Microcirculatory perfusion disturbances in septic shock: results from the ProCESS trial

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Abstract

Background

We sought to determine the effects of alternative resuscitation strategies on microcirculatory perfusion and examine any association between microcirculatory perfusion and mortality in sepsis.

Methods

This was a prospective, formally designed substudy of participants in the Protocolized Care in Early Septic Shock (ProCESS) trial. We recruited from six sites with the equipment and training to perform these study procedures. All subjects were adults with septic shock, and each was assigned to alternative resuscitation strategies. The two main analyses assessed (1) the impact of resuscitation strategies on microcirculatory perfusion parameters and (2) the association of microcirculatory perfusion with 60-day in-hospital mortality. We measured sublingual microcirculatory perfusion using sidestream dark field in vivo video microscopy at the completion of the 6-h ProCESS resuscitation protocol and then again at 24 and 72 h.

Results

We enrolled 207 subjects (demographics were similar to the overall ProCESS cohort) and observed 40 (19.3%) deaths. There were no differences in average perfusion characteristics between treatment arms. Analyzing the relationship between microcirculatory perfusion and mortality, we found an association between vascular density parameters and mortality. Total vascular density (beta = 0.006, p < 0.003), perfused vascular density (beta = 0.005, p < 0.04), and De Backer score (beta = 0.009, p < 0.01) were higher overall in survivors in a generalized estimating equation model, and this association was significant at the 72-h time point ( p < 0.05 for each parameter).

Conclusions

Microcirculatory perfusion did not differ between three early septic shock treatment arms. We found an association between microcirculatory perfusion parameters of vascular density at 72 h and mortality.

Trial registration

ClinicalTrials.gov, NCT00510835. Registered on August 2, 2007.

Electronic supplementary material

The online version of this article (10.1186/s13054-018-2240-5) contains supplementary material, which is available to authorized users.

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Most cited references 14

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American College of Chest Physicians/Society of Critical Care Medicine Consensus Conference

(1992)

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The microcirculation is the motor of sepsis

Can Ince (2005)

Regional tissue distress caused by microcirculatory dysfunction and mitochondrial depression underlies the condition in sepsis and shock where, despite correction of systemic oxygen delivery variables, regional hypoxia and oxygen extraction deficit persist. We have termed this condition microcirculatory and mitochondrial distress syndrome (MMDS). Orthogonal polarization spectral imaging allowed the first clinical observation of the microcirculation in human internal organs, and has identified the pivotal role of microcirculatory abnormalities in defining the severity of sepsis, a condition not revealed by systemic hemodynamic or oxygen-derived variables. Recently, sublingual sidestream dark-field (SDF) imaging has been introduced, allowing observation of the microcirculation in even greater detail. Microcirculatory recruitment is needed to ensure adequate microcirculatory perfusion and the oxygenation of tissue cells that follows. In sepsis, where inflammation-induced autoregulatory dysfunction persists and oxygen need is not matched by supply, the microcirculation can be recruited by reducing pathological shunting, promoting microcirculatory perfusion, supporting pump function, and controlling hemorheology and coagulation. Resuscitation following MMDS must include focused recruitment of hypoxic-shunted microcirculatory units and/or resuscitation of the mitochondria. A combination of agents is required for successful rescue of the microcirculation. Single compounds such as activated protein C, which acts on multiple pathways, can be expected to be beneficial in rescuing the microcirculation in sepsis.

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The effects of dobutamine on microcirculatory alterations in patients with septic shock are independent of its systemic effects.

Jean-Louis Vincent, D Backer, Marc Koch … (2006)

To evaluate the effects of dobutamine on microcirculatory blood flow alterations in patients with septic shock. Prospective, open-label study. A 31-bed, medico-surgical intensive care unit of a university hospital. Twenty-two patients with septic shock. Intravenous administration of dobutamine (5 mug/kg.min) for 2 hrs (n = 22) followed by the addition of 10 M acetylcholine (topically applied, n = 10). Complete hemodynamic measurements were obtained before and after dobutamine administration. In addition, the sublingual microcirculation was investigated with an orthogonal polarization spectral imaging technique before and after dobutamine administration and after topical application of acetylcholine. Dobutamine significantly improved capillary perfusion (from 48 +/- 15 to 67 +/- 11%, p = .001), but with large individual variation, whereas capillary density remained stable. The addition of topical acetylcholine completely restored capillary perfusion (98 +/- 1%, p = .001) and capillary density. The changes in capillary perfusion during dobutamine administration were not related to changes in cardiac index (p = .45) or arterial pressure (p = .29). Interestingly, the decrease in lactate levels was proportional to the improvement in capillary perfusion (y = 0.07 - 0.02x, r = .46, p = .005) but not to changes in cardiac index (p = .55). The administration of 5 mug/kg.min dobutamine can improve but not restore capillary perfusion in patients with septic shock. These changes are independent of changes in systemic hemodynamic variables.

