Intranodal Lymphangiography and Lymphatic Embolization for Management of Iatrogenic Chylous Ascites in Children

Abstract

Background:

To demonstrate the value of intranodal lymphangiography (INL) and lymphatic embolization (LE) in management of iatrogenic chylous ascites in children who fail conservative management.

Methods and Results:

Retrospective review of medical records revealed six patients (four males and two females; age range 11–39 months) who underwent eight INLs and three LEs between 2017 and 2019. In one patient, the leak was visualized and embolized. In three patients, the leak was not visualized and no embolization was done, but drain output decreased and INL was not repeated. In two patients, the leak was not visualized and no embolization was done, but drain output did not decrease and INL was repeated. Repeat INL identified a leak in one patient and targeted LE was done. Repeat INL did not identify a leak in the other patient, but empirical LE was performed at the sites suspicious for leakage after multidisciplinary discussion. INL was able to identify the site of lymphatic leak in two patients (33%). In the three patients who underwent LE (two targeted at the site of identified leak and one empirical at sites suspicious for leak), one (33%) was clinically successful and the other two required surgery to address the lymphatic leak. In three patients, chylous ascites resolved after INL alone with no additional interventions. Three patients developed complications after the procedure, but only one appears to be related to the procedure itself. Follow-up for 13.8 months (13–26 months) revealed no long-term complications or mortality.

Conclusion:

INL with or without LE is a safe treatment for iatrogenic pediatric chylous ascites. Early utilization before more invasive surgical intervention should be considered in light of the response to INL.

Introduction

Chylous ascites, defined as accumulation of intestinal lymph (chyle) rich in triglycerides within the peritoneal cavity, is a rare entity that is even less frequent in the pediatric population.¹ Primary chylous ascites is most often caused by congenital lymphatic dysplasias, whereas secondary chylous ascites is caused by inflammation, trauma, neoplasia, or abdominal surgery.² The incidence of chylous ascites after abdominal surgery is reported to be as high as 11% in the adult population, and is strongly associated with the number of retroperitoneal lymph nodes dissected during the surgery.^3–6

In the pediatric population, chylous ascites is a reported complication after surgical resection of abdominal tumors, specifically nephroblastomas and neuroblastomas.^6–8 It is likely caused by injury or interruption of the retroperitoneal lymphatic vessels during dissection, resulting in the formation of a lymphoperitoneal fistula with accumulation of chyle in the peritoneum.⁹ Postoperative chylous ascites is associated with significant morbidity due to the continuous loss of chyle, which is rich in nutrients and immunoglobulins, leading to malnutrition, electrolyte imbalance, and immune deficiency, which compounds the already fragile state of the postoperative patient.^9,10

The mainstay of treatment for postoperative chylous ascites is conservative management. This includes repeated paracentesis to decrease the abdominal distention, low-fat diet, or total parenteral nutrition to decrease the formation of chyle and correct the malnutrition and electrolyte imbalance, as well as intravenous octreotide (synthetic somatostatin analog), which is believed to decrease the lymph production and its flow rate.^5,10,11 Approximately 66%–77% of adult patients respond to conservative management, with this number reaching as high as 80% in the scarce reports in the pediatric population.^7–9 Patients who do not respond to conservative management undergo surgical management through peritoneovenous shunting or surgical exploration and ligation of the leaking lymphatic vessels or fibrin glue application, which adds to their morbidity.^1,8,9

There is no consensus on the exact duration conservative treatment should be tried before resorting to surgical treatment, with some authors advocating a trial period of 4–8 weeks owing to the high rate of response.^1,7 However, some authors recommend early surgical intervention to avoid prolonged hospitalization and deterioration of the metabolic state of the patient.¹²

Intranodal lymphangiography (INL) and lymphatic embolization (LE) have proven efficient in the management of patients with iatrogenic chylothorax.¹³ They have also reported efficacy in adult patients with iatrogenic chylous ascites, although less established.^5,14 The literature supporting this procedure in the pediatric population is, however, scarce and limited to case reports or subsets of larger cohorts^5,15–18 (Table 1). This single-center retrospective study highlights the role of INL with or without embolization in management of iatrogenic chylous ascites in the pediatric population.

