Professional Documents
Culture Documents
T h o r a c i s i n L o w - R e s o u rc e
Settings
Abebe Bekele, MD, FCS (ECSA), FACSa,b,*,
Barnabas Tobi Alayande, MBBS, MBA, FMCSa,c
KEYWORDS
Empyema thoracis (thoracic empyema) Low-resource settings (LRS) Chest tube Thoracotomy
Decortication
KEY POINTS
Most cases of empyema thoracis are sequelae of severe pneumonia, but chest trauma and com-
plications of chest tube insertion as cause are not uncommon in low-resource settings.
The diagnosis is usually late due to delayed presentation to health care facilities, low index of sus-
picion among health care professionals, and inability to properly stage the disease with the avail-
able diagnostic tools.
Early use of antibiotics and appropriate-sized and well-placed chest tube drainage is associated
with good outcomes at a decreased cost.
Surgical management of empyema thoracis is indicated when chest tube drainage and antibiotic
treatment fails to achieve complete resolution.
The decision to operate on patients with thoracic empyema in an LRS should not be taken lightly
due to the risks of bleeding, incomplete expansion, and lung injury.
a
University of Global Health Equity Kigali Heights, Plot 772, KG 7 Avenue, 5th floor, PO Box 6955, Kigali,
Rwanda; b Addis Ababa University, School of Medicine, Addis Ababa, Ethiopia; c Program in Global Surgery
and Social Change, Harvard Medical School, Boston, MA, USA
* Corresponding author. University of Global Health Equity Kigali Heights, Plot 772, KG 7 Avenue, 5th floor,
PO Box 6955, Kigali, Rwanda.
E-mail address: abekele@ughe.org
is mainly a transudate from systemic vessels that of empyema in LMICs. These risk factors include
supply the parietal pleura. This fluid is important comorbidities (cancer, tuberculosis, malnutrition,
to minimize friction between the 2 pleural surfaces diabetes), immunosuppressants (human immu-
during respiration. The negative pressure inside nodeficiency virus/AIDS, chronic steroid use),
the pleural cavity creates a vacuum that keeps alcohol and intravenous (IV) abuse, and underly-
the airways open at all times.3 ing structural lung disease.6,8,9 The epidemiology
The parietal pleura is innervated by somatic fi- and cause of post-chest tube empyema is usually
bers from the intercostal nerves and by the phrenic underreported in low-resource contexts; howev-
nerves. Hence, it is able to sense the classical er, substandard care for chest tubes after inser-
pleuritic type of pain when irritated.3 However, tion, duration of the chest tube in situ, retained
the visceral pleura is not supplied by somatic hemothorax or chylothorax, and the presence of
nerves and is thus insensitive to pain, touch, or pulmonary contusions increase the incidence of
pressure. The visceral pleura receives its blood post–chest tube empyema.10
supply from the bronchial circulation, and the pari-
etal pleura receives its blood supply from the chest CAUSES
wall. The right and left pleural cavities have no
Thoracic empyemas are always secondary—infec-
anatomic connection.3
tious agents need to get access to the normally
EPIDEMIOLOGY sterile pleural cavity (Fig. 2). Empyemas occur
when infections spread to the pleural cavity from
In the United States, up to 1.5 million cases of the lung, mediastinum, chest wall, diaphragm;
pleural effusion occur yearly.4 China records up from the external environment; or from circula-
to 4684 effusions per million adults.5 Many LMICs tion.11 These infections may be bacterial, viral, or
lack comprehensive data on the local incidence atypical; however, bacterial infections are the
and epidemiology of pleural effusions and empy- most common. Pneumonia is the single most signif-
ema. Epidemiology varies globally based on the icant cause because more than 50% of empyemas
prominent locoregional underlying cause. Both result from infected parapneumonic effusions.12
uncomplicated parapneumonic effusions and Empyema also results from penetrating or blunt
empyema are common at the extremes of age: chest injuries where undrained hemothorax subse-
in the very young and in the elderly.6,7 In addition, quently gets infected.13 One of the most underre-
various risk factors contribute to the development cognized and underreported causes of empyema
Descargado para Anonymous User (n/a) en National Autonomous University of Mexico de ClinicalKey.es por Elsevier en marzo 22, 2023. Para
uso personal exclusivamente. No se permiten otros usos sin autorización. Copyright ©2023. Elsevier Inc. Todos los derechos reservados.
