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Pediatric Malignant Pleural Effusion
Introduction
The pleural cavity is the space between the parietal and visceral pleura of the lungs. The pleura is a serous membrane that folds upon itself to create a 2-layered structure. An inner layer covers the surface of the lungs called the visceral pleura. The outer layer is the parietal pleural attached to the chest wall.[1][2] Pleural fluid is a small amount of fluid (a few milliliters) in the pleural cavity controlled by the starling forces.[3][4] Pleural fluid is regulated by a balance in the oncotic and hydrostatic pressures between the pleural space and the intravascular components coupled with the perilymphatic drainage.[5][6][7]
Malignant pleural effusion (MPE) is the accumulation of pleural exudate and the presence of malignant cells within the pleural fluid.[8] In MPEs, cancer cells infiltrate into pleural tissue; therefore, pleural tissue invasion by malignant cells is evident on pleural biopsy, and positive fluid cytology is predicted.[9] Up to 15% of patients with cancer develop malignant MPEs.[10] The majority of MPEs result from metastatic disease, with lung cancer being the most common cause in men and breast cancer in women, both combined accounting for 50% to 65% of MPEs.[8] Lymphoma is the most common pediatric malignancy associated with pleural effusion. Mesothelioma, the most common type of primary pleural tumor, is associated with MPE in over 90% of cases.[11] Generally, the presence of an MPE implies a poor prognosis with a median survival ranging from 3 to 12 months.[12][13][14]
Etiology
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Etiology
The third leading etiology of pleural effusion in the pediatric population is malignancy. MPE can develop due to the direct invasion of the pleural wall, impairment of lymphatic drainage from the pleural cavity, or obstruction of the bronchial tree with the development of bronchial obstruction and atelectasis.[15][16] Pleural effusion secondary to malignancy can be unilateral or bilateral.
Various primary or metastatic malignancies can cause pleural effusion in children, including lymphomas, leukemias, and pulmonary tumors.
Lymphoma
Lymphoma is the most common malignancy associated with pleural effusion. About 13 % of all childhood malignancies are attributable to lymphoma. Lymphomas are also the most common cause of anterior mediastinal mass in children. Approximately 60% of lymphomas are non-Hodgkin lymphoma, while the remaining 40% are Hodgkin lymphoma. About 5% of Hodgkin or non-Hodgkin lymphoma patients will develop pleural effusion.[17]
Leukemia
T-cell lymphoblastic leukemia can also result in MPE. In 50% to 70% of lymphoblastic leukemia, pleural effusion will develop. Bone marrow biopsy is necessary to differentiate between leukemia and lymphoma.[18]
Germ Cell Tumor
Germ cell tumors account for about 20% of all anterior mediastinal masses in children.[19] Pathological classifications consist of teratomas and non-teratomatous germ cell tumors. Non-teratomatous germ cell tumors are rare malignant tumors that predominantly occur in young males, most commonly affecting the anterosuperior mediastinum. Encroachment into adjacent structures in the mediastinum can cause respiratory symptoms. Compression of the tracheobronchial tree and obstruction of lymphatic flow by these tumors can result in pleural effusion.[20]
Neurogenic Tumor
Neuroblastoma and ganglioneuroma make up about 90% of the posterior mediastinal mass. Growth and expansion can cause mass effects, respiratory distress, and cord compression. Neurogenic tumors generally do not cause pleural effusion.[21]
Primary Malignant Lung Neoplasms
Primary lung tumors are rare in childhood. The most common primary malignant pediatric lung neoplasms are carcinoid tumors (63%), followed by mucoepidermoid carcinoma of the lung (18%).[22] Carcinoid tumors account for about 80% to 85% of all tracheobronchial tumors in children. They can cause compressive atelectasis and pneumonia that can lead to the development of an effusion.
