Chylous Ascites and Lymphoceles: Evaluation and Interventions

Abstract

Kinmonth introduced lymphangiography in 1955 and it became an important tool in the diagnosis and treatment of malignant disease. The technique, based on bipedal approach, was difficult and time-consuming which limited its use in clinical practice. Cope is the father of percutaneous lymphatic interventions and he was the first person to access and intervene on the lymphatic system. After his initial work published on 1999, there has been an expansion of the lymphatic embolization techniques, particularly since the development of intranodal lymphangiography and advance lymphatic imaging. This article is focused on the evaluation and management of postoperative chylous ascites and lymphoceles. Their incidence is growing due to longer survival of cancer patients and more radical surgical approaches, leading to an increased morbidity and mortality in this patient population. Minimally invasive percutaneous lymphatic embolization is becoming a first-line therapy in patients with postoperative lymphatic leakage.

Chylous Ascites: Management and Interventions

Chylous ascites (CA) is a rare form of ascites that results from the leakage of lipid-rich fluid into the peritoneal cavity. ^{1 2 3} It usually happens due to trauma and rupture of the lymphatics or increased peritoneal lymphatic pressure secondary to obstruction of the lymphatic system or one of its tributaries producing ascites with a turbid or milky appearance due to the high triglyceride content. ¹ Morton reported the first case of CA in 1694 in a 2-year-old boy who died with tuberculosis. ⁴ The etiology of CA can be classified as traumatic, congenital, infectious, neoplastic, postoperative, cirrhotic, or cardiogenic. Malignancy and cirrhosis approximately account for two-thirds of all the cases of CA in Western countries. ¹

The incidence of CA has increased due to the prolonged survival of patients with cancer and more aggressive surgical interventions. The prognosis is different depending on the underlying cause. It is associated with high mortality rates (71% at 1 year), up to 90% in patients with cancer. The mortality is lower in patients with congenital diseases, traumatic cases, and postoperative CA. ⁴

Lymph Formation and Anatomy of the Lymphatic System

Lymph consists of cells, particles, proteins, and chylomicrons which arises from the exudation of the plasma and its constituents from capillaries into interstitial compartments of the body. ¹ The lymphatic fluid flows from the lymphatic capillaries into the lymphatic vessels (one-way valves), the lymph nodes, and finally in the lymphatic trunks. The majority of the lymph originates in the liver and intestine. Long chain triglycerides are reduced to monoglycerides and fatty acids in the small bowel, which are absorbed as chylomicrons into the lymphatic system and explains the milky appearance of lymph. ⁵

The anatomy of the lymphatic system runs parallel to the peripheral vascular system. The lymphatic system is present through the body, except in the central nervous system and bone marrow and has several important functions: regulation of the tissue pressure (balance of proteins and interstitial fluid), immune surveillance (defense against foreign particles and microorganisms), and the absorption of dietary fat in the intestine.

The lymphatic system in the abdomen and pelvis includes the lymphatic vessels and the external and common iliac nodes connecting with the retroperitoneal lymph nodes and the lumbar trunks. The cisterna chyli is the abdominal origin of the thoracic duct (TD) and it receives the bilateral lumbar lymphatic trunks as well as the intestinal and the hepatic trunks. It is located in the retrocrural space, to the right side typically at L1–L2 vertebral level. The cisterna chyli ranges from 0.5 to 2 cm in diameter. The TD starts from the cisterna chyli and then enters the thorax through the aortic hiatus of the diaphragm and ascends in the posterior mediastinum between the descending aorta and the azygos vein. It empties into the left jugulo-subclavian junction ( Fig. 1 ). The anatomy of the central lymphatic system is frequently variable. The typical pathway of the TD occurs in 65% of the population due to embryological variations. The central lymphatic system (cisterna chyli and the TD) and the lymph nodes can be reliably identified on thin slice thickness using multidetector row computed tomography (CT). ⁶ In contrast to CT, MR imaging (MRI) can be used to assess lymph nodes as well as the central and peripheral lymphatics. MR lymphangiography can be performed for diagnostic purposes or for preprocedural planning. It can be performed with or without contrast administration into the lymphatic system to delineate the anatomy of the lymphatic system and its disorders involving the chest, abdomen, and extremities. ⁷

Fig. 1.

