Background
Methods
Literature search
Study selection
Data extraction
Subgroup analysis
Quality assessment
Statistical analysis
Results
Study characteristics
First author (year) | Journal | Study design | Study sites (countries) | Patient description | Study period | Population (n) | Reason for exclusion (n) | Number of patients including in the analysis | Age (years) | Sex (n, male/female) | Diagnosis of COVID-19 by RT-PCR | Other tests for cardiac evaluation | Presence of cardiac symptoms at the time of CMR | Cardiac enzyme level at the time of CMR | Population restricted to athletes | CMR field strength | CMR scan time | CMR sequences |
---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
Ng et al. (2020) | JACC Cardiovasc Imaging | Retrospective, single-center, observational | Hong Kong | Recovered COVID-19 patients | NA | 16 | Ischemic etiology (1) | 15 | Median 68 (IQR: 53–69) | 9/7 | Yes | Troponin, CRP | Various (5/16) | Undetermined | No | 1.5 T (GE) | Median 56 days after recovery | Cine, Mapping (T1 and T2), LGE |
Huang et al. (2020) | JACC Cardiovasc Imaging | Retrospective, single-center, observational | China | Recovered COVID-19 patients | NA | 26 | None | 26 | Median 38 (IQR: 32–45) | 10/16 | Yes | hs-troponin I assay | Yes (26) | Normal (26) | No | 3 T (Skyra, Siemens) | Median 47 days (IQR: 36–58) after symptom onset | Cine, T2WI, mapping (T1 and T2), LGE |
Rajpal et al. (2020) | JAMA Cardiol | Prospective, single-center, observational | U.S | Athletes recovered from COVID-19 | Between June 2020 and August 2020 | 26 | None | 26 | Mean 19.5 (SD: 1.5) | 16/10 | Yes | ECG, troponin I assay, echocardiography | Various (12/26) | Normal (26) | Yes | 1.5 T (Magnetom Sola, Siemens) | 11–53 days after recommended quarantine | Cine, mapping (T1 and T2), LGE, ECV |
Knight et al. (2020) | Circulation | Retrospective, single-center, observational | England | Recovered COVID-19 | Until April 2020 | 51 | Acute coronary syndromes (6) pulmonary emboli (12), or known cardiac pathology (7) | 29 | Mean (SD) 64 (9) | 24/5 | Yes | NR | Yes (29) | Undetermined | No | 1.5 T (Avanto Aera;Siemens) | Mean 46 days after symptom onset | Cine, Mapping (T1 and T2), LGE, Adenosine stress perfusion |
Puntmann et al. (2020) | JAMA Cardiol | Prospective, single-center, observational | Germany | Recovered COVID-19 patients | Between April 2020 and June 2020 | 100 | None | 100 | Mean 49 (SD: 14) | 53/47 | Yes | Hs-troponin T assay | Various (36/100) | Undetermined | No | 3 T (Skyra, Siemens) | Median 71 (IQR 64–92) after COVID-19 diagnosis | Cine, Mapping (T1 and T2) LGE |
Eiros et al. (2020) | MedRxiv | Retrospective, single-center observational | Spain | Recovered COVID-19 patients (health care workers) | Between May 25, 2020 and June 12, 2020 | 142 | Claustrophobia (1),history of hypertrophic myocardiopathy (1), inherited immune deficiency (1) | 139 | Median 52 (IQR: 41–57) | 39/100 | 103 diagnosed by RT-PCR, 36 by serology | ECG; NT-pro-BNP and hs-troponin T assays | Various (91/139) | Normal (138), elevated (1) | No | 1.5 T (Achiva, Philips) | Median 10.4 (IQR: 9.3–11.0) weeks after symptom onsetb | Cine, T2WI Mapping (T1 and T2), LGE |
