Skip to main content

Advertisement

Log in

Hybrid tracers and devices for intraoperative imaging: the future for radioguided surgery?

  • Review Article
  • Published:
Clinical and Translational Imaging Aims and scope Submit manuscript

Abstract

Radioguided surgery (RS) allows surgeons to identify tissues of interest that were preoperatively or intraoperatively marked with radiotracers. This discipline has seen major changes related to the development of new tracers, instrumentation and software. The goal of this review is to comment on current development and perspectives in the RS field. The review is based on published papers that highlight the role of RS and explore current advances such as the Guided intraOperative Scintigraphic Tumour Targeting (GOSTT) concept, which established the see, open and see strategy and propose a new one, Guided Hybrid intraOperative Specific Targeting (GHOST). We examine the development of radioactive, fluorescent and hybrid tracers and corresponding instrumentation and software to detect them and suggest ways in which these developments could be integrated. The role of hybrid tracers in RS, in particular 99mTc nanocolloid indocyanine green on sentinel node procedures, is highlighted. Labeled specific targeted peptides, antibodies and nanostructures will allow better preoperative diagnosis and intraoperative localization of tissue of interest. Photodynamic therapy could be applied during surgery to eliminate residual tumoral tissue. In the follow up, patients could be considered for treatment with targeted radiotherapy. RS has moved from open surgery to laparoscopic and robotic surgery. In each of them it is possible to add fluorescent, radioactive and hybrid modules able to detect labeled tissue of interest, while preserving healthy ones. As we have seen, RS is advancing through an interdisciplinary collaboration that will provide surgeons with new tools to improve surgical outcomes.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  1. Zaknun JJ, Giammarile F, Valdés Olmos RA, Vidal-Sicart S, Mariani G (2012) Changing in radioguided surgery and intraoperative imaging: the GOSTT concept. Eur J Nucl Med Mol Imaging 39:1–3. doi:10.1007/s00259-011-1951-5

    Article  PubMed  Google Scholar 

  2. Valdés Olmos RA, Vidal-Sicart S, Giammarile F, Zaknun JJ, Van Leeuwen FW, Mariani G (2014) The GOSTT concept and hybrid mixed/virtual/augmented reality environment radioguided surgery. Q J Nucl Med Mol Imaging 58(2):207–215

    PubMed  Google Scholar 

  3. Ikeda Y, Takayama J, Takami H (2010) Minimally invasive radioguided parathyroidectomy for hyperparathyroidism. Ann Nucl Med 24(4):233–240. doi:10.1007/s12149-010-0366-x

    Article  PubMed  Google Scholar 

  4. García-Talavera P, Ruano R, Riojac ME, Cordero JM, Razola P, Vidal-Sicart S (2014) Radioguided surgery in neuroendocrine tumors. A review of the literature. Rev Esp Med Nucl Imagen Mol 33(6):358–365. doi:10.1016/j.remn.2014.07.004

    PubMed  Google Scholar 

  5. Moncayo VM, Aarsvold JN, Alazraki NP (2015) Lymphoscintigraphy and sentinel nodes. J Nucl Med 56(6):901–907. doi:10.2967/jnumed.114.141432

    Article  PubMed  Google Scholar 

  6. Liu Z, Niu G, Wang F, Chen X (2009) (68)Ga-labeled NOTA-RGD-BBN peptide for dual integrin and GRPR-targeted tumor imaging. Eur J Nucl Med Mol Imaging 36(9):1483–1494. doi:10.1007/s00259-009-1123-z

    Article  CAS  PubMed  Google Scholar 

  7. Wang W, Ke S, Kwon S, Yallampalli S, Cameron AG, Adams KE, Mawad ME, Sevick-Muraca EM (2007) A new optical and nuclear dual-labeled imaging agent targeting interleukin 11 receptor alpha-chain. Bioconjug Chem 18(2):397–402

