Hyperspectral evaluation of hepatic oxygenation in a model of total vs. arterial liver ischaemia.


Journal

Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288

Informations de publication

Date de publication:
22 09 2020
Historique:
received: 30 07 2020
accepted: 08 09 2020
entrez: 23 9 2020
pubmed: 24 9 2020
medline: 16 12 2020
Statut: epublish

Résumé

Liver ischaemia reperfusion injury (IRI) is a dreaded pathophysiological complication which may lead to an impaired liver function. The level of oxygen hypoperfusion affects the level of cellular damage during the reperfusion phase. Consequently, intraoperative localisation and quantification of oxygen impairment would help in the early detection of liver ischaemia. To date, there is no real-time, non-invasive, and intraoperative tool which can compute an organ oxygenation map, quantify and discriminate different types of vascular occlusions intraoperatively. Hyperspectral imaging (HSI) is a non-invasive optical methodology which can quantify tissue oxygenation and which has recently been applied to the medical field. A hyperspectral camera detects the relative reflectance of a tissue in the range of 500 to 1000 nm, allowing the quantification of organic compounds such as oxygenated and deoxygenated haemoglobin at different depths. Here, we show the first comparative study of liver oxygenation by means of HSI quantification in a model of total vascular inflow occlusion (VIO) vs. hepatic artery occlusion (HAO), correlating optical properties with capillary lactate and histopathological evaluation. We found that liver HSI could discriminate between VIO and HAO. These results were confirmed via cross-validation of HSI which detected and quantified intestinal congestion in VIO. A significant correlation between the near-infrared spectra and capillary lactate was found (r = - 0.8645, p = 0.0003 VIO, r = - 0.7113, p = 0.0120 HAO). Finally, a statistically significant negative correlation was found between the histology score and the near-infrared parameter index (NIR) (r = - 0.88, p = 0.004). We infer that HSI, by predicting capillary lactates and the histopathological score, would be a suitable non-invasive tool for intraoperative liver perfusion assessment.

Identifiants

pubmed: 32963333
doi: 10.1038/s41598-020-72915-6
pii: 10.1038/s41598-020-72915-6
pmc: PMC7509803
doi:

