Impaired Right Ventricular Longitudinal Strain Without Pulmonary Hypertension in Patients Who Have Recovered From COVID-19
2021; Lippincott Williams & Wilkins; Volume: 14; Issue: 4 Linguagem: Inglês
10.1161/circimaging.120.012166
ISSN1942-0080
AutoresVincenzo Nuzzi, Matteo Castrichini, Valentino Collini, Erik Roman‐Pognuz, Stefano Di Bella, Roberto Luzzati, Giorgio Berlot, Marco Confalonieri, Marco Merlo, Davide Stolfo, Gianfranco Sinagra,
Tópico(s)Cardiac Imaging and Diagnostics
ResumoHomeCirculation: Cardiovascular ImagingVol. 14, No. 4Impaired Right Ventricular Longitudinal Strain Without Pulmonary Hypertension in Patients Who Have Recovered From COVID-19 Free AccessLetterPDF/EPUBAboutView PDFView EPUBSections ToolsAdd to favoritesDownload citationsTrack citationsPermissions ShareShare onFacebookTwitterLinked InMendeleyReddit Jump toFree AccessLetterPDF/EPUBImpaired Right Ventricular Longitudinal Strain Without Pulmonary Hypertension in Patients Who Have Recovered From COVID-19 Vincenzo Nuzzi, Matteo Castrichini, Valentino Collini, Erik Roman-Pognuz, Stefano Di Bella, Roberto Luzzati, Giorgio Berlot, Marco Confalonieri, Marco Merlo, Davide Stolfo and Gianfranco Sinagra Vincenzo NuzziVincenzo Nuzzi https://orcid.org/0000-0002-9643-2697 Department of Cardiology (V.N., M. Castrichini, V.C., M.M., D.S., G.S.), Azienda Sanitaria Universitaria Integrata Giuliano Isontina, University of Trieste, Italy. , Matteo CastrichiniMatteo Castrichini https://orcid.org/0000-0002-2405-3364 Department of Cardiology (V.N., M. Castrichini, V.C., M.M., D.S., G.S.), Azienda Sanitaria Universitaria Integrata Giuliano Isontina, University of Trieste, Italy. , Valentino ColliniValentino Collini Department of Cardiology (V.N., M. Castrichini, V.C., M.M., D.S., G.S.), Azienda Sanitaria Universitaria Integrata Giuliano Isontina, University of Trieste, Italy. , Erik Roman-PognuzErik Roman-Pognuz https://orcid.org/0000-0002-0859-3424 Department of Anesthesia and Intensive Care Medicine (E.R.-P., G.B.), Azienda Sanitaria Universitaria Integrata Giuliano Isontina, University of Trieste, Italy. , Stefano Di BellaStefano Di Bella https://orcid.org/0000-0001-6121-7009 Infectious Diseases Department (S.D.B., R.L.), Azienda Sanitaria Universitaria Integrata Giuliano Isontina, University of Trieste, Italy. , Roberto LuzzatiRoberto Luzzati https://orcid.org/0000-0001-5546-0715 Infectious Diseases Department (S.D.B., R.L.), Azienda Sanitaria Universitaria Integrata Giuliano Isontina, University of Trieste, Italy. , Giorgio BerlotGiorgio Berlot Department of Anesthesia and Intensive Care Medicine (E.R.-P., G.B.), Azienda Sanitaria Universitaria Integrata Giuliano Isontina, University of Trieste, Italy. , Marco ConfalonieriMarco Confalonieri Pneumology Department (M. Confalonieri), Azienda Sanitaria Universitaria Integrata Giuliano Isontina, University of Trieste, Italy. , Marco MerloMarco Merlo Department of Cardiology (V.N., M. Castrichini, V.C., M.M., D.S., G.S.), Azienda Sanitaria Universitaria Integrata Giuliano Isontina, University of Trieste, Italy. , Davide StolfoDavide Stolfo Davide Stolfo, MD, Division of Cardiology, Cardiovascular Department, Azienda Sanitaria Universitaria Integrata Giuliana Isontina, Via Valdoni 7, 34149 Trieste, Italy. Email E-mail Address: [email protected] https://orcid.org/0000-0002-4538-6811 Department of Cardiology (V.N., M. Castrichini, V.C., M.M., D.S., G.S.), Azienda Sanitaria Universitaria Integrata Giuliano Isontina, University of Trieste, Italy. and Gianfranco SinagraGianfranco Sinagra Department of Cardiology (V.N., M. Castrichini, V.C., M.M., D.S., G.S.), Azienda Sanitaria Universitaria Integrata Giuliano Isontina, University of Trieste, Italy. Originally published8 Apr 2021https://doi.org/10.1161/CIRCIMAGING.120.012166Circulation: Cardiovascular Imaging. 