Skip to main content
Top
Published in:

Open Access 07-02-2024 | Post-COVID Syndrome | Research

Endothelial dysfunction and cardiovascular risk in post-COVID-19 patients after 6- and 12-months SARS-CoV-2 infection

Authors: Paula Poyatos, Neus Luque, Gladis Sabater, Saioa Eizaguirre, Marc Bonnin, Ramon Orriols, Olga Tura-Ceide

Published in: Infection | Issue 4/2024

Login to get access

Abstract

Introduction

SARS-CoV-2 infection causes severe endothelial damage, an essential step for cardiovascular complications. Endothelial-colony forming cells (ECFCs) act as a biomarker of vascular damage but their role in SARS-CoV-2 remain unclear. The aim of this study was to assess whether the number of ECFCs and angiogenic biomarkers remained altered after 6 and 12-months post-infection and whether this imbalance correlated with the presence of long-COVID syndrome and other biological parameters measured.

Methods

Seventy-two patients were recruited at different time-points after overcoming COVID-19 and thirty-one healthy controls. All subjects were matched for age, gender, BMI, and comorbidities. ECFCs were obtained from peripheral blood and cultured with specific conditions.

Results

The results confirm the presence of a long-term sequela in post-COVID-19 patients, with an abnormal increase in ECFC production compared to controls (82.8% vs. 48.4%, P < 0.01) that is maintained up to 6-months (87.0% vs. 48.4%, P < 0.01) and 12-months post-infection (85.0% vs. 48.4%, P < 0.01). Interestingly, post-COVID-19 patients showed a significant downregulation of angiogenesis-related proteins compared to controls indicating a clear endothelial injury. Troponin, NT-proBNP and ferritin levels, markers of cardiovascular risk and inflammation, remained elevated up to 12-months post-infection. Patients with lower numbers of ECFC exhibited higher levels of inflammatory markers, such as ferritin, suggesting that ECFCs may play a protective role. Additionally, long-COVID syndrome was associated with higher ferritin levels and with female gender.

