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Molecular Imaging and Biology

, Volume 19, Issue 3, pp 357–362 | Cite as

Optical Surgical Navigation for Precision in Tumor Resections

  • Stefan Harmsen
  • Nutte Teraphongphom
  • Michael F. Tweedle
  • James P. Basilion
  • Eben L. Rosenthal
Special Topic

Abstract

Optical imaging methods have significant potential as effective intraoperative tools to visualize tissues, cells, and biochemical events aimed at objective assessment of the tumor margin and guiding the surgeon to adequately resect the tumor while sparing critical tissues. The wide variety of approaches to guide resection, the range of parameters that they detect, and the interdisciplinary nature involving biology, chemistry, engineering, and medicine suggested that there was a need for an organization that could review, discuss, refine, and help prioritize methods to optimize patient care and pharmaceutical and instrument development. To address these issues, the World Molecular Imaging Society created the Optical Surgical Navigation (OSN) interest group to bring together scientists, engineers, and surgeons to develop the field to benefit patients. Here, we provide an overview of approaches currently under clinical investigation for optical surgical navigation and offer our perspective on upcoming strategies.

Key words

Optical navigation Surgery Image guidance Probes Oncology 

Notes

Author Contribution

S.H. and N.T. wrote the manuscript. M.F.T., J.P.B., and E.L.R. wrote and revised the manuscript. All authors reviewed and approved the manuscript.

Compliance with Ethical Standards

Conflict of Interests

S.H., N.T., M.F.T., and E.L.R. declare no conflicts of interests. J.P.B. has an interest in Akrotome Imaging Inc., a company developing probes in this space, and consults for Vergent Biosciences and LightPoint Medical Ltd.

