Log in | Register

Monitoring the microcirculation in the critically ill patient: current methods and future approaches

Daniel De Backer| Gustavo Ospina-Tascon| Diamantino Salgado| Raphaël Favory| Jacques Creteur| Jean-Louis Vincent
Review
Volume 36, Issue 11 / November , 2010

Pages 1813 - 1825

Abstract

Purpose

To discuss the techniques currently available to evaluate the microcirculation in critically ill patients. In addition, the most clinically relevant microcirculatory alterations will be discussed.

Methods

Review of the literature on methods used to evaluate the microcirculation in humans and on microcirculatory alterations in critically ill patients.

Results

In experimental conditions, shock states have been shown to be associated with a decrease in perfused capillary density and an increase in the heterogeneity of microcirculatory perfusion, with non-perfused capillaries in close vicinity to perfused capillaries. Techniques used to evaluate the microcirculation in humans should take into account the heterogeneity of microvascular perfusion. Microvideoscopic techniques, such as orthogonal polarization spectral (OPS) and sidestream dark field (SDF) imaging, directly evaluate microvascular networks covered by a thin epithelium, such as the sublingual microcirculation. Laser Doppler and tissue O2 measurements satisfactorily detect global decreases in tissue perfusion but not heterogeneity of microvascular perfusion. These techniques, and in particular laser Doppler and near-infrared spectroscopy, may help to evaluate the dynamic response of the microcirculation to a stress test. In patients with severe sepsis and septic shock, the microcirculation is characterized by a decrease in capillary density and in the proportion of perfused capillaries, together with a blunted response to a vascular occlusion test.

Conclusions

The microcirculation in humans can be evaluated directly by videomicroscopy (OPS/SDF) or indirectly by vascular occlusion tests. Of note, direct videomicroscopic visualization evaluates the actual state of the microcirculation, whereas the vascular occlusion test evaluates microvascular reserve.

