Best Practice & Research Clinical Gastroenterology 28 (2014) 19–27

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The potential benefits and disadvantages of laparoscopic surgery for ulcerative colitis: A review of current evidence Christianne J. Buskens, MD, PhD, Consultant Colorectal Surgeon *, Saloomeh Sahami, MD, PhD, Student, Pieter J. Tanis, MD, PhD, Consultant Colorectal Surgeon, Willem A. Bemelman, MD, Consultant Colorectal Surgeon Department of Surgery, Academic Medical Center, PO Box 22660, 1100 DD Amsterdam, The Netherlands

a b s t r a c t Keywords: Ulcerative colitis Laparoscopy Proctocolectomy Ileal-anal pouch

Up to 35% of patients with ulcerative colitis will require surgery during the course of their disease. Nowadays, a total colectomy with ileal pouch-anal anastomosis is the preferred procedure, which can be performed open or via laparoscopic approach. Since the early ’90s, minimally invasive techniques have gained popularity, but the extend of restorative procedures in these patients has restricted the use of laparoscopic approaches mainly to elective procedures in specialised centres. This review discusses the benefits and disadvantages of laparoscopic surgery when compared to open surgery. It presents the current evidence on short-term and long-term post-operative results, functional outcome, fecundity, and costs, for both elective and emergency indications. In addition, the value of new techniques (including single port surgery) and alternative laparoscopic approaches (e.g. ileo-rectal anastomosis, Kock-pouch and appendectomy) will be discussed. Ó 2013 Elsevier Ltd. All rights reserved.

Introduction Ulcerative colitis (UC) is an inflammatory bowel disease (IBD) affecting the colon, with an increasing incidence and prevalence in the West [1]. The options for medical treatment have expanded in recent years, but surgical management is still required in up to 35% of patients [2,3]. Although any decision on * Corresponding author. Tel.: þ31 20 566 9111; fax: þ31 20 566 9243. E-mail address: [email protected] (C.J. Buskens). 1521-6918/$ – see front matter Ó 2013 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.bpg.2013.11.007

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surgical resection should be preceded by multidisciplinary discussion, both the European Crohn’s and Colitis Organization (ECCO) and American Society of Colon and Rectal Surgeons (ASCRS) issued guidelines establishing indications for surgical treatment [4,5]. In the elective setting, these indications include steroid-dependence, therapy refractory disease, unacceptable medical side-effects and noncompliant patients. Surgical resection of the colon is also warranted when there is (suspicion of) malignant degeneration. A total colectomy with ileal pouch-anal anastomosis (IPAA, also known as ‘restorative proctocolectomy’) is described as standard of care in these ECCO and ASCRS guidelines [4,5], although no recommendation is made regarding the preference of the surgical approach. This procedure can be performed by midline incision or (hand-assisted) laparoscopic procedure, as a one- or two-stage procedure, and with or without defunctioning of the ileal-anal anastomosis. In highly selected patients, a single stage procedure can be performed without a diverting stoma [6]. In the acute setting, medication (cyclosporine, anti-TNF, and tacrolimus) has reduced the short-term emergency colectomy rate for toxic mega-colon or uncontrolled haemorrhage from 40% to 70% to approximately 10% in the last decades [3]. Severe acute colitis patients mostly undergo a subtotal colectomy with end ileostomy, so that restorative proctectomy can be performed when patients are in better condition. These procedures can also be performed by laparoscopic approach, but in daily clinical practice open surgery is frequently performed due to the urgent circumstances with ill patients and fragile colons. In addition, in daily clinical practice it is not always possible to have a specialised laparoscopic colorectal surgeon available for these patients. While good quality (audit) studies have been published in the literature demonstrating the advantages of laparoscopy for colorectal cancer [7,8], and ileocoecal resections for Crohn [9], the extend of restorative procedures in UC patients, including rectal and pelvic dissection, has restricted the use of minimally invasive approaches to highly specialised tertiary referral centres. However, patients with UC are, theoretically, ideal candidates for advanced minimally invasive surgery. The benefit of improved cosmetic outcomes and earlier post-operative recuperation is often considered an important outcome parameter in this patient group that is in the prime of their life. Also, the possible long-term advantages in terms of facilitated re-operation and fecundity in women might be especially beneficiary in these young patients. This review discusses the current evidence on the benefits and disadvantages of laparoscopic surgery when compared to open surgery. Literature was identified searching the MEDLINE database using the following search terms: ‘laparoscopy’, ‘inflammatory bowel disease’, ‘ulcerative colitis’, ‘proctocolectomy’, ‘ileal-anal pouch’. Review articles, meta-analyses, and studies performing randomized controlled trials (RCT) were used when available. We will present the short-term and long-term post-operative results, functional outcome, fecundity, and costs for both elective and emergency indications. In addition, the value of new techniques (including single port surgery) and alternative laparoscopic approaches (e.g. ileo-rectal anastomosis, Kock-pouch and appendectomy) will be discussed. Elective setting Short-term outcome Although mortality is rarely reported in IPAA procedures [10], morbidity rates remain relatively high. Especially the incidence of post-operative anastomotic leakage and pelvic sepsis is noteworthy when compared to other colorectal procedures, ranging from 7 to 20% in various studies [11–13]. A systematic review demonstrated that leakage was significantly more frequent in patients without a defunctioning stoma, but pouch-related sepsis was comparable between the two groups [14]. Since these local infectious processes can influence long-term functional pouch results, all efforts should be focussed on reducing these potentially dangerous complications. Several studies have compared the short-term post-operative results of laparoscopic and open approaches for IPAA. Most studies combine hand-assisted and straight laparoscopic techniques in their results, since a meta-analysis did not demonstrated major differences in the outcomes of both techniques [15].

