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Thoracic: Lung Transplantation| Volume 1, P61-70, March 2020

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Contemporary analysis of charges and mortality in the use of extracorporeal membrane oxygenation: A cautionary tale

Open AccessPublished:March 05, 2020DOI:https://doi.org/10.1016/j.xjon.2020.02.003

      Abstract

      Objective

      The use of extracorporeal membrane oxygenation (ECMO) has increased exponentially. Costs and outcomes, however, vary considerably by indication. We sought to elucidate and quantify these differences.

      Methods

      Adult patients supported on ECMO between 2008 and 2016 were analyzed using the Nationwide Inpatient Sample. We divided the study period into an early (2008-2013) and late period (2013-2016). The primary outcome was hospital charges, and the secondary outcomes were mortality, length of stay (LOS), and duration of ECMO support. These were stratified by the 5 most common indications: postcardiotomy shock (PCS), cardiogenic shock (CS), severe acute respiratory failure (SARF), heart (HT), and lung transplantation (LT). Both patient and hospital characteristics were assessed. Charges were adjusted for inflation and analyzed using a generalized linear model with gamma distribution. Pairwise comparison with Bonferroni correction was used to evaluate the cost and multivariate logistic regression to assess the risk of mortality.

      Results

      Data pertaining to 15,829 adult patients were evaluated. Mean age of the entire cohort was 52.8 years, 8895 (56%) were white, and 10,278 (65%) were male. PCS was the predominant indication for ECMO (39%), followed by CS (37%). SARF accounted for 15% and HT and LT accounted for 3.9% and 5.4%, respectively. Mean LOS and duration of ECMO support were 23.4 days and 5.3 days respectively. Mean hospital charges per hospitalization for the entire cohort were USD 731,914 per patient. Charges per patient pertaining to hospitalizations in which ECMO was used in transplant patients were the highest: USD 1,448,931 and USD 1,574,378 (P = .99) for HT and LT, respectively. Charges were lower for the other indications: PCS USD 798,909, CS USD 655,099, and SARF USD 824,852. Overall mortality for the entire cohort was 55%. PCS and CS (53% vs 58%, P = .34) had similar survival, whereas SARF was 45%, LT was 39% and HT 32%. There were no differences in survival in these latter indications (SARF, LT and HT). The cumulative charges (proportion × hospital charges) reveal that PCS and CS (39% and 37%) account for both the majority of charges as well as the greatest mortality. Conversely, SARF and transplantation accounted for the smaller proportion of charges and the lower mortality. Patients undergoing HT had the longest LOS (51.7 days) and duration on ECMO (15.9 days), followed by LT (35.4 and 8.8 days respectively), and patients with SARF (28.6 and 6.6 respectively). LOS and duration of ECMO for those with PCS were 18.7 days and 4.8 days, respectively. Those on ECMO for CS were hospitalized for 19.7 days and spent an average of 3.8 days on ECMO. Mortality decreased, whereas charges increased in the late era.

      Conclusions

      The use of ECMO is associated with high hospital charges and a wide variation in outcomes. Hospitalizations, in which ECMO is used to support patients with cardiogenic shock (PCS and CS), are individually associated with lower LOS and charges. Cumulatively, however, these account for greater charges and greater mortality. Although mortality may be decreasing, overall charges are increasing with time. These variations may influence reimbursement decisions in value-based healthcare.

      Graphical abstract

      Key Words

      Abbreviations and Acronyms:

