Chylous Ascites: Overview, Pathophysiology, Etiology (original) (raw)

Overview

Chylous ascites is the extravasation of milky chyle rich in triglycerides into the peritoneal cavity, which can occur de novo as a result of trauma or obstruction of the lymphatic system. [1, 2] Moreover, an existing clear ascitic fluid can turn chylous as a secondary event.

True chylous ascites is defined as the presence of ascitic fluid with high fat (triglyceride) content, usually higher than 110 mg/dL.

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Pathophysiology

Within the enterocytes of the small intestine, dietary long-chain fatty acids are re-esterified into triglycerides. Long-chain triglycerides are subsequently coated with lipoprotein, cholesterol, and phospholipid to form chylomicrons. Chylomicrons subsequently enter the lymphatic system of the small intestines and gradually pass along larger omental lymphatics to the cisterna chyli located anterior to the second lumbar vertebra. The cisterna is joined by the descending thoracic, right and left lumbar, and liver lymphatic trunks, and, collectively, these form the thoracic duct, which passes through the aortic hiatus and courses through the right posterior mediastinum and eventually enters the venous system. The thoracic duct carries lymphatic drainage from the entire body, except for the right side of the head and neck, right arm, and right side of thorax. Chylous effusions may develop when these channels are injured or obstructed. [3]

Based on animal experiments, Blalock concluded that obstruction of the thoracic duct alone was not sufficient to cause chylous ascites. [4] Patients with a limited reserve of lymphaticovenous anastomotic channels were suspected to have greater risk of developing persistent ascites when obstruction or injury of the lymphatic channels occurred.

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Etiology

Chylous ascites is an uncommon clinical condition that occurs as a result of disruption of the abdominal lymphatics. Multiple causes have been described, with the most common causes being malignancy (hepatoma, small bowel lymphoma, small bowel angiosarcoma, and retroperitoneal lymphoma), cirrhosis (≤0.5% of patients with ascites from cirrhosis may have chylous ascites), and trauma after abdominal surgery. [2] Other causes include the following:

In adults, chylous ascites is associated most frequently with malignant conditions. These conditions particularly include lymphomas and disseminated carcinomas from primary neoplasms in the pancreas, breast, colon, prostate, ovary, testes, and kidney. Infectious diseases, such as tuberculosis [5] and filariasis, [6] can cause chylous ascites. Chylous ascites has also been reported in adults in association with hepatoma, small bowel angiosarcoma, retroperitoneal lymphoma, jejunal carcinoid, [7, 8] and sclerosing mesenteritis. [9]

In children, the most common causes of chylous ascites are congenital abnormalities, such as lymphangiectasia, mesenteric cyst, and idiopathic "leaky lymphatics." Other congenital causes include primary lymphatic hypoplasia associated with Turner syndrome and yellow nail syndrome, and the lymphatic malformations associated with Klippel-Trenaunay syndrome. [6] Neoplasia is an uncommon cause of pediatric chylous ascites.

The incidence of spontaneous chylous ascites in patients with chronic liver diseases is estimated to be 0.5%. Fluid in the space of Disse may enter the lymphatic channels in the portal and central venous areas of the liver. An increase in portal pressure can lead to increased flow of fluid into both the space of Disse and the liver's lymphatic system. Indeed, patients with cirrhosis have increased thoracic duct lymph flow. [10] Lymphatics may spontaneously rupture in patients with cirrhosis as a result of higher than typical flow, with the formation of chylous ascites. Chylous ascites has been reported in patients with polycythemia vera and resulting hepatic vein thrombosis.

Abdominal surgery is a common cause of chylous ascites. The most frequently associated surgical procedures are resection of abdominal aortic aneurysm and retroperitoneal lymph node dissection. In a series of 329 patients with testicular cancer who underwent postchemotherapy retroperitoneal lymph node dissection, 7% of patients developed chylous ascites. [11] Chylous ascites has also been described after several abdominal procedures, such as peritoneal dialysis catheter insertion [12] , pancreatic resection, [13] splenorenal shunt surgery, [14] cadaveric [15] and living donor liver transplantation, [16, 17] open thoracoabdominal aortic aneurysm repair, [18] laparoscopic donor nephrectomy, [19, 20, 21] and laparoscopic Nissen fundoplication. A review by Aalami et al provides an excellent overview of the causes of chylous ascites, as well as a history of chylous ascites management. [6]

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Classification

Milky ascites is subdivided into three groups as follows:

This classification is not clinically useful and has been discarded by some.

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Epidemiology

Frequency

Chylous ascites accounts for less than 1% of cases. [2] The rarity of chylous ascites in clinical practice can be judged by the fact that only 28 cases were identified at Massachusetts General Hospital over a period of 20 years. Of these 28 patients, 4 were children. The mean age at detection in adults was 54.3 years. [22]

A report from the 1950s estimated the incidence of chylous ascites to be 1 case per 187,000 hospital admissions. [23] By the 1980s, the incidence of chylous ascites had increased to 1 case per 11,584 hospital admissions, perhaps due to more aggressive retroperitoneal and cardiothoracic surgical techniques and longer survival of cancer patients. [24]

Sex- and age-related demographics

No differences in sex distribution have been cited, but, of the 28 patients with chylous ascites from Massachusetts General Hospital, 75% were women. [22] Chylous ascites can occur in adult and pediatric populations. In adults, it commonly is observed in individuals aged 50-65 years.

