Cardiopulmonary Complications after Pulmonary Embolism in COVID-19
Abstract
:1. Introduction
2. Results
2.1. COVID-19 Pneumonia Population during Hospitalization
2.2. Clinical Characteristics at Follow-up
2.3. Respiratory and Cardiovascular Consequences
2.3.1. CTPA Findings at Follow-up
2.3.2. Pulmonary Function and Six-Minute Walking Test
2.3.3. Echocardiography Findings
2.4. Laboratory Findings
2.4.1. Baseline Blood Test on Admission
2.4.2. Inflammatory and Thrombotic Biomarkers on Admission
2.4.3. Blood Test at Follow-up
2.4.4. Biomarkers of Interstitial Lung Disease, Inflammation, and Coagulation Collected on Admission
2.5. Factors Associated with Lung Abnormalities
3. Discussion
3.1. Clinical Characteristics, Respiratory and Cardiovascular Consequences at Medium-Term Follow-up
3.2. Laboratory Findings and Inflammatory and Thrombotic Biomarkers on Admission
3.3. PCRLA Predictive Score
3.4. Strengths and Limitations
4. Material and Methods
4.1. Study Design
4.2. Description of Investigations Undertaken
4.3. Biomarkers
4.4. Ethics Statement
4.5. Statistical Analysis
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
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Blanco | All (n = 141) | Non-PE (n = 85) | PE (n = 56) | p Value |
---|---|---|---|---|
Age, yrs. | 62 (54–72) | 61 (54–73) | 63 (54–70) | 0.99 |
Age >65 yrs. | 63 (44.7) | 37 (43.5) | 26 (46.4) | 0.74 |
BMI, kg/m2 | 28.9 (26.2–31.6) | 28.5 (26–31.2) | 29.8 (26.6–31.6) | 0.13 |
Smoking status | 0.84 | |||
Current smoker, n (%) | 6 (4.3) | 3 (3.5) | 3 (5.4) | |
Former smoker, n (%) | 44 (31.2) | 26 (30.6) | 18 (32.1) | |
Smoking, Pack-year | 0 (0–10) | 0 (0–10) | 0 (0–10) | 0.73 |
Hypertension, n (%) | 65 (46.1) | 40 (47.1) | 25 (44.6) | 0.78 |
Diabetes mellitus, n (%) | 39 (27.7) | 23 (27.1) | 16 (28.6) | 0.84 |
Cardiovascular disease, n (%) | 25 (17.7) | 11 (12.9) | 14 (25) | 0.07 |
Cerebrovascular disease, n (%) | 9 (6.4) | 5 (5.9) | 4 (7.1) | 0.76 |
Chronic kidney disease, n (%) | 11 (7.8) | 5 (5.9) | 6 (10.7) | 0.29 |
COPD, n (%) | 5 (3.5) | 2 (2.4) | 3 (5.4) | 0.34 |
Asthma, n (%) | 7 (5) | 4 (4.7) | 3 (5.4) | 0.86 |
COVID-19 Admission | ||||
Physical examination | ||||
Respiratory rate, breaths per min | 24 (19–28) | 24 (19–28) | 22 (19–28) | 0.59 |
Heart rate, beats per min | 86 (74–99) | 87 (76–99) | 85 (71–103) | 0.57 |
Systolic BP, mm Hg | 125.00 (114–138) | 125 (114–139) | 125 (116–135) | 0.92 |
