Skip to main content
Key Specialties
Cardiology Diabetology Endocrinology Gastroenterology Geriatrics and Gerontology Gynecology and Obstetrics Hematology Infectious Disease Internal Medicine Nephrology Neurology Oncology Pediatrics Respiratory Medicine Rheumatology Surgery
Congress Coverage
2024 ACC Congress 2023 ESMO Congress 2023 EASD Congress 2023 ERS Congress 2023 ESC Congress 2023 EHA Congress 2023 ASCO Annual Meeting
Clinical Collections
Advances in Alzheimer’s

At a glance: The ONWARDS insulin icodec trials

A round-up of the ONWARDS phase 3 clinical trials evaluating the novel weekly insulin icodec in people with diabetes.
ADVANCED SEARCH
Log in
Top
Annals of Intensive Care
Published in: Annals of Intensive Care 1/2019

Open Access 01-12-2019 | Septicemia | Review

Narrative review: clinical assessment of peripheral tissue perfusion in septic shock

Authors: Geoffroy Hariri, Jérémie Joffre, Guillaume Leblanc, Michael Bonsey, Jean-Remi Lavillegrand, Tomas Urbina, Bertrand Guidet, Eric Maury, Jan Bakker, Hafid Ait-Oufella

Published in: Annals of Intensive Care | Issue 1/2019

Login to get access

Abstract

Sepsis is one of the main reasons for intensive care unit admission and is responsible for high morbidity and mortality. The usual hemodynamic targets for resuscitation of patients with septic shock use macro-hemodynamic parameters (hearth rate, mean arterial pressure, central venous pressure). However, persistent alterations of microcirculatory blood flow despite restoration of macro-hemodynamic parameters can lead to organ failure. This dissociation between macro- and microcirculatory compartments brings a need to assess end organs tissue perfusion in patients with septic shock. Traditional markers of tissue perfusion may not be readily available (lactate) or may take time to assess (urine output). The skin, an easily accessible organ, allows clinicians to quickly evaluate the peripheral tissue perfusion with noninvasive bedside parameters such as the skin temperatures gradient, the capillary refill time, the extent of mottling and the peripheral perfusion index.
Literature
1.
Rhee C, Dantes R, Epstein L, Murphy DJ, Seymour CW, Iwashyna TJ, et al. Incidence and trends of sepsis in US hospitals using clinical vs claims data, 2009–2014. JAMA. 2017;318(13):1241–9.PubMedPubMedCentral
2.
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(3):791–9.PubMed
3.
De Backer D, Creteur J, Dubois MJ, Sakr Y, Koch M, Verdant C, et al. The effects of dobutamine on microcirculatory alterations in patients with septic shock are independent of its systemic effects. Crit Care Med. 2006;34(2):403–8.PubMed
4.
Hernandez G, Bruhn A, Luengo C, Regueira T, Kattan E, Fuentealba A, et al. Effects of dobutamine on systemic, regional and microcirculatory perfusion parameters in septic shock: a randomized, placebo-controlled, double-blind, crossover study. Intensive Care Med. 2013;39(8):1435–43.PubMed
5.
Dubin A, Pozo MO, Casabella CA, Palizas F Jr, Murias G, Moseinco MC, et al. Increasing arterial blood pressure with norepinephrine does not improve microcirculatory blood flow: a prospective study. Crit Care. 2009;13(3):R92.PubMedPubMedCentral
6.
Thooft A, Favory R, Salgado DR, Taccone FS, Donadello K, De Backer D, et al. Effects of changes in arterial pressure on organ perfusion during septic shock. Crit Care. 2011;15(5):R222.PubMedPubMedCentral
7.
8.
Lima A, Bakker J. Noninvasive monitoring of peripheral perfusion. Intensive Care Med. 2005;31(10):1316–26.PubMed
