Miniature fluorescence sensor for quantitative detection of brain tumour

Ndabakuranye, Jean Pierre; Belcourt, James; Sharma, Deepak; O'Connell, Cathal D.; Mondal, Victor; Srivastava, Sanjay K.; Stacey, Alastair; Long, Sam; Fleiss, Bobbi; Ahnood, Arman

doi:10.1039/d3lc00982c

Miniature fluorescence sensor for quantitative detection of brain tumour

Journal Article · Thu Jan 25 23:00:00 EST 2024 · Lab on a Chip

DOI:https://doi.org/10.1039/d3lc00982c· OSTI ID:2326054

^[1]; ^[1]; ^[2]; O'Connell, Cathal D. ^[3]; Mondal, Victor ^[1]; ^[4]; Stacey, Alastair ^[5]; Long, Sam ^[6]; ^[1]; ^[1]

Royal Melbourne Institute of Technology (RMIT), VIC (Australia)
Royal Melbourne Institute of Technology (RMIT), VIC (Australia); National Physical Laboratory (CSIR), New Delhi (India); Academy of Scientific and Innovative Research (AcSIR), Ghaziabad (India)
Royal Melbourne Institute of Technology (RMIT), VIC (Australia); St. Vincent's Hospital Melbourne, VIC (Australia)
National Physical Laboratory (CSIR), New Delhi (India); Academy of Scientific and Innovative Research (AcSIR), Ghaziabad (India)
Royal Melbourne Institute of Technology (RMIT), VIC (Australia); Princeton Plasma Physics Laboratory (PPPL), Princeton, NJ (United States)
Veterinary Referral Hospital, Victoria (Australia)

Fluorescence-guided surgery has emerged as a vital tool for tumour resection procedures. As well as intraoperative tumour visualisation, 5-ALA-induced PpIX provides an avenue for quantitative tumour identification based on ratiometric fluorescence measurement. To this end, fluorescence imaging and fibre-based probes have enabled more precise demarcation between the cancerous and healthy tissues. These sensing approaches, which rely on collecting the fluorescence light from the tumour resection site and its “remote” spectral sensing, introduce challenges associated with optical losses. In this work, we demonstrate the viability of tumour detection at the resection site using a miniature fluorescence measurement system. Unlike the current bulky systems, which necessitate remote measurement, we have adopted a millimetre-sized spectral sensor chip for quantitative fluorescence measurements. A reliable measurement at the resection site requires a stable optical window between the tissue and the optoelectronic system. This is achieved using an antifouling diamond window, which provides stable optical transparency. The system achieved a sensitivity of 92.3% and specificity of 98.3% in detecting a surrogate tumour at a resolution of 1 × 1 mm². In conclusion, as well as addressing losses associated with collecting and coupling fluorescence light in the current ‘remote’ sensing approaches, the small size of the system introduced in this work paves the way for its direct integration with the tumour resection tools with the aim of more accurate interoperative tumour identification.

View Accepted Manuscript (DOE)

Research Organization:: Princeton Plasma Physics Laboratory (PPPL), Princeton, NJ (United States)

Sponsoring Organization:: USDOE; Australian Research Council (ARC)

Grant/Contract Number:: AC02-09CH11466

OSTI ID:: 2326054

Journal Information:: Lab on a Chip, Journal Name: Lab on a Chip Journal Issue: 4 Vol. 24; ISSN 1473-0197

Publisher:: Royal Society of ChemistryCopyright Statement

Country of Publication:: United States

Language:: English

References (54)

