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Intensive Care Medicine
Published in: Intensive Care Medicine 3/2018

01-03-2018 | Conference Reports and Expert Panel

Second consensus on the assessment of sublingual microcirculation in critically ill patients: results from a task force of the European Society of Intensive Care Medicine

Authors: Can Ince, E. Christiaan Boerma, Maurizio Cecconi, Daniel De Backer, Nathan I. Shapiro, Jacques Duranteau, Michael R. Pinsky, Antonio Artigas, Jean-Louis Teboul, Irwin K. M. Reiss, Cesar Aldecoa, Sam D. Hutchings, Abele Donati, Marco Maggiorini, Fabio S. Taccone, Glenn Hernandez, Didier Payen, Dick Tibboel, Daniel S. Martin, Alexander Zarbock, Xavier Monnet, Arnaldo Dubin, Jan Bakker, Jean-Louis Vincent, Thomas W. L. Scheeren, On behalf of the Cardiovascular Dynamics Section of the ESICM

Published in: Intensive Care Medicine | Issue 3/2018

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Abstract

Purpose

Hand-held vital microscopes (HVMs) were introduced to observe sublingual microcirculatory alterations at the bedside in different shock states in critically ill patients. This consensus aims to provide clinicians with guidelines for practical use and interpretation of the sublingual microcirculation. Furthermore, it aims to promote the integration of routine application of HVM microcirculatory monitoring in conventional hemodynamic monitoring of systemic hemodynamic variables.

Methods

In accordance with the Delphi method we organized three international expert meetings to discuss the various aspects of the technology, physiology, measurements, and clinical utility of HVM sublingual microcirculatory monitoring to formulate this consensus document. A task force from the Cardiovascular Dynamics Section of the European Society of Intensive Care Medicine (with endorsement of its Executive Committee) created this consensus as an update of a previous consensus in 2007. We classified consensus statements as definitions, requirements, and/or recommendations, with a minimum requirement of 80% agreement of all participants.

Results

In this consensus the nature of microcirculatory alterations is described. The nature of variables, which can be extracted from analysis of microcirculatory images, is presented and the needed dataset of variables to identify microcirculatory alterations is defined. Practical aspects of sublingual HVM measurements and the nature of artifacts are described. Eleven statements were formulated that pertained to image acquisitions and quality statements. Fourteen statements addressed the analysis of the images, and 13 statements are related to future developments.

Conclusion

This consensus describes 25 statements regarding the acquisition and interpretation of microcirculatory images needed to guide the assessment of the microcirculation in critically ill patients.
Literature
1.
Groner W, Winkelman JW, Harris AG, Ince C, Bouma GJ, Messmer K, Nadeau R (1999) Orthogonal polarization spectral imaging: a new method for study of the microcirculation. Nat Med 5(10):1209–1212PubMedCrossRef
2.
Mathura KR, Bouma GJ, Ince C (2001) Abnormal microcirculation in brain tumours during surgery. Lancet 358(9294):1698–1699PubMedCrossRef
3.
De Backer D, Creteur J, Preiser JC, Dubois MJ, Vincent JL (2002) Microvascular blood flow is altered in patients with sepsis. Am J Respir Crit Care Med 166(1):98–104PubMedCrossRef
4.
Spronk PE, Ince C, Gardien MJ, Mathura KR, Oudemans-van Straaten HM, Zandstra DF (2002) Nitroglycerin in septic shock after intravascular volume resuscitation. Lancet 360:1395–1396PubMedCrossRef
5.
6.
Top APC, Ince C, de Meij N, van Dijk M, Tibboel D (2011) Persistent low microcirculatory vessel density in nonsurvivors of sepsis in pediatric intensive care. Crit Care Med 39(1):8–13PubMedCrossRef
7.
Edul VS, Enrico C, Laviolle B, Vazquez AR, Ince C, Dubin A (2012) Quantitative assessment of the microcirculation in healthy volunteers and in patients with septic shock. Crit Care Med 40(5):1443–1448PubMedCrossRef
8.
De Backer D, Donadello K, Sakr Y, Ospina-Tascon G, Salgado D, Scolletta S, Vincent JL (2013) Microcirculatory alterations in patients with severe sepsis: impact of time of assessment and relationship with outcome. Crit Care Med 41(3):791–799PubMedCrossRef
9.