Table 1.

Review of Literature

Author	Year	Patients	Age in years	Original surgery	Presentation	Leak	Surgery to address chylous leak	Intervention	Results
Snow et al.¹⁵	2014	1	9	Resection of retroperitoneal myofibroblastic tumor and multivisceral transplantation	Right chylothorax and chylous ascites	Identified	None	Thoracic duct embolization using microcoils and NBCA glue	Right chest tube removed 2 weeks later, outcome of chylous ascites not reported
Nadolski el al.¹⁶	2017	2	12 and 18	1st patient: retroperitoneal dissection for testicular cancer 2nd patient: portosystemic anastomosis for splenic vein thrombosis	Chylous ascites	Identified	None	1st patient: lymphangiography alone 2nd patient: nodal NBCA glue embolization	Resolved
Gemmete et al.¹⁸	2017	1	3	Resection of the right kidney, ureter, and IVC for Wilms' tumor	Chylous ascites	Identified	Initial treatment, with lymphatic vessels suture ligated and Fibrin sealant used	Nodal NBCA glue embolization	Nodal NBCA glue embolization, with repeat embolization of the right side 4 days later, followed by resolution of leak in 10 days
Majdalany et al.⁵	2018	2	3 and 15	1st patient: radical right nephrectomy for Wilms' tumor 2nd patient: retroperitoneal mass resection for testicular cancer	Chylous ascites	1st patient: leak identified 2nd patient: leak not identified	None	1st patient: nodal NBCA glue embolization 2nd patient: retrograde thoracic duct embolization	1st patient: repeat nodal glue embolization after 4 days, followed by resolution of leak in <15 days 2nd patient: resolution of leak in <15 days
Vora et al.¹⁷	2019	1	7	Resection of abdominal lymphangioma at 4 months, followed by re-excision at 3 years	Chylous ascites	Identified	None	Lymphangiography alone	No ascites visualized on imaging 7 days postprocedure
Woerner et al.²²	2020	2	1 and 5	1st patient: right adrenalectomy, retroperitoneal lymph node dissection, and nonsegmental liver resection 2nd patient: left adrenal mass resection and extensive retroperitoneal lymph node resection	Chylous ascites	Identified	None	Nodal NBCA glue embolization	1st patient: resolved after 1 month 2nd patient: resolved after 2 weeks

IVC, inferior vena cava; NBCA, n-butyl cyanoacrylate.

Materials and Methods

Institutional Review Board approval was granted for this retrospective study. Medical records review from 2017 to 2019 captured six patients (four females and two males; age range 11–39 months) who underwent INL with or without LE for management of chylous ascites after abdominal surgery. Demographics and clinical data of study patients are shown in Table 2. All cases were done under general anesthesia.

Table 2.

Demographics and Clinical Data of Patients

Patient number	Age in months	Gender	Weight in kilograms	Primary cancer	Surgery	Lymphatic involvement during surgery	Time between surgery and lymphatic intervention in days	Output from drain 1 day before lymphangiography in mL	Presentation
1	34	Female	10.3	Left neuroblastoma	Left thoracoabdominal incision with adrenal tumor resection and retroperitoneal lymph node dissection	Retroperitoneal lymph node dissection	57	700	Chylous ascites
2	29	Male	10	Right neuroblastoma	Right thoracoabdominal incision with adrenal tumor resection and retroperitoneal lymph node dissection	Retroperitoneal lymph node dissection	18	1390	Right chylothorax then chylous ascites
3	11	Female	9.2	Left neuroblastoma	Left thoracoabdominal incision with adrenal tumor resection and retroperitoneal lymph node dissection	Retroperitoneal lymph node dissection	7	725	Chylous ascites
4	51	Female	16	Recurrent left neuroblastoma	Left thoracoabdominal incision with resection of recurrent mass anterior to the aorta and retroperitoneal lymph node dissection	Lymphatic leak managed by 4-0 silk sutures	6	400	Chylous ascites
5	13	Female	12.2	Right neuroblastoma	Right thoracoabdominal incision with adrenal tumor resection and retroperitoneal lymph node dissection	Lymphatic leak managed by titanium hemoclips	4	40 from right chest tube, 900 from abdominal drain	Right chylothorax and chylous ascites
6	39	Male	13.6	Left neuroblastoma	Gross total resection	Not reported	52	2000 drained on the day of the lymphangiography	Chylous ascites

