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 Table of Contents  
INTERESTING CASE REPORT
Year : 2021  |  Volume : 5  |  Issue : 2  |  Page : 177-180

Extensive Pulmonary Thromboembolism and Serious Threat of Systemic Thromboembolism in a Suspected COVID Recovered Patient


Department of Pediatric Cardiology, Madras Medical Mission, Chennai, Tamil Nadu, India

Date of Submission24-May-2021
Date of Acceptance13-Jun-2021
Date of Web Publication19-Aug-2021

Correspondence Address:
Dr. Kothandam Sivakumar
Department of Pediatric Cardiology, Institute of Cardio Vascular Diseases, Madras Medical Mission, 4A, Dr. J J Nagar, Mogappair, Chennai - 600 037, Tamil Nadu
India
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/jiae.jiae_19_21

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  Abstract 

Hemodynamically significant large pulmonary embolism causes right ventricular dysfunction that stretches open the foramen ovale in the atrial septum. Paradoxical embolism is common in patients with right ventricular dysfunction. While anticoagulation and thrombolysis are considered the treatment of choice in pulmonary embolism, a large thrombus in transit across the patent foramen ovale carries a serious risk of systemic thromboembolism and warrants urgent surgery. The recent coronavirus disease 2019 (COVID-19) pandemic has led to a significant increase in the incidence of thromboembolic illnesses. A patient acutely presented with deep vein thrombosis, pulmonary embolism, large thrombus in transit across the foramen ovale along with elevation of multiple inflammatory biomarkers that were suggestive of a possible post-COVID sequelae. Images and management strategies are discussed in this report.

Keywords: Acute pulmonary embolism, COVID infection, paradoxical embolism, patent foramen ovale, thrombus in transit


How to cite this article:
Sagar P, Sheriff EA, Sivakumar K. Extensive Pulmonary Thromboembolism and Serious Threat of Systemic Thromboembolism in a Suspected COVID Recovered Patient. J Indian Acad Echocardiogr Cardiovasc Imaging 2021;5:177-80

How to cite this URL:
Sagar P, Sheriff EA, Sivakumar K. Extensive Pulmonary Thromboembolism and Serious Threat of Systemic Thromboembolism in a Suspected COVID Recovered Patient. J Indian Acad Echocardiogr Cardiovasc Imaging [serial online] 2021 [cited 2021 Dec 5];5:177-80. Available from: https://www.jiaecho.org/text.asp?2021/5/2/177/324095


  Introduction Top


Paradoxical embolism through a patent foramen ovale (PFO) is sometimes documented on echocardiogram as a thrombus in transit from the right heart.[1] Patients with pulmonary thromboembolism are predisposed to develop paradoxical embolism as the resultant elevated right atrial pressure forces open a PFO.[2],[3] Patients with intermediate or high-risk pulmonary embolism and right ventricular (RV) dysfunction develop paradoxical embolism more often than those without RV dysfunction.[4] The recent pandemic of coronavirus disease 2019 (COVID-19) infection has led to increased risk of thromboembolic events warranting different anticoagulation strategies.[5] Echocardiography and advanced imaging in a patient treated for deep-vein thrombosis and pulmonary embolism demonstrated a large thrombus in transit through a PFO. The blood investigations were suggestive of a sequel of a recovering COVID-19 infection, but reverse transcription-polymerase chain reaction (RT-PCR) was negative. This report details the clinical presentation, imaging, and management strategy.


  Case Report Top


A 52-year-old female, obese with a body mass index of 40.1 kg/m2, diabetic and hypertensive for 6 years, with no prior history of thrombosis presented with complaints of swelling of the left leg for 1 week followed by shortness of breath, New York Heart Association Class III to IV for 3 days. There was no history of chest pain, cough, and palpitation. She was evaluated elsewhere by computerized tomography pulmonary angiogram and diagnosed to have pulmonary thromboembolism involving proximal right and left pulmonary artery. Venous Doppler of lower limb showed deep-vein thrombosis involving left femoral vein and tibial veins. She had no preceding febrile illnesses and so was not tested for COVID-19 infection during her initial presentation. She was managed by thrombolysis with intravenous reteplase 5 days after symptom onset at the primary hospital and referred to us for further management. Although there was no hypotension, transthoracic echocardiography showed RV systolic dysfunction and a mobile intracardiac mass in both right and left atrium. Cardiac magnetic resonance imaging showed a thrombus in transit, straddling the PFO [Video 1] [Additional file 1] and [Figure 1]. There was no evidence of overt clinical systemic thromboembolism.
Figure 1: Cardiac magnetic resonance imaging in systolic frame (a) and diastolic frame (b) shows a large thrombus (arrow) in transit across the patent foramen ovale straddling across the atrioventricular valves

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Video 1: Cardiac magnetic resonance imaging shows a fourchamber view demonstrating a large thrombus in transit across the patent oval foramen extending into both the atrium.

