Red blood cell transfusion-related dynamics of extracellular vesicles in intensive care patients: a prospective subanalysis.
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
09 Jan 2024
09 Jan 2024
Historique:
received:
12
06
2023
accepted:
23
11
2023
medline:
10
1
2024
pubmed:
10
1
2024
entrez:
9
1
2024
Statut:
epublish
Résumé
Extracellular vesicles (EVs) accumulate during packed red blood cell (PRBC) storage. To date, the involvement of EVs in transfusion-related immunomodulation (TRIM) has not been prospectively evaluated in intensive care unit (ICU) patients. This was a prospective subanalysis of a recent observational feasibility study in postoperative ICU patients after: (1) open aortic surgery (Aorta), (2) bilateral lung transplantation (LuTx), and (3) other types of surgery (Comparison). Patient plasma was collected three times each before and after leukoreduced PRBC transfusion at 30-min intervals. The total number of EVs and EVs derived from erythrocytes (EryEVs), total platelets (total PEVs), activated platelets, granulocytes (GEVs), monocytes, and myeloid cells in PRBC samples and patient plasma were analyzed by flow cytometry. Statistical analysis was performed by Spearman's correlation test, linear mixed models and pairwise comparisons by Wilcoxon matched-pairs test. Twenty-three patients (Aorta n = 5, LuTx n = 9, Comparison n = 9) were included in the final analysis. All EV subgroups analyzed were detectable in all PRBCs samples (n = 23), but concentrations did not correlate with storage time. Moreover, all EVs analyzed were detectable in all plasma samples (n = 138), and EV counts were consistent before transfusion. Concentrations of total EVs, EryEVs, total PEVs, and GEVs increased after transfusion compared with baseline in the entire cohort but not in specific study groups. Furthermore, the change in plasma EV counts (total EVs and EryEVs) after transfusion correlated with PRBC storage time in the entire cohort. Extracellular vesicles were detectable in all PRBC and plasma samples. Individual EV subtypes increased after transfusion in the entire cohort, and in part correlated with storage duration. Future clinical studies to investigate the role of EVs in TRIM are warranted and should anticipate a larger sample size.Trial registration: Clinicaltrials.gov: NCT03782623.
Identifiants
pubmed: 38195728
doi: 10.1038/s41598-023-48251-w
pii: 10.1038/s41598-023-48251-w
doi:
Banques de données
ClinicalTrials.gov
['NCT03782623']
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
911Subventions
Organisme : Medical Scientific Fund of the Mayor of the City of Vienna
ID : 19046
Informations de copyright
© 2024. The Author(s).
Références
Almizraq, R. J., Holovati, J. L. & Acker, J. P. Characteristics of extracellular vesicles in red blood concentrates change with storage time and blood manufacturing method. Transfus Med. Hemother. 45(3), 185–193 (2018).
doi: 10.1159/000486137
pubmed: 29928174
pmcid: 6006624
Antonelou, M. H. & Seghatchian, J. Update on extracellular vesicles inside red blood cell storage units: Adjust the sails closer to the new wind. Transfus Apher. Sci. 55(1), 92–104 (2016).
doi: 10.1016/j.transci.2016.07.016
pubmed: 27452642
Baron, D. M., Lei, C. & Berra, L. Old, older, the oldest: Red blood cell storage and the potential harm of using older red blood cell concentrates. Curr. Opin. Anaesthesiol. 33(2), 234–239 (2020).
doi: 10.1097/ACO.0000000000000824
pubmed: 31876784
Bilgin, Y. M. & Brand, A. Transfusion-related immunomodulation: A second hit in an inflammatory cascade? Vox Sang. 95(4), 261–271 (2008).
doi: 10.1111/j.1423-0410.2008.01100.x
pubmed: 19138255
Remy, K. E. et al. Mechanisms of red blood cell transfusion-related immunomodulation. Transfusion 58(3), 804–815 (2018).
doi: 10.1111/trf.14488
pubmed: 29383722
pmcid: 6592041
Flatman, L. K. et al. Association between leukoreduced red blood cell transfusions and hospital-acquired infections in critically ill children: A secondary analysis of the TRIPICU study. Vox Sang. 117(4), 545–552 (2022).
doi: 10.1111/vox.13224
pubmed: 34820856
Flatman, L. K. et al. Association between the length of storage of transfused leukoreduced red blood cell units and hospital-acquired infections in critically ill children: A secondary analysis of the TRIPICU study. Transfus Med. 31(6), 467–473 (2021).
