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Nano Research 2023, 16(12): 13226-13249 https://doi.org/10.1007/s12274-023-6364-9
Review Article | Issue | Published: 14 December 2023

Nanomaterials for visualized tumor surgical navigation and postoperative recurrence inhibition

Show Author's Information Fuming Liang1,2,§,  Qing You1,§,  Hongjiang Ye2,§,  Wenqiao Fu2,  Xiaopeng Ma3,  Jiahe Tan2,  Yinrui Ma2,  Chen Wang1,  Yanlian Yang1( ),  Zhaohui He2( ),  Ling Zhu1( )
CAS Key Laboratory of Standardization and Measurement for Nanotechnology, CAS Key Laboratory for Biomedical Effects of Nanomaterials and Nanosafety, CAS Center for Excellence in Nanoscience, National Center for Nanoscience and Technology, Beijing 100190, China
Department of Neurosurgery, The First Affiliated Hospital of Chongqing Medical University, Chongqing 400016, China
The First Affiliated Hospital University of Science and Technology of China, Anhui Provincial Hospital, Hefei 230000, China

§ Fuming Liang, Qing You, and Hongjiang Ye contributed equally to this work.

Keywords:
nanomaterials, surgical navigation, tumor recurrence inhibition, tumor resection
Topics:
Theranostics
Cite this article:
Liang F, You Q, Ye H, et al. Nanomaterials for visualized tumor surgical navigation and postoperative recurrence inhibition. Nano Research, 2023, 16(12): 13226-13249. https://doi.org/10.1007/s12274-023-6364-9
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Abstract Full text About this article

Preoperative localization of the tumor sites and intraoperative real-time monitoring are essential for precise surgery but are meanwhile challenging due to the lack of high-resolution, easy-to-operate, and fast visualization techniques. On the other hand, tumor recurrence and metastasis after surgery greatly reduce the survival rate of patients. Intervening tumor recurrence during surgery is a future direction of tumor treatment. Nanomaterials with external condition responsiveness (light, ultrasound, and magnetic field) can accurately assist intraoperative detection and surgical resection due to their functions such as tumor cell targeting, fluorescence imaging, and real time monitoring, providing a more accurate, shorter duration, and visualization method of surgical resection. Moreover, nanomaterials are versatile and can easily be tailored for application in different tumors. Locally filled or systemically circulating nanomaterials with slow drug release and residual tumor cell-targeting ability have promising applications in inhibiting tumor recurrence. Here, we review surgical navigation and postoperative recurrence interventional nanomaterials and their landscape in guiding tumor treatment. We summarize the classification and characteristics of these nanomaterials and discuss their application in the surgical navigation and recurrence inhibition of different tumors. We also provide an outlook on the challenges and future development of nanomaterials for visualized tumor surgical navigation and postoperative recurrence inhibition.


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About this article

Nanomaterials for visualized tumor surgical navigation and postoperative recurrence inhibition

Show Author's information Fuming Liang1,2,§, Qing You1,§, Hongjiang Ye2,§, Wenqiao Fu2, Xiaopeng Ma3, Jiahe Tan2, Yinrui Ma2, Chen Wang1, Yanlian Yang1( ), Zhaohui He2( ), Ling Zhu1( )
CAS Key Laboratory of Standardization and Measurement for Nanotechnology, CAS Key Laboratory for Biomedical Effects of Nanomaterials and Nanosafety, CAS Center for Excellence in Nanoscience, National Center for Nanoscience and Technology, Beijing 100190, China
Department of Neurosurgery, The First Affiliated Hospital of Chongqing Medical University, Chongqing 400016, China
The First Affiliated Hospital University of Science and Technology of China, Anhui Provincial Hospital, Hefei 230000, China

§ Fuming Liang, Qing You, and Hongjiang Ye contributed equally to this work.

Abstract

Preoperative localization of the tumor sites and intraoperative real-time monitoring are essential for precise surgery but are meanwhile challenging due to the lack of high-resolution, easy-to-operate, and fast visualization techniques. On the other hand, tumor recurrence and metastasis after surgery greatly reduce the survival rate of patients. Intervening tumor recurrence during surgery is a future direction of tumor treatment. Nanomaterials with external condition responsiveness (light, ultrasound, and magnetic field) can accurately assist intraoperative detection and surgical resection due to their functions such as tumor cell targeting, fluorescence imaging, and real time monitoring, providing a more accurate, shorter duration, and visualization method of surgical resection. Moreover, nanomaterials are versatile and can easily be tailored for application in different tumors. Locally filled or systemically circulating nanomaterials with slow drug release and residual tumor cell-targeting ability have promising applications in inhibiting tumor recurrence. Here, we review surgical navigation and postoperative recurrence interventional nanomaterials and their landscape in guiding tumor treatment. We summarize the classification and characteristics of these nanomaterials and discuss their application in the surgical navigation and recurrence inhibition of different tumors. We also provide an outlook on the challenges and future development of nanomaterials for visualized tumor surgical navigation and postoperative recurrence inhibition.

Keywords: nanomaterials, surgical navigation, tumor recurrence inhibition, tumor resection

References(126)

[1]

Weller, M.; Van Den Bent, M.; Preusser, M.; Le Rhun, E.; Tonn, J. C.; Minniti, G.; Bendszus, M.; Balana, C.; Chinot, O.; Dirven, L. et al. EANO guidelines on the diagnosis and treatment of diffuse gliomas of adulthood. Nat. Rev. Clin. Oncol. 2021, 18, 170–186.
DOI Google Scholar
[2]

Vogel, A.; Meyer, T.; Sapisochin, G.; Salem, R.; Saborowski, A. Hepatocellular carcinoma. Lancet 2022, 400, 1345–1362.
DOI Google Scholar
[3]

Al-Hilli, Z.; Wilkerson, A. Breast surgery: Management of postoperative complications following operations for breast cancer. Surg. Clin. North Am. 2021, 101, 845–863.
DOI Google Scholar
[4]

Aziz, H.; Acher, A. W.; Krishna, S. G.; Cloyd, J. M.; Pawlik, T. M. Comparison of society guidelines for the management and surveillance of pancreatic cysts: A review. JAMA Surg. 2022, 157, 723–730.
DOI Google Scholar
[5]

