Capillary refill time variation induced by passive leg raising predicts capillary refill time response to volume expansion

Matthias Jacquet-Lagrèze, Nourredine Bouhamri, Philippe Portran, Rémi Schweizer, Florent Baudin, Marc Lilot, William Fornier, Jean-Luc Fellahi, Matthias Jacquet-Lagrèze, Nourredine Bouhamri, Philippe Portran, Rémi Schweizer, Florent Baudin, Marc Lilot, William Fornier, Jean-Luc Fellahi

Abstract

Background: A peripheral perfusion-targeted resuscitation during early septic shock has shown encouraging results. Capillary refill time, which has a prognostic value, was used. Adding accuracy and predictability on capillary refill time (CRT) measurement, if feasible, would benefit to peripheral perfusion-targeted resuscitation. We assessed whether a reduction of capillary refill time during passive leg raising (ΔCRT-PLR) predicted volume-induced peripheral perfusion improvement defined as a significant decrease of capillary refill time following volume expansion.

Methods: Thirty-four patients with acute circulatory failure were selected. Haemodynamic variables, metabolic variables (PCO2gap), and four capillary refill time measurements were recorded before and during a passive leg raising test and after a 500-mL volume expansion over 20 min. Receiver operating characteristic curves were built, and areas under the curves were calculated (ROCAUC). Confidence intervals (CI) were performed using a bootstrap analysis. We recorded mortality at day 90.

Results: The least significant change in the capillary refill time was 25% [95% CI, 18-30]. We defined CRT responders as patients showing a reduction of at least 25% of capillary refill time after volume expansion. A decrease of 27% in ΔCRT-PLR predicted peripheral perfusion improvement with a sensitivity of 87% [95% CI, 73-100] and a specificity of 100% [95% CI, 74-100]. The ROCAUC of ΔCRT-PLR was 0.94 [95% CI, 0.87-1.0]. The ROCAUC of baseline capillary refill time was 0.73 [95% CI, 0.54-0.90] and of baseline PCO2gap was 0.79 [0.61-0.93]. Capillary refill time was significantly longer in non-survivors than in survivors at day 90.

Conclusion: ΔCRT-PLR predicted peripheral perfusion response following volume expansion. This simple low-cost and non-invasive diagnostic method could be used in peripheral perfusion-targeted resuscitation protocols.

Trial registration: CPP Lyon Sud-Est II ANSM: 2014-A01034-43 Clinicaltrial.gov, NCT02248025 , registered 13th of September 2014.

Keywords: Capillary refill time; Circulatory shock; Fluid responsiveness; Microcirculation; PCO2gap; Passive leg raising; Peripheral perfusion.

Conflict of interest statement

The corresponding author has created a medtech company called DICARTECH which is developing a device to assess capillary refill time. All other authors declare that they have no competing interests.

Figures

Fig. 1
Fig. 1
Flow chart of the study. CRT, capillary refill time; ∆CRT-PLR, capillary refill time variation induced by passive leg raising; ∆CRT-PLR > 27%, positive index test defined as a decrease of capillary refill time induced by passive leg raising of at least 27%; ∆CRT-VE > 25%, CRT response defined as a decrease of capillary refill time induced by volume expansion of at least 25%; PLR, passive leg raising; VE, volume expansion
Fig. 2
Fig. 2
Scatter plot of capillary refill time variation induced by passive leg raising vs. by volume expansion. CRT, capillary refill time; PLR, passive leg raising; VE, volume expansion
Fig. 3
Fig. 3
ROC curves of CRT and ∆CRT-PLR to predict CRT response to volume expansion. CRT, capillary refill time; CRT responders, response to volume expansion defined as patients showing a decrease in CRT after VE of at least 25%; PCO2gap, central venous-to-arterial carbon dioxide difference; PLR, passive leg raising; VE, volume expansion

