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Original Clinical Science—General

Long-term Outcome in Severe Left Ventricular Primary Graft Dysfunction Post Cardiac Transplantation Supported by Early Use of Extracorporeal Membrane Oxygenation

Connolly, Sophie MD, MMed1; Granger, Emily FRACS2,3; Hayward, Christopher MD, FRACP3,4; Huang, David MD3; Kerr, Stephen PhD5,6; McCanny, Peter MBChB, FACEM, FCICM1,7; Buscher, Hergen DEAA, FCICM1,3,8

Author Information
doi: 10.1097/TP.0000000000003094
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Abstract

INTRODUCTION

Severe primary graft dysfunction (PGD) is the leading cause of early death following cardiac transplantation, with a 30-day mortality of up to 42%.1-6 PGD is a relatively common occurrence following orthotopic cardiac transplantation with a reported prevalence of up to 30%,1,5,6 acknowledging the significant heterogeneity of prevalence and mortality data in the existing literature, in part because of an inconsistency in definitions used by individual transplant centers.7 In 2014, the International Society for Heart and Lung Transplantation published a consensus statement on the definition, diagnosis, and management of PGD following cardiac transplantation. Severe left ventricular PGD (PGD-LV) is a subset of PGD, defined as the dependence on left or biventricular mechanical support in the first 24 hours following completion of cardiac transplantation.8

Despite inconsistencies in diagnosis and reporting, it is evident that there is an increasing incidence of PGD that is ubiquitous across transplant centers. As transplant centers continue to face donor shortages and growing recipient waiting lists, there has been an increased reliance on organs from “marginal” donors9-11 that do not meet traditional criteria for donation, such as those with increased age and the presence of left ventricular (LV) dysfunction.3,8 Recipient age and complexity have also increased, with greater numbers of patients being transplanted from chronic mechanical support over the last 10 years.12 Furthermore, in Australia, the greater geographical retrieval distance for donor organs contributes to prolonged ischemic time.13 These factors increase the risk of PGD and short-term mortality following cardiac transplantation.3,13,14

A recent systematic review of temporary mechanical circulatory support devices for PGD following cardiac transplantation revealed venoarterial extracorporeal membrane oxygenation (VA-ECMO) to be the most widely used modality.2 Single and multicenter data on the use of VA-ECMO for severe PGD report varying outcomes, with survival to hospital discharge rates of between 53% and 79%.6,7,10,15-18 An early report from our institution described a 30-day survival rate of 84% in a series of 17 patients who received VA-ECMO for severe PGD-LV.9 The aim of our current study was to describe our experience with VA-ECMO for patients with severe PGD-LV postorthotopic cardiac transplantation, with particular focus on both short- and longer-term outcomes.

MATERIALS AND METHODS

St Vincent’s Hospital, Sydney, serves as the heart and lung transplant center for the state of New South Wales, Australia (population 7 million). We conducted a retrospective review of hospital patient medical records of all patients who underwent an orthotopic heart transplantation from January 2009 to February 2016. Follow-up was until death or until March 1, 2017, whichever came first. Local ethical approval was granted, and the need for written patient consent was waived.

We included patients with biventricular PGD and severe PGD-LV post cardiac transplantation, defined according to the recent consensus report of the International Society for Heart and Lung Transplantation.8 Data collected included donor and recipient characteristics, intraoperative and postoperative variables and patient outcomes. The RADIAL score19 was not calculated retrospectively to predict postoperative risk of PGD in this cohort as data regarding preoperative right atrial pressure and donor age were not collected.

