Consensus Statement on the Use of Near-Infrared Fluorescence Imaging during Pancreatic Cancer Surgery Based on a Delphi Study: Surgeons' Perspectives on Current Use and Future Recommendations

Lysanne D A N de Muynck, Kevin P White, Adnan Alseidi, Elisa Bannone, Luigi Boni, Michael Bouvet, Massimo Falconi, Hans F Fuchs, Michael Ghadimi, Ines Gockel, Thilo Hackert, Takeaki Ishizawa, Chang Moo Kang, Norihiro Kokudo, Felix Nickel, Stefano Partelli, Elena Rangelova, Rutger Jan Swijnenburg, Fernando Dip, Raul J Rosenthal, Alexander L Vahrmeijer, J Sven D Mieog, Lysanne D A N de Muynck, Kevin P White, Adnan Alseidi, Elisa Bannone, Luigi Boni, Michael Bouvet, Massimo Falconi, Hans F Fuchs, Michael Ghadimi, Ines Gockel, Thilo Hackert, Takeaki Ishizawa, Chang Moo Kang, Norihiro Kokudo, Felix Nickel, Stefano Partelli, Elena Rangelova, Rutger Jan Swijnenburg, Fernando Dip, Raul J Rosenthal, Alexander L Vahrmeijer, J Sven D Mieog

Abstract

Indocyanine green (ICG) is one of the only clinically approved near-infrared (NIR) fluorophores used during fluorescence-guided surgery (FGS), but it lacks tumor specificity for pancreatic ductal adenocarcinoma (PDAC). Several tumor-targeted fluorescent probes have been evaluated in PDAC patients, yet no uniformity or consensus exists among the surgical community on the current and future needs of FGS during PDAC surgery. In this first-published consensus report on FGS for PDAC, expert opinions were gathered on current use and future recommendations from surgeons' perspectives. A Delphi survey was conducted among international FGS experts via Google Forms. Experts were asked to anonymously vote on 76 statements, with ≥70% agreement considered consensus and ≥80% participation/statement considered vote robustness. Consensus was reached for 61/76 statements. All statements were considered robust. All experts agreed that FGS is safe with few drawbacks during PDAC surgery, but that it should not yet be implemented routinely for tumor identification due to a lack of PDAC-specific NIR tracers and insufficient evidence proving FGS's benefit over standard methods. However, aside from tumor imaging, surgeons suggest they would benefit from visualizing vasculature and surrounding anatomy with ICG during PDAC surgery. Future research could also benefit from identifying neuroendocrine tumors. More research focusing on standardization and combining tumor identification and vital-structure imaging would greatly improve FGS's use during PDAC surgery.

Keywords: Delphi; cancer surgery; consensus; fluorescence-guided surgery; indocyanine green; intraoperative imaging; near-infrared fluorescence; pancreatic cancer.

Conflict of interest statement

J.S.D. Mieog is a guest editor for this special issue. All other authors declare they have no conflicts of interest.