Pleuropulmonary Blastoma
Pleuropulmonary blastomas are rare tumors that occur during early childhood. These neoplasms are embryonal, mesenchymal tumors originating from the lung and pleural cavity. Diagnosis of a pleuropulmonary blastoma malignancy is often late. Therefore, this tumor can invade adjacent structures, causing pneumonia, spontaneous pneumothorax, and effusion.[23]
Askin Tumor
An Askin tumor is a rare form of Ewing Sarcoma or primitive neuroectodermal tumor that can arise from the bones of the rib chest wall or lungs. The prognosis is poor in patients with Askin tumors. The tumor can invade adjacent structures like muscle ribs, pleura, and the lungs and cause mass effects, with compression of nearby organs and the development of pleural effusion.[24]
Epidemiology
The following 3 conditions are the primary causes of pleural effusion in children:
Lymphoma is the most common childhood malignancy associated with pleural effusion, with non-Hodgkin lymphoma accounting for the majority of cases.[27][28]
Pathophysiology
The visceral pleura receives blood supply from bronchial circulation, while the parietal pleura receives its supplies from the intercostal arteries; therefore, the 2 layers are 2 distinct anatomic structures. The visceral pleura has no sensory nerves; on the contrary, the parietal pleura has a rich network of sensory nerves, making it very sensitive to painful stimuli. The pleural cavity aids in the mechanics of inspiration and expiration during breathing. Kampmeier's foci are a collection of lymphoreticular and mesothelial cells that act as a "guard" by preventing the entry of undesirable substances from the pleural cavity into the media in the chest wall and mediastinum.[29] Most of the cellular content of the pleural fluid consists of macrophages and lymphocytes.[30] The composition of fluids and the number of cells in the pleural space can change considerably in pathologic conditions.
MPE occurs due to disrupted homeostatic forces that control fluid flow in and out of the pleural cavity. The pressure in the pleural cavity is determined by the opposing forces of the elastic recoil of the lung and the pressure from the chest wall. The pleural fluid is not in a state of hydrostatic equilibrium because the vertical gradient of the pleural fluid pressure is not equal to the hydrostatic pressure. This helps to create fluid movement in the pleural cavity. Pulmonary and cardiac mechanics also control the net movement of fluid in the pleural cavity. The fluid in the pleural cavity is an ultrafiltrate from the parietal pleura capillaries. The amount of fluid in the pleural cavity is regulated by a filtration rate matched by fluid outflow via the lymphatic stomata.
For the development of pleural effusion in malignancy, the following must occur:
- An increase in the production of pleural fluid secondary to increased hydrostatic pressure
- Decreased oncotic pressure or pleural pressure
- Increased the permeability of the microvasculature [31]
The increased pleural fluid production must exceed the lymphatic clearance, either due to decreased hydrostatic pressure or blocked lymphatic drainage.
The major contributing factors in the MPE formation are angiogenesis and vascular remodeling.[32] Immune responses within the MPE alter the angiogenesis and vascular remodeling pathways.[33] In MPE, macrophages regulate T cell proliferation and differentiation by releasing IL-1β, IL-8, and TNF-α.[32] Tumor-associated macrophages promote the growth and prevent apoptosis of malignant cells.[34][35] Tumor-associated macrophages also promote angiogenesis by releasing chemokines, cytokines, and growth factors.[36] Tissue injury signals are driven by the release of chemokines and cytokines, resulting in the recruitment and activation of neutrophils, mast cells, dendritic cells, and natural killer cells.[32]
Histopathology
Small round cell tumors, including Ewing and rhabdomyosarcoma, are the most common malignancies involving pediatric body fluids and serosal surface involvement. Small round cell tumors reveal a consistent morphology characterized by clusters of small round cells with central nuclei, scant cytoplasm, and frequent small vacuoles. While immunocytochemistry is valuable for accurate diagnosis, additional ancillary studies may be required, especially in hematologic malignancies.[37]
History and Physical
The history and physical examination can help diagnose pleural effusion, prompting imaging and laboratory workup to confirm MPE. Common presenting clinical features are fever, malaise, weakness, chest pain, weight loss, cough, and dyspnea.[38][39] Dyspnea can be due to reduced chest wall compliance, atelectasis, or mediastinal shift.[40]
Children may present with tachycardia, tachypnea, and diaphoresis on physical examination. Tachypnea can range from mild respiratory distress to respiratory failure. Breathing is typically shallow due to pleuritic pain. Dullness on percussion decreased, or absent breath sounds, reduced chest expansion, and pleural rub may be appreciated on the side of MPE.[41] Pleuritic chest rub might gradually disappear as the accumulation of pleural fluid increases. Excessive fluid accumulation can cause displacement of the cardiac apex and the trachea to the contralateral side. The presence of chest mass, lymph nodes, or signs of superior vena cava obstruction are essential findings to suspect malignancy.
