Lymphoceles are common and well-known complications that occur in 1% to 26% kidney transplant recipients (1, 2). The cause of lymphocele formation is unclear, but it is believed to result from transection of the lymphatic vessels accompanying the external iliac vessels during transplantation surgery and subsequent lymph accumulation in a nonepithelialized cavity in the extra-peritoneal plane adjacent to the transplanted kidney (3). Predisposing factors include the use of mammalian target of rapamycin inhibitors (4, 5), high dose corticosteroids, and delayed graft function (6). Equally, careful and limited dissection and ligation of iliac lymphatic trunks have been shown to decrease the incidence of lymphocele formation (7).
Lymphoceles are usually small, asymptomatic, and found incidentally on routine ultrasonography after kidney transplantation 2 weeks to 6 months after transplantation with a peak incidence at 6 weeks (8). However, depending on their size and position, a tense lymphocele may affect transplant function by mass effect directly to the kidney, or by direct compression of the ureter or transplant vasculature. In addition, urinary frequency can result from bladder displacement and deep vein thrombosis after compression of the external iliac vein (3).
The therapeutic options for lymphoceles occurring after kidney transplantation include simple aspiration under imaging control drainage with or without sclerotherapy, and more invasive options of laparoscopic or open surgery to fenestrate the lymphocele into the peritoneal cavity. However, treatment decisions seem to be center dependent (3). Given the variability in clinical practice, we aim to evaluate and quantify the benefits and harms associated with the different approaches to symptomatic lymphocele management in kidney transplant recipients, and in turn, assist the kidney transplant clinician when presented with a problematic lymphocele in an inpatient or outpatient setting.
The initial search yielded 492 articles (see Figure, SDC 1,http://links.lww.com/TP/A481). Duplicates were excluded (n=8), leaving 484 studies for further analysis. Of these 484 articles, 416 were excluded for the following reasons: not pertaining to lymphocele management, case report, opinion-based review, no evaluation of treatment, and lymphocele developed after a different surgical procedure. Of the remaining 68 studies, a further 16 were excluded after review of the full-text publication for the following reasons: duplicate populations, lymphatic leaks rather than lymphocele, and diagnostic study without evaluation of treatment. A total 52 studies were included in the final analysis. All included studies were, single-center, retrospective case series of consecutive kidney transplant recipients who developed primary symptomatic lymphocele within a defined time period.
Table 1 shows the outcomes of five interventions have been evaluated, with 20 studies reporting on aspiration (n=218 patients); 14 studies reporting on sclerotherapy (n=155); 18 studies on drain placement (n=219); 23 studies reporting on laparoscopic surgery (n=333); and 18 studies reporting on open surgery (n=188). On average, a total of 20 patients were included in each study.
Quality of Reporting
Overall, the study quality was low, with few studies meeting the checklist for methodological rigor (see Table, SDC 2,http://links.lww.com/TP/A482). Only two studies met all six criteria. Five studies fulfilled five of six criteria; 23 studies met four criteria, whereas the remaining 22 studies fulfilled three or less criteria for methodological rigor.
Overall Incidence of Lymphocele After Kidney Transplantation
Forty-two studies reported incidence of primary symptomatic lymphocele after kidney transplantation. Pooled event rate for incidence of symptomatic lymphocele after kidney transplantation was 5.2% (95% confidence interval [CI]: 4.9–5.6). The lowest and highest reported incidence were 1% and 26%, respectively. Excluding studies that did not provide an explicit definition of the method used to diagnose the posttransplant lymphocele, the pooled event rate was 5% (95% CI: 4.7–5.4) with the cumulative incidence of 5.6% (95% CI: 5.1–6.1). Of the 42 studies providing data for lymphocele incidence, only 31 studies (n=582) provided an explicit definition of symptomatic lymphocele. Furthermore, of the 42 studies providing data for lymphocele incidence, 39 studies (n=756) provided a detailed description of the diagnostic methods used to detect and confirm the presence of lymphocele.
Fifty-two studies (n=1113) provided data about primary treatment modalities used to treat lymphocele. Primary treatment modalities included the following: aspiration (n=218); sclerotherapy (n=155); drain placement (n=219); laparoscopic surgery (n=333); and open surgery (n=188).