Management of Empyema Thoracis 363
are complications of chest tubes and needle thora- In hospital-acquired infections, methicillin-
centesis procedures.10,14 Pleural infections also resistant S aureus (MRSA) accounts for about 60%
occur after thoracic or esophageal surgery espe- of the cases, whereas gram-negative aerobic organ-
cially if associated with esophageal anastomosis isms account for most of the remainder (37%).15
leak. However, a bronchopleural fistula should be MRSA and a variety of gram-negative organisms
assumed when empyema occurs after thoracic sur- and anaerobes (Klebsiella, Pseudomonas, and Hae-
gery. In addition, mediastinitis, pericarditis, ruptured mophilus sp) are also identified causes in children.
esophagus, pancreatitis, and subdiaphragmatic ab- Other uncommon causes of empyema include
scesses have been identified as causes.12 enterococci, Entamoeba histolytica, and compli-
The exact infectious cause of empyema cannot cated pulmonary Echinococcus granulosus (hydatid
be identified in most cases because culture results cysts).15
are negative in about 40% of aspirates.15 In about Postthoracotomy empyemas are usually caused
13%, cultures are polymicrobial.15 Streptococci by S aureus followed by Streptococcus. However,
are common pathogens. In Africa, Asia, and the delayed empyemas occurring after 14 days of tho-
Middle East, however, Staphylococcus aureus is racotomy and postesophagectomy empyema are
responsible for most (20% to 77%) empyema usually polymicrobial. Fungal empyema (Candida
cases15 and bacteria from the Streptococcus milleri sp) has been described following esophagectomy
group (Streptococcus intermedius, Streptococcus and typically results in high mortality rates.19 Em-
constellatus, and Streptococcus anginosus) are pyema secondary to chest tube insertion from
the predominant organisms cultured in adults with high-income settings suggests an incidence
underlying comorbidities.16 Tuberculous empyema ranging from 1% to 25% with predominantly
is also a very common finding in low-resource set- staphylococcal or streptococcal bacteriology.
tings (up to 29%).15,17 A recent review of 10,241 pa- Very rarely coronavirus disease 2019 can result
tients showed that S aureus is the predominant in loculated empyema.20
cause of pleural effusion in adults globally; howev-
er, there are variations in microbiology according to
the geographic location and setting of infections.15
In children, complicated community-acquired STAGES OF EMPYEMA
pneumonia secondary to Streptococcus pneumo-
niae is the predominant pathogen, and together Over a period of 4 to 6 weeks, the classical
with S aureus are responsible for up to 70% of aer- thoracic empyema passes through 3 stages of
obic gram-positive infections.18 development (Fig. 3).21,22
Descargado para Anonymous User (n/a) en National Autonomous University of Mexico de ClinicalKey.es por Elsevier en marzo 22, 2023. Para
uso personal exclusivamente. No se permiten otros usos sin autorización. Copyright ©2023. Elsevier Inc. Todos los derechos reservados.
364 Bekele & Alayande
Fig. 3. Classical stages of development of empyema thoracis. aClassical features may be masked by antibiotics.
b
Practical treatment options for low-resource settings.
Table 1
Pleural fluid characteristics: Parapneumonic effusion versus empyema
Descargado para Anonymous User (n/a) en National Autonomous University of Mexico de ClinicalKey.es por Elsevier en marzo 22, 2023. Para
uso personal exclusivamente. No se permiten otros usos sin autorización. Copyright ©2023. Elsevier Inc. Todos los derechos reservados.
Management of Empyema Thoracis 365
complete drainage in such situations may require on the affected hemithorax, diminished breath
video-assisted thoracoscopic surgery (VATS) or sounds, and sometimes mediastinal displacement
open thoracotomy drainage. to the opposite side.
