Characterization and photothermal effect of indocyanine green encapsulated poly lactic acid-co-glycolic acid microspheres

doi:10.12307/2023.032

Abstract

Abstract: BACKGROUND: Indocyanine green, an efficient photothermal conversion agent, can be used for photothermal therapy of oral squamous cell carcinoma, but it has some shortcomings such as water instability and photodegradation. Using a carrier to encapsulate indocyanine green to improve its stability was of great significance for exploring photothermal therapy of oral squamous cell carcinoma.
OBJECTIVE: Indocyanine green encapsulated poly lactic acid-co-glycolic acid microspheres were fabricated to delay the photodegradation of indocyanine green and improve its photothermal stability.
METHODS: (1) The indocyanine green encapsulated poly lactic acid-co-glycolic acid microspheres were prepared by emulsion-solvent evaporation method. The morphology, particle size distribution, surface charge, drug loading and encapsulation efficiency were characterized. (2) The free indocyanine green solution and the indocyanine green microsphere suspension were irradiated with near-infrared light at different mass concentrations (0.6, 0.8, 1.0, 1.2 g/L) for 5 minutes to investigate the temperature changes of the solutions. The free indocyanine green solution and the indocyanine green microsphere suspension were exposed to natural light for 0, 3, 6, and 9 days at a mass concentration of 1.0 g/L to observe the temperature changes within 5 minutes of near-infrared light irradiation. The free indocyanine green solution and the indocyanine green microsphere suspension were subjected to four on-off laser irradiation cycles at a mass concentration of 1.0 g/L to investigate the temperature changes of the solutions. (3) The tongue squamous cell carcinoma cell line SCC-25 was inoculated in a 48-well plate and cultured in eight groups: control group, blank microsphere group, 1.0 g/L free indocyanine green group, 1.0 g/L indocyanine green microsphere group, near-infrared light group, blank microsphere+near-infrared light group, 1.0 g/L free indocyanine green+near-infrared light group, and 1.0 g/L indocyanine green microsphere+near-infrared light group. After 12 hours of treatment, cell viability was detected by CCK-8 assay.
RESULTS AND CONCLUSION: (1) The indocyanine green microspheres had smooth surfaces with particle sizes of (2.54±0.29) μm and zeta potential of −(20.2±1.58) mV. Encapsulation efficiency and loading efficiency were (69.24±1.29)% and (4.87±0.15)%, respectively. (2) Free indocyanine green and indocyanine green microspheres had similar photothermal conversion ability, but after increasing the number of laser irradiation or storage without light, the photothermal conversion ability of free indocyanine green obviously decreased compared with indocyanine green microspheres. (3) The SCC-25 cells in the 1.0 g/L free indocyanine green+near-infrared light group and the 1.0 g/L indocyanine green microsphere+near-infrared light group shrank to a spherical shape, and the cell viability of the two groups was lower than that of the control group (P < 0.001). (4) Indocyanine green microspheres possess efficient photothermal conversion ability and can obviously delay photobleaching and photodegradation of indocyanine green.

Key words: poly lactic acid-co-glycolic acid, indocyanine green, microsphere, oral squamous cell carcinoma, photothermal therapy, SSC-25 cell, near-infrared, emulsion-solvent evaporation method

CLC Number:

Fan Yaru, Li Ruixin, Li Fengji, Luo Rui, Liu Hao, Yan Yingbin. Characterization and photothermal effect of indocyanine green encapsulated poly lactic acid-co-glycolic acid microspheres[J]. Chinese Journal of Tissue Engineering Research, 2023, 27(12): 1817-1823.