doi: 10.1111/tme.12824
pubmed: 34585466
Claridge, J. A., Sawyer, R. G., Schulman, A. M., McLemore, E. C. & Young, J. S. Blood transfusions correlate with infections in trauma patients in a dose-dependent manner. Am. Surg. 68(7), 566–572 (2002).
doi: 10.1177/000313480206800702
pubmed: 12132734
Malone, D. L. et al. Blood transfusion, independent of shock severity, is associated with worse outcome in trauma. J. Trauma 54(5), 898–905 (2003).
doi: 10.1097/01.TA.0000060261.10597.5C
pubmed: 12777902
Taylor, R. W. et al. Red blood cell transfusions and nosocomial infections in critically ill patients. Crit. Care Med. 34(9), 2302–2308 (2006).
doi: 10.1097/01.CCM.0000234034.51040.7F
pubmed: 16849995
Noulsri, E. & Palasuwan, A. Effects of donor age, donor sex, blood-component processing, and storage on cell-derived microparticle concentrations in routine blood-component preparation. Transfus Apher. Sci. 57(4), 587–592 (2018).
doi: 10.1016/j.transci.2018.07.018
pubmed: 30082165
Peters, A. L. et al. Transfusion of autologous extracellular vesicles from stored red blood cells does not affect coagulation in a model of human endotoxemia. Transfusion 58(6), 1486–1493 (2018).
doi: 10.1111/trf.14607
pubmed: 29577324
Hezel, M. E. V., Nieuwland, R., Bruggen, R. V. & Juffermans, N. P. The ability of extracellular vesicles to induce a pro-inflammatory host response. Int. J. Mol. Sci. 18(6), 1285 (2017).
doi: 10.3390/ijms18061285
pubmed: 28621719
pmcid: 5486107
Whitaker B. I. R. & Harris, A. The 2013 AABB Blood Collection, Utilization, and Patient Blood Management Survey Report (2015).
Raeven, P., Zipperle, J. & Drechsler, S. Extracellular vesicles as markers and mediators in sepsis. Theranostics 8(12), 3348–3365 (2018).
doi: 10.7150/thno.23453
pubmed: 29930734
pmcid: 6010985
Thery, C. et al. Minimal information for studies of extracellular vesicles 2018 (MISEV2018): A position statement of the International Society for Extracellular Vesicles and update of the MISEV2014 guidelines. J. Extracell. Vesicles 7(1), 1535750 (2018).
doi: 10.1080/20013078.2018.1535750
pubmed: 30637094
pmcid: 6322352
D’Alessandro, A. From omics technologies to personalized transfusion medicine. Expert Rev. Proteom. 16(3), 215–225 (2019).
doi: 10.1080/14789450.2019.1571917
Norris, P. J. et al. Influence of blood storage age on immune and coagulation parameters in critically ill transfused patients. Transfusion 59(4), 1223–1232 (2019).
doi: 10.1111/trf.15250
pubmed: 30882927
pmcid: 6450744
Boshuizen, M. et al. The effect of red blood cell transfusion on iron metabolism in critically ill patients. Transfusion 59(4), 1196–1201 (2019).
doi: 10.1111/trf.15127
pubmed: 30597563
Raeven, P. et al. Red blood cell transfusion-related eicosanoid profiles in intensive care patients—A prospective, observational feasibility study. Front. Physiol. 14, 1164926 (2023).
doi: 10.3389/fphys.2023.1164926
pubmed: 37008004
pmcid: 10060532
Vandenbroucke, J. P. et al. Strengthening the reporting of observational studies in epidemiology (STROBE): Explanation and elaboration. Epidemiology 18(6), 805–835 (2007).
doi: 10.1097/EDE.0b013e3181577511
pubmed: 18049195
Hobbhahn, J. et al. Heparin reversal by protamine in humans—Complement, prostaglandins, blood cells, and hemodynamics. J. Appl. Physiol. 71(4), 1415–1421 (1991).
doi: 10.1152/jappl.1991.71.4.1415
pubmed: 1757364
Szefel, J., Kruszewski, W. J. & Sobczak, E. Factors influencing the eicosanoids synthesis in vivo. Biomed. Res. Int. 2015, 690692 (2015).
doi: 10.1155/2015/690692
pubmed: 25861641
pmcid: 4377373
Wisgrill, L. et al. Peripheral blood microvesicles secretion is influenced by storage time, temperature, and anticoagulants. Cytometry A 89(7), 663–672 (2016).
