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Published in: Surgical Endoscopy 3/2020

01-03-2020 | Adrenalectomy | 2019 EAES Oral

Fluorescence-enabled assessment of adrenal gland localization and perfusion in posterior retroperitoneoscopic adrenal surgery in a preclinical model

Authors: Barbara Seeliger, Martin K. Walz, Pier F. Alesina, Vincent Agnus, Raoul Pop, Manuel Barberio, Alend Saadi, Marc Worreth, Jacques Marescaux, Michele Diana

Published in: Surgical Endoscopy | Issue 3/2020

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Abstract

Background

The posterior retroperitoneoscopic adrenal access represents a challenge in orientation and working space creation. The aim of this experimental acute study was to evaluate the impact of computer-assisted quantitative fluorescence imaging on adrenal gland identification and assessment of intraoperative remnant perfusion for adrenal resection in the posterior retroperitoneoscopic approach.

Methods

Six pigs underwent simultaneous (n = 5) or sequential (n = 1) bilateral posterior retroperitoneoscopic adrenalectomy (n = 12). Fluorescence imaging was obtained via intravenous administration of 3 mL of Indocyanine Green (ICG) and by switching the camera systems to near-infrared mode (D-LIGHT P, KARL STORZ; Germany). Fluorescence-based visualization of adrenal glands before vascular division (n = 4), after the main vascular pedicle ligation (negative control, n = 1) or after adrenal resection (n = 7), was followed by completion adrenalectomy. The fluorescence signal intensity dynamics were recorded and analyzed using proprietary software. For each pixel, the slope of fluorescence signal intensity evolution over time was translated into a color-coded perfusion cartography, which was superimposed onto real-time images obtained with the corresponding left and right camera systems. Quantitative fluorescence signal analysis in the regions of interest (ROIs) served to assess adrenal remnant perfusion in divided adrenal glands.

Results

In the retroperitoneum, the vascular anatomy was illuminated in fluorescence imaging first. The adrenal glands were promptly highlighted after primary intravenous ICG administration (n = 9) or showed a fluorescence signal intensity increase upon reinjection (n = 3). Quantitative fluorescence analysis showed a statistically significant difference between perfused and ischemic segments in divided glands (p = 0.0156).

