Transoesophageal echocardiography in cardiac arrest: A systematic review

      Abstract

      Aims

      To identify, appraise and synthesize all available clinical evidence to evaluate the diagnostic role of transoesophageal echocardiography (TEE) during resuscitation of in-hospital (IHCA) and out-of-hospital cardiac arrest (OHCA) in the identification of reversible causes of cardiac arrest and cardiac contractility.

      Methods

      We conducted a systematic review following PRISMA guidelines. Medline, EMBASE, Web of Science Core Collection, Proquest Dissertations, Open Grey, CDSR, Cochrane Central, Cochrane Clinical Answers, and the clinicaltrials.gov registry were searched for eligible studies. Studies involving adult patients, with non-traumatic cardiac arrest in whom TEE was used for intra-arrest evaluation, were included. Case studies and case series, animal studies, reviews, guidelines and editorials were excluded. The QUADAS-2 tool was used for quality assessment of all studies.

      Results

      Eleven studies with a total of 358 patients were included. Four studies involved perioperative IHCA, three involved OHCA, and four were mixed population settings. Overall, the risk of bias in the selected studies was either high or unclear due to evidence or lack of information. In all 11 studies, TEE allowed the identification of reversible causes of arrest. We found significant heterogeneity in the criteria used to interpret findings, TEE protocol used, and timing of TEE.

      Conclusion

      Due to heterogeneity of studies, small sample size and inconsistent reference standard, the evidence for TEE in cardiac arrest resuscitation is of low certainty and is affected by a high risk of bias. Further studies are needed to better understand the true diagnostic accuracy of TEE in identifying reversible causes of arrest and cardiac contractility.

      Keywords

      Introduction

      Cardiac arrest is one of the leading causes of death and disability worldwide, with out-of-hospital (OHCA) affecting over 350,000 individuals and in-hospital cardiac arrest (IHCA) occurring in over 290,000 patients each year in the United States alone.
      • Holmberg M.J.
      • Ross C.E.
      • Fitzmaurice G.M.
      • et al.
      American Heart Association’s Get With The Guidelines-Resuscitation Investigators. Annual Incidence of Adult and Pediatric In-Hospital Cardiac Arrest in the United States.
      • Virani S.S.
      • Alonso A.
      • Benjamin E.J.
      • et al.
      American Heart Association Council on Epidemiology and Prevention Statistics Committee and Stroke Statistics Subcommittee. Heart Disease and Stroke Statistics-2020 Update: A Report From the American Heart Association.
      Overall survival rate of OHCA and IHCA to hospital discharge is 10.4% and 25.8% respectively.
      • Virani S.S.
      • Alonso A.
      • Benjamin E.J.
      • et al.
      American Heart Association Council on Epidemiology and Prevention Statistics Committee and Stroke Statistics Subcommittee. Heart Disease and Stroke Statistics-2020 Update: A Report From the American Heart Association.
      Despite advances in cardiac arrest recognition and management, survival with good neurological outcomes remains low.
      • Berg K.M.
      • Soar J.
      • Andersen L.W.
      • et al.
      Adult Advanced Life Support Collaborators. Adult Advanced Life Support: 2020 International Consensus on Cardiopulmonary Resuscitation and Emergency Cardiovascular Care Science With Treatment Recommendations.
      The core of cardiopulmonary resuscitation (CPR) is centred around the rapid identification of reversible causes of arrest and the optimisation of coronary and cerebral perfusion.
      • Berg K.M.
      • Soar J.
      • Andersen L.W.
      • et al.
      Adult Advanced Life Support Collaborators. Adult Advanced Life Support: 2020 International Consensus on Cardiopulmonary Resuscitation and Emergency Cardiovascular Care Science With Treatment Recommendations.
      In the 1980s, point of care ultrasound (PoCUS) emerged as a valuable adjunct to clinical assessment during resuscitation. Over the past four decades, the application of PoCUS in the evaluation of cardiac arrest has expanded significantly and has been established as a core skill by many international societies.
      • Maconochie I.K.
      • Bingham R.
      • Eich C.
      • et al.
      European Resuscitation Council Guidelines for Resuscitation 2015.
      • Labovitz A.J.
      • Noble V.E.
      • Bierig M.
      • et al.
      Focused cardiac ultrasound in the emergent setting: a consensus statement of the American Society of Echocardiography and American College of Emergency Physicians.
      Echocardiography can aid in identifying reversible causes of arrest, such as pericardial tamponade and pulmonary embolism (PE).
      • Labovitz A.J.
      • Noble V.E.
      • Bierig M.
      • et al.
      Focused cardiac ultrasound in the emergent setting: a consensus statement of the American Society of Echocardiography and American College of Emergency Physicians.
      While transthoracic echocardiography (TTE) can provide valuable diagnostic information in cardiac arrest patients, there are important limitations to this modality. Factors such as defibrillation pads, automated compression devices, obesity, gastric insufflation, and subcutaneous emphysema can challenge the acquisition of interpretable images.
      • Blaivas M.
      Transesophageal echocardiography during cardiopulmonary arrest in the emergency department.
      Observational studies have suggested that the use of TTE may lead to delays in chest compressions.
      • Huis in 't Veld M.A.
      • Allison M.G.
      • Bostick D.S.
      • et al.
      Ultrasound use during cardiopulmonary resuscitation is associated with delays in chest compressions.
      • Reed M.
      • Gibson L.
      • Dewar A.
      • Short S.
      • Black P.
      • Clegg G.
      Introduction of paramedic led Echo in Life Support into the pre-hospital environment: The PUCA study.
      • Clattenburg E.J.
      • Wroe P.
      • Brown S.
      • et al.
      Point-of-care ultrasound use in patients with cardiac arrest is associated prolonged cardiopulmonary resuscitation pauses: a prospective cohort study.
      Transoesophageal echocardiography (TEE) can overcome many of the limitations of TTE.
      • Blaivas M.
      Transesophageal echocardiography during cardiopulmonary arrest in the emergency department.
      • Fair J.
      • Mallin M.
      • Mallemat H.
      • Zimmerman J.
      • et al.
      Transesophageal echocardiography: guidelines for point-of-care applications in cardiac arrest resuscitation.
      In addition to its diagnostic role, studies have suggested that TEE has unique advantages including the potential to optimize the quality of chest compressions, shorten CPR interruptions, and guide resuscitative procedures.
      • Fair J.
      • Mallin M.
      • Mallemat H.
      • Zimmerman J.
      • et al.
      Transesophageal echocardiography: guidelines for point-of-care applications in cardiac arrest resuscitation.
      • Teran F.
      • Prats M.I.
      • Nelson B.P.
      • et al.
      Focused transesophageal echocardiography during cardiac arrest resuscitation: JACC review topic of the week.
      • Anderson K.L.
      • Castaneda M.G.
      • Boudreau S.M.
      • Sharon D.J.
      • Bebarta V.S.
      Left ventricular compressions improve hemodynamics in a swine model of out-of-hospital cardiac arrest.
      • Kim Y.W.
      • Cha K.-C.
      • Kim Y.S.
      • et al.
      Kinetic analysis of cardiac compressions during cardiopulmonary resuscitation.
      • Fair J.
      • Tonna J.
      • Ockerse P.
      • Galovic B.
      • et al.
      Emergency physician-performed transesophageal echocardiography for extracorporeal life support vascular cannula placement.
      Transoesophageal echocardiography also provides continuous imaging throughout resuscitation, allowing for real-time visualization of the heart during CPR.
      In 2017, the first guidelines on TEE in cardiac arrest were established and subsequently endorsed by the American College of Emergency Physicians (ACEP).
      • Labovitz A.J.
      • Noble V.E.
      • Bierig M.
      • et al.
      Focused cardiac ultrasound in the emergent setting: a consensus statement of the American Society of Echocardiography and American College of Emergency Physicians.
      • Fair J.
      • Mallin M.
      • Mallemat H.
      • Zimmerman J.
      • et al.
      Transesophageal echocardiography: guidelines for point-of-care applications in cardiac arrest resuscitation.
      The proposed applications of TEE in cardiac arrest included the characterization of myocardial activity, gross assessment of left-sided systolic function, assessment for right ventricular enlargement, intravascular volume status, and identification of pericardial effusion. Studies in the emergency department and intensive care setting have shown that emergency and critical care physicians with prior competency in TTE, can successfully perform focused TEE following a structured simulation-based training program.
      • Arntfield R.
      • Pace J.
      • McLeod S.
      • Granton J.
      • Hegazy A.
      • Lingard L.
      Focused transesophageal echocardiography for emergency physicians—description and results from simulation training of a structured four-view examination.
      • Chenkin J.
      • Atzema C.L.
      Contemporary application of point-of-care echocardiography in the emergency department.
      A large body of evidence, as reflected in a recent systematic review and meta-analysis, has described the clinical impact of TTE in cardiac arrest resuscitation, both as a prognostic tool and for the identification of potentially reversible causes of arrest.
      • Lalande E.
      • Burwash-Brennan T.
      • Burns K.
      • et al.
      SHoC Investigators. Is point-of-care ultrasound a reliable predictor of outcome during atraumatic, non-shockable cardiac arrest? A systematic review and meta-analysis from the SHoC investigators.
      However, we are unaware of a systematic review of the literature involving TEE during cardiac arrest resuscitation.
      The aim of this review is to evaluate the diagnostic role of TEE in identifying clinically significant findings during cardiac arrest. The review question was formulated using the PICOST format:
      • Population: adult patients with in-hospital (IHCA) and out-of-hospital cardiac arrest (OHCA);
      • Intervention: TEE and standard resuscitation;
      • Comparative: standard resuscitation;
      • Outcome: identification of reversible causes of cardiac arrest and cardiac contractility;
      • Study type: all study types except for case studies and case series, animal studies, review articles, guidelines and editorials;
      • Time: during cardiopulmonary resuscitation.
      Secondary objective is to identify any reported adverse events secondary to TEE use in cardiac arrest in the included papers.

