466 Journal of the Royal Society of Medicine Volume 87 August 1994

Section Meetings Management of empyema thoracis

John A Odell ChB FRCS(Ed) Department of Cardiothoracic Surgery, Mayo Clinic, Rochester, MN 55905, USA

Keywords: empyema thoracis; drainage of empyema; decortication loculation, particularly posteriorly. The pleural fluid Paper read to pH and glucose level become progressively lower and Cardiothoracic Definitions the LDH level increases. In the third or organizational Section, An empyema thoracis is simply a collection of pus stage, fibroblasts grow into the exudate from both the 27 May 1993 in the pleural space. Some have tried to define it visceral and parietal pleural surfaces to produce an differently, but this is unnecessary; many term a inelastic membrane called the pleural peel or cortex. parapneumonic effusion associated with bacterial pneumonia, lung abscess, or bronchiectasis an Historical empyema whereas others state that only para- perspective pneumonic effusions with positive pleural fluid cultures can be called an Likewise, others Those cases of empyema or dropsy which are treated by empyema1. incision or the cautery, ifthe water or pus flows rapidly all use the term 'complicated parapneumonic effusion' at once, certainly prove fatal. to refer to those effusions that do not resolve without When empyema is treated either by the cautery or incision, tube thoracostomy'. Another term that is frequently if pure and white pus flow from the wound, the patients used, particularly in regions where tuberculosis is recover, but if mixed with blood, slimy and fetid they die. common, is the term 'tuberculous empyema'. However, Hippocrates2 we do not normally classify a straw-coloured effusion from which tubercle bacilli are isolated as an Cardiothoracic surgery probably began with the empyema, nor do we often find thick caseous management of empyema. Most empyemas were tuberculous pus within the pleura (this is invariably associated with pulmonary infection and sometimes a tuberculous lobar pneumonia which has been became obvious when pus discharged spontaneously intubated percutaneously because of difficulty in from the chest wall (an empyema necessitans or radiographic interpretation). What is frequently necessitatis or, in modem terms, a pointing empyema). meant by a 'tuberculous empyema' is a bacterial Those early physicians involved with medical empyema complicating active or previous tuberculosis. treatment determined the exact site for surgical An empyema may be associated with positive drainage by establishing the maximal site ofpain, or bacterial cultures or may even be sterile. The by smearing the chest with potters clay. The site that diagnosis does not require any complicated tests such dried first, the hottest and most inflamed, was chosen as glucose, LDH, pleural pH or leukocyte count (it is then as the site of drainage. Early chest drains used obvious to the naked eye!). If reliance on laboratory were hollow reeds. investigations influences management then patients Hippocrates described drainage of an empyema and with rheumatoid pleurisy, tuberculosis, malignancy he recognized the smell of anaerobic infection and or lupus pleuritis may be inadequately managed by its association with a poor prognosis2. The Greek intercostal drainage. The only investigations necessary physicians at that time had advanced the techniques are fluid and, if obtained, a pleural biopsy, sent of managing empyema to include early diagnosis, for bacteriological and histological examination. irrigation and placement of an indwelling tube. These Occasionally chylothorax, because ofits appearance, techniques became the standard of care for over two can be confused with empyema but this condition millennia. usually occurs in specific circumstances. Little therapeutic progress beyond open drainage The confusion in terminology probably is a result was made until the 19th century, when needles to of the stages in evolution of any empyema. The first locate and aspirate an empyema were developed3, stage is an exudative phase in which a focus of and drainage of the chest with an underwater infection adjacent to the visceral pleura leads to seal was introduced4. It was soon realized that increased permeability ofthe visceral pleura and the drainage was sometimes more effective after resection accumulation of a small usually sterile parapneumonic of a portion of rib. Thoracoplasty as a form of effusion. The pleural fluid is an exudate in which treatment for empyema was pioneered5; and the leukocytes may be found. For those who investigate, operation ofdecortication, which was discovered almost the glucose is normal as is the pH. Occasionally, the by accident6, was further developed7. Decortication septic lung focus adjacent to the pleura may rupture enjoyed a vogue after the First World War, only to directly into the pleural space; if it communicates fall into disuse until revived during the Second World with a bronchus a broncho-pleural fistula develops. War8'9. Only with the introduction ofbasic anaesthetic The second stage, the fibrinopurulent stage, is techniques, an understanding ofthe dangers of an open characterized by a much larger fluid collection which pleural cavity that