Transplant International ISSN 0934-0874

REVIEW

DCD lung donation: donor criteria, procedural criteria,

pulmonary graft function validation, and preservation
Michiel E. Erasmus,1 Dirk van Raemdonck,2 Mohammed Zeeshan Akhtar,3 Arne Neyrinck,2
David Gomez de Antonio,4 Andreas Varela4 and John Dark5
1 Department of Cardiothoracic Surgery, University Medical Center Groningen, University of Groningen, Groningen, The Netherlands
2 Department of Thoracic Surgery, University Hospitals Leuven, Leuven, Belgium
3 Nuffield Department of Surgical Sciences, Oxford Transplant Centre, University of Oxford, Oxford, UK
4 Thoracic Department, Hospital Universitario Puerta de Hierro Majadahonda, Madrid, Spain
5 Institute of Cellular Medicine, Newcastle University, Newcastle upon Tyne, UK

Keywords Summary
donation after cardiac death, donation after
circulatory death, guidelines, lung, nonheart In an era where there is a shortage of lungs for transplantation is increased utiliza-
beating donation, review. tion of lungs from donation after circulatory death (DCD) donors. We review the
reports of 11 controlled and 1 uncontrolled DCD programs focusing on donor
Correspondence criteria, procedural criteria, graft assessment, and preservation techniques includ-
Michiel E. Erasmus, Department of Thoracic ing the use of ex vivo lung perfusion. We have formulated conclusions and recom-
Surgery, University Medical Center Groningen,
mendations for each of these areas, which were presented at the 6th International
Groningen, The Netherlands.
Tel.: +31503613619;
Conference on Organ Donation. A table of recommendations, the grade of rec-
Fax: +31503611347; ommendations, and references are provided.
e-mail: [email protected]

Conflicts of interest
The authors have declared no conflicts of
interest.

Received: 13 May 2015

Revision requested: 2 August 2015
Accepted: 21 December 2015

doi:10.1111/tri.12738

a so-called uncontrolled DCD donor [3]. In this case, the

Introduction/background
successful pretransplant, ex vivo evaluation of graft function
The first lung transplantation was performed with an organ with a machine, now called ex vivo lung perfusion (EVLP),
recovered from a donation after circulatory death (DCD) was a crucial step. EVLP allowed both subjective assessment
donor [1]. Renewed interest in DCD lung transplantation of donor lung function and prolongation of the ischemic
was raised in the 1995 following the publication by time (in this case to 17 h) simplifying the logistics of trans-
D’Alessandro and co-workers in which they reported the first plantation in this unpredictable setting. The basic principle
successful DCD donor lung transplantations as part of an of EVLP is the use of a preservation fluid with a high oncotic
institutional DCD program [2]. They used DCD donors after pressure, pure or mixed with red blood cells (RBC), which is
withdrawal of life support on an ICU, nowadays referred to perfused by a pump in a pressure-controlled manner into
as controlled DCD (Maastricht DCD category III). the pulmonary artery and recollected in a reservoir. The per-
Further interest for DCD lung donation was triggered by fusion fluid is gradually warmed to 37°C. Gentle ventilation
Steen and co-workers in 2001 who successfully transplanted of the lungs is resumed for testing at 37°C after the perfusate
a single lung from a donor after failed cardiac resuscitation, is deoxygenated with a N2/CO2 gas mixture via a membrane

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DCD lung donation Erasmus et al.