      Methods

       Registration

      The systematic review protocol was registered with OSF Open Registries Network.

      OSF Open Registries Network. Registration link; https://osf.io/k7wah [accessed March 5, 2021].

      No registered related protocols were found on PROSPERO and Cochrane database for systematic reviews. The review is reported in accordance with the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) guidelines.
      • Moher D.
      • Liberati A.
      • Tetzlaff J.
      • et al.
      PRISMA Group. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement.

       Search strategy

      The search strategy was designed by first author (LH) and librarian (NA) using subject headings and free-text terms derived from the PICOST question. The outcome measures were not used as search terms. The comprehensive literature search was conducted on March 25th, 2020 by a librarian (NA) and peer-reviewed by (MB). The search was repeated using the same terms on October 6th, 2020. The following databases were searched: MEDLINE, EMBASE, and The Cochrane Library (CDSR, Cochrane Central, and Cochrane Clinical Answers). Grey literature search was conducted using clinicaltrials.gov, OpenGrey, Web of Science Core Collection, and Proquest Dissertations. An additional search was conducted by manually scanning references of all the selected studies. No language or publication period limitations were applied to eliminate bias. Several authors and experts in the field of TEE were contacted through correspondence to identify any ongoing trials. Rayyan QCRI (Qatar Computing Research Institute) web tool for systematic reviews was used to save and manage the search results.
      • Ouzzani M.
      • Hammady H.
      • Fedorowicz Z.
      • et al.
      Rayyan-a web and mobile app for systematic reviews.
      Duplicates identified by the web tool were manually reviewed. The search strategy can be found in Appendix 1.

       Study selection

      The eligibility criteria for study selection were: (1) studies involving adult patients (≥18 years old) with IHCA or OHCA; (2) TEE was used during resuscitation; (3) study should include diagnostic role of TEE in identification of causes of arrest or assessing cardiac contractility; (4) study type should include observational (prospective and retrospective) and interventional studies. Studies involving pediatric or traumatic arrest population, those where TEE was used exclusively after ROSC (post-arrest) were excluded. Case studies and case series, animal studies, review articles, guidelines and editorials were excluded (Table 1).
      Table 1Eligibility criteria for study selection.
      InclusionExclusion
      PopulationAdult patients ≥ 18 years with IHCA or OHCATraumatic arrest and pediatric patients
      InterventionTEE used during resuscitationTEE used after ROSC has been achieved
      OutcomePrimary Outcome

      Diagnostic ability of TEE to identify reversible causes of arrest and evaluate cardiac contractility

      Secondary Outcome

      Identify number and type of adverse events associated with TEE in cardiac arrest
      Study DesignRetrospective/Prospective/Randomised controlled studies/observational studies.

      Studies in any language that have been published in a peer reviewed journal, dissertation abstracts, forums or any sort of conference proceeding
      Case studies and case series

      Animal Studies

      Reviews

      Guidelines

      Editorial letters
      Abbreviations: CPR: Cardio-Pulmonary Resuscitation, IHCA: In-hospital cardiac arrest, ROSC: Return of spontaneous circulation, OHCA: Out-of-hospital cardiac arrest, TEE: Transoesophegeal echocardiography.
      The first selection of studies was completed by one investigator by reviewing the study title and abstract against the eligibility criteria. Two independent investigators conducted the second selection by reviewing the full text against the eligibility criteria. When disagreement occurred between two investigators, a third investigator was involved to reach a conclusion. The agreement among the investigators was substantial, where calculated inter-rater reliability represented by Cohen’s Kappa (κ) was 0.71. Inter-rater reliability for each pair of investigators, (AB/TJ) and (LH/AR), was 0.69 and 0.71 respectively. The secondary selection utilised a template to unify the process across investigators and improve the validity and reproducibility of the results (Appendix 2). The studies not meeting eligibility criteria in the secondary search were recorded and summarized (Appendix 3). The results of the study selection were recorded using the PRISMA flow diagram.
      • Lalande E.
      • Burwash-Brennan T.
      • Burns K.
      • et al.
      SHoC Investigators. Is point-of-care ultrasound a reliable predictor of outcome during atraumatic, non-shockable cardiac arrest? A systematic review and meta-analysis from the SHoC investigators.
      Where data were missing, authors were contacted in an attempt to obtain further clarification before exclusion. The investigators also communicated with authors in an attempt to find further subgroup analysis but results could not be segregated in a meaningful way. Similarly, authors were contacted in the situations where TTE and TEE data, or shock and cardiac arrest data were pooled together, in an attempt to obtain results of TEE alone.

       Data extraction and quality assessment

      The data extraction process and quality assessment were conducted by five investigators (LH, MA, TJ, AB, FT). The data extraction form was adopted from the Center of Reviews and Dissemination template.

      Systematic reviews, Centre for Reviews and Dissemination, University of York, York, 2009. https://www.york.ac.uk/media/crd/Systematic_Reviews.pdf [accessed May 7, 2020].

      The variables extracted were based on the PICO format and included general study characteristics, inclusion and exclusion criteria, operator skills, TEE views obtained, reference standard, and outcomes. A standardized data extraction form was developed, piloted and then refined with input from all coinvestigators (Appendix 4). Each study was reviewed by two investigators independently. Investigators then compared their results and confirmed no relevant information was missed or misinterpreted. The QUADAS-2 tool was used for quality assessment.
      • Whiting P.F.
      • Rutjes A.W.
      • Westwood M.E.
      • et al.
      QUADAS-2 Group. QUADAS-2: a revised tool for the quality assessment of diagnostic accuracy studies.
      Each study was independently evaluated by two investigators, and any discrepancy was discussed among them. Funding sources were not included as a variable.

