Abstract
In oncology, sensitive and reliable detection tumor tissue is crucial to prevent recurrences and to improve surgical outcome. Currently, extensive research is focused on the use of radionuclides as well as fluorophores to provide real-time guidance during surgery to aid the surgeon in the identification of malignant tissue. Particularly, dual-modality approaches combining radionuclide and near-infrared fluorescence (NIRF) imaging have shown promising results in preclinical studies. Radionuclide imaging allows sensitive intra-operative localization of tumor lesions using a gamma probe, whereas NIRF imaging allows more accurate real-time tumor delineation. Consequently, both radionuclide and NIRF imaging might complement each other, and dual-modality image-guided surgery may overcome limitations of the currently used single-modality imaging techniques. In this review, a comprehensive overview on recent preclinical advances in tumor-targeted radionuclide and fluorescence dual-modality imaging is provided. Subsequently, the clinical applicability of dual-modality image-guided surgery is discussed.
Similar content being viewed by others
References
Jemal A, Bray F, Center MM et al (2011) Global cancer statistics. CA Cancer J Clin 61:69–90
Bristow RE, Puri I, Chi DS (2009) Cytoreductive surgery for recurrent ovarian cancer: a meta-analysis. Gynecol Oncol 112:265–274
Cao C, Yan TD, Black D, Morris DL (2009) A systematic review and meta-analysis of cytoreductive surgery with perioperative intraperitoneal chemotherapy for peritoneal carcinomatosis of colorectal origin. Ann Surg Oncol 16:2152–2165
Povoski SP, Neff RL, Mojzisik CM et al (2009) A comprehensive overview of radioguided surgery using gamma detection probe technology. World J Surg Oncol 7:11
Vermeeren L, Klop WM, van den Brekel MW et al (2009) Sentinel node detection in head and neck malignancies: innovations in radioguided surgery. J Oncol 2009:681746
Azhdarinia A, Ghosh P, Ghosh S et al (2012) Dual-labeling strategies for nuclear and fluorescence molecular imaging: a review and analysis. Mol Imaging Biol 14:261–276
Terwisscha van Scheltinga AG, van Dam GM, Nagengast WB et al (2011) Intraoperative near-infrared fluorescence tumor imaging with vascular endothelial growth factor and human epidermal growth factor receptor 2 targeting antibodies. J Nucl Med 52:1778–1785
Cohen R, Stammes MA, de Roos HC et al (2011) Inert coupling of IRDye800CW to monoclonal antibodies for clinical imaging of tumor targets. EJNMMI Res 1:31
Keereweer S, Van Driel PB, Snoeks TJ et al (2013) Optical image-guided cancer surgery: challenges and limitations. Clin Cancer Res 19:3745–3754
Somasundaram SK, Chicken DW, Keshtgar MR (2007) Detection of the sentinel lymph node in breast cancer. Br Med Bull 84:117–131
van de Lande J, Torrenga B, Raijmakers PG et al (2007) Sentinel lymph node detection in early stage uterine cervix carcinoma: a systematic review. Gynecol Oncol 106:604–613
Côté V, Kost K, Payne RJ, Hier MP (2007) Sentinel lymph node biopsy in squamous cell carcinoma of the head and neck: where we stand now, and where we are going. J Otolaryngol 36:344–349
Harlow SP, Krag DN, Ashikaga T et al (2001) Gamma probe guided biopsy of the sentinel node in malignant melanoma: a multicentre study. Melanoma Res 11:45–55
Fortuin A, Md R, Zamecnik P et al (2013) Molecular and functional imaging for detection of lymph node metastases in prostate cancer. Int J Mol Sci 14:13842–13875
Bai M, Bornhop DJ (2012) Recent advances in receptor-targeted fluorescent probes for in vivo cancer imaging. Curr Med Chem 19:4742–4758
