Editorial Open Access
Copyright ©2012 Baishideng Publishing Group Co., Limited. All rights reserved.
World J Gastroenterol. Apr 28, 2012; 18(16): 1861-1870
Published online Apr 28, 2012. doi: 10.3748/wjg.v18.i16.1861
Surgical treatment of ulcerative colitis in the biologic therapy era
Alberto Biondi, Stefano Costa, Albert Troci, Ettore Contessini-Avesani, Emergency and General Surgery Unit, Fondazione IRCCS “Ca’ Granda” Policlinico Maggiore, 20122 Milan, Italy
Marco Zoccali, Alessandro Fichera, Department of Surgery, University of Chicago Medical Center, Chicago, IL 60637, United States
Marco Zoccali, First General Surgery Unit, Department of Surgery, Catholic University, 00168 Rome, Italy
Author contributions: Biondi A, Zoccali M, Costa S, Troci A, Contessini-Avesani E and Fichera A equally participated in the conception, design and drafting of this article; all the authors revised the article critically for important intellectual content and gave final approval of the version to be published.
Correspondence to: Alberto Biondi, MD, Emergency and General Surgery Unit, Fondazione IRCCS “Ca’ Granda” Policlinico Maggiore, Via F Sforza 35, 20122 Milan, Italy. biondi.alberto@tiscali.it
Telephone: +39-2-55033298 Fax: +39-2-55033468
Received: October 8, 2011
Revised: November 25, 2011
Accepted: March 10, 2012
Published online: April 28, 2012

Abstract

Recently introduced in the treatment algorithms and guidelines for the treatment of ulcerative colitis, biological therapy is an effective treatment option for patients with an acute severe flare not responsive to conventional treatments and for patients with steroid dependent disease. The reduction in hospitalization and surgical intervention for patients affected by ulcerative colitis after the introduction of biologic treatment remains to be proven. Furthermore, these agents seem to be associated with increase in cost of treatment and risk for serious postoperative complications. Restorative proctocolectomy with ileal pouch-anal anastomosis is the surgical treatment of choice in ulcerative colitis patients. Surgery is traditionally recommended as salvage therapy when medical management fails, and, despite advances in medical therapy, colectomy rates remain unchanged between 20% and 30%. To overcome the reported increase in postoperative complications in patients on biologic therapies, several surgical strategies have been developed to maintain long-term pouch failure rate around 10%, as previously reported. Surgical staging along with the development of minimally invasive surgery are among the most promising advances in this field.

Key Words: Ulcerative colitis, Inflammatory bowel disease, Infliximab, Surgery, Laparoscopy, Single incision laparoscopy, Total abdominal colectomy, Ileal pouch anal anastomosis, Restorative proctocolectomy



INTRODUCTION

Ulcerative colitis (UC) is a mucosal inflammatory process affecting the rectum and the colon. It is characterized by contiguous inflammation starting in the rectum and progressing for variable distance proximally[1]. Intermittent exacerbations are typical, with symptoms characterized by bloody diarrhea associated with urgency and tenesmus[2]. The activity of disease can range from complete remission to fulminant symptoms along with systemic toxic effects[3].

Although the exact pathogenesis of UC remains poorly understood, the most credited model states that the intestinal flora triggers and drives an aberrant intestinal immune response and subsequent inflammation in a genetically susceptible host[4]. Medical therapy aims at the control of symptoms and the resolution of the underlying inflammatory process, classically by a variety of agents in combination, such as 5-aminosalicylates, corticosteroids, and immunosuppressants, including purine antimetabolites and cyclosporine[5]. Treatment schemes are based on disease severity, (defined as mild, moderate or severe based on clinical ad laboratory parameters) and on the extent of the disease (pancolitis, left-sided colitis, rectosigmoiditis or proctitis)[6]. However, about a quarter of patients with UC end up needing a colectomy because of failure of medical therapy, onset of unacceptable side effects of chronic therapy, occurrence of acute complication of UC (fulminant colitis, severe bleeding, toxic megacolon, perforation), or development of malignancy[7].

For all of these patients, the removal of the colon and rectum represents a definitive cure for their disease, with cessation of symptoms, withdrawal of morbid medical therapy, and avoidance of the risk of developing a malignancy associated with the persistence of inflammation[8].

However, surgery is not without risks and can significantly affect patients’ lifestyle, therefore, is traditionally deemed as a salvage treatment when medical therapy is ineffective[1].

During the last three decades astounding progress has been accomplished both in medical and surgical treatments, which might lead to substantial changes in the traditional principles for the management of UC patients. Medical therapy of UC has recently entered the era of biologic treatments with the approval by Food and Drug Administration (FDA) in 2005 of Infliximab, a monoclonal antibody directed against tumor necrosis factor-alpha. The initial enthusiasm raised by the promise to reduce the colectomy rate in acute presentations, was subsequently partially dampened by conflicting reports regarding Infliximab’s safety and impact on the need for surgery in urgent/emergent setting[9-13].

As the number of available medications increases, more and more often patients are referred for surgery severely malnourished, immunocompromised, and experiencing the side effects of corticosteroids, immunomodulators, and biological agents. Whether they are referred for colectomy in an acute or chronic setting, these patients represent a unique challenge for colorectal surgeons, given the compromised general conditions and poor nutritional status in the former, and the side effects of long term corticosteroid use in the latter[14-16].

Together with the advances in medical therapy, the surgical treatment and techniques in UC has evolved as well. Restorative proctocolectomy with ileal pouch-anal anastomosis (IPAA) is today considered the gold standard and, in experienced hands, can now be performed safely for UC with a low postoperative complication rate and a long-term pouch failure rate reported less than 10%[17-19]. Moreover, the introduction of minimally invasive techniques might further decrease postoperative morbidity and improve patients’ satisfaction, with reduced impact on body image and better cosmesis[20-22].

The purpose of this report is to discuss the recent advances in medical and surgical treatment of UC patients addressing surgical concerns in the era of biologic therapy.

BIOLOGIC THERAPY IN UC: THE GASTROENTEROLOGIST’S VIEW

The primary goals of medical therapy in the treatment of UC are to induce remission of symptoms and maintain it on a long-term basis: by reducing the number of relapses, which occurs in 67% of patients and, at least, once over a 10-year period[23], medical therapy lowers the risk of long-term complications and improves patients’ quality of life.

The majority of UC patients present with moderate-to severe disease (80%) rather than mild disease (20%)[24] and, during their illness, nearly 20% of patients afflicted with UC will experience a severe acute episode that requires hospitalization[25].

Despite the progress accomplished in medical therapy, which broadened the horizon of possible treatments after failure of corticosteroids[26,27], the need for surgery in this patient population seems to be unchanged or slightly decreased over time. Reported colectomy rates are steadily ranging between 20% and 30% in most of the epidemiological studies with additional risk for needing a resection as the extent and severity of the disease increase[8,28-31]. Beside a 10% who have surgery for cancer or pre-neoplastic degeneration, the vast majority of patients need an operation for acute colitis with severe complications not responsive to medical therapy[32,33]. The advantage of prolonged medical therapy vs surgery in patients with acute severe colitis failing initial high dose corticosteroids is still debated. About one third of these patients undergo a colectomy within one year, most likely in an emergency setting, and even if second-line medical therapy may reduce the need for immediate colectomy, most of them will require colectomy by 10 years[32,34]. In this setting, early subtotal colectomy and ileostomy combined with a late reconstructive surgery remains a safe alternative[19] since second-line medical therapy carries with it a not negligible mortality risk[35].

Additionally, about 20% of patients with UC have a persistent active disease often requiring several courses of systemic steroids, but followed by relapse of symptoms during steroid tapering or soon after their discontinuation, a condition known as steroid-dependency. Steroid dependency is associated with serious complications, which, for a significant proportion of patients, become an indication for surgery[36].

Although surgery is curative of the underlying inflammation and restorative proctocolectomy with IPAA preserves the normal anatomic route for defecation, the procedure may lead to new symptoms, such as diarrhea, incontinence, nocturnal leakage, and in some patients does not obviate the need for medication. In several surgical series that follow patients a minimum of 5 years, up to 60% of patients are still having more than 8 bowel movements daily, with 55% of patients experiencing incontinence, and 50% nocturnal leakage[37-39]. Even if surgical techniques have dramatically evolved, surgery is still associated with significant early and late postoperative complications, e.g. anastomotic leak, pelvic sepsis, small bowel obstruction, pouchitis, sexual dysfunction, reduced fecundity in women and pouch failure[40,41]. Repeated surgery is sometimes necessary. A population-based study reported that approximately 20% of patients who had undergone IPAA required at least one additional surgery, and 15% of patients required at least two additional surgeries[42]. Pouch leak and the associated pelvic sepsis rate in large series have been reported to range from 5% to 15%[43]; incidence of late small-bowel resection after IPAA ranges from 12% to 35%. Pouchitis is the most frequent long-term complication of the IPAA[1]. It has been reported in 12% to 50% of patients postoperatively, and some patients (5%-19%) require chronic therapy. Finally, the risk of long-term pouch loss has been reported to range from 1% to 20% in different studies with an overall rate of pouch loss less than 10%, needing diverting ileostomy, pouch excision and end ileostomy, or pouch revision[17-19].

