Skip to main content
Annals of Intensive Care
Download PDF

Right ventricular injury in patients with COVID-19-related ARDS eligible for ECMO support: a multicenter retrospective study

Annals of Intensive Care volume 14, Article number: 40 (2024) Cite this article

Abstract

Background

Coronavirus disease 2019 (COVID-19)-related acute respiratory distress syndrome (ARDS) is associated with high mortality. Extracorporeal membrane oxygenation (ECMO) has been proposed in this setting, but optimal criteria to select target patients remain unknown. Our hypothesis is that evaluation of right ventricular (RV) function could be helpful. The aims of our study were to report the incidence and outcomes of patients eligible for ECMO according to EOLIA criteria, and to identify a subgroup of patients with RV injury, which could be a target for ECMO.

Methods

Retrospective observational study involving 3 French intensive care units (ICUs) of teaching hospitals. Patients with confirmed SARS-CoV-2 infection between March 2020 and March 2021, presenting ARDS and with available echocardiography, were included. Patients were classified in three groups according to whether or not they met the EOLIA criteria and the presence of RV injury (RVI) (“EOLIA −”, “EOLIA + RVI −” and “EOLIA + RVI + ”). RVI was defined by the association of RV to left ventricular end-diastolic area ratio > 0.8 and paradoxical septal motion. Kaplan–Meier survival curves were used to analyze outcome as well as a Cox model for 90 day mortality.

Results

915 patients were hospitalized for COVID-19, 418 of them with ARDS. A total of 283 patients with available echocardiography were included. Eighteen (6.3%) patients received ECMO. After exclusion of these patients, 107 (40.5%) were classified as EOLIA −, 126 (47.5%) as EOLIA + RVI −, and 32 (12%) as EOLIA + RVI + . Ninety-day mortality was 21% in the EOLIA-group, 44% in the EOLIA + RVI-group, and 66% in the EOLIA + RVI + group (p < 0.001). After adjustment, RVI was statistically associated with 90-day mortality (HR = 1.92 [1.10–3.37]).

Conclusions

Among COVID-19-associated ARDS patients who met the EOLIA criteria, those with significant RV pressure overload had a particularly poor outcome. This subgroup may be a more specific target for ECMO. This represented 12% of our cohort compared to 60% of patients who met the EOLIA criteria only. How the identification of this high-risk subset of patients translates into patient-centered outcomes remains to be evaluated.

Background

Severely ill coronavirus disease 2019 (COVID-19) patients often develop acute respiratory distress syndrome (COVID-19-associated ARDS) [1] and circulatory failure [2, 3]. COVID-19-associated ARDS is associated with high mortality, and extracorporeal membrane oxygenation (ECMO) has been used in this indication [4,5,6] with various impacts on the outcome [4, 7]. A few observational studies have reported that venovenous (VV) ECMO reduces mortality [8, 9], essentially if patients are treated in high-volume centers [9]. The French authorities recommend the use of EOLIA (ECMO to Rescue Lung Injury in Severe ARDS) [10] criteria to select patients eligible for ECMO. However, in a period of low resources due to the high number of critically ill patients, optimal selection of patients who can benefit from the technique is fundamental [11]. A large number of mortality prediction models have been developed for ECMO patients, but they are unsuitable to provide decision support as they were developed in ECMO patients only, and the decision to start ECMO had already been taken [12].

In a large retrospective international cohort of critically ill patients with COVID-19, Huang et al. reported a 19% incidence of severe right ventricular (RV) overload which was independently associated with mortality [13]. ECMO controls factors that risk worsening RV function and improves RV function when already impaired [14].

We hypothesized that adding information about respiratory and RV function to blood gases could help improve selection of patients at high risk of mortality, in accordance with our recent study performed in a large cohort of patients with moderate to severe non-COVID-19-associated ARDS [15].

In a multicenter cohort of COVID-19-associated ARDS, we report the incidence of patients potentially eligible for VV ECMO according to EOLIA criteria, as well as their outcome, and identify a specific subgroup with a remarkably high mortality, which could best benefit from VV ECMO.

Methods

Study design

This was a retrospective observational study involving 3 intensive care units (ICUs) of tertiary teaching hospitals in France. Participating centers all performed critical care echocardiography for RV function evaluation and restricted indications for VV ECMO according to their standards of care.

