Journal Logo

Feature Articles

Venoarterial Extracorporeal Membrane Oxygenation in Massive Pulmonary Embolism-Related Cardiac Arrest: A Systematic Review*

Scott, John Harwood MD1; Gordon, Matthew MD1; Vender, Robert MD2; Pettigrew, Samantha MD2; Desai, Parag MD1; Marchetti, Nathaniel DO1; Mamary, Albert James MD1; Panaro, Joseph MD3; Cohen, Gary MD3; Bashir, Riyaz MD4; Lakhter, Vladimir DO4; Roth, Stephanie MLIS5; Zhao, Huaqing PhD, MS6; Toyoda, Yoshiya MD, PhD7; Criner, Gerard MD1; Moores, Lisa MD8; Rali, Parth MD1

Author Information
doi: 10.1097/CCM.0000000000004828

Abstract

Venous thromboembolism (VTE) has a mortality rate of 10–30% within the first month of diagnosis (1). The number of annual VTE cases in the United States and Western Europe is approximately 900,000 and 700,000, respectively (2,3). The spectrum of pulmonary embolism (PE) severity ranges from low-risk to submassive to massive PE, each with an escalating expected mortality (4,5). A massive PE is defined by the American College of Chest Physicians (ACCP) as acute PE with sustained hypotension (systolic blood pressure < 90 mm Hg or systolic pressure drop > 40 mm Hg for at least 15 minutes, or requiring vasopressor or inotropic support) (6–9). Although only 8–10% of PEs are massive, they account for most of the PE-related mortality (4,6,10). Within massive PE, the hemodynamic instability can be further delineated by refractory hypotension, obstructive shock, or cardiac arrest (8). Massive PE leading to cardiac arrest has a mortality as high as 90–95% (11,12).

Venoarterial extracorporeal membrane oxygenation (VA-ECMO) is an emerging therapeutic option in the management of cardiogenic shock, with or without cardiac arrest, either as a bridge-to-therapy or bridge-to-recovery (13–16). VA-ECMO in massive PE-related cardiac arrest can unload the right ventricle and prevent subsequent cardiac arrest by rapidly establishing critical organ reperfusion and tissue oxygenation.

Guidelines from the ACCP (Grade 2B), American Heart Association (AHA) (class IIA, level of evidence B), and European society of cardiology (ESC) [class I, level of evidence B], all recommend the use of a systemic thrombolytic infusion for massive PE (8,9,17). Recently updated ESC 2019 guidelines suggest considering VA-ECMO for massive PE patients (class IIb, level of evidence C), in the appropriate clinical setting, even though randomized control trials are lacking (8). Massive PE-related cardiac arrest management is controversial with AHA guidelines recommending push-dose systemic thrombolysis in confirmed massive PE-related cardiac arrest (Class IIa, level of evidence C) (9,12). Push-dose thrombolytic brings an increased risk of bleeding particularly in the setting of ongoing cardiopulmonary resuscitation (CPR). Furthermore, traumatic or prolonged (≥ 10 min) CPR is a relative contraindication to the use of systemic thrombolysis (17,18). Whether VA-ECMO has any role in massive PE-related cardiac arrest remains unknown, particularly with the potential background thrombolysis. Previously published systematic reviews investigated outcomes of VA-ECMO in massive PE, not massive PE-related cardiac arrest (6,14). In this systematic review, we explored the role of VA-ECMO in massive PE-related cardiac arrest and performed multivariate analysis for predictors of death.

MATERIALS AND METHODS

To identify studies to include or consider for this systematic review, the reviewers worked with a medical librarian with systematic review expertise to develop the search. We created and followed the Preferred Reporting Items for Systematic Reviews and Meta-Analysis checklist protocol (Appendix 1, http://links.lww.com/CCM/G116). The search was developed for PubMed and translated for Embase, Cochrane Central, Cinahl, and Web of Science using a combination of subject headings and free-text terms. A gray literature search included a trial registry: clinicaltrials.gov and a Preprint search engine: bioPreprint. The search included no major limits or date restrictions. We began developing the search February 16, 2020, and last literature search was completed on March 16, 2020.

The search (complete details of the PubMed [National Library of Medicine] provided in Appendix 2, http://links.lww.com/CCM/G117) initially resulted in the 1,374 studies with the following studies from each database: PubMed 357 results, Embase (Elsevier) 568 results, Web of Science (Clarivate Analytics) 339 results, Cinahl (Ebscohost) 81 results, and Cochrane CENTRAL (Wiley) 16 results. There were 259 duplicate references found and omitted using Refworks, leaving 1,115 references (13 additional from gray literature sources) for screening (Fig. 1).

Figure 1.
Figure 1.:
Preferred reporting items for systematic reviews and meta-analysis diagram.

Studies were screened by title and abstract by two blinded and independent reviewers using the Rayyan online software (https://rayyan.qcri.org). If a tiebreaker was needed, a third reviewer was also called in. This process was repeated for full-text article screening and selection.