Diastolic BP, mm Hg | 71 (64–80) | 70 (63–78) | 72 (64–81) | 0.52 |
Temperature, °C | 36.9 (36.1–37.6) | 36.9 (36.2–37.6) | 36.9 (36.1–37.6) | 0.88 |
CURB 65 | 0.64 | 1 (0–2) | 1 (1–2) | 0.36 |
WHO severity classification | ||||
WHO category 3 | 6 (4.3) | 6 (7.1) | 0 (0) | 0.19 |
WHO category 4 | 67 (47.5) | 41 (48.2) | 26 (46.4) | |
WHO category 5 | 20 (14.2) | 9 (10.6) | 11 (19.6) | |
WHO category 6 | 27 (19.1) | 17 (20) | 10 (17.9) | |
WHO category 7 | 21 (14.9) | 12 (14.1) | 9 (16.1) | |
Treatment in hospital | ||||
High flow oxygen, n (%) | 37 (26.4) | 21 (25) | 16 (28.6) | 0.64 |
Non-Invasive ventilation, n (%) | 3 (2.1) | 1 (1.2) | 2 (3.6) | 0.33 |
Invasive ventilation, n (%) | 48 (34.3) | 29 (34.5) | 19 (33.9) | 0.94 |
Prone position, n (%) | 19 (13.5) | 16 (18.8) | 3 (5.4) | 0.02 |
Azithromycin, n (%) | 24 (17) | 15 (17.6) | 9 (16.1) | 0.78 |
Hydroxychloroquine, n (%) | 32 (22.7) | 15 (17.6) | 17 (30.4) | 0.77 |
Lopinavir/ritonavir, n (%) | 25 (17.7) | 12 (14.1) | 13 (23.2) | 0.24 |
Remdesivir, n (%) | 21 (15) | 13 (15.5) | 8 (14.3) | 0.85 |
IFNb, n (%) | 2 (1.4) | 1 (1.8) | 1 (1.2) | 0.76 |
Tocilizumab, n (%) | 35 (24.8) | 15 (26.8) | 20 (23.5) | 0.66 |
Systemic Corticosteroids, n (%) | 121 (85.8) | 73 (85.9) | 48 (85.7) | 0.97 |
ICU, n (%) | 59 (41.8) | 33 (38.8) | 26 (46.6) | 0.37 |
Columna1 | All (n = 119) | Non-PE (n = 76) | PE (n = 43) | p Value |
---|---|---|---|---|
FVC, (%) | 92 (83–101) | 92 (83–101) | 91 (83–102) | 0.87 |
FEV1, (%) | 94 (85–105) | 94 (85–105) | 95 (84–101) | 0.80 |
FEV1/FVC, (%) | 78.5 (41.6–83.1) | 78.9 (75–83.3) | 76.9 (74–82) | 0.32 |
DLCOc, (%) | 72 (58–87) | 71 (58–88) | 73 (59–88) | 0.42 |
KCOc, (%) | 77 (66–87) | 4.1 (3.2–4.6) | 3.9 (3.4–4.5) | 0.56 |
Walking distance, (m) | 510 (437–570) | 503 (428–540) | 512 (4663–584) | 0.07 |
Walking distance, (%) | 100 (89–114) | 98 (88–113) | 105 (96–114) | 0.40 |
Resting oxygen saturation, (%) | 97 (96–98) | 97 (96–98) | 97 (96–98) | 0.78 |
End-exercise oxygen saturation, (%) | 96 (94–97) | 96 (94.5–97) | 96 (94–97) | 0.29 |
Lowest oxygen saturation, (%) | 95 (93–95) | 95 (93–95.5) | 94 (93–95) | 0.49 |
All (n = 141) | Non-PE (n = 85) | PE (n = 56) | p Value | |
---|---|---|---|---|
Blood count, baseline | ||||
Hemoglobin, g/dL | 13.7 (12.6–15) | 13.7 (12.2–15) | 13.8 (12.9–15) | 0.72 |
Leucocyte count, 103/µL | 13.8 (9–19.8) | 14.6 (10–20.4) | 11.1 (7.8–16) | 0.04 |
Lymphocyte count, 103/µL | 1.1 (0.8–1.4) | 1.1 (0.8–1.4) | 1 (0.7–1.3) | 0.37 |