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Clinical Features and Complications

Clinical features

Abdominal distention is the most common symptom in patients with chylous ascites. Other clinical features include abdominal pain, anorexia, weight loss/gain, edema, weakness, nausea, dyspnea, lymphadenopathy, early satiety, fever, and night sweats. Fever, night sweats, and lymphadenopathy are usually observed in patients with lymphoma. Often, features of the primary illness, such as cirrhosis or of an associated malignancy, dominate the clinical picture. Rarely, it can present as acute peritonitis, [25, 26] or as a consequence of acute gallstone pancreatitis. [27]

Complications

Sepsis is the most common complication, and sudden death has been reported in patients with chylous ascites. The prognosis in adult patients with chylous ascites is poor due to its association with malignancy and severe liver disease. However, pediatric patients and adult patients with postsurgical and posttraumatic chylous ascites have a favorable prognosis.

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Diagnostic Tests

Laboratory Studies

Routine laboratory tests may show hypoalbuminemia, lymphocytopenia, anemia, hyperuricemia, elevated levels of alkaline phosphatase and liver enzymes, and hyponatremia. Serum cholesterol and triglyceride levels are usually normal.

Abnormal liver enzyme levels are more common in patients with disseminated carcinoma than in patients with lymphoma or nonmalignant disorders. Anemia is common in patients with neoplasia.

The diagnosis of chylous ascites is made by peritoneocentesis and by analysis of the ascitic fluid. An ascitic triglyceride concentration above 200 mg/dL is consistent with chylous ascites. [2]

Ascitic fluid study

Ascitic fluid is usually white or milky. Gross milkiness of the ascitic fluid corresponds poorly with absolute triglyceride levels, because turbidity also reflects the size of the chylomicrons.

The ascites triglyceride level is elevated in all patients. Typically, chylous ascites is diagnosed when the ascites triglyceride level is greater than 110 mg/dL. Levels as high as 8100 mg/dL have been described. [24] Other authors have identified an elevated ascites-to-plasma triglyceride ratio (between 2:1 and 8:1) as being indicative of chylous ascites. [6]

Other ascites tests include the following [22] :

Other diagnostic tests

Other studies may be indicated, such as the following:

CT scanning, lymph node biopsy, and laparotomy carry the highest yield of diagnostic information. The role of magnetic resonance imaging (MRI) is not well defined. Note that lymphangiography can transiently worsen chylous ascites due to the oily contrast medium used for the test.

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Treatment

Because chylous ascites is a manifestation rather than a disease by itself, the prognosis depends on the cause and the treatment of the underlying disease. [2]

Supportive measures can relieve the symptoms. These measures include repeated paracentesis, diuretic therapy, salt and water restriction, elevation of the legs and the use of supportive stockings, and dietary measures.

Lymphatic flow increases after the ingestion of a fatty meal. The fatty acids derived from short-chain and medium-chain triglycerides diffuse directly across enterocytes into the portal venous system. Their absorption does not affect lymphatic flow. However, the fatty acids derived from long-chain triglycerides are re-esterified into triglycerides in the enterocyte. They are then incorporated into chylomicrons which subsequently enter the lymphatic system.

A low-fat diet with medium-chain triglyceride supplementation can reduce the flow of chyle into the lymphatics. [28] Typically, medium-chain triglyceride oil is administered orally at a dose of 15 mL three times per day with meals. However, this approach is frequently not successful. One case report described the successful use of orlistat (Xenical) in a patient who had difficulty complying with a low-fat diet. [29]

If chylous ascites persists despite dietary management, the next step may involve bowel rest and the institution of total parenteral nutrition. [16] Bowel rest and total parenteral nutrition are postulated to be beneficial in patients with posttraumatic or postsurgical chylous ascites.

Paracentesis can result in immediate symptom relief; however, reaccumulation of the fluid usually follows, and patients may require repeated paracentesis. Some authorities have advocated large-volume paracentesis. Morbidity from a single tap is usually low, but complications (eg, peritonitis, hemorrhage) can occur. Transfusion of albumin and/or red blood cells (RBCs) during paracentesis may help prevent hypovolemia in patients with hypoalbuminemia or anemia.

