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Review Article

A Systematic Review of Preexisting Sepsis and Extracorporeal Membrane Oxygenation

Sangli, Swathi S.*; Noronha, Shaun F.*; Mourad, Bashar; Jean, Raymonde; Bohman, John K.; Seelhammer, Troy G.

Author Information
doi: 10.1097/MAT.0000000000000934
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Abstract

Extracorporeal membrane oxygenation (ECMO) was initially developed as salvage therapy for refractory severe respiratory failure. In the past 4 decades, technologic advancements have facilitated the emergence of extracorporeal life support as accepted standard therapy for resuscitation and support. Medical indications include emergent temporary cardiopulmonary bypass, in-hospital cardiac arrest,1 bridge-to-transplant or placement of a ventricular assist device, refractory or severe hypercapnic respiratory failure,2 severe acute respiratory distress syndrome,3 and massive pulmonary embolism. When experienced clinicians implement it, ECMO decreases mortality among select patients. With recent technologic innovations, ECMO can now be mobilized for patients at medical centers that would otherwise be unable to provide ECMO services.

Despite the growing number of indications for ECMO, several contraindications still exist for its implementation, including poor prognosis before the primary indication, poor patient adherence to therapy, lack of reversibility without transplant candidacy, chronic organ dysfunction, and prolonged cardiopulmonary resuscitation (CPR) without adequate tissue perfusion.4,5 The definitive role of ECMO for patients with refractory septic shock is heterogeneous and undefined, lacking proper clinical studies for assessing its efficacy. Additionally, the Extracorporeal Life Support Organization (ELSO) registry does not identify sepsis as a primary indication for ECMO in adults, so it is difficult to determine the extent to which sepsis contributes to respiratory failure.5

Traditionally, septic shock has been viewed as a relative contraindication to ECMO support in adults because of limitations in providing adequate cardiac output in patients with vasodilation despite maximal ECMO blood flow.6,7 Furthermore, sepsis often results in a coagulopathic state that can exacerbate complications of bleeding and thrombosis during ECMO. The ECMO circuit can also harbor organisms and further delay resolution of the underlying infection.

Although primarily considered a supportive technology designed to improve oxygen delivery to end organs, ECMO provides other benefits. With use of an artificial oxygenator and carbon dioxide diffuser, ECMO improves acid–base status. In patients with sepsis, ECMO promotes cytokine immune homeostasis and limits the derangement of the coagulation response.8 This leads to decreased microthrombosis with resultant improvement in systemic perfusion and associated oxygen delivery.8 For patients with hemodynamic collapse, which often occurs in patients with septicemia, these measures can provide more time to respond to conventional treatment for the underlying infection.

Practitioners have limited evidence to guide them in the use of ECMO for adult patients with sepsis.9–11 The decision to use venovenous (VV) or venoarterial (VA) ECMO is determined case by case according to patient factors and cannulation protocols at centers where ECMO is used. The development of appropriate treatment algorithms has been hampered by the limited evidence. Given the high incidence of sepsis in intensive care units (ICUs), increased use of ECMO could tremendously increase hospital costs. Hence, it is important to understand whether the safe and effective use of ECMO gives patients more time to recover from their underlying illness and transient cardiomyopathy, leading to a mortality benefit.12 We retrospectively reviewed the published literature on ECMO studies of adult patients with sepsis, with or without cardiac dysfunction, as a primary indication for intervention and its association with mortality.

Materials and Methods

A comprehensive literature search of all pertinent, English-language studies published from January 1995 to September 2017 was undertaken in PubMed, Scopus, and Ovid MEDLINE databases using the following keywords: (“ECMO” OR “ECLS” OR “extracorporeal membrane oxygenation” OR “extracorporeal life support”) AND (“sepsis” OR “severe sepsis” OR “septic shock” OR “bacteremia” OR “septicemia”) AND (“mortality” OR “outcomes”). In addition, study personnel manually searched the resultant full texts for relevant review articles and original studies.