Neutrophil counts, 103/µL | 6.1 (4.3–9) | 5.7 (4–7.8) | 7 (4.6–10) | 0.03 |
Biochemical profile, baseline | ||||
Glucose, mg/dL | 124 (105–151) | 120 (104–140) | 130 (110–170) | 0.16 |
ALT, U/L | 31 (18–56) | 27 (17–65) | 36 (21–50) | 0.85 |
Urea, mg/dL | 35 (26–47) | 32 (24–45) | 38 (31–52) | 0.08 |
Creatinine, mg/dL | 0.8 (0.7–1.1) | 0.8 (0.7–1) | 0.9 (0.8–1.2) | 0.08 |
Sodium, mEq/L | 137 (135–140) | 138 (135–140) | 137 (135–139) | 0.34 |
Potassium, mEq/L | 4 (3.7–4.5) | 4 (3.7–4.4) | 4.1 (3.8–4.5) | 0.23 |
Cholesterol, mg/dL | 145 (121–170) | 140 (121–160) | 153 (122–187) | 0.03 |
Triglyceride, mg/dL | 135 (103–189) | 126 (94–177) | 152 (120–207) | 0.05 |
Coagulation function, baseline | ||||
PT, % | 81 (71–89) | 81 (73–90) | 81 (67–87) | 0.29 |
INR | 1.13 (1.07–1.23) | 1.13 (1.06–1.21) | 1.13 (1.10–1.30) | 0.13 |
Fibrinogen, mg/dL | 690 (513–833) | 686 (509–793) | 724 (595–860) | 0.18 |
Arterial blood test, baseline | ||||
PaO2/FiO2 ratio | 276 (217–324) | 290 (225–323) | 257 (214–324) | 0.27 |
pH | 7.46 (7.43–7.50) | 7.46 (7.43–1.50) | 7.46 (7.45–7.49) | 0.50 |
PaO2, mmHg | 63 (55–74) | 62 (55–71) | 64 (56–83) | 0.18 |
PaCO2, mmHg | 33 (29–36) | 33 (30–36) | 30 (28–35) | 0.11 |
Follow-up laboratory findings | ||||
Hemoglobin, g/dL | 14 (12.8–15) | 14.3 (12.9–15) | 14 (12.7–14.8) | 0.42 |
Leukocyte count, 103/µL | 6.6 (5.6–8.4) | 6.7 (5.6–8.5) | 6.3 (5.52–8.2) | 0.53 |
Neutrophil count, 103/µL | 3.6 (2.7–4.7) | 3.6 (2.7–4.8) | 3.6 (2.9–4.6) | 0.72 |
Lymphocyte count, 103/µL | 2.2 (1.8–2.8) | 2.2 (1.9–2.7) | 2.3 (1.6–2.8) | 0.74 |
Platelet count, 103/µL | 232 (200–275) | 230 (196–274) | 245 (212–276) | 0.34 |
ERS, mm/h | 15 (7–30) | 14 (7–23) | 17 (10–36) | 0.11 |
D-dimer, ng/mL | 108 (60–203) | 134 (72–216) | 84 (50–141) | 0.00 |
Elevated D-dimer, n (%) | 8 (6.7) | 7 (9.7) | 1 (2.1) | 0.13 |
CRP, mg/dL | 0.27 (0.12–0.46) | 0.27 (0.12–0.43) | 0.26 (0.13–0.53) | 0.61 |
Ferritin, ng/ml | 70 (33–137) | 81 (35–160) | 57 (33–101) | 0.07 |
LDH, U/L | 200 (174–225) | 195 (170–227) | 209 (188–225) | 0.21 |
NT-pro-BNP, pg/mL | 70 (35–169) | 60 (28–165) | 86 (41–160) | 0.29 |
Non-PE (n = 85) | PE (n = 56) | p Value | DLCOc ≥ 80% (n = 36) | DLCOc < 80% (n = 76) | p Value | No PCRLA (n = 43) | PCRLA (n = 53) | p Value | |
---|---|---|---|---|---|---|---|---|---|
LDH | |||||||||
Baseline, U/L | 360 (291–531) | 359 (287–493) | 0.92 | 354.50 (293–464) | 365 (291–528) | 0.63 | 376.50 (288–494) | 411 (299–588) | 0.54 |