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With respect to the most important short-term outcome parameters, a meta-analysis from the Cochrane foundation including a total of 607 patients, did not demonstrate significant differences in mortality and post-operative complications [9]. Although the operative time was significantly longer in the laparoscopic group with a weighted mean difference of 91 min (95% CI 53–130), the hospital stay of this group was shorter with a weighted mean difference of 2.66 days (95% CI 4.3, 1.0). The two trials evaluating cosmesis found significantly higher cosmetic scores in the laparoscopic group. The authors concluded that laparoscopic IPAA is feasible and safe, but since the short-term advantages of laparoscopy seemed to be limited, the clinical significance of this procedure was suggested to be arguable. The results are summarized in Table 1. The difficulties in interpreting these mediocre results, is that only one of the included trials was an RCT with a total of 60 patients [16], and that most studies included patients that had been operated on early in the learning curve for laparoscopy. For instance, Schmitt et al reported in 1994 considerable fewer complications in the open group [17]. More recent studies show improved laparoscopic results, especially in terms of reduced hospital stay and faster post-operative recovery [18]. The largest, more recent study by Fleming et al, presenting the results from the National Surgical Quality Improvement Program of the American College of Surgeons (676 patients, 339 laparoscopic procedures) even demonstrated that the laparoscopic approach was associated with significantly lower major (OR 0.67; 95% CI 0.45, 0.99) and minor (OR 0.44; 95% CI 0.27, 0.70) complications [19]. Finally, laparoscopy has also been associated with faster progression to restoration of intestinal continuity after defunctioning ileostomy. Fajardo et al demonstrated that the only two significant parameters associated with faster time to closure of loop ileostomy in multivariate analysis were laparoscopic IPAA approach and length of hospital stay (p ¼ 0.004) [18]. Long-term outcome The only RCT comparing laparoscopic and open restorative proctocolectomy presented the longterm outcome results at a median of 2.7 years after surgery [20]. Morbidity, functional outcome, and quality of life were comparable for the two approaches. However, the laparoscopic group had longlasting improved body image and cosmesis scores. Overall, long-term functional pouch results (reported up to 20 years after surgery) seem to be satisfactory with a mean number of bowel movements of six per day (including one during night-time), complete continence in >70% of patients and >80% were able to postpone at least 30 minutes [21,22]. A meta-analysis of 53 observational studies, including 14,966 patients, evaluated the developments in Table 1 Results of various outcome parameters in meta-analyses comparing open to laparoscopic IPAA procedures in elective setting, and subtotal colectomies in acute setting for UC patients.

