Clinical assessment of endothelial function in convalescent COVID-19 patients: a meta-analysis with meta-regressions

References

• Guan WJ, Ni ZY, Hu Y, et al. Clinical characteristics of coronavirus disease 2019 in China. N Engl J Med. 2020;382(18):1708–1720.
   PubMed Web of Science ®Google Scholar
• Kampf G. The epidemiological relevance of the COVID-19-vaccinated population is increasing. Lancet Reg Health Eur. 2021;11:100272.
   PubMedGoogle Scholar
• Yang BY, Barnard LM, Emert JM, et al. Clinical characteristics of patients with coronavirus disease 2019 (COVID-19) receiving emergency medical services in king county, Washington. JAMA Netw Open. 2020;3(7):e2014549.
   PubMed Web of Science ®Google Scholar
• Ambrosino P, Papa A, Maniscalco M, et al. COVID-19 and functional disability: current insights and rehabilitation strategies. Postgrad Med J. 2021;97(1149):469–470.
   PubMed Web of Science ®Google Scholar
• Nalbandian A, Sehgal K, Gupta A, et al. Post-acute COVID-19 syndrome. Nat Med. 2021;27(4):601–615.
   PubMed Web of Science ®Google Scholar
• Xie Y, Xu E, Bowe B, et al. Long-term cardiovascular outcomes of COVID-19. Nat Med. 2022;28(3):583–590.
   PubMed Web of Science ®Google Scholar
• Curci C, Pisano F, Bonacci E, et al. Early rehabilitation in post-acute COVID-19 patients: data from an italian COVID-19 rehabilitation unit and proposal of a treatment protocol. Eur J Phys Rehabil Med. 2020;56(5):633–641.
   PubMed Web of Science ®Google Scholar
• Wang TJ, Chau B, Lui M, et al. Physical medicine and rehabilitation and pulmonary rehabilitation for COVID-19. Am J Phys Med Rehabil. 2020;99(9):769–774.
   PubMed Web of Science ®Google Scholar
• Groff D, Sun A, Ssentongo AE, et al. Short-term and long-term rates of postacute sequelae of SARS-CoV-2 infection: a systematic review. JAMA Netw Open. 2021;4(10):e2128568.
   PubMed Web of Science ®Google Scholar
• Gluckman TJ, Bhave NM, Allen LA, et al. 2022 ACC expert consensus decision pathway on cardiovascular sequelae of COVID-19 in adults: myocarditis and other myocardial involvement, post-acute sequelae of SARS-CoV-2 infection, and return to play: a report of the American college of cardiology solution set oversight committee. J Am Coll Cardiol. 2022;79(17):1717–1756.
   PubMed Web of Science ®Google Scholar
• Ambrosino P, Calcaterra IL, Mosella M, et al. Endothelial dysfunction in COVID-19: a unifying mechanism and a potential therapeutic target. Biomedicines. 2022;10(4):812.
   PubMed Web of Science ®Google Scholar
• Crook H, Raza S, Nowell J, et al. Long covid-mechanisms, risk factors, and management. BMJ. 2021;374:n1648.
   PubMedGoogle Scholar
• Evans PC, Rainger GE, Mason JC, et al. Endothelial dysfunction in COVID-19: a position paper of the ESC working group for atherosclerosis and vascular biology, and the ESC council of basic cardiovascular science. Cardiovasc Res. 2020;116(14):2177–2184.
   PubMed Web of Science ®Google Scholar
• Matsuzawa Y, Kwon TG, Lennon RJ, et al. Prognostic value of Flow-Mediated vasodilation in brachial artery and fingertip artery for cardiovascular events: a systematic review and Meta-Analysis. J Am Heart Assoc. 2015;4(11):e002270.
   PubMed Web of Science ®Google Scholar
• Oikonomou E, Souvaliotis N, Lampsas S, et al. Endothelial dysfunction in acute and long standing COVID-19: a prospective cohort study. Vascul Pharmacol. 2022;144:106975.