       Data synthesis

      Due to the heterogeneity of the studies, the feasibility of conducting a robust meta-analysis was not possible. A narrative synthesis was used to present the study results.

      Results

       Literature search and study selection results

      The first literature search identified 6551 results and the subsequent second search found an additional 374 studies. After duplicates were removed, 5243 titles were screened for inclusion with 5164 excluded for not meeting study criteria. Of the 79 remaining studies that underwent a thorough full-text review, 11 studies were selected for final review (Fig. 1).
      • Teran F.
      • Dean A.J.
      • Centeno C.
      • et al.
      Evaluation of out-of-hospital cardiac arrest using transesophageal echocardiography in the emergency department.
      • Kim Y.W.
      • Jung W.J.
      • Cha K.C.
      • et al.
      Diagnosis of aortic dissection by transesophageal echocardiography during cardiopulmonary resuscitation.
      • Jung W.J.
      • Cha K.C.
      • Kim Y.W.
      • et al.
      Intra-arrest transoesophageal echocardiographic findings and resuscitation outcomes.
      • Lin T.
      • Chen Y.
      • Lu C.
      • et al.
      Use of transoesophageal echocardiography during cardiac arrest in patients undergoing elective non-cardiac surgery.
      • Memtsoudis S.G.
      • Rosenberger P.
      • Loffler M.
      • et al.
      The usefulness of transesophageal echocardiography during intraoperative cardiac arrest in noncardiac surgery.
      • Shillcutt S.K.
      • Markin N.W.
      • Montzingo C.R.
      • et al.
      Use of rapid “rescue” perioperative echocardiography to improve outcomes after hemodynamic instability in noncardiac surgical patients.
      • Hilberath J.N.
      • Burrage P.S.
      • Shernan S.K.
      • et al.
      Rescue transoesophageal echocardiography for refractory haemodynamic instability during transvenous lead extraction.
      • Varriale P.
      • Maldonado J.M.
      Echocardiographic observations during in hospital cardiopulmonary resuscitation.
      • van der Wouw P.A.
      • Koster R.W.
      • Delemarre B.J.
      • et al.
      Diagnostic accuracy of transesophageal echocardiography during cardiopulmonary resuscitation.
      • Comess K.A.
      • DeRook F.A.
      • Russell M.L.
      • et al.
      The incidence of pulmonary embolism in unexplained sudden cardiac arrest with pulseless electrical activity.
      • Miyake M.
      • Izumi C.
      • Takahashi S.
      • et al.
      Efficacy of transesophageal echocardiography in patients with cardiac arrest or shock.
      One study was excluded as the data from traumatic and nontraumatic arrests were pooled together. Two studies were excluded as they were conference abstracts. Disagreement in decision occurred on 7 studies and was resolved by involving a third investigator in the review. Japanese and Spanish language translation was used in two studies with native speakers with research and subject matter familiarity.

       Study characteristics

      A population of 358 patients were studied in the 11 selected studies. Three studies were conducted in the ED setting and included only OHCA.
      • Teran F.
      • Dean A.J.
      • Centeno C.
      • et al.
      Evaluation of out-of-hospital cardiac arrest using transesophageal echocardiography in the emergency department.
      • Kim Y.W.
      • Jung W.J.
      • Cha K.C.
      • et al.
      Diagnosis of aortic dissection by transesophageal echocardiography during cardiopulmonary resuscitation.
      • Jung W.J.
      • Cha K.C.
      • Kim Y.W.
      • et al.
      Intra-arrest transoesophageal echocardiographic findings and resuscitation outcomes.
      Four studies have involved patients with IHCA in the operating theatre during elective or emergent procedures.
      • Lin T.
      • Chen Y.
      • Lu C.
      • et al.
      Use of transoesophageal echocardiography during cardiac arrest in patients undergoing elective non-cardiac surgery.
      • Memtsoudis S.G.
      • Rosenberger P.
      • Loffler M.
      • et al.
      The usefulness of transesophageal echocardiography during intraoperative cardiac arrest in noncardiac surgery.
      • Shillcutt S.K.
      • Markin N.W.
      • Montzingo C.R.
      • et al.
      Use of rapid “rescue” perioperative echocardiography to improve outcomes after hemodynamic instability in noncardiac surgical patients.
      • Hilberath J.N.
      • Burrage P.S.
      • Shernan S.K.
      • et al.
      Rescue transoesophageal echocardiography for refractory haemodynamic instability during transvenous lead extraction.
      The remaining four studies aggregated data from both IHCA and OHCA presentations.
      • Varriale P.
      • Maldonado J.M.
      Echocardiographic observations during in hospital cardiopulmonary resuscitation.
      • van der Wouw P.A.
      • Koster R.W.
      • Delemarre B.J.
      • et al.
      Diagnostic accuracy of transesophageal echocardiography during cardiopulmonary resuscitation.
      • Comess K.A.
      • DeRook F.A.
      • Russell M.L.
      • et al.
      The incidence of pulmonary embolism in unexplained sudden cardiac arrest with pulseless electrical activity.
      • Miyake M.
      • Izumi C.
      • Takahashi S.
      • et al.
      Efficacy of transesophageal echocardiography in patients with cardiac arrest or shock.
      The characteristics of the 11 included studies are summarised in Table 2.
      Table 2Summary of included studies.

       Assessment of risk of bias and applicability

      The risk of bias was unclear in 55% (6/11) of studies related to lack of information regarding patient selection, description of index test (TEE), and the flow and timing of TEE. The risk of bias was high in 36% (4/11) in regards to patient selection and flow and timing of TEE. Major sources of risk of bias were due to enrollment of convenience sample of patients (or lack of specification regarding consecutive sampling), variation in the criteria used for diagnostic assessment, lack of blinding or uncertainty regarding if outcome evaluators were blinded to TEE findings, evidence of lack of control or uncertainty regarding control for known prognostic variables such as downtime, bystander CPR, pre-hospital interventions (OHCA), chest compression quality, drug administration, resuscitation length and resuscitation-time bias, and airway management. The risk of bias for applicability was low for patient selection (55%; 6/11) and index testing (73%; 8/11) in most studies. The results of quality assessment for all the studies are summarized in Table 3.
      Table 3Quality assessment by QUADAS-2 criteria.

       Diagnostic findings of TEE

      In all 11 studies, TEE allowed the identification of reversible causes of arrest in 148 of 358 patients (41%). Commonly reported intra-arrest diagnostic findings of TEE included the presence of pericardial effusion and cardiac tamponade in 21 patients, pulmonary embolism in 43 patients, hypovolemia in 5, and aortic dissection in 41 patients. Additional TEE findings reported are fine ventricular fibrillation, left ventricular dysfunction, intracardiac thrombus, papillary muscle rupture, and presence of “coalescent echocardiographic contrast”. Reported TEE findings in each study are summarised in Table 4.
      Table 4TEE findings in cardiac arrest.
      StudyNPEADTampMIHypovolemiaFine VFOther findings
      N[%]N[%]N[%]N[%]N[%]N[%]N[%]
      Teran 2019212[9.5]----3[14.2]Intracardiac thrombus 1[4.7],

      LV dysfunction 21[100],

      obstructive shock 3[14.2]
      Kim 2020455[11]10[2]2[4.4]---
      Jung 20201588[5]19[12]4[2.5]---Intracardiac thrombi 9[5.7]
      Lin 2006102[20]--5[50]1[10]-
      Memtsoudis 2006229[40]-2[9]6[27]2[9]-
      Shillcutt 201242[50]---1[25]-LV dysfunction 1[25]
      Hilberath 20146--5[83]---
      Varriale 199741[25]--1[25]1[25]-Coalescent echo contrast 3[75]
      van der Wouw 1997486[12.5]6[12.5]6[12.5]21[43.7]--Papillary muscle rupture 6[12.5]
      Comess 2000368[22]2[5.5]02[5.5]--Ventricular dysfunction 11[30.5]
      Miyaki 20044-4[100]2[50]---Pleural effusion with aortic dissection 2[50]
      Abbreviations: AD: Aortic dissection, LV: Left ventricle, MI: Myocardial infarction, PE: Pulmonary embolism, Tamp: pericardial tamponade, VF: Ventricular fibrillation.