      ARF (acute respiratory failure), CS (cardiogenic shock), ECMO (extracorporeal membrane oxygenation), HT (heart transplant), ICD-9 (International Classification of Diseases), IHM (in-hospital mortality), LOS (length of stay), LT (lung transplant), NIS (Nationwide Inpatient Sample), PCS (postcardiotomy shock), SARF (severe acute respiratory failure), USD (United States Dollars)
      Figure thumbnail fx2
      ECMO cumulative charges and mortality.
      ECMO hospitalizations for postcardiotomy shock and cardiogenic shock are associated with the greatest charges and the lowest survival.
      ECMO use in postcardiotomy and cardiogenic shock is a common occurrence. It is, however, associated with hospitalizations worth billions of dollars yet with comparatively low survival. Value-based health care considerations may look unfavorably on the nonjudicious use of ECMO in the future.
      See Commentaries on pages 71 and 73
      Extracorporeal support is used increasingly to support patients with severe, acute cardiac and pulmonary failure. Indeed, it is rapidly becoming the option of first choice for support. Indications have been broadened to include severe influenza, bridging to heart (HT) and lung transplantation (LT), cardiogenic shock (CS) as well as, more traditionally, postcardiotomy shock (PCS). Extracorporeal support has increased by more than 400%, and it is fast becoming a common feature in many high-volume centers in the United States.
      • McCarthy F.H.
      • McDermott K.M.
      • Kini V.
      • Gutsche J.T.
      • Wald J.W.
      • Xie D.
      • et al.
      Trends in US extracorporeal membrane oxygenation use and outcomes: 2002-2012.
      • Sanaiha Y.
      • Bailey K.
      • Downey P.
      • Seo Y.J.
      • Aguayo E.
      • Dobaria V.
      • et al.
      Trends in mortality and resource utilization for extracorporeal membrane oxygenation in the United States: 2008-2014.
      • Maxwell B.G.
      • Powers A.J.
      • Sheikh A.Y.
      • Lee P.H.
      • Lobato R.L.
      • Wong J.K.
      Resource use trends in extracorporeal membrane oxygenation in adults: an analysis of the nationwide inpatient sample 1998-2009.
      Similarly, use in the treatment of respiratory failure has also increased. In this vein, the CESAR (conventional ventilatory support vs extracorporeal membrane oxygenation for severe adult respiratory failure) trial elevated the popularity of extracorporeal membrane oxygenation (ECMO) support, providing a compelling rationale for the transfer of severely ill patients to ECMO centers for specialized care.
      • Peek G.J.
      • Mugford M.
      • Tiruvoipati R.
      • Wilson A.
      • Allen E.
      • Thalanany M.M.
      • et al.
      Efficacy and economic assessment of conventional ventilatory support versus extracorporeal membrane oxygenation for severe adult respiratory failure (CESAR): a multicentre randomised controlled trial.
      The provision of extracorporeal support, however, is resource-intensive, and the associated costs are high. Various reports estimate these as ranging between US dollars (USD) 20,000 and 40,000 per day.
      • Mahle W.T.
      • Forbess J.M.
      • Kirshbom P.M.
      • Cuadrado A.R.
      • Simsic J.M.
      • Kanter K.R.
      Cost-utility analysis of salvage cardiac extracorporeal membrane oxygenation in children.
      ,
      • Harvey M.J.
      • Gaies M.G.
      • Prosser L.A.
      US and international in-hospital costs of extracorporeal membrane oxygenation: a systematic review.
      Hospitalizations for PCS-ECMO are estimated at approximately USD 200,000 to 500,000 and where it is used as a bridge to LT, the median hospital charges are increased by as much as 50%.
      • Hayanga J.A.
      • Shigemura N.
      • Aboagye J.K.
      • Ensor C.
      • Dew M.A.
      • Hayanga H.K.
      • et al.
      ECMO support in lung transplantation: a contemporary analysis of hospital charges in the United States.
      Despite these high costs, however, outcomes vary by indication.
      • Sanaiha Y.
      • Bailey K.
      • Downey P.
      • Seo Y.J.
      • Aguayo E.
      • Dobaria V.
      • et al.
      Trends in mortality and resource utilization for extracorporeal membrane oxygenation in the United States: 2008-2014.
      The best results have been demonstrated in the use of ECMO to treat adult respiratory distress syndrome, influenza, and as a bridge to transplantation.
      • Peek G.J.
      • Mugford M.
      • Tiruvoipati R.
      • Wilson A.
      • Allen E.
      • Thalanany M.M.
      • et al.
      Efficacy and economic assessment of conventional ventilatory support versus extracorporeal membrane oxygenation for severe adult respiratory failure (CESAR): a multicentre randomised controlled trial.
      ,
      • Hayanga A.J.
      • Aboagye J.
      • Esper S.
      • Shigemura N.
      • Bermudez C.A.
      • D'Cunha J.
      • et al.
      Extracorporeal membrane oxygenation as a bridge to lung transplantation in the United States: an evolving strategy in the management of rapidly advancing pulmonary disease.
      Conversely, poor outcomes have been observed in CS, specifically in the context of cardiopulmonary resuscitation. Overall, advancements in technological design and clinical management have driven a dramatic improvement in ECMO outcomes over the past decade. As such, this past decade has been termed the “ECMO-2 era,” distinguishing it from the poor outcomes before 2008. Surprisingly, however, despite the exorbitant costs of ECMO, there are few published analyses of charges or cost-effectiveness. The results of the CESAR trial justified ECMO use in the treatment of influenza A during the H1N1 pandemic but are not necessarily extrapolatable to any other kind of shock.
      • Peek G.J.
      • Mugford M.
      • Tiruvoipati R.
      • Wilson A.
      • Allen E.
      • Thalanany M.M.
      • et al.
      Efficacy and economic assessment of conventional ventilatory support versus extracorporeal membrane oxygenation for severe adult respiratory failure (CESAR): a multicentre randomised controlled trial.
      ,
      • Peek G.J.
      • Clemens F.
      • Elbourne D.
      • Firmin R.
      • Hardy P.
      • Hibbert C.
      • et al.
      CESAR: conventional ventilatory support vs extracorporeal membrane oxygenation for severe adult respiratory failure.
      In this study, we sought to use a national sample to describe the variation in charges for ECMO and mortality with different indications. With an evaluation of charges and outcomes, we aim to take a step closer toward a value-based appraisal of ECMO.

      Methods

      The data analyzed were obtained from the Nationwide Inpatient Sample (NIS). The NIS is sponsored by the Agency for Healthcare Research and Quality and is part of the Healthcare Cost and Utilization Project. The data represent a 20% stratified sample of nonfederal, acute-care hospitals in all states in the United States, and it is the largest all-payer database of hospital inpatients admissions.
      • Healthcare Cost and Utilization Project (HCUP)
      Overview of the National (Nationwide) Inpatient Sample (NIS).

      Study Population

      We included all hospital discharges between 2008 and 2016, for all adult patients (age 18 or older) supported on ECMO as defined by International Classification of Diseases (ICD), 9th Revision procedure code 39.65 and 10th Revision code 5A15233. We excluded recipients younger than the age of 18 years and those with missing data on age, sex, mortality, or hospital charges.

