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Vol. 73. Issue 8.
Pages 680-682 (August 2020)
Scientific letter
DOI: 10.1016/j.rec.2020.05.010
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COVID-19 quarantine and acute pulmonary embolism
Embolia pulmonar aguda durante la cuarentena por COVID-19
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Luca Vanninia,
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luca.vannini84@gmail.com

Corresponding author:
, Juan Manuel Llanos Gómezb, Alejandro Quijada-Fumeroc, Ana Belén Fernández Pérezd, Julio S. Hernández Afonsoc
a Departamento de Medicina Preventiva y Salud Pública, Universidad Rey Juan Carlos, Madrid, Spain
b Servicio de Radiología, Hospital Nuestra Señora de Candelaria, Santa Cruz de Tenerife, Spain
c Servicio de Cardiología, Hospital Nuestra Señora de Candelaria, Santa Cruz de Tenerife, Spain
d Servicio de Anestesia, Hospital Nuestra Señora de Candelaria, Santa Cruz de Tenerife, Spain
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Tables (2)
Table 1. Characteristics of patients with acute pulmonary embolism lockdown subgroups (14 March to 18 April, 2020) vs the no-lockdown period (14 March to 18 April, 2019)
Table 2. Patients with acute pulmonary embolism during the COVID–19-related lockdown period (14 March to 18 Abril, 2020) and during the no-lockdown period (14 March to 18 Abril, 2019)
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To the Editor,

As the COVID-19 outbreak has increased worldwide, many countries have imposed lockdown restrictions to movement. Since 14 March 2020 in Spain, most people have been confined to home with an absolute ban on outdoor physical activity.

While the number of in-hospital positive COVID-19 patients was growing exponentially, there was a drastic decline in non–COVID-19 emergency patients with a drop of nearly 40% of ST-elevation myocardial infarction patients worldwide.1

Although the number of non–COVID-19 emergency patients decreased, there was an increase in the number of pulmonary embolisms (PE) in non–COVID-19 patients. In this scenario, the role of thromboprophylaxis is uncertain.2

From 14 March to 18 April 2020, in our center we diagnosed 17 acute PE with computed tomography pulmonary angiography. The number of PE cases clear increased compared with 2019 (average of 8 PE cases per month in 2019, with 9 cases from 14 March to 18 April, 2019). To examine whether there was a quarantine-related effect in the increased rate of acute PE, we compared the characteristics of acute PE patients by lockdown subgroups (ie, 14 March to 18 April, 2020) vs the no-lockdown period (ie, 14 March to 18 April, 2019) (table 1) in a single-center observational case series study.

Table 1.

Characteristics of patients with acute pulmonary embolism lockdown subgroups (14 March to 18 April, 2020) vs the no-lockdown period (14 March to 18 April, 2019)

  Lockdown groupN=17  No-lockdown groupN=P 
Female sex, %  52.9  66.7  .500 
Age, y  68 [56-81]  83 [75-87]  .012 
≥ 65 y, %  55.8  88.9  .114 
Hypertension, %  52.9  88.9  .067 
Diabetes mellitus, %  17.6  55.6  .046 
Hypercholesterolemia, %  29.4  100  .001 
Current smoker, %  23.5  33.3  .592 
BMI, kg/m2  25 [23-29]  29 [28-30]  .037 
Heart rate, bpm  97 [85-114]  99 [75-125]  .403 
Hemoptysis, %  11  .161 
D-dimer  4695 [2310-18 649]  15 059 [6800-19 000]  .307 
DVT signs or symptoms, %  29.4  55.6  .192 
Previous DVT, %  23.5  .114 
Surgery in previous 4 wk or immobilization at least 4 d, %  11.8  22.2  .161 
Active malignant condition, %  17.6  22.2  .778 
Mental disorders, %  35.3  44.4  .648 
PE risks factors*  3 [0.6-3]  4 [3-4]  .011 
Geneva score, points  6 [6-9]  11 [6-14]  .089 
Wells score, points  4.5 [3-6]  7.5 [4.5-7.5]  .159 
Padua score, points  3 [1-4]  2 [1-4]  .216 
Padua score for VTE including immobility as a risk factor in COVID–19-related lockdown group, points  5 [4-7]  2 [1-4]  .019 
Geneva risk for PE      .038 
Low (0-3 points), %  12   
Moderate (4-10 points), %  70  44   
High (> 10 points), %  18  56   
Wells risk for PE      .051 
Low (0-1 points), %   
Moderate (2-6 points), %  82  44   
High (> 6 points), %  18  56   
Padua score risk for VTE      .102 
Low (0-3 points), %  76.5  44.4   
High (≥ 4 points), %  23.5  55.6   
Padua score risk for VTE including immobility as a risk factor in the COVID–19-related lockdown group      .272 
Low (0-3 points), %  23.5  44.4   
High (≥ 4 points), %  76.5  55.6   