The initiation of VA-ECMO in patients with PGD-LV post cardiac transplantation was largely a clinical decision in this patient cohort, based on echocardiographic graft performance and lack of response to first-line therapy including inotropic support. Graft function during separation from cardiopulmonary bypass post transplantation was continuously assessed by intraoperative transesophageal echocardiography (TOE) and inotropes including adrenaline, milrinone or dobutamine progressively escalated. Similarly, for patients who separated from cardiopulmonary bypass and were admitted to the intensive care unit (ICU) post transplantation, serial assessments of cardiac function using TOE were made to first guide progressive escalation of inotropic supports and then consideration of VA-ECMO. Mechanical circulatory support with VA-ECMO was initiated post cardiac transplantation if there was significant hemodynamic instability refractory to titration of inotropes and pulmonary vasodilators, either while weaning from cardiopulmonary bypass or within 24 hours of admission to the ICU. Following initiation of VA-ECMO, pharmacological supports were subsequently titrated based on hemodynamic parameters and serial TOE assessments of graft function, aiming to maintain biventricular ejection and adequate end-organ perfusion. Equipment used included centrifugal pumps (Rotaflow or Cardiohelp) with polymethylpentene hollow-fiber membrane oxygenators (Quadrox-D) and heparin-coated circuits (all Maquet Getinge Group, Rastatt, Germany). Intravenous heparin was used according to activated partial thromboplastin time targets and usually commenced after 24 hours of surgery and only if bleeding was controlled.

Cannulation was performed either peripherally or centrally, with the preference being for peripheral cannulation, and central cannulae placed only if the chest was to be left open. All peripheral VA-ECMO configurations included use of a distal limb perfusion cannula, inserted into the superficial femoral artery either by percutaneous or open approach. There was a flowmeter to ensure adequacy of distal limb perfusion and if cannula occlusion or kinking was suspected, this was revised in theatres. If an intraaortic balloon pump was inserted before cannulation it remained in situ, with the aim of improving coronary perfusion pressure and decompressing the left ventricle.

In the context of improving graft function, a systematic TOE weaning study was undertaken to assess graft function and hemodynamics at decremental VA-ECMO flow settings. Patients were subsequently decannulated in the operating theatre with concurrent assessment of the need for thrombectomy and arterial repair.

Statistical Analysis

Categorical variables are expressed as frequencies and percentages and compared using the Fisher exact test. Continuous variables are expressed as median (interquartile [IQ] range) and compared using the Mann–Whitney–Wilcoxon test. The survival rate was calculated using Kaplan–Meier analysis and compared using the log-rank test for categorical variables. Potential independent predictors of survival in this patient cohort were identified using univariable and multivariable logistic regression. Univariable testing was performed to identify variables for which P < 0.1 which were then included in a multivariable logistic regression model. A P of <0.05 was considered statistically significant. The statistical software used was Stata 15 (StataCorp, TX, USA).

RESULTS

A total of 192 patients underwent cardiac transplantation at our institution (Table 1). Forty-nine (25%) of these developed severe PGD requiring VA-ECMO, comprising our main study population.

TABLE 1. - Baseline and perioperative characteristics of all heart transplantations
Characteristic a Total (n = 192) ECMO (n = 49) No ECMO (n = 143) P
Age (y) 51 (18.25) 53 (13.12) 51 (18) 0.48
Male 129 (67%) 33 (67%) 96 (67%) 1.00
Weight (kg) 73 (20.68) 77 (19.3) 72 (21.45) 0.45
Height (cm) 172 (14) 172 (15) 172 (13.5) 0.93
LVAD before transplant 58 (30%) 20 (40%) 38 (27%) 0.07
Previous sternotomy 80 (41%) 29 (59%) 51 (36%) 0.019
DCD heart 8 (2%) 2 (4%) 6 (4%) 1.00
Donor ischemic time (min) 224 (112) 232 (96.5) 222 (112.5) 0.18
Cardiopulmonary bypass time (min) 193 (75) 220 (63) 176 (73) <0.001
Total operation time (min) 439.8 (150) 495 (139.8) 412.8 (132) <0.001
Characteristics in bold were significantly associated with the use of VA-ECMO post cardiac transplantation.aContinuous data are presented as median (IQ range) and categorical as number (%).
DCD, donation after circulatory death; ECMO, extracorporeal membrane oxygenation; IQ, interquartile; LVAD, left ventricular assist device.

