Review Article

Right ventricular dysfunction during acute respiratory distress

syndrome and veno-venous extracorporeal membrane
oxygenation
Jeroen J. H. Bunge1, Kadir Caliskan2, Diederik Gommers1, Dinis Reis Miranda1
1
Department of Intensive Care, 2Department of Cardiology, Erasmus MC University Medical Center, Rotterdam, The Netherlands
Contributions: (I) Conception and design: All authors; (II) Administrative support: None; (III) Provision of study materials or patients: None; (IV)
Collection and assembly of data: JJ Bunge, D Reis Miranda; (V) Data analysis and interpretation: None; (VI) Manuscript writing: All authors; (VII)
Final approval of manuscript: All authors.
Correspondence to: Dinis Reis Miranda, MD, PhD. Department of Intensive Care, Erasmus MC, Room H-619, s Gravendijkwal 230, 3015 CE,
Rotterdam, The Netherlands. Email: [Link]@[Link].

Abstract: Severe ARDS can be complicated by right ventricular (RV) failure. The etiology of RV failure
in ARDS is multifactorial. Vascular alterations, hypoxia, hypercapnia and effects of mechanical ventilation
may play a role. Echocardiography has an important role in diagnosing RV failure in ARDS patients. Once
extracorporeal membrane oxygenation (ECMO) is indicated in these patients, the right ECMO modus
needs to be chosen. In this review, the etiology, diagnosis and management of RV failure in ARDS will be
briefly outlined. The beneficial effect of veno-venous (VV) ECMO on RV function in these patients will be
illustrated. Based on this, we will give recommendations regarding choice of ECMO modus and provide an
algorithm for management of RV failure in VV ECMO supported patients.

Keywords: Acute respiratory distress syndrome (ARDS); human; extracorporeal membrane oxygenation (ECMO);
veno-venous extracorporeal membrane oxygenation (VV ECMO); heart failure; right sided; cor pulmonale

Submitted Aug 14, 2017. Accepted for publication Oct 11, 2017.
doi: 10.21037/jtd.2017.10.75
View this article at: [Link]

Introduction associated with mortality (1,4,5); other groups did not find
a significant contribution to mortality (6,7). The conflicting
Acute respiratory distress syndrome (ARDS) is frequently
findings can be explained by differences in study population,
complicated by pulmonary hypertension causing right
different definitions of RV failure, and sample size. If RV
ventricular (RV) failure (1). Symptoms are determined by
failure results in true circulatory impairment, it is a likely
low cardiac output and/or systemic venous congestion. Low
cardiac output can result in organ failure and hemodynamic contributor to morbidity and mortality.
collapse. Recently, venous congestion is more and more In the severe ARDS population referred for veno-venous
acknowledged as an important contributor to organ failure extracorporeal membrane oxygenation (VV ECMO),
in both heart failure and septic shock patients. RV failure pulmonary hypertension or RV failure may be present
results in systemic congestion with a detrimental effect in more than half of patients and seems associated with
particularly on kidney and liver function (2,3). mortality (8). This will influence patient management
There are conflicting reports on the incidence of regarding choice of ECMO modus [VV, veno-arterial (VA)
RV failure in ARDS, and how it affects prognosis in the or veno-arterial and venous (VAV)], and circulatory support
current era of lung protective ventilation. Depending on and ventilator settings after ECMO initiation. There is
definition, the incidence of RV failure in ARDS is 10–25%. limited literature on management of RV failure during VV
Whereas several groups found RV failure in ARDS to be ECMO support. This review briefly outlines the underlying

