key: cord-0733334-yulwjgow
authors: Ramadan, Mohammad Said; Bertolino, Lorenzo; Zampino, Rosa; Durante-Mangoni, Emanuele
title: Cardiac sequelae after COVID-19 recovery: a systematic review
date: 2021-06-23
journal: Clin Microbiol Infect
DOI: 10.1016/j.cmi.2021.06.015
sha: cf274d51603fc678b56be3722049931a5edc807e
doc_id: 733334
cord_uid: yulwjgow

BACKGROUND: Coronavirus disease 2019 (COVID-19) has been implicated in a wide spectrum of cardiac manifestations following the acute phase of the disease. OBJECTIVES: To assess the range of cardiac sequelae after COVID-19 recovery. DATA SOURCES: PubMed, Embase, Scopus (inception through 17 February 2021), and Google scholar (2019 through 17 February 2021). STUDY ELIGIBILITY CRITERIA: Prospective and retrospective studies, case reports and case series. PARTICIPANTS: Adult patients assessed for cardiac manifestations after COVID-19 recovery. EXPOSURE: Severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) infection diagnosed by polymerase chain reaction (PCR). METHODS: Systematic review. RESULTS: Thirty-five studies (fifteen prospective cohort, seven case reports, five cross-sectional, four case series, three retrospective cohort and one ambidirectional cohort) evaluating cardiac sequelae in 52609 patients were included. Twenty-nine studies utilized objective cardiac assessments, mostly cardiac magnetic resonance imaging (CMR) in sixteen studies, echocardiography in fifteen, electrocardiography (ECG) in sixteen and cardiac biomarkers in eighteen. Most studies had a fair risk of bias. The median time from diagnosis/recovery to cardiac assessment was 48 days (1-180). Common short-term cardiac abnormalities (<3 months) included increased T1 (proportion: 30%), T2 (16%), pericardial effusion (15%) and late gadolinium enhancement (LGE, 11%) on CMR, with symptoms such as chest pain (25%) and dyspnea (36%). In the medium term (3-6 months), common changes included reduced left ventricular global longitudinal strain (30%) and LGE (10%) on CMR, diastolic dysfunction (40%) on echocardiography and elevated NT-proBNP (18%). In addition, COVID-19 survivors had higher risk (RR = 3; 95% CI: 2.7-3.2) of developing heart failure, arrythmias and myocardial infarction. CONCLUSIONS: COVID-19 appears to be associated with persistent/de novo cardiac injury after recovery, particularly subclinical myocardial injury in the earlier phase and diastolic dysfunction later. Larger well-designed and controlled studies with baseline assessments are needed to better measure the extent of cardiac injury and its clinical impact.

Introduction process, including the initial search for the identification of references, the selection of 117 potentially relevant titles for review of abstracts and, among them, of those chosen for review 118 of the full-length report, according to prespecified inclusion and exclusion criteria (Table 1) . 119

Conflicts in data abstraction were resolved by consensus. The screening and selection process 120 are presented in Figure 1 . 121

The Newcastle-Ottawa Scale (NOS) was used to assess the quality of cohort 123 nonrandomized studies (Supplementary Table S3 ). This scale is an ongoing collaboration 124 between the Universities of Newcastle, Australia and Ottawa, Canada. The tool assesses risk of 125 bias in selection of participants, comparability of study groups and ascertainment of either 126 exposure or outcome of interest in case-control or cohort studies respectively. Alternatively, we 127 used the Joanna Briggs Institute (JBI) critical appraisal checklist to assess the quality of cross-128 sectional studies (Supplementary Table S4 Outcomes of interest included both subjective or reported cardiac symptoms and 135 objectively measured outcomes. Data for cardiac sequelae were counted by patient. Where data 136 were reported for multiple time points, we presented the whole dataset according to the time 137 of assessment. Extracted outcomes included only those reported during the post-recovery 138 period. For that purpose, we assessed the lower limit of the reported time range between 139 COVID-19 and cardiac assessment. The lower limit needed to be equal to or greater than our 140 pre-specified time to assessment criteria. Where outcomes were reported earlier than our 141 inclusion criteria with no possibility of retrieving the relevant outcomes, the article was 142 excluded. 143