2021;14:e012166Other version(s) of this articleYou are viewing the most recent version of this article. Previous versions: April 8, 2021: Ahead of Print Right ventricular (RV) dysfunction (RVD) is associated with worse outcome in coronavirus disease 2019 (COVID-19).1 Pulmonary hypertension (PH) is a cause of RVD in COVID-19 respiratory failure and is associated with negative prognosis.2 Major pulmonary embolism, alveolar and endothelial injury, and thrombotic microangiopathy are potential triggers for new-onset PH in the acute phase.3Persistent RV involvement has been reported in patients recovered from COVID-19.4 However, the association between persistent RV impairment and new-onset PH remains unexplored. We evaluated the prevalence of PH and RVD in patients recovered from COVID-19.The data that support the findings of this study are available from the corresponding author upon reasonable request. All the patients with severe COVID-19 (ie, arterial oxygen saturation, <90%) without preexisting cardiovascular or lung disease discharged from our hospital between February and September 2020 were offered the opportunity to perform an echocardiography, including speckle-tracking imaging (admission-to-echo time, 74 [51–98] days).COVID-19 infection diagnosis was made by polymerase chain reaction of nasopharyngeal swabs. A healthy age-, sex-, and hypertension-matched cohort was used as comparison.Echocardiograms were analyzed according to current recommendations4 using the TomTec 2D Cardiac Performance Analysis software. RVD was defined by RV fractional area shortening 35 mm Hg, and impaired RV longitudinal free-wall strain (RVLS) by values >−20% (less negative).5 Patients with poor acoustic windows or inadequate tricuspid regurgitation for pulmonary artery systolic pressure estimation were excluded.Data are reported as mean±SD, median and interquartile range, or number and percentages. Comparison was performed by ANOVA and χ2 test. The study complied with the Declaration of Helsinki and was approved by the institutional ethics board. Patients provided informed consent.Among the 136 COVID-19 patients without cardiovascular and lung disease, 20 died, 21 declined participation to the study, 19 had poor acoustic windows or inadequate tricuspid, while 23 were not available for follow-up. Fifty-three patients were included (61±12 years; 64% men; 38% required invasive ventilation; median in-hospital stay, 19 [10–28] days; Table).Table. Overall Characteristics of the Study PopulationCOVID recovered (n=53)Control (n=37)P valueAge, y61 (12)58 (12)0.255Male sex, n (%)34 (64)26 (70)0.545Atrial fibrillation, n (%)3 (6)3 (8)0.479Diabetes type 2, n (%)12 (23)5 (14)0.209Smoker (active or former), n (%)8 (15)8 (22)0.425Hypertension, n (%)22 (42)18 (49)0.502Troponin, ng/mL*11 (11)……CRP, mg/L49 (14–108)……d-dimer, mg/L FEU0.61 (0.46–1.04)……Invasive mechanical ventilation, n (%)†20 (38)……Invasive mechanical ventilation duration, d12 (7–18)……Noninvasive mechanical ventilation, n (%)†27 (51)……Follow-up dataFollow-up time, d74 (51–98)……Systolic blood pressure, mm Hg136 (16)126 (14)0.005Heart rate, bpm72 (10)69 (15)0.289Oxygen saturation (room air), %98 (1)……β-Blocker, n (%)12 (23)17 (46)0.020ACE inhibitor/ARB, n (%)17 (32)9 (24)0.392Mineralocorticoid antagonist, n (%)1 (2)0 (0)0.589Diuretics, n (%)4 (8)0 (0)0.115LVEDV, mL88 (28)92 (23)0.573LVEF, %63 (6)63 (7)0.878Diastolic dysfunction grade 148 (91)30 (81)0.105E/E′9 (4)9 (2)0.408LAESV, mL53 (28)74 (24)0.003RAESA, cm215 (4)18 (4)0.002RVEDA, cm218 (4)17 (3)0.112RV-FAC, %44 (5)46 (6)0.124RV dysfunction, n (%)0 (0)0 (0)…TAPSE, mm22 (4)25 (4)0.056RV S′, cm/s12 (2)13 (2)0.572RV longitudinal strain−19.7 (−3.6)−22.1 (−1.5) 35 mm Hg), n (%)0 (0)0 (0)…ACE indicates angiotensin-converting enzyme; ARB, angiotensin receptor blocker; COVID, coronavirus disease; CRP, C-reactive protein; FEU, fibrinogen equivalence unit; LAESV left atrial end-systolic volume; LVEDV, left ventricular end-diastolic volume; LVEF, left ventricular ejection fraction; PASP pulmonary artery systolic pressure; RAESA, right atrial end-systolic area; RV right ventricle; RV-FAC right ventricular fractional area shortening; RVEDA right ventricular end-diastolic area; and TAPSE tricuspid anulus peak systolic excursion.* Fourteen of 53 patients had a troponin assessment available. Among these, 3 patients had abnormal troponin value (2 of 3 had reduced RV strain) and 9 had normal troponin value (2 of 9 had reduced RV strain).† Five patients received both noninvasive mechanical ventilation and invasive mechanical ventilation.No patients had left ventricular dysfunction, significant valvulopathies, diastolic dysfunction grade >1, PH (pulmonary artery systolic pressure, 27±6 mm Hg), or RVD (RV fractional area shortening, 44±5%). However, impaired RVLS was found in 42% of cases. RVLS was similar between mechanically ventilated and nonmechanically ventilated patients (−19.7±−3.9% versus −19.6±−2.1%; P=0.942). No patients reported heart failure symptoms at follow-up.Control subjects (n=37) showed normal RVLS. In COVID-recovered patients, RVLS was lower (P 50% of COVID-19 recovered patients. In these patients, functional RV parameters were concomitantly impaired.5Some limitation should be acknowledged. The population size and retrospective nature of the study limit the strength of our observations. Biomarkers were available only in a minority of the cohort. Moreover, most of patients did not have previous echocardiographic evaluations; therefore, the assessment of RVLS trends was not feasible.Although recent symptomatic COVID-19 infection was not associated with PH or RV dysfunction by conventional echo parameters, subclinical RV dysfunction by RVLS was noted in 42% of recovered COVID-19 patients. Long-term follow-up is required to define the evolution of these abnormalities, and larger series are warranted to validate our findings.AcknowledgmentsWe thank the Cassa di Risparmio di Trieste Foundation for the continuous support in research.Sources of FundingNone.Disclosures None.Footnotes*V. Nuzzi and M. Castrichini contributed equally.Davide Stolfo, MD, Division of Cardiology, Cardiovascular Department, Azienda Sanitaria Universitaria Integrata Giuliana Isontina, Via Valdoni 7, 34149 Trieste, Italy. Email davide.stolfo@gmail.comReferences1. Li Y, Li H, Zhu S, Xie Y, Wang B, He L, Zhang D, Zhang Y, Yuan H, Wu Cet al. Prognostic value of right ventricular longitudinal strain in patients with COVID-19.JACC Cardiovasc Imaging. 2020; 13:2287–2299. doi: 10.1016/j.jcmg.2020.04.014CrossrefMedlineGoogle Scholar2. Pagnesi M, Baldetti L, Beneduce A, Calvo F, Gramegna M, Pazzanese V, Ingallina G, Napolano A, Finazzi R, Ruggeri A, et al. Pulmonary hypertension and right ventricular involvement in hospitalised patients with COVID-19.Heart. 2020; 106:1324–1331. doi: 10.1136/heartjnl-2020-317355CrossrefMedlineGoogle Scholar3. Pellikka PA, Naqvi TZ. The right ventricle: a target in COVID-19 cardiac insult.J Am Coll Cardiol. 