A 67-year-old patient with history of renal cell carcinoma status post left nephrectomy and lymphadenectomy. The patient developed chylous ascites and she underwent four high-volume weekly paracenteses (> 5 L). ( a ) Intranodal lymphangiography demonstrates a 25-gauge needle (arrowhead) inside the groin lymph node (arrow) and the upstream lymphatics to the pelvis. ( b ) Abdominal radiograph reveals filling of the pelvic and retroperitoneal system with ethiodol extravasation at the level of L4–L5 paraspinal region (arrow) and the lymphatics vessels/node supplying the leak (arrowhead). ( c ) Magnified view of the area of leakage (long arrow) with the lymphatic vessels (arrowheads) and the lymph node (short arrow) supplying the leak. ( d, e ) 22-gauge needle was inserted under fluoroscopy into the lymph node (arrows) closest to the leak (arrowhead). Two oblique projections were performed to confirm the location of the needles tip in the lymph node. Then, glue embolization of the lymph node was performed (dilution 1:3). ( f ) CT scan obtained 1 month after the lymphatic embolization. The patient did not require any paracentesis after the procedure. Note the contrast (glue/ethiodol) retained in the culprit lymph node (arrow).

Pathophysiology and Etiology of Chylous Ascites

CA formation is typically related to the disruption of the lymphatic system. Three basic mechanisms have been described: exudation of lymph through the walls of acquired of congenital vessels into the peritoneal cavity, malignant infiltration of the lymphatic system leading to leakage from the subserosal lymphatics, and direct injury (traumatic or iatrogenic) of the retroperitoneal lymphatics. ⁸ Besides this, patients with portal hypertension and elevated caval pressures can develop CA likely due to increase in the production of hepatic lymph. ^{9 10}

The etiologies of CA can be classified into traumatic and nontraumatic causes and the underlying etiology determines the workup and management. ² The main causes of CA are summarized in Table 1 .

Table 1. Etiology of chylous ascites: traumatic and nontraumatic.

Nontraumatic	Traumatic
Malignancy: 25%  - Lymphoma: 35%  - Stomach, pancreas, esophagus, endometrial: 40%  - Carcinoid and Kaposi: 20%  - Leukemia	Postoperative (% incidence)  - Abdominal surgery: 1.1%  - Retroperitoneal, gastric, esophageal, or cytoreductive surgeries: 7%
Cirrhosis/Portal hypertension: 16%  - Prehepatic (portal vein/splenic vein thrombosis)  - Hepatic (cirrhosis, congenital hepatic fibrosis, venous occlusive disease)  - Posthepatic (Budd-Chiari syndrome, restrictive cardiomyopathy, constrictive pericarditis, congestive heart failure)	Nonsurgical: radiation therapy (% incidence)  - Abdominal/pelvic radiation: 3%
Infection: 15%  - Mycobacterium, filariasis	Non iatrogenic  - Blunt and penetrating abdominal trauma  - Battered child syndrome
Uncommon causes: 23% - Inflammatory, drugs, gastrointestinal disease
Children: lymphatic anomalies: 84%  - Congenital: lymphatic hypoplasia, yellow nail syndrome, Klippel-Trenaunay syndrome, primary lymphatic hyperplasia, intestinal lymphangiectasia

Source: Adapted from Al-Busafi et al, Steinemann et al, and Kass et al. ^{2 9 10}

Clinical Complications and Diagnosis of Chylous Ascites

Loss of the lymphatic fluid in the peritoneal cavity can lead to serious complications due to the depletion of proteins, lipids, immunoglobulins, electrolytes and water. These patients can develop hypoproteinemia, dehydration, electrolyte imbalance, and immunosuppression, which may increase mortality in the postoperative setting. ¹¹

Patients typically present with abdominal distention, weight gain, and shortness of breath and can be associated with anorexia, diarrhea, nausea, enlarged lymph nodes, early satiety, and fever. ^{1 2 8} Paracentesis is the most important tool in evaluating and managing patients with CA. Chyle typically has a cloudy or turbid appearance and should be distinguished from pseudochylous ascites in which the turbid appearance is due to cellular degeneration from infection or malignancy without high level of triglycerides. ¹² Ascitic fluid should be sent for cell count, Gram stain, glucose, lactate dehydrogenase, total protein, albumin, triglyceride level. ¹³ The serum-to-ascites albumin gradient should be calculated to determine if the ascites is related to portal hypertension or other causes (> 1.1 g/dL in CA secondary to cirrhosis). ¹³ In patients with suspected tuberculosis, adenosine deaminase activity should be performed. Many studies have established elevated triglyceride levels as the best parameter for diagnosis of CA. The current consensus utilizes a cutoff value of > 200 mg/dL as the criteria for the diagnosis of CA. ^{14 15}

