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Original Article

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Blood Res 2021; 56(4):

Published online December 31, 2021

https://doi.org/10.5045/br.2021.2021131

© The Korean Society of Hematology

The demographic, clinical, and medical manifestations of pulmonary thromboembolism development in COVID-19

Somayeh Sadeghi1,2, Maryam Nasirian1,3, Elaheh Keivany4,5, Peiman Nasri6,7, Maryam Sadat Mirenayat8

Author Info. +

1Infectious Diseases and Tropical Medicine Research Center, Isfahan University of Medical Sciences, 2Acquired Immunodeficiency Research Center, Al-Zahra Hospital, Isfahan University of Medical Sciences, 3Epidemiology and Biostatistics Department, Health School, Isfahan University of Medical Sciences, 4Department of Internal Medicine, School of Medicine, Isfahan University of Medical Sciences, 5Department of Pulmonology, Isfahan University of Medical Sciences, 6Metabolic Liver Disease Research Center, Isfahan University of Medical Sciences, 7Child Growth and Development Research Center, Research Institute for Primordial Prevention of Non-Communicable Disease, Isfahan University of Medical Sciences, Isfahan, 8Chronic Respiratory Diseases Research Center, National Research Institute of Tuberculosis and Lung Diseases, Shahid Beheshti University of Medical Sciences, Tehran, Iran

Correspondence to : Maryam Sadat Mirenayat, M.D.
ChronicRespiratory Diseases Research Center, National Research Institute of Tuberculosis and Lung Diseases, Shahid Beheshti University of Medical Sciences, Tehran 19839-63113, Iran
E-mail: mirenayat_m@yahoo.com

*This study was supported by Isfahan University of Medical Sciences.

Received: July 27, 2021; Revised: October 5, 2021; Accepted: November 4, 2021

This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

Abstract

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Background
Since the emergence of coronavirus disease 2019 (COVID-19), various clinical manifestations ranging from asymptomatic to severe, life-threatening courses have been presented. It is well known that COVID-19 patients are at an increased risk of pulmonary thromboembolism (PTE) development; however, the associated demographic, medical, and clinical factors for developing PTE remain unknown. The current study aimed to assess the characteristics of patients with PTE.
Methods
This case-control study was derived from an ongoing population-based investigation of hospitalized patients with COVID-19 pneumonia. The case group included 99 patients with PTE confirmed by computed tomography pulmonary angiography (CTPA), and the controls (N=132) were age-matched patients selected from the PTE-suspected patients with a negative CTPA. The demographic, medical, and clinical characteristics of the study population were entered into the study checklist and compared. A logistic regression test was used to determine the factors associated with PTE development.
Results
Among the 13,099 admitted patients, 690 (5.26%) were suspected of having PTE according to their clinical manifestations. CTPA was performed for suspected cases, and PTE was confirmed in 132 patients (19.13%). Logistic regression assessments revealed that male gender (OR, 2.39; 95%CI, 1.38‒4.13), decreased oxygen saturation (OR, 2.33; 95%CI, 1.27‒4.26), and lower hemoglobin (OR, 0.83, 0.95), and albumin (OR, 0.31; 95%CI, 0.18‒0.53) levels were associated with PTE development.
Conclusion
PTE was confirmed in one-fifth of suspected patients who underwent CTPA imaging. Male sex, decreased oxygen saturation, and lower levels of hemoglobin and albumin were independent predictors of PTE in patients with COVID-19 pneumonia.

Keywords COVID-19, Pulmonary embolism, Computed tomography angiography, Coronavirus

Article

Original Article

Blood Res 2021; 56(4): 293-300

Published online December 31, 2021 https://doi.org/10.5045/br.2021.2021131

Copyright © The Korean Society of Hematology.

The demographic, clinical, and medical manifestations of pulmonary thromboembolism development in COVID-19

Somayeh Sadeghi1,2, Maryam Nasirian1,3, Elaheh Keivany4,5, Peiman Nasri6,7, Maryam Sadat Mirenayat8

1Infectious Diseases and Tropical Medicine Research Center, Isfahan University of Medical Sciences, 2Acquired Immunodeficiency Research Center, Al-Zahra Hospital, Isfahan University of Medical Sciences, 3Epidemiology and Biostatistics Department, Health School, Isfahan University of Medical Sciences, 4Department of Internal Medicine, School of Medicine, Isfahan University of Medical Sciences, 5Department of Pulmonology, Isfahan University of Medical Sciences, 6Metabolic Liver Disease Research Center, Isfahan University of Medical Sciences, 7Child Growth and Development Research Center, Research Institute for Primordial Prevention of Non-Communicable Disease, Isfahan University of Medical Sciences, Isfahan, 8Chronic Respiratory Diseases Research Center, National Research Institute of Tuberculosis and Lung Diseases, Shahid Beheshti University of Medical Sciences, Tehran, Iran