BMI, body mass Index; DVT, deep vein thrombosis; PE, pulmonary embolism; VTE, venous thromboembolism.

Data are expressed as No. (%), or median [interquartile range].

PE risks factors*: Strong risk factors: fracture of lower limb, hospitalization for heart failure or atrial fibrillation/flutter (within previous 3 months), hip or knee replacement, major trauma, myocardial infarction (within previous 3 months), previous VTE, spinal cord injury. Moderate risk factors: arthroscopic knee surgery, autoimmune diseases, blood transfusion, central venous lines, intravenous catheters and leads, chemotherapy, congestive heart failure or respiratory failure, erythropoiesis-stimulating agents, hormone replacement therapy, in vitro fertilization, oral contraceptive therapy, postpartum period, infection (specifically pneumonia, urinary tract infection, and human immunodeficiency virus, inflammatory bowel disease, cancer (highest risk in metastatic disease), paralytic stroke, superficial vein thrombosis, and thrombophilia. Weak risk factors: bed rest> 3 days, diabetes mellitus, hypertension, immobility due to sitting, increasing age, laparoscopic surgery, obesity, pregnancy, and varicose veins.

Comparison between categorical data was performed using the chi-square test or the McNemar test for paired data and the Mann-Whitney U-test for ordinal and continuous variables. Statistical analysis was performed with SPSS version 21 (SPSS Inc, Chicago, IL) and a value of P <.05 was considered the threshold for statistical significance.

Patients in the PE lockdown period were younger (median age, 68 years; interquartile range [IQR][56-81] versus 83 [75-87] years; P=.012), with a lower prevalence of diabetes mellitus (17.6% vs 55.6%; P=.046), hypercholesterolemia (29.4% vs 100%; P=.001), and lower body mass index) (median body mass index=25 [23-29] vs 29 [28-30]; P=.037).

There were numerous environmental and patient-related predisposing venous thromboembolism (VTE) risk factors that we summarize in table 1, as described in the European Society of Cardiology guidelines for acute PE.3

Patients in the COVID–19-related lockdown period had a lower number of PE risk factors (median PE risk factors, 3 [0.6-3] vs 4 [3-4]; P=.011) (table 1). COVID–19-related lockdown patients also had a significantly lower PE risk when assessed with the Wells and Geneva risk scores as categorical (low, moderate, and high risk) variables.

Sixteen patients had VTE risk factors added to prolonged immobility due to quarantine; 11 patients had moderate or strong risk factors for PE (table 2). Only 1 patient with chronic lymphocytic leukemia had a positive nasal-pharyngeal swab sample polymerase chain reaction (PCR) for COVID-19 at diagnosis. One patient, who had previous COVID-19 severe pneumonia and negative nasal-pharyngeal swab sample at discharge, developed acute PE 1 week later.

Table 2.