Articles and abstracts were considered eligible for inclusion if they: 1) described very specific clinical scenario of massive PE with cardiac arrest managed with VA-ECMO and 2) reported whether patient(s) survived to discharge. All dates of publication prior to our search date were included. Articles were excluded if not published in English. About 77 studies were included in this review (Fig. 1) and were assessed for bias using Joanna Briggs Institute Critical Appraisal Checklist for Systematic Reviews and Research Syntheses (19–95). Our review considered articles to have a low risk of bias if all checklist criteria were met, moderate risk if greater than or equal to 75% of criteria were met, and high risk if less than 75% of criteria were met. Risk of bias assessment found 34 articles to be low risk, 37 moderate risk, and six high risk (Supplemental Table 1, http://links.lww.com/CCM/G118). Data were extracted independently by four physician participants. The primary outcome was survival to discharge. Secondary outcomes included the impact of age, systemic thrombolysis before extracorporeal membrane oxygenation (ECMO), ECMO cannulation during CPR or after return of spontaneous circulation (ROSC), PE as primary reason for admission, and hospital location of ECMO cannulation on mortality. We also recorded the occurrence rate of major bleeding (Appendix 3, http://links.lww.com/CCM/G117, for complete definitions [96]) and neurologic outcome per the cerebral performance category (CPC) score.

Differences between the groups were assessed using unpaired t tests for continuous variables and chi-square tests for categorical variables. Univariate analyses on the secondary outcomes listed above were examined with t test or chi-square test as well. Univariate and multivariable logistic regression models were performed to derive the unadjusted or adjusted odds ratios (ORs) of mortality. ORs and 95% CIs (95% CI) were calculated and based on the selected published studies. A p value of less than 0.05 was considered statistically significant. All the data were analyzed using Stata 14.0 (Stata Corp., College Station, TX).

RESULTS

About 301 patients met inclusion criteria and were used for analysis. The mean age was 48 years old (n = 113) and 63% (n = 71) were females. About 183 out of 301 patients (61%) survived to discharge. There was a three-fold increase in risk of death for patients greater than 65 years old (OR, 3.56; 95% CI, 1.29–9.87; p = 0.02). Patients who were cannulated during CPR (survival 65%; n = 64 of 99) (Fig. 2) had a seven-fold increase in risk of death (OR, 6.84; 95% CI, 1.53–30.58; p = 0.01) compared with those cannulated after ROSC (survival 93%; n = 25 of 27).

Figure 2.
Figure 2.:
Total reported patients (black bar) and reported patients surviving to discharge (gray bar). Odds risk of death between the first and second groups listed above for each category with its associated p value (95% CI). CPR = cardiopulmonary resuscitation, OR = odds ratio, PE = pulmonary embolism, ROSC = return of spontaneous circulation.

We identified a cohort of 51 patients who received systemic thrombolysis prior to VA-ECMO cannulation. Survival to discharge in this cohort was 67% (n = 34). There was no increased risk of death in patients receiving systemic thrombolysis prior to VA-ECMO cannulations versus those who did not (OR, 0.78; 95% CI, 0.39–1.54; p = 0.48) (Table 1). Six patients who received thrombolysis prior to cannulation had a reported major bleeding event; all of them survived.

There was no difference in survival when PE was the primary reason for admission (76%, n = 68 of 90) or not (83%, n = 30 of 36) (OR, 1.62; 95% CI, 0.60–4.40; p = 0.35]. Non-PE-related admissions were for surgery (n = 15), trauma (n = 11), cesarean section (n = 3), myocardial infarction (n = 3), deep venous thrombosis (n = 1), and diabetic ketoacidosis (n = 1). We did not find a difference in risk of death based on where in the hospital VA-ECMO cannulation was performed (emergency department [ED] vs all other sites; OR, 2.52; 95% CI, 0.69–9.26; p = 0.16). Locations for cannulation were the ED (n = 35) with 77% survival, cardiac catheterization laboratory (n = 15; 80% survival), ICU (n = 10; 90% survival), operating room (n = 10; 100% survival), and medical/surgical floors (n = 3; 100% survival). About 21 patients had reported major bleeding with 76% survival (n = 16), whereas 30 patients had no major bleeding with 80% survival (n = 24). Seven patients experienced critical site bleed with six surviving. About 88% of patients were neurologically intact (CPC of 1) at discharge or follow-up (n = 53 of 60).

Multivariate analysis demonstrated statistically significant risk of death for two secondary outcomes: age greater than 65 and cannulation during CPR. There was still a three-fold increase in the adjusted risk of death for patients greater than 65 years old (adjusted OR, 3.08; 95% CI, 1.09–8.67; p = 0.03). Patients who were cannulated during CPR had a six-fold increase in the adjusted risk of death (adjusted OR, 5.67; 95% CI, 1.23–26.20; p = 0.03) compared with those cannulated after ROSC.