Keywords

References

  1. Beach JM, McGahren ED, Duling BR (1998) Capillaries and arterioles are electrically coupled in hamster cheek pouch. Am J Physiol 275:H1489–H1496
    • View reference on PubMed
  2. Haglund U, Rasmussen I (1993) Oxygenation of the gut mucosa. Br J Surg 80:955–956
    • View reference on PubMed
  3. Aird WC (2007) Phenotypic heterogeneity of the endothelium: II. Representative vascular beds. Circ Res 100:174–190
    • View reference on PubMed
  4. Collins DM, McCullough WT, Ellsworth ML (1998) Conducted vascular responses: communication across the capillary bed. Microvasc Res 56:43–53
    • View reference on PubMed
  5. Hangai-Hoger N, Nacharaju P, Manjula BN, Cabrales P, Tsai AG, Acharya SA, Intaglietta M (2006) Microvascular effects following treatment with polyethylene glycol-albumin in lipopolysaccharide-induced endotoxemia. Crit Care Med 34:108–117
    • View reference on PubMed
  6. Bateman RM, Tokunaga C, Kareco T, Dorscheid DR, Walley KR (2007) Myocardial hypoxia-inducible HIF-1α, VEGF and GLUT1 gene expression is associated with microvascular and ICAM-1 heterogeneity during endotoxemia. Am J Physiol Heart Circ Physiol 293:H448–H456
    • View reference on PubMed
  7. Farquhar I, Martin CM, Lam C, Potter R, Ellis CG, Sibbald WJ (1996) Decreased capillary density in vivo in bowel mucosa of rats with normotensive sepsis. J Surg Res 61:190–196
    • View reference on PubMed
  8. Goldman D, Bateman RM, Ellis CG (2006) Effect of decreased O2 supply on skeletal muscle oxygenation and O2 consumption during sepsis: role of heterogeneous capillary spacing and blood flow. Am J Physiol Heart Circ Physiol 290:H2277–H2285
    • View reference on PubMed
  9. Borgstrom P, Bruttig SP, Lindbom L, Intaglietta M, Arfors KE (1990) Microvascular responses in rabbit skeletal muscle after fixed volume hemorrhage. Am J Physiol 259:H190–H196
    • View reference on PubMed
  10. Kerger H, Waschke KF, Ackern KV, Tsai AG, Intaglietta M (1999) Systemic and microcirculatory effects of autologous whole blood resuscitation in severe hemorrhagic shock. Am J Physiol 276:H2035–H2043
    • View reference on PubMed
  11. Zuurbier CJ, van Iterson M, Ince C (1999) Functional heterogeneity of oxygen supply-consumption ratio in the heart. Cardiovasc Res 44:488–497
    • View reference on PubMed
  12. Stein JC, Ellis CG, Ellsworth ML (1993) Relationship between capillary and systemic venous PO2 during nonhypoxic and hypoxic ventilation. Am J Physiol 265:H537–H542
    • View reference on PubMed
  13. Humer MF, Phang PT, Friesen BP, Allards MF, Goddard CM, Walley KR (1996) Heterogeneity of gut capillary transit times and impaired gut oxygen extraction in endotoxemic pigs. J Appl Physiol 81:895–904
    • View reference on PubMed
  14. Ince C, Vink H, Wieringa PA, Giezeman M, Spaan JA (1990) Heterogeneous NADH fluorescence during post-anoxic reactive hyperemia in saline perfused rat heart. Adv Exp Med Biol 277:477–482
    • View reference on PubMed
  15. 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 282:H156–H164
  16. Goldman D, Bateman RM, Ellis CG (2004) Effect of sepsis on skeletal muscle oxygen consumption and tissue oxygenation: interpreting capillary oxygen transport data using a mathematical model. Am J Physiol Heart Circ Physiol 287:H2535–H2544
    • View reference on PubMed
  17. Rivers E, Nguyen B, Havstadt S, Ressler J, Muzzin A, Knoblich B, Peterson E, Tomlanovich M (2001) Early goal-directed therapy in the treatment of severe sepsis and septic shock. N Engl J Med 345:1368–1377
    • View reference on PubMed
  18. Joly HR, Weil MH (1969) Temperature of the great toe as an indication of the severity of shock. Circulation 39:131–138
    • View reference on PubMed
