Surgical Treatment of Pleural Empyema in Children

Abstract

Pleural empyema is a common infectious pathology in pediatrics that requires timely treatment to achieve ad integrum recovery. The clinical understanding of the pathophysiological evolution of the disease and the knowledge of the methods of its imaging study allow the treating physician to add to the antibiotic treatment, such as drainage of the pleural space and/or thoracoscopy that has historically been performed. In recent years, many centers have replaced it with intrapleural injection of fibrinolytics with good results. Drainage and minimally invasive surgery procedures are detailed. The aim of the chapter is that the student has a comprehensive knowledge of the treatment and to keep in mind that both early diagnosis and timely treatment prevent the progressing of the disease and its possible complications.

1. Introduction

The visceral pleura covers the lung and the parietal pleura covers the inner wall of the hemithorax, leaving a virtual space between both, which in normal conditions houses between 0.1 and 0.2 ml/kg of pleural fluid with physical-chemical characteristics that serves as a lubricant for the pleural surfaces moving. The blood supply to the parietal pleura is from the arteries’ superior intercostals and phrenics and that of the visceral does of the pulmonary and pericardiophrenic arteries; some areas may be supplied by bronchial arteries. Venous drainage from the visceral pleura goes to the pulmonary veins and that of the parietal to the intercostal veins. The pleural lymphatics drain to supra and infradiaphragmatic networks. The flow of pleural fluid is regulated by Starling’s law which influences the hydrostatic and osmotic pressure of the pleural liquid. Under normal conditions, it can be renewed up to 500 ml of pleural fluid per day in a permanent active balance of transport and purification, in adults. In children, a production of 2 ml/hour in each hemithorax, has been noted. Pleural fluid accumulates when a disturbance occurs on the gradient between hydrostatic and oncotic pressure [1, 2].

The parapneumonic effusions are the result of the spread of inflammation to the pleura with the consequent accumulation of proteins, fluids and leukocytes in the pleural space forming the spill. Small amounts of protein are removed easily by the lymphatic system but when they increase as occurs in pneumonia due to increased capillary permeability, the lymphatic system is insufficient, producing the spill pleural. Initially, the pleural effusion is sterile with a low count of leukocytes. Over the hours or days, the bacteria invade the fluid, and the effusion can become thick and fibrotic resulting in empyema, which is defined as the presence of purulent fluid in the pleural cavity. The risk of developing a true pleural empyema is determined by a balance between the host resistance, bacterial virulence and timing presentation for medical treatment [1, 2].

The aim of the chapter is to analyze a common infectious pathology in pediatrics that may require various medical-surgical treatments. To achieve a good understanding of the topic, the definitions will be indicated according to the pathophysiological evolution of the disease and the study methods that will allow deciding the best complementary therapeutic alternative to antibiotics, from pleurodesis, drainage of the pleural space to minimally minimal surgery invasive that will be detailed, so that you can be put into practice. The non-thoracoscopic alternative of treatment with fibrinolytics that is used in many centers will also be taught and finally, the possible complications that, unfortunately, are not exempt from the treatment of pleural empyema will be indicated.

2. Definition

Pleural empyema is defined as the accumulation of fluid infected in the pleural space. Empyema derived from the Greek word empyein which means to “put pus in.” The most common infectious agents are bacteria, but they also may be caused by viral, fungal and Mycoplasma pneumoniae. Much less commonly can also result from chest trauma, post thoracic surgery, esophageal perforation or extension of an infection retropharyngeal, mediastinal, paravertebral, abdominal and retroperitoneal spaces, especially in immunocompromised children [1, 2].

An inflammation or an infection within or adjacent to the pleural space, rarely resolves spontaneously because host defenses are limited by the anatomy and physiology of the pleural space [3, 4, 5].

2.1 Definitions relation to pleural effusions/empyema

• Pleural effusions in general can be of two types depending on the underlying pathology: transudative effusion that is produced by an imbalance between hydrostatic and oncotic pressure in different pathologies, unlike parapneumonic effusion, which is an exudative effusion. Represents an alteration of factors localities that lead to an accumulation of pleural fluid. Initially, this pleural effusion is free-flowing and sterile.

• Pleural empyema is defined macroscopically by the presence of cloudy purulent fluid, frank pus or fibrinopus in the pleural cavity. Microscopically, when the study of the pleural fluid that is carried out immediately in the microbiology laboratory shows bacteria in the Gram stain and when the seeding of the fluid by the laboratory shows germs in the culture, the result of which takes hours or days depending on the different techniques used and type of germ.

• Complicated parapneumonic effusion corresponds when the initial exudate changes due to the invasion of germs in the pleural space or when the proteins increase and coagulate forming septa that loculate said space, causing greater accumulation of fluid. As the child has usually been treated with antibiotics to treat pneumonia and the defensive mechanisms eliminate the bacteria or pass them into the lymphatic circulation network, cultures of the fluid are usually negative.

• Loculated parapneumonic effusion refers to the presence of septations within the effusion, which interfere with the free flow of fluid. Loculations are caused by the accumulation of proteinaceous debris in the fluid as the disease progresses and can be detected by imaging ultrasonography.

• Complicated pneumonia refers to pneumonia with any complication, including in different percentages loculated parapneumonic effusion, empyema, necrotizing pneumonia, parenchymal cavitations, bronchiopleura fistula, pneumothorax or lung abscess.

3. History

After the Second World War, a commission was formed to study the cause of the high mortality from cadres’ respiratory problems among soldiers and how to avoid it. The call Graham Commission, in 1918, concluded that: “the infected liquid in the pleural space must be completely drained: early with closed methods and late, surgical drainage is more effective” and that “chronic empyema is avoided by early treatment of the infected pleural space” [2], what is valid to date.