Association of the Extent of Resection With Survival in Glioblastoma Brown, Timothy J.; Brennan, Matthew C.; Li, Michael JAMA Oncology, Vol. 2, Issue 11 https://doi.org/10.1001/jamaoncol.2016.1373	journal	November 2016
Laser Driven Miniature Diamond Implant for Wireless Retinal Prostheses Ahnood, Arman; Cheriton, Ross; Bruneau, Anne Advanced Biosystems, Vol. 4, Issue 11 https://doi.org/10.1002/adbi.202000055	journal	October 2020
Slippery quartz surfaces for anti‐fouling optical windows Li, Minjing; Yang, Tongzhen; Yang, Qing Droplet, Vol. 2, Issue 1 https://doi.org/10.1002/dro2.41	journal	December 2022
Multimodal imaging to explore endogenous fluorescence of fresh and fixed human healthy and tumor brain tissues Mehidine, Hussein; Sibai, Mira; Poulon, Fanny Journal of Biophotonics, Vol. 12, Issue 3 https://doi.org/10.1002/jbio.201800178	journal	October 2018
Widefield fluorescence lifetime imaging of protoporphyrin IX for fluorescence‐guided neurosurgery: An ex vivo feasibility study Erkkilä, Mikael T.; Bauer, Bianca; Hecker‐Denschlag, Nancy Journal of Biophotonics, Vol. 12, Issue 6 https://doi.org/10.1002/jbio.201800378	journal	February 2019
A multispectral fluorescence imaging system: Design and initial clinical tests in intra‐operative Photofrin‐photodynamic therapy of brain tumors Yang, Victor X. D.; Muller, Paul J.; Herman, Peter Lasers in Surgery and Medicine, Vol. 32, Issue 3 https://doi.org/10.1002/lsm.10131	journal	February 2003
Optical touch pointer for fluorescence guided glioblastoma resection using 5‐aminolevulinic acid Haj‐Hosseini, Neda; Richter, Johan; Andersson‐Engels, Stefan Lasers in Surgery and Medicine, Vol. 42, Issue 1 https://doi.org/10.1002/lsm.20868	journal	January 2010
Time course of neurological deficits after surgery for primary brain tumours Zetterling, Maria; Elf, Kristin; Semnic, Robert Acta Neurochirurgica, Vol. 162, Issue 12 https://doi.org/10.1007/s00701-020-04425-3	journal	July 2020
Fluorescence Photodiagnostics and Photobleaching Studies of Cancerous Lesions using Ratio Imaging and Spectroscopic Techniques Scott, M. A.; Hopper, C.; Sahota, A. Lasers in Medical Science, Vol. 15, Issue 1 https://doi.org/10.1007/s101030050049	journal	January 2000
Visualization technologies for 5-ALA-based fluorescence-guided surgeries Wei, Linpeng; Roberts, David W.; Sanai, Nader Journal of Neuro-Oncology, Vol. 141, Issue 3 https://doi.org/10.1007/s11060-018-03077-9	journal	December 2018
The friction of diamond-like carbon coatings in a water environment Sutton, D. C.; Limbert, G.; Stewart, D. Friction, Vol. 1, Issue 3 https://doi.org/10.1007/s40544-013-0023-1	journal	September 2013
Friction and wear properties of diamonds and diamond coatings Hayward, I. P. Surface and Coatings Technology, Vol. 49, Issue 1-3 https://doi.org/10.1016/0257-8972(91)90116-E	journal	December 1991
Control wettability of the hydrogen-terminated diamond surface and the oxidized diamond surface using an atomic force microscope Kaibara, Yu; Sugata, Kenta; Tachiki, Minoru Diamond and Related Materials, Vol. 12, Issue 3-7 https://doi.org/10.1016/S0925-9635(02)00373-4	journal	March 2003
In vitro and in vivo porphyrin accumulation by C6 glioma cells after exposure to 5-aminolevulinic acid Stummer, Walter; Stocker, Susanne; Novotny, Alexander Journal of Photochemistry and Photobiology B: Biology, Vol. 45, Issue 2-3 https://doi.org/10.1016/S1011-1344(98)00176-6	journal	September 1998
Fluorescence-guided surgery with 5-aminolevulinic acid for resection of malignant glioma: a randomised controlled multicentre phase III trial Stummer, Walter; Pichlmeier, Uwe; Meinel, Thomas The Lancet Oncology, Vol. 7, Issue 5 https://doi.org/10.1016/S1470-2045(06)70665-9	journal	May 2006