   PubMed Web of Science ®Google Scholar
• Ratchford SM, Stickford JL, Province VM, et al. Vascular alterations among young adults with SARS-CoV-2. Am J Physiol Heart Circ Physiol. 2021;320(1):H404–H410.
   PubMed Web of Science ®Google Scholar
• Jud P, Gressenberger P, Muster V, et al. Evaluation of endothelial dysfunction and inflammatory vasculopathy after SARS-CoV-2 infection-A cross-sectional study. Front Cardiovasc Med. 2021;8:750887.
   PubMed Web of Science ®Google Scholar
• Skow RJ, Nandadeva D, Grotle AK, et al. Impact of breakthrough COVID-19 cases during the omicron wave on vascular health and cardiac autonomic function in young adults. Am J Physiol Heart Circ Physiol. 2022;323:H59–H64.
   PubMed Web of Science ®Google Scholar
• Moher D, Liberati A, Tetzlaff J, et al. Preferred reporting items for systematic reviews and Meta-analyses: the PRISMA statement. PLoS Med. 2009;6(7):e1000097.
   PubMed Web of Science ®Google Scholar
• Ottawa Hospital Research Institute. The Newcastle-Ottawa Scale (NOS) for assessing the quality of nonrandomized studies in meta-analyses. Available from: http://www.ohri.ca/programs/clinical_epidemiology/oxford.asp
   Google Scholar
• IntHout J, Ioannidis JP, Rovers MM, et al. Plea for routinely presenting prediction intervals in Meta-analysis. BMJ Open. 2016;6(7):e010247.
   PubMed Web of Science ®Google Scholar
• Borenstein M, Hedges LV, Higgins JP, et al. A basic introduction to fixed-effect and random-effects models for Meta-analysis. Res Synth Methods. 2010;1(2):97–111.
   PubMed Web of Science ®Google Scholar
• Cheung MW. A guide to conducting a Meta-Analysis with non-independent effect sizes. Neuropsychol Rev. 2019;29(4):387–396.
   PubMed Web of Science ®Google Scholar
• Higgins JP, Thompson SG, Deeks JJ, et al. Measuring inconsistency in Meta-analyses. BMJ. 2003;327(7414):557–560.
   PubMed Web of Science ®Google Scholar
• Sterne JA, Egger M, Smith GD. Systematic reviews in health care: investigating and dealing with publication and other biases in Meta-analysis. BMJ. 2001;323(7304):101–105.
   PubMed Web of Science ®Google Scholar
• Duval S, Tweedie R. Trim and fill: a simple funnel-plot-based method of testing and adjusting for publication bias in Meta-analysis. Biometrics. 2000;56(2):455–463.
   PubMed Web of Science ®Google Scholar
• Inaba Y, Chen JA, Bergmann SR. Prediction of future cardiovascular outcomes by flow-mediated vasodilatation of brachial artery: a Meta-analysis. Int J Cardiovasc Imaging. 2010;26(6):631–640.
   PubMed Web of Science ®Google Scholar
• Mathur MB, VanderWeele TJ. Sensitivity analysis for unmeasured confounding in meta-analyses. J Am Stat Assoc. 2020;115(529):163–172.
   PubMed Web of Science ®Google Scholar
• Johnston R, Jones K, Manley D. Confounding and collinearity in regression analysis: a cautionary tale and an alternative procedure, illustrated by studies of british voting behaviour. Qual Quant. 2018;52(4):1957–1976.
   PubMedGoogle Scholar
• Ambrosino P, Calcaterra I, Molino A, et al. Persistent endothelial dysfunction in post-acute COVID-19 syndrome: a case-control study. Biomedicines. 2021;9(8):957.
   PubMed Web of Science ®Google Scholar
• Ciftel M, Ates N, Yilmaz O. Investigation of endothelial dysfunction and arterial stiffness in multisystem inflammatory syndrome in children. Eur J Pediatr. 2022;181(1):91–97.