Patients with acute pulmonary embolism during the COVID–19-related lockdown period (14 March to 18 Abril, 2020) and during the no-lockdown period (14 March to 18 Abril, 2019)

Year  Sex  Age  BMI  Smoker  HTA  Hypercholesterolemia  Diabetes  Mental disorder  PE risk factors  COVID-19  d-dimer  RV dysfunction  DVTDoppler US  DVTSigns/symptoms  Death 
2019  Female  73  34  Yes  Yes  No  No  No  -Active lung cancer-Obesity  Yes  Yes  Yes 
2019  Female  87  29  No  Yes  Yes  Yes  Anxiety  -Reduced mobility-Overweight  17 051  No  Yes  Yes  No 
2019  Male  44  28  No  Yes  Yes  Yes  No  -Rheumatoid arthritis under treatment-Overweight  7485  No  Yes  Yes  No 
2019  Female  86  29  No  Yes  Yes  No  No  -Overweight-Advanced age  15 059  No  Yes  Yes  No 
2019  Male  87  30  Former smoker  Yes  Yes  No  No  -Vertebral fracture-Obesity  1474  No  No  Yes 
2019  Female  84  31  Yes  Yes  Yes  Yes  No  -Hip fracture-Obesity  Yes    No 
2019  Female  75  32  Yes  Yes  Yes  Yes  ParkinsonAnxiety  - Obesity  6800  No  No  No  No 
2019  Male  76  30  No  No  Yes  Yes  Bipolar disorder  -No active colorectal cancer-Obesity  19 000  Yes  Yes  No  No 
2019  Female  83  25  No  Yes  Yes  No  Psychotic disorderDementia  - Active colorectal cancer  71 649  No  Yes  No 
2020  Male  56  32  No  Yes  Yes  No  Anxiety  -DVT under LMWH treatment-Obesity  No  1117  No  Yes  Yes  No 
2020  Female  69  24  Yes  No  No  No  No  -Previous PE with DVT  No  2800  No  Yes  Yes  No 
2020  Female  43  23  No  No  No  No  No  -Oral contraceptive  No  4695  No  No  No  No 
2020  Female  34  25  No  No  No  No  Psychotic disorders  -Psychotic attack-Bedridden-Obesity  No  63 409  Yes  No  No  No 
2020  Male  56  33  No  No  No  No  No  -Previous DVT-Obesity  No  2639  No  Yes  Yes  No 
2020  Male  62  17  Yes  No  No  No  No  -Orchiepididymitis-Bedridden  No  Yes  No  No  No 
2020  Male  83  21  Former smoker  No  No  No  No  -Advanced age  No  18 649  Yes  No  No 
2020  Female  56  23  Yes  No  Yes  No  Psychotic disorders  No  No  27 361  No  Yes  No  No 
2020  Male  81  28  No    No  Yes  No  -Chronic lymphocytic leukemia  Positive  6057  No  No  No 
2020  Female  70  29  No  Yes  No  No  Depression  -Overweight  No  3685  No  No  No  No 
2020  Female  68  30  No  Yes  No  Yes  No  -Active breast cancer-Obesity  No  2006  No  No  No 
2020  Male  67  28  No  Yes  No  No  No  -Previous PE with DVT  No  15 252  Yes  No  No  No 
2020  Male  85  29  No  Yes  No  No  No  -Advanced age-Overweight  No  2310  Yes  No  No  Yes 
2020  Female  70  17  No  Yes  Yes  No  No  -Ventricular dysfunction with heart failure  No  800  Yes  No  No  No 
2020  Female  83  23  No  Yes  Yes  Yes  Dementia  -COVID-19 infection discharged with negative PCR-Advanced age  Discharged for COVID-19 infection 1 week before  13 340  No  No  No 
2020  Female  71  32  No  No  Yes  No  Parkinson's - Dementia  -Parkinson's Dementia disease-Obesity  No  Yes  No  No 
2020  Male  65  25  Yes  Yes  No  No  No  Active pancreatic cancer under LMWH treatment  No  137 741  No  No  No 

BMI, body mass index; DVT, deep vein thrombosis; LMWH, low molecular weight heparin; PCR, polymerase chain reaction; PE, pulmonary embolism; PHT, pulmonary hypertension; RV dysfunction, right ventricular dysfunction.