Postoperative stereotactic radiosurgery compared with whole brain radiotherapy for resected metastatic brain disease (NCCTG N107C/CEC·3): a multicentre, randomised, controlled, phase 3 trial Brown, Paul D.; Ballman, Karla V.; Cerhan, Jane H. The Lancet Oncology, Vol. 18, Issue 8 https://doi.org/10.1016/S1470-2045(17)30441-2	journal	August 2017
Real-time fluorescence imaging in intraoperative decision making for cancer surgery Lauwerends, Lorraine J.; van Driel, Pieter B. A. A.; Baatenburg de Jong, Robert J. The Lancet Oncology, Vol. 22, Issue 5 https://doi.org/10.1016/S1470-2045(20)30600-8	journal	May 2021
Lessons from brain mapping in surgery for low-grade glioma: insights into associations between tumour and brain plasticity Duffau, Hugues The Lancet Neurology, Vol. 4, Issue 8 https://doi.org/10.1016/S1474-4422(05)70140-X	journal	August 2005
Patterned hydrophobic and hydrophilic surfaces of ultra-smooth nanocrystalline diamond layers Mertens, M.; Mohr, M.; Brühne, K. Applied Surface Science, Vol. 390 https://doi.org/10.1016/j.apsusc.2016.08.130	journal	December 2016
Diamond encapsulated photovoltaics for transdermal power delivery Ahnood, A.; Fox, K. E.; Apollo, N. V. Biosensors and Bioelectronics, Vol. 77 https://doi.org/10.1016/j.bios.2015.10.022	journal	March 2016
Detection improvement of gliomas in hyperspectral imaging of protoporphyrin IX fluorescence – in vitro comparison of visual identification and machine thresholds Lehtonen, Samu J. R.; Vrzakova, Hana; Paterno, Jussi J. Cancer Treatment and Research Communications, Vol. 32 https://doi.org/10.1016/j.ctarc.2022.100615	journal	January 2022
Combination of hand-held probe and microscopy for fluorescence guided surgery in the brain tumor marginal zone Richter, Johan C. O.; Haj-Hosseini, Neda; Hallbeck, Martin Photodiagnosis and Photodynamic Therapy, Vol. 18 https://doi.org/10.1016/j.pdpdt.2017.01.188	journal	June 2017
Friction of Diamond in the Presence of Water Vapor and Hydrogen Gas. Coupling Gas-Phase Lubrication and First-Principles Studies De Barros Bouchet, Maria-Isabel; Zilibotti, Giovanna; Matta, Christine The Journal of Physical Chemistry C, Vol. 116, Issue 12 https://doi.org/10.1021/jp211322s	journal	March 2012
Fluorescence-guided surgery with live molecular navigation — a new cutting edge Nguyen, Quyen T.; Tsien, Roger Y. Nature Reviews Cancer, Vol. 13, Issue 9 https://doi.org/10.1038/nrc3566	journal	August 2013
Surgical oncology for gliomas: the state of the art Sanai, Nader; Berger, Mitchel S. Nature Reviews Clinical Oncology, Vol. 15, Issue 2 https://doi.org/10.1038/nrclinonc.2017.171	journal	November 2017
Hyperspectral data processing improves PpIX contrast during fluorescence guided surgery of human brain tumors Bravo, J. J.; Olson, J. D.; Davis, S. C. Scientific Reports, Vol. 7, Issue 1 https://doi.org/10.1038/s41598-017-09727-8	journal	August 2017
Optical properties, spectral, and lifetime measurements of central nervous system tumors in humans Poulon, F.; Mehidine, H.; Juchaux, M. Scientific Reports, Vol. 7, Issue 1 https://doi.org/10.1038/s41598-017-14381-1	journal	October 2017
Optical Characterization of Neurosurgical Operating Microscopes: Quantitative Fluorescence and Assessment of PpIX Photobleaching Belykh, Evgenii; Miller, Eric J.; Patel, Arpan A. Scientific Reports, Vol. 8, Issue 1 https://doi.org/10.1038/s41598-018-30247-6	journal	August 2018
Optical filtering technologies for integrated fluorescence sensors Dandin, Marc; Abshire, Pamela; Smela, Elisabeth Lab on a Chip, Vol. 7, Issue 8 https://doi.org/10.1039/b704008c	journal	January 2007