4. Epidemiology

Parapneumonic effusion/empyema develops in 2–12%of children with pneumonia and in up to 28%of children requiring hospitalization [6, 7] and on the other hand, between 75 and 95% of cases of empyema are the result of pneumonia complicated by infected. It is most common among young children; rates are 3.7, 3.9 and 1.3 cases per 100,000 population among children under 2 years, 2 to 4 years and 5 to 17 years, respectively. Males and females are equally affected [6]. The mortality rate is low but may be higher in infants [6, 7]. Most deaths are due to the acute pneumonia or sepsis rather than the pleural disease.

Certain underlying diseases may increase the risk of parapneumonic effusion/empyema in children. In one review of 61 children with parapneumonic effusion/empyema, 11%had an underlying illness or condition [8]. Predisposing problems include immunodeficiencies [7, 8, 9, 10], influenza [11], malignancy [8], Down syndrome [7, 9], congenital thrombocytopenia [8], cerebral palsy [7, 8, 9], prior surgery [8, 12, 13] tuberculosis [10], congenital heart disease [7], prematurity [7], history of esophageal stricture [7, 8] and cystic fibrosis [7].

The bacteriology of infected pleural fluid has varied with the introduction of antibiotics, the development of resistance to them and the widespread use of vaccines for Haemophilus influenzae type B and Streptococcus pneumoniae [14]. Unfortunately, 35–46% of children do not achieve to identify etiological agents in the culture. In a review by Strong Memorial Hospital - University of Rochester, New York between 1962 and 1980, empyema was reported in approximately 0.6% of children with bacterial pneumonia, despite diagnosis and treatment [15]. However, the number of children with parapneumonic is increasing as demonstrated prospective studies of pneumonia acquired in the community [7]. Some other less common bacteria are being identified as a cause of empyema, such as Streptococcus viridans [16], Streptococcus group A and Actinomyces sp. [17]. The beta-hemolytic Streptococcus A infection associated with empyema and septic shock syndrome has been reported as a complication of chickenpox, immunodeficiency and rarely in healthy children [18]. In Chile, in the Pediatric Service of the Clinical Hospital of the Pontifical Catholic University of Chile, cultures were made in 24 children with pleural empyema, achieving a bacteriological yield in 15 (63%) and of these the Streptococcus pneumoniae was the most frequent with 60% of cases [19]. Empyema occurs twice as frequently in winter/spring than in summer/autumn and the mortality rate is higher in the children under 2 years [6].

In relation to pleural empyema during the recent Covid-19 pandemic there are already several interesting reports in world literature. In Hong Kong, in the post-COVID-19 period, a marked decrease in the incidence of pleural empyema in children was observed, while the incidence in adults remained similar. Polymicrobial etiology increased while Streptococcus pneumoniae etiology decreased. The authors postulate that this is related to the delay of children with pneumonia in going to the hospital [20]. In Australia, social distancing measures instituted due to #SARSCoV2 dramatically reduced cases of pleural empyema in children, according to the authors [21]. In the Netherlands, the increase in notifiable invasive group A streptococcal (iGAS) infections doubled between July 2021 and June 2022 compared to before COVID-19. There was a strong increase, more pronounced in children under 5 years of age and for the diagnoses of pleural empyema and necrotizing fasciitis. As the authors note, this increase in pediatric iGAS warrants investigation and surveillance [22].

Despite pediatric pleural empyema being included in the International Classification of Diseases, 10th Revision, Clinical Modification or Procedure Coding System (ICD-10-CM/PCS), there is no comparative literature on smoking, obese or diabetic children with pleural empyema compared to previously healthy children who develop pleural empyema [23].

Studies in adults show that in patients with empyema, the rate of smokers and diabetics exceeded the average rate of the general population of smokers and diabetic patients [24].

Studies in adult diabetics with pleural empyema indicate that the time to lung expansion after operation was longer. Stricter pre- and post-operative control of blood-sugar levels and adequate antibiotics are required to facilitate postoperative lung re-expansion. In patients with thickened pleurae, prolonged chest tube placement is unavoidable [25].

5. Etiology

Parapneumonic effusion/empyema in children occurs primarily in association with underlying bacterial pneumonia. Streptococcus pneumoniae (pneumococcus), community-acquired Staphylococcus aureus including methicillin-resistant S. aureus [MRSA] and group A Streptococcus are the predominant causative organisms.

Streotococcus pneumoniae (pneumococcus) has been the most common pathogen causing parapneumonic effusions and empyema, but its prevalence has decreased with the use of pneumococcal vaccines [26, 27]. The predominant causative organisms have changed over time with the advent of antibiotic therapy. The widespread use of polysaccharide and conjugate vaccines against Haemophilus influenzae type b2 and Streptococcus pneumoniae has also contributed [14].

Over a decade, in several places in the world, Methicillin-resistant Staphylococcus aureus has increased its frequency, and Streptococcus pneumoniae has invasive strain variants. Other germs such as Pseudomonas have appeared as etiological agents. It is due to the appearance of non-susceptible serotypes and multidrug-resistant phenotypes especially after the introduction of new conjugate vaccines of a broader spectrum [28, 29, 30]. To reduce resistance to antibiotics, it is necessary to strictly comply with the schemes indicated by the infectious diseases committee of each hospital, and be attentive to changes in the frequency of etiological germs and their sensitivity and the appearance of new serotypes that may be resistant.

