Since 1990, the Thoracic Surgery Directors Association (TSDA) has presented an award annually to an outstanding article
presented by a resident at The Society of Thoracic Surgeons (STS) Annual Meeting. Established to encourage resident research in
cardiothoracic surgery, the award was renamed in 2009 to honor Benson R. Wilcox, MD, who was instrumental in establishing
TSDA and who served as the organization’s first secretary/treasurer and later as its president. Abstracts submitted to the STS
Program Committee representing research performed by residents were forwarded to the TSDA to be considered for this award.
The abstracts were reviewed and the winner selected by the TSDA Executive Committee.
In 2013, the recipient of the TSDA Benson R. Wilcox Award was Bryan A. Whitson, MD, PhD, a resident of the Division of
Cardiac Surgery at The Ohio State University Wexner Medical Center Department of Surgery.
Use of the Donor Lung After Asphyxiation or
Drowning: Effect on Lung Transplant Recipients
Bryan A. Whitson, MD, PhD, Marshall I. Hertz, MD, Rosemary F. Kelly, MD,
Robert S. D. Higgins, MD, MSHA, Ahmet Kilic, MD, Sara J. Shumway, MD, and
Jonathan D’Cunha, MD, PhD
Departments of Surgery and Medicine, The University of Minnesota, Minneapolis, Minnesota; Department of Surgery, Division of
Cardiac Surgery, The Ohio State University Wexner Medical Center, Columbus, Ohio; and Department of Cardiothoracic Surgery, The
University of Pittsburgh Medical Center, Pittsburgh, Pennsylvania
Background. With the relative paucity of acceptable
donors for lung transplantation, criteria for extended
donor consideration are being explored. We sought to
evaluate the suitability of donors whose cause of death
was asphyxiation or drowning (A/D) as a potential option
to enlarge the donor pool.
Methods. We queried the United Network for Organ
Sharing (UNOS) Standard Transplant Analysis and
Research registry for lung transplantation from 1987 to
2010 to assess associations between cause of death and
recipient survival using the Kaplan-Meier method. To
adjust for potential confounders, we used a Cox proportional hazards model and a logistic regression model to
evaluate incidence of rejection within the first year.
Results. There were 18,250 adult primary lung transplantations performed, with 309 A/D donors. There was
no difference in survival between groups (log-rank, p [
0.52). There were no differences in demographics, length
of stay, airway dehiscence, lung allocation score (LAS),
or ischemic time in univariate analysis (all p > 0.05). The
A/D lung recipients had fewer deaths from pulmonary
causes (5.8% versus 9.5%; p [ 0.02). Proportional hazards
analysis was significant for double lung transplantation
(hazard ratio [HR], 0.85; 95% confidence interval [CI], 0.8–
0.9), height difference (HR, 1.002; 95% CI, 1.00–1.003),
donor age greater than 50 years (HR, 0.89; 95% CI, 0.83–
0.96), and recipient age greater than 55 years (HR, 0.8; 95%
CI, 0.76–0.84). A/D cause of death did not impact survival
in multivariate analysis.
Conclusions. A/D as a donor cause of death was not
associated with poor long-term survival or incidence of
rejection in the first year after transplantation. Donor
cause of death by A/D, when carefully evaluated and
selected, should not automatically exclude the organ from
transplant consideration. These results provide important
justification for potentially broadening the donor pool
safely.
F
offers the potential of being both a life-saving and lifeenhancing therapy. Although this therapy is critically
needed, there is a relatively inadequate supply of
acceptable quality organs suited for transplantation, with
only 17% of lungs offered for transplantation being able
to be successfully transplanted [1].
In the modern era, there are novel approaches to
enlarging the donor pool, such as extended criteria [2, 3],
donation after cardiac death (DCD) [4–9], and ex vivo
perfusion [5]. The lungs from donors who have either
been asphyxiated or drowned are not routinely used as
lung donors. We sought to evaluate the suitability of
or patients with end-stage lung disease, there are few
viable long-term options. For the appropriate candidate with end-stage lung disease, lung transplantation
Accepted for publication May 7, 2014.