Pretransplantation data for all patients are presented in Table 1. Significantly more patients in the ECMO group had undergone prior sternotomy (29 [59%] versus 51 [36%], P = 0.019) and 40% of the ECMO patients versus 27% of non-ECMO patients had a left ventricular assist device (LVAD) (HeartWare HVAD, Framingham, USA) in situ before transplantation (P = 0.07). Operation time and time spent on cardiopulmonary bypass were significantly longer in patients who required subsequent ECMO support (P < 0.001).

Detailed pre- and perioperative data of the ECMO cohort are presented in Table 2. The most common indications for transplantation were dilated idiopathic cardiomyopathy (49%), ischemic cardiomyopathy (22%), and hypertrophic cardiomyopathy (18%). Median follow-up time was 508 days (IQ range 1201 d) post cardiac transplantation. The decision was made to place LV vents in 3 patients after commencing VA-ECMO based on echocardiographic findings of LV dilatation, a closed aortic valve and no ejection. Vents were placed in theatres into the left ventricle. Forty-three patients (88%) were successfully weaned from VA-ECMO after a median duration of 108 hours (IQ range 69.6 h). All 43 patients who were successfully weaned from VA-ECMO survived to ICU discharge, and 39 patients (80%) survived to hospital discharge. One-year survival in the ECMO cohort was 71% (35 patients). All patients who survived to 1 year had a normal left ventricular ejection fraction at 12-month follow-up (median 70%, IQ range 8.8).

TABLE 2. - Detailed characteristics of the ECMO cohort and 1-y survival
Characteristic a All ECMO
(n = 49)
Alive at 1 y (n = 35) Not alive at 1 y (n = 14)
Age (y) 53 (13.12) 53 (18) 52.5 (18.5)
Male (%) 33 (67%) 27 (77%) 7 (50%)
Weight (kg) 77 (19.3) 77 (20.2) 75.8 (17.8)
Height (cm) 172 (15) 172 (12.5) 165.5 (13.5)
New York Heart Association Classification
 II 5 (10%) 5 (29%) 0
 III 33 (70%) 24 (69%) 10 (71%)
 IV 10 (20%) 6 (17%) 4 (29%)
Left ventricular ejection fraction (%) 27 (17.5%) 24 (15.3%) 33 (21.6%)
Chronic kidney disease 37 (76%) 26 (74%) 11 (79%)
Baseline creatinine (µmol/L) 110 (45) 112 (39) 103 (233.5)
Type 2 diabetes mellitus 10 (20%) 5 (14%) 5 (36%)
LVAD before transplant 20 (41%) 14 (40%) 6 (43%)
Implantable cardioverter defibrillator 37 (76%) 27 (77%) 10 (71%)
Previous sternotomy 29 (59%) 20 (57%) 9 (64%)
Donor ischemic time (min) 232 (96.5) 229 (90) 258 (89)
Cardiopulmonary bypass time (min) 220 (63) 211 (51) 258.5 (49.5)
Duration of ECMO support (h) 108 (69.6) 93.6 (43.2) 129.95 (71.4)
Central cannulation 8 (16%) 5 (14%) 3 (21%)
Transfused blood products in the first 48 h
 Red blood cells (units) 8 (12) 8 (11.25) 10 (12.25)
 Cryoprecipitate (units) 8 (14) 10 (14) 6 (21)
 Fresh frozen plasma (units) 4 (8) 4 (8.5) 5 (9.25)
 Platelets (units) 3 (4) 4 (4) 2.5 (4)
Complications
 Any ECMO-related complication 18 (37%) 11 (31%) 7 (50%)
 Lower limb ischemia 9 (18%) 4 (11%) 5 (36%)
 Bacteremia 4 (8%) 3 (8%) 1 (7%)
 Left ventricular clot 3 (6%) 2 (6%) 1 (7%)
 Neurological complication b 3 (6%) 3 (8%) 0
aContinuous data are presented as median (IQ range) and categorical as number (%).
bNeurological complications included right MCA stroke and left MCA embolic infarct.
ECMO, extracorporeal membrane oxygenation; IQ, interquartile; LVAD, left ventricular assist device.