had not been made rigid by fibrin is obviously pus (it contains many polymorphonuclear deposition and the use of antimicrobial therapy did leukocytes, bacteria and cellular debris). Ofimportance real progress in the management of empyema occur. is a tendency for fibrin to be deposited on both the One surgeon, Evarts Graham, stands as one of visceral and parietal pleura and a tendency for those, who advanced considerably our understanding Journal of the Royal Society of Medicine Volume 87 August 1994 467 of empyema' "'. In 1918 he was appointed to the US Management Army Empyema Commission which was charged to The patient with an empyema may have variable investigate the high mortality, averaging 30.2%, but symptoms difficult to distinguish from those of the ranging as high as 70% or more, in camps where open primary provocation, whether this be 'pneumonia', drainage was standard practice. He defined the mediastinitis, subphrenic abscess or posttraumatic difference between pneumococcal and streptococcal haemothorax. He may be virtually asymptomatic or empyema: pneumococcal empyema tended to occur may be frankly toxic, depending upon the causal late in the course of pneumococcal pneumonia organisms, the volume ofpus within the pleural space and be associated with thick and creamy pus and the host defence mechanisms. Other features whereas streptococcal empyema occurred earlier in result from occupation ofthe pleural space: dyspnoea; the phase ofthe disease when the pleural exudate was diminished movement of a hemithorax; dullness to serofibrinous. percussion; diminished breath sounds; and, if the Early open drainage as practised at that time empyema is large, displacement of the mediastinum frequently led to collapse of the lung from pneumo- to the opposite side. thorax which, superimposed upon pneumonia, was The patient with a bronchopleural fistula gives a often fatal. When the principles Dr Graham elucidated distinctive history - whenever he lies on the side were applied by the Empyema Commission, the opposite to the empyema he coughs excessively and mortality was reduced to 3.4%. The essential points the volume of pus produced is frequently large. The ofthese new principles were: (1) careful avoidance of patient with a pointing empyema characteristically an open pneumothorax in the acute stage: (2) the has a discharging sinus or a chest wall swelling that prevention of a chronic empyema by the rapid may be confused with an abscess. Most pointing sterilization and obliteration of the infected cavity; empyemata are associated with tuberculosis: if and (3) careful attention to the nutrition ofthe patient. associated with trauma or previous chest surgery this may occur at any site where the chest wall Aetiology of empyema was previously breached. The patient with an An empyema follows infection of the structures amoebic empyema usually has a painful tender surrounding the pleural space; an infection solely of liver. the pleural space probably does not occur. A relatively asymptomatic patient may be referred In the lung, empyema commonly follows pneumonia with an opacity on the chest radiograph that raises but may also be associated with lung abscess and the possibility of empyema, but the differential bronchiectasis. Lung abscess usually elicits an diagnosis may include pleural tumor, pulmonary inflammatory pleuritis over the adjacent pleura that tumor or even hydatid disease. Occasionally, pus obliterates the pleural space and lessens the may be loculated (encysted, fissural, mediastinal, likelihood of empyema, but, if the lung abscess subpulmonary). The appropriate first investigation in is particularly acute and the organisms virulent, this patient is ultrasound or computerized tomography the abscess may rupture into the pleural space (CT) examination to determine as far as possible the before obliteration has occurred, producing a pyo- nature of the opacity. Hydatid disease is obvious: it pneumothorax or empyema. In the vast majority of has a density approximating water: a tumour has a patients with bronchiectasis the pleural space is solid density; an empyema is ofvariable density and also obliterated but there are exceptions and in this a fluid component is usually present. Recently using situation empyema is possible. In both bronchiectasis CT examination attenuation in the extrapleural and lung abscess an empyema can develop on the tissues has been described in association with contralateral side presumably because ofaspiration of empyemal7 8. Occasionally, by CT or ultrasound, it pus and the development of a subpleural pneumonia. is impossible to differentiate tumor from empyema In some communities trauma is the most frequent and some clinicians would aspirate at this point to cause of empyema. During the First World War obtain a diagnosis; others would proceed direct to and the early part ofthe Second World War empyema thoracotomy if the patient was fit and the tumour occurred in 25-30% of all thoracic casualties but thought resectable. decreased to 6% among thoracic casualties in Some assessment ofthe underlying lung is essential Vietnam12"13. The frequent finding of resistant if major surgery such as decortication is planned. organisms in empyema fluid that follows