6. Pathogeny

The pathological manifestations of the natural evolution of the pleural empyema according to the consensus of the American Thoracic Society (1962) have been divided into three phases or stages, that develop chronologically as follows:

• 1st exudative phase

• 2nd phase fibrinopurulent and

• 3rd and last phase of the process is the organization

However, prior to these states, there is always a pre-collection stage that is characterized by a localized pleuritis.

As shown in Table 1, the physical-chemical and bacteriological characteristics of the pleural effusion change according to the pathological phases in the natural evolution of the parapneumonic effusion that develops chronologically, if no treatment is provided.

Phase	Exudative	Fibrino purulent	Organization
Pleural fluid	Serous	Cloudy or purulent	Scant
pH	>7.3	<7.1	<7.1
Bacteria	Sterile	Present according to the use of antibiotics	Present or not according to antibiotic uses
Glycemia (mg/dl)	> 60	< 40	< 40
Units of Lactic dehydrogenase	< 500	> 1.000	> 1.000
White Blood Cells	< 1.000	> 5.000	Variable
Pleural Peel	Absent or thin elastic	Thin inelastic	Thick rigid to fibrous
Duration	24–72 hours	7–10 days	Starts in 3rd–4th week (lasts for months)

Table 1.

Physical–chemical and bacteriological characteristics of the pleural effusion according to the pathological phases in the natural evolution of the parapneumonic effusion.

6.1 Exudative phase

There is an accumulation of inflammatory fluid with characteristics of exudate, serous in appearance and generally sterile. Contains white blood cells in less than 1000 per mm3, lactic dehydrogenase with more than 500 units, the pH is greater than 7.3, glucose is between 40 and 60 mg/dl and staining of Gram no bacterial agents are found. It is a liquid easy to drain, and does not interfere with lung expansion when its volume is low. This phase can last as little as 24 to 72 hours [31].

6.2 Fibrinopurulent phase

This phase or classic empyema corresponds to a complicated parapneumonic effusion. The pleural space is infected. Fibrinogenesis occurs and fibrinolytic activity decreases. The procoagulant effect as the pH decreases, increases fibrinopus deposits on the pleurae. A matrix of septa is formed between the visceral and parietal pleura with multiple loculations. In addition, white blood cells in the pleural fluid increase.

The fluid changes characteristics of exudate to fibrinopurulent with a cloudy or purulent appearance and with the presence of germs. The physical-chemical characteristics also change: there is a greater number of white blood cells that can exceed 5.000 per mm3, lactic dehydrogenase rises above 1.000 units, the pH is more acid (which allows more coagulation of proteins), even reaching 7.1 or less and at Gram there are germs although the culture may be negative for the use of antibiotics and glucose drops to less than 40 mg/dl, for consumption as energy by bacteria. As the purulent pleural fluid becomes acidic, it thickens and septa appear that subdivide the pleural space in multiple loculations. The fibrin is deposited on the pleurae especially in decubitus areas, beginning to form a thin and inelastic fibrin peel or shell which ends up thickening and progressively restricting lung expansion, decreasing the ability to oxygen exchange in that lung, rendering it ineffective ipsilateral kinesiotherapy. Antibiotic levels are low in the pleural fluid and the physicochemical conditions make them less effective, as occurs with aminoglycosides [32, 33]. This phase can last 7 to 10 days.

6.3 Organization phase or fibrosis

If the process continues its natural course, it reaches the phase of organization or fibrosis in which the pleural fluid increasingly is less until it disappears, the leukocytes are in quantity variable, lactic dehydrogenase is also maintained at variable levels, pH remains below 7.1, glucose persists below 40 mg/dl and there may or may not be bacteria on the staining of Gram, according to the use of antibiotics.

Fibroblasts proliferate in both pleurae, producing a membrane or fibrin shell that is thicker and more rigid, known as peel. In addition, there is a large increase in newly formed capillaries between the peel or fibrous shell and the visceral pleura, between the fourth to fifth and even sixth week of initiation of the empyema. Fibrosis progressively increases until finally the lung is trapped and immobilized firmly, which prevents its normal expansion. The organizational phase or stage results in a thick cortex that can trap the lung. It is perfused but not ventilated, which manifests as chronic restrictive lung disease.

Despite being sequentially outlined, there is no certainty that each will progress to the next and on the other hand, it is important to point out that not all the pleural space is always in the same phase with the same intensity, since the dorsal decubitus and the recesses of the pleural cavity are generally areas with more compromised or advanced disease. More importantly, the stage of pleural disease may not relate to the degree of physiologic illness of a child. The severity of illness is determined by the extent of underlying parenchymal disease, the extent of intravascular inflammatory response and the extent of the impact in the pleural space of the hemithorax. Patients may be quite systemically ill early in the course of severe pneumonia but clinically later on in empyema development, which should be considered prior to intervention should always be viewed considering the layers of processes when treating empyema.

7. Clinical diagnosis

The symptoms and signs of pleural empyema are generally difficult to differentiate from those of pneumonia since it is observed fever, malaise, dyspnea, chest pain with breathing, usually productive cough and exceptionally cyanosis. Anorexia and chest pain with inspiratory stop are added that can make a difference. On physical examination the signs are also similar to those of pneumonia such as tachypnea with variable degree retraction, inspiratory stop, decrease to a greater or lesser degree of the lung murmur; in addition to crackles, tubal murmur, dullness to percussion and there may be abdominal distension from ileus which may increase respiratory distress, so it should be evaluated with a chest x-ray and abdominal x-ray if necessary [34].

Empyema should always be suspected when a child with pneumonia does not improve with antibiotic therapy, or your symptoms worsen after early signs of improvement. A significant rise in temperature, oxygen-demanding hypoxia, leukocytosis and an increase in C-reactive protein are suggestive of an infected parapneumonic pleural effusion.