Follow-Up Time of Included Studies
The median follow-up time was 28 months (range, 1–51 months) for aspiration therapy; 20 months (range, 3–144 months) for sclerotherapy; 16 months (range, 1–144) for drain placement; 21 months (range, 1–72 months) for laparoscopic surgery; and 28 months (range, 3–53 months) for open surgery.
Twenty studies (n=218) reported rate of recurrent lymphocele formation after aspiration (Fig. 1). Of 218 cases treated with simple aspiration, 141 cases recurred, associated with a recurrence rate of 59% (95% CI: 51–67). The rate of recurrent lymphocele formation after aspiration ranged between 10% and 95%, with only eight studies (n=54) having specified a follow-up period. Six studies (n=85) specified the diagnostic methods used to detect the presence or absence of recurrent lymphocele formation after aspiration.
Fourteen studies (n=155) reported rate of recurrent lymphocele formation after sclerotherapy. Of 155 cases treated with sclerotherapy, 41 cases recurred, associated with an overall recurrence rate of 31% (95% CI: 23–40).
Of the 14 studies that reported outcomes of sclerotherapy, 7 studies (n=68) used povidone-iodine solution; 2 studies reported (n=23) using a combination of human fibrinogen, bovine protease inhibitor, human thrombin, calcium chloride, and gentamycin; 2 studies (n=22) used ethanol solutions; 1 study (n=31) used tetracycline or ethanol without reporting exact numbers; 1 study (n=10) used streptomycin; 1 study (n=1) used tetracycline.
Three studies (n=44) described the total volume of sclerosing agents, varying between 80 and 200 mL of sclerosant instilled after aspiration of symptomatic lymphoceles Eight studies (n=89) reported the frequency of sclerosant injections, varying between thrice daily to once per month. Seven studies (n=79) reported the duration of sclerosing agent being left inside the lymphocele cavity before drainage. The duration varied between 5 minutes and 24 hr across all included studies.
Eighteen studies (n=219) reported the rates of recurrent lymphocele formation after percutaneous drain placement. Of these 18 studies, only 15 studies (n=195) reported outcomes of drain placement. Of these 195 cases, 100 recurred, associated with a recurrence rate of 50% (95% CI: 42–58). Of the 18 studies providing data on the rate of recurrent lymphocele formation, only 11 studies (n=67) specified a follow-up period. Only three studies (n=38) specified the diagnostic methods used to detect the presence or absence of recurrent lymphocele formation after drain placement.
Figure 2 shows the rate of lymphocele recurrence after laparoscopic surgery. Twenty studies (n=322) reported the rate of recurrent lymphocele formation after laparoscopic surgery. Of the 322 cases treated with laparoscopic surgery, 19 recurred, associated with a recurrence rate of 8% (95% CI: 6–12). Of the 20 studies providing data on the rate of recurrent lymphocele formation, only 12 (n=194) studies specified a follow-up period, and 5 studies (n=62) specified the diagnostic methods used to detect the presence or absence of recurrent lymphocele formation after laparoscopic surgery.
Twenty-six cases required conversion to open surgery, with an estimated conversion rate of a conversion rate of 12% (95% CI: 8–16). Indications for conversion were as follows: difficulty accessing lymphocele due to location (n=10); adhesions (n=2); injury to adjacent structure requiring repair (n=2); risk of injury to adjacent structure (n=2); preexisting hernia repair (n=2); and thick wall of lymphocele (n=1). Indication for conversion was not reported in seven cases.
Figure 3 shows the rate of lymphocele recurrence after open surgery. Seventeen studies (n=176) reported rate of recurrent lymphocele formation after open surgery. Of the 176 cases treated with open surgery, 18 recurred, associated with a recurrence rate of 16% (95% CI: 10–24). The rate of recurrent lymphocele formation after aspiration varied between 10% and 95%, with only seven studies (n=84) having specified a follow-up period. Furthermore, seven studies (n=50) described the diagnostic methods used to detect the presence or absence of recurrent lymphocele after open surgery.
Figure 1 also shows the complication rate after aspiration therapy. Three studies with 58 cases reported complications after aspiration. Of the 58 cases, eight developed complications, associated with a complication rate of 16% (95% CI: 9–27). Local infections (n=8) are the most commonly reported complications after aspiration therapy. The rates of local infections varied between 6% and 17%, with only one study (n=7) specifying a follow-up time.
