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Asian J Endosc Surg ISSN 1758-5902

O R I G I N A L A RT I C L E

Chylous ascites after laparoscopic donor nephrectomy Ho Yee Tiong,1 Raj K Goel,2 Wesley M White,2 David A Goldfarb1 & Jihad H Kaouk2 1 The Transplant Center/Glickman Kidney and Urological Institute, Cleveland Clinic, Cleveland, Ohio, USA 2 Section of Laparoscopic and Robotic Surgery, Cleveland Clinic, Cleveland, Ohio, USA

Keywords Complications; donor nephrectomy; laparoscopy Correspondence Jihad Kaouk, Section of Laparoscopic and Robotic Surgery, Cleveland Clinic, Cleveland, OH 44195, USA. Tel: +1 216 445 7241 Fax: +1216 445 2267 Email: [email protected] The present address of H. Y. Tiong is: Department of Urology, National University Hospital, 1E Kent Ridge Road. Singapore 119228. Email: [email protected] Received 15 May 2014; revised 7 August 2014; accepted 8 August 2014 DOI:10.1111/ases.12144

Abstract Introduction: The aim of this study was to determine the incidence, presentation, management, and outcomes of chylous ascites following laparoscopic donor nephrectomy. Methods: An Internet-based, multi-institutional survey was performed using http://www.surveymonkey.com. An email invitation to the voluntary survey was sent to 30 transplant centers and posted on CenterSpan, an email forum for transplant surgeons. The number of living donor transplantations and the number of cases of chylous ascites with clinical information, treatment and outcomes were sought from the questionnaire. Results: A total of 12 centers responded and reported 7683 cases of live donor nephrectomy. The reported incidence of postoperative chylous ascites was 0.013% (n = 12). Six centers reported 10 cases of chylous ascites following laparoscopic donor nephrectomy and 2 cases after open donor nephrectomy. Among the eight patients who developed chylous ascites following laparoscopic donor nephrectomy, presentation was typically 2 weeks after the date of initial surgery. Conservative therapy was successful in 50% of cases. Refractory ascites managed secondarily with surgical intervention had a success rate of 100%. Conclusion: Chylous ascites is a rare complication following laparoscopic donor nephrectomy. Initial treatment should be conservative, with surgical therapy reserved for refractory cases.

Introduction Living kidney donation increased from 1817 cases in 1998 to 5966 cases in 2007 (1). This manifold increase is largely because of the introduction of minimally invasive donor nephrectomy procedures (based on Organ Procurement and Transplantation Network data as of 1 May 2009) (1). Live donor kidney transplantation offers many significant advantages over deceased donor transplantation, including better graft and recipient survival outcomes (1). Living donor nephrectomy, especially via minimally invasive approaches, is increasingly accepted to be of low risk, with complication rates reported to be 0.2%–0.6% for major complications and 8%–9.8% for minor complications (2–4). However, surgical complications are often documented with little consistency, and unique problems associated with them are likely to be under-reported (5).

Chylous ascites is an uncommon complication following major retroperitoneal surgery such as abdominal aortic surgery (6). Recent anecdotal case reports have likewise documented chylous ascites following laparoscopic donor nephrectomy (7–12). Chylous ascites can present a difficult problem with serious metabolic consequences. Its current incidence after donor nephrectomy is not known. The overriding concern in living kidney donation must be the safety and welfare of the healthy donor. To this end, all potential surgical complications inherent to donor nephrectomy must be known so that the donor can be fully informed prior to undertaking the altruistic act of kidney donation. The objective of this study was to undertake a multi-institutional Internet-based survey to assess the incidence, presentation, management, and outcomes of chylous ascites following donor nephrectomy.

