Brief High Oxygen Concentration Induces Oxidative Stress in Leukocytes and Platelets: A Randomized Cross-over Pilot Study in Healthy Male Volunteers.
Adolescent
Adult
Aged
Blood Platelets
/ drug effects
Cross-Over Studies
Humans
Leukocytes
/ drug effects
Male
Middle Aged
Oxidative Stress
/ drug effects
Oxygen
/ administration & dosage
Oxygen Inhalation Therapy
Pilot Projects
Platelet Aggregation
/ drug effects
Reactive Oxygen Species
/ blood
Reference Values
Young Adult
Journal
Shock (Augusta, Ga.)
ISSN: 1540-0514
Titre abrégé: Shock
Pays: United States
ID NLM: 9421564
Informations de publication
Date de publication:
01 09 2021
01 09 2021
Historique:
pubmed:
17
3
2021
medline:
9
3
2022
entrez:
16
3
2021
Statut:
ppublish
Résumé
Supplemental oxygen is administered routinely in the clinical setting to relieve or prevent tissue hypoxia, but excessive exposure may induce oxidative damage or disrupt essential homeostatic functions. It is speculated that oxidative stress in leukocytes and platelets may contribute to vascular diseases by promoting inflammation and cell aggregation. In this pilot study 30 healthy male volunteers (18-65 years) were exposed to high oxygen concentration (non-rebreather mask, 8 L/min, 100% O2) and synthetic air (non-rebreather mask, 8 L/min, 21% O2) in a cross-over design for 20 min at a 3-week interval. Venous blood samples were obtained at baseline and 1, 3, and 6 h postintervention. Primary outcome was generation of reactive oxygen species in leukocytes as measured by the redox-sensitive fluorescent dye dihydrorhodamine 123. Additional outcomes were oxidative stress in platelets and platelet aggregation as measured by thromboelastography (ROTEM) and Multiplate analyses. High oxygen exposure induced oxidative stress in leukocytes as evidenced by significantly higher mean fluorescence intensity (MFI) compared with synthetic air at 3 h postintervention (47% higher, P = 0.015) and 6 h postintervention (37% higher, P = 0.133). Oxidative stress was also detectable in platelets (33% higher MFI in comparison with synthetic air at 6 h, P = 0.024; MFI 20% above baseline at 3 h, P = 0.036; 37% above baseline at 6 h, P = 0.002). ROTEM analyses demonstrated reduced mean clotting time 1 h postintervention compared with baseline (-4%, P = 0.049), whereas there were no significant effects on other surrogate coagulation parameters. Clinically relevant oxygen exposure induces oxidative stress in leukocytes and platelets, which may influence the immune and clotting functions of these cells.
Sections du résumé
BACKGROUND
Supplemental oxygen is administered routinely in the clinical setting to relieve or prevent tissue hypoxia, but excessive exposure may induce oxidative damage or disrupt essential homeostatic functions. It is speculated that oxidative stress in leukocytes and platelets may contribute to vascular diseases by promoting inflammation and cell aggregation.
METHODS
In this pilot study 30 healthy male volunteers (18-65 years) were exposed to high oxygen concentration (non-rebreather mask, 8 L/min, 100% O2) and synthetic air (non-rebreather mask, 8 L/min, 21% O2) in a cross-over design for 20 min at a 3-week interval. Venous blood samples were obtained at baseline and 1, 3, and 6 h postintervention. Primary outcome was generation of reactive oxygen species in leukocytes as measured by the redox-sensitive fluorescent dye dihydrorhodamine 123. Additional outcomes were oxidative stress in platelets and platelet aggregation as measured by thromboelastography (ROTEM) and Multiplate analyses.
FINDINGS
High oxygen exposure induced oxidative stress in leukocytes as evidenced by significantly higher mean fluorescence intensity (MFI) compared with synthetic air at 3 h postintervention (47% higher, P = 0.015) and 6 h postintervention (37% higher, P = 0.133). Oxidative stress was also detectable in platelets (33% higher MFI in comparison with synthetic air at 6 h, P = 0.024; MFI 20% above baseline at 3 h, P = 0.036; 37% above baseline at 6 h, P = 0.002). ROTEM analyses demonstrated reduced mean clotting time 1 h postintervention compared with baseline (-4%, P = 0.049), whereas there were no significant effects on other surrogate coagulation parameters.