Vago et al. (2020) | JACC Cardiovasc Imaging | Retrospective, single-center observational | Hungary | Athletes recovered from COVID-19 | NA | 12 | None | 12 | Median 23 (IQR: 20–23) | 2/10 | Yes | CRP, NT-pro-BNP, and hs-troponin T assays | Yes (12) | Normal (11), undetermined (1) | Yes | 1.5 T (Magnetom, Aera, Siemens) | Median 17 (IQR: 17–19) days after positive PCR in 10 female athletes, 67 and 90 days in 2 male athletes | Cine, T2WI, mapping (T1 and T2), LGE |
Brito et al. (2020) | JACC Cardiovasc Imaging | Retrospective, single-center observational | U.S | Student athletes recovered from COVID-19 | By August 2020 | 54 | Claustrophobia (1), no CMR (5) | 48 | Median 19 (range 19–21)a | 46/8a | PCR or antibody test | Echocardiography, troponin I assay, ECG | Various (37/48) | Undetermined | Yes | 1.5 T (Magnetom, Aera; Siemens) | Median 27 days (range 22–33 days) from diagnosis of COVID-19 | Cine, T2WI, mapping (T1 and T2), LGE |
Clark et al. (2021) | Circulation | Retrospective, single-center, observational | U.S | Athletes recovered from COVID-19 | Since August 2020 | 22 | None | 22 | Median 20 | 9/11 | Yes | ECG, troponin I assay, echocardiography | NR | Normal (18) | Yes | 1.5 T (Avanto fit, Siemens) | Median 52 days after COVID-19 diagnosis | Cine, mapping (T1 and T2), LGE, ECV |
Malek et al. (2021) | J Magn Reson Imaging | Retrospective, single-center observational | Germany | Student athletes recovered from COVID-19 | Diagnosed COVID-19 between August and October 2020 | 26 | None | 26 | Median 19 (IQR 19–21) | 5/21 | Yes | ECG, CRP, hs-troponin I assay | NR | Normal (26) | Yes | 1.5 T (Magnetom Avanto Fit, Siemens) | Median 32 days (IQR 22–62 days) after diagnosis | Cine, T2WI, Mapping (T1 and T2), LGE |
Li et al. (2021) | Radiology | Prospective, single-center, observational | China | Recovered COVID-19 patients | Between May and September 2020 | 78 | Due to discharge < 90 days (n = 5), abnormal cardiac enzyme (n = 3), abnormal ECG findings (n = 4), not underwent CMR (n = 16), history of cardiovascular disease or HTN (7), contrast allergy (1), image quality (2) | 40 | Mean 54 (SD: 12) | 24/160 | Yes | ECG, CRP, CK, CKMB Troponin I assays | No | Normal (40) | No | 3 T (Skyra, Siemens) | Mean 124 ± 17 days after discharge, Mean 158 ± 18 after admission | Cine, LGE, Strain |
Starekova et al. (2021) | JAMA Cardiology | Retrospective, single-center observational | U.S | Athletes recovered from COVID-19 | Between January 1, 2020, and November 29, 2020 | 145 | none | 145 | Mean 20 (range: 17–23) | 108/37 | Yes | ECG, Troponin I, NT-proBNP, CRP, ESR assays and echocardiography | Various (1/145) | Normal (141), elevated (2) | Yes | 1.5 T or 3 T (GE) | Median 15 days after diagnosis | Cine, T2WI, Mapping (T1 and T2), LGE |