8. Evaluation and study

When a child with pneumonia does not respond to antibiotic treatment within 48 hours, the possibility of a parapneumonic effusion should be considered. Since it is not always possible to determine if there is an effusion or more aggressive pneumonia during a physical examination, a chest x-ray should be used. Radiology constitutes an element of valuable help to determine the presence of occupancy of the space fluid pleural. Pleural effusions in the exudative phase or stages in children are classified as small effusion if the opacification is less than a quarter of a hemithorax, moderate if the opacification is between a quarter and a half hemithorax and large when it is more than half a hemithorax on upright radiographs [35]. Unfortunately, the standing position, which is very useful in older children, cannot be performed in small children, so we must know how to interpret the x-rays in the supine position.

As shown in Figure 1 of an infant child in a supine position with partial opacification of the pleural space, it is not possible to determine whether the pleural effusion is septated or not. As the effusion is more than 10 millimeters thick, we complemented it with Figure 2, which demonstrates a liquid pleural effusion without septa, so it is free.

Figure 1.

Anteroposterior chest X-ray in decubitus: Moderate right pleural effusion (unfilled arrow) with intercissural effusion (single arrow).

Figure 2.

Chest ultrasound showing free pleural effusion without septations (unfilled arrow), corresponding to the patient in Figure 1.

In chest Figure 3 of a preschool girl in a supine position shows complete opacification of the pleural space with air bronchogram. Nor can we define whether said spill pleural is septated or not. In this scenario, it is appropriate to perform Figure 4, which demonstrates a pleural effusion with multiple septa with the formation of locules with heterogeneous content.

Figure 3.

Anteroposterior chest X-ray in decubitus: Complete opacification of the right hemithorax (unfilled arrow) with air bronchogram (single black arrow). Radiologically, it is not possible to clarify whether or not said pleural effusion has septations.

Figure 4.

Chest ultrasound corresponding to the patient in the Figure 3 showing pleural effusion with multiple septations (White arrow) with formation of loculations (asterisk), echoes inside (red arrow) and thickening of the visceral pleura (unfilled arrow).

According to the distribution of the effusions in pleural space, the clinician can determine if this fluid is free or not, and thus be able to define which treatment is the most appropriate for the girl or boy which we will see in the treatment subsection.

Is it different in schoolchildren and adolescents who have had a chest x-ray taken in a standing position? If it has opacification of the pleural space with the classic Damoiseau curve we must assume that said fluid could be free in the costophrenic sinus but if the effusion does not have the typical marked curve, most likely the fluid is already septated. However, radiographs alone cannot differentiate an empyema from a parapneumonic effusion [36]. In this scenario, it is preferable to request an ultrasound of the spill, which provides excellent information. The need for chest x-rays in pleuropneumonia for diagnosis and treatment control in relation to radiation corresponds to the sum of each of them. It is not dangerous from the point of view of radiation biology unlike computed tomography [37, 38].

There is an inappropriate practice - there being the possibility of performing an ultrasound of the effusion - of performing x-rays in the lateral decubitus position with a horizontal beam to try to clarify whether the fluid is free or distributed. Unfortunately, the occupation of space pleural radiologically does not differentiate between thickening pleural, fluids and septations. If there is free liquid on the side right, for example, occupation of the space should be observed right pleural in the film in right lateral decubitus, which would have to disappear on the plate in the lateral decubitus position left. Loculated pleural effusions are usually not evident in decubitus radiographs, which can delay treatment. If on the lateral decubitus film, the radiograph shows a space occupation greater than 10 mm thick, the test of choice to continue is a chest ultrasound that allows us to see the pleural fluid, its characteristics and the presence or absence of partitions with the added advantage of being portable, relatively inexpensive and radiation-free (see Figure 5 = Use of images for management of pleural effusion). On a stage more advanced, ultrasound allows us to see fibrin septa that form locules of variable size and content in different coagulation stages from semi-liquid, semi-coagulated or coagulated according to the evolution time. In addition, it allows marking the ideal puncture or drainage site and/or ultrasound guidance of the procedure to evacuate fluid and send a sample to the laboratory for study [39]. Since it has already been noted that pleural effusions are not always in the same phase throughout the pleural space, ultrasound should inspect the entire pleural space from the apex to the costophrenic and cardiophrenic sinuses.

Figure 5.

Pleuropneumonia with free effusion management (low grade).

Quite useful is the ultrasonographic classification of infectious pleural effusion, which classifies them in grades according to ultrasound characteristics of the pleural effusion. As shown in Figure 2, the low-grade pleural effusion is homogeneous without echoes in suspension or septa and is not associated with pleural thickening and as shown in Figure 4, the high-grade effusion presents echoes inside with formation of loculations and thickening of the visceral pleura [40]. This classification makes it possible to define complementary treatment behaviors to the antibiotic such as pleurocentesis, drainage or video surgery, according to the degree and volume of the effusion, as will be indicated in the subsection treatment.

Computed tomography (CT) is useful when we suspect that the condensation of the parenchyma is undergoing changes that can modify our behavior, such as necrotization late-stage pneumonia or abscess formation, but it does not allow us to specify the nature of the liquid, the presence of empyema or see the fibrin septa since these are not vascularized and therefore cannot be visualized [41]. As a result of these limitations, chest CT should not be routinely performed in the evaluation of children with parapneumonic effusions.

Blood cultures should be performed in all children with parapneumonic effusion, being positive between 10% and 22% of children with complicated effusions and are particularly useful if the culture of pleural fluid is negative [42].

Pleural fluid should be studied for analysis including Gram stain and bacterial culture; there are reports of positivity in up to 63% but most studies report culture positive in less than 25% [18].