      Data Collection

      The primary outcome was hospital charges. We also evaluated in-hospital mortality (IHM), length of hospitalization, and duration on ECMO stratified by clinical indication for descriptive purposes. Patient demographic variables analyzed included age, sex, race/ethnicity, and insurance status. We adjusted for disease burden using a modified version of the Charlson comorbidity index explicitly developed for use with administrative databases such as the NIS.
      • Elixhauser A.
      • Steiner C.
      • Harris D.R.
      • Coffey R.M.
      Comorbidity measures for use with administrative data.
      Using specific ICD 9th Revision codes and Tenth Revision codes, we identified the 5 major indications for ECMO using a modified methodology from previous reports.
      • McCarthy F.H.
      • McDermott K.M.
      • Kini V.
      • Gutsche J.T.
      • Wald J.W.
      • Xie D.
      • et al.
      Trends in US extracorporeal membrane oxygenation use and outcomes: 2002-2012.
      ,
      • Maxwell B.G.
      • Powers A.J.
      • Sheikh A.Y.
      • Lee P.H.
      • Lobato R.L.
      • Wong J.K.
      Resource use trends in extracorporeal membrane oxygenation in adults: an analysis of the nationwide inpatient sample 1998-2009.
      These included PCS, CS, acute respiratory failure (ARF), pre- and post-HT, and pre- and post-LT. (Codes are available in Table 1.) This is a similar methodology used in other studies that have used the NIS, permitting the categorization of codes into mutually exclusive groups that, for example, allow CS to be evaluated in the absence of cardiac surgery, respiratory failure, or transplantation codes.
      • Maxwell B.G.
      • Powers A.J.
      • Sheikh A.Y.
      • Lee P.H.
      • Lobato R.L.
      • Wong J.K.
      Resource use trends in extracorporeal membrane oxygenation in adults: an analysis of the nationwide inpatient sample 1998-2009.
      Similarly, patients undergoing transplant were evaluated separately as either HT or LT recipients and excluded from those requiring support for PCS.
      • Sanaiha Y.
      • Bailey K.
      • Downey P.
      • Seo Y.J.
      • Aguayo E.
      • Dobaria V.
      • et al.
      Trends in mortality and resource utilization for extracorporeal membrane oxygenation in the United States: 2008-2014.
      ,
      • Maxwell B.G.
      • Powers A.J.
      • Sheikh A.Y.
      • Lee P.H.
      • Lobato R.L.
      • Wong J.K.
      Resource use trends in extracorporeal membrane oxygenation in adults: an analysis of the nationwide inpatient sample 1998-2009.
      Table 1ECMO indication ICD and CCS codes
      ECMO indicationICD-CM-9 (procedure)ICD-CM-10CCS diagnoses
      Post cardiotomy35.x, 36.x, 37.1, 37.3x, 441.x02TN0ZZ, 02TN3ZZ, 02NN3ZZ, 025N0ZZ, 02CN0ZZ, 02UM0JZ, 02U50JZ, 02QF0ZZ, 02QG0ZZ, 02QH0ZZ, 02QJ0ZZ, 0210093, 02100A3, 02100J3, 02100K3, 02100Z3, 021008W, 021009W, 02100AW, 02100JW 02100KW, 021108W, 021109W, 02110AW, 0211OJW, 02110KW"021208W, 02120AW, 02120JW, 02120KW, 021308W, 021309W, 02130AW, 02130JW, 02130KW, 0210088, 0210089, 021008C, 0210098, 0210099, 021009C, 02100A8, 02100A9, 02100AC, 02100J8, 02100J9, 02100JC, 02100K8, 02100K9, 02100KC, 02100Z8, 02100Z9, 02100ZC, 02100AF, 02100A3
      Cardiogenic shockI502, I503, I5040, I5041, I5021, I5031, "I5020, I5039, I5023, I5033, I5043, I97130, I97131, I219, "I39" I38, I30, I31, I301, I300, I32" I40" I401, I514, I408, I409, I4901, I97120, I469" I33"97, 100, 101, 103, 107, 108
      Acute respiratory failureJ9620, J9600, J962, J9691, J9692, J9582, J9602, J9621, J9622, J9690, J9600, R093, 122, 123, 126, 130, 132
      Heart transplant37.5102YA0Z0
      Lung transplant33.51, 33.520BYK0Z0, 0BYM0Z0, 0BYL0Z0
      ECMO, Extracorporeal membrane oxygenation; ICD-9 CM, International Classification of Diseases, Ninth revision, Clinical Modification; ICD-10 CM, International Classification of diseases, Tenth revision, Clinical Modification; CCS, clinical classifications software.

      Statistical Analysis

      We used a data analytic approach accounting for the built-in weighting incorporated within NIS methodology. Descriptive statistics on the patient and hospital characteristics were obtained for the entire cohort. Because hospital charges were positively skewed, we used a generalized linear model with gamma distribution to calculate differences in total charges by ECMO indication. A pairwise comparison with Bonferroni correction was performed on predicted mean charges obtained from the model for each of the clinical indications. Variables included within the model were age, sex, race/ethnicity, Charlson comorbidity index, insurance status, hospital region, and year of procedure. All hospital charges were inflation-adjusted using 2017 USD. We compared differences in charges between survivors and nonsurvivors. Similar models were fitted using length of stay (LOS) and duration on ECMO as outcome variables. We performed a multivariable logistic regression to evaluate the association between clinical indication for ECMO and IHM, adjusting for the aforementioned variables. A similar pairwise comparison was performed on the predicted mortality rates by clinical indication for ECMO. To evaluate the impact of time on charges and mortality, we stratified the study period into 2 eras, early (2008-2012) and late (2013-2016). We fitted the aforementioned models individually for each era. A 2-tailed P < .05 was considered statistically significant. All analyses were performed on STATA MP, Version 14 (StataCorp, College Station, Tex). This study was granted an exemption by West Virginia University of School of Medicine institutional review board.