2020; 76:1978–1981. doi: 10.1016/j.jacc.2020.09.529CrossrefMedlineGoogle Scholar4. Huang L, Zhao P, Tang D, Zhu T, Han R, Zhan C, Liu W, Zeng H, Tao Q, Xia Let al. Cardiac involvement in patients recovered from COVID-2019 identified using magnetic resonance imaging.JACC Cardiovasc Imaging. 2020; 13:2330–2339. doi: 10.1016/j.jcmg.2020.05.004CrossrefMedlineGoogle Scholar5. Lang RM, Badano LP, Mor-Avi V, Afilalo J, Armstrong A, Ernande L, Flachskampf FA, Foster E, Goldstein SA, Kuznetsova T, et al. 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. 2015; 16:233–270. doi: 10.1093/ehjci/jev014CrossrefMedlineGoogle Scholar Previous Back to top Next FiguresReferencesRelatedDetailsCited By Luchian M, Higny J, Benoit M, Robaye B, Berners Y, Henry J, Colle B, Xhaët O, Blommaert D, Droogmans S, Motoc A, Cosyns B, Gabriel L, Guedes A and Demeure F (2023) Unmasking Pandemic Echoes: An In-Depth Review of Long COVID's Unabated Cardiovascular Consequences beyond 2020, Diagnostics, 10.3390/diagnostics13213368, 13:21, (3368) Zhang Z, Wang D, Zuo W, Wang X, Yang F, Luo H, Xiao Z, Liu Q and Xiao Y (2023) COVID-19 vaccination for children with pulmonary hypertension: efficacy, safety and reasons for opting against vaccination, Frontiers in Pediatrics, 10.3389/fped.2023.1259753, 11 Stefani L, Brown P, Gerges M, Emerson P, Ferkh A, Kairaitis K, Gilroy N, Altman M and Thomas L (2023) Echocardiographic Assessment in Patients Recovered from Acute COVID-19 Illness, Journal of Cardiovascular Development and Disease, 10.3390/jcdd10080349, 10:8, (349) Parhizgar P, Yazdankhah N, Rzepka A, Chung K, Ali I, Lai Fat Fur R, Russell V and Cheung A (2023) Beyond Acute COVID-19: A Review of Long-term Cardiovascular Outcomes, Canadian Journal of Cardiology, 10.1016/j.cjca.2023.01.031, 39:6, (726-740), Online publication date: 1-Jun-2023. Barros L, Castillo J and Lacerda H (2023) Abnormal right ventricular echocardiographic findings in recovered patients associated with severe acute respiratory syndrome in COVID‐19, Echocardiography, 10.1111/echo.15538, 40:3, (227-234), Online publication date: 1-Mar-2023. Jordan-Rios A, Nuzzi V, Bromage D, McDonagh T, Sinagra G and Cannata A (2023) Reshaping care in the aftermath of the pandemic. Implications for cardiology health systems, European Journal of Internal Medicine, 10.1016/j.ejim.2022.11.029, 109, (4-11), Online publication date: 1-Mar-2023. Lorente-Ros M, Das S, Elias J, Frishman W and Aronow W (2023) Cardiovascular Manifestations of the Long COVID Syndrome, Cardiology in Review, 10.1097/CRD.0000000000000552, Publish Ahead of Print Murata N, Yamada A, Fujito H, Hashimoto N, Nagao T, Tanaka Y, Fukumoto K, Arai R, Wakamatsu Y, Ebuchi Y, Monden M, Kojima K, Hayashi K, Gon Y and Okumura Y (2022) Cardiovascular manifestations identified by multi-modality imaging in patients with long COVID, Frontiers in Cardiovascular Medicine, 10.3389/fcvm.2022.968584, 9 Kaziród-Wolski K, Zając P, Zabojszcz M, Kołodziej A, Sielski J and Siudak Z (2022) The Effect of COVID-19 on the Perioperative Course of Acute Coronary Syndrome in Poland: The Estimation of Perioperative Prognosis and Neural Network Analysis in 243,515 Cases from 2020 to 2021, Journal of Clinical Medicine, 10.3390/jcm11185394, 11:18, (5394) Carubbi F, Alunno A, Carducci A, Grassi D and Ferri C (2022) Electrocardiographic Abnormalities in Hospitalized Patients with COVID-19 and the Associations with Clinical Outcome, Journal of Clinical Medicine, 10.3390/jcm11175248, 11:17, (5248) Nuzzi V, Del Mestre E, Degrassi A, Bromage D, Manca P, Piper S, Artico J, Gentile P, Scott P, Chiatto M, Merlo M, Pareek N, Giacca M, Sinagra G, McDonagh T and Cannata A (2022) Cardiovascular Damage in COVID-19: What We Know Two Years Later, Current Cardiology Reports, 10.1007/s11886-022-01730-4, 