British Medical Bulletin

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British Medical Bulletin 61:203-214 (2002)
© 2002 Oxford University Press

Radiological perspectives in empyema

Childhood respiratory infections

Susan King^* and Anne Thomson

^* Department of Paediatric Radiology, Bristol Royal Hospital for Children, Bristol, UK
Department of Paediatric Respiratory Medicine, John Radcliffe Hospital, Oxford, UK

	Abstract

Top Footnotes Abstract Introduction The clinical perspective Radiation hazards of thoracic... Chest radiography Fluoroscopy Ultrasound Computed tomography Magnetic resonance imaging (MRI) Follow-up imaging Conclusions Key points for clinical... References

 
Empyema is a common cause for hospital admission in children. For years, clinicians have relied on chest X-rays to aid diagnosis and monitor treatment. New imaging techniques, particularly ultrasound, have helped in planning the management of children with empyema. Other cross-sectional radiological investigations are useful in a small proportion of children with complicated disease. The mainstays of imaging in the vast majority of children with empyema are chest radiography and ultrasound.

	Introduction

Top Footnotes Abstract Introduction The clinical perspective Radiation hazards of thoracic... Chest radiography Fluoroscopy Ultrasound Computed tomography Magnetic resonance imaging (MRI) Follow-up imaging Conclusions Key points for clinical... References

 
Empyema is defined as pus in the pleural cavity and has significant clinical morbidity¹. Most empyemas in childhood follow acute bacterial pneumonia. Rarer causes include spread from other sites of sepsis such as from septic emboli, lung abscess, subphrenic abscess, osteomyelitis of a rib, or as a result of a missed inhaled foreign body. Recently, some centres in North America and Europe have seen a rise in the incidence of empyema in children^2,3. The reasons for this are unclear, but this trend has not been seen everywhere. A recent study from Liverpool reviewing children with empyema over the previous 20 years showed no increase in the number of cases over this period⁴.

The diagnosis of empyema is made when the pleural fluid is purulent, organisms are detected on Gram stain or when the fluid has a white blood cell count of greater than 5 x 10⁹ cells/l^5,6. When empyema develops, there is both increased production and decreased absorption of pleural fluid. Fibrin is deposited at re-absorption sites due to both a decrease in the normal function of fibrinolytic pathways and an increase in fibrin production⁷.

Amongst clinicians, there is much debate and little consensus about how best to manage children with empyema. Some favour early thoracotomy and decortication of the lung, whilst others advocate conservative management with antibiotics and closed tube drainage. Recently, intrapleural fibrinolytic agents (urokinase and streptokinase) have been used to facilitate closed tube drainage.

Video-assisted thorascopic surgery has emerged as another treatment option for children with empyema^8–10.

There is considerable uncertainty about how to use radiology in the management of empyema in children. Imaging is required to assist the diagnostic process, and chest radiography is the initial examination to confirm the presence of pleural fluid. Increasingly, clinicians request further imaging to determine the size, site, and consistency of the pleural fluid including the presence of loculations and to assess movement of the underlying lung. The radiology department can also help plan further management of the child after the initial chest X-ray and monitor treatment with chest X-rays and cross-sectional imaging techniques, particularly ultrasound. Radiologists may be able to help guide aspiration of pleural fluid or locate the best place to insert a catheter or chest drain.

There has not been consensus on the type or sequence of imaging investigations after the initial chest X-ray and practice varies between centres and countries. Unfortunately, there is little good evidence available about how best to use radiological investigations in children with empyema. Local differences in access to the various imaging techniques and availability of paediatric radiology expertise causes variations in practice.

The aims of this review are to summarise the imaging investigations in children with empyema, provide an overview of the risks and benefits of these techniques, and discuss the appearances of empyema on imaging studies. We will deal with chest radiography, fluoroscopy, ultrasound, computed tomography (CT) and magnetic resonance imaging (MRI).

	The clinical perspective

Top Footnotes Abstract Introduction The clinical perspective Radiation hazards of thoracic... Chest radiography Fluoroscopy Ultrasound Computed tomography Magnetic resonance imaging (MRI) Follow-up imaging Conclusions Key points for clinical... References

 
The way clinicians use the radiology department varies between centres depending on many factors as mentioned in the previous section. We will discuss the approach used by one of us (AT) to manage children with empyema in Oxford, UK.