References

  1. 1.
    Hinni ML, Ferlito A, Brandwein-Gensler MS et al (2013) Surgical margins in head and neck cancer: a contemporary review. Head Neck 35:1362–1370CrossRefPubMedGoogle Scholar
  2. 2.
    Woolgar JA, Triantafyllou A (2005) A histopathological appraisal of surgical margins in oral and oropharyngeal cancer resection specimens. Oral Oncol 41:1034–1043CrossRefPubMedGoogle Scholar
  3. 3.
    Stummer W, Novotny A, Stepp H et al (2000) Fluorescence-guided resection of glioblastoma multiforme by using 5-aminolevulinic acid-induced porphyrins: a prospective study in 52 consecutive patients. J Neurosurg 93:1003–1013CrossRefPubMedGoogle Scholar
  4. 4.
    Stummer W, Pichlmeier U, Meinel T et al (2006) Fluorescence-guided surgery with 5-aminolevulinic acid for resection of malignant glioma: a randomised controlled multicentre phase III trial. Lancet Oncol 7:392–401CrossRefPubMedGoogle Scholar
  5. 5.
    Garland M, Yim JJ, Bogyo M (2016) A bright future for precision medicine: advances in fluorescent chemical probe design and their clinical application. Cell Chem Biol 23:122–136CrossRefPubMedPubMedCentralGoogle Scholar
  6. 6.
    Rosenthal EL, Warram JM, de Boer E et al (2016) Successful translation of fluorescence navigation during oncologic surgery: a consensus report. J Nucl Med 57:144–150CrossRefPubMedGoogle Scholar
  7. 7.
    Tummers QR, Verbeek FP, Schaafsma BE et al (2014) Real-time intraoperative detection of breast cancer using near-infrared fluorescence imaging and methylene blue. Eur J Surg Oncol 40:850–858CrossRefPubMedPubMedCentralGoogle Scholar
  8. 8.
    Schaafsma BE, Mieog JSD, Hutteman M et al (2011) The clinical use of indocyanine green as a near-infrared fluorescent contrast agent for image-guided oncologic surgery. J Surg Oncol 104:323–332CrossRefPubMedPubMedCentralGoogle Scholar
  9. 9.
    Ishizawa T, Fukushima N, Shibahara J et al (2009) Real-time identification of liver cancers by using indocyanine green fluorescent imaging. Cancer 115:2491–2504CrossRefPubMedGoogle Scholar
  10. 10.
    Satou S, Ishizawa T, Masuda K et al (2013) Indocyanine green fluorescent imaging for detecting extrahepatic metastasis of hepatocellular carcinoma. J Gastroenterol 48:1136–1143CrossRefPubMedGoogle Scholar
  11. 11.
    van der Vorst JR, Schaafsma BE, Hutteman M et al (2013) Near-infrared fluorescence-guided resection of colorectal liver metastases. Cancer 119:3411–3418CrossRefPubMedPubMedCentralGoogle Scholar
  12. 12.
    Keating J, Tchou J, Okusanya O et al (2016) Identification of breast cancer margins using intraoperative near-infrared imaging. J Surg Oncol 113:508–514CrossRefPubMedGoogle Scholar
  13. 13.
    Holt D, Okusanya O, Judy R, et al. (2014) Intraoperative near-infrared imaging can distinguish cancer from normal tissue but not inflammation. Plos One 9Google Scholar
  14. 14.
    Jiang JX, Keating JJ, Jesus EM et al (2015) Optimization of the enhanced permeability and retention effect for near-infrared imaging of solid tumors with indocyanine green. Am J Nucl Med Mol Imaging 5:390–400PubMedPubMedCentralGoogle Scholar
  15. 15.
    van Dam GM, Themelis G, Crane LM et al (2011) Intraoperative tumor-specific fluorescence imaging in ovarian cancer by folate receptor-alpha targeting: first in-human results. Nat Med 17:1315–1319CrossRefPubMedGoogle Scholar
  16. 16.
    De Jesus E, Keating JJ, Kularatne SA et al (2015) Comparison of folate receptor targeted optical contrast agents for intraoperative molecular imaging. Int J Mol Imaging 2015:469047CrossRefPubMedPubMedCentralGoogle Scholar
  17. 17.
    Hoogstins CES, Tummers QRJG, Gaarenstroom KN et al (2016) A novel tumor-specific agent for intraoperative near-infrared fluorescence imaging: a translational study in healthy volunteers and patients with ovarian cancer. Clin Cancer Res 22:2929–2938CrossRefPubMedGoogle Scholar
  18. 18.
    Chen H, Niu G, Wu H, Chen X (2016) Clinical application of radiolabeled RGD peptides for PET imaging of integrin alphavbeta3. Theranostics 6:78–92CrossRefPubMedPubMedCentralGoogle Scholar
  19. 19.
    Mansi R, Fleischmann A, Macke HR, Reubi JC (2013) Targeting GRPR in urological cancers—from basic research to clinical application. Nat Rev Urol 10:235–244CrossRefPubMedGoogle Scholar
  20. 20.
    Mojtahedi A, Thamake S, Tworowska I et al (2014) The value of 68Ga-DOTATATE PET/CT in diagnosis and management of neuroendocrine tumors compared to current FDA approved imaging modalities: a review of literature. Am J Nucl Med Mol Imaging 4:426–434PubMedPubMedCentralGoogle Scholar
  21. 21.
    Patil C, Walker D, Butte P et al (2015) Phase 1 dose escalation and expansion safety study opf blz-100 for fluorescence guided resection of glioma in adults [abstract]. Neuro-Oncology 17:v14CrossRefPubMedCentralGoogle Scholar
  22. 22.
    Burggraaf J, Kamerling IMC, Gordon PB et al (2015) Detection of colorectal polyps in humans using an intravenously administered fluorescent peptide targeted against c-Met. Nat Med 21:955–961CrossRefPubMedGoogle Scholar
  23. 23.
    Sturm MB, Joshi BP, Lu S et al (2013) Targeted imaging of esophageal neoplasia with a fluorescently labeled peptide: first-in-human results. Sci Transl Med 5:184ra161CrossRefGoogle Scholar
  24. 24.
    O’Neil BH, Allen R, Spigel DR et al (2007) High incidence of cetuximab-related infusion reactions in Tennessee and North Carolina and the association with atopic history. J Clin Oncol 25:3644–3648CrossRefPubMedGoogle Scholar
  25. 25.
    Kim GP, Grothey A (2008) Targeting colorectal cancer with human anti-EGFR monoclonocal antibodies: focus on panitumumab. Biologics 2:223–228PubMedPubMedCentralGoogle Scholar
