Research Article

Blood Purif 2020;49:341–347 Received: July 3, 2019

Accepted: October 18, 2019
DOI: 10.1159/000504287 Published online: December 19, 2019

Outcomes among Patients Treated with Renal

Replacement Therapy during Extracorporeal
Membrane Oxygenation: A Single-Center
Retrospective Study

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David N. Dado a, e Craig R. Ainsworth f Sarah B. Thomas b Benjamin Huang a
Lydia C. Piper b Valerie G. Sams b Andriy Batchinsky c, d Benjamin D. Morrow a, e
Anthony P. Basel f Robert J. Walter a, e Phillip E. Mason b Kevin K. Chung e
a Department of Medicine, San Antonio Military Medical Center, San Antonio, TX, USA; b Department of Surgery and
Trauma, San Antonio Military Medical Center, San Antonio, TX, USA; c The Geneva Foundation, Tacoma, WA, USA;
d U. S. Army Institute of Surgical Research, Ft. Sam Houston, San Antonio, TX, USA; e Department of Medicine, Uniformed

Services University, Bethesda, MD, USA; f Burn Center, U. S. Army Institute of Surgical Research, San Antonio, TX, USA

Keywords Results: The demographic and clinical data of 92 patients

Extracorporeal membrane oxygenation · Extracorporeal who underwent ECMO at our center were reviewed includ-
life support · Acute kidney injury · Continuous renal ing primary diagnosis, indications for and mode of ECMO
replacement therapy · Acute respiratory distress syndrome support, illness severity, oxygenation index, vasopressor re-
quirement, and presence of acute kidney injury. In those pa-
tients that required ECMO with CRRT, we reviewed urine out-
Abstract put prior to initiation, modality used, prescribed dose, net
Background: Extracorporeal membrane oxygenation fluid balance after 72 h, requirement of renal replacement
(ECMO) and continuous renal replacement therapy (CRRT) therapy (RRT) at discharge, and use of diuretics prior to RRT
are modalities used in critically ill patients suffering organ initiation. Our primary endpoint was survival to hospital dis-
failure and metabolic derangements. Although the effects of charge. During the study period, 48 patients required the
CRRT have been extensively studied, the impact of simulta- combination of ECMO with CRRT. Twenty-nine of these pa-
neous CRRT and ECMO is less well described. The purpose of tients survived to hospital discharge. Of the 29 survivors, 6
this study is to evaluate the incidence and the impact of were dialysis dependent at hospital discharge. The mortality
CRRT on outcomes of patients receiving ECMO. Methods: A rate was 39.5% with combined ECMO/CRRT compared to
single center, retrospective chart review was conducted for 31.4% among those receiving ECMO alone (p = 0.074). Of
patients receiving ECMO therapy over a 6-year period. Pa- those receiving combined therapy, nonsurvivors were more
tients who underwent combined ECMO and CRRT were com- likely to have a significantly positive net fluid balance at 72 h
pared to those who underwent ECMO alone. Intergroup (p = 0.001). A multivariate linear regression analysis showed
­statistical comparisons were performed using Wilcoxon/ net positive fluid balance and increased age were indepen-
Kruskal-Wallis and chi-square tests. Logistic regression was dently associated with mortality. Conclusions: Use of CRRT
performed to identify independent risk factors for mortality. is prevalent among patients undergoing ECMO, with over