Conclusions

These findings highlight the presence of vascular sequela that last up to 6- and 12-months post-infection and point out the need for preventive measures and patient follow-up.
Appendix
Available only for authorised users
Literature
1.
go back to reference Huertas A, Montani D, Savale L, Pichon J, Tu L, Parent F, et al. Endothelial cell dysfunction: a major player in SARS-CoV-2 infection (COVID-19)? Eur Respir J. 2020;56:2001634.PubMedPubMedCentral Huertas A, Montani D, Savale L, Pichon J, Tu L, Parent F, et al. Endothelial cell dysfunction: a major player in SARS-CoV-2 infection (COVID-19)? Eur Respir J. 2020;56:2001634.PubMedPubMedCentral
2.
go back to reference Sungnak W, Huang N, Bécavin C, Berg M, Queen R, Litvinukova M, et al. SARS-CoV-2 entry factors are highly expressed in nasal epithelial cells together with innate immune genes. Nat Med. 2020;26:681–7.PubMedPubMedCentral Sungnak W, Huang N, Bécavin C, Berg M, Queen R, Litvinukova M, et al. SARS-CoV-2 entry factors are highly expressed in nasal epithelial cells together with innate immune genes. Nat Med. 2020;26:681–7.PubMedPubMedCentral
3.
go back to reference Ambrosino P, Calcaterra IL, Mosella M, Formisano R, D’anna SE, Bachetti T, et al. Endothelial dysfunction in COVID‐19: a unifying mechanism and a potential therapeutic target. Biomedicines. 2022;10. Ambrosino P, Calcaterra IL, Mosella M, Formisano R, D’anna SE, Bachetti T, et al. Endothelial dysfunction in COVID‐19: a unifying mechanism and a potential therapeutic target. Biomedicines. 2022;10.
4.
go back to reference Hamming I, Timens W, Bulthuis MLC, Lely AT, Navis GJ, van Goor H. Tissue distribution of ACE2 protein, the functional receptor for SARS coronavirus. A first step in understanding SARS pathogenesis. J Pathol. 2004;203:631–7.PubMedPubMedCentral Hamming I, Timens W, Bulthuis MLC, Lely AT, Navis GJ, van Goor H. Tissue distribution of ACE2 protein, the functional receptor for SARS coronavirus. A first step in understanding SARS pathogenesis. J Pathol. 2004;203:631–7.PubMedPubMedCentral
5.
go back to reference Monteil V, Kwon H, Prado P, Hagelkrüys A, Wimmer RA, Stahl M, et al. Inhibition of SARS-CoV-2 infections in engineered human tissues using clinical-grade soluble human ACE2. Cell. 2020;181:905-913.e7.PubMedPubMedCentral Monteil V, Kwon H, Prado P, Hagelkrüys A, Wimmer RA, Stahl M, et al. Inhibition of SARS-CoV-2 infections in engineered human tissues using clinical-grade soluble human ACE2. Cell. 2020;181:905-913.e7.PubMedPubMedCentral
6.
go back to reference Maccio U, Zinkernagel AS, Shambat SM, Zeng X, Cathomas G, Ruschitzka F, et al. SARS-CoV-2 leads to a small vessel endotheliitis in the heart. EBioMedicine. 2021;63: 103182.PubMedPubMedCentral Maccio U, Zinkernagel AS, Shambat SM, Zeng X, Cathomas G, Ruschitzka F, et al. SARS-CoV-2 leads to a small vessel endotheliitis in the heart. EBioMedicine. 2021;63: 103182.PubMedPubMedCentral
7.
go back to reference Xu Sw, Ilyas I, Weng Jp. Endothelial dysfunction in COVID-19: an overview of evidence, biomarkers, mechanisms and potential therapies. Acta Pharmacol Sin. 2023;44:695–709.PubMed Xu Sw, Ilyas I, Weng Jp. Endothelial dysfunction in COVID-19: an overview of evidence, biomarkers, mechanisms and potential therapies. Acta Pharmacol Sin. 2023;44:695–709.PubMed
8.
go back to reference Esper RJ, Nordaby RA, Vilariño JO, Paragano A, Cacharrón JL, Machado RA. Endothelial dysfunction: a comprehensive appraisal. Cardiovasc Diabetol. 2006;5:1–18. Esper RJ, Nordaby RA, Vilariño JO, Paragano A, Cacharrón JL, Machado RA. Endothelial dysfunction: a comprehensive appraisal. Cardiovasc Diabetol. 2006;5:1–18.
9.
10.
go back to reference Rodríguez C, Luque N, Blanco I, Sebastian L, Barberà JA, Peinado VI, et al. Pulmonary endothelial dysfunction and thrombotic complications in COVID-19 patients. Am J Respir Cell Mol Biol. 2021. Rodríguez C, Luque N, Blanco I, Sebastian L, Barberà JA, Peinado VI, et al. Pulmonary endothelial dysfunction and thrombotic complications in COVID-19 patients. Am J Respir Cell Mol Biol. 2021.
