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FEATURED PAPERS

Intermediate outcomes with ex-vivo allograft

perfusion for heart transplantation
Joshua L. Chan, MD,a,b Jon A. Kobashigawa, MD,a Heidi J. Reich, MD,a,b
Danny Ramzy, MD, PhD,a,b Maria M. Thottam, BS,a Zhe Yu, MD, MPH,a
Tamar L. Aintablian, BS,a Frank Liou, BS,a Jignesh K. Patel, MD, PhD,a
Michelle M. Kittleson, MD, PhD,a Lawrence S. Czer, MD,a Alfredo Trento, MD,a,b
and Fardad Esmailian, MDa,b

From the aCedars-Sinai Heart Institute, Los Angeles, California, USA; and the bDepartment of Surgery, Cedars-Sinai
Medical Center, Los Angeles, California, USA.

KEYWORDS:
ex-vivo perfusion;
heart preservation;
heart transplantation;
mechanical perfusion;
organ care system
BACKGROUND: The Organ Care System, an ex-vivo heart perfusion platform, represents an alternative
to the current standard of cold organ storage that sustains the donor heart in a near-physiologic state. It is
unknown whether using the Organ Care System influences 2-year outcomes after heart transplantation.
We reviewed our institutional experience to compare 2-year outcomes for patients randomized to the
Organ Care System or standard cold storage.
METHODS: Between 2011 and 2013, heart transplant candidates from a single tertiary-care medical
center enrolled within the PROCEED II trial were randomized to either standard cold storage or the
Organ Care System. Outcomes assessed included 2-year survival, freedom from cardiac allograft
vasculopathy (CAV), non-fatal major cardiac events (NF-MACE), biopsy-proven cellular rejection
(CMR) and biopsy-proven antibody-mediated rejection (AMR).
RESULTS: Thirty-eight patients were randomized to the Organ Care System (n ¼ 19) or cold storage
group (n ¼ 19). There was no significant difference in 2-year patient survival (Organ Care System:
72.2%; cold storage: 81.6%; p ¼ 0.38). Similarly, there were no differences in freedom from CAV,
NF-MACE, CMR or AMR. The Organ Care System group had significantly longer total ischemia time
(361 ⫾ 96 minutes vs 207 ⫾ 50 minutes; p o 0.001) and shorter cold ischemia time (134 ⫾ 45 minutes
vs 207 ⫾ 50 minutes; p o 0.001) compared with the cold storage group.
CONCLUSION: The Organ Care System did not appear to be associated with significant differences in
intermediate results compared with conventional strategies. These results suggest that this ex-vivo
allograft perfusion system is a promising and valid platform for donor heart transportation.
J Heart Lung Transplant 2017;36:258–263
r 2017 International Society for Heart and Lung Transplantation. All rights reserved.

Despite advances with modern medical therapy, heart failure
remains a leading cause of morbidity and mortality.1,2 Heart
transplantation is the only definitive therapeutic option for
patients with irreversible end-stage heart disease. The field of
Reprint requests: Fardad Esmailian, MD, Cedars-Sinai Heart Institute,
127 South San Vicente Boulevard A-3103, Los Angeles, CA 90048.
Telephone: 310-423-3851. Fax: 310-423-0127.
E-mail address: fardad.esmailian@cshs.org
1053-2498/$ - see front matter r 2017 International Society for Heart and Lung Transplantation. All rights reserved.
http://dx.doi.org/10.1016/j.healun.2016.08.015
heart transplantation continues to advance with innovations in
immunosuppressive therapies and allocation protocols; median
survival has improved to 11 years.3 However, a significant
disparity remains between the number of patients requiring heart
transplantation and the current supply of donor organs. The
number of heart transplant candidates continues to increase in
See Related Editorial, page 247
Chan et al. Ex-vivo Heart Transplant Perfusion 259

Figure 1 The Organ Care System (TransMedics, Andover, MA). (A) Schematic depiction of the Organ Care System unit components.
(B) Placement of donor heart within perfusion module. (C) Positioning of pulmonary artery cannula and (D) ascending aortic cannula,
allowing for uninterrupted warm ex-vivo perfusion.