Sakr Y, Dubois MJ, De Backer D, Creteur J, Vincent JL (2004) Persistent microcirculatory alterations are associated with organ failure and death in patients with septic shock. Crit Care Med 32(9):1825–1831PubMedCrossRef
10.
Trzeciak S, McCoy JV, Phillip Dellinger R, Arnold RC, Rizzuto M, Abate NL, Shapiro NI, Parrillo JE, Hollenberg SM (2008) Early increases in microcirculatory perfusion during protocol-directed resuscitation are associated with reduced multi-organ failure at 24 h in patients with sepsis. Intensive Care Med 34:2210–2217PubMedPubMedCentralCrossRef
11.
De Uil CA, Bezemer R, Miranda DR, Ince C, Lagrand WK, Hartman JM, Bogers A, Spronk PE, Somoons ML (2009) Intra-operative assessment of human pulmonary alveoli in vivo using SDF imaging: a feasibility study. Med Sci Monit 15(10):137–140
12.
Snoeijs MG, Vink H, Voesten N, Christiaans MH, Daemen JH, Peppelenbosch AG, Tordoir JH, Peutz-Kootstra CJ, Buurman WA, Schurink GWH, van Heurn WE (2010) Acute ischemic injury to the renal microvasculature in human kidney transplantation. Am J Physiol Renal Physiol 299:F1134–F1140PubMedCrossRef
13.
Nilsson J, Eriksson S, Blind PJ, Rissler P, Sturesson C (2014) Microcirculation changes during liver resection—a clinical study. Microvasc Res 94:47–55PubMedCrossRef
14.
Pérez-Bárcena J, Goedhart P, Ibáñez J, Brell M, García R, Llinás P, Jiménez C, Ince C (2011) Direct observation of human microcirculation during decompressive craniectomy after stroke. Crit Care Med 39(5):1126–1923PubMedCrossRef
15.
de Bruin AF, Tavy A, van der Sloot K, Smits A, Van Ramshorst B, Boerma CE, Kars P, Noordzij PG, Boerma D, van Iterson M (2016) Use of an image acquisition stabilizer improves sidestream dark field imaging of the serosa during open gastrointestinal surgery. J Vasc Res 53(3–4):121–127PubMedCrossRef
16.
Djaberi R, Schuijf JD, de Koning EJ, Wijewickrama DC, Pereira AM, Smit JW, Kroft LJ, Roos A, Bax JJ, Rabelink TJ, Jukema JW (2013) Non-invasive assessment of microcirculation by sidestream dark field imaging as a marker of coronary artery disease in diabetes. Diab Vasc Dis Res 10(2):123–134PubMedCrossRef
17.
Dondorp AM, Ince C, Tipmanee P, Hanson J, van Kuijen A, Faiz MA, Rahman MR, Hasan M, Bin Yunus E, Ghose A, Ruangveerayut R, Limmathurotsakul D, Mathura K, White NJ, Day NPJ (2008) Direct in vivo assessment of microcirculatory dysfunction in severe falciparum malaria. J Infect Dis 197(1):79–84PubMedCrossRef
18.
Khalilzada M, Dogan K, Ince C, Stam J (2011) Sublingual microvascular changes in patients with cerebral small vessel disease. Stroke 42(7):2071–2073PubMedCrossRef
19.
Dababneh L, Cikach F, Alkukhun L, Dweik RA, Tonelli AR (2014) Sublingual microcirculation in pulmonary arterial hypertension. Ann Am Thoracic Soc 11(4):504–512CrossRef
20.
Lindeboom JAH, Mathura KR, Aartman IH, Kroon F, Ince C (2007) The influence of the application of platelet enriched plasma’s in oral mucosal wound healing. Clin Oral Impl Res 18:133–139CrossRef
21.
Meinders AJ, Elbers P (2009) Images in clinical medicine. Leukocytosis and sublingual microvascular blood flow. N Engl J Med 360(7):e9PubMedCrossRef
22.
Vollebregt KC, Boer K, Mathura KR, de Graaff JC, Ubbink DT, Ince C (2001) Impaired vascular function in women with pre-eclampsia observed with OPS imaging. Br J Obst Gyn 41:1148–1153
23.
Meinders AJ, Nieuwenhuis L, Ince C, Bos WJ, Elbers PW (2015) Haemodialysis impairs the human microcirculation independent from macrohemodynamic parameters. Blood Purif 40(1):38–44PubMedCrossRef
24.