References

    1. Cecconi Maurizio, De Backer Daniel, Antonelli Massimo, Beale Richard, Bakker Jan, Hofer Christoph, Jaeschke Roman, Mebazaa Alexandre, Pinsky Michael R., Teboul Jean Louis, Vincent Jean Louis, Rhodes Andrew. Consensus on circulatory shock and hemodynamic monitoring. Task force of the European Society of Intensive Care Medicine. Intensive Care Medicine. 2014;40(12):1795–1815. doi: 10.1007/s00134-014-3525-z.
    1. Rhodes A, Evans LE, Alhazzani W, Levy MM, Antonelli M, Ferrer R, et al. Surviving Sepsis Campaign: international guidelines for management of sepsis and septic shock. Crit Care Med. 2017;1.
    1. De Backer D, Creteur J, Preiser J, Dubois M, Vincent J. Microvascular blood flow is altered in patients with sepsis. Am J Respir Crit Care Med. 2002;166:98–104. doi: 10.1164/rccm.200109-016OC.
    1. Garcia-Alvarez M, Marik P, Bellomo R. Sepsis-associated hyperlactatemia. Crit Care. 2014;18:503. doi: 10.1186/s13054-014-0503-3.
    1. Brunauer A, Koköfer A, Bataar O, Gradwohl-Matis I, Dankl D, Bakker J, et al. Changes in peripheral perfusion relate to visceral organ perfusion in early septic shock: a pilot study. J Crit Care. 2016;35:105–109. doi: 10.1016/j.jcrc.2016.05.007.
    1. Pickard A, Karlen W, Ansermino JM. Capillary refill time: is it still a useful clinical sign? Anesth Analg. 2011;113:120–123. doi: 10.1213/ANE.0b013e31821569f9.
    1. Ait-Oufella H., Bige N., Boelle P. Y., Pichereau C., Alves M., Bertinchamp R., Baudel J. L., Galbois A., Maury E., Guidet B. Capillary refill time exploration during septic shock. Intensive Care Medicine. 2014;40(7):958–964. doi: 10.1007/s00134-014-3326-4.
    1. Fleming Susannah, Gill Peter, Jones Caroline, Taylor James A., Van den Bruel Ann, Heneghan Carl, Roberts Nia, Thompson Matthew. The Diagnostic Value of Capillary Refill Time for Detecting Serious Illness in Children: A Systematic Review and Meta-Analysis. PLOS ONE. 2015;10(9):e0138155. doi: 10.1371/journal.pone.0138155.
    1. Hernandez G, Pedreros C, Veas E, Bruhn A, Romero C, Rovegno M, et al. Evolution of peripheral vs metabolic perfusion parameters during septic shock resuscitation. A clinical-physiologic study. J Crit Care. 2012;27:283–288. doi: 10.1016/j.jcrc.2011.05.024.
    1. de Moura Edmilson Bastos, Amorim Fábio Ferreira, da Cruz Santana Alfredo Nicodemos, Kanhouche Gabriel, de Souza Godoy Lucas Garcia, de Jesus Almeida Lucila, Rodrigues Thais Almeida, da Silveira Carlos Darwin Gomes, de Oliveira Maia Marcelo. Skin mottling score as a predictor of 28-day mortality in patients with septic shock. Intensive Care Medicine. 2016;42(3):479–480. doi: 10.1007/s00134-015-4184-4.
    1. Ait-Oufella H, Lemoinne S, Boelle PY, Galbois A, Baudel JL, Lemant J, et al. Mottling score predicts survival in septic shock. Intensive Care Med. 2011;37:801–807. doi: 10.1007/s00134-011-2163-y.
    1. Hernandez G, Bruhn A, Castro R, Regueira T. The holistic view on perfusion monitoring in septic shock. Curr Opin Crit Care. 2012.
    1. Dünser MW, Takala J, Brunauer A, Bakker J. Re-thinking resuscitation: leaving blood pressure cosmetics behind and moving forward to permissive hypotension and a tissue perfusion-based approach. Crit Care. 2013;17:326. doi: 10.1186/cc12727.
    1. van Genderen ME, Engels N, van der Valk RJP, Lima A, Klijn E, Bakker J, et al. Early peripheral perfusion-guided fluid therapy in patients with septic shock. Am J Respir Crit Care Med. 2015;191:477–480. doi: 10.1164/rccm.201408-1575LE.
    1. Hernández G, Ospina-Tascón GA, Damiani LP, Estenssoro E, Dubin A, Hurtado J, et al. Effect of a resuscitation strategy targeting peripheral perfusion status vs serum lactate levels on 28-day mortality among patients with septic shock: the ANDROMEDA-SHOCK randomized clinical trial. JAMA. 2019;321:654–664. doi: 10.1001/jama.2019.0071.
    1. Pranskunas Andrius, Koopmans Matty, Koetsier Peter M., Pilvinis Vidas, Boerma E. Christiaan. Microcirculatory blood flow as a tool to select ICU patients eligible for fluid therapy. Intensive Care Medicine. 2012;39(4):612–619. doi: 10.1007/s00134-012-2793-8.
    1. Monnet X, Marik P, Teboul J-L. Passive leg raising for predicting fluid responsiveness: a systematic review and meta-analysis. Intensive Care Med. 2016.