Consecutive patients with confirmed SARS-CoV-2 infection between March 2020 and March 2021 admitted to the ICU for invasive mechanical ventilation with a diagnosis of ARDS using Berlin definition [16] were screened. The period of observation was 7 days after intubation and patients with no available echocardiography during this period were excluded. The study protocol was approved by the ethics committee of the French Society of Intensive Care Medicine (ref SRLF CE 21–98).

Patient characteristics and clinical evaluation

We calculated the Sequential Organ Failure Assessment (SOFA) score [17] at admission and the simplified acute physiology score II (SAPS II) [18]. Pre-intubation characteristics, in particular history of vaccination, body mass index, co-morbidities, interval between onset of symptoms and ICU admission and between ICU admission and intubation, were collected. We also reported the use of dexamethasone, anti-IL-6-receptor, prone position, nitric oxide inhalation, and VV ECMO, as well as clinical and respiratory characteristics (time since intubation, respiratory settings with tidal volume, respiratory rate, positive end-expiratory pressure [PEEP], plateau pressure, driving pressure, PaO2, PaCO2, FiO2) at the time the patient met for the first time the EOLIA criteria, or at the time of the worst PaO2/FiO2 if never met, during the first 7 days of mechanical ventilation. EOLIA criteria were defined as follows: PaO2/FiO2 of < 50 mmHg for > 3 h or PaO2/FiO2 < 80 mmHg for > 6 h or an arterial blood pH < 7.25 with a PaCO2 > 60 mmHg despite ventilator optimization. In-ICU, in-hospital, and 90 day mortality were recorded.

Echocardiography

Echocardiography was performed by either a transesophageal or transthoracic approach according to the usual practice of the centers. Patients were all intubated, sedated, and adapted to the ventilator. We focused on the echocardiography performed within 24 h when patients met the EOLIA criteria, or the worst PaO2/FiO2 when EOLIA criteria were not met, during the first 7 days of invasive mechanical ventilation. Conventional parameters of RV and left ventricular (LV) function traditionally reported in ARDS patients [19, 20] were systematically obtained. Briefly, we measured LV ejection fraction as a marker of LV systolic function, and maximal velocity of mitral inflow (E and A waves) as a marker of LV diastolic function and filling pressure. RV function was evaluated by the RV/LV end-diastolic area (EDA) ratio, the fractional area change (calculated as RV EDA minus end-systole area divided by EDA), and the septal motion (whether or not paradoxical). Pulmonary acceleration time was also recorded as a marker of pulmonary hypertension, as well as the velocity–time integral (VTI) in the LV outflow track (aortic VTI).

Statistical analysis

Baseline characteristics were reported as median [interquartile range] and n (%) for quantitative and qualitative variables, respectively. Quantitative variables were compared using nonparametric tests, the Mann–Whitney test, or the Kruskal–Wallis test, as appropriate. Qualitative variables were compared using Pearson’s Chi-square test or Fisher’s exact test, as appropriate.

Missing data were reported. Determination of different subgroups was performed in patients in whom ECMO was not implemented. Accordingly, 18 patients were excluded from this analysis. Subgroups were defined according to whether or not the EOLIA criteria were met, and the presence of RV injury (RVI), leading to 3 different subgroups, “EOLIA -”, “EOLIA + RVI −” and “EOLIA + RVI + ” (Fig. 1). RVI was defined as the presence of significant RV dilatation (RVEDA/LVEDA > 0.8) and paradoxical septal motion. The cutoff for RV dilatation was chosen based on the median in the cohort. Survival analysis was compared between groups using the Kaplan–Meier method to estimate cumulative death rates, which were then compared by the log rank test. Risk factors associated with 90 day mortality in patients presenting EOLIA criteria were analyzed using a multivariable Cox model. Briefly, the variable of interest, i.e., RVI, and all variables known to have an impact on mortality in COVID-19-associated ARDS and associated with survival in univariate analysis, were included. The effects of the variables were reported in hazard ratios with 95% confidence intervals and reported on a Forest plot.

