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Published in: Surgical Endoscopy 3/2019

Open Access 01-03-2019 | New Technology

Near-infrared fluorescence laparoscopy of the ureter with three preclinical dyes in a pig model

Authors: Jacqueline van den Bos, Mahdi Al-Taher, Nicole D. Bouvy, Laurents P. S. Stassen

Published in: Surgical Endoscopy | Issue 3/2019

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Abstract

Background

Ureteric injury is reported to occur in 1–7.6% of colorectal surgeries. To reduce the incidence of ureteral injury, it is essential to identify the ureters. The use of near-infrared fluorescence (NIRF) imaging with intravenously administered dyes might be of added value for ureteral visualization during laparoscopy. The aim of this study is to assess the performance of three preclinical dyes; IRDye® 800BK, IRDye® 800NOS and IRDye® 800CW, for near-infrared fluorescence laparoscopy of the ureter in pigs.

Methods

In three female Dutch landrace pigs, the new dyes were evaluated. In each pig, 1 dye was tested using a 6-mg intravenous dose in a concentration of 1 mg/ml. Imaging was performed in fluorescence mode and white light mode with a laparoscopic imaging system. In order to further evaluate the dyes, an ex vivo imaging experiment was performed, in which 8 decreasing concentrations per dye, diluted in PBS, were evaluated in a transparent test tube with NIRF mode at a distance of 1, 5 and 10 cm from the laparoscope.

Results

All three dyes were effective in allowing the identification of the ureter with NIRF imaging. The ureter became fluorescent after 35, 45 and 10 min, respectively, for IRDye® 800BK, IRDye® 800NOS and IRDye® 800CW with a maximum target-to-background ratio (TBR) of 2.14, 0.66 and 1.44, respectively. In the ex vivo imaging experiment, all three dyes produced a strong fluorescence signal at all concentrations and all distances evaluated.