Figures/Tables 5

References

[1] YANAMOTO S, DENDA Y, OTA Y, et al. Postoperative adjuvant therapy for patients with loco-regionally advanced oral squamous cell carcinoma who are at high risk of recurrence. Int J Oral Maxillofac Surg. 2020;49(7):848-853.
[2] KORDZINSKA-CISEK I, GRZYBOWSKA-SZATKOWSKA L. Complications of radio- and radiochemotherapy in patients undergoing major salivary gland cancer surgery. Otolaryngol Pol. 2019;73(3):26-31.
[3] LIU Y, BHATTARAI P, DAI Z, et al. Photothermal therapy and photoacoustic imaging via nanotheranostics in fighting cancer. Chem Soc Rev. 2019;48(7):2053-2108.
[4] LONG S, XU Y, ZHOU F, et al. Characteristics of temperature changes in photothermal therapy induced by combined application of indocyanine green and laser. Oncol Lett. 2019;17(4):3952-3959.
[5] CHEN J, LI Q, WANG F, et al. Biosafety, Nontoxic Nanoparticles for VL-NIR Photothermal Therapy Against Oral Squamous Cell Carcinoma. ACS Omega. 2021;6(17):11240-11247.
[6] LAU CT, AU DM, WONG K. Application of indocyanine green in pediatric surgery. Pediatr Surg Int. 2019;35(10):1035-1041.
[7] HIROHASHI K, ANAYAMA T, WADA H, et al. Lung cancer photothermal ablation by low-power near-infrared laser and topical injection of indocyanine green. Interact Cardiovasc Thorac Surg. 2019;29(5):693-698.
[8] LIU C, RUAN C, SHI R, et al. A near infrared-modulated thermosensitive hydrogel for stabilization of indocyanine green and combinatorial anticancer phototherapy. Biomater Sci. 2019;7(4):1705-1715.
[9] HWANG J, JIN J. Attachable Hydrogel Containing Indocyanine Green for Selective Photothermal Therapy against Melanoma. Biomolecules (Basel, Switzerland). 2020;10(8):1124.
[10] SAXENA V, SADOQI M, SHAO J. Degradation kinetics of indocyanine green in aqueous solution. J Pharm Sci. 2003;92(10):2090-2097.
[11] OTT P. Hepatic elimination of indocyanine green with special reference to distribution kinetics and the influence of plasma protein binding. Pharmacol Toxicol. 1998;83 Suppl 2:1-48.
[12] WU L, FANG S, SHI S, et al. Hybrid polypeptide micelles loading indocyanine green for tumor imaging and photothermal effect study. Biomacromolecules. 2013;14(9):3027-3033.
[13] MIRANDA D, WAN C, KILIAN HI, et al. Indocyanine green binds to DOTAP liposomes for enhanced optical properties and tumor photoablation. Biomater Sci. 2019;7(8):3158-3164.
[14] WANG Y, NIU C, FAN S, et al. Indocyanine Green Loaded Modified Mesoporous Silica Nanoparticles as an Effective Photothermal Nanoplatform. Int J Mol Sci. 2020;21(13):4789.
[15] MAKADIA HK, SIEGEL SJ. Poly Lactic-co-Glycolic Acid (PLGA) as Biodegradable Controlled Drug Delivery Carrier. Polymers (Basel). 2011;3(3):1377-1397.
[16] TAN H, HUANG D, LAO L, et al. RGD modified PLGA/gelatin microspheres as microcarriers for chondrocyte delivery. J Biomed Mater Res B Appl Biomater. 2009;91(1):228-238.
[17] RAFIEI P, HADDADI A. Docetaxel-loaded PLGA and PLGA-PEG nanoparticles for intravenous application: pharmacokinetics and biodistribution profile. Int J Nanomedicine. 2017;12:935-947.
[18] CHOI S, LEE SH, PARK S, et al. Indocyanine Green-Loaded PLGA Nanoparticles Conjugated with Hyaluronic Acid Improve Target Specificity in Cervical Cancer Tumors. Yonsei Med J. 2021;62(11):1042-1051.
[19] CHEN HH, LU IL, LIU TI, et al. Indocyanine green/doxorubicin-encapsulated functionalized nanoparticles for effective combination therapy against human MDR breast cancer. Colloids Surf B Biointerfaces. 2019;177:294-305.
[20] SAXENA V, SADOQI M, SHAO J. Indocyanine green-loaded biodegradable nanoparticles: preparation, physicochemical characterization and in vitro release. Int J Pharm. 2004;278(2):293-301.
[21] LI Y, PEI Y, ZHANG X, et al. PEGylated PLGA nanoparticles as protein carriers: synthesis, preparation and biodistribution in rats. J Control Release. 2001;71(2):203-211.
[22] LAN M, ZHU L, WANG Y, et al. Multifunctional nanobubbles carrying indocyanine green and paclitaxel for molecular imaging and the treatment of prostate cancer. J Nanobiotechnology. 2020;18(1):121.