© Journal of Thoracic Disease. All rights reserved. [Link] J Thorac Dis 2018;10(Suppl 5):S674-S682
Journal of Thoracic Disease, Vol 10, Suppl 5 March 2018 S675

mechanisms of RV failure in ARDS and its general Effects of mechanical ventilation on RV function
management. Hereafter, it will focus on how it impacts
There has been much debate about which component of
on choice of ECMO modus and patient management on
mechanical ventilation is the most important determinant
ECMO support.
of RV afterload: Pplateau, mean airway pressure, or lung
volume and Vt. The relationship between lung volume and
Causes of RV failure during ARDS RV impedance in normal lungs is a U-shaped curve, with the
lowest RV impedance found around FRC (20). Therefore,
Factors directly related to the respiratory disease as well
lung overdistension by high airway pressures results in
as the effects of mechanical ventilation may influence
increased RV afterload. In damaged, low compliant lungs,
pulmonary vascular function and form a complex interplay
intra-alveolar pressures will not necessarily result in
in RV afterload. Moreover, mechanical ventilation can
overdistension and not be fully transmitted to the pleural
influence RV preload as well. Apart from RV pre- and
space. Indeed, Vieillard-Baron et al. (21) demonstrated that
afterload, RV function may also directly be negatively
affected by sepsis (septic cardiomyopathy) and metabolic Vt is the main determinant of RV afterload in ARDS and
derangements like acidosis which will not be discussed in not airway pressure per se. Moreover, Vt and not Pplateau
this review (9-11). was significantly correlated with occurrence of RV failure
in 145 ARDS patients included in the French pulmonary
artery catheter study (6). Clearly, low Vt is recommended in
Pulmonary vascular determinants of RV afterload in all ARDS patients to prevent VILI, and the right ventricle
ARDS will benefit from a low Vt strategy as well.
Microvascular obstruction in the lung is often present Apart from afterload, mechanical ventilation may also
in ARDS (12,13). This obstruction can be caused by influence RV preload. If a high Vt or inappropriate high
pulmonary vasoconstriction or by pulmonary capillary PEEP level results in an increase in pleural pressure, part
coagulation. Hypoxic pulmonary vasoconstriction, which of this pressure will be transmitted to the superior vena
is a fast acting adaptive response, decreases blood flow cava and right atrium, resulting in diminished venous
in poorly aerated parts of the lung, improving V/Q return (22).
match. However, in a state of generalized hypoxia due to PEEP works as a two-sided sword. Too low PEEP
severe lung injury, as in severe pneumonia or ARDS, it will result in atelectasis with a detrimental effect on RV
contributes to increased RV afterload (14). Furthermore, afterload. In a rat model, apart from increased afterload,
in ARDS, an imbalance in mediators of vascular tone like atelectasis was linked to vascular leak and progressive
eNOS, endothelins and prostanoids, causes a shift towards lung injury as well (23). In contrast, using the open lung
vasoconstriction (14,15). concept in adequately fluid resuscitated post cardiac surgery
Lung protective ventilation, using low tidal volume patients, PEEP of 14±4 cmH 2O was well tolerated and
(Vt) and low plateau pressures (Pplateau), may result in did not increase RV impedance compared to conventional
hypercapnia in ARDS patients. Hypercapnia causes a ventilation with a PEEP of 5 cmH2O (24). The key is that
significant increase of pulmonary arterial pressure (16), high PEEP did achieve full lung recruitment in these post
and severe hypercapnia was recently found to be an cardiac surgery patients and was combined with very low Vt
independent predictor of mortality in moderate to severe (4–6 mL/kg), so regional overdistension by Vt did not occur
ARDS (17). and impact of Vt on RV impedance was minimal. In ARDS,
Postmortem histological studies have shown however, the disease is usually not homogenously distributed
microvascular thrombi in early phases of ARDS, and and a large part of the lung may not react to recruitment. In
loss of capillaries in later phases of ARDS (18). The that situation, too high PEEP in combination with normal
links between microvascular alterations, coagulopathy Vt may result in regional tidal overdistension without
and inflammation in ARDS are complex, not yet fully reversing atelectasis, increasing RV afterload. We therefore
understood and beyond the scope of this review (19). believe that increasing PEEP only benefits the patient if it
However, microvascular thrombi and loss of capillaries is accompanied by an increase in lung compliance, as a sign
will contribute to an increase of total pulmonary vascular of successful reversal of atelectasis not counterbalanced by
resistance. regional overdistension (25).