Evaluation
A detailed history and thorough physical examination should be performed when MPE is suspected. Imaging is crucial to diagnose and assess the extent of the pleural effusion and to plan invasive procedures. Chest x-ray and ultrasonography are quickly available diagnostic tools. A pleural tissue biopsy for the histological exam is needed for a definitive diagnosis and to guide treatment.
Imaging Studies
Chest x-ray
In most cases, a chest x-ray can help to confirm the size and location of the pleural effusion. Radiographic findings of pleural effusion include meniscus sign, blunting of the costophrenic angle, obscured heart border or hemidiaphragm, and shifting of the mediastinum to the other side. It might not be able to delineate a small effusion. X-ray findings of solitary or multiple nodules, pleural opacities, atelectasis, consolidation, massive effusion, and hilar enlargement suggest malignancy.[42]
Ultrasonography
Thoracic ultrasound has more than 90% sensitivity and specificity in detecting pleural effusion.[43] It can detect small effusions, differentiate between consolidation and pleural thickening, and assist in diagnostic and therapeutic procedures. It reduces the risk of complications during the procedure and can detect post-procedural complications. The presence of pleural thickening of >10 mm, diaphragmatic wall thickening of >7 mm, and pleural nodularity have almost 100% specificity in diagnosing malignancy.[44] Metastatic tumors are generally multiple, hypogenic to moderately echogenic, and can have circular, nodular, or broad-based shapes with frondlike protrusions.[45]
Computed tomography scan
CT scan is a valuable imaging study with around 78% specificity and 68% sensitivity for identifying MPE with a positive and negative predictive value of 80% and 65%, respectively.[46] It can determine the size, location, and extent of the effusion. A CT scan can also help identify the primary or metastatic tumor causing the effusion. Lung parenchymal and lymph node involvement is better detected by CT scan. CT scan findings suggestive of malignancy include circumferential pleural thickening, pleural nodularity, parietal pleural thickening >1 cm, and mediastinal pleural involvement.[46]
Magnetic resonance imaging
Because of poor spatial resolution, magnetic resonance imaging (MRI) is limited in diagnostic imaging studies for pleural effusion. It provides high-quality images of soft tissue and is sensitive in detecting the tumor involvement of the diaphragm and chest wall.[47]
Positron emission tomography (PET)
Positron emission tomography (PET)-CT scan for the workup of MPE is not routinely performed. False-positive results can occur in conditions like parapneumonic effusions and following pleurodesis, while the early disease can result in false-negative results.[48] The TARGET trial did not support using PET-CT to guide pleural biopsies in patients with a prior non-diagnostic biopsy. The diagnostic sensitivity in the CT-only group was higher, and results supported the approach of repeating a CT-guided biopsy when clinical suspicion of malignancy remains after an inconclusive result.[49]
Pathological Examination
Histopathological examination is crucial for the diagnosis and can be performed by pleural thoracocentesis and analysis of pleural fluid, pleural biopsy, and thoracoscopy.
Pleural thoracocentesis
Thoracocentesis is a valuable test that can serve both diagnostic and therapeutic purposes. The pleural fluid should be analyzed for pH, protein, glucose, lactate dehydrogenase (LDH), red and white blood cells, neutrophils, basophils, eosinophils, and pleural fluid adenosine deaminase.[31][50] Hemorrhagic or exudative drainage should raise a high index of suspicion for malignancy. Pleural effusion is identified as an exudate in malignancy according to Light's criteria with a ratio of the pleural fluid protein to serum protein >0.5, a ratio of the pleural fluid LDH to serum LDH >0.6, and LDH of the pleural fluid that is more than two-thirds the upper limit of serum LDH.[51][52] Lymphocyte count is usually above 50% to 70%, pH <7.3, and glucose <50 to 60 mg/dL. MPE can be transudative in 5% to 10% of the cases.[53]
Cytology is the definitive method for diagnosing MPE, with a diagnostic accuracy of approximately 60%.[46] The diagnostic yield depends on the number of specimens taken, type of fixative solutions, time of specimen transportation, expertise of cytopathologists, histopathology of the specimen, extent of the disease, type of primary malignancy, and the use of cell blocks.[54][55][56] The sensitivity of cytology in diagnosing MPE varies significantly depending on the type of cancer, ranging from 6% for mesothelioma to 80% for adenocarcinomas.[57] Immunohistochemistry can help differentiate adenocarcinoma from mesothelioma.
