Systematic Review of Photodynamic Therapy in Gliomas
Abstract
:Simple Summary
Abstract
1. Introduction
2. Photodynamic-Therapy-Mediated Tumoricidal Effect
2.1. PDT Induces Cell Death following PS Uptake, Accumulation, and Activation
2.2. PDT Controls Glioma Stem Cell (GSC) Processes
2.3. PDT Modulates Neurovasculature: Disruption of the Blood–Brain Barrier (BBB) and Destruction of Tumor Vasculature
2.4. PDT Stimlates Anti-Tumor Immunity
3. Photosensitizers
3.1. First Generation: Naturally Occurring Porphyrins
3.2. Second Generation: Increased Singlet Oxygen Potency
Combining Second-Generation PDT with Standard Therapies
3.3. Third-Generation PS: Increased Tumor Selectivity
4. Optimizing Light Delivery
5. PDT in Other CNS Tumors
6. Limitations
6.1. Limitations of PDT and Its Synergistic Agents
6.2. PDT Efficacy Negatively Influenced by the Harsh Glioma Microenvironment
6.3. Innate PDT Resistance
6.4. Peri-Tumor Edema Limits PDT Efficacy
6.5. PDT Drug Interactions and Synergistic Agents
7. Conclusions and Future Directions
Author Contributions
Funding
Data Availability Statement
Conflicts of Interest
References
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Photosensitizer | Intracellular Localization | Excitation Wavelength (nm) | Treatment Window a | Clearance Time | Tumor: Normal Fluorescence Ratio b | Administration | Side Effects | |
---|---|---|---|---|---|---|---|---|
First Generation | Porfimer Sodium | Inner mitochondrial membrane | 630 | 48–150 h | 4–8 weeks | 2.5–4:1 | Systemic | Skin sensitization, thrombocytopenia |
Hematoporphyrin derivative [HpD] | 408, 510, 630 c | 24–48 h | 4–6 weeks | Systemic | ||||
Dihematoporphyrin ether [DHE] | 395, 630 c | 24–72 h | 4–6 weeks | Systemic | ||||
Second Generation | 5-Aminolevulinic Acid (Levulin®, Gliolan®) | Early: mitochondria Late: plasma membrane, lysosomes | 410, 510, 635 c | 4–8 h | 2 days | 10–20:1 | Oral | Skin sensitization, nausea, elevated liver enzymes, anemia |
Talaporfin sodium (Laserphyrin, AptocineTM, LS11, PhotoIon®) | Lysosomes | 664 | 12–26 h | 15 days | ND | Systemic | Skin sensitization | |
Temoporfin [m-THPC; m-tetrahydroxyphenylchlorin] (Foscan®, liquid formulation; Foslip®, liposomal formulation) | Strong: Golgi apparatus, Endoplasmic reticulum Weak: mitochondria, lysosomes | 652 | 48–110 h | 15 days | 150:1 | Systemic | Skin sensitization | |
Boronated protoporphyrin [BOPP] | Lysosomes | 630 | 24 h | 4–6 weeks | 400:1 | Systemic | Skin sensitization, thrombocytopenia | |
Benzoporphyrin derivative [BPD] | Lysosomes | 680–690 | 15–30 min. | 1–5 days | ND | Systemic | Vascular damage |
Study Group a (n, Number of GBM Patients in Study) | Mean Age | PS b | Dose c | Route d | Time Prior to Photoillumination | Photoillumination Method e | Laser/Light Wavelength f (nm) | Photoillumination Energy (ED unless Otherwise Specified) | Reported Survival g | Survival Statistics | Adverse Events | |||