© Journal of Thoracic Disease. All rights reserved. [Link] J Thorac Dis 2018;10(Suppl 5):S674-S682
S676 Bunge et al. RV failure in ARDS and VV-ECMO

Table 1 Commonly used echo parameters of RV failure in ARDS

Echo parameter Normal RV/pulmonary vascular dysfunction

RV Systolic function

TAPSE (tricuspid annulus systolic excursion) (mm) >15 <15

TDI S’ lateral tricuspid annulus (cm/s) >10 <10

RV dilatation

RVEDA/LVEDA* <0.6 >0.6; >1.0 (severe)

RV afterload
†
Systolic PA pressure (RVSP) (mmHg) <30 >30

Paradoxical septal motion (end systolic) Absent Present

†
*, right ventricular end diastolic area/left ventricular end diastolic area; , systolic PA pressures equal right ventricular systolic pressure in
2
absence of pulmonary stenosis; RVSP = 4 × max velocity tricuspid regurgitation + estimated right atrial pressure. RV, right ventricular; PA,
pulmonary artery.

How to diagnose increased RV afterload, and describes a situation where

RV dilatation may compromise LV filling. There are
There are several modalities to assist in diagnosis and
several echocardiographic definitions of ACP. A widely
management of increased RV afterload and RV failure in
adopted definition is the presence of both paradoxical
patients with severe ARDS.
septal movement and RV dilatation (RVEDA/LVEDA
>0.6 ACP; RVEDA/LVEDA >1 severe ACP) (7). However,
Echocardiography large interobserver variability and poor correlation with
MRI derived RV volumes have been reported for RVEDA
Echocardiography is a quick noninvasive tool to monitor the
measurements and this may partly explain contradicting
right ventricle. Both transthoracic echocardiography (TTE) findings regarding the impact of ACP on prognosis (29).
and transesophageal echocardiography (TEE) can be used,
although TTE often delivers suboptimal images in these
patients. Common echocardiographic parameters include Pulmonary artery catheter (PAC)
indexes of dilatation, systolic function and RV afterload and A PAC or Swan-Ganz catheter can be of great value in
are listed in Table 1. Full echocardiographic work-up of RV both diagnosis and management of ARDS patients with
and pulmonary vascular function has been well described by suspected RV failure. Apart from measuring CVP, PA and
Kaplan et al. (26). RV impedance is adequately reflected by PA occlusion pressure (PAOP), it can measure the most
pulmonary artery (PA) flow patterns. PA acceleration time important consequence of pulmonary vascular and RV
correlates with mean PA pressure, with PA acceleration time dysfunction: reduced stroke volume and cardiac output.
>120 ms considered normal in the general population and Continuous measurements are useful to monitor response
values <100 ms indicating mean PA pressure >28 mmHg to treatment alterations. A CVP higher than PAOP is a
(26,27). Mean acceleration time, which is the ratio between clear sign of RV failure, and a condition in which fluid
peak PA flow and acceleration time, has been experimentally loading can have a detrimental effect on cardiac output and
validated to correlate with RV impedance, with a decrease venous congestion.
in mean acceleration time reflecting an increase in Pulmonary vascular resistance [(PVR) = (meanPAP −
afterload, and can be used for follow up after adjustment PAOP)/cardiac output] measured with Swan-Ganz catheter
of ventilator settings or other interventions (21,24,28). No is not a good reflection of true RV afterload due to the
normal values of the mean acceleration time are known yet. high capacitance of the pulmonary vessels. Increase of
In our experience, values between 9.5 and 11 m/s2 during flow (cardiac output) easily recruits total pulmonary vessel
expiration are normal. diameter without much increase of PA pressures (30,31).
Acute cor pulmonale (ACP) is a result of (acute) Transpulmonary pressure gradient [(TPG), mPAP − PAOP]