doi: 10.1002/cyto.a.22892
pubmed: 27442840
van der Pol, E., van Gemert, M. J., Sturk, A., Nieuwland, R. & van Leeuwen, T. G. Single vs swarm detection of microparticles and exosomes by flow cytometry. J. Thromb. Haemost. 10(5), 919–930 (2012).
doi: 10.1111/j.1538-7836.2012.04683.x
pubmed: 22394434
Kuznetsova, A., Brockhoff, P. B. & Christensen, R. H. lmerTest package: Tests in linear mixed effects models. J. Stat. Softw. 82(13), 1–26 (2017).
doi: 10.18637/jss.v082.i13
Jy, W. et al. Presurgical levels of circulating cell-derived microparticles discriminate between patients with and without transfusion in coronary artery bypass graft surgery. J. Thorac. Cardiovasc. Surg. 149(1), 305–311 (2015).
doi: 10.1016/j.jtcvs.2014.10.042
pubmed: 25524686
van der Pol, E., Welsh, J. A. & Nieuwland, R. Minimum information to report about a flow cytometry experiment on extracellular vesicles: Communication from the ISTH SSC subcommittee on vascular biology. J. Thromb. Haemost. 20(1), 245–251 (2022).
doi: 10.1111/jth.15540
pubmed: 34637195
Witwer, K. W. et al. Updating MISEV: Evolving the minimal requirements for studies of extracellular vesicles. J. Extracell. Vesicles 10(14), e12182 (2021).
doi: 10.1002/jev2.12182
pubmed: 34953156
pmcid: 8710080
Arraud, N., Gounou, C., Turpin, D. & Brisson, A. R. Fluorescence triggering: A general strategy for enumerating and phenotyping extracellular vesicles by flow cytometry. Cytometry A 89(2), 184–195 (2016).
doi: 10.1002/cyto.a.22669
pubmed: 25857288
Haller, P. M. et al. Changes in circulating extracellular vesicles in patients with ST-elevation myocardial infarction and potential effects of remote ischemic conditioning—A randomized controlled trial. Biomedicines 8(7), 218 (2020).
doi: 10.3390/biomedicines8070218
pubmed: 32708657
pmcid: 7400268
Tzounakas, V. L. et al. Early and late-phase 24 h responses of stored red blood cells to recipient-mimicking conditions. Front. Physiol. 13, 907497 (2022).
doi: 10.3389/fphys.2022.907497
pubmed: 35721567
pmcid: 9198496
Juffermans, N. P., Vlaar, A. P., Prins, D. J., Goslings, J. C. & Binnekade, J. M. The age of red blood cells is associated with bacterial infections in critically ill trauma patients. Blood Transfus 10(3), 290–295 (2012).
pubmed: 22395349
pmcid: 3417727
Spinella, P. C. et al. Duration of red blood cell storage is associated with increased incidence of deep vein thrombosis and in hospital mortality in patients with traumatic injuries. Crit. Care 13(5), R151 (2009).
doi: 10.1186/cc8050
pubmed: 19772604
pmcid: 2784373
Gerner, M. C. et al. Packed red blood cells inhibit T-cell activation via ROS-dependent signaling pathways. J. Biol. Chem. 296, 100487 (2021).
doi: 10.1016/j.jbc.2021.100487
pubmed: 33676898
pmcid: 8042437
Tzounakas, V. L. et al. Deciphering the relationship between free and vesicular hemoglobin in stored red blood cell units. Front. Physiol. 13, 840995 (2022).
doi: 10.3389/fphys.2022.840995
pubmed: 35211035
pmcid: 8861500
Ohlinger, T. et al. Storage of packed red blood cells impairs an inherent coagulation property of erythrocytes. Front. Physiol. 13, 1021553 (2022).
doi: 10.3389/fphys.2022.1021553
pubmed: 36505041
pmcid: 9732456
Tzounakas, V. L., Kriebardis, A. G., Papassideri, I. S. & Antonelou, M. H. Donor-variation effect on red blood cell storage lesion: A close relationship emerges. Proteom. Clin. Appl. 10(8), 791–804 (2016).
doi: 10.1002/prca.201500128
Isiksacan, Z. et al. Assessment of stored red blood cells through lab-on-a-chip technologies for precision transfusion medicine. Proc. Natl. Acad. Sci. U.S.A. 120(32), e2115616120 (2023).
doi: 10.1073/pnas.2115616120
pubmed: 37494421