Current Respiratory Medicine Reviews, 2012, 8, 274-279
274
Empyema and Bronchopleural Fistula Following Lung Resection
Alan A. Simeone*
Division of Cardiac Surgery, The Johns Hopkins Hospital, Sheikh Zayed Tower, Suite 7107, 1800 Orleans Street,
Baltimore, MD 21287, USA
Abstract: Formal resectional surgery for benign and malignant diseases of the lungs was one of the last frontiers to be
explored and mastered within the broad specialty of surgery. This was the result of the unique physiological properties of
the pleural space and the mechanics of respiration. Additional obstacles included the requirement for refined anesthesia,
surgical techniques and equipment in order to allow successful control of the airway and vasculature. Despite impressive
and ongoing improvement in operative technique, anesthetic management, patient selection and perioperative care, the
complexities unique to the airway, pleural space and rigid chest wall continue to make pulmonary resection a challenging
undertaking. Post-resection bronchopleural fistula and post-resection empyema, while relatively uncommon, remain
perhaps the most morbid and difficult complications encountered in thoracic surgery. Understanding of and adherence to
basic principles of management as well as the thoughtful application of innovative therapies have resulted in improved
outcomes when these dreaded complications occur.
Keywords: Bronchopleural fistula, empyema, lobectomy, pneumonectomy, thoracic surgery complications.
INTRODUCTION
Empyema after lung resection is frequently a disastrous
complication, as it is associated with a loss of bronchial
integrity in sixty to eighty percent of cases [1, 2]. Historically, post-pneumonectomy empyema (PPE) with bronchopleural fistula (BPF) has resulted in high mortality, profound
morbidity, and prolonged hospitalization, and has required
multiple debilitating and disfiguring operative procedures
during its treatment course. Post-lobectomy empyema (PLE)
with BPF is less common and much less likely to cause
death or major morbidity, in part because of the presence of
residual lung parenchyma in the affected pleural space. Over
the past ten to fifteen years the incidence of PNE, PLE and
BPF seems to be decreasing. Simultaneously, the interventions available for the treatment of these dreaded complications have multiplied [3]. The role of many of these novel
modalities is unclear and often controversial. Airway and
contralateral lung protection, pleural space drainage, fistula
closure, pleural space management, treatment of infection
and nutrition optimization remain the foundation upon which
successful salvage relies.
For the sake of clarity several definitions and concepts
should be emphasized. Bronchopleural fistula, in the
context of this review, refers to a breakdown in the surgical
closure of the airway after lung resection, allowing
communication between the tracheobronchial tree and the
pleural space. In the case of pneumonectomy, the fistula
involves the left or right main stem bronchial closure and in
the case of lobectomy it originates in the closure of the
upper, middle, lower or intermediate bronchus. Empyema
refers to a pleural space infection. This review focuses on
*Address correspondence to this author at the Division of Cardiac Surgery,
The Johns Hopkins Hospital, Sheikh Zayed Tower, Suite 7107, 1800
Orleans Street, Baltimore, MD 21287, USA; Tel: 410-955-9780; Fax: 410502-2399; E-mail: [email protected]
1875-6387/12 $58.00+.00
empyema occurring after lung resection, specifically
pneumonectomy and lobectomy/bilobectomy. Post-resection
empyema is frequently associated with a bronchopleural
fistula, but, particularly in the case of limited resection such
as lobectomy, can occur in the absence of fistula. The
interval between operation and presentation is of prognostic
and therapeutic importance, as the risk of mortality with
early BPF is greater [2, 4, 5]. Early BPF is arbitrarily
defined as within 30 days by most clinicians.