Asian J Endosc Surg •• (2014) ••–•• © 2014 Japan Society for Endoscopic Surgery, Asia Endosurgery Task Force and Wiley Publishing Asia Pty Ltd

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Table 1 Work volumes at hospitals that participated in the survey (n = 12)

Total number of living donor kidney transplants at each center over the last 10 years Total number of laparoscopic donor nephrectomies at each center over the last 10 years Total number of open donor nephrectomies at each center over the last 10 years Average number of living donor kidney transplants reported at each center/year Average number of laparoscopic donor nephrectomies at each center/year Number of laparoscopic kidney donor surgeons at each center Number of open kidney donor surgeons involved at each center

Materials and Methods A two-part survey instrument was developed on the Internet using an online survey editor at http:// www.surveymonkey.com (Portland, USA). The first part of the survey included 10 questions to assess the total and annual number of living donor kidney transplantations at each participating transplant center over 10 years, the number of donor surgeons, and their experience with laparoscopic versus open donor nephrectomy. The second part of the survey included 22 questions and solicited data regarding the number of cases of chylous ascites at each hospital (if any) and clinical details regarding donor nephrectomy, presentation, management, and outcome for each case. Invitations were sent via email to the directors of living donor kidney transplantation programs at 30 institutions in the USA. These institutions were selected based on their literature reported clinical volume. The invitation was also posted on CenterSpan, an email forum hosted by the American Society of Transplant Surgeons for its members. The majority of its members are board-certified surgeons with additional training or experience in transplantation. Participation in the survey was voluntary. No identifiable patient information was solicited via the survey, and clinical details entered into the survey were kept anonymous and confidential. Data collection was secured with SSL encryption. Data were accrued beginning in February 2009 and continued for 2 months. Duplication was avoided by coding responses based on respondents’ assigned IP addresses. Institutional review board exemption for this study was approved by our institution. Descriptive analyses were used to ascertain the case volume of centers participating in the study and to report the incidence of chylous ascites after donor nephrectomy. Clinical data for each reported case, including donor patient demographics, kidney anatomy, operative details and its clinical features, management, and outcomes, were reviewed.

Results Of the 30 surveys sent to specific institutions, 12 (40%) were completed. Table 1 shows the case volume reported

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Mean ± SD

Total for all 12 centers

641.7 ± 506.8 386.3 ± 257.5 253.9 ± 330.2 52.4 ± 31.8 51.7 ± 30.7 2.8 ± 1.8 3.3 ± 2.3

7700 4636 3047 629 620 33 40

Table 2 Number of centers and cases reporting chylous ascites after donor nephrectomy with their calculated incidence n Centers reporting experience with chylous ascites after donor nephrectomy Chylous ascites cases reported after laparoscopic donor nephrectomy Chylous ascites cases reported after open donor nephrectomy

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10 2

Calculated incidence over 10 years –

2 per 1000 0.6 per 1000

by the transplant centers that participated in this survey. Overall, this series spanned a total of 4636 laparoscopic donor nephrectomies and 3047 open donor nephrectomies over a period of 10 years. A total of 33 laparoscopic donor surgeons and 40 open donor surgeons were involved in the series. Table 2 shows that 6 of the 12 centers reported experience with the complication of chylous ascites following donor nephrectomy. A total of 12 cases were reported by the six centers. Incidence was calculated for laparoscopic and open donor nephrectomy by dividing the number of reported cases by the total number of cases over the 10-year period surveyed. Complete clinical data were available for 8 of the 12 cases of postoperative chylous ascites. All cases with complete data were laparoscopic donor nephrectomies. Table 3 shows the demographic and clinical features of the cases reported. Only one of the patients had previous abdominal surgery (appendectomy). All the kidneys procured were left-sided with a single vein and ureter. Single arterial anatomy was found in six of the cases. Hilar control for all cases was with conventional techniques – locking clips or surgical staplers. All cases were reported to be straightforward, performed within 5 hours, and with a mean hospital stay of 3 days (range, 1–4 days). Abdominal pain and distension were the most commonly reported complaints in our series, as seen in Table 4. Fever was sparingly reported. One case reported leakage of ascites from the trocar insertion sites. The majority of patients presented approximately 2 weeks following donor surgery (range, 4–26 days). CT was

Asian J Endosc Surg •• (2014) ••–•• © 2014 Japan Society for Endoscopic Surgery, Asia Endosurgery Task Force and Wiley Publishing Asia Pty Ltd

Chylous ascites after donor nephrectomy

H Tiong et al.