9.
Ait-Oufella H, Bourcier S, Alves M, Galbois A, Baudel JL, Margetis D, et al. Alteration of skin perfusion in mottling area during septic shock. Ann Intensive Care. 2013;3(1):31.PubMedPubMedCentral
10.
Ait-Oufella H, Bourcier S, Lehoux S, Guidet B. Microcirculatory disorders during septic shock. Curr Opin Crit Care. 2015;21(4):271–5.PubMed
11.
Bourcier S, Joffre J, Dubee V, Preda G, Baudel JL, Bige N, et al. Marked regional endothelial dysfunction in mottled skin area in patients with severe infections. Crit Care. 2017;21(1):155.PubMedPubMedCentral
12.
Becker L, Prado K, Foppa M, Martinelli N, Aguiar C, Furian T, et al. Endothelial dysfunction assessed by brachial artery ultrasound in severe sepsis and septic shock. J Crit Care. 2012;27(3):316e9–14.
13.
Ait-Oufella H, Maury E, Lehoux S, Guidet B, Offenstadt G. The endothelium: physiological functions and role in microcirculatory failure during severe sepsis. Intensive Care Med. 2010;36(8):1286–98.PubMed
14.
Ait-Oufella H, Bakker J. Understanding clinical signs of poor tissue perfusion during septic shock. Intensive Care Med. 2016;42(12):2070–2.PubMed
15.
Lima A, Bakker J. Clinical assessment of peripheral circulation. Curr Opin Crit Care. 2015;21(3):226–31.PubMed
16.
Cecconi M, De Backer D, Antonelli M, Beale R, Bakker J, Hofer C, et al. Consensus on circulatory shock and hemodynamic monitoring. Task force of the European Society of Intensive Care Medicine. Intensive Care Med. 2014;40(12):1795–815.PubMedPubMedCentral
17.
18.
19.
Thompson MJ, Ninis N, Perera R, Mayon-White R, Phillips C, Bailey L, et al. Clinical recognition of meningococcal disease in children and adolescents. Lancet. 2006;367(9508):397–403.PubMed
20.
Kaplan LJ, McPartland K, Santora TA, Trooskin SZ. Start with a subjective assessment of skin temperature to identify hypoperfusion in intensive care unit patients. J Trauma. 2001;50(4):620–7 (discussion 7–8).PubMed
21.
Lima A, Jansen TC, van Bommel J, Ince C, Bakker J. The prognostic value of the subjective assessment of peripheral perfusion in critically ill patients. Crit Care Med. 2009;37(3):934–8.PubMed
22.
Joly HR, Weil MH. Temperature of the great toe as an indication of the severity of shock. Circulation. 1969;39(1):131–8.PubMed
23.
Ibsen B. Treatment of shock with vasodilators measuring skin temperature on the big toe. Ten years’ experience in 150 cases. Dis Chest. 1967;52(4):425–9.PubMed
24.
House JR, Tipton MJ. Using skin temperature gradients or skin heat flux measurements to determine thresholds of vasoconstriction and vasodilatation. Eur J Appl Physiol. 2002;88(1–2):141–5.PubMed
25.
Bailey JM, Levy JH, Kopel MA, Tobia V, Grabenkort WR. Relationship between clinical evaluation of peripheral perfusion and global hemodynamics in adults after cardiac surgery. Crit Care Med. 1990;18(12):1353–6.PubMed
26.
Vincent JL, Moraine JJ, van der Linden P. Toe temperature versus transcutaneous oxygen tension monitoring during acute circulatory failure. Intensive Care Med. 1988;14(1):64–8.PubMed
27.
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(3):283–8.PubMed
28.
Bourcier S, Pichereau C, Boelle PY, Nemlaghi S, Dubee V, Lejour G, et al. Toe-to-room temperature gradient correlates with tissue perfusion and predicts outcome in selected critically ill patients with severe infections. Ann Intensive Care. 2016;6(1):63.PubMedPubMedCentral
29.