  26. 26.
    Day KE, Sweeny L, Kulbersh B et al (2013) Preclinical comparison of near-infrared-labeled cetuximab and panitumumab for optical imaging of head and neck squamous cell carcinoma. Mol Imaging Biol 15:722–729CrossRefPubMedPubMedCentralGoogle Scholar
  27. 27.
    Lamberts LE, Koch M, de Jong JS, et al. (2016) Tumor-specific uptake of fluorescent bevacizumab-IRDye800CW microdosing in patients with primary breast cancer: a phase I feasibility study. Clin Cancer ResGoogle Scholar
  28. 28.
    Sexton K, Tichauer K, Samkoe KS et al (2013) Fluorescent affibody peptide penetration in glioma margin is superior to full antibody. PLoS One 8:e60390CrossRefPubMedPubMedCentralGoogle Scholar
  29. 29.
    Olson OC, Joyce JA (2015) Cysteine cathepsin proteases: regulators of cancer progression and therapeutic response. Nat Rev Cancer 15:712–729CrossRefPubMedGoogle Scholar
  30. 30.
    Whitley MJ, Cardona DM, Lazarides AL et al (2016) A mouse-human phase 1 co-clinical trial of a protease-activated fluorescent probe for imaging cancer. Sci Transl Med 8:320ra324CrossRefGoogle Scholar
  31. 31.
    Zinn KR, Korb M, Samuel S et al (2015) IND-directed safety and biodistribution study of intravenously injected cetuximab-IRDye800 in cynomolgus macaques. Mol Imaging Biol 17:49–57CrossRefPubMedPubMedCentralGoogle Scholar
  32. 32.
    Phillips E, Penate-Medina O, Zanzonico PB et al (2014) Clinical translation of an ultrasmall inorganic optical-PET imaging nanoparticle probe. Sci Transl Med:6:260ra149Google Scholar
  33. 33.
    Blanco E, Shen H, Ferrari M (2015) Principles of nanoparticle design for overcoming biological barriers to drug delivery. Nat Biotechnol 33:941–951CrossRefPubMedPubMedCentralGoogle Scholar
  34. 34.
    Mohs AM, Mancini MC, Singhal S et al (2010) Hand-held spectroscopic device for in vivo and intraoperative tumor detection: contrast enhancement, detection sensitivity, and tissue penetration. Anal Chem 82:9058–9065CrossRefPubMedGoogle Scholar
  35. 35.
    Rosenthal EL, Warram JM, de Boer E et al (2015) Safety and tumor specificity of cetuximab-IRDye800 for surgical navigation in head and neck cancer. Clin Cancer Res 21:3658–3666CrossRefPubMedPubMedCentralGoogle Scholar
  36. 36.
    DSouza AV, Lin H, Henderson ER et al (2016) Review of fluorescence guided surgery systems: identification of key performance capabilities beyond indocyanine green imaging. J Biomed Opt 21:80901CrossRefPubMedGoogle Scholar
  37. 37.
    Troyan SL, Kianzad V, Gibbs-Strauss SL et al (2009) The FLARE((TM)) intraoperative near-infrared fluorescence imaging system: a first-in-human clinical trial in breast cancer sentinel lymph node mapping. Ann Surg Oncol 16:2943–2952CrossRefPubMedPubMedCentralGoogle Scholar
  38. 38.
    Mieog JS, Troyan SL, Hutteman M et al (2011) Toward optimization of imaging system and lymphatic tracer for near-infrared fluorescent sentinel lymph node mapping in breast cancer. Ann Surg Oncol 18:2483–2491CrossRefPubMedPubMedCentralGoogle Scholar
  39. 39.
    Eljamel MS, Goodman C, Moseley H (2008) ALA and photofrin (R) fluorescence-guided resection and repetitive PDT in glioblastoma multiforme: a single Centre phase III randomised controlled trial. Laser Med Sci 23:361–367CrossRefGoogle Scholar
  40. 40.
    Penson DF, McLerran D, Feng Z et al (2008) 5-year urinary and sexual outcomes after radical prostatectomy: results from the prostate cancer outcomes study (reprinted from The Journal of Urology, vol 173, pg 1701-1705, 2005). J Urol 179:S40–S44CrossRefPubMedGoogle Scholar
  41. 41.
    Gibbs-Strauss SL, Nasr KA, Fish KM et al (2011) Nerve-highlighting fluorescent contrast agents for image-guided surgery. Mol Imaging 10:91–101PubMedPubMedCentralGoogle Scholar
  42. 42.
    Whitney MA, Crisp JL, Nguyen LT et al (2011) Fluorescent peptides highlight peripheral nerves during surgery in mice. Nat Biotechnol 29:352–356CrossRefPubMedPubMedCentralGoogle Scholar
  43. 43.
    Azzouzi AR, Vincendeau S, Barret E, et al. (2016) Padeliporfin vascular-targeted photodynamic therapy versus active surveillance in men with low-risk prostate cancer (CLIN1001 PCM301): an open-label, phase 3, randomised controlled trial. Lancet OncolGoogle Scholar
  44. 44.
    Antaris AL, Chen H, Cheng K et al (2016) A small-molecule dye for NIR-II imaging. Nat Mater 15:235–242CrossRefPubMedGoogle Scholar
  45. 45.
    Wang TD, Mandella MJ, Contag CH, Kino GS (2003) Dual-axis confocal microscope for high-resolution in vivo imaging. Opt Lett 28:414–416CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© World Molecular Imaging Society 2017

Authors and Affiliations

  • Stefan Harmsen
    • 1
  • Nutte Teraphongphom
    • 2
  • Michael F. Tweedle
    • 3
  • James P. Basilion
    • 4
    • 5
    • 6
  • Eben L. Rosenthal
    • 7
    • 8
  1. 1.Department of PediatricsStanford UniversityStanfordUSA
  2. 2.Department of Otolaryngology—Head and Neck SurgeryStanford UniversityStanfordUSA
  3. 3.Department of Radiology, The Wright Center for Innovation in Biomedical ImagingThe Ohio State University College of MedicineColumbusUSA
  4. 4.Department of Biomedical EngineeringCase Western Reserve UniversityClevelandUSA
  5. 5.Department of RadiologyCase Western Reserve UniversityClevelandUSA
  6. 6.National Foundation for Cancer Research Center for Molecular ImagingCase Western Reserve UniversityClevelandUSA
  7. 7.Department of Otolaryngology—Head and Neck Surgery and RadiologyStanford UniversityStanfordUSA
  8. 8.Ann and John Doerr Medical Director, Stanford Cancer CenterStanfordUSA

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