Presented at the Poster Session of the Forty-ninth Annual Meeting of The
Society of Thoracic Surgeons, Los Angeles, CA, Jan 26–30, 2013. Winner of
the Thoracic Surgery Directors Association Benson R. Wilcox Award.
Address correspondence to Dr Whitson, Department of Surgery, Division
of Cardiac Surgery, The Ohio State University Wexner Medical Center, N825 Doan Hall, 410 W 10th Ave, Columbus, OH 43210; e-mail: bryan.
whitson@osumc.edu.
Ó 2014 by The Society of Thoracic Surgeons
Published by Elsevier
(Ann Thorac Surg 2014;98:1145–51)
Ó 2014 by The Society of Thoracic Surgeons
0003-4975/$36.00
http://dx.doi.org/10.1016/j.athoracsur.2014.05.065
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Table 1. Donor Mechanism of Death
Donor Mechanism of Death
Intracranial hemorrhage/stroke
Blunt trauma
Gunshot wound or stabbing
Other
Asphyxiation
Drowning
Frequency
%
6,637
4,919
4,179
2,206
280
29
36.4
27
22.9
12.1
1.5
0.2
donors whose cause of death was asphyxiation or
drowning (A/D) as a potential option to enlarge the
donor pool using national data.
Material and Methods
We used the United Network for Organ Sharing (UNOS)/
Organ Procurement and Transplantation Network
(OPTN) Standard Transplant Analysis and Research
(STAR) database. The STAR database is administrated
through UNOS/OPTN as overseen by the US Department
of Health and Human Services. The UNOS/OPTN STAR
database maintains data elements reflecting donor characteristics (eg, donor mechanism of death, donor age,
donor sex), pretransplantation recipient characteristics
(eg, indication for transplantation, recipient age, recipient
sex), and posttransplantation recipient characteristics and
outcomes (ie, length of stay, recipient survival, development of postoperative complications) [10]. The STAR
database contains data on solid organ transplantation
performed in the United States and contains data on
lung transplant recipients from 1987 to the present [11].
The data registry contains information from all 11 of the
United States subdivided OPTN regions.
This retrospective analysis of the UNOS/OPTN STAR
database was approved by the Institutional Review Board
at the University of Minnesota (1006E83853) and The
Ohio State University (2012H0306) with a waiver of need
for individual consent. We evaluated all adult (18 years of
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Table 2. Recipient Diagnosis as Indication for Lung
Transplantation
Diagnosis
Chronic obstructive pulmonary disease
Idiopathic pulmonary fibrosis
Cystic fibrosis
Other
Alpha-1 Antitrypsin Deficiency
Primary pulmonary hypertension
Sarcoidosis
Frequency
%
6,763
4,232
2,456
2,251
1,270
727
538
37.1
23.2
13.5
12.3
7
4
3
age and older) lung transplant recipients in the United
States whose transplantation procedures were performed
between 1987 and 2010. We limited our analysis to single
and bilateral lung transplant recipients from cadaveric
donors only. Those patients undergoing repeated transplantation had their second or further lung transplants
excluded, and their survival was censored at the time of
repeated transplantation, if performed.
The data were analyzed with SAS for Windows, version
9.3 (SAS Institute Inc, Cary, NC). For all statistical testing,
we used a 2-sided significance level of 0.05. For betweengroup comparisons, we used a 2-sample t test for
continuous variables and a c2 test for categorical variables. Unless otherwise stated, results are reported as
mean standard deviation. The Kaplan-Meier method
was used to compare unadjusted all-cause mortality
[12, 13]. To adjust our survival analysis for potentially
confounding patient factors, we used a Cox proportional
hazards regression model to adjust for covariates associated with survival and a logistic regression model for
covariates associated with treatment for rejection.
