunnybrook Research Institute, Toronto, Ontario, Canada.
Department of Laboratory Medicine and Pathobiology, University of Toronto, Toronto, Ontario, Canada.

Benjamin Davidson (B)

Sunnybrook Research Institute, Toronto, Ontario, Canada.
Division of Neurosurgery, Department of Surgery, University of Toronto, Toronto, Ontario, Canada.

Clement Hamani (C)

Sunnybrook Research Institute, Toronto, Ontario, Canada.
Division of Neurosurgery, Department of Surgery, University of Toronto, Toronto, Ontario, Canada.

Yutaka Amemiya (Y)

Sunnybrook Research Institute, Toronto, Ontario, Canada.

Arun Seth (A)

Sunnybrook Research Institute, Toronto, Ontario, Canada.
Department of Laboratory Medicine and Pathobiology, University of Toronto, Toronto, Ontario, Canada.

Hon Leong (H)

Sunnybrook Research Institute, Toronto, Ontario, Canada.
Department of Medical Biophysics, University of Toronto, Toronto, Ontario, Canada.

Chinthaka C Heyn (CC)

Sunnybrook Research Institute, Toronto, Ontario, Canada.
Department of Medical Imaging, Sunnybrook Health Sciences Centre, University of Toronto, Toronto, Ontario, Canada.

Isabelle Aubert (I)

Sunnybrook Research Institute, Toronto, Ontario, Canada.
Department of Laboratory Medicine and Pathobiology, University of Toronto, Toronto, Ontario, Canada.

Kullervo Hynynen (K)

Sunnybrook Research Institute, Toronto, Ontario, Canada.
Department of Medical Biophysics, University of Toronto, Toronto, Ontario, Canada.

Nir Lipsman (N)

Sunnybrook Research Institute, Toronto, Ontario, Canada.
Division of Neurosurgery, Department of Surgery, University of Toronto, Toronto, Ontario, Canada.

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