   PubMed Web of Science ®Google Scholar
• Ergül E, Yılmaz AS, Öğütveren MM, et al. COVID 19 disease independently predicted endothelial dysfunction measured by flow-mediated dilatation. Int J Cardiovasc Imaging. 2022;38(1):25–32.
   PubMed Web of Science ®Google Scholar
• Gao YP, Zhou W, Huang PN, et al. Persistent endothelial dysfunction in coronavirus disease-2019 survivors late after recovery. Front Med (Lausanne). 2022;9:809033.
   PubMed Web of Science ®Google Scholar
• Lambadiari V, Mitrakou A, Kountouri A, et al. Association of COVID-19 with impaired endothelial glycocalyx, vascular function and myocardial deformation 4 months after infection. Eur J Heart Fail. 2021;23(11):1916–1926.
   PubMed Web of Science ®Google Scholar
• Nandadeva D, Young BE, Stephens BY, et al. Blunted peripheral but not cerebral vasodilator function in young otherwise healthy adults with persistent symptoms following COVID-19. Am J Physiol Heart Circ Physiol. 2021;321(3):H479–H484.
   PubMed Web of Science ®Google Scholar
• Riou M, Oulehri W, Momas C, et al. Reduced flow-mediated dilatation is not related to COVID-19 severity three months after hospitalization for SARS-CoV-2 infection. J Clin Med. 2021;10(6):1318.
   PubMed Web of Science ®Google Scholar
• Mansiroglu AK, Seymen H, Sincer I, et al. Evaluation of endothelial dysfunction in COVID-19 with Flow-Mediated dilatation. Arq Bras Cardiol. 2022;119:319–325.
   PubMed Web of Science ®Google Scholar
• Castro P, Palomo M, Moreno-Castano AB, et al. Is the endothelium the missing link in the pathophysiology and treatment of COVID-19 complications? Cardiovasc Drugs Ther. 2022;36(3):547–560.
   PubMed Web of Science ®Google Scholar
• Libby P, Luscher T. COVID-19 is, in the end, an endothelial disease. Eur Heart J. 2020;41(32):3038–3044.
   PubMed Web of Science ®Google Scholar
• Agostini F, Mangone M, Ruiu P, et al. Rehabilitation setting during and after covid-19: an overview on recommendations. J Rehabil Med. 2021;53(1):jrm00141.
   PubMed Web of Science ®Google Scholar
• Polastri M, Nava S, Clini E, et al. COVID-19 and pulmonary rehabilitation: preparing for phase three. Eur Respir J. 2020;55(6):2001822.
   PubMed Web of Science ®Google Scholar
• Lopez-Leon S, Wegman-Ostrosky T, Perelman C, et al. More than 50 long-term effects of COVID-19: a systematic review and Meta-analysis. Sci Rep. 2021;11(1):16144.
   PubMed Web of Science ®Google Scholar
• Chen Y, Ding C, Yu L, et al. One-year follow-up of chest CT findings in patients after SARS-CoV-2 infection. BMC Med. 2021;19(1):191.
   PubMed Web of Science ®Google Scholar
• Barini M, Percivale I, Danna P, et al. 18 Months computed tomography follow-up after covid-19 interstitial pneumonia. J Public Health Res. 2022;11(2):2782.
   PubMed Web of Science ®Google Scholar
• Peluso MJ, Lu S, Tang AF, et al. Markers of immune activation and inflammation in individuals with postacute sequelae of severe acute respiratory syndrome coronavirus 2 infection. J Infect Dis. 2021;224(11):1839–1848.
   PubMed Web of Science ®Google Scholar
• Visvabharathy L, Hanson B, Orban Z, et al. Neuro-COVID long-haulers exhibit broad dysfunction in T cell memory generation and responses to vaccination. MedRxiv. 2021.
   Google Scholar
• Gold JE, Okyay RA, Licht WE, et al. Investigation of long COVID prevalence and its relationship to Epstein-Barr virus reactivation. Pathogens. 2021;10(6):763.