    Article  CAS  PubMed  Google Scholar 

  8. Alander JT, Kaartinen I, Laakso A, Pätilä T, Spillmann T, Tuchin VV, Venermo M, Välisuo P (2012) A review of indocyanine green fluorescent imaging in surgery. Int J Biomed Imaging 2012:940585. doi:10.1155/2012/940585

    Article  PubMed  PubMed Central  Google Scholar 

  9. Zelken JA, Tufaro AP (2015) Current trends and emerging future of indocyanine green usage in surgery and oncology: an update. Ann Surg Oncol 22(3):1271–1283. doi:10.1245/s10434-015-4743-5

    Article  Google Scholar 

  10. Lozano N, Al-Ahmady ZS, Beziere NS, Ntziachristos V, Kostarelos K (2015) Monoclonal antibody-targeted PEGylated liposome ICG encapsulating doxorubicin as a potential theranostic agent. Int J Pharm 482(1–2):2–10. doi:10.1016/j.ijpharm.2014.10.045

    Article  CAS  PubMed  Google Scholar 

  11. Bahmani B, Guerrero Y, Bacon D, Kundra V, Vullev VI, Anvari B (2014) Functionalized polymeric nanoparticles loaded with indocyanine green as theranostic materials for targeted molecular near infrared fluorescence imaging and photothermal destruction of ovarian cancer cells. Lasers Surg Med 46(7):582–592. doi:10.1002/lsm.22269

    Article  PubMed  Google Scholar 

  12. Costa RA, Scapucin L, Moracs NS, Calucci D, Melo LA, Cardillo JA, Farah ME (2002) Indocyanine green-mediated photothrombosis as a new technique of treatment for persistent central serous chorioretinopathy. Curr Eye Res 25:287–297

    Article  PubMed  Google Scholar 

  13. Klein A, Szeimies RM, Baumler W, Zeman F, Schreml S, Hohenleutner U, Landthaler M, Koller M, Babilas P (2012) Indocyanine green-augmented diode laser treatment of port-wine stains: clinical and histological evidence for a new treatment option from a randomized controlled trial. Br J Dermatol 167:333–342. doi:10.1111/j.1365-2133.2012.10950.x

    Article  CAS  PubMed  Google Scholar 

  14. Klein A, Baumler H, Buschmann M, Landthaler M, Babilas P (2013) A randomized controlled trial to optimize indocyanine green augmented diode laser therapy of capillary malformations. Lasers Surg Med 45:216–224. doi:10.1002/lsm.22136

    Article  PubMed  Google Scholar 

  15. Genina EA, Bashkatov AN, Simonenko GV, Odoevskaya OD, Tuchin VV, Altshuler GB (2004) Low-intensity indocyanine-green laser phototherapy of acne vulgaris: pilot study. J Biomed Opt 9(4):828–834

    Article  PubMed  Google Scholar 

  16. Ballardini B, Santoro L, Sangalli C, Gentilini O, Renne G, Lissidini G, Pagani GM, Toesca A, Blundo C, del Castillo A, Peradze N, Caldarella P, Veronesi P (2013) The indocyanine green method is equivalent to the 99mTc-labeled radiotracer method for identifying the sentinel node in breast cancer: a concordance and validation study. Eur J Surg Oncol 39(12):1332–1336. doi:10.1016/j.ejso.2013.10.004

    Article  CAS  PubMed  Google Scholar 

  17. Samorani D, Fogacci T, Frisoni G, Accardi FG, Panzini I, Tassinari D (2014) Comment to: Ballardini B, Santoro L, Sangalli C, et al. The indocyanine green method is equivalent to the 99mTc-labeled radiotracer method for identifying the sentinel node in breast cancer: a concordance and validation study. Eur J Surg Oncol 40(6):782–783. doi:10.1016/j.ejso.2014.01.022