Table 3 Patient demographics and clinical variables of reported cases of chylous ascites after laparoscopic donor nephrectomy (n = 8)

Table 4 Clinical features, treatment, and outcomes of reported cases of chylous ascites after laparoscopic donor nephrectomy (n = 8)

Clinical variables

Clinical variable

Clinical variables Type of surgery (n) Open Pure laparoscopic Hand-assisted laparoscopic Age, mean ± SD (years) BMI, mean ± SD Sex Male Female Race Caucasian African American Prior abdominal surgery Yes No Side of donor nephrectomy Left kidney Hilar anatomy Single artery Multiple arteries Surgical technique to control artery Multiple locking clips Endo GIA surgical stapler Endo TA surgical stapler Surgical technique to control vein Endo GIA surgical stapler Endo TA surgical stapler Operative duration 1–2 hours 2–3 hours 3–4 hours 4–5 hours Hospital stay after donor nephrectomy (mean days ± SD)

Clinical variable Presenting symptoms (n) Pain Abdominal distension Fever Time to presentation after donor nephrectomy, mean ± SD (days) Investigations performed (n) Ultrasound CT Paracentesis and fluid analysis Treatment and outcomes

0 6 2 37.4 ± 7.9 26.5 ± 2.3 3 5 7 1 1 7 8 6 2 4 2 2 7 1 1 1 4 1 3.0 ± 1.1

Endo-GIA and Endo-TA (Covidien, Mansfield, USA).

universally performed in the eight patients for diagnosis. Percutaneous drainage was performed by diagnostic and therapeutic purposes in six of the eight patients. Conservative therapy including dietary modification (low-residue diet) was initiated in all patients with documented chylous ascites (Table 4). Four of the eight cases demonstrated complete resolution following conservative treatment (Clavien grade II). An additional patient for whom initial dietary modification alone failed was subsequently salvaged with placement of a percutaneous drain (Clavien grade IIIa), which highlights the benefit that may be realized with this treatment approach. Three patients for whom conservative treatment failed were administered second-line medical therapy in the form of diuretics and/or somatostatin. No benefit was noted with these regimens, and these three patients subsequently underwent surgical intervention (two had open surgery

Dietary modifications Diuretics Somatostatin Percutaneous drainage Open surgery Laparoscopic surgery Duration of treatment period, mean ± SD (weeks) Follow-up, mean ± SD (months) Clinical recurrences after resolution (n)

4 6 1 15.0 ± 8.7

2/8 8/8 6/8 n

Resolved with treatment 8/8 4 1/8 0 2/8 0 6/8 1 2/8 2 1/8 1 5.4 ± 3.6 5.1 ± 8.8 0

and one had laparoscopic surgery) with a success rate of 100% (Clavien grade IIIb). On average, patients underwent treatment for more than 5 weeks (range, 2–12 weeks), representing significant morbidity. At a mean follow-up of over 5 months (range, 2–25 months), no recurrences were reported.

Discussion By using an Internet-based questionnaire survey, we obtained multi-institutional data from 12 transplant centers in the USA regarding their experience with chylous ascites following more than 7700 cases of donor nephrectomy over 10 years. Based on the information obtained in this survey, the incidence of chylous ascites following laparoscopic and open donor nephrectomy was 2 per 1000 and 0.6 per 1000, respectively. This confirms the rare nature of the condition, which was previously evidenced by few anecdotal case reports (7–12). To our knowledge, this is the first collaborative report of its kind, and this information should facilitate discussion of the condition with the prospective living kidney donor. Chylous ascites can result in significant morbidity with resultant nutritional and immunological disturbances (6). Patients in our series typically presented at 2 weeks after an initial apparently uneventful laparoscopic donor surgery and short hospital stay. Our survey did not reveal any hilar control techniques that might have been