During the admission in our hospital, screening for COVID-19 infection with a RT-PCR was negative. On initial evaluation, she was hemodynamically stable with a pulse rate of 86/min and blood pressure of 112/74 mm Hg. Echocardiography confirmed the presence of thrombus straddling the PFO and RV systolic dysfunction. Transesophageal echocardiography showed a large mobile thrombus in transit straddling the PFO moving in and out of the atrioventricular valves during the cardiac cycle [Video 2] [Additional file 2] and [Figure 2]. A second computed tomographic pulmonary angiogram to study the response to thrombolysis showed persistence of thrombus in proximal right and left pulmonary artery as well as extension into the segmental and subsegmental arteries [Figure 3]. Blood investigations showed elevated inflammatory markers including ferritin levels of 590 ng/mL, C-reactive protein 33.2 mg/dL, interleukin-6 19.96 pg/mL. Evaluation for connective tissue disorders associated with thrombosis, like systemic lupus erythematosus, anti-neutrophilic cytoplasmic antibody-associated vasculitis, Bechet's disease, antiphospholipid antibody syndrome were done by the autoimmune panel and was negative. Other hypercoagulable states including underlying malignancy were evaluated by computed tomography of neck, chest, abdomen pelvis, and tumor markers which were negative. Evaluation for protein C, protein S, antithrombin deficiency, factor V Leiden mutation was negative. In view of persistent elevation of inflammatory markers beyond 1–2 weeks of the onset of the deep vein thrombosis and absence of other immediate predisposing factors, it was assumed to be secondary to RT-PCR negative COVID-19 infection in the setting of the pandemic.
Figure 2: Transesophageal echocardiography in multiple planes (a-d) shows a very large thrombus (white arrow), advancing through the foramen ovale (black arrow) into the left atrium (LA) from the right atrium (RA)

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Figure 3: Computed tomographic pulmonary angiogram shows a large pulmonary embolus at the bifurcation of the pulmonary trunk (a), and in the hilar right and left pulmonary arteries (b) extending to lobar (c) and segmental (d) branches

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Video 2: Transesophageal echocardiogram demonstrating a large thrombus in transit across the patent foramen ovale with impending threat of a large pulmonary or systemic embolism.

In view of significant thrombus burden in both the proximal pulmonary artery and more importantly a large straddling thrombus across the patent foramen ovale, an urgent decision for early surgical exploration, pulmonary thrombectomy, removal of intracardiac thrombus, and closure of PFO was made. Antibody testing for COVID-19 was not done before this emergent surgery. After a median sternotomy, the right atrium was opened after establishing cardiopulmonary bypass and the right atrial side of the thrombus was visualized. An incision was made in the interatrial septum and the whole thrombus was removed in toto. The pulmonary artery was opened to remove thrombus from both hilar pulmonary arteries. A retrograde saline injection into all the pulmonary veins was done to flush out all the recent thrombus from the pulmonary artery.

Postoperative recovery was uneventful and she was started on early anticoagulation after the surgery. Even though a thrombophilia workup did not reveal any significant abnormality and a possible COVID-19 related thrombosis, she was advised oral anticoagulation with warfarin considering the very large thrombus burden. Implantation of a filter in the inferior vena cava was not considered in the absence of recurrence of thrombosis on warfarin. At 6-month follow-up, she was asymptomatic with no echocardiographic evidence of RV dysfunction and pulmonary arterial hypertension.


  Discussion Top


Thrombus in transit straddling the PFO is sometimes documented in patients with pulmonary embolism.[1],[6] When it is diagnosed, it triggers immediate alarm in view of impending catastrophic systemic embolism.[7] About 40% of patients documented to have a thrombus in transit are associated with paradoxical systemic thromboembolism.[6] Early recognition and surgical removal on cardiopulmonary bypass are very important to prevent systemic embolism as the occurrence of stroke poses a significant risk to initiate cardiopulmonary bypass on systemic full heparinization. Moreover, surgery addresses the increased mortality and morbidity posed by associated acute pulmonary thromboembolism.[6],[7]

The recent COVID-19 pandemic has led to an increased incidence of thromboembolic complications during the illness as well as in the recovery phase.[5] Though the mechanisms are not clear, viral-mediated endothelial inflammation, increased concentrations of procoagulants, decreased concentrations of endogenous anticoagulants are implicated as reasons.[8] In the absence of uniform guidelines, prophylactic anticoagulation is recommended for critically ill and noncritically ill hospitalized patients till discharge and an additional 30 days of anticoagulation is recommended for those with high thrombotic risk and less bleeding risk. In the presence of thrombosis, management is the same as non-COVID-19 related thrombosis.[8] Different anticoagulation regimens are advocated to manage these complications. Even though our patient did not have a clear preceding febrile illness, the persistently elevated inflammatory markers even after 1 week of the onset of the illness made us suspect the illness to be a sequel to the infection. The emergency situation created by the dangling large thrombus across the mitral valve forced us to perform an immediate surgery, rather than investigate for different antibodies to identify a preceding infection.