VA-ECMO was associated with significant morbidity, and 18 patients (37%) experienced a complication related to VA-ECMO. The most frequent postoperative ECMO-related complication was lower limb ischemia (18%), which was associated with clotting of the backflow cannula in all 9 patients. Of these, 4 patients required fasciotomies and 2 patients required amputation. Other complications were bacteremia (8%), left ventricular thrombus (6%), pulmonary embolism and ischemic stroke (both 4%), deep vein thrombosis, hemolysis, hemothorax, and pulmonary hemorrhage (1 case each). Five patients required a circuit change.

In a multivariable logistic regression model (Table 3), baseline creatinine in µmol/L (odds ratio [OR] 0.99 [95% confidence interval {CI} 0.99-1.00], P = 0.019) and duration of ECMO support in days (OR 0.65 [95% CI 0.44-0.97], P = 0.034) were inversely and independently associated with 1-year survival. Male gender (OR 7.48, P = 0.031) was also independently associated with 1-year survival with a wide 95% CI of 1.2-46.39. Long-term survival in the ECMO group was significantly lower compared to non-ECMO patients (Figure 1) but equivalent when conditioned on hospital survival. Those patients who were weaned from ECMO earlier than our median runtime of 108 hours had a similar 1-year survival compared to those who did not require ECMO (Figure 2).

TABLE 3. - Multivariable logistic regression model for 1-y survival in the ECMO cohort
Variables Univariate analysis Multivariate analysis for P < 0.1 in univariable analysis
OR 95% CI P OR 95% CI P
Age 1.01 0.96-1.06 0.76
Male 3.38 0.85-13.41 0.084 7.48 1.20-46.39 0.031
Weight 1.01 0.97-1.05 0.76
Height 1.01 0.94-1.08 0.78
New York Heart Association Classification 0.35 0.10-1.26 0.11
Left ventricular ejection fraction (%) 0.98 0.94-1.01 0.23
Chronic kidney disease 0.96 0.21-4.36 0.96
Baseline creatinine (µmol/L) 1.00 0.99-1.00 0.064 0.99 0.99-1.00 0.019
Type 2 diabetes mellitus 0.33 0.72-1.54 0.16
LVAD before transplant 0.67 0.18-2.49 0.55
ICD before transplant 1.13 0.24-5.18 0.88
Previous sternotomy 0.67 0.17-2.63 0.56
Donor ischemic time (min) 1.00 0.99-1.01 0.87
CPB time (min) 1.00 0.98-1.01 0.45
Duration of ECMO (d) 0.71 0.52-0.97 0.033 0.65 0.44-0.97 0.034
Transfused blood products in the first 48 h
 Red blood cells 0.99 0.90-1.08 0.78
 Cryoprecipitate 1.00 0.94-1.06 0.99
 Fresh frozen plasma 1.00 0.91-1.10 0.99
 Platelets 1.04 0.86-1.25 0.72
 Perioperative complications 0.30 0.56-1.62 0.16
CI, confidence interval; CPB, cardiopulmonary bypass; ECMO, extracorporeal membrane oxygenation; ICD, implantable cardioverter defibrillator; LVAD, left ventricular assist device; OR, odds ratio.

FIGURE 1.
FIGURE 1.:
Kaplan–Meier survival estimate curves for patients who required VA-ECMO for PGD post cardiac transplantation compared to patients who did not require VA-ECMO post cardiac transplantation. PGD, primary graft dysfunction; VA-ECMO, venoarterial extracorporeal membrane oxygenation.
FIGURE 2.
FIGURE 2.:
Kaplan–Meier survival estimate curves for median duration of VA-ECMO support. VA-ECMO, venoarterial extracorporeal membrane oxygenation.