Chronic empyema is characterized by a pro-
The Organized (Fibrous) Phase longed history of deteriorating general health sta-
Approximately at 6 weeks, the collected pus be- tus, recurrent and intermittent low-grade fever,
comes very thick pus and the septa become very weight loss, dyspnea, chest tightness and pain,
tough. Granulations start to occur all over the and chronic cough. Examination will reveal a
pleural space, and both the parietal and the chronically sick and malnourished patient with fea-
visceral pleura thicken.21 The thickened pleura tures of respiratory distress. The affected chest
become apparent in radiological imaging. Thick- shows reduced movement with breathing, and its
ening of the visceral pleura and the large amount size may be contracted; intercostal space may
of pus collection result in the collapse of the be narrowed. In some instances, patients may pre-
adjacent lung, and expansion of the lung is sent with empyema necessitans in which an un-
significantly restricted. Thickening of the parietal drained empyema ruptures to the skin.
pleura leads to a frozen chest wall and rib Occasionally, the empyema persists to involve
crowding hence impairing the physiologic chest the ribs giving features of rib chronic osteomyelitis.
wall mechanics during respiration. Thickening Breath sounds may be absent or reduced, and all
of the diaphragmatic pleura can also restrict sorts of respiratory sounds may be present. Clin-
the diaphragmatic movement. If left untreated, ical findings of underlying or associated abdominal
the thickened pleura can become calcified, diseases like pancreatitis, subdiaphragmatic ab-
hence further worsening the restriction to lung scess, and amebic liver abscesses may be
expansion, chest wall mechanics, and diaphrag- present.
matic movement. The pus can spontaneously
burst through the chest wall (empyema necessi- APPROACH TO DIAGNOSIS
tans) and fistulize toward the lung (bronchopleu- The diagnosis of empyema thoracic in low-
ral fistula) or into any of the mediastinal resource countries should be mainly clinical
structures adjacent to it.24 and established by plain chest radiograph and
microscopy, culture, and sensitivity. Hence,
CLINICAL FEATURES practitioners in such situations should have a
Clinical presentation of patients with empyema high index of suspicion when faced with such
depends on the stage of the disease, age of the patients.
patients, associated comorbidities, treatment his-
Needle Aspiration
tory, and the health-seeking behavior of patients.
The symptoms of acute empyema and parapneu- Needle thoracocentesis is a safe bedside proced-
monic effusion are usually similar to those of un- ure that should be performed under sterile tech-
complicated pneumonia, including features of niques, and the use of wide-bore needle is
acute febrile illness, cough, pleuritic chest pain, advised. In some instances, the procedure is
and respiratory distress. However, these symp- important to relieve life-threatening collections un-
toms can be masked or significantly altered in der tension.25 In addition, the procedure should be
cases of partial treatment with antibiotics, in pa- carried out with caution in the presence of uncon-
tients with comorbidities such as immunocompro- trolled coughing, bleeding disorders, and altered
mised patients, and in the elderly. Patients may chest wall anatomy. Image-guided aspiration is
also have a suggestive recent history of tube thor- advised in cases of uncertain fluid locations and
acostomy or thoracotomy. Recent chest trauma minimal volumes. Cellulitis at the potential needle
with gradual worsening respiratory symptoms insertion site and overlying herpes zoster are
and fever is also suggestive. contraindications.
As the pleural fluid collection worsens, the clas- The needle insertion site is typically the mid-
sical pleuritic pain improves; however, the respira- scapular line at the upper border of the sixth or
tory symptoms (cough, respiratory distress), the seventh rib (or at least 1 intercostal space below
fever with a swinging pattern, and the general fea- the top of the effusion if image guided). The
tures of toxemia persist or worsen. A physical ex- preferred site is the triangle of safety. Local anes-
amination will show an acutely sick patient with thesia should be used, and the large needle is
tachycardia, tachypnea, pyrexia, and features of advanced till the pleural space is entered. Aspira-
dehydration. The effusion in the pleural space will tion of pleural fluid or pus is thus attained
be characterized by stony dull percussion notes (Table 2).25
Descargado para Anonymous User (n/a) en National Autonomous University of Mexico de ClinicalKey.es por Elsevier en marzo 22, 2023. Para
uso personal exclusivamente. No se permiten otros usos sin autorización. Copyright ©2023. Elsevier Inc. Todos los derechos reservados.