Similar outcomes from original studies were summarized in a proportion (observed 144 cases/number of tested participants), median (in percentage), and range of reported findings (in 145 percentage), excluding results from case reports. We present also outcomes stratified by COVID-146 19 severity, and short (<3 months) or medium-term (≥3 months) cardiac sequelae in percent 147

proportions. COVID-19 severity was determined, if not explicitly stated in the study, using the 148 WHO scale for COVID-19 severity (15). All statistical analyses were done on SPSS V.26 (IBM) or 149

Microsoft Excel. Owing to the differences in design of the studies, we were not able to perform 150 a meta-analysis. 151

The database search identified 2867 records after removing duplicates. Through 154 screening of titles and abstracts, we excluded 2670 records, leaving 197 to be assessed as full 155 text. Of these, we finally included in this review 35 studies (5, 8, 11, 12, , of which 3 were 156 pre-prints (5, 23, 50), three were presented as research letters (21, 43, 51) and three were 157 presented as research communications (22, 31, 44) . The reasons for excluding 162 articles are 158 listed in the PRISMA flow chart (see Figure 1 ) (52). 159

Of the 35 studies included in this review, 15 were prospective cohort (8, 12, 22, 29-31, 160 34, 35, 40-42, 44, 45, 47, 50) , 7 were case reports (21, 25, 28, 36, 37, 39, 48) , 5 had a cross-161 sectional design (5, 20, 24, 26, 38) , 4 were case series (23, 32, 43, 46) , 3 were retrospective 162 cohort (11, 27, 49) , and 1 was ambidirectional cohort study (33) . 163

The main characteristics of all included studies are listed in Supplementary Table S7 . 165

The number of included patients totaled 52609 with a median age of 53 years (range: 167 19-74 years) and one study not specifying the age, but inferred adults since they are collegiate 168 athletes (23). No study included children. 169 22 articles (63%) included patients previously hospitalized for COVID-19 (N=51117, 170 97.2%) (11, 21, 24, 25, 31-46, 48, 49) , 8 studies a mixed population of discharged patients and 171 outpatients (N= 1330, 2.5%) (5, 8, 12, 22, 26, 29, 47, 50) among which one included healthcare 172 workers (5), 5 included only outpatients (N=122; 0.3%) (20, 23, 27, 28, 30) , among which 4 173 included solely athletes (20, 23, 27, 30) . 174 COVID-19 severity was not clearly demarcated in 14/35 studies (N=51100 participants) 175 (5, 8, 12, 25, 29, 33, 38, 42-46, 48, 49) . Using the WHO scale for COVID-19 severity (15), we 176 divided the latter population into severity categories and then combined them with other 177 studies with pre-specified groups. Studies included participants with a majority of 178 asymptomatic-mild (13/35 studies; N=1359 participants) (5, 12, 20-24, 26-30, 50) , moderate-179 critical (21/35 studies; N=51234 participants) (8, 11, 25, (31) (32) (33) (34) (35) (36) (37) (38) (39) (40) (41) (42) (43) (44) (45) (47) (48) (49) For cardiac sequelae assessment, utilized methods included CMR (n=16 studies, 45.7%) 184 (5, 11, 12, 20, 23, 25, 27-30, 34, 35, 37, 39, 40, 46) , echocardiography (n=14, 40%) (20-23, 25, 28, 185 30, 32, 36, 38, 44, 45, 47, 48) , electrocardiography (ECG) (n=16, 45.3%) (5, 20-23, 25, 27, 28, 30, 186 32, 34, 36-39, 48) , troponin (n=17, 48.5%) (5, 11, 20, 23, 27-30, 32, 34-37, 39, 44-46) , 187 questionnaire (n=9, 25.7%) (8, 12, 24, 26, 32, 33, (41) (42) (43) , 25.7%) (5, 11, 28, 29, 188 32, 34, 39, 45, 47) in studies with discharged patients (11, 21, 24, 25, 31-46, 48, 49) , 66.5 days (range: 28-103) in 193 those with mixed discharged patients and outpatients (5, 8, 12, 22, 26, 29, 47, 50), and 28 days 194 (range: 23-104) in those with outpatients (20, 23, 27, 30) . In one study, the reported range was 195 11-53 days, but this was kept in the analysis since individual data for those assessed ≥14 days 196 were available (30). Another study included only the time since admission (74-88 days), and was 197 also included because the maximum hospitalization time was 17 days (31). 198