Technical aspects of INL and LE have been previously reported.^14,19 Before starting the INL, fluoroscopic scout films of the abdomen and pelvis are taken, which are very valuable in identifying a site of leakage due to the large number of surgical clips these patients have in the retroperitoneum. The skin from the costal margin to the mid thighs is then surgically prepped and draped.

Under ultrasound guidance, a 25-gauge needle is advanced into the corticomedullary junction of one of the inguinal lymph nodes (bilateral access is preferred if feasible). Once needle position is confirmed by ultrasound, Lipiodol is slowly injected by hand. The beaded narrow appearance of the lymphatic vessels on fluoroscopic imaging, along with the slow filling confirms intralymphatic location (Fig. 1). The dose of Lipiodol used was according to the manufacturer's recommendations; 0.25 mL/kg with a maximum dose of 6 mL.

FIG. 1.

(a) An ultrasound image of a longitudinal section view of an inguinal lymph node (thick arrow), which is used for lymphangiography. (b) A 25-gauge needle (arrowheads) positioned within the inguinal lymph node (thick arrow) under ultrasound guidance to initiate lymphangiography. (c) A fluoroscopic image with the needle positioned within the inguinal lymph node and Lipiodol injected and flowing within the small lymphatic vessels (thin arrow).

Fluoroscopic images are captured at intervals to visualize progressive filling of the pelvic and abdominal lymphatics. Images are compared with the prelymphangiography scout films to identify the site of lymphatic leakage, seen as pooling of Lipiodol (Fig. 2). Once a site of leak is identified, a 25-gauge needle is used to percutaneously access the site of leak or the lymph node upstream from the leak under fluoroscopic guidance. The location of the needle tip is confirmed by oblique fluoroscopic views and visualized dispersal of Lipiodol under fluoroscopy on injection of Dextrose 5% through the needle (Fig. 3). LE is then done using Lipiodol and n-butyl cyanoacrylate (n-BCA) (TRUFILL; Codman Neuro, Raynham, MA) mixture in a ratio determined by the operator according to the distance between the access site and the leak (1:1 if accessing the site of the leak, higher ratio of Lipiodol if accessing the upstream lymph node). LE is completed when the Lipiodol—n-BCA mixture is seen filling the site of the leak under fluoroscopy, and the needle is then removed and the procedure is completed.

FIG. 2.

This figure shows a fluoroscopic image of the Lipiodol-filled abdominal lymph nodes during lymphangiography, with filling in of a site of leakage seen (circle) in figure (a) followed by (b) and (c). In this group of patients, the large number of radio-opaque surgical clips make it difficult to identify a site of leakage, which is why prelymphangiography scout films are important for comparison.

FIG. 3.

This figure shows a fluoroscopic image of a 25-gauge needle (arrowheads) used to puncture the lymph node (thick arrow) immediately upstream from the site of leakage. Once the tip of the needle is confirmed to be within the lymph node using oblique views and fluoroscopic visualization of dispersal of Lipiodol upon puncturing the lymph node, glue embolization is done. Lipiodol to n-BCA ratio is decided by the operator and varies according to the distance of the site of leakage from the site of needle access for embolization. n-BCA, n-butyl cyanoacrylate.