  19. Boerma EC, Kuiper MA, Kingma WP, Egbers PH, Gerritsen RT, Ince C (2008) Disparity between skin perfusion and sublingual microcirculatory alterations in severe sepsis and septic shock: a prospective observational study. Intensive Care Med 34:1294–1298
    • View reference on PubMed
  20. Lima A, Jansen TC, van Bommel J, Ince C, Bakker J (2009) The prognostic value of the subjective assessment of peripheral perfusion in critically ill patients. Crit Care Med 37:934–938
    • View reference on PubMed
  21. 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 34:403–408
    • View reference on PubMed
  22. Ospina-Tascon G, Neves AP, Occhipinti G, Donadello K, Buchele G, Simion D, Chierego M, Oliveira Silva T, Fonseca A, Vincent JL, De Backer D (2010) Effects of fluids on microvascular perfusion in patients with severe sepsis. Intensive Care Med 36:949–955
    • View reference on PubMed
  23. Marechal X, Favory R, Joulin O, Montaigne D, Hassoun S, Decoster B, Zerimech F, Neviere R (2008) Endothelial glycocalyx damage during endotoxemia coincides with microcirculatory dysfunction and vascular oxidative stress. Shock 29:572–576
    • View reference on PubMed
  24. Duranteau J, Sitbon P, Teboul JL, Vicaut E, Anguel N, Richard C, Samii K (1999) Effects of epinephrine, norepinephrine, or the combination of norepinephrine and dobutamine on gastric mucosa in septic shock. Crit Care Med 27:893–900
    • View reference on PubMed
  25. Boyle NH, Roberts PC, Ng B, Berkenstadt H, McLuckie A, Beale RJ, Mason RC (1999) Scanning laser Doppler is a useful technique to assess foot cutaneous perfusion during femoral artery cannulation. Crit Care 3:95–100
    • View reference on PubMed
  26. Altintas MA, Altintas AA, Guggenheim M, Aust MC, Niederbichler AD, Knobloch K, Vogt PM (2010) Insight in microcirculation and histomorphology during burn shock treatment using in vivo confocal-laser-scanning microscopy. J Crit Care 25:1–7
  27. Altintas MA, Altintas AA, Guggenheim M, Steiert AE, Aust MC, Niederbichler AD, Herold C, Vogt PM (2009) Insight in human skin microcirculation using in vivo reflectance-mode confocal laser scanning microscopy. J Digit Imaging. doi:10.1007/s10278-009-9219-3
    • View reference on PubMed
  28. Lamblin V, Favory R, Boulo M, Mathieu D (2006) Microcirculatory alterations induced by sedation in intensive care patients. Effects of midazolam alone and in association with sufentanil. Crit Care 10:R176
    • View reference on PubMed
  29. Fagrell B, Fronek A, Intaglietta M (1977) A microscope-television system for studying flow velocity in human skin capillaries. Am J Physiol 233:H318–H321
    • View reference on PubMed
  30. Awan ZA, Wester T, Kvernebo K (2010) Human microvascular imaging: a review of skin and tongue videomicroscopy techniques and analysing variables. Clin Physiol Funct Imaging 30:79–88
    • View reference on PubMed
  31. Sherman H, Klausner S, Cook WA (1971) Incident dark-field illumination: a new method for microcirculatory study. Angiology 22:295–303
    • View reference on PubMed
  32. Slaaf DW, Tangelder GJ, Reneman RS, Jager K, Bollinger A (1987) A versatile incident illuminator for intravital microscopy. Int J Microcirc Clin Exp 6:391–397
    • View reference on PubMed
  33. Groner W, Winkelman JW, Harris AG, Ince C, Bouma GJ, Messmer K, Nadeau RG (1999) Orthogonal polarization spectral imaging: a new method for study of the microcirculation. Nat Med 5:1209–1212
    • View reference on PubMed
  34. Goedhart P, 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. Optics Express 15:15101–15114
    • View reference on PubMed
  35. Harris AG, Sinitsina I, Messmer K (2001) Validation of OPS imaging for microvascular measurements during isovolumic hemodilution and low hematocrits. Am J Physiol Heart Circ Physiol 282:H1502–H1509