the face of heart donation rates that have remained stagnant over
the past decade: 44,000 candidates currently remain on the
waiting list and it is estimated that approximately 10% will die
waiting for a heart transplant.4
The standard of care for management of the allograft from
time of harvest to implantation in the recipient is static cold
storage. This crucial stage has remained fundamentally the same
since the 1960s; it typically involves arresting the heart in situ
using a cardioplegia solution and placing the organ within a cold
ice bath to a storage temperature of 41C, resulting in a period
of non-function.5,6 In this ex-vivo environment, the allograft
is susceptible to cellular damage, and prolonged cold ische-
mia times 46 hours have been associated with early graft
failure.7–10 Constraints surrounding organ sharing and procure-
ment distances are often a direct consequence of ischemic time
limitations, leading to an underutilization in the current pool of
available donor organs. Recent analysis of the Organ Procure-
ment and Transplantation Network (OPTN) database revealed
significant regional discrepancies in donor heart acceptance
rates, which further contributes to non-recovery of suitable
organs.11 In addition to improving organ donation recruitment,
optimization of the very process by which the organs are
procured has been a major focus. Innovations in donor heart
preservation that permit longer travel times without compromis-
ing graft quality could reduce the strain on the present allocation
system by easing this severe organ donor shortage.
The Organ Care System (TransMedics, Andover, MA)
was developed as a mobile perfusion module that maintains
260 The Journal of Heart and Lung Transplantation, Vol 36, No 3, March 2017
Table 1 Recipients’ Demographic Characteristics Stratified by Ex-vivo Organ Preservation Treatment
Recipient characteristics Organ Care System (n ¼ 19)
Age (mean ⫾ SD) 51.9 ⫾ 11.8
BMI (mean ⫾ SD) 26.2 ⫾ 5.9
Donor/recipient BMI ratio 1.2 ⫾ 0.3
Female 26.3% (5 of 19)
Female donor/male recipient 5.3% (1 of 19)
Primary reason for transplant CAD 26.3% (5 of 19)
Insertion of VAD 31.6% (6 of 19)
History of diabetes 21.1% (4 of 19)
History of hypertension 52.6% (10 of 19)
Pre-transplant sensitization 21.1% (4 of 19)
Previous blood transfusions 47.4% (9 of 19)
BMI, body mass index; CAD, coronary artery disease; VAD, ventricular assist device.
the donor heart in a functional, physiologic state with warm,
oxygenated, nutrient-enriched donor blood (Figure 1). In
addition to the potential benefits of physiologic preserva-
tion, the Organ Care System provides valuable data
allowing for real-time assessment of the allograft, including
coronary flow rate and oxygen saturation, hematocrit and
lactate levels.12 Furthermore, because of the resuscitative
capabilities of this platform, it may offer significant
advantages in cases of high-risk extended-criteria donor
hearts.13 The PROCEED II trial, a prospective, multi-
institutional, randomized study, described non-inferior
short-term outcomes of donor hearts perfused with the
Organ Care System when compared with those preserved
with standard of care cold storage.14 Although the short-
term results of ex-vivo perfusion of donor hearts are
promising, longer term outcomes have not been described.
In this study, we report intermediate heart transplantation
outcomes, including rejection, antibody development and
patient survival at 2 years, for grafts preserved using the
Organ Care System or standard cold preservation.
Methods
This investigation was a prospective, randomized study that was
part of the multinational PROCEED II trial. Eligible adult patients
(Z18 years old) were active candidates on the heart transplant
waiting list. The exact protocol can be found in the PROCEED II
study, but, briefly, eligible participants meeting the study’s
inclusion criteria were randomly assigned in a 1:1 manner to
receive donor hearts preserved with either standard cold storage or
the Organ Care System.14 Donor criteria included age o60 years, mean
arterial pressure 460 mm Hg and a satisfactory echocardiogram.14
After donor heart arrest, the allograft was immediately cannulated and
connected to the Organ Care System mobile perfusion module. The
donor heart was then reanimated to sinus rhythm and transported to its
destination using this platform.
Between 2011 and 2013, 38 heart transplant patients from a single
tertiary-care medical center enrolled within the PROCEED II trial were
randomized to either standard cold storage or the Organ Care System.
The primary outcome was 2-year patient survival. Secondary outcomes
evaluated included freedom from cardiac allograft vasculopathy,
incidence of non-fatal major cardiac events (myocardial infarction,
heart failure, angioplasty, pacemaker/implantable cardioverter-
defibrillator, stroke), freedom from any-treated rejection, biopsy-proven
cellular rejection (Grade 42R) and biopsy-proven antibody-mediated
Cold storage (n ¼ 19) p-value
59.9 ⫾ 11.8 0.04
23.1 ⫾ 4.2 0.08
1.0 ⫾ 0.3 0.06
36.8% (7 of 19) 0.73
15.8% (3 of 19) 0.60
42.1% (8 of 19) 0.50
21.1% (4 of 19) 0.71
31.6% (6 of 19) 0.71
57.9% (11 of 19) 1.00
36.8% (7 of 19) 0.48
47.4% (9 of 19) 1.00
rejection (Grades 1, 2 or 3). Furthermore, patients were assessed for total
ischemia time and cold ischemia time.
Continuous variables were defined as mean ⫾ standard
deviation and categorical variables as a percentage. p o 0.05
was considered statistically significant. Kaplan–Meier survival
curves were used to estimate patient survival and were compared
using the log-rank test. The institutional review board approved the
study protocol and compliance was monitored by an independent
data safety and monitoring board. The study was performed in
strict compliance with the ethical standards set forth by the World
Medical Association, as stated in the Declaration of Helsinki, as
well as the International Society for Heart and Lung Trans-
plantation’s Statement on Transplant Ethics. Informed consent was
obtained from all study participants.
All statistical analyses were performed using SAS software,
version 9.2 (SAS Institute, Cary, NC).
Results
During the 2-year study period, 38 patients were randomly
assigned to the Organ Care System group (n ¼ 19) or the
standard-of-care static cold storage group (n ¼ 19). Recipient
demographic characteristics are presented in Table 1. Recipients
were age 51.9 ⫾ 11.8 (mean ⫾ SD) years in the Organ Care
System group and 59.9 ⫾ 11.8 years in the cold storage group
(p ¼ 0.04). There were no significant differences in other
baseline characteristics such as body mass index (BMI) or
gender. There was a trend toward a higher incidence of diabetes
and hypertension in the cold storage group. However, this
difference did not reach statistical significance. The percentages
of previous blood transfusions were equal in the 2 populations,
whereas there was a non-significantly higher percentage of pre-
transplant sensitizations in the cold storage group (36.8% vs
21.1%; p ¼ 0.48). Donor characteristics, summarized in
Table 2, were similar in both groups. As shown in Table 3,
the total ischemia time in allografts using the Organ Care
System was significantly longer compared with the cold storage
group (361 ⫾ 96 minutes vs 207 ⫾ 50 minutes; p o 0.001).
Longer total ischemic times were expected in the Organ Care
System group, as additional time is required to mount the graft
onto the platform and perform system diagnostics. Cold
ischemia time, which represents the time without ex-vivo
perfusion, was shorter in the Organ Care System group (134 ⫾
45 minutes vs 207 ⫾ 50 minutes; p o 0.001).
Chan et al. Ex-vivo Heart Transplant Perfusion 261