DISCUSSION

In our large cohort of 301 patients presenting with massive PE-related cardiac arrest that was managed with post-arrest VA-ECMO, we found survival to discharge to be 61%. We identified age greater than 65 and cannulation during CPR to be independent markers of mortality (adjusted OR, 3.08; p = 0.03 and adjusted OR, 5.67; p = 0.03, respectively) in our multivariate analysis.

Massive PE-related cardiac arrest has mortality as high as 90% (11,12). We specifically assessed whether thrombolysis before ECMO cannulation lowered the chance of survival. Prior literature, particularly Al-Bawardy et al (19) in a small case series, showed a survival rate of 62% (eight of 13) when thrombolysis and ECMO were used concomitantly in setting of massive PE. We identified 51 cases (17% of total 301 patients) in our review who had systemic thrombolysis prior to VA-ECMO; survival to hospital discharge was 67% (34 of 51). The odds of death for patients receiving pre-ECMO thrombolytics versus not (OR, 0.78; 95% CI, 0.39–1.54; p = 0.48) (Table 1) were not different. There were only six patients with reports of major bleed in this cohort (all survived). These findings are suggestive that preceding thrombolysis did not confer an additional risk of death leading us to feel it should not be considered a contraindication to subsequent ECMO. This finding is particularly germane given the high likelihood that patients with massive PE-related cardiac arrest have been considered for or have received preceding thrombolytics (8,9,17). Once thrombolytics are used but unsuccessful at restoring hemodynamic stability, the use of other reperfusion modalities (e.g., pulmonary embolectomy, catheter-directed thrombolysis, and VA-ECMO) is often not considered in the immediate postthrombolytic setting due to the increased risk of bleeding.

TABLE 1. - Odds Ratios for Secondary Outcomes With the Number of Patients That These Values Were Reported on
Group Number of Patients With Variable Known OR (Risk of Death) (95% CI) p
Age > 65 vs age ≤ 65 113 3.56 (1.29–9.87) 0.02
Male vs female 113 0.59 (0.22–1.56) 0.29
Pulmonary embolism primary reason for admission vs not primary reason for admission 126 1.62 (0.60–4.40) 0.35
Systemic thrombolysis prior to ECMO cannulation vs no systemic thrombolysis prior to ECMO cannulation 179 0.78 (0.39–1.54) 0.48
Cannulation during cardiopulmonary resuscitation vs after return-of-spontaneous-circulation 126 6.84 (1.53–30.58) 0.01
Cannulated in emergency department vs all other sites combined 73 2.52 (0.69–9.26) 0.16
ECMO = extracorporeal membrane oxygenation, OR = odds ratio.

There were 21 (7% of all patients in our review, n = 301) reports of major bleeding reported in our study and the survival among that cohort was 76% (n = 16). For comparison, Al-Bawardy et al (19) reported 54% major bleeding events in their case series and a large meta-analysis involving 1,866 patients looking at ECMO complications in patients with cardiogenic shock reported close to 40% major bleeding events (97). Based on these prior reports, we suspect our reported rate of bleeding rates may be subject to reporting bias and the true occurrence rate is likely higher. We found no significant difference in survival when PE was the primary reason for admission versus not (76% and 83%, respectively). This likely reflects that ECMO centers were prepared for emergent cannulation irrespective of the primary reason for hospitalization. There was also no difference in risk of death if cannulation occurred in the ED versus other sites in the hospital (OR, 2.52; p = 0.16), again likely reflecting ECMO centers’ preparedness.

In addition to survival, neurologic recovery remains the other main important outcome for massive PE-related cardiac arrest. Stub et al (98), in a single-center prospective study showed that nearly half of the patients (54%) had acceptable neurologic outcomes (CPC of 1) at the time of hospital discharge in the setting of ECMO use in cardiac arrest. Our study had 60 patients with reported neurologic outcomes, 88% (n = 53) of whom had an excellent neurologic recovery (CPC of 1). Although encouraging, this finding is limited by the absence of a neurologic status at discharge being reported for the majority of our included patients.

There are several limitations of this review, reporting bias being the most notable. Our study can only report a survival to discharge without significant comment on short- or long-term survival. Literature in abstract form was used but often did not often provide additional detail beyond our primary outcome. Furthermore, there was heterogeneous reporting of important clinical variables (neurologic status at discharge, presence or absence of significant bleed, cannulation during or after CPR, and duration of CPR) among the majority of literature found that made it difficult to comment confidently on all of these variables’ impact on survival. We also did not have sufficient detail to comment on comorbid conditions and other important secondary outcomes: long-term need for dialysis, chronic ventilator dependency, discharge to nursing facilities versus home, need for percutaneous endoscopic gastrostomy and artificial feeding, readmissions, and long-term PE-related complications like chronic thromboembolic pulmonary hypertension.