CONCLUSION
Clinically relevant oxygen exposure induces oxidative stress in leukocytes and platelets, which may influence the immune and clotting functions of these cells.
Identifiants
pubmed: 33725433
pii: 00024382-202109000-00008
doi: 10.1097/SHK.0000000000001728
doi:
Substances chimiques
Reactive Oxygen Species
0
Oxygen
S88TT14065
Types de publication
Journal Article
Randomized Controlled Trial
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
384-395Informations de copyright
Copyright © 2021 by the Shock Society.
Déclaration de conflit d'intérêts
The authors report no conflicts of interest.
Références
Asfar P, Singer M, Radermacher P. Understanding the benefits and harms of oxygen therapy. Intensive Care Med 41:1118–1121, 2015.
Helmerhorst HJF, Schultz MJ, van der Voort PHJ, de Jonge E, van Westerloo DJ. Bench-to-bedside review: the effects of hyperoxia during critical illness. Crit Care 19 (1):284, 2015.
Kulkarni AC, Kuppusamy P, Parinandi N. Oxygen, the lead actor in the pathophysiologic drama: enactment of the trinity of normoxia, hypoxia, and hyperoxia in disease and therapy. Antioxid Redox Signal 9 (10):1717–1730, 2007.
Mandelker L. The natural activities of cells, the role of reactive oxygen species, and their relation to antioxidants, nutraceuticals, botanicals, and other biologic therapies. Vet Clin North Am Small Anim Pract 34 (1):39–66, 2004.
Blokhina O, Virolainen E, Fagerstedt KV. Antioxidants, oxidative damage and oxygen deprivation stress: a review. Ann Bot 91 ((Spec. Iss. Jan.)):179–194, 2003.
Loscalzo J. Oxidant stress: a key determinant of atherothrombosis. Biochem Soc Trans 31:1059–1061, 2003.
Griffin JH, Fernández JA, Deguchi H. Plasma lipoproteins, hemostasis and thrombosis. Thromb Haemost 86 (1):386–394, 2001.
Ruggeri ZM. Von Willebrand factor, platelets and endothelial cell interactions. J Thromb Haemost 1 (7):1335–1342, 2003.
Krötz F, Sohn HY, Pohl U. Reactive oxygen species: players in the platelet game. Arterioscler Thromb Vasc Biol 24:1988–1996, 2004.
Mittal M, Siddiqui MR, Tran K, Reddy SP, Malik AB. Reactive oxygen species in inflammation and tissue injury. Antioxidants Redox Signal 20 (7):1126–1167, 2014.
Feuring M, Christ M, Roell A, Schueller P, Losel R, Dempfle CE, Schultz A, Wehling M. Alterations in platelet function during the ovarian cycle. Blood Coagul Fibrinolysis 13 (5):443–447, 2002.
Yuan T, Yang T, Chen H, Fu D, Hu Y, Wang J, Yuan Q, Yu H, Xu W, Xie X. New insights into oxidative stress and inflammation during diabetes mellitus-accelerated atherosclerosis. Redox Biol 20:247–260, 2019.
Griendling KK, FitzGerald GA. Oxidative stress and cardiovascular injury Part I: basic mechanisms and in vivo monitoring of ROS. Circulation 108 (16):1912–1916, 2003.
Griendling KK, FitzGerald GA. Oxidative stress and cardiovascular injury: Part II: animal and human studies. Circulation 108 (17):2034–2040, 2003.
Karbach S, Wenzel P, Waisman A, Munzel T, Daiber A. eNOS uncoupling in cardiovascular diseases—the role of oxidative stress and inflammation. Curr Pharm Des 20 (22):3579–3594, 2014.
Szabó C. The pathophysiological role of peroxynitrite in shock, inflammation, and ischemia-reperfusion injury. Shock 6 (2):79–88, 1996.
Medzhitov R. Origin and physiological roles of inflammation. Nature 454 (7203):428–435, 2008.
