Right Atrial Thrombosis and Pulmonary Embolism: A Narrative Review

Nina D. Anfinogenova; Oksana Y. Vasiltseva; Alexander V. Vrublevsky; Irina N. Vorozhtsova; Sergey V. Popov; Andrey V. Smorgon; Olga V. Mochula; Wladimir Y. Ussov

doi:10.1055/s-0040-1718399

Seminars in Thrombosis and Hemostasis, Table of Contents

Semin Thromb Hemost 2020; 46(08): 895-907
DOI: 10.1055/s-0040-1718399

Review Article

Right Atrial Thrombosis and Pulmonary Embolism: A Narrative Review

Nina D. Anfinogenova

¹Cardiology Research Institute, Tomsk National Research Medical Center, Russian Academy of Sciences, Tomsk, Russia

,

Oksana Y. Vasiltseva

²Unit of Aorta and Coronary Artery Surgery, E. Meshalkin National Medical Research Center, Ministry of Health of Russian Federation, Novosibirsk, Russia

,

Alexander V. Vrublevsky

¹Cardiology Research Institute, Tomsk National Research Medical Center, Russian Academy of Sciences, Tomsk, Russia

,

Irina N. Vorozhtsova

¹Cardiology Research Institute, Tomsk National Research Medical Center, Russian Academy of Sciences, Tomsk, Russia

,

Sergey V. Popov

¹Cardiology Research Institute, Tomsk National Research Medical Center, Russian Academy of Sciences, Tomsk, Russia

,

Andrey V. Smorgon

¹Cardiology Research Institute, Tomsk National Research Medical Center, Russian Academy of Sciences, Tomsk, Russia

,

Olga V. Mochula

¹Cardiology Research Institute, Tomsk National Research Medical Center, Russian Academy of Sciences, Tomsk, Russia

,

Wladimir Y. Ussov

¹Cardiology Research Institute, Tomsk National Research Medical Center, Russian Academy of Sciences, Tomsk, Russia

› Author Affiliations

Abstract

Prompt diagnosis of pulmonary embolism (PE) remains challenging, which often results in a delayed or inappropriate treatment of this life-threatening condition. Mobile thrombus in the right cardiac chambers is a neglected cause of PE. It poses an immediate risk to life and is associated with an unfavorable outcome and high mortality. Thrombus residing in the right atrial appendage (RAA) is an underestimated cause of PE, especially in patients with atrial fibrillation. This article reviews achievements and challenges of detection and management of the right atrial thrombus with emphasis on RAA thrombus. The capabilities of transthoracic and transesophageal echocardiography and advantages of three-dimensional and two-dimensional echocardiography are reviewed. Strengths of cardiac magnetic resonance imaging (CMR), computed tomography, and cardiac ventriculography are summarized. We suggest that a targeted search for RAA thrombus is necessary in high-risk patients with PE and atrial fibrillation using transesophageal echocardiography and/or CMR when available independently on the duration of the disease. High-risk patients may also benefit from transthoracic echocardiography with right parasternal approach. The examination of high-risk patients should involve compression ultrasonography of lower extremity veins along with the above-mentioned technologies. Algorithms for RAA thrombus risk assessment and protocols aimed at identification of patients with RAA thrombosis, who will potentially benefit from treatment, are warranted. The development of treatment protocols specific for the diverse populations of patients with right cardiac thrombosis is important.

Keywords

pulmonary embolism - atrial fibrillation - right atrium - right atrial appendage - risk assessment