This review reflects the continued emergence of VA-ECMO as a treatment modality for patients with obstructive shock due to massive PE (6,54,99). A strength of this study is that we sought to identify the cohort with the highest risk of death by selecting patients who not only had massive PE but also presented with or acutely developed cardiac arrest. To our knowledge, this is the first systematic review focused on evaluating outcomes of VA-ECMO in massive PE-related cardiac arrest or attempted to identify predictors of mortality with multivariate analysis (6,14,100). We were able to find the largest number of patients to include in our systemic review, which allowed us to perform a multivariate analysis that led to significant findings of age greater than 65 years old and cannulation during CPR being associated with a notable increased risk of death. We feel our findings are helpful for clinical decision-making in rapidly accessing candidacy for VA-ECMO and providing assurance that systemic thrombolysis is not a contraindication for ECMO use.

CONCLUSIONS

The use of VA-ECMO in management of massive PE-related cardiac arrest has a survival rate of 61%. Systemic thrombolysis prior to VA-ECMO did not confer increased odds of death and this review suggests that both modalities can be complimentary to each other with a focus on achieving ROSC. In our study, age greater than 65 and ECMO cannulation during CPR had increased mortality (three- and six-fold risks of death, respectively) and may aid in the decision-making process of deploying VA-ECMO for massive PE-related cardiac arrest.

Drs. Scott and Rali involved with article selection, data extraction, and article preparation. Drs. Gordon, Desai, Marchetti, Mamary, Panaro, Cohen, Bashir, Lakhter, Toyoda, Criner, and Moores contributed to article review and preparation. Dr. Vender helped in article selection (third party for disagreements) and data extraction. Drs. Pettigrew and Kim involved in data extraction and article assessment for risk-of-bias. Mr. Roth provided complete literature search and software to include or exclude articles in addition to guidance on systematic review methods. Dr. Zhao helped in statistical analysis.