Imaging Studies in Chylous Ascites

CT scan of the abdomen can detect abdominal masses and lymph nodes that can be present in patients with CA. Besides that, it may be helpful to identify the location of the lymphatic injury in the setting of postoperative or traumatic CA. On CT, CA is indistinguishable from water on density measurements but fat-fluid levels are common. ¹⁶

Lymphoscintigraphy (LS) can be used to detect abnormal lymphatic drainage in patients with CA. It can be repeated several times with no adverse events. LS can accurately identify the sites of lymphatic leak. ¹ The addition of SPECT/CT to planar images can deliver relevant information regarding the anatomic localization of the lymphatic leakage, which can help planning surgical or percutaneous interventions. Weiss et al reported an overall sensitivity of LS in the detection of thoracoabdominal lymphatic transport disorders of 88%. ¹⁷

MRI often demonstrates signal dropout on fat-saturated sequences due to the high fat content of CA. The use of MR lymphangiography and dynamic contrast-enhanced MR lymphangiography (DC-MRL) with inguinal lymph node injection has been increasing as an alternative to traditional invasive lymphangiography. DC-MRL produces good images of the central lymphatic system as well as the flow of the contrast up to the central ducts. ^{7 18} This technique can be used in evaluating children with plastic bronchitis, neonatal lymphatic flow disorders, nontraumatic chylothorax, identification of the source of CA, and clarifying the anatomy of lymphatic malformations. In addition, it is helpful for planning lymphatic embolization or alternative percutaneous interventions depending on the lymphatic anatomy. ^{19 20 21} Nadolski et al reported nine patients who underwent DC-MRL in the setting of CA demonstrating lymphatic leakage in seven patients all of which had traumatic etiology. ²²

Lymphangiography is an important technique for the detection and treatment of lymphatic leaks. The development of intranodal lymphangiography (INL) has simplified the access to the lymphatic system. ²³ Under ultrasound guidance, the groin lymph nodes can be accessed with a 25-gauge needle. The tip of the needle is placed at the corticomedullary junction and ethiodized oil is injected into the lymphatic system. The contrast is followed under fluoroscopy and spot radiographs through the pelvis and retroperitoneal lymphatic vessels/lymph nodes to the upper abdomen, draining in the cisterna chyli and TD. The most common findings on lymphangiography are contrast extravasation due to a lymphatic leak and lymphatic obstruction. Studies have reported a detection rate of 55% for leakage sites in patients with CA. ^{22 24} This rate is lower compared with those patients with chylothorax. Anatomically, the intestinal and the hepatic lymphatic ducts that carry the chyle to join lumbar ducts or the cisterna chyli are often outside the pathway of the contrast that is injected in the groin lymph nodes. ²² To overcome this limitation of the INL, several techniques have been proposed to perform retrograde access of the TD in an attempt to identify leaks in the upper abdomen and distal intestinal lymphatics: transvenous catheterization, cervical percutaneous access (under ultrasound or fluoroscopy guidance), and snaring a wire previously inserted in the TD from an anterograde approach into the venous system. ^{24 25 26}

Lymphangiography has a therapeutic role in patients with chylous leaks due to the embolic properties of the ethiodized oil. It is hypothesized that this contrast can slow the lymphatic flow down and its accumulation at the leakage point may induce an inflammatory reaction. ²⁷ The therapeutic effect of lymphangiography is volume dependent and its efficacy is higher in patients with lymphatic leakage with low-output leaks. Alejandre-Lafont et al reported that the leak could be occluded in 70% of the patients in which the output was less than 500 mL/day and in 35% of the patients with more than 500 mL/day. ²⁷ Gruber-Rouh et al reported that the lymphatic leak could be occluded in 96.8% of the patients with lymphatic drainage volume less than 200 mL/day. ²⁸