   PubMed Web of Science ®Google Scholar
• Wang EY, Mao T, Klein J, et al. Diverse functional autoantibodies in patients with COVID-19. Nature. 2021;595(7866):283–288.
   PubMed Web of Science ®Google Scholar
• Rinaldo RF, Mondoni M, Parazzini EM, et al. Deconditioning as main mechanism of impaired exercise response in COVID-19 survivors. Eur Respir J. 2021;58(2):2100870.
   PubMed Web of Science ®Google Scholar
• Varga Z, Flammer AJ, Steiger P, et al. Endothelial cell infection and endotheliitis in COVID-19. Lancet. 2020;395(10234):1417–1418.
   PubMed Web of Science ®Google Scholar
• Ackermann M, Verleden SE, Kuehnel M, et al. Pulmonary vascular endothelialitis, thrombosis, and angiogenesis in covid-19. N Engl J Med. 2020;383(2):120–128.
   PubMed Web of Science ®Google Scholar
• Kolivras A, Dehavay F, Delplace D, et al. Coronavirus (COVID-19) infection-induced chilblains: a case report with histopathologic findings. JAAD Case Rep. 2020;6(6):489–492.
   PubMedGoogle Scholar
• Mehrabadi ME, Hemmati R, Tashakor A, et al. Induced dysregulation of ACE2 by SARS-CoV-2 plays a key role in COVID-19 severity. Biomed Pharmacother. 2021;137:111363.
   PubMed Web of Science ®Google Scholar
• Gheblawi M, Wang K, Viveiros A, et al. Angiotensin-converting enzyme 2: SARS-CoV-2 receptor and regulator of the Renin-Angiotensin system: celebrating the 20th anniversary of the discovery of ACE2. Circ Res. 2020;126(10):1456–1474.
   PubMed Web of Science ®Google Scholar
• McCracken IR, Saginc G, He L, et al. Lack of evidence of Angiotensin-Converting enzyme 2 expression and replicative infection by SARS-CoV-2 in human endothelial cells. Circulation. 2021;143(8):865–868.
   PubMed Web of Science ®Google Scholar
• Lee C, Lim HK, Sakong J, et al. Janus kinase-signal transducer and activator of transcription mediates phosphatidic acid-induced interleukin (IL)-1beta and IL-6 production. Mol Pharmacol. 2006;69(3):1041–1047.
   PubMed Web of Science ®Google Scholar
• Chernyak BV, Popova EN, Prikhodko AS, et al. COVID-19 and oxidative stress. Biochemistry (Mosc). 2020;85(12):1543–1553.
   PubMed Web of Science ®Google Scholar
• Calabretta E, Moraleda JM, Iacobelli M, et al. COVID-19-induced endotheliitis: emerging evidence and possible therapeutic strategies. Br J Haematol. 2021;193(1):43–51.
   PubMed Web of Science ®Google Scholar
• Matsuishi Y, Mathis BJ, Shimojo N, et al. Severe COVID-19 infection associated with endothelial dysfunction induces multiple organ dysfunction: a review of therapeutic interventions. Biomedicines. 2021;9(3):279.
   PubMed Web of Science ®Google Scholar
• Di Minno MN, Ambrosino P, Peluso R, et al. Lipid profile changes in patients with rheumatic diseases receiving a treatment with TNF-alpha blockers: a Meta-analysis of prospective studies. Ann Med. 2014;46(2):73–83.
   PubMed Web of Science ®Google Scholar
• Hottz ED, Azevedo-Quintanilha IG, Palhinha L, et al. Platelet activation and platelet-monocyte aggregate formation trigger tissue factor expression in patients with severe COVID-19. Blood. 2020;136(11):1330–1341.
   PubMed Web of Science ®Google Scholar
• Merad M, Martin JC. Pathological inflammation in patients with COVID-19: a key role for monocytes and macrophages. Nat Rev Immunol. 2020;20(6):355–362.