HISTORICAL CONTEXT
Anatomic lung resection is a relatively young treatment
modality. The complex physiology of the lung, pleural space
and chest wall thwarted early operative efforts. Control of
the transected airway was crude and the pleural space was
considered a nemesis. The first report of successful
pneumonectomy was by Nissen in 1931, for bronchiectasis
[6]. The procedure was staged over two months and involved
a preliminary thoracotomy for packing, phrenic ablation,
mass ligation of the pulmonary hilum, sloughing of the
devascularized lung and a subsequent open chest wound. A
bronchial fistula healed by granulation and the chest wall
closed by secondary intent. In 1933 Evarts Graham reported
the first single stage pneumonectomy in a patient with
squamous cell carcinoma. This procedure involved ligation
of the artery, veins and bronchus. The bronchial stump
closure was supplemented with fulguration of the mucosa.
The pleural space was almost completely eliminated by an
immediate 7-rib thoracoplasty. This patient manifested a
postoperative bronchopleural fistula and empyema in the
residual apical pleural space and required drainage and a
completion thoracoplasty, but did well and survived for
many years [7]. The work of Overholt and Rienhoff showed
that the healthy empty pleural space filled with pleural fluid
over time after successful closure of the bronchial stump and
permitted the first single-stage pneumonectomy without
thoracoplasty or drainage [8]. Subsequently an autopsy study
refuted this assertion by showing that the post© 2012 Bentham Science Publishers
Empyema and Bronchopleural Fistula Following Lung Resection
pneumonectomy space can remain complex and
heterogeneous in up to 30% of patients [9]. The issues that
made early thoracic surgery so daunting represent factors
that contribute to the incidence, pathophysiology and
morbidity seen with contemporary BPF and post-resection
empyema.
INCIDENCE
Since the late 1930’s the mortality and morbidity of
pulmonary resection have decreased significantly. Despite
remarkable improvements in operative technique, surgical
instrumentation and perioperative care, post-pneumonetomy
and to a much lesser degree post-lobectomybronchopleural
fistula and empyema continue to represent some of the major
causes of morbidity and mortality in current practice.
Empyema and BPF are extremely uncommon after lobetomy
in contemporary series, particularly after thoracoscopic
lobectomy. Empyema is seen in less than 2% of cases, and
BPF in less than 1% [10-13]. These series represent discrete
patient populations, those undergoing lobectomy for the
most part for malignancy. BPF and empyema can complicate
from 5 to 11% of lobectomies performed for infectious or
inflammatory disease, and those performed in immunosuppressed or irradiated patients [14, 15]. In contrast, PPE and
PPBPF are reported to occur with much greater frequency,
although the incidence ranges from 0 to 16% depending on
the series referenced. A series from Vienna evaluating the
use of pericardial flap coverage of the bronchial stump
reported no BPF or PPE in 93 consecutive patients [16].
Shapiro reviewed the Society of Thoracic Surgeons data base
from 2002 to 2007 and found an incidence of postpneumonectomy bronchopleural fistula (PPBPF) of 0.8%
and PPE of 0.6% [17]. Alifano, in a series of pneumonectomies after neoadjuvant chemotherapy saw 1 BPF and 1
empyema in 118 patients [18]. Other reports cite a much
higher incidence [19-25].
FACTORS AFFECTING INCIDENCE
Numerous authors have investigated possible risk factors
for the development of PPBPF and empyema. Various
patient and operative characteristics have been suggested as
likely risk factors. Evidence is strong for some and less
strong for others. (Table 1) Almost every series exhibits a
higher percentage of BPF/PNE in right sided pneumonectomy compared to left. This is often explained by the fact
that the right bronchus normally is supplied by only one
bronchial artery while the left normally receives two. In
addition, the left bronchus tends to retract under the cover of
the arch of the aorta when divided, while the right is more
likely to protrude into the free pleural space. Older series, in
which the proportion of lung resection for TB and other
infectious or inflammatory diseases is higher, tend to suggest
a higher risk of BPF and empyema. While it seems to make
sense that pneumonectomy in patients having undergone
chemotherapy and/or radiation therapy would be associated
with higher risk, this is not confirmed universally. Positive
pressure ventilation, long or large diameter bronchial stump,
positive resection margin, excessive bronchial devascularization and technical misadventures are generally believed to
contribute to higher risk of BPF. The influence of other
factors such as stapled versus hand sewn and buttressed
Current Respiratory Medicine Reviews, 2012, Vol. 8, No. 4
275
versus not buttressed has never clearly been determined.