Fig. 1
figure 1

Study flowchart. ICU: Intensive Care Unit, ARDS Acute Respiratory Distress Syndrome, VV ECMO VenoVenous Extracorporeal Membrane Oxygenation, RVI Right Ventricular Injury

Full size image

A p value lower than 0.05 was considered significant. All statistical analyses were performed using R Studio (R version 4.2.0, The R Foundation for statistical computing).

Results

Patients’ characteristics at admission

Between March 2020 and 2021, 915 patients were hospitalized in the participating ICUs for COVID-19, 418 of them with ARDS. A total of 283 patients with available echocardiography were enrolled in the study (Fig. 1). Their baseline characteristics on ICU admission are given in Table 1. Median age was 67 [59;72] years, SOFA score was 4 [3;5], and SAPS II 37 [31;43]. During these first three waves, only 14 patients were vaccinated against SARS-CoV-2. One hundred and eighty-three (65%) patients were treated with corticosteroids and 21 (7.4%) with anti-IL6-receptor. Median time from ICU admission to intubation was 1 [1;3] day. Most patients (80%) were prone positioned within 7 days following tracheal intubation.

Table 1 Baseline characteristics of patients on ICU admission Categorical variables are expressed as number (%) and continuous variables as median [interquartile ranges]
Full size table

Patients’ characteristics on meeting EOLIA criteria (or at the worst PaO2/FiO2) and outcome

Respiratory and echocardiographic parameters are listed in Table 2. Patients were ventilated with a median tidal volume of 6.3 [5.9;7] mL/kg of predicted body weight, with a plateau pressure of 27 [24;30] cmH2O, a driving pressure of 16 [13;19] cmH2O, and a PEEP of 10 [8;13] cmH2O. Most patients (76%) experienced RV dilatation and median RV/LV EDA was 0.74 [0.59;0.88]. Paradoxical septal motion was identified in 93 (39%) patients. Median ICU stay was 20 [12;36] days, and median time on invasive ventilation was 15 [9;30] days. In-ICU, in-hospital, and 90-day mortalities were 36.0%, 36.4%, and 37.5%, respectively.

Table 2 Clinical characteristics and echocardiographic findings at the time the patient met the EOLIA criteria or of the worst PaO2/FiO2 within the first 7 days after tracheal intubation
Full size table

Characteristics of the different subgroups with their respective outcome and factors associated with 90 day mortality

Eighteen patients (6%) received VV ECMO with a worst PaO2/FiO2 and concomitant PaCO2 values of 59 [49;72] mmHg and 65 [54;71] mmHg, respectively. Their in-hospital mortality was 44%. After exclusion of these patients, 158/265 (60%) patients were eligible for ECMO according to EOLIA criteria within 7 days following tracheal intubation. Among them, 126 were classified in the EOLIA + RVI– subgroup and 32 in the EOLIA + RVI + subgroup (Fig. 1, Table 3). No difference in shock and in norepinephrine dose was observed between subgroups.

Table 3 Characteristics of the 265 patients included in the subgroup analysis according to their subgroups
Full size table

In the EOLIA- group, patients had lower severity according to blood gases and respiratory mechanics with a moderate RVI reflected by a median RVEDA/LVEDA of 0.74 [0.66;0.85] and paradoxical septal motion in 40% of cases. In the EOLIA + RVI + group, patients displayed the highest severity of RVI with median RVEDA/LVEDA of 1 [0.93, 1.18] and the lowest pulmonary acceleration time (69 [50, 80] ms). By definition, all had paradoxical septal motion. In contrast, in the EOLIA + RVI− group, while the patients had similar respiratory severity, RVI was less severe (RVEDA/LVEDA of 0.70 [0.58, 0.81]), median pulmonary acceleration time was 83 [60, 100] ms, and paradoxical septal motion was seen in 17% of cases).

Survival curves among the three groups are shown in Fig. 2. At day 90, mortality was 21% in the EOLIA− group, 44% in the EOLIA + RVI− group, and 66% in the EOLIA + RVI + group (p < 0.001). In a multivariable model, including age, SOFA score at admission, immunosuppression, driving pressure, prone positioning and corticosteroids, RVI was statistically associated with 90-day mortality (HR = 1.92 [1.10–3.37]) (Fig. 3).

