Background and aims
Confocal laser endomicroscopy (CLE) can provide real-time evaluation of bowel perfusion. We aimed to evaluate CLE perfusion imaging in a hemorrhagic shock model.
Materials and methods
Five pigs were equipped to ensure hemodynamic monitoring. Three ileostomies per animal (total n = 15) were randomly created (T0). Blood was withdrawn targeting a mean arterial pressure of 40 mmHg (shock phase, T1), for 90 min. Infusion of Ringer’s lactate was started and continued for 90 min (T2). At the different time points: (a) stomas’ mucosa was scanned with CLE; (b) capillary lactates were measured on blood obtained by puncturing stomas’ mucosa; and (c) full-thickness stomas’ biopsies were sampled for histology, mitochondrial respiratory rate (V 0 = basal and V ADP = respiratory rate in excess of adenosine diphosphate), and levels of superoxide anion evaluation. Functional capillary density (FCD) was measured using ad hoc software.
Confocal scanning provided consistent and specific imaging of bowel hypoperfusion at T1: vascular hyperpermeability (blurred and enlarged capillaries) and edema (enhanced visualization of the brush border due to increased intercellular spaces and fluorescein leakage). At the end of T2, there was an improved capillary flow. FCD-A index expressed statistically significant correlation with (1) stoma capillary lactates (p = 0.023); (2) systemic capillary lactates (p = 0.031); (3) inflammation pathology score (p = 0.048); (4) central venous pressure (p = 0.0043); and (5) pulmonary artery pressure (p = 0.01). Stoma capillary lactates (mmol/L) were significantly increased at T1 (8.81 ± 4.23; p < 0.0001) and at T2 (4.77 ± 3.13; p < 0.01) when compared to T0 inclusion values (1.86 ± 0.56). V 0 and V ADP (pmol O2/min/mg tissue) were both significantly decreased at T1 versus T0 (p < 0.007 and p < 0.01, respectively) and recovered by the end of reanimation (T2 vs. T0, p = n.s.). Mean O 2 ·− production (µmol/min/mg/dry tissue) increased at T1 and significantly decreased at T2.
Confocal laser endomicroscopy (CLE) imaging could identify morphological signs congruent with biochemical markers of bowel perfusion and could be useful for assessment of stomas.
This is a preview of subscription content, log in to check access.
Buy single article
Instant unlimited access to the full article PDF.
Price includes VAT for USA
Ashley EA (2015) The precision medicine initiative: a new national effort. JAMA 313:2119–2120
Committee AT (2014) Confocal laser endomicroscopy. Gastrointest Endosc 80:928–938
Laemmel E, Genet M, Le Goualher G, Perchant A, Le Gargasson JF, Vicaut E (2004) Fibered confocal fluorescence microscopy (Cell-viZio) facilitates extended imaging in the field of microcirculation. A comparison with intravital microscopy. J Vasc Res 41:400–411
Park JJ, Del Pino A, Orsay CP, Nelson RL, Pearl RK, Cintron JR, Abcarian H (1999) Stoma complications: the Cook County Hospital experience. Dis Colon Rectum 42:1575–1580
Pearl RK, Prasad ML, Orsay CP, Abcarian H, Tan AB, Melzl MT (1985) Early local complications from intestinal stomas. Arch Surg 120:1145–1147
Schmidt C, Lautenschläger C, Petzold B, Sakr Y, Marx G, Stallmach A (2013) Confocal laser endomicroscopy reliably detects sepsis-related and treatment-associated changes in intestinal mucosal microcirculation. Br J Anaesth 111(6):996–1003. doi:10.1093/bja/aet219
Kilkenny C, Browne WJ, Cuthill IC, Emerson M, Altman DG (2010) Improving bioscience research reporting: the ARRIVE guidelines for reporting animal research. PLoS Biol 8:e1000412
Balkamou X, Xanthos T, Stroumpoulis K, Moutzouris DA, Rokas G, Agrogiannis G, Demestiha T, Patsouris E, Papadimitriou L (2010) Hydroxyethyl starch 6 % (130/0.4) ameliorates acute lung injury in swine hemorrhagic shock. Anesthesiology 113:1092–1098
Diana M, Agnus V, Halvax P, Liu YY, Dallemagne B, Schlagowski AI, Geny B, Diemunsch P, Lindner V, Marescaux J (2015) Intraoperative fluorescence-based enhanced reality laparoscopic real-time imaging to assess bowel perfusion at the anastomotic site in an experimental model. Br J Surg 102:e169–e176
Diana M, Dallemagne B, Chung H, Nagao Y, Halvax P, Agnus V, Soler L, Lindner V, Demartines N, Diemunsch P, Geny B, Swanstrom L, Marescaux J (2014) Probe-based confocal laser endomicroscopy and fluorescence-based enhanced reality for real-time assessment of intestinal microcirculation in a porcine model of sigmoid ischemia. Surg Endosc 28:3224–3233