Correspondence to:Maryam Sadat Mirenayat, M.D.
ChronicRespiratory Diseases Research Center, National Research Institute of Tuberculosis and Lung Diseases, Shahid Beheshti University of Medical Sciences, Tehran 19839-63113, Iran
E-mail: mirenayat_m@yahoo.com

*This study was supported by Isfahan University of Medical Sciences.

Received: July 27, 2021; Revised: October 5, 2021; Accepted: November 4, 2021

This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

Abstract

Background
Since the emergence of coronavirus disease 2019 (COVID-19), various clinical manifestations ranging from asymptomatic to severe, life-threatening courses have been presented. It is well known that COVID-19 patients are at an increased risk of pulmonary thromboembolism (PTE) development; however, the associated demographic, medical, and clinical factors for developing PTE remain unknown. The current study aimed to assess the characteristics of patients with PTE.
Methods
This case-control study was derived from an ongoing population-based investigation of hospitalized patients with COVID-19 pneumonia. The case group included 99 patients with PTE confirmed by computed tomography pulmonary angiography (CTPA), and the controls (N=132) were age-matched patients selected from the PTE-suspected patients with a negative CTPA. The demographic, medical, and clinical characteristics of the study population were entered into the study checklist and compared. A logistic regression test was used to determine the factors associated with PTE development.
Results
Among the 13,099 admitted patients, 690 (5.26%) were suspected of having PTE according to their clinical manifestations. CTPA was performed for suspected cases, and PTE was confirmed in 132 patients (19.13%). Logistic regression assessments revealed that male gender (OR, 2.39; 95%CI, 1.38‒4.13), decreased oxygen saturation (OR, 2.33; 95%CI, 1.27‒4.26), and lower hemoglobin (OR, 0.83, 0.95), and albumin (OR, 0.31; 95%CI, 0.18‒0.53) levels were associated with PTE development.
Conclusion
PTE was confirmed in one-fifth of suspected patients who underwent CTPA imaging. Male sex, decreased oxygen saturation, and lower levels of hemoglobin and albumin were independent predictors of PTE in patients with COVID-19 pneumonia.

Keywords: COVID-19, Pulmonary embolism, Computed tomography angiography, Coronavirus

Table 1 . Demographic, clinical, and laboratory characteristics of the studied population..

