Imaging of Complications Transplantation PeterB.
O’Donovan,
With
the
increasing
recipients, lung
MB,
radiologists
response,
that
a mild
haze
perihilar lung
bases.
bronchial the tions ble
be
are
evaluation.
radiography,
chial
effusions,
cuffing,
and
Radiographic
air-space
features
diminished
lung
volumes,
lung
tive
pneumonias,
tion,
markings.
candidiasis,
with
fewer
and
invasive
can edema,
increase
in the
or in-
peribron-
in cardiac
include
both
peripheral
size.
increased
and
bronchiectasis,
atelectasis,
thin
thickening,
and seen,
occurrences
visi-
aid
as new
subpleural
is frequently
Stric-
local-
linear
irregular
diminished
periph-
especially
gram-nega-
of cytomegalovirus
infec-
aspergillosis.
INTRODUCTION
U
The
past
and
heart-lung
lung
decade
and
has seen
Abbreviations:
Index
heart
diseases.
RadloGraphics From
vember quests ©J.5N&
in
AP
terms:
the
the emergence
transplantation
transplantation
I
Infection
collec-
is usually
tomography
and
through air
lumina
without
central
to prevent
dehiscence.
bronchial
rejection
from
areas
Extrabronchial
radiographically
disease,
of chronic
ized air-space disease, partial lobar areas of increased opacity, pleural eral
(used
lines,
after
perihilar
contents
of anastomotic
septal
hours
of abdominal
is evident
rejection
pleural
48
in the
computed
of
in appearance
of omentopexy
the but
features
seen varies
thorax.
manifestation compromises
Acute
creasing
the
transplant
Reimplantation
consolidation
into
imaging
edema resolves,
is herniation incision
plain
of the
of lung
complications.
complication
a radiologic
with
aware
associated
to a dense
that
survival
pulmonary
A late
formation
improved
subsequently
dehiscence)
diaphragmatic
ture
the
a noncardiogenic
transplantation and
and
should
and
1
.
BCh
number
transplants
of Lung
=
Lung, 1993;
as therapeutic
Since
1983
(1),
anteroposterior,
infection,
60.20
Cooper there
PA #{149} Lung,
=
has
of lung transplantation, options for patients
performed been
an
single with
the first successful exponential
growth
and double, end-stage
single-lung in the
frequency
posteroanterior transplantation,
60.458
13:787-796
Department
of Radiology,
9, 1992; revision to the author. 1993
requested
Cleveland
February
Clinic
16, 1993
Foundation, and
received
9500 March
Euclid
Aye,
Cleveland,
3; accepted
March
OH
44 195.
8. Address
Received reprint
Nore-
787
a. Figure
b. 1.
(a) Posteroanterior
(PA) radiograph obtained 10 months after right lung transplantation for end-stage obstructive pulmonary disease. Note the mediastinal shift and compression of the transplanted lung by the extensive bullous disease present in the native left lung. (b) Anteropostenor (AP) bedside radiograph obtained after left pneumonectomy. Note better expansion of the transplanted lung and shift of the mediastinum toward the side of the pneumonectomy after the
removal
of the emphysematous
left lung.
of this procedure. As of the end of December 1991, 716 single-lung, 289 double-lung, and six lobar transplantations had been reported to the transplant registry (2). A number of factors have contributed to the success of lung transplantation, including improved pa-
U
tient
out evidence of infiltrate. They must be capable of adequate gas exchange (arterial partial pressure of oxygen greater than 300 mm Hg, an inspired oxygen fraction of 1.0, and a positive end expiratory pressure of 5 cm H2O).
selection,
advances
improved
in surgical
tive care, and improved
organ
preservation,
technique and postoperaimmunosuppressive
therapy. The increasing number and improved survival of transplant recipients have facilitated descriptions of the associated imaging features (3). This article reviews the spectrum of radiographic findings associated with singleand double-lung transplantations and discusses their causes. The cases illustrated were selected from the first 25 procedures performed at the Cleveland Clinic, Ohio. The radiographic findings of the well-recognized complications associated with lung transplantation are discussed in chronologic order of their appearance after transplantation. A brief description of pulmonary allografts as they relate to the hung size of the recipient is also included.
