Abstract
Introduction
The clinical significance of Type II endoleak remains contentious; the strategies used for its management have continued to expand. We systematically review the literature and comprehensively appraise the effectiveness of laparoscopic intervention in the management of this common complication.
Methods
A systematic search was performed in accordance to the Preferred Reporting Items for Systematic Reviews and Meta-Analysis (PRISMA) guidelines on MEDLINE, EMBASE and Cochrane Library for relevant articles reporting laparoscopic surgery of Type II endoleak post-endovascular aortic repair.
Results
Thirteen studies representing 40 patients were investigated. Mean age was 72.7 years, and proportion of males was 90.0%. All patients were American Society of Anesthesiologists grade II and above and underwent standard infrarenal endovascular aneurysm repair. The mean duration of operation was 130.2 min, with a mean blood loss across of 173.8 mL. The overall technical success rate was 90% (27/30). Two patients required reoperation within 24 h, with further lumbar ligations that were successful. One other patient required conversion to open surgery due to significant bleeding at the dorsal aorta. The perioperative and 30-day mortality rate was 2.5% (1/40). The mean length of hospital stay was 3.7 days (range 1 to 10 days). The mean length of follow-up was 36.7 months (range 3 to 103.2 months), where the rate of recurrence was 22.5% (9/40).
Conclusions
Laparoscopic ligation of feeding vessels causing Type II endoleak is potentially an alternative treatment after failed standard endovascular embolization, particularly in select centres with necessary resources and capabilities.
Introduction
Randomised control trials have demonstrated that endovascular repair reduces aneurysm-related death within the short and medium term.1,2 Despite this, concern remains about the long-term durability of endovascular stent grafts and life-long surveillance is now universally recommended.3–7 Re-intervention rates are 11.5% higher in EVAR vs. conventional open repair, and this is mostly accounted for by the development of endoleak. 8 White et al. first proposed the term ‘endoleak’ in 1996 9 describing ‘incomplete aneurysm exclusion by an endoluminal graft’. In 1998, further refinements to the definitions with endoleak classes I–IV followed.10,11
Type II endoleak is characterised by retrograde flow of blood from collateral arteries, (Figure 1) which may over time cause aneurysm sac growth 4 and rupture.7,12 This type of endoleak is common, complicating between 10 and 25% of EVARs.8,13–15 Although the clinical significance of Type II remains contentious,4,12,14,16 Sidloff et al. recently reported that patients with Type II endoleak were not associated with aneurysm-related mortality; instead, patients with Type II endoleaks had improved survival rates as compared to patients without endoleak complications. 17 Hitherto, the type of treatment modality remains controversial. 16 Endovascular coiling and embolization have traditionally been used as first line interventions, but it is increasingly recognised that this method carries the risk of coil migration and recanalization. 18 Studies have shown that endovascular techniques fail to achieve long-term success in 60–80% of cases.13,18

PRISMA flow diagram of search strategy (last date of search: 27 August 2017). PRISMA: Preferred Reporting Items for Systematic Reviews and Meta-Analysis.
Laparoscopic surgery to ligate aneurysm side branches are used as definitive treatment and this has previously been described in certain specialized centres that are well equipped enough to carry out such a procedure.19,20 Such a technique may be useful as an alternative option in failed endovascular interventions and in patients with chronic renal failure where contrast agent is contraindicated; it also minimises radiation exposure. We aim to assess the impact of laparoscopic surgical repair of Type II endoleaks assembling real-world evidence.
Methods
Literature search
The review methodology was followed according to the PRISMA checklist for systematic reviews as outlined in the PRISMA statement. 21
Medline (via PubMed), Embase, and Cochrane databases searches were performed to identify all case reports of laparoscopic repair of Type II endoleaks. A repetitive and exhaustive combination of the following ‘MeSH’ search terms was used: ‘laparoscopy’, ‘ligation’ and ‘endoleak’.
The ‘related articles’ function was utilised to broaden the search, and all abstracts, studies and citations were scanned and reviewed. Based on the title and abstract of the publication, we searched for cases in which a laparoscopic approach was taken to repair a Type II endoleak. References of the articles acquired were also searched manually. No date or language restrictions were made. The last date for this search was 27 August 2017 (can be obtained on request).