       Complications associated with TEE

      Only one study reported the absence of any adverse events related to TEE.
      • Comess K.A.
      • DeRook F.A.
      • Russell M.L.
      • et al.
      The incidence of pulmonary embolism in unexplained sudden cardiac arrest with pulseless electrical activity.
      Several authors reported successful insertion of TEE and adequate image acquisition in all patients.
      • Teran F.
      • Dean A.J.
      • Centeno C.
      • et al.
      Evaluation of out-of-hospital cardiac arrest using transesophageal echocardiography in the emergency department.
      • van der Wouw P.A.
      • Koster R.W.
      • Delemarre B.J.
      • et al.
      Diagnostic accuracy of transesophageal echocardiography during cardiopulmonary resuscitation.
      • Comess K.A.
      • DeRook F.A.
      • Russell M.L.
      • et al.
      The incidence of pulmonary embolism in unexplained sudden cardiac arrest with pulseless electrical activity.
      In the study by Teran et al., 7 patients received external defibrillation while the TEE probe was in place and held by the operator. No adverse events were reported during delivery of shock.
      • Teran F.
      • Dean A.J.
      • Centeno C.
      • et al.
      Evaluation of out-of-hospital cardiac arrest using transesophageal echocardiography in the emergency department.

      Discussion

      Despite decades of clinical use of TEE in perioperative, emergency and critical care settings, only 11 studies have evaluated the use of TEE to identify reversible causes of cardiac arrest and assessing cardiac contractility during CPR.
      • Teran F.
      • Dean A.J.
      • Centeno C.
      • et al.
      Evaluation of out-of-hospital cardiac arrest using transesophageal echocardiography in the emergency department.
      • Kim Y.W.
      • Jung W.J.
      • Cha K.C.
      • et al.
      Diagnosis of aortic dissection by transesophageal echocardiography during cardiopulmonary resuscitation.
      • Jung W.J.
      • Cha K.C.
      • Kim Y.W.
      • et al.
      Intra-arrest transoesophageal echocardiographic findings and resuscitation outcomes.
      • Lin T.
      • Chen Y.
      • Lu C.
      • et al.
      Use of transoesophageal echocardiography during cardiac arrest in patients undergoing elective non-cardiac surgery.
      • Memtsoudis S.G.
      • Rosenberger P.
      • Loffler M.
      • et al.
      The usefulness of transesophageal echocardiography during intraoperative cardiac arrest in noncardiac surgery.
      • Shillcutt S.K.
      • Markin N.W.
      • Montzingo C.R.
      • et al.
      Use of rapid “rescue” perioperative echocardiography to improve outcomes after hemodynamic instability in noncardiac surgical patients.
      • Hilberath J.N.
      • Burrage P.S.
      • Shernan S.K.
      • et al.
      Rescue transoesophageal echocardiography for refractory haemodynamic instability during transvenous lead extraction.
      • Varriale P.
      • Maldonado J.M.
      Echocardiographic observations during in hospital cardiopulmonary resuscitation.
      • van der Wouw P.A.
      • Koster R.W.
      • Delemarre B.J.
      • et al.
      Diagnostic accuracy of transesophageal echocardiography during cardiopulmonary resuscitation.
      • Comess K.A.
      • DeRook F.A.
      • Russell M.L.
      • et al.
      The incidence of pulmonary embolism in unexplained sudden cardiac arrest with pulseless electrical activity.
      • Miyake M.
      • Izumi C.
      • Takahashi S.
      • et al.
      Efficacy of transesophageal echocardiography in patients with cardiac arrest or shock.
      In this systematic review, TEE performed during cardiac arrest found diagnostic findings in near one-half of the patients, however there was significant clinical heterogeneity among studies, relatively small sample sizes, and a high risk of bias that limit the interpretation of the findings. Together our findings indicate that overall, current evidence investigating the effects of TEE in cardiac arrest resuscitation is of low certainty.
      One of the central arguments for the incorporation of TEE in cardiac arrest is its unique capability to visualize the heart in real-time during resuscitation, making it an ideal diagnostic modality to identify important and potentially reversible causes of arrest such as cardiac tamponade. With better image quality and the ability to visualize the heart throughout ongoing chest compressions, TEE should theoretically provide the best diagnostic opportunity to make these diagnoses during resuscitation.
      Among the total of 358 patients included in this review, diagnosis of PE was the most commonly reported finding. However, heterogeneity was notable among studies in their diagnostic criteria for this entity. Transoesophageal echocardiography can only identify indirect signs of PE, such as right ventricular dilatation or thrombus in the right side of the heart or proximal segments of the pulmonary arteries. Such variation in the criteria used to make this diagnosis makes the prevalence found of low certainty, particularly in light of pre-clinical and clinical evidence indicating that right ventricular dilatation is a common finding during the intra-arrest phase of resuscitation among cardiac arrest patients in the absence of PE.
      • Aagaard R.
      • Caap P.
      • Hansson N.C.
      • Bøtker M.T.
      • Granfeldt A.
      • Løfgren B.
      Detection of Pulmonary Embolism During Cardiac Arrest-Ultrasonographic Findings Should Be Interpreted With Caution.
      • Aagaard R.
      • Granfeldt A.
      • Bøtker M.T.
      • Mygind-Klausen T.
      • Kirkegaard H.
      • Løfgren B.
      The right ventricle is dilated during resuscitation from cardiac arrest caused by hypovolemia: a porcine ultrasound study.
      • Wardi G.
      • Blanchard D.
      • Dittrich T.
      • Kaushal K.
      • Sell R.
      Right ventricle dysfunction and echocardiographic parameters in the first 24h following resuscitation in the post-cardiac arrest patient: A retrospective cohort study.
      Determining the sensitivity and specificity of the individual or a combination of TEE findings suggesting PE during cardiac arrest has important potential implications for resuscitative care. Until now, the use of thrombolytics during cardiac arrest has failed to show an improvement of outcomes when given to the unselected population of cardiac arrest patients.
      • Böttiger B.W.
      • Arntz H.R.
      • Chamberlain D.A.
      • et al.
      TROICA Trial Investigators; European Resuscitation Council Study Group. Thrombolysis during resuscitation for out-of-hospital cardiac arrest.
      The potential of TEE to help identify the sub-ground of cardiac arrest patients with a confirmed or high likelihood of PE, could help better direct the use of thrombolytic therapies. Furthermore, with the expanding availability of extracorporeal cardiopulmonary resuscitation (ECPR), TEE could be a key diagnostic tool to identify patients who may benefit from ECPR as a bridge to thrombectomy.
      The largest prospective study evaluating TTE in cardiac arrest showed that cardiac tamponade is the most prevalent reversible cause and that early treatment is associated with higher SHD.
      • Gaspari R.
      • Weekes A.
      • Adhikari S.
      • et al.
      Emergency department point-of-care ultrasound in out-of-hospital and in-ED cardiac arrest.
      In this systematic review we confirmed those findings with higher survival to hospital discharge identified in patients with cardiac tamponade in the perioperative subgroup.
      • Memtsoudis S.G.
      • Rosenberger P.
      • Loffler M.
      • et al.
      The usefulness of transesophageal echocardiography during intraoperative cardiac arrest in noncardiac surgery.
      • Hilberath J.N.
      • Burrage P.S.
      • Shernan S.K.
      • et al.
      Rescue transoesophageal echocardiography for refractory haemodynamic instability during transvenous lead extraction.
      Cardiac tamponade can only be identified with echocardiography during cardiac arrest, and therefore the rationale for its use in resuscitation is evident. The comparative diagnostic performance between TTE and TEE for the diagnosis of this entity remains to be established.
      Patients presenting in cardiac arrest caused by an aortic dissection are known to have very high mortality.
      • Meron Giora
      • Kürkciyan Istepan
      • Sterz Fritz
      • et al.
      Non-traumatic aortic dissection or rupture as cause of cardiac arrest: presentation and outcome.
      In this review, none of the patients reported with aortic dissection survived to hospital discharge. Identification of aortic dissection on TEE may be helpful in both the identification of potentially salvageable patients as well as an adjunct in the decision to discontinue resuscitation in patients who are unlikely to be resuscitated, thus avoiding futile interventions.
      Several studies have included myocardial infarction as an identifiable cause of arrest.
      • Lin T.
      • Chen Y.
      • Lu C.
      • et al.
      Use of transoesophageal echocardiography during cardiac arrest in patients undergoing elective non-cardiac surgery.
      • Memtsoudis S.G.
      • Rosenberger P.
      • Loffler M.
      • et al.
      The usefulness of transesophageal echocardiography during intraoperative cardiac arrest in noncardiac surgery.
      • Varriale P.
      • Maldonado J.M.
      Echocardiographic observations during in hospital cardiopulmonary resuscitation.
      • van der Wouw P.A.
      • Koster R.W.
      • Delemarre B.J.
      • et al.
      Diagnostic accuracy of transesophageal echocardiography during cardiopulmonary resuscitation.
      • Comess K.A.
      • DeRook F.A.
      • Russell M.L.
      • et al.
      The incidence of pulmonary embolism in unexplained sudden cardiac arrest with pulseless electrical activity.
      However, TEE can only identify wall motion abnormality in the presence of cardiac activity. In most situations, diagnosis of myocardial infarction relies on the presence of ischemic changes on echocardiogram or raised cardiac biomarkers. Furthermore, TEE cannot differentiate if wall motion abnormality is the underlying cause of arrest or the result of hypoperfusion during an arrest. Transoesophageal echocardiography may be of benefit in patients with ROSC in the absence of ischemic electrocardiographic findings of acute myocardial infarction.
      Certain cases of fine VF may be indistinguishable from asystole on cardiac monitors. This has led to the proposal of TEE as a tool to enhance the recognition of this rhythm. In one study fine VF was observed in three patients who were thought to be in asystole based on an electrocardiographic tracing.
      • Teran F.
      • Dean A.J.
      • Centeno C.
      • et al.
      Evaluation of out-of-hospital cardiac arrest using transesophageal echocardiography in the emergency department.
      Subsequently all three patients received defibrillation. Further studies are needed to confirm these findings and characterize the impact of identification and defibrillation of these patients.
      Given the high quality of images and its ability to provide continuous live images throughout the resuscitation, TEE has been proposed as an ideal tool to characterize the changes in myocardial contractility intra-arrest. In two studies, eight patients were found to have organized ventricular contractions on TEE with no detectable pulse on manual palpation.
      • Teran F.
      • Dean A.J.
      • Centeno C.
      • et al.
      Evaluation of out-of-hospital cardiac arrest using transesophageal echocardiography in the emergency department.
      • Varriale P.
      • Maldonado J.M.
      Echocardiographic observations during in hospital cardiopulmonary resuscitation.
      This state has been previously described as pseudo-PEA.
      • Paradis N.A.
      • Martin G.B.
      • Goetting M.G.
      • Rivers E.P.
      • Feingold M.
      • Nowak R.M.
      Aortic pressure during human cardiac arrest. Identification of pseudo-electromechanical dissociation.
      • Gaspari R.
      • Weekes A.
      • Adhikari S.