Acute severe ulcerative colitis

According to current treatment algorithms, in case of acute colitis, unless toxic megacolon, perforation or severe bleeding-which are absolute indication for surgery-occur, patients are started on high-dose iv steroids[44]. Response to treatment is assessed by objective measures (e.g., Oxford index or Sweden index) on day 3-4. Two different strategies have been developed in the attempt of avoiding surgery when a first course of steroids fails to control an acute flare. The standard approach in the ‘80s was to prolong the administration of steroids for other 7-10 d, which did not show any reduction in colectomy rates[45-47]. Ten years later, cyclosporine was found to be effective in patients with acute severe UC non responsive to steroids, and has been used as rescue therapy[44,48-51]. In a randomized controlled trial (RCT) 82% of patients on cyclosporine improved, while no patient improved in the placebo group[52]. However, as many as 50% of patients that responded to cyclosporine, required colectomy in subsequent studies with longer follow-up[35,53]. Moreover, the management of patients under cyclosporine can represent a real challenge, given the risk of severe and potentially fatal toxicities, which greatly limit the use of this medication.

Infliximab, an anti-tumor necrosis factor (TNF) antibody, has been approved recently by the United States FDA for the treatment of UC to reduce signs and symptoms, to induce clinical remission and healing of the intestinal mucosa, and to eliminate the use of corticosteroids in patients presenting with moderately-to-severely active UC without adequate response or who are intolerant or have medical contraindications to therapy with corticosteroids or immune modulators[54].

Response to infliximab has been assessed in RCTs with various endpoints such as clinical response, remission and colectomy rates. In patients with severe, steroid-refractory UC, the initial small trials demonstrated modest efficacy after single infusions when early clinical response was determined. The first published trial by Sands et al[55] in 2001 randomized 11 patients with steroid refractory UC to a single infliximab infusion or placebo, and noted a 50% (4/8) clinical response rate with infliximab at a week 2 evaluation. Subsequent studies by Probert et al[56] and Järnerot et al[51] also enrolled patients with steroid-refractory disease. The first study failed to show any significant difference between placebo and 2 infusions of infliximab 5 mg/kg in inducing remission as measured by endoscopy or clinical score. However, Järnerot et al[51] demonstrated in patients with moderate and severe steroid-refractory UC that only 7/24 (29%) patients who received a single infliximab infusion underwent colectomy within 90 d, compared with 14/21 (67%) who received placebo. The superiority of infliximab was only statistically significant in patients with moderate to severe disease, but not in those with more severe disease on the fulminant colitis score, although the study was not powered to detect differences between these two last groups. Even though a later report showed that at 2 years follow-up, the colectomy rate in patients who received infliximab had increased to 46%[57], these studies positioned infliximab as a therapeutic option for patients with steroid-refractory disease. The first controlled trial[58] involving patients who had moderate to severe disease that were neither steroid-dependent nor steroid-refractory, reported superior clinical response rates compared to those seen in steroid-refractory populations. These trials reported high response rates (100% and 83%, respectively), but follow-up was short (9.7 and 3 mo, respectively). The active ulcerative colitis trial (ACT) 1 and ACT 2 trials[59] each randomized 364 patients with moderate to severe UC who were failing conventional therapy (but did not require hospitalization) to either placebo or induction/maintenance infliximab 5 mg/kg or 10 mg/kg. Both in ACT 1 and ACT 2, eligible patients had moderate to severe UC despite concurrent treatment with corticosteroids, alone or in combination with azathioprine or mercaptopurine, but ACT 2 also required that the patient had failed 5-aminosalicylic acid (5-ASA) therapy. In ACT 1, both doses of infliximab (5 mg/kg and 10 mg/kg) resulted in a statistically significant clinical response at week 8 (68.4% and 61.5% respectively, P < 0.01, compared to a placebo response of 37.2%). This was similar in ACT 2, with clinical response at week 8 in 64.5% of patients in the infliximab 5 mg/kg group and 69.2% in the infliximab 10 mg/kg group, compared to a 29.3% response rate in the placebo group (P < 0.001). Clinical remission rates in the infliximab arms at week 8 ranged from 27.5% to 38.8% across both studies compared to placebo-induced remission rates of 14.9% (ACT 1) and 5.7% (ACT 2). Mucosal healing and steroid-free remission rates were also superior in the infliximab arms of these studies. Sandborn et al[60] reported colectomy rates in ACT 1 and ACT 2 patients in a follow-up study. The cumulative colectomy rate at 54 wk was 10% in patients treated with infliximab, compared with 17% in those treated with placebo. These colectomy rates were not unexpected since the enrolled patients had moderate to severe disease, however in 13% of the enrolled patients the colectomy follow-up data was unavailable. The ACT 1 and ACT 2 studies were well-designed, large studies, with comprehensive assessment of clinical and secondary endpoints. They provided important data to support the use of infliximab in patients with moderate to severe UC who have failed other therapies such as steroids, immunomodulators and mesalamine. However, infliximab is not a panacea for all; the proportion of patients who started the study on steroids and were able to come off and remain in remission, was low (20%)[59].

In a recent study by Colombel et al[61], the association between early mucosal healing (defined as Mayo endoscopy subscore at week 8 endoscopy) and clinical outcomes in ACT-1 and ACT-2 patients was investigated. The authors observed that a low week 8 endoscopy subscore was significantly associated with a lower rate of colectomy at 54 wk follow-up (P = 0.0004; placebo P = 0.47) and better outcomes in terms of symptoms and need for steroids at weeks 30 and 54 (P < 0.0001, infliximab; P < 0.01, placebo), especially for those patients who did not achieve clinical remission at week 8[61].

A Cochrane meta-analysis of RCTs concluded that, when compared to placebo, treatment with infliximab is three-fold as effective in inducing clinical remission [relative risk (RR) 3.22; 95% CI: 2.18-4.76] and nearly twice as effective in inducing clinical response (RR: 1.99; 95% CI: 1.65-2.41) or endoscopic remission (RR: 1.88; 95% CI: 1.54-2.28) at week 8 in patients presenting with moderate-to-severe UC refractory to conventional treatment with corticosteroids and/or immune modulators[10].

Steroid dependent ulcerative colitis

Another specific pattern of UC disease is represented by steroid-dependent patients, in whom a response can be obtained with systemic steroids, but the relapse will occur as the dose is tapered or a few weeks or months after discontinuation, making it necessary to increase the dosage again or resume treatment to achieve control of symptoms[36]. As UC patients become dependent-upon or refractory to corticosteroids, the range of action from a medical standpoint become limited and a colectomy becomes a treatment option as the disease is deemed as refractory to medical treatment, or because of the occurrence of complications either related to the disease or associated with side effects of medications[1].

Often, immunomodulator therapies, such as azathioprine or mercaptopurine (6-mercaptopurine) are considered in these patients before surgery as a steroid-sparing treatment. However, the efficacy of azathioprine or mercaptopurine in UC is still debated[62]. Thiopurines are an effective maintenance therapy for patients who require repeated courses of steroids, however the quality of available data is quite poor, as stated in a recent Cochrane review[63]. Currently, the recommendation for using thiopurines in UC is based on the evidence shown by only one RCT of Ardizzone et al[64] which found steroid-free, clinical and endoscopic remission in 53% patients on azathioprine compared with 21% given only 5-ASA [odd ratio (OR) on intention to treat analysis 4.78, 95% CI: 1.57-14.5]. Azathioprine maintenance treatment of UC is beneficial for at least 2 years if patients have achieved remission while taking the drug, but not in those with chronic activity despite the drug[65].

When a steroid-dependent patient fails to benefit from thiopurines or shows intolerance to them, there are very few alternatives to conventional drugs, which lack of current definitive evidence of efficacy. Methotrexate has been tested and, although some uncontrolled studies suggested some benefit with its use[66-68], the only double-blind, placebo-controlled trial, showed no therapeutic benefit[69]. Therefore, current guidelines do not consider methotrexate as an evidence-based therapy in steroid-dependent UC.

After the demonstration of clinical efficacy of infliximab in the treatment of moderate-severe resistant UC, few small series have included steroid dependent patients. Only one study from Italy[70] specifically evaluated steroid dependent UC in an open-label study on 20 patients randomized to infliximab or methylprednisolone. This was the first RCT to implement a regimen of a triple infliximab infusion for induction followed by infusions to maintain remission. Even if this study was statistically underpowered, it demonstrated the benefit of infliximab therapy for responders, who were able to taper and then discontinue steroids during the maintenance phase (9 of 10 patients), as compared with the methylprednisolone group (8 of 10 patients), where responders required continued steroid therapy.

BIOLOGIC THERAPY IN UC: THE SURGEON’S VIEW

Biologic therapy has shown the ability to induce and maintain remission, but, as we stated above, its introduction in the therapeutic algorithm did not substantially affect the overall rate of colectomies, suggesting that it is effective only in delaying but not in avoiding surgery for a subgroup of patients who at some point will require an operation[54,59,60,71]. The clinical efficacy of infliximab in UC still remains unpredictable. Induction therapy is not always effective, and, to date, clinical and/or molecular predictors of response have not been identified. No RCT has been conducted comparing infliximab and cyclosporine in severe UC. Most of the current knowledge comes from the ACT 1 and ACT 2 trials. Those results are in part influenced by the heterogeneity of the sample (including both steroid-dependent and/or immunomodulator-dependent and steroid responsive and/or immunomodulator-responsive patients). More studies are needed to assess the role of concomitant administration of immunosuppressants and infliximab[59]. Furthermore, data on maintenance therapy with infliximab in UC are scant and the benefits of continued maintenance therapy, as well as its long-term safety, are poorly known. The results of the ACT-1 and ACT-2 extension studies conducted on the 229 patients who achieved improvements with infliximab during the trials, showed that the benefits observed in the main studies are basically maintained up to 3 additional years, however an high drop-off rate was observed, due to adverse events (10.5%), lack of efficacy (4.8%), need for surgery (0.4%), or other reasons (14.8%)[72]. Furthermore, it is not clear to what extent postponing surgery by the means of a quite morbid medical therapy represents a safe and effective strategy.

