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Published in: Surgical Endoscopy 11/2017

01-11-2017

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

Authors: Salvatore Paiella, Matteo De Pastena, Luca Landoni, Alessandro Esposito, Luca Casetti, Marco Miotto, Marco Ramera, Roberto Salvia, Erica Secchettin, Deborah Bonamini, Gessica Manzini, Mirko D’Onofrio, Giovanni Marchegiani, Claudio Bassi

Published in: Surgical Endoscopy | Issue 11/2017

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Abstract

Background

The intraoperative identification of pancreatic neuroendocrine tumors (PanNETs) is of utmost importance to drive their laparoscopic resection. Near-infrared (NIR) surgery has emerged as a new technique for localizing tumors or neoplastic tissue. This study aimed to explore the results of the application of NIR in the laparoscopic resection of PanNETs.

Methods

Per protocol we enrolled ten subjects undergoing laparoscopic pancreatic surgery for PanNET from March 2016 to October 2016. During surgery, the patients were injected with indocyanine green dye (ICG, 25 mg given in 5 boli of 5 mg each). The switch-activation of NIR was performed to identify PanNETs. An ex-post analysis of the images was realized using ImageJ Software® to calculate the fluorescence signal.

Results

NIR imaging identified all ten PanNETs. Nine (90%) laparoscopic distal pancreatectomy with splenectomy and one (10%) laparoscopic enucleation were performed. The mean maximum tumor dimension was 2.4 cm (range 1–4 cm). Eight non-functioning PanNETs (80%) and two insulinomas (20%) were found at the final pathology. Nine out of ten (90%) PanNETs were detected after the second ICG bolus. The mean latency time was 80 s and the mean visibility time was 220 s. The peak of tumor visualization was reached 20 min after the last bolus. This finding was confirmed by the ex-post analysis of the fluorescence signal (mean signal-to-background ratio of 7.7, p = 0.001). NIR identified two additional lesions, which turned out to be normal lymph nodes at final pathology. A fluorescent signal was identified at the bed of the enucleation, and thus, a further exeresis was performed and final pathology revealed that is was residual neoplastic tissue.

