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Longitudinal strain and myocardial work in symptomatic patients having recovered from COVID-19 and possible associations with the severity of the disease

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Abstract

COVID-19 may have residual consequences in multiple organs, including the cardiovascular system. The purpose of the present investigation is to quantify myocardial function in symptomatic individuals with long COVID and investigate the association between illness severity and myocardial function. A retrospective cross-sectional study was conducted in which symptomatic individuals with previous COVID-19 underwent echocardiographic analysis of left ventricle global longitudinal strain (LVGLS) and myocardial work (MW). Individuals also performed cardiopulmonary testing (CPX) to assess peak oxygen uptake (VO2peak). Differences between illness severity subgroups were analyzed by the Mann–Whitney test. Correlations were calculated using the Spearman correlation test. Multilinear regressions were performed to evaluate the influences of COVID-19 severity, body mass index, age, and sex on MW. Fifty-six individuals were included (critical subgroup: 17; moderate/severe subgroup: 39), 59% females; median age: 56 years (IQR: 43–63). CPX revealed a substantial reduction in VO2peak (median of 53% of predicted values). LVGLS were not statistically different between subgroups. Global wasted work (GWW) was higher in the critical subgroup [146 (104–212) versus 121 (74–163) mmHg%, p = 0.01], and global work efficiency (GWE) was lower in this subgroup [93 (91–95) versus 94 (93–96), p = 0.03]. Illness severity was the only independent predictor of GWW and GWE (GWW: r2 = 0.167; p = 0.009; GWE: r2 = 0.172; p = 0.005) in multilinear regressions. In our study with long COVID-19 individuals, despite having a similar LVGLS, patients had subclinical LV dysfunction, demonstrated only by an increase in GWW and a decrease in GWE.

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The data supporting this article are available in the article and can be shared upon reasonable request to the corresponding author (A).

References

  1. Han E, Tan MMJ, Turk E, Sridhar D, Leung GM, Shibuya K et al (2020) Lessons learnt from easing COVID-19 restrictions: an analysis of countries and regions in Asia Pacific and Europe. Lancet 396(10261):1525–1534

    CAS  PubMed  PubMed Central  Google Scholar 

  2. Zhou P, Yang XL, Wang XG, Hu B, Zhang L, Zhang W et al (2020) A pneumonia outbreak associated with a new coronavirus of probable bat origin. Nature 579(7798):270–273

    CAS  PubMed  PubMed Central  Google Scholar 

  3. Gupta A, Madhavan MV, Sehgal K, Nair N, Mahajan S, Sehrawat TS et al (2020) Extrapulmonary manifestations of COVID-19. Nat Med 26(7):1017–1032

    CAS  PubMed  Google Scholar 

  4. Madjid M, Safavi-Naeini P, Solomon SD, Vardeny O (2020) Potential effects of coronaviruses on the cardiovascular system: a review. JAMA Cardiol 5(7):831–840

    PubMed  Google Scholar 

  5. Nishiga M, Wang DW, Han Y, Lewis DB, Wu JC (2020) COVID-19 and cardiovascular disease: from basic mechanisms to clinical perspectives. Nat Rev Cardiol 17(9):543–558

    CAS  PubMed  PubMed Central  Google Scholar 

  6. Driggin E, Madhavan MV, Bikdeli B, Chuich T, Laracy J, Biondi-Zoccai G et al (2020) Cardiovascular considerations for patients, health care workers, and health systems during the COVID-19 pandemic. J Am Coll Cardiol 75(18):2352–2371

    CAS  PubMed  PubMed Central  Google Scholar 

  7. Milani M, Milani JGPO, Cipriano GFB, Cahalin LP, Stein R, Cipriano Jr. G. Cardiopulmonary Exercise Testing in Post-COVID-19 Patients: Where Does Exercise Intolerance Come From? Arquivos Brasileiros de Cardiologia 120(2) https://doi.org/10.36660/abc.20220150

  8. Szekely Y, Lichter Y, Taieb P, Banai A, Hochstadt A, Merdler I et al (2020) Spectrum of cardiac manifestations in COVID-19: a systematic echocardiographic study. Circulation 142(4):342–353

    CAS  PubMed  PubMed Central  Google Scholar 

  9. Rey JR, Caro-Codon J, Rosillo SO, Iniesta AM, Castrejon-Castrejon S, Marco-Clement I et al (2020) Heart failure in COVID-19 patients: prevalence, incidence and prognostic implications. Eur J Heart Fail 22(12):2205–2215

