Thrombosis in Multisystem Inflammatory Syndrome Associated with COVID-19 in Children: Retrospective Cohort Study Analysis and Review of the Literature
Abstract
:1. Introduction
2. Methods
2.1. Study Design
2.2. Epidemiological Data
2.3. Diagnostics for SARS-CoV-2 Infection
2.4. Evaluated Parameters and Their Outcomes
2.5. Statistical Analysis
3. Results
3.1. Analysis of Predictors of Thrombotic Events
3.2. Course of Disease Characteristics of Patients with Thrombotic Events
3.3. Clinical Manifestations
3.4. Laboratory Data
3.5. General Characteristics of Patients with Thrombotic Events
3.6. Venous Thromboses
3.7. Arterial Thromboses
3.8. Treatment
3.9. Outcomes
4. Discussion
5. Research Limitations
6. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
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Characteristics | MIS-C with Thrombosis (n = 8) | MIS-C without Thrombosis (n = 52) | p |
---|---|---|---|
Demographics | |||
Age (months), mean (min–max) | 90.3 (3–204) | 88.1 (3–204) | 0.757 |
Gender, boys, n (%) | 6 (75) | 28 (54) | |
Number of days before admission, mean (min–max) | 6.8 (2–15) | 10.4 (2–32) | 0.096 |
Duration of hospitalization, days, mean (min–max) | 59 (27–90) | 31 (10–80) | 0.0086 |
Epidemiological data | |||
Number of children with detected IgG to SARS-CoV-2, n (%) | 6 (86) | 48/57 (96) | 0.253 |
Number of children with detected IgM to SARS-CoV-2, n (%) | 0 (0) | 10/58 (17) | 0.197 |
Family contact, n (%) | 2 (25) | 28 (55) | 0.115 |
Clinical symptoms | |||
Duration of fever (days), mean (min–max) | 19 (1–59) | 12 (3–32) | 0.388 |
Gastrointestinal symptoms, n (%) | 4 (50) | 35 (67) | 0.339 |
Neurological symptoms, n (%) | 6 (75) | 24 (46) | 0.128 |
Coma, n (%) | 3 (37) | 0 (0) | 0.000006 |
Aseptic meningitis, n (%) | 5 (62) | 7 (13) | 0.0012 |
Polyserositis, n (%) | 4 (50) | 30 (58) | 0.682 |
Pharyngitis, n (%) | 2 (25) | 29 (56) | 0.104 |
Cervical lymphoadenopathy, n (%) | 7 (87) | 45 (86) | 0.940 |
Rash, n (%) | 2 (25) | 32 (61) | 0.052 |
Conjunctivitis, n (%) | 4 (50) | 38 (73) | 0.184 |
Cheilitis n (%) | 3 (37) | 37 (71) | 0.060 |
Glossitis/stomatitis, n (%) | 5 (62) | 39 (75) | 0.456 |
Respiratory symptoms, n (%) | 3 (37) | 13 (25) | 0.456 |
Palms and feet edema/desquamation, n (%) | 5 (62) | 39 (75) | 0.456 |
Soft tissues sedema, n (%) | 5 (62) | 38 (73) | 0.536 |
Hepatomegaly, n (%) | 6 (75) | 41 (79) | 0.805 |
Splenomegaly, n (%) | 4 (50) | 24 (46) | 0.839 |
Arthritis/arthralgia, n (%) | 1 (12) | 21 (40) | 0.127 |
Myocardial damage, n (%) | 5 (62) | 33 (64) | 0.903 |
Acute heart failure, n (%) | 3 (37) | 9 (17) | 0.183 |
Pulmonary edema, n (%) | 4 (50) | 9 (17) | 0.036 |
Coronary artery dilatation, n (%) | 1/8 (12.5) | 7 (13.5) | 0.952 |
Myocarditis, n (%) | 5 (62) | 25 (48) | 0.447 |
Pericarditis, n (%) | 2/7 (28) | 26 (50) | 0.286 |
ICU admission, n (%) | 7 (87) | 24 (46) | 0.029 |
Artificial lung ventilation, n (%) | 3 (37) | 7 (13) | 0.089 |
Macrophage activation syndrome, n (%) | 4 (50) | 9 (17) | 0.036 |
Laboratory data | |||
Hemoglobin (n.v. 120–140 g/L), mean (min–max) | 93 (73–114) | 104 (63–158) | 0.111 |
White blood cells (n.v. 4–9 × 109/L), mean (min–max) | 22.4 (6.6–58) | 13.9 (2–43) | 0.126 |
Patients with leukocytosis, n (%) | 3 (37) | 19 (36) | 0.958 |