Sonego G, Abonnenc M, Tissot JD, Prudent M, Lion N. Redox proteomics and platelet activation: understanding the redox proteome to improve platelet quality for transfusion. Int J Mol Sci 18 (2):387, 2017.
Stuart MJ, Holmsen H. Hydrogen peroxide, an inhibitor of platelet function: effect on adenine nucleotide metabolism, and the release reaction. Am J Hematol 2 (1):53–63, 1977.
Ambrosio G, Golino P, Pascucci I, Rosolowsky M, Campbell WB, DeClerck F, Tritto I, Chiariello M. Modulation of platelet function by reactive oxygen metabolites. Am J Physiol 267 (1 pt 2):H308–H318, 1994.
Praticò D, Iuliano L, Ghiselli A, Alessandri C, Violi F. Hydrogen peroxide as trigger of platelet aggregation. Pathophysiol Haemost Thromb 21 (3):169–174, 1991.
Freedman JE. Oxidative stress and platelets. Arterioscler Thromb Vasc Biol 28 (3):s11–s16, 2008.
Chakrabarti S, Clutton P, Varghese S, Cox D, Mascelli MA, Freedman JE. Glycoprotein IIb/IIIa inhibition enhances platelet nitric oxide release. Thromb Res 113 (3–4):225–233, 2004.
Capelle C, Zeng N, Danileviciute E, Rodrigues SF, Ollert M, Balling R, He F. Identification of VIMP as a gene inhibiting cytokine production in human CD4+ effector T cells. SSRN Electron J 2020.
Schober P, Schwarte LA. From system to organ to cell: oxygenation and perfusion measurement in anesthesia and critical care. J Clin Monit Comput 26 (4):255–265, 2012.
Mikolajczyk TP, Nosalski R, Szczepaniak P, Budzyn K, Osmenda G, Skiba D, Sagan A, Wu J, Vinh A, Marvar PJ, et al. Role of chemokine RANTES in the regulation of perivascular inflammation, T-cell accumulation, and vascular dysfunction in hypertension. FASEB J 30 (5):1987–1999, 2016.
Salminen A, Kaarniranta K, Kauppinen A. Crosstalk between oxidative stress and SIRT1: impact on the aging process. Int J Mol Sci 14 (2):3834–3859, 2013.
Rohr-Udilova NV, Stolze K, Sagmeister S, Nohl H, Schulte-Hermann R, Grasl-Kraupp B. Lipid hydroperoxides from processed dietary oils enhance growth of hepatocarcinoma cells. Mol Nutr Food Res 52 (3):352–359, 2008.
Wan S, Kuo N, Kryczek I, Zou W, Welling TH. Myeloid cells in hepatocellular carcinoma. Hepatology 62 (4):1304–1312, 2015.
Yang WS, SriRamaratnam R, Welsch ME, Shimada K, Skouta R, Viswanathan VS, Cheah JH, Clemons PA, Shamji AF, Clish CB, et al. Regulation of ferroptotic cancer cell death by GPX4. Cell 156 (1–2):317–331, 2014.
Hussain SP, Hofseth LJ, Harris CC. Radical causes of cancer. Nat Rev Cancer 3 (4):276–285, 2003.
Wang P, Wu Y, Li X, Ma X, Zhong L. Thioredoxin and thioredoxin reductase control tissue factor activity by thiol redox-dependent mechanism. J Biol Chem 288 (5):3346–3358, 2013.
Schulte J. Peroxiredoxin 4: a multifunctional biomarker worthy of further exploration. BMC Med 9:137, 2011.
Wetterslev J, Meyhoff CS, Jørgensen LN, Gluud C, Lindschou J, Rasmussen LS. The effects of high perioperative inspiratory oxygen fraction for adult surgical patients. Cochrane database Syst Rev 6:CD008884, 2015.
Allegranzi B, Zayed B, Bischoff P, Kubilay NZ, de Jonge S, de Vries F, Gomes SM, Gans S, Wallert ED, Wu X, et al. New WHO recommendations on intraoperative and postoperative measures for surgical site infection prevention: an evidence-based global perspective. Lancet Infect Dis 16 (12):e288–e303, 2016.