Inclusion criteria for review
We included any English article that reported the use of laparoscopic surgery to perform an intervention for the correction of a Type II endoleak post-EVAR. Additionally, laparoscopic repairs of Type II endoleaks were only included if they were post-infra-renal EVAR.
Exclusion criteria for review
Patients who suffered from other types of endoleaks were excluded. Studies that utilised laparoscopic surgery to prevent the development of Type II endoleaks were also excluded.
Study selection
Two reviewers independently screened and assessed the studies for inclusion. The studies were first screened by their titles and abstracts. We then retrieved the full-text articles for review if we could not confirm the relevance of the studies for inclusion. Conflicts were resolved by consensus, or by appeal to a third author. The study authors were contacted for clarification if necessary.
Data extraction and validation of studies
By utilizing a standardized data extraction sheet, two reviewers independently extracted the following data from each study: first author, year of publication, type of publication, age of patient, sex of patient, comorbidities, aneurysm size, size of endoleak, vessel causing endoleak, previous interventions and surgery performed. Data were extracted on the technical details of the operation including: duration of operation, laparoscopic technique, size and number of trocars, blood transfusion amount. Data were also retrieved on the following outcomes of interest: technical success rate, postoperative complications, duration of follow-up, 30-day mortality, length of hospital stay and need for re-intervention.
Data synthesis
The extracted data were then synthesised and pooled. The heterogeneity of data coupled with the overall low level of evidence precludes any meaningful meta-analytic tests. Descriptive data will be presented since there are no comparative studies.
Results
Systematic search strategy
The systematic search revealed a total of 160 publications for possible inclusion, of which 13 publications met our inclusion criteria to review them their entirety; two were excluded based upon the full text leaving 11 publications remaining. One additional publication was added having manually reviewed the reference lists of the 11 publications. Data extraction was performed on these 13 remaining papers. This included three retrospective analyses,22–24 nine case reports and series,19,20,25–32 and one technical case report. 33 This search strategy is shown in Figure 1 and is based on the PRISMA flow diagram systematic reviews. 21
Baseline characteristics
Between 2003 and 2017, there have been 40 documented cases in the literature of laparoscopic intervention for Type II endoleak (Table 1). Of those reported, the population is predominantly male (90.0%; 27/30) with an average age of 72.7 years (range 44 to 84 years). The mean abdominal aortic aneurysm (AAA) diameter prior to laparoscopic surgery was 61.6 mm (range 50.0 to 93.0 mm). Patients had a variety of comorbidities and all were American Society of Anesthesiologists (ASA) grade II or above. Demographic and comorbidities are displayed in Table 1. In 19 patients (47.5%), the inferior mesenteric artery (IMA) was the only vessel causing the endoleak; 8 (20%) patients had endoleaks caused by only by the lumbar arteries; 8 (20%) patients had endoleaks caused by both the lumbar and inferior mesenteric arteries, 1 (3%) patient’s endoleak occurred in both the middle sacral artery and inferior mesenteric artery 30 and for 1 (3%) occurred in both the internal iliac artery and inferior mesenteric artery. 31 The source of endoleak was not reported in three patients (9%). Notably, 65% of all indications for treating Type II endoleaks were due to sac enlargement, whilst 35% of cases were indicated as a result of failed endovascular techniques involving percutaneous coil embolization.
Baseline characteristics and comorbidities.
AF: atrial fibrillation; AAA: abdominal aortic aneurysm; CAD: coronary artery disease; CABG: coronary artery bypass graft; CTA: computed tomographic angiography; CE: coil embolization; COPD: shronic obstructive pulmonary disease; CT: computer tomographic scan; DM: diabetes mellitus; RF: renal failure; HL: hyperlipidemia; HT: hypertension; IMA: inferior mesenteric artery; LA: lumbar artery; MSA: median sacral artery; PTI: percutaneous thrombin injection; TA: transabdominal.