788
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RadioGraphics
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O’Donovan
PULMONARY
The
limited
susceptibility
tion,
ALLOGRAFTS
supply of donor lungs reflects the of the lung to aspiration, infec-
atelectasis,
quent
and
to brain
allografts
death
must
Results
be
of the
pulmonary
(1).
edema
Potential
subse-
pulmonary
radiographically
clear
bronchoscopic
with-
examination
must
be normal. When an allograft becomes available and blood group compatibility has been estabhished, it must be sized to the recipient’s thorax. The optimization oflong-term function and the need for good pulmonary mechanics mandate careful attention to pretransplantation
matching.
in patients
oversized sirable:
For with
lung The
single-lung
transplantation
obstructive
(up
thoracic
lung
to 25%-30% cavity
will
disease,
larger)
an
is de-
compensate
for the larger size, and the of pulmonary parenchyma long-term results (4). Despite careful attention before the transplantation,
increased volume may provide better
hems
1). When
are
encountered
(Fig
Volume
to compatibility matching prob-
13
the
do-
Number
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a.
b.
Figure 2. (a) Bedside AP recumbent radiograph of the chest in a 44-year-old woman obtained 3 days after left lung transplantation for primary pulmonary hypertension. Note the relative oligemia in the native right lung and the marked reimplantation response in the transplanted lung. (b) Radiograph obtained 2 days later reveals increased perfusion in the native right lung and some clearing of the reimplantation response from the transplanted left lung.
nor
lungs
are
hemithoraces racic
smaller
than
(due
to chronic
hyperinflation
cipient’s
thorax
size over
time.
in the will
the
recipient’s
marked
recipient),
conform
to donor
thothe relung
muhation. Dogs derwent biopsy 3rd postoperative specimens
showed
interstitium. graphic
REIMPLANTATION RESPONSE Reimplantation response refers to an infiltrate that appears within 48 hours after transplantaU
tion
that
is not
related
to fluid
overload,
left
ventricular failure, infection, atehectasis, or rejection. The condition is diagnosed by exclusion and is believed to represent noncardiogenic pulmonary edema. In reviewing 14 single-lung transplantations, Herman et al (3) encountered the reimplantation response in 13 patients. The severity of the radiographic appearance
is variable,
ranging
from
mild
perihilar haze to unilateral or bilateral dense consolidation involving the perihilar areas and the lung bases. The infiltrates usually peak by the 4th postoperative day and subsequently resolve at a variable rate. Clinically, the infiltrate manifests itself before extubation by increasing hypoxia. Experimental suggests
that
dogs
is the
July
1993
work
the result
by
Siegelman
reimplantation of extravascular
receiving lung allografts unof the lung on the 1st and days. Analysis of biopsy fluid
Chiles pattern
accumulation
et a! (6)
consistent
in the
reported with
a radio-
pulmonary
edema in all of 10 recipients of heart-lung transplants. The pathogenesis of the reimplantation response is unknown, but several causes been postulated. These include lymphatic
interruption, organ trauma
pulmonary
preservation associated
reimplantation observed tients
that who
denervation,
poor
or ischemia, and physical with the harvesting and of the lung (7). Herman (8) the process was milder in pa-
underwent
heart-lung
transplanta-
tion than in those who underwent transplantation. In our experience, plantation response has been more sive
radiographically
single-lung hypertension lung (Fig
have
in patients
single-lung the reimimpres-
who
received
transplants for primary pulmonary than in those who underwent
transplantation
for other
conditions
2).
et a! (5)
response in fluid accu-
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Figure
4.
Axial CT scan
obtained
through
the right
,ronchial anastomosis in a right lung transplant recipt reveals a surgical clip anterior to the bronchial inastomosis and sutures at the right pulmonary anas-
I omosis.
Note the bronchial anastomotic stricture solid arrow). An intercostal muscle flap in the left side of the chest (open arrow) is also
:straight )osterior
Iseen.