11.
go back to reference Bonetti PO, Lerman LO, Lerman A. Endothelial dysfunction. Arterioscler Thromb Vasc Biol. 2003;23:168–75.PubMed Bonetti PO, Lerman LO, Lerman A. Endothelial dysfunction. Arterioscler Thromb Vasc Biol. 2003;23:168–75.PubMed
12.
go back to reference Elyaspour Z, Zibaeenezhad MJ, Razmkhah M, Razeghian-Jahromi I. Is it all about endothelial dysfunction and thrombosis formation? The secret of COVID-19. Clin Appl Thromb. 2021;27:1–11. Elyaspour Z, Zibaeenezhad MJ, Razmkhah M, Razeghian-Jahromi I. Is it all about endothelial dysfunction and thrombosis formation? The secret of COVID-19. Clin Appl Thromb. 2021;27:1–11.
13.
go back to reference Varga Z, Flammer AJ, Steiger P, Haberecker M, Andermatt R, Zinkernagel AS, et al. Endothelial cell infection and endotheliitis in COVID-19 [Internet]. Lancet. 2020; p. 1417–8. Varga Z, Flammer AJ, Steiger P, Haberecker M, Andermatt R, Zinkernagel AS, et al. Endothelial cell infection and endotheliitis in COVID-19 [Internet]. Lancet. 2020; p. 1417–8.
14.
go back to reference Rotoli BM, Barilli A, Visigalli R, Ferrari F, Dall’Asta V. Endothelial cell activation by SARS-CoV-2 spike S1 protein: a crosstalk between endothelium and innate immune cells. Biomedicines. 2021;9:1220.PubMedPubMedCentral Rotoli BM, Barilli A, Visigalli R, Ferrari F, Dall’Asta V. Endothelial cell activation by SARS-CoV-2 spike S1 protein: a crosstalk between endothelium and innate immune cells. Biomedicines. 2021;9:1220.PubMedPubMedCentral
15.
go back to reference Fogarty H, Townsend L, Morrin H, Ahmad A, Comerford C, Karampini E, et al. Persistent endotheliopathy in the pathogenesis of long COVID syndrome. J Thromb Haemost. 2021;19:2546–53.PubMed Fogarty H, Townsend L, Morrin H, Ahmad A, Comerford C, Karampini E, et al. Persistent endotheliopathy in the pathogenesis of long COVID syndrome. J Thromb Haemost. 2021;19:2546–53.PubMed
16.
go back to reference Klok FA, Kruip MJHA, van der Meer NJM, Arbous MS, Gommers DAMPJ, Kant KM, et al. Incidence of thrombotic complications in critically ill ICU patients with COVID-19. Thromb Res. 2020;191:145–7.PubMedPubMedCentral Klok FA, Kruip MJHA, van der Meer NJM, Arbous MS, Gommers DAMPJ, Kant KM, et al. Incidence of thrombotic complications in critically ill ICU patients with COVID-19. Thromb Res. 2020;191:145–7.PubMedPubMedCentral
17.
go back to reference Rezabakhsh A, Sadat-Ebrahimi S-R, Ala A, Nabavi SM, Banach M, Ghaffari S. A close-up view of dynamic biomarkers in the setting of COVID-19: Striking focus on cardiovascular system. J Cell Mol Med. 2022;26:274–86.PubMed Rezabakhsh A, Sadat-Ebrahimi S-R, Ala A, Nabavi SM, Banach M, Ghaffari S. A close-up view of dynamic biomarkers in the setting of COVID-19: Striking focus on cardiovascular system. J Cell Mol Med. 2022;26:274–86.PubMed
18.
go back to reference Sibila O, Perea L, Albacar N, Moisés J, Cruz T, Mendoza N, et al. Elevated plasma levels of epithelial and endothelial cell markers in COVID-19 survivors with reduced lung diffusing capacity six months after hospital discharge. Respir Res. 2022;23:1–10. Sibila O, Perea L, Albacar N, Moisés J, Cruz T, Mendoza N, et al. Elevated plasma levels of epithelial and endothelial cell markers in COVID-19 survivors with reduced lung diffusing capacity six months after hospital discharge. Respir Res. 2022;23:1–10.
19.
go back to reference Chioh FWJ, Fong SW, Young BE, Wu KX, Siau A, Krishnan S, et al. Convalescent covid-19 patients are susceptible to endothelial dysfunction due to persistent immune activation. Elife. 2021;10. Chioh FWJ, Fong SW, Young BE, Wu KX, Siau A, Krishnan S, et al. Convalescent covid-19 patients are susceptible to endothelial dysfunction due to persistent immune activation. Elife. 2021;10.
20.