Zaffino, P.; Moccia, S.; De Momi, E.; Spadea, M. F. A review on advances in intra-operative imaging for surgery and therapy: Imagining the operating room of the future. Ann. Biomed. Eng. 2020, 48, 2171–2191.
DOI Google Scholar
[6]

Moiyadi, A.; Shetty, P. Navigable intraoperative ultrasound and fluorescence-guided resections are complementary in resection control of malignant gliomas: One size does not fit all. J. Neurol. Surg. A Cent. Eur. Neurosurg. 2014, 75, 434–441.
DOI Google Scholar
[7]

Yoo, T. K.; Kang, Y. J.; Jeong, J.; Song, J. Y.; Kang, S. H.; Lee, H. Y.; Kim, E. T.; Yi, O.; Lee, H. B.; Choi, S. et al. A randomized controlled trial for doing vs. omitting intraoperative frozen section biopsy for resection margin status in selected patients undergoing breast-conserving surgery (OFF-MAP trial). J. Breast. Cancer 2021, 24, 569–577.
DOI Google Scholar
[8]

Cruz, C.; Afonso, M.; Oliveiros, B.; Pêgo, A. Recurrence and risk factors for relapse in patients with non-small cell lung cancer treated by surgery with curative intent. Oncology 2017, 92, 347–352.
DOI Google Scholar
[9]

Wu, Y. M.; Shi, X. C.; Li, J. P.; Wu, G. S. Prognosis of surgical treatment after ipsilateral breast tumor recurrence. J. Surg. Res. 2021, 258, 23–37.
DOI Google Scholar
[10]

Algar, W. R.; Massey, M.; Rees, K.; Higgins, R.; Krause, K. D.; Darwish, G. H.; Peveler, W. J.; Xiao, Z. J.; Tsai, H. Y.; Gupta, R. et al. Photoluminescent nanoparticles for chemical and biological analysis and imaging. Chem. Rev. 2021, 121, 9243–9358.
DOI Google Scholar
[11]

Mitchell, M. J.; Billingsley, M. M.; Haley, R. M.; Wechsler, M. E.; Peppas, N. A.; Langer, R. Engineering precision nanoparticles for drug delivery. Nat. Rev. Drug. Discov. 2021, 20, 101–124.
DOI Google Scholar
[12]

Bogart, L. K.; Pourroy, G.; Murphy, C. J.; Puntes, V.; Pellegrino, T.; Rosenblum, D.; Peer, D.; Lévy, R. Nanoparticles for imaging, sensing, and therapeutic intervention. ACS Nano 2014, 8, 3107–3122.
DOI Google Scholar
[13]

Duan, G. X.; Zhang, J. Y.; Wei, Z. X.; Wang, X. M.; Zeng, J. F.; Wu, S. W.; Hu, C. H.; Wen, L. Intraoperative diagnosis of early lymphatic metastasis using neodymium-based rare-earth NIR-II fluorescence nanoprobe. Nanoscale Adv. 2023, 5, 4240–4249.
DOI Google Scholar
[14]

Xu, Y. Q.; Cui, M. Y.; Zhang, W. C.; Liu, T. G.; Ren, X. Y.; Gu, Y. Q.; Ran, C. Z.; Yang, J.; Wang P. A sulfatase-activatable AIEgen nanoprobe for inhalation imaging-guided surgical excision of lung cancer. Chem. Eng. J. 2022, 428, 132514.
DOI Google Scholar
[15]

Colby, A. H.; Berry, S. M.; Moran, A. M.; Pasion, K. A.; Liu, R.; Colson, Y. L.; Ruiz-Opazo, N.; Grinstaff, M. W.; Herrera, V. L. M. Highly specific and sensitive fluorescent nanoprobes for image-guided resection of sub-millimeter peritoneal tumors. ACS Nano 2017, 11, 1466–1477.
DOI Google Scholar
[16]

Wang, Z. J.; Zhang, M.; Chi, S. Y.; Zhu, M. T.; Wang, C. X.; Liu, Z. H. Brain tumor cell membrane-coated lanthanide-doped nanoparticles for NIR-IIb luminescence imaging and surgical navigation of Glioma. Adv Healthc. Mater. 2022, 11, 2200521.
DOI Google Scholar
[17]

Qian, Q. H.; Song, J.; Chen, C.; Pu, Q.; Liu, X. C.; Wang, H. L. Recent advances in hydrogels for preventing tumor recurrence. Biomater. Sci. 2023, 11, 2678–2692.
DOI Google Scholar
[18]

Ditto, A.; Ferla, S.; Martinelli, F.; Bogani, G.; Maggiore, U. L. R.; Raspagliesi, F. Real-time fluorescent ICG and 99m-Tc nanocolloid tracer navigation in bilateral sentinel lymph node mapping of vulvar cancer. J. Minim. Invasive. Gynecol. 2023, 30, 780–781.
DOI Google Scholar
[19]

Nicoli, F.; Saleh, D. B.; Baljer, B.; Chan, C. D.; Beckingsale, T.; Ghosh, K. M.; Ragbir, M.; Rankin, K. S. Intraoperative near-infrared fluorescence (NIR) imaging with indocyanine green (ICG) can identify bone and soft tissue sarcomas which may provide guidance for oncological resection. Ann. Surg. 2021, 273, e63–e68.
DOI Google Scholar
[20]

Ushijima, H.; Kawamura, J.; Ueda, K.; Yane, Y.; Yoshioka, Y.; Daito, K.; Tokoro, T.; Hida, J. I.; Okuno, K. Visualization of lymphatic flow in laparoscopic colon cancer surgery using indocyanine green fluorescence imaging. Sci. Rep. 2020, 10, 14274.
DOI Google Scholar
[21]

Hu, Z. H.; Fang, C.; Li, B.; Zhang, Z. Y.; Cao, C. G.; Cai, M. S.; Su, S.; Sun, X. W.; Shi, X. J.; Li, C. et al. First-in-human liver-tumour surgery guided by multispectral fluorescence imaging in the visible and near-infrared-I/II windows. Nat. Biomed. Eng. 2020, 4, 259–271.
DOI Google Scholar
[22]

Xu, H. Y.; Han, Y. H.; Zhao, G.; Zhang, L.; Zhao, Z. R.; Wang, Z.; Zhao, L.; Hua, L.; Naveena, K.; Lu, J. et al. Hypoxia-responsive lipid-polymer nanoparticle-combined imaging-guided surgery and multitherapy strategies for glioma. ACS Appl. Mater. Interfaces 2020, 12, 52319–52328.
DOI Google Scholar
[23]