References

    1. Bengtsson A., Andersson R., Ansari D. The actual 5-year survivors of pancreatic ductal adenocarcinoma based on real-world data. Sci. Rep. 2020;10:16425. doi: 10.1038/s41598-020-73525-y.
    1. Handgraaf H., Sibinga Mulder B., Shahbazi Feshtali S., Boogerd L., van der Valk M., Fariña Sarasqueta A., Swijnenburg R., Bonsing B., Vahrmeijer A., Mieog J. Staging laparoscopy with ultrasound and near-infrared fluorescence imaging to detect occult metastases of pancreatic and periampullary cancer. PLoS ONE. 2018;13:e0205960. doi: 10.1371/journal.pone.0205960.
    1. Ghaneh P., Kleeff J., Halloran C.M., Raraty M., Jackson R., Melling J., Jones O., Palmer D.H., Cox T.F., Smith C.J., et al. The Impact of Positive Resection Margins on Survival and Recurrence Following Resection and Adjuvant Chemotherapy for Pancreatic Ductal Adenocarcinoma. Ann. Surg. 2019;269:520–529. doi: 10.1097/SLA.0000000000002557.
    1. Ethun C.G., Kooby D.A. The importance of surgical margins in pancreatic cancer. J. Surg. Oncol. 2016;113:283–288. doi: 10.1002/jso.24092.
    1. Tummers W.S., Groen J.V., Sibinga Mulder B.G., Farina-Sarasqueta A., Morreau J., Putter H., van de Velde C.J., Vahrmeijer A.L., Bonsing B.A., Mieog J.S., et al. Impact of resection margin status on recurrence and survival in pancreatic cancer surgery. Br. J. Surg. 2019;106:1055–1065. doi: 10.1002/bjs.11115.
    1. Ferrone C.R., Marchegiani G., Hong T.S., Ryan D.P., Deshpande V., McDonnell E.I., Sabbatino F., Santos D.D., Allen J.N., Blaszkowsky L.S., et al. Radiological and surgical implications of neoadjuvant treatment with FOLFIRINOX for locally advanced and borderline resectable pancreatic cancer. Ann. Surg. 2015;261:12–17. doi: 10.1097/SLA.0000000000000867.
    1. Allen V.B., Gurusamy K.S., Takwoingi Y., Kalia A., Davidson B.R. Diagnostic accuracy of laparoscopy following computed tomography (CT) scanning for assessing the resectability with curative intent in pancreatic and periampullary cancer. Cochrane Database Syst. Rev. 2016;2016:CD009323. doi: 10.1002/14651858.CD009323.pub3.
    1. de Geus S.W., Kasumova G.G., Sachs T.E., Ng S.C., Kent T.S., Moser A.J., Vahrmeijer A.L., Callery M.P., Tseng J.F. Neoadjuvant therapy affects margins and margins affect all: Perioperative and survival outcomes in resected pancreatic adenocarcinoma. HPB. 2018;20:573–581. doi: 10.1016/j.hpb.2017.12.004.
    1. Mieog J.S.D., Achterberg F.B., Zlitni A., Hutteman M., Burggraaf J., Swijnenburg R.J., Gioux S., Vahrmeijer A.L. Fundamentals and developments in fluorescence-guided cancer surgery. Nat. Rev. Clin. Oncol. 2021;19:9–22. doi: 10.1038/s41571-021-00548-3.
    1. Muynck L., Gaarenstroom K.N., Sier C.F.M., Duijvenvoorde M.V., Bosse T., Mieog J.S.D., Kroon C.D., Vahrmeijer A.L., Peters I.T.A. Novel Molecular Targets for Tumor-Specific Imaging of Epithelial Ovarian Cancer Metastases. Cancers. 2020;12:1562. doi: 10.3390/cancers12061562.
    1. Hoogstins C.E.S., Boogerd L.S.F., Sibinga Mulder B.G., Mieog J.S.D., Swijnenburg R.J., van de Velde C.J.H., Farina Sarasqueta A., Bonsing B.A., Framery B., Pèlegrin A., et al. Image-Guided Surgery in Patients with Pancreatic Cancer: First Results of a Clinical Trial Using SGM-101, a Novel Carcinoembryonic Antigen-Targeting, Near-Infrared Fluorescent Agent. Ann. Surg. Oncol. 2018;25:3350–3357. doi: 10.1245/s10434-018-6655-7.