8.1 Exudative phase

If the child has an uncomplicated parapneumonic pleural effusion (low grade) will respond to thoracentesis, sucking up liquid as much as possible (up to a maximum of 10 to 20 ml/kg) plus antibiotic [43]. If the spill cannot be adequately evacuated, if it is reproducing or if the volume of non-septate pleural fluid is greater than 1 cm on a radiograph in decubitus or the opacity is greater than a quarter of the hemithorax based on the upright film, it must be drained. This behavior will allow for improved inspiratory volume and decrease the possibility of that said effusion is septated. On the other hand, if the parapneumonic free pleural effusion is complicated from the cytochemical point of view in the sample of the pleurocentesis for presenting germs to the Gram or the pH is lower than 7.2 or glucose less than 40 mg/dl or dehydrogenase greater than 1000 units, consider adding to the antibiotic treatment the installation of a pleural drainage tube or pleural catheter depending on the size of the child, to prevent the process from progressing.

8.2 Fibrinopurulent phase

When there is macroscopic pus in the puncture, antibiotics along with a thick chest tube has been the traditional management, which has changed to thinner tubes or small diameter catheters that are easy to install and cause less pain to the patient, with a high success when said empyema is free [5]. Currently, most pediatric centers do not install traditional chest tubes but rather pig tail catheters for the treatment of non-septum empyema.

Once the septa are formed the pleural tube will evacuate fluid only from some locules of the septate empyema and will not be able to completely evacuate the fibrin clots that have formed especially in the pleuropulmonary spaces decubitus or destroy the partitions that have formed between the visceral and parietal pleura, for which video surgery is necessary for the removal of septa by debridement pleuropulmonary [44, 45].

If at this stage the installation of a thoracostomy tube fails to evacuate the purulent pleural fluid from the pleural space on the follow-up chest x-ray, it is surely the child already had septa formed. A surgeon must be consulted to ensure complete drainage through thoracoscopy, optionally with prior ultrasound.

8.3 Organization phase or fibrosis

When the final stage of fibrous sequela is reached, the antibiotics are not necessary and kinesiotherapy does not achieve lung re-expansion it is necessary to perform a formal pleuropulmonary decortication, which in the pediatric age is the exception, since it is generally possible to reverse the box fibrosis in several months [46]. For a stage III empyema in the organization phase, thoracostomy tube drainage alone will almost assuredly result in treatment failure and consideration for surgical intervention to definitively address the empyema may supplant the role of a thoracostomy tube.

9. Preoperative investigations and preparation

Dr. Richard W. Light has the merit of having differentiated from a physical-chemical point of view the pleural fluids in transudative effusion and exudative effusion more than 50 years ago [47, 48] and subsequently classified exudative effusion according to different criteria, being that of complicated parapneumonic effusions when the pH is equal to or less than 7.2, lactate dehydrogenase greater than 1000 units, glucose less than 40 mg/dL or less than 25% of the blood glucose level and the Gram stain or culture is positive [49]. Light’s criteria are still accepted as the default reference test for separating transudates and pleural exudates after half a century [50].

Loculations or septations should have been shown with images. A consensus statement from the American College of Chest Physicians in 2000 noted an increase in interventions as the stage of effusion increased. Similarly, a pleural fluid pH of less than 7.1 has been found to result in a sixfold increase in the likelihood of surgical intervention based on retrospective data [51]. While these criteria document the pathophysiological progression of disease, the clinical relevance of the physicochemical analysis is not critical because the prognostic value is less important in the practice. Once pleural space debris causes symptoms and requires removal, drainage or surgery is required based on the nature of the debris.

10. Treatment

The classic treatment of the fibrinopurulent phase has been antibiotic therapy and pleural drainage with good success but with prolonged treatments and hospital stays. In children in phase or stages exudative with small and same moderate-sized effusions were effectively managed without drainage (015). This suggests that intervention should also be based on symptoms and not just on the size of the effusion alone. The symptoms of intervention are tachypnea and increasing oxygen requirement [52].

When deciding to drain the fluid, options include single or multiple thoracentesis versus tube thoracostomy. It may be reasonable in an older child who tolerates the procedure with local anesthesia; probably would not be appropriate in younger children. The British Thoracic Society guidelines recommend a chest tube in cases where the first thoracentesis fails to adequately drain the effusion and thus avoid multiple attempts [53].

Almost all authors recommend the procedure with sedation in children according to local guidelines. The skin and soft tissues around the fifth intercostal space in the midaxillary line are asepticized according to each hospital’s protocol and infiltrated with 1% lidocaine. A 12 Fr or larger chest tube can be used depending on the size of the child with the classic technique through a small incision or a pig tail catheter can be introduced using the Seldinger technique through a small incision and using dilators up to the desired number of catheters. Regarding appropriate chest tube sizing, no advantage has been confirmed with tubes larger than 14 Fr and on the other hand smaller caliber tubes are not hindered when used in spills. No differences have been found in pleural effusions in children treated with standard chest tubes compared to those treated with pigtail tubes. Image guidance is not considered necessary to guide the procedure in most patients but if you have the resources and expertise in handling the ultrasound transducer, you can use it. In some centers, the installation of the drain is performed under general anesthesia with tracheal intubation, especially in infants and preschoolers.

Once the tube or pig tail catheter is inserted, the fluid that is withdrawn is sent for physical-chemical study, Gram and bacteriological culture and the tube is attached to a − 20-centimeters H20 suction collection device and it is recommended to evaluate with a portable chest x-ray.

