Chapter 5
Pleural effusion
Christopher Merrick1, Rachelle Asciak2,3,4, Anthony Edey5, Fabien Maldonado1 and Ioannis Psallidas2,3,4
1Vanderbilt University Medical Center, Tennessee, Nashville, TN, USA. 2Oxford Centre for Respiratory Medicine, Churchill Hospital, Oxford University Hospitals NHS Foundation Trust, Oxford, UK. 3Oxford Respiratory Trials Unit, Nuffield Dept of Medicine, University of Oxford, UK. 4Laboratory of Pleural and Lung Cancer Translational Research, Nuffield Dept of Medicine, University of Oxford, UK. 5Dept of Radiology, Southmead Hospital, North Bristol NHS Trust, Bristol, UK.
Correspondence: Ioannis Psallidas, Oxford University NHS Foundation Trust, Old Road, Churchill site, Oxford, OX3 7LE, UK. E-mail: ioannis.psallidas@ndm.ox.ac.uk
Pleural effusions represent a significant disease burden globally. TUS, performed by both radiologists and physicians, has increasingly become an essential tool in the evaluation and management of pleural effusions. It detects pleural effusions with higher sensitivity and specificity than CXR, and provides valuable information about the size and depth of the pleural effusion, the echogenicity of the fluid, the presence of septated or loculated fluid, pleural thickening and nodularity, and the presence of any contralateral pleural effusion. TUS can provide information on diaphragm position and movement with respiration, and can assess the presence of lung sliding and the accessibility of pockets of fluid in loculated pleural effusions, thereby improving the success rate and safety of pleural procedures. Given the added detail that US provides and its increasing availability, it is no surprise that its use is increasingly expanding in clinical practice.
Cite as: Merrick C, Asciak R, Edey A, et al. Pleural effusion. In: Laursen CB, Rahman NM, Volpicelli G, eds. Thoracic Ultrasound (ERS Monograph). Sheffield, European Respiratory Society, 2018; pp. 64–74 [https://doi.org/10.1183/2312508X.10014817].
Pleural effusions represent a significant burden of disease globally, related to both primary pleural and systemic pathologies. It is estimated that 3000 people per million of the population are affected by pleural effusion [1]. A broad range of diagnostic and treatment modalities is available to the physician treating individuals suffering from pleural effusion. The role of TUS in pleural effusion is multifaceted, and this technique is useful for diagnosis, treatment and even, in some cases, prognosis. It is useful in both inpatient and outpatient settings for treating individuals with pleural disease.
Physician competency
With the growing use of bedside US by treating clinicians, there is an increasing awareness that US practice need no longer be isolated to the radiology department. Bedside TUS has been shown to decrease expense, as well as time in hospital [2]. Optimal management of pleural effusion from a healthcare cost and patient wellness perspective is best initiated by the chest physician through skilled TUS analysis and TUS-guided procedures at the bedside. However, patient safety requires that bedside physicians have received appropriate training and hands-on experience with TUS prior to independent use for management of patients. Multiple studies have demonstrated a decreased incidence of iatrogenic thoracentesis complications following initiation of formalised TUS training and regular use of US for percutaneous procedures [3, 4]. An increasing number of respiratory medicine training programmes internationally are creating formal US training programmes to promote physician competency. Competence in pleural US is now a compulsory part of respiratory medicine training programmes in the UK [5]. The Royal College of Radiologists stipulates that obtaining a certificate of basic TUS competence (level 1) includes keeping a logbook of US examinations by the trainee and an assessment of competence by an experienced trainer. Required competencies include the performance of safe and accurate examinations, recognition of anatomy and pathology, recognition of when to appropriately refer for a second opinion, and an understanding of the relationship between US imaging and other imaging techniques. With more practice and experience, including the performance of noncomplex US-guided procedures, and with conductance of research in US, the trainee can then be certified as level 2 competent. Level 3 is an advanced level of practice, which in the UK would usually equate to a consultant radiologist with a subspecialty practice [6].
At all stages, respiratory physicians should collaborate with radiologists, and TUS findings should be correlated and combined with other imaging techniques, such as CT scanning, in order to deliver the best care for patients with pleural effusions.
With the growing use of US in various specialties, there is also a move to integrate US training into medical school curricula [7].
Pleural effusion
Aetiology and pathogenesis
The pleural space is a tightly regulated virtual space that contains a small amount of pleural fluid in physiological conditions, governed by a balance of plasma ultrafiltration and venous and lymphatic drainage. This delicate balance can be disturbed in a variety of situations, such as in the setting of pleural tumour, infection, and lymphatic obstruction or disruption, resulting in a net accumulation of pleural fluid.