REFERENCES

1. Beckman MG, Hooper WC, Critchley SE, et al. Venous thromboembolism: A public health concern. Am J Prev Med. 2010; 38:S495–S501
2. Cohen AT, Agnelli G, Anderson FA, et al.; VTE Impact Assessment Group in Europe (VITAE). Venous thromboembolism (VTE) in Europe. The number of VTE events and associated morbidity and mortality. Thromb Haemost. 2007; 98:756–764
3. Roger VL, Go AS, Lloyd-Jones DM, et al. Heart disease and stroke statistics--2012 update: A report from the American Heart Association. Circulation. 2012; 125:e2–e220
4. Kucher N, Rossi E, De Rosa M, et al. Massive pulmonary embolism. Circulation. 2006; 113:577–582
5. Goldhaber SZ, Visani L, De Rosa M. Acute pulmonary embolism: Clinical outcomes in the International Cooperative Pulmonary Embolism Registry (ICOPER). Lancet. 1999; 353:1386–1389
6. Yusuff HO, Zochios V, Vuylsteke A. Extracorporeal membrane oxygenation in acute massive pulmonary embolism: A systematic review. Perfusion. 2015; 30:611–616
7. Konstantinides SV. 2014 ESC guidelines on the diagnosis and management of acute pulmonary embolism. Eur Heart J. 2014; 35:3145–3146
8. Konstantinides SV, Meyer G. The 2019 ESC guidelines on the diagnosis and management of acute pulmonary embolism. Eur Heart J. 2019; 40:3453–3455
9. Jaff MR, McMurtry MS, Archer SL, et al.; American Heart Association Council on Cardiopulmonary, Critical Care, Perioperative and Resuscitation; American Heart Association Council on Peripheral Vascular Disease; American Heart Association Council on Arteriosclerosis, Thrombosis and Vascular Biology. Management of massive and submassive pulmonary embolism, iliofemoral deep vein thrombosis, and chronic thromboembolic pulmonary hypertension: A scientific statement from the American Heart Association. Circulation. 2011; 123:1788–1830
10. Weinberg A, Tapson VF, Ramzy D. Massive pulmonary embolism: Extracorporeal membrane oxygenation and surgical pulmonary embolectomy. Semin Respir Crit Care Med. 2017; 38:66–72
11. Laher AE, Richards G. Cardiac arrest due to pulmonary embolism. Indian Heart J. 2018; 70:731–735
12. Lavonas EJ, Drennan IR, Gabrielli A, et al. Part 10: Special circumstances of resuscitation: 2015 American Heart Association guidelines update for cardiopulmonary resuscitation and emergency cardiovascular care. Circulation. 2015; 132:S501–S518
13. Rao P, Khalpey Z, Smith R, et al. Venoarterial extracorporeal membrane oxygenation for cardiogenic shock and cardiac arrest. Circ Heart Fail. 2018; 11:e004905
14. O’Malley TJ, Choi JH, Maynes EJ, et al. Outcomes of extracorporeal life support for the treatment of acute massive pulmonary embolism: A systematic review. Resuscitation. 2020; 146:132–137
15. van Diepen S, Katz JN, Albert NM, et al.; American Heart Association Council on Clinical Cardiology; Council on Cardiovascular and Stroke Nursing; Council on Quality of Care and Outcomes Research; and Mission: Lifeline. Contemporary management of cardiogenic shock: A scientific statement from the American Heart Association. Circulation. 2017; 136:e232–e268
16. Vahdatpour C, Collins D, Goldberg S. Cardiogenic shock. J Am Heart Assoc. 2019; 8:e011991
17. Kearon C, Akl EA, Ornelas J, et al. Antithrombotic therapy for VTE disease: CHEST guideline and expert panel report. Chest. 2016; 149:315–352
18. Macovei L, Presura RM, Arsenescu Georgescu C. Systemic or local thrombolysis in high-risk pulmonary embolism. Cardiol J. 2015; 22:467–474
19. Al-Bawardy R, Rosenfield K, Borges J, et al. Extracorporeal membrane oxygenation in acute massive pulmonary embolism: A case series and review of the literature. Perfusion. 2019; 34:22–28
20. Algahtani H, Azzam M, Albanna AS, et al. Neurological recovery from multiple cardiac arrests due to acute massive pulmonary embolism managed by cardiopulmonary resuscitation and extracorporeal membrane oxygenation. Cardiovasc Revasc Med. 2018; 19:120–122
21. Apranaji K, Cavagnaro J, D’Alessandro D, et al. Extracorporeal membrane oxygenation in massive pulmonary embolism associated with life-threatening circulatory collapse. Crit Care Med. 2011; 39:260
22. Arlt M, Philipp A, Iesalnieks I, et al. Successful use of a new hand-held ECMO system in cardiopulmonary failure and bleeding shock after thrombolysis in massive post-partal pulmonary embolism. Perfusion. 2009; 24:49–50
23. Bataillard A, Hebrard A, Gaide-Chevronnay L, et al. Extracorporeal life support for massive pulmonary embolism during pregnancy. Perfusion. 2016; 31:169–171
24. Bougouin W, Marijon E, Planquette B, et al.; on behalf from the Sudden Death Expertise Center. Pulmonary embolism related sudden cardiac arrest admitted alive at hospital: Management and outcomes. Resuscitation. 2017; 115:135–140
25. Carroll B, Kabrhel C, Dudzinski DM, et al. C56 clinical cases in pulmonary vascular medicine: Survival in a 45 year old male with massive pulmonary embolism and cardiac arrest with treatment utilizing novel technology after activation of a multi-disciplinary pulmonary embolism response team (pert). Am J Respir Crit Care Med. 2014; 189:1