Conclusions

This explorative study shows that NIR with ICG can have a role in laparoscopic pancreatic resection of PanNETs. Further studies are needed to assess the proper setting and role of this new and promising technology.
Literature
1.
go back to reference Kuo EJ, Salem RR (2013) Population-level analysis of pancreatic neuroendocrine tumors 2 cm or less in size. Ann Surg Oncol 20:2815–2821CrossRefPubMed Kuo EJ, Salem RR (2013) Population-level analysis of pancreatic neuroendocrine tumors 2 cm or less in size. Ann Surg Oncol 20:2815–2821CrossRefPubMed
2.
go back to reference Kim SC, Park KT, Hwang JW, Shin HC, Lee SS, Seo DW, Lee SK, Kim MH, Han DJ (2008) Comparative analysis of clinical outcomes for laparoscopic distal pancreatic resection and open distal pancreatic resection at a single institution. Surg Endosc 22:2261–2268CrossRefPubMed Kim SC, Park KT, Hwang JW, Shin HC, Lee SS, Seo DW, Lee SK, Kim MH, Han DJ (2008) Comparative analysis of clinical outcomes for laparoscopic distal pancreatic resection and open distal pancreatic resection at a single institution. Surg Endosc 22:2261–2268CrossRefPubMed
3.
go back to reference Cho CS, Kooby DA, Schmidt CM, Nakeeb A, Bentrem DJ, Merchant NB, Parikh AA, Martin RC 2nd, Scoggins CR, Ahmad SA, Kim HJ, Hamilton N, Hawkins WG, Weber SM (2011) Laparoscopic versus open left pancreatectomy: can preoperative factors indicate the safer technique? Ann Surg 253:975–980CrossRefPubMed Cho CS, Kooby DA, Schmidt CM, Nakeeb A, Bentrem DJ, Merchant NB, Parikh AA, Martin RC 2nd, Scoggins CR, Ahmad SA, Kim HJ, Hamilton N, Hawkins WG, Weber SM (2011) Laparoscopic versus open left pancreatectomy: can preoperative factors indicate the safer technique? Ann Surg 253:975–980CrossRefPubMed
4.
go back to reference Kulke MH, Anthony LB, Bushnell DL, de Herder WW, Goldsmith SJ, Klimstra DS, Marx SJ, Pasieka JL, Pommier RF, Yao JC, Jensen RT, North American Neuroendocrine Tumor S (2010) NANETS treatment guidelines: well-differentiated neuroendocrine tumors of the stomach and pancreas. Pancreas 39:735–752CrossRefPubMedPubMedCentral Kulke MH, Anthony LB, Bushnell DL, de Herder WW, Goldsmith SJ, Klimstra DS, Marx SJ, Pasieka JL, Pommier RF, Yao JC, Jensen RT, North American Neuroendocrine Tumor S (2010) NANETS treatment guidelines: well-differentiated neuroendocrine tumors of the stomach and pancreas. Pancreas 39:735–752CrossRefPubMedPubMedCentral
5.
go back to reference Mehrabi A, Fischer L, Hafezi M, Dirlewanger A, Grenacher L, Diener MK, Fonouni H, Golriz M, Garoussi C, Fard N, Rahbari NN, Werner J, Buchler MW (2014) A systematic review of localization, surgical treatment options, and outcome of insulinoma. Pancreas 43:675–686CrossRefPubMed Mehrabi A, Fischer L, Hafezi M, Dirlewanger A, Grenacher L, Diener MK, Fonouni H, Golriz M, Garoussi C, Fard N, Rahbari NN, Werner J, Buchler MW (2014) A systematic review of localization, surgical treatment options, and outcome of insulinoma. Pancreas 43:675–686CrossRefPubMed
6.
go back to reference Nikfarjam M, Warshaw AL, Axelrod L, Deshpande V, Thayer SP, Ferrone CR, Fernandez-del Castillo C (2008) Improved contemporary surgical management of insulinomas: a 25-year experience at the Massachusetts General Hospital. Ann Surg 247:165–172CrossRefPubMedPubMedCentral Nikfarjam M, Warshaw AL, Axelrod L, Deshpande V, Thayer SP, Ferrone CR, Fernandez-del Castillo C (2008) Improved contemporary surgical management of insulinomas: a 25-year experience at the Massachusetts General Hospital. Ann Surg 247:165–172CrossRefPubMedPubMedCentral
7.
go back to reference Berends FJ, Cuesta MA, Kazemier G, van Eijck CH, de Herder WW, van Muiswinkel JM, Bruining HA, Bonjer HJ (2000) Laparoscopic detection and resection of insulinomas. Surgery 128:386–391CrossRefPubMed Berends FJ, Cuesta MA, Kazemier G, van Eijck CH, de Herder WW, van Muiswinkel JM, Bruining HA, Bonjer HJ (2000) Laparoscopic detection and resection of insulinomas. Surgery 128:386–391CrossRefPubMed
8.