Turley, A. T.; Saha, P. K.; Danos, A.; Bismillah, A. N.; Monkman, A. P.; Yufit, D. S.; Curchod, B. F. E.; Etherington, M. K.; McGonigal, P. R. Extended conjugation attenuates the quenching of aggregation-induced emitters by photocyclization pathways. Angew. Chem., Int. Ed. 2022, 61, e202202193.
DOI Google Scholar
[24]

Hong, Y. N.; Lam, J. W. Y.; Tang, B. Z. Aggregation-induced emission. Chem. Soc. Rev. 2011, 40, 5361–5388.
DOI Google Scholar
[25]

Xu, R. T.; Jiao, D.; Long, Q.; Li, X. L.; Shan, K.; Kong, X. L.; Ou, H. L.; Ding, D.; Tang, Q. Y. Highly bright aggregation-induced emission nanodots for precise photoacoustic/NIR-II fluorescence imaging-guided resection of neuroendocrine neoplasms and sentinel lymph nodes. Biomaterials 2022, 289, 121780.
DOI Google Scholar
[26]

Chen, L. L.; Zhao, L.; Wang, Z. G.; Liu, S. L.; Pang, D. W. Near-infrared-II quantum dots for in vivo imaging and cancer therapy. Small 2022, 18, 2104567.
DOI Google Scholar
[27]

Xu, Z.; Huang, H. B.; Xiong, X.; Wei, X. Q.; Guo, X.; Zhao, J. Y.; Zhou, S. B. A near-infrared light-responsive extracellular vesicle as a “Trojan horse” for tumor deep penetration and imaging-guided therapy. Biomaterials 2021, 269, 120647.
DOI Google Scholar
[28]

Liu, X. Y.; Braun, G. B.; Zhong, H. Z.; Hall, D. J.; Han, W. L.; Qin, M. D.; Zhao, C. Z.; Wang, M.; She, Z. G.; Cao, C. B. et al. Tumor-targeted multimodal optical imaging with versatile cadmium-free quantum dots. Adv. Funct. Mater. 2016, 26, 267–276.
DOI Google Scholar
[29]

Juengpanich, S.; Li, S. J.; Yang, T. R.; Xie, T. N.; Chen, J. D.; Shan, Y. K.; Lee, J.; Lu, Z. Y.; Chen, T. N.; Zhang, B. et al. Pre-activated nanoparticles with persistent luminescence for deep tumor photodynamic therapy in gallbladder cancer. Nat. Commun. 2023, 14, 5699.
DOI Google Scholar
[30]

Li, S. H.; Wei, X. D.; Li, S. S.; Zhu, C. M.; Wu, C. H. Up-conversion luminescent nanoparticles for molecular imaging, cancer diagnosis and treatment. Int. J. Nanomed. 2020, 15, 9431–9445.
DOI Google Scholar
[31]

Chen, G. Y.; Ohulchanskyy, T. Y.; Kumar, R.; Ågren, H.; Prasad, P. N. Ultrasmall monodisperse NaYF4: Yb3+/Tm3+ nanocrystals with enhanced near-infrared to near-infrared upconversion photoluminescence. ACS Nano 2010, 4, 3163–3168.
DOI Google Scholar
[32]

Zhang, Q. Z.; O'Brien, S.; Grimm, J. Biomedical applications of lanthanide nanomaterials, for imaging, sensing and therapy. Nanotheranostics 2022, 6, 184–194.
DOI Google Scholar
[33]

Xiao, Y. D.; Paudel, R.; Liu, J.; Ma, C.; Zhang, Z. S.; Zhou, S. K. MRI contrast agents: Classification and application (Review). Int. J. Mol. Med. 2016, 38, 1319–1326.
DOI Google Scholar
[34]

Kaittanis, C.; Shaffer, T. M.; Bolaender, A.; Appelbaum, Z.; Appelbaum, J.; Chiosis, G.; Grimm, J. Multifunctional MRI/PET nanobeacons derived from the in situ self-assembly of translational polymers and clinical cargo through coalescent intermolecular forces. Nano Lett. 2015, 15, 8032–8043.
DOI Google Scholar
[35]

Shiozawa, M.; Kobayashi, S.; Sato, Y.; Maeshima, H.; Hozumi, Y.; Lefor, A. T.; Kurihara, K.; Sata, N.; Yasuda, Y. Magnetic resonance lymphography of sentinel lymph nodes in patients with breast cancer using superparamagnetic iron oxide: A feasibility study. Breast Cancer 2014, 21, 394–401.
DOI Google Scholar
[36]

Fu, C. P.; Duan, X. H.; Cao, M. H.; Jiang, S. Q.; Ban, X. H.; Guo, N.; Zhang, F.; Mao, J. J.; Huyan, T.; Shen, J. et al. Targeted magnetic resonance imaging and modulation of hypoxia with multifunctional hyaluronic acid-MnO2 nanoparticles in glioma. Adv. Healthc. Mater. 2019, 8, e1900047.
DOI Google Scholar
[37]

Liu, Y. J.; Bhattarai, P.; Dai, Z. F.; Chen, X. Y. Photothermal therapy and photoacoustic imaging via nanotheranostics in fighting cancer. Chem. Soc. Rev. 2019, 48, 2053–2108.
DOI Google Scholar
[38]

Thawani, J. P.; Amirshaghaghi, A.; Yan, L. S.; Stein, J. M.; Liu, J.; Tsourkas, A. Photoacoustic-guided surgery with indocyanine green-coated superparamagnetic iron oxide nanoparticle clusters. Small 2017, 13, 1701300.
DOI Google Scholar
[39]
Xia, J. Z.; Feng, G.; Xia, X. R.; Hao, L.; Wang, Z. G. NH4HCO3 gas-generating liposomal nanoparticle for photoacoustic imaging in breast cancer. Int. J. Nanomed. 2017 , 12, 1803–1813.
[40]

Renaudin, N.; Pezet, S.; Ialy-Radio, N.; Demene, C.; Tanter, M. Backscattering amplitude in ultrasound localization microscopy. Sci. Rep. 2023, 13, 11477.
DOI Google Scholar
[41]

