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J Thorac Cardiovasc Surg 2008;136:650-656
© 2008 The American Association for Thoracic Surgery

Surgery for Acquired Cardiovascular Disease

Chylopericardium in adults: A literature review over the past decade (1996–2006)

Chadi Dib, MD, A. Jamil Tajik, MD, Soon Park, MD, Mohammed E.L. Kheir, MD, Bijoy Khandieria, MD, Farouk Mookadam, MD, MSc*

Mayo Clinic College of Medicine, Division of Cardiovascular Diseases and Cardiovascular Surgery, Scottsdale, Ariz

Received for publication August 28, 2007; revisions received February 18, 2008; accepted for publication March 30, 2008.

* Address for references: Farouk Mookadam, MD, FRCPC, FACC, MSc, 13400 E Shea Blvd, Scottsdale, AZ 85259. (Email: mookadam.farouk{at}mayo.edu).


   Abstract
Top
 Abstract
Introduction
 Methods
 Statistical Analysis
 Results
 Treatment
 Discussion
 Conclusion
 References
 
Objectives: We present a systematic overview of the literature on reported cases of chylous pericardial effusion in adults over the past 10 years, assessing clinical presentation, etiology, diagnosis, and treatment.

Methods: We conducted an evidence-based literature review searching for all reported adult cases of chylopericardium in the past 10 years (January 1996–December 2006).

Results: A total of 33 reported cases of chylopericardium were identified through a systematic literature search. There was no gender bias in the incidence of chylous pericardial effusion. Age at diagnosis varied from 18 to 68 years with a mean ± standard deviation of 36.78 ± 14.71 years. Time from symptom onset to diagnosis was variable (ranging from acute presentation to several years).The most common reported etiology was idiopathic. The diagnosis was made by pericardiocentesis in all patients. A search for secondary causes included computed tomography of the chest, lymphoscintigraphy, and lymphangiography along with radioactive oral 131I-triolein. Conservative therapy was prescribed in 28 patients and failed in 16, in whom subsequent surgery was necessary. Overall, 21 patients underwent various types of surgery. Thoracic duct ligation with creation of a pericardial window was the most common surgical procedure.

Conclusion: Chylopericardium is a rare entity. The fluid appearance, triglyceride content, cytologic characteristics, and negative cultures are crucial to make the correct diagnosis. Treatment is dependent on the etiology. Surgical management is the most successful. Conservative therapy is reserved for patients with idiopathic chylopericardium, those with an untreatable etiology, those considered at high risk for surgical treatment, or those with a predictably short lifespan.

Abbreviations and Acronyms VATS = video-assisted thoracoscopic surgery


   Introduction
Top
 Abstract
 Introduction
Methods
 Statistical Analysis
 Results
 Treatment
 Discussion
 Conclusion
 References
 
Chylopericardium is a rare entity in which chylous fluid containing triglycerides in high concentrations accumulates in the pericardial cavity. It was first described by Hasebrock in 18881Go and subsequently reviewed in 1935,2Go with 3 cases of chylopericardium being identified among 100 cases of nontraumatic chylothorax.1Go The etiology of chylopericardium includes congenital mediastinal lymphangiectasia,3Go iatrogenic after cardiac surgery,4-6Go gastric signet ring cell carcinoma,7Go Gorham syndrome (osteolysis that results from lymphangiomatosis with adjacent bone resorption),8Go malignant tumors (eg, mediastinal tumors including mediastinal dysgerminomas9Go), blunt or penetrating trauma, infection, radiation, congenital lymphatic anomalies,6Go or primary idiopathic.10-15Go There is no evidence-based systematic overview on the topic in the past decade. Diagnosis can be challenging and optimal treatment of chylopericardium remains controversial.


   Methods
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 Abstract
 Introduction
 Methods
Statistical Analysis
 Results
 Treatment
 Discussion
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 References
 
A computerized Ovid and MEDLINE database search (from January 1, 1996, until December 31, 2006) was undertaken to identify English and French articles describing chylopericardium. Search terms included the following: "chylopericardium," "chylous pericardial effusion," and the combined term "chylopericardium and pericardial effusion" without limits. We identified 70 articles on the basis of a priori inclusion criteria16Go: 29 were deemed relevant for inclusion in this study (ie, adult patients > 18 years of age with a confirmed diagnosis of chylous pericardial effusion). A second search using the EMBASE database (from January 1996 until December 1, 2006) was undertaken using similar search terms and revealed two additional articles.17,18Go In addition, a qualified librarian independently completed a MEDLINE, Ovid, and EMBASE search and identified no new articles. The reference section of all articles was scanned for further articles and no new cases were identified beyond the electronic search. All relevant articles were independently reviewed and analyzed by two of the authors (F.M. and C.D.). Thirty-three cases were identified from 31 articles. Patient demographics, clinical presentation, diagnosis, and treatment were identified for each of the cases ( Table 1).