  36. Laemmel E, Tadayoni R, Sinitsina I, Boczkowski J, and Vicaut E (2000) Using orthogonal polarization spectral imaging for the experimental study of microcirculation: comparison with intravital microscopy. In: Messmer K (ed) Orthogonal polarization spectral imaging—Progress in applied microcirculation, vol 26, pp 50–60. Basel, Karger
  37. Harris AG, Sinitsina I, Messmer K (2000) The Cytoscan™ Model E-II, a new reflectance microscope for intravital microscopy: comparison with the standard fluorescence method. J Vasc Res 37:469–476
    • View reference on PubMed
  38. Mathura KR, Vollebregt KC, Boer K, De Graaff JC, Ubbink DT, Ince C (2001) Comparison of OPS imaging and conventional capillary microscopy to study the human microcirculation. J Appl Physiol 91:74–78
    • View reference on PubMed
  39. Pennings FA, Ince C, Bouma GJ (2006) Continuous real-time visualization of the human cerebral microcirculation during arteriovenous malformation surgery using orthogonal polarization spectral imaging. Neurosurgery 59:167–171
    • View reference on PubMed
  40. den Uil CA, Bezemer R, Miranda DR, Ince C, Lagrand WK, Hartman M, Bogers AJ, Spronk PE, Simoons ML (2009) Intra-operative assessment of human pulmonary alveoli in vivo using sidestream dark field imaging: a feasibility study. Med Sci Monit 15:137–141
  41. Dubin A, Edul VS, Pozo MO, Murias G, Canullan CM, Martins EF, Ferrara G, Canales HS, Laporte M, Estenssoro E, Ince C (2008) Persistent villi hypoperfusion explains intramucosal acidosis in sheep endotoxemia. Crit Care Med 36:535–542
    • View reference on PubMed
  42. Dubin A, Pozo MO, Ferrara G, Murias G, Martins E, Canullan C, Canales HS, Kanoore Edul V, Estenssoro E, Ince C (2009) Systemic and microcirculatory responses to progressive hemorrhage. Intensive Care Med 35:556–564
    • View reference on PubMed
  43. Verdant CL, De Backer D, Bruhn A, Clausi C, Su F, Wang Z, Rodriguez H, Pries AR, Vincent JL (2009) Evaluation of sublingual and gut mucosal microcirculation in sepsis: a quantitative analysis. Crit Care Med 37:2875–2881
    • View reference on PubMed
  44. Bracht H, Krejci V, Hiltebrand L, Brandt S, Sigurdsson G, Ali SZ, Takala J, Jakob SM (2008) Orthogonal polarization spectroscopy to detect mesenteric hypoperfusion. Intensive Care Med 34:1883–1890
    • View reference on PubMed
  45. Langer S, von Dobschuetz E, Harris AG, Krombach F, Messmer K (2000) Validation of the orthogonal polarization spectral imaging technique on solid organs. In: Messmer K (ed) Orthogonal polarization spectral imaging—Progress in applied microcirculation, vol 24, pp 32–46. Basel, Karger
  46. Puhl G, Schaser KD, Vollmar B, Menger MD, Settmacher U (2003) Noninvasive in vivo analysis of the human hepatic microcirculation using orthogonal polorization spectral imaging. Transplantation 75:756–761
    • View reference on PubMed
  47. Biberthaler P, Langer S, Luchting B, Khandoga A, Messmer K (2001) In vivo assessment of colon microcirculation: comparison of the new OPS imaging technique with intravital microscopy. Eur J Med Res 6:525–534
    • View reference on PubMed
  48. Tugtekin I, Radermacher P, Theisen M, Matejovic M, Stehr A, Ploner F, Matura K, Ince C, Georgieff M, Trager K (2001) Increased ileal-mucosal-arterial PCO2 gap is associated with impaired villus microcirculation in endotoxic pigs. Intensive Care Med 27:757–766
    • View reference on PubMed
  49. Lupi O, Semenovitch I, Treu C, Bouskela E (2008) Orthogonal polarization technique in the assessment of human skin microcirculation. Int J Dermatol 47:425–431
    • View reference on PubMed