gas exchanger inserted in the circuit before it enters the bronchoscopic examination is carried out after death. It is
pulmonary artery. The feasibility to establish a successful important to realize is that the criteria are applied in the
uncontrolled DCD lung transplant program was shown by situation of a potential donor as the DCD procedure itself
the Madrid group headed by A. Varela [4]. might affect the value of the criteria. Therefore, although
Today, 11 centers [5–23] have published results after arbitrary, specific procedural DCD criteria may play a role
lung transplantation in a controlled DCD program. Only such as heparin pretreatment, the allowed length of the
the pioneering Madrid group have reported experience in agonal phase, withdrawal of the tracheal tube, maximum
an uncontrolled DCD program [4,24–28]. Recently, a length of initial warm ischemic period, timing of re-infla-
working group within the International Society for Heart tion, and the use of EVLP. Of note using only the period of
and Lung Transplantation has taken an initiative to collect warm ischemia is based on experimental data alone [30],
multicenter data to gain insight into selection, procedures, other factors are mainly based on clinical practice. Recently,
and outcome after DCD lung donation). Over 300 DCD some centers advocate standard ex vivo evaluation of graft
lung transplants were included in the Registry, but it is function with EVLP for all controlled DCD lungs [23].
likely that the total is in excess of 450 worldwide [29].
This article is based on the reports of 11 controlled DCD
Premortem ‘management’ in the donor
programs and the 1 uncontrolled DCD program. We focus
on donor criteria, procedural criteria, graft assessment, and There are widely varying ethical frameworks for interven-
preservation techniques. For outcome after DCD lung trans- tions in the premortem management of patients. These
plantation, these four steps are closely interlinked. There- need to reconcile appropriate treatment of the patient who
fore, we formulated conclusions and recommendations for is not a donor until death occurs, with good outcomes after
each topic. These were discussed at the 6th International transplantation, the presumed wish of the patient, and the
Conference on Organ Donation in Paris in 2014. This article reason for considering donation. Steps that are consistent
represents a summary of the conclusions from this initiative. with both aims are the most acceptable. These should cer-
tainly include a mode of ventilation which reduces lung
injury (i.e., a tidal volume of 6–8 ml/Kg ideal body weight,
Donor and procedural criteria
with PEEP of 8 cm H2O, frequent suctioning and appro-
For controlled DCD lung donation, most centers use the priate recruitment maneuvers). Ideally, they should also
same donor criteria as for DBD donation. In addition, include a premortem bronchoscopy, to assess the mucosa
specific procedural criteria play an important role in deter- when perfused and the placement of a naso-gastric tube.
mining whether to accept the controlled DCD lung or not.
Clinical criteria for uncontrolled DCD lung donation are
Heparin pretreatment
scarce and based on a few patients.
Several centers reported good outcome without heparin
pretreatment. This is often based on ethical consideration
Controlled DCD lung donation
[16,20,22]. Importantly, these centers all use retrograde
The generally agreed DBD donor criteria for suitability for flushing during preservation. In assessing this heparin-free
transplantation form the background of the controlled scenario, no emboli or thrombi could be detected in DCD
DCD donor criteria (Table 1). In addition, most groups lungs that were harvested to search for thrombo-embolic
also use lungs from ‘extended’ criteria donors defined as lesions by pathologic and histopathologic investigation
age > 65, smoking > 20 pack years, ICU period > 5 days, [31]. Other centers do use heparin pretreatment of the
and abnormal chest X-ray. A PO2/FiO2 < 40 kPa is gener- potential DCD donor [5,7,10,11]. Experimentally, pretreat-
ally not accepted for DCD. Functional criteria may be ment with heparin of DCD donor lungs was shown to be
relaxed if EVLP is to be used to recondition and evaluate beneficial in a way that it prevented worsening of lung
the lungs. Significant aspiration remains a contraindication function during EVLP [32]. No clinical study is available
but may be difficult to recognize, particularly if the first comparing both strategies. With current data and criteria
available, no conclusion can be drawn. Theoretically, hep-
Table 1. DCD donor criteria. arin pretreatment seems to be beneficial.
Age <65 years
Smoking <20 pack years
Chest X-ray Clear The agonal phase
Mechanical ventilation <5 days
The maximal length of the agonal phase (withdrawal of life
Blood transfusion <5 units RBC
support until circulatory arrest) is arbitrarily set at 2 h.
Oxygenation PO2 > 40 kPa
There is no information to determine the maximal save

