Objectives: Chyle leak or chylous ascites remains a rare complication after laparoscopic living-donor nephrectomy. Its cause and management have not been well elucidated in the literature. Thus, the aim of this study was to review the incidence of chyle leak/chylous ascites after laparoscopic living-donor nephrectomy in our institute and in the literature to propose a classification system with its associated treatment strategy.

Materials and Methods: In this retrospective review of laparoscopic living-donor nephrectomy patients from January 2005 to April 2016, we identified patients with chyle leak/chylous ascites along with the care performed. A proposed classification system based on our experience and literature is described.

Results: Chylous leak developed in 4 donors (2.25%). Of the 4 donors, 3 were treated nonoperatively with diet modification and subcutaneous octreotide injection. One patient required surgical intervention after not responding to second-line therapy with total parenteral nutrition.

Conclusions: Chyle leak/chylous ascites after laparoscopic living-donor nephrectomy is rare, but a delayed diagnosis may lead to morbidity secondary to malnutrition and immunosuppression. Meticulous surgical dissection is essential to seal the lymphatic tubes during laparoscopic living-donor nephrectomy. The proposed classification system provides a practical and tailored guide to management based on the drainage volume of chyle leak and a guide to the earlier identification of refractory cases.

Key words : Chylous ascites, Retroperitoneoscopic approach, Transperitoneal approach

Introduction

Laparoscopic living-donor nephrectomy (LDN) has become the standard of care in most transplant centers in the world, owing to its multiple benefits of quicker recovery, less postoperative pain, better cosmetic results, and comparable graft function.¹ Postoperative chyle leak (CL) or chylous ascites (CA) is a rare complication that could be detrimental to a healthy donor. The incidence is reported to be from 0.2% to 6.7% in surgeries with dissection adjacent to the lymphatic systems, such as repair of abdominal aortic aneurysm, dissection of retroperitoneal lymph nodes, pancreatic resections, thoracic surgeries, esophageal surgery, left neck dissections, laparoscopic colorectal surgery, liver transplant, and gynecologic procedures.^2-8 Chyle leak/chylous ascites after LDN was first described by Shafizadeh and associates in 2002,⁹ with subsequent reports showing incidences ranging from 0.07% to 3.8%.^10-15 However, the cause, preventive measures, and definitive management have not been well described in the literature. Therefore, the aim of this study was to review CL/CA in our cohort of patients after LDN and to review the literature to propose a classification for CL/CA and its associated therapeutic strategies.

Materials and Methods

This study was approved by the human research ethics committee of our institute before the study began. This study conformed to the ethical guidelines of the 1975 Helsinki Declaration. A retrospective review of medical records was conducted of 178 laparoscopic donor nephrectomies performed between January 2005 and August 2016. Of the 178 LDNs, 134 were performed by the transperitoneal approach (TA), whereas 44 were by the retroperitoneoscopic approach (RA) without hand assistance in either group.

The technique for TA has been previously described.¹⁶ For RA, briefly, the patient is placed on a lateral decubitus position with the table flexed. Three ports are used for all cases. A balloon dilator is inserted into the retroperitoneal space via a small port incision below the 12th rib at the middle axillary line to establish the working space. Two more 12-mm ports are placed under vision. Pneumoretro-peritoneum pressure is set at 12 mm Hg. The ureter is usually first visualized and dissected toward the kidney, and the Gerota fascia is incised. The kidney is pushed medially by a fan retractor, and the renal artery and vein are identified. The dissection of the renal artery and vein is conducted meticulously using LigaSure (Medtronic, Minneapolis, MN, USA) and an electrocautery hook device followed by dissection of the kidney from the attachment. The ureter is divided at the level of the iliac vessels. At this stage, a small incision is made at the iliac fossa with the insertion of GelPort (Applied Medical, Rancho Santa Margarita, CA, USA) for kidney extraction. The renal artery is divided with the EndoTA (Medtronic) stapler with placement of an additional Hem-o-lok (Teleflex Medical, Research Triangle Park, NC, USA); the renal vein is divided after occlusion with 2 large Hem-o-loks. The kidney is then extracted via the GelPort. A 15F Blake drain is placed in the kidney bed after check of hemostasis and CL. The wound and port sites are closed in layers.

Results

Of the 178 LDNs, there were 4 cases of CL/CA (1 from the TA group and 3 from the RA group).