The child presents febrile and unwell with unilateral chest signs. The first investigation is a plain chest radiograph, which reveals a pneumonic process and a pleural based collection. If the collection is small, the child has a short history and has not had effective antibiotic treatment, it may be sensible to treat and wait 24 h. Most pneumonias ± parapneumonic effusions respond rapidly to antibiotic therapy. If the effusion is moderate-to-large or the child has been unwell for some days with a spiking fever despite antibiotic treatment, the effusion should be drained. Ultrasound of the chest is generally performed before the empyema is drained to assess the size and consistency of the pleural fluid and mark an appropriate site for drainage.

We place a small percutaneous catheter with the child under sedation. This can be done under ultrasound guidance. A repeat chest X-ray may be obtained after catheter insertion. The catheter is placed on negative pressure suction and we routinely use a fibrinolytic agent (urokinase) instilled intrapleurally, twice daily.

Further radiology depends on patient progress, but most commonly a repeat chest X-ray is performed around day 3–4. By this stage, there has been significant drainage and the patient is often apyrexial. Once the child's temperature has been normal for 24 h, the catheter is removed, they start oral antibiotics, and are allowed home. A chest X-ray is often performed before discharge from hospital and is likely to show pleural shadowing and considerable residual lung disease. Follow-up chest X-ray is at 3 months and generally shows complete resolution even in those with substantial pleural abnormality at discharge.

In more complicated cases where the child remains pyrexial beyond 3–4 days, a repeat ultrasound may be requested to demonstrate the size of the residual collection, whether there is an isolated loculated component to the fluid and, if possible, whether the drain is sited appropriately. Computed tomography (CT) is used very rarely in < 2% of children treated in Oxford for empyema.

Of 61 consecutive patients (1996–2001) treated as described above, the median length of hospital stay following drainage was 5 days. None required CT or thoracotomy. One child was re-admitted with a fever spike, which resolved in 36 h with antibiotic treatment and all made complete clinical and radiological recovery. The capacity for healing and remodelling is remarkable in children and may have been underestimated in the past.

Clinical practice and the treatment options available vary between centres, but the following discussion aims to show how clinicians can use radiology to help them make management decisions.

	Radiation hazards of thoracic imaging

Top Footnotes Abstract Introduction The clinical perspective Radiation hazards of thoracic... Chest radiography Fluoroscopy Ultrasound Computed tomography Magnetic resonance imaging (MRI) Follow-up imaging Conclusions Key points for clinical... References

 
Radiation dose to children is a particular concern for paediatric radiologists. Increasingly, parents are worried about radiation hazards and frequently ask staff in radiology departments about risks their child faces from having radiological procedures. Radiation hazards arise when we perform imaging investigations that use ionising radiation. For children with empyema these are chest radiography, fluoroscopy and CT.

We are concerned about two main biological effects of ionising radiation called deterministic effects and stochastic effects. Deterministic effects are those in which the number of cells lost in an organ or tissue is so great that there is loss of tissue function¹¹. Examples of deterministic effects include skin erythema and ulceration. They are not usually a concern for children being investigated for empyema because the radiation dose delivered is not high enough to cause them. However, radiologists and others have recently expressed concerns about radiation doses from the new multislice CT scanners which are higher than the previous generation of helical CT scanners¹².

Stochastic effects are more important than deterministic effects in paediatric radiology and occur if an irradiated cell is modified rather than killed and subsequently goes on to reproduce. This may result in a cancer developing after a variable length of time, known as the latent period. Stochastic effects are particularly important in children because potentially they have a long life-time ahead of them that may exceed the latent period.

Paediatric radiologists make every effort to keep radiation doses to children as low as possible to minimise the risk of harmful biological effects. Wherever possible, we use imaging techniques that employ non-ionising radiation such as ultrasound and magnetic resonance imaging (MRI).

	Chest radiography

Top Footnotes Abstract Introduction The clinical perspective Radiation hazards of thoracic... Chest radiography Fluoroscopy Ultrasound Computed tomography Magnetic resonance imaging (MRI) Follow-up imaging Conclusions Key points for clinical... References

 
For many years, chest radiography was the only imaging technique available to investigate children with suspected empyema. Chest X-ray cannot diagnose empyema, only the presence of parapneumonic fluid. This is because it is only possible to see structures containing air, bone/calcium, soft tissue/fluid and fat on a chest radiograph. Soft tissue and fluid will appear the same on a chest X-ray, and, for example, tumour of the pleura can mimic a pleural effusion. A meniscus sign and movement of the pleural opacity with change in posture of the child indicates that the opacity is due to presence of fluid.