Conclusions

Intravenous administration of the preclinical dyes IRDye® 800CW, IRDye® 800 BK and IRDye® 800NOS facilitated successful identification of the anatomical course of the ureter in living pig models. The highest measured TBR occurred with the use of IRDye® 800BK. Ex vivo, a correlation was observed between the fluorescence intensities of the signal with the concentration of the dye and with the distance to the object.
Literature
1.
go back to reference Andersen P, Andersen LM, Iversen LH (2015) Iatrogenic ureteral injury in colorectal cancer surgery: a nationwide study comparing laparoscopic and open approaches. Surg Endosc 29(6):1406–1412CrossRef Andersen P, Andersen LM, Iversen LH (2015) Iatrogenic ureteral injury in colorectal cancer surgery: a nationwide study comparing laparoscopic and open approaches. Surg Endosc 29(6):1406–1412CrossRef
2.
go back to reference Marcelissen TA, Den Hollander PP, Tuytten TR, Sosef MN (2016) Incidence of iatrogenic ureteral injury during open and laparoscopic colorectal surgery: a single center experience and review of the literature. Surg Laparosc Endosc Percutan Tech 26(6):513–515 Marcelissen TA, Den Hollander PP, Tuytten TR, Sosef MN (2016) Incidence of iatrogenic ureteral injury during open and laparoscopic colorectal surgery: a single center experience and review of the literature. Surg Laparosc Endosc Percutan Tech 26(6):513–515
3.
go back to reference Zafar SN, Ahaghotu CA, Libuit L, Ortega G, Coleman PW, Cornwell III EE, et al (2014) Ureteral injury after laparoscopic versus open colectomy. JSLS 18(3) Zafar SN, Ahaghotu CA, Libuit L, Ortega G, Coleman PW, Cornwell III EE, et al (2014) Ureteral injury after laparoscopic versus open colectomy. JSLS 18(3)
4.
go back to reference da Silva G, Boutros M, Wexner SD (2012) Role of prophylactic ureteric stents in colorectal surgery. Asian J Endosc Surg 5(3):105–110CrossRefPubMed da Silva G, Boutros M, Wexner SD (2012) Role of prophylactic ureteric stents in colorectal surgery. Asian J Endosc Surg 5(3):105–110CrossRefPubMed
5.
go back to reference Abboudi H, Ahmed K, Royle J, Khan MS, Dasgupta P, N’Dow J (2013) Ureteric injury: a challenging condition to diagnose and manage. Nat Rev Urol 10(2):108–115CrossRefPubMed Abboudi H, Ahmed K, Royle J, Khan MS, Dasgupta P, N’Dow J (2013) Ureteric injury: a challenging condition to diagnose and manage. Nat Rev Urol 10(2):108–115CrossRefPubMed
6.
go back to reference Esparaz AM, Pearl JA, Herts BR, LeBlanc J, Kapoor B (2015) Iatrogenic urinary tract injuries: etiology, diagnosis, and management. Semin Intervent Radiol 32(2):195–208CrossRefPubMedPubMedCentral Esparaz AM, Pearl JA, Herts BR, LeBlanc J, Kapoor B (2015) Iatrogenic urinary tract injuries: etiology, diagnosis, and management. Semin Intervent Radiol 32(2):195–208CrossRefPubMedPubMedCentral
7.
go back to reference Zhang X, Wang Z, Zhou H, Liang J, Zhou Z (2014) Analysis of ureteral injuries for laparoscopic rectal cancer surgery. J Laparoendosc Adv Surg Tech A 24(10):698–701CrossRefPubMed Zhang X, Wang Z, Zhou H, Liang J, Zhou Z (2014) Analysis of ureteral injuries for laparoscopic rectal cancer surgery. J Laparoendosc Adv Surg Tech A 24(10):698–701CrossRefPubMed
8.
go back to reference Osayi SN, Wendling MR, Drosdeck JM, Chaudhry UI, Perry KA, Noria SF et al (2015) Near-infrared fluorescent cholangiography facilitates identification of biliary anatomy during laparoscopic cholecystectomy. Surg Endosc 29(2):368–375CrossRef Osayi SN, Wendling MR, Drosdeck JM, Chaudhry UI, Perry KA, Noria SF et al (2015) Near-infrared fluorescent cholangiography facilitates identification of biliary anatomy during laparoscopic cholecystectomy. Surg Endosc 29(2):368–375CrossRef
9.
go back to reference Narasaki H, Noji T, Wada H, Ebihara Y, Tsuchikawa T, Okamura K et al (2017) Intraoperative real-time assessment of liver function with near-infrared fluorescence imaging. Eur Surg Res 58(5–6):235–245CrossRefPubMed Narasaki H, Noji T, Wada H, Ebihara Y, Tsuchikawa T, Okamura K et al (2017) Intraoperative real-time assessment of liver function with near-infrared fluorescence imaging. Eur Surg Res 58(5–6):235–245CrossRefPubMed
10.
go back to reference Boni L, Fingerhut A, Marzorati A, Rausei S, Dionigi G, Cassinotti E (2017) Indocyanine green fluorescence angiography during laparoscopic low anterior resection: results of a case-matched study. Surg Endosc 31(4):1836–1840CrossRef Boni L, Fingerhut A, Marzorati A, Rausei S, Dionigi G, Cassinotti E (2017) Indocyanine green fluorescence angiography during laparoscopic low anterior resection: results of a case-matched study. Surg Endosc 31(4):1836–1840CrossRef