The
tround
COMPLICATIONS The use of an omental the time of transplantation
OF pedicle
U
around
the bronchial
effective
in the
The
omentum
duced
into
incision incision line
the
in the may or
with
its blood
chest
cavity
through
diaphragm. be
through
supply This
made
is intro-
aspect
mosis
effected
the
blood
supply
within
vessels
from
omentum, effusion’
mid-
‘
the
omentum.
however, appearance. brought
posterior
mediastinum the
3 days
lung,
it can
within
that the anasto-
and
are
cle along bronchial
with
its blood
technique
(Fig
an
effusion
4)
frequently
supply
3) or
prominence on plain of the bronchial wrap fled at CT (Fig 4).
anterior
because
anasto-
(9).
Use
of the
it ascends
of a problem
arterial
preserved
anastomosis. results
anasto-
anastomo-
is less
transplantation
The
the
is more
at the
bronchial
bronchial
(Fig
use
trans-
anastomosis
ischemia
of
diaphrag-
changes
of heart-lung networks
the
A double-lung
bilateral
collateral
in a “pseudothe omentum
complication
herniation
An alternative approach to omental zation is the harvesting of an intercostal
pexy
of bronchial
when mimic
are
Tracheal
the coronary motic
3d).
through
may result Although up
.
A late
a tracheal
to ischemic than
(8)
3).
through
(Fig with
in cases
of the
have shown the bronchial
restoration
is usually hind
I
studies to wrap
defect
mosis
dome on the left side. The mobilized omentum is extended cephalad into the chest and wrapped around the bronchial anastomosis. Results of canine use of omentum
(Fig
contents
plantation
ses
arrows).
is diaphragmatic
susceptible
a small in the
posterior
matic
diaphragmatic
anteriorly
the
radiograph
abdominal
(9).
and can be seen
(curved
of omentopexy
has been
of dehiscence
medially
bronchus
supine
OMENTOPEXY harvested at and wrapped
anastomosis
prevention
flap courses
the
to wrap
of the the
mobilimus-
the
omento-
intercostal
in increased
radiographs. can usually
wrap hihar
The origin be identi-
or beon
a
Figure 3. (a) Bedside AP supine chest radiograph obtained 1 week after left lung transplantation in a 44year-old patient with cor pulmonale secondary to chronic berylhiosis. Loss ofvisualization ofthe left hemidiaphragm was thought to be consistent with a left pleural effusion. (b) On a computed tomographic (CT) scan obtained 3’/2 weeks hater, the appearance of the left hemithorax has changed little. Fat is seen posteriorly (arrows) in the left side ofthe chest, accounting for the pseudoeffusion appearance. (c) Another CT scan demonstrates the omentum (arrow), which extends anteriorly between the aorta and left pulmonary artery as it wraps around the left main-stem bronchus. (d) AP image from a barium swallow study performed 2’/2 months after transplantation when the patient returned complaining of chest pain. There is herniation of the gastric fundus through the diaphragmatic defect created for passage of the omentum. (e) Axial CT scan demonstrates the enhanced gastric fundus surrounded by omentum within the left hemithorax.
July
1993
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h14;,*..c _:
a. b. Figure 5. (a) Bedside AP chest radiograph obtained 3 weeks after left lung transplantation in a 33-year-old man with chronic obstructive pulmonary disease. A newly appearing infiltrate is seen in the left lower lung. (b) Angiogram performed after a ventilation-perfusion study that was interpreted as high probability for pulmonary (black embohi
embolism. There arrows) and several (white arrows).
AIRWAY
U
AND
is evidence of a moderate filling defects within the
VASCULAR
tive
of anastomotic images
should
dehiscence. be
Postopera-
carefully
evaluated
for
the presence of small extrabronchial collections of air at the site of the anastomosis. In the experience of the Toronto lung transplan-
severe
strictures
may
with
benefit
from placement of stents (1 1). Mild to moderate strictures can be treated with laser resection and balloon bronchoplasty. Little has appeared in the radiologic literature about the integrity of the arterial anastomosis
in patients
after
lung
transplantation.
chest images in five of six cases of bronchial anastomotic dehiscence (10). CT can be useful in demonstrating more subtle gas collections.
