Optical diagnostic imaging and therapy for thyroid cancer

Abstract

Thyroid cancer, as one of the most common endocrine cancers, has seen a surge in incidence in recent years. This is most likely due to the lack of specificity and accuracy of its traditional diagnostic modalities, leading to the overdiagnosis of thyroid nodules. Although there are several treatment options available, they are limited to surgery and ¹³¹I radiation therapy that come with significant side effects and hence cannot meet the treatment needs of anaplastic thyroid carcinoma with very high malignancy. Optical imaging that utilizes optical absorption, refraction and scattering properties, not only observes the structure and function of cells, tissues, organs, or even the whole organism to assist in diagnosis, but can also be used to perform optical therapy to achieve targeted non-invasive and precise treatment of thyroid cancer. These applications of screening, diagnosis, and treatment, lend to optical imaging's promising potential within the realm of thyroid cancer surgical navigation. Over the past decade, research on optical imaging in the diagnosis and treatment of thyroid cancer has been growing year by year, but no comprehensive review on this topic has been published. Here, we review key advances in the application of optical imaging in the diagnosis and treatment of thyroid cancer and discuss the challenges and potential for clinical translation of this technology.

Keywords: 131I-BSA@CuS, 131I-labeled BSA-modified CuS nanoparticles; 5-ALA, 5-Aminolevulinic acid; ASIR, age-standardized rates of cancer incidence; ATC, anaplastic thyroid carcinoma; Au@MSNs, photo-triggered Gold nanodots capped mesoporous silica nanoparticles; AuNCs@BSA-I, innovative iodinated gold nanoclusters; BRAF, V-Raf murine sarcoma viral oncogene homolog B; CBDCA, Carboplatin; CDFI, color doppler flow imaging ultrasound; CLND, central compartmentalized node dissection; CPDA-131I NPs, the 131I-radiolabeled cerebroid polydopamine nano-particles; CT, Computed Tomography; DOT, Diffuse Optical Tomography; DTC, differentiated thyroid cancer; ECDT, enhanced chemodynamical therapy; EGF, epidermal growth factor; EGFR, epidermal growth factor receptor; ESMO, European Society of Medical Oncology; FDA, U.S. Food and Drug Administration; FI, fluorescence imaging; FNAB, fine-needle aspiration biopsy; FNAs, fine needle aspirations; FTC, follicular thyroid carcinoma; GC, germinal center; HAOA, Hyaluronic Acid and Oleic Acid; HYP, hypericin; ICG, indocyanine green; IJV, internal jugular vein; IR825@B-PPNs, Polymeric NPs with bevacizumab and IR825 conjugated on the surface; L-A PTA, laparoscopic photothermal ablation; MDR, multidrug resistance; MTC, medullary thyroid carcinoma; Multimodal therapy; NIR, near-infrared; NIR-FI, near-infrared fluorescence imaging; NIR-PIT, near-infrared photoimmunotherapy; NIRF, near-infrared fluorescence; NMRI, Nuclear Magnetic Resonance Imaging; OCT, Optical Coherence Tomography; OI, optical imaging; OS, overall survival; Optical imaging; Optical imaging-guided surgery; PAI, Photoacoustic Imaging; PDT, photodynamic therapy; PET, Positron Emission Tomography; PGs, parathyroid glands; PLP, porphyrin-HDL nanoparticle; PTA, photothermal reagents; PTC, papillary thyroid carcinoma; PTT, photothermal therapy; Pd-MOF, porphyrin–palladium metal–organic framework; Phototherapy; RIT, radioactive iodine therapy; ROS, reactive oxygen species; SEC, Selenocysteine; SV, subclavian vein; SiRNA, interfering RNA; TC, thyroid cancer; TD, Thoracic Duct; TF, tissue factor; Thyroid cancer; mETE, microscopic extrathyroidal extension.

Graphical abstract

Scheme 1

Schematic diagram of fluorescence imaging.

Scheme 2

The light from the source is divided into two paths, namely the two arms of the interferometer (the reference arm and the sample arm). In the reference arm, the mirror reflects light. In the sample arm, light has three paths, scattering, absorbing and returning to the source (backscattering). By comparing and analyzing the backscattered light signal of the sample arm and the reference arm, the image is finally obtained.

Fig. 1

Hyperplastic nodules (A & B); lymphocytic thyroiditis (C & D); classic variation of PTC (E & F); solid variant of PTC (G & H); follicular variant of PTC (I & J); and thyroid adenoma (K & L) histological and OCT appearances [37] (Reproduced from Ref. [37] with permission. Copyright 2019 Wiley Periodicals, Inc.).