Patterson MS, Chance B, Wilson BC (1989) Time resolved reflectance and transmittance for the non-invasive measurement of tissue optical properties. Appl Opt 28:2331–2336
Fomina N, McFearin CL, Sermsakdi M et al (2011) Low power, biologically benign NIR light triggers polymer disassembly. Macromolecules 44:8590–8597
East JM, Valentine CS, Kanchev E, Blake GO (2009) Sentinel lymph node biopsy for breast cancer using methylene blue dye manifests a short learning curve among experienced surgeons: a prospective tabular cumulative sum (CUSUM) analysis. BMC Surg 9:2
Kiesslich R, Fritsch J, Holtmann M et al (2003) Methylene blue-aided chromoendoscopy for the detection of intraepithelial neoplasia and colon cancer in ulcerative colitis. Gastroenterology 124:880–888
Keereweer S, Kerrebijn JD, van Driel PB et al (2011) Optical image-guided surgery—where do we stand? Mol Imaging Biol 13:199–207
Polom K, Murawa D, Rho YS et al (2011) Current trends and emerging future of indocyanine green usage in surgery and oncology: a literature review. Cancer 117:4812–4822
van der Poel HG, Buckle T, Brouwer OR et al (2011) Intraoperative laparoscopic fluorescence guidance to the sentinel lymph node in prostate cancer patients: clinical proof of concept of an integrated functional imaging approach using a multimodal tracer. Eur Urol 60:826–833
van den Berg NS, Valdés-Olmos RA, van der Poel HG, van Leeuwen FW (2013) Sentinel lymph node biopsy for prostate cancer: a hybrid approach. J Nucl Med 54:493–496
Schaafsma BE, Verbeek FP, Rietbergen DD et al (2013) Clinical trial of combined radio- and fluorescence-guided sentinel lymph node biopsy in breast cancer. Br J Surg 100:1037–1044
Brouwer OR, Klop WM, Buckle T et al (2012) Feasibility of sentinel node biopsy in head and neck melanoma using a hybrid radioactive and fluorescent tracer. Ann Surg Oncol 19:1988–1994
van den Berg NS, Brouwer OR, Klop WM et al (2012) Concomitant radio- and fluorescence-guided sentinel lymph node biopsy in squamous cell carcinoma of the oral cavity using ICG-(99m)Tc-nanocolloid. Eur J Nucl Med Mol Imaging 39:1128–1136
Kelloff GJ, Krohn KA, Larson SM et al (2005) The progress and promise of molecular imaging probes in oncologic drug development. Clin Cancer Res 11:7967–7985
Luo S, Zhang E, Su Y et al (2011) A review of NIR dyes in cancer targeting and imaging. Biomaterials 32:7127–7138
Zhang Y, Hong H, Engle JW et al (2012) Positron emission tomography and near-infrared fluorescence imaging of vascular endothelial growth factor with dual-labeled bevacizumab. Am J Nucl Med Mol Imaging 2:1–13
Sampath L, Kwon S, Ke S et al (2007) Dual-labeled trastuzumab-based imaging agent for the detection of human epidermal growth factor receptor 2 overexpression in breast cancer. J Nucl Med 48:1501–1510
Sampath L, Kwon S, Hall MA et al (2010) Detection of cancer metastases with a dual-labeled near-infrared/positron emission tomography imaging agent. Transl Oncol 3:307–217
Zhang Y, Hong H, Severin GW et al (2012) ImmunoPET and near-infrared fluorescence imaging of CD105 expression using a monoclonal antibody dual-labeled with (89)Zr and IRDye 800CW. Am J Transl Res 4:333–346
Hall MA, Kwon S, Robinson H et al (2012) Imaging prostate cancer lymph node metastases with a multimodality contrast agent. Prostate 72:129–146
Hall MA, Pinkston KL, Wilganowski N et al (2012) Comparison of mAbs targeting epithelial cell adhesion molecule for the detection of prostate cancer lymph node metastases with multimodal contrast agents: quantitative small-animal PET/CT and NIRF. J Nucl Med 53:1427–1437
Banerjee SR, Pullambhatla M, Byun Y et al (2011) Sequential SPECT and optical imaging of experimental models of prostate cancer with a dual modality inhibitor of the prostate-specific membrane antigen. Angew Chem Int Ed Engl 50:9167–9170