DISCUSSION

The main findings in our study are first, that our incidence of PGD was high and we could identify some potential risk factors for PGD in our cohort. Second, the likelihood of survival at 1 year after development of PGD was independently associated with baseline renal function and the duration of ECMO support. Third, graft function recovered to normal levels for all survivors and finally, long-term survival in severe PGD was better than previously described but still inferior to that of patients who did not develop the condition. Early recovery of PGD on VA-ECMO support negates its negative impact on short- and long-term survival.

In comparison to our cohort, the prevalence of PGD requiring temporary circulatory mechanical support reported by Phan et al was relatively low at 6.0%.2 This lower prevalence of PGD is also described in a retrospective review by Jacob et al, who reported just 31 of their 1030 patients (3%) who underwent cardiac transplantation to have developed PGD requiring VA-ECMO.20 However, other single-center series have reported a prevalence of up to 28.2%.8,11,18,21 As acknowledged by Phan et al, this likely reflects heterogeneity of PGD definitions between studies and institutional management preferences.2 In addition, the incidence of severe PGD post cardiac transplantation is rising, posing a significant challenge to transplant centers as growing recipient waiting lists obligate the use of “marginal” donors. Longer waiting lists also translates to increased frailty and more frequent LVAD use in the recipient population.3,14,21 Long procedural and cardiopulmonary bypass time are also associated with these recipient risk factors for PGD; and, concurrent with the literature6,8,21 we could demonstrate that this is also associated with a higher incidence of PGD. Long organ retrieval times secondary to the geography of Australia as well as relatively favorable outcomes in our institution may have also contributed to a higher utilization of VA-ECMO in comparison to other centers.

There is a paucity of published literature describing pretransplantation factors that may influence outcomes in patients with severe PGD. However, long-term follow-up on these patients is rare. In our cohort, 1-year survival was significantly influenced by the degree of chronic kidney disease rather than its presence per se. Our study is likely underpowered to confirm any true association and larger multicenter investigations are needed, however type 2 diabetes mellitus was more frequent in the patients who did not survive to 1 year. These factors do reflect the risk factors for development of PGD identified in a retrospective review of 450 adult heart transplants performed over a 3-year period in the United Kingdom6 and they may remain important after the development of PGD.

In our patient cohort, the use of VA-ECMO for severe PGD post cardiac transplantation provided temporary hemodynamic support and subsequent opportunity for graft recovery in a patient cohort which by definition is expected to have inferior short- and long-term survival. The cohort size of our study is relatively large in comparison to similar publications, and data have been reviewed over a 7-year period, adding value to the body of existing literature describing the management of severe PGD. The survival to hospital discharge and 1-year survival rates of 80% and 71%, respectively, are favorable when compared with previous publications6,7,10,15-22 and similar to the 30-day survival described in an earlier series from our institution.9 A recent systematic literature review and meta-analysis by Phan et al examined outcomes with the use of various temporary circulatory mechanical support devices for PGD post cardiac transplantation.2 Our survival to hospital discharge compares favorably to the pooled outcome data of patients who received VA-ECMO in that study (51.5% versus 80%), and to outcome data from centers reporting a similar prevalence of PGD.18,20,23 This is likely multifactorial, reflecting heterogeneity of study design, case-mix, varying experience between institutions, and changes in survival over time. Extracorporeal support developed considerably over the last decade and we only included patients treated during the “modern era of ECMO.”24 However, the long-term outcome of patients in this cohort is still inferior to that of patients without severe PGD, secondary to early hospital mortality. Conditioned on hospital survival we could demonstrate that patients with severe PGD managed with VA-ECMO not only have a similar long-term survival but also display full recovery of graft function. Importantly, the patients who had a fast recovery of graft function demonstrated by a short period of VA-ECMO support had a hospital and long-term survival similar to patients without PGD. The same time-dependent effect of VA-ECMO used for all indications has previously been demonstrated by Smith et al25 which could allow the conclusion that the intervention is safe and possibly beneficial. Lower survival in patients supported for a longer period may be because of poor recovery of the graft and hence part of the natural course of PGD or secondary to acquired ECMO-related complications. Seven out of 16 female patients who required VA-ECMO died. It is most likely that this small cohort overcalls any significant predictor of mortality with a very wide 95% CI. Preoperatively impaired renal function however was an independent predictor of 1-year survival which demonstrates its importance particularly when it is associated with PGD. Although preoperative renal function has not been directly associated with poor long-term outcome following cardiac transplantation, it is associated with an increased risk of PGD8 and impaired renal function postoperatively.26 Furthermore, persistent renal impairment post heart transplantation is associated with worse short- and long-term outcomes.27 Therefore, the significance of preoperative renal function as a predictor of outcome in all heart transplantation patients, and particularly those that develop PGD, is an area for further investigation.