    Article  CAS  PubMed  Google Scholar 

  18. Guo W, Zhang L, Ji J, Gao W, Liu J, Tong M (2014) Breast cancer sentinel lymph node mapping using near-infrared guided indocyanine green in comparison with blue dye. Tumour Biol 35(4):3073–3078. doi:10.1007/s13277-013-1399-2

    Article  CAS  PubMed  Google Scholar 

  19. Stoffels I, Dissemond J, Pöppel T, Schadendorf D, Klode J (2015) Intraoperative fluorescence imaging for sentinel lymph node detection: prospective clinical trial to compare the usefulness of indocyanine green vs technetium Tc 99m for identification of sentinel lymph nodes. JAMA Surg 150(7):617–623. doi:10.1001/jamasurg.2014.3502

    Article  PubMed  Google Scholar 

  20. Brouwer OR, Buckle T, Vermeeren L, Klop WM, Balm AJ, van der Poel HG, van Rhijn BW, Horenblas S, Nieweg OE, van Leeuwen FW, Valdés Olmos RA (2012) Comparing the hybrid fluorescent-radioactive tracer indocyanine green-99mTc-nanocolloid with 99mTc-nanocolloid for sentinel node identification: a validation study using lymphoscintigraphy and SPECT/CT. J Nucl Med 53(7):1034–1040. doi:10.2967/jnumed.112.103127

    Article  CAS  PubMed  Google Scholar 

  21. Stoffels I, Leyh J, Pöppel T, Schadendorf D, Klode J (2015) Evaluation of a radioactive and fluorescent hybrid tracer for sentinel lymph node biopsy in head and neck malignancies: prospective randomized clinical trial to compare ICG-(99m)Tc-nanocolloid hybrid tracer versus (99m)Tc-nanocolloid. Eur J Nucl Med Mol Imaging 42(11):1631–1638. doi:10.1007/s00259-015-3093-7

    Article  CAS  PubMed  Google Scholar 

  22. van den Berg NS, Brouwer OR, Schaafsma BE, Mathéron HM, Klop WM, Balm AJ, van Tinteren H, Nieweg OE, van Leeuwen FW, Valdés Olmos RA (2015) Multimodal surgical guidance during sentinel node biopsy for melanoma: combined gamma tracing and fluorescence imaging of the sentinel node through use of the hybrid tracer indocyanine green-(99m)Tc-nanocolloid. Radiology 275(2):521–529. doi:10.1148/radiol.14140322

    Article  PubMed  Google Scholar 

  23. Schaafsma BE, Verbeek FP, Rietbergen DD, van der Hiel B, van der Vorst JR, Liefers GJ, Frangioni JV, van de Velde CJ, van Leeuwen FW, Vahrmeijer AL (2013) Clinical trial of combined radio- and fluorescence-guided sentinel lymph node biopsy in breast cancer. Br J Surg 100(8):1037–1044. doi:10.1002/bjs.9159

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. van der Poel HG, Buckle T, Brouwer OR, Valdés Olmos RA, van Leeuwen FW (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(4):826–833. doi:10.1016/j.eururo.2011.03.024

    Article  PubMed  Google Scholar 

  25. KleinJan GH, van den Berg NS, Brouwer OR, de Jong J, Acar C, Wit EM, Vegt E, van der Noort V, Valdés Olmos RA, van Leeuwen FW, van der Poel HG (2014) Optimisation of fluorescence guidance during robot-assisted laparoscopic sentinel node biopsy for prostate cancer. Eur Urol 66(6):991–998. doi:10.1016/j.eururo.2014.07.014

    Article  PubMed  Google Scholar 

  26. Brouwer OR, van den Berg NS, Mathéron HM, van der Poel HG, van Rhijn BW, Bex A, van Tinteren H, Valdés Olmos RA, van Leeuwen FW, Horenblas S (2014) A hybrid radioactive and fluorescent tracer for sentinel node biopsy in penile carcinoma as a potential replacement for blue dye. Eur Urol 65(3):600–609. doi:10.1016/j.eururo.2013.11.014