---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
Perria et al. (1980) | GBM | 2 | n/a | HpD | 5 mg/kg | IV | n/a | n/a | 628 | 720–2400 J/cm2 | MS | GBM | 6.9 mo | n/a |
Laws et al. (1981) | rMG | 5 | 14–75 | HpD | 5 mg/kg | IV | 48–72 h | Interstitial | 630 | 30–60 mW/cm2 § | TTP | rMG | 1–6 mo | Increased skin photosenstivity |
McCulloch et al. (1984) | GBM | 9 | n/a | HpD | 5 mg/kg | IV | n/a | n/a | 627.8 (>1 laser) | n/a | OS | GBM (n = 3) | 17–42 mo | Increase in P/O cerebral edema |
Muller and Wilson (1985) h | GBM rGBM | 1 2 | 53 32, 44 | HpD | 2.5 mg/kg 2 mg/kg | IV | 24 h | Cavitary (balloon) | 630 | 8–68 J/cm2 | n/a | None | ||
Kaye et al. (1987) i | GBM rGBM | 13 6 | 45 *** 40 *** | HpD | 5 mg/kg | IV | 24 h | Interstitial | AI (9) GMVL (14) | 70–120 J/cm2 120–230 J/cm2 | PFS | GBM rGBM | 3–13 mo 12–16 wk | No AEs |
Kostron et al. (1987) j | GBM | 6 | 63.3 | HpD | 1.0 mg/cm3 | IV IA Direct tumor | 3 d | LED (n = 9) Cavitary (n = 5) | 620–640 632 | 422 J/cm2 § <1600 J/cm2 § | MS/OS | GBM | 12 mo | IA/Direct tolerated without skin phototoxicity |
rGBM (1x) | 5 | 50.8 | rGBM (1x) | 2–7 mo | ||||||||||
rGBM (mult) | 3 | 57.0 | rGBM (mult) | 5 mo | ||||||||||
Muller and Wilson (1987) h | [HpD] GBM | 1 | 52 | HpD (8) DHE (24) | 2.14 mg/kg 2.08 mg/kg | IV | 18–24 h | Cavitary | 630 | HpD: 32 J/cm2 DHE: 23 J/cm2 | MS | [HpD] GBM | 2.9 mo | Skin photosensitivity (n = 3) |
[HpD] rGBM | 1 | 32 | [HpD] rGBM | 5.8 mo | ||||||||||
[DHE] GBM | 7 | 58.3 | Total dose | 150 mg | [DHE] GBM | 1.1–13.6 mo | ||||||||
[DHE] rGBM | 7 | 39.4 | [DHE] rGBM | 0.2–10.7 mo | ||||||||||
Kostron et al. (1988) j | GBM | 8 | 55 ** | HpD | 1 mg/cm3 | IV, IA and/or Direct | 3 d | LED Cavitary | 590–750 632 | 422 J/cm2 § 60–200 J/cm2 | OS | GBM rGBM (1x) rGBM (mult) | 0.5–19 m 3–14 mo 1–6 mo | Skin phototoxicity (IA/IV only) |
rGBM (1x) | 9 | |||||||||||||
rGBM (mult) | 3 | |||||||||||||
HPD only (n = 9), [HPD+single dose radiation of 4 Gy fast electrons] (n=10), [HPD+single dose radiation+conventional radiotherapy] (n = 4); 3 cases of recurrence and subsequent re-treatment. | ||||||||||||||
Kostron et al. (1990) j | GBM rGBM | 9 18 | n/a | HpD | n/a | IV, IA and/or Direct | n/a | Interstitial | 630 | 40–220 J/cm2 | OS | GBM rGBM | 0.5–29 mo 4–13 mo | Increased phototoxicity of the skin |
Muller and Wilson (1990) h | GBM rGBM | 9 14 | 48 | HpD DHE | 5 mg/kg 2 mg/kg | IV | 18–24 h | Cavitary | 630 | 24 J/cm2 | MS | GBM + rGBM | 6.3 mo | Increased skin photosensitivity |
Powers et al. (1991) | rGBM rMG | 1 5 | 42–61 | HPE | 2.0 mg/kg | IV | 24 h | Interstitial | 630 | 1000 J §§ | TTP | rGBM rMG | 2–27 wk 6–45 wk | Edema, increased intracranial pressure and skin photosensitivity |
Origitano et al. (1993) | rGBM | 8 | 42.2 | PNa | 2.0 mg/kg | IV | 48–72 h | Cavitary Interstitial + post-resection cavitary | 630 630 | 50 J/cm2 100 J/cm per fiber | TTP | rGBM | 5–22 mo | Increased skin photosensitivity |