    CAS  PubMed  Google Scholar 

  10. Carfi A, Bernabei R, Landi F (2020) Gemelli against C-P-ACSG persistent symptoms in patients after acute COVID. JAMA 324(6):603–605

    CAS  PubMed  PubMed Central  Google Scholar 

  11. Huang C, Huang L, Wang Y, Li X, Ren L, Gu X et al (2021) 6-month consequences of COVID-19 in patients discharged from hospital: a cohort study. Lancet 397(10270):220–232

    CAS  PubMed  PubMed Central  Google Scholar 

  12. Puntmann VO, Carerj ML, Wieters I, Fahim M, Arendt C, Hoffmann J et al (2020) Outcomes of Cardiovascular Magnetic Resonance Imaging in Patients Recently Recovered From Coronavirus Disease 2019 (COVID-19). JAMA Cardiol 5(11):1265–1273

    PubMed  PubMed Central  Google Scholar 

  13. Rajpal S, Tong MS, Borchers J, Zareba KM, Obarski TP, Simonetti OP et al (2021) Cardiovascular magnetic resonance findings in competitive athletes recovering from COVID-19 infection. JAMA Cardiol 6(1):116–118

    PubMed  Google Scholar 

  14. Kotecha T, Knight DS, Razvi Y, Kumar K, Vimalesvaran K, Thornton G et al (2021) Patterns of myocardial injury in recovered troponin-positive COVID-19 patients assessed by cardiovascular magnetic resonance. Eur Heart J 42(19):1866–1878

    CAS  PubMed  PubMed Central  Google Scholar 

  15. Moody WE, Liu B, Mahmoud-Elsayed HM, Senior J, Lalla SS, Khan-Kheil AM et al (2021) Persisting adverse ventricular remodeling in COVID-19 survivors: a longitudinal echocardiographic study. J Am Soc Echocardiogr 34(5):562–566

    PubMed  PubMed Central  Google Scholar 

  16. Tryfou ES, Kostakou PM, Chasikidis CG, Kostopoulos VS, Serafetinidis II, Ferdianaki EK et al (2021) Biventricular myocardial function in Covid-19 recovered patients assessed by speckle tracking echocardiography: a prospective cohort echocardiography study. Int J Cardiovasc Imaging 38(5):995–1003

    PubMed  PubMed Central  Google Scholar 

  17. Herrmann J, Lenihan D, Armenian S, Barac A, Blaes A, Cardinale D et al (2022) Defining cardiovascular toxicities of cancer therapies: an International Cardio-Oncology Society (IC-OS) consensus statement. Eur Heart J 43(4):280–299

    PubMed  Google Scholar 

  18. Laufer-Perl M, Arnold JH, Mor L, Amrami N, Derakhshesh M, Moshkovits Y et al (2020) The association of reduced global longitudinal strain with cancer therapy-related cardiac dysfunction among patients receiving cancer therapy. Clin Res Cardiol 109(2):255–262

    CAS  PubMed  Google Scholar 

  19. Houard L, Benaets MB et al (2019) Additional prognostic value of 2d right ventricular speckle-tracking strain for prediction of survival in heart failure and reduced ejection fraction: a comparative study with cardiac magnetic resonance. JACC Cardiovasc Imaging. 12(12):2373–2385

    PubMed  Google Scholar 

  20. Russell K, Eriksen M, Aaberge L, Wilhelmsen N, Skulstad H, Remme EW et al (2012) A novel clinical method for quantification of regional left ventricular pressure-strain loop area: a non-invasive index of myocardial work. Eur Heart J 33(6):724–733

    PubMed  PubMed Central  Google Scholar 

  21. Russell K, Eriksen M, Aaberge L, Wilhelmsen N, Skulstad H, Gjesdal O et al (2013) Assessment of wasted myocardial work: a novel method to quantify energy loss due to uncoordinated left ventricular contractions. Am J Physiol Heart Circ Physiol 305(7):H996-1003

    CAS  PubMed  Google Scholar 

  22. Roemer S, Jaglan A, Santos D, Umland M, Jain R, Tajik AJ et al (2021) The utility of myocardial work in clinical practice. J Am Soc Echocardiogr 34(8):807–818

    PubMed  Google Scholar 

  23. COVID-19 Treatment Guidelines Panel. Coronavirus Disease 2019 (COVID-19) Treatment Guidelines. [Internet]. 2022 [cited https://www.covid19treatmentguidelines.nih.gov].