Fang, Y.; Lin, W.; Zhou, Y. W.; Wang, W. W.; Liu, X. P. Evaluation of tumor resection effect of color doppler ultrasound positioning guided breast-conserving surgery using nano-contrast agent. Cell Mol. Biol. (Noisy-le-grand) 2022, 68, 365–373.
DOI Google Scholar
[42]

Wang, J. Q.; Xie, L. T.; Shi, Y.; Ao, L. J.; Cai, F. Y.; Yan, F. Early detection and reversal of cell apoptosis induced by focused ultrasound-mediated blood-brain barrier opening. ACS Nano 2021, 15, 14509–14521.
DOI Google Scholar
[43]

Yin, H.; Jin, Z. Y.; Duan, W. J.; Han, B.; Han, L. M.; Li, C. Emergence of responsive surface-enhanced Raman scattering probes for imaging tumor-associated metabolites. Adv. Healthc. Mater. 2022, 11, 2200030.
DOI Google Scholar
[44]

Han, L. M.; Duan, W. J.; Li, X. W.; Wang, C.; Jin, Z. Y.; Zhai, Y. T.; Cao, C.; Chen, L.; Xu, W. J.; Liu, Y. et al. Surface-enhanced resonance Raman scattering-guided brain tumor surgery showing prognostic benefit in rat models. ACS Appl. Mater. Interfaces 2019, 11, 15241–15250.
DOI Google Scholar
[45]

Karabeber, H.; Huang, R. M.; Iacono, P.; Samii, J. M.; Pitter, K.; Holland, E. C.; Kircher, M. F. Guiding brain tumor resection using surface-enhanced Raman scattering nanoparticles and a hand-held Raman scanner. ACS Nano 2014, 8, 9755–9766.
DOI Google Scholar
[46]

Malone, J. X-rays for medical imaging: Radiation protection, governance and ethics over 125years. Phys. Med. 2020, 79, 47–64.
DOI Google Scholar
[47]

Seeram, E. Computed tomography: A technical review. Radiol. Technol. 2018, 89, 279CT–302CT.
Google Scholar
[48]

Wang, X. Y.; Wang, J. J.; Pan, J. B.; Zhao, F. S.; Kan, D.; Cheng, R.; Zhang, X. N.; Sun, S. K. Rhenium sulfide nanoparticles as a biosafe spectral CT contrast agent for gastrointestinal tract imaging and tumor theranostics in vivo. ACS Appl. Mater. Interfaces 2019, 11, 33650–33658.
DOI Google Scholar
[49]

Bowles, H.; Sánchez, N.; Tapias, A.; Paredes, P.; Campos, F.; Bluemel, C.; Olmos, R. A. V.; Vidal-Sicart, S. Radioguided surgery and the GOSTT concept: From pre-operative image and intraoperative navigation to image-assisted excision. Rev. Esp. Med. Nucl. Imagen. Mol. 2017, 36, 175–184.
DOI Google Scholar
[50]

Li, T. Z.; Li, J. F.; Chen, Z.; Zhang, S. H.; Li, S. L.; Wageh, S.; Al-Hartomy, O. A.; Al-Sehemi, A. G.; Xie, Z. J.; Kankala, R. K. et al. Glioma diagnosis and therapy: Current challenges and nanomaterial-based solutions. J. Control. Release 2022, 352, 338–370.
DOI Google Scholar
[51]

Natale, G.; Stouthandel, M. E. J.; Van Hoof, T.; Bocci, G. The lymphatic system in breast cancer: Anatomical and molecular approaches. Medicina (Kaunas) 2021, 57, 1272.
DOI Google Scholar
[52]

Yao, C. Y.; Wu, S. L.; Kong, J.; Sun, Y. W.; Bai, Y. N.; Zhu, R. H.; Li, Z. X.; Sun, W. B.; Zheng, L. M. Angiogenesis in hepatocellular carcinoma: Mechanisms and anti-angiogenic therapies. Cancer Biol. Med. 2023, 20, 25–43.
DOI Google Scholar
[53]

Kumbhar, P.; Manjappa, A.; Shah, R.; Jha, N. K.; Singh, S. K.; Dua, K.; Disouza, J.; Patravale, V. Inhalation delivery of repurposed drugs for lung cancer: Approaches, benefits and challenges. J. Control. Release 2022, 341, 1–15.
DOI Google Scholar
[54]

Goéré, D.; Glehen, O.; Quenet, F.; Guilloit, J. M.; Bereder, J. M.; Lorimier, G.; Thibaudeau, E.; Ghouti, L.; Pinto, A.; Tuech, J. J. et al. Second-look surgery plus hyperthermic intraperitoneal chemotherapy versus surveillance in patients at high risk of developing colorectal peritoneal metastases (PROPHYLOCHIP-PRODIGE 15): A randomised, phase 3 study. Lancet Oncol. 2020, 21, 1147–1154.
DOI Google Scholar
[55]

Carpino, G.; Cardinale, V.; Di Giamberardino, A.; Overi, D.; Donsante, S.; Colasanti, T.; Amato, G.; Mennini, G.; Franchitto, M.; Conti, F. et al. Thrombospondin 1 and 2 along with PEDF inhibit angiogenesis and promote lymphangiogenesis in intrahepatic cholangiocarcinoma. J. Hepatol. 2021, 75, 1377–1386.
DOI Google Scholar
[56]

Huang, C. B.; Li, H.; Xu, Y.; Xu, C.; Sun, H. Z.; Li, Z. X.; Ge, Y.; Wang, H. W.; Zhao, T. S.; Gao, S. et al. BICC1 drives pancreatic cancer progression by inducing VEGF-independent angiogenesis. Signal. Transduct. Target. Ther. 2023, 8, 271.
DOI Google Scholar
[57]

Ljubimova, J. Y.; Sun, T.; Mashouf, L.; Ljubimov, A. V.; Israel, L. L.; Ljubimov, V. A.; Falahatian, V.; Holler, E. Covalent nano delivery systems for selective imaging and treatment of brain tumors. Adv. Drug Deliv. Rev. 2017, 113, 177–200.
DOI Google Scholar
[58]

Song, X. W.; Qian, H. S.; Yu, Y. Q. Nanoparticles mediated the diagnosis and therapy of glioblastoma: Bypass or cross the blood-brain barrier. Small 2023, 19, 2302613.
DOI Google Scholar
[59]