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  		Table 1 General characteristics of studies meeting inclusion criteria
 

   Statistical Analysis
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Results
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 Discussion
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Means and standard deviations were used for categorical variables (Table 1). A formal Kappa test of heterogeneity was not performed inasmuch as the articles were from different continents, spanned a decade, and were sufficiently different to preclude the necessity of formal Kappa testing.


   Results
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 Methods
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 Results
Treatment
 Discussion
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 References
 
There was no gender bias in disease occurrence: 16 (48%) female and 17 (52%) male (Table 1). Age at diagnosis ranged from 18 to 68 years with a mean ± standard deviation of 36.78 ± 14.71 years. Time from onset of symptoms to diagnosis showed wide variation ranging from several years (13 years19Go in a patient who was incidentally discovered to have an enlarged heart and remained asymptomatic and 12 years15Go in a patient whose condition also was discovered incidentally and who refused pericardiocentesis) to acute presentations with tamponade.20,21Go The commonest causes of chylopericardium over the past decade were as follows: idiopathic (56%),3,10-15,19,20,22-31Go postoperative (9%) (viz, mitral valve replacement [6%],1,4Go coronary artery surgery [3%],5Go and orthotopic heart transplantation [3%]6Go), malignant disease of the lymphatic system or other mediastinal neoplasms (6%) including mediastinal lymphangioma (3%)32Go and mediastinal dysgerminoma (3%),9Go signet ring cell carcinoma (3%),7Go Gorham syndrome (3%),8Go blunt trauma (3%),28Go mediastinal lymphangiectasis (3%),3Go vein thrombosis (3%),17Go endovascular treatment of superior vena cava syndrome (3%),33Go and tuberculosis (3%).34Go Abnormalities of the lymphatic system22Go and mediastinal lymphangiectasis3Go causing chylopericardial effusions were referred to as idiopathic causes. The commonest presentation for patients with chylopericardium was dyspnea (64%), * including patients with tamponade (33%)1,5,6,17,18,21-23,32,37Go and patients with chest pain or discomfort (12%).9,9,18,20Go Two (6%) patients presented with syncope,14,23Go and chylopericardium was diagnosed later.

Diagnosis is usually established after pericardiocentesis with meticulous fluid analysis, emphasizing fluid color and triglyceride content (Go Table 2). Four patients had low pericardial fluid triglyceride levels4,7,20Go (181 mg/dL, 216 mg/dL, 245 mg/dL, and 197 mg/dL) and still had a diagnosis of chylous pericardial effusion. All other patients had a triglyceride level in the pericardial fluid of more than 500 mg/dL with the highest being 2546 mg/dL.22Go Characteristics of the pericardial fluid analysis are summarized in Table 2. There are no unique features on echocardiogram, chest x-ray film, or electrocardiogram that could predict the diagnosis of chylous pericardial effusion.


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  		Table 2 Characteristics of chylous fluid analysis
 

   Treatment
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 Methods
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 Results
 Treatment
Discussion
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Conservative management was prescribed in 28 (84.84%) patients and consisted of pericardiocentesis alone (27%),12,19,20,25,28,29,33Go pericardiocentesis followed by medium chain triglycerides diet (6%)23,34Go and total parenteral nutrition (12%),1,6,22,24Go pericardiocentesis followed by total parenteral nutrition and external beam radiation (3%),8Go pericardiocentesis only followed by total parenteral nutrition (6%),5,17Go pericardiocentesis followed by vena caval revascularization (3%),33Go and diagnostic nontherapeutic pericardiocentesis followed by total parenteral nutrition (9%),4,9,21Go low fat diet (6%),7,18Go or medium chain triglyceride diet (9%).3,14,26Go In one patient conservative therapy was not described (3%).10Go

Surgery was performed in 21 patients (57.57%), consisting of open thoracotomy in 7 patients (33.33%)9,11,12,15,17,18,21,31Go or video-assisted thoracoscopic surgery (VATS) in 10 patients (47.6%)6,10,13,22,25,28-30,32Go with subsequent thoracic duct ligation and creation of a pericardial window. One case (4.7%)19Go consisted of thoracotomy and laparotomy with lymphovenous anastomosis between the thoracic duct and left renal vein. Another case (4.7%) consisted of pleuropericardial window and tumor resection.9Go There have been 2 case reports of chylopericardium in which the type of surgery (VATS vs open thoracotomy) was not defined (10.5%).14,23Go

Conservative treatment failed in 16 of 28 cases (57.1%). {dagger} Time period from diagnosis to surgical treatment varied from 2 days21Go to 4 years28Go with a mean of 150 days.

