Endothelial damage in septic shock patients as evidenced by circulating syndecan-1, sphingosine-1-phosphate and soluble VE-cadherin: a substudy of ALBIOS

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Abstract

Background

Septic shock is characterized by breakdown of the endothelial glycocalyx and endothelial damage, contributing to fluid extravasation, organ failure and death. Albumin has shown benefit in septic shock patients. Our aims were: (1) to identify the relations between circulating levels of syndecan-1 (SYN-1), sphingosine-1-phosphate (S1P) (endothelial glycocalyx), and VE-cadherin (endothelial cell junctions), severity of the disease, and survival; (2) to evaluate the effects of albumin supplementation on endothelial dysfunction in patients with septic shock.

Methods

This was a retrospective analysis of a multicenter randomized clinical trial on albumin replacement in severe sepsis or septic shock (the Albumin Italian Outcome Sepsis Trial, ALBIOS). Concentrations of SYN-1, S1P, soluble VE-cadherin and other biomarkers were measured on days 1, 2 and 7 in 375 patients with septic shock surviving up to 7 days after randomization.

Results

Plasma concentrations of SYN-1 and VE-cadherin rose significantly over 7 days. SYN-1 and VE-cadherin were elevated in patients with organ failure, and S1P levels were lower. SYN-1 and VE-cadherin were independently associated with renal replacement therapy requirement during ICU stay, but only SYN-1 predicted its new occurrence. Both SYN-1 and S1P, but not VE-cadherin, predicted incident coagulation failure. Only SYN-1 independently predicted 90-day mortality. Albumin significantly reduced VE-cadherin, by 9.5% ( p = 0.003) at all three time points.

Conclusion

Circulating components of the endothelial glycocalyx and of the endothelial cell junctions provide insights into severity and progression of septic shock, with special focus on incident coagulation and renal failure. Albumin supplementation lowered circulating VE-cadherin consistently over time.

Clinical Trial Registration: ALBIOS ClinicalTrials.gov number NCT00707122.

Supplementary Information

The online version contains supplementary material available at 10.1186/s13054-021-03545-1.

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Most cited references 42

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Severe Sepsis and Septic Shock

Derek C Angus, Tom van der Poll (2013)

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Proteoglycan form and function: A comprehensive nomenclature of proteoglycans

Renato Iozzo, Liliana Schaefer (2015)

We provide a comprehensive classification of the proteoglycan gene families and respective protein cores. This updated nomenclature is based on three criteria: Cellular and subcellular location, overall gene/protein homology, and the utilization of specific protein modules within their respective protein cores. These three signatures were utilized to design four major classes of proteoglycans with distinct forms and functions: the intracellular, cell-surface, pericellular and extracellular proteoglycans. The proposed nomenclature encompasses forty-three distinct proteoglycan-encoding genes and many alternatively-spliced variants. The biological functions of these four proteoglycan families are critically assessed in development, cancer and angiogenesis, and in various acquired and genetic diseases where their expression is aberrant.

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Albumin replacement in patients with severe sepsis or septic shock.

Pietro Caironi, Gianni Tognoni, Serge Masson … (2014)

Although previous studies have suggested the potential advantages of albumin administration in patients with severe sepsis, its efficacy has not been fully established. In this multicenter, open-label trial, we randomly assigned 1818 patients with severe sepsis, in 100 intensive care units (ICUs), to receive either 20% albumin and crystalloid solution or crystalloid solution alone. In the albumin group, the target serum albumin concentration was 30 g per liter or more until discharge from the ICU or 28 days after randomization. The primary outcome was death from any cause at 28 days. Secondary outcomes were death from any cause at 90 days, the number of patients with organ dysfunction and the degree of dysfunction, and length of stay in the ICU and the hospital. During the first 7 days, patients in the albumin group, as compared with those in the crystalloid group, had a higher mean arterial pressure (P=0.03) and lower net fluid balance (P<0.001). The total daily amount of administered fluid did not differ significantly between the two groups (P=0.10). At 28 days, 285 of 895 patients (31.8%) in the albumin group and 288 of 900 (32.0%) in the crystalloid group had died (relative risk in the albumin group, 1.00; 95% confidence interval [CI], 0.87 to 1.14; P=0.94). At 90 days, 365 of 888 patients (41.1%) in the albumin group and 389 of 893 (43.6%) in the crystalloid group had died (relative risk, 0.94; 95% CI, 0.85 to 1.05; P=0.29). No significant differences in other secondary outcomes were observed between the two groups. In patients with severe sepsis, albumin replacement in addition to crystalloids, as compared with crystalloids alone, did not improve the rate of survival at 28 and 90 days. (Funded by the Italian Medicines Agency; ALBIOS ClinicalTrials.gov number, NCT00707122.).

