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Published in: Annals of Intensive Care 1/2018

Open Access 01-12-2018 | Research

Skin microcirculatory reactivity assessed using a thermal challenge is decreased in patients with circulatory shock and associated with outcome

Authors: Diego Orbegozo, Wasineenart Mongkolpun, Gianni Stringari, Nikolaos Markou, Jacques Creteur, Jean-Louis Vincent, Daniel De Backer

Published in: Annals of Intensive Care | Issue 1/2018

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Abstract

Background

Shock states are characterized by impaired tissue perfusion and microcirculatory alterations, which are directly related to outcome. Skin perfusion can be noninvasively evaluated using skin laser Doppler (SLD), which, when coupled with a local thermal challenge, may provide a measure of microcirculatory reactivity. We hypothesized that this microvascular reactivity would be impaired in patients with circulatory shock and would be a marker of severity.

Methods

We first evaluated skin blood flow (SBF) using SLD on the forearm and on the palm in 18 healthy volunteers to select the site with maximal response. Measurements were taken at 37 °C (baseline) and repeated at 43 °C. The 43 °C/37 °C SBF ratio was calculated as a measure of microvascular reactivity. We then evaluated the SBF in 29 patients with circulatory shock admitted to a 35-bed department of intensive care and in a confirmatory cohort of 35 patients with circulatory shock.

Results

In the volunteers, baseline SBF was higher in the hand than in the forearm, but the SBF ratio was lower (11.2 [9.4–13.4] vs. 2.0 [1.7–2.6], p < 0.01) so we used the forearm for our patients. Baseline forearm SBF was similar in patients with shock and healthy volunteers, but the SBF ratio was markedly lower in the patients (2.6 [2.0–3.6] vs. 11.2 [9.4–13.4], p < 0.01). Shock survivors had a higher SBF ratio than non-survivors (3.2 [2.2–6.2] vs. 2.3 [1.7–2.8], p < 0.01). These results were confirmed in the second cohort of 35 patients. In multivariable analysis, the APACHE II score and the SBF ratio were independently associated with mortality.