De Backer D, Creteur J, Dubois MJ, Sakr Y, Vincent JL (2004) Microvascular alterations in patients with acute severe heart failure and cardiogenic shock. Am Heart J 147(1):91–99PubMedCrossRef
25.
Tachon G, Harrois A, Tanaka S, Kato H, Huet O, Pottecher J, Vicaut E, Duranteau J (2014) Microcirculatory alterations in traumatic hemorrhagic shock. Crit Care Med 42(6):1433–1441PubMedCrossRef
26.
Edul VSK, Ince C, Estenssoro E, Ferrara G, Arzani Y, Salvatori C, Dubin A (2015) The effects of arterial hypertension and age on the sublingual microcirculation of healthy volunteers and outpatients with cardiovascular risk factors. Microcirculation 22:485–492CrossRef
27.
Kuipers JW, Tiboel D, Ince C (2016) The pediatric microcirculation. Crit Care 20(1):352CrossRef
28.
Vellinga NA, Boerma EC, Koopmans M, Donati A, Dubin A, Shapiro NI, Pearse RM, Machado FR, Fries M, Akarsu-Ayazoglu T, Pranskunas A, Hollenberg S, Balestra G, van Iterson M, van der Voort PH, Sadaka F, Minto G, Aypar U, Hurtado FJ, Martinelli G, Payen D, van Haren F, Holley A, Pattnaik R, Gomez H, Mehta RL, Rodriguez AH, Ruiz C, Canales HS, Duranteau J, Spronk PE, Jhanji S, Hubble S, Chierego M, Jung C, Martin D, Sorbara C, Tijssen JG, Bakker J, Ince C, microSOAP Study Group (2015) International study on microcirculatory shock occurrence in acutely ill patients. Crit Care Med 43(1):48–56PubMedCrossRef
29.
Top AP, van Dijk M, van Velzen JE, Ince C, Tibboel D (2011) Functional capillary density decreases after the first week of life in term neonates. Neonatology 99(1):73–77PubMedCrossRef
30.
van den Berg VJ, van Elteren HA, Buijs EA, Ince C, Tibboel D, Reiss IK, de Jonge RC (2015) Reproducibility of microvascular vessel density analysis in sidestream dark-field-derived images of healthy term newborns. Microcirculation 22(1):37–43PubMedCrossRef
31.
Sheena MA, Hubble A, Hayley L, Kyte A, Gooding K, Shore AC (2009) Variability in sublingual microvessel density and flow measurements in healthy volunteers. Microcirculation 16:183–191CrossRef
32.
Bartels SA, Bezemer R, Milstein DM, Radder M, Lima A, Cherpanath TG, Heger M, Karemaker JM, Ince C (2011) The microcirculatory response to compensated hypovolemia in a lower body negative pressure model. Microvasc Res 82(3):374–380PubMedCrossRef
33.
Gu YM, Wang S, Zhang L, Liu YP, Thijs L, Petit T, Zhang Z, Wei FF, Kang YY, Huang QF, Sheng CS, Struijker-Boudier HA, Kuznetsova T, Verhamme P, Li Y, Staessen JA (2005) Characteristics and determinants of the sublingual microcirculation in populations of different ethnicity. Hypertension 65(5):993–1001CrossRef
34.
Gilbert-Kawai E, Coppel J, Court J, van der Kaaij J, Vercueil A, Feelisch M, Levett D, Mythen M, Grocott MP, Martin D, Xtreme Everest 2 Research Group (2017) Sublingual microcirculatory blood flow and vessel density in Sherpas at high altitude. J Appl Physiol 122(4):1011–1018PubMedCrossRef
35.
Gassmann NN, van Elteren HA, Goos TG, Morales CR, Rivera-Ch M, Martin DS, Cabala Peralta P, Passano Del Carpio A, Aranibar Machaca S, Huicho L, Reiss IK, Gassmann M, de Jonge RC (2016) Pregnancy at high altitude in the andes leads to increased total vessel density in healthy newborns. J Appl Physiol 121(3):709–715PubMedPubMedCentralCrossRef
36.
Slaaf DW, Tangelder GJ, Reneman RS, Jäger K, Bollinger A (1987) A versatile incident illuminator for intravital microscopy. Int J Microcirc Clin Exp 6(4):391–397PubMed
37.
Goedhart PT, Khalilzada M, Bezemer R, Merza J, Ince C (2007) Sidestream dark field (SDF) imaging: a novel stroboscopic LED ring-based imaging modality for clinical assessment of the microcirculation. Opt Express 15(23):15101–15114PubMedCrossRef
38.