  24. A clinical case definition of post COVID-19 condition by a Delphi consensus [Internet]. 2021 [cited WHO/2019-nCoV/Post_COVID-19_condition/Clinical_case_definition/2021.1].

  25. Raveendran AV, Jayadevan R, Sashidharan S (2021) Long COVID: an overview. Diabetes Metab Syndr 15(3):869–875

    CAS  PubMed  PubMed Central  Google Scholar 

  26. Balady GJ, Arena R, Sietsema K, Myers J, Coke L, Fletcher GF et al (2010) Clinician’s guide to cardiopulmonary exercise testing in adults: a scientific statement from the American Heart Association. Circulation 122(2):191–225

    PubMed  Google Scholar 

  27. Herdy AH, Ritt LE, Stein R, Araujo CG, Milani M, Meneghelo RS et al (2016) Cardiopulmonary exercise test: background, applicability and interpretation. Arq Bras Cardiol 107(5):467–481

    CAS  PubMed  PubMed Central  Google Scholar 

  28. Meneghelo RSAC, Stein R, Mastrocolla LE, Albuquerque PF, Serra SM et al (2010) III Diretrizes da Sociedade Brasileira de Cardiologia Sobre Teste Ergométrico. Arq Bras Cardiol 95(5):1–26

    Google Scholar 

  29. Juliana Goulart Prata Oliveira, Milani Mauricio, Milani Graziella França Bernardelli, Cipriano Isac, de Castro Dominique, Hansen Gerson, Cipriano Junior (2023) Oxygen Uptake Efficiency Slope in South American Healthy Adults Journal of Cardiopulmonary Rehabilitation and Prevention 43(4) 290–300 https://doi.org/10.1097/hcr.0000000000000778

  30. ReizoBaba M, Nagashima M, Goto M, Nagano Y, Yokota M, Tauchi N, Nishibata K (1996) Oxygen Uptake Efficjenq’ Slop’e: A ‘New Index of Cardiorespiratory, FuntitJonal reserve derived from the relation between oxygen uptake and minute ventilation during incremental exercise. J Am College Cardiol 28:1567–1572

    Google Scholar 

  31. Milani M, Milani J, Cipriano GFB, de Castro I, Cipriano JG (2022) Reference standards for cardiorespiratory fitness in Brazil: A Pooled Analysis And Overview Of Heterogeneity In National And International Studies. J Cardiopulm Rehabil Prev 42(5):366–372

    PubMed  Google Scholar 

  32. Hirofumi Tanaka P, Monahan KD, Seals DR (2001) Age-predicted maximal heart rate revisited. J Am College Cardiol 37:153–156

    Google Scholar 

  33. Lang RM, Badano LP, Mor-Avi V, Afilalo J, Armstrong A, Ernande L et al (2015) Recommendations for cardiac chamber quantification by echocardiography in adults: an update from the American Society of Echocardiography and the European Association of Cardiovascular Imaging. Eur Heart J Cardiovasc Imaging 16(3):233–270

    PubMed  Google Scholar 

  34. Nagueh SF, Smiseth OA, Appleton CP, Byrd BF 3rd, Dokainish H, Edvardsen T et al (2016) Recommendations for the evaluation of left ventricular diastolic function by echocardiography: an update from the American Society of Echocardiography and the European Association of Cardiovascular Imaging. J Am Soc Echocardiogr 29(4):277–314

    PubMed  Google Scholar 

  35. Voigt JU, Pedrizzetti G, Lysyansky P, Marwick TH, Houle H, Baumann R et al (2015) Definitions for a common standard for 2D speckle tracking echocardiography: consensus document of the EACVI/ASE/Industry Task Force to standardize deformation imaging. Eur Heart J Cardiovasc Imaging 16(1):1–11

    CAS  PubMed  Google Scholar 

  36. Badano LP, Kolias TJ, Muraru D, Abraham TP, Aurigemma G, Edvardsen T et al (2018) Standardization of left atrial, right ventricular, and right atrial deformation imaging using two-dimensional speckle tracking echocardiography: a consensus document of the EACVI/ASE/Industry Task Force to standardize deformation imaging. Eur Heart J Cardiovasc Imaging 19(6):591–600