Muller and Wilson (1995) h | rGBM | 32 | 41 ** | HpD PNa HPE | 5 mg/kg 2 mg/kg 2 mg/kg | IV IV IV | 12–36 h | Cavitary | 630 | 38 J/cm2 | MS | [Stratify by light dose] Energy: >1700 J <1700 J | 28 wk 29 wk | Edema, increased skin photosensitivity |
Popovic et al. (1995) i | GBM rGBM | 38 40 | n/a | HpD | 2.0–2.5 mg/kg | IV | 24 h | Cavitary | AI: 1986–1987 GMVL: 1987–1994 | 240–260 J/cm2 (initial pts: 70) | MS | GBM rGBM | 24 mo 9 mo | n/a |
Muller and Wilson (1997) h | GBM rGBM | 11 32 | 40 58 | PNa | 2 mg/kg | IV | 12–36 h | Cavitary | 630 | GBM: 30 J/cm2 * rGBM: 43 J/cm2 * | MS | GBM rGBM | 37 wk 30 wk | Increased P/O cerebral edema |
Muller et al. (2001) [Phase II] h | rGBM (ED ≤ 50) (ED ≥ 50) | 37 (22) (15) | 41 ** | PNa | 2 mg/kg | IV | 12–36 h | Cavitary | 630 | 8–110 J/cm2 | MS | rGBM (ED ≤ 50) (ED ≥ 50) | avg 29 wk (29 wk) (34 wk) | Increased P/O cerebral edema |
Muller et al. (2001) [Phase III] h | GBM High light | 20 | 54 | PNa | 2 mg/kg | IV | 12–36 h | Cavitary | 630 | 30–50 J/cm2 (low) 110–130 J/cm2 (high) | MS | GBM High | 92 wk | n/a |
rGBM Low light High light | 26 26 | 48 52 | rGBM Low High | 29 wk 51 wk | ||||||||||
Schmidt et al. (2004) | Recurrent brain tumors (include GBM) | NS | n/a | PNa | 0.75 mg/kg 1.20 mg/kg 1.60 mg/kg 2.00 mg/kg | IV | 18–24 h | Laser/LED + Cavitary balloon | Laser: 630 LED: 20–25 | 100 J/cm2 | Not specified | No neurotoxicity | ||
Stylli et al. (2004) i | GBM rGBM | 31 27 | 44 *** | HpD | 5 mg/kg | IV | 24 h | Cavitary | AI: 1986–1987 GMVL: 1987–1994 KTP: 1994–2000 | 240 J/cm2 §§ | MS | GBM/rGBM | 24 mo | n/a |
Stylli et al. (2005) i | GBM rGBM | 31 55 | 47 * 42 * | HpD | 5 mg/kg | IV | 24 h | Cavitary | AI: 1986–1987 GMVL: 1987–1994 KTP: 1994–2000 | 240 J/cm2 §§ | MS | GBM rGBM | 14.3 mo 13.5 mo | Increased cerebral edema (n = 3) |
Muller et al. (2006) h | GBM rGBM | 12 37 | 59 41 | PNa | 2 mg/kg | IV | 12–36 h | Cavitary (balloon/cont. filling with Intralipid) +/− interstitial | AI KTP | 58 J/cm2 §§§ | MS | GBM rGBM | 33 wk 29 wk | Skin photosensitivity |
Kaneko (2008) | GBM | 26 | n/a | HPE | 3 mg/kg | IV | 2 d | Interstitial | 640 | 180 J/cm | n/a | n/a |
Study Group a (n, Number of Patients with Disease and Treatment) | Mean Age | PS b | Dose c | Route d | Time Prior to Photoillumination | Photoillumination Method e | Laser/Light Wavelength f (nm) | Photoillumination Energy g (ED unless otherwise specified) | Reported Survival h | Survival Statistics | Adverse Events | |||
---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
Kostron et al. (1998) | GBM rGBM | 2 8 | 61–72 34–72 | mTHPC x | 0.15 mg/kg | IV | 4 d | Interstitial I/O cavitary | KTP 652 | 300 mW/cm2 § 20 J/cm2 | TTP MS | rGBM rGBM | 4 mo 6 mo | Phototoxicity |
Rosenthall et al. (2001/2003) i | GBM rGBM | 7 9 | 51 * | BOPP | 0.25–8.0 mg/kg | IV | 24 h | I/O fiber diffuser for focused surface irradiation | 630 | 25 J/cm2 | MS | GBM rGBM | 5 mo 11 mo | n/a |