      Results

      Figure 1 shows the composition of the inclusion criteria used. A total of 15,829 patients were included in the analysis. Of the total, there were 5584 and 10,245 in the early and late eras, respectively. Female patients accounted for 35%of the population, 8895 (56%) were white, and the mean age was 52.8 years. Postcardiotomy was the most common indication for ECMO (39%), followed by CS (37%). Acute respiratory failure accounted for 15%, and HT and LT accounted for 3.9% and 5.4%, respectively. The mean LOS and duration on ECMO were 23.4 days and 5.3 days, respectively (Table 2). Table 3 depicts the distribution of these characteristics by ECMO indication.
      Figure thumbnail gr1
      Figure 1Chart illustrating patient inclusion criteria into study population. ECMO, Extracorporeal membrane oxygenation.
      Table 2Patient- and hospital-level characteristics
      VariableN = 15,829
      Mean age, y, SD52.8 (16.2)
      Female sex, n (%)5551 (35)
      Race, n (%)
       White8895 (56)
       Black2121 (13)
       Hispanic2516 (16)
       Other2297 (15)
      Indication for ECMO, n (%)
       Postcardiotomy6148 (39)
       Cardiogenic shock5864 (37)
       Respiratory failure2350 (15)
       Pre/post-heart transplant611 (3.9)
       Pre/post-lung transplant855 (5.4)
      Insurance status, n (%)
       Private6733 (43)
       Medicare5329 (34)
       Medicaid2636 (17)
       Other1130
      Hospital region
       Northeast4630 (29)
       Midwest3600 (23)
       South5161 (33)
       West2437 (15)
      Charlson Comorbidity index
       02440 (15)
       14049 (26)
       >19339 (59)
      Mean length of stay, d (SE)23.4 (27.9)
      Mean length on ECMO, d (SE)5.3 (11.6)
      SD, Standard deviation; ECMO, extracorporeal membrane oxygenation; SE, standard error.
      Table 3Population characteristics by ECMO indication
      VariablePCSCSSAR (n = 2350)HTXLUNGTX (n = 855)
      Mean age, y (SD)57.5 (14.9)50.8 (16.2)45.5 (17.0)52.5 (14.1)52.0 (14.4)
      Female sex, n (%)1868 (30)2117 (36)1052 (45)173 (28)341 (40)
      Race, n (%)
       White3555 (58)3065 (52)1363 (57.9)344 (56.3)568 (66.4)
       Black674 (11)887 (15)341 (14.9)144 (23.6)74 (8.7)
       Hispanic1025 (17)969 (17)357 (15)64 (10.5)101 (11.8)
       Other894 (15)943 (16)289 (11.9)59 (9.6)112 (13.1)
      Insurance status, n (%)
       Private2485 (40)2565 (44)954 (40.6)279 (45.7)450 (52.6)
       Medicare2468 (39.9)1666 (28)641 (27.3)240 (39.3)313 (36.6)
       Medicaid831 (14)1122 (19)518 (22)83 (13.6)82 (9.6)
       Other363 (5.8)511 (8.7)237 (10.1)9 (1.4)10 (1.2)
      Hospital region
       Northeast1764 (29)1684 (29)690 (29.4)186 (31)305 (35.7)
       Midwest1556 (25)1313 (22)445 (18.9)105 (17)181 (2.1)
       South1828 (30)2007 (34)861 (36.6)215 (35.)250 (29.2)
       West999 (16)860 (15)355 (15.1)104 (17.)120 (14.0)
      Charlson Comorbidity index
       0452 (7.4)820 (14)823 (35)14 (2.3)332 (24.8)
       11595 (26)1414 (24)582 (24.8)135 (22.1)323 (37.8)
       >14101 (67)3630 (62)945 (40.2)462 (75.6)200 (23.4)
      Mean length of stay, d (SE)19.5 (22.7)19.7 (22.6)28.9 (28.3)51.4 (56.8)41.3 (40)
      Mean length on ECMO, d (SE)4.8 (7.5)3.8 (9.2)6.6 (12.4)16.0 (32.6)8.8 (13.7)
      PCS, Postcardiotomy shock; CS, cardiogenic shock; SARF, severe acute respiratory failure; HTX, heart transplantation; LUNGTX, lung transplantation; SD, standard deviation; SE, standard error; ECMO, extracorporeal membrane oxygenation.

      Hospital Charges

      The mean hospital charges in the entire cohort were USD 731,914. Tables 4 and 5 depict unadjusted and predicted mean hospital charges by clinical indication for ECMO, based on the adjusted model. In adjusted analysis, there were no statistically significant differences in total hospital charges between HT and LT recipients (USD 1,448,931 vs USD 1,574,378; P = .99). These 2 indications had significantly greater total charges than any of the other indications. (PCS USD 798,909, CS USD 655,099, severe acute respiratory failure [SARF] USD 824,852). In a pairwise comparison, there were no differences between PCS and SARF. CS was associated with the lowest total individual hospital charges when compared with SARF, HT, and LT. There were no differences in charges between survivors and nonsurvivors for any indications except ECMO use for CS and PCS. In both these latter indications, survivors had greater hospital charges compared with nonsurvivors (Figure 2, A). In all indications, there was a statistically significant increase in average hospital charges from the early era (2008-2012) to the late-era (2012-2016) (Figure 2, B).
      Table 4Unadjusted and adjusted hospital charges by indication for ECMO
      Indication for ECMOUnadjusted charges (95% CI)Adjusted charges
      Adjusted for age, sex, race, comorbidities, hospital region, insurance status.
      (95% CI)
      Postcardiotomy658,519 (610,149.2-706,889)798,909 (715,196-882,621)
      Cardiogenic shock642,719 (582,532.9-702,905.8)655,099 (591,476-718,721)
      Respiratory failure832,786 (716,161.8-949,410.9)824,852 (725,280-924,423.80)
      Heart transplant1,362,123 (1,175,213-1,549,033)1,448,931 (1,252,694-1,645,167)
      Lung transplant1,219,430 (933,913.2-1,504,947)1,574,378 (1,328,121-1,820,635)
      ECMO, Extracorporeal membrane oxygenation; CI, confidence interval.
      Adjusted for age, sex, race, comorbidities, hospital region, insurance status.
      Table 5Pairwise comparison of adjusted hospital charge by ECMO indication
      Indication for ECMOHospital charge
      Adjusted for age, sex, race, comorbidities, hospital region, insurance status.
      (USD)
      Post cardiotomyCardiogenic shockAcute respiratory failureHeart transplantLung transplant
      Post cardiotomy798,909<0.010.99<0.001<0.001
      Cardiogenic shock655,099<0.001<0.001<0.001
      Acute respiratory failure824,852<0.001<0.001
      Heart Transplant1,448,9310.99
      Lung transplant1,574,378
      ECMO, Extracorporeal membrane oxygenation; USD, US dollars.
      Adjusted for age, sex, race, comorbidities, hospital region, insurance status.
      Figure thumbnail gr2
      Figure 2A, Adjusted hospital charges for survivors and nonsurvivors by indication for ECMO indication. B, Adjusted hospital charges in the 2 eras, 2008-2012 and 2013-2016, by indication for ECMO. ECMO, Extracorporeal membrane oxygenation.