Procedural technique and 30-day outcomes
All procedures were completed under general anaesthetic with a variety of surgical techniques employed. Twenty-six cases adopted a fully transperitoneal approach using >3 abdominal trochars to achieve triangulation.19,20,23,24,26,28,31,33 Sac fenestration is described by Touma et al. in their paper with diagrams and pictures
33
and is a novel approach unique to their centre. They clipped off all aortic collaterals, followed by employing laparoscopic scissors to incise the sac and the thrombus was removed thereafter. Laparoscopic stitching was performed to close the sac. You can say that their method is well described in their paper which is a technical tip: The last step consists in sac fenestration and thrombus extraction. Before sac incision, a laparoscopic clamp (Storz-France SA, Paris, France) can be positioned at the level of the proximal aortic neck to prevent bleeding from occult type I or III endoleak. Large sac fenestration is performed using laparoscopic scissors, and thrombus is removed. We verify the absence of residual backbleeding. The sac is closed using 3–0 polypropylene interrupted sutures to cover the stent graft. A retroperitoneal suction drain is inserted, and the patient is returned to the supine position.
33
Technical details and perioperative outcomes.
RP: retroperitoneal; IMA: inferior mesenteric artery; TA: transabdominal; LA: lumbar arteries.
The mean duration of operation was 130.2 min (range 50 to 249 min). The mean blood loss across 16 cases was 173.8 mL (range 50 to 800 mL).29–31,33 Technical success was determined postoperatively by either computed tomographic angiography (CTA) or duplex ultrasound (Table 3). The success rate was 90% (27/30). Two patients required reoperation within 24 h, with further lumbar ligations that were successful.19,25 One other patient required conversion to open surgery due to significant bleeding at the dorsal aorta. However, a tear occurred in the vena cava during the conversion, disrupting hemostasis that could not be salvaged due to religious reasons. 30 The perioperative and 30-day mortality rate was 2.5% (1/40). The mean length of hospital stay was 3.7 days (range 1 to 10 days).
Postoperative outcomes and follow-up.
CTA: coronary tomographic angiography; DSA: digital subtraction angiography; LA: lumbar arteries.
Follow-up outcomes
The mean length of follow-up was 36.7 months (range 3 to 103.2 months) and included re-imaging for persistent endoleak and clinical assessment. On follow-up, the rate of recurrence was 22.5% (9/40), all of which required reintervention. In particular, there were four cases of persistent Type II endoleak resulting in sac growth, of which two required conversion to open surgery; 22 one required iliac extension of graft; 22 and one required coil embolization. 30 Three patients suffered from Type I endoleak of which one was accompanied by another Type II endoleak. 30 As a result, one required proximal fenestrated cuff replacement; one required reoperation with ligation of two lumbar arteries; and one required iliac extension of graft placement. 30 Two patients suffered from Type III endoleak, of which one required uni-iliac endograft placement followed by femoral-femoral crossover 30 and the other required endovascular repair. 29 As evident from above, outcome was largely dependent on the nature of the surgical procedure as demonstrated in Table 4. Involvement of a retroperitoneal approach carried a higher risk of complications (87.5%), and re-interventions (62.5%), compared to a fully transabdominal laparoscopic approach (3.8% for both complications and re-interventions). Double IMA ligation was also a safe and successful treatment option and may afford patients permanent resolution of Type II endoleak.
Laparoscopic failure and re-intervention rates stratified according to technical approach.
Discussion
Endovascular repair of infra-renal aortic aneurysms has been proven to reduce 30-day mortality compared with open repair by as much as 70%.34,35 This early benefit is maintained for up to two years 36 after which there is a relative equalization of mortality owing to the accumulation of EVAR-related complications37–39 of which endoleak accounts for the majority. 40 As a result, it has been in the interests of the surgical community to characterise the natural history of endoleaks and their need for intervention. Given the frequency of Type II endoleak following EVAR (10–25%), its management has posed ongoing problems for interventionalists, vascular and general surgeons alike. Furthermore, whereas Type I and Type III endoleaks are widely accepted as a harbinger of impending aneurysm rupture, 41 opinion regarding the fate of the aneurysm sac exposed to Type II endoleak varies considerably. Hitherto, whilst some advocate for early intervention, many feel that Type II endoleak represents a negligible risk to the patient. Sidloff et al. 17 reported that only 0.9 of patients with Type II endoleak suffer from ruptured aneurysms. In addition, more than 33.3% of ruptured aneurysms after EVAR occurred without sac expansion. 17 Contrariwise, Jones et al. 42 argued that persistent Type II endoleak is associated with unfavourable outcomes, including aneurysmal sac growth, reintervention, conversion to open repair and rupture. Recent consensus and systematic review however conclude that conservative management with close radiological surveillance should be utilised first-line, with treatment reserved for cases where sac growth exceeds 5 mm over a six-month period or 10 mm when compared with pre-EVAR diameter. 4 Within our systematic review, a significant proportion (73%) had documented evidence directly complying with these recommendations for intervention; the remaining were not reported (27%). With regards to indication for the laparoscopic approach, our review has also showed that 35% of indications for treating Type II endoleaks was due to previous failed endovascular interventions, hence warranting the need for alternative treatments such as laparoscopy. Given the absence of large prospective series or randomised trials in patients with Type II endoleak, great emphasis still remains on both patient and clinician preference in determining expectant vs. surgical or endovascular management. 16