Conclusions

Fluorescence imaging provides real-time guidance during minimally invasive adrenal surgery. Prior to dissection, it allows to easily discriminate the adrenal gland from surrounding retroperitoneal structures. After adrenal gland division, ICG injection associated with a computer-assisted quantitative analysis helps to distinguish between well-perfused and ischemic segments. Further studies are underway to establish the correlation between remnant perfusion and viability.
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Literature
1.
go back to reference Weissleder R, Pittet MJ (2008) Imaging in the era of molecular oncology. Nature 452:580–589CrossRef Weissleder R, Pittet MJ (2008) Imaging in the era of molecular oncology. Nature 452:580–589CrossRef
3.
go back to reference Baiocchi GL, Diana M, Boni L (2018) Indocyanine green-based fluorescence imaging in visceral and hepatobiliary and pancreatic surgery: state of the art and future directions. World J Gastroenterol 24:2921–2930CrossRef Baiocchi GL, Diana M, Boni L (2018) Indocyanine green-based fluorescence imaging in visceral and hepatobiliary and pancreatic surgery: state of the art and future directions. World J Gastroenterol 24:2921–2930CrossRef
4.
go back to reference Vrielink OM, Wevers KP, Kist JW, Borel Rinkes IHM, Hemmer PHJ, Vriens MR, de Vries J, Kruijff S (2017) Laparoscopic anterior versus endoscopic posterior approach for adrenalectomy: a shift to a new golden standard? Langenbecks Arch Surg 402:767–773CrossRef Vrielink OM, Wevers KP, Kist JW, Borel Rinkes IHM, Hemmer PHJ, Vriens MR, de Vries J, Kruijff S (2017) Laparoscopic anterior versus endoscopic posterior approach for adrenalectomy: a shift to a new golden standard? Langenbecks Arch Surg 402:767–773CrossRef
5.
go back to reference Gaujoux S, Mihai R, Joint working group of ESES and ENSAT (2017) European Society of Endocrine Surgeons (ESES) and European Network for the Study of Adrenal Tumours (ENSAT) recommendations for the surgical management of adrenocortical carcinoma. Br J Surg 104:358–376CrossRef Gaujoux S, Mihai R, Joint working group of ESES and ENSAT (2017) European Society of Endocrine Surgeons (ESES) and European Network for the Study of Adrenal Tumours (ENSAT) recommendations for the surgical management of adrenocortical carcinoma. Br J Surg 104:358–376CrossRef
6.
go back to reference Walz MK (1998) Minimally invasive adrenalectomy–comparison of surgical approaches. Langenbecks Arch Chir Suppl Kongressbd 115:113–115PubMed Walz MK (1998) Minimally invasive adrenalectomy–comparison of surgical approaches. Langenbecks Arch Chir Suppl Kongressbd 115:113–115PubMed
7.
go back to reference Brunt LM (2013) SAGES guidelines for minimally invasive treatment of adrenal pathology. Surg Endosc 27:3957–3959CrossRef Brunt LM (2013) SAGES guidelines for minimally invasive treatment of adrenal pathology. Surg Endosc 27:3957–3959CrossRef
8.
go back to reference Arezzo A, Bullano A, Cochetti G, Cirocchi R, Randolph J, Mearini E, Evangelista A, Ciccone G, Bonjer HJ, Morino M (2018) Transperitoneal versus retroperitoneal laparoscopic adrenalectomy for adrenal tumours in adults. Cochrane Database Syst Rev 12:CD011668PubMed Arezzo A, Bullano A, Cochetti G, Cirocchi R, Randolph J, Mearini E, Evangelista A, Ciccone G, Bonjer HJ, Morino M (2018) Transperitoneal versus retroperitoneal laparoscopic adrenalectomy for adrenal tumours in adults. Cochrane Database Syst Rev 12:CD011668PubMed
9.
go back to reference Vrielink OM, Engelsman AF, Hemmer PHJ, de Vries J, Vorselaars W, Vriens MR, Karakatsanis A, Hellman P, Sywak MS, van Leeuwen BL, El Moumni M, Kruijff S (2018) Multicentre study evaluating the surgical learning curve for posterior retroperitoneoscopic adrenalectomy. Br J Surg 105:544–551CrossRef Vrielink OM, Engelsman AF, Hemmer PHJ, de Vries J, Vorselaars W, Vriens MR, Karakatsanis A, Hellman P, Sywak MS, van Leeuwen BL, El Moumni M, Kruijff S (2018) Multicentre study evaluating the surgical learning curve for posterior retroperitoneoscopic adrenalectomy. Br J Surg 105:544–551CrossRef
10.