      • et al.
      A retrospective study of pulseless electrical activity, bedside ultrasound identifies interventions during resuscitation associated with improved survival to hospital admission. A REASON Study.
      In the largest study of TTE in OHCA to date, the presence of cardiac activity was the variable most strongly associated with survival at all time-points including hospital discharge.
      • Gaspari R.
      • Weekes A.
      • Adhikari S.
      • et al.
      A retrospective study of pulseless electrical activity, bedside ultrasound identifies interventions during resuscitation associated with improved survival to hospital admission. A REASON Study.
      A subsequent analysis of this cohort indicated that survival in patients with PEA was higher in those treated with infusion of vasopressors when they have organized myocardial activity but not in those with disorganized activity. This data raises the question of whether TEE could be used to better characterize myocardial activity during arrest, and thus allow individualized therapies that deviate from the one-size-fits-all approach recommended by resuscitation guidelines. Further studies are needed to determine if TEE could improve outcomes by helping clinicians to make the distinction of true PEA vs pseudo-PEA, and potentially guiding to different treatment pathways of care.
      The finding of spontaneous echo contrast was reported in three studies.
      • Teran F.
      • Dean A.J.
      • Centeno C.
      • et al.
      Evaluation of out-of-hospital cardiac arrest using transesophageal echocardiography in the emergency department.
      • Jung W.J.
      • Cha K.C.
      • Kim Y.W.
      • et al.
      Intra-arrest transoesophageal echocardiographic findings and resuscitation outcomes.
      • Varriale P.
      • Maldonado J.M.
      Echocardiographic observations during in hospital cardiopulmonary resuscitation.
      None of the patients with this finding survived to hospital discharge. This finding is thought to be related to fibrinogen mediated red blood cell aggregation during low flow states.
      • Rastegar Raymonda
      • Harnick David J.
      • Weidemann Peter
      • et al.
      Spontaneous echo contrast videodensity isflow-related and is dependent on the relative concentrations of fibrinogen and red blood cells.
      Echo contrast has been described in severe circulatory shock or low flow state.
      • Rastegar Raymonda
      • Harnick David J.
      • Weidemann Peter
      • et al.
      Spontaneous echo contrast videodensity isflow-related and is dependent on the relative concentrations of fibrinogen and red blood cells.
      However, identification of echo contrast on TEE is subjective to imaging presets. Echo contrast could potentially aid the team to terminate unnecessary resuscitation efforts. Larger studies are needed before this finding can be recommended as a prognostic tool.
      As cardiac arrest has multiple underlying causes, using a single reference standard is not applicable. Individual circumstances of arrest pose challenges in performing such research in cardiac arrest. In the reviewed studies variable reference standards were used: autopsy, laboratory test, imaging or surgery, or use of experienced investigators to review saved TEE images and videos. Clear reporting on how these reference standards were implemented was missing in most cases. It is therefore difficult to compare the diagnostic accuracy of TEE across the studies. Better standardization of TEE protocols and consistency in reporting of reference standards may improve data on TEE accuracy in future research.
      Operator skills play an important role in the reliability of the findings of TEE. In three studies, the TEE was performed by skilled Emergency Medicine physicians who have completed dedicated training on TEE.
      • Teran F.
      • Dean A.J.
      • Centeno C.
      • et al.
      Evaluation of out-of-hospital cardiac arrest using transesophageal echocardiography in the emergency department.
      • Kim Y.W.
      • Jung W.J.
      • Cha K.C.
      • et al.
      Diagnosis of aortic dissection by transesophageal echocardiography during cardiopulmonary resuscitation.
      • Jung W.J.
      • Cha K.C.
      • Kim Y.W.
      • et al.
      Intra-arrest transoesophageal echocardiographic findings and resuscitation outcomes.
      In another three studies, TEE was performed by anaesthetists or cardiologists with advanced training in comprehensive TEE.
      • Memtsoudis S.G.
      • Rosenberger P.
      • Loffler M.
      • et al.
      The usefulness of transesophageal echocardiography during intraoperative cardiac arrest in noncardiac surgery.
      • Shillcutt S.K.
      • Markin N.W.
      • Montzingo C.R.
      • et al.
      Use of rapid “rescue” perioperative echocardiography to improve outcomes after hemodynamic instability in noncardiac surgical patients.
      • Hilberath J.N.
      • Burrage P.S.
      • Shernan S.K.
      • et al.
      Rescue transoesophageal echocardiography for refractory haemodynamic instability during transvenous lead extraction.
      The remaining five studies did not provide sufficient details on the operator skills. This reporting bias places the accuracy of interpretation TEE findings into question. In several studies, images and videos from TEE were retrospectively reviewed by experienced emergency physicians, cardiologists, or one of the investigators.
      • Teran F.
      • Dean A.J.
      • Centeno C.
      • et al.
      Evaluation of out-of-hospital cardiac arrest using transesophageal echocardiography in the emergency department.
      • Kim Y.W.
      • Jung W.J.
      • Cha K.C.
      • et al.
      Diagnosis of aortic dissection by transesophageal echocardiography during cardiopulmonary resuscitation.
      • Memtsoudis S.G.
      • Rosenberger P.
      • Loffler M.
      • et al.
      The usefulness of transesophageal echocardiography during intraoperative cardiac arrest in noncardiac surgery.
      • Hilberath J.N.
      • Burrage P.S.
      • Shernan S.K.
      • et al.
      Rescue transoesophageal echocardiography for refractory haemodynamic instability during transvenous lead extraction.
      This was used as a reference standard. The literature supports that Emergency Medicine physicians can successfully attain focused TEE images after a short, structured training programme on simulators.
      • Fair J.
      • Tonna J.
      • Ockerse P.
      • Galovic B.
      • et al.
      Emergency physician-performed transesophageal echocardiography for extracorporeal life support vascular cannula placement.
      • Arntfield R.
      • Pace J.
      • McLeod S.
      • Granton J.
      • Hegazy A.
      • Lingard L.
      Focused transesophageal echocardiography for emergency physicians—description and results from simulation training of a structured four-view examination.
      • Chenkin J.
      • Atzema C.L.
      Contemporary application of point-of-care echocardiography in the emergency department.
      ACEP recommends achieving credentialing in TTE before TEE is attempted and advocates for standardised assessments to demonstrate competency.
      • Labovitz A.J.
      • Noble V.E.
      • Bierig M.
      • et al.
      Focused cardiac ultrasound in the emergent setting: a consensus statement of the American Society of Echocardiography and American College of Emergency Physicians.
      • Fair J.
      • Mallin M.
      • Mallemat H.
      • Zimmerman J.
      • et al.
      Transesophageal echocardiography: guidelines for point-of-care applications in cardiac arrest resuscitation.
      The TEE approach and windows used were similar across the studies. All the studies that have predefined the TEE windows have used the midoesophageal 4 chamber and midoesophageal long axis views. In addition, transgastric short axis view was used.
      • Teran F.
      • Dean A.J.
      • Centeno C.
      • et al.
      Evaluation of out-of-hospital cardiac arrest using transesophageal echocardiography in the emergency department.
      • Lin T.
      • Chen Y.
      • Lu C.
      • et al.
      Use of transoesophageal echocardiography during cardiac arrest in patients undergoing elective non-cardiac surgery.
      • van der Wouw P.A.
      • Koster R.W.
      • Delemarre B.J.
      • et al.
      Diagnostic accuracy of transesophageal echocardiography during cardiopulmonary resuscitation.
      All these views can be used to assess cardiac contractility, left sided systolic function, volume status, assessment of right ventricular enlargement, detecting pericardial effusion, identifying LV thrombus and detecting fine ventricular fibrillation. The midoesophageal long axis view was also used to evaluate the quality of chest compressions in one study.
      • Teran F.
      • Dean A.J.
      • Centeno C.
      • et al.
      Evaluation of out-of-hospital cardiac arrest using transesophageal echocardiography in the emergency department.
      In some studies, aortic views were used to detect aortic dissection and pulmonary artery views to identify proximal pulmonary emboli.
      • Kim Y.W.
      • Jung W.J.
      • Cha K.C.
      • et al.
      Diagnosis of aortic dissection by transesophageal echocardiography during cardiopulmonary resuscitation.
      • Jung W.J.
      • Cha K.C.
      • Kim Y.W.
      • et al.
      Intra-arrest transoesophageal echocardiographic findings and resuscitation outcomes.
      • Lin T.
      • Chen Y.
      • Lu C.
      • et al.
      Use of transoesophageal echocardiography during cardiac arrest in patients undergoing elective non-cardiac surgery.
      • Shillcutt S.K.
      • Markin N.W.
      • Montzingo C.R.
      • et al.
      Use of rapid “rescue” perioperative echocardiography to improve outcomes after hemodynamic instability in noncardiac surgical patients.
      • van der Wouw P.A.
      • Koster R.W.
      • Delemarre B.J.
      • et al.
      Diagnostic accuracy of transesophageal echocardiography during cardiopulmonary resuscitation.
      Finally, midoesophageal bicaval view was used for procedural guidance during extracorporeal membrane oxygenation initiation and for volume responsiveness during ROSC. Several studies excluded the transgastric view during cardiac arrest as in this position the probe tip is closest to the site of chest compressions and there is a potential risk of gastric perforation.
      Identifying specific diagnoses on TEE led to active interventions in many patients. Most common interventions included administration of thrombolytics and emergency embolectomy in suspected PE, pericardiocentesis in cardiac tamponade, fluid administration and blood transfusion in hypovolemia or suspected hemorrhagic shock, and initiation of infusion of vasopressors.
      The reported iatrogenic trauma from the TEE probe includes dental and lip trauma, vocal cord injury, tracheal intubation, oropharyngeal laceration, and oesophageal and gastric laceration and perforation.
      • Hilberath J.N.
      • Oakes D.A.
      • Shernan S.K.
      • Bulwer B.E.
      • D’Ambra M.N.
      • Eltzschig H.K.
      Safety of transesophageal echocardiography.
      Rate of complications from TEE were found to be 0.2–1.2% during intraoperative TEE on intubated patients.
      • Kallmeyer I.J.
      • Collard C.D.
      • Fox J.A.
      • Body S.C.
      • Shernan S.K.
      The safety of intraoperative transesophageal echocardiography: a case series of 7200 cardiac surgical patients.
      Little is known, about the rate of complications during CPR. Theoretically, the external force used during chest compressions poses a risk of aggravating these complications. No studies were identified that have directly investigated this in cardiac arrest patients. From the 11 studies, only one study reported the absence of any complications due to TEE insertion.
      • Comess K.A.
      • DeRook F.A.
      • Russell M.L.
      • et al.
      The incidence of pulmonary embolism in unexplained sudden cardiac arrest with pulseless electrical activity.
      Absence of this data from other studies does not necessarily portend complications did not occur and reporting bias is possible.