© Journal of Thoracic Disease. All rights reserved. [Link] J Thorac Dis 2018;10(Suppl 5):S674-S682
Journal of Thoracic Disease, Vol 10, Suppl 5 March 2018 S677

is a flow sensitive parameter as well (32). However, an before choosing the right ECMO modus, the main origin
increase in TPG >12 was independently associated with of circulatory failure should be determined: is it cardiogenic
mortality in ARDS patients in the FACCT trial (33). shock due to severe RV failure, cardiogenic shock due to left
heart disease or septic shock with adequate cardiac output?
Of course, combinations of these factors may be present, i.e.,
Management of RV failure in ARDS
left and right sided heart failure due to concurrent septic
There are several reviews on this topic (34,35). General shock with septic cardiomyopathy in a patient with ARDS
management include: fluid optimization, inotropes, and high RV afterload. In the presence of shock due to
adjustment of ventilator settings and consideration of prone severe LV failure, VA ECMO is indicated (Figure 1).
positioning and inhaled Nitric Oxide (iNO). VV ECMO leads to an improvement of RV failure,
Fluid optimization is crucial, as a failing right ventricle may as shown in a study of our group (43). In this study, 13
initially benefit from fluid. However, fluid overloading may consecutive patients with severe respiratory failure were
have a detrimental effect in these patients, worsening systemic given a PAC before VV ECMO cannulation. Immediately
congestion and thereby aggravating organ dysfunction. after start of VV ECMO, PA pressures dropped significantly
Moreover, fluid overloading promotes further RV dilatation, before ventilator settings were altered, followed by a slight
thereby compromising LV filling and output. Pulse pressure drop in CVP and an increase in cardiac index, under stable
variation, often used as an indicator for fluid responsiveness, dose of vasopressors. Both oxygenation and decarboxylation
can be falsely elevated and may not be a good indicator of play a role here. Hypoxic pulmonary vasoconstriction
fluid responsiveness in patients with severe RV failure (36). reacts quickly to altered precapillary pO2 (15). In contrast,
Vasopressors and inotropes are the second step in reducing ECMO sweep gas flow induced an increase of
management of RV failure related shock. Norepinephrine systolic PA pressures in an earlier study in ten ARDS
increases preload by increasing systemic filling pressure, patients as shown by Schmitt et al. (44). Another illustration
increases arterial blood pressure and increases right of the effect of CO2-removal comes from a study on an
coronary perfusion. Dobutamine and phosphodiesterase ARDS model in pigs, in which low flow extracorporeal CO2
inhibitors stimulate RV contractility and increase cardiac removal (ECCO2R) reduced PA pressures and improved
output. Levosimendan, a calcium sensitizer, showed RV function (45).
beneficial effects on mean PA pressure, RV function and Since normalizing arterial pO 2, pCO 2 and pH may
cardiac output in a pilot randomized trial in 35 patients with have a beneficial effect on cardiac contractility as well, we
ARDS and septic shock (37). recommend starting VV ECMO for respiratory failure,
iNO diminishes PA pressures, and positively influences even in the presence of shock due to RV failure. If shock
V/Q matching. However, clinical trials have failed to prove does not improve during VV ECMO and cardiac failure is
a net benefit in terms of mortality or days on mechanical the reason for shock, then placement of an arterial cannula
ventilation (38). There may be a niche indication in selected and switching to VAV-modus is recommended (Figure 1).
patients with severe RV failure, although meta-analyses have The fact that the vast majority of ARDS patient can be
shown an association with kidney injury and need for renal initiated on VV ECMO is illustrated by a study based on
replacement therapy after prolonged use of iNO (39,40). the ELSO registry, in which only 18% of ARDS patients
As outlined in the previous chapter, Vt should be with shock (one or more inotrope/vasopressor) were started
limited. PEEP and Pplateau should be on such level that on VA ECMO, and this percentage seemed dropping over
unnecessary derecruitment is avoided. Prone positioning the years. The rate of conversion from VV to VA ECMO in
is recommended in severe ARDS to improve oxygenation, this study was low: 4.1% (46). Furthermore, a recent study
ventilation and prognosis (41). It was shown to reduce of 17 ARDS patients on vasopressors qualifying for VV
RV afterload as well, as described by Vieillard-Baron and ECMO, reported a significant decrease in total vasopressor
colleagues (42). score after initiation of VV ECMO and no conversions to
VA ECMO (47).