  50. Genzel-Boroviczeny O, Strotgen J, Harris AG, Messmer K, Christ F (2002) Orthogonal polarization spectral imaging (OPS): a novel method to measure the microcirculation in term and preterm infants transcutaneously. Pediatr Res 51:386–391
    • View reference on PubMed
  51. Kroth J, Weidlich K, Hiedl S, Nussbaum C, Christ F, Genzel-Boroviczeny O (2008) Functional vessel density in the first month of life in preterm neonates. Pediatr Res 64:567–571
    • View reference on PubMed
  52. Schaser KD, Settmacher U, Puhl G, Zhang L, Mittlmeier T, Stover JF, Vollmar B, Menger MD, Neuhaus P, Haas NP (2003) Noninvasive analysis of conjunctival microcirculation during carotid artery surgery reveals microvascular evidence of collateral compensation and stenosis-dependent adaptation. J Vasc Surg 37:789–797
    • View reference on PubMed
  53. Lindeboom JA, Mathura KR, Harkisoen S, van den Akker HP, Ince C (2005) Effect of smoking on the gingival capillary density: assessment of gingival capillary density with orthogonal polarization spectral imaging. J Clin Periodontol 32:1208–1212
    • View reference on PubMed
  54. 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 166:98–104
    • View reference on PubMed
  55. 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 147:91–99
    • View reference on PubMed
  56. 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
    • View reference on PubMed
  57. Trzeciak S, Dellinger RP, Parrillo JE, Guglielmi M, Bajaj J, Abate NL, Arnold RC, Colilla S, Zanotti S, Hollenberg SM (2007) Early microcirculatory perfusion derangements in patients with severe sepsis and septic shock: relationship to hemodynamics, oxygen transport, and survival. Ann Emerg Med 49:88–98
    • View reference on PubMed
  58. Boerma EC, van der Voort PH, Spronk PE, Ince C (2007) Relationship between sublingual and intestinal microcirculatory perfusion in patients with abdominal sepsis. Crit Care Med 35:1055–1060
    • View reference on PubMed
  59. Dondorp AM, Ince C, Charunwatthana P, Hanson J, van Kuijen A, Faiz MA, Rahman MR, Hasan M, Bin YE, Ghose A, Ruangveerayut R, Limmathurotsakul D, Mathura K, White NJ, Day NP (2008) Direct in vivo assessment of microcirculatory dysfunction in severe falciparum malaria. J Infect Dis 197:79–84
    • View reference on PubMed
  60. 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
    • View reference on PubMed
  61. Buchele GL, Silva E, Ospina-Tascon G, Vincent JL, De Backer D (2009) Effects of hydrocortisone on microcirculatory alterations in patients with septic shock. Crit Care Med 37:1341–1347
    • View reference on PubMed
  62. Jhanji S, Lee C, Watson D, Hinds C, Pearse RM (2009) Microvascular flow and tissue oxygenation after major abdominal surgery: association with post-operative complications. Intensive Care Med 35:671–677
    • View reference on PubMed
  63. Boerma EC, Mathura KR, van der Voort PH, Spronk PE, Ince C (2005) Quantifying bedside-derived imaging of microcirculatory abnormalities in septic patients: a prospective validation study. Crit Care 9:R601–R606
    • View reference on PubMed
  64. Arnold RC, Parrillo JE, Phillip DR, 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
    • View reference on PubMed
  65. Salgado DR, Favory R, Creteur J, Vincent JL, De Backer D (2009) Automate microcirculation analysis still requires a human intervention. Intensive Care Med 35:S27 (abstract)
  66. Lindert J, Werner J, Redlin M, Kuppe H, Habazettl H, Pries AR (2002) OPS imaging of human microcirculation: a short technical report. J Vasc Res 39:368–372
    • View reference on PubMed
  67. Pinsky MR, Vincent JL (2005) Let us use the pulmonary artery catheter correctly and only when we need it. Crit Care Med 33:1119–1122
    • View reference on PubMed