Results
Study Cohort
There were 19,115 lung transplant procedures performed
during the study period. Of those recipients, 18,250 met
Table 3. Univariate Analysis Associated With Donor Cause of Death
Donor Cause of Death
Variable
Lung allocation score
Single/double
Donor M/F
Recipient M/F
Treated for rejection in first year
Length of stay (d)
Airway dehiscence
Ischemic time (h)
Posttransplantation dialysis
Posttransplantation stroke
Donor smoking
Recipient age 55 y
Donor age 50 y
Asphyxiation/Drowning
Other
p Value
44 15.4
41.8%/58.2%
66%/34%
46%/54%
50.8%
27.3 35.9
1.5%
4.9 1.8
5.4%
0.7%
14.2%
50.8%
1.9%
43.6 14.8
49.5%/50.5%
63%/38%
53%/47%
47.4%
26.5 71
1.4%
4.7 1.7
5.2%
2.1%
22.6%
49.1%
13.7%
0.47
<0.001
0.15
0.01
0.45
<0.001
0.16
0.68
0.47
0.054
<0.001
0.55
<0.001
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Fig 1. (A) Distribution of the 309 asphyxia/
drowning donors as a percentage by year. (B)
Distribution of recipient lung allocation score
(LAS) by donor cause of death (p ¼ 0.47).
(ASP/DRO ¼ asphyxiation/drowning.)
the inclusion and exclusion criteria from 1987 to 2010.
Over the study period, the annual number of lung
transplantations performed in the United States
increased. Similarly, the annual number of A/D donors
increased over the study period, with the majority being
accepted for donation after 2005.
Donor Characteristics
Of the donor mechanisms of death (Table 1), the highest
proportion were caused by intracranial hemorrhage and
stroke (36.4%). As an aggregate, trauma (blunt and
penetrating) composed 49.9% of donor mechanism of
death. Donors who died of A/D composed 1.9%, or 309, of
the total donors. The overall donor age was 31.8 13.8
years. For those donors who died of A/D, the donor age
was 25.7 11.1 years. This donor age was significantly
younger than those donors who died of other causes,
whose age was 31.9 13.8 years (p < 0.001). There was no
difference in the proportion of male to female donors
(p ¼ 0.15) regarding donor causes of death (Table 3). The
donors who died of A/D were significantly less likely to
have had a smoking history.
Recipient Characteristics
Of the 18,250 recipients, the largest indication for lung
transplantation was chronic obstructive pulmonary
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Fig 2. (A) Recipient survival after transplantation by donor cause of death—all causes (p ¼ 0.40). (B) Recipient survival after
transplantation by donor cause of death—
asphyxiation and drowning versus all other
causes (p ¼ 0.52). (GSW ¼ gunshot wound;
ICH ¼ intracranial hemorrhage; STAB ¼
stabbing; STRO ¼ stroke.)
disease (37.1%) (Table 2). This was followed by idiopathic
pulmonary fibrosis (23.3%) and cystic fibrosis (13.5%).
The mean age of all recipients was 50.8 12.6 years.
For those recipients whose donors died of A/D, the age
was 50.8 12.9 years, and this was not different from
those recipients whose donors died of other causes at
50.8 12.6 years (p ¼ 0.98). Of the donor-recipient
matches, 56.7% were local allocations, 17.9% were
regional allocations, and 25.6% were national allocations.
The recipients’ blood types were as follows: 43.7% type O,
41.1% type A, 11.1% type B, and 4.1% type AB.
Those recipients whose donors died of A/D were more
likely to be women (54% compared with 47% men; p ¼
0.01). There was a significantly higher proportion of
bilateral lung transplantations performed in recipients
whose donors died of A/D. There was no difference in the
lung allocation score (LAS) in recipients whose donors
died of A/D and those who died of other causes (Table 3;
Fig 1) or in the ischemic time based on donor cause of
death.
Survival and Outcome
The overall recipient survival was not influenced by
donor cause of death (Fig 2A) when evaluated by
individual mechanism. This was similarly seen when
recipient overall survival was evaluated based on donor
cause of death in which A/D was compared with all
other causes (Fig 2B) (p ¼ 0.40). The A/D recipients had
a lower proportion of deaths from pulmonary causes
(5.8% versus 9.5%; p ¼ 0.02) after transplantation.