© 2019 The Author(s) David N. Dado, DO

Published by S. Karger AG, Basel San Antonio Military Medical Center
3551 Roger Brooke Drive, JBSA-Fort Sam Houston
[email protected] This article is licensed under the Creative Commons Attribution-
NonCommercial-NoDerivatives 4.0 International License (CC BY- San Antonio, TX 78234 (USA)
www.karger.com/bpu E-Mail david.n.dado.mil @ mail.mil
NC-ND) (http://www.karger.com/Services/OpenAccessLicense).
Usage and distribution for commercial purposes as well as any dis-
tribution of modified material requires written permission.
50% of our patient population receiving combination thera- The decision to initiate RRT is not without risk. While
py. Fluid balance appears to be an important variable associ- 2 large ECMO center studies showed no incidence of end-
ated with outcomes in this cohort. Rates of renal recovery stage renal disease in the absence of primary renal disease
and overall survival were higher compared to previously among pediatric patients receiving combined ECMO and
published reports among those requiring combined ECMO/ CRRT therapy over a 20-year follow-up, outcomes in adult
CRRT. © 2019 The Author(s) patients remain poorly defined [19–20]. The purpose of
Published by S. Karger AG, Basel this study was to conduct a single-center retrospective re-
view of adult patients receiving combined ECMO and
CRRT. We hypothesized that a high number of patients
Introduction receive concurrent ECMO and CRRT and that ECMO pa-
tients who receive CRRT have a higher mortality.
Extracorporeal membrane oxygenation (ECMO) is a
life-saving therapy being used more frequently in criti-
cally ill patients, allowing for removal of carbon dioxide Materials and Methods
while providing oxygenation and circulatory support [1,

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2]. Due to the underlying severity of illness, these pa- This study was approved by the Brooke Army Medical Center
tients are at high risk of developing acute kidney injury Institutional Review Board. This is a retrospective analysis of all
adult patients admitted to the San Antonio Military Medical
(AKI) as well as fluid overload [3–5]. Continuous renal ­Center and the US Army Institute for Surgical Research Burn Cen-
replacement therapy (CRRT) is frequently used in criti- ter requiring ECMO with or without CRRT support between
cally ill patients with a survival benefit for many popula- ­January 1, 2012, and July 31, 2018. In total, 104 patient encounters
tions [6–9]. It should be no surprise that the 40–60% of were found to be eligible for analysis; however, 12 patient encoun-
patients on ECMO who developed AKI were placed on ters were subsequently excluded as these patients required only
transport ECMO support or they failed to provide consent (9 and
CRRT [7, 8]. To date, most data evaluating combined 3 patients, respectively). The remaining 92 patient encounters
therapy (ECMO + CRRT) stem from the pediatric litera- were included in the final analysis. Of note, 2 patients required
ture. ECMO support twice during their hospitalization at our facility.
Using the Extracorporeal Life Support Organization The demographic and clinical data of these 92 encounters were
registry including nearly 10,000 neonates and children, reviewed to include age, gender, race, primary diagnosis, indica-
tions for and mode of ECMO support, illness severity, oxygenation
Askenazi et al. [9] revealed a higher mortality in patients index, vasopressor requirement, and AKI severity. Illness severity
with AKI requiring CRRT versus patients with AKI alone. was calculated using the Simplified Acute Physiology Score and
In 4 small, single-center studies looking at adult patients AKI severity was determined by Kidney Disease Improving Glob-
with AKI requiring combined therapy, the mortality rates al Outcomes stage [21, 22]. In those patients that required ECMO
were 60,78, 80, and 100%, respectively [5, 7, 10, 11]. In a with CRRT support, we additionally reviewed urine output in the
24 h prior to RRT initiation, use of a diuretic prior to RRT initia-
larger, more recent single-center study; 63 among 135 pa- tion, CRRT modality utilized, prescribed CRRT dose, net fluid bal-
tients required combined ECMO and CRRT; however, ance after 72 h on CRRT, and requirement of RRT at discharge.
mortality rates were similar among groups receiving Our primary endpoint was survival to hospital discharge. All data
ECMO without AKI, ECMO with AKI, and ECMO with were obtained by manual chart review.
AKI requiring CRRT [12]. At our institution, ECMO is performed most commonly with
the Cardiohelp systemTM by Maquet (Rastatt, Germany). A small
According to a recent survey, providers reported that portion of patients underwent ECMO using the Maquet Rotaflow
the primary indication for renal replacement therapy systemTM (2.9%) or a combination of the 2 systems (0.96%). The
(RRT) during ECMO therapy is for either fluid overload decision to use venovenous or venoarterial ECMO was made at the
prevention or active volume management in nearly 60% discretion of the ECMO-trained intensivist based on the patient’s
of cases [10]. In both adult and pediatric literature, fluid underlying diagnosis and need for pulmonary or cardio-pulmo-
nary support. The decision to initiate CRRT along with dosing,
overload has been associated with mortality and pro- fluid removal, and replacement fluid selection was at the discretion
longed ECMO duration, while a negative fluid balance of the intensivist (if credentialed in CRRT) or by a consulting ne-
leads to improved respiratory function and time to wean- phrologist. CRRT was performed using the NxStage (Lawrence,
ing ECMO [8, 13–16]. Additionally, pediatric studies MA, USA) or Prismaflex (Deerfield, IL, USA) machines. The vast
have shown that combining ECMO and CRRT leads to a majority of our patients received CRRT in line with their ECMO
circuit (i.e., not through a separate, dedicated CRRT access). Stan-
decrease in cumulative fluid balance compared to those dard premixed replacement fluids were prescribed as required by
receiving ECMO alone [8, 17, 18]. Data in the adult pop- the patient’s metabolic derangements. Anticoagulation was estab-
ulation remain sparse. lished with standard heparin protocol unless otherwise contrain-