While it is nearly unanimously believed that “high-risk”
patients should have their bronchial stumps protected by
vascularized tissue, the benefit of this practice has not been
well-studied [26]. Empyema after lobectomy is usually
attributed to prolonged postoperative air leak and therefor
chest tube duration, as well as lobectomy in the setting of
suppurative lung or pleural space disease. It is worth
recalling that any instrumented persistent pleural space,
when not filled with aerated lung, is at risk for the
development of infection [2, 15, 26].
PRESENTATION, DIAGNOSIS AND MORTALITY
Post-pneumonectomy BPF and empyema are associated
with mortality rates that vary from 5% up to nearly 50%,
again depending upon the series evaluated [2, 4, 5, 20, 22,
24, 25, 27-32]. The mortality of early PPBPF is significantly
greater than that of late PPBPF [4]. In early PPBPF the open
bronchus permits what amounts to drowning as fluid from
the pleural space is aspirated into the contralateral lung,
resulting in profound respiratory failure. The fistula, prior to
causing aspiration, permits polymicrobial inoculation of the
pleural space. Sepsis, hemodynamic instability and requirement for airway control and positive pressure ventilation are
the end results. Interference with ventilation caused by often
significant air leak makes both positive pressure and
spontaneous respiration problematic, even in the noncritically ill. Patients present from one day to several weeks
after resection with dyspnea, cough, and expectoration of
large amounts of bloody, serosanguineous fluid. If a chest
tube is still in place it generally reveals a substantial air leak.
In the absence of a chest tube subcutaneous emphysema is
often present. Hypoxemia and Hypercarbia may be present,
along with all of the manifestations of a systemic inflammatory response, sepsis or shock. If prior chest radiographs
are available they will often reveal a decrease in the amount
of pleural fluid, an increase in the amount of pleural space
air and overall volume and a shift of the mediastinum away
from the operated side [33]. Bronchoscopy is an essential
tool to evaluate the bronchial stump and assist with airway
clearance. In general, early PPBPF is not difficult to
diagnose, and additional testing such as methylene blue
instillation, radiolabelled ventilation scanning or detection of
high intrapleural O2 or N2O partial pressures is not required
[34]. Late PPBPF can result in airway contamination and
contralateral lung injury but more commonly is associated
with effects reflective of chronic infectious and inflammatory disease [4, 20]. Patients report fever, malaise, night
sweats, and often pain and pressure sensations. They may
complain of cough with foul-smelling sputum. Cachexia,
severe malnutrition and weight loss are generally present.
Chest radiographs generally reveal a decreasing fluid level in
the pleural space, again usually in combination with an
increase in the amount of air and in the total volume of the
operated pleural space, with mediastinal shift away from the
operated side. Bronchoscopy is again essential in confirming
the diagnosis and in evaluating the fistula characteristics.
Chest CT scanning can provide additional information,
particularly in cases where the diagnosis is unclear and in
patients whose operative procedure was lobectomy or
bilobectomy. In contrast to early BPF, patients presenting
late after resection can be difficult to diagnose. Methylene
276 Current Respiratory Medicine Reviews, 2012, Vol. 8, No. 4
blue instillation, radionuclide ventilation scanning and
pleural gas sampling for high oxygen or nitrous oxide partial
pressures can be helpful [26, 34]. The majority of patients
presenting with BPF and empyema after lung resection
manifest marginal pulmonary function and nutritional status
and are deconditioned due to recent surgery, disease-related
factors and often neo- or adjuvant therapy. They can be
considered to be immunosuppressed. All of these issues
represent significant difficulties as therapy is begun.