Substances chimiques

Oxygen S88TT14065

Types de publication

Evaluation Study Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

15441

Références

Itri, J. N., Heller, M. T. & Tublin, M. E. Hepatic transplantation: Postoperative complications. Abdom. Imaging 38, 1300–1333. https://doi.org/10.1007/s00261-013-0002-z (2013).
doi: 10.1007/s00261-013-0002-z pubmed: 23644931
Ciobanu, A. O. & Gherasim, L. Ischemic hepatitis - Intercorrelated pathology. Maedica (Buchar) 13, 5–11 (2018).
doi: 10.26574/maedica.2018.13.1.5
Quiroga, S. et al. Complications of orthotopic liver transplantation: Spectrum of findings with helical CT. Radiographics 21, 1085–1102. https://doi.org/10.1148/radiographics.21.5.g01se061085 (2001).
doi: 10.1148/radiographics.21.5.g01se061085 pubmed: 11553818
Rethy, A., Lango, T. & Marvik, R. Laparoscopic ultrasound for hepatocellular carcinoma and colorectal liver metastasis: An overview. Surg. Laparosc. Endosc. Percutan. Tech. 23, 135–144. https://doi.org/10.1097/SLE.0b013e31828a0b9a (2013).
doi: 10.1097/SLE.0b013e31828a0b9a pubmed: 23579506
de Moura Almeida, A. et al. Fatty liver disease in severe obese patients: diagnostic value of abdominal ultrasound. World J. Gastroenterol. 14, 1415–1418, https://doi.org/10.3748/wjg.14.1415 (2008).
Lu, G. & Fei, B. Medical hyperspectral imaging: A review. J. Biomed. Opt. 19, 10901. https://doi.org/10.1117/1.JBO.19.1.010901 (2014).
doi: 10.1117/1.JBO.19.1.010901 pubmed: 24441941
Jansen-Winkeln, B. et al. Determination of the transection margin during colorectal resection with hyperspectral imaging (HSI). Int. J. Colorectal Dis. 34, 731–739. https://doi.org/10.1007/s00384-019-03250-0 (2019).
doi: 10.1007/s00384-019-03250-0 pubmed: 30712079
Li, Q. et al. Review of spectral imaging technology in biomedical engineering: Achievements and challenges. J. Biomed. Opt. 18, 100901. https://doi.org/10.1117/1.JBO.18.10.100901 (2013).
doi: 10.1117/1.JBO.18.10.100901 pubmed: 24114019
Wang, Q. et al. A hyperspectral vessel image registration method for blood oxygenation mapping. PLoS ONE 12, e0178499. https://doi.org/10.1371/journal.pone.0178499 (2017).
doi: 10.1371/journal.pone.0178499 pubmed: 28570589 pmcid: 5453521
Holmer, A., Marotz, J., Wahl, P., Dau, M. & Kammerer, P. W. Hyperspectral imaging in perfusion and wound diagnostics - Methods and algorithms for the determination of tissue parameters. Biomed. Tech. (Berl) 63, 547–556. https://doi.org/10.1515/bmt-2017-0155 (2018).
doi: 10.1515/bmt-2017-0155
Ortega, S., Halicek, M., Fabelo, H., Callico, G. M. & Fei, B. Hyperspectral and multispectral imaging in digital and computational pathology: A systematic review [Invited]. Biomed. Opt. Express 11, 3195–3233. https://doi.org/10.1364/BOE.386338 (2020).
doi: 10.1364/BOE.386338 pubmed: 32637250 pmcid: 7315999
Hadoux, X. et al. Non-invasive in vivo hyperspectral imaging of the retina for potential biomarker use in Alzheimer’s disease. Nat. Commun. 10, 4227. https://doi.org/10.1038/s41467-019-12242-1 (2019).
doi: 10.1038/s41467-019-12242-1 pubmed: 31530809 pmcid: 6748929
Yoon, J. et al. A clinically translatable hyperspectral endoscopy (HySE) system for imaging the gastrointestinal tract. Nat. Commun. 10, 1902. https://doi.org/10.1038/s41467-019-09484-4 (2019).
doi: 10.1038/s41467-019-09484-4 pubmed: 31015458 pmcid: 6478902
Wang, J. & Li, Q. Quantitative analysis of liver tumors at different stages using microscopic hyperspectral imaging technology. J. Biomed. Opt. 23, 1–14. https://doi.org/10.1117/1.JBO.23.10.106002 (2018).
doi: 10.1117/1.JBO.23.10.106002 pubmed: 30574694
Urade, T. et al. Hyperspectral enhanced reality (HYPER) for anatomical; liver resection. Surg. Endosc. https://doi.org/10.1007/s00464-020-07586-5 (2020).
doi: 10.1007/s00464-020-07586-5 pubmed: 32342212
Barberio, M. et al. HYPerspectral Enhanced Reality (HYPER): A physiology-based surgical guidance tool. Surg. Endosc. 34, 1736–1744. https://doi.org/10.1007/s00464-019-06959-9 (2020).
doi: 10.1007/s00464-019-06959-9 pubmed: 31309313
Barberio, M. et al. Quantitative fluorescence angiography versus hyperspectral imaging to assess bowel ischemia: A comparative study in enhanced reality. Surgery 168, 178–184. https://doi.org/10.1016/j.surg.2020.02.008 (2020).
doi: 10.1016/j.surg.2020.02.008 pubmed: 32223983
Stewart, Z. A. et al. Increased risk of graft loss from hepatic artery thrombosis after liver transplantation with older donors. Liver Transplant 15, 1688–1695. https://doi.org/10.1002/lt.21946 (2009).