The pleural fluid can also be analyzed for tumor markers. This is more commonly done in adults with pulmonary, breast, colon, ovary, and prostate cancer. Tumor markers are useful as an adjunct in clinical diagnosis, identification of metastases in the pleural cavity, and identification of the malignancy's primary origin. Some of the common tumor markers are carcinoembryonic antigen (CEA), carbohydrate antigen 15-3 (CA 15-3), cytokeratin 19 fragments (CYFRA 21-1), cancer antigen 125 (CA-125), CA 72-4, carbohydrate antigen 19-9 (CA 19-9), stage-specific embryonic antigen-1, and nonspecific enolase.[58][59]
Pleural biopsy
Pleural biopsy is the gold standard for diagnosing MPE and pleural malignancy.[14] False-negative results can occur, and needle biopsy of pleural tissue combined with fluid cytology of MPE can aid in diagnosis. The procedure can be done under local or general anesthesia, and CT or ultrasound-guided pleural biopsy increases the diagnostic yield.
Medical thoracoscopy and video-assisted thoracoscopic surgery
Both procedures allow for direct visualization and biopsy of the tumor. Medical thoracoscopy can be performed with local anesthesia or moderate sedation and is a less invasive procedure than video-assisted thoracoscopic surgery (VATS). The reported sensitivity of medical thoracoscopy for diagnosing malignant disease is 92.6%.[60] Using ultrasound before medical thoracoscopy enhances visualization of the pleural space and has become an integral part of routine practice. VATS is usually performed under general anesthesia with single-lung ventilation. Complications of thoracoscopy are hemorrhage, bronchopleural fistula, pneumothorax, empyema, postoperative fever, wound infection, dysrhythmias, and pneumonia.[61]
Treatment / Management
Managing malignant pleural effusion requires an interprofessional approach with coordinated care between a pediatric oncologist, a pediatric surgeon, and an interventional radiologist. The primary goal of the treatment is to relieve the symptoms and improve the quality of life. The most common cause of MPE in a pediatric population is non-Hodgkin lymphoma, and the first step in management involves administering targeted chemotherapy for the primary malignancy. Asymptomatic and small effusions can be observed and usually do not require interventions.[62] Thoracentesis is performed in symptomatic patients with large MPE and may require repeated procedures and other alternative interventions.(B3)
Thoracocentesis
Therapeutic thoracocentesis is the first step in the management of symptomatic patients. The goals of the procedure are the removal of pleural effusion, clinical improvement in symptoms, and the prevention of fluid reaccumulation.[63] Thoracocentesis for MPE is for both diagnostic and therapeutic purposes. Moderate to large MPE causes respiratory compromise and difficulty breathing. Mild effusion can be monitored with serial x-rays and chest ultrasound while the patient is undergoing chemotherapy. Thoracocentesis using the Seldinger technique can be utilized for moderate to large effusion. For patients with large pleural effusion, slow removal of the fluid is recommended, as aggressive removal of pleural fluid might lead to the reexpansion of pulmonary edema, which can also compromise the patient's respiratory status.
In the absence of improvement following the thoracocentesis, alternative causes of dyspnea, including nonexpandable lungs, severe cardiopulmonary failure, pulmonary thromboembolism, restrictive or constrictive cardiomyopathy, tumor-induced airway obstruction, and lymphangitic cancer, should be considered.[64] In cases with symptom improvement, patients should still be monitored for the clinical recurrence of dyspnea and chest pain. Any clinical evidence of recurrence dictates the follow-up with a chest x-ray, chest CT, or chest ultrasound. The recurrence of pleural effusion should be differentiated from the alternative causalities, including but not limited to nonexpandable lungs and severe cardiopulmonary failure.(B3)
Patients with recurrent MPE after thoracocentesis and systemic chemotherapy should be evaluated for intrapleural catheter placement and drainage or pleurodesis.