Because of the early onset and chronic nature of inflammatory bowel diseases, patients can be expected to utilize considerable health care resources. Costs analysis are complicated, because they must calculate the impact that such therapies have on the direct costs of health care and the indirect costs for both the patient and their families and the health care system[73]. Surgeries and hospitalizations account for the majority of health care direct costs in inflammatory bowel disease (IBD), and medication costs, on the other hand, accounted for a quarter of total direct medical costs. Moreover, the cost data are right-skewed, with 25% of patients accounting for 80% of total costs[74]. This division of health care costs implies that the most effective cost-containment measure would be the one that reduces the number of hospitalizations and surgeries. With the improved response and remission rates seen with the use of infliximab for induction and maintenance treatment in IBD patients, the clinical benefits may likely translate into economic benefits as well[75]. Surprisingly, many of the cost-effectiveness and utility analyses suggested that infliximab use was associated with rather high incremental cost per quality adjusted year life[73] and the expanding use of infliximab has not significantly impacted the use of surgical procedures for patients with either UC or Crohn’s disease, and rates of nonsurgical hospitalizations have actually increased[76,77]. This belief is supported by the observation that in the United States the hospitalization rates for IBD increased between 1998 and 2004, leading to a concurrent rise in the economic burden, with medical hospitalizations accounting for the largest proportion (58%) of inpatient services costs and biologic agents representing the most costly medications[78,79]. Further pharmaco-economic analyses are needed to accurately assess the impact of infliximab treatment on the costs associated with the treatment of UC.

Surgery in the biologic era: Treatment in evolution

The concept of pushing conservative treatment until surgery is strictly required may be risky, as it has been shown that mortality three years after elective colectomy for UC (3.7%) is significantly lower than that after admission without surgery (13.6%) or when an emergency operation is performed (13.2%)[80]. Moreover, a British study recently reported a significantly higher risk to develop major complications at a 5 year follow up for patients who received a longer course of medical therapy for acute severe UC before surgery, suggesting that the threshold for elective surgery may be too high in current practice[81].

While it’s well known that high-dose systemic corticosteroid therapy (> 40 mg/d prednisolone-equivalent) is a widely recognized risk factor for pouch-related septic complications after restorative surgery[82], whether or not the preoperative administration of infliximab may increase the rates of septic complications is still controversial (Table 1)[9,12,13,83-86]. Nevertheless, the group from the Cleveland Clinic has found a covariate-adjusted risk of early complication for patients treated with infliximab 3.54 times higher, with the rate of sepsis increased by 13.8 folds, despite a significantly higher rate of three-stage procedures in the infliximab group[85]. Similar results have been shown in a paper by Mayo Clinic, where patients treated with infliximab prior to pouch surgery had a significantly higher incidence of anastomotic leaks, pouch specific and infectious complications, with the administration of anti-TNF-alpha as the only factor independently associated with septic complications (OR 3.5)[13]. In another study, a synergic interaction in increasing surgical morbidity was found between infliximab and cyclosporine A when administered together in the preoperative time[12]. These concerns are supported by a recent meta-analysis conducted including 5 studies and 706 patients, which revealed an increased risk of short-term post-operative complications (OR 1.80, 95% CI: 1.12-2.87) associated with preoperative infliximab use, along with a trend towards increased post-operative infection[87].

Table 1 Literature-based comparison of postoperative complication risk associated with preoperative use of infliximab.
Ref.YearNon-IFX/IFX patientsInfectious complicationNon-infectious complication
IFX groupNon-IFX groupOR (95% CI)IFX groupNon-IFX groupOR (95% CI)
Selvasekar et al[13]2007254/4713 (28%)25 (10%)3.50 (1.64-7.5)16 (34%)99 (39%)0.81 (0.4-1.55)
Schluender et al[12]2007134/173 (18%)11 (8%)2.40 (0.6-9.63)3 (18%)26 (19%)0.89 (0.24-3.33)
Kunitake et al[9]2008312/1016 (6%)32 (10%)0.55 (0.22-1.36)11 (11%)17 (5%)2.12 (0.96-4.69)
Mor et al[85]200846/4610 (22%)1 (2%)13.8 (1.82-105)6 (13%)6 (13%)1.00 (0.3-3.37)
Ferrante et al[83]2009119/222 (9%)29 (24%)0.31 (0.07-1.141)NRNRNR
Coquet-Reinier et al[84]201013/13NRNRNR3 (23%)4 (38%)NR
Gainsbury et al[86]201152/295 (17%)14 (27%)1.87 (0.46-7.57)12 (41% )16 (31%)0.59 (0.19-1.87)

Given the concern of increased rate of complications in patients on aggressive medical management, several different surgical approaches have been proposed. First described by Parks and Nichols in 1978, restorative proctocolectomy with IPAA has progressively gained acceptance to become the gold standard in the surgical treatment of UC for the last 25 years[88,89]. The introduction of this technique-most often fashioned as a J pouch created with the terminal ileum and anastomosed to the anal canal-was a real breakthrough, offering a curative treatment to these patients without the need for a permanent stoma, thus preserving their body image, achieving a quality of life comparable to that of the general population[38,90]. However, the procedure is technically demanding and is associated with a significant morbidity rate (around 30%), and an incidence of postoperative pelvic sepsis ranging between 5%-24%[91]. Since it has been shown that the occurrence of a pelvic infection can dramatically affect the functional outcome of the pouch, and considering that long-term steroid use and malnutrition are recognized risk factors for pelvic sepsis, surgical strategies have been developed in order to minimize the occurrence of infectious complications, especially in this subset of patients[92,93]. A total abdominal colectomy with end ileostomy is the operation of choice as first step of a restorative procedure, as it can be performed safely and quickly in the hands of an experienced colorectal surgeon, allowing the patient to overcome the colitis, wean off the medications, and return to an optimal health and nutritional status[94,95]. Moreover, as it is well known that a postoperative diagnosis of indeterminate colitis or Crohn’s disease is not rare after colectomy in these patients[96], a multistep surgical procedure allows for selecting the most appropriate reconstructive surgery on the basis of the pathological findings of the colectomy specimen[19,94,97].

The removal of the rectum and the restoration of the bowel continuity with IPAA are performed as a second step when the patient has fully recovered, and the creation of a temporary ileostomy, although adding the need for one more operation, can further reduce the risk of local sepsis secondary to anastomotic leaks[98,99]. Albeit restorative surgery is not free from long term complications, such as incontinence and soiling (10%-60% of patients, depending on series and entity), pouchitis (about 50% of patients), and sexual dysfunction (20%-25% of cases), with a rate of pouch failure requiring excision ranging between 5%-15%, the majority of these conditions are manageable with medical and physical therapy, which explains the overall satisfaction in patients after IPAA, which exceeds the 90% in most series[40,98,100-105].

Indeed, most recent researches have shown that social and sexual function as well as overall quality of life is significantly improved after restorative surgery, when compared to the period with active UC or diverting ileostomy[106-109].

The application of minimally invasive techniques to the surgical treatment of UC at the beginning of the 1990s contributed in significantly improving the acceptance and tolerability of the procedure[110]. Numerous case series and, finally, two meta-analyses have been published since then, demonstrating the feasibility and safety of the laparoscopic approach, at the cost of longer operative times[110-117]. A subsequent RCT showed that operative time could be significantly reduced with the adoption of a hand-assisted technique, which at the same time allows for preserving the advantages of a minimal invasive approach[118]. Scant data is available so far regarding long-term outcomes, however the few series with adequate follow-up report laparoscopy pouch function results as good as the ones achieved with open surgery[21,119]. Laparoscopy has also been adopted with good results in the emergency setting[120,121], and similarly as for open surgery, a staged approach to a minimally invasive restorative procedure should be preferred which is as effective in significantly reducing the rate of postoperative pelvic sepsis[121-123]. Furthermore, when a staged procedure is planned, laparoscopy has been shown to decrease postoperative adhesion formation with less intraoperative adhesiolysis required during subsequent completion proctectomy and IPAA[124]. Similarly, a study by Indar and colleagues on 34 patients who underwent laparoscopic IPAA, where a laparoscopic exploration of the abdominal cavity was performed during the ileostomy closure, found that no patient had dense adhesion and only a minority of patients had filmy avascular adhesion to the abdominal wall (32%) and to the adnexa (29%), which represents a significant improvement compare to the rates reported for open surgery (as high as 90%)[125].

Despite the lack of strong evidence about the benefits attainable with laparoscopy in terms of short-term outcomes[21,126], it has been proven that patients treated laparoscopically are more satisfied with the cosmetic results and perceive a better body image-aspect anything but negligible in this usually young and socially active patient population-especially in the women’s subset, as confirmed by the results of a RCT with a median follow-up of 2.7 years[21,119]. More recently, the quest for further minimizing surgical trauma and extent of incisions, has led to the development of single incision laparoscopy (SIL), which has already been applied in the field of colorectal diseases with proven benefits in terms of short-term outcomes over standard laparoscopy[127-131]. To date only few cases of SIL for UC has been reported, but preliminary results show that particularly for the total abdominal colectomy, this “no scar” approach have the potential for improving not only the cosmesis, but also the postoperative course, with less pain and reduced need for narcotics, which may translate in shorter hospital stay and faster return to normal activities[132-135]. Considering the excellent outcome of restorative surgery, heightened by the potentials of minimal invasive techniques, surgery should not be considered the last resort when everything has failed, but rather a valid alternative to an expensive and risky medical therapy[136].