Tibby SM, Hatherill M, Murdoch IA. Capillary refill and core-peripheral temperature gap as indicators of haemodynamic status in paediatric intensive care patients. Arch Dis Child. 1999;80(2):163–6.PubMedPubMedCentral
30.
Gorelick MH, Shaw KN, Murphy KO. Validity and reliability of clinical signs in the diagnosis of dehydration in children. Pediatrics. 1997;99(5):E6.PubMed
31.
Evans JA, May J, Ansong D, Antwi S, Asafo-Adjei E, Nguah SB, et al. Capillary refill time as an independent prognostic indicator in severe and complicated malaria. J Pediatr. 2006;149(5):676–81.PubMed
32.
Gove S, Tamburlini G, Molyneux E, Whitesell P, Campbell H. Development and technical basis of simplified guidelines for emergency triage assessment and treatment in developing countries. WHO Integrated Management of Childhood Illness (IMCI) Referral Care Project. Arch Dis Child. 1999;81(6):473–7.PubMedPubMedCentral
33.
Alsma J, van Saase J, Nanayakkara PWB, Schouten W, Baten A, Bauer MP, et al. The power of flash mob research: conducting a nationwide observational clinical study on capillary refill time in a single day. Chest. 2017;151(5):1106–13.PubMed
34.
van Genderen ME, Paauwe J, de Jonge J, van der Valk RJ, Lima A, Bakker J, et al. Clinical assessment of peripheral perfusion to predict postoperative complications after major abdominal surgery early: a prospective observational study in adults. Crit Care. 2014;18(3):R114.PubMedPubMedCentral
35.
Ait-Oufella H, Bige N, Boelle PY, Pichereau C, Alves M, Bertinchamp R, et al. Capillary refill time exploration during septic shock. Intensive Care Med. 2014;40(7):958–64.PubMed
36.
Brunauer A, Kokofer 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;35:105–9.PubMed
37.
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(5):801–7.PubMed
38.
Galbois A, Bige N, Pichereau C, Boelle PY, Baudel JL, Bourcier S, et al. Exploration of skin perfusion in cirrhotic patients with septic shock. J Hepatol. 2015;62(3):549–55.
39.
de Moura EB, Amorim FF, da Cruz Santana AN, Kanhouche G, de Souza Godoy LG, de Jesus Almeida L, et al. Skin mottling score as a predictor of 28-day mortality in patients with septic shock. Intensive Care Med. 2016;42(3):479–80.PubMed
40.
Coudroy R, Jamet A, Frat JP, Veinstein A, Chatellier D, Goudet V, et al. Incidence and impact of skin mottling over the knee and its duration on outcome in critically ill patients. Intensive Care Med. 2015;41(3):452–9.PubMed
41.
Preda G, Bourcier S, Joffre J, Boelle PY, Dubee V, Baudel JL, et al. Mottling score is associated with 28-day mortality in critically ill patients with sepsis. Minerva Anestesiol. 2017;83(6):664–6.PubMed
42.
Hales JR, Stephens FR, Fawcett AA, Daniel K, Sheahan J, Westerman RA, et al. Observations on a new non-invasive monitor of skin blood flow. Clin Exp Pharmacol Physiol. 1989;16(5):403–15.PubMed
43.
van Genderen ME, Bartels SA, Lima A, Bezemer R, Ince C, Bakker J, et al. Peripheral perfusion index as an early predictor for central hypovolemia in awake healthy volunteers. Anesth Analg. 2013;116(2):351–6.PubMed
44.
Oskay A, Eray O, Dinc SE, Aydin AG, Eken C. Prognosis of Critically ill patients in the ED and value of perfusion index measurement: a cross-sectional study. Am J Emerg Med. 2015;33(8):1042–4.PubMed
45.
He HW, Liu DW, Long Y, Wang XT. The peripheral perfusion index and transcutaneous oxygen challenge test are predictive of mortality in septic patients after resuscitation. Crit Care. 2013;17(3):R116.PubMedPubMedCentral
46.