Table 2 Donors’ Demographic Characteristics Stratified by Ex-vivo Organ Preservation Treatment

Donor characteristics Organ Care System (n ¼ 19) Cold storage (n ¼ 19) p-value
Age (mean ⫾ SD) 30.9 ⫾ 13.1 31.8 ⫾ 13.5 0.42
BMI (mean ⫾ SD) 27.0 ⫾ 3.7 25.8 ⫾ 4.9 0.19
Female (%) 21.1% (4 of 19) 31.6% (6 of 19) 0.71
Race
White 31.6% (6 of 19) 42.1% (8 of 19) 0.74
Hispanic 21.1% (4 of 19) 47.4% (9 of 19) 0.17
African-American 26.3% (5 of 19) 10.5% (2 of 19) 0.40
Other 21.1% (4 of 19) 0% (0 of 19) 0.11
Cause of death
Head trauma 63.2% (12 of 19) 57.9% (11 of 19) 1.00
Anoxia 26.3% (5 of 19) 21.1% (4 of 19) 1.00
Cerebrovascular accident/stroke 10.5% (2 of 19) 21.1% (4 of 19) 0.66
History of diabetes 5.3% (1 of 19) 5.3% (1 of 19) 1.00
History of hypertension 5.3% (1 of 19) 10.5% (2 of 19) 1.00
Vasoactive medication requirements 5.3% (1 of 19) 21.1% (4 of 19) 0.34
Dopamine 0% (0 of 19) 10.5% (2 of 19) 0.49
Vasopressin 5.3% (1 of 19) 5.3% (1 of 19) 1.00
Nitroprusside 0% (0 of 19) 5.3% (1 of 19) 1.00
BMI, body mass index.