Intraoperative mass spectrometry mapping of an onco-metabolite to guide brain tumor surgery Santagata, S.; Eberlin, L. S.; Norton, I. Proceedings of the National Academy of Sciences, Vol. 111, Issue 30 https://doi.org/10.1073/pnas.1404724111	journal	June 2014
Transparent antifouling material for improved operative field visibility in endoscopy Sunny, Steffi; Cheng, George; Daniel, Daniel Proceedings of the National Academy of Sciences, Vol. 113, Issue 42 https://doi.org/10.1073/pnas.1605272113	journal	September 2016
-aminolevulinic acid-induced protoporphyrin IX concentration correlates with histopathologic markers of malignancy in human gliomas: the need for quantitative fluorescence-guided resection to identify regions of increasing malignancy Valdes, P. A.; Kim, A.; Brantsch, M. Neuro-Oncology, Vol. 13, Issue 8 https://doi.org/10.1093/neuonc/nor086	journal	July 2011
Origin of Ultralow Friction and Wear in Ultrananocrystalline Diamond Konicek, A. R.; Grierson, D. S.; Gilbert, P. U. P. A. Physical Review Letters, Vol. 100, Issue 23 https://doi.org/10.1103/PhysRevLett.100.235502	journal	June 2008
Monitoring ALA‐induced PpIX Photodynamic Therapy in the Rat Esophagus Using Fluorescence and Reflectance Spectroscopy Kruijt, Bastiaan; De Bruijn, Henriette S.; Van Der Ploeg‐van den Heuvel, Angelique Photochemistry and Photobiology, Vol. 84, Issue 6 https://doi.org/10.1111/j.1751-1097.2008.00379.x	journal	November 2008
5‐Aminolevulinic Acid‐induced Protoporphyrin IX Levels in Tissue of Human Malignant Brain Tumors Johansson, Ann; Palte, Gesa; Schnell, Oliver Photochemistry and Photobiology, Vol. 86, Issue 6 https://doi.org/10.1111/j.1751-1097.2010.00799.x	journal	September 2010
Fluorescence Spectra of Highlighter Inks Birriel, Jennifer J.; King, Damon The Physics Teacher, Vol. 56, Issue 1 https://doi.org/10.1119/1.5018682	journal	January 2018
Yield stress and wall slip phenomena in colloidal silica gels Walls, H. J.; Caines, S. Brett; Sanchez, Angelica M. Journal of Rheology, Vol. 47, Issue 4 https://doi.org/10.1122/1.1574023	journal	July 2003
Some Rheological Measurements on Magnetic Iron Oxide Suspensions in Silicone Oil Yang, M. ‐C.; Scriven, L. E.; Macosko, C. W. Journal of Rheology, Vol. 30, Issue 5 https://doi.org/10.1122/1.549892	journal	October 1986
Fluorescence-Guided Resection of Malignant Glioma with 5-ALA Kaneko, Sadahiro; Kaneko, Sadao International Journal of Biomedical Imaging, Vol. 2016 https://doi.org/10.1155/2016/6135293	journal	January 2016
Review of Techniques to Achieve Optical Surface Cleanliness and Their Potential Application to Surgical Endoscopes Kreeft, Davey; Arkenbout, Ewout Aart; Henselmans, Paulus Wilhelmus Johannes Surgical Innovation, Vol. 24, Issue 5 https://doi.org/10.1177/1553350617708959	journal	May 2017
Adverse long-term effects of brain radiotherapy in adult low-grade glioma patients Surma-aho, O.; Niemela, M.; Vilkki, J. Neurology, Vol. 56, Issue 10 https://doi.org/10.1212/WNL.56.10.1285	journal	May 2001
Concept of a high-resolution miniature spectrometer using an integrated filter array Wang, Shao-Wei; Xia, Changsheng; Chen, Xiaoshuang Optics Letters, Vol. 32, Issue 6, p. 632-634 https://doi.org/10.1364/OL.32.000632	journal	January 2007
Intraoperative Fluorescence-Guided Resection of High-Grade Malignant Gliomas Using 5-Aminolevulinic Acid–Induced Porphyrins: A Systematic Review and Meta-Analysis of Prospective Studies Zhao, Shiguang; Wu, Jianing; Wang, Chunlei PLoS ONE, Vol. 8, Issue 5 https://doi.org/10.1371/journal.pone.0063682	journal	May 2013