Full Text

References

References
1 Konstantinides SV, Meyer G, Becattini C. et al; 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). Eur Heart J 2020; 41 (04) 543-603
2 Konstantinides SV, Torbicki A, Agnelli G. et al; Task Force for the Diagnosis and Management of Acute Pulmonary Embolism of the European Society of Cardiology (ESC). 2014 ESC guidelines on the diagnosis and management of acute pulmonary embolism. Eur Heart J 2014; 35 (43) 3033-3069 , 3069a–3069k
3 Farge D, Frere C, Connors JM. et al; International Initiative on Thrombosis and Cancer (ITAC) advisory panel. 2019 International clinical practice guidelines for the treatment and prophylaxis of venous thromboembolism in patients with cancer. Lancet Oncol 2019; 20 (10) e566-e581
4 Gilon D, Schechter D, Rein AJ. et al. Right atrial thrombi are related to indwelling central venous catheter position: insights into time course and possible mechanism of formation. Am Heart J 1998; 135 (03) 457-462
5 Kukla P, McIntyre WF, Koracevic G. et al. Relation of atrial fibrillation and right-sided cardiac thrombus to outcomes in patients with acute pulmonary embolism. Am J Cardiol 2015; 115 (06) 825-830
6 Casazza F, Bongarzoni A, Centonze F, Morpurgo M. Prevalence and prognostic significance of right-sided cardiac mobile thrombi in acute massive pulmonary embolism. Am J Cardiol 1997; 79 (10) 1433-1435
7 Koć M, Kostrubiec M, Elikowski W. et al; RiHTER Investigators. Outcome of patients with right heart thrombi: the Right Heart Thrombi European Registry. Eur Respir J 2016; 47 (03) 869-875
8 Ogren M, Bergqvist D, Eriksson H, Lindblad B, Sternby NH. Prevalence and risk of pulmonary embolism in patients with intracardiac thrombosis: a population-based study of 23 796 consecutive autopsies. Eur Heart J 2005; 26 (11) 1108-1114
9 Torbicki A, Galié N, Covezzoli A, Rossi E, De Rosa M, Goldhaber SZ. ICOPER Study Group. Right heart thrombi in pulmonary embolism: results from the International Cooperative Pulmonary Embolism Registry. J Am Coll Cardiol 2003; 41 (12) 2245-2251
10 Cresti A, García-Fernández MA, Miracapillo G. et al. Frequency and significance of right atrial appendage thrombi in patients with persistent atrial fibrillation or atrial flutter. J Am Soc Echocardiogr 2014; 27 (11) 1200-1207
11 de Divitiis M, Omran H, Rabahieh R. et al. Right atrial appendage thrombosis in atrial fibrillation: its frequency and its clinical predictors. Am J Cardiol 1999; 84 (09) 1023-1028
12 Torbicki A, Perrier A, Konstantinides S. et al; ESC Committee for Practice Guidelines (CPG). Guidelines on the diagnosis and management of acute pulmonary embolism: the Task Force for the Diagnosis and Management of Acute Pulmonary Embolism of the European Society of Cardiology (ESC). Eur Heart J 2008; 29 (18) 2276-2315
13 Chapoutot L, Nazeyrollas P, Metz D. et al. Floating right heart thrombi and pulmonary embolism: diagnosis, outcome and therapeutic management. Cardiology 1996; 87 (02) 169-174
14 Anwar AM, Nosir YF, Ajam A, Chamsi-Pasha H. Central role of real-time three-dimensional echocardiography in the assessment of intracardiac thrombi. Int J Cardiovasc Imaging 2010; 26 (05) 519-526
15 Tufano A, Galderisi M. Can echocardiography improve the prediction of thromboembolic risk in atrial fibrillation? Evidences and perspectives. Intern Emerg Med 2020; 15 (06) 935-943
16 Kronik G. European Working Group on Echocardiography. The European Cooperative Study on the clinical significance of right heart thrombi. Eur Heart J 1989; 10 (12) 1046-1059