Conclusions

Microcirculatory reactivity is decreased in patients with circulatory shock and has prognostic value. This simple, noninvasive test could help in monitoring the peripheral microcirculation in acutely ill patients.
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Literature
1.
go back to reference Sakr Y, Reinhart K, Vincent JL, Sprung CL, Moreno R, Ranieri VM, et al. Does dopamine administration in shock influence outcome? results of the sepsis occurrence in acutely Ill patients (SOAP) study. Crit Care Med. 2006;34:589–97.CrossRefPubMed Sakr Y, Reinhart K, Vincent JL, Sprung CL, Moreno R, Ranieri VM, et al. Does dopamine administration in shock influence outcome? results of the sepsis occurrence in acutely Ill patients (SOAP) study. Crit Care Med. 2006;34:589–97.CrossRefPubMed
2.
go back to reference De Backer D, Biston P, Devriendt J, Madl C, Chochrad D, Aldecoa C, et al. Comparison of dopamine and norepinephrine in the treatment of shock. N Engl J Med. 2010;362:779–89.CrossRefPubMed De Backer D, Biston P, Devriendt J, Madl C, Chochrad D, Aldecoa C, et al. Comparison of dopamine and norepinephrine in the treatment of shock. N Engl J Med. 2010;362:779–89.CrossRefPubMed
3.
go back to reference Weil MH, Shubin H. Proposed reclassification of shock states with special reference to distributive defects. Adv Exp Med Biol. 1971;23:13–23.CrossRefPubMed Weil MH, Shubin H. Proposed reclassification of shock states with special reference to distributive defects. Adv Exp Med Biol. 1971;23:13–23.CrossRefPubMed
5.
go back to reference Edul VS, Enrico C, Laviolle B, Vazquez AR, Ince C, Dubin A. Quantitative assessment of the microcirculation in healthy volunteers and in patients with septic shock. Crit Care Med. 2012;40:1443–8.CrossRefPubMed Edul VS, Enrico C, Laviolle B, Vazquez AR, Ince C, Dubin A. Quantitative assessment of the microcirculation in healthy volunteers and in patients with septic shock. Crit Care Med. 2012;40:1443–8.CrossRefPubMed
6.
go back to reference den Uil CA, Lagrand WK, van der Ent M, Jewbali LS, Cheng JM, Spronk PE, et al. Impaired microcirculation predicts poor outcome of patients with acute myocardial infarction complicated by cardiogenic shock. Eur Heart J. 2010;31:3032–9.CrossRef den Uil CA, Lagrand WK, van der Ent M, Jewbali LS, Cheng JM, Spronk PE, et al. Impaired microcirculation predicts poor outcome of patients with acute myocardial infarction complicated by cardiogenic shock. Eur Heart J. 2010;31:3032–9.CrossRef
7.
go back to reference De Backer D, Donadello K, Cortes DO. Monitoring the microcirculation. J Clin Monit Comput. 2012;26:361–6.CrossRefPubMed De Backer D, Donadello K, Cortes DO. Monitoring the microcirculation. J Clin Monit Comput. 2012;26:361–6.CrossRefPubMed
8.
go back to reference Lima A, Bakker J. Noninvasive monitoring of peripheral perfusion. Intensive Care Med. 2005;31:1316–26.CrossRefPubMed Lima A, Bakker J. Noninvasive monitoring of peripheral perfusion. Intensive Care Med. 2005;31:1316–26.CrossRefPubMed
9.
go back to reference De Backer D, Creteur J, Preiser JC, Dubois MJ, Vincent JL. Microvascular blood flow is altered in patients with sepsis. Am J Respir Crit Care Med. 2002;166:98–104.CrossRefPubMed De Backer D, Creteur J, Preiser JC, Dubois MJ, Vincent JL. Microvascular blood flow is altered in patients with sepsis. Am J Respir Crit Care Med. 2002;166:98–104.CrossRefPubMed
10.
go back to reference Trzeciak S, Dellinger RP, Parrillo JE, Guglielmi M, Bajaj J, Abate NL, et al. Early microcirculatory perfusion derangements in patients with severe sepsis and septic shock: relationship to hemodynamics, oxygen transport, and survival. Ann Emerg Med. 2007;49(88–98):98. Trzeciak S, Dellinger RP, Parrillo JE, Guglielmi M, Bajaj J, Abate NL, et al. Early microcirculatory perfusion derangements in patients with severe sepsis and septic shock: relationship to hemodynamics, oxygen transport, and survival. Ann Emerg Med. 2007;49(88–98):98.