Ni, D. L.; Zhang, J. W.; Bu, W. B.; Xing, H. Y.; Han, F.; Xiao, Q. F.; Yao, Z. W.; Chen, F.; He, Q. J.; Liu, J. N. et al. Dual-targeting upconversion nanoprobes across the blood-brain barrier for magnetic resonance/fluorescence imaging of intracranial glioblastoma. ACS Nano 2014, 8, 1231–1242.
DOI Google Scholar
[60]

Lee, C.; Hwang, H. S.; Lee, S.; Kim, B.; Kim, J. O.; Oh, K. T.; Lee, E. S.; Choi, H. G.; Youn, Y. S. Rabies virus-inspired silica-coated gold nanorods as a photothermal therapeutic platform for treating brain tumors. Adv. Mater. 2017, 29, 1605563.
DOI Google Scholar
[61]

Waks, A. G.; Winer, E. P. Breast cancer treatment: A review. JAMA 2019, 321, 288–300.
DOI Google Scholar
[62]

Yang, R. Q.; Chen, M.; Zhang, Q.; Gao, Y. Y.; Lou, K. L.; Lin, T. T.; Huang, W. H.; Zeng, Y. Z.; Zhang, Y. Q.; Dang, Y. Y. et al. Development and preclinical evaluation of a near-infrared fluorescence probe based on tailored Hepatitis B core particles for imaging-guided surgery in breast cancer. Int. J. Nanomed. 2022, 17, 1343–1360.
DOI Google Scholar
[63]

Giuliano, A. E.; Ballman, K. V.; McCall, L.; Beitsch, P. D.; Brennan, M. B.; Kelemen, P. R.; Ollila, D. W.; Hansen, N. M.; Whitworth, P. W.; Blumencranz, P. W. et al. Effect of axillary dissection vs no axillary dissection on 10-year overall survival among women with invasive breast cancer and sentinel node metastasis: The ACOSOG Z0011 (alliance) randomized clinical trial. JAMA 2017, 318, 918–926.
DOI Google Scholar
[64]

Dai, R. Y.; Peng, X. R.; Lin, B.; Xu, D. Y.; Lv, R. C. NIR II luminescence imaging for sentinel lymph node and enhanced chemo-/photothermal therapy for breast cancer. Bioconjugate Chem. 2021, 32, 2117–2127.
DOI Google Scholar
[65]

Forner, A.; Reig, M.; Bruix, J. Hepatocellular carcinoma. Lancet 2018, 391, 1301–1314.
DOI Google Scholar
[66]

Zhang, X. J.; Zhou, C. S.; Wu, F. H.; Gao, C.; Liu, Q. Q.; Lv, P.; Li, M.; Huang, L. Y.; Wu, T.; Li, W. G. Bio-engineered nano-vesicles for IR820 delivery: A therapy platform for cancer by surgery and photothermal therapy. Nanoscale 2022, 14, 2780–2792.
DOI Google Scholar
[67]
Tsai, C. N.; Yu, S. C.; Lee, C. W.; Pang, J. H. S.; Wu, C. H.; Lin, S. E.; Chung, Y. H.; Tsai, C. L.; Hsieh, S. Y.; Yu, M. C. SOX4 activates CXCL12 in hepatocellular carcinoma cells to modulate endothelial cell migration and angiogenesis in vivo. Oncogene 2020 , 39, 4695–4710.
DOI
[68]

Zou, R. H.; Lin, Q. G.; Huang, W.; Li, X. L.; Cao, Y.; Zhang, J.; Zhou, J. H.; Li, A. H.; Beretta, L.; Qian, C. N. Quantitative contrast-enhanced ultrasonic imaging reflects microvascularization in hepatocellular carcinoma and prognosis after resection. Ultrasound Med. Biol. 2015, 41, 2621–2630.
DOI Google Scholar
[69]

Zhang, Z. Y.; Fang, C.; Zhang, Y.; Su, S.; Li, B.; Liu, G.; Hu, Z. H.; Tian, J. NIR-II nano fluorescence image guided hepatic carcinoma resection on cirrhotic patient. Photodiagnosis Photodyn. Ther. 2022, 40, 103098.
DOI Google Scholar
[70]

Nasim, F.; Sabath, B. F.; Eapen, G. A. Lung Cancer. Med. Clin. North Am. 2019, 103, 463–473.
DOI Google Scholar
[71]

Jin, Q. T.; Zhu, W. J.; Zhu, J. F.; Zhu, J. J.; Shen, J. J.; Liu, Z.; Yang, Y.; Chen, Q. Nanoparticle-mediated delivery of inhaled immunotherapeutics for treating lung metastasis. Adv. Mater. 2021, 33, 2007557.
DOI Google Scholar
[72]
Jin, M.; Liu, B. H.; Zhang, Z.; Mu, Y. L.; Ma, L.; Yao, H.; Wang, D. A. Catechin-functionalized cationic lipopolymer based multicomponent nanomicelles for lung-targeting delivery. Adv. Mater., in press, https://doi.org/10.1002/adma.202302985.
DOI
[73]

Vaes, N.; Idris, M.; Boesmans, W.; Alves, M. M.; Melotte, V. Nerves in gastrointestinal cancer: From mechanism to modulations. Nat. Rev. Gastroenterol. Hepatol. 2022, 19, 768–784.
DOI Google Scholar
[74]

Li, T. W.; Cao, K. L.; Yang, X. H.; Liu, Y. Y.; Wang, X. Y.; Wu, F.; Chen, G. C.; Wang, Q. B. An oral ratiometric NIR-II fluorescent probe for reliable monitoring of gastrointestinal diseases in vivo. Biomaterials 2023, 293, 121956.
DOI Google Scholar
[75]

Chen, Z. W.; Kang, F. P.; Xie, C. K.; Liao, C. Y.; Li, G.; Wu, Y. D.; Lin, H. Y.; Zhu, S. C.; Hu, J. F.; Lin, C. F. et al. A novel trojan horse nanotherapy strategy targeting the cPKM-STMN1/TGFB1 axis for effective treatment of intrahepatic cholangiocarcinoma. Adv. Sci. 2023, 10, 2303814.
DOI Google Scholar
[76]

Zhou, Q.; Shao, S. Q.; Wang, J. Q.; Xu, C. H.; Xiang, J. J.; Piao, Y.; Zhou, Z. X.; Yu, Q. S.; Tang, J. B.; Liu, X. R. et al. Enzyme-activatable polymer-drug conjugate augments tumour penetration and treatment efficacy. Nat. Nanotechnol. 2019, 14, 799–809.
DOI Google Scholar
[77]