chest An investigation frequently undertaken previously, trauma suggests that this may be associated with in the relatively asymptomatic patient with a poor techniques of chest intubation rather than a radiographic opacity compatible with an empyema, contaminated weapon. or patients who have had an empyema previously An empyema may be associated with infection drained, was bronchography. It was argued that below the diaphragm (a liver abscess, either pyogenic decortication of an empyema would be inappropriate or amoebic, or a subphrenic abscess). Interestingly, and unsuccessful ifthe underlying lung was abnormal empyema does not result in subdiaphragmatic and bronchiectatic: the patient would still be at risk infection, probably because ofthe cranial direction of of the complications of bronchiectasis and more the lymphatics and the negative intrathoracic pressure importantly the underlying lung would not readily compared to the abdominal cavity. expand and obliterate the space after decortication. The Mediastinal infection may result in an empyema. correct operation in these circumstances is pulmonary The most common example is rupture of the resection plus decortication. Although in theory this is oesophagus. The patient usually has a characteristic the right approach there are disadvantages. If the history and clinical signs, but occasionally patients opacity is large and dense interpretation of a broncho- are seen late in the disease and the diagnosis only gram may be impossible and, sometimes the bronchi suspected after food contents are drained from the are so crowded together that the presence of normal pleural space. Mediastinitis and empyema may also or bronchiectatic lung cannot be excluded. Today follow infections of the head and neck'4-'6. the concern about bronchography no longer prevails 468 Journal of the Royal Society of Medicine Volume 87 August 1994

because a suitable bronchographic agent no longer Open drainage of an empyema does not exclude the exists. The manufacture ofDionisol has been stopped patient from later management by decortication if and bronchography can no longer be done safely. CT the patient's condition improves. scanning is said to be adequate for the diagnosis of The underlying cause of the empyema should be bronchiectasis but one requires expensive equipment, treated at the same time as the empyema. Pneumonia an experienced radiologist who needs to take multiple usually responds to appropriate antibiotics. A lung fine cuts ofthe lung and who understand the bronchial abscess in association with an empyema requires anatomy. CT scanning of the chest therefore should separate drainage ofthe abscess and empyema. This be considered prior to decortication, if the aetiology is usually done as an open procedure. A soft de Pezzar of the empyema could possibly be bronchiectasis or drain is placed in the centre of the abscess and the lung abscess. All too frequently the surgeon is told pleura separately drained19. The abscess usually that underlying bronchiectasis is present but not the decreases in size quite rapidly. Bronchiectasis should distribution of bronchiectasis. The procedure has be resected at the same time as decortication, or if become analogous to exercise testing in ischaemic total unilateral bronchiectasis is present a heart disease: one can prove it exists but the surgeon pneumonectomy should be performed through the does not know which vessel to graft. empyema space20. This rather radical procedure In the majority ofpatients the diagnosis is obvious. offers the only chance ofcure: although postoperative The patient is ill and pyrexial, he may have a empyema is likely, it is not inevitable20. Subphrenic productive cough, a leucocytosis and chest pain. collections of pus should be separately drained. The chest radiograph is, in the vast majority, Oesophageal rupture can be managed using various characteristic- a posterior D-shaped opacity that methods, the discussion ofwhich is outside the scope invariably reaches the hemidiaphragm. The diagnosis of this article. The empyema cannot be cured unless is confirmed by needle aspiration at the site deter- the oesophageal leak is controlled. Wide drainage of mined by the chest radiograph. The finding of the mediastinum and dependent drainage of the 'anchovy sauce' pus, caseous material, a draining pleural space through a thoracotomy is usually sinus, orpus that contains sulphurgranules may suggest necessary. the diagnosis ofamoebic, tuberculous, or actinomyces with the need for special culture techniques or other Drainage investigations. Drainage, whether closed or open should be done at Any delay in the correct management of empyema the most dependant site of the empyema collection. may lead to prolonged hospitalization and morbidity: The exact site may be determined after the installation the later the stage ofthe empyema, the more difficult of oily Lipiodal into the empyema cavity. Invariably and prolonged it is to treat. Too much reliance this is at the angle of the eighth or ninth rib on antibiotics and aspiration rather than well posteriorly. The technique of drainage is well established principles, in the belief that this avoids described by Le Roux et al.19. 