11.
go back to reference De Backer D, Donadello K, Sakr Y, Ospina-Tascon G, Salgado D, Scolletta S, et al. Microcirculatory alterations in patients with severe sepsis: impact of time of assessment and relationship with outcome. Crit Care Med. 2013;41:791–9.CrossRefPubMed De Backer D, Donadello K, Sakr Y, Ospina-Tascon G, Salgado D, Scolletta S, et al. Microcirculatory alterations in patients with severe sepsis: impact of time of assessment and relationship with outcome. Crit Care Med. 2013;41:791–9.CrossRefPubMed
12.
go back to reference De Backer D, Orbegozo CD, Donadello K, Vincent JL. Pathophysiology of microcirculatory dysfunction and the pathogenesis of septic shock. Virulence. 2014;5:73–9.CrossRefPubMed De Backer D, Orbegozo CD, Donadello K, Vincent JL. Pathophysiology of microcirculatory dysfunction and the pathogenesis of septic shock. Virulence. 2014;5:73–9.CrossRefPubMed
13.
go back to reference Wright CI, Kroner CI, Draijer R. Non-invasive methods and stimuli for evaluating the skin’s microcirculation. J Pharmacol Toxicol Methods. 2006;54:1–25.CrossRefPubMed Wright CI, Kroner CI, Draijer R. Non-invasive methods and stimuli for evaluating the skin’s microcirculation. J Pharmacol Toxicol Methods. 2006;54:1–25.CrossRefPubMed
14.
go back to reference Roustit M, Blaise S, Millet C, Cracowski JL. Reproducibility and methodological issues of skin post-occlusive and thermal hyperemia assessed by single-point laser Doppler flowmetry. Microvasc Res. 2010;79:102–8.CrossRefPubMed Roustit M, Blaise S, Millet C, Cracowski JL. Reproducibility and methodological issues of skin post-occlusive and thermal hyperemia assessed by single-point laser Doppler flowmetry. Microvasc Res. 2010;79:102–8.CrossRefPubMed
15.
go back to reference Doerschug KC, Delsing AS, Schmidt GA, Haynes WG. Impairments in microvascular reactivity are related to organ failure in human sepsis. Am J Physiol Heart Circ Physiol. 2007;293:H1065–71.CrossRefPubMed Doerschug KC, Delsing AS, Schmidt GA, Haynes WG. Impairments in microvascular reactivity are related to organ failure in human sepsis. Am J Physiol Heart Circ Physiol. 2007;293:H1065–71.CrossRefPubMed
16.
go back to reference Creteur J, Carollo T, Soldati G, Buchele G, De Backer D, Vincent JL. The prognostic value of muscle StO2 in septic patients. Intensive Care Med. 2007;33:1549–56.CrossRefPubMed Creteur J, Carollo T, Soldati G, Buchele G, De Backer D, Vincent JL. The prognostic value of muscle StO2 in septic patients. Intensive Care Med. 2007;33:1549–56.CrossRefPubMed
17.
go back to reference Payen D, Luengo C, Heyer L, Resche-Rigon M, Kerever S, Damoisel C, et al. Is thenar tissue hemoglobin oxygen saturation in septic shock related to macrohemodynamic variables and outcome? Crit Care. 2009;13(Suppl 5):S6.CrossRefPubMedPubMedCentral Payen D, Luengo C, Heyer L, Resche-Rigon M, Kerever S, Damoisel C, et al. Is thenar tissue hemoglobin oxygen saturation in septic shock related to macrohemodynamic variables and outcome? Crit Care. 2009;13(Suppl 5):S6.CrossRefPubMedPubMedCentral
18.
go back to reference Gomez H, Torres A, Polanco P, Kim HK, Zenker S, Puyana JC, et al. Use of non-invasive NIRS during a vascular occlusion test to assess dynamic tissue O(2) saturation response. Intensive Care Med. 2008;34:1600–7.CrossRefPubMed Gomez H, Torres A, Polanco P, Kim HK, Zenker S, Puyana JC, et al. Use of non-invasive NIRS during a vascular occlusion test to assess dynamic tissue O(2) saturation response. Intensive Care Med. 2008;34:1600–7.CrossRefPubMed