A spectrum of techniques is currently utilised in an attempt to control Type II endoleak. Translumbar and transcaval embolization are alternative treatments with high success rates (72–81 and 62.5–78%, respectively) and low complication rates (3.2 and 0%, respectively).17,43,44 Secondary conversion to an open procedure remains a valid consideration but does carry a significant complication rate and an average 30-day mortality reported by several studies to be as high as 10%,45 12.4%, 46 21%, 47 and 23%. 48 Moreover, Ultee et al. showed that conversion surgery was associated with an increased occurrence of any complication (OR = 1.5, 95% CI: 1.2–1.9). 45 New onset of Type I and Type III endoleaks may occur, as evident in our findings. We propound this to be plausibly due to the creation of pneumoperitoneum, peri-aortic dissection and the application of laparoscopic clips, all of which may alter the aortic anatomy in an unforeseen way, hence affecting the endovascular sealing zones. Whilst we have no evidence for this, it is an area worthy of investigation for future research particularly for those centres that employ these laparoscopic techniques in greater numbers.
As a result, far less invasive options have emerged as viable alternatives and include endovascular coiling, glue embolization of feeding vessels, sac embolization, graft explantation and increasingly laparoscopic arterial ligation. 40 Of these approaches, transarterial endovascular coiling is the most widely employed. Despite early data suggesting that this approach was robust in controlling Type II endoleak, more recent evidence has been less favourable with a majority of patients at five years continuing to experience persistent sac growth requiring a secondary procedure. 40 These outcomes are likely due to a combination of the high level of technical skill required to manipulate microcatheters and the intrinsic capability of feeding arteries to re-canalise over time. 18 Endovascular interventions have also been shown to carry their own unique set of complications including colonic 49 and spinal cord ischaemia. 50 In the light of this, fully laparoscopic approaches have continued to evolve in an attempt to provide both safe and definitive treatment. Nonetheless, we concede that such an intervention has not gained acceptance as a therapeutic option, perhaps due to the small pool of vascular surgeons trained to perform such a procedure; this warrants the need for collaboration with a general surgeon.
Laparoscopic ligation aims to discontinue blood entering the aneurysm sac through feeding arteries which have reversed their flow post-endovascular repair. This serves to reduce intra-aneurysmal pressure 51 and thus the subsequent risk of rupture. As with embolization techniques, there is a great emphasis on reliably identifying endoleak and the feeding vessel(s) responsible. Triple-phase-computed tomographic (CT) angiography plays a pivotal role in EVAR surveillance and can clearly demonstrate endoleak by revealing contrast outside the stent graft. Determining the type of endoleak however requires dynamic investigation which is afforded by the use of digital subtraction angiography (DSA), contrast enhanced (CE) ultrasonography or time-resolved CT or magnetic resonance imaging. In our review, 73% of cases of TYPE II endoleak were identified using angiography, and most of these specifically described cannulation of the superior mesenteric artery to observe the passage of contrast into the aneurysm sac via the marginal artery of Drummond and subsequently a patent IMA. Lin et al. and Voute et al. 22 both describe CT angiography as their method of identifying Type II endoleak. Presumably they utilised ‘time-resolved’ imaging techniques, which are fast increasing in popularity owing to their high diagnostic performance. 52 Although the main advantage that laparoscopic management confers is the reduction of radiation exposure, angiography is evidently still widely practised from our systematic review. However, this pales in comparison to wholly endovascular procedures, where radiation exposure occurs during preoperative planning, graft placement and follow-up checks. For instance, radiation exposure has been reported to be as long as 44 min in aneurysm sac embolization procedures, 53 and the impact of radiation exposure associated with endovascular aneurysm repairs may be harmful given well-recognised carcinogenic risks.54,55 In this light, vascular surgeons should strive to practise the judicious use of CT-scans and if possible to maintain the lowest dose possible reasonably. 56
The case series presented in this review appears to demonstrate encouraging results on laparoscopic intervention as a technique for Type II endoleak repair in those where endovascular management has failed. As none of the patients in this review had previous open abdominal operations, we could not comment on the efficacy of laparoscopic approaches in such circumstances, where adhesions and scar tissues predominate.