    Article  CAS  PubMed  Google Scholar 

  27. Mathéron HM, van den Berg NS, Brouwer OR, Kleinjan GH, van Driel WJ, Trum JW, Vegt E, Kenter G, van Leeuwen FW, Valdés Olmos RA (2013) Multimodal surgical guidance towards the sentinel node in vulvar cancer. Gynecol Oncol 131(3):720–725. doi:10.1016/j.ygyno.2013.09.007

    Article  PubMed  Google Scholar 

  28. Vidal-Sicart S, van Leeuwen FW, van den Berg NS, Valdés Olmos RA (2015) Fluorescent radiocolloids: are hybrid tracers the future for lymphatic mapping? Eur J Nucl Med Mol Imaging 42(11):1627–1630. doi:10.1007/s00259-015-3132-4

    Article  PubMed  Google Scholar 

  29. van den Berg NS, Brouwer OR, Klop WM, Karakullukcu B, Zuur CL, Tan IB, Balm AJ, van den Brekel MW, Valdés Olmos RA, van Leeuwen FW (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(7):1128–1136. doi:10.1007/s00259-012-2129-5

    Article  CAS  PubMed  Google Scholar 

  30. Zhang X, Bloch S, Akers W, Achilefu S (2012) Near-infrared molecular probes for in vivo imaging. Curr Protoc Cytom 12(12):27. doi:10.1002/0471142956.cy1227s60

    CAS  PubMed  Google Scholar 

  31. Luo S, Zhang E, Su Y, Cheng T, Shi C (2011) A review of NIR dyes in cancer targeting and imaging. Biomaterials 32(29):7127–7138. doi:10.1016/j.biomaterials.2011.06.024

    Article  CAS  PubMed  Google Scholar 

  32. Emerson DK, Limmer KK, Hall DJ, Han SH, Eckelman WC, Kane CJ, Wallace AM, Vera DR (2012) A receptor-targeted fluorescent radiopharmaceutical for multireporter sentinel lymph node imaging. Radiology 265(1):186–193. doi:10.1148/radiol.12120638

    Article  PubMed  PubMed Central  Google Scholar 

  33. Hosseini A, Baker JL, Tokin CA, Qin Z, Hall DJ, Stupak DG, Hayashi T, Wallace AM, Vera DR (2014) Fluorescent-tilmanocept for tumor margin analysis in the mouse model. J Surg Res 190(2):528–534. doi:10.1016/j.jss.2014.05.012

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Azhdarinia A, Ghosh P, Ghosh S, Wilganowski N, Sevick-Muraca EM (2012) Dual-labeling strategies for nuclear and fluorescence molecular imaging: a review and analysis. Mol Imaging Biol 14(3):261–276. doi:10.1007/s11307-011-0528-9

    Article  PubMed  Google Scholar 

  35. Lütje S, Rijpkema M, Helfrich W, Oyen WJ, Boerman OC (2014) Targeted radionuclide and fluorescence dual-modality imaging of cancer: preclinical advances and clinical translation. Mol Imaging Biol 16(6):747–755. doi:10.1007/s11307-014-0747-y

    Article  PubMed  Google Scholar 

  36. Ghosh SC, Azhdarinia A (2015) Advances in the development of multimodal imaging agents for nuclear/near-infrared fluorescence imaging. Curr Med Chem 22(29):3390–3404. doi:10.2174/0929867322666150904111214

    Article  CAS  PubMed  Google Scholar 

  37. Sampath L, Kwon S, Ke S, Wang W, Schiff R, Mawad ME, Sevick-Muraca EM (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(9):1501–1510. doi:10.2967/jnumed.107.042234

    Article  CAS  PubMed  Google Scholar 

  38. Iqbal N, Iqbal N (2014) Human epidermal growth factor receptor 2 (HER2) in cancers: overexpression and therapeutic implications. Mol Biol Int 2014:852748. doi:10.1155/2014/852748