'painful and dangerous' surgical interventions, may, If a visceral fibrin layer has not formed, exposure in fact, worsen the situation. of the empyema cavity to atmospheric pressure will Further management depends upon the consistency result in collapse of the underlying lung. This of the pus and the state of the patient and is shown possibility must be considered at the time of rib diagrammatically in Figure 1. If the pus is thin a resection. If movement of the underlying lung is large closed intercostal drain is inserted. If the pus present the 'open drain' must be converted to a closed is thick fibrin and pus will not drain effectively, then system by suturing the skin layers closed around the either rib resection (open drainage) or decortication drain. It may later be converted to an open system is necessary. What determines whether the patient within a few days, once a fibrin layer has formed. should have a decortication or a rib resection depends Drains are removed only when drainage is minimal upon the state of the patient. A toxic ill patient, and obliteration of the pleural cavity as judged by and included in this category is the patient with a serial chest radiographs and the use ofsinograms has broncho-pleural fistula, and the patient obviously occurred. In patients drained during the exudative unfit for major surgery is managed by open drainage. phase, obliteration occurs within days. In those patients drained later, this takes longer. In adult patients with a thick restrictive cortex managed only EMPYEMA by open drainage, obliteration ofthe empyema space may take 3 months or longer2'. In children ASPIRATE CXR ?EMPYEMA obliteration occurs more rapidly and is measured in THIN PUS Thick pus I weeks. Obliteration takes place by adherence of / 4 CT OR BR'OGRAPHY the parietal and visceral cortex at the periphery ofthe ICD Open drain empyema space and the formation of granulation tissue. Once the two layers of fibrin are adherent CURE * FEVER DECORTICATION/ absorption ofthe fibrin takes place. Despite good open * PL OPACITY PULMONARY RESECTION drainage, the space may become loculated during Unfit healing and exudate trapped may cause recurrence Large space of symptoms of infection. * Small space CURE The patient initially managed by closed intercostal Perm. OD I drainage usually improves dramatically within 24 Conservative Mx. to 48 h. If his clinical condition does not improve Figure 1. Flow diagram demonstrating how empyema is and ifthe chest radiograph demonstrates incomplete managed. CXR= Chest X-ray; ICD= intercostal drain; CT= evacuation ofpleural pus, possibly because ofloculation computerized tomography; Br'ography=bronchography; PL= or fibrin formation the patient may require rib pleura; Perm. OD=permanent open drain; Mx= mix resection and open drainage. In patients with multiple Journal of the Royal Society of Medicine Volume 87 August 1994 469 pleural fluid levels, 'the disorganized pleural space' in a patient with a long-standing empyema associated management is best done by an open procedure as with crowding of the ribs and scoliosis. In these loculi and adhesions need to be broken down. patients, the parietal cortex may inhibit chest wall There is a group of patients including, the elderly movement and expansion of the decorticated lung. unfit patient with a large empyema space or the patient Ifdecortication fails and the lung does not expand to with a calcified empyema, in whom management is fill the pleural space an open drainage procedure and best suited by the creation ofa permanent open drain conservative management is pursued. In these patients (Eloesser flap)22. In this procedure flaps are created the underlying lung is likely to be abnormal and in order to line the drainage tract with skin. This should be carefully reassessed. Repeat decortication obviates the need for chest tubes to maintain patency is seldom worth while. ofthe drainage tract and prevents premature closure. There is considerable debate, particularly, of the correct management of childhood empyema, con- Antibiotic therapy cerning the merits ofearly decortication versus open Although antibiotic therapy has definitely improved drainage32. Many believe that postoperative hospital the outlook ofpatients with empyema the principles of stay is reduced ifearly decortication rather than open treatment that were learned by hard-won experience drainage is performed. Using the approach advocated in the preantibiotic era should not be forgotten. management does not involve a choice: those that are Reliance on antibiotics may in fact delay appropriate fit are managed by decortication; those unfit or ill are surgical intervention and prolong morbidity. managed by a drainage procedure. In children, rapid Aminoglycosides concentrations are not detected in defervescence rapidly follows drainage and the child pleural pus after systemic administration either can often be discharged within a week or two. It must because they do not penetrate the blood-pleural be appreciated that radiographic improvement lags barrier in empyema or are bio-inactivated by the behind clinical improvement and the temptation to pleural pus23'24. It is possible that this situation continually seek radiographic improvement by physical exists with