  68. Podbregar M, Mozina H (2007) Skeletal muscle oxygen saturation does not estimate mixed venous oxygen saturation in patients with severe left heart failure and additional severe sepsis or septic shock. Crit Care 11:R6
    • View reference on PubMed
  69. Marik PE, Bankov A (2003) Sublingual capnometry versus traditional markers of tissue oxygenation in critically ill patients. Crit Care Med 31:818–822
    • View reference on PubMed
  70. Dyson A, Stidwill R, Taylor V, Singer M (2009) The impact of inspired oxygen concentration on tissue oxygenation during progressive haemorrhage. Intensive Care Med 35:1783–1791
    • View reference on PubMed
  71. VanderMeer TJ, Wang H, Fink MP (1995) Endotoxemia causes ileal mucosal acidosis in the absence of mucosal hypoxia in a normodynamic porcine model of septic shock. Crit Care Med 23:1217–1225
    • View reference on PubMed
  72. Dyson A, Stidwill R, Taylor V, Singer M (2007) Tissue oxygen monitoring in rodent models of shock. Am J Physiol Heart Circ Physiol 293:H526–H533
    • View reference on PubMed
  73. 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. Crit Care Med 37:1961–1966
    • View reference on PubMed
  74. Schwarz B, Hofstotter H, Salak N, Pajk W, Knotzer H, Mayr A, Labeck B, Kafka R, Ulmer H, Hasibeder W (2001) Effects of norepinephrine and phenylephrine on intestinal oxygen supply and mucosal tissue oxygen tension. Intensive Care Med 27:593–601
    • View reference on PubMed
  75. Albuszies G, Radermacher P, Vogt J, Wachter U, Weber S, Schoaff M, Georgieff M, Barth E (2005) Effect of increased cardiac output on hepatic and intestinal microcirculatory blood flow, oxygenation, and metabolism in hyperdynamic murine septic shock. Crit Care Med 33:2332–2338
    • View reference on PubMed
  76. Sakr Y, Gath V, Oishi J, Klinzing S, Simon TP, Reinhart K, Marx G (2010) Characterization of buccal microvascular response in patients with septic shock. Eur J Anaesthesiol 27:388–394
    • View reference on PubMed
  77. Vollmar B, Rüttinger D, Menger MD (1997) Monitoring of microvascular hemoglobin oxygenation in liver and skeletal muscle tissue of endotoxin-exposed rats using reflection spectrophotometry. Adv Exp Med Biol 428:397–402
  78. Temmesfeld-Wollbrück B, Szalay A, Mayer K, Olschewski H, Seeger W, Grimminger F (1998) Abnormalities of gastric mucosal oxygenation in septic shock. Am J Respir Crit Care Med 157:1586–1592
    • View reference on PubMed
  79. Jobsis FF (1977) Noninvasive, infrared monitoring of cerebral and myocardial oxygen sufficiency and circulatory parameters. Science 198:1264–1267
    • View reference on PubMed
  80. Myers DE, Anderson LD, Seifert RP, Ortner JP, Cooper CE, Beilman GJ, Mowlem JD (2005) Noninvasive method for measuring local hemoglobin oxygen saturation in tissue using wide gap second derivative near-infrared spectroscopy. J Biomed Opt 10:034017
  81. Creteur J, Carollo T, Soldati G, Buchele G, De Backer D, Vincent JL (2007) The prognostic value of muscle StO2 in septic patients. Intensive Care Med 33:1549–1556
    • View reference on PubMed
  82. Mulier KE, Skarda DE, Taylor JH, Myers DE, McGraw MK, Gallea BL, Beilman GJ (2008) Near-infrared spectroscopy in patients with severe sepsis: correlation with invasive hemodynamic measurements. Surg Infect (Larchmt) 9:515–519
  83. Gomez H, Torres A, Polanco P, Kim HK, Zenker S, Puyana JC, Pinsky MR (2008) Use of non-invasive NIRS during a vascular occlusion test to assess dynamic tissue O2 saturation response. Intensive Care Med 34:1600–1607
    • View reference on PubMed
  84. Pareznik R, Knezevic R, Voga G, Podbregar M (2006) Changes in muscle tissue oxygenation during stagnant ischemia in septic patients. Intensive Care Med 32:87–92
    • View reference on PubMed