Pleural effusions are categorised as exudative or transudative, based on time-honoured criteria involving fluid lactate dehydrogenase and protein, which remains an initial crucial step in determining the aetiology of the pleural effusion [8]. Exudative pleural effusions typically result from a combination of pleural space inflammation from increased cellular recruitment and decreased lymphatic drainage. Transudative effusions, characterised by low fluid lactate dehydrogenase and protein levels, are the consequence of alterations of the Starling law, which regulates capillary microcirculation and can be observed in such processes as congestive heart failure, renal insufficiency, and hypoalbuminaemia from liver disease or proteinuria. Rarely, pleural effusions may result from the accumulation of extravascular fluid that finds its way into the pleural space, such as in the case of intrapleural misplacement of central venous access (infusothorax), transdiaphragmatic passage of ascites or, rarely, urine in the setting of hydronephrosis (hydrothorax and urinothorax, respectively) or chyle (chylothorax) [9, 10]. Invariably, any given case of pleural effusion may be multifactorial and can incorporate a combination of the above mechanisms.
Epidemiology
Pleural effusions represent the end result of a variety of clinical conditions, which vary based on patient characteristics and local disease patterns. There are an estimated 1.4 million cases of pleural effusions annually in the United States, with an estimated incidence of pleural effusion in the developed world of 320 cases per 100 000 persons per year [11]. There are no obvious gender predilections, and men and women seem to be affected equally. Pleural effusions are much less common in children, where they are primarily due to infectious aetiologies [12].
Diagnosis
Pleural effusions are sometimes clinically asymptomatic and discovered incidentally on routine imaging. When symptomatic, they result in varying degrees of breathlessness, felt to be the consequence of diaphragmatic dysfunction due to the weight of the column of fluid, according to the length–tension inappropriateness theory [13]. CXR typically serves as the initial evaluation for pleural effusion. At the time of diagnosis, a minority of cases are found to be bilateral on CXR, which typically results from congestive heart failure [14]. Effusion characteristics can vary widely based on effusion aetiology and chronicity. The fluid character may range from viscous and loculated to thin and free flowing. The variability in fluid volume and character can significantly affect findings on physical examination, often yielding physical examination inferior to CXR for detection of pleural effusions [15]. TUS has, however, been shown to be superior to both CXR and physical examination for detection of pleural effusion. It can provide immediate valuable information at the bedside on the character, volume and complexity of the pleural effusion not typically evident on conventional radiographic imaging [15–17]. TUS serves a key role in pleural effusion evaluation, as fluid echogenicity, diaphragmatic motion and the appearance of the pleura are all important considerations in investigating the aetiology of an effusion and planning the subsequent diagnostic and therapeutic steps.
Sonographic characteristics of pleural effusions
Basic principles
A basic understanding of US image appearance is required for adequate pleural effusion evaluation on TUS. On US, fluid or structural characteristics such as density affect the sonographic appearance of the structure in question; this appearance is referred to as echogenicity. Unimpeded passage of US through tissue is associated with a lack of echoes, rendering the images hypoechoic (grey) or anechoic (black), for example as seen in a simple effusion. Increasing complexity and density of material increase the echogenicity and may be uniform or heterogeneous; thus, proteinaceous fluid contains uniform internal echoes rendering the fluid grey or white (hyperechoic) on the image. US is reflected by air and cannot penetrate it; gas interfaces produce a bright linear interface with disorganised, irregular bright shadowing distal to the line, which is simply an absence of echoes and not amenable to interrogation.
Simple effusion
Simple effusions are characterised by a free-flowing consistency and lack of loculations. On US, these effusions are found as homogeneous hypoechoic fluid collections just deep to the chest wall [18]. Compressed lung can be visualised as a moderately hyperechoic structure on the far side of the fluid collection. The diaphragm is visualised as a hyperechoic rounded stripe on the inferior border of the pleural effusion (figure 1). Transudative effusions, such as those due to cardiac or renal disease, are most commonly simple.
Figure 1 . A simple pleural effusion with echogenic contents, in this case a transudate. Note that atelectasis (arrow) has a texture similar to liver (*).
The ability of US to discriminate between transudative and exudative effusions was evaluated in a small prospective cohort of patients with pleural effusions [19]. This study demonstrated that anechoic effusions could be either transudates or exudates, but transudates were always anechoic. Echogenic effusions were always exudates. As would be expected, complex-appearing or septated effusions were indicative of exudates. Finally, homogeneous echogenic effusions were due to empyema or haemorrhage [19]. Categorisation of effusion based on US appearance is generally described as follows: anechoic, complex septated, complex nonseptated or homogeneous nonseptated.
Complex effusion
Complex effusions are characterised by loculations (collections of fluid that do not follow gravity) and septations (fibrin strands) and are typically not free flowing. On US, the appearance of complex effusions is characterised by heterogeneous fluid collections with interspersed hyperechoic tissue strands. These effusions are typically composed of cellular material, which can organise into fibrinous or proteinaceous strands of cellular debris called septations (figure 2). These septations can ultimately result in the compartmentalisation of the pleural effusion into several smaller locules, which may or may not communicate with one another. Effusion complexity is variable, and can range from relatively mild with only a few loculations to severe complexity with a substantial loculation burden and intense heterogeneity of the fluid collection on US. Exudative effusions, such as those due to malignancy and infection, are often complex. Effusion chronicity also appears to be important in terms of development of a complex effusion. A simple effusion, if left untreated for a substantial period of time, may develop loculations [20].