      Cumulative Charges

      The cumulative charges (proportion × hospital charges) show that PCS and CS (39% and 37%) account for both the most charges and the lowest survival. Conversely, SARF, and transplantation accounted for the smaller proportion of charges and higher survival (Figure 3).
      Figure thumbnail gr3
      Figure 3Cumulative charges and mortality per ECMO indication. HT, Heart transplant; LT, lung transplant; ARF, acute respiratory failure; PCS, postcardiotomy shock; CS, cardiogenic shock.

      Mortality

      The in-hospital mortality for the entire cohort was 8727 (55%). In the adjusted analysis, there was no difference in the IHM rate between PCS and CS (53% vs 58%, P = .34). Descriptively, the in-hospital mortality rate for patients with CS was greater than in patients with ARF (45%), pre/post HT (39%), and pre/post LT (32%). There were no differences in in-hospital mortality between patients with ARF compared with HT and LT recipients (Table 6). For all indications, however, there was a decrease in the risk of IHM in the late-era (Table 7).
      Table 6Mortality pairwise comparisons of in-hospital mortality by ECMO indication
      Mortality
      P < .05.
      Post cardiotomyCardiogenic shockAcute respiratory failureHeart transplantLung transplant
      Postcardiotomy0.53 (0.49-0.57)0.340.060.03<0.01
      Cardiogenic shock0.58 (0.54-0.61)<0.01<0.01<0.01
      Acute respiratory failure0.45 (0.40-0.49)0.990.19
      Heart transplant0.39 (0.31-0.48)0.99
      Lung transplant0.32 (0.23-0.41)
      Adjusted for age, sex, race, comorbidities, hospital region, insurance status.
      P < .05.
      Table 7Comparison of risk-adjusted mortality stratified by era (2008-2012 and 2013-2016) per ECMO indication
      Indication for ECMO2008-20122009-2016P value
      Postcardiotomy0.59 (0.51-0.68)0.49 (0.44-0.54)<.001
      Cardiogenic shock0.65 (0.57-0.73)0.52 (0.49-0.56)<.001
      Respiratory failure0.50 (0.40-0.59)0.40 (0.35-0.45).002
      Heart transplant0.48 (0.34-0.63)0.34 (0.23-0.46).04
      Lung transplant.0.44 (0.2-0.60)0.14 (0.02-0.65).002
      ECMO, Extracorporeal membrane oxygenation.

      Length of Stay

      Heart transplant recipients had the most extended mean total hospital LOS (51.7 days) and duration on ECMO (15.9 days) compared with the other clinical indications for ECMO. LT recipients had the next most prolonged LOS (35.4 vs 8.8), followed by patients with SARF (28.6 vs 6.6). Mean hospital LOS and duration on ECMO for PCS patients were 18.7 days and 4.8 days, respectively. On average, patients with CS were hospitalized for 19.7 days and spent an average of 3.8 days on ECMO.