Case 1
Case 1 was a 31-year-old male patient who underwent an elective left LDN (TA procedure). Chyle leak presented after the lymphatic tubes were divided, and a Hem-o-lok was applied to the lymphatic stump. On postoperative day 1 (POD1), the drain output was 400 mL of serum fluid, which increased to 1050 mL later that day and was milky in appearance. The patient showed distension of abdomen on POD2, with drain output again of 1500 mL of milky fluids. Chylous ascites was diagnosed (Figure 1), and a low-fat/medium-chain triglyceride diet (LFD/MDT) was commenced with subcu-taneous injection of octreotide (100 μg 3 times/day). Improvement was observed as the drain output gradually reduced to 150 mL/24 hours on POD5. The drain was removed, and the patient was discharged on POD5. On POD9 at clinic follow-up, the patient presented with abdominal distention and left thigh and scrotal edema. An ultrasonograph of the abdomen showed only a small amount of free fluid (35 × 11 mm). The patient was advised to continue on LFD/MDT.

Two weeks later, the patient presented with gross abdominal distention and shortness of breath. Repeat ultrasonography showed massive ascites that was subsequently drained with insertion of a pigtail drain. The drainage volume was 7500 mL of chyle fluid (Figure 2). He was readmitted and commenced on total parental nutrition (TPN), restricted to clear fluids with subcutaneous octreotide (100 μg 3 times/day). The dose of octreotide was increased to 200 μg at 3 times/day on day 5 of readmission. The drain output gradually reduced to 800 mL on day 6. The patient was then weaned from TPN and again commenced on LFD/MCT. He was discharged with drain in situ on POD29 and followed-up daily through community nurse visits.

Drainage continued consistently at about 800 mL/day. One week later (POD36), he was readmitted for laparoscopic exploration and ligation of chylous lymphatic leakage. During laparoscopic exploration, a cavity was found medial to psoas at level of hilum and was closed with 4/0 Prolene stitches (Ethicon, West Somerville, NJ, USA); a piece of omentum was sutured to the psoas muscle to reinforce the closure followed by placement of a 15F Blake drain. On day 2 after the laparotomy (POD38), the patient commenced on TPN, clear fluids, and subcutaneous octreotide at 100 μg (3 times/day). Drain output continued to be about 1000 to 1400 mL daily up to POD43, which led to further investigation.

Lymphoscintigraphy (99mTc antimony sulfide colloid) was performed, which demonstrated presence of isotope in the abdominal cavity. However, the investigation could not identify the leak site. Open exploratory laparotomy was required on POD79, and a leakage was suspected at the medial side of the left kidney bed adjacent to the course of inferior mesenteric vein. The leaking point was repaired in 2 layers with 3/0 Vicryl (Ethicon) and omentum anchored to the area. The patient continued on TPN, clear fluids, and subcutaneous octreotide at 100 μg (3 times/day) for an additional 5 days postoperatively. After the drainage, volume was less than 300 mL/day; the patient ceased TPN and commenced on LFD and was discharged home on POD104. The drain was removed before discharge. On follow-up clinic review on POD134, his CA had resolved, and he had returned to a full diet.

In summary, the patient had 2 readmissions; he was on TPN twice for 72 days in total, LFD for 55 days, and subcutaneous octreotide for 27 days during the first admission and for 14 days after the second surgery.

Cases 2-4
These 3 cases of CL occurred in the RA group (2 female and 1 male patient; age ranging from 26 to 59 y). The surgeries were completed without any complications. All incidences of CL were diagnosed on POD1 with classical chyle appearance in the drain fluid and with volume ranging from 300 to 700 mL over 24 hours (Figure 3). Drain fluid cytology and biochemical tests (triglycerides) were done for 2 patients, which confirmed the diagnosis of CL. An LFD/MCT diet was initiated on the day of diagnosis in all cases. Subcutaneous octreotide was commenced on the same day for 2 patients, whereas 1 patient was not given this owing to the small volume of CL. All 3 patients responded well without need for interventional procedures. One patient had the drain tube removed before discharge on day 5, whereas the other 2 patients were discharged home with the drain in situ on days 5 and 7. The drain volume consistently declined on daily measurement. The drains were removed on day 8 and day 13, respectively, when the drainage was dry and patients were back to normal diet. There was no further adverse sequela.

Discussion

Chyle leak/chylous ascites is a rare but potentially serious complication after abdominal surgery. It is most commonly reported after repair of abdominal aortic aneurysm and surgeries with dissection of the lymphatic trunks.² At present, it appears that CL after LDN has a higher incidence of 0.07% to 3.8%^10-13 than previously reported (0 to 1.83%)¹⁷. Hence, it is considered to be a significant complication after LDN for healthy donors. In our cohort, the incidence was 2.25%, although only one (0.56%) was classified as a Clavien IIIb complication, for which the patient required laparotomy twice and TPN for a total of 72 days.