Elective procedures Mortality Procedure specific complications Severe complications Minor complications Operative time (minutes) Blood loss (ml) Hospital stay (days) Reoperation Acute procedures Mortality Wound infection Intra-abdominal abscess Hospital stay (days) Reoperation Ileus Gastro-intestinal bleeding

Laparoscopic approach

Open approach

0/232 5/164 8/157 48/213

1/323 8/256 20/258 93/306

7/172

16/275

1/402 25/357 3/90

3/516 54/449 12/96

Outcome measure

Effect size (95% CI)

Risk ratio Risk ratio Risk ratio Mean difference Mean difference Mean difference Risk ratio

ns 0.81 (0.3, 2.0) 0.65 (0.3, 1.5) 1.05 (0.8–1.4) 91.5 (53.4, 129.7) 98.6 (261.0, 63.9) 2.66 (4.3, 1.0) 0.74 (0.3–1.7)

Risk ratio Risk difference Risk ratio Mean difference Risk ratio Risk ratio Risk ratio

0.46 (0.07, 3.1) 0.06 (0.09, 0.02) 0.27 (0.08, 0.91) 3$17 (3.98, 2.37) 0.83 (0.51, 1.34) 0.83 (0.43, 1.61 1.03 (0.3, 4.3)

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functional outcome over time [23]. Functional outcome was independent of the surgical approach. In this study the overall pouch failure rate was 4.7% in a sensitivity analysis including only studies with minimal follow-up of 5 years. Although pouch failure could not be related to any surgical technique, a significantly lower incidence was found in more recent studies versus those published prior to 2000. Other studies analysing predictive parameters of pouch failure also never identified the surgical approach as a prognostic factor [24,25]. Pouch failure was demonstrated to be related to completion proctectomy, Crohn’s disease, handsewn anastomosis, and diabetes [25]. Incisional hernias and adhesion related small bowel obstruction are other long-term outcome parameters that were previously demonstrated to be reduced in laparoscopic colorectal surgery [7]. Unfortunately, these outcome results are difficult to compare for IPAA surgery since only a few small observational studies with indirect results have been published. One prospective cohort study showed less adhesiolysis (6 vs. 47%, p < 0.001) and hernia repair (0 vs. 14%, p ¼ 0.024) during completion proctectomy after laparoscopic emergency colectomy in one hundred consecutive patients [26]. Although overall morbidity and post-operative hospital stay were not related to the surgical approach, the interval to completion proctectomy was also longer after open colectomy. Another interesting study by Hull et al, presented the incisional and total abdominal adhesion score, determined during a diagnostic laparoscopy performed at time of ileostomy closure in 40 patients (28 patients after laparoscopic resection). Both the incisional and total abdominal adhesion score were significantly lower in the laparoscopic IPAA group when compared to open procedures: 0 versus 4 (p ¼ 0.004) and 2 versus 8 (p ¼ 0.002) respectively [27]. However, one should keep in mind that these studies reporting on adhesion formation could be confounded if patients receive a temporary ileostomy. Reports are emerging that adhesions predominantly occur at the previous ileostomy-site, independent of the original surgical approach. Hiranyakas et al demonstrated that the overall post-operative complication rate after loop ileostomy closure was significantly lower in the laparoscopic group when compared to open surgery, whereas there was no significant difference in the incidence of post-operative ileus in both groups [28]. Sexual dysfunction and fecundity In men, IPAA has been reported to be associated with erectile dysfunction and/or retrograde ejaculation in 2–3% of patients [29]. None of the trials in the Cochrane meta-analysis identified a significant difference between the open and laparoscopic approach regarding this outcome [9]. More recent studies demonstrate that if the rectal dissection is carried out close to the rectal wall, this complication can be avoided [30]. In women, IPAA increases the incidence of dyspareunia or sexual dysfunction in up to 40% of patients [30], and it has been associated with a significant drop in the probability of becoming pregnant [31]. Three meta-analyses on post-operative fecundity demonstrated infertility rates of 26–63% [31–33]. Most studies reported their results after open IPAA, with higher rates of intra-abdominal adhesion which can lead to post-operative tubular infertility. Indeed, a recent cross-sectional study carried out in three university hospitals in The Netherlands and Belgium showed a higher pregnancy rate in 179 females after laparoscopic IPAA. Kaplan–Meier survival analyses demonstrated a decreased time to first spontaneous pregnancy (Fig. 1, log-rank p ¼ 0.023), and an increase in pregnancy rates for the laparoscopic group (log-rank p ¼ 0.033) [34]. Acute setting Severe acute colitis (SAC) is one of the few emergencies in gastroenterology. The mortality rate from SAC dropped from over 70% in 1933 to around 1% [35]. Both ECCO and ASCRS guidelines define SAC using the Truelove and Witts criteria [4,5]. Diagnosis is based on a combination of six or more bloody stools per day with at least one of the following criteria: fever (>37.8  C), tachycardia (>90 bpm), anaemia (30 mg/l). Indications for surgery include all patients with SAC who have surgical complications (perforation, massive haemorrhage, toxic megacolon), as well as therapy refractory SAC. In case of SAC, the patient is often far more ill compared to the patient undergoing colectomy in an elective setting. Most patients are exhausted due to prolonged medical treatment, malnutrition, sepsis, and rectal blood loss, which make the patient more susceptible for post-operative morbidity.