Recipients of A/D donors had a 0.8-day longer length
of stay (Table 3). The incidence of treatment for rejection
in the first year, posttransplantation dialysis,
posttransplantation stroke, or incidence of airway
dehiscence was not different based on A/D or other
causes of death (Table 3). In the logistic regression
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model of treatment for rejection within the first year after
transplantation, donor characteristics of sex and older
donor age influenced the incidence of treated rejection.
A/D cause of death did not have an influence (Table 4).
In our multivariate Cox proportional hazards analysis
model, several covariates influenced overall long-term
survival (Table 5). A/D as a cause of donor death did
not negatively impact overall survival in this model,
with a hazard ratio of 0.999 (95% confidence interval
[CI], 0.82–1.22).
Comment
In this analysis of 18,250 lung transplant recipients using
the UNOS/OPTN STAR, we found that donors whose
cause of death was A/D did not have worse outcomes or
survival compared with recipients whose donors died of
other causes. Although the use of A/D donors contributed
only a modest proportion of the donor pool (309 of 18,250
[1.9%]), there is a potential for expanding that donor pool
if these donors are considered, thus supporting the aim of
this study.
Considerations in Donors Who Drowned
There is a relative paucity of articles regarding drowning
victim donor lungs that have been used for transplantation [14, 15]. Unfortunately, there are a large number of
drowning deaths worldwide, with an estimated occurrence in the United States of 6,000 to 8,000 per year
[14, 16, 17]. In individuals who experience “dry drowning,”
in which water is not aspirated, the mechanisms of death
are attributed to acute laryngospasm and a coincident
asphyxiation, with an incidence of 10% to 15% of drowning
cases [14, 16–18]. This mechanism of death could potentially increase the lung transplant donor pool from 600 to
1,200 donors per year annually (6,000 10% to 8,000 15%)
in the United States alone.
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Table 4. Logistic Regression Analysis Associated With
Treatment for Rejection in the First Year After Transplantation
95% Wald
Odds Ratio Confidence
Estimate
Limits
p Value
Effect
Donor mechanism of death:
A/D versus other
Donor sex:
F versus M
Recipient sex:
F versus M
Donor smoking history:
No versus yes
Recipient age 55 y:
No versus yes
Donor age 50 y:
No versus yes
Transplant type:
Double versus single
Height difference (cm)
Ischemic time (h)
1.01
0.685–1.489
0.96
0.832
0.744–0.93
0.001
1.157
1.038–1.29
0.008
0.831
0.74–0.933
0.28
1.47
1.322–1.636
<0.001
1.216
1.054–1.404
0.008
0.544
0.484–0.612
<0.001
1.005
1.005
1.001–1.009
0.972–1.038
0.016
0.78
In the potential drowning victim lung donor, those who
drown in cold (< 5 C) water may have a higher tendency
toward laryngospasm and a lesser incidence of postdrowning pneumonia [19]. Cold water immersion has
been thought to be favorable in the setting of victims
who are able to be resuscitated [20]. This tendency
toward laryngospasm can make the attempted
resuscitation of the victim difficult when supraglottic
airways are used [21].
Marine microbial flora and fauna are different from
those on dry land. This aquatic environment can harbor
organisms such as Aeromonas hydrophilia,15 cyanobacteria,
and a multitude of algae [22–25]. Aspiration and contact of
the lung airways with seawater can induce a direct lung
injury and should be considered in the donor who
Table 5. Proportional Hazards Analysis Associated With Survival
Measurement
Donor mechanism
Donor sex
Recipient sex
Donor smoking history
Recipient age 55 y
Donor age 50 y
Transplant type
Height difference (cm)
Ischemic time (h)
p Value
A/D
Other
Female
Male
Female
Male
No
Yes
No
Yes
No
Yes
Double
Single
0.9959
0.9488
0.2239
<0.0001
<0.0001
0.0013
<0.0001
0.0318
0.1486
Hazard Ratio
95% Hazard Ratio Confidence Interval
0.999
Reference
1.002
Reference
0.968
Reference
0.896
Reference
0.801
Reference
0.89
Reference
0.847
Reference
1.002
0.988
0.82–1.22
0.95–1.06
0.92–1.02
0.85–0.95
0.76–0.84
0.83–0.96
0.8–0.9
1–1.003
0.97–1.00
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drowns at sea [26]. The aggregate effect of these
conditions in the lung donor who dies of drowning
needs to be further evaluated because the impact on
primary graft dysfunction cannot be ascertained from
the UNOS/OPTN STAR data, and it is known that the
development of primary graft dysfunction adversely
affects long-term outcomes in lung transplantation [27].