Asian J Endosc Surg •• (2014) ••–•• © 2014 Japan Society for Endoscopic Surgery, Asia Endosurgery Task Force and Wiley Publishing Asia Pty Ltd

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associated with its provocation or development. The results of our survey and prior published reports show that cases of chylous ascites can develop via both the transperitoneal and the retroperitoneal approach (7–12). In addition, chylous ascites has been reported in a handful of cases after laparoscopic radical nephrectomy, but the exact incidence is unknown. However, it is likely to be less common than donor nephrectomy because there is less dissection of the para-aortic lymphatics (13). Although the rarity of the condition may make it difficult to diagnose, any previously healthy kidney donor who develops unexplained abdominal distention and enlarging girth at 14 days postoperatively should be evaluated for chylous ascites. Its subsequent diagnosis is fairly straightforward and involves a combination of imaging and/or paracentesis for ascitic fluid analysis. The typical fluid yield is milky, odorless, alkaline, and sterile. Typically, it has a high triglyceride content that is two- to eight-fold that of plasma (range, 0.4–4.0 g/dL) and has a specific gravity greater than 3 g/dL. Microscopic examination of fluid smears stained with Sudan III shows fat globules and leukocytes with lymphocytic predominance. Although CT findings are not specific to chylous ascites, it can distinguish the ascites with identical attenuation coefficients as water from a denser postoperative hematoma. Occasionally, CT may reveal the pathognomonic development of a fat-fluid level in the peritoneal collection when the patient remains horizontal for a sufficient period (14). Lymphangiography has been advocated early in the course to facilitate diagnosis and localization of the lymphatic leak in retroperitoneal and pelvic surgical cases. Unfortunately, lymphangiography is painful and tedious, and lacks reproducibility (15). As the area of lymphatic dissection for donor nephrectomy is around the aorta at the level of the renal hilum, its role in localizing the lymphatic leak in chylous ascites following donor nephrectomy is probably limited. Proposed treatments for chylous ascites from other types of retroperitoneal surgery include initial conservative modalities such as dietary intervention, treatment with diuretics, somatostatin analogs and even total parenteral nutrition (TPN) (6). Dietary intervention is the mainstay of non-operative therapy and involves a highprotein, low-fat, medium-chain triglyceride diet to decrease lymph flow into the major lymphatic tracts and facilitate closure of the chylous fistulae. In combination with paracentesis, dietary intervention is reported to be successful in about 50% to 67% of postoperative chylous asicites (16). Based on our survey, outcomes of chylous ascites following donor nephrectomy have similar results with conservative treatment regimens. However, it should be noted that paracentesis alone as a solitary measure is not as successful, with only 7% resolution in

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the review by Aalami et al. (16). It is part of the treatment regime as a symptomatic palliation for decreasing pain and dyspnea from abdominal distension. The disadvantages of repeat drainage of the ascitic fluid through multiple abdominal taps or a permanent catheter include prolongation of leakage, continued nutritional and immunological depletion, and a potentially higher risk of infection. TPN is usually recommended as a second-line therapy when enteral dietary manipulation fails, especially in patients who cannot tolerate adequate oral intake or those with refractory chylous ascites (17). TPN allows bowel rest, which may further decrease the production and flow of lymph. It can also restore nutritional deficits and metabolic impairments. After 2–6 weeks of TPN, 60%–100% of cases were reported to be resolved (16). In combination with TPN, somatostatin therapy can also be given both intravenously or subcutaneously with dose titration. An excellent response to somatostatin with a drastic decrease in output after 24–72 hours of therapy has been reported in a case of chylous ascites following radical nephrectomy (18). However, this report is anecdotal and other reports with somatostatin monotherapy have been disappointing (19). Although 8–12 weeks of conservative treatment is generally advocated for chylous ascites (6), the role and timing of surgical repair remains controversial. The contention of many transplant surgeons, our group included, is that surgical intervention for chylous ascites following donor nephrectomy should be instituted early to minimize the complications from a long period of conservative treatment (10). This may explain why our survey reported use of TPN and somatostatin in only two of the patients; the addition of TPN and somatostatin after initial failed conservative measures further prolongs the morbidity period of these originally healthy patients. Indeed, the patients from the centers in our survey were treated over a mean period of 5 weeks. Meinke et al. have identified that the most suitable candidates for early surgical intervention in chylous ascites following abdominal aortic surgery are those with good performance status and a localized lymphatic fistula (20). Kidney donors are younger and healthier than the majority of patients with chylous ascites after other major retroperitoneal operations; hence, they fit the criterion for early surgical repair. In addition, chylous fistula after donor nephrectomy is generally localized to the ascending lumbar lymphatic trunks along the aorta on the left and the inferior vena cava on the right around the level of the ipsilateral renal hilum. These lumbar lymphatic trunks merge posterior and medial to the aorta, behind the left crus of the diaphragm and in front of the first and second lumbar vertebrae to form the cisterna chili.