26. Chen CH, Chin HY, Chen HH, et al. Pills-related severe adverse events: A case report in Taiwan. Taiwan J Obstet Gynecol. 2016; 55:588–590
27. Cho YH, Kim WS, Sung K, et al. Management of cardiac arrest caused by acute massive pulmonary thromboembolism: Importance of percutaneous cardiopulmonary support. ASAIO J. 2014; 60:280–283
28. Chon MK, Park YH, Choi JH, et al. Thrombolytic therapy complemented by ECMO: Successful treatment for a case of massive pulmonary thromboembolism with hemodynamic collapse. J Korean Med Sci. 2014; 29:735–738
29. Chuang CJ, Hsu CS. Successful application of extracorporeal membrane oxygenation and pulmonary thromboembolectomy in a patient with a life-threatening pulmonary embolism. Taiwan J Obstet Gynecol. 2015; 54:467–468
30. Conzelmann L, Mehlhorn U, Kayhan N, et al. Successful management of fulminant pulmonary embolism using the LIFEBRIDGE-B2T® portable extracorporeal life support system. J Thorac Cardiovasc Surg. 2010; 58
31. Corsi F, Lebreton G, Bréchot N, et al. Life-threatening massive pulmonary embolism rescued by venoarterial-extracorporeal membrane oxygenation. Crit Care. 2017; 21:76
32. Davies MJ, Arsiwala SS, Moore HM, et al. Extracorporeal membrane oxygenation for the treatment of massive pulmonary embolism. Ann Thorac Surg. 1995; 60:1801–1803
33. Pineton de Chambrun M, Bréchot N, Lebreton G, et al. Venoarterial extracorporeal membrane oxygenation for refractory cardiogenic shock post-cardiac arrest. Intensive Care Med. 2016; 42:1999–2007
34. Deehring R, Kiss AB, Garrett A, et al. Extracorporeal membrane oxygenation as a bridge to surgical embolectomy in acute fulminant pulmonary embolism. Am J Emerg Med. 2006; 24:879–880
35. Desai R, Calder M, Reber R, et al. B54 case reports in the pulmonary circulation: Complimentary role of extracorporeal membrane oxygenation therapy and ultrasound assisted catheter directed thrombolysis in management of cardiac arrest due to massive pulmonary embolism: A report of 2 cases. Am J Respir Crit Care Med. 2016; 193:1
36. DiIorio G, Goodgold HM. Lung perfusion imaging in electromechanical dissociation from massive pulmonary embolization. Clin Nucl Med. 1992; 17:818
37. Dolmatova EV, Moazzami K, Cocke TP, et al. Extracorporeal membrane oxygenation in massive pulmonary embolism. Heart Lung J Acute Crit Care. 2016; 46:106–109
38. Fernandes P, Allen P, Valdis M, et al. Successful use of extracorporeal membrane oxygenation for pulmonary embolism, prolonged cardiac arrest, post-partum: A cannulation dilemma. Perfusion. 2015; 30:106–110
39. Frickey N, Kraincuk P, Zhilla I, et al. Fulminant pulmonary embolism treated by extracorporeal membrane oxygenation in a patient with traumatic brain injury. J Trauma. 2008; 64:E41–E43
40. George B, Parazino M, Omar HR, et al. A retrospective comparison of survivors and non-survivors of massive pulmonary embolism receiving veno-arterial extracorporeal membrane oxygenation support. Resuscitation. 2018; 122:1–5
41. Giraud R, Banfi C, Siegenthaler N, et al. Massive pulmonary embolism leading to cardiac arrest: One pathology, two different ECMO modes to assist patients. J Clin Monit Comput. 2016; 30:933–937
42. Haller I, Kofler A, Lederer W, et al. Acute pulmonary artery embolism during transcatheter embolization: Successful resuscitation with veno-arterial extracorporeal membrane oxygenation. Anesth Analg. 2008; 107:945–947
43. Hashiba K, Okuda J, Maejima N, et al. Percutaneous cardiopulmonary support in pulmonary embolism with cardiac arrest. Resuscitation. 2012; 83:183–187
44. Hsieh PC, Wang SS, Ko WJ, et al. Successful resuscitation of acute massive pulmonary embolism with extracorporeal membrane oxygenation and open embolectomy. Ann Thorac Surg. 2001; 72:266–267
45. Hsieh Y, Siao F, Chiu C, et al. Massive pulmonary embolism mimicking acute myocardial infarction: Successful use of extracorporeal membrane oxygenation support as bridge to diagnosis. Heart Lung Circ. 2016; 25:e78–e80
46. Huber TC, Haskal ZJ. The role of interventional radiologists in the use of extracorporeal membranous oxygenation in the catheter-directed treatment of pulmonary embolism. J Vasc Interv Radiol. 2017; 28:945–948
47. Jeong WJ, Lee JW, Yoo YH, et al. Extracorporeal cardiopulmonary resuscitation in bedside echocardiography–diagnosed massive pulmonary embolism. Am J Emerg Med. 2015; 33:1545.e1–1545.e2
48. Kamiya H, Aubin H, Akhyari P, et al. Successful treatment of fulminant pulmonary embolism with extracorporeal life support and simultaneous systemic thrombolytic therapy after 1 h of cardiopulmonary resuscitation. Gen Thorac Cardiovasc Surg. 2015; 63:664–666
49. Kawahito K, Murata S, Adachi H, et al. Resuscitation and circulatory support using extracorporeal membrane oxygenation for fulminant pulmonary embolism. Artif Organs. 2000; 24:427–430
50. Kim YS, Choi W, Hwang J. Resuscitation of prolonged cardiac arrest from massive pulmonary embolism by extracorporeal membrane oxygenation. Eur J Cardiothorac Surg. 2017; 51:1206–1207