Dane, E. L.; Belessiotis-Richards, A.; Backlund, C.; Wang, J. N.; Hidaka, K.; Milling, L. E.; Bhagchandani, S.; Melo, M. B.; Wu, S. W.; Li, N. et al. STING agonist delivery by tumour-penetrating PEG-lipid nanodiscs primes robust anticancer immunity. Nat. Mater. 2022, 21, 710–720.
DOI Google Scholar
[78]

Yong, T. Y.; Zhang, X. Q.; Bie, N. N.; Zhang, H. B.; Zhang, X. T.; Li, F. Y.; Hakeem, A.; Hu, J.; Gan, L.; Santos, H. A. et al. Tumor exosome-based nanoparticles are efficient drug carriers for chemotherapy. Nat. Commun. 2019, 10, 3838.
DOI Google Scholar
[79]

Pitsilos, C.; Givissis, P.; Papadopoulos, P.; Chalidis, B. Treatment of recurrent giant cell tumor of bones: A systematic review. Cancers (Basel) 2023, 15, 3287.
DOI Google Scholar
[80]

Swetha, K. L.; Roy, A. Tumor heterogeneity and nanoparticle-mediated tumor targeting: The importance of delivery system personalization. Drug Deliv. Transl. Res. 2018, 8, 1508–1526.
DOI Google Scholar
[81]

Yang, S. T.; Liu, Y.; Wang, Y. W.; Cao, A. N. Biosafety and bioapplication of nanomaterials by designing protein-nanoparticle interactions. Small 2013, 9, 1635–1653.
DOI Google Scholar
[82]

Cao, J. Y.; Gao, M. K.; Wang, J.; Liu, Y.; Zhang, X.; Ping, Y.; Liu, J.; Chen, G.; Xu, D. H.; Huang, X. D. et al. Construction of nano slow-release systems for antibacterial active substances and its applications: A comprehensive review. Front. Nutr. 2023, 10, 1109204.
DOI Google Scholar
[83]

Chen, C.; Jing, W. Q.; Chen, Y.; Wang, G. Y.; Abdalla, M.; Gao, L.; Han, M. S.; Shi, C. D.; Li, A. N.; Sun, P. et al. Intracavity generation of glioma stem cell-specific CAR macrophages primes locoregional immunity for postoperative glioblastoma therapy. Sci. Transl. Med. 2022, 14, eabn1128.
DOI Google Scholar
[84]

Bunse, L.; Pusch, S.; Bunse, T.; Sahm, F.; Sanghvi, K.; Friedrich, M.; Alansary, D.; Sonner, J. K.; Green, E.; Deumelandt, K. et al. Suppression of antitumor T cell immunity by the oncometabolite ( R)-2-hydroxyglutarate. Nat. Med. 2018, 24, 1192–1203.
DOI Google Scholar
[85]

Zhang, J.; Chen, C.; Li, A. N.; Jing, W. Q.; Sun, P.; Huang, X. Y.; Liu, Y. C.; Zhang, S. C.; Du, W.; Zhang, R. et al. Immunostimulant hydrogel for the inhibition of malignant glioma relapse post-resection. Nat. Nanotechnol. 2021, 16, 538–548.
DOI Google Scholar
[86]
Li, C. Y.; Wan, Y. L.; Zhang, Y. F.; Fu, L. H.; Blum, N. T.; Cui, R.; Wu, B. D.; Zheng, R.; Lin, J.; Li, Z. M. et al. In situ sprayed starvation/chemodynamic therapeutic gel for post-surgical treatment of IDH1 (R132H) glioma. Adv. Mater. 2022 , 34, 2103980.
DOI
[87]

Chandrasekharan, P.; Tay, Z. W.; Hensley, D.; Zhou, X. Y.; Fung, B. K.; Colson, C.; Lu, Y.; Fellows, B. D.; Huynh, Q.; Saayujya, C. et al. Using magnetic particle imaging systems to localize and guide magnetic hyperthermia treatment: Tracers, hardware, and future medical applications. Theranostics 2020, 10, 2965–2981.
DOI Google Scholar
[88]

Kang, T.; Cha, G. D.; Park, O. K.; Cho, H. R.; Kim, M.; Lee, J.; Kim, D.; Lee, B.; Chu, J. Y.; Koo, S. et al. Penetrative and sustained drug delivery using injectable hydrogel nanocomposites for postsurgical brain tumor treatment. ACS Nano 2023, 17, 5435–5447.
DOI Google Scholar
[89]

Kimiz-Gebologlu, I.; Oncel, S. S. Exosomes: Large-scale production, isolation, drug loading efficiency, and biodistribution and uptake. J. Control. Release 2022, 347, 533–543.
DOI Google Scholar
[90]

Zhang, Y. Y.; Tian, S. D.; Huang, L. P.; Li, Y. N.; Lu, Y.; Li, H. Y.; Chen, G. P.; Meng, F. L.; Liu, G. L.; Yang, X. L. et al. Reactive oxygen species-responsive and Raman-traceable hydrogel combining photodynamic and immune therapy for postsurgical cancer treatment. Nat. Commun. 2022, 13, 4553.
DOI Google Scholar
[91]

Tang, J. Y.; Xiang, Z. Y.; Bernards, M. T.; Chen, S. F. Peritoneal adhesions: Occurrence, prevention and experimental models. Acta Biomater. 2020, 116, 84–104.
DOI Google Scholar
[92]

Fang, Y.; Yang, J. P.; Zhang, M. L.; Song, J. H.; Lin, R. L. A longitudinal study of stress in new nurses in their first year of employment. Int. J. Clin. Pract. 2022, 2022, 6932850.
DOI Google Scholar
[93]

Bu, L. L.; Yan, J. J.; Wang, Z. J.; Ruan, H. T.; Chen, Q.; Gunadhi, V.; Bell, R. B.; Gu, Z. Advances in drug delivery for post-surgical cancer treatment. Biomaterials 2019, 219, 119182.
DOI Google Scholar
[94]

Mathios, D.; Kim, J. E.; Mangraviti, A.; Phallen, J.; Park, C. K.; Jackson, C. M.; Garzon-Muvdi, T.; Kim, E.; Theodros, D.; Polanczyk, M. et al. Anti-PD-1 antitumor immunity is enhanced by local and abrogated by systemic chemotherapy in GBM. Sci. Transl. Med. 2016, 8, 370ra180.
DOI Google Scholar
[95]