Wang et al. (2021) | J Cardiovasc Magn Reson | Prospective, single-center, observational | China | Recovered COVID-19 patients | From May 8 to July 20, 2020 | 47 | History of cardiovascular disease (3) | 44 | Mean 47.6 (SD: 13.3) | 19/25 | Yes | NR | NR | Undetermined | No | 3 T (Ingenia, Philips) | Mean 102.5 ± 20.6 days after diagnosis | Cine, T2WI, T2 star map, LGE, strain |
Pan et al. (2021) | J Magn Reson Imaging | Prospective, single-center observational | China | Recovered COVID-19 patients | Between March 2020 and April 2020 | 31 | History of cardiovascular disease, presence of cardiac symptoms, or elevated cardiac enzymes (10) | 21 | Median 36 (IQR: 31–47) | 10/11 | Yes | NR | No | Undetermined | No | 3 T (Signa, GE) | Median 46 day (IQR 43–50 days) | Cine, T2WI, Mapping (T1 and T2) |
Zhou et al. (2021) | Plos one | Prospective, single-center, observational | Hong Kong | Recovered COVID-19 patients | Diagnosed up to April 2020 | 97 | No CMR (85) | 12 | Mean 46.5 (SD:18.6)a | 52/45a | Yes | ECG, Troponin I, NT-proBNP assay and echocardiography | NR | Normal (7), elevated (4) | No | NR | NR | Cine, T2WI, LGE |
Kotecha et al. (2021) | Eur Heart J | Retrospective, Multicenter study | U.K | Recovered COVID-19 patients | Discharged up to 20 June 2020 | 820 | No CMR (672) | 148 | Mean 64 (SD:12) | 104/44 | Yes | NR | NR | Undetermined | No | 1.5 T (Magnetom, Aera, Siemens) | Median 56 days (IQR 30–88 days) after discharge | Cine, Mapping (T1 and T2), LGE, stress perfusion |
First author (year) | CMR abnormality, n (%) | Fulfilled diagnostic criteria of myocarditis on CMRa (n) | Cine abnormality (n) | T1 mapping abnormality (n) | T2w abnormality (n) | T2 mapping abnormality (n) | T2 segment | T2 abnormality (T2w or T2 map) | ECV abnormality (n) | Myocardial LGE (n) | Pericardial LGE (n) | Total LGE | LGE segment | LGE pattern | Increased T2 value without LGE (n) | LGE without T2 elevation (n) | Pericardial effusion (n) |
---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
Ng et al. (2020) | 9 (66.7%) | 4 | NR | 5 | NA | 5 | Global | 5 | NR | 3 | NR | 3 | NR | Non-ischemic (3)a | 2 | 1 | 0 |
Huang et al. (2020) | 15 (57.7%) | 7 | NR | NR | 14 | NR | NR | 14 | NR | 8 | 0 | 8 | Inferior or lateral at the mid and basal segments | Focal linear subepicardial and patchy mesocardial | 7 | 1 | 7 |
Rajpal et al. (2020) | 13 (50%) | 4 | 1 | 0 | NA | 4 | Mid-inferoseptal (3) mid-anteroseptal (2), basal inferoseptal (1) | 4 | 1 | 12 | 0 | 12 | Septal (19), inferior or lateral (5) at the mid and basal segments | Patchy (6), linear (3), epicardial (1), RV insertion (2) | 0 | 8 | 2 |
Knight et al. (2020) | 20 (69%) | NR | 2 | NR | NA | 0 | NR | 0 | NA | 20 | 0 | 20 | NR | Non-ischemic (11), ischemic (5), dual (4) | NR | NR | 2 |