  85. De Blasi RA, Palmisani S, Alampi D, Mercieri M, Romano R, Collini S, Pinto G (2005) Microvascular dysfunction and skeletal muscle oxygenation assessed by phase-modulation near-infrared spectroscopy in patients with septic shock. Intensive Care Med 31:1661–1668
    • View reference on PubMed
  86. Boushel R, Piantadosi CA (2000) Near-infrared spectroscopy for monitoring muscle oxygenation. Acta Physiol Scand 168:615–622
    • View reference on PubMed
  87. Levy B, Gawalkiewicz P, Vallet B, Briancon S, Nace L, Bollaert PE (2003) Gastric capnometry with air-automated tonometry predicts outcome in critically ill patients. Crit Care Med 31:474–480
    • View reference on PubMed
  88. Schlichtig R, Bowles SA (1994) Distinguishing between aerobic and anaerobic appearance of dissolved CO2 in intestine during low flow. J Appl Physiol 76:2443–2451
    • View reference on PubMed
  89. Poeze M, Solberg BC, Greve JW, Ramsay G (2005) Monitoring global volume-related hemodynamic or regional variables after initial resuscitation: what is a better predictor of outcome in critically ill septic patients? Crit Care Med 33:2494–2500
    • View reference on PubMed
  90. Creteur J, De Backer D, Vincent JL (1999) Does gastric tonometry monitor splanchnic perfusion? Crit Care Med 27:2480–2484
    • View reference on PubMed
  91. Nevière R, Mathieu D, Chagnon JL, Lebleu N, Wattel F (1996) The contrasting effects of dobutamine and dopamine on gastric mucosal perfusion in septic patients. Am J Respir Crit Care Med 154:1684–1688
    • View reference on PubMed
  92. Weil MH, Nakagawa Y, Tang W, Sato Y, Ercoli F, Finegan R, Grayman G, Bisera J (1999) Sublingual capnometry: a new noninvasive measurement for diagnosis and quantitation of severity of circulatory shock. Crit Care Med 27:1225–1229
    • View reference on PubMed
  93. Cammarata GA, Weil MH, Castillo CJ, Fries M, Wang H, Sun S, Tang W (2009) Buccal capnometry for quantitating the severity of hemorrhagic shock. Shock 31:207–211
    • View reference on PubMed
  94. Marik PE (2001) Sublingual capnography: a clinical validation study. Chest 120:923–927
    • View reference on PubMed
  95. Baron BJ, Dutton RP, Zehtabchi S, Spanfelner J, Stavile KL, Khodorkovsky B, Nagdev A, Hahn B, Scalea TM (2007) Sublingual capnometry for rapid determination of the severity of hemorrhagic shock. J Trauma 62:120–124
    • View reference on PubMed
  96. Rackow EC, O’Neil P, Astiz ME, Carpati CM (2001) Sublingual capnometry and indexes of tissue perfusion in patients with circulatory failure. Chest 120:1633–1638
    • View reference on PubMed
  97. Creteur J, De Backer D, Sakr Y, koch M, Vincent JL (2006) Sublingual capnometry tracks microcirculatory changes in septic patients. Intensive Care Med 32:516–523
    • View reference on PubMed
  98. de Boer J, Potthoff H, Mulder PO, Dofferhoff AS, van Thiel RJ, Plijter-Groendijk H, Korf J (1994) Lactate monitoring with subcutaneous microdialysis in patients with shock: a pilot study. Circ Shock 43:57–63
    • View reference on PubMed
  99. Jorgensen VL, Nielsen SL, Espersen K, Perner A (2006) Increased colorectal permeability in patients with severe sepsis and septic shock. Intensive Care Med 32:1790–1796
    • View reference on PubMed
  100. Jorgensen VL, Reiter N, Perner A (2006) Luminal concentrations of L- and D-lactate in the rectum may relate to severity of disease and outcome in septic patients. Crit Care 10:R163
    • View reference on PubMed
  101. Spanos A, Jhanji S, Vivian-Smith A, Harris T, Pearse RM (2010) Early microvascular changes in sepsis and severe sepsis. Shock 33:387–391
    • View reference on PubMed
  102. Draisma A, Bemelmans R, van der Hoeven JG, Spronk P, Pickkers P (2009) Microcirculation and vascular reactivity during endotoxemia and endotoxin tolerance in humans. Shock 31:581–585