Fig. 2
figure 2

Kaplan–Meier survival estimates among the three subgroups. p value was obtained with a log rank test. RVI Right Ventricular Injury

Full size image
Fig. 3
figure 3

Risk factors for death at day 90 among patients reaching EOLIA criteria within 7 days after intubation. SOFA Sequential Organ Failure Assessment

Full size image

Discussion

In a large cohort of patients with COVID-19-associated ARDS, an approach combining clinical, respiratory, and echocardiographic parameters characterized 3 different subgroups within 7 days after tracheal intubation. A specific subgroup of patients with the most severe respiratory impairment and RV pressure overload (as shown by significant increase in RV size and paradoxical septal motion), had a significantly higher mortality compared to the other patients.

How we define the target population that could best benefit from VV ECMO is crucial when a pandemic and ICU surge lead to resource constraints. When only based on blood gases and EOLIA criteria [10], a large proportion of our patients (60%) were potentially eligible for ECMO. Conversely, it was in only 8.9% in our previous cohort of 752 patients with moderate to severe non-COVID-19-associated ARDS [15]. This well reflects the particular severity of lung injury in patients ventilated for COVID-19-related pneumonia. Moreover, in-hospital mortality of the 158 patients meeting EOLIA criteria within 7 days following tracheal intubation but managed without ECMO in the present cohort was similar to that of the 18 patients managed with ECMO (47% versus 44%, respectively). It was also similar to the in-hospital mortality rate previously reported in patients managed with ECMO in the international Extracorporeal Life Support Organization registry which ranged between 38% and 59%, according to the time of ECMO implantation (before/after May 1, 2020) and to early or late-adopting centers in a much younger population than ours [7]. In this latter series, only 60% of patients were turned prone compared to 80% in our study population.

Our results suggest that the target population could be patients presenting the EOLIA criteria and displaying RVI (12% of the population) combining very severe illness according to blood gases and respiratory mechanics with remarkable RV pressure overload. Those patients had the highest mortality (90 day mortality of 66%). Evrard et al. [21] have shown that ventilated patients with COVID-19-associated ARDS exhibited worsening of respiratory function when they developed RVI. Importantly, VV ECMO reduces RV afterload by rapidly and efficiently improving blood oxygenation and decarboxylation [14, 20], and by allowing ultra-protective ventilation with a more pronounced reduction of plateau and driving pressures [22]. A recent study in a small cohort of 15 patients with COVID-19-associated ARDS found that 47% of them exhibited severe RV pressure overload, and that RV function as well as circulatory failure rapidly improved within 24 h following ECMO [14].

In a recent systematic review and meta-analysis among patients receiving ECMO for COVID-19, driving pressure higher than 16 cmH2O was associated with mortality (high certainty), whereas pre-cannulation renal replacement therapy was not (low certainty) [23]. However, we did not find in our cohort an association between driving pressure and mortality.

Cain et al. found that RV dysfunction on VV ECMO was independently associated with survival and may occur or persist after VV ECMO initiation, even after controlling for all risk factors of pulmonary hypertension [24]. While there is no actual recommendation for the treatment of such a condition, prone positioning on ECMO can be tested as it can improve respiratory system compliance [25], and then hemodynamics. Inhaled nitric oxide can also be considered [26, 27]. Finally, veno-pulmonary ECMO with the ProtekDuo cannula has the interesting advantage of combining both cardiocirculatory support (for the right ventricle) and oxygenation without recirculation. A few studies have reported successful outcomes in COVID-19-associated ARDS [28]. However, the device is not available everywhere and more studies are needed to evaluate its potential benefit.

Our study suffers from limitations. First, the impact of the pandemic on the burden of healthcare workers precluded us from conducting a prospective study. Therefore, a large number of ventilated patients (n = 135) were excluded from the present study because echocardiography was not available, resulting in a selection bias which could alter our results. Timing of ICU admission and high strain could influence the decision to perform echocardiography. However, the way we selected patients could lead us to include the most severely ill ones, those who underwent echocardiography, thus reinforcing our results. Second, the timing of echocardiographic assessment was not standardized among centers, and timing between echocardiography and the first session of prone positioning was not collected. However, RVI was assessed within 24 h of compliance with the EOLIA criteria, during which ECMO implantation can be discussed. Third, missing data forced us to exclude some variables from the analysis because they were rarely recorded, as central venous pressure, which is of importance in evaluating RVI. Fourth, the study was performed in patients admitted to centers in which critical care echocardiography is usual practice for most physicians, and this could limit the external validity of our results. Indeed, applying our suggested approach to a target ECMO population means that intensivists are trained enough to evaluate RV pressure overload by this technique. Finally, due to the retrospective nature of the cohort, the reason for the clinical decision whether or not to initiate ECMO cannot be captured. Decision-making is complex and factors other than classical ECMO criteria can intervene. Therefore, we chose to exclude patients already treated with ECMO from the survival analysis, but it remains to be demonstrated prospectively how our approach can positively affect the therapeutic strategy and outcome of patients with ARDS.

