Skip to main content

Advertisement

SpringerLink
Log in

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

  • Conference Reports and Expert Panel
  • Published:
Intensive Care Medicine Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

References

  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):1209–1212

    Article  CAS  PubMed  Google Scholar 

  2. Mathura KR, Bouma GJ, Ince C (2001) Abnormal microcirculation in brain tumours during surgery. Lancet 358(9294):1698–1699

    Article  CAS  PubMed  Google Scholar 

  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):98–104

    Article  PubMed  Google Scholar 

  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 360:1395–1396

    Article  PubMed  Google Scholar 

  5. Ince C (2005) The microcirculation is the motor of sepsis. Crit Care 9(Suppl 4):S13–S19

    Article  PubMed  PubMed Central  Google Scholar 

  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):8–13

    Article  PubMed  Google Scholar 

  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):1443–1448

    Article  PubMed  Google Scholar 

  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):791–799

    Article  PubMed  CAS  Google Scholar 

  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):1825–1831

    Article  PubMed  Google Scholar 

  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 34:2210–2217

    Article  PubMed  PubMed Central  Google Scholar 

  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

    Google Scholar 

  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–F1140

    Article  CAS  PubMed  Google Scholar 

  13. Nilsson J, Eriksson S, Blind PJ, Rissler P, Sturesson C (2014) Microcirculation changes during liver resection—a clinical study. Microvasc Res 94:47–55

    Article  PubMed  Google Scholar 

  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):1126–1923

    Article  PubMed  Google Scholar 

  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):121–127

    Article  PubMed  Google Scholar 

  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):123–134

    Article  PubMed  Google Scholar 

  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):79–84

    Article  CAS  PubMed  Google Scholar 

  18. Khalilzada M, Dogan K, Ince C, Stam J (2011) Sublingual microvascular changes in patients with cerebral small vessel disease. Stroke 42(7):2071–2073

    Article  PubMed  Google Scholar 

  19. Dababneh L, Cikach F, Alkukhun L, Dweik RA, Tonelli AR (2014) Sublingual microcirculation in pulmonary arterial hypertension. Ann Am Thoracic Soc 11(4):504–512

    Article  Google Scholar 

  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 18:133–139

    Article  Google Scholar 

  21. Meinders AJ, Elbers P (2009) Images in clinical medicine. Leukocytosis and sublingual microvascular blood flow. N Engl J Med 360(7):e9

    Article  PubMed  Google Scholar 

  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

    Google Scholar 

  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):38–44

    Article  CAS  PubMed  Google Scholar 

  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):91–99

    Article  PubMed  Google Scholar 

  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):1433–1441

    Article  PubMed  Google Scholar 

  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 22:485–492

    Article  Google Scholar 

  27. Kuipers JW, Tiboel D, Ince C (2016) The pediatric microcirculation. Crit Care 20(1):352

    Article  Google Scholar 

  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):48–56

    Article  PubMed  Google Scholar 

  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):73–77

    Article  CAS  PubMed  Google Scholar 

  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):37–43

    Article  PubMed  Google Scholar 

  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 16:183–191

    Article  Google Scholar 

  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):374–380

    Article  PubMed  Google Scholar 

  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):993–1001

    Article  CAS  Google Scholar 

  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):1011–1018

    Article  PubMed  Google Scholar 

  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):709–715

    Article  PubMed  PubMed Central  Google Scholar 

  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):391–397

    CAS  PubMed  Google Scholar 

  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):15101–15114

    Article  CAS  PubMed  Google Scholar 

  38. Sherman H, Klausner S, Cook WA (1971) Incident dark-field illumination a new method for microcirculation study. Angiology 22:295–303