      Discussion

      Several published reports have attempted to quantify trends in ECMO use over the past decade. It has been established that ECMO admissions increased by 369% between 2008 and 2014.
      • Sanaiha Y.
      • Bailey K.
      • Downey P.
      • Seo Y.J.
      • Aguayo E.
      • Dobaria V.
      • et al.
      Trends in mortality and resource utilization for extracorporeal membrane oxygenation in the United States: 2008-2014.
      When stratified by indication, the most substantial increase occurred in patients with respiratory failure.
      • Sanaiha Y.
      • Bailey K.
      • Downey P.
      • Seo Y.J.
      • Aguayo E.
      • Dobaria V.
      • et al.
      Trends in mortality and resource utilization for extracorporeal membrane oxygenation in the United States: 2008-2014.
      Our results reflect a similar increase in ECMO use; however, this was predominantly for treating PCS and CS. Nevertheless, mortality associated with ECMO use has decreased, as our results have also shown. This has been primarily attributed independently to the decrease in mortality in the postcardiotomy cohort in whom in-hospital age-adjusted mortality has reportedly dropped by 20%, from 62% to 42%. This has mainly been attributed to improvements in overall postcardiac surgery care and survival.
      • Sanaiha Y.
      • Bailey K.
      • Downey P.
      • Seo Y.J.
      • Aguayo E.
      • Dobaria V.
      • et al.
      Trends in mortality and resource utilization for extracorporeal membrane oxygenation in the United States: 2008-2014.
      The majority of patients who receive ECMO are treated in large urban teaching hospitals.
      • Sanaiha Y.
      • Bailey K.
      • Downey P.
      • Seo Y.J.
      • Aguayo E.
      • Dobaria V.
      • et al.
      Trends in mortality and resource utilization for extracorporeal membrane oxygenation in the United States: 2008-2014.
      ,
      • Harvey M.J.
      • Gaies M.G.
      • Prosser L.A.
      US and international in-hospital costs of extracorporeal membrane oxygenation: a systematic review.
      The trend is driven by the implicit assumption that high-volume centers are the de facto centers of excellence, a notion predicated on the volume–outcome relationship that has been observed and reported for complex surgical interventions and that tends to favor outcomes in these settings.
      • Reames B.N.
      • Ghaferi A.A.
      • Birkmeyer J.D.
      • Dimick J.B.
      Hospital volume and operative mortality in the modern era.
      The volume–outcome relationship, however, is conspicuously different in the context of ECMO.
      • Bailey K.L.
      • Downey P.
      • Sanaiha Y.
      • Aguayo E.
      • Seo Y.J.
      • Shemin R.J.
      • et al.
      National trends in volume-outcome relationships for extracorporeal membrane oxygenation.
      • Ko W.J.
      • Lin C.Y.
      • Chen R.J.
      • Wang S.S.
      • Lin F.Y.
      • Chen Y.S.
      Extracorporeal membrane oxygenation support for adult postcardiotomy cardiogenic shock.
      • McCarthy F.H.
      • McDermott K.M.
      • Spragan D.
      • Hoedt A.
      • Kini V.
      • Atluri P.
      • et al.
      Unconventional volume-outcome associations in adult extracorporeal membrane oxygenation in the United States.
      Greater mortality has been observed in tandem with greater volume.
      • Maxwell B.G.
      • Powers A.J.
      • Sheikh A.Y.
      • Lee P.H.
      • Lobato R.L.
      • Wong J.K.
      Resource use trends in extracorporeal membrane oxygenation in adults: an analysis of the nationwide inpatient sample 1998-2009.
      ,
      • Bailey K.L.
      • Downey P.
      • Sanaiha Y.
      • Aguayo E.
      • Seo Y.J.
      • Shemin R.J.
      • et al.
      National trends in volume-outcome relationships for extracorporeal membrane oxygenation.
      Indeed, several theories have been proffered to explain this phenomenon and include, first, an acknowledgment that these centers tend to manage the highest-acuity patients consistent with the accepted, oft expected ethos of specialized centers. Second, the existence of programmatic “hub-and-spoke” models that effectively direct locoregional referrals to a main quaternary center from a peripheral base of community hospitals, often lacking the infrastructure to support patients on ECMO.
      • Sanaiha Y.
      • Bailey K.
      • Downey P.
      • Seo Y.J.
      • Aguayo E.
      • Dobaria V.
      • et al.
      Trends in mortality and resource utilization for extracorporeal membrane oxygenation in the United States: 2008-2014.
      The transfer to a higher level of care often occurs with little resistance from the receiving hospital, which must then assume an unpredictable burden of morbidity and mortality. Bailey and colleagues
      • Bailey K.L.
      • Downey P.
      • Sanaiha Y.
      • Aguayo E.
      • Seo Y.J.
      • Shemin R.J.
      • et al.
      National trends in volume-outcome relationships for extracorporeal membrane oxygenation.
      estimated mortality rates of 59% and 54% for transferred versus index patients, respectively. Third, quaternary referral centers replete with robust multidisciplinary infrastructure, and personnel may be more liberal with the use of ECMO.
      • Bailey K.L.
      • Downey P.
      • Sanaiha Y.
      • Aguayo E.
      • Seo Y.J.
      • Shemin R.J.
      • et al.
      National trends in volume-outcome relationships for extracorporeal membrane oxygenation.
      There is a notion, however, that the use of ECMO has outstripped existing evidence, and there is a growing demand for objective quantification and improvement of outcomes. Technological design and clinical expertise will promote the use of criteria to guide patient selection better and explicitly demarcate contraindications. In this way, enhance decision-making at the bedside. To this end, there has been an evolution in practice with a growing interest in left ventricular decompression to decrease left ventricular afterload and mitigate the distension that accompanies the pressurization of the arterial system in venoarterial ECMO.
      • Tepper S.
      • Masood M.F.
      • Garcia M.B.
      • Pisani M.
      • Ewald G.A.
      • Lasala J.M.
      • et al.
      Left ventricular unloading by Impella device versus surgical vent during extracorporeal life support.
      ,

      Vallabhajosyula S, O'Horo JC, Antharam P, Ananthaneni S, Vallabhajosyula S, Stulak JM, et al. Impella on top of ECMO treatment in cardiogenic shock results in effective left ventricular unloading. Presented at: EuroIntervention; 2015.

      This is viewed as a means of optimizing cardiac function and may be achieved through several different techniques that include atrial septostomy, placing a vent through the left ventricle and most commonly, through the use of an Impella device (Abiomed, Danvers, Mass) or intra-aortic balloon pump.
      • Tepper S.
      • Masood M.F.
      • Garcia M.B.
      • Pisani M.
      • Ewald G.A.
      • Lasala J.M.
      • et al.
      Left ventricular unloading by Impella device versus surgical vent during extracorporeal life support.

      Vallabhajosyula S, O'Horo JC, Antharam P, Ananthaneni S, Vallabhajosyula S, Stulak JM, et al. Impella on top of ECMO treatment in cardiogenic shock results in effective left ventricular unloading. Presented at: EuroIntervention; 2015.