doi: 10.1002/lt.21946
Pischke, S. E. et al. Hepatic and abdominal carbon dioxide measurements detect and distinguish hepatic artery occlusion and portal vein occlusion in pigs. Liver Transplant 18, 1485–1494. https://doi.org/10.1002/lt.23544 (2012).
doi: 10.1002/lt.23544
Levesque, E. et al. Plasma disappearance rate of indocyanine green: A tool to evaluate early graft outcome after liver transplantation. Liver Transplant 15, 1358–1364. https://doi.org/10.1002/lt.21805 (2009).
doi: 10.1002/lt.21805
Levesque, E. et al. Non-invasive ICG-clearance: A useful tool for the management of hepatic artery thrombosis following liver transplantation. Clin. Transplant 25, 297–301. https://doi.org/10.1111/j.1399-0012.2010.01252.x (2011).
doi: 10.1111/j.1399-0012.2010.01252.x pubmed: 20412097
Kubota, K. et al. Intraoperative assessment of reconstructed vessels in living-donor liver transplantation, using a novel fluorescence imaging technique. J. Hepatobiliary Pancreat. Surg. 13, 100–104. https://doi.org/10.1007/s00534-005-1014-z (2006).
doi: 10.1007/s00534-005-1014-z pubmed: 16547669
Skowno, J. J., Karpelowsky, J. S., Watts, N. R. & Little, D. G. Can transcutaneous near infrared spectroscopy detect severe hepatic ischemia: A juvenile porcine model. Paediatr. Anaesth. 26, 1188–1196. https://doi.org/10.1111/pan.13004 (2016).
doi: 10.1111/pan.13004 pubmed: 27663858
Diana, M. Enabling precision digestive surgery with fluorescence imaging. Transl. Gastroenterol. Hepatol. 2, 97. https://doi.org/10.21037/tgh.2017.11.06 (2017).
doi: 10.21037/tgh.2017.11.06 pubmed: 29264435 pmcid: 5723751
Nachabe, R. et al. Effect of bile absorption coefficients on the estimation of liver tissue optical properties and related implications in discriminating healthy and tumorous samples. Biomed. Opt. Express 2, 600–614. https://doi.org/10.1364/BOE.2.000600 (2011).
doi: 10.1364/BOE.2.000600 pubmed: 21412465 pmcid: 3047365
Eipel, C., Abshagen, K. & Vollmar, B. Regulation of hepatic blood flow: The hepatic arterial buffer response revisited. World J. Gastroenterol. 16, 6046–6057. https://doi.org/10.3748/wjg.v16.i48.6046 (2010).
doi: 10.3748/wjg.v16.i48.6046 pubmed: 21182219 pmcid: 3012579
Lautt, W. W. in Hepatic Circulation: Physiology and Pathophysiology Colloquium Series on Integrated Systems Physiology: From Molecule to Function to Disease (ed New York: Raven Press) 203–226 (1981).
Haugaa, H. et al. Early bedside detection of ischemia and rejection in liver transplants by microdialysis. Liver Transplant 18, 839–849. https://doi.org/10.1002/lt.23425 (2012).
doi: 10.1002/lt.23425
Halicek, M., Fabelo, H., Ortega, S., Callico, G. M. & Fei, B. In-vivo and ex-vivo tissue analysis through hyperspectral imaging techniques: Revealing the invisible features of cancer. Cancers (Basel) 11, https://doi.org/10.3390/cancers11060756 (2019).
Lautt, W. W., Schafer, J. & Legare, D. J. Hepatic blood flow distribution: Consideration of gravity, liver surface, and norepinephrine on regional heterogeneity. Can. J. Physiol. Pharmacol. 71, 128–135. https://doi.org/10.1139/y93-018 (1993).
doi: 10.1139/y93-018 pubmed: 8319136
Kilkenny, C. et al. Animal research: Reporting in vivo experiments: the ARRIVE guidelines. Br. J. Pharmacol. 160, 1577–1579. https://doi.org/10.1111/j.1476-5381.2010.00872.x (2010).
doi: 10.1111/j.1476-5381.2010.00872.x pubmed: 20649561 pmcid: 2936830
Barberio, M. et al. Quantitative fluorescence angiography versus hyperspectral imaging to assess bowel ischemia: A comparative study in enhanced reality. Surgery https://doi.org/10.1016/j.surg.2020.02.008 (2020).
doi: 10.1016/j.surg.2020.02.008 pubmed: 32223983
Uchida, M. et al. Calcium in pig livers following ischemia and reperfusion. J. Hepatol. 20, 714–719. https://doi.org/10.1016/s0168-8278(05)80140-0 (1994).
doi: 10.1016/s0168-8278(05)80140-0 pubmed: 7930470
Kulcke, A. et al. A compact hyperspectral camera for measurement of perfusion parameters in medicine. Biomed. Tech. (Berl) 63, 519–527. https://doi.org/10.1515/bmt-2017-0145 (2018).
doi: 10.1515/bmt-2017-0145
Suzuki, S., Toledo-Pereyra, L. H., Rodriguez, F. J. & Cejalvo, D. Neutrophil infiltration as an important factor in liver ischemia and reperfusion injury. Modulating effects of FK506 and cyclosporine. Transplantation 55, 1265–1272, https://doi.org/10.1097/00007890-199306000-00011 (1993).