17 Vasiltseva OYa, Vorozhtsova IN, Lavrov AG, Karpov RS. Thrombi in the right cardiac chambers in patients with pulmonary embolism and atrial fibrillation. Vestnik Aritmologii 2018; 92: 16-20
18 Mohan B, Chhabra ST, Gulati A. et al. Clinical and echocardiographic diagnosis, follow up and management of right-sided cardiac thrombi. Indian Heart J 2013; 65 (05) 529-535
19 Takeuchi Y, Sakamoto H, Sakaguchi G, Shimada T. The invaluable observation of a hazardous patient with a floating and Gecko-like-shaped right atrial thrombus diagnosed by echocardiography and computed tomography imaging. J Echocardiogr 2019; 17 (02) 104-105
20 Mansencal N, Attias D, Caille V. et al. Computed tomography for the detection of free-floating thrombi in the right heart in acute pulmonary embolism. Eur Radiol 2011; 21 (02) 240-245
21 Arisha MJ, Hsiung MC, Nanda NC. et al. Two- and three-dimensional transthoracic echocardiographic assessment of superior vena cava, crista terminalis, and right atrial appendage using the right parasternal approach. Echocardiography 2017; 34 (12) 1919-1929
22 Sahin T, Ural D, Kilic T. et al. Right atrial appendage function in different etiologies of permanent atrial fibrillation: a transesophageal echocardiography and tissue Doppler imaging study. Echocardiography 2010; 27 (04) 384-393
23 Hussain B, Tipoo Sultan FA, Shahzad T, Punjani S. Caught in the act - migration of a large right atrial thrombus to pulmonary artery during transthoracic echocardiography - a case report. J Pak Med Assoc 2017; 67 (12) 1927-1929
24 Cowie BS, Kluger R, Rex S, Missant C. The relationship between superior vena cava diameter and collapsibility and central venous pressure. Anaesth Intensive Care 2015; 43 (03) 357-360
25 Faletra FF, Ho SY, Auricchio A. Anatomy of right atrial structures by real-time 3D transesophageal echocardiography. JACC Cardiovasc Imaging 2010; 3 (09) 966-975
26 Patel V, Nanda NC, Upendram S. et al. Live three-dimensional right parasternal and supraclavicular transthoracic echocardiographic examination. Echocardiography 2005; 22 (04) 349-360
27 Marcella CP, Johnson LE. Right parasternal imaging: an underutilized echocardiographic technique. J Am Soc Echocardiogr 1993; 6 (04) 453-466
28 Mitchell C, Rahko PS, Blauwet LA. et al. Guidelines for performing a comprehensive transthoracic echocardiographic examination in adults: recommendations from the American Society of Echocardiography. J Am Soc Echocardiogr 2019; 32 (01) 1-64
29 Jin CN, Salgo IS, Schneider RJ. et al. Using anatomic intelligence to localize mitral valve prolapse on three-dimensional echocardiography. J Am Soc Echocardiogr 2016; 29 (10) 938-945
30 Song H, Zhou Q, Deng Q. et al. Morphologic assessment of the left atrial appendage in patients with atrial fibrillation by gray values-inverted volume-rendered imaging of three-dimensional transesophageal echocardiography: a comparative study with computed tomography. J Am Soc Echocardiogr 2016; 29 (11) 1100-1108
31 Veulemans V, Hellhammer K, Polzin A, Bönner F, Zeus T, Kelm M. Current and future aspects of multimodal and fusion imaging in structural and coronary heart disease. Clin Res Cardiol 2018; 107 (Suppl. 02) 49-54
32 Neskovic AN, Skinner H, Price S. et al; Reviewers: This document was reviewed by members of the 2016–2018 EACVI Scientific Documents Committee. Focus cardiac ultrasound core curriculum and core syllabus of the European Association of Cardiovascular Imaging. Eur Heart J Cardiovasc Imaging 2018; 19 (05) 475-481