Peak, U/L | 459 (343–626) | 434 (345–586) | 0.48 | 436 (349–523) | 475 (355–616) | 0.27 | 425 (334–600) | 473 (349–615) | 0.37 |
CRP | |||||||||
Baseline, mg/dL | 10.5 (4.8–19.2) | 10.8 (4.6–19.2) | 0.85 | 9.8 (5.0–19.0) | 12.0 (5.3–23.3) | 0.390 | 11.0 (5.2–18.4) | 10.9 (4.8–22.7) | 0.94 |
Peak, mg/dL | 14.6 (7.7–21.8) | 15.3 (8.5–25.8) | 0.59 | 15.1 (7–21.7) | 16.0 (8.8–26.8) | 0.37 | 14.4 (6.9–19.3) | 16.0 (7.7–26.8) | 0.25 |
ESR | |||||||||
Baseline, mm/h | 69 (46–88) | 68 (49–88) | 0.77 | 65 (49–85) | 69 (44.5–87.5) | 0.88 | 74 (50–92) | 66 (45–89) | 0.29 |
Peak, mm/h | 80 (57–104) | 76 (65–94) | 0.92 | 78.5 (62–103) | 76 (60.5–99.5) | 0.65 | 77 (62–101) | 75.50 (60.50–99) | 0.55 |
D-dimer | |||||||||
Baseline, ng/mL | 561 (237–1634) | 1489 (321–5199) | 0.01 | 534 (232–2307) | 672 (314–2165) | 0.46 | 918 (256–2228) | 519 (294–2332) | 0.74 |
Peak, ng/mL | 2345 (1618–3583) | 3653 (2774–8585) | 0.00 | 2620 (1901–377) | 2857 (1920–5230) | 0.36 | 2410 (1616–4032) | 3364 (2329–7281) | 0.04 |
Ferritin | |||||||||
Baseline, ng/mL | 764 (360–1392) | 612 (378–932) | 0.18 | 811 (482–1433) | 764 (391–1159) | 0.57 | 582 (254–1017) | 726 (471–1106) | 0.18 |
Peak, ng/mL | 1071 (551–2474) | 865 (419–1689) | 0.06 | 1057 (628–1760) | 1068 (496–2290) | 0.95 | 765 (348–2333) | 1162 (527–2179) | 0.16 |
Platelet count | |||||||||
Baseline, 103/µL | 205 (173–295) | 237 (175–312) | 0.26 | 255 (189–312) | 193 (156–289) | 0.04 | 236 (182–312) | 204 (151–277) | 0.18 |
Peak, 103/µL | 409 (312–512) | 363 (292–490) | 0.12 | 401 (314–516) | 373 (283–496) | 0.12 | 387 (303–503) | 373 (297–495) | 0.78 |
Lymphocyte counts | |||||||||
Baseline, % | 14.6 (9.7–20.2) | 11.0 (7.8–15.9) | 0.36 | 16.0 (9.4–23.6) | 12.50 (8.8–18.5) | 0.15 | 15.60 (8.63–20.50) | 11.70 (9.3–16.8) | 0.18 |
Peak *, % | 8.2 (4.7–13.4) | 6.07 (4.8–8.9) | 0.08 | 8.1 (5.3–15.2) | 6.23 (4.5–10.1) | 0.10 | 7.68 (5.06–14.15) | 6.52 (4.8–9.8) | 0.23 |
NLR | |||||||||
Baseline | 5.1 (3.5–8.4) | 7.2 (4.8–10.6) | 0.01 | 4.8 (2.9–8.8) | 9.2 (3.9–9.5) | 0.14 | 4.9 (3.4–9.7) | 6.9 (4.5–0.1) | 0.19 |
Peak | 10.7 (5.9–18.6) | 14.7 (9.8–18.9) | 0.07 | 10.7 (4.8–17.1) | 14.4 (8.0–20.8) | 0.12 | 11 (5.8–18.1) | 12.8 (8.0–19.3) | 0.27 |
RDW, % | |||||||||
Baseline | 12.3 (11.9–13.0) | 12.2 (11.9–12.9) | 0.57 | 12.1 (11.9–12.8) | 12.4 (12.0–13.2) | 0.14 | 12.2 (12.0–12.9) | 12.2 (11.8–12.7) | 0.53 |