Acute pulmonary embolism is primarily managed medically by systemic thrombolysis in high and intermediate-high risk cases and anticoagulation in intermediate-low and low-risk cases.[9] Surgical embolectomy is indicated only in those with contraindication to thrombolysis and those with failed thrombolysis. A thrombus in transit straddling the PFO complicating pulmonary embolism is a major factor influencing the decision-making. Even though transesophageal echocardiography readily identified thrombus in transit, the current pandemic forced clinicians to perform initial noninvasive methods such as computed tomography and magnetic resonance imaging before transesophageal echocardiography, an aerosol-generating investigation. Majority of these cases are managed by surgical exploration with good outcomes compared to those managed by thrombolysis.[6],[7] Recent techniques allow percutaneous retrieval in patients with high surgical risk.[10]


  Conclusion Top


RV dysfunction secondary to acute pulmonary embolism elevates the right atrial pressure thereby increasing the risk of paradoxical embolism through an oval foramen. Echocardiography is an important tool to identify thrombus in transit as well as quantify RV function. This allows risk stratification and guides further management. Even though surgery is rarely indicated in acute pulmonary embolism, thrombus in transit across the PFO risks systemic thromboembolism and warrants urgent surgical exploration, pulmonary embolectomy, and removal of the intracardiac thrombus.

Financial support and sponsorship

Nil.

Conflicts of interest

K Sivakumar is an editorial board member of the Journal of The Indian Academy of Echocardiography & Cardiovascular Imaging. The article was subject to the journal's standard procedures, with peer review handled independently of this editor and their research groups.

There are no other conflicts of interest.

 
  References Top

1.
Nellessen U, Daniel WG, Matheis G, Oelert H, Depping K, Lichtlen PR. Impending paradoxical embolism from atrial thrombus: Correct diagnosis by transesophageal echocardiography and prevention by surgery. J Am Coll Cardiol 1985;5:1002-4.  Back to cited text no. 1
    
2.
Maron BA, Shekar PS, Goldhaber SZ. Paradoxical embolism. Circulation 2010;122:1968-72.  Back to cited text no. 2
    
3.
Clergeau MR, Hamon M, Morello R, Saloux E, Viader F, Hamon M. Silent cerebral infarcts in patients with pulmonary embolism and a patent foramen ovale: A prospective diffusion-weighted MRI study. Stroke 2009;40:3758-62.  Back to cited text no. 3
    
4.
Goliszek S, Wiśniewska M, Kurnicka K, Lichodziejewska B, Ciurzyński M, Kostrubiec M, et al. Patent foramen ovale increases the risk of acute ischemic stroke in patients with acute pulmonary embolism leading to right ventricular dysfunction. Thromb Res 2014;134:1052-6.  Back to cited text no. 4
    
5.
Aryal MR, Gosain R, Donato A, Pathak R, Bhatt VR, Katel A, et al. Venous thromboembolism in COVID-19: Towards an ideal approach to thromboprophylaxis, screening, and treatment. Curr Cardiol Rep 2020;22:52.  Back to cited text no. 5
    
6.
Fauveau E, Cohen A, Bonnet N, Gacem K, Lardoux H. Surgical or medical treatment for thrombus straddling the patent foramen ovale: Impending paradoxical embolism? Report of four clinical cases and literature review. Arch Cardiovasc Dis 2008;101:637-44.  Back to cited text no. 6
    
7.
Sultan FA, Allen S, Sharif M, Mookadam F. Paradoxical thrombus 'caught in the act': Case report and review of the literature. Am J Med 2017;130:e23-5.  Back to cited text no. 7
    
8.
Piazza G, Morrow DA. Diagnosis, management, and pathophysiology of arterial and venous thrombosis in COVID-19. JAMA 2020;324:2548-9.  Back to cited text no. 8
    
9.
Konstantinides SV, Meyer G, Becattini C, Bueno H, Geersing GJ, Harjola VP, et al. 2019 ESC guidelines for the diagnosis and management of acute pulmonary embolism developed in collaboration with the European Respiratory Society (ERS): The Task Force for the diagnosis and management of acute pulmonary embolism of the European Society of Cardiology (ESC). Eur Respir J 2019;54:1901647.  Back to cited text no. 9
    
10.
Gill D, Evans S, Brown MT, Vadde A, Chang R, Stanley MD, et al. Percutaneous thromboembolectomy in a high-risk surgical patient with thrombus straddling a patent foramen ovale. JACC Cardiovasc Interv 2021;14:e45-7.  Back to cited text no. 10
    


    Figures

  [Figure 1], [Figure 2], [Figure 3]



 

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