When asked about previous daily activity, most patients reported a previously active lifestyle followed by a sedentary lifestyle during the quarantine with prolonged immobility.

Six patients had mental disorders that could worsen immobility during the quarantine and predispose them to PE,4 but we found no significant difference between the groups corresponding to the COVID-19-related lockdown period and the non–COVID-19 period in the prevalence of mental disorders (35.3% vs 44.4%; P=.648).

In an attempt to explain that immobility due to the hard lockdown could be one of the triggers for PE, we calculated the Padua score, which stratifies patients as being at high (≥ 4 points) or low (< 4 points) risk for VTE. We considered the hard lockdown quarantine as a “reduced mobility” risk factor; immobility in this score is penalized with 3 points. There was no significant difference in the baseline Padua prediction score for VTE (median Padua score, 3 [1-4] vs 2 [1-4]; P=.216). The COVID–19-related lockdown group had a significantly higher score in the subanalysis including immobility as a risk factor during the lockdown (median Padua score, 5 [4-7] vs 2 [1-4]; P=.019). We found a significant increase in high-risk patients in the lockdown subgroup considering lockdown as immobility (Padua score without immobility: 23.5% patients at high risk, Padua score with immobility: 76.5% patients at high risk; P=.004). When we compared the Padua score as a categorical risk variable, we found no significant difference between the lockdown period group and the no-lockdown group.

We hypothesized that a rigorous quarantine in patients with strong risk factors could predispose them to acute PE. Immobility causes an 6-fold increase in the risk of deep vein thrombosis (or PE in patients with previous events compared with patients without deep vein thrombosis or PE history).5

The increasing number of COVID–19-related acute PE cases described recently suggests that COVID-19 infection could be an added risk factor for acute PE during quarantine. In our series, the low prevalence of COVID-19 infection on nasal smear PCR tests does not suggest a causative relationship. A single effect, either of quarantine immobility or undiagnosed COVID-19 infection, cannot be excluded and would require a large study including COVID-19 serology-based testing with high sensitivity and specificity.

In the emergency department, elevated D-dimer with dyspnea in COVID-19 quarantine patients might be misleading. Clinicians should pay attention to a possible PE in the setting of a COVID-19 infection.

In nations imposing a hard lockdown, all patients with VTE risk factors might be counseled for mechanical prophylaxis and to stay active at home. Pharmacological prophylaxis could be advised in patients at high risk, especially previous VTE and active malignancy, which must be weighed against the risk of bleeding.

.

References
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O. Rodríguez-Leor, B. Cid-Álvarez, S. Ojeda, et al.
Impacto de la pandemia de COVID-19 sobre la actividad asistencial en cardiología intervencionista en España.
REC Interv Cardiol., 2 (2020), pp. 82-89
[2]
COVID-19 and Thrombotic or Thromboembolic Disease: Implications for Prevention, Antithrombotic Therapy, and Follow-up | JACC: Journal of the American College of Cardiology. Available at: http://www.onlinejacc.org/content/early/2020/04/15/j.jacc.2020.04.031?_ga=2.84405337.1380747230.1587329638-1120860459.1559245908. Accessed 19 Apr 2020.
[3]
S.V. Konstantinides, G. Meyer, C. Becattini, ESC Scientific Document Group.2019 ESC Guidelines for the diagnosis and management of acute pulmonary embolism developed in collaboration with the European Respiratory Society (ERS), et al.
Eur Heart J., 41 (2020), pp. 543-603
[4]
L. Parkin, A. Balkwill, S. Sweetland, et al.
Antidepressants, Depression, and Venous Thromboembolism Risk: Large Prospective Study of UK Women.
[5]
M.-M. Samama.
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Arch Intern Med., 160 (2000), pp. 3415-3420
Copyright © 2020. Sociedad Española de Cardiología
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