11.
go back to reference Jafari MD, Lee KH, Halabi WJ, Mills SD, Carmichael JC, Stamos MJ et al (2013) The use of indocyanine green fluorescence to assess anastomotic perfusion during robotic assisted laparoscopic rectal surgery. Surg Endosc 27(8):3003–3008CrossRef Jafari MD, Lee KH, Halabi WJ, Mills SD, Carmichael JC, Stamos MJ et al (2013) The use of indocyanine green fluorescence to assess anastomotic perfusion during robotic assisted laparoscopic rectal surgery. Surg Endosc 27(8):3003–3008CrossRef
12.
go back to reference Kin C, Vo H, Welton L, Welton M (2015) Equivocal effect of intraoperative fluorescence angiography on colorectal anastomotic leaks. Dis Colon Rectum 58(6):582–587CrossRefPubMed Kin C, Vo H, Welton L, Welton M (2015) Equivocal effect of intraoperative fluorescence angiography on colorectal anastomotic leaks. Dis Colon Rectum 58(6):582–587CrossRefPubMed
13.
go back to reference Kudszus S, Roesel C, Schachtrupp A, Hoer JJ (2010) Intraoperative laser fluorescence angiography in colorectal surgery: a noninvasive analysis to reduce the rate of anastomotic leakage. Langenbecks Arch Surg 395(8):1025–1030CrossRef Kudszus S, Roesel C, Schachtrupp A, Hoer JJ (2010) Intraoperative laser fluorescence angiography in colorectal surgery: a noninvasive analysis to reduce the rate of anastomotic leakage. Langenbecks Arch Surg 395(8):1025–1030CrossRef
14.
go back to reference Wada T, Kawada K, Takahashi R, Yoshitomi M, Hida K, Hasegawa S et al (2017) ICG fluorescence imaging for quantitative evaluation of colonic perfusion in laparoscopic colorectal surgery. Surg Endosc 31(10):4184–4193CrossRef Wada T, Kawada K, Takahashi R, Yoshitomi M, Hida K, Hasegawa S et al (2017) ICG fluorescence imaging for quantitative evaluation of colonic perfusion in laparoscopic colorectal surgery. Surg Endosc 31(10):4184–4193CrossRef
15.
go back to reference Jafari MD, Wexner SD, Martz JE, McLemore EC, Margolin DA, Sherwinter DA et al (2015) Perfusion assessment in laparoscopic left-sided/anterior resection (PILLAR II): a multi-institutional study. J Am Coll Surg 220(1):82–92 e1CrossRefPubMed Jafari MD, Wexner SD, Martz JE, McLemore EC, Margolin DA, Sherwinter DA et al (2015) Perfusion assessment in laparoscopic left-sided/anterior resection (PILLAR II): a multi-institutional study. J Am Coll Surg 220(1):82–92 e1CrossRefPubMed
16.
go back to reference Levesque E, Martin E, Dudau D, Lim C, Dhonneur G, Azoulay D (2016) Current use and perspective of indocyanine green clearance in liver diseases. Anaesth Crit Care Pain Med 35(1):49–57CrossRefPubMed Levesque E, Martin E, Dudau D, Lim C, Dhonneur G, Azoulay D (2016) Current use and perspective of indocyanine green clearance in liver diseases. Anaesth Crit Care Pain Med 35(1):49–57CrossRefPubMed
17.
go back to reference Lee Z, Simhan J, Parker DC, Reilly C, Llukani E, Lee DI et al (2013) Novel use of indocyanine green for intraoperative, real-time localization of ureteral stenosis during robot-assisted ureteroureterostomy. Urology 82(3):729–733CrossRef Lee Z, Simhan J, Parker DC, Reilly C, Llukani E, Lee DI et al (2013) Novel use of indocyanine green for intraoperative, real-time localization of ureteral stenosis during robot-assisted ureteroureterostomy. Urology 82(3):729–733CrossRef
18.
go back to reference Siddighi S, Yune JJ, Hardesty J (2014) Indocyanine green for intraoperative localization of ureter. Am J Obstet Gynecol 211(4):436 e1–e2CrossRef Siddighi S, Yune JJ, Hardesty J (2014) Indocyanine green for intraoperative localization of ureter. Am J Obstet Gynecol 211(4):436 e1–e2CrossRef
19.
go back to reference Schols RM, Lodewick TM, Bouvy ND, van Dam GM, Dejong CH, Stassen LP (2014) Application of a new dye for near-infrared fluorescence laparoscopy of the ureters: demonstration in a pig model. Dis Colon Rectum 57(3):407–411CrossRefPubMed Schols RM, Lodewick TM, Bouvy ND, van Dam GM, Dejong CH, Stassen LP (2014) Application of a new dye for near-infrared fluorescence laparoscopy of the ureters: demonstration in a pig model. Dis Colon Rectum 57(3):407–411CrossRefPubMed
20.
go back to reference van den Bos J, Al-Taher M, Hsien SG, Bouvy ND, Stassen LPS (2017) Near-infrared fluorescence laparoscopy of the cystic duct and cystic artery: first experience with two new preclinical dyes in a pig model. Surg Endosc 31(10):4309–4314CrossRefPubMedPubMedCentral van den Bos J, Al-Taher M, Hsien SG, Bouvy ND, Stassen LPS (2017) Near-infrared fluorescence laparoscopy of the cystic duct and cystic artery: first experience with two new preclinical dyes in a pig model. Surg Endosc 31(10):4309–4314CrossRefPubMedPubMedCentral