Puntmann et al. (2020) | 78 (78%) | NR | NR | 73 | NA | 60 | NR | 60 | NR | 32 | 22 | NR | NR | Nonischemic (20), ischemic (12), pericardial (22) | NR | NR | 20 |
Eiros et al. (2020) | 104 (75%) | 51 | 7 | 58 | 6 | 6 | NR | NR | 52 | 10 | 0 | 10 | NR | NR | NR | NR | 42 |
Vago et al. (2020) | 0 (0%) | 0 | 0 | 0 | 0 | 0 | NR | 0 | NA | 0 | 0 | 0 | NR | NR | 0 | 0 | NR |
Brito et al. (2020) | 26 (54.2%) | 0 | 1 | 9 | 0 | 0 | NR | 0 | NA | 1 | 19 | NR | Lateral | Pericardial (19), myocardial (1) | 0 | 1 | 28 |
Clark et al. (2021) | 4 (6.8%) | 2 | 0 | NA | NA | 1 | Mid septum | NR | NA | 3 | 1 | 4 | NR | NR | NA | NA | NA |
Malek et al. (2021) | 7 (26.9%) | 0 | 2 | 0 | 3 | 1 | NR | 4 | 0 | 1 | 0 | 1 | Inferolateral segment | Mid wall | 4 | 1 | 2 |
Li et al. (2021) | 24 (60%) | NR | NA | NA | NR | NA | NR | NA | 24 | 1 | 0 | 1 | Mid-inferior segment | NR | NR | NR | NA |
Starekova et al. (2021) | 4 (2.8%) | 2 | NA | 2/141 | 2 | 1/102 | Apical inferolateral, and basal inferior segment | 2 | NR | 4 | 1 | 4 | Apical inferolateral, and basal inferior segment | Mid myocardial and subepicardial (1), epicardial (1), mid myocardial (2) | 0 | 2 | 1 |
Wang et al. (2021) | 13 (29.5%) | NA | NA | NA | NA | NA | NA | NA | NR | 13 | 0 | 13 | Inferior wall and inferior-lateral wall of the basal segment | Mid myocardium, subepicardium | NA | NA | NA |
Pan (2021) | 15 (71.4%) | NA | 3 | 5 | NR | 10 | NR | 10 | NR | NR | NR | NR | NR | NR | NR | NR | NA |
Zhou (2021) | 1 (8.3%) | 0 | 0 | NR | 0 | NR | NR | 0 | NR | 1 | 0 | 1 | Basal anterolateral segment | Subepicardial | 0 | 1 | NA |
Kotecha (2021) | 80 (54.1%) | 12 | 17 | 23/137 | NR | 12/137 | NR | 12/137 | NR | 70/144 | 0 | 70/144 | NR | Subepicardial (28), midwall (14), subendocardia and subepicardial (3), subendocardial and midwall (2) | NA | NA | 8 |
Pooled prevalence of abnormal CMR findings
Parameter (number of studies) | Overall | Study population | Cardiac enzyme level† | |||||||
---|---|---|---|---|---|---|---|---|---|---|
Prevalence (%) | Heterogeneity* | Non-athletes (n = 10) | Athletes (n = 6) | Normal (n = 9) | Undetermined (n = 8) | |||||
Prevalence (%) | Heterogeneity* | Prevalence (%) | Heterogeneity* | Prevalence (%) | Heterogeneity* | Prevalence (%) | Heterogeneity* | |||
Abnormal CMR findings (n = 16) | 46.4 [43.2–49.7] | < 0.01, 95% | 62.5 [58.5–66.4] (n = 10) | < 0.01 86% | 17.1 [13.3–21.7] (n = 6) | < 0.01, 92% | 35.9 [31.7–40.3] (n = 9) | < 0.01, 95% | 59.4 [54.5–64.04] (n = 8) | < 0.01, 77% |
Diagnosis of myocarditis on CMR (n = 12) | 14.0 [11.6–16.8] | < 0.01, 93% | 23.9 [19.8–28.5] (n = 6) | < 0.01, 85% | 2.5 [01.3–5.0] (n = 6) | 0.11, 64% | 15.2 [12.1–19.0] (n = 8) | < 0.01, 90% | 12.0 [8.5–16.8] (n = 5) | < 0.01, 90% |
Presence of pericardial LGE (n = 14) | 5.0 [3.8–6.7] | < 0.01, 94% | 4.1 [2.7–6.1] (n = 8) | > 0.99, 98% | 6.7 [4.4–10.0] (n = 6) | < 0.01, 86% | 10.4 [7.1–15.1] (n = 5) | < 0.01, 88% | 24.8 [20.6–29.6] (n = 7) | < 0.01, 96% |