go back to reference Grover AC, Skarulis M, Alexander HR, Pingpank JF, Javor ED, Chang R, Shawker T, Gorden P, Cochran C, Libutti SK (2005) A prospective evaluation of laparoscopic exploration with intraoperative ultrasound as a technique for localizing sporadic insulinomas. Surgery 138:1003–1008 (discussion 1008)CrossRefPubMed Grover AC, Skarulis M, Alexander HR, Pingpank JF, Javor ED, Chang R, Shawker T, Gorden P, Cochran C, Libutti SK (2005) A prospective evaluation of laparoscopic exploration with intraoperative ultrasound as a technique for localizing sporadic insulinomas. Surgery 138:1003–1008 (discussion 1008)CrossRefPubMed
9.
go back to reference de Herder WW, Niederle B, Scoazec JY, Pauwels S, Kloppel G, Falconi M, Kwekkeboom DJ, Oberg K, Eriksson B, Wiedenmann B, Rindi G, O’Toole D, Ferone D, Frascati Consensus C, European Neuroendocrine Tumor S (2006) Well-differentiated pancreatic tumor/carcinoma: insulinoma. Neuroendocrinology 84:183–188CrossRefPubMed de Herder WW, Niederle B, Scoazec JY, Pauwels S, Kloppel G, Falconi M, Kwekkeboom DJ, Oberg K, Eriksson B, Wiedenmann B, Rindi G, O’Toole D, Ferone D, Frascati Consensus C, European Neuroendocrine Tumor S (2006) Well-differentiated pancreatic tumor/carcinoma: insulinoma. Neuroendocrinology 84:183–188CrossRefPubMed
10.
go back to reference Vahrmeijer AL, Hutteman M, van der Vorst JR, van de Velde CJ, Frangioni JV (2013) Image-guided cancer surgery using near-infrared fluorescence. Nat Rev Clin Oncol 10:507–518CrossRefPubMedPubMedCentral Vahrmeijer AL, Hutteman M, van der Vorst JR, van de Velde CJ, Frangioni JV (2013) Image-guided cancer surgery using near-infrared fluorescence. Nat Rev Clin Oncol 10:507–518CrossRefPubMedPubMedCentral
11.
go back to reference Boni L, David G, Mangano A, Dionigi G, Rausei S, Spampatti S, Cassinotti E, Fingerhut A (2015) Clinical applications of indocyanine green (ICG) enhanced fluorescence in laparoscopic surgery. Surg Endosc 29:2046–2055CrossRefPubMed Boni L, David G, Mangano A, Dionigi G, Rausei S, Spampatti S, Cassinotti E, Fingerhut A (2015) Clinical applications of indocyanine green (ICG) enhanced fluorescence in laparoscopic surgery. Surg Endosc 29:2046–2055CrossRefPubMed
12.
go back to reference Yokoyama N, Otani T, Hashidate H, Maeda C, Katada T, Sudo N, Manabe S, Ikeno Y, Toyoda A, Katayanagi N (2012) Real-time detection of hepatic micrometastases from pancreatic cancer by intraoperative fluorescence imaging: preliminary results of a prospective study. Cancer 118:2813–2819CrossRefPubMed Yokoyama N, Otani T, Hashidate H, Maeda C, Katada T, Sudo N, Manabe S, Ikeno Y, Toyoda A, Katayanagi N (2012) Real-time detection of hepatic micrometastases from pancreatic cancer by intraoperative fluorescence imaging: preliminary results of a prospective study. Cancer 118:2813–2819CrossRefPubMed
13.
go back to reference von Burstin J, Eser S, Seidler B, Meining A, Bajbouj M, Mages J, Lang R, Kind AJ, Schnieke AE, Schmid RM, Schneider G, Saur D (2008) Highly sensitive detection of early-stage pancreatic cancer by multimodal near-infrared molecular imaging in living mice. Int J Cancer 123:2138–2147CrossRef von Burstin J, Eser S, Seidler B, Meining A, Bajbouj M, Mages J, Lang R, Kind AJ, Schnieke AE, Schmid RM, Schneider G, Saur D (2008) Highly sensitive detection of early-stage pancreatic cancer by multimodal near-infrared molecular imaging in living mice. Int J Cancer 123:2138–2147CrossRef
14.
go back to reference Tran Cao HS, Kaushal S, Lee C, Snyder CS, Thompson KJ, Horgan S, Talamini MA, Hoffman RM, Bouvet M (2011) Fluorescence laparoscopy imaging of pancreatic tumor progression in an orthotopic mouse model. Surg Endosc 25:48–54CrossRefPubMed Tran Cao HS, Kaushal S, Lee C, Snyder CS, Thompson KJ, Horgan S, Talamini MA, Hoffman RM, Bouvet M (2011) Fluorescence laparoscopy imaging of pancreatic tumor progression in an orthotopic mouse model. Surg Endosc 25:48–54CrossRefPubMed
15.
go back to reference Hutteman M, van der Vorst JR, Mieog JS, Bonsing BA, Hartgrink HH, Kuppen PJ, Lowik CW, Frangioni JV, van de Velde CJ, Vahrmeijer AL (2011) Near-infrared fluorescence imaging in patients undergoing pancreaticoduodenectomy. Eur Surg Res 47:90–97CrossRefPubMedPubMedCentral Hutteman M, van der Vorst JR, Mieog JS, Bonsing BA, Hartgrink HH, Kuppen PJ, Lowik CW, Frangioni JV, van de Velde CJ, Vahrmeijer AL (2011) Near-infrared fluorescence imaging in patients undergoing pancreaticoduodenectomy. Eur Surg Res 47:90–97CrossRefPubMedPubMedCentral