De Bonis, P.; Anile, C.; Pompucci, A.; Fiorentino, A.; Balducci, M.; Chiesa, S.; Maira, G.; Mangiola, A. Safety and efficacy of Gliadel wafers for newly diagnosed and recurrent glioblastoma. Acta Neurochir. (Wien) 2012, 154, 1371–1378.
DOI Google Scholar
[96]

Ong, B. Y. S.; Ranganath, S. H.; Lee, L. Y.; Lu, F.; Lee, H. S.; Sahinidis, N. V.; Wang, C. H. Paclitaxel delivery from PLGA foams for controlled release in post-surgical chemotherapy against glioblastoma multiforme. Biomaterials 2009, 30, 3189–3196.
DOI Google Scholar
[97]

Klode, J.; Klötgen, K.; Körber, A.; Schadendorf, D.; Dissemond, J. Polidocanol foam sclerotherapy is a new and effective treatment for post-operative lymphorrhea and lymphocele. J. Eur. Acad. Dermatol. Venereol. 2010, 24, 904–909.
DOI Google Scholar
[98]

Liu, R.; Wolinsky, J. B.; Walpole, J.; Southard, E.; Chirieac, L. R.; Grinstaff, M. W.; Colson, Y. L. Prevention of local tumor recurrence following surgery using low-dose chemotherapeutic polymer films. Ann. Surg. Oncol. 2010, 17, 1203–1213.
DOI Google Scholar
[99]

Jiang, W.; Wei, L. L.; Chen, B.; Luo, X. Y.; Xu, P. P.; Cai, J. F.; Hu, Y. Platinum prodrug nanoparticles inhibiting tumor recurrence and metastasis by concurrent chemoradiotherapy. J. Nanobiotechnol. 2022, 20, 129.
DOI Google Scholar
[100]

Zhang, Z. Y.; Liu, S.; Qi, Y. X.; Zhou, D. F.; Xie, Z. G.; Jing, X. B.; Chen, X. S.; Huang, Y. B. Time-programmed DCA and oxaliplatin release by multilayered nanofiber mats in prevention of local cancer recurrence following surgery. J. Control. Release 2016, 235, 125–133.
DOI Google Scholar
[101]

Chen, R. M.; Zhao, C.; Chen, Z. P.; Shi, X. Y.; Zhu, H. X.; Bu, Q.; Wang, L.; Wang, C. F.; He, H. A bionic cellulose nanofiber-based nanocage wound dressing for NIR-triggered multiple synergistic therapy of tumors and infected wounds. Biomaterials 2022, 281, 121330.
DOI Google Scholar
[102]

Liu, Z.; Luo, X.; Mo, Y. X.; Zhao, P. K.; Wang, H. X.; Fang, Y. Q.; Xu, Y. T. Enzyme-enhanced codelivery of doxorubicin and Bcl-2 inhibitor by electrospun nanofibers for synergistic inhibition of prostate cancer recurrence. Pharmaceuticals (Basel) 2022, 15, 1244.
DOI Google Scholar
[103]
You, Q.; Liang, F. M.; Wu, G. G.; Cao, F. F.; Liu, J. Y.; He, Z. H.; Wang, C.; Zhu, L.; Chen, X. Y.; Yang, Y. L. The landscape of biomimetic nanovesicles in brain diseases. Adv. Mater., in press, https://doi.org/10.1002/adma.202306583.
DOI
[104]

Peng, Z. H.; Zhang, X. C.; Yuan, L.; Li, T.; Chen, Y. J.; Tian, H.; Ma, D. D.; Deng, J.; Qi, X. W.; Yin, X T. Integrated endotoxin-adsorption and antibacterial properties of platelet-membrane-coated copper silicate hollow microspheres for wound healing. J. Nanobiotechnol. 2021, 19, 383.
DOI Google Scholar
[105]

Han, H. J.; Bártolo, R.; Li, J. C.; Shahbazi, M. A.; Santos, H. A. Biomimetic platelet membrane-coated nanoparticles for targeted therapy. Eur. J. Pharm. Biopharm. 2022, 172, 1–15.
DOI Google Scholar
[106]

Liu, Y. F.; Qi, Y.; Chen, C.; Jin, Y. C.; Du, S.; Qiao, J. N.; Yao, J. Platelet-mimetic nano-sensor for combating postoperative recurrence and wound infection of triple-negative breast cancer. J. Control. Release 2023, 362, 396–408.
DOI Google Scholar
[107]

Li, B. Z.; Zhang, X. P.; Wu, Z. L.; Chu, T. J.; Yang, Z. L.; Xu, S.; Wu, S. Y.; Qie, Y. K.; Lu, Z. F.; Qi, F. L. et al. Reducing postoperative recurrence of early-stage hepatocellular carcinoma by a wound-targeted nanodrug. Adv. Sci. (Weinh.) 2022, 9, 2200477.
DOI Google Scholar
[108]

Wang, J.; Tang, W.; Yang, M.; Yin, Y.; Li, H.; Hu, F. F.; Tang, L.; Ma, X. Y.; Zhang, Y.; Wang, Y. Z. Inflammatory tumor microenvironment responsive neutrophil exosomes-based drug delivery system for targeted glioma therapy. Biomaterials 2021, 273, 120784.
DOI Google Scholar
[109]

Xue, J. W.; Zhao, Z. K.; Zhang, L.; Xue, L. J.; Shen, S. Y.; Wen, Y. J.; Wei, Z. Y.; Wang, L.; Kong, L. Y.; Sun, H. B. et al. Neutrophil-mediated anticancer drug delivery for suppression of postoperative malignant glioma recurrence. Nat. Nanotechnol. 2017, 12, 692–700.
DOI Google Scholar
[110]

Zhou, C. Y.; Wang, Z. Z.; Jiang, B. H.; Di, J. B.; Su, X. Q. Monitoring Pre- and post-operative immune alterations in patients with locoregional colorectal cancer who underwent laparoscopy by single-cell mass cytometry. Front. Immunol. 2022, 13, 807539.
DOI Google Scholar
[111]

