Cold Atmospheric Pressure Plasma (CAP) as a New Tool for the Management of Vulva Cancer and Vulvar Premalignant Lesions in Gynaecological Oncology
Abstract
:1. Introduction
- (a)
- Vulva cancer is technically easy to approach using CAP.
- (b)
- The effect of radioresistance in subtypes of this malignancy is becoming a clinical problem.
- (c)
- VIN lesions are commonly treated/managed with local drugs or by applying tracer, which may be suitable for large PAM (plasma-activated medium) treatment.
- (d)
- (e)
- Anatomical circumstances usually restrict re-excisions after primary surgery, which is often combined with advanced plastic flaps (e.g., in the case of “worrisome” surgical margins).
- (f)
2. Epidemiology and the Prevalence of Vulvar Cancer
3. Aetiopathology, Clinical Aspects and Current Treatment of Vulvar Cancer and Its Premalignant Lesions
3.1. Precursors and Classification of the Disease
3.2. Current Treatment of the Disease
4. Current Knowledge of In Vitro Cell Lines and Further Potential for Clinical Application of CAP Oncogynaecology
5. Plasma Physical and Chemical Characteristics and Plasma Sources in Medicine
Sources of Cold Atmospheric Plasma
- Direct plasma sources: These plasmas use the human body (such as the skin, internal tissues, etc.) as an electrode. Thus, the current produced by plasmas has to pass through the body. The most commonly utilised technology in this category is the dielectric barrier discharge (DBD) plasma source. The major disadvantage of this technique is the application distance (between the electrodes) which must remain within a close range, generally less than three mm2, thus limiting its use for small areas of the human body [15].
- Indirect plasma sources: These plasmas are generated between two electrodes. Active species that are created by the plasmas are subsequently transported to target application areas. Several devices are available, ranging from very narrow plasma needles or jets to larger plasma torches such as the kINPen® MED, Atmospheric Pressure MicroPlasma Jet (APMPJ), InvivoPen, and MicroPlaSter® α and β. Plasma jets can be classified according to parameters such as discharge geometry, electrode arrangement, excitation frequency or pattern.
- Hybrid plasma sources: These plasmas combine the benefits of the two aforementioned plasma source types (e.g., using the plasma production technique of direct plasma sources and the essentially current-free property of indirect plasma sources). This is achieved by introducing a grounded wire mesh electrode, which has significantly smaller electrical resistance than that of the tissue. Thus, in principle, all current can pass through the wire mesh. The MiniFlatPlaSter is an example of a hybrid plasma source.
6. Plasma Interaction with Human Tissue
7. Plasma Promoted Wound Healing and Its Possibilities in the Surgical Treatment of VSCC
8. CAP Specific Abilities Predisposing Its Application in Anticancer Therapy
8.1. CAP Effect on Cellular and Extracellular Level
8.2. CAP and Apoptosis
8.3. CAP and Induced Gene Expressions, Proteomic and Epigenetic Changes
8.4. CAP Induced DNA Breaks and Modifications
8.5. CAP and Induced Redox ROS and RNS Effect
9. CAP as a Novel Anticancer Treatment Modality, Including Vulvar Pathologies
9.1. Direct Anti-Tumour Effects of CAP
9.2. Indirect Anti-Tumour Effects of CAP
9.3. Dual Cancer Therapeutic Approach: Synergy of CAP and Nanotechnology
9.4. Immunotherapy and CAP
10. Advancements in VC Therapy Based on Better Profiling and Novel Technologies Combining CAP with Existing Treatments
11. A paradigm Shift from Reactive to Predictive, Preventive and Personalised Medicine (3PM)—Prominent Examples in the Context of Vulva Cancer and Premalignant Lesions
11.1. The Primary Level of Targeted Prevention
11.2. The Secondary Level of Targeted Prevention
11.3. The Tertiary Level of Targeted Prevention
12. Status Quo and Clinically Relevant Perspectives
13. Conclusions
Author Contributions
Funding
Conflicts of Interest
References
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Cell Line Origin | Cell Line/s | Main Effects of CAP on Cell Lines Observed in the Studies | Ref. |
---|---|---|---|