33 Jammal M, Milano P, Cardenas R, Mailhot T, Mandavia D, Perera P. The diagnosis of right heart thrombus by focused cardiac ultrasound in a critically ill patient in compensated shock. Crit Ultrasound J 2015; 7: 6
34 Bannas P, Groth M, Lund G. Typical cardiac MRI findings of a prominent crista terminalis mimicking a right atrial mass on echocardiography. RoFo Fortschr Geb Rontgenstr Nuklearmed 2012; 184 (08) 740-741
35 Kuno T, Imaeda S, Hashimoto K. et al. Recent inferior myocardial infarction complicated with a right ventricular thrombus detected by three cardiac imaging modalities. Intern Med 2018; 57 (05) 693-695
36 Takeuchi D, Inai K, Shinohara T, Nakanishi T, Park IS. Blood coagulation abnormalities and the usefulness of D-dimer level for detecting intracardiac thrombosis in adult Fontan patients. Int J Cardiol 2016; 224: 139-144
37 Camm AJ, Kirchhof P, Lip GY. et al; ESC Committee for Practice Guidelines. Guidelines for the management of atrial fibrillation: the Task Force for the Management of Atrial Fibrillation of the European Society of Cardiology (ESC). Europace 2010; 12 (10) 1360-1420
38 Jordan RA, Scheifley CH, Edwards JE. Mural thrombosis and arterial embolism in mitral stenosis; a clinico-pathologic study of fifty-one cases. Circulation 1951; 3 (03) 363-367
39 Sawyer CG, Bolin LB, Stevens EL, Daniel Jr LB, O'Neil NC, Hayes DM. Atrial fibrillation: its etiology, treatment and association with embolization. South Med J 1958; 51 (01) 84-93
40 Rowe JC, Bland EF, Sprague HB, White PD. The course of mitral stenosis without surgery: ten- and twenty-year perspectives. Ann Intern Med 1960; 52: 741-749
41 Ng AC, Adikari D, Yuan D. et al. The prevalence and incidence of atrial fibrillation in patients with acute pulmonary embolism. PLoS One 2016; 11 (03) e0150448
42 Ptaszynska-Kopczynska K, Kiluk I, Sobkowicz B. Atrial fibrillation in patients with acute pulmonary embolism: clinical significance and impact on prognosis. BioMed Res Int 2019; 2019: 7846291
43 Flegel KM. When atrial fibrillation occurs with pulmonary embolism, is it the chicken or the egg?. CMAJ 1999; 160 (08) 1181-1182
44 Barra SN, Paiva LV, Providência R, Fernandes A, Leitão Marques A. Atrial fibrillation in acute pulmonary embolism: prognostic considerations. Emerg Med J 2014; 31 (04) 308-312
45 Guler GB, Can MM, Guler E. et al. Asymptomatic pulmonary embolism after ablation. Cardiology 2016; 134 (04) 426-432
46 Krajewska A, Ptaszynska-Kopczynska K, Kiluk I. et al. Paroxysmal atrial fibrillation in the course of acute pulmonary embolism: clinical significance and impact on prognosis. BioMed Res Int 2017; 2017: 5049802
47 Bikdeli B, Abou Ziki MD, Lip GYH. Pulmonary embolism and atrial fibrillation: two sides of the same coin? a systematic review. Semin Thromb Hemost 2017; 43 (08) 849-863
48 Kim YG, Han KD, Choi JI. et al. Impact of the duration and degree of hypertension and body weight on new-onset atrial fibrillation: A nationwide population-based study. Hypertension 2019; 74 (05) e45-e51
49 Matthews JC, McLaughlin V. Acute right ventricular failure in the setting of acute pulmonary embolism or chronic pulmonary hypertension: a detailed review of the pathophysiology, diagnosis, and management. Curr Cardiol Rev 2008; 4 (01) 49-59
50 Naksuk N, Padmanabhan D, Yogeswaran V, Asirvatham SJ. Left atrial appendage: embryology, anatomy, physiology, arrhythmia and therapeutic intervention. JACC Clin Electrophysiol 2016; 2 (04) 403-412
51 Suratkal V, Ahmed A. Right atrial thrombus and challenges in its management. J Assoc Physicians India 2018; 66 (12) 65-68
