Hyperthermia treatment advances for brain tumors

Figures & data

Figure 1. Brain tumor illustration demonstrating laser interstitial thermal therapy (LITT). (A) Schematic representation of intratumoral placement of laser catheter and brain tumor ablation. (B) Schematic representation of brain tumor ablation demonstrating post-LITT contrast enhancement consistent with LITT related blood brain barrier (BBB) disruption and LITT related perifocal edema.

Figure 2. Schematic representation of magnetic hyperthermia therapy in the brain. (A) Alternating magnetic field is applied to the patient after local administration of magnetic nanoparticles (black spheres), generating highly localized hyperthermia. (B) Heat is produced via hysteresis losses and Brownian relaxation (a process in which frictional heating is generated by the physical rotation of the magnetic particle).

Table 1. Nanoparticle constructs utilized for magnetic hyperthermia therapy.

Study	Design	Brain tumor type	Nanoparticle construct
Adamiano et al. [184]	Preclinical	Human GBM (U87-MG + E297);	Superparamagnetic calcium phosphate nanocomposites (iron-doped hydroxyapatite and iron oxide nanoparticles coated with amorphous calcium phosphate)
Carvalho et al. [193]	Preclinical	Human GBM (U87-MG)	Magnetic iron oxide nanoparticles stabilized with carboxymethylcellulose
Fernandez et al. [183]	Preclinical	Human GBM (U87-MG)	Manganese-doped ferrite nanoparticles
Grauer et al. [204]	Clinical	GBM	Superparamagnetic iron oxide nanoparticles
Gupta et al. [172]	Preclinical	Rodent Glioma (C6)	Stevioside-coated iron oxide nanoparticles (STE-Fe3O4)
Pandey et al. [202]	Preclinical	Human GBM (U87-MG)	Iron Platinum alloy nanoparticles (FePt NP)
Rego et al. 2019 [171]	Preclinical	Rodent glioma (C6)	Aminosilane-coated superparamagnetic iron oxide nanoparticles
Shi et al. [190]	Preclinical	Human GBM (U87-MG); rodent glioma (C8-D1A)	Dual-functionalized liposomes (DOX@P1NS/TNC-FeLPs)
Tapeinos et al. [194]	Preclinical	Human GBM (U87-MG)	Lipid-based magnetic nanovectors (LMNVs)
Babincova et al. [195]	Preclinical	Human GBM (U87-MG)	Etoposide-carrying human serum albumin immobilized magnetic nanoparticles
Babincova et al. [191]	Preclinical	Rodent glioma (C6)	Thermosensitive magnetoliposomes containing SPIONs and doxorubicin
Jia et al. 2018 [189]	Preclinical	Human GBM (U251)	RGE-modified, SPION-, and Cur-loaded exosomes (RGE-Exo-SPION/Cur)
Lu et al. [188]	Preclinical	Human GBM (U251)	Cetuximab (C225)-encapsulated core-shell Fe3O4@Au magnetic nanoparticles
Nguyen et al. [173]	Preclinical	Human GBM (U87-MG)	Fluorescently labeled MPIC micelles (G1@Fe3O4)
Shirvalilou et al. [168]	Preclinical	Rodent glioma (C6)	5-Iodo-2-deoxyuridine (IUdR)-loaded magnetic nanoparticles (NGO/PLGA)
Zhou et al., 2018 [187]	Preclinical	Human GBM (U87-MG)	c(RGDyK) peptide PEGylated Fe@Fe3O4 nanoparticles (RGD-PEG-MNPs)
Alphandéry et al. [175,176]	Preclinical	Human GBM (U87-MG-Luc)	Magnetosomes (CM)
Hamdous et al. [177]	Preclinical	Rodent glioma (GL261 + RG2);	Chitosan (M-Chi), polyethyleneimine (M-PEI), and neridronate (M-Neri) coated nanoparticles
Le Fevre et al. [174]	Preclinical	Rodent glioma (GL261)	Magnetosomes-poly-L-lysine (M-PLL) and iron oxide nanoparticles
Ohtake et al. [196]	Preclinical	Human GBM (U87-MG + U251 + YKG)	Fe(Salen) nanoparticles
Zamora-Mora et al. [192]	Preclinical	Human GBM (A-172)	Chitosan nanoparticles (CSNPs)
Liu et al. [169]	Preclinical	Human GBM (U87-MG)	Ferromagnetic IMO nanoflowers (FIMO-NFs)
Shevstov et al. [185]	Preclinical	Rodent glioma (C6)	Superparamagnetic iron oxide nanoparticles conjugated with heat shock protein (Hsp70-SPIONs)
Pala et al. [186]	Preclinical	Human GBM (U87-MG)	Dextran-coated, aptamer-bound, aptamer-fluorescein magnetic NPs (NPAF)
Yi et al. [162]	Preclinical	Rodent glioma (C6)	Magnetic nano-iron
Jiang et al. [178]	Preclinical	Human GBM (U251)	Silver nanoparticles (AgNPs)
Meenach et al. [250]	Preclinical	Human GBM (M059K)	Magnetic PEG-based hydrogel nanocomposites
Zhao et al. [197]	Preclinical	Human GBM (U251)	Solar-planet structured magnetic nanocomposites (Amino silane coated magnetic nanoparticles)
Hua et al. [198]	Preclinical	Rodent glioma (C6)	Polymer poly[aniline-co-N-(1-one-butyric acid) aniline] (SPAnH) coated iron oxide nanoparticles
Liu et al. [179]	Preclinical	Human GBM (U251); Rodent glioma (C6)	Silver nanoparticles (AgNPs)
Liu et al. [156]	Preclinical	Rodent glioma (C6)	Magnetic nanoparticles
Maier-Hauff et al. [203]	Clinical	GBM	Iron-oxide (magnetite) nanoparticles