Initiating ECMO in ARDS patients with RV failure

RV failure while on VV ECMO
In patients with ARDS and RV failure, VV ECMO can
generally be safely chosen as initial strategy. However, If RV failure progresses during VV ECMO, one has to

© Journal of Thoracic Disease. All rights reserved. [Link] J Thorac Dis 2018;10(Suppl 5):S674-S682
S678 Bunge et al. RV failure in ARDS and VV-ECMO

Severe ARDS with indication for ECMO

No signs of shock Signs of shock

lsolated respiratory failure High inotropes/vasopressors, low urinary output/acute
kidney injury, high lactate

Identify type
of shock
Echocardiography, PA catheter

RV failure/Acute cor pulmonale Septic shock LV/biventricular

Adequate cardiac output failure

VV ECMO VA ECMO

Figure 1 Algorithm for choice of ECMO modus. ARDS, adult respiratory distress syndrome; ECMO, extracorporeal membrane
oxygenation; VV, veno-venous; VA, veno-arterial; RV, right ventricular; LV, left ventricular; PA, pulmonary artery.

rethink the etiology since VV ECMO usually improves RV et al. (52) found an association with survival comparing
failure. First of all, ventilator settings can be adjusted, aiming high PEEP during the first 3 days of ECMO versus low
for low Vt, far beyond 6 mL/kg, as Vt is a major determinant PEEP. Furthermore, Guervilly et al. (53) showed that prone
of RV afterload. Although there is not much evidence positioning improved oxygenation in 15 ARDS patients
on ventilator settings while on VV ECMO, the Xtravent on VV ECMO, the authors did not report RV function in
study showed that ultralow Vt of 3 mL/kg combined with this study, but it could in theory decrease RV afterload as in
ECCO2R is safe, and resulted in more ventilator free ARDS patients without ECMO. Finally, the original lung
days in ARDS patients with PaO2/FiO2 ≤150 compared to disease may progress and thereby increase RV afterload, as
conventional lung protective ventilation (48). we have seen a few times in our practice.
There are several other causes of progressive RV failure When reversible causes of progressive RV failure
that need to be considered (Figure 2). Fluid overload can have been adequately addressed, and inotropes alone did
exacerbate RV failure. In general, fluid balance should be not improve the situation enough, one has to consider
as neutral as possible in ARDS patients, with or without mechanical support. Pappalardo et al. (54) reported
ECMO (49,50). Pulmonary emboli can occur, especially beneficial effects of inserting an intra-aortic balloon pump
when anticoagulation has not been adequate or thrombus (IABP) in a small group of patients with RV or biventricular
has been identified in the reinfusion cannula or the failure on VV ECMO. IABP insertion resulted in lower
reinfusion site of the membrane. Lowering of PEEP and CVP and inotrope score. Improvement of right coronary
Vt after initiation of VV ECMO may cause derecruitment, perfusion in the pressure overloaded right ventricle may be
thereby increasing RV afterload. Indeed, experts advise to part of the explanation of its effect. The alternative or next
maintain PEEP on a relatively high level (15 cmH2O) after step is switching ECMO modus. Our approach is to switch
starting VV ECMO in severe ARDS (51), and Schmidt from VV- to VAVECMO by adding an arterial cannula.

© Journal of Thoracic Disease. All rights reserved. [Link] J Thorac Dis 2018;10(Suppl 5):S674-S682
Journal of Thoracic Disease, Vol 10, Suppl 5 March 2018 S679

Progressive circulatory failure while on VV ECMO

lactate , vasopressors , urinary output

Aim for low Vt

(<6 mL/kg)

YES NO
Echocardiography:
RV failure?

Further diagnostic work-up (chest X-ray/CT- Consider:

scan) to rule out/in: - Septic shock/new infection
- Fluid overload - Hypovolemia
- Pulmonary emboli - Neurological complication
- Derecruitment/atelectasis
- Progression of respiratory
disease

Add arterial canula

and switch to VA VECMO
Reversible causes
adequately addressed

Figure 2 Management of circulatory failure after starting VV ECMO. VV ECMO, veno-venous extracorporeal membrane oxygenation; Vt,
tidal volume; RV, right ventricular; VAV, veno-arterial and venous.