342 Blood Purif 2020;49:341–347 Dado et al.

DOI: 10.1159/000504287
 Table 1. Clinical characteristics of ECMO survivors vs. nonsurvivors

Demographic/clinical variables ECMO survivor (n = 61) ECMO nonsurvivor (n = 29) p value

Age, years* 37.5 (18–57) 45.6 (16–79) 0.054

Gender, male 38 (62.3) 25 (89.3) 0.006
Race
Caucasian 13 (39.4) 8 (44.4) 0.648
Hispanic 13 (39.4) 7 (21.2)
ECMO mode (VV) 53 (86.9) 20 (71.4) 0.086
SAPS2* 58.0 (23–86) 73.5 (27–92) 0.023
Oxygenation index* 42.1 (24.4–77.2) 44.4 (16.9–99.3) 0.585
Vasopressor requirement 21 (77.8) 14 (73.7) 0.749
ECMO indication
ARDS 49 (80.3) 19 (67.9) 0.206
Cardiac failure 7 (11.5) 4 (12.5) 0.711

Data presented as n (%) and median (range/IQR).

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* Wilcoxon/KW test.
Comparison of characteristics of ECMO patients by mortality.
VV, venovenous; SAPS2, simplified acute physiology score; ECMO, extracorporeal membrane oxygenation;
IQR, interquartile range.

dicated at the discretion of the ECMO attending. Kidney Disease higher in the nonsurvivor group, 73.5 vs. 58.0 (p = 0.23).
Improving Global Outcomes definitions were used to grade AKI Male gender was also associated with mortality for both
severity using data for the 24 h prior to ECMO cannulation.
Statistical analysis was performed using SPSS Statistical Soft-
ECMO patients and the ECMO/CRRT subset (p = 0.006
ware version 25 (IBM, Armonk, NY, USA). Intergroup statistical and 0.001, respectively).
comparisons were performed using Wilcoxon/Kruskal-Wallis for Of those receiving combined ECMO/CRRT therapy,
the continuous variables (age, severity score, oxygenation index, nonsurvivors were more likely to have a significantly posi-
urine output, CRRT duration, dose, and net fluid balance) and chi- tive net fluid balance at 72 h (p = 0.001) as seen in Table 2.
square tests for the categorical data (gender, race, ECMO/CRRT
modes/indications, vasopressor requirement, diuretic use, need
There was no mortality difference in ECMO indication,
for intermittent hemodialysis). Logistic regression was performed AKI severity, CRRT indication, or CRRT initial dose for
using age, gender, and net fluid balance as variables to identify in- the combination ECMO/CRRT group. CVVH was the mo-
dependent risk factors for mortality. Statistical significance as de- dality used in all cases. In a multivariate linear regression
fined at p ≤ 0.05. analysis, net fluid balance and age were found to be inde-
pendently associated with mortality as seen in Table 3.