19.
go back to reference Orbegozo Cortes D, Puflea F, De Backer D, Creteur J, Vincent JL. Near infrared spectroscopy (NIRS) to assess the effects of local ischemic preconditioning in the muscle of healthy volunteers and critically ill patients. Microvasc Res. 2015;102:25–32.CrossRefPubMed Orbegozo Cortes D, Puflea F, De Backer D, Creteur J, Vincent JL. Near infrared spectroscopy (NIRS) to assess the effects of local ischemic preconditioning in the muscle of healthy volunteers and critically ill patients. Microvasc Res. 2015;102:25–32.CrossRefPubMed
20.
go back to reference Vongsavan N, Matthews B. Some aspects of the use of laser Doppler flow meters for recording tissue blood flow. Exp Physiol. 1993;78:1–14.CrossRefPubMed Vongsavan N, Matthews B. Some aspects of the use of laser Doppler flow meters for recording tissue blood flow. Exp Physiol. 1993;78:1–14.CrossRefPubMed
21.
go back to reference Levy MM, Fink MP, Marshall JC, Abraham E, Angus D, Cook D, et al. 2001 SCCM/ESICM/ACCP/ATS/SIS international sepsis definitions conference. Crit Care Med. 2003;31:1250–6.CrossRefPubMed Levy MM, Fink MP, Marshall JC, Abraham E, Angus D, Cook D, et al. 2001 SCCM/ESICM/ACCP/ATS/SIS international sepsis definitions conference. Crit Care Med. 2003;31:1250–6.CrossRefPubMed
22.
go back to reference Knaus WA, Draper EA, Wagner DP, Zimmerman JE. APACHE II: a severity of disease classification system. Crit Care Med. 1985;13:818–29.CrossRefPubMed Knaus WA, Draper EA, Wagner DP, Zimmerman JE. APACHE II: a severity of disease classification system. Crit Care Med. 1985;13:818–29.CrossRefPubMed
23.
go back to reference Vincent JL, Moreno R, Takala J, Willatts S, De Mendonca A, Bruining H, et al. The SOFA (sepsis-related organ failure assessment) score to describe organ dysfunction/failure. On behalf of the working group on sepsis-related problems of the European society of intensive care medicine. Intensive Care Med. 1996;22:707–10.CrossRefPubMed Vincent JL, Moreno R, Takala J, Willatts S, De Mendonca A, Bruining H, et al. The SOFA (sepsis-related organ failure assessment) score to describe organ dysfunction/failure. On behalf of the working group on sepsis-related problems of the European society of intensive care medicine. Intensive Care Med. 1996;22:707–10.CrossRefPubMed
24.
go back to reference Shapiro NI, Arnold R, Sherwin R, O’Connor J, Najarro G, Singh S, et al. The association of near-infrared spectroscopy-derived tissue oxygenation measurements with sepsis syndromes, organ dysfunction and mortality in emergency department patients with sepsis. Crit Care. 2011;15:R223.CrossRefPubMedPubMedCentral Shapiro NI, Arnold R, Sherwin R, O’Connor J, Najarro G, Singh S, et al. The association of near-infrared spectroscopy-derived tissue oxygenation measurements with sepsis syndromes, organ dysfunction and mortality in emergency department patients with sepsis. Crit Care. 2011;15:R223.CrossRefPubMedPubMedCentral
25.
go back to reference Duret J, Pottecher J, Bouzat P, Brun J, Harrois A, Payen JF, et al. Skeletal muscle oxygenation in severe trauma patients during haemorrhagic shock resuscitation. Crit Care. 2015;19:141.CrossRefPubMedPubMedCentral Duret J, Pottecher J, Bouzat P, Brun J, Harrois A, Payen JF, et al. Skeletal muscle oxygenation in severe trauma patients during haemorrhagic shock resuscitation. Crit Care. 2015;19:141.CrossRefPubMedPubMedCentral
26.
go back to reference Petroni T, Harrois A, Amour J, Lebreton G, Brechot N, Tanaka S, et al. Intra-aortic balloon pump effects on macrocirculation and microcirculation in cardiogenic shock patients supported by venoarterial extracorporeal membrane oxygenation. Crit Care Med. 2014;42:2075–82.CrossRefPubMed Petroni T, Harrois A, Amour J, Lebreton G, Brechot N, Tanaka S, et al. Intra-aortic balloon pump effects on macrocirculation and microcirculation in cardiogenic shock patients supported by venoarterial extracorporeal membrane oxygenation. Crit Care Med. 2014;42:2075–82.CrossRefPubMed