21.
go back to reference Leung K IRDye 800CW-Human serum albumin. Molecular imaging and contrast agent database (MICAD). Bethesda (MD)2004 Leung K IRDye 800CW-Human serum albumin. Molecular imaging and contrast agent database (MICAD). Bethesda (MD)2004
22.
go back to reference Schols RM, Bouvy ND, van Dam RM, Masclee AA, Dejong CH, Stassen LP (2013) Combined vascular and biliary fluorescence imaging in laparoscopic cholecystectomy. Surg Endosc 27(12):4511–4517CrossRefPubMed Schols RM, Bouvy ND, van Dam RM, Masclee AA, Dejong CH, Stassen LP (2013) Combined vascular and biliary fluorescence imaging in laparoscopic cholecystectomy. Surg Endosc 27(12):4511–4517CrossRefPubMed
23.
go back to reference Lee Z, Moore B, Giusto L, Eun DD (2015) Use of indocyanine green during robot-assisted ureteral reconstructions. Eur Urol 67(2):291–298CrossRef Lee Z, Moore B, Giusto L, Eun DD (2015) Use of indocyanine green during robot-assisted ureteral reconstructions. Eur Urol 67(2):291–298CrossRef
24.
go back to reference Verbeek FP, van der Vorst JR, Schaafsma BE, Swijnenburg RJ, Gaarenstroom KN, Elzevier HW et al (2013) Intraoperative near infrared fluorescence guided identification of the ureters using low dose methylene blue: a first in human experience. J Urol 190(2):574–579CrossRefPubMedPubMedCentral Verbeek FP, van der Vorst JR, Schaafsma BE, Swijnenburg RJ, Gaarenstroom KN, Elzevier HW et al (2013) Intraoperative near infrared fluorescence guided identification of the ureters using low dose methylene blue: a first in human experience. J Urol 190(2):574–579CrossRefPubMedPubMedCentral
25.
go back to reference Barnes TG, Hompes R, Birks J, Mortensen NJ, Jones O, Lindsey I et al (2018) Methylene blue fluorescence of the ureter during colorectal surgery. Surg Endosc 32(9):4036–4043CrossRefPubMedPubMedCentral Barnes TG, Hompes R, Birks J, Mortensen NJ, Jones O, Lindsey I et al (2018) Methylene blue fluorescence of the ureter during colorectal surgery. Surg Endosc 32(9):4036–4043CrossRefPubMedPubMedCentral
26.
go back to reference Al-Taher M, van den Bos J, Schols RM, Bouvy ND, Stassen LP (2016) Fluorescence ureteral visualization in human laparoscopic colorectal surgery using methylene blue. J Laparoendosc Adv Surg Tech A 26(11):870–875CrossRefPubMed Al-Taher M, van den Bos J, Schols RM, Bouvy ND, Stassen LP (2016) Fluorescence ureteral visualization in human laparoscopic colorectal surgery using methylene blue. J Laparoendosc Adv Surg Tech A 26(11):870–875CrossRefPubMed
28.
go back to reference Kono Y, Ishizawa T, Tani K, Harada N, Kaneko J, Saiura A et al (2015) Techniques of fluorescence cholangiography during laparoscopic cholecystectomy for better delineation of the bile duct anatomy. Medicine (Baltimore) 94(25):e1005CrossRef Kono Y, Ishizawa T, Tani K, Harada N, Kaneko J, Saiura A et al (2015) Techniques of fluorescence cholangiography during laparoscopic cholecystectomy for better delineation of the bile duct anatomy. Medicine (Baltimore) 94(25):e1005CrossRef
29.
go back to reference Baek HY, Lee HJ, Kim JM, Cho SY, Jeong S, Yoo KY (2015) Effects of intravenously administered indocyanine green on near-infrared cerebral oximetry and pulse oximetry readings. Korean J Anesthesiol 68(2):122–127CrossRefPubMedPubMedCentral Baek HY, Lee HJ, Kim JM, Cho SY, Jeong S, Yoo KY (2015) Effects of intravenously administered indocyanine green on near-infrared cerebral oximetry and pulse oximetry readings. Korean J Anesthesiol 68(2):122–127CrossRefPubMedPubMedCentral
30.
go back to reference Ediriwickrema LS, Francis JH, Arslan-Carlon V, Dalecki PH, Brodie SE, Marr BP et al (2015) Intravenous injection of indocyanine green results in an artificial transient desaturation by pulse oximetry. Retin Cases Brief Rep 9(3):252–255CrossRefPubMed Ediriwickrema LS, Francis JH, Arslan-Carlon V, Dalecki PH, Brodie SE, Marr BP et al (2015) Intravenous injection of indocyanine green results in an artificial transient desaturation by pulse oximetry. Retin Cases Brief Rep 9(3):252–255CrossRefPubMed
Metadata
Title
Near-infrared fluorescence laparoscopy of the ureter with three preclinical dyes in a pig model
Authors
Jacqueline van den Bos
Mahdi Al-Taher
Nicole D. Bouvy
Laurents P. S. Stassen
Publication date
01-03-2019
Publisher
Springer US
Published in
Surgical Endoscopy / Issue 3/2019
Print ISSN: 0930-2794
Electronic ISSN: 1432-2218
DOI
https://doi.org/10.1007/s00464-018-6596-z

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