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Erasmus et al. DCD lung donation

length of the agonal phase for lungs based on clinical ECMO-like circuit. Clamping of the descending aorta to
research. Multiple definitions of agonal phase are described prevent any possibility of restarting brain perfusion is an
in the literature. The most often used definition for the absolute requirement. The abdominal team will cannulate
agonal phase in papers concerning lung transplantation is the abdominal aorta and IVC, and the cardiothoracic team
the period between withdrawal of life support and the dec- will then clamp the lower thoracic aorta and then immedi-
laration of death. Definitions and criteria to declare a ately proceed to flush the lungs in vivo. Limited topical
donor death might, however, differ between countries and cooling should be used. The intrapericardial IVC should be
centers (e.g., absent peripheral pulsation, flat ECG). For clamped at an early stage to reduce the chance of entraining
lungs, re-inflation might be an important extra step in the air into the perfusion circuit. While abdominal perfusion
agonal phase, most often before flush perfusion. It is well continues, the thoracic team removes the lungs, for retro-
known that inflation is an effective preservation method to grade perfusion on the back table. Ensuring complete
maintain lung cell viability. In practice, the duration of the hemostasis in the chest, given the donor is systemically hep-
agonal phase is greatly based on logistics of the procedure. arinized, is important [35].
A waiting time of more than 2 h is generally too significant
of a workforce burden. As shown in kidney DCD donation,
Ex vivo lung perfusion
the save agonal phase might be influenced by injury caused
by hypotension after withdrawal of life support [33]. The Recently, the Toronto group advocated the use of EVLP for
Leuven group in an experimental model of porcine EVLP all controlled DCD donors [23]. Nine DCD lung transplan-
demonstrated that pulmonary function is worse in lungs tations were performed. There is, however, no detailed
coming from donors dying from hypoxic cardiac arrest information about the specific behavior or injury of the 9
(mimicking clinical situation in controlled donation after controlled DCD lungs during EVLP evaluation. The grow-
ventilator switch off) compared to exsanguination and ing evidence that EVLP improves suboptimal lungs sup-
acute ventricular fibrillation (mimicking clinical situation ports the use of EVLP after controlled DCD donation,
in uncontrolled donation) [34]. Only one clinical study especially when the outer ranges of accepted criteria are
[22] showed a slightly worsening oxygenation capacity of applied.
transplanted controlled DCD lungs when the period from
the start of hypotension (RR < 6.6 KPa [50 mm Hg]) till
Uncontrolled DCD lung donation
circulatory arrest became longer during the agonal phase.
The Madrid group is currently the only group who has
reported clinical experience with uncontrolled DCD lung
Withdrawal of tracheal tube
transplantations [27]. Using the procedural criteria of
Good results are reported with or without withdrawal of acceptable cold in vivo blood gas measurement and accept-
the tube. There is no clear consensus whether withdrawal able visual inspection, they reported on 29 transplantations
of the tracheal tube is harmful or beneficial for the process. with uncontrolled DCD lungs. This led to a similar 1-year
It might protect the airways for aspiration, but it also might survival but to a higher percentage of primary graft dys-
prolong the agonal phase by preventing a collapse of the function as compared to results in their DBD program. The
upper airway with asphyxia of the donor. group is now investigating the use of EVLP on the OCS
LungTM device as a tool to assess and to condition the pul-
monary graft prior to transplantation [36]. Stig Steen
Maximum length of initial warm ischemic period
(Lund, Sweden) was the first author to report in 2001 in a
The initial warm ischemic period, defined as the period detailed way on a successful transplantation of lungs from
after circulatory arrest and start of flush perfusion preserva- an uncontrolled DCD after EVLP [3].
tion, reported in clinical series is approximately 30 min.
Nevertheless, success is reported in cases with a period up
Uncontrolled DCD lung donor criteria (as used by the
to 93 min [15]. Most centers have protocols with a maxi-
Madrid group) reference
mum tolerable length of initial warm ischemic period of
1 h based on experimental data [30]. 1. Witnessed cardiac arrest.
2. Basic and advanced resuscitation maneuvers within
15 min.
Lung preservation in case of normothermic regional
3. Continuing resuscitation during transportation.
perfusion (NRP) of the abdominal organs
4. Decision on failed resuscitation and declaration of
A number of liver teams have introduced perfusion of the death by ICU personnel.
abdominal organs with oxygenated blood, using an 5. Legal permission to proceed with donation.