Cervix | HeLa SiHa HFB | ° Reduced viability of cells after plasma treatment in a dose-dependent manner ° Selective inhibition of proliferation in cancer cells compared to HFB ° Higher inhibition effect in the case of SiHa cells in comparison to Hela cells ° Significant increase of cells in subG0 phase cell and vice versa: reduction of populations in S phase and G2/M phase in a cell-type-specific manner ° Identification of caspase-3, -8 and -9 activation as an important mechanism underlying apoptosis in plasma-treated cells | [12] |
Cervix | HeLa HFB detroit551 | ° Induction of HeLa cell apoptosis by facilitating an accumulation of intracellular reactive oxygen and nitrogen species (RONS) in a dose-dependent manner by both dielectric barrier discharge (DBD) plasma and nitric oxide-plasma activated water (NO-PAW) ° Higher selectivity of NO-PAW at given conditions | [62] |
Cervix | HeLa | ° Inhibited proliferation and induced cell death in an exposure time-dependent manner ° Significant suppression of the migration and invasion ° Reduced activity and expression of the matrix metalloproteinase (MMP)-9 enzyme ° Decreased phosphorylation level of both ERK1/2 and JNK, but not p38 MAPK | [63] |
Cervix | CaSki DoTc2-4510 SiHa C-33-A | ° Time- and energy-dependent effects of the treatment on cell proliferation ° Higher sensitivity of cervical cancer cells to plasma treatment in comparison to non-cancerous cervical tissue cells ° Decreased metabolic activity in cancer cells lines when compared to NCCT | [64] |
Cervix | CaSki | ° Distance and flow rate-dependent effect of CAP on tumour cell viability ° Dose-dependent induction of tumour cell death by CAP treatment | [65] |
Cervix | HeLa | ° Augmented number of early apoptotic cells, late apoptotic cells, but rarely necrotic cells by treatment with N2 and air plasma jets ° Induced apoptotic cell death in a dose-dependent manner ° Increased level of ROS and consequently, induction of apoptosis ° Induction of the mitochondria membrane depolarisation, causing increased mitochondrial transmembrane permeability and release of proapoptotic factors ° Blocking of ROS mediated plasma-induced apoptosis by D-mannitol, sodium pyruvate, carboxyl-PTIO or N-acetyl-cysteine ° Generation of different types and compositions of ROS by different plasma sources | [66] |
Cervix | HeLa | ° After controlled application of plasma with the precision of tens of nanometres observed killing of plasma-treated cells, neighbouring cells were not affected significantly ° Induction of morphological changes as well as indicators of apoptosis in treated cells ° Crucial role of ROS in cancer cell death induction | [67] |
Cervix | HeLa | ° Induction of cellular lipid membrane collapse by atmospheric-pressure plasma ° Alteration of electrical conductivity of the cells and induction of lipid oxidation by ROS | [68] |
Cervix | SiHa + healthy human cervical tissue cells from cervical conus | ° Immediate and persisting decrease in CC cell growth and cell viability associated with significant plasma-dependent effects on lipid structures | [69] |
Endometrium | AMEC HEC50 | ° Reduction of cell viability and induction of cell death by PAM ° Increased autophagic cell death ° Inactivation of the mTOR pathway by PAM ° G2/M-phase arrest in all PAM concentrations ° Induction of intracellular ROS accumulation | [70] |
Endometrium | HEC-1 HEC-108 | ° Reduction of cells containing high levels of aldehyde dehydrogenase (ALDH) - a marker of cancer-initiating cells (CICs) ° Synergistic effect of combined treatment with cisplatin, especially at lower doses ° Combination of plasma and cisplatin treatment is effective both in ALDH high and low cells | [71] |
Endometrium | HEC-1 GCIY | ° Reduction of cell viability ° Reduction of the number of cells with high aldehyde dehydrogenase (ALDH) production | [72] |
Ovary | OVCAR-3 SKOV-3 TOV-21G TOV-112D | ° Variation of anti-proliferative efficacy of CAP dependent on treatment duration as well as on the OC cell line used ° Decreased motility, invasion, and metastasis potential ° Culture medium treated with plasma before addition mediates the CAP effect on the cells, however, this effect depends on the cell medium composition | [73] |
Ovary | SKOV-3 OV-90 HOSE | ° Selective anticancer activity of plasma-activated Ringer’s Lactate solution (PA-RL) containing reactive oxygen and nitrogen species (RONS) | [74] |
Ovary | TOV21G ES-2 SKOV3 NOS2 OHFC HPMC | ° Decreased viability of CCC cell line after plasma-activated medium treatment ° Induction of morphological changes in EOC cell lines treated with PAM ° Anti-tumour effects mediated by produced ROS ° Selective anti-proliferative effect on cancer cells without causing adverse reactions in normal cells | [75] |