Selection Criteria

For the initial review, studies were considered eligible if they referred to the use of ECMO in patients with sepsis or septic shock. Studies were also eligible if they included patients with bacteremia who underwent ECMO for severe refractory cardiopulmonary dysfunction. The search was then restricted to studies reporting specific mortality data. Reviews, letters, correspondence, editorials, and studies on nonhuman animals were excluded. However, the reference lists of those articles were searched to identify other potential studies.

Study Selection and Data Abstraction

Two physician-reviewers independently reviewed and selected studies according to the inclusion criteria. Disagreement in study selection or data extraction was resolved with consensus. The following data were abstracted from each study independently by each reviewer, who used a standardized data collection form: author information, year of publication, study location, type of study, configuration of ECMO, outcomes, effect size, and other salient features.

Data Analysis

Considerable definitional, methodologic, and statistical differences between the studies precluded the use of meta-analytic techniques for collating the combined data. Instead, a qualitative analysis was used for a systematic review of the available studies that evaluated the outcomes of the use of ECMO in patients with sepsis or septic shock.

Results

A total of 389 studies were selected and screened; 10 were included for systematic review. Each is discussed below in chronologic order (Tables 1 and 2).

Rich et al.13 evaluated 100 adult patients with severe respiratory failure; 14% had sepsis, and 57% of those patients with sepsis required inotropic support after institution of ECMO. Further, the ECMO configuration was not specified in this study. Univariate analysis showed no significant difference in the incidence of concomitant organ dysfunction. Respiratory recovery or survival was not different between the groups (patients with sepsis versus patients without sepsis). Patients with positive blood cultures required more prolonged ECMO support than those without a positive blood culture.

A retrospective study of the ELSO registry performed by Brogan et al.14 analyzed 1,473 patients supported with ECMO for respiratory failure (2002–2006); a majority of the patients (78%) received VV ECMO. Of those who had sepsis between 2002 and 2006, 13 patients survived and 23 did not. The independent factors for improved survival included young age and VV ECMO; those for poor outcomes included arterial blood pH less than 7.16.

In a single-center, retrospective observational study, Bréchot et al.15 found that patients with severe bacterial septic shock who received ECMO had a mortality of 29% during their ICU stay. All these patients underwent VA ECMO. The 10 survivors included patients who received ECMO for refractory cardiovascular dysfunction and also had bacterial septic shock. Survivors were successfully weaned from ECMO with no further requirement for assist devices or cardiac transplant. At least one major ECMO-related complication occurred in 60% of patients. Median duration of ECMO support was 5 days (range, 2–12 days), and the median left ventricular ejection fraction was 60% when ECMO was successfully withdrawn. At 13 months of follow-up, the surviving patients had normal cardiac function with a documented good quality of life. Their physical disability was similar to that of a postmyocardial infarction group of patients, and their 36-Item Short Form Health Survey (SF-36) scores, from a generic health survey, were higher than scores for patients receiving long-term hemodialysis. The survivors and nonsurvivors were comparable for age, sex, body mass index, comorbidities, and immunocompromised status. Compared with survivors, nonsurvivors had higher (but not statistically different) Simplified Acute Physiology Score (SAPS) III and Sequential (Sepsis-Related) Organ Failure Assessment (SOFA) scores.

A retrospective single-center study by Huang et al.16 included 52 patients with refractory septic shock during a 6 year period (median age, 56.8 years; median body mass index, 24.1 kg/m2). Of these 52 patients, 40% had hemodynamic deterioration and cardiac arrest that required CPR before the decision was made to initiate ECMO. With septic shock as their primary indication, all the patients in this study received VA ECMO. The median age of the survivors was 43.8 years. Survival analysis showed that patients younger than 60 years had improved survival compared with patients 60 years or older (p = 0.029); 15% of the selected population survived to hospital discharge.