The venous return cannula should be partially clamped to The ASD closed spontaneously after transplantation.
redirect most of the flow towards the artery, the VV-flow There are no reports of using this strategy in patients with
being usually one third of the total ECMO blood flow. An ARDS or other condition awaiting recovery instead of
alternative is to switch to VA-modus, using the subclavian transplantation. There is a risk of a residual ASD that needs
artery for the arterial cannula. These two ECMO to be closed afterwards.
configurations prevent risk for Harlequin syndrome, which
may occur with peripheral VA ECMO: supply of hypoxic
Conclusions
blood to the upper part of the body and brain due to poor
oxygenation of residual cardiac output. Hypoxia, hypercarbia, and the effects of mechanical
A rarely practiced solution for RV failure whilst on ventilation, most importantly Vt, determine RV afterload.
VV ECMO is to create an ASD by percutaneous balloon Atelectasis can contribute as well. Although RV failure is
atrial septostomy. This way, a right to left atrial shunt of a major concern in patients with severe ARDS, it is less
oxygenated blood is created, unloading the right ventricle. a concern whilst starting ECMO support. VV ECMO
This procedure has been described in one case report in has a beneficial effect on RV afterload by oxygenation,
a patient on VV ECMO with pulmonary fibrosis on the decarboxylation and normalization of pH. This improves
waiting list for lung transplantation (55). RV function RV function and hemodynamics. Furthermore, Vt and peak
improved and the patient could be weaned of all inotropes. airway pressures can be reduced, additionally decreasing

© Journal of Thoracic Disease. All rights reserved. [Link] J Thorac Dis 2018;10(Suppl 5):S674-S682
S680 Bunge et al. RV failure in ARDS and VV-ECMO

afterload. Therefore, if ECMO is indicated in severe 7. Vieillard-Baron A, Schmitt JM, Augarde R, et al. Acute cor
ARDS, we recommend VV ECMO as initial approach. If pulmonale in acute respiratory distress syndrome submitted
RV failure further deteriorates while on VV ECMO, despite to protective ventilation: incidence, clinical implications, and
addressing reversible factors and treatment with inotropes, prognosis. Crit Care Med 2001;29:1551-5.
diuretics and prone positioning has been considered, then 8. Lazzeri C, Cianchi G, Bonizzoli M, et al. Right ventricle
VA- or VAV-ECMO is indicated. dilation as a prognostic factor in refractory acute
respiratory distress syndrome requiring veno-venous
extracorporeal membrane oxygenation. Minerva Anestesiol
Acknowledgements
2016;82:1043-9.
None. 9. Parker MM, McCarthy KE, Ognibene FP, et al. Right
ventricular dysfunction and dilatation, similar to left
ventricular changes, characterize the cardiac depression of
Footnote
septic shock in humans. Chest 1990;97:126-31.
Conflicts of Interest: D Gommers is a member of the medical 10. Hunter JD, Doddi M. Sepsis and the heart. Br J Anaesth
advisory board of Novalung and received travel expenses 2010;104:3-11.
and fees for giving oral presentations from Novalung and 11. Chan CM, Klinger JR. The right ventricle in sepsis. Clin
Maquet; D Reis Miranda received speaking fees for oral Chest Med 2008;29:661-76, ix.
presentation from Novalung and Hillrom. The other 12. Vesconi S, Rossi GP, Pesenti A, et al. Pulmonary
authors have no conflicts of interest to declare. microthrombosis in severe adult respiratory distress
syndrome. Crit Care Med 1988;16:111-3.
13. Tomashefski JF, Jr., Davies P, Boggis C, et al. The
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Cite this article as: Bunge JJ, Caliskan K, Gommers D,

Reis Miranda D. Right ventricular dysfunction during acute
respiratory distress syndrome and veno-venous extracorporeal
membrane oxygenation. J Thorac Dis 2018;10(Suppl 5):S674-
S682. doi: 10.21037/jtd.2017.10.75

© Journal of Thoracic Disease. All rights reserved. [Link] J Thorac Dis 2018;10(Suppl 5):S674-S682