Outcomes 199

The main outcomes of all included studies are presented in Table 2 . In 12 studies with CMR (excluding 4 case reports) (5, 11, 12, 20, 23, 27, 29, 30, 34, 35, 202 40, 46) , median time to assessment was 63 days (range: 14-124 days) and participants totaled 203 1018 (785 patients; 233 controls). Reported outcomes included increased T1 intensity ( In 9 studies utilizing echocardiography for cardiac assessment (excluding 5 case reports) 219 (20, 22, 23, 30, 32, 38, 44, 45, 47) and a median time to assessment of 44 days (23-124 days) did not report any abnormality on 238 ECG (27, 30, 32, 34) . 239

In 13 studies (excluding 4 case reports) which included troponin level assessment (5, 11, 241 20, 23, 27, 29, 30, 32, 34, 35, 44-46) , median time to assessment was 48 days (14-124 days) and 242 participants totaled 968 (766 patients; 202 controls). Elevated levels were observed in 27/766 243 patients, with a median of 0% and range 0-20%. In contrast, 8 studies with 444/968 participants 244 J o u r n a l P r e -p r o o f (45.9%) and a median time to assessment of 44.5 days (14-124 days) reported no increased 245 troponin levels (11, 23, 27, 30, 32, 34, 35, 44) . 246

In 7 studies (excluding 2 case reports) which included NT-pro-BNP level assessment (5, 247 11, 29, 32, 34, 45, 47) , median time to assessment was 71 days (14-124 days) and participants 248 totaled 723 (571 patients; 152 controls). Increased NT-pro-BNP levels were reported in 57/571, 249 with a median of 0% and range 0-23%. Four studies with 351/723 participants (48.5%) and a 250 median time to assessment of 64 days (range: 14-124 days) did not report NT-pro-BNP level 251 increase (11, 29, 32, 34) . 252

In studies which reported coronary angiogram (n=4) (21, 28, 36, 39), of which 3 were 254 case reports (28, 36, 39) and 1 a case series (21) Cardiac Symptoms 262 20 studies (excluding 2 case reports) reported cardiac symptoms (5, 8, 11, 12, 20, 24, 26, 263 29, 31-33, 35, 38, 41-43, 45-47, 50) The issue of cardiac sequelae of COVID-19 remains a highly clinically relevant topic, 287 which prompted us to perform a systematic review of cardiac manifestations in adults after 288 COVID-19 recovery. Cardiac abnormalities were common and were detected more frequently 289 when higher accuracy diagnostic tests were employed. Indeed, cardiac abnormalities were 290 observed in decreasing rates on CMR, echocardiography, ECG, biomarkers' assessment. This was 291 in contrast to a very high rate of reported symptoms of cardiac disease, mostly chest pain and 292

Included studies were observational in nature, and most had a fair risk of bias, the latter 294 being primarily due to absence of a comparison group in cohort studies (8, 12, 22, 27, 30, 31, 33, 295 41, 44, 45, 47, 50) . The studies included a variety of patients with diverse baseline health 296 profiles, demographic characteristics, and COVID-19 severity. One study (49), included most 297 participants (89.9%); however, as the sole study reporting on MACE, it is unlikely to alter the 298 pooled results of other studies. The studies had a range of utilized methods, with most using 299 CMR, echocardiography, ECG and biomarkers' measurement. However, most positive findings 300 came from CMR, which has higher sensitivity for detecting myocardial damage (53) and in line 301 with studies using these methods concomitantly to detect cardiac pathology (20, 29, 34) . 302

