Photodynamic effect of indocyanine green and its application to hepatocellular carcinoma treatment

Abstract

Hepatocellular carcinoma (HCC) stands as the primary cause of liver cancers, with limited treatment options outside of surgical resection or transplant. Photodynamic therapy (PDT) using indocyanine green (ICG) as a photosensitizer offers a promising therapeutic option for HCC. ICG PDT has demonstrated efficacy in vitro and in vivo, providing a safe treatment option for patients ineligible for resection or transplant. Challenges in PDT optimization include limited light delivery, poor photosensitizer optimization, and low oxygen generation. Innovative solutions, such as ICG incorporation into nanostructures and direct administration for HCC cases, show promise. Combining ICG PDT with Lentinula edodes mycelia (LEM) and hydrogen gas inhalation may address oxygen production limitations. Utilizing a combination of therapeutic approaches and therapies may increase the efficacy of ICG PDT, making it the safer and more effective treatment option for patients. ICG’s proven clinical safety may expedite potential approval for its use in PDT. Advancements in photosensitizer technology, such as aggregation-induced emission photosensitizers (AIE-PSs), and combination therapies will enhance PDT efficacy shortly, as developments show promise for improved outcomes. For HCC patients, ICG PDT presents a valuable therapeutic option. This work is novel because it explores new combination therapy approaches, leveraging the benefits of PDT with ICG and the developments in photosensitizer technology, nanotechnology, and the combination of other treatments such as LEM and hydrogen gas, which could potentially revolutionize the treatment of HCC and offer a better prognosis for patients.

Keywords

Biomarkers / cancer therapy / hepatocellular carcinoma / photodynamic therapy / indocyanine green / ICG / HCC / PDT

References

[1] Llovet JM,Villanueva A.Hepatocellular carcinoma.Nat Rev Dis Primers2021;7:6

[2] Asafo-Agyei KO. Hepatocellular carcinoma. Available from: http://www.ncbi.nlm.nih.gov/books/NBK559177/ [Last accessed on 8 Apr 2024]

[3] Balogh J,Asham EH.Hepatocellular carcinoma: a review.J Hepatocell Carcinoma2016;3:41-53 PMCID:PMC5063561

[4] Colagrande S,Taliani GG,Inghilesi AL.Advanced hepatocellular carcinoma and sorafenib: diagnosis, indications, clinical and radiological follow-up.World J Hepatol2015;7:1041-53 PMCID:PMC4450181

[5] Allaire M,Lim C,Wagner M.New frontiers in liver resection for hepatocellular carcinoma.JHEP Rep2020;2:100134 PMCID:PMC7360891

[6] Belghiti J.Surgical treatment of hepatocellular carcinoma.HPB2005;7:42-9 PMCID:PMC2023921

[7] Madkhali AA,Aljiffry MM.Surgical treatment for hepatocellular carcinoma.Saudi J Gastroenterol2015;21:11-7 PMCID:PMC4355856

[8] Olthoff KM.Surgical options for hepatocellular carcinoma: resection and transplantation.Liver Transpl Surg1998;4:S98-104.

[9] Chapman WC,Hemming A.Surgical treatment of hepatocellular carcinoma in North America: can hepatic resection still be justified?.J Am Coll Surg2015;220:628-37

[10] Vogel A,Sapisochin G,Saborowski A.Hepatocellular carcinoma.Lancet2022;400:1345-62

[11] Pravisani R,Isola M.Impact of surgical complications on the risk of hepatocellular carcinoma recurrence after hepatic resection.Updates Surg2018;70:57-66

[12] Kaneko J,Inagaki Y.Innovative treatment for hepatocellular carcinoma (HCC).Transl Gastroenterol Hepatol2018;3:78 PMCID:PMC6232072

[13] Shirata C,Inagaki Y.Near-infrared photothermal/photodynamic therapy with indocyanine green induces apoptosis of hepatocellular carcinoma cells through oxidative stress.Sci Rep2017;7:13958 PMCID:PMC5654824

[14] Yao S,Ma J,Chen H.Precise right hemihepatectomy for the treatment of hepatocellular carcinoma guided by fusion ICG fluorescence imaging.J Cancer2020;11:2465-75 PMCID:PMC7066014

[15] Sebagh M,Feray C.Indocyanine green fluorescence patterns of hepatocellular carcinoma correlate with pathological and molecular features.HPB2023;25:198-209

[16] Huang SW,Wong HP.The use of indocyanine green imaging technique in patient with hepatocellular carcinoma.Transl Gastroenterol Hepatol2018;3:95 PMCID:PMC6286918