Cheng et al.9 conducted a retrospective study with 108 patients who had preexisting sepsis and received ECMO. They were matched by propensity score with 108 patients without sepsis who received ECMO. There was no disparity in overall survival between patients who had sepsis (28.7%) and those who did not (37.0%) (p = 0.192). In this population with sepsis, 44 patients underwent VV ECMO, and 132 required VA ECMO. Among the survivors with sepsis, survival was 24.4% for those who underwent VA ECMO and 45.5% among those who underwent VV ECMO. However, patients who receive VA ECMO usually have more cardiopulmonary compromise and a greater risk of death than patients who receive VV ECMO.

Park et al.17 evaluated 32 adult patients, all of whom received VA ECMO support for refractory septic shock, and found an overall survival of 22%. Myocardial injury with higher peak troponin levels was associated with lower in-hospital mortality (adjusted hazard ratio [HR], 0.34; 95% CI, 0.12–0.97). In cases where initiation of ECMO was delayed beyond 30.5 hours after the onset of shock (which occurred in 31% of patients), patients did not survive. Of the 32 patients, 14 required CPR, with only seven patients achieving return of spontaneous circulation before initiation of ECMO. Thirteen patients were successfully weaned from ECMO, and seven patients survived to hospital discharge. Compared with nonsurvivors, the survivors had a lower peak lactate level (4.5 vs. 15.1 mmol/L, p = 0.03), a lower median SOFA score on day 3 (15 vs. 18, p = 0.01), and a higher peak troponin I level (32.8 vs. 3.7 ng/ml, p = 0.02). In multivariable, adjusted models, CPR (adjusted HR, 4.61; 95% CI, 1.55–13.69; p = 0.006) was an independent predictor of in-hospital death after ECMO among patients with refractory septic shock.

Baek et al.19 evaluated 12 patients after kidney transplant who subsequently had sepsis necessitating ECMO. Indications for ECMO primarily included sepsis due to pneumonia with refractory cardiomyopathy (n = 9), stress-induced cardiomyopathy from fungemia (n = 1), and septic shock due to either urinary tract infection or unknown origin (n = 2); most patients (66%) required VV ECMO. The mean duration of ECMO support was 9.1 days (range, 3.5–15.1 days). Arterial blood pH before initiation was considerably lower among nonsurvivors. Of the immunosuppressed patients in this study, 50% were successfully weaned from ECMO.

Kim et al.18 studied the effect of bloodstream infections (BSIs) on ECMO catheter colonization among 126 adults who underwent ECMO. Of these patients, 27.7% were found to have a BSI during ECMO, with catheter colonization identified in 46.2% of the patients compared with 8.8% in the non-BSI group. The organisms responsible were primarily multidrug-resistant pathogens, including carbapenem-resistant Acinetobacter baumannii, methicillin-resistant Staphylococcus aureus (MRSA), and Candida tropicalis. Weaning success was significantly less among patients with BSIs compared with patients without BSIs (p < 0.001). In addition, 91% of the group without BSIs survived to hospital discharge, but weaning from ECMO was possible for only 46% of the BSI group, and only 7.7% of the BSI patients survived to hospital discharge.

In a study from Sweden20 of 255 adult patients with respiratory failure who received ECMO and had pre-ECMO sepsis, 64.4% survived to discharge. Among those survivors, 17% died within 3 months, but the remaining survivors had a favorable prognosis.

Vogel et al.21 reported a single-center experience of veno-arterio-venous ECMO for 12 patients with septic shock secondary to septic cardiomyopathy. Of the 12 patients, 42% had cardiac arrest before ECMO initiation. The median left ventricular function was 16.25%. In-hospital mortality was 25%; no reported deaths occurred during the 6 month follow-up period. These results were similar to those reported by Bréchot et al.15 In all the survivors, cardiac function returned to normal (left ventricular ejection fraction, 55–60%).

Discussion

Clinical studies describing the use of ECMO in patients with sepsis are limited. Two decades after Rich et al.13 reported on their experiences with ECMO for patients with sepsis, there is still no consensus on the role of ECMO in the management of septic shock. However, despite the widely disparate patient populations and study designs cited in our review, certain trends are worth noting.