Schmidt et al. (2004) | Recurrent brain tumors (including GBM) | NS | n/a | BPD | 0.25 mg/kg | IV | 3–6 h | Laser fiber optic catheter/balloon LED balloon | 680 | 1,800 J §§ (at 100 J/cm2) | Not specified | No cytotoxic effects | ||
Kostron et al. (2006) | GBM | 26 | n/a | mTHPC x | 0.15 mg/kg | IV | 4 d | I/O cavitary I/O fiber diffuser | KTP 652 | 300 mW/cm2 § 20 J/cm2 | MS | GBM | 15 mo | Increased skin sensitivity |
Beck et al. (2007) | rGBM | 10 | 51.7 | 5-ALA | 20 mg/kg | Oral | 1 h | I/O fiber diffuser for focused surface irradiation | 633 | 100 J/cm2 | MS | 15 m | n/a | |
Elijamel et al. (2007) | GBM, PDT(+) GBM, PDT(−) | 13 14 | 59.6 60.1 | 5-ALA -- | 20 mg/kg -- | Oral -- | 3 h -- | P/O cavitary balloon | 630 | 100 J/cm2 | PFS MS | GBM | 8.6 mo 52.8 wk | Deep venous thrombosis (n = 2) |
Stepp et al. (2005) | GBM | 5 | n/a | 5-ALA | 20 mg/kg | Oral | 3 h | I/O fiber diffuser for focused surface irradiation | 633 | 100–200 J/cm2 | n/a | n/a | ||
Stepp et al. (2007) | GBM (a) GBM (b) GBM (c) | 5 8 7 | n/a | 5-ALA | 20 mg/kg | Oral | 3 h | I/O fiber diffuser for focused surface irradiation | 633 | (a) 100 J/cm2 (b) 150 J/cm2 (c) 200 J/cm2 | n/a | No AEs | ||
Akimoto et al. (2012) | GBM rGBM | 6 8 | 49–82 41–61 | TS | 40 mg/m2 | IV | 24 h | I/O fiber diffuser for focused surface irradiation (1.0 cm diameter) | 664 | 27 J/cm2 | PFS | GBM | 24.8 mo | Increased photosensivity |
Lyons et al. (2012) | Total (GBM) PDT(+) PDT(−) PDT(+): [a], [b] PDT(-): [c], [d] | 73 30 43 17, 13 18, 25 | 59 ** | 5-ALA | 20 mg/kg | Oral | 3 h | [a] IORT, I/O cavitary, MSR [b] I/O cavitary, MSR [c] IORT, MSR [d] MSR only | 630 | 100 J/cm2 | PFS MS | [a] [b] PDT+ PDT- | 79 wk 39.7 wk 62.9 wk 20.6 wk | n/a |
Johansson et al. (2013) | GBM rGBM | 1 4 | 42 56 | 5-ALA | 20–30 mg/kg | Oral | 5–8 h | Interstitial | 635 | 720 J/cm2 | TTP | 3–36 mo | n/a | |
Muragaki et al. (2013) | GBM | 13 | 47.1 ** | TS | 40 mg/m2 | IV | 22–27 h | I/O fiber diffuser for focused surface irradiation (1.5 cm diameter) | 664 | 27 J/cm2 | PFS MS | 12 mo 27.9 mo | Increased photosensitivity | |
Schwartz et al. (2015) | GBM | 15 | n/a | 5-ALA | 20 mg/kg 30 mg/kg | Oral | n/a | Interstitial | 633 | 12.96 J §§ | PFS MS | 16 m 34 m | Transient aphasia, pulmonary embolism | |
Vanaclocha et al. (2015) | GBM | 20 | 49 *** | DHE mTHPC x | 2 mg/kg 0.15 mg/kg | IV | 48 h 96 h | I/O cavitary | 630 652 | 75 J/cm2 20 J/cm2 | PFS MS MS (from 1st diagnosis) | 10 mo 9 mo 17 mo | Skin photosensitivity dermatitis | |
Nitta et al. (2018) | GBM | 11 | 54 | TS | 40 mg/m2 | IV | 22–26 h | I/O fiber diffuser for focused surface irradiation (1.5 cm diameter) | 664 | 27 J/cm2 | PFS MS | 19.6 mo27.5 mo | Asymptomatic transient peripheral edema | |
Shimizu et al. (2018) | GBM rGBM | 7 7 | 45–74 40–69 | TS | 40 mg/m2 | IV | 22–26 h | I/O fiber diffuser for focused surface irradiation (1.5 cm diameter) | 664 | 100 J/cm2 | n/a | Pulmonary embolism (if vessels are not shielded) | ||