    Article  PubMed  PubMed Central  Google Scholar 

  39. Edwards WB, Xu B, Akers W, Cheney PP, Liang K, Rogers BE, Anderson CJ, Achilefu S (2008) Agonist-antagonist dilemma in molecular imaging: evaluation of a monomolecular multimodal imaging agent for the somatostatin receptor. Bioconjug Chem 19(1):192–200. doi:10.1021/bc700291m

    Article  CAS  PubMed  Google Scholar 

  40. De Jong M, Valkema R, Jamar F, Kvols LK, Kwekkeboom DJ, Breeman WA, Bakker WH, Smith C, Pauwels S, Krenning EP (2002) Somatostatin receptor-targeted radionuclide therapy of tumors: preclinical and clinical findings. Semin Nucl Med 32(2):133–140. doi:10.1053/snuc.2002.31027

    Article  PubMed  Google Scholar 

  41. Kwekkeboom DJ, de Herder WW, Kam BL, van Eijck CH, van Essen M, Kooij PP, Feelders RA, van Aken MO, Krenning EP (2008) Treatment with the radiolabeled somatostatin analog [177 Lu-DOTA 0, Tyr3]octreotate: toxicity, efficacy, and survival. J Clin Oncol 26(13):2124–2130. doi:10.1200/JCO.2007.15.2553

    Article  CAS  PubMed  Google Scholar 

  42. Banerjee SR, Pullambhatla M, Byun Y, Nimmagadda S, Foss CA, Green G, Fox JJ, Lupold SE, Mease RC, Pomper MG (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(39):9167–9170. doi:10.1002/anie.201102872

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Ahmadzadehfar H, Rahbar K, Kürpig S, Bögemann M, Claesener M, Eppard E, Gärtner F, Rogenhofer S, Schäfers M, Essler M (2015) Early side effects and first results of radioligand therapy with (177)Lu-DKFZ-617 PSMA of castrate-resistant metastatic prostate cancer: a two-centre study. EJNMMI Res 5(1):114. doi:10.1186/s13550-015-0114-2

    PubMed  Google Scholar 

  44. Baum RP, Kulkarni HR, Schuchardt C, Singh A, Wirtz M, Wiessalla S, Schottelius M, Mueller D, Klette I, Wester HJ (2016) Lutetium-177 PSMA radioligand therapy of metastatic castration-resistant prostate cancer: safety and efficacy. J Nucl Med. doi:10.2967/jnumed.115.168443

    Google Scholar 

  45. Kiess A, Minn IL, Vaidyanathan G, Hobbs RF, Josefsson A, Shen C, Brummet M, Chen Y, Choi J, Koumarianou E, Baidoo K, Brechbiel M, Mease RC, Sgouros G, Zalutsky MR, Pomper M (2016) (2S)-2-(3-(1-Carboxy-5-(4-[211At]astatobenzamido)pentyl)ureido)-pentanedioic acid for PSMA-targeted α-particle radiopharmaceutical therapy. J Nucl Med. doi:10.2967/jnumed.116.174300

  46. Maruyama T, Akutsu Y, Suganami A, Tamura Y, Fujito H, Ouchi T, Akanuma N, Isozaki Y, Takeshita N, Hoshino I, Uesato M, Toyota T, Hayashi H, Matsubara H (2015) Treatment of near-infrared photodynamic therapy using a liposomally formulated indocyanine green derivative for squamous cell carcinoma. PLoS One 10(4):e0122849. doi:10.1371/journal.pone.0122849

    Article  PubMed  PubMed Central  Google Scholar 

  47. Jokerst JV, Gambhir SS (2011) Molecular imaging with theranostic nanoparticles. Acc Chem Res 44:1050–1060. doi:10.1021/ar200106e

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Abou DS, Pickett JE, Thorek DL (2015) Nuclear molecular imaging with nanoparticles: radiochemistry, applications and translation. Br J Radiol 88(1054):20150185. doi:10.1259/bjr.20150185