52 January CT, Wann LS, Calkins H. et al. 2019 AHA/ACC/HRS Focused Update of the 2014 AHA/ACC/HRS Guideline for the Management of Patients With Atrial Fibrillation: a report of the American College of Cardiology/American Heart Association Task Force on Clinical Practice Guidelines and the Heart Rhythm Society in Collaboration With the Society of Thoracic Surgeons. Circulation 2019; 140 (02) e125-e151
53 Ahmed A, Bagga S, Clark B, Gilge J, Padanilam B. Using cardiac implantable electronic device to noninvasively perform electrophysiology study to reduce procedural risk in a patient with right atrial lead thrombus and pulmonary embolism. J Am Coll Cardiol 2019; 73: 2658-2658
54 Lenz CJ, DeSimone CV, Ponamgi SP. et al. Cardiac implantable electronic device lead-based masses and atrial fibrillation ablation: a case-based illustration of periprocedural anticoagulation management strategies. J Interv Card Electrophysiol 2016; 46 (03) 237-243
55 Dan GA, Iliodromitis K, Scherr D. et al. Translating guidelines into practice for the management of atrial fibrillation: results of an European Heart Rhythm Association Survey. Europace 2018; 20 (08) 1382-1387
56 Vasiltseva OYa, Vorozhtsova IN, Karpov RS. Method of estimating probability of mural thrombosis of right heart chambers: right atrium and right ventricle. Patent of the Russian Federation No. RU2488347C1. Published on July 27, 2013. Bulletin No. 12, 11p
57 Vasiltseva OYa, Vorozhtsova IN, Lavrov AG, Gorlova AA, Panfilova IKh, Krishkevich EV. Approach to the assessment of probability of pulmonary embolism from the right atrial appendage in adult patients. Patent of the Russian Federation No. RU2677013. Published on January 14, 2019. Bulletin No. 2, 13p
58 Martínez-Quintana E, Rodríguez-González F. Cor triatriatum dexter: more than a simple membrane. J Thorac Cardiovasc Surg 2016; 151 (01) 276-277
59 Hussain ST, Pettersson GB. Cor triatriatum dexter in adults: clinical implications. J Thorac Cardiovasc Surg 2016; 151 (01) 277-278
60 Sugimoto A, Shiraishi S, Watanabe M. et al. Non-bacterial thrombotic endocarditis in the right atrium caused by pectus excavatum. Surg Case Rep 2016; 2 (01) 105
61 Citarella A, Boulemden A, Nadarajah D, Apicella G, Mahmoud A, Shanmuganathan S. A traveler in transit: A case of an impending thrombus entrapped in a patent foramen ovale. J Card Surg 2019; 34 (11) 1402-1404
62 Pappas AJ, Knight SW, McLean KZ, Bork S, Kurz MC, Sawyer KN. Thrombus-in-transit: A case for a multidisciplinary hospital-based pulmonary embolism system of care. J Emerg Med 2016; 51 (03) 298-302
63 Byard RW. Entrapped paradoxical thromboembolism. Forensic Sci Med Pathol 2019; 15 (01) 147-150
64 Corban MT, Alothman OWJ, Martin WP. et al. Neither here nor there: intracardiac thrombus in transit wedged in a patent foramen ovale. Mayo Clin Proc 2019; 94 (03) 547-549
65 Huang G, Pavan D, Antonini-Canterin F, Piazza R, Cassin M, Nicolosi GL. Thrombus in the right atrial appendage during pulmonary and paradoxical embolism: a case report. Ital Heart J 2002; 3 (08) 486-489
66 Mirijello A, D'Errico MM, Curci S. et al. Paradoxical embolism with thrombus stuck in a patent foramen ovale: a review of treatment strategies. Eur Rev Med Pharmacol Sci 2018; 22 (24) 8885-8890
67 Lu C, Li J, Wang W, Gong K, Zhao L, Fu X. Large thrombus-in-transit within a patent foramen ovale in a patient with pulmonary embolism: a case report. J Int Med Res 2018; 46 (10) 4332-4337
68 Schaefer A, Treede H, Reichenspurner H, Conradi L. Large biatrial thrombembolus caught in transit across a patent foramen ovale. Thorac Cardiovasc Surg Rep 2015; 4 (01) 44-45