In conclusion, we identified a subgroup of patients with significant RV pressure overload and respiratory impairment with a poor outcome, which could help physicians determine when and in whom to initiate ECMO. This represented 12% of our cohort compared to 66% of patients who met the EOLIA criteria. How the identification of this high-risk subset of patients translates into patient-centered outcomes will need to be evaluated in the future.

For further studies focusing on the use of ECMO in ARDS, evaluation of RV function before cannulation should be performed prospectively to confirm or not the impact of RVI on prognosis before designing a randomized control trial comparing a strategy of initiation of ECMO on the basis of RVI criteria to a more conventional indication.

Availability of data and materials

The data set used during this study is available from the corresponding author on reasonable request.

Abbreviations

ARDS:

Acute Respiratory Distress Syndrome

COVID-19:

Coronavirus disease 2019

ECMO:

ExtraCorporeal Membrane Oxygenation

EDA:

End-Diastolic Area

ICU:

Intensive Care Unit

LV:

Left Ventricular

PEEP:

Positive End-Expiratory Pressure

RV:

Right Ventricular

RVI:

Right Ventricular Injury

SOFA:

Sequential Organ Failure Assessment

SAPS II:

Simplified Acute Physiology Score II

VTI:

Velocity–Time Integral

References

  1. Zhou F, Yu T, Du R, Fan G, Liu Y, Liu Z, et al. Clinical course and risk factors for mortality of adult inpatients with COVID-19 in Wuhan, China: a retrospective cohort study. The Lancet. 2020;395(10229):1054–62.

    Article  CAS  Google Scholar 

  2. Michard F, Vieillard-Baron A. Critically ill patients with COVID-19: are they hemodynamically unstable and do we know why? Intensive Care Med. 2021;47(2):254–5.

    Article  CAS  PubMed  Google Scholar 

  3. Hendren NS, Drazner MH, Bozkurt B, Cooper LT. Description and proposed management of the acute COVID-19 cardiovascular syndrome. Circulation. 2020;141(23):1903–14.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Barbaro RP, MacLaren G, Boonstra PS, Iwashyna TJ, Slutsky AS, Fan E, et al. Extracorporeal membrane oxygenation support in COVID-19: an international cohort study of the extracorporeal life support organization registry. Lancet Lond Engl. 2020;396(10257):1071–8.

    Article  CAS  Google Scholar 

  5. Badulak J, Antonini MV, Stead CM, Shekerdemian L, Raman L, Paden ML, et al. Extracorporeal membrane oxygenation for COVID-19: updated 2021 guidelines from the extracorporeal life support organization. ASAIO J Am Soc Artif Intern Organs. 2021;67(5):485–95.

    Google Scholar 

  6. Schmidt M, Hajage D, Lebreton G, Monsel A, Voiriot G, Levy D, et al. Extracorporeal membrane oxygenation for severe acute respiratory distress syndrome associated with COVID-19: a retrospective cohort study. Lancet Respir Med. 2020;8(11):1121–31.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Barbaro RP, MacLaren G, Boonstra PS, Combes A, Agerstrand C, Annich G, et al. Extracorporeal membrane oxygenation for COVID-19: evolving outcomes from the international extracorporeal life support organization registry. Lancet Lond Engl. 2021;398(10307):1230–8.