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Fig. 1. Kaplan–Meier estimates of time to spontaneous pregnancy. Reproduced with Permission from Bartels et al, Ann. Surg. 2012; 256:1045–1048.

In a recent systematic review comparing short-term outcomes for laparoscopic and open emergency subtotal colectomy in patients with SAC, a favourable effect of laparoscopy was observed on the risk of wound infections (pooled risk ratio 0.60; 95% CI 0.38, 0.95), and the development of intraabdominal abscesses (pooled risk ratio 0.27; 95% CI 0.08, 0.91) [36]. In 966 patients from six cohorts and three case-matched series, a three day shorter hospital stay was observed after laparoscopic subtotal colectomy (p < 0.001). No differences in number of reoperations, ileus, gastrointestinal bleed or mortality were observed for open or laparoscopic acute colectomy (Table 1). Therefore, laparoscopic subtotal colectomy can be regarded as safe and has important short-term benefits over the open procedure in patients with SAC, although one should be aware that there are no studies addressing the laparoscopic approach in patients with perforating disease. Costs Although a laparoscopic procedure itself is always more expensive than an open procedure, studies in colorectal cancer and Crohn’s disease have demonstrated that overall costs favour a laparoscopic approach due reduced post-operative morbidity and shorter recovery time [7,9]. Studies comparing costs for laparopscopic and open IPAA are scarce. The only study that directly compared operative costs for pouch patients is the previously mentioned RCT [16]. Pre-operative costs were not taken into account. The median costs for a laparoscopic procedures (i.e. material and use of an operating theatre with personnel) were V3.387 versus V1.721 for open surgery (p < 0.001). However, median overall costs including relaparotomies, hospital stay, and readmission costs (stoma closure) were comparable for both groups (V16.728 and V13.405 respectively, p ¼ 0.1). These results are in line with a more recent study from Liu et al, comparing hand-assisted laparoscopic and open subtotal colectomy. No significant differences in costs between both methods were found (US $5593 versus $5638, p ¼ 0.3) [37]. For laparoscopy, concerns have been raised that the procedure could be associated with initially increased costs during the (relatively long) learning curve period due to prolonged operating time, increased conversions and complications. However, one study specifically dedicated to analyse this hypothesis could not substantiate these concerns for laparoscopic colectomy [38]. Alternative laparoscopic approaches New techniques Single-incision laparoscopic surgery (SILS) for IPAA as an alternative to the traditional laparoscopic technique has first been reported in 2010 [39]. SILS is expected to have benefits in the early postoperative course with respect to enhanced recovery, length of hospital stay and cosmesis. So far, the literature is limited to a few case-series demonstrating the feasibility and safety of both two- and threestage procedures with complication rates comparable to conventional laparoscopy [40,41]. Additional studies are needed to compare SILS with respect to operative times, convalescence, and (functional) outcomes.