Nine studies (n=72) reported complications associated with sclerotherapy. Among these 72 cases, six reported complications after sclerotherapy. All six cases reported pericatheter infections.
Only two studies (n=6) reported complications associated with drain placement. Of which, two cases with local infections were reported.
Figure 2 also shows the complication rate after laparoscopic surgery. Fifteen studies with 274 cases reported intraoperative complications during laparoscopic surgery. Of the 274 cases, 14 intraoperative complications occurred, associated with an intraoperative complication rate of 8% (95% CI: 5–12).
Intraoperative complications associated with laparoscopic surgery were as follows: bladder injury/accidental cystostomy (n=4); transection of ureter (n=3); bleeding from peritoneal window due to inadequate hemostasis (n=1); inferior epigastric artery injury (n=1); renal capsular hemorrhage (n=1); laryngospasm (n=1); perforation of renal pelvis (n=1); colon perforation (n=1); and an incisional port hernia (n=1). The complication rates after laparoscopic surgery varied between 2% and 20%, with 14 studies (n=193) specifying the surgical techniques by which laparoscopic lymphocele fenestration was conducted.
Ten studies with 163 cases reported postoperative complications after laparoscopic surgery. Of the 163 cases, six developed postoperative complications, associated with a complication rate of 6% (95% CI: 3–10). Postoperative complications associated with laparoscopic surgery were defined as follows: fever of unknown origin (n=2); urinary retention (n=2); postoperative port-site hernia (n=1); and a hydrocele that appeared 2 days after surgery (n=1). The postoperative complication rate associated with laparoscopic surgery varied between 4% and 16%, with seven studies (n=145) specifying a follow-up period, and four studies (n=20) describing methods by which follow-up was conducted.
Figure 3 also shows the complication rate associated with open surgery. Seven studies with 91 cases reported intraoperative complications during open surgery. Of the 91 cases, there were a total of five reported intraoperative complications, associated with an intraoperative complication rate of 8% (95% CI: 4–16). The nature of the intraoperative complications was reported in all but three studies. Intraoperative complications associated with open surgery included the following: transection of ureter (n=1) and insufficient fenestration (n=1).The intraoperative complication rate after open surgery varied between 4% and 13%, with four studies (n=47) detailing the surgical technique by which the open surgery was conducted.
No study provided a detailed description of the methods by which intraoperative complications were detected. Four studies with 41 cases reported postoperative complications after open surgery. Of the 41 cases, 7 developed postoperative complications, associated with a postoperative complication rate of 22% (95% CI: 10–40). Postoperative complications associated with open surgery included the follows: infection (n=3); pneumonitis (n=1); delayed wound closure (n=1); prolonged ileus (n=1); and fever (n=1). The postoperative complicated rate associated with open surgery varied between 7.7% and 50%, with three studies (n=33) providing data on follow-up period, and two studies (n=11) describing the methods by which follow-up was conducted.
Twelve studies (n=274) reported mean hospital stay after laparoscopic surgery. The mean (range) hospital stay after laparoscopic surgery was 2.5 days (1–5). Seven studies (n=23) reported mean hospital stay after open surgery. The mean (range) hospital stay after open surgery was 5.5 days (3.8–8 days).
Our study findings suggest that laparoscopic surgery may be the preferred surgical option for the treatment of primary symptomatic lymphocele after kidney transplantation. Laparoscopic surgery to fenestrate the lymphocele into the peritoneal cavity is associated with a lower overall rate of recurrence of 8%, compared with 16% and 51% for open surgery and aspiration therapy, respectively. Laparoscopic surgery also seems to have the lowest rates of surgical complications, with an overall complication rate of 14% compared with 30% and 16% among those who had open surgery and aspiration therapy. Furthermore, compared with open surgery, the average length of stay associated with laparoscopic surgery is shorter by at least 50% (2.5 days compared with 5.5 days).