Platelets (n.v. 150–350 × 109/L), mean (min–max) | 76.8 (4–182) | 284 (26–1077) | 0.0132 |
Patients with thrombocytosis, n (%) | 0 (0) | 15 (28) | 0.079 |
Patients with thrombocytopenia, n (%) | 7 (87) | 29 (56) | 0.088 |
Patients with platelets < 103 × 109/L *, n (%) | 7 (87) | 21 (41) | 0.014 |
ESR (n.v. 0–30 mm/h), mean (min–max) | 39 (4–70) | 42 (2–112) | 0.856 |
Patients with increased ESR, n (%) | 6 (75) | 37 (71) | 0.822 |
C-reactive protein (n.v. 0–5 mg/L), mean (min–max) | 107.2 (19.7–245.6) | 124 (0.3–335) | 0.940 |
Ferritin (n.v. 7–140 ng/mL), mean (min–max) | 583 (221–853) | 454 (43–2254) | 0.106 |
Patients with increased ferritin, n (%) | 6/6 (100) | 33/46 (72) | 0.132 |
ALT (n.v. <33 IU/L), mean (min–max) | 658 (9.9–3101) | 135 (10–2816) | 0.320 |
Patients with increased ALT, n (%) | 5 (62) | 21/51 (41) | 0.258 |
AST (n.v. <39 IU/L), mean (min–max) | 608 (12.6–2383) | 128 (13–2402) | 0.413 |
Patients with increased AST, n (%) | 5 (62) | 30/51 (59) | 0.843 |
Total bilirubin (n.v. 0–21 μmol/L), mean (min–max) | 11.1 (1.5–28.8) | 17.6 (1.2–372) | 0.887 |
Albumin (n.v. 28–54 g/L), mean (min–max) | 31.6 (25–42.3) | 32.2 (20–46.1) | 0.760 |
Triglycerides (n.v. 0.2–1.7 mmol/L), mean (min–max) | 3.1 (0.7–7.3) | 2.5 (0.6–7.7) | 0.732 |
Creatinine (n.v. 28–70 μmol/L), mean (min–max) | 80.1 (30–225) | 69.1 (14–298) | 0.769 |
LDH (n.v. 240–480 IU/L), mean (min–max) | 1020 (148–3325) | 410.3 (79–2390) | 0.063 |
Patients with increased LDH, n (%) | 4 (50) | 11/51 (21.57) | 0.085 |
Procalcitonin (n.v. 0–0.5 μg/mL), mean (min–max) | 53.9 (0.1–183) | 10.8 (0.1–88.6) | 0.458 |
Аntithrombin III (n.v. 80–120%), mean (min–max) | 69.8 (16.6–103.7) | nd | nd |
Protein C (n.v. 60–140%), mean (min–max) | 96.0 (28.7–178.1) | nd | nd |
Troponin (n.v. 0–14 ng/mL), mean (min–max) | 16.3 (0.1–100) | 23.3 (0–450) | 0.789 |
Fibrinogen (n.v. 2.0–3.9 g/L) mean (min–max) | 2.7 (0.1–4.1) | 3.8 (0.1, 8.8) | 0.191 |
D-dimer (n.v. 0–500 ng/mL), mean (min–max) | 6537 (3026–14,800) | 2838 (433–8836) | 0.0007 |
Patients with D-dimer > 3778 ng/mL *, n (%) | 7 (87) | 12/51 (23) | 0.0003 |
NT-proBNP (n.v. < 160 pg/mL *), mean (min–max) | 5795 (10–30,879) | 596 (10–6783) | 0.066 |
Increase in NT-proBNP, n (%) | 5/7 (71) | 16/48 (33) | 0.053 |
Creatine kinase-MB (n.v. 0–25 IU/L), mean (min–max) | 31.9 (9–70.9) | 27.4 (5.0–94.7) | 1.0 |
Treatment and outcome | |||
IVIG (1.8–2 g/kg/course), n (%) | 6 (75) | 32 (61) | 0.462 |
Acetylsalicylic acid, n (%) | 4 (50) | 33 (63) | 0.466 |
GCS (dexamethasone 10–20 mg/m2/day), n (%) | 6 (75) | 35 (67) | 0.663 |
Biologic treatment, n (%) | 2 (25) | 3 (6) | 0.066 |
Deaths, n (%) | 1 (13) | 2 (4) | |
CNS damage (stroke), n (%) | 3 (38) | 0 | 0.083 |
Predictors | OR (95% CI) | p |
---|---|---|
Coma | - | 0.000006 |
Aseptic meningitis | 10.7 (2.1–55.1) | 0.001 |
Platelets ≤ 103 × 109/L | 9.6 (1.1–83.3) | 0.017 |
D-dimer > 3778 ng/mL | 22.8 (25–203.9) | 0.0003 |
Ferritin > 594 ng/mL | 8.7 (1.4–54.9) | 0.010 |
LDH > 382 U/L | 6.2 (1.13–33.9) | 0.022 |
Elevation of NT-proBNP levels | 5.0 (0.9–28.7) | 0.053 |
Elevation of NT-proBNP > 280 pg/mL | 6.73 (1.15–39.1) | 0.019 |
ID, # | Sex, Age | SARS-CoV-2 Confirmation | Clinic Signs | Type of Thrombosis | Treatment of MIS-C/Thrombosis | Outcome |
---|---|---|---|---|---|---|