Multiple case reports describe the use of octreotide, a somatostatin analogue, in the management of chylous ascites, typically at a dose of 100 mcg administered subcutaneously three times per day. [16, 17, 30, 31, 32] A combination of total parenteral nutrition and subcutaneous octreotide has been used successfully to treat congenital chylous ascites in a newborn. [33] Experimental work in humans has shown that somatostatin can significantly decrease postprandial increases in triglyceride levels. This effect cannot be explained by either the inhibition of gastric emptying or inhibition of exocrine pancreatic secretion. [34, 35] Octreotide is most likely effective in chylous ascites owing to its ability to inhibit lymphatic flow. Indeed, in a canine model, infusion of somatostatin resulted in a decrease in lymph flow, measured via a cannula inserted into the thoracic duct. [36]

A 2017 case report noted that the addition of octreotide to sirolimus therapy reduced chylous effusion in a woman with lymphangioleimyomatosis who developed refractory chylothorax and chylous ascites during sirolimus therapy. [37]

Postsurgical chylous ascites usually resolves with supportive therapy. Early reoperation is indicated when the site of leakage is apparent and if the patient is a good operative candidate. [38] Case reports have described the laparoscopic treatment of chylous leaks, using suture ligation and fibrin glue to control the leak. [39] In a separate report, fibrin glue applied to absorbable mesh was useful in patients with large areas of diffuse lymphatic leakage. [40] Another report described the treatment of chylous ascites after laparoscopic Nissen fundoplication with percutaneous injection of tissue glue (ie, N -butyl-cyanoacrylate mixed with ethiodol) into the thoracic duct. [41]

Lymphangiography itself may play more than a diagnostic role in the management of lymphatic leaks. [1] Lymphangiography with lipiodol led to the resolution of lymphatic leakage in a small number of patients with postoperative chylous ascites. [42, 43] Lipiodol has been used as an embolic agent in a variety of angiographic procedures. Furthermore, it has been postulated that leakage of lipiodol from the site of lymphatic vessel perforation may stimulate a local inflammatory reaction in the surrounding soft tissues. This, in turn, may lead to the closure of the leaks. [42]

The combination of lymphangiography and lymphatic embolization appears to be effective in the treatment of refractory chylous ascites. In a retrospective study of 31 patients with refractory chylous ascites, the investigators visualized the lymphatic leak in 17 (55%) of the 31 patients who underwent conventional lymphangiography and in 7 (78%) of 9 patients who underwent magnetic resonance lymphangiography. Eleven of the 17 patients whose leak was identified underwent embolization with N-butyl cyanoacrylate glue and/or coils, with 9 patients (82%) achieving resolution of the chylous ascites. There was a 52% overall rate of ascites resolution, with greater success when the leak site was identified. [44]

Similar results were noted in a retrospective study (2016-2017) of three patients with previously unidentifiable leakage site or failed lymphatic embolization who underwent endolymphatic balloon-occluded retrograde abdominal lymphangiography (BORAL) and embolization (BORALE) for the diagnosis and treatment of chylous ascites. [45] Technical success with pelvic lymphangiography and BORAL was achieved in all three patients, and BORAL was technically successful in the two patients it was attempted in. Resolution of the chylous ascites occurred in all the patients, with no minor/major complications reported. [45] More investigation is needed.

Peritoneovenous shunting has been used successfully in small numbers of patients with chylous ascites. [46] However, shunt failure is common and the procedure may be fraught with complications.

Use of transjugular intrahepatic portosystemic shunts (TIPS) to successfully treat chylous ascites related to cirrhosis has been reported. [47, 48]

Malignant chylous ascites requires specific therapy directed at the primary cause as well as supportive therapy. These therapies may include chemotherapy, radiation, and surgery. Laparotomy and ligation of the leaking lymphatics, resection of a leaking small bowel segment, and removal of an obstructing tumor all have been attempted with varying degrees of success. Transient success also has been achieved with peritoneovenous shunts.

Laparotomy should not be used in pediatric patients with chylous ascites unless the condition is unresponsive to conservative therapy and a lesion that can be corrected by surgery is apparent.

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Author

David C Wolf, MD, FACP, FACG, AGAF, FAASLD Medical Director of Liver Transplantation, Westchester Medical Center; Professor of Clinical Medicine, Division of Gastroenterology and Hepatobiliary Diseases, Department of Medicine, New York Medical College

David C Wolf, MD, FACP, FACG, AGAF, FAASLD is a member of the following medical societies: American Association for the Study of Liver Diseases, American College of Gastroenterology, American College of Physicians, American Gastroenterological Association

Disclosure: Serve(d) as a speaker or a member of a speakers bureau for: Salix; Gilead; Abbvie; Intercept; Merck.

Coauthor(s)

Unnithan V Raghuraman, MD, FACG, FACP, FRCP Consulting Staff, Department of Gastroenterology, St John Medical Center

Unnithan V Raghuraman, MD, FACG, FACP, FRCP is a member of the following medical societies: American Association for the Study of Liver Diseases, American College of Gastroenterology, American College of Physicians, American Gastroenterological Association, American Society for Gastrointestinal Endoscopy

Disclosure: Nothing to disclose.

Specialty Editor Board

Francisco Talavera, PharmD, PhD Adjunct Assistant Professor, University of Nebraska Medical Center College of Pharmacy; Editor-in-Chief, Medscape Drug Reference

Disclosure: Received salary from Medscape for employment. for: Medscape.

Chief Editor

Acknowledgements

Mounzer Al Samman, MD Assistant Professor, Department of Internal Medicine, Division of Gastroenterology, Texas Tech University School of Medicine

Mounzer Al Al Samman, MD is a member of the following medical societies: American College of Gastroenterology, American College of Physicians, and American Gastroenterological Association

Disclosure: Nothing to disclose.