    Article  CAS  PubMed  Google Scholar 

  49. KleinJan HG, Bunschoten A, Brouwer OR, van den Berg NS, Valdés-Olmos RA, van Leeuwen FWB (2013) Multimodal imaging in radioguided surgery. Clin Transl Imaging 1:433–444. doi:10.1007/s40336-013-0039-6

    Article  Google Scholar 

  50. KleinJan GH, van den Berg NS, de Jong J, Wit EM, Thygessen H, Vegt E, van der Poel HG, van Leeuwen FW (2016) Multimodal hybrid imaging agents for sentinel node mapping as a means to (re)connect nuclear medicine to advances made in robot-assisted surgery. Eur J Nucl Med Mol Imaging 7:1278–1287. doi:10.1007/s00259-015-3292-2

    Article  Google Scholar 

  51. Chi C, Du Y, Ye J, Kou D, Qiu J, Wang J, Tian J, Chen X (2014) Intraoperative imaging-guided cancer surgery: from current fluorescence molecular imaging methods to future multi-modality imaging technology. Theranostics 4(11):1072–1084. doi:10.7150/thno.9899

    Article  PubMed  PubMed Central  Google Scholar 

  52. Benezra M, Penate-Medina O, Zanzonico PB, Schaer D, Ow H, Burns A, DeStanchina E, Longo V, Herz E, Iyer S, Wolchok J, Larson SM, Wiesner U, Bradbury MS (2011) Multimodal silica nanoparticles are effective cancer-targeted probes in a model of human melanoma. J Clin Invest 121(7):2768–2780. doi:10.1172/JCI45600

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Phillips E, Penate-Medina O, Zanzonico PB, Carvajal RD, Mohan P, Ye Y, Humm J, Gönen M, Kalaigian H, Schöder H, Strauss HW, Larson SM, Wiesner U, Bradbury MS (2014) Clinical translation of an ultrasmall inorganic optical-PET imaging nanoparticle probe. Sci Transl Med 6(260):260ra149. doi:10.1126/scitranslmed.3009524

    Article  PubMed  PubMed Central  Google Scholar 

  54. Solomon SB, Cornelis F (2016) Interventional molecular imaging. J Nucl Med 57(4):493–496. doi:10.2967/jnumed.115.161190

    Article  PubMed  Google Scholar 

  55. Houston JP, Ke S, Wang W, Li C, Sevick-Muraca EM (2005) Quality analysis of in vivo near-infrared fluorescence and conventional gamma images acquired using a dual-labeled tumor-targeting probe. J Biomed Opt 10(5):054010. doi:10.1117/1.2114748

    Article  PubMed  Google Scholar 

  56. Azhdarinia A, Wilganowski N, Robinson H, Ghosh P, Kwon S, Lazard ZW, Davis AR, Olmsted-Davis E, Sevick-Muraca EM (2011) Characterization of chemical, radiochemical and optical properties of a dual-labeled MMP-9 targeting peptide. Bioorg Med Chem 19(12):3769–3776. doi:10.1016/j.bmc.2011.04.054

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Welling MM, Bunschoten A, Kuil J, Nelissen RG, Beekman FJ, Buckle T, van Leeuwen FW (2015) Development of a hybrid tracer for SPECT and optical imaging of bacterial infections. Bioconjug Chem 26(5):839–849. doi:10.1021/acs.bioconjchem.5b00062

    Article  CAS  PubMed  Google Scholar 

  58. Okusanya OT, Madajewski B, Segal E, Judy BF, Venegas OG, Judy RP, Quatromoni JG, Wang MD, Nie S, Singhal S (2015) Small portable interchangeable imager of fluorescence for fluorescence guided surgery and research. Technol Cancer Res Treat 14(2):213–220. doi:10.7785/tcrt.2012.500400