It is believed
fined,
in the
immediate
aid
group,
in the
When tion,
the
extraluminal
cases
air
that
healing
was
avoidance
postoperative
visible
on
of steroids
period
may
process.
healing
occurs
luminal
compromise
on a well-penetrated Herman and colleagues
of moderately
with
stricture is often
PA chest radiograph. (3) encountered
severe
bronchial
RadioGraphics
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O’Donovan
and
luminal
anastomosis lar anastomoses
is rarely are
studied
have encountered one bolism in a 33-year-old
two
derwent
single-lung
at the site of
encountered. therefore not
visible
stricture
subsequent
compromise
forma-
in 14 single-lung transplantations. If a suspected stricture is not evident at radiography, the bronchial anastomosis can be evaluated well with both bronchoscopy and CT (Fig 4).
U
with
anastomosis consistent
The anastomosis may be technically difficult, particularly in transplant recipients with longstanding pulmonary hypertension in whom the central vessels are markedly dilated but the donor artery is of normal caliber. Techniques of arterial anastomosis have been re-
tation
792
of stenosis at the site of arterial left pulmonary artery branches,
Patients
COMPLI-
CATIONS The presence of extraluminal air collections at the site of anastomosis is a radiologic manifestation
degree proximal
The vascuroutinely
to this procedure. case man
We
of pulmonary (Fig 5) who
transplantation
for
emunoblit-
erative bronchiolitis. The acute embolic episode occurred 1 month after transplantation. Pulmonary angiography helped confirm the presence of emboli and also revealed a stricture of the pulmonary artery at the site of anastomosis. The prevalence ofvascular stricture formation has not been evaluated in this patient population.
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a. b. Figure 6. (a) AP chest radiograph obtained 4% weeks after double-lung man with cystic fibrosis. Note the bilateral pleural effusions, prominent normal heart size, and suboptimal definition of the central vascuhature walls.
(b)
typical with
Lateral
radiograph
for acute steroids,
rejection. and
U ACUTE Although
the
early
in the
tion
is usually
days
after
appearance
response course,
not encountered
shows
and later shoughed
acute
histologic tion and
rejec-
before Acute
a mononuclear
a fibrinous pneumocytes
5-10
rejection cell
his-
infiltrate
and
changes are specific for early may be seen in transbronchial
cuffing,
and
air-space
disease.
rejecbiopsy
Usually,
there is no associated increase in the patient’s weight or in the cardiac size. Septal lines and new or increasing pleural effusions are the most common radiographic features of acute lung rejection (Fig 6). The combination of septal lines and new or increasing pleural ef-
July
1993
diac
biopsy.
The
patient
was
treated
without size,
a concomitant
vascular
pedicle
increase width,
in car-
vascular
re-
has been reported as 90% specific and 68% sensitive in the diagnosis of acute lung rejection (13). The diagnosis of acute rejection is usually made on the basis of a drop in the arterial pardistribution
tial
exudate with oc(12). These
specimens. The radiographic findings associated with rejection include an increased volume of fluid in the ipsilateral pleural space, the presence of septal lines, subpleural edema, peribronchial
consistent with with transbronchial
improved.
is seen
the arteries, veins, bronchioles, septa. Initially, there is alveolar
edema casional
fissures
was confirmed
fusions
REJECTION reimplantation postoperative
thickened
diagnosis
radiographic
transplantation.
tologically
around alveolar
the
reveals
The
transplantation in a 28-year-old septal lines, normal vascular pedicle, in addition to thickened bronchial the presence of fluid. Findings are
pressure
infection,
load.
The
corticosteroids
3 consecutive normalities with
of oxygen, airway
steroids,
with
no
obstruction,
condition
is treated administered
days. improve the
When rapidly radiologic
evidence
or
fluid
with
of over-
a bolus
of
intravenously
the
for
radiologic after
ab-
treatment
diagnosis
of
acute rejection is confirmed. Although pulsed doses of methylprednisone are the first line of treatment in acute lung rejection, polyclonal T-cell antibody (antithymocyte globulin), monoclonal antibodies (CD3, OKT3), and lymphoid irradiation have also been used to suppress the immune system (14).
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793
a. Figure
b.
Bedside AP chest year-old man with cystic fibrosis. siderable nodular coalescence on tamed 5 days later helps confirm Specimen from open lung biopsy (arrow), which relates to a bilateral
hated
7.