24:9, (1085-1091), Online publication date: 1-Sep-2022. Manca P, Nuzzi V, Cannatà A, Castrichini M, Bromage D, De Luca A, Stolfo D, Schulz U, Merlo M and Sinagra G (2022) The right ventricular involvement in dilated cardiomyopathy: prevalence and prognostic implications of the often-neglected child, Heart Failure Reviews, 10.1007/s10741-022-10229-7, 27:5, (1795-1805), Online publication date: 1-Sep-2022. Son K, Kim W, Kwak J, Choi C, Lee S, Ko U, Kim H, Lee H, Chung E, Kim J, Jang W, Jung J, Kim J, Yoon Y, Song S, Sung M, Jang M, Kim Y, Jeong I, Kim D, Kim T, Kim S, Kim S, Hong J and An H (2022) Hyperglycemia and Hypoglycemia Are Associated with In-Hospital Mortality among Patients with Coronavirus Disease 2019 Supported with Extracorporeal Membrane Oxygenation, Journal of Clinical Medicine, 10.3390/jcm11175106, 11:17, (5106) Singh J, Bhagaloo L, Sy E, Lavoie A, Dehghani P, Bardutz H, Mang C, Buttigieg J and Neary J (2022) Cardiac impairments in postacute COVID ‐19 with sustained symptoms: A review of the literature and proof of concept , Physiological Reports, 10.14814/phy2.15430, 10:16, Online publication date: 1-Aug-2022. Tobler D, Pruzansky A, Naderi S, Ambrosy A and Slade J (2022) Long-Term Cardiovascular Effects of COVID-19: Emerging Data Relevant to the Cardiovascular Clinician, Current Atherosclerosis Reports, 10.1007/s11883-022-01032-8, 24:7, (563-570), Online publication date: 1-Jul-2022. Rind I, Cannata A, McDonaugh B, Cassimon B, Bannister C, Scott P, Piper S, Bromage D and McDonagh T (2022) Patients hospitalised with heart failure across different waves of the COVID-19 pandemic show consistent clinical characteristics and outcomes, International Journal of Cardiology, 10.1016/j.ijcard.2021.12.042, 350, (125-129), Online publication date: 1-Mar-2022. Polito M, Silverio A, Bellino M, Iuliano G, Di Maio M, Alfano C, Iannece P, Esposito N and Galasso G (2021) Cardiovascular Involvement in COVID-19: What Sequelae Should We Expect?, Cardiology and Therapy, 10.1007/s40119-021-00232-8, 10:2, (377-396), Online publication date: 1-Dec-2021. Shimoni O, Korenfeld R, Goland S, Meledin V, Haberman D, George J and Shimoni S (2021) Subclinical Myocardial Dysfunction in Patients Recovered from COVID-19 Disease: Correlation with Exercise Capacity, Biology, 10.3390/biology10111201, 10:11, (1201) Nuzzi V, Merlo M, Specchia C, Lombardi C, Carubelli V, Iorio A, Inciardi R, Bellasi A, Canale C, Camporotondo R, Catagnano F, Dalla Vecchia L, Giovinazzo S, Maccagni G, Mapelli M, Margonato D, Monzo L, Oriecuia C, Peveri G, Pozzi A, Provenzale G, Sarullo F, Tomasoni D, Ameri P, Gnecchi M, Leonardi S, Agostoni P, Carugo S, Danzi G, Guazzi M, La Rovere M, Mortara A, Piepoli M, Porto I, Volterrani M, Senni M, Metra M and Sinagra G (2021) The prognostic value of serial troponin measurements in patients admitted for COVID‐19, ESC Heart Failure, 10.1002/ehf2.13462, 8:5, (3504-3511), Online publication date: 1-Oct-2021. Maestre-Muñiz M, Arias Á, Mata-Vázquez E, Martín-Toledano M, López-Larramona G, Ruiz-Chicote A, Nieto-Sandoval B and Lucendo A (2021) Long-Term Outcomes of Patients with Coronavirus Disease 2019 at One Year after Hospital Discharge, Journal of Clinical Medicine, 10.3390/jcm10132945, 10:13, (2945) April 2021Vol 14, Issue 4 Advertisement Article Information Metrics © 2021 American Heart Association, Inc.https://doi.org/10.1161/CIRCIMAGING.120.012166PMID: 33827250 Originally publishedApril 8, 2021 KeywordsCOVID-19echocardiographyhypertension, pulmonaryprognosisventricular function, rightPDF download Advertisement Subjects Contractile Function Echocardiography Imaging Ultrasound
Referência(s)