    Article  CAS  PubMed  Google Scholar 

  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 3:40

    Article  PubMed  Google Scholar 

  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):130–131

    Article  Google Scholar 

  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 16:10

    Article  PubMed  PubMed Central  Google Scholar 

  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):261–271

    Article  PubMed  Google Scholar 

  43. Massey MJ, Shapiro NI (2016) A guide to human in vivo microcirculatory flow image analysis. Crit Care 10(20):35

    Google Scholar 

  44. Ince C (2015) Hemodynamic coherence and the rationale for monitoring the microcirculation. Crit Care 19(Suppl 3):S8

    PubMed  PubMed Central  Google Scholar 

  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 39:612–619

    Article  CAS  PubMed  Google Scholar 

  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):972–981

    Article  CAS  PubMed  Google Scholar 

  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):1961–1966

    Article  CAS  Google Scholar 

  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:R9

    Article  Google Scholar 

  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):343–354

    Article  PubMed  Google Scholar 

  50. Vincent JL, Taccone FS (2016) Microvascular monitoring – Do ‘global’ markers help? Best Pract Res Clin Anaesth 30(4):399–405

    Article  Google Scholar 

  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):5311–5317

    Article  Google Scholar 

  52. Ince C, Sinaasappel M (1999) Microcirculatory oxygenation and shunting in sepsis and shock. Crit Care Med 27:1369–1377

    Article  CAS  PubMed  Google Scholar 

  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:R101

    Article  PubMed  PubMed Central  Google Scholar 

  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 40:1795–1815

    Article  PubMed  PubMed Central  Google Scholar 

  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 42:1350–1956

    Article  PubMed  Google Scholar 

  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):140–144

    Article  PubMed  Google Scholar 

  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):965–970

    Article  CAS  PubMed  Google Scholar 

  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 28:913–917

    Article  PubMed  Google Scholar 

  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 31:981–988

    Article  PubMed  Google Scholar 

  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):298–306

    Article  CAS  PubMed  Google Scholar 

  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–R606

    Article  PubMed  PubMed Central  Google Scholar 

  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 2012:102483

    PubMed  PubMed Central  Google Scholar 

  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 19:388

    Article  PubMed  PubMed Central  Google Scholar 

  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 35:1761–1766

    Article  PubMed  Google Scholar 

  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 62:123–128

    Article  PubMed  Google Scholar 

  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 20:310

    Article  PubMed  PubMed Central  Google Scholar 

  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):239–244

    Article  PubMed  Google Scholar 

  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):659–670

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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):1269–1278

    Article  PubMed  PubMed Central  Google Scholar 

  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 12:37–50

    Article  PubMed  PubMed Central  Google Scholar 

  71. Liu C, Gomez H, Narasimhan S, Dubrawski A, Pinsky MR, Zuckerbraun A (2015) Real-time visual analysis of microvascular blood flow for critical care. IEEE Conference on Computer Vision and Pattern Recognition (CVPR), pp 2217–2225. https://doi.org/10.1109/CVPR.2015.7298834

  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):669–676

    Article  PubMed  Google Scholar 

  73. Sorelli M, Ince C, Bocchi L (2017) Particle tracking for the assessment of microcirculatory perfusion. Physiol Meas 38(2):358–373

    Article  PubMed  Google Scholar 

  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):37

    Article  PubMed  PubMed Central  Google Scholar 

  75. Elbers PE, Ince C (2006) Mechanisms of critical illness: classifying microcirculatory flow abnormalities in distributive shock. Crit Care 10(4):221–299