Results
Discussion/Conclusion
During the study period, 90 patients received ECMO
with 48 (53.3%) requiring the combination of ECMO The intended purpose of this study was to define the
with CRRT. Of those patients receiving ECMO with incidence of concurrent CRRT with ECMO therapy and
CRRT, the mortality rate was 39.5%. The mortality rate to determine the overall impact of this strategy on patient
among those receiving ECMO alone was 31.4%, which outcomes such as mortality and renal recovery. It was
was not statistically different from those on combined found that the majority of patients who underwent ECMO
therapy (p = 0.074). Of the 29 survivors, 6 (20.7%) were also received CRRT. This relationship is consistent with
dialysis dependent at hospital discharge. our study’s hypothesis. The reciprocal risk of AKI and
Of all patients receiving ECMO therapy, there was no ARDS is a previously described phenomenon affecting
difference between survivors and non-survivors with re- many critically ill patients [3]. This association is impor-
spect to ECMO mode, indication, vasopressor require- tant as it highlights the need for multisystem expertise
ment, or oxygenation score as seen in Table 1. However, and a multidisciplinary approach to the critically ill
Simplified Acute Physiology Score severity score was ECMO patient. This study also found that this combined

Outcomes of RRT with ECMO Blood Purif 2020;49:341–347 343

DOI: 10.1159/000504287
 Table 2. Clinical characteristics of ECMO/CRRT survivors vs. ECMO/RRT nonsurvivors

Demographic/clinical variables ECMO/CRRT ECMO/CRRT p value

survivor (n = 29) nonsurvivor (n = 19)

Age, years* 38.6 (18 to 63) 42.7 (16 to 79) 0.104

Gender, male 16 (55.2%) 18 (94.7) 0.001
Race
Caucasian 8 (30.8) 8 (44.4) 0.586
Hispanic 13 (50.0) 8 (44.4)
ECMO mode (VV) 23 (79.3) 13 (68.4) 0.398
SAPS2* (n = 27) 66.5 (51 to 86) 75.0 (27 to 92) 0.288
Oxygenation index* (n = 21) 44.1 (20.1 to 80.8) 40.7 (26.4 to 77.2) 0.823
Vasopressor requirement 21 (77.8) 14 (73.7) 0.749
ECMO indication
ARDS 23 (79.3) 19 (67.9) 0.398
Cardiac failure 5 (17.2) 13 (68.4) 0.512
KDIGO stage AKI 0.613

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0 9 (31.0) 3 (15.7)
1 3 (10.3) 2 (10.5)
2 6 (20.6) 3 (15.7)
3 11 (37.9) 10 (52.6)#
UOP prior 24 h* 1,229 (0 to 4,715) 1,809 (0 to 5,488) 0.134
Diuretic use (n = 48) 12 (44.4) 4 (22.2) 0.122
CRRT indication volume management 24 (82.7) 14 (73.7) 0.122
Days requiring CRRT* 10 (1 to 59) 8 (1 to 24) 0.642
Initial dose, mL/kg/h* 34.8 (11.8 to 75.3) 37.7 (20.0 to 71.4) 0.620
72 h net fluid balance, mL (L)* –3,353 (–12.6 to 10) 1,897 (–3.6 to 15.1) 0.001

Data presented as n (%) and median (range/IQR).

* Wilcoxon/KW test.
# One nonsurvivor was ESRD at baseline.

Comparison of characteristics of ECMO + CRRT patients by mortality.

VV, venovenous; SAPS2, simplified acute physiology score; ECMO, extracorporeal membrane oxygenation;
RRT, renal replacement therapy; CRRT, continuous RRT; AKI, acute kidney injury; KDIGO, Kidney Disease
Improving Global Outcomes; IQR, interquartile range.

Table 3. Multivariate logistic regression analysis for mortality

Clinical factor OR Lower 95% Upper 95% p value

Age, years* 1.0671 1.008778 1.128794 0.0109

Net fluid balance, dL* 1.022739 1.006318 1.039428 0.0009
Gender, male/female 16.657854 1.4769763 187.87309 0.0229

* OR per unit change in regressor.