   PubMed Web of Science ®Google Scholar
• Raman B, Bluemke DA, Luscher TF, et al. Long COVID: post-acute sequelae of COVID-19 with a cardiovascular focus. Eur Heart J. 2022;43(11):1157–1172.
   PubMed Web of Science ®Google Scholar
• Moretta P, Maniscalco M, Papa A, et al. Cognitive impairment and endothelial dysfunction in convalescent COVID-19 patients undergoing rehabilitation. Eur J Clin Invest. 2022;52(2):e13726.
   PubMed Web of Science ®Google Scholar
• Ambrosino P, Parrella P, Formisano R, et al. Cardiopulmonary exercise performance and endothelial function in convalescent COVID-19 patients. J Clin Med. 2022;11(5):1452.
   PubMed Web of Science ®Google Scholar
• Fan BE, Wong SW, Sum CLL, et al. Hypercoagulability, endotheliopathy, and inflammation approximating 1 year after recovery: assessing the long-term outcomes in COVID-19 patients. Am J Hematol. 2022;97:915–923.
   PubMed Web of Science ®Google Scholar
• Haffke M, Freitag H, Rudolf G, et al. Endothelial dysfunction and altered endothelial biomarkers in patients with post-COVID-19 syndrome and chronic fatigue syndrome (ME/CFS). J Transl Med. 2022;20(1):138.
   PubMed Web of Science ®Google Scholar
• Corretti MC, Anderson TJ, Benjamin EJ, et al. Guidelines for the ultrasound assessment of endothelial-dependent flow-mediated vasodilation of the brachial artery: a report of the international brachial artery reactivity task force. J Am Coll Cardiol. 2002;39(2):257–265.
   PubMed Web of Science ®Google Scholar
• Heiss C, Rodriguez-Mateos A, Bapir M, et al. Flow-mediated dilation reference values for evaluation of endothelial function and cardiovascular health. Cardiovasc Res. 2022;Online ahead of print:cvac095.
   PubMed Web of Science ®Google Scholar
• Di Minno MN, Ambrosino P, Lupoli R, et al. Cardiovascular risk markers in patients with psoriatic arthritis: a Meta-analysis of literature studies. Ann Med. 2015;47(4):346–353.
   PubMed Web of Science ®Google Scholar
• Ambrosino P, Lupoli R, Tortora A, et al. Cardiovascular risk markers in patients with primary aldosteronism: a systematic review and Meta-analysis of literature studies. Int J Cardiol. 2016;208:46–55.
   PubMed Web of Science ®Google Scholar
• Ambrosino P, Lupoli R, Iervolino S, et al. Clinical assessment of endothelial function in patients with chronic obstructive pulmonary disease: a systematic review with Meta-analysis. Intern Emerg Med. 2017;12(6):877–885.
   PubMed Web of Science ®Google Scholar
• Cassar MP, Tunnicliffe EM, Petousi N, et al. Symptom persistence despite improvement in cardiopulmonary health - insights from longitudinal CMR, CPET and lung function testing post-COVID-19. EClinicalMedicine. 2021;41:101159.
   PubMedGoogle Scholar
• Evans RA, McAuley H, Harrison EM, et al. Physical, cognitive, and mental health impacts of COVID-19 after hospitalisation (PHOSP-COVID): a UK multicentre, prospective cohort study. Lancet Respir Med. 2021;9(11):1275–1287.
   PubMed Web of Science ®Google Scholar
• Sowers JR, Epstein M, Frohlich ED. Diabetes, hypertension, and cardiovascular disease: an update. Hypertension. 2001;37(4):1053–1059.
   PubMed Web of Science ®Google Scholar
• Corban MT, Lerman LO, Lerman A. Endothelial dysfunction. Arterioscler Thromb Vasc Biol. 2019;39(7):1272–1274.
   PubMed Web of Science ®Google Scholar
• Collard D, Nurmohamed NS, Kaiser Y, et al. Cardiovascular risk factors and COVID-19 outcomes in hospitalised patients: a prospective cohort study. BMJ Open. 2021;11(2):e045482.