51. Kjærgaard B, Frost A, Rasmussen BS, et al. Extra corporeal life support makes advanced radiologic examinations and cardiac interventions possible in patients with cardiac arrest. Resuscitation. 2011; 82:623–626
52. Kurakazu M, Ueda T, Matsuo K, et al. Percutaneous cardiopulmonary support for pulmonary thromboembolism caused by large uterine leiomyomata. Taiwan J Obstet Gynecol. 2012; 51:639–642
53. Leeper WR, Valdis M, Arntfield R, et al. Extracorporeal membrane oxygenation in the acute treatment of cardiovascular collapse immediately post-partum. Interact Cardiovasc Thorac Surg. 2013; 17:898–899
54. Maggio P, Hemmila M, Haft J, et al. Extracorporeal life support for massive pulmonary embolism. J Trauma. 2007; 62:570–576
55. Maj G, Melisurgo G, De Bonis M, et al. ECLS management in pulmonary embolism with cardiac arrest: Which strategy is better? Resuscitation. 2014; 85:e175–e176
56. Misawa Y, Fuse K, Yamaguchi T, et al. Mechanical circulatory assist for pulmonary embolism. Perfusion. 2000; 15:527–529
57. Munakata R, Yamamoto T, Hosokawa Y, et al. Massive pulmonary embolism requiring extracorporeal life support treated with catheter-based interventions. Int Heart J. 2012; 53:370–374
58. Newman J, Park D, Manetta F. Extracorporeal membrane oxygenation for failed tPA therapy of pulmonary embolism. Cardiovasc Thorac Open. 2016; 2:205555201663396
59. Ornato J. Resuscitation after a massive PE: My personal experience with ED ECMO. JEMS. 2017; 42:35–37
60. Pavlovic G, Banfi C, Tassaux D, et al. Peri-operative massive pulmonary embolism management: Is veno-arterial ECMO a therapeutic option? Acta Anaesthesiol Scand. 2014; 58:1280–1286
61. Samuel D, Gressel GM, Isani S, et al. Saddle pulmonary embolus resulting in cardiovascular collapse requiring extracorporeal membrane oxygenation in a postoperative patient with endometrial cancer. Gynecol Oncol Rep. 2018; 24:36–38
62. Sharma V, Goldberg HD, Zubkus D, et al. Successful management of cardiac arrest due to pulmonary embolus using extracorporeal membrane oxygenation and ultrasound-accelerated catheter-directed thrombolysis. Ann Thorac Surg. 2016; 101:e107–e109
63. Silvetti S, Pappalardo F, Melisurgo G, et al. Ultrasound-accelerated thrombolysis and extracorporeal membrane oxygenation in a patient with massive pulmonary embolism and cardiac arrest. Circ Cardiovasc Interv. 2013; 6:e34–e36
64. Szocik J, Rudich S, Csete M. ECMO resuscitation after massive pulmonary embolism during liver transplantation. Anesthesiology. 2002; 97:763–764
65. Watanabe Y, Sakakura K, Akashi N, et al. Veno-arterial extracorporeal membrane oxygenation with conventional anticoagulation can be a best solution for shock due to massive PE. Int Heart J. 2017; 58:831–834
66. Wei J, Yang HS, Tsai SK, et al. Emergent bedside real-time three-dimensional transesophageal echocardiography in a patient with cardiac arrest following a caesarean section. Eur J Echocardiogr. 2011; 12:E16
67. Wu MY, Liu YC, Tseng YH, et al. Pulmonary embolectomy in high-risk acute pulmonary embolism: the effectiveness of a comprehensive therapeutic algorithm including extracorporeal life support. Resuscitation. 2013; 84:1365–1370
68. Belohlavek J, Rohn V, Jansa P, et al. Veno-arterial ECMO in severe acute right ventricular failure with pulmonary obstructive hemodynamic pattern. J Invasive Cardiol. 2010; 22:365–369
69. Cao J, Liu Y, Wang Y, et al. Salvage thrombolysis and extracorporeal membrane oxygenation for massive pulmonary embolism during the distal femur fracture surgery. Am J Emerg Med. 2016; 34:1189.e3–1189.e5
70. Chen J, Rosenzweir EB, Bacchetta MD, et al. D105 ICU quality and safety: Improvement opportunities: Endobronchial ultrasound for diagnosis of massive pulmonary embolism in an intubated patient requiring extracorporeal membrane oxygenation. Am J Respir Crit Care Med. 2015; 191:1
71. Swol J, Buchwald D, Strauch J, et al. Extracorporeal life support (ECLS) for cardiopulmonary resuscitation (CPR) with pulmonary embolism in surgical patients - a case series. Perfusion. 2016; 31:54–59
72. Chatterjee R, Hunninghake J, Sobieszczyk M, et al. Veno-arterial ECMO as a bridge to emergent pulmonary thrombectomy in a patient with cardiopulmonary arrest. Chest. 2019; 156:A1814–A1815
73. Connor-Schuler R, Hrabec D, Corrales JP. Cardiac arrest from massive PE in nephrotic syndrome successfully treated with embolectomy and ECMO. Respir Med Case Rep. 2018; 24:163–164
74. Das Gupta J, Saavedra R, Guliani S, et al. Decompressive laparotomy for a patient on VA-ECMO for massive pulmonary embolism that suffered traumatic liver laceration after mechanical CPR. J Surg Case Rep. 2018; 2018:rjy292
75. Dumantepe M, Okten M, Karabulut H, et al. Impact of rescue catheter-directed thrombolysis and extracorporeal membrane oxygenation during cardiopulmonary resuscitation in patients with a massive pulmonary embolism. Innovations: Technology and techniques in cardiothoracic and vascular surgery. 2018;13:S51
76. Imankulova B, Terzic M, Ukybassova T, et al. Repeated pulmonary embolism with cardiac arrest after uterine artery embolization for uterine arteriovenous malformation: A case report and literature review. Taiwan J Obstet Gynecol. 2018; 57:890–893