go back to reference Stefanidis D, Goldfarb M, Kercher KW, Hope WW, Richardson W, Fanelli RD, Society of Gastrointestinal and Endoscopic Surgeons (2013) SAGES guidelines for minimally invasive treatment of adrenal pathology. Surg Endosc 27:3960–3980CrossRef Stefanidis D, Goldfarb M, Kercher KW, Hope WW, Richardson W, Fanelli RD, Society of Gastrointestinal and Endoscopic Surgeons (2013) SAGES guidelines for minimally invasive treatment of adrenal pathology. Surg Endosc 27:3960–3980CrossRef
11.
go back to reference Perrier ND, Kennamer DL, Bao R, Jimenez C, Grubbs EG, Lee JE, Evans DB (2008) Posterior retroperitoneoscopic adrenalectomy: preferred technique for removal of benign tumors and isolated metastases. Ann Surg 248:666–674PubMed Perrier ND, Kennamer DL, Bao R, Jimenez C, Grubbs EG, Lee JE, Evans DB (2008) Posterior retroperitoneoscopic adrenalectomy: preferred technique for removal of benign tumors and isolated metastases. Ann Surg 248:666–674PubMed
12.
go back to reference DeLong JC, Chakedis JM, Hosseini A, Kelly KJ, Horgan S, Bouvet M (2015) Indocyanine green (ICG) fluorescence-guided laparoscopic adrenalectomy. J Surg Oncol 112:650–653CrossRef DeLong JC, Chakedis JM, Hosseini A, Kelly KJ, Horgan S, Bouvet M (2015) Indocyanine green (ICG) fluorescence-guided laparoscopic adrenalectomy. J Surg Oncol 112:650–653CrossRef
13.
go back to reference Rieder JM, Nisbet AA, Wuerstle MC, Tran VQ, Kwon EO, Chien GW (2010) Differences in left and right laparoscopic adrenalectomy. JSLS 14:369–373CrossRef Rieder JM, Nisbet AA, Wuerstle MC, Tran VQ, Kwon EO, Chien GW (2010) Differences in left and right laparoscopic adrenalectomy. JSLS 14:369–373CrossRef
14.
go back to reference Colvin J, Zaidi N, Berber E (2016) The utility of indocyanine green fluorescence imaging during robotic adrenalectomy. J Surg Oncol 114:153–156CrossRef Colvin J, Zaidi N, Berber E (2016) The utility of indocyanine green fluorescence imaging during robotic adrenalectomy. J Surg Oncol 114:153–156CrossRef
15.
go back to reference Kahramangil B, Berber E (2017) The use of near-infrared fluorescence imaging in endocrine surgical procedures. J Surg Oncol 115:848–855CrossRef Kahramangil B, Berber E (2017) The use of near-infrared fluorescence imaging in endocrine surgical procedures. J Surg Oncol 115:848–855CrossRef
16.
go back to reference Pathak RA, Hemal AK (2019) Intraoperative ICG-fluorescence imaging for robotic-assisted urologic surgery: current status and review of literature. Int Urol Nephrol 51:765–771CrossRef Pathak RA, Hemal AK (2019) Intraoperative ICG-fluorescence imaging for robotic-assisted urologic surgery: current status and review of literature. Int Urol Nephrol 51:765–771CrossRef
17.
go back to reference Diana M, Noll E, Agnus V, Liu YY, Kong SH, Legner A, Diemunsch P, Marescaux J (2017) Reply to letter: “enhanced reality fluorescence videography to assess bowel perfusion: the cybernetic eye”. Ann Surg 265:e49–e52CrossRef Diana M, Noll E, Agnus V, Liu YY, Kong SH, Legner A, Diemunsch P, Marescaux J (2017) Reply to letter: “enhanced reality fluorescence videography to assess bowel perfusion: the cybernetic eye”. Ann Surg 265:e49–e52CrossRef
18.
go back to reference Diana M, Noll E, Diemunsch P, Dallemagne B, Benahmed MA, Agnus V, Soler L, Barry B, Namer IJ, Demartines N, Charles AL, Geny B, Marescaux J (2014) Enhanced-reality video fluorescence: a real-time assessment of intestinal viability. Ann Surg 259:700–707CrossRef Diana M, Noll E, Diemunsch P, Dallemagne B, Benahmed MA, Agnus V, Soler L, Barry B, Namer IJ, Demartines N, Charles AL, Geny B, Marescaux J (2014) Enhanced-reality video fluorescence: a real-time assessment of intestinal viability. Ann Surg 259:700–707CrossRef
19.
go back to reference Kilkenny C, Browne W, Cuthill IC, Emerson M, Altman DG, Group NCRRGW (2010) Animal research: reporting in vivo experiments: the ARRIVE guidelines. J Gene Med 12:561–563CrossRef Kilkenny C, Browne W, Cuthill IC, Emerson M, Altman DG, Group NCRRGW (2010) Animal research: reporting in vivo experiments: the ARRIVE guidelines. J Gene Med 12:561–563CrossRef
20.
go back to reference Walz MK, Peitgen K, Diesing D, Petersenn S, Janssen OE, Philipp T, Metz KA, Mann K, Schmid KW, Neumann HP (2004) Partial versus total adrenalectomy by the posterior retroperitoneoscopic approach: early and long-term results of 325 consecutive procedures in primary adrenal neoplasias. World J Surg 28:1323–1329CrossRef Walz MK, Peitgen K, Diesing D, Petersenn S, Janssen OE, Philipp T, Metz KA, Mann K, Schmid KW, Neumann HP (2004) Partial versus total adrenalectomy by the posterior retroperitoneoscopic approach: early and long-term results of 325 consecutive procedures in primary adrenal neoplasias. World J Surg 28:1323–1329CrossRef