Age

Accompanying the increased use of ECMO is a growing body of evidence of its use in patients with sepsis. The 2007 update from the American College of Critical Care Medicine recommended the use of ECMO for hemodynamic support of neonates with septic shock.22 Subsequently, a 2008 Cochrane analysis concluded that four trials showed an impressive 44% mortality benefit for infants.23 MacLaren et al.7 also reported a positive outcome among up to 75% of their pediatric patients until hospital discharge.

The evidence supporting use of ECMO in adults with sepsis is limited to small retrospective studies and anecdotal case reports.10,13,24 In general, older age appears to be a risk factor for poor outcomes among patients with sepsis who undergo ECMO, but the results are mixed. Rich et al.13 showed that advanced age was a risk factor for mortality. Huang et al.16 also found that in-hospital mortality was significantly different between older and younger patients with sepsis who were receiving ECMO (p = 0.017): None of the patients 60 years or older survived. Cheng et al.9 established that in-hospital mortality was higher among patients 55 years or older who had sepsis and received ECMO. However, when Park et al.17 studied adults who had sepsis and were receiving ECMO, patient age was not correlated with likelihood of survival. Similarly, the study by Bréchot et al.15 did not identify a correlation between patient age and survival. Even among patients without sepsis, advanced age was consistently an independent predictor of mortality for patients requiring ECMO.9,13,16

Organ Dysfunction

Sepsis, as defined by the Third International Consensus Definitions for Sepsis and Septic Shock (Sepsis-3) guidelines, is characterized by organ dysfunction. Park et al.17 showed that among patients with sepsis who received ECMO, patients with a higher SOFA score had higher mortality: By day 3, SOFA scores were higher for patients who did not survive compared with SOFA scores for patients who did survive (p = 0.01). Huang et al.16 and Cheng et al.9 did not find differences in SOFA scores at initiation of ECMO in their patient cohorts. However, those authors did not report SOFA scores after initiation of ECMO, which, according to Park et al.,17 is relevant for prognosticating survival. Bréchot et al.15 also identified a similar finding between SOFA score post-ECMO and survival of patients with sepsis: Survivors had improving SOFA scores, but nonsurvivors had worsening or static SOFA scores.

From the available data, for patients with sepsis, progression of the SOFA score appears to be a useful predictor of the response to ECMO as a temporizing measure in stabilizing cardiopulmonary abnormalities. Persistently increased SOFA scores after the start of ECMO may reflect the refractory nature of the underlying abnormality despite cardiopulmonary support with ECMO.

Cardiopulmonary Resuscitation

Not surprisingly, Park et al.17 found that the need for CPR (p = 0.009) and duration of CPR affected survival among patients with sepsis who received ECMO, and they found that survivors underwent shorter periods of CPR compared with nonsurvivors. Among patients who received CPR, only two survived to hospital discharge, and they received CPR for a total of only 4 and 5 minutes with a rapid return of spontaneous circulation. Investigators in Taiwan9 also showed that CPR performed while the patient was receiving ECMO was a predictor of mortality.

Extracorporeal Membrane Oxygenation Configuration

Despite the controversial use of VA ECMO, only a few case reports have reported the use of VA ECMO in patients with severe myocardial dysfunction due to sepsis.25,26 Cheng et al.9 found that among patients receiving VA ECMO, the risk of mortality was higher if they had sepsis compared with those who did not have sepsis. However, this difference between patients with and without sepsis did not exist for patients receiving VV ECMO, which suggests that either (1) VV ECMO is safer for patients with sepsis or (2) patients who required VA ECMO instead of VV ECMO have a higher risk of death.27 In support of the possibility that VV ECMO is safer, Baek et al.19 found that the survival rate was nearly 50% among patients who received VV ECMO and were immunocompromised and had sepsis-induced cardiomyopathy. Vogel et al.21 selected patients for a hybrid strategy with veno-arterio-venous ECMO for septic cardiomyopathy and demonstrated that this was a feasible rescue strategy for patients who had severe respiratory failure in combination with septic cardiomyopathy.