    PubMed  Google Scholar 

  37. Papadopoulos K, OzdenTok O, Mitrousi K, Ikonomidis I (2021) Myocardial work: methodology and clinical applications. Diagnostics 11:3

    Google Scholar 

  38. Manganaro R, Marchetta S, Dulgheru R, Ilardi F, Sugimoto T, Robinet S et al (2019) Echocardiographic reference ranges for normal non-invasive myocardial work indices: results from the EACVI NORRE study. Eur Heart J Cardiovasc Imaging 20(5):582–590

    PubMed  Google Scholar 

  39. Raman B, Bluemke DA, Luscher TF, Neubauer S (2022) Long COVID: post-acute sequelae of COVID-19 with a cardiovascular focus. Eur Heart J 43(11):1157–1172

    CAS  PubMed  PubMed Central  Google Scholar 

  40. Singh I, Joseph P, Heerdt PM, Cullinan M, Lutchmansingh DD, Gulati M et al (2022) Persistent exertional intolerance after covid-19: insights from invasive cardiopulmonary exercise testing. Chest 161(1):54–63

    CAS  PubMed  Google Scholar 

  41. Baratto C, Caravita S, Faini A, Perego GB, Senni M, Badano LP et al (2021) Impact of COVID-19 on exercise pathophysiology: a combined cardiopulmonary and echocardiographic exercise study. J Appl Physiol 130(5):1470–1478

    CAS  PubMed  PubMed Central  Google Scholar 

  42. Minhas AS, Gilotra NA, Goerlich E, Metkus T, Garibaldi BT, Sharma G et al (2021) Myocardial work efficiency, a novel measure of myocardial dysfunction, is reduced in covid-19 patients and associated with in-hospital mortality. Front Cardiovasc Med 8:667721

    PubMed  PubMed Central  Google Scholar 

  43. Mahajan S, Kunal S, Shah B, Garg S, Palleda GM, Bansal A et al (2021) Left ventricular global longitudinal strain in COVID-19 recovered patients. Echocardiography 38(10):1722–1730

    PubMed  PubMed Central  Google Scholar 

  44. Sorensen J, Harms HJ, Aalen JM, Baron T, Smiseth OA, Flachskampf FA (2020) Myocardial efficiency: a fundamental physiological concept on the verge of clinical impact. JACC Cardiovasc Imaging 13(7):1564–1576

    PubMed  Google Scholar 

  45. Lairez O, Blanchard V, Houard V, Vardon-Bounes F, Lemasle M, Cariou E et al (2021) Cardiac imaging phenotype in patients with coronavirus disease 2019 (COVID-19): results of the cocarde study. Int J Cardiovasc Imaging 37(2):449–457

    PubMed  Google Scholar 

  46. Luchian ML, Motoc A, Lochy S, Magne J, Belsack D, De Mey J et al (2021) Subclinical myocardial dysfunction in patients with persistent dyspnea one year after covid-19. Diagnostics 12(1):57

    PubMed  PubMed Central  Google Scholar 

  47. Cui C, Li Y, Liu Y, Huang D, Hu Y, Wang Y et al (2021) Association between echocardiographic non-invasive myocardial work indices and myocardial fibrosis in patients with dilated cardiomyopathy. Front Cardiovasc Med 8:704251

    PubMed  PubMed Central  Google Scholar 

  48. Petrilli CM, Jones SA, Yang J, Rajagopalan H, O’Donnell L, Chernyak Y et al (2020) Factors associated with hospital admission and critical illness among 5279 people with coronavirus disease 2019 in New York City: prospective cohort study. BMJ 369:m1966

    PubMed  PubMed Central  Google Scholar 

  49. Gupta S, Hayek SS, Wang W, Chan L, Mathews KS, Melamed ML et al (2020) Factors associated with death in critically ill patients with coronavirus disease 2019 in the US. JAMA Intern Med 180(11):1436–1447

    CAS  PubMed  Google Scholar 

  50. Clark A, Jit M, Warren-Gash C, Guthrie B, Wang HHX, Mercer SW et al (2020) Global, regional, and national estimates of the population at increased risk of severe COVID-19 due to underlying health conditions in 2020: a modelling study. Lancet Glob Health 8(8):e1003–e1017