With the development of surgical and radiological technologies over the past decades, laparoscopic surgery and percutaneous drainage are becoming the widely used treatment options for lymphoceles occurring after kidney transplantation and are replacing the traditional open surgical procedure. Laparoscopic surgery, however, is not without risks that include the need to convert to open surgery. Our meta-analyses have reported a 12% overall conversion rate from laparoscopic techniques to open surgery. The need for conversion also appears to be associated with the presence of abdominal adhesions and the level of laparoscopic experience of the surgeons involved, but can be minimized if intra- operative ultrasound is used in conjunction with the laparoscopic surgical approach (9). Careful and detailed assessment of all underlying anatomical structures using radiological imaging and placement of an in-dwelling bladder catheter before the surgery should assist in minimizing injuries and complications. Appropriate patient selection is also required. For example, open surgery rather than laparoscopic techniques might be preferable if substantial peritoneal adhesions are anticipated, or the location of the lymphocele is in an awkward position or multi-locular in nature.
The role of aspiration therapy is less clear. The obvious advantage is that it can be performed in a more convenient ambulatory care setting and without need for general anesthesia. However, aspiration therapy is associated with the highest risk of lymphocele recurrence, with over 50% and of all lymphoceles recurring after percutaneous drainage without sclerotherapy. Even with sclerotherapy and drain placement after aspiration therapy, the risk of lymphocele recurrence remained high, reporting up to 80% in some included cases. Given that aspiration therapy is a relatively simple, economical and safe procedure, it may be reasonable to recommend aspiration therapy as the first-line treatment and reserve laparoscopic fenestration for lymphoceles recurring after aspiration. The clinical response to aspiration can also be of diagnostic importance. However, the anecdotal experience of the authors is that large lymphoceles occurring in the initial weeks after kidney transplantation are more likely to recur and may be best managed by early surgical rather than radiological intervention. Furthermore, surgical localization of a lymphocele can be challenging at the best of times, but is particularly so if the size of lymphocele has been reduced by recent aspiration.
To our knowledge, this systematic review is the first comprehensive analysis of all published data regarding the management of symptomatic lymphocele after kidney transplantation, comprising of 52 retrospective case series with 1113 cases of primary lymphocele. Using detailed and novel methodologies in critically appraising all available evidence from published case series and case reports, our systematic review provides an important guide for transplant clinicians managing this important and common complication after kidney transplantation.
There are limitations to this systematic review. First, this is a systematic review of case-series and there is a lack of data on control groups to conduct comparative analyses. Second, the average follow-up time is short, which may have affected the outcomes of study. With longer follow-up time, a higher rate of recurrent lymphoceles may be expected. Third, there is also substantial variability in the follow-up time across all included studies, potentially underestimating the overall incidence of recurrent lymphocele formation and postoperative complications. Fifth, publication bias may occur in studies of lymphocele management, leading to overestimation of the treatment effect because studies with more favorable outcomes are likely to be published than studies with negative outcomes. Previous studies have reported that the instillation of sclerotherapy agent reduces the risk lymphocele recurrences after aspiration therapy, but it is associated with a higher rate of infections (45). Given the limited information and the heterogeneity about the treatment effects of sclerotherapy and drain placement in the included studies, we were unable to account for the differences in lymphocele recurrences rate associated with the various types of sclerotherapy instillations, and the frequency, the duration and the location of drain placement after aspiration therapy.
Subgroup analyses to define the predictors for lymphocele recurrences for each of the treatment modalities were also not feasible. Furthermore, the lack of baseline characteristics among the transplant recipients across all included studies precluded any meaningful subgroup analyses based on the donor source and the types of immunosuppressive regimen.
Findings from our systematic reviews were based solely on data from case series and case reports and highlight the need for prospective comparative studies to assess the safety and the efficacy of the proposed treatment modalities for lymphoceles occurring after kidney transplantation. A prospective randomized controlled trial would be the ideal reference standard to assess the different management options of lymphocele after transplantation, but it is unlikely to occur because of feasibility issues: an adequately powered multi-center randomized controlled trial with sufficient sample size is needed to detect significant differences between interventions, and the ethical dilemma of clinical equipoise associated with the design of any surgical intervention trials. Given the difficulties associated with a prospective randomized controlled surgical trial, decision analytical modeling of cost- effectiveness or cost-utility analysis provides the next best alternative for evaluating both the short- and long-term effectiveness of treatment interventions and should be considered in future studies. In addition, the efficacy and the effectiveness of the various types of aspiration therapy could potentially be explored with a prospective cohort study.