CONCLUSION

Medical therapy in UC is rapidly evolving and the introduction of modern biological drugs has led to substantial changes in the traditional principles of management. Infliximab, the first biological agent used as rescue therapy after failure of steroids in UC, appears to be effective in reducing the need for urgent colectomy, although its efficacy in the long-term is not proven. In addition, concerns have been raised regarding the economic burden related to this drugs and the risk for serious postoperative complications.

Surgery continues to play an important role in UC treatment and its evolution keeps pace with the advance in medical therapy and the risk associated with it. Restorative proctocolectomy with IPAA, staged procedures, and minimally invasive surgery are important treatment tools to limit postoperative morbidity and achieve excellent long-term outcomes in these patients.

In an attempt at avoiding surgery, aggressive medical therapy is not without complications. A complex decision making process in a multidisciplinary fashion should take into consideration the excellent results of modern surgical therapies to avoid unnecessary morbidity.

Footnotes

Peer reviewer: Keiji Hirata, MD, Surgery 1, University of Occupational and Environmental Health, 1-1 Iseigaoka, Yahatanishi-ku, Kitakyushu 807-8555, Japan

S- Editor Cheng JX L- Editor A E- Editor Li JY

References
1.  Cima RR, Pemberton JH. Medical and surgical management of chronic ulcerative colitis. Arch Surg. 2005;140:300-310.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 62]  [Cited by in F6Publishing: 68]  [Article Influence: 3.6]  [Reference Citation Analysis (0)]
2.  Rao SS, Holdsworth CD, Read NW. Symptoms and stool patterns in patients with ulcerative colitis. Gut. 1988;29:342-345.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in F6Publishing: 1]  [Reference Citation Analysis (0)]
3.  Langholz E, Munkholm P, Davidsen M, Binder V. Course of ulcerative colitis: analysis of changes in disease activity over years. Gastroenterology. 1994;107:3-11.  [PubMed]  [DOI]  [Cited in This Article: ]
4.  Abraham C, Cho JH. Inflammatory bowel disease. N Engl J Med. 2009;361:2066-2078.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 1967]  [Cited by in F6Publishing: 2046]  [Article Influence: 136.4]  [Reference Citation Analysis (5)]
5.  Hanauer SB. Medical therapy for ulcerative colitis 2004. Gastroenterology. 2004;126:1582-1592.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 126]  [Cited by in F6Publishing: 131]  [Article Influence: 6.6]  [Reference Citation Analysis (0)]
6.  Rogler G. Medical management of ulcerative colitis. Dig Dis. 2009;27:542-549.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 12]  [Cited by in F6Publishing: 13]  [Article Influence: 0.9]  [Reference Citation Analysis (0)]
7.  Cima RR. Timing and indications for colectomy in chronic ulcerative colitis: Surgical consideration. Dig Dis. 2010;28:501-507.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 36]  [Cited by in F6Publishing: 38]  [Article Influence: 2.7]  [Reference Citation Analysis (0)]
8.  Langholz E, Munkholm P, Davidsen M, Binder V. Colorectal cancer risk and mortality in patients with ulcerative colitis. Gastroenterology. 1992;103:1444-1451.  [PubMed]  [DOI]  [Cited in This Article: ]
9.  Kunitake H, Hodin R, Shellito PC, Sands BE, Korzenik J, Bordeianou L. Perioperative treatment with infliximab in patients with Crohn's disease and ulcerative colitis is not associated with an increased rate of postoperative complications. J Gastrointest Surg. 2008;12:1730-1736; discussion 1730-1736.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 171]  [Cited by in F6Publishing: 175]  [Article Influence: 10.9]  [Reference Citation Analysis (0)]
10.  Lawson MM, Thomas AG, Akobeng AK. Tumour necrosis factor alpha blocking agents for induction of remission in ulcerative colitis. Cochrane Database Syst Rev. 2006;CD005112.  [PubMed]  [DOI]  [Cited in This Article: ]
11.  Russo EA, Harris AW, Campbell S, Lindsay J, Hart A, Arebi N, Milestone A, Tsai HH, Walters J, Carpani M. Experience of maintenance infliximab therapy for refractory ulcerative colitis from six centres in England. Aliment Pharmacol Ther. 2009;29:308-314.  [PubMed]  [DOI]  [Cited in This Article: ]
12.  Schluender SJ, Ippoliti A, Dubinsky M, Vasiliauskas EA, Papadakis KA, Mei L, Targan SR, Fleshner PR. Does infliximab influence surgical morbidity of ileal pouch-anal anastomosis in patients with ulcerative colitis? Dis Colon Rectum. 2007;50:1747-1753.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 101]  [Cited by in F6Publishing: 101]  [Article Influence: 5.9]  [Reference Citation Analysis (0)]
13.  Selvasekar CR, Cima RR, Larson DW, Dozois EJ, Harrington JR, Harmsen WS, Loftus EV, Sandborn WJ, Wolff BG, Pemberton JH. Effect of infliximab on short-term complications in patients undergoing operation for chronic ulcerative colitis. J Am Coll Surg. 2007;204:956-962; discussion 962-963.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in F6Publishing: 1]  [Reference Citation Analysis (0)]
14.  Aberra FN, Lewis JD, Hass D, Rombeau JL, Osborne B, Lichtenstein GR. Corticosteroids and immunomodulators: postoperative infectious complication risk in inflammatory bowel disease patients. Gastroenterology. 2003;125:320-327.  [PubMed]  [DOI]  [Cited in This Article: ]
15.  Lake JP, Firoozmand E, Kang JC, Vassiliu P, Chan LS, Vukasin P, Kaiser AM, Beart RW. Effect of high-dose steroids on anastomotic complications after proctocolectomy with ileal pouch-anal anastomosis. J Gastrointest Surg. 2004;8:547-551.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 37]  [Cited by in F6Publishing: 37]  [Article Influence: 1.9]  [Reference Citation Analysis (0)]
16.  Alavi K, Sturrock PR, Sweeney WB, Maykel JA, Cervera-Servin JA, Tseng J, Cook EF. A simple risk score for predicting surgical site infections in inflammatory bowel disease. Dis Colon Rectum. 2010;53:1480-1486.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in F6Publishing: 1]  [Reference Citation Analysis (0)]
17.  Cohen JL, Strong SA, Hyman NH, Buie WD, Dunn GD, Ko CY, Fleshner PR, Stahl TJ, Kim DG, Bastawrous AL. Practice parameters for the surgical treatment of ulcerative colitis. Dis Colon Rectum. 2005;48:1997-2009.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 87]  [Cited by in F6Publishing: 91]  [Article Influence: 4.8]  [Reference Citation Analysis (0)]
18.  Becker JM. Surgical therapy for ulcerative colitis and Crohn's disease. Gastroenterol Clin North Am. 1999;28:371-390, viii-ix.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 93]  [Cited by in F6Publishing: 92]  [Article Influence: 3.7]  [Reference Citation Analysis (0)]
19.  Alves A, Panis Y, Bouhnik Y, Maylin V, Lavergne-Slove A, Valleur P. Subtotal colectomy for severe acute colitis: a 20-year experience of a tertiary care center with an aggressive and early surgical policy. J Am Coll Surg. 2003;197:379-385.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 96]  [Cited by in F6Publishing: 100]  [Article Influence: 4.8]  [Reference Citation Analysis (0)]
20.  Marcello PW, Milsom JW, Wong SK, Hammerhofer KA, Goormastic M, Church JM, Fazio VW. Laparoscopic restorative proctocolectomy: case-matched comparative study with open restorative proctocolectomy. Dis Colon Rectum. 2000;43:604-608.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 180]  [Cited by in F6Publishing: 191]  [Article Influence: 8.0]  [Reference Citation Analysis (0)]
21.  Dunker MS, Bemelman WA, Slors JF, van Duijvendijk P, Gouma DJ. Functional outcome, quality of life, body image, and cosmesis in patients after laparoscopic-assisted and conventional restorative proctocolectomy: a comparative study. Dis Colon Rectum. 2001;44:1800-1807.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 200]  [Cited by in F6Publishing: 216]  [Article Influence: 9.4]  [Reference Citation Analysis (0)]
22.  Tan JJ, Tjandra JJ. Laparoscopic surgery for ulcerative colitis - a meta-analysis. Colorectal Dis. 2006;8:626-636.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 54]  [Cited by in F6Publishing: 57]  [Article Influence: 3.2]  [Reference Citation Analysis (0)]
23.  Höie O, Wolters F, Riis L, Aamodt G, Solberg C, Bernklev T, Odes S, Mouzas IA, Beltrami M, Langholz E. Ulcerative colitis: patient characteristics may predict 10-yr disease recurrence in a European-wide population-based cohort. Am J Gastroenterol. 2007;102:1692-1701.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in F6Publishing: 1]  [Reference Citation Analysis (0)]
24.  Langholz E, Munkholm P, Nielsen OH, Kreiner S, Binder V. Incidence and prevalence of ulcerative colitis in Copenhagen county from 1962 to 1987. Scand J Gastroenterol. 1991;26:1247-1256.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 182]  [Cited by in F6Publishing: 188]  [Article Influence: 5.7]  [Reference Citation Analysis (0)]