Hernandez G, Luengo C, Bruhn A, Kattan E, Friedman G, Ospina-Tascon GA, et al. When to stop septic shock resuscitation: clues from a dynamic perfusion monitoring. Ann Intensive Care. 2014;4:30.PubMedPubMedCentral
47.
Lara B, Enberg L, Ortega M, Leon P, Kripper C, Aguilera P, et al. Capillary refill time during fluid resuscitation in patients with sepsis-related hyperlactatemia at the emergency department is related to mortality. PLoS ONE. 2017;12(11):e0188548.PubMedPubMedCentral
48.
Hernandez G, Cavalcanti AB, Ospina-Tascon G, Zampieri FG, Dubin A, Hurtado FJ, et al. Early goal-directed therapy using a physiological holistic view: the ANDROMEDA-SHOCK—a randomized controlled trial. Ann Intensive Care. 2018;8(1):52.PubMedPubMedCentral
49.
van Genderen ME, Engels N, van der Valk RJ, 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(4):477–80.PubMed
50.
Misango D, Pattnaik R, Baker T, Dunser MW, Dondorp AM, Schultz MJ, et al. Haemodynamic assessment and support in sepsis and septic shock in resource-limited settings. Trans R Soc Trop Med Hyg. 2017;111(11):483–9.PubMed
51.
Lavillegrand JR, Dumas G, Bige N, Zafimahazo D, Guidet B, Maury E, et al. Should we treat mild hypotension in septic patients in the absence of peripheral tissue hypoperfusion? Intensive Care Med. 2018;44(9):1593–4.PubMed
52.
Boerma EC, Koopmans M, Konijn A, Kaiferova K, Bakker AJ, van Roon EN, et al. Effects of nitroglycerin on sublingual microcirculatory blood flow in patients with severe sepsis/septic shock after a strict resuscitation protocol: a double-blind randomized placebo controlled trial. Crit Care Med. 2010;38(1):93–100.PubMed
53.
Lima A, van Genderen ME, van Bommel J, Klijn E, Jansem T, Bakker J. Nitroglycerin reverts clinical manifestations of poor peripheral perfusion in patients with circulatory shock. Crit Care. 2014;18(3):R126.PubMedPubMedCentral
54.
Depret F, Sitbon A, Soussi S, De Tymowski C, Blet A, Fratani A, et al. Intravenous iloprost to recruit the microcirculation in septic shock patients? Intensive Care Med. 2018;44(1):121–2.PubMed
55.
Legrand M, Ait-Oufella H, Ince C. Could resuscitation be based on microcirculation data? Yes. Intensive Care Med. 2018;44(6):944–6.PubMed
56.
Hernandez G, Ospina-Tascon 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(7):654–64.PubMed
Metadata
Title
Narrative review: clinical assessment of peripheral tissue perfusion in septic shock
Authors
Geoffroy Hariri
Jérémie Joffre
Guillaume Leblanc
Michael Bonsey
Jean-Remi Lavillegrand
Tomas Urbina
Bertrand Guidet
Eric Maury
Jan Bakker
Hafid Ait-Oufella
Publication date
01-12-2019
Publisher
Springer International Publishing
Published in
Annals of Intensive Care / Issue 1/2019
Electronic ISSN: 2110-5820
DOI
https://doi.org/10.1186/s13613-019-0511-1

Other articles of this Issue 1/2019

Annals of Intensive Care 1/2019 Go to the issue

Letter to the Editor

Comparing video and direct laryngoscopy for tracheal intubation in the general ward

Research

A multiplex analysis of sepsis mediators during human septic shock: a preliminary study on myocardial depression and organ failures

Review

Diagnosis and management of metabolic acidosis: guidelines from a French expert panel

Correction

Correction to: Recruiting the microcirculation in septic shock

Review

Withholding and withdrawing life-support in adults in emergency care: joint position paper from the French Intensive Care Society and French Society of Emergency Medicine

Editorial

Lung recruitment: What has computed tomography taught us in the last decade?