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DCD lung donation Erasmus et al.

6. Adequate blood gas measurement with in vivo single be within 1 h as stated earlier [29]. Because of the uncertain
flush technique (53.3 KPa [400 mm Hg] or above cor- effect of this period, some groups advocate the use of EVLP
rected for temperature) and acceptable at visual lung in the setting of controlled DCD lung donation. EVLP
inspection (collapse test, correct flushing, no thrombi enables pulmonary graft validation after the potentially
on retrograde perfusion, etc.). inflicted injury and, importantly, before implantation.
7. Chest X-ray on ICU.
8. Age 7–70 years. Lung function validation in the donor
9. No specific contraindications other than for DBD lung Most groups in Europe and the USA successfully use the
donation. lung validation technique in the donor for DCD as used for
DBD donation after BD [5–22]. The lung function valida-
tion is based on measurement of the PO2 at a FiO2 of 100%
Uncontrolled DCD lung procedural criteria
oxygen with a standardized PEEP of 5 cm H2O during
1. A total warm ischemia time (cardiac arrest + resuscita- mechanical ventilation. Generally, a cutoff point of
tion + 5 min hands-off, ventilatory, and circulatory >40 kPa (300 mm Hg) is used to accept the lungs. Impor-
support until start of topical cooling) of maximal tant prerequisites that are reported in combination with
120 min. This arbitrary period of warm ischemia was this method are as follows:
adopted by the Madrid group as the adequacy of lung
1. An agonal phase not exceeding 2 h (period between
perfusion during resuscitation is unknown. The ‘true
stop treatment and circulatory arrest).
warm ischemia time’ starting at end of resuscitation
2. A warm ischemia time (WIT) (time between circula-
was not defined but is probably of importance.
tory arrest and start flush perfusion preservation) of
2. In vivo topical cooling period of up to 240 min. The
30 min or shorter.
cooling fluid returning from the pleura should reach a
temperature below the 21°C (personal communica- As part of graft evaluation, inspection of the pulmonary
tion). To control the cooling of the lungs is of specific artery for possible clots and of deflation of the lungs during
importance when normothermic iRP of the abdominal a collapse test is recommended. Based on these methods,
organs is performed as described above. the immediate pulmonary graft function of DCD lungs is
Using above criteria, 40% of lungs are rejected after cold comparable to DBD lungs [15–18,21,22]. As scaled with the
in vivo blood gas measurement and visual lung inspection. primary graft dysfunction (PGD) score proposed by the
Steen et al. mentioned in their case report an age below ISHLT, PGD grades after controlled DCD donation are
70 years and an initial warm ischemic period of 1 h as found to be similar to those after DBD donation and trans-
acceptable for transplantation after uncontrolled DCD plantation [16,17,22].
donation. EVLP was used for lung validation and preserva-
tion. No specific EVLP criteria to decide on uncontrolled Lung preservation
DCD lung function are yet available. Measures to improve preservation might already start
before withdrawal of life support. Some centers administer
heparin iv to the donor. As described above in the procedu-
Pulmonary graft assessment and preservation
ral criteria, till now no differences in outcome are seen
techniques
between series with or without heparin. Topical cooling
Controlled DCD lung donation might be used in controlled DCD, but is not often
Traditionally in heart beating brain-dead donors (DBD), described. The most used method of preservation is flush
lung function is validated before the donation procedure. perfusion although no clinical studies are available on the
This is made by interpretation of the partial oxygen pressure best flush solution and on the best flush route (antegrade
(PaO2) in relation to the percentage-inhaled oxygen (FiO2) versus retrograde) for DCD lungs. The Leuven group has
in a peripheral arterial blood sample and ventilation pres- demonstrated in a porcine model evaluating DCD pul-
sure settings (PEEP 5 cm H2O). The same validation tech- monary function during EVLP that in vivo topical cooling
nique is being used for controlled DCD lung donation was effective up to 7 h after circulatory arrest including 90-
although potentially, the cessation of ventilation and circu- min warm ischemia [37]. In another study from the same
lation and the subsequent unavoidable period of warm group using the same model, it was demonstrated that ret-
ischemia may decrease the quality of the DCD lung. To pre- rograde flush of DCD lungs was superior compared to
serve the lung in the period between circulatory arrest and antegrade flush after both warm ischemia [38] and after
cold flush preservation with the lung untouched in the tho- topical cooling [39]. The current clinical practice is ante-
rax of the donor, topical cooling might be used [3]. To be grade and retrograde flush with Perfadex, Celsior, or UW
successful, the preceding period of warm ischemia should as mostly used flush solutions. The antegrade flush is