Tube Thoracostomy
A tube thoracostomy can be performed under local anesthesia or moderate sedation for patients with a short life expectancy and recurrent MPE or very young patients. A 7- to 16-F chest tube can be utilized for drainage. The tube is usually inserted in the fourth or fifth intercostal space along the anterior or middle axillary line. It should not be in place for too long because of the risk of infection, bleeding, or pneumothorax.
Chest tube or small-bore catheter drainage is considered an alternative to large-volume thoracocentesis. Chest tube drainage might be specifically performed in patients with large fluid volumes. A consistent and slow rate of pleural fluid removal must be planned for this group of patients.[65]
Pleurodesis
Pleurodesis involves obliterating the pleural space to prevent the reaccumulation of pleural effusion. Pleurodesis is considered for patients who are not candidates for pleural catheter placement or have not responded to systemic chemotherapy. The exact mechanism remains unclear, but inflammation or fibrosis, mediated by the activation of transforming growth factor beta, is believed to play a critical role.[66] Pleurodesis can be performed by using chemical agents or mechanical abrasion. Several agents can be used for pleurodesis, including bleomycin, talc, tetracycline, Corynebacterium parvum, etoposide, iodopovidone, quinacrine, and interferons.[67](B3)
Talc is the most common agent used because of its low cost and easy availability. In a Cochrane meta-analysis, talc was more efficacious than other sclerosants.[68] Talc can be administered during thoracoscopy either by using an atomizer (talc poudrage) or in suspension form (talc slurry) through a chest tube.[67] Respiratory distress, fever, and chest pain are some of the complications of intrapleural talc. (A1)
Tunneled Pleural Catheter
A tunneled pleural catheter (TPC) is a silicone tube tunneled subcutaneously and placed in the pleural space. The tunneled subcutaneous portion has a small cuff, and the part of the tube coming out of the chest has a 1-way valve. TPC allows the patient or the caregiver to drain the fluid at home or in the outpatient setting. It improves the quality of life, with symptom improvement in 80% to 90% and spontaneous pleurodesis in 45.6% of the cases.[69] Some of the complications of the procedure are pneumothorax, bleeding, infection, catheter obstruction, empyema, and tumor dissemination along the catheter tract.[70] TPC is a less invasive procedure than pleurodesis, decreases hospital stay, and is the first choice for patients with nonexpandable lungs.[31](A1)
Pleuroperitoneal Shunt
Pleuroperitoneal shunt is a palliative measure that can be used for patients who are not candidates for pleurodesis. The procedure creates a chronic drainage system that connects the pleural and peritoneal cavity. A pleuroperitoneal shunt is an invasive procedure with higher chances of infection and blockage than TPC and, therefore, is rarely used in the pediatric population and only as a palliative measure in adults. A pleuroperitoneal shunt procedure is not yet part of the standard management pathway or recommendations.[71](A1)
Differential Diagnosis
The differential diagnosis of MPE should include other causes of pleural effusion. In pediatrics, the most common cause of pleural effusion is an infection. This is usually pneumonia with parapneumonic effusion. Pleural effusion from congestive heart failure should also be considered, as fluid can accumulate in the pleural cavity from heart failure.[72] Most of the heart failure in the pediatric population is from congenital heart disease.[73]
Chylothorax can develop in pediatric patients with congenital heart disease after surgery. This might be due to injury to the thoracic duct, venous or lymphatic congestion, or central venous thrombosis.[74] Chylous fluid with a milky white appearance can accumulate in the pleural fluid and cause significant effusion with respiratory compromise.