Included studies demonstrate increased risk of clinical and subclinical cardiac sequelae 303 in COVID-19 recovered patients. Clinically, these patients seemed to be at a greater risk than 304 controls who never had COVID-19 for a range of cardiac diseases, including heart failure, 305 myocardial infarction, myocarditis, pericarditis, and arrythmia. This was evident in a high quality 306 study with matched control groups assessing a large UK cohort of COVID-19 patients at 140 days 307 after hospital discharge, where the authors found three times higher risk of developing heart 308 J o u r n a l P r e -p r o o f failure, myocardial infarction, stroke, and arrhythmia in the COVID-19 cohort, as compared to 309 matched controls with similar baseline characteristics (49). On the other hand, evidence for 310 clinical myocarditis and pericarditis was more variable across studies, and many did not report 311 them as explicit diagnoses despite findings suggesting myocardial involvement on imaging (11, 312 20, 29) . Alarmingly, myocarditis was reported in groups with asymptomatic/mild 313 12, 30) , and in healthy populations such as athletes (30), but without evidence of a greater 314 arrythmia risk. Increased risk for cardiac injury was also observed in other respiratory viral 315 illnesses (54), such as with severe acute respiratory syndrome coronavirus (SARS-CoV), whose 316 genomic sequence is 79.6% homologous to SARS-CoV-2 (4). Both SARS-CoV and SARS-CoV-2 317 attach to the angiotensin-converting enzyme 2 (ACE2) receptor, found on the surface of host 318 cells, and highly expressed in the heart, kidneys, lungs and blood vessels. This could explain 319 direct damage though cell invasion, translating into increased inflammation and coagulation (4), 320 which could provide a pathophysiological basis for cardiac injury due to both viruses. 321

Short term cardiac sequelae after COVID-19 (<3 months after diagnosis/discharge) 322 clustered in increased CMR test parameters (T1, T2, peri/myocardial enhancement), ECG 323 abnormalities (T wave abnormalities and ST segment changes), and persistent symptoms (chest 324 pain and dyspnea) (Figure 2 ). These short-term findings could point towards an active 325 inflammatory process of the myocardium (evidenced by an increase in both T1 and T2) (20, 29, 326 55, 56) . The latter observation is further strengthened by EMB, done in the short-term post 327 recovery period, showing active inflammatory infiltrate (28, 29). Medium-term cardiac sequelae 328 (3-6 months after COVID-19 recovery), on the other hand, mostly included reduced GLS and 329 elevated ECV on CMR, diastolic dysfunction and pulmonary hypertension on echocardiography, 330 and elevated NT-proBNP (Figure 2 ). In one study with two-point follow-ups, chest pain, diastolic 331 dysfunction and pulmonary hypertension observed at day 60 persisted at day 100 (47), while in another study, chest pain (3%) and palpitations (2.3%) reported in the first week subsided on 333 the third week of follow-up (0%) (41). These findings could indicate later development of 334 myocardial scarring and fibrosis, subclinical LV and RV dysfunction, and non-ischemic 335 cardiomyopathy (20, 29, 34, 55, 56) . Diastolic dysfunction and pulmonary hypertension could 336 result from direct viral injury and/or indirectly from chronic pulmonary disease and ongoing 337 inflammation caused by COVID-19, increasing the long-term risk of developing sub/clinical heart 338 failure with preserved ejection fraction (57). Moreover and outside of COVID-19, ongoing 339 myocardial inflammation associates with more severe complications such as heart failure (58), 340 and LGE may be associated with life-threatening arrythmias and sudden cardiac death (59). 341

However, properly determining the clinical significance of CMR findings and their evolution with 342 time requires follow-up over multiple time points, which was not evident in most included 343 studies. 344