Technical success of INL was defined as cranial flow of Lipiodol (Guerbet, Villepinte, France) into the lymphatic vessels of the pelvis and abdomen. Technical success of LE was defined as the ability to access the site of leakage or an upstream lymph node with needle and administration of intended amount of glue embolic. Clinical success was defined as resolution of chylous ascites and removal of the drainage catheter without the need for surgical intervention. If there was no decrease in catheter output 5–7 days after the procedure, then the procedure was deemed clinically unsuccessful.

In one patient out of six, the leak was visualized on the first INL and LE was done. In three patients, the leak was not visualized on the first INL and no embolization was done, but drain output decreased and INL was not repeated. In two patients, the leak was not visualized and no embolization was done, but drain output did not decrease and INL was repeated. Repeat INL identified a leak in one patient and targeted LE was done. Repeat INL did not identify a leak in the other patient, but empirical LE was performed at the sites suspicious for leakage after discussion with the pediatric surgery team.

In that patient, LE was targeted at two lymph nodes; a left external iliac lymph node and a left retroperitoneal lymph node at the level of the umbilicus similar to the technique described earlier.

Results

All eight INL procedures were technically successful (100%). INL was able to identify the site of lymphatic leak in two patients (33%). In the three patients who underwent LE (two targeted at the site of identified leak and one empirical at sites suspicious for leak), one of the targeted LEs (33%) was technically and clinically successful and the other two (one targeted and one empirical) were technically successful but clinically unsuccessful, and required surgery to address the lymphatic leak (27 and 10 days, respectively) with identification of the site of leakage and successful management. In three patients, chylous ascites resolved after INL alone with no additional interventions. The results are displayed in Table 3.

Table 3.

Procedural Details, Complications, and Outcomes

Patient number	Lymphangiography	Leak	Embolization	Complications	Outcome
1	Bilateral	Not visualized	Not attempted	None	No decrease in drain output, procedure repeated 6 days later
1 (second procedure)	Bilateral	Not visualized	Percutaneous glue embolization of left external iliac lymph node and left retroperitoneal lymph node	None	No decrease in drain output, surgical exploration 10 days later with successful identification of leakage site and management, with drain removal 3 days later
2	Bilateral	Visualized on the right side at level of L4	Percutaneous glue embolization of the site of the leakage	None	Gradual decrease in drain output, with drain removed 18 days later
3	Bilateral	Not visualized	Not attempted	Diarrhea	Gradual decrease in drain output, with drain removed 6 days later
4	Bilateral	Not visualized, but right iliac venolymphatic communication seen	Not attempted	None	Gradual decrease in drain output, with drain removed 4 days later
5	Bilateral	Not visualized	Not attempted	Aspiration pneumonia requiring PICU admission	Gradual decrease in drain output, with right pleural drain removed 2 days later and abdominal drain removed 11 days later
6	Unilateral, left	Not visualized	Not attempted	Hypotension after paracentesis done at the same setting requiring PICU admission	No decrease in drain output, procedure repeated 15 days later
6 (second procedure)	Unilateral, left	Visualized on the left side at level of L1	Percutaneous glue embolization of the site of the leakage	None	No decrease in drain output, surgical exploration 27 days later with successful identification of leakage site at the same location and management, with drain removal 6 days later

PICU, pediatric intensive care unit.

Three patients had complications related to lymphangiography, two were class D and one was class B according to the Society of Interventional Radiology complication classification system. One patient had diarrhea for 2 weeks after the procedure that resolved with no additional interventions. One patient became hypotensive during the lymphangiography and after paracentesis of 2 L done during the same session, which required pediatric intensive care unit (PICU) admission and pressor support. One patient developed decreased oxygen saturation after the INL with a clinical diagnosis of aspiration pneumonia, which also required PICU admission. Both patients were discharged from the PICU 2 days later with no additional interventions. The average length of follow-up was 13.8 months (13–26 months) with no reported long-term complications and no mortality.