366 Bekele & Alayande
Table 2
Characteristics of pleural aspirate
Chest Radiograph
Plain chest radiographs are important in the diag-
nosis and follow-up of patients with empyema.26
Posteroanterior views (P/A chest radiograph) are
the most frequently used. However, it should be
noted that a negative P/A chest radiograph does
not rule out the presence of empyema because
the volume of the pleural collection must be
more than 250 mL before becoming detectable
on an erect chest radiograph. A lateral decubitus
view, ultrasound scan, in this case, is sensitive
for collections as small as 50 to 200 mL. In Fig. 4. Posteroanterior chest radiograph from a 37-
contrast, supine chest radiographs can mask large year-old male, showing right-sided pleural collection.
quantities of fluid.26 Arrow shows blunting of right costophrenic angle and
The typical radiologic features include blunting fluid levels.
of the costophrenic and cardiophrenic angles,
presence of fluid within the lung fissures, and a Computed Tomographic Scan
typical air fluid level. In large-volume collections,
The use of CT scan for the diagnosis of pleural col-
a mediastinal shift from the side of the effusion to
lections in low-resource settings is often not
the contralateral aspect can be observed. (Figs.
routine mainly due to unavailability of the CT scans
4 and 5).26
and radiologists in LIC settings, and emphasis
Ultrasound Scan
An ultrasound scan can be used to detect minimal
amounts of fluid, as small as 3 to 5 mL, and is
significantly more sensitive than a plain chest
radiograph. Ultrasound scan is very effective in
guiding aspiration of small pleural volumes and
collections located in unusual sites.26 The ultra-
sound appearance of an empyema depends on
the composition of the collection. Typical findings
are of collections that are not uniformly anechoic
and are often septate.27
However, in low-resource settings), ultrasound
scans may not be considered as a first-line inves-
tigation for thoracic empyema diagnosis but can
be used to define complex collections, or to
make diagnoses especially in the absence of radi-
ography or computed tomography (CT). Therefore,
Fig. 5. Posteroanterior chest radiograph from a 22-
it is imperative that health facilities and institutions year-old male patient taken 6 h after insertion of a
embark on expansion of training programs and chest tube for left-sided empyema. Note the signifi-
increased access to relevant diagnostic devices cant postprocedure pneumothorax, deviation of the
to help overcome the barriers of not having reliable mediastinum to the right side despite the correctly
CT scanning in these settings. placed chest tube, and the trapped lung.
Descargado para Anonymous User (n/a) en National Autonomous University of Mexico de ClinicalKey.es por Elsevier en marzo 22, 2023. Para
uso personal exclusivamente. No se permiten otros usos sin autorización. Copyright ©2023. Elsevier Inc. Todos los derechos reservados.
Management of Empyema Thoracis 367
should be on clinical diagnosis and judicious use 3. Supportive measures to improve patient’s
of plain chest radiographs and ultrasonography. general condition (pulmonary physiotherapy,
However, CT provides the best diagnostic oppor- nutritional support and rehabilitation, correc-
tunity to precisely characterize the location and tion of anemia, and treatment of underlying
stage of the disease.26 CT is also very useful in medical conditions)
the identification of small-volume collections and
the detection of underlying intrathoracic or
Antibiotic Therapy
abdominal pathologic conditions.
Typical findings include an enhancing thickened All patients with thoracic empyema should receive
pleura known as the split pleural sign, which is due antibiotic therapy. The choice of antibiotics is best
to fibrin coating of both parietal and visceral pleural guided by the availability of Gram stain and culture
surfaces and ingrowth of blood vessels.28 Both results.30 In addition, the local antibiotic sensitivity
layers of the pleura are visualized as linear regions and resistance pattern should be used when deci-
of enhancement that meet at the margins of the sions are made.30 When microbiology results are
collection.28 This sign is the most reliable one used not available or take long time to organize, a com-
to distinguish empyema from a peripheral pulmo- bination of third-generation cephalosporin (cefur-
nary abscess. Other findings during CT scan include oxime or ceftriaxone) and metronidazole, or
visible septations, distortion and compression of amoxicillin/clavulanic acid and metronidazole
adjacent lung, associated consolidation, presence should be considered for community-acquired
or absence of gas locules, and adjacent infections empyema.30 In hospital-acquired cases, vanco-
like subdiaphragmatic abscess (Figs. 6 and 7).26 mycin plus meropenem is an appropriate choice.