    1. Tummers W.S., Miller S.E., Teraphongphom N.T., Gomez A., Steinberg I., Huland D.M., Hong S., Kothapalli S.-R., Hasan A., Ertsey R., et al. Intraoperative Pancreatic Cancer Detection using Tumor-Specific Multimodality Molecular Imaging. Ann. Surg. Oncol. 2018;25:1880–1888. doi: 10.1245/s10434-018-6453-2.
    1. Vuijk F.A., de Muynck L.D.A.N., Franken L.C., Busch O.R., Wilmink J.W., Besselink M.G., Bonsing B.A., Bhairosingh S.S., Kuppen P.J.K., Mieog J.S.D., et al. Molecular targets for diagnostic and intraoperative imaging of pancreatic ductal adenocarcinoma after neoadjuvant FOLFIRINOX treatment. Sci. Rep. 2020;10:16211. doi: 10.1038/s41598-020-73242-6.
    1. van Manen L., Handgraaf H.J., Diana M., Dijkstra J., Ishizawa T., Vahrmeijer A.L., Mieog J.S.D. A practical guide for the use of indocyanine green and methylene blue in fluorescence-guided abdominal surgery. J. Surg. Oncol. 2018;118:283–300. doi: 10.1002/jso.25105.
    1. Dip F., Boni L., Bouvet M., Carus T., Diana M., Falco J., Gurtner G.C., Ishizawa T., Kokudo N., Lo Menzo E., et al. Consensus Conference Statement on the General Use of Near-Infrared Fluorescence Imaging and Indocyanine Green Guided Surgery: Results of a Modified Delphi Study. Ann. Surg. 2020;275:685–691. doi: 10.1097/SLA.0000000000004412.
    1. Lwin T.M., Hoffman R.M., Bouvet M. The development of fluorescence guided surgery for pancreatic cancer: From bench to clinic. Expert Rev. Anticancer Ther. 2018;18:651–662. doi: 10.1080/14737140.2018.1477593.
    1. Hutteman M., van der Vorst J.R., Mieog J.S.D., Bonsing B.A., Hartgrink H.H., Kuppen P.J.K., Löwik C.W.G.M., Frangioni J.V., van de Velde C.J.H., Vahrmeijer A.L. Near-Infrared Fluorescence Imaging in Patients Undergoing Pancreaticoduodenectomy. Eur. Surg. Res. 2011;47:90–97. doi: 10.1159/000329411.
    1. Keeney S., Hasson F., McKenna H.P. The Delphi Technique in Nursing and Health Research. Wiley-Blackwell; Chichester, UK: 2011.
    1. Keller D.S., Ishizawa T., Cohen R., Chand M. Indocyanine green fluorescence imaging in colorectal surgery: Overview, applications, and future directions. Lancet Gastroenterol. Hepatol. 2017;2:757–766. doi: 10.1016/S2468-1253(17)30216-9.
    1. Majlesara A., Golriz M., Hafezi M., Saffari A., Stenau E., Maier-Hein L., Müller-Stich B.P., Mehrabi A. Indocyanine green fluorescence imaging in hepatobiliary surgery. Photodiagn. Photodyn. Ther. 2017;17:208–215. doi: 10.1016/j.pdpdt.2016.12.005.
    1. Morrell A.L.G., Morrell A.C., Morrell-Junior A.C., Mendes J.M., Tustumi F., Morrell A.G. Indocyanine green fluorescence imaging in robotic surgery: State of art, tips and tricks in current applications. Arq. Gastroenterol. 2021;58:61–70. doi: 10.1590/s0004-2803.202100000-11.
    1. Ishizawa T., Saiura A., Kokudo N. Clinical application of indocyanine green-fluorescence imaging during hepatectomy. Hepatobiliary Surg. Nutr. 2016;5:322. doi: 10.21037/hbsn.2015.10.01.
    1. Maeda H., Wu J., Sawa T., Matsumura Y., Hori K. Tumor vascular permeability and the EPR effect in macromolecular therapeutics: A review. J. Control Release. 2000;65:271–284. doi: 10.1016/S0168-3659(99)00248-5.
    1. Shi Y., van der Meel R., Chen X., Lammers T. The EPR effect and beyond: Strategies to improve tumor targeting and cancer nanomedicine treatment efficacy. Theranostics. 2020;10:7921–7924. doi: 10.7150/thno.49577.