When analyzing the primary end-point (Figure 2), there
was no statistically significant difference in 2-year patient
survival rate between groups (Organ Care System: 72.2%;
cold storage: 81.6%; p ¼ 0.38). Similarly, there was no
difference in freedom from non-fatal major cardiac events or
cardiac allograft vasculopathy (Table 4). Secondary out-
comes focusing on allograft rejection rates also demon-
strated comparable results (Table 5). In the Organ Care
System group, 53.0% of patients remained free from any
treated rejection, in contrast to 61.8% in the cold storage
group (p ¼ 0.48). Likewise, no significant difference was
demonstrated in rates of freedom from acute cellular
rejection or biopsy-negative rejection. One patient in the
Organ Care System group developed antibody-mediated
rejection within 2 years post-transplant.
Discussion
For over half a century, donor heart preservation techniques
for transportation have remained largely unchanged.15
Although the use of static cold storage represents an
inexpensive and easily replicable solution, it remains
imperfect as low-level anaerobic metabolism continues
and is unable to prevent ongoing myocardial injury.16–19
Furthermore, this method of preservation is limited by the
total ischemia time; the risk of early graft failure is doubled
with increases in ischemia time from 3 to 6 hours.3 As a
result, research into alternative preservation techniques,
including extracorporeal heart perfusion systems, has
increased.17,20,21 An ex-vivo organ perfusion platform
represents a significant advancement in the field of trans-
plantation, as it allows for near-physiologic preservation in
addition to addressing concerns regarding the large gap
between organ demand and availability. The initial concept
of an ex-vivo perfusion apparatus dates back to work
performed by Wicomb and Barnard in 1981,22 and has been
demonstrated in various iterations in both pre-clinical23–26
and clinical27–29 settings. Findings of decreased oxidative
and myocardial injury markers, improved microvascular
function and superior myocardial ultrastructure highlight the
advantages of continuous normothermic perfusion.24,30–32
Currently as the only commercially available mobile
cardiac perfusion device, the Organ Care System aims to
reduce cold ischemia time, minimize myocardial dysfunc-
tion, and diminish constraints of procurement distances,
thereby optimizing donor utilizations and geographic
usage variabilities. Its initial evaluation in the PROCEED
II trial assessed clinical outcomes of the Organ Care
System compared with standard cold storage, and
demonstrated 30-day mortality rates comparable to those
of standard cold storage therapy.14 However, until now,
longer term outcomes on the use of the Organ Care System
perfusion platform in heart transplantation have not been
assessed.

Table 3 Comparison of Mean Total Ischemia Time and Cold Ischemia Time in Organ Care System and Cold Storage Cohorts