21.
go back to reference Walz MK, Alesina PF, Wenger FA, Deligiannis A, Szuczik E, Petersenn S, Ommer A, Groeben H, Peitgen K, Janssen OE, Philipp T, Neumann HP, Schmid KW, Mann K (2006) Posterior retroperitoneoscopic adrenalectomy–results of 560 procedures in 520 patients. Surgery 140:943–948 (Discussion 948–950) CrossRef Walz MK, Alesina PF, Wenger FA, Deligiannis A, Szuczik E, Petersenn S, Ommer A, Groeben H, Peitgen K, Janssen OE, Philipp T, Neumann HP, Schmid KW, Mann K (2006) Posterior retroperitoneoscopic adrenalectomy–results of 560 procedures in 520 patients. Surgery 140:943–948 (Discussion 948–950) CrossRef
23.
go back to reference Dip FD, Roy M, Perrins S, Ganga RR, Lo Menzo E, Szomstein S, Rosenthal R (2015) Technical description and feasibility of laparoscopic adrenal contouring using fluorescence imaging. Surg Endosc 29:569–574CrossRef Dip FD, Roy M, Perrins S, Ganga RR, Lo Menzo E, Szomstein S, Rosenthal R (2015) Technical description and feasibility of laparoscopic adrenal contouring using fluorescence imaging. Surg Endosc 29:569–574CrossRef
24.
go back to reference Dondelinger RF, Ghysels MP, Brisbois D, Donkers E, Snaps FR, Saunders J, Deviere J (1998) Relevant radiological anatomy of the pig as a training model in interventional radiology. Eur Radiol 8:1254–1273CrossRef Dondelinger RF, Ghysels MP, Brisbois D, Donkers E, Snaps FR, Saunders J, Deviere J (1998) Relevant radiological anatomy of the pig as a training model in interventional radiology. Eur Radiol 8:1254–1273CrossRef
25.
go back to reference Suzuki K, Nagai H, Hoshino T, Tamate H (1985) The branching site of the posterior adrenal artery in pigs. Okajimas Folia Anat Jpn 62:27–33CrossRef Suzuki K, Nagai H, Hoshino T, Tamate H (1985) The branching site of the posterior adrenal artery in pigs. Okajimas Folia Anat Jpn 62:27–33CrossRef
26.
go back to reference Walz MK, Alesina PF (2009) Single access retroperitoneoscopic adrenalectomy (SARA)–one step beyond in endocrine surgery. Langenbecks Arch Surg 394:447–450CrossRef Walz MK, Alesina PF (2009) Single access retroperitoneoscopic adrenalectomy (SARA)–one step beyond in endocrine surgery. Langenbecks Arch Surg 394:447–450CrossRef
27.
go back to reference Lowery AJ, Seeliger B, Alesina PF, Walz MK (2017) Posterior retroperitoneoscopic adrenal surgery for clinical and subclinical cushing’s syndrome in patients with bilateral adrenal disease. Langenbecks Arch Surg 402:775–785CrossRef Lowery AJ, Seeliger B, Alesina PF, Walz MK (2017) Posterior retroperitoneoscopic adrenal surgery for clinical and subclinical cushing’s syndrome in patients with bilateral adrenal disease. Langenbecks Arch Surg 402:775–785CrossRef
28.
go back to reference Alesina PF, Hinrichs J, Meier B, Schmid KW, Neumann HP, Walz MK (2012) Minimally invasive cortical-sparing surgery for bilateral pheochromocytomas. Langenbecks Arch Surg 397:233–238CrossRef Alesina PF, Hinrichs J, Meier B, Schmid KW, Neumann HP, Walz MK (2012) Minimally invasive cortical-sparing surgery for bilateral pheochromocytomas. Langenbecks Arch Surg 397:233–238CrossRef
29.
go back to reference Brunt LM, Molmenti EP, Kerbl K, Soper NJ, Stone AM, Clayman RV (1993) Retroperitoneal endoscopic adrenalectomy: an experimental study. Surg Laparosc Endosc 3:300–306PubMed Brunt LM, Molmenti EP, Kerbl K, Soper NJ, Stone AM, Clayman RV (1993) Retroperitoneal endoscopic adrenalectomy: an experimental study. Surg Laparosc Endosc 3:300–306PubMed
30.
go back to reference Hoenig DM, Magee RR, Chrostek CA, Amaral JF, Stein BS (1995) Direct retroperitoneoscopic adrenalectomy in the porcine model. J Laparoendosc Surg 5:385–388CrossRef Hoenig DM, Magee RR, Chrostek CA, Amaral JF, Stein BS (1995) Direct retroperitoneoscopic adrenalectomy in the porcine model. J Laparoendosc Surg 5:385–388CrossRef
31.
go back to reference Park A, Gagner M (1995) A porcine model for laparoscopic adrenalectomy. Surg Endosc 9:807–810CrossRef Park A, Gagner M (1995) A porcine model for laparoscopic adrenalectomy. Surg Endosc 9:807–810CrossRef
32.