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Robotic surgery has also been introduced as a promising technique, especially in technically demanding operations like IPAA [42]. However, so far all studies demonstrate increased operative time and cost, with no difference in post-operative complications and length of hospital stay when compared to standard laparoscopic colonic surgery [43]. Therefore, no recommendation with respect tot his technique can be made. Alternative surgical procedures Before the introduction of IPAA in 1980, a proctocolectomy with end-ileostomy or colectomy with ileal-rectal anastomosis was the preferred choice for UC patients. Nowadays, some centres have reintroduced the latter technique for a selected group of patients (e.g colorectal cancer in UC patients without active inflammation or young patients with relatively spared and distensible rectum) [44]. So far there is only limited data available to support this surgical approach. It is a less complex procedure than IPAA with lower morbidity rates, but the functional results and quality of life between the IPAA and the ileo-rectal group were comparable in a recent study from the Cleveland Clinics [45]. In addition, it should be bared in mind that an ileo-rectal anastomosis is not a definitive operation for many UC patients, and that life-long follow-up of the retained rectal stump is required [46]. With respect to either open or laparoscopic approach, the preferred technique should be a laparoscopic resection, as there is good level I and II evidence demonstrating the benefits of this procedure (Table 1). Another surgical approach for patients with UC that was popular before the introduction of IPAA is the continent ileostomy (or Kock pouch). This procedure reached its height of popularity in the late 1960s and early 1970s, but has been replaced as first choice due to the decreased morbidity rate and higher patient satisfaction in IPAA. However, it might be considered in patients in whom restorative proctocolectomy failed or when construction of an IPAA is not possible (e.g. when the small intestine is not long enough to reach the pelvic floor or if anal sphincter function is inadequate) [47]. No study analysing the preferred surgical approach is available. Finally, a novel surgical approach for UC patients is the laparoscopic appendectomy. Several studies report beneficial results linking prior appendectomy inversely with subsequent risk of the development of ulcerative colitis [48]. A recent Australian study reported impressive results in a prospective case series of 30 UC patients. After appendicectomy, 90% of the patients showed a significantly improved clinical activity index score (SSCAI score), and 40% had complete resolution of their symptoms (SSCAI score of 0), such that no further pharmacologic treatment was required [49]. Although there is no discussion whether this procedure should be performed laparoscopically (especially since the effect of this procedure on the inflammatory process is still unclear and patients are at risk for reintervention), the indication for this procedure is still unclear. A systematic review analysing the effect of appendectomy on the disease course of UC patients showed conflicting data. In six observational studies (five case–control studies and one cohort study) with a total of 2532 patients [50], three studies found a beneficiary effect (either lower relapse rate, reduced requirement for immunosuppression or lower colectomy rates). However, two studies found no differences in the requirement for immunosuppression, and one study actually found higher colectomy rates in appendectomised patients. At the moment, a randomized controlled trial is being performed which will hopefully answer the intriguing questions about the role of appendectomy in UC patients. Conclusions Laparoscopy can be regarded as one of the major technical advances in colorectal surgery over the past 20 years. Obviously, one should be aware that laparoscopic proctocolectomy and IPAA are complex procedures with long learning curves. Although no study has specifically focused on this topic in UC setting, a meta-analysis including 5000 laparoscopic procedures indicated that optimal operating time, intra-operative blood loss, and length of hospital stay are achieved after 100 cases and that optimal conversion and complication rates are achieved after 150 cases [51]. Despite these drawbacks, and the initial higher costs of laparoscopy, this review demonstrated that there is numerous level I and II evidence emphasising the important short-term advantages (postoperative recovery and hospital stay) and long-term benefits (adhesions and incisional hernia’s) of this

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approach over open procedures. Although there is no meta-analysis demonstrating a beneficiary effect on the most important post-operative complications, this is probably due to the majority of reports published in the early laparoscopic days. Nowadays, there is increasing solid data from audit studies suggesting that laparoscopic surgery is also associated with lower risks of mortality and morbidity [19], adding to the conclusion that laparoscopy should become the standard of care for UC patients. Perhaps the time is right to identify selection criteria for open surgery, rather than identifying good candidates for laparoscopy?

Practice points  IPAA is the preferred surgical procedure for UC patients  Advantages and disadvantages for laparoscopy in elective setting: ^ increased operative time ^ reduced post-operative morbidity ^ shorter length of hospital stay ^ increased fecundity ^ comparable functional results  Advantages and disadvantages for laparoscopy in acute setting ^ decreased wound infections and intra-abdominal abscesses ^ shorter length of hospital stay ^ comparable incidence of ileus and gastro-intestinal bleeding

Research agenda  The long-term advantages of laparoscopic IPAA need to be determined  The role of laparoscopic appendectomy in UC patients needs to be analysed  It should be considered to state a preference for laparoscopic surgical approach in the ECCO and ASCRS guidelines

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The potential benefits and disadvantages of laparoscopic surgery for ulcerative colitis: A review of current evidence.

Up to 35% of patients with ulcerative colitis will require surgery during the course of their disease. Nowadays, a total colectomy with ileal pouch-an...
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