    PubMed  Google Scholar 

  59. Gambini JP, Tassano M, Vila R, Font M, Queijo P, Laza S, Quinn T, Hermida J, Alonso O, Cabral P (2014) Development of a portable indocyanine green (ICG) detection system to be used in ICG guided surgical procedures. J Nucl Med 55:1447

    Google Scholar 

  60. Liu Y, Bauer AQ, Akers WJ, Sudlow G, Liang K, Shen D, Berezin MY, Culver JP, Achilefu S (2011) Hands-free, wireless goggles for near-infrared fluorescence and real-time image-guided surgery. Surgery 149(5):689–698. doi:10.1016/j.surg.2011.02.007

    Article  PubMed  PubMed Central  Google Scholar 

  61. Ringhausen E, Wang T, Pitts J, Sarder P, Akers WJ (2015) Evaluation of dynamic optical projection of acquired luminescence for sentinel lymph node biopsy in large animals. Technol Cancer Res Treat. doi:10.1177/1533034615604978

    PubMed  Google Scholar 

  62. Zhu N, Mondal S, Gao S, Achilefu S, Gruev V, Liang R (2014) Engineering light-emitting diode surgical light for near-infrared fluorescence image-guided surgical systems. J Biomed Opt 19(7):076018. doi:10.1117/1.JBO.19.7.076018

    Article  PubMed  PubMed Central  Google Scholar 

  63. van den Berg NS, Miwa M, KleinJan GH, Sato T, Maeda Y, van Akkooi AC, Horenblas S, Karakullukcu B, van Leeuwen FW (2016) (Near-infrared) fluorescence-guided surgery under ambient light conditions: a next step to embedment of the technology in clinical routine. Ann Surg Oncol. doi:10.1245/s10434-016-5186-3

    PubMed Central  Google Scholar 

  64. Heller S, Zanzonico P (2011) Nuclear probes and intraoperative gamma cameras. Semin Nucl Med 41(3):166–181. doi:10.1053/j.semnuclmed.2010.12.004

    Article  PubMed  Google Scholar 

  65. Bluemel C, Matthies P, Herrmann K, Povoski SP (2016) 3D scintigraphic imaging and navigation in radioguided surgery: freehand SPECT technology and its clinical applications. Expert Rev Med Devices 2:1–13. doi:10.1586/17434440.2016.1154456

    Google Scholar 

  66. Fuerst B, Sprung J, Pinto F, Frisch B, Wendler T, Simon H, Mengus L, van den Berg N, van der Poel H, van Leeuwen F, Navab N (2016) First robotic SPECT for minimally invasive sentinel lymph node mapping. IEEE Trans Med Imaging 35(3):830–838. doi:10.1109/TMI.2015.2498125

    Article  PubMed  Google Scholar 

  67. Hellingman D, Vidal-Sicart S, de Wit-van der Veen LJ, Paredes P, Valdés Olmos RA (2016) A new portable hybrid camera for fused optical and scintigraphic imaging: first clinical experiences. Clin Nucl Med 41(1):e39–e43. doi:10.1097/RLU.0000000000000874

    Article  PubMed  Google Scholar 

  68. van den Berg NS, Simon H, Kleinjan GH, Engelen T, Bunschoten A, Welling MM, Tijink BM, Horenblas S, Chambron J, van Leeuwen FW (2015) First-in-human evaluation of a hybrid modality that allows combined radio- and (near-infrared) fluorescence tracing during surgery. Eur J Nucl Med Mol Imaging 42(11):1639–1647. doi:10.1007/s00259-015-3109-3

    Article  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Juan Pablo Gambini.

Ethics declarations

Conflict of interest

All authors (Juan Pablo Gambini and Thomas P. Quinn) declare that they have no conflict of interest.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Gambini, J.P., Quinn, T.P. Hybrid tracers and devices for intraoperative imaging: the future for radioguided surgery?. Clin Transl Imaging 4, 343–351 (2016). https://doi.org/10.1007/s40336-016-0198-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s40336-016-0198-3

Keywords

Navigation