go back to reference Mancuso P, Gidaro A, Gregato G, Raveane A, Cremonesi P, Quarna J, et al. Circulating endothelial progenitors are increased in COVID-19 patients and correlate with SARS-CoV-2 RNA in severe cases. J Thromb Haemost. 2020;18:2744–50.PubMedPubMedCentral Mancuso P, Gidaro A, Gregato G, Raveane A, Cremonesi P, Quarna J, et al. Circulating endothelial progenitors are increased in COVID-19 patients and correlate with SARS-CoV-2 RNA in severe cases. J Thromb Haemost. 2020;18:2744–50.PubMedPubMedCentral
21.
go back to reference Poyatos P, Luque N, Eizaguirre S, Sabater G, Sebastián L, Francisco-Albesa Í, et al. Post-COVID-19 patients show an increased endothelial progenitor cell production. Transl Res. 2022;243:14–20.PubMedPubMedCentral Poyatos P, Luque N, Eizaguirre S, Sabater G, Sebastián L, Francisco-Albesa Í, et al. Post-COVID-19 patients show an increased endothelial progenitor cell production. Transl Res. 2022;243:14–20.PubMedPubMedCentral
22.
go back to reference Tousoulis D, Andreou I, Antoniades C, Tentolouris C, Stefanadis C. Role of inflammation and oxidative stress in endothelial progenitor cell function and mobilization: therapeutic implications for cardiovascular diseases. Atherosclerosis. 2008;201:236–47.PubMed Tousoulis D, Andreou I, Antoniades C, Tentolouris C, Stefanadis C. Role of inflammation and oxidative stress in endothelial progenitor cell function and mobilization: therapeutic implications for cardiovascular diseases. Atherosclerosis. 2008;201:236–47.PubMed
23.
go back to reference Yoder MC, Mead LE, Prater D, Krier TR, Mroueh KN, Li F, et al. Redefining endothelial progenitor cells via clonal analysis and hematopoietic stem/progenitor cell principals. Blood. 2007; p. 1801–9. Yoder MC, Mead LE, Prater D, Krier TR, Mroueh KN, Li F, et al. Redefining endothelial progenitor cells via clonal analysis and hematopoietic stem/progenitor cell principals. Blood. 2007; p. 1801–9.
24.
go back to reference Huertas A, Montani D, Savale L, Pichon J, Tu L, Parent F, et al. Endothelial cell dysfunction: a major player in SARS-CoV-2 infection (COVID-19)?. Eur Respir J NLM (Medline). 2020; p. 1524–6. Huertas A, Montani D, Savale L, Pichon J, Tu L, Parent F, et al. Endothelial cell dysfunction: a major player in SARS-CoV-2 infection (COVID-19)?. Eur Respir J NLM (Medline). 2020; p. 1524–6.
25.
go back to reference Sen S, McDonald SP, Coates PTH, Bonder CS. Endothelial progenitor cells: novel biomarker and promising cell therapy for cardiovascular disease. Clin Sci. 2011; p. 263–83. Sen S, McDonald SP, Coates PTH, Bonder CS. Endothelial progenitor cells: novel biomarker and promising cell therapy for cardiovascular disease. Clin Sci. 2011; p. 263–83.
26.
go back to reference Soriano JB, Murthy S, Marshall JC, Relan P, Diaz JV. A clinical case definition of post-COVID-19 condition by a Delphi consensus. Lancet Infect Dis. 2022;22:e102–7.PubMed Soriano JB, Murthy S, Marshall JC, Relan P, Diaz JV. A clinical case definition of post-COVID-19 condition by a Delphi consensus. Lancet Infect Dis. 2022;22:e102–7.PubMed
27.
go back to reference Puntmann VO, Carerj ML, Wieters I, Fahim M, Arendt C, Hoffmann J, et al. Outcomes of cardiovascular magnetic resonance imaging in patients recently recovered from coronavirus disease 2019 (COVID-19). JAMA Cardiol. 2020;5:1265–73.PubMedPubMedCentral Puntmann VO, Carerj ML, Wieters I, Fahim M, Arendt C, Hoffmann J, et al. Outcomes of cardiovascular magnetic resonance imaging in patients recently recovered from coronavirus disease 2019 (COVID-19). JAMA Cardiol. 2020;5:1265–73.PubMedPubMedCentral
28.
go back to reference Stanojevic S, Kaminsky DA, Miller MR, Thompson B, Aliverti A, Barjaktarevic I, et al. ERS/ATS technical standard on interpretive strategies for routine lung function tests. Eur Respir J. 2022;60:2101499.PubMed Stanojevic S, Kaminsky DA, Miller MR, Thompson B, Aliverti A, Barjaktarevic I, et al. ERS/ATS technical standard on interpretive strategies for routine lung function tests. Eur Respir J. 2022;60:2101499.PubMed