(a)
hydropneumothorax
radiograph obtained 1 month after double-lung transplantation in an 18Note the nodular infiltrate, more pronounced in the lung bases, with conthe right with associated right pleural thickening. (b) Axial CT scan obthe presence ofa nodular infiltrate and small bilateral pleural effusions. revealed cytomegalovirus. Note the overriding sternal fracture anteriorly inframammary incisional approach for transplantation, and a small locu-
on the right.
INFECTION The prevalence of infection after lung transplantation may be as high as 50% (15). This is a significantly higher frequency than in other perfused organ transplant groups. Many of the infections involve the transplant itself, and impaired mucocihiary transport in the denervated lung after transplantation may be a conU
tributing plications Maurer tions
factor. In a review of infectious cornfollowing lung transplantation, et al (15) found that bacterial infec-
were
the
most
common,
particularly
in
the first 2 months after transplantation. Pneumonias encountered were frequently due to gram-negative infections. A mixed group of extrapulmonary infections were found that constituted 40% of the infectious complications. Every attempt is made to match donors who test negative for cytomegalovirus with recipients who also test negative for cytomegalovirus. Should either donor or recipient or both test positive for cytomegalovirus, routine prophylaxis with gancyclovir is started postoperatively. Nodular opacities with coalescence are a typical radiographic manifestation of cytomegalovirus infection (Fig 7). In the series reported by Maurer et al (15), fungal infections were limited to four cases of candidiasis,
one
ofwhich
was
an
empyerna,
and
a case
also
encountered
of invasive
RadioGraphics
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O’Donovan
aspergillo-
(Fig 8). Srnyth et al (16) reported a similar case in which invasive aspergillosis developed in the native lung after single-lung transplantation. The possibility ofsaprophytic colonization of the native lung with Afumigatus, which becomes invasive after transplantation, is raised
by
Shaffer
(17).
Pneumocystis
carinii
pneumonia is infrequent in this patient lation because postoperative prophylaxis routinely administered. U
CHRONIC
Experience surviving
popuis
REJECTION to date
allograft
suggests
that
recipients
long-term
may
expect
sub-
stantial clinical and functional improvement (18, 19). The development ofchronic rejection appears to be the major problem in longterm (ie, longer than 3 months) survivors. Morrish et al (20) reported the development of chronic rejection 3-75 months after transplantation in 10 of4l patients who underwent lung transplantation (27 single-lung and 14 double-lung
procedures).
the pathologic were obliterative pneumonitis, lopathy. Symptoms
In their
series,
correlates of chronic rejection bronchiolitis, interstitial and rejection-mediated vascuof chronic
coughing,
ening exertional recently reported
U
We have
of invasive
sis
sistent
794
aspergillosis.
a case
rejection
wheezing,
include
and
slowly
dyspnea. Burke the development
Volume
perwors-
et al (21) of bron-
13
Number
4
(a) Axial CT image man with idiopathic
Figure 8. 56-year-old
bent
chest
radiograph
native right lung. (c) Axial CT scan
trate,
some associated in the transplanted Aspergillusfumigatus
chiohitis
obhiterans
al (22) itis
obtained
3 months patchy
the carina
fibrosis.
after
Note
left lung
parenchymal
for a pre-lung
peripheral
transplantation.
opacities
2 days before the chest radiograph and exclude pleural involvement.
are
in five
reported
obliterans
of
14 long-term
transplantation. 1 1 cases in which
developed
after
sur-
Skeens bronchiol-
et
heart-lung
transplantation
honeycombing.
to assess Honeycombed
in the
Bedside
infiltrate
in a
AP recum-
is seen
transplanted
the extent spaces areas The
evaluation
(b)
Extensive
identified
central infiltrate, are seen. Occasional, small nodular lung. The findings are consistent with aspergillosis. infection 4 days after the CT examination.
of heart-lung
vivors
just below
pulmonary
Occasional
obtained out cavitation,
rule
obtained
in the
left lung.