Ovary | NOS2 NOS3 NOS2TR NOS2CR NOS3TR NOS3CR | ° Decreased viability of ovarian cancer cells treated with PAM in plasma activation time-dependent manner ° Treatment with PAM decreased proliferation rate of paclitaxel and cisplatin-resistant cells derived from parental cell lines ° Addition of ROS scavenger into activated medium decreases anticancer activity, the addition of ROS scavenger inhibitor re-established anticancer activity, thus this point on the crucial role of ROS in an anti-tumour mechanism | [76] |
Ovary | K2 K2R100 TOV-21G ES-2 | ° An anti-tumour effect of PAM on acquired chemo-resistant OC cells ° An anti-tumour effect of aqueous plasma against clear-cell carcinoma, which is natively chemo-refractory OC ° PAM has a selective cytotoxic effect on OC cells | [77] |
Ovary | SKOV3 HRA | ° Effective killing of ovarian cancer cells lines by the plasma, while plasma-treated fibroblast cells were not damaged ° Plasma treatment induces apoptosis ° The exposure time of treatment affects the proliferation rate | [78] |
Ovary | OVCAR-3 NOS2 TOV21G ES-2 | ° Negative impact of cell density on PAM-induced proliferation inhibition rate ° Selective, cell line dependent sensitivity to PAM ° Dependence of PAM effect on the proportion of ROS and the cell number ° Sensitivity to PAM affected by morphological characteristics of the cells ° TGF-β induced epithelial-mesenchymal morphological transition sensitised cancer cells to PAM | [11] |
Ovary | ES2 SKOV3 WI-38 HPMCs | ° Inhibition of cell viability of ovarian cancer cells depends on the cell type, cell number, and plasma-activated medium (PAM) dilution ratio ° PAM mediated suppression of cell migration, invasion, and adhesion ° PAM-induced down-regulation of matrix metalloproteinase-9 (MMP-9) prevents cell plantation in co-culture with human peritoneal mesothelial cells ° Inhibition of anti-metastatic effect of PAM by the ROS scavenger | [157] |
Breast | MCF-7 | ° CAP inhibitory effect on the cell proliferation is mediated by miR-19a-3p (miR-19a, oncomiR) ° CAP induces hypermethylation at the promoter CpG sites and subsequent downregulation of miR-19a ° CAP recovers production of ABCA1 and PTEN which are targets of miR-19a | [38] |
Breast | MCF-7 MCF-7/TamR | ° CAP induces restoration of sensitivity to tamoxifen (Tam) in Tam-resistant cells ° Increase of ROS levels in CAP-treated cells ° Inhibition of the proliferation and promotion of the apoptosis in MCF-7/TamR ° Oppositely altered expression of 20 genes involved in Tam resistance in TamR cells and CAP-treated TamR cells ° MX1 and HOXC6 mediated the restoration of sensitivity against Tam | [39] |
Breast | MSC MDA-MB-231 | ° Synergistic inhibition of breast cancer cell growth after treatment with the combination of CAP and drug (5FU) loaded core-shell nanoparticles ° Induction of down-regulation of metastasis-related genes (VEGF, MTDH, MMP9, and MMP2) ° Facilitation of the uptake of drug-loaded nanoparticles | [40] |
Breast | MCF7 MCF10A MTT | ° Reduction of the viability of breast cancer cells ° Significantly lower CAP-induced damage on normal cells ° Enhanced reduction of cancer cells viability after addition of 5% oxygen to the helium plasma | [41] |
Breast | metastatic BrCa cells MSC | ° CAP-induced selective ablation of metastatic BrCa cells in vitro without damaging healthy MSC ° Inhibition of the migration and invasion of BrCa cells after CAP treatment ° Different BrCa cell and MSC responses under varied CAP conditions | [42] |
Breast | MCF-7 | ° Induction of apoptosis in cultured human breast cancer cells ° Significant portion of CAP-treated cells exhibits apoptotic fragmentation, with only limited necrosis | [43] |
Breast | MDA-MB-231 MCF-7 HMEC | ° ROS in a liquid phase is generated via plasma irradiation of gas, producing the reactive species (electrons, ions, and radicals) and these species dissolve into the liquid phase and/or react with water ° Irradiation time, distance to the liquid surface and voltage affects OH radical generation in the extracellular culture medium | [44] |
Breast | MDAMB231 MDAMB468 MCF7 MCF10A | ° Induction of apoptosis, inhibition of the proliferation and migration of triple-negative breast cancers (TNBC) after PAM treatment ° Significant increase of H2O2 concentration in the media after CAP treatment ° PAM selectively inhibits the activity of JNK and NF-κB in TNBC cells | [55] |