go back to reference Ludwig AT, Wagner KR, Lowry PS, Papaconstantinou HT, Lairmore TC (2010) Robot-assisted posterior retroperitoneoscopic adrenalectomy. J Endourol 24:1307–1314CrossRef Ludwig AT, Wagner KR, Lowry PS, Papaconstantinou HT, Lairmore TC (2010) Robot-assisted posterior retroperitoneoscopic adrenalectomy. J Endourol 24:1307–1314CrossRef
33.
go back to reference Arora E, Bhandarwar A, Wagh A, Gandhi S, Patel C, Gupta S, Talwar G, Agarwal J, Rathore J, Chatnalkar S (2018) Role of indo-cyanine green (ICG) fluorescence in laparoscopic adrenalectomy: a retrospective review of 55 Cases. Surg Endosc 32:4649–4657CrossRef Arora E, Bhandarwar A, Wagh A, Gandhi S, Patel C, Gupta S, Talwar G, Agarwal J, Rathore J, Chatnalkar S (2018) Role of indo-cyanine green (ICG) fluorescence in laparoscopic adrenalectomy: a retrospective review of 55 Cases. Surg Endosc 32:4649–4657CrossRef
34.
go back to reference Kahramangil B, Kose E, Berber E (2018) Characterization of fluorescence patterns exhibited by different adrenal tumors: determining the indications for indocyanine green use in adrenalectomy. Surgery 164:972–977CrossRef Kahramangil B, Kose E, Berber E (2018) Characterization of fluorescence patterns exhibited by different adrenal tumors: determining the indications for indocyanine green use in adrenalectomy. Surgery 164:972–977CrossRef
35.
go back to reference Sound S, Okoh AK, Bucak E, Yigitbas H, Dural C, Berber E (2016) Intraoperative tumor localization and tissue distinction during robotic adrenalectomy using indocyanine green fluorescence imaging: a feasibility study. Surg Endosc 30:657–662CrossRef Sound S, Okoh AK, Bucak E, Yigitbas H, Dural C, Berber E (2016) Intraoperative tumor localization and tissue distinction during robotic adrenalectomy using indocyanine green fluorescence imaging: a feasibility study. Surg Endosc 30:657–662CrossRef
36.
go back to reference Manny TB, Pompeo AS, Hemal AK (2013) Robotic partial adrenalectomy using indocyanine green dye with near-infrared imaging: the initial clinical experience. Urology 82:738–742CrossRef Manny TB, Pompeo AS, Hemal AK (2013) Robotic partial adrenalectomy using indocyanine green dye with near-infrared imaging: the initial clinical experience. Urology 82:738–742CrossRef
37.
go back to reference Dobbie JW, Symington T (1966) The human adrenal gland with special reference to the vasculature. J Endocrinol 34:479–489CrossRef Dobbie JW, Symington T (1966) The human adrenal gland with special reference to the vasculature. J Endocrinol 34:479–489CrossRef
38.
go back to reference Walz MK (2004) Extent of adrenalectomy for adrenal neoplasm: cortical sparing (subtotal) versus total adrenalectomy. Surg Clin North Am 84:743–753CrossRef Walz MK (2004) Extent of adrenalectomy for adrenal neoplasm: cortical sparing (subtotal) versus total adrenalectomy. Surg Clin North Am 84:743–753CrossRef
39.
go back to reference Ishizawa T, Saiura A (2019) Fluorescence Imaging for Minimally Invasive Cancer Surgery. Surg Oncol Clin N Am 28:45–60CrossRef Ishizawa T, Saiura A (2019) Fluorescence Imaging for Minimally Invasive Cancer Surgery. Surg Oncol Clin N Am 28:45–60CrossRef
40.
go back to reference Quero G, Lapergola A, Barberio M, Seeliger B, Gockel I, Saccomandi P, Guerriero L, Mutter D, Saadi A, Worreth M, Marescaux J, Agnus V, Diana M (2019) Discrimination between arterial and venous bowel ischemia by computer-assisted analysis of the fluorescent signal. Surg Endosc 33:1988–1997CrossRef Quero G, Lapergola A, Barberio M, Seeliger B, Gockel I, Saccomandi P, Guerriero L, Mutter D, Saadi A, Worreth M, Marescaux J, Agnus V, Diana M (2019) Discrimination between arterial and venous bowel ischemia by computer-assisted analysis of the fluorescent signal. Surg Endosc 33:1988–1997CrossRef
Metadata
Title
Fluorescence-enabled assessment of adrenal gland localization and perfusion in posterior retroperitoneoscopic adrenal surgery in a preclinical model
Authors
Barbara Seeliger
Martin K. Walz
Pier F. Alesina
Vincent Agnus
Raoul Pop
Manuel Barberio
Alend Saadi
Marc Worreth
Jacques Marescaux
Michele Diana
Publication date
01-03-2020
Publisher
Springer US
Published in
Surgical Endoscopy / Issue 3/2020
Print ISSN: 0930-2794
Electronic ISSN: 1432-2218
DOI
https://doi.org/10.1007/s00464-019-06997-3

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