Auteurs

Eric Felli (E)

Institute of Physiology, EA3072 Mitochondria Respiration and Oxidative Stress, University of Strasbourg, Strasbourg, France. eric.felli@ihu-strasbourg.eu.
IHU-Strasbourg, Institute of Image-Guided Surgery, Strasbourg, France. eric.felli@ihu-strasbourg.eu.

Mahdi Al-Taher (M)

IHU-Strasbourg, Institute of Image-Guided Surgery, Strasbourg, France.

Toby Collins (T)

Surgical Data Science Department, Research Institute Against Digestive Cancer (IRCAD), Strasbourg, France.

Andrea Baiocchini (A)

Department of Pathology, San Camillo Forlanini Hospital, Rome, Italy.

Emanuele Felli (E)

Department of General, Digestive, and Endocrine Surgery, University Hospital of Strasbourg, Strasbourg, France.
INSERM, Institute of Viral and Liver Disease, U1110, Strasbourg, France.

Manuel Barberio (M)

IHU-Strasbourg, Institute of Image-Guided Surgery, Strasbourg, France.
Department of Visceral, Transplant, Thoracic and Vascular Surgery, University Hospital of Leipzig, Leipzig, Germany.

Giuseppe Maria Ettorre (GM)

Department of Transplantation and General Surgery, San Camillo Hospital, Rome, Italy.

Didier Mutter (D)

Department of General, Digestive, and Endocrine Surgery, University Hospital of Strasbourg, Strasbourg, France.
Surgical Data Science Department, Research Institute Against Digestive Cancer (IRCAD), Strasbourg, France.

Veronique Lindner (V)

Department of Pathology, University Hospital, Strasbourg, France.

Alexandre Hostettler (A)

Surgical Data Science Department, Research Institute Against Digestive Cancer (IRCAD), Strasbourg, France.

Sylvain Gioux (S)

ICUBE Laboratory, Photonics Instrumentation for Health, University of Strasbourg, Strasbourg, France.

Catherine Schuster (C)

INSERM, Institute of Viral and Liver Disease, U1110, Strasbourg, France.
University of Strasbourg, Strasbourg, France.

Jacques Marescaux (J)

IHU-Strasbourg, Institute of Image-Guided Surgery, Strasbourg, France.
Surgical Data Science Department, Research Institute Against Digestive Cancer (IRCAD), Strasbourg, France.

Michele Diana (M)

Institute of Physiology, EA3072 Mitochondria Respiration and Oxidative Stress, University of Strasbourg, Strasbourg, France.
IHU-Strasbourg, Institute of Image-Guided Surgery, Strasbourg, France.
Department of General, Digestive, and Endocrine Surgery, University Hospital of Strasbourg, Strasbourg, France.
Surgical Data Science Department, Research Institute Against Digestive Cancer (IRCAD), Strasbourg, France.
ICUBE Laboratory, Photonics Instrumentation for Health, University of Strasbourg, Strasbourg, France.

Articles similaires

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male
Humans Meals Time Factors Female Adult

Classifications MeSH