Peak | 13.4 (12.5–16.3) | 13.0 (12.5–14.3) | 0.13 | 12.8 (12.2–13.4) | 13.6 (12.7–15.1) | 0.00 | 12.8 (12.4–13.4) | 13.4 (12.6–14.9) | 0.06 |
PDW, % | |||||||||
Baseline | 16.1 (15.7–16.7) | 16.7 (16.2–17.2) | 0.00 | 15.0 (15.8–16.9) | 16.2 (15.8–16.8) | 0.38 | 16.4 (15.9–16.8) | 16.5 (16.0–16.9) | 0.59 |
Peak | 17.1 (16.8–17.7) | 17.3 (17.0–18.0) | 0.09 | 17.2 (16.8–17.7) | 17.2 (16.9–17.7) | 0.50 | 17.2 (16.9–17.7) | 17.5 (17.0–17.8) | 0.21 |
IL-6, pg/mL peak | 66.0 (19.6–195.0) | 59.4 (27.0–89.4) | 0.59 | 59.0 (23.0–94.0) | 56.0 (19.0–23.5) | 0.45 | 42.0 (22.5–107.4) | 65.0 (25–235.0) | 0.24 |
IL-10, pg/mL peak | 10.0 (6.7–17.1) | 5.0 (3.3–10.1) | 0.00 | 7.0 (3.5–9.9) | 10.1 (4.8–17.1) | 0.02 | 7.7 (4.0–12.7) | 8.7 (4.7–13.1) | 0.75 |
NT-pro BNP, pg/mL peak | 205 (93–488.50) | 205 (110–630) | 0.69 | 166 (82–223) | 283 (114–687) | 0.02 | 172 (87–391) | 273 (106–581) | 0.23 |
hs Troponin I, ng/L peak | 8.1 (3.4–21.3) | 8.2 (4.2–18.7) | 0.63 | 5.2 (2.6–17.1) | 6.6 (4.1–21.6) | 0.27 | 5.3 (3.6–18.9) | 8.1 (4.0–52.4) | 0.52 |
Fibrinogen, mg/dL peak | 881 (725–109) | 864 (739–1033) | 0.71 | 880 (762–1019) | 899 (740–1040) | 0.8 | 826 (717–975) | 886 (728–1040) | 0.36 |
Non-PE (n = 85) | PE (n = 56) | p | DLCOc ≥ 80% (n = 36) | DLCOc < 80% (n = 76) | p | No PCRLA (n = 43) | PCRLA (n = 53) | p | |
---|---|---|---|---|---|---|---|---|---|
Plasminogen, ng/mL | 580.8 (412–804.5) | 535.3 (415.1–771) | 0.83 | 599 (459.3–915.6) | 525.1 (408.6–756.1) | 0.32 | 694.9 (525.1–2046.6) | 475.5 (239.3–617.3) | 0.00 |
Protein C, µg/mL | 13.9 (9.9–18.9) | 14.8 (11.3–19.5) | 0.88 | 13.9 (9.8–20.7) | 13.9 (9.7–18.6) | 0.60 | 13.8 (10.7–19) | 14 (9.5–16.9) | 0.77 |
P selectin, ng/mL | 67.5 (29.9–213.1) | 107.2 (40.3–230.9) | 0.22 | 107.2 (26.1–213.1) | 94 (32.9–213.1) | 0.54 | 111.5 (38.5–227.7) | 103.4 (32.8–213.1) | 0.42 |
Sphingosine 1 phosphate receptor-1, ng/mL | 2.1 (0.9–4.9) | 1.6 (0.7–3.3) | 0.06 | 4.15 (1.28–5) | 1.3 (0.80–3.6) | 0.04 | 2.34 (0.88–4.91) | 1.36 (0.79–4.6) | 0.11 |
VE-Cadherin, ng/mL | 427.3 (322.5–601) | 474.2 (322.8–648.6) | 0.63 | 473.2 (364.4–692.1) | 415.7 (304.5–578.2) | 0.15 | 544.6 (327.7–728.9) | 417 (288.7–551.7) | 0.05 |
Galectin, ng/mL | 175.7 (102.7–354.5) | 210.7 (141.7–346.8) | 0.30 | 168.5 (115.5–268.1) | 205.7 (103.5–358.3) | 0.53 | 204.4 (132.2–308.4) | 178.5 (77–335.7) | 0.32 |
Matrix metalloproteinase 7, ng/mL | 7.4 (5.4–10.6) | 6.3 (5.5–9.5) | 0.39 | 6.6 (5.7–9.5) | 6.5 (4.9–11) | 0.88 | 6.5 (5.7–9.7) | 7.2 (4.8–10.6) | 0.95 |