    • View reference on PubMed
  103. Sakr Y, Dubois MJ, De Backer D, Creteur J, Vincent JL (2004) Persistant microvasculatory alterations are associated with organ failure and death in patients with septic shock. Crit Care Med 32:1825–1831
    • View reference on PubMed
  104. Trzeciak S, McCoy JV, Phillip DR, 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
    • View reference on PubMed
  105. Doerschug KC, Delsing AS, Schmidt GA, Haynes WG (2007) Impairments in microvascular reactivity are related to organ failure in human sepsis. Am J Physiol Heart Circ Physiol 293:H1065–H1071
    • View reference on PubMed
  106. Skarda DE, Mulier KE, Myers DE, Taylor JH, Beilman GJ (2007) Dynamic near-infrared spectroscopy measurements in patients with severe sepsis. Shock 27:348–353
    • View reference on PubMed
  107. den Uil CA, Caliskan K, Lagrand WK, van der Ent M, Jewbali LS, van Kuijk JP, Spronk PE, Simoons ML (2009) Dose-dependent benefit of nitroglycerin on microcirculation of patients with severe heart failure. Intensive Care Med 35:1893–1899
  108. den Uil CA, Lagrand WK, Spronk PE, van der Ent M, Jewbali LS, Brugts JJ, Ince C, Simoons ML (2009) Low-dose nitroglycerin improves microcirculation in hospitalized patients with acute heart failure. Eur J Heart Fail 11:386–390
  109. 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 114:42–46
  110. Jung C, Ferrari M, Rodiger C, Fritzenwanger M, Goebel B, Lauten A, Pfeifer R, Figulla HR (2009) Evaluation of the sublingual microcirculation in cardiogenic shock. Clin Hemorheol Microcirc 42:141–148
    • View reference on PubMed
  111. Jung C, Rodiger C, Fritzenwanger M, Schumm J, Lauten A, Figulla HR, Ferrari M (2009) Acute microflow changes after stop and restart of intra-aortic balloon pump in cardiogenic shock. Clin Res Cardiol 98:469–475
    • View reference on PubMed
  112. Jung C, Ferrari M, Gradinger R, Fritzenwanger M, Pfeifer R, Schlosser M, Poerner TC, Brehm BR, Figulla HR (2008) Evaluation of the microcirculation during extracorporeal membrane-oxygenation. Clin Hemorheol Microcirc 40:311–314
    • View reference on PubMed
  113. Pearse R, Dawson D, Fawcett J, Rhodes A, Grounds M, Bennett D (2005) Early goal directed therapy following major surgery reduces complications and duration of hospital stay. A randomized, controlled trial. Crit Care 9:R687–R693
    • View reference on PubMed
  114. Pottecher J, Deruddre S, Teboul JL, Georger J, 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. Intensive Care Med. doi:10.1007/s00134-010-1966-6
  115. Bauer A, Kofler S, Thiel M, Eifert S, Christ F (2007) Monitoring of the sublingual microcirculation in cardiac surgery using orthogonal polarization spectral imaging: preliminary results. Anesthesiology 107:939–945
    • View reference on PubMed
  116. den Uil CA, Lagrand WK, Spronk PE, van Domburg RT, Hofland J, Luthen C, Brugts JJ, van der Ent M, Simoons ML (2008) Impaired sublingual microvascular perfusion during surgery with cardiopulmonary bypass: a pilot study. J Thorac Cardiovasc Surg 136:129–134
  117. De Backer D, Dubois MJ, Schmartz D, koch M, Ducart A, Barvais L, Vincent JL (2009) Microcirculatory alterations in cardiac surgery: effects of cardiopulmonary bypass and anesthesia. Ann Thorac Surg 88:1396–1403
    • View reference on PubMed
  118. Parthasarathi K, Lipowsky HH (1999) Capillary recruitment in response to tissue hypoxia and its dependence on red blood cell deformability. Am J Physiol 277:H2145–H2157
    • View reference on PubMed
  119. Schumacker PT, Chandel N, Agusti AGN (1993) Oxygen conformance of cellular respiration in hepatocytes. Am J Physiol 265:L395–L402
    • View reference on PubMed

Sign In

Connect with ICM

Top 5 Articles Editors Picks Supplement