Lymphatic leakage from the hepatic lymphatics into the abdominal cavity (hepatic lymphorrhea) is a very rare condition apparently as a consequence of liver surgery particularly requiring nodal dissection within the hepatoduodenal ligament. ^{29 30} Hepatic lymphorrhea can cause massive ascites. There are two pathways in the hepatic lymphatic system: along the hepatic veins (upstream flow) and along the portal system toward the hepatoduodenal ligament (downstream flow). The hepatic lymphatic flow is approximately 0.25 mL/min, which is significantly higher in patients with cirrhosis. ³⁰ Percutaneous transhepatic lymphangiography can be attempted to identify the leakage. The lymphatic vessels run parallel to the portal vein; so, the Chiba needle should be placed parallel to the wall of the peripheral portal vein to fill the hepatic lymphatic vessels. The hepatic lymphatic vessels are easy to identify due to its beaded appearance and the presence of valves. ³¹

Management of Chylous Ascites

Treatment options for CA include dietary measures, drugs, and surgical or percutaneous interventions. ¹ Treatment of the underlying cause is critical to adequately manage these patients.

The goal of nutrition therapy is to decrease the production of chyle, replace fluid and electrolytes, and maintain the nutrition status. ³² Dietary measures for patients with symptomatic CA include high-protein and low-fat diet with medium-chain triglycerides. Patients with cirrhosis should be managed with low-sodium diet and diuretics. ² Patients who do not respond to these measures should be started on total parenteral nutrition. Several medications (Orlistat, somatostatin, octreotide, and etilefrine) have been used to reduce the production/volume of chyle. These drugs can be used alone or in combination with TPN and are effective in the management of CA due to different causes. ^{2 33}

Percutaneous Interventions in Patients with Chylous Ascites

The percutaneous armamentarium in the treatment of CA comprises different techniques such as paracentesis, transjugular intrahepatic portosystemic shunt (TIPS), peritoneovenous shunting (PVS), and lymphatic embolization. This part of the article will focus on advanced lymphatic interventions for the treatment of CA.

Paracentesis has a twofold role in patients with CA: diagnostic and palliative. Paracentesis could be repeated as needed and is typically combined with other conservative measures. Repeated large-volume paracentesis may be a reasonable option for patients with end-stage liver disease who are not candidates for medical or other percutaneous treatments. ^{1 2} Despite that, repeated drainage of patients with CA can lead to immunosuppression with higher risk of infection and increased nutritional requirements. ³⁴

TIPS has been successfully used in patients with cirrhosis and CA or chylothorax, particularly in cases with acceptable liver function. ³⁵ TIPS can reduce the lymphatic hypertension besides the portal pressure. ³⁶ Reported patency rate after TIPS placement with current stent technology is 75% at 2 years. ³⁷

PVS was considered an option for patients with CA refractory to medical treatment and poor candidates for surgery. In the past, they were associated with high rate of serious complications. ¹ Nowadays, the safety and efficacy of Denver shunts in patients with malignant ascites and ascites in cirrhotic patients has been reported in different articles. ³⁸ PVS is based on a two-catheter limbs with an interposed unidirectional valve. One limb is inserted into the peritoneal cavity and the other limb in the superior vena cava via internal jugular vein. The shunt functions by returning the chylous fluid back to the venous system to improve the hemodynamic, nutritional, and immunological status. ³⁹ In the largest study published with 28 patients with iatrogenic CA (any cancer etiology), Denver shunt was successful in 92% of the patients. ⁴⁰ Based on unpublished data from our institution, PVS permanently resolved CA in patients with urological malignancies who underwent retroperitoneal lymph node dissection in 90% of the cases. Shunt occlusion was the most common complication (30%). The risk of complications increased when the shunt placement was delayed by more than 70 days after the surgery or when the patient had more than five paracenteses. Disseminated intravascular coagulopathy has been reported between 2 and 10%. ⁴¹

Lymphatic Interventions in Patients with Chylous Ascites

Dr. Constantine Cope was the father of the lymphatic interventions. He envisioned thoracic duct embolization (TDE) as a minimally invasive treatment for patient with chylous effusions and as an alternative to TD ligation. ^{42 43} Due to his work, TDE has become the preferred intervention for the treatment of chylothorax and this procedure is supported by multiple studies. ^{43 44 45}