Zhong, X. W.; Li, C. Y.; Zhao, G. Z.; Li, M. M.; Chen, S. N.; Cao, Y.; Wang, Q.; Sun, J. C.; Zhu, S. Y.; Chang, S. F. Photoacoustic mediated multifunctional tumor antigen trapping nanoparticles inhibit the recurrence and metastasis of ovarian cancer by enhancing tumor immunogenicity. J. Nanobiotechnol. 2022, 20, 468.
DOI Google Scholar
[112]

Domingos-Pereira, S.; Roh, V.; Hiou-Feige, A.; Galliverti, G.; Simon, C.; Tolstonog, G. V.; Nardelli-Haefliger, D. Vaccination with a nanoparticle E7 vaccine can prevent tumor recurrence following surgery in a human papillomavirus head and neck cancer model. Oncoimmunology 2021, 10, 1912473.
DOI Google Scholar
[113]

Dai, J.; Cheng, Y.; Wu, J.; Wang, Q.; Wang, W. W.; Yang, J. L.; Zhao, Z. J.; Lou, X. D.; Xia, F.; Wang, S. X. et al. Modular peptide probe for pre/intra/postoperative therapeutic to reduce recurrence in ovarian cancer. ACS Nano 2020, 14, 14698–14714.
DOI Google Scholar
[114]

Zhou, T. J.; Liang, X. L.; Wang, P. F.; Hu, Y. Y.; Qi, Y. F.; Jin, Y. S.; Du, Y.; Fang, C. H.; Tian, J. A hepatocellular carcinoma targeting nanostrategy with hypoxia-ameliorating and photothermal abilities that, combined with immunotherapy, inhibits metastasis and recurrence. ACS Nano 2020, 14, 12679–12696.
DOI Google Scholar
[115]

Thao, L. Q.; Lee, C.; Kim, B.; Lee, S.; Kim, T. H.; Kim, J. O.; Lee, E. S.; Oh, K. T.; Choi, H. G.; Yoo, S. D. et al. Doxorubicin and paclitaxel co-bound lactosylated albumin nanoparticles having targetability to hepatocellular carcinoma. Colloids Surf. B Biointerfaces 2017, 152, 183–191.
DOI Google Scholar
[116]

Zhang, X. P.; Chen, X. J.; Li, B. Z.; Xu, S.; Wu, Z. L.; Hu, M. G.; Zhao, Z. M.; Zhao, G. D.; Wang, C. R.; Hong, W. et al. Active targeted Janus nanoparticles enable anti-angiogenic drug combining chemotherapy agent to prevent postoperative hepatocellular carcinoma recurrence. Biomaterials 2022, 281, 121362.
DOI Google Scholar
[117]

Ling, M. J.; Sun, R.; Li, G.; Syeda, M. Z.; Ma, W.; Mai, Z. Y.; Shao, L. Q.; Tang, L. G.; Yu, Z. Q. NIR-II emissive dye based polymer nanoparticle targeting EGFR for oral cancer theranostics. Nano Res. 2022, 15, 6288–6296.
DOI Google Scholar
[118]

Nichols, J. W.; Bae, Y. H. EPR: Evidence and fallacy. J. Control. Release 2014, 190, 451–464.
DOI Google Scholar
[119]

Song, C.; Ouyang, Z. J.; Guo, H. H.; Qu, J.; Gao, Y.; Xia, J. D.; Shen, M. W.; Shi, X. Y. Core–shell tecto dendrimers enable enhanced tumor MR imaging through an amplified EPR effect. Biomacromolecules 2021, 22, 2181–2188.
DOI Google Scholar
[120]

An, R. B.; Liu, L. J.; Wei, S. X.; Huang, Z.; Qiu, L.; Lin, J. G.; Liu, H.; Ye, D. J. Controlling disassembly of paramagnetic prodrug and photosensitizer nanoassemblies for on-demand orthotopic glioma theranostics. ACS Nano 2022, 16, 20607–20621.
DOI Google Scholar
[121]
You, Q.; Wang, F.; Du, R.; Pi, J. N.; Wang, H. Y.; Huo, Y.; Liu, J. Y.; Wang, C.; Yu, J.; Yang, Y. L. et al. m6A reader YTHDF1-targeting engineered small extracellular vesicles for gastric cancer therapy via epigenetic and immune regulation. Adv. Mater. 2023 , 35, 2204910.
DOI
[122]

Hu, H.; Huang, P.; Weiss, O. J.; Yan, X. F.; Yue, X. Y.; Zhang, M. G.; Tang, Y. X.; Nie, L. M.; Ma, Y.; Niu, G. et al. PET and NIR optical imaging using self-illuminating 64Cu-doped chelator-free gold nanoclusters. Biomaterials 2014, 35, 9868–9876.
DOI Google Scholar
[123]

Bhatia, S. N.; Chen, X. Y.; Dobrovolskaia, M. A.; Lammers, T. Cancer nanomedicine. Nat. Rev. Cancer 2022, 22, 550–556.
DOI Google Scholar
[124]

Moon, B.; Chang, S. Exosome as a delivery vehicle for cancer therapy. Cells 2022, 11, 316.
DOI Google Scholar
[125]

Wang, H. R.; Li, Q. Y.; Alam, P.; Bai, H. T.; Bhalla, V.; Bryce, M. R.; Cao, M. Y.; Chen, C.; Chen, S. J.; Chen, X. R. et al. Aggregation-induced emission (AIE), life and health. ACS Nano 2023, 17, 14347–14405.
DOI Google Scholar
[126]

Yu, M.; Duan, X. H.; Cai, Y. J.; Zhang, F.; Jiang, S. Q.; Han, S. S.; Shen, J.; Shuai, X. T. Multifunctional nanoregulator reshapes immune microenvironment and enhances immune memory for tumor immunotherapy. Adv. Sci. 2019, 6, 1900037.
DOI Google Scholar
Publication history
Copyright
Acknowledgements

Publication history

Received: 07 October 2023
Revised: 23 November 2023
Accepted: 23 November 2023
Published: 14 December 2023
Issue date: December 2023

Copyright

© Tsinghua University Press 2023

Acknowledgements

Acknowledgements

The authors are grateful to the National Natural Science Foundation of China (Nos. 31971295, 12374406, and 27121002), Strategic Priority Research Program of Chinese Academy of Science (No. XDB36000000), and Natural Science Foundation Project of Chongqing Science and Technology Commission (No. CSTB2023NSCQ-MSX0112).

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