25.  Baudet A, Rahmi G, Bretagne AL, Gloro R, Justum AM, Reimund JM. Severe ulcerative colitis: present medical treatment strategies. Expert Opin Pharmacother. 2008;9:447-457.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 6]  [Cited by in F6Publishing: 7]  [Article Influence: 0.4]  [Reference Citation Analysis (0)]
26.  Solberg IC, Lygren I, Jahnsen J, Aadland E, Høie O, Cvancarova M, Bernklev T, Henriksen M, Sauar J, Vatn MH. Clinical course during the first 10 years of ulcerative colitis: results from a population-based inception cohort (IBSEN Study). Scand J Gastroenterol. 2009;44:431-440.  [PubMed]  [DOI]  [Cited in This Article: ]
27.  Talley NJ, Abreu MT, Achkar JP, Bernstein CN, Dubinsky MC, Hanauer SB, Kane SV, Sandborn WJ, Ullman TA, Moayyedi P. An evidence-based systematic review on medical therapies for inflammatory bowel disease. Am J Gastroenterol. 2011;106 Suppl 1:S2-25; quiz S26.  [PubMed]  [DOI]  [Cited in This Article: ]
28.  Henriksen M, Jahnsen J, Lygren I, Sauar J, Kjellevold Ø, Schulz T, Vatn MH, Moum B. Ulcerative colitis and clinical course: results of a 5-year population-based follow-up study (the IBSEN study). Inflamm Bowel Dis. 2006;12:543-550.  [PubMed]  [DOI]  [Cited in This Article: ]
29.  Cottone M, Scimeca D, Mocciaro F, Civitavecchia G, Perricone G, Orlando A. Clinical course of ulcerative colitis. Dig Liver Dis. 2008;40 Suppl 2:S247-S252.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 26]  [Cited by in F6Publishing: 24]  [Article Influence: 1.5]  [Reference Citation Analysis (0)]
30.  Hendriksen C, Kreiner S, Binder V. Long term prognosis in ulcerative colitis--based on results from a regional patient group from the county of Copenhagen. Gut. 1985;26:158-163.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 210]  [Cited by in F6Publishing: 224]  [Article Influence: 5.7]  [Reference Citation Analysis (0)]
31.  Langholz E, Munkholm P, Davidsen M, Nielsen OH, Binder V. Changes in extent of ulcerative colitis: a study on the course and prognostic factors. Scand J Gastroenterol. 1996;31:260-266.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 169]  [Cited by in F6Publishing: 173]  [Article Influence: 6.2]  [Reference Citation Analysis (0)]
32.  Leijonmarck CE, Persson PG, Hellers G. Factors affecting colectomy rate in ulcerative colitis: an epidemiologic study. Gut. 1990;31:329-333.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 151]  [Cited by in F6Publishing: 155]  [Article Influence: 4.6]  [Reference Citation Analysis (0)]
33.  Beck DE, Gathright JB. Ulcerative colitis: surgical indications and alternatives. South Med J. 1994;87:773-779.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in F6Publishing: 1]  [Reference Citation Analysis (0)]
34.  Bojic D, Radojicic Z, Nedeljkovic-Protic M, Al-Ali M, Jewell DP, Travis SP. Long-term outcome after admission for acute severe ulcerative colitis in Oxford: the 1992-1993 cohort. Inflamm Bowel Dis. 2009;15:823-828.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 49]  [Cited by in F6Publishing: 48]  [Article Influence: 3.2]  [Reference Citation Analysis (0)]
35.  Moskovitz DN, Van Assche G, Maenhout B, Arts J, Ferrante M, Vermeire S, Rutgeerts P. Incidence of colectomy during long-term follow-up after cyclosporine-induced remission of severe ulcerative colitis. Clin Gastroenterol Hepatol. 2006;4:760-765.  [PubMed]  [DOI]  [Cited in This Article: ]
36.  Bianchi Porro G, Cassinotti A, Ferrara E, Maconi G, Ardizzone S. Review article: the management of steroid dependency in ulcerative colitis. Aliment Pharmacol Ther. 2007;26:779-794.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 43]  [Cited by in F6Publishing: 35]  [Article Influence: 2.1]  [Reference Citation Analysis (0)]
37.  Martin A, Dinca M, Leone L, Fries W, Angriman I, Tropea A, Naccarato R. Quality of life after proctocolectomy and ileo-anal anastomosis for severe ulcerative colitis. Am J Gastroenterol. 1998;93:166-169.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in F6Publishing: 1]  [Reference Citation Analysis (0)]
38.  Fazio VW, O'Riordain MG, Lavery IC, Church JM, Lau P, Strong SA, Hull T. Long-term functional outcome and quality of life after stapled restorative proctocolectomy. Ann Surg. 1999;230:575-584; discussion 584-586.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in F6Publishing: 1]  [Reference Citation Analysis (0)]
39.  Weinryb RM, Gustavsson JP, Liljeqvist L, Poppen B, Rössel RJ. A prospective study of the quality of life after pelvic pouch operation. J Am Coll Surg. 1995;180:589-595.  [PubMed]  [DOI]  [Cited in This Article: ]
40.  Ørding Olsen K, Juul S, Berndtsson I, Oresland T, Laurberg S. Ulcerative colitis: female fecundity before diagnosis, during disease, and after surgery compared with a population sample. Gastroenterology. 2002;122:15-19.  [PubMed]  [DOI]  [Cited in This Article: ]
41.  Hueting WE, Buskens E, van der Tweel I, Gooszen HG, van Laarhoven CJ. Results and complications after ileal pouch anal anastomosis: a meta-analysis of 43 observational studies comprising 9,317 patients. Dig Surg. 2005;22:69-79.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in F6Publishing: 1]  [Reference Citation Analysis (0)]
42.  Dhillon S, Loftus EV, Tremaine WJ, Jewell DA, Harmsen WS, Zinsmeister AR, Melton LJ, Pemberton H, Wolff BG, Dozois EJ. The natural history of surgery for ulcerative colitis in a population based cohort from Olmsted County, Minnesota. Am J Gastroenterol. 2005;100:A819.  [PubMed]  [DOI]  [Cited in This Article: ]
43.  Bach SP, Mortensen NJ. Ileal pouch surgery for ulcerative colitis. World J Gastroenterol. 2007;13:3288-3300.  [PubMed]  [DOI]  [Cited in This Article: ]
44.  Travis SP, Stange EF, Lemann M, Oresland T, Bemelman WA, Chowers Y, Colombel JF, D'Haens G, Ghosh S, Marteau P. European evidence-based Consensus on the management of ulcerative colitis: Current management. J Crohns Colitis. 2008;2:24-62.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 392]  [Cited by in F6Publishing: 402]  [Article Influence: 25.1]  [Reference Citation Analysis (0)]
45.  Järnerot G, Rolny P, Sandberg-Gertzén H. Intensive intravenous treatment of ulcerative colitis. Gastroenterology. 1985;89:1005-1013.  [PubMed]  [DOI]  [Cited in This Article: ]
46.  Caprilli R, Vernia P, Latella G, Torsoli A. Early recognition of toxic megacolon. J Clin Gastroenterol. 1987;9:160-164.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in F6Publishing: 1]  [Reference Citation Analysis (0)]
47.  Meyers S, Lerer PK, Feuer EJ, Johnson JW, Janowitz HD. Predicting the outcome of corticoid therapy for acute ulcerative colitis. Results of a prospective, randomized, double-blind clinical trial. J Clin Gastroenterol. 1987;9:50-54.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in F6Publishing: 2]  [Reference Citation Analysis (0)]
48.  Travis SP, Farrant JM, Ricketts C, Nolan DJ, Mortensen NM, Kettlewell MG, Jewell DP. Predicting outcome in severe ulcerative colitis. Gut. 1996;38:905-910.  [PubMed]  [DOI]  [Cited in This Article: ]
49.  Lindgren SC, Flood LM, Kilander AF, Löfberg R, Persson TB, Sjödahl RI. Early predictors of glucocorticosteroid treatment failure in severe and moderately severe attacks of ulcerative colitis. Eur J Gastroenterol Hepatol. 1998;10:831-835.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 186]  [Cited by in F6Publishing: 177]  [Article Influence: 6.8]  [Reference Citation Analysis (0)]
50.  Hyde GM, Jewell DP, Kettlewell MG, Mortensen NJ. Cyclosporin for severe ulcerative colitis does not increase the rate of perioperative complications. Dis Colon Rectum. 2001;44:1436-1440.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 95]  [Cited by in F6Publishing: 97]  [Article Influence: 4.2]  [Reference Citation Analysis (0)]
51.  Järnerot G, Hertervig E, Friis-Liby I, Blomquist L, Karlén P, Grännö C, Vilien M, Ström M, Danielsson A, Verbaan H. Infliximab as rescue therapy in severe to moderately severe ulcerative colitis: a randomized, placebo-controlled study. Gastroenterology. 2005;128:1805-1811.  [PubMed]  [DOI]  [Cited in This Article: ]
52.  Lichtiger S, Present DH, Kornbluth A, Gelernt I, Bauer J, Galler G, Michelassi F, Hanauer S. Cyclosporine in severe ulcerative colitis refractory to steroid therapy. N Engl J Med. 1994;330:1841-1845.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 1217]  [Cited by in F6Publishing: 1128]  [Article Influence: 37.6]  [Reference Citation Analysis (0)]
53.  Campbell S, Travis S, Jewell D. Ciclosporin use in acute ulcerative colitis: a long-term experience. Eur J Gastroenterol Hepatol. 2005;17:79-84.  [PubMed]  [DOI]  [Cited in This Article: ]
54.  Ford AC, Sandborn WJ, Khan KJ, Hanauer SB, Talley NJ, Moayyedi P. Efficacy of biological therapies in inflammatory bowel disease: systematic review and meta-analysis. Am J Gastroenterol. 2011;106:644-659, quiz 660.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in F6Publishing: 1]  [Reference Citation Analysis (0)]
55.  Sands BE, Tremaine WJ, Sandborn WJ, Rutgeerts PJ, Hanauer SB, Mayer L, Targan SR, Podolsky DK. Infliximab in the treatment of severe, steroid-refractory ulcerative colitis: a pilot study. Inflamm Bowel Dis. 2001;7:83-88.  [PubMed]  [DOI]  [Cited in This Article: ]