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Erasmus et al. DCD lung donation

performed during slow ventilation or inflation. The retro- donor that is circulated with some extra chest compres-
grade flush is performed on a back table by cannulating sions. After topical lung cooling and subsequent ster-
four lung veins separately. Lungs are stored inflated on ice. notomy and antegrade flush perfusion preservation of the
lungs, 300 ml of 4–10°C donor blood is flushed via the
Ex vivo lung perfusion pulmonary artery while the lungs are ventilated with
The Toronto group was the first to use EVLP in a standard 100% oxygen. The blood is collected from the lung veins
fashion for controlled DCD lungs. Their series compromise till and the PO2 is measured and corrected for the tempera-
now 22 controlled DCD lungs that were perfused and venti- ture used during flushing. Cutoff point for PO2 is
lated for 4–6 h and transplanted successfully [23]. Four DCD <53.3 KPa (400 mm Hg). Acceptance of the lung was fur-
lungs did not meet the acceptance criteria and were rejected ther based on visual appearance (collapse test, correct
after EVLP. Ten of the 22 successfully transplanted DCD lungs flushing, no thrombi on retrograde perfusion. . .). Results
would normally have been rejected due to low oxygenation are described of 29 to 32 uncontrolled DCD lung trans-
capacity while ventilated in the donor but were judge suitable plantations. Due to higher incidence of PGD and early
after EVLP. A recent experimental study from the same group mortality compared to DBD donation with this in vivo
looking at pulmonary function in a porcine model after 10 h single flush technique, the Madrid group now recom-
brain death and 24 h cold ischemia demonstrated that an mends that some form of ex vivo validation of pulmonary
ex vivo measured low PO2 during EVLP may not be the first graft function should be adopted in uncontrolled DCD
indicator of lung injury and, taken alone, may be misleading lung donation.
in assessing the ex vivo lung. Thus, evaluation of other physio-
logic parameters like compliance and pulmonary vascular Ex vivo lung perfusion
resistance during EVLP takes on greater importance [40]. There are only two clinical reports on EVLP in the situation
of uncontrolled DCD donation [3,32]. In the first case
report by the group of Stig Steen EVLP showed excellent
Uncontrolled DCD lung donation
performance of the uncontrolled DCD lung. The subse-
In uncontrolled DCD lung donation, a method to validate quent single lung transplantation procedure was successful.
lung function after donation is a necessity as lung function The basic principle of EVLP is the use of a preservation
is unknown before donation. EVLP is thought to be a good fluid with a high oncotic pressure mixed with RBC’s that is
method to evaluate lungs from uncontrolled DCD donors. perfused by a pump in a pressure-controlled way into the
However, the largest experience with lung validation in pulmonary artery and recollected in a reservoir. The perfu-
uncontrolled DCD is with an in vivo single flush technique sion fluid is gradually warmed to 37°C. Gentle ventilation
as described by the Madrid group. the lungs is resumed for testing at 37°C after the perfusate
is deoxygenated with a N2/CO2 gas mixture via a mem-
Lung preservation brane gas exchanger inserted in the circuit before it enters
After failed resuscitation and certification of death, lungs the pulmonary artery. Recently, the Madrid group reported
will suffer an obligatory period of warm ischemia. As their experience with EVLP for validation of uncontrolled
described by the Madrid group, this expands up to 2 h DCD lungs during the 2011 annual meeting of the ISHLT
[26]. After this period, chest tubes are inserted for topical in San Diego (32 = 34 n). Besides PaO2, lung compliance
lung cooling [3,26] and the patient can be connected to a and ventilatory pressures might be important parameters
veno-arterial ECMO system via catheters inserted in the to evaluate graft quality similar to EVLP after controlled
groin for preservation of abdominal organs. The subse- DCD donation [36].
quent generally used flush perfusion is already described in
the Controlled DCD section. The retrograde flush might be
Conclusions and recommendations
of great importance in programs not using heparin before
withdrawal of life support. The method for lung preserva- Controlled DCD
tion differs for category IV DCD, where the heart stops pre- The current use of the same DBD donor criteria in con-
maturely during organ retrieval in a brain-dead patient and trolled DCD results in good lung transplant outcome. Pul-
prior to aortic cross-clamp and cardioplegia. In this infre- monary graft validation in the donor leads to good results.
quent, uncontrolled DCD category a cannula can be rapidly Combined antegrade and retrograde flush perfusion and
inserted in the pulmonary artery for cold flush perfusion. inflated storage do preserve the DCD lung as good as the
DBD lung. This is true regardless of the use of heparin or
In vivo single flush lung validation technique withdrawal of the tracheal tube but with a time between
The in vivo single flush technique is a very simple and withdrawal of treatment and circulatory arrest of <90 min
practical method. It is used after heparinization of the and an initial warm ischemic period of <60 min. EVLP was