Diagnostic Potential of Autofluorescence for an Assisted Intraoperative Delineation of Glioblastoma Resection Margins¶ Croce, Anna C.; Fiorani, Sabrina; Locatelli, Donata Photochemistry and Photobiology, Vol. 77, Issue 3 https://doi.org/10.1562/0031-8655(2003)077<0309:DPOAFA>2.0.CO;2	journal	January 2003
Fluorescence Monitoring of a Topically Applied Liposomal Temoporfin Formulation and Photodynamic Therapy of Nonpigmented Skin Malignancies Bendsoe, Niels; Persson, Linda; Johansson, Ann Journal of Environmental Pathology, Toxicology and Oncology, Vol. 26, Issue 2 https://doi.org/10.1615/JEnvironPatholToxicolOncol.v26.i2.60	journal	January 2007
Quantitative Spectroscopic Analysis of 5-Aminolevulinic Acid-Induced Protoporphyrin IX Fluorescence Intensity in Diffusely Infiltrating Astrocytomas Ishihara, Ryutaro; Katayama, Yoichi; Watanabe, Takao Neurologia medico-chirurgica, Vol. 47, Issue 2 https://doi.org/10.2176/nmc.47.53	journal	January 2007
Quantitative fluorescence in intracranial tumor: implications for ALA-induced PpIX as an intraoperative biomarker Valdés, Pablo A.; Leblond, Frederic; Kim, Anthony Journal of Neurosurgery, Vol. 115, Issue 1 https://doi.org/10.3171/2011.2.JNS101451	journal	July 2011
The long-term side effects of radiation therapy for benign brain tumors in adults Al-Mefty, Ossama; Kersh, Jane E.; Routh, Anupam Journal of Neurosurgery, Vol. 73, Issue 4 https://doi.org/10.3171/jns.1990.73.4.0502	journal	October 1990
Fluorescence-Guided Surgery: A Review on Timing and Use in Brain Tumor Surgery Schupper, Alexander J.; Rao, Manasa; Mohammadi, Nicki Frontiers in Neurology, Vol. 12 https://doi.org/10.3389/fneur.2021.682151	journal	June 2021
Fluorescence Lifetime Imaging and Spectroscopic Co-Validation for Protoporphyrin IX-Guided Tumor Visualization in Neurosurgery Reichert, David; Erkkilae, Mikael T.; Gesperger, Johanna Frontiers in Oncology, Vol. 11 https://doi.org/10.3389/fonc.2021.741303	journal	September 2021
Intraoperative Fluorescence Imaging for Personalized Brain Tumor Resection: Current State and Future Directions Belykh, Evgenii; Martirosyan, Nikolay L.; Yagmurlu, Kaan Frontiers in Surgery, Vol. 3 https://doi.org/10.3389/fsurg.2016.00055	journal	October 2016
The Use of Spectroscopy Handheld Tools in Brain Tumor Surgery: Current Evidence and Techniques Lakomkin, Nikita; Hadjipanayis, Constantinos G. Frontiers in Surgery, Vol. 6 https://doi.org/10.3389/fsurg.2019.00030	journal	May 2019
Quantitative Wide-Field Imaging Techniques for Fluorescence Guided Neurosurgery Valdes, Pablo A.; Juvekar, Parikshit; Agar, Nathalie Y. R. Frontiers in Surgery, Vol. 6 https://doi.org/10.3389/fsurg.2019.00031	journal	June 2019
Supramarginal Resection for Glioblastoma: It Is Time to Set Boundaries! A Critical Review on a Hot Topic Guerrini, Francesco; Roca, Elena; Spena, Giannantonio Brain Sciences, Vol. 12, Issue 5 https://doi.org/10.3390/brainsci12050652	journal	May 2022

Similar Records

Intraoperative β{sup -} detecting probe for radio-guided surgery in tumour resection

Conference · Wed Jul 01 00:00:00 EDT 2015 · OSTI ID:22531367

Optical diagnostics of tumour cells at different stages of pathology development

Journal Article · Fri Nov 29 23:00:00 EST 2013 · Quantum Electronics (Woodbury, N.Y.) · OSTI ID:22373689

Spectrally resolved fluorescence diffuse tomography of biological tissues

Journal Article · Fri Aug 27 00:00:00 EDT 2010 · Quantum Electronics (Woodbury, N.Y.) · OSTI ID:21471341

Related Subjects

59 BASIC BIOLOGICAL SCIENCES

Miniature fluorescence sensor for quantitative detection of brain tumour

Citation Formats

References (54)

Similar Records

Related Subjects