No PTE (N=132)PTE (N=99)P
Age (yr), mean (SD)58.0 (17.9)59.0 (17.6)0.665
Gender-male, N (%)63 (47.7)68 (68.7)0.001a)
Comorbidities, N (%)
Diabetes mellitus22 (16.7)19 (19.2)0.619
Chronic obstructive pulmonary disease 8 (6.1) 2 (2.0)0.135
End-stage renal disease 0 (0) 3 (3.0)-
Malignancy 3 (3.0) 3 (3.0)1.000
Cerebrovascular accident 7 (5.3) 6 (6.1)0.805
Ischemic heart disease15 (11.4)20 (20.2)0.064
Previous history of pulmonary thromboembolism 1 (0.76) 1 (1.0)0.838
Having the least of one comorbidity48 (36.4)38 (38.4)0.753
Current smoking, N (%)10 (7.6)12 (12.1)0.244
History of medications, N/N (%)
None31/103 (30.1)66/94 (70.2)<0.0001a)
Aspirin13/102 (12.8)20/94 (21.3)0.111
Clopidogrel0/131 (0)1/99 (1.0)0.249
Anticoagulant prophylaxis2/132 (1.52)3/99 (3.0)0.434
Therapeutic anticoagulant0/132 (0)2/99 (2.0)0.156
On admission clinical presentations
Systolic blood pressure, mean (SD)127.1 (23.6)124.1 (17.8)0.297
Systolic blood pressure <90 mmHg, N (%) 3 (2.3) 1 (1.0)0.637
Diastolic blood pressure, mean (SD)77.8 (15.8)78.8 (13.1)0.624
Diastolic blood pressure <60 mmHg, N (%) 3 (2.3) 1 (1.0)0.637
Pulse rate per minute, mean (SD)92.3 (18.6)94.7 (18.0)0.332
Pulse rate >100 per minute, N (%)33 (25.0)33 (33.3)0.165
Respiratory rate per minute-mean (SD)24.5 (6.4)24.6 (5.7)0.838
Respiratory rate >30 per minute, N (%)15 (11.4)13 (13.1)0.684
O2 saturation (%), mean (SD)86.1 (8.2)81.8 (10.9)0.001a)
O2 saturation t <90%, N (%)83 (62.9)79 (79.8)0.005a)
O2 saturation 90–93%, N(%)25 (18.9) 9 (9.1)0.037a)
O2 saturation >93%, N(%)24 (18.2)11 (11.1)0.138
Clinical presentations three days before CT-scan, N (%)
Relative bed rest75 (56.8)34 (40.5)0.019a)
Complete bed rest77 (58.3)63 (75.0)0.012a)
On admission laboratory characteristics, mean (SD)
Neutrophil count (per mL)6,042 (4,100)7,851 (4,016)0.001a)
Lymphocyte count (per mL)1,239 (1,015)1,048 (1,016)0.161
Platelet ×103 (per mL)193.9 (95.7)216.3 (94.4)0.905
Neutrophil-to-lymphocyte ratio6.9 (6.9)10.3 (8.1)0.001a)
International normalized ratio1.23 (0.56)1.27 (0.43)0.544
Hemoglobin (mg/dL)13.3 (1.9)12.6 (2.3)0.006a)
Ferritin (μg/L)814.7 (582.5)817.2 (554.7)0.978
Fibrinogen degradation products (μg/mL)25.8 (8.9)26.2 (5.8)0.871
Fibrinogen (mg/dL)331.7 (111.4)278.3(106.5)0.040a)
Prothrombin time (s)13.8 (5.5)14.1 (4.4)0.721
Partial thromboplastin time (s)37.2 (15.7)32.4 (8.2)0.010a)
Albumin (g/dL)3.64 (0.63)3.25 (0.52)<0.0001a)
Troponin (ng/mL)68.2 (232.8)230.0 (495.1)0.019a)
D-dimer (μg/mL)2,869 (3,285)4,775 (3,641)0.001a)
C-reactive protein (mg/L)67.6 (46.3)85.2 (45.4)0.006a)
Lactate dehydrogenase (IU/L)794.2 (385.1)1,016.6 (527.4)0.001a)
Maximum laboratory characteristics-Median (IQR)
D-dimer (μg/mL)1,971 (817–4,732)3,550 (2,259–8,191)<0.0001a)
C-reactive protein (mg/L)77 (54–111)98 (60–125)0.034a)
Lactate dehydrogenase (IU/L)803 (629–1,215)1,020 (683–1,380)0.017a)
Maximum increase compared to admission time, mean (min–max)
D-dimer (μg/mL)575.9 (0–8,909)359.7 (0–9,363)0.050
C-reactive protein (mg/L)11.0 (0–102)5.0 (0–86)0.032a)
Lactate dehydrogenase (IU/L)188.6 (0–2,242)114.3 (0–2,644)0.206

a)Chi2/exact test for categorical variable, independent T-test or Wilcoxon rank-sum test for continuous variable were significant if P-value <0.05..

Abbreviation: PTE, pulmonary thromboembolism..

Table 2 . Hospital-related characteristics of the studied population..

No PTEPTEP
Prescribed DrugsN=131N=84-
Hydroxychloroquine61 (46.6)20 (23.8)0.001a)
Antibiotic118 (9.1)74 (88.1)0.647
Remdesivir23 (17.6)14 (16.7)0.866
Interferon18 (13.8)4 (4.8)0.034a)
Favipiravir2 (1.53)1 (1.20)0.845
Corticosteroid87 (66.4)68 (81.0)0.020a)
Kaletra13 (9.1)7 (8.3)0.695
Unknown1 (0.75)15 (15.1)
Anticoagulation prior to PTE diagnosis, N (%)N=130N=84-
None34 (26.2)38 (45.2)0.004a)
Prophylactic doses71 (54.6)27 (32.1)0.001a)
Intermediate doses6 (4.6)8 (9.5)0.156
Therapeutic doses19 (14.6)11 (13.1)0.754
Unknown2 (1.5)15 (15.1)
Side effects of anticoagulants, N (%)N=132N=84-
GI-bleeding6 (4.6)6/84 (7.2)0.389
Hemoptysis8 (6.1)5/84 (6.0)0.0001a)
Hematuria2 (1.5)3/84 (3.6)0.327
Other2 (1.5)3/84 (3.6)0.327
Missing0 (0)15 (15.1)
Disease severitya), N (%)13 (9.9)10 (10.1)0.949
Hospitalization outcome, N (%)N=132N=99-
Intensive care unit admission59 (44.7)47 (47.5)0.675
Non-invasive ventilation12 (9.1)25 (25.3)0.001a)
Intubation18 (13.6)19 (19.2)0.255
Discharge124 (93.9)81 (81.8)0.004a)
Death8 (6.1)18 (18.2)
Interval times-day, median (IQR)N=132N=99-
Symptom to admission7 (4–10)7 (4–14)0.467
Symptom to computed tomography, scan13 (7–17)14 (6–20)0.841
Admission to computed tomography, scan2 (0–7)4 (3–8)0.607
Admission to intensive care unit2 (0–5)3 (1–6)0.247
Admission to discharged9 (5–14)10 (7–19)0.033a)
Admission to dead13 (12–21)8 (13.5–30)0.837