It is evident that CL/CA is associated with prolonged hospital stays and hence health care costs. It may lead to high morbidity due to malnutrition, electrolyte imbalances, and immunosuppression secondary to protein and lymphocyte loss^5,17,18 if diagnosis and treatment are delayed. To the best of our knowledge, there are 48 cases of CL reported after LDN in the literature. Of the 48 cases, Coumartin and associates¹⁹ reported a patient with severe CL who was refractory to both conservative (LFD/MCT and TPN) and surgical intervention (clipping and suturing the prominent lymphatic channels around the aorta at the level of left renal hilum) and required prolonged hospitalization. Of note, the donor developed psychiatric stress during the prolonged hospitalization. Another case was reported by Aerts and associates¹⁷ in which the patient was extremely cachectic secondary to ongoing CL despite nonoperative care 52 days after LDN. The patient subsequently underwent a 6-hour laparoscopic retroperitoneal surgical exploration on POD57 with subsequent complete resolution of CL. Details from the published literature are listed in Table 1.^{4,9,10,14,15,17,19-33}

From an anatomic perspective, the cause of CL is understood due to division of paralymphatic trunks that connect with the intestinal truck to form the cistern chyli at the level of renal hilum during dissection of renal vessels. In LDN, the dissection is adjacent to the aorta to obtain a maximum length of renal vessels for the subsequent kidney transplant. In addition, along the para-aortic area, it is rich in lymph vessels and lymphatic major trunks (Figure 4). In the literature, left LDN is generally preferred over right due to its favorable longer renal vein. Therefore, CL/CA is mostly reported from the left side. Another explanation is due to the lateral dissection of the right-side kidney without need of dissection close to the para-aortic area. Perhaps it is underreported, as shown in a survey in which 18 of 30 centers did not respond.³⁴ In a large Korean study,4 the incidence of CA was 6.7% after laparoscopic radical nephrectomy. The incidence was also significantly higher in the group involving laparoscopic radical nephrectomy with lymphade-nectomy (13.9% vs 4.0%; P = .027). In their study, CL/CA was more common in the left than right (7.3% vs 2.5%; P = .010). The number of vessels was not associated with CL/CA10,^17,34 as found in our study.

It is inevitable that some major lymphatic tubes will be divided during donor nephrectomy. Based on the experience of 1510 cases of LDNs, Simforoosh and colleagues suggested avoiding dissection close to the aorta to prevent the division of lymphatic tubes.³⁵ The use of electrocautery and LigaSure allows the lymphatic tubes to be automatically sealed.³⁶ Chyle leak occurs as some of these lymphatic tubes may be not sealed properly or may subsequently reopen. Moreover, small lymphatic tubes could be overlooked in the setting of pneumoperitoneum.^24,30 Malik and associates investigated LigaSure and tissue glue for control of CL, but there was no significant change in the incidence of CL.³⁷ However, a change in technique by applying clips in addition to the use of an energy device has reduced the occurrence of CL.4,38

An alternative technique was explored where bipolar electrocoagulation was used instead of monopolar electrocautery. In an initial experience of bipolar electrocoagulation, there were no cases of CL after laparoscopic retroperitoneal lymph node dissection for patients with nonseminomatous germ cell tumors.³⁹ In TA, smaller volume CL may be absorbed without causing clinical significance; it may only become apparent if the leak has a large volume such as in our case 1. The time frame of CL/CA ranges from 7 to 45 days after TA, and this may be associated with a patient increasing diet during recovery.⁴⁰ In RA, a small volume of CL is more likely to be symptomatic due to malabsorption from the retroperitoneal cavity. It may leak into the chest and develop chylothorax as a result of local pressure.²⁴ The time frame for CL/CA after RA should present early due to the small retroperitoneal space, although this was not observed in the literature (mean 11 d; range, 8-14 d).^24,31 It was noted that CL/CA was recognized earlier in our cases (POD1) as a result of placement of drainage after surgery compared with other case series.^4,10,22,31 Therefore, placement of a drain may help early diagnosis and prompt management of CL.32 Careful inspection during hemostasis is also important to identify any potential CL and to secure it with additional clips.^{4,7,10,21,24,26,27,41,42}

Abdominal ultrasonography for diagnostic and therapeutic (paracentesis) purposes is essential. A percutaneous pigtail drain should be inserted for drainage concurrently if the primary drain is dysfunctional. Computed tomography may be considered for complicated cases. The findings are normally difficult to differentiate from other liquids such as urine, bile, and bowel secretions.³ The fluid obtained from drain or paracentesis should be sent to the laboratory for lipid profile and microbiology tests, which is typically characterized as chylomicron-rich with triglyceride concentration of more than 1.2 mmol/L.⁴⁰ It is also paramount to exclude an infection by microbiology test. Bipedal lymphan-giography can be used to identify the site of leakage, but this is cumbersome and operator dependent, whereas lymphoscintigraphy is easier to perform and is valuable for identification of leak site.^3,26