Research on cardiac involvement after COVID-19 is evolving with a fast-pace, given the 345 possible clinical impact of such an interaction on increased morbidity and mortality rates. 346

Evidence from current studies suggests a higher risk of cardiac involvement in patients with 347 severe COVID-19 than those with a milder disease (Supplementary Table S8 ). Assessment of 348 other risk factors for cardiac involvement was not possible due to individual limitations of the 349 studies and limited available data. Moreover, symptoms did not seem to correlate with cardiac 350 involvement, as shown by the high percentage of cardiac findings on CMR in asymptomatic 351 patients in the moderate-severe COVID-19 group compared to the mild COVID-19 group. This 352 finding could be due to the nonspecific nature of these symptoms, which could be explained by 353 non-cardiac causes such as pulmonary or psychiatric involvement (depression, anxiety), which 354 have been increasingly reported with 26, 42) . Nonetheless, these studies suggest 355 that cardiac assessment in the short and long-term is warranted, irrespective of symptoms, and more importantly in high-risk groups, including those with severe COVID-19 and/or baseline 357 comorbidities, and those who could be at a high risk for cardiac dysfunction and/or arrythmias 358 with subclinical myocarditis, such as athletes. 359

Cardiac workup should take the urgency, cost and availability into account, among other 360 considerations. Included studies suggest that CMR was the most sensitive method for cardiac 361 sequelae detection, especially in the short-term (<3 months) period after Detection in this period could be further improved when combining CMR with ECG, cardiac 363 biomarkers evaluation and symptom assessment. In the medium-term recovery period (3-6 364 months), the combination of echocardiography, CMR, cardiac biomarkers and symptom 365 assessment could be a relevant strategy for cardiac assessment. 366

Studies assessing cardiac sequelae after COVID-19 to date included heterogeneous 367 populations, variable assessment methods and timeline, and most did not include baseline 368 cardiac study and/or control groups. Thus, we could not exclude the presence at baseline of at 369 least part of the observed cardiac findings in some studies. Moreover, cardiac sequelae, in turn, 370 could be part of increasingly reported syndromes post COVID-19, such as long COVID syndrome, 371 with symptoms such as palpitations and dyspnea stretching past the acute phase (60), and/or 372 multisystem inflammatory syndrome which causes multi-organ damage, many weeks after 373 . Also, despite that current trials did not conclude any significant burden of 374 cardiac sequelae with major utilized drugs for COVID-19 treatment (62-64), these should be 375 considered in sequelae assessment. Thus, in order to categorize cardiac findings as either 376 occurring alone, as part of these syndromes, or due to COVID-19 treatment, proper assessment 377 of other organ systems and drug effects could be warranted. 378

To improve the current understanding of cardiac sequelae after COVID-19, we believe 379 future studies should include larger number of participants, with prospective serial and long-380 term follow-up. Assessments shall be done at different time points up to several months after 381 recovery, with standard questionnaires for cardiac symptoms, and objectively by multiple 382 modalities including ECG, cardiac biomarkers (NT-proBNP, TN-I), echocardiography, and 383 possibly CMR. We believe it is important to perform inter-group analysis to identify risk factors 384 for cardiac involvement after recovery. Moreover, the presence of recent pre-COVID-19 cardiac 385 assessments are optimal to compare progression of cardiac manifestations and the inclusion of 386 one or more control groups, matched to baseline characteristics, with negative SARS-CoV-2 387 swabs and serologies, is crucial to control for possible confounders. 

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Chest pain: 25%.Cardiac arrest and acute myocardial infarction: 25%.

89.5% NA Inferior regional wall motion abnormality: (0.5%);LV hypertrophy: : (0.5%); pulmonary hypertension:(0.5%);worsening of pre-existing heart failure: (0.5%).

100% NA NA NA NA Chest pain: 5%;Palpitations: 9%.None.

100%. Myocardial edema: 54%;LGE (