Interestingly, not all ominous post-operative chest
radiograph findings are what they seem. Using serial chest
radiographs Christiansen studied the pneumonectomy space
in a series of 54 patients who proved over time to be free
from PPE and BPF, and compared it to the space in six
patients who did develop PPBPF. Nine of the 54 patients had
at least one x-ray which showed a significant pleural fluid
level drop during their post-operative course. When
compared to the six patients with BPF, benign fluid level
drops were characterized by a decrease in the total volume
and volume of air in the operated pleural space, and a shift of
the mediastinum towards the operated side. Additionally, the
pleural spaces were found (by chest X-ray) to be completely
filled between 3 weeks to 7 months, with an average of 3.9
months [33]. This phenomenon has been revisited recently
and termed “Benign Emptying of the Post-pneumonectomy
Space” (BEPS) by Merritt et al. [35]. They describe seven
patients with dropping post-operative pleural space fluid
levels who on long-term follow up showed no sign of BPF or
empyema, and suggest that such patients who have no fever,
cough or expectoration, normal white blood cell counts and
normal bronchoscopies may be followed closely.
TREATMENT
Appropriate treatment of post-resection empyema and
BPF is dependent on multiple factors. The nature of the
resection (pneumonectomy or lobectomy), the interval
between surgery and presentation (early or late), the
condition of the patient and the underlying disease
prompting lung resection are all major determinants of the
therapeutic plan. Post-lobectomy empyema, (PLE) early or
late, is not commonly associated with BPF. Early PLE is best
managed by prompt, complete pleural space drainage, if
necessary including debridement of the residual pleural
space via thoracoscopy or thoracotomy. Chest drains should
be placed above the thoracotomy incision, to avoid
diaphragmatic injury as the diaphragm often rises and
adheres to the site of the thoracotomy. Antibiotic coverage
based on culture and sensitivity data is important. Complete
re-expansion of the remaining lung is essential, as the
smaller the persistent pleural space the better and more
expeditious the resolution [2, 15, 36]. It is often reasonable
to treat an early PLE similarly to a post pneumonic
empyema, with prolonged chest tube drainage, nutritional
support and patience. The residual pleural space will shrink
as the remaining lung expands, the diaphragm rises and the
mediastinum shifts [2, 15]. In the case of bilobectomy with a
large empty space, more aggressive measures may need to be
undertaken that resemble modalities utilized for PPBPF and
PPE. Late PLE represents a much different situation. The
lung is more likely to be trapped, the mediastinum and
diaphragm more likely to be immobile and inflamed and the
Alan A. Simeone
chest wall more likely to be woody, indurated and immobile.
Thoracotomy and decortication in this situation can be
unwise, as morbidity is high and likelihood of success
questionable. While urgent drainage is important,
particularly if signs and symptoms of sepsis are present,
prolonged chest tube drainage is not the optimal approach
unless the patient will not tolerate more involved measures
[36]. Open window thoracotomy (OWT), Eloesser flap or
Modified Eloesser flap [37, 38] with debridement, dressing
changes and either obliteration by secondary intent,
obliteration by vascularized tissue flap or closure over
debridement antibiotic solution (DABS) are more likely to
result in healing [36]. Recently negative pressure wound
therapy using the Vacuum Assisted Closure (VAC) system
(Kinetic Concepts, Inc., San Antonio, TX) has been reported
to provide good results while simplifying the management of
these patients [39-41]. If a bronchopleural fistula is present
along with the PLE the treatment generally becomes more
complex. The pleural space problem will not resolve without
closure of the airway. The standard approach to these
patients consists of appropriate drainage, thoracotomy or
OWT with debridement of the bronchus and closure
supported by intercostal muscle, diaphragm, omentum,
pericardium or chest wall muscle flap buttress [15, 36]. The
residual pleural space has been managed by persistent OWT,
obliteration by vascularized tissue transfer, closure after
filling with DABS or VAC therapy. Some surgeons continue
to utilize a thoracoplasty, which revisits the early days of
chest surgery and consists of sub-periosteal resection of the
ribs, allowing the unsupported soft tissues of the chest wall
to collapse inward to fill residual space [42, 43]. While it is
an effective means of obliterating a pleural space, it is
disfiguring, associated with substantial morbidity and
mortality and thankfully not often required or utilized.