Discussion

INL has become the preferred approach for opacifying the lymphatic system in chest, abdomen and pelvis, effectively replacing the more time-consuming and invasive conventional pedal lymphangiography.¹⁹ In addition to its usefulness as a diagnostic modality to identify and localize lymphatic leaks in preparation for interventional or surgical management, lymphangiography has also been reported to be useful as a treatment method in some patients.²⁰ This is believed to occur because of a localized inflammatory reaction that happens surrounding the site of Lipiodol leakage that obstructs the afferent and efferent lymphatic vessels.²⁰ Dynamic contrast-enhanced magnetic resonance lymphangiography is a developing technique that is proving value in imaging of the lymphatic system, but it is still not widely available.²¹

The use of INL with or without embolization for the management of iatrogenic chylous ascites in pediatric patients has been reported in a handful of patients with encouraging results (Table 1). Of the nine reported cases in the literature, INL was successful in identifying a leak in eight patients (88.9%). Two patients in the literature underwent intranodal lymphangiogram with no embolization, and both were clinically successful.^16,17 The remaining seven patients underwent embolization with reported clinical success, with two patients requiring repeat embolization.^5,18,22 Lower clinical success in this series might be explained by publication bias.

In the reported cases in the literature and in four of six patients in this study, additional surgery was successfully avoided. Although it has been reported that surgery to address lymphatic leaks in pediatric patients with iatrogenic chylous ascites does not significantly affect mortality, it is not without added morbidity and risks.⁷ The reported complications after lymphangiography and embolization in adult population are leg swelling, diarrhea, and asymptomatic embolization of lungs with glue.^5,13 The complications in this study population are relatively higher than reported in the literature, although one can argue that the hypotension in one patient was likely related to the paracentesis rather than the lymphangiogram, and the hypoxia in another patient was related to aspiration and not lymphangiography as there was no evidence of Lipiodol in the patient's lungs on computed tomography images after the procedure.

The suggested duration for conservative treatment is 4–8 weeks, with most patients resolving in 1–6 weeks.^7,16 However, most authors advocate for early intervention in adult patients with drainage exceeding 1 L/day for 5 days, and some authors advocate for early intervention in all patients to avoid nutritional and immunological depletion.^20,23 Dugue et al. identified a cutoff value of 10 mL/kg drain output in adult patients with chylothorax 5 days after esophagectomy, which showed 100% specificity in identifying patients who needed surgical management from those who did not.²⁴ These recommendations specifically address iatrogenic chylothorax in adult patients and applicability to a pediatric population is not known.

The low complication rate and relatively high efficacy reported with INL and embolization for iatrogenic chylous ascites, along with the added morbidity of surgical exploration, encourage having a low threshold for undergoing INL with or without embolization. This particularly applies to patients who had retroperitoneal surgery, where the site of lymphatic leakage is likely from the retroperitoneal lymphatics and is, therefore, reached by the Lipiodol administered during INL, as opposed to patients with chylous ascites after surgeries where the retroperitoneal lymphatics were not touched, who may have lymphatic leaks from hepatic or mesenteric lymphatics, which are not visualized by INL. This is hypothesized to minimize metabolic and immunological deterioration through decreasing the duration of chyle loss by accelerating the healing process of leaks that were potentially going to heal after prolonged conservative treatment alone, and possibly identifying leaks that would likely fail conservative treatment and would inevitably need surgical intervention.

Conclusion

INL with or without LE is safe in treatment of iatrogenic pediatric chylous ascites. Early utilization before more invasive surgical intervention should be considered given the percentage of patients that responded clinically to INL without LE.

Footnotes

Author Disclosure Statement

The authors declare that they have no conflict of interest.

Funding Information

This study was funded in part through the NIH/NCI Cancer Center Support Grant P30 CA008748.

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