ICG-augmented hyperspectral imaging for visualization of intestinal perfusion compared to conventional ICG fluorescence imaging: an experimental study.
Journal
International journal of surgery (London, England)
ISSN: 1743-9159
Titre abrégé: Int J Surg
Pays: United States
ID NLM: 101228232
Informations de publication
Date de publication:
01 Dec 2023
01 Dec 2023
Historique:
received:
12
05
2023
accepted:
13
08
2023
medline:
23
1
2024
pubmed:
23
1
2024
entrez:
23
1
2024
Statut:
epublish
Résumé
Small bowel malperfusion (SBM) can cause high morbidity and severe surgical consequences. However, there is no standardized objective measuring tool for the quantification of SBM. Indocyanine green (ICG) imaging can be used for visualization, but lacks standardization and objectivity. Hyperspectral imaging (HSI) as a newly emerging technology in medicine might present advantages over conventional ICG fluorescence or in combination with it. HSI baseline data from physiological small bowel, avascular small bowel and small bowel after intravenous application of ICG was recorded in a total number of 54 in-vivo pig models. Visualizations of avascular small bowel after mesotomy were compared between HSI only (1), ICG-augmented HSI (IA-HSI) (2), clinical evaluation through the eyes of the surgeon (3) and conventional ICG imaging (4). The primary research focus was the localization of resection borders as suggested by each of the four methods. Distances between these borders were measured and histological samples were obtained from the regions in between in order to quantify necrotic changes 6 h after mesotomy for every region. StO2 images (1) were capable of visualizing areas of physiological perfusion and areas of clearly impaired perfusion. However, exact borders where physiological perfusion started to decrease could not be clearly identified. Instead, IA-HSI (2) suggested a sharp-resection line where StO2 values started to decrease. Clinical evaluation (3) suggested a resection line 23 mm (±7 mm) and conventional ICG imaging (4) even suggested a resection line 53 mm (±13 mm) closer towards the malperfused region. Histopathological evaluation of the region that was sufficiently perfused only according to conventional ICG (R3) already revealed a significant increase in pre-necrotic changes in 27% (±9%) of surface area. Therefore, conventional ICG seems less sensitive than IA-HSI with regards to detection of insufficient tissue perfusion. In this experimental animal study, IA-HSI (2) was superior for the visualization of segmental SBM compared to conventional HSI imaging (1), clinical evaluation (3) or conventional ICG imaging (4) regarding histopathological safety. ICG application caused visual artifacts in the StO2 values of the HSI camera as values significantly increase. This is caused by optical properties of systemic ICG and does not resemble a true increase in oxygenation levels. However, this empirical finding can be used to visualize segmental SBM utilizing ICG as contrast agent in an approach for IA-HSI. Clinical applicability and relevance will have to be explored in clinical trials. Not applicable. Translational animal science. Original article.
Sections du résumé
BACKGROUND
BACKGROUND
Small bowel malperfusion (SBM) can cause high morbidity and severe surgical consequences. However, there is no standardized objective measuring tool for the quantification of SBM. Indocyanine green (ICG) imaging can be used for visualization, but lacks standardization and objectivity. Hyperspectral imaging (HSI) as a newly emerging technology in medicine might present advantages over conventional ICG fluorescence or in combination with it.
METHODS
METHODS
HSI baseline data from physiological small bowel, avascular small bowel and small bowel after intravenous application of ICG was recorded in a total number of 54 in-vivo pig models. Visualizations of avascular small bowel after mesotomy were compared between HSI only (1), ICG-augmented HSI (IA-HSI) (2), clinical evaluation through the eyes of the surgeon (3) and conventional ICG imaging (4). The primary research focus was the localization of resection borders as suggested by each of the four methods. Distances between these borders were measured and histological samples were obtained from the regions in between in order to quantify necrotic changes 6 h after mesotomy for every region.
RESULTS
RESULTS
StO2 images (1) were capable of visualizing areas of physiological perfusion and areas of clearly impaired perfusion. However, exact borders where physiological perfusion started to decrease could not be clearly identified. Instead, IA-HSI (2) suggested a sharp-resection line where StO2 values started to decrease. Clinical evaluation (3) suggested a resection line 23 mm (±7 mm) and conventional ICG imaging (4) even suggested a resection line 53 mm (±13 mm) closer towards the malperfused region. Histopathological evaluation of the region that was sufficiently perfused only according to conventional ICG (R3) already revealed a significant increase in pre-necrotic changes in 27% (±9%) of surface area. Therefore, conventional ICG seems less sensitive than IA-HSI with regards to detection of insufficient tissue perfusion.
CONCLUSIONS
CONCLUSIONS
In this experimental animal study, IA-HSI (2) was superior for the visualization of segmental SBM compared to conventional HSI imaging (1), clinical evaluation (3) or conventional ICG imaging (4) regarding histopathological safety. ICG application caused visual artifacts in the StO2 values of the HSI camera as values significantly increase. This is caused by optical properties of systemic ICG and does not resemble a true increase in oxygenation levels. However, this empirical finding can be used to visualize segmental SBM utilizing ICG as contrast agent in an approach for IA-HSI. Clinical applicability and relevance will have to be explored in clinical trials.