GBM: glioblastoma.

Figure 3. Illustration of brain tumor nanoparticle-mediated photothermal therapy (PTT). (A) Schematic representation of local NIR light application to a brain tumor after photothermal agents (PTAs) administration (black spheres). (B) Schematic illustration demonstrating NIR light excitation of PTAs within the brain tumor. PTAs absorb NIR light and emit thermal energy acting as local heat sources.

Table 2. Nanoparticle constructs utilized for photothermal therapy.

Study	Design	Brain tumor type	Nanoparticle construct
Casanova-Carvajal et al. [216]	Preclinical	Rodent glioma (CT-2A)	Gold nanorods biofunctionalized with CD133 antibody (B-GNRs)
Kwon et al. [165]	Preclinical	Human GBM (U87-MG)	Temozolomide/ICG-loaded iron oxide nanoparticles
Qian et al. [226]	Preclinical	Human GBM (U87-MG); rodent glioma (C6)	Pep22 linked polyethylene glycol (PEG) and oxidized nanocrystalline mesoporous carbon particles (OMCN)
Liu et al. [52]	Preclinical	Rodent glioma (CT-2A)	Gold nanostars
Shibata et al. [231]	Preclinical	Rodent glioma (9L gliosarcoma)	Phospholipid-conjugated indocyanine green (LP-iDOPE) nanoparticle
Zeng et al. [222]	Preclinical	Human GBM (NCH-421K); rodent glioma (C6)	TMZ-loaded porous silicon nanoparticles (TMZ/PSi NPs)
Han et al. [251]	Preclinical	Human GBM (U87-MG)	Two-dimensional Nb2C MXenes
Lu et al. [188]	Preclinical	Human GBM (U251)	Cetuximab (C225)-encapsulated core-shell Fe3O4@Au magnetic nanoparticles
Qian et al. [215]	Preclinical	Human GBM (U87-MG)	Multicolor highly crystalline carbon nanodots (HCCDs)
Tsai et al. [235]	Preclinical	Rodent glioma (ALTS1C1)	Angiopep-2/cholesterol-conjugated poly(ethylene glycol) oleic acid-coated upconversion nanoparticles (ANG-IMNPs)
Wang et al. [210]	Preclinical	Rodent glioma (C6)	Iron oxide-carbon core-shell nanoparticles
Xu et al. [221]	Preclinical	Rodent glioma (C6)	Indocyanine green dyed silk fibroin nanoparticles (ICG-SFNPs)
Christie et al. [217]	Preclinical	Human GBM (ACBT); rodent glioma (P388-D1)	Macrophage loaded gold-silica nanoshells (AuNS) and gold nanorod (AuNR)
Yang et al. [252]	Preclinical	Human GBM (U87-MG)	Semiconducting poly (perylene diimide) (PPDI) and poly(ethylene glycol (PEG) tethered gold nanoparticles
Zhu et al. [253]	Preclinical	Human GBM (U87-MG)	Holo-Tf-indocyanine green (holo-Tf-ICG) nanoassemblies
Eldridge et al. [212]	Preclinical	Human GBM (U87-MG)	Short multi-walled carbon nanotubes (MWCNTs)
Kafa et al. [207]	Preclinical	Human GBM (primary astrocytoma type I)	Amino-functionalized multi-walled carbon nanotubes