After the development of INL in 2011, ²³ there has been a revival of the lymphatic interventions and expansion of the lymphatic embolization approaches. This development has allowed treating hepatic lymphorrhea, protein loosing enteropathy, and CA. ²⁰

Results of Lymphatic Interventions in Patients with Chylous Ascites

The published experience in the percutaneous treatment of postoperative CA is limited to case reports and retrospective series. ^{22 24 46} Majdalany et al recently reviewed the published experience for percutaneous treatment of traumatic CAs. They found 18 studies besides their cohort that included 96 patients with CA or CA associated with chylothorax, chylopericardium, or lymphoceles. ^{23 47} Only 61 patients had traumatic CA and included specific data regarding the duration and etiology of the leak, output, identification of the leak, and follow-up. The leak was identified in 75% of the patients and clinical success was achieved in 67% who underwent therapeutic lymphangiography and 89% who underwent lymphangiography + embolization. ²³ Nadolski et al analyzed a cohort of 31 patients with CA (25 traumatic-iatrogenic and 6 nontraumatic). Two different embolization techniques were used: glue embolization of the lymph node proximal to the leak and endovascular coils + glue at the site of the leak. The site of the leak was identified in 17 patients (55%) and only 11 patients underwent embolization; 9 of them had resolution of the CA. Therapeutic lymphangiography was successful in 35% of the cases. Denver shunt placement was used as a bail-out treatment in seven patients. ²² Majdalany et al published a multi-institutional study with 21 patients for isolated, iatrogenic CAs. The authors used three different embolization techniques depending on the location of the leak (nodal glue embolization in the pelvis, cannulation, and catheter-based glue embolization in the retroperitoneum and retrograde TD cannulation with balloon-assisted sclerotherapy). A total of 29 procedures were performed and the lymphatic leakage was identified in 55% of the cases. Clinical success was achieved in 67% after one procedure with an overall success in 86% of the patients. Hur et al reported a success rate of 85% in patients with CA, lymphocele, and chylothorax. ⁴⁶ This retrospective study included 27 patients of whom 17 had ascites. They used three different glue embolization techniques: “lymphopseudoaneurysm” embolization, closest upstream lymph node embolization ( Fig. 1 ), or direct upstream lymphatic vessels or lymphatic channels supplying the leak.

Percutaneous CT-guided glue injection or sclerotherapy at the site of the leakage identified during the lymphangiography has shown to be successful in patients with CA. ^{48 49} Kortes et al analyzed 18 patients with refractory lymphatic leakage (pelvic, abdominal, and thoracic lymphatic leaks) treated with therapeutic lymphangiography. Ten patients underwent CT-guided sclerotherapy with ethanol injection at the site of the leakage. Overall clinical success rate was 72%. ⁴⁹

Pathways for Lymphangiography and Lymphatic Embolization in Patients with CA

Different authors have described several percutaneous approaches to treat refractory ascites with different embolic materials. ^{20 22 24 25 29 30 46 47 48 49 50 51 52 53 54 55}

INL has been accepted as the gold standard invasive imaging test to delineate the anatomy of the lymphatic system and identify the site of leakage, particularly lymphatic leaks arising from the pelvis, retroperitoneum, and central lymphatics (cisterna chyli and TD). Patients with CA after pelvic lymphadenectomy or retroperitoneal lymphadenectomy (RPLDN) are good candidates for INL alone or associated with glue embolization of the lymph node or lymphatic vessels feeding the leak. This approach can be helpful as well in patients with injury of the cisterna chyli or TD after upper abdominal surgery (gastric and pancreatic surgery) and may require TDE to seal the leak off.

Balloon-occluded retrograde abdominal lymphatic embolization can be used in patients with complex lymphatic leakage when the leak or the central lymphatics are not well identified or nonvisualized with INL. This approach can be combined with sclerotherapy or glue injection to stop the leakage. ^{25 47 53} Retrograde access can be achieved via transvenous retrograde thoracic ductography (success rate, 61.5%), ⁵⁶ under ultrasound or fluoroscopic guidance at the cervical segment of the TD ²⁶ or by snaring a wire previously placed in the TD via transabdominal approach.