Follow-up was reported in 29 of the cases and ranged from 1 month29Go to 108 months3Go with a mean of 16 months. Four papers did not report follow-up.1,17,20,33Go A small residual pericardial effusion was noted in 2 cases at 3 months and 1 month after surgery.26,29Go Mortality from chylopericardium was low (only 2 cases, 6%). One patient died of bleeding 11 days after surgery.7Go Reports complicated by death were attributed to signet ring cell carcinoma7Go and mediastinal dysgerminoma.9Go Among the 18 cases of idiopathic chylous effusion, conservative therapy failed in 11 (61%) and surgery was necessary {ddagger}; there were no deaths. Two (11%) patients were treated surgically13,15Go and 5 (27.7%) responded to conservative therapy alone.


   Discussion
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 Abstract
 Introduction
 Methods
 Statistical Analysis
 Results
 Treatment
 Discussion
Conclusion
 References
 
The accumulation of chyle in the pericardial cavity is rare. Causes are multiple and include trauma, mediastinal neoplasm, thrombosis of the subclavian vein, tuberculosis, thoracic surgery,24Go Behçet syndrome,35Go or Gorham syndrome. Primary idiopathic chylopericardium is known to be a less common cause of chylopericardium24Go but has been reported with increasing frequency in the past 10 years. Given that idiopathic chylous pericardial effusion is rare, it lends itself to the bias of reporting and publication.

Idiopathic chylopericardium is a diagnosis of exclusion and is invoked when no discernible cause is evident. This entity has two possible explanations: (1) the presence of damaged lymphatic vessels with abnormal communication of the thoracic duct to the pericardial lymphatics resulting in chylous reflux or (2) elevated pressure in the thoracic duct, which may occur in lymphangiectasia.24Go

Symptoms at presentation are not indicative of the cause of the pericardial effusion. Some patients remain asymptomatic3,4,11-13;15,24-26Go and are noted to have cardiomegaly on routine chest radiograph. Most of the patients who have severe shortness of breath and tamponade1,5,17,21,23,32Go receive therapeutic and diagnostic pericardiocentesis.

Many diagnostic modalities have been described, including (1) observation of Sudan III dye distribution into the pericardial cavity after oral intake of Sudan III dye,20Go (2) lymphangioscintigraphy,14,23Go (3) lymphangiography,19Go and (4) evaluation of chest radioactivity after an oral dose of 131I-triolein.20Go All of these methods are used to ascertain the cause of the chylous pericardial effusion. Because of the paucity of cases, the sensitivity and specificity of each diagnostic modality is unknown and likely reflects the expertise of the local center. Lymphoscintigraphy appears to be the most commonly used modality. Pericardiocentesis followed by cytology, chemistry, and culture is necessary to definitively make the diagnosis. Analysis of the fluid usually shows a whitish or milky aspirate with a high triglyceride and protein content, a predominance of lymphocytes, and the presence of fat globules by Sudan III staining. Blood cultures are universally negative. There have been a few cases4,7,20Go in which the triglyceride level was low and the diagnosis of a chylous pericardial effusion was made. This occurs because there is no universally accepted triglyceride level that is required to confirm the diagnosis. There is no doubt in the diagnosis if the pericardial fluid analyses meets the criteria shown in Table 2: a milky yellowish appearance, a triglyceride level greater than 500 mg/dL, a cholesterol/triglyceride ratio less than 1, and negative cultures with lymphocyte predominance on cytologic examination (one point). A score of 2 (specificity and sensitivity of 100%) is required for a diagnosis of chylopericardium.