Azhdarinia A, Wilganowski N, Robinson H et al (2011) Characterization of chemical, radiochemical and optical properties of a dual-labeled MMP-9 targeting peptide. Bioorg Med Chem 19:3769–3776
Huang M, Xiong C, Lu W et al (2014) Dual-modality micro-positron emission tomography/computed tomography and near-infrared fluorescence imaging of EphB4 in orthotopic glioblastoma xenograft models. Mol Imaging Biol 16:74–84
Meadows KL, Hurwitz HI (2012) Anti-VEGF therapies in the clinic. Cold Spring Harb Perspect Med 2(10). doi:10.1101/cshperspect.a006577
Yarden Y (2011) Biology of HER2 and its importance in breast cancer. Oncology 61(Suppl 2):1–13
Ogawa M, Regino CA, Seidel J et al (2009) Dual-modality molecular imaging using antibodies labeled with activatable fluorescence and a radionuclide for specific and quantitative targeted cancer detection. Bioconjug Chem 20:2177–2184
Faybik P, Hetz H (2006) Plasma disappearance rate of indocyanine green in liver dysfunction. Transplant Proc 38:801–802
Fonsatti E, Nicolay HJ, Altomonte M et al (2010) Targeting cancer vasculature via endoglin/CD105: a novel antibody-based diagnostic and therapeutic strategy in solid tumours. Cardiovasc Res 86:12–19
Dallas NA, Samuel S, Xia L et al (2008) Endoglin (CD105): a marker of tumor vasculature and potential target for therapy. Clin Cancer Res 14:1931–1937
Seon BK, Haba A, Matsuno F et al (2011) Endoglin-targeted cancer therapy. Curr Drug Deliv 8:135–143
Hong H, Zhang Y, Severin GW et al (2012) Multimodality imaging of breast cancer experimental lung metastasis with bioluminescence and a monoclonal antibody dual-labeled with (89)Zr and IRDye 800CW. Mol Pharm 9:2339–2349
Zhang Y, Hong H, Nayak TR et al (2013) Imaging tumor angiogenesis in breast cancer experimental lung metastasis with positron emission tomography, near-infrared fluorescence, and bioluminescence. Angiogenesis 16:663–674
Went P, Vasei M, Bubendorf L et al (2006) Frequent high-level expression of the immunotherapeutic target Ep-CAM in colon, stomach, prostate and lung cancers. Br J Cancer 94:128–135
Schülke N, Varlamova OA, Donovan GP et al (2003) The homodimer of prostate-specific membrane antigen is a functional target for cancer therapy. Proc Natl Acad Sci U S A 100:12590–12595
Malik N, Machulla HJ, Solbach C et al (2011) Radiosynthesis of a new PSMA targeting ligand ([18F]FPy-DUPA-Pep). Appl Radiat Isot 69:1014–1018
Silver DA, Pellicer I, Fair WR et al (1997) Prostate-specific membrane antigen expression in normal and malignant human tissues. Clin Cancer Res 3:81–85
Lütje S, Rijpkema M, Franssen GM et al (2014) Dual-modality image-guided surgery of prostate cancer with a radiolabeled fluorescent anti-PSMA monoclonal antibody. J Nucl Med. doi:10.2967/jnumed.114.138180
Paudyal P, Paudyal B, Iida Y et al (2009) Dual functional molecular imaging probe targeting CD20 with PET and optical imaging. Oncol Rep 22:115–119
van Dam GM, Themelis G, Crane LM et al (2011) Intraoperative tumor-specific fluorescence imaging in ovarian cancer by folate receptor-α targeting: first in-human results. Nat Med 17:1315–1319
Conflict of Interest
The authors declare they have no conflicts of interest.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Lütje, S., Rijpkema, M., Helfrich, W. et al. Targeted Radionuclide and Fluorescence Dual-modality Imaging of Cancer: Preclinical Advances and Clinical Translation. Mol Imaging Biol 16, 747–755 (2014). https://doi.org/10.1007/s11307-014-0747-y
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11307-014-0747-y