The selected antibiotics should be administered
PRINCIPLES OF TREATMENT IV and converted to oral antibiotics once patients
are symptomatically well improved (fever
There are 3 objectives in the treatment of thoracic controlled, respiratory rate normalized, feeding
empyema. These objectives include29: well). Antibiotics should also be continued until
1. Control of ongoing infection (sepsis) the chest drainage returns to normal (pus fully
2. Evacuation of infected material from the drained) and the chest tubes are removed. Antibi-
pleural space otics are to be continued for a total duration of
3. Reexpansion of the lung 14 days.30
The aforementioned objectives can be achieved
by: Pleural Space Drainage
1. Appropriate antibiotic therapy with specific
emphasis on selection, route of administra- Surgical interventions used in the treatment of
tion, and duration of treatment thoracic empyema include the insertion of a thora-
2. Drainage of the intrapleural collection costomy tube (chest tube), simple open drainage
(thoracotomy or VATS assisted), thoracotomy
with decortication, and thoracic window
procedures.
CHEST TUBES
The best way to completely drain the pleural space
is by the insertion of a chest tube. Chest tubes are
most effective in the exudative and early fibropur-
ulent stage of the empyema. If available, 10F to
14F Seldinger drains can also be tried as first-
line treatment in simple exudative effusions. How-
ever, larger-sized (28F–32F) chest drains are
preferred.31 The authors discourage the practice
of repeated needle thoracentesis because it rarely
results in a complete evacuation of the pleural
space, is very painful, and predisposes patients
Fig. 6. Coronal section of a chest computed tomo- to complications. In addition, the exudative stage
graphic scan showing left-sided empyema (A) under of empyema is very short and cannot always be
tension associated with almost complete lung collapse detected even during hospital treatment of pneu-
(B), mediastinal deviation to the right (black arrow), monia, hence proper chest tube insertion is more
and depression of the left diaphragm (white arrow). favorable than multiple thoracentesis.25
Descargado para Anonymous User (n/a) en National Autonomous University of Mexico de ClinicalKey.es por Elsevier en marzo 22, 2023. Para
uso personal exclusivamente. No se permiten otros usos sin autorización. Copyright ©2023. Elsevier Inc. Todos los derechos reservados.
368 Bekele & Alayande
Fig. 7. (A,B) Contrast-enhanced axial computed tomographic scan of a young male showing left-sided empyema
with significant collection posteriorly (C), and reduced lung volume (D). Note the chest tube on the left side (ar-
row). Minimal collection on the right side is also noted (arrow).
Descargado para Anonymous User (n/a) en National Autonomous University of Mexico de ClinicalKey.es por Elsevier en marzo 22, 2023. Para
uso personal exclusivamente. No se permiten otros usos sin autorización. Copyright ©2023. Elsevier Inc. Todos los derechos reservados.
Management of Empyema Thoracis 369
The techniques used during surgical interven- It should be noted that the late third stage of the
tion are the evacuation of all necrotic and purulent disease that is associated with a fibrothorax, sig-
materials from the pleural space, decortication or nificant trapping of the lungs and significant chest
peeling of the organized parietal and visceral wall deformity, needs the attention of a thoracic
pleura, and complete separation of the diaphragm surgeon.29,30,37
from the lung. Empyemectomy, or the complete
enucleating of the infected sac, can also be
attempted.29
Descargado para Anonymous User (n/a) en National Autonomous University of Mexico de ClinicalKey.es por Elsevier en marzo 22, 2023. Para
uso personal exclusivamente. No se permiten otros usos sin autorización. Copyright ©2023. Elsevier Inc. Todos los derechos reservados.