other antibiotics. Ciprofloxacin, however, means must be resisted. has been shown to penetrate the pleural space easily and achieve concentrations well above the MIC90 of Other surgical options most pathogens normally associated with empyema25. Empyectomy The prime object of management is therefore This refers to a specific manoeuvre - the complete drainage of the pus. If this has been adequate there excision of a small empyema without spillage ofpus. is little need for long-term antibiotic therapy. A previous drainage procedure or the presence of a Antibiotics are used until defervescence has occurred broncho-pleural fistula precludes this operation. (usually within a week) and as perioperative cover Operative details have been well described by Dugan during a surgical procedure. The selection of the and Samson3. Dissection is begun in the extrapleural appropriate antibiotic is based on the Gram stain of plane and when the edges of the empyema sac are pleural fluid, culture ofaspirated fluid or sputum and reached, the surgeon 'turns the corner' and then of the likely organism if cultures or Gram stain are decorticates the inner surface of the empyema from unhelpful. In the intervening period while awaiting the visceral pleura. Dissection is particularly difficult results a broad spectrum antibiotic effective against over the diaphragm where the endothoracic fascia is anaerobes and aerobes should be used. thin and the extra pleural plane poorly developed. There are isolated reports of the instillation of antibiotics26, antiseptics27'28 and streptokinasel,21930 Microvascular free muscle flaps into the empyema space: presently there is no general There are patients in whom multiple previous agreement on their use. operations to deal with a chronic empyema, usually with a broncho-pleural fistula, have failed. Under Decortication normal circumstances the use ofa muscle flap would This procedure involves a full thoracotomy with be considered but if the local muscles have been removal ofall pus and fibrous tissue from the visceral divided at previous thoracotomies, these muscles are pleura. It is a major procedure and should not be fiequently small and atrophied. In these cimcumstances performed on patients who are debilitated, either from Chen et al.34 have used microvascular free muscle the empyema, the underlying pathological process or flaps. Contralateral latissimus dorsi and the lower four age. In patients with post traumatic empyema it can digitations of serratus anterior are mobilized on the safely be assumed that the underlying lung is, in the same vascular pedicle, namely the thoracodorsal artery vast majority, normal. In other patients the underlying and vein. These muscle flaps are then anastomosed to lung should be assessed by CT scanning to exclude the remnants ofthe thoracodorsal artery and vein on bronchiectasis or lung abscess. Ifthere is bronchiectasis the affected side. He states these vessels are easily this should be resected at the same procedure. A rigid found39. His results in his small series are excellent. bronchoscopy is done at the induction ofanaesthesia The fistula is closed and the empyema space is to exclude an empyema complicating a foreign body obliterated. or a malignant tumour obstructing a lobar of main stem bronchus. If a tumour is observed it is best to 'Clagett' open-window thoracostomy abandon the procedure and carefully reevaluate the An option that may be considered in patients unwilling patient. or unable to cope with a permanent open drain, in It is not necessary to remove the parietal pleura at whom decortication is undesirable or unsuccessful, decortication as the underlying lung more readily fills is the procedure initially described by Clagett the space and the parietal pleural peel absorbs with and Geracim for management ofpostpneumonectomy time31. Removal of the parietal cortex, especially if empyema. The same principles may be used for chronic, may be associated with excessive bleeding. patients with an empyema who have had a limited There are exceptions: the parietal cortex is removed or no previous pulmonary resection. Results appear 470 Journal of the Royal Society of Medicine Volume 87 August 1994

to be better compared to a postpneumonectomy 19 Le Roux BT, Mohlala ML, Odell JA, Whitton ID. group36. Suppurative disease of the lung and pleural space. Part I: empyema and lung abscess. Curr Problems Surg Thoracoplasty 1986;23:4-89 The purpose ofthoracoplasty is to remove the rigidity 20 Odell JA, Henderson BJ. Pneumonectomy through an empyema. J Thorac Cardiovasc Surg 1985;89:423-7 of the outer chest wall and so establish contact 21 Bartlett JG, Finegold SM. Anaerobic infections of the between the now flexible chest wall and either lung and pleural space. Am Rev Respir Dis residual lung; or, after pneumonectomy, with the 1974;110:56-77 mediastinum in order to obliterate the empyema 22 Eloesser L. Recollections: Ofan operation for tuberculous space. The procedure is rarely undertaken today empyema. Ann Thorac Surg 1971;11:210 because ofthe deformity that results and the success 23 Thys JP, Vanderhoeft P, Herchuelz A, Bergmann P, of other forms of management. Yourassowsky E. 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