Scheme 3

Using different wavelengths of near-infrared light to illuminate the tissue, the ultrasound signal is generated after different light pulses. Photoacoustic images are generated by the reconstruction of photoacoustic signals.

Fig. 2

Dual-mode imaging (PAI combined with FI). The NIR-II fluorescence images (A) of epidermal growth factor receptor (EGFR)-positive FTC-133 tumor-bearing mice were captured before injection and 1, 4, 24, and 48 ​h after tail vein injection of Affibody-DAPs, respectively. The blocking group was co-injected with Affibody ZEGFR:1904 and Affibody-DAPs. (Images of both groups using the same acquisition parameters.) Coronal views of the 3D volume rendering of the PAI (B) of the FTC-133 tumors were obtained at the predefined time intervals right after FI. White dashed lines and white arrows indicate tumors [25] (Reproduced from Ref. [25] with permission. Copyright 2017 American Chemical Society).

Scheme 4

Schematic diagram of diffuse optical tomography.

Fig. 3

Thermal efficacy of IR825@B-PPNs (A), CPDA-¹³¹I NPs (B), ¹³¹I-BSA@CuS (C), B–OMe-NPs (D), PPR_ILK (E) [[52], [53], [54], [55], [56]]. The temperature fluctuation curves of the indocyanine green (ICG) solution and IR825@B-PPNs after four photothermal heating cycles (A1). The different power-density irradiation (A2) (Reproduced from Ref. [52] with permission. Copyright 2019 Acta Materialia Inc. Published by Elsevier Ltd). The five photothermal cycles of BSA@CuS's temperature fluctuations (B1). The images of the photothermal heating curve at various light intensities (B2) (Reproduced from Ref. [54] with permission. Copyright 2022 International Union of Biochemistry and Molecular Biology). Time-dependent temperature variation of B–OMe-NPs at different laser powers (C1). Photothermal cycle of BOMe-NPs and ICG solutions during laser irradiation (C2) (Reproduced from Ref. [55] with permission. Copyright 2022, American Chemical Society). Heating curves of PPRNC in gradient concentrations during 10 ​min of laser irradiation (D1). Temperature changes in PPRNC during three laser irradiating and natural cooling-down cycles (D2) (Reproduced from Ref. [56] with permission. Copyright 2022, American Chemical Society). (For interpretation of the references to colour in this figure legend, the reader is referred to the Web version of this article.)

Fig. 4

The schematic representation of the multimodal nano-platform: H₂ mediated cascade enhancing synergetic treatment [74].

Fig. 5

In vivo NIR imaging of organs from B (A). After receiving a single dosage of NIR NPs, a BRAFV600E-mutated 8505C tumor-bearing animal showed time-dependent FI (B) [81] (Reproduced from Ref. [81] with permission. Copyright 2022 National Academy of Science).

Fig. 6

Serial FI following injection of IRDye 800CW-ALT-836 and image-guided tumor removal seven days later. In vitro fluorescent imaging, strong fluorescent signals were seen in the tumor, but not in the other organs. Blue dashed circles indicated the tumor [92] (Reproduced from Ref. [92] with permission. Copyright 2020 The Authors. Published by WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim). (For interpretation of the references to colour in this figure legend, the reader is referred to the Web version of this article.)

Fig. 7

A description of the intrinsic fluorescence observed in both normal lymph nodes and formalin-fixed PTC nodal metastases under quantitative spectroscopy conditions [96]. (Reproduced from Ref. [96] with permission. Copyright 2022 The Author(s). Published by Springer Nature).

Fig. 8

Papillary architecture (A1 & A2) (arrows) and follicular architecture (B1 & B2) (arrows) are observed in histological and OCT appearances of metastatic PTC to lymph nodes. Homogeneous parenchyma and vessels (C1 & C2) (arrow) are observed in histopathological and OCT of the benign lymph node [37] (Reproduced from Ref. [37] with permission. Copyright © 2019 Wiley Periodicals, Inc).

Fig. 9

Patient undergoing subtotal parathyroidectomy. Residual parathyroid gland (arrow) (A). Greyscale ICGA demonstrating excellent residual perfusion (B). Green ICGA fluorescence of residual parathyroid (C & D) [100] (Reproduced from Ref. [100] with permission. Copyright 2019 Elsevier Ltd). (For interpretation of the references to colour in this figure legend, the reader is referred to the Web version of this article.)

Fig. 10

NIR imaging of thoracic ducts for patients #4 and #5 [109]. (IJV: internal jugular vein; SV: subclavian vein; TD: thoracic duct) (Reproduced from Ref. [109] with permission. Copyright 2018, Society of Surgical Oncology).