Sherman H, Klausner S, Cook WA (1971) Incident dark-field illumination a new method for microcirculation study. Angiology 22:295–303PubMedCrossRef
39.
Aykut G, Veenstra G, Scorcella C, Ince C, Boerma C (2015) Cytocam-IDF (incident dark field illumination) imaging for bedside monitoring of the microcirculation. Intensive Care Med Exp 3:40PubMedCrossRef
40.
van Elteren H, van den Berg V, de Jonge R, Ince C, Reiss I (2014) Cutaneous microcirculation in preterm neonates: comparison between sidestream darkfield (SDF) and incident darkfield (IDF) imaging. Pediatr Crit Care Med 15(4):130–131CrossRef
41.
Gilbert-Kawai E, Coppel J, Bountziouka V, Ince C, Martin D, Caudwell Xtreme Everest 2 Research Group (2016) A comparison of the quality of image acquisition between the incident dark field and sidestream dark field video-microscopes. BMC Med Imaging 16:10PubMedPubMedCentralCrossRef
42.
Hutchings S, Watts S, Kirkman E (2016) The cytocam video microscope. A new method for visualising the microcirculation using incident dark field technology. Clin Hemorheol Microcirc 62(3):261–271PubMedCrossRef
43.
Massey MJ, Shapiro NI (2016) A guide to human in vivo microcirculatory flow image analysis. Crit Care 10(20):35
44.
45.
Pranskunas A, Koopmans M, Koetsier PM, Pilvinis V, Boerma EC (2013) Microcirculatory blood flow as a tool to select ICU patients eligible for fluid therapy. Intensive Care Med 39:612–619PubMedCrossRef
46.
Hanson JP, Sophia M, Lam W, Mohanty S, Alam S, Pattnaik R, Mahanta KC, Hasan MU, Charunwatthana P, Mishra SK, Day NPJ, White NJ, Dondorp AM (2013) Fluid resuscitation of adults with severe falciparum malaria: effects on acid-base status, renal function, and extravascular lung water. Crit Care Med 41(4):972–981PubMedCrossRef
47.
Jhanji S, Stirling S, Patel N, Hinds CJ, Pearse RM (2009) The effect of increasing doses of norepinephrine on tissue oxygenation and microvascular flow in patients with septic shock. Critl Care Med 37(6):1961–1966CrossRef
48.
Dubin A, Pozo O, Casabell C, Murias G, Mosinco M, Kanoore Edul V, Pálizas F, Estenssoro A, Ince C, Ince EC (2009) Increasing arterial blood pressure with norepinephrine does not improve microcirculatory blood flow: a prospective study. Crit Care 13:R9CrossRef
49.
Buijs EA, Reiss IK, Kraemer U, Andrinopoulou ER, Zwiers AJ, Ince C, Tibboel D (2014) Increasing mean arterial blood pressure and heart rate with catecholaminergic drugs does not improve the microcirculation in children with congenital diaphragmatic hernia: a prospective cohort study. Pediatr Crit Care Med 15(4):343–354PubMedCrossRef
50.
Vincent JL, Taccone FS (2016) Microvascular monitoring – Do ‘global’ markers help? Best Pract Res Clin Anaesth 30(4):399–405CrossRef
51.
Arnold RC, Dellinger RP, Parrillo JE, Chansky ME, Lotano VE, McCoy JV, Jones AE, Shapiro NI, Hollenberg SM, Trzeciak S (2012) Discordance between microcirculatory alterations and arterial pressure in patients with hemodynamic instability. J Crit Care 27(5):5311–5317CrossRef
52.
Ince C, Sinaasappel M (1999) Microcirculatory oxygenation and shunting in sepsis and shock. Crit Care Med 27:1369–1377PubMedCrossRef
53.
De Backer D, Hollenberg S, Boerma C, Goedhart P, Buchele G, Ospina-Tascon G, Dobbe I, Ince C (2007) How to evaluate the microcirculation: report of a round table conference. Crit Care 11:R101PubMedPubMedCentralCrossRef
54.
Cecconi M, De Backer D, Antonelli M, Beale R, Bakker J, Hofer C, Jaeschke R, Mebazaa A, Pinsky MR, Teboul JL, Vincent JL, Rhodes A (2014) Consensus on circulatory shock and hemodynamic monitoring. Task force of the European Society of Intensive Care Medicine. Intensive Care Med 40:1795–1815PubMedPubMedCentralCrossRef
55.