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Author and article information

Contributors

Roberto Latini:

ORCID: http://orcid.org/0000-0002-3729-4650

roberto.latini@marionegri.it

: albios@marionegri.it

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): 19 March 2021

Publication date PMC-release: 19 March 2021

Publication date Collection: 2021

Volume: 25

Electronic Location Identifier: 113

Affiliations

[1 ]GRID grid.4527.4, ISNI 0000000106678902, Department of Biochemistry and Molecular Pharmacology, , Mario Negri Institute for Pharmacological Research IRCCS, ; Milan, Italy

[2 ]GRID grid.4527.4, ISNI 0000000106678902, Department of Cardiovascular Medicine, , Mario Negri Institute for Pharmacological Research IRCCS, ; Via Mario Negri 2, 20156 Milan, Italy

[3 ]GRID grid.415025.7, ISNI 0000 0004 1756 8604, Emergency Department, , Ospedale San Gerardo, ; Monza, Italy

[4 ]GRID grid.419663.f, ISNI 0000 0001 2110 1693, Anestesia E Rianimazione, , ISMETT IRCCS, ; Palermo, Italy

[5 ]GRID grid.460094.f, ISNI 0000 0004 1757 8431, Anestesia III Terapia Intensiva Adulti, ASST Ospedale Papa Giovanni XXIII, ; Bergamo, Italy

[6 ]GRID grid.415217.4, ISNI 0000 0004 1756 8364, UOC Anestesia E Rianimazione, IRCCS Arcispedale Santa Maria Nuova, ; Reggio Emilia, Italy

[7 ]GRID grid.414818.0, ISNI 0000 0004 1757 8749, Dipartimento Di Anestesia, , Rianimazione Ed Emergenza Fondazione IRCCS Ca’ Granda Ospedale Maggiore Policlinico, ; Milan, Italy

[8 ]GRID grid.7563.7, ISNI 0000 0001 2174 1754, Department of Medicine and Surgery, , University of Milan-Bicocca, ; Milan, Italy

[9 ]Department of Anesthesiology and Critical Care, AOU S. Luigi Gonzaga, Orbassano, Italy

[10 ]GRID grid.7605.4, ISNI 0000 0001 2336 6580, Department of Oncology, , Università Degli Studi Di Torino, ; Turin, Italy

[11 ]GRID grid.7450.6, ISNI 0000 0001 2364 4210, Department of Anesthesiology, Emergency and Intensive Care Medicine, , University of Gӧttingen, ; Gӧttingen, Germany

Author information

Roberto Latini http://orcid.org/0000-0002-3729-4650

Article

Publisher ID: 3545

DOI: 10.1186/s13054-021-03545-1

PMC ID: 7980645

PubMed ID: 33741039

SO-VID: 3704314d-fc40-422b-9368-6782b0c36090

License:

Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. 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 in a credit line to the data.

History

Date received : 18 November 2020

Date accepted : 15 March 2021

Funding

Funded by: FundRef http://dx.doi.org/10.13039/501100003197, Agenzia Italiana del Farmaco, Ministero della Salute;

Award ID: FARM6JS3R5

Award Recipient : Luciano Gattinoni

Funded by: Italian Ministry of Health

Award ID: RF-2011-02348358

Award Recipient : Luciano Gattinoni

Funded by: Grifols

Award ID: ALBUS Grifols Award, 2015

Award Recipient : Pietro Caironi

Custom metadata

ScienceOpen disciplines: Emergency medicine & Trauma

Keywords: septic shock,biomarker,glycocalyx,syndecan-1,sphingosine-1-phosphate,ve-cadherin

Data availability:

ScienceOpen disciplines: Emergency medicine & Trauma

Keywords: septic shock, biomarker, glycocalyx, syndecan-1, sphingosine-1-phosphate, ve-cadherin

Endothelial damage in septic shock patients as evidenced by circulating syndecan-1, sphingosine-1-phosphate and soluble VE-cadherin: a substudy of ALBIOS

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Journal of Circulating Biomarkers

Most cited references 42

Severe Sepsis and Septic Shock

Proteoglycan form and function: A comprehensive nomenclature of proteoglycans

Albumin replacement in patients with severe sepsis or septic shock.

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