Multivariate logistic regression analysis for mortality.
Tests and CIs on ORs are wald based.

therapy was associated with increased mortality com- Several factors may account for the difference in sur-
pared with ECMO alone. Although this theme is consis- vival rates between our patients and those previously re-
tent with previous literature, our mortality rates for com- ported. First, our patients that received CRRT may have
bination ECMO/CRRT were considerably lower than less severe AKI at initiation of therapy. Of the patients in
published data, 39.5 vs. 60–100% [7, 8, 23, 24]. our series who required combined ECMO and CRRT,

344 Blood Purif 2020;49:341–347 Dado et al.

DOI: 10.1159/000504287
41% of survivors were initiated on CRRT with no AKI or volume management for fluid overload or fluid overload
stage 1 AKI versus only 25% of nonsurvivors. Although prevention [10]. Fluid overload is associated with in-
our overall incidence was similar to the published rate of creased mortality and prolonged ECMO duration [8, 13,
AKI for ECMO patients (71–81%), it is difficult to com- 14]. Addressing volume overload with fluid removal via
pare these findings to the current literature as a break- ultrafiltrate is associated with improved respiratory func-
down of AKI severity is not available in those reports [2, tion and time to weaning ECMO [8, 15, 16]. Peak fluid
3, 23, 24]. Whether the impact on survival is related to overload and fluid overload at ECMO initiation were
lower illness severity or early aggressive initiation of ther- both predictive of hospital mortality in children [27]. Sev-
apy is an intriguing and unanswered question. eral studies in neonates and children have shown that
Second, age and patient comorbidities likely impacted combining ECMO and RRT leads to less cumulative fluid
our overall survival. The median age in our survival group overload than those receiving ECMO alone [8, 17, 18].
was 39 years compared to 43 years in the nonsurvival While there is sparse data among adult patients, higher
group. Although this difference was insignificant, multi- fluid balance was consistently associated with poor sur-
variate logistic regression analysis revealed age to be a de- vival in adults receiving venoarterial-ECMO [17]. The in-
terminant for mortality (p = 0.01). Our institution is a ternational ELSO guidelines recognize this and thus rec-

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military facility that cares for military members, benefi- ommend to “return the extracellular fluid volume to nor-
ciaries and retirees. Because of this, our patient popula- mal (dry weight) and maintain it there” [2].
tion as a whole is younger and with less comorbidities While this may appear to suggest that early and ag-
when compared with civilian hospitals. We do receive a gressive initiation of RRT to prevent hypervolemia may
fair number of civilian trauma and burn patients, ac- improve outcomes, a couple of caveats apply. We believe
counting for roughly one-third of our registry. However, this represents only an association between negative flu-
they are also classically a younger cohort of patients, but id balance in the first 72 h and survival. Our patient pop-
with significant injury similar to civilian facilities. ulation included medical, surgical, and traumatic etiolo-
Lastly, the physicians and nurses who have developed gies prompting ECMO and/or CRRT therapy. The un-
and maintained our ECMO program are by and large the derlying mechanisms and physiology behind ARDS
same physicians and nurses who have helped develop and development in each of these populations may dictate
maintain our CRRT program. There are multiple publi- different goals of treatment. For example, resuscitation
cations that demonstrate improved outcomes at centers after a devastating burn injury will differ considerably
who perform a high volume of complicated or specialized than fluid goals for patients presenting with cardiac fail-
procedures [25, 26]. Stemming from this, our intensive ure. Those with reversible volume overload as a compo-
care program is a proponent of early and aggressive ini- nent of their ARDS were more likely to benefit from ag-
tiation of RRT. However, each patient is managed indi- gressive fluid removal and survive. On the other hand,
vidually by a credentialed Intensivist or Nephrologist those who were not volume overloaded upon initiation
with CRRT rather than via a protocolized approach as of ECMO may have had a less reversible form of lung
many centers do. This is evident in the vast variations in pathology.
dosing. This early integration of therapy, in combination We are one of only a few studies in adults and pediat-
with our program’s experience and expertise, may con- rics to report on the rates of renal recovery after com-
tribute to our improved outcomes. However, it also po- bined ECMO and CRRT. Twenty percent of patients in
tentially increases our selection bias with a less critically our study who required combined therapy went on to re-
ill population undergoing combined ECMO/CRRT than quire on-going renal support at hospital discharge. Two
at other institutions who may reserve combination ther- pediatric studies report long-term RRT requirements of
apy for sicker patients. 4 and 6% over 20 years of follow-up in the absence of pri-
In our 48 patients who received combined ECMO and mary renal disease [19, 20]. One small study showed that
CRRT, a 3 L negative fluid balance in the first 72 h was among adult ECMO patients receiving CRRT, 3 out of 8
independently associated with survival (p = 0.001). In survivors (35%) required ongoing renal support at dis-
contrast, those patients in the series who died had an av- charge and 1-month follow-up [28]. We were unable to
erage 1.8 L positive fluid balance in the first 72 h. Accord- find any data on survival and renal outcomes beyond this
ing to a recent multicenter survey of physicians perform- in adult patients. This is an area that needs further inves-
ing ECMO regarding the combined use of RRT and tigation as the critical care community continues to in-
ECMO, the most common reason for RRT initiation is crease its use of these advanced organ support modalities.