Some patients with CA may develop a small, contained collection at the site of the leakage (“lymphopseudoaneurysm”). ⁴⁶ This cavity can be treated under fluoroscopy or CT guidance with glue embolization or sclerotherapy. Retrograde lymphatic embolization through the leakage pouch/cavity can be helpful, particularly in patients with multifocal leaks, which may require several punctures. ^{50 55} This can be achieved by direct catheterization of the lymphatic vessels from the cavity or by injecting the embolic agent into the cavity leading to retrograde embolization of the leaking lymphatic vessels.

Lymphangiography may not be able to demonstrate the source of the leak in patients with CA, particularly in cases with injury of the intestinal and hepatic trunks and patients with nontraumatic CA. As previously described, the intestinal lymphatic ducts drain the chyle into the cisterna chyli and the lumbar trunks, outside of the pathway of the contrast injected during the lymphangiography. ²² CA due to injury of the intestinal trunks may need retrograde cannulation of the TD or mesenteric INL to identify the lymphatic leak. ⁵²

Hepatic lymphorrhea is usually caused by injury to the lymphatic system from the hepatic lymph to the hepatoduodenal ligament. Surgical treatment is challenging due to the difficulty in identifying the leakage site in the hepatoduodenal ligament. A few case reports have been published regarding transhepatic lymphangiography and percutaneous treatment. If the site of leakage is identified during the lymphangiography, liquid embolic agents (glue and Onyx) can be used to seal the leak off. ^{29 30} Retrograde sclerotherapy through the drainage catheter at the site of the leak has been successfully reported as a treatment option in these unusual cases. ³⁰

Lymphoceles: Management and Interventions

Lymphoceles are fluid-filled cysts without an epithelial lining that occur after surgical intervention in lymphatic rich locations, such as the pelvis or the retroperitoneum. ⁵⁷ The absence of an epithelial lining makes the term “lymphocele” more accurate than “lymphocyst,” which is sometimes used to describe it. ⁵⁸ Initially described in 1950, lymphoceles have been described following several extraperitoneal procedures, such as surgery for urologic or gynecologic malignancies. ⁵⁸ This is related to lymph node dissection, which is considered an integral part of these procedures. ^{59 60 61} In addition, lymphoceles have developed following other extraperitoneal procedures with no intended involvement of lymphatic architecture, such as renal transplantation and vascular and spinal surgery, suggesting that lymphoceles can theoretically develop following any lymphatic injury. ^{58 62}

Lymphoceles have been reported to occur in up to 61% of patients who undergo pelvic lymph node dissection for prostate cancer and up to 26% of patients who have received renal transplants. ^{62 63} However, most lymphoceles are asymptomatic and only seen on imaging. Lymphoceles may become symptomatic if they grow enough in size to compress surrounding structures, such as ureters causing hydronephrosis or veins causing lower extremity edema or nerves causing pain. ⁵⁷ They may also become symptomatic if they become infected and present with fever and localized pain at the site of the lymphocele. ⁵⁸ Asymptomatic lymphoceles do not require intervention and regress on their own. ⁵⁸ Symptomatic lymphoceles require intervention, which can be divided into two components: drainage to relieve symptoms and additional intervention to prevent reaccumulation of fluid.

Historically, the gold standard of management for lymphoceles was surgical open drainage with or without marsupialization into the peritoneal cavity. ⁶⁴ Laparoscopic drainage methods were then developed which also involved marsupialization into the peritoneal cavity with shorter hospitalization and less recurrence rate than open surgical drainage. ⁶⁵ Percutaneous catheter drainage was later introduced and proved to be safe and effective in the management of symptomatic lymphoceles, but high recurrence rates and long catheter dwelling times meant that other methods were needed to prevent reaccumulation of fluid. ⁶⁶ This introduced the concept of sclerotherapy through the percutaneous drainage catheter, which relies on potential obliteration of the lymphatic leak or lymphocele cavity through the chemical effect of one of many different sclerosants. ⁶⁷ More recently, lymphangiography and lymphatic embolization have been used to address the lymphatic leak directly, which, when combined with percutaneous drainage, are thought to decrease the catheter dwelling time and decrease the rate of recurrence. ^{68 69}