A detailed history and physical examination can help the clinician make a differential diagnosis. Ancillary studies can assist with the history and physical examination. Thoracocentesis with the pleural fluid analysis is especially useful. The Lights criteria can differentiate between exudate and transudate. The glucose level in the pleural fluid is similar to the level in the plasma. The pleural fluid glucose level in MPE is usually <60 mg/dL, and the pH is generally <7.3. Pleural effusion secondary to infection is exudative, while effusion from heart failure is transudative. Distinguishing between the 2 types of effusion in MPE can be difficult; however, the pleural fluid is exudative in nearly 95% of the MPE cases. Analysis of pleural fluid for malignant cells can sometimes be helpful, albeit with false positive results. The pleural fluid can be evaluated for tumor markers to help identify the primary tumor causing the effusion.[75]
Prognosis
Prognosis is generally poor in patients with MPE. Studies have shown that mortality in patients with MPE is higher than in patients with malignancy without MPE.[76][77] MPE is associated with advanced and metastatic malignancies, with median survival ranging from 3 to 12 months, depending on other factors.[78] The prognosis depends on the tumor type and stage, age, response to the therapy, and other medical conditions. Pleural fluid pH of <7.2, glucose <60 mg/dL, elevated LDH, and elevated vascular endothelial growth factor are associated with poor prognosis.[79] Patients with hematologic malignancies and malignant mesothelioma have a better prognosis and survival range as compared with patients with lung and gastrointestinal malignancies.
Complications
The most common complications from MPE are respiratory distress and respiratory failure. The risk of respiratory failure or cardiovascular collapse is high if MPE is caused by a mediastinal mass compressing the trachea and other vital organs in the mediastinum.
Consultations
Management of MPE requires coordination of care between several subspecialties. The hematologist-oncologist plays a critical role in the establishment of the initial diagnosis of the tumor and initiation of chemotherapy and/or radiation therapy. Management of the MPE depends on the effusion's size, type, and location. Thoracocentesis, thoracotomy, pleurodesis, and placement of a tunneled pleural catheter are the surgical treatment options for MPE, requiring the involvement of either a pediatric surgeon, a cardiothoracic surgeon, or an interventional radiologist. Palliative care and rehabilitation teams are essential in managing patients with MPE.
Deterrence and Patient Education
Deterrence of pediatric MPE primarily involves early detection and management of underlying malignancies, such as lymphoma, which is the most common cause in children. Routine health check-ups, awareness of early symptoms like persistent cough, unexplained weight loss, or respiratory distress, and prompt medical evaluation can aid in early diagnosis and intervention. Clinicians should emphasize the importance of timely cancer screening and monitoring in high-risk pediatric patients to prevent complications associated with MPE.
Patient education is crucial in managing pediatric MPE, ensuring caregivers understand the condition, its symptoms, and treatment options. Families should be informed about the significance of follow-up care, adherence to chemotherapy or other cancer treatments, and recognizing warning signs of worsening pleural effusion, eg, increased difficulty breathing or chest pain. Clear communication about available treatment strategies, including thoracentesis, pleurodesis, or tunneled pleural catheter placement, can help caregivers make informed decisions. Providing psychological support and addressing concerns about prognosis and quality of life is also essential to patient-centered care.
Enhancing Healthcare Team Outcomes
Effective management of pediatric MPE requires a collaborative, interprofessional approach to ensure patient-centered care, improved outcomes, and enhanced patient safety. Physicians, including pediatric hematologist-oncologists, pediatric surgeons, and interventional radiologists, play a central role in diagnosing and treating MPE. The hematologist-oncologist determines the appropriate chemotherapy regimen to target the underlying malignancy, while surgeons and radiologists perform procedures such as thoracentesis, pleurodesis, and tunneled pleural catheter placement to relieve symptoms and manage fluid accumulation. Advanced practitioners assist in monitoring treatment response, managing complications, and providing ongoing patient and family education. Their role in early symptom recognition and intervention helps prevent disease progression and improve quality of life.
Nurses, pharmacists, and other healthcare professionals are integral to optimizing care coordination and ensuring seamless communication between team members. Oncology nurses provide essential bedside care, monitor respiratory status, manage pain, and educate families on postprocedural care. Pharmacists contribute by ensuring appropriate chemotherapy dosing, managing drug interactions, and providing guidance on supportive medications to alleviate symptoms. The palliative care team, including pain specialists and social workers, plays a crucial role in addressing symptom relief, emotional support, and end-of-life care when necessary. Clear and continuous communication among all clinicians is vital to preventing treatment delays, avoiding errors, and ensuring a unified approach to patient management. Regular interprofessional meetings, shared electronic health records, and direct collaboration between specialists enhance team performance, improve patient safety, and support the best possible outcomes for children with MPE.
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