Although pleural fluid can be diagnosed on chest X-ray, this test cannot identify the type of fluid present.

Radiographically, empyema appears as pleural fluid that is usually unilateral. When there are bilateral effusions, the infected side is much larger⁶. An effusion that is not loculated has homogeneous opacity, changes in position with change in posture of the child and has a meniscus sign. Loculated effusions are defined as effusions that do not shift freely in the pleural space and occur in children with empyema when there are adhesions between the visceral and parietal pleura⁵. If the fluid is loculated, very purulent or contains particulate material, there is very little change in the X-ray appearances of the fluid with changes in the child's position (Fig. 1).

View larger version (118K): [in this window] [in a new window]   Fig. 1 Loculated fluid has a fixed appearance on a frontal chest X-ray. The appearances were unchanged on a decubitus chest X-ray.

 
Loculated effusions can appear confusing on chest X-ray and may be difficult to distinguish from a peripheral lung abscess. Loculated fluid appears lenticular in shape and the opacity has a different appearance on frontal and lateral chest radiographs. Helpful radiographic signs of loculated pleural fluid on chest X-ray include incomplete layering on decubitus films, scalloped effusion contours and fixed apical fluid¹³.

Pleural based opacities form obtuse angles with the chest wall^6,14,15, whereas a lung abscess is usually round, appears the same shape on X-rays taken at right angles to each other and forms an acute angle to the chest wall (Fig. 2). Free pleural fluid accumulates in the apex of the chest in supine patients because this is the most dependent part of the thorax¹⁶ and is sometimes seen in small babies and infants when X-rays are obtained with the child in the supine position. However, a more common radiographic finding of fluid in the pleural space in the smallest children is a homogeneous increase in opacity over a hemithorax without blunting of the costophrenic angle or a classic pleural based shadow.

View larger version (141K): [in this window] [in a new window]   Fig. 2 Lung abscess in the right upper lobe forms an acute angle with the lateral chest wall.

 
We do not perform a lateral chest X-ray routinely in children with empyema although some centres outside the UK do. Sometimes, a lateral view can be helpful when trying to differentiate between pleural and intrapulmonary shadows.

Chest radiography carries a radiation burden but the radiation dose of a chest X-ray is small (0.02 mSv) equivalent to 2–3 day's exposure to background radiation. The advantages of using radiography are that it is readily available, simple to perform, cheap, convenient and reproducible. The benefits from having the investigation unquestionably outweigh the risks of radiation exposure in most instances.

	Fluoroscopy

Top Footnotes Abstract Introduction The clinical perspective Radiation hazards of thoracic... Chest radiography Fluoroscopy Ultrasound Computed tomography Magnetic resonance imaging (MRI) Follow-up imaging Conclusions Key points for clinical... References

 
As it is a dynamic investigation, fluoroscopy has some advantages over plain radiography. It can be used to differentiate free pleural fluid from loculated fluid and look for a lung abscess.

Fluoroscopy has been used successfully to guide percutaneous catheter placement for drainage of acute empyema in adults and children^17,18, and can be very helpful to guide re-positioning of suboptimally placed chest drains.

Fluoroscopy, after administering contrast medium into the pleural space, has been used with good results for diagnosing bronchopleural fistula in adults¹⁹ and is probably underused in children when this complication is suspected. The radiation dose from a fluoroscopic examination is considerably less than the dose from CT, the alternative method of looking for bronchopleural fistula. Movement of the lung underlying empyema may be assessed fluoroscopically but ultrasound is generally used in preference because it is easy to perform and does not have a radiation burden.

	Ultrasound

Top Footnotes Abstract Introduction The clinical perspective Radiation hazards of thoracic... Chest radiography Fluoroscopy Ultrasound Computed tomography Magnetic resonance imaging (MRI) Follow-up imaging Conclusions Key points for clinical... References

 
The aims of imaging following chest X-ray in children with suspected empyema are to demonstrate whether pleural collections are clear or complex, look for septations or loculations and assess the thickness of any pleural rind. Some assessment of the underlying lung is also desirable.