Organ Care System (n ¼ 19) Cold storage (n ¼ 19) p-value

Total ischemia time (min) 361 ⫾ 96 207 ⫾ 50 o0.001
Cold ischemia time (min) 134 ⫾ 45 207 ⫾ 50 o0.001
Cold ischemia period refers to time before placement within the Organ Care System circuit (while harvesting allograft) and after separation from the
Organ Care System (during implantation of allograft into recipient).
262 The Journal of Heart and Lung Transplantation, Vol 36, No 3, March 2017
Figure 2 Kaplan–Meier curve comparing patient survival at
2 years between those receiving donor hearts maintained on the
Organ Care System (OCS) versus preservation with standard cold
storage (CS). Tick marks denote censoring.
In this report we have described the intermediate
outcomes of heart transplantation with the Organ Care
System. As expected, the Organ Care System group was
demonstrated to have a significantly longer total ischemia
time but shorter cold ischemia time compared with the static
cold storage group. This was primarily attributed to the time
(approximately 30 minutes) required to mount the allograft
onto the Organ Care System. Furthermore, additional time
was required at the donor hospital to ensure that the donor
organ’s metabolic parameters, such as arterial and venous
lactate levels, were within an acceptable range before
departure. At 2 years, no significant differences were
demonstrated between groups in freedom from cardiac
allograft vasculopathy or development of non-fatal major
cardiac events. A clinically relevant trend toward higher
freedom from cardiac allograft vasculopathy was observed
in those treated with the Organ Care System, which may be
explained by the shorter cold ischemic time in this group.
Rates of any treated rejection, biopsy-proven cellular
rejection, biopsy-proven antibody-mediated rejection and
biopsy-negative rejection were not statistically different.
Although a statistically significant difference was not
detected with regard to survival at 2 years in patients with
graft transportation with the Organ Care System compared
with standard cold storage during organ procurement, a
Table 4 Patient Survival and Freedom From Adverse Events at 2 Years After Heart Transplantation Using the Organ Care System or Cold
Storage Preservation of the Donor Allograft
Organ Care System (n ¼ 19)
Survival 72.2%
Freedom from NF-MACE 90.9%
Freedom from CAV 100.0%
CAV, cardiac allograft vasculopathy; NF-MACE, non-fatal major cardiac events.
trend toward decreased survival was observed in the
experimental group. We found that all deaths in patients
receiving ex-vivo–perfused grafts occurred within 1 year of
transplant. Of note, these recipients were identified as
having pre-existing features of post-transplant complications
(e.g., older age, chronic kidney disease, ECMO use, Status
1A listing of the United Network for Organ Sharing) and
may have been at high risk for sub-optimal outcomes,
regardless of donor heart preservation technique.
Several limitations of this study are recognized. We
acknowledge the shortcomings inherent in a retrospective
review, including potential imperfections with data report-
ing and collection. In addition, this study was a single-
institution experience and therefore the results may be
influenced by center-specific protocols, techniques and
geographic variables. We appreciate that not all preoperative
risk factors were completely equivalent between groups;
patients were notably older in the cold storage group. This
likely reflects the fundamental shortcomings of a small
sample size. Moreover, we have presented a retrospective
evaluation of a single-center experience in the context of a
multi-institution trial and therefore recognize the limitations
of low power (with a calculated power of 4.7% to detect a
survival difference in the present cohort). Thus, these results
must be interpreted cautiously and it will be critically
important to validate our findings in a larger population,
such as analyses of outcomes at all centers participating in
the PROCEED II trial. The patients evaluated in this study
were enrolled in the PROCEED II trial and therefore had
specific exclusion criteria, including 44 previous sternot-
omies, mechanical ventilator dependence and use of
ventricular assist devices for 430 days.14 These exclusions
may limit applicability of our study’s results to those
specific populations. Expanded-criteria donor hearts or
organs after circulatory arrest were not evaluated, although
further studies (i.e., the EXPAND Heart Trial, Clinical-
Trials.gov identifier: NCT02323321) will focus on the
Organ Care System’s ability to reanimate and resuscitate the
allograft.
In conclusion, implementation of the Organ Care System
during donor procurement and transportation in a single-
institutional setting was not found to be associated with
significant differences in intermediate outcomes among cardiac
transplantation recipients at 2 years. The results of this study
suggest that the Organ Care System may be a valid adjunct to
allograft preservation, which encourages further development of
this platform. Confirmation of these findings is necessary and
may be achieved through additional long-term analyses of multi-
center results from the PROCEED II trial.
Cold storage (n ¼ 19) p-value
81.6% 0.38
94.7% 0.90
78.5% 0.09
Chan et al. Ex-vivo Heart Transplant Perfusion
Table 5 Freedom From Rejection at 2 Years After Heart Transplantation Using the Organ Care System or Cold Storage Preservation of the
Donor Allograft
Organ Care System (n ¼ 19)
Freedom from ATR 53.0%
Freedom from ACR 72.5%
Freedom from AMR 94.7%
Freedom from BNR 79.2%
ACR, acute cellular rejection; AMR, antibody-mediated rejection; ATR, any-treated rejection; BNR, biopsy-negative rejection.
Disclosure statement
J.A.K. serves on the steering committee for the OCS PROCEED
trial and the EXPAND trial, is a co–primary investigator for these
studies, and receives study grants from TransMedics. The
remaining authors have no conflicts of interest to disclose.
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