    PubMed  PubMed Central  Google Scholar 

  51. Sharma J, Rajput R, Bhatia M, Arora P, Sood V (2021) Clinical predictors of covid-19 severity and mortality: a perspective. Front Cell Infect Microbiol 11:674277

    CAS  PubMed  PubMed Central  Google Scholar 

  52. Morbach C, Sahiti F, Tiffe T, Cejka V, Eichner FA, Gelbrich G et al (2020) Myocardial work - correlation patterns and reference values from the population-based STAAB cohort study. PLoS ONE 15(10):e0239684

    CAS  PubMed  PubMed Central  Google Scholar 

  53. Sahiti F, Morbach C, Cejka V, Tiffe T, Wagner M, Eichner FA et al (2022) Impact of cardiovascular risk factors on myocardial work-insights from the STAAB cohort study. J Hum Hypertens 36(3):235–245

    PubMed  Google Scholar 

  54. Foldi M, Farkas N, Kiss S, Zadori N, Vancsa S, Szako L et al (2020) Obesity is a risk factor for developing critical condition in COVID-19 patients: a systematic review and meta-analysis. Obes Rev 21(10):e13095

    PubMed  PubMed Central  Google Scholar 

  55. Kass DA, Duggal P, Cingolani O (2020) Obesity could shift severe COVID-19 disease to younger ages. Lancet 395(10236):1544–1545

    CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

We would like to thank the laboratory staff, the University of Brasilia, primary physicians, and other health professionals who referred patients for CPET assessment.

Funding

This study was funded in part by Brazilian public research grants and scholarships from Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq [National Council of Scientific and Technological Development]) (author H),Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES [Coordination for the Advancement of Higher Education Personnel]) (authors B and E) and Fundação de Apoio à Pesquisa do Distrito Federal (FAPDF [Federal District Research Support Foundation] (author H). There were also fundings from the Special Research Fund (BOF) from Hasselt University, Belgium (Number: BOF23DOCBL10 and BOF23KV10).

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Authors and Affiliations

  1. Health Sciences and Technologies Graduate Program, University of Brasilia (UnB), Brasilia, DF, Brazil

    Luciana Bartolomei Orru D’Ávila, Mauricio Milani, Alexandra Correa Gervazoni Balbuena de Lima, Juliana Goulart Prata Oliveira Milani, Graziella França Bernardelli Cipriano, Vinicius Zacarias Maldaner da Silva & Gerson Cipriano Jr

  2. Heart Centre Hasselt, Jessa Hospital, Hasselt, Belgium

    Mauricio Milani

  3. University of São Paulo | USP Heart Institute São Paulo (InCor), São Paulo, SP, Brazil

    David C. S. Le Bihan

  4. Rehabilitation Sciences Program, University of Brasilia (UnB), Brasilia, DF, Brazil

    Mauricio Milani & Graziella França Bernardelli Cipriano

  5. REVAL/BIOMED, Hasselt University, Hasselt, Belgium

    Juliana Goulart Prata Oliveira Milani

  6. Medcor, CLSW 105 Bloco A salas 37 a 39 Sudoeste, Brasilia, DF, CEP: 70670431, Brazil

    Luciana Bartolomei Orru D’Ávila

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  1. Luciana Bartolomei Orru D’Ávila
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Contributions

LBOD (A): conception and design, acquisition of data, analysis and interpretation of the results, drafted the article; MM (B): conception and design, interpretation of data, analysis and interpretation of the results revised it critically, supervision; DLB (C): conception and design, acquisition of data, analysis and interpretation of the results, revised it critically; ACGBL(D): conception and design, revised it critically; JGPOM(E): conception and design, revised it critically;GFBC (F): conception and design, revised it critically; VZMS(G): conception and design, interpretation of data, analysis and interpretation of the results revised it critically; GCJ(H): conception and design, analysis and interpretation of data, revised it critically, supervision. All authors gave final approval of the version to be published and agreed to be responsible for all aspects of the research.

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Correspondence to Luciana Bartolomei Orru D’Ávila.

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This study received approval from the Human Research Ethics Committee (certificate number: 56994822.5.0000.809) (Supplementary File S1).

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D’Ávila, L.B.O., Milani, M., Le Bihan, D.C.S. et al. Longitudinal strain and myocardial work in symptomatic patients having recovered from COVID-19 and possible associations with the severity of the disease. Int J Cardiovasc Imaging 40, 745–756 (2024). https://doi.org/10.1007/s10554-023-03042-2

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