Asian J Endosc Surg •• (2014) ••–•• © 2014 Japan Society for Endoscopic Surgery, Asia Endosurgery Task Force and Wiley Publishing Asia Pty Ltd

Chylous ascites after donor nephrectomy

H Tiong et al.

Surgical treatment for this condition involves direct surgical ligation of the leaking lymphatic glands or even non-selective ligation in which fibrin glue is applied to the retro-aortic tissues targeted at that specific area. These reasons may explain, in part, the higher success rate realized with surgical intervention in our series (100%) as compared to the lower success rate (41%) demonstrated following surgical repair for chylous ascites after other interventions (17). Given these high success rates, surgical therapy should be considered a mainstay in the treatment of refractory chylous ascites following donor nephrectomy, and its application with laparoscopic approaches should be considered early and aggressively to avoid patient morbidity (12,13,21,22). Prospective prevention of lymphatic leaks during the initial surgery is probably the best cure and should be the primary goal. For laparoscopic donor nephrectomy, electrocautery alone may not be adequate in controlling the lymphatics around the aorta. Hence, at the initial donor nephrectomy surgery, locking or metal clips should be applied to the periaortic tissues during dissection of the renal hilum around the origin of the renal artery. During open donor nephrectomy, these are often easily suture ligated or clipped, which may explain why the incidence in open donor nephrectomy (0.6 per 1000) was lower than in laparoscopic donor nephrectomy (2 per 1000). We acknowledge the retrospective nature of this study and the likely selection and recall bias that may arise from survey-based studies. However, we believe that the novel use of an Internet-based survey enabled us to pool information on a rare condition from multiple institutions rapidly. In fact, Friedman et al. also used questionnaire surveys to report on uncommon hemorrhagic complications following donor nephrectomies (5). SurveyMonkey is an online survey tool that enables people of all experience levels to create their own surveys quickly and easily. It uses a powerful backend database and caching protocols to collect large amounts of data and organize these data in a way that can be viewed and manipulated through a Web-based interface. Currently, it is used by more than 80% of Fortune 100 companies to obtain feedback. With SSL encryption to secure medical data, we believe that it has uses in medical research. In conclusion, our Internet-based, multi-institutional survey confirms that chylous ascites is a rare complication after laparoscopic and open donor nephrectomy. Treatment can be initially conservative with surgical approaches used as second-line therapy with good success rates.

Acknowledgments The authors have no conflicts of interest to declare.

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Asian J Endosc Surg •• (2014) ••–•• © 2014 Japan Society for Endoscopic Surgery, Asia Endosurgery Task Force and Wiley Publishing Asia Pty Ltd

Chylous ascites after laparoscopic donor nephrectomy.

The aim of this study was to determine the incidence, presentation, management, and outcomes of chylous ascites following laparoscopic donor nephrecto...
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