The management of CL has not been well described in the literature, although various algorithms have been reported.^3,32,43 The goal of conservative management is to reduce mesenteric lymphatic flow and subsequently decrease CL into the peritoneal/retroperitoneal cavity, allowing the injured site to heal. A trial period of 4 to 8 weeks of conservative care is generally recommended, as about 60% of CL tend to resolve.^17,40,44 Diet modification (LFD and MCT) is the mainstay of conservative care, where it is crucial for reducing lymphatic flow. Medium-chain triglycerides are primarily absorbed across the intestinal mucosa and directly into the portal system compared with long-chain triglycerides. Thus, the lymphatic channels are bypassed. Apart from that, early administration of somatostatin and its analogs is recommended as they are believed to reduce intestinal fat absorption, lymphatic flow, and triglyceride concentration.^3,45 Salt restriction or diuretic treatment has been only described sparingly in the literature with uncertain results.^9,27,28

No consensus has been established for the duration of diet modification on clinical resolution, especially in patients with moderate CL.^{3,19,22,28,32} A time frame of 1 week to 6 months after resolution of CL has been reported in the literature for diet modification. Instead of applying a similar duration for all, we advocate considering it according to clinical response to avoid the problem of compliance.⁴⁶ Similarly, the appropriate duration for octreotide administration remains unknown. It was suggested to be at least 2 weeks of octreotide and reassessment if necessary for further management.³² There have been advancements in interventional radiologic techniques; however, these are yet to be universally accepted. These include percutaneous embolization from outside of the lymph vessel and computed tomography-guided percutaneous injection of adhesive glue (N-butyl cyanoacrylate glue) to the extralymphatic leakage site.^47-49

It has been recognized that the management of CL varies greatly (Table 2). Therefore, we would like to propose a classification system and an associated strategy for care based on our clinical experience and literature review.

First, we define mild CL as volume of less than 300 mL. The treatment is noninterventional, and the patient is restricted to LFD/MCT for 1 to 2 weeks, after which a normal diet can be resumed. Subcutaneous octreotide at 100 μg at 3 times/day should be commenced immediately. The drain is to remain in situ until it is dry. A dietician should be involved early to provide education to patients about the exact food to be allowed and assist in protein supplementation.

Second, moderate CL is defined as leakage volume of between 300 and 800 mL. The treatment is noninterventional. The patient is restricted to LFD/MCT for 2 weeks. The patient is commenced on subcutaneous octreotide at 100 to 200 μg 3 times/day concurrently. The drain is kept in situ until it is dry. The patient can be discharged, and a community nurse providing daily follow-up is recommended. Having this support will identify those who warrant urgent surgical review and provide mental support to prevent the development of psychiatric disorders.¹⁹

Finally, severe CL is defined as leakage volume of more than 800 mL. The treatment includes restricting the patient to nil by mouth but allowed to have water only18 and initiating TPN at an early stage of the diagnosis. Surgical intervention should be consi-dered during early observation depending on the response to the initial management. This is because prolonged drainage of large volumes will result in loss of protein and lymphocytes, leading to malnutrition and risk of infection.^3,19,32,43 Nonetheless, the timing to consider surgical exploration has not been well defined. We recommend that no response after 2 weeks with nil by mouth and TPN warrants surgical exploration.³² Laparoscopic exploration can be attempted to identify the leakage and repair it, with success rates of up to 86%.^{4,17,20,21,25-27,32} High-fat diet/milk can be given before surgery to help identify the leaking site.^20,21 Multiple techniques have been described in the literature to repair the defective laparoscopically with clipping and applying fibrin glue to the leaking site. A suture ligation is more definite during surgical approach.^17,20,27 Omentum may be used to reinforce the surgical repair if it is appropriate during surgical exploration.

Conclusions

In summary, CL/CA after LDN is rare, but it may increase the morbidity for a healthy donor if the diagnosis and management are delayed. The incidence ranges from 0.07% to 3.8%. Its cause is believed to be due to disruption of lymphatic tubes during dissection of renal vessels. Meticulous surgical dissection is essential to seal the lymphatic tubes during the procedure. Early diagnosis and treatment are critical to minimize morbidity. Mild and moderate CL usually recovers with restriction on LFD/MCT diet modification and octreotide administration. Use of TPN and subsequent surgical exploration may be inevitable in severe cases. The proposed classification system may provide guidance for diagnosis and definitive treatment, improving outcomes.

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