[23] HOUTHOOFD S, VUYLSTEKE M, MORDON S, et al. Photodynamic therapy for atherosclerosis. The potential of indocyanine green. Photodiagnosis Photodyn Ther. 2020;29:101568.
[24] YOON HJ, LEE HS, LIM JY, et al. Liposomal Indocyanine Green for Enhanced Photothermal Therapy. ACS Appl Mater Interfaces. 2017; 9(7):5683-5691.
[25] SAXENA V, SADOQI M, SHAO J. Enhanced photo-stability, thermal-stability and aqueous-stability of indocyanine green in polymeric nanoparticulate systems. J Photochem Photobiol B. 2004;74(1):29-38.
[26] Reinhart MB, Huntington CR, Blair LJ, et al. Indocyanine Green: Historical Context, Current Applications, and Future Considerations. Surg Innov. 2016;23(2):166-175.
[27] 余柳丹,罗一帆,陈小菊,等.吲哚菁绿稳定性及光敏性和声敏性研究[J].化学研究与应用,2016,28(3):400-403.
[28] LIM HJ, CHIOW A, LEE LS, et al. Novel method of intraoperative liver tumour localisation with indocyanine green and near-infrared imaging. Singapore Med J. 2021;62(4):182-189.
[29] WANG Q, SHEN M, LI W, et al. Controlled-release of fluazinam from biodegradable PLGA-based microspheres. J Environ Sci Health B. 2019; 54(10):810-816.
[30] LIU Z, YE W, ZHENG J, et al. Hierarchically electrospraying a PLGA@chitosan sphere-in-sphere composite microsphere for multi-drug-controlled release. Regen Biomater. 2020;7(4):381-390.
[31] GAIGNAUX A, REEFF J, DE VRIESE C, et al. Evaluation of the degradation of clonidine-loaded PLGA microspheres. J Microencapsul. 2013;30(7): 681-691.
[32] HAN S, ZHANG X, LI M. Progress in research and application of PLGA embolic microspheres. Front Biosci (Landmark Ed). 2016;21:931-940.
[33] ABULATEEFEH SR, ALKAWAREEK MY, ABDULLAH FR, et al. Preparation of Aqueous Core-Poly(d,l-Lactide-co-Glycolide) Shell Microcapsules With Mononuclear Cores by Internal Phase Separation: Optimization of Formulation Parameters. J Pharm Sci. 2017;106(4):1136-1142.
[34] PALAZZO I, LAMPARELLI EP, CIARDULLI MC, et al. Supercritical emulsion extraction fabricated PLA/PLGA micro/nano carriers for growth factor delivery: Release profiles and cytotoxicity. Int J Pharm. 2021;592:120108.
[35] SHI NQ, ZHOU J, WALKER J, et al. Microencapsulation of luteinizing hormone-releasing hormone agonist in poly (lactic-co-glycolic acid) microspheres by spray-drying. J Control Release. 2020;321:756-772.
[36] Ohta S, Matsuura M, Kawashima Y, et al. Facile fabrication of PEG-coated PLGA microspheres via SPG membrane emulsification for the treatment of scleroderma by ECM degrading enzymes. Colloids Surf B Biointerfaces. 2019;179:453-461.
[37] WU B, WU L, HE Y, et al. Engineered PLGA microspheres for extended release of brexpiprazole: in vitro and in vivo studies. Drug Dev Ind Pharm. 2021;47(6):1001-1010.
[38] GASPAR MC, PAIS A, SOUSA J, et al. Development of levofloxacin-loaded PLGA microspheres of suitable properties for sustained pulmonary release. Int J Pharm. 2019;556:117-124.
[39] BUTREDDY A, GADDAM RP, KOMMINENI N, et al. PLGA/PLA-Based Long-Acting Injectable Depot Microspheres in Clinical Use: Production and Characterization Overview for Protein/Peptide Delivery. Int J Mol Sci. 2021;22(16):8884.
[40] ZHAI P, CHEN XB, SCHREYER DJ. PLGA/alginate composite microspheres for hydrophilic protein delivery. Mater Sci Eng C Mater Biol Appl. 2015; 56:251-259.
[41] PARK JS, YANG HN, JEON SY, et al. The use of anti-COX2 siRNA coated onto PLGA nanoparticles loading dexamethasone in the treatment of rheumatoid arthritis. Biomaterials. 2012;33(33):8600-8612.
[42] LIU R, MA GH, WAN YH, et al. Influence of process parameters on the size distribution of PLA microcapsules prepared by combining membrane emulsification technique and double emulsion-solvent evaporation method. Colloids Surf B Biointerfaces. 2005;45(3-4):144-153.
[43] KONAN YN, CERNY R, FAVET J, et al. Preparation and characterization of sterile sub-200 nm meso-tetra(4-hydroxylphenyl)porphyrin-loaded nanoparticles for photodynamic therapy. Eur J Pharm Biopharm. 2003; 55(1):115-124.
[44] JAQUE D, MARTINEZ ML, DEL RB, et al. Nanoparticles for photothermal therapies. Nanoscale. 2014;6(16):9494-9530.