of a newly appearing infilin the native lung, with
of high patient
attenuation are identified died of overwhelming
minished peripheral lung markings. Nodular or reticular nodular opacities associated with peribronchial thickening have also been reported. We have seen a number ofthese ra-
transplantation. The diagnosis was documented with results from open lung biopsy in five cases, transbronchial biopsy in three, and autopsy in two; in one case, the diagnosis was
diographic
findings
this
insti-
tution who obhiterans,
have developed bronchiohitis proved with open lung biopsy
re-
made
eral bronchiectasis markings were
on the basis
A wide
been sis
variety
reported
sis,
rejection
creased
air-space thin
opacity,
1993
criteria
linear
pleural
alone.
features with
(20-22).
both increased and central and peripheral
localized
atelectasis,
July
in association
of chronic
included volumes,
of clinical of radiographic
the
have diagno-
These
have
diminished lung bronchiecta-
disease,
partial
lobar
irregular
areas
of in-
thickening,
and
suits.
sions
In one
appeared
in patients
patient,
seen
both
from
central
and increased (Fig 9). Large
in the
periphery
and
periph-
interstitial cystic Icof the
lung before the patient’s death. The these findings is uncertain, but they resent a manifestation of barotrauma.
right
cause of may rep-
di-
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795
CONCLUSION
U
Single-
or
double-lung
transplantation
is now
a treatment option for patients with end-stage lung disease. With the dramatic growth in the number of these procedures being performed,
radiologists
expected
should
radiographic
transplants
and
be aware
appearances
the
associated
of the
of lung
complications.
REFERENCES
U
1.
2.
Winton TL, MillerJD, Patterson GA, and the plant Group. Donor nary transplantation. 23:2472-2474. Registry of the
and
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GC, Patterson GA, CooperJD. lung transplantation: imaging features. ology 1989; 170:89-93. 4.
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Siegelman SJ, Sinha SB, Veith FJ. Pulmonary reimplantation response. Ann Surg 1971; 177:30-36. Chiles C, Guthaner DF, Jameison SW, Stinson EB, Oyer PE, Silverman JF. Heart-lung transplantation: the postoperative chest radiograph. Radiology 1985; 154:299-304. Tsai SH, Arnar 0, HaglinJJ. Roentgenographic appearance of the transplanted pri-
mate
lung:
1969;
the autotransplanted
lung.
tient as in Fig 7). Note the thickened bronchial wails, right cardiophrenic angle.
base
R,
MaurerJ, and the Toronto Lung Transplant Group. Double-lung transplant for advanced chronic obstructive lung disease. Am Rev Respir Dis 1989; 139:303-307. 5.
Figure 9. Bedside AP chest radiograph 8 months after left lung transplantation
AJR
Herman SJ. Radiologic assessment after lung transplantation. Clin Chest Med 1990;
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LadowskiJS,
to open
lung
dilated bronchi best appreciated Sutures in the
biopsy
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performed
at the
time of severe cytomegalovirus pneumonia (see Fig 7). There are sutures in the left mid-lung zone peripherally at the site of a second open lung biopsy,
which
yielded
a diagnosis
of bronchiolitis
obhiter-
ans and vasculopathy consistent with chronic rejection. The biopsy was performed 2 months before this radiographic study. The middle portion of the right lung reveals peripheral cystic air spaces, which appeared shortly before the patient’s death. They may
represent a manifestation tively relate to obliterative interstitial
to complain
106:563-566.
8.
relate
obtained (same pa-
findings
markings
ofbarotrauma bronchiolitis.
appeared
or altemaThe increased
as the
patient
began
of increasing shortness of breath. are typical for chronic rejection.
The
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monary
artery
nal trachea.
blood
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RL, Griffith BP. Pulsupply to the supracari-
Transplant
1984;
lung 17.
4:40-
1 1.
Morgan Fordman
E, Lima 0, Goldberg
M, Ayabo H, A, CooperJD. Improved bronchial healing in canine left lung reimplantation using omental pedicle wrap. J Thorac Cardiovasc Surg 1983; 85:134-139. Klepetko W, Grimm M, Laufer G, et al. One and one-halfyear experience with and bilateral lung transplantation. Surg 1992; 7:126-133.
12.
Tsai
SH, Anderson
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TF, Kiesel
HaghinJJ,
Graft
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in
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