Liu et al. [206]	Preclinical	Human GBM (U87-MG)	Novel Cs-based upconversion nanoparticles (UCNP-ICG-TOS-RGD)
Sheikh Mohamed et al. [224]	Preclinical	Human GBM (glioma)	Plasmonic fluorescent CdSe/Cu2S hybrid nanocrystals
Hao et al. [229]	Preclinical	Human GBM (U87-MG)	Docetaxel loaded ploy (lactide-co-glycolide) gold nanoparticles
Mohamed et al. [225]	Preclinical	Human GBM (glioma)	Ribotoxin-curin conjugated biogenic gold nanoparticles
Santos et al. [213]	Preclinical	Human GBM (U87-MG + U251 + LN229 + T98G)	Carbon nanotubes
Bidwell et al. [31]	Preclinical	Human GBM (U87-MG +  D54); rodent glioma (C6)	Cell-penetrating peptides
Botella et al. [230]	Preclinical	Human GBM (42-MG-BA)	Mesoporous silica protected gold nanoclusters (Au@SiO2)
Fernandez Cabada et al. [209]	Preclinical	Human astrocytoma (1321N1)	Gold nanorods
Day et al. [227]	Preclinical	Human astrocytoma (U-373 MG)	Polyethylene glycol-coated nanoshells and VEGF-coated nanoshells
Baek et al. [218]	Preclinical	Human GBM (ACBT)	PEGylated gold nanoshells
Wang et al. [214]	Preclinical	Human GBM (GBM-CD133^+; GBM-CD133^− CSC)	Carbon nanotubes with CD133 monoclonal antibody
You et al. [219]	Preclinical	Human GBM (U87-MG)	Paclitaxel hollow gold nanospheres

GBM: glioblastoma; CSC: cancer stem-like cells.

Figure 4. Schematic illustration summarizing some of the less common HT modalities that have been employed for brain tumor treatment. HT for brain tumors has been performed with ultrasound (US), radiofrequency (RF) and microwaves (MW).

Table 3. Understudied HT modalities for the treatment of brain tumors.

Study	Design	HT modality	Brain tumor type
Byun et al. [248]	Clinical	Novel hyperthermia device	BM
Schooneveldt et al. [247]	Clinical	M/W	PT
Bredlau et al. [244]	Preclinical	R/F	Canines with no tumors
Rozumenko et al. [249]	Clinical	LSTT	HGGs
Roussakow SV, 2017 [246]	Clinical	EHT	HGGs
Cha et al. [243]	Preclinical	EHT	Human GBM (U87-MG + A172)
Man et al. [32]	Preclinical	M/W	Human GBM (patient derived glioma stem cells specimens 3691 and 387)
Coluccia et al. [237]	Clinical	U/S	HGGs
James et al. [14]	Preclinical	R/F	Rodent glioma (9L gliosarcoma)
McDannold et al. [236]	Clinical	U/S	HGGs
Wismeth et al. [245]	Clinical	EHT	HGGs
Park et al. [238]	Clinical	U/S	HGGs

HT: hyperthermia; R/F: radio-frequency hyperthermia; EHT: electro-hyperthermia; U/S: ultrasound; M/W: microwave hyperthermia; LSTT: laser surface thermal therapy; BM: brain metastasis; HGGs: high grade gliomas; PT: pediatric tumor.

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