29.
go back to reference Gallogly S, Fujisawa T, Hung JD, Brittan M, Skinner EM, Mitchell AJ, et al. Generation of a novel in vitro model to study endothelial dysfunction from atherothrombotic specimens. Cardiovasc Drugs Ther. 2021;2021:1–10. Gallogly S, Fujisawa T, Hung JD, Brittan M, Skinner EM, Mitchell AJ, et al. Generation of a novel in vitro model to study endothelial dysfunction from atherothrombotic specimens. Cardiovasc Drugs Ther. 2021;2021:1–10.
30.
go back to reference Tura O, Skinner EM, Barclay R, Samuel K, Gallagher RCJ, Brittan M, et al. Late outgrowth endothelial cells resemble mature endothelial cells and are not derived from bone marrow. Stem Cells. 2013;31:338–48.PubMed Tura O, Skinner EM, Barclay R, Samuel K, Gallagher RCJ, Brittan M, et al. Late outgrowth endothelial cells resemble mature endothelial cells and are not derived from bone marrow. Stem Cells. 2013;31:338–48.PubMed
31.
go back to reference Alvarado-Moreno JA, Davila-Moreno J, Dominguez-Reyes V, Arreola-Diaz R, Isordia-Salas I, Chavez-Gonzalez A, et al. Morphological and functional alterations in endothelial colony-forming cells from recovered COVID-19 patients. Thromb Res. 2021;206:55–9.PubMedPubMedCentral Alvarado-Moreno JA, Davila-Moreno J, Dominguez-Reyes V, Arreola-Diaz R, Isordia-Salas I, Chavez-Gonzalez A, et al. Morphological and functional alterations in endothelial colony-forming cells from recovered COVID-19 patients. Thromb Res. 2021;206:55–9.PubMedPubMedCentral
32.
go back to reference Modarai B, Burnand KG, Sawyer B, Smith A. Endothelial progenitor cells are recruited into resolving venous thrombi. Circulation. 2005;111:2645–53.PubMed Modarai B, Burnand KG, Sawyer B, Smith A. Endothelial progenitor cells are recruited into resolving venous thrombi. Circulation. 2005;111:2645–53.PubMed
33.
go back to reference Lala A, Johnson KW, Januzzi JL, Russak AJ, Paranjpe I, Richter F, et al. Prevalence and impact of myocardial injury in patients hospitalized with COVID-19 INfection. J Am Coll Cardiol. 2020;76:533–46.PubMedPubMedCentral Lala A, Johnson KW, Januzzi JL, Russak AJ, Paranjpe I, Richter F, et al. Prevalence and impact of myocardial injury in patients hospitalized with COVID-19 INfection. J Am Coll Cardiol. 2020;76:533–46.PubMedPubMedCentral
34.
go back to reference Lippi G, Lavie CJ, Sanchis-Gomar F. Cardiac troponin I in patients with coronavirus disease 2019 (COVID-19): Evidence from a meta-analysis. Prog Cardiovasc Dis. 2020;63:390–1.PubMedPubMedCentral Lippi G, Lavie CJ, Sanchis-Gomar F. Cardiac troponin I in patients with coronavirus disease 2019 (COVID-19): Evidence from a meta-analysis. Prog Cardiovasc Dis. 2020;63:390–1.PubMedPubMedCentral
35.
go back to reference Huang L, Zhao P, Tang D, Zhu T, Han R, Zhan C, et al. Cardiac involvement in patients recovered from COVID-2019 identified using magnetic resonance imaging. JACC Cardiovasc Imaging. 2020;13:2330–9.PubMedPubMedCentral Huang L, Zhao P, Tang D, Zhu T, Han R, Zhan C, et al. Cardiac involvement in patients recovered from COVID-2019 identified using magnetic resonance imaging. JACC Cardiovasc Imaging. 2020;13:2330–9.PubMedPubMedCentral
36.
go back to reference Søyseth V, Kononova N, Neukamm A, Holmedahl NH, Hagve TA, Omland T, et al. Systemic inflammation induced by exacerbation of COPD or pneumonia in patients with COPD induces cardiac troponin elevation. BMJ Open Respir Res. 2021;8:1–8. Søyseth V, Kononova N, Neukamm A, Holmedahl NH, Hagve TA, Omland T, et al. Systemic inflammation induced by exacerbation of COPD or pneumonia in patients with COPD induces cardiac troponin elevation. BMJ Open Respir Res. 2021;8:1–8.
37.