a)Chi2/exact test for categorical variable, independent T-test or Wilcoxon rank-sum test for continuous variable were significant if P-value <0.05 and severity considered as O2 sat <90 and respiratory rate >30..

Abbreviation: PTE, pulmonary thromboembolism..

Table 3 . The effect of PTE on hospitalization outcomes..

ICU admissionNIVIntubationDeadTime from admission to
DischargeDeath
OR/exp(Beta)a)(95% CI)Crude1.11
(0.66–1.88)		3.37
(1.60–7.12)b)		1.50
(0.74–3.04)		3.44
(1.43–8.20)b)		9.42
(0.36–245)		8.73
(0.002– 302)
Adjustedb)1.09
(0.64–1.86)		3.40
(1.59–7.25)b)		1.48
(0.73–3.02)		3.41
(1.41–8.28)b)		4.25
(0.001–271.9)		9.86
(0.39–249.3)

a)Binary logistic regression was used to estimate crude and adjusted odds ratio for categorical variables, and linear logistic regression was used to estimate crude and adjusted exponential beta for time to death and discharge. b)Adjusted for severity, age, have at least one underlying disease. P-value <0.05..

Abbreviations: CI, confidence interval; ICU, intensive care unit; NIV, non-invasive ventilation; OR, odds ratio..

Table 4 . Logistic regression analysis of factors associated with PTE..

OR (95% CI)c)
CrudeAdjustedb)
Age1.00 (0.98–1.01)-
Gender-male2.40 (1.39–4.14)d)2.39 (1.38–4.13)d)
On admission clinical presentations
O2 saturation percentage0.95 (0.92–0.98)d)-
O2 saturation <93%2.33 (1.27–4.26)d)-
Hemoglobin0.83 (0.73–0.95)d)0.83 (0.73–0.95)d)
Fibrinogen0.99 (0.98–0.99)d)0.99 (0.99–1.00)
Albumin0.32 (0.18–0.53)d)0.31 (0.18–0.55)d)
NLR1.07 (1.02–1.11)d)1.07 (1.02–1.12)
Troponin1.00 (1.00–1.00)d)1.01 (1.00–1.01)d)
D-dimer1.00 (1.00–1.00)d)1.00 (1.00–1.00)d)
CRP1.00 (1.00–1.01)d)1.00 (1.00–1.01)d)
LDH1.00 (1.00–1.00)d)1.00 (1.00–1.00)d)
Maximum laboratory characteristics
D-dimer1.00 (1.00–1.00)d)1.00 (1.00–1.00)d)
CRP1.01 (0.99–1.01)1.01 (0.99–1.01)
LDH1.00 (0.99–1.00)1.00 (0.99–1.00)
Maximum increase compared to admission time
D-dimer0.99 (0.99–1.00)0.99 (0.99–1.00)
CRP0.98 (0.96–0.99)d)0.98 (0.96–0.99)d)
LDH0.99 (0.99–1.00)0.99 (0.99–1.00)
Disease severitya)1.03 (0.43–2.5)-
At least have one underlying disease1.09 (0.63–1.86)1.05 (0.61–1.85)
Hemoptysis0.98 (0.30–3.10)1.01 (0.30–3.34)

a)Disease severity defined as O2 sat<90, respiratory rate>30. b)Adjusted by age and severity. c)Binary logistic regression was used to estimate crude and adjusted odds ratio. d)P-value <0.05..

Abbreviations: CRP, C reactive protein; LDH, lactate dehydrogenase; NLR, neutrophil lymphocyte ratio..
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