LEVEL OF EVIDENCE
METHODS
Not applicable. Translational animal science. Original article.
Identifiants
pubmed: 38258996
doi: 10.1097/JS9.0000000000000706
pii: 01279778-202312000-00018
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
3883-3895Informations de copyright
Copyright © 2023 The Author(s). Published by Wolters Kluwer Health, Inc.
Références
Bala M, Kashuk J, Moore EE, et al. Acute mesenteric ischemia: guidelines of the World Society of Emergency Surgery. World J Emerg Surg 2017;12:38.
Gilshtein H, Ghuman A, Dawoud M, et al. Indications for, and outcomes of, end ileostomy revision procedures. Colorec Dis 2020;24:1352–1357.
Srisajjakul S, Prapaisilp P, Bangchokdee S. Comprehensive review of acute small bowel ischemia: CT imaging findings, pearls, and pitfalls. Emerg Radiol 2022;29:531–544.
Amini A, Nagalli S. Bowel Ischemia. StatPearls. StatPearls Publishing. Copyright © 2022. StatPearls Publishing LLC.; 2022.
Nwaiwu CA, Buharin VE, Mach A, et al. Feasibility and comparison of laparoscopic laser speckle contrast imaging to near-infrared display of indocyanine green in intraoperative tissue blood flow/tissue perfusion in preclinical porcine models. Surg Endosc 2022;37:1086–1095.
Heeman W, Wildeboer ACL, Al-Taher M, et al. Experimental evaluation of laparoscopic laser speckle contrast imaging to visualize perfusion deficits during intestinal surgery. Surg Endosc 2022;37:950–957.
Furusawa K, Yoshimitsu M, Matsukawa H, et al. Precise diagnosis of acute mesenteric ischemia using indocyanine green imaging prevents small bowel resection: a case report. Int J Surg Case Rep 2022;97:107463.
Аlexander K, Ismail M, Alexander M, et al. Use of ICG imaging to confirm bowel viability after upper mesenteric stenting in patient with acute mesenteric ischemia: case report. Int J Surg Case Rep 2019;61:322–326.
Guerra F, Coletta D, Greco PA, et al. The use of indocyanine green fluorescence to define bowel microcirculation during laparoscopic surgery for acute small bowel obstruction. Colorec Dis 2021;23:2189–2194.
Duprée A, Rieß H, von Kroge PH, et al. Intraoperative quality assessment of tissue perfusion with indocyanine green (ICG) in a porcine model of mesenteric ischemia. PLoS One 2021;16:e0254144.
Karampinis I, Keese M, Jakob J, et al. Indocyanine green tissue angiography can reduce extended bowel resections in acute mesenteric ischemia. J Gastrointest Surg 2018;22:2117–2124.
Nakagawa Y, Kobayashi K, Kuwabara S, et al. Use of indocyanine green fluorescence imaging to determine the area of bowel resection in non-occlusive mesenteric ischemia: a case report. Int J Surg Case Rep 2018;51:352–357.
Szoka N, Kahn M. Acute-on-chronic mesenteric ischemia: the use of fluorescence guidance to diagnose a nonsurvivable injury. Case Rep Surg 2022;2022:5459774.
Gosvig K, Jensen SS, Qvist N, et al. Remote computer-assisted analysis of ICG fluorescence signal for evaluation of small intestinal anastomotic perfusion: a blinded, randomized, experimental trial. Surg Endosc 2020;34:2095–2102.
Irie T, Matsutani T, Hagiwara N, et al. Successful treatment of non-occlusive mesenteric ischemia with indocyanine green fluorescence and open-abdomen management. Clin J Gastroenterol 2017;10:514–518.
Nakamoto H, Yokota R, Namba H, et al. Effectiveness of intraoperative indocyanine green fluorescence-navigated surgery for superior mesenteric vein thrombosis that developed during treatment for intravascular lymphoma: a case report. Am J Case Rep 2021;22:e929549.
Chu W, Chennamsetty A, Toroussian R, et al. Anaphylactic shock after intravenous administration of indocyanine green during robotic partial nephrectomy. Urol Case Rep 2017;12:37–38.
Papadia A, Gasparri ML, Mueller M. Are allergic reactions to indocyanine green really that uncommon? A single institution experience. Obstetr Gynecol Rep 2017;1:1–2.
Reinhart MB, Huntington CR, Blair LJ, et al. Indocyanine green: historical context, current applications, and future considerations. Surg Innov 2016;23:166–175.
Giraudeau C, Moussaron A, Stallivieri A, et al. Indocyanine green: photosensitizer or chromophore? Still a debate. Curr Med Chem 2014;21:1871–1897.
Gosvig K, Jensen SS, Qvist N, et al. Quantification of ICG fluorescence for the evaluation of intestinal perfusion: comparison between two software-based algorithms for quantification. Surg Endosc 2021;35:5043–5050.