go back to reference Miró Ò, Jiménez S, Mebazaa A, Freund Y, Burillo-Putze G, Martín A, et al. Pulmonary embolism in patients with COVID-19: incidence, risk factors, clinical characteristics, and outcome. Eur Heart J. 2021;42:3127–42.PubMed Miró Ò, Jiménez S, Mebazaa A, Freund Y, Burillo-Putze G, Martín A, et al. Pulmonary embolism in patients with COVID-19: incidence, risk factors, clinical characteristics, and outcome. Eur Heart J. 2021;42:3127–42.PubMed
38.
go back to reference Fish-Trotter H, Ferguson JF, Patel N, Arora P, Allen NB, Bachmann KN, et al. Inflammation and circulating natriuretic peptide levels. Circ Hear Fail. 2020;13:135–44. Fish-Trotter H, Ferguson JF, Patel N, Arora P, Allen NB, Bachmann KN, et al. Inflammation and circulating natriuretic peptide levels. Circ Hear Fail. 2020;13:135–44.
39.
go back to reference Wang L, Chen F, Bai L, Bai L, Huang Z, Peng Y. Association between NT-proBNP level and the severity of COVID-19 pneumonia. Cardiol Res Pract. 2021;2021:5537275.PubMedPubMedCentral Wang L, Chen F, Bai L, Bai L, Huang Z, Peng Y. Association between NT-proBNP level and the severity of COVID-19 pneumonia. Cardiol Res Pract. 2021;2021:5537275.PubMedPubMedCentral
40.
go back to reference Gul M, Ozyilmaz S, Bastug Gul Z, Kacmaz C, Satilmisoglu MH. Evaluation of cardiac injury with biomarkers and echocardiography after COVID-19 infection. J Physiol Pharmacol. 2022;73. Gul M, Ozyilmaz S, Bastug Gul Z, Kacmaz C, Satilmisoglu MH. Evaluation of cardiac injury with biomarkers and echocardiography after COVID-19 infection. J Physiol Pharmacol. 2022;73.
41.
go back to reference Feld J, Tremblay D, Thibaud S, Kessler A, Naymagon L. Ferritin levels in patients with COVID-19: A poor predictor of mortality and hemophagocytic lymphohistiocytosis. Int J Lab Hematol. 2020;42:773–9.PubMedPubMedCentral Feld J, Tremblay D, Thibaud S, Kessler A, Naymagon L. Ferritin levels in patients with COVID-19: A poor predictor of mortality and hemophagocytic lymphohistiocytosis. Int J Lab Hematol. 2020;42:773–9.PubMedPubMedCentral
42.
go back to reference Abohelwa M, Peterson CJ, Landis D, Le D, Conde C, DeWare C, et al. Clinical characteristics of hospital follow-up for patients hospitalized from SARS CoV-2 (COVID 19) in an academic outpatient internal medicine clinic. J Prim Care Community Health. 2022;13:1–6. Abohelwa M, Peterson CJ, Landis D, Le D, Conde C, DeWare C, et al. Clinical characteristics of hospital follow-up for patients hospitalized from SARS CoV-2 (COVID 19) in an academic outpatient internal medicine clinic. J Prim Care Community Health. 2022;13:1–6.
43.
go back to reference Banchini F, Cattaneo GM, Capelli P. Serum ferritin levels in inflammation: a retrospective comparative analysis between COVID-19 and emergency surgical non-COVID-19 patients. World J Emerg Surg. 2021;16:9.PubMedPubMedCentral Banchini F, Cattaneo GM, Capelli P. Serum ferritin levels in inflammation: a retrospective comparative analysis between COVID-19 and emergency surgical non-COVID-19 patients. World J Emerg Surg. 2021;16:9.PubMedPubMedCentral
44.
go back to reference Taneri PE, Gómez-Ochoa SA, Llanaj E, Raguindin PF, Rojas LZ, Roa-Díaz ZM, et al. Anemia and iron metabolism in COVID-19: a systematic review and meta-analysis. Eur J Epidemiol. 2020;35:763–73.PubMedPubMedCentral Taneri PE, Gómez-Ochoa SA, Llanaj E, Raguindin PF, Rojas LZ, Roa-Díaz ZM, et al. Anemia and iron metabolism in COVID-19: a systematic review and meta-analysis. Eur J Epidemiol. 2020;35:763–73.PubMedPubMedCentral
45.
go back to reference Mahroum N, Alghory A, Kiyak Z, Alwani A, Seida R, Alrais M, et al. Ferritin – from iron, through inflammation and autoimmunity, to COVID-19. J Autoimmun. 2022;126: 102778.PubMed Mahroum N, Alghory A, Kiyak Z, Alwani A, Seida R, Alrais M, et al. Ferritin – from iron, through inflammation and autoimmunity, to COVID-19. J Autoimmun. 2022;126: 102778.PubMed
46.