56.  Probert CS, Hearing SD, Schreiber S, Kühbacher T, Ghosh S, Arnott ID, Forbes A. Infliximab in moderately severe glucocorticoid resistant ulcerative colitis: a randomised controlled trial. Gut. 2003;52:998-1002.  [PubMed]  [DOI]  [Cited in This Article: ]
57.  Gustavsson A, Jarnerot G, Hertervig E. A 2-year followup of the Swedish-Danish Infliximab/Placebo trial in steroid resistant acute ulcerative colitis. Gastroenterology. 2007;132:A-983.  [PubMed]  [DOI]  [Cited in This Article: ]
58.  Ochsenkühn T, Sackmann M, Göke B. Infliximab for acute, not steroid-refractory ulcerative colitis: a randomized pilot study. Eur J Gastroenterol Hepatol. 2004;16:1167-1171.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 84]  [Cited by in F6Publishing: 81]  [Article Influence: 4.1]  [Reference Citation Analysis (0)]
59.  Rutgeerts P, Sandborn WJ, Feagan BG, Reinisch W, Olson A, Johanns J, Travers S, Rachmilewitz D, Hanauer SB, Lichtenstein GR. Infliximab for induction and maintenance therapy for ulcerative colitis. N Engl J Med. 2005;353:2462-2476.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 2744]  [Cited by in F6Publishing: 2712]  [Article Influence: 142.7]  [Reference Citation Analysis (2)]
60.  Sandborn WJ, Rutgeerts P, Feagan BG, Reinisch W, Olson A, Johanns J, Lu J, Horgan K, Rachmilewitz D, Hanauer SB. Colectomy rate comparison after treatment of ulcerative colitis with placebo or infliximab. Gastroenterology. 2009;137:1250-1260; quiz 1520.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 332]  [Cited by in F6Publishing: 360]  [Article Influence: 24.0]  [Reference Citation Analysis (0)]
61.  Colombel JF, Rutgeerts P, Reinisch W, Esser D, Wang Y, Lang Y, Marano CW, Strauss R, Oddens BJ, Feagan BG. Early mucosal healing with infliximab is associated with improved long-term clinical outcomes in ulcerative colitis. Gastroenterology. 2011;141:1194-1201.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 643]  [Cited by in F6Publishing: 666]  [Article Influence: 51.2]  [Reference Citation Analysis (0)]
62.  Lopez-Sanroman A, Bermejo F, Carrera E, Garcia-Plaza A. Efficacy and safety of thiopurinic immunomodulators (azathioprine and mercaptopurine) in steroid-dependent ulcerative colitis. Aliment Pharmacol Ther. 2004;20:161-166.  [PubMed]  [DOI]  [Cited in This Article: ]
63.  Timmer A, McDonald JW, Macdonald JK. Azathioprine and 6-mercaptopurine for maintenance of remission in ulcerative colitis. Cochrane Database Syst Rev. 2007;CD000478.  [PubMed]  [DOI]  [Cited in This Article: ]
64.  Ardizzone S, Maconi G, Russo A, Imbesi V, Colombo E, Bianchi Porro G. Randomised controlled trial of azathioprine and 5-aminosalicylic acid for treatment of steroid dependent ulcerative colitis. Gut. 2006;55:47-53.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 367]  [Cited by in F6Publishing: 349]  [Article Influence: 19.4]  [Reference Citation Analysis (0)]
65.  Hawthorne AB, Logan RF, Hawkey CJ, Foster PN, Axon AT, Swarbrick ET, Scott BB, Lennard-Jones JE. Randomised controlled trial of azathioprine withdrawal in ulcerative colitis. BMJ. 1992;305:20-22.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in F6Publishing: 1]  [Reference Citation Analysis (0)]
66.  Kozarek RA, Patterson DJ, Gelfand MD, Botoman VA, Ball TJ, Wilske KR. Methotrexate induces clinical and histologic remission in patients with refractory inflammatory bowel disease. Ann Intern Med. 1989;110:353-356.  [PubMed]  [DOI]  [Cited in This Article: ]
67.  Baron TH, Truss CD, Elson CO. Low-dose oral methotrexate in refractory inflammatory bowel disease. Dig Dis Sci. 1993;38:1851-1856.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in F6Publishing: 1]  [Reference Citation Analysis (0)]
68.  Cummings JR, Herrlinger KR, Travis SP, Gorard DA, McIntyre AS, Jewell DP. Oral methotrexate in ulcerative colitis. Aliment Pharmacol Ther. 2005;21:385-389.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in F6Publishing: 1]  [Reference Citation Analysis (0)]
69.  Oren R, Arber N, Odes S, Moshkowitz M, Keter D, Pomeranz I, Ron Y, Reisfeld I, Broide E, Lavy A. Methotrexate in chronic active ulcerative colitis: a double-blind, randomized, Israeli multicenter trial. Gastroenterology. 1996;110:1416-1421.  [PubMed]  [DOI]  [Cited in This Article: ]
70.  Armuzzi A, De Pascalis B, Lupascu A, Fedeli P, Leo D, Mentella MC, Vincenti F, Melina D, Gasbarrini G, Pola P. Infliximab in the treatment of steroid-dependent ulcerative colitis. Eur Rev Med Pharmacol Sci. 2004;8:231-233.  [PubMed]  [DOI]  [Cited in This Article: ]
71.  Jakobovits SL, Jewell DP, Travis SP. Infliximab for the treatment of ulcerative colitis: outcomes in Oxford from 2000 to 2006. Aliment Pharmacol Ther. 2007;25:1055-1060.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 87]  [Cited by in F6Publishing: 61]  [Article Influence: 3.6]  [Reference Citation Analysis (0)]
72.  Reinisch W, Sandborn WJ, Rutgeerts P, Feagan BG, Rachmilewitz D, Hanauer SB, Lichtenstein GR, de Villiers WJ, Blank M, Lang Y. Long-term infliximab maintenance therapy for ulcerative colitis: the ACT-1 and -2 extension studies. Inflamm Bowel Dis. 2012;18:201-211.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 147]  [Cited by in F6Publishing: 140]  [Article Influence: 11.7]  [Reference Citation Analysis (0)]
73.  Cohen RD, Thomas T. Economics of the use of biologics in the treatment of inflammatory bowel disease. Gastroenterol Clin North Am. 2006;35:867-882.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 24]  [Cited by in F6Publishing: 25]  [Article Influence: 1.4]  [Reference Citation Analysis (0)]
74.  Odes S. How expensive is inflammatory bowel disease? A critical analysis. World J Gastroenterol. 2008;14:6641-6647.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in CrossRef: 47]  [Cited by in F6Publishing: 50]  [Article Influence: 3.1]  [Reference Citation Analysis (0)]
75.  Zisman TL, Cohen RD. Pharmacoeconomics and quality of life of current and emerging biologic therapies for inflammatory bowel disease. Curr Treat Options Gastroenterol. 2007;10:185-194.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 12]  [Cited by in F6Publishing: 12]  [Article Influence: 0.7]  [Reference Citation Analysis (0)]
76.  Aratari A, Papi C, Clemente V, Moretti A, Luchetti R, Koch M, Capurso L, Caprilli R. Colectomy rate in acute severe ulcerative colitis in the infliximab era. Dig Liver Dis. 2008;40:821-826.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in F6Publishing: 1]  [Reference Citation Analysis (0)]
77.  Cannom RR, Kaiser AM, Ault GT, Beart RW, Etzioni DA. Inflammatory bowel disease in the United States from 1998 to 2005: has infliximab affected surgical rates? Am Surg. 2009;75:976-980.  [PubMed]  [DOI]  [Cited in This Article: ]
78.  Nguyen GC, Tuskey A, Dassopoulos T, Harris ML, Brant SR. Rising hospitalization rates for inflammatory bowel disease in the United States between 1998 and 2004. Inflamm Bowel Dis. 2007;13:1529-1535.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 116]  [Cited by in F6Publishing: 90]  [Article Influence: 5.3]  [Reference Citation Analysis (0)]
79.  Kappelman MD, Rifas-Shiman SL, Porter CQ, Ollendorf DA, Sandler RS, Galanko JA, Finkelstein JA. Direct health care costs of Crohn's disease and ulcerative colitis in US children and adults. Gastroenterology. 2008;135:1907-1913.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 469]  [Cited by in F6Publishing: 510]  [Article Influence: 31.9]  [Reference Citation Analysis (0)]
80.  Roberts SE, Williams JG, Yeates D, Goldacre MJ. Mortality in patients with and without colectomy admitted to hospital for ulcerative colitis and Crohn's disease: record linkage studies. BMJ. 2007;335:1033.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 120]  [Cited by in F6Publishing: 127]  [Article Influence: 7.5]  [Reference Citation Analysis (0)]
81.  Randall J, Singh B, Warren BF, Travis SP, Mortensen NJ, George BD. Delayed surgery for acute severe colitis is associated with increased risk of postoperative complications. Br J Surg. 2010;97:404-409.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 150]  [Cited by in F6Publishing: 150]  [Article Influence: 10.7]  [Reference Citation Analysis (0)]
82.  Heuschen UA, Hinz U, Allemeyer EH, Autschbach F, Stern J, Lucas M, Herfarth C, Heuschen G. Risk factors for ileoanal J pouch-related septic complications in ulcerative colitis and familial adenomatous polyposis. Ann Surg. 2002;235:207-216.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 177]  [Cited by in F6Publishing: 187]  [Article Influence: 8.5]  [Reference Citation Analysis (0)]
83.  Ferrante M, D'Hoore A, Vermeire S, Declerck S, Noman M, Van Assche G, Hoffman I, Rutgeerts P, Penninckx F. Corticosteroids but not infliximab increase short-term postoperative infectious complications in patients with ulcerative colitis. Inflamm Bowel Dis. 2009;15:1062-1070.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 193]  [Cited by in F6Publishing: 178]  [Article Influence: 11.9]  [Reference Citation Analysis (0)]