The appearances of empyema on ultrasound probably represent different stages of the disease process. Anechoic or hypo-echoic, non-septated fluid precedes hyperechoic fluid and later on septations or loculations develop. This may correlate with progression of empyema from the exudative to fibrinopurulent stage when increasing fibrin deposition causes formation of septations and loculations in the pleural fluid and a rind or peel on the pleural surface^20,21. Septations, loculations and thickness of the pleural rind are easy to assess on ultrasound. The underlying lung can also be assessed in real time for consolidation, collapse and movement with respiration (Fig. 3).

View larger version (103K): [in this window] [in a new window]   Fig. 3 Sagittal ultrasound demonstrates echogenic pleural fluid (P) and collapse of the lower lobe (L). D, diaphragm, A, aerated lung.

 
Ultrasound has many advantages as an imaging technique, the most important being using non-ionising radiation and providing a dynamic assessment of the chest. In addition, ultrasound is freely available, cheap and easy to perform and can be carried out at the bedside. It is generally well-tolerated by children and is often performed with the child in the sitting position. This is often necessary when follow-up ultrasound is performed with a chest drain in situ. In addition, the child can be examined supine to look for free movement of pleural fluid.

Some workers have found ultrasound to be an effective method of assessing disease severity, predicting outcome and planning treatment^8,22,23. The study by Shankar et al²² included children and indicated that percutaneous drainage of empyema without using fibrinolytic agents had the best chance of success when the fluid was anechoic and was least likely to succeed when the fluid was complex and septated.

In their study of empyema in children, Shankar et al⁴ used the presence of loculated pleural fluid on ultrasound to determine which patients required a thoracotomy.

In contrast, ultrasound findings did not affect outcome in a recent randomised trial of intrapleural urokinase therapy in children with empyema²⁴, and was unhelpful in predicting the stage of pleural infection in adult patients²⁵.

Several authors have found that ultrasound lacks specificity in differentiating solid from cystic areas in the pleural cavity and is poor at predicting the nature of the fluid or whether or not it is infected^25–28.

Empyema in children usually appears as homogeneously echogenic pleural fluid on ultrasound, but so do haemorrhagic effusion and chylothorax. Echogenic pleural fluid is caused by cellular elements such as erythrocytes, inflammatory cells, fat droplets, or air bubbles and ultrasound cannot differentiate between these entities²⁸.

The pleural layers are frequently thickened in children with empyema and together with collapse of the underlying lung will cause failure of the lung to re-expand on inspiration. These abnormalities are easy to assess on ultrasound and affect clinical management of the child. When the pleural fluid is clear on ultrasound and there is no pleural thickening with good mobility of the underlying lung, percutaneous drainage is usually effective²².

	Computed tomography

Top Footnotes Abstract Introduction The clinical perspective Radiation hazards of thoracic... Chest radiography Fluoroscopy Ultrasound Computed tomography Magnetic resonance imaging (MRI) Follow-up imaging Conclusions Key points for clinical... References

 
As discussed before, the challenge for paediatric radiologists in children with suspected empyema is to differentiate empyema from parapneumonic effusion. Although this distinction is based on analysis of pleural fluid, certain CT features have been described as being highly suggestive of empyema^15,29–31. These include findings of enhancement and thickening of the parietal and visceral pleura, thickening of the extrapleural subcostal tissues and increased density of the extrapleural subcostal fat. These features on CT were described as being highly suggestive but non-specific for empyema rather than sterile pleural effusion^29,30.

Others have found CT to be unhelpful in diagnosing empyema secondary to pneumonia in children³.

CT is accurate for detecting pleural effusions³² and loculations in the fluid^13,29. It is the best method to differentiate peripheral lung abscess from empyema^15,30,31 and, in the UK, CT is generally used in instances where an underlying disorder of the lung is suspected. It may be necessary to use CT if a pleural collection is difficult to define on ultrasound because of the presence of pleural air (Fig. 4). It can sometimes be helpful to demonstrate poor chest tube position or failure of lung re-expansion.

View larger version (133K): [in this window] [in a new window]   Fig. 4 CT of empyema with loculated fluid and air in the pleural space (arrows). Satisfactory ultrasound examination was impossible because of the presence of the air.