go back to reference Kuragano T, Joki N, Hase H, Kitamura K, Murata T, Fujimoto S, et al. Low transferrin saturation (TSAT) and high ferritin levels are significant predictors for cerebrovascular and cardiovascular disease and death in maintenance hemodialysis patients. PLoS ONE. 2020;15:1–12. Kuragano T, Joki N, Hase H, Kitamura K, Murata T, Fujimoto S, et al. Low transferrin saturation (TSAT) and high ferritin levels are significant predictors for cerebrovascular and cardiovascular disease and death in maintenance hemodialysis patients. PLoS ONE. 2020;15:1–12.
47.
go back to reference Balla J, Vercellotti GM, Jeney V, Yachie A, Varga Z, Jacob HS, et al. Heme, heme oxygenase, and ferritin: how the vascular endothelium survives (and Dies) in an iron-rich environment. Antioxid Redox Signal. 2007;9:2119–37.PubMed Balla J, Vercellotti GM, Jeney V, Yachie A, Varga Z, Jacob HS, et al. Heme, heme oxygenase, and ferritin: how the vascular endothelium survives (and Dies) in an iron-rich environment. Antioxid Redox Signal. 2007;9:2119–37.PubMed
48.
go back to reference Araujo JA, Zhang M, Yin F. Heme oxygenase-1, oxidation, inflammation, and atherosclerosis. Front Pharmacol. 2012;3:119.PubMedPubMedCentral Araujo JA, Zhang M, Yin F. Heme oxygenase-1, oxidation, inflammation, and atherosclerosis. Front Pharmacol. 2012;3:119.PubMedPubMedCentral
49.
go back to reference Meizlish ML, Pine AB, Goshua G, Chang C-H, Zhang H, Bishai J, et al. Circulating markers of angiogenesis and endotheliopathy in COVID-19. Pulm Circ. 2020;10:2045894020966547.PubMedPubMedCentral Meizlish ML, Pine AB, Goshua G, Chang C-H, Zhang H, Bishai J, et al. Circulating markers of angiogenesis and endotheliopathy in COVID-19. Pulm Circ. 2020;10:2045894020966547.PubMedPubMedCentral
50.
go back to reference Beltrán-Camacho L, Eslava-Alcón S, Rojas-Torres M, Sánchez-Morillo D, Martinez-Nicolás MaP, Martín-Bermejo V, et al. The serum of COVID-19 asymptomatic patients up-regulates proteins related to endothelial dysfunction and viral response in circulating angiogenic cells ex-vivo. Mol Med. 2022;28:1–16. Beltrán-Camacho L, Eslava-Alcón S, Rojas-Torres M, Sánchez-Morillo D, Martinez-Nicolás MaP, Martín-Bermejo V, et al. The serum of COVID-19 asymptomatic patients up-regulates proteins related to endothelial dysfunction and viral response in circulating angiogenic cells ex-vivo. Mol Med. 2022;28:1–16.
51.
go back to reference Willems LH, Jacobs LMC, Groh LA, ten Cate H, Spronk HMH, Wilson-Storey B, et al. Vascular Function, Systemic Inflammation, and Coagulation Activation 18 Months after COVID-19 Infection: An Observational Cohort Study. J Clin Med. 2023;12. Willems LH, Jacobs LMC, Groh LA, ten Cate H, Spronk HMH, Wilson-Storey B, et al. Vascular Function, Systemic Inflammation, and Coagulation Activation 18 Months after COVID-19 Infection: An Observational Cohort Study. J Clin Med. 2023;12.
52.
go back to reference Ungvari Z, Tarantini S, Kiss T, Wren JD, Giles CB, Griffin CT, et al. Endothelial dysfunction and angiogenesis impairment in the ageing vasculature. Nat Rev Cardiol. 2018;15:555–65.PubMedPubMedCentral Ungvari Z, Tarantini S, Kiss T, Wren JD, Giles CB, Griffin CT, et al. Endothelial dysfunction and angiogenesis impairment in the ageing vasculature. Nat Rev Cardiol. 2018;15:555–65.PubMedPubMedCentral
53.
go back to reference Zhu R, Liu TW, Liu F. Exogenous urokinase inhibits proteasomal degradation of its cognate urokinase plasminogen activator receptor. Front Pharmacol. 2022;13: 754271.PubMedPubMedCentral Zhu R, Liu TW, Liu F. Exogenous urokinase inhibits proteasomal degradation of its cognate urokinase plasminogen activator receptor. Front Pharmacol. 2022;13: 754271.PubMedPubMedCentral
54.
go back to reference Lang IM, Moser KM, Schleef RR. Elevated expression of urokinase-like plasminogen activator and plasminogen activator inhibitor type 1 during the vascular remodeling associated with pulmonary thromboembolism. Arterioscler Thromb Vasc Biol. 1998;18:808–15.PubMed Lang IM, Moser KM, Schleef RR. Elevated expression of urokinase-like plasminogen activator and plasminogen activator inhibitor type 1 during the vascular remodeling associated with pulmonary thromboembolism. Arterioscler Thromb Vasc Biol. 1998;18:808–15.PubMed