Surfactant protein D, ng/mL | 5.1 (0.7–17) | 5.9 (2.3–14) | 0.49 | 3.3 (0.5–8.1) | 8 (3.2–24.5) | 0.00 | 4.3 (0.4–11.46) | 6.4 (2.2–26.1) | 0.08 |
TNF-α, pg/mL | 12.7 (4–16.9) | 9.8 (5.7–16.2) | 0.60 | 11.7 (4.4–17.1) | 10.6 (5.4–16.7) | 0.99 | 9.8 (3.8–16) | 10.2 (5.7–16.2) | 0.73 |
TNF-α receptor-1, ng/mL | 1.8 (1.3–2.6) | 1.6 (1.3–2.2) | 0.47 | 1.5 (1.3–2.1) | 1.8 (1.3–2.9) | 0.31 | 1.5 (1.2–2) | 1.7 (1.2–2.7) | 0.22 |
TNF-α receptor-2, ng/mL | 16.2 (9.7–45.3) | 16.1 (9.6–28.8) | 0.35 | 11.4 (8.7–26.7) | 18.3 (11.1–42) | 09 | 11.6 (8.4–24.1) | 16.2 (11.5–28.9) | 0.06 |
IL-1-β, pg/mL | 1.6 (1–3.8) | 1.63 (0.97–2.79) | 0.52 | 1.4 (0.7–2.9) | 1.6 (1–3.1) | 0.2 | 1.2 (0.9–2.7) | 1.8 (1.2–4.3) | 0.02 |
CA15-3, U/mL | 19.8 (8.8–68) | 23.8 (10–81.4) | 0.58 | 13.7 (8.8–38.1) | 23.2 (10.5–97.1) | 0.08 | 21.7 (13.3–68.2) | 23.8 (9.9–88.2) | 0.94 |
Macrophage inflammatory protein 4-α, ng/mL | 8.8 (5.7–16.8) | 10.3 (7.2–16.1) | 0.46 | 9.4 (6.6–15.6) | 9.6 (6.5–17) | 0.94 | 12.1 (7.8–21.5) | 8.5 (6.5–14.5) | 0.05 |
Epidermal growth factor receptor, ng/mL | 48.2 (40.4–64.9) | 48.8 (40–61.7) | 0.97 | 47.4 (38.1–55.6) | 48.8 (39.1–62.4) | 0.67 | 49.5 (38.8–57.3) | 48.2 (40–61.9) | 0.69 |
Value | |
---|---|
Age > 65 yrs. | |
Yes | 3 |
No | 0 |
Minimum lymphocyte counts | |
≤6.7 × 103/µL | 1 |
>6.7 × 103/µL | 0 |
IL-1β | |
<1.2 pg/mL | 0 |
≥1.2 pg/mL | 2 |
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Suarez-Castillejo, C.; Calvo, N.; Preda, L.; Córdova Díaz, R.; Toledo-Pons, N.; Martínez, J.; Pons, J.; Vives-Borràs, M.; Pericàs, P.; Ramón, L.; et al. Cardiopulmonary Complications after Pulmonary Embolism in COVID-19. Int. J. Mol. Sci. 2024, 25, 7270. https://doi.org/10.3390/ijms25137270
Suarez-Castillejo C, Calvo N, Preda L, Córdova Díaz R, Toledo-Pons N, Martínez J, Pons J, Vives-Borràs M, Pericàs P, Ramón L, et al. Cardiopulmonary Complications after Pulmonary Embolism in COVID-19. International Journal of Molecular Sciences. 2024; 25(13):7270. https://doi.org/10.3390/ijms25137270
Chicago/Turabian StyleSuarez-Castillejo, Carla, Néstor Calvo, Luminita Preda, Rocío Córdova Díaz, Nuria Toledo-Pons, Joaquín Martínez, Jaume Pons, Miquel Vives-Borràs, Pere Pericàs, Luisa Ramón, and et al. 2024. "Cardiopulmonary Complications after Pulmonary Embolism in COVID-19" International Journal of Molecular Sciences 25, no. 13: 7270. https://doi.org/10.3390/ijms25137270