84.  Coquet-Reinier B, Berdah SV, Grimaud JC, Birnbaum D, Cougard PA, Barthet M, Desjeux A, Moutardier V, Brunet C. Preoperative infliximab treatment and postoperative complications after laparoscopic restorative proctocolectomy with ileal pouch-anal anastomosis: a case-matched study. Surg Endosc. 2010;24:1866-1871.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 54]  [Cited by in F6Publishing: 47]  [Article Influence: 3.4]  [Reference Citation Analysis (0)]
85.  Mor IJ, Vogel JD, da Luz Moreira A, Shen B, Hammel J, Remzi FH. Infliximab in ulcerative colitis is associated with an increased risk of postoperative complications after restorative proctocolectomy. Dis Colon Rectum. 2008;51:1202-1207; discussion 1202-1207.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 219]  [Cited by in F6Publishing: 218]  [Article Influence: 13.6]  [Reference Citation Analysis (0)]
86.  Gainsbury ML, Chu DI, Howard LA, Coukos JA, Farraye FA, Stucchi AF, Becker JM. Preoperative infliximab is not associated with an increased risk of short-term postoperative complications after restorative proctocolectomy and ileal pouch-anal anastomosis. J Gastrointest Surg. 2011;15:397-403.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 80]  [Cited by in F6Publishing: 80]  [Article Influence: 6.2]  [Reference Citation Analysis (0)]
87.  Yang Z, Wu Q, Wu K, Fan D. Meta-analysis: pre-operative infliximab treatment and short-term post-operative complications in patients with ulcerative colitis. Aliment Pharmacol Ther. 2010;31:486-492.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 109]  [Cited by in F6Publishing: 105]  [Article Influence: 7.5]  [Reference Citation Analysis (0)]
88.  Parks AG, Nicholls RJ. Proctocolectomy without ileostomy for ulcerative colitis. Br Med J. 1978;2:85-88.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 968]  [Cited by in F6Publishing: 886]  [Article Influence: 19.3]  [Reference Citation Analysis (0)]
89.  Jimmo B, Hyman NH. Is ileal pouch-anal anastomosis really the procedure of choice for patients with ulcerative colitis? Dis Colon Rectum. 1998;41:41-45.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 47]  [Cited by in F6Publishing: 46]  [Article Influence: 1.8]  [Reference Citation Analysis (0)]
90.  Umanskiy K, Fichera A. Health related quality of life in inflammatory bowel disease: the impact of surgical therapy. World J Gastroenterol. 2010;16:5024-5034.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in CrossRef: 27]  [Cited by in F6Publishing: 28]  [Article Influence: 2.0]  [Reference Citation Analysis (0)]
91.  McGuire BB, Brannigan AE, O'Connell PR. Ileal pouch-anal anastomosis. Br J Surg. 2007;94:812-823.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 81]  [Cited by in F6Publishing: 84]  [Article Influence: 4.9]  [Reference Citation Analysis (0)]
92.  Heuschen UA, Allemeyer EH, Hinz U, Lucas M, Herfarth C, Heuschen G. Outcome after septic complications in J pouch procedures. Br J Surg. 2002;89:194-200.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 94]  [Cited by in F6Publishing: 99]  [Article Influence: 4.5]  [Reference Citation Analysis (0)]
93.  Ziv Y, Church JM, Fazio VW, King TM, Lavery IC. Effect of systemic steroids on ileal pouch-anal anastomosis in patients with ulcerative colitis. Dis Colon Rectum. 1996;39:504-508.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 78]  [Cited by in F6Publishing: 80]  [Article Influence: 2.9]  [Reference Citation Analysis (0)]
94.  Hyman NH, Cataldo P, Osler T. Urgent subtotal colectomy for severe inflammatory bowel disease. Dis Colon Rectum. 2005;48:70-73.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 65]  [Cited by in F6Publishing: 66]  [Article Influence: 3.5]  [Reference Citation Analysis (0)]
95.  Williamson ME, Lewis WG, Sagar PM, Holdsworth PJ, Johnston D. One-stage restorative proctocolectomy without temporary ileostomy for ulcerative colitis: a note of caution. Dis Colon Rectum. 1997;40:1019-1022.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 81]  [Cited by in F6Publishing: 74]  [Article Influence: 2.7]  [Reference Citation Analysis (0)]
96.  Fazio VW, Tekkis PP, Remzi F, Lavery IC, Manilich E, Connor J, Preen M, Delaney CP. Quantification of risk for pouch failure after ileal pouch anal anastomosis surgery. Ann Surg. 2003;238:605-614; discussion 614-617.  [PubMed]  [DOI]  [Cited in This Article: ]
97.  Hancock L, Windsor AC, Mortensen NJ. Inflammatory bowel disease: the view of the surgeon. Colorectal Dis. 2006;8 Suppl 1:10-14.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 31]  [Cited by in F6Publishing: 34]  [Article Influence: 1.9]  [Reference Citation Analysis (0)]
98.  Tjandra JJ, Fazio VW, Milsom JW, Lavery IC, Oakley JR, Fabre JM. Omission of temporary diversion in restorative proctocolectomy--is it safe? Dis Colon Rectum. 1993;36:1007-1014.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 116]  [Cited by in F6Publishing: 98]  [Article Influence: 3.2]  [Reference Citation Analysis (0)]
99.  Wong KS, Remzi FH, Gorgun E, Arrigain S, Church JM, Preen M, Fazio VW. Loop ileostomy closure after restorative proctocolectomy: outcome in 1,504 patients. Dis Colon Rectum. 2005;48:243-250.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 168]  [Cited by in F6Publishing: 146]  [Article Influence: 7.7]  [Reference Citation Analysis (0)]
100.  Leowardi C, Hinz U, Tariverdian M, Kienle P, Herfarth C, Ulrich A, Kadmon M. Long-term outcome 10 years or more after restorative proctocolectomy and ileal pouch-anal anastomosis in patients with ulcerative colitis. Langenbecks Arch Surg. 2010;395:49-56.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 55]  [Cited by in F6Publishing: 54]  [Article Influence: 3.6]  [Reference Citation Analysis (0)]
101.  Ferrante M, Declerck S, De Hertogh G, Van Assche G, Geboes K, Rutgeerts P, Penninckx F, Vermeire S, D'Hoore A. Outcome after proctocolectomy with ileal pouch-anal anastomosis for ulcerative colitis. Inflamm Bowel Dis. 2008;14:20-28.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 134]  [Cited by in F6Publishing: 126]  [Article Influence: 7.9]  [Reference Citation Analysis (0)]
102.  Cornish JA, Tan E, Teare J, Teoh TG, Rai R, Darzi AW, Paraskevas P, Clark SK, Tekkis PP. The effect of restorative proctocolectomy on sexual function, urinary function, fertility, pregnancy and delivery: a systematic review. Dis Colon Rectum. 2007;50:1128-1138.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 158]  [Cited by in F6Publishing: 158]  [Article Influence: 9.3]  [Reference Citation Analysis (0)]
103.  Hueting WE, Gooszen HG, van Laarhoven CJ. Sexual function and continence after ileo pouch anal anastomosis: a comparison between a meta-analysis and a questionnaire survey. Int J Colorectal Dis. 2004;19:215-218.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 67]  [Cited by in F6Publishing: 63]  [Article Influence: 3.2]  [Reference Citation Analysis (0)]
104.  Berndtsson I, Lindholm E, Oresland T, Börjesson L. Long-term outcome after ileal pouch-anal anastomosis: function and health-related quality of life. Dis Colon Rectum. 2007;50:1545-1552.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 74]  [Cited by in F6Publishing: 74]  [Article Influence: 4.4]  [Reference Citation Analysis (0)]
105.  Michelassi F, Lee J, Rubin M, Fichera A, Kasza K, Karrison T, Hurst RD. Long-term functional results after ileal pouch anal restorative proctocolectomy for ulcerative colitis: a prospective observational study. Ann Surg. 2003;238:433-441; discussion 442-445.  [PubMed]  [DOI]  [Cited in This Article: ]
106.  Damgaard B, Wettergren A, Kirkegaard P. Social and sexual function following ileal pouch-anal anastomosis. Dis Colon Rectum. 1995;38:286-289.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in F6Publishing: 1]  [Reference Citation Analysis (0)]
107.  Davies RJ, O'Connor BI, Victor C, MacRae HM, Cohen Z, McLeod RS. A prospective evaluation of sexual function and quality of life after ileal pouch-anal anastomosis. Dis Colon Rectum. 2008;51:1032-1035.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 62]  [Cited by in F6Publishing: 63]  [Article Influence: 3.9]  [Reference Citation Analysis (0)]
108.  Heikens JT, de Vries J, van Laarhoven CJ. Quality of life, health-related quality of life and health status in patients having restorative proctocolectomy with ileal pouch-anal anastomosis for ulcerative colitis: a systematic review. Colorectal Dis. 2012;14:536-544.  [PubMed]  [DOI]  [Cited in This Article: ]
109.  Hahnloser D, Pemberton JH, Wolff BG, Larson DR, Crownhart BS, Dozois RR. Results at up to 20 years after ileal pouch-anal anastomosis for chronic ulcerative colitis. Br J Surg. 2007;94:333-340.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 305]  [Cited by in F6Publishing: 274]  [Article Influence: 16.1]  [Reference Citation Analysis (0)]