    Article  CAS  Google Scholar 

  8. Shaefi S, Brenner SK, Gupta S, O’Gara BP, Krajewski ML, Charytan DM, et al. Extracorporeal membrane oxygenation in patients with severe respiratory failure from COVID-19. Intensive Care Med. 2021;47(2):208–21.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Hajage D, Combes A, Guervilly C, Lebreton G, Mercat A, Pavot A, et al. Extracorporeal membrane oxygenation for severe acute respiratory distress syndrome associated with COVID-19: an emulated target trial analysis. Am J Respir Crit Care Med. 2022;206(3):281–94.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Combes A, Hajage D, Capellier G, Demoule A, Lavoué S, Guervilly C, et al. Extracorporeal membrane oxygenation for severe acute respiratory distress syndrome. N Engl J Med. 2018;378(21):1965–75.

    Article  PubMed  Google Scholar 

  11. Ramanathan K, Antognini D, Combes A, Paden M, Zakhary B, Ogino M, et al. Planning and provision of ECMO services for severe ARDS during the COVID-19 pandemic and other outbreaks of emerging infectious diseases. Lancet Respir Med. 2020;8(5):518–26.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Pladet LCA, Barten JMM, Vernooij LM, Kraemer CVE, Bunge JJH, Scholten E, et al. Prognostic models for mortality risk in patients requiring ECMO. Intensive Care Med. 2023;49(2):131–41.

    Article  PubMed  PubMed Central  Google Scholar 

  13. Huang S, Vignon P, Mekontso-Dessap A, Tran S, Prat G, Chew M, et al. Echocardiography findings in COVID-19 patients admitted to intensive care units: a multi-national observational study (the ECHO-COVID study). Intensive Care Med. 2022;48(6):667–78.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Levy D, Desnos C, Lebreton G, Théry G, Pineton de Chambrun M, Leprince P, et al. Early reversal of right ventricular dysfunction after venovenous ECMO in patients with COVID-19 Pneumonia. Am J Respir Crit Care Med. 2022;207:784–7.

    Article  PubMed Central  Google Scholar 

  15. Petit M, Mekontso-Dessap A, Masi P, Legras A, Vignon P, Vieillard-Baron A. Evaluation of right ventricular function and driving pressure with blood gas analysis could better select patients eligible for VV ECMO in severe ARDS. Crit Care Lond Engl. 2021;25(1):220.

    Article  Google Scholar 

  16. Ranieri VM, Rubenfeld GD, Thompson BT, Ferguson ND, Caldwell E, et al. ARDS Definition Task Force, Acute respiratory distress syndrome: the Berlin definition. JAMA. 2012;307(23):2526–33.

    PubMed  Google Scholar 

  17. Vincent JL, Moreno R, Takala J, Willatts S, De Mendonça A, Bruining H, et al. The SOFA (Sepsis-related Organ Failure Assessment) score to describe organ dysfunction/failure. On behalf of the Working Group on Sepsis-Related Problems of the European Society of Intensive Care Medicine. Intensive Care Med. 1996;22(7):707–10.

    Article  CAS  PubMed  Google Scholar 

  18. Le Gall JR, Lemeshow S, Saulnier F. A new simplified acute physiology score (SAPS II) based on a European/North American multicenter study. JAMA. 1993;270(24):2957–63.

    Article  PubMed  Google Scholar 

  19. Petit M, Jullien E, Vieillard-Baron A. Right ventricular function in acute respiratory distress syndrome: impact on outcome, respiratory strategy and use of veno-venous extracorporeal membrane oxygenation. Front Physiol. 2021;12: 797252.

    Article  PubMed  Google Scholar 

  20. Mekontso Dessap A, Boissier F, Charron C, Bégot E, Repessé X, Legras A, et al. Acute cor pulmonale during protective ventilation for acute respiratory distress syndrome: prevalence, predictors, and clinical impact. Intensive Care Med. 2016;42(5):862–70.

    Article  PubMed  Google Scholar 

  21. Evrard B, Goudelin M, Giraudeau B, François B, Vignon P. Right ventricular failure is strongly associated with mortality in patients with moderate-to-severe COVID-19-related ARDS and appears related to respiratory worsening. Intensive Care Med. 2022;48(6):765–7.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Schmidt M, Pham T, Arcadipane A, Agerstrand C, Ohshimo S, Pellegrino V, et al. Mechanical ventilation management during extracorporeal membrane oxygenation for acute respiratory distress syndrome. An International Multicenter Prospective Cohort. Am J Respir Crit Care Med. 2019;200(8):1002–12.