[17] Liu F,Ma W.Short- and long-term outcomes of indocyanine green fluorescence navigation- versus conventional-laparoscopic hepatectomy for hepatocellular carcinoma: a propensity score-matched, retrospective, cohort study.Ann Surg Oncol2023;30:1991-2002 PMCID:PMC10027802

[18] Urade T,Iwatani Y.Laparoscopic anatomical liver resection using indocyanine green fluorescence imaging.Asian J Surg2020;43:362-8

[19] Qian X,Gao L.Trans-arterial positive ICG staining-guided laparoscopic liver watershed resection for hepatocellular carcinoma.Front Oncol2022;12:966626 PMCID:PMC9354495

[20] Nanashima A,Imamura N,Hamada T.Recent advances in photodynamic imaging and therapy in hepatobiliary malignancies: clinical and experimental aspects.Curr Oncol2021;28:4067-79 PMCID:PMC8534451

[21] Park JS,Park SJ.Synergistic effects of concurrent photodynamic therapy with indocyanine green and chemotherapy in hepatocellular carcinoma cell lines and mouse models.J Photochem Photobiol B2023;239:112642

[22] Wang Q,Yuan JP.Targeting therapy of hepatocellular carcinoma with doxorubicin prodrug PDOX increases anti-metastatic effect and reduces toxicity: a preclinical study.J Transl Med2013;11:192 PMCID:PMC3765954

[23] Zhang Z,Miyake K.A novel patient-derived orthotopic xenograft (PDOX) mouse model of highly-aggressive liver metastasis for identification of candidate effective drug-combinations.Sci Rep2020;10:20105 PMCID:PMC7676248

[24] Hong F,Kim SW,Kim SK.Near-infrared phototherapy for patient-derived orthotopic xenograft model of hepatocellular carcinoma in combination with indocyanine green.J Photochem Photobiol B2020;209:111938

[25] Hu B,Guo W.Establishment of a hepatocellular carcinoma patient-derived xenograft platform and its application in biomarker identification.Int J Cancer2020;146:1606-17

[26] Zhang Y,Sun X.Establishment of a murine breast tumor model by subcutaneous or orthotopic implantation.Oncol Lett2018;15:6233-40 PMCID:PMC5876452

[27] Kumar A,Mordon S,Boleslawski E.Could photodynamic therapy be a promising therapeutic modality in hepatocellular carcinoma patients? A critical review of experimental and clinical studies.Cancers2021;13:5176 PMCID:PMC8534013

[28] Peng Z,Huang S.Photoimmunotherapy: a new paradigm in solid tumor immunotherapy.Cancer Control2022;29:107327482210888 PMCID:PMC9016614

[29] Sevieri M,Bonizzi A.Indocyanine green nanoparticles: are they compelling for cancer treatment?.Front Chem2020;8:535 PMCID:PMC7378786

[30] Gunaydin G,Ayan S.Photodynamic therapy-current limitations and novel approaches.Front Chem2021;9:691697 PMCID:PMC8223074

[31] Sun B,Zhang Y.Advanced techniques for performing photodynamic therapy in deep-seated tissues.Biomaterials2022;291:121875

[32] Dinakaran D.The use of nanomaterials in advancing photodynamic therapy (PDT) for deep-seated tumors and synergy with radiotherapy.Front Bioeng Biotechnol2023;11:1250804 PMCID:PMC10577272

[33] Bae KH,Park TG.Nanomaterials for cancer therapy and imaging.Mol Cells2011;31:295-302 PMCID:PMC3933969

[34] Kamkaew A,Goel S.Cerenkov radiation induced photodynamic therapy using chlorin e6-loaded hollow mesoporous silica nanoparticles.ACS Appl Mater Interfaces2016;8:26630-7 PMCID:PMC5061626

[35] Du W,Luo Q.Optical molecular imaging for systems biology: from molecule to organism.Anal Bioanal Chem2006;386:444-57 PMCID:PMC1592253

[36] Kim J,Yoon H,Rhew K.The in vitro and in vivo anticancer effect of photomed for photodynamic therapy: comparison with photofrin and radachlorin.Curr Issues Mol Biol2023;45:2474-90 PMCID:PMC10047247

[37] Cuenca RE,Sibata C.Breast cancer with chest wall progression: treatment with photodynamic therapy.Ann Surg Oncol2004;11:322-7

[38] Zhao H,Feng C.Tailoring aggregation extent of photosensitizers to boost phototherapy potency for eliciting systemic antitumor immunity.Adv Mater2022;34:e2106390

[39] Tseng HC,Liao WT,Hsiao JK.Indocyanine green as a near-infrared theranostic agent for ferroptosis and apoptosis-based, photothermal, and photodynamic cancer therapy.Front Mol Biosci2022;9:1045885 PMCID:PMC9768228