17.
go back to reference Bassi C, Dervenis C, Butturini G, Fingerhut A, Yeo C, Izbicki J, Neoptolemos J, Sarr M, Traverso W, Buchler M, International Study Group on Pancreatic Fistula D (2005) Postoperative pancreatic fistula: an international study group (ISGPF) definition. Surgery 138:8–13CrossRefPubMed Bassi C, Dervenis C, Butturini G, Fingerhut A, Yeo C, Izbicki J, Neoptolemos J, Sarr M, Traverso W, Buchler M, International Study Group on Pancreatic Fistula D (2005) Postoperative pancreatic fistula: an international study group (ISGPF) definition. Surgery 138:8–13CrossRefPubMed
18.
go back to reference Tamburrino D, Partelli S, Renzi C, Crippa S, Muffati F, Perali C, Parisi A, Randolph J, Fusai GK, Cirocchi R, Falconi M (2016) Systematic review and meta-analysis on laparoscopic pancreatic resections for neuroendocrine neoplasms (PNENs). Expert Rev Gastroenterol Hepatol 11(1):65–73CrossRefPubMed Tamburrino D, Partelli S, Renzi C, Crippa S, Muffati F, Perali C, Parisi A, Randolph J, Fusai GK, Cirocchi R, Falconi M (2016) Systematic review and meta-analysis on laparoscopic pancreatic resections for neuroendocrine neoplasms (PNENs). Expert Rev Gastroenterol Hepatol 11(1):65–73CrossRefPubMed
19.
go back to reference Graziani R, Brandalise A, Bellotti M, Manfredi R, Contro A, Falconi M, Boninsegna L, Pozzi Mucelli R (2010) Imaging of neuroendocrine gastroenteropancreatic tumours. Radiol Med 115:1047–1064CrossRefPubMed Graziani R, Brandalise A, Bellotti M, Manfredi R, Contro A, Falconi M, Boninsegna L, Pozzi Mucelli R (2010) Imaging of neuroendocrine gastroenteropancreatic tumours. Radiol Med 115:1047–1064CrossRefPubMed
20.
go back to reference Halfdanarson TR, Rubin J, Farnell MB, Grant CS, Petersen GM (2008) Pancreatic endocrine neoplasms: epidemiology and prognosis of pancreatic endocrine tumors. Endocr Relat Cancer 15:409–427CrossRefPubMedPubMedCentral Halfdanarson TR, Rubin J, Farnell MB, Grant CS, Petersen GM (2008) Pancreatic endocrine neoplasms: epidemiology and prognosis of pancreatic endocrine tumors. Endocr Relat Cancer 15:409–427CrossRefPubMedPubMedCentral
21.
go back to reference van der Vorst JR, Vahrmeijer AL, Hutteman M, Bosse T, Smit VT, van de Velde CJ, Frangioni JV, Bonsing BA (2012) Near-infrared fluorescence imaging of a solitary fibrous tumor of the pancreas using methylene blue. World J Gastrointest Surg 4:180–184CrossRefPubMedPubMedCentral van der Vorst JR, Vahrmeijer AL, Hutteman M, Bosse T, Smit VT, van de Velde CJ, Frangioni JV, Bonsing BA (2012) Near-infrared fluorescence imaging of a solitary fibrous tumor of the pancreas using methylene blue. World J Gastrointest Surg 4:180–184CrossRefPubMedPubMedCentral
22.
go back to reference Tummers QR, Boonstra MC, Frangioni JV, van de Velde CJ, Vahrmeijer AL, Bonsing BA (2015) Intraoperative near-infrared fluorescence imaging of a paraganglioma using methylene blue: a case report. Int J Surg Case Rep 6C:150–153CrossRefPubMed Tummers QR, Boonstra MC, Frangioni JV, van de Velde CJ, Vahrmeijer AL, Bonsing BA (2015) Intraoperative near-infrared fluorescence imaging of a paraganglioma using methylene blue: a case report. Int J Surg Case Rep 6C:150–153CrossRefPubMed
23.
go back to reference Charlson M, Szatrowski TP, Peterson J, Gold J (1994) Validation of a combined comorbidity index. J Clin Epidemiol 47:1245–1251CrossRefPubMed Charlson M, Szatrowski TP, Peterson J, Gold J (1994) Validation of a combined comorbidity index. J Clin Epidemiol 47:1245–1251CrossRefPubMed
Metadata
Title
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
Authors
Salvatore Paiella
Matteo De Pastena
Luca Landoni
Alessandro Esposito
Luca Casetti
Marco Miotto
Marco Ramera
Roberto Salvia
Erica Secchettin
Deborah Bonamini
Gessica Manzini
Mirko D’Onofrio
Giovanni Marchegiani
Claudio Bassi
Publication date
01-11-2017
Publisher
Springer US
Published in
Surgical Endoscopy / Issue 11/2017
Print ISSN: 0930-2794
Electronic ISSN: 1432-2218
DOI
https://doi.org/10.1007/s00464-017-5501-5

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