    Article  CAS  PubMed  Google Scholar 

  23. Tran A, Fernando SM, Rochwerg B, Barbaro RP, Hodgson CL, Munshi L, et al. Prognostic factors associated with mortality among patients receiving venovenous extracorporeal membrane oxygenation for COVID-19: a systematic review and meta-analysis. Lancet Respir Med. 2022;11:235-S2213-2600(22)00296-X.

    Article  PubMed  PubMed Central  Google Scholar 

  24. Cain MT, Taylor LJ, Colborn K, Teman NR, Hoffman J, Mayer KP, et al. Worse survival in patients with right ventricular dysfunction and COVID-19–associated acute respiratory distress requiring extracorporeal membrane oxygenation: A multicenter study from the ORACLE Group. J Thorac Cardiovasc Surg. 2022; S0022522322013514.

  25. Petit M, Fetita C, Gaudemer A, Treluyer L, Lebreton G, Franchineau G, et al. Prone-positioning for severe acute respiratory distress syndrome requiring extracorporeal membrane oxygenation. Crit Care Med. 2022;50(2):264–74.

    Article  CAS  PubMed  Google Scholar 

  26. Pappalardo F, Montisci A. Adjunctive therapies during veno-venous extracorporeal membrane oxygenation. J Thorac Dis. 2018;10(S5):S683–91.

    Article  PubMed  PubMed Central  Google Scholar 

  27. Heuts S, Ubben JF, Banks-Gonzales V, Sels JW, Lorusso R, Van Mook WNKA, et al. Nitric oxide ventilation improves recirculation and right ventricular function during veno-venous extracorporeal membrane oxygenation in a COVID-19 patient. J Cardiothorac Vasc Anesth. 2021;35(9):2763–7.

    Article  CAS  PubMed  Google Scholar 

  28. El Banayosy AM, El Banayosy A, Brewer JM, Mihu MR, Chidester JM, Swant LV, et al. The ProtekDuo for percutaneous V-P and V-VP ECMO in patients with COVID-19 ARDS. Int J Artif Organs. 2022;45(12):1006–12.

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

None.

Funding

None.

Author information

Authors and Affiliations

  1. Medical Intensive Care Unit, Ambroise Paré Hospital, APHP, 9 Avenue Charles de Gaulles, Boulogne-Billancourt, France

    Matthieu Petit, Edouard Jullien, Adrien Joseph, Cyril Charron, Anousone Daulasim & Antoine Vieillard-Baron

  2. Paris-Saclay University, UVSQ, Inserm, CESP, 94807, Villejuif, France

    Matthieu Petit & Antoine Vieillard-Baron

  3. Intensive Care Unit, University Hospital of Tours, Tours, France

    Misylias Bouaoud, Annick Legras & Maeva Gourraud

  4. Medical-Surgical Intensive Care Unit and Inserm CIC 1435, Dupuytren Teaching Hospital, 87000, Limoges, France

    Bruno Evrard, Marine Goudelin & Philippe Vignon

Authors
  1. Matthieu Petit
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Misylias Bouaoud
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Edouard Jullien
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Adrien Joseph
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Bruno Evrard
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Cyril Charron
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Anousone Daulasim
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Annick Legras
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Maeva Gourraud
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Marine Goudelin
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Philippe Vignon
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Antoine Vieillard-Baron
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

MP, EJ, PV, and AVB designed the study; MP, EJ, CC, MP, MB, EJ, and MG collected the data; MP, AD, and AJ did the statistical analysis; MP and AVB wrote the manuscript; all authors reviewed the manuscript.

Corresponding author

Correspondence to Antoine Vieillard-Baron.

Ethics declarations

Ethics approval and consent to participate

The study protocol was approved by the ethics committee of the French Society of Intensive Care Medicine (ref SRLF CE 21–98), which waived the need for informed consent.

Consent for publication

Not applicable.

Competing interests

AVB reports personal fees from Air Liquide for clinical research. PV gave a lecture at a Baxter symposium during the 2022 SRLF congress.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Petit, M., Bouaoud, M., Jullien, E. et al. Right ventricular injury in patients with COVID-19-related ARDS eligible for ECMO support: a multicenter retrospective study. Ann. Intensive Care 14, 40 (2024). https://doi.org/10.1186/s13613-024-01256-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1186/s13613-024-01256-8

Keywords