[40] Sekar R,Thathapudi JJ.Recent progress of gold-based nanostructures towards future emblem of photo-triggered cancer theranostics: a special focus on combinatorial phototherapies.Pharmaceutics2023;15:433 PMCID:PMC9963714

[41] Mahmut Z,Ruan F.Medical applications and advancement of near infrared photosensitive indocyanine green molecules.Molecules2023;28:6085 PMCID:PMC10459369

[42] Li B,Li T.Ultra-small gold nanoparticles self-assembled by gadolinium ions for enhanced photothermal/photodynamic liver cancer therapy.J Mater Chem B2021;9:1138-50

[43] Chuang CC,Wang YY.Stem cell-based delivery of gold/chlorin e6 nanocomplexes for combined photothermal and photodynamic therapy.ACS Appl Mater Interfaces2020;12:30021-30

[44] Qi S,Liu G.Plasmonic-doped melanin-mimic for CXCR4-targeted NIR-II photoacoustic computed tomography-guided photothermal ablation of orthotopic hepatocellular carcinoma.Acta Biomater2021;129:245-57

[45] Ni J,Zhang H,Tang BZ.Aggregation-induced generation of reactive oxygen species: mechanism and photosensitizer construction.Molecules2021;26:268 PMCID:PMC7827197

[46] Meng Z,Wang T.Aggregation-induced emission photosensitizer-based photodynamic therapy in cancer: from chemical to clinical.J Nanobiotechnology2022;20:344 PMCID:PMC9327335

[47] Teng M,Xie Y.Bright near-infrared aggregation-induced emission dots for long-term bioimaging in vitro/vivo.Dyes Pigments2021;195:109679

[48] Xia Q,Zhou Y.Near-infrared organic fluorescent nanoparticles for long-term monitoring and photodynamic therapy of cancer.Nanotheranostics2019;3:156-65 PMCID:PMC6470342

[49] Trevisani F,Garuti F.Metronomic capecitabine as second-line treatment for hepatocellular carcinoma after sorafenib discontinuation.J Cancer Res Clin Oncol2018;144:403-14

[50] Granito A,Terzi E.Metronomic capecitabine as second-line treatment in hepatocellular carcinoma after sorafenib failure.Dig Liver Dis2015;47:518-22

[51] Ma Z,Ji G,Han W.Facile construction of dual-drug loaded nanoparticles for improvement synergistic chemotherapy in prostate cancer.Int J Polym Mater Polym Biomater2023;72:856-66

[52] Yorozu K,Kimura S.Experience with photodynamic therapy using indocyanine green liposomes for refractory cancer.J Pers Med2022;12:1039 PMCID:PMC9318386

[53] Gu Z,Van der Maaden K,Cruz LJ.Liposome-based drug delivery systems in cancer immunotherapy.Pharmaceutics2020;12:1054 PMCID:PMC7694212

[54] Inagaki FF,Ito K,Kurokawa T.Intraoperative indocyanine green fluorescence navigation facilitates complete removal of lymph node metastases from hepatocellular carcinoma.Glob Health Med2021;3:406-8 PMCID:PMC8692099

[55] Chow AK,Ng L.Novel molecular targets in hepatocellular carcinoma.World J Clin Oncol2020;11:589-605 PMCID:PMC7443834

[56] Hoshida Y,Tanabe KK.Prevention of hepatocellular carcinoma: potential targets, experimental models, and clinical challenges.Curr Cancer Drug Targets2012;12:1129-59 PMCID:PMC3776581

[57] Chen Z,Hu M.Recent progress in treatment of hepatocellular carcinoma.Am J Cancer Res2020;10:2993-3036. PMCID:PMC7539784

[58] Chakraborty E.Emerging therapies for hepatocellular carcinoma (HCC).Cancers2022;14:2798 PMCID:PMC9179883

[59] Tsuda T,Hishikawa H.Near-infrared fluorescence imaging and photodynamic therapy with indocyanine green lactosome has antineoplastic effects for hepatocellular carcinoma.PLoS One2017;12:e0183527 PMCID:PMC5578495

[60] Qi S,Chen J.Targeted multifunctional nanoplatform for imaging-guided precision diagnosis and photothermal/photodynamic therapy of orthotopic hepatocellular carcinoma.Int J Nanomed2022;17:3777-92 PMCID:PMC9440712

[61] Shemesh CS,Yu DS,Zhang H.Indocyanine green loaded liposome nanocarriers for photodynamic therapy using human triple negative breast cancer cells.Photodiagnosis Photodyn Ther2014;11:193-203

[62] Kita K,Ito T.Photodynamic therapy of rat liver cancer: protection of the normal liver by indocyanine green.Gastroenterol Jpn1987;22:465-73