27.
go back to reference Taylor WF, Johnson JM, O’Leary D, Park MK. Effect of high local temperature on reflex cutaneous vasodilation. J Appl Physiol Respir Environ Exerc Physiol. 1984;57:191–6.PubMed Taylor WF, Johnson JM, O’Leary D, Park MK. Effect of high local temperature on reflex cutaneous vasodilation. J Appl Physiol Respir Environ Exerc Physiol. 1984;57:191–6.PubMed
28.
go back to reference Minson CT, Berry LT, Joyner MJ. Nitric oxide and neurally mediated regulation of skin blood flow during local heating. J Appl Physiol. 1985;2001(91):1619–26. Minson CT, Berry LT, Joyner MJ. Nitric oxide and neurally mediated regulation of skin blood flow during local heating. J Appl Physiol. 1985;2001(91):1619–26.
29.
go back to reference Kellogg DL Jr. In vivo mechanisms of cutaneous vasodilation and vasoconstriction in humans during thermoregulatory challenges. J Appl Physiol. 1985;2006(100):1709–18. Kellogg DL Jr. In vivo mechanisms of cutaneous vasodilation and vasoconstriction in humans during thermoregulatory challenges. J Appl Physiol. 1985;2006(100):1709–18.
30.
go back to reference Kellogg DL Jr, Liu Y, Kosiba IF, O’Donnell D. Role of nitric oxide in the vascular effects of local warming of the skin in humans. J Appl Physiol. 1985;1999(86):1185–90. Kellogg DL Jr, Liu Y, Kosiba IF, O’Donnell D. Role of nitric oxide in the vascular effects of local warming of the skin in humans. J Appl Physiol. 1985;1999(86):1185–90.
31.
go back to reference Kellogg DL Jr, Zhao JL, Wu Y. Roles of nitric oxide synthase isoforms in cutaneous vasodilation induced by local warming of the skin and whole body heat stress in humans. J Appl Physiol. 1985;2009(107):1438–44. Kellogg DL Jr, Zhao JL, Wu Y. Roles of nitric oxide synthase isoforms in cutaneous vasodilation induced by local warming of the skin and whole body heat stress in humans. J Appl Physiol. 1985;2009(107):1438–44.
32.
go back to reference Vaughn MW, Kuo L, Liao JC. Effective diffusion distance of nitric oxide in the microcirculation. Am J Physiol. 1998;274:H1705–14.PubMed Vaughn MW, Kuo L, Liao JC. Effective diffusion distance of nitric oxide in the microcirculation. Am J Physiol. 1998;274:H1705–14.PubMed
33.
go back to reference Kim-Shapiro DB, Schechter AN, Gladwin MT. Unraveling the reactions of nitric oxide, nitrite, and hemoglobin in physiology and therapeutics. Arterioscler Thromb Vasc Biol. 2006;26:697–705.CrossRefPubMed Kim-Shapiro DB, Schechter AN, Gladwin MT. Unraveling the reactions of nitric oxide, nitrite, and hemoglobin in physiology and therapeutics. Arterioscler Thromb Vasc Biol. 2006;26:697–705.CrossRefPubMed
34.
go back to reference Lupp C, Baasner S, Ince C, Nocken F, Stover JF, Westphal M. Differentiated control of deranged nitric oxide metabolism: a therapeutic option in sepsis? Crit Care. 2013;17:311.CrossRefPubMedPubMedCentral Lupp C, Baasner S, Ince C, Nocken F, Stover JF, Westphal M. Differentiated control of deranged nitric oxide metabolism: a therapeutic option in sepsis? Crit Care. 2013;17:311.CrossRefPubMedPubMedCentral
37.
go back to reference Alexander JH, Reynolds HR, Stebbins AL, Dzavik V, Harrington RA, Van de Werf F, et al. Effect of tilarginine acetate in patients with acute myocardial infarction and cardiogenic shock: the TRIUMPH randomized controlled trial. JAMA. 2007;297:1657–66.CrossRefPubMed Alexander JH, Reynolds HR, Stebbins AL, Dzavik V, Harrington RA, Van de Werf F, et al. Effect of tilarginine acetate in patients with acute myocardial infarction and cardiogenic shock: the TRIUMPH randomized controlled trial. JAMA. 2007;297:1657–66.CrossRefPubMed