Optimal treatment of patients with chylopericardium is unclear. Conservative therapy in the absence of hemodynamic compromise is one option.25Go Rarely, a single pericardiocentesis will prevent recurrence.20Go Pericardiocentesis followed by pericardiostomy,24Go a medium chain triglyceride diet,1,3,26,33Go or total parenteral nutrition4,5,8Go can be tried, especially if the patient is reluctant to undergo surgery or has concomitant life-limiting disease . Conservative treatment failed in 57.1% of the cases reported,25Go and surgical treatment was curative in all. One late death resulting from bleeding was described. There are no clinical indicators to predict the failure of conservative therapy. Given the low mortality rate in idiopathic chylopericardium, initial treatment should include pericardiocentesis with a pericardiostomy tube, along with medium chain triglyceride diet. Failure of this therapy should prompt surgical intervention. The average time from the initiation of conservative therapy to the scheduling of surgical intervention has been 150 days on average, but the median was 12 days (ranging from 1 day to 1460 days) as reported in the literature in the past 10 years. This skewing is the result of a single case28Go in which the time from conservative to surgical treatment period was 4 years (1460 days). We concur with Wurnig and associates28Go and suggest surgical intervention in all patients with hemodynamically significant effusions. In addition, recurrence after pericardiocentesis and failed conservative treatment should be indications for surgical management. Given that a continuing leakage of chyle can lead to serious metabolic, nutritional, and immunologic abnormalities, an average daily loss of chyle of 500 mL daily over a 5-day period should be an indication for surgical intervention. Almost all patients who had a recurrent chylous pericardial effusion in a 3-month period required surgical treatment. Therefore, recurrence should prompt evaluation for surgical intervention. Treatment of patients with secondary chylopericardium should be directed against the underlying cause. Surgery is indicated early in the course of tumor-induced chylous pericardial effusion and also after a traumatic event when the daily loss of chyle exceeds 1500 mL per day in an adult patient.37Go Consideration to the use of radiotherapy and chemotherapy can be discussed if malignant disease is present in the absence of hemodynamic instability.

Surgical intervention may include thoracic duct ligation, which usually leads to collateral circulation regardless of the level of ligation. After ligation, pressures as high as 50 mm Hg have been recorded in the pericardium. This was subsequently followed by a fall in the blood lipid level (from > 500 mg/dL to 280 mg/dL), gradually returning to normal within 16 days.38Go To ensure the success of the surgical procedure, the thoracic duct should be ligated in the lower part of the thorax and a pericardial window should be created to allow adequate drainage and prevent complications such as constrictive pericarditis.28Go Creation of a pericardial window without thoracic duct ligation is associated with recurrence in 50% of the cases, whereas it is rare after ligation39,40Go and mostly occurs if duplication of the thoracic duct is present.41Go

The specific type of surgical procedure, VATS versus open thoracotomy, depends on the local expertise. Left or right thoracotomy may be used. Akamatsu and associates39Go prefer left thoracotomy inasmuch as the thoracic duct has its main course in the left hemithorax, surgical time is shorter, and the likelihood of injury to the esophagus and descending aorta are lower. The right-sided approach allows easier access to the duct. The duct should be ligated near the diaphragm owing to the variation in its anatomy above that level,28Go and mass ligation is recommended because of wide anatomic variations in that specific area above the diaphragm.29Go Cases involving identification and clipping of the thoracic duct have been described,28,42,43Go and VATS has been used,28Go with magnification allowing easier identification of mediastinal structures. The VATS procedure is being used increasingly and is associated with less postoperative pain and pulmonary dysfunction.44Go


   Conclusion
Top
 Abstract
 Introduction
 Methods
 Statistical Analysis
 Results
 Treatment
 Discussion
 Conclusion
References
 
Chylopericardium is a rare entity. Presentation may be acute, chronic, or even subclinical. Diagnosis always requires pericardiocentesis when the color of the fluid characteristics, triglyceride content, cytologic examination, and negative culture suggests the diagnosis. Patients should undergo chest computed tomography followed by lymphangioscintigraphy/lymphangiography to rule out secondary causes. Treatment of the underlying cause should always be the therapy of choice. Cases of idiopathic chylopericardium have been reported in which conservative therapy with follow-up may be successful. Conservative therapy should be performed in cases of idiopathic chylopericardium or if there is an untreatable underlying medical condition that shortens lifespan or surgical risks are considered too high. Open thoracotomy or VATS, when available, should be considered when conservative measures fail or there are no contraindications to surgery. Surgery should include thoracic duct mass ligation above the diaphragm with a pericardial window for subsequent drainage and prevention of complications such as constrictive pericardial disease.


   Footnotes
 
* References 1, 5-10, 14, 17-22, 26, 29-33, 35, 36Go. Back

{dagger} References 6, 9, 10, 12, 14, 17-19, 21-23, 25, 27-31Go. Back

{ddagger} References 10, 12, 14, 18, 19, 22, 23, 25, 29-31Go. Back


   References
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 Abstract
 Introduction
 Methods
 Statistical Analysis
 Results
 Treatment
 Discussion
 Conclusion
 References
 

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