Teboul JL, Saugel B, Cecconi M, De Backer D, Hofer CK, Monnet X, Perel A, Pinsky MR, Reuter DA, Rhodes A, Squara P, Vincent JL, Scheeren TW (2016) Less invasive hemodynamic monitoring in critically ill patients. Intensive Care Med 42:1350–1956PubMedCrossRef
56.
Atasever B, Boer C, van der Kuil M, Lust E, Beishuizen A, Speekenbrink R, Seyffert J, de Mol B, Ince C (2011) Quantitative imaging of microcirculatory response during nitroglycerin-induced hypotension. J Cardiothorac Vasc Anesth. 25(1):140–144PubMedCrossRef
57.
Kildal AB, Stenberg TA, Sanden E, Myrmel T, How OJ (2015) Prolonged observation time reveals temporal fluctuations in the sublingual microcirculation in pigs given arginine vasopressin. J Appl Physiol 118(8):965–970PubMedCrossRef
58.
Massey MJ, Larochelle E, Najarro G, Karmacharla A, Arnold R, Trzeciak S, Angus DC, Shapiro NI (2013) The microcirculation image quality score: development and preliminary evaluation of a proposed approach to grading quality of image acquisition for bedside videomicroscopy. J Crit Care 28:913–917PubMedCrossRef
59.
Damiani E, Ince C, Scorcella C, Domizi R, Carsetti A, Mininno N, Pierantozzi S, Adrario E, Romano R, Pelaia P, Donati A (2017) Impact of microcirculatory video quality on the evaluation of sublingual microcirculation in critically ill patients. J Clin Monit Comput 31:981–988PubMedCrossRef
60.
Sallisalmi M, Oksala N, Pettilä V, Tenhunen J (2012) Evaluation of sublingual microcirculatory blood flow in the critically ill. Acta Anaesth Scand 56(3):298–306PubMedCrossRef
61.
Boerma EC, Mathura KR, van der Voort PHJ, Spronk PE, Ince C (2005) Quantifying bedside-derived imaging of microcirculatory abnormalities in septic patients: a prospective validation study. Crit Care 9:R601–R606PubMedPubMedCentralCrossRef
62.
Pozo MO, Kanoore Edul VS, Ince C, Dubin A (2012) Comparison of different methods for the calculation of the microvascular flow index. Crit Care Res Pract 2012:102483PubMedPubMedCentral
63.
Tanaka S, Harrois A, Nicolaï C, Flores M, Hamada S, Vicaut E, Duranteau J (2015) Qualitative real-time analysis by nurses of sublingual microcirculation in intensive care unit: the MICRONURSE study. Crit Care 19:388PubMedPubMedCentralCrossRef
64.
Arnold RC, Parrillo JE, Phillip Dellinger R, Chansky ME, Shapiro NI, Lundy DJ, Trzeciak S, Hollenberg SM (2009) Point-of-care assessment of microvascular blood flow in critically ill patients. Intensive Care Med 35:1761–1766PubMedCrossRef
65.
Cerny V, Abdoa I, George RB, Maddisond L, Sharawie N, Lehmann C (2016) Analysis of microcirculation measurements by novice users trained by a standardized interactive tutorial: an inter-observer variability study. Clin Hemorheol Microcirc 62:123–128PubMedCrossRef
66.
Naumann DN, Mellis C, Husheer SL, Hopkins P, Bishop J, Midwinter MJ, Hutchings SD (2016) Real-time point of care microcirculatory assessment of shock: design, rationale and application of the point of care microcirculation (POEM) tool. Crit Care 20:310PubMedPubMedCentralCrossRef
67.
Lima A, Lopez A, van Genderen ME, Hurtado FJ, Angulo M, Grignola C, Shono A, van Bommel J (2015) Interrater reliability and diagnostic performance of subjective evaluation of sublingual microcirculation images by physicians and nurses: a multicenter observational study. Shock 44(3):239–244PubMedCrossRef
68.
Dobbe JG, Streekstra GJ, Atasever B, van Zijderveld R, Ince C (2008) Measurement of functional microcirculatory geometry and velocity distributions using automated image analysis. Med Biol Eng Comput 46(7):659–670PubMedPubMedCentralCrossRef
69.
Bezemer R, Dobbe J, Bartels SA, Boerma EC, Elbers PWG, Heger M, Ince C (2011) Rapid automatic assessment of microvascular density in sidestream dark field images. Med Biol Eng Comput 49(11):1269–1278PubMedPubMedCentralCrossRef
70.