Breast | 4T1 | ° Inhibition of cell migration after both plasma and doxorubicin treatment, assessed by wound healing assay | [56] |
Breast | MCF-7 MCF-7/TxR | ° Restoration of sensitivity to paclitaxel in resistant cells ° Identification of altered expression of multiple drug resistance-related genes ° DAGLA and CEACAM1 were essential for the acquisition of resistance and the recovery of sensitivity | [158] |
Anti-Cancer Potential of CAP | Cancer Types | Study Details | Reference | |
---|---|---|---|---|
Direct anti-tumour effects of CAP | Melanoma cells (Mel Im and Mel Juso) | → calcium influx → senescence | [264] | |
↑ acidification: → anti-cancer efficacy | [30] | |||
Melanoma cell A375 and A875 | → apoptosis (Sestrin2-mediated nitric oxide synthase signalling) | [151] | ||
Breast cancer cells MCF-7 | Opposite regulation of ZNRD1 and its lncRNA | [265] | ||
Ovarian cancer cells | ↓ growth and mobility | [73] | ||
Lung cancer cells A549 | Atmospheric pressure plasma irradiation: 8-oxoguanine formation DNA strand breaks | [247] | ||
Indirect anti-tumour effects of CAP (PAM) | Breast cancer cells SKBR3 | O3 formation | [266] | |
Triple negative breast cancer cells MDAMB231, MDAMB468 and Balb/c mice transplanted with MDAMB231 cells | → apoptosis ↓ proliferation, migration | [55] | ||
Ovarian cancer cells ES2 and Balb/c mice injected with ES2 | ↓ migration, invasion, adhesion ↓ metastatic potential ↓ MMP9 ↓ MAPK activation ↓ phosphorylation of JNK1/2 and p38 MAPK | [157] | ||
Gastric cancer cells SC-2-NU, AGS, GCIY-EGFP and peritoneal dissemination mouse model using GCIY-EGFP gastric cancer cells | ↓ migration, adhesion ↓ peritoneal metastatic modules | [267] | ||
Synergy of CAP and nanotechnology | CAP + iron oxide-based magnetic NPs | Lung cancer cells A549 and Balb/c mice injected with A549 cells | ↓ proliferation, viability → apoptosis ↓ xenograft tumours | [91] |
CAP + core-shell NPs | Breast cancer cells MDA-MB-231 | ↓ growth ↓ metastasis-related genes (VEGF. MTDH, MMP9, MMP2) → drug loaded NP uptake | [40] | |
CAP + silymarin nanoemulsion | Melanoma cells | → autophagy PI3K/mTOR and EGFR activation Modulation of transcription factors (ZKSCAN3, TFEB, FOXO1, CRTC2, and CREBBP) and autophagy-related genes (BECN-1, AMBRA-1, MAP1LC3A, and SQSTM) | [268] | |
CAP + PEG-coated gold NPs | Glioblastoma T98G and lung adenocarcinoma A549 and Balb/c female nude mice injected with glioma U87MG cells | PI3K/AKT blockage EMT reversion: ↑ E-cadherin ↓ N-cadherin, Slug, Zeb-1 | [269] | |
CAP + gold NPs | Colon cancer cells HCT-116 | ↓ cell deaths | [270] | |
CAP + platinum NPs | Human lymphoma U937 cells | Attenuated CAP-induced ROS-mediated apoptosis | [271] | |
CAP + gold NPs | Glioblastoma multiforme U373MG cells | → clathrin-dependent endocytosis to repair oxidised membrane → uptake of nanomaterial | [48] | |
CAP + gold NPs | Glioblastoma multiforme U373MG cells | Activation of NPs toxicity ↑ endocytosis ↑ trafficking to lysosomes | [272] | |
CAP + paclitaxel-loaded core-shell magnetic NPs | Non-small cell lung cancer cells A549 | ↓ growth | [273] |
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Zubor, P.; Wang, Y.; Liskova, A.; Samec, M.; Koklesova, L.; Dankova, Z.; Dørum, A.; Kajo, K.; Dvorska, D.; Lucansky, V.; et al. Cold Atmospheric Pressure Plasma (CAP) as a New Tool for the Management of Vulva Cancer and Vulvar Premalignant Lesions in Gynaecological Oncology. Int. J. Mol. Sci. 2020, 21, 7988. https://doi.org/10.3390/ijms21217988
Zubor P, Wang Y, Liskova A, Samec M, Koklesova L, Dankova Z, Dørum A, Kajo K, Dvorska D, Lucansky V, et al. Cold Atmospheric Pressure Plasma (CAP) as a New Tool for the Management of Vulva Cancer and Vulvar Premalignant Lesions in Gynaecological Oncology. International Journal of Molecular Sciences. 2020; 21(21):7988. https://doi.org/10.3390/ijms21217988
Chicago/Turabian StyleZubor, Pavol, Yun Wang, Alena Liskova, Marek Samec, Lenka Koklesova, Zuzana Dankova, Anne Dørum, Karol Kajo, Dana Dvorska, Vincent Lucansky, and et al. 2020. "Cold Atmospheric Pressure Plasma (CAP) as a New Tool for the Management of Vulva Cancer and Vulvar Premalignant Lesions in Gynaecological Oncology" International Journal of Molecular Sciences 21, no. 21: 7988. https://doi.org/10.3390/ijms21217988