      Limitations

      As is the case with many other resuscitative interventions, evaluating the clinical impact of TEE during resuscitation presents important challenges. The eleven selected studies in this review were all relatively small, single-center observational studies. Lack of control groups in all studies precludes the identification of the true impact of TEE on outcomes. All studies have included convenience samples, which represents an important potential source of selection bias. Many of the studies did not have clear predefined inclusion and exclusion criteria. There was also a considerable discrepancy in the TEE operator skills across the studies and their definitions of diagnostic criteria for the identified pathologies. The majority of the studies also lacked confirmatory test to validate the TEE findings. There was underreporting of interventions preceding TEE insertion, some of which could potentially affect the findings in TEE (e.g. epinephrine effect on myocardial activity or administration of intravenous fluids affecting intra-arrest preload and therefore interpretation of right ventricular dilation). Lastly, and probably the most important limitation, is that most observational studies in cardiac arrest are likely affected by resuscitation time bias.
      • Andersen L.W.
      • Grossestreuer A.V.
      • Donnino M.W.
      “Resuscitation time bias”-A unique challenge for observational cardiac arrest research.
      Patients who have longer resuscitation time are more likely to receive the “intervention”, which in this case is TEE. Given that a longer time of arrest is known to be associated with worse outcomes, the evaluation of the effects of TEE may be biased toward a negative effect. Patients with shorter resuscitation times (and therefore better outcomes) are less likely to be enrolled and have TEE performed.