Etiology

Lymphoceles occur due to injury of a lymph node or lymphatic vessel, with consequent accumulation of lymph in a localized, extraperitoneal space, as was proven by Ferguson et al ⁷⁰ who observed contrast filling of lymphoceles in patients who underwent lymphangiography. ⁵⁸ They develop in extraperitoneal locations as the peritoneum is able to absorb lymph and thus prevents formation of lymphoceles, which is why traditional treatments of lymphoceles entailed drainage and marsupialization into the peritoneum. ^{58 64 71}

Lymphoceles are often detected between 12 days and 6 months after surgery, but can be detected later, even years after surgery. ^{62 72 73 74 75} This may be because some patients are only imaged when they become symptomatic, and the lymphocele may have been present but asymptomatic until imaging was done. However, this may also highlight the fact that lymphoceles develop slowly, with less factors limiting their growth compared with hematomas, owing to the low concentrations of clotting factors and absence of smooth muscle cells in lymphatic vessels. ⁷⁶

Development of symptomatic lymphoceles has been linked to many factors, which include an older age, lower body mass index, and hypertension. ^{63 77} The theoretical correlation between low-molecular-weight heparin prophylaxis or antiplatelet therapy before or after surgery and the development of symptomatic lymphoceles has been disproven by several studies. ^{63 78 79} Incidence of symptomatic lymphoceles was, however, correlated to the number of lymph nodes removed from patients with prostate cancer, which was also seen in patients with rectal cancer and gynecologic cancer undergoing pelvic lymph node dissection. ^{77 79 80} Factors associated with the development of lymphoceles in patients who underwent renal transplantation include the use of mammalian target of rapamycin (mTOR) inhibitors, laparoscopic procurement of graft, and the presence of more than one renal artery. ⁸¹

Diagnosis

Most lymphoceles are asymptomatic and detected incidentally on imaging done for follow-up after surgery. The appearance of an asymptomatic lymphocele on ultrasound is often that of an anechoic cystic structure. ⁵⁸ A retrospective study comparing ultrasound findings between asymptomatic and symptomatic lymphoceles found that symptomatic lymphoceles were more likely to be larger, have septations and debris, and have anechoic content as opposed to ground-glass content. ⁸²

On CT, lymphoceles often appear as a low-attenuation cystic mass. Evidence of compression on surrounding structures can sometimes be seen, such as ipsilateral hydronephrosis when the lymphocele is compressing the ureter. ⁵⁷ Infected lymphoceles usually have a thick, irregular enhancing wall, which is interpreted in the appropriate clinical setting of fever and pain with history of surgery involving lymph node dissection. ⁵⁸ Lymphoceles on MR imaging show hyperintensity on T2-weighted images with a thin wall that shows no enhancement on T1-weighted images in the absence of infection. ^{7 58} MR lymphangiography has been used to identify the source of lymphatic leak with success using a three-dimensional spoiled gradient echo sequence, which was typically done using intraoperative lymphatic mapping with the use of dye. ⁸³

Historically, bipedal lymphangiography and more recently nodal lymphangiography have been used to show the source of lymphatic leak in lymphoceles. ^{58 68 69} Ethiodized oil is injected through a lymphatic vessel in the foot in conventional lymphangiography, or through one of the inguinal lymph nodes in nodal lymphangiography, and images are acquired using fluoroscopy showing flow of contrast into the lymphatic vessels and reaching the lymphocele cavity. ^{68 84}

Percutaneous Management of Lymphoceles

Surgical management with internal marsupialization, as with any surgical intervention, entailed significant patient morbidity and was not suitable for patients with infected lymphoceles. ^{58 85} Laparoscopic management was then developed, which also entailed marsupialization into the peritoneum, with reduced procedure time and patient morbidity. ⁸⁶

Interventional radiology has also been involved in the management of lymphoceles. Percutaneous aspiration under image guidance was reported, but given the high recurrence rate, this approach has strictly a diagnostic role. ^{67 87} Percutaneous catheter drainage was then introduced, which improved greatly on the incidence of recurrence seen with aspiration alone, but required long-term indwelling catheters, which can sometimes last for months. ^{66 67}

Sclerotherapy was later developed in an attempt to decrease catheter dwell time. Different sclerosant materials were used, such as ethanol, doxycycline, povidone iodine, and bleomycin and showed encouraging results. ⁵⁸ A retrospective analysis of sclerotherapy in the management of lymphoceles by Mahrer et al showed that ethanol, povidone iodine, or doxycycline sclerotherapy was successful in 77% of patients, and showed that the initial output was correlated with the success of sclerotherapy, with lower drainage volumes seen in the successful treatment group. ⁶⁷ Kim et al showed similar results in their experience with sclerotherapy for the management of lymphoceles, reporting 76.5 and 92.9% success of sclerotherapy in noninfected and infected lymphoceles, respectively, with no statistically significant difference between both groups. ⁸⁸