      • Vallabhajosyula S.
      • O’Horo J.C.
      • Antharam P.
      • Ananthaneni S.
      • Vallabhajosyula S.
      • Stulak J.M.
      • et al.
      Concomitant intra-aortic balloon pump use in cardiogenic shock requiring veno-arterial extracorporeal membrane oxygenation: a systematic review and meta-analysis.
      • Pappalardo F.
      • Schulte C.
      • Pieri M.
      • Schrage B.
      • Contri R.
      • Soeffker G.
      • et al.
      Concomitant implantation of Impella® on top of veno-arterial extracorporeal membrane oxygenation may improve survival of patients with cardiogenic shock.
      • Stulak J.M.
      • Dearani J.A.
      • Burkhart H.M.
      • Barnes R.D.
      • Scott P.D.
      • Schears G.J.
      ECMO cannulation controversies and complications.
      • Russo J.J.
      • Aleksova N.
      • Pitcher I.
      • Couture E.
      • Parlow S.
      • Faraz M.
      • et al.
      Left ventricular unloading during extracorporeal membrane oxygenation in patients with cardiogenic shock.
      Mortality is greatest in patients with CS and lowest in patients at post-transplantation. The opposite is true, however, for LOS. Comparison of charges, however, yields diametrically opposite results depending on whether the consideration is individual or cumulative hospitalizations. Individual hospitalizations are lowest in CS but greatest in transplantation. For cumulative charges, however, the opposite is true, and these are driven, not by the seemingly high cost of transplantation, but by the comparatively greater volume of individual PCS-ECMO cases compared with the fairly small, and relatively stable, number of transplantations requiring ECMO. The mean total charges per hospitalization range from USD 97,000 to 600,000.
      • Harvey M.J.
      • Gaies M.G.
      • Prosser L.A.
      US and international in-hospital costs of extracorporeal membrane oxygenation: a systematic review.
      The median duration of ECMO has been estimated at 9 days.
      • Harvey M.J.
      • Gaies M.G.
      • Prosser L.A.
      US and international in-hospital costs of extracorporeal membrane oxygenation: a systematic review.
      The average LOS is 18 days.
      • Maxwell B.G.
      • Powers A.J.
      • Sheikh A.Y.
      • Lee P.H.
      • Lobato R.L.
      • Wong J.K.
      Resource use trends in extracorporeal membrane oxygenation in adults: an analysis of the nationwide inpatient sample 1998-2009.
      ,
      • Snell G.I.
      • Rabinov M.
      • Griffiths A.
      • Williams T.
      • Ugoni A.
      • Salamonsson R.
      • et al.
      Pulmonary allograft ischemic time: an important predictor of survival after lung transplantation.
      The use of ECMO for cardiac conditions was associated with a mean of USD 530,000.
      • Harvey M.J.
      • Gaies M.G.
      • Prosser L.A.
      US and international in-hospital costs of extracorporeal membrane oxygenation: a systematic review.
      These charges have increased in the later years, with the majority of the costs attributed to personnel, often perfusionists or ECMO specialists at the bedside. Medication and procedures surprisingly represent less than 10% of charges.
      • Mishra V.
      • Svennevig J.L.
      • Bugge J.F.
      • Andresen S.
      • Mathisen A.
      • Karlsen H.
      • et al.
      Cost of extracorporeal membrane oxygenation: evidence from the Rikshospitalet University Hospital, Oslo, Norway.
      ,
      • Tseng Y.H.
      • Wu M.Y.
      • Tsai F.C.
      • Chen H.J.
      • Lin P.J.
      Costs associated with extracorporeal life support used in adults: a single-center study.
      This underscores the value in training a “homegrown” institution-specific cadre of nursing staff and respiration therapists capable of performing the bedside monitoring to mitigate the daily costs, reportedly ranging from USD 18,000 and USD 40,000.
      • Harvey M.J.
      • Gaies M.G.
      • Prosser L.A.
      US and international in-hospital costs of extracorporeal membrane oxygenation: a systematic review.
      ,
      • Bott R.
      Applied methods of cost-effectiveness analysis in health care.
      Indeed, in our own experience, a perfusion-led program can result in triple the costs.
      The majority of published reports on the high cost of ECMO typically report these in the context of individual cases and hospitalizations. In these discussions, transplantation is highlighted as a costly indication for ECMO. Indeed, the use of ECMO as a bridge to LT raises charges by 50%.
      • Hayanga J.A.
      • Shigemura N.
      • Aboagye J.K.
      • Ensor C.
      • Dew M.A.
      • Hayanga H.K.
      • et al.
      ECMO support in lung transplantation: a contemporary analysis of hospital charges in the United States.
      That notwithstanding, the total number of cases in which ECMO was used in this manner between 2005 and 2017 was only 600. In the same vein, the total number of heart transplants performed in any given year rarely exceeds 3500. Thus, transplantation charges seem much higher in comparison, whereas, in reality, the number of patients undergoing transplantation is much smaller. PCS accounts for 57% of all ECMO cases.
      • Sanaiha Y.
      • Bailey K.
      • Downey P.
      • Seo Y.J.
      • Aguayo E.
      • Dobaria V.
      • et al.
      Trends in mortality and resource utilization for extracorporeal membrane oxygenation in the United States: 2008-2014.
      The corresponding comparative cumulative charges for hospitalization are also much lower. A focus on cumulative charges per indication and provides a unique global portrait of the financial footprint by ECMO on the health system as a whole.
      The staggering scope of charges is likely to spark a debate about the establishment of criteria for eligibility. This, in the case of PCS and CS, is likely to favor patients with the most optimal outcomes who typically have been younger and with fewer comorbidities without the burden of advanced age, ischemic cardiomyopathy, or right ventricular failure, each of which impairs survival. Indeed, recovery is typically apparent within 4 days of support, beyond which mortality is greater.
      • Fux T.
      • Holm M.
      • Corbascio M.
      • Lund L.H.
      • van der Linden J.
      Venoarterial extracorporeal membrane oxygenation for postcardiotomy shock: risk factors for mortality.
      • Chen S.W.
      • Tsai F.C.
      • Lin Y.S.
      • Chang C.H.
      • Chen D.Y.
      • Chou A.H.
      • et al.
      Long-term outcomes of extracorporeal membrane oxygenation support for postcardiotomy shock.
      • Grunau B.
      • MacRedmond R.
      • Gill J.
      A promising therapy in jeopardy.
      As the collective experience expands further, a variety of contraindications is likely to emerge. Aortic dissection, for example, has a particularly poor prognosis and is slowly emerging as a contraindication. Anecdotally, patients with infective endocarditis also have poor outcomes with the use of ECMO and represent a growing contraindication for extracorporeal support. The duration of support also proffers prognostic value, and typically, patients who do not respond clinically within 4 days have poor survival. The timely identification of these patients may allow early determination of futility. It may be used to define a set of contraindications to extracorporeal support, particularly in the context of CS and extracorporeal cardiopulmonary resuscitation.
      • Distelmaier K.
      • Wiedemann D.
      • Binder C.
      • Haberl T.
      • Zimpfer D.
      • Heinz G.
      • et al.
      Duration of extracorporeal membrane oxygenation support and survival in cardiovascular surgery patients.
      Respiratory failure and transplantation are associated with the lowest mortality, whereas patients receiving ECMO support for CS have the greatest mortality. A vast amount of resources is, thus, paradoxically, spent on patients with the lowest chances of survival. Previous cost considerations have centered on the price of individual hospitalization, and, as such, transplantation dominates the single hospitalization cost category at approximately USD 1 million. Transplant hospitalizations, however, are, in turn, characterized by prolonged LOS, whereas those associated with CS are significantly shorter.
      • Maxwell B.G.
      • Powers A.J.
      • Sheikh A.Y.
      • Lee P.H.
      • Lobato R.L.
      • Wong J.K.
      Resource use trends in extracorporeal membrane oxygenation in adults: an analysis of the nationwide inpatient sample 1998-2009.
      ,
      • Harvey M.J.
      • Gaies M.G.
      • Prosser L.A.
      US and international in-hospital costs of extracorporeal membrane oxygenation: a systematic review.
      ,
      • Vallabhajosyula S.
      • Arora S.
      • Sakhuja A.
      • Lahewala S.
      • Kumar V.
      • Shantha G.P.
      • et al.
      Trends, predictors, and outcomes of temporary mechanical circulatory support for postcardiac surgery cardiogenic shock.
      These lower costs and the short LOS, however, are each counterbalanced by the sheer magnitude of the volume of ECMO used for CS and represent a considerably larger denominator.
      • Harvey M.J.
      • Gaies M.G.
      • Prosser L.A.
      US and international in-hospital costs of extracorporeal membrane oxygenation: a systematic review.
      ,
      • Vallabhajosyula S.
      • Arora S.
      • Sakhuja A.
      • Lahewala S.
      • Kumar V.
      • Shantha G.P.
      • et al.
      Trends, predictors, and outcomes of temporary mechanical circulatory support for postcardiac surgery cardiogenic shock.
      There is a pressing impetus to contain costs and prove the value of resource-intensive technologies currently deployed in contemporary health care and injudicious use of ECMO in the face of dire survival probability may come under greater scrutiny and disapproval. Whereas this may not be the first report of the magnitude of charges attributable to cardiogenic indications for ECMO, this will be the first that addresses the quantity in cumulative terms. There is a growing trend toward value-based rather than volume-based models of care, and the federal government has already attempted to reconfigure ECMO reimbursement. Health economists, however, will likely continue to seek metrics to quantify and improve the quality of care in a bid to reduce healthcare costs and allow more thoughtful and stringent selection of candidates.
      The study has several limitations. First, the use of total charges does not equate to cost and there is a complicated, nonlinear relationship between reimbursement, charges, and cost. Second, the use of ICD codes does not allow for any distinction between venoarterial and venovenous-ECMO support. Third, the use of administrative data is fraught with bias and missing data as well as a likely host of other unmeasured confounding factors. Fourth, because the data pertain only to centers in the United States, the results may not necessarily be generalizable, particularly as costs in the United States are often in excess of this in non-US settings. Fifth, we did not calculate incremental costs that would have served to differentiate costs between those patients who received support versus those who did not. Sixth, the charges here pertain to the entire hospitalization and are not necessarily ECMO-specific. Furthermore, the limitations related specifically to the use of NIS data are myriad and include the inability to evaluate center-specific volume outcomes, discharges outside the index center, long-term outcomes, differences between perfusion-led and specialist-led models, or identify patients bridged to destination therapy. To this end, there are no data regarding concomitant devices or techniques such as left ventricular venting or the use of Impella intra-aortic- balloon pump, etc. Finally, the absence of granular detail precludes the ability to perform a more detailed risk-adjustment, which would, in turn, proffer an even more accurate analysis.
      In summary, this is the first study to report ECMO survival in the context of cumulative charges stratified by indication in the contemporary era, highlighting the billion-dollar impact it bears on the health care system. Like previous studies, it highlights the disproportionate burden that PCS exerts on mortality at an individual level and acknowledges that this is increasing with time.
      • Whitman G.J.
      Extracorporeal membrane oxygenation for the treatment of postcardiotomy shock.
      As such, we also draw attention to the excess financial burden borne by the sheer volume of cases and proffer a lens through which interventions and policy may be viewed and challenged to refine the selection process and indications for ECMO, seeking to perpetuate the quest for improved quality and accountability so as to satisfy the needs of a system that is leaning ever closer to value-based model of health care delivery.