Debilitated, malnourished patients with advanced or
metastatic malignancy can be palliated by drainage via OWT
alone, as long as the residual lung is adherent and stable in
the pleural space and tidal volume losses are tolerable. Less
invasive modalities, commonly utilizing bronchoscopic
delivery, have been reported with increasing frequency in
recent years in both post-lobectomy and postpneumonectomy patients who had either failed or could not
tolerate standard operative approaches. Successful closure of
bronchopleural fistulae using endobronchial adjuncts
requires that the fistulae be small (less than 5 to 8 mm). The
pleural space must at the very least be adequately drained in
order to prevent a recurrence of a closed-space infection.
These techniques include silver nitrate application [44],
Fibrin glue and spongy bone [45], collagen matrix plug (anal
fistula plug) [46], Bioglue [47] and aneurysm coils and fibrin
glue [48-51]. Clemson and colleagues reported CT-guided
transthoracic delivery of coils and cyanoacrylate glue in the
successful closure of two large PPBPFs in patients not
candidates for major operation [52]. Endobronchial stent
delivery to either occlude or exclude a BPF has also been
reported with increasing frequency in contemporary series
[53-58]. Some groups have also used endobronchial
Amplatzer devices for BPF control [41, 59-61]. The majority
of these reports have involved patients who either were too
unwell to tolerate standard operative therapy or who had
failed operative attempts at BPF closure. At this time the
Empyema and Bronchopleural Fistula Following Lung Resection
new techniques are exciting but their ultimate utility remains
to be determined [3, 62].
Post-pneumonectomy empyema and BPF represents a much
more complex and difficult management problem than postlobectomy empyema and BPF, with much greater morbidity
and a substantially higher risk of mortality. Early PPBPF
represents an emergency due to the risk of aspiration, lung
injury, pneumonitis and pneumonia and ultimately lifethreatening respiratory failure [1, 4, 20, 27, 63, 64]. The patient
should be positioned with the pneumonectomy side dependent.
A chest tube should be placed immediately, with the
pneumonectomy side dependent, in order to rapidly evacuate
fluid and air and protect the remaining lung. If lung injury has
already occurred endotracheal intubation should be performed
with selective contralateral main stem intubation, a double
lumen tube or a bronchial blocker to ensure that the remaining
lung can be ventilated without unmanageable volume loss
through the fistula. Broad spectrum antibiotics should be started
and pleural fluid cultured to allow de-escalation based on
sensitivities. Unstable patients with noncompliant residual lung
and refractory hypoxemia/hypercarbia are not candidates for
emergency re-thoracotomy. Extracorporeal Membrane Oxygenation (ECMO) has been utilized as a salvage modality [63].
Patients without evidence of ongoing or incipient respiratory
failure should undergo prompt thoracotomy, with debridement
of the bronchial stump, shortening if it is possible, and bronchial
closure buttressed by a flap of vascularized tissue such as
diaphragm, intercostal, pericardium, omentum or chest wall
muscle. The pleural space should be debrided. The subsequent
management depends on surgeon preference and to some
degree patient factors. Clagett, in 1963, proposed a method of
treating the PPE and BPF. Thoracotomy, stump closure and
pleural debridement were performed. Subsequently, the pleural
space was treated by repeated dressing changes until the entire
surface appeared clean and granulated. At this point the space
was filled with debridement antibiotic solution and watertight
chest closure performed. Forty percent of the closures failed due
to recurrent bronchial stump dehiscence. After repeat treatment
ultimately about 90% were successful [65]. Pairolero in 1990
reported on a modification of the Clagett Procedure in which the
first stage (open drainage and dressing changes) was
supplemented with muscle flap closure in those patients with
BPF. Success was achieved in 85% [66]. Recent reports
elaborate on the technique and confirm the good results [31].