Other sclerosants have been used less frequently, such as bleomycin and polidocanol foam, with promising results. ^{89 90} An enlarging variety of sclerosants have been used, in many different intervals and volumes, with different end points, indicating that the ultimate method for sclerotherapy has not yet been discovered. Complications with sclerotherapy are rare, with the most commonly reported complications being infection and pain, which is likely related to the chemical inflammation induced by the sclerosant. The main downside to sclerotherapy is the relatively high rate of repeat sclerotherapy, with some studies reporting a mean number of treatments as high as 4, with a maximum as high as 14. ⁶⁷

A novel method for the management of lymphoceles makes use of the newer, less-cumbersome, nodal approach for lymphangiography to address the leaking lymphatic vessel directly. In addition to percutaneous drainage catheter placement, nodal lymphangiography is done to identify the leaking lymphatic vessel. Once the leaking lymphatic vessel is identified, N -butyl cyanoacrylate–ethiodized oil mixture is injected into the lymph node, or lymph nodes, supplying the leaking lymphatic vessels to embolize the source of lymphatic leakage ( Figs. 2 and 3 ). ^{68 69} This technique draws on the success of TDE for the management of iatrogenic chylothorax, and has shown promising results. ⁴⁴ Smolock et al reported an 80% clinical success rate with this technique, which is similar to sclerotherapy, yet with a median number of embolizations of 1 and a maximum of 2, and a median time to resolution of 7 days, which is much less than the results of sclerotherapy reported elsewhere. ^{67 68} Chu et al reported similar promising results, with a clinical success rate of 100% and a median number of embolizations of 1 and a maximum of 3, and a median time to resolution of 7 days. ⁶⁹ While both groups had a small number of patients, their results warrant a prospective study investigating the potential of this technique in rapid, minimally invasive management of lymphoceles.

Fig. 2.

A 35-year-old man with history of germ cell tumor status post orchiectomy and retroperitoneal lymphadenectomy. The patient developed postoperative abdominal pain. ( a ) CT scan demonstrated a large retroperitoneal lymphocele (arrows) which was drained under CT guidance in the prone position. ( b ) A drain was placed and the output was 1.1 L/day. ( c ) Intranodal lymphangiography revealed two areas of leakage (arrows) and the feeding lymphatic vessels and lymph nodes (arrowheads). ( d–g ) The closest lymph nodes (arrows) to both areas of leakage were accessed with a 22-gauge needle under fluoroscopy and oblique views were obtained to confirm adequate position of the needle tip. Diluted glue was injected (1:6) and visualized under fluoroscopy extending from the node to the level of the leak (arrowhead). ( h ) Post–lymphatic embolization CT scan was performed 1 month after the procedure with resolution of the retroperitoneal lymphocele. The drainage catheter was pulled out 8 days after the lymphatic embolization.

Fig. 3.

A 54-year-old man with history of prostate carcinoma status post prostatectomy and pelvic lymphadenectomy, complicated by right pelvic sidewall symptomatic lymphocele (arrows) ( a ). ( b ) The lymphocele (arrow) was drained with a 10F pigtail catheter (arrowhead) and 200 mL of fluid were aspirated. There was a daily output of 250 mL/day. ( c, d ) Intranodal lymphangiography via 25 gauge needle (arrowhead) demonstrated ethiodol extravasation into the lymphocele (arrow). ( e ) A second 25-gauge needle was use to access the lymphatic vessel supplying the lymphatic leak under fluoroscopy (arrow). ( f ) Dextrose 5% was injected through the needle (arrow) with wash out of the ethiodol in the lymphatic vessel (arrowheads) cranial to the tip of the needle. ( g ) Diluted glue (1:4) was injected with filling of the lymphatic vessel feeding the leak (arrow). ( h ) CT scan of the abdomen and pelvis performed 2 months after the lymphatic embolization with resolution of the lymphocele. The drainage catheter was removed 3 days after the embolization.