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      Conflict of Interest Statement

      The authors reported no conflicts of interest.
      The Journal policy requires editors and reviewers to disclose conflicts of interest and to decline handling or reviewing manuscripts for which they may have a conflict of interest. The editors and reviewers of this article have no conflicts of interest.

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      Linked Article

      • Commentary: Extracorporeal membrane oxygenation: Is it life-saving and cost effective for all patients?
        JTCVS OpenVol. 1
        • Preview
          There has been a tremendous increase in the use of extracorporeal membrane oxygenation (ECMO) over the past decade. Advances in ECMO equipment and technology have expanded the use of this technique to treat not only severe adult respiratory failure (SARF) but also as a temporary form of mechanical support for patients with postcardiotomy syndrome (PCS), cardiogenic shock (CS), and as a bridge to heart transplantation (HT) and lung transplantation (LT). However, ECMO is expensive and costs can range from 20,000 to 40,000 USD per day of hospitalization.
        • Full-Text
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        Open Access
      • Commentary: To ECMO or not to ECMO: That is the question
        JTCVS OpenVol. 1
        • Preview
          In the current issue of the Journal, Hayanga and colleagues1 use the Nationwide Inpatient Sample database to assess hospital charges and outcomes after extracorporeal membrane oxygenation (ECMO) in more than 15,000 patients based on indication and time period. ECMO in the perioperative period for heart (HT) and lung transplant (LT) resulted in the longest length of stay and duration of ECMO support and, not surprisingly, carried the greatest charges per patient by far (∼1.5 million USD). ECMO for postcardiotomy shock (PCS) and cardiogenic shock (CS) resulted in shorter length of stay and duration of ECMO support and carried lower per-patient charges.
        • Full-Text
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        Open Access