Demir SU, Hakimzadeh R, Hargraves RH, Ward KR, Myer EV, Najarian K (2012) An automated method for analysis of microcirculation videos for accurate assessment of tissue perfusion. BMC Med Imaging 12:37–50PubMedPubMedCentralCrossRef
71.
72.
Carsetti A, Aya HD, Pierantozzi S, Bazurro S, Donati A, Rhodes A, Cecconi M (2017) Ability and efficiency of an automatic analysis software to measure microvascular parameters. J Clin Monit Comput 31(4):669–676PubMedCrossRef
73.
Sorelli M, Ince C, Bocchi L (2017) Particle tracking for the assessment of microcirculatory perfusion. Physiol Meas 38(2):358–373PubMedCrossRef
74.
Arnemann PH, Hessler M, Kampmeier T, Morelli A, Van Aken HK, Westphal M, Rehberg S, Ertmer C (2016) Comparison of an automatic analysis and a manual analysis of conjunctival microcirculation in a sheep model of haemorrhagic shock. Intensive Care Med Exp 4(1):37PubMedPubMedCentralCrossRef
75.
Elbers PE, Ince C (2006) Mechanisms of critical illness: classifying microcirculatory flow abnormalities in distributive shock. Crit Care 10(4):221–299PubMedPubMedCentralCrossRef
76.
Ospina-Tascon G, Neves AP, Occhipinti G, Donadello K, Büchele G, Simion D, Chierego ML, Silva TO, Fonseca A, Vincent JL, De Backer D (2010) Effects of fluids on microvascular perfusion in patients with severe sepsis. Intensive Care Med 36(6):949–955PubMedCrossRef
77.
Pottecher J, Deruddre S, Teboul JL, Georger JF, Laplace C, Benhamou D, Vicaut E, Duranteau J (2010) Both passive leg raising and intravascular volume expansion improve sublingual microcirculatory perfusion in severe sepsis and septic shock patients. Intensive Care Med 36(11):1867–1874PubMedCrossRef
78.
Dubin A, Pozo MO, Casabella CA, Murias G, Pálizas F Jr, Moseinco MC, Kanoore Edul VS, Pálizas F, Estenssoro E, Ince C (2010) Comparison of 6% hydroxyethyl starch 130/0.4 and saline solution for resuscitation of the microcirculation during the early goal-directed therapy of septic patients. J Crit Care 25(4):1–8CrossRef
79.
Tanaka S, Escudier E, Hamada S, Harrois A, Leblanc PE, Vicaut E, Duranteau J (2017) Effect of RBC transfusion on sublingual microcirculation in hemorrhagic shock patients: a pilot study. Crit Care Med 45(2):e154–e160PubMedCrossRef
80.
Sakr Y, Chierego M, Piagnerelli M, Verdant C, Dubois MJ, Koch M, Creteur J, Gullo A, Vincent JL, De Backer D (2007) Microvascular response to red blood cell transfusion in patients with severe sepsis. Crit Care Med 35(7):1639–1644PubMedCrossRef
81.
Yuruk K, Almac E, Bezemer R, Goedhart P, de Mol B, Ince C (2011) Blood transfusions recruit the microcirculation during cardiac surgery. Transfusion 51(5):961–967PubMedCrossRef
82.
Atasever B, van der Kuil M, Boer C, Vonk A, Schwarte L, Girbes AR, Ince C, Beishuizen A, Groeneveld AB (2012) Red blood cell transfusion compared with gelatin solution and no infusion after cardiac surgery: effect on microvascular perfusion, vascular density, hemoglobin, and oxygen saturation. Transfusion 52(11):2452–2458PubMedCrossRef
83.
De Backer D, Creteur J, Dubois MJ, Sakr Y, Koch M, Verdant C, Vincent JL (2006) The effects of dobutamine on microcirculatory alterations in patients with septic shock are independent of its systemic effects. Crit Care Med 34(2):403–408PubMedCrossRef
84.
Hernandez G, Bruhn A, Luengo C, Regueira T, Kattan E, Fuentealba A, Florez J, Castro R, Aquevedo A, Pairumani R, McNab P, Ince C (2013) Effects of dobutamine on systemic, regional and microcirculatory perfusion parameters in septic shock: a randomized, placebo-controlled, double-blind, crossover study. Intensive Care Med 39(8):1435–1443PubMedCrossRef
85.