Compared with open surgery and aspiration therapy, laparoscopic surgery seems to be the better overall treatment option for symptomatic lymphoceles occurring after kidney transplantation. Although aspiration therapy is associated with the highest rates of lymphocele recurrence, it is of low risk and can be performed as an ambulatory care procedure and may obviate the need for an operation in the proportion of patients in whom it is successful. The nature of aspiration therapy, however, whether it is by simple aspiration or more prolonged drainage, is unresolved and might be appropriate for prospective cohort study.
MATERIALS AND METHODS
Inclusion and Exclusion Criteria
“Symptomatic” lymphoceles were defined as cases where the lymphatic collection is accompanied by a clinical manifestation of the lymphocele, including an asymptomatic rise in serum creatinine, hydronephrosis, pain or abdominal swelling over graft, ipsilateral leg edema, thrombosis, or changes in micturition.
Inclusion criteria were kidney transplant recipients from deceased or living donor; developed a symptomatic lymphocele requiring treatment; received a specified intervention (aspiration, sclerotherapy, drain placement, laparoscopic surgery, or open surgery); and the outcome of treatment was described. Studies involving lymphoceles that developed after other types of pelvic surgery and single case reports were excluded. Asymptomatic recurrences, defined as radiologically proven lymphatic fluid collections not accompanied by clinical manifestations, were excluded from our analysis. Disagreement about study inclusion was resolved by consensus (between A.L. and G.W.).
A comprehensive literature search was performed for studies documenting the management and outcomes of symptomatic lymphocele after kidney transplantation. Key search terms were the following: “Kidney Transplantation/”; “Lymphocele/”; “lymphocel$.tw.”; “lymphoc?ele$.tw.”; and “lymphatic cyst$.tw.” The search was limited to human studies. The search was not restricted to studies published in English. Using the OvidSP search engine, the following databases were searched: MEDLINE (January 1954 to January 2010), EMBASE (January 1980 to January 2010), and the Cochrane Central Register of Clinical Trials (January 2010). Conference proceedings and abstracts from the Transplant Society and the American Transplant Congress annual meetings were also evaluated. Bibliographies of key articles were manually perused.
Two authors (A.L. and G.W.) independently assessed all titles and abstracts for eligible studies. Data extraction was carried out by the same two reviewers using a standard data extraction form. Extracted data included incidence, treatment, and treatment outcomes of primary symptomatic lymphocele after kidney transplantation. Primary treatment outcome was the rate of lymphocele recurrence. Secondary outcomes included the rate of conversion from laparoscopic to open surgery, the total length of hospital stay, intraoperative (defined as complications occurring during the surgical procedure), and postoperative complication rates (defined as complications occurring after the surgical procedure).
The methodological quality of all included studies was assessed independently by two investigators (A.L. and G.W.). The checklist for methodological rigor included the following domains: the explicitness of the definition of lymphocele to differentiate studies about lymphoceles from those referring to lymphatic leaks; comprehensive description of methods of lymphocele diagnosis, the transplantation techniques, and interventions for lymphocele management. A follow-up time of 6 months or greater was defined a priori as the adequate follow-up time for lymphocele recurrences.
The primary outcome was defined as the rate of recurrent lymphocele formation after treatment. Secondary outcomes included the rate of conversion from laparoscopic to open surgery, the total length of hospital stay in days, the intraoperative and postoperative complication rates. Event rates were calculated for studies that provided data for the estimation of treatment outcomes: recurrence, conversion, and complication rates. Point estimates and the 95% confidence intervals were calculated for each study. Summary estimates of the frequencies for all outcomes were calculated using a random effects model which generated a weighted average mean. All analyses were performed using Comprehensive Meta Analysis version 2.2.055 (Biostat, Englewood, NJ). Given that such summary statistics may obscure heterogeneity among pooled studies, we have displayed results in forest plots to illustrate variability in results across studies. We have also elicited potential sources of variability which have been analyzed descriptively, for example, variation in disease definition, diagnostic technique, and follow-up time among included studies.
The authors thank Gail Higgins, Trials Search Coordinator, Cochrane Renal Group, Centre for Kidney Research, Children's Hospital at Westmead, NSW, Australia.
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