    1. Kobayashi H., Choyke P.L., Ogawa M. Monoclonal antibody-based optical molecular imaging probes; considerations and caveats in chemistry, biology and pharmacology. Curr. Opin. Chem. Biol. 2016;33:32–38. doi: 10.1016/j.cbpa.2016.05.015.
    1. Hernot S., van Manen L., Debie P., Mieog J.S.D., Vahrmeijer A.L. Latest developments in molecular tracers for fluorescence image-guided cancer surgery. Lancet Oncol. 2019;20:e354–e367. doi: 10.1016/S1470-2045(19)30317-1.
    1. Holzapfel K., Reiser-Erkan C., Fingerle A.A., Erkan M., Eiber M.J., Rummeny E.J., Friess H., Kleeff J., Gaa J. Comparison of diffusion-weighted MR imaging and multidetector-row CT in the detection of liver metastases in patients operated for pancreatic cancer. Abdom. Imaging. 2011;36:179–184. doi: 10.1007/s00261-010-9633-5.
    1. Oba A., Inoue Y., Ono Y., Ishizuka N., Arakaki M., Sato T., Mise Y., Ito H., Saiura A., Takahashi Y. Staging laparoscopy for pancreatic cancer using intraoperative ultrasonography and fluorescence imaging: The SLING trial. Br. J. Surg. 2020;108:115–118. doi: 10.1093/bjs/znaa111.
    1. Groen J.V., Stommel M.W.J., Sarasqueta A.F., Besselink M.G., Brosens L.A.A., van Eijck C.H.J., Molenaar I.Q., Verheij J., de Vos-Geelen J., Wasser M.N., et al. Surgical management and pathological assessment of pancreatoduodenectomy with venous resection: An international survey among surgeons and pathologists. HPB. 2021;23:80–89. doi: 10.1016/j.hpb.2020.04.015.
    1. Verbeke C. Resection margins and R1 rates in pancreatic cancer–are we there yet? Histopathology. 2008;52:787–796. doi: 10.1111/j.1365-2559.2007.02935.x.
    1. Oronsky B., Ma P.C., Morgensztern D., Carter C.A. Nothing But NET: A Review of Neuroendocrine Tumors and Carcinomas. Neoplasia. 2017;19:991–1002. doi: 10.1016/j.neo.2017.09.002.
    1. Handgraaf H.J.M., Boogerd L.S.F., Shahbazi Feshtali S., Fariña Sarasqueta A., Snel M., Swijnenburg R.-J., Vahrmeijer A.L., Bonsing B.A., Mieog J.S.D. Intraoperative Near-Infrared Fluorescence Imaging of Multiple Pancreatic Neuroendocrine Tumors: A Case Report. Pancreas. 2018;47:130–133. doi: 10.1097/MPA.0000000000000951.
    1. Shirata C., Kawaguchi Y., Kobayashi K., Kobayashi Y., Arita J., Akamatsu N., Kaneko J., Sakamoto Y., Kokudo N., Hasegawa K. Usefulness of indocyanine green-fluorescence imaging for real-time visualization of pancreas neuroendocrine tumor and cystic neoplasm. J. Surg. Oncol. 2018;118:1012–1020. doi: 10.1002/jso.25231.
    1. Paiella S., De Pastena M., Landoni L., Esposito A., Casetti L., Miotto M., Ramera M., Salvia R., Secchettin E., Bonamini D., et al. Is there a role for near-infrared technology in laparoscopic resection of pancreatic neuroendocrine tumors? Results of the COLPAN “colour-and-resect the pancreas” study. Surg. Endosc. 2017;31:4478–4484. doi: 10.1007/s00464-017-5501-5.
    1. Tummers W.S., Warram J.M., van den Berg N.S., Miller S.E., Swijnenburg R.-J., Vahrmeijer A.L., Rosenthal E.L. Recommendations for reporting on emerging optical imaging agents to promote clinical approval. Theranostics. 2018;8:5336–5347. doi: 10.7150/thno.27384.
    1. Rosenthal E.L., Warram J.M., De Boer E., Basilion J.P., Biel M.A., Bogyo M., Bouvet M., Brigman B.E., Colson Y.L., DeMeester S.R. Successful translation of fluorescence navigation during oncologic surgery: A consensus report. J. Nucl. Med. 2016;57:144–150. doi: 10.2967/jnumed.115.158915.

Source: PubMed

Спонсоры и соавторы

Заболевания

Медикаментозные вмешательства

Подписаться