77. Ius F, Hoeper MM, Fegbeutel C, et al. Extracorporeal membrane oxygenation and surgical embolectomy for high-risk pulmonary embolism. Eur Respir J. 2019; 53:1801773
78. Kaese S, Lebiedz P. Extracorporeal life support after failure of thrombolysis in pulmonary embolism. Adv Respir Med. 2020; 88:13–17
79. Kagawa E, Kato M, Oda N, et al. Percutaneous thrombectomy for refractory cardiac arrest due to massive pulmonary embolism in the extracorporeal cardiopulmonary resuscitation era. Catheter Cardio Inte. 2019; 93:71
80. Kjaergaard B, Kristensen JH, Sindby JE, et al. Extracorporeal membrane oxygenation in life-threatening massive pulmonary embolism. Perfusion. 2019; 34:467–474
81. Ksela J, Knafelj R, Sostaric M, et al. Veno-arterial extracorporeal membrane oxygenation and embolectomy in massive pulmonary thromboembolism. Kardiol Pol. 2016; 74:393
82. Lee SN, Yoo KD, Jo MS. Successful endovascular management of common femoral artery perforation during cannulation for extracorporeal membrane oxygenation. Int Heart J. 2019; 60:231–234
83. Li I, Filiberti A, Mokszycki R, et al. Multiple boluses of alteplase followed by extracorporeal membrane oxygenation for massive pulmonary embolism. Am J Emerg Med. 2019; 37:1808.e5–1808.e6
84. Lauren Lindsey J, Jain R, Vachharajani V. Catheter directed thrombolysis combined with ECMO for massive pulmonary emboli. Respir Med Case Rep. 2018; 25:6–8
85. Lupei MI, Kloesel B, Trillos L, et al. Survival of intraoperative massive pulmonary embolism using alteplase and VA-ECMO. J Clin Anesth. 2019; 57:112
86. Mandigers L, Scholten E, Rietdijk WJR, et al. Survival and neurological outcome with extracorporeal cardiopulmonary resuscitation for refractory cardiac arrest caused by massive pulmonary embolism: A two center observational study. Resuscitation. 2019; 136:8–13
87. Miyazaki K, Hikone M, Kuwahara Y, et al. Extracorporeal CPR for massive pulmonary embolism in a “hybrid 2136 emergency department”. Am J Emerg Med. 2019; 37:2132–2135
88. Moon D, Lee SN, Yoo KD, et al. Extracorporeal membrane oxygenation improved survival in patients with massive pulmonary embolism. Ann Saudi Med. 2018; 38:174–180
89. Oh YN, Oh DK, Koh Y, et al. Use of extracorporeal membrane oxygenation in patients with acute high-risk pulmonary embolism: A case series with literature review. Acute Crit Care. 2019; 34:148–154
90. Okoronkwo TE, Zhang X, Dworet J, et al. Early detection and management of massive intraoperative pulmonary embolism in a patient undergoing repair of a traumatic acetabular fracture. Case Rep Anesthesiol. 2018; 2018:7485789
91. Russ A, Payne N, Bonnell M, et al. Use of extracorporeal membrane oxygenation and surgical embolectomy for massive pulmonary embolism in the emergency department. J Emerg Med. 2017; 53:708–711
92. Stefaniak S, Puślecki M, Ligowski M, et al. Venoarterial extracorporeal membrane oxygenation in massive pulmonary embolism. Kardiol Pol. 2018; 76:931
93. Takacs ME, Damisch KE. Extracorporeal life support as salvage therapy for massive pulmonary embolus and cardiac arrest in pregnancy. J Emerg Med. 2018; 55:121–124
94. Thind GS, Hanane T, Bribriesco A, et al. Extracorporeal cardiopulmonary resuscitation in a patient with fulminant pulmonary embolism refractory to intraarrest thrombolysis. Perfusion. 2020; 35:163–165
95. Wu XY, Zhuang ZQ, Zheng RQ, et al. Extracorporeal membrane oxygenation as salvage therapy for acute massive pulmonary embolism after surgery for tibiofibular fractures. Chin Med J (Engl). 2018; 131:2611–2613
96. Kaatz S, Ahmad D, Spyropoulos AC, et al. Definition of clinically relevant non-major bleeding in studies of anticoagulants in atrial fibrillation and venous thromboembolic disease in non-surgical patients: Communication from the SSC of the ISTH. J Thromb and Haemost. 2015; 13:2119–2126
97. Cheng R, Hachamovitch R, Kittleson M, et al. Complications of extracorporeal membrane oxygenation for treatment of cardiogenic shock and cardiac arrest: A meta-analysis of 1,866 adult patients. Ann Thorac Surg. 2014; 97:610–616
98. Stub D, Bernard S, Pellegrino V, et al. Refractory cardiac arrest treated with mechanical CPR, hypothermia, ECMO and early reperfusion (the CHEER trial). Resuscitation. 2015; 86:88–94
99. Pasrija C, Kronfli A, George P, et al. Utilization of veno-arterial extracorporeal membrane oxygenation for massive pulmonary embolism. Ann Thorac Surg. 2018; 105:498–504
100. Sakuma M, Nakamura M, Yamada N, et al. Percutaneous cardiopulmonary support for the treatment of acute pulmonary embolism: Summarized review of the literature in Japan including our own experience. Ann Vasc Dis. 2009; 2:7–16
Keywords:

extracorporeal membrane oxygenation/methods; heart arrest/etiology; heart arrest/therapy; pulmonary embolism/complications; pulmonary embolism/therapy; thrombolytic therapy; treatment outcome

Supplemental Digital Content

Copyright © 2021 by the Society of Critical Care Medicine and Wolters Kluwer Health, Inc. All Rights Reserved.