Myocardial Dysfunction

Anecdotal case reports have shown successful use of ECMO in patients with septic cardiomyopathy from toxic shock syndrome26 and from streptococcal sepsis.25 Cheng et al.9 found that myocarditis portended favorable outcomes for patients with sepsis who received ECMO; this finding is in agreement with the studies that portend a similar prognosis, despite a fulminant or catastrophic presentation, with a return of cardiac function to baseline. Park et al.17 reported similar findings, with survivors having higher percentages of myocardial damage compared with nonsurvivors. Interestingly, Baek et al.19 found that ECMO could be used as rescue therapy in immunosuppressed patients with severe refractory cardiopulmonary insufficiency due to severe sepsis. Bréchot et al.15 described eventual, successful weaning from ECMO for 12 of 14 patients who had confirmed sepsis-induced cardiomyopathy that was refractory to standard treatment.

One postulation is that this seemingly paradoxical effect of myocardial dysfunction predicting improved survival reflects the reversibility of myocardial dysfunction after ECMO (applied as a temporizing measure) facilitates improvement in cardiac function over time.17 This was demonstrated by Vogel et al.,21 with similar results as Bréchot et al., where all the survivors with septic cardiomyopathy had normal cardiac function upon follow-up.

We are familiar with two distinct hemodynamic patterns in early septic shock: peripheral vascular failure from vasoplegia resulting in microcirculatory dysfunction, which is distinct from septic cardiomyopathy with decreased ejection fraction.28 Studies have demonstrated that patients with sepsis and peripheral vascular failure have higher mortality.29 However, data are lacking about the usefulness of ECMO in this distinct subset of patients with vasoplegia.

Biomarkers

Several studies identified the utility of biomarkers in predicting mortality in patients with sepsis who received ECMO. Bréchot et al.15 found that the procalcitonin levels in survivors were lower than in nonsurvivors (41 vs. 164 ng/ml, p = 0.008). MacLaren et al.10 and Park et al.17 found lower peak lactate levels among survivors than among nonsurvivors, again underlining the prognostic utility of this test in patients with sepsis. Severe acidosis before administration of ECMO in patients with severe sepsis was a predictor of failure to wean patients from ECMO.9,13,16 Park et al.17 found that patients with higher peak troponin levels had lower in-hospital mortality, a finding not reported in other studies. However, elevated troponin levels may reflect the prevalence of myocarditis in these patients, who have improved survival, as opposed to troponin being an independent predictor of survival.

Bacteremia

The most common nosocomial infection during ECMO is bacteremia. The lack of clinical signs and symptoms in patients with these nosocomial infections presents a diagnostic challenge.30 As mentioned above, Kim et al.18 found that 90.5% of the group without BSI survived to hospital discharge, but weaning from ECMO was possible for less than half the BSI group, which suggests that bacteremia is a crucial factor for patients receiving ECMO. Patients with sepsis who receive ECMO have numerous risk factors for bacteremia and multiorgan failure (Figure 1). A single center30–32 reported that bacteremia or BSIs predominated over soft tissue infections, respiratory infections, and urinary infections. During ECMO, the risk factors include multiple indwelling catheters, including arterial catheters (pulmonary and radial)33; high-risk intravascular devices, including intraaortic balloon pumps34 and left ventricular assist devices35; and indwelling ECMO cannulas. In addition to the different catheters, the risk factors depend on multiple variables, including the insertion technique, the duration that the vascular catheters or devices are used, and the duration of ECMO itself. Duration of ECMO was a risk factor for a higher incidence of bacteremia.30

Figure 1
Figure 1:
Risk factors for bacteremia in patients with sepsis who are undergoing ECMO. Multiorgan failure commonly includes the kidneys, liver, heart, and lungs. ABG, arterial blood gas; ECMO, extracorporeal membrane oxygenation; WBC, white blood cell count. (Used with permission of Mayo Foundation for Medical Education and Research.)