      Conclusion

      This systematic review has investigated the use of TEE during cardiac arrest in the emergency setting, hospital wards, intensive care unit and the operating room in OHCA and IHCA. Intra-arrest TEE can identify reversible causes of arrest in both IHCA and OHCA patients. Due to the lack of confirmatory tests and a high degree of bias in most of the studies included, the accuracy of TEE findings cannot be established. However, in several patients these findings prompted emergent resuscitative interventions. Given the heterogeneity of studies, small sample size and uncertainty regarding important prognostic variables the evidence for TEE in cardiac arrest resuscitation is of low certainty and is affected by a high risk of bias. Larger, multicenter studies are needed to determine the diagnostic accuracy of TEE in identification of reversible causes of arrest and evaluating cardiac contractility.

      Declaration of Competing Interest

      The authors declare the following financial interests/personal relationships which may be considered as potential competing interests: One of the authors, FT, is a co-author of an included study. To avoid any bias, FT was not involved in the decision to include the study, or in data extraction or quality assessment of that study. No funding was received for this review. Authors have no financial or personal conflicts of interest to disclose.

      Acknowledgements

      Andrew Nashed, Rady Faculty of Health Sciences - University of Manitoba, has contributed to the study selection and data extraction of this systematic review.
      Maureen Babb, MLIS, University of Manitoba, has peer reviewed the MEDLINE search strategy.

      Appendix A. Supplementary material

      The following are the Supplementary data to this article:

      References

        • Holmberg M.J.
        • Ross C.E.
        • Fitzmaurice G.M.
        • et al.
        American Heart Association’s Get With The Guidelines-Resuscitation Investigators. Annual Incidence of Adult and Pediatric In-Hospital Cardiac Arrest in the United States.
        Circ Cardiovasc Qual Outcomes. 2019; 12e005580
        • Virani S.S.
        • Alonso A.
        • Benjamin E.J.
        • et al.
        American Heart Association Council on Epidemiology and Prevention Statistics Committee and Stroke Statistics Subcommittee. Heart Disease and Stroke Statistics-2020 Update: A Report From the American Heart Association.
        Circulation. 2020; 141: e139-e596
        • Berg K.M.
        • Soar J.
        • Andersen L.W.
        • et al.
        Adult Advanced Life Support Collaborators. Adult Advanced Life Support: 2020 International Consensus on Cardiopulmonary Resuscitation and Emergency Cardiovascular Care Science With Treatment Recommendations.
        Circulation. 2020; 142: S92-S139
        • Maconochie I.K.
        • Bingham R.
        • Eich C.
        • et al.
        European Resuscitation Council Guidelines for Resuscitation 2015.
        Resuscitation. 2015; 95: 223-248https://doi.org/10.1016/j.resuscitation.2015.07.028
        • Labovitz A.J.
        • Noble V.E.
        • Bierig M.
        • et al.
        Focused cardiac ultrasound in the emergent setting: a consensus statement of the American Society of Echocardiography and American College of Emergency Physicians.
        J Am Soc Echocardiogr. 2010; 23: 1225-1230
        • Blaivas M.
        Transesophageal echocardiography during cardiopulmonary arrest in the emergency department.
        Resuscitation. 2008; 78: 135-140https://doi.org/10.1016/j.resuscitation.2008.02.021
        • Huis in 't Veld M.A.
        • Allison M.G.
        • Bostick D.S.
        • et al.
        Ultrasound use during cardiopulmonary resuscitation is associated with delays in chest compressions.
        Resuscitation. 2017; 119: 95-98https://doi.org/10.1016/j.resuscitation.2017.07.021
        • Reed M.
        • Gibson L.
        • Dewar A.
        • Short S.
        • Black P.
        • Clegg G.
        Introduction of paramedic led Echo in Life Support into the pre-hospital environment: The PUCA study.
        Resuscitation. 2017; 112: 65-69https://doi.org/10.1016/j.resuscitation.2016.09.003
        • Clattenburg E.J.
        • Wroe P.
        • Brown S.
        • et al.
        Point-of-care ultrasound use in patients with cardiac arrest is associated prolonged cardiopulmonary resuscitation pauses: a prospective cohort study.
        Resuscitation. 2018; 122: 65-68https://doi.org/10.1016/j.resuscitation.2017.11.056
        • Fair J.
        • Mallin M.
        • Mallemat H.
        • Zimmerman J.
        • et al.
        Transesophageal echocardiography: guidelines for point-of-care applications in cardiac arrest resuscitation.
        Ann Emerg Med. 2018; 71: 201-207
        • Teran F.
        • Prats M.I.
        • Nelson B.P.
        • et al.
        Focused transesophageal echocardiography during cardiac arrest resuscitation: JACC review topic of the week.
        J Am Coll Cardiol. 2020; 76: 745-754
        • Anderson K.L.
        • Castaneda M.G.
        • Boudreau S.M.
        • Sharon D.J.
        • Bebarta V.S.
        Left ventricular compressions improve hemodynamics in a swine model of out-of-hospital cardiac arrest.
        Prehospital Emergency Care. 2017; 21: 272-280https://doi.org/10.1080/10903127.2016.1241328
        • Kim Y.W.
        • Cha K.-C.
        • Kim Y.S.
        • et al.
        Kinetic analysis of cardiac compressions during cardiopulmonary resuscitation.
        J Critical Care. 2019; 52: 48-52https://doi.org/10.1016/j.jcrc.2019.04.003
        • Fair J.
        • Tonna J.
        • Ockerse P.
        • Galovic B.
        • et al.
        Emergency physician-performed transesophageal echocardiography for extracorporeal life support vascular cannula placement.
        Am J Emerg Med. 2016; 34: 1637-1639
        • Arntfield R.
        • Pace J.
        • McLeod S.
        • Granton J.
        • Hegazy A.
        • Lingard L.
        Focused transesophageal echocardiography for emergency physicians—description and results from simulation training of a structured four-view examination.
        Critical Ultrasound J. 2015; 7https://doi.org/10.1186/s13089-015-0027-3
        • Chenkin J.
        • Atzema C.L.
        Contemporary application of point-of-care echocardiography in the emergency department.
        Can J Cardiol. 2018; 34: 109-116https://doi.org/10.1016/j.cjca.2017.08.018
        • Lalande E.
        • Burwash-Brennan T.
        • Burns K.
        • et al.
        SHoC Investigators. Is point-of-care ultrasound a reliable predictor of outcome during atraumatic, non-shockable cardiac arrest? A systematic review and meta-analysis from the SHoC investigators.
        Resuscitation. 2019; 139: 159-166
      1. OSF Open Registries Network. Registration link; https://osf.io/k7wah [accessed March 5, 2021].