When a child with pneumonia does not respond to antibiotic treatment within 48 hours, a practical approach developed by the author is shown in Figure 6. A chest x-ray should always be indicated in this scenario. If there is no pleural effusion, the treating pediatrician continues the treatment of the pneumonia. If there is an effusion, the study must be complemented with ultrasound. If this shows septate fluid, a thoracoscopy is indicated (in some centers a fibrinolytic protocol is initiated as will be explained in detail later). If the pleural effusion is free on the ultrasound, the treatment is maintained and an evacuative pleurocentesis will be performed or a pleural drainage will be installed depending on the volume of the effusion and each case. The treatment is maintained, and the antibiotic can be adapted to the result of the culture and the sensitivity of the causative germ, if it is positive. The child will be monitored clinically and radiologically. If the drainage is partial and the child remains febrile with leukocytosis and elevated C-reactive protein 48 to 72 hours after the procedure, video-assisted thoracoscopy is proposed unless it is proven that the condition is due to necrotizing pneumonia.

Figure 6.

Study of pneumonia that does not respond to treatment.

When a child with free and small parapneumonic pleural effusion has an indication for pleurocentesis according to Figures 5 and 6 is proposed. If the extracted fluid is purulent, a pleural drainage is installed and antibiotics are maintained according to the protocol of the local infections committee, which will be modified according to the results of the culture. If the pleurocentesis fluid is not macroscopically purulent and its laboratory study indicates that it is not complicated, antibiotics are continued. If it is considered that the pleural effusion is of limiting volume, the installation of a pleural drainage is added on a case-by-case basis. If the study of the fluid shows that it is complicated according to Light’s criteria, a pleural drainage is installed regardless of the volume of the pleural effusion. All post-pleural drainage installation scenarios will be controlled clinically and radiologically.

11. Surgical treatment

With the formation of septa that trap the pleural fluid, the drainage tube becomes insufficient since it only manages to drain some locules, so the surgical release of the fibrin must be performed.

The goal of surgical treatment of pleural empyema in this phase is:

1. transform the multiloculated collection into a collection unique to achieve complete drainage of residual fluid.

2. debride fibrin as much as possible to control pleural infection and free the lung to expand and reestablish contact between the visceral pleura and the parietal pleura. In this way, the resolution of the infection is accelerated, achieves lung re-expansion and that antibiotic treatment be more effective. With minimally invasive techniques, obtain an excellent result, achieving post-operative with little pain, shorter hospital stays and good outcome esthetic [54, 55].

The critical consideration prior to embarking on thoracoscopic or open debridement for empyema is the status of the underlying parenchyma. Patients with persistent illness may have pulmonary necrosis as their source instead of pleural space disease. In this circumstance, an operation should be avoided in favor of patience.

The surgical technique described below corresponds to that used in our surgery service that we have performed for around 20 years. Some modifications have been the product of personal experience and exchange with American experts that we have visited and with some who have visited us.

For each of the following surgical techniques, the procedure is performed under general anesthesia with tracheal intubation facilitated by selective one-lung ventilation. The patient is placed in the lateral decubitus position with the affected side up and an axillary roll is placed. An attempt should be made to place the patient’s iliac crest at the break point that all operating tables have. Subsequently, the table is angled at an angle greater than 180 degrees, which allows an expansion in the thorax that opens the intercostal spaces, facilitating the introduction and motility of either the trocars or the thoracoscopic instruments.

Initial incision and insertion of a 10 mm port being positioned in the area deemed advantageous for accessing the majority of disease after a review of the ultrasound images. Typically, this initial 10 mm port is best placed directly overlying the empyema. In infants and preschoolers, one of 5 mm trocar is preferred. The placement of the port in the fifth intercostal space at the mid-axillary line is also a good starting point. A low pressure (4 mmHg) and low flow (1 L/min) CO₂ pneumothorax facilitates lung collapse. A 10 or 5 mm angled telescope, depending on the first trocar is used to create a working space by freeing the virtual pleural space of septa or fibrinopus deposits from the lung to the chest wall with the end of the telescope.

As seen in the author’s unpublished photographic series in Figure 7, the thoracoscopic view shows once the underlying lung has been adequately released and the 5 mm instrument has been introduced into the site where most of the fibrinopus must be released.

Figure 7.

The thoracoscopic view of a large amount of fibrinpus filling a fairly widened pleural space (asterisk) which do not initially allow visualization of the lung as is usual in advanced cases. The instrument (5 mm) being observed (arrow) will allow the lung to be released.

When two incisions are not enough a small third incision can be made for a second working port.

Other authors use a single trocar thoracoscopic operation with a conventional rigid scope with a working channel with good results in the treatment of pleural empyema in children [56].

Samples for physical-chemical study, Gram and bacteriological culture are routinely sent by attaching a Lukens trap to the suction device. In addition, fibrin is sent to histopathology, which can also help in trying to determine the microorganism.

For pleural debridement and peel are using a ring forceps or Yankauer suction devices. In adolescent children, alternatively, atraumatic grasping forceps from open surgery can also be used.

In Figures 8–10 you can see how the thick fibrin pus shell adhered to the lung is carefully removed and the pleural cavity is released step by step. In photographs C and D, you can see that the underlying lung, at least at that level, is in good condition.

Figure 8.

Advancing the release, thick septa (asterisk) are observed on the upper edge that goes from the visceral to the parietal pleura. There are abundant deposits of fibrinopus adhered to the lung (unfilled arrow) and chest wall (single white arrow) and slowly space is opening (red arrow) up for better visualization.

Figure 9.

The peel of fibrin pus over the lung has been partially released (Asterik). The lung is seen in good condition at that level (unfilled arrow).

Figure 10.

Progressing in the release of the peel on the visceral pleural (black asterisk), reaching the edge of the lung lobe. At the level of the parietal pleura there is abundant fibrin pus (red asterisk). Lung (unfilled arrow).