38.
go back to reference Engelberger RP, Pittet YK, Henry H, Delodder F, Hayoz D, Chiolero RL, et al. Acute endotoxemia inhibits microvascular nitric oxide-dependent vasodilation in humans. Shock. 2011;35:28–34.CrossRefPubMed Engelberger RP, Pittet YK, Henry H, Delodder F, Hayoz D, Chiolero RL, et al. Acute endotoxemia inhibits microvascular nitric oxide-dependent vasodilation in humans. Shock. 2011;35:28–34.CrossRefPubMed
39.
go back to reference Ninet J, Fronek A. Cutaneous postocclusive reactive hyperemia monitored by laser Doppler flux metering and skin temperature. Microvasc Res. 1985;30:125–32.CrossRefPubMed Ninet J, Fronek A. Cutaneous postocclusive reactive hyperemia monitored by laser Doppler flux metering and skin temperature. Microvasc Res. 1985;30:125–32.CrossRefPubMed
40.
go back to reference Metzler-Wilson K, Kellie LA, Tomc C, Simpson C, Sammons D, Wilson TE. Differential vasodilatory responses to local heating in facial, glabrous and hairy skin. Clin Physiol Funct Imaging. 2012;32:361–6.CrossRefPubMed Metzler-Wilson K, Kellie LA, Tomc C, Simpson C, Sammons D, Wilson TE. Differential vasodilatory responses to local heating in facial, glabrous and hairy skin. Clin Physiol Funct Imaging. 2012;32:361–6.CrossRefPubMed
41.
go back to reference Del Pozzi AT, Hodges GJ. To reheat, or to not reheat: that is the question: the efficacy of a local reheating protocol on mechanisms of cutaneous vasodilatation. Microvasc Res. 2015;97:47–54.CrossRefPubMed Del Pozzi AT, Hodges GJ. To reheat, or to not reheat: that is the question: the efficacy of a local reheating protocol on mechanisms of cutaneous vasodilatation. Microvasc Res. 2015;97:47–54.CrossRefPubMed
42.
go back to reference Roustit M, Millet C, Blaise S, Dufournet B, Cracowski JL. Excellent reproducibility of laser speckle contrast imaging to assess skin microvascular reactivity. Microvasc Res. 2010;80:505–11.CrossRefPubMed Roustit M, Millet C, Blaise S, Dufournet B, Cracowski JL. Excellent reproducibility of laser speckle contrast imaging to assess skin microvascular reactivity. Microvasc Res. 2010;80:505–11.CrossRefPubMed
43.
go back to reference Bezemer R, Klijn E, Khalilzada M, Lima A, Heger M, van Bommel J, et al. Validation of near-infrared laser speckle imaging for assessing microvascular (re)perfusion. Microvasc Res. 2010;79:139–43.CrossRefPubMed Bezemer R, Klijn E, Khalilzada M, Lima A, Heger M, van Bommel J, et al. Validation of near-infrared laser speckle imaging for assessing microvascular (re)perfusion. Microvasc Res. 2010;79:139–43.CrossRefPubMed
44.
go back to reference Pauling JD, Shipley JA, Raper S, Watson ML, Ward SG, Harris ND, et al. Comparison of infrared thermography and laser speckle contrast imaging for the dynamic assessment of digital microvascular function. Microvasc Res. 2012;83:162–7.CrossRefPubMed Pauling JD, Shipley JA, Raper S, Watson ML, Ward SG, Harris ND, et al. Comparison of infrared thermography and laser speckle contrast imaging for the dynamic assessment of digital microvascular function. Microvasc Res. 2012;83:162–7.CrossRefPubMed
Metadata
Title
Skin microcirculatory reactivity assessed using a thermal challenge is decreased in patients with circulatory shock and associated with outcome
Authors
Diego Orbegozo
Wasineenart Mongkolpun
Gianni Stringari
Nikolaos Markou
Jacques Creteur
Jean-Louis Vincent
Daniel De Backer
Publication date
01-12-2018
Publisher
Springer International Publishing
Published in
Annals of Intensive Care / Issue 1/2018
Electronic ISSN: 2110-5820
DOI
https://doi.org/10.1186/s13613-018-0393-7

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