    1. Pottecher J, Deruddre S, Teboul J-L, Georger J-F, Laplace C, Benhamou D, et al. Both passive leg raising and intravascular volume expansion improve sublingual microcirculatory perfusion in severe sepsis and septic shock patients. Intensive Care Med. 2010;36:1867–1874. doi: 10.1007/s00134-010-1966-6.
    1. Pettilä V, Merz T, Wilkman E, Perner A, Karlsson S, Lange T, et al. Targeted tissue perfusion versus macrocirculation-guided standard care in patients with septic shock (TARTARE-2S): study protocol and statistical analysis plan for a randomized controlled trial. Trials. 2016;17:384. doi: 10.1186/s13063-016-1515-x.
    1. Bossuyt PM, Reitsma JB, Bruns DE, Gatsonis CA, Glasziou PP, Irwig L, et al. STARD 2015: an updated list of essential items for reporting diagnostic accuracy studies. BMJ. 2015:h5527.
    1. Vincent JL, Moreno R, Takala J, Willatts S, De Mendonça 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;22:707–710. doi: 10.1007/BF01709751.
    1. Le Gall JR, Lemeshow S, Saulnier F. A new Simplified Acute Physiology Score (SAPS II) based on a European/North American multicenter study. JAMA. 1993;270:2957–2963. doi: 10.1001/jama.1993.03510240069035.
    1. Monnet X, Teboul J-L. Passive leg raising: five rules, not a drop of fluid! Crit Care Lond Engl. 2015;19:18. doi: 10.1186/s13054-014-0708-5.
    1. Obuchowski NA. Sample size calculations in studies of test accuracy. Stat Methods Med Res. 1998;7:371–392. doi: 10.1177/096228029800700405.
    1. Brown LH, Prasad NH, Whitley TW. Adverse lighting condition effects on the assessment of capillary refill. Am J Emerg Med. 1994;12:46–47. doi: 10.1016/0735-6757(94)90196-1.
    1. Anderson B, Kelly A-M, Kerr D, Clooney M, Jolley D. Impact of patient and environmental factors on capillary refill time in adults. Am J Emerg Med. 2008;26:62–65. doi: 10.1016/j.ajem.2007.06.026.
    1. Schriger DL, Baraff L. Defining normal capillary refill: variation with age, sex, and temperature. Ann Emerg Med. 1988;17:932–935. doi: 10.1016/S0196-0644(88)80675-9.
    1. Monnet Xavier, Persichini Romain, Ktari Mariem, Jozwiak Mathieu, Richard Christian, Teboul Jean-Louis. Precision of the transpulmonary thermodilution measurements. Critical Care. 2011;15(4):R204. doi: 10.1186/cc10421.
    1. Jacquet-Lagrèze M, Izaute G, Fellahi J-L. Diagnostic accuracy studies: the methodologic approach matters! Anesthesiology. 2017;127:728–729. doi: 10.1097/ALN.0000000000001824.
    1. Maitland K, Pamba A, Newton CRJC, Levin M. Response to volume resuscitation in children with severe malaria. Pediatr Crit Care Med. 2003;4:426–431. doi: 10.1097/01.PCC.0000090293.32810.4E.
    1. De Backer D, Ortiz JA, Salgado D. Coupling microcirculation to systemic hemodynamics. Curr Opin Crit Care. 2010;16:250–4.
    1. 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.
    1. García MIM, Romero MG, Cano AG, Aya HD, Rhodes A, Grounds RM, et al. Dynamic arterial elastance as a predictor of arterial pressure response to fluid administration: a validation study. Crit Care. 2014;18:626.
    1. Guérin L, Teboul J-L, Persichini R, Dres M, Richard C, Monnet X. Effects of passive leg raising and volume expansion on mean systemic pressure and venous return in shock in humans. Crit Care. 2015;19.
    1. Klijn Eva, Niehof Sjoerd, Johan Groeneveld A. B., Lima Alexandre Pinto, Bakker Jan, van Bommel Jasper. Postural change in volunteers: sympathetic tone determines microvascular response to cardiac preload and output increases. Clinical Autonomic Research. 2015;25(6):347–354. doi: 10.1007/s10286-015-0286-x.
    1. Mallat J, Lazkani A, Lemyze M, Pepy F, Meddour M, Gasan G, et al. Repeatability of blood gas parameters, PCO2 gap, and PCO2 gap to arterial-to-venous oxygen content difference in critically ill adult patients. Medicine (Baltimore). 2015;94.
    1. Blaxter L L, Morris D E, Crowe J A, Henry C, Hill S, Sharkey D, Vyas H, Hayes-Gill B R. An automated quasi-continuous capillary refill timing device. Physiological Measurement. 2015;37(1):83–99. doi: 10.1088/0967-3334/37/1/83.

Source: PubMed

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