Outcomes of RRT with ECMO Blood Purif 2020;49:341–347 345

DOI: 10.1159/000504287
 There were several limitations of our study. First, it is id balance is something that should be pursued and fur-
a single-center study so equipment and capabilities as ther prospective trials are needed to confirm these
well as provider practice may vary significantly at differ- outcomes. Additional investigation is needed regarding
ent institutions. For instance, a small portion of patients long-term outcomes of patients requiring combined
underwent ECMO using the Maquet Rotaflow systemTM, therapy.
but the standard of care in our institution is now the Car-
diohelp systemTM by Maquet. Our study was also retro-
spective so patients were not randomly assigned and Acknowledgments
therefore variations in treatment, namely, volume man-
The Geneva Foundation to include Brendan Beely (Research
agement, must be interpreted and applied with caution. Coordinator), John Jones (Statistician), and Daniel Wendorff (Re-
We also did not have complete data on all patients prior search Associate). James Lantry of Baltimore STC/CSTARS (Con-
to their arrival at our facility so some variables such as ill- sultant).
ness severity, vasopressor use, diuretic use, fluid and re-
suscitation status, and prior therapies were unknown and
may have affected outcomes. Last, we practice in a mili- Statement of Ethics

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tary facility and many of our patients were civilians trans-
Regional Health Command-Central Institutional Review
ferred from various parts of the region, as such we do not Board, Reference No. C.2017.152d. Approved August 25, 2017.
have long-term follow-up data beyond discharge for
many of these patients. We have updated our patient da-
tabase collection methods to have a greater emphasis on Disclosure Statement
tracking patients beyond discharge to determine long-
term outcomes. The authors have no conflicts of interest to declare. The authors
The majority of patients on ECMO in our series went declare that they have no competing interests. The opinions or as-
sertions contained herein are the private views of the authors and
on to require CRRT. This is important information for are not to be construed as official or as reflecting the views of the
aspiring hospitals to consider when discussing planning Department of the Army, Air Force or the Department of Defense.
and staffing needs for new ECMO programs. Patients in
our series who required CRRT in addition to ECMO had
survival rates comparable to the survival rates published Funding Sources
by the Extracorporeal Life Support Organization for pa-
tients requiring ECMO alone [23]. These survival rates USAF/AFMS (59 MDW), Award# FA8650-15-C-6692.
are higher than previously published survival rates for pa-
tients on combined therapy. Author Contributions
The use of CRRT is prevalent among patients under-
going ECMO, with over 50% of our patient population D.N.D., C.R.A., S.B.T., and A.B. all assisted in compiling, ana-
receiving combination therapy. Univariate and multivar- lyzing, and interpreting patient data. Additionally, they wrote and
iate predictors of outcome pointed to age, gender, and revised the manuscript. B.H. and L.C.P. assisted in the compilation
of the patient database. A.P.B., V.G.S., B.D.M., R.J.W.,P.E.M., and
fluid balance as main predictors of survival. Fluid bal- K.K.C. consented patients, offered project oversight, and assisted
ance is a modifiable risk factor. Early and aggressive ini- in concept proposal and manuscript revision. All authors read and
tiation of CRRT while on ECMO to target a negative flu- approved the final manuscript.

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DOI: 10.1159/000504287