69 Chowdhury MA, Ramanathan K, Grande RD, Letcher JR. Incidental finding of a mass fitting into a patent foramen ovale. J Echocardiogr 2019; 17 (03) 162-163
70 Barros-Gomes S, El Sabbagh A, Eleid MF, Mankrad SV. Concomitant acute stroke, pulmonary and myocardial infarction due to in-transient thrombus across a patent foramen ovale. Echo Res Pract 2018; 5 (04) I9-I10
71 Nkoke C, Faucher O, Camus L, Flork L. Free floating right heart thrombus associated with acute pulmonary embolism: An unsettled therapeutic difficulty. Case Rep Cardiol 2015; 2015: 364780
72 Saura D, García-Puente J, Oliva MJ. et al. Treatment of right heart thromboemboli: the need of a randomized multicentre trial. Int J Cardiol 2009; 134 (03) 419-420
73 Barrios D, Chavant J, Jiménez D. et al; Registro Informatizado de la Enfermedad TromboEmbólica Investigators. Treatment of right heart thrombi associated with acute pulmonary embolism. Am J Med 2017; 130 (05) 588-595
74 Moosavi J, Shafe O, Alizadehasl A. et al. Half-dose thrombolytic therapy in patients with right heart thrombi. J Int Med Res 2019; 47 (07) 3400-3407
75 Basman C, Rashid U, Parmar YJ, Kliger C, Kronzon I. The role of percutaneous vacuum-assisted thrombectomy for intracardiac and intravascular pathology. J Card Surg 2018; 33 (10) 666-672
76 Resnick SA, O'Brien D, Strain D. et al. Single-center experience using AngioVac with extracorporeal bypass for mechanical thrombectomy of atrial and central vein thrombi. J Vasc Interv Radiol 2016; 27 (05) 723.e1-729.e1
77 Patnaik S, Rammohan HS, Shah M. et al. Percutaneous embolectomy of serpentine thrombus from the right atrium in a 51-year-old man. Tex Heart Inst J 2016; 43 (06) 524-527
78 Moriarty JM, Al-Hakim R, Bansal A, Park JK. Removal of caval and right atrial thrombi and masses using the AngioVac device: initial operative experience. J Vasc Interv Radiol 2016; 27 (10) 1584-1591
79 AbuHalimeh B, Desai MY, Tonelli AR. Effect of abnormal right heart structures on the diagnosis of pulmonary hypertension. Pulm Circ 2018; 8 (02) 2045894018773053
80 Wann LS, Curtis AB, January CT. et al; ACCF/AHA/HRS. 2011 ACCF/AHA/HRS focused update on the management of patients with atrial fibrillation (Updating the 2006 Guideline): a report of the American College of Cardiology Foundation/American Heart Association Task Force on Practice Guidelines. J Am Coll Cardiol 2011; 57 (02) 223-242
81 Pescetelli I, Genovesi E, Renda G, Di Renzo E, De Caterina R. Intracardiac thrombi during warfarin anticoagulation – a case report and a brief literature review. Cor Vasa 2017; 59: E277-E281
82 Dudiy Y, Kronzon I, Cohen HA, Ruiz CE. Vacuum thrombectomy of large right atrial thrombus. Catheter Cardiovasc Interv 2012; 79 (02) 344-347
83 Ram H, Gerlach RM, Hernandez Conte A, Ramzy D, Jaramillo-Huff AR, Gerstein NS. The AngioVac device and its anesthetic implications. J Cardiothorac Vasc Anesth 2017; 31 (03) 1091-1102
84 Hameed I, Lau C, Khan FM. et al. AngioVac for extraction of venous thromboses and endocardial vegetations: A meta-analysis. J Card Surg 2019; 34 (04) 170-180
85 Starck CT, Eulert-Grehn J, Kukucka M. et al. Managing large lead vegetations in transvenous lead extractions using a percutaneous aspiration technique. Expert Rev Med Devices 2018; 15 (10) 757-761
86 Hakman EN, Cowling KM. Paradoxical embolism. StatPearls [Internet]. Treasure Island, FL: StatPearls Publishing; 2020 Jan-. 2019 Nov 18
87 Chaikof EL, Campbell BE, Smith III RB. Paradoxical embolism and acute arterial occlusion: rare or unsuspected?. J Vasc Surg 1994; 20 (03) 377-384