Diana M, Noll E, Diemunsch P, Moussallieh F-M, Namer I-J, Charles A-L, Lindner V, Agnus V, Geny B, Marescaux J (2015) Metabolism-guided bowel resection: potential role and accuracy of instant capillary lactates to identify the optimal resection site. Surg Innov 22(5):453–461. doi:10.1177/1553350615598620
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 259:700–707
Diana M, Pop R, Beaujeux R, Dallemagne B, Halvax P, Schlagowski I, Liu YY, Diemunsch P, Geny B, Lindner V, Marescaux J (2015) Embolization of arterial gastric supply in obesity (EMBARGO): an endovascular approach in the management of morbid obesity. Proof of the concept in the porcine model. Obes Surg 25(3):550–558. doi:10.1007/s11695-014-1535-0
Schlagowski AI, Singh F, Charles AL, Gali Ramamoorthy T, Favret F, Piquard F, Geny B, Zoll J (1985) Mitochondrial uncoupling reduces exercise capacity despite several skeletal muscle metabolic adaptations. J Appl Physiol 116(4):364–375. doi:10.1152/japplphysiol.01177.2013
Dikalov SI, Li W, Mehranpour P, Wang SS, Zafari AM (2007) Production of extracellular superoxide by human lymphoblast cell lines: comparison of electron spin resonance techniques and cytochrome c reduction assay. Biochem Pharmacol 73:972–980
Lejay A, Choquet P, Thaveau F, Singh F, Schlagowski A, Charles AL, Laverny G, Metzger D, Zoll J, Chakfe N, Geny B (2015) A new murine model of sustainable and durable chronic critical limb ischemia fairly mimicking human pathology. Eur J Vasc Endovasc Surg 49:205–212
Turnbull GB (2003) Ostomy statistics: the $64,000 question. Ostomy/Wound Manag 49:22–23
Kann BR (2008) Early stomal complications. Clin Colon Rectal Surg 21:23–30
Husain SG, Cataldo TE (2008) Late stomal complications. Clin Colon Rectal Surg 21:31–40
Yasumura M, Mori Y, Takagi H, Yamada T, Sakamoto K, Iwata H, Hirose H (2003) Experimental model to estimate intestinal viability using charge-coupled device microscopy. Br J Surg 90:460–465
Colantuoni A, Bertuglia S, Intaglietta M (1985) Microvessel diameter changes during hemorrhagic shock in unanesthetized hamsters. Microvasc Res 30:133–142
Diana M, Halvax P, Dallemagne B, Nagao Y, Diemunsch P, Charles AL, Agnus V, Soler L, Demartines N, Lindner V, Geny B, Marescaux J (2014) Real-time navigation by fluorescence-based enhanced reality for precise estimation of future anastomotic site in digestive surgery. Surg Endosc 28(11):3108–3118. doi:10.1007/s00464-014-3592-9
Diana M, Halvax P, Dallemagne B, Nagao Y, Diemunsch P, Charles AL, Agnus V, Soler L, Demartines N, Lindner V, Geny B, Marescaux J (2014) Real-time navigation by fluorescence-based enhanced reality for precise estimation of future anastomotic site in digestive surgery. Surg Endosc 28:3108–3118
Noll E, Bouitbir J, Collange O, Zoll J, Charles AL, Thaveau F, Diemunsch P, Geny B (2012) Local but not systemic capillary lactate is a reperfusion biomarker in experimental acute limb ischaemia. Eur J Vasc Endovasc Surg 43:339–340
Guillot M, Charles AL, Chamaraux-Tran TN, Bouitbir J, Meyer A, Zoll J, Schneider F, Geny B (2014) Oxidative stress precedes skeletal muscle mitochondrial dysfunction during experimental aortic cross-clamping but is not associated with early lung, heart, brain, liver, or kidney mitochondrial impairment. J Vasc Surg 60(1043–1051):e1045
Selka F, Nicolau S, Agnus V, Bessaid A, Marescaux J, Soler L (2015) Context-specific selection of algorithms for recursive feature tracking in endoscopic image using a new methodology. Comput Med Imaging Graph 40:49–61
Jacques Marescaux is the president of both IRCAD and IHU institutes, which are partly funded by Karl Storz, Medtronic, and Siemens Healthcare. Michele Diana, Eric Noll, Anne-Laure Charles, Pierre Diemunsch, Bernard Geny, Yu-Yin Liu, Francesco Marchegiani, Luigi Schiraldi, Vincent Agnus, Veronique Lindner, Lee Swanström, and Bernard Dallemagne have no conflicts of interest or financial ties to disclose.
Electronic supplementary material
Below is the link to the electronic supplementary material.
The narrated video-clip displays the experimental setting and highlights the main morphological changes of bowel mucosa that could be identified by Confocal Endomicroscopy during the hemorrhagic shock and the fluid therapy (MP4 100563 kb)
About this article
Cite this article
Diana, M., Noll, E., Charles, A. et al. Precision real-time evaluation of bowel perfusion: accuracy of confocal endomicroscopy assessment of stoma in a controlled hemorrhagic shock model. Surg Endosc 31, 680–691 (2017). https://doi.org/10.1007/s00464-016-5022-7
- Confocal laser endomicroscopy
- Functional capillary density area
- Bowel perfusion
- Stoma perfusion
- Hemorrhagic shock model
- Mitochondria respiratory rate
- Electron paramagnetic resonance
- Oxidative stress