Our units take a multi-disciplinary approach to such cases. Our indications to employ a laparoscopic ligation are when there is a radiological evidence of a persistent Type II endoleak with continued aneurysm sac pressurisation (as evidenced by an increasing sac size), where endovascular embolization has either failed or is impossible.
It is quintessential to acknowledge that the occurrence of Type II endoleak post-EVAR may actually be predictable and preventable. 57 Multiple reports58,59 have emerged supporting the use of protective preoperative IMA embolization to reduce the risk of Type II endoleak occurrence. A retrospective analysis by Kray et al. 59 showed that a preoperatively patent IMA was associated with heightened risk of Type II endoleak formation and inferior AAA sac regression. This was echoed in a recent publication by Manunga et al., 58 who reported a protective effect of preoperative embolization of the IMA on the occurrence of Type II endoleaks, after which secondary interventions may potentially result in rapid regression of aneurysm sac.
Given the well-understood association between anti-coagulation medication and aneurysm rupture,60,61 an attempt was made to investigate the association between the use of anti-coagulation and anti-platelet medications and endoleak persistence; however, only one study (case report) reported the use of long-term anticoagulation; 25 hence, no meaningful statistical analysis could be performed. Although this may theoretically result in endoleak persistence, it was not evident in the patient reported by Wisselink et al. 25 Hence, this relationship cannot be commented on. Nonetheless, the use of anti-coagulation therapy would blunt the chances of spontaneous thrombosis, warranting the need for surgical or endovascular intervention.
Limitation
Chief of limitations is the overall low quality of evidence, because it was a collection of case reports, case series and retrospective analyses. Moreover, as laparoscopic procedures were only performed in selected centres, it limits the external validity of the results. Lastly, we excluded non-English literature, hence missing out on potential relevant studies.
Agreement or disagreement with other reviewers
To date, there has only been one other review by Spanos et al., which analysed a total of eight case studies and one retrospective study. 62 Although we included four more studies, our results are in agreement with theirs on technical success rate and mortality rate, therefore strengthening the evidence regarding the efficacy and safety of laparoscopic approaches for Type II endoleak after EVAR.
Conclusion
Although the laparoscopic approach may be less harmful in terms of radiation exposure as compared to endovascular approaches, current evidence does not support any suggestion of this method as a first-line treatment based on the fact that there is no head-to-head comparison among laparoscopy and other techniques. Nonetheless, in our opinion and without any definitive supporting data, we believe that in unusual circumstances such as pre-existing superior mesenteric or internal iliac artery occlusion, laparoscopic techniques for Type II endoleaks that require treatment may be considered as first-line therapy, as an endovascular path to the potential target vessel is already precluded. We feel a laparoscopic approach is equivalent to a direct aortic sac puncture in terms of invasiveness and complication profile.
However, we strongly believe that in the absence of precluding pre-existing conditions, endovascular techniques should remain first-line wherever possible. These remain arguably less invasive and risky than the creation of even a single laparoscopic port, pneumoperitoneum and the potential associated complications.
Footnotes
What this paper adds
Type II endoleak is characterised by retrograde flow of blood from collateral arteries, which may over time cause aneurysm sac growth and rupture. Although the clinical significance of Type II endoleak remains controversial, there is yet no threshold for intervention has been established and consensus is yet to be reached with regard to the optimum treatment modality. Although endovascular and open methods remain to be the first-line treatment in most centres, laparoscopic approaches have been definitively described to ligate aneurysm side branches and present a potential alternative. The current systematic review provides encouraging evidence on the use of laparoscopic surgery as an alternative treatment for Type II endoleaks, which have undergone failed endovascular interventions.
Ethics approval
Ethics approval for research was not obtained for this review as it involves secondary analyses of previously published datasets, with no direct involvement of human subjects.
Declaration of conflicting interests
The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.
Funding
The author(s) received no financial support for the research, authorship, and/or publication of this article.