Presence of myocardial LGE (n = 15) | 20.7 [18.1–23.5] | < 0.01, 93% | 28.8 [25.2–32.7] (n = 9) | < 0.01, 92% | 6.7 [4.4–10.0] (n = 6) | < 0.01, 82% | 8.6 [6.0–12.1] (n = 8) | < 0.01, 83% | 36.5 [31.8–41.4] (n = 7) | < 0.01, 93% |
Presence of LGE (myocardial or pericardial) (n = 13) | 20.5 [17.7–23.6] | < 0.01, 92% | 28.1 [24.1–32.4] (n = 8) | < 0.01, 92% | 7.8 [5.2–11.7] (n = 5) | < 0.01, 84% | 8.3 [5.8–11.8] (n = 8) | < 0.01, 85% | 45.5 [39.2–51.9] (n = 5) | < 0.01, 75% |
Increased native T1 value on the T1 map (n = 10) | 26.3 [23.1–29.8] | < 0.01, 97% | 39.8 [35.2–44.6] (n = 5) | < 0.01, 92% | 4.4 [2.4–7.7] (n = 5) | 0.02, 81% | 1.0 [0.1–8.7] (n = 4) | > 0.99, 0% | 35.7 [30.7–41.1] (n = 6) | < 0.01, 88% |
T2 abnormality (n = 12) | 16.9 [14.3–19.8] | < 0.01, 94% | 22.9 [19.3–26.9] (n = 7) | < 0.01, 95% | 4.4 [2.4–8.0] (n = 5) | 0.08, 75% | 10.4 [7.1–15.1] (n = 5) | < 0.01, 88% | 24.8 [20.6–29.6] (n = 7) | < 0.01, 96% |
T2 abnormality without LGE (n = 8) | 4.0 [2.3–6.7] | 0.98, 91% | 12.9 [6.8–22.9] (n = 3) | 0.061, 73% | 1.6 [0.6–4.1] (n = 5) | > 0.99, 90% | 5.7 [3.3–9.5] (n = 5) | < 0.01, 83% | 2.2 [0.5–8.2] (n = 4) | > 0.99, 76% |
Presence of myocardial LGE without T2 abnormality (n = 7) | 4.0 [2.3–7.0] | 0.01, 58% | 3.8 [0.2–46.6] (n = 3) | 0.85, 0% | 4.1 [2.2–7.4] (n = 4) | < 0.01, 71% | 4.4 [2.4–8.0] (n = 5) | < 0.01, 64% | 1.6 [0–100] (n = 2) | > 0.99, 0% |
Pericardial effusion (n = 11) | 15.7 [13.2–18.5] | < 0.01, 93% | 17.3 [14.1–21.0] (n = 6) | < 0.01, 86% | 12.8 [9.3–17.5] (n = 5) | < 0.01, 89% | 5.2 [3.0–9.0] (n = 5) | < 0.01, 75% | 17.0 [13.4–21.4] (n = 6) | < 0.01, 91% |
Ventricular systolic dysfunction on cine (n = 10) | 4.7 [3.3–6.6] | 0.17, 62% | 7.4 [2.9–17.3] (n = 4) | 0.28, 27% | 1.3 [0.4.–4.5] (n = 6) | 0.98, 0% | NA | NA | 7.4 [3.1–16.8] (n = 4) | 0.34, 22% |
Prevalence of abnormal CMR findings relative to patient characteristics
Non-athletes vs. athletes
Normal cardiac enzyme level vs. undetermined cardiac enzyme level
Parameter | Univariable meta-regression analysis | Multivariable meta-regression analysis | Residual heterogeneity after multivariable meta-regression analysis | |
---|---|---|---|---|
p-value | I2 | p-value | I2 | |
Abnormal CMR findings | 92.8% | |||
Athlete group | 0.002 | 93.4% | 0.018 | |
Undetermined cardiac enzyme level group | 0.061 | 94.6% | 0.173 | |
Diagnosis of myocarditis on CMR | N/A | |||
Athlete group | < 0.001 | 90.6% | N/A | |
Undetermined cardiac enzyme level group | 0.405 | 93.7% | N/A | |
Presence of myocardial LGE | 93.9% | |||
Athlete group | 0.050 | 95.4% | 0.206 | |
Undetermined cardiac enzyme level group | 0.033 | 94.0% | 0.138 | |
T2 abnormality | N/A | |||
Athlete group | 0.035 | 97.2% | N/A | |
Undetermined cardiac enzyme level group | 0.629 | 96.9% | N/A | |
Pericardial effusion | N/A | |||
Athlete group | 0.753 | 93.8% | N/A | |
Undetermined cardiac enzyme level group | 0.353 | 92.1% | N/A |