    Article  PubMed  PubMed Central  Google Scholar 

  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):949–955

    Article  PubMed  Google Scholar 

  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):1867–1874

    Article  PubMed  Google Scholar 

  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):1–8

    Article  CAS  Google Scholar 

  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–e160

    Article  PubMed  Google Scholar 

  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):1639–1644

    Article  PubMed  Google Scholar 

  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):961–967

    Article  PubMed  Google Scholar 

  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):2452–2458

    Article  CAS  PubMed  Google Scholar 

  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):403–408

    Article  PubMed  Google Scholar 

  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):1435–1443

    Article  CAS  PubMed  Google Scholar 

  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):473–478

    Article  CAS  PubMed  Google Scholar 

  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):791–798

    Article  PubMed  CAS  Google Scholar 

  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):2075–2082

    Article  CAS  PubMed  Google Scholar 

  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):265

    Article  PubMed  PubMed Central  Google Scholar 

  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):386–391

    Article  PubMed  Google Scholar 

  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):344

    Article  PubMed  PubMed Central  Google Scholar 

  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–H975

    Article  CAS  PubMed  Google Scholar 

  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):364–370

    Article  PubMed  PubMed Central  Google Scholar 

  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):784–790

    Article  PubMed  Google Scholar 

  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):R16

    Article  Google Scholar 

  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):679–687

    Article  PubMed  Google Scholar 

  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):42–46

    Article  CAS  Google Scholar 

  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):26

    Article  PubMed  PubMed Central  Google Scholar 

  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 44:214–225

    Article  CAS  PubMed  Google Scholar 

  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–S259

    Article  CAS  PubMed  Google Scholar 

  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):833–838

    Article  PubMed  Google Scholar 

  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):1726–1731

    Article  CAS  PubMed  Google Scholar 

  102. Desjardins C, Duling BR (1987) Microvessel hematocrit: measurement and implications for capillary oxygen transport. Am J Physiol 252:H494–H503

    CAS  PubMed  Google Scholar 

  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):665–667

    Article  PubMed  Google Scholar 

  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–H164

    Article  CAS  PubMed  Google Scholar 

  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 6:1616–1631

    Article  PubMed  PubMed Central  Google Scholar 

  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):S1

    PubMed  PubMed Central  Google Scholar 

  107. Hernández G, Teboul JL (2016) Is the macrocirculation really dissociated from the microcirculation in septic shock? Intensive Care Med 42(10):1621–1624

    Article  PubMed  Google Scholar 

  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):S5

    PubMed  PubMed Central  Google Scholar 

  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:i1152

    Article  PubMed  PubMed Central  Google Scholar 

  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):e1002207

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

Many have contributed with their expertise to the formation of this paper. The authors wish to specifically thank the following persons: Marly van Assen, Sam Arend, Sam Boerma, Vanina Edul, Hernanado Gomez, Matthias Hilty, Yasin Ince, Michael Massey, Gerke Veenstra, Claudia Scorcella, Sherezade Tovar-Doncel, and ZuhreUz.

Author information

Authors and Affiliations

  1. Department of Intensive Care, Erasmus MC University Medical Center Rotterdam, ‘s-Gravendijkwal 230, 3015 CE, Rotterdam, The Netherlands

    Can Ince & Jan Bakker

  2. Department of Translational Physiology, Academic Medical Center, Amsterdam, The Netherlands

    Can Ince

  3. Department of Intensive Care, Medical Centre Leeuwarden, Leeuwarden, The Netherlands

    E. Christiaan Boerma

  4. Anaesthesia and Intensive Care, St George’s Hospital and Medical School, London, UK

    Maurizio Cecconi

  5. Department of Intensive Care, CHIREC Hospitals, Université Libre de Bruxelles, Brussels, Belgium

    Daniel De Backer

  6. Department of Emergency Medicine and Center for Vascular Biology Research, Beth Israel Deaconess Medical Center and Harvard Medical School, Boston, MA, USA

    Nathan I. Shapiro

  7. Anesthesia and Intensive Care Department, Hôpitaux Universitaires Paris-Sud, Université Paris-Sud, Hôpital De Bicêtre, Assistance Publique Hôpitaux de Paris, Le Kremlin-Bicêtre, France

    Jacques Duranteau

  8. Department of Critical Care Medicine, University of Pittsburgh, Pittsburgh, PA, USA

    Michael R. Pinsky

  9. Critical Care Center, Hospital de Sabadell, CIBER Enfermedades Respiratorias, Universidad Autónoma de Barcelona, Sabadell, Spain

    Antonio Artigas

  10. Service de Réanimation Médicale Hôpital de Bicêtre, Hôpitaux Universitaires Paris-Sud, AP-HP, Le Kremlin-Bicêtre, France

    Jean-Louis Teboul & Xavier Monnet

  11. Department of Pediatrics, Division of Neonatology, Erasmus MC-Sophia Children’s Hospital, Erasmus Medical Center, Rotterdam, The Netherlands