In a retrospective study conducted in a tertiary care center by a group of Japanese investigators, bacteremia was associated with catheter colonization and poorer outcomes.18 Although those investigators could not identify a causal relationship between bacteremia and infection related to ECMO catheters, the study emphasized that ECMO catheters often became colonized in patients with bacteremia. Extracorporeal Life Support Organization registry data showed similar results with more infectious complications in patients who had a positive culture before ECMO was started.36

The role of antibiotic prophylaxis and daily surveillance cultures in management of ECMO patients is unclear. A study in Canada supported the use of daily surveillance cultures as an alternative to antibiotic prophylaxis because of the higher mortality among patients with BSI.37 This finding is consistent with the ELSO registry study by Vogel et al.,36 although they emphasized that this intervention led to a cost difference for patients with and without sepsis. With no clearly defined guidelines on this matter, practice continues to be variable.38

Infectious Complications with Extracorporeal Membrane Oxygenation

Vogel et al.36 assessed the risk of infectious complications with ECMO and reported that patients who had bacteremia before ECMO cannulation had a significant risk for infectious complications (odds ratio [OR], 2.12; 95% CI, 1.92–2.34; p < 0.001). They were also more likely to have a multidrug-resistant organism during ECMO (resistant Gram-negative rods: OR, 3.09 and 95% CI, 2.62–3.64; MRSA: OR, 5.77 and 95% CI, 4.04–8.24; fungi: OR, 4.37 and 95% CI, 3.63–5.26).

Despite this, limited data are available to support the use of routine antibiotic prophylaxis. Furthermore, the type of antibiotics used for prophylaxis varies widely.38 Given the lack of prospective trials, the question arises as to whether antibiotic prophylaxis should be targeted toward causative organisms identified in certain studies, including nosocomial pathogens, multidrug-resistant organisms, and fungal pathogens.18,39–41 Future research is required to further elucidate the use of prophylaxis and antimicrobial agent selection and to define the duration of therapy in patients receiving ECMO.

Sepsis Definitions and Extracorporeal Membrane Oxygenation

Evidence is scarce for defining sepsis in patients receiving ECMO, and validation data do not exist for accepted sepsis criteria for patients supported with this technology. Further, patients with refractory severe cardiopulmonary failure who are receiving ECMO often have considerable pathophysiologic overlap with patients in septic shock; this may impair the utility of the Sepsis-3 criteria for detection of the onset of sepsis in patients supported with ECMO. With these concerns about the generalizability of the Sepsis-3 definition to the ECMO population, further validation of this definition for patients receiving ECMO is necessary.

Limitations

The studies included in this review specifically focusing on the adult population were retrospective and mostly conducted at single centers. Investigations of how ECMO affects survival of patients with sepsis undeniably involve selection bias. Use of an adequately matched control group of patients with sepsis and refractory respiratory or cardiac failure is unrealistic.

These studies, which cannot be generalized to a widespread ECMO adult population given the differences in treatment regimens at different ECMO centers, draw attention to the need for robust prospective efficacy trials to determine the utility of ECMO in sepsis. Such trials would benefit from data from multiple sites or, alternatively, from a single, large-volume ECMO center, where factors such as marked heterogeneity would not contribute to different results as illustrated by a recent survey.42 Well-designed retrospective studies that include detailed information on SOFA scores, circuit configurations, and shock state (cardiogenic versus distributive) would also be informative. Remaining concerns include the optimal timing of ECMO initiation in patients with sepsis, the effect of BSI on ECMO catheters, and the subsequent outcomes.

Conclusions

This systematic review reported on all studies in the English-language medical literature describing the use of ECMO in patients with sepsis and septic shock and showed that few published data exist on the use of ECMO in these patients despite the frequent pathophysiologic overlap between patients who could benefit from ECMO and patients who have sepsis or septic shock. The published studies do not present well-defined patterns supporting the use of ECMO in these patients, and the results are limited by sample size and disparate study designs. With the increased availability of ECMO in more medical centers and for more indications, a well-designed, prospective study should be performed to better characterize patients with sepsis who may benefit from ECMO.

Table 1
Table 1:
Study Type, Patient Profile, and Outcome
Table 2
Table 2:
Characteristics of Patients and Studies

References

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Keywords:

ECMO; ECMO in sepsis; extracorporeal membrane oxygenation; septic shock; septic shock with ECMO

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