In order not to repeatedly remove fibrin fragments from the thorax with the instrument and reintroduce it again to continue debridement, it is useful and reduces surgical time to accumulate the fibrin in an accessible recess and at the end of debridement, remove or aspirate it at once.

In Figure 11, you can see that both pleurae have been freed from the fibrin pus. The surgical objective was obtained. Lung was re-expanded and pleura-to-pleura contact was achieved, which cannot be seen in the photography since we are still working with carbon dioxide pneumothorax that separates them.

Figure 11.

Both the visceral (black asterisk) and parietal pleura (red arrow) have been freed from the fibrin pus. The surgical objective was obtained. Lung (unfilled arrow) was re-expanded and pleura-to-pleura contact was achieved, which cannot be seen in the photograph since we are still working with carbon dioxide pneumothorax that separates them.

Finally, in Figure 12 you can see that the multiloculated collection has been transformed into a single collection and a soft and flexible chest drain is installed in the pleural space under direct vision.

Figure 12.

The third surgical objective was achieved. Transform the multiloculated collection into a single collection (Asterik). Finally, a soft and flexible chest drain (Unfilled arrow) is installed in the pleural space under direct vision. Lung (single arrow).

To reduce the possibility of pneumothorax when the tube is removed, it should not be inserted directly from the skin to the pleura, so it is preferable to tunnel the drainage tube at the subcutaneous cellular level over the costal space in a cephalad direction to the site of the port where it enters the next pleural space.

Once the drainage tube is installed, it is fixed to the skin using a technique according to local protocol and the other incisions that were made are closed with absorbable suture and sterile dressings are applied to each one.

When video thoracoscopy equipment is not available, which is currently an exception, pleural debridement can be performed through a small thoracotomy. It is done under direct vision. Loculations of fibrin pus are released and eliminated. An appropriately sized chest drain is placed. The costal wall is closed in the usual manner. In the past, Raffensberger [57] recommended doing it with a two-centimeter resection of the rib, which is not accepted today.

12. Postoperative care

The chest drain is initially placed in a system with 20-centimeters water suction that is available from different commercial brands in different markets. If there are no air leaks or the output is not serious, you can switch to a bulb suction system (with springs) or to the classic underwater trap. A postoperative chest x-ray in the recovery room is necessary. Chest tube or catheter is removed once there is no evidence of air leakage and the drainage is less than 1 ml/kg/day in at least a 24-hour period, without the need for post-removal radiographs, unless otherwise indicated. After the drainage is removed, the incision is closed with absorbable suture or taking advantage of the suture with which, the tube had been fixed and sterile dressings are applied.

Pain should be treated according to local pain guidelines, initial non-invasive monitoring with oxygen supply as needed together with control of hemoglobin, hydrosaline and acid-base balance are necessary. Maintenance kinesiotherapy and antibiotics, according to crop must be modified.

There are no data from randomized controlled trials on the appropriate duration of the antibiotic or whether the duration should vary depending on the causative organism. Some continue intravenous antibiotics for 48 hours after the fever is gone. Others maintain it for a total of 7 to 10 days that the patient is afebrile. When switching to oral treatment, this should be continued for 2 to 3 weeks more [58]. The current consensus guidelines on empyema recommend antibiotics 10 days after the resolution of fever.

The child must remain hospitalized while connected to the drainage system and discharge is preferably based on clinical criteria: afebrile, no need for oxygen, the pain is controlled, good appetite with nutritional issues are optimized, good level of activity and general condition, rather than radiological criteria, since the radiograph chest lesions take between 4 to 8 weeks to clean after debridement and in some cases they still maintain some degree of residual pleural thickening until 12 to 24 weeks postoperatively. A follow-up visit and chest radiograph are recommended 3−4 weeks following discharge [58].

13. Complications

As treatments depend on the different phases or pathophysiological states of the pleural effusion, most children with parapneumonic effusion or empyema recover completely. In the majority of cases, both the lung parenchyma and the pleurae appear normal in the months after the event [59, 60].

Complications may be inherent to the pneumonia causing the effusion, of the empyema itself or its treatment like drainage tubes or catheter, thoracoscopy and vascular lines. We analyze them separately.

13.1 Complications inherent to the pneumonia

The lung can develop a serious complication such as necrotizing pneumonia. Cavitations may develop which can rupture and cause tension pneumothorax. A bronchopleural fistula may also occur in severe cases. These complications are rare, but if they occur, treatment is complex and recovery is prolonged [58]. Exceptionally, a perforation through the chest wall may occur, which is called empyema necessitans [61, 62].

13.2 Complications inherent to the pleural effusion and empyema

Arriving late to the treatment of exudate or empyema can cause its progression, reproduction of the process with greater complications or end in the last phase or stage of the process that traps the lung and causes a ventilatory restricted lung.

13.3 Complications inherent to the insertion of drainage tubes or catheters

Placing a thoracostomy tube or catheter is rare malposition, bleeding or wound infection at the exit site and persistent atelectasis. Also, can be associated with severe but very rare complications including damage to the lung, diaphragm, heart, liver or spleen, intercostal nerve or artery or vein injury. To avoid iatrogenesis and minimize complications, the use of ultrasound or another imaging modality such as fluoroscopy, may be used to guide placement of the thoracostomy tube or catheter [63, 64]. The increasingly common use of small tubes (pigtail catheters) has reduced installation complications and postoperative pain [65, 66].

During the insertion of drainage tubes or catheters, it is impossible to evaluate the presence of adhesions between the lung and the pleural surface when the patient has had previous pleuropulmonary processes. Knowing the child’s previous medical/surgical history and the use of ultrasound before and during tube insertion minimize this potential complication [67].