While it is effective, the Modified Clagett procedure requires
multiple procedures and a long hospital stay. In an effort to
address this some groups have proposed further modifications.
Schneiter and colleagues report on a technique which utilizes
open drainage, stump closure with omental flap, dressing
changes every 48 hours until macroscopic cleanliness is
achieved and chest closure after the space is filled with
antibiotic solution [67]. Chest closure was achieved by 8 days in
all patients, hospital stay ranged from 7 to 35 days and no
recurrence was seen. Both early and late BPF/PPE cases were
included. Other groups, particularly in early PPBPF or in cases
where the pleural space and mediastinum are reasonably pliable
utilize pleural space antibiotic irrigation rather than open
packing and dressing changes. Pleural effluent is cultured at
prescribed intervals and when sterile the chest is closed after
filling with antibiotic solution [2]. The management of late PPE
and BPF represents different challenges. The mediastinum and
Current Respiratory Medicine Reviews, 2012, Vol. 8, No. 4
277
hilum tend to be indurated, inflamed and unrecognizable.
Drainage and debridement remain essential, but early bronchial
closure is often not possible. Classically, prolonged open
window drainage and repeated debridement is performed
followed by attempts to identify and close the bronchus, again
with vascularized tissue coverage. Additional bulky muscle or
omental flaps are transposed into the pleural space in order to
obliterate it and the chest is closed over drains. As might be
imagined in these patients it is often difficult to find enough
bulk to work with. Free flaps can be options but can be difficult
[68]. If bronchial integrity can be restored with confidence the
modified Clagett procedure is also an option [31]. When the
hilum is deemed too hostile to allow a safe approach to the
bronchial stump, the bronchus has been approached
transsternally as well as transcervically [30, 69, 70]. These
alternate approaches to the main bronchi improve safety but do
not permit access to the pleural space, thus necessitating at least
one additional procedure to address drainage and debridement.
As mentioned in the discussion of post-lobectomy BPF, small
fistulas may be amenable to endobronchial interventions,
allowing a sort of hybrid approach to management. Finally, the
role of negative pressure wound therapy has still not been
completely defined. Wound VAC therapy has been shown to be
ideal in other types of complex wounds and is likely to become
a cornerstone in the treatment of the difficult postpneumonectomy space [2].
CONCLUSION
Post resection BPF is uncommon, but there are defined
groups at increased risk. Initial management relies on
draining the pleural space and preventing aspiration.
Subsequent management will be determined by the timing
relative to the original surgery and the patient’s physiologic
status. Early (within one week) bronchial leaks may be
approached by repeat thoracotomy, but more chronic spaces
often require approach via sternotomy and/or separate
strategies to manage the residual space. Any attempt to
directly seal the origin of the leak at the bronchial level
should include the use of tissue flaps. Depending on the size
of the leak and the patient’s overall status, avoiding direct
repair and concentrating on space draining procedures (such
as open window thoracostomy) may be the safer approach.
The role of non-traditional approaches to the disrupted
airway requires additional study.
Table 1.
Risk Factors for Bronchopleural Fistula
Immunosuppression
Right Pneumonectomy
Diabetes
Completion Pneumonectomy
Pneumonia, Active TB
Extrapleural Pneumonectomy
Empyema
Long Bronchial Stump
Malnutrition
Large Diameter Bronchial Stump
COPD
Positive Resection Margin
Smoking
Positive Pressure Ventilation
Chemotherapy
Large Postoperative Fluid Requirement
Benign Diagnosis
Prolonged Chest Tube Utilization
XRT
278 Current Respiratory Medicine Reviews, 2012, Vol. 8, No. 4
ACKNOWLEDGMENTS
Alan A. Simeone
[22]
Declared none.
[23]
CONFLICT OF INTEREST
The author confirms that this article content has no
conflict of interest.
[24]
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Revised: November 30, 2011
Accepted: December 29, 2011