    Irwin K. M. Reiss

  12. Department of Anesthesiology and Surgical Critical Care, Hospital Universitario Rio Hortega, Valladolid, Spain

    Cesar Aldecoa

  13. Kings College Hospital, Denmark Hill, London, UK

    Sam D. Hutchings

  14. Anesthesia and Intensive Care Unit, Università Politecnica delle Marche, Ancona, Italy

    Abele Donati

  15. Medical Intensive Care Unit, University Hospital of Zurich, Zurich, Switzerland

    Marco Maggiorini

  16. Department of Intensive Care, Hôpital Erasme, Brussels, Belgium

    Fabio S. Taccone & Jean-Louis Vincent

  17. Departamento de Medicina Intensiva, Facultad de Medicina, Pontificia Universidad Católica de Chile, Santiago, Chile

    Glenn Hernandez & Jan Bakker

  18. Department of Anesthesiology and Critical Care, Lariboisière Hospital, University of Paris Denis Diderot 7, Paris, France

    Didier Payen

  19. Intensive Care and Department of Pediatric Surgery, Erasmus Medical Center, Sophia Children’s Hospital, Rotterdam, The Netherlands

    Dick Tibboel

  20. Intensive Care Unit, University College London, London, UK

    Daniel S. Martin

  21. Division of Surgery and Interventional Science, Royal Free Hospital, London, UK

    Daniel S. Martin

  22. Department of Anaesthesiology, Intensive Care Medicine and Pain Medicine, University Hospital Münster, Munster, Germany

    Alexander Zarbock

  23. Servicio de Terapia Intensiva, Sanatorio Otamendi y Miroli, Buenos Aires, Argentina

    Arnaldo Dubin

  24. Department of Pulmonology and Critical Care Medicine, Columbia University Medical Center, New York, USA

    Jan Bakker

  25. Department of Anesthesiology, University Medical Center Groningen, University of Groningen, Groningen, The Netherlands

    Thomas W. L. Scheeren

Authors
  1. Can Ince
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. E. Christiaan Boerma
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Maurizio Cecconi
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Daniel De Backer
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Nathan I. Shapiro
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Jacques Duranteau
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Michael R. Pinsky
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Antonio Artigas
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Jean-Louis Teboul
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Irwin K. M. Reiss
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Cesar Aldecoa
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Sam D. Hutchings
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Abele Donati
    View author publications

    You can also search for this author in PubMed Google Scholar

  14. Marco Maggiorini
    View author publications

    You can also search for this author in PubMed Google Scholar

  15. Fabio S. Taccone
    View author publications

    You can also search for this author in PubMed Google Scholar

  16. Glenn Hernandez
    View author publications

    You can also search for this author in PubMed Google Scholar

  17. Didier Payen
    View author publications

    You can also search for this author in PubMed Google Scholar

  18. Dick Tibboel
    View author publications

    You can also search for this author in PubMed Google Scholar

  19. Daniel S. Martin
    View author publications

    You can also search for this author in PubMed Google Scholar

  20. Alexander Zarbock
    View author publications

    You can also search for this author in PubMed Google Scholar

  21. Xavier Monnet
    View author publications

    You can also search for this author in PubMed Google Scholar

  22. Arnaldo Dubin
    View author publications

    You can also search for this author in PubMed Google Scholar

  23. Jan Bakker
    View author publications

    You can also search for this author in PubMed Google Scholar

  24. Jean-Louis Vincent
    View author publications

    You can also search for this author in PubMed Google Scholar

  25. Thomas W. L. Scheeren
    View author publications

    You can also search for this author in PubMed Google Scholar

Consortia

On behalf of the Cardiovascular Dynamics Section of the ESICM

Corresponding author

Correspondence to Can Ince.

Ethics declarations

Conflicts of interest

C. Ince has developed SDF imaging and is listed as inventor on related patents commercialized by MicroVision Medical (MVM) under a license from the Academic Medical Center (AMC). He has been a consultant for MVM in the past but has not been involved with this company for more than 5 years now, and hold no shares. Braedius Medical, a company owned by a relative of Dr. Ince, has developed and designed a hand-held microscope called CytoCam-IDF imaging. Dr. Ince has no financial relation with Braedius Medical of any sort, i.e., he has never owned shares or received consultancy or speaker fees from Braedius Medical. He runs an Internet site https://microcirculationacademy.org which offers services (training, courses, and analysis) related to clinical microcirculation. The other authors have no declared interest with respect to this paper.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ince, C., Boerma, E.C., Cecconi, M. et al. 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. Intensive Care Med 44, 281–299 (2018). https://doi.org/10.1007/s00134-018-5070-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00134-018-5070-7

Keywords

Search

Navigation