13.4 Complications post insertion of the drainage tubes or catheter

Draining pleural fluid too quickly can occasionally cause pulmonary edema, known as “pulmonary reexpansion edema.” It is recommended after draining the initial 10 ml/kg of pleural fluid to stop and clamp the tube for 1 hour to avoid sudden re-expansion. The tube is then unclamped and another 10 ml/kg of pleural fluid is allowed to drain if there is still any.

For adolescents, some experts suggest that drainage should be limited to 500 ml/hour with the previously mentioned 1-hour rest with the tube clamped. It is continued in the same way without exceeding a total of 1500 ml of pleural fluid [43, 68].

Reexpansion pulmonary edema usually arises after rapid reexpansion of a lung that has been collapsed for at least 3 days due to pneumothorax or effusion. An initial report reported that it was more likely after pneumothorax drainage; however, in later publications, it has been more associated with drainage of pleural effusions [69, 70].

If in the postoperative period the tube continuously bubbling, the position of the tube should be assessed since it may be partly out of the thorax with one of its drainage holes open to the atmosphere [58]. If the tube is in situ ok, the problem may also be caused by a bronchopleural fistula, especially in cases of necrotizing pneumonia, a complication that sometimes requires endoscopic or autologous blood therapy through drainage [71] and exceptionally with a surgical intervention.

Morbidity and mortality from thoracostomy tube or catheter placement are related to the experience and training of the clinician, the indication for placement and the circumstances under which the tube is placed: planned or urgency [72, 73, 74, 75].

The complications of video thoracoscopy are those inherent to other thoracic surgeries and are beyond the objectives of the chapter, as are the complications of the venous and arterial lines used.

14. Fibrinolytics

The definitive management for empyema has traditionally been surgical debridement [76], which has historically been performed by video-assisted thoracic surgery (VATS) that has resulted in earlier and more complete resolution of empyema than chest tube drainage alone in both retrospective and prospective studies, translating shorter hospitalization with primary VATS. However, primary management of empyema with surgical debridement is changing and fibrinolysis has developed a more prominent role in empyema management.

The British Thoracic Society recommended years ago fibrinolytic therapy as a medical option for patients in whom fluid pleural is thick or septate as a reasonable alternative to videothoracoscopy for children with parapneumonic effusion septum who are hospitalized in institutions that lack from a pediatric surgeon trained in videothoracoscopy, based on the fact that there are no differences in the clinical results [58] and another author has very similar results with both methods except for the lower cost with the use of fibrinolytics [77].

Three prospective, randomized trials compared fibrinolysis with VATS in the treatment of pleural empyema in children more than 10 years ago. They were carried out in three countries. Spain [78], the United Kingdom [79] and the United States [80] in 103, 60 and 36 patients respectively. All three studies compared the installation of fibrinolytic agents for 3 days to VATS as the initial therapy for empyema. The first fibrinolytic dose in both studies was given upon diagnosis and/or chest tube placement. The Spanish study used urokinase every 12 hours for 3 days while the other two studies used every 24-hour to complete the three-dose. The results were concordant, with all the studies documenting no difference in the duration of hospitalization, the primary outcome in all the trials. The failure rate for fibrinolysis was 10% in the Spanish study and 16.6% in the other two studies. These failure rates were similar to previous studies investigating the utility of fibrinolysis, so that fibrinolysis is an effective first-line therapy.

Fibrinolysis is performed by mixing 4 mg of tissue plasminogen activator (tPA) = Alteplase ® in 40 mL of normal saline which is injected directly into the tube, which is then clapped for 1 hour. After the dwell time, the tube returns to continuous suction. Two additional doses are then administered at 24-hour intervals using the same technique. If, after three doses, the patient has not clinically improved, another ultrasound is performed to evaluate for intrapleural disease. Minimally invasive pleural debridement is considered eventually if the tissue plasminogen activator (tPA) has failed to eradicate the pleural space of fibrinopurulent material [81].

An interesting retrospective single-center observational study of 97 children hospitalized in Belgium, with a diagnosis of parapneumonic pleural effusion during a 15-year period, indicates that corticosteroids may be a part of the therapeutic armamentarium for children with parapneumonic effusion when conventional nonsurgical management fails, especially when the fever does not subside, as an anti-inflammatory therapy [82].

In our country, the high cost of urokinase has not allowed its use to be introduced, except in isolated cases, so there is not enough experience. In particular, the use of Alteplase ® is being initiated in our hospital, so we do not have objective results.

Keypoints

• An early clinical diagnosis of parapneumonic effusions is important.

• The most common symptoms of empyema are fever, cough, malaise, anorexia, chest pain, dyspnea or lack of response within 48 hours of appropriate therapy for pneumonia.

• Children with the described symptoms should be evaluated with chest x-ray.

• If the radiological effusion is greater than 1 cm in lateral decubitus radiography or a quarter of the hemithorax in the upright position, an ultrasound should be continued, which is the image indicated to confirm the presence of fluid in the pleural space and evaluate loculations and septa.

• If the effusion is free, a diagnostic pleurocentesis should be added if the liquid is scarce.

• Depending on the type and amount of spillage, a tube or catheter pleural should be placed.

• If the spill reproduces or is blocked, the best recommendation is video-assisted thoracoscopy to perform a pleuropulmonary debridement that improves the child in minor time and with fewer sequelae.

• If the center has experience and practice in fibrinolytic therapies, an initial attempt is a good decision based on controlled trials that show no significant difference in several important outcome variables.

• The author declares that he has no conflicts of interest in relation to this article.