Optimal timing for institution of VA-ECMO in the setting of PGD post cardiac transplantation remains unclear. Of our patients with biventricular or PGD-LV, 73% had VA-ECMO initiated in the operating theatre, and our favorable short- and long-term outcomes suggest that early institution of mechanical support may be beneficial. This is supported by the findings of Kittleson et al who reported a statistically significant difference in survival to hospital discharge and 6-year survival in patients with PGD that had VA-ECMO placed preemptively, in comparison to those in which it was used as salvage therapy.15 Similarly, 2 other institutions have described improved short-term outcomes in patients who had VA-ECMO initiated in the operating theatre, immediately post transplantation.7,28 It is scientifically plausible that the early institution of VA-ECMO may aid graft recovery by facilitating down-titration of inotropes and vasopressors, while organ perfusion is maintained. Importantly, ECMO can also increase the cardiac afterload and managing necessary flows and duration of support is essential for a successful application.

Severe PGD postcardiac transplantation by definition mandates a form of mechanical circulatory support.8 Our center uses VA-ECMO in this setting in preference to ventricular assist devices. This is supported by the findings of several retrospective reviews demonstrating improved outcomes, including survival to hospital discharge and 1-year survival, in patients who received VA-ECMO in comparison to ventricular assist devices for management of severe PGD post cardiac transplantation.2,29,30

Thirty-seven percent of our patients did experience a complication associated with VA-ECMO, the majority of these being lower limb ischemia (18% of patients). Vascular complications associated with the use of VA-ECMO for PGD are a significant cause of morbidity with reported rates between 2% and 36%.11,15 Some institutions report a preference for central rather than peripheral cannulation, describing decreased vascular complications and improved venous drainage.11,18 Our single-center population is too small to make a meaningful comparison; however, this could be an area for future investigation. If VA-ECMO is to become the standard of treatment for severe PGD, we must continue to reduce associated complications with further research to elucidate optimal configuration and establish standards of monitoring. Newer devices including the Abiomed Impella (Abiomed Inc., Massachusetts, USA) may reduce afterload more efficiently and may have a role as an alternative to VA-ECMO or in combination; however, clinical experience is so far limited.31,32

There are several limitations of our study. Primarily, it is a retrospective review of a single-center experience. Therefore, the results described may not be applicable to other centers as they are based on local surgical and postoperative management practices. Additionally, outcomes were not compared with patients who did not receive VA-ECMO for PGD. In our institution, VA-ECMO is the preferred mechanical circulatory support for management of severe PGD-LV, and thus comparison against patients with PGD that did not have VA-ECMO was not possible. Finally, the incidence of the use of VA-ECMO for PGD-LV was high, consistent with a “preemptive” rather than “salvage” strategy, which may in part explain the low mortality demonstrated in our study. However, the overall long-term outcome of our cohort was comparable to international standards of patients who did not develop PGD and other factors in our local cohort such as the frequent use of pretransplant use of LVADs and long-distance organ retrievals may contribute to this observation.

CONCLUSION

In conclusion, we have demonstrated that VA-ECMO may offer a bridge to graft recovery in patients with severe PGD post cardiac transplantation. It is a viable management option, which is associated with a high complexity and complication rate but favorable short- and long-term outcomes. Patient with early recovery of severe PGD displayed no additional mortality risk when supported with VA-ECMO and long-term graft function recovered in all survivors.

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