Koch M, De Backer D, Vincent JL, Barvais L, Hennart D, Schmartz D (2008) Effects of propofol on human microcirculation. Br J Anaesth 101(4):473–478PubMedCrossRef
86.
Özarslan NG, Ayhan B, Kanbak M, Çelebioğlu B, Demircin M, Ince C, Aypar Ü (2012) Comparison of the effects of sevoflurane, isoflurane, and desflurane on microcirculation in coronary artery bypass graft surgery. J Cardiothorac Vasc Anesth 26(5):791–798PubMedCrossRef
87.
Petroni T, Harrois A, Amour J, Lebreton G, Brechot N, Tanaka S, Luyt CE, Trouillet JL, Chastre J, Leprince P, Duranteau J, Combes A (2014) Intra-aortic balloon pump effects on macrocirculation and microcirculation in cardiogenic shock patients supported by venoarterial extracorporeal membrane oxygenation. Crit Care Med 42(9):2075–2082PubMedCrossRef
88.
Akin S, Dos Reis Miranda D, Caliskan K, Soliman OI, Guven G, Struijs A, van Thiel RJ, Jewbali LS, Lima A, Gommers D, Zijlstra F, Ince C (2017) Functional evaluation of sublingual microcirculation indicates successful weaning from VA-ECMO in cardiogenic shock. Crit Care 21(1):265PubMedPubMedCentralCrossRef
89.
Krupičková P, Huptych M, Mormanová Z, Bouček T, Belza T, Šmíd O, Král A, Skalická H, Linhart A, Bělohlávek J (2017) Effect of pulsatility on microcirculation in patients treated with extracorporeal cardiopulmonary resuscitation: a pilot study. ASAIO J 63(4):386–391PubMedCrossRef
90.
Kara A, Akin S, Dos Reis Miranda D, Struijs A, Caliskan K, van Thiel RJ, Dubois EA, de Wilde W, Zijlstra F, Gommers D, Ince C (2016) Microcirculatory assessment of patients under VA-ECMO. Crit Care 20(1):344PubMedPubMedCentralCrossRef
91.
Koning NJ, Simon LE, Asfar P, Baufreton C, Boer C (2014) Systemic microvascular shunting through hyperdynamic capillaries after acute physiological disturbances following cardiopulmonary bypass. Am J Physiol Heart Circ Physiol 307(7):H967–H975PubMedCrossRef
92.
Yuruk K, Bezemer R, Euser M, Milstein DM, de Geus HH, Scholten EW, de Mol BA, Ince C (2012) The effects of conventional extracorporeal circulation versus miniaturized extracorporeal circulation on microcirculation during cardiopulmonary bypass-assisted coronary artery bypass graft surgery. Interact Cardiovasc Thorac Surg 15(3):364–370PubMedPubMedCentralCrossRef
93.
Atasever B, Boer C, Goedhart P, Biervliet J, Seyffert J, Speekenbrink R, Schwarte L, de Mol B, Ince C (2011) Distinct alterations in sublingual microcirculatory blood flow and hemoglobin oxygenation in on-pump and off-pump coronary artery bypass graft surgery. J Cardiothorac Vasc Anesth 25(5):784–790PubMedCrossRef
94.
Munsterman LDH, Elbers PWG, van Dongen EPA, van Iterson M, Ince C (2010) Withdrawing intra-aortic counter pulsation improves microvascular flow. Crit Care 14(4):R16CrossRef
95.
Jung C, Fuernau G, de Waha S, Eitel I, Desch S, Schuler G, Figulla HR, Thiele H (2015) Intraaortic balloon counter-pulsation and microcirculation in cardiogenic shock complicating myocardial infarction: an IABP-SHOCK II substudy. Clin Res Cardiol 104(8):679–687PubMedCrossRef
96.
den Uil CA, Lagrand WK, van der Ent M, Jewbali LS, Brugts JJ, Spronk PE, Simoons ML (2009) The effects of intra-aortic balloon pump support on macrocirculation and tissue microcirculation in patients with cardiogenic shock. Cardiology 114(1):42–46CrossRef
97.
Hilty MP, Pichler J, Ergin B, Hefti U, Merz TM, Ince C, Maggiorini M (2017) Assessment of endothelial cell function and physiological microcirculatory reserve by video microscopy using a topical acetylcholine and nitroglycerin challenge. Intensive Care Med Exp 5(1):26PubMedPubMedCentralCrossRef
98.