110.  Peters WR. Laparoscopic total proctocolectomy with creation of ileostomy for ulcerative colitis: report of two cases. J Laparoendosc Surg. 1992;2:175-178.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 72]  [Cited by in F6Publishing: 69]  [Article Influence: 2.2]  [Reference Citation Analysis (0)]
111.  Larson DW, Cima RR, Dozois EJ, Davies M, Piotrowicz K, Barnes SA, Wolff B, Pemberton J. Safety, feasibility, and short-term outcomes of laparoscopic ileal-pouch-anal anastomosis: a single institutional case-matched experience. Ann Surg. 2006;243:667-670; discussion 670-672.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in F6Publishing: 1]  [Reference Citation Analysis (0)]
112.  Wexner SD, Johansen OB, Nogueras JJ, Jagelman DG. Laparoscopic total abdominal colectomy. A prospective trial. Dis Colon Rectum. 1992;35:651-655.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 180]  [Cited by in F6Publishing: 180]  [Article Influence: 5.6]  [Reference Citation Analysis (0)]
113.  Hashimoto A, Funayama Y, Naito H, Fukushima K, Shibata C, Naitoh T, Shibuya K, Koyama K, Takahashi K, Ogawa H. Laparascope-assisted versus conventional restorative proctocolectomy with rectal mucosectomy. Surg Today. 2001;31:210-214.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in F6Publishing: 1]  [Reference Citation Analysis (0)]
114.  Schmitt SL, Cohen SM, Wexner SD, Nogueras JJ, Jagelman DG. Does laparoscopic-assisted ileal pouch anal anastomosis reduce the length of hospitalization? Int J Colorectal Dis. 1994;9:134-137.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 106]  [Cited by in F6Publishing: 109]  [Article Influence: 3.6]  [Reference Citation Analysis (0)]
115.  Fichera A, Silvestri MT, Hurst RD, Rubin MA, Michelassi F. Laparoscopic restorative proctocolectomy with ileal pouch anal anastomosis: a comparative observational study on long-term functional results. J Gastrointest Surg. 2009;13:526-532.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in F6Publishing: 1]  [Reference Citation Analysis (0)]
116.  Ahmed Ali U, Keus F, Heikens JT, Bemelman WA, Berdah SV, Gooszen HG, van Laarhoven CJ. Open versus laparoscopic (assisted) ileo pouch anal anastomosis for ulcerative colitis and familial adenomatous polyposis. Cochrane Database Syst Rev. 2009;CD006267.  [PubMed]  [DOI]  [Cited in This Article: ]
117.  Wu XJ, He XS, Zhou XY, Ke J, Lan P. The role of laparoscopic surgery for ulcerative colitis: systematic review with meta-analysis. Int J Colorectal Dis. 2010;25:949-957.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 47]  [Cited by in F6Publishing: 50]  [Article Influence: 3.6]  [Reference Citation Analysis (0)]
118.  Maartense S, Dunker MS, Slors JF, Cuesta MA, Gouma DJ, van Deventer SJ, van Bodegraven AA, Bemelman WA. Hand-assisted laparoscopic versus open restorative proctocolectomy with ileal pouch anal anastomosis: a randomized trial. Ann Surg. 2004;240:984-991; discussion 991-992.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 10]  [Cited by in F6Publishing: 6]  [Article Influence: 0.3]  [Reference Citation Analysis (0)]
119.  Polle SW, Dunker MS, Slors JF, Sprangers MA, Cuesta MA, Gouma DJ, Bemelman WA. Body image, cosmesis, quality of life, and functional outcome of hand-assisted laparoscopic versus open restorative proctocolectomy: long-term results of a randomized trial. Surg Endosc. 2007;21:1301-1307.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 113]  [Cited by in F6Publishing: 103]  [Article Influence: 6.1]  [Reference Citation Analysis (0)]
120.  Bell RL, Seymour NE. Laparoscopic treatment of fulminant ulcerative colitis. Surg Endosc. 2002;16:1778-1782.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 54]  [Cited by in F6Publishing: 60]  [Article Influence: 2.7]  [Reference Citation Analysis (0)]
121.  Marcello PW, Milsom JW, Wong SK, Brady K, Goormastic M, Fazio VW. Laparoscopic total colectomy for acute colitis: a case-control study. Dis Colon Rectum. 2001;44:1441-1445.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 113]  [Cited by in F6Publishing: 123]  [Article Influence: 5.3]  [Reference Citation Analysis (0)]
122.  Ky AJ, Sonoda T, Milsom JW. One-stage laparoscopic restorative proctocolectomy: an alternative to the conventional approach? Dis Colon Rectum. 2002;45:207-210; discussion 210-211.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 81]  [Cited by in F6Publishing: 92]  [Article Influence: 4.2]  [Reference Citation Analysis (0)]
123.  Pandey S, Luther G, Umanskiy K, Malhotra G, Rubin MA, Hurst RD, Fichera A. Minimally invasive pouch surgery for ulcerative colitis: is there a benefit in staging? Dis Colon Rectum. 2011;54:306-310.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in F6Publishing: 1]  [Reference Citation Analysis (0)]
124.  Gu J, Stocchi L, Geisler DP, Kiran RP. Staged restorative proctocolectomy: laparoscopic or open completion proctectomy after laparoscopic subtotal colectomy? Surg Endosc. 2011;25:3294-3299.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 19]  [Cited by in F6Publishing: 17]  [Article Influence: 1.3]  [Reference Citation Analysis (0)]
125.  Indar AA, Efron JE, Young-Fadok TM. Laparoscopic ileal pouch-anal anastomosis reduces abdominal and pelvic adhesions. Surg Endosc. 2009;23:174-177.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 89]  [Cited by in F6Publishing: 95]  [Article Influence: 5.9]  [Reference Citation Analysis (0)]
126.  Larson DW, Davies MM, Dozois EJ, Cima RR, Piotrowicz K, Anderson K, Barnes SA, Harmsen WS, Young-Fadok TM, Wolff BG. Sexual function, body image, and quality of life after laparoscopic and open ileal pouch-anal anastomosis. Dis Colon Rectum. 2008;51:392-396.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 87]  [Cited by in F6Publishing: 76]  [Article Influence: 4.8]  [Reference Citation Analysis (0)]
127.  Adair J, Gromski MA, Lim RB, Nagle D. Single-incision laparoscopic right colectomy: experience with 17 consecutive cases and comparison with multiport laparoscopic right colectomy. Dis Colon Rectum. 2010;53:1549-1554.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in F6Publishing: 1]  [Reference Citation Analysis (0)]
128.  Champagne BJ, Lee EC, Leblanc F, Stein SL, Delaney CP. Single-incision vs straight laparoscopic segmental colectomy: a case-controlled study. Dis Colon Rectum. 2011;54:183-186.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 102]  [Cited by in F6Publishing: 109]  [Article Influence: 8.4]  [Reference Citation Analysis (0)]
129.  Gandhi DP, Ragupathi M, Patel CB, Ramos-Valadez DI, Pickron TB, Haas EM. Single-incision versus hand-assisted laparoscopic colectomy: a case-matched series. J Gastrointest Surg. 2010;14:1875-1880.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 48]  [Cited by in F6Publishing: 47]  [Article Influence: 3.4]  [Reference Citation Analysis (0)]
130.  Ross H, Steele S, Whiteford M, Lee S, Albert M, Mutch M, Rivadeneira D, Marcello P. Early multi-institution experience with single-incision laparoscopic colectomy. Dis Colon Rectum. 2011;54:187-192.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in F6Publishing: 1]  [Reference Citation Analysis (0)]
131.  Chambers WM, Bicsak M, Lamparelli M, Dixon AR. Single-incision laparoscopic surgery (SILS) in complex colorectal surgery: a technique offering potential and not just cosmesis. Colorectal Dis. 2011;13:393-398.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 127]  [Cited by in F6Publishing: 114]  [Article Influence: 8.8]  [Reference Citation Analysis (0)]
132.  Leblanc F, Makhija R, Champagne BJ, Delaney CP. Single incision laparoscopic total colectomy and proctocolectomy for benign disease: initial experience. Colorectal Dis. 2011;13:1290-1293.  [PubMed]  [DOI]  [Cited in This Article: ]
133.  Cahill RA, Lindsey I, Jones O, Guy R, Mortensen N, Cunningham C. Single-port laparoscopic total colectomy for medically uncontrolled colitis. Dis Colon Rectum. 2010;53:1143-1147.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 49]  [Cited by in F6Publishing: 52]  [Article Influence: 3.7]  [Reference Citation Analysis (0)]
134.  Geisler DP, Condon ET, Remzi FH. Single incision laparoscopic total proctocolectomy with ileopouch anal anastomosis. Colorectal Dis. 2010;12:941-943.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 96]  [Cited by in F6Publishing: 104]  [Article Influence: 7.4]  [Reference Citation Analysis (0)]
135.  Fichera A, Zoccali M, Gullo R. Single incision ("scarless") laparoscopic total abdominal colectomy with end ileostomy for ulcerative colitis. J Gastrointest Surg. 2011;15:1247-1251.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 26]  [Cited by in F6Publishing: 32]  [Article Influence: 2.5]  [Reference Citation Analysis (0)]
136.  Tariverdian M, Leowardi C, Hinz U, Welsch T, Schmidt J, Kienle P. Quality of life after restorative proctocolectomy for ulcerative colitis: preoperative status and long-term results. Inflamm Bowel Dis. 2007;13:1228-1235.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 18]  [Cited by in F6Publishing: 18]  [Article Influence: 1.1]  [Reference Citation Analysis (0)]