Lietke et al. (2021) | rGBM | 37 | 49.4 * | 5-ALA | 20 mg/kg | Oral | 3–5 h | Interstitial | 635 | 8883 J §§ | TTP MS (from 1st diagnosis) | Study combines GBM and AA | 7.1 mo 39.7 mo | Transient worsening of pre-existing neurological deficits |
Vermandel et al. (2021) | GBM | 10 | 57.1 * | 5-ALA | 20 mg/kg | Oral | 6 h | I/O cavitary | 635 | 200 J/cm2 | PFS MS | 17.1 mo 23.1 mo | No AEs | |
Kobayashi et al. (2022) | GBM | 43 | 46.7 ** | TS | 40 mg/m2 | IV | 22–26 h | I/O fiber diffuser for surface irradiation (1.5 cm diameter) | 664 | 27 J/cm2 | PFS MS | 6.3 mo 15.4 mo | No AEs | |
Kozlikina et al. (2022) | GBM | CR | 29 | 5-ALA + Ce6 | 20 mg/kg 1 mg/kg | Oral IV | 4–4.5 h 3–3.5 h | I/O fiber | 660 | 60 J/cm2 §§§ | n/a | n/a |
Study Name | Trial Phase (Study ID) | Type of Cancer | Drug | Principal Investigator |
---|---|---|---|---|
Photodynamic Therapy (PDT) for malignant brain tumor in children | Phase I/II (UMIN000030883) | Brain Tumor (Pediatric) | TS (Leserphyrin) | Kawamata Takakazu (Tokyo Women’s Medical University) |
Clinical Safety Study on 5-Aminolevulinic Acid (5-ALA) in Children and Adolescents With Supratentorial Brain Tumors | Phase II (NCT04738162) | Brain Tumor (Pediatric) | 5-ALA (Gliolan) | Walter Stummer (Univ. Hospital, Münster) |
Stereotactical Photodynamic Therapy With 5-aminolevulinic Acid (Gliolan®) in Recurrent Glioblastoma | Phase II (NCT04469699) | GBM | 5-ALA (Gliolan) | Walter Stummer (Univ. Hospital, Münster) |
PD L 506 for Stereotactic Interstitial Photodynamic Therapy of Newly Diagnosed Supratentorial IDH Wild-type Glioblastoma | Phase II (NCT03897491) | GBM | 5-ALA (PD L 506) | Niklas Thon (Univ. Hospital, Munich) |
Dose Finding for Intraoperative Photodynamic Therapy of Glioblastoma | Phase II (NCT04391062) | GBM | 5-ALA (Gliolan) | Nicholas Reyns (Univ. Hospital, Lille) |
Study to Evaluate 5-ALA Combined With CV01 Delivery of Ultrasound in Recurrent High Grade Glioma | Phase I (NCT05362409) | High Grade Glioma | 5-ALA (Gliolan) | Alpheus Medical (Wash. Univ. St. Louis, Dent Institute, Northwell Health) |
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Hsia, T.; Small, J.L.; Yekula, A.; Batool, S.M.; Escobedo, A.K.; Ekanayake, E.; You, D.G.; Lee, H.; Carter, B.S.; Balaj, L. Systematic Review of Photodynamic Therapy in Gliomas. Cancers 2023, 15, 3918. https://0-doi-org.brum.beds.ac.uk/10.3390/cancers15153918
Hsia T, Small JL, Yekula A, Batool SM, Escobedo AK, Ekanayake E, You DG, Lee H, Carter BS, Balaj L. Systematic Review of Photodynamic Therapy in Gliomas. Cancers. 2023; 15(15):3918. https://0-doi-org.brum.beds.ac.uk/10.3390/cancers15153918
Chicago/Turabian StyleHsia, Tiffaney, Julia L. Small, Anudeep Yekula, Syeda M. Batool, Ana K. Escobedo, Emil Ekanayake, Dong Gil You, Hakho Lee, Bob S. Carter, and Leonora Balaj. 2023. "Systematic Review of Photodynamic Therapy in Gliomas" Cancers 15, no. 15: 3918. https://0-doi-org.brum.beds.ac.uk/10.3390/cancers15153918