56.
go back to reference Bontekoe E, Brailovsky Y, Hoppensteadt D, Bontekoe J, Siddiqui F, Newman J, et al. Upregulation of inflammatory cytokines in pulmonary embolism using biochip-array profiling. Clin Appl Thromb. 2021;27:1–9. Bontekoe E, Brailovsky Y, Hoppensteadt D, Bontekoe J, Siddiqui F, Newman J, et al. Upregulation of inflammatory cytokines in pulmonary embolism using biochip-array profiling. Clin Appl Thromb. 2021;27:1–9.
57.
go back to reference Smadja DM, Laurendeau I, Avignon C, Vidaud M, Aiach M, Gaussem P. The angiopoietin pathway is modulated by PAR-1 activation on human endothelial progenitor cells. J Thromb Haemost. 2006;4:2051–8.PubMed Smadja DM, Laurendeau I, Avignon C, Vidaud M, Aiach M, Gaussem P. The angiopoietin pathway is modulated by PAR-1 activation on human endothelial progenitor cells. J Thromb Haemost. 2006;4:2051–8.PubMed
58.
go back to reference Lopez-Leon S, Wegman-Ostrosky T, Perelman C, Sepulveda R, Rebolledo PA, Cuapio A, et al. More than 50 long-term effects of COVID-19: a systematic review and meta-analysis. Sci Rep. 2021;11:16144.PubMedPubMedCentral Lopez-Leon S, Wegman-Ostrosky T, Perelman C, Sepulveda R, Rebolledo PA, Cuapio A, et al. More than 50 long-term effects of COVID-19: a systematic review and meta-analysis. Sci Rep. 2021;11:16144.PubMedPubMedCentral
59.
go back to reference Sykes DL, Holdsworth L, Jawad N, Gunasekera P, Morice AH, Crooks MG. Post-COVID-19 Symptom Burden: What is Long-COVID and How Should We Manage It? Lung. 2021;199:113–9.PubMedPubMedCentral Sykes DL, Holdsworth L, Jawad N, Gunasekera P, Morice AH, Crooks MG. Post-COVID-19 Symptom Burden: What is Long-COVID and How Should We Manage It? Lung. 2021;199:113–9.PubMedPubMedCentral
60.
go back to reference Huang C, Huang L, Wang Y, Li X, Ren L, Gu X, et al. 6-month consequences of COVID-19 in patients discharged from hospital: a cohort study. Lancet. 2021;397:220–32.PubMedPubMedCentral Huang C, Huang L, Wang Y, Li X, Ren L, Gu X, et al. 6-month consequences of COVID-19 in patients discharged from hospital: a cohort study. Lancet. 2021;397:220–32.PubMedPubMedCentral
Metadata
Title
Endothelial dysfunction and cardiovascular risk in post-COVID-19 patients after 6- and 12-months SARS-CoV-2 infection
Authors
Paula Poyatos
Neus Luque
Gladis Sabater
Saioa Eizaguirre
Marc Bonnin
Ramon Orriols
Olga Tura-Ceide
Publication date
07-02-2024
Publisher
Springer Berlin Heidelberg
Published in
Infection / Issue 4/2024
Print ISSN: 0300-8126
Electronic ISSN: 1439-0973
DOI
https://doi.org/10.1007/s15010-024-02173-5

Keynote series | Spotlight on managing health in obesity

Obesity is a major contributor to cardiorenal metabolic disease, but its impact extends throughout the body. Understand how obesity can affect other organ systems and impact treatment, and whether weight-loss measures improve outcomes.

Prof. Eva L. Feldman
Prof. Jonette Keri
Developed by: Springer Medicine
Watch now
Video

Women’s health knowledge hub

Elevate your patient care with our comprehensive, evidence-based medical education on women's health. Designed to help you provide exceptional care for your female patients at every stage of life, we provide expert insights into topics such as reproductive health, menopause, breast cancer and sex-specific health risks and precision medicine.

Read more

Keynote webinar | Spotlight on advances in lupus

  • Live
  • Webinar | 27-05-2025 | 18:00 (CEST)

Systemic lupus erythematosus is a severe autoimmune disease that can cause damage to almost every system of the body. Join this session to learn more about novel biomarkers for diagnosis and monitoring and familiarise yourself with current and emerging targeted therapies.

Join us live: Tuesday 27th May, 18:00-19:15 (CEST)

Prof. Edward Vital
Prof. Ronald F. van Vollenhoven
Developed by: Springer Medicine
Register now
Webinar