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Author and article information

Contributors

Michael J. Massey: mmassey@mothmop.com

Peter C. Hou: phou@partners.org

Michael Filbin: mfilbin@partners.org

Henry Wang: henry.e.wang@uth.tmc.edu

Long Ngo: lngo@bidmc.harvard.edu

David T. Huang: huangdt@ccm.upmc.edu

William C. Aird: waird@bidmc.harvard.edu

Victor Novack: vnovack@medoracle.com

Stephen Trzeciak: trzeciak-Stephen@cooperhealth.edu

Donald M. Yealy: yealydm@upmc.edu

John A. Kellum: kellum@pitt.edu

Derek C. Angus: angusdc@ccm.upmc.edu

Nathan I. Shapiro:

ORCID: http://orcid.org/0000-0003-3508-4390

(617) 754-2323 , nshapiro@bidmc.harvard.edu

: processmicroscan@list.pitt.edu

Journal

Journal ID (nlm-ta): Crit Care

Title: Critical Care

Publisher: BioMed Central (London )

ISSN (Print): 1364-8535

ISSN (Electronic): 1466-609X

Publication date (Electronic): 20 November 2018

Publication date PMC-release: 20 November 2018

Publication date Collection: 2018

Volume: 22

Electronic Location Identifier: 308

Affiliations

[1 ]ISNI 0000 0000 9011 8547, GRID grid.239395.7, Department of Emergency Medicine and Center for Vascular Biology Research, , Beth Israel Deaconess Medical Center, ; 1 Deaconess Road, CC2-W, Boston, MA 02215 USA

[2 ]ISNI 0000 0004 0378 8294, GRID grid.62560.37, Department of Emergency Medicine, , Brigham and Women’s Hospital, ; Boston, MA USA

[3 ]ISNI 0000 0004 0386 9924, GRID grid.32224.35, Department of Emergency Medicine, , Massachusetts General Hospital, ; Boston, MA USA

[4 ]ISNI 0000000106344187, GRID grid.265892.2, Department of Emergency Medicine, , University of Alabama at Birmingham, ; Birmingham, AL USA

[5 ]Division of General Medicine, Department of Medicine, Beth Isarel Deaconess Medical Center, Boston, MA USA

[6 ]ISNI 0000 0004 1936 9000, GRID grid.21925.3d, Department of Critical Care Medicine, , University of Pittsburgh School of Medicine, ; Pittsburgh, PA USA

[7 ]ISNI 0000 0000 9011 8547, GRID grid.239395.7, Division of Molecular Medicine, Department of Medicine, and Center for Vascular Biology Research, , Beth Israel Deaconess Medical Center, ; Boston, MA USA

[8 ]ISNI 0000 0004 0470 8989, GRID grid.412686.f, Clinical Research Center, , Soroka University Medical Center, ; Be’er-Sheva, Israel

[9 ]ISNI 0000 0004 0384 9827, GRID grid.411896.3, Center for Critical Care Services, , Cooper University Hospital, ; Camden, NJ USA

[10 ]ISNI 0000 0004 1936 9000, GRID grid.21925.3d, Department of Emergency Medicine, , University of Pittsburgh School of Medicine, ; Pittsburgh, PA USA

Author information

Nathan I. Shapiro http://orcid.org/0000-0003-3508-4390

Article

Publisher ID: 2240

DOI: 10.1186/s13054-018-2240-5

PMC ID: 6245723

PubMed ID: 30458880

SO-VID: 28c5e1c2-1d85-4fa8-84fb-c7b7392f8809

License:

Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

History

Date received : 5 April 2018

Date accepted : 15 October 2018

Funding

Funded by: FundRef http://dx.doi.org/10.13039/100000050, National Heart, Lung, and Blood Institute;

Award ID: R01 HL091757

Funded by: FundRef http://dx.doi.org/10.13039/100000057, National Institute of General Medical Sciences;

Award ID: P50 GM076659

Award Recipient : Derek C. Angus

Custom metadata

ScienceOpen disciplines: Emergency medicine & Trauma

Keywords: sepsis,microcirculation,pathophysiology,mortality

Data availability:

ScienceOpen disciplines: Emergency medicine & Trauma

Keywords: sepsis, microcirculation, pathophysiology, mortality

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Microcirculatory perfusion disturbances in septic shock: results from the ProCESS trial

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Abstract

Background

Methods

Results

Conclusions

Trial registration

Electronic supplementary material

Related collections

Irish Journal of Paramedicine

Most cited references 14

American College of Chest Physicians/Society of Critical Care Medicine Consensus Conference

The microcirculation is the motor of sepsis

The effects of dobutamine on microcirculatory alterations in patients with septic shock are independent of its systemic effects.

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Contributors

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Affiliations

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Cited by 40

Most referenced authors 546