The STAR database does not have information on donor
lung function or specific information on donor tracheal
aspirates or microbiological findings.
Considerations in Asphyxiation Donors
A clinical situation potentially analogous to asphyxiation
would be a DCD scenario or drowning victims who
experienced dry drowning and severe acute laryngospasm. In the DCD setting, the terminal extubation
of a patient leads to an asphyxiation event and hypoxia. In
this scenario, there have been modest but consistent investigations into using this potential donor source. Many
institutions have a broad and lengthy history of DCD
experience, and this expansion may additionally increase
the donor pool [2, 4–9].
The conditions around death associated with a DCD
donor can have an effect on the allograft function, with
prolonged hypoxia and hypoventilation potentially
contributing to graft dysfunction [28]. An increase in
warm ischemia time can lead to a decrease in surfactant
[29]. Changes in surfactant have also been seen in the
patient who experiences asphyxiation, drowning, or
hypothermia [30]. Some investigators have proposed
the use of exogenous surfactant at the time of recovery
as an adjunct to organ resuscitation [31]. It bears
mentioning that the use of ex vivo organ perfusion as
an adjunct in DCD donors and organ recovery may
allow A/D donors to be used to a greater degree in the
future and improve even further on the potential of our
findings [5, 8].
Strengths and Limitations
In this analysis of the UNOS/OPTN STAR database, we
used retrospective registry data. Because of this, our
study has the inherent limitations of all observational
studies, particularly selection bias. Our study also has the
inherent limitations of the UNOS/OPTN STAR registry,
which contains US data only. Numerous clinically relevant data are not collected in the UNOS/OPTN STAR
registry, including functional status, detailed comorbidity
data, and data between listing and transplantation. We
could not assess the surgical approach, previous thoracic
procedures on the recipients, surgeon or hospital volume,
or detailed posttransplantation outcome metrics. With
the data available, we are unable to construct meaningful
comorbidity matching and analyses. As with other
large administrative databases, this data set has the possibility of missing data entries and inaccurately entered
data [11–13, 32]. The STAR database does not have information on donor lung function or specific information
about donor tracheal aspirates or microbiological findings. In addition, we do not have data on the number of
potential lung donors with A/D that were either not
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evaluated or evaluated and declined. This proportion
would give us a better ability to relate the potential
impact of A/D donors on the overall transplant pool.
Despite these limitations, there are a number of
strengths of our study. We had a large cohort of lung
transplant recipients who met out study criteria—18,250.
Although our study is neither prospective nor randomized, it is multiinstitutional. Because it uses populationbased data, it reflects the practice and patterns of care
across the United States. It is an accurate reflection of the
outcome and treatment of the population of patients
treated.
Conclusions
In our retrospective analysis of the UNOS/OPTN STAR
registry of lung transplant recipients across the United
States, we found that A/D as a donor cause of death was
not associated with poor long-term survival. This association was consistent in unadjusted and proportional
hazards analysis of survival. In addition, A/D as a donor
cause of death was not associated with an increased
incidence of treated rejection in the first year after
transplantation. Asphyxiation or drowning as a donor
cause of death should not automatically exclude the organ from transplant consideration. A point of caution,
however: consideration of very carefully selected donors
who experienced A/D deaths must give attention to the
unknown risks of primary graft dysfunction, microbiological findings, and lung parenchymal injury attributed
to the injury may be considered for lung transplantation.
These findings and the dawning of the era of ex vivo
perfusion may incrementally improve on the number of
donor lungs in the US in a positive way on behalf of our
patients.
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