   PubMed Web of Science ®Google Scholar
• Shah P, Owens J, Franklin J, et al. Demographics, comorbidities and outcomes in hospitalized covid-19 patients in rural southwest Georgia. Ann Med. 2020;52(7):354–360.
   PubMed Web of Science ®Google Scholar
• Nagele MP, Haubner B, Tanner FC, et al. Endothelial dysfunction in COVID-19: current findings and therapeutic implications. Atherosclerosis. 2020;314:58–62.
   PubMed Web of Science ®Google Scholar
• Diaz-Arocutipa C, Melgar-Talavera B, Alvarado-Yarasca A, et al. Statins reduce mortality in patients with COVID-19: an updated Meta-analysis of 147 824 patients. Int J Infect Dis. 2021;110:374–381.
   PubMed Web of Science ®Google Scholar
• Wu KS, Lin PC, Chen YS, et al. The use of statins was associated with reduced COVID-19 mortality: a systematic review and Meta-analysis. Ann Med. 2021;53(1):874–884.
   PubMed Web of Science ®Google Scholar
• Hasan SS, Kow CS, Hadi MA, et al. Mortality and disease severity among COVID-19 patients receiving Renin-Angiotensin system inhibitors: a systematic review and Meta-analysis. Am J Cardiovasc Drugs. 2020;20(6):571–590.
   PubMed Web of Science ®Google Scholar
• Wahlgren C, Divanoglou A, Larsson M, et al. Rehabilitation needs following COVID-19: five-month post-discharge clinical follow-up of individuals with concerning self-reported symptoms. EClinicalMedicine. 2022;43:101219.
   PubMedGoogle Scholar
• Dun Y, Liu C, Ripley-Gonzalez JW, et al. Six-month outcomes and effect of pulmonary rehabilitation among patients hospitalized with COVID-19: a retrospective cohort study. Ann Med. 2021;53(1):2099–2109.
   PubMed Web of Science ®Google Scholar
• Sinoway LI, Musch TI, Minotti JR, et al. Enhanced maximal metabolic vasodilatation in the dominant forearms of tennis players. J Appl Physiol (1985). 1986;61(2):673–678.
   PubMed Web of Science ®Google Scholar
• Ross MD, Malone E, Florida-James G. Vascular ageing and exercise: focus on cellular reparative processes. Oxid Med Cell Longev. 2016;2016:3583956.
   PubMed Web of Science ®Google Scholar
• Merlo C, Bernardi E, Bellotti F, et al. Supervised exercise training improves endothelial function in COPD patients: a method to reduce cardiovascular risk? ERJ Open Res. 2020;6(2):00304–2019.
   PubMedGoogle Scholar
• Kitzman DW, Brubaker PH, Herrington DM, et al. Effect of endurance exercise training on endothelial function and arterial stiffness in older patients with heart failure and preserved ejection fraction: a randomized, controlled, single-blind trial. J Am Coll Cardiol. 2013;62(7):584–592.
   PubMed Web of Science ®Google Scholar
• Dai R, Zhuo H, Chen Y, et al. Mechanism of isosorbide dinitrate combined with exercise training rehabilitation to mobilize endothelial progenitor cells in patients with coronary heart disease. Bioengineered. 2022;13(1):1126–1136.
   PubMedGoogle Scholar
• Lanza GA, Golino M, Villano A, et al. Cardiac rehabilitation and endothelial function. J Clin Med. 2020;9(8):2487.
   PubMed Web of Science ®Google Scholar
• Ambrosino P, Molino A, Calcaterra I, et al. Clinical assessment of endothelial function in convalescent COVID-19 patients undergoing multidisciplinary pulmonary rehabilitation. Biomedicines. 2021;9(6):614.
   PubMed Web of Science ®Google Scholar
• Maruhashi T, Soga J, Fujimura N, et al. Relationship between flow-mediated vasodilation and cardiovascular risk factors in a large community-based study. Heart. 2013;99(24):1837–1842.
   PubMed Web of Science ®Google Scholar