 
There are a number of disadvantages of CT particularly where children are concerned. The radiation dose of modern chest CT is has been estimated to be 400 times the dose from a chest radiograph (CT approximately 8 mSv, chest X-ray approximately 0.02 mSv)³³. Radiation burden is a particular concern in the young who potentially have many years of life during which the harmful effects of radiation may be expressed. Small children often require general anaesthesia for a CT examination even with modern fast scanners.

The test does not provide a dynamic examination of the chest and will not show whether the lung is mobile. A further disadvantage is that the examination requires an injection of intravenous contrast medium that is associated a small risk of complications ranging from a mild allergic reaction to severe anaphylaxis.

	Magnetic resonance imaging (MRI)

Top Footnotes Abstract Introduction The clinical perspective Radiation hazards of thoracic... Chest radiography Fluoroscopy Ultrasound Computed tomography Magnetic resonance imaging (MRI) Follow-up imaging Conclusions Key points for clinical... References

 
MRI is an attractive imaging technique for use in children because it does not use ionising radiation and it has the capability of imaging in any anatomical plane. It is also able to give some tissue characterisation, for example indicate areas of haemorrhage in the chest in children with pulmonary haemosiderosis³⁴.

However, it is difficult to use MRI in small children as often they will not tolerate the procedure and the smallest children require general anaesthesia.

Availability of MRI varies greatly and in the UK access is often limited. This and the problems of scanning patients with chest drains and other medical support equipment makes MRI impractical as a routine imaging investigation in children with empyema.

	Follow-up imaging

Top Footnotes Abstract Introduction The clinical perspective Radiation hazards of thoracic... Chest radiography Fluoroscopy Ultrasound Computed tomography Magnetic resonance imaging (MRI) Follow-up imaging Conclusions Key points for clinical... References

 
The aim of treatment in children with empyema is to restore the situation in the healthy individual where there is an active pleural circulation with parietal filtration and re-absorption of pleural fluid. When an effective pleural circulation is re-established, pleural fluid gradually reduces. This may take a considerable period of time and follow-up chest X-rays may show abnormalities for weeks after clinical recovery. The chest X-ray is normal in the majority of children by 3 months after the illness³⁵.

Plain radiography is the most convenient imaging investigation for following progress after treatment of empyema.

	Conclusions

Top Footnotes Abstract Introduction The clinical perspective Radiation hazards of thoracic... Chest radiography Fluoroscopy Ultrasound Computed tomography Magnetic resonance imaging (MRI) Follow-up imaging Conclusions Key points for clinical... References

 
Ultrasound is used widely together with chest radiography to provide useful information about fluid in the pleural space. People have different opinions about how useful ultrasound is in predicting outcome in patients with empyema, but increasingly clinicians request this investigation.

Further cross-sectional imaging is usually with CT, but both CT and MRI should be reserved for children with suspected underlying lung abnormality or where ultrasound examination is difficult.

	Key points for clinical practice

Top Footnotes Abstract Introduction The clinical perspective Radiation hazards of thoracic... Chest radiography Fluoroscopy Ultrasound Computed tomography Magnetic resonance imaging (MRI) Follow-up imaging Conclusions Key points for clinical... References

 

• • The diagnosis of empyema is made by clinical assessment and chest X-ray
  
• • Chest ultrasound helps to confirm the diagnosis and suggest appropriate treatment
  
• • Consider using fluoroscopy to diagnose a bronchopleural fistula in preference to CT
  
• • When ultrasound is available, CT of the chest is required in a very small proportion of children to look for an underlying lung abnormality.
  

	Footnotes

Top Footnotes Abstract Introduction The clinical perspective Radiation hazards of thoracic... Chest radiography Fluoroscopy Ultrasound Computed tomography Magnetic resonance imaging (MRI) Follow-up imaging Conclusions Key points for clinical... References

 
Correspondence to: Dr Susan King, Consultant Paediatric Radiologist, Bristol Royal Hospital for Children, Paul O'Gorman Building, Upper Maudlin Street, Bristol BS2 8BJ, UK

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Top Footnotes Abstract Introduction The clinical perspective Radiation hazards of thoracic... Chest radiography Fluoroscopy Ultrasound Computed tomography Magnetic resonance imaging (MRI) Follow-up imaging Conclusions Key points for clinical... References

 

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