Diana M, Noll E, Diemunsch P, et al. Enhanced-reality video fluorescence: a real-time assessment of intestinal viability. Ann Surg 2014;259:700–707.
Nickel F*, Studier-Fischer* A, Özdemir B, et al. Optimization of anastomotic technique and gastric conduit perfusion with hyperspectral imaging in an experimental model for minimally invasive esophagectomy. Eur J Surg Oncol 2023;18:S0748–7983(23)00444-4.
Seidlitz S, Sellner J, Odenthal J, et al. Robust deep learning-based semantic organ segmentation in hyperspectral images. Med Image Anal 2022;80:102488.
Studier-Fischer A, Seidlitz S, Sellner J, et al. Spectral organ fingerprints for machine learning-based intraoperative tissue classification with hyperspectral imaging in a porcine model. Sci Rep 2022;12:11028.
Holmer A, Tetschke F, Marotz J, et al. Oxygenation and perfusion monitoring with a hyperspectral camera system for chemical based tissue analysis of skin and organs. Physiol Measure 2016;37:2064–2078.
Kulcke A, Holmer A, Wahl P, et al. A compact hyperspectral camera for measurement of perfusion parameters in medicine. Biomed Tech (Berl) 2018;63:519–527.
Marotz J, Kulcke A, Siemers F, et al. Extended perfusion parameter estimation from hyperspectral imaging data for bedside diagnostic in medicine. Molecules 2019;24:4164.
Tetschke F, Markgraf W, Gransow M, et al. Hyperspectral imaging for monitoring oxygen saturation levels during normothermic kidney perfusion. J Sens. Sens Syst 2016;5:313–318.
Kilkenny C, Browne W, Cuthill IC, et al. Animal research: reporting in vivo experiments: the ARRIVE guidelines. Br J Pharmacol 2010;160:1577–1579.
Holmer A, Marotz J, Wahl P, et al. Hyperspectral imaging in perfusion and wound diagnostics - methods and algorithms for the determination of tissue parameters. Biomed Tech (Berl) 2018;63:547–556.
Ballardini B, Santoro L, Sangalli C, et al. The indocyanine green method is equivalent to the 99mTc-labeled radiotracer method for identifying the sentinel node in breast cancer: a concordance and validation study. Eur J Surg Oncol (EJSO) 2013;39:1332–1336.
Gioux S, Choi HS, Frangioni JV. Image-guided surgery using invisible near-infrared light: fundamentals of clinical translation. Mol Imaging 2010;9:7290.2010.00034.
Luo S, Zhang E, Su Y, et al. A review of NIR dyes in cancer targeting and imaging. Biomaterials 2011;32:7127–7138.
Muraleedharan S, Tripathy K. Indocyanine Green (ICG) Angiography. StatPearls. StatPearls Publishing. Copyright © 2022, StatPearls Publishing LLC; 2022.
Lim SH, Tan HTA, Shelat VG. Comparison of indocyanine green dye fluorescent cholangiography with intra-operative cholangiography in laparoscopic cholecystectomy: a meta-analysis. Surg Endosc 2021;35:1511–1520.
Iwamoto M, Ueda K, Kawamura J. A narrative review of the usefulness of indocyanine green fluorescence angiography for perfusion assessment in colorectal surgery. Cancers 2022;14:5623.
Quero G, Lapergola A, Barberio M, et al. Discrimination between arterial and venous bowel ischemia by computer-assisted analysis of the fluorescent signal. Surg Endosc 2018;33:1988–1997.
Soares AS, Bano S, Clancy NT, et al. Multisensor perfusion assessment cohort study: preliminary evidence toward a standardized assessment of indocyanine green fluorescence in colorectal surgery. Surgery 2022;172:69–73.
Ryu S, Hara K, Goto K, et al. Fluorescence angiography versus direct palpation for bowel viability evaluation with strangulated bowel obstruction. Langenbecks Arch Surg 2022;407:797–803.
Jansen-Winkeln B, Germann I, Köhler H, et al. Comparison of hyperspectral imaging and fluorescence angiography for the determination of the transection margin in colorectal resections-a comparative study. Int J Colorec Dis 2021;36:283–291.
Barberio M, Felli E, Seyller E, et al. Quantitative fluorescence angiography versus hyperspectral imaging to assess bowel ischemia: a comparative study in enhanced reality. Surgery 2020;168:178–184.
Barberio M, Longo F, Fiorillo C, et al. HYPerspectral Enhanced Reality (HYPER): a physiology-based surgical guidance tool. Surg Endosc 2020;34:1736–1744.
Meessen S, Rother J, Zheng X, et al. Establishment of real-time multispectral imaging for the detection of bladder cancer using a preclinical in vivo model. Bladder Cancer 2020;6:285–294.
Hardy NP, Dalli J, Khan MF, et al. Inter-user variation in the interpretation of near infrared perfusion imaging using indocyanine green in colorectal surgery. Surg Endosc 2021;35:7074–7081.
Soares AS, Clancy NT, Bano S, et al. Interobserver variability in the assessment of fluorescence angiography in the colon. Surg Innov 2023;0:15533506221132681.