Ellis CG, Ellsworth ML, Pittman RN, Burges WL (1992) Application of image analysis for evaluation of red blood cell dynamics in capillaries. Microvasc Res 44:214–225PubMedCrossRef
99.
DeGeorge BR, Olenczak JB, Cottler PS, Drake DB, Lin KY, Morgan RF, Campbell CA (2016) Evaluation of sidestream darkfield microscopy for real-time imaging acellular dermal matrix revascularization. Ann Plast Surg 76(Suppl 4):S255–S259PubMedCrossRef
100.
Weber MA, Diedrich CM, Ince C, Roovers JP (2016) Focal depth measurements of the vaginal wall: a new method to noninvasively quantify vaginal wall thickness in the diagnosis and treatment of vaginal atrophy. Menopause 23(8):833–838PubMedCrossRef
101.
Keenan S, Guyatt G, Sibbald W, Cook D, Heyland D, Jaeschke D (1999) How to use articles about diagnostic technology: gastric tonometry. Crit Care Med 27(9):1726–1731PubMedCrossRef
102.
Desjardins C, Duling BR (1987) Microvessel hematocrit: measurement and implications for capillary oxygen transport. Am J Physiol 252:H494–H503PubMed
103.
Boerma EC, Scheeren TWL (2017) Digging into the microcirculation: the rush for gold may excavate apples and oranges. J Clin Monit Comput 31(4):665–667PubMedCrossRef
104.
Ellis CG, Bateman RM, Sharpe MD, Sibbald WJ, Gill R (2002) Effect of a maldistribution of microvascular blood flow on capillary O2 extraction in sepsis. Am J Physiol Heart Circ Physiol 282:H156–H164PubMedCrossRef
105.
Kurata T, Li Z, Oda S, Kawahira H, Haneishi H (2015) Impact of vessel diameter and bandwidth of illumination in sidestream dark-field oximetry. Biomed Opt Express 6:1616–1631PubMedPubMedCentralCrossRef
106.
Marini JJ, Gattinoni L, Ince C, Kozek-Langenecker S, Mehta RL, Pichard C, Westphal M, Wischmeyer P, Vincent JL (2015) A few of our favorite unconfirmed ideas. Crit Care 19(Suppl 3):S1PubMedPubMedCentral
107.
Hernández G, Teboul JL (2016) Is the macrocirculation really dissociated from the microcirculation in septic shock? Intensive Care Med 42(10):1621–1624PubMedCrossRef
108.
Donati A, Tibboel D, Ince C (2013) Towards integrative physiological monitoring of the critically ill: from cardiovascular to microcirculatory and cellular function monitoring at the bedside. Crit Care 17(Suppl 1):S5PubMedPubMedCentral
109.
Brouwers MC, Kerkvliet K, Spithoff K (2016) The AGREE Reporting Checklist: a tool to improve reporting of clinical practice guidelines. Brit Med J 352:i1152PubMedPubMedCentralCrossRef
110.
Vernooij RWM, Alonso-Coello P, Brouwers M, Martínez García L, CheckUp Panel (2017) Reporting items for updated clinical guidelines: checklist for the reporting of updated guidelines (CheckUp). PLoS Med 14(1):e1002207PubMedPubMedCentralCrossRef
Metadata
Title
Second consensus on the assessment of sublingual microcirculation in critically ill patients: results from a task force of the European Society of Intensive Care Medicine
Authors
Can Ince
E. Christiaan Boerma
Maurizio Cecconi
Daniel De Backer
Nathan I. Shapiro
Jacques Duranteau
Michael R. Pinsky
Antonio Artigas
Jean-Louis Teboul
Irwin K. M. Reiss
Cesar Aldecoa
Sam D. Hutchings
Abele Donati
Marco Maggiorini
Fabio S. Taccone
Glenn Hernandez
Didier Payen
Dick Tibboel
Daniel S. Martin
Alexander Zarbock
Xavier Monnet
Arnaldo Dubin
Jan Bakker
Jean-Louis Vincent
Thomas W. L. Scheeren
On behalf of the Cardiovascular Dynamics Section of the ESICM
Publication date
01-03-2018
Publisher
Springer Berlin Heidelberg
Published in
Intensive Care Medicine / Issue 3/2018
Print ISSN: 0342-4642
Electronic ISSN: 1432-1238
DOI
https://doi.org/10.1007/s00134-018-5070-7

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