370 Bekele & Alayande
Descargado para Anonymous User (n/a) en National Autonomous University of Mexico de ClinicalKey.es por Elsevier en marzo 22, 2023. Para
uso personal exclusivamente. No se permiten otros usos sin autorización. Copyright ©2023. Elsevier Inc. Todos los derechos reservados.
Management of Empyema Thoracis 371
Descargado para Anonymous User (n/a) en National Autonomous University of Mexico de ClinicalKey.es por Elsevier en marzo 22, 2023. Para
uso personal exclusivamente. No se permiten otros usos sin autorización. Copyright ©2023. Elsevier Inc. Todos los derechos reservados.
372 Bekele & Alayande
23. Intrapleural Use of Tissue Plasminogen Activator 31. Porcel JM. Chest tube drainage of the pleural
and DNase in Pleural Infection | NEJM. Available at: space: a concise review for pulmonologists. Tuberc
https://www.nejm.org/doi/full/10.1056/ Respir Dis 2018;81(2):106–15.
NEJMoa1012740. Accessed November 2, 2021. 32. Chest-Tube Insertion | NEJM. Available at: https://
24. Pugh CP. Empyema necessitans a rare complication www.nejm.org/doi/full/10.1056/nejmvcm071974.
of methicillin-resistant staphylococcus aureus empy- Accessed October 25, 2021.
ema in a child. Pediatr Infect Dis J 2020;39(3): 33. Idell S, Rahman NM. Intrapleural fibrinolytic therapy
256–7. for empyema and pleural loculation: knowns and un-
knowns. Ann Am Thorac Soc 2018;15(5):515–7.
25. Havelock T, Teoh R, Laws D, Gleeson F. Pleural pro-
34. Maskell NA, Davies CWH, Nunn AJ, et al. U.K.
cedures and thoracic ultrasound: British Thoracic
Controlled Trial of Intrapleural Streptokinase for
Society pleural disease guideline 2010. Thorax
Pleural Infection. N Engl J Med 2005;352(9):865–74.
2010;65(Suppl 2):i61–76.
35. Raveenthiran V. Empyema thoracis: controversies
26. Hallifax RJ, Talwar A, Wrightson JM, Edey A, and technical hints. J Indian Assoc Pediatr Surg
Gleeson FV. State-of-the-art: Radiological investiga- 2005;10(3):191.
tion of pleural disease. Respir Med 2017;124:88–99. 36. Pediatric empyema thoracis management: should
27. King S, Thomson A. Radiological perspectives in the consensus be different for the developing
empyema: childhood respiratory infections. Br Med countries? - Journal of Pediatric Surgery. Available
Bull 2002;61(1):203–14. at: https://www.jpedsurg.org/article/S0022-3468(19)
30516-0/fulltext. Accessed October 25, 2021.
28. Kraus GJ. The Split Pleura Sign. Radiology 2007;
37. Gupta DK, Sharma S. Management of empyema -
243(1):297–8.
role of a surgeon. J Indian Assoc Pediatr Surg
29. Scarci M, Abah U, Solli P, et al. EACTS expert 2005;10(3):142.
consensus statement for surgical management of 38. Kaufman AJ, Flores RM. Technique of pleurectomy
pleural empyema. Eur J Cardiothorac Surg 2015; and decortication. Oper Tech Thorac Cardiovasc
48(5):642–53. Surg 2010;15(4):294–306.
30. Shen KR, Bribriesco A, Crabtree T, et al. The Amer- 39. Light RW, Macgregor MI, Luchsinger PC, Ball WC Jr.
ican Association for Thoracic Surgery consensus Pleural effusions: the diagnostic separation of tran-
guidelines for the management of empyema. sudates and exudates. Ann Intern Med 1972;77(4):
J Thorac Cardiovasc Surg 2017;153(6):e129–46. 507–13. Unpublished others.
Descargado para Anonymous User (n/a) en National Autonomous University of Mexico de ClinicalKey.es por Elsevier en marzo 22, 2023. Para
uso personal exclusivamente. No se permiten otros usos sin autorización. Copyright ©2023. Elsevier Inc. Todos los derechos reservados.