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DCD lung donation Erasmus et al.

shown to be beneficial in extending donor criteria and in continued

using donor lungs with initially unacceptable PO2. Results
Recommendation Grade References
for DCD lung transplants have been shown in a large num-
ber of reports and summarized in a recent meta-analysis 1. Witnessed cardiac arrest. D
[41], to be essentially identical to those from DBD donors. 2. Basic and advanced resuscitation D
maneuvers within 15 min.
The single, and as yet unconfirmed dissenting report, sug-
3. Continued resuscitation during D
gests a slightly higher incidence of PGD and a higher risk of
transport of potential donor.
early bronchiolitis obliterans [42]. 4. Total warm ischemia period D
(cardiac arrest – start preservation)
should be <120 min.
Uncontrolled DCD
5. Effective in vivo topical cooling D
Uncontrolled lung donation has shown to be successful prior to flush preservation 20°C.
6. Transplant suitability of these lungs D
using general criteria and strict procedural criteria with the
should in general be tested ex vivo
help of in vivo pulmonary graft testing, visual inspection,
using EVLP before acceptance based
and chest X-ray investigation. However, outcome remains on measures of pulmonary
somewhat inferior as compared to DBD lung transplanta- compliance, vascular resistance, and
tion. The use of EVLP to validate and preserve the lung is gas exchange.
still under investigation. Combined topical cooling and
flush perfusion is currently the only described preservation
method.
Funding

Recommendation table DCD lung The authors have declared no funding.

Recommendation Grade References

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