1 | M. 1.5 y. | IgG (+) | MIS-C, Kawasaki-like features, MOFS, shock, myocarditis, severe CNS damage, distal gangrene | Arterial thrombosis of the lower extremities, multiple ischemic strokes, venous thrombosis (morphological) | IVIG 2.0 g/kg 2 courses, DEXA 15 mg/m2/day, MP pulse therapy, cyclophospha-mid pulse therapy, etanercept, heparin/nadroparin, ASA | Recovery with residual severe neurological sequelae |
2 | M. 8 y. | IgG (+) | MIS-C, Kawasaki-like features, mild coronary dilation, MOFS, shock, severe CNS involvement, | Bilateral ischemic stroke Secondary renal TMA | IVIG 2.0 g/kg/course DEXA 15 mg/m2/day heparin/nadroparin, ASA | Full recovery in 2 years |
3 | F. 4 y. | IgG (+) | Kawasaki-like features, MIS-C, shock, MOFS, severe damage to the central nervous system, aHUS, secondary HFS | Secondary renal TMA (aHUS), catheter-associated thrombosis of the femoral vein, disseminated PE | IVIG 2 courses, DEXA15 mg/m2/day Tocilizumab, Eculizumab, Heparin/nadroparin | Recovery with residual neurological sequelae in 2 years and full restoration of the renal function on the eculizumab |
4 | M. 15 y. | IgG (+) | MIS-C, (hereditary AT III deficiency) | Deep vein thrombosis of the upper and lower extremities | IVIG, dexamethasone, ASA, Heparin/nadroparin/warfarin | Recanalization of clots, recovery |
5. | F. 13 y. | IgG (+) | MIS-C | Deep vein thrombosis of the lower extremity | Heparin/nadroparin/warfarin | Recanalization of clots, recovery |
6 | M. 5 m. | IgG (+) | MIS-C with Kawasaki-like features, severe, MOFS, shock | Secondary renal TMA | IVIG, DEXA, heparin/nadroparin, ASA | Full recovery |
7 | M. 3 m. | PCR (+) IgG (+) | MIS-C, severe MOFS, shock, RDS, myocarditis, sepsis, severe CNS involvement, (background—CVSD) | Cerebral sinus thrombosis, deep vein thrombosis—branches of VCS, VCI | IVIG, DEXA, Heparin/nadroparin | Recanalization of clots, recovery |
8 | M. 17 m | IgG (+) | MIS-C, severe MOFS, secondary HFS. Comorbidity—Prader–Willi syndrome | Deep vein thrombosis, PE | DEXA, heparin/nadroparin | Fatal outcome |
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Bregel, L.V.; Efremova, O.S.; Kostyunin, K.Y.; Rudenko, N.Y.; Kozlov, Y.A.; Albot, V.V.; Knyzeva, N.А.; Tolmacheva, O.V.; Ovanesyan, S.V.; Barakin, A.O.; et al. Thrombosis in Multisystem Inflammatory Syndrome Associated with COVID-19 in Children: Retrospective Cohort Study Analysis and Review of the Literature. Biomedicines 2023, 11, 2206. https://doi.org/10.3390/biomedicines11082206
Bregel LV, Efremova OS, Kostyunin KY, Rudenko NY, Kozlov YA, Albot VV, Knyzeva NА, Tolmacheva OV, Ovanesyan SV, Barakin AO, et al. Thrombosis in Multisystem Inflammatory Syndrome Associated with COVID-19 in Children: Retrospective Cohort Study Analysis and Review of the Literature. Biomedicines. 2023; 11(8):2206. https://doi.org/10.3390/biomedicines11082206
Chicago/Turabian StyleBregel, Liudmila V., Olesya S. Efremova, Kirill Y. Kostyunin, Natalya Y. Rudenko, Yury A. Kozlov, Vadim V. Albot, Natalya А. Knyzeva, Olga V. Tolmacheva, Svetlana V. Ovanesyan, Alexander O. Barakin, and et al. 2023. "Thrombosis in Multisystem Inflammatory Syndrome Associated with COVID-19 in Children: Retrospective Cohort Study Analysis and Review of the Literature" Biomedicines 11, no. 8: 2206. https://doi.org/10.3390/biomedicines11082206