        • Moher D.
        • Liberati A.
        • Tetzlaff J.
        • et al.
        PRISMA Group. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement.
        Ann Intern Med. 2009; 151 (264–9, W64)
        • Ouzzani M.
        • Hammady H.
        • Fedorowicz Z.
        • et al.
        Rayyan-a web and mobile app for systematic reviews.
        Syst Rev. 2016; 5: 210
      2. Systematic reviews, Centre for Reviews and Dissemination, University of York, York, 2009. https://www.york.ac.uk/media/crd/Systematic_Reviews.pdf [accessed May 7, 2020].

        • Whiting P.F.
        • Rutjes A.W.
        • Westwood M.E.
        • et al.
        QUADAS-2 Group. QUADAS-2: a revised tool for the quality assessment of diagnostic accuracy studies.
        Ann Intern Med. 2011; 155: 529-536
        • Teran F.
        • Dean A.J.
        • Centeno C.
        • et al.
        Evaluation of out-of-hospital cardiac arrest using transesophageal echocardiography in the emergency department.
        Resuscitation. 2019; 137: 140-147
        • Kim Y.W.
        • Jung W.J.
        • Cha K.C.
        • et al.
        Diagnosis of aortic dissection by transesophageal echocardiography during cardiopulmonary resuscitation.
        Am J Emerg Med. 2021; 39: 92-95
        • Jung W.J.
        • Cha K.C.
        • Kim Y.W.
        • et al.
        Intra-arrest transoesophageal echocardiographic findings and resuscitation outcomes.
        Resuscitation. 2020; 154: 31-37
        • Lin T.
        • Chen Y.
        • Lu C.
        • et al.
        Use of transoesophageal echocardiography during cardiac arrest in patients undergoing elective non-cardiac surgery.
        Br J Anaesth. 2006; 96: 167-170
        • Memtsoudis S.G.
        • Rosenberger P.
        • Loffler M.
        • et al.
        The usefulness of transesophageal echocardiography during intraoperative cardiac arrest in noncardiac surgery.
        Anesth Analg. 2006; 102: 1653-1657
        • Shillcutt S.K.
        • Markin N.W.
        • Montzingo C.R.
        • et al.
        Use of rapid “rescue” perioperative echocardiography to improve outcomes after hemodynamic instability in noncardiac surgical patients.
        J Cardiothorac Vasc Anesth. 2012; 26: 362-370
        • Hilberath J.N.
        • Burrage P.S.
        • Shernan S.K.
        • et al.
        Rescue transoesophageal echocardiography for refractory haemodynamic instability during transvenous lead extraction.
        Eur Heart J Cardiovasc Imaging. 2014; 15: 926-932
        • Varriale P.
        • Maldonado J.M.
        Echocardiographic observations during in hospital cardiopulmonary resuscitation.
        Crit Care Med. 1997; 25: 1717-1720
        • van der Wouw P.A.
        • Koster R.W.
        • Delemarre B.J.
        • et al.
        Diagnostic accuracy of transesophageal echocardiography during cardiopulmonary resuscitation.
        J Am Coll Cardiol. 1997; 30: 780-783
        • Comess K.A.
        • DeRook F.A.
        • Russell M.L.
        • et al.
        The incidence of pulmonary embolism in unexplained sudden cardiac arrest with pulseless electrical activity.
        Am J Med. 2000; 109: 351-356
        • Miyake M.
        • Izumi C.
        • Takahashi S.
        • et al.
        Efficacy of transesophageal echocardiography in patients with cardiac arrest or shock.
        J Cardiol. 2004; 44: 189-194
        • Aagaard R.
        • Caap P.
        • Hansson N.C.
        • Bøtker M.T.
        • Granfeldt A.
        • Løfgren B.
        Detection of Pulmonary Embolism During Cardiac Arrest-Ultrasonographic Findings Should Be Interpreted With Caution.
        Crit Care Med. 2017; 45 (PMID: 28403120): e695-e702https://doi.org/10.1097/CCM.0000000000002334
        • Aagaard R.
        • Granfeldt A.
        • Bøtker M.T.
        • Mygind-Klausen T.
        • Kirkegaard H.
        • Løfgren B.
        The right ventricle is dilated during resuscitation from cardiac arrest caused by hypovolemia: a porcine ultrasound study.
        Crit Care Med. 2017; 45 (PMID: 28430698): e963-e970https://doi.org/10.1097/CCM.0000000000002464
        • Wardi G.
        • Blanchard D.
        • Dittrich T.
        • Kaushal K.
        • Sell R.
        Right ventricle dysfunction and echocardiographic parameters in the first 24h following resuscitation in the post-cardiac arrest patient: A retrospective cohort study.
        Resuscitation. 2016; 103 (Epub 2016 Apr 11 PMID: 27079665): 71-74https://doi.org/10.1016/j.resuscitation.2016.03.009
        • Böttiger B.W.
        • Arntz H.R.
        • Chamberlain D.A.
        • et al.
        TROICA Trial Investigators; European Resuscitation Council Study Group. Thrombolysis during resuscitation for out-of-hospital cardiac arrest.
        N Engl J Med. 2008; 359 (PMID: 19092151): 2651-2662https://doi.org/10.1056/NEJMoa070570
        • Gaspari R.
        • Weekes A.
        • Adhikari S.
        • et al.
        Emergency department point-of-care ultrasound in out-of-hospital and in-ED cardiac arrest.
        Resuscitation. 2016; 109: 33-39https://doi.org/10.1016/j.resuscitation.2016.09.018
        • Meron Giora
        • Kürkciyan Istepan
        • Sterz Fritz
        • et al.
        Non-traumatic aortic dissection or rupture as cause of cardiac arrest: presentation and outcome.
        Resuscitation. 2004; 60: 143-150
        • Paradis N.A.
        • Martin G.B.
        • Goetting M.G.
        • Rivers E.P.
        • Feingold M.
        • Nowak R.M.
        Aortic pressure during human cardiac arrest. Identification of pseudo-electromechanical dissociation.
        Chest. 1992; 101 (PMID: 1729058): 123-128https://doi.org/10.1378/chest.101.1.123
        • Gaspari R.
        • Weekes A.
        • Adhikari S.
        • et al.
        A retrospective study of pulseless electrical activity, bedside ultrasound identifies interventions during resuscitation associated with improved survival to hospital admission. A REASON Study.
        Resuscitation. 2017; 120 (Epub 2017 Sep 13 PMID: 28916478): 103-107https://doi.org/10.1016/j.resuscitation.2017.09.008
        • Rastegar Raymonda
        • Harnick David J.
        • Weidemann Peter
        • et al.
        Spontaneous echo contrast videodensity isflow-related and is dependent on the relative concentrations of fibrinogen and red blood cells.
        J Am College Cardiol. 2003; 41: 603-610
        • Hilberath J.N.
        • Oakes D.A.
        • Shernan S.K.
        • Bulwer B.E.
        • D’Ambra M.N.
        • Eltzschig H.K.
        Safety of transesophageal echocardiography.
        J Am Soc Echocardiogr. 2010; 23 (quiz 1220-1): 1115-1127https://doi.org/10.1016/j.echo.2010.08.013
        • Kallmeyer I.J.
        • Collard C.D.
        • Fox J.A.
        • Body S.C.
        • Shernan S.K.
        The safety of intraoperative transesophageal echocardiography: a case series of 7200 cardiac surgical patients.
        Anesth Analg. 2001; 92 (PMID: 11323333): 1126-1130https://doi.org/10.1097/00000539-200105000-00009
        • Andersen L.W.
        • Grossestreuer A.V.
        • Donnino M.W.
        “Resuscitation time bias”-A unique challenge for observational cardiac arrest research.
        Resuscitation. 2018; 125: 79-82https://doi.org/10.1016/j.resuscitation.2018.02.006